Exotic Fruits Reference Guide 0128031530, 9780128031537
Exotic Fruits Reference Guide is the ultimate, most complete reference work on exotic fruits from around the world. The
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Exotic Fruits Reference Guide
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Exotic Fruits Reference Guide
Edited by Sueli Rodrigues Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Ebenezer de Oliveira Silva Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Edy Sousa de Brito Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1800, San Diego, CA 92101-4495, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright r 2018 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN: 978-0-12-803138-4 For Information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals
Publisher: Andre Gerhard Wolff Acquisition Editor: Nancy Maragioglio Editorial Project Manager: Mariana L. Kuhl Production Project Manager: Punithavathy Govindaradjane Cover Designer: Greg Harris Typeset by MPS Limited, Chennai, India
Contents List of Contributors Preface Acknowledgment
xv xix xxi
Ac¸aı´—Euterpe oleracea Maria do S.P. de Oliveira and Gustavo Schwartz Ac¸aı´ Origin, Ecology, Botany, and Socioeconomic Importance Harvest Season Estimated Annual Production and Harvest/Postharvest Conservation Fruit Physiology, Biochemistry, Chemical Composition, and Nutritional Value Sensory Characteristics Industrial Application or Potential Industrial Application References
3 4 4 4 5
Carlos F.H. Moura, Luciana de S. Oliveira, Kellina O. de Souza, Lorena G. da Franca, Laiza B. Ribeiro, Pahlevi A. de Souza and Maria R.A. de Miranda 7 8 8 8 10 13
Ambarella—Spondias cytherea Benoit B. Koubala, Germain Kansci and Marie-Christine Ralet Introduction Origin and Distribution Botanical Aspects Taxonomy and Colloquial Names Description Harvest and Production Fruit Physiology and Biochemistry Fruit Development and Maturation
18 18 20 20 20 21 21
Annatto/Urucum—Bixa orellana 1 3
Acerola—Malpighia emarginata
Origin and Botanical Classification Production Harvest Postharvest Postharvest Quality References
Fruit Ripening Chemical Composition and Nutritional Value of the Fruit Sensory Characteristics of the Fruit Conservation Application Acknowledgment References
15 15 16 16 16 17 17 17
Paulo C. Stringheta, Pollyanna I. Silva and Andre´ G.V. Costa Cultivation Origin and Botanical Aspects Harvest and Postharvest Conservation Harvest Postharvest Estimated Production and Trade of Annatto Chemical Composition of Annatto Biosynthesis of Annatto Compounds Biological Activities of Annatto Compounds Industrial Application and Potential Industrial Application References Further Reading
23 23 23 24 24 25 26 26 27 28 30
Arac¸a—Psidium cattleyanum Sabine Moˆnica M. de Almeida Lopes and Ebenezer de Oliveira Silva Origin and Botanical Aspects Production Fruit Physiology and Nutritional Value Postharvest Conservation Potential Industrial application References
31 31 32 34 34 35
Avocado fruit—Persea americana Elena Hurtado-Ferna´ndez, Alberto Ferna´ndez-Gutie´rrez and Alegrı´a Carrasco-Pancorbo Botany and Origin Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Sensory Characteristics
37 39 40 42 v
vi
Contents
Harvest Season Harvest and Postharvest Conservation Estimated Annual Production World Trade Industrial Applications and Other Potential Uses Acknowledgment References
42 43 44 44 44 46 46
Bacuri—Platonia insignis Angelo P. Jacomino, Patricia M. Pinto and Camilla Z. Gallon Cultivar Origin and Botanical Aspects Production Harvest and Postharvest Technology Chemical Composition and Nutritional Value Potential Industry Application Concluding Remarks References
49 49 50 50 50 51 51
Origin and Botanical Aspects Harvest and Potential of Industrialization Cocoa Beans Processing Chemical Composition and Nutritional Value References
69 72 72 72 75
Eli R.B. de Souza, Yanuzi M.V. Camilo and Rosaˆngela Vera Origin, Culture, and Botanical Aspects Harvest Season and Estimated Annual Production Physiology and Biochemistry of Fruits Harvest, Postharvest, and Potential Industrial Application References
77 78 79 80 82
Caju—Anacardium occidentale
Diane Ragone 53 53 54 55 55 55 57 57 58 59 59
Buriti fruit—Mauritia flexuosa
Edy Sousa de Brito, Ebenezer de Oliveira Silva and Sueli Rodrigues Botanical and Agronomical Aspects Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolics and Antioxidant Compounds Among Others Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application References
85 85
86 87 88 88
Cambuci—Campomanesia phaea (O. Berg.) Landrum
Hector H.F. Koolen, Felipe M.A. da Silva, Vitor S.V. da Silva, Weider H.P. Paz and Giovana A. Bataglion Origin and Botany Origin and Considerations Botanical Aspects Harvest Season and Annual Production Fruit Physiology and Biochemistry Buriti Fruit Morphology Buriti Fruit Nutrient Content Buriti Fruit Metabolites Biological Benefits Sensory Characteristics and Food Application Harvest, Postharvest Conservation and Industrial Applications Acknowledgment References
Pahlevi A. de Souza, Lunian F. Moreira, Dio´genes H.A. Sarmento and Franciscleudo B. da Costa
Cagaita—Eugenia dysenterica
Breadfruit—Artocarpus altilis (Parkinson) Fosberg Introduction Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgments References
Cacao—Theobroma cacao
61 61 61 62 62 62 63 64 65 66 66 66 66
Tatiane de O. Tokairin, Horst Bremer Neto and Angelo P. Jacomino Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Physiology and Biochemistry of Cambuci Fruit Chemical Composition and Nutritional Value Including Vitamins, Minerals, Phenolics and Antioxidant Compounds Sensory Attributes Harvest and Postharvest Conservation Perspectives and Industrial Applications Acknowledgments References
91 92 92 92
92 93 93 94 94 94
Contents
Camu-camu—Myrciaria dubia (Kunth) McVaugh Juan C. Castro, J. Dylan Maddox and Sixto A. Ima´n Cultivar Origin and Botanical Aspects Harvest Season and Estimated Annual Production Fruit Physiology and Biochemistry Chemical and Nutritional Compositions Health-Promoting Phytochemicals Sensory Characteristics Harvest and Postharvest Conservation Potential Industrial Application Acknowledgments References
97 98 98 99 99 102 102 103 103 103
Canistel—Pouteria campechiana (Kunth) Baehni Fadzilah Awang-Kanak and Mohd Fadzelly Abu Bakar Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Values Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgment References
107 108 108 108 109 109 110 110 111 111
Anticancer Activity Antimalarial Activity Lectin and Cell Adhesion Activity Cytotoxicity Potential and Traditional Medicinal Uses References
vii
124 124 124 125 125 126
Chilean Guava—Myrtus ugni Marcia A.A. Lorca The Species Ethnic Uses Socioeconomic Importance Phytochemistry and Biological Activity Our Experience Murtilla Fruits Murtilla Leaves In Vitro Determination of the Antioxidant Capacity of Extracts and Phenolic Compounds From Ugni molinae Turcz. Leaves Antioxidant Activity of Ugni molinae Turcz. (“Murtilla”) Infuses Consumption of Ugni molinae (Turcz.) Tea Elicits Increased Plasma Antioxidant Potential in Humans References Further Reading
129 130 130 132 133 133 134
135 135
135 138 139
Ciruela/Mexican Plum—Spondias purpurea L. Georgina Vargas-Simo´n
Caqui—Diospyros kaki Ricardo Alfredo Kluge and Magda Andre´ia Tessmer Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value, Including Vitamins, Mineral, Phenolics, and Antioxidant Compounds Sensory Features Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgment References
113 114 114 115
116 116 117 117 117 117
Cultivar Origin and Ethnobotanical Aspects Botanical Description Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolic, Antioxidant Compounds, and Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Propagation Acknowledgment References Further Reading
Cempedak—Artocarpus champeden
Cocona—Solanum sessiliflorum
Moˆnica M. de Almeida Lopes, Kellina O. de Souza and Ebenezer de Oliveira Silva
Pedro Jime´nez
Origin and Botanical Aspects Nutritive and Medicinal Properties
121 123
Introduction Origin, Distribution, and Morphology Fruit Composition
141 142 143 144 144
145 145 148 149 149 149 152
153 153 155
viii
Contents
Agronomical Aspects Pests and Diseases Uses and Perspectives Conclusions References
156 157 157 158 158
Cupuassu—Theobroma grandiflorum Ana L.F. Pereira, Virgı´nia K.G. Abreu and Sueli Rodrigues Introduction Cultivar Origin, Botanical Aspects and Harvest Season Chemical Composition and Nutritional Value Harvest and Postharvest Conservation and Potential Industrial Application Final Remarks References
159 159 160 161 162 162
Umesh B. Jagtap and Vishwas A. Bapat 163 163 163 164 164 164 164 165 165 166 166 166 166 166
Durian—Durio zibethinus Saichol Ketsa Introduction Cultivar Origin and Botanical Aspects Estimated Annual Production Fruit Physiology and Biochemistry Respiration Ethylene Production Softening Color Development Weight Loss Dehiscence Chemical Composition and Nutritional Value Vitamins and Minerals Antioxidants Fatty Acids Carbohydrates Carotenoids
174 175 175 175 175 176 176 176 176 176 177 177 177 177 180
Elderberry—Sambucus nigra L. Sueli Rodrigues, Edy Sousa de Brito and Ebenezer de Oliveira Silva
Custard apple—Annona squamosa L. Introduction Origin and Distribution Botanical Description Total Production and Market Uses Dietary Uses Use in Traditional Medicine Phytochemistry Fruits Seeds Harvest and Postharvest Conservation Potential Industrial Application Acknowledgment References
Sensory Characteristics Harvest and Postharvest Conservation Harvest Season Harvesting Ripening Surface Coating 1-MCP Storage Industrial Application or Potential Industrial Application Fresh Fruit Durian Products Durian Husk Concluding Remarks References Further Reading
169 169 170 170 170 170 171 171 172 172 173 173 173 174 174 174
Cultivar Origin and Botanical Aspects Postharvest Estimated Production Biochemical and Physiology Chemical Composition and Nutritional Value Industrialization References
181 182 182 183 183 184 185
Figo da india—Opuntia spp. Jose´ A´. Guerrero-Beltra´n and Carlos E. Ochoa-Velasco Fruit Origin and Botanical Aspects Origin Taxonomy Fruit Characteristics Cultivation and Harvest Physiology and Biochemistry Physical Changes Respiration Characteristics Chemical Composition and Nutritional Value Composition Nutritive Characteristics Minerals Amino Acids Vitamins Phenolic Compounds and Antioxidants Pigments Volatile Compounds and Sensory Characteristics Harvest and Postharvest Conservation Harvest Postharvest Conservation Potential Industrialization Juice and Nectar Jams, Jellies, and Candies
187 187 187 188 190 190 190 191 191 191 191 192 192 192 193 194 194 195 195 196 197 197 197
Contents
Fudge, Cheese or “ate” Dehydrated Products Alcoholic Drink “colonche” Minimal Processing Pigments Final Remarks References
198 198 198 198 199 199 199
Finger lime/The Australian Caviar—Citrus australasica Estelle Delort and Yong-Ming Yuan Botanical Classification Physiology and Harvest Season Sensory Characteristics, Chemical Composition, and Nutritional Value Sensory Characteristics and Volatile Composition Nutritional Value: Vitamins, Mineral, Phenolics, and Antioxidant Compounds Production and Industrial Applications of Commercialized Varieties References
204 204 206 206 206 208 209
Gooseberry—Ribes uva-crispa, sin. R. grossularia L
Andre´ Luiz Atroch and Firmino J. do Nascimento Filho Introduction Cultivar Origin and Botanical Aspects Flowering, Pollination, and Harvest Season Estimated Annual Production The Guarana and Polyploidy Genetic Resources Genetic Variability Brief History of Guarana Genetic Improvement Objectives of Guarana Breeding Genetic Improvement Methods Mass Selection Plant Selection With Progeny Testing Clonal Selection Recurrent Intraspecific Selection Transcriptome of Fruit With Seeds Future Prospects References Further Reading
225 225 227 228 229 229 230 233 233 233 233 234 234 234 235 235 235 236
Luiz C.C. Saloma˜o, Dalmo L. de Siqueira, Ce´sar F. Aquino and Leila C.R. de Lins 211 212 213 214
215 215 215 217 217 218
Grumixama—Eugenia brasiliensis Lam Luciane de L. Teixeira, Neuza M.A. Hassimotto and Franco M. Lajolo Introduction Plant Chemical and Nutritional Composition Phytochemical Profile Harvest Season and Production: Purple Grumixama Potential Industrial Application Acknowledgment References Further Reading
Guarana—Paullinia cupana Kunth var. sorbilis (Mart.) Ducke
Jabuticaba—Myrciaria spp.
Stanislaw Pluta Cultivar Origin and Botanical Aspects Harvest Season Fruit Physiology and Biochemistry Estimated Annual Production Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolics, and Antioxidant Compounds Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Market Potential References
ix
219 219 219 220 222 223 223 223 224
Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Harvest and Postharvest Conservation Industrial Application References
237 239 239 239 240 241 242 242
Jambo—Syzygium malaccense Fabiano A.N. Fernandes and Sueli Rodrigues Introduction Botanical Aspects Harvest Season Harvest and Postharvest Conservation Chemical Composition and Nutritional Value Sensory Characteristics Industrial Application References
245 245 245 246 247 248 248 248
Jambolan—Syzygium jambolanum Luiz B. de Sousa Sabino, Edy Sousa de Brito and Ivanildo J. da Silva Ju´nior Cultivar Origin and Botanical Aspects Harvest Season Fruit Physiology and Biochemistry
251 251 251
x
Contents
Chemical Composition and Nutritional Value Anthocyanins Biological Properties of Jambolan Sensory Characteristics Harvest and Postharvest Conservation Industrial Application and Potential Industrial Application References Further Reading
252 252 253 254 254 254 255 256
Jatoba—Hymenaea courbaril Gustavo Schwartz Species Origin, Ecology, Botany, and Socioeconomic Importance Harvest Season Estimated Annual Production and Harvest/Postharvest Conservation Fruit Physiology, Biochemistry, Chemical Composition, and Nutritional Value Sensory Characteristics Industrial Application or Potential Industrial Application References
257 259 259
260 260 260 261
Jujuba—Ziziphus jujuba Xinwen Jin Cultivar Origin and Botanical Aspects Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Chemical Composition Nutritional Values Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Red Date (Dry Date) Candied Jujube (Honey Jujube) Spirited Jujube (“Drunk Jujube”) Smoked Jujube Roasted Jujube Jujube Jam Jujube Paste/Filling Reaching Additional Consumers Acknowledgments References
263 265 265 265 265 266 266 267 267 267 267 267 267 268 268 268 268 268
Kumquat—Fortunella japonica Amedeo Palma and Salvatore D’Aquino Classification Origin and Distribution Botany, Morphology, and Anatomy Postharvest Physiology and Storage
271 271 271 272
Fruit Compositions, Nutritional, and Nutraceuticals Properties Fresh and Processed Products References
274 276 276
Langsat—Lansium domesticum Chairat Techavuthiporn Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology Chemical Compositions and Nutritional Values Sensory Characteristics Harvest and Postharvest Conservation Potential Industrial Application References Further Reading
279 280 280 280 280 281 282 282 283 283
Loquat/Nispero—Eriobotrya japonica Lindl. Moˆnica M. de Almeida Lopes, Alex Guimara˜es Sanches, Kellina O. de Souza and Ebenezer de Oliveira Silva Origin and Botanical Aspects Production Postharvest and Nutritional Value Postharvest Conservation Potential Industrial and Medicinal Uses References Further Reading
285 285 286 288 289 290 292
Maboque/Monkey Orange—Strychnos spinosa Sueli Rodrigues, Edy Sousa de Brito and Ebenezer de Oliveira Silva Botanical Origin Postharvest and Physiology Sensory and Physicochemical Characterization Industrialization and Uses References
293 293 294 295 296
Macauba Palm—Acrocomia aculeata Jose´ M.C. Costa, Dalany M. Oliveira and Luis E.C. Costa Introduction Botanic and Production Aspects of Macau´ba Palm Drying Processes Drying Adjuvants Fruit Drying Macau´ba Palm Fruit Components
297 298 298 299 300 300
Contents
Whole Fruit Pulp With and Without Maltodextrin Addition Dried Macau´ba Pulp Powder The Influence of Drying Processes on the Chemical Composition of Macau´ba Palm Fruit Bioactive Compounds References Further Reading
300 301
301 302 304
Narendra Narain, Fernanda R.M. Franc¸a and Maria T.S.L. Neta
Pitaya—Hylocereus undatus (Haw)
305 305 305 306 307 307 308 309 309 311 316 316 318
Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value: Vitamins, Mineral, Phenolics, and Antioxidant Compounds Sensory Characteristics Harvest and Postharvest Conservation Packing Systems Alternative Treatments Pests and Diseases Quarantine Treatments Industrial Application or Potential Industrial Application References
Noni—Morinda citrifolia L.
Pitomba—Talisia esculenta
Moˆnica M. de Almeida Lopes, Alex Guimara˜es Sanches, Joa˜o A. de Sousa and Ebenezer de Oliveira Silva
Sueli Rodrigues, Edy Sousa de Brito and Ebenezer de Oliveira Silva
Origin and Botanical Aspects Cultivation Practices and Harvest Postharvest and Nutritional Value Industrial Uses References
319 319 322 323 324
Pidada—Sonneratia caseolaris Azlen Che Rahim and Mohd Fadzelly Abu Bakar Cultivar Origin and Botanical Aspects Harvest Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Antioxidant Properties Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Application Acknowledgment References
Botanical Aspects and Harvest Season Estimated Annual Production Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolics, and Antioxidant Compounds Industrial Application or Potential Industrial Application References
339 340 340 341
342 343 343 344 344 345 345 345 346
351 351
351 353 353
Pomegranate/Roma—Punica granatum 327 327 328 328 329 329 330 330 331 331
Pitanga—Eugenia uniflora L. Rodrigo C. Franzon, Silvia Carpenedo, Maximiliano D. Vin˜oly and Maria do C.B. Raseira Cultivar Origin and Botanical Aspects
334 335 336 337 337 337
Edmundo M. Mercado-Silva
Mangaba—Hancornia speciosa
Introduction Origin and Production Botanical Aspects Cultivation and Harvest Physiology and Biochemistry Fruit Development Chemical Composition and Nutrition Vitamin C Phenolic Compounds Volatile Constituents Final Considerations References Further Reading
Harvest Season Chemical Composition and Nutritional Value Sensory Characteristics Harvest and Postharvest Conservation Industrial Potential References
xi
333
Mustafa Erkan and Adem Dogan Cultivars, Origin, and Botanical Aspects Harvest Seasons Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Harvest and Postharvest Conservation Controlled Atmosphere/Modified Atmosphere Storage Problems Under Suboptimal Conditions Industrial Application Minimally Processed or Ready-to-Eat Arils Jelly, Beverages, and Other Usage References Further Reading
355 357 357 358 358 358 359 359 360 360 360 360 361
xii
Contents
Quince—Cydonia oblonga Moˆnica M. de Almeida Lopes, Alex Guimara˜es Sanches, Kellina O. de Souza and Ebenezer de Oliveira Silva Origin and Botanical Aspects Production Postharvest Physiology and Nutritional Value Postharvest Conservation Industrial Application References Further Reading
363 363 364 366 366 366 368
Rambuta˜n—Nephelium lappaceum 369 369 369 370 371 371 371 371 371 371 371 372 372 372 373 373 373 374 374 375
Safou—Dacryodes edulis Sueli Rodrigues, Edy Sousa de Brito and Ebenezer de Oliveira Silva Cultivar Origin and Botanic Aspects Chemical Composition and Nutritional Value Sensory Aspects Harvest Season, Postharvest Conservation, Physiology, and Biochemistry Industrial Application or Potential Industrial Application References
377 377 378 380 380 381
Salak—Salacca zalacca
Shuaibu Babaji Sanusi and Mohd Fadzelly Abu Bakar Introduction Cultivar Origin and Distribution Taxonomy and Botanical Description Harvesting Season Estimated Annual Production Physiology and Biochemistry Sensory Characteristics of Soursop Fruit Harvest and Postharvest Conservation Industrial Application Acknowledgments References
391 391 391 392 392 393 394 394 395 395 395
Sugar Apple—Annona squamosa Linn. Muhammad Murtala Mainasara, Mohd Fadzelly Abu Bakar, Maryati Mohamed, Alona C. Linatoc and Fatimah Sabran Annona squamosa International Common Names Cultivar Origin Botanical Aspects Description Harvest Season Estimated Annual Production Plant Chemicals Fruit Composition Sensory Characteristics Harvest and Postharvest Conservation Industrial Application Economic Value References Further Reading
397 397 397 398 398 400 400 400 400 401 401 402 402 402 402
Tamarindo—Tamarindus indica
Nur Amalina Ismail and Mohd Fadzelly Abu Bakar Introduction Cultivar Origin and Botanical Description Morphology and Physiology
385 385 385 385 385 387 387 388 388 388 388 388 389 389
Soursop—Annona muricata
Wen Li, Jiaoke Zeng and Yuanzhi Shao Origin and Botanical Aspects Origin Morphological Characteristics Cultivars and Harvest Season Cultivation Propagation Growing Behavior and Management Sensory Characteristics Chemical Composition and Nutritional Value Nutritional Component Antioxidant Compounds Polyamine Harvest and Postharvest Conservation Harvest and Postharvest Physiology Postharvest Conservation Industrial Applications Peel Application Seed Application References Further Reading
Harvest Season Estimated Annual Production Chemical Composition and Nutritional Value Nutritional Composition Phytochemical Content Antioxidant Activity Immunostimulatory Activity Antihyperuricemic Activity Antiproliferative Activity Sensory and Physicochemical Characteristics Conservation Current and Potential Industrial Application Acknowledgment References
383 383 384
Md.Salim Azad Introduction Taxonomy
403 403
Contents
Distribution and Habitat General Description Food Value Chemical Composition Harvesting and Storage Cultivars Postharvest Uses Household Uses Medicinal Uses Industrial Uses Other Uses Propagation and Conservation Acknowledgment References Further Reading
404 404 406 406 406 407 407 408 408 408 409 409 410 410 412
Tarap—Artocarpus odoratissimus Fazleen Izzany Abu Bakar and Mohd Fadzelly Abu Bakar Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Including Vitamins, Mineral, Phenolics and Antioxidant Compounds Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgment References
413 414 414 415
415 417 417 418 418 418
The Tucuma˜ of Amazonas— Astrocaryum aculeatum
419 419 419 420 422 422 424
Umbu—Spondias tuberosa Maria Auxiliadora C. de Lima, Silvanda de M. Silva and Viseldo R. de Oliveira Introduction Origin and Botanical Aspects Genetic Variability Harvest Season Estimated Annual Production
427 427 428 429 429
429 429 431 431 431 432 432
Uvaia—Eugenia pyriformis Cambess Angelo P. Jacomino, Aline P.G. da Silva, Thais P. de Freitas and Veroˆnica S. de Paula Morais Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Including Vitamins, Minerals, Phenolics, and Antioxidant Compounds Sensory Characteristics Harvest and Postharvest Conservation Harvest Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgments References Further Reading
435 435 436 436
436 436 436 436 437 437 437 438 438
Wampee—Clausena lansium Sueli Rodrigues, Edy Sousa de Brito and Ebenezer de Oliveira Silva Cultivar Origin and Botanical Aspects Harvest Season Composition and Uses References
Roberto C.V. Santos, Michele R. Sagrillo, Euler E. Ribeiro and Ivana B.M. Cruz Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Uses and Applications Recent In Vitro Studies References
Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Final Remarks References
xiii
439 439 439 441
Wood Apple—Limonia acidissima Sueli Rodrigues, Edy Sousa de Brito and Ebenezer de Oliveira Silva Cultivar Origin and Botanical Aspects Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Including Vitamins, Mineral, Phenolics and Antioxidant Compounds Harvest and Postharvest Conservation Potential Industrial Application Medicinal Use Food Uses References Author Index Subject Index
443 443
444 444 444 444 446 446 447 459
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List of Contributors Virgı´nia K.G. Abreu, Federal University of Maranha˜o, Imperatriz, MA, Brazil Fazleen Izzany Abu Bakar, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Lorena G. da Franca, Federal Institute of Education, Science and Technology of Ceara´, Limoeiro do Norte, Brazil
Mohd Fadzelly Abu Bakar, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Aline P.G. da Silva, University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil
Ce´sar F. Aquino, Federal University of Vic¸osa, Vic¸osa, Minas Gerais, Brazil
Felipe M.A. da Silva, Federal University of Amazonas, Manaus, Brazil
Andre´ Luiz Atroch, Embrapa Manaus, Brazil
Ivanildo J. da Silva Ju´nior, Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Western
Amazon,
Fadzilah Awang-Kanak, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia; Universiti Malaysia Sabah, Sabah, Malaysia
Vitor S.V. da Silva, Amazonas Manaus, Brazil
State
University,
Md. Salim Azad, Khulna University, Khulna, Bangladesh
Moˆnica M. de Almeida Lopes, Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Vishwas A. Bapat, Shivaji Maharashtra, India
Kolhapur,
Edy Sousa de Brito, Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Giovana A. Bataglion, Federal University of Amazonas, Manaus, Brazil
Thais P. de Freitas, University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil
University,
Yanuzi M.V. Camilo, Federal University of Goia´s, Goiaˆnia, Brazil Silvia Carpenedo, Embrapa Temperate Agriculture, Pelotas, Rio Grande do Sul, Brazil Alegrı´a Carrasco-Pancorbo, University of Granada, Granada, Spain Juan C. Castro, National University of the Peruvian Amazon, Iquitos, Peru Andre´ G.V. Costa, Federal University of Espı´rito Santo, Alegre, Espı´rito Santo, Brazil Jose´ M.C. Costa, Federal University of Ceara´, Fortaleza, Ceara´, Brazil Luis E.C. Costa, Federal University of Ceara´, Fortaleza, Ceara´, Brazil Ivana B.M. Cruz, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil Salvatore D’Aquino, Institute of Sciences of Food Production, National Research Council, Sassari, Italy Franciscleudo B. da Costa, UFCG/CCTA, Pombal, Brazil
Maria Auxiliadora C. de Lima, Embrapa Semia´rido, Petrolina, Pernambuco, Brazil Leila C.R. de Lins, Federal University of Vic¸osa, Vic¸osa, Minas Gerais, Brazil Maria R.A. de Miranda, Federal University of Ceara´, Fortaleza, Ceara´, Brazil Maria do S.P. de Oliveira, Embrapa Eastern Amazon, Bele´m, Para, Brazil Viseldo R. de Oliveira, Embrapa Semia´rido, Petrolina, Pernambuco, Brazil Ebenezer de Oliveira Silva, Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil Veroˆnica S. de Paula Morais, Federal Institute of Education, Science and Technology of Southern Minas Gerais, IFSULDEMINAS, Inconfidentes, Minas Gerais, Brazil Dalmo L. de Siqueira, Federal University of Vic¸osa, Vic¸osa, Minas Gerais, Brazil
xv
xvi
List of Contributors
Joa˜o A. de Sousa, Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Germain Kansci, University of Yaounde, Yaounde, Cameroon
Luiz B. de Sousa Sabino, Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Saichol Ketsa, Kasetsart University, Bangkok, Thailand; The Royal Society of Thailand, Bangkok, Thailand
Eli R.B. de Souza, Federal University of Goia´s, Goiaˆnia, Brazil
Ricardo Alfredo Kluge, University of Sa˜o Paulo/ ESALQ, Piracicaba, Sa˜o Paulo, Brazil
Kellina O. de Souza, Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Hector H.F. Koolen, Amazonas Manaus, Brazil
Pahlevi A. de Souza, Federal Institute of Education, Science and Technology of Ceara´, Limoeiro do Norte, Brazil
Benoit B. Koubala, University of Maroua, Maroua, Cameroon
State
University,
Estelle Delort, Firmenich SA, Geneva, Switzerland
Franco M. Lajolo, University of Sa˜o Paulo, Sa˜o Paulo, Brazil
Firmino J. do Nascimento Filho, Embrapa Western Amazon, Manaus, Brazil
Wen Li, Hainan University, Hai Kou, People’s Republic of China
Adem Dogan, Akdeniz University, Antalya, Turkey
Alona C. Linatoc, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia Marcia A.A. Lorca, University of Concepcio´n, Concepcio´n, Chile
Mustafa Erkan, Akdeniz University, Antalya, Turkey Fabiano A.N. Fernandes, Federal University of Ceara´, Fortaleza, Ceara´, Brazil Alberto Ferna´ndez-Gutie´rrez, University of Granada, Granada, Spain Fernanda R.M. Franc¸a, Federal University of Sergipe, Sa˜o Cristo´va˜o, Sergipe, Brazil Rodrigo C. Franzon, Embrapa Temperate Agriculture, Pelotas, Rio Grande do Sul, Brazil Camilla Z. Gallon, University of Espirito Santo, Vito´ria, Brazil ´ . Guerrero-Beltra´n, Universidad de las Ame´ricas Jose´ A Puebla, Puebla, Mexico Neuza M.A. Hassimotto, University of Sa˜o Paulo, Sa˜o Paulo, Brazil Elena Hurtado-Ferna´ndez, University Granada, Spain Sixto A. Ima´n, National Innovation, Iquitos, Peru
Institute
of
J. Dylan Maddox, The Field Museum of Natural History, Chicago, IL, United States; American Public University System, Charles Town, WV, United States Muhammad Murtala Mainasara, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia Edmundo M. Mercado-Silva, Autonomous University of Queretaro, Santiago de Quere´taro, Mexico Maryati Mohamed, Universiti Tun Malaysia (UTHM), Johor, Malaysia
Hussein
Onn
Lunian F. Moreira, Federal Institute of Education, Science and Technology of Ceara´, Limoeiro do Norte, Brazil
Granada,
Carlos F.H. Moura, Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Agricultural
Narendra Narain, Federal University of Sergipe, Sa˜o Cristo´va˜o, Sergipe, Brazil
of
Nur Amalina Ismail, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia Angelo P. Jacomino, University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil Umesh B. Jagtap, Government Vidarbha Institute of Science and Humanities, Amravati, Maharashtra, India
Maria T.S.L. Neta, Federal University of Sergipe, Sa˜o Cristo´va˜o, Sergipe, Brazil Horst Bremer Neto, University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil Carlos E. Ochoa-Velasco, Beneme´rita Auto´noma de Puebla, Puebla, Mexico
Universidad
Pedro Jime´nez, Universidad Militar Nueva Granada, Bogota´, Colombia
Dalany M. Oliveira, Federal Institute of Education, Science and Technology of Paraiba, Sousa, Paraiba, Brazil
Xinwen Jin, Institute of Food Science and Technology, XAARS, Shihezi City, Xinjiang Uygur Autonomous Region, P.R. China
Luciana de S. Oliveira, Federal University of Ceara´, Fortaleza, Ceara´, Brazil
List of Contributors xvii
Amedeo Palma, Institute of Sciences of Food Production, National Research Council, Sassari, Italy
Shuaibu Babaji Sanusi, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Weider H.P. Paz, Federal University of Amazonas, Manaus, Brazil
Dio´genes H.A. Sarmento, UNIVALE, Limoeiro do Norte, Brazil
Ana L.F. Pereira, Federal University of Maranha˜o, Imperatriz, MA, Brazil
Gustavo Schwartz, Embrapa Eastern Amazon, Bele´m, Para, Brazil
Patricia M. Pinto, Cantareira College, Sa˜o Paulo, Brazil
Yuanzhi Shao, Hainan University, Hai Kou, People’s Republic of China
Stanislaw Pluta, Research Institute of Horticulture, Skierniewice, Poland
Pollyanna I. Silva, Federal University of Espı´rito Santo, Alegre, Espı´rito Santo, Brazil
Diane Ragone, National Tropical Botanical Garden, Kalaheo, HI, United States
Silvanda de M. Silva, Federal University of Paraiba State, Areia, Paraiba, Brazil
Azlen Che Rahim, Universiti Tun Malaysia (UTHM), Johor, Malaysia
Paulo C. Stringheta, Federal University of Vic¸osa, Vic¸osa, Minas Gerais, Brazil
Hussein
Onn
Marie-Christine Ralet, INRA, Nantes Research Center, Nantes, France
Chairat Techavuthiporn, Huachiew University, Samut Prakarn, Thailand
Maria do C.B. Raseira, Embrapa Temperate Agriculture, Pelotas, Rio Grande do Sul, Brazil
Luciane de L. Teixeira, University of Sa˜o Paulo, Sa˜o Paulo, Brazil
Euler E. Ribeiro, University for the Third Age, University of Amazonas State, Manaus, Amazonas, Brazil
Magda Andre´ia Tessmer, University of Sa˜o Paulo/ ESALQ, Piracicaba, Sa˜o Paulo, Brazil
Laiza B. Ribeiro, Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Tatiane de O. Tokairin, University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil
Sueli Rodrigues, Federal University of Ceara´, Fortaleza, Ceara´, Brazil Fatimah Sabran, Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia Michele R. Sagrillo, Franciscan University Center, Santa Maria, Rio Grande do Sul, Brazil Luiz C.C. Saloma˜o, Federal University of Vic¸osa, Vic¸osa, Minas Gerais, Brazil Alex Guimara˜es Sanches, Federal University of Ceara´, Fortaleza, Ceara´, Brazil Roberto C.V. Santos, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil
Chalermprakiet
Georgina Vargas-Simo´n, Universidad Jua´rez Auto´noma de Tabasco, Villahermosa, Tabasco, Mexico Rosaˆngela Vera, Federal University of Goia´s, Goiaˆnia, Brazil Maximiliano D. Vin˜oly, Federal University of Pelotas, Pelotas, Rio Grande do Sul, Brazil Yong-Ming Yuan, Firmenich Shanghai, China
Aromatics
Co.
Ltd.,
Jiaoke Zeng, Hainan University, Hai Kou, People’s Republic of China
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Preface Fruit consumption is increasing due to the world concern for health and well-being. Fruit consumption is nowadays associated with the life quality improvement due to their high content of vitamins, minerals, and antioxidant compounds. However, the most known and consumed fruits are the ones cultivated on a large scale, industrialized, and sold worldwide. Exotic fruits are usually local fruits known and consumed according to the cultural practices. Besides their atypical shape and their unique taste, exotic fruits might be richer in functional compounds than the regular ones. Some of them are cultivated on a large scale, but as any fruit, they are usually perishable and seasonal, and their exportation is limited. Other are not produced on a large scale, and most of them are not cultivated but collected and consumed by the local population. The Exotic Fruit Reference Guide introduces exotic fruits from several parts of the world. Their origin and botanical aspects, cultivation and harvest, physiology and biochemistry, chemical composition, and nutritional value are covered within the book chapters. The harvest and postharvest conservation, as well as their potential industrialization, are also presented as a way of stimulating the interest in their consumption and large-scale production. The book chapters were written by expert authors from different institutions around the world. The exotic fruits are present within the book in short and easy to read chapters to serve as a reference guide for the ones interested in exotic and different fruits. The chapters are independent and can be read in any order. Thus, enjoy the reading!
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Acknowledgment The editors acknowledge the National Institute of Tropical Fruits (INCT-FT-CNPq/FAPITEC) for funding the research in fruit processing in Brazil.
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Ac¸aı´—Euterpe oleracea Maria do S.P. de Oliveira and Gustavo Schwartz Embrapa Eastern Amazon, Bele´m, Para, Brazil
Chapter Outline Ac¸aı´ Origin, Ecology, Botany, and Socioeconomic Importance Harvest Season Estimated Annual Production and Harvest/Postharvest Conservation
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Fruit Physiology, Biochemistry, Chemical Composition, and Nutritional Value Sensory Characteristics Industrial Application or Potential Industrial Application References
4 4 4 5
AC¸AI´ ORIGIN, ECOLOGY, BOTANY, AND SOCIOECONOMIC IMPORTANCE Ac¸aı´ (Euterpe oleracea Mart.) is a palm species (family Arecaceae) native from the river Amazon’s basin. This palm species is also known as acai, assai, or huasai. Because of the denomination ac¸aı´, the species is often confused with its sister species, the lone-ac¸aı´ (Euterpe precatoria Mart.). The main difference between the two species is that E. oleracea occurs in clumps of many stems while E. precatoria always occurs in a single stem (Oliveira et al., 2015). Individuals of ac¸aı´ are commonly found in high densities spread over swamps and floodplains in clumps that can have up to 20 stems (Cavalcante, 2010). Ac¸aı´ palms have cylindrical, ringed, erect, fibrous, and branchless stems, which can reach 30 m in height and 18 cm in diameter (Fig. 1). High stem heights are only reached by individuals in their natural environments under competition against other palms and trees inside a forest. Cultivated ac¸aı´ palms are not as tall as those in nature, because they face less or no competition from other palms or trees (Oliveira et al., 2012). Each ac¸aı´ stem supports on average 1012 compound leaves of 3.5 m in length, all of them spirally arranged. Scars left by fallen leaves are found along the whole stem forming nodes and internodes (Henderson, 2000; Fig. 1). Ac¸aı´’s roots are fasciculated, dense, and superficial, with lenticels and aerenchymas sizing 1 cm in diameter. These roots are reddish and usually grow 3040 cm above ground. They are densely aggregated around each stem basis. Male and female flowers develop in the same inflorescence, hence ac¸aı´ is a monoecious species. In terms of reproduction, cross-fertilization is the most common system as incompatibility and flowering asynchrony of male and female flowers are observed (Oliveira et al., 2012). However, up to 12.9% of self-fertilization (autogamy) can occur in the species (Souza, 2002). There are two main varieties of ac¸aı´ palm: the purple or black, and the green or white ac¸aı´, where the difference is in the fruit’s skin (epicarp) color of ripe fruits (Oliveira et al., 2015). Purple ac¸aı´ contains dark skin (Fig. 2) and pulp that is used to produce purplish juice. Green ac¸aı´ has a shiny dark green pulp and its juice is soft and greenish (Cavalcante, 2010). Fruits and seeds of ac¸aı´ are spread out by a wide number of dispersers. Over short distances, fruits and seeds are dispersed by small rodents, while birds, such as toucans, guans, arac¸aris, parakeets, parrots, and thrushes, spread ac¸aı´ over long distances. Rivers and humans can also work as dispersal agents (Cymerys and Shanley, 2005). In nature, each ac¸aı´ cluster is composed by hundreds of fruits (globular drupes) with a slight depression of 12 cm in diameter and 0.62.8 g in weight (Fig. 2). They are bright green when unripe and purple or opaque green when ripe, depending on the variety (Oliveira, 2002). Each fruit contains a mesocarp 12 mm thick, which varies in color, and an edible part (epicarp and mesocarp) representing 7%25% of the fruit (Cavalcante, 2010). Seeds have a fibrous seed coat, hard endocarp and a small embryo, with abundant recalcitrant endosperm. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00002-2 © 2018 Elsevier Inc. All rights reserved.
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2
Exotic Fruits Reference Guide
FIGURE 1 Ac¸aı´ (Euterpe oleracea) palms with many stems per clump. Source: Photo by Maria do Socorro Padilha de Oliveira.
Seeds are not dormant and the species regeneration normally occurs through seedling banks. During the seedling stage, ac¸aı´ is a shade-tolerant plant, but such shade tolerance is no longer observed in adult palms, which normally reach a nearly 2025 years lifespan. Seeds are an important way of producing ac¸aı´ seedlings, so they can germinate in a few days. Seed sizes vary from 0.5 to 2.5 cm in diameter and seed weights vary from 0.6 to 2.8 g. These weights result in an average of 900 seeds per kilogram, where the variation ranges from 435 to 1250 seeds per kilogram (Queiroz and Mochiutti, 2001; Oliveira et al., 2015). Fruit production of ac¸aı´ appears as an ancient activity of the indigenous people from the Amazon. Nowadays, the palm is widely used by the local people to produce juice and palm heart, two important economic products in the Amazon, especially in the Para´ state of Brazil (Oliveira et al., 2015). The juice, obtained by macerating fruits mixed with water, is also known as ac¸aı´, which is usually sold unprocessed and pasteurized or as a mixed frozen pulp. Juice is currently the most financially profitable product of the ac¸aı´ palm for both small farmers and industrial producers. Known as an energy drink, ac¸aı´ has been accepted beyond the Amazon region. Its juice has been consumed worldwide in beverages, fruit mixes, and icecreams, where consumers recognize it as a pulp with great nutritional power. Besides the juice production, ac¸aı´ palms are widely used for ornamentation in gardens and parks of the Amazon region. Moreover, the ac¸aı´ palm has been planted to grow and protect degraded soils due to its constant leaves deposition and abundant root system to work on soil formation. In the Amazon region, ac¸aı´ has a relevant socioeconomic role. The ac¸aı´ juice is usually consumed with tapioca flour and fish as a side dish, being part of the traditional local food. Para´ is the leading ac¸aı´ production in Brazil, supplying nearly 90% of the Brazilian domestic market (Oliveira et al., 2015). Ac¸aı´ is widely appreciated in other Brazilian states and countries of the Amazon region. More recently, ac¸aı´ has also been consumed in southern and southeastern states of Brazil and many countries from South America and other continents (Santana et al., 2008). In addition to the fruit, the palm heart is appreciated and considered a fine dish. Differently from another sister species (Euterpe edulis Mart.) present in the Atlantic forest of South America, the harvesting of palm heart from ac¸aı´ does not cause the plant death. Thus, the ac¸aı´’s palm heart is commercialized in large scale, including exportation. Pasteurization/acidification and juice
Ac¸aı´—Euterpe oleracea
3
FIGURE 2 Hundreds of ripe ac¸aı´ (Euterpe oleracea) fruits from the purple variety in a single cluster. Source: Photo by Maria do Socorro Padilha de Oliveira.
freezing are part of the industrial processing of ac¸aı´. Most of the ac¸aı´ production in Para´ is sold to other nonAmazonian Brazilian states and exported. Consumers outside Para´, to where ac¸aı´ is sold or exported, usually consume processed ac¸aı´ in blends with banana, guarana, condensed milk, and cereals.
HARVEST SEASON Palms of ac¸aı´ start their reproduction phase (flowering) at nearly four years of age and the fruit production lasts an average 510 years after germination. Reproduction can start even earlier in plants under cultivation (Oliveira et al., 2002). The species presents continuous flowering and fruiting, so this means a constant production for the whole year. Flowering peaks happen from February to July and fruiting from August to December (during the rainy season) in the Eastern Amazon (Oliveira et al., 2002).
ESTIMATED ANNUAL PRODUCTION AND HARVEST/POSTHARVEST CONSERVATION A single ac¸aı´ palm, in nature, can produce 48 clusters per year, where each cluster can reach 4 kg on average in weight. Thus, an ac¸aı´ clump can produce nearly 120 kg of fruit per yearly harvest. In intensively managed ac¸aı´ crops, the average production is even higher. It can reach 1215 tons of fruits/ha/year in uplands and floodplains, respectively (Cymerys and Shanley, 2005). Fruits are harvested when completely mature, but they are not consumed without processing, as they are tasteless and present low yields from the edible parts, when compared to most of the tropical fruits (Oliveira et al., 2015). Ripe fruits, after processing to obtain the ac¸aı´ juice, present a pasty consistency. The ac¸aı´ processing is carried out mechanically or manually, where only water is added after the fruit maceration. The water makes it easier to extract pulp and filtrate the obtained juice.
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Exotic Fruits Reference Guide
Postharvest conservation of ac¸aı´ fruits consists of maintaining them under temperatures around 10 C. Fruit conservation and transport for periods longer than 48 h is traditionally done with bags covered by ice, these bags can carry up to 60 kg of fruit. When fruits or pulp are sold outside Para´ or exported, refrigerating chambers are employed to conserve their natural properties (Oliveira et al., 2015).
FRUIT PHYSIOLOGY, BIOCHEMISTRY, CHEMICAL COMPOSITION, AND NUTRITIONAL VALUE In the composition of ac¸aı´ fruits, there are nearly 90 bioactive substances, including flavonoids (31%), phenolic compounds (23%), lignoids (11%), and anthocyanins (9%). Fatty acids, quinoses, terpenes, and norisoprenoids are also found in ac¸aı´ fruits (Yamaguchi et al., 2015; Carvalho et al., 2017). The ac¸aı´ juice is a complete food that contains high lipid and fiber quantities, as well as proteins, minerals (calcium, magnesium, potassium, nickel, manganese, copper, boron, and chromium), and vitamins (B1 and E). Regarding the nutrient composition, ac¸aı´ juice is considered as complete as milk (Rogez, 2000). Anthocyanin is a pigment from the flavonoids class present in high quantities in the purple ac¸aı´ and is responsible for the characteristic fruit color (Torma et al., 2017; Carvalho et al., 2017). This pigment can offer benefits to the human health. It can help in reducing LDL (bad cholesterol). Pulp of ac¸aı´ has antiaging properties and antioxidant capacity in blood plasma. It also presents biological activity to reduce oxidative damage, inflammation in brain cells, and coronary disease risk (Heinrich et al., 2011; Yamaguchi et al., 2015). Anthocyanins are very sensible to light, heat, and oxygen, so any delay in processing ac¸aı´ fruits can interfere negatively with their natural concentration. Ac¸aı´ fruits are significantly caloric due to their high lipid levels (21%53%). Besides lipids, ac¸aı´ present total fibers (17%71%), proteins (6%12%), and carbohydrates (36%43%). Lipids from the processed pulp have high levels of unsaturated fatty acids (68%71%). The ac¸aı´’s fatty acid profile is similar to the olive and avocado oil (Rogez, 2000; Domingues et al., 2017), which is rich in oleic acid (omega 6) and linoleic (omega 9). Higher amounts of the three following fatty acids are commonly present in ac¸aı´: oleic acid (60%), palmitic acid (22%), and linoleic acid (12%). Because of its complex composition and beneficial effects to the human health, ac¸aı´ has been classified as a functional food. Nevertheless, the chemical properties and composition of ac¸aı´ fruits, including anthocyanin, phenolic compounds, acidity, soluble solids, and total solids, vary in relation to genetic features, cultivation system, harvesting techniques, maturation stage, transport time, cleaning process, and maceration (Carvalho et al., 2017; Domingues et al., 2017). Furthermore, the green ac¸aı´ contains no anthocyanin and lower oil contents compared to the purple ac¸aı´.
SENSORY CHARACTERISTICS Juice of ac¸aı´ is rarely consumed without mixing with other products, due to its low appreciated taste (Melo Neto et al., 2013). In Brazilian Amazonian states, ac¸aı´ juice is normally consumed in mixes with tapioca flour (made from manioc) and sugar. Outside this region ac¸aı´ has been consumed in blends with banana, guarana, condensed milk, and cereals, which significant changes the original ac¸aı´ taste. The specific composition of ac¸aı´ fruits permits chemical enzymatic alterations as oxidation. A visible alteration involves color changes of the juice, from purple to brown. This leads to losses of anthocyanin, the most important ac¸aı´’s pigment, due to enzymatic action. Hence, ac¸aı´ oxidation can impair the juice’s sensorial characteristics such as flavor, color, and texture.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION To make the ac¸aı´ juice, fruits need to be harvested and transported in clusters. Fruit clusters are received in places that require artisanal or industrial equipment to process fruits to obtain the ac¸aı´ juice. These processing places and equipment need to be perfectly clean, as the ac¸aı´ fruits are highly perishable, with a few hours of lifecycle at room temperature. Ac¸aı´ fruits are highly perishable due to the absence of a protective pulp skin and the fruit chemical composition (Oliveira et al., 2015; Domingues et al., 2017). Fruits have pH $ 4.5, which favors microorganism infestations that can include human pathogens. Besides the traditional use of ac¸aı´ juice, the processed pulp has been used in north Brazil to make icecream, ac¸aı´ powder jelly, sweets, and cakes (Cymerys and Shanley, 2005; Yamaguchi et al., 2015). The current domestic market in Brazil and exportation of ac¸aı´ are increasing. In the Brazilian states out of the Amazon region, ac¸aı´ has been consumed
Ac¸aı´—Euterpe oleracea
5
as frozen pulp and outside Brazil the fruit is mainly consumed as juice. Due to the rapid increase in ac¸aı´ consumption, new investments in plantings for industrial ac¸aı´ production and the management of large natural populations have been done, especially in Para´ (Nogueira and Santana, 2014). Pulp of ac¸aı´ has been used in the food industry as a natural pigment, cosmetic, pharmaceutic, or for oil extraction. Besides the traditional juice, ac¸aı´ has been used to make sweets, gelatine capsules, powders, and teas (Costa et al., 2013; Carvalho et al., 2010). Seeds of ac¸aı´ have been used for manufacturing bio jewels. Ac¸aı´ stem, besides its palm heart extraction, cellulose is produced. These stems have also been traditionally used as a support for rural buildings, lathes for fencing, corrals, walls and rafters for roofing tents, and firewood for ovens.
REFERENCES Carvalho, A.V., Mattietto, R.A., Silva, P.A., Arau´jo, E.A.F., 2010. Otimizac¸a˜o dos paraˆmetros tecnolo´gicos para produc¸a˜o de estruturado a partir de polpa de ac¸aı´. Braz. J. Food Technol. 13, 232241. Carvalho, A.V., Silveira, T.F.F.da, Mattietto, R.de A., Oliveira, M.do S.P.de, Godoy, H.T., 2017. Chemical composition and antioxidant capacity of ac¸aı´ (Euterpe oleracea) genotypes and commercial pulps. J. Sci. Food Agric. 97, 14671474. Cavalcante, P.B., 2010. Frutas comestı´veis na Amazoˆnia. Museu Paraense Emilio Goeldi, Bele´m, 280 pp. Costa, A.G.V., Garcia-Diaz, D.F., Jimenez, P., Silva, P.I., 2013. Bioactive compounds and health benefits of exotic tropical red-black berries. J. Funct. Foods. 5, 539549. Cymerys, M., Shanley, P., 2005. Ac¸aı´: Euterpe oleracea Mart. In: Shanley, P., Medina, G. (Eds.), Frutı´feras e plantas u´teis na vida amazoˆnica. CIFOR/Imazon, Bele´m, pp. 163170. Domingues, A.F.N., Mattietto, R.de A., Oliveira, M.do S.P., 2017. Teor de lipı´deos em caroc¸os de Euterpe oleracea Mart. Boletim de Pesquisa 115. Embrapa Amazoˆnia Oriental, Bele´m, 17 pp. Heinrich, M., Dhanji, T., Casselman, I., 2011. Ac¸aı´ (Euterpe oleracea Mart.)a phytochemical and pharmacological assessment of the species’ health claims. Phytochem. Lett. 4, 1021. Henderson, A., 2000. The genus Euterpe in Brazil. Sellowia. 4952, 122. Melo Neto, B.A., Carvalho, E.A., Pontes, K.V., Barreto, W.S., Sacramento, C.K., 2013. Chemical, physico-chemical and sensory characterization of mixed ac¸ai (Euterpe oleracea) and cocoa’s honey (Theobroma cacao) jellies. Rev. Bras. Frutic. 35, 587593. Nogueira, A.K.M., Santana, A.C., 2014. Benefı´cios socioeconoˆmicos da adoc¸a˜o de novas tecnologias no cultivo do ac¸aı´ no Estado do Para´. Ceres. 63, 17. Oliveira, M.do S.P.de, 2002. Aspectos da biologia floral do ac¸aizeiro nas condic¸o˜es de Bele´m, PA. Boletim de Pesquisa 8. Embrapa Amazoˆnia Oriental, Bele´m, 19 pp. Oliveira, M.do S.P.de, Carvalho, J.E.U.de, Nascimento, W.M.O.do, Mu¨ller, C.H., 2002. Cultivo do ac¸aizeiro para produc¸a˜o de frutos. Circular Te´cnica 26. Embrapa Amazoˆnia Oriental, Bele´m, 18 pp. Oliveira, M.do S.P.de, Mochiutti, S., Farias Neto, J.T.de, 2012. Domestication and breeding of assai palm. In: Bore´m, A., Lopes, M.T.G., Clement, C. R., Noda, H. (Eds.), Domestication and Breeding: Amazonian Species, first ed. Suprema Editora LTDA. P, Vic¸osa, pp. 209236. Oliveira, M.do S.P.de, Farias Neto, J.T.de, Mochiutti, S., Nascimento, W.M.O.do, Mattietto, R.de A., Pereira, J.E.S., 2015. Ac¸aı´-do-para´. In: Lopes, R., Oliveira, M. do S.P. de, Cavallari, M.M., Barbieri, R.L., Conceic¸a˜o, L.D.H.C.Hda (Eds.), Palmeiras Nativas do Brasil. Embrapa, Brası´lia, pp. 3581. Queiroz, J.A.L., Mochiutti, S., 2001. Cultivo de ac¸aizeiros e manejo de ac¸aizais para produc¸a˜o de frutos. Documentos 30. Embrapa Amapa´, Macapa´, 33 pp. Rogez, H., 2000. Ac¸aı´: preparo, composic¸a˜o e melhoramento da conservac¸a˜o. EDUFPA, Bele´m, 313 pp. Santana, A.C.de, Carvalho, D.F., Mendes, F.A.T., 2008. Ana´lise sisteˆmica da fruticultura paraense: organizac¸a˜o, mercado e competitividade empresarial. Banco da Amazoˆnia, Bele´m, 255 pp. Souza, P.C.A.de, 2002. Aspectos ecolo´gicos e gene´ticos de uma populac¸a˜o natural de Euterpe oleracea Mart. no estua´rio amazoˆnico (Masters dissertation). University of Sa˜o Paulo, Piracicaba, 60 pp. Torma, P.C.M.R., Brasil, A.S., Carvalho, A.V., Jablonski, A., Rabelo, T.K., Moreira, J.C.F., et al., 2017. Hydroethanolic extracts from different genotypes of ac¸aı´ (Euterpe oleracea) presented antioxidant potential and protected human neuron-like cells (SH-SY5Y). Food Chem. 222, 94104. Yamaguchi, K.K.L., Pereira, L.F.R., Lamara˜o, C.V., Lima, E.S., Veiga-Junior, V.F., 2015. Amazon acai: chemistry and biological activities: a review. Food Chem. 179, 137151.
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Acerola—Malpighia emarginata Carlos F.H. Moura1, Luciana de S. Oliveira2, Kellina O. de Souza2, Lorena G. da Franca3, Laiza B. Ribeiro1, Pahlevi A. de Souza3 and Maria R.A. de Miranda2 1 3
Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil, 2Federal University of Ceara´, Fortaleza, Ceara´, Brazil Federal Institute of Education, Science and Technology of Ceara´, Limoeiro do Norte, Brazil
Chapter Outline Origin and Botanical Classification Production Harvest
7 8 8
Postharvest Postharvest Quality References
8 10 13
ORIGIN AND BOTANICAL CLASSIFICATION Acerola or the Barbados cherry tree are the common names of Malpighia emarginata D.C., and its taxonomic classification is: class Magnoliopsida, order Malpighiales, family Malpighiaceae, genus Malpighia, and species M. emarginata D.C. It is not precisely determined, but the acerola tree is probably native to islands of the Caribbean and Antilles, although it may be found in the wild and cultivated in northern South America, Central America and Southern Mexico. Its dissemination proceeded gradually by the inhabitants of these regions, as they travelled and emigrated to other areas and islands (Manica et al., 2003; Marino Neto, 1986; Montimet al., 2010). According to Santos (2009), there are several genetic acerola materials currently cultivated in Brazil, and among them, those with registry under the Brazilian Ministry of Agriculture Livestock and Supply (MAPA, 2012) are Apodi (BRS 235), BRS Cabocla, Cereja (BRS 236), Frutacor (BRS 238), Okinawa, Roxinha (BRS 237), Jaburu (BRS 366), BRS Rubra, Flor Branca, Sertaneja (BRS 152), among others (MAPA, 2012). The acerola plant is considered a medium sized evergreen shrub, reaching 24 m in diameter with a single branched trunk and dense canopy of bent down branches with small dark green leaves, that produce fruit throughout the year (Castro and Kluge, 2003; Portal Sao Francisco, 2017; Sebrae, 2016). The leaves are opposite with short petioles, oval to elliptical-shaped as their base and apex are often pointy, ranging from 2.5 to 9.0 cm in length and 1.2 to 6.0 cm in width. The adaxial surface is dark green and shiny while, the abaxial surface is light green and their pilosity is more intense in younger leaves (Oliveira et al., 2003). The flowers are hermaphroditic, arranged in small axillary petiolated clusters with three to five perfect flowers ranging from 2.0 to 2.5 cm in diameter and with buds usually opening at 45 a.m. (Oliveira et al., 2003; Sazan et al., 2014). Flower pollination depends on external agents and the effect of pollination influences fruit yield as the number of established fruit may decrease due to self-incompatibility and the absence of an effective pollination (Ritzinger et al., 2004). Acerola has a high rate of autoincompatibility which results from an interaction between pollen and flower stigma and restrains pollen tube germination in the stigma of the same plant. Autoincompatibility is set as incapacity of a fertile hermaphrodite plant in producing zygotes after self-pollination, it is of importance to genetic improvement programs as a means to obtain hybrids without the need of manual crossings. Cross-pollination is promoted by pollinators as they collect food material in different flowers, whilst pollen is adhered to their body parts (Vilhena and Augusto, 2007).
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00003-4 © 2018 Elsevier Inc. All rights reserved.
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Exotic Fruits Reference Guide
The acerola tree bears fruit in the first year of development, and from thereon may present four to seven production peaks per year, depending on edaphoclimatic conditions and crop management. The average production ranges from 2.0 kg/plant, in the first year to 47.0 kg/plant in the sixth year and under irrigation, production is continuous year-round (Portal Sao Francisco, 2017; Vilela, 2009). The fruit is a drupe and when ripe, has a thin epicarp, a mesocarp (pulp) that represents 70%80% of total fruit weight, and a tri-lobed endocarp enveloping an average of one seed with 35 mm in diameter, an oval shape and two cotyledons (Almeida et al., 2000). After fruit establishment, development happens over an average 22 day period leading to a ripe edible pulp which is fleshy, soft, juicy with an acidic flavor and extremely rich in vitamin C (Chitarra and Chitarra, 2006). After maturation, acerola ripening and senescence are fast which makes it difficult to handle and storage after harvest.
PRODUCTION The acerola tree is a tropical species characterized by a rapid growth and establishment of disorderly orchards when plants are originated from sexual reproduction with significant differences in plant size and production as well as in fruit size, shape, color, and vitamin C content. Although acerola is grown in several countries of the Americas, Brazil is currently the largest world producer, consumer and exporter (Sazan et al., 2014). In 1950, acerola was introduced in the Northeast region of Brazil by researchers of the Rural Federal University of Pernambuco, who brought the first seeds from Puerto Rico (Souza et al., 2006). However, in Brazil, its cultivated area grew more intensely during 198892 due to greater interest for the fruit’s high vitamin C content by consumers, industrialists, and exporters (Arau´jo et al., 2007). Acerola is cultivated throughout Brazils Northeast, North, South and Southeast regions (Ritzinger and Ritzinger, 2004) with an average production of 29.65 t/ha per year equivalent to 59.3 kg/plant per year (Agrianual, 2010). The ideal climate for acerola growth is characterized by an average temperature of 26 C and 12001600 mm of rainfall with the spacing between plants ranging from 4.0 3 4.0 to 6.0 3 6.0 m. Under such conditions of spacing and irrigation, a better productivity may be achieved with 625 plants occupying a hectare and yielding up to 100 kg of fruits/plant per year (Sebrae, 2016). Regarding its susceptibility to pests, the acerola tree is quite resistant with occasional predation by cochineal bugs and aphids on branches and leaves. However, it is necessary to control fruit fly to avoid greater losses, while the most common diseases are Cercospora, scab and anthracnose (Sebrae, 2016).
HARVEST Harvest is the removal of whole plant or their parts in a timely manner as to minimize loss. Breeding programs have focused on the improvement of cultivars better adapted to mechanical harvesting systems as a means to lower production costs. Among acerola cultivars, variety BRS 366-Jaburu is well adapted to both manual and mechanized harvesting. However, fruit harvest is mostly manual and happens on a daily basis, due to accelerated ripening and fragility of produce (Almeida et al., 2000). Moreover, harvest will depend mainly upon the kind of market the fruit is destined for, thus fruit destined for in natura or fresh consumption or processed pulp and juice production should be harvested with a fully ripe red-colored peel (Fig. 1). However, if it is destined for industrial uses as a pharmaceutical or concentrated extracts to supplement other foodstuff, harvesting should be done with immature vitamin C rich green-colored fruit (Table 1). (Portal Sao Francisco, 2017). Fruit destined for more distant markets should be harvested at the physiological maturity with largest size and peel turning red, a stage which requires further care at harvest and postharvest handling so the metabolism will not be accelerated due to injuries or damages. Therefore, after harvest, fruit should be placed and transported to packing house in plastic boxes with a maximum height of 15.0 cm (Almeida et al., 2000).
POSTHARVEST The mature or ripe acerola (Fig. 1) is a very delicate and highly perishable product with a storage life of 24 days at temperature higher than 20 C (Vendramini and Trugo, 2000; Scalon et al., 2004). Thus, the fragility of ripe acerola is by far one of the main problems faced by producers during harvesting, packing, processing, and distribution. The thin and delicate peel of ripe fruit can be easily damaged, resulting in general deterioration of pulp quality. The main reason
Acerola—Malpighia emarginata
9
FIGURE 1 Acerolas cv. BRS 366 “Jaburu” in different developmental stages: (A) Immature-green; (B) Physiological maturity-turning red and (C) Ripe-red colored. From Souza, K.O., Moura, C.F.H., Brito, E.S., Miranda, M.R.A., 2014. Antioxidant compounds and total antioxidant activity in fruits of acerola from cv. flor branca, florida sweet and BRS 366. Rev. Brasileira de Fruticul. 36, 294304.
TABLE 1 Quality Attributes During the Development of Acerola Characteristics
pH
Developmental stage Immature
Physiological maturity
Ripe
3.033.55
3.033.56
3.323.68
Soluble solids ( Brix)
5.507.06
6.409.10
6.7012.70
Titrable acidity (% malic acid)
0.901.59
0.831.17
0.611.06
SS/TA ratio
4.567.80
4.9210.96
5.1115.42
Total sugar (%)
1.603.59
2.475.72
2.756.03
Vitamin C (mg/100 g)
1501.173756.06
1239.602495.91
862.861820.70
Protein (mg/g)
1.20
0.90
0.20
Firmness (N)
22.3438.36
11.1222.16
8.5410.50
From Figueiredo Neto, A., Reis, D.S., Alves, E., Gonc¸alves, E., Anjos, F.C., Ferreira, M., 2014. Determinac¸a˜o de vitamina C e avaliac¸a˜o fı´sico-quı´mica em treˆs variedades de acerola cultivadas em Petrolina-Pe. Nucleus 11, 83-92; Oliveira, L.S., Moura, C.F.H., Brito, E.S., Mamede, R.V.S., Miranda, M.R.A., 2012. Antioxidant metabolism during fruit development of different acerola (Malpighia emarginata D.C) clones. J. Agric. Food Chem. 60, 79577964; Souza, K.O., Moura, C.F.H., Brito, E.S., Miranda, M.R.A., 2014. Antioxidant compounds and total antioxidant activity in fruits of acerola from cv. flor branca, florida sweet and BRS 366. Rev. Brasileira de Fruticul. 36, 294304.
for acerola perishability is the climacteric maturation behavior with a high respiratory rate, 900 mL CO2/kg per h, in spite of the low ethylene production, 3 μL C2H4/kg per h (Carrington and King, 2002). After harvest, ripening and senescence proceeds as several physiological reactions take place that result in chlorophyll degradation while other pigments accumulate, reduction of acidity and vitamin C and increase in sugars (Table 1). Therefore, postharvest technologies have been developed to maintain fruit quality for longer storage periods. Thus, whole acerolas harvested at physiological maturity can have their storage life extended to 12 days under refrigeration at 12 C, and an atmosphere modified by polyvinylchloride (PVC) film (Scalon et al., 2004). The storage life of whole ripe fruit can be extended to 3 more days at room temperature (. 20 C), if covered with PVC film (Alves and Filgueiras, 1999). It is therefore important that producers clearly define which product and/or market is aimed for, thus determining the optimal harvest stage. International markets have different requirements regarding fruit quality, e.g., in Europe, buyers require fruit with a minimum 7.0 Brix of soluble solids (SS), 7.5 Brix to Japan and an average vitamin C content of 1000 mg/100 g pulp to the United States. For the vitamin C market, after harvest, fruit stability is also affected by sunlight, as exposure to radiation for over 4 h induces a substantial loss of this vitamin, requiring that harvesting occurs at early hours of day.
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Exotic Fruits Reference Guide
Furthermore, Realini et al. (2015) reported the stability of vitamin C in acerola fruits or derived products depends on both the processing system and storage temperature, and that pasteurization followed by freezing results in greatest vitamin C retention.
POSTHARVEST QUALITY Quality refers to a set of attributes or properties that make fruit appreciable as food and can be influenced by several factors. Weight and size are physical characteristics inherent to each species or cultivars, however, they are used as quality criteria for selection and classification of products according to the consumer market (Chitarra and Chitarra, 2006). The mature acerola weighs from 4 to 10 g with a juicy pulp representing up to 80% of total weight, and at this stage, ripe fruit are soft, while an immature green fruit is three times firmer (Table 2) (Batista et al., 2015; Lima et al., 2014; Moura et al., 2007). Fruit firmness is due to cell turgidity and to mechanical properties of biological membranes and cell wall. Lipids are the major constituents of cell membranes, and are highly susceptible to oxidation by free radicals produced as fruit ripens, leading to loss of membrane integrity. Thereby, as acerola ripens, there is an increase in lipid peroxidation degree which is correlated to vitamin C loss (Oliveira et al., 2012), indicating that this antioxidant compound is the major antioxidant protection against cellular oxidative damage in this species. Among the components of acerola cell wall, pectins have contents varying from 94.93 to 246.71 mg/100 g pulp (Batista et al., 2015) and are responsible for the turbidity and viscosity of juice. When fruit tissue is macerated, soluble pectin is found in the liquid phase, leading to an increase in viscosity, whereas other pectin molecules remain bound to cellulose, and thus facilitate the retention of water. In immature acerola, pectin is insoluble and attached to cellulose microfibrils contributing to cell wall resistance, but during ripening, the pectin structure is modified by enzymes with an increasing solubility (Assis et al., 2008). In acerola, flavor is influenced by aromatic profile represented by a mixture of volatile compounds as esters, ketones, and terpenes (Table 3) and degradation of flavonoids and tannins, which contribute to the astringency. Ripe acerola has a subtle aroma described as resembling those of apples and slightly sweet (Delva and Schneider, 2013). The distinctive sour taste of these fruits is influenced during maturation by sugar accumulation due to starch hydrolysis or to gluconeogenesis (Oliveira et al., 2011), and mainly by the decrease in acidity as organic acids are consumed as substrates in respiration causing a relative increase in sugar/acid that varies from 4.22 to 8.31 (Lima et al., 2014; Batista et al., 2015). As shown in Table 3, over 65% of the aromatic volatile compounds identified in mature acerola belong to three groups: esters (29%), alcohols (23%), and ketones (16%), among which furfural, 3-methyl-3-butenol, limonene, and hexadecanoic acid are the main constituents (Arra´zola et al., 2014). Some of the identified compounds are products of ascorbic acid degradation pathways (Delva and Schneider, 2013).
TABLE 2 Physical Characteristics of Ripe Acerola Characterı´stics
Values
Mass (g)
4.039.88
Diameter (cm)
1.662.70
Color L
20.4842.42
Chroma
16.3648.23
9.1735.25
Hue
From Batista, P.F., Lima, M.A.C., Trindade, D.C.G., Alves, R.E., 2015. Quality of different tropical fruit cultivars produced in the lower basin of the Sa˜o Francisco valley. Rev. Cieˆncia Agr. 46, 176184; Lima, P.C.C., Souza, B.S., Souza, P.S., Borges, S.D.S., Assis, M.D.O., 2014. Characterization and evaluation of fruits of West Indian cherry. Rev. Brasileira de Fruticul. 36, 550555.
Acerola—Malpighia emarginata
11
TABLE 3 Volatile Compounds of Ripe Acerola Compounds
Content (ppm)
Furfural
2.19
3-methyl-3-butenol
0.72
Limonene
0.68
Hexadecanoic acid
0.58
Methyl hexanoate
0.36
Ethyl hexanoate
0.23
From Delva, L., Schneider, R.G., 2013. Acerola (Malpighia emarginata D. C.): Production, postharvest handling, nutrition, and biological activity. Food Rev. Int. 29, 107126.
Color is an important attribute of consumer acceptance and during ripening, it changes from green to red due to chlorophyll degradation enabling preexisting pigments to stand out and/or synthesis of new pigments such as anthocyanins and carotenoids (Prasanna et al., 2007; Moura et al., 2008). In acerola, the yellow color imparted by the carotenoids is masked by reddish pigments such as anthocyanins (Freitas et al., 2006). The chemical composition of acerola is influenced by genotype, environment and maturation stage. Table 4 shows the average composition of mature acerola pulp with a pH ranging from 2.90 to 3.70 and titratable acidity ranging from 0.70% to 1.87% malic acid, which represents 32% of total acids in mature fruits (Righetto et al., 2005; Maciel et al., 2010). In acerola, the predominant organic acids are malic acid, 0.25%0.38%, citric, 0.01%0.03%, and tartaric acid 0.002%0.01%. The SS influences directly ripe fruit flavor and ranges between 5.48 and 11.46 Brix (Maciel et al., 2010; Lima et al., 2014). As only traits of starch are found in mature acerola, gluconeogenesis is probably the main route for sugar synthesis. However, in mature fruits, other compounds besides organic acids also contribute to the increase in SS for positive correlations with vitamin C, and polyphenols and anthocyanins contents have been reported (Oliveira et al., 2011). Considering its chemical composition (for 100 g fruit), acerola has a water content ranging from 92% to 95%, 332 kcal of calories which are assigned to carbohydrates (57.24 g), lipids (3.2 g) and protein (16.94 g) contents (Dembitsky et al., 2011). Regarding the lipid fraction, the following fatty acids were identified: oleic (31.9%), linoleic (29.2%), palmitic (21.8%), stearic (13.9%) and linolenic (1.3%) (Medeiros-Aguiar et a1., 2010). The main sugars are fructose and glucose, and to a lesser extent, sucrose (Mezadri et al., 2008). Among the phytochemical constituents of acerola, there are vitamins as thiamine (B1), riboflavin (B2), niacin (B3), and provitamin A and minerals as calcium, iron, potassium, magnesium, and phosphorus (Adriano et al., 2011). However, its greatest nutritional appeal is a very high content vitamin C ranging from 862.86 to 1465.22 mg/100 g pulp in ripe fruit that can reach up to 3756.06 mg/100 g pulp in immature fruit (Figueiredo Neto et al., 2014; Oliveira et al., 2012; Souza et al., 2014). The concentration of this important compound for human health decreases during ripening mainly due to biochemical oxidation. This hypothesis was verified when the compound 3-hydroxy-2-pyrone, a product of oxidative degradation of ascorbic acid, was detected in aroma profile of mature acerola (Vendramini and Trugo, 2000). The synthesis and retention of vitamin C in these fruits are influenced by factors including propagation form as fruit from sexually propagated plants have lower contents than those of plants obtained by asexual methods (Silva, 1994) and, furthermore, the concentration of vitamin C is greatest between 16 and 18 days after anthesis. Postharvest processing and storage strongly affects vitamin C stability, thus acerolas pulp puree stored for 10 months at 18 C presented a decline of 60% in vitamin C content (Oliveira et al., 2011) and the same authors stated vitamin C was the major contributor to the antioxidant potential of acerola pure´e. In acerola, polyphenols are the most abundant secondary metabolites, and as vitamin C, are important antioxidants for humans (Chim et al., 2013). Ripe fruits have high concentrations of total polyphenols ranging from 1561.67 to 2631.34 mg gallic acid equivalent/100 g pulp, among which flavonoids and phenolic acids stand out (Souza et al., 2014). Among the flavonoids, anthocyanins, procyanidins, flavonols, and catechins are the main identified
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Exotic Fruits Reference Guide
TABLE 4 Nutritional Composition of Ripe Acerola Nutrient
Values
Data from
Water (%)
92.6095.00
Arra´zola et al. (2014)
Protein (%)
0.211.20
Arra´zola et al. (2014)
Fat (%)
0.230.80
Mezadri et al. (2008)
Carbohydrates (%)
0.43
Arra´zola et al. (2014)
Starch (%)
0.050.23
Batista et al. (2015)
Sugar (%)
2.756.03
(Souza et al., 2014)
Vitamin C
862.861465.22
Lima et al. (2014); Souza et al. (2014)
Vitamin B6
0.009
Freitas et al. (2006)
Vitamin B2
0.006
Freitas et al. (2006)
Vitamin B3
0.40
Freitas et al. (2006)
Vitamin B5
0.31
Freitas et al. (2006)
Phosphorous
11.0
Freitas et al. (2006)
Calcium
12.0
Freitas et al. (2006)
Iron
0.20
Freitas et al. (2006)
Potassium
146.0
Freitas et al. (2006)
Magnesium
18.0
Freitas et al. (2006)
Sodium
7.0
Freitas et al. (2006)
Vitamins (mg/100 g)
Minerals (mg/100 g)
Ash (%)
4.915.23
Arra´zola et al. (2014); Rufino et al. (2010)
Fiber (%)
0.161.63
Arra´zola et al. (2014); Rufino et al. (2010)
Pectin (mg/100 g)
94.93246.71
Batista et al. (2015)
Lipid peroxidation (nmol MDA/g)
59.75119.97
Oliveira et al. (2012)
(Schreckinger et al., 2010). Anthocyanins and yellow flavonoids are main responsible for fruit pigmentation, as the characteristic red color of fruit peel is one of the most important indicators of its maturity and its edible quality. The anthocyanin content can vary between 6.49 and 17.72 mg/100 g (Oliveira et al., 2012) and consists mainly of cyanidin 3-O-α-rhamnoside and pelargonidin-3-α rhamnoside, although malvidin 3.5-diglucoside has also been found (Oliveira et al., 2013; Dembitsky et al., 2011). Cyanidin contents have ranged from 58 to 241 mg/100 g dry matter of ripe acerola fruits from six different genotypes (Oliveira et al., 2012). As acerola ripens, the anthocyanin content would be preserved by the high levels of vitamin C, once the latter presents a much higher decay rate than anthocyanin (Oliveira et al., 2013). The flavonols quercetin and kaempferol are abundant in ripe acerolas with average concentrations of 27 μg/g dry weight and 14 mg/g dry matter, respectively (Betaglion et al., 2015). Oliveira et al. (2012) reported quercetin contents ranging from 12 to 33 mg/100 g dry matter of ripe acerola fruits from six different genotypes. The caffeic phenolic acids, ρ-coumaric and ferulic were also found in fruits of this species (Schreckinger et al., 2010). Due to its composition, acerola is considered a functional fruit despite the reports that show a reduction in bioactive compounds content during ripening (Oliveira et al., 2012; Souza et al., 2014). Thus, it still presents a high potential in the food industry as a great source of both vitamin C and phenolics that may be used as nutritional supplement or as natural additives to improve the nutritional quality of other foods.
Acerola—Malpighia emarginata
13
REFERENCES Adriano, E., Leonel, S., Evangelista, R.M., 2011. Fruit quality of Barbados cherry trees Cv. Olivier in two stages of maturity. Rev. Bras. Fruticultura. 33, 541545. Agrianual, 2010. Anua´rio da Agricultura Brasileira. FNP Consultoria e Come´rcio, Sa˜o Paulo. Almeida, J.I.L., Lopes, J.G.V., Oliveira, F.M.M., 2000. Produtor de acerola. Edic¸o˜es Demo´crito Rocha, Instituto Centro de Ensino Tecnolo´gico, Fortaleza. Alves, R.E., Filgueiras, H.A.C., Mosca, J.L., Menezes, J.B., 1999. Brazilian experience on the handling of acerola fruits for international trade: Harvest and postharvest recommendations. Acta Hortic. 485, 3136. Arau´jo, P.G.L., Figueiredo, R.W., Alves, R.E., Maia, G.A., Paiva, J.R., 2007. β-Carotene, ascorbic acid and total anthocyanins in fruit pulp of the acerola tree conserved by the cold for 12 months. Cieˆnc. Tecnol. Aliment. 27, 104107. Arra´zola, G., Alvis, A., Pa´ez, M., 2014. Composicio´n, ana´lisis termofı´sico y sensorial de frutos colombianos. Parte 2: Acerola (Malpighia emarginata D. C.). Inf. Tecnol. 25, 2330. Assis, S.A., Fernandes, F.P., Martins, A.B.G., Oliveira, O.M.M.F., 2008. Acerola: Importance, culture conditions, production and biochemical aspects. Fruits. 63, 93101. Batista, P.F., Lima, M.A.C., Trindade, D.C.G., Alves, R.E., 2015. Quality of different tropical fruit cultivars produced in the lower basin of the Sa˜o Francisco valley. Rev. Cieˆnc. Agron. 46, 176184. Betaglion, G.A., Silva, F.M.A., Eberlin, M.N., Koolen, H.H.F., 2015. Determination of the phenolic composition from brazilian tropical fruits by UHPLC Ms/Ms. Food. Chem. 180, 280287. Carrington, C.M.S., King, R.A.G., 2002. Fruit development and ripening in Barbados cherry, Malpighia emarginata D. C. Sci. Hortic. (Amsterdam). 92, 17. Castro, P.R.C., Kluge, R.A., 2003. Ecofisiologia de fruteiras: abacateiro, aceroleira, macieira, pereira e videira. Editora Agronoˆmica Ceres Ltda, Piracicaba. Chim, J.F., Zambiazi, R.C., Rodrigues, R.S., 2013. Estabilidade da vitamina C em ne´ctar de acerola sob diferentes condic¸o˜es de armazenamento. Rev. Bras. Prod. Agroind. 15, 321327. Chitarra, M.I.F., Chitarra, A.B., 2006. Po´s-colheita de frutas e hortalic¸as: Glossa´rio. Editora UFLA, Lavras. Dembitsky, V.M., Poovarodom, S., Leontowicz, H., Leontowicz, M., Vearasilp, S., Trakhtenberg, S., et al., 2011. Review. The multiple nutrition properties of some exotic fruits: Biological activity and active metabolics. Food Res. Inter. 44, 16711701. Delva, L., Schneider, R.G., 2013. Acerola (Malpighia emarginata D. C.): Production, postharvest handling, nutrition, and biological activity. Food Rev. Inter. 29, 107126. Freitas, C.A.S., Maia, G.A., Costa, J.M.C., Figueiredo, R.W., Sousa, P.H.M., Fernandes, A.G., 2006. Stability of carotenoids, anthocyanins and vitamin c presents in acerola sweetened tropical juice preserved by hot fill and aseptic processes. Rev. Cieˆnc. Agrotecnol. 30, 942949. Figueiredo Neto, A., Reis, D.S., Alves, E., Gonc¸alves, E., Anjos, F.C., Ferreira, M., 2014. Determinac¸a˜o de vitamina C e avaliac¸a˜o fı´sico-quı´mica em treˆs variedades de acerola cultivadas em Petrolina-Pe. Nucleus. 11, 8392. Lima, P.C.C., Souza, B.S., Souza, P.S., Borges, S.D.S., Assis, M.D.O., 2014. Characterization and evaluation of fruits of West Indian cherry. Rev. Bras. Fruticultura. 36, 550555. Maciel, M.I.S., Me´lo, E., Lima, V., Souza, K.A., Silva, W., 2010. Caracterizac¸a˜o fı´sico-quı´mica de frutos de geno´tipos de aceroleira (Malpighia emarginata D.C.). Cieˆnc. Tecnol. Aliment. 30, 865869. Manica, I., Icuma, I.M., Fioravanc¸o, J.C., Paiva, J.R., Paiva, M.C., Junqueira, N.T.V., 2003. Clima e Solo. In: Manica, I. (Ed.), Acerola: tecnologia de produc¸a˜o, po´s-colheita, congelamento, exportac¸a˜o, mercados, first ed. Cinco Continentes, Porto Alegre. Marino Neto, L., 1986. Acerola: A cereja tropical. Nobel, Sa˜o Paulo. Medeiros de Aguiar, T., Rodrigues, F.D.S., Ribeiro dos Santos, E., Sabaa-Srur, A.U.D.O., 2010. Chemical characterization and evaluation of the nutritional value Malpighia punicifoliaseeds. Nutrire. 19, 6772. Mezadri, T., Villano, D., Fernandez-Pachon, M.S., Garcia-Parrilla, M.C., Troncoso, A.M., 2008. Antioxidant compounds and antioxidant activity in acerola (Malpighia emarginata D.C.) fruits and derivatives. J. Food Composit. Anal. 21, 282290. Ministe´rio da Agricultura, Pecua´ria e Abastecimento (MAPA), 2012. Cultivarweb: Gerenciamento Da Informac¸a˜o. Registro Nacional de Cultivares (Rnc). Brası´lia, Available at: ,http://extranet.agricultura.gov.br/php/snpc/cultivarweb/cultivares_registradas.php.. Montim, M., Oliveira, C.A., Vieira, M.L.C., 2010. Karyotype characterization of Malpighia emarginata (Malpighiaceae). Rev. Bras. Fruticultura. 32, 369374. Moura, C.F.H., Alves, R.E., De Figueiredo, R.W., De Paiva, J.R., 2007. Physical and physical-chemical evaluations of fruits of West Indian cherry (Malpighia emarginata D.C.) Clones. Rev. Cieˆnc. Agron. 38, 5257. Moura, C.F.H., Alves, R.E., Figueiredo, R.W., Paiva, J.R., 2008. Avaliac¸o˜es fı´sicas e fı´sico-quı´micas de frutos de clones de aceroleira (Malpighia emarginata D. C.). Rev. Cieˆnc. Agron. 38, 5257. Oliveira, L.S., Rufino, M.S.M., Moura, C.F.H., Cavalcanti, F.R., Alves, R.E., Miranda, M.R.A., 2011. The influence of processing and long-term storage on the antioxidant metabolism of acerola (Malpighia emarginata D.C.) pure´e. Braz. J. Plant Physiol. 23, 151160. Oliveira, L.S., Moura, C.F.H., Brito, E.S., Mamede, R.V.S., Miranda, M.R.A., 2012. Antioxidant metabolism during fruit development of different acerola (Malpighia emarginata D.C) clones. J. Agric. Food. Chem. 60, 79577964. Oliveira, L.S., Moura, C.F.H., Brito, E.S., Fernandes, F.N., Miranda, M.R.A., 2013. Quality changes and anthocyanin and vitamin c decay rates of frozen acerola pure´e during long-term storage. J. Food Process Preservat. 37, 2533.
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Exotic Fruits Reference Guide
Oliveira, J.R.P., Reinhardt, D.H., Soares Filho, W.S.S., 2003. Colheita. In: Ritzinger, R., Kobayashi, A.K., Oliveira, J.R.P. (Eds.), A cultura da aceroleira, ed. 1 Embrapa Mandioca e Fruticultura, Cruz das Almas. Portal Sa˜o Francisco, Acerola, 2017. Disponı´vel em: ,http://www.portalsaofrancisco.com.br/alfa/acerola/acerola.php.. Acesso em abr./2017. Prasanna, V., Prabha, T.N., Tharanathan, R.N., 2007. Fruit ripening phenomena - An overview. Crit. Rev. Food. Sci. Nutr. 47, 119. Realini, C.E., Guardia, M.D., Diaz, I., Garcia-Regueiro, J.A., Arnau, J., 2015. Effects of acerola fruit extract on sensory and shelf-life of salted beef patties from grinds differing in fatty acid composition. Meat Sci. 99, 1824. Righetto, A.M., Netto, F.M., Carraro, F., 2005. Chemical composition and antioxidant activity of juices from mature and immature acerola (Malpighia emarginata D.C.). Food Sci. Technol. Inter. 11, 315321. Ritzinger, R., Ritzinger, C.H.S.P., 2004. Acerola: aspectos gerais da cultura. Embrapa Mandioca e Fruticultura, Cruz das Almas. Ritzinger, R., Silva, L.C.V., Alves, M.G.V., 2004. Polinizac¸a˜o da aceroleira. Embrapa Mandioca e Fruticultura. Acerola em foco, Cruz das Almas, p. 7. Rufino, M.S.M., Perez-Jimenez, J., Tabernero, M., Alves, R.E., Brito, E.S., Saura-Calixto, F., 2010. Acerola and cashew apple as sources of antioxidants and dietary fibre. Inter. J. Food Sci. Technol. 45, 22272233. Santos, S.M.L. Resfriamento ra´pido de acerola por ar forc¸ado: avaliac¸a˜o dos paraˆmetros fı´sicos, fı´sico-quı´micos, sensoriais e do processo, 2009. 123 f. Dissertac¸a˜o (Mestrado em Tecnologia de Alimentos) - Centro de Cieˆncias Agra´rias, Universidade Federal do Ceara´. Fortaleza. Sazan, M.S., Queiroz, E.P., Caliman, L.J.F., Parra-Hinijosa, A., Silca, C.I., Fonseca, V.L.I., et al., 2014. Manejo de polinizadores da aceroleira. Holos, Ribeira˜o Preto. Scalon, S.D.P.Q., Dell’olio, P., Fornasieri, J.L., 2004. Temperatura e embalagens na conservac¸a˜o po´s-colheita de eugenia uvalha cambess - mirtaceae cambess - mirtaceae. Cieˆnc. Rural. 34, 19651968. Schreckinger, M.E., Lotton, J., Lila, M.A., Mejia, E.G., 2010. Berries from south america: A comprehensive review on chemistry, health potential and commercialization. J. Med. Food. 13, 233246. Sebrae-Sistema Brasileiro de Apoio a Micro e Pequena Empresa, 2016. O Cultivo e o mercado da acerola. Sebrae. Available at: ,http://www.sebrae. com.br/sites/portalsebrae/artigos/O-cultivo-e-o-mercado-da-acerola.. Silva, J.J.M., 1994. Fatores que afetam o conteu´do de acido asco´rbico de acerola (Malpighia glabra L.). Secretaria Municipal de Produc¸a˜o e Abastecimento, Sa˜o Luis. Souza, K.O., Moura, C.F.H., Brito, E.S., Miranda, M.R.A., 2014. Antioxidant compounds and total antioxidant activity in fruits of acerola from cv. flor branca, florida sweet and BRS 366. Rev. Bras. Fruticultura. 36, 294304. Souza, M.J.H., Guimara˜es, M.C.A., Guimara˜es, C.D.L., Freitas, W.S., Oliveira, A.M.S., 2006. Potencial agroclima´tico para a cultura da acerola no estado de Minas Gerais. Rev. Bras. Engenh. Agrı´c. Ambient. 10, 390396. Vendramini, A.L., Trugo, L.C., 2000. Chemical composition of acerola fruit (Malpighia punicifolia L.) at three stages of maturity. Food. Chem. 71, 195198. Vilela, P.A. Servic¸o Brasileiro de Apoio a Micro e Pequena Empresa Sebrae. Disponı´vel em: ,http://sebrae.com.br/setor/fruticultura/o-setor/frutas/ acerola. Acesso em: abr./2009. Vilhena, A.M.G.F., Augusto, S.C., 2007. Polinizadores da aceroleira Malpighia emarginata D. C. (Malpighiaceae) em a´rea de cerrado no triaˆngulo mineiro. Biosci. J. 23, 1423.
Ambarella—Spondias cytherea Benoit B. Koubala1, Germain Kansci2 and Marie-Christine Ralet3 1
University of Maroua, Maroua, Cameroon, 2University of Yaounde, Yaounde, Cameroon, 3INRA, Nantes Research Center, Nantes, France
Chapter Outline Introduction Origin and Distribution Botanical Aspects Taxonomy and Colloquial Names Description Harvest and Production Fruit Physiology and Biochemistry Fruit Development and Maturation Fruit Ripening
15 15 16 16 16 17 17 17 18
Chemical Composition and Nutritional Value of the Fruit Sensory Characteristics of the Fruit Conservation Application Acknowledgment References
18 20 20 20 21 21
INTRODUCTION Ambarella, like most other exotic fruits, is tropically widespread. This species has many common names according to the place where it grows. It is called Ambarella, Golden apple, Cajarana or Cassemango. Along with mango and cashew, they are the main economical trees in the family of Anacardiceae (De Laroussilhe, 1980; Morton, 1987). In Africa it is mostly found in Cameroon and Gabon (Pele and Le Berre, 1966). It is also found in many tropical regions and countries such as Florida, Venezuela, Grenada, and Indonesia (Backer and Bakhuisen, 1965; Morton, 1987). Mango tree is more widespread and than ambarella. However, cassemango fruit exhibits the highest amount of organic acid as vitamin C. For a long time, ambarella was not commercially cultivated in some countries. It was at first considered a backyard tree or forest plant. In the last three decades, because of the world crisis in production of commercial crops, some countries have encouraged the development of nontraditional fruit crops. This was the case of golden apple in Grenada (Daulmerie, 1994). According to Bauer et al. (1993), and despite its worldwide distribution and importance, ambarella has received little recognition from scientific community. It is only during the 1990s that research on Spondias cytherea started to increase (Favier et al., 1993; Campbell et Sauls, 1994; Daulmerie, 1994; Vivien and Faure, 1996; Jirovetz et al., 1999). Before this date, only the botanical aspect of the plant was studied.
ORIGIN AND DISTRIBUTION The ambarella tree grows in humid tropical and subtropical regions. It can grow at an altitude of up to 700 m (Mohammed et al., 2011). Generally, Golden apple is native from Melanesia (Morton, 1987). But specifically it is from Tahiti where the epithet “Cytherea” is derived from the island of Cythere (Tahiti) (Popenoe, 1979). Before being introduced in Jamaica, it was brought to Mauritius in 1768 (Airy Shaw and Forman, 1967; Morton, 1961). In 1915, this plant first fruited in the Philippines. Nowadays it is cultivated or grown on a small scale in Asia, Indonesia, Australia, Gabon, Cameroon, Cuba, Haiti, the Dominican Republic, Trinidad, Central America, Florida, Venezuela and Surinam (Pele and Le Berre, 1966; Morton, 1987; Backer and Bakhuisen, 1965; Popenoe, 1979). According to Airy Shaw and Forman (1967), it is very difficult to distinguish the exact area of indigenous occurrence. But in southeast tropical Asia, the genus Spondias exhibits the maximum diversification. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00005-8 © 2018 Elsevier Inc. All rights reserved.
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Exotic Fruits Reference Guide
BOTANICAL ASPECTS Taxonomy and Colloquial Names This plant belongs to the family of Anarcardiaceae (De Laroussilhe, 1980). In 1753, Linnaeaus established the genus Spondias L. The species S. cytherea was described by Sonnerat (Geurts et al., 1986; Airy Shaw and Forman, 1967). According to Campbell and Sauls (1994), no variety have been previously named and described. This species has been variously named: Condondum malaccense, Chrysomelon pomiferum, Evia amara, Evia dulcis, Spondias dulcis, Spondias macrocarpa and Spondias mangifera. But nowadays, only two names exist: S. dulcis Forst. and S. cytherea Sonn. (Airy Shaw and Forman, 1967; Ding Hou, 1978). S. cytherea or S. dulcis exhibit various colloquial names including some confusion with Spondias mombin (Hot plum). In Gabon and Cameroon where the tree is mostly found in Africa, it is called Cassemango. In Asia, we can have Ambarella, Pomme-cythe`re or Pommier de cythere, Hot plum and Mokak. In America it is called Caja-mango, Mango jobo, Juplan, Ambarella and Mazana de oro. In the South Pacific it is called Air, Kedongdong, Great hog plum, Dedongdong, Maradda, Ustubal, Aimemiek, Hevi, and Tahitian quince. In Caribbean and Indian Ocean, we have: Jew plum, Ciruela dulce and Prune de cythere (Winton and Winton, 1935; Popenoe, 1979; Morton, 1987; Geurts et al., 1986).
Description Golden apple is a hermaphroditic tree that can reach a height of 825 m and a trunk diameter of 2040 cm (Fig. 1). It is a straight tree with a cylindrical and highly branched trunk. The bark is smooth and light gray exhibiting a few lenticels and a yellowish sap (Ochse et al., 1961; Popenoe, 1979; Morton, 1987, Mitchell and Daly, 2015). The ornamental, deciduous and pinnate leaves exhibit 412 jugate, 1160 cm long and 915 cm long petiole. They are elliptic or obovateoglong leaflets 6.2510 cm long and composed of 925 glossy leaves. These leaves are very aromatic after being crushed. After the raining season, the leaves fall with a bright yellow color (Geurts et al., 1986; Morton, 1987; Mitchell and Daly, 2015). Fruits are gathered in bunches of a dozen and more. Two distinct types of fruits exist: the large type and the miniature or dwarf type (Mohammed et al., 2011). The fruits are oval and are 510 cm long with a thin hard skin. At maturity the fruit is green and turns to a golden-yellow color within ripening. A sooty mould can cover extensive areas on fruit skin (Popenoe, 1974; Mohammed et al., 2011). Fruits exhibit an average weight of 150240 g. The juicy flesh is
FIGURE 1 Young Ambarella tree bearing mature green fruits. Data from http://www.mi-aime-a-ou.com/Spondias_dulcis.php.
Ambarella—Spondias cytherea
17
FIGURE 2 Mature green and ripe golden apple fruits (A) and endocarp exhibiting irradiating spines (B). Data from (A) Morton, J., 1987. Ambarella. In Fruits of warm climates, ed. J.F. Morton, 240242. Miami, Floridaa and (B) Mitchell, J.D., Daly, D.C., 2015. A revision of Spondias L. (Anacardiaceae) in the Neotropics. PhytoKeys 55, 192.
fibrous and subacid with a terebenthin flavor. The seed shape looks like a virus because of the various fibers on it (Fig. 2). Due to the spiny projections of the fibers into the mesocarp, the flesh is hard to cut (Morton, 1987; Vivien and Faure, 1996).
HARVEST AND PRODUCTION The tree starts bearing fruits about 5 years after planting and continues fruiting up to 40 years or more. Depending on the time of flowering, the maturity stage begins from November to July and the fruit can be harvested any day and in any weather conditions (Fa’Anunu, 2009; Daulmerie, 1994). Harvesting can be processed when the fruit reaches the mature green stage. This means that the fruits ripe in some storage conditions. Golden apple is harvested using a pole and a bag. The fruit can be also harvested by hand but as the trees are very tall, there is no protection for the climber. After harvesting, the fruits are transported to the packhouse where they are washed, graded and stocked. When stored at ambient temperature, the fruits take 46 days to ripen but in a refrigerated room, the ripening can occur after 10 days. As this fruit is not commercially important, Ambarella can yield 300700 kg of fruits per tree depending on the age of this tree (Winsborrow, 1994; IICA, 1996). In Cameroon, the production can reach 20,000 tons per year (Temple, 1999). As for others fruits, the production is reduced by postharvest losses which can reach 50%. The major causes are a short period of high production associated with a high perishability of the fruit, pests, diseases, immature fruits and mechanical damage.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Fruit Development and Maturation On the tree of tropical fruits, after fruit-set, many physiological and biochemical modifications occur in the fruit. This is also the case of Ambarella fruit which exhibits various changes during development and maturity (Daulmerie, 1994; Youmbi et al., 2010; Mohammed et al., 2011; Guadarrama and Andrade, 2012; Emanuel and Benkeblia, 2012). Morphological parameters of golden apple fruit were studied. From 2 to 28 weeks after fruit-set, the length (670 mm), the diameter (6100 mm), the volume (1120 mL) and the weight (0120 g) of the ambarella fruit vary in a sigmoidal manner. During the development of the fruit, the chlorophyll a and b content of the peels also change. From 6 to 30 weeks after fruit-set, chlorophyll a content of the peels decreases from 2.75 to 0.93 μg/mg. That of chlorophyll b decreases from 1.05 to 0.23 (Youmbi et al., 2010). During the fruit development, the water (90.83%85.60%), minerals, lipids and proteins contents also decrease. However, as the fruit increases in size, the pH, total carbohydrates
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Exotic Fruits Reference Guide
(2.73%13.75 %), and vitamin C content increase (Youmbi et al., 2010; Graham et al., 2004). Graham et al. (2004) found that the harvest maturity (mature green) stage of the miniature golden apple fruit was attained at 1921 weeks after fruit-set. Color measurement indicated that these green mature fruits present a green (negative a* value) and a yellow (positive b* value) skin (Franquin et al., 2005). This stage is characterized by the constant weight of the fruit; 6468 g for dwarf type and 140224 g for the large type (Bauer et al., 1993; Graham et al., 2004; Franquin et al., 2005).
Fruit Ripening To reduce postharvest losses, golden apple fruits are harvested on the tree when they are mature green and presenting traces of green yellow on the skin. Once harvested, these fruits exhibit a respiratory pattern similar to that of climacteric fruits. During this process and depending on the period and the type of storage conditions, the fruit undergoes significant physiological and biochemical modifications. The fruit flesh changes color from white to yellow and the skin from green to yellow or orange (Graham et al., 2004; Ishak et al., 2005). This is due to the degradation of chlorophyll and synthesis of carotenoids or anthocyanin (Guadarrama and Andrade, 2012). These colors changes occur after the first 3 or 4 storage days which are characterized by the preclimateric stages (Graham et al., 2004). Climateric process of mature green ambarella fruit shows a rapid increase in respiration rate and ethylene production. Values of respiration rate and ethylene production increase with the temperature of storage, and the higher the temperature the earlier the peaking value. The highest values are obtained 68 days after storage. An important increase in these parameters are observed when the fruit is fully ripe and begins to overripe (Daulmerie, 1994; Graham et al., 2004). As for all tropical fruit, climacteric process of ambarella fruit is also characterized by textural changes. The fruit becomes soft. This softening process is due to the degradation of protopectin into pectin (Daulmerie, 1994; Ishak et al., 2005; Mohammed et al., 2011). This hydrolysis is due to the action of pectin methyl esterase and polygalacturonase enzymes (Guadarrama and Andrade, 2012). Table 1 illustrate the significant differences between the biochemical properties of golden apple at two ripening stages. During the climacteric process, the amino acid content of the fruit increases. Alanine, a precursor of ethylene, is the main amino acid produced. The synthesis of amino acids does not affect the protein content (Ishak et al., 2005). The production of CO2 and H2O is due to the breakdown of macromolecules. The degradation of carbohydrates as starch increases the monosaccharides contents, evidencing the sweet taste of the ripening fruit (Daulmerie et al., 1994). The phenolic compounds decrease is a result of the synthesis of volatiles compounds which characterized the flavor of the fruit (Ishak et al., 2005; Mohammed et al., 2011). This is caused by the variation of the main volatiles compounds (1,8-cineole, α-pinene, β-pinene, terpinolene and limonene) contents from the green to the ripe stage of the fruit (Jirovetz et al., 1999). From the partial ripe to a fully ripe stage, the organic acid content of the ripening fruit also decreases. Since carotenoids are synthesized during ripening, the lipids content of the fruit should also increase (Ishak et al., 2005).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE OF THE FRUIT Table 1 shows that Golden apple fruit is very poor in dry matter as the other exotic fruits (Favier et al., 1993, Leterme, 2006). Vitamins C and A are the main vitamins found in the pulp of ripe ambarella fruit. This value is higher than that found in mango pulp, but the latter exhibits higher value of vitamin A content (Favier et al., 1993). This high value of vitamin C suggests a high value of titratable acidity. Golden apple fruit also exhibits a high pH value (3.874.05) compared to most of the other tropical fruits. However, the fruit peel exhibits a lower pH value than the pulp. This is due to the presence of an acidic layer between the peel and the endocarp. As most of the tropical fruits, Ambarella fruit is poor in lipid and protein (Table 1). Carbohydrates represent more than 50% of the major molecules of the pulp. Monosaccharides such as fructose, glucose, and mannose are the major individual sugars found in the golden apple fruit pulp (Favier et al., 1993). Others carbohydrates found in this fruit are fibers. Spondias fruit contains an important amount of pectin (2.13%). This is why this fruit shows a good suitability for processing into jam (Koubala et al., 2012). S. cytherea fruit is more rich in ash than the other edible Anacardiaceae fruit (mango, Yellow mombin and cashew) (Leterme, 2006). Potassium, phosphorus, and calcium are the main minerals. Phenolic compounds constitute the other microelements found in the fruits (338 mg/100 g). Their metabolism yields volatiles molecules which characterize the aroma of the fruit. These are ethyl(S)(1) 2-methyl butyrate, ethyl isovalerate, ethyl propionate, ethyl butyrate, linalol, and trans-pinocarveol (Fraga and Rezende, 2001; Jirovetz et al., 1999).
Ambarella—Spondias cytherea
TABLE 1 Biochemical and Physicochemical Composition of Mature Green and Ripe Golden Apple (Spondias cytherea) Fruit Pulp and Peels Characteristics Compounds Macroelements
Unit Energy
Kcal/100 g
Moisture
g/100 g
Favier et al. (1993). Leung et al. (1972). Ishak et al. (2005). d Franquin et al. (2005). e Youmbi et al. (2010). f Koubala (2008). g Koubala et al. (2013). h Lago-Vanzela et al. (2011). i Graham et al. (2004). j Koubala et al. (2008). b c
Pulp
Pulp
Ripe Peels a,b
44.046 79.690.5c,d,e
0.100.53
0.85h
Protein
g/100 g
0.641.76c,d,e
0.40 2.33a,c
1.47h
Carbohydrates
g/100 g
12.313.75e,i
11.017.5a,i
21.4745.0f,g,h
Starch
g/100 g
7.1d
Ash
g/100 g
0.56.78c,d
0.396.23c,b,h
0.860.98f,g,h
2.603.59c,d,f
3.874.05c,f
2.222.78j,f,h
0.821.3c,d,i
0.81c
0.85h
2.13
2.494.05j,g,h
0.96f
10.8f
5.1f
20.8j
g/100 g
0.43f
5.54j
Galactose
g/100 g
0.23f
3.31j
Fructose
g/100 g
Mannose
g/100 g
Pectin
g/100 g
Uronic acid
g/100 g
Glucose
g/100 g
Arabinose
c
a,c
73.44f,g
0.070.34
g/100 g
c,e
87.290.0a,c
g/100 g
Titratable acidity
a
Ripe
Fat
pH
Microelements
Mature green
c
1.56
1.2d
1.5d
3.10f 0.26f c,d
2.18j a,c,h
Fibers
g/100 g
2.02.4
1.01.7
Phenolics
mg/100 g
350686c,d
338c
Sodium
mg/100 g
4.36c
1.04.14a,c,b
Calcium
mg/100 g
13.5032.76c,e
35.0556.00a,c,b
Potassium
mg/100 g
125e
93.095.0a,b
Iron
mg/100 g
Phosphorus
mg/100 g
0.3a,b 18e
65.067a,b c
Zinc
mg/100 g
0.25
0.24c
Magnesium
mg/100 g
4.511.76c,e
10.34c
Carotenoids
μg/100 g
Ascorbate
mg/100 g
Thiamin
mg/100 g
0.05a,b
Riboflavin
mg/100 g
0.02a,b
Niacin
mg/100 g
1.4a,b
Folates
μg/100 g
7.0a
200.0205.0a,b 5.552.0c,d
5.8635.0a,c,b
18.5f
19
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Exotic Fruits Reference Guide
Golden apple fruit is one of the most appreciated exotic fruits. The high consumption of the fruit is due to its delicious and sweet-smelling characteristics (Jirovetz et al., 1999). One hundred grams of the edible portion of this fruit can yield about 45 kcalories (Leung et al., 1972; Favier et al., 1993). This fruit can cover dietary needs of vitamin C and minerals. Besides its important quantity of vitamin C and phenolics, the pulp can be a good source of natural antioxidants that prevent diseases caused by oxidative stress (Fu et al., 2011). Morton (1961) noted that the consumption of fresh golden apple fruit is useful against cardiovascular diseases, ingestion and haemorrhoids. Ambarella fruit exhibits high fiber content. It has been shown that pectic polysaccharides from S. cytherea fruit pulp can activate peritoneal macrophage and therefore be important for the healing process after injuries (Iacomini et al., 2005).
SENSORY CHARACTERISTICS OF THE FRUIT Ripe ambarrella fruit exhibits a yellow or bright orange color which is more attractive. This fruit is called golden apple because of this color and its shape similar to that of an apple. The skin of golden apple fruit is slightly rough (Popenoe, 1979). According to Jirovetz et al. (1999), the high characteristic odor of this fruit can be correlated to minor alcohols and esters, monoterpenes, hexane derivatives, and fatty acids. It is a fibrous and fleshy fruit, exhibiting a sour aroma and flavor (Popenoe, 1979). Cassemango fruit pulp is very sweet and slightly acid. According to a survey conducted on the consumer usage of golden apple fruit, about 99% of the consumers said that they liked this fruit. However, concerning the form in which the preferred consume this fruit, only 23% of them preferred eating it fresh and 53% as pickled, salted, and peppered (Browne and Bradie, 2006).
CONSERVATION Fruits preservation or processing reduces the postharvest losses recorded during the overproduction period. The life expectancy of the fruit is prolonged and they can be available all year. The transformation of fruits allows us to obtain products with high added value. The transformation of fruits and vegetables bypasses the fluctuations and offers employment opportunities (Martine, 1993; Dury et al., 1999). As with most of the tropical fruits, cassemango fruits are naturally preserved or transformed into various products. For commercial purposes, golden apple fruits are harvested at the full mature stage. They are then cleansed and treated with an antimicrobial solution before being kept in refrigerated room (1020 C) to slow down the ripening process. Fruits can be stored up to 1014 days before sale (Daulmerie, 1994; Graham et al., 2004). Most of the households store unpeeled golden apple fruit in the refrigerator (510 C) for a maximum of 18 days. The mature or ripe fresh-cut peeled fruit is processed into juice or frozen for 8 months before being cooked in curry (Morton, 1961; Mohammed et al., 2011). In addition to these conservation process, household also prepared jam or jellies from the ripe peeled fruit. Ambarella fruit pulp exhibits a better suitability for jam processing than that of mango fruit (Koubala et al., 2012). For commercial purposes, the pulp of the fruit is used for making jelly, jams, pickles, chutney, alcoholic beverages, relishes soups, stews, nectars and juices. The pulp is also dried or canned in sucrose (Ramsundar et al., 2002; Morton, 1987; Campbell et Sauls, 1994; Mohammed et al., 2011).
APPLICATION The pulp and the peel of S. cytherea fruit presents numerous applications. The juice of this fruit is used to improve the sensorial and physichochemical properties of yoghurt (Bartoo et al., 2005). In India, the pulp is used as food additive in the preparation of sauces (Katerson and Bradie, 2002). Because of its high flavor characteristic, it has been used in wine processing (Khan et al., 1998). According to Iacomini et al. (2005), pectic polysaccharides from S. cytherea fruit pulp can be used in the healing process after injuries by activating peritoneal macrophage. It has been shown that the peels of cassemango fruit can be an alternative source of pectin and fibers (Koubala et al., 2008, 2013). Using an oxalic acid/ammonium oxalate solution, pectin is extracted from ripe peels with a yield of 14% (dried peel) compared to the commercial lime peel exhibiting 23% (Koubala et al., 2008). Pectin from ambarella fruit peel showed better rheological properties compared to commercial lime pectin (Koubala et al., 2009). The use of ambarella pectin in fruit processing increases (three- to sixfold) the viscoelastic strength of the prepared jams (Koubala et al., 2012). Golden apple fruit peels fibers are rich sources of fiber (85% dried weight). Their good swollen volume and water absorption capacity could lead to satisfactory functionality as a dietary ingredient in food products (Koubala et al., 2013).
Ambarella—Spondias cytherea
21
ACKNOWLEDGMENT We are grateful to the “Fruits et Le´gumes” programme of IRAD (Yaounde, Cameroon) for providing us all information available on S. cytherea. We are also very grateful to the National Institute for Agricultural Research of Nantes (France) for providing reference publications on Ambarella.
REFERENCES Airy Shaw, H.K., Forman, L.L., 1967. The genus Spondias L. (Anacardiaceae) in tropicalAsia. Kew Bull. 21, 119. Bauer, T., Kim, J., Baldeo, I., 1993. A Preliminary Study on the Golden Apple (Spondias dulcis) Production and Marketing in Grenada. Inter-American Institute for Cooperation on Agriculture, Grenada, 21p. Backer, C., Bakhuisen, Van den Brink, R.C., 1965. Flora of Java, vol. 2. NVP Noordholf, Groningen, pp. 150151. Bartoo, A., Shelly, Badrie, N., Neela, 2005. Physicochemical, nutritional and sensory quality of stirred ‘dwarf’ golden apple (Spondias cytherea Sonn) yoghurts. Inter. J. Food Sci. Nutr. 56 (6), 445454. Browne, J., Badrie, N., 2006. Effects of pre-treatments on the physicochemical quality and sensory acceptance of osmo-air-dehydrated ‘dwarf’ golden apples (Spondias cytherea Sonn.). J. Food Agric. Environ. 4 (1), 1116. Campbell, C.W., Sauls, J.W., 1994. Spondias in Florida. Horticultural sciences Department, Institute of food and Agricultural Sciences University of Florida, Sheet HS-63, 3p. Daulmerie, S., 1994. Investigations on Golden apple (Spondias cytherea) Production with Particular Reference to Post-harvest Technology and Processing. Miscellaneous Publications Series, Port of spain, Trinida & Tabago, 112 p. De Laroussilhe, F., 1980. Le Manguier. Techniques Agricoles et productions tropicales, e´d. G.P. Maisonneuve & Larose Paris, 312 p. Hou, D., 1978. Anarcadiaceae. Flora Malesiana, Ser. I, vol. 8: 479483. Dury, S., Essomba, J.-M., Dissake, H.-C., et Bricas, N., 1999. La consommation des produits alimentaires des PME: le cas des jus de fruits au Cameroun. CIRAD-AMIS / IITA, 15 p. Emanuel, M.A., Benkeblia, N., 2012. Variation of Color, Reducing and Total Sugars, Total Phenolics and Chlorophylls in june plum (Spondias dulcis) during “On Tree” Ripening Stages. Acta Horticul. 894, 243246. Fa’Anunu, H.‘O., 2009. Final Report on the Application for Market Access of Polynesian Plum (Spondias dulcis) from Fiji, Vanuatu, Samoa. FAO, Cook Islands and Tonga to New Zealand, 41 p. Favier, J.-C., Ireland-Ripeit, J., Laussuc, C., et Feinberg, M., 1993. Table de composition des fruits exotiques, fruits de cueillette d’Afrique, Dans Re´pertoire ge´ne´rale des alimentsTome. third ed. ORSTOM, INRA, pp. 5559. et 171. Paris : Technique & Documentation. Fraga, S.R.G., Rezende, C.M., 2001. The aroma of Brazilian ambarella fruit (Spondias cytherea Sonnerat). J. Essential Oil Res. 13, 252255. Franquin, S., Marcelin, O., Aurore, G., Reynes, M., Brillouet, J.-M., 2005. Physicochemical characterisation of the mature-green Golden apple (Spondias cytherea Sonnerat). Fruits. 60, 203210. Fu, L., Xu, B.T., Xu, X.R., Gan, R.-Y., Zhang, Y., Xia, E.-Q., et al., 2011. Antioxidant capacities and total phenolic contents of 62 fruits. Food. Chem. 129, 345350. Geurts, F., Blaak, G., El Baradj, T., 1986. Spondias cytherea. Genetic Resources of Tropical and Subtropical Fruits and Nuts (excludingMusa). International Board for Plant Genetic Resources, Rome, pp. 1819. Graham, O.S., Wickham, L.D., Mohammed, M., 2004. Growth, development and quality attributes of miniature golden apple fruit (Spondias cytherea). Part II: Physicochemical and organoleptic attributes associated with ripening. Food Agric. Environ. 2 (1), 101106. ´ ., Andrade, S., 2012. Physical, Chemical and Biochemical Changes of Sweetsop (Annona squamosa L.) and Golden Apple (Spondias Guadarrama, A cytherea Sonner) Fruits during Ripening. J. Agric. Sci. Technol. B. 2, 11481157. Iacomini, M., Serrato, R.V., Sassaki, G.L., Lopes, L., Buche, D.F., Gorin, P.A.J., 2005. Isolation and partial characterization of a pectic polysaccharide from the fruit pulp of Spondias cytherea and its effect on peritoneal macrophage activation. Fitoterapia. 76, 676683. IICA (Inter-American Institute for Cooperation on Agriculture), 1996. Third Regional Workshop on Tropical Fruits. Port of Spain, Trinidad and Tobago. 1993p. Ishak, S.A., Ismail, N., Noor, M.A.M., Ahmad, H., 2005. Some physical and chemical properties of ambarella (Spondias cytherea Sonn.) at three different stages of maturity. J. Food Compos. Anal. 18, 819827. Jirovetz, L., Buchbauer, G., Ngassoum, M.B., 1999. Analysis of the aroma compounds of the fruit extracts of Spondias cytherea (“ambarella”) from Cameroon. Zeitschrift fu¨r Lebensmitteluntersuchung und -Forschung A. 208, 7476. Katerson, A., Badrie, N., 2002. Sensory and physicochemical quality of ‘Reduce Sodium’ hot sauces from dwarf golden apples (Spondias cytherea): Effects of brining and debrining. J. Food. Sci. 67 (9), 34763483. Khan, K., Mohammed, M., Bradie, N., 1998. The utilization of pomme cythere (Spondias cytherea) or golden apple (Spondias cytherea, Sonn.) in the production of dry wine. Trop. Fruits Newsletter. 29, 1517. Koubala, B.B., Mbome, L.I., Kansci, G., Mbiapo, T.F., Crepeau, M.-J., Thibault, J.-F., et al., 2008. Physicochemical properties of pectins from ambarella peels (Spondias cytherea) obtained using different extraction conditions. Food. Chem. 106, 12021207. Koubala, B.B., Kansci, G., Garnier, C., Mbome, L.I., Durand, S., Thibault, J.-F., et al., 2009. Rheological and high gelling properties of mango (Mangifera indica) and ambarella (Spondias cytherea) peel pectins. J. Food Sci. Technol. 44 (9), 18091817.
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Exotic Fruits Reference Guide
Koubala, B.B., Kansci, G., Garnier, C., Ralet, M.-C., 2012. Mango (Mangifera indica) and ambarella (Spondias cytherea) peel extracted pectins improve viscoelastic properties of derived jams. Afr. J. Food Agric. Nutr. Develop. 12 (3), 62006212. Koubala, B.B., Kansci, G., Garnier, C., Thibault, J.-F., Ralet, M.-C., 2013. Physicochemical properties of dietary fibres prepared from ambarella (Spondias cytherea) and mango (Mangifera indica) peels. Food Bioproc. Technol. 6 (2), 591597. Lago-Vanzela, E.S., Ramin, P., Umsza-Guez, M.A., Santos, G.V., Gomes, E., Da Silva, R., 2011. Chemical and sensory characteristics of pulp and peel ‘caja´-manga’ (Spondias cytherea Sonn.) jelly. Cieˆnc. Tecnol. Aliment. 31 (2), 398405. Leterme, P., Buldgen, A., Estrada, F., London˜o, A.M., 2006. Mineral content of tropical fruits and unconventional foods of the Andes and the rain forest of Colombia. Food. Chem. 95, 644652. Leung, W.T.W., Buthum, R.R., Chang, F.H., 1972. Food Composition Tables for Use in East Asia, Part1. National Institutes of Health, Bethesda, Maryland. Martine, F., 1993. Transformer les fruits tropicaux. Le Point sur les technologies. Editeurs GRET, CTA, ACCT, Ministe`re de la Coope´ration Franc¸aise, Paris, 220 p. Mitchell, J.D., Daly, D.C., 2015. A revision of Spondias L. (Anacardiaceae) in the Neotropics. PhytoKeys. 55, 192. Mohammed, M., Hajar Ahmad, S., Abu Bakar, R., Lee Abdullah, T., 2011. Golden apple (Spondias dulcis Forst. syn. Spondias cytherea Sonn.). In: Yahia, E.M. (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruits, vol. 3. Woodhead Publishing Limited, Sawston, Cambridge, pp. 159178. Morton, J.F., 1961. Why no use and improve the fruitful ambarella. Hort. Adv. 5, 1316. Morton, J., 1987. Ambarella. In: Morton, J.F. (Ed.), Fruits of Warm Climates. Florida, Miami, pp. 240242. Ochse, J.J., Soule Jr., M.J., Djikman, M.J., Wehlburg, C., 1961. Tropical and Subtropical Agriculture (English edition of Indiche Groenten 1931), vol. 1. Macmillan, New York, 527548. Pele, J., et Le Berre, S., 1966. Les aliments d’origine ve´ge´tale au Cameroun. ORSTOM, 34 p. Popenoe, W., 1974. Manual of Tropical and Subtropical Fruits.. Hafner Press, New York, pp. 155157. Popenoe, J., 1979. The genus Spondias in Florida. Proc. Florida State Horticul. Soc. 92, 277279. Ramsundar, D., Comissiong, E., Badrie, N., Baccus-Taylor, G.S.H., Spence, J., 2002. Processing and quality evaluation of whole canned ‘dwarf’ golden apples (Spondias cytherea). J. Food. Qual. 25, 1325. Temple, L., 1999. Le marche´ des fruits et le´gumes au Cameroun. Bulletin technique. CIRAD-IRAD, Yaounde´, Cameroun, 163 p. Vivien, J., et Faure, J.-J., 1996. In: Nguila-Kerou, Clohars Carnoet (Eds.), Fruitiers sauvages d’Afrique, espe`ces du Cameroun. CTA, France, pp. 3538. Winsborrow, C., 1994. Golden apple production. Third Regional Workshop on Tropical Fruits. Miscellaneous Publications, Grenada, pp. 113116. Winton, L.A., Winton, K.B., 1935. The Structure and Composition of Foods, vol. 2. John Wiley, London, pp. 733734. Youmbi, E., Zemboudem, M.N., Tonfack, L.B., 2010. Changements morphologiques et biochimiques au cours du de´veloppement et de la maturation des fruits de Spondias cytherea Sonn. (Anacardiaceae). Fruits. 65, 285292.
Annatto/Urucum—Bixa orellana Paulo C. Stringheta1, Pollyanna I. Silva2 and Andre´ G.V. Costa2 1
Federal University of Vic¸osa, Vic¸osa, Minas Gerais, Brazil, 2Federal University of Espı´rito Santo, Alegre, Espı´rito Santo, Brazil
Chapter Outline Cultivation Origin and Botanical Aspects Harvest and Postharvest Conservation Harvest Postharvest Estimated Production and Trade of Annatto Chemical Composition of Annatto
23 23 23 24 24 25
Biosynthesis of Annatto Compounds Biological Activities of Annatto Compounds Industrial Application and Potential Industrial Application References Further Reading
26 26 27 28 30
CULTIVATION ORIGIN AND BOTANICAL ASPECTS Bixa orellana L. is a species belonging to the Angiospermae subdivision, Dicotiledoneae class, Parietales order, Cristianeae suborder, Bixaceae family, and bixa genus (Ramalho et al., 1987). Although originally from tropical America (Smith et al., 1992; Stringheta and Silva, 2008), this species is cultivated in the tropics around the world (Ramalho et al., 1987). In Brazil, it has been identified as a native plant of the northern and northeastern states, mainly Amazonas, Para, Paraiba, Piaui, Maranhao, Ceara, and Bahia (Smith et al., 1992; Baliane, 1984). It is a small tree, usually less than 6 m, reaching up to 8 m, with diameter of 1520 cm at the stem base, wide copse and abundantly branched (Cruz et al., 2008). The fruits are ovoid and flattened capsules, oval, hemispherical ellipsoid or conical, containing numerous seeds, surrounded by a reddish pulp. The capsules open in two equal parts and their colors range from dark brown or reddish to green or pale yellow, according to plant variety (Costa et al., 2008). They are densely covered by flexible spines and have on average 54 seeds containing pigment. Fruiting occurs throughout the year, with a sharp increase in winter. The fruits ripen in late summer and early fall. Fruiting starts in the second year and the products are marketable by the third year. The seeds per fruit can be numerous. They are angular, 34 mm long, covered by a yellowish red resinous substance, which becomes dry, hard and dark upon maturation (Fig. 1). Bixin is the pigment present in higher concentration in the seeds, representing over 80% of total carotenoids (Stringheta and Silva, 2008; Costa et al., 2008).
HARVEST AND POSTHARVEST CONSERVATION Harvest Harvesting is done manually when the capsules are dry at the ends of the branches. Pruning shears are used to cut branches and also remove inflorescence containing 1520 capsular fruits. Once harvested, the fruit are carried in baskets to a land or a warehouse where, after drying, they will be processed in specific equipments or manually. The machines separate the capsules from the seeds and classify them for subsequent packing in polyethylene bags, where they remain preserved for more than five years in perfect condition without any plant protection treatment (Cruz et al., 2008).
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00006-X © 2018 Elsevier Inc. All rights reserved.
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Exotic Fruits Reference Guide
FIGURE 1 Annatto seeds.
Postharvest Harvesting of fruit in the field Harvesting of fruits in the field depends on the amount of product, climate and buyer’s requirement. There is an alternative of leaving the harvested fruits in the lanes among the plants for a few days, depending on the local pluvial conditions. One can also directly harvest in baskets or bags and then store in an appropriate location (Cruz et al., 2008; Franco et al., 2002). Predrying of fruits The annatto seeds can be either dried in artificial dryers or by natural means, such as sun drying. The main purpose of this step is to promote the lowering of the moisture content of the fruit, so that they can be kept for longer periods and to facilitate the subsequent operation of withdrawal of seeds from the capsules. Withdrawal of seeds from the capsules Withdrawal of seeds from the capsules can be done manually or mechanically by means of specific equipment that undertakes mechanical separation of the seeds and foreign material. These machines separate the capsules from the seeds and they can classify the seeds based on standards (Cruz et al., 2008). Sieving Sieving can be done either manually or mechanically. There are some machines that are coupled with sieves and therefore perform sieving after the withdrawal of seeds from the capsules. This is an operation that must be carried out carefully, because due to friction, there may be loss of bixin from the seeds. Drying of seeds Drying of the seeds is another operation which can be done either by natural or artificial means. Natural drying is carried out in terraces, with seeds exposed to the sun and the environment. Artificial drying is one where dryers that use temperature and air flow are utilized. Drying should be done in the shortest possible time and with the least possible use of heat (in the case of artificial dryers), as heavy losses in the dye content of seeds may occur (Cruz et al., 2008). Storage of seeds The seeds can be stored in clean 50 kg polyethylene or polypropylene bags (Cruz et al., 2008; Franco et al., 2002). Furthermore, they should be kept in clean places, airy and under light without the presence of pests. The moisture content ideal for good storage is up to 14%.
ESTIMATED PRODUCTION AND TRADE OF ANNATTO Annatto is one of the most consumed natural dyes worldwide. The majority of the production of the annatto seeds comes from Latin America, followed by Africa and Asia. Peru is the main producer and exporter in the world. However, Kenya has its production dedicated to Japan, while Brazil produces for local consumption (Albuquerque and Meireles, 2011; Green, 1995). According to the FAO, by the end of the 1990s, the harvested quantity of annatto seeds was estimated to be 14,500 tons and about 7500 tons were used as dye in the world. The remaining 7000 tons were consumed mainly in Brazil, Peru, and Ecuador (Albuquerque and Meireles, 2011). In 2009, the cultivated area of annatto seeds occupied 11,707 ha and its production reached 12,472 tons. The main producing regions were the north, northeast, and southeast of Brazil (Albuquerque and Meireles, 2011). Seed is the main form of exporting annatto, although to increase export values, several suppliers now also carry out partial processing of annatto seeds into concentrates, pastes, or colorants (Smith and Wallin, 2006). The main forms of commerce are water soluble and oil soluble extracts. Oil soluble extracts can be sold in the dried state or as ready-to-use solutions/suspensions in edible vegetable oils. Solid products may contain up to 99% bixin and vegetable oil solutions may
Annatto/Urucum—Bixa orellana
25
be more diluted (Green, 1995). The water soluble forms are imported basically as aqueous pastes or dried or spray-dried products. Water solutions usually contain a minimum of 0.1% pigment (Green, 1995). The main market for annatto is the USA and North America, Western Europe and Japan, although there is also considerable inter-trade (in seeds) between the Central and South American suppliers (Smith and Wallin, 2006). The market trend in developed countries has been a progressive increase in imports of extracts and for more stringent quality requirements (bixin content) of imported seeds.
CHEMICAL COMPOSITION OF ANNATTO Bixin [6ʹ-methyl hydrogen (9ʹZ)-cis-6,6ʹ-diapocarotene-6,6ʹ-dioate] (Shahid-ul-Islam et al., 2015) is a diapocarotenoid, mainly present in annatto seeds, accounting for at least 80% of total carotenoids present in the seed (Shahid-ul-Islam et al., 2014). It is the pigment present in “colorau”, a spice used in South America, and in fat soluble preparation of annatto, while norbixin and its salt are the major pigments for water-soluble preparation of annatto (Stringheta et al., 2008). Bixin is the methyl ester of dicarboxylic acid norbixin (Scotter, 2009). It is soluble in concentrated alkaline solutions, where it undergoes saponification, forming a norbixin salt. This salt when in acidic media forms dicarboxylic acid norbixin (Silva and Stringheta, 2008) (Fig. 2). Studies with the objective of isolating and identifying carotenoids
FIGURE 2 Structural formulas of bixin, norbixin and norbixin salt.
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Exotic Fruits Reference Guide
and other compounds have been conducted on both the seeds and other parts of the plant, and were recently reviewed (Shahid-ul-Islam et al., 2015). Crude seeds of annatto present 4045% cellulose, 3.55.5% sugar, 0.30.9% essential oil, 3% lipids, 14.5 % pigment, 1116% protein, fixed mineral residue in the range of 5%, alpha and beta carotene, tannins, and saponins (Albuquerque and Meireles, 2011; Vale´rio et al., 2015; Oliveira, 2005). Minor carotenoids have been identified in the annatto seed, such as beta carotene, cryptoxanthin, lutein, zeaxanthin, methyl bixin, methyl-9ʹZ-apo-6ʹ-lycopenoate, besides phytoene, ε-carotene, and neurosporene (Tirimanna, 1981; Jondiko and Pattenden, 1989; Mercadante et al., 1996; Mercadante et al., 1997b), dimethyl (9Z, 9ʹZ)-6,6ʹ-diapocarotene-6,6ʹ-dioate, methyl (9Z)-10ʹ-oxo-6,10ʹ-diapocaroten-6-oate, methyl (9Z)-6ʹ-oxo-6,5ʹ-diapocaroten-6-oate and methyl (4Z)-4,8-dimethyl-12-oxododecyl-2,4,6,8,10-pentaenoate and methyl (9Z)-8ʹ-oxo-6,8ʹ-diapocaroten-6-oate (Mercadante et al., 1997a). In addition, three other minor carotenoids were isolated from the annatto seeds, which were: 6geranylgeranyl 8ʹ-methyl-6,8ʹ-diapocarotene-6,8ʹ-dioate, 6-geranylgeranyl 6ʹ-methyl (9ʹZ)-6,6ʹ-diapocarotene-6,6ʹ-dioate and 6-geranylgeranyl,6ʹ-methyl-6,6ʹ-diapocarotene-6,6ʹdioate (Mercadante et al., 1999). In addition to carotenoids, the presence of terpenes and terpenoid compounds is reported. An example would be the C-20 alcohol terpene all-geranylgeraniol (Jondiko and Pattenden, 1989). Other compounds of this class found were farnesylacetone, geranylgeranyl octadecanoate, geranylgeranylformate, and some sesquiterpenes (Shahid-ul-Islam et al., 2015; Jondiko and Pattenden, 1989). Compounds of another nature such as organic acids, phenols, and phenolic compounds as ellagic acid, luteolin, and apigenin were found in the roots and leaves of annatto (Shahid-ul-Islam et al., 2015). There is also the presence of volatile compounds in the oil seeds, such as (Z, E)-farnezyl acetate and ishwarane (Pino and Correa, 2003).
BIOSYNTHESIS OF ANNATTO COMPOUNDS It is suggested that a carotenoid containing 40 carbon atoms, most likely lycopene, is a precursor of bixin (Siva et al., 2010; Bouvier et al., 2003). Bixin biosynthesis reaction may involve the action of a dioxygenase, an aldehyde dehydrogenase and a methyltransferase in a series of reactions proceeding sequentially from lycopene (Bouvier et al., 2003). In the bixin biosynthesis pathway there is a condensation reaction of two molecules of geranyl geranyl pyrophosphate (GGPP) to yield phytoene with an intermediate product of feranyl feranyl pyrophosphate (FFPP). Phytoene is converted into lycopene and finally bixin is synthesized in Bixa by three enzymes: lycopene cleavage dioxygenase, bixin aldehyde dehydrogenase, and carboxyl methyl transferase (Stringheta et al., 2008; Siva et al., 2010). Fig. 3 shows a simplified scheme of bixin biosynthesis pathway. Three genes from Bixa orellana govern bixin biosynthesis. These genes code for lycopene cleavage dioxygenase, bixin aldehyde dehydrogenase, and norbixin carboxyl methyltransferase.Siva et al. (2010) functionally characterized and identified that bixin coding genes are not only present in Bixa, but also in Crocus and Vitis, reporting that this could be an alternative and competitive source for natural bixin production. Regarding genes that govern biosynthesis of bixin, Bouvier et al. (2003) introduced three genes that catalyze the sequential conversion of lycopene into bixin in Escherichia coli engineered to produce lycopene induced bixin synthesis. These discoveries can expand the availability of this economically important plant product.
BIOLOGICAL ACTIVITIES OF ANNATTO COMPOUNDS Several investigations have been reported on the biological activities of annatto such as antioxidant and free radical scavenging activities (Barcelos et al., 2012), antiinflammatory activity (Giriwono et al., 2013), anticarcinogenic activity (Pierpaoli et al., 2013; Shibata et al., 2008; Matuo et al., 2013; Reddy et al., 2005), antibacterial and antifungal activities, enhanced gastrointestinal motility, and europharmacological and anticonvulsant activities (Roehrs et al., 2014; Vilar et al., 2014). In general, the biological activities were due to the concentration of carotenoids, apocarotenoids, terpenes, terpenoids, sterols, and aliphatic compounds found in all parts of this plant, such as leaf, root, seed, shoot, and even the whole plant (Vilar et al., 2014). In a study with Wistar rats on dietary supplementation with geranylgeraniol (48.3 mg/kg), an isoprenoid with antiinflammatory effect extracted from annatto was effective in suppressing LPS-induced inflammation and liver damage, respectively, due to the lower levels of plasma inflammatory cytokines (tumor necrosis factor: TNF-a; interleukins: IL1b and IL-6) and lower levels of alanine and aspartate aminotransferases (ALT and AST) (Giriwono et al., 2013). Another study with rats showed a protective effect of bixin and norbixin against the adverse effects of methylmercury
Annatto/Urucum—Bixa orellana
27
FIGURE 3 Biosynthesis route of bixin. Abbreviations: BiADH, bixin aldehyde dehydrogenase; Crt1SO, carotenoid isomerase; GGPP, geranyl geranyl diphosphate; LCD, lycopene cleavage (di)oxygenase; nBMT, norbixin methyltransferase; PSY, phytoene syntase; PDS, phytoene desaturase (Stringheta et al., 2008; Giuliano et al., 2003).
(Barcelos et al., 2012). These authors found a moderate increase in glutathione and suggested that consumption of bixin and norbixin may protect humans against the adverse health effects caused by exposure to organic mercury. Regarding antitumor effects, Pierpaoli et al. (2013) reported that the effect of dietary supplementation with tocotrienols from annatto (90% δ-T3 and 10% γ-T3) might be related to the induction of oxidative stress, senescent-like growth arrest and apoptosis in HER-2/neu overexpressing mammary tumors and in tumor cells. Shibata et al. (2008) demonstrated that δ-T3 even at low concentrations inhibits tumor angiogenesis. On the other hand, Matuo et al. (2013) investigated the effects of bixin and norbixin on gene expression of cytochrome P450 isoforms in human hepatoma cells. Cytochrome P450 plays a dominant role in phase I biotransformation, being responsible for the activation/detoxification of a large number of exogenous chemicals, including drugs and carcinogenic compounds. The authors concluded that the inducer potential of cytochrome P450 isoforms of annatto could be attributed to bixin, but not to norbixin. Additionally, Reddy et al. (2005) suggest that the main effective compound was thought to be bixin. Shahid-ul-Islam et al. (2015) in a review reported that annatto extracts exhibit biological activity compared to standard drugs, suggesting that studies should be developed in this area. On the other hand, the studies utilize different doses of the compounds, which hinder comparison (Vilar et al., 2014). In two recent reviews on the implementation of annatto in biological assays (Shahid-ul-Islam et al., 2015; Vilar et al., 2014), a large number of in vitro studies was observed. However, few studies have investigated the effects of annatto or its components in human clinical trials. Further studies should be conducted in order to verify the effects of annatto components, especially bixin and norbixin and the mechanisms involved. Moreover, clinical trials should be encouraged in order to elucidate the effects of these compounds.
INDUSTRIAL APPLICATION AND POTENTIAL INDUSTRIAL APPLICATION Annatto (E-160B) is a natural yelloworange dye obtained from the plant Bixa orellana, which causes less toxicity and generally exhibits better biodegradability and compatibility with the environment, when compared with synthetic
28
Exotic Fruits Reference Guide
colorants (Shahid-ul-Islam et al., 2014). Annatto colorants are used in several ways, extensively in food industry, particularly in dairy (Barcelos et al., 2012; Giriwono et al., 2013; Pierpaoli et al., 2013) and meat products (Shibata et al., 2008; Matuo et al., 2013). Annatto preparations are also used in makeup products and in textile industries (Shahid-ulIslam et al., 2014; Reddy et al., 2005; Roehrs et al., 2014). Nowadays, in the food industry, annatto pigments are used mainly in cheese (Vilar et al., 2014), dairy products (Kang et al., 2010), cereal-derived products, sweets, beverages, sauces, and sausages (Galindo-Cuspinera et al., 2003), representing almost the totality of annatto market. The lipid soluble pigments are used in products like margarines, vegetable creams, cheese, and icecream, among others (GalindoCuspinera et al., 2003; Prabhakara Rao et al., 2005; Zarringhalami et al., 2009). The mixture of annatto colorants with other natural colorants increases their applications in foods, for the possibility of producting various color shades. Red coloration can be obtained when annatto is mixed with carmine, beet, or anthocyanins. The dark coloration is obtained when annatto and chlorophyll are mixed (Costa et al., 2008). Mixtures such as annatto/carmine, annatto/curcumin and annatto/caramel are common in the food industry. Annatto pigments also can be used in medicines (liquids and solids) (Albuquerque and Meireles, 2011; Galindo-Cuspinera et al., 2003). In addition to the vast use as a colorant in the food industry, annatto pigment, in its various forms, can be used as an antioxidant (Matuo et al., 2013), acting in the prevention of lipid peroxidation in food (Figueiredo et al., 2014), autoxidation (Gulrajani et al., 1999) and acting against reactive oxygen and nitrogen species (Giridhar et al., 2014). They also have antimicrobial activity (Giriwono et al., 2013; Smith et al., 2014). In animal feed it has been used in poultry feed composition (Galindo-Cuspinera et al., 2003) and to improve the coloration of egg yolk. Some patents have been registered regarding the development of new technologies for obtaining annatto seed products and processing. For example, degreased and solvent-free seeds rich in dye content, obtaining annatto oil fractions rich in δ-tocotrienol (Parvin et al., 2011), processes using supercritical CO2 technology for dye extraction, bioactive seed compounds and compounds from other annatto plant parts (Stringheta, 2008). There is also the use of technologies such as microencapsulation and nanoencapsulation, aimed at protecting dyes against hazards such as the presence of light and oxygen, which can increase the range of products in which these may be added. Furthermore, one can produce stable dyes that are dispersible in water and which when incorporated, do not alter the texture and taste of the product (Lancaster and Lawrence, 1995). It can also recover residues from pigment extractions. Tan and Foley (see also Giuliano et al., 2003) described a waste recovery method in which, starting with water or organic solvent from the extraction of pigment from annatto seeds, tocotrienol and geranylgeraniol components can be obtained. These compounds have antioxidant activity, inhibition action against some types of cancer, hypocholesterolemic action, among others. According to Albuquerque and Meireles (2011), in the last few decades 410 patents on the subject were registered, confirming the increased interest in obtaining annatto compounds that can be used not only in the food industry, but also in the cosmetic and pharmaceutical industry and in the medical field.
REFERENCES Albuquerque, C.L.C., Meireles, M.A.A., 2011. Trends in annatto agroindustry: Bixin processing technologies and market. Recent Patents Eng. 5, 94102. Baliane, A., 1984. A cultura do urucuzeiro. Emater. Barcelos, G.R.M., et al., 2012. Bixin and norbixin protect against DNA-damage and alterations of redox status induced by methylmercury exposure in vivo. Environ. Mol. Mutagen. 53, 535541. Bouvier, F., Dogbo, O., Camara, B., 2003. Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Science (New York, N.Y.). 300, 20892091. Costa, M.G.C. et al., 2008. Genetic improvement through in vitro propagation in annatto (Bixa orellana L.). In: Thangadurai, D., Tripathi, L., Vasanthaiah, H.K.N., Cantu´, D.J. (Eds.), Crop Improvement and Biotechnology. Bioscience Publications, Tamil Nadu, pp. 3957. Cruz, A.F., da Costa, M.G.C., Otoni, W.C., 2008. Aspectos gerais da cultura e beneficiamento do urucum. In: Stringheta, P.C., Silva, P.I. (Eds.), Pigmentos de urucum: extrac¸a˜o, reac¸o˜es quı´micas, usos e aplicac¸o˜es. Gra´fica e Editora Suprema, Vic¸osa, pp. 1123. Figueiredo, B.C., Trad, I.J., Mariutti, L.R.B., Bragagnolo, N., 2014. Effect of annatto powder and sodium erythorbate on lipid oxidation in pork loin during frozen storage. Food Res. Int. 65, 137143. Franco, C.F.O., et al., 2002. Urucuzeiro: agronego´cio de corantes naturais. Emepa, PB. Galindo-Cuspinera, V., Westhoff, D.C., Rankin, S.A., 2003. Antimicrobial properties of commercial annatto extracts against selected pathogenic, lactic acid, and spoilafe microorganisms. J. Food Prot. 66, 10741078. Giridhar, P., Venugopalan, A., Parimalan, R., 2014. A review on annatto dye extraction, analysis and processing a food technologyperspective. J. Sci. Res. Rep. 3, 327348. Giriwono, P.E., et al., 2013. Dietary supplementation with geranylgeraniol suppresses lipopolysaccharide-induced inflammation via inhibition of nuclear factor-κB activation in rats. Eur. J. Nutr. 52, 11911199.
Annatto/Urucum—Bixa orellana
29
Giuliano, G., Rosati, C., Bramley, P.M., 2003. To dye or not to dye: Biochemistry of annatto unveiled. Trends Biotechnol. 21, 513516. Green, C.L., 1995. Natural Colourants and Dyestuffs. Gulrajani, M.L., Gupta, D., Maulik, S.R., 1999. Studies on dyeing with natural dyes. Part I, dyeing of annatto on nylon and polyester. Indian J. Fibre Textile Res. 24, 131135. Jondiko, I.J.O., Pattenden, G., 1989. Terpenoids and an apocarotenoid from seeds of Bixa orellana. Phytochemistry. 28, 31593162. Kang, E.J., Campbell, R.E., Bastian, E., Drake, M.A., 2010. Invited review: Annatto usage and bleaching in dairy foods. J. Dairy Sci. 93, 38913901. Lancaster, F.E., Lawrence, J.F., 1995. Determination of annatto in high-fat dairy products, margarine and hard candy by solvent extraction followed by high-performance liquid chromatography. Food Addit. Contam. 12, 919. Matuo, M.C.S., de Oliveira Takamoto, R.T., Kikuchi, I.S., de Jesus Andreoli Pinto, T., 2013. Effect of bixin and norbixin on the expression of cytochrome P450 in HepG2 cell line. Cell Biol. Int. 37, 843848. Mercadante, A.Z., Steck, A., Pfander, H., 1997a. Isolation and identification of new apocarotenoids from Annatto (Bixa orellana) seeds. J. Agric. Food Chem. 45, 10501054. Mercadante, A.Z., Steck, A., Pfander, H., 1997b. Isolation and structure elucidation of minor carotenoids from annatto (Bixa orellana L.) seeds. Phytochemistry. 46, 13791383. Mercadante, A.Z., Steck, A., Pfander, H., 1999. Three minor carotenoids from annatto (Bixa orellana) seeds. Phytochemistry. 52, 135139. Mercadante, A.Z., Steck, A., Rodriguez-Amaya, D., Pfander, H., Britton, G., 1996. Isolation of methyl 90 Z-apo-60 -lycopenoate from Bixa orellana. Phytochemistry. 41, 12011203. Oliveira, J.S., 2005. Characterization extraction and purification by chromatography of annatto compounds (Bixa orellana L.). Federal University of Santa Catarina. Parvin, K., Aziz, M.G., Yusof, Y.A., Sarker, M.S.H., Sill, H.P., 2011. Degradation kinetics of water-soluble annatto extract and sensory evaluation of annatto colored yoghurt. J. Food Agric. Environ. 9, 139142. Pierpaoli, E., et al., 2013. Effect of annatto-tocotrienols supplementation on the development of mammary tumors in HER-2/neu transgenic mice. Carcinogenesis. 34, 13521360. Pino, J.A., Correa, M.T., 2003. Chemical composition of the essential oil from Annatto (Bixa orellana L.) Seeds. J. Essential Oil Res. 15, 6667. Prabhakara Rao, P.G., Jyothirmayi, T., Balaswamy, K., Satyanarayana, A., Rao, D.G., 2005. Effect of processing conditions on the stability of annatto (Bixa orellana L.) dye incorporated into some foods. LWT Food Sci. Technol. 38, 779784. Ramalho, R.S., Pinheiro, A.L., Diniz, G.S., 1987. Informac¸o˜es ba´sicas sobre a cultura e utilizac¸a˜o do urucum (Bixa orellana L.). Reddy, M.K., Alexander-Lindo, R.L., Nair, M.G., 2005. Relative inhibition of lipid peroxidation, cyclooxygenase enzymes, and human tumor cell proliferation by natural food colors. J. Agric. Food Chem. 53, 92689273. Roehrs, M., et al., 2014. Bixin and norbixin have opposite effects on glycemia, lipidemia, and oxidative stress in streptozotocin-induced diabetic rats. Int. J. Endocrinol.839095. Scotter, M., 2009. The chemistry and analysis of annatto food colouring: a review. Food Addit. Contam. Part A. 26, 11231145. Shahid-ul-Islam, Rather, L.J., Mohammad, F., 2015. Phytochemistry, biological activities and potential of annatto in natural colorant production for industrial applications a review. J. Adv. Res. Shahid-ul-Islam, Rather, L.J., Shahid, M., Khan, M.A., Mohammad, F., 2014. Study the effect of ammonia post-treatment on color characteristics of annatto-dyed textile substrate using reflectance spectrophotometery. Ind. Crops Prod. 59, 337342. Shibata, A., et al., 2008. Tumor anti-angiogenic effect and mechanism of action of delta-tocotrienol. Biochem. Pharmacol. 76, 330339. Silva, P.I., Stringheta, P.C., 2008. Extrac¸a˜o dos pigmentos do urucum. In: Stringheta, P.C., Silva, P.I. (Eds.), Pigmentos de urucum: extrac¸a˜o, reac¸o˜es quı´micas, usos e aplicac¸o˜es. Gra´fica e Editora Suprema, pp. 4777. Siva, R., Doss, F.P., Kundu, K., Satyanarayana, V.S.V., Kumar, V., 2010. Molecular characterization of bixin-An important industrial product. Ind. Crops Prod. 32, 4853. Smith, J., Wallin, H., 2006. Annatto Extracts: Chemical and TechnicalAssessment., 21. FAO -Food and Agriculture Organization of the United Nations. Smith, N.J.H., Williams, J.T., Plucknet, D.L., Talbot, J.P., 1992. Tropical forests and their crops. In: Smith, N.J.H., Williams, J.T., Plucknet, D.L., Talbot, J.P. (Eds.), Spices and Natural Food Colorants. Comstock Pub. Assoc, Ithaca, pp. 364370. Smith, T.J., Li, X.E., Drake, M.A., 2014. Short communication: norbixin and bixin partitioning in Cheddar cheese and whey. J. Dairy Sci. 97, 33213327. Stringheta, P.C., 2008. Aplicac¸o˜es. In: Stringheta, P.C., Silva, P.I. (Eds.), Pigmentos de urucum: extrac¸a˜o, reac¸o˜es quı´micas, usos e aplicac¸o˜es. Gra´fica e Editora Suprema, pp. 110119. Stringheta, P.C. et al., 2008. Pigmentos de urucum - estrutura quı´mica, biossı´ntese e degradac¸a˜o. In: Pigmentos de urucum: extrac¸a˜o, reac¸o˜es quı´micas, usos e aplicac¸o˜es (eds. Stringheta, P.C. & Silva, P.I.) 2446 (Gra´fica e Editora Suprema). Stringheta, P.C., Silva, P.I., 2008. Pigmentos de urucum: extrac¸a˜o, reac¸o˜es quı´micas, usos e aplicac¸o˜es. Gra´fica e Editora Suprema. Tirimanna, A.S.L., 1981. Study of the carotenoid pigments of Bixa orellana L. Seeds by thin layer chromatography. Mikrochim. Acta.1116. Vale´rio, M.A., Ramos, M.I.L., Braga Neto, J.A., Macedo, M.L.R., 2015. Annatto seed residue (Bixa orellana L.): nutritional quality. Food Sci. Technol. (Campinas). 35, 326330. Vilar, D., de, A., et al., 2014. Traditional uses, chemical constituents, and biological activities of Bixa orellana L.: a review. Sci. World J. 2014, 111. Zarringhalami, S., Sahari, M.A., Hamidi-Esfehani, Z., 2009. Partial replacement of nitrite by annatto as a colour additive in sausage. Meat Sci. 81, 281284.
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FURTHER READING Chiste, R.C., et al., 2011. In vitro scavenging capacity of annatto seed extracts against reactive oxygen and nitrogen species. Food Chem. 127, 419426. Kiokias, S., Gordon, M.H., 2003. Antioxidant properties of annatto carotenoids. Food Chem. 83, 523529. Meireles, M.A.A., Albuquerque, C.L.C., 2013. Processo de obtenc¸a˜o de o´leo de urucum e sementes desengorduradas, pp. 119. Meireles, M.A.A., Leal, P.F., Rosa, P.T.V., 2006. Processo de extrac¸a˜o e processo de purificac¸a˜o em se´rie de substaˆncias ativas e corantes a partir de matrizes so´lidas, utilizando CO2 supercrı´tico: bixina proveniente do urucum, pp. 113. Sabliov, C.M., Astete, C., 2010. Water-Soluble Nanoparticles Containing Water-Insoluble Compounds. Sancho, R.A.S., de Lima, F.A., Costa, G.G., Mariutti, L.R.B., Bragagnolo, N., 2011. Effect of annatto seed and coriander leaves as natural antioxidants in fish meatballs during frozen storage. J. Food Sci. 76. Tan, B., Foley, J., 2002. Tocotrienols and Geranylgeraniol From Bixa orellana Byproducts. Viuda-Martos, M., et al., 2012. In vitro antioxidant and antibacterial activities of extracts from annatto (Bixa orellana L.) leaves and seeds. J. Food Saf. 32, 399406.
Arac¸a—Psidium cattleyanum Sabine Moˆnica M. de Almeida Lopes1 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Origin and Botanical Aspects Production Fruit Physiology and Nutritional Value
31 31 32
Postharvest Conservation Potential Industrial application References
34 34 35
ORIGIN AND BOTANICAL ASPECTS Arac¸a´ is a common name of Psidium cattleyanum, a plant species native from the Atlantic coast of Brazil, classified taxonomically as: class Magnoliopsida, order Myrtales, family Myrtaceae, genus Psidium, and species P. cattleyanum (Mattos, 1989). The species more indicated to commercial exploitation are P. cattleyanum Sabine and Psidium guineense Swartz (Franzon et al., 2009; Bezerra et al., 2006), due mainly to their exotic flavor, high content of vitamin C (Raseira and Raseira 1996) and good acceptance by consumers (Manica et al., 2000), both in natura and in processed forms such as jams and juices. The arac¸a´-peˆra (Psidium acutangulum D.C.) is a wild or cultivated fruit species of Amazonia, with acid but flavorful fruits, normally consumed as a juice (Frazon et al., 2009; Correˆa et al., 2011). The arac¸a´ plant is considered a small or shrub-like tree, reaching 14 m tall, which grows in a moist and luminous environment. The leaves are opposite, obovate to elliptic, coriaceous, glabrous, with an intense green color. The flowers are white (1.52.5 cm in diameter), pentamera, hermaphrodite, and zygomorphic, with period of bloom between June and December (Raseira et al., 2004; Bezerra et al., 2006). The arac¸a´ fruits are small (2 cm in diameter) containing numerous seeds and its weight can exceed 20 g in some cases (Raseira et al., 2004) with yellow or red epicarp when ripe (Fig. 1A,B). Botanically, the fruits are obovoid berries (24 cm in diameter), pyriformes, with flat or oval shape, crowned by the chalice, and ripen between September and March (Biegelmeyer et al., 2011). The fruit pulp is translucent, aromatic and juicy, presenting an excellent strawberrylike flavor, with a spicy touch (Bielgelmeyer et al., 2011). The breeding programs seek agronomically important traits, such as more productive plants and low vulnerability to pests and diseases, coupled with products rich in nutrients. Selective breeding programs involving Psidium species over a number of years has resulted in genotype selection in the Germplasm Bank of Embrapa Temperate Weather, located in South of Brazil, with propagation of two cultivars, named “Ya-Cy” and “Irapua˜” (Frazon et al., 2009). The cv. Ya-Cy produces yellow fruits with sweet taste, low acidity and weighing up to 45 g that start to appear 1 year after planting, while the native plant requires 4 years. The cv. Irapua˜ gives fruits with a purplered color and of a medium to large size, with a production that begins 2 years after planting (Raseira and Raseira, 1996). Both are characterized by the productive potential, but only on a small scale (Biegelmeyer et al., 2011; Frazon et al., 2009).
PRODUCTION Arac¸a´ species occur in areas under constant abiotic stress conditions, including water and temperature extremes (Coelho de Souza et al., 2003; Haminiuk et al., 2006). The propagation of arac¸a´ is carried out mainly by seeds (up 95% of germination) as vegetative propagation is not satisfactory (less of 3% of rooting) (Fachinello et al., 1994; Bezerra et al., 2010). The temperature range between 20 C and 30 C is considered as adequate for germination of seeds, as these are Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00007-1 © 2018 Elsevier Inc. All rights reserved.
31
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Exotic Fruits Reference Guide
FIGURE 1 Different peel color of ripe Arac¸a´ (Psidium cattleyanum Sabine): (A): yellow peel; (B): red peel. Source: Medina, A.L., Haas, L.I.R., Chaves, F.C., Salvador, M., Zambiazi, R.C., da Silva, W.P., et al. 2011. Arac¸a´ (Psidium cattleianum Sabine) fruit extracts with antioxidant and antimicrobial activities and antiproliferative effect on human cancer cells. Food Chem. 128, 916922 Medina et al. (2011).
the temperatures commonly found in their native regions at the time of natural germination (Kissmann and Scalon 2011; Dresch et al., 2014). Few arac¸a´ species are exploited on a commercial scale and, when exploited, the production is small and limited to certain regions of Brazil, mainly in the south. In terms of productivity, the cultivars selected by Embrapa as Ya-cy can yield until 4 kg/plant per year, with three annual harvests. Already, the production of cv. Irapua˜ is more expressive, reaching 3.414 kg/plant per year, being most suitable for processing, especially sweet paste (Frazon et al., 2009). The fruit fly is the main pest for native arac¸azeiros. South of Brazil, Anastrepha fraterculus is responsible for quality loss in P. cattleyanum. Also, it is observed in this species the occurrence of anthracnose (Colletotrichum gloesporioides), especially at beginning of ripening fruits (Raseira and Raseira, 1996).
FRUIT PHYSIOLOGY AND NUTRITIONAL VALUE In climateric fruits such as arac¸a´, during the ripening process even when detached from the parent plant, physiological, biochemical and molecular changes occur that directly affect its quality (Fetter et al., 2010). When ripe, arac¸a´ pulp present a high pulp yield (81.43%), soluble solids (11.93oBrix), moisture (77.46%), folate (47.25 g/100 g), fiber (5.5%) cal% g/100 g) (Table 1) (Hamacek et al., 2013; Silva et al., 2014). cium (485 mg/kg) but low contents of carotenoids (0.32 Whereas the ripening is an important environmental factor capable of changing the physiochemical responsible for arac¸a´ quality, Galho et al. (2007) characterized the P. cattleyanum Sabine during their ontogeny (112 days), and concluded that the contents of starch, total soluble sugars, reduced sugars, lipids and organic acids increased as the fruits ripened, while the protein contents and the components of cell wall decreased during fruit ontogeny, with strong accumulation during ripening. Enzymes such as polygalacturonase (PG) and pectinmethylesterase (PME) act to degrade the total pectin amount, making it soluble and, consequently, softening the fruit during ripening process. The total amount of pectin reported for arac¸a´ pulp is 0.72 g/100 g, with solubility of 69.4 g/100 g resulting in low values of firmness (0.42 N) at end of development, consequence of softening of fruits (Damiani et al., 2011). Phenolic compounds are found in high concentrations in many fruits and vegetables and play a particularly important role in human health, because these compounds have antioxidant, chemoprevention, cytoprotection, antimutagenic, antiinflammatory, antimicrobial antiestrogenic, and antiangiogenic activities (Albuquerque et al., 2012; Sun et al., 2015). The arac¸a´ fruit is rich in antioxidant compounds as phenolics (Silva et al., 2014), more than strawberry (Fragaria ananassa Duch.) and grape (Vitis vinifera L.) (Medina et al., 2011). HPLC-UV shows that epicatechin (Cardoso et al., 2011), gallic acid (Mitsuoka, 2014), and taxifolin (Gonc¸alves et al., 2010) are the major phenolic compounds present in arac¸a´ (Medina et al., 2011). Interestingly, quercetin (Sano et al., 2010), and ellagic acid (Miranda-Vilela et al., 2009) were also detected. Ramos et al. (2015) evaluating the chemical characterization and antioxidant capacity of the arac¸a´-peˆra (Psidium acutangulum D.C), characterized 22 compounds by UHPLC-HRMS and NMR methods, among them: one disaccharide, five monosaccharides, two organic acids, one trihydroxycinnamic acid glucopyranosyl, one tannine digalloyl glucopyranosyl, five triterpenoid acids, and six fatty acids. The quantification of ascorbic acid by HPLC-MS reached values of 74.32 mg/100 g of fresh weight (FW). Antioxidant activities measured by DPPHU (24.96 mg of vitamin C 100 g FW), and ABTS1U (90.57 mg of vitamin C 100 g FW) assays, reflected the high content of ascorbic acid in arac¸a´ fruit.
Arac¸a—Psidium cattleyanum Sabine
33
TABLE 1 Nutritional Value of Arac¸a´ Pulp Nutrient
Pulp
References
Protein (g/100 g)
1.451.87
Damiani et al. (2011), Hamacek et al. (2013)
Fat (g/100 g)
0.331.07
Damiani et al. (2011), Hamacek et al. (2013)
Carbohydrates (g/100 g)
6.9116.95
Damiani et al. (2011), Hamacek et al. (2013)
Sucrose (g/100 g)
3.87
Damiani et al. (2011)
Carotenoids (g/100 g)
0.010.32
Fetter et al. (2010), Hamacek et al. (2013)
74.32
Ramos et al. (2015)
Citric acid
881.25
Damiani et al. (2011)
Malic acid
761.30
Damiani et al. (2011)
Tartaric acid
296.30
Damiani et al. (2011)
Folate (g/100 g)
47.25
Hamacek et al. (2013)
Vitamin E (g/100 g)
336.43
Hamacek et al. (2013)
Phosphorous
97.50
Damiani et al. (2011)
Calcium
485.00
Damiani et al. (2011)
Iron
5.48
Damiani et al. (2011)
Copper
3.20
Damiani et al. (2011)
Magnesium
292.00
Damiani et al. (2011)
Zinc
2.72
Damiani et al. (2011)
Ash (g/100)
0.440.75
Damiani et al. (2011), Hamacek et al. (2013)
Fiber (%)
4.435.5
Damiani et al. (2011), Silva et al. (2014)
Total pectin (g/100 g)
0.72
Damiani et al. (2011)
Moisture (%)
77.46
Hamacek et al. (2013)
Calories (kcal)
260
Silva et al. (2014)
Ascorbic acid (mg/100 g) Others organic acids (μg/g)
Minerals (mg/kg)
Source: Damiani, C., Vilas-Boas, E.V.B., Asquieri, E.R., Lage, M.E., Oliveira, R.A., Silva, F.A., et al., 2011. Characterization of fruits from the savanna: Arac¸a (Psidium guinnensis Sw.) and Marolo (Annona crassiflora Mart.). Cieˆnc. Tecnol. Alimen. 31, 723729; Hamacek, F.R., Santos, P.R.G., Cardoso, L.M., Ribeiro, S.M.R. and Pinheiro-Sant”Ana, H.M., 2013. Arac¸a´ of Cerrado from the Brazilian savannah: physical characteristics, chemical composition, and content of carotenoids and vitamins. Fruits 68, 467481; Silva, N.A., Rodrigues, E., Mercadante, A.Z. and Rosso, V.V., 2014. Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic forest. J. Agric. Food Chem. 62, 50725284; Ramos, A.S., Souza, R.O.S., Boleti, A.P.A., Bruginski, E.R. D., Lima, E.S., Campos, F.R., et al., 2015.Chemical characterization and antioxidant capacity of the arac¸a´-peˆra (Psidium acutangulum): An exotic Amazon fruit. Food Res. Int. 75, 315327.
The color is a critical parameter of quality and is often directly related to the concentration of pigments in fruits (peel or pulp), which in the case of arac¸a´ are majority due the anthocyanins in peel (Fetter et al., 2010) (Fig. 1A,B). However, arac¸a´ pulp is not a good source of carotenoids, and these compounds were identified by Palhares (2003), using spectrometry of mass, and the all-trans-β-cryptoxanthin was the major carotenoid, representing 34% of the total carotenoid content in this fruit, followed by β-carotene (26%) (Roesler et al., 2007) and lutein (20%) (Oliveira Sousa et al., 2011; Silva et al., 2014). According to Deshmukh et al. (2011), the concentration of antioxidant compounds in plant organisms is strongly influenced by genetics, cultivar, ontology, and environment as climate and soil conditions, among other factors. Table 2 shows the evident influence of cultivar in phytochemicals content and antioxidant activity in arac¸a´ fruits, where peˆra arac¸a´ presented more phenolics and antioxidant activity than others in two cultivars evaluated by Fetter et al. (2010).
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Exotic Fruits Reference Guide
TABLE 2 Phytochemicals Content and Antioxidant Activity of Different Species of Ripe Arac¸a´ Cultivar
Parameters* 1
Anthocyanins3
Antioxidant activity4
1.07 6 0.08a
36.12 6 5.56a
7884.33 6 124.18b
294.51 6 38.63c
0.99 6 0.16a
10.69 6 9.49b
3617.00 6 448.73c
1851.38 6 34.09a
0.59 6 0.09b
10.41 6 1.66b
20324.82 6 605.68a
Phenolic compounds
Carotenoids
Red arac¸a´
668.63 6 41.32b
Yellow arac¸a´ Peˆra arac¸a´
2
*Means of four replicates 6 standard deviation. Numbers followed by equal letters in the same column do not differ by Tukey’s test at 5% 1 mg of chlorogenic acid. 100 g of fresh weight (FW) 2 mg of β-caroteno. 100 g (FW) 3 mg of cyanidin-3-glucoside. 100 g (FW) 4 μg of trolox.g (FW). Source: Fetter, M.R., Vizzoto, M., Corbelini, D.D., Gonzalez, T.N., 2010. Functional properties of yellow guava, red guava (Psidium cattleyanum Sabine) and pear guava (Psidium acutangulum D.C) grown in Pelotas/RSBrazil. Braz. J. Food Techonol. doi: 10.4260/BJFT20101304115.
A study comparing the chemical composition and antioxidant activity of red (P. cattleyanum) and yellow (P. cattleyanum var. lucidum) arac¸a´ fruit reported that P. cattleyanum presented a higher content of polyphenolic compounds (501.33 mg/100 g), than P. cattleyanum var. lucidum (292.03 mg/100 g), with a hyperoside being one of the major flavonoids identified for both cultivars. P. cattleyanum presented an anthocyanin, identified as cyanidin as its major flavonoid. However, the antioxidant activity varied in a concentration-dependent manner for both arac¸a´ species (Bielgelmeyer et al., 2011). More recent ethnopharmacological studies show the protective effect of dietary intake of arac¸a´, such as decreased levels of total cholesterol, LDL, and fat in the mouse liver (Nora et al., 2014). Balisteiro et al. (2013) associated the high amounts of phenolic compounds, antioxidant capacity and proantocyanidins in arac¸a´ juice with effects on postprandial glycemia in vivo. Arac¸a´ extracts presented antimicrobial effects against Salmonella enteritidis, possibly owing to the presence of phenolic compounds, which destabilize the bacterial cell membrane responsible for prokaryotic respiration (Medina et al., 2011). Interestingly, arac¸a´ extracts reduced survival rates of breast and colon cancer cells (MCF-7 and Caco-2, respectively) in vitro, by mechanisms not yet described, indicating an antiproliferative effect (Medina et al., 2011).
POSTHARVEST CONSERVATION The maturation stage at which fruits are harvested, determines its postharvest conservation potential and when offered to the consumer. Fruits harvested immature, beyond the low sensorial quality, are susceptible to dehydration and physiological disorders. On the other hand, when harvested very ripe, the fruit very rapidly develops the senescence process (Chitarra and Chitarra, 2005). The ripe arac¸a´ is highly perishable, lasting one to two days at room temperature, which makes it difficult to handle and store after harvest (Drehmer and Amarante, 2008). The main reason for this perishability is the climacteric maturation behavior with a respiratory rate of 194 mg CO2/fruit per day after complete cycle of grown (122 days after anthesis-ripe) (Galho et al., 2007). The conservation of arac¸a´ is influenced by maturation stage and storage temperature. Fruits harvested at green maturity stage, in comparison to fruit harvested at mature stage, present a decrease in the quality, characterized by lower soluble solids content and higher titratable acidity, but better firmness and green color retention, especially for fruits stored at 0 C (Drehmer and Amarante, 2008). For extended shelf-life, arac¸a´, especially red fruits, should be harvested at the mature stage and immediately stored at temperatures close to 0 C, this procedure is recommended due the high respiratory rates and rapid maturation at room temperature (20 C) (Drehmer and Amarante, 2008).
POTENTIAL INDUSTRIAL APPLICATION The chemical composition and nutritional characteristics give arac¸a´ a potential for industrialization through preparations such as jams, juices, icecreams, and liqueurs, among others. The oil can be extracted from seeds (Patel, 2012).
Arac¸a—Psidium cattleyanum Sabine
35
Damiani et al. (2012) evaluated the antioxidant potential of Psidium guinnensis jam during storage. The centesimal composition including sugars, fibers, pectin, and consistency showed that the use of arac¸a´ was suitable for jam production, and that the product remained within the standards established by the Brazilian legislation. The antioxidant activity increased during the 12 months of storage, collaborating with a reduction in the free radicals to which people are daily exposed, and, during storage, the arac¸a´ jam underwent a darkening process, with a decrease in luminosity (L*), and a*; b* values. Arac¸a´ fruits deserves special attention as this fruit can be consumed fresh or processed. The fruit are rich in phytochemicals, mainly phenolics and vitamin C, which are recognized for biological activities, such as antioxidants, justifying the inclusion of arac¸a´ fruits among functional foods.
REFERENCES Albuquerque, U.P., Ramos, M.A., Melo, J.G., 2012. New strategies for drug discovery in tropical forests based on ethnobotanical and chemical ecological studies. J. Ethnopharmacol. 140, 197201. Balisteiro, D.M., Alezandro, M.R., Genovese, 2013. Characterization and effect of clarified arac¸a´ (Psidium guineenses Sw.) juice on postprandial glycemia in healthy subjects. Cieˆnc. Tecnol. Alimen. 33, 6674. Bezerra, J.E.F., Lederman, I.E., Silva, J.F.J., Proenc¸a, C.R.B., 2006. Frutas nativas da regia˜o Centro-Oeste do Brasil. Documentos Embrapa Recursos Gene´ticos e Biotecnologia: Brası´lia. 21p. Bezerra, J.E.F., Lederman, I.E., Silva, J.F.J., Proenc¸a, C.E.B., 2010. Arac¸a´: Frutas Nativas da Regia˜o Centro-Oeste do Brasil. Embrapa Informac¸a˜o Tecnolo´gica: Brası´lia, 20p. Biegelmeyer, R., Andrade, J.M.M., Aboy, A.L., Apel, M.A., Dresch, R.R., Marin, R., et al., 2011. Comparative analysis of the chemical composition and antioxidant activity of red (Psidium cattleianum) and yellow (Psidium cattleianum var. lucidum) strawberry guava fruit. J. Food. Sci. 76. Available from: http://dx.doi.org/10.1111/j.1750-3841.2011.02319.x. Cardoso, L.M., Martino, H.S.D., Moreira, A.V.B., Ribeiro, S.M.R., Pinheiro-Sant’Ana, H.M., 2011. Cagaita (Eugenia dysenterica D.C) of the Cerrado of Minas Gerais, Brazil: Physical and chemical characterization, carotenoids and vitamins. Food Res. Int. 44, 21512154. Chitarra, M.I.F., Chitarra, A.B., 2005. Po´s-colheita de frutos e hortalic¸as: fisiologia e manuseio. second ed. UFLA, Lavras, 785 p. Coelho de Souza, G., Haas, A.P.S., von Poser, G.L., Schapoval, E.E.S., Elisabetsky, E., 2003. Ethnopharmacological studies of antimicrobial remedies in the south of Brazil. J. Ethnopharmacol. 90 (1), 135143. Correˆa, L.C., Santos, C.A.F., Vianello, F., Lima, G.P.P., 2011. Antioxidant content in guava (Psidium guajava) and arac¸a´ (Psidium spp.) germplasm from different Brazilian regions. Plant Genet. Resour. Charact. Util. 9 (3), 384391. Damiani, C., Vilas-Boas, E.V.B., Asquieri, E.R., Lage, M.E., Oliveira, R.A., Silva, F.A., et al., 2011. Characterization of fruits from the savanna: Arac¸a (Psidium guinnensis Sw.) and Marolo (Annona crassiflora Mart.). Cieˆnc. Tecnol. Alimen. 31, 723729. Damiani, C., Silva, F.A., Asquieri, E.R., Lage, M.E., Vilas-Boas, E.V.B., 2012. Antioxidant potential of Psidium guinnensis Sw. jam during storage. Pesquisa Agropecua´ria Trop. 42, 9098. Deshmukh, S.R., Wadegaonkar, V.P., Bhagat, R.P., Wadegaonkar, P.A., 2011. Tissue specific expression of anthraquinones, flavonoids and phenolics in leaf, fruit and root suspension cultures of Indian Mulberry (Morinda citrifola L.). Plant Omics. 4 (1), 6. Drehmer, A.M.F., Amarante, C.V.T., 2008. Post-harvest preservation of red strawberry-guavas as affected by maturity stage and storage temperature. Rev. Bras. Frutic. 30, 322326. Dresch, D.M., Sacalon, S.P.Q., Neves, E.M.S., Massetto, T.E., Mussury, R.M., 2014. Effect of pre-treatments on seed germination and seedling growth in Psidium guineense Swartz. Agrociencia Uruguay. 8, 3339. Fachinello, J.C., Hoffmann, A., Nachtigal, J.C., Kersten, E., Fortes, G.R.L., 1994. Propagac¸a˜o de plantas frutı´feras de clima temperado. UFPEL, Pelotas, 179 p. Fetter, M.R., Vizzoto, M., Corbelini, D.D., Gonzalez, T.N., 2010. Functional properties of yellow guava, red guava (Psidium cattleyanum Sabine) and pear guava (Psidium acutangulum D.C) grown in Pelotas/RSBrazil. Braz. J. Food Techonol. Available from: http://dx.doi.org/10.4260/ BJFT20101304115. Frazon, R.C., Campos, L.Z.O., Proenc¸a, C.E.B., Silva, J.C.S., 2009. Arac¸a´s do geˆnero Psidium: espe´cies, ocorreˆncias, descric¸a˜o e usos. Documentos Embrapa Cerrados: Brası´lia. 48 p. Galho, A.S., Lopes, N.F., Bacarin, M.A., Lima, M.G.S., 2007. Chemical composition and growth respiration in Psidium Cattleyanum Sabine fruits during the development cycle. Rev. Bras. Frutic. 29, 6166. Gonc¸alves, A.E.S.S., Lajolo, F.M., Genovese, M.I., 2010. Chemical composition and antioxidant/antidiabetic potential of Brazilian native fruits and commercial frozen pulps. J. Agric. Food. Chem. 58, 46664674. Hamacek, F.R., Santos, P.R.G., Cardoso, L.M., Ribeiro, S.M.R., Pinheiro-Sant”Ana, H.M., 2013. Arac¸a´ of Cerrado from the Brazilian savannah: Physical characteristics, chemical composition, and content of carotenoids and vitamins. Fruits. 68, 467481. Haminiuk, C.W.I., Sierakowski, M.R., Vidal, J.R.M.B., Masson, M.L., 2006. Influence of temperature on the rheological behavior of whole arac¸a´ pulp (Psidium cattleianum Sabine). LWT Food Sci. Technol. 39 (4), 426430. Kissmann, C., Scalon, S.P.Q., 2011. Seed biometry and the effect of pre germinative treatments, temperature, and light on seed germination and subsequent growth of three Stryphnodendron species. J. Torrey Bot. Soc. 138, 123133.
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Exotic Fruits Reference Guide
Manica, I., 2000. Frutas nativas, silvestres e exo´ticas: te´cnicas de produc¸a˜o e mercado: abiu, amora-preta, arac¸a´, bacuri, biriba, carambola, cereja-dorio-grande, jabuticaba. Cinco Continentes, Porto Alegre, 327 p. Mattos, J.R., 1989. Myrtaceae do Rio Grande do Sul. CEUE, Porto Alegre, 721 p. Medina, A.L., Haas, L.I.R., Chaves, F.C., Salvador, M., Zambiazi, R.C., da Silva, W.P., et al., 2011. Arac¸a´ (Psidium cattleianum Sabine) fruit extracts with antioxidant and antimicrobial activities and antiproliferative effect on human cancer cells. Food. Chem. 128, 916922. Miranda-Vilela, A.L., Akimoto, A.K., Alves, P.C., Pereira, L.C., Gonc¸alves, C.A., Klautau Guimara˜es, M.N., et al., 2009. Dietary carotenoid-rich pequi oil reduces plasma lipid peroxidation and DNA damage in runners and evidence for an association with MnSOD genetic variant-Val9Ala. Genet. Mol. Res. 8, 14811495. Mitsuoka, T., 2014. Development of functional foods. Biosci. Microbiota Food Health. 33, 117128. Nora, C.D., Danielli, D., Sousa, L.F., Rios, A.O., Jong, E.V., Floˆres, S.H., 2014. Protective effect of guabiju (Myrcianthes pungens (O. Berg) D. Legrand) and red guava (Psidium cattleyanum Sabine) against cisplatin-induced hypercholesterolemia in rats. Braz. J. Pharmaceut. Sci. 50, 483490. Oliveira Sousa, A.G., Fernandes, D.C., Alves, A.M., de Freitas, J.B., Naves, M.M.V., 2011. Nutritional quality and protein value of exotic almonds and nut from the Brazilian savanna compared to peanut. Food Res. Int. 44, 23192325. Palhares, D., 2003. Caracterizac¸a˜o farmacogno´stica das folhas de Eugenia dysenterica D.C (Myrtaceae Jussieu). Rev. Lecta. 21, 2936. Patel, S., 2012. Exotic tropical plant Psidium cattleianum: a review on prospects and threats. Rev. Environ. Sci. Biotechnol. 11, 243248. Ramos, A.S., Souza, R.O.S., Boleti, A.P.A., Bruginski, E.R.D., Lima, E.S., Campos, F.R., et al., 2015. Chemical characterization and antioxidant capacity of the arac¸a´-peˆra (Psidium acutangulum): An exotic Amazon fruit. Food Res. Int. 75, 315327. Raseira, C.B.M., Antunes, L.E.C., Trevisan, R., Gonc¸alves, E.D., 2004. Espe´cies frutı´feras nativas do Sul do Brasil. Documentos Embrapa Clima Temperado: Pelotas: 124p. Raseira, M.C.B., Raseira, A., 1996. Contribuic¸a˜o ao estudo do arac¸azeiro (Psidium cattleyanum). Embrapa/CPACT, Pelotas, 95p. Roesler, R., Malta, L.G., Carrasco, L.C., Holanda, R.B., Sousa, C.A.S., Pastore, G.M., 2007. Antioxidant activity of cerrado fruits. Cieˆnc. Tecnol. Alimen. 27, 5360. Sano, E.E., Rosa, R., Brito, J.L., Ferreira, L.G., 2010. Land cover mapping of the tropical savanna region in Brazil. Environ. Monit. Assess. 166, 113124. Silva, N.A., Rodrigues, E., Mercadante, A.Z., Rosso, V.V., 2014. Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic forest. J. Agric. Food. Chem. 62, 50725284. Sun, Q., Heilmann, J., Konig, B., 2015. Natural phenolic metabolites with anti-angiogenic properties-A review from the chemical point of view. Beilstein. J. Org. Chem. 11, 249264.
Avocado fruit—Persea americana Elena Hurtado-Ferna´ndez, Alberto Ferna´ndez-Gutie´rrez and Alegrı´a Carrasco-Pancorbo University of Granada, Granada, Spain
Chapter Outline Botany and Origin Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Sensory Characteristics Harvest Season Harvest and Postharvest Conservation
37 39 40 42 42 43
Estimated Annual Production World Trade Industrial Applications and Other Potential Uses Acknowledgment References
44 44 44 46 46
BOTANY AND ORIGIN The avocado is an evergreen tree, despite the fact that the leaves present a surprisingly short longevity, which is no longer than 12 months. It is characterized by a rapid growth in height and spread, reaching heights up to 20 m, its roots are shallow and have poor water uptake and hydraulic conductance. Although the trees produce high amounts of flowers, usually less than 0.1% of these flowers set fruit. The flowering and fruit set can be influenced by three different climacteric factors: (1) the occurrence of frost during the winter; (2) the existence of low mean temperatures; and (3) the occurrence of extreme high temperatures during fruit set (Carr, 2013). The avocado tree belongs to the Lauraceae family—typical from the tropical or subtropical climates—and the Persea genus, which is divided in three different subgenera that enclose more than 150 species: Persea (only 2 species, P. americana and P. schiedeana), Eriodaphne (about 70 species, such as P. caerulea, P. indica and P. lingue, among others), and Machilus (including around 80 species, such as P. japonica, P. kobu). The most relevant and widely studied member of the Persea genus is P. americana, whose fruit is the commercial avocado. Avocado is the most common English name, but it is also known as alligator pear and butter pear. The name avocado is derived from the Aztec Nahuatl language word, ahuacatl, meaning “testicle.” This name refers to the shape of the fruit, which was considered by the Aztecs as the fertility fruit. Avocado is native from Central America and Mexico, where it has been a staple dietary component for at least 9000 years (Chen et al., 2009). Within P. americana, it is possible to differentiate three different ecological races: Mexican, Guatemalan, and West Indian (or Antillean). Each race presents typical characteristics in terms of leaves, fruits, flowering period, etc., which have been summarized in Table 1 (Paull and Duarte, 2010): There are no sterility barriers among the three races or among any taxonomic category classified under P. americana. Hence, hybridization readily occurs wherever trees of different races are growing in proximity. For this reason, most commercial avocado cultivars are interracial hybrids, developed from chance seedlings, with different degrees of hybridization (Whiley et al., 2002; Alcaraz and Hormaza, 2007). Avocado cultivars present very different characteristics among them, for instance in size, shape and color, as can be appreciated in Fig. 1. Usually, the cultivars grown in tropical climates are not the same as those in the subtropical areas. Some of the principal avocado cultivars commercially available are shown in Table 2.
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00001-0 © 2018 Elsevier Inc. All rights reserved.
37
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Exotic Fruits Reference Guide
TABLE 1 Comparison of the Three Different Horticultural Races of Avocado Fruit
Fruit
Tree
Trait
Race Guatemalan (G)
Mexican (M)
West Indian (WI)
Climate
Subtropical
Semitropical
Tropical
Cold tolerance
Intermediate
Most
Least
Salinity tolerance
Intermediate
Least
Most
Leaf anise
Absent
Present
Absent
Young leaf color
Green with red tinge
Green
Pale yellow
Mature leaf color
Dark green
Dark green
Pale green
Blooming season
March to April
January to February
February to March
Bloom to fruit maturity
10 2 18 months
5 2 7 months
6 2 8 months
Size
Small to large
Tiny to medium
Medium to very large
Shape
Mostly round
Mostly elongate
Variable
Color
Green
Often dark
Green or reddish
Skin thickness
Thick
Very thin
Medium
Skin surface
Rough
Waxy bloom
Shiny
Skin peelability
Rigid
Membranous
Leathery
Seed size
Small
Large
Variable
Seed cavity
Tight
Loose
Variable
Seed surface
Smooth
Smooth
Rough
Oil content
High
Highest
Low
Pulp flavor
Rich
Anise-like, rich
Sweeter, milder
FIGURE 1 External appearance of different avocado cultivars. From left to right, top: Gwen, Hass, Reed; bottom: Ettinger, Fuerte, Pinkerton.
Avocado fruit—Persea americana
39
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Avocado fruit (P. americana) is a berry that consists of a large central seed and pericarp, which is the sum of the skin (exocarp), the edible portion (mesocarp) and the inner layer surrounding the seed (endocarp) (see Fig. 2) (Meyer et al., 2011). Avocado fruit development is the result of complex metabolic activities that can be affected by environmental factors such as temperature, plant water and nutrient status, light quality and quantity, etc., as well as by different plant
TABLE 2 Some Relevant Avocado Cultivars Grown in Tropical and Subtropical Climates Subtropical Climate
Tropical Climate
Cultivar
Race
Cultivar
Race
Bacon
MxG
Blair
G
Colin V 33
M
Booth 7
GxWI
Edranol
G
Booth 8
GxWI
Ettinger
M
Choquette
GxWI
Fuerte
MxG
Hickson
G
Gwen
GxM
Lisa
MxWI
Hass
G/GxM
Loretta
GxWI
Lamb Hass
GxM
Lula
GxWI
Pinkerton
GxM
Monroe
GxWI
Reed
G
Pollock
WI
Ryan
MxG
Simmonds
WI
Shepard
M
Taylor
G
Sir Prize
M
Tonnage
G
Zutano
MxG
Waldin
WI
FIGURE 2 The different parts of the avocado fruit.
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Exotic Fruits Reference Guide
hormones (Cowan et al., 2001). This process is usually divided in three main phases, which can be differentiated in the single sigmoid curve that characterizes avocado growth. The first phase (lag phase) includes ovary development, fertilization and fruit set; there is a slow growth and 90% abscission occurred at this time. In the second phase (growth), an important number of cell divisions take place, as well as seed formation and early embryo development. Finally, the third stage (physiological maturation phase) is characterized by seed maturation together with a decrease of cell division (Cowan et al., 2001; Lee and Young, 1983). It has been observed that this tropical fruit is quite unusual, considering that cell division in the mesocarp does not occur only in the early period of growth—where it takes place rapidly—but it also continues, at a slow rate, over the rest of development and maturation. Therefore, avocado growth is due to both cell division and cell enlargement (Bower and Cutting, 1988; Scora et al., 2002). One of the most remarkable characteristics of avocados, when compared with other fruits, is that they do not ripen on the tree; they start ripening after harvesting, which usually occurs after fruits reach the physiological maturity (defined as the stage in which avocados could continue the developmental process even if detached from the tree) (Watada et al., 1984). Ripening has been described as a “highly coordinated, genetically programmed, and an irreversible phenomenon” (Prasanna et al., 2007) in which the avocado undergoes important chemical and physiological modifications such as pulp softening, textural changes, change in color (as a consequence of pigments synthesis and loss of chlorophylls), formation of aroma volatiles, increase of flavor, and alteration of sugar and acid concentrations (Hiwasa-Tanase and Ezura, 2014) that make the fruit acceptable for consumption. Apart from that, avocado ripening is marked by an important increase of fruit respiration and ethylene production (Seymour and Tucker, 1993) which explains why this tropical fruit is classified into the group of climacteric fruits. According to Kassim et al. (2013), three stages can be distinguished in avocado respiration: preclimacteric (minimum respiration), climacteric (maximum respiration), and postclimacteric (decline in respiration). Most of the aforementioned changes take place during preclimacteric and climacteric stages. Ethylene is a phytohormone with a key role in the ripening process, as the increase of its production at the onset of ripening acts as initiator of this process. Moreover, several authors have stated that ethylene has also a direct influence in the maintenance of this process (Hiwasa-Tanase and Ezura, 2014).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE The first information about the nutritional composition of avocado fruits dates back to 1922. Data about the macro- and micronutrients found in avocado have been compiled in different food composition tables, although the nutrient content of the edible portion of the fruit (pulp or mesocarp) highly varies depending on factors such as variety, ripening degree and cultivation conditions. Avocado is a very complex matrix formed by a wide variety of compounds. It is greatly appreciated for being an excellent source of energy, fatty acids, and vitamins. Table 3 shows the nutritional composition of 100 g of avocado fruit according to the USDA National Nutrient Database for Standard Reference (United States Department of Agriculture USDA Nutrient Data Laboratory, Food and Nutrition Information Center FNIC and Information Systems Division of the National Agricultural Library, 2011). One of the main components of avocado is the fat, and because of this characteristic is not surprising that it is also known as the “butter fruit.” In general, the oil content of avocado increases with the ripening process (Ozdemir and Topuz, 2004). Monounsaturated fatty acids are the predominant ones; oleic acid stands out within this group as one of the most characteristic. Other important fatty acids of avocado fruit, although less abundant, are linoleic (polyunsaturated) and palmitic (saturated) acids. The abundance of these substances, together with the fact that some of the principal healthy benefits of avocado have been attributed to its high monounsaturated fatty acid content, make lipids one of the most studied chemical families in avocado (Villa-Rodrı´guez et al., 2010). Paying attention to the rest of constituents, the avocado protein level is higher than the protein concentrations of other fruits, reaching values about 2%, whereas most of the fruits present a protein content of around 1% (Paull and Duarte, 2010). Avocado is also a very important source of vitamins (especially vitamins E and C), pigments (anthocyanins, chlorophylls, and carotenoids) (Gross et al., 1973; Ashton et al., 2006), sterols (Plaza et al., 2009), phenolic compounds (Golukcu and Ozdemir, 2010), and seven-carbon sugars and its related alcohols (D-mannoheptulose and perseitol) (Meyer and Terry, 2010). The determination of all these metabolites has been possible, thanks to the advances in the field of metabolomics and the analytical tool improvements that allow carrying out increasingly complex determinations. In the last few years, the number of published articles related to avocado metabolome characterization by applying new and powerful analytical methodologies has increased, providing large amount of information regarding avocado composition and contributing to enlarge the knowledge about this topic (HurtadoFerna´ndez et al., 2011a,b, 2013a,b, 2014, 2015; Esteve et al., 2012; Contreras-Gutie´rrez et al., 2013). All these nutritive and non-nutritive substances present in avocado fruit are responsible for some of its organoleptic properties and may contribute to enhance human health (because of the health-promoting effects attributed to some of
Avocado fruit—Persea americana
41
TABLE 3 Nutritional Content of 100 g of Avocado Fruit 160 kcal
Water
73.23 g
Protein
2.00 g
Total lipids
14.66 g
Carbohydrates
8.53 g
Total dietary fiber
6.70 g
Sugars
0.66 g
Saturated fatty acid
2.13 g
Monounsaturated fatty acids
9.80 g
General nutritional composition
Fatty acids
Energy
Unsaturated fatty acids
1.82 g
Vitamin C (ascorbic acid)
10.00 mg
Thiamine (B1)
0.07 mg
Riboflavin (B2)
0.13 mg
Niacin (B3)
1.74 mg
Pyridoxine (B6)
0.26 mg
Folate (DFE)*
89 μg
Vitamins
Vitamin A (RAE)*
7 μg
Vitamin E (α-tocopherol)
2.07 mg
Vitamin K (phylloquinone)
21 μg
Calcium (Ca)
12 mg
Iron (Fe)
0.55 mg
Magnesium (Mg)
29 mg
Phosphorus (P)
52 mg
Potassium (K)
485 mg
Sodium (Na)
7 mg
Zinc (Zn)
0.64 mg
Minerals
*DFE, dietary folate equivalents; RAE, retinol activity equivalents.
the metabolites present in this matrix). Over the years, numerous researchers have drawn attention to the connection between avocado consumption and a better health, finding that some of the numerous substances present in the avocado fruit are closely related to several healthy effects for the human beings: maintenance of normal serum cholesterol, weight management, diabetes control, cancer prevention, etc. (Dreher and Davenport, 2013; Ding et al., 2007; Devalaraja et al., 2011; Grant, 1960). Studies reveal that all these effects are mainly due to the presence of fatty acids, dietary fiber, D-mannoheptulose and perseitol, potassium, magnesium, vitamins C, E, K and B group, carotenoids, phenolics, phytosterols or terpenoids in this fruit (Dreher and Davenport, 2013). For all of the aforementioned, it can be concluded that the inclusion of avocado in the everyday diet could bring positive effects to the health of human beings. However, every time that a statement like this is pronounced, seems necessary to remind people that a single food will never provide all required nutrients and nutraceuticals, because no food is 100% complete from a nutritional point of view. Thus, it is advisable to include several food items from all the different groups (fruits, vegetables, legumes and potatoes, fish and meat, etc.) in our diet in order to ensure good nutrition. Besides, the combined consumption of different foods can improve the bioavailability and absorption of specific nutrients or bioactive compounds. In this sense, it has been observed, for instance, that consuming carotenoid-rich fruits or
42
Exotic Fruits Reference Guide
vegetables together with avocado or avocado oil can significantly increase carotenoids absorption, a fact that may help to enhance its health effects (Unlu et al., 2005).
SENSORY CHARACTERISTICS The avocado is characterized by an attractive color, a distinguishing texture, and an exquisite flavor and aroma. All these sensory attributes are closely related to its eating quality, which increases as the fruit ripens, and some of them are used for consumers as a guide at purchasing time (Kassim et al., 2013). According to Razeto et al. (2004), consumer acceptability is mainly correlated with pulp texture (more than flavor or oil content) and it is negatively affected by the presence of fibers and mesocarp discoloration. When an evaluation with panelists was carried out to study avocado likeability or acceptability, texture and flavor are usually the most widely evaluated attributes. The descriptors usually included in terms of texture are mushy, firm, stringy, gritty, creamy, smooth, dry, watery and oily; whereas the terms more widely used to describe the flavor are bland, grassy, woody-pine, sweet, nutty, buttery, savory, oily, rancid, canned pea, with sharp, astringent, metallic and bitter (referring to aftertaste). In a very interesting study, Obenland et al. (2012) highlighted that the higher fruit likeability was achieved for ripe avocados, which presented creamy, smooth and buttery texture with nuttiness and a minimum of grassy flavor. Pereira et al. (2014) also carried out a sensory evaluation, where the tasters described the texture of the preferred fruits as creamy, smooth and buttery, and the flavor as buttery and nutty. The ripening process has a substantial influence on the sensory attributes of avocados; indeed, it is over this process when one of the main alterations of this fruit happens: the softening. This textural change is the most remarkable event during ripening and it is the result of enzymatic degradation of structural and storage polysaccharides. The final texture of avocado fruit is affected by several factors, such as turgor pressure generated within cells by osmosis, accumulation of storage polysaccharides, or structural integrity of the primary cell wall and the middle lamella, among others (Prasanna et al., 2007). Avocado flavor varies considerably during ripening too, as it is strongly influenced by fruit composition, especially in terms of sugars, acids and lipids (Defilippi et al., 2009). Over the last few years several authors have described the close connection between flavor and aroma (Obenland et al., 2012; Defilippi et al., 2009). Aroma is due to the presence in avocado of volatile compounds, which can be alcohols, aldehydes, and esters. The most abundant are aldehydes, as they derive from lipid degradation and, as stated before, avocado is a rich lipid matrix. Both Defilippi et al. (2009) and Obenland et al. (2012) remarked that aldehydes found in avocado pulp may contribute to a fruit flavor with a grassy aroma, although there are other volatile compounds that are also involved. The concentration of these aldehydes decreases as fruit ripen at the same time as the perception of grassiness diminish. We think that taking into account the preferences of the consumers on the basis of sensory attributes is, nowadays, essential to establish future research as well as conceive the best marketing strategies.
HARVEST SEASON The harvest season of avocado fruit widely varies depending on numerous factors, such as maturity, climate, water regime and sunlight, among others; although the most important one is the cultivar (Moretti et al., 2010). Different avocado varieties mature at different times throughout the year, but for each variety this process approximately occurs at the same time each year. As seen above, avocados are categorized into three ecological races: Mexican, Guatemalan and West Indian; each one exhibits a specific harvest season. In terms of maturity time (the time between the blooming season and harvest) the Guatemalan race requires the longest period (1018 months), followed by West Indian (68 months) and Mexican (57 months) races. Notwithstanding that the growing conditions and local environment can affect the time of harvest, avocado fruits from Guatemalan race are, in general, harvested between September and January, whereas the harvest seasons of West Indian and Mexican avocado varieties are, usually, between May and September, and between June and October, respectively (Crane et al., 2013). Avocado reaches physiological or harvest maturity on the tree, which means that fruits are picked green and hard. However, the ripening process occurs after the harvest, and it can take from a few days to a week (depending on the avocado variety, storage temperature and degree of maturity). Knowing the adequate date to harvest avocado fruits is difficult, because there are no external changes on the fruits that indicate that moment (Ozdemir and Topuz, 2004). For this reason, there are several parameters or properties that can be controlled and determined to establish the optimum picking time, such as minimum oil content, dry matter in the flesh, assigned picking date, specific gravity, examination
Avocado fruit—Persea americana
43
of seed coat thickness and sugar content, among others (Vekiari et al., 2004; Lee, 1981). In 1925, the determination of avocado oil content was standardized as a maturity index, due to its close relationship with the development of the fruit (the amount of oil increases as the avocado matures). A minimum oil content of 8% was accepted as an indicator of physiological maturity, although it was later observed that oil content considerably varies depending on the avocado variety and, therefore, 8% is probably not a good minimum standard for all of them. This fact, together with the difficulties for determining oil content, favored or promoted the development of a new and easier analytical strategy to determine avocado maturity based on the percent dry weight, which is the mass of avocado that remains after water is completely removed. Thus, since the beginning of 1980, this is the official method to estimate avocado maturity and the regulation defines a minimum of 21% dry weight to consider the avocado fruit has reached the physiological maturity (Lee, 1981; Coria-Avalos, 2008). Avocados harvested before the optimum picking time could result in a deficient maturation and poor quality (due to shriveling, rubbery texture, etc.); whereas those fruits harvested after the optimum moment could be internally damaged, because of the seed growth, and the fact that its shelf-life could be reduced (Lee, 1981). However, the time to harvest the fruit is not established just considering the minimum maturity standard; it is also determined by the required storage or transport time, and market prices. Taking advantage of the fact that avocados do not ripen until harvested, nowadays, “on-tree storage” is a widely used strategy. It consists of retaining avocado on the tree for days, weeks or even months, and harvesting the fruit on the basis of marketing opportunities. This practice obviously has some drawbacks and can cause problems such as biennial bearing or crop failure in the following year (Paull and Duarte, 2010; Whiley, 2002).
HARVEST AND POSTHARVEST CONSERVATION It is important to bear in mind that approximately 60% of the total cost of avocado production and marketing derives from the harvest and postharvest phases, which are characterized by important quality and quantity losses (from 5% to 50%, depending on the country) if proper strategies are not adopted to delay fruit deterioration from the production site ´ lvarez et al., 2004). The risk of appearance of undesirable to the final destination (Hofman et al., 2002; Dorantes-A changes in fruit quality increases the longer the time from harvest to consumption. As climacteric fruit, avocado is characterized by an increase of respiration rate and ethylene production when the ripeness process begins. It is well known that avocado quality and shelf-life are inversely related to respiration and ethylene rates (Kassim et al., 2013), because fruit tissues deteriorate at a high rate, turning this tropical fruit into a highly perishable commodity (Hiwasa-Tanase and Ezura, 2014). Thus, to avoid undesirable changes in quality parameters and extend the shelf-life during transport and exportation, applying the most convenient postharvest technologies becomes essential to slow down avocado ripening (reducing respiration rates, and decreasing ethylene production or its action) ´ lvarez et al., 2012). (Kassim et al., 2013; Moretti et al., 2010; Dorantes-A During harvest, it is important that avocados are carefully handled; indeed, one of the most relevant problems in this stage is mechanical damage, which arises as a consequence of an inadequate handling of the fruits and can decrease their commercial value. It causes an increase of water loss, respiration and ethylene release, which are related to the appearance of different defects, such as bruising, peel injuries, loss of pulp firmness, etc. Some of these problems will not be seen until avocado ripens. Manual clipping is usually the technique of choice to harvest avocado fruit, because ´ lvarez et al., 2004). Once picked, it presents the lowest risk of mechanical injuries (Hofman et al., 2002; Dorantes-A avocados should be placed in pallets or field bins, always in the shade to avoid fruit overheating, which can produce sunburn and dehydration (Paull and Duarte, 2010). It has also been observed that covering the bins with leaves reduces the discoloration of avocado pulp and the appearance of diseases after storage (Hofman et al., 2002). After harvest, bins containing avocados should be transported as soon as possible to the packing house, where fruits are weighed, cleaned with rotating brushes, and selected (manually or with the help of machines) on the basis of shape, ´ lvarez et al., 2012). After that, and size, sanitary characteristics and defects caused by insects, rodents, etc. (Dorantes-A prior to fruit packaging, different treatments can be applied to enhance avocado quality and prolong its shelf-life: heat treatments, low temperature conditioning, surface coating and wax treatments, low oxygen atmosphere/hypoxic acclimation, and the use of 1-methylcyclopropene (acts as inhibitor of ethylene action) (Kassim et al., 2013). Subsequently, fruits are packed by using several materials (cardboard, plastic, or wood) depending on the destination market. Among the different methods that can be used for avocado packaging, modified atmosphere packaging and controlled atmosphere storage are the most recognized techniques. The main objective of packaging is to preserve avocados in the best possible conditions during the storage, as it has been observed that a well-designed package contributes to minimizing fruit damage (Kassim et al., 2013). Once packed, containers are placed in pallets and they are immediately carried into
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Exotic Fruits Reference Guide
´ lvarez et al., 2012). Then, avocados can be stored in approrefrigerated chambers for a precooling process (Dorantes-A priate areas for a short time or for considerably prolonged periods, depending on the distances between the packing house and the market, and, during this time, it is absolutely mandatory to maintain certain storage conditions: temperature, relative humidity, and gas concentration. Temperature is certainly the most important factor during storage, because of its influence in reducing respiration and ethylene production. The optimum temperature oscillates from 5 C ´ lvarez et al., 2012). Relative humidity to 13 C for unripe avocados, and from 2 C to 4 C for ripe avocados (Dorantes-A is related to the loss of water of avocado fruit during storage and it has been established that atmospheres containing a relative humidity around 85%90% are favorable for preserving water loss. Regarding gases concentration, it has been proved that the combination of determined concentrations of oxygen, carbon dioxide and nitrogen (usually low oxygen and elevated carbon dioxide levels) can favor the storage of avocado, although the amount of each gas depends on the fruit variety (Kassim et al., 2013). Moreover, air circulation through the boxes and containers should be guaranteed during storage to control the temperature and minimize ethylene accumulation (Hofman et al., 2002). All these conditions should be kept during transportation to the destination market, especially in the case of sea freight as it requires several weeks of storage. Particular attention must be paid to the maintenance of a correct temperature, because a break in the cold chain of avocado fruit could lead to an increase of fruit softening as well as the appearance of several physiological disorders (Bower and Cutting, 1988; Kassim et al., 2013).
ESTIMATED ANNUAL PRODUCTION Although the origin of this crop is Central America, avocado is nowadays widely cultivated throughout the world (Alcaraz and Hormaza, 2007; Alcaraz et al., 2011). The world’s leading producers are Mexico (31.1%), Dominican Republic (8.2%), Colombia (6.4%), Peru (6.1%), and Indonesia (5.9%). Considering these numbers, it is evident that the American continent conquers the avocado production (70.3%), being also the continent with the highest amount of harvested hectares (ha), followed by Africa (15.2%), Asia (10.9%), Europe (1.9%), and Oceania (1.6%) (Statistics Division of the Food and Agriculture Organization for the United Nations, 2013). The main countries producing avocado fruit within each continent are highlighted in Fig. 3, where it has been illustrated the fact that Kenya, Mexico, Indonesia, Spain and Australia are those with remarkably higher production. As this fruit has distinctive and pleasant sensory attributes, and it is perceived by buyers as beneficial to health, its demand has underwent an increase over the past few years, a fact that has consequently caused an increase of the area harvested (Rodrı´guez-Fragoso et al., 2011). In 2013, the world production of avocado was of about 4.7 million tonnes, increasing 5% over the previous year (Statistics Division of the Food and Agriculture Organization for the United Nations, 2013). An important agricultural parameter is the crop yield, which refers to the measure of the production of a specific crop per unit area of land cultivation. The higher the crop yields, the better the land quality or the higher the cultivation efficiency. The crop yield for avocado fruit is, globally, of about 9.5 t/ha. The principal avocado producers present higher values; around 9.513.8 t/ha for Mexico, Colombia, Peru and Indonesia, and 30.0 t/ha for Dominican Republic. A slight increase of the crop yields would generate a considerable impact on avocado production.
WORLD TRADE In general, those countries that produce the highest avocado amount also tend to be the main consumers of this fruit. However, over the last decades, the demand for this fruit has considerably grown in several markets, causing an important rise of the volume of avocado that is intended for exporting; specifically the exports have increased a 65.6% in the last 10 years (Statistics Division of the Food and Agriculture Organization for the United Nations, 2013). The principal avocado exporter countries are Mexico (47.0%), The Netherlands (10.0%), Chile (8.7%) and Peru (7.9%); whereas the main importers of this tropical fruit are United States (44.6%), The Netherlands (10.7%), France (8.4%) and Japan (5.2%) (Statistics Division of the Food and Agriculture Organization for the United Nations, 2013). The fact that The Netherlands and France appear in both lists can be explained by considering that they reexport a significant percentage of their avocado imports to other countries in the European Union.
INDUSTRIAL APPLICATIONS AND OTHER POTENTIAL USES The presence of avocado in the world market has been steadily growing in the past few decades, and it is no longer considered an exotic fruit, but part of the daily diet of many countries. Avocado has a large market as a fresh fruit;
Avocado fruit—Persea americana
Asia
Africa
Philippines 3.9%
Democratic Republic of the Congo 9.1% Ethiopia 3.8%
Others 1.5%
Lebanon 1.6%
China 21.7%
Israel 17.8%
Cameroon 10.6%
Others 3.8%
Côte d'Ivoire 4.6%
South Africa 12.5%
Morocco 4.4%
America
United States of America 5.3%
Venezuela Others 4.6% 3.4%
Portugal 19.4%
Spain 77.1%
Brazil 4.8% Chile 5.0%
Dominican Republic 11.7% Mexico 44.4%
Greece 2.2%
Madagascar 3.6%
Colombia 9.2%
Peru 8.7%
Europe
Kenya 26.7%
Rwanda 20.7%
Indonesia 53.5%
Bosnia and Herzegovina 1.2%
45
Guatemala 2.9%
Oceania Samoa 1.7%
New Zealand 27.9%
Australia 70.4%
FIGURE 3 Sector diagrams representing the principal avocado producers, distributed by continents in 2013 (Statistics Division of the Food and Agriculture Organization for the United Nations, 2013).
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Exotic Fruits Reference Guide
however, in order to increase commercialization on a larger scale and give avocado an added value, it is important to develop food products derived from this fruit with a long enough shelf-life to assure their transportation and distribution to consumers. Some work has been already done in this direction, and it is possible nowadays to find a wide variety of processed foods derived from avocado, such as guacamole, frozen products, refreshing drinks and avocado paste, as well as numerous uses of it in the cosmetic, soap, and shampoo industry. Moreover, avocado oil is gaining interest in the fat and oil market, as this fruit is the only one that can rival the olive and palm fruits in oil content, and also because diverse health effects have been attributed to its consumption—although, as stated above, it is also used in cosmetics ´ vila et al., 2013). Furthermore, industries are taking advan(Quin˜ones-Islas et al., 2013; dos Santos et al., 2014; Ortı´z-A tage of avocado byproducts (seed and peel) to extract oil, as well as several interesting compounds that are present at important concentration levels and can be used as antioxidants, flavoring, colorants or texturizer additives, making possible a better exploitation of avocado fruit (Dabas et al., 2013; Ayala-Zavala et al., 2011). The economic and social importance of avocado principally resides in the benefits that its cultivation gives to producers, processors, and consumers. The orchards create jobs by demanding labor for farming operations, harvest, packing house operations, transportation, and marketing. In addition, the development of new products would also promote the creation of processing plants, which in turn would generate new jobs, and increase the farmers’ profits. This chapter gives an overview about different aspects of avocado (P. americana), including, among others, the origin of this tropical fruit, its physiology, chemical composition, harvest season and conservation, as well as information about its production and industrial applications. It has been brought to light the importance of avocado fruit and the great interest that its study has currently for several fields, such as nutrition, agriculture, and industry. Its relevance explains the fact that there are numerous research groups focused on the study of this matrix, trying to go in depth into the knowledge of its biochemistry, healthy effects, and enhancement of its production. The emergence of powerful analytical tools will definitively help to clarify some of the hypotheses which are, nowadays, awakening more interest.
ACKNOWLEDGMENT The authors are very grateful to the University of Granada (postdoctoral contract) for financial assistance. They appreciate as well the support from Prof. J.I. Hormaza and his research group, who contributed with valuable scientific support.
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Avocado fruit—Persea americana
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CABI International, Wallingford, pp. 2750. Moretti, C.L., Mattos, L.M., Calbo, A.G., Sargent, S.A., 2010. Climate changes and potential impacts on postharvest quality of fruit and vegetable crops: a review. Food Res. Int. 43, 18241832. Obenland, D., Collin, S., Sievert, J., Negm, F., Arpaia, M.L., 2012. Influence of maturity and ripening on aroma volatiles and flavor in ‘Hass’ avocado. Postharvest Biol. Technol. 71, 4150. ´ vila, O., Samano-Garcı´a, C.A., Caldero´n-Corte´s, E., Pe´rez-Herna´ndez, I.H., Mejı´a-Zepeda, R., Rodrı´guez-Orozco, A.R., et al., 2013. Dietary Ortı´z-A avocado oil supplementation attenuates the alterations induced by type I diabetes and oxidative stress in electron transfer at the complex II-complex III segment of the electron transport chain in rat kidney mitochondria. J. Bioenerg. Biomemb. 45, 271287. Ozdemir, F., Topuz, A., 2004. Changes in dry matter, oil content and fatty acids composition of avocado during harvesting time and post-harvesting ripening period. Food Chem. 86, 7983. Paull, R.E., Duarte, O., 2010. Avocado. In: Paull, R.E., Duarte, O. (Eds.), Tropical Fruits (Crop Production Science in Horticulture). CABI Publishing, Wallingford, pp. 153184. Pereira, M.E.C., Sargent, S.A., Sims, C.A., Huber, D.J., Crane, J.H., Brecht, J.K., 2014. Ripening and sensory analysis of Guatemalan-West Indian hybrid avocado following ethylene pretreatment and/or exposure to gaseous or aqueous 1-methylcyclopropene. Postharvest Biol. Technol. 92, 121127. Plaza, L., Sa´nchez-Moreno, C., de Pascual-Teresa, S., de Ancos, B., Cano, M.P., 2009. Fatty acids, sterols, and antioxidant activity in minimally processed avocados during refrigerated storage. J. Agric. Food Chem. 57, 32043209.
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Prasanna, V., Prabha, T.N., Tharanathan, R.N., 2007. Fruit ripening phenomena: an overview. Crit. Rev. Food Sci. Nutr. 47, 119. Quin˜ones-Islas, N., Meza-Ma´rquez, O.G., Osorio-Revilla, G., Gallardo-Vela´zquez, T., 2013. Detection of adulterants in avocado oil by Mid-FTIR spectroscopy and multivariate analysis. Food Res. Int. 51, 148154. Razeto, B., Romero, F., Araya, E., 2004. Influence of some sensory properties on acceptability of avocados (Persea americana Mill.). Agric. Te´c. 64, 8994. Rodrı´guez-Fragoso, L., Martı´nez-Arismendi, J.L., Orozco-Bustos, D., Reyes-Esparza, J., Torres, E., Burchiel, S.W., 2011. Potential risks resulting from fruit/vegetable-drug interactions: effects on drug-metabolizing enzymes and drug transporters. J. Food Sci. 76, R112R124. Scora, R.W., Wolstenholme, B.N., Lavi, U., 2002. Taxonomy and botany. In: Whiley, A.W., Schaffer, B., Wolstenholme, B.N. (Eds.), The Avocado: Botany, Production and Uses. CABI Publishing, Wallingford, pp. 1538. Seymour, G.B., Tucker, G.A., 1993. Avocado. In: Seymour, G.B., Taylor, J.E., Tucker, G.A. (Eds.), Biochemistry of Fruit Ripening. SpringerScience 1 Business Media, B. V, Dordrecht. Statistics Division of the Food and Agriculture Organization for the United Nations, 2013. FAOSTAT data. Available from: ,http://faostat3.fao.org/ home/E.. United States Department of Agriculture (USDA) Nutrient Data Laboratory, Food and Nutrition Information Center (FNIC) and Information Systems Division of the National Agricultural Library, 2011. USDA National Nutrient Database for Standard Reference. Available from: ,http://ndb.nal. usda.gov/.. Unlu, N.Z., Bohn, T., Clinton, S.K., Schwartz, S.J., 2005. Carotenoid absorption from salad and salsa by humans is enhanced by the addition of avocado or avocado oil. J. Nutr. 135, 431436. Vekiari, S.A., Papadopoulou, P.P., Lionakis, S., Krystallis, A., 2004. Variation in the composition of Cretan avocado cultivars during ripening. J. Sci. Food Agric. 84, 485492. Villa-Rodrı´guez, J.A., Molina-Corral, F.J., Ayala-Zavala, J.F., Olivas, G.I., Gonza´lez-Aguilar, G.A., 2010. Effect of maturity stage on the content of fatty acids and antioxidant activity of ‘Hass’ avocado. Food Res. Int. 44, 12311237. Watada, A.E., Herner, R.C., Kader, A.A., Romani, R.J., Staby, G.L., 1984. Terminology for the description of developmental stages of horticultural crops. HortScience. 19, 2021. Whiley, A.W., 2002. Crop management. In: Whiley, A.W., Schaffer, B., Wolstenholme, B.N. (Eds.), The Avocado: Botany, Production and Uses. CABI Publishing, Wallingford, pp. 231258. Whiley, A.W., Schaffer, B., Wolstenholme, B.N., 2002. The Avocado: Botany, Production, and Uses. CABI Publishing, Wallingford.
Bacuri—Platonia insignis Angelo P. Jacomino1, Patricia M. Pinto2 and Camilla Z. Gallon3 1 3
University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil, 2Cantareira College, Sa˜o Paulo, Brazil University of Espirito Santo, Vito´ria, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Production Harvest and Postharvest Technology Chemical Composition and Nutritional Value
49 49 50 50
Potential Industry Application Concluding Remarks References
50 51 51
CULTIVAR ORIGIN AND BOTANICAL ASPECTS The Amazon is recognized as the largest existing rainforest, corresponding to one third of the reserves of tropical rainforests, and it is the largest genetic resource of the planet (Ministry of the EnvironmentBrazil, 2015), and their economic exploitation has great importance for the region. Among the fruits extracted in the Amazon, many are exceptionally rich in micronutrients, particularly in antioxidants, such as carotenoids, anthocyanins, and other polyphenols. Bacuri is a fruit of Platonia insignis Mart, a native species of Amazon, which is popularly known as the Bacuri tree. This fruit assumes economic importance in the Brazilian states of Para´, Maranha˜o, Mato Grosso and Tocantins (Menezes et al., 2010). Bacuri belongs to the Clusiaceae family, subfamily Clusioideae and Platonia genre. The Clusiaceae family consists of 47 genera and 1000 species, distributed in tropical and subtropical regions of the world (Aguiar et al., 2008). The origin of the species is the eastern Amazon, occurring spontaneously in all states of the north region of Brazil. It is also found in Guyana, Peru, Bolivia, Colombia, and Ecuador. The plant can reach 3035 m in height, but the average plant height is 25 m (Calzavara, 1970). Bacuri’ trees have a straight trunk, 1 m in diameter, are brown to dark brown, with rough and abundant resin (Menezes et al., 2010). Bacuri’s leaves are simple and opposite, petiolate, glabrous and glossy green on the upper surface. (Manica, 2000). The flowers are hermaphroditic, consisting of 4 sepals and 46 at the petals that are rosy and red after being very showy with numerous stamens, gathered in bundles of 5 opposite to the petals (Manica, 2000). Bacuri’ fruit is round, orange size, with thick skin, with yellow viscous and very tasty pulp. It is a uniloculated berry, with rounded, oval or flattened shape (Cavalcante, 1996), containing inside, most of the time, from one to five seeds, which is the edible part of the fruit (Carvalho et al., 1998). Most bacuri consists of the epicarp and mesocarp, which together constitute the skin of the fruit, which has rigid consistency and thickness ranging between 0.7 cm and 2.0 cm (Cavalcante, 1996).
PRODUCTION Bacuri is one of the few tree species in the Amazon that is bred in both sexual and asexual ways. The current production of bacuri pulp originates primarily from trees of the forestry (not cultivated), which was not yet devastated by the agriculture progress and wood extraction that has happened in Para´ and Maranha˜o in the last four centuries (Homma et al., 2011). The harvest of bacuri in the Amazon, in general, takes place from January to May, with peak production in February and March (Ferreira et al., 1987). An adult plant, about 15 years of age, can produce 350750 fruits per harvest. With a density of 100 plants per hectare, the probable fruit production would be 2025 tons per hectare (Manica, 2000). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00008-3 © 2018 Elsevier Inc. All rights reserved.
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HARVEST AND POSTHARVEST TECHNOLOGY The meaning of the name of bacuri is “falling as soon as mature” (Fonseca, 1954), due to the fact that the fruit is usually collected and not harvested after its detachment from the tree. Bacuri’ fruit is ready for harvest between 4 and 4.5 months after anthesis. Harvesting is done manually, collecting the fruits that falls spontaneously when ripe. Due to the protection provided by the hard skin, the fruit does not get damaged easily and can be transported over long distances if good conditions for its conservation are kept (Calzavara, 1970). The pulp quality for consumption range from 5 to 10 days, from the moment of the fall of the fruit. This period may be extended when the fruits are manually harvested from trees (Villachica et al., 1996). Teixeira (2000) found that at ambient conditions the fruit has 16 days of shelf life when harvested directly from the plants. Furthermore, it was observed that bacuri is not a typical climacteric fruit (Teixeira et al., 2005). There is no doubt about the potential for using bacuri in industry and its economic importance. However, currently there is a lack of proper handling techniques, transport and storage, associated with food preservation technologies (such as refrigeration, freezing, dehydration, etc.) that can improve the production chain making this fruit accessible and known for the others regions in Brazil and in the world.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Diets rich in fruits and vegetables are being encouraged due to their inverse relationship with the incidence of chronic diseases. This beneficial effect is thought to be related to the presence of diverse secondary metabolites, which is commonly referred to as phytochemicals. In this sense, Bacuri has a research potencial as it contains diverse health-related antioxidants and a large amount of vitamins, minerals and fibers. Bacuri’s considerable levels of bioactive compounds turn it into a promising commercial nontraditional, Amazon region, tropical fruit (Rufino et al., 2009). The Platonia genre is very rich in various natural substances as xanthones, fatty acids, triglycerides, ascorbic acid, and polyphenols (Clerici and Carvalho-Silva, 2011; Santos et al., 2013). Recent studies have already analyzed the main physical and chemical characteristics of fruit pulp, such as total soluble solids, pH, titratable acidity and lipids (Table 1) (Canuto et al., 2010). Bacuri is also a good source for culinary products (juices, icecream, yogurts, puddings, sweets and creams). According to Teixeira (2000), bacuri has small amounts of starch, taking effect on the taste and texture of the fruit. The wax obtained from the bacuri oil seeds is widely used for its antiinflammatory action and well used by the local people in treating burns. Known as “lard of bacuri” this substance is used in popular medicine as a treatment of dermatological diseases (Santos et al., 2013).
POTENTIAL INDUSTRY APPLICATION The extraordinary diversity and potential use of regional fruits of the Brazilian Amazon have attracted much attention for tropical fruits. This suggests a promising opportunity for the marketing of fresh fruits and for their products by the industry.
TABLE 1 Physical and Chemical Characterization of Bacuri (Platonia insignis Mart.) Pulp in the Literature Properties
Santos (1982)
Moraes et al. (1994)
Teixeira et al. (2000)
Canuto et al. (2010)
Humidity (%)
76.16
80.70
75.96
84.8
Vitamin C (mg 100 g )
10
12.38
Soluble solids (Brix)
19.10
16.40
16.80
13.0
2.80
3.50
3.37
21
pH
3.40
Bacuri—Platonia insignis
51
Bacuris fruit is among the most important fruit in the Amazon because of the characteristic flavor which make it highly appreciated and consumed by locals (Ferreira et al., 1987). This fruit can be used not only fresh, because of the appreciated taste and flavor, but also in the preparation of juices, icecream, pasta, jams, jellies, preserves, candied sweet, liqueurs, wine, etc. (Lorenzi et al., 2006). Those products are obtained after the separation of the existing resin in the pulp (Aguiar et al., 2008). For the pulp to be used, seeds are carefully separated with the use of scissors because any wound to the core releases a resin that stains the pulp. There is no existing machine on the market that helps to extract the pulp mechanically (Homma et al., 2011). This exemplifies how much has to be done to make bacuri widespread. Moreover, phytochemicals and pharmacological studies of extracts and compounds isolated from bacuri indicate that its’ compounds are promising sources for preparation of herbal medicines (Santos et al., 2013). The production of bacuri is commercialized mainly in the large fruit’s distribution center central supply and fairs, and has not been sufficient to meet the growing consumer demand. As frozen pulp, the marketing is done mainly in major supermarket chains of mid-north region of Brazil, with prices higher than those of already known tropical fruits as cupuac¸u, the hog plum, guava and soursop, for example (Souza et al., 2001). Nowadays, the increased exposure of the region in the media, even inside the country and abroad, draws attention to this exotic tropical fruit. Increased demand for bacuri’s pulp raised its value, indicating that the local production is unable to attend even the local market (Homma et al., 2011). There is much to be done in terms of crop management and postharvest techniques.
CONCLUDING REMARKS The Amazon region is the largest tropical forest area in the world, and its flora bears plenty of still unexplored or underutilized fruit species. Due to the postulated contribution to a promotion of beneficial health effects, interest has arisen in exploiting new and exotic types of fruits during recent years. Bacuri seems to be a prospective source of health supporting phytochemicals and therefore a suitable source of economically accessible nutraceutical preparations. Moreover, they may also represent an opportunity for local growers to reach niche markets, increasing their revenues. However, this edible fruit has not attained economic importance as there are insufficient studies regarding commercialization possibilities, chemical composition, crop growing conditions and postharvest.
REFERENCES Aguiar, L.P., Figueiredo, R.W., Alves, R.E., Maia, G.A., Souza, V.A.B., 2008. Caracterizac¸a˜o fı´sica e fı´sico-quı´mica de frutos de diferentes geno´tipos de bacurizeiro (Platonia insignis Mart.). Cieˆncia e Tecnologia de Alimentos. 28, 423428. Calzavara, B.B.G., 1970. Fruteiras: abieiro, abricozeiro, bacurizeiro, biribazeiro, cupuac¸ueiro. IPEAN- Cultura da Amazoˆnia. 1, 6368. Canuto, G.A.B., Xavier, A.A.O., Neves, L.C., Benassi, M.T., 2010. Caracterizac¸a˜o fı´sico-quı´mica de polpas de frutos da amazoˆnia e sua correlac¸a˜o com a atividade anti-radical livre. Revista Brasileira Fruticultura. 32 (4), 11961205. Carvalho, J.D., Mu¨ller, C.H., Lea˜o, N.V.M., 1998. Cronologia dos eventos morfolo´gicos associados a` germinac¸a˜o e sensibilidade ao dessecamento em sementes de bacuri (Platonia insignis Mart. -Clusiaceae). Revista Brasileira de Sementes. 20 (2), 236240. Cavalcante, P.B., 1996. Frutas comestı´veis da Amazoˆnia. CNPq/Museu Paraense Emı´lio Goeldi, Bele´m. Clereci, M.T.P.S., Carvalho-Silva, L.B., 2011. Nutritional bioactive compounds and technological aspects of minor fruits grown in Brazil. Food Resour. Int. 44 (7), 16581670. Ferreira, F.R., Ferreira, S.A.N., Carvalho, J.E.U., 1987. Espe´cies frutı´feras pouco exploradas com potencial econoˆmico e social para o Brasil. Revista Brasileira de Fruticultura. 9, 1122. Fonseca, E.T., 1954. Frutas do Brasil. MEC, Rio de Janeiro. Homma, A., Carvalho, J.E.U., Menezes, A.J.E.A., 2011. Bacuri: fruta amazoˆnica em ascensa˜o. Cieˆncia Hoje. 46 (271), 4145. Lorenzi, H., Bacher, L.B., Lacerda, M.T.C., Sartori, S.F., 2006. Frutas Brasileiras e Exo´ticas Cultivadas. Instituto Plantarum de Estudos da Flora Ltda, Sa˜o Paulo. Manica, I., 2000. Frutas nativas, silvestres e exo´ticas: Te´cnicas de produc¸a˜o e mercado: abiu, amora-preta, arac¸a´, bacuri, biriba´, carambola, cereja-doreo-grande, jabuticaba. Cinco Continentes, Porto Alegre. Menezes, A.J.E.A., Scho¨ffel, E.R., Homma, A.K.O., 2010. Caracterizac¸a˜o de sistemas de manejo de bacurizeiro (Platonia insignis Mart.) nas mesorregio˜es do Nordeste Paraense e do Marajo´, Estado do Para´. Amazoˆnia: Cieˆncia & Desenvolvimento. 6 (11), 4962. Ministry of the EnvironmentBrazil. Amazoˆnia. Available in: ,http://www.mma.gov.br/biomas/amaz%C3%B4nia. (accessed 28.07.15). Moraes, V.H.D.F., Mu¨ller, C.H., Souza, D.A.G.C., Antonio, I.C., 1994. Native fruit species of economic potential from the Brazilian Amazon. Angew. Botanik. 68 (1), 4752. Rufino, M.S.M., Fernandes, F.A.N., Alves, R.E., Brito, E.S., 2009. Free radical-scavenging behaviour of some north-east Brazilian fruits in a DPPH system. Food Chem. 114 (2), 693695.
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Santos, M.D.S.S.A., 1982. Caracterizac¸a˜o fı´sica, quı´mica e tecnolo´gica do bacuri (Platonia insignis Mart.) e seus produtos. Dissertac¸a˜o (Mestrado em Tecnologia de Alimentos)-Universidade Federal do Ceara´, Brasil, Fortaleza, p. 75. Santos, P.R.P., Carvalho, R.B.F., Costa Ju´nior, J.S., Freitas, R.M., Feitosa, C.M., 2013. Levantamento das propriedades fı´sico-quı´mcas e farmacolo´gicas de extratos e compostos isolados de Platonia insignis Mart. uma perspectiva para o desenvolvimento de fitomedicamentos. Revista Brasileira de Farma´cia. 94 (2), 161168. Souza, V.D., Arau´jo, E.C.E., Vasconcelos, L.F.L., Lima, P.D.C., 2001. Variabilidade de caracterı´sticas fı´sicas e quı´micas de frutos de germoplasma de bacuri da Regia˜o Meio-Norte do Brasil. Revista Brasileira de Fruticultura. 23 (3), 677683. Teixeira, G.H.D.A., 2000. Frutos do bacurizeiro (Platonia insignis Mart): caracterizac¸a˜o, qualidade e conservac¸a˜o. Dissertac¸a˜o (Mestrado em Agronomia)-Faculdade de Cieˆncias Agra´rias e Veterina´rias, Universidade Estadual Paulista, Brasil, Jaboticabal, p. 106. Teixeira, G.H.D.A., Durigan, J.F., Lima, M.A., Alves, R.E., Filgueiras, H.A.C., 2005. Postharvest changes and respiratory pattern of bacuri fruit (Platonia insignis Mart.) at different maturity stages during ambient storage. Acta Amazoˆnica. 35 (1), 1721. Villachica, H., Carvalho, J.E.U., Mu¨ller, C.H., Diaz, S.C., Almanza, M., 1996. Frutales y hortalizas promissoras de la Amazoˆnia. Tratado de Cooperacio´n Amazoˆnica. 44, 152156.
Breadfruit—Artocarpus altilis (Parkinson) Fosberg Diane Ragone National Tropical Botanical Garden, Kalaheo, HI, United States
Chapter Outline Introduction Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value
53 53 54 55 55 55
Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgments References
57 57 58 59 59
INTRODUCTION Breadfruit has a long and storied history of cultivation and use. After decades of decline in many regions, there is a renewed interest in promoting breadfruit as a nutritious food for food security, and encouraging the planting of trees for regenerative agriculture, agroforestry, home gardens, and income generation. In the past decade, numerous scientists, farmers, educators, aid agencies, government and nongovernmental agencies, and food processors convened in Fiji (Ragone and Taylor, 2007), Trinidad and Tobago (Roberts-Nkrumah and Duncan, 2016), and American Samoa, to share and discuss ideas, research, projects, and programs to take breadfruit into the 21st century and beyond.
CULTIVAR ORIGIN AND BOTANICAL ASPECTS The Pacific Islands are the center of origin and diversity for breadfruit (Artocarpus altilis (Parkinson) Fosberg) where it has been grown for several millennia. A. altilis was derived from a seeded, diploid ancestral species, Artocarpus camansi Blanco (see Fig. 1), native to Papua New Guinea and possibly the Philippines (Ragone, 2006a,b; Zerega et al., 2005, 2015). Hundreds of indigenous cultivars of breadfruit have been selected and cultivated in Oceania, representing a range of seeded and few-seeded diploids (2n) and seedless triploids (3n) (Ragone, 1997, 2001) (see Fig. 1). Historically, fewer than 10 seedless Polynesian cultivars of A. altilis have been distributed to other tropical regions. The British introduced several Tahitian cultivars to St. Vincent and Jamaica in 1793 (Powell, 1977) and the French introduced a Tongan cultivar (Leakey, 1977) around the same time. These Polynesian cultivars were spread over subsequent decades throughout the Caribbean and into Central and South America, West Africa, the Indian Ocean islands, and Southeast Asia. Breadfruit is now grown in 90 countries (Ragone and Cavaletto, 2006). In most of these areas breadfruit cultivars are generally referred to as “Yellow” or “White.” However, numerous local cultivar names have been documented in St. Vincent (Roberts-Nkrumah, 1997). Breadfruit was introduced from the Pacific directly to Australia in the 19th century. Seeded A. camansi (breadnut, chataigne, castan˜a) (Ragone, 2006b) (Fig. 1) was also distributed by the French in the late 1700s and widely disseminated along with seedless breadfruit. It is often considered to be a seeded form of breadfruit, and frequently identified in the literature as A. altilis, but is a distinct species (Aurore et al., 2014). A. altilis and A. camansi are still inaccurately designated by some authors as Artocarpus communis, or more rarely, Artocarpus incisa or Artocarpus incisus. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00009-5 © 2018 Elsevier Inc. All rights reserved.
53
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FIGURE 1 Artocarpus camansi Blanco (breadnut) and seeded and seedless varieties of Artocarpus altilis (Parkinson) Fosberg (breadfruit) (from left to right). Photos r Jim Wiseman.
Breadfruit is a member of the Artocarpus (Moraceae) genus which contains approximately 70 species from India eastwards into Oceania (Zerega et al., 2004, 2005, 2015; Zerega and Ragone, 2016). This attractive long-lived perennial tree grows to 1520 m in height with large glossy alternate dark-green leaves ranging from almost entire to deeply dissected. Milky white sap (latex) is present in all parts of the tree (Ragone, 1997; Zerega et al., 2004, 2005). Breadfruit is monoecious with male and female flowers occurring on the same tree. The male inflorescence is an elongated club shape, up to 45 cm long, comprised of thousands of tiny flowers attached to a central spongy core. The female inflorescence, or syncarp, consists of 15002000 reduced flowers attached to a spongy core (Ragone, 1997; Zerega et al., 2005). The flowers fuse together and develop into the skin and fleshy, edible portion of the fruit. Breadfruit is considered to be parthenocarpic with the fruit developing without pollination; an important attribute for seedless triploid cultivars, which are infertile and produce little viable pollen (Ragone, 2001). Fruit are usually round, oval, or oblong, weighing 0.255 kg (Jones et al., 2011, 2013a). Seeded and few-seeded cultivars do produce viable pollen and can cross-pollinate. However, most of the cultivar diversity of breadfruit originated from repeated vegetative reproduction over centuries and somatic mutations resulted in variation in fruit characteristics, leaf morphology, and horticultural traits such as salinity tolerance (Jones et al., 2011, 2013a; Ragone, 1997; Zerega et al., 2004, 2005, 2015). Breadfruit has traditionally been grown as one of many crops in complex, agroforestry systems throughout the Pacific (Elevitch et al., 2014; Elevitch, 2015; Ragone, 2006a). Such diverse systems have multiple benefits. They can help with plant health by providing important ecological functions such as replenishing the litter layer to protect soil and nutrient cycling. Biodiversity may also reduce the incidence of certain pests and diseases. On an ecosystem level, agroforests can function similarly to natural forests in protecting soil and water, fulfilling important watershed functions. Agroforests provide the grower with multiple products, and can increase total yield compared with a single crop.
HARVEST SEASON The breadfruit season in most locations begins around the date the sun reaches zenith prior to the Summer months—a date that varies by latitude—and extends throughout the Summer months (Jones et al., 2010). Timing of precipitation and temperature variation may also play a significant role in breadfruit production and their effects need to be studied. Fruit was produced most frequently between August and January, approximately 34 months after the main season of male flower production for 130 cultivars in a breadfruit germplasm repository at the National Tropical Botanical
Breadfruit—Artocarpus altilis (Parkinson) Fosberg
55
Garden (NTBG) in Maui, Hawaii (Jones et al., 2010). Timing and duration of male flower and fruit production varied from year to year and among cultivars and 10 distinct seasonality groups were identified. Introduction of new cultivars (Redfern, 2007) may allow extended or year-round fruit production in tropical areas that currently only have a limited number of cultivars.
ESTIMATED ANNUAL PRODUCTION Breadfruit begins bearing fruit in 35 years depending upon the cultivar and local environmental conditions and produces nutritious fruit for decades. It is believed that it is one of the most productive crops in the world, yet yield estimates under orchard conditions vary widely, ranging from 16 to 50 t/ha of fruit (fresh weight basis (FW) based on a density of 100 trees/ha) (Jones et al., 2010; Ragone, 1997, 2006). Approximately 5.5 t/ha (FW) were produced in a traditional mixed agroforestry system in Pohnpei, Federated States of Micronesia (Raynor and Fownes, 1991). Lincoln and Lagefoged (2014) estimated that precontact mixed crop breadfruit plantations in Hawaii produced 1.963.61 ha21 (dry weight basis (DW)). Depending upon the cultivar, trees could produce over 250 fruit/year with an average weight of 1.2 kg. The expected yield after 7 years was 5.23 t/ha (FW) based on a density of 50 trees/ha (Liu et al., 2014). This compares favorably with the average global yields of rice, wheat, or corn at 4.1, 2.6, and 4.0 t/ha, respectively (Jones et al., 2011; Liu et al., 2014).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Breadfruit is a chilling-sensitive climacteric fruit with a short postharvest life of 25 days. It has a high postharvest rate of respiration with the climacteric in mature fruit reaching a maximum of 150 6 200 mL CO2/kg per h, while younger, slightly immature fruit had respiratory peaks of 300 6 350 mL CO2/kg per h Ethylene production coincided with complete softening of the fruit with low levels of peak ethylene production at 0.7 6 1.2 and 1.0 6 1.5 mL kg per h, respectively, for mature and immature fruit (Worrell et al., 1998). Fruit can be cooked and used at all stages of development, but is preferred at the starchy, “mature” or “fit” stage. A ripe fruit is one that continues to develop becoming soft and sweet. It can be eaten raw at this stage. Reports on time to maturity of the fruit vary from 9 to 21 weeks after the inflorescence emerges, depending upon the cultivar and fruit growth temperature (Worrell et al., 1998; Latchoumia et al., 2014). The “White” cultivar in Barbados attained the desired stage of maturity at 1519 weeks while an unspecified cultivar in Martinique reached maximum development at week 16. Latchoumia et al. (2014) monitored soluble sugars content during weeks 1118. On a DW basis, fructose content decreased progressively from 67 mg/100 g to 19 mg/100 g. Glucose varied between 37 and 28 mg/100 mg, with a peak at 56 mg/100 g in the 12th week, falling to 12 mg/100 g in the 16th week. Sucrose content varied between 2 and 5 mg/100 g. Sugar content of ripe fruit was not determined.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Breadfruit is an excellent dietary staple and compares favorably with other starchy crops (e.g., plantains, cassava, sweet potato, taro, corn, and white rice) commonly eaten in the tropics. Breadfruit is an energy-rich food, high in complex carbohydrates, low in fat, and a good source of fiber and minerals (Tables 1 and 2). Some cultivars are good sources of antioxidants and pro-vitamin A carotenoids (Table 3). Fruit morphology, protein, mineral content, and total carotenoid contents and carotenoid profiles of a diverse group of 94 cultivars in NTBG’s breadfruit germplasm repository were studied at the mature stage (Jones et al., 2011, 2013b). There were significant cultivar differences and elite cultivars with superior nutritional profiles and fruit characteristics for the fresh fruit market as well as the development of a breadfruit flour industry were identified. Average protein content of fresh fruit was 3.9% (DW) or 1.2% (FW). Protein content of flour ranged from 1.8% to 7.6%. Flour made from the cultivar “Ma’afala” contained 7.6% protein, which is similar to rice (7.4%), and higher than many tropical staples. All of the essential amino acids are found in breadfruit protein, and it is especially rich in phenylalanine, leucine, isoleucine, and valine (Liu et al., 2015). The protein is higher quality protein than staples such as corn, wheat, rice, soybean, potato, and pea. A metaanalysis of 41 published papers (Turi et al., 2015) provides a comprehensive overview of the nutritional profile of breadfruit (Tables 13). Cooked breadfruit has a low to moderate glycemic index (4772 GI value) which could be beneficial to control diabetes. By selecting and growing nutrient-rich cultivars, breadfruit’s potential to contribute to food and nutritional security can be maximized.
56
Exotic Fruits Reference Guide
TABLE 1 Minimum and Maximum Reported Values for Breadfruit (Artocarpus altilis and Hybrids) Proximate Analysesa,b Nutrient
Fresh (100 g) Min
Max
Cooked (100 g) Min
Max
Flour (100 g) Min
Max
Ash (%)
0.8
4.6
NA
NA
0.8
6.7
Moisture (%)
19
83
53.2
83.6
2.5
21
Dry matter (%)
17
80.9
16.4
46.8
79
97.5
Energy (kcal)
102
310
80
160.9
279.8
378
Total carbohydrates (g)
14.3
70.1
18.1
37
50
88
Lipid (g)
0.1
4.5
0.1
4.9
0.5
11.8
Protein (g)
0.07
5.2
0.6
11.4
1.9
18.7
Crude fiber (g)
0.9
4.9
1.8
7.4
0.8
15.3
Insoluble fiber (g)
3.1*
25.6*
2.4
20
7.5*
62.3*
Soluble fiber (g)
0.20
0.2
NA
7.2
0.2*
11.4*
a
Reported values were rounded to one decimal place. Values marked with * are extrapolated and based on the calculated average dry weight for breadfruit (fresh 5 37.55%, baked 5 29.35%, flour 5 91.40%). A value of 0 indicates that a specific group was either not detected or below the limits of quantification. Source: From Turi, C., Liu, Y., Ragone, D., Murch, S., 2015. Breadfruit (Artocarpus altilis and hybrids): a traditional crop with the potential to prevent hunger and mitigate diabetes in Oceania. Trends Food Sci. Technol. 45, 264272. b
TABLE 2 Reported Minimum and Maximum Mineral Content for Breadfruit (Artocarpus altilis and Hybrids)a,b Nutrient
Fresh (100 g)
Cooked (100 g)
Flour (100 g)
Min
Max
Min
Max
Min
Max
Boron (mg)
0.52
0.52
0.41*
0.41*
1.27*
1.27*
Calcium (mg)
18
54
10
30
5
800
Chlorine (mg)
0
2.0
0*
1.6*
0*
4.9*
Cobalt (μg)
0*
1.1*
0*
0.9*
0
2.7
Copper (mg)
0.08
0.25
0.45
0.45
0.10
4.95
Iron (mg)
0.26
52.0
0
1.1
0.5
12.0
Magnesium (mg)
20
70
14
30
9.9
200
Manganese (mg)
0.04
0.33
0.09
0.30
0.1
2.63
Nickel (mg)
0
0.08
0*
0.06*
0.08
0.19*
Phosphorus (mg)
7
116
18
41
74
1920
Potassium (mg)
289
2390
240
522
67
2830
Sodium (mg)
3
27
2
70
2
598
Sulfur
20
31
16*
24*
49*
76*
Zinc (mg)
0.09
0.53
0
0.13
0.13
2.97
a Reported values were rounded as follows: nearest nearest whole number (calcium, magnesium, phosphorus, potassium, sodium, sulfur), to one decimal place (chlorine, cobalt, iron), and two decimal places (boron, copper, manganese, nickel, zinc). b Values marked with * are extrapolated and based on the calculated average dry weight for breadfruit (fresh 5 37.55%, baked 5 29.35%, flour 5 91.40%). A value of 0 indicates that a specific group was either not detected or below the limits of quantification. Source: From Turi, C., Liu, Y., Ragone, D., Murch, S., 2015. Breadfruit (Artocarpus altilis and hybrids): a traditional crop with the potential to prevent hunger and mitigate diabetes in Oceania. Trends Food Sci. Technol. 45, 264272.
Breadfruit—Artocarpus altilis (Parkinson) Fosberg
57
TABLE 3 Minimum and Maximum Carotenoid and Vitamin Content for Breadfruit (Artocarpus altilis and hybrids)a,b Nutrient
Fresh (100 g)
Cooked (100 g)
Flour (100 g)
Min
Max
Min
Max
Min
Max
Total carotenoids (μg)
0
3769
0
1260
0*
6549*
Alpha carotene (μg)
0
260
0
142
0*
538*
Beta carotene (μg)
0
3410
0
868
0*
5502*
Beta cryptoxanthin (μg)
0
3.3
0
10.6
0*
21*
Lutein (μg)
0
690
0
759
0*
2022*
Lycopene (μg)
0
48.7
0
25.9
0*
100*
Zeaxanthin (μg)
0
60
0
70
0*
182*
Folic acid (μg)
0*
1.3*
0
1.0
0*
3.1*
Vitamin B1 (mg)
0.12
0.28
0.09
0.14
0.29
0.56*
Vitamin B2 (mg)
0.05
0.10
0.02
0.06
0.16
0.39
Vitamin B3 (mg)
0.84
1.70
0.64
1.40
2.30
4.38
Vitamin C (mg)
16.2
21.0
1.6
12.1
0
22.7
a
Reported values were rounded to one decimal place. Values marked with * are extrapolated and based on the calculated average dry weight for breadfruit (fresh 5 37.55%, baked 5 29.35%, flour 5 91.40%). A value of 0 indicates that a specific group was either not detected or below the limits of quantification. Source: From Turi, C., Liu, Y., Ragone, D., Murch, S., 2015. Breadfruit (Artocarpus altilis and hybrids): a traditional crop with the potential to prevent hunger and mitigate diabetes in Oceania. Trends Food Sci. Technol. 45, 264272. b
SENSORY CHARACTERISTICS The “White” cultivar in Barbados was rated for palatability, maturity, flavor, sweetness, texture, and discoloration at six stages of development to ascertain the preferred stage of maturity for consumption (Worrell et al., 1998). Mature fruit in the 1519 week age range were deemed acceptable. Twenty cultivars in NTBG’s germplasm repository were evaluated for 14 sensory traits (Ragone and Cavaletto, 2006). The goal was to provide an objective descriptive characterization of the cultivars’ sensory properties, not to determine acceptability or preference. There were significant differences in aroma, visual texture, flavor intensity, sweetness, starchiness, moistness, stringiness, firmness, and color. The greatest differences were in color and texture. Skin, pulp color, and texture of 21 breadfruit cultivars grown in Trinidad and Tobago were assessed using sensory and instrument methods (Daley et al., 2016). Sensory evaluation identified a range of skin, pulp color, and skin textures. Instrument assessment of skin and pulp color and texture showed significant variability among cultivars and a moderate, but significant, linear relationship existed between sensory skin and pulp color and instrument color parameters. Consumer attitudes, consumption characteristics, the most common cooking methods, and cultivar preference for the “Yellow” and “White” cultivars in Trinidad were studied (Roberts-Nkrumah and Badrie, 2005). Most consumers rated the “Yellow” cultivar as being superior to the “White” cultivar, primarily in taste, and used a wider range of methods to prepare it.
HARVEST AND POSTHARVEST CONSERVATION Production manuals available to guide breadfruit growers include NWC (2005), Webster (2006), Elevitch et al. (2014), and Roberts-Nkrumah (2015). Although breadfruit is edible at any stage of development, it is necessary to understand and recognize the different stages of fruit development and maturity, and harvest fruit at the optimal stage for the desired market or use. Fruit picked too green and still immature have a longer shelf life than fruit harvested at the full mature stage, but fruit at this stage is undesirable for most consumers and processors. Determining the optimal stage of maturity to harvest fruit is essential and the grower must rely upon visual cues such as skin color, scabbing on and
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Exotic Fruits Reference Guide
around fruit sections, skin texture changes, and less reliably, deposition of dried latex on the surface (Elevitch et al., 2014). Proper handling will increase shelf life and fruit quality, reduce losses, and help maintain and enhance product value and desirability. The fruit is susceptible to bruising—causing discoloration of the skin and flesh and release of latex— ripening, and decay, when handled improperly. Tall trees are difficult and dangerous to harvest and fruit can easily be damaged by dropping. Fruit never touching the ground is a key element of food safety best practices. Controlling tree size through regular pruning is an essential component of an efficient and effective harvesting program. Minimizing field heat and heat generated from internal respiration is crucial. Harvest in the early morning and immediately cut off the stem and place cut side down until the flow of latex stops. Keep in well-ventilated open boxes placed in the shade. Other options for field cooling include placing the fruit in tubs containing icy water for 1015 min. The fruit quickly cools as the ice melts. Prolonged storage in icy water may cause brown discoloration of the skin due to chilling injury. Fruit fully submerged in cool, clean fresh water can maintain quality for several days or longer. A gentle rinsing with water, air blowing, or gently brushing with a soft bristle brush can be used to remove loose debris from the surface of the fruit, particularly around the stem where organic debris and insects tend to accumulate. Pressure washing or vigorous brushing should be avoided. There are currently no nationally or internationally accepted grading standards for breadfruit, with the desired size and weight varying by cultivar and market. Suggested grading standards are provided by NWC (2005). Fruit precooled to an internal temperature of 16 C were stored untreated or in sealed polyethylene bags under ambient and refrigerated conditions (Maharaj and Sankat, 1990). At 28 C untreated fruits lasted only 23 days before softening while those stored in water had a maximum shelf life of 5 days. Fruits sealed in polyethylene bags had a shelf life of 57 days and waxed fruits lasted 8 days. Shelf life was markedly increased by refrigeration. Satisfactory fruit quality can best be maintained at 1216 C as the fruit skin turns an undesirable brown at colder temperatures. A shelf life of 10 days appears possible for untreated fruit and 14 days for packaged fruits 1216 C. Fruit kept at 16 C in atmospheric containers of 5% carbon dioxide and 5% oxygen showed significantly less skin browning and remained firm for 25 days.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Greater utilization of breadfruit is hindered by its perishability. Processing fruit into chips and other snacks, fries, beverages, dips, fruit bars, baked goods, and other value-added products is fundamental to using the fruit and expanding markets. Pacific islanders used pit storage, a semianaerobic fermentation process involving intense acidification that transforms mature starchy fruit into a long-lasting doughy form (Ragone, 1997, 2002). Breadfruit has been fermented and processed into a product comparable to fermented cassava, an important dietary staple in West Africa (Adeniran et al., 2012; Adeniran and Ajifolokun, 2015). Widespread interest in gluten-free flours has begun driving efforts to process breadfruit into flour. The flour, and flour-based value-added products, are bringing greater attention to breadfruit as a crop for food security and sustainability as well as economic development. Potential demand for breadfruit flour will expand and complement existing and potential markets for fresh or processed fruit. The nascent breadfruit flour industry currently involves researchers, farmers, cooperatives, and entrepreneurs in Hawaii, Samoa, the Caribbean, Central America, and West Africa who are producing small quantities of flour for local use and for export (Ragone, 2016). Basic guidelines to drying and grinding breadfruit into flour have been produced by Jones et al. (2011), NARI (2010), CTI (2012), TTFF (2016), and Murch and Ragone (2016). Theoretical models for drying agricultural produce (Chinweuba et al., 2016) were tested for shredded breadfruit using varying temperature, air velocity, humidity, and initial moisture content variables (George et al., 2016). Regulatory issues regarding the use of breadfruit flour in North America have recently been addressed. Health Canada determined in 2015 that breadfruit and flour derived from it would not be considered a novel food or novel food ingredient and these products are not subject to premarket notification under B.28.002 of the Food and Drug Regulations (Ragone, 2016). The US Food and Drug Administration (FDA) approved an application for breadfruit flour to be granted “Generally Recognized as Safe” status (FDA, 2016). Producers of breadfruit flour and other products who are based outside of the United States will need to use facilities that comply with the FDA Food Safety Modernization Act to ensure food safety and will also need to register food production facilities in compliance with the Public Health Security and Bioterrorism Preparedness and Response Act of 2002 (FDA, 2015) in order to market their products in the United States.
Breadfruit—Artocarpus altilis (Parkinson) Fosberg
59
The fruit, and some of the byproducts of breadfruit processing, can be used as livestock feed (Ragone, 1997). There are secondary and tertiary products such as latex, ethanol, and carbon credits that could develop from a global breadfruit market (Jones et al., 2011). Insecticides derived from extracts of the male inflorescence have promising potential (Jones et al., 2012). Regions where breadfruit can be grown (Lucas and Ragone, 2012) are among the poorest in the world. By developing a global market for an environmentally sustainable, locally grown nutritious crop, these regions would strengthen their positions in the global economy as well as improving economic conditions locally.
ACKNOWLEDGMENTS The author is grateful to the Trustees and Fellows of NTBG for their support of the Breadfruit Institute and its mission to promote the conservation, study, and use of breadfruit for food and reforestation. A global renaissance in breadfruit would not be possible without the myriad individuals and organizations throughout the world who are working to make breadfruit an important staple crop for the tropics.
REFERENCES Adeniran, A.H., Gbadamosi, S.O., Omobuwajo, T.O., 2012. Microbiological and physico-chemical characteristics of fufu analogue from breadfruit (Altocarpus altilis F). Int. J. Food Sci. Technol. 47, 332340. Adeniran, H.A., Ajifolokun, O.M., 2015. Microbiological studies and sensory evaluation of breadfruit and cassava co-fermented into gari analogue. Niger. Food J. 33, 3947. Aurore, G., Nacitas, J., Parfait, B., Fahrasmane, L., 2014. Seeded breadfruit naturalized in the Caribbean is not a seeded variety of Artocarpus altilis. Genet. Resour. Crop Evol. 61, 901907. Chinweuba, D.C., Nwakuba, R.N., Okafor, V.C., Nwajinka, C.O., 2016. Thin layer drying modelling for some selected Nigerian produce: a review. Am. J. Food Sci. Nutr. Res. 3, 115. CTI, 2012. Breadfruit Flour: Tools that Empower Communities. Compatible Technology International, St. Paul, MN. Daley, O.O., Roberts-Nkrumah, L.B., Alleyne, A.T., 2016. Sensory and instrument assessment of colour and texture among breadfruit [Artocarpus altilis (Parkinson) Fosberg] cultivars. Tropical Agriculture (Trinidad). In: Special Issue International Breadfruit Conference 2015, pp. 92108. Elevitch, C., Ragone, D., Cole, I., 2014. Breadfruit Production Guide: Recommended Practices for Growing, Harvesting, and Handling. second ed Breadfruit Institute, National Tropical Botanical Garden & Hawaii Homegrown Food Network, Hawaii. Elevitch, C.R. (Ed.), 2015. Food-Producing Agroforestry Landscapes of the Pacific: Creating Abundant and Resilient Food Systems. Permanent Agriculture Resources, Holualoa, HI. FDA, 2015. Guidance & Regulation. ,http://www.fda.gov/Food/GuidanceRegulation/FSMA/ucm268229.htm.; ,http://www.fda.gov/Food/ GuidanceRegulation/FoodFacilityRegistration/ucm2006831.htm.. FDA, 2016. GRAS Notice (GRN) No. 596. ,http://www.accessdata.fda.gov/scripts/fdcc/?set 5 GRASNotices&id 5 596.. George, C., Mogil, Q., Andrews, M., Ewing, G., 2016. Thin layer drying curves for shredded breadfruit (Artocarpus altilis). J. Food Process. Preserv.18. Jones, A.M.P., Murch, S.J., Ragone, D., 2010. Diversity of breadfruit (Artocarpus altilis, Moraceae) seasonality: a resource for year-round nutrition. Econ. Bot. 64, 340351. Jones, A.M.P., Ragone, D., Aiona, K., Lane, W.A., Murch, S.J., 2011. Nutritional and morphological diversity of breadfruit (Artocarpus, Moraceae): identification of elite cultivars for food security. J. Food Compos. Anal. 24, 10911102. Jones, A.M.P., Klun, J.A., Cantrell, C.L., Ragone, D., Chauhan, K.R., Brown, P.N., et al., 2012. Isolation and identification of mosquito (Aedes aegypti) biting deterrent fatty acids from male inflorescences of breadfruit (Artocarpus altilis (Parkinson) Fosberg). J. Agric. Food Chem. 60, 28673873. Jones, A.M.P., Murch, S.J., Wiseman, J., Ragone, D., 2013a. Morphological diversity in breadfruit (Artocarpus, Moraceae): insights into domestication, conservation, and cultivar identification. Genet. Resour. Crop Evol. 60, 175192. Jones, A.M.P., Baker, R., Ragone, D., Murch, S.J., 2013b. Identification of pro-vitamin A carotenoid-rich cultivars of breadfruit (Artocarpus, Moraceae). J. Food Compos. Anal. 31, 5161. Latchoumia, J.N., Adenet, S., Aurore, G., Rochefort, K., Bule´on, A., Fahrasmane, L., 2014. Composition and growth of seedless breadfruit Artocarpus altilis naturalized in the Caribbean. Sci. Hortic. 175, 187192. Leakey, C.L.A., 1977. Breadfruit Reconnaissance Study in the Caribbean Region. CIAT/Inter American Development Bank, Bogota. Lincoln, N., Lagefoged, T., 2014. Agroecology of pre-contact Hawaiian dryland farming: the spatial extent, yield and social impact of Hawaiian breadfruit groves in Kona, Hawai’i. J. Archaeol. Sci. 49, 192202. Liu, Y., Jones, A.M.P., Murch, S.J., Ragone, D., 2014. Crop productivity, yield, and seasonality of breadfruit (Artocarpus spp.) Moraceae. Fruits. 69, 345361. Liu, Y., Ragone, D., Murch, S.J., 2015. Breadfruit (Artocarpus altilis): a source of high-quality protein for food security and novel food products. Amino Acids. 47, 847856. Lucas, M.P., Ragone, D., 2012. Will breadfruit solve the world hunger crisis? New developments in an innovative food crop. ArcNews. Summer, 67. Maharaj, R., Sankat, C.K., 1990. The shelf-life of breadfruit stored under ambient and refrigerated conditions. Acta Hortic. 269, 411424.
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Murch, S.J., Ragone, D., 2016. How to Dry and Grind Breadfruit into Flour. Breadfruit Institute, National Tropical Botanical Garden, Kalaheo, Hawaii. NARI, 2010. Breadfruit flour. In: Homenauth, O. (Ed.), Agroprocessing Manual. The Guyana Ministry of Agriculture Agro Advertising & Marketing Service, Georgetown, p. 29. NWC, 2005. A Manual for the Growing and Marketing of Breadfruit for Export. Nature’s Way Cooperative (Fiji) Ltd, Nadi, Fiji. Powell, D., 1977. Voyage of the Plant Nursery, HMS Providence. 17911793. Econ. Bot. 31, 387431. Ragone, D., 1997. Breadfruit: Artocarpus altilis (Parkinson) Fosberg. Promoting the Conservation and Use of Underutilized and Neglected Crops 10. IPGRI, Rome. Ragone, D., 2001. Chromosome numbers and pollen stainability of three species of Pacific Island breadfruit (Artocarpus, Moraceae). Am. J. Bot. 88, 693696. Ragone, D., 2002. Breadfruit storage and preparation in the Pacific Islands. In: Yoshida, S., Matthews, P.J. (Eds.), Vegeculture in Eastern Asia and Oceania, JCAS Symposium Series 16. Japan Center for Area Studies, National Museum of Ethnology, Osaka, pp. 217232. Ragone, D., 2006a. Artocarpus altilis (breadfruit). In: Elevitch, C.R. (Ed.), Traditional Trees of Pacific Islands. Permanent Agriculture Resources, Holualoa, HI, pp. 85100. Ragone, D., 2006b. Artocarpus camansi (breadnut). In: Elevitch, C.R. (Ed.), Traditional Trees of Pacific Islands. Permanent Agriculture Resources, Holualoa, HI, pp. 101110. Ragone, D., 2016. Breadfruit for food and nutrition security in the 21st century. Tropical Agriculture (Trinidad). In: Special Issue International Breadfruit Conference 2015, pp. 1829. Ragone, D., Cavaletto, C.G., 2006. Sensory evaluation of fruit quality and nutritional composition of 20 breadfruit (Artocarpus, Moraceae) cultivars. Econ. Bot. 60, 335346. Ragone, D. and Taylor, M.B. (Eds.), 2007. I International Symposium on Breadfruit Research and Development. Acta Hortic. 757. Raynor, W.C., Fownes, J.H., 1991. Indigenous agroforestry of Pohnpei. 1. Plant species and cultivars. Agroforest. Syst. 16, 139157. Redfern, T.N., 2007. Breadfruit improvement activities in Kiribati. Acta Hortic. 757, 9399. Roberts-Nkrumah, L.B., 1997. Towards a description of the breadfruit germplasm in St. Vincent. Fruits. 52, 2735. Roberts-Nkrumah, L.B., 2015. Breadfruit and Breadnut Orchard Establishment and Management. FAO, Rome. Roberts-Nkrumah, L.B., Badrie, N., 2005. Breadfruit consumption, cooking methods and cultivar preference among consumers in Trinidad, West Indies. Food Qual. Pref. 16, 267274. Roberts-Nkrumah, L.B., Duncan, E.J. (Eds.), 2016. Proceedings of the International Breadfruit Conference Commercialising Breadfruit for Food and Nutrition Security. Republic of Trinidad and Tobago: The University of the West Indies. TTFF, 2016. Factory in a Box and Breadfruit Flour Production. Trees That Feed Foundation, Winnetka, IL. Turi, C., Liu, Y., Ragone, D., Murch, S., 2015. Breadfruit (Artocarpus altilis and hybrids): a traditional crop with the potential to prevent hunger and mitigate diabetes in Oceania. Trends Food Sci. Technol. 45, 264272. Webster, S.A., 2006. The Breadfruit in Jamaica: A Commercial and Horticultural Perspective. Webster Seymour, Port Antonio. Worrell, D.B., Carrington, C.M.S., Huber, D.J., 1998. Growth, maturation and ripening of breadfruit, Artocarpus altilis (Park.) Fosb. Sci. Hortic. 76, 1728. Zerega, N.J.C., Ragone, D., Motley, T.J., 2004. Complex origins of breadfruit (Artocarpus altilis, Moraceae): implications for human migrations in Oceania. Am. J. Bot. 91, 760766. Zerega, N.J.C., Ragone, D., Motley, T.J., 2005. Systematics and species limits of breadfruit (Artocarpus, Moraceae). Syst. Bot. 30, 603615. Zerega, N.J.C., Ragone, D., 2016. Toward a global view of breadfruit genetic diversity. Tropical Agriculture (Trinidad). In: Special Issue International Breadfruit Conference 2015, pp 7791. Zerega, N., Wiesner-Hanks, T., Ragone, D., Irish, B., Scheffler, B., Simpson, S., et al., 2015. Diversity in the breadfruit complex (Artocarpus, Moraceae): genetic characterization of critical germplasm. Tree Genet. Genomes. 11, 4.
Buriti fruit—Mauritia flexuosa Hector H.F. Koolen1, Felipe M.A. da Silva2, Vitor S.V. da Silva1, Weider H.P. Paz2 and Giovana A. Bataglion2 1
Amazonas State University, Manaus, Brazil, 2Federal University of Amazonas, Manaus, Brazil
Chapter Outline Origin and Botany Origin and Considerations Botanical Aspects Harvest Season and Annual Production Fruit Physiology and Biochemistry Buriti Fruit Morphology Buriti Fruit Nutrient Content
61 61 61 62 62 62 63
Buriti Fruit Metabolites Biological Benefits Sensory Characteristics and Food Application Harvest, Postharvest Conservation and Industrial Applications Acknowledgment References
64 65 66 66 66 66
ORIGIN AND BOTANY Origin and Considerations Mauritia flexuosa L.f. (Arecaceae) is a palm tree (Fig. 1B) native to the Peruvian Amazon that spread through the lowlands of the Amazon, Orinoco, Parana´, and Tocantins basins Santos (2005) (Fig. 1A). Buriti is the most popular name for this palm in Brazil, whereas it is also known as aguaje in Peru, kikyura in Bolivia and moriche in Colombia and Venezuela (Silva et al., 2014). Buriti is the most abundant palm tree in South America, occupying exclusively areas that have hydromorphic soils (Endress et al., 2013), and was the first Amazonian palm tree scientifically described in 1781. Homogenous forests dominated by buriti are easily found in swampy areas of the Amazon region formations known as “buritizais” (Fig. 1C) covering millions of hectares and playing several important ecological roles (Bodmer, 1991; Gurgel-Gonc¸alves et al., 2012).
Botanical Aspects The buriti tree presents remarkable botanical characteristics, which easily discriminates this species from several other palm trees from the huge Amazon biodiversity. Adult specimens present a spherical crown with large composite leaves reaching 6 m long and a group of 1020 leaves is located at the stalk terminal portions (Passos and de Mendonc¸a, 2006). The trunk is cylindrical and smooth, with a diameter of 3060 cm (Fig. 1B), and under favorable conditions, buriti trees can reach 3440 m in height. Buriti roots grow down 60 cm deep and then develop horizontally reaching as far as 40 m (Santos, 2005). Aerial roots are observed under hydromorphic conditions to allow respiration (Fig. 2B). The buriti palm is polygamous, having female, male, or bisexual flowers that appear from December to April. The “female” is the one that produces the fruit, but it needs the “male” flower to be pollinated. The male flowers are orange in color and have pineapple-like spikelets. Each spikelet contains approximately 115 flowers, which adds up to 45,000 flowers per blossom (Fig. 2E). The female flowers are orange colored and become brighter and more fragrant during the reproductive stage (Santos, 2005).
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00004-6 © 2018 Elsevier Inc. All rights reserved.
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Exotic Fruits Reference Guide
FIGURE 1 (A) Buriti distribution through South America with the Amazon basin highlighted. (B) A buriti palm tree. (C) A buritizal next to a water source in the municipality of Manaus, Amazonas state, Brazil (2 420 26.4vS, 60 020 55.7vW).
HARVEST SEASON AND ANNUAL PRODUCTION Each buriti palm produces an average of eight blossoms, and each blossom produces approximately 500 fruits (Fig. 2A). Hence, the estimated average production is 290 kg per palm tree per year. From a single hectare of “buritizal,” approximately, 23 tons of fruits per year can be produced and the oil yield can reach 380 kg (Sampaio et al., 2008). The harvest season goes from December to July, with a maximum yield at April (Santos, 2005). The propagation of buriti occurs through seeds, with a germination period of 75 days at 30 C (Silva et al., 2014). A study that measured the ethylene and CO2 levels, as well as the metabolic responses of buriti to such compounds throughout the process of development and maturation, classified buriti cultivated in the Amazon region as a climacteric fruit (Milanez et al., 2016). Its ideal harvest point should be 210 days after anthesis (fully open and functional) (Milanez et al., 2016).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Buriti Fruit Morphology Buriti fruits are drupoid and oblongellipsoid in shaped. The fruit is composed of about 20% skin, 10%20% mesocarp, 15%20% endocarp, and 40%45% seed (until three seeds per fruit) (Santos, 2005). According to Silva et al.
Buriti fruit—Mauritia flexuosa
63
FIGURE 2 (A) A buriti blosson. (B) Aerial roots from a buriti specimen. (C) Buriti fruit. (D) Cross-section of a buriti fruit. (E) Buriti flowers.
(2014), buriti’s pericarp does not develop a lignified endocarp and the exocarp is covered with diamond-shaped, juxtaposed, reddish-brown scales (Fig. 2C). The pulp, 46 mm thick, has an orange color with a sweet aroma, oily texture, and pasty consistence (Silva et al., 2014) (Fig. 2D). Globular or semispherical seeds, with the raphe aligned along their longitudinal axis and a prominent operculum, form a small depression (Silva et al., 2014) (Fig. 2D).
Buriti Fruit Nutrient Content Among all the parts of buriti fruit, the edible part (pulp) is the most explored in relation to nutrient content. Macromolecules (proteins, carbohydrates, and lipids), micronutrients (minerals), water, ash, moisture, and fiber contents in buriti pulps have been described (Santos, 2005; Lognay et al., 1987; Va´squez-Ocmı´n et al., 2009; Escriche et al., 1999; Carrera, 2000; Caˆndido et al., 2015) (see also Table 1). In some cases, considerable variations are observed, which may be due to different analyzed cultivars, and by the existence of different morphotypes. The water content of the edible part normally ranges from 50% to 70% (Santos, 2005) and fibers constitute approximately 10% of the weight. The crude fat content normally reaches values around 20 g/100 g, justifying its oily texture (Va´squez-Ocmı´n et al., 2009). The carbohydrate content for buriti pulp reaches values around 20 g/100 g, indicating that buriti is a prolific source of this class of macromolecules. Further studies confirmed this statement, carbohydrate fractions of buriti showed to be composed mainly by arabinan-rich pectic (Cantu-Jungles et al., 2015) and unusual linear polysaccharides (Cordeiro et al., 2015). The crude protein level in buriti pulp achieves values around 1.8 g/100 g, as described previously (Mariath et al., 1989). The ash amount normally ranges from 0.7 to 1.9 g/100 g and presents potassium as the most recurrent microelement, followed by calcium, magnesium, and phosphorous (Va´squez-Ocmı´n et al., 2009) (Table 1). Vitamins, mainly provitamins A (carotenoids and tocopherols), are responsible for some of the biological benefits observed from the regular intake of the buriti pulps and/or its oil (Santos et al., 2013a; Bataglion et al., 2015a).
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Exotic Fruits Reference Guide
TABLE 1 Nutritional Content of Buriti Fruit Pulp Total a
Energy (kcal)
145
Water (%)
69
Crude fiber (%) d
b
143
62c
10 5.1e
Protein (g)
1.8
Carbohydrate (g)
20
Lipids (g)
10
22
24
Ash (g)
0.71.9
potassiumc
ironc
660
0.83
6.2
c
Vitamins (mg)
32
20 a
phosphorusa
zincc
19
0.65 c
sodium
0.43 g,h
25
c
copper
3.0f
a
manganese
calciumc
98
132 a
thiamine
riboflavin
niacin
ascorbic acidc
0.03
0.2
0.7
25
a
Santos et al. (2005). Lognay et al. (1987). Va´squez-Ocmı´n et al. (2009). d Expressed as grams per 100 g of buriti fresh pulp (g/100 g). e Escriche et al. (1999). f Carrera (2000). g Caˆndido et al. (2015). h Expressed as milligrams per 100 g of buriti fresh pulp (mg/100 g). b c
BURITI FRUIT METABOLITES Secondary metabolites are natural products that play a highly significant role in drug discovery and development processes. As opposed to macromolecules and micronutrients, secondary metabolites are not directly involved in the normal growth, development, or reproduction of the plants. However, secondary metabolites possess many biological benefits for humans (da Silva et al., 2014). In this sense, chemical and pharmaceutical investigations have been conducted to correlate the chemical composition with biological benefits from a regular intake of buriti (Koolen et al., 2013). Tetraterpenoids, also referred to as provitamins A, are the main class of compounds present in buriti pulps (52.86 mg/100 g) with more than 20 different individuals previously identified (Caˆndido et al., 2015). Carotenes, mainly β-carotene ((1) in Fig. 3), are the main tetraterpenoids in buriti pulps. In addition, most of the different tetraterpenoids are derivatives from 1. In minor proportions, xanthophylls, that are oxygenated tetraterpenoids, e.g., α-cryptoxanthin (2), are also observed in buriti pulp (Caˆndido et al., 2015). Besides provitamins, buriti fruit also possess polyphenols in much lower levels (378.0 mg/100 g), which composition has been studied over the past few years (Bataglion et al., 2014a). Protocatechuic acid (3) was observed as the main phenolic compound in buriti pulp (2.1 mg/g), followed by ()-epicatechin (4, 1.2 mg/g), chlorogenic acid (5, 1.1 mg/g), luteolin (6, 1.0 mg/g), (1)-catechin (7, 0.9 mg/g), and caffeic acid (8, 0.8 mg/g) (Bataglion et al., 2014a). Beyond catechins, hydroxybenzoic acids (9, gallic acid), anthocyanins (10, cyanidin-3-glucoside and 11, cyanidin-3-rutinoside), flavonoid O-glucosides (12, rutin), and flavonoid C-glucosides (13, vixetin and 14, scoparin) were identified in buriti (Koolen et al., 2013). Several studies have also explored the composition of the oil obtained from cold pressing procedures with buriti fruits (Bataglion et al., 2014b). Triacylglicerides and fatty acids (Santos et al., 2013b; Bataglion et al., 2015a), mainly composed by palmitic, oleic, and stearic acids (1517), are the main compounds classes in buriti’s oil. Tocopherols, mainly α- and β-tocopherols (18 and 19) and phytosterols, such as brassicasterol, campesterol, stigmasterol, β-sitosterol, and Δ5-avenasterol (2024) are also biologically relevant compounds present in the oil (Santos et al., 2013a; Bataglion et al., 2015a).
Buriti fruit—Mauritia flexuosa
65
FIGURE 3 Secondary metabolites identified in buriti fruit.
BIOLOGICAL BENEFITS Buriti, as a prolific source of different metabolites, displays several biological benefits for humans (Bataglion et al., 2015b). Commonly, buriti oil is used in the treatment of burns and as a potent vermifuge (Koolen et al., 2012). Buriti showed pharmacological benefits for pregnant women, fetuses, and newborn children to retard weight gain and reflex maturation accelerating the somatic maturation, and also increasing serum and liver retinol deposition (Medeiros et al., 2015). Buriti oil emulsions were able to reduce the damage caused by ultraviolet radiation due to its phenolic composition (Zanatta et al., 2010). Additionally, creams and lotions with buriti displayed low cytotoxicity (Zanatta et al., 2008). Particularly, the most remarkable property of buriti fruit is still its antioxidant capacity, which has been evaluated by different approaches (Koolen et al., 2013). The pulp of the buriti fruit, independent of the morphotypes, is resistant to oxidation, supposedly due to the high levels of β-carotene, tocopherols and oleic acid. Its resistance to oxidation, makes buriti fruit a high quality food source, comparable to olives (Va´squez-Ocmı´n et al., 2010).
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Exotic Fruits Reference Guide
SENSORY CHARACTERISTICS AND FOOD APPLICATION Buriti fruit has unique and noticeable aroma that is not comparable to any other fruit. Regarding its flavor, buriti pulps are in general sweet, with acidity differences according to its morphotypes (Va´squez-Ocmı´n et al., 2009). Buriti fruit has a high economic value in the Amazon region, where local population found many usages for the pulp. Among them, juice, jelly, icecream, popsicles, and yogurt-related products are popular food applications of buriti, especially in Peru and Brazil.
HARVEST, POSTHARVEST CONSERVATION AND INDUSTRIAL APPLICATIONS Buriti is a prime candidate for sustainable management in the Amazon region, as all buriti production in the Amazon comes from extractivism activities (Carrera, 2000). In the Amazon region, buritizais provide cash income for poor rural families, being in some cases the only source of income (Manzi and Coomes, 2009). So far, buriti palms are not planted despite its easy propagation. Industries, mainly cosmetic and food, purchase the raw buriti fruits from extractive cooperatives. After collected, buriti fruits are microbiologically stable at 25 C, if the moisture content is below 10 g of water per 100 g of pulp (Melo et al., 2011). For usage that needs long time of conservation (e.g., pulps for juice production), the dried pulps and fibrous parts of buriti are required as they can be stored frozen for many months. The cosmetic industry dominates the annual purchase of buriti extracted in the Amazon Rain Forest. Several products, especially lotions, creams, soaps, shampoos, and more elaborate products are produced with the buriti oil and exported worldwide (Koolen et al., 2013). The food industry is also a customer of buriti fruit, especially for exploring the pulps for production and exportation of energy drinks, flour, candies, and juices (Santos, 2005). The fibers still require more studies in order to be commercially explored, but preliminary results are encouraging (Santos et al., 2010). In minor proportions, pharmaceutical industries apply buriti seed oil, i.e., rich in lauric acid, into cream-based formulations (Santos, 2005).
ACKNOWLEDGMENT We would like to thank CNPq, FAPEAM, and CAPES for financial support.
REFERENCES Bataglion, G.A., da Silva, F.M.A., Eberlin, M.N., Koolen, H.H.F., 2014a. Simultaneous quantification of phenolic compounds in buriti fruit (Mauritia flexuosa L.f.) by ultra-high performance liquid chromatography coupled to tandem mass spectrometry. Food Res. Inter. 66, 396400. Bataglion, G.A., da Silva, F.M.A., Santos, J.M., dos Santos, F.N., Barcia, M.T., de Lourenc¸o, C.C., et al., 2014b. Comprehensive characterization of lipids from Amazonian vegetable oils by mass spectrometry techniques. Food Res. Inter. 64, 472481. Bataglion, G.A., da Silva, F.M.A., Santos, J.M., Barcia, M.T., Godoy, H.T., Eberlin, M.N., et al., 2015a. Integrative approach using GC-MS and easy ambient sonic-spray ionization mass spectrometry (EASI-MS) for comprehensive lipid characterization of buriti (Mauritia flexuosa) oil. J. Braz. Chem. Soc. 26, 171177. Bataglion, G.A., da Silva, F.M.A., Eberlin, M.N., Koolen, H.H.F., 2015b. Determination of the phenolic composition from Brazilian tropical fruits by UHPLCMS/MS. Food. Chem. 180, 280287. Bodmer, R.E., 1991. Strategies of seed dispersal and seed predation in Amazonia ungulates. Biotropica. 23, 255261. Caˆndido, T.L.N., Silva, M.R., Agostini-Costa, T.S., 2015. Bioactive compounds and antioxidant capacity of buriti (Mauritia flexuosa L.f.) from the Cerrado and Amazon biomes. Food. Chem. 177, 313319. Cantu-Jungles, T.M., de Almeida, C.P., Iacomini, M., Cipriani, T.R., Cordeiro, L.M.C., 2015. Arabinan-rich pectic polysaccharides from buriti (Mauritia flexuosa): An Amazonian edible palm fruit. Carbohydr. Polym. 122, 276281. Carrera, L., 2000. Aguaje (Mauritia flexuosa) A promising crop of the Peruvian Amazon. Acta Hortic. 531, 229236. Cordeiro, L.C.M., de Almeida, C.P., Iacomini, M., 2015. Unusual linear polysaccharides: (1-5)-α-L-Arabinan, (1-3)-(1-4)-α-D-glucan and (1-4)-β-D-xylan from pulp of buriti (Mauritia flexuosa), an edible palm fruit from the Amazon region. Food. Chem. 173, 141146. Endress, B.A., Horn, C.M., Gilmore, M.P., 2013. Mauritia flexuosa palm swamps: Composition, structure and implications for conservation and management. Forest Ecol. Manage. 302, 346353. Escriche, I., Restrepo, J., Serra, J.A., Herrera, L.F., 1999. Composition and nutritive value of Amazonian palm fruits. Food. Nutr. Bull. 20, 361364. Gurgel-Gonc¸alves, R., Cura, C., Schijman, A.G., Cuba Cuba, C.A., 2012. Infestation of Mauritia flexuosa palms by triatomines (Hemiptera: Reduviidae), vectors of Trypanosoma cruzi and Trypanosoma rangeli in the Brazilian savanna. Acta Trop. 121, 105111. Koolen, H.H.F., Soares, E.R., da Silva, F.M.A., de Souza, A.Q.L., Rodrigues Filho, E., de Souza, A.D.L., 2012. Triterpenes and flavonoids from the roots of Mauritia flexuosa. Rev. Bras. Farmacog. 22, 189192.
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Koolen, H.H.F., da Silva, F.M.A., Gozzo, F.C., de Souza, A.Q.L., de Souza, A.D.L., 2013. Antioxidant, antimicrobial activities and characterization of phenolic compounds from buriti (Mauritia flexuosa L. f.) by UPLCESI-MS/MS. Food Res. Inter. 51, 467473. Lognay, G., Trevejo, E., Jordan, E., Marlier, M., Severin, M., de Zarate, O.I., 1987. Investigations on Mauritia flexuosa L. oil. Grasas y Aceites. 38, 303306. Manzi, M., Coomes, O.T., 2009. Managing Amazonian palms for community use: A case of aguaje palm (Mauritia flexuosa) in Peru. Forest Ecol. Manage. 257, 510517. Mariath, J.G.R., Lima, M.C.C., Santos, L.M.P., 1989. Vitamin A activity of buriti (Mauritia vinifera Mart.) and its effectiveness in the treatment and prevention of xerophthalmia. Am. J. Clin. Nutr. 49, 849853. Medeiros, M.C., Aquino, J.S., Soares, J., Figueiroa, E.B., Mesquita, H.M., Pessoa, D.C., et al., 2015. Buriti oil (Mauritia flexuosa L.) negatively impacts somatic growth and reflex maturation and increases retinol deposition in young rats. Inter. J. Develop. Neurosci. 46, 713. Melo, W.S., Pena, R.S., Rodrigues, A.M.C., da Silva, L.H.M., 2011. Hygroscopic behavior of buriti (Mauritia flexuosa) fruit. Food Sci. Technol. 31, 935940. Milanez, J.T., Neves, L.C., da Silva, P.M.C., Bastos, V.J., Shahab, M., Colombo, R.C., et al., 2016. Pre-harvest studies of buriti (Mauritia flexuosa L.F.), a Brazilian native fruit, for the characterization of ideal harvest point and ripening stages. Sci. Hortic. (Amsterdam). 202, 7782. Passos, M.A.B., de Mendonc¸a, M.S., 2006. Epidermis of leaf segments from Mauritia flexuosa L. f. (Arecaceae) on three phases of development. Acta Amazonica. 36, 431436. Sampaio, M.B., Schmidt, I.S., Figueiredo, I.B., 2008. Harvesting effects and population ecology of the buriti palm (Mauritia flexuosa L. f., Arecaceae) in the Jalapa˜o region, Central Brazil. Econ. Bot. 62, 171181. Santos, L.M.P., 2005. Nutritional and ecological aspects of buriti or aguaje (Mauritia flexuosa Linnaeus filius): A carotene-rich palm fruit from Latin America. Ecol. Food. Nutr. 44, 345358. Santos, R.S., Souza, A.A., de Paoli, M.A., Souza, C.M.L., 2010. Cardanolformaldehyde thermoset composites reinforced with buriti fibers: Preparation and characterization. Compos. Part A: Appl. Sci. Manufact. 41, 11231129. Santos, M.F.G., Alves, R.E., Ruı´z-Me´ndez, M.V., 2013a. Minor components in oils obtained from Amazonian palm fruits. Grasas y Aceites. 64, 531536. Santos, M.F.G., Marmesat, S., Brito, E.S., Alves, R.E., Dobarganes, M.C., 2013b. Major components in oils obtained from Amazonian palm fruits. Grasas y Aceites. 64, 328334. Silva, R.S., Ribeiro, L.M., Mercadante-Simo˜es, M.O., Nunes, Y.R.F., Lopes, P.S.N., 2014. Seed structure and germination in buriti (Mauritia flexuosa), the Swamp palm. FloraMorphol. Distribut. Funct. Ecol. Plants. 209, 674685. Va´squez-Ocmı´n, P.G., Solı´s, V.E.S., Torres, D.C., Alvarado, L.F., Luja´n, M.M.M., 2009. Diferenciacio´n quı´mica de tres morfotipos de Mauritia flexuosa L. f. de la Amazonı´a Peruana. Rev. Soc. Quı´mica Peru´. 75, 320328. Va´squez-Ocmı´n, P.G., Alvarado, L.F., Solı´s, V.S., Torres, R.P., Mancini-Filho, J., 2010. Chemical characterization and oxidative stability of the oils from three morphotypes of Mauritia flexuosa L.f, from the Peruvian Amazon. Grasas y Aceites. 61, 390397. Zanatta, C.F., Urgatondo, V., Mitjans, M., Rocha-Filho, P.A., Vinardell, M.P., 2008. Low cytotoxicity of creams and lotions formulated with Buriti oil (Mauritia flexuosa) assessed by the neutral red release test. Food Chem. Toxicol. 46, 27762781. Zanatta, C.F., Mitjans, M., Urgatondo, V., Rocha-Filho, P.A., Vinardell, M.P., 2010. Photoprotective potential of emulsions formulated with Buriti oil (Mauritia flexuosa) against UV irradiation on keratinocytes and fibroblasts cell lines. Food Chem. Toxicol. 48, 7075.
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Cacao—Theobroma cacao Pahlevi A. de Souza1, Lunian F. Moreira1, Dio´genes H.A. Sarmento2 and Franciscleudo B. da Costa3 1
Federal Institute of Education, Science and Technology of Ceara´, Limoeiro do Norte, Brazil, 2UNIVALE, Limoeiro do Norte, Brazil
3
UFCG/CCTA, Pombal, Brazil
Chapter Outline Origin and Botanical Aspects Harvest and Potential of Industrialization Cocoa Beans Processing
69 72 72
Chemical Composition and Nutritional Value References
72 75
ORIGIN AND BOTANICAL ASPECTS Cocoa (Theobroma cacao L.), known worldwide for being the raw material of chocolate, belongs to the class Magnoliopsida, order Malvales, family Malvaceae, genus Theobroma and species Cacao, being the main fruit of the genus cultivated, due to the value and importance of the seeds (Argout et al., 2001; CEPLAC, 2001; Alexandre et al., 2015; Kongor et al., 2016). The cacao tree originates from rainforest regions of tropical America, where until today, is found in the wild state, from Peru to Mexico. Charles de L’Ecluse was the first to cite the cacao in the botanical literature as Cacao fructus. Later (1737), Linneu described it as Theobroma fructus. However, in 1753, the same Linneu proposed the specific name of Theobroma cacao, which remains to this day. Botanists believe that cocoa originates from the headwaters of the Amazon River, and it has expanded in two main directions, originating into two important groups: Criollo and Forastero (Pires, 2003). According to Beckett (1994), these terms were initially used in Venezuela to distinguish the native material of the region (Criollo) from the introduced material (Forastero). The Criollo, which spread northward to the Orinoco River, penetrating central America and southern Mexico, produces large fruits with a wrinkled, thin or thick surface, which presents red or green color (Tucci et al., 1996) (Fig. 1). In addition, its seeds are large, with a white or pale violet interior. It was the type of cacao cultivated by the Aztec and Mayan Indians. The Forastero has spread through the Amazon basin towards the Guianas. It is the true Brazilian cacao, which presents intensely pigmented seeds, with dark violet or blackish interior, green fruits when immature and yellow when ripe, ovoid shaped, smooth surface, imperceptibly furrowed or wrinkled (Beckett, 1994; CEPLAC, 2001) (Fig. 2). According to Batalha (2009) the cocoa plant develops in the hot and humid climate in a geographic range comprised between the 20oN and 20oS parallels. Its cultivation extends from Venezuela, passing through Colombia, Central % America and Mexico. When% dispersing along the Amazon River, it also reaches the Guianas. However, about 70% of world production comes from West Africa, mainly from Ivory Coast (40%), Ghana (20%), Nigeria (5%), and Cameroon (5%). Brazil, before the introduction of the witch-broom disease (Moniliophtora perniciosa) in 1989, was the world’s second largest cocoa producer, falling to the fourth position, accounting for only 4% after this disease (Leite, 2012). According to data from CEPLAC (2001), the cocoa plant can be described as follows. Height: it can reach 58 m of height and 46 m of diameter of the crown. However, it can reach up to 20 m under forest condition, due to competition for light with other species.
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00010-1 © 2018 Elsevier Inc. All rights reserved.
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Exotic Fruits Reference Guide
FIGURE 1 Aspect of the plant of the cacao tree.
FIGURE 2 Aspect of the plant and fruit of the cacao tree.
Cacao—Theobroma cacao
71
Root system: consists of a pivoting root that has its length and shape varying according to the structure, texture, and consistency of the soil. In deep soils with good aeration it can have a growth of the pivoting root of up to 2 m. The secondary roots are responsible for the plant nutrition, and generally 70%90% of these are in the first 30 cm of the soil. Stem: it is erect, and with 2-years aged, the growth of the terminal yolk is stopped with 1.01.5 m of height. Afterwards, the first crowns appearing, composed of 35 main branches, that multiply in other lateral and secondary branches. In the first years, the cacao tree presents smooth stems bark. Later, due to development of flowers cushions, it becomes rough and rugged. Leaves: the leaves are oblong, acuminate, and glabas with prominent central rib. When new, depending on the clone or cultivar, they have a color ranging from green (more or less rosy) to violet, depending on the amount of anthocyanin present. When old, the leaves lose their pigmentation, becoming pale green, and finally, dark green and stiff. Flowers: cacao flowers appear in floral cushions on the trunk or woody branches, from buds that develop in the armpits of old leaves. The flowers are hermaphroditic and have the following constitution: five sepals, five petals, five estaminodes, five stamens and one pistil whose ovary has five ovules. The cacao flowers have structural characteristics that limit their pollination exclusively by insects. The main pollinating agents of cacao are a small group of insects belonging to the Ceratopogonidae family, genus Forcipomya. In the Amazon Region, the cacao tree has two flowering peaks: a minor that coincides with the beginning of the less rainy period and a main one that occurs at the end of the dry season and the beginning of the rainy season. Annually, an adult cacao tree can produce more than 100,000 flowers, but only about 0.1% turn into fruit. The unpollinated flowers fall within 48 h. On the other hand, the pollinated and fertilized flowers remain fixed on the peduncle, and they develop the fruit. Fruit: it presents a fleshy pericarp composed of three distinct parts: the epicarp, which is fleshy and thick, whose outer epidermal extract may be pigmented. The mesocarp, which is thin and hard, but not very lignified, and the endocarp, which is fleshy and not very thick. Usually the fruit when immature is green, and yellow when ripe. Others are purple (red-wine) in the development phase and orange in the ripening period. The period between pollination and fruit ripening varies from 140 to 205 days, with an average of 167 days. The fruit index (number of fruits required to obtain 1 kg of commercial cocoa) is generally from 15 to 31 fruits (Fig. 3). Seed: the shape varies from ellipsoid to ovoid with 23 cm in length. It is covered by white mucilaginous pulp that has an acid-sweet taste. The embryo has two cotyledons with colors ranging from white to violet. Cocoa’s seeds are very sensitive to temperature changes and die in a short time when suffer from dehydration.
FIGURE 3 Aspect of fruit of the cacao tree.
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HARVEST AND POTENTIAL OF INDUSTRIALIZATION Harvest starts from the second year. From the second to the fourth year, the fruits can be harvested practically throughout the year. From the fifth year, harvest occurs in two periods: harvest season, November to February, and off-season, April to August (CEPLAC, 2001). In practice, the change in color of the bark, from green to yellow or red depending on the variety, indicates the harvest point of the cocoa fruit (EFRAIM, 2009). According to Verı´ssimo (2012), the pulp has an exotic flavor and is pleasing to the palate like other fruits, such as soursop (Annona muricata) or cupuac¸u (Theobroma grandiflorum). The main product of cocoa is chocolate (Santos, 2012), but other products such as cosmetics, fine drink, juice and icecream use this fruit as raw material. Sousa (2015) states that the taste and aroma of chocolate are unique to Theobroma cacao and no one, until 2015, had been able to synthesize this artificially. Chocolate industries use cocoa fruits from three groups: Criollo, Forastero and Trinitario (Alexandre et al., 2015). In addition, the chocolate industry uses another 2-categories classification: regular cocoa and fine-flavor cocoa. ´ lvarez et al. (2007), the Criollo variety produces the best chocolate due to the sweet taste of its According to A seeds, which are less bitter and more aromatic than the other two varieties. Its use as raw material for chocolate varies from 5% to 10% only. Trinita´rio is a hybrid variety from Criollo and Forastero, and its use ranges 10%15% of the world production of chocolate. These two varieties belong to the fine-flavor category, being used in products with more delicate flavors and aromas (Verı´ssimo, 2012). Forastero, classified as regular, is the cheapest variety and, therefore, its use in the industry is around 80%, especially in products with high concentration of chocolate (Rusconi and Conti, 2010).
COCOA BEANS PROCESSING After harvest, the fruits should been opened in order to separate the bark and the placenta (80%) from the seeds and pulp (20%) (Sousa, 2015; Santos et al., 2013; Pires et al., 2005). Seeds are separated from the pulp by a fermentation process (Guilloteau et al., 2005). In this fermentation process, the enzymatic and microorganism action on polyphenols, proteins, and carbohydrates (Elwers et al., 2009; Maˆcedo, 2014) induces the development of precursors and numerous compounds responsible for the taste and aroma of chocolate (Oetterer, 2006), as well as other products made from cocoa (Lagunes Ga´lvez et al., 2007). Industrially, this process turns the seeds into cocoa beans. After fermentation, the cocoa beans are dried and toasted until reaching a moisture content of 7%, and many reactions initiated in the fermentation process continue in the drying and roasting step, such as the oxidation reactions that reduce the acidity (Beckett, 1994) and phenolic compounds that are responsible for bitterness and astringency of cocoa (Fellows, 2006). Cocoa beans can be dried in the sun (Pontillon, 2009) or in dryers (Cruz, 2002). However, in the latter method, the increase in temperature may lead to a hardening of the cotyledons with eventual loss of quality (Beckett, 2009). Thus, the genotype (Luna et al., 2002) and the harvesting, drying (Rocha et al., 2014) and fermentation stages (Hue et al., 2016; Loureiro, 2014) directly influence the quality of cocoa, mainly when seeds of different cocoa genotypes are mixed in the fermentation process (Ioanonne et al., 2015; Menezes et al., 2016). After drying, the beans should be stored, avoiding high volume conditions in high humidity and low air circulation, as the beans are hygroscopic and moisture gain may lead to the development of fungi and other undesirable microorganisms (Beckett, 1994). However, the processing generates significant amounts of byproducts, such as bark, pulp, and ‘cocoa honey’ (Santos et al., 2014). The ‘cocoa honey’ is a Brazilian name for the transparent liquid extracted from the pulp prior to fermentation, consisting of water, fermentable sugars (10%18%), nonvolatile acids (0.77%1.52%), pectin (0.9%2.5%), and fibers (0.7%). The bark can be destined for animal feeding, such as ruminants, fuel, or for application in the soil (CEPLAC, 2001; Silva et al., 2005; Carvalho, 2007), replacing or in association with chemical compounds used in soil fertilization, because it is rich in K, Ca, P, and Mg (Chepote, 2003).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Cacao-based products are classified as highly energetic, stimulating (Lopes, 2008) and antioxidants (Nasrollahzadeh ´ lvarez et al., 2007; Rusconi and Conti, 2010), and bioactive et al., 2015), due to the high fat content of 40%50% (A
Cacao—Theobroma cacao
73
compounds (Santos et al., 2015) such as polyphenols (Ioanonne et al., 2015). The main phenolic compounds found in cocoa are within the group of tannins and flavonoids (Efraim et al., 2011). Flavonoids have an antiinflammatory action against cardiovascular diseases and cholesterol oxidation prevention (Santos et al., 2015), preventing or delaying the accumulation of fats in the walls of blood vessels (Silva et al., 2013). Herewith we display tables that show the physicochemical composition of the pulp (Table 1), physical characteristics of the fruits and seeds (Table 2), chemical composition of the seeds (Table 3), centesimal composition of the fermented and dried cocoa beans (Table 4), and chemical composition of the cocoa bark (Table 5).
TABLE 1 Physicochemical Composition of the Cocoa Pulp Characteristics
Unit
Values
pH
3.19
Titratable acidity
% of citric acid
Soluble solids
Vitamin C Protein Lipids Water content
Source
3.45
Alexandre et al. (2015)
1.57
2.12
Alexandre et al. (2015)
12.97
16.55
Alexandre et al. (2015)
mg 100 g
3.30
7.60
Penha and Matta (1998)
21
0.73
1.13
Penha and Matta (1998)
21
0.12
0.65
Penha and Matta (1998)
21
75.33
80.06
Penha and Matta (1998)
Brix 21
g 100 g g 100 g g 100 g
Activity of water
0.90
0.94
Penha and Matta (1998)
Fibers
21
g 100 g
0.29
0.35
Penha and Matta (1998)
Starch
g 100 g21
3.65
4.58
Penha and Matta (1998)
21
6.62
8.22
Penha and Matta (1998)
21
3.72
5.29
Penha and Matta (1998)
21
4.41
5.95
Penha and Matta (1998)
Sucrose Glucose Fructose
g 100 g
g 100 g g 100 g
TABLE 2 Physical Characteristics of Cocoa Fruits and Seeds Characteristics
Unit
Total fruit mass
g
491.50
Values 1,124.27
Source Alexandre et al. (2015)
Total bark mass
g
362.92
912.04
Alexandre et al. (2015)
Percentage of pulp
%
18.67
31.64
Alexandre et al. (2015)
Transversal diameter of the fruit
cm
8.46
11.14
Penha and Matta (1998)
Longitudinal diameter of the fruit
cm
13.89
23.23
Penha and Matta (1998)
Number of seeds
average
24.30
39.90
Penha and Matta (1998)
Seed width
mm
11.86
14.45
Penha and Matta (1998)
Seed thickness
mm
6.19
9.85
Penha and Matta (1998)
Seed mass
g
0.68
1.93
Loureiro (2012)
TABLE 3 Chemical Composition of Cocoa Seeds Characteristics
Unit
Values
pH Titratable acidity Water content
21
meq NaOH 100 g 21
g 100 g
Activity of water Sucrose Glucose
5.25
Efraim (2009)
2.17
3.93
Efraim (2009)
52.95
58.15
Efraim (2009)
0.97
0.99
Efraim (2009)
21
7.37
11.84
Efraim (2009)
21
21.09
61.94
Efraim (2009)
mg g
mg g
21
Fructose
mg g
Phenolic compounds
mg 100 g21
Total nitrogen
Source
4.66
21
g 100 g
16.82
66.43
Efraim (2009)
129.04
168.83
Efraim (2009)
24.05
29.13
Efraim (2009)
TABLE 4 Centesimal Composition of the Fermented and Dried Cocoa Beans Characteristics
Unit
Values
Source
Water content
%
35.00
Koblitz (2011)
Lipids
%
31.30
Koblitz (2011)
Protein
%
8.40
Koblitz (2011)
Theobromine
%
2.40
Koblitz (2011)
Caffeine
%
0.80
Koblitz (2011)
Polyphenols (tannins)
%
5.20
Koblitz (2011)
Carbohydrates, acids, and fibers
%
13.70
Koblitz (2011)
Ashes
%
3.20
Koblitz (2011)
Total
%
100.00
TABLE 5 Chemical Composition of the Cocoa Bark Characteristics
Unit
Values
Source
Water content
%
8.50
Vriesmann et al. (2011)
Ashes
%
6.70
Vriesmann et al. (2011)
Protein
%
8.60
Vriesmann et al. (2011)
Lipids
%
1.50
Vriesmann et al. (2011)
Total carbohydrates
%
32.30
Vriesmann et al. (2011)
Low molecular weight carbohydrates
%
19.20
Vriesmann et al. (2011)
Lignin
%
21.40
Vriesmann et al. (2011)
Insoluble fibers
%
27.00
Vriesmann et al. (2011)
Soluble fibers
%
9.60
Vriesmann et al. (2011)
Total fibers
%
36.60
Vriesmann et al. (2011)
Ca
%
0.254
Vriesmann et al. (2011)
K
%
2.768
Vriesmann et al. (2011)
Mg
%
0.1109
Vriesmann et al. (2011)
Fe
%
0.0058
Vriesmann et al. (2011)
Na
%
0.0105
Vriesmann et al. (2011)
Cacao—Theobroma cacao
75
REFERENCES Alexandre, R.S., Chagas, K., Marques, H.I.P., Costa, P.R., Filho, J.C., 2015. Caracterizac¸a˜o de frutos de clones de cacaueiros na regia˜o litoraˆnea de Sa˜o Mateus, ES. Revista Brasileira de Engenharia Agrı´cola e Ambiental. 19 (8), 785790. Argout, X., et al., 2001. The genome of Theobroma cacao. Nat. Genet. 43, 101109. ´ lvarez, C., Pe´rez, E., Lares, M.C., 2007. Physical-chemical characterization of fermented, dried and roasted cocoa beans cultivated In the region of A cuyagua, aragua state. Agronomı´a Tropical. 57 (4), 249256. Batalha, P.G., 2009. Caracterizac¸a˜o do cacau catongo de Sa˜o Tome´ e Prı´ncipe. Mestrado (Mestre em Engenharia de AlimentosTecnologia de Produtos vegetais) Universidade Te´cnica de Lisboa. Instituto Superior de Agronomia, LisboaPortugal. Beckett, J.R., 1994. Industrial chocolate manufacture and use. second ed. Black Academic & Professional, London, 407p. Beckett, S.T., 2009. In: Beckett, Stephen T. (Ed.), Industrial chocolate manufacture and use, fourth ed. Blackwell Publishing Ltd, London, 732p. Carvalho, G.G.P., Garcia, R., Pires, A.J.V., Preira, O.G., Azevedo, J.A.G., Carvalho, B.M.A., et al., 2007. Valor nutritivo de silagens de capim-elefante emurchecido ou com adic¸a˜o de farelo de cacau. Revista Brasileira de Zootecnia. 36 (5), 14951501. CEPLAC, 2001. Sistema de produc¸a˜o de cacau para a Amazo´nia brasileira. CEPLAC, Bele´m, 125p. Chepote, R.E., 2003. Efeito do composto da casca do fruto de cacau no crescimento e produc¸a˜o do cacaueiro. Revista Agrotro´pica. 15 (1), 8. Cruz, C.L.C.V., 2002. Melhoramento do sabor de ameˆndoas de cacau atrave´s de tratamento te´rmico em forno convencional e de microondas. Dissertac¸a˜o (Mestre em Tecnologia de Alimentos). Faculdade de Engenharia de Alimentos. Universidade Estadual de Campinas. CampinasSP, 101p. Efraim, P., 2009. Contribuic¸a˜o a` melhoria de qualidade de produtos de cacau no Brasil, por meio da caracterizac¸a˜o de derivados de cultivares resistente a Vassoura de Bruxa e de sementes danificadas pelo fungo. Tese (Doutorado em Tecnologia em Alimentos). Universidade Estadual de Campinas, Campinas, Sa˜o Paulo, p. 208f. Efraim, P., Alves, A.B., Jardim, D.C.P., 2011. Polifeno´is em cacau e derivados: teores, fatores de variac¸a˜o e efeito na sau´de. Braz. J. Food Technol. 14 (3), 181201. Elwers, S., Zambrano, A., Rohsius, C.H., Lieberei, R., 2009. Differences between the content of phenolic compounds in criollo, forastero and trinitario cocoa seed (Theobroma cacao L.). Eur. Food Res. Technol. 229 (6), 937948. Fellows, P.J., 2006. Tecnologia do processamento de alimentos. Princı´pios e pra´tica. 2 Edic¸a˜o. Ed Artmed, pp. 183205, 602. Guilloteau, M., Lalaoi, M., Michaux, S., Bucheli, P., McCarthy, J., 2005. Identification and characterization of the majoraspartic proteinase activity in Theobroma cacao seeds. J. Sci. Food Agric. 85, 549562. Hue, C., Gunata, Z., Breysse, A., Davrieux, F., Boulanger, R., Sauvage, F.X., 2016. Impact of fermentation on nitrogenous compounds of cocoa beans (Theobroma cacao L.) from various origins. Food Chem. 192, 958964. Ioanonne, F., Mattia, C.D., Gregorio, M., Sergi, M., Serafini, M., Sacchetti, G., 2015. Flavanols, proanthocyanidins and antioxidant activity changes during cocoa (Theobroma cacao L.) roasting as affected by temperature and time of processing. Food Chem. 174, 256262. Koblitz, M.G.B., 2011. Mate´rias-primas alimentı´cias: composic¸a˜o e controle de qualidade. Guanabara Koogan, Rio de Janeiro (RJ), 301 p. Kongor, J.E., Hinneh, M., Walle, D.V., Afoakwa, E.O., Boeckx, P., Dewettinck, K., 2016. Factors influencing quality variation in cocoa (Theobroma cacao L.) bean flavour profile—a review. Food Res. Int. 82, 4452. Lagunes Ga´lvez, S., Loiseau, G., Paredes, J.L., Barel, M., Guiraud, J.P., 2007. Study on the microflora and biochemistry of cocoa fermentation in the Dominican Republic. Int. J. Food Microbiol. 114, 124130. Leite, P.B., 2012. Caracterizac¸a˜o de chocolates provenientes de variedades de cacau Theobroma cacao L. resistentes a vassoura de bruxa. Mestrado (Mestre em Cieˆncia dos Alimentos) Universidade de Farma´cia da Universidade Federal da Bahia. Lopes, A.S., Pezoa-Garcı´a, N.H., Amaya-Farfa´n, J., 2008. Qualidade nutricional das proteı´nas de cupuac¸u e de cacau. Cieˆncia e Tecnologia de Alimentos. 28 (2), 263268. Loureiro, G.A.H.A., 2012. Atributos qualitativos de solo e ameˆndoas de cacau comum: revisa˜o, ana´lises e interpretac¸a˜o de relac¸o˜es. Monografia (Bacharelado em Engenharia Agronoˆmica). Universidade Estadual de Santa Cruz, Ilhe´us, Bahia, p. 87f. Loureiro, G.A.H.A., 2014. Qualidade de solo e qualidade de cacau. Dissertac¸a˜o. Programa de Po´s-Graduac¸a˜o em Produc¸a˜o vegetal. Universidade Estadual de Santa Cruz, Ilhe´usBahia, p. 236f. Luna, F., Crouzillat, D., Cirou, L., Bucheli, P., 2002. Chemial composition and flavor of Ecuadorian cocoa liquor. J. Agric. Food Chem. Easton. 50, 35273532. Maceˆdo, A.S.L., 2014. Caracterizac¸a˜o de enzimas em dois cultivares de cacau Theobroma cacao L. Dissertac¸a˜o. Programa de Po´s-Graduac¸a˜o em Cieˆncia de Alimentos. Universidade Federal da Bahia Salvador, p. 89f. Menezes, A.G.T., Batista, N.N., Ramos, C.L., Silva, A.R.A., Efraim, P., Pinheiro, A.C.M., et al., 2016. Investigation of chocolate produced from four different Brazilian varieties of cocoa (Theobroma cacao L.) inoculated with Saccharomyces cerevisiae. Food Res. Int. 81, 8390. Nasrollahzadeh, M., Sajadi, S.M., Rostami-Vartooni, A., Bagherzadeh, M., 2015. Green synthesis of Pd/CuO nanoparticles by Theobroma cacao L. seeds extract and their catalytic performance for the reduction of 4-nitrophenol and phosphine-free Heck coupling reaction under aerobic conditions. J. Colloid Interface Sci. 448 (15), 106113. Oetterer, M., 2006. Tecnologias de obtenc¸a˜o de cacau, produtos do cacau e do chocolate. In: Oetterer, M., Regitano d’Arce, A., Spoto (Org.), M.H.F. (Eds.), Fundamentos de Cieˆncia e Tecnologia de Alimentos, vol. 1. Manole, Barueri, Sa˜o Paulo. Penha, E., Matta, M., Caracterı´sticas, V.M., 1998. fı´sico-quı´micas e microbiolo´gicas da polpa de cacau. Pesquisa Agropecua´ria Brasileira. 33 (11), 19451949.
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Pires, J.L., 2003. Avaliac¸a˜o quantitativa e molecular de germoplasma para o melhoramento do cacaueiro com eˆnfase na produtividade, qualidade de frutos e resisteˆncia a doenc¸as. 2003. 220p. Tese Doutorado. Universidade Federal de Vic¸osa, Vic¸osa, MG. Pires, A.J.V., Vieira, V.F., Silva, F.F., Veloso, C.M., Souza, A.L., Oliveira, T.N., et al., 2005. Nı´veis de Farelo de Cacau (Theobroma cacao L.) na alimentac¸a˜o de bovinos. Revista Electro´nica de Veterinaria. 6 (2), 110. Pontillon, J., 2009. Do cacao ao tablete. A Cieˆncia na cozinha, Sa˜o Paulo, v. 1, pp. 6271. Rocha, I.S., Miranda, A.L., Amorim, F.L., Silveira, P.T.S., Soares, S.E., 2014. Prospecc¸a˜o tecnolo´gica com o enfoque na produc¸a˜o e preprac¸a˜o de alimentos com aroma e sabor de cafe´ e cacau. RevistaGEINTEC. 4 (4), 14181425. Rusconi, M., Conti, A., 2010. Theobroma cacao L., the food of the gods: A scientific approach beyond myths and claims. Pharmacol. Res. 61 (1), 513. Santos, C.O., 2012. Aproveitamento industrial de ‘mel’ de cacau (Theobroma cacao L.) na produc¸a˜o de gele´ia sem adic¸a˜o de ac¸u´car. Dissertac¸a˜o (Mestrado em Cieˆncia dos Alimentos). Universidade Federal da Bahia, Salvador, Bahia, p. 92f. Santos, T.C., Rocha, T.J.O., Oliveira, A.C., Filho, G.A., Franco, M., 2013. Aspergellus niger como produtor de enzimas celuloliticas a partir farelo de cacau (Theobroma cacao L.). Arquivos do Instituto Biolo´gico. 80 (1), 6571. Santos, C.O., Bispo, E.S., Santana, L.R.R., Carvalho, R.D.S., 2014. Use of ‘cocoa honey’ (Theobroma cacao L.) for diet jelly preparation: an alternative technology. Revista Brasileira de Fruticultura, Jaboticabal. 36 (3), 640648. Santos, A.T., Uchoa, F.N.M., Lima, M.S., Uchoa, N.M., Foschetti, D.A., Daniele, T.M.C., et al., 2015. Ana´lise sensorial de um biscoito funcional a base de cacau e aveia. Revista Intertox-EcoAdvisor de Toxicologia Risco Ambiental e Sociedade. 8 (3), 7989. Silva, H.G.O., Pires, A.J.V., Silva, F.F., Veloso, C.M., Carvalho, G.G.P., Ceza´rio, A.S., et al., 2005. Farelo de Cacau (Theobroma cacao L.) e Torta de Dendeˆ (Elaeis guineensis, Jacq) na Alimentac¸a˜o de Cabras em Lactac¸a˜o: Consumo e Produc¸a˜o de Leite. Revista Brasileira de Zootecnia. 34 (5), 17861794. Silva, S.A.M., Valarini, M.F.C., Chorilli, M., Venturini, A., Leonardi, G.R., 2013. Atividade antioxidante do extrato seco do cacau (Theobroma cacao L.)Estudo de estabilidade e teste de aceitac¸a˜o de cremes acrescidos deste extrato. Revista de Cieˆncias Farmaceˆuticas Ba´sica e Aplicada. 34 (4), 493501. Sousa, L.S., 2015. Atividade enzima´tica das proteases e suas isoenzimas no processamento de fermentac¸a˜o de dois cultivares de cacau (Theobroma cacao L.) produzido no sul da Bahia, Brasil. Dissertac¸a˜o (Mestrado em Cieˆncia dos Alimentos). Universidade Federal da Bahia, Salvador, Bahia, p. 85f. Tucci, M.L.S., Abreu, M.F., Coral, F.J., Futino, A.M., Alfonsi, R.R., Saes, L.A., 1996. Teores de gordura e a´cidos graxos de clones de cacau nas condic¸o˜es do Vale do Ribeira (SP). Bragantia. 55, 207213. Verı´ssimo, A.J.M., 2012. Efeito da origem do cacau na sua qualidade comercial, funcional e sensorial. O caso do cacau catongo de Sa˜o Tome´ e Prı´ncipe e do Brasil. Dissertac¸a˜o. Instituto Superior de Agronomia, Universidade de Lisboa, p. 87f. Vriesmann, L.C., Amboni, R.D.M.C., Petrowicz, C.L.O., 2011. Cacao pod husks (Theobroma cacao L.) composition and hot water soluble pectins. Ind. Crops Product. 34, 11731181.
Cagaita—Eugenia dysenterica Eli R.B. de Souza, Yanuzi M.V. Camilo and Rosaˆngela Vera Federal University of Goia´s, Goiaˆnia, Brazil
Chapter Outline Origin, Culture, and Botanical Aspects Harvest Season and Estimated Annual Production Physiology and Biochemistry of Fruits
77 78 79
Harvest, Postharvest, and Potential Industrial Application References
80 82
ORIGIN, CULTURE, AND BOTANICAL ASPECTS Popularly known as “cagaita” or “cagaiteira” Eugenia dysenterica DC belongs to the Myrtaceas Family, which is considered one of the ten most representative families in the Cerrado biome (Mendonc¸a et al., 1998). The Eugenia genus comprises about 500 species, widely distributed in tropical (Silva et al., 1994) and subtropical regions (Duarte et al., 2009), in which 350 are found in Brazil (Oliveira et al., 2012; Zucchi et al., 2005) and approximately 15 species are in the Cerrado (Naves et al., 1995). The most used botanical nomenclature for the species is E. dysenterica D.C. (Zucchi et al., 2005); however, some authors cite its synonyms Stenocalyx dysentericus (Mart. ex D.C.) Berg and Myrtus dysenterica Mart. (Duarte, 2009). E. dysenterica stands out for its potential for food and medical exploration, and can be found along almost the entire extent of the Cerrado. The plant occurrence is described in Cerrada˜o and Cerrado (Martinotto et al., 2008; Souza et al., 2008), predominantly in the states of Bahia, Distrito Federal, Goia´s, Maranha˜o, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Para´, Piauı´, Sa˜o Paulo, and Tocantins (Silveira et al., 2013; Jorge et al., 2010). The cagaiteira is characterized by being a fruiting, hermaphroditic and deciduous tree (Martinotto et al., 2008; Brito et al., 2003), with trunks and winding branches (Almeida et al., 1998) measuring between 20 and 40 cm in diameter (Martinotto et al., 2008) (Fig. 1). As an adult, the shrubby tree reaches 48 m (Brito et al., 2003), reaching up to 1015 m high (Martinotto et al, 2008; Brito et al., 2003). The canopy has an amplitude of about 7.58 m, with an average of basal area of 0.86 m in trunk circumference (Brito et al., 2003). The leaves are described as membranous, with estimated size of 313.8 cm in length and 18.2 cm wide, glabrous at maturity and puberulas at youth, with luster on the upper face (Martinotto et al., 2008; Brito et al., 2003). They are deciduous during flowering (Marinotto et al., 2008). The leaves emergence occurs throughout the year and with a higher proportion between September and October, when the temperature is higher and the relative humidity is lower (Souza et al., 2008). The flowering is ephemeral, and the flowers just bloom in the morning and for a tiny period (Brito et al., 2003; Zucchi et al., 2003). In general, flowering lasts one week (Marinotto et al., 2008). The maximum point of leaves exchange is simultaneous to the floral buds emergence (Brito et al., 2003). Souza et al. (2008) state that this phenophase is intense and simultaneous with the sprouting. About 6.8% of the emerged buds by plant will originate fruits (Brito et al., 2003). The fruits are berry type with a thin, green peel at youth and light yellow at maturity (Almeida et al., 1987), with a round and a little flat shape (Faria Junior, 2010; Souza et al., 2008) (Fig. 2). Some authors have reported that the fruit has from 2 to 5 cm in diameter and 3 to 5 cm length (Camilo et al., 2014; Jorge et al., 2010). Weighing between 16 and 20 g (Camilo et al., 2014), the fruits have 14 seeds that have about 11.5 cm long, they are cream-colored,
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00011-3 © 2018 Elsevier Inc. All rights reserved.
77
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Exotic Fruits Reference Guide
FIGURE 1 Flowering of the cagaiteira.
oval-shaped, and may be globular or ellipsoids (Martinotto et al., 2008; Brito et al., 2003). The seeds weigh about 3.39 6 1.22 g (Cardoso et al., 2011), and a kilogram of seeds contains 7001600 units (Jorge et al., 2010). A morphobiometric study indicated this feature may exhibit a variation, because there have been measured masses of between 8.61 and 29.85 g and longitudinal diameter from 20.55 to 36.61 mm, and cross-sectional diameter of 25.3338.32 mm, which shows the phenotypic variation in the species (Camilo et al., 2014). The knowledge of the fruit physical characteristics is of great importance to know the diversity of size and mass of each species, and to enable the manufacture of packaging for storage and marketing, so that no damage will occur in their physical structure, and its appearance is appealing to the consumer (Rocha et al., 2013).
HARVEST SEASON AND ESTIMATED ANNUAL PRODUCTION The cagaiteira fruiting period occurs between September and November (Chaves and Telles, 2010; Brito et al., 2003). There is no knowledge of organized planting of this species, as the whole fruit production is carried out in an extractive way with natural populations (Chaves and Telles, 2010). Silva et al. (1994) reported that plants cultivated by seeds begin to bear fruit when they reach between 4 and 5 years. However, studies performed by Souza et al. (2013) point out that in the fifth year after planting, 23 of 440 plants started production. Ten years after planting, 245 plants (55.7%) reached the reproductive stage, bearing fruit in at least one year. Therefore, it is verified that the change from the vegetative phase to the reproductive phase in cagaita is slow and uneven. This fact requires attention in order to create conditions to increase uniformity and promote their development in the field. According to Souza et al. (2013), besides the fact of few plants going into production after the fifth year of their planting in the field, the number of fruits is very low, indicating a slow production in plant and fruit number. There is a tendency to increase the number of fruits with the age of the cagaiteiras, although they are very uneven to start
Cagaita—Eugenia dysenterica
79
FIGURE 2 Fruiting of the cagaiteira.
production. This phenophase correlates with climatic parameters (Camilo et al., 2013; Souza et al., 2008), year and region (Brito et al., 2003). According to Souza et al. (2008), cultivated and native plants have identical fruiting behavior. The fruits develop and become mature in a short period, about 30 to 40 days or a little more than 4 weeks (Martinotto et al., 2008; Souza et al., 2008). From October to December there is the development and maturation of the fruit (Souza et al., 2008; Brito et al., 2003). The climax is in October (Camilo et al., 2013). In general, cagaiteiras have high yield potential (Camilo et al., 2014), with about 15002000 fruits per tree (Martinotto et al., 2008; Brito et al., 2003). Fourteen-year-old plants can present 3001300 fruits (Camilo et al., 2013). It was observed that the production is typically higher in native areas than when the plants are cultivated experimentally (Souza, 2006). Studies also show that there is fruit production shifting every two years. According to Camilo (2015), who evaluated cagaiteiras populations grown experimentally in the Cerrado, there was a decrease in the average production from 300 fruits per plant in 2011 to 77 fruits in 2012, and a new decrease to 67 fruits in 2013, returning to an increase in 2014, with an average of 168 fruits per plant. Although the average production of selected plants was considered low, it is possible to observe cagaiteiras producing up to 1000 fruits per plant which confirms the wide production range. Research seeking E. dysenterica progenies revealed some candidates that stood out for precocity, productivity, and chemical characteristics of interest for the fruit pulp processing industry, being identified as able to be used for genetic improvement (Camilo et al., 2013, 2014).
PHYSIOLOGY AND BIOCHEMISTRY OF FRUITS Information regarding the physicochemical characteristics and nutritional and functional value of the fruits of the Cerrado are basic tools to encourage the consumption and the formulation of new products. The knowledge of the physical, macronutrients, micronutrients and antioxidant compounds in these fruits will provide a better indication of their
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consumption and use in the food industry. However, few data are available in the literature regarding the chemical composition and technological application of these fruits, highlighting the need for scientific research on the subject (Silva et al., 2008; Rocha et al., 2013). Based on scientific literature, Rocha et al. (2013) state that it is difficult to compare the antioxidant activity of different samples due to the use of different sample dilutions, different types of solvents and methods, as each sample has an antioxidant power and behaves differently in each type of analysis. The same authors found for cagaita values in mg/100 g of Vitamin C (126.3 6 45.8), flavonoids (9.51 6 0.4), anthocyanins (0.8 6 0.38) and β-carotene in μg/100 g of fruit (201.23 6 25.1), high moisture content (90.0 6 8.4) and low calorific value (36.6 6 7.2). This demonstrates physicochemical, nutritional, and functional characteristics that enable their use in the food industry. For presenting high water content (over 90%), the fruit pulp of cagaiteiras has a low mineral residues content, ranging from 0.21% to 0.37%. Regarding the content of proteins and lipids, there is a low average percentage of 0.92% and 1.02%, respectively, but very relevant, considering that most of the fruit levels of these constituents are often low (Camilo et al., 2014; Silva et al., 2008). The fruits are acidic, which favors the process of industrialization in sweets, but inhibits their fresh consumption. The fruits of E. dysenterica are sensitive to heat, so they start the fermentative process easily, therefore, they should not be consumed when exposed to high temperatures. Excessive consumption may cause diarrhea and intoxication (Martinotto et al., 2008; Brito et al., 2003). Furthermore, as the fruit has high perishability due to the high moisture content, the most viable destiny for the fruit production would be industry, with an appreciable added value (Camilo et al., 2014). Ribeiro (2011) studied the antioxidant activity and total polyphenols in cagaita (E. dysenterica DC) peeled and unpeeled fruits. Both fruits showed good yield, being superior the unpeeled ones; according to the pH (2.8) and titratable acidity (8.5), the fruit can be considered acidic; regarding the soluble solids (14.2 Brix), it was evident that the fruit is not too sweet; the predominant minerals were potassium (75.83 mg/100 g), phosphorus (6.68 mg/100 g) and magnesium (5.92 mg/100 g). The cagaita, peeled or unpeeled, is considered rich in the ascorbic acid content which is superior to the Recommended Daily Intake (RDI); regarding their centesimal composition, the fruits are basically composed of water and carbohydrates, also present low caloric value. In cagaita pulp with peel, there was a higher concentration of fructose (2.54 g/100 g 6 0.05) and glucose (1.75 g/100 g 6 0.04) and reduced value in sucrose (0.59 g/ 100 g 6 0.05), probably because the study sample was in a great ripening stage. According to Ribeiro (2011), the three in vitro methods used to evaluate the antioxidant capacity of cagaita fruit with and without peel provided satisfactory and promising results, and the fruit with peel showed higher antioxidant activity in all tests, and the ORAC method (oxygen radical absorbance capacity) proved to be the most efficient. The high antioxidant capacity of the fruit is a result of the high amounts of bioactive substances, such as phenolics and ascorbic acid; the fruit also showed significant amounts of phenolic compounds, being higher in unpeeled fruits. The seeds, which are usually discarded during consumption, also have excellent biochemical indications and may also be used. In a study about the antioxidant capacity of native fruits, including cagaita, Roesler et al. (2007) found that the seeds of this species have a high content of total phenolics (136.96 g GAE. kg21). Although the seeds are discarded during consumption, it does not mean that the pulp and peel have no antioxidants. The pulp has antioxidants in small quantities, because most of it is composed of sugar and water. Thus, the study indicates the presence of compounds with high antioxidant potential in the seed extracts of cagaita. The relation between concentration of total phenolics and the ability to scavenge free radicals extracts seems to be quite significant, as the extracts with higher concentration of total phenolics are exactly the ones with higher antioxidant activity.
HARVEST, POSTHARVEST, AND POTENTIAL INDUSTRIAL APPLICATION In the Cerrado region, the fruits of cagaiteira begin to ripen in October, when the harvest begins, and lasts until December (Andrade et al., 2003). The harvest can be made picking up the fallen ripe fruits that are in good condition or shaking up the branches to collect the ones that are almost ripe (Almeida et al., 1987). The fruits for trade and transport should be collected when almost ripe; however, if this is not possible, ripe fruits are ideal, but are highly perishable, requiring immediate use (Silva et al., 1994; Almeida et al., 1987). Studying the effect of temperature and packaging use in postharvest conservation of cagaita, Carneiro et al. (2015) concluded that E. dysenterica fruits showed short shelf life (5 days), when they had 50% damage. The temperature of 5 C was not effective for the conservation of fruits because it promoted the appearance of chilling injury symptoms. At 25 C, the fruits presented color change, loss of firmness, pH increase, and intense consumption of carbohydrates. The use of packaging did not have significant effects on the fruit conservation.
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The use of the fresh fruit by the local population is relatively small compared to other native species in the Cerrado. The high perishability of the fruit, combined with seasonality, have driven the development of technological processes aiming to improve the use of these fruits beyond the scope of their postharvest life. Given these factors, Santos (2015) evaluated the effect of freezing and atomization of cagaita bioactive compounds and assessed the useful life of atomized cagaita pulp stored for 45 days at 30 C. The spray dryer method showed a better performance than the freezing technique, being observed higher total phenolic compounds, total flavonoids, and tannins, after drying the pulp contributing to the antioxidant potential increase. However, the food preservation methods were not effective for the preservation of the vitamin C content in fresh cagaita. E. dysenteric has been explored by the local population for food purposes. The fruit consumption occurs in natura (Almeida et al., 1998), however, due to its high perishability and great fruit loss, processed products as liquors, soft drinks, icecream, jellies, jams, and pulp (Martinotto et al., 2008; Brito et al., 2003) are produced and marketed regionally, and the processing of such products has been studied and tested in order to minimize fruit waste and increase the added value. In the study of osmotic dehydration of cagaita, Silva et al. (2015) found that there was a greater water loss, weight loss, and increased incorporation of soluble solids in the samples of dehydrated cagaita under the conditions of 65 Brix at 70 C. The lower shrinkage rate and higher rehydration capacity were observed in the osmotically dehydrated samples of 45 Brix at 50 C. The sensory analysis showed that dehydrated cagaita had good acceptance, constituting a valid option to add value to the fruit. Rocha et al. (2008) tested the preparation and evaluation of yogurt with fresh fruits from Cerrado. They concluded that the physico-chemical and sensory analysis of yogurts, including cagaita flavor, showed product stability under refrigeration for a short period of time, ranging from 5 to 6 days because there was no preservative addition. The manufactured products are good food alternatives because besides the high nutritional value, the fruits used in the flavor are highly appreciated by the people of the region. It is believed that this factor had contributed to the good acceptance of the products, as shown in the acceptance tests. The products are economically viable because besides the easy preparation and low cost of production, many of the Cerrado native species has high potential for economic utilization. Benedetti et al. (2013) developed the cagaita nectar and performed its microbiological, sensory, chemical characterization, and stability study. It was concluded that cagaita nectar formulations met the chemical and microbiological standards established by the Brazilian legislation. For all the sensory attributes that were evaluated, the formulations containing 40% and 50% of cagaita pulp were better accepted by consumers. The cagaita nectar containing 50% of pulp proved to be an excellent source of vitamin C for children, pregnant women, and adults. It was observed a resultant reduced content of proteins, lipids, total dietary fiber, carotenoids and vitamin A. It was verified excellent stability of the product, with no significant change in its chemical and nutritional characteristics during storage under refrigeration (5 C/72 h) and freezing (218 C/90 days). The cagaita nectar presented technological potential and can be produced, consumed, and marketed by native populations of the Cerrado, contributing to the nutritional intake and income generation for these populations. In an attempt to produce a compound of cagaita nectar (E. dysenterica) and mangaba (Hancornia speciosa), Assumpc¸a˜o et al. (2013) concluded that the mixed nectar presented itself as an attractive product in terms of sensory characteristics and with great technological and nutritional potential. Both formulations had good consumer acceptance, indicating that the product can be included in the market with good prospects. According to Jorge et al. (2010), cagaita seeds are also an important source of total carbohydrates and may be utilized as food products for human consumption. The seeds have a significant antioxidant activity and a high content of phenolic compounds. The oil seed is a good source of tocopherol when compared with other oils and fats. Abreu (2015) evaluated the effect of heat treatment on the technological functional properties, nutritional characteristics and antinutritional factors of cagaita seed flour, subjected to drying at 60 C and roasted at 110 C and 130 C for 10, 20, and 30 min, compared to the seed in natura. The cagaita seed flour showed higher calcium, lead, phosphorus, magnesium, potassium, and zinc after being subjected to heat treatment. Therefore, the use of seed cagaita as an ingredient in food products can be performed, because the seeds provide macronutrients and micronutrients that are important for feeding, and also have antioxidant activity. The presence of cyanogenic compounds was not detected in the analyzed samples. The heat treatment reduced the amount of trypsin inhibitors when compared to the sample. Also, it influences the reduction of phytate content of all samples. In contrast, the heat treatment increased tannin levels in all evaluated flours. It was concluded, therefore, that the seed flour showed good nutritional value, the presence of significant amounts of minerals from the RDI for adults, pregnant women and children, showed bioactive compounds and antioxidant activity, and its use is an alternative for the food industry because it presents absorption characteristics in water, oil and milk, and solubility characteristics in water and milk.
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Other studies considering the industrial potential of cagaita have been performed in the pharmaceutical field. Moreira (2013) reports the consistent and continuous growth of the skin cosmetics market in the recent years, motivating the search for new active ingredients for skin signals treatment. Along this new reality, it aroused the desire for natural products in association with environmental sustainability and authenticity. Considering that E. dysenterica has antioxidant activity similar to the vitamin C, this study investigated the effectiveness of the hydroalcoholic standardized extract of E. dysenterica leaves (EED) against aging signs. The study concluded that the EED is presented as a promising constituent for antissinais dermocosmetic formulations due to its antienzimatic and regenerating action and hypopigmentation disorders and showing confidence about phototoxicity. Prado (2013) studied the gastroprotective activity of the lyophilized aqueous extract of E. dysenterica leaves and showed that it protected the gastric mucosa from lesions induced by HCl/ethanol, this effect shows a biopharmaceutical potential for this species. Thus, cagaita has a great potential in food, medical, pharmaceutical areas, due to its chemical composition and nutritional value, with good content of vitamins, minerals, phenolic compounds and antioxidants, but requires several studies that can give scientific foundation for its production on a commercial scale to obtain enough raw material for future industrialization.
REFERENCES Abreu, P.A. de A., 2015. Caracterizac¸a˜o dos fatores nutricionais e antinutricionais de sementes de frutos do cerrado. Dissertac¸a˜o de mestrado. 157f. Universidade Federal de Goia´s, Goiaˆnia, GO. Almeida, S.P., Silva, J.A., Ribeiro, J.F., 1987. Aproveitamento alimentar de espe´cies nativas dos Cerrados: araticum, baru, cagaita e jatoba´. Embrapa-CPAC, Planaltina. Almeida, S.P., Proenc¸a, C.E.B., Sano, S.M., Ribeiro, J.F., 1998. Cerrado: Espe´cies vegetais u´teis. Embrapa-CPAC, Planaltina. Andrade, A.C.S., Cunha, R., Souza, A.F., Reis, R.B., Almeida, K.J., 2003. Physiological and morphological aspects of seed viability of a neotropical savannah tree, Eugenia dysenterica DC. Seed Sci. Technol. 31 (1), 125137. Assumpc¸a˜o, C.F., Bachiega, P., Santana, A.T.M.C., Morzelle, M.C., Boas, B.M.V., Souza, E´.C. de, 2013. Ne´ctar misto de mangaba (Hancoria speciosa Gomes) e cagaita (Eugenia dysenterica): perfil sensorial e caracterı´sticas fı´sico-quı´micas. Revista Brasileira de Produtos Agroindustriais. 15 (3), 219224. Bedetti, Sde F., Cardoso, Lde M., Santos, P.R.G., Dantas, M.I., et al., 2013. Ne´ctar de cagaita (Eugenia dysenterica DC.): desenvolvimento, caracterizac¸a˜o microbiolo´gica, sensorial, quı´mica e estudo da estabilidade. B. CEPPA. 31 (1), 125138. Brito, M.A., Pereira, E.B.C., Pereira, A.V., Ribeiro, J.F., 2003. Cagaita: biologia e manejo. Embrapa, Planaltina. Camilo, Y.M.V., 2015. Avaliac¸a˜o de cagaiteiras (Eugenia dysenterica DC.) cultivadas no municı´pio de Goiaˆnia, GO. Tese de doutorado. Universidade Federal de Goia´s, Goiaˆnia, Goia´s, p. 157f. Camilo, Y.M.V., Souza, E.R.B., Vera, R., Naves, R.V., 2013. Fenologia, produc¸a˜o e precocidade de plantas de Eugenia dysenterica visando melhoramento gene´tico. Revista de Cieˆncias Agra´rias. 36 (2), 192198. Camilo, Y.M.V., Souza, E.R.B., Vera, R., Naves, R.V., 2014. Caracterizac¸a˜o de frutos e selec¸a˜o de progeˆnies de cagaiteiras (Eugenia dysenterica DC.). Cientı´fica. 42 (1), 110. Cardoso, L.D.M., Martino, H.S.D., Moreira, A.V.B., Ribeiro, S.M.R., Pinheiro-Santana, H.M., 2011. Cagaita (Eugenia dysenterica DC.) of the Cerrado of Minas Gerais, Brazil: physical and chemical characterization, carotenoids and vitamins. Food Res. Int. 44, 21512154. Carneiro, J. de O., de Souza, M.A. de A., Rodrigues, Y.J. de M., Mapeli, A.M., 2015. Efeito da temperatura e do uso de embalagem na conservac¸a˜o po´s-colheita de frutos de cagaita (Eugenia dysenterica DC.). Rev. Bras. Frutic. 37 (3), 568577. Chaves, L.J., Telles, M.P. de C., 2010. Cagaita. Futas Nativas da Regia˜o Centro-Oeste do Brasil. Embrapa Informac¸o˜es tecnolo´gicas, Brası´lia, pp. 127141. Duarte, A.R., Naves, R.R., Santos, S.C., Seraphin, J.C., Ferri, P.H., 2009. Seasonal influence on the essential oil variability of Eugenia dysenterica. J Braz Chem Soc. 20 (5), 967974. Faria Ju´nior, J.E.Q., 2010. O geˆnero Eugenia L. (Myrtaceae) nos estados de Goia´s e Tocantins. Dissertac¸a˜o de Mestrado. Universidade de Brası´lia, Brası´lia, DF. Jorge, N., Moreno, D.M., Bertanha, B.J., 2010. Eugenia dysenterica DC: actividad antioxidante, perfil de a´cidos grasos y determinacio´n de tocoferoles. Rev. Chil. Nutr. 37 (2), 208214. Martinotto, C., Paiva, R., Soares, F.P., Santos, B.R., Nogueira, R.C., 2008. Cagaiteira (Eugenia dysenterica DC.). Universidade Federal de Lavras, Lavras. Mendonc¸a, R.C., Felfili, J.M., Walter, B.M.T., Silva Junior, M.C., Rezende, A.V., Filgueiras, T.S., et al., 1998. Flora vascular do cerrado. Cerrado: ecologia e flora. EmbrapaCPAC, Planaltina, pp. 289556. Moreira, L.C., 2013. Avaliac¸a˜o de alguns aspectos de toxicidade e efica´cia do extrato etano´lico de Eugenia dysenterica DC para dermocosme´tico. Dissertac¸a˜o de mestrado. Universidade Federal de Goia´s, Faculdade de Fa´rma´cia, Goiaˆnia, GO, p. 90f.
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Naves, R.V., Almeida Neto, J.X., Rocha, M.R., Borges, J.D., Carvalho, G.C., Chaves, L.J., et al., 1995. Determinac¸a˜o de caracterı´sticas fı´sicas em frutos e teor de nutrientes, em folhas e no solo, de treˆs espe´cies frutı´feras de ocorreˆncia natural nos cerrados de Goia´s. An Esc Agron Vet. 25 (2), 107114. Oliveira, V.B., Yamada, L.T., Fagg, C.W., Branda˜o, M.G.L., 2012. Native foods from Brazilian biodiversity as a source of bioactive compounds. Food Res. Int. 48 (1), 170179. Prado, L.C. da S., 2013. Avaliac¸a˜o da atividade gastroprotetora de extrato aquoso de folhas de Eugenia dysenterica DC. e Campomanesia pubescens O. Berg. 91f. Dissertac¸a˜o de mestrado. Universidade Federal de Uberlaˆndia, Uberlaˆndia, MG. Ribeiro, E.M.G., 2011. Atividade antioxidante e polifeno´is totais do fruto de cagaita (Eugenia dysenterica DC) com e sem casca. Dissertac¸a˜o de mestrado. 77f. Universidade Federal do Rio de Janeiro, Faculdade de Farma´cia. Rio de Janeiro, RJ. Rocha, C., Cobucci, R. de M.A., Maitan, V.R., Silva, O.C., 2008. Elaborac¸a˜o e avaliac¸a˜o de iogurte sabor frutos do cerrado. B. CEPPA. 26 (2), 255266. Rocha, M.S., Figueiredo, R.W., Arau´jo, M.A.M., Moreira-Arau´jo, R.S.R., 2013. Caracterizac¸a˜o fı´sico-quı´mica e atividade antioxidante (in vitro) de frutos do cerrado piauiense. Rev. Bras. Frutic. 35 (4), 933941. Roesler, R., Malta, L.G., Carrasco, L.C., Holanda, R.B., Sousa, C.A.S., Pastore, G.M., 2007. Atividade antioxidante de frutas do cerrado. Cieˆnc. Tecnol. Aliment. 27 (1), 5360. Santos, M.N.G. dos, 2015. Avaliac¸a˜o de polpa de cagaita (Eugenia dysenterica DC.) submetida ao congelamento e atomizac¸a˜o. Dissertac¸a˜o de mestrado. 107f. Universidade Federal de Goia´s, Programa de Po´s-Graduac¸a˜o em Cieˆncia e Tecnologia de Alimentos. Goiaˆnia, GO. Silva, J.A., Silva, D.B., Junqueira, N.T.V., Andrade, L.R.M., 1994. Frutas nativas dos cerrados. EMBRAPA-CPAC, Brası´lia. Silva, M.R., Lacerda, D.B.C.L., Santos, G.G., Martins, D.O., 2008. Caracterizac¸a˜o quı´mica de frutos nativos do cerrado. Cieˆncia Rural. 38 (6), 17901793. Silva, C.D.M., da, Pires, C.R.F., Lima, J.P., Pereira, A.S., Silva, C.A., 2015. Desidratac¸a˜o osmo´tica para obtenc¸a˜o de cagaita passa. J. Bioeng. Food Sci. 02 (4), 226233. Silveira, C.E.S., Palhares, D., Pereira, L.A.R., Pereira, K.B.D., Silva, F.A.B., 2013. Strategies of plant establishment of two Cerrado species: Byrsonima basiloba Juss. (Malpighiaceae) and Eugenia dysenterica Mart. ex DC (Myrtaceae). Plant Sp Biol. 28 (2), 130137. Souza, E.R.B., Naves, R.V., Oliveira, M.F., 2013. Inı´cio da produc¸a˜o de frutos de cagaiteira (Eugenia dysenterica DC.) implantada em Goiaˆnia, GO. Rev. Bras. Frutic. 35 (3), 906909. Souza, E.R.B., Naves, R.V., Borges, J.D., Vera, R., Fernandes, E.P., Silva, L., et al., 2008. Fenologia de cagaiteira (Eugenia dysenterica DC.) no Estado de Goia´s. Rev Bras Frutic. 30 (4), 10091014. Souza, E.R.B., 2006. Fenologia, dados biome´tricos, nutric¸a˜o de plantas e qualidade de frutos de cagaiteira (Eugenia dysenterica DC.) no Estado de Goia´s. 114f. Tese de Doutorado. Universidade Federal de Goia´s, Goiaˆnia, GO. Zucchi, M.I., Brondani, R.P.V., Pinheiro, J.B., Chaves, L.J., Coelho, A.S.G., Vencovsky, R., 2003. Genetic structure and gene flow in Eugenia dysenterica DC. in the Brazilian Cerrado utilizing SSR markers. Genet. Mol. Biol. 26 (4), 449457. Zucchi, M.I., Pinheiro, J.B., Chaves, L.J., Coelho, A.S.G., Couto, M.A., Morais, L.K., et al., 2005. Genetic structure and gene flow of Eugenia dysenterica natural populations. Pesq Agropec Bras. 40 (10), 975980.
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Caju—Anacardium occidentale Edy Sousa de Brito1, Ebenezer de Oliveira Silva1 and Sueli Rodrigues2 1
Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil, 2Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Chapter Outline Botanical and Agronomical Aspects 85 Fruit Physiology and Biochemistry 85 Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolics and Antioxidant Compounds Among Others 86
Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application References
87 88 88
BOTANICAL AND AGRONOMICAL ASPECTS The cashew tree originates from Brazil, occurring naturally on Caatinga, Cerrados and Amazonian biomes (Fig. 1). Nowadays, the cashew tree is grown around the world especially in Brazil, Vietnam, India, Nigeria, Indonesia, Philippines, Benin, Guinea-Bissau, and the Ivory Coast. It belongs to Anacardiaceae family and the genera Anacardium has approximately 22 species; Anacardium occidentale has the commercial utilization. The cashew tree is evergreen with different sizes, but usually, it is from 8 to 15 m height. The real fruit from cashew tree is the nut, a brown, reniform achene composed of the pericarp (shell) and the almond. The peduncle, known as the cashew apple (Fig. 2), responsible for 90% of the weight, is, in fact, a pseudofruit. Its color ranges from yellow to red. Both parts are edible, but the nut needs to be removed from the shell that contains a corrosive liquid called “cashew nut shell liquid.” Fruit set occurs in the dry season, and normally it takes nearly 60 days from fruit set to harvest. The nut establishes first, and after that, the peduncle grows quickly until its ripening stage. In 2014, according to the FAO (www.fao.org/faostat/en/), countries around the world produced 3,713,467 t of cashew nuts (with shell). Africa was responsible for 49.9%, Asia 46.6%, and Americas 3.5%. The top 10 producing countries were Nigeria (855 kt), Vietnam (849 kt), India (703 kt), Ivory Coast (448 kt), Benin (165 kt), Philippines (143 kt), Guinea-Bissau (130 kt), Brazil (127 kt), United Republic of Tanzania (123 kt), and Indonesia (119 kt). In the same year, the world produced 1,889,934 t of cashew apple, mainly in Brazil (1766 kt), followed by Mali (91 kt) and Madagascar (74 kt).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The first report on cashew apple physiology (Biale and Barcus, 1970) indicated that the peduncle (pseudofruit) has a high rate of respiration at 20 C, ranging from 770 to 890 mmol CO2/kg per h. This accelerated metabolism makes cashew apple highly perishable; under ambient conditions (without cooling and high relative humidity), it lasts only 1 or 2 days. However, its respiratory pattern is nonclimateric (Irtwange, 2006; Paul et al., 2012) and the production of ethylene, at 20 C, is very low, ranging from 8 to 17 ηmol C2H4/kg per h (Pratt and Mendoza, 1980). During maturity stages 17 (Figueiredo et al., 2002), the cashew apple changes color due to chlorophyll loss and synthesis of other pigments. According to these authors, from stages 1 to 7, the loss of chlorophyll (from 53 to 7 mg/ 100 g) was parallel to the gradual increase in carotenoid (from 1.25 to 32.0 mg/100 g) and anthocyanin pigments (from 4.5 to 21.5 mg/100 g). There is a decrease in acidity and astringency and increase in soluble solids, reducing sugars and ascorbic acid (Figueiredo et al., 2002) as well as changes in the enzymatic antioxidant system (Lopes et al., 2015). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00012-5 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Cashew tree.
FIGURE 2 Cashew fruit (nut and peduncle).
Mature cashew apple color may vary from yellow to red, and there is a market trend towards red cashew apple as opposed to yellow ones (Filgueiras et al., 1999). According to these authors, quality of cashew apple for fresh consumption is also related to low astringency and acidity, sweetness, size (48 per tray) and shape (pear shaped).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING, VITAMINS, MINERAL, PHENOLICS AND ANTIOXIDANT COMPOUNDS AMONG OTHERS Cashew apple juice has a typical soluble solids content of 1012 Brix, reducing sugar content of 9.8 g/100 g and total sugars of 9.9 g/100 g (Damasceno et al., 2008). Among the reducing sugars, glucose (4.3 g/100 g) and fructose (3.7 g/
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100 g) are the major constituents (Luz et al, 2008). Cashew apple juice is considered a good source of ascorbic acid (145161 mg/100 mL). Based on kinetic studies, cashew apple juice antioxidant activity was attributed mainly to its ascorbic acid content (Rufino et al., 2009). Cashew apple juice also contains citric, malic, and tartaric acids (434578, 238237, 2127 mg/100 mL, respectively) (Scherer et al., 2008). Cashew apple has a total dietary fiber content of 209 g/kg, most of it being insoluble (88%). This fiber has nonextractable polyphenols that were more abundant than extractable polyphenols. These nonextractable polyphenols linked to dietary fiber would reach the colon and can improve the colonic antioxidant status (Rufino et al., 2010). The cashew nut corresponds to nearly 10% of the whole fruit weight and is rich in unsaturated lipids such as oleic and linoleic (57% and 21%, respectively) acids. Its oil contains squalene and γ-tocoferol (89 and 57 mg/g of oil, respectively) besides β-sitosterol, stigmasterol, and campesterol (1768, 117 and 105 mg/g of oil, respectively) (Ryan et al., 2006). The amount of β-sitosterol in 100 g of nut was estimated to be 113 mg in a total of 150 mg of phytosterols (Phillips et al., 2005). The nut has a dietary fiber amount of 3.6% (Cardozo and Li, 1994). The nuts contain anacardic acids, known alkyl phenols with bioactivity, in a total of 1.06 and 0.64 g/kg for unroasted and roasted nuts, respectively (Trevisan et al., 2006). Cashew apple main phenolics are the flavonoids, notably, glycosidic flavonols, among them 3-O-galactoside, 3-Oglucoside, 3-O-rhamnoside, 3-O-xylopyranoside, 3-O-arabinopyranoside, and 3-O-arabinofuranoside derived from myricetin (0.1511 mg/g dry weight) and quercetin (0.1139 mg/g dry weight) (Brito et al., 2007). In minor amounts, gallic acid and its derivatives are also found in cashew apple (Michodjehoun-Mestres et al., 2009; Cunha et al., 2017). The brightly red cashew apple peel contains a unique anthocyanin identified as 7-O-methylcyanidin 3-O-β-D-galactopyranoside. Another phenolic compound present in cashew is the cinnamic acid derivative 1-O-trans-cinnamoyl-β-D-glucopyranose. It is absent in the immature cashew apple, but at its maturity stage the concentration rises up to 620 mg/100 g of fresh weight and its production is correlated to PAL activity (Michodjehoun-Mestres et al., 2009; Cunha et al., 2017). Anacardic acids were also associated with the cashew apple (6 g/kg) (Trevisan et al., 2006), mainly associated to the fiber portion and its content is influenced by the maturity stage (Cunha et al., 2017). Both β-cryptoxanthin and β-carotene were the major carotenoids found in cashew apples and its products (Assunc¸a˜o and Mercadante 2003a,b; Schweiggert et al., 2016). The carotenoid concentration is higher in the peel (28155278 μg/ 100 g fresh weight) than the pulp (6932228 μg/100 g fresh weight) and has variations as the cashew apple color differs from yellow to red (Schweiggert, 2013). Moreover, a concentrated carotenoid extract (54 mg/kg) from the byproduct of juice processing contains also auroxanthin, mutatoxanthin, lutein, and zeaxanthin (Abreu et al., 2013). GC/MS and GCO analyses confirmed that cashew apple juice has a complex aroma profile and that its typical flavor is formed from the contributions of a wide spectrum of compounds. The main volatile contributors to cashew apple flavor are the esters ethyl 3- methyl butanoate, methyl 3-methyl butanoate, ethyl butanoate, ethyl trans-2-butenoate, methyl butanoate and methyl 3-methyl pentanoate. The compounds with green has notes cis-3-hexenol, 2-methyl-2pentenal and hexanal (Garruti et al., 2003). Additional to vitamin C, cashew juice is also rich in folate (Sancho et al., 2012).
HARVEST AND POSTHARVEST CONSERVATION According to Filgueiras et al. (1999), there are many useful indices for identifying the harvest point such as color, firmness, and composition. However, from a practical standpoint, the producer harvests cashew apple when it is easily detachable from the three by hand. The harvester should hold the cashew apple carefully, using only the tips of the fingers, and make a small twist clockwise or counterclockwise, but without pulling it. If the fruit is ripe, it will be easily detached from the tree. Once harvested, it is advisable to pack the cashew apples in single layers into plastic boxes (15 cm deep with openings at the bottom and sides), and lined with a layer of foam rubber (1 cm), aiming to avoid physical damage as well as to facilitate heat exchange. In the orchard, the plastic boxes containing cashew apples should be sat in the shade and taken to the packing house as quickly as possible. Upon arrival at the packing house the following actions are recommended (Berry and Sargent, 2011): grading, packing, palletization, rapid cooling (for more details, see Filgueiras et al., 1999), and refrigerated storage. In Brazil, the number of cashew apples per retail tray determines the commercial grading (Filgueiras et al., 1999). Cashew apples are packed in single layers into plastic trays (length (21 cm), width (14 cm), and depth (35 cm) depending on the cashew apple diameter). Grading is made based on the number of cashew apples per tray, which usually varies from 4 to 8. In Brazil, types 4 and 5 are preferred and attract higher prices. For more details on the Brazilian classification system, please see Filgueiras et al. (1999).
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The trays are covered with plastic film (PVC, 12 μm) (Moura et al., 2004), labeled then placed into corrugated boxes designed to facilitate palletization (Berry and Sargent, 2011). Refrigerated storage: Cashew apple, like most tropical fruits, is sensitive to chilling injury. This means that if it is stored at a temperature below its tolerance range, it may develop adverse symptoms such as brown spots on the bark, change colors (from reddish or orange to brownish tones), and softening. However, the procedure of covering with plastic film reduces chilling injury symptoms, allowing storage at 5 C for red cashew apples, and at 3 C for orange ones. Also, when cashew apples are sealed with plastic film, the inner atmosphere of the package (headspace) is passively modified (passive modified atmosphere, MAP), decreasing the oxygen pressure and increasing carbon dioxide as a result of the cashew’s own metabolism. This change in atmosphere, together with refrigeration, reduces the respiratory rate and extends shelf postharvest life (from 2 days) to more than 15 days (Moura et al., 2004).
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION The cashew is an important industrial crop cultivated for commercial purpose in many countries. The most valuable product from cashew tree is the cashew nut, which is the real fruit. The nut is removed from the shell and toasted and distributed around the word. The pseudofruit or the cashew apple is processed into many products such as jams, juices, syrup, icecream, and sweets. Cashew apple juice is produced by pressing the cashew apple into an expeller press. The juice is extracted, and the bagasse (the fiber portion) is separated from the juice. The juice is then homogenized, thermally treated and bottled, and is commercialized as concentrated juice or ready to drink. The juice can be consumed pure or is mixed with other fruits (Carvalho et al., 2007). The clarified cashew apple juice is obtained by adding gelatin to the cashew apple juice. The gelatin removes the juice tannins and promotes the precipitation of suspended solids. The clarified cashew juice is used as raw material to prepare a popular beverage in Brazilian Northwest named “cajuı´na.” Cajuı´na is produced by heating the glass bottled clarified cashew apple juice. The heat treatment promotes the microbial stabilization increasing the product shelf life. The clarified cashew apple juice is also used to produce a carbonated soft drink, which is also appreciated in Brazil. The clarified cashew apple juice is also used to produce the cashew syrup obtained by vacuum concentration of the clarified cashew juice. The cashew syrup is rich in minerals and sugars and presents a pleasant aroma and flavor. The syrup can be used with icecream to or can be consumed like honey with toast and yogurt, for instance (Guilherme et al., 2009). Products other than the traditional juice have been developed using the cashew peduncle. Probiotic cashew juice was developed using the clarified. The juice was fermented by Lactobacillus casei and is alternative for probiotic consumption for those who do not consume dairy-based products (Pereira et al., 2011). The probiotic juice was sensory evaluated and good acceptance and a shelf life of at least 42 at 4 C with good preservation of the vitamin C content (Pereira et al., 2013). Prebiotic cashew apple juice was also developed by enzyme synthesis. The clarified juice was showed to be adequate for the prebiotic oligosaccharides synthesis directly into the juice. The prebiotic oligosaccharides synthesis decreased the level of the product sugar (Silva et al., 2014). The cashew bagasse is rich in fibers and antioxidant compounds. The bagasse was ultrasound processed to prepare a puree rich in vitamins, phenolics, and with a pleasant aroma. The puree resembled a fruit smoothie (Fonteles et al., 2016).
REFERENCES Abreu, F.P., Dornier, M., Dionisio, A.P., Carail, M., Caris-Veyrat, C., Dhuique-Mayer, C., 2013. Cashew apple (Anacardium occidentale) extract from by-product of juice processing: a focus on carotenoid. Food Chem. 138, 2531. Assunc¸a˜o, R.B., Mercadante, A.Z., 2003a. Carotenoids and ascorbic acid composition from commercial products of cashew apple (Anacardium occidentale L.). J. Food Comp. Anal. 16, 647657. Assunc¸a˜o, R.B., Mercadante, A.Z., 2003b. Carotenoids and ascorbic acid from cashew apple (Anacardium occidentale L.) variety and geographic effects. Food Chem. 81, 495502. Berry, A.D., Sargent, S.A., 2011. Cashew apple and nut (Anacardium occidentale L.), Postharvest Biology and Technology of Tropical and Subtropical Fruits, vol. 2. Yahia, EM Woodhead Publishing Limited, Cambridge, pp. 414422. Biale, J.B., Barcus, D.E., 1970. Respiratory patterns in tropical fruits of the Amazon Basin. Trop. Sci. 12, 93104. Brito, E.S., Arau´jo, M.C.P., Lin, L.Z., Harnly, J., 2007. Determination of the flavonoid components of cashew apple (Anacardium occidentale) by LC-DAD-ESI/MS. Food Chem. 105, 11121118. Cardozo, M.S., Li, B.W., 1994. Total dietary fiber content of selected nuts by two enzymatic-gravimetric methods. J. Food Comp. Anal. 7, 3743. Carvalho, J.M., Maia, G.A., Figueiredo, R.W., Brito, E., Rodrigues, S., 2007. Development of a blended non-alcoholic beverage composed of coconut-water and cashew apple juice containing caffeine. J. Food Quality. 30, 664681.
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Cunha, A.G., Brito, E.S., Moura, C.F.H., Ribeiro, P.R.V., Miranda, M.R.A., 2017. UPLC-qTOF-MS/MS-based phenolic profile and their biosynthetic enzyme activity used to discriminate between cashew apple (Anacardium occidentale) maturation stages. J. Chromatogr. B. 1051, 2432. Damasceno, L.F., Fernandes, F.A.N., Magalha˜es, M.M.A., Brito, E.S., 2008. Non-enzymatic browning in clarified cashew apple juice during thermal treatment: kinetics and process control. Food Chem. 106, 172179. Figueiredo, R.W., Lajolo, F.M., Alves, R.E., Filgueiras, H.A.C., 2002. Physicalchemical changes in early dwarf cashew pseudofruits during development and maturation. Food Chem. 77 (3), 343347. Filgueiras, H.A.C., Alves, R.E., Mosca, J.L., Menezes, J.B., 1999. Cashew apple for fresh consumption: research on harvest and postharvest technology in Brazil. In: International Symposium Effect of Pre-& Postharvest factors in Fruit Storage, vol. 485, pp. 155160. Fonteles, T.V., Leite, A.K.F., Silva, A.R.A., Carneiro, A.P.G., Miguel, E., Cavada, B.S., et al., 2016. Ultrasound processing to enhance drying of cashew apple bagasse puree: influence on antioxidant properties and in vitro bioaccessibility of bioactive compounds. Ultrason. Sonochem. 31, 237249. Garruti, D.S., Franco, M.R.B., Silva, M.A.A.P., Janzantti, N.S., Alves, G.L., 2003. Evaluation of volatile flavour compounds from cashew apple (Anacardium occidentale L) juice by Osme gas chromatography/olfatometry technique. J. Sci. Food Agric. 83, 14551462. Guilherme, A.A., Honorato, T.L., Dorneles, A.S., Pinto, G.A.S., Brito, E.S., Rodrigues, S., 2009. Quality evaluation of mesquite (Prosopis juliflora) pods and cashew (Anacardium occidentale) apple syrups. J. Food Process Eng. 32 (4), 606622. Irtwange, S.V., 2006. Application of modified atmosphere packaging and related technology in postharvest handling of fresh fruits and vegetables. Agric. Eng. Int. CIGR Ejournal. 4 (VIII), 113. Lopes, M.M.A., Moura, C.F.H., Germano, T., Cunha, A.G., Rabelo, M.C., Souza, K.O., et al., 2015. Behavior of enzymatic antioxidant system during development and ripening of cashew apples. J. Agric. Environ. Sci. 4 (2), 1824. Luz, D.A., Rodrigues, A.K.O., Silva, F.R.C., Torres, A.E.B., Cavalcante Jr, C.L., et al., 2008. Adsorptive separation of fructose and glucose from an agroindustrial waste of cashew industry. Bioresour. Technol. 99, 24552465. Michodjehoun-Mestres, L., Amraoui, W., Brillouet, J.M., 2009. Isolation, characterization and determination of 1-O-trans-cinnamoyl-β-D-glucopyranose in the epidermis and flesh of developing cashew apple (Anacardium occidentale L.) and four of its genotypes. J. Agric. Food Chem. 57, 13771382. Moura, C.F.H., Figueirado, R.W., Alves, R.E., Araujo, P.G.L., Silva, A.S., Silva, E.O. 2004. Avaliac¸a˜o respirato´ria de clones de cajueiro ana˜o precoce (Anacardium occidentale L.) armazenados sob diferentes camadas de PVC. In: Proceedings of the Interamerican Society for Tropical Horticulture, vol. 47, pp. 143145. Paul, V., Pandey, R., Srivastava, G.C., 2012. The fading distinctions between classical patterns of ripening in climacteric and non-climacteric fruit and the ubiquity of ethylene—an overview. J. Food Sci. Technol. 49 (1), 121. Pereira, A.L.F., Maciel, T.C., Rodrigues, S., 2011. Probiotic beverage from cashew apple juice fermented with Lactobacillus Casei. Food Res. Int. 5, 12761283. Pereira, A.L.F., Almeida, F.D.L., de Jesus, A.L.T., Costa, J.M.C., Rodrigues, S., 2013. Storage stability and acceptance of probiotic beverage from cashew apple juice. Food Bioprocess Technol. 6, 31553165. Phillips, K.M., Ruggio, D.M., Ashraf-Khorassani, M., 2005. Phytosterol composition of nuts and seeds commonly consumed in the United States. J. Agric. Food Chem. 53, 94369445. Pratt, H.K., Mendoza Jr., D.B., 1980. Influence of nut removal on growth and ripening of the cashew apple. J. Am. Soc. Hortic. Sci. 105 (4), 540542. Rufino, M.S.M., Fernandes, F.A.N., Alves, R.E., Brito, E.S., 2009. Free radical-scavenging behavior of some north-east Brazilian fruits in a DPPH system. Food Chem. 114, 693695. Rufino, M.S.M., Pe´rez-Jime´nez, J., Tabernero, M., Alves, R.E., Brito, E.S., Saura-Calixto, F., 2010. Acerola and cashew apple as sources of antioxidants and dietary fibre. Int. J. Food Sci. Technol. 45, 22272233. Ryan, E., Galvin, K., OConnor, T.P., Maguire, A.R., OBrien, N.M., 2006. Fatty acid profile, tocopherol, squalene and phytosterol content of brazil, pecan, pine, pistachio and cashew nuts. Int. J. Food Sci. Nutr. 57, 219228. Sancho, S.O., Silva, A.R.A., Maia, Rodrigues, S., 2012. Folate determination in cashew apple juice: method development and validation. Rev. Holos. 4, 106119. Scherer, R., Rybka, A.C.P., Godoy, H.T., 2008. Simultaneous determination of tartaric, malic, ascorbic and citric acids in acerola, ac¸ai and cashew pulps, and stability evaluation in cashew juices. Quı´m. Nova. 31, 11371140. Schweiggert, R.M., Vargas, E., Conrad, J., Hempel, J., Gras, C.C., Ziegler, J.U., et al., 2016. Carotenoids, carotenoid esters, and anthocyanins of yellow-, orange-, and red-peeled cashew apples (Anacardium occidentale L.). Food Chem. 200, 274282. Silva, I.M., Rabelo, M.C., Rodrigues, S., 2014. Cashew juice containing prebiotic oligosaccharides. J. Food Sci. Technol. 51 (9), 20782084. Trevisa, M.T.S., Pfundestein, B., Haubner, R., Wurtele, G., Spiegelhalder, B., Bartsch, H., et al., 2006. Characterization of alkyl phenols in cashew (Anacardium occidentale) products and assay of their antioxidant capacity. Food Chem. Toxicol. 44, 188197.
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Cambuci—Campomanesia phaea (O. Berg.) Landrum Tatiane de O. Tokairin, Horst Bremer Neto and Angelo P. Jacomino University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Physiology and Biochemistry of Cambuci Fruit Chemical Composition and Nutritional Value Including Vitamins, Minerals, Phenolics and Antioxidant Compounds
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Sensory Attributes Harvest and Postharvest Conservation Perspectives and Industrial Applications Acknowledgments References
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CULTIVAR ORIGIN AND BOTANICAL ASPECTS The cambuci tree (Campomanesia phaea (O. Berg.) Landrum) is a fruitful plant that belongs to the family Myrtaceae, within the genus Campomanesia, having the synonyms Abbevillea phaea O. Berg and Paivaea langsdorfii O. Berg. (Lorenzi et al., 2006). The cambuci tree produces a fruit commonly known as cambuci. Cambuci fruit is also known as ubucambuci, cambuhi, camuci, camucim, camoti, cambucy and cambuchi, which refer to an indigenous vessel or bowl called Kamu-si (Donadio et al., 2002; Andrade et al., 2011). The enormous potential of cambuci has encouraged producer groups formation, activities from nongovernmental organizations devoted to sustainability issues, and the creation of food festivals (Cambuci Route), in addition to research projects in public institutions. The cambuci plant is native to the Atlantic rainforest, a threatened biome which extends along the Brazilian east coast, and is also commonly found in the Brazilian southeastern region. Cambuci plants are found in the states of Rio de Janeiro, Minas Gerais and Sa˜o Paulo, particularly at Serra do Mar (Lorenzi et al., 2006). The climate of this region varies from tropical to humid subtropical, with an average annual precipitation of 15004000 mm. In the area represented by the counties of Paraibuna, Saleso´polis and Natividade da Serra (Sa˜o Paulo state), cambuci trees grow in backyards, in nature reserves, as well as in small commercial orchards that supply the incipient market of fresh cambuci fruits and cambuci-derived products. This species grows and produces fruits in acidic soils containing high organic matter content, low concentrations of phosphorus, calcium, magnesium and potassium, and a high concentration of aluminum. The cambuci tree is a semi-deciduous, halophytic, and selective hygrophilous plant (Donadio et al., 2002; Lorenzi et al., 2006). Its crown is elongated, reaching more than 16 meters tall in a natural habitat. Cambuci trees grown in nonirrigated commercial crops at escarpment of Serra do Mar, e.g., reach 48 and 1216 m in height when reaching the ages of 10 and 40 years, respectively. The cambuci trees’ trunk exhibits a dark gray tone and a peeling texture, which are characteristics of the family Myrtaceae (Donadio et al., 2002). This species presents a high phenotypic variability, which is clearly manifested in the morphological and chemical characteristics of its fruits. Cambuci fruit exhibits significant phenotypic variations of interest for genetic engineering, management and agroindustrial usages. Cambuci trees’ leaves are glabrous, sub coriaceous, stalked, and vary in shape from ovate to ovateoblong and obovateoblong. Their adaxial face is bright green, while the abaxial face is light green (Donadio et al., 2002). The leaves are 710 cm long and 34 cm width, and display undulate margins. Their venation is pinnate with secondary veins oppositely paired (Donadio et al., 2002). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00013-7 © 2018 Elsevier Inc. All rights reserved.
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The flowers are hermaphroditic, pentamerous, with insertion at the armpit of the branches. They exhibit a white color and large amount of stamens and pollen, which is a typical characteristic of the family Myrtaceae (Kawasaki et al., 1997; Donadio et al., 2002), with anthesis duration of 2 days (Cordeiro, 2015). Cambuci fruit is a smooth berry with rhomboid shape and a thin green peel with membranous consistency (Donadio et al., 2002). Each cambuci fruit contains approximately 913 seeds, among which approximately 30% are fertile. The seeds are orbicular and flat, and are a pale white color (Donadio et al., 2002). The cambuci tree reproduction requires transfer of pollen among trees (self-incompatible reproductive system), thus pollination methods become essential, mainly the use of nocturnal and crepuscular bees such as Megalopta sodalis, Megommation insigne, Ptiloglossa latecalcarata, Zikanapis seabrai, and Apis mellifera (Cordeiro, 2015). Furthermore, individuals with self-incompatible reproductive systems require appropriate strategies of composition and orchard management to favor the presence of pollinators and pollen transfer between individuals, e.g., using different cambuci plant varieties, insecticides selective to pollinators, surrounding vegetation maintenance, and beehives insertion.
HARVEST SEASON Cambuci tree flowering occurs continuously throughout the spring and early summer (OctoberJanuary), reaching a maximum intensity between November and December. However, a low intense extemporaneous flowering also occurs throughout the year. Fructification extends until June, with the highest intensity in March. The flowering occurs during a period of up to 4 months, with the opening of a few flowers per day (Cordeiro, 2015). A single tree can present fruits with different ripening levels, even during the harvest season, which requires daily harvest. At the peak harvest window, some producers harvest cambuci fruits up to 3 times per day. In general, the period from flowering to harvesting is 150 days. Ripe cambuci fruits maintain their green peel color, which becomes less bright and intense (yellowgreen), but they lose firmness and fall off trees naturally. The cambuci harvest typically consists of hand-picking fruits from ground.
ESTIMATED ANNUAL PRODUCTION The average annual fruit production from cambuci trees with age between 10 and 12 years, and grown in nonirrigated agroforestry systems in the region of Paraibuna, Sa˜o Paulo, is of 10 kg of fruit per tree. It has been reported that cambuci trees produce 50 kg of fruits (Douglas Bello, 2015, personal information). Moreover, according to producers and technicians, some cambuci trees can produce more than 100 kg of fruit per year.
PHYSIOLOGY AND BIOCHEMISTRY OF CAMBUCI FRUIT The physiology and biochemistry of cambuci fruit is practically unknown. Knowledge about respiration, ripening, development and physiological changes of cambuci fruit is based on observations in field and recently started preliminary works. It has been supposed that cambuci is a nonclimacteric fruit. Usually, producers harvest cambuci after its complete ripening, because the fruit does not ripen if harvested at a stage preceding its natural abscission. This behavior has been proven by studies on cambuci respiration pattern, which are underway at the Postharvest Laboratory of Horticultural Products of ESALQ/USP, Brazil. Recent studies show that cambuci exhibits symptoms of chilling injury when they are stored under refrigeration. Because cambuci is a tropical fruit, it is possible that physiological disorders are caused by low temperatures, which generally occur when the fruit is stored at temperatures below a critical threshold above the freezing temperature. This results in quantitative and qualitative postharvest losses (Levitt, 1980; Wang, 1994). However, further studies on cambuci freezing storage are still necessary to explain this behavior.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING VITAMINS, MINERALS, PHENOLICS AND ANTIOXIDANT COMPOUNDS Cambuci shows a pulp yield larger than 80% (84.68% 6 4.1) and high moisture content (80.47% 6 1.03). Its centesimal composition is determined by lipids (3.16% 6 0.84), ashes (2.64% 6 0.70), proteins (8.86% 6 1.45), insoluble fibers (33.12% 6 3.46) and soluble fibers (5.50% 6 1.38). Cambuci is also chemically characterized by its high acidity. In an unpublished study about genetic diversity of plants originated from seeds, the titratable acidity (TA) values ranged from
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1.29% to 4.5% of citric acid. The main organic acids present in cambuci fruits are citric acid (38 mg/g), malic acid (25 mg/g), and succinic acid (67 mg/g). The soluble solids (SSs) content of cambuci ranges from 5.10 to 11.00 Brix, while the average SS/TA ratio is 4.62. These values are in good agreement with previous reports. Vallilo et al. (2005) and Sanches (2013) determined cambuci has a TA between 2.1% and 3.0% of citric acid and pH equal to 2.91. The SS content found by Sanches et Al. (2013) was approximately 10 Brix. Broad compositional differences among plants, in terms of ascorbic acid and phenolic compound contents, and antioxidant activity, suggest a considerable genetic variability among cambuci trees. This creates new perspectives for cambuci breeding programs devoted not only to increase production, but also to improve quality and functional properties of the fruits. Bianchini et al. (2016) observed from 120 individuals that the cambuci average ascorbic acid content ranges from 25.62 mg/100 g to 127.40 mg/100 g. Thus, cambuci can be considered as an important source of vitamin C according to the Brazilian legislation (Brasil, 1998), which recommends a vitamin C intake for adults of 60 mg/day. Recent studies reveal that cambuci juice consumption helps prevent diseases caused by oxidative stress, in addition to being a good nutritional strategy. The beneficial properties of cambuci to human health are attributed to phenolic compounds, flavonoids and sugars, as well as to the antioxidant and antiproliferative activities of the fruit (Ferrari, 2014). The total phenolic compound contents of cambuci range from 330.50 mg GAE/100 g to 3526.04 mg GAE/100 g. According to the classification proposed by Vasco et al. (2008), cambuci presents large phenolic contents (.500 mg GAE/100 g). However, these values are larger than those recently determined by Ferrari et al. (2014), 367.84 6 10.79 mg GAE/100 g. Regarding antioxidant activity measured by the DPPH radical scavenging capacity method, cambuci exhibits an average activity of 65.03 μmol trolox/g pulp (wet basis), which is superior to that of blueberry which is 191.88 μmol trolox/g pulp on a wet basis (Lutz et al., 2015). Gonc¸alves (2008) found an average antioxidant activity of 139 μmol trolox/g pulp on a dry cambuci fruit basis.
SENSORY ATTRIBUTES Ripe cambuci presents an astringent taste and a citrus, slightly sweet, and persistent aroma, which causes a quite pleasant olfactory sensation (Vallilo et al., 2005). Large variations in mass (27190 g), diameter (4.69.3 cm) and length (3.85.3 cm) have been observed among cambuci fruits harvested from wild trees and trees cultivated at Serra do Mar. The cambuci pulp exhibits a cream color and yield is between 80% and 92%. It is astringent and presents a specific aroma. Cambuci fruits are acidic and contain high tannin contents (substances responsible for pulp astringency), which generally hamper the consumption of fresh fruit. In this case, selection of cultivars displaying low concentrations of tannins, and development of distanninization methods for cambuci are aspects that must be addressed in future research.
HARVEST AND POSTHARVEST CONSERVATION Cambuci harvest occurs after natural abscission of fruits. At this stage, fruits are ripened and exhibit a translucent appearance, green-yellowish tone, rounded corner and a pulp with low firmness (Fig. 1). Hand harvesting ripe cambuci after its natural abscission is not appropriate although it is a routine traditionally used by farmers. Mechanical injuries
FIGURE 1 Unripe cambuci (A) and ripe cambuci (B) fruits.
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caused by falling, and resultant contact between ripe cambuci fruits and soil, lead to quality loss, microbiological contamination, dehydration, and self-life reduction. Some techniques are recommended to prevent direct contact between cambuci fruits and soil, and to attenuate fall impact, for instance, covering the projection area of the cambuci tree’s crown with straw or analogous materials, as well as using plastic netting resembling an inverted umbrella beneath cambuci trees. The limited knowledge about physiology and postharvest behavior of cambuci is an important drawback to its commercial exploitation, because the idea that cambuci fruits become ripe and are ready for consumption only after natural abscission is already widespread among growers and technicians. Research in progress at the Postharvest Laboratory of Horticultural Products of ESALQ-USP indicates that ripe cambuci can be hand-harvested directly from trees before natural abscission, without prejudicing their intrinsic quality attributes. This also reduces microbiological contamination and increases the shelf-life of fresh cambuci fruits. Preliminary studies on physicochemical parameters of cambuci (total SS content, TA, vitamin C content and firmness) show that ripe cambuci fruits hand-harvested from trees display quality and shelf-life equivalent or superior to those of fruits hand-picked from ground. For example, loss by rot for cambuci fruits hand-picked from ground is 60%, which is much larger than that of fruits hand-picked from trees (30%). The major difficulty is to identify ripe cambuci fruits at the tree, because the differences of color and size between unripe and ripe fruits are subtle. Cambuci is habitually sold as frozen fruits in individual packages of 1 kg. Freezing of cambuci occurs in three stages, namely: (1) preselection, which consists in eliminating injured, unripe and rotten fruits; (2) sanitization, in which cambuci fruits are immersed into water containing chlorine-based sanitizers; and (3) freezing, in which the fruits are placed into plastic container and froze in a refrigerator at a temperature of 220 C. Research on cambuci harvest point from trees surely will contribute to the improvement of the postharvest technology of this tropical fruit. Basic storage techniques that could be explored in this regard, such as cold storage, will depend on correctly harvesting ripe cambuci fruits from trees.
PERSPECTIVES AND INDUSTRIAL APPLICATIONS Most of production of Brazilian cambuci is commercialized as frozen pulps or whole fruits. The main consumers of cambuci are restaurants of high gastronomy and coffee shops of Sa˜o Paulo, that use the fruit to make juices and a variety of recipes. Growers also process by hand a part of produced cambuci into jellies, liqueurs, wines, rum, syrups, preserves, biscuits, flours, cakes, mousses and icecream, among other consumer goods. Cambuci is increasingly receiving attention from consumers, and is leveraging the native fruit sector due to its attributes that are favorable for industrialization. Cambuci presents large fiber and pectin contents, high SS content, high pulp yield, and high TA, which are features with enormous industrial and commercial potentials. Moreover, the essential oil found into the leaves is highly valued by cosmetic and pharmaceutical industries (Adati, 2001).
ACKNOWLEDGMENTS The authors thank the National Council for Scientific and Technological Development (CNPq Process n 458123/20145) for the financial support, and H&H Fauzer, AUA Institute, Sı´tio do Belo, Sı´tio do Cambuci Alto da Serra and Sı´tio do Cambuci for the support, material and information provided for this work.
REFERENCES Adati, R.T., 2001. Estudos biofarmagno´stico de Campomanesia phae O. Berg. Landrum. Myrtacea, 2001. 128f. Dissertac¸a˜o (Mestrado em Farmacognosia) - Faculdade de Cieˆncias Farmaceˆuticas, Universidade de Sa˜o Paulo, Sa˜o Paulo. Andrade, B.A.G., Fonseca, P.Y.G., Lemos, F., 2011. Cambucio fruto, a rota, cultura, sustentabilidade e gastronomia. Ourivesaria da Palavra, Sa˜o Paulo. Bianchini, F.G., Balbi, R.V., Pio, R., Silva, D.F., Pasqual, M., Vilas Boas, E.V.B., 2016. Caracterizac¸a˜o morfolo´gica e quı´mica de frutos de cambucizeiro. Bragantia, Campinas. 75 (1), 1018. Brasil. Portaria no 685 de 27 de agosto de 1995, da Ageˆncia Nacional de Vigilaˆncia Sanita´ria (ANVISA). Princı´pios gerais para o estabelecimento de % nı´veis ma´ximos de contaminantes quı´micos em alimento. Dia´rio Oficial da Unia˜o, Brası´lia, DF, 24 set. 1998. Sec¸a˜o 1, no 183E, p. 03. % Cordeiro, G.D., 2015. Fenologia reprodutiva, polinizac¸a˜o e vola´teis florais do cambuci Campomanesia phaea (O. Berg) Landrun 1984Myrtaceae. Tese (Doutorado emEntomologia)Faculdade de Filosofia, Cieˆncias e Letras de Ribeira˜o Preto, Universidade de Sa˜o Paulo, Ribeira˜o Preto, 89 pp. Donadio, L.C., Moˆro, F.V., Servidone, A.A., 2002. Frutas Brasileiras. Novos Talentos, Jaboticabal.
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Ferrari, A.S., 2014. 82 pp. Avaliac¸a˜o de fitoquı´micos e das atividades antioxidante celular e antiproliferativa de suco de grumixama e (Eugenia brasiliensis) e do suco de cambuci (Campomanesia phaea). Tese (Mestrado em Biocieˆncias Aplicadas a Sau´de)Universidade Federal de Alfenas, Alfenas, MG. Gonc¸alves, A.E.S.S., 2008. Avaliac¸a˜o da capacidade antioxidante de fruta s e polpas de frutas nativas e determinac¸a˜o dos teores de flavono´ides e vitamina C. Dissertac¸a˜o (Mestre). Faculdade de Cieˆncias Farmaceˆuticas. Universidade de Sa˜o Paulo, Sa˜o Paulo, 88 pp. Kawasaki, M.L., Landrum, L.R., 1997. A rare and potentially economic fruit of Brazil: cambuci Campomanesia phaea (Myrtaceae). Econ. Bot. 51, 403407. Levitt, J., 1980. Responses of Plants to Environmental Stresses: Chilling, Freezing, and High Temperature Stresses. second ed. Academic Press, New York, NY, 497 pp. Lorenzi, H., Sartori, S.F., Bacher, B., Lacerda, M., 2006. Brazilian Fruits & Cultivated Exotics (for Consuming in Natura). Instituto Plantarum de Estudos da Flora, Sa˜o Paulo. Lutz, M., Herna´ndez, J., Henrı´quez, C., 2015. Phenolic content and antioxidant capacity in fresh and dry fruits and vegetables grown in Chile. J. Food. 13, 17. Sanches, M.C.R., 2013. Caracterizac¸a˜o do fruto de cambuci (Campomanesia phaea O. Berg) e efeito sobre a destanizac¸a˜o sobre o potencial funcional in vitro. Tese (Doutorado em Cieˆncias dos Alimentos e Nutric¸a˜o Experimental) Faculdade de Cieˆncias Farmaceˆuticas, Universidade de Sa˜o Paulo, Sa˜o Paulo, 92 pp. Vallilo, M.I., Garbelotti, M.L., Oliveira, E., Lamarco, L.C., 2005. Caracterı´sticas fı´sicas e quı´micas dos frutos de cambucizeiro (Campomanesia phaea). Rev. Bras. Frutic. 27, 241244. Vasco, C., Ruales, J., Kamal-Eldin, A., 2008. Total phenolic compounds and antioxidant capacities of major fruits from Ecuador. Food Chem. 111, 816823. Wang, C.Y., 1994. Chilling injury of tropical horticultural commodities. HortScience. 29 (9), 986988.
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Camu-camu—Myrciaria dubia (Kunth) McVaugh Juan C. Castro1, J. Dylan Maddox2,3 and Sixto A. Ima´n4 1
National University of the Peruvian Amazon, Iquitos, Peru, 2The Field Museum of Natural History, Chicago, IL, United States
3
American Public University System, Charles Town, WV, United States, 4National Institute of Agricultural Innovation, Iquitos, Peru
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season and Estimated Annual Production Fruit Physiology and Biochemistry Chemical and Nutritional Compositions Health-Promoting Phytochemicals
97 98 98 99 99
Sensory Characteristics Harvest and Postharvest Conservation Potential Industrial Application Acknowledgments References
102 102 103 103 103
CULTIVAR ORIGIN AND BOTANICAL ASPECTS Myrciaria dubia (Kunth) McVaugh “camu-camu” is a typical native fruit shrub found in the tropical rainforests of the Amazon. Natural populations of this species grow in dense areas exposed to substantial flooding (complete submergence for four to five months) on the banks of rivers, streams, lakes and swamps of Guyana, Venezuela (Casiquiare Oreda, Pargueni, Caura, and Orinoco), Colombia (Putumayo and Inirida), Ecuador, Brazil (Mac¸angana, Urupa, Javari, Madeira, and Black), and Bolivia (Villachica, 1996; Lim, 2012). The greatest concentration of natural populations and source of genetic variability, however, is found in the Loreto region of the Peruvian Amazon, specifically along the basins of the Amazon, Putumayo, Napo, Curaray, Tigre, Maran˜on, Yavari, Ucayali, Itaya, Nanay, Tahuayo, Pintuyacu, Ampiyacu, Apacayu, Manati, Orozam, and Curaray rivers (Villachica, 1996; Peters and Vasquez, 1987; Rodrigues et al., 2001). Camu-camu can adapt very well to different edaphoclimatic conditions. Populations can be found in the welldrained loamy oxisols and clay-rich floodplains of the Amazon River as well as in the sandy soils of black water rivers that are nutrient poor (Lim, 2012). In addition to its preferred habitat, it can thrive in land soils, acid soils, low fertility soils, and poor drainage soils (Villachica, 1996) that are present in land forms such as lowlands, riversides, low and high restinga, and others (Penn, 2006). This habitat flexibility has enabled the expansion of M. dubia cultivation to other macroregions such as the highlands and coast of Peru where increased production is essential to meet the growing regional, national, and global demand for fruit pulp and other products derived from this species. Camu-camu is approximately 48 m in height that branches from the base to form several secondary stems, which in turn branch out as an open vessel. The trunk (B14 cm in basal diameter) and branches are glabrous, cylindrical, smooth, and the bark is light or reddish brown, which peels off naturally in periods of drought (Peters and Vasquez, 1987; Ima´n et al., 2011). The shrub is deeply rooted and the roots contain numerous absorbing hairs. The leaves are opposed, single, petiolar, elliptical or lanceolate of 312 cm in length and 1.54.5 cm in width, with an acuminated apex and rounded base, provided with a central vein with 1820 pairs of lateral veins. The petiole is cylindrical with a length of 39 mm and width of 12 mm. The inflorescences are axillary with 112 (generally four) subsesiles and hermaphrodite flowers arranged in two pairs on the axis. The rounded ciliated bracts and bracteoles are persistent. The calyx is approximately 2 mm long and 2 mm wide and includes 4 sepals with apex broadly and the hypanthium is prolonged and circumscissile at the summit of the ovary and falls with the calyx as a unit after anthesis (Landrum and Kawasaki, 1997). The corolla has four white ovate petals of 34 mm long with a ciliated margin. The ovary is inferior with a simple style that is Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00014-9 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Myrciaria dubia “camu-camu” fruit.
1011 mm long and the androecium has 125 stamens of 610 mm in length and anthers of 0.50.7 mm length. Although camu-camu flowers are hermaphroditic, inbreeding is largely prevented by the lack of synchrony between the development of the gynoecium and androecium, leading to facultative allogamy (Villachica, 1996; Peters and Vasquez, 1987; Ima´n et al., 2011). The fruit is globular (Fig. 1), 1.04.0 cm in diameter and their weight averages 8.4 g. The shiny peel can be pink to deep red or even black when completely ripe, with a slightly pinkish pulp (Villachica, 1996; Peters and Vasquez, 1987; Ima´n et al., 2011). The seeds are kidney-shaped to ellipsoid, flattened bilaterally and are exalbuminous (reserve materials are accumulated within the cotyledons). A fruit contains one to four seeds with an average length of 13.5 6 1.6 mm and width of 4.8 6 0.6 mm. The average fresh seed weight is 440 6 170 mg. The elongated seed coats are brown, thin, and covered with spiny-celled villi (Uchiyama et al., 1996; Medina et al., 2014).
HARVEST SEASON AND ESTIMATED ANNUAL PRODUCTION Natural and cultivated populations are harvested between September and April. The estimated annual fruit production of camu-camu is highly variable in both natural and cultivated populations. For example, in Sahua Lake, a natural population located in the floodplain of the Ucayali river, Peters and Vasquez (1987) estimated that fruit production ranged between 9.5 and 12.7 t/ha per year. Recently, however, the Minister of Agriculture and the Agrarian Regional Direction of Loreto estimated that natural and cultivated populations in the Loreto Region fruit production ranged between 1.5 and 8 t/ha per year, with an average of 3 t/ha per year (Defilippi, 2011; Direccio´n Regional Agraria Loreto, 2010). This high variability is due to the high density of seedlings per hectare in some areas, which can be as dense as ten thousand (Peters and Vasquez, 1987). In addition, investigations have consistently shown that fruit production is highly and positively correlated (r values from 0.97 to 0.99) with the trunk basal diameter (Peters and Vasquez, 1987). In the Loreto region, there are 7820 ha of cultivated populations with an estimated fruit production of 5.7 to 12.7 t/ha per year (Defilippi, 2011). This variability is attributed to several factors, such as the use of unselected seeds obtained directly from natural populations (94% of cultivated areas) and only a small fraction of cultivated areas have been planted with improved seeds provided by the Instituto Nacional de Innovacio´n Agraria (INIA). This improved seed is an amalgamation of populations MD-014-INIA and MD-015-INIA that were obtained by a genetic improvement program conducted by INIA during the past 10 years. These populations are characterized by increased fruit production of .15 t/ha per year with high L-ascorbic acid (vitamin C) content of more than 2.0 g per 100 g of fruit pulp (Ima´n et al., 2011).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The development of camu-camu fruits from flowering to ripening takes a period of approximately 1415 weeks (Bardales et al., 2008; Neves et al., 2015). After anthesis, the fruits show a sigmoidal growth curve, characterized by
Camu-camu—Myrciaria dubia (Kunth) McVaugh
99
an initial period (until 60 days after anthesis) of rapid growth rate (B683 mg/day). In the second period, the growth rate decreases and the fruit reaches its final full size (B81 days after anthesis). Finally, ripening takes place, which is characterized by a slight decrease in weight and change in the fruit color from green to red and finally purple. Such changes are intended to reflect the onset of fruit ripening and senescence. The fruit exhibits nonclimacteric patterns both in respiration rate and ethylene production. In the first, because fruits are characterized by the absence of a respiratory peak and a decrease in respiration rate levels (below 100 mg CO2/kg per h) throughout development (Bardales et al., 2008; Neves et al., 2015; Gonza´les et al., 2013). Looking at ethylene production, the fruits exhibit a low and a steady-state production of this gaseous signal molecule during development and ripening (Bardales et al., 2008; Neves et al., 2015). In contrast to ethylene production, other biochemical components exhibit significant concentration variation during fruit development, such as total sugars, reducing sugars, soluble pectin, total flavonols, cyanidin-3-glucoside, and vitamin C (Neves et al., 2015; Alves et al., 2002; Chirinos et al., 2010). Vitamin C concentration, however, decreases in the last step of ripening (Neves et al., 2015). The biochemical components that exhibit decreases in concentrations are starch and total pectin. The decrease in total pectin is due to depolymerization and subsequent solubilization by catalytic activity of pectin methyl esterase and polygalacturonase (Neves et al., 2015; Alves et al., 2002). Also, our research group has conducted several biochemical and molecular studies related to vitamin C metabolism in camu-camu. First, we have demonstrated the capability for vitamin C biosynthesis of leaves, pulp, and peel through the D-mannose/L-galactose pathway, because we detected mRNAs of the six key genes (GDP-D-mannose pyrophosphorylase [GMP]), GDP-D-mannose-30 ,50 -epimerase, GDP-L-galactose phosphorylase, L-galactose-1-phosphate phosphatase, L-galactose dehydrogenase [GDH], and L-galactono-1-4-lactone dehydrogenase (GLDH)] and catalytic activities of the corresponding enzymes (GMP, GDH, and GLDH) (Castro et al., 2015). In addition, with nextgeneration sequencing, de novo assembly, and transcriptome annotation of the fruits we identified five metabolic pathways for vitamin C biosynthesis: animal-like pathway, myo-inositol pathway, L-gulose pathway, D-mannose/L-galactose pathway, and uronic acid pathway. We also identified transcripts coding enzymes involved in the ascorbate-glutathione cycle, polyphenol biosynthesis, starch and pectin metabolism, and several other metabolic pathways (Castro et al., 2015).
CHEMICAL AND NUTRITIONAL COMPOSITIONS Pioneering work on chemical and nutritional compositions of camu-camu fruits were performed in the early 1990s by Zapata and Dufour (1993). Further investigations have allowed us to understand, more exhaustively, the various chemical and nutritional components that are contained within this native fruit plant of the Amazon. The chemical and nutritional compositions of camu-camu fruits are shown in Table 1. These fruits are composed of carbohydrate, proteins, lipids, ash, and several other chemical constituents. It is also a good source of essential amino acids and fatty acids, as well as vitamin C, B-complex vitamins, and vitamin A. This fruit, however, is very interesting especially for their exceptional high content of vitamin C (0.962.99 g/100 g), which is approximately 60 times higher than that of orange juice (Villachica, 1996; Alves et al., 2002; Castro et al., 2015; Castro et al., 2015; Zapata and Dufour, 1993; Rodrigues and Marx, 2006). Additionally, it contains several minerals such as potassium, phosphate, sulfate, calcium, magnesium, chloride, sodium, copper, cobalt, iron, and selenium.
HEALTH-PROMOTING PHYTOCHEMICALS In the Loreto region of Peru, camu-camu is widely used in folk medicine for the treatment of diseases such as asthma, atherosclerosis, cataracts, depression, flu, gingivitis, glaucoma, hepatitis, infertility, migraine, osteoporosis, Parkinson’s disease, and malaria (Rengifo, 2009). These traditional uses are in agreement with recent investigations showing that camu-camu is a significant source of various bioactive phytochemicals with demonstrated beneficial properties for health (Table 2) (da Silva et al., 2012; Nascimento et al., 2013; Azeveˆdo et al., 2015; Zanatta and Mercadante, 2007; Kaneshima et al., 2016). For example, Inoue et al. (2008) demonstrated that camu-camu fruits provide powerful antioxidant and antiinflammatory properties in comparison to vitamin C tablets. Similarly, findings of Yazawa et al. (2011) suggest that camu-camu seed extract is a potentially useful material as a source of betulinic acid and as a functional food for the prevention of immune-related diseases. Also, the active compound 1-methylmalate, present in the juice of camu-camu, was found to have hepatoprotective activity, as evidenced by significantly suppressing D-galactosamine induced liver injury in rats (Akachi et al., 2010). In addition, ethanol extract of fruits exhibited antiplasmodial activity with the ferriprotoporphyrin inhibition test with IC50 5 1 μg/mL (Ruiz et al., 2011). The ethanolic and aqueous extract from the cortex of camu-camu have also demonstrated antiplasmodial activity against the chloroquine resistant strain
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TABLE 1 Chemical and Nutritional Compositions of Camu-Camu Fruit Pulp (per 100 g) Components
Contents in pulp Fresh
Freeze-dried
Moisture (g)
94.194.4
Carbohydrate (g)
3.54.7
Monosaccharides (g)
0.871.77
Citric acid cycle intermediates (g)
2.482.90
Protein (g)
0.40.5
6.65 6 0.14
Lipids (g)
0.20.3
0.98 6 0.07
Ash (g)
0.20.3
3.67 6 0.21 19.23 6 0.00
Fiber (g)
0.10.6
Total sugars (%)
1.281.48
Starch (%)
0.340.44
Total pectin (%)
47.00 6 0.00
0.110.21
Total soluble solids ( Brix)
5.56.8
Total titrable acidity (%)
2.632.86
pH
2.512.54
Energy (cal)
1720.9
2.61 6 0.02
Essential Aminoacids Phenylalanine (mg)
2243
128
Threonine (mg)
2836
124
Valine (mg)
16.831.6
176
Leucine (mg)
13.228.9
219
Isoleucine (mg)
124
Lysine (mg)
196
Histidine (mg)
110
Methionine (mg)
58 a
Essential Fatty Acids
C18:3ω6 (α-Linolenic acid)
16
C18:2ω6 (Linoleic acid)
9.7
Vitamins Vitamin C (g)
0.962.99
Niacin (μg)
62
Riboflavin (μg)
40
Thiamine (μg)
10
Vitamin A value (RE/100 g)
14.224.5
Vitamin B12 (μg)
20.31 6 0.04
0.34
Minerals K (mg)
60144.1
PO4 (mg)
25.629.5
SO4 (mg)
13.216.3
796.99 6 43.94
(Continued )
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TABLE 1 (Continued) Components
Contents in pulp Fresh
Freeze-dried
Ca (mg)
6.215.7
22.12 6 2.54
Mg (mg)
4.712.4
33.47 6 1.30
Cl (mg)
6.611.6
Na (mg)
2.711.1
Co (mg)
0.62.4
Cu (μg)
200800
0.84 6 0.03
Fe (μg)
180665
2.23 6 0.12
Zn (μg)
120472
1.26 6 0.07
Al (μg)
210300
Mn (μg)
140211
B (μg)
50
Br (μg)
1726.8
Cr (μg)
8.819.9
Mo (μg)
2.36.2
Se (μg)
0.330.52
1.29 6 0.08
a
Percentage in total lipids.
TABLE 2 Extracts and Bioactive Phytochemicals of Camu-Camu and Its Demonstrate Health-Promoting Properties Components
Part of plant
Health-promoting properties
Reference
Methanolic, freeze dried
Seed, pulp, peel
Antimicrobial, antidiabetic
Myoda et al. (2010), Fujita et al. (2013)
Aqueous and ethanolic
Pulp, peel, cortex
Antiplasmodial
Ruiz et al. (2011), Gutierrez et al. (2008)
Aqueous
Fruit juice, pulp
Antioxidant, antiinflammatory, antigenotoxic, antiobesity
da Silva et al. (2012), Nascimento et al. (2013), Inoue et al. (2008)
Aqueous and acetonic
Seed, peel
Neuroprotective
Azeveˆdo et al. (2015)
Extracts
Bioactive Phytochemical Polyphenols
Pulp, peel
Antioxidant, antidiabetic, antimicrobial, cellular regeneration
Fracassetti et al. (2013), Fujita et al. (2013)
Carotenoids
Peel
Antioxidant
Zanatta and Mercadante (2007)
Ellagic acid and derivatives
Leaves
Aldose reductase inhibitor
Ueda et al. (2004)
1-methylmalate
Fruit juice
Hepatoprotective
Akachi et al. (2010)
C-glycosidic ellagitannins
Peel, seed
Antioxidant
Kaneshima et al. (2016)
Betulinic acid
Seed
Antiinflammatory
Yazawa et al. (2011)
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FCR3 of Plasmodium falciparum with IC50 of 6 and 3 μg/mL, respectively (Gutierrez et al., 2008). Finally, Japanese research groups showed that the leaves contain aldose reductase inhibitors (Ueda et al., 2004), and the extract of camucamu juice residue (seeds and peel) exhibit antimicrobial activity against Staphylococcus aureus (Myoda et al., 2010).
SENSORY CHARACTERISTICS The high content of L-ascorbic acid and phenolic acid compounds makes the fruit very sour, affecting their palatability and making direct consumption of fruits nearly impossible. According to several researchers, the palatability index (total soluble solids: titratable acidity ratio) of camu-camu fruit is extremely low, ranging from 1.60 to 2.75. For comparison, the desired ratio is between 12 and 24 in plums and above 16 in apples (Vangdal, 1985). This ratio is an important qualitative attribute, because it indicates the relative contributions of the compounds responsible for sweetness and acidity, and therefore provides an indication of the fruit flavor (Prasanna et al., 2007). Despite the abundant information on the health benefits of the fruits, the juice has high sensory rejection (Vidigal et al., 2011). Due to its high L-ascorbic acid content, however, the pulp and juice are used to provide nutritional enrichment in soft drinks, juices, jams, icecream, concentrates, nectars, isotonic beverages, and yogurt (Rodrigues et al., 2001; Rodrigues et al., 2004). These preparations, particularly yogurt drinks, have high sensory acceptability, providing the population with a more nutritious and functional food option (Rodrigues and Marx, 2006; Aguiar and do Amaral, 2015).
HARVEST AND POSTHARVEST CONSERVATION In the nonfloodable regions, harvesting is carried out manually, once or twice per week, according to the stage of production (Rodrigues et al., 2001). In natural populations, harvesting is also carried out manually, but canoes are used to move easily during the harvesting process, because at harvest time plants are submerged and it is possible to harvest only those that are above the water surface (Villachica, 1996; Alves et al., 2002). As the camu-camu fruits are nonclimacteric (Neves et al., 2015; Gonza´les et al., 2013), they are harvested in the three stages of ripening (i.e., greenunripe, half-ripe, and full-ripe fruit) approximately 70100 days after anthesis (Peters and Vasquez, 1987; Ima´n et al., 2011). The fruits are marketed in the three stages of maturation alone or in combination, but ripe fruits in good condition usually have greater demand and higher costs. The green-unripe fruits, at their maximum size, are also harvested to be used for vitamin C obtention (Rodrigues et al., 2001). A significant proportion of fruits, however, are lost by several factors before they can be sold. For example, the mechanical damage during harvest and the increase in metabolic activity by unsuitable conditions during transport and storage. In conjunction, these factors influence the shortening of the shelf life of fruits. In addition, production areas are remote from the consumption cities and commonly the only means of transport is fluvial. Consequently, during the past 15 years some technological approaches have been evaluated and developed to reduce costs associated with packaging, storage, and transportation. Currently, there are five postharvest conservation approaches that focus on the dehydration processes of juice and fruit pulp for camu-camu: (1) hot air drying (Dib et al., 2003; da Silva et al., 2005; Fracassetti et al., 2013), (2) spouted bed drying (Fujita et al., 2013), (3) reverse osmosis (Rodrigues et al., 2004), (4) osmotic evaporation (Souza et al., 2013), and (5) freeze drying (Fujita et al., 2013; Silva et al., 2006; da Silva et al., 2006). However, these dehydration technological approaches differ significantly in the quality and quantity of the bioactive compounds present in the dehydrated material. For example, the hot air drying and spouted bed drying show a decrease from 45% to 64% of vitamin C. In contrast, reverse osmosis (7.6%18.4% losses of vitamin C) and osmotic evaporation (2.1%4.4% losses of vitamin C) processes can concentrate camu-camu juice up to about 4-fold without damaging the nutritional potential of the raw material (Rodrigues et al., 2004). Also, the concentration of camu-camu juice by the coupling of reverse osmosis and osmotic evaporation processes proved to be an interesting alternative to the concentration of thermosensitive juices, reaching concentration levels up to 7 times for camu-camu juice’s bioactive compounds (Souza et al., 2013). On the other hand, freeze drying is the best approach for bioactive compounds preservation in fruit pulp of camu-camu (Fujita et al., 2013). Its impact is minimal because the samples remain at a temperature below the freezing point during the process of sublimation, which tends to better preserve food quality. However, the expensive equipment, high energy costs, and long drying times are disadvantages which limits the application of these techniques (Ratti, 2001).
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POTENTIAL INDUSTRIAL APPLICATION Frozen fruit pulp is being exported to Japan, Asia, Europe, and the United States, where it is utilized as the main added value product for pharmaceutical and cosmetics industry, as well as for the food industry. In the food industry it is commonly used for mixed drinks to increase the vitamin C content. In Latin American countries, camu-camu is used at a small scale in the food, cosmetic, and pharmaceutical industry. In the first, the pulp is used to produce mainly juice, nectar, jam, icecream, candy, yogurt, cereal bars, and alcoholic drinks (Aguiar and do Amaral, 2015; Ayala-Zavala et al., 2011; Bustamante et al., 2000; Maeda and Andrade, 2003; Peuckert et al., 2010). In the cosmetic industry, it is used in shampoo (Bustamante et al., 2000), and a pilot study showed promise as a sunscreen in lotion and gel (Inocente-Camones et al., 2014). Finally, frequently after freeze-drying of the pulp, it is used to produce tablets and capsules as a source of natural vitamin C. Also, it is used for the elaboration of nutraceutical concentrates mixed with other fruits, honey from bees, or resinous substances such as copaiba and propolis (Santa Natura-Productos Naturales, 2016). To support the growing demand for industrial use of camu-camu, however, it is important to increase cultivation areas, because demand currently outweighs supply.
ACKNOWLEDGMENTS We thank Dr. Jorge L. Marapara for his help with the infrastructure and equipment of Unidad Especializada de Biotecnologı´a and Instituto Nacional de Innovacio´n Agraria (INIA) San Roque-Iquitos for access to the germplasm collection of Myrciaria dubia.
REFERENCES Aguiar, J.P., do Amaral, F., 2015. Camu-camu (Myrciaria dubia HBK): yogurt processing, formulation, and sensory assessment. Am. J. Anal. Chem. 6 (5), 377381. Akachi, T., Shiina, Y., Kawaguchi, T., Kawagishi, H., Morita, T., Sugiyama, K., 2010. 1-methylmalate from camu-camu (Myrciaria dubia) suppressed D-galactosamine-induced liver injury in rats. Biosci. Biotechnol. Biochem. 74 (3), 573578. Alves, R., Filgueiras, H., Moura, C., Araujo, N., Almeida, A., 2002. Camu camu (Myrciaria dubia Mc Vaugh): a rich natural source of vitamin C. Proc. Interamer. Soc. Trop. Hortic. 46, 1113. Ayala-Zavala, J.F., Vega-Vega, V., Rosas-Domı´nguez, C., Palafox-Carlos, H., Villa-Rodriguez, J.A., Siddiqui, M.W., et al., 2011. Agro-industrial potential of exotic fruit byproducts as a source of food additives. Food Res. Int. 44 (7), 18661874. Azeveˆdo, J.C., Borges, K.C., Genovese, M.I., Correia, R.T.P., Vattem, D.A., 2015. Neuroprotective effects of dried camu-camu (Myrciaria dubia HBK McVaugh) residue in C. elegans. Food Res. Int. 73, 135141. Bardales, X.I., Carrillo, M.P., Herna´ndez, M.S., Barrera, J.A., Ferna´ndez-Trujillo, J.P., Martı´nez, O., 2008. Camu-camu fruit (Myrciaria dubia) a new option for productive systems in Colombian Amazonian Region. Acta Hortic. (773), 173178. Bustamante, F., Flores, F., Metz, F., Moreno, A., 2000. Estudio de Mercado para Myrciaria dubia H.B.K. McVaugh (camu camu). Instituto Latino Alema´n de la Tecnologı´a del AprendizajeILATA. Castro, J.C., Maddox, J.D., Cobos, M., Requena, D., Zimic, M., Ima´n, S., et al., 2015. De novo assembly and functional annotation of Myrciaria dubia fruit transcriptome reveals multiple metabolic pathways for L-ascorbic acid biosynthesis. BMC Genomics. 16, 997. Castro, J.C., Cobos, M., Maddox, J.D., Ima´n, S.A., Egoavil, A., Torres, J., et al., 2015. Gene expression and enzyme activities of the D-mannose/ L-galactose pathway influence L-ascorbic acid content in Myrciaria dubia. Biol. Plant. 15, 15. Chirinos, R., Galarza, J., Betalleluz-Pallardel, I., Pedreschi, R., Campos, D., 2010. Antioxidant compounds and antioxidant capacity of Peruvian camu camu (Myrciaria dubia (H.B.K.) McVaugh) fruit at different maturity stages. Food Chem. 120 (4), 10191024. da Silva, F.C., Arruda, A., Ledel, A., Dauth, C., Roma˜o, N.F., Viana, R.N., et al., 2012. Antigenotoxic effect of acute, subacute and chronic treatments with Amazonian camucamu (Myrciaria dubia) juice on mice blood cells. Food Chem. Toxicol. 50 (7), 22752281. da Silva, M.A., Pinedo, R.A., Kieckbusch, T.G., 2005. Ascorbic acid thermal degradation during hot air drying of Camu-Camu (Myrciaria dubia [H.B.K.] McVaugh) slices at different air temperatures. Dry Technol. 23 (911), 22772287. da Silva, M.A., Sobral, P.J., Kieckbusch, T.G., 2006. Water sorption and glass transition of freeze-dried camu-camu (Myrciaria dubia (H.B.K.) McVaugh) pulp. J. Therm. Anal. Calorim. 84 (2), 435439. Defilippi, E., 2011. La cadena de valor del camu camu en la regio´n Loreto. Ana´lisis y lineamientos estrate´gicos para su desarrollo. Primera edicio´n. Proyecto Peru´biodiverso-PBD, Lima, Peru´, 70 p. Dib, C.M., de Menezes, H.C., Santos, A.B., Grosso, C.R., 2003. Study of the microencapsulation of camu-camu (Myrciaria dubia) juice. J. Microencapsul. 20 (4), 443448. Direccio´n Regional Agraria Loreto, 2010. Informe de estimado de produccio´n mensual del cultivo de camu camu para el an˜o 2011. Gobierno Regional de Loreto, Iquitos-Peru´, 50 p. Fracassetti, D., Costa, C., Moulay, L., Toma´s-Barbera´n, F.A., 2013. Ellagic acid derivatives, ellagitannins, proanthocyanidins and other phenolics, vitamin C and antioxidant capacity of two powder products from camu-camu fruit (Myrciaria dubia). Food Chem. 139 (14), 578588.
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Fujita, A., Borges, K., Correia, R., Franco, B.D., Genovese, M.I., 2013. Impact of spouted bed drying on bioactive compounds, antimicrobial and antioxidant activities of commercial frozen pulp of camu-camu (Myrciaria dubia McVaugh). Food Res. Int. 54 (1), 495500. Gonza´les, L., Aylas, B., Paima, K., Baza´n, A., 2013. Determinacio´n de la tasa respiratoria de Eugenia stipitata Mc Vaugh (araza´) y Myrcyaria dubia HBK (camu-camu). Cienc Amaz. 3 (1), 5358. Gutierrez, D., Sangama, D., Rengifo, E., Gimenez, A., 2008. Evaluation of the in vitro antiplasmodic activity of extracts from Euterpe oleracea, Myrciaria dubia and Croton lechleri. Biofarbo. 16, 1620. Ima´n, S., Bravo, L., Sotero, V., Oliva, C., 2011. Contenido de vitamina C en frutos de camu camu Myrciaria dubia (H.B.K) Mc Vaugh, en cuatro estados de maduracio´n, procedentes de la Coleccio´n de Germoplasma del INIA Loreto, Peru´. Sci. Agropecu. 2 (3), 123130. Ima´n, S.A., Pinedo, S., Melchor, M., 2011. Caracterizacio´n morfolo´gica y evaluacio´n de la coleccio´n nacional de germoplasma de camu camu Myrciaria dubia (H.B.K) McVaugh, del INIA Loreto-Peru´. Sci. Agropecu. 2, 189201. ´ ., Tomas-Chota, G.E., Huama´n-Malla, J., Mun˜oz-Ja´uregui, A.M., Garcı´a-Mora´n, R.I., Quispe-Fuentes, G., et al., 2014. Inocente-Camones, M.A Antioxidant activity and photoprotective in vitro of lotion and gel processed with extract stabilized of camu camu (Myrciaria dubia Kunth.). Rev. Soc. Quı´m. Peru´. 80 (1), 6577. Inoue, T., Komoda, H., Uchida, T., Node, K., 2008. Tropical fruit camu-camu (Myrciaria dubia) has anti-oxidative and anti-inflammatory properties. J. Cardiol. 52 (2), 127132. Kaneshima, T., Myoda, T., Nakata, M., Fujimori, T., Toeda, K., Nishizawa, M., 2016. Antioxidant activity of C-Glycosidic ellagitannins from the seeds and peel of camu-camu (Myrciaria dubia). LWT - Food Sci. Technol. 69, 7681. Landrum, L.R., Kawasaki, M.L., 1997. The genera of Myrtaceae in Brazil: an illustrated synoptic treatment and identification keys. Brittonia. 49 (4), 508536. Lim, T.K., 2012. Myrciaria dubia. Edible Medicinal And Non Medicinal Plants. Springer, Netherlands. Maeda, R.N., Andrade, J.S., 2003. Aproveitamento do camu-camu (Myrciaria dubia) para produc¸a˜o de bebida alcoo´lica fermentada. Acta Amaz. 33 (3), 489498. Medina, A., Cordova, E., Fasabi, J., Rodriguez, H., Ima´n, S.A., Castro, J.C., 2014. Semillas y pla´ntulas de Myrciaria dubia “camu-camu”: biometrı´a, germinacio´n y crecimiento inicial. Sci. Agropecu. 5 (2), 8592. Myoda, T., Fujimura, S., Park, B., Nagashima, T., Nakagawa, J., Nishizawa, M., 2010. Antioxidative and antimicrobial potential of residues of camu-camu juice production. J. Food Agric. Environ. 8 (2), 304307. Nascimento, O.V., Boleti, A.P.A., Yuyama, L.K.O., Lima, E.S., 2013. Effects of diet supplementation with Camu-camu (Myrciaria dubia HBK McVaugh) fruit in a rat model of diet-induced obesity. An. Acad. Bras. Cieˆnc. 85 (1), 355363. Neves, L.C., da Silva, V.X., Chagas, E.A., Lima, C.G.B., Roberto, S., 2015. Determining the harvest time of camu-camu [Myrciaria dubia (H.B.K.) McVaugh] using measured pre-harvest attributes. Sci. Hortic. 186, 1523. Penn, J.W., 2006. The cultivation of camu camu (Myrciaria dubia): a tree planting programme in the Peruvian Amazon. For Trees Livelihoods. 16 (1), 85101. Peters, C.M., Vasquez, A., 1987. Estudios ecolo´gicos de Camu-Camu (Myrciaria dubia). I. Produccio´n de frutos en poblaciones naturales. Acta Amaz. 17, 161173. Peuckert, Y.P., Viera, V.B., Hecktheuer, L.H., Marques, C.T., Rosa, C.S., 2010. Caracterizac¸a˜o e aceitabilidade de barras de cereais adicionadas de proteı´na texturizada de soja e camu-camu (Myrciaria dubia). Aliment E Nutr Araraquara. 21 (1), 149154. Prasanna, V., Prabha, T.N., Tharanathan, R.N., 2007. Fruit ripening phenomenaan overview. Crit. Rev. Food Sci. Nutr. 47 (1), 119. Ratti, C., 2001. Hot air and freeze-drying of high-value foods: a review. J. Food Eng. 49 (4), 311319. Rengifo, E., 2009. Monografı´a: camu camu - Myrciaria dubia (H.B.K) Mc Vaugh. Perubiodiverso. 29 p. Rodrigues, R.B., Marx, F., 2006. Camu Camu [Myrciaria dubia (H.B.K.) Mc Vaugh]: a promising fruit from the Amazon Basin. Erna¨hrung/Nutrition. 30 (9), 376381. Rodrigues, R.B., De Menezes, H.C., Cabral, L.M., Dornier, M., Reynes, M., 2001. An Amazonian fruit with a high potential as a natural source of vitamin C: the camu-camu (Myrciaria dubia). Fruits. 56 (5), 345354. Rodrigues, R.B., Menezes, H.C., Cabral, L.M., Dornier, M., Rios, G.M., Reynes, M., 2004. Evaluation of reverse osmosis and osmotic evaporation to concentrate camucamu juice (Myrciaria dubia). J. Food Eng. 63 (1), 97102. Ruiz, L., Ruiz, L., Maco, M., Cobos, M., Gutierrez-Choquevilca, A.L., Roumy, V., 2011. Plants used by native Amazonian groups from the Nanay River (Peru) for the treatment of malaria. J. Ethnopharmacol. 133 (2), 917921. Santa Natura-Productos Naturales. Homepage. Available from: ,http://www.santanatura.com.pe/#1.. Silva, M.A., Sobral, P.J., Kieckbusch, T.G., 2006. State diagrams of freeze-dried camu-camu (Myrciaria dubia (HBK) McVaugh) pulp with and without maltodextrin addition. J. Food Eng. 77 (3), 426432. Souza, A.L., Pagani, M.M., Dornier, M., Gomes, F.S., Tonon, R.V., Cabral, L.M., 2013. Concentration of camucamu juice by the coupling of reverse osmosis and osmotic evaporation processes. J. Food Eng. 119 (1), 712. Uchiyama, H., Koyama, T., Yoneda, K., 1996. Seed morphology and germination of camu camu Myrciaria dubia (Myrtaceae). Bull. Coll. Agric. Vet. Med-Nihon Univ. 53, 9295. Ueda, H., Kuroiwa, E., Tachibana, Y., Kawanishi, K., Ayala, F., Moriyasu, M., 2004. Aldose reductase inhibitors from the leaves of Myrciaria dubia (H. B. & K.) McVaugh. Phytomed. Int. J. Phytother. Phytopharm. 11 (78), 652656. Vangdal, E., 1985. Quality Criteria for fruit for fresh consumption. Acta Agric. 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Canistel—Pouteria campechiana (Kunth) Baehni Fadzilah Awang-Kanak1,2 and Mohd Fadzelly Abu Bakar1 1
Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia, 2Universiti Malaysia Sabah, Sabah, Malaysia
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Values
107 108 108 108 109
Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgment References
109 110 110 111 111
CULTIVAR ORIGIN AND BOTANICAL ASPECTS Kingdom Order Family Genus Species Vernacular names Distribution
Ecology
Plantae Ebenales Sapotaceae Pouteria Pouteria campechiana Canistel, egg fruit, yellow sapote (English), Zapote, mamey, sapota, amarillo (Spanish), Lawalu, lavulu (Sri Lankan), Buah kuning telur, buah mentega, sawo mentega (Malay), Zaituni (East African). Central America; Bahamas, Belize, El Salvador, Guatemala, Southern Mexico (native). Nicaragua, Costa Rica, Panama, Puerto Rico, Jamaica, and Cuba, Africa: North America; Florida, South America; Africa; Kenya, Tanzania, Uganda, Middle East; Egypt, South Asia; India, Sri Lanka, South East Asia; Cambodia, Indonesia, Malaysia, Thailand, and Philippine (cultivar). Tropical to subtropical climate, heavy clay to sandy limestone soils, altitude; sea level to 1400 m elevation.
Pouteria campechiana or canistel (Fig. 1) is a tropical fruit and a member of Sapotaceae family. This fruit is a native plant to Central America region, namely the Bahamas, Belize, El Salvador, Guatemala, and Southern Mexico. The distribution is well spread around the region including Nicaragua, Costa Rica, Panama, Puerto Rico, Jamaica, and Cuba. Previously the spread was as far south as to reach Brazil. In the United States, this fruit was introduced in Florida. It is also planted in East Africa countries such as Kenya, Tanzania, and Uganda, Egypt, in the Middle East, South Asian countries such as Sri Lanka and India, and also introduced into the Philippines, and later in most countries in South East Asia region; Thailand, Cambodia, Vietnam, Malaysia, Indonesia. The introduction of this fruit reached further east to Taiwan and further south to Australia (De Lanerolle et al., 2008; Orwa et al., 2009; Silva et al., 2009; Lim, 2012; Elsayed et al., 2016). Ecologically, canistel needs a tropical or subtropical climate to grow, however, it is found to survive in the colder climate of north Florida, and in California region. The tree in this latter locality was unable to successfully produce fruit. This tree can grow at sea level altitude and in Guatemala, this tree is found at 1400 m elevations. It needs a moderate precipitation, and able to tolerate well a long hot dry season such as that seen in the South Asia region (Orwa et al., 2009; Lim, 2012). Canistel has high tolerance in various soil types, the soil types needed for canistel growth ranged from acidic sandy of Guatemala, heavy clay of Puerto Rico, and limestone sand of Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00015-0 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 (A) Canistel fruit and (B) cross sectional canistel fruit.
Florida (Almeyda and Martin, 1976). The most suitable type of soils to grow fertile canistel is a well-drained soils and shallow soils (Orwa et al., 2009; Lim, 2012). Distribution and cultivation of this fruit is widespread to many countries, and often sold in the markets, thus the common names of this fruit are assigned based on the yellowish to yellow colored flesh, the shape, and also the taste and texture of the aril. In English this fruit is known as yellow sapote, egg fruit, and canistel. In Spanish speaking Central and South American countries, this fruit is known as zapote, mamey, sapota, amarillo, fruta de huevo, custiczapoti, ti-es and cucuma. In Malaysia and Indonesia this fruit is often treated as type of mango, it is called buah kuning telur (egg yolk fruit), kanistel, mangga susu or buah susu or buah mentega or sawo mentega, due to the texture of the ripen pulp is buttery and the milky taste. The Filipino population named it chesa or toesa or boracho. In Sri Lanka, it is known as laulu, lavulu, or lawalu. On the other hand in Thailand it is more treated as a type of peach, or locals call it Khmer Peach or lamut or lamut khamen, with a sense that this fruit originated from Cambodia. Eastern African regions called this fruit as zaituni, referring to olive in Arabic and Swahili language. This is rather rare, as olive is a berry, but the canistel is a drupe with single seed, wrapped inside fleshy aril or pulp (Pushpakumara, 2007; Orwa et al., 2009; Lim, 2012; Kong et al., 2013; Atapattu and Mendis, 2013). The canistel is a monopodial tree that stands tall, between 8 and 30 m from the ground. The trunk is slender in physique with diameter up to 1 m, furrowed bark, and like any other member of Sapotaceae family, the trunk contains rubbery white latex. It has a spreading crown, with velvet brown young branches, alternate evergreen leaves, leaves are ranged from oblonglanceolate to obovate with blunt apex with size of 11.2528 cm long and 47.5 cm wide. Flowers are bisexual, fragrant, solitary or in small clusters, 56 lobed, cream colored, and with silky hairs (Morton, 1987).
HARVEST SEASON Canistel is often cultivated in home gardens in Sri Lanka, India, Malaysia, and the Philippines as a fruit tree. The mature period for this fruit varies from one locality to the another; in Sri Lanka the fruiting season is from September to February, meanwhile in Mexico, the blooming period is from June to February, and in Cuba the flowering starts in April and May and main fruiting season is from October and February (Morton, 1987; Pushpakumara, 2007; Orwa et al., 2009). Harvesting season in Puerto Rico begins in September to early November (Almeyda and Martin, 1976). However, some trees in Sri Lanka are able to produce fruit throughout the year (Pushpakumara, 2007; Atapattu and Mendis, 2013).
ESTIMATED ANNUAL PRODUCTION A tree can produce fruits up to 136250 kg/year and the weight of a fruit is about 175 g (Atapattu et al., 2014).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The fruit is variable in shape with uneven bulged, from round to egg shaped, nearly round, oval, ovoid or spindle shaped. Length varies from 7 to 12.5 cm, and width from 5 to 7.5 cm. Young fruit has green skin, leathery textured peel, and contains latex. The flesh of young fruit is hard to gummy with a bitter and sour taste. Ripen or matured fruit has yellowish to yellow colored skin, soften texture peel, and the aril of matured fruit is soft with few fine fibers and creamy, with a sweet taste. Freestone seeds range in size from 5 to 7.5 cm long (Morton 1987; Orwa et al., 2009;
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TABLE 1 Physical Properties of Pouteria campechiana Fruit Sample
Weight (g)
Length (cm)
Width (cm)
Circumferences (cm)
Pulp thickness (cm)
Fruit Fruit part Seeds Pulp Peel
118.09 6 35.48 Weight (g) 19.77 6 7.32 90.83 6 27.47 7.16 6 0.83
7.43 6 0.21 Portion (%) 16.50 6 1.50 77.11 6 0.12 6.39 6 1.59
5.40 6 0.62 Moisture (%) 50.17 6 4.70 46.41 6 1.64 48.28 6 3.04
17.90 6 2.44
1.10 6 0.10
Data are presented as mean standard (n 5 3). Source: Adopted from Kong, K.W., Khoo, H.E., Prasad, N.K., Chew, L.Y., Amin, I., 2013. Total phenolics and antioxidant activities of Pouteria campechiana fruit parts. Sains Malays. 42 (2), 123127.
Elsayed et al., 2016). Fruit pulp thickness makes up 77.11% of total fruit weight. Seeds and peel made approximately 16.5% and 6.39% of total fruit weight. It has the highest moisture recorded for seeds, containing 50.17% of moisture. Meanwhile pulp and peel composed 46.1% and 48.8% of moisture, respectively. All these physical properties of P. campechiana fruit is shown in Table 1. Seventy percent of the fruit weight is edible (Orwa et al., 2009).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUES The chemical composition of P. campechiana has been investigated in terms of selected phytochemical components. Franco (2006), Hernandez et al. (2008), and Silva et al. (2009) reported the fruit juice contains antioxidant, antinitrosative, and antimitotic qualities. Leaves of P. campechiana were found to content six stilbenes and six flavonoid glycosides, these compounds were identified having antimitotic activity (Hernandez et al., 2008). Meanwhile the fruit of P. campechiana is an essential source of plant carotenoids, total carotenoid content in fruit was varied from 1.9 to 23.5 mg/g dry weight (DW) (De Lanerolle et al., 2008; Costa et al., 2010). Furthermore, Kong et al. (2013) reported that 70% ethanol extract of the fruit parts are great source of plant phenolics and flavonoid, with total phenolic content (TPC) content at the highest for peel (2304.7 mg GAE/100 g), and total flavonoid content (TFC) at the highest for pulp (6414 mg RE/100 g). On the other hand, TPC for pulp is 2257.8 mg GAE/100 g and for seeds is 2304.7 mg GAE/100 g. TFC values were recorded at 6180.6 and 4242.3 mg RE/100 g for peel and seed, respectively (Kong et al., 2013). Findings by Kong et al. (2013) were inconsistent with Ma et al. (2004), as the latter reported that P. campechiana had the lowest levels of phenolics compared to the other two species of Pouteria they had studied. This inconsistency could be the result of growing environment, season, soil, rain fall, and fertilizer used (Manach et al. 2004). Elsayed et al. (2016) supported the use of P. campechiana in traditional medicine for conditions related to inflammation, pain, and peptic ulcers. They found ethanolic extract of the canistel seeds had arresting effect on inflammation, and ethanolic extract of the leaves showed analgesic activity. This reasonably justified the used of P. campechiana seeds employed as traditional fever and ulcer remedies in Mexico and Cuba, and also as painkiller for headache and antiseptic for wound during SpanishAmerican war (Orwa et al., 2009; Lim, 2012). Canistel is a fruit loaded with carbohydrates, vitamin C, vitamin B, and minerals, such as calcium, phosphorus, and iron. Food value for canistel per 100 g of edible portion was reported as follows (Table 2); calories 138.8 mg, moisture 60.6 g, protein 1.68 g, fat 0.13 g, carbohydrates 36.69 g, fiber 0.10 g, ash 0.90 g, calcium 26.5 mg, phosphorus 37.3 mg, iron 0.92 mg, carotene 0.32 mg, thiamine 0.17 mg, riboflavin 0.01 mg, niacin 3.72 mg, ascorbic acid 58.1 mg, tryptophan 28 mg, methionine 13 mg, and lysine 84 mg (Morton, 1987). Neoxanthin was found as the most abundant carotenoid in the canistel, and the total carotenoids content varied from 1.9 to 23.5 mg/g DW (Table 3) (De Lanerolle et al., 2008).
SENSORY CHARACTERISTICS The young fruit of canistel has greenish mesocarp with sticky latex, and often has a bittersour taste. The ripened fruit mesocarp turns from yellowish to creamy yellow color. Matured canistel is often eaten fresh as a dessert fruit, and its fleshy pulp has a buttery or creamy texture, sweet and milky taste. The consistency of ripened canistel pulp quality is similar to a hard boiled yolk (De Lanerolle et al., 2008; Lim, 2012; Atapattu et al., 2014).
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TABLE 2 Food Value for per 100 g of Edible Portion of Pouteria campechiana (Morton, 1987) Nutrition
Value in weight
Calories Moisture Protein Fat Carbohydrates Fiber Ash Calcium Phosphorus Iron Carotene Thiamine Riboflavin Niacin Ascorbic acid
138.8 mg 60.6 g 1.68 g 0.13 g 36.69 g 0.10 g 0.90 g 26.5 mg 37.3 mg 0.92 mg 0.32 mg 0.17 mg 0.01 mg 3.72 mg 58.1 mg
Amino Acids Tryptophan Methionine Lysine
28 mg 13 mg 84 mg
TABLE 3 Carotenoid Content and Retinol Equivalent (RE) of Pouteria campechiana Carotenoids
(μg/g DW)
β-Carotene β-Cryptoxanthin Violaxanthin Neoxanthin Unidentified I Unidentified II RE/100 g DW
156 1106 1151 19,720 628 1162 11,813
Source: Extracted from De Lanerolle, M., Priyadarshani, A.M. Sumithraarachchi, D.B., Jansz, E.R., 2008. The carotenoids of Pouteria campechiana (Sinhala: ratalawulu). J. Natl. Sci. Found. Sri Lanka. 36 (1), 9598.
HARVEST AND POSTHARVEST CONSERVATION It is rather subjective to determine when the canistel fruit is sufficiently ripened, the harvest shall begin when the fruit shows some reddish color. Effort should be made to ensure the quality of the product and avoiding the lopsided ripening that could affect storage life of the fruit. One suggested harvesting technique is to use a ladder to climb up the tree and pre-ripened fruits should be clipped to avoid damage (Almeyda and Martin, 1976; Morton, 1987). The sustainable practice would be to harvest a sample of 1012 fruits from tree, and judge the maturity of the fruits by removing the peel and evaluating the pulp. If it has reached satisfactory color, soft texture, and sweet taste, the entire crop is ready to be yielded. If the fruits are left to ripen on the tree, the fruits can tear at the stem and fall on the ground (Morton, 1987). Fruits are only harvested from matured tree not from vegetative growing tree (Almeyda and Martin, 1976).
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Canistel is often eaten fresh as a dessert fruit, and also as fruit salad with condiments such as salt, pepper, lime juice, or mayonnaise. The pureed of canistel can be added to cake or icecream as flavor and used as filling for pie. This fruit is
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also used in drinks, fresh pressed juice, milkshake, or eggnog. The blended drink is enriched with milk and sugar, flavored with vanilla, nutmeg, and spices. The pulp can be dried, make into powder, and use in pudding mixes (Lim, 2012). The ripened pulp can be mashed, flavored with sugar, heated, and prepared as butter or a spread (Morton, 1987). Additional to the use of the fruit, the latex of canistel tree has been used as material in production of traditional chewing gum in central America (Lim, 2012). In Sri Lanka, canistel fruit meal is used as a poultry feed to enhance growth performance and carcass parameters in broiler chickens (Atapattu et al., 2014). The grown tree has been used as a shed for coffee plant, for shelter and it can be exploited as timber and wood plank as building material for house frames, cart, or furniture (Almeyda and Martin 1976; Orwa et al., 2009; Lim, 2012). The bark of the tree can be simmered and the mixture has been used as antipyretic medication to lessen fever in Mexico, and in Cuba it has been used to treat skin blisters or soreness (Orwa et al., 2009).
ACKNOWLEDGMENT Authors would like to thank funding grant FRGS (Vot No. 1560) from Ministry of Higher Education, Malaysia and Universiti Tun Hussein Onn Malaysia.
REFERENCES Almeyda, N., Martin, F.W., 1976. Cultivation of neglected tropical fruit with promise. Part 2. Mamey zapote. USDA, ARS Tech. Bull. (156), 113. Atapattu, N.S.B.M., Mendis, A.P.S., 2013. Evaluation of Canistel (Pouteria campechiana) fruit meal as feed ingredient for poultry. Iran. J. Appl. Anim. Sci. 3 (1), 177183. Atapattu, N.S.B.M., Sanjeewani, K.G.S., Senaratna, D., 2014. Effects of dietary canistel (Pouteria campechiana) fruit meal on growth performance and carcass parameters of broiler chicken. Trop. Agric. Res. Ext. 16 (2), 2014. Costa, D.S.A., Wondracek, D.C., Lopes, R.M., Vieira, R.F., Ferreira, F.R., 2010. Carotenoids composition of canistel (Pouteria campechiana (Kunth) Baehni). Rev. Bras. Frutic. 32 (3), 903906. De Lanerolle, M., Priyadarshani, A.M., Sumithraarachchi, D.B., Jansz, E.R., 2008. The carotenoids of Pouteria campechiana (Sinhala: ratalawulu). J. Natl. Sci. Found. Sri Lanka. 36 (1), 9598. Elsayed, A.M., El-Tanbouly, N.D., Moustafa, S.F., Abdou, R.M., El Awdan, S.A.W., 2016. Chemical composition and biological activities of Pouteria campechiana (Kunth) Baehni. J. Med. Plants Res. 10 (16), 209215. Franco, E.M., 2006. Actividad antioxidante in vitro de las bebidasde frutas. Bebidas-Alfa Editores Te´cnicos. Junio/Julio, 2027. Hernandez, C., Villasen˜or, I., Joseph, E., Tolliday, N., 2008. Isolation and evaluation of antimitotic activity of phenolic compounds from Pouteria campechiana Baehni. Philip J. Sci. 137, 110. Kong, K.W., Khoo, H.E., Prasad, N.K., Chew, L.Y., Amin, I., 2013. Total phenolics and antioxidant activities of Pouteria campechiana fruit parts. Sains Malays. 42 (2), 123127. Lim, T.K., 2012. Edible Medicinal and Non-Medicinal Plants, 6 vols. Springer, New York, NY, USA, p. 742. Ma, J., Yang, H., Basile, M.J., Kenelly, E.J., 2004. Analysis of polyphenolic antioxidants from the fruits of three Pouteria species by selected iron monitoring liquid chromatography-mass spectrometry. J. Agric. Food Chem. 52, 58735878. Manach, C., Scalbert, A., Morand, C., Re´mse´y, C., Jime´nez, L., 2004. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79, 727747. Morton, J.F., 1987. Fruits of warm climates. Julia F. Morton, Miami, FL. Orwa, C., Mutua, A., Kindt, R., Jamnadass, R., Anthony, S., 2009. Agroforestree Database: A Tree Reference and Selection Guide Version 4.0. World Agroforestry Centre, Kenya. Pushpakumara, D.K.N.G., 2007. Chapter 16: Lavulu Pouteria campechiana Kunth Baehni. In: Pushpakumara, D.K.N.G., Gunasena, H.P.M., Sing, H.V.P. (Eds.), Underutilized Fruit Trees in Sri Lanka. World Agroforestry Centre, South Asia Office, New Delhi, pp. 426436. Silva, C.A., Simeoni, L.A., Silveira, D., 2009. Genus Pouteria: chemistry and biological activity. Rev. Bras. Farmacogn. 19 (2A), 501509.
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Caqui—Diospyros kaki Ricardo Alfredo Kluge and Magda Andre´ia Tessmer University of Sa˜o Paulo/ESALQ, Piracicaba, Sa˜o Paulo, Brazil
Chapter Outline Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value, Including Vitamins, Mineral, Phenolics, and Antioxidant Compounds
113 114 114 115
Sensory Features Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgment References
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ORIGIN AND BOTANICAL ASPECTS The persimmon tree belongs to family Ebenaceae and to genus Diospyrus. The genus holds more than 2000 species of commercial interest applied to different means such as logging (Diospyrus ebenum), landscaping (Diospyrus incostans and Diospyrus rhombifolia), tannin extraction (Diospyrus oleifera) and fruit production (Diopyros kaki)—persimmon cultivars are in this group. The naming of this species reflects its colloquial name of “Food of the Gods” (Dios 5 God, Pyros 5 food) (Nissan and Nambour, 2011; Zhuang et al., 1990). The genus Diospyros is native to Asia, mainly to China, and there are records of its cultivation centuries before Christ (Martı´nez-Calvo et al., 2012). The D. kaki species was introduced in Japan during the 7th century (Martı´nezCalvo et al., 2012) and in Korea during the 14th century (Yakushiji and Nakatsuka, 2007). It spread from Korea to other continents due to its strong adaptation to tropical and temperate regions. There are records that persimmon was brought to Europe between the 17th and 19th centuries, due to the species used for logging purposes. As for countries in the Mediterranean region, species from genus Diospyros were mixed with ornamental and fructiferous trees planted in gardens and orchards. They were planted along with citric fruits and olive trees cultivated for local consumption (Martı´nez-Calvo et al., 2012). The Diospyros virginiana species is native to North America. The species is nowadays used as rootstock for commercial persimmon cultivars. D. kaki was introduced in the United States in the mid1800s and the cultivars were adapted and expanded in the early 1900s. Next, the cultivars were also introduced in Australia and in New Zealand. As for South America, the persimmon tree was introduced in Sa˜o Paulo, Brazil, in the late 19th century. From the 1920s on, after the arrival of Japanese migrants, the production technologies and the varieties adapted to the Brazilian climate were introduced (Martins and Pereira, 1989). The persimmon tree is a deciduous species; therefore, it needs some time to rest in order to complete its annual cycle. Each cultivar demands specific hours of cold. Flowers blossom right after seedling and they may be staminate (males), pistillate (females) or monoclinous (Yakushiji and Nakatsuka, 2007). Overall, the commercial cultivars present only pollinating-crop pollinated female flowers (Fig. 1A) that form seeds or fruits by parthenocarpy. The persimmon tree fruit is a berry and its size and shape vary among cultivars. It often has a mass of between 250 and 350 g. When the flowers are pollinated, the normal fruits can hold up to eight seeds (Fig. 1B). The cultivars are classified according to their response or not to flower pollination, pulp color change, and to fruit astringency persistence. According to Sugiura (1983), Kitagawa and Glucina (1984), and Yonemori et al. (2000), the types are: pollination constant (PC), the fruits do not present pulp color change due to pollination; pollination variant (PV), the fruits present clear pulp when they are partenocarpic, and dark pulp, when they are fertilized. Both types are Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00016-2 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 (A) Female flower of ‘Giombo’ persimmon trees and (B) ripe ‘Fuyu’ persimmon fruit.
divided into astringent (A) and nonastringent (NA) according to the presence or absence of astringency in the ripe fruits (Sugiura, 1983). Thus, the persimmon tree cultivars may be classified according to the basic types: PCA (‘Taubate´’, ‘Hachiya’, ‘Pomelo’ and ‘Rubi’), PCNA (‘Fuyu’, ‘Jiro’ and ‘Hana Fuyu’) and PV, the fruits from varying pollination cultivars may be astringent (‘Aizumishirazu’, ‘Rama Forte’, ‘Giombo’ and ‘Rojo Brillante’) or nonastringent (‘Zenjimaru’, ‘Shogatsu’ and ‘Mizushima’).
HARVEST SEASON Persimmon fruits usually start growing when the trees are approximately three years old (Neuwald et al., 2009). Fruits are greenish when they start growing; chlorophyll is degraded during the ripening process; and carotenoids promote color change from yellow to orange. The harvest ripening stage is set by peel color and pulp firmness (Salvador et al., 2006). There is a specific harvest time for each cultivar and it may change depending on the climatic conditions and on local cultivation practices. Harvest takes place in the first semester of the year in southern hemisphere countries such as Brazil, New Zealand and Australia. Harvest in Brazil occurs between February and May. In European and Asian countries, it happens in the second semester, between October and December. The different harvest times among producing countries allow exportation in times when the product is not available in the market and also exportation to nonproducing countries or to countries that do not present the right conditions for this cultivar.
ESTIMATED ANNUAL PRODUCTION The global persimmon production reached 3.702.232 tons in 2007 and 5.190.324 tons in 2014 (Table 1). The harvested area increased 578.020 ha in 10 years, whereas production increased 1.488.090 ton in the same period (FAOSTAT, 2017). It confirms the economic importance of this species worldwide. The biggest persimmon producers in the world are China, Korea, Japan, Spain and Brazil. China increased 145% the production in the past 10 years (FAOSTAT, 2017). Other Asian countries (Korea, Azerbaijan, Uzbekistan, Iran and Nepal) also presented an expressive increase in their persimmon production. Brazil stands out as the fifth highest world producer. Mexico is also part of the fruit’s producers in the American continent. Although there are no FAO data available, the United States have persimmon production records in high temperature states such as Texas, Florida, and California. The production in California was estimated to be 16.000 tons in 2012 (California Ag. Commissioners, 2012). Italy is the country with the greatest persimmon cultivation tradition in the Mediterranean region. Nowadays, Spain and Slovenia started producing it for export. The persimmon production in Spain reaches up to 245.000 tons in 2014 (FAOSTAT, 2017).
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TABLE 1 Persimmon Fruit World Production in 2007 to 2014, According to Data From Food and Agriculture Organization of the United Nations (FAOSTAT, 2017) Country
Production Quantity (ton) 2007
2014
China
2.607.105
3.803.564
Korea Republic
395.614
428.363
Japan
244.800
240.600
Spain
67.000
245.000
Brazil
152.851
182.290
Azerbaijan
128.407
140.405
Italy
52.500
39.149
Israel
37.347
36.592
Uzbekistan
2.800
66.000
New Zealand
2.417
2.600
Iran
1.907
2.452
Nepal
489
1.918
Slovenia
538
801
Australia
415
715
Mexico
442
175
Total
3.702,232
5.190.324
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Persimmon tree fruits present double sigmoidal growth curve and they comprise two fast growth periods (phase I and III). These periods are separated by a slow growth period (phase II). Growth corresponds to abundant cell division in the mesocarp in the first phase; in the second phase, the cell division stops and the growth becomes stable; in the third phase, the mesocarp cells elongate and the intercellular space increases (Sugiura et al., 1991). The tannin cells are distinguishable (idioblasts) and start accumulating tannins in the vacuole (Tessmer et al., 2014; Akagi et al., 2011) when the flower bud starts developing during meristematic cell division. According to studies by Yonemori and Matsushima (1985) and Tessmer et al. (2014), the tannin cells in PCNA persimmons stop their growth process in early stages and, consequently, they are found in smaller number and size in their final development phase. Therefore, they present natural astringency reduction during the ripening process. The PCA, PVNA, and PVA types persimmon keep their tannin cells growth and high condensed tannin levels, which promote astringency even in ripe fruits. The condensed tannins (CT), also called proanthocyanidin (PA), are phenolic oligomers resulting from the polymerization of two flavan-3-ol unit types (Dixon, 2005): catechin (C) and gallocatechin (GC), and its ester-gallate, C-3O-gallate (CG) and GC-3-O-gallate (GCG) forms (Matsuo and Itoo, 1978). There is also the cis-trans form of the flavan-3-ol: 2,3-cis-epicatechin-3-O-gallate (ECG) and 2,3-cis of epigallotechin-3-O-gallate (EGCG) (Tanaka et al., 1994). Polimerization occurs due to the addition of catechin and epicatechin sequence units (polycondensation) and it forms complex nonastringent composites (Akagi et al., 2009). There are many physical and chemical changes during fruit ripening such as color changes, pulp firmness reduction, pectin degradation, changes in carbohydrate and organic acids levels, production of volatile substances, wax formation on the epidermis as well as on the condensed tannins depending whether the persimmon cultivar is astringent or nonastringent.
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Changes take place during the ripening phase due to ethylene production and respiration. Both the ethylene production (0.11.0 μL C2H4 kg21 h21 at 20 C) (Chitarra and Chitarra, 2005) and the respiratory rate (48 mg CO2 kg21 h21 at 5 C; 2024 mg CO2 kg21 h21 at 20 C) (Hardenburg et al., 1986) are considered to be low in comparison to that of other fruits. However, they are enough to trigger the climacteric ripening process. Setting the adequate harvest ripening degree is crucial for the product to reach the market in perfect conditions.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE, INCLUDING VITAMINS, MINERAL, PHENOLICS, AND ANTIOXIDANT COMPOUNDS Persimmon is an important fruit for protein, fiber, mineral, carbohydrate, carotenoid, phenolic composites, and vitamin sources (Del Bubba et al., 2009; Veberic et al., 2010). According to Baltacioglu and Artik (2013), pulp from different persimmon cultivars present 0.40%1.16% gross fiber, 80% water (on average), 0.40%0.60% protein, and 0.05% total fat, besides presenting low caloric rates (70 kcal 100 g). Regarding nutrients, persimmons have more minerals in the skin (K, Mg, Ca, Fe, Mn, Zn, and Cu) than in the pulp, with the exception of Na (Gorinstein et al., 2001). The biological activity of the mineral is remarkably strong and when incorporated into organomineral complexes, this activity is enhanced and helping to prevent diseases. Sugars in persimmon fruits are composed of 90% glucose and fructose; saccharose is found in smaller rates (Baltacioglu and Artik, 2013). The sugar content is equivalent to 12 and 22 Brix values and it shows great variation among cultivars, in the ripening stage and depending on the astringency removal method (Del Bubba et al., 2009). There are biochemical changes that take place during the ripening process as well as changes in the color of the fruits. This color change is related to chlorophyll degradation, to carotenoid pigment content increase, and to phenolic composite composition changes. β-cryptoxanthin, β-caroten, zeaxanthin, lycopene and lutein are carotenoids found in persimmon fruits (Ancos et al., 2000). These pigments are responsible for the yellow, orange and red colors in fruits and they play an important role in human health, due to pro-vitamin A and to antioxidant activities (Costa et al., 2010). Persimmon is also considered to be source of phenolic and polyphenolic composites, such as flavonoids (catechins and condensed tannins) and vitamin C (18 and 40 mg 10021 g pulp level). The main antioxidants found in persimmons are carotenoids, phenolic composites, and vitamin C; they prevent free radicals causing damage and work to prevent antimutagenic and anticarcinogenic diseases (Suzuki et al., 2005).
SENSORY FEATURES Sensory features in persimmon fruits are set by the flavor, smell, and the condensed tannins found in the fruits. Flavor is set by the balance between sugars and organic acids, mainly by the malic acid in the persimmon fruit. Another sensory feature that sets persimmon consumption is astringency, which is promoted by the soluble tannins reaction with the proteins found in the saliva. These proteins bind to flavor receptors and cause dry palate sensation (Ittah, 1993). Astringency is such an undesired feature found in varieties from PCA, PVNA, and PVA groups. Astringency removal treatments are performed after the fruits are harvested. Nowadays, the methods used to remove astringency are based on the over ripening of fruits as well as on the exposure to anaerobic respiration conditions (Pesis, 2005), such treatments using ethylene, ethanol steam and CO2. Astringency removal using ethylene application is based on the over-ripening of fruits and it leads to tannin solubilization. Such a method results in drastic pulp firmness reduction due to increased activity of cell wall degradation enzymes such as cellulase, pectinmethylesterase, and polygalacturonase (Taira et al., 1997). It also results in acetaldehyde production by ethylene. This method shortens the fruits shelf life; it may cause mechanical damages, and impair fruits transportation and trade (Edagi and Kluge, 2009). Ethanol and CO2 treatments cause acetaldehyde accumulation in the fruits, thus insolubilizing the tannins due to covalent bonds among molecules. Ethanol’s efficiency as deastringency agent is set by the dose, application time, and temperature during application (Terra et al., 2014; Monteiro et al., 2012; Antoniolli et al., 2000). As a consequence, there is also pulp firmness reduction. High CO2 concentrations are used in the deastringency process. For example, for the ‘Rojo Brillante’ cultivar, 95% CO2 for 24 h at 20 C is recommended, as well as 90% RH for complete deastringency and fruit firmness maintenance (Salvador et al., 2007). This technology allows trading fruits such as “caqui crisp” and it has helped this fruit trading in the internal and external market.
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Deastringency by anaerobiosis may also be obtained by plastic bags that may cause atmosphere changes. Ben-Arie et al. (1991) found adequate persimmon fruit deastringency using polyethylene plastic bags. The acetaldehyde is formed during fruit ripening under normal conditions (Pesis, 2005). It is one of the composites responsible for aroma formation. Therefore, the deastringency must be done using correct doses of ethanol and CO2 to avoid flavor and aroma changes in the persimmon fruit.
HARVEST AND POSTHARVEST CONSERVATION The maturation stage for persimmon harvest is determined by skin color and pulp firmness (Salvador et al., 2006). The harvest of the fruits is done manually or with scissors to preserve a small part of the peduncle and keep the calyx of fruit. Afterwards, the fruits are packed in containers and appropriate boxes to avoid injury and mechanical damage. Persimmon fruits are taken to storage in chambers right after harvest depending on these cultivar’s need or not for astringency removal. Temperatures lower than 20 C must be avoided in order to accomplish effective treatments. Temperature reduction methods such as refrigeration, controlled atmosphere, packaging and 1-methylcyclopropene (1-MCP) application have been used to increase the conservation period by delaying fruit ripening. The ideal temperature for persimmon fruit conservation differs among cultivars. Studies performed on ‘Fuyu’ (Crisosto et al., 2007) and ‘Rojo Brillante’ persimmons (Salvador et al., 2007) indicate that these fruits are susceptible to damages caused by low temperatures. Inadequate temperatures for long periods of time may lead to damage caused by the cold. Such damages are seen through symptoms such as drastic pulp firmness reduction after the fruit is taken out of the chamber, pulp darkening, aqueous and translucent texture (Arnal et al., 2005; Woolf et al., 1997). 1-MCP has been applied to inhibit ripening evolution and to reduce damages caused by low temperatures. This blocking molecule impairs ethylene actions, which along with storage, inhibit ripening evolution.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Most persimmon fruits are traded for in natura consumption and it results in a great amount of fruits that are not able to meet the quality standards for size, shape, and ripening stage. Alternatives such as dry persimmon fruit, persimmon vinegar, and persimmon hard liquor production have been used to avoid disposing of these fruits and to add value to the raw material. Although there are no official production data, records of these products are found in Japan, Korea and in Brazil. Dry persimmon fruit production is traditional in Japan; the fruits are suspended by wire lines and dehydrated under room ventilation. Studies were already conducted on artificial drying as well as on different cut types for fruit dehydration, with good acceptance among consumers (Raupp et al., 2008). Although these products are locally produced and on a small scale, they present industrial potential, as persimmon pleases consumer’s taste in different countries worldwide.
ACKNOWLEDGMENT We are grateful to the research group from the Postharvest Physiology and Biochemistry Laboratory of the Biological Sciences Department at ESALQ/USP for the support given to the development of different research projects related to persimmon astringency. We are also grateful to Fundac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo for granting the PhD scholarship to the second author and for financing the research support projects.
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Woolf, A., Bola, S., Spooner, K.J., Lay-Yee, M., Ferguson, I.B., Watkins, C.B., et al., 1997. Reduction of chilling injury in the sweet persimmon ‘Fuyu’ during storage by dry air heat treatments. Postharvest Biol. Technol. 11, 155164. Yakushiji, H., Nakatsuka, A., 2007. Recent persimmon research in Japan. Jpn. J. Plant Sci. 1, 4262. Yonemori, K., Matsushima, J., 1985. Property of development of the tannin cells in non-astringent type fruits of Japanese persimmon (Diospyros kaki) and its relationship to natural deastringency. J. Jpn. Soc. Hortic. Sci. 54, 201208. Yonemori, K., Sugiura, A., Yamada, M., 2000. Persimmon genetics and breeding. Plant Breed. Rev. 19, 191225. Zhuang, D.H., Kitajima, A., Ishida, M., Sobajima, Y., 1990. The number of chromosomes in domestic varieties of Japanese persimmon (Diospyros kaki Thunb.). J. Jpn. Soc. Hortic. Sci. 59, 289297.
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Cempedak—Artocarpus champeden Moˆnica M. de Almeida Lopes1, Kellina O. de Souza1 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Origin and Botanical Aspects Nutritive and Medicinal Properties Anticancer Activity Antimalarial Activity
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Lectin and Cell Adhesion Activity Cytotoxicity Potential and Traditional Medicinal Uses References
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ORIGIN AND BOTANICAL ASPECTS Cempedak (Artocarpus champeden), also spelled “chempedak”, is a tropical fruit from the Moraceae family native to India, but can be found in Myanmar, Thailand, Vietnam, Malaysia, and Indonesia. Cempedak is similar to the jackfruit in appearance (Artocapus heteropyhllus Lam.) but is smaller and has a softer flesh (Bamroongrugsa and Yaacob, 1990). Various vernacular names are common for A. champeden (Lour.) such as: Banturung Manuk, Chempedak, Menkahai, Nakan and Temedak (Borneo); Sonekadat (Burmese); Uto Ni Idia (Fijian); Kathal and Kathar (Hindi) (India); Chakka (Malayalam), Panasa (Sanskrit), Pilual (Tamil); (Indonesia), Campedak or Baroh (Sri Lanka); Pani Varaka or Champada (Thailand); Campedak, Cempedak or Comedak (Java), Tundak (Japanese); Koparamitsu (Malaysia); Chempedak Mit Toˆ Nu (Vietnamese) (Jensen, 1995). The chempedak tree is an evergreen, medium-sized, mid-canopy, branched, monoecious tree. The tree can grow reach heights of 1030 m, and each fruit can have between 100 and 500 seeds. Its smooth bark becomes thick and rough as it ages, and usually fruits between September and January (Lim, 2012). The bark is grayish brown with bumps on the trunk and main limbs where leafy twigs are produced, which bears the fruits. The stem has white sap. Brown stiff, reflexed hairs 3 mm long cover the twigs, stipules, and leaves. Twigs are 2.54.0 mm thick, with annulate stipular scars. Leaves are alternate and borne on 13 cm long petiole. The lamina is obovate to elliptic, 525 3 2.512 cm size, and the base is cuneate to rounded, with entire margin, and acuminate apex, glossy green above and pale green and pubescent below. The lateral veins are in 610 pairs and curve forward. The inflorescences are solitary, unisexual, cauliflorous or ramiflorous and borne on the axillary position of short leafy shoots. Male heads are cylindrical, 35 cm, with small, 1 mm diameter, yellowish flowers with 1 straight stamen and 2 oblongs, concave, whitishyellow perianth segments. The female heads have small, tubular flowers, with perianths cohering at base and simple filiform styles with a 1.5 mm long exserted stigma (Phillipps and Dahlen, 1985). The fruit is a syncarp, formed by the enlarged connate perianths that are adnate to the axis of the inflorescence (Figs. 1 and 2). The fruit is cylindrical to oblongcylindrical, densely beset with short pyramidal, faintly prominent tubercles, 2035 cm 3 1015 cm in size and borne on a 712 cm long peduncle. The fruit can grow up to 30 cm long; the spines on its rind are not as pronounced as the jackfruit, and it usually has a “waist”, a slight narrowing near the middle of the fruit (Phillipps and Dahlen, 1985). The pulp covering the seeds found within the fruit is sought after for its fragrant taste. However, the hard seeds can also be cooked and eaten. The fruit is yellowish, brownish, or orangeyellow, and smells strongly at maturity. Pericarps, including the seeds, are ellipsoid to oblong about 3 3 2 cm, and the seeds are encased by a membranous testa. Cotyledons are unequal, thick, and fleshy (Lim, 2012). A. champeden is strictly a tropical species. In its natural ecological range, it commonly grows as an understorey tree in undisturbed mixed dipterocarp forests rainforest areas up to 500 m altitude or sometimes higher, where there is no Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00017-4 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Cempedak on the tree (Artocarpus champeden).
FIGURE 2 Infructescences present in the Cempedak fruit.
distinct dry season. It occurs mostly on ridges with clay to sandy soils. In secondary forests, it is usually present as a pre-disturbance remnant, or cultivated. The tree thrives on fertile well-drained soils, but prefers a high water table. It can survive periodic waterlogging (Phillipps and Dahlen, 1985). From an economic point of view, the Artocarpus species are well known for their fruits, such as jackfruit (Artocarpus heterophyllus) whose edible part corresponds to the developed walls of the ovaries, popularly known as berries (Peixoto and Toledo, 2002). Another fruit very appreciated is the breadfruit (Artocarpus altilis), typical food of the northern and northeastern regions of Brazil. The species Artocarpus hirsutus and A. champeden stand out for the economic value of their woods and for their use in folk medicine of the countries of origin, for the treatment of malaria, among other pathological occurrences.
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A number of Artocarpus species are used as food and for traditional folk medicines in south-east Asia, Indonesia, the western part of Java, and India. Artocarpus plants offer advantages as a profitable multipurpose crop for producing fruits and timber. The exceptional medicinal value of Artocarpus has long been recognized and economically the genus is of appreciable importance as a source of edible aggregate fruit; such as A. heterophyllus (jackfruit), A. altilis (breadfruit) and Artocarpus chempeden (Chempedak) and yielding fairly good timber (Verheij and Coronel, 1992).
NUTRITIVE AND MEDICINAL PROPERTIES The sweet, fragrant and flavorsome, fleshy perianth of the fruit is eaten fresh or preserved in syrup. In Malaysia, 12 perianth balls are coated with flour and deep fried to make into fritters for consumption as dessert or snacks. The ripe and unripe pulp is salted in Malaysia and used as a pickle called jerami. The perianths are also candied or made into chips by sun-drying. Young fruits are cooked in coconut milk and eaten as a curried vegetable or in soup or made into pickles. The seeds are rich in starch, eaten roasted or after boiling in salty water for 30 min and peeling off the seed coat. The seeds have a pleasant, nutty flavor. A starchy flour may be obtained from the seeds. The young, tender leaves are also cooked as vegetable in Sarawak (Lim, 2012). Jansen (1991) reported that chempedak seeds are made up of 10%25% of the fresh fruit weight, comprised mainly of carbohydrate, protein, and dietary fiber. The total fruit weight was found to vary from 0.6 to 3.5 kg and is generally smaller than the jackfruit. The total edible portion (perianths 1 seeds) is 25%50% of fresh fruit weight. The total weight of all perianths of a fresh fruit varied from 100 g to 1200 g. The proximate composition of the fleshy perianths on dry weight basis per 100 g edible portion was reported as: protein 3.57.0 g, fat 0.52.0 g, carbohydrates 8487 g, fibers 5.06.0 g, and ashes 2.04.0 g. The moisture (fresh weight basis) was 58%85% (Suranant, 2001). The proximate composition of seeds, per dry weight basis was reported as: 56 g of moisture, 12 g of protein, 0.9 g of fat crude, 2 g of fiber crude, 2 g of ash, 24 g of carbohydrate, and 30 g of starch (Chong et al., 2008b). The firmness of fresh chempedak is around: 9 g of hardness, 0.6 g of springiness, 0.6 g of cohesiveness and 3 g of chewiness. The color values for L*, a*, and b* parameters are 54, 2.5, and 44, respectively. For dried chempedak, the firmness parameters are: 345 g of hardness, 0.6 g springiness, 0.4 g of cohesiveness and 97 g of chewiness. Color values for L*, a*, and b* parameters are 44, 9.5, and 33, respectively (Chong et al., 2008a). According to these authors, in terms of quality, the changes of results for color and texture for dried chempedak was relatively significant compared to fresh chempedak. Others quality parameters found in fresh pulp chempedak were: 37 Brix for total soluble solids; pH of 5.0; sugars composition: 4.5 g/100 mL of fructose, 6.5 g/100 mL of glucose and 18 g/100 mL of sucrose, and organic acids: 0.8 g/ 100 mL of citric acid, 0.9 g/100 mL of malic acid and 0.5 g/100 mL of succinic acid (Lee et al., 2013). Fruit sweetness is an important aspect of fruit quality and is highly dependent on its sugar composition. Sucrose, glucose, and fructose are the main sugars found in fruits of commercial importance (Wrolstad and Shallenberger, 1981). In the fresh pulp of chempedak, bioactive compounds found are: ascorbic acid content of 6.2 mg/100 g (Fernandes et al., 2010) and total phenolic content 384 mg GAE/kg fresh weight (FW) (Lee et al., 2013). The antioxidant activity measured by the fluorescence recovery after photobleaching (FRAP) method is 3.88 mM Fe21/g FW and for β-carotene is 95.82% (Jelani et al., 2016). The potential of chempedak fruit rind as the source of pectin has been shown. The yield of chempedak rind pectin was 17.6%20.5%, in which nitric acid extracted the lowest yield of pectin (Leong et al., 2016). Chempedak fruit is one of the underexploited tropical fruits, as reported by the Rural Industries Research and Development Corporation (RIRDC). However, chempedak cultivation and consumption has increased substantially due to its nutritional value, delicacy, and flavor. The negative aspects of chempedak are short shelf life, unstable market price, and overproduction. However, these limitations could be overcome by processing it into dried fruit (Chong et al., 2008a). At the mature stage, chempedak has a strong unique aroma which is preferable among consumers (Wong et al., 1992; Chong et al., 2008a). Moreover, chempedak flavor has been reported to be similar to durian (Nakasone and Paull, 1998). The key odorants of two chempedak cultivars were clearly identified as 3-methylbutanal, octanal, ethyl 3-methylbutanoate and methyl 3-methylbutanoate which contribute to chempedak aroma composition (Buttara, 2014). Chempedak fruit volatiles contained 54 components of which 37.4%, were alcohols and 32.2% carboxylic acids. The main constituents were 3-methylbutanoic acid (28.2%) and 3-methylbutan-1-ol (24.3%). Other important flavor compounds include 2-acetyl-1-pyrroline and the tentatively identified 2,5-dimethyl-4-hydroxy-3(2 H)-furanone (Wong et al., 1992).
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Anticancer Activity The Artocarpus species are rich in phenolic compounds including flavonoids, stilbenoids, and arylbenzofurons (Hakim et al., 2006). From the roots the following prenylated flavones were isolated: artoindonesianin A, artoindonesianin B and anonin A. Anoindonesianins A and B exhibited cytotoxic activity against murine leukemia (P-388) cells (Hakim et al., 1999). Two isoprenylated flavones anoindonesianins U and V were isolated from the heartwood and the latter showed strong cytotoxic activity against P-388 cell lines (Syah et al., 2004). Also isolated was a new prenylated flavone, named cyclochampedol, together with four known triterpenes: cycloeucalenol, glutinol, cycloartenone, and 24-methylenecycloartanone as well as β-sitosterol (Achmad et al., 1996). Cyclochampedol was found to be bioactive in the brine shrimp lethality assay. This assay is useful tool for preliminary assessment of cytotoxicity.
Antimalarial Activity The stem bark and roots of Artocarpus integer contain prenylated flavones that possess cytotoxic and antimalarial activities. From the stem bark, the following prenylated flavones were isolated: artocarpones A and B, and seven known isoprenylated flavonoids: artoindonesianin E, artoindonesianin R, heterophyllin, heteroflavanone C, and artoindonesianin A2 (Widyawaruyanti et al., 2007). The inhibitory activities of these prenylated flavones support the traditional use of the dried stem bark of A. champeden as an antimalarial drug. Among the flavones isolated, heteroflavanone had the most potent inhibitory activity against the growth of Plasmodium falciparum 3D7 clone, with an IC50 value of I nmol/L. From the heartwood, 4 prenylated flavones artoindonesianins QT were isolated (Syah et al., 2006). In Thailand, researchers isolated an antimalarial prenylated stilbene, trans-4- (3-methyl-Ebut-1-eny1)-3, 5, 20 , 0 4 tetrahydroxystilbene with an EC50 of 1.7 μg/mL against Plasmodium falciparum in culture (Boonlaksiri et al., 2000). The quantitative assessment of antimalarial activity in vitro was determined by the microculture radioisotope technique based on the method described by Desjardins et al. (1979); which was used to examine the antiplasmodial activities of crude extracts of the aerial parts of A. champeden. An in vitro antimalarial assay was carried out using a multidrug resistant strain of the malarial parasite Plasmodium falciparum K1. The crude extracts of aerial parts of A. champeden showed moderate in vitro antimalarial activity against Plasmodium falciparum with an EC50 of 6.8 g/mL.
Lectin and Cell Adhesion Activity Purified lectins from seeds of six distinct clones of A. champeden (lectin C) were shown to be structurally and functionally similar (Hashim et al., 1993). The lectins appeared to interact with several human scrum proteins, with the predominance of the IgA1 and C1 inhibitor molecules. Interaction was not detected with IgA2, IgD, IgG, and IgM. The lectin Cs were also shown to precipitate monkey, sheep, rabbit, cat, hamster, rat and guinea pig serum. Due to their uniform properties, lectin C may be a better alternative to the A. heterophyllus lectin, jacalin, for use in future investigations. In another study, purified and crude extract of lectin C from six cultivars of A. champeden seeds were found to consume complement and thus decreased the complement-induced haemolytic activity of sensitized sheep erythrocytes (Hashim et al., 1994). The change in the complement-mediated haemolytic activity was significantly decreased when incubation of the lectins was performed in the presence of melibiose. The reversal effect of the carbohydrate, a potent inhibitor of the lectin binding to O-linked oligosaccharides of glycoprotein, demonstrated involvement of the lectins interaction with O-glycans of glycoproteins in the consumption of guinea O-pig complement. A mannose-binding lectin, termed chempedak lectin-M, was isolated from an extract of the crude seeds of chempedak (A. champeden) (Lim et al., 1997). When tested with all isotypes of immunoglobulins, chempedak lectin-M demonstrated a selective strong interaction with human IgE and IgM, and a weak interaction with IgA2. The binding interactions of lectin-M were metal ion independent. Further studies (Lim et al., 2012) showed that the lectin was the main mitogenic component in the crude extract of the chempedak seeds. It stimulated the proliferation of murine T cells at an optimal concentration of 2.5 μg/mL in a 3-day culture. Lectin-M appeared to be a T cell mitogen as it does not induce significant DNA synthesis when cultured with spleen cells from the nude mouse. In the absence of T cells, the lectin was incapable of inducing resting B cells to differentiate into immunoglobulin-secreting plasma cells. Further studies found chempedak lectin-M to be a lectin with high specificity and affinity for the core mannosyl residues of the N-linked oligosaccharides of glycoproteins (Hashim et al., 2001).
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Gabrielsen et al. (2010) found that the mannose-binding lectin from chempedak was a homotetramer with a single monomer molecular weight of 16,800 Da. Chempedak mannose-binding lectin had successfully been used to detect altered glycosylation states of serum proteins. A Ga1β1-3GaINAc- and IgAl-reactive lectin was isolated and purified from the seeds of chempedak (A. champeden) (Rahman et al., 2002). The lectin demonstrated at least 95% homology to the N-terminal sequence of the α chains of a few other galactose-binding Artocarpus lectins. The two smaller subunits of the lectin, each comprised of 21 amino acid residues, demonstrated minor sequence variability. Their sequences were generally comparable to the β chains of the other galactose-binding Artocarpus lectins. When used to probe human serum glycopeptides that were separated by two-dimensional gel electrophoresis, the lectin demonstrated strong apparent interactions with glycopeptides of IgAl, hemopexin, α2HS glycoprotein, α1-antichymotrypsin, and a few unknown glycoproteins. The galactose-binding lectin from chempedak (A. champeden) was found to consist of two chains: α and β (133 and 21 amino acids, respectively) (Gabrielsen et al., 2009).
Cytotoxicity Two new isoprenylated flavones, artoindonesianins U and V, have been isolated from the heartwood of A. chempeden and showed strong cytotoxicity against P-388 tumor cells with IC50 2.0 and 0.5 g/mL, respectively (Syah et al., 2004). In another report, Ko et al. (2005) isolated new prenylated flavonoids, artelastoheterol, artelasticinol, cycloartelastoxanthone, artelastoxanthone and cycloartelastoxanthendiol from the root bark of Artocarpus elasticus. The previously known compound artonol A exhibited cytotoxic activity against the A549 human cancer cell line, with an ED50 value of 1.1 g/mL. The prenylated flavones artoindonesianin A-2, artoindonesianin A-3, heterophyllin, cudraflavone C, artoindonesianin T have been isolated and identified from the chloroform extract of the heartwood of A. chempeden. These compounds showed strong cytotoxic activity against murine leukemia P388 cells with an IC50 value of 3.66, 5.45, 4.50, 4.50, 7.33 M, respectively (Syah et al., 2006). Cycloartobiloxanthone and artonin E have been isolated from the bark of Artocarpus rigida Blume which have a high cytotoxicity against leukemia P-388 cells (Suhartati et al., 2008).
POTENTIAL AND TRADITIONAL MEDICINAL USES Cempedak’s yellow, custard-like flesh and its hard seed are edible. The flesh is eaten fresh or cooked, it can be fried or its pulp creamed to make jams and cakes. Its flesh can be salted to make a pickle called jerami (Burkill, 2002). The hard seeds are boiled or roasted and eaten, a popular practice among the Malayan jungle tribes. Cempedak’s young leaves and whole young fruits are cooked as vegetables (Jensen, 1995). In traditional folkloric medicine, the Iban in Sarawak apply a chempedak paste of the inner bark to heal wounds and prevent infection. In peninsular Malaysia, chempedak juice of the roots has been used for fever. The ash from burnt leaves, maize, and coconut shell chempedak has been used to treat ulcers. An infusion of the root ash is mixed with Selaginella ash and prescribed as a protective medicine after childbirth. The bark of chempedak is used in poultices for painful feet, hands, and for ulcers. In the Philippines, the leaves of chempedak are heated and applied to wounds. The pith has been reported to cause abortion and the wood is a sedative. Unripe chempedak fruit is astringent and ripe fruit can be used as a laxative (Lim, 2012). A. chempeden is one of the Indonesian folk medicines; the seeds have been used against diarrhea and its roots against malaria fever. In the western part of Java, has been used to treat inflammation, dysentery (latex) and in female contraception (bark), and young leaves for treating tuberculosis (Heyne, 1987). The Artocarpus fruits and fruit products hold potential in the diet as they possess not only pleasant taste but are also source of naturally and readily available instant energy. Phenolic compounds including flavonoids, stilbenoids, and arylbenzofurons seem to be typical of the genus as they were detected in several species. Significant activity of the prenylated stilbenes and flavones isolated from certain species against Plasmodium have been reported (Namdaung et al., 2006; Boonphong et al., 2007; Widyawaruyanti et al., 2007). On the basis of biological activities of Artocarpus species, crude extract and derived phytochemicals and their uses as nutraceutical and pharmacological agents in traditional and modern research are possible but will first require clinical trials and product development. The current evidence is large limited to in vitro data. Artocarpus species is a very important part of biodiversity and it’s sustainable use for future generations.
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Suhartati, T., Yandri, H.S., 2008. The bioactivity test of artonin E from the bark of Artocarpus rigida Blume. Eur. J. Sci. Res. 23, 330337. Suranant, S., 2001. Under-Utilized Tropical Fruits of Thailand. RAP Publication, Bangkok, Thailand, pp. 1617. Syah, Y.M., Achmad, S.A., Ghisalberti, E.L., Hakim, E.H., Mujahidin, D., 2004. Two new cytotoxic isoprenylated flavones, artoindonesianins U and V, from the heartwood of Artocarpus champeden. Fitoterapia. 75 (2), 134140. Syah, Y.M., Juliawaty, L.D., Achmad, S.A., Hakim, E.H., Ghisalberti, E.L., 2006. Cytotoxic prenylated flavones from Artocarpus chempeden. J. Nat. Med. 60, 308312. Verheij, E.W.M., Coronel, R.E., 1992. Plant Resources of South-East Asia No. 2. Edible Fruits and Nut. Prosea, Bogor Indonesia. % Widyawaruyanti, A., Subehan, Kalauni, S.K., Awale, S., Nindatu, M., Zaini, N.C., et al., 2007. New prenylated flavones from Arocarpus champeden and their antimalarial activity in vitro. J. Nat. Med. 61, 410413. Wong, K.C., Lim, C.L., Wong, L.L., 1992. Volatile flavour constituents of chempedak (Artocapus polyphema Pers.) fruit and jackfruit (Artocarpus heterophyllus Lam.) from Malaysia. Flavour Fragrance J. 7, 307311. Wrolstad, R.E., Shallenberger, R.S., 1981. Free sugars and sorbitol in fruits: a compilation from the literature. J. Assoc. Offic. Anal. Chem. 64, 91103.
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Chilean Guava—Myrtus ugni Marcia A.A. Lorca University of Concepcio´n, Concepcio´n, Chile
Chapter Outline The Species Ethnic Uses Socioeconomic Importance Phytochemistry and Biological Activity Our Experience Murtilla Fruits Murtilla Leaves
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In Vitro Determination of the Antioxidant Capacity of Extracts and Phenolic Compounds From Ugni molinae Turcz. Leaves Antioxidant Activity of Ugni molinae Turcz. (“Murtilla”) Infuses Consumption of Ugni molinae (Turcz.) Tea Elicits Increased Plasma Antioxidant Potential in Humans References Further Reading
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THE SPECIES Chile is a country characterized by a rich and diverse flora, composed of about 6265 species of vascular plants (Maticorena, 1994). Of them, 85.5% are autochthonous and the remaining plants (14.5%) are introduced. One of the botanical families that occupy an important place due to its great abundance and diversity within Chilean flora is that to the Myrthaceae (Maticorena and Quezada, 1985). This family comprises more than 3000 species of trees and shrubs, divided into around 140 genera, which positions it as the largest family of Myrtales (Hoffmann, 1991; Gomes et al., 2009). Ugni molinae Turcz. is one of the most known Myrthaceae in central-southern Chile, because its fruit is abundantly consumed (Medel, 1979). Therefore, this species has aroused great interest among scientists, who have carried out various investigations related to its chemical composition and biological activity. It is commonly known as murtilla, myrtle, murillo or un˜i. The species corresponds to a wild perennial plant, distributed in the Chilean territory from Maule to Ayse´n regions, including the Archipelago of Juan Ferna´ndez (Fig. 1). It is extended mainly in the north area by the coastal mountains, some inland places, and the Andes mountains to the south. It usually grows in clear lands, and on the edges of forests, forming part of the thicket. Its development is considered frequent and its ecological distribution is predominantly in warm/wet environments, such as the typical Valdivian forest (Hoffmann, 1991; Gomes et al., 2009; Scheuermann et al., 2008; Fuenzalida, 2008). It is a shrub of great foliage, polymorphic, and small in drought conditions, but it can grow to two meters in areas with great rainfall. Its branches are compressed, covered by hairs and ascending stems and branching up 200 cm in length (Hoffmann, 1991). Its leaves are petiolate, opposed, without stipules, ovateoblong, with sharp apex, green lamina, glaucous, and marks in the underside. Leaves measure between 2 and 2.5 cm in length (Hoffmann, 1991). Its pendulous flowers are solitary, axillary, long pedunculated, and hermaphroditic. There are five sepals united at the base and bent outwards, five linear petals, sharp and rounded, and numerous stamens, and a style longer than these. The flowering season is between November and December (Hoffmann, 1991). The fruit is a small globose berry that contains a large amount of seeds, from 10 to 27, fleshy, sweet and aromatic, with the remains of the chalices in pentamers and tetramers in the same plant. The equatorial diameter ranges between 0.7 and 1.3 cm and the unit weight reaches 0.45 g. Its pulp is white and according to the different areas where this plant grows there are varieties for the tonality of the epicarp, including pale green, yellow, fuchsia, and dark and light red (Hoffmann, 1991; Scheuermann et al., 2008; Torres et al., 1999) (Fig. 2). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00018-6 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Distribution of Ugni molinae in the continental and insular Chilean territory (Landrum, 1988; Rojas & Pequen˜o, 1998).
ETHNIC USES The fruits of murtilla are known by the native people with the name “grapes of the forest” and these berries are considered useful to ease circulation disorders and to increase visual acuity, especially at night. In addition, the skin is useful for treating mouth conditions, such as thrush and stomatitis (Rozzi, 1984). On the other hand, murtilla fruits are consumed fresh due to its organoleptic characteristics and they are also used for the preparation of jams, syrups, desserts, and liquors (Hoffmann, 1991).
SOCIOECONOMIC IMPORTANCE Many plants have useful properties for the human being, among which, medicinal, nutritional, and industrial application properties can be emphasized. However, these characteristics, often transmitted through oral stories have not
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FIGURE 2 Botanical parts of Ugni molinae (www.chileflora.cl; Avello et al., 2009a). (A) Leaves and fruits. (B) Branch with floral buds. (C) Shrub.
been scientifically proven in a large number of plants (Montenegro, 2000). Undoubtedly, one of the most attractive organs of murtilla is the fruit, due to its smell, color or taste, usually pleasant. From a nutritional point of view, vegetal natural products provide a wide variety of compounds with a remarkable chemical structure, so they can be considered a biosynthesis laboratory capable of supplying the nutritional needs of all living beings (Table 1) (Montes et al., 1992). The fruit is characterized by having a high consumption level, especially in southern Chile. The consume is renewed annually with fruiting, Murtilla fruit is collected from its wild relics and sold at local markets and fairs. A study of these places of sale was carried out in the project entitled “Domestication and development of the murtilla (U. molinae Turcz.), a berry native to Southern Chile,” financed by CORFO FDI (Development and Innovation Fund of the Corporation of Promotion of Production, Chile) and carried out by the Austral University of Chile and INIA researchers of the Carillanca and Remehue Centers. This study has pointed out important information referred to the dynamics of these markets which until now only operate with harvested murtilla. In summary, data collected indicate that the trading period of the murtilla begins from the end of February (from Temuco to Valdivia) until early June (Ensenada locality). The final consumer price varies from $850 to $2000 Chilean
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TABLE 1 Proximal Chemical Analysis of the Ugni molinae Fruit (Hevia et al., 1993; Torres et al., 1999; Fuenzalida, 2008) Water content
77.2%
Ash content
1.17%
Total soluble carbohydrates
10.90 g/100 g P.S.
Total proteins
0.30 g/100 g P.S.
Soluble solids
19.4 Brix
Starch
2.51 μg/mL
pesos per kg at the end of the season delivered in plastic bags or in case of large sales, in banana boxes of 20 or 22 kg. In average, between 17 and 30 kg/day are sold, depending on the location of the store and on a good day, the sales can reach 500 kg to individuals. In the best located stores, 1000 kg have been sold per day to jam producers. In general, there are three types of merchants who sell in fairs and small localities: eventual sellers, permanent sellers, and collectors who sell directly. They indicate that once the fruit is acquired, this lasts between 3 days and a week and then it deteriorates. This durability varies according to the locality. There are also very notable differences between fruits traded in the different markets studied and among the characteristics, color and size varied the most. Special mention should be made of the locality of Ensenada, which seems to be organized to coordinate the sale to large buyers. In 2003 this locality, with the support by the municipality of Puerto Varas, held the first Fair of Murtilla. During this event, all kinds of preparations based on murtilla were traded, such as pasties, juice, murtao (murtilla liquor), syrup, turnovers, murtilla jam, and others. In recent times, small agroindustries have acquired fruits for the preparation of processed products, causing the demand for the fresh fruit to increase. Likewise, some shipments of fresh fruit have been successfully shipped overseas, but without continuity (Murtilla, 2009). Given the above, some challenges of the murtilla market are: G
G
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Increasing domestic consumption in the country, as most inhabitants of Chile are not aware of this interesting native fruit. From the O’Higgins region to the north there is no such species and it is not consumed. For example, in Santiago, the main market in Chile, the benefits of the murtilla are not known. Increasing agroindustrial consumption of the country, as according to a study carried out by the FDI-INIA project team, large agroindustries of Chile hardly know this fruit or its properties. Positioning the murtilla and its derivatives as distinctive products of southern Chile in an international context. Although the country is well known for table grapes, apples, peaches, and blueberries, none of these fruits are native, but murtilla is native, and its food characteristics are equally or more interesting in comparison with these or other fruits. Generating a consolidated and articulated murtilla industry, This means involving all parties and links of the murtilla productive chain, from research to commercialization.
In recent studies carried out on murtilla fruit, the existence of new attributes have been indicated, especially the presence of antioxidants, which has generated greater interest by the market, enhancing the compliance of the proposed goals (Murtilla, 2009).
PHYTOCHEMISTRY AND BIOLOGICAL ACTIVITY The aroma (essential oil) plays a significant role for the distribution of murtilla in the market of the fruit and the industry of the flavor. Different researchers have been interested in identifying the main volatile compounds, as well as studying their stability after the refrigerated storage of the fruit. The particular aroma can be defined as fruity, sweet, and floral and it is mainly due to 24 volatile compounds that were identified. These correspond to the same compounds located in fruits widely consumed worldwide. Compounds in greater concentration in the murtilla aroma are: methyl 2-methyl butanoate, ethyl butanoate, ethyl 2-methyl butanoate, methyl hexanoate, ethyl hexanoate, methyl benzoate, and ethyl benzoate. The concentration of each of the
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compounds detected is in the range of 1.2 and 250.5 μg/kg. This concentration corresponds to the measurement of the volatile fraction absorbed by a Porapak Q column from the head space of a recipient with intact fresh fruit respect to the weight thereof. A statistical analysis indicates that the storage for 60 days at 0 C causes different effects in the volatile compounds present in all studied ecotypes of murtilla. Ecotypes are subpopulations genetically differentiated that are restricted to a specific habitat, a particular environment, a defined ecosystem, and a defined ecosystem with tolerance limits to environmental factors. This could suggest that there may be differences related to the very nature of these ecotypes (INIA Carillanca, www.inia.cl). Ecotype 19-1 of murtilla fruit, can be considered the best for refrigerated storage, since the odor activity values of seven aromatic compounds which are presumed to be the most significant, maintain high values during the period, with the exception of methyl 2-methyl butonoate at the end of the storage (Scheuermann et al., 2008). Regarding the sugar content, there are several ecotypes that have interesting average levels of fructose (21.6 mg/gpf) and sucrose (68.6134.2 mg/gpf) (Torres et al., 1999). Studies carried out in 1993 by Pessa and Caprile showed that murtilla fruits have in their seeds a high level of unsaturation; a significant content of linoleic acid, and absence of linolenic acid. This indicates that it would be potentially a good source of edible oil, and may constitute a good quality dietary supplement. From the aforementioned studies it was also concluded that murtilla seed oil surpasses safflower in terms of linoleic acid contents (85.8% and 78.7%, respectively). Linoleic acid is an essential nutrient in the synthesis of prostaglandins, generation of cell membranes, defense mechanisms, and tissue regeneration. This suggests that murtilla oil would also represent a potential source in the manufacture of cosmetics (Pessa and Caprile, 1993). The fruit is also rich in antioxidants. There are ecotypes with comparatively high levels of ascorbic acid (average 65.4 mg/100 g), as well as carotenes and polyphenols (Murtilla, 2009). Flavonols detected correspond mainly to derivatives from myricetin and quercetin, and in minor proportion to derivatives from laricillin, isorhamnetin, and syringetin. The concentrations of total flavonols vary from 43 to 1.56 μmol/g, depending on the locality in which the fruits were collected. These concentrations exceed those of total flavonols in Chilean wineberry and Magellan barberry. Total concentrations of flavan-3-oles present an increment from north to south, varying between 0.94 and 1.81 μmol/g. Total resveratrol determined after acid hydrolysis to the form of transresveratrol varies from 0.19 to 0.25 μmol/g of dry fruit, and is comparatively lower than that detected in Magellan barberry fruits (Ruiz, 2008). Murtilla fruit presents two anthocyanins, peonidin-3-glucoside and cyanindin-3-glucoside. Total concentrations are about 1 μmol/g of dry matter, with the most abundant being cyanindin-3-glucoside. These concentrations are much lower than those of other studied fruits such as wineberry and Magellan barberry, but this is somewhat expected, because murtilla presents a much lower intensity of colored compounds (Ruiz, 2008). The levels of antioxidant activity among the different samples analyzed of the fruit fluctuate between 65 and 67 μmol/g Trolox, equivalents, values much lower than those observed for other fruits, even though the concentration of flavonols was higher. This indicates that such compounds to which a high antioxidant power is attributed would not be responsible of such ability, but according to the results that power would be the phenolic fraction as a whole (Ruiz, 2008).
OUR EXPERIENCE Murtilla Fruits In 2013, our research team initiated a study to assess the antioxidant capacity of the murtilla fruit. The corresponding results were published in 2014 (Suwalsky and Avello, 2014). The general objective of this study was to determine the effects produced by the compounds present in aqueous extracts of the fruit of murtilla on molecular models of biological membranes, constituted by lipid multilayers and liposomes, and extend these studies to a biological system constituted by human red blood cells. The specific objectives and transversally the method used were as follows: G
G
Evaluate the effect of the aqueous extract of the fruit of murtilla on molecular aspects of the fluidity of cell membranes, using molecular systems constituted by lipid multilayers, large unilamellar liposomes, and membranes of human erythrocytes as model. Determine the antioxidant capacity of the aqueous extract of the fruit of murtilla in cell membranes in a human erythrocytes model.
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The main conclusions were as follows: G
G
G
G
G
G
G
G
G
The 2% aqueous extract of murtilla (plant material collected in the Biobı´o Province of Chile) contains an average of 10.64 6 0.04 mM GAE (gallic acid equivalents) determined by the FolinCiocalteu method. GAE are very good chemical markers, representative of a sample rich in polyphenols, easily measurable by analytical methods. The aqueous extract of the fruit contains flavonoids and anthocyanins, compounds with recognized antioxidant properties. The latter correspond to cyaniding and peonidin, identified by HPLC/MS in their glycosylated forms. Studies by X-ray diffraction indicated that the phytocomplex of the aqueous extract caused structural disorders in both polar heads and acyclic chains, in the phospholipid multilayers of DMPC (simulation of interaction with outer monolayer of the cell membrane). On the other hand, there were no significant interactions with the outer monolayer of the cell membrane, without considering toxic effects. Studies by fluorescence spectrometry in large unilamellar vesicles of DMPC (simulation of interaction with the outer monolayer of the cell membrane) indicated that the phytocomplex caused molecular disorders in both polar head and acyclic chain regions in gel and liquid crystalline state. The results by fluorescence spectroscopy in nonsealed membranes of human erythrocytes (IUM) indicated a decrease in the values of generalized polarization and anisotropy. This indicates structural disturbances in both polar head and acyclic chains of the phospholipids that form these membranes. These results are in accordance with the previous ones. Observations by scanning electron microscopy of intact human red cells showed that the phytocomplex of the aqueous extract (constituted by flavonoids and anthocyanins) induced morphological changes in which the echinocyte form predominates. This is due to an interaction with the outer monolayer of the erythrocyte. According to the microscopic observation, these changes are not considered toxic. Studies on antioxidant capacity have showed that the aqueous extract of the fruit is capable of protecting the cell membrane of the damage induced by hypochlorous acid (HClO), a recognized oxygen reactive species. The protection exerted by the extract against hemolysis produced by HClO in red cells complement the background in relation to the antioxidant capacity of these species. The set of experimental results allowed verifying that the phytocomplex of the species interacts with lipid bilayers. This interaction occurs in the outer monolayer, so that it can be deduced that the components of this phytocomplex remain outside the cell. This would explain the protective effect against the oxidizing action of HClO. All these antecedents contribute to the validation of antioxidant properties of the fruit and that its consumption is indicated as beneficial for health and with potential to prevent diseases derived from oxidative stress.
Murtilla Leaves The sustainable botanical parts are always of interest to the industry. The reasons are preferably of yield and supply throughout the harvest year. This, depending on the chemical interest a vegetal species has, directed to the pharmaceutical, cosmetic or food industry. Murtilla is a shrub that contains in its leaves a battery of chemical compounds of interest to the business interests of Chile and the world. Unlike the fruits, the leaves of this species contain tannins of the ellagitannin and gallotannin type, flavonols such as myricetin and quercetin in the form of genins and glycosides. Galloylated forms of these flavonoids have been identified in our studies. In addition, the presence of flavan-3-ols such as catechins and phenolic acids is evidenced. In our research, in the leaves of this species, the presence of pentacyclic triterpene saponins has been detected (Avello et al., 2014). This chemical composition corresponds to the ethnomedical uses described for murtilla, such as treatments against diarrhea, dysentery, and oral infections. This is due to the fact that these components have potent antimicrobial and astringent properties (Avello et al., 2013a). This background has led the species to become raw material for cosmetic industry, due to its antiage (phenolic compounds) and lipolytic (triterpene saponins) properties, in national cosmetic lines such as the VitaMurtilla line (www.dermik.cl). Based on these phytochemical data, our research team has developed several studies focused on evidencing the antioxidant capacity of the leaves of this species in diverse models: in vitro, cellular, and in human volunteers, supported on the identification of groups of polyphenolic phytochemical compounds. Some examples of these studies (abstracts) are presented as follows.
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IN VITRO DETERMINATION OF THE ANTIOXIDANT CAPACITY OF EXTRACTS AND PHENOLIC COMPOUNDS FROM UGNI MOLINAE TURCZ. LEAVES The antioxidant activity of two extracts (ethyl acetate and methanol) of U. molinae Turcz. (Myrtaceae) leaves was assessed using different assays. HPLC profiling of both extracts showed the presence of flavan-3-ols (catechin) and gallic acid, flavonoid, and caffeic acid derivates as main constituents. These extracts showed significant activity on 2,2diphenyl-1-picrylhydrazyl, cupric ion reducing antioxidant capacity (CUPRAC), and hydroxyl radical assays. Importantly, bleaching of β-carotene-linoleate liposomes and copper-induced oxidation of human LDL were prevented by both extracts. Therefore, these results suggest that polyphenol-rich extracts of U. molinae could slow lipid peroxidation and limit free radical damage (Avello et al., 2013c).
ANTIOXIDANT ACTIVITY OF UGNI MOLINAE TURCZ. (“MURTILLA”) INFUSES There is epidemiological evidence that support the pathogenic role of free radicals in biological processes, which may decrease by increasing antioxidant intake. Preliminary studies carried out on the leaves of the Chilean plant U. molinae Turcz. (“Murtilla”) showed the presence of high concentrations of phenolic compounds with in vitro antioxidant capacity. This study was aimed to evaluate the effect of U. molinae on the plasmatic antioxidant status of healthy volunteers after ingesting the infusion (1%) during a period of 3 days. For this, the oxygen radicals absorption capacity (ORAC) method was used in blood samples obtained at the beginning and at the end of the study, The determination of ORAC values in volunteers allowed detecting significant changes in the basal levels of hydrophilic plasmatic antioxidants. This increment in the antioxidant capacity expressed as plasmatic ORAC (μM Trolox equiv/L) reached 27.3% in relation to basal levels. The ORAC value for the infusion (1%) corresponded to 533.11 μM Trolox/g equivalents of dry leaves. In this study, the antioxidant capacity of the infusion (1%) of U. molinae leaves and the increment in the plasmatic antioxidant capacity associated to its regular intake (Avello and Pastene, 2005).
CONSUMPTION OF UGNI MOLINAE (TURCZ.) TEA ELICITS INCREASED PLASMA ANTIOXIDANT POTENTIAL IN HUMANS U. molinae Turcz. is a native Chilean plant widely distributed in central-southern Chile and in the Juan Ferna´ndez archipelago. Comparative quantitative studies of U. molinae populations revealed that total phenol contents were 40.7% higher in the Juan Ferna´ndez archipelago than in the Bı´o-Bı´o Region. This figure constitutes a significant difference. Teas made from the leaves of continental and island U. molinae populations were given to healthy volunteers, and their antioxidant plasma capacity was evaluated before and after consumption by monitoring conjugated dienes, thiobarbituric acid reactive substances, and CUPRAC. These levels were higher in volunteers who drank the tea made from the plants of the Juan Ferna´ndez archipelago (Avello et al., 2013b). These results allow suggesting that the intake of infuses of murtilla leaves can be beneficial in the preservation of health. Interesting note: The national Company N-Active, destined to the export of raw materials for cosmetic, food, and pharmaceutical industry has also turned its focus on the leaves of this species and its chemical attributes. Currently we collaborate (University-Company) in the development of raw materials in function of improving the quality of life of the population (www.nactive.cl). Lately, the scientific community has focused their studies on the action of metabolome of several compounds and their consequent biological action. Regarding the compounds described for murtilla leaves, these would have interesting effects for anticancer in gastrointestinal tracts. These compounds correspond to tannins, galloylated forms of flavonols, and pentacyclic triterpene saponins. At this time, our research team is evaluating this, subjecting the aqueous extracts of the leaves of this species to in vitro gastrointestinal digestion and observing what is happening in gastric and colorectal cancer. This is because there is evidence that product of the gastrointestinal metabolism of these compounds, metabolites with significant anticancer action, would be generated for this kind of pathologies (Proyecto Fondecyt de Iniciacio´n, 11160275). Based on the results of the application of basic science, both fruit and leaves of U. molinae could be constituted as therapeutic, nutraceutical, and cosmoceutical resources of socioeconomic importance at both national and global level, driven by the productive sector (Avello et al., 2009b) (Figs. 3 and 4).
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FIGURE 3 Chromatogram at 520 nm of the aqueous extract of Ugni molinae. Anthocyanin 3-0-glucoside and peondin 3-0-glucoside are identified (Orellana, 2011).
FIGURE 4 Effect on the morphology of human erythrocytes (RBC) of hipoclorous acid (HClO) 0.5 mM in extract concentration (Orellana, 2011). (A) Control (RBC 10%). (B) Extract 0.8 mM 1 RBC 10%. (C) RBC 10% 1 HClO 0.5 mM. (D) RBC 10% 1 HClO 0.5 mM 1 Extract 0.8 mM.
Chilean Guava—Myrtus ugni
FIGURE 4 (Continued).
FIGURE 4 (Continued).
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FIGURE 4 (Continued).
REFERENCES Avello, M., Pastene, E., 2005. Antioxidant capacity of Ugni molinae Turcz. (“Murtilla”) infuses. Bol. Latinoam. Caribe Plant. Med. Aroma´t. 4 (2), 3339.23. Avello, M., Valdivia, R., Mondaca, M.A., Ordo´n˜ez, J.L., Bittner, M., Becerra, J., 2009a. Actividad de Ugni molinae Turcz. frente a microorganismos de importancia clı´nica. BLACPMA. 8 (2), 141144a. Avello, M., Valdivia, R., Sanzana, R., Mondaca, M.A., Mennickent, S., Aeschlimann, V., et al., 2009b. Extractos a Partir de Berries Nativos Para su Uso como Preservantes Naturales en Productos Cosme´ticos. Bol. Latinoam. Caribe Plant. Med. Aroma´t. 8 (6), 479486. Avello, M., Bittner, M., Becerra, J., 2013a. Efectos Antibacterianos de Extractos de Especies del Ge´nero Ugni que Crecen en Chile. Rev. Cubana Plant. Med. 18 (2), 247257. Avello, M., Pastene, E., Bustos, E., Bittner, M., Becerra, J., 2013b. Variation in phenolic compounds of Ugni molinae populations and their potential use as antioxidant supplement. Rev. Bras. Farmacogn. 23 (1), 4450. Avello, M., Pastene, E., Gonza´lez, M., Bittner, M., Becerra, J., 2013c. In vitro determination of the antioxidant capacity of Ugni molinae extracts. Rev. Cubana Plant. Med. 18 (4), 596608. Avello, M., Pastene, E., Barriga, A., Bittner, M., Ruiz, E., Becerra, J., 2014. Chemical properties and assessment of the antioxidant capacity of leaf extracts from populations of Ugni molinae growing in Continental Chile and in Juan Ferna´ndez Archipelago. Int. J. Pharmacogn. Phytochem. Res. 6 (4), 746752. Fuenzalida, C. (2008). Caracterizacio´n Fı´sica-Quı´mica y Bota´nica de Berries de Mirta´ceas Nativas de la Cordillera Costera de la Provincia de Valdivia, Chile. Tesis para Optar al Tı´tulo de Quı´mico Farmace´utico, Universidad Austral de Chile, pp. 2957. Gomes, S., Somavilla, N., Gomes-Bezerra, K., do Cuoto, S., Simao, P., Graciano-Ribeiro, D., 2009. Leaf anatomy of Myrtaceae species: contributions to the taxonomy and phylogeny. Acta Bot. Bras. 23 (1), 223238. Hevia, F., Venegas, A., Wilckens, R., Araya, F., Tapia, M., 1993. Murtilla (Ugni molinae T.) III. Algunas Caracterı´sticas del Fruto Recolectado en Chile. Agro-Ciencia. 9 (1), 6366. Hoffmann, A., 1991. Flora Silvestre de Chile Zona Araucana. Editorial Claudio Gay, Santiago, p. 160. Segunda Edicio´n. Landrum, L., 1988. The Myrtle family (Myrtaceae) in Chile. Proc. Calif. Acad. Sci. 45 (12), 293298. Maticorena, C., 1994. Contribucio´n a la Estadı´stica de la Flora Vascular de Chile. Gayana Bot. 47 (34), 85113. Maticorena, C., Quezada, M., 1985. Cata´logo de la Flora Vascular de Chile. Gayana Bot. 42 (12), 1155. Medel, F., 1979. Prospeccio´n de Arbustos Frutales en el Sur de Chile. Agro Sur. 7 (2), 9497. ´ til. Ediciones Universidad Cato´lica de Chile, Santiago, p. 267. Montenegro, G., 2000. Nuestra Flora U Montes, M., Wilkomirsky, T., Valenzuela, L., 1992. Plantas Medicinales. Ediciones Universidad de Concepcio´n, Concepcio´n, p. 207. Murtilla Ugni molinae, el berry nativo del sur de chile. Murtilla [Internet], Murtilla Chile, INIA Chile, Agosto2009. Disponible en: ,http://www.murtillachile.cl/. (accessed 30.09.09.).
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Orellana, P., 2011. Efectos Estructurales del Extracto del Fruto de Ugni molinae Turcz. (Murtilla) sobre Membranas Celulares. Trabajo de Fin de Carrera para Optar al Tı´tulo de Quı´mico Farmace´utico, Facultad de Farmacia, Universidad de Concepcio´n. Chile. Pessa, J., Caprile, L., 1993. Ana´lisis y Composicio´n de Aceite en Semilla de Murta (Ugni molinae). Alimentos. 18 (1), 1114. Proyecto Fondecyt de Iniciacio´n 11160275. “Evaluation of the Effect of Aqueous Extracts and Fractions Obtained from Leaves of Ugni molinae and their Respective Products of in vitro Gastrointestinal Digestion on the Viability of Human Gastric and Colorectal Cancer Cells”. Director. Dra. Avello M. 2016-2019. Rojas, J., Pequen˜o, G., 1998. Peces serra´nidos de la isla Alejandro Selkirk, archipie´lago Juan Ferna´ndez, Chile (Pisces: Serranidae): a´nalisis ictiogeogra´fico. Invest. Mar. 26, 4158. Rozzi, S., 1984. Las Plantas, Fuente de Salud. Pı´a Sociedad San Pablo, Santiago, p. 230. Ruiz, M., 2008. Compuestos Feno´licos en Frutos de Calafate (Berberis Microphylla) y Comparacio´n de su Capacidad Antioxidante con otros Berries del Sur de Chile. Tesis para Optar al Tı´tulo de Bioquı´mico, Universidad de Concepcio´n, 4348, 8691. Scheuermann, E., Seguel, I., Montenegro, A., Bustos, R., Hormaza´bal, E., Quiroz, A., 2008. Evolution of aroma compounds of murtilla fruits (Ugni molinae Turcz.) during storage. J. Sci. Food Agric. 88, 485492. Suwalsky, M., Avello, M., 2014. Antioxidant capacity of Ugni molinae fruit extract on human erythrocytes: an in vitro study. J. Membr. Biol. 247 (8), 703712. Torres, A., Seguel, I., Contreras, G., Castro, M., 1999. Caracterizacio´n Fı´sico-Quı´mica de Frutos de Murta (Murtilla) Ugni molinae Turcz. Agric. Te´cn. 59 (4), 260270.
FURTHER READING Escobar, M., Olivares, S., Zacarı´as, I., 2002. Manejo Alimentario del Adulto con Sobrepeso u Obesidad. Ministerio de Salud, Santiago, p. 64.
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Ciruela/Mexican Plum—Spondias purpurea L. Georgina Vargas-Simo´n Universidad Jua´rez Auto´noma de Tabasco, Villahermosa, Tabasco, Mexico
Chapter Outline Cultivar Origin and Ethnobotanical Aspects Botanical Description Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolic, Antioxidant Compounds, and Sensory Characteristics
141 142 143 144 144
Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Propagation References Acknowledgment Further Reading
145 148 149 149 149 152
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CULTIVAR ORIGIN AND ETHNOBOTANICAL ASPECTS Spondias purpurea is a highly appreciated fruit species; it has different common names according to the zone. In Mexico and Central America is known as ciruela, chiabal, cirgu¨ela, ciruela calentana, ciruela tuxpana, ciruela mexicana, ciruela morada, ciruela roja, ciruela sanjuanera, hobo Colorado, jocote, jocote amarillo (yellow form), and jocote de corona, among others. In South America it is known as ciruela de huesito; Siriguela, cirigu¨eleira, ambu, ameixa da Espanha, caja´ vermelha, ciriguela, ciroela, imbu or umbu in Brazil; cirouelle, mombin rouge, prune du Chili, prune d’Espagne, prune jaune (yellow form) or prune rouge in French; and red mombin, red mombin, Spanish plum, scarlet plum; purple plum in the Virgin Islands, Jamaica plum in Trinidad, and Chile plum in Barbados (Morton, 1987; Hoyos, 1994). It is originally from Mesoamerica, although its distribution is from central Mexico to Peru and Brazil. Generally it grows at between 10 and 2000 m above sea level and it has been introduced in Florida and the Caribbean. It is known that wild populations can be found in altitudes up to 1800 m above sea level associated with low elevation tropical deciduous forest and semideciduous tropical forest, as well as with high and medium elevation tropical deciduous and semideciduous forest. It is also found in natural savannas of Colombia and northwest part of Brazil, in the Caatinga bioma (Silva et al., 2014; Vargas-Simo´n and Gama, 2010; Miller, 2008; Miller and Knouft, 2006; Ca´rdenas and Ramı´rez, 2004). It can also be commonly seen in home gardens and used as a living fence (Albuquerque et al., 2009; Maldonado et al., 2004; Avitia et al., 2000). Many clonal varieties are known. For example, 20 of them have been determined in the Gulf of Mexico coastal area. These varieties can be differentiated by some ecophysiological characteristics but mostly by color and fruit size (Vargas-Simo´n et al., 2011; Avitia et al., 2000). Zizumbo-Villarreal et al. (2012) referred to the S. purpurea as an important foodstuff used since the pre-Hispanic era. Nowadays it is consumed fresh, unripe (fresh or cooked with beans Phaseolus vulgaris) or ripe, macerated in sugarcane alcohol, and dehydrated (sweet or salty). Also, the juice of this fruit is commonly used for preparing jams, atoles, desserts, beverages (fresh or fermented) and vinegar. In Nicaragua, there is a very typical dessert made of red mombin (S. purpurea), mango (Mangifera indica), and cashew apple (Anacardium occidentale) with honey called curbasa (Avitia et al., 2000; Barbeau, 1990; Morton, 1987). The sprouts and leaves are eaten uncooked or cooked as vegetables. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00052-6 © 2018 Elsevier Inc. All rights reserved.
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In addition, exudates are used as glue. The wood is light and soft, useful for producing paper and the ash is ideal for making soap. Leaves are used for feeding goats and the fruits for feeding pigs (Cordero and Boshier, 2003). In the wild, the fruits are eaten mostly by monkeys (Cebus capucinus and Alouatta palliata) and iguanas (Ctenosaura similis) (Gonza´lez-Garcı´a et al., 2009; Wehncke et al. 2004). Thus, female S. purpurea trees can act as a recruitment center for seedlings in dry tropical forests due to the wild fauna feeding on its fruits during the drought season and acting as seed dispersers (Me´ndez-Toribio et al., 2014). Furthermore, S. purpurea is a melliferous species (Niembro et al., 2010). The red mombin is medicinal. The fruits are diuretic and antispasmodic, commonly used as an antihistaminic and the extract from the bark is used for stomach upset such as dysentery (Lozano et al., 2014; Hopkins and Stepp, 2012). In the Philippines, bark sap is used for stomatitis in toddlers. The extract of boiled leaves and bark works as a febrifuge. The tree resin mixed with pineapple (Ananas comosus) or soursop (Annona graveolens) juice is used for treating icterus (Morton, 1987). A study of its organic matter input (branches, leaves, and fruits) in home gardens revealed that it produces 110 kg/ha per year of litter, 3 kg/ha per year of N, 0.66 kg/ha per year of P and 47 kg/ha per year of C due to its deciduous condition. Although is a small input compared with other ecosystems, it is important for nutrient recycling (Benjamin et al., 2001).
BOTANICAL DESCRIPTION S. purpurea has been described as a deciduous tree that can reach 1215 m in height and 80 cm of diameter at breast height (Fig. 1). Nonetheless, because of the domestication and vegetative propagation, they are generally short trees, 810 m high, a winding trunk with thick branches, wide canopy, smooth and plain bark, grayish or whitish. Compound leaves are imparipinnate, alternate, opposed, subopposed, bright green or purple when young, 1225 cm in length, leaflets of 26 cm of length in average, with 411 pairs, almost subsessile, variable in form, from oblong to trapezoidal or obovate, sometimes pubescent when young (Fig. 2). Flowers are hermaphroditic although physiologically unisexual (dioic trees), arranged in small and thin panicles, commonly produced when the tree is defoliated, female flowers, red, petals (45) of 3 mm of length, masculine flowers are hipogin, with 46 pink, red or greenish yellow petals, from 9 to 12 stamens and 1 ovary. Fruits are drupe, oblong,
FIGURE 1 Spondias purpurea tree, home garden in Tabasco, Me´xico.
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143
FIGURE 2 Spondias purpurea compound leaves (A) Ecotype ‘purple’, (B) Ecotype ‘yellow tuxpana’, (C) Ecotype ‘red’ and (D) Inflorescence.
oval, obovoid or pear shaped, generally red to purple, sometimes yellow, from 2.5 to 5.5 cm in length, its equatorial diameter is of 2.13.6 cm, its fresh weight varies from 4 to 43.2 g (Fig. 3). There is a smooth or semismooth epicarp; mesocarp, yellowish, juicy, thin of 15 mm, woody endocarp, it occasionally has protuberances at the apical end, corresponding to the remains of the stigmas, these are nominated “crown fruits.” In wild trees it is possible to find from 1 to 6 seeds of 12 mm of length, whose embryos are achlorophyllous, in clonal varieties this does not happen (Alia-Tejacal et al., 2012; Guerrero et al., 2011; Vargas-Simo´n et al., 2011; Pe´rez-Arias et al., 2008; Pennington and Sarukha´n, 2005; Vanegas, 2005; Avitia et al., 2000; Cuevas, 1992; Morton, 1987; Janzen, 1982; Standley and Steyermark, 1949). It is a drought-tolerant species, values up to 21 MPa can be found in the stem, it can store water (Borchert, 1994). As a deciduous species, the defoliation takes place between January and June, which coincides with the blooming and fruiting season (Vargas-Simo´n et al., 2011; Querejeta et al., 2007; Bullock and Solis-Magallanes, 1990).
HARVEST SEASON The principal harvest season is from January to June in both Mexico and South America, with another in September to December. The fruits from both seasons can be distinguished by the size. In the first season, the fruits are relatively smaller (2.54.1 cm in length), and in the second one it is possible to find fruits up to 5 cm in length (Vargas-Simo´n et al., 2011; Avitia et al., 2000; Hoyos, 1994). The fruit takes approximately 6 months from its formation until is ready for harvesting (Baraona and Rivera, 1995).
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FIGURE 3 (A) Spondias purpurea fruit showing mesocarp and endocarp, (B) Fruit: ecotypes ‘yellow’ and ‘red’ collected in Oaxaca, Mexico, (C) ecotype ‘yellow’ collected in Oaxaca, Me´xico, (D) ecotype ‘purple’, collected in Tabasco, Me´xico.
ESTIMATED ANNUAL PRODUCTION The cultivation of this species varies depends on the zone. In Mexico, there is 15,160.92 ha of crop with a 7 Mg/year production (SIAP, 2014). In Brazil, the annual production is 69 Mg/year (Lima, 2009); Venezuela and El Salvador produce 2 Mg/year (Vanegas, 2005; Avilan et al., 1989), with an average yield of 3.2505.137 Mg/ha (SIAP, 2014; Pe´rez-Arias et al., 2008; Cordero and Boshier, 2003). The production per tree depends on the variety. Ranges have been reported from 5.96 to 17.62 kg/tree in selected clones like IPA-4 and IPA-6 from Pernambuco, Brazil, respectively (Ju´nior et al., 2014).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The epicarp of the fruits shows a range of colors, which includes yellow, yellowish red, coppery red, dark red, deep red, reddish yellow, orange and yellowish green. Pe´rez-Arias et al. (2008) determined that red-colored fruits had a shade between 22.2 and 33.7; the orange-colored, 58.9; and the yellow-colored, between 73 and 91.7. The chromaticity ranges were about 23.54 and 45.35 and the shade ranges were between 22.2 and 91.69; the yellow-colored fruits the ones that reflect the highest values for these two characteristics. The firmness, depending on the ripeness stage and ecotype, can vary between 1.23 and 3.42 N. The highest values found corresponded to the fruits with the highest epicarp weight. This data was described in ecotypes from Guerrero, Mexico (Pe´rez-Arias et al., 2008). Sampaio et al. (2008) classifies the fruits of S. purpurea as climacteric. A maximum CO2 liberation 111.8 mL/kg per h and O2 absorption 124.2 mL/kg per h occurred at 140 and 130 h, respectively. Another study carried out in harvested fruits in Oaxaca, Mexico determined that respiration rate and ethylene did not experimented significant changes in any of the three stages of ripeness evaluated (unripe, 50% of epicarp reddish yellow-colored and 75% of epicarp reddish yellow-colored) (Pe´rez et al., 2004). These differences between Brazilian and Mexican fruits may be attributed to the difference in variety and climate (Sampaio et al., 2008). The disappearance of chlorophyll in the epicarp starts in the preclimacteric stage. Subsequently, it turns yellowish-orange during the climacteric peak. It keeps that color until the end of the climacteric stage while the carotene level increases. This corresponds with the total soluble solids increased from 7.70 Brix (initial) to 15.70 Brix (postclimacteric stage) during maturation. In this same
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145
study, it was possible to observe that the ascorbic acid content of red mombin decreased during ripening and the difference among the stages of ripeness was significant (Sampaio et al., 2008).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING, VITAMINS, MINERAL, PHENOLIC, ANTIOXIDANT COMPOUNDS, AND SENSORY CHARACTERISTICS Table 1 shows the chemical composition of red mombin fruits, though it should be noted that those values differ according to the variety, genotype (wild or cultivated) and the stage of ripeness in which the analyses were done. Studies from Ecuador, Brazil and Mexico (varieties from central and west area) showed that this species is an important source of vitamins and minerals. One of the most important polysaccharide detected is pectin. In average, the content of total pectin in ripe fruits of S. purpurea is 1.73%3.24% (Maldonado-Astudillo et al., 2014). The red mombin stands out for the great quantity of volatile compounds (Tables 2 and 3). Ceva-Antunes et al. (2006) mentions that this species shows a different range of compounds, in which the esters and aldehydes predominate. This is a special characteristic of this species because in other tropical fruits, the terpenic hydrocarbons are the principal constituents. Table 2 shows the relation between these compounds and the flavor. Table 3 shows other volatile compounds of which there is no flavor record. Augusto et al. (2000) identified 27 substances in this species, including isoamyl alcohol, caproic aldehyde, nonyl aldehyde and decyl aldehyde. Correspondingly, Tadisco et al. (2014) also detected the presence of hexane, 2,3-pentanedione, 3,3-dimethyl pentane, cyclohexane, 2-methyl-butanol, 3,4-dimethyl-pentanol, 1-penten-3-ol, 2-penten1-ol, 2,3-butanediol, 5-hexen,2-one, 4 pentenal, ethyl 2-methylbutanoate, 2,6-dimethyl-1-heptene, α-muurolene, pentadecane, and α-bisabolol in fresh fruits. Maldonado-Astudillo et al. (2014) show different studies about the quantity of total phenolic compounds in ripe fruits. These studies have been done in both Mexico and Brazil, reporting values from 1 to 869 mg/100 g. Silva et al. (2012) emphasize the particularity of the genotype IPA-10 in which the highest average concentration of phenol was obtained (862.31 mg/g). These compounds showed a strong antioxidant capacity by performing a sequestration of DPPH (1,1difenil-2-picrilhidrazil) radicals and ABTS11 (2,20 -azino-bis-3-etilbenzotiazoline-6-sulfonic acid) of up to 70%. Omena et al. (2012) reported similar results in epicarp and seeds with an acetylcholinesterase inhibition assay with chlorogenic acid, one of the main constituents of red mombin seeds, revealing that this acid showed activity similar to that of the control physostigmine. Furthermore, is an antocianines source, 1.35 mg/100 g in average (epicarp and mesocarp) (Almeida et al., 2011). Additionally, the wine produced from this fruit contains phenolic compounds like catechins and epicatechins: 9.97 and 4.38 mg/L, respectively. Engels et al. (2012) identified 32 phenolic compounds in the epicarp of the fruit, including flavonols like galloyl glucose, gallic acid, 3-caffeoylquinic acid, dihydroxybenzoic acid hexoside, diferentes quercetin, kaempferol, rhamnetin, isorhamnetin and kaempferide. These phenolic compounds play an important role in human health, because an uncontrolled production of oxygen-derived from free radicals is involved in the onset of many diseases such as cancer, rheumatoid arthritis, among others (Ramalho et al., 2014; Almeida et al., 2011). Another characteristic of red mombin is its total dietary fiber content, the epicarp contains 43.9 6 3.7 (dry basis/100 g). Fiber is important for reducing cholesterol and glucose, apart from benefit intestinal flora growth (Pire et al., 2010). These authors found a SDF/IDF relation (soluble fractions/insoluble fractions) equal or approximate to 0.5, affirming that this value is acceptable when this fruit is used as a feed additive.
HARVEST AND POSTHARVEST CONSERVATION In general, the fruits of red mombin have a short shelf life. If they are harvested ripe, the shelf life is low (1 day). However, if they have a slightly green tone, they can remain up to 3 days at ambient temperature (Pe´rez et al., 2004) or they can be refrigerated at 13 C with an 85%90% relative humidity (RH). If they are stored at a temperature below 10 6 2 C there can be some damage to the fruit, irrespective of the stage of maturity (Vanegas, 2005). Among the variables that get affected by storage time is the weight loss, which can vary between 7.6% and 8.8% in 2 days of storage at 20 C (Pe´rez et al., 2004). In this same study, the authors concluded that the ideal moment of harvest is when fruits in the tree reach 50% of yellowish or reddish coloring on the surface. This means that they will obtain an acceptable quality for postharvest consumption and a greater storage life. A chemical method for extending the shelf life is with the application of 1-Metilciclopropene (1-MCP) and with this treatment, the storage life of the fruits can be extended up to 3 days when it is applied to unripe fruits. The 1-MCP decrease with the respiration and weight loss and it does not affect total soluble solids (Osuna et al., 2011). This has also been proven with the epicarp coverage with galactomannans obtained from Caesalpinia pulcherrima (0.5% and
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TABLE 1 Chemical Composition of Red Mombin (Spondias purpurea), per 100 g Edible Portion Component
Unit
Average
Moisture
g
77.6a; 86.9%c
Protein
g
0.7a; 0.23b; 0.80c
Fat
g
0.2a; 0.4c
Fiber
g
0.5a; 1.7c
Minerals (ash)
g
0.7a
Total carbohydrates
g
19.1a; 11.8c
Food energy
kcal
74a
Starch
g
2.47a
Pectins
g
0.22a
Fructose
g
2.53a
Glucose
g
2.00a
Reducing sugars
g
8.08a; 0.36b
Sucrose
g
6.59a
Nitrogen
mg
7.11b
Calcium
mg
17a; 3.5b; 15.0c
Phosphorus
mg
42a; 2.0b
Iron
mg
0.72a; 3.68b; 0.80c
Sodium
mg
6a
Potassium
mg
250a; 8.05b
Magnesium
mg
3.3b; 9.0c
Copper
mg
0.69b
Manganese
mg
0.33b
Zinc
μg
20a; 1.28b
Carotene
μg
119a
Thiamine
μg
84a; 50c
Riboflavin
μg
40a; 30c
Retinol
μg
11c
Niacin
mg
1.0a; 0.9c
Ascorbic acid
mg
49a; 12c; 7.3688.1d
Piridoxina
mg
0.2c
pH
3.29a; 3.3b; 2.56.0d
18a; 11.7b; 3.225.9d
Brix
Citric acid
mg
30a
Malic acid
mg
110a
Oxalic acid
mg
30a
Tartaric acid
mg
20a
a
Koziol and Macı´a (1998). Ramı´rez Hernandez et al. (2008). c Mun˜oz et al. (1999). d Maldonado-Astudillo et al. (2014). b
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TABLE 2 Volatile Flavor Compounds Identified in Red Mombin (Spondias purpurea) Compound
Abundance (%)
Flavor
6.95a; 10.6b
Fatty, green grass-like (tallow)
Aldehydes Hexanal 2-Hexenal Trans-2-hexenal
a
Green, fruity, vegetable-like (apple)
38.99 b
(Green, leaf)
5
a
b
2-Heptenal
0.07 ; 0.5
Pungent green, somewhat fatty odor, pleasant only on extreme dilution
Phenylacetaldehyde
0.04a
Pungent green, floral, sweet, wallflowers-like
2,4-Heptadienal
a
0.08
Rotten apple, rancid, hazelnut
2b
(Fruit, herb)
Esters Hexyl acetate 3-Methylbutyl acetate Ethyl acetate
a
Fruity, pear-like, banana-like
0.22 b
Pineapple, fruit
8.4
a
b
Methyl benzoate
0.76 ; 0.3
Ethyl hexanoate
a
0.89
Fruity, floral, wine-like; powerful fruity with pineapple-banana note
3-Hexen-1-ol acetate
0.88a
(Grass, moss, fresh)
Ethyl benzoate Ethyl octanoate Ethyl decanoate Ethyl dodecanoate Ethyl tetradecanoate
Fruity, similar to cananga
a
Blackcurrant-like
a
Apricot-like, banana-like, wine-like
a
Floral, sweet, oily nut-like, brandy-like
a
Faint fruity, flower petal-like, slightly mango-like
a
0.66
Oily, ethereal, violet-like, orris-like
5.0b
(Leaf, green, wine, fruit)
0.21 0.45 0.47 0.55
Simple Alcohols and Ketones 2-Hexen-1-ol Monoterpene Hydrocarbons Trans β-ocimene α-Pinene Linalool oxide α-Terpinolene
0.03a; 0.1b
Warm, herbaceous
a
Floral, warm, resinous, pine, cedar-wood like
a
Sweet, woody, floral, earthy
a
Floral, sweet, pine-like
0.12 0.40
1.19
Sesquiterpene Hydrocarbons Tetradecanoic acid Hexadecanoic acid
3.07a
Faint waxy, oily a
18.51
Virtually odorless
a Koziol and Macı´a (1998). Values for “abundance” are the percentages of the area of the total ion chromatagram represented by the peaks of each of the compounds identified. b Ceva-Antunes et al. (2006), (based on frozen pulp).
1.5% of glycerol). This formulation is mostly applied as immersion or spray-drying at ambient temperature for 3 days (Cerqueira et al., 2009). In a fruit drying process experiment with the spray-drying method, it was observed that most of the volatile compounds were being conserved. This means that this process can be a useful way to conserve the original flavor and transport the fruits across relatively long distances because this experiment was carried out 100 days after the harvest (Tadisco et al., 2014). The sugar content in red mombin consists of fructose, glucose, and sucrose. These soluble solids are the main chemical products that contribute to suppress the water activity of the fruit powder (Guerrero-Beltra´n et al., 2015).
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TABLE 3 Other Volatile Compounds Identified in Red Mombin (Spondias purpurea) Compound
Abundance (%)
Heptanal
1.0a
2,4-Hexadienal
0.1a
Benzaldehyde
0.1a
4-Penten-lyl-acetate
1.29b
Ethyl tiglate
1.0a
Butyl butyrate
0.2a
Ethyl caproate
Tracesb (,0.1)
Propyl tiglate
0.1a
n-Butyl tiglate
0.1a
Methyl 2-hydroxybenzoate
0.49b; 0.1a
3-Methyl-2-buten-1-1-ol acetate
1.30b
Ethyl 2-methyl but-2-enoate
0.19b
Methyl 4-pyridenacarboxylate (methyl isonicotinate)
0.05b
Acetophenone
0.1a
3-Hexen-1-ol
6.8a
Hexanol
1.0a
1-Octen 3-ol
0.4a
Ethyl vinyl ketone
0.5a
(E)-Caryophyllene
0.1a
Aromadendrene
Tracesb (,0.1)
α-Humelene
Tracesb (,0.1)
Limonene
0.2b
2,6,6-Trimethyl-2-ethylene tetrahydro-2H-pyran
0.20b
3-Ethyl-5-methyl-1-propyl-cyclohexane
0.26b
1,1,6-Trimethyl-1,2-dihydronaphthalene
0.11b
1,2-Benzenedicarboxylic acid
0.52b
a
Ceva-Antunes et al. (2006), (based on frozen pulp). Koziol and Macı´a (1998). Values for “abundance” are the percentages of the area of the total ion chromatagram represented by the peaks of each of the compounds identified. b
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION In order to increase the added value of the fruit, it is common to create products such as jams or candies. Proportions such as 40:60 or 50:50 (fruit/sugar) haven well accepted by consumers. These proportions are pathogen- and microorganism-free (Silva and Meleiro, 2012). As a food supplement, it has been proven that adding red mombin syrup to Mozzarella cheese has been well accepted by consumers. The most accepted formulation was 30% sucrose and with this, the authors affirm an improvement in flavor, color, texture, and presentation characteristics of the product (Acevedo and Garcı´a, 2012). This species is characterized for containing clear consistency gums soluble in water, it contains galactose (59%), arabinose (9%), mannose (2%), xylose (2%), rhamnose (2%) and uronic acid residues (26%) (Martı´nez et al., 2008). Gutie´rrez et al. (2005) found purified acidic polysaccharide isolated from gum of S. purpurea (yellow form), which contains galactosyl, arabinosyl, xylosyl, rhamnosyl, and uronic acid residues. In the same way, an analysis of tree exudate
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149
polysaccharide identified protein material (1-3) linked galactan backbone substituted at C6 with D-galactose, D-xylose, L-arabinose, L-rhamnose and glucuronic acid units. Gums, in general, have a great use in the alimentary industry as a base for producing icecream and yogurt. Brazilian polysaccharides differs from Venezuelan types by the amount of acid and arabinose as well as the presence of fructose and glucose as a minor sugar. The D-galactose substitution (1-6) confers to the polysaccharide with the peculiar capacity of binding a-D-galactose specific lectins after crosslinking with epichlorohydrin. The gel obtained was able to specifically retain D-galactose-binding-lectins. This confers a great usefulness for biochemical process of agglutination (Texeira et al., 2007). The leaf extract of S. purpurea contains different oxygenated sesquiterpenoic oils (72.2%) which have a strong larvicidal activity against Aedes aegypti that includes caryophyllene oxide (22.9%), α-cadinol (22.9%) and epi-α-muurolol (11.8%), among others (Lima et al., 2011). The hexanic extract of the leaves contains promissory antimicrobial properties against Bacillus cereus ATCC 11778, a bacterium that causes intestinal infections (Miranda-Cruz et al., 2012). The endocarp, seminal coat, and seed have an important amount of cellulose, useful for phosphate ions flocculation from wastewaters. The thermodynamic parameters evaluated indicated that the adsorption of phosphate ions were feasible, spontaneous, and endothermic at 2580 C (Arshadi et al., 2015). According to its rheological properties, it has been demonstrated that the frozen flesh acts like a weak gel with storage modulus higher than loss modulus in the evaluated frequency range; a power modified CoxMerz rule could describe the rheological properties of S. purpurea pulp (R2 . 0.96) (Augusto et al., 2012). The organic waste capacity of the fruits of S. purpurea for lipase production in solid-state processes using Lichtheimia ramosa fungus were successful. Protein enrichment was obtained from all media, the most superior obtained 391.66%. Lipase production was around 0.41 U/g (Silva et al., 2014). Another agroindustrial use for the waste of this species is the cellulolytic enzymes production (cellulases and hemicellulases) by solid fermentation with Aspergillus niger, which are used in the alimentary industry for the fruit juice extraction and clarification (Santos et al., 2013).
Propagation As S. purpurea is limited in its sexual reproduction, is commonly propagated vegetatively via cuttings about 610 cm in diameter and 50150 cm length. They are cut before the leaves shoot so the rooting takes place when the rainy season begins. The cuttings are kept in the shade for a couple of weeks and are planted at 30 cm depth. This way, the plants start fruiting just 2 years after being planted (Campos and Espı´ndola, 2007; Baraona and Rivera, 1995). Grafts can be another way of propagation using side veneer or English style grafting, using as a pattern the wild plum or the same variety propagated by cuttings (Campos and Espı´ndola, 2007). Spondias tuberosa has obtained a success rate over 85% with buds of 11.5 cm long (Lima Filho and Santos, 2009). The cuttings should be first planted in nursery bags in an almost vertical position, just slightly leaned so at least two shoots keep underground (Avilan et al., 1989). For wild varieties, if being reproduced by seeds, Niembro et al. (2010) recommend collection when the fruits are entirely ripe. Then they are soaked in water for 12 h in order to detach the epicarp and flesh easily and finally are laid out for drying in a ventilated area. Seeds stored in hermetic containers are viable for 27 months at temperatures between 2 C and 5 C.
ACKNOWLEDGMENT Ing. Julio Moguel Yanez for help in translation, Dr. Ebenezer de Oliveira Silva for the invitation and Dr. Sueli Rodrigues for your attentions.
REFERENCES Acevedo, P.I.C., Garcı´a, O., 2012. Elaboracio´n y evaluacio´n de ciruela (Spondias purpurea L.) en almı´bar como rellenos en queso tipo Mozzarella de bu´fala (Bubalus bubalis). Rev. Cient. UDO Agrı´c. 12 (3), 720729. Albuquerque, U.P., Arau´jo, S.T.A., Ramos, M.A., Nascimento, V.T., de Lucena, R.F.P., Monteiro, J.M., et al., 2009. How ethnobotany can aid biodiversity conservation: reflections on investigations in the semi-arid region of NE Brazil. Biodivers. Conserv. 18 (1), 127150. Almeida, M.M.B., de Sousa, P.H.M., Arriaga, A.M.C., do Prado, G.M., Magalha˜es, C.E.C., Maia, G.A., et al., 2011. Bioactive compounds and antioxidant activity of fresh exotic fruits from northeastern Brazil. Food Res. Int. 44, 21552159. Alia-Tejacal, I., Astudillo-Maldonado, Y.I., Nu´n˜ez-Colı´n, C.A., Valdez-Aguilar, L.A., Bautista-Ban˜os, S., Garcı´a-Va´zquez, E., et al., 2012. Caracterizacio´n de frutos de ciruela mexicana (Spondias purpurea L.) del sur de Me´xico. Rev. Fitotec. Mex. 35 (SPE5), 2126. Arshadi, M., Foroughifard, S., Gholtash, J.E., Abbaspourrad, A., 2015. Preparation of iron nanoparticles-loaded Spondias purpurea seed waste as an excellent adsorbent for removal of phosphate from synthetic and natural waters. J. Colloid Interface Sci. 452, 6977. Augusto, F., Valente, A.L.P., Tada, E.S., Rivellino, S.R., 2000. Screening of Brazilian fruit aromas using solid-phase microextraction-gas chromatography-mass spectrometry. J. Chromatogr. A. 873, 117127.
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Augusto, P.E.D., Cristianini, M., Ibarz, A., 2012. Effect of temperature on dynamic and steady-state shear rheological properties de siriguela (Spondias purpurea L.) pulp. J. Food Eng. 108, 283289. Avilan, L., Leal, F., Bautista, D., 1989. Manual de fruticultura. Americana, Caracas, pp. 437441. Avitia, G.E., Castillo, A.M.G., Pimienta, E.B., 2000. Ciruela mexicana y otras especies del ge´nero Spondias L. Texcoco. Universidad Auto´noma Chapingo, Departamento de Fitotecnia, p. 63. Baraona, M., Rivera, G., 1995. Desarrollo del jocote (Spondias purpurea L.) y del cas (Psidium friedrichsthalianum (Berg.)Niedz) en el bosque hu´medo premontano de Costa rica. Agron. Mesoam. 6, 2331. Barbeau, G., Frutas tropicales en Nicaragua, 1990. Ministerio de Desarrollo Agropecuario y Reforma Agraria, Direccio´n General de Te´cnicas Agropecuarias, Managua. Benjamin, T.J., Montan˜ez, P.I., Jime´nez, J.J.M., Gillespie, A.R., 2001. Carbon, water and nutrient flux in Maya homegardens in the Yucata´n peninsula of Me´xico. Agroforestry Syst. 53, 103111. Borchert, R., 1994. Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology. 75 (5), 14371449. Bullock, S.H., Solis-Magallanes, J.A., 1990. Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica. 22 (1), 2235. Campos, R.E., Espı´ndola, M.C.B., 2007. Ciruela mexicana. Fundacio´n Salvador Sa´nchez Colı´n CICTAMEX, S.C, Coatepec Harinas, 14 pp. Ca´rdenas, L.D., Ramı´rez, J.G.A., 2004. Plantas u´tiles y su incorporacio´n a los sistemas productivos del departamento del Guiaviare (Amazonia colombiana). Caldasia 26 (1), 95110. Cerqueira, M.A., Lima, A.M., Teixeira, J.A., Moreira, R.A., Vicente, A.A., 2009. Suitability of novel galactomannans as edible coatings for tropical fruits. J. Food Eng. 94, 372378. Ceva-Antunes, P.M.N., Bizzo, H.R., Silva, A.S., Carvalho, C.P.S., Antunes, O.A.C., 2006. Analysis of volatile composition of siriguela (Spondias purpurea L.) by solid phase microextraction (SPME). LWT-Food Sci. Technol. 39 (4), 437443. ´ rboles de Centroame´rica, 2003, Oxford Forestry Institute, Centro Agrono´mico Tropical de Investigacio´n y Cordero, J. and Boshier D.H. (Eds), A Ensen˜anza, Turrialba. Cuevas, J.A., 1992. Jocote, ciruelo. In: Herna´ndez Bermejo, J.E., Leo´n, J. (Eds.), Cultivos marginados, otra perspectiva de 1492.. FAO, Roma, p. 110. Engels, C., Gra¨ter, D., Esquivel, P., Jime´nez, V.M., Ga¨nzle, M.G., Schieber, A., et al., 2012. Characterization of phenolic compounds in jocote (Spondias purpurea L.) peels by ultra high-performance liquid chromatography/electrospray ionization mass spectrometry. Food Res. Int. 46, 557562. Gonza´lez-Garcı´a, A., Belliure, J., Go´mez-Sal, A., Da´vila, P., 2009. The role of urban greenspace in fauna conservation: the case of the iguana Ctenosaura similis in the ‘patios’ of Leo´n city, Nicaragua. Biodivers. Conserv. 18, 19091920. Guerrero, R., Manzanilla, M., Herna´ndez, C., Chacı´n, J., Clamens, C., 2011. Caracterizacio´n fisicoquı´mica de frutos de ciruelo de huesito (Spondias purpurea L.) en el municipio Mara. Rev. Fac. Agron. (LUZ) 28 (suppl. 1), 670676. Guerrero-Beltra´n, J.A., Ruiz-Herna´ndez, F., Welti-Chanes, J., 2015. Mexican plum (Spondias purpurea L.) moisture sorption properties. In: Gutie´rrezLo´pez, G.F., et al., (Eds.), Water Stress in Biological, Chemical, Pharmaceutical and Food Systems. Springer Science 1 Business Media, New York, NY, p. 329. Available from: http://dx.doi.org/10.1007/978-1-4939-2578-0_25. Gutie´rrez, G.O., Martı´nez, M., Sanabria, L., Leo´n de, P.G., Igartuburu, J.M., 2005. ID- and 2D-NMR spectroscopy studies of the polysaccharide gum from Spondias purpurea var. lutea. Food Hydrocolloids 19, 3743. Hopkins, A.L., Stepp, J.R., 2012. Distribution of herbal remedy knowledge in Tabi, Yucatan, Mexico. Econ. Bot. 66 (3), 249254. Hoyos, J., 1994. Frutales en Venezuela. Sociedad de Ciencias Naturales La Salle, Caracas, p. 33. Janzen, D.H., 1982. Ecological distribution of chlorophyllous developing embryos among perennial plants in a Tropical Decidous Forest. Biotropica. 14 (3), 232236. Kozioł, M.J., Macı´a, M.J., 1998. Chemical composition, nutritional evaluation, and economic prospects of Spondias purpurea (Anacardiaceae). Econ. Bot. 52 (4), 373380. Lima, I.C.G.S., 2009. Seriguela (Spondias purpurea L.): propiedades fisico-quı´micas e desenvolvimento de gele´ia de doce de corte e aceitabilidade desses productos. Tesis grau de Mestre em Cieˆncias. Universidade Federal Rural do Rio de Janeiro. Instituto de Tecnologia. Serope´dica, 87 pp. Lima, M.A.A., de Oliveira, F.F.M., Gomes, G.A., Lavor, P.L., Santiago, G.M.P., Nagao-Dias, A.T., et al., 2011. Evaluation of larvicidal activity of the essential oils of plants species from Brazil against Aedes aegypti (Diptera: Culicidae). Afr. J. Biotechnol. 10 (55), 1171611720. Lima Filho, P.J.M., Santos, C.A.F., 2009. Avaliac¸o˜es fenotı´picas e fisiolo´gicas de espe´cies de Spondias tendo como porta enxerto o umbuzeiro (Spondias tuberosa Cam.). Rev. Caatinga. 22 (1), 5963. Lozano, A., Araujo, E.L., Medeiros, M.F.T., Albuquerque, U.P., 2014. The apparency hypothesis applied to a local pharmacopoeia in the Brazilian northeast. J. Ethnobiol. Ethnomed. 10, 2, URL: ,http://www.ethnobiomed.com/cont/10/1/2.. Maldonado, M.F., Vargas-Simo´n, G., Molina, R.F.M., Sol, A.S., 2004. Frutales Tropicales de Tabasco. Instituto para el Desarrollo de Sistemas de Produccio´n del Tro´pico Hu´medo de Tabasco-Universidad Jua´rez Auto´noma de Tabasco, Villahermosa, 137 pp. Maldonado-Astudillo, Y.I., Alia-Tejacal, I., Nu´n˜ez-Colı´n, C.A., Jime´nez-Herna´ndez, J., Pelayo-Zaldı´var, C., Lo´pez-Martı´nez, V., et al., 2014. Postharvest physiology and technology of Spondias purpurea L. and S. mombin L. Sci. Hortic. 174, 193206. Martı´nez, M., de Pinto, G.L., de Gonza´lez, M.B., Herrera, J., Oulyadi, H., Guilhaudis, L., 2008. New structural features of Spondias purpurea gum exudate. Food Hydrocol. 22 (7), 13101314. Me´ndez-Toribio, M., Gonza´lez-Di Pierro, A.M., Quesada, M., Benı´tez-Malvido, J., 2014. Regeneration beneath a dioecious tree species (Spondias purpurea) in a Mexican tropical dry forest. J. Trop. Ecol. 30, 265268.
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151
Miller, A.J., 2008. Characterization of a domesticated tree lineage (Spondias purpurea, Anacardiaceae) based on nuclear and chloroplast sequence data. J. Torrey Bot. Soc. 135 (4), 463474. Miller, A.J., Knouft, J.H., 2006. GIS-Based characterization of the geographic distributions of wild and cultivated populations of the Mesoamerican fruit tree Spondias purpurea (Anacardiaceae). Am. J. Bot. 93 (2), 17571767. Miranda-Cruz, E., Espinosa-Moreno, J., Centurio´n-Hidalgo, D., Vela´zquez-Martı´nez, J.R., Alor-Cha´vez, M.J., 2012. Actividad antimicrobiana de extractos de Psidium friedrichsthalianum L., Pterocarpus hayesii L., Tynanthus guatemalensis L. y Spondias purpurea L. Bol. Latinoam. Caribe Plant. Med. Aroma´t. 11 (4), 354361. Morton, J., 1987. Purple mombin (Spondias purpurea L.). Fruits of Warm Climates. J.F. Morton, Miami, FL, pp. 242245. Mun˜oz de Ch, M., Cha´vez, A.V., Roldan, J.A.A., Ledesma, J.A.S., Mendoza, E.M., Pe´rez-Gil, F.R., et al., 1999. Tabla de valor nutritivo de los alimentos de mayor consumo en Latinoame´rica. Internacional, Me´xico, 109 pp. ´ rboles de Veracruz, 100 especies para la reforestacio´n estrate´gica. Comisio´n Organizadora del Niembro, R.A., Va´zquez, M.T., Sa´nchez, O.S., 2010. A Estado de Veracruz de Ignacio de la Llave para la Conmemoracio´n del Bicentenario de la Independencia Nacional y del Centenario de la Revolucio´n Mexicana/Secretarı´a de Educacio´n-Gobierno del Estado de Veracruz, Xalapa, pp. 202204. Omena, C.M.B., Calentim, I.B., Guedes, GdaS., Rabelo, L.A., Mano, A.G.F., Bechara, E.J.H., et al., 2012. Antioxidant, anti-acetylcholinesterase and cytotoxic activities of etanol extracts of peel, pulp and sedes of exotic Brazilian fruits. Food Res. Int. 49, 334344. Osuna Garcia, J.A., Pe´rez Barraza, M., Va´zquez Valdivia, V., Go´mez Jaimez, R., 2011. Aplicacio´n de 1-metilciclopropeno (1-MCP) y su efecto en ciruela mexicana (Spondias purpurea L.). Rev. Fitotec. Mex. 34 (3), 197204. Pennigton T.D. and J. Sarukha´n, Guı´a para la identificacio´n de a´rboles tropicales de Me´xico, 2005, UNAM, Me´xico, D. F. Pe´rez Lopex, A., Saucedo Veloz, C., Are´valo Galarza, M.D.L., Muratalla Lua, A., 2004. Efecto del grado de madurez en la calidad y vida postcosecha de ciruela mexicana (Spondias purpurea L.). Rev. Fitotec. Mex. 27 (2), 133139. Pe´rez-Arias, G.A., Alia-Tejacal, I., Andrade-Rodrı´guez, M., Lo´pez-Martı´nez, V., Pe´rez-Lopez, A., Ariza-Flores, R., et al., 2008. Caracterı´sticas fı´sicas y quı´micas de ciruelas mexicana (Spondias purpurea) en Guerrero. Inv. Agropec. 5, 141149. Pire, S.M.C., Garrido, E., Gonza´lez, H., Pe´rez, H., 2010. Estudio comparativo del aporte de fibra alimentaria en cuatro tipos de frutas de consumo comu´n en Venezuela. Interciencia. 35 (12), 939944. Querejeta, J.I., Estrada-Medina, H., Allen, M.F., Jime´nez-Osornio, J.J., 2007. Water source partitioning among trees growing on shallow karst soils in a seasonally dry tropical climate. Oecologia. 152 (1), 2636. Ramalho, S.A., Gualberto, N.C., Neta, M.T.S.L., Batista, R.A., Arau´jo, S.M., da Silveira Moreira, J.D.J., et al., 2014. Catechin and epicatechin contents in wines obtained from Brazilian exotic tropical fruits. Food Nutr. Sci. 5 (5), 449457. Ramı´rez Hernandez, B.C., Barrios Eulogio, P., Castellanos Ramos, J.Z., Mun˜oz Urias, A., Palomino Hasbach, G., Pimienta Barrios, E., 2008. Sistemas de produccio´n de Spondias purpurea (Anacardiaceae) en el centro-occidente de Me´xico. Rev. Biol. Trop. 56 (2), 675687. Sampaio, A.S., Bora, P.S., Holschuh, H.J., 2008. Postharvest respiration and maturation of some lesser-known exotic fruits from Brazilciriguela (Spondias purpurea L.). Rev. Ceres. 55 (2), 141145. Santos, T.C., Filho, G.A., Oliveira, A.C., Rocha, T.J.O., Machado, F.P.P., Bonomo, R.C.F., et al., 2013. Application of response surface methodology for producing cellulolytic enzymes by solid-state fermentation from the purple mombin (Spondias purpurea L.) residue. Food Sci. Biotechnol. 22 (1), 17. SIAP (Servicio de Informacio´n Agroalimentaria y Pesquera), 2014. Anuario Estadı´stico de la Produccio´n Agrı´cola. URL: ,http://www.siap.gob.mx/ cierre-de-la-produccion-agricola-por-cultivo/.. Fecha de consulta: 9 de agosto, 2015. Silva, C.A.A., Lacerda, M.P.F., Leite, R.S.R., Fonseca, G.G., 2014. Physiology of Lichtheimia ramosa obtained by solid-state bioprocess using fruit wastes as substrate. Bioprocess Biosyst. Eng. 37, 727734. Silva, Q.J., Moreira, A.C.C.G., Melo, E.A., Lima, V.L.A.G., 2012. Compostos feno´licos e atividade antioxidante de geno´tipos de ciriguela (Spondias purpurea L.). Aliment. Nutr. Araraquara. 23 (1), 7380. Standley, P.C., Steyermark, J.A., 1949. Flora de Guatemala. Fieldiana: Botany, Vol. 24, Part VI Chicago. Natural History Museum, Chicago, IL, p. 193. Tadisco, M.K., Castro-Alves, V.C., Garruti, D.S., da Costa, J.M.C., Clemente, E., 2014. The use of headspace solid-phase microextraction (HSSPME) to assess the quality and stability of fruit products: an example using red mombin pulp (Spondias purpurea L.). Molecules 19 (10), 1685116860. Texeira, D.M., Braga, R.C., Horta, A.C., Moreira, R.A., de Brito, A.C., Maciel, J.S., et al., 2007. Spondias purpurea exudate polysaccharide as affinity matrix for the isolation of a galactose-binding-lectin. Carbohydr. Polym. 70 (4), 369377. Vanegas, M.J., 2005. Guı´a te´cnica del cultivo del jocote. IICA, MAG FRUTAL ES, Santa Tecla, 26 pp. Vargas-Simo´n, G., Gama, L., 2010. Caracterı´sticas geogra´ficas y ecolo´gicas en la distribucio´n del frutal Spondias purpurea L. en Mexico. In: 61 Congreso Agrono´mico de Chile, 56th ISTH Annual Meeting, 11 Congreso de la Sociedad Chilena de Fruticultura. 26 a 29 septiembre, 2010. Santiago de Chile. Vargas-Simo´n, G., Herna´ndez-Cupil, R., Moguel-Ordon˜ez, E., 2011. Caracterizacio´n morfolo´gica de ciruela (Spondias purpurea L.) en tres municipios del estado de Tabasco, Me´xico. Bioagro. 23 (2), 141149. Wehncke, E.V., Numa, C.V., Domı´nguez, C.A., 2004. Seed dispersal and defecation patterns of Cebus capucinus and Alouatta palliate: consequences for seed dispersal effectiveness. J. Trop. Ecol. 20, 535543. Zizumbo-Villarreal, D., Flores-Silva, A., Colunga-Garcı´a, P.M., 2012. The archaic diet in Mesoamerica: incentive for milpa development and species domestication. Econ. Bot. 66 (4), 328343.
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FURTHER READING Lima, I.C.G.S., Meleiro, C.H.A., 2012. Desenvolvimento, avaliac¸a¯ fı´sico-quı´mica e sensorial de geleia e doce de corte de seriguela (Spondias purpurea L.) visando o crescimento da cadeia produtiva do fruto. B. CEPPA. Curitiba. 30 (2), 221232. Lira, J.J.S., Bezerra, J.E.F., de Moura, R.J.M., dos Santos, V.F., 2014. Repetibilidad da produc¸a¯ o, nu´mero e peso de fruto em cirigueleira (Spondias purpurea L.). Rev. Bras. Frutic. 36 (1), 214220.
Cocona—Solanum sessiliflorum Pedro Jime´nez Universidad Militar Nueva Granada, Bogota´, Colombia
Chapter Outline Introduction Origin, Distribution, and Morphology Fruit Composition Agronomical Aspects
153 153 155 156
Pests and Diseases Uses and Perspectives Conclusions References
157 157 158 158
INTRODUCTION The botanical family Solanaceae includes several genera used by mankind for different purposes. Among these genera the most popular genus is Solanum, which includes species globally consumed such as S. lycopersicum L. (tomato) and S. tuberosum L. (potato). Also in this genus some less known, but increasingly popular, fruits are already used by ancient South American civilizations and their descendants such as Solanum betaceum (tamarillo), Solanum muricatum Alt. (pepino or melon shrub), Solanum quitoense Lam. (naranjilla or lulo), and more recently Solanum sessiliflorum Dunal (Morton, 1987; Silva Filho, 1998; Lim, 2013; Duarte and Paull, 2015). This last species has many vernacular names (Lim, 2013), but is usually named cocona, Orinoco apple, or peach tomato in English, cocona or tupiro in Spanish, and cubiu´ or mana´-cubiu in Portuguese (Morton, 1987; Silva Filho, 1998; Lim, 2013; Duarte and Paull, 2015). The latter, S. sessiliflorum, is an Amazonic fruit which has been used traditionally by people of the upper Amazon and Orinoco basins, including actual territories of Brazil, Colombia, Ecuador, Peru´, and Venezuela, even before the European arrival to South America (Silva Filho, 1998; Volpato et al., 2004; Duarte, 2011; Duarte and Paull, 2015). However, its domestication and industrialization processes has been very slow. In the last 30 years the characteristics of this species have been discussed and explained by different authors (Morton, 1987; Silva Filho, 1998; Duarte, 2011; Lim, 2013; Duarte and Paull, 2015). Particularly frequent are references related to its potential uses in the food industry as jelly, juices, marmalades, and also to its effects on human health. Lately, some interest has emerged for exploring those effects on improving human health, particularly controlling high blood pressure, reducing sugar and cholesterol levels in blood, and overall effect on wellness (Silva Filho et al., 2003; Pardo Sandoval, 2004, 2010). Also, the composition of the fruits has been explored, not only in terms of nutrient contents but also in terms of the secondary metabolite production (Marx et al., 1998; Quijano and Pino, 2006; Cardona et al., 2011; Lim, 2013).
ORIGIN, DISTRIBUTION, AND MORPHOLOGY The center of origin of this species is the upper Amazon region, which includes from the Eastern foothills of the Andes to the upper Orinoco river basin (Silva Filho, 1998; Volpato et al., 2004; Duarte, 2011; Duarte and Paull, 2015). At the Europeans’ arrival, this species was already cultivated in the area and the domestication process by Piaroa people, at upper Orinoco river, has been studied (Volpato et al., 2004; Duarte and Paull, 2015). In the middle of the past century, cocona was introduced in Central and North America and Caribbean areas: Costa Rica, Nicaragua, Honduras, Puerto Rico, and the United States of America (Florida), and also in South Africa, with differing degrees of success (Morton, 1987; Duarte and Paull, 2015). It is frequent to find descriptions of cocona plant presented by several authors (i.e. Morton, 1987; Silva Filho, 1998; Lim, 2013; Duarte and Paull, 2015), which slightly differ in dimensions of organs as leaves, flowers, and fruits. Additionally, a scale for identifying phenological stages for this species has been proposed by Moreno et al. (2016). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00020-4 © 2018 Elsevier Inc. All rights reserved.
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However, it seems to be agreed, among authors mentioned above, to describe the plant as an erect, herbaceous shrub, which at maturity becomes woody. Its stems and twigs are pubescent, being denser on later stages. Several branches emerge from the base of the trunk, and the plant can reach a height between 1 and 2 m (Fig. 1). The root system is well-ramified, not deeper than 5060 cm, and those plants propagated by seeds have a main pivotal root (Duarte, 2011; Duarte and Paull, 2015). Leaves are simple, alternate, and thin-textured. Base is asymmetrically truncated and apex varies from obtuse to acute, with variable margins including coarsely dentated, lobated, and sinuous, with trichomes on adaxial and abaxial sides. Two varieties are recognized, sessiliflorum and georgium. The former is spineless, while the last presents spines on branches and leaves. Lack of spines in sessiliflorum is probably a consequence of domestication processes (Volpato et al., 2004; Duarte and Paull, 2015). Flowers occur in axillary inflorescences, clustered in groups of 2 or more flowers (Lim (2013) mentions 616 and Duarte (2011) reports 515) with a short peduncle. A flower has five pale greenish-yellow petals and yellow stamens, and a five pointed campanulated calyx, which remains attached to the fruit even after harvested. The fruit is a berry with a high variability in form. This variability allows the identification of several ecotypes, being the most frequently occurring the globose, oblate, and conical-oval (Morton, 1987; Silva Filho, 1998; Duarte, 2011). The fruit is coated with fuzz, which is easily removed when fully ripeness is reached, showing a smooth, thin but tough skin (Fig. 2). Fruit color will change from green in immature stages to a different final color: golden-to orange-yellow,
FIGURE 1 Cocona plant architecture, with branches emerging from the base of the trunk, it is noticeable the form of leaves.
FIGURE 2 (A). Cluster of unmature fruits, covered by fuzz. (B). Ripe fruit, change of color is completed, and fuzz is almost totally disappeared. Campanulated calyx is noticeable.
Cocona—Solanum sessiliflorum
155
burnt-orange, red, red-brown, or deep purple red (Morton, 1987; Silva Filho, 1998; Duarte, 2011). Under this tough skin, a thick layer of hard cream-colored flesh is presented, enclosing four to six (Duarte, 2011) locular compartments containing the pulp. Pulp surrounds the seeds, and it has a jelly-like consistency, usually creamy-colored, slightly acidic, fragant with characteristic aroma and taste (Morton, 1987). Seed number is variable and ranges from 600 to 2000 seeds per fruit, however they are unnoticeable when the pulp is consumed (Morton, 1987; Duarte and Paull, 2015).
FRUIT COMPOSITION Several authors have made contributions regarding the composition of cocona and the results of some of these studies are presented in Table 1.
TABLE 1 Chemical Composition of Cocona (S. sessiliflorum) Component
Pahlen
Morton
Villachica
Marx et al. 90.5
Yuyama et al.
Humidity (g)
91.0
89.0
Energy (Kcal)
33.0
41.0
33.7
Protein (g)
0.6
0.6
0.9
0.5
Lipids (g)
1.4
Extract free of nitrogen (g)
5.7
Fiber (g)
0.4
0.2
1.6
Ashes (g)
0.9
0.7
0.6
90.5
3.15
Total sugars (%)
5.7
32.10
Reducing sugar (%)
25.4
No reducing sugars (%)
6.67
5.0
Citric acid Brix/acidity%
Tannins (mg)
125
Ascorbic acid (mg)
4.5
Niacin (mg)
2.5
0.5
2.3
Carotene (mg)
0.2
0.14
0.2
Thiamine (mg)
0.3
25.0
0.1
Riboflavin (mg)
0.1
Calcium (mg)
12.0
12.0
16.0
99.0
Magnesium (mg)
188.0
Phosporus (mg)
14.0
14.0
30.0
383.0
Potassium (mg)
356.40
Sodium (μgÞ
128.7
Cooper (μgÞ
Iron (μgÞ
0.6
2500.0
423.51
Zinc (μgÞ
1080.0
122.16
Magnesium (μgÞ
640.0
Soluble solids ( Brix) %
5.9
14.1
12.54
Source: From 100 g of pulp (von der Pahlen, A., 1977. Cubiu (Solanum topiro Humb. & Bonpl.), uma fruteira da Amazô nia. Acta Amazô nica, 7, 301307; Morton, J.F., 1987. Cocona. In: Fruits of warm climates. Julia F. Morton, Miami, pp. 428430; Villachica, H., 1996. Cocona (Solanum sessiliflorum Dunal). In: Frutales y hortalizas promisorios del Amazonas. Por Hugo Villachica. Lima, Peru´: Secretaria Pro-Tempore. Tratado de Cooperacio´n Amazo´nica. 102 pp, Villachica, 1996; Marx, F., Andrade, E.H.A., Maia, J.A.G., 1998. Chemical composition of the fruit of Solanum sessiliflorum. Zeitsch Lebensm Unters Forsch A 206, 364366; Yuyama, L.K.O., Macedo, S.H.M., Aguiar, J.P.L., Silva Filho, D., Yuyama, K., Fa´varo, D.I.T., et al., 2007. Quantificação de macro e micro nutrientes em algumas etnovariedades de cubiu (Solanum sessiliflorum Dunal). Acta Amazô nica, 37(3), 425430, Yuyama et al. 2007).
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Marx et al. (1998) also determined other compounds such as biogenic amines, fatty acids, free amino acids, special organic acids, and volatile compounds: G G
G
G G
Biogenic amines (mg per 100 g): ethanolamine 1.60, ornithine 3.20, and taurine traces. Fatty acids (g per 100 g): linoleic acid 0.16, linolenic acid 0.13, myristic acid 0.01, oleic acid 1.53, palmitic acid 1.00, palmitoleic acid 0.08, stearic acid 0.09, and tetracosanoic acid 0.01. Free amino acids (mg per 100 g): alanine 5.60, β-alanine 21.60, arginine 34.80, asparagine 366.80, aspartic acid 64.40, glutamic acid 74.80, glutamine 172.80, glycine 7.60, histidine 18.80, isoleucine 23.60, leucine 17.20, lysine 30.40, methionine 4.40, phenylalanine 60.80, proline 12.00, serine 321.00, threonine 22.80, tyrosine 7.60, valine 25.60, α-aminoadipic acid 0.40, γ-aminobutyric acid 298.00, α-aminobutyric acid 1.60, and hydroxylysine 2.00. Special organic acids (g per 100 g): citric acid 14.10, and malic acid 0.36. volatile compounds (relative peak area %): apiole 2.38, α-bisabolol 0.53, dodecanoic acid 0.58, dodecanone 0.87, 1-dodecanol 6.09, elemicin 0.65, eugenol 0.40, eugenol methyl ether 1.05, guaiazulene 3.51, (z)-3-hexen-1-ol 4.23, 1-hexanol 1.62, methyl salicylate 8.73, myristic acid 0.68, myristicin, 1.17, 1-nonanol 0.68, palmitic acid 18.20, phenylacetaldehyde 1.28, safrole 40.34, spathulenol 1.19, and undecane 0.39.
The composition of the volatile compounds in cocona has been studied by different authors and under different conditions. Quijano and Pino (2006) determined the composition of volatile compounds in pulp, during the ripening process at three stages of maturation: green, mature, and ripe. They reported 76 compounds: 40 from green fruits, 67 from mature, and 66 from ripe fruits. During maturation they found an increment in concentration of esters and alcohols, while concentration of carbonyl compounds decreased. Tough similar compounds were found in all of the stages, for ripe fruits the highest concentrations of methyl salicylate (0.85 mg/kg), α-terpineol (0.42 mg/kg), and (Z)-3-hexenol (0.26 mg/kg) were recorded. In opposition, the concentration of aldehydes, such as (Z)-3-hexenal (0.40 mg/kg), (Z)-2hexenal (0.35 mg/kg), (E)-2-hexenal (0.79 mg/kg), and hexanal (52 mg/kg) decreased along the maturation process. Cardona et al. (2011) compared the secondary metabolites profile in three different fruit morphotypes and reported chemical differences among them. The compounds reported as important by these authors were methyl salicylate, naringenin, p-coumaric acid, p-hydroxidihi- drocumaric acid, fatty acids, and their methyl and ethyl esters. Exploring the cocona composition of carotenoids and phenolic compounds, Rodrigues et al. (2013) found 17 carotenoids and 3 phenolic compounds. As a result, the major compounds were determined in each group, and for carotenoids compounds (all-E)-β-carotene (7.15 μg/g of dry weight) and (all-E)-lutein (2.41 μg/g of dry weight) resulted the major carotenoids, while 5-caffeoylquinic acid (1351 μg/g of dry weight) represented more than 78% (w/w) of the phenolic compounds found. These authors also reported two dihydrocaffeoyl spermidines in the hydrophilic extract. Additionally, the antioxidant propierties of both extracts, the hydrophilic and carotenoid, were evaluated against reactive oxygen (ROOd, H2O2, HOCl, and HOd) and nitrogen (ONOO2) species. Their results showed that the extracts scavenged all the tested reactive species. Moreover, some scavenging specialization was detectable as carotenoid extract resulted in a potent scavenger of peroxyl radical, meanwhile hydrophilic extract resulted in an effective hydrogen peroxide and hypochlorous acid scavenger.
AGRONOMICAL ASPECTS The plant can live three to five years, but in some areas can only be cultivated as an annual crop (Duarte, 2011). Although this species is usually cultivated between 0 and 600 m, there are reports of cultivation between 900 and 1200 m (Morton, 1987; Silva Filho, 1998). It requires full sun, temperatures ranging from 18 C to 30 C, and a relative humidity of 85%. Soils of medium fertility, latisols, and sandy soils are enough for this species to thrive (Morton, 1987; Silva Filho, 1998; Lim, 2013: Duarte and Paull, 2015). Additionally, the growth cycle of fruits is fast during the 80 days after anthesis, then it takes 10 more days for the color to change from yellow to orange, 10 more days to reach the deep orange, finally reaching the orange-brown about 110 days after anthesis (Souza et al., 2008). Propagation of cocona can be accomplished by using either sexual or vegetative propagules (Silva Filho, 1998; Duarte and Paull, 2015). When seeds are used, they can be extracted from ripe fruits with desirable characteristics, and allowed to ferment for 48 h under shade (Morton, 1987; Duarte et al., 2000) before washing and drying them for subsequent storage. However, there is evidence indicating that neither 48 h fermentation nor washing enhances germination, but fermentation for 4 days results in inhibition of the process (Duarte et al., 2000). The percentage of germination will remain up to 100% up to a month after seeds are harvested, and the process should be accomplished on a substrate composed by sandy soil, clay soil, and manure (1:1:1 v:v:v) (Silva Filho, 1998). Under these conditions germination will start
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after 7 days and will end 40 days later (Silva Filho, 1998). After 20 days, the seedling should be transplanted in individual containers, kept in those containers for 40 additional days and then transplanted into the field (Silva Filho, 1998). Air layers and cuttings have been used successfully for vegetative propagation (Morton, 1987; Silva Filho, 1998; Duarte et al., 2000; Duarte and Paull, 2015). However, when this method is used, plants obtained are less vigorous than seedlings (Duarte et al., 2000; Duarte and Paull, 2015). More recently, techniques for in vitro regeneration of the cocona have been developed (Medina Rivas et al., 2008; Schuelter et al., 2009). These techniques should assist in solving challenges related to cocona production. One of these challenges is the necessity to generate somaclonal variability, as interspecific crosses with close species usually fail, or have very low success rates, preventing the transfer of resistance or fruit quality genes in breeding programs (Medina Rivas et al., 2008). Another reason for using this alternative propagation strategy is the necessity of homogeneous seedlings presenting superior agronomic characteristics (Schuelter et al., 2009). Planting densities for cocona seems need to be determined for each soil and environmental condition, as different authors present different results and recommendations. Gonzalez Vega et al. (2012), working in Loreto, in the Peruvian Amazon region, tested four planting densities: 2.0 m 3 2.0 m, 1.5 m 3 1.5 m, 2.0 m 3 1.0 m, and 1.5 m 3 1 m, resulting in 2500 plants per ha, 4444 plants per ha, 5000 plants per ha, 6666 plants per ha, respectively. These planting densities were evaluated for the number of fruits, fruit weight, and fruit yield per density. The 6666 plants per ha rendered the highest production: 14 600 kg/ha21 of fruit, which significantly outperformed the other treatments. In experiments where a broad range of densities was evaluated, Duarte et al. (2002) reported results that support the recommendation of using 13 333 plants per ha. Additionally, Silva Filho (1998) indicates that each soil condition, availability of technology, and cultural technique, allow the utilization of a particular planting density.
PESTS AND DISEASES Cocona is susceptible to fungal (Colletotrichum gloeosporioides, Fusarium sp., Rhizoctonia solani, and Sclerotium sp.), oomycetes (Phytophthora infestans and Pythium sp.), and bacterial (Pseudomonas solanacearum) attacks (Morton, 1987; Silva Filho, 1998; Duarte and Paull, 2015). The insects more recognized as cocona pests are Diabrotica spp. (Duarte and Paull, 2015), Corythaica cyathicollis, Phrydenus muriceus, Planococcus pacificus (Silva Filho, 1998; Duarte and Paull, 2015), Psara periosalis, Pseudococcus sp., also cutworms and leaf-eating insects are pests in some areas (Morton, 1987). Silva Filho (1998) mentioned occurrence of some viruses in the Peruvian Amazon area. Last, among the nematodes, Meloydogine incognita has been reported (Morton, 1987; Duarte and Paull, 2015).
USES AND PERSPECTIVES Cocona is mainly used for fresh consumption or for preparation of jelly, juices, and marmalades, among other products (Morton, 1987; Silva Filho, 1998). However, uses in traditional and popular medicine are recognized, and the fruit is used by the Amazonian people to treat several ailments as burns, diabetes, skin mycoses, to lower uric acid and cholesterol blood levels (Silva Filho et al., 2003; Pardo Sandoval, 2004), and affecting the growth of human pathogenic bacterium Helicobacter pylori (Pardo Sandoval, 2010). Some South American native people use the juice for cosmetic purposes such as making the hair brighter. Furthermore, the leaves and roots have been used for medicinal purposes (Marx et al. 1998), including elimination of lice (Morton, 1987). Pardo Sandoval (2004) studied the effect of cocona extract, 40 mL/day during 3 days, on the glucose, cholesterol, LDL-c, HDL-c, and triglycerides levels of 100 individuals. After the treatment, the levels of glucose, cholesterol, LDLc, and triglycerides were significantly lower than the values at the beginning of the experiment, and HDL-c levels were higher than before. Pardo Sandoval (2010) compared the in vitro effect of cocona extract on growth of H. pylori against the effect of antibiotics: amikacin, amoxicilin, claritromicin, and tetraciclin. Her results showed that cocona extract exerted a higher inhibitory effect on the bacterial growth than the antibiotics. Another protective effect of cocona was studied by Frenedoso da Silva et al. (2014), which demonstrated the protection exerted by the extract against the deleterious effect of methyl mercury on reproductive system of rats. The utilization of cocona as a component of juices, jelly, liquor, and for fresh consumption, is becoming of great interest. Studies directed to the production of cocona chips with a high degree of crispness have been reported with promising results (Agudelo et al., 2015). Furthermore, Natividad and Ca´ceres (2013) claim the production of water-soluble powder (84.33%) by freeze-drying cocona, which facilitates the commercialization and increases the uses of the fruit in the food industry. Efforts to explore the potential of cocona as a basic component in the development of new products, such as functional diets, food additives, and supplements are nowadays a hot spot (Serna-Cock et al., 2015).
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CONCLUSIONS Cocona is a tropical fruit with a great potential to become an important product in the food industry. Not only because of its adaptability to tropical areas, but also because of its organoleptic characteristics, and its possible roles as a nutraceutical food. Research that aims to find new uses along with good publicity could make this fruit an interesting product in the regional and extraregional markets.
REFERENCES Agudelo, C., Igual, M., Talens, P., Martı´nez-Navarrete, N., 2015. Optical and mechanical properties of cocona chips as affected by the drying process. Food Bioprod. Process. 95, 192199. Cardona, J.E., Cuca, L.E., Barrera, J.A., 2011. Determinacio´n de alguno smetabolitos secundarios en tres morfotipos de cocona (Solanum sessiliflorum Dunal). Rev. Col. Quim. 40 (2), 185200. Duarte, O., 2011. Cocona (Solanum sessiliflorum Dunal). In: Yadhia Elhadi (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruits. Volumen 3: Cocona to Mango. Woodhead Publishing Series in Food Science, Technology and Nutrition, Cambridge, UK, Number 208. Duarte, O., Sandoval, X., 2002. Rendimiento y rentabilidad de seis densidades de plantacio´n de cocona (Solanum sessiliflorum Dunal) en Honduras. Proc. Interamer. Soc. Trop. Hortic. 46, 2122. Duarte, O., Paull, R., 2015. Exotic Fruits and Nuts of the New World. CABI, Boston. Duarte, O., Leiva, M., Huete, M., 2000. Estudios sobre propagacio´n sexual y asexual de la cocona (Solanum sessiliflorum Dunal). Proc. Interamer. Soc. Trop. Hortic. 44, 981101. Lim, T.K., 2013. Edible medicinal and non-medicinal plants, Fruits, vol. 6. Spinger Science 1 Business Media, Dordrecht. Frenedoso da Silva, R., Missassi, G., dos Santos Borges, C., Silva de Paula, E., Hornos Carneiro, M.F., Grotto, D., et al., 2014. Phytoremediation potential of Mana´-Cubiu (Solanum sessiliflorum Dunal) for the Deleterious effects of methylmercury on the reproductive system of rats. BioMed Res. Int. http://dx.doi.org/10.1155/2014/309631. Gonzales Vega, R., Ima´n Correa, S., Pinedo Tello, E., 2012. Evaluacio´n de densidades de siembra en Solanum sessiliflorum Dunal “cocona” y su efecto en el rendimiento de fruto. Ciencia Amazo´nica (Iquitos). 2 (2), 142145. Marx, F., Andrade, E.H.A., Maia, J.A.G., 1998. Chemical composition of the fruit of Solanum sessiliflorum. Zeitsch Lebensm Unters Forsch A. 206, 364366. Medina Rivas, M.A., Sepu´lveda Asprilla, N.I., Murillo, M.V., 2008. Regeneracio´n in vitro de plantas a partir de explantes foliares del lulo chocoano, Solanum sessiliflorum Dunal vı´a organoge´nesis. Revista Institucional Universidad Tecnolo´gica del Choco´: Investigacio´n, Biodiversidad y Desarrollo. 27 (1), 9295. Moreno, C., Quin˜ones, J.C., Jime´nez, P., 2016. Phenological growth stages of Solanum sessiliflorum according to BBCH scale. Ann. Appl. Biol. 168 (1), 151157. Morton J.F., 1987. Cocona. In: Fruits of warm climates. Julia F. Morton, Miami, pp. 428430. Natividad Marı´n, L., Ca´ceres Paredes, J.R., 2013. Algunos aspectos te´cnicos sobre la liofilizacio´n de pulpa de cocona (Solanum sessiliflorum Dunal). Rev. Venez. Cienc Tecnol. Alimentos. 4 (2), 207218. Pardo Sandoval, M.A., 2004. Efecto de Solanum sessiliflorum Dunal sobre el metabolismo lipı´dico y de la glucosa. Ciencia e Invest. 7 (2), 4348. Pardo Sandoval, M.A., 2010. Efecto in vitro del extracto de Solanum sessiliflorum “cocona” sobre el crecimiento de Helicobacter pylori. Ciencia e Invest. 13 (1), 3033. Quijano, C.E., Pino, J.A., 2006. Changes in volatile constituents during the ripening of cocona (Solanum sessiliflorum Dunal) fruit. Rev. CENIC Cienc Quı´m. 37 (3), 133136. Rodrigues, E., Mariutti, L.R.B., Mercadante, A.Z., 2013. Carotenoids and phenolic compounds from Solanum sessiliflorum, an unexploited Amazonian fruit, and their scavenging capacities against reactive oxygen and nitrogen species. J. Agric. Food Chem. 61, 30223029. Schuelter, A.R., Grunvald, A.K., Amaral Ju´nior, A.T., da Luz, C.L., Luz, C.L., Gonc¸alves, L.M., et al., 2009. In vitro regeneration of cocona (Solanum sessiliflorum, Solanaceae) cultivars for commercial production. Gen. Mol. Res. 8 (3), 963975. Serna-Cock, L., Vargas-Mun˜oz, D.P., Rengifo-Guerrero, C.A., 2015. Chemical characterization of the pulp, peel and seeds of cocona (Solanum sessiliflorum Dunal). Bras. J. Food Technol. 18 (3), 192198. Silva Filho, D.F., 1998. Cocona (Solanum sessiliflorum Dunal): Cultivo y utilizacio´n. Secretaria Pro-tempore. Tratado de Cooperacio´n Amazo´nica, Caracas, Venezuela, 114 pp. Silva Filho D.F., Noda H., Yuyama L.K.O., Aguiar J.P.L., Machado F.M., 2003. Cubiu (Solanum sessiliflorum, Dunal): Uma planta medicinal nativa da Amazoˆnia em processo de selec¸a˜o para o cultivo e Manaus, Amazonas, Brasil. Rev. Bras. Plantas Med. 5(2), 6570. Souza, L.T., Zonta, J.B., Zonta, J.H., Braun, H., Martins Filho, S., 2008. Caracterizac¸a˜o fı´sica e quı´mica de cu´bio (Solanum sessiliflorum Dunal) durante seu desenvolvimento. Rev. Cieˆnc Agron. 39, 449454. Villachica, H., 1996. Cocona (Solanum sessiliflorum Dunal). Frutales y hortalizas promisorios del Amazonas. Secretaria Pro-Tempore. Tratado de Cooperacio´n Amazo´nica, Por Hugo Villachica. Lima, Peru´, 102 pp. Volpato, G., Marcucci, R., Tornadore, N., Paoletti, M.G., 2004. Domestication process of two Solanum section Lasiocarpa species among Amerindians in the Upper Orinoco, Venezuela, wiht special focus on Piaroa indians. Econ. Bot. 58 (2), 184194. von der Pahlen, A., 1977. Cubiu (Solanum topiro Humb. & Bonpl.), uma fruteira da Amazônia. Acta Amazônica. 7, 301307. Yuyama, L.K.O., Macedo, S.H.M., Aguiar, J.P.L., Silva Filho, D., Yuyama, K., Fa´varo, D.I.T., et al., 2007. Quantificação de macro e micro nutrientes em algumas etnovariedades de cubiu (Solanum sessiliflorum Dunal). Acta Amazônica. 37 (3), 425430.
Cupuassu—Theobroma grandiflorum Ana L.F. Pereira1, Virgı´nia K.G. Abreu1 and Sueli Rodrigues2 1
Federal University of Maranha˜o, Imperatriz, MA, Brazil, 2Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Chapter Outline Introduction Cultivar Origin, Botanical Aspects and Harvest Season Chemical Composition and Nutritional Value Harvest and Postharvest Conservation and Potential Industrial Application
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Final Remarks References
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INTRODUCTION The cupuassu (Theobroma grandiflorum) is also known as cupu, pupu, pupuac¸u (in Brazil), cupuazur (in Iquitos, Peru), bacau (in Colombia), blanco cacau, pastate (in Mexico, Costa Rica and Panama); patashte, cupuassu (in England); patas (in Ecuador), and lupo (in Surinam). Cupuassu is a composed word from Tupi language, where kupu means “similar to cocoa” and uasu means “great” (Gondim et al., 2001). Among the Amazonian fruits, the cupuassu stands out in its economic potential. The pulp of the fruit has a yellowish-white color and strong flavor, being very appreciated by local communities, and also international markets, as an ingredient in fruit juice drinks. Moreover, the pulp is composed of a large proportion of starch, pectin polysaccharides, and dietary fiber, mainly in the form of insoluble fibers, which improves the texture parameters of dairy products. The seeds can also be processed to yield a chocolate-like product called “cupulate” (Alves et al., 2007; Genovese and Lannes, 2009). Thus, the rising commercial interest of this fruit has led to the development of new industries and has encouraged research on this food product. Moreover, this tree grows in synergy with other native rainforest species, offering an ecological approach for sustainable agroflorestal management and preservation.
CULTIVAR ORIGIN, BOTANICAL ASPECTS AND HARVEST SEASON The cupuassu tree, Theobroma grandiflorum (Willdenow ex. Sprengel) K. Schum., is naturally distributed in Brazilian rainforests, which are main producers of cupuassu. The cultivation occurs mainly in the states of Amazonas, Para´, Maranha˜o, Rondoˆnia, and Acre, while commercial crops can be found in other states, such as Bahia. Other tropical countries also cultivate this tree, such as Costa Rica, Colombia, Ecuador, French Guyana, Guyana, and Surinam (Yang et al., 2003). This plant belongs to Sterculiaceae family and Theobroma genus, composed of 22 species. One of those is Theobroma cacao, the cocoa tree, that has great economic importance and is largely studied for the flavor of the processed seeds (Gondim et al., 2001). Before 1980, the most of the produced cupuassu was carried out in an extractivist and semi-extractivist way. However, commercial plantations started in 1980 and, in recent decades, the area cultivated with this species had a significant increase. The Brazilian state of Para´ is the main producer having 41.142 tons and 3325 kg/ha of productivity in 2010 (Homma, 2012). The cupuassu is a tropical rainforest tree, which in nature, can reach 20 m in height and diameter 45 cm from stem to breast height. In cultivated trees, the size ranges from 6 to 8 m, and the canopy may reach 7 m in diameter. Usually, Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00021-6 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Cupuassu fruit.
the cupuassu tree flourishes two to three years after planting. However, any shaded plants flourish later. Flowering and fruiting can occur simultaneously from November to March. The flowering begins in June and can extend through to March, with incidence peak between November and January. Fruiting occurs between November and June, with incidence peak in February and March. The fruit ripening occurs between 120 and 135 days after the beginning of flowering, which occurs in the rainy season (Gondim et al., 2001). The fruit is brown, fuzzy and oblong, 1225 cm long, has a diameter of 1012 cm and weighs from 1 to 2 kg. The shell is hard, with a thickness of 13 cm, covered by a brown dust. The fruit cupuassu is presented in Fig. 1. Each fruit contains between 20 and 50 seeds surrounded by a mucilaginous pulp (Franco and Shibamoto, 2000).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Cupuassu has one of the best industrial application benefits due to its variety of food applications and high nutritional level. The fruit is composed of shell (43%), pulp (38%), seed (17%), and placenta (2%). The main pulp chemical characteristics, which is the fruit component with higher value economic are moisture (81.3%89.0%), total soluble solids (9.0010.8 Brix), reducing sugars (2.83.1 g/100 g), pH (3.23.6), and acidity (1.50%2.00%). The protein and lipid content is low in the pulp with 0.48% and 1.92%, respectively. Cupuassu is a potential source of dietary fiber (0.50%2.12%), mainly soluble fiber, and contains a considerable amount of starch as well as pectin polysaccharides (Salgado et al., 2011; SUFRAMA, 2003; Vriesmann and Petkowicz, 2009). Cupuassu pulp also has high content of ascorbic acid, with 102 mg/100 g. Moreover, the pulp has great concentration of phenolic compounds (3.54.9 mg catechin equivalent/g dry weight sample). It has considerable antioxidant activity (1.72.0 μM Trolox/g) superior to strawberry and similar to other Brazilian native fruits like “araca¸-boi (Eugenia stipitata Mc. Vaugh) and jaracatia´ (Jaracatia spinosa Aubli). The major minerals are potassium (34.27 mg), phosphorus (15.73 mg), magnesium (13.07 mg), iron (0.43 mg), and zinc (0.53 mg) (Pugliese et al., 2013; Rogez et al., 2004). The seed composition includes moisture (5.30%), proteins (7.81%), fibers (5.56%), and carbohydrates (23.09%). The cupuassu seed is very rich in fats ( 6 60% dry weight), which are 91% digestible by humans. The fatty acid profile include palmitic (11.22%11.70%), stearic (37.86%38.15%), oleic (37.83%3979%), araquidic (7.44%7.97%), and linoleic acids (2.37%247%) (Cohen and Jackix, 2005). Oliveira and Genovese (2013) compared the chemical composition of liquors of seeds (crushed seeds after fermentation and roasting) of cupuassu (Theobroma grandiflorum) with cocoa (Theobroma cacao) and their effects on streptozotocin-induced diabetic rats. These authors concluded that both cupuassu and cocoa liquors demonstrated positive effects on lipid profile and antioxidant status of STZ-diabetic rats. Moreover, the results indicated that the synergism between fatty acids and phenolic compounds in cupuassu and cocoa liquors might contribute to the reduction of hypertriglyceridemia caused by lack of insulin. Although cupuassu liquor had approximately 3.5-fold less phenolic compounds than cocoa liquor, it also presented a much lower amount of palmitic acid, and chronic intake of cupuassu was equally effective in ameliorating lipid profile and improving antioxidant status in STZ-diabetic rats. Thus, the authors suggested that the specific fatty acid and phenolic profile in cupuassu liquor may be superior to cocoa.
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FIGURE 2 Steps of the industrial cupuassu process. Source: Adapted from Superintendeˆncia da Zona Franca de Manaus (SUFRAMA), 2003. Projeto: Potencialidades Regionais Estudo de Viabilidade Econoˆmica do Cupuassu. Instituto Superior de Administrac¸a˜o e Economia ISAE/Fundac¸a˜o Getu´lio Vargas (FGV), Manaus, p. 71 SUFRAMA (2003).
HARVEST AND POSTHARVEST CONSERVATION AND POTENTIAL INDUSTRIAL APPLICATION Cupuassu has a high economic potential because of its excellent characteristics such as aroma, flavor, and texture (Faber and Yuyama, 2015). However, because of its distinctive flavor and strong acidity, cupuassu pulp is used as an ingredient in the manufacture of ice cream, juice, liquors, wines, jellies, filling for chocolate candies and other products, such as yogurts, rather than being consumed in natura. The seeds may be used in food products (such as cupulate) and in a variety of cosmetics. The shells can be used as fertilizer, having 0.72% of nitrogen, 0.04% of phosphorus, and 1.5% of potassium (Vriesmann and Petkowicz, 2009). The main steps of industrial cupuassu process are presented in Fig. 2. The fruit processing consists of extracting the pulp surrounding the seeds. This process can be done manually or mechanically. In the machining process, the fruits are washed and broken manually to remove the seeds with the pulp, and are then placed in the removing device machine, for separating pulp seed. Afterwards, the pulp is pasteurized, packed, and frozen (Gondim et al., 2001). The acidity of the pulp and the high pectin content are characteristics that favor the production of nectars, jelly, jams, and soft candy. However, the pulp also has been used in products such as yogurts. Costa et al. (2015) used the cupuassu pulp to produce goat milk yogurts. According to authors, compared with cow milk yogurts, it is difficult to make goat milk yogurt with a good consistency. These authors observed that pectin polysaccharides improved the texture of goat milk yogurts. Therefore, this pulp could be an important technological strategy for the dairy goat industry. Duarte et al. (2010) reported that the pulp of cupuassu also can be used for fruit wine production. These authors observed that this fruit has the potential to be used to produce fermented beverages, with good acceptance by consumers, according to sensory analysis evaluations. Functional foods have also been produced from the pulp. An example is a probiotic beverage produced (Pereira et al., 2017). The cupuassu presented technological advantage as a substrate for probiotic fermentation since its composition (natural sugars and organic acids) provides an enabling environment for the development of probiotic. The cupuassu seed is very rich in fats and its processing is similar to the processing of cocoa beans: fermentation, roasting, milling, and pressing to obtain fat. From the defatted mass, the cupuassu powder is obtained. During the seed fermentation, the cotyledon”s pH increases from 5.2 to 6.8, the phenolic compounds from 1.12 to 1.34 mg/100 g, the fats remain unchanged at 63.5% dry weight, and the color changes from a beige cream to a dark reddish caramel. The flavor and aroma of the fermented seed is indistinguishable from that of fermented cocoa seed. The seeds can be used to make chocolate and show a great potential to substitute cocoa in chocolate products. Cupuassu fat is very similar to cocoa butter, although with a different fatty acid profile and its application for the confectionery industry is very promising (Lannes et al., 2002).
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FINAL REMARKS The cupuassu, as a new product, litlle known outside the Amazon until recently, it is able to consolidate at the market. The use of cupuassu in the production of pulp, juices, jam, candies, yogurt and “cupulate” is a viable alternative that allows the use of harvest surplus, resulting in the introduction of new products into the market.
REFERENCES Alves, A.R., Sebbenn, A.A.C., Clement, A.F., 2007. High levels of genetic divergence and inbreeding in populations of cupuassu (Theobroma grandiflorum). Tree Genet. Genomes. 3 (4), 289298. Cohen, K.O., Jackix, M.N.H., 2005. Estudo do liquor de cupuac¸u. Cieˆnc. Tecnol. Aliment. 25 (1), 182190. Costa, M.P., Frasao, B.S., Silva, A.C.O., Freitas, M.Q., Franco, R.M., Conte Junior, C.A., 2015. Cupuassu (Theobroma grandiflorum) pulp, probiotic, and prebiotic: influence on color, apparent viscosity, and texture of goat milk yogurts. J. Dairy Sci. 98 (9), 59956003. Duarte, W.F., Dias, D.R., Oliveira, J.M., Teixeira, J.A., Silva, J.B.A., Schaw, R.F., 2010. Characterization of different fruit wines made from cacao, cupuassu, gabiroba, jaboticaba and umbu. LWT-Food Sci. Technol. 43 (10), 15641572, 2010. Faber, M.A., Yuyama, L.K.O., 2015. Nectar mix functional based on Amazonian fruits. J. Cell Sci. Therapy. 6, 197. Franco, M.R.B., Shibamoto, T., 2000. Volatile composition of some brazilian fruits: umbu-caja (Spondias citherea), camu-camu (Myrciaria dubia), araca´-boi (Eugenia stipitata), and Cupuacu (Theobroma grandiflorum). J. Agric. Food Chem. 48 (4), 12631265. Genovese, M.I., Lannes, S.C.S., 2009. Comparison of total phenolic content and antiradical capacity of powders and “chocolates” from cocoa and cupuassu. Cieˆnc. Tecnol. Aliment. 29 (4), 810814. Gondim, T.M.S., Thomazini, M.J., Cavalvante, M.J.B., Souza, J.M.L., 2001. Aspectos da Produc¸a˜o de Cupuac¸u. Empresa Brasileira de Pesquisa Agropecua´ria, Rio Branco, 43 p. Homma, A.K.O., 2012. Plant extractivism or plantation: what is the best option for the Amazon? Estudos avanc¸ados. 26 (74), 167186. Lannes, S.C.S., Amaral, R.L., Medeiros, M.L., 2002. Formulac¸a˜o de “chocolate” de cupuac¸u. Braz. J. Pharmaceut. Sci. 38 (3), 463469. Oliveira, T.B., Genovese, M.I., 2013. Chemical composition of cupuassu (Theobroma grandiflorum) and cocoa (Theobroma cacao) liquors and their effects on streptozotocin-induced diabetic rats. Food Res. Int. 51 (2), 929935. Pereira, A.L.F., Feitosa, W.S.C., Abreu, V.K.G., Lemos, T.O., Gomes, W.F., Narain, N., et al., 2017. Impact of fermentation conditions on the quality and sensory properties of a probiotic cupuassu (Theobroma grandiflorum) beverage. Food Res. Int. 100, 603611. Pugliese, A.G., Tomas-Barberan, F.A., Truchado, P., Genovese, M.I., 2013. Flavonoids, proanthocyanidins, vitamin c, and antioxidant activity of Theobroma grandiflorum (Cupuassu) pulp and seeds. J. Agric. Food Chem. 61 (11), 27202728. Rogez, H., Buxant, R., Mignolet, E., Souza, J.N.S., Silva, E.M., Larondelle, Y., 2004. Chemical composition of the pulp of three typical Amazonian fruits: arac¸a-boi (Eugenia stipitata), bacuri (Platonia insignis) and cupuac¸u (Theobroma grandiflorum). Eur. Food Res. Technol. 218, 380384. Salgado, J.M., Rodrigues, B.S., Donado-Pestana, C.M., Dias, C.T., dos, S., Morzelle, M.C., 2011. Cupuassu (Theobroma grandiflorum) peel as potential source of dietary fiber and phytochemicals in whole-bread preparations. Plant Foods Human Nutr. 66, 384390. Superintendeˆncia da Zona Franca de Manaus (SUFRAMA), 2003. Projeto: Potencialidades Regionais Estudo de Viabilidade Econoˆmica do Cupuac¸u. Instituto Superior de Administrac¸a˜o e Economia ISAE/Fundac¸a˜o Getu´lio Vargas (FGV), Manaus, p. 71. Vriesmann, L.C., Petkowicz, C.L., 2009. Polysaccharides from the pulp of cupuassu (Theobroma grandiflorum): Structural characterization of a pectic fraction. Carbohydr. Polym. 77, 7279. Yang, H., Protiva, P., Cui, B.M.A.C., Baggett, S., Hequet, V., Mori, S., et al., 2003. New bioactive polyphenols from Theobroma grandiflorum (“cupuac¸u”). J. Nat. Prod. 66, 15011504.
Custard apple—Annona squamosa L. Umesh B. Jagtap1 and Vishwas A. Bapat2 1
Government Vidarbha Institute of Science and Humanities, Amravati, Maharashtra, India, 2Shivaji University, Kolhapur, Maharashtra, India
Chapter Outline Introduction Origin and Distribution Botanical Description Total Production and Market Uses Dietary Uses Use in Traditional Medicine
163 163 163 164 164 164 164
Phytochemistry Fruits Seeds Harvest and Postharvest Conservation Potential Industrial Application Acknowledgment References
165 165 166 166 166 166 166
INTRODUCTION Annona squamosa L. (Family: Annonaceae), is also known as the sugar apple or custard apple (in India) or sweetsop. A. squamosa L. is a fruit tree cultivated in different tropical countries around the world for its sweet and delicious fruits. This plant is a rich source of pharmaceutically important anticancer compound acetogenins (AGEs) (Liaw et al., 2010).
ORIGIN AND DISTRIBUTION The original home of sugar apple is unknown. It most likely originates from central America, like most Annona species; the tree is supposed to have spread to Mexico, South America, and the Caribbean in the 16th to 17th centuries. It was brought to India by the Portuguese during the same period, then to south-east Asia, and was also introduced into Africa and Oceania (Pinto et al., 2005). Currently, the custard apple is extensively cultivated as a fruit tree in orchards and on commercial farms throughout tropical and subtropical areas, comprising southern Florida, south Asia, the south Pacific, some areas of central and western India, and in the Deccan Peninsula. However, in some areas, it has escaped from cultivation and is found wild in pastures, forests and along roadsides (Morton, 1987).
BOTANICAL DESCRIPTION The custard apple tree ranges from 3 to 6 m in height with open crown of irregular branches and somewhat zigzag twigs (Morton, 1987). Deciduous leaves alternately arranged on short, hairy petioles, are lanceolate or oblong, blunt tipped, 515 cm long and 25 cm wide; dull-green on upper side pale, with a bloom below; slightly hairy when young; aromatic when crushed. Along the branch tips, opposite to the leaves, the fragrant flowers are born singly or in groups of 24. They are oblong 2.53.8 cm long, never fully open; with 2.5 cm long, drooping stalks, and 3 fleshy outer petals, yellow-green on the outside and pale-yellow inside with a purple or dark-red spot at the base. The three inner petals are merely tiny scales. The compound fruit is nearly round, ovoid or conical, 610 cm long; its thick rind composed of knobby segments, pale-green, graygreen, bluish-green or in one form, dull, deep-pink externally (nearly always with a bloom); separating when the fruit is ripe and revealing the mass of conically segmented, creamy-white glistening, delightfully fragrant, juicy, sweet and having delicious flesh. The fruits are tasty, though a nuisance to eat. Many of the Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00019-8 © 2018 Elsevier Inc. All rights reserved.
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segments enclose a single oblong-cylindric, black or dark-brown seed about 1.25 cm long (Morton, 1987). Almost 30% of the weight of the fruit consists of seeds. Generally, 20 to 40 seeds are present in a single fruit.
TOTAL PRODUCTION AND MARKET Statistics on minor fruits, such as Annona species, are unavailable in many countries, and where reported they often lack reliability, uniformity, and continuity. Although custard apple data is scarce, the information collected shows that the potential for expanding the custard apple market is high in many countries. It is grown commercially in the West Indies, Florida, middle-East India, Malaysia, and Thailand. It is still considered a backyard fruit used mainly for domestic consumption in the Philippines. In Brazil the custard apple production is concentrated in Alagoas and Sa˜o Paulo states. In India, the custard apple is cultivated in rainfed orchards mainly in Maharashtra, Gujarat, Andhra-Pradesh, Karnataka, Madhya Pradesh, Uttar-Pradesh, Bihar, Assam, and Orissa (Singh, 1992). Few plantings are commercial except for areas of Gujarat. Most fruits come to market from semi-wild forests of the Deccan plateau where the custard apple has gone wild.
USES Dietary Uses The ripe custard apple fruits have strong consumer demand due to its white, sweet delicate flesh. The fruits are consumed as a fresh dessert fruit and use for preparing juice, icecream, sherbets, soft drinks, and other refreshing drinks. Fruit flesh is often mixed with milk to make milkshakes (Morton, 1987; Hiwale, 2015).
Use in Traditional Medicine The aerial and underground plant parts are rich sources of bioactive compounds like acetogenins (AGEs), alkaloids and flavonoids which are routinely used in traditional medicine (Table 1). The roots are used to treat acute dysentery, depression, and spinal marrow diseases, while leaves have been used in cases of prolapse of the anus, sores, and swelling (Chao-Ming et al., 1997). Ethanol extracts of the bark appear to have antitumor activity (Hopp et al., 1998). The fruit contains 16-β, 17-dihyroxykauran-19-oic acid which has demonstrated anti-HIV activity (Wu et al., 1996). Annotemoyin-1, Annotemoyin2, squamocin, and cholesteryl glucopyranoside were isolated from the seeds of A. squamosa (Rahman et al., 2005). These compounds and plant extracts showed remarkable antimicrobial and cytotoxic activities.
TABLE 1 Ethnomedicinal Uses of Annona squamosa L. Plant part
Method of preparation
Use
Reference
Leaves
Crushed
Hysteria, fainting spells, ulcers and wounds
Morton (1987)
Decoction
Dysentery
Chao-ming et al. (1997)
Prolapse of the anus, sores and swelling
Chao-ming et al. (1997)
Insecticidal and antiplasmodic agents, Treatment of rheumatism and painful spleen
Chavan et al. (2010)
Analgesic, antiinflammatory
Dash et al. (2001)
Cardiotonic activity
Wagner et al. (1980)
Grounded and macerated in water
Insecticide, antiheadlice
Rahman et al. (2005)
Decoction
Dyspepsia
Morton (1987)
Vasorelaxant effect on rat aorta
Morita et al. (2006)
Seeds
Fruits
Crushed ripe fruits mixed with salt
Applied on tumors
Morton (1987)
Bark
Decoction
Tonic and halt to diarrhea
Morton (1987)
Root
Dysentery, Depression, spinal marrow diseases and other oilments
Chao-ming et al. (1997)
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Ahmad et al. (2006) carried out the epoxidation of A. squamosa oil to utilize a sustainable resource through the development of an anticorrosive coating material. A cyclic octapeptide, cyclosquamosin B, isolated from the seeds of A. squamosa showed a vasorelaxant effect on rat aorta (Morita et al., 2006). Panda and Kar (2007) demonstrated the role of A. squamosa seed extract in the regulation of hyperthyroidism and lipid peroxidation in mice. Phytochemical analyses revealed the involvement of quercetin in the mediation of antithyroidal activity of A. squamosa seed extract. In vitro and in vivo pharmacological studies have demonstrated the plant’s antiinflammatory (Chavan et al., 2010; Yang et al., 2008) vasorelaxant (Morita et al., 2006), antimicrobial and cytotoxic (Rahman et al., 2005) properties. The AGEs with insecticidal properties is present in roots, stems, leaves, and seeds. The plant is a good candidate for agroforestry because the leaves are bitter to goats and cattle.
PHYTOCHEMISTRY The Annona species are rich in AGEs are a unique class of C35 or C37 secondary metabolites of Annonaceous plants derived from the polyketide pathway. Extensive studies on AGEs have indicated that these naturally occurring compounds possess a broad spectrum of bioactivity, including anticancer, antiparasitic, insecticidal and immunosuppressive effects. More than 500 AGEs were isolated from various parts of the plants of Annonaceae family (Liaw et al., 2010).
Fruits Custard apple pulp is slightly granular, creamy yellow or white, sweet with a good flavor and low acidity (Mowry et al., 1941). It is considered the sweetest of the Annona fruits. The edible portion is 28%37% of the total fruit weight and seeds correspond to 23%40%. Carbohydrates present in the pulp include fructose (3.5%), sucrose (3.4%), glucose (5.1%), and oligosaccharides (1.2%2.5%). The nutrient composition of the edible pulp of A. squamosa L. is shown in Table 2.
TABLE 2 Nutrient Composition of the Edible Pulp of Annona squamosa L. (Per 100 g Fresh Weight) Components
Content
Water
68.675.9 g
Proteins
1.22.4 g
Lipids
0.11.1 g
Carbohydrates
18.226.2 g
Fiber
1.12.5 g
Total acidity
0.1 g
Ash
0.61.3 g
Energy
86114 Calories
Calcium
1744.7 mg
Phosphorous
23.655.3 mg
Iron
0.31.8 mg
Vitamin A
0.0040.007 mg
Vitamin B1
0.100.11 mg
Vitamin B12
0.0570.167 mg
Vitamin B5
0.651.28 mg
Ascorbic acid
3442.2 mg
Tannins
Source: Pareek, S., Yahia, E.M., Pareek, O.P., Kaushik, R.A., 2011. Postharvest physiology and technology of Annona fruits. Food Res. Int. 44, 17411751.
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Seeds Besides fruits, seed kernels are used in the oil and soap industries. Seed extracts are very poisonous and have insecticidal properties, saponins extracted from the seeds hemolyzes red blood cells and is toxic to fish. In India the extract of the seed is used to induce abortion by tribes in Madhya Pradesh state, often combined with leaves of Plumbago zeylanica (Pinto et al., 2005).
HARVEST AND POSTHARVEST CONSERVATION The custard apple tree starts bearing fruits at 4 years of age and its production declines on the 15th year depending upon the maintenance. The custard apple tree produces a single crop in a year during AugustOctober in south India and SeptemberNovember in north India. Fruit yield differs extensively from tree to tree. Usually a 7-year-old tree produces 100150 fruits, the total yield being 7 tonnes/ha (Hiwale, 2015). Custard apple fruits are considered to be mature and attain their harvesting point when the skin changes color and segments spread far apart, exposing a creamy yellow skin. Like other Annonaceae members, the custard apple is highly susceptible to spoilage, softens very rapidly during ripening, and becomes squashy and not easy to consume fresh (Okigbo and Obire, 2009). It is sold in local markets and are many times rejected because of external injuries or uneven shape and size. Premature harvesting can result in poor fruit quality, and fruits left to ripe on the tree are often eaten by birds and bats, and when overmature have a tendency to break and decay (Pareek et al., 2011). However, following maturity and harvest, large quantities of ripe fruits rapidly deteriorate and are usually wasted as a result of poor handling and inadequate storage facility. Several strategies were developed such as low temperature storage, modified and controlled atmospheric conditions, and chemical treatments (1-methylcyclopropene, salicylic acid) to retard ripening process and packaging to extend the storage and shelf life of the fruit (Pareek et al., 2011). Additionally there is an urgent need to develop alternative fruit processing methods to minimize postharvest losses and generate more income. Therefore, there is greater need to process the ripe custard apple fruits into suitable products to minimize the postharvest losses. Jagtap and Bapat (2015) evaluated the potential of custard apple pulp in the production of wine. The wine produced from custard apple pulp may serve as a good source of antioxidants and provide health benefits.
POTENTIAL INDUSTRIAL APPLICATION The production of wine from custard apple fruit might have potential health applications providing opportunities to develop value-added products. This will reduce the postharvest losses, improves nutritional value, increases consumption, export, cultivation, and commercialization of custard apple. Additionally, it helps not only to generate more profits for custard apple growers, but also contribute to the economy of the wine industry (Jagtap and Bapat, 2015). Furthermore, in nonfood applications, A. squamosa leaves are utilized for cost effective, eco-friendly and sustainable method for the production of silver nanoparticles (Jagtap and Bapat, 2013).
ACKNOWLEDGMENT VAB acknowledges the Indian National Science Academy, India, for providing the INSA Senior Scientist Fellowship.
REFERENCES Ahmad, S., Naqvi, F., Sharmin, E., Verma, K., 2006. Development of amineacid cured Annona squamosa oil epoxy anticorrosive polymeric coatings. Prog. Org. Coat. 55, 268275. Chao-ming, L., Ning Hua, T., Qing, M., Hui-Lan, Z., Xiao Jang, Yu. W., Jun, Z., 1997. Cyclopeptide from the seeds of Annona squamosa L. Phytochemistry. 45, 521523. Chavan, M.J., Wakte, P.S., Shinde, D.B., 2010. Analgesic and anti-inflammatory activity of caryophyllene oxide from Annona squamosa L. bark. Phytomedicine. 17, 14915. Dash, G.K., Ganapathy, S., Suresh, P., Panda, S.K., Sahu, S.K., 2001. Analgesic and anti-inflammatory activity of Annona squamosa leaves. Indian J. Nat. Prod. 17, 3235. Hiwale, S., 2015. Sustainable Horticulture in Semiarid Dry Lands. Springer, India. Hopp, D.C., Alali, F.Q., Gu, Z.M., Mclaughlin, J.L., 1998. Mono- Thf Ring Annonaceous acetogenins from Annona squamosa L. Phytochemistry. 47, 803809.
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Jagtap, U.B., Bapat, V.A., 2013. Biosynthesis, characterization and antibacterial activity of silver nanoparticles by aqueous Annona squamosal L. leaf extract at room temperature. J. Plant Biochem. Biotechnol. 22, 434440. Jagtap, U.B., Bapat, V.A., 2015. Phenolic composition and antioxidant capacity of wine prepared from custard apple (Annona squamosa L.) fruits. J. Food Process. Preserv. 39, 175182. Liaw, C.C., Wu, T.Y., Chang, F.R., Wu, Y.C., 2010. Historic perspectives on annonaceous acetogenins from the chemical bench to preclinical trials. Planta Med. 76, 13901404. Morita, H., Iizuka, T., Choo, C.Y., Chan, K.L., Takeyad, K., Kobayashie, J., 2006. Vasorelaxant activity of cyclic peptide, cyclosquamosin B, from Annona squamosa. Bioorg. Med. Chem. Lett. 16, 46094611. Morton, J., 1987. Sugar apple. In: Fruits of warm climates. Julia F Morton, Miami, Florida, USA. Mowry, H., Toy, L.R., Wolfe, H.S., 1941. Miscellaneous tropical and subtropical Florida fruits. Agric. Extension Service Gainesville Florida Bull. 109, 1121. Okigbo, R.N., Obire, O., 2009. Mycoflora and production of wine from fruits of soursop (Annona muricata L.). Int. J. Wine Res. 1, 19. Panda, S., Kar, A., 2007. Annona squamosa seed extract in the regulation of hyperthyroidism and lipidperoxidation in mice: possible involvement of quercetin. Phytomedicine. 14, 799805. Pareek, S., Yahia, E.M., Pareek, O.P., Kaushik, R.A., 2011. Postharvest physiology and technology of Annona fruits. Food Res. Int. 44, 17411751. Pinto, A.C.D.E.Q., Cordeiro, M.C.R., De Andrade, S.R.M., Ferreira, F.R., Filgueiras, H., Alves, R.E., et al., 2005. Annona Species, International Centre for Underutilized Crops. University of Southampton, Southampton, U.K. Rahman, M.M., Parvin, S., Haque, M.E., Islam, M.E., Mosaddik, M.A., 2005. Antimicrobial and cytotoxic constituents from the seeds of Annona squamosa. Fitoterapia. 76, 484489. Singh, S.P., 1992. Fruit Crops for Wasteland. Scientific Publisher, Jodhpur, India. Wagner, H., Reiter, M., Frest, W., 1980. Neue herzwirksame Drrogen L: Zur chemie und pharmacologie des herzwirksame prinzips von Annona squamosa. Planta Med. 40, 7785. Wu, Y.C., Hung, Y.C., Chang, F.R., Cosentino, M., Wang, H.K., Lee, K.H., 1996. Identification of ent 16 β, 17 dihydroxykauran-19-oic acid as an anti-HIV principle and isolation of the new diterpenoids annosquamosins A and B from Annona squamosa. J. Nat. Prod. 59, 635637. Yang, Y.L., Hua, K.F., Chuang, P.H., Wu, S.H., Wu, K.Y., Chang, F.R., et al., 2008. New cyclic peptides from the seeds of Annona squamosa L. and their anti-inflammatory activities. J. Agric. Food Chem. 56, 386392.
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Durian—Durio zibethinus Saichol Ketsa1,2 1
Kasetsart University, Bangkok, Thailand, 2The Royal Society of Thailand, Bangkok, Thailand
Chapter Outline Introduction Cultivar Origin and Botanical Aspects Estimated Annual Production Fruit Physiology and Biochemistry Respiration Ethylene Production Softening Color Development Weight Loss Dehiscence Chemical Composition and Nutritional Value Vitamins and Minerals Antioxidants Fatty Acids Carbohydrates Carotenoids
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Sensory Characteristics Harvest and Postharvest Conservation Harvest Season Harvesting Ripening Surface Coating 1-MCP Storage Industrial Application or Potential Industrial Application Fresh Fruit Durian Products Durian Husk Concluding Remarks References Further Reading
174 175 175 175 175 176 176 176 176 176 177 177 177 177 180
INTRODUCTION Durian is a famous and popular native fruit of Southeast Asia, known as the King of Fruit. It is considered exceedingly delicious, and the fruit is rather expensive in oversea markets to buy. Durian is a climacteric fruit that undergoes rapid postharvest changes resulting in a short shelf life at ambient temperature. These changes are essential for a good quality for consumption. The fruit is usually consumed fresh, but it can be processed into different products. Nowadays both fresh and processed durians have become popular in both local and export market, possibly because new ways of eating the fruit have been so well received. In addition, a huge amount of inedible husk left has created biomass that can be developed into many innovative products.
CULTIVAR ORIGIN AND BOTANICAL ASPECTS Durian is a native fruit of Southeast Asia. Its range appears to be the Malay Peninsula, Indonesia, and the island of Borneo (Subhadrabandhu et al., 1991). The durian is a tropical fruit tree in the order Malvales, family Bombacaceae. There are 51 genera within this family. The genus Durio has approximately 28 species. The most common and economically valuable species is Durio zibethinus Murr. (Reksodihardjo, 1962). The common name “durian” is derived from the Malay word “duri” meaning thorn. The species name “zibethinus” is derived from the Italian word ‘zibetto’ meaning strong aroma. Durian leaves are alternately elliptical and lanceolate, 46 cm wide and 1020 cm long. Inflorescences on older branches form fascicles of corymbs of 350 flowers, up to 15 cm long. The five petals are white, light yellow or cream and longer than the calyx (Subhadrabandhu and Ketsa, 2001). Durian has complete or perfect flowers, meaning each flower has a stamen and pistil (Polprasid, 1960). The fruits which located on the underside of the branches are stalked. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00022-8 © 2018 Elsevier Inc. All rights reserved.
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They are pendulous, round to oblong, commonly 1316 cm wide and 1525 cm long, but may be up to 35 cm long. The fruit may exceed 3 kg in weight, olive-green to yellow, covered with broadly pyramidal, coarse, hard, and sharp spines. The aril is the edible portion of the fruit and varies in color, texture and thickness among varieties (Subhadrabandhu and Ketsa, 2001).
ESTIMATED ANNUAL PRODUCTION Commercial production of durian is concentrated mostly in Thailand followed by Malaysia and Indonesia. It is also grown in the Philippines and other ASEAN nations but at much smaller levels. In addition, north Queensland (Tully to Cape Tribulation) and the Northern Territory of Australia, Papua New Guinea, Sri Lanka, and India have also grown durian but mainly for the domestic market. Thailand’s capacity to produce durian is approximately 5060% of the global supply. Most Thai durians are domestically consumed fresh, accounting for 85% of the overall production, while export of fresh and frozen durians is 10% and the processed forms account for 5%. Fruit yield is variable, but in Thailand and Malaysia, good orchards produce 1018 tons per hectare annually. This corresponds to a durian tree having about 50 fruits weighing 1.54 kg each. Although most production in Malaysia is consumed domestically, there are some exports to neighboring countries such as Singapore and Brunei. Sometimes Malaysia still needs to import durian from Thailand to supply domestic demand especially in April and May before the harvesting season of Malaysian durian (Subhadrabandhu and Ketsa, 2001). Moreover, the production in Indonesia, the Philippines, and Brunei is not sufficient to meet domestic demand, thus imports from Malaysia and Thailand are necessary.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY After harvest, durian fruit continues to undergo physiological and biochemical changes during ripening such as respiration, ethylene production, softening and color development. These characters are essential for a good taste of durian fruit.
Respiration Ripening durian fruit exhibits a respiratory climacteric pattern (Tongdee et al., 1988; Booncherm, 1990). The rise in respiratory coincides with ripening. There are three major factors influencing respiration: temperature, cultivar and fruit maturity. The elevation of temperature from 24 C to 33 C induced the rise of respiration rate (Ketsa and Daengkanit, 1998a, 1998b). At 13 C, durian fruits cultivars Chanee, Kanyao, and Monthong harvested at commercial maturity had respiration rates in the ranges of 1659, 638, and 756 mL CO2/kg per h, respectively. At 25 C, these values increased to 106155, 60121, and 29106 mL CO2/kg per h, respectively (Kosiyachinda and Tansiriyakul, 1988). Booncherm and Siriphanich (1991) reported that respiration rate for Chanee durian could be up to 450 mg CO2/kg per h. Fruits harvested at different stages also had different rates of respiration. At 22 C, durian fruit cv. Chanee harvested at 95% maturity reached a respiration peak on day 4 with rate of 180 mL CO2/kg per h, earlier than durian harvest at 85% that reached its peak on day 6 with rate of 140 mL CO2/kg per h (Tongdee et al., 1990a). When the aril and husk of cv. Chanee durian were separated, respiration of the husk was much higher than that of the aril. The climacteric pattern of respiration in the husk continued for a few days before declining (Booncherm, 1990).
Ethylene Production Durian is a climacteric fruit (Tongdee et al., 1988; Booncherm, 1990). Ethylene production of durian fruit coincides with respiration during ripening. At 13 C, durian fruits cvs. Chanee, Kanyao, and Monthong harvested at commercial maturity had ethylene production of 7.0, 1.2, and 2.4 μL/kg per h, respectively. At 25 C, these values increased to 26.3, 10.8, and 9.5 μL/kg per h, respectively (Kosiyachinda and Tansiriyakul, 1988). Durian held at 33 C inhibited ethylene production (Ketsa and Pangkool, 1995a). The mechanism of high temperature reduced ethylene production may involve in inhibiting the conversion of 1-aminocyclopropane-1-carboxylic acid (ACC) to ethylene (Atta-Aly, 1992).
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Booncherm and Siriphanich (1991) separated the pulp from the husk and found that most of ethylene production came from the husk. Ethylene production of the husk continued to increase for a few days before declining similar to the respiration. In the case of the pulp, ethylene production decreased soon after the separation. Durian pulp alone could not be ripened normally. This indicates that the ripening of durian pulp required ethylene from the surrounding husk. Ethylene production rates of cv. Chanee were higher than that of cv. Monthong during ripening (Chaiprasart, 1993; Maninang et al., 2011). In fact, Durian cv. Chanee ripens earlier than cv. Monthong (Chaiprasart, 1993). Cv. Chanee had higher ACC content and ACC oxidase (ACO) activity in both pulp and husk than that of cv. Monthong. ACS activities in the pulp and husk of both cultivars were comparable but ASC activity of cv. Chanee reached its peak earlier than that of cv. Monthong during ripening (Chaiprasart, 1993). Data of ACC content and activities of ACC synthase (ACS) and ACO in the pulp and husk confirm the difference in ethylene production among cultivars and between pulp and husk. Amornputti et al. (2016) confirmed the difference in ACC content and activities of ACS and ACO in the pulp and husk of durian during ripening. 1-methylcyclopropene (1-MCP) treatment also decreased ACC content and activities of ACS and ACO in both pulp and husk of durian, but the reduction of ACO activity was more severe in the pulp (Amornputti et al., 2016).
Softening Durian pulp decreases rapidly in firmness upon ripening (Ketsa and Pangkool, 1995a; Ketsa and Daengkanit, 1998b). Fruits harvested at 109 6 2 and 123 6 2 days after anthesis for cvs. Chanee and Monthong, respectively and showed a marked decline in firmness 2 days after harvest. However, the pulp of cv. Monthong was firmer than that of cv. Chanee at all stages of fruit growth until mature stage (Wisutiamonkul et al., 2015a) but their pulp firmness was almost the same at fully ripe stage (Ketsa and Daengkanit, 1999b; Wisutiamonkul et al., 2015b). Ethylene treatment increased pulp softening whereas 1-MCP treatment delayed softening of durian fruit (Amornputti et al., 2014; Palapol et al., 2015; Wisutiamonkul et al., 2015a, 2015b). Pulp firmness rapidly decreased during ripening and coincided with the sharp increase in pectin methylesterase and polygalacturonase activities together with an increase of water-soluble pectin. Pectin methylesterase activity was found to be high in unripe durians and remained high towards the end of ripening (Ketsa and Daengkanit, 1998b, 1999a). The activities of the softening enzymes in the pulp had pattern change differences between cultivars (Ketsa and Daengkanit, 1999a). The pulp of cv. Monthong was firmer and contained less water-soluble pectin and pectin methylesterase activity than that of cv. Chanee, while their polygalacturonase activities were comparable during ripening (Ketsa and Daengkanit, 1999b). No correlation was found between softening and pectin methylesterase activity, while the softening was correlated with polygalacturonase activity (Imsabai et al., 2002). Palapol et al. (2015) reported the relationship of α-expansins and pulp softening of ripening durian. Exogenous ethylene promoted gene expression of DzEXP1 in the pulp, but had a smaller effect on DzEXP2. 1-MCP inhibited the expression of DzEXP1 and, somewhat less, of DzEXP2 in pulp. While both ethylene and 1-MCP treatment had no effect on the expression of DzEXP3. This indicates the close relationship between expression of DzEXP1 and DzEXP2 in pulp softening processes of ripening durian.
Color Development During fruit growth of cv. Monthong, yellow pulp started at 99 days after anthesis and became darker at 113127 days after anthesis concomitant with the increase in β-carotene content (Sangwanangkul, 1998). The durian pulp changes from light to dark yellow upon ripening and depending on the cultivar (Ketsa and Pangkool, 1994; Wisutiamonkul et al., 2015a). After week 12 of anthesis the pulp color of cv. Chanee changed to creamy (Fig. 1A), while pulp color of cv. Monthong was remained white (Fig. 1B). This difference became more apparent from this stage onwards. When the fruit was ripe, the color of the pulp was darker yellow in cv. Chanee than in cv. Monthong (Wisutiamonkul et al., 2017a). In cv. Monthong after harvest the pulp color was light cream. After 4 days of storage at 25 C the pulp was dark yellow. The L*, b*, and hue values of the pulp increased after 1 day of storage while 1MCP treatment delayed an increase for 6 days (Amornputti et al., 2014). In cv. Chanee after harvest the pulp color changed from light to dark yellow during ripening. The L* value of the pulp decreased while the b* value increased. For fruits stored at 34 C their pulp color changed from light to dark yellow more rapidly than that of the fruits stored at room temperature. Fruits stored at 12 C showed only little change of L* and b* values through 5 days of storage (Imsabai, 1999). Water stress after harvest had no significant effect on color development of the pulp of ripened durian. Ripening based on color development of the pulp increased slightly at all levels of 75, 83, and 93% humidity (Ketsa and Pangkool, 1994).
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FIGURE 1 Pulp color during fruit development and ripening and whole ripe fruit of cultivars Chanee (A) and Monthong (B) (Wisutiamonkul et al., 2017a).
Weight Loss Over the five-day period, durian fruit lost significantly more weight at lower RH (75%) than at higher RH (8393%). Average daily weight loss as a proportiod of the original weight over the five-day period was 3.8, 2.7, and 2.6% per day at 75, 83, and 93% RH, respectively (Ketsa and Pangkool, 1994). This was high (Sriyook et al., 1994), compared to values obtained from tangerines (Ketsa, 1990), mangoes (Pantastico et al., 1984), and sugar apples (Kasiolarn, 1991). The rind (husk) of durian fruit is covered with spines (Subhadrabhandhu and Ketsa, 2001), resulting in a large surface area unit per volume of fruit which enhances the weight loss (Ketsa. 1990). The maximum permitted weight loss of most commercial procedures is less than 10% (Burton, 1982), but despite the 21% weight loss of ripened durian fruit over a nine-day period at ambient temperature (30 C and 70% RH), the fruit is still saleable (Sriyook et al., 1994). This may be due to the thick and extremely tough husk which shows no shrinkage despite the huge weight loss. The majority of weight loss in durian fruit apparently occurs in the husk tissue because moisture content of the pulp under different RHs is not significantly different (Ketsa and Pangkool, 1994). This is similar to plaintains (Asiedu, 1987) and rambutans (Lam et al., 1987). Weight loss of ripened durian fruit may not result from the withdrawal of water from the pulp. The durian fruit has a white membrane-like embedded in each locule, acting as a partition between the pulp and rind tissues. This may restrict the movement of water from the pulp to the husk during weight loss. Therefore, weight loss of ripened durian fruit is confined only to the rind which is exposed directly to the surrounding air.
Dehiscence Durian fruit have 35 longitudinal sutures in the peel (pericarp; husk), covering the full length of the fruit. These sutures open in overripe fruit, in a process called dehiscence. Durian dehiscence zones can be up to about 40 cm long in large fruit, and, due to the thick peel, up to 2 cm wide. As there can be five dehiscence zones per fruit, the total cell separation area is as much as about 400 cm2 per fruit. This means that durian fruit might have among the largest cell separation surfaces in the plant kingdom. Dehiscence of durian fruit occurs frequently during late ripening or overripe. The blossom end of the fruit is usually first to dehisce, but any point along the suture is vulnerable. Dehiscent fruit cannot be kept for long periods of time, particularly in warm conditions, because the aril (pulp) is easily infected by microorganisms (Subhadrabhandhu and Ketsa, 2001).
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The early stages of dehiscence, at least, are due to cell separation, which is the same as in abscission, the more widely studied type of cell separation (Roberts et al., 2002). Dehiscence in durian fruit is greater in the low humidity than in the high humidity (Sriyook et al, 1994; Ketsa and Pangkool, 1995a). Similarly, An˜abesa et al. (2006) reported a delay of dehiscence in durian fruit after waxing, which prevented water loss. Treatment with gibberellic acid (Sriyook et al., 1994) and 1-MCP (Maninang et al., 2011; Palapol et al., 2015) delayed dehiscence. Ethephon slightly increased the rate of ethylene production by the fruit. The rate and timing of ethylene production was correlated with both dehiscence and pulp softening (Maninang et al., 2011; Palapol et al., 2015). The increase in ethylene production in ripening durian is mainly due to the peel (Booncherm and Siriphanich, 1991). The data are consistent in the idea that the processes regulating the onset of dehiscence are the same as those regulating abscission, while at later stages mechanical factors seem to hasten durian dehiscence. Durian fruit dehiscence is preceded by an increase in soluble pectin levels, concomitant with an increase in smaller pectin molecules, which indicates pectin degradation. Hemicellulose is also broken down. Increased activity of polygalacturonase, β-1,4-endoglucanase, pectin methylesterase, and β-galactosidase has also been found (Khurnpoon et al., 2008). Khurnpoon (2007) sprayed durian fruit with gibberellic acid, which delayed dehiscence. The treatment reduced the activities of polygalacturonase, β-1, 4-endoglucanase, pectin methylesterase and β-galactosidase in the dehiscence zone, indicating that these enzymes are involved in the separation process. Three α-expansin genes have been found in dehiscence zone tissue of durian. Transcript abundance of all three expansin genes increased in the dehiscence zone, in fruit at 25 C. The highest abundance of DzEXP genes in the dehiscence zones of control fruit was found prior to dehiscence. Exogenous ethylene promoted gene expression of DzEXP1. It had a smaller effect on DzEXP2, but did not affect DzEXP3 expression.1-MCP inhibited the expression of DzEXP1 and, somewhat less, of DzEXP2, but did not affect DzEXP3 expression. Data indicated that DzEXP1 and DzEXP2 are related to durian dehiscence (Palapol et al., 2015).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Vitamins and Minerals The edible part of the durian fruit (technically a capsule) is the fleshy aril that surrounds the seed, representing 2035% of the fruit weight. The importance of durian fruit as a nutraceutically valued source can be correlated to their composition and presence of bioactive antioxidant compounds (Poovarodom et al., 2010; Ho and Bhat, 2015). The flesh is rich in carbohydrate, proteins, vitamins (thiamine, riboflavin and vitamins A, C, and E) (Isabelle et al., 2010), and minerals (calcium, phosphorus, potassium, iron). Most of the health benefits come from durian’s impressive vitamin and mineral content. It contains vitamins such as vitamin C, folic acid, thiamin, riboflavin, niacin, B6 and vitamin A (Isabelle et al., 2010). Important minerals such as potassium, iron, calcium, magnesium, sodium, zinc, and phosphorus are also found in durian (Haruenkit et al., 2010; Gorinstein et al., 2011).
Antioxidants The importance of this fruit is mostly connected with its composition and antioxidant properties (Arancibia-Avila et al., 2008; Leontowicz et al., 2008; Toledo et al., 2008; Charoensiri et al., 2009; Haruenkit et al., 2010; Poovarodom et al., 2010). The antioxidant activity of Monthong cultivar determined by ferric-reducing/antioxidant power (FRAP), cupric reducing antioxidant capacity (CUPRAC) and 2, 20 -azinobis (3-ethylbenzothiazoline-6-sulfonic acid-diammonium salt) (ABTS) with Trolox equivalent antioxidant capacity (TEAC) assays was significantly higher than in Kradum and in Kan Yao cultivars. The correlation coefficients between polyphenols, flavonoids, flavanols and FRAP, CUPRAC and TEAC capacities were highly significant (Apak et al., 2004; Toledo et al., 2008). The bioactivity of durian cultivars Monthong, Chanee and Puangmanee was high and the total polyphenols were the main contributors to the overall antioxidant capacity. The total polyphenols, flavonoids, flavanols, ascorbic acid, tannins and the antioxidant activity determined by four assays (CUPRAC, DPPH, ABTS, and FRAP) differed in immature, mature, ripe and overripe samples. The content of polyphenols and antioxidant activity were the highest in overripe durian, flavonoids were the highest in ripe durian, and flavanols and antiproliferative activity were the highest in mature durian (Haruenkit et al., 2010; Chingsuwanrote et al., 2016). The results in vitro are comparable with other fruits widely used in human diets. Durian can be used as a supplement for nutritional and health purposes, especially Monthong, Chanee, and Puangmanee cultivars (Toledo et al., 2008). The antioxidant properties of durian at different stages of ripening showed that total polyphenols, flavonoids, anthocyanins, and flavanols in ripe durian were significantly higher than in mature and overripe fruits.
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Caffeic acid and quercetin were the dominant antioxidant substances in ripe durian. The bioactivity of ripe durian was high and the total polyphenols were the main contributors to the overall antioxidant capacity (Arancibia-Avila et al., 2008). Based on the results, durian cultivars can be used as a relatively new source of antioxidants (Leontowicz et al., 2007).
Fatty Acids It has been reported that durian has additional valuable health properties: polysaccharide gel from the fruit hulls reacts on immune responses and is responsible for cholesterol reduction (Chansiripornchai and Pongsamart, 2008). The health properties of durian are based not only on the antioxidant properties, but also on its fatty acid composition. Cholesterol hypothesis implies that reducing the intake of saturated fats and cholesterol while increasing that of polyunsaturated oils is effective in lowering serum cholesterol, and thereby in reducing coronary heart disease. The protective activity is linked with a high supply of n-3 fatty acids coming from fish and seafood, and high consumption of whole grain products, as well as fruits and vegetables (Siondalski and Lysiak-Szydlowska, 2007). Durian is rich in n-3 fatty acids, compared to some other fruits (Phutdhawong et al., 2005).
Carbohydrates The unripe durian pulp contains about 2326% starch and decreases rapidly during ripening, while soluble solids and total sugars increase rapidly with ripening (Ketsa and Pangkool, 1995a; Ketsa and Daengkanit, 1998a). This decrease in starch accompanies an increase in soluble solids and total sugars, is typical of postharvest changes in the carbohydrates of durin fruits (Ketsa and Pangkool, 1994; Ketsa and Pangkool, 1995b). Reducing sugars (glucose and fructose) and nonreducing sugars (sucrose) rapidly increase with ripening. Cv. Chanee pulp has more reducing sugars than that of cv. Monthong. In contrast, pulp of cv. Monthong contains more nonreducing sugars than that of cv. Chanee, with nonreducing sugars made up 7080% of the total sugars. Therefore, sucrose has an important role in sweetening in ripening durian pulp. The total sugar content in the pulp of cv. Chanee is higher than that of cv. Monthong. This can explain why the ripe pulp of cv. Chanee tastes sweeter than that of cv. Monthong (Sutthaphan, 1993). This makes ripe durian pulp very sweet, with a richness of taste unlike any other fruit.
Carotenoids Both α-carotene and β-carotene contents are the main carotenoid in the durian pulp and they gradually increase with maturity (Wisutiamonkul et al., 2015a) and ripening (Ketsa and Pangkool, 1995a; Wisutiamonkul et al., 2015a). β-carotene content is about five times higher than α-carotene (Isabelle et al., 2010), i.e. β-carotene represents about 70% of the total carotenoids (Khoo et al., 2008). The pulp of ripening durian cv. Chanee contains two to three times more β-carotene than that of cv. Monthong (Charoensiri et al., 2009; Wisutiamonkul et al., 2015a). Pulp carotenoid concentration in ripe fruit is related to the deepness of the yellow color (Wisutiamonkul et al., 2015a). This may be due to the increase in β-carotene synthesis in the pulp during ripening (Wisutiamonkul et al., 2015b). This can explain why the pulp of cv. Chanee is a darker yellow than that of cv. Monthong (Wisutiamonkul et al., 2015a). Wisutiamonkul et al. (2017b) have recently reported that 1-MCP influenced carotenoid accumulation in the pulp. This effect on the carotenoid accumulation pattern was highly correlated with the expression of key genes in carotenoid biosynthetic pathway such as ζ-carotene desaturase (ZDS), lycopene β-cyclase (LCYB), chromoplast specific lycopene β-cyclase (CYCB), and β-carotene hydroxylase (BCH). Carotenoid accumulation in durian appears to be regulated by endogenous ethylene through modulation of pathway gene expression. In addition, durian cultivars Chanee, Kradom, and Puangmanee, with their yellow to deep-yellow color pulp, have the highest carotenoid content compared to cultivars with light yellow pulp (Kongkachuichai et al., 2010).
Sensory Characteristics The sensory properties of fresh durian combine a pleasant creamy consistency, a pronounced sweet taste, and a strong, penetrating odor, not comparable to that of any other kind of fruit. The aroma of ripe durian is unique. The typical durian aroma at ripe stage can be detected one day before the respiratory peak (Tongdee et al., 1988; Nanthachai et al., 1994). The presence of strong odor and flavor development during ripening is due to the production of volatile compounds. The sulfur containing compounds and esters were consistently cited as having a major impact on the characteristic aroma and flavor of the fresh pulp. Only propanethiol and ethyl α-methyl butyrate were the
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predominant constituents of the odor of durian (Baldry et al., 1972). Thirty-eight volatile compounds were identified in the fresh durian flesh, of which eleven were esters, ten alcohols, six carboxylic acids, six sulfurous and nitrogenous compounds, and five hydrocarbons. Processed durian fruit leather retained most of the aroma components of fresh durian fruit. During storage, the relative proportion of acids in the product increased. Esters, alcohols and aldehydes during storage decreased, while hydrocarbons, phenolic, sulfurous and nitrogenous compounds fluctuated (Jaswir et al., 2008). Maninang et al. (2011) reported 137 volatile compounds in ripening durian. The effect of maturity on the volatile profile of the durian pulp is apparently more striking in cv. Chanee than in cv. Monthong. This makes ripe cv. Chanee stronger aroma than ripe cv. Monthong. In cv. Chanee, 17 volatile compounds were found in 100% maturity fruits but only 13 were detected at 7585% maturity, with the difference mainly attributed to the ester compounds (Maninang et al., 2011). This is why ripe durian with less maturity has a weaker aroma than ripe durian with more maturity. Li et al. (2012) recently reported that new 24 odor-active compounds in the flavor cv. Monthong that had not been reported in durian before. Among these, 1-(propylsulfanyl)ethanethiol, 1-{[1-(methylsulfanyl) ethyl]-sulfanyl}ethanethiol, and 1-{[1-(ethylsulfanyl) ethyl] sulfanyl}ethanethiol were reported for the first time in a natural product.
HARVEST AND POSTHARVEST CONSERVATION Harvest Season In Thailand and Malaysia, peak harvest is between June and July; in Indonesia, October to February; and in the Philippines, August to September. However, it has been observed that harvest period varies with elevation and cultivar. Orchards in low elevations tend to produce fruits early, August to September. Durian is a seasonal fruit produced once a year. The marketing periods differ according to the growing region. In Thailand, early maturing cultivars are harvested between 95 and 105 days after bloom while late cultivars are harvested after 130 days or more. The durian season in the major durian-growing countries of Thailand, west Malaysia, and Indonesia generally peaks in the middle of the year around JuneJuly. Harvest seasons are quite short, generally lasting 12 months.
Harvesting The maturity of the durian fruits is determined by combined techniques: day count, character of fruit spines, tapping the fruit, the color and shape of the fruit (Yaacob and Subhadrabandhu, 1995) and dry matter (Siriphanich and Khurnpoon, 2003). Dry matter of the pulp is now reliably accepted by growers. In Thailand, most of the mature fruits are harvested manually and then allowed to ripen. In Malaysia, Indonesia and the Philippines, mature fruits ripen on the trees, drop naturally and are collected later. Natural fruit drop usually last about 10 weeks and follows a specific pattern: a few during the first week, then peaking in the second and third week and decreasing again in the later weeks. A grower will harvest mature fruits at the correct harvesting indices or allow the fruits to drop naturally. Harvested fruit should not be placed on the ground to avoid contact with dirt and infection by pathogens.
Ripening Durian is a climacteric fruit (Booncherm and Siriphanich, 1991), which means that its ripeness is regulated by ethylene. Ethylene treatment can accelerate ripening and dehiscence of maturity, while inhibition of ethylene action and scrubbing can delay their ripening. Durian can be ripened with ethylene (Ketsa and Pangkool, 1995b) or ethephon (Cheyglinted, 1993). Ethylene gaseous or liquid ethylene treatment induces peel yellowing or even browning of durian fruits. Consumers do not prefer fruit treated with ethylene because they think these fruits are not fresh. For this reason many growers, wholesalers, and retailers in Thailand induce durian ripening by quickly dipping the fruit stalk (fruit stem) into a high concentration of ethephon solution, or brush the stalk with such a solution without husk yellow when ripened. Concentrations of ethephon applied vary mostly between about 30005000 μL/L or higher. This treatment prevents peel yellowing or browning (Paull and Ketsa, 2015), but at too high concentration can cause the fruit stalk to be abscised. Cheyglinted (1993) showed that ethephon treatment with cv. Chanee fruit harvested at 75% maturity either failed to ripen or ripened abnormally, whilst fruit harvested at 85% maturity reached good eating quality. Normal ripening such as yellowing of the pulp and development of full flavor and aroma of fruit harvested at 75% maturity was obtained
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if treated with 1000 or 2000 μL/L ethephon at the fruit stalk. Fruit ripened at a lower relative humidity (75%) have a better eating quality that is less juicy and easier to open up the husk than fruit ripened at higher relative humidity.
Surface Coating Durian fruit have high rates of weight loss after harvest (Ketsa and Pangkool, 1994). Therefore, it is imperative to reduce weight loss of durian fruit after harvest. Waxing or surface coating of durian has been reported to increase the resistance of the peel to gas exchange, thus creating modified atmosphere internally to extend fruit life (Tongdee et al., 1990a). Waxing reduces ripening processes, weight loss and dehiscence. An˜abesa et al. (2006) reported a delay of dehiscence in durian fruit after waxing, which prevented water loss.
1-MCP 1-MCP is an ethylene action inhibitor (Blankenship and Dole, 2003). 1-MCP treatment inhibited ethylene production and ripening of durian fruit. In addition, inhibitory effect of 1-MCP on their activities was much higher at 25 C than at 15 C (Amornputti et al., 2016). 1-MCP can be used to delay ripening processes of durian fruit and increase shelf life at ambient temperature and storage life at low temperature (Amornputti et al., 2014). Fumigation of durian with 1-MCP ranged 10002000 ppb depending on cultivar, temperature and time, can delay increase of TSS, softening, color, and aroma development (Ratanachinakorn et al., 2007; Maninang et al., 2011). Thai exporters have adopted a 6-h 1-MCP fumigation to delay ripening. Care is needed to avoid high rate of 1-MCP fumigation that can lead to an abnormal ripening such as uneven ripening and hardening pulp.
Storage The storage temperature of durian cannot be lower than 13.5 C because of the risk of chilling injury (CI) (Romphophak et al., 1997). As a result of CI, the peel turns dark brown starting at the base of the spines, while the pulp shows loss of aroma and does not soften (Booncherm and Siriphanich, 1991). When stored at 15 C, durian has an extended shelf life up to 35 days compared to ambient temperature (Amornputti et al., 2014). Relative humidity of 8595% is best. The pulp of half to near full ripe fruit is much less sensitive to chilling injury than the peel, and the pulp can be stored for 4 weeks at 5 C. Although modified and controlled atmospheres (MA and CA) delayed durian ripening (Mohamed,1990; Tongdee et al., 1990a, 1990b; Ratanachinakorn et al., 2000), commercial CA or MA storage has still not been adopted (Siriphanich, 1996). The minimally processed durian fruit could be kept at 4 C for 14 days with acceptable microbiological count and without off-odor development. At ambient temperature, minimally processed durian could only be stored for 1 day after which the pulp became acidified (Voon et al., 2006).
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Fresh Fruit Durian is a favorite among Hong Kong residents because they consider it as a medicine to give heat to the body. Hong Kong prefers edible or soft ripe durian, thus most of consumption is supplied from Thailand. The annual amount of domestic demand is estimated around 500010,000 tons, of which 90% is supplied by imports from Thailand and the remainder from Malaysia. Most durian demand is met by imports from Thailand. Taiwan is the destination of half of the fresh durian exported from Thailand (36,000 tons in 1997). The consumer prefers good quality durian, Monthong is believed to be the best eating quality, so most imports are Monthong cv. followed by Chanee. The major export market is Asia, specifically China, Taiwan, Hong Kong, Singapore, and Brunei. China, Taiwan, and Hong Kong prefer the edible or soft ripe durians with a mild aroma, thus imports are mostly from Thailand. Singaporeans like to consume the overripe fruit like Malaysians. Normally Singapore imports 25,000 tons of fresh durian mostly from Malaysia and Thailand. Malaysia accounts for 80% of the total imports. Thailand supplies 20% of total imports during April and May before the harvesting season of Malaysian durian. China is becoming an important import market with high potential due to the large population with an increasing income. Thailand supplies most of the domestic demand. The import channel from Thailand is made via Hong Kong with an estimate that 85% of its export to Hong Kong was re-exported to China (the equivalent of 20,00025,000 tons in 1997).
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Durian Products The market values of fresh durians of the ASEAN countries increase every year in both local and export markets because durian is one of the most popular fruits in this region (Subhadrabandhu and Ketsa, 2001). However, the price of fresh durian fruit fluctuates annually depending on the supply. If oversupply happens, then the price of fresh durian will be lowered and vice versa. This has encouraged new innovative products from the excess of fresh fruit. Many more durian products have been developed in recent years, possibly because new ways of eating the fruit have been so well received. Durian aril can be processed into several products such as minimally processed durian, frozen durian, powder, paste, chips, icecream, candy, milkshakes, candles, jams, rolls, tarts, and pies. These durian products have become increasingly popular in both local and export markets. Moreover, minimally processed durian has become increasingly popular. Many consumers love to eat fresh durian; others would like to try fresh durian but they do not want the whole fruit because it is too big for them or they do not know how to open up the husk. Therefore, they prefer to buy a small portion of durian pulp. This leads to the sale of minimally processed durian which may contain 1 or 2 locules of the pulp held on a polystyrene tray wrapped with plastic film. This product has become popular in both supermarkets and roadside markets. However, this product can only be kept for 12 days at ambient temperature and longer a few days at lower temperatures (Voon et al., 2006).
Durian Husk The edible part of the durian fruit (technically a capsule) is the fleshy aril that surrounds the seed, representing 2035% of the fruit weight. After fresh consumption of durian, there is a biomass of 6580% husk. This creates a huge amount of raw agricultural waste product. Therefore, physical and chemical properties of durian have intensively studied (Wilaipon, 2011; Bujang, 2014; Aimi et al., 2015). Data about durian husks have led to advanced innovation development of durian biomass in areas such as adsorption science, bioplastic film, plywood, fiberboard, biofuel, plant growing media, building insulation, pharmaceutical and food manufacturing products (Foo and Hameed, 2011; Wiyaratn and Watanapa, 2012; Bujang, 2014). Because the world production of durian still increases every year, the resultant durian biomass becomes more available for further new product development.
CONCLUDING REMARKS Many ASEAN countries have commercially grown durian that is exported worldwide. Durian fruit is now accepted internationally as more and more consumers have discovered its appeal. In addition, durian products including processing and biomass give pathways for new innovative development. Therefore, durian fruit have great potential in international markets.
REFERENCES Aimi, M.N.N., Anuar, H., Maizirwan, M., Sapuan, S.M., Wahit, M.U., Zakaria, S., 2015. Preparation of durian skin nanofibre (DSNF) and its effect on the properties of polylactic acid (PLA) biocomposites. Sains Malays. 44, 15511559. Amornputti, S., Ketsa, S., van Doorn, W.G., 2014. Effect of 1-methylcyclopropene (1- MCP) on storage life of durian fruit. Postharvest Biol. Technol. 97, 111114. Amornputti, S., Ketsa, S., van Doorn, W.G., 2016. 1-Methylcyclopropene (1-MCP) inhibits ethylene production of durian fruit which is correlated with a decrease in ACC oxidase activity in the peel. Postharvest Biol. Technol. 114, 6975. An˜abesa, M.S., Oria, D.V., Esguerra, E.B., Sarcos, M.A., 2006. Postharvest behavior and storage life of 3 durian cultivars with varying maturity, waxing and temperature. Philippines J. Crop Sci. 31, 2946. Apak, R., Guclu, K., Ozyurek, M., Karademir, S.E., 2004. Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. J. Agric. Food Chem. 52, 79707981. Arancibia-Avila, P., Toledo, F., Park, Y.-S., Jung, S.-T., Kang, S.-G., Heo, B.G., et al., 2008. Antioxidant properties of durian fruit as influenced by ripening. LWT-Food Sci. Technol. 41, 21182125. Asiedu, J.J., 1987. Physiological changes in plantain (Musa paradisiacal) during ripening and the effect of the degree of ripeness on drying. Trop. Sci. 27, 222249222260. Atta-Aly, M.A., 1992. Effect of high temperature on ethylene biosynthesis by tomato fruit. Postharvest Biol. Technol. 2, 1924. Baldry, J., Dougan, J., Howard, G.E., 1972. Volatile flavoring constituents of durian. Phytochemistry. 11, 20812084. Blankenship, S., Dole, J.M., 2003. 1-Methylcyclopropene: a review. Postharvest Biol. Technol. 28, 125. Booncherm, P., 1990. Physiological Changes in Durian (Durio zibethinus Murr.) cv. Chanee After Harvest. M.Sc. Thesis. Kasetsart University, Bangkok.
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Booncherm, P., Siripanich, J., 1991. Postharvest physiology of durian pulp and husk. Kasetsart J. (Nat. Sci. Suppl.). 25, 119125. Bujang, A.S., 2014. Utilization of Durian Biomass for Biorenewable Applications. Ph.D. thesis.Iowa State University, Iowa. Burton, W.G., 1982. Post-harvest Physiology of Food Crops. Longman, London. Chansiripornchai, N., Chansiripornchai, P., Pongsamart, S., 2008. A preliminary study of polysaccharide gel extracted from the fruit hulls of durian (Durio zibethinus) on immune responses and cholesterol reduction in chicken. Acta Hortic. 786, 5760. Charoensiri, R., Kongkachuichai, R., Suknicom, S., Sungpuag, P., 2009. Beta-carotene, lycopene, and alpha-tocopherol contents of selected Thai fruits. Food Chem. 113, 202207. Chayprasat, P. 1993. Enzymes and Intermediates in Ethylene Production of Durian Fruits. M.Sc. thesis. Kasetsart University, Bangkok. Cheyglinted, S. 1993. Effect of Ethephon on the Physio-chemical Changes During the Ripening of ‘Chanee’ Durian (Durio zibethinus Murray) Harvested at Different Maturity Stages. M.S. thesis. The University of Philippines, Los Banos. Chingsuwanrote, P., Muangnoi, C., Parengam, K., Tuntipopipat, S., 2016. Antioxidant and anti-inflammatory activities of durian and rambutan pulp extract. Int. Food Res. J. 23, 939947. Foo, K.Y., Hameed, B.H., 2011. Transformation of durian biomass into a highly valuable end commodity: Trends and opportunities. Biomass Bioenergy. 35, 24702478. Gorinstein, S., Poovarodom, S., Leontowicz, H., Leontowicz, M., Namiesnik, J., Vearasilp, S., et al., 2011. Antioxidant properties and bioactive constituents of some rare exotic Thai fruits comparison with conventional fruits in vitro and in vivo studies. Food Res. Int. 44, 22222232. Haruenkit, R., Poovarodom, S., Vearasilp, S., Namiesnik, J., Sliwka-Kaszynska, M., Park, Y.-S., et al., 2010. Comparison of bioactive compounds, antioxidant and antiproliferative activities of Mon Thong durian during ripening. Food Chem. 118, 540547. Ho, L.-H., Bhat, R., 2015. Exploring the potential nutraceutical values of durian (Durio zibethinus L.) an exotic tropical fruit. Food Chem. 168, 8089. Imsabai, W., 1999. Effect of Temperature on Ripening in ‘Chanee’ Durian. M.Sc. thesis. Kasetsart University, Bangkok. Imsabai, W., Ketsa, S., van Doorn, W.G., 2002. Effect of temperature on softening and the activities of polygalacturonase and pectinesterase in durian fruit. Postharvest Biol. Technol. 26, 347351. Isabelle, M., Lee, B.L., Lim, M.T., Koh, W.P., Huang, D., Ong, C.N., 2010. Antioxidant activity and profiles of common fruits in Singapore. Food Chem. 123, 7784. Jaswir, I., Man, Y.B.C., Selamat, J., Ahmad, F., Sugisawa, H., 2008. Retention of volatile components of durian fruit leather during processing and storage. J. Food Process. Preserv. 32, 740750. Kasiolarn, H., 1991. Post-harvest Physiology of Sugar Apple (Annona squamosa Linn.) and Storage of Atemoya (Annona x ‘Africa Pride’) Fruit. M. Sc. thesis. Kasetsart University, Bangkok. Ketsa, S., 1990. Effect of fruit size on weight loss and shelf life of tangerines. J. Hortic. Sci. 65, 485488. Ketsa, S., Pangkool, S., 1994. The effect of humidity on ripening of durians. Postharvest Biol. Technol. 4, 159165. Ketsa, S., Pangkool, S., 1995a. Ripening behaviour of durians (Durio zibethinus Murray) at different temperatures. Trop. Agric. (Trinidad). 72, 141145. Ketsa, S., Pangkool, S., 1995b. The effect of temperature and humidity on the ripening of durian fruits. J. Hortic. Sci. 70, 827831. Ketsa, S., Daengkanit, T., 1998a. Physiological changes during postharvest ripening of durian fruit (Durian zibethinus Murray). J. Hortic. Sci. Biotechnol. 73, 575577. Ketsa, S., Daengkanit, T., 1998b. Changes in softening enzymes of durian fruit during ripening. Acta Hortic. 464, 451454. Ketsa, S., Daengkanit, T., 1999a. Firmness and activities of polygalacturonase, pectinesterase, β -galactosidase and cellulase in ripening durian harvested at different stages of maturity. Sci. Hortic. 80, 181188. Ketsa, S., Daengkanit, T., 1999b. Softening of durian cultivars. J. Plant Physiol. 154, 408411. Khoo, H.E., Ismail, A., Mohd-Esa, N., Idris, S., 2008. Carotenoid content of underutilized tropical fruits. Plant Foods Hum. Nutr. 63, 170175. Khurnpoon, L., 2007. Changes in cell wall composition and enzyme activities in husk dehiscence of ‘Monthong’ durians. Ph.D. thesis. Kasetsart University, Bangkok. Khurnpoon, L., Siriphanich, J., Labavitch, J.M., 2008. Cell wall metabolism during durian fruit dehiscence. Postharvest Biol. Technol. 48, 391401. Kongkachuichai, R., Charoensiri, R., Sungpuag, P., 2010. Carotenoid, flavonoid profiles and dietary fiber contents of fruits commonly consumed in Thailand. Int. J. Food Sci. Nutr. 61, 536548. Kosiyachinda, S., Tansiriyakul, S., 1988. Respiration rate and ethylene production of fresh fruit, vegetables and cut flowers. Food. 18, 18. Lam, P.F., Kosiyachinda, K., Licada, M.C.C., Mendoza Jr., D.B., Prabawati, S., Lee, S.K., 1987. Postharvest physiology and storage of rambutan. In: Lam, P.F., Kosiyachinda, S. (Eds.), Rambutan: Fruit Development, Postharvest Physiology and Marketingin ASEAN. ASEAN Food Handling Bureau, Kuala Lumpur, pp. 3950. Leontowicz, H., Leontowicz, M., Haruenkit, R., Poovarodom, S., Jastrzebski, Z., Drzewiecki, J., et al., 2008. Durian (Durio zibethinus Murr.) cultivars as nutritional supplementation to rat’s diets. Food Chem. Toxicol. 46, 581589. Leontowicz, M., Leontowicz, H., Jastrzebski, Z., Jesion, I., Haruenkit, R., Poovarodom, S., et al., 2007. The nutritional and metabolic indices in rats fed cholesterol containing diets supplemented with durian at different stages of ripening. Biofactors. 29, 123136. Li, J.-X., Schieberle, P., Steinhaus, M., 2012. Characterization of the major odor-octive compounds in Thai durian (Durio zibethinus L. ‘Monthong’) by aroma extract dilution analysis and headspace gas chromatography 2 olfactometry. J. Agric. Food Chem. 60, 1125311262. Maninang, J.S., Wongs-Aree, C., Kanlayanarat, S., Sugaya, S., Gemma, H., 2011. Influence of maturity and postharvest treatment on the volatile profile and physiological properties of the durian (Durio zibethinus Murray) fruit. Int. Food Res. J. 18, 10671075.
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Mohamed, K., 1990. Extending the shelf life of fresh durian. ASEAN Food J. 5, 117119. Nanthachai, S., Siriphanich, J., Wahab, A.R., Kosiyachinda, S., 1994. Harvesting indices and harvesting. In: Nanthachai, S. (Ed.), Durian: Fruit Development, Maturity, Handling and Marketing in ASEAN. ASEAN Food Handling Bureau, Kuala Lumpur, pp. 7788. Palapol, Y., Kunyamee, S.M., Thongkhum, M., Ketsa, S., Ferguson, I.B., van Doorn, W.G., 2015. Expression of expansin genes in the pulp and the dehiscence zone of ripening durian (Durio zibethinus) fruit. J. Plant Physiol. 182, 3339. Pantastico, E.B., Lam, L.F., Ketsa, S., Yunitari, Kosittrakul, M., 1984. Post-harvest physiology and storage of mango. In: Mendoza Jr., D.B., Wills, R.B.H. (Eds.), Mango: Fruit Development, Postharvest Physiology and Marketing in ASEAN. ASEAN Food Handling Bureau, Kuala Lumpur, pp. 3952. Paull, R.E., Ketsa, S., 2014. Durian: Postharvest quality-maintenance quidelines. Cooperative Extension. University of Hawaii at Manoa. Available Source: http://www.ctahr.hawaii.edu/oc/freepubs/pdf/F_N-27.pdf. Phutdhawong, W., Kaewkong, S., Buddhasukh, D., 2005. GCMS analysis of fatty acids in Thai durian aril. Chiang Mai J. Sci. 32, 169172. Polprasid, P., 1960. Durian flowers. Kasikorn. 33, 3745. Poovarodom, S., Haruenkit, R., Vearasilp, S., Namiesnik, J., Cvikrova, M., Martincova, O., et al., 2010. Comparative characterisation of durian, mango and avocado. Int. J. Food Sci. Technol. 45, 921929. Ratanachinakorn, B., Siriphanich, J., Phumgiran, J., 2000. Prolong storage life of durian by controlled atmospheres. Research Report on Research program for Development of Production and Marketing of Durian for Export. National Research Council of Thailand, Bangkok, pp. 372434. Ratanachinakorn, B., Sujarittaweesuk, U., Jangchud, A., 2007. Effect of 1-methylcyclopropene concentration on durian ripening. Agric. Sci. J. 38: 5 (Suppl.), 9598. Reksodihardjo, W.S., 1962. The species of Durio with edible fruits. Econ. Bot. 16, 270282. Roberts, J.A., Elliott, K.A., Gonzales-Carranza, Z.H., 2002. Abscission, dehiscence, and other cell separation processes. Annu. Rev. Plant Biol. 53, 131158. Romphophak, T., Kunprom, J., Siriphanich, J., 1997. Storage of durians on a semi-commercial scale. Kasetsart J. (Nat. Sci.). 31, 141154. Sangwanangkul, P., 1998. Growth and Development of Durian Fruit cv. Monthong and the Effect of Ethephon Preharvest Treatment. M.Sc. thesis. Kasetsart University, Bangkok. Siondalski, P., Lysiak-Szydlowska, W., 2007. Food components in the protection of the cardiovascular system. In: Sikorski, Z.E. (Ed.), Chemical and Functional Properties of Food Components. CRC Press, Boca Raton, pp. 439450. Siriphanich, J., 1996. Storage and transportation of tropical fruits: a case study on durian. In: Vijaysegaran, S., Pauziah, M., Mohamed, M.S., Ahmed Tarmizi, S. (Eds.), Proceedings of the International Conference on Tropical Fruits. MARDI, Kuala Lumpur, pp. 439451. Siriphanich, J., Khurnpoon, L., 2003. Dry matter as a possible maturity index of ‘Monthong’ durians. Thai J. Agric. Sci. 37, 365372. Sriyook, S., Siriatiwat, S., Siriphanich, J., 1994. Durian fruit dehiscence-water status and ethylene. HortScience. 29, 11951198. Subhadrabandhu, S., Ketsa, S., 2001. Durian: King of Tropical Fruit. Daphne Brasell Associates Ltd, Wellington. Subhadrabandhu, S., Schneemann, J.M.P., Verheij, E.W.M., 1991. Durio zibethinus Murray. In: Verheij, E.W.M., Coronel, R.E. (Eds.), Plant Resource of South-East Asia No2: Edible Fruits and Nuts. Pudoc, Wageningen, pp. 157161. Sutthaphan, S., 1993. Post-Harvest Changes in Chemical Composition of Chanee and Mon Thong Durian Pulp. M.Sc. thesis. Kasetsart University, Bangkok. Toledo, F., Arancibia-Avila, P., Park, Y.S., Jung, S.T., Kang, S.G., Gu, et al., 2008. Screening of the antioxidant and nutritional properties, phenolic contents and proteins of five durian cultivars. Int. J. Food Sci. Nutr. 59, 415427. Tongdee, S.C., Chayasombat, A., Neamprem, S., 1988a. Respiration, ethylene production and changes in the internal atmosphere of durian (Durio zibethinus Murr.). Proceedings of the Seminar on Durian. Thailand Institute of Scientific and Technological Research, Bangkok, pp. 2230. Tongdee, S., Suwanagul, C., Neamprem, S., Bunruengsri, U., 1990a. Effect of surface coatings on weight loss and internal atmosphere of durian (Durio zibethinus Murray) fruit. J. ASEAN Food. 5, 103107. Tongdee, S.C., Suwanagul, C., Neamprem, S., 1990b. Durian fruit ripening and the effect of variety, maturity stage at harvest, and atmospheric gases. Acta Hortic. 269, 323334. Voon, Y.Y., Sheikh Abdul Hamida, N., Rusul, G., Osmana, A., Quek, S.Y., 2006. Physicochemical, microbial and sensory changes of minimally processed durian (Durio zibethinus cv. D24) during storage at 4 and 28 C. Postharvest Biol. Technol. 42, 168175. Wilaipon, P., 2011. Durian husk properties and its heating value equation. Am. J. Appl. Sci. 8, 893896. Wisutiamonkul, A., Ketsa, S., van Doorn, W.G., 2015a. Carotenoids in durian fruit pulp during growth and postharvest ripening. Food Chem. 180, 301305. Wisutiamonkul, A., Ketsa, S., van Doorn, W.G., 2015b. Endogenous ethylene regulates accumulation of α- and β-carotene in the pulp of harvested durian fruit. Postharvest Biol. Technol. 110, 1823. Wisutiamonkul, A., Ampomah-Dwamena, C., Allan, A.C., Ketsa, S., 2017a. Carotenoid accumulation and gene expression during durian (Durio zibethinus) fruit growth and ripening, Sci. Hortic. 220, 233242. Wisutiamonkul, A., Ampomah-Dwamena, C., Allan, A.C., Ketsa, S., 2017b. Carotenoid accumulation in durian (Durio zibethinus) fruit is affected by ethylene via modulation of carotenoid pathway gene expression. Plant Physiol. Biochem. 115, 308315. Wiyaratn, W., Watanapa, A., 2012. A Study on mechanical properties of fiberboard made of durian rind through latex with phenolic resin as binding agent. Int. J. Chem. Mol. Nucl. Mater. Metal. Eng. 6, 407410. Yaacob, O., Subhadrabandhu, S., 1995. The Production of Economic Fruits in South-East Asia. Oxford University Press, Kuala Lumpur.
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FURTHER READING Ketsa, S., Pangkool, S., 1995. Effect of maturity stages and ethylene treatment on ripening of durian fruits. In: Frisinia, C., Mason, K., Faragher, J. (Eds.), Proceedings of Australasian Postharvest Conference. Science and Technology for Fresh Food Revolution, Melbourne, pp. 6772. Leontowicz, H., Leontowicz, M., Jesion, I., Bielecki, W., Poovarodom, S., Vearasilp, S., et al., 2011. Positive effects of durian fruit at different stages of ripening on the hearts and livers of rats fed diets high in cholesterol. Eur. J. Intergr. Med. 3, e169e181. Tongdee, S.C., Chayasombat, A., Neamprem, S., 1988. Effect of harvest maturity on respiration, ethylene production and the composition of internal atmosphere of durian (Durio zibethinus Murr.). In: Proceedings of the Seminar on Durian. Thailand Institute of Scientific and Technological Research, Bangkok, pp. 3136.
Elderberry—Sambucus nigra L. Sueli Rodrigues1, Edy Sousa de Brito2 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Postharvest Estimated Production Biochemical and Physiology
181 182 182 183
Chemical Composition and Nutritional Value Industrialization References
183 184 185
CULTIVAR ORIGIN AND BOTANICAL ASPECTS The plants of the genus Sambucus are called elderberry in English and sauco in Spanish. The genus Sambucus L. (Caprifoliaceae) comprises more than 20 species widely distributed in temperate and subtropical zones (Valle`s et al., 2004). Sambucus are deciduous shrubs reaching the height of 13 m or small trees native mostly to the northern hemisphere (Fig. 1). The plant stems are smooth and numerous. The younger ones contain a large white pith. The large leaves present 511 leaflets with 513 cm in length that are borne on short stalks. The fragrant flowers (Fig. 2) are white flat-topped and the flower season is June or July, when the 5-lobed, wheel-shaped, creamy-white flowers clusters appear. The clustered flowers are pollinated by insects, especially by hoverflies. The small, round, shining, and juicy fruits are edible and appear as clusters with a black or dark purple color (Fig. 3) (Sievers, 1930). The hermaphroditic flowers are small and borne in flat umbels. The small fruits (0.30.6 cm) are produced in large clusters that are very dark purple or nearly black in color. In some species, the fruit color ranges from bright red to blue and dark purple (Lee et al., 2005; Moerman, 2002; Stange, 1990; Ritter and Mcakee, 1964). The fruit is strongly appreciated by birds, which contributes to the plant spread. Aside from the forest edges, Sambucus grows in fence lines, along roadways and railways. The large pinnately leaves are usually dark green. However, ornamental selected species present in lime green and dark purple leaves that are appreciated for landscapes. Among the Sambucus species, the most cultivated and studied are Sambucus nigra L. (native from Europe and western Asia) and S. nigra ssp. canadensis (native to eastern North America; with blueblack berries). Sambucus canadensis is cultivated in the USA for the fruit. S. canadensis leaves are large and the stems are hollow or pithy. The fruits are produced in large flat clusters (1522 cm) and the individual berries are small (0.40.6 cm in diameter), globose, with prominent seeds. Colors vary from red to blueblack. The fruits are harvested from the wild in considerable quantities (Magness and Markle, 1971). S. nigra is throughout Europe and Asia. In the Denmark, the tree is commercially cultivated as a colorant for juices and wine production. S. nigra is predominantly a shrub in open areas and woodland edges and is associated with eutrophic and disturbed soils (Atkinson and Atkinson, 2002). The elderberry cultivars in North America are from New York Agricultural Experiment Station or Agriculture and Agri-Food Canada in Nova Scotia. The commercial cultivars are named Adams I, Adams II, Johns, York, and Nova (Finn et al., 2008). The cultivar Wyldewood was introduced by the scientist from the University of Missouri and is described as a tall and vigorous plant with high yield and high harvesting efficiency to produce fruits for processing (Cernusca et al., 2011).
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00023-X © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Elberberry plant.
FIGURE 2 Elderberry flowers.
POSTHARVEST The first flourishing is usually in the third or fourth year and the first crop of fruits is possible from 4-year-old bushes. The plants produce large amounts of fruit and viable seed every year, except for shrubs that grew in the deep shade inside woodland, which may produce few or no flowers (Atkinson and Atkinson, 2002).The mild-flavored fruits ripen in mid- to late summer in the northern hemisphere (6090 days before flowering). The flowers appear from May to July, and the fruits are harvested in September and October (Magness and Markle, 1971). The fruit harvesting is difficult because the fruit clusters are not easily separated. Thus the entire cluster is usually picked, and the crop is processed into juices, extracts, or puree (Cernusca et al., 2011).
ESTIMATED PRODUCTION According to a market study carried out in the USA (Cernusca et al., 2011), little official information has been published regarding production volume and costs. The study concluded that about 90,000 lb/year of fresh or frozen elderberries are industrially processed in products ranging from jam and jelly to syrup and wine. The price was $01.5/kg of fruit in 2009. The concentrated juice is exported to Europe, where the market is more consolidated. The local trade is mainly for jams and jelly made by small companies in midwestern US, where the fruits are cultivated and picked by the producers. Large companies purchase high amounts of fresh fruits from growers, with only a verbal contract.
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183
FIGURE 3 Elderberry fruits.
Wineries purchase concentrated juice from the national producers. The juice producers require large amounts and higher production investments. The juice and wine market can be complemented with the nutraceuticals and organic colorings promoting the sales expansion and encouraging the producer’s growth (Cernusca et al., 2011).
BIOCHEMICAL AND PHYSIOLOGY The fruit changes during the fruit ripening process. Titratable acid content declines while the anthocyanin and soluble solids contents increases. Changes in amino acid concentration and composition during the ripening and senescence of S. nigra is characterized by a decrease of the total (bound and free) amino acid content in ripe fruit. The amino acid content declines initially and then rises at the maturity stage. This behavior is attributed to the increase in leucine, tyrosine, and phenylalanine, the predominant free amino acids in the fully developed fruit. The fruit senescence is characterized by a marked increase in free amino acids with a slight decrease in the bound amino acids content in ripe fruit. Cyanogenic glycosides have been reported from S. nigra. The most commonly reported is the sambunigrin, followed by prunasin and m-hydroxysubstituted glycosides. The Danish species present zierin and holocalin. S. nigra collected in sourthern Italy presented sambunigrin, prunasin, holocalin and its acetyl derivative, as well as 2S-β-D-apio-D-furanosyl(1-2)-β-D-glucopyranosylmandelonitrile, a new glycoside found in the fruit. Sambunigrin and prunasin are phytotoxic. Three cyanohydrins isolated from southern Italian samples may be involved in the detoxification of the plant (Atkinson and Atkinson, 2002).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE The raw berry taste is reported to be unpleasant. As the fruits may contain low amounts of toxic compounds (cyanogenic glycosides), they should be cooked to destroy the toxic compounds, and any raw fruit consumption might cause vomiting. Only the flowers and the berries are used for human consumption. The flowers are used to make a herbal tea used for colds and fever treatment. The berries are used to prepare jams, pies, and sauces. The leaves contain cyanogenic glycosides in high amounts and cannot be used. On the other hand, the fruit and its products are important for human nutrition. The berries are source of important compounds for the human body, such as polyphenols and anthocyanins in high amounts. The high level of vitamins, minerals, pectins, and dietetic fibers, and the low energetic value makes the berries interesting for food purposes. The anthocyanins and polyphenolics are important fruit quality indicators, and strongly influence the appearance and flavor of berries and berry products (Vuli´c et al., 2008). The berries nutritional composition of berry is given in Table 1. Approximately 14 new aroma compounds were reported in elderberry products. Among them, 2 are ketones (methyl vinyl ketone and damas-cenone) and 12 are higher fatty acids of methyl and ethyl esters (myristic, palmitic,
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TABLE 1 Centesimal Composition of Elderberry Parameter
Content
Total sugars
8.88 (%)
Reducing sugar
8.55 (%)
Sucrose
0.33 (%)
Pectin
0.16 (%)
Pectic acid
0.23 (%)
Protopectin
0.04 (%)
Calcium-pectato
1.53 (%)
Cellulose
1.65 (%)
Total acidity
1.30 (% citric acid)
Ash
0.92 (%)
Dry matter
20.22 (%)
Protein
2.84 (g/100 mL)
Anthocyanins
863.89 (mg/L)
Vitamin C
34.10 (mg/100 g)
Potassium
391.33 (mg/100 g)
Phosphorus
54.00 (mg/100 g)
Calcium
28.06 (mg/100 g)
Sodium
2.17 (mg/100 g)
Magnesium
25.99 (mg/100 g)
Iron
1.86 (mg/100 g)
Zinc
0.36 (mg/100 g)
Manganese
0.27 (mg/100 g)
Copper
0.14 (mg/100 g)
ˇ Source: Vuli´c, J., Ljubo, J., Vraˇcar, O., Sumi´ c, Z.M., 2008. Chemical characteristics of cultivated elderberry fruit. Acta Periodica Technol. 39, 8590 Vuli´c et al. (2008).
palmitooleic, stearic, oleic, linoleic and linolenic). Other aroma compounds reported for elderberry products are: hexenal, hexenol, hexanol, linalool, hotrienol, phenylacetaldehyde, damascenone and linalool oxide. Unripe berries do not have hexenol and hexanol and have less phenylacetaldehyde than ripe ones. The characteristic aroma of elderberries is related to dihydroedulan and β-damascenone. The fruity odors are due to aliphatic alcohols and aldehydes and aromatic esters. The odors associated with the flowers migh be attributed to 1-nonanol, nerol oxide and (Z)- and (E)-Rose oxide (4-methyl-2-(2-methyl-1-propenyl) tetrahydro-2H-pyran). Other flower odors were associated with hotrienol, linalool, and α-terpineol. Other aroma compounds identified were: 1-hexanal (E)2- hexen-1-al (Z)-3-hexen-1-ol (E)-2-hexen-1-ol and (E)-2- octen-1-al 1-octen-3-ol and 1-octen-3-one (Atkinson and Atkinson, 2002).
INDUSTRIALIZATION Sambucus can be used for several food applications such as wine, jams, jelly, juice, concentrated juice, and other zbeverages. The most famous beverage is the Italian liquor”Black Sambuca”, which is a blend of elderberry extract, anise, and licorice.
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185
Usually, the processing is undertaken by the plant grower, who propagates the plants, grows elderberry, and producse the value-added products (wine, juice or jelly) instead of focusing only on one product or service. The flower and the berries are also used in herbal medicine. Tea made from the flowers is used to reduce inflammation or as a diuretic. Other medicinal applications such as treating sinusitis, and standardized preparations containing extracts or juice of elderberries have been shown to reduce flu symptoms. Other medicinal uses are addressing coughs, colds, and constipation. Elderberry is used as an immune booster, perhaps supported by the presence of anthocyanidins in the berries (chemical compounds that are known to have immunostimulant effects). Elderflower is also used against diabetes: research has shown that extracts of elderflower stimulate glucose metabolism and the secretion of insulin, lowering blood sugar levels. However, elderberry products can cause allergic reactions and are not recommended for pregnant and breastfeeding women due to the lack of adequate studies.
REFERENCES Atkinson, M.D., Atkinson, E., 2002. Sambucus nigra L. J. Ecol. 90 (5), 895923. Cernusca, M., Gold, M., Godsey, L., 2011. Elderberry Market Research. In: Elderberry Market Research, The Center for Agroforestry, University of Missouri. Finn, C.E., Thomas, A.L., Byers, P.L., Kemal, M., 2008. Evaluation of American (Sambucus canadensis) and European (S. nigra) elderberry genotypes grown. Diverse Environ. Implic. Cultivar Dev. Hort Sci. 43 (5), 13851391. Lee, J., Durst, R.W., Wrolstad, R.E., 2005. Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: collaborative study. J. AOAC Int. 88 (5), 12691278. Magness, J.R., Markle, G.M., Compton, C.C., 1971. Food and feed crops of the United States. New Jersey Agric. Expertise Stat. Bull. 828. Moerman, D.E., 2002. Native American Ethnobotany. Timber Press, Portland, OR. Ritter, C.M., McKee, G.W. 1964. The elderberry: history, classification and culture. Pennsylvania State University, Agricultural Expertise Statistic Bulletin 709. Sievers, A.F. 1930. The Herb Hunters Guide. Miscellaneous Publication. No. 77. USDA, Washington DC. Stang, E.J., 1990. Elderberry, highbush cranberry, and juneberry management. In: Galletta, G.J., Himelrick, D.G. (Eds.), Small Fruit Crop Management. Prentice-Hall, Englewood Cliffs, NJ, pp. 363374. Valle`s, J., Bonet, M.A., Agelet, A., 2004. Ethnobotany of Sambucus nigra L in Catalonia (Iberian Peninsula): The Integral Exploitation of a Natural Resource in Mountain Regions. Econ. Bot. 58 (3), 456469. ˇ Vuli´c, J., Ljubo, J., Vraˇcar, O., Sumi´ c, Z.M., 2008. Chemical characteristics of cultivated elderberry fruit. Acta Periodica Technol. 39, 8590.
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Figo da india—Opuntia spp. Jose´ A´. Guerrero-Beltra´n1 and Carlos E. Ochoa-Velasco2 1
Universidad de las Ame´ricas Puebla, Puebla, Mexico, 2Beneme´rita Universidad Auto´noma de Puebla, Puebla, Mexico
Chapter Outline Fruit Origin and Botanical Aspects Origin Taxonomy Fruit Characteristics Cultivation and Harvest Physiology and Biochemistry Physical Changes Respiration Characteristics Chemical Composition and Nutritional Value Composition Nutritive Characteristics Minerals Amino Acids Vitamins Phenolic Compounds and Antioxidants
187 187 187 188 190 190 190 191 191 191 191 192 192 192 193
Pigments Volatile Compounds and Sensory Characteristics Harvest and Postharvest Conservation Harvest Postharvest Conservation Potential Industrialization Juice and Nectar Jams, Jellies, and Candies Fudge, Cheese or “ate” Dehydrated Products Alcoholic Drink “colonche” Minimal Processing Pigments Final Remarks References
194 194 195 195 196 197 197 197 198 198 198 198 199 199 199
FRUIT ORIGIN AND BOTANICAL ASPECTS Origin It has been hypothesized that the Opuntia genus (Figs. 1 and 2) is native to Mexico. The Cactaceae family, to where the Opuntia genus belongs, is distributed in America from western and southern Canada to the Patagonia. Since its domestication, it has been grown, for centuries, in many countries in arid and semiarid areas (Kiesling, 1998; Griffith, 2004). The origin of Opuntia genus and its domestication is centered in Mexico (Griffith, 2004). The cactus pads tree, prickly pear tree or “nopal” is the plant that produces the prickly pear, cactus pear, Indian fig or “tuna” fruits. Some species of Opuntia are used for production of cladodes or “nopalitos” to be eaten as vegetables. Also, some species of Opuntia are wild and fruits are not eaten by humans but animals. In some parts of the world, the domesticated Opuntia is a crop that is of great economic importance. The edible fruits of Opuntia spp. are consumed in Mexico, Chile, Argentina, Peru, Uruguay, Ecuador, Colombia, Italy (Sicily and southern Italy), Spain (Canary Islands, Andalucia, and Castilla) (Barbera et al., 1992a; Inglese et al., 2002; Stintzing and Carle 2008), Morocco, Algeria, Egypt, Israel, and Saudi Arabia among other places in the whole world.
Taxonomy Linnaei (1753) classified this plant as Cactus opuntia and C. ficus-indica in the Species Plantarum plants compendium. Philip Miller in 1768 classified the plant as Opuntia ficus-indica (Griffith, 2004); however, today classifications have had to change according to different species found in of the Opuntia genus found elsewhere in Mexico, America and across the world. The classification of the genus Opuntia is: Kingdom: Plantae; Subkingdom: Tracheobionta; Superdivision: Spermatophyta; Division: Magnoliophyta; Class: Magnoliopsida; Subclass: Caryophyllidae; Order: Caryophyllales; Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00024-1 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Flower of prickly pear of cactus pads tree (Opuntia spp.) or “nopal”.
FIGURE 2 Prickly pear, cactus pear or “tuna” of cactus pads tree (Opuntia spp.) or “nopal”.
Family: Cactaceae; Subfamily: Opuntioideae; Tribe: Opuntieae; Genus: Opuntia; Species (edible): there exist various names (INE, 1994; USDA 2016): ficus-indica, albicarpa, megacantha, undulata, among others and many others not mentioned in this chapter.
Fruit Characteristics Prickly pear or cactus pear can be with or without prickles, depending on the species. Cactus pear is an oval elongated fruit weighing 75250 g and consists of a thick skin (31.652% w/w of skin) (Sawaya et al., 1983; Sepu´lveda and
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189
Sa´enz, 1990; Rodrı´geuz et al., 1996) surrounding a juicy tissue containing many hard seeds (in a beige color) (6% 13%) (Pimienta-Barrios, 1987; Barbera et al., 1992b; Cantwell, 1995; Piga, 2004). Mature fruits have a very sweet pulp (Mondrago´n-Jacobo and Gallegos-Va´zquez, 2010; Piga, 2004) and interesting colors. The bulk composition is pulp (43%57%), seeds (2%10%), and peel (33%55%); in Table 1 are listed several cultivars of Opuntia spp. fruits, including size (6.810.8 cm in length and 4.571 cm in width), weight (74.4246.5 g) and pulp content (44.563.7 g). Percentages of components in Table 1 depend on cultivar, climate, and season of harvest (Mondrago´nJacobo and Gallegos-Va´zquez, 2010). All these species listed in Table 1, and subsequently mentioned, are fruits with a
TABLE 1 Physicochemical Characteristics of Several Cultivars of Opuntia spp. Fruits Species (Cultivar)
Color
Size (cm)
Weight (g)
Pulp (%)
TSS (%)
Pe
Pu
L
W
Opuntia albicarpa (Queen or “Alfajayucan”)
PG
PG
7.10 6 0.10
4.90 6 0.07
102.4 6 2.1
63.7
16.40 6 0.20
(Crystalina/“Cristalina”)
PG
PG
9.61 6 9.03
6.63 6 0.72
207.5 6 2.35
60.2
12.72 6 0.26
Opuntia albicarpa (“Burrona”)
PG
PG
9.24 6 0.90
6.69 6 0.48
217.4 6 2.09
59.8
12.07 6 0.18
Opuntia albicarpa (Emerald/ “Esmeralda”)
PG
PG
8.10 6 0.16
5.80 6 0.12
148.6 6 3.34
59.1
15.20 6 0.19
Opuntia sp. (White San Jose´)
PG
PG
9.46 6 1.17
5.55 6 0.52
144.2 6 3.21
61.8
13.15 6 0.11
Opuntia albicarpa (“La Gavia”)
PG
PG
6.75 6 0.12
4.60 6 0.09
95.5 6 2.92
62.8
14.44 6 0.21
Opuntia albicarpa (Flushed/ “Chapeada”)
G
PG
7.27 6 1.45
5.03 6 0.64
108.6 6 2.12
50.1
14.06 6 0.24
Opuntia albicarpa (“Villanueva”)
G
PG
8.26 6 0.10
5.26 6 0.06
129.3 6 2.27
60.9
13.49 6 0.17
Opuntia albicarpa (“Fafayuca”)
Y
PG
7.81 6 1.00
5.80 6 0.86
146.0 6 2.21
46.1
14.57 6 0.07
Opuntia sp. (Banana yellow)
Y
Y
9.34 6 2.08
5.58 6 0.76
152.5 6 3.92
59.6
12.07 6 0.19
Opuntia ficus-indica (Dimond yellow)
Y
Y
10.5 6 2.32
6.12 6 0.69
184.6 6 5.01
59.1
11.90 6 0.16
Opuntia megacantha (“Pico Chulo”)
O
O
8.32 6 1.14
5.97 6 0.52
170.2 6 2.23
51.7
13.15 6 0.24
Opuntia megacantha (“Montesa” yellow)
O
O
9.20 6 1.67
5.91 6 1.06
174.2 6 3.87
57.1
12.57 6 0.40
Opuntia sp. (“Miquihuana” yellow)
O
O
10.81 6 0.30
5.54 6 0.12
172.5 6 3.92
59.9
14.53 6 0.29
Opuntia megacantha (Orange genuine)
O
O
9.84 6 1.42
7.06 6 0.60
256.5 6 3.38
59.1
13.66 6 0.24
Opuntia megacantha (“Torreoja”)
RP
R
8.76 6 1.41
5.75 6 0.49
145.4 6 3.17
53.7
12.56 6 0.29
Opuntia ficus-indica (Red San Martı´n)
P
P
7.89 6 0.09
5.24 6 0.06
116.2 6 2.16
44.5
13.70 6 0.41
Opuntia sp. (Red “Liria”)
RP
M
6.96 6 0.09
4.52 6 0.08
74.4 6 1.16
53.3
13.40 6 0.20
Opuntia undulate (“Bolan˜era”)
P
P
9.36 6 2.38
4.92 6 0.85
99.7 6 3.01
59.7
9.67 6 0.32
Opuntia ficus-indica (Red smooth)
RP
R
8.50 6 0.12
5.68 6 0.13
160.1 6 3.92
63.7
15.46 6 0.11
Opuntia ficus-indica (“Vigor” red)
RP
R
10.1 6 2.65
6.01 6 0.67
171.2 6 6.01
59.5
11.88 6 0.42
Opuntia joconstle* (Xoconostle)
GY
M
53.4
69.4
5.32
Pe: peel; Pu: pulp; L: large; W: width; PG: pale-green; G: green; Y: yellow; O: orange; RP: redpurple; R: red; P: purple; M: magenta; GY: green-yellow. Sources: Mondrago´n-Jacobo, C., Gallegos-Va´zquez, C., 2010. Cultivares mexicanos del nopal tunero de importancia econo´mica en Me´xico. In Manejo Poscosecha de la Nochtli o Tuna (Opuntia spp.). Universidad Auto´noma Metropolitan-Iztapalapa. Mexico, D.F.; * Mayorga, M.C., Urbiloa, M.C., Sua´rez, R., Escamilla, S.H.M., 1990. Estudio agrono´mico de xoconostle Opuntia spp. en la zona semia´rida del Estado de Quere´taro. In: Lo´pez, J.J., Ayala, M.J.S., (Eds.), Proceedings of the “3a Reunio´n Nacional y 1a Reunio´n Internacional sobre Conocimiento y Aprovechamiento del nopal”. Universidad Auto´noma Agraria “Antonio Narro”. Saltillo, Coahuila, Mexico, pp. 239245.
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slightly thick peel and sweet pulp of different colors with seeds that vary in size depending on the variety of prickly pear. The pulp and seeds content ranges from 48.0% to 68.4% (Sawaya et al., 1983; Sepu´lveda and Sa´enz, 1990; Rodrı´geuz et al., 1996) which also depend on the variety and season of harvesting. Even though in Table 1 are listed the main cultivar from Mexico, there are many other cultivar around the world. Examples of other species of Opuntia spp. are listed in later in the chapter. The total soluble solids range from 9.7% to 16.4% (Askar and El-Samahy, 1981; Sawaya et al., 1983; Sepu´lveda and Sa´enz, 1990; Mun˜oz-de-Cha´vez et al., 1995; Rodrı´geuz et al., 1996; Mondrago´n-Jacobo and Gallegos-Va´zquez, 2010), containing mainly sugars (8.1%14.1%) (Sawaya et al., 1983; Pimiento, 1990; Mun˜oz-de-Cha´vez et al., 1995; Sepu´lveda and Sa´enz, 1990; Rodrı´geuz et al., 1996) which are in general glucose and fructose. The pH of the pulp ranges from 5.3 to 6.4, acidity (as citric acid) ranges 0.01%0.18% (Askar and El-Samahy, 1981; Sawaya et al., 1983; Mun˜oz-de-Cha´vez et al., 1995; Sepu´lveda and Sa´enz, 1990; Rodrı´geuz et al., 1996), and pectin ranges from 0.17% to 0.21% (Sawaya et al., 1983; Sepu´lveda and Sa´enz, 1990; Rodrı´geuz et al., 1996).
CULTIVATION AND HARVEST There exist more than 300 species of Opuntia; however, only a few of them are used for human consumption (around 12 species). Cactus pads tree or “nopales”, prickly pear producers are native and cultivated in arid or semi-arid areas (Nobel et al., 1987; Duru and Tucker 2005). Across the world, the cactus pads tree is grown in the northern areas around the Tropic of Cancer (Mexico, Egypt, Turkey, Italy, Spain, northern Africa, among others) and by the Tropic of Capricorn in Chile in South America, south Africa and Australia (Erre et al., 2009). The parts of the two hemispheres have different climate conditions where the temperature in spring and summer is hot and rainfall is low. The prickly pear production is for a short period only, especially between the months of May and September (in Mexico); therefore, different varieties of prickly pear are produced at different times but especially in the hot seasons.
PHYSIOLOGY AND BIOCHEMISTRY Physical Changes During growing and maturation of the prickly pear, some biochemical changes occur. Montiel-Rodrı´guez (1986) reported (Table 2) some physical and compositional changes during growing and ripening of O. amyclaea (“Copena 18” white tuna). The definitions of different stages are: G G G
G G
Unripe: green shell and undeveloped (incompletely grown). Ripe green: light green shell and nearly completely developed. Transitional or in-between stage: color changes in shell; color varies from initial to about 75% on the whole surface. Mature: 75%100% color developed on surface. Declining: color may be pale yellow and some brown spots start to appear.
TABLE 2 Physical and Compositional Changes in Opuntia amyclaea White Tuna Physical phase
W. (g)
Diam. (mm)
FD (mm)
Pulp (%)
Firm. (kg/cm2)
TSS (%)
TA (%) pH
Vit. C (mg/100 g)
Unripe
86
4244
7.2
44
4.6
7.5
0.08
5.2
12
Ripe green
102
4749
3.5
57
3.7
8.8
0.04
6.1
18
In-between
105
4953
1.9
63
2.7
10.1
0.03
6.2
18
Mature
112
5054
1.4
65
2.4
11.5
0.02
6.3
26
Declining
108
4953
1.0
75
2.2
12.5
0.02
6.4
28
W: weight; Diam.: diameter; Firm.: firmness; TSS; total soluble solids; TA: titratable acidity; FD: floral depth. Source: Montiel-Rodrı´guez, S.M., 1986. Produccio´n y calidad de frutas maduras de 9 selecciones de tuna blanca (Opuntia amyclaea) en la costa de Hermosillo. Professional thesis. Universidad de Sonora. Hermosillo, Sonora, Mexico.
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191
TABLE 3 Carbon Dioxide and Ethylene Production During Respiration Rate of Opuntia amyclaea “White Tuna” Physical phase
Carbon dioxide (mL/kg per h)
Ethylene (μL/kg per h)
2d
8d
16 d
2d
8d
16 d
Ripe green
21.1 6 2.9
19.4 6 1.4
18.4 6 1.5
0.20 6 0.06
0.20 6 0.05
0.25 6 0.08
In-between
20.9 6 1.6
20.0 6 2.9
18.6 6 2.9
0.16 6 0.06
0.21 6 0.07
0.26 6 0.10
Mature
19.8 6 3.0
19.0 6 3.6
18.6 6 3.1
0.17 6 0.06
0.20 6 0.08
0.30 6 0.10
An increase of weight, diameter, pulp content, total soluble solids (sugars), pH (decreasing acidity), and vitamin C is observed during ripening. However, during ripening other characteristics may appear that indicate the senescence of the fruit such as brown spots and softening. A declination of firmness and floral depth is also observed during ripening. It is important to note that peel of any color (pale green to purple) starts to show tiny brown spots when senescence is initiated. Afterward, the brown spots grow in size and they may cover the whole surface of the fruit (Ochoa-Velasco and Guerrero-Beltra´n, 2012, 2013). However, in many cases, if the fruit is not rotten or completely brown, the fruit pulp is still acceptable in appearance (natural color), flavor (light), and texture (firmness). The brown spots formed are related to polyphenol oxidase that increases as the storage temperature increases (Ochoa-Velasco and Guerrero-Beltra´n, 2012, 2013).
Respiration Characteristics Opuntia species grow in arid and semi-arid areas that has minimal rainfall during the year. Opuntia spp. are considered to have a Crassulacean acid metabolism (CAM); CO2 is acquired in the night and then fixed and stored as organic acids; also, the use of water is more efficient in arid environments (Nobel, 1988; Lu¨ttge, 2001). Fruits have to be harvested in the mature state. As fruits are non-climacteric (low respiration rate after harvested and do not continue ripening), their respiration rate is slow during storage (Table 3). The fruits respiration rate is about 2736 mg CO2/kg per h at 20 C producing heat of about 1900 kcal/ton day (Cantwell, 1995). The carbon dioxide and ethylene production remains almost constant for the three physical states and time of storage; this behavior is because of the non-climacteric conditions of the fruit. During maturation of fruits, the fruit pulp store sugars (glucose and fructose mainly) (Barbera, 1992b); the acid content in general is minimal at any physiological stage of the fruit (Barbera, 1992b).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Composition As there are a number of species, the proximal composition is given in a range that comes from many prickly pears. The raw edible part prickly pear is composed of: moisture (84.2%91%), total sugars (8.1%17%), proteins (0.21%1.6%), fat (0.10%0.83%), raw fiber (0.33%3.1%), and ash (0.02%3.16%); the physicochemical composition is: pH (5.37.1), acidity (0.01%0.18% as citric acid), total soluble solids (9.6%16.4%), and total solids (10.0%16.2%) (Askar and El-Samahy, 1981; Sawaya et al., 1983; Pimienta-Barrios, 1990; Sepu´lveda and Sa´enz, 1990; Mun˜oz-de-Cha´vez et al., 1995; Rodrı´geuz et al., 1996; Aquino et al., 2012). Table 4 lists the proximal characteristics and minerals content of fruits of three colors (white, orange, and red). The main difference of fruits is color (given by different betalains). As for any other type of fruit or vegetable, prickly pear is source of vitamin C (20.024.1 mg/100 g), minerals, water, and sugars (as energy).
Nutritive Characteristics Today, the nutritive characteristics of fruits such a prickly pear are due not only to sugars, minerals and vitamins, but also to other components called nutraceuticals such as the antioxidants on many different chemical structures: phenolic compounds, vitamins, pigments (anthocyanins, betalains, carotenoids, among other pigments) and some amino acids.
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TABLE 4 Chemical and Nutritional Composition of Tunas of Different Colors Characteristic
Green
Orange
Purple
83.8
85.1
85.98
Protein (%)
0.8
0.8
0.38
Fat (%)
0.1
0.02
Fiber (%)
0.2
0.05
Moisture content (%)
Ash (%)
0.4
0.3
0.32
Total sugars (%)
14.1
14.1
13.25
Vitamin C (mg/100 g)
20.3
24.1
20.00
β-carotene (mg/100 g)
0.5
2.3
Betanin (mg/100 g)
100.0
Ca (mg/100 g)
12.8
35.8
13.2
Mg (mg/100 g)
16.1
11.8
11.5
Fe (mg/100 g) Na (mg/100 g)
0.40 0.60
0.20 0.90
0.10 0.50
K (mg/100 g)
217.0
117.7
19.60
P (mg/100 g)
32.8
8.5
4.90
Sources: Sepu´lveda, E., Sa´enz, E., 2001. Ecotipos coloreados de tuna (Opuntia ficus-indica). Aconex (Chile) 72:2932; Sepu´lveda, E., Sa´enz, C., 1990. Chemical and physical characteristics of prickly pear (Opuntia ficus-indica). Rev. Agroquim. Technol. 30, 551555; Sa´enz, C., Sepu´lveda, E., Moreno, M., 1995. Caracterizacio´n tecnolo´gica de pulpa de tuna roja. In: Proceedings of the XI Congreso Nacional de Ciencia y Tecnologı´a de Alimentos. Vin˜a del Mar, Chile. p. 159.
The nutraceutical characteristics of prickly pear depend on their color and variety (Pimienta-Barrios, 1990; Stintzing et al., 1999; Piga, 2003; El-Samahy et al., 2006).
Minerals Minerals such as calcium (12.835.8 mg/100 g), magnesium (11.116.1 mg/100 g), potassium (19.6217 mg/100 g), and phosphorus (4.932.8 mg/100 g) are listed in Table 4 (Sepu´lveda and Sa´enz, 1990, 2001; Sa´enz et al., 1995). Various researchers have reported other levels of minerals in mg/100 g of pulp of Opuntis spp: Ca (12.849.0), Mg (16.198.4), Fe (0.402.6), Na (0.85.0), K (78.8220.0), and P (15.432.8) (Sawaya et al., 1983; Askar and El-Samahy, 1981; Sawaya et al., 1983; Sepu´lveda and Sa´enz, 1990; Mun˜oz-de-Cha´vez et al., 1995; Rodrı´guez et al., 1996).
Amino Acids The fruits are not a source of amino acids because they are not a source of proteins; however, some free amino acids can be found in pulp. Stintzing et al. (1999) and Piga (2004) reported the content (mg/100 mL) of proline (176.9), glutamine (57.5), serine (21.8), alanine (9.7), glutamic acid (8.3), methionine (7.7), and lysine (5.3). Taurine was also found (57.2 mg/mL), which is an organic acid, considered as antioxidant (Tesoriere et al., 2005).
Vitamins Ascorbic acid as a nutraceutical and essential vitamin is found in prickly pear. As an essential chemical for the human diet, vitamin C is found in differing amounts in different cultivars of Opuntia spp. of various colors (Tables 7 and 8). Additional to vitamin C (an antioxidant) found in prickly pears, USDA (2016) reports, in amount/100 g, vitamin A (25 μg), riboflavin, B2 (0.1 mg), niacin (0.5 mg), vitamin B6 (0.1 mg), folate, and B9 (6 μg).
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Phenolic Compounds and Antioxidants Phenolic compounds and antioxidant activity along with pigments and vitamin C have been found in prickly pear. In some cases phenolic compounds and antioxidant activity or any other group of compounds may be correlated. OchoaVelasco and Guerrero-Beltra´n (2012, 2013, 2014) reported an antioxidant activity and phenol content in two species of prickly pear (Table 5). However, Ordoux and Dominguez (1996) (Table 6), Butera et al. (2002) (Table 7), Stintzing et al. (2005) (Table 8), and Aquino et al. (2012) (Table 9), among other researchers, have reported antioxidant activity, phenolic compounds, vitamin C, and pigments in prickly pears.
TABLE 5 Antioxidant Activity and Phenolic Compounds in Prickly Pear Species
Color of fruit
Antioxidant activity (mg trolox/100 mL)
Phenolic compounds (mg gallic acid/100 mL)
Opuntia ficus-indica (San Martı´n)
Red
12.27 6 0.9288.80 6 6.00
42.01 6 6.0848.8 6 2.30
Opuntia albicarpa (Villanueva)
White
39.80 6 0.50112.50 6 3.10
21.10 6 1.1057.2 6 2.20
TABLE 6 Betalains in Several Species of Different Colors Species
Fruit color
Peel (mg/100 g)
Pulp (mg/100 g)
Opuntia ficus-indica
Magenta
1.1
4.1
Opuntia decumbers
Red
22.1
37.3
Opuntia acidulata
Red
1.8
0.3
Opuntia microdasys
Red
0.9
0.0
Opuntia curvispina
Red
112.4
99.0
Opuntia sp.
Purple
72.0
49.3
Opuntia robusta
Purple
19.0
58.2
Opuntia robusta-robusta
Purple
40.5
86.1
Opuntia sp.
Purple
118.3
126.8
Opuntia sp.
Purple
44.8
27.6
Opuntia sherri
Purple
8.4
6.0
Source: Odoux, E., Domı´nguez-Lo´pez, A., 1996. Le Figuier de Barbarie: une source industrielle de Betalaines? Fruits 51, 6178 Odoux y Domı´nguez (1996).
TABLE 7 Betalains and Vitamin C in Prickly Pear (Sicilian) of Different Colors Cultivar
Indicaxanthin (mg/100 g)
Betanin (mg/100 g)
Ascorbic acid (mg/100 g)
White
5.86 6 0.49
0.10 6 0.02
28.0 6 2.5
Yellow
8.42 6 0.51
1.04 6 0.12
30.0 6 2.8
Red
2.61 6 0.30
5.12 6 0.51
29.0 6 1.7
Source: Butera, D., Tesoriere, L., Di Gaudio, F., Bongiorno, A., Allegra, M., Pintaudi, A.M., et al., 2002. Antioxidant activities of Sicilian prickly pear (Opuntia ficus-indica) fruit extracts and reducing properties of its betalains: betanin and indicaxanthin. J. Agric. Food Chem. 50, 68956901.
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TABLE 8 Nutraceutical Characteristics of Some Cultivars of Prickly Pear According to Color Cultivar
PC (mg GAE/100 mL)
Betaxanthin (IE/100 mL)
Betacyanins (BE/100 mL)
Ascorbic acid (mg/100 mL)
Green
24.2 6 1.34
0.04 6 0.002
0.01 6 0.001
5.11 6 0.30
Orange
24.7 6 2.31
7.63 6 0.038
0.66 6 0.004
7.02 6 1.60
Red
33.5 6 1.93
6.79 6 0.019
12.00 6 0.044
6.79 6 1.65
Purple
66.0 6 3.58
19.58 6 0.046
43.10 6 0.104
9.54 6 0.06
GAE: Gallic acid equivalents; IE: indicaxanthin equivalents; BE: betanin equivalents. Source: Stintzing, F.C., Herbach, K.M., Mosshammer, M.R., Carle, R., Yi, W., Sellappan, S., et al., 2005. Color, betalain pattern, and antioxidant properties of cactus pear (Opuntia spp.) clones. J. Agric. Food Chem. 53, 442451.
TABLE 9 Betalain in RedPurple Prickly Pears From El Orinoco, Zacatecas, Mexico Species (Cultivar)
Betalains (mg/100 g)
Opuntia megacantha (“Rubi Reyna”)
13.55 6 0.47
Opuntia megacantha (“Camuezo”)
24.24 6 0.79
Opuntia robusta (“Tapo´n aguanoso”)
58.12 6 0.81
Opuntia sp. (“Moradilla 1”)
19.97 6 0.94
Opuntia sp. (“Moradilla 2”)
14.46 6 0.18
Opuntia sp. (“Apastillada”)
27.02 6 0.44
Source: Aquino, E.N., Chavarrı´a, Y., Cha´vez, J.L., Guzma´n, R.I., Silve, E.R., Verdalet, I., 2012. Physicochemical characterization of seven red-purple prickly pear fruit varieties (Opuntia spp.) and pigment stability of two varieties with the highest concentration. Investigacio´n y Ciencia de la Universidad Auto´noma de Aguascalientes (Mexico) 55, 310.
Pigments As mentioned above, the colors of prickly pear pulp are pale green, yellow, orange, magenta, red and redpurple, indicating that their pigments (also considered antioxidants) are different. Cacti fruits synthesize betalains, which are pigments that give pale yellow, red, and redpurple colors (Stintzing et al., 2005). However, pale-green pigments (chlorophylls) are found in the “pale green” prickly pears (Piga, 2004). Prickly pears, similar to other cactus fruits, have pigments of different color due to the betalains group. In the group of betalains (N-heterocyclic hydrosoluble pigments) are the betaxanthins (yelloworange) and betacyanins (redpurple). Betaxanthins found in plants are indicaxanthin, miraxanthin, portulaxanthin, and vulgaxanthin. Betacyanins in plants include betanin, isobetanin, neobetanin, and probetanin (Stintzing et al., 2005; Stintzing and Carle, 2008). Ordoux and Dominguez (1996) reported red betalains in peel and pulps for different Opuntia species with different colors (Table 6). Butera et al., (2002) reported the amount of indicaxanthin (yelloworange) and betanin (redpurple) and ascorbic acid from Sicilian O. ficus-indica cultivars of different colors (Table 7). Stintzing et al. (2005) reported quantities and relationship among phenolic compounds (PC), betaxanthin, betacyanins, and ascorbic acid for Opuntia cultivars of different colors (Table 8). Aquino et al., (2012) studied the red color of some purple prickly pears from the northern part of Mexico (Zacatecas, state) (Table 9). As observed, the nutraceutical compounds reported may differ according to the color of prickly pear which is mainly due to species and season of harvesting.
Volatile Compounds and Sensory Characteristics Volatile Compounds The aroma flavor of prickly pear is characteristic for each color of the pulp. The aroma and flavor of prickly pears is very light and sweet. According to Arenas et al. (2001) the main components or aroma of prickly pears are
Figo da india—Opuntia spp.
195
TABLE 10 Volatile Compounds (μg/100 g) in Prickly Pears of Different Colors Compound White 2-Metylbutanoic acid methyl-ester
Fruit color Red
Yellow
11.0
8.6
10.3
0.3
2.5
0.3
(E)-2-Hexanal
44.9
22.0
26.3
2-Hydroxybutanona
20.3
30.1
14.4
Hexanal
(Z)-2-Penten-1-ol
4.1
8.7
4.3
319.2
277.9
188.0
(Z)-3-Hexen-1-ol
17.6
21.2
16.2
(E)-2-Hexen-1-ol
607.7
639.7
439.3
Linalool
2.9
2.4
3.1
(Z)-3-Nonen-1-ol
2.3
3.5
5.2
(E)-2-Nonen-1-ol
16.8
29.4
32.3
(Z,Z)-3,6-Nonadien-1-ol
2.1
4.6
8.0
(E,Z)-2,6-Nonadien-1-0l
Hexan-1-ol
18.8
39.3
38.7
Salicylic acid methyl ester
5.4
1.9
3.1
Hexanoic acid
8.0
3.7
4.6
7.4
8.6
Octanoic acid
(E,Z)-2-6-nona-1-ol and 2-methyl-acid methyl ester. They report volatile compounds for white, orange, and red cultivars (Table 10). However, the other volatile compounds also contribute to the whole flavor of the fruits.
Sensory Characteristics Ochoa-Velasco and Guerrero-Beltra´n (2014) performed a sensory evaluation in white (Opuntia albicarpa) and red (Opuntia ficus-indica) prickly pears using a hedonic test (color aroma, texture, flavor, overall acceptability) of 9 points (1 5 dislike extremely; 5 5 neither like nor dislike; 9 5 like extremely); they found in general scores between 6 (like slightly) and 7 (like very moderately).
HARVEST AND POSTHARVEST CONSERVATION Harvest Prickly pears are harvested when they are completely ripe. Prickly pears develop characteristic colors and flavor for each variety. Some Opuntia species produce prickly pears with very thin spines that can be easily detached from the peel, they can fly in the air and harm harvesters; other fruits are smooth without spines. Nevertheless, special tools are required for detaching prickly pears from the cactus pads. It is also important not to damage the peduncle of prickly pears during cutting. Peduncle damage can be a cause of microbial growing; therefore, prickly pears could rot faster. Similar to other fruits, the harvest process is very important in the quality of prickly pear during the storage and commercialization. In Me´xico there exists two methods for harvesting prickly pears. One technique is called “torzon”: the harvester, using special gloves, takes the prickly pear and quickly turns the fruit until it separates from the stem. This harvest technique can significantly damage the skin of the prickly pear if not performed adequately; howeverit is a quick way to harvest the fruit (Corrales-Garcı´a, 2000). The other technique is cutting off the fruit using a knife; this process is slow but does not damage the fruit (Corrales-Garcı´a, 2000). Prickly pears are collected in plastic boxes and transported to the packing house, at this site fruits are dry-cleaned using mechanical plastic bristles. The objective of
196
Exotic Fruits Reference Guide
the cleaning is to remove the physical garbage and detach prickles (thorns). Prickly pears are classified into five categories (according to their size), the larger fruit is exported. Fruits are packed into wood boxes for the domestic market and in cardboard boxes for export (Yahia, 2012). The main conservation process of prickly pear during postharvest is the refrigeration; however, recent research reported that the use of other technologies in combination with cooling significantly increases the shelf life of prickly pear (Corbo et al., 2004). Prickly pear is a highly perishable fruit due to the high water content, low acidity, and high soluble solids (Piga et al., 2000). Therefore, a good harvest and postharvest conservation are necessary to offer consumers a fruit with adequate quality and presentation (Sharma et al., 2009). Prickly pear is a seasonal fruit typically produced in the months of MaySeptember (depending on the variety), they may have a very short shelf life (79 days) if the storage conditions are inadequate (Ochoa-Velasco and Guerrero-Beltra´n (2013)). In general, the factors that strongly affect the quality of the prickly pear during the storage are physical (mechanical damage during the harvest and dehydration during the postharvest storage). However, biological damage related to microbial growing such as the appearance of Fusarium spp., Alternaria spp., Chlamydomyces spp., and Penicillium spp. just to mention a few, may occur (Cantwell, 1995). Prickly pears can suffer chilling injury when stored at temperatures below 5 C (Cantwell, 1995). Chilling injury causes prickly pear pulp to form hard and dry parts attach to the inner part of the shell. Fruits produced in Summer are more sensitive to chilling injury than those produced in Autumn (Schirra et al., 1999).
Postharvest Conservation Refrigeration Refrigeration is the most common method for the conservation of fresh fruits and vegetables. This method does not affect the quality of products and enhanced the storage life of fruits and vegetables by reducing the respiration process, microbial growth, and enzyme action (Arte´s et al., 2002). However, the storage temperature must be not create a chilling injury that can affect the fruit quality (Ding et al., 2002). As already mentioned, prickly pear is a non-climacteric fruit with low respiration rate (1699 mg CO2/kg h at 5 C) that depends on the storage temperature (Yahia, 2012). Therefore, the main factor that significantly affects the quality of the fruit during storage under refrigeration is the variety of the fruits and storage conditions such as temperature and relative humidity (Ochoa-Velasco and GuerreroBeltra´n, 2013). Corrales-Garcı´a and Herna´ndez-Silva (2005) pointed out that the varieties of prickly pear stored during 20 days at 10 C and 90% RH significantly affect the quality of the product. They reported that the firmness of the fruit was higher in Rubi Reina variety compared with “Cristalina” and “Naranjona” varieties. Corrales-Garcı´a et al. (1997) also reported similar results. They noted that varieties “Burrona” and “Cristalina” presented a low loss of pulp, firmness, weight loss, respiration rates, and chilling injury after 3 months of storage at 9 C. Ochoa-Velasco and GuerreroBeltra´n (2012) studied the effect of the storage temperature on the quality of red prickly pear (Opuntia ficus-indica L. Miller). They pointed out that at room temperature the growth of microorganisms was higher compared to refrigeration condition (4 C and 9 C), and weight loss was significant lowered at refrigeration condition (4 C) compared to 9 C and room temperature after 28 days of storage. It is important to note that the weight loss was in the skin of the fruit; therefore, the prickly pear pulp was still in good condition for consumption, although the skin presented dehydration (Ochoa-Velasco and Guerrero-Beltra´n, 2013). Depending on the species, fruits are stored at 25 weeks at temperatures between 5 C and 8 C at a relative humidity between 90 and 95% (Cantwell, 1995). During storage, fruits may lose water, become rotten, and form brown spots on the entire surface, an effect that is more visible in green prickly pears (Ochoa-Velasco and Guerrero-Beltra´n, 2013, 2014).
Modified Atmosphere Packaging The use of a modified atmosphere for packaging fruits needs to be combined with refrigeration. In order to delay the dehydration, Gonza´lez et al. (2001) used wax (paraffin) for coating prickly pears, and refrigeration as conservation method. They reported that the weight loss was significantly reduced in prickly pear; however, microorganisms were higher in the prickly pear with wax compared to the prickly pear without coating. Piga et al. (1996) reported that the use of wrapping (polyethylene) could enhance the storage life (6 weeks at 6 C) of prickly pear “Gialla” variety; they observed a reduction of chilling injury and weight losses; therefore, the appearance was improved. Pinedo-Espinoza et al. (2010) used plastic or paper film to enhance the storage life of prickly pears (“Burrona” and “Cristalina” varieties). The use of paper delayed the weight losses and firmness in prickly pear stored at 5 C for 30 days. Ochoa-Velasco
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197
and Guerrero-Beltra´n (2016) evaluated the packaging of prickly pear (O. albicarpa) under passive and active atmospheres at 4 C, 10 C, and 27 C. The storage of prickly pears in passive or active atmosphere delayed weight losses, dehydration, and changes in external color that were decisive to the acceptance of the products.
POTENTIAL INDUSTRIALIZATION Sa´enz (2000) and Corrales and Flores (2003) have pointed out that the some products have involved the use of prickly pears: juices and nectars, preserves and jellies, dehydrated fruit slices, sweeteners, alcohol and wines, vinegar, canned fruit, and frozen pulp. Other prickly pear products found around the world are syrup, fudge (“queso de tuna”, prickly pear cheese, or “ate”), and sugar crystallized peeled fruits. As prickly pear is produced in arid and semi-arid climates, it has the potential for being industrialized in several ways. In Table 11 are listed some products that can be obtained using prickly pear. However, additional to the sale of fresh prickly pears, around the world there are many other products not mentioned in this chapter: they are local products. In the follow paragraphs we will describe the main studies of the potential industrialization of prickly pear.
Juice and Nectar Similar to other fruits, obtaining the juice is the first step for manufacturing other processed items. Due to the high pH of the prickly pear juice (5.36.4), some organic acids or acidic juices must be added to reduce the pH. Thermal treatment does not affect the sensory and nutritional characteristics of the juice (Saenz and Sepulveda, 2001). In case of prickly pear, prolonged thermal treatments may cause undesirable pigments in prickly pear juices that might cause an unattractive color and taste similar to “hay”. Also, certainly no pleasurable changes of aroma in the prickly pear juice should occur. Paredes and Rojo (1973) obtained a pleasant and stable prickly pear juice (pH 5 4.3) by adding citric acid and sodium benzoate (500 ppm), and applying a thermal treatment at 90 C for 5 min. Moreover, El-Samahy et al. (2007) evaluated different combinations of treatments in order to obtain a stable prickly pear juice. They adjusted the total soluble solids (15 Brix) and pH (5) of prickly pear juice with sugar and citric acid solutions, respectively. Then, the juice was separated into three parts. One part was pasteurized (95 C during 25 min), another part was pasteurized and 100 ppm sodium benzoate was added, and the last part was sterilized (121 C during 10 min). Results showed that the pasteurized juice presented better sensory characteristics compared to sterilized juice. However, all juices were microbiologically stable during storage for 6 months. On the other hand, El-Samahy et al. (2008) evaluated the effect of thermal treatment on chemical and sensory characteristics of canned prickly pear nectar (juice plus syrup). They pointed out that unprocessed nectars presented similar chemical composition compared to sterilized prickly pear nectars; however, sensory attributes of processed prickly pear nectars were significantly affected by the thermal treatment.
Jams, Jellies, and Candies Prickly pears have been used for jams, jellies, and candies. One of the first studies about the elaboration of prickly pear jam was conducted by Sawaya et al. (1983). They made different combinations of prickly pear pulp with sugar
TABLE 11 Prickly Pear Products Product
References
Juice and nectar
Paredes and Rojo (1973); Saenz and Sepulveda (2001); El-Samahy et al. (2007).
Preserves
Sawaya et al. (1983).
Fudge (Queso de tuna or “ate”)
Lo´pez et al. (1997); Alvarado (2010).
Dehydrated
Sepu´lveda et al. (2000).
Alcoholic drinks “Colonche”
Arrizon et al. (2006).
Minimally processed
Cerezal and Duarte (2004); Moβhammer et al. (2006).
Pigments
Stintzing et al., (2000), Stintzing et al. (2003).
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Exotic Fruits Reference Guide
(60:40%), pectin, and different organic acids. They reported that citric and tartaric acids (1:1) were the best combination for the consumers’ acceptance of jellies and candies; however, prickly pear jams needed to be combined with flavors such as cloves, grapefruit extract, orange extract, or almond flavor to improve their acceptance by consumers. Vignoni et al. (1997) evaluated the use of lemon juice and lemon peel to formulate prickly pear jams; they reported that jams did not have any significant difference among them.
Fudge, Cheese or “ate” Prickly pear cheese is a traditional type of fudge (“ate”) make with prickly pears that are not used for sale in fresh form. The prickly pear juice is collected in copper pots for foods and heated until the juice is concentrated and a prickly pear paste is obtained. The paste is cooled, kneaded, and placed in molds for 24 h; after that, the prickly pear cheese is ready for consumption. Occasionally, prickly pear cheese is packed in vacuum conditions for retail (Lo´pez et al., 1997; Alvarado, 2010).
Dehydrated Products Dehydration may be a good alternative for prickly pear preservation. Dried products help to offer new options for industrial applications of fruit products (energetic fruit bars, desserts, breakfast cereals, just to mention a few examples). One of the first studies of drying of prickly pear was conducted by Ewaidah and Hassan (1992). They obtained prickly pear sheets from pulp added with sucrose, citric acid, sodium metabisulphite, and olive oil. Dried prickly pear sheets were well accepted; a score of 89 was given by judges using a 9 points hedonic scale. Sepulveda et al. (1996) combined prickly pear with quince pulps (75:25%), thin layers were prepared, and dried. The product showed good texture and flavor. This product may be a good alternative for children as a food bars. Recent studies have been conducted to obtain spray-dried prickly pear powder (Rodrı´guez-Herna´ndez et al., 2005). They reported that spray drying slightly affects the color of powder, reporting a total change in color (ΔE) in the range 69. Vitamin C was maintained in a 45%50%. Moßhammer et al. (2006) evaluated the spray-drying and freeze-drying of yelloworange prickly pear and singlestrength juice, respectively. They noted that both technologies maintained the betalains content. Vitamin C was retained more with the freeze-dried process (10% losses) compared with spray-drying (50%55% losses). However, the spraydried juice had the lowest total change in color changes (ΔE 5 2.3).
Alcoholic Drink “colonche” An alternative for processing prickly pear juice is the preparation of low alcoholic drinks. In Mexico, for many years, an alcoholic beverage called “colonche” has been prepared (Sa´enz et al., 1995). Flores (1992) obtained wine and alcohol from O. streptacantha and O. robusta prickly pear juices. They pointed out that beverages have a characteristic fruit-like flavor and a pleasant taste; an initial wine aroma prevailing. Lee et al. (2000) evaluated different mixtures of prickly pear and grape juices; they found that an increase of prickly pear juice in the mixture reduces the ethanol yield in the fermentation process. Arrizon et al. (2006) researched the effect of different factors (thermal treatment, yeast strain, and variety and ripeness of prickly pears) on the volatile profile of prickly pear distilled beverage. Thermal treatment and prickly pear variety were the factors that strongly affected the volatile profile of distilled beverages.
Minimal Processing Minimal processing is an alternative to obtaining products with characteristics similar to fresh fruits and vegetables. Prickly pears have been treated in different methods in order to obtain minimally processed products. Peeled prickly pear was combined with sucrose syrup (to obtained two water activities of 0.96 and 0.975), phosphoric or citric acid solutions (to obtained pHs of 4.0 and 4.2), potassium sorbate or ascorbic acid, and sodium bisulphite. After 14 days of storage, the sensory attributes of minimally processed prickly pears were evaluated by trained judges. Judges reported that prickly pear show a good acceptance in sweetness, astringency, and bitterness. Piga et al. (2000) obtained minimally processed prickly pears (Opuntia ficus-indica “Gialla” variety). They evaluated the effect of polystyrene trays and storage time at 4 C and 15 C. Results indicated that physicochemical and sensorial attributes did not show significant changes during 8 days at 4 C. White (Opuntia albicarpa) and red (Opuntia ficus-indica) prickly pears were peeled and submerged in chitosan solutions containing different concentrations of acetic acid (1.0% or 2.5%) to obtain ready-to-eat prickly pear products (Ochoa-Velasco and Guerrero-Beltra´n, 2014); physicochemical, antioxidant,
Figo da india—Opuntia spp.
199
microbiological, and sensory characteristics were assessed during 16 days of storage at temperatures of 4 6 1 C and 85 6 5% relative humidity. The quality sensory characteristics of white prickly pear coated with chitosan was unaffected during 16 d of storage; however, red prickly pear showed loss of firmness during this time, affecting its quality.
Pigments One of the recent uses of the pulp and peel of prickly pear is to obtain pigments. Prickly pear has an attractive color that varies from a pale green, green, yellow, orange, red, and redpurple hues (El-Samahy et al., 2007). These attractive colors are due to the betalains comprising the redviolet betacyanins and the yelloworange betaxanthins (Stintzing et al., 2003). These pigments maintain their appearance over a wide pH range (from 4 to 7), which makes them ideal pigments for coloring many foods (Stintzing et al., 2000).
FINAL REMARKS Biochemical, composition, manipulation, storing conditions, and fresh and processed products of prickly pear from a number of species of the genus Opuntia, a crop (even growing in wild conditions) that may resist extreme dry conditions in many areas around the world, have been performed and reported elsewhere. Opuntia spp., producer of prickly pears of many colors (white, green, yellow, orange, pink, red, and redpurple) and its composition (proximal composition and nutritive compounds) is a promising crop for growth many hot and dry parts around the world.
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Nutr. Diet. 77, 109134. Nobel, P.S., Russell, C.E., Felker, P., Medina, J.G., Acuna, E., 1987. Nutrient relations and productivity of prickly pear cacti. Agron. J. 79, 550555. Nobel, P.S., 1988. Environmental Biology of Agave and Cacti. Cambridge University Press, Cambridge, p. 270. Ochoa, C.E., Guerrero, J.A., 2012. Efecto del almacenamiento a diferentes temperaturas sobre la calidad de tuna roja (Opuntia ficus indica (L.) Miller). Inform. Tecnol. (Chile). 23 (1), 117128. Ochoa-Velasco, C.E., Guerrero-Beltra´n, J.A., 2013. Efecto de la temperatura de almacenamiento en las caracterı´sticas de calidad de tuna verde Villanueva (Opuntia albicarpa). Rev. Iberoam. Tecnol. Postcosecha. 14 (2), 149161. Ochoa-Velasco, C.E., Guerrero-Beltra´n, J.A., 2014. Postharvest quality of peeled prickly pear fruit treated with acetic acid and chitosan. Postharvest. Biol. Technol. 92 (2), 139145. Ochoa-Velasco, C.E., Guerrero-Beltra´n, J.A., 2016. The effects of modified atmospheres on prickly pear (Opuntia albicarpa) stored at different temperatures. Postharvest. Biol. Technol. 111, 314321. Odoux, E., Domı´nguez-Lo´pez, A., 1996. Le Figuier de Barbarie: une source industrielle de Betalaines? Fruits. 51, 6178. Paredes, O., Rojo, R., 1973. Estudio para el enlatado del jugo de tuna. Tecnol. Aliment. 8, 237240. Piga, A., Aquino, S.D., Agabbio, M., Emonti, G., Farris, G.A., 2000. Influence of storage temperature on shelf-life of minimally processed cactus pear fruits. Lebensm-Wiss Technol. 33, 1520. Piga, A., Aquino, S.D., Agabbio, M., Schirra, M., 1996. Storage life and quality attributes of cactus pears cv Gialla as affected by packaging. Agric. Mediterr. 126, 423427. Piga, A., Del Caro, A., Pinna, I., Agabbio, M., 2003. Changes in ascorbic acid, polyphenol content and antioxidant activity in minimally processed cactus pear fruit. Lebensm-Wiss Technol. 36, 257262. Piga, A., 2004. Cactus pear: a fruit of nutraceutical and functional importance. J. Prof. Assoc. Cactus Dev. 6, 922. Pinedo-Espinoza, J.M., Franco-Ban˜uelos, A., Herna´ndez-Fuentes, A.D., 2010. Comportamiento poscosecha de cultivares de tuna por efecto del manejo del huerto y temperatura de frigoconservacio´n. Revista Iberoamericana de Tecnologı´a Postcosecha. 11 (1), 4358.
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Pimienta-Barrios, E., Delgado-Alvarado A., Mauricio-Leguizamo R. (1987) Evaluacio´n de la variacio´n en formas de nopal tunero de la Zona Centro de Me´xico. Strategies for classification and management of native visitation for food production in Arid Zones. USDA/RM/SARH/INIFAP. General Technical Report RM-150. p 8286. Pimienta-Barrios, E., 1990. El nopal tunero. Universidad de Guadalajara, Guadalajara, Mexico, pp. 217235. Rodrı´guez, S., Orphee, C., Macias, S., Generos, S., Gomes, L., 1996. Tuna: Propiedades fı´sico-quı´micas de dos variedades. Aliment Latinoam. 210, 3437. Rodrı´guez-Herna´ndez, G.R., Gonza´lez-Garcı´a, R., Grajales-Lagunes, A., Ruiz-Cabrera, M.A., Abud-Archila, M., 2005. Spray-drying of cactus pear juice (Opuntia streptacantha): Effect on the physicochemical properties of powder and reconstituted product. Dry Technol. 23, 955973. Sa´enz, C., 2000. Processing technologies: an alternative for cactus pear (Opuntia app.) fruits and cladodes. J Arid Environ. 46, 209225. Sa´enz, C., Sepu´lveda, E., 2001. Cactus-pear juices. J Prof Assoc Cactus Develop. 4, 310. Sa´enz, C., Sepu´lveda E., Moreno M., 1995. Caracterizacio´n tecnolo´gica de pulpa de tuna roja. In: Proceedings of the XI Congreso Nacional de Ciencia y Tecnologı´a de Alimentos. Vin˜a del Mar, Chile. p 159. Sawaya, W.H., Khatchadourian, A., Safi, W.M., Al-Hammad, H.M., 1983. Chemical characterization of prickly pear pulp, Opuntia ficus-indica, and the manufacturing of prickly pear jam. J Food Technol. 18, 183193. Schirra, M., Inglese, P.E.R., La Mantia, T., 1999. Quality of cactus pear (Opuntia ficus-indica (L.) Mill.) fruit in relation to ripening time, CaCl2 pre harvest sprays and storage conditions. Sci Hortic-England. 81, 425436. Sepu´lveda, E., Sa´enz, C., 1990. Chemical and physical characteristics of prickly pear (Opuntia ficus-indica). Rev Agroquim Tecnol. 30, 551555. Sepu´lveda, E., Sa´enz, E., 2001. Ecotipos coloreados de tuna (Opuntia ficus-indica). Aconex (Chile). 72, 2932. ´ lvarez, M., 2000. Physical, chemical and sensory characteristics of dried fruit sheets of cactus pear (Opuntia ficus-indica Sepu´lveda, E., Sa´enz, C., A (L.) Mill.) and quince (Cydonia oblonga Mill.). Ital J Food Sci. 1, 4754. Sepu´lveda, E., Sa´enz, C., Moreno, M., 1995. Obtencio´n y caracterizacio´n de harina de nopal (Opuntia ficus-indica (L.) Miller) VI Congreso Nacional and IV Congreso Internacional sobre Conocimiento y Aprovechamiento del Nopal. Jalisco, Mexico. pp. 28-31 Sharma, R.R., Singh, D., Singh, R., 2009. Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: A review. Biol Control. 50, 205221. Stintzing, F.C., Carle, R., 2008. Betalains in food: occurrence, stability, and postharvest modifications. In: Socaciu, C. (Ed.), Food colorants: chemicals and functional properties. Taylor and Francis/CRC Press, Boca Raton, FL, USA. Stintzing, F.C., Schieber, A., Carle, R., 1999. Amino acid composition and betaxanthin in fruits from Opuntia ficus-indica. Planta Med. 65 (7), 632635. Stintzing, F.C., Schieber, A., Carle, R., 2000. Cactus peara promising component to functional food. Obst-Gemu¨se- und Kartoffelverarbeitung. 85, 4047. Stintzing, F.C., Schieber, A., Carle, R., 2003. Evaluation of colour properties and chemical quality parameters of cactus juices. Eur. Food Res. Technol. 216, 303311. Stintzing, F.C., Herbach, K.M., Mosshammer, M.R., Carle, R., Yi, W., Sellappan, S., et al., 2005. Color, betalain pattern, and antioxidant properties of cactus pear (Opuntia spp.) clones. J. Agric. Food Chem. 53, 442451. Tesoriere, L., Butera, D., Allegra, M., Fazzari, M., Livrea, M.A., 2005. Distribution of betalain pigments in red bool cells after consumption of cactus pear fruits and increased desistence of the cells to ex vivo induced oxidative hemolysis in humans. J. Agric. Food Chem. 53, 12661270. USDA, 2016. Plants profile for Opuntia (prickly pear). Planta Database. ,http://plants.usda.gov/core/profile?symbol5opunt.. Vignoni, L., Bauza, H.M., Bautista, P., Germano, C., 1997. Elaboracio´n de pulpa y mermelada de tuna (Opuntia ficus indica) preferencia y aceptabilidad. Resu´menes: X Seminario Latinoamericano y del Caribe de Ciencia y Tecnologı´a de Alimentos. Buenos Aires, Argentina, pp. 1022. Yahia, E.Y., 2012. Prickly Pear Fruit and Cladodes. In: Rees, D., Farrell, G., Orchard, J. (Eds.), Crop Post-Harvest: Science and Technology, first ed. Blackwell Publishing Ltd.
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Finger lime/The Australian Caviar—Citrus australasica Estelle Delort1 and Yong-Ming Yuan2 1
Firmenich SA, Geneva, Switzerland, 2Firmenich Aromatics Co. Ltd., Shanghai, China
Chapter Outline Botanical Classification Physiology and Harvest Season Sensory Characteristics, Chemical Composition, and Nutritional Value Sensory Characteristics and Volatile Composition
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Nutritional Value: Vitamins, Mineral, Phenolics, and Antioxidant Compounds Production and Industrial Applications of Commercialized Varieties References
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The long isolation history and the diversity of geological and climatic conditions found in Australia have led to a unique biodiversity with a vast number of endemic plant species (Konczak and Roulle, 2011). Many species have been consumed as food and medicine by the indigenous groups for thousands of years, but remain largely unknown to the rest of the population. Recently, interest has been growing in Australian native fruits for the development of so-called bushfood. Some native fruits were selected in the 1990s to be commercially cultivated, such as Davidson’s plum, muntries, riberries, quandong, Illawarra plum, and Kakadu plum (Graham and Hart, 1997). Shortly afterward, some Australian native citrus were also considered for commercial production (Robins, 2004). Compared to their citrus relatives, they adapted to the unusual soil and various climate conditions found in Australia, from extreme drought to rainforest (Riley, 2001). As a result, they have many traits of potential interest, including drought tolerance, shortened fruiting period, salt tolerance, disease resistance and dwarf habit, as well as a unique genetic diversity (Hamilton et al., 2005). Australia probably has the largest number of indigenous species within one country. Seven Citrus species are endemic: C. australasica F. Muell, C. australis Planch., C. glauca (Lindl.) Burkill, C. inodora F. M. Bailey, C. garrawayae F. M. Bailey, C. gracilis Mabb., and C. maideniana (Domin.) Swingle, the latter of which is sometimes reported as a variety or subspecies of C. inodora (Clarke and Prakash, 2001). There are also two Citrus species restricted to New Guinea: C. wintersii (synonym C. papuana) and C. warburgiana (Mabberley, 1998). The Australian species are known by a range of common names, including Australian finger lime for Citrus australasica, Australian round lime for Citrus australis, Australian desert lime for Citrus glauca, Russell River lime for Citrus inodora, Mount White lime for Citrus garrawayae, Kakadu lime or Humpty Doo lime for Citrus gracilis, and Maiden’s Australian wild lime for Citrus maideniana. Today, three of these species are commercially available: the finger lime, the round lime and the desert lime. With many additional traits not found in other citrus fruits, the finger lime is probably the most promising native citrus. Its unique caviar-like pulp, attractive color range, and organoleptic profile makes this lime a potential candidate to be marketed in the restaurant trade and as an ornamental plant. In 2013, it was reported as an emerging new trend as a fruit flavor (Anthony, 2013). However, the volatile and nutritional compositions of Australian finger limes have only recently been studied and reported in the literature.
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00025-3 © 2018 Elsevier Inc. All rights reserved.
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BOTANICAL CLASSIFICATION The Australian native Citrus species belong to the subtribe Citrinae of the tribe Citreae within the subfamily Aurantiodeae of the family Rutaceae. The world-renowned Citrus expert W. T. Swingle (18711952) assigned the native Australian and New Guinean Citrus species to the genera Eremocitrus (Australian desert lime) and Microcitrus (all other species). The term Eremocitrus was used to mark the xerophytic adaptation of the Australian desert lime, and the term Microcitrus was chosen to highlight the relatively smaller dimorphic leaves and slender twigs of the Australian and New Guinean species compared with those of all other Citrus plants. This separation from other species of Citrus was based on a number of characters that he believed to be distinctive, namely dimorphic foliage showing marked contrast between the juvenile and mature forms, flowers with free stamens and very short pistils, parallel venation of the leaves with very short wingless petioles, few-celled fruits with subglobose stalked pulp vesicles, and small rounded seed (Swingle, 1915). However, Mabberley (1998) recently reassessed the relationship of the Australian citrineae to the genus Citrus. On the basis of his taxonomic study, he considered these characteristics insufficient to create a new genus and reunited them with the genus Citrus (Mabberley, 1998). Since then, phylogenetic studies based on DNA sequences strongly supported the circumscription of the Australian and New Guinean species within the genus Citrus (Bayer et al., 2009).
PHYSIOLOGY AND HARVEST SEASON The Australian finger lime is native to the rainforests of the border ranges of south east Queensland and north east New South Wales. In its natural habitat, the finger lime grows as an understory shrub or tree up to 6 meters tall in a range of soil types. Trees are thorny, quite vigorous, and can tolerate light frost. However, in the wild they generally prefer being protected from excess wind and sun by taller native trees. On the north coast of New South Wales, flowering generally starts in June and extends through early October. Sporadic flowering may occur during Spring and Summer in warmer coastal regions. Depending on climatic conditions and variety, the fruit matures between December and May, with the main period occurring between March and May (Hardy et al., 2010). As shown in Fig. 1, the branchlets of young plants are almost horizontal, with short internodes and stiff erect spines. The juvenile leaves are oval or ovate. Mature leaves are ovate (cuneiform or subrhombic) and small (ca. 1.54 cm long and 1.22.5 cm broad) (Swingle, 1915). Finger lime fruits are cylindrical and fusiform (6.510 3 1.52.5 cm), often slightly curved and narrowed at both tip and base. The peel is rough with numerous oil glands. The pulp vesicles are nearly free or loosely cohering, longstalked, and ovoid, reminding one of caviar, which explains why finger lime is also called “lemon caviar.” Compared with other citrus fruits, the finger lime is also probably one of the most curious and interesting because of its unique natural genetic diversity, with trees and fruit varying in size, shape, color, and number of seeds. In the wild, skin colors range from yellow to green, red and purple, with many color variations in between. Pulp colors are generally green or yellow (Fig. 2). A naturally occurring form of this species, which has pink to red flesh and red to purple or even black skin, is often recognized as a distinct variety named C. australasica var. sanguinea. FIGURE 1 Finger lime tree. Source: Shutterstock.
Finger lime/The Australian Caviar—Citrus australasica
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A few reports have been published on the flower morphology and physiology of finger limes. The flowers of the Australian finger lime are small, borne singly or occasionally in pairs in the axillary of leaves, and usually 5-merous but sometimes 3- or 4-merous; the petals are white or slightly purple at the base and outer surface, imbricate in the buds, and reflexed or assurgent when open; the 2025 stamens are free and divergent; the pistils are short and stout, with an ovary containing 57 locules; and the ovules are numerous, with 816 in each locule (Clarke and Prakash, 2001; Swingle and Reece, 1967). The mature seeds of finger limes are generally whitish-cream to cream colored. Compared with the seeds of most cultivated Citrus species, they are smaller (ca. 67 mm long and 4 mm wide), round and textured on top, and usually flattened and smooth underneath, possibly due to the pressure of the pulp vesicles during seed development (Fig. 3). Recently, a comparative morphological characterization of the seeds of three Australian wild Citrus species (C. inodora, C. garrawayae, and C. australasica) was detailed by Hamilton et al. (2008). The seeds of the three native species were monoembryonic. C. australasica showed the greatest variability in the number of seeds per fruit, from fewer than 5 up to 39, depending on the location and date of harvest (Hamilton et al., 2008).
FIGURE 2 Finger lime fruits. Source: Shutterstock.
FIGURE 3 Finger lime seeds. Source: Firmenich SA.
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SENSORY CHARACTERISTICS, CHEMICAL COMPOSITION, AND NUTRITIONAL VALUE Sensory Characteristics and Volatile Composition The peel of finger limes is often described as having a powerful floral lime flavor and aroma, and the juice as being sour and rather strongly pungent. However, finger limes are as diverse in flavor as they are in peel and pulp color. In 2015, the sensory characteristics of three finger lime cultivars (cv. Alstonville, cv. Judy’s Everbearing and cv. Durham’s Emerald) were reported (Delort et al., 2015). A panel of perfumers and flavorists who were expert in citrus reported the organoleptic profile of the peel. Compared with that of the two most common lime varieties, Key lime (C. aurantifolia) and Tahiti lime (C. latifolia), the odor of the peel of finger limes was lime-like, but with more green notes and a less floral character. The odor of the peel varied from one cultivar to another: greener, terpenic, and slightly minty for cv. Alstonville; citronella-like, terpenic, mint-like, spicy, and fruity for cv. Judy’s Everbearing; and citronella-like, woody, phenolic, and slightly smoky notes for cv. Durham’s Emerald. The taste of the juice also depended on the cultivars. It was generally described to be in between that of lemon and lime juice, but with distinctive notes: bitter and slightly resinous for cv. Alstonville, green and citronellalike for cv. Judy’s Everbearing, and citronella-like with turpentine and vegetable notes for cv. Durham’s Emerald. The volatile composition of finger limes has been reported only recently, with all studies highlighting the unique volatile composition of finger lime compared with that of other citrus, as well as the presence of volatile molecules that have never been reported in any other citrus. In 1993, Trozzi et al. reported the volatile composition of a cold-pressed oil of “Faustrime”, a trigeneric hybrid of M. australasica 3 Fortunella sp. 3 Citrus aurantifolia, grown in Italy. High citronellal (16.3%) and piperitone (2.1%) content was observed, with limonene (43.2%), γ-terpinene (4.5%), α-phellandrene (4.5%) and terpinene-4-yl acetate (2.7%) as other major constituents (Trozzi et al., 1993). In 2000, the chemical composition of the peel essential oil of C. australasica var. sanguinea acclimatized in Sicily was investigated (Ruberto et al., 2000). Sixty-five components were identified by GC/MS analysis. The major volatile constituents were bicyclogermacrene (26%), α-pinene (10%), spathulenol (10%), and (Z)-β-ocimene (5.1%), whereas limonene was found as only 1.2% of the total oil. A few years later, the chemical compositions of the peel and leaf oil of 43 lemons and limes grown in Corsica were compared (Lota et al., 2002). Results showed that the lime species could be grouped into three chemotypes: limonene, limonene/β-pinene and limonene/β-pinene/γ-terpinene. In this study, the peel oil of C. australasica showed a unique pattern, sabinene (19.6%) being the second most abundant component after limonene (51.1%). In the study mentioned earlier, Delort et al. (2015) performed a comparative qualitative and quantitative analysis of the volatile composition of the three finger lime cultivars. The volatile constituents of three cultivars, namely cv. Alstonville, cv. Judy’s Everbearing and cv. Durham’s Emerald, were identified by GC/MS analysis and quantified by GC-FID. Three unique chemotypes were identified: limonene/sabinene for cv. Alstonville, limonene/citronellal/isomenthone for cv. Judy’s Everbearing, and limonene/citronellal/citronellol for cv. Durham’s Emerald. These chemotypes have never been reported in any other Citrus species. The comparative analysis also showed that some volatile molecules tended to be specific to one cultivar (e.g. aliphatic and terpenyl acetates in cv. Alstonville; citronellyl esters in cv. Judy’s Everbearing; 4-methylnonanal, cuminaldehyde and methyl thymol ether in cv. Durham’s Emerald). In addition, six volatile constituents were reported for the first time in a citrus extract and confirmed by synthesis. In a previous study by the same authors, six terpenyl esters had been identified for the first time in a finger lime peel extract having limonene/isomenthone/citronellal as the chemotype (Delort and Jaquier, 2009). In both studies, finger limes also differed from common lime species in that they had low amounts of γ-terpinene, α- and β-pinene, and citral. These studies indicate that the unique diversity observed externally is also observed at the molecular level. This may contribute to the unique organoleptic profile of finger limes and also suggests that the finger lime results from a different evolution compared with all other Citrus species.
Nutritional Value: Vitamins, Mineral, Phenolics, and Antioxidant Compounds Several studies have focused on the nutritious value of finger limes, likely stimulated by a growing interest in food with antioxidant activity. Polyphenols and anthocyanins in vegetables and fruits are known to protect human cells against oxidative damage by scavenging free radicals, and they play an active role in the prevention of cardiovascular disease, diabetes, arthritis, and cancer. Vitamin E, one of the most important lipophilic antioxidants, protects cells against lipid peroxidation. Minerals also have a key role in some reactions in the human body (oxygen transport, enzyme cofactors, etc.). In this context, different assays have been used to evaluate the antioxidant capacity of hydrophilic and lipophilic extracts obtained from commercially grown finger limes. The main potential sources of antioxidant capacity have been further studied: phenolic compounds, organic acids, minerals, anthocyanins, vitamin E, and vitamin C (Table 1).
TABLE 1 Antioxidant Capacity and Content of Total Phenolics, Organic Acids, Anthocyanins and Vitamins Reported in Australian Finger Limes Antioxidant capacity TEAC μmol TE/g FWa,b
Antioxidant capacity PCL μmol TE/g FWa,b
FL yellow (Netzel et al., 2007)
16.24 6 0.49
FL red (Netzel et al., 2007)
13.82 6 0.96
Antioxidant capacity FRAP μmol Fe21/g FW
Total phenolics μmol GAE/g FWb,c
Ascorbic acid mg/g FW
5.43 6 0.12
10.93 6 0.48
0.59 6 0.04
3.25 6 0.09
8.65 6 0.59
0.41 6 0.2
0.38 6 0.04
Antioxidant capacity ORAC-H μmol TE/g FW
Antioxidant capacity ORAC-L μmol TE/g FW
Citric acid mg/g FW
Total anthocyanins μmol CE/g FWd
Vitamin E mg/100 g FW
Lutein mg/100 g FW
FL green (Konczak et al., 2010)
12.6 6 0.5
45.9 6 6.6
11.86 6 1.25
6.8 6 0.4
0.26 6 0.01
46.8 6 0.47
0.52 6 0.03
0.40 6 0.03
FL pink (Konczak et al., 2010)
23.2 6 0.8
65.1 6 12.8
23.73 6 0.75
9.2 6 0.5
0.91 6 0.02
58.8 6 1.70
0.06 6 0.01
2.36 6 0.23
0.14 6 0.01
FL: finger lime; TEAC: Trolox equivalent antioxidant capacity; PCL: photochemiluminescence; FRAP: ferric reducing antioxidant power; ORAC-H: oxygen radical absorbance capacity for hydrophilic compounds; ORAC-L: oxygen radical absorbance capacity for lipophilic compounds. a The antioxidant capacity was expressed as micromoles of Trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid) equivalents (TE) per gram of fresh weight (μmol TE/g FW). b Values were corrected for ascorbic acid, which may react with the Folin-Ciocalteu (F-C) reagent and enhance the value. c The total phenolic content was determined by using the F-C assay and expressed as micromoles of total phenolics (gallic acid equivalents; GAE) per gram of fresh weight (μmol GAE/g FW). d The total anthocyanin content was expressed in cyaniding 3-glucoside equivalents (CE) per gram of fresh weight (μmol CE/g FW).
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In 2007, the antioxidant capacity of some Australian native fruits was investigated, including finger limes (yellow and red), plums and berries (Netzel et al., 2007). Trolox equivalent antioxidant capacity (TEAC) and photochemiluminescence (PCL) assays (radical-scavenging activity; RSA) showed some antioxidant activity in finger lime extracts, although it was half to 1/15 of that found in the other studied fruits. The levels of total phenolics and anthocyanins that may contribute to the antioxidant activity were determined by the Folin-Ciocalteu (F-C) assay. The total phenolic content was determined and corrected for the effect of ascorbic acid (Table 1). It was only about one third of that found earlier in blueberry (Netzel et al., 2006). A positive correlation was observed between the antioxidant activity and the total phenols, which indicates that the phenols play a major role in antioxidant activity. The contribution of anthocyanins was also investigated. The anthocyanin glycosides were separated and tentatively identified by HPLC/ESI/MS-MS. Yellow finger lime contained no anthocyanin, whereas the red variety contained cyanidin 3-glucoside and peonidin 3-glucoside as major anthocyanins in a proportion of ca. 2/1. The total anthocyanin content was relatively low, however, being only 3.3% of that reported in blueberry (Netzel et al., 2006). In 2010, the antioxidant capacity was investigated by using two other antioxidant assays: oxygen radical absorbance capacity for hydrophilic compounds (ORAC-H) and ferric reducing antioxidant power (FRAP) (Konczak et al., 2010). The level of total phenolics that was measured with the F-C assay was similar to that for red and yellow forms evaluated earlier (Table 1). The total phenolic values determined with the F-C assay were similar to those obtained by HPLC quantitation. Anthocyanins were also detected in pink finger limes, but in a lower amount than reported earlier. Organic acids were extracted for analysis. Results showed that finger limes are a good source of vitamin C (3-fold the level in mandarin), the second most abundant organic acid after citric acid (Table 1). In 2011, the same group investigated the contribution of lipophilic compounds to total antioxidant capacity (Konczak and Roulle, 2011). Results showed that these compounds are responsible for 20%26% of the total antioxidant capacity. The major lipophilic phytochemicals identified by HPLC were vitamin E (α-tocopherol, γ-tocopherol) and lutein. The level of vitamin E was particularly high in pink finger lime (2.4 mg/100 g FW) in comparison with the levels reported earlier for lemon (0.15 mg/100 g FW of juice, 0.25 mg/100 g FW of peels) and lime (0.22 mg/100 g FW of juice) (USDA, 2016). Lutein was detected in finger limes at levels 14- to 40-fold higher than that reported for lemon and grapefruit juice (ca. 0.010 mg/100 g FW) (USDA, 2016). Vitamin E and lutein are known to protect plant cells from photoinhibition and photooxidative stress. Such nutritional value is of interest, as in humans lutein improves visual function by protecting the retina from the damaging effects of free radicals produced by blue light. As hypothesized by the authors, the higher level of vitamin E and lutein in finger limes may be due to the exposure of native Australian plants to a higher level of UV radiation than for citrus fruits that are grown elsewhere. This exposure may have generated an increased accumulation of phytochemicals such as vitamin E and lutein, protecting plant cells from damaging UVB rays. In the same study, the mineral levels (potassium, phosphorus, calcium, magnesium, iron, zinc, manganese, selenium, copper, cobalt, nickel, aluminum, and lead) found in finger limes were measured and found to be similar to those in a range of vegetables and fruits produced and consumed in Europe and Mexico. In 2013, Sommano et al. investigated the antioxidant activity and the phenolic and flavonoid content in finger limes. The total phenol content was 457.5 mg/100 g. The percentage of radical scavenger activity (DPPH) at 1000 μg/mL was 87.20 and the antioxidant capacity (TEAC) was 28.46 TE/100 g. The nonvolatile constituents were further investigated by LC-MS analysis. Results showed that finger limes contain caffeic acid and vanillic acid.
PRODUCTION AND INDUSTRIAL APPLICATIONS OF COMMERCIALIZED VARIETIES Among native Australian and New Guinean Citrus species, the Australian finger lime is the most widely cultivated. The commercial production of finger lime began only in the past 20 years. Like any other citrus fruits, Australian native Citrus species hybridize easily, and their unique characteristics (drought and salinity tolerance, disease resistance, caviar-like pulp, peel and pulp color palette, etc.) have attracted the interest of citrus researchers and breeders. For the time being, a few selected finger lime varieties are commercially grown. Some were collected from the wild and grafted on modern citrus rootstock to improve their yield and quality of production. According to a recent article (Anon., 2014), there are about 30 finger lime growers in Australia, with orchard sizes varying from ca. 30 trees to 4000. The total production is estimated to reach about 10 tons per annum, half being exported to Europe and Asia, and is expected to increase. To date, seven finger lime cultivated varieties have been registered by the Australian Cultivar Registration Authority (ACRA), which is the International Registration Authority for Australian plant genera. Such registration ensures that the cultivated plants differ sufficiently from their wild ancestors to merit a special name, and it facilitates traceability during commercialization or propagation (Hardy et al., 2010). These cultivars are “Alstonville,” “Blunobia Pink Crystal,”
Finger lime/The Australian Caviar—Citrus australasica
209
“Byron Sunrise,” “Durham’s Emerald,” “Jali Red,” “Judy’s Everbearing” and “Pink Ice” (for more information on their origin, description and cultivation, see the ACRA website www.anbg.gov.au/acra and www.citruspages.free.fr). One finger lime variety (“Rainforest Pearl”) and two hybrids (“Australian Blood lime” and “Australian Sunrise lime”) have been submitted by the Commonwealth Scientific and Industrial Research Organization (CSIRO) for the registration of plant variety rights in Australia. “Rainforest Pearl” is a Citrus australasica var. sanguinea cultivar, which was selected for its pink pulp, ease of propagation, and vigor (Birmingham, 2002). “Australian Blood lime” is a natural hybrid between a zygotic seedling of Rangpur lime (Citrus limonia) and C. australasica var. sanguinea. It was selected for its striking red rind and flesh and pleasant aroma (Sykes, 1997). The trigeneric hybrid “Australian Sunrise lime” is an open-pollinated seedling selected from a Faustrimedin [C. australasica 3 (Fortunella sp. 3 C. reticulata)], a hybrid of the finger lime and the calamondin, the latter itself being a hybrid between kumquat and mandarine (Sykes, 1997). This variety has been grown commercially since 2001 and the fruit is appreciated for its juice or eaten as a whole fruit like a kumquat. These two hybrid varieties are currently used as orchard trees to produce fruits for the fresh fruit market, as well as for processing as jams and chutneys. “Rainforest Pearl” and “Australian Blood lime” are also sold as ornamental trees due to their highly colored fruits. Another trigeneric hybrid called ’Faustrime’ is grown mainly as an ornamental plant. It is a cross between the finger lime (C. australasica) and the limequat Eustis, itself a hybrid between a Mexican lime (C. aurantifolia) and a round kumquat (Fortunella japonica). The fruit is close to a finger lime but bigger and juicier. Unlike a finger lime, it has oval juice vesicles and yellow peel when ripe. Australian native Citrus can also hybridize. For example, the wild hybrid called “Sydney hybrid” results from a cross between two Australian native Citrus, Australian finger lime (C. australasica) and Australian round lime (C. australis) (Mabberley, 1998). Finger limes are one of the most curious citrus fruits, with many characteristics that are never or rarely found in other Citrus species: finger-like shape, caviar-like pulp, unique diversity in terms of peel and pulp color, and small monoembryonic seeds. On a molecular level, most studies done on the volatile composition of finger limes also indicate a divergent evolution from all other Citrus species. Regarding their nutritional benefits, preliminary results indicate a higher antioxidant potential than other common Citrus, but more studies are needed to confirm their nutritional value. All of these characteristics may be due to the isolation of Australia from other lands, as well as the unique soil and climate conditions found in the Australian rainforest to which finger limes had to adapt. First used by Australian chefs for so-called bushfood cuisine, this unique citrus has begun to be exploited in Australia in recent decades. Today, finger limes are becoming more and more popular all over the world, and the demand is growing rapidly, allowing this precious part of Australian heritage to enter the rest of the world.
REFERENCES Anon, 2014. Citrus caviar. Food Australia. 66 (4), 42. Anthony, M., 2013. Flavor and ingredient trends for the new year. Food Process. 7 (1), 3541. Bayer, R.J., Mabberley, D.J., Morton, C., Miller, C.H., Sharma, I.K., Pfeil, B.E., et al., 2009. A molecular phylogeny of the orange subfamily (Rutaceae: Aurantioideae) using nine cpDNA sequences. Am. J. Bot. 96, 668685. Birmingham, E., 2002. ‘Rainforest Pearl’. Plant Var. J. 15 (2), 3334. Clarke, K., Prakash, N., 2001. Studies on the Australian Rutaceae with particular reference to subtribe Citrinae. Malayan Nat. J. 55 (12), 231239. Delort, E., Jaquier, A., 2009. Novel terpenyl esters from Citrus australasica peel extract. Flavour Fragrance J. 24, 123132. Delort, E., Jaquier, A., Decorzant, E., Chapuis, C., Casilli, A., Fre´rot, E., 2015. Identification of unique citrus chemotypes and new volatile molecules. Phytochemistry. 109, 111124. Graham, C., Hart, D., 1997. Bushfoods. In: Hyde, K.W. (Ed.), The New Rural Industries. A Handbook for Farmers and Investors. Rural Industries Research & Development Corporation, Barton, ACT, Australia, pp. 225234. Hamilton, K.N., Ashmore, S.E., Drew, R.A., 2005. Development of conservation strategies for Citrus species of importance to Australia. Acta. Hortic. 694, 111115. Hamilton, K.N., Ashmore, S.E., Drew, R.A., 2008. Morphological characterization of seeds of three Australian wild Citrus species (Rutaceae): Citrus australasica F. Muell., C. inodora F.M. Bailey and C. garrawayi F.M. Bailey. Genet. Resourc. Crop Evol. 55 (5), 683693. Hardy, S., Wilk, P., Viola, J., Rennie, S., 2010. Growing Australian native finger limes. Primefact. 979, 112. Konczak, I., Roulle, P., 2011. Nutritional properties of commercially grown native Australian fruits: Lipophilic antioxidants and minerals. Food Res. Int. 44, 23392344. Konczak, I., Zabaras, D., Dunstan, M., Aguas, P., 2010. Antioxidant capacity and hydrophilic phytochemicals in commercially grown native Australian fruits. Food. Chem. 123 (4), 10481054.
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Lota, M.-L., De Rocca Serra, D., Tomi, F., Jacquemond, C., Casanova, J., 2002. Volatile components of peel and leaf oils of lemon and lime species. J. Agric. Food. Chem. 50, 796805. Mabberley, D.J., 1998. Australian Citreae with notes on other Aurantioideae (Rutaceae). Telopea. 7, 333344. Netzel, M., Netzel, G., Tian, Q., Schwartz, S., Konczak, I., 2006. Sources of antioxidant activity in Australian native fruits. Identification and quantification of anthocyanins. J. Agric. Food. Chem. 54, 98209826. Netzel, M., Netzel, G., Tian, Q., Schwartz, S., Konczak, I., 2007. Native Australian fruits—A novel source of antioxidants for food. Innovat. Food Sci. Emerging Technol. 8 (3), 339346. Riley, J.M., 2001. Wild fruits of Australia. West Austral. Nut Tree Crops Assoc. Yearb. 25, 1622. Robins, J., 2004. Native foods overview. In: Salvin, S., Bourke, M., Byrne, T. (Eds.), The New Crop Industry Handbook. Rural Industries Research & Development Corporation, Barton, ACT, Australia, pp. 417426. Ruberto, G., Rocco, C., Rapisarda, P., 2000. Chemical composition of the peel essential oil of Microcitrus australasica var. sanguinea (F.M. Bail) Swing. J. Essential Oil Res. 12, 379382. Sommano, S., Caffin, N., Kerven, G., 2013. Screening for antioxidant activity, phenolic content, and flavonoids from Australian native food plants. Int. J. Food Prop. 16 (6), 13941406. Swingle, W.T., 1915. Microcitrus, a new genus of Australian citrous fruit. J. Washington Acad. Sci. 5, 569578. Swingle, W.T., Reece, P.C., 1967. The botany of Citrus and its wild relatives. In: secnd ed Reuther, W., Webber, H.J., Batchelor, L.D. (Eds.), The Citrus Industry, vol. I. University of California, Riverside, pp. 190423. Sykes, S.R., 1997. Australian native limes (Eremocitrus and Microcitrus). Austral. Bushfoods. 3, 1215. Trozzi, A., Verzera, A., Stagno d’Alcontres, I., 1993. Constituents of the cold-pressed oil of Faustrime, a trigeneric hybrid of M. australasica sp. 3 Fortunella sp. 3 C. aurantifolia. J. Essential Oil Res. 5, 97100.
Gooseberry—Ribes uva-crispa, sin. R. grossularia L Stanislaw Pluta Research Institute of Horticulture, Skierniewice, Poland
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Fruit Physiology and Biochemistry Estimated Annual Production Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolics, and Antioxidant Compounds
211 212 213 214
Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Market Potential References
215 215 217 217 218
215
CULTIVAR ORIGIN AND BOTANICAL ASPECTS The gooseberries and currants belong to the genus Ribes L., which includes more than 150 different species of shrubs (bushes). They are native throughout northern Europe, Asia, North America, and in mountainous areas of South America and northwest Africa (Brennan, 1996; Barney and Hummer, 2005). Cultivated types of gooseberries are divided into two major groups: European (Ribes grossularia var. uva-crispa), and American (Ribes hirtellum). In North America besides R. hirtellum, other species (Ribes divaricatum Dougl. and Ribes oxyacanthoides L.) were used in conjunction with R. grossularia to increase berry size (Brennan, 2005). Within the European types, fruit size varies widely, from pea size to as large as a small egg. The skin color of berries can also be different, with fruit maturing of green, yellow, white, pink, red, and purple. This diversity is due to the historical popularity of the European gooseberry. Over the past two centuries, hundreds of cultivars have been developed, with a focus on prize-winning fruit size and color. Native American gooseberry species have smaller fruit size and less flavor, but are very resistant to diseases compared to European cultivars, which are noted for powdery mildew and leaf spot susceptibility. This has limited their commercial growing, because they require significant fungicide applications to ensure regular cropping. However, disease resistance is improving through additional breeding with American types, and several new promising European cultivars have been released and introduced into cultivation in many countries. Natural polyploidy occurs only rarely in Ribes (Brennan 1996), although experimentally induced polyploids have been utilized by Nilsson (1959, 1966) and Keep (1962), mainly in the development of allotetraploids through interspecific hybridization. The basic chromosome number of all Ribes species is x 5 8, cultivars are diploid (2n 5 2x 5 16), (Zielinski, 1953). Gooseberries grow on a bush approximately 11.8 m tall and about 11.2 m wide. Most gooseberries have spines or thorns at each of the leaf nodes. The spines may be single, double, or triple, and they may be large (1015 mm) to small (15 mm). The habit of the plant may vary from low spreading to upright and tall. Flowers occur in axillary clusters of one to three (much fewer than those on currant racemes), are pale green, sometimes pinkish, and have a hemispherical hypanthium, reflexed sepals, and short white petals (Fig. 1). Berry color may vary from green to yellow/ green, to yellow, or white, to pink, to red, to dark red or purple (Fig. 2). The size of the berries varies from about 1.5 g to more than 12 g. The average is about 36 g. The berries are usually borne in ones, twos, or threes, and hang under Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00027-7 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Flowers of gooseberry (Ribes grossularia L.).
FIGURE 2 Yellowgreen fruits cv. “White Smith” (left) and red cv. “Captivator” (right).
the branches. The taste ranges from very tart to very sweet. Gooseberries are generally classified as dessert berries, those that are used raw, and culinary, or “cookers” that are used primarily for processing or cooking. There are some that fall into both categories depending on the stage of ripeness when picked. Generally the dessert berries are larger and used when completely ripe. The culinary berries are generally smaller, a little tart and used before they are fully ripe. Some growers use some of the dessert type berries while still unripe as cookers and as a means of thinning and using the crop. The remaining berries become larger and are used as they ripen. Some of the cultivars used as dessert berries are: “Achilles”, “Captivator”, “Early Sulphur”, “Hoenings Earliest”, “Invicta”, “Hinnomaki Red”, “Hinnomaki Yellow”, “Whinham’s Industry”, “Telegraph” and “Tixia”. Some of the culinary cultivars are: “Careless” (dual use), “Oregon Champion”, “Poorman”, “Red Jacket”, “Whitesmith” and (“Pixwell” less recommended). There are many other cultivars available in varying supplies that could be used in plantings for berries for sale at farmer’s markets or big commercial plantations with machine fruit harvesting.
HARVEST SEASON Generally, gooseberries ripen starting about mid-June and the latest are ripe about mid-July. The seasons may vary a week or more either way, depending on cultivar, the weather, and your location. For fresh and juice use, fruit should be allowed to reach full ripeness and color expression. For cooking (processing), fruit are harvested when they reach a typical color and an acceptable size. For handpicked fresh fruit, the gooseberries are often harvested in three pickings. During the first picking, one-third of the ripe or nearly ripe fruit are removed evenly from throughout the bush. A week
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213
FIGURE 3 Two types of harvesters: half-row “Arek” (left) and self-propelled “Victor” (right).
later, half of the remaining ripe fruit are collected and the rest on well-exposed spurs on the outside of the bush are left. Finally, the remainder of the fruits are harvested, when they are fully ripe. Gooseberries from the first two pickings is normally used for processing. Fruits from the last picking are usually larger and sweeter, and are suitable for fresh or processing. On small-scale production, hand harvesting still remains the most economical method of harvest, but adds significant cost to production and profitability. Fruit are produced in small groups or singly on stems, and are picked individually by hand on small plantations or in case of selling fruits as dessert on fresh market. Gooseberries can be difficult to harvest if shoots of the cultivar are thorny and it requires the use of gloves. For large commercial plantations, specialized mechanical harvesters have been developed in Europe for both currants and gooseberries. Fruit destined for processing are harvested once using two types of harvesters: half-row and self-propelled (over-the-row) (Fig. 3), although the fruits tend to be punctured by thorns during harvest. Gooseberries are harvested when they are full size but not yet ripe. Commercially, this is called the green berry trade (or the technological ripening of fruit), which is preferred for pies and jam. An average yield from one gooseberry bush in the full fruiting period (56 year-old plants) is between 4 and 5 kg of fruit. On commercial plantations the fruit yield of 1215 MT (or more) is harvested depending on cultivar and their maintenance.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Soft fruits, including gooseberries, share some common features during their development with a wide diversity of fleshy fruits, both edible and inedible. An initial phase of growth and enlargement is followed by a maturation phase during which the fruit acquires the capacity to ripen. Ripening itself is defined by a set of physico-chemical changes characteristic of each fruit. These usually involve transitions in color arising from the degradation of existing pigments and the synthesis of new and often intensely colored pigments, texture changes resulting in tissue softening, and sometimes liquefaction, and the production of highly distinctive flavors and aromas which affect the palatability of the fruit. Changes involving senescence occur throughout development and are most obvious in the later stages as the fleshy tissues disintegrate, leaving the seeds to survive. Ripening is thus part of a continuous developmental process in which several physiological phases may overlap (Seymour et al., 1993). In the literature little is known on fruit physiology and biochemistry of the gooseberry fruit. According to Seymour et al. (1993) of the soft fruits the strawberry (Fragaria x annanassa) is perhaps the best studied in terms of its physiology and biochemistry. Much of the information inevitably relates to the strawberry but where appropriate, other soft fruits are referred to. Fruit of the strawberry grow rapidly, with full size being attained approximately 30 days after anthesis, depending upon conditions and cultivar. For gooseberry fruit growth and development into mature size takes longer, about 5060 days after pollination. For most soft fruits ripening occurs rapidly and fruit retain optimum condition for a relatively short time. Most of the earlier data on composition of soft fruits is still accurate and relevant today and referred to (e.g., Hulme, 1971). However, advances in analytical techniques have improved the quantitative aspects of analysis and biochemistry of these fruits. Sugars are important in flavor and they are one of the main soluble components in soft fruit and provide energy for metabolic changes. For strawberry and other soft fruits, sucrose, glucose, and fructose account for more than 99% of the total sugars in ripe fruit, with sorbitol, xylitol, and xylose occurring in trace amounts (Makinen and So¨derling, 1980). Like sugars, organic acids are important flavor components and sugar/acid ratios are often used as an index of consumer acceptability and quality in fruits. Acids can affect flavor directly and are also important in processing, as they affect the formation of off-flavors and the gelling properties of pectin. The pigments in fruits, especially in
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soft fruits (highly colored), are important aesthetic components, they are natural indicators of fruit ripeness and some pigments including carotenoids and flavonoids have vitamin activity. Many present day cultivars of these fruits may have complements of pigments which are the result of breeding and color selection. Much of what is known about the pigment composition of soft fruits can be found in Hulme (1971). Phenolics comprise a diverse group of substances including the secondary plant metabolites polyphenols (tannins), proanthocyanidins (condensed tannins) and esters of hydroxybenzoic acids and hydroxycinnamic acids. Phenolics are normal constituents of fruits (Hulme, 1971; Foo and Porter, 1980, 1981) affecting their taste, palatability and nutritional value. The aroma of soft fruits is an important component of their flavor. The relative abundance of individual volatiles from a fruit is a ’finger print’ of a particular cultivar and species. Studies were made on the qualitative composition of volatiles from strawberry; esters, alcohols and carbonyls are important for its fruity flavor. The mixture of volatiles from strawberry is complex, with over two hundred compounds having been identified (Tressl et al., 1969). Seymour and co-authors (1993) noted that information on the metabolic pathways and enzymes in soft fruits related to ripening was very limited, even for the strawberry. This situation not only reflects the relatively low economic value of soft fruit compared with, for example, apples, but also the technical difficulties encountered in isolating enzymes and unraveling the biochemistry of recalcitrant fruit such as the strawberry on account of its high levels of polyphenols and soluble pectins that interfere with protein purification.
ESTIMATED ANNUAL PRODUCTION The United Nations Food and Agriculture Organization database (FAOSTAT, 2017) show approximately worldwide gooseberry production in the countries, where this crop is cultivated (Table 1). TABLE 1 Gooseberry Fruit Production (Metric Tons—MT) in the World, in 200814 Countries
2008
2009
2010
2011
2012
2013
2014a
1
Austria
1815
1654
1654
2359
1875
1895
1920
2
Belgium
100
100
110
89
90
100
100
3
Czech Republic
3021
3326
3000
3100
3100
2246
2115
4
Denmark
106
98
249
358
436
252
259
5
Estonia
121
117
147
141
163
141
132
6
Finland
30
67
55
71
52
52
35
7
Germanyb
83,888
82,000
64,246
75,904
77,000
82,683
88,191
8
Hungary
1700
1870
904
829
745
870
720
9
Kyrgyzstan
100
100
100
110
115
120
120
10
Latvia
12
4
5
5
3
22
37
11
Lithuania
270
347
350
300
300
100
125
12
New Zealand
10
10
10
10
10
11
11
13
Poland
16,156
15,787
14,189
14,590
16,318
14,987
12,448
14
Republic of Moldova
5
8
5
7
2
3
15
15
Russian Federation
52,000
54,000
48,000
54,000
51,000
55,000
55,000
16
Slovakia
135
60
66
66
23
1
17
Switzerland
50
74
77
80
67
76
71
18
Ukraine
6800
6100
6800
7300
7500
7300
6810
19
United Kingdom
2200
2600
2550
2514
2620
2364
2406
168,384
168,397
142,511
161,833
161,462
168,245
170,516
Lp.
Total a
The latest and final statistic data available for 2014. The production level (figures) seems to be very overestimated.
b
Gooseberry—Ribes uva-crispa, sin. R. grossularia L
215
According to the official data from the FAO of the United Nations (FAOSTAT, 2017), the total fruit production of gooseberry has ranged from 142.5 to 170.5 metric tons (MT) in recent years. The highest gooseberry production was recorded in 2008 and 2009, it declined by 2010 (probably inferable weather conditions and spring frost injuries) and increased again to 168.2 and 170.5 MT in 201314, respectively. According to experts, the total production is very overvalued due to the gooseberry production in Germany, which appears to be very overstated (overestimated, probably 10 times). Germany, Russian Federation, and Poland are the largest world’s gooseberry producers. The steady increase trend in gooseberry production (6.87.5 MT) appeared in Ukraine in 201014. In Austria, Czech Rep., Hungary, and United Kingdom, this production is between 1.0 and 3.3 MT. Other countries produce gooseberries on a small scale from a few to several hundred tons of fruit (Table 1).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING, VITAMINS, MINERAL, PHENOLICS, AND ANTIOXIDANT COMPOUNDS The gooseberry fruit contains more than 80% water. It also has protein, carbohydrate, fiber, minerals, vitamins, and lipids (Table 2). Gooseberry fruits are a natural source of organic acids, such as citric acid (1114 mg/100 g of fresh mass [fm]), malic acid (1013 mg/100 g of fm), and shikimic acid (12 mg/100 g of fm). Organic acids are responsible for the characteristic tart and sour taste of the fruits and these compounds have application in the food industry. They are widely used in the manufacture of juices and beverages as pH regulators and preservatives (Stewart, 2005; Flores, et al., 2012). It was reported that citric acid inhibits Listeria monocytogenes bacteria, it was also found that malic acid was a more effective inhibitor of thermophilic bacteria than acetic or lactic acids (Theron and Lues, 2011). Thanks to their chelating properties, organic acids may reduce human susceptibility to diseases. Compounds such as citric, tartaric, malic, succinic, fumaric, glutaric and ketoglutaric acids may decrease the risk of stroke and Alzheimer’s disease if consumed on a regular basis (Keenan et al., 2010). Phenolic compounds are important antioxidant components of gooseberry fruits, with a total content of approx. 190 mg/100 g of fm (Moyer et al., 2002). The main constituent group of phenolic compounds in gooseberry fruits consists of flavonols, including quercetin, myricetin, and kaempferol. The following phenolic acids have been identified in gooseberry fruits: caffeic, coumaric, hydroxybenzoic, and ellagic. It has been shown that consumption of products rich in polyphenolic compounds may reduce the risk of cardiac and cardiovascular disorders by antioxidant action towards low-density lipoproteins (LDLs), delaying the process of arteriosclerosis (Borkowska, 2003). In vitro studies have revealed a potentially beneficial effect of gooseberry fruit extracts in the treatment of type 2 diabetes and hypertension (Pinto et al., 2010). Consumption of berries from various sources including the genus Ribes (currants and gooseberries) has been associated with diverse potential health benefits. The 14 examined cultivars of European gooseberry (R. grossularia L.) contained in various proportions the 3-glucoside, 3-rutinoside, 3-xyloside, 3-O-beta-(6v-E-caffeoylglucopyranoside), and 3-O-beta(6v-E-p-coumaroylglucopyranoside) of cyaniding, the 3-rutinoside and 3-glucoside of peonidin (Jordheim et al., 2007).
SENSORY CHARACTERISTICS The flavor quality of food (including fruits) is a combination of the sensory impressions of taste detected by the tongue and aroma sensed by the nose. Information on the flavor chemistry of natural and processed fruit products is of great importance to the food industry for determining optimal harvesting dates and storage conditions, and for the production of essences (Seymour et al., 1993). Fruit quality covers a range of traits, including physical characters such as berry size, berry color, berry conformation (drupelet structure and cohesion), firmness and shelf-life in the case of fresh fruit, and characters linked to chemical composition, such as color, sweetness, sourness, and flavor intensity and the levels of nutritionally important compounds. The selection of new Ribes (blackcurrant and gooseberry) cultivars with improved sensory profiles, leading to enhanced consumer acceptability, has become one of the main objectives in most contemporary breeding programs (Brennan and Graham, 2009).
HARVEST AND POSTHARVEST CONSERVATION Old bushes should be regularly pruned to keep them open, which not only facilitates harvesting, but improves fruit quality. As with all berries, harvest and postharvest care of fruit can extend the shelf life of fruit. Berries of some of
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TABLE 2 Chemical Composition and Nutritional Value of Gooseberry (Ribes grossularia) Fruit (Nutrient Values and Weights are for Edible Portion) Nutrient
Unit
Value per 100 g
1 cup 150 g
Proximates Water
g
87.87
131.80
Energy
kcal
44
66
Protein
g
0.88
1.32
Total lipid (fat)
g
0.58
0.87
Carbohydrate, by difference
g
10.18
15.27
Fiber, total dietary
g
4.3
6.4
Calcium, Ca
mg
25
38
Iron, Fe
mg
0.31
0.46
Magnesium. Mg
mg
10
15
Phosphorus, P
mg
27
4C
Potassium, K
mg
198
297
Sodium, Na
mg
1
2
Zinc, Zn
mg
0.12
0.18
Vitamin C, total ascorbic acid
mg
27.7
41.6
Thiamin
mg
0.040
0.060
Riboflavin
mg
0.030
0.045
Niacin
mg
0.300
0.450
Vitamin B-6
mg
0.080
0.120
Foliate, DFE
mg
6
9
Vitamin B-12
mg
0.00
0.00
Vitamin A, RAE
mg
15
22
Vitamin A, IU
IU
290
435
Vitamin E (alpha-tocopherol)
mg
0.37
0.56
Fatty acids, total saturated
g
0.038
0.057
Fatty acids, total monounsaturated
g
0.051
0.076
Fatty acids, total polyunsaturated
g
0.317
0.476
Fatty acids, total trans
g
0.000
0.000
Cholesterol
mg
0
0
Minerals
Vitamins
Lipids
Sources: USDA National Nutrient Database for Standard Reference Release 28, Software v.2.3.2 The National Agricultural Library, Basic Report 09107, Gooseberries, Raw, Report Date: October 24, 2015.
Gooseberry—Ribes uva-crispa, sin. R. grossularia L
217
gooseberry cultivars hang longer on the plant and others will ripen off the plant. They ripen slowly in cold storage. Gooseberries generally lose their distinct venation as they ripen and become overripe—the fruit develops a stronger, mustier flavor, loses acid, and can become mealy. Hand harvesting: At harvest, one should avoid pricking gooseberries on thorns, and leave the blossom and stem end of the berry intact. Avoid bruising fruit. In all Ribes crops, including gooseberry, free moisture should be avoided, and berries should be shaded in the field and chilled as quickly as possible. Machine harvesting: It is a popular method of fruit harvesting on commercial plantations of gooseberry and currants (black and red) used mainly in Europe. Proper adjustment of harvesters’ shakers is critical so that a thorough job of picking is undertaken, fruits are not damaged and the bushes are not badly beaten. Very little fruit destined for fresh market is harvested by machines because the damage likely to be caused to them could result in rapid deterioration in quality during the marketing chain. Fruit destined for processing are harvested mechanically. However, it usually important to process it very soon after harvesting. Precooling is applied to achieve maximum storage life for many fruit crops or reduce losses during their marketable life. So it is essential to keep them at the most appropriate temperature which is usually just above that which will cause chilling or freezing injury. To maximize the effect of precooling the crop should be brought to the optimal temperature as quickly as possible after harvest. Precooling always needs to be combined with a cold chain. It means that crops are transferred to storage at the optimum temperature directly after precooling. Forced air cooling with high humidity was the most acceptable method. Air cooling in a conventional cold store was suitable and hydrocooling and vacuum cooling less suitable for these fruits. Gooseberry fruit can be stored at 2.2 C4.4 C for two to three weeks, but at lower temperature (0.5 C) for as long as four to six weeks. Certain gooseberry cultivars were held for as long as 3 months at 0 C in air (McKay and Van Eck, 2006), but for even longer storage they suggested harvesting at the green mature stage and placing them at 0.5 C to 0.9 C with 93% r.h. in 2.5%3.0% O2 1 20%25% CO2. Also the Control Atmosphere (CA) storage methods have been developed for these fruits. Gooseberries and redcurrants can be kept a number of months with palletized CA storage (Thompson, 2014).
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Gooseberry (R. grossularia) belongs to a group of minor fruit crops. However, in some countries such as Germany, Russia, Poland, or Scandinavia, gooseberries are cultivated on large commercial plantations. Increasing gooseberry production is of high economic interest for many gooseberry growers. In addition, this crop is a good supplement to the cultivation of blackcurrants (R. nigrum) and redcurrants (R. rubrum) to reduce the risk of production and expand the use of machines for the maintenance of the plantations and especially fruit harvesting. In Europe, mechanical harvesting is commonly applied in the commercial gooseberry (and currants) plantations. Different types of harvesters have been developed and manufactured by several companies in different countries. Gooseberries that are harvested by machines are destined mainly for processing and freezing (including IQF). For this technology bushes are planted closer: 3.54.0 m between rows and 0.40.6 m in row spacing, as a tight hedgerow is critical for success in mechanical harvesting. Gooseberries are grown for 1015 years when proper weeding, fertilizing, pruning and plant protection against major fungal diseases and pests are provided on plantations. Fruit are ’stripped’ of berries while still fairly green (unripe) and hard. Gooseberries for the fresh market, when berries are generally handpicked, are often planted at the density of 2.5 3 1.0 m, unless trained to vertical cordons. Details on this training system recommended for gooseberries (and redcurrants) are provided by McKay (2005), and McKay and Van Eck (2006). In countries such as Canada and the USA, gooseberries (also currants) are often planted in the pick-your-own (PYO) operations using different spacing, depending on the training system and equipment. It is very important to know about the growth habit of your selected cultivars and the space requirements of equipment. It is important especially, if you plan to mechanically harvest, because the growth and branch structure of the crop make machineharvesting difficult to achieve effectively without considerable damage to the plant.
MARKET POTENTIAL Gooseberries are relatively easy to grow and local supply can quickly meet consumer demand. These fruits have the greatest potential for fresh market sales. However, preserving the berries for sale during the off-season may also be a way of diversifying a grower’s offerings and spreading the risk of production for a new crop across different target markets.
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As with all specialty crops, gooseberry producers should estimate the local production and demand before investing in producing and marketing. Decisions to commercially produce “minor” small fruit crops such as the gooseberry should be driven by the availability of market outlets for the fruit. A market should be secured before plants are set in the ground. Fresh fruit sales are options for direct marketers, although most consumers are unfamiliar with the fruit and its uses. Consequently, processing the crop into jams, jellies, and fresh juice in addition to other products may be the best way to utilize these fruits. In Europe, significant fresh and processing markets exist and may be an indication of the undeveloped market potential in different countries. Growers near populations of people who are already familiar with the crop may have a ready market. Successful and profitable production of these unique fruit involves knowledge of cultivars, their horticultural characteristics and requirements as well as proper management of plantation, including agro-technical treatments and plant protection against pests and diseases.
REFERENCES Barney, D.L., Hummer, K.E., 2005. Currants, Gooseberries, and Jostaberries: A Guide for Growers, Marketers, and Researchers in North America. New York: Haworth Press Inc, 260 p. Borkowska, J., 2003. Fruits and vegetables as source of natural antioxidant. Przem. Ferm. Ow. Warz. 5, 1112. Brennan, R.M., 1996. Currants and gooseberries. In: Janick, J., Moore, J.N. (Eds.), Fruit Breeding, Vol. II: Vine and Small Fruits Crops. John Wiley and Sons, Inc, New York, pp. 191295. Brennan, R.M., 2005. Currants and gooseberries (Ribes L.. In: Janick, J. (Ed.), The Encyclopedia of Fruit and Nut Crops. CABI (in press). Inc, New York, pp. 191295. Brennan, R., Graham, J., 2009. Improving Fruit Quality in Rubus and Ribes through Breeding. Funct. Plant Sci. Biotechnol. 3 (Special Issue 1), 2229. Flores, P., Hellı´n, P., Fenoll, J., 2012. Determination of organic acids in fruits and vegetables by liquid chromatography with tandem-mass spectrometry. Food Chem. 132, 10491054, http://dx.doi.org/10.1016/j.foodchem.2011.10.064. Foo, L.Y., Porter, L.J., 1980. The phytochemistry of proanthocyanidin polymers. Phytochemistry. 19, 17471754. Foo, L.Y., Porter, L.J., 1981. The structure of tannins of some edible fruits. J. Sci. Food Agric. 31, 711716. Food and Agriculture Organization of the United Nations, 2017. FAOSTAT. ,http://faostat3.fao.org. [21.10.17]. Hulme, A.C., 1971. The Biochemistry of Fruits and Their Products, vol. II. Academic Press, New York. Jordheim, M., Ma˚ge, F., Andersen, Ø.M., 2007. Anthocyanins in berries of Ribes including gooseberry cultivars with a high content of acylated pigments. J. Agric. Food Chem. 55 (14), 55295535. Available from: http://dx.doi.org/10.1021/jf0709000. Keenan, B.M., Robinson, S.R., Bishop, G.M., 2010. Effects of carboxylic acids on the uptake of non-transfer in-bound iron by astrocytes. Neurochem. Int. 56, 843849, http://dx.doi.org/10.1016/j.neuint.2010.03.009. Keep, E., 1962. Interspecific hybridisation in Ribes. Genetica. 33, 123. Makinen, K.K., So¨derling, E., 1980. A quantitative study of mannitol, sorbitol, xylitol and xylose in wild berries and commercial fruits. J. Food Sci. 45, 67371. McKay, S., 2005. Improved fresh fruit quality of gooseberries and red currants with the cordon training system. N.Y. Fruit Q. 13 (2), 2932. McKay, S., Van Eck, A., 2006. Red currants and gooseberries: extended season and marketing flexibility with controlled atmosphere storage. N.Y. Fruit Q. 14 (1), 4345. Moyer, R.A., Hummer, K.E., Finn, C.E., Frei, B., Wrolstad, R.E., 2002. Anthocyanins, phenolics, and antioxidant capacity in diverse small fruits: Vaccinium, Rubus, and Ribes. J. Agric. Food Chem. 50, 519525, http://dx.doi.org/10.1021/jf011062r. Nilsson, F., 1959. Polyploidy in the genus Ribes. Genet. Agric. 11, 225242. Nilsson, F. 1966. Cytogenetic studies in Ribes. In: Proc. Balsgard Fruit Breeding Symposium, Fjalkestad, pp. 197204. Pinto, M.D.S., Kwon, Y.I., Apostolidis, E., Lajolo, F.M., Genovese, M.I., Shey, K., 2010. Evaluation of red currants (Ribes rubrum L.) red and green gooseberries (Ribes uva-crispa) for potential management of type 2 diabetes and hypertension using in vivo models. J. Food Biochem. 34, 639660. Available from: http://dx.doi.org/10.1111/j.1745-4514.2009.00305.x. Seymour, C., Taylor, J., Tucker, G., 1993. Biochemistry of Fruit Ripening (Edited). Chapman & Hall, London, ISBN 0412 40830 9. Stewart, K., 2005. Processing of Cranberry, Blueberry, Currant and Gooseberry. In: Barre, D.M., Somogyi, L., Ramsawamy, H. (Eds.), Processing Fruits: Science and Technology. CRC Press, Boca Raton, FL, USA, pp. 563584. Theron, M.M., Lues, J.F.R., 2011. Nature and Composition of Organic Acids, Organic Acids and Food Preservation, 2011. CRC Press, Boca Raton, FL, USA, pp. 2938. Thompson, A.K., 2014. Fruit and Vegetables: Harvesting, Handling and Storage. John Wiley & Sons Inc, Hoboken, New Jersey. Tressl, R., Drawert, F., Heimann, W., 1969. Gaschromatographischmassenspektrometrische Bestandsaufnahme von ErdbeerAromastoffen. Z. Naturforsch. B24, 12011202. Zielinski, Q.B., 1953. Chromosome numbers and meiotic studies in Ribes. Bot. Gaz. 114, 265274.
Grumixama—Eugenia brasiliensis Lam Luciane de L. Teixeira, Neuza M.A. Hassimotto and Franco M. Lajolo University of Sa˜o Paulo, Sa˜o Paulo, Brazil
Chapter Outline Introduction Plant Chemical and Nutritional Composition Phytochemical Profile Harvest Season and Production: Purple Grumixama
219 219 219 220 222
Potential Industrial Application Acknowledgment References Further Reading
223 223 223 224
INTRODUCTION The grumixama (Eugenia brasilienses Lam.) belongs to the Myrtaceas family. It is a little cherry also known as grumichama, cumbixaba, ibaporoiti, or Brazilian cherry (Suguino et al., 2011). The name “grumixama” derived from the Tupi-Guarani “guamicha˜”, a language spoken by the natives who inhabited the Brazilian coast, which means “which should pick up in the tongue” due to the quite palatable taste (Schaffer, 2013). The grumixama is a rustic plant growing and distributed in the south and southeast regions of Brazil (Flores et al., 2012). Its fruits are known to be a good source of bioactive compounds, usually present in fresh fruit and vegetables, which are related to health promotion and for reducing the risk of chronic disease development. The main bioactive compounds present in grumixama fruits are the phenolic compounds, mainly flavonoids and ellagitannins (Okuda et al., 1982; Fracassetti et al., 2013; Abe et al., 2012; Reynertson et al., 2008). In the plant, flavonoids contribute to protecting and minimizing the ultraviolet damage in plant tissues and to protect against biotic stress (Reynertson et al., 2008). In humans, flavonoids can help the biological systems to improve normal functions and health (Sangiovanni et al., 2013; Nijveldt et al., 2001).
PLANT The grumixama is an evergreen tree with a dense treetop. The leaves are large, 69 cm in length, leathery and glossy. The flowers are white, axillary and solitary (Lorenzi et al., 2000) (Fig. 1). The tree can reach about 15 m high but already starts to produce fruits when it reaches 2 m. The fruits are small reaching about 2 cm diameter, with 13 seeds (Aguiar et al., 2015), but we have found up to 8 seeds per fruit. It has a thick, juicy and firm pulp with a sweet acidic flavor (Lorenzi et al., 2000). Three varieties of grumixama are recognized by Cambesse`des (183233) according to their fruit colors: α-variety, with purple fruits; β-variety, with red fruits; and γ-variety, with white fruits, being the last one described as yellow (Moreno et al., 2007). Morphologically, the yellow and the purple fruits are very similar and the most common varieties (Fig. 1).
CHEMICAL AND NUTRITIONAL COMPOSITION The chemical composition of purple and yellow grumixama fruits is described in Table 1. These fruits show similar chemical composition presenting about 2.6%3.5% of soluble sugars, mostly glucose in the ripe stage. The calculated energetic value found is about 30.6 Kcal/100 g. There are no data in the literature about minerals. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00028-9 © 2018 Elsevier Inc. All rights reserved.
219
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FIGURE 1 Grumixama fruits (A) purple or α-variety, (B) yellow or γ-variety and (C) flowers and leaves. Source: Bello’s farm (Cintia Bello).
TABLE 1 Chemical Composition of the Flesh of Eugenia brasiliensis Lam, Purple and Yellow Fruits Variety Yellow (g/100 g FW)
Purple (g/100 g FW)
85.21
83.6795.29
Total soluble sugar
2.97
2.613.53
Glucose
2.84
2.263.38
Frutose
0.12
0.110.13
Moisture
Sucrose Lipid
nd 0.22
0.02 0.0130.26
Protein
0.56
0.270.66
Total fiber
3.08
0.994.18
Total carbohydrates
6.05
4.207.60
Ash
0.56
0.230.61
15.67
14.2430.6
Energetic values (Kcal)
nd, not detected; FW, fresh weight. Adapted from Silva, N.A., Rodrigues, E., Mercadante, A.Z., Rosso, V.V., 2014. Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic forest. J. Agric. Food Chem 62, 5072 2 5084; Aguiar, T.M., Sabaa-Srur, A.U.O., Barbosa, N., 2015. Determinac¸a˜o fı´sica e quı´mica da polpa de grumixama (Eugenia brasiliensis, Lam). J. Fruits Veg., 1(1), 6770; Teixeira, L.L., Bertoldi, F.C., Lajolo, F.M., Hassimotto, N.M.A.J., 2015. Identification of ellagitannins and flavonoids from Eugenia brasilienses Lam. (Grumixama) by HPLC-ESI-MS/MS. Agric. Food Chem. 63(22), 54175427
PHYTOCHEMICAL PROFILE The yellow and purple grumixama have distinct chemotypes according to its terpenes profile (Table 2). The secondary metabolism of terpenes is upregulated on the sesquiterpene pathway in the purple variety, while the monoterpenes pathway is upregulated in the yellow variety (Moreno et al., 2007). According to that, the purple and yellow grumixama are characterized by sesquiterpenes (β-caryophyllene, caryophyllene oxide, τ-cadinol and β-bisabolene), and monoterpenes (α-pinene, β-pinene, Myrcene, and α-terpineol) (Table 2), respectively (Moreno et al., 2007). The main classes of phenolic compounds identified in purple and yellow grumixama varieties are flavonoids and ellagitannins (Table 3 and Fig. 2). While purple grumixama shows the higher amount of anthocyanin, mainly cyanidin 3-O-glucoside, responsible for the purple color, quercetin (flavonols) is the main flavonoid on the yellow fruit (Teixeira et al., 2015) (Table 3). The ellagitannin content of grumixama fruits varies from 7 to 14.88 mg/100 g of dry weight, expressed as total ellagic acid (Teixeira et al., 2015). Fig. 2 shows the main ellagitannins we have identified in both varieties (purple and yellow fruits). The main ellagitannins identified are the monomeric form of strictinin and castalagin/vescalagin in yellow and purple grumixama, respectively (Teixeira et al., 2015). Dimeric forms of ellagitannins such as Sanguinin H-6 and
Grumixama—Eugenia brasiliensis Lam
221
TABLE 2 Compounds Presents in Essential Oils of Edible Part of Purple and Yellow Grumixama, Identified by CG-MS Compounds
Varieties Yellow (%)a
Compounds
Purple (%)a
Varieties Yellow (%)a
Purple (%)a
0.9
0.2
α-muurolol
2.5
2.2
α-pinene
15.4
0.6
C15H22O (calemenenol)
1.5
0.8
β-pinene
9.3
0.2
Phenyl ethyl 2-acetate
nd
0.6
Limonene
4.4
0.7
β-elemene
nd
2.0
α-fenchene
0.2
nd
(E)-β-farnesene
nd
0.2
Myrcene
10.7
nd
allo-aromadendrene
nd
0.4
p-cymene
0.7
nd
γ-muurolene
nd
1.8
ethyl acetate
1,8-cineol
7.5
0.3
germacrene D
nd
0.5
(Z)-β-ocimene
0.3
nd
ar-curcumene
nd
0.3
(E)-β-ocimene
0.2
nd
β-selinene
nd
0.9
Terpinolene
0.8
nd
β-bisabolene
nd
9.6
Perilene
0.9
0.3
(Z)-calamenene
nd
2.4
exo-fenchol
0.4
nd
(E)-nerolidol
nd
1.6
(E)-sabinol
0.4
nd
Hidroxy-caryophyllene
nd
1.0
α-terpineol
10.2
0.5
Caryophyllene oxide
nd
22.2
α-copaene
1.1
1.6
epi-globulol
nd
1.7
β-caryophyllene
5.4
9.2
5-epi-7-epi-α-eudesmol
nd
1.7
α-humulene
1.4
2.1
Humulene oxide II
nd
1.5
Viridiflorene
0.5
1.7
1-epi-cubenol
nd
3.1
α-muurolene
0.4
1.4
γ-eudesmol
nd
0.6
δ-cadinene
4.3
nd
α-cadinol
nd
10.4
Spathulenol
4.4
nd
β-bisabolenol
nd
0.6
1,10-di-epi-cubenol
2.4
nd
Ethyl hexadecanoate
nd
0.6
iso-spathulenol
0.5
nd
τ-cadinol
3.2
9.9
Cubenol
1.0
nd
a Percentage calculated from the total area of the chromatogram; nd: not detected; GC-MS: Gas Chromatography coupled to Mass Spectrophotometry. Data from Moreno, P.R.H., Lima, M.E.L., Sobral, M., Young, M.C.M., Cordeiro, I., Apel, M.A., et al., 2007. Essential oil composition of fruit color varieties of Eugenia brasiliensis Lam. Sci. Agric. (Piracicaba, Braz.), 64 (4), 428432.
Sanguinin H-10, commonly found in berries (Silva et al., 2014), and oligomeric forms as melasquanin A, common in species of Myrtaceae (Gonzalez-Barrio et al., 2011), have not been detected in grumixama fruits (Teixeira et al., 2015). The other compounds, besides the ellagitannins, are mostly phenolic compounds, such as flavonoids, free ellagic acid, and ellagic acid derivates (Fig. 2). Also, another important class of phytochemical detected in grumixama fruit is the carotenoids, mainly mono hydroxy carotenoids (Table 4). The major carotenoid in purple grumixama is all-trans-β-cyptoxanthin, followed by all-trans-lutein and all-trans-β-carotene (Silva et al., 2014). There is no data about the carotenoids in yellow grumixama. The bioactive compounds as flavonoids, ellagitannins, and carotenoids have been investigated as possible agents to reduce the incidence of chronical diseases, such as tumoral disorders, cardiovascular diseases, type II diabetes and other chronic inflammatory disorders. The carotenoids can also improve immune enhancement and prevent macular degeneration (Sangiovanni et al., 2013; Nijveldt et al., 2001; Rodriguez-Amaya, 2010; Crozier et al., 2009; Del Rio et al., 2013).
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TABLE 3 Phenolic Compounds Detected in Yellow and Purple Grumixama Fruits by LC-ESI-MS/MS Phenolic compounds
Variety Yellow (mg/g DW)
Purple (mg/g DW)
Quercetin aglycone
1.78
0.662.17
Quercetin-3-glucoside
0.95
0.300.62
Myricetin aglycone
0.25
0.06
Catechin
0.19
nd
Epicatechin
0.18
nd
Delphinidin-3-glucosidea
nd
0.191.05
Cyanidin-3-galactoside
nd
Tr
Cyanidin 3-glucoside
nd
2.3210.04
Cyanidin-3-xyloside/arabinoside
nd
Tr
Cyanidin aglycone
nd
0.061.19
0.89
0.320.91
Flavonol
Flavanol
Anthocyanins
Phenolic acid Free ellagic acid
DW: dry weight; nd: not detected. Tr: traces. a Quantified as delphinidin aglycone Source: Adapted from: Teixeira, L.L., Bertoldi, F.C., Lajolo, F.M., Hassimotto, N.M.A.J., 2015. Identification of ellagitannins and flavonoids from Eugenia brasilienses Lam. (Grumixama) by HPLC-ESI-MS/MS. Agric. Food Chem. 63(22), 54175427.
FIGURE 2 Ellagitannins identified in purple and yellow grumixama fruits by LC-ESI-MS/MS. Percentage calculated from the total area of the chromatogram. Source: Adapted from Teixeira, L.L., Bertoldi, F.C., Lajolo, F.M., Hassimotto, N.M.A.J., 2015. Identification of ellagitannins and flavonoids from Eugenia brasilienses Lam. (Grumixama) by HPLC-ESI-MS/MS. Agric. Food Chem. 63(22), 54175427.
Extracts of yellow and purple grumixama demonstrated high antioxidant capacity and the purple fruit showed antiinflammatory action in cell models. Also, leaves of grumixama are used by folk medicine for the treatment of various diseases such as arthritis, diabetes, and rheumatitis (Colla et al., 2012).
HARVEST SEASON AND PRODUCTION: PURPLE GRUMIXAMA In Brazil, the commercial production can be found mainly in the region of ‘Vale do Paraı´ba’ in Sa˜o Paulo State, but it is spread in the southeast and south of Brazil (Okuda et al., 1982). Furthermore, grumixama is used to afforestation and for environmental reforestation of public squares and public gardens or in-house gardens (Suguino et al., 2011; Schaffer, 2013; Lorenzi et al., 2000). The flower bloom begins in November and the harvest season is between November and February (Suguino et al., 2011). As non-climacteric fruits, it must be harvest ripened. There are no data about the total annual commercial production.
Grumixama—Eugenia brasiliensis Lam
223
TABLE 4 Concentration of Carotenoids Detected in the Edible Part of Purple Grumixama by LC-ESI-MS/MS Content (mg/g DW)a
Compounds 9-cis-neoxanthin
1.60
All-trans-neochrome
0.35
All-trans-lutein
6.03
5,6-epoxy-β-cryptoxanthin
1.48
cis-lutein
0.02
5,8-epoxyi-β-cryptoxanthin
1.01
15-cis-β-cryptoxanthin
1.57 0
2.91
0
13-cis-β-cryptoxanthin/13 -cis-β-cryptoxanthinc
1.03
All-trans-zeinoxanthin
0.80
13-cis-β-cryptoxanthin/13 -cis-β-cryptoxanthinc
All-trans-β-cryptoxanthin
31.16
0
0.77
0
9-cis-β-cryptoxanthin/9 -cis-β-cryptoxanthin
0.67
All-trans-α-carotene
0.46
All-trans-β-carotene
3.38
9-cis-β-carotene
0.58
9-cis-β-cryptoxanthin/9 -cis-β-cryptoxanthin
a
Peaks quantified as equivalent to all-trans-β-cryptoxanthin; DW: dry weight. Source: Adapted from Silva, N.A., Rodrigues, E., Mercadante, A.Z., Rosso, V.V., 2014. Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic forest. J. Agric. Food Chem 62, 5072 2 5084
POTENTIAL INDUSTRIAL APPLICATION The grumixama has not been used in industrial application but is restricted to artisanal goods. However, the peel of purple grumixama and jambola˜o (Syzygium cumini (L.) Skeels) have been used as raw material to extract natural dye for the food industry by Embrapa (Santiago et al., 2016). Grumixama fruits are commercially available as frozen fruit or commercial frozen pulp and jelly. The bioactivity attribute to this fruit can be a factor to support the increase in commercial production as juice, commercial pulp and other derivates. However, more studies in cell models, animals, and human must be developed to support their functionality.
ACKNOWLEDGMENT We thank Bello’s farm for providing the photographs and CNPq (scholarship 153453/2012-5) and Fapesp (2013/07914-8) for financial support.
REFERENCES Abe, L.T., Lajolo, F.M., Genovese, M.I., 2012. Potential dietary sources of ellagic acid and other antioxidants among fruits consumed in Brazil: Jabuticaba (Myrciaria jaboticaba (Vell.) Berg). J. Sci. Food Agric. 92, 16791687. Aguiar, T.M., Sabaa-Srur, A.U.O., Barbosa, N., 2015. Determinac¸a˜o fı´sica e quı´mica da polpa de grumixama (Eugenia brasiliensis, Lam). J. Fruits Veg. 1 (1), 6770. Colla, A.R.S., Machado, D.G., Bettio, L.E.B., Colla, G., Magina, M.D.A., Brighente, I.M.C., et al., 2012. Involvement of monoaminergic systems in the antidepressant-like effect of Eugenia brasiliensis Lam. (Myrtaceae) in the tail suspension test in mice. J. Ethnopharmacol. 143, 720731. Crozier, A., Jaganath, I.B., Clifford, M.N., 2009. Dietary phenolics: chemistry, bioavailability and effects on health. Nat. Prod. Rep. 26, 10011043. Del Rio, D., Rodriguez-Mateos, A., Spencer, J.P.E., Tognolini, M., Borges, G., Crozier, A., 2013. Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid. Redox Signal. 18 (14), 18181892.
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Flores, G., Dastmalchi, K., Paulino, S., Whalen, K., Dabo, A.J., Reynertson, K.A., et al., 2012. Anthocyanins from Eugenia brasiliensis edible fruits as potential therapeutics for COPD treatment. Food Chem. 134, 12561262. Fracassetti, D., Costa, C., Moulay, L., Toma´s-Barbera´n, F.A., 2013. Ellagic acid derivatives, ellagitannins, proanthocyanidins and other phenolics, vitamin C and antioxidant capacity of two powder products from camu-camu fruit (Myrciaria dubia). Food Chem. 139, 578588. Gonzalez-Barrio, R., Edwards, C.A., Crozier, A., 2011. Colonic Catabolism of Ellagitannins, Ellagic Acid, and Raspberry Anthocyanins: In Vivo and In Vitro Studies. Drug Metab. Disposition. 39 (9), 16801688. ´ rvores Brasileiras, Manual de Identificac¸a˜o e Cultivo de Plantas Arboo´reas Nativas do Brasil. Lorenzi, H., Bacher, L., Lacerda, M., Sartori, S., 2000. A Instituto Plantarum de Estudos da Flora, Nova Odessa SP. Moreno, P.R.H., Lima, M.E.L., Sobral, M., Young, M.C.M., Cordeiro, I., Apel, M.A., et al., 2007. Essential oil composition of fruit color varieties of Eugenia brasiliensis Lam. Sci. Agric. (Piracicaba, Braz.). 64 (4), 428432. Nijveldt, R.J., Nood, E.V., Hoorn, D.E.C.V., Boelens, P.G., Norren, K.V., Leeuwen, P.A.M.V., 2001. Flavonoids: a review of probable mechanisms of action and potential applications. Am. J. Clin. Nutr. 74, 418425. Okuda, T., Yoshida, T., Hatano, T., Yazaki, K., Ashida, M., 1982. Ellagitannins of the Casuarinaceae, Stachyuraceae and Myrtaceae. Phytochemistry. 21, 28712874. Reynertson, K.A., Yang, H., Jiang, B., Basile, M.J., Kennelly, E.J., 2008. Quantitative analysis of antiradical phenolic constituents from fourteen edible Myrtaceae fruits. Food Chem. 109, 883890. Rodriguez-Amaya, D.B., 2010. Quantitative analysis, in vitro assessment of bioavailability and antioxidant activity of food carotenoids—a review. J Food Compos. Anal. 23, 726740. Sangiovanni, E., Vrhovsek, U., Rossoni, G., Colombo, E., Brunelli, C., Brembati, L., et al., 2013. Ellagitannins from Rubus berries for the control of gastric inflammation: in vitro and in vivo studies. PLoS One. 8, 7176271774. Santiago, M.C.P.A., Gouveˆa, A.C.M.S., Peixoto, F.M., Borguini, R.G., Godoy, R.L.O., Pacheco, S., et al., 2016. Characterization of jamela˜o (Syzygium cumini (L.) Skeels) fruit peel powder for use as natural colorant. Fruits. 71 (1), 38. Schaffer, C.C. 2013. Grumixama, a surpresa de natal da mata atlaˆntica. Apremavi - Associac¸a˜o de Preservac¸a˜o do Meio Ambiente e da Vida. Available at: ,http://www.apremavi.org.br/grumixama-a-surpresa-de-natal-da-mata-atlantica/.. Silva, N.A., Rodrigues, E., Mercadante, A.Z., Rosso, V.V., 2014. Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic Forest. J. Agric. Food Chem. 62, 50725084. Suguino, E., Martins, A.N., Minami, K., Narita, N., Perdona, J., 2011. Efeito da porosidade do substrato casca de pinus no desenvolvimento de mudas de grumixama. Rev. Bras. Frutic.643648, Jaboticabal - SP, special vol. Teixeira, L.L., Bertoldi, F.C., Lajolo, F.M., Hassimotto, N.M.A.J., 2015. Identification of Ellagitannins and Flavonoids from Eugenia brasilienses Lam. (Grumixama) by HPLC-ESI-MS/MS. Agric. Food Chem. 63 (22), 54175427.
FURTHER READING Yoshida, T., Amakura, Y., Yoshimura, M., 2010. Structural features and biological properties of ellagitannins in some plant families of the order myrtales. Int. J. Mol. Sci. 11, 79106.
Guarana—Paullinia cupana Kunth var. sorbilis (Mart.) Ducke Andre´ Luiz Atroch and Firmino J. do Nascimento Filho Embrapa Western Amazon, Manaus, Brazil
Chapter Outline Introduction Cultivar Origin and Botanical Aspects Flowering, Pollination, and Harvest Season Estimated Annual Production The Guarana and Polyploidy Genetic Resources Genetic Variability Brief History of Guarana Genetic Improvement Objectives of Guarana Breeding
225 225 227 228 229 229 230 233 233
Genetic Improvement Methods Mass Selection Plant Selection With Progeny Testing Clonal Selection Recurrent Intraspecific Selection Transcriptome of Fruit With Seeds Future Prospects References Further Reading
233 233 234 234 234 235 235 235 236
INTRODUCTION Guarana (Paullinia cupana Kunth var. sorbilis (Mart.) Ducke, Sapindaceae) is a native Brazilian species of considerable economic and social importance; it is a rainforest perennial climbing shrub that was domesticated in the Amazon due its caffeine-rich seeds. Brazil is the only producer of guarana in the world, satisfying both domestic and international demand. Over the last few decades, the area planted with guarana has expanded beyond Amazonia and guarana now planted in the states of Amazonas, Acre, Para´, Rondoˆnia, Bahia, and Mato Grosso. The guarana breeding program coordinate by Embrapa Western Amazon (Embrapa’s Western Amazonia unit) began in 1976 and after almost 39 years of very successful research, released 19 clonal cultivars between 1999 and 2015. The objective of this chapter is to summarize current knowledge and advances on the guarana breeding program.
CULTIVAR ORIGIN AND BOTANICAL ASPECTS Father Betendorf first reported guarana plant in 1669 on a trip up the Amazon River. He was a high-ranking Jesuit of the Company of Jesus in the state of Maranha˜o, Brazil, and discovered that the Andira Indians (more correctly known as the Satere´ Maue´) were using the guarana plant. Betendorf does not mention guarana in connection with any other local ethnic groups. When the first European naturalists explored Amazonia in the 19th century, they noted that the Satere´ Maue´ were the original cultivators of guarana and at that time, it was attracting the attention of colonists throughout the region (Monteiro, 1965). The Satere´ Maue´ is an ethnic group speaking a branch of Tupi, the most important indigenous language group in Brazil. In the mythology of the Satere´ Maue´, guarana is an essential, if not primordial, element of their society, as it is directly associated with the actual origin of the Satere´ Maue´. The meaning of this story has recently become clearer. The variety Sorbilis cultivated by the Satere´ Maue´ is polyploid with 210 chromosomes, whereas the other species in this genus have 24 (Freitas et al., 2007). In essence, the story reports on the domestication of the guarana, which occurred when a primordial Tupi woman recognized that she had Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00029-0 © 2018 Elsevier Inc. All rights reserved.
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discovered a special type of guarana, a type different from the more common and less useful false guarana, and that this type should be planted to benefit future generations. Note that the Satere´ Maue´ also became a distinct ethnic group at that time, different from the other Tupi groups in Central Amazonia. This recently interpreted myth raises a number of obvious questions: is the myth specific to the Satere´ Maue´ people or do other local ethnic groups share it? Did the Satere´ Maue´ live in a region formerly known as Mundurucaˆnia, a geographic area the size of Switzerland, delimited by the Amazon River to the north, the Tapajo´s River to the east, the Madeira River to the west and the Juruena River to the south (Monteiro, 1965)? Many other indigenous groups used to live in Mundurucaˆnia, including the important and once very numerous Munduruku, to the south of the Satere´ Maue´, but none of them has a myth similar to that of the Satere´ Maue´, although other groups use guarana. The first European naturalists documented little on the other indigenous groups in relation to guarana. When these naturalists appeared, the Satere´ Maue´ lived on the Maue´s and Andira´ rivers, in what is now the municipality of Maue´s, and they still live in this region. Based on this information, we can affirm that guarana originated in this relatively restricted geographic region. The Satere´ Maue´ probably arrived in the Maue´s and Andira´ Rivers region between 1000 and 2000 years ago, giving some idea of earliest time at which the domestication event in the myth occurred. It is worth bearing in mind that the other Tupi-speaking groups in Mundurucaˆnia did not attribute such importance to the guarana as the Satere´ Maue´ do, it seems likely that the domestication event occurred after the arrival of the Satere´ Maue´, perhaps much later, as the region already contained gardens with Brazil nut trees. New evidence in support of a later domestication event is seen in the lack of molecular genetic structure observed using RAPD markers (random amplified polymorphic DNA) in the Sorbilis variety (Sousa, 2003). Based on this analysis of the myth, it is also possible to analyze a few ideas concerning the origin of the guarana from the previous century. Lleras (1992) suggested that the geographic isolation between P. cupana in Venezuela and var. Sorbilis could be due to human intervention, i.e., the Indians of Central Amazonia could have taken the guarana to the upper Rio Negro and Orinoco. Lleras also suggests that it was the Bare´ Indians, speaking Arawak, who were responsible for dispersal. Although the Bare´ were still present from the lower to upper Rio Negro at the time of European conquest, there are no reports of guarana in the lower Rio Negro until the 20th century. If the Bare´ had taken guarana upriver, there must have been guarana populations along the river instead of the disjunct distribution that we see today. It is possible that these populations existed but died off. However, the spontaneous existence of P. cupana is reported on the upper Rio Negro (Nascimento Filho et al., 2001a), suggesting that it is capable of adapting to nonanthropic environments. Polyploid plants have a high morphological and ecological segregating ability, which could explain their spontaneous appearance, even though this Maue´s region has not been observed, nor along the Rio Negro. However, these arguments are lacking evidence in support of geographic isolation, which remains a mystery. In the first revision relating to guarana, Ducke (1937) suggested that guarana cultivation originated on the upper Rio Negro and upper Orinoco and went brought to the Maue´s region. Obviously, this contradicts Lleras’ theory, but both are relevant. The guarana (Paullinia cupana Kunth var. sorbilis (Mart.) Ducke) is a dicotyledon belonging to the family Sapindaceae, which contains around 130 recognized genera (Tro´picos, 2008), according to recent taxonomic revisions. Although the circumscription of this botanical family is subject to dispute, at least three subfamilies are recognized, with the guarana tree included in the subfamily Sapindoideae (Tro´picos, 2008). Within this subfamily, Harrington et al. (2005) recommend keeping the genus Paullinia in the Paullinieae tribe originally defined by Radlkofer in 1933. The tribe also includes the genera Serjania and Cardiospermum, which form a monophyletic clade based on the analysis of two DNA sequences (Fig. 2). These three genera include scandent plants, which exhibit tendrils and stipules. However, the authors also suggested that the Thouinieae tribe could absorb the Paullinieae tribe. The distribution of genus Paullinia is throughout tropical and subtropical America with a single species, P. pinnata, in tropical Africa. Radlkofer (1931) recognized 147 species in the genus Paullinia, organized into 13 sections. The classification of the species of Paullinia cupana was in the section Pleurotoechus, which has 28 species distributed from Mexico to the state of Rio de Janeiro, in Brazil, with nine species occurring in Brazilian Amazonia. At present, 195 species are acknowledged in the genus Paullinia (Tropicos, 2008) and at least four of the divisions of Radlkofer, including Pleurotoechus, are still list on the International Plant Names Index website (IPNI, 2008). In 1810, Humboldt and Bonpland were the first European naturalists to observe the guarana on a trip to southern Venezuela. This material was first described and classified by Kunth as Paullinia cupana and is known to have originated in the area to the south of the Atures and Maipures falls on the Orinoco river, and in the upper regions of the Rio Negro and its tributaries, on the borders of Brazil, Venezuela, and Colombia. Twenty years later, on a trip along the Amazon River, Martius collected botanical material that he classified as Paullinia sorbilis. The guarana tree was already cultivated and subspontaneous in the Maue´s region (and rarely in Parintins). It was also cultivated near the city
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FIGURE 1 Guarana fruits (Paullinia cupana var. sorbilis) at harvesting point.
of Manaus (Ducke, 1938). Given the similarity between the two plants, sorbilis and cupana went considered synonyms in 1897, on publication of the “Flora Brasiliensis de Martius”, and cupana went kept as the earlier term (Ducke, 1937; von Martius, 2008). Ducke (1938) noticed that the morphological differences were sufficient to differentiate the plants in the populations found by Humboldt and Bonpland and by Martius, and completed the description of the Maue´s guarana drafted by Martius, treating it as a variety, with the name Paullinia cupana Kunth var. sorbilis (Mart.) Ducke (IPNI, 2008). To differentiate the guarana observed by Humboldt and Bonpland and described by Kunth, Ducke created the typical form (species type). Based on the current rules of taxonomic nomenclature, this kind of distinction is unnecessary, because the name Paullinia cupana is the most appropriate. The name P. cupana var. cupana can still be found in the literature for P. cupana typical form, but should be discarded. According to Ducke (1938), the P. cupana observed by Humboldt and Bonpland had heavily serrate-lobate leaves in early development and no tendrils at any age. The flowers and fruits were larger than those of the variety sorbilis, and the fruits were markedly oval and pear-shaped, of a fairly dark red color and not particularly glossy. The plants of var. sorbilis have less deeply lobate leaflets when young and tendrils when adult. The flowers of var. sorbilis are slightly smaller, and it produces only half to one third as many fruits and they are bright red and glossy. The inflorescence is a variable-sized cluster, which can be larger than 25 cm, and generally sprouts at the axilla or at the base of a tendril. The flowers are arrange along the main axis of the inflorescence, organized in fascicules of three to seven flowers, and are functionally unisexual. The female flowers have rudimentary stamens, with indehiscent anthers and three carpels, with trifid stigmas. The male flowers have atrophied ovaries with underdeveloped ovules, styles, and stigmas. There are eight stamens, with filaments of three different sizes and long hairs, but the anthers are hairless. The pollen grains are triangular. The calyx consists of five sepals, two of which are smaller and external, whereas the other three are narrower and similar to the petals (Souza et al., 1996). The fruit is a dehiscent capsule and, when mature, its color ranges from orangish-yellow, through yellowish-red to vibrant bright red (Fig. 1). When it splits, the dark brown seed partially wrapped in a white aril is visible (Souza et al., 1996). The majority of seeds are round, but this can vary if the capsules are obovate or oblate, with one, two, three or more seeds. Fruits with one, two or three fertilized ovules are common. In Bahia, the ratio of male to female flowers observed was 5.4:1 (Pereira and Sacramento, 1987). Each plant can produce up to 400 inflorescences and around 38 000 flowers (Escobar et al., 1985).
FLOWERING, POLLINATION, AND HARVEST SEASON Although male and female flowers are present in the same inflorescence, male and female flowering are not synchronized (Gondim, 1978). Pereira and Sacramento (1987) in Bahia also observed this. Apparently, the longer the inflorescence period, the greater the likelihood of more than one female flowering period. This is why fruits and flowers at different stages of maturation went found, which could mean that more than one harvest is necessary.
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These characteristics, already well-studied in populations obtained by open pollination, need to be analyzed in depth for clonal cultivars, as the results could be used to define good clone combination, and produce progenies and multiclone commercial crops. Angelo et al. (2007) found differences in the flowering patterns of three clones of guarana and confirmed that simultaneous anthesis of male and female flowers in the same inflorescence was rare, corroborating the studies cited. Gondim (1978) collected 32 species of insects from five different orders on guarana. The Hymenoptera account for 71% of the individuals, with 27 species of bee visiting the flowers. The author suggests that the general pollination syndrome of the guarana tree is adapted to the Hymenoptera and that the species Melipona seminigra, Xylocopa muscaria, and Apis mellifera are among the most important pollinators, the others being only occasional. Artificial pollination went developed to support controlled crossing programs. The technique consists of three stages: G
G
G
Isolating the inflorescences—carried out close to floral anthesis, using semitransparent paper bags and taking care to avoid contamination by foreign pollen and damage by insects; Pollination—carried out by repeatedly brushing the anthers with the selected pollen over the receptive stigmas, while maintaining the isolation; and Identification—labeling with the name of the parent plants and the pollination date.
Knowledge of the species’ reproductive system is fundamental for choosing the most appropriate breeding methods. The species has morphological mechanisms favoring cross-fertilization. Due to the flowering and pollination, the harvest of guarana´ fruits is very unequal with many harvests per year on the same plant. The harvest season of guarana fruits is between October and December each year.
ESTIMATED ANNUAL PRODUCTION In the state of Amazonas, both small and large producers plant guarana. Large corporate groups own plantations varying from 80 to 500 ha (Atroch, 2001, 2002). In contrast, Maue´s (state of Amazonas) has some 1600 family farmers of guarana, with an average area of 3 hectares, and they are responsible for 35% of the planted area and 35% of the state’s production. The Satere´ Maue´ Amerindians who domesticated the guarana in the Maue´s region are expanding organic production with a view to certification for the European market. In general, the guarana farmer in Amazonas is a landowner, with relatively easy access to agricultural credit for improved production planning and guaranteed minimum prices. Brazil has about 15 000 ha with guarana crop. The harvested area is about 13 000 ha, with production of 3600 metric tons of dry seed and productivity of 278 kg/ha. The State of Bahia is the largest guarana producer in Brazil (47% of domestic production) followed by Amazonas (39%), Mato Grosso (10%), Acre (2%), Rondoˆnia (1%), and Para´ (1%). The cash value of domestic production in 2013 was R$32.5 million (IBGE, 2015). Fig. 2 shows Brazil guarana yield between 1990 and 2013. The tendency curve is to increase the yield along the time. Currently, most of the guarana produced in Brazil is consumed in the domestic market, but the amount exported, mainly as concentrated dry extract and guarana powder, is increasing annually. Estimates put the supply of domestic guarana seeds used by soft drinks manufacturers at around 70%, with the remaining 30% marketed as syrup, sticks, FIGURE 2 Brazil guarana yield between 1990 and 2013 years.
Brazil-Guarana Yield 6000
Yield (tons)
5000 4000 3000 2000 1000 0 1990
1995
2000
2005 Year
2010
2015
Guarana—Paullinia cupana Kunth var. sorbilis (Mart.) Ducke
229
powder, and extract consumed both internally and in the export market (Atroch, 2001, 2002). Fluctuations in prices paid to producers as well as difficulties in harvesting and storing the product are the main obstacles to commercializing guarana (Atroch, 2001, 2002), but generally speaking, there are no major problems, especially in regard to the soft drinks industry. Guarana production in Amazonas amounts to 664 metric tons, worth some R$12.4 million. Maue´s is the main producer, with output of 300 metric tons of guarana seeds and annual income of R$5.4 million (IBGE, 2015), as the price paid for the product in this region is higher. Guarana from Maue´s attracts a good price on the domestic market and especially in Europe, because it is considered ‘stronger’ than the guarana produced in other regions, even in Amazonas. This is in part due to the Satere´ Maue´ Amerindians, who not only own the rights to the Amazonia brand but can also take advantage the indigenous product and fair trade markets. They are also seeking organic certification. The municipality of Maue´s was the biggest producer of guarana in Brazil for most of the 20th century. However, phytosanitary problems and the aging plantations resulted in a gradual decline in production, year on year, until it lost its leading status to Bahia in the 1980s. Today, guarana production in Amazonas shows signs of recovery as a result of the availability of genetic materials bred by Embrapa and being distributed to guarana producers in the main producing regions of Amazonas, mainly Maue´s. The demand for other product differentials is also boosting the market, and a large national corporation intends to launch a new guarana soft drink in the global market.
THE GUARANA AND POLYPLOIDY Knowledge of genomic structure and organization is becoming increasingly important for understanding the evolution and manipulation of genes of agronomic interest. The vast majority of authors familiar with cytogenetic studies admit that this knowledge is extremely important for understanding kinship and the genetic mechanisms involved in evolution, both within lower taxa (species and genera) and at higher levels (families and divisions) (Guerra, 1986; Soltis and Soltis, 2004). The sorbilis variety has 2n 5 210 chromosomes and average DNA content for a diploid nucleus of 22.8 pg (Freitas et al., 2007). These results confirmed preliminary counts (Nascimento Filho et al., 2007). In the genus Paullinia, seven species were subjected to karyotype characterization and they were all 2n 5 24 (Solı´s Neffa and Ferrucci, 2001). In the Paullinieae tribe, the basic numbers found were x 5 7, 10, 11, 12, and 14 (Ferrucci and Solı´s Neffa, 1997). These data mean that, because of the number and types of chromosomes, we can consider the guarana karyotype to be of complex origin, including polyploidization and numeric rearrangement (Freitas et al., 2007). Within the family, Ferrucci and Solı´s Neffa (1997) cite at least two more genera that occur in South America that are polyploid, sometimes followed by aneuploid reduction: Allophylus (A. pauciflorus has 2n 5 28 and A. guaraniticus has 2n 5 56) and Urvillea (U. chacoe¨nsis has 2n 5 22, U. uniloba has 2n 5 44 and U. ulmacea has 2n 5 22 and 2n 5 86). Allophylus occupies a clade close to Paullinia, Serjania, and Cardiospermum in the analysis of Harrington et al. (2005). As there are no other known polyploids in the genus Paullinia and the event described in the origin myth mentions only one false guarana, and also in view of the complexity of the karyotype, it is plausible that the guarana tree is an auto-allopolyploid, derived from the combination of at least two species, which may be from different genera. Karyotype analysis of other species of Paullinia, especially those that could have contributed to the origin of the sorbilis variety, as well as the P. cupana observed by Humboldt and Bonpland, will be important in helping us understand the evolutionary origin of the cultivated guarana, and in facilitating other types of genetic-molecular analysis to back up the breeding program. These common differences in polyploid plants could explain the categorical differences between P. cupana and other species, such as the false guarana found near the villages of the Satere´ Maue´ and still not identified (Fig. 3). Concerning the biometric approach used in the improvement of guarana, it is important to know the type of ploidy. If the guarana is an allopolyploid, the biometric approach should be similar to that used with diploids. If it is an autopolyploid, other genetic models should be used. In this case, it is not possible to estimate additive genetic variance and individual narrow-sense heritability based only on the evaluation of half-sibling progenies or parents and offspring (Resende, 2002). This is because these kinship relations for autotetraploids also include fractions of dominance variance and not just additive variance.
GENETIC RESOURCES Embrapa Western Amazon is the institution responsible for guarana genetic resource conservation in Brazil. It has a clonal germplasm bank with 270 guarana accessions. The collection is maintained on the Embrapa Western Amazon
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FIGURE 3 False guarana (not identified) found on Andira´-Marau Indigenous Land, near the village of the Satere´ Maue´, in Maue´s, Amazonas, Brazil. 2008. Source: Credit: Gina Frausin.
experimental site at 29 km off the AM-010 ManausItacoatiara highway, latitude 02 520 South and longitude 59 590 West, in the municipality of Manaus (Nascimento Filho et al., 2001a). All the germplasm cultivated commercially in Brazil originates from Maue´s, in the state of Amazonas, and the germplasm used initially in genetic breeding programs was collected from a small number of commercial populations at locations near the cities of Maue´s and Manaus. Bearing in mind that the guarana from Manaus also originated in Maue´s, the genetic base is obviously very narrow (Nascimento Filho et al., 2001a; Sousa, 2003). Older germplasm collected in 1950 at the Maue´s Experimental Site relates to the traditional crop within the perimeter of the experimental site. Collections that are more recent were in 1986 and 1987 (Table 1). It is worth noting that there is no P. cupana from Venezuela in the Embrapa germplasm bank. Ducke collected this material in 1937 at a location called Marabitanas on the upper Rio Negro, 18 km south of Cucuı´, and planted at the Northern Agronomic Institute (IAN). In the 1950s, it was collected again and planted at the IAN and the National Research Institute for Amazonia (INPA) (William Rodrigues, personal communication to Clement, 2008). In the years of turbulence between the IAN and the IPEAN (Northern Farming Research and Experimentation Institute), and the creation of Embrapa in 1973, this material disappeared in Bele´m. The material planted at INPA also vanished. In 1981, researchers at Embrapa Amazoˆnia Oriental returned to the location and observed that all the material had been eradicated. With no material on hand, we still do not know whether the Venezuelan P. cupana is polyploid, like var. sorbilis.
GENETIC VARIABILITY The guarana tree exhibits wide phenotypic variability for all the traits analyzed to date, but there is little genetic variability. This paradoxical situation is due to its recent domestication as a polyploid. However, there is sufficient genetic variability in populations for a number of traits to allow selection of superior individuals with a greater number of desirable characteristics for use directly by producers or in breeding programs (Nascimento Filho et al., 2001a). This affirmation is based on 30 years of study, during which the guarana has been characterized and evaluated for both morphometric variability and molecular genetic variability. This period also saw the distribution of cultivars produced by the breeding program. The variability of various traits has been studied in cultivated germplasm, both in traditional producer areas and at experimental sites. The variability of qualitative and quantitative traits was evaluated by Correˆa (1989) in open pollinated progenies as well as clones, resulting in a proposed minimum descriptor list for guarana morphological characterization. This list incorporates morpho-anatomical observations of the leaf (width, length, shape and leaflet-3 size; stomatic density and leaf hair density), carpological observations (rachis length, cluster insertion on the branch, cluster weight, number of fruits per cluster, fruit shape, fruit color, pericarp surface, skin fresh and dry weight, seed fresh and dry weight) and chemical observations (dry seed caffeine content). The disease resistance index is also very variable (Pereira et al., 2007a, b).
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TABLE 1 Number of Guarana Genetic Resource Plants Collected Over a Period of 50 Years and Currently Available to the Embrapa Western Amazon Guarana Breeding Program Year of collection
Collection location
Planting location
Number of plants
Comments
1950
Maue´s
Embrapa experimental site in Manaus
6116
Plants from around Maue´s, Apoquitaua river and from a traditional crop within the perimeter of the Embrapa experimental site
197278
Cacau Pirera (Iranduba)
Embrapa experimental site in Manaus
819
Plants of unknown origin
19681970
Maue´s
Embrapa experimental site in Maue´s
2554
Plants from around Maue´s
1977
Maue´s
Embrapa experimental site in Maue´s
2112
Plants from the Apoquitaua river that originated most of the breeding program clones
197679
Maue´s
Embrapa experimental site in Maue´s
1943
Plants from the Embrapa Experimental Site in Maue´s
1978
Maue´s
Embrapa CPATU in Bele´m
201
Progenies planted at Embrapa Amazonia Oriental, in Bele´m, Para´
198687
Maue´s
Embrapa experimental site in Maue´s
241
Collection program aimed at introducing 1000 genotypes in five years
198687
Manaus
Embrapa experimental site in Manaus
23
Collection program aimed at introducing 1000 genotypes in five years
198687
Cacau Pirera (Iranduba)
Embrapa experimental site in Manaus
21
Collection program aimed at introducing 1000 genotypes in five years
199598a
Manaus and Maue´s
Embrapa experimental site in Manaus
270
Deployment of the Active Germplasm Bank of Embrapa Amazonia Ocidental
a
Current Active Germplasm Bank held by Embrapa Western Amazon, based on the other collections held.
On discovering the guarana’s polyploidy (Freitas et al., 2007), some of this variability could be attributed to epistasis among the numerous genes coding for different morphological traits (Stebbins, 1985). Polyploids are subject to phenotypic, physiological and chemical changes, which could explain the morphometric variability observed in guarana. Genetic changes are based on alterations in the arrangement of DNA sequences, resulting in permanent changes in the molecule or gene loss. Possible alterations in the sequence or in the chromosomes include unequal crossing-over, recombination of homoeologs, aneuploids, gene conversion, insertions, deletions and punctual mutations. Epigenetic changes, such a DNA methylation, histone modification, interference RNA and dosage compensation, can alter the gene expression pattern, without changing the DNA sequence and produce dramatic phenotypic effects within the species. At present, the priority evaluations for the guarana germplasm collection and clone competition experiments focus on disease resistance and traits related to the plant’s two developmental phases. The vegetative phase encompasses traits associated with initial plant vigor during the first twelve months after planting, and the productive phase extends to traits related to flowering, fruiting and production (Nascimento Filho et al., 2001). The descriptors are: 1. Vegetative phase: survival rate, main branch length, number of leaves, number of branches, leaf area, petiole length and leaflet-3 width and length. 2. Productive phase: production per plant (fruit 1 rachis), seed dry weight, incidence of diseases and caffeine content. Valois et al. (1979) observed that the plant’s reproduction method and the ratio of female to male flowers in an inflorescence could be responsible for the low correlation between inflorescence size, number of buds, number of fruits, and number of seeds per fruit. They also verified that these factors are genetically variable: for example, inflorescence
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size (CV 5 30.6%), number of buds (CV 5 24.9%), and number of seeds (CV 5 27.9%), and can be significantly increased by selection. Dry seed production is the main trait of economic interest for guarana. Nascimento Filho et al. (1994) studied 26 characters related to the aerial part and root system of guarana plants, finding high variability for all traits among the clones studied. They obtained genotypic determination coefficients of over 70% for the majority of variables studied, showing that simple breeding methods could be applied to give good selection gains. With the aim of identifying productive, divergent guarana tree clones that could be used in a crossing program to obtain hybrids with high heterosis, as well as materials for vegetative propagation, Nascimento Filho et al. (2001) evaluated 148 guarana clones for length of the main branch, number of branches and leaves, and production of dry seed in kilograms per plant. The phenotypic variability analysis was significant for all traits evaluated. To analyze genetic divergence among groups of clones, they used average Euclidean distance, Toucher’s optimization method and the nearest neighbor method. Genetic distance estimates allowed seven separate groups to be formed, with the majority of clones (85%) in one group, which shows that genetic divergence among the clones currently used in the guarana genetic improvement program at Embrapa Western Amazon is not wide (Nascimento Filho et al., 2001). This set of results clearly shows the influence of recent domestication via polyploidy on the phenotypic and genetic variability of the guarana. Molecular markers have provided an important tool for helping researchers involved in plant genetic improvement programs. According to Ferreira and Grattapaglia (1996), the use of molecular markers in plant breeding programs can be subdivided into short-, medium- and long-term applications. In the short term, it is possible to identify and differentiate genotypes. In the medium and long term, markers can be used to quantify genetic variability in the DNA and correlate it with the phenotypic expression. This molecular information, integrated into genotype selection and recombination methods, can be used to achieve faster genetic advances in conventional breeding programs. Using RAPD molecular markers and traits related to fruit production, Sousa (2003) evaluated genetic parameters and divergence in guarana clones in the Active Germplasm Bank at Embrapa Western Amazon and 27 elite clones from the state network for guarana clonal evaluation and selection. Existing variation in the germplasm was efficiently identified by molecular and phenotypic evaluation, but with no association with collection locations, corroborating the results obtained by Nascimento Filho et al. (2001), working with phenotypic traits, once again confirming the recent origin of the guarana based on the polyploidization event. The high correlation (r 5 0.85**) between the similarities of RAPD and Mahalanobis generalized distances, taking only the average and extreme estimates, was used to predict that clones CIR217, CMA227, CMU300, and CMU611 were the most suitable for producing superior combinations in a crossing program. The high heritability of the total number of normal fruits per cluster trait (h2 5 0.67) and its positive phenotypic correlation with average cluster weight (r 5 0.47**) highlight the importance of these two traits as production components. The search for guarana genome regions that contain microsatellites, or SSRs (simple sequence repeats) and that would be useful for developing markers was begun in 2004, in a project coordinated by Embrapa Western Amazon, with the collaboration of the Federal University of Amazonas and INPA, and funded by FAPEAM (Amazonas State Research Support Foundation). This resulted in the enrichment of the Sau3AI and MseI genome libraries with probes (CA)12, (CT)12, and (TC)14. The bank of Expressed Sequence Tags (EST) for guarana fruits and seeds kept by REALGENE (see below) was also searched for repeat blocks using STADEN/TROLL applications (Martins et al., 2006). Individual sequences were examined and electropherograms taken (Angelo et al., 2007). The relative frequency of perfect blocks with a number of 8 or more was 0.77% (66/8597) in the EST bank and 0.29% (2/688) in the genome libraries, and there was no statistical difference (Angelo et al., 2007). In diversity analyses of eucalyptus, kiwi, coconut palm, olive and massaranduba, microsatellites were used with minimum numbers of 15, 8, 13, and 9, and the maximum number was always higher than 20 repeats in perfect arrangements and also in composite arrangements. Therefore, we can consider perfect blocks with more than eight repeats as rare in the guarana tree. This could be due to size of the guarana tree genome. Ten pairs of primers were tested for di-, trinucleotide and composite repeats. Five of these primer pairs (loci GRN02, 03, 10, 13, and 16) produced monomorphic patterns with up to three types of alleles per individual, even in genotyping conducted using morphologically divergent accessions (Nascimento Filho et al., 2001). This corroborates the low level of variability observed using RAPDs (Sousa, 2003) and could also be due to the short time interval assumed to have elapsed since polyploidization, insufficient to allow divergence between alleles. In the other five loci (GRN01, 04, 05, 07, and 08), polymorphism was observed and the number of types of alleles varied from one to five per individual. As we do not yet have sufficient information on the species that contributed to originating var. sorbilis to attempt to analyze the data, such as codominant traits, it will be necessary at least to have a methodology for quantifying the number of copies of each allele. We will also need to verify whether there is pairing and recombination among homologs and validate microsatellite loci by genotyping the progenies of controlled crossings.
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BRIEF HISTORY OF GUARANA GENETIC IMPROVEMENT Phenotypic selection of superior parents began in 1976 at the Maue´s Experimental Site, and initially 36 genitors were identified in a population originating from 3074 plants with an age range of 920 years grown by farmers. In 1984, a national network for evaluating open-pollinated progenies and clones was set up at Embrapa centers in northern Brazil and at CEPLAC/CEPEC in the state of Bahia. These experiments were conducted until 1994, but the objective of recommending materials was not achieved, because the majority of experiments were abandoned due to lack of funding. In 1996, Embrapa Western Amazon set up a state network for evaluating 32 promising clones in order to assess their behavior under varied environmental conditions in Amazonas. Between 1999 and 2000, Embrapa Western Amazon distributed the first 12 guarana clones for planting in Amazonas. At present, six clonal varieties and one open pollination variety exist with productive potential up to 10 times higher than the average for the state of Amazonas, and they are being distributed for planting.
OBJECTIVES OF GUARANA BREEDING The general objective of plant breeding is to identify and select superior genotypes in commercial production. The work therefore aims to obtain a so-called plant ideotype (Bueno et al., 2001). The objectives were set for the breeding program coordinated by Embrapa Western Amazon: to select guarana clones with a yield greater than 1.5 kg of seeds per plant, wide adaptability, good stability, tolerance to the main diseases (anthracnosis and supersprouting disease), with improved fruit quality (higher caffeine content), resistance to pre-harvest fruit drop and more uniform maturation (Nascimento Filho and Atroch, 2002). Seed productivity is the most important selection criterion. The minimum period for evaluating productivity is five years (Nascimento Filho, 2003; Atroch, 2004). Other variables help in deciding which are the best genotypes, such as main branch length, number of branches and number of leaves, indicating the plants’ ability to establish itself and survive after planting in the field (Nascimento Filho and Atroch, 2002). Adaptability and production stability are measured by average productivity of genotypes in a variety of environmental conditions, cropping systems, locations, as well as year-on-year variations (Nascimento Filho and Atroch, 2002). The plant is generally evaluated for anthracnosis twice a year, in the dry season (SeptemberOctober) and the rainy season (MarchMay), using a scale from 0 to 3. Zero indicates absence of the disease. Genotypes rated 2 and 3 are discarded during the selection process. For supersprouting disease, the percentage of infected branches is measured and the severity of the disease is also evaluated on a scale from 0 to 3 (Nascimento Filho and Atroch, 2002). One problem observed in guarana plantations is the significant lack of uniformity in the harvest. A plant is harvested ten to twenty times during the harvest period (October to December). However, using hormones to render the harvest uniform would not be economically viable, and would lead to market rejection, given the stringent requirements for chemical residues on crops. To overcome this problem, the number of harvests has been treated as a selection variable since the year 2000. This means that a genotype that requires a greater number of collections can be selected for small farmers with the required labor force. For large producers with limited labor and storage facilities, genotypes with a lower number of collections per harvest can be selected (Nascimento Filho and Atroch, 2002).
GENETIC IMPROVEMENT METHODS Guarana breeding methods used at Embrapa Western Amazon to date vary according to the objective of the program and the human, material and infrastructure resources available. The main methods are described below.
Mass Selection The unconscious preservation of the most attractive or productive plants by the first humans increased the frequency of favorable alleles. The first improved varieties were developed by this method in the majority of seed-propagated crops. In 1981, plant selection work was begun at the Grego´rio Bondar Experimental Station in Barrolaˆndia in the municipality of Belmonte, Bahia. Plants were selected on the basis of the following criteria: canopy conformation, vigor and abundant flowering, with subsequent individual production control. In 1982, new selections were carried out on commercial plants. The success of this method in Bahia is mainly due to the absence of pests (thrips) and diseases (anthracnosis), factors that limit cultivation in Amazonas. Thus, yields in Bahia (12 kg/plant) are 510 times higher than in
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Amazonas (200 g/plant). This method was not successful in Amazonas, and production figures of 12 kg/plant are achieved only with improved clones.
Plant Selection With Progeny Testing According to Bore´m (1997), progeny testing consists of evaluating the genotypes of progeny based on the phenotypes of their descendants. Selection with progeny testing is more efficient than mass selection because it provides a more accurate evaluation of the plants selected, as progenies are evaluated in trials with rigorous experimental designs, resulting in more accurate measurements (Bueno et al., 2001). This method was use in the genetic improvement program at Embrapa Western Amazon from 1976 until the end of the 1980s, and was then abandoned due to the high incidence of anthracnosis in the progenies tested, so no decision could be taken as to which were the best progenies.
Clonal Selection When the technique of rooting cuttings of guarana were achieved at the end of the 1970s, Embrapa Western Amazon began developing clones, and selecting parent plants in progeny tests and in traditional production areas. Clone competition trials was set up for selection and recommendation. This method is still used in the guarana genetic breeding program. In Bahia, 24 guarana clones from the Embrapa Western Amazon breeding program were introduced in 2001 to begin the clone selection program. These clones are being evaluated for yield and incidence of disease. At present, 12 evaluation trials with 27 clones are under way at four locations: four in Manaus (Amazonas), two in Iranduba (Amazonas), four in Maue´s (Amazonas) and two in Itubera´ (Bahia).
Recurrent Intraspecific Selection Ongoing selection can result in restricted genetic diversity and reduce the likelihood of future gains in selection programs, because the breeder has only a limited gene pool to work with. This is an important concern in the guarana breeding program, as the genetic base is naturally narrow. One alternative to attenuate this problem is recurrent selection, which is a breeding method that increases the frequency of favorable alleles in a population, using repeated selection cycles, without drastically reducing the variability of the population, which is maintained by recombination in a selected population of adequate size (Bore´m, 1997). Recurrent selection has been widely used in allogamous perennial species, such as the eucalyptus, pine, and rubber trees, and is very important for successful selection. In the Embrapa Western Amazon breeding program, this method is to be implemented with morpho-agronomic and molecular evaluation of 36 half-sibling progenies to produce a firstcycle improved population, provide support to the clonal selection program and start a controlled-cross breeding program. The project involves selecting progenies and genotypes based on morpho-agronomic traits using a selection index with predicted genetic values, aimed at maximizing genetic gain and genetic diversity in a population, with the specific aim of genetic improvement. Genetic molecular analysis will be used to monitor the variability of parents and progenies, and to help identify divergent parents that could contribute to increasing variability via specific crossings. In the guarana breeding program, the strategy is similar to that proposed by Grattapaglia (2001) and differs only in regard to phenotypic selection and selection indexing, which will be carried out using genetic values estimated by the procedure known as BLUP (best linear unbiased predictor). A selection index aggregates all the morpho-agronomic information, using predicted genetic values, and selection is carried out based on the agronomic potential of the genotypes. A genetic diversity index is calculated based on molecular data and the genotypes with the highest genetic diversity are selected. The best genotypes of the best progenies, with higher agronomic potential and better genetic diversity, are selected, cloned and planted in a recombination plot to produce an improved population in the first cycle. The genotypes with the highest genotypic value are then cloned and evaluation trials set up. The parent stock of the superior genotypes with the greatest additive genetic variance is then used as a source of seeds for open-pollination variety tests. The first-cycle population originates new progenies to continue the process until no further genetic gains are obtained through selection.
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Transcriptome of Fruit With Seeds The Guarana functional and genetic genome project began in 2004. The proposal, involving the CNPq/MCT, was partly to set up Regional Genome Projects, and this has already been done by the recently-formed REALGENE Legal Amazonia Network for Genomic Research (Realgene, 2008). The sequencing of transcripts of three fruit development phases (green immature, intermediate, and mature) of the guarana cultivar BRS-Amazonas produced a bank of ESTs (expressed sequence tags) with 2628 contigs and 5969 sinˆ gletons, with an average length of 773 base pairs (Angelo et al., 2008). Some ESTs are particularly interesting and could, at least in part, explain the medicinal properties attributed to the powder extract of roasted seeds. These properties are gradually being proved by scientific experimentation. They include enzymes that play a part in the pathways for synthesizing and catalyzing flavenoids and carotenoids (146/15 387) and caffeine synthases (94/15 387). A group of related sequences (177/15 387) was also identified with genes for plantpathogen interaction pathways, including pathogenesis-related proteins not yet classified, cystein protease inhibitors, and sequences related to endochitinases. Some of these sequences could contribute to our understanding of documented inter-clone variability, for instance using structural divergence analysis, and the differences in expression between genes that code for them, when correlated with the phenotypic diversity of guarana clones.
FUTURE PROSPECTS Marker-assisted selection is one of the priorities of the guarana breeding program, as well as the selection of openpollination varieties that could be grown in Amazonas and have wide adaptability, good stability and resistance to anthracnosis and super-shooting disease. The current yield figure for recommended genetic materials is 1 kg of dry seeds/plant per year and this should be increased to 2 kg/plant per year to achieve the current yield of guarana in Bahia. In other words, cloned open-pollination varieties should be selected based on this yield figure. A crossing program has already been started and new genetic combinations will be produced to increase the crop’s genetic base so as to guarantee fresh selection gains in the future. Determining the ploidy type and which species are involved in the ploidy event and should be included in the primary gene pool are important factors for the future of the guarana breeding program.
REFERENCES Angelo, P.C.S., Atroch, A.L., Nascimento Filho, F.J., Sousa, N.R., Mendonc¸a, W.S., Fonseca, A.P.A., 2007. Padro˜es de florescimento de clones de ˆ 358 Atroch, Nascimento Filho, Angelo, Freitas, Sousa, Resende and Clement guaranazeiro. In: Pereira, J.C.R., Arruda, M.R. (Eds.), Pesquisa com guaranazeiro na Embrapa Western Amazon: status atual e perspectivas.. Embrapa Western Amazon, Manaus, pp. 244250. Angelo, P.C.S., Nunes-Silva, C.G., Brı´gido, M.M., Azevedo, J.S.N., Assunc¸a˜o, E.N., Sousa, A.R.B., et al., 2008. Brazilian Amazon Consortium for Genomic Research (REALGENE). Guarana (Paullinia cupana var. sorbilis), an anciently consumed stimulant from the Amazon rain forest: the seeded-fruit transcriptome. Plant. Cell. Rep. 27, 117124. Atroch, A.L., 2001. Situac¸a˜o da cultura do guarana´ no Estado do Amazonas. In: Atroch, A.L. (Ed.), Reunia˜o Te´cnica da Cultura do Guarana´, 1. Manaus, AM, 6 a 9 de novembro, 2000.. Embrapa Western Amazon, Anais. Manaus (Embrapa Western Amazon. Documentos, 16). Atroch, A.L., 2002. Aspectos gerais da cultura do guarana´. Foods Food Ingredients J. Japan. 204, 5359. Atroch, A.L., Resende, M.D.V., Nascimento Filho, F.J. do, 2004. Selec¸a˜o clonal em guaranazeiro via metodologia de modelos lineares mistos (REML/BLUP). Rev. Cieˆnc. Agra´r. 41, 193201. Bore´m, A., 1997. Melhoramento de plantas. UFV, Vic¸osa, 547p. Bueno, L.C., de; Mendes, A.N.G., Carvalho, S.P. de, 2001. Melhoramento gene´tico de plantas: princı´pios e procedimentos.. UFLA, Lavras, 282 p. Ducke, A., 1937. Diversidade dos guarana´s. Rodrigue´sia. 3 (9), 155156. Ducke, A., 1938. Plantes nouvelles. Arch. Inst. Biol. Veg. 4 (1), 4647. Escobar, J.R., Costa, P.R.C., Correˆa, M.P.F., 1985. Estimativa de variac¸a˜o do nu´mero de flores femininas efetivas do guaranazeiro. Pesq. Agropecu. Bras. 20 (12), 13651371. Ferreira, M.E., Grattapaglia, D., 1996. Introduc¸a˜o ao uso de marcadores moleculares em ana´lise gene´tica. second ed. EMBRAPA-CENARGEN, Brası´lia, 220 p. (EMBRAPA-CENARGEN. Documentos, 20). Ferrucci, M.S., Solı´s Neffa, V.G., 1997. Citotaxonomia de Sapindaceae sudamericanas. Bol. Soc. Argent. Bot. 33, 7783. Freitas, D.V., Carvalho, C.R., Nascimento-Filho, F.J., Astolfi-Filho, S., 2007. Karyotype with 210 chromosomes in guarana´ (Paullinia cupana ‘Sorbilis’. J. Plant. Res. 120, 399404. Gondim, C.J.E., 1978. Alguns aspectos da biologia reprodutiva do guarana´ (Paullinia cupana var. sorbilis). Dissertac¸a˜o de Mestrado. INPA/FUA, Manaus, 83p. Grattapaglia, D., 2001. Marcadores moleculares em espe´cies florestais: Eucalyptus como modelo. In: Nass, L.L., Valois, A.C.C., Melo, I.T., Valadares-Inglis, M.C. (Eds.), Recursos gene´ticos & melhoramento: plantas. Fundac¸a˜o MT, Rondono´polis, pp. 967993.
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Guerra, M., dos, S., 1986. Citogene´tica de Angiospermas coletadas em Pernambuco. I. Rev. Bras. Gene´t. 9, 2140. Harrington, M.G., Edwards, K.J., Johnson, S.A., Chase, M.W., Gadek, P.A., 2005. Phylogenetic inference in Sapindaceae sensu lato using plastid matK and rbcL DNA sequences. Syst. Bot. 30, 366382. IBGE, 2015. Instituto Brasileiro de Geografia e Estatı´stica. Available at: ,www.sidra.ibge.gov.br.. IPNI, 2008. The International Plant Names Index. Query: family 5 Sapindaceae; genus 5 Paullinia. Available at: ,www.ipni.org/ipni/ query_ipni.html.. Lleras, E., 1992. Espe´cies de Paullinia com potencial econoˆmico. In: Herna´ndez Bermejo, J.E., Leo´n, J. (Eds.), Cultivos marginados: Otra perspectiva de 1492.. FAO, Roma, pp. 193201. , Plant Production and Protection Paper, n. 26. Martins, W., Sousa, D., Proite, K., Guimara˜es, P., Moretzsohn, M., Bertioli, D., 2006. New softwares for automated microsatellite marker development. Nucleic. Acids. Res. 34 (4), e31. Monteiro, M.Y., 1965. Antropogeografia do guarana´. Cadernos da Amazoˆnia, vol. 6. INPA, Manaus, pp. 184. Nascimento Filho, F. J. do, 2003. Interac¸a˜o geno´tipos x ambientes, adaptabilidade, estabilidade e repetibilidade em clones de guarana´ (Paullinia cupana var. sorbilis (Mart.) Ducke). Tese de Doutorado. Universidade Federal de Vic¸osa, Vic¸osa, 182p. Nascimento Filho, F.J., Atroch, A.L., 2002. Guaranazeiro. In: Brukner, C.H. (Ed.), Melhoramento de fruteiras tropicais. UFV, Vic¸osa, pp. 291307. Nascimento Filho, J.F. do, Garcia, T.B., Cruz, C.D., 1994. Estimativa de paraˆmetros gene´ticos em clones de guaranazeiro. Pesq. Agropecu. Bras. 29 (1), 9196. Nascimento Filho, F.J., Garcia, T.B., Sousa, N.R., Atroch, A.L., 2001. Recursos gene´ticos de guarana´. In: first ed Sousa, N.R., Souza, A.G.C. (Eds.), (Org.) Recursos fitogene´ticos na Amazoˆnia Ocidental, vol. 1. Embrapa Amazoˆnia Ocidental, Manaus, pp. 128141. Nascimento Filho, F. J. do, Perecin, M. L. R. de A., Vieira, M.L.C., 2007. Estudos preliminares para a determinac¸a˜o do nu´mero de cromossomos do guaranazeiro (Paullinia cupana var sorbilis (Mart.) Ducke. In: Pereira, J.C.R., Arruda, M. R. de (Eds.), Pesquisa com guaranazeiro na Embrapa Western Amazon: status atual e perspectivas. Embrapa Western Amazon, Manaus, pp. 228231. Pereira, J.C.R., Arau´jo, J.C.A., Nascimento Filho, F.J., Atroch, A.L., Gasparotto, L., Arruda, M.R., et al., 2007a. Avaliac¸a˜o da estabilidade fenotı´pica e da previsibilidade da resisteˆncia em clones de guaranazeiro a Colletotrichum guaranicola. In: Pereira, J.C.R., Arruda, M. R. de (Eds.), Pesquisa com guaranazeiro na Embrapa Western Amazon: status atual e perspectivas.. Embrapa Western Amazon, Manaus, pp. 6267. Pereira, J.C.R., Arau´jo, J.C.A., Nascimento Filho, F.J., Atroch, A.L., Gasparotto, L., Arruda, M.R., et al., 2007b. Avaliac¸a˜o da resisteˆncia a` antracnose em clones de guaranazeiro. In: Pereira, J.C.R., Arruda, M. R. de (Eds.), Pesquisa com guaranazeiro na Embrapa Western Amazon: status atual e perspectivas. Embrapa Western Amazon, Manaus, pp. 7579. Pereira, T.N.S., Sacramento, C.K., 1987. Comportamento floral do guaranazeiro nas condic¸o˜es da Bahia. Rev. Theobroma. 17 (3), 201208. Radlkofer, L., 1931. Sapindacea. In: Engler, A. (Ed.), Das Pflanzenreich, 98. Engelmann, Leipzig, p. 1539. REALGENERede da Amazoˆnia Legal de Pesquisas Genoˆmicas Disponı´vel em: ,http://www.realgene.ufam.edu.br/rede/index_arede.php. (acessado em 28.09.08.). Resende, M.D.V., 2002. Gene´tica biome´trica e estatı´stica no melhoramento de plantas perenes. Embrapa Informac¸a˜o Tecnolo´gica, Brası´lia, 975p. Solis Neffa, V.G., Ferrucci, M.S., 2001. Karyotype analysis of some Paullineae species (Sapindaceae). Caryologia. 54, 371376. Soltis, P.S., Soltis, D.E., 2004. The origin and diversification of angiosperms. Am. J. Bot. 91, 16141626. Sousa, N.R. 2003. Variabilidade gene´tica e estimativas de paraˆmetros gene´ticos Domestication and breeding of the guarana tree em germoplasma de guaranazeiro. Tese de Doutorado. Universidade Federal de Lavras, Lavras. 99p. Souza, A.G.C., et al., 1996. Fruteiras da Amazoˆnia. EMBRAPA-SPI/, Brası´lia, Manaus: EMBRAPA-CPAA. 204p. (Biblioteca Botaˆnica Brasileira, 1). Stebbins, G.L., 1985. Polyploidy, hybridization, and the invasion of new habitats. Ann. Missouri Bot. Garden. 72, 824832. Tropicos, 2008. Tropicos. org. Missouri Botanical Garden. Query: Sapindaceae. Available at: ,http://www.tropicos.org/Name.. Valois, A.C.C., Correa, M.P.F., Vasconcellos, M.E.C., 1979. Estudo de caracteres correlacionados com a produc¸a˜o de ameˆndoas secas no guaranazeiro. Bras. Pesq. Agropecu. Bras. 14 (2), 175179. von Martius, C.F.P., Flora Brasiliensis. Vol. XIII, Part III, Fasc. 122, Coluna 371-372. Disponı´vel em: ,http://florabrasiliensis.cria.org.br. [Consultado em 22.06.08.].
FURTHER READING ´ gua Fria, Municı´pio de Manaus. Manaus, AM: [s.n.]. 6p. Gonc¸alves, J.R., 1964. Relato´rio sobre o trabalho de selec¸a˜o de guarana´ em A Nascimento Filho, F.J. do, Ando, A., Cruz, C.D., Garcia, T.B., 1993. Ana´lise de caminhamento em mudas de guarana´. Pesq. Agropecu. Bras. 28 (4), 447452. Nascimento Filho, F.J. do, Atroch, A.L., Sousa, N.R. de, Garcia, T.B., Cravo, M. da S., Coutinho, E.F., 2001. Divergeˆncia gene´tica entre clones de guaranazeiro. Pesq. Agropecu. Bras. 36 (3), 501506. Patin˜o, V., 1967. M. Plantas cultivadas y animales domesticos en America Equinoccial: fibras, medicinas, miscelanea, vol. 3. Imprenta Departamental, Cali, Coloˆmbia, 65p. Pereira, N., 1954. Os ´ındios Maue´s. Organizac¸o˜es Simo˜es, Rio de Janeiro, 176 p. Ramsey, J., Schemske, D.W., 2002. Neopolyploidy in flowering plants. Ann. Rev. Ecol. Syst. 33, 589639. Souza, A.P., 2001. Biologia molecular aplicada ao melhoramento. In: Nass, L.L., Valois, A.C.C., Melo, I.T., Valadares-Inglis, M.C. (Eds.), Recursos gene´ticos & melhoramento: plantas. Fundac¸a˜o MT, Rondono´polis, pp. 939965. Straus, N.A., 1971. Comparative DNA renaturation kinetics in amphibians. Proc. Natl. Acad. Sci. U.S.A. 68, 799802.
Jabuticaba—Myrciaria spp. Luiz C.C. Saloma˜o, Dalmo L. de Siqueira, Ce´sar F. Aquino and Leila C.R. de Lins Federal University of Vic¸osa, Vic¸osa, Minas Gerais, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry
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Chemical Composition and Nutritional Value Harvest and Postharvest Conservation Industrial Application References
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CULTIVAR ORIGIN AND BOTANICAL ASPECTS The jabuticaba tree is native to the Brazilian south and southeast subtropical regions, and it is also found in Paraguay and Argentina (Mattos, 1983). This tree is found in forests and subforests, in lowlands on riverbanks, but it rarely develops in dense forests (Suguino et al., 2012). The name “jabuticaba” has indigenous origin and it comes from two words: “jabuti” (tortoise), which is the common name given to reptiles of genus Chelonoidis, order Chelonia, family Testudinidae; and “caba”, which means “place”, thus it means the place where one finds tortoises. This designation comes from the presence of these animals near jabuticaba trees; they feed on the fruits that fall to the ground. The jabuticaba tree belongs to the order Myrtales, family Myrtaceae and genus Myrciaria (Mattos, 1983). This family comprises approximately 100 genera and 3500 tree and shrub species spread worldwide (Marchiori and Sobral, 1997). The term ‘jabuticaba’ comprises several species, although there is no consensus on their exact number and botanical classification (Pereira et al., 2005; Lorenzi et al., 2006). This chapter will adopt the classification proposed by Mattos (1983), who assumes the existence of nine jabuticaba tree species: 1—Myrciaria jaboticaba (Vell) O. Berg 5 Myrtus jaboticaba Vell. 5 Myrcia jaboticaba Baill. 5 Eugenia jaboticaba (Vell.) Kiaersk. 5 Plinia jaboticaba (Vell.) Kausel (common name: jabuticaba sabara´, jabuticaba murta); 2—Myrciaria coronata Mattos (common name: jabuticaba coroada, jabuticaba de coroa); 3—Myrciaria cauliflora (DC.) O. Berg 5 Eugenia cauliflora DC. 5 Myrtus cauliflora Mart. 5 Plinia cauliflora (DC.) Kausel (common name: jabuticaba paulista, jabuticaba ponhema, jabuticaba ac¸u, jabuticaba hı´brida); 4—Myrciaria oblongata Mattos (common name: jabuticaba azeda, jabuticaba a´cida); 5—Myrciaria spirito-santensis Mattos; 6—Mirciaria grandifolia Mattos (common name: jaboticatuba, jabuticaba grau´da); 7—Myrciaria peruviana (Poir). Mattos var. trunciflora (Berg) Mattos 5 Myrciaria trunciflora (Berg) 5 Eugenia rubeniana 5 Plinia trunciflora (O. Berg) Kausel (common name: jabuticaba de cabinho, jabuticaba de penca, jabuticaba cafe´, jabuticaba preta); 8—Myrciaria aureana Mattos (common name: jabuticaba branca) and 9—Myrciaria phitrantha (Kiaersk.) Mattos 5 Eugenia phitrantha (Kiaersk.) (common name: jabuticaba costada, jabuticaba branca vinho). All these species are cultivated to a greater or lesser degree in Brazil. However, Myrciaria jaboticaba, commonly known as jabuticaba Sabara´, is the most cultivated species (Fig. 1). It is a 69 m tall semi-deciduous tree. The branches are elongate, cylindrical, and glabrous; with flattened terminal branches. The leaves are membranaceous, glabrous, 2.4 4.3 cm long and 0.61.6 cm wide, with pubescent midrib on the underside. Flowers are white, gathered in fascicles along the main stem and mature branches. The number of flower structures per branch meter ranges from 42 to 185; the number of flowers ranges from 170 to 1500, and the number of fruits ranges from 30 to 400 according to the branch diameter. The fruits are of globoid berry type, with thin and fragile black color peel when the fruit is ripe. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00030-7 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Jabuticaba Sabara´ (Myrciaria jaboticaba) tree with trunk and branches covered with flowers (on the left) and with ripe fruits ready for harvesting (on the right).
TABLE 1 Fruit Characteristics of Several Jabuticaba Tree Species Grown in Vic¸osa, Minas Gerais, Brazil DM (g)
FL (cm)
FD (cm)
SS ( Brix)
AT (%)
6.78
1.20
2.29
2.27
14.0
0.45
M. cauliflora
15.38
2.53
2.91
3.08
14.4
0.65
Branca Vinho
M. phitrantha
7.14
1.37
2.53
2.31
16.1
0.36
Cabinho
M. peruviana
6.52
0.96
2.37
2.24
9.1
0.86
Ac¸u do Horto
M. cauliflora
7.19
1.49
2.27
2.36
14.2
0.90
Canaa˜-Ac¸u
unidentified
7.02
1.48
2.20
2.33
17.6
0.60
Rajada
unidentified
7.84
1.31
2.37
2.39
11.4
0.82
Sabara´ Sul de Minas
M. jabuticaba
10.66
1.97
2.55
2.66
15.4
0.32
Common name
Species
Sabara´
M. jabuticaba
Ac¸u
FM (g)
FM: Fresh matter mass; DM: dry matter mass; FL: fruit length; FD: fruit diameter; SS: soluble solids; TA: titratable acidity citric acid Source: Compiled from Pereira, M.C.T., Saloma˜o, L.C.C., Mota, W.F., Vieira, G., 2000. Atributos fı´sicos e quı´micos de oito clones de jabuticabeiras. Rev. Bras. Frutic. 22, 1621 Pereira et al. (2000).
The pulp, which is the main component of the ripe fruit, is white, gelatinous, with 14 seeds, very sweet, with soluble solid content of approximately 14 Brix and titratable acidity below 0.5%. Seeds are polyembryonic (Barros et al., 1996; Duarte et al., 1997; Magalha˜es et al., 1996a; Mattos, 1983). Another species largely grown in Brazil is jabuticaba hı´brida (Myrciaria cauliflora), a name that comes from the species’ capacity to bear fruit early and often. The fruits are of globoid berry type, black, larger than those from Sabara´ species, 2.22.8 cm long, 2.22.9 cm diameter, with thicker peel. The pulp is white, very sweet, with 1 to 4 seeds (Mattos, 1983; Lorenzi et al., 2006). The jabuticaba tree species show great diversity in its fruits’ physical and chemical features (Table 1). The jabuticaba tree usually sprouts in late Winter and early Spring. However, it may occur at different times of the year. New sprouting events occur on the canopy periphery and they are a purple or light green color dependent on the species (Donadio, 2000).
Jabuticaba—Myrciaria spp.
239
HARVEST SEASON The jabuticaba tree usually flowers twice a year, between July and December, although more flowerings might occur. The harvest takes place from August to February, according to the time of flowering (Suguino et al., 2012). Eighty percent of the jabuticaba production in Brazil occurs from August to November and its peak is in September (Conab, 2015). According to the General Warehouses and Storehouses Company of Sa˜o Paulo (Companhia de Entrepostos e Armaze´ns Gerais de Sa˜o Paulo) (CEAGESP, 2015), which is the largest fruits, vegetables and flowers trading center in Brazil, September and October hold the highest jabuticaba sales volume; during the other months, sales are very small.
ESTIMATED ANNUAL PRODUCTION Although the fruit is well appreciated by the population and despite the large production capacity of the plant—annual average of 200 kg fruits per adult plant—jabuticaba tree orchards are almost exclusively domestic in Brazil. In addition, part of the commercialized product comes from riparian forest native plants, which occur on riverbanks and riverheads, where extractive exploration is carried out. Commercial planting of jabuticaba does not exist in Brazil due to the lack of improved cultivars, the plant’s long juvenile period—which usually lasts more than eight years—and the short fruit harvest and postharvest conservation period. Even grafted plants have a juvenile period longer than five years. However, the plant has strong potential for cultivation and commercialization, depending on the nutritional and organoleptic features of the fruits (Barros et al., 1996). In 2014, fresh jabuticaba sales reached approximately 3.35 thousand tons in Brazil (Conab, 2015). Nevertheless, jabuticaba production and commercialization is quite bigger than that recorded by official agencies, as family farmers and street vendors usually sell much of the fruit in street markets in the cities or along the highways in the producing regions. In addition, part of the production is processed as homemade liquors, jams, and jellies (Suguino et al., 2012). A significant part of the fruits is lost due to the difficulty in harvesting them—because they grow over almost all the branches of the tree, which achieves high size heights (Fig. 1)—and due to the fragility and rapid deterioration of the fruits and to bird and insect attacks. Among the few commercial plantations in Brazil, the one in Hidrolaˆndia County stands out. It is located in the central region of the country, with approximately 38,000 jabuticaba trees distributed in 130 hectares, where the consumer himself picks the desired amount of fruits after paying a fee to enter the farm.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The jabuticaba tree flower can self-pollinate or receive pollen from another plant. Insects are its main pollinator. The fruit set ranges from 7% to 30% (Donadio, 2000). Jabuticaba development can be described by a simple sigmoidal curve. The development period is short and depends on the temperature in the cultivation place. The Sabara´ fruit variety develops during SpringSummer elevated temperatures and its cycle ranges from 35 to 40 days from flowering to harvest (Coletti, 2012). Below a mean temperature of 22 C, the period from flowering to harvest was 42 days (Jesus et al., 2004). Barros et al. (1996) and Magalha˜es et al. (1996a, 1996b) developed the most comprehensive studies on jabuticaba Sabara´ phenology. During the Winter (from June to August), fruit development extended from 60 to 65 days below the mean temperature of 15.8 C. The dry matter accumulation up to 23 days after flowering was only 4% of the maximum value achieved by the fruit. From this period on, it was possible to see the acceleration in this accumulation. On the other hand, the volume of fruits significantly increased approximately 35 days after flowering and it kept on increasing until ripening. Approximately 50% of jabuticaba dry matter is concentrated in the pulp and the proportions for peel and seeds are 30% and 20%, respectively. The fruit maximum dimensions of 1.73 cm long and 1.77 cm diameter were achieved 50 days after flowering (83% of the cycle). However, the dry matter and soluble sugars contents kept on increasing until almost the end of the development period (Barros, et al., 1996; Correˆa et al., 2007). The increased content of total and reducing soluble sugars in the pulp was significant after 35 days (54% of the cycle), thus presenting maximum accumulation near 55 days (85% of the cycle) after flowering. From this period on, the contents of these sugars started decreasing due to oxidation by the respiratory process and due to the beginning of the fruit senescence period (Correˆa et al., 2007). The starch content remained approximately 1 g per 100 g dry matter, until 20 days after flowering. It increased until 47 days after flowering and reached 4.5 g per 100 g dry matter. After
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this period, the content decreased until fruit ripening and again reached approximately 1 g per 100 g dry matter (Barros, et al., 1996). The stabilization in fruit dimensions and sugar accumulation indicated that jabuticaba maturation occurred from 50 days after flowering commenced. In addition, after this time, there was decrease in peel chlorophyll content; it went from approximately 100 μmol/m2 to approximately 10 μmol/m2 at harvest time (60 days after flowering). There was also increase in the anthocyanin contents; it ranged from 0.5 μmol/m2 to approximately 240μmol/m2 at harvest time (Barros et al., 1996; Magalha˜es et al., 1996a). The jabuticaba respiratory activity progressively increased 25 days after flowering and it reached its maximum near the 55th day (84% of the cycle). From this period on, the respiratory rate decreased until 62 days after flowering (95% of the cycle). In this phase, it was possible to see all the typical features of the ripe fruit, when the maximum peroxidase activity values met the maximum respiratory activity (Correˆa et al., 2007). From the 62nd to the 65th day, the respiratory rate increased again. This fact may indicate fruit senescence with cell walls dissolution (Wallace and Fry, 1999) and it corroborates the study by Magalha˜es et al. (1996b) who found a drastic decrease in fruit pectin content 55 days after flowering. Results from studies on jabuticaba respiratory pattern are scarce and conflicting. Teixeira et al. (2011) suggested that jabuticaba shows the typical respiratory pattern of nonclimacteric fruits. However, according to Daiuto et al. (2009) and Correˆa et al. (2007), jabuticaba shows the typical respiratory pattern of climacteric fruits. There was mineral content increase during fruit growth until approximately 51 days after flowering (78% of the cycle). At 43 days after flowering, the peel showed approximately 80% of total phosphorus, potassium, calcium, zinc, and manganese, and 60% of total nitrogen, magnesium, and iron accumulated in the fruit. Thereafter, as the fruits developed, the mineral content diminished in the peel and increased in the pulp and in the seed. There were higher ratios of minerals in the pulp at the end of the cycle, except for calcium and manganese, that showed higher levels in the peel (Souza, 1992).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Jabuticaba is a considerable source of carbohydrates, dietary fiber, vitamin C, mineral salts, and phenolic compounds (Lima et al., 2008; Ascheri et al., 2006). The fruit and its products have a characteristic flavor and aroma, which depend on the balance among organic acids, sugars, polyphenols, and volatile compounds in the fruit. The fruit peel and seed altogether represent 50% of the fruit mass and they are rich in insoluble fibers. The insoluble fraction contains cellulose, and some hemicelluloses and lignin. The soluble fraction consists of pectins, gums, mucilages and some hemicelluloses (Lima et al., 2008; Magalha˜es et al., 1996b). The insoluble fiber content in the peel is 27.03 g per 100 g dry matter and the soluble fiber content is 6.77 g per 100 g dry matter (Lima et al., 2008). Reducing sugars are the most abundant soluble carbohydrates in the pulp, and fructose is found in greater amounts (Lima et al., 2011b; Barros et al., 1996). The peel contribution to the total amount of sugars in the fruit is low (Barros et al., 1996). The entire fruit shows 48.33 g of total soluble sugars per 100 g dry matter, 40.21 g of reducing sugar per 100 g DM and 7.70 g of non-reducing sugars per 100 g DM (Lima et al., 2011b). The fruit pulp accumulates approximately 60 g of total soluble sugars per 100 g dry matter, and approximately 81% of it corresponds to reducing sugars. Reducing sugars also predominate in the peel and in the seeds (Barros, et al., 1996; Correˆa et al., 2007). The scientific literature reports soluble solids in the pulp ranging between 9.1 Brix and 17.9 Brix, in different varieties and cultivation regions, and the highest values are found in Sabara´ variety (Pereira et al., 2000; Oliveira et al., 2003; Lima et al., 2008). As for the jabuticaba phenolic compounds, the values range from 6.49 to 8.51 g per 100 g dry mass of the entire ripe fruit in Paulista and Sabara´ varieties, respectively. The fruit main phenolic compounds are the anthocyanins. They are water-soluble flavonoid class pigments, which give color to flowers, fruits, and leaves. These colors range among purple, red, or violet depending on the medium pH (Lima et al., 2008). The anthocyanin contents in the fruit peel range between 1.58 and 2.05 g per 100 g dry matter in Paulista and Sabara´ varieties, in which there is the occurrence of cyanidin-3-glucoside and delphinidin-3-glucoside anthocyanins (Lima et al., 2011a; Santos et al., 2010). Recent studies also showed that jabuticaba is an ellagic acid source—a polyphenol with antioxidant properties—and its largest amount is found in the seeds (5.05 g per 100 g dry matter) (Abe et al., 2011; Alezandro et al., 2013). Nonripe fruits have higher phenolic compound contents (proanthocyanidins and ellagitannins) and higher antioxidant capacity; ripening leads to 47% decrease in ellagic acid derivatives, 43% decrease in proanthocyanidins and to 60%77% decrease in antioxidant ability (Alezandro et al., 2013).
Jabuticaba—Myrciaria spp.
241
The main organic acids found in jabuticaba in quantitative descending order are: citric acid, succinic acid, malic acid, oxalic acid, and acetic acid (Lima et al., 2011b). Oliveira et al. (2003) found vitamin C content ranging from 14.86 to 24.67 mg ascorbic acid per 100 g pulp of fruits in the Sabara´ variety. Tannins are mainly found in the peel and they provide the astringent sensation when the fruit is chewed. They are also important in wine production (Rezende, 2011). Forty-five volatile compounds were identified in the fruits, 23 of them provide sensory impressions. Among the identified compounds, terpenes, organic acids and alcohols are the most volatile jabuticaba components; especially terpenes that contribute to the fruit flavor (Plagemann et al., 2012). As for the minerals, the order of macronutrients exportation by the fruits is K (1.8) . N (1.54) . Mg (0.22) . P (0.18) . Ca (0.06 kg/ton of fresh matter). As for the micronutrients, the order is Fe (18) . Zn (2.92) . Mn (2.05 g/ton of fresh matter) (Souza, 1992). According to the Brazilian Food Composition Table (Brazil, 2011), the mean centesimal composition of the jabuticaba edible part consists of 83.6% water, 58 kcal or 243 kJ of energy value, 0.6 g protein, 0.1 g lipids, 15.3 g carbohydrates, 2.3 g dietary fiber, 0.4 g ash, 8.0 mg calcium, 0.1 mg iron, 15.0 mg phosphorus, 130.0 mg potassium, and 16.2 mg vitamin C.
HARVEST AND POSTHARVEST CONSERVATION The fruits must be harvested when they are fully ripe, because partially ripe fruits do not complete maturation (Duarte et al., 1997). At the end of maturation, the peel dry matter and thickness decreases and the pulp dry matter increases, titratable acidity decreases, pH and soluble solids content increase, total and reducing soluble sugar values show significant increase, and the starch content decreases. Fruits also lose consistency due to pectin solubilization. There is chlorophyll content decrease and anthocyanin accumulation in the peel when the fruits reach the species-typical color (Arau´jo et al., 2010; Barros et al., 1996; Magalha˜es et al., 1996a). The harvesting point is indicated by the usual black color of the fruits and by their softness at finger compression. Harvesting is done manually and the fruits must be carefully placed into small containers in order to avoid mechanical damage. Fruits must be promptly transported for commercialization in order to preferably reach the consumer in the same day they are harvested, as they are highly perishable (Duarte et al., 1997; Donadio, 2000). The harvesting period lasts few days, because flowering is quite homogeneous and fruits quickly senesce on the plant. The postharvest commercialization period is short due to the rapid change in the fruit appearance resulting from intense moisture loss, and pulp deterioration and fermentation, which can be seen within two to three days after harvest at ambient conditions. The microbial deterioration as well as the fermentation may be associated with high sugar content in the fruit (Barros et al., 1996; Jesus et al., 2004). Using technologies to delay the postharvest metabolism in order to prolong the shelf life of the fruits, both for fresh consumption and for processing, is important to the commercial success of jabuticabas. The temperature of 12 C, associated with relative humidity of 87 6 2%, helps keeping the functional quality and biochemistry of Sabara´ jabuticaba for up to 30 days (Duarte et al., 1997; Vieites et al., 2011). At this temperature, the fruits show higher content of total phenolic compounds as well as higher antioxidant activity in comparison to fruits stored at lower temperatures. In addition, fruits stored at 12 C show delayed and decreased respiratory peak (Vieites et al., 2011). Hot water treatment followed by cold storage is another alternative for jabuticaba conservation. Fruits immersed in water at 20 C25 C, for 10 min, and subsequently stored at 9 C and 85%90% relative humidity, exhibit delay in the maximum respiratory rate, keep the vitamin C content and decrease polyphenoloxidase enzyme activity, thus maintaining postharvest quality for up to 45 days under these conditions (Daiuto et al., 2010). Jabuticabas packed in stretchable and self-adhering PVC plastic films (020 μm thick) and kept in polystyrene trays at the temperature of 11 C 1 1 C with 98% relative humidity are able to reduce the fresh mass loss and show good appearance and quality for up to 6 days (Brunini et al., 2004). The use of 15 μm thick plastic bags with 0.5 mm diameter perforations was effective to keep the commercial quality of jabuticabas intended for fresh consumption for 8 days, at 0 C and 90% RH, plus two days at 20 C22 C and 70%75% RH. In the case of fruits intended for processing, the quality was kept for 10 days at 0 C and 90% RH (Machado et al., 2007). Calcium is associated with fruit ripening regulation due to the formation of bridges between pectic acids and other acidic polysaccharides, which work as antisenescence sites. However, calcium contribution to increase fruit commercialization period is small. The fruit immersion in CaCl2 40 g/L solution for 40 min leads to increased consistency retention without reducing the fruit fresh mass loss (Mota et al., 2002).
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INDUSTRIAL APPLICATION Different types of beverages may be manufactured out of jabuticaba. Asquieri et al. (2004) studied the production process of alcohol beverages similar to dry and sweet red wine made out of the entire jabuticaba fruit and they found that consumers preferred the sweet wine. The fruit may be also processed as nectar, which is natural, nutritious, and ready for consumption drink. Making jellies and jams is also an alternative for fruits conservation, because the heat and the increase in sugar concentration due to osmotic pressure changes increase the product shelf life (Krolow, 2005). The jelly made out of jabuticaba peel shows good sensory and nutritional features and acceptability. In addition, it has higher nutrient content than that made out of the pulp, and it stands out as source of natural fibers and pigments (Dessimoni-Pinto et al., 2011). Pulp freezing is an industrialization process that preserves fruits features and enables its consumption in off-season periods. In addition, it gives producer the alternative to use fruits that do not meet the fresh product commercial standard or fruits with noncompensating prices (Garcia, 2014; Matta et al., 2005) Jabuticaba peel and seeds are usually discarded as waste when the fruit is consumed. However, their use in the food industry may be quite promising due to their high nutritional value, high content of fibers and phenolic compounds as well as to their good antioxidant potential. The jabuticaba peel flour may be used as additive in formulations such as soups, sauces, sausages, pasta, cheeses, cakes, bakery products, yoghurt dye, among others (Alves et al., 2013; Silva et al., 2010; Brunini et al., 2004). Peel and dregs, as byproducts from fermented jabuticaba, are raw materials used to produce jabuticaba brandy (Asquieri et al., 2009). Jabuticaba peel may be also used to produce red wine (Asquieri et al., 2004). Dried or sweetmeat jabuticaba peels may be obtained by osmotic dehydration using saccharose solution at 70 Brix and 60 C, followed by drying process at 60 C for 4 h. The obtained product has mean moisture content of 23% and low water activity (Garcia, 2014). The jabuticaba tree may also be used as ornamental plant due to its beautiful flowering, appearance, and the delicate aroma of the flowers as well as to its exotic fruiting; the fruits are attached to the plant trunk and branches (Citadin et al., 2010; Lorenzi et al., 2006). According to Borges and Melo (2013), the jabuticaba tree timber is durable and may be allocated to woodwork; however, the plant takes tens of years to become an adult, although with relatively thin trunks. Therefore, its commercial use for timber exploitation is unprofitable. The jabuticaba tree has the following phytotherapeutic indications in the folk medicine: anti-asthma, inflamed tonsils, inflamed intestines, hemoptysis, erysipelas, and chronic quinsy (Borges and Melo, 2013). The jabuticaba peel flour is proven effective in cardiovascular protection since it increases HDL serum level, shows good antioxidant activity and has hepatoprotective effect (Lage, 2014). Phenolic compounds found in jabuticaba peel have inhibitory effect on α-amylase enzyme and it allows the use of its flour in diabetes and obesity prevention and control by reducing the ingested starch degradation (Alezandro et al., 2013; Lage, 2014). The main phenolic compounds identified in the jabuticaba pulping residue (anthocyanins and ellagic and gallic acids) are associated with the lower risk of developing certain types of cancer, cardiovascular diseases, diabetes, and other chronic diseases (Inada et al., 2015; Nile; Park, 2014). Some studies suggest the jabuticaba extract antimicrobial effect. Haminiuk et al. (2011) showed slight in vitro inhibitory effect of the fruit extract on Klebsiella pneumoniae. The jabuticaba leaf extract has potential antimicrobial activity against bacteria in the oral cavity (Streptococcus mutans, Streptococcus sobrinus, and Streptococcus saguis) and some Candida species (C. albicans, C. parapsilosis and C. tropicalis) (Souza-Moreira et al., 2010; Carvalho et al., 2009). As antidiarrheal, Souza-Moreira et al. (2010) reported that the jabuticaba leaf extract shows activity against Enterocococcus faecalis, Escherichia coli, Salmonella spp. and Shigella spp., but it has no effect on gastrointestinal motility.
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Ascheri, D.P.R., Ascheri, J.L.R., Carvalho, C.W.P., 2006. Efeito da extrusa˜o sobre a adsorc¸a˜o de a´gua de farinhas mistas pre´-gelatinizadas de arroz e bagac¸o de jabuticaba. Cieˆnc. Tecnol. Aliment. 26, 325335. Asquieri, E.R., Candido, M.A., Damiani, C., Assis, E.M., 2004. Fabricacio´n de vino blanco y tinto de jabuticaba (Myrciaria jaboticaba Berg) utilizando la pulpa y la ca´scara respectivamente. Alimentaria. 355, 97109. Asquieri, E.R., Silva, A.G.M., Candido, M.A., 2009. Aguardente de jabuticaba obtida da casca e borra da fabricac¸a˜o de fermentado de jabuticaba. Cieˆnc. Tecnol. Aliment. 29, 896904. Barros, R.S., Finger, F.L., Magalha˜es, M.M., 1996. Changes in non-structural carbohydrates in developing fruit of Myrciaria jaboticaba. Sci. Hortic. (Amsterdam). 66, 209215. Borges, M.H.C.B., Melo, B., 2013. Cultura da jabuticabeira. Nu´cleo de Estudo em Fruticultura no Cerrado, Uberlaˆndia. Available at: ,http://www. fruticultura.iciag.ufu.br/jabuticaba.html.. Brasil, 2011. Ministe´rio da Sau´de. Ageˆncia Nacional de Vigilaˆncia Sanita´ria, Tabela brasileira de composic¸a˜o de alimentos. fourth ed. TACO, Campinas, 164 p. Brunini, M.A., Oliviera, A.L., Salandini, A.R., Bazzo, F.R., 2004. Influeˆncia de embalagens e temperatura no armazenamento de jabuticaba (Myrciaria jabuticaba (Vell) Berg) cv Sabara´. Cieˆnc. Tecnol. Aliment. 24, 378383. Carvalho, C.M., Macedo-Costa, M.R., Pereira, M.S.V., Higino, J.S., Carvalho, L.F.P.C., Costa, L.J., 2009. Efeito antimicrobiano in vitro do extrato de jabuticaba [Myrciaria cauliflora (Mart.) O. Berg.] sobre Streptococcus da cavidade oral. Rev. Bras. Plantas Med. 11, 7983. CEAGESP-Companhia de Entrepostos e Armaze´ns Gerais de Sa˜o Paulo, Sazonalidade dos produtos comercializados no ETSP. Available at: ,http:// www.ceagesp.gov.br/wp-content/uploads/2015/05/produtos_epoca.pdf.. Conab-Companhia Nacional de Abastecimento, Programa brasileiro de modernizac¸a˜o do mercado hortigranjeiro. Disponı´vel em: ,http://dw.prohort. conab.gov.br/pentaho/Prohort.. Acesso em: 01 jun. 2015. Citadin, I., Danner, M.A., Sasso, S.A.Z., 2010. Jabuticabeiras. Rev. Bras. Frutic. 32, 343656. Coletti, L.Y., 2012. Curva de maturac¸a˜o de frutos e potencial germinativo de sementes de jabuticaba ‘Sabara´’ (Myrciaria jaboticaba Berg.). Dissertac¸a˜o de Mestrado (Mestrado em Fitotecnia). Universidade de Sa˜o Paulo, Piracicaba, 59p. Correˆa, M.O.G., Pinto, D.D., Ono, E.O., 2007. Ana´lise da atividade respirato´ria em frutos de jabuticabeira. Rev. Bras. Biocieˆnc. 5, 831833. Daiuto, E´.R., Vieites, R., Moraes, M., Evangelista, M., 2010. Qualidade po´s-colheita dos frutos de jabuticaba tratada por hidrotermia. Agron. Trop. 60, 231240. Daiuto, E´.R., Vieites, R.L., Moraes, M.R., Evangelista, R.M., 2009. Conservac¸a˜o po´s colheita de frutos de jabuticaba por irradiac¸a˜o. Rev. Iberoam. Tecnol. Postcosecha. 10, 3644. Dessimoni-Pinto, N.A.V., Moreira, W.A., Cardoso, L.M., Pantoja, L.A., 2011. Jaboticaba peel for jelly preparation: na alternative technology. Cieˆnc. Tecnol. Aliment. 31, 864869. Donadio, L.C., 2000. Jabuticaba (Myrciaria jabuticaba (Vell.) Berg). Funep, Sa˜o Paulo, Brasil, 55 p. (Se´rie Frutas Nativas, 3). Duarte, O., Huete, M., Ludders, P., 1997. Extending storage life of jaboticaba (Myrciaria cauliflora (Mart.) Berg)fruits. Acta. Hortic. 452, 131136. Garcia, L.G.C., 2014. Aplicabilidade tecnolo´gica da jabuticaba. Dissertac¸a˜o de Mestrado (mestrado Cieˆncia e Tecnologia de Alimentos). Universidade Federal de Goia´s, Goiaˆnia, 220p. Haminiuk, C.W.I., Plata-Oviedo, M.S.V., Guedes, A.R., Stafussa, A.P., Bona, E., Carpes, S.T., 2011. Chemical, antioxidant and antibacterial study of Brazilian fruits. Int. J. Food Sci. Technol. 46, 15291537. Inada, K.O.P., Oliveira, A.A., Revoreˆdo, T.B., Martins, A.B.N., Lacerda, E.C.Q., Freire, A.S., et al., 2015. Screening of the chemical composition and occurring antioxidants in jabuticaba (Myrciaria jaboticaba) and jussara (Euterpe edulis) fruits and their fractions. J. Funct. Foods. 17, 422433. Jesus, N., Martins, A.B.G., Almeida, E.J., Leite, J.B.V., Ganga, R.M.D., Scaloppi Junior, E.J., et al., 2004. Caracterizac¸a˜o de quatro grupos de jabuticabeira, nas condic¸o˜es de Jaboticabal-SP. Rev. Bras. Frutic. 26, 482485. Krolow, A.C.R., 2005. Preparo artesanal de geleias e geleiadas.. Embrapa Clima Temperado, Pelotas, 29 p. Lage, F.F., 2014. Casca de jabuticaba: inibic¸a˜o de enzimas digestivas, antioxidante, efeitos biolo´gicos sobre o fı´gado e perfil lipı´dico. Tese de Doutorado (Programa de Po´s-Graduac¸a˜o em Agroquı´mica) Universidade Federal de Lavras, Lavras, 138 p. Lima, A.J.B., Correˆa, A.D., Alves, A.P.C., Abreu, C.M.P., Dantas-Barros, A.M., 2008. Caracterizac¸a˜o quı´mica do fruto jabuticaba (Myrciaria cauliflora Berg) e de suas frac¸o˜es. Arch. Latinoam. Nutr. 58, 416421. Lima, A.J.B., Correˆa, A.D., Saczk, A.A., Martins, M.P., Castilho, R.O., 2011a. Anthocyanins, pigment stability and antioxidant activity in jabuticaba [Myrciaria cauliflora (Mart.) O. Berg]. Rev. Bras. Frutic. 33, 877887. Lima, A.J.B., Correˆa, A.D., Dantas-Barros, A.M., Nelson, D.L., Amorim, A.C.L., 2011b. Sugars, organic acids, minerals and lipids in jabuticaba. Rev. Bras. Frutic. 33, 540550. Lorenzi, H., Bacher, L.B., Lacerda, M., Sartori, S., 2006. Frutas Brasileiras e exo´ticas cultivadas de consumo in natura. Instituto Plantarum de Estudos da Flora, Nova Odessa-SP, Sa˜o Paulo, 640p. Machado, N.C., Coutinho, E.F., Caetano, E.R., 2007. Embalagens Pla´sticas e refrigerac¸a˜o na conservac¸a˜o po´s-colheita de jabuticabas. Rev. Bras. Frutic. 29, 166168. Magalha˜es, M.M., Barros, R.S., Lopes, N.F., 1996a. Growth relations and pigment changes in developing fruit of Myrciaria jaboticaba. J. Hortic. Sci. 71, 925930. Magalha˜es, M.M., Barros, R.S., Finger, F.L., 1996b. Changes in structural carbohydrates in developing fruit of Myrciaria jaboticaba. Sci. Hortic. (Amsterdam). 66, 1722. Marchiori, J.N.C., Sobral, M., 1997. Dendrologia das angiospermas-Myrtales. Editora UFSM, Santa Maria, 304 p.
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Matta, V.M., Freire Junior, M., Cabral, L.M.C., Furtado, A.A., 2005. Polpa de fruta congelada. Agroindustrial Familiar. Embrapa Informac¸a˜o Tecnolo´gica, Brası´lia, 38 p. Mattos, J.R., 1983. Fruteiras nativas do Brasil: Jaboticabeiras.. Instituto de Pesquisas de Recursos Naturais Renova´veis, Porto Alegre, 92p. Mota, W.F., Saloma˜o, L.C.C., Pereira, M.C.T., Cecon, P.R., 2002. Influeˆncia do tratamento po´s-colheita com ca´lcio na conservac¸a˜o de jabuticabas. Rev. Bras. Frutic. 24, 049052. Nile, S.H., Park, S.W., 2014. Edible berries: Bioactive components and their effect on human health. Nutrition. 30, 134144. Oliveira, A.L., Brunini, M.A., Salandini, C.A.R., Bazzo, F.R., 2003. Caracterizac¸a˜o tecnolo´gica de jabuticabas ‘Sabara´’ provenientes de diferentes regio˜es de cultivo. Rev. Bras. Frutic. 25, 397400. Pereira, M.C.T., Saloma˜o, L.C.C., Mota, W.F., Vieira, G., 2000. Atributos fı´sicos e quı´micos de oito clones de jabuticabeiras. Rev. Bras. Frutic. 22, 1621. Pereira, M., Oliveira, A.L., Pereira, R.E.A., Sena, J.A.D., Costa, J.R.V., Almeida, M., et al., 2005. Morphologic and molecular characterization of Myrciaria spp species. Rev. Bras. Frutic. 27, 507510. Plagemann, I., Kringsa, U., Bergera, R.G., Marostica Jr, M.R., 2012. Volatile constituents of jabuticaba (Myrciaria jaboticaba (Vell.) O. Berg) fruits. J. Essent. Oil Res. 24, 4551. Rezende, L.C.G., 2011. Influeˆncia do processamento no teor de compostos feno´licos e na avaliac¸a˜o sensorial de gele´ia de jabuticaba (Myrciaria jaboticaba Vell. Berg). Dissertac¸a˜o de Mestrado. Universidade Federal de Minas Gerais, 89 p. Santos, D.T., Veggi, P.C., Meireles, M.A.A., 2010. Extraction of antioxidant compounds from Jabuticaba (Myrciaria cauliflora) skins: Yield, composition and economical evaluation. J. Food Eng. 101, 2331. Silva, F.J.F., Constant, P.B.L., Figueiredo, R.W., Moura, S.M., 2010. Formulation and stability of anthocyanins’s colorantes formulated with peels jabuticaba (Myrciaria spp.). Aliment. Nutr. 21, 429436. Souza, R.B., 1992. Acu´mulo e distribuic¸a˜o de minerais no fruto de jaboticaba (Myciaria jaboticaba Berg cv. ‘Sabara´’) em desenvolvimento. Dissertac¸a˜o de mestrado (mestrado em Fisiologia Vegetal). Universidade Federal de Vic¸osa, Vic¸osa, MG, 69p. Souza-Moreira, T.M., Moreira, R.R.D., Sacramento, L.V.S., Pietro, R.C., 2010. Histochemical, phytochemical and biological screening of Plinia cauliflora (DC.) Kausel, Myrtaceae, leaves. Braz. J. Pharmacogn. 20, 4853. Suguino, E., Martins, A.N., Turco, P.H.N., Cividanes, T.M.S., Faria, A.M., 2012. A cultura da jabuticabeira. Pesqui. Tecnol. 9, 17. Teixeira, G.H., Durigan, J.F., Santos, L.O., Hojo, E.T.D., Cunha Ju´nior, L.C., 2011. Changes in the quality of jaboticaba fruit (Myriciaria jaboticaba (Vell) Berg. cv. Sabara´) stored under different oxygen concentrations. J. Sci. Food Agric. 91, 28442849. Vieites, R.L., Daiuto, E.R., Moraes, M.R., Neves, L.C., Carvalho, L.R., 2011. Caracterizac¸a˜o fı´sico-quı´mica, bioquı´mica e funcional da jabuticaba armazenada sob diferentes temperaturas. Rev. Bras. Frutic. 33, 362375. Wallace, G., Fry, S.C., 1999. Action of diverse peroxidases and laccases six related cell wall- related phenolic compounds. Phytochemistry. 52, 769773.
Jambo—Syzygium malaccense Fabiano A.N. Fernandes and Sueli Rodrigues Federal University of Ceara´, Fortaleza, Ceara´, Brazil
Chapter Outline Introduction Botanical Aspects Harvest Season Harvest and Postharvest Conservation
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Chemical Composition and Nutritional Value Sensory Characteristics Industrial Application References
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INTRODUCTION Syzygium malaccense belongs to the Myrtaceae Family and it is a species of flowering tree native to the Indo-China region, more specifically to Malaysia, Indonesia, Vietnam, and Thailand. Its occurrence has spread to Australia, India, Brazil, and many Caribbean countries. The fruit of this tree has a variety of common names, it is known as the Malay apple, Malay rose, nakavita, jambu merah, jambu bol, jambo, otaheite cashew, mountain apple, and pommerac.
BOTANICAL ASPECTS S. malaccense is a fast-growing tree, which reaches between 12 and 18 m when fully grown (Fig. 1). It has an erect trunk and a pyramidal or cylindrical crown. Its evergreen leaves are opposite, short-petioled, ellipticlanceolate or oblanceolate, are about 1545 cm in length and 920 cm in width. The flowers are abundant, mildly fragrant, and borne on the upper trunk and along leafless portions of mature branches. The flowers grow in short-stalked clusters of 28 and are pink to dark-red colored (Martin et al., 1987). The fruit (Malay apple) (Fig. 2) is oblong, obovoid, or bell-shaped. It ranges from 5 to 10 cm in length and from 2 to 8 cm in width in its widest part. The skin is red colored and smooth. The fruit presents a white and juicy flesh, with a sweet flavor that resembles the taste of green grapes. It has a single light-brown and nearly-round seed of about 2 cm in diameter. Each fruit weighs about 39 6 2 g. Most of the weight refers to the meat of the fruit (30 6 2 g), followed by the seed (7 6 1 g) and the skin (3 6 1 g) (Augusta et al., 2010). Besides the traditional Malay apple, two other varieties are reported. A white variety (djamboo pootih) is cultivated in Java (Indonesia); and a more sweet variety was introduced in the Philippines and Hawaii.
HARVEST SEASON In the Indo-China region, the tree flowers in May and June and the fruits ripen in August and September. In India, the main crop occurs from May to July and there is often a second crop in November and December. In the Caribbean and in Brazil, the tree flowers 2 or 3 times a year (Spring, Summer and Fall) but the biggest crops are during the Spring and Fall flowering seasons. The fruits mature in approximately 60 days after full opening of the flowers. The fruit usually falls quickly after becoming fully ripe and deteriorates very fast. Harvesting is carried out by hand picking. There is no estimate on world or regional production of Malay apples, but each tree produces from 20 to 80 kg of fruit per season. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00031-9 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Syzygium malaccense tree.
FIGURE 2 The Malay apple.
HARVEST AND POSTHARVEST CONSERVATION S. malaccense fruits are highly perishable and have a short shelf-life, ranging from 3 to 6 days after harvesting. Each fruit has to be carefully picked from the tree and maintained at ambient temperature (28 C). The susceptibility of Malay apples to cold is uncertain. While some researchers report that the fruit deteriorates fast in the refrigerator, a study carried out by Basanta and Sankat (1994) have shown that the optimum storage temperature is of 5 C and that under this condition the fruit increase their shelf-life to 30 days and present reduced skin color decay. Storage should be preferably in a dark storage room as the fruit deteriorates more rapidly when exposed to light. Exposure to light fades the fruit’s bright red skin color.
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CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Malay apples are not a major source of any particular vitamin but has a regular amount of vitamins B1 and B2 compared to other common fruits. Table 1 presents the nutritional value and chemical composition of Malay apples and Table 2 presents the nutritional value and chemical composition of the skin of Malay apples. Malay apples have from 0.2 to 1.1 mg of volatiles per 100 g of fruit pulp (wet basis), depending on the variety. The varieties from Indo-China present the lowest volatile content, while the variety cultivated in the Americas present the highest volatile content. Table 3 presents the major volatile constituents of the Malay apple (Pino et al., 2004). The volatile profile of Malay apples give them a rose odor with slight sweet and herbaceous odor. Minor constituents of Malay apples also include other aromatic compounds, monoterpenoids, sesquiterpene hydrocarbons, and aliphatic compounds (alcohols, aldehydes, ketones, and esters) (Wong and Lai, 1996). TABLE 1 Chemical Composition and Nutritional Value of Syzygium malaccense Fruit Component
Amount per 100 g of the edible portion
Moisture
88 6 4 g
Fat
0.2 6 0.1 g
Fiber
0.7 6 0.1 g
Protein
0.6 6 0.1 g
Ash
0.3 6 0.1 g
Calcium
5.7 6 0.2 mg
Iron
0.5 6 0.3 mg
Phosphorus
14.7 6 3.2 mg
Vitamin A
7 6 4 I.U.
Vitamin C
11.7 6 5.2 mg
Vitamin B1 (Thiamine)
27 6 12 μg
Vitamin B2 (Riboflavin)
30 6 10 μg
Vitamin B3 (Niacin)
0.3 6 0.1 mg
TABLE 2 Chemical Composition and Nutritional Value of the Skin of Syzygium malaccense Fruit (Augusta et al., 2010) Component
Amount per 100 g of skin
Moisture
14.1 6 0.4 g
Fat
4.5 6 0.1 g
Fiber
9.3 6 0.2 g
Protein
8.6 6 0.2 g
Sugars
3.0 6 0.4 g
Ash
4.2 6 0.4 g
Vitamin C
292.6 6 0.8 mg
Anthocyanins
300.5 6 0.5 mg
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TABLE 3 Major Volatile Constituents of Malay Apple (Pino et al., 2004) Constituent
Concentration (mg/kg)
Odor unit
Ethanol
1.77
,1
1-Propanol
0.77
,1
1-Octen-3-ol
0.32
320.0
(Z)-3-Hexanol
0.16
2.3
1-Hexanol
0.14
,1
Isobutanol
0.12
,1
Isoamyl alcohol
0.11
,1
Hexanal
0.09
18.0
Ethyl acetate
0.08
16.0
Diacetyl
0.05
12.5
Antioxidant assays with the fruit showed an IC50 of 269 6 8 μg/mL (DPPH assay), 8.6 6 0.1 mg GAE/g dry weight of total phenolic content and only traces of total anthocyanin content (mg C3G/g dry weight). The quantification of phenolic showed the presence of cyaniding-3-glycoside (0.02 mg/g), quercitrin (0.02 mg/g), rutin (0.02 mg/g), and ellagic acid (0.01 mg/g) on a dry basis (Reynertson et al., 2008). Anthocyanin content decreases with storage time. Malay apples may lose up to 70% of their anthocyanin content in 10 days after harvesting and up to 95% in 30 days of storage (Sankat et al., 2000).
SENSORY CHARACTERISTICS The ripe fruits presents a rose-like fragrance. Their taste has been described as crisp, watery, earthy, insipid, and slightly sweet. In most cases, their taste resembles the taste of green grapes. Some varieties are astringent with a slightly bitter aftertaste. The texture of a ripe Malay apple is similar to the texture of pears. Some fruits are spongier than others. Fading of the bright red skin color increases with storage time and the fading is more pronounced on fruits stored under light (Sankat et al., 2000).
INDUSTRIAL APPLICATION Malay apples are used to produce red and white table wines in the Caribbean. The fruits are picked as soon as they are fully colored. To make the red table wine, the meat and skin are grinded together, while to produce the white table wine only the meat is used. The wine is produced adding yeast, 1 L of water and 150 g of sugar to each 1 kg of fruit and letting it rest for 612 months in barrels stored in a cool storage room. After this period, the wine is filtered and bottled. Other common uses of Malay apples is in the production of sauces and preserves. The slightly unripe fruits are used for making jelly and pickles. Agro-industrial possibilities for processed Malay apples include canned and candied fruit (Sankat et al., 2000).
REFERENCES Augusta, I.M., Resende, J.M., Borges, S.V., Maia, M.C.A., Couto, M.A.P.G., 2010. Caracterizac¸a˜o fı´sica e quı´mica da casca e polpa de jambo vermelho (Syzygium malaccensis, (L.) Merryl & Perry). Cieˆnc. Tecnol. Aliment. 30, 928932. Basant, A., Sankat, C.K., 1994. Postharvest storage of the pomerac (Syzygium malaccense) under refrigeration. In: Proceeding of the 30th Annual Meeting of the Caribbean Food Crop Society, pp. 365368.
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Martin, F.W., Campbell, C.W., Ruberte, R.M., 1987. Perennial Edible Fruits of the Tropics: An Inventory. USDA Agricultural Research Service, Washington, DC. Pino, J.A., Marbot, R., Rosado, A., Vazquez, C., 2004. Volatile constituents of Malay rose apple [Syzygium malaccense (L.) Merr. & Perry]. Flavour Fragrance J. 19, 3235. Reynertson, K.A., Yang, H., Jiang, B., Basile, M.J., Kennelly, E.J., 2008. Quantitative analysis of antiradical phenolic constituents from fourteen edible Myrtaceae fruits. Food Chem. 109, 883890. Sankat, C.K., Basanta, A., Maharaj, V., 2000. Light mediated red colour degradation of the pomerac (Syzygium malaccense) in refrigerated storage. Postharvest Biol. Technol. 18, 253257. Wong, K.C., Lai, F.Y., 1996. Volatile constituents from the fruits of four Syzygium species grown in Malaysia. Flavour Fragrance J. 11, 6166.
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Jambolan—Syzygium jambolanum Luiz B. de Sousa Sabino1, Edy Sousa de Brito2 and Ivanildo J. da Silva Ju´nior1 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Anthocyanins Biological Properties of Jambolan
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Sensory Characteristics Harvest and Postharvest Conservation Industrial Application and Potential Industrial Application References Further Reading
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CULTIVAR ORIGIN AND BOTANICAL ASPECTS Syzygium cumini (L.) Skeels is a tree belonging to the Myrtaceae Family, originally from India and widely distributed in Asian countries such as Malaysia, Thailand, and the Philippines. The plant was introduced in many countries in the African continent and in Latin America where it easily adapted to the tropical and subtropical climate (Grover et al., 2002; Mahmoud et al., 2001). Due to its geographic dispersion different synonyms and popular nominations can be used to designate the S. cumini species. The main names given to S. cumini species are listed in Table 1. The S. cumini tree (Fig. 1A) is broad and densely foliated, reaching a height of 15 m and a crown diameter of 4 m. The immature bark is light brown, while the mature is dark brown and scaly. The leaves (Fig. 1B) are 612 cm long, leathery, dark green, smooth, shiny and elongate or oblong shape. The flowers (Fig. 1C) are small (712 mm), numerous, fragrant, white, creamy or greenish. It does not present stems and born in fascicles in the branches of the tree (Warrier et al., 1996). The jambolan fruits (Fig. 1D) are berries, fleshy, elliptically shaped and composed of a single dark brown central seed. Its length varies from 1.5 to 3.5 cm and are 2 cm in diameter. The fruits can be found in groups of 420 in different parts of the tree canopy (Baliga et al., 2011; Ayyanar and Subash-Babu, 2012).
HARVEST SEASON The jambolan harvest begins after 910 years of planting. The fruits show maturity after flowering, period of 35 months, depending on the climate of the region and the cultivar (AGRIFARM, 2014; FRUITIPEDIA, 2013). In northern Asia, e.g., flowering begins in March and continues in April and full fruit ripening occurs between June and July, while in Brazil the flowering occurs from September to November and the ripe fruit from December to February (Danadio et al., 1998; Ross, 1999; Alberton et al., 2001). The jambolan is a nonclimacteric fruit and should be harvested at the appropriate stage of maturity, indicated mainly by the complete development of the epicarp coloration. Due to nonuniform maturation time, more than one harvest is necessary (FRUITIPEDIA, 2013). If not harvested, the fruits fall or, due to the attractive color and aroma, are eaten by bats, squirrels, and monkeys (Warrier et al., 1996).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Fruit development takes about 2 months, and it is a process marked by intense changes in its physiological characteristics resulting from the synthesis of new compounds. The remarkable physical change associated with the chemical and Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00032-0 © 2018 Elsevier Inc. All rights reserved.
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TABLE 1 Scientific and Popular Names Used to Designate Syzygium cumini Species Languagea
Names
Scientific names
Eugenia jambolana Lam., Myrtus cumini Linn., Syzygium jambolana DC., Syzygium jambolanum (Lam.) DC., Eugenia djouant Perr., Calyptranthes jambolana Willd., Eugenia cumini (Linn.) Druce., and Eugenia caryophyllifolia Lam
Popular namesb
Jambola˜o, jamun, jamblon, jambolana, jamoon, black plum, blackberry, jamela˜o, jala˜o, azeitona-roxa, murta, jambuı´, oliva, oliveira, java plum, portuguese plum, malabar plum, purple plum, damson plum, jaman, jambu, jambool, jambhool, jamelong, jamblang, jiwat, salam, jambeiro
a
Sharma et al. (2006), Grover et al. (2002), Timbola et al. (2002), Garcia et al. (2003), Veigas et al. (2007), Ayyanar and Subash-Babu (2012). Popular names including: Indian, English and Portuguese language.
b
FIGURE 1 (A) Tree, (B) leaves, (C) flowers, and (D) fruit of Syzygium cumini (L.) Skeels.
biochemical processes that occur in the fruit is the evolution of the color of its pericarp due to the anthocyanin synthesis. When immature, the fruit exhibits white pericarp and it turns dark purple or black with maturation. In the physiological maturity, the mesocarp becomes purple, fleshy, juicy and with an exotic flavor resulting from the combination of sweetness, acidity and light astringency. The astringency occurs due tannins and other phenolic present (Alberton et al., 2001; Benherlal and Arumughan, 2007; Jadhav et al., 2009).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Jambolan has a complex chemical composition rich in different chemical compounds with nutritional and biological value. In the fruit are found carbohydrates such as sucrose, mannose, glucose, fructose, galactose, and maltose; water soluble vitamins such as thiamine and niacin; the free amino acids: alanine, asparagine, tyrosine, glutamine and cysteine; minerals: sodium, potassium, calcium, phosphorus, iron, and zinc; oxalic and malic acid. The concentration of the compounds is variable depending, e.g., on soil nutrition, climatic conditions and harvesting techniques employed in the cultivation (Jadhav et al., 2009; Sari et al., 2009; Baliga et al., 2011; Ayyanar and Subash-Babu, 2012). The approximate chemical composition of jambolan is present in Table 2. Different phenolic compounds are present as constituents of the jambolan and these substances are responsible for the color and flavor characteristic of the fruit. Phenolic acids, flavones, and flavonoids such as gallic acid, myricetin, and anthocyanins, respectively, are examples of phenolic classes present in the fruit composition (Mercadante et al., 2011). Anthocyanins are an important subclass of flavonoids responsible for the coloring and different biological properties of jambolan (Baliga et al., 2011) which makes these substances subject to different studies (Pallavi et al., 2012; Tsuda, 2012; Algarra et al., 2014). In addition to the previously reported components, the fruits may have essential oils such as α-pinene, camphene, β-pinene, myrcene, and cis-ocimene (Ayyanar and Subash-Babu, 2012).
Anthocyanins The profile of anthocyanins that compose the jambolan is marked by the presence of different aglycones linked to a common 3,5-diglycoside. Five of the six aglycones commonly found in foods can be found in this fruit, corresponding
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TABLE 2 Chemical Composition of Jambolan Fruit Composition
Contenta
Moisture
77.2 g/100 g
Protein
1.4 g/100 g
Fat
0.6 g/100 g
Fiber
0.6 g/100 g
Carbohydrates
16.6 g/100 g
Sucrose
95.5 mg/g
Maltose
210 mg/g
Fructose
57.5 mg/g
Galactose
52.5 mg/g
Vitamins β-Carotene
50 mg/100 g
Thiamine
0.12 mg/100 g
Riboflavin
0.06 mg/100 g
Ascorbic acid
30 mg/100 g
Minerals Na
3.5 mg/100 g
K
130 mg/100 g
P
18.5 mg/100 g
Ca
21.5 mg/100 g
Fe
0.15 mg/100 g
Mg
49.8 mg/100 g
Zn
0.28 mg/100 g
Cu
0.07 mg/100 g
a
Results obtained from Noomrio and Dahot (1996) and Paul and Shaha (2004).
to anthocyanins derived from cyanidin, delphinidin, malvidin, peonidine, and petunidine. In general, these anthocyanins have different amounts in plants from different cultivars (Mercadante et al., 2011; Ayyanar and Subash-Babu, 2012; Sari et al., 2012). According to Kong et al. (2003) 50% of the anthocyanins present in fruits and vegetables correspond to cyanidin3,5-diglycoside, and it is the major anthocyanin in fruits such as strawberry, jaboticaba, blackberry, and jambolan (Mazza and Miniati, 1993). Delphinidin, occurring in 12% of the plants and its 3,5-diglycoside form, has already been pointed out as predominant in the jambolan harvested in Brazil, while malvidin glycosides were reported as predominant in the fruits harvested in India (Kong et al., 2003; Veigas et al., 2007; Brito et al., 2007; Mercadante et al., 2011). Studies have pointed out that the content of anthocyanins found in jambolan was higher than that of vegetables such as grapes and red cabbage, known as sources of these substances (Giusti and Wrolstad, 2001; Sari et al., 2009). In this context, it can be stated that jambolan is a natural source of anthocyanins, which may be an important attribute due to the benefits related to the ingestion of these compounds.
Biological Properties of Jambolan Different studies have indicated that the ingestion of the jambolan presents health beneficial effects due to the pronounced pharmacological effects of extracts obtained from the fruit. Antiviral activities (Bhanuprakash et al., 2008),
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antioxidants (Veigas et al., 2007), gastroprotective (Chaturvedi et al., 2007), hepatoprotective (Veigas et al., 2008), and anticancer (Barh and Viswanathan, 2008) effects are reported in the literature on the different extracts obtained from jambolan fruit, however, an emphasis has been given to the antidiabetic action of this fruit, which leads to the development of different studies (Grover et al., 2000; Arayne et al., 2007). These and other biological properties reported to jambolan are related to the various phytochemicals present in its constitution such as anthocyanins and other polyphenols (Baliga et al., 2011).
SENSORY CHARACTERISTICS Jambolan is an exotic fruit with a remarkable sensory characteristic. The synthesis of compounds that occur during maturation has a direct impact on the taste, color, and aroma of the fruit. The flavor is the result of the association of sugars, organic acids, and phenolics, while the aroma is related to the last two compounds. The jambolan does not present a high sweetness and this fact is due to the high concentration of maltose in its composition in contrast to the other sugars. The acidity of the fruits is given by the malic, citric, and mostly by gallic acid. The hydrolysis of these acids, together with phenolics and carotenoids, generate volatile compounds responsible for the aroma (Ayyanar and Subash-Babu, 2012). The tannins confer astringency to the pulp of the fruit. The intensity of the astringency can contribute to the development of an unpleasant taste, however in the mature fruit, the association of tannins with sugars and acids reduces the intensity of the astringency and gives to the fruit the exotic flavor. As previously reported (see “Fruit Physiology and Biochemistry” and “Chemical Composition and Nutritional Value” sections) the typical jambolan color is conferred by the different anthocyanins present. Cultivation issues will influence the quality of the aglycone and consequently the different shades presented by the fruits. Besides, the coloring anthocyanins will contribute to the development of the flavor due to its catabolism in the respiratory processes of the fruit.
HARVEST AND POSTHARVEST CONSERVATION Jambolan is considered a perishable fruit especially for the fragility of its pulp and epicarp that offers little protection against physical damages or infectious agents. However, special care in harvesting and postharvesting is essential to extend the shelf-life of the fruit. Under environmental conditions the shelf-life of jambolan is 2 days. Refrigerated storage and moisture control are postharvest practices that are commonly applied to vegetables and may be allied to reduce perishability due to the reduction of catabolic reactions resulting from respiration. Temperatures of 810 C and an atmosphere with relative humidity of 85%95% showed positive effects extending the shelf-life of jambolan to three weeks. The use of modified atmospheres reduces gas exchanges and slows down degradation processes. Da Silva et al. (2017) indicated that polyvinyl chloride films associated with storage at 5 C kept jambolan quality for 10 days, preventing the incidence of rot in this period. In general, a high waste percentage is still seen in the harvest of the jambolan mainly due to the lack of investments and appreciation (Lago et al., 2006).
INDUSTRIAL APPLICATION AND POTENTIAL INDUSTRIAL APPLICATION Both the rind and the flesh of jambolan is a consumed, resulting in approximately 80% of the total of the fruit being edible (Shajib et al., 2013). In general, the final destination is different in each location. In Brazil, e.g., the tree has a domestic origin and the fruit is consumed almost in natura and there is no evidence as to the use of the fruit as an industrial raw material. In Asia the fruit is commonly processed and found in the form of juices, pulps, and jellies. In parts of India, jambolan pulp is used to make wine and the immature fruit serves as a base for the manufacture of vinegar, which according to local culture is a potent antidiuretic (Banerjee et al., 2005). Dried fruits are considered delicacies, finding a market in the United States and in several European countries (Veigas et al., 2007). Considering the nutritional and biological aspects previously reported, there is a great potential for the industrialization of jambolan both in the food and pharmaceutical sectors. However, what is observed is that, independently of the producing region, the lack of investments in technologies for the postharvest handling of the jambolan results in high rates of waste, not stimulating the cultivation and commercialization of the jambolan.
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REFERENCES AGRIFARM, 2014. Jamun farm information (Indian Black plum). Available at: ,http://www.agrifarming.in/jamun-farming/.. (accessed04.04.17.). Alberton, J.R., RIbeiro, A., Sacramento, L.V.S., Franco, S.L., 2001. Caracterizac¸a˜o farmacogno´stica do jambola˜o (Syzygium cumini (L.) Skeels). Rev. Bras. Farmacogn. 11, 3750. Algarra, A.M., Fernandes, A.B., Nuno Mateus, B., De Freitas, V.B., Joaquim, C.G., Da Silva, E.B., et al., 2014. Anthocyanin profile and antioxidant capacity of black carrots (Daucus carota L. ssp. sativus var. atrorubens Alef.) from Cuevas Bajas, Spain. J. Food Compos. Anal. 33, 7176. Arayne, M.S., Sultana, N., Mirza, A.Z., Zuberi, M.H., Siddiqui, F.A., 2007. In vitro hypoglycaemic activity of methanolic extract of some indigenous plants. Pak. J. Pharm. Sci. 20, 268273. Ayyanar, M., Subash-Babu, P., 2012. Syzygium cumini (L.) Skeels: a review of its phytochemical constituents and traditional uses. Asian Pacific J. Trop. Biomed. 2, 240246. Baliga, M.S., Bhat, H.P., Baliga, B.R.V., Wilson, R., Palatty, P.L., 2011. Phytochemistry, traditional uses and pharmacology of Eugenia jambolana Lam. (black plum): a review. Food Res. Int. 44, 17761789. Banerjee, A., Dasgupta, N., De, B., 2005. In vitro study of antioxidant activity of Syzygium cumini fruit. Food Chem. 90, 727733. Barh, D., Viswanathan, G., 2008. Syzygium cumini inhibits growth and induces apoptosis in cervical cancer cell lines: a primary study. Ecancermedicalscience. 2, 83. Benherlal, P.S., Arumughan, C., 2007. Chemical composition and in vitro antioxidant studies on Syzygium cumini fruit. J. Sci. Food Agric. 87, 25602569. Bhanuprakash, V., Hosamani, M., Balamurugan, V., Gandhale, P., Naresh, R., Swarup, D., et al., 2008. In vitro antiviral activity of plant extracts on goatpox virus replication. Indian J. Exp. Biol. 46, 120127. Brito, E.S., Arau´jo, M.C.P., Alves, R.E., Carkeet, C., Clevidence, B.A., Novotny, J.A., 2007. Anthocyanins present in selected tropical fruits: acerola, jambola˜o, jussara, and guajiru. J. Agric. Food Chem. 55, 93899394. Chaturvedi, A., Kumar, M.M., Bhawani, G., Chaturvedi, H., Kumar, M., Goel, R.K., 2007. Effect of ethanolic extract of Eugenia jambolana seeds on gastric ulceration and secretion in rats. Indian J. Physiol. Pharmacol. 51, 131140. Da Silva, M., Radaelli, J.C., Porto, H.P., Stefeni, A.R., Junior, A.M., 2007. Temperature and modified atmosphere in postharvest jambolao conservation. Int. J. Agric. Environ. Res. 03, 22042212. Danadio, L.C., Nachtigal, J.C., Sacramento, C.K., 1998. Frutas exo´ticas. Funep, Jaboticabal. FRUITIPEDIA, 2013. Jamun (Syzigium cumuni). Available at: ,http://www.fruitipedia.com/jamun.htm/. (accessed 04.04.17.). Garcia, C.G., Polo, A.S., Iha, N.Y.M., 2003. Photoelectrochemical solar cell using extract of, Eugenia jambolana Lam as a natural sensitizer. An. Acad. Bras. Cieˆnc. 75, 163165. Giusti, M.M., Wrolstad, R.E., 2001. Characterization and measurement of anthocyanins by UVvisible spectroscopy. In: Wrolstad, R.E., Acree, T.E., Decker, E.A., Penner, M.H., Reid, D.S., Schwartz, S.J., Shoemaker, C.F., Smith, D., Sporns, P. (Eds.), Handbook of Food Analytical Chemistry: Pigments, Colorants, Flavors, Texture, and Bioactive Food Components. John Wiley & Sons Inc, New Jersey, NJ, pp. 1931. Grover, J.K., Vats, V., Rathi, S.S., 2000. Anti-hyperglycemic effect of Eugenia jambolana and Tinospora cordifolia in experimental diabetes and their effects on key metabolic enzymes involved in carbohydrate metabolism. J. Ethnopharmacol. 73, 461470. Grover, J.K., Rathi, S.S., Vats, V., 2002. Amelioration of experimental diabetic neuropathy and gastropathy in rats following oral administration of plant (Eugenia jambolana, Mucuna pruriens and Tinospora cordifolia) extracts. Indian J. Exp. Biol. 40, 273276. Jadhav, V.W., Kamble, S.S., Kadam, V.J., 2009. Herbal medicine: Syzygium cumini: a review. J. Pharm. Res. 2, 12121219. Kong, J.M., Chia, L.S., Goh, N.K., Chia, T.F., Brouillard, R., 2003. Analysis and biological activities of anthocyanins. Phytochemistry. 64, 923933. Lago, E.S., Gomes, E., Da-Silva, R., 2006. Produc¸a˜o de gele´ia de jambola˜o (Syzygium cumini Lamarck): processamento, paraˆmetro fı´sico-quı´micos e avaliac¸a˜o sensorial. Cieˆnc. Tecnol. Aliment. 26, 847852. Mahmoud, I.I., Marzouk, M.S., Moharram, F.A., El-Gindi, M.R., Hassan, A.M., 2001. Acylated flavonol glycosides from Eugenia jambolana leaves. Phytochemistry. 58, 12391244. Mazza, G., Miniati, E., 1993. Anthocyanins in Fruits, Vegetables and Grains. CRC Press, Boca Raton, FL. Mercadante, A.Z., Faria, A.F., Marques, M.C., 2011. Identification of bioactive compounds from jambola˜o (Syzygium cumini) and antioxidant capacity evaluation in different pH conditions. Food Chem. 126, 15711578. Noomrio, M.H., Dahot, M.U., 1996. Nutritive value of Eugenia jambosa fruit. J. Islamic Acad. Sci. 9, 912. Pallavi, R., Elakkiya, S., Tennety, S.S.R., Devi, P.S., 2012. Anthocyanin analysis and its anticancer property from sugarcane (Saccharum officinarum L.) peel. Int. J. Res. Pharm. Chem. 2, 338345. Paul, D.K., Shaha, R.K., 2004. Nutrients, vitamins and mineral content in common citrus fruits in the northern region of Bangladesh. Pak. J. Biol. Sci. 7, 238242. Ross, I.A., 1999. Medicinal Plants of the World: Chemical Constituents, Traditional and Modern Uses. Human, Totowa. Sari, P., Wijaya, C.H., Sajuthi, D., Supratman, U., 2009. Identification of anthocyanins in jambolan (Syzygium cumini) fruit by high performance liquid chromatographydiode array detection. J. Food Technol. Ind. 20, 102108. Sari, P., Wijaya, C.H., Sajuthi, D., Supratman, U., 2012. Colour properties, stability, and free radical scavenging activity of jambolan (Syzygium cumini) fruit anthocyanins in a beverage model system: natural and copigmented anthocyanins. Food Chem. 132, 19081914. Shajib, M.T.I., Kawser, M., Miah, M.N., Begum, P., Bhattacharjee, L., Hossain, A., et al., 2013. Nutritional composition of minor indigenous fruits: cheapest nutritional source for the rural people of Bangladesh. Food Chem. 140, 466470.
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Sharma, S.B., Nasir, A., Prabhu, K.M., Murthy, P.S., 2006. Antihyperglycemic effect of the fruit-pulp of Eugenia jambolana in experimental diabetes mellitus. J. Ethnopharmacol. 104, 367373. Timbola, A.K., Szpoganicz, B., Branco, A., Monache, F.D., Pizzolatti, M.G., 2002. A new flavonol from leaves of Eugenia jambola. Fitoterapia. 73, 174176. Tsuda, T., 2012. Dietary anthocyanin-rich plants: biochemical basis and recent progress in health benefits studies. Mol. Nutr. Food Res. 56, 59170. Veigas, J.M., Narayan, M.S., Laxman, P.M., Neelwarne, B., 2007. Chemical nature, stability and bioefficacies of anthocyanins from fruit peel of Syzygium cumini Skeels. Food Chem. 105, 619627. Veigas, J.M., Shrivasthava, R., Neelwarne, B., 2008. Efficient amelioration of carbon tetrachloride induced toxicity in isolated rat hepatocytes by Syzygium cumini Skeels extract. Toxicol. In Vitro. 22, 14401446. Warrier, P.K., Nambiar, V.P.K., Ramankutty, C., 1996. Indian Medicinal Plants. Orient Longman Ltd, Hyderabad.
FURTHER READING Oliveira, L.C., Bloise, M.I., 1995. Extratos e o´leos naturais vegetais funcionais. Cosmet. Toiletries. 7, 3037. Pepato, M.T., Mori, D.M., Baviera, A.M., Harami, J.B., Vendramini, R.C., Brunetti, I.L., 2005. Fruit of the jambolan tree (Eugenia jambolana Lam.) and experimental diabetes. J. Ethnopharmacol. 96, 4348.
Jatoba—Hymenaea courbaril Gustavo Schwartz Embrapa Eastern Amazon, Bele´m, Para, Brazil
Chapter Outline Species Origin, Ecology, Botany, and Socioeconomic Importance Harvest Season Estimated Annual Production and Harvest/Postharvest Conservation
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Fruit Physiology, Biochemistry, Chemical Composition, and Nutritional Value Sensory Characteristics Industrial Application or Potential Industrial Application References
260 260 260 261
SPECIES ORIGIN, ECOLOGY, BOTANY, AND SOCIOECONOMIC IMPORTANCE Jatoba (Hymenaea courbaril L.) is a tree species of the family Fabaceae. The species is also known as Jutai-acu (Brazil), guapinol (Mexico and Central America), courbaril (Peru and Ecuador), algarrobo (Colombia and Venezuela), locust (Belize and Guyana), and rode lokus (Suriname). H. courbaril is the biggest species belonging to the genus Hymenaea. It has a straight stem that, on average, reaches 40 m in height and 1 m in diameter (Cavalcante, 2010). In some cases, as observed in the primary tropical forests of the Amazon, old trees of jatoba can attain more than 50 m in height and 2 m in diameter. The species has alternate leaves composed by two leaflets (De Souza et al., 1997) and during its seedling stage growths similar to a liana (Fig. 1). A wide geographical distribution is characteristic of jatoba. The species is distributed over the tropical regions of South America, Central America, and south Mexico. In these areas, jatoba is naturally found from lowland tropical forests up to 900 m in altitude, usually in clay soils. In the natural environments of jatoba, the annual precipitation varies between 1,500 and 3,000 mm (De Melo and Mendes, 2005). In the Amazon, the natural populations of jatoba found in primary forests present very low numbers of individuals. Based on its ecological feature of having no more than one adult tree per hectare, it is possible to consider H. courbaril a rare species (Schwartz et al., 2014). Several products from jatoba have been used for many purposes. From the jatoba’s fruits one can prepare cookies and, from its high value timber, furniture and canoes are made. The species has also been used for environmental purposes in order to restore native forests or areas that demand protection through forest covering. Trees of jatoba have a large and superficial root system, which naturally makes associations with the Rhizobium bacteria to fix atmospheric nitrogen in the soil. They are also able to grow and develop well over poor soils. Due to these two features, jatoba is recommended to be planted for recovering degraded lands. The nutritive and sweet fruits of jatoba attract a lot of animals from the native fauna such as tapirs, capuchin monkeys, pacas, and agoutis. The attracted animals can work as seed dispersers when they drop or bury jatoba’s seeds elsewhere far from the mother tree. Hence, these animals have the key function of dispersing seeds of jatoba. Furthermore, once attracted by jatoba, the animals can also disperse seeds of neighboring trees belonging to other species. This is essential in the recovery of degraded lands and conservation of the native flora. In the Amazon region, the main commercial use of jatoba is for timber production. In these forests, the harvested trees of jatoba are at least 50 cm in diameter and produce high volumes of timber. The jatoba’s timber is heavy and hard (density from 0.80 to 1.00 g/cm3) and its timber core varies in color from red to light-brown. The jatoba’s timber is used to make doors, windows, painting frames, boats, and house interiors as well as to craft furniture and musical instruments. Jatoba trees exude, from their stems, branches, roots, and the fruit pericarp, a transparent brown-yellowish resin or gum, named copal or jutaicica (De Melo and Mendes, 2005; Ferreira and Sampaio, 2015). This resin can also Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00033-2 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Seedling of jatoba (Hymenaea courbaril) planted in its natural habitat showing its alternate leaves composed by two leaflets. Source: Photo by Gustavo Schwartz.
be collected from the soil close to the trunk. This kind of collection is possible because part of the resin is exuded by the roots, so the resin remains buried in the soil. The resin produced by jatoba’s trees is mainly used to manufacture varnish. It is also used as incense as well as to coat canoes to make them waterproof. H. courbaril is a medicinal plant with a well popular acceptance for the treatment of several health problems (Souza et al., 2014). It was showed that the species has an antiviral activity against rotavirus (Cecı´lio et al., 2012). The jatoba’s bark has medicinal properties that allow it to work as an expectorant and for wound healing. The bark is also popularly used to treat headache, general pain, and inflammation (De Souza et al., 1997). Like bark, the leaves of jatoba also have medicinal properties, when prepared as a tea they are used to treat colds and bronchitis (Embrapa, 2004). However, these leaves contain terpenes, tannins, and glycosides, which permits its usage as a fungicide and repellent against some agricultural plagues such as leaf-cutter ants and caterpillars. Like its timber, bark, and leaves, the fruits produced by jatoba are also appreciated. Its edible pulp is consumed fresh or used to prepare flour used in cookies and snacks for humans. Both the pulp and seeds of jatoba are also used to feed livestock (Ferreira and Sampaio, 2015). Fruits of jatoba have a subcylindrical shape. They are covered by the exocarp, a brownish, woody, and sometimes slightly shiny pod measuring 0.7 cm in thickness (Fig. 2). Like the leaves, the pods are rich in terpenes (Nogueira et al., 2001) with potential use as an insect repellent. The jatoba’s fruits are classified as indehiscent, which means that they do not split open at maturity. The pods measure 815 cm in length, 36 cm in diameter, and are 90300 g in weight (De Andrade et al., 2010). The jatoba’s fruits are composed by pods (50%70%), pulp (5%10%), and seeds (25% 40%). Each fruit contains one to eight seeds, brown colored, hard, flat, and with a nearly ellipsoid shape (Fig. 2). The jatoba’s seeds are 2.1 cm in length, 1.6 cm in diameter, and weigh 2.9 g (nearly equal to 350 seeds/kg) on average (Cruz and Pereira, 2015; Ferreira and Sampaio, 2015). In the endocarp of the jatoba’s fruits there is an edible pulp. This pulp is composed of a yellow-greenish powder that involves each seed. The pulp of the jatoba’s fruits can be eaten fresh or used to prepare jelly, liquor, bread, cream,
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FIGURE 2 Closed and open fruits of jatoba (Hymenaea courbaril), its edible pulp and seeds. Source: Photo by Gustavo Schwartz.
or flour. The flour made from pulp has several usages for humans. With this flour it is possible to prepare cookies. It can be also mixed with wheat flour and brown sugar to prepare other kinds of cookies (Silva et al., 2001). It is reported that, from the pulp, one can prepare a sweet beverage.
HARVEST SEASON The harvest season of H. courbaril varies along the year according to the different climates present in the wide geographical area where the species is distributed. Flowering of jatoba trees is observed at the end of the rainy season and the fruit production usually occurs four months later (Cavalcante, 2010). The jatoba’s flowers are white and open at night, which indicates that they are pollinated by bats. The fruit production occurs in part or along the whole dry season. In the eastern Amazon, jatoba’s trees produce fruits from August to October. Due to differences in climate, in the central Amazon they produce in AugustSeptember while in the western Amazon, jatoba’s trees produce fruits from May to September (Shanley and Schulze, 2010). There is no specific harvest season to collect resin from the stems or buried in the soil.
ESTIMATED ANNUAL PRODUCTION AND HARVEST/POSTHARVEST CONSERVATION Fruit production normally begins when the jatoba trees reach the age of 812 years. An adult tree, 10 years old, is able to produce 1,0002,000 fruits or 50100 kg of fruits per year (Ferreira and Sampaio, 2015). However, the production of jatoba’s fruits is not constant over the years. The trees have peaks of fruit production each 2 or 4 years. In the nonpeak production years, the number of fruits per tree strongly decreases. Moreover, there is a great variation in the number of fruits produced by different trees placed in the same area. There is still little information available on the resin production from stems of H. courbaril. Field reports say that it is possible to collect up to 15 kg of resin buried around the trunk of a big jatoba tree. Trees of jatoba are naturally found in low densities inside tropical forests within the species geographical distribution. An effective way to increase the fruit production is to have more trees per unit of area in the native forest, the
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place where jatoba occurs. The increase of jatoba’s populations can be done through the silvicultural treatment of assisted densification (Schwartz and Lopes, 2015). This treatment consists in planting jatoba seedlings or seeds in the species’ natural environment. The planting can also be done in open areas, degraded or secondary forests (De Souza et al., 2010). The species should merely be better studied in terms of genetic improvement to increase the fruit’s production and percentage of pulp. There is still no scientific literature on the harvest and postharvest conservation of the jatoba’s fruits. Reports from popular open markets in the Amazon say that the fruits can be stored for some weeks, because the thick pod stays closed. Thus the powder pulp can remain edible for such time. Scientific information is also not available on the conservation of the pulp after detached from the pod and seeds.
FRUIT PHYSIOLOGY, BIOCHEMISTRY, CHEMICAL COMPOSITION, AND NUTRITIONAL VALUE The major chemical compounds of the pulp, the only edible component of the jatoba’s fruits, are sucrose and linolenic acid. Fruits of H. courbaril have a strong role to inhibit the activities of the cyclooxygenase (COX) enzymes and lipid peroxidation. The two enzymes, COX-1 and COX-2, catalyze a rate-limiting step in the synthesis of prostaglandin, which is related to inflammation (Jayaprakasam et al., 2007). The pharmaceutical inhibition of the COX enzymes, found in the jatoba’s pulp, can contribute to alleviate symptoms of inflammation and pain. Within the important functional components for the human health present in the jatoba’s pulp there are the crude fibers. They are the main component of the pulp, the edible part of the fruit (Silva et al., 2001). These fibers are important for the human organism to stimulate the growth of intestinal flora. More than a half of the pulp is composed of crude fibers (50.02%), followed by carbohydrates (32.20%), protein (12.32), ash (4.53%), and lipids (1.94%). The pulp of the jatoba’s fruits is a rich source of minerals due to its high ash content (Dias et al., 2013). The mineral components of the pulp (mg/100 g), according to Dias et al. (2013) are sodium (468.15), potassium (229.40), phosphorus (137.60), magnesium (99.15), calcium (57.39), manganese (7.62), copper (2.07), iron (1.75), boron (1.32), zinc (1.14), and selenium (0.27). Besides these macro and micronutrients, 100 g of the pulp of the jatoba’s fruits contains 121.5 mg of vitamin C. Humans need 7590 mg of vitamin C per day, and the pulp of jatoba can provide more than this amount (Dias et al., 2013). In terms of energy, 100 g of pulp of the jatoba’s fruits has 115 kcal.
SENSORY CHARACTERISTICS Pulp is the only edible part of the jatoba’s fruits, it can be eaten fresh or prepared as a flour that will become other products. The pulp has a good sweet taste but with an unappetizing and nonattractive smell (De Souza et al., 1997; Dias et al., 2013). The pulp is naturally dry (see Fig. 2) and largely starchy, which brings the sensorial feeling of eating flour. Because of this feature, the pulp is largely used as a source to prepare flours.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Besides the wide use of the jatoba’s timber from the Amazon in the industry as well as its seeds by artisans for handicraft (Matuda and Maria Netto, 2005), there is a potential use of its fruits’ pulp in the food industry. Due to the flourlike endocarp, the pulp of the jatoba’s fruits can be used in the formulation of extruded snacks in order to reach a more palatable taste in the food. It can also be used to enrich foods with fibers (Chang et al., 1998). Having high levels of total dietary fibers as well as other healthy nutritional features means that the pulp of the jatoba’s fruits has a great potential in the food industry. The current main problem for the jatoba’s pulp to increase its participation in the food industry is its low and unpredictable production. Different from its timber, mainly harvested in the Brazilian Amazon, markets for the jatoba’s fruits are weak. There are still no firmly established production chains for these fruits, which are not easily found for sale. Fruits are hardly found in a few open markets located in the production regions during the fruit production period. Commercial plantations of H. courbaril aiming fruit production would strengthen markets and food industry for this species. H. courbaril can be used not only in the timber and food industries, but also in the pharmaceutics and cosmetics industries. Based on results presented by Dias et al. (2013), α-tocopherol, β-sitosterol, oleic and linoleic acids are the most abundant bioactive substances found in oils from pulp and seeds of jatoba. The authors therefore suggest the lipid from both pulp and seed’s oil should be explored by the food, pharmaceutics, and cosmetic industries.
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There is the potential of the industries linked to the food conservation and agricultural defensives. Pulp of the jatoba’s fruits shows the potential to be applied in the food conservation industry. It has an inhibitory activity against the bacterium Escherichia coli (Tamayo et al., 2011). The jatoba’s pulp also showed to be more attractive to leaf-cutter ants than the dehydrated citric pulp, the most commercially used substance for such purpose (Teixeira and Santos, 2008). Pods of jatoba have sesquiterpenes with an effective larvicidal activity (Aguiar et al., 2010). These are indications on the potential of both pods and pulp to be used in the industry to control leaf-cutter ants, caterpillars, and pathogens related to agricultural crops.
REFERENCES Aguiar, J.C., Santiago, G.M., Lavor, P.L., Veras, H.N., Ferreira, Y.S., Lima, M.A., et al., 2010. Chemical constituents and larvicidal activity of Hymenaea courbaril fruit peel. Nat. Prod. Commun. 5, 19771980. Cavalcante, P.B., 2010. Frutas comestı´veis na Amazoˆnia. Museu Paraense Emilio Goeldi, Bele´m, 280 pp. Cecı´lio, A.B., De Faria, D.B., Oliveira, P.C., Caldas, S., de Oliveira, D.A., Sobral, M.E.G., et al., 2012. Screening of Brazilian medicinal plants for antiviral activity against rotavirus. J. Ethnopharmacol. 141, 975981. Cruz, E.D., Pereira, A.G., 2015. Germinac¸a˜o de sementes de espe´cies amazoˆnicas: jatoba´ (Hymenaea courbaril L.). Comunicado Te´cnico 263. Embrapa, Bele´m, 5 pp. Chang, Y.K., Silva, M.R., Gutkoski, L., Sebio, L., Silva, M.A.A.P., 1998. Development of extruded snacks using jatoba´ [Hymenaea stigonocarpa Mart] flour and cassava starch blends. J. Sci. Food Agric. 78, 5966. De Andrade, L.A., Bruno, R.L.A., De Oliveira, L.S.B., Da Silva, T.F., 2010. Aspectos biome´tricos de frutos e sementes, grau de umidade e superac¸a˜o de dormeˆncia de jatoba´. Acta Sci. Agron. 32, 293299. De Melo, M.G.G., Mendes, A.M.S., 2005. Jatoba´ Hymenaea courbaril L. Informativo Te´cnico Rede de Sementes da Amazoˆnia 9. On line URL: ,https://www.inpa.gov.br/sementes/iT/9_Jatoba.pdf. (accessed 20.10.15.). De Souza, A. das G.C., Sousa, N.R., Da Silva, S.E.L., Nunes, C.D.M., Canto, A. do C., Cruz, L.A de A., 1997. Fruit Trees of the Amazon Region. Embrapa, Brası´lia, 204 pp. De Souza, C.R., De Azevedo, C.P., Lima, R.M., Rossi, L.M.B., 2010. Comportamento de espe´cies florestais em plantios a pleno sol e em faixas de enriquecimento de capoeira na Amazoˆnia. Acta Amazonica. 40, 127134. Dias, L.S., Luzia, D.M.M., Jorge, N., 2013. Physicochemical and bioactive properties of Hymenaea courbaril L. pulp and seed lipid fraction. Ind. Crops Prod. 49, 610618. Embrapa, 2004. A Embrapa nos biomas brasileiros. Embrapa, Brası´lia, 16 pp. Ferreira, C.A.C., Sampaio, P.T.B., 2015. Jatoba´. FAO. Available at: ,http://www.fao.org/docrep/v0784e/v0784e0s.htm.. (accessed 22.10.15.). Jayaprakasam, B., Alexander-Lindo, R.L., DeWitt, D.L., Nair, M.G., 2007. Terpenoids from Stinking toe (Hymenaea courbaril) fruits with cyclooxygenase and lipid peroxidation inhibitory activities. Food Chem. 105, 485490. Matuda, T.G., Maria Netto, F., 2005. Caracterizac¸a˜o quı´mica parcial da semente de jatoba´-do-cerrado (Hymenaea stigonocarpa Mart.). Cieˆnc. Tecnol. Aliment. 25, 353357. Nogueira, R.T., Shepherd, G.J., Laverde Jr., A., Marsaioli, A.J., Imamura, P.M., 2001. Clerodane-type deterpenes from the seed pod of Hymenaea courbaril var. stilbocarpa. Phytochemistry. 58, 11531157. Schwartz, G., Lopes, J.C., 2015. Logging in the Brazilian Amazon forest: the challenges of reaching sustainable future cutting cycles. In: Daniels, J.A. (Ed.), Advances in Environmental Research, vol. 36. Nova, New York, NY, pp. 113137. Schwartz, G., Lopes, J.C., Kanashiro, M., Mohren, G.M., Pen˜a-Claros, M., 2014. Disturbance level determines the regeneration of commercial tree species in the Eastern Amazon. Biotropica. 46, 148156. Shanley, P., Schulze, M., 2010. Jatoba´, Hymenaea courbaril L. In: Shanley, P., Serra, M., Medina, G. (Eds.), Frutı´feras e plantas u´teis na vida amazoˆnica. Embrapa/Cifor, Bele´m, pp. 109117. Silva, M.R., Silva, M.S., Martins, K.A., Borges, S., 2001. Utilizac¸a˜o tecnolo´gica dos frutos de jatoba´-do-cerrado e jatoba´-da-mata na elaborac¸a˜o de biscoitos fontes de fibra alimentar e isentos de ac¸u´cares. Cieˆnc. Tecnol. Aliment. 21, 176182. Souza, R.K.D., Da Silva, M.A.P., De Menezes, I.R.A., Ribeiro, D.A., Bezerra, L.R., Souza, M.M.A., 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J. Ethnopharmacol. 157, 99104. Tamayo, L.M.A., Gonza´lez, D.M.A., Garce´s, Y.J., 2011. Evaluacio´n de usos potenciales del desecho del fruto del algarrobo (Hymenaea courbaril L) ca´scara y semillas como conservante natural para alimentos. Rev. Lasallista Invest. 8, 9095. Teixeira, M.L.F., Santos, M.N., 2008. Atratividade da isca granulada de polpa de fruto do jatoba´ para sau´va-lima˜o, no campo. Cieˆnc. Rural. 38, 907911.
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Jujuba—Ziziphus jujuba Xinwen Jin Institute of Food Science and Technology, XAARS, Shihezi City, Xinjiang Uygur Autonomous Region, P.R. China
Chapter Outline Cultivar Origin and Botanical Aspects Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Chemical Composition Nutritional Values Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Red Date (Dry Date)
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Candied Jujube (Honey Jujube) Spirited Jujube (“Drunk Jujube”) Smoked Jujube Roasted Jujube Jujube Jam Jujube Paste/Filling Reaching Additional Consumers Acknowledgments References
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CULTIVAR ORIGIN AND BOTANICAL ASPECTS The jujube originated in China where they have been cultivated for more than 4000 years and where there are over 400 cultivars. The plants traveled beyond Asia centuries ago and today are grown to some extent in Russia, northern Africa, southern Europe, the Middle East and the southwestern United States. Jujube seedlings, inferior to the Chinese cultivars, were introduced into Europe at the beginning of the Christian era and carried to the United States in 1837. It not until 1908 that improved Chinese selections were introduced by the USDA. Jujubes are species of the genus Ziziphus Tourn. ex L. The Zijihus belongs to the family Rhamnaceae named after the genus Rhamnus. The Rhamnaceae have fruits which are drupes or are dry and are closely related to another family, Vitaceae, which includes major economic species whose fruits are berries. The name Ziziphus is related to an Arabic word and ancient Greeks used the word ziziphon for the jujube. There are two major domesticated jujubes, Ziziphus mauritiana Lam. (the Indian jujube or ber), and Ziziphus jujuba Mill. (common jujube). These two species have been cultivated over vast areas of the world. The species has a wide range of morphologies from shrubs to small or medium sized trees which might be erect, semierect or spreading. Height can vary from 34 to 1016 m or more although trees of 20 m are rare. Trees are semideciduous and much branched. The bark has deep longitudinal furrows and is grayish brown or reddish in color. Usually the shrub or tree is spinous, but occasionally unarmed. Branchlets are densely white pubescent, especially when young and tend to be zigzag. Branches spread erect, becoming flexuous and dull brown gray. Fruiting branches are not deciduous. Leaf laminae are elliptic to ovate or nearly orbicular. The apex is rounded, obtuse or subacute to emarginated, the base rounded, sometimes cuneate, mostly symmetrical or nearly so. Margins are minutely seriate. There are three marked nerves almost to the apex, the nerves being depressed in the upper, light or dark green, glabrous surface. Lower surface is whitish due to persistent dense hairs but may be buff colored. Occasionally the lower surface is glabrous. Leaves are petiolate 1.15.8 mm long and stipules are mostly spines, in each pair one hooked and one straight, or both hooked, or more rarely developed into a spine. Flowers have sepals which are dorsally tomentose, a disk about 3 mm in diameter and a two-celled ovary, immersed in the disk. Styles are 2, 1 mm long and connate for half their length. Flowers tend to have an acrid smell. Flowers are borne in cymes or small axillary clusters. Cymes can be sessile or shortly pedunculate, peduncles 14 mm tomentose. Pedicels are also tomentose and are 24 mm at flowering and 36 mm at fruiting. Fruit is a glabrous globose or oval edible drupe varying greatly in size from 1 to 2 cm diameter but some oval varieties can reach 5 3 3 cm. The pulp is acidic and sweet, the fruit greenish yellow or sometimes reddish (Majumdar, 1945) (see also Figs. 13). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00034-4 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Jujube fruits from Xinjiang, P.R.C.
FIGURE 2 Jujube fruits on the tree.
FIGURE 3 Jujube fruits.
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ESTIMATED ANNUAL PRODUCTION The production of jujube has developed very rapidly in China and the annual production of jujube was 5,887,121 t in 2012.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Jujube fruit has an obvious peak of respiration and ethylene generation after postharvest. A 0 C temperature can reduce the intensity of respiration and release rate of ethylene and delay the appearance of the peak of respiration and ethylene generation. The respiration intensity and ethylene formation rate in early-picking fruit were higher than those in late-picking fruit. The increase of membrane permeability was accompanied by respiratory peak during the ripening of fruit. However, the fruit membrane permeability was lowest during the stage of turning color. The water loss in postharvest jujube fruit was extremely easy, and thus leads to the significant increase of respiration, ethylene and membrane permeability.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Chemical Composition Alkaloids Alkaloids are distributed in all parts of plant. The stem bark of Ziziphus species contains alkaloids (Pareek, 2001). A sapogenin, zizogenin has been isolated from Z. mauritiana stems (Srivastava and Srivastava, 1979). The cyclic peptide alkaloids, mauritine-A, mucronine-D, amphibine-H, nummularine-A and -B, sativanine-A and sativanine-B, frangulanine, nummularine-B and mucronine were isolated from the bark of Z. jujuba by (Tschesche et al., 1979). The cyclic peptide alkaloids sativanine-C, sativanine-G, sativanine-E, sativanine-H, sativanine-F, sativanine-D and sativanine-K isolated from Z. jujuba stem bark (Shah et al., 1985a). The alkaloids coclaurine, isoboldine, norisoboldine, asimilobine, iusiphine, and iusirine were isolated from Z. jujuba leaves by Ziyaev et al. (1977). Cyclopeptide and peptide alkaloids from Z. jujuba were found to show sedative effects (Han and Park, 1986). The seeds of Z. jujube var. spinosa also contain cyclic peptide alkaloids sanjoinenine, franguloine and amphibine-D and four peptide alkaloids; sanjoinine-B-D-F and -G2 (Han et al., 1990). The seeds are used in Chinese medicine as a sedative. Chemical studies of Z. mauritiana led to the isolation of the cyclopeptide alkaloids, mauritines A and B; C-F, G and H, frangufoline; amphibines D, E, B and F; hysodricanin-A, scutianin-F, and aralionin-C (Tschesche et al., 1979). The cyclopeptide alkaloid, mauritine J, was isolated from the root bark of Z. mauritiana (Jossang et al., 1996). For the first time, Tschesche et al. (1979) reported six cyclopeptide alkaloids isolated from the stem bark of Z. jujuba: Mauritine-A; Amphibine-H; Jubanine-A; Jubanine-B; Mucronine-D and Nummularine-B. Latterly, Shah et al. (1985a) reported the finding of sativanine-E. antibacterial peptide alkaloid. Frangufoline from Ziziphus species was reported (Devi et al., 1987). Han and coworkers (1990) reported melonovine-A; franganine; frangulanine; daechuine-S3; daechuine-S6; nummularine-A and nummularine-R, all cyclopeptide alkaloids. Four cyclopeptide alkaloids from the stem bark of Z. jujuba were are scutianine-C; scutianine-D; jubanine-C and ziziphine-A reported by Tripathi et al. (2001). Two reports appeared in the literature on isolated ingredients from the root bark of Z. jujuba. Adouetine-X and Frangulanine which are active (sedative) ingredient cyclopeptide alkaloids were isolated and characterized (Otsuka et al., 1974).
Glycosides The structure of spinosin (2v-O-beta-glucosylswertisin) extracted from Z. jujuba var. spinosa seed (Woo et al., 1979). They later identified three acylated flavone-C-glycosides(6w-sinapoylspinosin, 6w-feruloylspinosin and 6w-p-coumaroylspinosin), that pharmacologically have a sedative activity in rats. Different parts of Z. jujuba seeds, leafs and stem contain glycosides.
Saponins The saponins isolated from the seeds of Z. jujuba include jujubosides A, B (Zeng et al., 1987), A1, B1, C, and acetyljujuboside B (Yoshikawa et al., 1997), and the protojujubosides A, B, and B1 (Matsuda et al., 1999). Kurihara et al. (1988) extracted the saponin, ziziphin, from the dried leaves of Z. jujuba. Ikram et al. isolated a saponin from Z. jujuba leaves and stem.
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Flavonoids Sedative flavonoids such as Swertish and spinosin were isolated and reported by Cheng et al. (2000), from fruit and seeds of Z. jujuba: puerarin; 6w-feruloylspinosin; apigenin-6-C-b-D-glucopyranoside; 6w-feruloylisospinosin; isospinosin and isovitexin-2v-O-b-D-glucopyranoside. Ten flavonoids were reported by Pawlowska et al. (2000): Quercetine 3-O-robinobioside; Quercetine 3-O-rutinoside; Quercetine 3-O-α-L-arabinosyl-(1-2)-α-L-rhamnoside; Quercetine 3-O-b-D-xylosyl-(1-2)-α-L-rhamnoside; Quercetine 3-O-β-D-galactoside; Quercetine 3-O-β-D-glucoside; 30 ,50 -Di-Cβ-D-glucosylphloretin; Quercetine 3-O-β-D-xylosyl-(1-2)-α-L- hamnoside-40 -O-a-L-rhamnoside; Kaempferol 3-O-robinobioside and Kaempferol 3-O-rutinoside. Some of the representative flavonoids are described by Cheng et al. (2000) who discovered a new flavonoid, named zivulgarin.
Terpenoids The triterpenoic acids have been isolated from the fruits of Z. jujuba: some of them are colubrinic acid, alphitolic acid, 3-O-cis-p-coumaroylalphitolic acid, 3-O-transpcoumaroylalphitolic acid, 3-O-cis-p-coumaroylmaslinic acid, 3-O-transp-coumaroylmaslinic acid, oleanolic acid, betulonic acid, oleanonic acid, zizyberenalic acid and betulinic acid (Lee et al., 2003). Triterpenoic acids have also been extracted from roots of Z. mauritiana (Kundu et al., 1989). Betulin; betulinic acid; ursolic acid; 2α-hydroxyursolic acid and ceanothic acid are triterpenes reported by Shoei et al. (1996). Some of them have anticancer and anti-HIV properties. Sang et al. (2004) demonstrated three triterpene esters: 2-oprotocatechuoyl alphitolic acid, caffeoyl alphitolic acid and ceanothic aciddimethyl ester.
Phenolic Compounds Recently Pawlowska et al. (2000) reported phenolic compounds from the fruit of Z. jujuba, without citing any biological activity. Betulinic acid is widely distributed in all parts of the plant. It is a naturally occurring pentacyclic triterpenoid that has demonstrated selective cytotoxicity against a number of specific tumor types. It has been found to selectively kill human melanoma cells while leaving healthy cells alive. In addition, betulinic acid has been found to have antiinflammatory activity (Kim et al., 1998) and antibacterial properties and inhibits the growth of both Staphylococcus aureus and Escherichia coli (Eiznhamer and Xu, 2004).
NUTRITIONAL VALUES The desiccated fruit has been analyzed for nutritional qualities; per 100 g, it has: calories: 350; from fat, protein, carbohydrate as follows: protein: 7.3 g fat: 1.2 g carbohydrate: 84 g fiber: 4 g minerals, mainly the following of interest: ash: 3.0 g; potassium: 1050 mg phosphorus: 168 mg calcium: 130 mg sodium: 12 mg iron: 3.5 mg vitamins: about 0.5 g, mainly the following: vitamin C: 300 mg vitamin A: 125 mg niacin: 2.8 mg riboflavin: 0.2 mg thiamine: 0.1 mg. The fruit without water is 84% sugar, which explains its very sweet taste. In a serving of 10 g of desiccated fruit pulp (derived from about one half-ounce of edible dried fruit with the pit removed), the only significant nutrients for a modern diet would be 3.63.7 g of protein and 30 mg of vitamin C. It is interesting to note that the fruit yields relatively high amounts of cAMP and cGMP. The contents in dry fruit were 100500 nmol/g and 3050 nmoL/g, respectively. From the seed of Z. jujuba, three saponins of jujubosides A and B, and ziziphin were isolated. Furthermore, flavone C-glycosides swertisin and spinosin as well as the acylated derivatives of spinosin sinapoyl-, feruloyl- and coumaroylspinosin were also found in the seed.
HARVEST AND POSTHARVEST CONSERVATION As the fruit begins to mature, fruit color changes from dark green to yellowgreen, known as the creamy, white mature stage. As maturation continues, brown/red spots develop at the petiole end (where the fruit joins the stem) or randomly in the middle of the fruit. The color further changes to half red/half creamy, and eventually becomes fully red/brown, known as the fully mature stage. People often compare firm jujube fruit texture to that of a crispy apple. Several days after fully red, the fruit texture starts to soften and wrinkles appear on the surface. Fruit maturity is not uniform. Fresh-eating cultivars can be marketed from the white mature stage until they are fully red but still firm. Fresh fruit harvested when first ripe can be stored at 40 F (5 C) for 2 weeks or more without losing quality. The best time to harvest drying cultivars is when they are fully red. In New Mexico’s arid climate, fruits can be harvested when they start to wrinkle or can be left hanging on the trees for a while after wrinkling. In humid areas, fruits must be harvested when they are fully red in color and dried as soon as possible to avoid yeast or mold infection.
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Manual harvest is preferable for fresh-eating cultivars. For drying cultivars, growers in China lay tarps below trees and then shake the trees or use long poles to dislodge fruits. Mechanical harvest using trunk shakers may be applicable for production of large acreage of drying cultivars.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION When jujube fruits are close to maturity, their skin color turns from dark green to light green/creamy with high vitamin C content (white mature stage). The soluble solid content measures B20% for most cultivars. The fruit then changes color and become half cream/half red and eventually turn fully red/brown (crisp mature stage). At this stage, the fruit becomes crispy, sweet, and juicy with high sugar and acid content. The fruit skin gets thicker, harder, and easier to separate from the flesh after boiling. Fruit have the best fresh-eating quality at this point, but the vitamin C content starts to decrease. After that, the skin of the fruit will wrinkle and start to dehydrate and the flesh color near the kernel changes from greenish white to yellow/light brown and turns soft. Sugar and acid contents continue to increase, and vitamin C content continues to decrease (fully mature stage). Depending on the purpose, jujube fruit can be picked from the white mature stage, to the crisp mature stage, or the fully mature stage. Fresh-eating cultivars can be picked from the white mature stage until the crisp mature stage when the fruit texture is still firm.
Red Date (Dry Date) Red date is the dominant jujube product for the domestic and export markets in China. Fruits are picked when they are fully red or the fully mature stage because the more mature they are, the higher their sugar content and drying quality. After picking, fruits can be air-, sun-, or heat-dried. Heat drying is the optimal method because it retains more vitamin C, leads to better fruit quality, and avoids disease-related fruit losses. Red dates can be consumed directly as snacks; used in porridge, stew, soup, or tea; or processed further as jujube paste or other products. ‘‘Zongzi’’ is a traditional Chinese food that is consumed just before the Dragon Boat Festival to remember the patriotic poet, Qu Yuan. Red dates are placed in the middle of sweet rice, which is then wrapped by bamboo or reed leaves and cooked for 2 to 3 h. After the cooking process, the red date is sweet, tasty, and gives the surrounding glutinous sweet rice great flavor. The red dates of small-sized cultivars like “Jin sze tsao” and “Wu hu tsao” (pitless) are excellent when cooked with rice or millet in porridge.
Candied Jujube (Honey Jujube) Frank Meyer (1911) mentioned the cooking process of honey jujubes, which have been popular in China for 200 years. Fruits are picked at white mature stage and 60%80% of vitamin C content can be kept, which is much higher than the sun-dried jujube. Fruit surfaces are sliced with rows of blades or needles to enhance sugar-soaking and product appearance.
Spirited Jujube (“Drunk Jujube”) Fruits are picked during the fully red stage and 60%70% of the vitamin C content is preserved. Spirits of 130140 proof or good-quality hard liquor is used for this product. The jujube fruits are poured into the liquor and fully covered with liquor. They are then sealed in jars or zip bags and can be stored for 6 months to 1 year. They can also be sealed in small packages and sold directly in those packages several months later.
Smoked Jujube This product is mainly produced from the cultivar Yuan ling tsao in Shandong Province. Fruits are picked at the fully red stage, precooked in boiling water, and then smoked. The product can be eaten directly or used in cooking.
Roasted Jujube Red dates are used for this purpose. The fruit are first pitted and then sliced vertically to pieces 3 mm wide before roasting. Fully mature fresh fruit of drying cultivars can also be used but require a longer roasting time than using dried fruit.
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Jujube Jam Full red fruits are also used for jam, which can preserve 65%80% of the vitamin C content. The fruit needs to be skinned and pitted for this purpose.
Jujube Paste/Filling Jujube filling is widely used in the pastry industry in China; it is one of the traditional fillings of moon-cakes. It can also be directly spread over bread.
Reaching Additional Consumers Jujubes can also be used to make juice, wine, and vinegar, whereas the red date is also widely used in the culinary world. The Chinese and Southeast Asian populations in the United States are used to having jujubes in their diets, consuming them fresh, dried, or processed. If we promote jujubes and want the rest of Americans to consume them, American-style jujube products are needed. Eating fresh would be the easiest way for Americans to accept the fruit. The author conducted some jujube fruit-tasting workshops, including the New Mexico State Fair, and with school kids through the Cooking with Kids program in Santa Fe, NM. Most people who tasted the fruit liked them. Fresh jujubes have an apple-like texture without any strong flavor and are sweet and nutritious. With a good promotion program, it would not be difficult for the public to accept this nutritious fruit. Fresh fruit can also be used solely in pies or together with apples. It seems the ascorbic acid preserved well for products cooked with fresh fruit, which would be beneficial because people have more concern about health than before. Fresh fruit can also be used in icecream or fruit salad or processed into jam. Dried jujubes can be directly used in fruit and nut mixes or used to replace raisins or palm dates in baking for cakes, tarts, or other pastry products or baked goods. Jujube paste can be used directly as a spread or used as filling for other pastries. A popular product is needed to promote the jujube and to develop a viable market. Jujube is also a multipurpose plant. Except for its fruit, jujube is a nice nectar plant with a long blooming period and jujube honey is popular in China. Its seeds, especially the seeds from Ziziphus spinosa, are a famous traditional Chinese herb, ‘‘Suanzaoren.” Its wood is very hard and good for instruments or utensils.
ACKNOWLEDGMENTS I would like to express my gratitude to all those who helped me during the writing of this manuscript. I gratefully acknowledge the help of my old friend, Mr. Zhang Qunyuan, who has offered me valuable conferences from the United States.
REFERENCES Cheng, G., Bai, Y., Zhao, Y., Tao, J., Liu, Y., Tu, G., et al., 2000. Flavonoids from Ziziphus jujuba Mill var. spinosa. Tetrahedron. 56, 89158920. Devi, S., Pandey, V.B., Singh, J.P., Shah, A.H., 1987. Peptide alkaloids from Ziziphus species. Phytochemistry. 26 (1), 33743375. Eiznhamer, D., Xu, Z., 2004. Betulinic acid: a promising anticancer candidate. Int. Drugs. 4, 359373. Han, B.H., Park, M.H., 1986. Studies on the sedative alkaloids from Ziziphus spinosa semen (seed). Saengyak Hakhoechi. 16 (4), 233238. Han, B.H., Park, M.H., Han, Y.N., 1990. Cyclic peptide and peptide alkaloids from seeds of Ziziphus vulgaris. Phytochemistry. 29 (10), 33153319. Jossang, A., Zahir, A., Diakite, D., 1996. Mauritine J, a cyclopeptide alkaloid from Ziziphus mauritiana. Phytochemistry. 42, 565567. Kim, D.S.H.L., Pezzuto, J.M., Pisha, E., 1998. Synthesis of betulinic acid derivatives with activity against human melanoma. Bioorg. Med. Chem. Lett. 8, 17071712. Kundu, A.D., Barik, B.R., Mandal, D.N., Dey, A.K., Banerji, A., 1989. Zizybernalic acid, a penta cyclic riterpenoid of Ziziphus jujuba. Phytochemistry. 28 (11), 31553158. Kurihara, Y., Oohubo, K., Tasaki, H., Kodama, H., Akiyama, Y., Yagi, A., et al., 1988. Studies on taste modifiers. I. Purification and structure in leaves of Ziziphus jujuba. Tetrahedron. 44 (1), 6166. Lee, S., Min, B., Lee, C., Kim, K., Kho, Y., 2003. Cytotoxic triterpenoids from the fruits of Zizyphus jujuba. Lanta Med. 69, 1821. Majumdar, G.P., 1945. Vedic Plants in BC, vol. 1. Law Commemoration, Calcutta. Matsuda, H., Murakami, T., Ikebata, A., Yamahara, J., Yoshikawa, M., 1999. Bioactive saponins and glycosides. IV. Structure elucidation and immunological adjuvant activity of novel protojujubogenin type triterpene isdesmosides, protojujubosides A, B, and B1, from the seeds of Zizyphus jujuba var. spinosa (Zizyphi spinosi semen). Chem. Pharm. Bull. 47, 1214. Otsuka, H., Ogihara, Y., Shibata, S., 1974. Isolation of coclaurine from Zizyphus jujuba by droplet counter-current chromatography. Phytochemistry. 13, 2016.
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Pareek, O.P., 2001. Fruits for the Future 2: Ber. International Centre for Underutilized Crops, University of Southampton, Southampton. Pawlowska, A.M., Camangi, F., Bader, A., Braca, A., 2000. Flavonoids of Zizyphus jujuba and Zizyphus spina-christi (L) Wild (Rhamnaceae) fruits. Food Chem. 112, 858862. Sang, M.L., Jin, G.P., You, H.L., Cheal, G.L., Byung, S.M., Jung, H.K., 2004. Anti-complementary activity of triterpenoides from fruits of Zizyphus jujuba. Biol. Pharm. Bull. 27 (11), 18831886. Shah, A.H., Pandey, V.B., Eckhardt, G., Tschesche, R., 1985a. A 13-membraned cyclopeptide alkaloid from Ziziphus sativa. Phytochemistry. 24 (11), 27652767. Shoei, S.L., Buh, F.L., Karin, C.L., 1996. Three triterpene esters from Zizyphus jujuba. Phytochemistry. 43 (4), 847851. Srivastava, S.K., Srivastava, S.D., 1979. Structure of Zizogenin, a new sapogenin from Ziziphus auritiana. Phytochemistry. 18 (10), 17581759. Tripathi, M., Pandey, M.B., Jha, R.N., Pandey, V.B., Tripathi, P.N., Singh, J.P., 2001. Cyclopeptide alkaloids from Ziziphus jujuba. Fitoterapia. 72, 507510, Preeti et al., AprilMay, 2014. 3 (3), 959966. Tschesche, R., Shah, A.H., Eckhardt, G., 1979. Sativanine-A and sativanine-B, two new cyclopeptide alkaloids from the bark of Ziziphus sativa. Phytochemistry. 18, 911. Woo, W.S., Kang, S.S., Shim, S.H., Wagner, H., Chari, V.M., Seligmann, O., et al., 1979. The structure of spinosin (2v-O-betaglucosyiswertisin) from Ziziphus vulgaris var. spinosus (seeds). Phytochemistry. 18 (2), 353355. Yoshikawa, M., Murakami, T., Ikebata, A., Wakao, S., Murakami, N., Matsuda, H.J.Y., 1997. Bioactive aponins and glycosides. X. On the constituents of Zizyphi spinosi semen, the seeds of Ziziphus jujuba Mill. var. spinosa Hu (1): structures and histamine release-inhibitory effect of jujubosides A1 and C and acetyljujuboside B. Chem. Pharm. Bull. 45, 11861192. Zeng, L., Zhang, R.Y., Wang, X., 1987. Studies on the constituents of Ziziphus spinosus Hu. Acta Pharm. Sin. 22, 114120. Ziyaev, R., Irgashev, T., Israilov, I.A., Abdullaev, N.D., Yunusov, M.S., Yunusov, S.Y., 1977. Alkaloids of Ziziphus jujuba. Structure of iusiphine and iusirine. Khim. Prir. Soedin. 2, 239243.
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Kumquat—Fortunella japonica Amedeo Palma and Salvatore D’Aquino Institute of Sciences of Food Production, National Research Council, Sassari, Italy
Chapter Outline Classification Origin and Distribution Botany, Morphology, and Anatomy Postharvest Physiology and Storage
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Fruit Compositions, Nutritional, and Nutraceuticals Properties Fresh and Processed Products References
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CLASSIFICATION For several decades, kumquats were included within the family Rutaceae into the genus Citrus. Walter T. Swingle reclassified them in the genus Fortunella which embraces in six species (F. japonica, F. margarita, F. obovate, F. crassifolia, F. hindsii, F. polyandra): all the Citrus japonica varieties (Swingle et al., 1967; Ye et al., 1985; Ortiz, 2002). In this chapter, the features of Fortunella spp. will be discussed.
ORIGIN AND DISTRIBUTION Kumquats are native to south-eastern China. In China the fruit were widely appreciated during the Tang (618907) and Song (9601279) dynasties and were first described in the Chinese literature in AD 1178 (Morton, 1987). Now, kumquats cultivations are spread not just in Asia and in Japan, where were included in a list of cultivated plants in 1712, but also in Argentina, Brazil, Florida, California, in the Mediterranean region, Australia and South Africa, although representing a minor crop (Huang et al., 2011; Delort and Naef, 2011; Ladaniya, 2008a). The two most important cultivated species are “Marumi” or “Round” Kumquat (Fortunella japonica Swingle) and “Nagami” or “Oval” Kumquat (Fortunella margarita Swingle). Another extensively cultivated group, particularly in China, the United States and Australia, is “Meiwa” kumquat (Citrus crassiflora Swingle), considered as a natural hybrid between “Marumi” and “Nagami” kumquats. The name kumquat is supposed to come from the earliest Chinese name “chin kan,” that means “gold orange.” In Japan, the equivalent name of “Marumi” Kumquat is “kin kan” or “kin kit.” In Southeast Asia, kumquats are called “kin kuit,” in Brazil the trade name is “kumquat,” “kunquat,” or “laranja de ouro dos orientais,” while in the United States and Mediterranean countries, kumquat is the most common name (Vaughan and Geissler, 2009). Of the total world citrus production, which was around 100 million tons in 200304 (FAO, 2006), about 10% was shared by the seedless pomelos, kumquats, and other minor citrus (Ladaniya, 2008a). In 2001 the production of kumquat in Korea was estimated to be 3589 t (Jeju Provincial Development Corp, 1999). However, reliable statistical sources of the world production of kumquats or of individual countries are not available.
BOTANY, MORPHOLOGY, AND ANATOMY Kumquats (Fortunella spp. Swingle) are the smallest trees among citrus species. The plant is an evergreen small tree, 2.54.5 m tall, with compact crown and branches with a few spines. The leaves are alternate, lanceolate and similar to small mandarin leaves. The white flowers are bisexual and generally solitary with sweet fragrance (Morton, 1987). Kumquat trees grow well in areas with hot summer (2538 C), but are also able to overcome stormy winters with temperatures as low as 210 C. Therefore, they can be cultivated in areas where the climate is too cold for other citrus Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00035-6 © 2018 Elsevier Inc. All rights reserved.
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fruits (Morton, 1987). The ability to tolerate temperatures of different degrees below 0 C for long time is due to the long state of dormancy occurring in winter, which is discontinued only after several weeks of warm weather, when new shoots or blossoms occur. Despite this, kumquat trees grow better and produce best quality fruits in warmer regions. Kumquats are rarely grown from seeds and generally are grafted onto the trifoliate orange (Poncirus trifoliata) that has been found as the best rootstock not only for crops in the field but also in pots. Sour orange and grapefruit are also good rootstocks but their use is quite limited (Wutscher, 1979). In an orchard, kumquats can be set with high planting density. Reducing the development of the canopy facilitates fruit harvest that can be done by hand from the ground (see Fig. 1). The kumquat fruit is a modified berry (hesperidium) resulting from a single ovary. The calyx is attached to the peduncle and remains firmly linked to the branch even when the fruit is ripe, thus the natural abscission is not frequent (Ladaniya, 2008b). Kumquats are round, slightly oblate or obovate in shape, with a diameter of about 3 cm and an average weight of 12 g (Kassim et al., 2016; Jaliliantabar et al., 2013). In the northern hemisphere, kumquats mature from late November to February. As maturity advances, the peel turns from green to orange and, at the optimal maturation stage, reaches a yellow reddish-orange gold color. At the same time, the large oily glands become evident and the peel becomes smooth and shiny. Kumquat must be picked full ripe because the best organoleptic and nutritional properties can be reached only on the tree (Ladaniya, 2008b). However, once reached the best optimal maturity stage, fruit harvest can be delayed for several weeks as their prolonged permanence on the plant does not lead to significant physical, microbiological and nutritional alterations. Kumquats differ from other citrus fruits for different features. The flavedo, consisting of the outermost tissue of pericarp is colored, fleshy, thick, tightly clinging, sweet, edible, and contains oil glands; immediately below, the albedo, consisting of parenchymatous colorless cells, is almost absent (Tadeo et al., 2008; Ladaniya, 2008b). The endocarp, differently than in most other citrus fruits where represents the major and edible part, in kumquats is scant and radially divided into 36 segments delimited by fine membranes with little acid to subacid juicy and small seeds. For these characteristics, kumquats can be eaten as a whole, being its rind sweet and fragrant, leaving a pleasant long lasting flavor (Choi, 2005; Facciola, 1990) (see Fig. 2).
POSTHARVEST PHYSIOLOGY AND STORAGE The kumquat, as all other citrus fruits, is not climacteric: fruit mature gradually over the growing season whilst attached to the plant. They do not continue the ripening process once harvested. During maturation their respiration rate and ethylene production do not exhibit remarkable increases (Biale, 1950; Rhodes, 1980; Ladaniya, 2008b). A gradual fruit enlargement, color change, sugar accumulation in the peel and modification in secondary metabolites content (i.e., essential oils and polyphenols) characterize the maturation process (Barreca et al., 2010; Lou et al., 2015, 2016). After harvest, the respiration rate of kumquat is higher compared to other citrus fruit due to their high FIGURE 1 A Kumquat orchard in Sicily. Source: Photo by A. Continella.
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FIGURE 2 Ripe kumquat fruit.
surface area to volume ratio, reaching values of about 40 mg CO2/kg per h at 20 C, while ethylene production rate is about 0.19 μL/kg per h at 20 C (Schirra et al., 1995). The high surface area to volume ratio is also responsible for the high transpiration rate, which leads to excessive water loss in fruit held at room conditions and a rapid dehydration of peel. Weight loss of just 5%6% can markedly alter the appearance and reduce firmness, resulting in detrimental marketability. Water loss is one of the main cause of quality loss; in kumquats stored at 20 C for 3 or 6 weeks, weight loss ranged between 6% and 12% (Schirra et al., 1995). The high perishability of kumquats is also affected by spoilage losses caused mainly by Penicillium spp. and other postharvest pathogens common to other citrus fruits, such as Geotrichum candidum (Chalutz et al., 1989; Schirra et al., 2011; Youssef et al 2014) (see also Fig. 3). Various postharvest technologies are applied to improve kumquat keeping quality and prolong the shelf-life. Cold storage can extend kumquat postharvest life for some weeks, but as in other citrus fruits, the susceptibility to chilling injury when fruit are exposed at temperatures below 8 C can negatively affect postharvest quality (Chalutz et al., 1989; Paull et al., 1990; Rodov et al., 1995; Schirra et al. 1997). Recommended storage conditions are temperatures ranging from 8 C to 11 C for 4 weeks (Mercantilia 1989; Chalutz et al., 1989) and 6 weeks at 6 C (Schirra et al., 1995). According to the cultivar and the environmental conditions, the response to low storage temperature can change considerably. For example, SeaLand (1991) recommended storage at 4.4 C and 90%95% RH for 1428 days. However, when fruit are held at room temperature, the quality declines rapidly. The shelf-life was reduce to only 1 week when fruit were stored at 20 C and 60% RH (Mercantilia, 1989). Whilst cold storage is an effective means to preserve fruit quality and prevent pathogen growth, it is unable to completely control rot development. Schirra et al. (1995) reported 10% and 45% losses for decay due to natural infections after 3 or 6 weeks of storage at 6 C, respectively. However, postharvest synthetic fungicides are not allowed, as the whole fruit, including the peel, is eaten. Thus, alternative technologies to reduce postharvest decay have been tested. Hot water dipping (HWD), developed as a nonchemical method to prevent chilling injury, has resulted to be one of the most effective treatment to preserve quality and prevent decay (De-Villiers et al., 1997). HWD for 2 min at 53 C or 56 C maintained for long time kumquat nutritional and nutraceutical properties, reduced water loss and controlled green (Penicillium digitatum) and blue (Penicillium italicum) molds (Rodov et al., 1995; Ben-Yehoshua et al., 2000; Schirra et al., 2011). However, a further increase of treatment temperature at 59 C or 61 C, rather than improving, reduced decay control (Ben-Yehoshua et al., 2000). A 2-min dip treatment at 50 C reduced by 50% and 75% decay incidence in kumquats stored at 17 C and 80% RH for 14 or 21 days, respectively (Schirra et al., 2008, 2011). In contrast, in fruit conditioned at 37 C and 99% RH for 30 h, the reduction of decay was modest (Schirra et al., 2011). The lower loss of
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FIGURE 3 Fruit at harvest time.
decay in hot water treated kumquat was correlated with an increase in the level of phytoalexin (scoparone) in the flavedo (Dubery, 1992; Ben-Yehoshua et al., 2005). Ultraviolet (UV) treatment is another means that can effectively be implemented at a commercial level to reduce pathogen growth. Decay incidence in kumquats inoculated with P. digitatum and irradiated with UV was reduced by 40% (Rodov et al., 1992). UV treatment was demonstrated to induce phytoalexin production in kumquat as well as in other citrus fruit. When UV irradiation was combined with HWD, the production of phytoalexins (scoparone) increased and flavedo resistance to infection was higher compared with treatments alone (Rodov et al., 1992, 1995; Ben-Yehoshua et al., 1992, 2005). Washing with chlorinate or anolyte water either alone or in combination with HWD (Kassim et al., 2016) was also effective in delaying the onset of decay. In addition, these treatments reduced weight loss and preserved firmness, moisture, and soluble solids content. No scientific reports of the practice at a retail level of packaging kumquats plastic packs are currently available in the literature.
FRUIT COMPOSITIONS, NUTRITIONAL, AND NUTRACEUTICALS PROPERTIES Among citrus fruit species, kumquats are excellent sources of nutrients and phytochemicals. Several studies have been investigated to characterize the nutritional and nutraceutical profile of kumquats. Results reported in the literature are quite different not only in terms of nutritional composition but, above all, in terms of quantitative and qualitative secondary metabolites (Lou et al., 2016; Ogawa et al., 2001; Ortiz, 2002; Sadek et al., 2009; Schirra et al., 2008; Wang et al., 2008). This is due to several factors such as different cultural management, production areas, climate conditions, genetic diversity as well as nonstandardized methods for extraction and analysis (Arpaia, 1994; Kondo et al., 2005; Lou et al., 2016). Kumquats are nutritious fruits, rich in fiber, sugar, and microelements. According to the Department of Agriculture, Agricultural Research Service of the United States (USDA, 2015), the nutritional composition of fresh kumquat referred to 100 g of edible portion is: water 80.85 g, protein 1.88 g, total lipid 0.86 g, ash 0.52 g, carbohydrate 15.90 g, total dietary fiber 6.5 g, total sugars 9.36 g, Ca 62 mg, Fe 0.86 mg, Mg 20 mg, P 19 mg, K 186 mg, Na 10 mg, Zn 0.17 mg, Cu 0.095 mg, Mn 0.135, and account for 71 kcal (296 kJ) of energy. Sugars, mainly concentrated in the peel, are represented by sucrose, which reaches values of about 5.66 g/100 g of fresh weight, and glucose and fructose that present in similar quantities (2.5 g/100 g of fresh weight) (Schirra et al., 2008).
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Citric acid is the main organic acid, with a concentration of about 2.8 g/100 mL juice, while malic and ossalic acid are present in low quantity, 0.35 and 0.02 mg/100 mL juice, respectively (Schirra et al., 2011). Kumquats are an important source of health beneficial secondary metabolites including flavonoids, vitamins, carotenoids, and terpenoids, with by higher antioxidant activity (Koyasako et al., 1983; Ortiz, 2002; Schirra et al., 2008, 2011). The total phenolic and flavonoid contents of kumquat are higher in the peel extracts compared with the pulp or with over-ripe kumquats. Total phenolic content of immature kumquat is in the range of 23463000 mg gallic acid equivalent/ 100 g dry extract and is two times higher than that of mature fruit (Lou et al., 2015, 2016; Lou and Ho, 2017). Significantly lower levels of total phenols were reported in Greek and Egyptian kumquats, ranging between 80 and 40 and between 100 and 40 mg gallic acid equivalent/g of peel dry fraction, respectively, while in kumquats cultivated in Italy the total phenols ranged between and 290 and 253 mg gallic acid equivalent/100 fresh weight (Schirra et al., 2008, 2011). The main flavonoids detected in kumquats are narirutin, apigenin, rhoifolin, isorhoifolin, kaempferol, luteolin, poncirin, hesperidin, neoponcirin, eriocitrin, didymin, and quercetin (Kawail et al., 1999; Ramful et al., 2011; Jayaprakasha et al., 2012; Schirra et al., 2008; Wang et al., 2008; Barreca et al., 2010). Dihydrochalcone derivative, 30 ,50 -di-C-β-glucopyranosylphloretin was also found in the genus Fortunella (peel, 6.515.2 mg/g in dry weight; juice, 1.510.5 mg/g) (Ogawa et al., 2001; Lou et al., 2016). Narirutin and rhoifolin, (107 and 37 mg/100 g of fresh weight respectively) were the most abundant flavonoids detected by Schirra et al. (2008). Similarly, Lou and Ho (2017) found narirutin as a major flavonoid (20821348 mg/100 mg dried sample) which, after reinvestigation, was shown to be a 30 ,50 -di-C-β-glucopyranosylphloretin. Fairly high is also the level of fortunellin (23497 mg/100 mg in dried sample) (Lou and Ho, 2017; Cho et al., 2005), while other flavonoid generally occur only in small amounts. The vitamins composition of raw kumquat per 100 g edible portion is: vitamin C (4320 mg), vitamin B1 (0.03 mg), vitamin B2 (0.09 mg), vitamin B3 (0.04 mg), vitamin B5 (0.037 mg), vitamin B6 (0.03 mg), total folate (17 μg), vitamin A (290 UI), vitamin E as α-tocopherol (0.15 mg), total vitamin E (1.19 mg) (USDA, 2015; Schirra et al., 2008). Carotenoids are available in larger amounts in the peel, while the pulp contains only a very small quantity. The amount of total carotenoids found by Schirra et al. (2008) were 1.27 mg/100 g of edible portion. Carotenoids composition of the peel was identified by Ago´cs et al. (2007), who detected β-citraurin (16.6%), violeoxanthin (16.9%), β-cryptoxanthin (11.4%) and violaxanthin (9.8%) as main components and cryptochromes (5.7%), lutein (5.5%), luteoxanthin (3.7%), β-cryptoxanthin (2.8%), β-citraurins (2.4%), violaxanthin (1.7%), neochrome (1.5%), ξ-carotene (0.9%) and α-cryptoxanthin (0.2%) as minor components. Among the secondary metabolites, the content of fruit phytosterols is particularly important for their healthy properties in controlling cholesterol metabolism (Katan et al., 2003). Total phytosterol content of kumquat was found to be 12.56 μg/g dry weight and identified as campesterol (1.02 μg/g), stigmasterol (1.33 μg/g), sitosterol (7.04 μg/g), amyrin (10.45 μg/g), and lupenone (8.43 μg/g) (Chen et al., 2017). As in the other citrus species, in kumquat essential oils are greatly accumulated in the oil glands of the peel. However, rather than being important as a source of raw material for applications in pharmaceutical, sanitary, cosmetic, agricultural and food industries, kumquats play a very important role for the flavor and taste conferred the fruit as well as for their healthy properties, as they are consumed as a whole, including their peel. Essential oil composition of kumquat peel extracts is reported in several works and the number of detected components has grown over time due to refinement of analytical techniques. Currently the number of compounds identified is greater than 90, including terpenes, aldehydes, alcohols, esters, and amines. Terpenes are the most representative compounds and limonene is the most abundant terpene, accounting for more than 90% of the whole oil. Other important compounds are myrcene (B1.84%), linalool (B1.4%) and ethyl acetate (B1.13%). Kumquat essential oils differ from those of other citrus species for the presence of a larger variety of terpenyl alcohols and esters, such as terpinen-4-ol, p-menth-1-en-9-yl acetate, trans-p-mentha-2,8-dien-1-ol and its acetate, p-mentha-1,8-dien-9-yl acetate and its propanoate, as well as higher amounts of sesquiterpenoids (Crowell, 1999; Kwang et al., 1992; Choi, 2005; Koyasako and Bernhard, 1983; Umano and Shibamoto, 1988; Peng et al., 2013; Gu¨ney et al., 2015; Schirra et al., 2008; Lim, 2012; USDA, 2015). Whilst limonene is the major component of peel oil, it has no impact on flavor, while, citronellyl acetate, a minor ester compound, is considered to impart a characteristic odor to kumquat peel oil. Food antioxidants play an important role in the free radical scavenging mechanism and in the control of the oxidation processes that naturally occur in the human body that are responsible for cellular ageing and development of most diseases (Seifried, 2007). In the past few decades, new knowledge has been gained on the role played by the antioxidant activity of fruits and vegetables to cure and prevent a number of chronic diseases. Several studies report of relevant antioxidant properties and antimicrobial activity detected in kumquat extracts (Sadek et al., 2009;
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Jayaprakasha et al., 2012). Phenolics and in particular flavonoids exhibit a wide range of biological effects including antioxidant and radical scavenging activity besides the ability to positively modulate the activity of different enzyme systems (Gattuso et al., 2007; Vicente et al., 2009; Lv et al., 2015). Flavonoids are the main compounds that contribute to free radical scavenging activity in kumquat extracts. This is confirmed by the fact that the antioxidant activity decreases alongside as the level of flavonoids declines during the ripening process (Barreca et al., 2010). Essential oils also have relevant antioxidant properties, but the contribution of the individual compounds is very variable. Limonene and myrcene, e.g., showed a low radical scavenging activity, which in contrast was higher in α-terpinene, nootkatone, citronellal, citral, geraniol, γ-terpinene, and terpinolene. The terpenes γ-terpinene and terpinolene, despite being a minor component of kumquat essential oils, are considered important contributors of the overall radical scavenging activity of kumquats (Choi et al., 2000). Irrelevant of the recent scientific evidence related to the antiageing activity of kumquat and the beneficial effects of the numerous bioactive compounds, the role played by kumquat in health promotion and disease risk reduction has long been recognized by the traditional medicines of the regions where kumquats are largely cultivated, such as China (Lin et al., 2008; Sadek et al., 2009). These properties are associated with the prevention of cardiovascular disorders, cancers, infectious diseases, antibacterial, antiinflammatory, antiallergic and vasodilatory actions. Kumquat extract also seems to regularize the metabolic disorders caused by obesity, showing promising applications as potential dietary supplement (Chen et al., 2017; Tan et al., 2016; Jayaprakasha et al., 2012; Kumamoto et al., 1985; Lou and Ho, 2017; Nagahama et al., 2015).
FRESH AND PROCESSED PRODUCTS Kumquat fruits can be eaten raw or processed to obtain different preparations. To fully appreciate their organoleptic characteristics, the raw fruit are usually consumed as a whole and before eating, it is suggested to roll the fruit between the hands to release the essential oils of the rind. This way the contrast of taste due to the acidity of pulp and the sweet flavor of the essential oils present in the peel can be better appreciated. Moreover, the characteristic taste of the fruit lasts for a long time in the mouth. Fresh fruit can be sliced and added to salads, can be used to decorate cakes and desserts or to prepare cocktails such as in “Kumquat mojitos,” a variant of the traditional mojitos, where limes are replaced by kumquats. Kumquats are appreciated in the confectionery industry, being excellent to prepare marmalades or candies glazed with pectin, crystalline sugar, edible coating, or chocolate. Kumquat can also be cooked and used as a garnish in several recipes based on fish or meat and, if cooked in syrup, can be combined with icecream to make an excellent dessert. Macerated in vodka or other clear spirit, kumquats can add flavor to liqueurs, while if canned can be stored for a long time and marketed in countries distant from the production regions (Small, 2012).
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Choi, H.S., Song, H.S., Ukeda, H., Sawamura, M., 2000. Radical-scavenging activities of citrus essential oils and their components: detection using 1, 1-diphenyl-2-picrylhydrazyl. J. Agric. Food Chem. 48, 41564161. Crowell, P.L., 1999. Prevention and therapy of cancer by dietary monoterpenes. J. Nutr. 129, 775778. Delort, E., Naef, R., 2011. Volatile components in less common citrus species. In: Dugo, G., Mondello, L. (Eds.), Citrus Oils: Composition, Advanced Analytical Techniques, Contaminants, and Biological Activity. CRC Press, Boca Raton, FL, pp. 163191. De-Villiers, E.E., Van Dyle, K., Korsten, L., Swart, S.H., Smit, J.H., 1997. Potential alternative decay control strategies for South African citrus packhouses. In: Proc. Int. Soc. Citric, South Africa, pp. 410412. Dubery, I.A., 1992. Elicitation of enhanced phenylpropanoid metabolism in citrus flavedo by gamma radiation. Phytochemistry 31, 26592662. Facciola, S., 1990. Cornucopia. A Source Book of Edible Plants. 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Phenolic compounds and biological activities of small-size citrus: kumquat and calamondin. J. Food Drug. Anal. 25, 162175. Lou, S.N., Lai, Y.C., Huang, J.D., Ho, C.T., Ferng, L.H.A., Chang, Y.C., 2015. Drying effect on flavonoid composition and antioxidant activity of immature kumquat. Food Chem. 171, 356363. Lou, S.N., Lai, Y.C., Hsu, Y.S., Ho, C.T., 2016. Phenolic content, antioxidant activity and effective compounds of kumquat extracted by different solvents. Food Chem. 197, 16. Lv, X., Zhao, S., Ning, Z., Zeng, H., Shu, Y., Tao, O., et al., 2015. Citrus fruits as a treasure trove of active natural metabolites that potentially provide benefits for human health. Chem. Cent. J. 9 (68), 114. Mercantilia, 1989. Guide to Food Transport Fruit and Vegetables. Mercantilia Publishers, Copenhagen. Morton, J., 1987. Kumquat. In: Morton, J. (Ed.), Fruits of Warm Climates. Julia F. Morton, Miami, FL, pp. 182185. 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Ramful, D., Tarnus, E., Aruoma, O.I., Bourdon, E., Bahorun, T., 2011. Polyphenol composition, vitamin C content and antioxidant capacity of Mauritian citrus fruit pulps. Food Res. Int. 44, 20882099. Rhodes, M.J.C., 1980. The maturation and ripening of fruits. In: Thimann, K.V. (Ed.), Senescence in Plants.. CRC Press, Boca Raton, pp. 157204. Rodov, V., Ben-Yehoshua, S., Kim, J.J., Shapiro, B., Ittah, Y., 1992. Ultraviolet illumination induces scoparone production in kumquat and orange fruit and improves decay resistance. J. Am. Soc. Hort. Sci. 117, 788792. Rodov, V., Ben-Yehoshua, S., Albagli, R., Fang, D.Q., 1995. Reducing chilling injury and decay of stored citrus fruit by hot water dips. Postharvest Biol. Technol. 5, 119127. Sadek, E.S., Makris, D.P., Kefalas, P., 2009. Polyphenolic composition and antioxidant characteristics of kumquat (Fortunella margarita) peel fractions. Plant Foods Hum. Nutr. 64, 297302. Schirra, M., Agabbio, M., Continella, G., D’Aquino, S., 1995. Extension of kumquat fruit storage life by postharvest hot dip treatments in water and freshening agent. Adv. Hort. Sci. 9, 8386. Schirra, M., Agabbio, M., D’hallewin, G., Pala, M., Ruggiu, R., 1997. Response of Tarocco oranges to picking date, postharvest hot water dips, and chilling storage temperatures. J. Agric. Food Chem. 45, 32163220. Schirra, M., Palma, A., D’Aquino, S., Angioni, A., Minello, E.V., Melis, M., et al., 2008. Influence of postharvest hot water treatment on nutritional and functional properties of kumquat (Fortunella japonica Lour. Swingle Cv. Ovale) fruit. J. Agric. Food Chem. 56, 455460. Schirra, M., Angioni, A., Cabras, P., D’Aquino, S., Palma, A., 2011. Effects of postharvest hot water and hot air treatments on storage decay and quality traits of kumquat (Fortunella japonica Lour. Swingle, cv. Ovale) fruit. J. Agric. Sci. Technol. 13, 8994. SeaLand, 1991. Shipping Guide to Perishables. SeaLand Services Inc, New Jersey, NJ. Seifried, H.E., 2007. Oxidative stress and antioxidants: a link to disease and prevention? Nutr. Biochem. 18, 168171. Small, E., 2012. Kumquat. In: Small, E. (Ed.), Top 100 Exotic Food Plants. CRC Press, Taylor & Francis Group, Boca Raton, London, New York, pp. 339350. Swingle, W.T., 1967. The botany of Citrus and its wild relatives of the orange subfamily (family Rutaceae, subfamily Aurantiodeae). In: Webber, H.J., Batchelor, L. (Eds.), Citrus Industry, vol. 1. University of California, Riverside, CA, pp. 129474. Tadeo, F.R., Cerco´s, M., Colmenero-Flores, J.M., Iglesias, D.J., Naranjo, M.A., Rios, G., et al., 2008. Molecular physiology of development and quality of citrus. Adv. Bot. Res. 47, 147223. Tan, S., Zhao, X., Yang, Y., Ke, Z., Zhou, Z., 2016. Chemical profiling using Uplc Q-Tof/Ms and antioxidant activities of Fortunella fruits. J. Food Sci. 81, 16461653. Umano, K., Shibamoto, T.A., 1988. A world perspective. In: Lawrence, B.M., Mookherjee, B.D., Willis, B.J. (Eds.), Proceedings of the 10th International Congress of Essential Oils, Fragrances and Flavors. Washington, DC. Elsevier Science Publishers, Amsterdam, p. 998. United States Department of Agriculture, Agricultural Research Service (USDA), 2015. National nutrient database for standard reference, Release 28. Nutrient data laboratory home page. ,https://ndb.nal.usda.gov/ndb/foods/show/2254?manu 5 &fgcd 5 &ds 5 .. Vaughan, J.G., Geissler, C., 2009. The New Oxford Book of Food Plants. Oxford University Press, New York, NY, p. 98. Vicente, A.R., Manganaris, G.A., Sozzi, G.O., Crisosto, C.H., 2009. Nutritional quality of fruits and vegetables. In: Florkowski, W.J., Shewfelt, R.L., Brueckner, B., Prussia, S.E. (Eds.), Postharvest Handling: A Systems Approach., second ed. Academic Press, San Diego, CA, pp. 57106. Wang, Y.C., Chuang, Y.C., Hsu, H.W., 2008. The flavonoid, carotenoid and pectin content in peels of citrus cultivated in Taiwan. Food Chem. 106, 277284. Wutscher, H.K., 1979. Citrus rootstock. Hortic. Rev. 1, 237269. Ye, Y., 1985. The status of Fortunella genetic resources in China. Fruit Var. J. 39, 1720. Youssef, K., Sanzani, S.M., Ligorio, A., Ippolito, A., Terry, L.A., 2014. Sodium carbonate and bicarbonate treatments induce resistance to postharvest green mould on citrus fruit. Postharvest Biol. Technol. 87, 6169.
Langsat—Lansium domesticum Chairat Techavuthiporn Huachiew Chalermprakiet University, Samut Prakarn, Thailand
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology Chemical Compositions and Nutritional Values
279 280 280 280 280
Sensory Characteristics Harvest and Postharvest Conservation Potential Industrial Application References Further Reading
281 282 282 283 283
CULTIVAR ORIGIN AND BOTANICAL ASPECTS Langsat (Lansium domesticum) originates in western South-East Asia and is both wild and cultivated in Malaysia, Thailand, Indonesia, and the Philippines. On a small scale, langsat is also cultivated in other humid areas namely Vietnam, Burma, India, Sri Lanka, Australia, Surinam, and Puerto Rico. The fruits are plentiful on local markets. In addition, langsat was introduced into Hawaii before 1930, and is frequently grown at low elevations. It may occasionally be found on other Pacific islands. L. domesticum includes different important cultivars; langsat, longkong, and duku. Lansium spp. belongs to the Meliaceae family (Tilaar et al., 2008). As the morphological appearance of all cultivars is nearly the same, identification of the cultivars is very difficult for growers. Langsat and longkong can only be identified after bearing fruit, which requires 57 years, compared to the duku that can be identified by its bitter leaf taste at seeding stage. In term of L. domesticum, there are two distinct botanical varieties. The first is var. pubescens, the typical wild langsat which is a rather slender, open tree with hairy branchlets and nearly round, thick-skinned fruits having much milky latex. The second is var. domesticum, called duku, doekoe, or dookoo, which is a more robust tree, broad-topped and densely foliaged with conspicuously-veined leaflets. Duku fruits, borne few to a cluster, are oblong-ovoid or ellipsoid, with thin, pale-brownish skin, only faintly aromatic and containing little or no milky latex. In both groups, some small fruits are completely seedless and fairly sweet. L. domesticum var. pubescens has different common names belonging to the nationality, e.g. Burmese (duku, langsak); English (Langsat, duku); Filipino (lanzone, lanzon, lansones, lansone, buahan); Indonesian (duku, kokosan, langsat); Malay (langseh, langsep, lansa); Thai (duku, longkong, langsat); Vietnamese (bo`n-bon); Chinese (lan sa); Japanese (ransa); and Spanish (arbol de lanza). The langsat tree is an erect and between 10 and 15 m in height and trunk 75 cm in diameter, with redbrown or yellowbrown, furrowed bark, containing milky, sticky resinous; twigs glabrous to pilose. Leaves are large, up to 50 cm long, pinnate with 69 leaflets. The leaflets are either obovate or elliptic-oblong, 1425 cm long by 612 cm wide, whist the two basal ones are smallest, 716 cm long by 510 cm wide. Leaflet stalk varies from 4 to 15 mm long. The upper surface of the leaflet is slightly leathery, dark-green and glossy while the beneath is paler and dull. They are chartaceous-corieceous, apex short acuminate, lateral veins 1014 pairs, thickened at base. Flowers are arranged spirally on the peduncle. The flower is scented, mostly bisexual, sessile to pedicelled, small; calyx fleshy, cup-shaped, five-lobed, greenish-yellow, erect, 57 mm in diameter and 24 mm high, white to pale yellow; anthers in one whorl, ovary globose, appressed pilose. It is pentamerous with five sepals and petals. The sepals are small, greyish green, 0.52.3 mm long by 1.12.6 mm wide. The petals are thick, fleshy, yellow, ovate, curved, Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00036-8 © 2018 Elsevier Inc. All rights reserved.
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1.33.3 mm long by 3.36.0 mm wide. Ten stamens of about 1 mm long are attached on the stamina tube which surrounds the style. The style is short and thick. The stigma is five-angled and truncate. The fruit are borne in either loose or compact clusters in a bunch (230 fruits irrespective of its length and compactness). Each fruit is oval, ovoid-oblong or nearly round, 2.55 cm in diameter, 25 cm in length, and weighs 850 g. It has light grayishyellow to pale brownish, velvety skin, leathery, fruit peel is thin (11.5 mm) or thick (up to 6 mm) and containing milky latex. Usually there are three sizes of fruits in a bunch and they are distributed at random along the bunch. The fruit contains five locales separated by a white membraneous septum. Three bigger arils hold near each other while two smaller ones are on the opposite side. Seeds are usually present in 13 of the segments, which enveloped by a closely adhering. One seed in each fruit is the largest. Occasionally, two big seeds are found. They are in green color, 22.5 cm in length and 1.252 cm in width, very bitter. The green seed is covered with a white translucent flesh and is slightly sour. The number of cotyledons in a seed varies from 2 to 8 indicating the number of embryos in a single seed varies from 1 to 4. Cells without developed seed are also filled with aril tissue (Morton, 1987; Salma and Razali, 1987).
HARVEST SEASON The langsat is a tree of tropical lowland forest and is damaged by frost. It cannot be grown at an altitude over 650750 m. It needs a humid atmosphere, plenty of moisture and will not tolerate long dry seasons. A tree begins to bear fruit only after 15 years. It is a seasonal crop so it produces fruits only in late September through to early November. Langsats in Malaya generally bear fruit twice a year, in June and July and again in December and January or even until February. In India, the fruits ripen from April to September but in the Philippines the season is short and most of the fruits are off the market in less than 1 month. The harvest season of langsat fruit is usually between August and September of each year in Thailand.
ESTIMATED ANNUAL PRODUCTION Langsat generally bears fruit once a year and twice a year in some areas. This period can vary between areas, but blooming is generally after the beginning of the rainy season and fruit production some 4 months later. Production often varies from year to year, and depends to some extent on having a dry period to induce flowering. In Thailand, the average production is only 1 t/rai per year (1 rai 5 1600 m2). In Indonesia, around 146,000 trees have been planted. With productivity approaching 7080 kg per tree, in 2010, more than 7250 t were produced. A productive tree averages 1000 fruits per year in the Philippines. Moreover, trees in the Nilgiris, India, average 13.5 kg of fruits annually produce. Another example of 10 trees recorded in Costa Rica as about 25 years old produced during 5 years the following weights of saleable fruits: 2008: 50 kg, 2009: 2000 kg, 2010: 1000 kg, 2011: 100 kg, 2012: 1500 kg.
FRUIT PHYSIOLOGY Each fruit has about five separate segments with 15 seeds. The astringency taste of fruit declines during fruit ripening and the sugar content increases (see Figs. 1 and 2). The fruits in a single bunch do not all ripen simultaneously. Usually, a few fruits ripen together acropetally. The respiration rate of langsat after harvest decline and of small fruit have a higher rate than that of large fruit. At 9 C and 20 C, the respiration rate is about 4050 mg CO2/kg per h and 5090 mg CO2/kg per h, respectively.
CHEMICAL COMPOSITIONS AND NUTRITIONAL VALUES Langsat (L. domesticum) is a tropical fruit containing a wide variety of macronutrients such as vitamins and minerals that are beneficial to human health. It exhibits high antioxidant activity as determined based on DPPH assay. It also exhibits powerful secondary antioxidant potential as measured by the iron (II) chelating experiment (Lim et al., 2007). The lipophilic antioxidants of the fruit are also available such as lutein, Zea xanthin and α-tocopherol (Table 1) (Isabelle et al., 2010). The edible portion is 68% of the fruit weight. In 100 g of edible portion, it contains water 84 g, a small amount of protein and fat, carbohydrates 14.2 g (mainly reducing sugar, predominantly glucose), fiber 0.8 g, ash 0.6 g, some minerals such as Ca 19 mg and K 275 mg, and some vitamin B1 and B2.
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281
FIGURE 1 Lansium domesticum; tree and bunch of fruit. Source: https://en.wikipedia.org/wiki/Lansium_parasiticum#/ media/File:Lanzones.jpg
FIGURE 2 Lansium domesticum; peeled fruit with 5 separate segments. Source: https://en.wikipedia.org/wiki/Lansium_parasiticum#/ media/File:Lanzones_fruits_-_Mindanao,_Philippines.jpg
The profiles of the organic acids such as malic, ascorbic, citric, and piroglutamic acids are contained in langsat fruit. The major organic acids in langsat fruits are malic and citric acid with the concentration of 0.691% and 0.391%, respectively (Pontoh et al., 2015).
SENSORY CHARACTERISTICS The fruit contains 15 seeds, flat, and are bitter tasting; the seeds are covered with a thick, clear-white aril that tastes sweet and sour. The taste of langsat is sour as the pH of the fruit is low at about 3.85. This is agreed with the total titratable acidity of fruit is about 1.04% (Pontoh et al., 2015). The taste has been likened to a combination of grape and grapefruit and is considered excellent by most. The sweet juicy flesh contains sucrose, fructose, and glucose. Its sugar content varies from 13 to 24 Brix (Salma and Razali, 1987). For consumption, cultivars with small or undeveloped seeds and thick aril are preferred.
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TABLE 1 Chemical Composition, Antioxidant Activity and Nutritional Value of Langsat (Lansium domesticum) Characteristic
Pulp of langsat
Moisture (%)
81.086.5
a
TPC (mg GAE/g FW)
1.001.48
Ascorbic acid (μg/g FW)
0.33.0
b
H-ORAC (μmol TE/g FW) EC50c
(μg/mL)
Peel of langsat
140.5
6.45 0.25
Calcium (mg/100 g FW)
20.0
Phosphorus (mg/100 g FW)
30.0
Carotene; vitamin A (I.U.)
13.0
47.94
Ellagic acid (mg/g DW)
0.23
Corilagin (mg/g DW)
0.11
a
Total phenolics expressed as milligrams of gallic acid equivalents per gram fresh weight basis (mg GAE/g FW). Hydrophilic ORAC data expressed as micromoles of Trolox equivalents per gram fresh weight basis (μmol TE/g FW). c EC50 value is the effective concentration value at which the DPPH radical is scavenged by 50%. Source: Data are modified from Isabelle, M., Lee, B.L., Lim, M.T., Koh, W.P., Huang, D., Ong, C.N., 2010. Antioxidant activity and profiles of common fruits in Singapore. Food Chem. 123, 7784 (Isabelle et al., 2010), Kee, M.E., Khoo, H.E., Sia, C.M., Yim, H.S., 2015. Fractionation of potent antioxidative components from langsat (Lansium domesticum) peel. Pertanika J. Trop. Agric. Sci. 38, 103112 (Kee et al., 2015), Samuagam, L., Khoo, H.E., Akowuah, G.A., Okechukwu, P.N., Yim, H.S., 2014. HPLC analysis of antioxidant compounds in some selected tropical fruit’s peel. Innovative Rom. Food Biotechnol. 14, 6168 (Samuagam et al., 2014), Tilaar, M., Wih, W.L., Ranti, A.S., Wasitaatmadja, S.M., Suryaningsih, Junardy, F.D., Maily, 2008. Review of Lansium domesticum Correˆa and its use in cosmetics. Bol. Latinoam. Caribe Plant. Med. Aroma´t. 7, 183189 (Tilaar et al., 2008). b
HARVEST AND POSTHARVEST CONSERVATION Fruits are ready to harvest 140150 days from flower formation. Do the harvesting early in the morning or late in the afternoon. The harvesting index of langsat fruit is indicated by the skin color changing from light to dark yellow. At the full-ripe stage, the other occurrences are dryness of the sepals and loss of the green color from the peduncle or the stem. Fruit ripening are generally over a very short period. They should be harvested as soon as possible, as overripe fruit easily abscise from the peduncle. Pack the fruits in carton box with newspaper, dried leaves or foam. However, fruit are harvested at 70%80% ripe to avoid excessive fruit drop during long distance transportation. The main problem after harvest of langsat fruit is mechanical injury, loss of weight and browning appearance of peel, as the fruit peel is highly perishable. The short shelf-life of the fruit freshness could be the reason why the fruits are sold only locally from where they are picked. The harvested fruit should be sorted cleaned, graded and packed in cartons or crates with liners or cushion to reduce damage during handling. After harvest, langsat fruits are spoiled after 4 days at room temperature. Pre-cooling conditions such as room cooling is recommended. Stored fruit at 15 C developed skin browning symptoms after 21 days according to the chilling sensitivity. Chilling injury symptoms are not only brown scalding but also pitting of the skin. However, they can be kept in cold storage for 2 weeks at 13 C and relative humidity (RH) of 85%90% (Srivastana and Mathur, 1955). Sugar content increases over this period, while acidity rises only up to the seventh day and then gradually declines. Fruits treated with fungicide and stored under controlled atmosphere condition of 5% O2 without CO2 at 13 C with 85%90% RH, have remained in good condition for more than 2 weeks as compared to fruit held in atmospheric areas (Yahia, 1998). High CO2 promotes browning and elevates acidity. Increasing the CO2 from 0% to 5% did not increase the acidity of fruit. Packaging into a plastic bag reduces weight loss but increases surface browning due to the accumulation of CO2 in the package (Brown and Lizada, 1984; Phatdiphan, 2007). Coating, such as chitosan solution, reduces weight loss, increases sweetness, retains high content of vitamin C, but some causes browning over at least half the surface within 5 days in storage.
POTENTIAL INDUSTRIAL APPLICATION The flesh of the langsat is practically eaten fresh out of hand, or served as a dessert. In addition, it may be cooked in various ways depending on the area. Peeled and seedless fruit can be processed to fruit in syrup, beverages and sometimes candied.
Langsat—Lansium domesticum
283
As the langsat is cultivated mainly for its fruit, in some areas, the peel of langsat has been traditionally used as medicine. Langsat peel possesses strong antimicrobial activity against Candida lipolytica (Mohamed et al., 1994). The peel, rich in oleoresin, is used against diarrhea and intestinal spasms. Huang et al. (2010) reported a higher total antioxidant capacity, total phenolic content, and carotenoids were investigated in the peel of langsat. Moreover, the dried peel is burned in Java, the aromatic smoke serving as a mosquito repellent and as incense in the rooms of sick people. Three onoceranoid triterpenes were isolated from the fruit peel of L. domesticum. They exhibited mild toxicity against brine shrimp (Artemia salina). In the nonedible portion of langsat, 5 main tetranorterpenoid, domesticulide A-E, were isolated from seed together with 11 known triterpenoids. The seed extract are also a rich source of limonoids including andirobin derivates, methyl angolensates, mexicanolides, an azadiradione, onocerannoids and dukunolides. Some class showed antimalarial activity against Plasmodium falciparum with IC50 of 2.49.7 μg/mL. Therefore, the crushed seeds are used to treat fevers and the astringent bark which is administered against dysentery and malaria. The dried Hydroethanol extract of L. domesticum fruit can be used as cosmetic. It is used as a skin care product for depigmentation and moisturizing (Tilaar et al., 2008).
REFERENCES Brown, B.I., Lizada, M.C.C., 1984. Modified atmospheres and deterioration of lanzones (Lansium domesticum Correa.). Postharvest Res. Notes 1, 36. Huang, W.Y., Cai, Y.Z., Corke, H., Sun, M., 2010. Survey of antioxidant capacity and nutritional quality of selected edible and medicinal fruit plants in Hong Kong. J. Food Compos. Anal. 23, 510517. Isabelle, M., Lee, B.L., Lim, M.T., Koh, W.P., Huang, D., Ong, C.N., 2010. Antioxidant activity and profiles of common fruits in Singapore. Food Chem. 123, 7784. Kee, M.E., Khoo, H.E., Sia, C.M., Yim, H.S., 2015. Fractionation of potent antioxidative components from langsat (Lansium domesticum) peel. Pertanika J. Trop. Agric. Sci. 38, 103112. Lim, Y.Y., Lim, T.T., Tee, J.J., 2007. Antioxidant properties of several tropical fruits: a comparative study. Food Chem. 103, 10031008. Mohamed, S., Hassan, Z., Abd Hamid, N., 1994. Antimicrobial activity of some tropical fruit wastes (guava, starfruit, banana, papaya, passionfruit, langsat, duke, rambutan and rambai). Pertanika J. Trop. Agric. Sci. 17, 219227. Morton, J., 1987. Langsat. Fruits of Warm Climates. Julia F. Morton, Miami, FL, pp. 201203. Phatdiphan, S., 2007. Prolonging storage life of langsat under modified atmosphere conditions. Agric. Sci. J. 35, 234237 (in Thai with English abstract). Pontoh, J., Kamu, V.S., Sitorus, L.P., 2015. Analysis of organic acid in Landsat (Lansium domesticum var pubescens) and Duku (Lansium domesticum var domesticum) fruits by reversed phase HPLC technique. Int. J. ChemTech Res. 8, 238242. Salma, I., Razali, B., 1987. The reproductive biology of duku langsat, Lansium domesticum Corr. (Meliaceae), in Peninsular Malaysia. Mardi Res. Bull. 15, 141150. Samuagam, L., Khoo, H.E., Akowuah, G.A., Okechukwu, P.N., Yim, H.S., 2014. HPLC analysis of antioxidant compounds in some selected tropical fruit’s peel. Innovative Rom. Food Biotechnol. 14, 6168. Srivastana, H.C., Mathur, P.B., 1955. Studies in the cold storage of langsat. J. Sci. Food Agric. 6, 511513. Tilaar, M., Wih, W.L., Ranti, A.S., Wasitaatmadja, S.M., Suryaningsih, Junardy, F.D., Maily, 2008. Review of Lansium domesticum Correˆa and its use in cosmetics. Bol. Lainoam. Caribe de Plant. Med. Aroma´t. 7, 183189. Yahia, E., 1998. Modified and controlled atmosphere for tropical fruits. Hortic. Rev. 22, 123183.
FURTHER READING Tanaka, T., Ishibashi, M., Fujimoto, H., Okayama, E., Moyano, T., Kowithayakorn, T., et al., 2002. New onoceranoid triterpene constituents from Lansium domesticum. J Nat. Prod. 65, 17091711.
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Loquat/Nispero—Eriobotrya japonica Lindl. Moˆnica M. de Almeida Lopes1, Alex Guimara˜es Sanches1, Kellina O. de Souza1 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Origin and Botanical Aspects Production Postharvest and Nutritional Value Postharvest Conservation
285 285 286 288
Potential Industrial and Medicinal Uses References Further Reading
289 290 292
ORIGIN AND BOTANICAL ASPECTS The loquat (Eriobotrya japonica Lindl.), also known as the Japanese plum tree and the yellow plum tree, is a plant of the Rosaceae family and Pomoideas subfamily, and with its origin in southwest China. The loquat fruits are spread in worldwide, as observed in various regions of Asian continent (Japan, India, Madagascar, and South Korea), Mediterranean (Spain, France, Turkey, Greece, Portugal and Italy) and across the Americas (United States, Brazil, Argentina, and Chile) (Caballero and Ferna´ndez, 2004; Gong et al., 2015). The species can reach up to 10 m in height, but in the regions of cultivation it is generally smaller, about 34 m. The canopy is rounded; the branches are velvety and composed of simple leaves, generally with elliptic-lanceolate format of rigid texture and serrated border with size ranging from 10 to 25 cm and a very accentuated coloration in tone of dark green in the upper face and white or rusty on the underside. The flowers are about 2 cm in diameter, white, sweetly fragrant, with five petals and produced in bunches with three to ten flowers and, before opening, have a velvety texture (Lin et al., 1999; Delucchi and Keller, 2010). Loquat fruits are considered to be fruits of pommel type, with the fleshy portion composing a small floral container (35 cm in diameter) and a shape varying from spherical to oval and a unit weight of about 1080 g. The peel shows a velvety texture of a yelloworange and sometimes pink color (Pio et al., 2007a,b). The pulp is juicy, presenting a pleasant aroma with a coloration ranging from white to orangesalmon, rich in vitamin C and minerals such as calcium and phosphorus. The pulp is firm and fleshy, or more softened, and the flavor varies from sweet to acidic depending on the variety and stage of maturation. The seeds are located in the center of the fruits, and often found in number of 35 per fruit with brown coloration. The trunk is relatively short and the root system is characterized as superficial, extending approximately 2530 cm deep (Rodrı´guez, 1983; Ojima et al., 1999; Delucchi and Keller, 2010).
PRODUCTION According to Pio et al. (2008) the cultivation of loquat has intensified in the world due to the excellent organoleptic and nutraceutical qualities and reduced phytosanitary problems. In Brazil, the cultivation is concentrated between the months of July and September, when there is a shortage of other fruits in the market that can be processed industrially in the manufacture of sweets, mainly due to the richness of pectin in these fruits (Melo and Lima 2003; Grassi et al., 2010). The loquat adapts very well to temperate and subtropical regions whose average annual temperature is above 15 C. Cultivation is best at altitudes above 600 m in deep soils rich in organic matter combined with an annual average Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00037-X © 2018 Elsevier Inc. All rights reserved.
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rainfall of 12001800 mm of water and good drainage as the species is intolerant to environments with high soil moisture (Hartmann et al., 2002; Scaloppi Ju´nior et al., 2004). The propagation is carried out mainly by seeds because the species has low rooting capacity (,15%), especially using herbaceous cuttings (Silva and Pereira, 2004). According to Pio et al. (2007b) the seeds must be extracted from ripe fruits, dried in the shade and sown in about a week, thus ensuring their germination. In storage cases, the seeds can be stored in plastic bags of low density polyethylene and kept in a refrigerator at 8 C for up to 180 days (Brasileiro et al., 2011). Grafting is a common practice in the culture being done in seedlings (rootstock) or quince trees that induces dwarfism in the plants, allowing a denser spacing and giving rise to a more compact orchard. Pio et al. (2006) explain that the practices of soil correction and fertilization for the crop must be made by soil analysis, applying when necessary limestone in the total area in order to raise the saturation by bases up to 70%. The fertilization should be done by applying in cover, around the seedlings and every 2 months, 60 g per plant of N, in four plots of 15 g. From the second year of planting, it is recommended to fertilize by applying 60120 g per plant of the nutrients: N, P and K; with the N with dose divided into four plots every 2 months. The production fertilization is mainly aimed at productivity and is carried out after the fourth year of planting, applying 3 t/ha of chicken manure or 15 t/ha of manure, well-turned and 60120 kg/ha of N, 2090 kg/ha of phosphorus and 20100 kg/ha of potassium. The planting of the seedlings is carried out with dimensions of 60 3 60 3 60 cm, with spacing between plants of 8 3 4 to 8 3 6 m when using the own graft of the species and in more densified spacing 5 3 3 and 4 3 2 m when the graft is the quince (Pio et al., 2008). According to Perosa et al. (2006), during the development of the loquat is essential to perform some technical operations for a good commercial production. Examples of such operations are: thinning of the fruits, leaving from 2 to 4 fruits per panicle to reach the required weight and size for commercial pattern, and the bagging of the fruits with the purpose of avoiding the attack by the fruit fly and the incidence of purplish spot (a disorder related to the intense exposure to the sun’s rays). The harvest period begins after the second year of installation of the orchard, and is quite extensive, usually from April to October, as the flowering of the loquat tree occurs in stages, being therefore much less affected when compared to other crops over the year (Pio et al., 2008). China is the world’s largest producer of loquat fruit, however, production is specifically focused for domestic market (Vicente, 2013). In Brazil, the production is concentrated mainly in the state of Sa˜o Paulo (3.7 million boxes per year), with emphasis in the area of Mogi das Cruzes, responsible for the annual production of 2 million boxes, representing 70% of national production (Pio et al., 2007b). The high productivity of the loquat in Brazil is associated with the climatic and soil conditions and mainly to the development of cultivars with high potential (Hasegawa et al., 2010). In Brazil the cultivars of loquat are divided into two groups: white pulp and orange pulp. The most commonly used are: Mizuho, Precoce de Itaquera and Precoce de Campinas IAC 16531, Parmogi IAC 26617, Crystal Nectar IAC 8667, Centenarian IAC 1567420, Mizumo IAC 1567411 and Mizauto IAC 1674 (Babosa et al., 2003; Bettiol Neto et al., 2010).
POSTHARVEST AND NUTRITIONAL VALUE The fruit maturation involves a set of changes as increase in respiration and ethylene rates, as well as changes in color, taste, texture, and consequently determines sensory quality and shelf-life of fruits (Chitarra and Chitarra, 2005). There are a few and contradictory reports on the maturation of loquat fruit that, due to the nonmodification of ethylene and CO2 production, both before and after harvesting, has been classified as nonclimacteric fruit (Ding et al., 1998; Sanches et al., 2011; Edagi et al., 2011). According to Campos et al. (2007), a study of the respiratory activity of loquat fruit and the influence of ethylene on maturation process would help to improve handling and storage techniques, even though nonclimacteric fruit does not produce high ethylene production, but these may be sensitive to this phytoregulator during ripening and the postharvest. Due to the nonclimacteric characteristic it is fundamental to harvest at the ideal maturity in order to guarantee the quality during storage (Abbasi et al., 2013). Undurraga et al. (2011) notes that the first indications of maturation of the loquat are observed by changes related to the change of color from green to orange or yellow (Fig. 1), at this stage the fruits are already mature and can be stored or transported for the long distances. The changes in the color of peel involves the alteration in two main groups of pigments: the degradation of chlorophyll responsible for the green coloration in the immature fruits and the synthesis of carotenoids responsible for the yellow or orange coloring of the loquat, being mainly β-carotene and β-cryptoxanthin and at lower concentrations lutein, violaxanthin, α-carotene and γ-carotene (Ding et al., 2006; Petriccione et al., 2015).
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FIGURE 1 Different maturation stages of loquat fruit.
The texture changes occur after the harvesting and is characterized by the softening of the pulp due to modifications in the cell wall structure as the solubilization of pectin by the action of specific enzymes such as polygalacturonases (PG). The PG transforms the polymers of galacturonic acids in water-soluble pectic acids, thus creating a serious problem during loquat storage, due to the increase of susceptibility to mechanical injury and deterioration (Yang et al., 2008). The main sugars accumulated during maturation are glucose, fructose, sucrose, and sorbitol (Amoro´s et al., 2003; Xu and Chen, 2011). Galactose was found in small concentrations (#0.1%) (Cao et al., 2013). In unripe loquat, fructose and sorbitol, which are at higher levels, are reduced considerably during development, and sucrose increases rapidly with progress of development, becoming the predominant sugar (Amoro´s et al., 2003). Glucose, fructose, sucrose, and sorbitol have different sweetening powers in fruits and the variations between these sugars and their concentrations are important for the formation of different sweet tastes, both between maturation stages and various cultivars of loquat fruit (Ding et al., 2006; Pareek et al., 2014). As regards the composition of organic acids in loquat pulp during development, Chen et al. (2009) reported that the main ones are malate and quinate, and in small amounts: isocitrate, α-ketoglutarate, fumarate, oxaloacetate, tartrate, ferule, cis-aconitate and β-coumarate. At maturation, the organic acids with the highest concentration in loquat pulp are malic, citric, succinic, fumaric, tartaric, and ascorbic (Amoro´s et al., 2004; Pareek et al., 2014). The malic acid represents approximately 90% of the organic acids present, being the main component responsible for the acidity of this fruit. The ideal harvest time of loquat fruit is when the characteristics during development and ripening are observed, including: values of luminosity variable L are between 61 and 64, parameters a and b (0.170.21), firmness (3.04.0 N), soluble solids (5.06.0 Brix), titratable acidity (1.01.5 g/100 g malic acid), ratio SS/AT (6.06.5), and pH (3.403.60) (Amoro´s et al., 2004; Tian et al., 2007). The nutritional composition of the loquat consists of moisture (86.5%90.2%), calories (47168 kcal), carbohydrates (9.643.3 g/100 g), fibers (0.8%1.7%), proteins (0.431.4 g/100 g), lipids (0.20.7 g/100 g), Ash (0.40.5 g/100 g), vitamin C (3.010 g/100 g) and minerals such as calcium (1670 g/100 g), iron (0.281.4 g/100 g), magnesium (913 g/100 g), manganese (0.051.0 g/100 g), phosphorus (20126 g/100 g), potassium (2661216 g/100 g) and sodium (0.51 g/100 g) (Barreto et al., 2009; Hasegawa et al., 2010; Pareek et al., 2014; Wei et al., 2017) (see Table 1).
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TABLE 1 Nutritional Composition of Loquat Fruit Nutrient
Pulp
References
Moisture (%)
86.590.2
Hasegawa et al. (2010)
Protein (g/100 g)
0.431.4
Barreto et al. (2009)
Calories (kcal)
47168
Pareek et al. (2014)
Carbohydrates (g/100 g)
9.643.3
Pareek et al. (2014)
Lipids (g/100 g)
0.20.7
Barreto et al. (2009)
Fibers (%)
0.81.7
Barreto et al. (2009)
Ash (g/100 g)
0.400.50
Hasegawa et al. (2010)
Sucrose (g/100 g)
1.018.0
Hasegawa et al. (2010), Wei et al. (2017)
Ascorbic acid (mg/100 g)
3.010.0
Barreto et al. (2009), Hasegawa et al. (2010)
Potassium
2661216
Barreto et al. (2009), Pareek et al. (2014)
Phosphorous
20126
Barreto et al. (2009), Pareek et al. (2014)
Calcium
1670
Barreto et al. (2009), Pareek et al. (2014)
Iron
0.281.40
Barreto et al. (2009), Pareek et al. (2014)
Manganese
0.051.0
Barreto et al. (2009), Pareek et al. (2014)
Magnesium
9.013.0
Barreto et al. (2009), Pareek et al. (2014)
Sodium
0.51.0
Barreto et al. (2009), Pareek et al. (2014)
Minerals (mg/100 g)
Sources: Barreto et al., 2009; Hasegawa, P.N., Faria, A.F., Mercadante, A.Z., Chagas, E.A., Pio, R., Lajolo, F.M., et al., 2010. Chemical composition of five loquat cultivars planted in Brazil. Cieˆnc. Tecnol. Aliment. 30 (2), 552559; Pareek, S., Benkebia, N., Janick, B.J., Caod, S. and Myhaia, E. 2014. Postharvest physiology and technology of loquat (Eriobotrya japonica Lindl.) fruit. J. Sci. Food Agric. 3 (2), 110; Wei, Y., Xu, F., Shao, X., 2017. Changes in soluble sugar metabolism in loquat fruit during different cold storage. J. Food Sci. Technol. 54 (5), 10431051.
According to Zhou et al. (2011) the phenolic profile of the loquat tree varies according to the growth, maturation stage, genetic factors of each cultivar, environmental conditions, and extraction methods. This variation was also reported by Akbulut et al. (2016), who evaluated different genotypes of loquat pulp, and found mean values of total phenolic compounds (22263 μg GAE/g), flavonoids (3.6836.22 μg of rutin/g), total carotenoids (7.6244.30 μg of β-carotene/g) and vitamin C (2.8011.62 mg/100 g). In a study of the phenolic and antioxidant capacity present in the peel and pulp of six loquat tree cultivars, HPCL 18 compounds were identified (8 derivatives of hydroxycinnamic acid and 10 glycosides flavonoids). The quantification of these compounds revealed distinct profiles among the evaluated cultivars, highlighting predominantly the 3- and 5-caozoylquinic acids, and 5-feruloylquinic acids, and loquat pulp exhibited the smallest amounts of phenolics (Ferreres et al., 2009). Zhang et al. (2015) identified and quantified eleven phenolic compounds in the peel and pulp of different loquat cultivars, among them: 3-p-coumaroilquinoline (3-p-CoQA), 5-caozoylquinic acid (5-CQA), 4-caozoylquinic acid (4-CQA), 3-caozoylquinic acid, 5-feruloylquinic acid (5-FQA), quercetin-O-galactoside (Q-3-Gal), quercetin-3-Oglucoside (Q-3-Glu), quercetin-3-O-(Q-3-Rha), kaempferol-3-O-galactoside (K-3-Gal), kaempferol-3-O-rhamnoside (K-3-Rha) and kaempferol-3-O-glucoside (K-3-Glu), with 3-CQA and -CQA predominant phytochemicals in peel and pulp of the loquat fruit. These same authors evaluated the antioxidant potential by the DPPH, ABTS and FRAP methods and found a good correlation between the antioxidant compounds present in the peel (64.15100) with the pulp (54.4997.95) in different cultivars, characterizing the loquat as excellent source of phytochemicals and natural antioxidants.
POSTHARVEST CONSERVATION The modified atmosphere condition, such as packaging and plastic films, provides a microatmosphere with greater relative humidity than the external environment by altering the rate of transpiration and, consequently, reduces water loss and changes associated to the color, texture, and biochemical compounds of loquat fruits (He et al., 2004). Controlled
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289
atmosphere involving the modification of gas concentration as the increase of CO2 and the reduction of O2, are also excellent alternatives to increase the shelf-life of the loquat fruit, reducing the injury caused by cold (Pareek et al., 2014). Campos et al. (2007) showed that when stored in polyethylene terephthalate trays, coated with a 10 μm PVC plastic film and stored at 6 C, the loquat presented lower respiration rate and ethylene production with lower loss of fresh mass and maintenance of sugar contents such as glucose, sucrose, and fructose for 18 days of storage compared to storage at 18 C. The use of 30 μm polypropylene plastic film, associated with refrigerated storage at 3 C, reduced the respiration rate and delayed the conservation of loquat fruit for 40 days (Amoro´s et al., 2008). Sanches et al. (2011) also reported that loquat fruit cv. Precoce of Itaquera coated with polypropylene film and stored in refrigeration at 1 C preserved their physicochemical characteristics, as well maintained the levels low of CO2 and O2 for 48 days of storage. In the controlled atmosphere, the loquat fruit could be stored at 10 kPa O2 1 1 kPa CO2 for 50 days at 1 C with good flavor and low incidence of quality loss (Ding et al., 2006). In these same controlled atmosphere conditions (10% O2 1 1% CO2) was observed little effects on flavor of loquat fruit, but the activity of enzymes such as polygalacturonase (PG), polyphenoloxidase (PPO) and peroxidase (POD) were reduced after 24 h of storage at 1 C (Gao et al., 2006). Technology related to the use of blockers or inhibitors of ethylene synthesis such as 1-methylcyclopropene (1-MCP), potassium permanganate (KMnO4), and salicylate compounds such as salicylic acid (SA) and methyl salicylate have been widely used in postharvest processing of loquat. Although the maturation of nonclimacteric fruits seems to be independent of the action of ethylene, some studies have found responses of these fruits to the presence of exogenous ethylene, stimulating respiration and accelerating maturation processes (Edagi et al., 2011). Cai et al. (2006a) observed that the application of 1-MCP in loquat fruits delayed the symptoms of cold injury and decreased the activity of the PPO, responsible for darkening in pulp. Similarly, Cao et al. (2010) and Zheng et al. (2010) evaluating the loquat fruits, observed that 1-MCP inhibited the activity of PPO, POD, PG and pectin methyl esterase (PME), besides the precursors enzymes of the metabolism of ethylene like ACC sintase and ACC oxidase. Cao et al. (2011) observed that loquat treated with 50 nL/L of 1-MCP during 24 h at 20 C and stored at 1 C for 35 days exhibited a lower incidence of quality loss and higher levels of total soluble solids, titratable acidity, fructose, glucose, sucrose, total phenolics and total flavonoids in relation to untreated fruits. According to Campos et al. (2007) the use of ethylene oxidants, such as potassium permanganate, has the purpose of reducing the ethylene released by loquat fruit during ripening process. These same authors concluded that loquat stored at 6 C for 20 days after application of potassium permanganate sachets presented a less respiratory activity and ethylene production, as well as lower loss fresh mass and degradation of vitamin C and soluble sugars when compared to the group control. Salicylated compounds such as SA and methyl jasmonate (MeJa) salicylic acid act primarily to reduce the free radicals and the activity of POD, which causes browning of fruit pulp and peel (Ding et al., 2006).
POTENTIAL INDUSTRIAL AND MEDICINAL USES The highest consumption of loquat is in natura, due to peculiar flavor and nutritional and functional compounds (Sanches et al., 2011). However, the low shelf-life during postharvest has allowed fruit consumption via being processed into jellies, jams, and jellies, among others (Hasegawa et al., 2010). Temiz et al. (2012) developed yoghurts using with loquat pulp that was widely accepted by consumers. The authors observed the maintenance of the physicochemical compounds during 18 days of storage and reported that the sensorial attributes as appearance, taste, and flavor were preferred by the evaluators. Curi et al. (2017) developed jellies with different cultivars of loquat fruit and reported good acceptance by consumers that prefer loquat jellies that are more acidic, less sweet, less firm or softer with a more intense red color. The phytochemical present in leaves, peels, seeds and pulp of the loquat ensure their potential use in the pharmacological industry as antiinflammatory, anticancer, hepatoprotective, anti-HIV, among others (Baljinder et al., 2010). Extracts from loquat leaves presents the phytochemical identified as sesquiterpene glycoside, an important compound with hypoglycemic effect, capable of inhibiting the development of diabetes and reduces cardiovascular complications (Chen et al., 2008; Ceylan-Isik et al., 2008). Said et al. (2009) evaluated a clinical study with 41 human volunteers with hypercholesterolemia, a problem associated with obesity, diabetes mellitus and hypertension, and observed that the patients presented a reduction of hypolipidemic activity during a diet with loquat leaves extract. Huang et al. (2009) and Zar et al. (2014) observed that the extract of the loquat leaves significantly reduced lung inflammation in alveolar macrophages and edemas in the ear and rat paws respectively. Loquat seeds extracts also showed in vivo antiinflammatory effects on hamsters through inhibition of mucositis, epithelial lesion and bacterial infection induced by chemotherapy and allergic dermatitis (Sun et al., 2010). Studies have demonstrated that loquat extracts can suppress the onset of cancer or reduce its effects at different stages of progression. According to Kim et al. (2011), loquat extracts composed of water and ethanol inhibited the development of breast cancer and the proliferation of tumor cells in rats.
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Exotic Fruits Reference Guide
The compounds identified as 3-O-(E)-p-coumaroylole triterpenic acids and trichloroacetic acid isolated from the methanol extracts of loquat leaf presented cytotoxicity against human cell cancer inducing apoptotic cell death through the mitochondria (Kikuchi et al., 2011). The loquat extracts showed other activities, such as improvement of liver function (Bae et al., 2010; Yoshioka et al., 2010), reduction of kidney problems (Hamada et al., 2004), inhibition of neurodegenerative cells (Kim et al., 2011), and antithrombotic potential (Lee et al., 2004), reduction of obesity-related disorders (Tanaka et al., 2010) antiaging (Muramoto et al., 2011) and antiallergic effects (Kim and Shin, 2009) among others. According to Liu et al. (2016), the of bioactive compounds present in the extracts of different loquat organs are still being studied for introduction into processed, functional and therapeutic food products once their benefits to human health have been identified.
REFERENCES Abbasi, N.A., Akhtar, A., Hussain, A., 2013. Maintaining quality of loquat (Eriobotrya japonica lindl.) Fruit after harvest. Pak. J. Bot. 45 (1), 247251. Akbulut, M., Gozlekci, S., Ercisli, S., Cakir, O., 2016. Morphological, biochemical and antioxidant properties of local loquat (Eriobotrya japonica (Thunb.) Lindl.) germplasm from Turkey. Erwerbs Obstbau 41, 17. Amoro´s, A., Zapata, P., Pretel, M.T., Botella, M.A., Serrano, M., 2003. Physicochemical and physiological changes during fruit development and ripening of five loquat (Eriobotrya japonica Lindl.) cultivars. Food Sci. Technol. Int. 9, 4351. Amoro´s, A., Zapata, P., Pretel, M.T., Botella, M.A., Almansa, M.S., Serrano, M., 2004. Role of naphthalene acetic acid and phenothiol treatments on increasing fruit size and advancing fruit maturity in loquat. Sci. Hortic. 101 (3), 387398. Amoro´s, A., Pretel, M.T., Zapata, P.J., Botella, M.A., Romojaro, F., Serrano, M., 2008. Use of modified atmosphere packaging with microperforated polypropylene films to maintain postharvest loquat fruit quality. Food Sci. Technol. Int. 14, 95103. Babosa, W., Pommer, C.V., Ribeiro, M.D., Veiga, R.F.A., Costa, A.A., 2003. Distribuic¸a˜o geogra´fica e diversidade varietal de frutı´feras e nozes de clima temperado no Estado de Sa˜o Paulo. Rev. Bras. Frutic. 25 (2), 341344. Bae, D., You, Y., Yoon, H.G., Kim, K., Lee, Y.H., Kim, Y., et al., 2010. Protective effects of loquat (Eriobotrya japonica) leaves against ethanolinduced toxicity in HepG2 cells transfected with CYP2E1. Food Sci. Biotechnol. 19, 10931096. Baljinder, S., Seema, G., Dharmendra, K., Vikas, G., Parveen, B., 2010. Potential of Eriobotrya japonica an overview. Int. Res. J. Pharm. Pharmacol. 1, 9599. Barreto, G.P.M., Benassi, M.T., Mercadante, A.Z., 2009. Bioactive compounds from several tropical fruits and correlation by multivariate analysis to free radical scavenger activity. J. Braz. Chem. Soc. 20, 18561861. Bettiol Neto, J.E., Dall’Orto, F.A.C., Barbosa, W., Chagas, E.A., Pio, R., Costa, F.C., 2010. Potencial produtivo de novas selec¸o˜es de nespereiras. Cieˆnc. Rural. 40 (6), 12771282. Brasileiro, B.G., Silva, D.F.P. Da, Bhering, M.C., Moura, E.B.B., Bruckner, C.H., 2011. Qualidade fisiolo´gica de sementes de neˆspera armazenadas em diferentes embalagens. Rev. Bras. Frutic. 2, 686691. Caballero, P., Ferna´ndez, M.A., 2004. Loquat, production and market. Options Me´diterrane´ennes 58 (1), 120. Cai, C., Chen, K., Xu, W., Zhang, W., Li, X., 2006a. Effect of 1MCP on postharvest quality of loquat fruit. Postharvest Biol. Technol. 41, 155162. Campos, J.T., Hasegawa, P.N., Purgatto, E., Lajolo, F., Cordenunsi, B.R., 2007. Qualidade po´s-colheita de neˆsperas submetidas ao armazenamento sob baixa temperatura e atmosfera modificada. Cieˆnc. Tecnol. Aliment. 27 (2), 401407. Cao, S., Zheng, Y., Yang, Z., 2011. Effect of 1-MCP treatment on nutritive and functional properties of loquat fruit during cold storage. Crop Hortic. Sci. 39, 6170. Cao, S., Yang, Z., Zheng, Y., 2013. Sugar metabolism in relation to chilling tolerance of loquat fruit. Food Chem. 136, 139143. Cao, S.F., Zheng, Y.H., Wang, K.T., Rui, H.J., Shang, H.T., Tang, S.S., 2010. The effects of 1-methylcyclopropene on chilling and cell wall metabolism in loquat fruit. J. Hortic. Sci. Biotechnol. 85, 147153. Ceylan-Isik, A.F., Fliethman, M.R., Wold, E.L., Ren, J., 2008. Herbal and traditional Chinese medicine for the treatment of cardiovascular complications in diabetes mellitus. Current Diabetes Reviews. Evidence-Based Complementary Altern. Med. 4, 320328. Chen, J., Li, W.L., Wu, J.L., Ren, B.R., Zhang, H.Q., 2008. Hypoglycemic effects of a sesquiterpene glycoside isolated from leaves of loquat (Eriobotrya japonica (Thunb.) Lindl.). Phytomedicine 15 (12), 98102. Chen, F.X., Liu, X.H., Chen, L.S., 2009. Developmental changes in pulp organic acid concentration and activities of acid-metabolising enzymes during the fruit development of two loquat (Eriobotrya japonica Lindl.) cultivars differing in fruit acidity. Food Chem. 114, 657664. Chitarra, A.B., Chitarra, M.I.F., 2005. Po´s-colheita de frutos e hortalic¸as: fisiologia e manuseio. Second edition, Lavras, UFLA, 783 pp. Curi, P.N., Nogueira, P.V., Almeida, A.B.De, Carvalho, CdosS., Pio, R., Pasquali, M., 2017. Processing potential of jellies from subtropical loquat cultivars. Food Sci. Technol. 37 (1), 7075. Delucchi, G., Keller, H., 2010. The naturalization of loquat, Eriobotrya japonica (Rosaceae, Maloideae) in Argentina. Bonplandia 19 (1), 7177. Ding, C.K., Chachin, K., Hamauzu, Y., Ueda, Imahori, Y., 1998. Effects of storage temperatures on physiology and quality of loquat fruit. Postharvest Biol. Technol. 14, 309315. Ding, Z., Tian, S., Wang, Y., Li, O., Chan, Z., Han, J., et al., 2006. Physiological response of loquat fruit to different storage conditions and its storability. Postharvest Biol. Technol. 41, 143150.
Loquat/Nispero—Eriobotrya japonica Lindl.
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Edagi, F.K., Sasaki, F.F., Sestari, I., Terra, F.A.M., Giro, B., Kluge, R.A., 2011. 1-metilciclopropeno e salicilato de metila reduzem inju´rias por frio em neˆspera ‘Fukuhara’ refrigerada. Cieˆnc. Rural 41 (5), 910916. Ferreres, F., Gomes, D., Valenta˜o, P., Gonc¸alves, R., Pio, R., Chagas, E.A., et al., 2009. Improved loquat (Eriobotrya japonica Lindl.) cultivars: variation of phenolics and antioxidative potential. Food Chem. 114, 10191027. Gao, H.Y., Chen, H.J., Chen, W.X., Yang, J.T., Song, L.L., Zheng, Y.H., 2006. Effect of hypobaric storage on physiological and quality attributes of loquat fruit at low temperature. Acta Hortic. 712, 269273. Gong, R.G., Lai, J., Yang, W., Liao, M.A., Wang, Z.H., Linag, G.L., 2015. Analysis of alterations to the transcriptome of Loquat (Eriobotrya japonica Lindl.) under low temperature stress via de novo sequencing. Genet. Mol. Res. 14 (3), 94239436. Grassi, A.M., Scarpare Filho, J.A., Chagas, E.A., Pio, R., Sanches, J., Cia, P., et al., 2010. Avaliac¸a˜o na intensidade de raleio na qualidade de frutos de nespereira. Bragantia 69 (1), 215220. Hamada, A., Yoshioka, S., Takuma, D., Yokota, J., Cui, T., Kusunose, M., et al., 2004. The effect of Eriobotrya japonica seed extract on oxidative stress in adriamycininduced nephropathy in rats. Biol. Pharm. Bull. 27, 19611964. Hartmann, H.T., Kester, D.E., Davies Jr, F.T., Geneve, R.L., 2002. Plant Propagation: Principles and Practices. seventh ed. Prentice Hall, New Jersey, NJ, 880 pp. Hasegawa, P.N., Faria, A.F., Mercadante, A.Z., Chagas, E.A., Pio, R., Lajolo, F.M., et al., 2010. Chemical composition of five loquat cultivars planted in Brazil. Cieˆnc. Tecnol. Aliment. 30 (2), 552559. He, Z.G., Li, W.X., Lin, X.Z., Lin, H., Zhuang, L.X., 2004. Effects of storage temperature and gas composition on loquat quality. J. Fruit Sci. 21, 438442. Huang, Y., Li, J., Meng, X.M., Jiang, G.L., Li, H., Cao, Q., et al., 2009. Effect of triterpene acids of Eriobotrya japonica (Thunb.) Lindl. leaf and MAPK signal transduction pathway on inducible nitric oxide synthase expression in alveolar macrophage of chronic bronchitis rats. Am. J. Chin. Med. 37, 10991111. Kikuchi, T., Akazawa, H., Tabata, K., Manosroi, A., Manosroi, J., Suzuki, T., et al., 2011. 3-O-(E)-p-coumaroyl tormentic acid from Eriobotrya japonica leaves induces caspase-dependent apoptotic cell death in human leukemia cell line. Chem. Pharm. Bull. 59, 378381. Kim, M., You, M., Rhyu, D., Jeong, K., Kim, Y., Baek, H., et al., 2011. Oral administration of loquat suppresses DMBA-induced breast cancer in rats. Food Sci. Biotechnol. 20, 491497. Kim, S.H., Shin, T.Y., 2009. Anti-inflammatory effect of leaves of Eriobotrya japonica correlating with attenuation of p38 MAPK, ERK, and NFB activation in mast cells. Toxicol. In Vitro. 23, 12151219. Lee, M.H., Son, Y.K., Han, Y.N., 2004. Tissue factor inhibitory sesquiterpene glycoside from Eriobotrya japonica. Arch. Pharm. Res. 27, 619623. Lin, S., Sharpe, R.H., Janick, J., 1999. Loquat: botany and horticulture. Hortic. Rev. 23, 234276. Liu, Y., Zhang, W., Xu, C., Li, X., 2016. Biological activities of extracts from loquat (Eriobotrya japonica Lindl.): a Review. Int. J. Mol. Sci. 17 (12), 1983. Available from: http://dx.doi.org/10.3390/ijms17121983. Melo, A.A.M., Lima, L.C.O., 2003. Influeˆncia de treˆs diferentes embalagens de PVC na vida po´s-colheita de neˆspera. Cieˆnc. Agrotecnol. 27 (6), 13301339. Muramoto, K., Quan, R.D., Namba, T., Kyotani, S., Miyamura, M., Nishioka, Y., et al., 2011. Ameliorative effects of Eriobotrya japonica seed extract on cellular aging in cultured rat fibroblasts. J. Nat. Med. 65, 254261. Ojima, M., Martins, F.P., Campo Dall’Orto, F.A., Barbosa, W., Santos, R.R., 1999. Cultura da Nespereira. IAC, Campinas, 36 pp. (Boletim te´cnico, 185). Pareek, S., Benkebia, N., Janick, B.J., Caod, S., Myhaia, E., 2014. Postharvest physiology and technology of loquat (Eriobotrya japonica Lindl.) fruit. J. Sci. Food Agric. 3 (2), 110. Perosa, J.M.Y., Vieira, E.M.V., Nitzshe, T., 2006. Cadeia produtiva da neˆspera na regia˜o do alto tieteˆ: Indicadores econoˆmicos da produc¸a˜o e mercado atacadista. Rev. Bras. Frutic. 28 (2), 214217. Petriccione, M., Pasquariello, M.S., Mastrobuoni, F., Zampella, L., Di Patre, D., Scortichini, M., 2015. Influence of a chitosan coating on the quality and nutraceutical traits of loquat fruit during postharvest life. Sci. Hortic. 197 (2), 287296. Pio, R., Dall’Orto, F.A.C., Chagas, E.A., Barbosa, W., 2006. Aspectos te´cnicos do cultivo da nespereira. Artigo em Hypertexto. Available at: ,http:// www.infobibos.com/Artigos/2006_3/nespereira/index.htm. (accessed 09.05.17.). Pio, R., Dall’Orto, F.A.C., Chagas, E.A., Barbosa, W., Ojima, M., Cia, P., 2007a. Produc¸a˜o de cultivares de nespereira na regia˜o Leste paulista. Pesqui. Agropecu. Bras. 42 (1), 10531056. Pio, R., Dall’Orto, F.A.C., Chagas, E.A., Barbosa, W., 2007b. Aspectos te´cnicos do cultivo de neˆsperas. Piracicaba: ESALQ/USP, 28 pp. (Se´rie Produtor Rural, 34). Pio, R., Dall’Orto, F.A.C., Chagas, E.A., Barbosa, W., 2008. Aspectos te´cnicos do cultivo de neˆsperas. Piracicaba: ESALQ, Divisa˜o de Biblioteca e Documentac¸a˜o. 30 pp. (Se´rie Produtor Rural, 39). Rodrı´guez, A. 1983. El cultivo del nı´spero em el valle del AlgarGuadalest. Alicante: Sociedad Cooperativa de Cre´dito de Callosa de Ensarria´, 262 pp. Said, O., Saad, B., Fulder, S., Amin, R., Kassis, E., Khalil, K., 2009. Hypolipidemic activity of extracts from Eriobotrya japonica and Olea europaea, traditionally used in the grecoarab medicine in maintaining healthy fat levels in the blood. Open Complement. Med. J. 1, 8491. Sanches, J., Cia, P., Valentini, S.R.T., Benato, E., Chagas, E.A., Pio, R., 2011. Atmosfera modificada e refrigerac¸a˜o para conservac¸a˜o po´s-colheita da neˆspera ‘Fukuhara’. Bragantia 70 (2), 455459. Scaloppi Ju´nior, E.J., Jesus, N., Martins, A.B.G., 2004. Capacidade de enraizamento de variedades de nespereira submetidas a` poda de renovac¸a˜o. Rev. Bras. Frutic. 26 (3), 6164. Silva, J.A.A., Pereira, F.M., 2004. Enraizamento de estacas herba´ceas de nespereira (Eriobotrya japonica Lindl). Rev. Bras. Frutic. 26 (2), 369371. Sun, G., Liu, Y., Zhu, J., Iguchi, M., Yoshioka, S., Miyamura, M., et al., 2010. Immunomodulatory effect of Eriobotrya japonica seed extract on allergic dermatitis rats. J. Nutr. Sci. Vitaminol. 56, 145149.
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Tanaka, K., Tamaru, S., Nishizono, S., Miyata, Y., Tamaya, K., Matsui, T., et al., 2010. Hypotriacylglycerolemic and antiobesity properties of a new fermented tea product obtained by tea-rolling processing of third-crop green tea (Camellia sinensis) leaves and loquat (Eriobotrya japonica) leaves. Biosci. Biotechnol. Biochem. 74, 6061612. Temiz, H., Tarakc¸i, Z., Karadeniz, T., Bak, T., 2012. The effect of loquat fruit (Eriobotrya japonica) marmalade addition and storage time on physicochemical and sensory properties of yogurt. J. Agric. Sci. 18, 329338. Tian, S., Li, B., Ding, Z., 2007. Physiological properties and storage technologies of loquat fruit. Fresh Prod. 1 (1), 7681. Undurraga, P.L., Olaeta, J.A., Cancino, C., 2011. Ethylene, enzymatic and respiratory pattern evolution in loquat (Eriobotrya japonica (thunb.) lindl.) cv. golden nugget in the last four sequential stages of maturation. Chil. J. Agric. Res. 71 (4), 525532. Vicente, P., 2013. A folha: Nespereira. Escola profissional de desenvolvimento rural de Abrantes. 8 pp. Available at: ,http://media.epdra.pt/multimedia/documentos/179/JORNAL_EPDRA_16.pdf. (accessed 09.05.17.). Wei, Y., Xu, F., Shao, X., 2017. Changes in soluble sugar metabolism in loquat fruit during different cold storage. J. Food Sci. Technol. 54 (5), 10431051. Xu, H., Chen, J., 2011. Commercial quality, major bioactive compound content and antioxidant capacity of 12 cultivars of loquat (Eriobotrya japonica Lindl.) fruits. J. Sci. Food Agric. 91, 10571063. Yang, S., Sun, C., Wang, P., Shan, L., Cai, C., Zhang, B., et al., 2008. Expression of expansin genes during postharvest lignification and softening of ‘Luoyangqing’ and ‘Baisha’ loquat fruit under different storage conditions. Postharvest Biol. Technol. 49 (2), 4353. Yoshioka, S., Hamada, A., Jobu, K., Yokota, J., Onogawa, M., Kyotani, S., et al., 2010. Effects of Eriobotrya japonica seed extract on oxidative stress in rats with non-alcoholic steatohepatitis. J. Pharm. Pharmacol. 62, 241246. Zar, P.P.K., Morishita, A., Hashimoto, F., Sakao, K., Fujii, M., Wada, K., et al., 2014. Antiinflammatory effects and molecular mechanisms of loquat (Eriobotrya japonica) tea. J. Funct. Foods 6, 523533. Zheng, Y.H., Cao, S.F., Ma, S.J., Yang, Z.F., Li, N., 2010. Effects of 1methylcyclopropene on internal browning and quality in cold stored loquat fruit. Acta Hortic. 857, 489492. Zhou, C.H., Sun, C.D., Chen, K.S., Li, X., 2011. Flavonoids, phenolics, and antioxidant capacity in the flower of Eriobotrya japonica Lindl. Int. J. Mol. Sci. 12, 29352945.
FURTHER READING Akhtar, A., Abbasi, N.A., Hussain, A., 2010. Effects of calcium chloride treatments on quality characteristics of loquat fruit during storage. Pak. J. Bot. 42, 181188. Alosa, E., MartinezFuentesb, A., Reigb, C., Mesejob, M.J., Rodrigoa, M., Zacarias, L., 2017. Ethylene biosynthesis and perception during ripening of loquat fruit (Eriobotrya japonica Lindl.). J. Plant Physiol. 210, 6471. Cai, C., Xian, L., Chen, K., 2006b. Acetylsalicylic acid alleviates chilling injury of postharvest loquat (Eriobotrya japonica Lindl.) fruit. Eur. Food Res. Technol. 223 (1), 533539. Cao, S., Zheng, Y., Wang, K., Rui, H., Tang, S., 2009. Effect of 1methylcyclopropene treatment on chilling injury, fatty acid and cell wall polysaccharide composition in loquat fruit. J. Agric. Food Chem. 57, 84398443. Ding, C.K., Chachin, K., Ueda, Y., Imahori, Y., Wang, C.Y., 2002. Modified atmosphere packaging maintains postharvest quality of loquat fruit. Postharvest Biol. Technol. 24, 341348. Gao, H., Tao, F., Song, L., Chen, H., Chen, W., Zhou, Y., 2009. Effects of short term N2 treatment on quality and antioxidant ability of loquat fruit during cold storage. J. Sci. Food Agric. 89, 11591163. Ghasemnezhad, M., Nezhad, M.A., Gerailoo, S., 2011. Changes in postharvest quality of loquat (Eriobotrya japonica) fruits influenced by chitosan. Hortic. Environ. Biotechnol. 52 (1), 4045. Jin, P., Zhang, Y., Huang, Y., Shan, T., Wang, L., Zheng, Y., 2016. Effect of hot water combined with glycine betaine alleviates chilling injury in cold-stored loquat fruit. Postharvest Biol. Technol. 118, 141147. Marquez, C.J., Cartegana, R.R., PerezGago, M.B., 2009. Effect of edible coatings on Japanese loquat (Eriobotrya japonica L.) postharvest quality. Vitae. 16, 304310. Rui, H., Cao, S., Shang, H., Jin, P., Wanga, K., Zhenga, Y., 2010. Effects of heat treatment on internal browning and membrane fatty acid in loquat fruit in response to chilling stress. J. Sci. Food Agric. 90, 15571561. Wang, Y., Shan, Y., Chen, J., Feng, J., Huang, J., Jiang, F., et al., 2016. Comparison of practical methods for postharvest preservation of loquat fruit. Postharvest Biol. Technol. 120, 121126. Zappi, D., Turner, J., 2001. Eriobotrya japoˆnica Rosaceae. Curtis’s Bot. Mag. 18 (2), 108113. Zhang, W., Zhao, X., Sun, C., Li, X., Chen, K., 2015. Phenolic composition from different loquat (Eriobotrya japonica Lindl.) cultivars grown in China and their antioxidant properties. Molecules. 20, 542555. Zheng, Y.H., Su, X.G., Yi, Y.B., Li, S.Y., Xi, Y.F., 2000a. Effects of SO2 on loquat fruits stored at 1 C. J. Nanjing Agric. Univ. 23, 8992. Zheng, Y.H., Su, X.G., Li, S.Y., Xi, Y.F., 2000b. Quality, active oxygen and polyamines metabolic changes in cold-stored loquat fruits as affected by postharvest SO2 treatment. Acta Phytophysiol. Sin. 26, 397401.
Maboque/Monkey Orange—Strychnos spinosa Sueli Rodrigues1, Edy Sousa de Brito2 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Botanical Origin Postharvest and Physiology Sensory and Physicochemical Characterization
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Industrialization and Uses References
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BOTANICAL ORIGIN The monkey orange is a small tree from Southern Africa and the three main species are Strychnos cocculoides Backer; Strychnos spinosa Lam.; and Strychnos pungens Solereder Loganiaceae (Wehmeyer, 1966; Fox and Norwood-Young, 1982; Taylor, 1986). The name comes from the fact that monkeys consume the fruit. The leaves are also consumed by herbivorous animals such as elephants. The tree is small, 17 m in height, and bears edible, round shaped fruits, 612 cm in diameter, which resembles an orange (see Figs. 1 and 2). Unripe fruits have a bright green wood peel (34 mm thick), which turns yellowbrown upon ripening. The fruit has an edible, juicy, sweetsour pulp, which is pale brown in color and contains many hard brown (13 cm) seeds. The seeds may be poisonous. The fruit is almost unknown in the western world, but in Africa, the fruits are usually eaten fresh. Common names for the species are Spiny Monkey orange/Green Monkey Orange (in English), Doringklapper (in African), Morapa (North-Sotho), Muramba (Venda), um Kwakwa (Swaziland), Nsala (Tswana), Mutamba (Shona),and Maboque (Portuguese). Due to good adaptation to arid areas S. spinosa is regarded as a promising crop. S. spinosa was introduced in the Besor area (Israel) with promising results. However, a high variability for growth, yields, fruit size, ripening season, and taste were reported. Some fruits are astringent, bitter, and very sour. However, some trees provide great tasty fruits. In sensory taste tests, people were asked to compare the monkey orange fruit with familiar fruits. The most common taste answers were: orange, banana, and apricot, and all possible combinations among them. The fruits aroma resembles the spice clove. A GC/MS analysis performed in Israel reported the presence of eugenol, the essential oil found in cloves, as one of the main volatile compounds. The fruit is large (4001200 g), round, has a thick shell 47 mm, and contains 30%45% juicy flesh with over 20% total soluble solids, and high acidity over 200 μeq H1 (Mizrahi et al., 2002).
POSTHARVEST AND PHYSIOLOGY Although the tree can produce thousands of small flowers, most of them do not develop into fruits, and most of them fall off after 2 weeks of flourish. Also, lots of fruits fall before reaching the ripe stage with only about 10% of the fruits reach the ripe stage. In Africa, the fruit needs 1214 months to ripen. The average fruit weight is 330 g, but the larger ones can reach 500 g. The fruit yield ranges from 11 to 24 kg/tree. The pulp content is about 40%, and more than 50 seeds are can be found in a single fruit. The color of the fruit peel changes from green to yellow, when ripening under storage. The fruit is climacteric with ethylene and carbon dioxide emission. An increase in the total soluble solids is observed during storage. The pH and Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00038-1 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Monkey orange tree.
FIGURE 2 Monkey orange fruit.
the total titratable acidity did not present significant changes. Citric and malic acid were the main organic acids in the fruit. Sucrose, fructose, and glucose were the major accumulated sugars during ripening, The volatile compounds are found in the peel of ripe fruits, and the main compounds are phenylpropanoids and trans-isoeugenol. The fruit is acidic with pH values around 3.0 (Sitrit et al., 2003).
SENSORY AND PHYSICOCHEMICAL CHARACTERIZATION The monkey orange fruit emits a characteristic aroma described as a complex with notes of pineapple, apricot, clove, melon, and citrus. Monkey orange is a source of protein, energy, fibers, and minerals. The physicochemical composition of Monkey orange is given in Table 1. The aroma of the monkey orange is found in the fruit peel, with the phenylpropanoids and the trans-isoeugenol corresponding to more than 75%. Trans-isoeugenol is found in cinnamon and clove essential oils as a minor component. Table 2 presents the aroma compounds found in monkey orange peel.
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295
TABLE 1 Monkey Orange Composition Compound
Content
Crude protein
5.4%
Fat
31.2%
Fiber
17.6%
Total carbohydrate
42.1%
Energy value
1923 kJ/100 g
Ash
4.1%
Dry matter
22.1%
Phosphorus
1081 μg/g
Calcium
149 μg/g
Magnesium
430 μg/g
Iron
136 μg/g
Potassium
19.68 mg/g
Sodium
253 μg/g
Source: Saka and Msonthi (1994).
TABLE 2 Volatile Compounds of Monkey Orange Peel (Ripe Yellow Stage) Compound
Content (μg/g)
trans-β-ocimene
161.5 6 117.5
Chavicol
172.0 6 75.0
p-trans-anol
647.5 6 68.0
Eugenol
307.0 6 30.0
Dihydroeugenol
123.5 6 31.0
Vanillin
47.5 6 16.5
trans-isoeugenol
4762.5 6 1643.5
2,6-Dimethoxyphenol
24.0 6 12
Source: Sitrit, Y., Loison, S., Ninio, R., Dishon, E., Bar, E., Lewinsohn, E., et al., 2003. Characterization of monkey orange (Strychnos spinosa Lam.), a potential new crop for arid regions. J. Agric. Food Chem. 51 (21), 62566260 (Sitrit et al., 2003).
INDUSTRIALIZATION AND USES Despite the potential of monkey orange as an industrial crop, the fruit and leaves use is still restricted to domestic consumption as juices and fresh fruit. The fruit is also used in popular medicine in Africa. Some pharmacological compounds have been reported. S. spinosa fruit is used against snake bite venom (Mors et al., 2000). Other medicinal uses are also reported against many diseases such as stomach disorders and venereal disease (Msonthi et al., 1985). No reports on the industrialization of the fruit were found as the plant studies are still scarce. Juices and dried fruit rolls are the potential uses for this fruit (Mizrahi et al., 2002).
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REFERENCES Fox, F.W., Norwood-Young, M.E., 1982. Food From the Wild-Edible Plants of Southern Africa. Delta, Johannesburg. Mizrahi, Y., Nerd, A., Sitrit, Y., 2002. New fruits for arid climates. In: J. Janick and A. Whipkey (eds.), Trends in new crops and new uses. ASHS Press, Alexandria, VA. pp. 378384. Mors, W.B., Nascimento, M.C., Pereira, B.M., Pereira, N.A., 2000. Plant natural products active against snake bite—the molecular approach. Phytochemistry 55 (6), 627642. Msonthi, J.D., Galeffi, C., Nicoletti, M., Messana, I., Marini_bettolo, G.B., 1985. Kingiside aglucone, a natural secoiridoid from unripe fruits of Strychnos spinosa. Phytochemistry 24 (4), 771772. Saka, J.D.K., Msonthi, J.D., 1994. Nutritional value of edible fruits of indigenous wild trees in Malawi. Forest Ecol. Manag. 64 (23), 245248. Sitrit, Y., Loison, S., Ninio, R., Dishon, E., Bar, E., Lewinsohn, E., et al., 2003. Characterization of monkey orange (Strychnos spinosa Lam.), a potential new crop for arid regions. J. Agric. Food Chem. 51 (21), 62566260. Taylor, F.W., 1986. The potential for utilization of indigenous plants in Botswana. In: Wickens, G.E., Goodin, J.R., Field, D.V. (Eds.), Plants for Arid Lands. George Allen and Unwin, London, pp. 231242. Wehmeyer, A.S., 1966. The nutrient composition of some edible wild fruit found in the Transvaal. S. Afr. Med. J. 40, 11021104.
Macauba Palm—Acrocomia aculeata Jose´ M.C. Costa1, Dalany M. Oliveira2 and Luis E.C. Costa1 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Federal Institute of Education, Science and Technology of Paraiba, Sousa, Paraiba, Brazil
Chapter Outline Introduction Botanic and Production Aspects of Macau´ba Palm Drying Processes Drying Adjuvants Fruit Drying Macau´ba Palm Fruit Components
297 298 298 299 300 300
Whole Fruit Pulp With and Without Maltodextrin Addition Dried Macau´ba Pulp Powder The Influence of Drying Processes on the Chemical Composition of Macau´ba Palm Fruit Bioactive Compounds References Further Reading
300 301 301 302 304
INTRODUCTION Palm trees mainly occur in tropical and subtropical regions, with most genus and species found in Asia, Indonesia, and the Americas. In the Americas, 67 genus and approximately 1440 species can be found; among these, 39 genus and 200 species occur in Brazil (Alves and Carvalho, 2010). These trees are very important economically, due to the huge diversity of compounds that they produce in their fruits and seeds. These compounds are seen as an important source of funds and are widely used in the local and international industries (Lorenzi, 2006). All the oilseed palm trees are also used as food due to the presence of starch, proteins, vitamins, and oils. Their fruits are traditionally consumed fresh, boiled or as juices and the high amount of starch is on occasion used in fermentation processes (Clement et al., 2005). Many Latin-American palm trees are being studied with the intent of developing new products. Palm trees are emblematic of the tropics, are abundant, productive, and vital for indigenous peoples’ subsistence (Clement et al., 2005). According to Rezende (2009), Brazil possesses a great diversity of oilseeds. Among these, the macau´ba (Acrocomia aculeata), which can be found in the northeast, southeast and south regions, stands out as the second-most productive palm tree found in arid and semiarid regions, with a production of 15005000 kg/ha, second only to the dendeˆ (Elaeis guineensis) (Scariot et al., 1995). Macau´ba, also known as macacauba, macaı´ba, macaibeira, and macajuba, among others, has many uses; its inflorescences are used in flower arrangements, the leaves provide textile fibers, the thorns can be used as pins, the heart of the palm is used in culinary ways and the trunk produces a sap that resembles honey after fermentation (Almeida et al., 1998; Machado et al., 2010). Macau´ba fresh pulp has a sweet flavor and mucilaginous texture, can be consumed in natural or dehydrated form, raw or after cooking, and can be used in several products such as drinks, cakes, icecreams, and jams. Additionally, oil can be extracted from its fruit pulp and seeds (Brasil, 2002). Oliveira et al. (2013) and Ramos et al. (2008) demonstrated the potential of macau´ba pulp as a nutritive food, able to contribute to the nutritional enrichment of supplementary feeding programs, being a natural source of vitamins and minerals.
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00039-3 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Macau´ba palm tree (Acrocomia sclerocarpa Mart.) located in Chapada do Araripe, Arajara district in the city of Barbalha, Ceara´, Brazil.
´ BA PALM BOTANIC AND PRODUCTION ASPECTS OF MACAU Macau´ba cultivation occurs in regions with an altitude of between 150 and 1000 m, annual rainfall inferior to 1500 mm and temperatures between 15 C and 35 C. The tree is planted once and can stays productive over 90 years, producing around 2401200 fruits (Silva et al., 1992). Its stipe reaches 1015 m high and 2030 cm in diameter and is frequently covered by the petioles bases which remains adhered for many years (Fig. 1). The node region is covered in dark, sharp spines, approximately 10 cm long (Miranda et al., 2001). The fructification process occurs throughout the year and the fruits ripen between September and January (Lorenzi, 2006). In this phase, they exude a characteristic aroma and the peel, usually very adherent to the pulp, loosens easily (Brasil, 2002). The fruits are spherical and are 2.55 cm in diameter (Fig. 2A and B). The epicarp breaks easily when ripened. The mesocarp (Fig. 2C) is edible, fibrous, mucilaginous, rich in glycerides, has a sweet flavor and a sticky aspect, hindering its separation, which results in low yields (Henderson et al., 1995; Brasil, 2002).
DRYING PROCESSES Water removal is one of the oldest known processes for food preserving. Through this process the water activity of the product is reduced, preventing the growth of microorganisms, particularly fungi and bacteria; slowing physicochemical and enzymatic deterioration during storage. Nowadays, food drying is widely used as a method of preservation of nutritional quality and commercial value and fuels the emergence of new products on the market, which motivates investments in agricultural production and processing (Soares et al., 2001). One of the advantages of the drying process is the reduction of the product weight and volume, which reduces transport, storage, and packaging costs (Eik, 2008; Shigematsu et al., 2005).
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FIGURE 2 Macau´ba fruit (A), peeled fruit (B), mesocarp (C), endocarp (D), seed (E).
According to Park (2006), each dryer type caters to different product needs. Therefore, one of the first requirements for choosing a dryer is to know the properties of the product that is going to be dehydrated. Many different types of drying equipment are used to a great extent in the food industry, e.g., freeze dryers, spray dryers and rotary drum dryers (Chua and Chou, 2003). The basic mechanisms employed from the heat transfer source indicate the necessary equipment to the process, likewise, the possible fluid mechanics equipment can also be chosen through observation of the vapor withdrawal on the product surface by fluid movement analysis (Park, 2006). For fruit and other products dehydration, the most commonly used driers are, in order of importance: spray dryer, fluidized bed dryer, tunnel dryer and lyophilizer. In all of these dryers, the dehydration process starts in a chamber that receives the products.
Drying Adjuvants Hygroscopicity and agglomeration of powdered foods are the biggest obstacles faced in drying raw materials rich in sugars, such as pulps and fruit juices. These two phenomena can cause many problems in powdered foods and low yields during the drying process (Fabra et al., 2011). To avoid these problems, the use of adjuvants in appropriate levels is essential to maintain product acceptability, ensure that the product does not exceed the limits established by legislation, and also help in the obtainment of freeflowing powders (Jaya and Das, 2004). Drying adjuvants are also known as carriers or wall materials and are used mainly for drying fruit pulp, reducing problems of agglomeration during the process, thereby improving the stability of the obtained powders (Oliveira et al., 2007; Silva et al., 2006). Different materials, such as antiagglutinant agents, isolated proteins and maltodextrins with different dextrose equivalents (DEs) are used for these purposes (Mosquera et al., 2010). Maltodextrin is one of the main additives used to aid fruit pulp drying in spray drying and freeze drying, due to its low cost and hygroscopicity, avoiding particle agglomeration (Ferrari et al., 2012; Ceballos et al., 2012). This material also has antioxidant activity and provides good retention of volatile substances (65%80%). Maltodextrin also has well defined physical properties and is soluble in water; these characteristics have popularized its use as an additive in the food industry (Mosquera et al., 2010). Maltodextrins with low (less than 20) DE are more efficient, possess better encapsulant properties and low moisture diffusivity (Anselmo et al., 2006). High DE maltodextrins have long molecular structures, with a large number of ramifications and hydrophilic groups, which easily bind to water molecules in the storage room (Oliveira et al., 2014).
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DE 20 maltodextrins have been quite effectively used in spray drying. Many different fruit pulps were dried through this process, such as blackberry pulp (Ferrari et al., 2012), mango pulp, caja´ pulp (Neto et al., 2015), and soursop pulp (Costa et al., 2014). They are also used in fruit pulp lyophilization, such as caja pulp (Oliveira et al., 2014) and macau´ba pulp (Oliveira et al., 2013). The addition of appropriate concentrations of maltodextrin to the fruit pulp before the drying process increases the efficiency and lowers the energy costs, generating a fruit pulp powder with better flowability and hygroscopic characteristics. Maltodextrin is also used in many other food products such as candies, icecreams, soups, and dehydrated beverages (Cereda and Franco, 2001).
Fruit Drying Drying is one of the preservation processes available for application to the fruit pulp industry, thereby concentrating the components of the raw material and enabling the product to be stored at ambient conditions for long periods (Gomes et al., 2004). The drying process consists of the elimination of water from the material by evaporation. There are several advantages in using the drying process in fruit preservation, such as obtaining a better conservation of the product, increased stability of the aromatic components, reducing product weight and increasing product availability during any time of year (Park et al., 2001). The drying process is substantiated by knowledge of balance of the initial and final moisture content of the product, the water molecules relation with the solid structure, and the water transportation ratio from the product interior to the surface (Brod et al., 1997). Various physical and chemical material changes can be observed in fruit drying, mainly the increased concentration of components and increased sugar content in the product (Lewicki and Pawlak, 2003). Most changes in dehydrated food quality occur during processing and storage, involving changes in physical structures, rehydration degree, appearance, and loss of aroma and flavor (Fellows, 2006). Fruit drying or dehydration should preferably preserve its flavor, aroma, original colors, avoid the use of chemical additives, and provide a texture similar to the fresh product (Queiroz et al., 2007). An additional advantage of fruit drying is to increase the availability of the product outside the harvest period (Park et al., 2002).
´ BA PALM FRUIT COMPONENTS MACAU Whole Fruit Pulp With and Without Maltodextrin Addition Table 1 presents the physicochemical characteristics, bioactive components, and color of whole macau´ba pulp (WP) and macau´ba pulp with 8% maltodextrin (MP). In general, the addition of 8% maltodextrin did not greatly change the physicochemical characteristics and bioactive components when compared to WP, except for the water activity (aw), vitamin C, and the color parameters L*, a* and b*. The pulps have low humidity and acidity, and a high content of soluble solids and aw, characterizing the fruit as sweet and susceptible to microbial growth. Different moisture and acidity levels were found in the literature; Ramos et al. (2008) observed higher moisture content and Hiane et al. (2005) lower acidity values. These variations can be caused by different weather conditions, time of harvest, pulping type and maturity stage. The loss of vitamin C in MP was 37.21% and is related to the addition of maltodextrin, which may have encapsulated the ascorbic acid molecule, hindering its extraction. The total phenolics level is higher than the values found by Kuskoski et al. (2005) for cupuassu pulp (20.50 mg GAE/100 g), and inferior to fruits such as grapes (117 mg GAE/ 100 g) and ac¸aı´ (136 mg GAE/100 g) that possess great phenological potential. Although MP showed a reduction of 32.14% of flavonoids compared to WP, there was no statistical difference. The flavonoids level comprised a range of values similar to the ones found in cabbage (266399 μg/g) (Huber and Rodriguez-Amaya, 2008), orange pear pulp (348 μg/g), and gala apple-1 (277 μg/g) (Arabbi et al., 2004). Macau´ba pulp also showed high β-carotene and vitamin A levels. It is important to note that these values were higher than those found by Charoensiri et al. (2009) for fruits such as orange, watermelon, and papaya. The macau´ba pulp studied by Ramos et al. (2008) showed β-carotene concentrations of 49 μg/g. The color range comprising yellow to red indicates fruits with high levels of carotenoids (Uenojo et al., 2007). The fact that the pulps exhibited an orange color explains the high content found in this study, as WP showed a more intense coloration than MP.
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TABLE 1 Characterization of Whole Macau´ba Pulp (WP) and the Macau´ba Pulp With 8% Maltodextrin (MP) Parameters
WP 6 δ
MP 6 δ
Moisture (g/100 g)
40.19 6 0.72a**
41.30 6 0.31a
Water activity (aw)
0.92 6 0.01b*
0.94 6 0.002a
Titratable acidity (g/100 g)
1.43 6 0.07a
1.64 6 0.27a
pH
5.50 6 0.02a*
5.68 6 0.14a
Soluble solids ( Brix)
29.70 6 0.58a
27.63 6 2.81a
Total phenolics (mg GAE/100 g)
51.34 6 10.72a
Yellow flavonoids (μg/g)
372.12 6 76.07
247.84 6 46.38a
Vitamin C (mg/100 g)
118.19 6 6.01a
72.83 6 8.70b
β-Carotene (μg/g)
35.99 6 1.09a
34.76 6 2.03a
Vitamin A (RE/100 g)
599.78 6 18.16a
579.29 6 33.86a
L*
42.43 6 0.43a
41.00 6 0.69b
a*
5.08 6 0.31a
1.46 6 0.17b
b*
17.31 6 1.80
49.88 6 2.03a a
Color
a
19.42 6 0.36a
Abbreviations: WP, whole pulp; MP, pulp with the addition of 8% (w/w) of maltodextrin; 6δ, standard deviation; aw, water activity; GAE, gallic acid equivalent; color parameters: L* (lightness-darkness), a*(redness-greenness) and b* (yellowness-blueness). **Equal low case letters in the same line do not differ significantly by Tukey test at 5% probability.
Dried Macau´ba Pulp Powder Table 2 shows the physicochemical characteristics, bioactive compounds, and the color of macau´ba powder obtained through different drying processes, T1: macau´ba powder, dried in an oven with air circulation without maltodextrin; T2: macau´ba powder, dried in an oven with air circulation, with the addition of 8% (w/w) maltodextrin; T3: macau´ba powder, freeze dried without maltodextrin; T4: macau´ba powder, freeze dried with addition of 8% (m/m) maltodextrin. The most efficient process for reducing moisture and aw was T3, however, all drying processes carried resulted in low levels of moisture and aw, inhibiting microbial growth, as food with aw below 0.60 are microbiologically stable products (Ordo´n˜ez, 2005). All processes were equal in relation to acidity and pH values. Also, T4 and T2 showed the highest amount of soluble solids, due to the addition of maltodextrin. Regarding bioactive compounds, T3 and T4 had the highest levels of phenolics, vitamin C, β-carotene and vitamin A, demonstrating that the lyophilization process maintained a high amount of bioactive components, however, these treatments showed lower flavonoids concentrations. This may have been caused by the higher number of steps in the lyophilization process compared to oven drying. Huber and Rodriguez-Amaya (2008) stated that processed products have significantly lower flavonoids contents than those found in fresh fruits. The macau´ba powder that presented the darker L* parameter was T2, and regarding the a* and b* chromaticity, T3 presented the most intense yellow color followed by T4, demonstrating a more attractive color, however, T1 and T2 showed a less intense chromaticity.
THE INFLUENCE OF DRYING PROCESSES ON THE CHEMICAL COMPOSITION OF ´ BA PALM FRUIT BIOACTIVE COMPOUNDS MACAU During processing, beginning at the removal of the fruit peel and pulping, many nutrient losses occur. Ordo´n˜ez (2005) states that the processes in which foods are subjected aims to provide a safe and suitable product life, while minimizing nutrient losses. The technological treatment applied and the types of nutrients are directly related to these losses during processing. In this study, it was observed that the two drying methods showed different percentages of nutrient loss.
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TABLE 2 Characterization Macau´ba Pulp Powder Obtained Through Different Drying Processes With the Addition of Maltodextrin Parameters
T1 (T0E) 6 δ
T2 (T1E) 6 δ
T3 (T0L) 6 δ
T4 (T1L) 6 δ
Moisture (g/100 g)
T1 (T0E) 6 δ
T2 (T1E) 6 δ
T3 (T0L) 6 δ
T4 (T1L) 6 δ
aw
3.28 6 0.08ab**
3.41 6 0.11
b
3.12 6 0.09
3.49 6 0.12a
Titratable acidity (g/100 g)
0.21 6 0.01a
0.22 6 0.01a
0.12 6 0.01b
0.22 6 0.01a
pH
2.10 6 0.01
2.47 6 0.55
a
2.06 6 0.05
2.50 6 0.32a
Soluble solids ( Brix)
5.57 6 0.02a
5.62 6 0.10a
5.71 6 0.01a
5.60 6 0.02a
Total phenolics (mg GAE/100 g)
40.30 6 0.89c
45.70 6 2.63ab
45.15 6 1.28bc
50.32 6 2.32a
Yellow flavonoids (μg/g)
82.76 6 7.98ab
65.15 6 6.72b
89.39 6 5.77a
86.95 6 8.49a
Vitamin C (mg/100 g)
135.74 6 12.69a
121.11 6 4.47ab
115.62 6 3.46b
93.68 6 3.51c
β-Carotene (μg/g)
52.06 6 5.64b
51.72 6 3.09b
103.36 6 5.59a
100.78 6 5.63a
Vitamin A (RE/100 g)
51.56 6 0.66bc
36.08 6 0.50c
80.09 6 7.32a
57.68 6 3.99b
L*
859.42 6 10.94bc
601.38 6 8.32c
1334.83 6 122.04a
961.39 6 66.41b
a*
49.76 6 0.09a
48.82 6 0.23b
49.76 6 0.26a
49.87 6 0.14a
b*
21.38 6 0.04c
21.03 6 0.14ab
21.24 6 0.10bc
20.94 6 0.09a
24.63 6 0.16c
22.62 6 0.14d
27.28 6 0.28a
26.35 6 0.35b
a
a
a
Color
Abbreviations: T1: macau´ba powder, dried in an oven with air circulation without maltodextrin; T2: macau´ba powder dried in an oven with air circulation, with the addition of 8% (w/w) maltodextrin; T3: macau´ba powder, freeze-dried without maltodextrin; T4: macau´ba powder, freeze-dried with the addition of 8% (m/m) maltodextrin; 6 δ: standard deviation; aw: Water activity; GAE: gallic acid equivalent; color parameters: L* (lightness-darkness), a* (rednessgreenness) and b* (yellowness-blueness). **Equal low case letters in the same line do not differ by Tukey test at 5% probability.
The phenolic content of macau´ba powder obtained in T1 was higher than in T2, probably due to the addition of 8% maltodextrin T2, which impairs the extraction of this constituent. Meanwhile, the processes T3 and T4 did not show any phenolic content losses. The flavonoid content was the most affected by the treatments; their losses were in the range from 77.40% to 80.82% both in oven and freeze-drying, with and without the addition of 8% maltodextrin respectively. In studies, Ewald et al. (1999) showed that the majority of flavonoids losses occurred during preprocessing, peeling, cutting, and bleaching. The vitamin C content decreased significantly during all processes. This phenomenon was expected, as the stability of vitamin C is affected by several factors such as temperature, presence of oxygen, pH, light, and catalysts (Ordo´n˜ez, 2005). The biggest losses occurred in T1 and T2 with a reduction from 72.76% to 72.90%, respectively; T3 and T4 showed lower reductions at 46.01% and 47.15%, respectively. Lyophilized products generally show the lowest reductions, as the stability of vitamin C increases as the processing temperature decreases (Ordo´n˜ez, 2005). In T1 and T2 there was a greater loss of β-carotene content (51.56; 36.08 μg/g, respectively) and vitamin A (859.42; 601.38 RE/100 g, respectively) compared to the yields of β-carotene (80.09; 57.68 μg/g) and vitamin A (1334.83, 961.39 RE/100 g) of T3 and T4 respectively. The results confirm the findings in literature that fruit processing changes the contents of its constituents. These changes can happen during the pulp processing (peeling, pulping, etc.) or in the application of heat treatments.
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Nutr. 19, 97108. Jaya, S., Das, H., 2004. Effect of maltodextrin, glycerol monostearate and tricalcium phosphate on vacuum dried mango powder properties. J. Food Eng. 3, 125134. Kuskoski, E.M., Asuero, G.A., Troncoso, A.M., Mancinifilho, J., Fett, R., 2005. Aplicacio´n de diversos me´todos quı´micos para determinar actividad antioxidante en pulpa de frutos. Rev. Cieˆnc. Tecnol. Aliment. 25, 726732. Lewicki, P.P., Pawlak, G., 2003. Effect of drying on microstructure of plant tissue. Drying Technol. 21, 57683. Lorenzi, G.M.A.C., 2006. Acrocomia aculeata (Lodd.) ex Mart. Arecaceae: bases para o extrativismo sustenta´vel. Universidade Federal do Parana´, Curitiba. Machado, C.A.C., Sanjinez-Argandona, E.J., Homem, G.R., Tommaselli, M.A.G., 2010. Viability model of production of the consortium: macau´ba (Acrocomia aculeata) and sugar cane (Saccharum officinarum). XXX National Meeting of Production Engineering. 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Characterization of grugru palm pulp for food applications. J. Food Sci. Eng. 2, 107112. Oliveira, V.S., Afonso, M.R.A., Costa, J.M.C., 2014. Caracterizac¸a˜o fı´sico-quı´mica e comportamento higrosco´pico de sapoti liofilizado. Rev. Cieˆnc. Agron. 42, 342348. Ordo´n˜ez, J.A., 2005. Tecnologia de alimentos: Componentes dos alimentos e processos. Artmed editora, Sa˜o Paulo. Park, J.K., 2006. Selec¸a˜o de processos e equipamentos de secagem. Palestra - Universidade Estadual de Campinas, Campinas. Park, K.J., Yado, M.K.M., Brod, F.P.R., 2001. Estudo de secagem de peˆra bartlett (Pyrus sp.) em fatias. Cieˆnc. Tecnol. Aliment. 21, 288292. Park, K.J., Bin, A., Brod, F.P.R. 2002. Drying of pear ‘d’Anjou’ with an without osmotic dehydration. J. Food Eng. 56, 97103. Queiroz, V.A.V., Berbert, P.A., Molina, A.B.M., Gravina, G.A., Queiroz, L.R., Deliza, R., 2007. Desidratac¸a˜o por imersa˜o-impregnac¸a˜o e secagem por convecc¸a˜o de goiaba. Pesqui. Agropecu. Bras. 42, 14791486.
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Ramos, M.I.L., Ramos, M.M.F., Hiane, P.A., Braga, J.A.N., Siqueira, E.M.A., 2008. Qualidade nutricional da polpa de bocaiu´va Acrocomia aculeata (Jacq.) Lodd. Cieˆnc. Tecnol. Aliment. 28, 9094. Rezende, J.R., 2009. Desacidificac¸a˜o de o´leo de macau´ba por extrac¸a˜o lı´quido-lı´quido, para produc¸a˜o de biodiesel. 61f. Dissertac¸a˜o. (Mestrado em Engenharia de Alimentos). Universidade Estadual do Sudoeste da Bahia. Scariot, A.O., Lleras, E., Hay, J.D., 1995. Flowering and fruiting phenologies of the palm Acrocomia aculeata: patterns and consequences. Biotropica. 27, 168173. Shigematsu, E., Eik, N.M., Kimura, M., Mauro, M.A., 2005. Influeˆncia de pre´ tratamentos sobre a desidratac¸ao osmotica de carambola. Cieˆnc. Tecnol. Aliment. Campinas, 25 (3), 536545. Silva, J.A., Silva, D.B., Junqueira, N.T.V., Andrade, L.R.M., 1992. Coleta de sementes, produc¸a˜o de mudas e plantio de espe´cies frutı´feras nativas dos cerrados: informac¸o˜es explorato´rias. EMBRAPA-CPAC. Planaltina, Planaltina. Silva, M.A., Sobral, P.J.A., Kieckbusch, T.G., 2006. State diagrams of freeze-dried camu-camu (Myrciaria dubia (HBK) Mc Vaugh) pulp with and without maltodextrin addition. J. Food Eng. 77, 426432. Soares, E.C., Oliveira, G.S.F., Maia, G.A., Monteiro, J.C.S., Silva, A., Filho, M.S.S., 2001. Desidratac¸a˜o da polpa de acerola (Malpighia emarginata D. C.) pelo processo “foam-mat”. Cieˆnc. Tecnol. Aliment. 21, 164170. Uenojo, M., Junior, M.R.M., Pastore, G.M., 2007. Caroteno´ides: Propriedades, aplicac¸o˜es e biotransformac¸o˜es para formac¸a˜o de compostos de aroma. Quı´m. Nova. 30, 616622.
FURTHER READING Ewald, B.T., Loyolla, C.M., Pereira, A.C.H., Lenz, D., Medeiros, A.R.S., Andrade, T.U., et al., 2015. Atividade gastroprotetora do extrato etano´lico de Pavonia alnifolia A.St.-Hil. Rev. Bras. Plantas Med. 17, 392397. Siqueira, E.M.A., 2008. Qualidade nutricional da polpa de bocaiu´va Acrocomia aculeata (Jacq.) Lodd. Cieˆnc. Tecnol. Aliment. 28, 9094.
Mangaba—Hancornia speciosa Narendra Narain, Fernanda R.M. Franc¸a and Maria T.S.L. Neta Federal University of Sergipe, Sa˜o Cristo´va˜o, Sergipe, Brazil
Chapter Outline Introduction Origin and Production Botanical Aspects Cultivation and Harvest Physiology and Biochemistry Fruit Development
305 305 305 306 307 307
Chemical Composition and Nutrition Vitamin C Phenolic Compounds Volatile Constituents Final Considerations References
308 309 309 311 316 316
INTRODUCTION The term “Mangabeira” is used for the tree in which the fruit mangaba are produced. The fruit possesses a pleasant acidic aroma and is very much appreciated in the northeast region of Brazil where it is largely cultivated (Gomes, 2010). The pulp is the main component that is commercialized in frozen form due to its rich flavor. The mangaba is one of the most abundant and sought after fruit in free markets, and its main form of consumption is as fresh pulp, juice and icecream (Rufino et al., 2009a). It is also used regionally for sweets, cookies, syrup, jams, fruit, wine, vinegar, alcohol, and in the production of jelly (Clerici and Silva, 2011; Lima et al., 2015a). This chapter reviews the scientific information available on its origin, production, botanical aspects, cultivation and harvest, physiology, fruit development, and its chemical composition with an emphasis on vitamin C, bioactive and volatile compounds.
ORIGIN AND PRODUCTION Mangabeira is a tree found naturally in Brazil and its distribution is more abundant in the areas of coastal lowlands of the northeast, principally in the state of Sergipe which is one of the largest domestic producers. In the northeast region of Brazil, the tree is found vegetating in the Cerrado or Tabuleiro (Coastal belt) regions. According to Vieira Neto (1994) and Souza (2004), mangabeira has a better vegetative performance in periods with high temperatures and water shortage. However, it can also be found in subtropical regions (in central Brazil) of Minas Gerais, Mato Grosso, Goias and Sao Paulo that have favorable conditions for the development of sandy texture soils and free waterlogging which is characteristic of some ecosystems in the north, southeast, midwest and northeast regions (Aguiar Filho et al., 1998). The state of Sergipe was the largest producer of the fruit in the country, occurring mainly in the areas of tableland and coastal plains, and in the municipalities of Indiaroba, Barra dos Coqueiros, Pirambu, Itaporanga, and Resorts (Santos et al., 2007).
BOTANICAL ASPECTS Mangaba (Hancornia speciosa Gomes) belongs to the class Dicotyledoneae, order Gentianales, family Apocynaceae, Rauvolfioideae subfamily, Willughbeieae tribe; Hancornia genus contains only this species, which was described by Gomes in 1812. The mangabeira is a medium-sized tree, varying from 2 to 10 m height, reaching up to 15 m, equipped with an irregular crown, twisted trunk, very branched and rough; branches being smooth and reddish. Every plant exudes latex. It presents alternate leaves that are simple, petiolate, glabrous, shiny, and leathery. The inflorescence Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00040-X © 2018 Elsevier Inc. All rights reserved.
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occurs from 1 to 7 fragrant flowers and has white coloration. Sometimes it characterizes with more vegetative growth at times when temperature is high and the ideal annual rainfall is between 750 and 1600 mm. The soils in which the plant develops are poor and sandy, predominant in the Cerrado and tableland region. In the Cerrado region, flowering occurs during the period of August to November, peaking in October. Fruiting can take place at any time of year, but occurs mainly from July to October and January to April. Mangabeira usually has two flowerings/year, first at the beginning of the cold season (April/May), with harvest between July/September and the second in a warmer and dry season (October/December), with harvest between January/March (Lederman et al., 2000).
CULTIVATION AND HARVEST The planting of mangabeira is undertaken preferably at the beginning or end of the cold season. Initially it becomes necessary to produce seedlings, which must be prepared in beds, using a seed, which should be properly washed to remove any residual pulp. Germination initiates after 35 days of cultivation. Upon reaching 10 cm it is considered that the seedlings are ready and adequate for transplantation. But the production of mangaba happens only after 5 years of planting, when it can provide fruit yields of up to 12 tons per hectare, depending on the general management, climate, and soil conditions. Planting should be done in advance in manured ground at least 1 month earlier using cattle manure. In general, organic fertilization is quite prevalent and seedlings should be placed in pits of 0.60 m 3 0.60 m 3 0.60 m. The ground should be weeded before planting. As to diseases and pests, the mangabeira is extremely resilient and no preventive action is necessary. Harvesting should be done when the fruit still is on the plant and when the fruit peel color changes from having a green tint to being yellow. At this stage, the fruit is slightly flaccid. A good indication for the beginning of fruit harvesting is when the first fruits start falling on the ground. Fruits collected from the ground are known as “fallen fruits” and these are those which detach from the tree on its own. The ripening finishes a few hours soon after the fall. These fruits are the most valued in the market, although some of the fruits can be bruised. However, these fruits cannot be stored at room temperature and should be immediately utilized. The fruits containing latex on its peel must be collected with the aid of gloves and later dipped in a solution containing detergent. Later, the fruits should be dried in the shade in fresh air and placed in lined wooden boxes or plastic paper. After harvesting, the mangaba fruit attains its best organoleptic quality in 23 days storage at room temperature. At this moment, softening of the pulp and production of its characteristic flavor occurs. Many studies have been performed on increasing the shelf life of the fruits of mangaba. New fruit conservation technologies have been developed, and the use of plant growth regulators have been promising. Campos et al. (2011) assessed the application of plant regulator, 1-MCP-ethylene, at different concentrations (250, 500, and 1000 ηL/L), and analyzed its postharvest characteristics stored in ambient and refrigerated conditions. Use of 1-MCP at all the three concentrations presented great benefit in postharvest preservation of fruits in atmospheric conditions, increasing the lifespan of mangaba. Moreover, storage at 11 C favors the reduction in weight loss and maintenance of titratable acidity, soluble solids and vitamin C; and when associated with the application of 1-MCP, reduced excessive ripening. In a study undertaken by Carnelossi et al. (2004), naturally fallen mangaba fruit deteriorated after 3 and 7 days of storage at 25 C and 18 C, respectively, showing the importance of the collection the fruit at its physiological maturity point, as well as the use of immediate cooling aimed at prolonging the postharvest life of the fruit. Naser (2014) evaluated the use of chitosan at four different concentrations (0.25%, 0.5%, 1%, and 2%) in postharvest preservation of mangaba fruits and the results showed that the use of chitosan provided smaller losses in mass and length of mangaba fruit stored under refrigeration. Treatments with chitosan in concentrations of 1% and 2% were effective with maximal sensorial notes up to the final storage. Naser (2014) tested different maturity stages (green, halfripe and ripe) of the fruit and the best packaging (plastic bag with closure, PET, and tray with PVC film) stored at controlled temperature for the postharvest conservation of mangaba for 6 days of storage. The fruit packed in tray covered with PVC resulted in the shelf life increase to 15 days, obtaining good visual appearance at the end of storage. The best conservation was in the fruits packed in the tray, maintaining optimal classification throughout the storage period. Due to its high susceptibility, many researchers seek new techniques aimed at better use of mangaba which may facilitate its cultivation and obtaining products that conserve the sensory, nutritional, and functional characteristics of mangaba fruit.
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PHYSIOLOGY AND BIOCHEMISTRY The good development of seedlings is subject to the use of a substrate that is fertile, free from pathogens, and which has a good water retention and aeration capacity. The mangabeira seedling, when the humidity is reduced, may lose its capacity to germinate. Thus the seeds should be planted soon after its removal from the fruit as the seed of the fruits from which pulp has been removed 7 days earlier lose its vigor in germination (Parente and Machado, 1986; Parente et al., 1988). Albuquerque et al. (2002a) studied seedlings of mangabeira in different water levels and they observed a reduction in dry matter in plants by 25% in the pot within 1 month. The treatment had a further tendency to decrease by 37.37%, 47.37%, 31.89%, and 36.39% in relation to total pot capacity for the dry matter of root, stem, leaves, and total plant material, respectively. However it was not verified whether there were any changes in the biomass allocation to the roots, which could be considered a good strategy of plant survival against drought stress. The water content retained in the plant tissue is the balance between the water absorbed from the soil and water lost by evaporation. The closing of the stomata is an attempt to maintain favorable water content in tissues as long as possible and it is one of the first lines of defense against desiccation. However, this reduction in stomatal opening portion restricts the gas transfer between the inner leaf and the atmosphere, causing reduction in the assimilation of CO2 that is used in the photosynthetic process (Silva et al., 2002). Preliminary results show that stomatal closure is a physiological strategy used by young mangabeiras to overcome water shortage and consequently resulting in reduction of the production of biomass. Water deficit tolerance mechanisms have been examined in various plant species, and the results of these analyses have been applied to speed recovery within degraded areas and in seedling production. Plants in arid and semiarid regions are frequently exposed to water deficits, that negatively affect plant growth and productivity (Wu et al., 2008; Zhang et al., 2011). Plants can avoid stress either by maximizing water absorption by deepening their roots, or by minimizing water loss via stomatal closure (Kozlowski and Pallardy, 2002). These morphological and physiological responses can lead to stress adaptation, but can vary considerably among species (Souza et al., 2004). Water stress leads to reduced leaf water reserves, which is associated with a lower transpiration (Baquedano and Castillo, 2006) caused by stomatal closing. This, in turn reduces internal CO2 availability and decreases the plant’s photosynthetic ability (Calbo and Moraes, 1997; Medrano et al., 2002; Parry et al., 2002; Souza et al., 2004; Singh and Singh, 2006; Osipova et al., 2011). Scalon et al. (2015) evaluated the gas exchange and photosynthetic activities of H. speciosa seedlings and examined their tolerance to water deficit and their metabolic recovery after rehydration. The photosynthetic rate, internal carbon concentration, transpiration rate, stomatal conductance, water-use efficiency, photosystem II quantum efficiency, instantaneous carboxylation efficiency, chlorophyll index, and recuperation potential of H. speciosa seedlings were evaluated after rehydration. Twelve month-old seedlings were used and maintained at 70% of their soil water retention capacity. Data were collected on 7, 10, 12, 14, 16, 18, 20, 23, 31, 33, 35, 37, 42, 44, 46, and 48 days after suspending irrigation; irrigation was reinitiated when the photosynthetic rate approached zero. Water deficit conditions reduced all parameters that were evaluated except the chlorophyll index; stressed seedlings required 42 days for the photosynthetic rate to reach zero, but photosynthetic equilibrium was reestablished just 5 days after rehydration. This temporary water deficiency did not cause any permanent deleterious effects on the photosynthetic apparatus of the seedlings. These results suggest that H. speciosa seedlings can be cultivated during periods of water restriction in a greenhouse or in areas of recomposition where the periods of water deficiency does not exceed 42 days. According to Macedo et al. (1998), another factor that can restrict the expansion of the cultivated area is salinity, a problem commonly found in arid and semiarid regions characterized by strong annual deficits of rainfall. Albuquerque et al. (2002b) submitted mangabeira seedlings grown in sand and subjected to irrigation with NaCl solution at four levels (0, 50, 100, and 150 mol/m) and evaluated the stomatal behavior, growth, and evaporative demand for 30 days. After this time it was possible to observe that mangabeira presented high sensitivity to saline application such as stomatal closure and thus a reduction in its growth. Salinity also decreased transpiration from the treatment with 50 mol/m with a reduction of up to 91.75% in the most severe treatment when compared to the control.
FRUIT DEVELOPMENT The quality of the fruits depends on the development conditions, which consequently influence the postharvest life. Harvests before the fruit reaches full physiological maturity affect their maturation process and consequently their quality. On the contrary, the fully ripe fruit harvest reduces its useful life, hampers their handling and transportation due to its low physical strength, causing qualitative and quantitative losses (Chitarra and Chitarra, 1990).
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TABLE 1 Physical Characteristics of Mangaba Fruit at Three Stages of Maturation Characteristics
Maturation stages Green
Half Ripe
Ripe
Skin color
Light green
Greenish yellow
Yellow
Stains on skin
Absent
Present
Present
Visual aspect on cutting fruit
White pulp; seeds in formation
White pulp; seeds formed although soft
Yellowish pulp; hard seeds
Fruit texture
Hard
Slightly soft
Soft
Source: Arola, F.M., 1982. Isolamento e Caracterizac¸a˜o da Goma da Mangaba (Dissertation Masters course). Federal University of Paraiba, Joa˜o Pessoa, Brazil (Arola, 1982).
One of the most efficient techniques to enhance durability and minimize fruit losses is postharvest storage at low temperature. The use of refrigeration is used to decrease the respiration rate, water loss and thus delay fruit ripening (Paull, 1994). Proper storage is also critical to the successful commercialization of tropical fruits. According to Aguiar Filho and Bosco (1995), the total period related to the time covered between the opening of flowers and ripening of the native mangabeira in the coastal tablelands of Paraiba varies from 100 to 110 days. There are very few studies performed on mangaba fruit maturity and the changes associated with the ripening of this fruit. Some of the data organized on the basis of maturity stage of mangaba fruit are presented in Table 1. The mature green term is used to designate fruits that have reached physiological maturity or attained the maximum edible quality but are still in the early maturation (Narain, 1990). Sampaio (2002) noted that fruits at Emepa-PB in Joao Pessoa, Paraiba state of Brazil were harvested when they had a clear green color on the peel. Mangaba is a fruit that has respiratory behavior of climacteric type. The author also notes that the CO2 evolution clearly shows the stages of preclimacteric, least climacteric rise, climacteric maximum and postclimacteric phases. The climacteric maximum (peak) was reached after 39 h of harvest and it marked the beginning of the postclimacteric phase. Experiments undertaken at the Biology Laboratory and Post-Harvest Technology Center for Agricultural Sciences of Federal University of Paraiba reveal that the onset of climacteric maximum was dependent on the maturity stage of the fruit harvested (Moura, 2005). Carnelossi et al. (2004) studied the effect of storage temperature on the postharvest conservation and determined the physicochemical characteristics of the naturally fallen fruits of mangaba. The fruits were selected and stored in refrigerated conditions at temperatures of 6 C, 18 C and 25.2 C. During the storage period, samples at every 1, 3, 5, 7 and 9 days were removed for determination of vitamin C content, pH, titratable acidity and soluble solids ( Brix), water activity, conductivity, resistivity and diffusivity. It was found that the fallen fruits had concentrations of vitamin C and soluble solids higher than half-ripe fruits. Storage at 6 C was effective in maintaining the physicalchemical characteristics of half-ripe fruits while in fallen fruits, the physicochemical characteristics were maintained for a period up to 3 days when subjected to temperatures of 18 C and 25 C. They also reported a decrease in water activity and increase in thermal conductivity of mangaba during refrigerated storage. Thus, the thermal conductivity, resistivity and the water activity may be used as tracking parameters in postharvest mangaba fruits when stored under refrigeration.
CHEMICAL COMPOSITION AND NUTRITION The mangaba fruit consists of pulp (77%), peel (11%), and seed (12%). However, only the pulp occupies a prominent position in the commercial aspects. It features a good nutritional value; with a protein content (0.7 g/100 g pulp) greater than the majority of other fruit species. It is rich in various elements and in vitamins A, B1, B2 and C, as well as iron, phosphorus and calcium. The high iron content (28 mg/100 g pulp) in the fruit causes mangaba to be one of the richest nutrients, besides being a source of ascorbic acid. Hence the importance attached to the fruit is in curing some diseases and, in particular, against fever. The energy value for each 100 g of fruit is 43 calories. High total soluble solids content associated with high acidity and an exotic taste result in a greater appreciation of mangaba fruit by consumers. The mangaba fruit is a potential source of essential minerals such as calcium (8.52 mg/100 g ), zinc ( 0.12 mg/ 100 g) (Almeida et al., 2009), phosphorus (18 mg) and iron (2.8 mg) (Oliveira and Rock, 2008). Studies have been
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309
developed to use mangaba in the form of raisins due to its medicinal effects, suitable for patients during convalescence in the treatment of gastric ulcers (Vieira Neto, 1997; Souza, 2007). The mangaba leaves are also traditionally used to treat diabetes in Brazil. Pereira et al. (2015) assessed the antidiabetic potential of mangaba leaf extract and its fractions. The results showed an inhibition of α-glucosidase in vitro. Only the crude extract and dichloromethane fraction inhibited the hyperglycemic effect induced by starch or glucose. The combination of iron with vitamin C or ascorbic acid present in mangaba is an important feature in the fruit composition, as this vitamin increases the bioavailability of iron, or vitamin C increases iron absorption by the body. The tannin contents, which are phenolic compounds of a quite varied polymerized chemical nature, is also considered high. These phenolic compounds, present in foods such as green tea, black tea, grapes, and wine, are associated with antioxidant potential of food and prevent the development of chronic degenerative diseases. However, when present in excessive quantities, tannins may be responsible for the complexing of protein and minerals, reducing the nutritional value of the diet. According to Almeida et al. (1998), mangaba has low lipid content (0.3%1.5%) and these are rich in palmitic (29%); oleic (12%), linoleic (18%), and linolenic (8%) acids. The lipid content in the pulp of mangaba is insufficient for the commercial extraction of the same, but the high content of polyunsaturated fatty acids enriches the nutritional value of fruit. In mangaba pulp these fatty acids are represented by linoleic acid and especially p-linolenic acid, which are considered essential to the human body (Pereira et al., 2006). The physical and physicochemical characteristics of fruits are influenced by the soil and climatic conditions, cultivation, harvest time, genetic constitution, maturity stage and postharvest treatment, among others (Nascimento et al., 2014). Such features are quality factors of fundamental importance to the use and marketing of fruit pulp and preparation of processed products. Table 2 presents the physicochemical characteristics of mangaba reported by some authors.
VITAMIN C The major bioactive compounds present in mangaba fruits are phenolic compounds (phenolic acids, flavonoids), carotenoids, ascorbic acid (vitamin C), which contribute to the beneficial effects of this fruit (Silva et al., 2008; Almeida et al., 2009). Vitamin C is considered an important nutrient that occurs naturally and has antioxidant action when consumed in the diet (Almeida et al., 2011). It is easily absorbed from the small intestine by active sodium-dependent process and by passive diffusion (Boni et al., 2010). It has an anticancer effect and reduces radical tocopherol back to its active form in cell membranes (Almeida et al., 2011). Table 3 assembles the data on vitamin C content in mangaba pulp, as reported by several researchers. The mangaba is a fruit rich in vitamin C and its content ranged from 96.3 to 474.1 mg/100 g in fresh fruit pulp. In pasteurized pulps, Silva and Silva (2012) found vitamin C content varying from 114.29 to 347.62 mg/100 g. Considerable differences in the vitamin C content in mangaba have been reported that may be due to different species and varieties especially when they grow in different environmental conditions. The climate, soil and fertilization practices also affect the concentrations of vitamins in plants (Maia et al., 2007). (Ramful et al. (2011) classified fruits into three categories according to their ascorbic acid content: low (less than 30 mg/100 g), medium (3050 mg/100 g), and high (.50 mg/100 g). Thus there has been the high vitamin C present in mangaba additional to the presence of vitamin A and of bioactive compounds such as flavonoids, total phenolics, total carotenoids, and anthocyanins that all contribute to high antioxidant activity.
PHENOLIC COMPOUNDS The beneficial effect of phenolic compounds on human health has been related to its antiinflammatory activity and its ability to prevent the action of free radicals in the body (Rocha, 2011). The phenolic compounds composition of fruits is determined by genetic and environmental factors, and it may be modified by oxidative reactions during fruit storage when two important processes: the antioxidant activity and oxidative browning, occur (Rotili et al., 2013). H. speciosa is traditionally used in the treatment of several diseases, including hypertension and inflammatory diseases, mainly dermatitis, rheumatism, and hepatitis (Branda˜o et al., 2010). Although reports on antioxidant activity and quantities of bioactive compounds present in mangaba pulp are still scarce. Table 4 assembles some of the available data. The phenolic profile of the mangaba fruit pulp was determined by Lima et al. (2015b) who indicated the presence of flavonoids (catechin and rutin) and nonflavonoids (gallic acid, chlorogenic acid, vanillic acid, o-coumaric acid, and rosmarinic acid) revealing a predominant presence of chlorogenic acid (18.091 6 1.68 mg/100 g) and rutin (10.260 6 1.13 mg/100 g). Assumpc¸a˜o et al. (2014) also reported the presence of phenols and flavonoids in the
TABLE 2 Physicochemical Characteristics of Mangaba Pulp and Its Products References
Carnelossi et al. (2004)
Souza et al. (2007)
Rufino et al. (2009a)
Cohen and Sano (2010)
Rocha (2011)
Silva and Silva (2012)
Cardoso et al. (2014)
Nascimento et al. (2014)
Characteristics
Pulp from fallen fruits
Mature fruits
Fresh fruit pulp
Pulp from fallen fruits
Fresh fruit pulp
Fresh fruit pulp
Lyophilized pulp powder
Pasteurized pulp
Fresh fruit pulp
Mature fruits
pH
3.5
2.99
3.22
3.32
3.6
3.07
3.01
3.23; 3.47; 3.37; 3.35
3.6
3.93
15.2
17.23
21.5
18.8
14.2
14.83
14.42
15.14
17.04
aw
0.988
Acidity (% citric acid)
0.7
1.77
0.72
1.39
22.7
0.961.33
0.8
0.98
Moisture (%)
90.8
82.8
95.02
20.69
85.2 91.0;
83.03
Ash (%)
0.1
0.62
0.60
0.10 0.15
0.6
Proteins (%)
1.4
1.05b
2.73a
0.68 1.19
0.8
Lipids (%)
1.3
1.7
Brix
Not analyzed.
Santos et al. (2012)
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311
TABLE 3 Vitamin C (mg/100 g) Content in Mangaba Pulp According to Different Researchers Rufino et al. (2010)
Almeida et al. (2011)
Rocha (2011)
Cardoso et al. (2014)
Silva and Silva (2012)
Rocha (2010)
Fresh fruit pulp
190
93.3
474.1
165.82
110.68
Pasteurized pulp
114.29347.62
196.99
Not analyzed.
TABLE 4 Bioactive Compounds (per 100 g Pulp) Present in Mangaba Fruit Characteristics
Brasil (2003) (IDR-RDC 269,2005)
Moura (2005)
Ferreira and Marinho (2007)
Antioxidant activity
Vitamin C (ascorbic acid) (mg)
45.00
Total carotenoids (mg expressed as β-carotenol) Total phenolic compounds (mg expressed as gallic acid equivalent)
33.00
Almeida et al. (2011)
Clerici and Silva (2011)
3385 CE (g DPPH/g) 14.6 mmol trolox/g (ABTS) 162.57 ABTS (VCEAC) 118.78 DPPH (VCEAC) 10.84 ABTS (TEAC) 5.27 DPPH (TEAC)
18.30 mmol Fe2SO4/g (FRAP)
96.30
190.00
0.30 0.20 0.40
Rocha (2011)
0.30
98.80
Flavonoids (mg)
169.00
15.00
TEAC, trolox equivalent antioxidant capacity; VCEAC, vitamin C equivalent antioxidant capacity.
ethanolic extract of mangaba fruit. Gomes et al. (2013) also found high concentrations (113.4 μg/g) of chlorogenic acid in mangaba fruit. Rocha (2011) reported the lowest total phenolic content of 0.041 g/100 g in mangaba pulp while Rufino et al. (2009b) reported 0.171 g/100 g in mangaba pulp wiches much higher than reported by Rocha (2011). From the data reported until now, mangaba fruit qualifies itself with higher concentrations of phenolic compounds such as rutin, quercetin, and chlorogenic acid, compared to concentrations found in fruits such as blackberry, raspberry, buriti, guava, and umbu.
VOLATILE CONSTITUENTS Studies on the chemical composition and on volatile compounds of mangaba fruit are still scarce. Sampaio and Nogueira (2006) reported a number of compounds from different chemical classes that could contribute to the typical aroma of mangaba fruit in three stages of maturation. The volatile compounds were extracted by simultaneous distillation technique and they identified 33 compounds in mature fruits; the principal compounds being 1-octen-3-ol (2.8%), such as (Z)-linalool oxide (9.1%), (E)-linalool oxide (6.3%), linalool (16.1%), 2-phenylethanol (4.5%), α-terpineol (5.5%), geraniol (3.1%), hexadecanal (2.5%) and octadecanol (2.7%); and 32 compounds in ripe fruits such as 3hydroxy-2-butanone (9.1%), 2,4,5-trimethyl-1,3-dioxolane (6.8%), 3-methyl-3-buten-1-ol (12.1%), 3-methyl-1-butanol
312
Exotic Fruits Reference Guide
TABLE 5 Volatile Compounds Present in Pulp of Ripe Mangaba Fruit and Their Characteristic Odor Notes Sampaio and Nogueira (2006)
Narain et al. (2010)
Assumpc¸a˜o et al. (2014)
Lima et al. (2015b)
Odor descriptionb
Ethanol
x
Sweet
3-Pentanol
x
Sweet, herbal, oily, nutty
3-Hexanol
x
Green, fruity, solvent
Compounds
Alcohols
3-Methyl-2-pentanol
x
3-Methyl 3-buten-1-ol
x
x
Sweet, fruity
x
Mushroom
(E)-2-Penten-1-ol
x
Sweet, caramellic
a
Benzyl alcohol
x
Sweet, flower
Butane-2,3 diol
x
Fruity, creamy, buttery
3-Methyl-1-butanol
x
Alcoholic, pungent, fruity
a
5-Methyl furfuryl alcohol
4-Penten-1-ol
x
trans-Hex-3-en-1-ol
x
Green, bitter, earthy, fatty
Hexane-1-ol
x
Herbal
Decan-1-ol
x
Waxy, floral, orange
Nonen-3-1-ol
x
Earthy
trans-Dec-2-en-1-ol
x
Waxy, fresh, air, citrus
Dodecanese-1-ol
x
2-Propyldecanol
x
1,3-Butanediol
x
Odorless
1-Octen-3-ol
x
Earthy, green, oily
3-Methyl-2-butenol
x
Sweet, fruity
(Z)-3-Hexenol
x
Grass
1-Hexanol
x
Herbal
Benzyl alcohol
x
Sweet, flower
2-Phenylethanol
x
Rose
x
Earthy, alcohol, nutty
Benzaldehyde
x
x
Almond, burnt, sugar
Furfural
x
x
Bread, almond, sweet
Hexanal
x
x
x
Grass, tallow, fat
2-Hexenal
x
x
Apple, green, fat, rancid
trans-Hexa-2,4-dienal
x
Sweet, green, spicy, floral
Aldehydes Propionaldehydea a
trans-Oct-2-enal
x
Fresh, fatty, green
Nonanal
x
Fat, citrus, green
trans-Non-2-enal
x
Green, cucumber, aldehydic
Decanal
x
Soap, orange peel, tallow (Continued )
Mangaba—Hancornia speciosa
313
TABLE 5 (Continued) Compounds
Sampaio and Nogueira (2006)
Narain et al. (2010)
Assumpc¸a˜o et al. (2014)
Lima et al. (2015b)
Odor descriptionb
trans-Dec-2-enal
x
Waxy, fatty, earthy
5-Methyl-furfural
x
Almond, caramel, burnt sugar
x
2-Phenylacetaldehyde
x
Green, sweet, floral
Phenyl acetaldehyde
x
Honey, floral, rose
x
Pungent, green, fruity
x
x
Pineapple
x
Fruity, sweet, banana
x
Fruity, raspberry, pear
Ethyl 2-methylbutyrate
x
Fruity, grape, pineapple
Butyl acetate
x
Pear
Amyl isobutyrate
x
Fruity, apricot, buttery
2-Methylethyl butanoate
x
Cyclohexyl formate
x
Fruity, sweet, musty
x
Sweet, coconut, nutty
n-Propyl n-heptanoate
x
(E)-5-Decen-1-yl acetate
x
Terpinyl acetate
x
Pine, citrus
Linalyl hexanoatea
x
Green, warm, fruity
n-Heptyl phenyl acetate
x
Methyl 1,2dimethyltetradecanoate
X
Methyl lactate
x
Ethyl lactate
x
Fruit
Hexyl acetate
x
Fruit, herb
Ethyl butanoate
x
Cashew, pineapple
Isopentyl acetate
X
Sweet, banana, fruity
4-Isopentyl acetate
X
3-Methyl-2-butenyl acetate
X
Sweet, fresh, fruity
Ethyl hexanoate
X
Apple peel, fruit
(Z)-3-Hexen-1-yl acetate
x
Fresh, green, sweet
n-Hexyl acetate
x
Fruit, herb
Benzyl acetate
x
Fresh, boiled vegetable
Methyl octadecanoate
x
2-Propyl furan a
(E)-2-Pentenal
a
Bicyclo [2.2.0] hexane-1carbaldehyde Esters Ethyl acetatea a
Isopropyl acetate a
Propyl acetate
a
a
a
a-Angelica lactone
a
a
(Continued )
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Exotic Fruits Reference Guide
TABLE 5 (Continued) Compounds
Sampaio and Nogueira (2006)
Narain et al. (2010)
Assumpc¸a˜o et al. (2014)
Lima et al. (2015b)
Odor descriptionb
Cinnamyl n-heptanoatea
x
n-Butyl acetate
x
Ethereal, fruity
3-Methyl-1-butanyl acetate
x
3-Methyl-3-buten-1-yl acetate
x
Fruity
Methyl benzoate
x
Prune, lettuce, herb, sweet
Methyl salicylate
x
Peppermint
2-Pentanone
x
Sweet, fruity, woody
1-Penten-3-one
x
2,3-Pentenedionea
x
Buttery, nutty, caramellic
3-Hidroxy-2-butanone
x
x
Sweet, buttery, creamy
3-Methoxy-3-methyl-2butanone
x
3-Hydroxy-2-butanone
x
2-Octanone
x
Earthy, weedy, woody
Acetophenone
x
Must, flower, almond
1,4-Cyclohex-2-enedione
x
2-Hydroxy-2-butanone
x
Buttery
x
Ripe apricot, fruit, woody
Ketones
a
Dihydro actinidiolide Lactones δ-Valerolactonea
x
Herbal, sweet, warm
γ-Decalactone
x
x
Fruity, peach, creamy
Camphene
x
Camphor
D-Limonene
x
Citrus, herbal, camphor
(E)-Linalool oxide
x
x
Flower
a
Linalool
x
x
x
Flower, lavender
β-Cubebene
x
Citrus, fruity, radish
β-Sesquiphelandrene
x
Geraniol
x
Rose, geranium
Eugenol
x
Clove, honey
(E,E)-Farnesol
x
Mild muguet, floral, lily
trans-Linalool oxide
x
Floral
α-Terpineol
x
Oil, anise, mint
Terpenes
Herbal, fruity, woody
Nerol
x
Sweet
α-Copaene
x
Wood, spice
β-Elemene
x
Pungent (Continued )
Mangaba—Hancornia speciosa
TABLE 5 (Continued) Compounds
Sampaio and Nogueira (2006)
Narain et al. (2010)
Assumpc¸a˜o et al. (2014)
Lima et al. (2015b)
Odor descriptionb
(Z)-β-Caryophyllene
x
Spicy
Isocitronellene
x
(Z)-Linalool oxide
x
Flower
α-Terpineol
x
Oil, anise, mint
1,3,8-p-Menthatriene
x
2-Ethyl-3-methylpyrazinea
x
Nutty, peanut, musty
2,5-Diethyl-3methylpyrazinea
x
Toasted, nutty, meaty
Benzene
x
Aromatic
Toluene
x
Paint
o-Xylene
x
Geranium
1,3,5-Trimethyl benzene
x
p-Isopropyl phenol
x
Woody, warm, spicy
Dimethyl disulfide
x
Onion, cabbage, putrid
Isopropyl disulfide
x
Sulfurous
Dihexylsulfidric
x
Tetradecane
x
Alkane
Hexadecane
x
Alkane
Heptadecane
x
Alkane
Octadec-1-ene
x
Octadecan
x
Alkane
Dimethylundecane
x
Alkane
Docosane
x
Alkane
Hex-1-ene
x
3,3-Dimethylhexane
x
2,4,5-Trimethyl-1,3dioxolane
x
2-Methyl furfuryla
x
Chocolate
Dodecanoic acid
x
Mild fatty, coconut
2-Ethyl-3-methylindole
x
Pyrazines
Aromatic Compounds
Sulfurous Compounds
Hydrocarbons
Others
() not identified. (x) Identified. a Identified tentatively based on retention index datum and spectrum verification from the NIST mass library or literature (Jennings and Shibamoto 1980 Adams, 1995). b Odor description from Good scents Company: http://www.thegoodscentscompany.com/index.html.
315
316
Exotic Fruits Reference Guide
(5.2%), furfural (8.3%), 3-methyl-1-butanyl acetate (8.8%) and 3-methyl-3-buten-1-yl acetate (28.2%). Table 5 lists the volatiles compounds identified in mangaba pulp by some authors. A total of 61 compounds were identified by Narain et al. (2010), out of which 38 compounds were positively identified and 23 were tentatively identified. The volatile compounds identified in the pulp of ripe mangaba fruit were 17 compounds belonging to the class of esters (23.54%), 13 alcohols (33.81%), 5 aldehydes (5.72%), 5 aromatics (2.89%), 4 terpenes (5.42%), 4 ketones (0.96%) and 2 sulfur compounds (0.23%). When related to the area of the chromatogram, the major compounds identified were 3-hexanol (12.75%), isopropyl acetate (11.30%), 3-pentanol (9.93%), 3-methyl 3-buten-1-ol (4.98%), ethyl acetate (4.44%), δ-limonene (4.63%), ethanol (3.97%), dihydro actinidiolide (3.69%), (E)-2-pentenal (3.27%), amyl isobutyrate (2.62%), 2-phenylacetaldehyde (2.20%), β-cubebene (1.89%) and linalyl hexanoate (1.25%). Assumpc¸a˜o et al. (2014) analyzed the volatile compounds of mangaba pulp through the technique of solid phase micro extraction using gas chromatography coupled to mass spectrometer. The identified volatile compounds which corresponded to 83.72% of the total area of the peaks. The chemical classes of compounds were esters (6 compounds), aldehydes (3 compounds), alcohols (3 compounds), hydrocarbons (2 compounds) and ketone (one compound). Esters represented majority area (68.11% of the total area of peaks), emphasizing the importance of this class of compounds present in mangaba. The esters are among the most important compounds for the flavor industry due to its fruity odor and it is important both for natural foods and in fermented foods, although these may be present at low concentrations (1100 ppm) (Kempler, 1983). Lima et al. (2015b) investigated the effects of storage on volatile constituents of mangaba fruit. The fruits were stored at four different temperatures (0 C, 6 C, 12 C, and 24 6 1 C) for 20 days with GC-MS analysis was performed on every 5 days. It was possible to identify a total of 36 compounds which included alcohols (25%), aldehydes (25%), terpenes (19%), esters (9%) and ketones (3%) and other compounds (19%). The compounds linalool, dodecan-1-ol and trans-hex-2-enal were present in all samples of mangaba fruit stored at different temperatures. Table 5 lists the compounds such as 3-hexanol, isopropyl acetate, 3-pentanol, 3-methyl 3-buten-1-ol, ethyl acetate, δ-limonene, ethanol, dihydro actinidiolide, (E)-2-pentenal, amyl isobutyrate, 2-phenylacetaldehyde, β-cubebene, linalyl hexanoate, 3-methyl-2-butenol, propyl acetate, ethyl 2-methylbutyrate and γ-decalactone, which characterize for, sweet, fruity and green odor and these could be responsible for mangaba aroma.
FINAL CONSIDERATIONS This chapter on mangaba fruit focuses on its production, botanical aspects, physiology, and biochemistry during the development of fruit at different stages of its maturity along with its physicochemical characteristics. Although there are few publications and the available data are still scant, emphasis is still on the fruits’ vitamin C, flavonoids and phenolic compound contents. Overall this review updates the work done on mangaba, however, it indicates that there is a greater need to undertake extensive systematic research so as to explore its potential fully.
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Compostos bioativos e atividade antioxidante na popla de mangaba (Hancornia speciosa Gomes) in natura e pasteurizada (Dissertac¸a˜o (mestrado)). Universidade Federal de Sergipe, Programa de Po´s-Graduac¸a˜o em Ciencia e Tecnologia de Alimentos. Aracaju SE. Rocha, M.S., 2011. Dissertac¸a˜o (mestado). Compostos Bioativos e Atividade Antioxidante (in vitro) de Frutos do Cerrado Piauiense. Universidade Federal do Piauı´ - Teresina PI. Rotili, M.C.C., Celant, V.M., Vorpagel, J.A., Barp, F.K., Salibe, A.B., Braga, G.C., 2013. Composic¸a˜o, atividade antioxidante e qualidade do maracuja´-amarelo durante armazenamento. Semina: Cieˆnc. Agra´r. 34 (1), 227240. Rufino, M.S.M., Alves, R.E., Brito, E.S., Silveira, M.R.S., Moura, C.F.H., 2009a. Quality for fresh consumption and processing of some non-traditional tropical fruits from Brazil. Fruits. 64, 361370. Rufino, M.S.M., Alves, R.E., Brito, E.S., Perez-Jimenez, J., Saura-Calixto, F.D., 2009b. Total phenolic content and antioxidant activity in acerola, ac¸aı´, mangaba and uvaia fruits by DPPH method. Acta Horticult. 841, 459462. Rufino, M.S.M., Alves, R.E., Brito, E.S., Perez-Jimenez, J., Saura-Calixto, F.D., Mancini Filho, J., 2010. Bioactive compounds and antioxidant capacities of eighteen non-traditional tropical fruits from Brazil. Food Chem. 121, 9961002. Sampaio, S. de A., 2002. Transformac¸o˜es durante o amadurecimento po´s-colheita de frutos de cajazeira (Spondias mombim), ciriguela (Spondias purpu´rea L.) e mangabeira (Hancornia speciosa Gomes). UFPB, Joa˜o Pessoa. 76f. Dissertac¸a˜o (Mestrado em Cieˆncia e Tecnologia de Alimentos). Sampaio, S.T., Nogueira L.P., 2006. Volatile components of mangaba fruit (Hancornia speciosa G.) at three stages of maturity. Food Chemistry, 95(4), 606610. Santos, A.R.F. dos, Silva, A.V.C. da, Goes, I.B., Souza, E.M. de, Muniz, E.N., Narain, N., 2007. Situac¸a˜o atual e perspectivas para o cultivo da mangaba no estado de Sergipe; 30a Reunia˜o Nordestina de Botaˆnica. Universidade Regional do Cariri, Crato. Santos, J.T.S., Costa, F.S.C., Soares, D.S.C., Campos, A.F.P., Carnelossi, M.A.G., Nunes, T.P., Ju´nior, A.M.O., 2012. Avaliac¸a˜o de mangaba liofilizada atrave´s de paraˆmetros fı´sico-quı´micos. Sci. Plena. 8 (3). Scalon, S.P.Q., Kodama, F.M., Dresch, D.M., 2015. Gas Exchange and photosynthetic activity in Hancornia speciosa GOMES seedlings under water deficit conditions and during rehydration. Biosci. J. 31 (4), 11241132. Silva, A.N.C. da, Silva, A.C.M.S., 2012. Qualidade da polpa congelada de mangaba, comercializada em Aracaju, Sergipe. Boletim de Pesquisa e Desenvolvimento, 70, Embrapa Tabuleiros Costeiros, Aracaju- SE, dez, pp. 116. Silva, E.C., Nogueira, R.J.M.C., Neto, A.D.Z., Santos, V.F., 2002. Comportamento estoma´tico e potencial da a´gua da folha em treˆs espe´cies lenhosas cultivadas sob estresse hı´drico. Acta Bot. Bras. 17, 231246. Silva, M.R., Lacerda, D.B.C.L., Santos, G.G., Martina, D.M., de, O., 2008. Caracterizac¸a˜o quı´mica dos frutos nativos do cerrado. Cieˆnc. Rural. 38 (6), 17901793. Singh, B., Singh, G., 2006. Effects of controlled irrigation on water potential, nitrogen uptake and biomass production in Dalbergia sissoo seedlings. Environ. Exp. Bot. 55, 209219. Souza, F.G., 2004. Qualidade po´s-colheita de mangabas (Hancornia speciosa GOMES) oriundas do Jardim Clonal da Emepa-PB. 90 f. Dissertac¸a˜o (Mestrado em Tecnologia de Alimentos) - Universidade Federal do Ceara´, Fortaleza. Souza, R.P., Machado, E.C., Silva, J.A.B., Lagoa, A.M.M.A., Silveira, J.A.G., 2004. Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ. Exp. Bot. 51, 4556. Souza, M.C., 2007. Qualidade e atividade antioxidante de frutos de diferentes progeˆnies de ac¸aizeiro (Euterpe oleracea Mart), 124 pp. Mestrado em Cieˆncia e Tecnologia de Alimentos) Universidade Federal do Ceara´, Fortaleza. Souza, F.G., Figueiredo, R.W., Alves, R.E., Maia, G.A., Arau´jo, I. Ad, 2007. Qualidade po´s-colheita de frutos de diferentes clones de mangabeira (Hancornia speciosa GOMES). Cieˆncia Agrotecnol. 31 (5), 14491454. Vieira Neto, R.D., 1994. Cultura da mangabeira EMBRAPA-CPATC, Aracaju, 16 pp. Vieira Neto, R.D., 1997. Caracterizac¸a˜o fı´sica de frutos de uma populac¸a˜o de mangabeiras (Hancornia speciosa Gomes). Rev. Bras. Frutic. 19 (2), 247250. Wu, F.Z., Bao, W.K., Li, F.L., Wu, N., 2008. Effects of drought stress and N supply on the growth, biomass partitioning and water-use efficiency of Sophora davidii seedlings. Environ. Exp. Bot. 63, 248255. Zhang, M., Chen, Q., Shen, S., 2011. Physiological responses of two Jerusalem artichoke cultivars to drought stress induced by polyethylene glycol. Acta Physiol. Plant. 33, 313318.
FURTHER READING Vieira Neto, R.D., Cintra, F.L.D., Ledo, A.S., Silva Junior, J.F., Costa, J.L.S., Silva, A.A.G., Cuenca, M.A.G., 2002. Sistema de produc¸a˜o de mangaba para os tabuleiros costeiros e baixada litoraˆnea. Aracaju: Embrapa Tabuleiros Costeiros. 22 pp. (Embrapa Tabuleiros Costeiros. Sistemas de Produc¸a˜o, 02). Available at: ,http//www.cpatc.embrapa.br. (accessed 02.07.16.).
Noni—Morinda citrifolia L. Moˆnica M. de Almeida Lopes1, Alex Guimara˜es Sanches1, Joa˜o A. de Sousa2 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Origin and Botanical Aspects Cultivation Practices and Harvest Postharvest and Nutritional Value
319 319 322
Industrial Uses References
323 324
ORIGIN AND BOTANICAL ASPECTS Noni is the Hawaiian name for the fruit of Morinda citrifolia Linn (Rubiaceae). A plant species native from southeast Asia to Australia, noni grows in tropical and subtropical climates as observed in Polynesia, India, the Caribbean, central and northern South America (Dixon et al., 1999; Ross 2001), classified taxonomically as: class Magnoliopsida, order Gentianales, family Rubiaceae, genus Morinda and species Morinda citrifolia. Various vernacular names are common for M. citrifolia as “Indian mulberry”, “nuna”, or “ach” on the Indian subcontinent, “mengkudu” in Malaysia, “nhau” in Southeast Asia, “painkiller bush” in the Caribbean, or “cheese fruit” in Australia (Morton, 1992; Nelson, 2001; Wang et al., 2002; Cardon, 2003). Currently, there are two recognized varieties of M. citrifolia (M. citrifolia var. citrifolia and M. citrifolia var. bracteata) and one cultivar (M. citrifolia cultivar Potteri). The most commonly found variety is M. citrifolia var. citrifolia, with the greatest health and economic importance (Pawlus and Kinghorn, 2007). M. citrifolia is a bush or small tree, 310 m tall, with abundant wide elliptical leaves (517 cm length, 1040 cm width). The small tubular white flowers are grouped together and inserted on the peduncle. The petioles leave ring-like marks on the stalks and the corolla is greenish-white (Morton, 1992; Dixon et al., 1999; Ross, 2001; Cardon, 2003). The noni fruit is a syncarp formed by united carpels (310 cm length, 36 cm width), oval and fleshy with an embossed appearance (Figs. 1 and 2). It is slightly wrinkly, semitranslucent, and ranges in color from green to yellow, to almost white at the time of harvest. It is covered with small reddish-brown buds containing the seeds (about 200 per fruit, measuring 310 mm length). Noni seeds are albuminous and have a thick seed coat, rich in lignin, lipid (43.50%) and protein (9.15%), and soluble sugars (5%). The linoleic acids is the lipid fraction most prevalent (68.10%) in noni seeds and are mobilized during germination, suffering a reduction of up to 38% of its total (Paula et al., 2016). The ripe fruit exhales a strong butyric acid-like rancid smell (Morton, 1992; Dixon et al., 1999). The fruits can weigh between 100 and 300 g, and each axillary gemma produces only one fruit, but there are cases of producing two or more fruits (Acosta, 2003). The pulp is juicy and bitter, light dull yellow or whitish, gelatinous when the fruit is ripe; numerous hard triangular reddish-brown pits are found, each containing four seeds (approximately 3.5 mm) (Wang et al., 2002; Dittmar 1993).
CULTIVATION PRACTICES AND HARVEST Noni grows on a wide variety of soils and survives in severe habitats, such as in rocky, sandy, coastal, and volcanic terrains. The noni plant is considered tolerant to salinity, including areas flooded by tsunamis, even benefiting from the minerals contained in seawater (Nelson, 2005). Noni is propagated either from seed or stem cuttings. The primary disadvantage from seed propagation is when the seed is untreated, resulting in the germination up to 612 months or Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00042-3 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Developmental stages of noni (Morinda citrifolia): (A): unripe noni; (B): breaker noni; (C) ripe noni. Source: Sousa, A., Neto, M.A.S., Garruti, D.S., Sousa, J. and Brito, E.S. 2010. Evaluation of noni (Morinda citrifolia) volatile profile by dynamic headspace and gas chromatography-mass spectrometry. Cieˆnc. Tecnol. Aliment. 30(3): 641644.
more, whereas stem cuttings can be rooted in approximately 12 months. The disadvantage of producing plants vegetatively from cuttings is that they may not be as strong and disease-resistant as seedlings, and the trunk and branches may split and break during the first years of fruit production (Nelson, 2003). The noni plant develops, grows, and produce fruits in areas with average annual precipitation between 250 and 4000 mm and altitude of up to 800 m, covering arid and extremely humid regions, however, when the precipitation is very low, irrigation is needed (Nelson and Elevitch, 2006). The noni plant has an adapted to variations of temperature with a maximum of 32 C38 C and the minimum between 5 C and 18 C (Gilani et al., 2010). Nelson and Elevitch (2006) indicate the use of fertilizer in commercial formulas 141414 or 161616 (Nitrogen, Phosphorus, Potassium or NPK, respectively) to fertilize young plants without production of fruits. However, in the phase of fructification of plants, the application of 102020 is indicated to stimulate the flowering and yield. Also, is important to point out that noni plants at all ages of development respond to foliar fertilizer applications. The production of noni present higher yield in terms of pulp with organic fertilization and potassium chloride, with greater viability in the period of high rainfall. Fertilization with potassium chloride and organic matter provide in the layers soil at 020 cm and 2040 cm higher levels of potassium, phosphorus, and pH. The plants grow more during the period of low rainfall and produced more during the period of high rainfall (Da Silva et al., 2012).
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321
FIGURE 2 Tree of Noni (Morinda citrifolia) overview.
TABLE 1 Evolution of Fruit Skin Color and Firmness in the Course of Ripening of Noni Fruits Maturity stage
Color
Firmness
1
Dark green
Very hard
2
Greenyellow
Very hard
3
Pale yellow
Very hard
4
Pale yellow
Fairly hard
5
Translucent grayish
Soft
Source: Chan-Blanco, Y., Vaillant, F., Perez, A.M., Reynes, M., Brillouet, J.M. and Brat, P. 2006. The noni fruit (Morinda citrifolia L.): a review of agricultural research, nutritional and therapeutic properties. J. Food Compos. Anal. 19, 645654.
M. citrifolia is a perennial bush and it is possible to find fruits at different stages of maturity on the same plant at the same time. The species is generally found from sea level to 400 m altitude, although it adapts better to coastal regions (Luberck and Hannes, 2001). Under favorable conditions, the plant can bear fruit about nine months to one year after planting, where M. citrifolia plots are usually harvested two or three times per month and one hectare of M. citrifolia can yield around 35 tons of juice. Fruits are usually harvested at different stages, but most processors buy them at the ‘hard white’ stage for juice production (Chan-Blanco et al., 2006). Some producers choose not to harvest in the first year, and they prune in order to let the bush grow stronger. In Hawaii, noni fruits are harvested throughout the year, although there are seasonal patterns in flowering and fruit bearing (meteorological factors, fumigation, and irrigation) (Nelson, 2001, 2003). In Hawaii, noni plots are usually harvested two or three times per month, although fruit production is lower during winter. Depending on the postharvest technology programme adopted, the fruits may be harvested at different stages of development and continue to mature (Table 1) (Chan-Blanco et al., 2006). Nonetheless, most processors buy noni harvested at the ‘hard white’ stage for juice production, as the fruits become soft too quickly once this stage is reached (Nelson, 2001, 2003). The change from stage 4 to stage 5 occurs very quickly (only a few hours) and the pulp practically liquefies and turns from green to white, as well as developing the characteristic butyric smell. The fruits are individually selected on the tree and harvested by hand. At the “hard white” stage (Fig. 1C), they are well able to withstand being transported in baskets or containers, and exposure of the fruits to light or high temperatures immediately after harvest does not affect their overall quality. Before processing, fruits are ripened at room temperature for a day or more, depending on the end products i.e. tea, juice, pulp or dietetic products (Nelson, 2003).
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POSTHARVEST AND NUTRITIONAL VALUE According to Wall et al. (2015), the noni during ripening presented a nonclimacteric respiratory pattern (34 mg CO2/kg per h) and it was not possible to detect ethylene production (, 0.1 μg/kg per h). According to these authors, fruit firmness decrease from 59.30N, when the fruit is physiologically mature (very hard) and reaches 1N for noni ripe, with fruits very soft and translucent. Mature fruits ripened fully within 3 days of harvest. During ripening of noni fruits, Ca´rdenas-Coronel et al. (2015) reported firmness values to unripe fruits of 235N (dark green), reaching at end of ripening values of 6N (translucent grayish). According to the same authors, the color of skin fruits, evaluated as luminosity, chromaticity and hue angle, decreased during ripening. These changes happen very rapidly after harvest, especially the transition from stage 4 to stage 5 (Table 1). Analyses of the physicochemical composition of noni have shown that the fruit contains 91% water, total carbohydrates (9.60%), protein (2.50%), lipids (0.30%), fibers (1.0%), soluble solids (9.20oBrix), and minerals as Na % (19.70 mg/100 g) and potassium (5012 mg/100 g) (Faria et al., 2014) (Table 2). Almost 200 phytochemicals were identified and isolated from different parts of M. citrifolia (Singh, 2012). The chemical compositions and their concentrations are related significantly not only to the part of the plant but also to its country of origin (Deng et al., 2010), and to the harvesting season (Iloki Assanga et al., 2013). Phenolic compounds are dominant in the fruit, including damnacanthal, scopoletin, morindone, alizarin, aucubin, nordamnacanthal, rubiadin, rubiadin-1-methyl ether, and anthraquinone glycosides (Mahanthesh et al., 2013). Fruit juice of M. citrifolia from Cambodia presented various minerals including potassium (0.25 g/100 g), sulfur (0.30 g/100 g), calcium (0.29 g/100 g), phosphorus (0.25 g/100 g), and traces of selenium (0.90 μg/g) (Chunhieng, 2003), while vitamins such as ascorbic (101.41 mg/100 g) acid and pro-vitamin A were detected in the Brazilian and Micronesian M. citrifolia fruit (Da Silva et al., 2012; Krishnaiah et al., 2012). Mexican M. citrifolia fruit was assessed during its different maturity stages (1—dark green; 2—green-yellow; 3— pale-yellow and 4—translucent grayish) for its phytochemical constituents, finding that it has high levels of soluble protein, carbohydrates, ascorbic acid, rutin and phenols, with an independent profile of season (Lewis-Luja´n et al., 2014). Brazilian M. citrifolia fresh fruit pulp showed the presence of reducing sugars mainly glucose (12.30%), proteins (2.72%), and suggested large amount of minerals (Da Silva et al., 2012). Recently, phytochemical screenings of different commercial Nigerian M. citrifolia juice extracts confirmed the presence of secondary metabolites such as reducing sugars, phenols, tannins, flavonoids, saponins, glycosides, steroids, terpenoids, alkaloids, and acidic components, and the study also reported the absence of anthraquinones, phylobatannins and resins (Anugweje, 2015). Due to their therapeutic potential, fruit juice noni is highly sought after in popular medicine because it is used against several diseases such as diabetes, antiinflammatory conditions, heart diseases, and it possesses a cancer-preventative effect (Palu et al., 2011; Fletcher et al., 2013).
TABLE 2 Physicochemical Composition of Ripe Noni Pulp (Morinda citrifolia L.) Without Seeds Physicochemical parameters
Content
References
Moisture
9091
Chunhieng et al. (2003), Faria et al. (2014)
5.279.60
Lewis-Luja´n et al. (2014), Faria et al. (2014)
Soluble solids ( Brix)
9.009.20
Canuto et al. (2010), Faria et al. (2014)
Protein (%)
2.362.50
Faria et al. (2014)
Lipids (%)
0.040.30
Faria et al. (2014)
Total fibers (%)
1.00
Faria et al. (2014)
Ashes (%)
0.661.34
Faria et al. (2014), Lewis-Luja´n et al. (2014)
Na (mg/100 g)
19.76
Faria et al. (2014)
K (mg/100 g)
39005012
Chunhieng et al. (2003), Faria et al. (2014)
Titratable acidity (g/100 g)
3.206.82
Canuto et al. (2010), Faria et al. (2014)
pH
3.544.00
Faria et al. (2014), Chan-Blanco et al. (2006)
Total carbohydrates (%)
Noni—Morinda citrifolia L.
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Noni fruits contain (2E,4Z,7Z)-decatrienoic acid (DTA). This uncommon polyunsaturated fatty acid is rarely found in the plant kingdom, but it contributes to the off-flavors and postharvest spoilage of plants as a result of lipoxygenase activity (Zhuang et al., 1994). DTA is sensitive to heat evaporation during juice processing. Therefore, it could be used to distinguish among juices produced via different methods; that is, those with or without a fermentation step, or those based on rehydration of fruit juice concentrates (Basar and Westendorf, 2011). A phytochemical screening for the presence of secondary metabolite was conducted on the Indian M. citrifolia fruit aqueous, ethanol and methanol extracts detecting steroids, cardiac glycosides, phenol, tannins, terpenoids, alkaloids, carbohydrates, flavonoids, reducing sugar, lipids and fats in all types of extracts, while saponins in aqueous and methanol extracts, as well as acidic compounds in aqueous extract only (Nagalingam et al., 2012). Brazilian aqueous extracts from M. citrifolia leaves that underwent phytochemical screening showed the presence of alkaloids, coumarins, flavonoids, tannins, saponins, steroids, and triterpenoids (Serafini et al., 2011). The volatile profile of noni pulp, cultivated on the northeast of Brazil, by headspace analysis revealed 37 volatile compounds were detected, mainly alcohols (63.30%), esters (26.90%), cetones (7.40%), and acids (1.20%) (Sousa et al., 2010). About 51 volatile compounds have been identified in the ripe fruit (Sang et al., 2001), including organic acids (mainly caproic, caprylic, octanoic, and hexanoic acids), alcohols (3 methyl 3-buten-1-ol), esters (methyl octanoate, methyl decanoate), ketones (2-heptanone), and lactones (E-6-dodeceno-γ-lactone) (Farine et al., 1996). Yang et al. (2009), after a screening for chemical composition from the Chinese dried M. citrifolia seeds, identified 20 compounds including: daucosterol, ursolic acid, 19-hydroxylursolic acid, 1,5,15-trimethylmorindol, 5,15-dimethylmorindol, scopoletin, 3,30 -bisdemethylpinoresinol, 3,4,30 40 -tetrahydroxy-9,70 α-epoxylignano-7α,90 -lactone, americanin D, americanin A, americanin, isoprincepin, deacetyl- asperulosidic acid, loganic acid, asperulosidic acid, rhodolatouside, quercetin-3-O-α-L-rhamnopyranosyl-(1-6)-β-D-glucopyranoside, 4-ethyl-2-hydroxyl-succinate, 5-hydroxymethyl2-furancarboxaldehyde, 3-methylbut-3-enyl-6-O-β-D-glucopyranosyl-β-D-glucopyranoside. The chemical constituents of the leaf, flower, root and bark of the noni root are described by Elkins (1998) as follows: In the leaf: amino acids (alanine, arginine, aspartic acid, cysteine, cystine, glycine, glutamic acid, histidine, leucine, isoleucine, methionine, phenylalanine, proline, serine, threonine, tryptophan, tyrosine, and valine), anthraquinones, glycosides, phenolic components, resins, β-sitosterol and ursolic acid. In flower: acacetin 7-O-D (1)—Glucopyranoside; 5,7-dimethyl apigenin-4-O-8-D (1)—galactofiranoside; and 6,8-dimethoxy-3-methyl antroquinone-1-O-8-rhamnosyl glucopyranoside. In the root and root bark: alizarin, anthraquinones, carbonate, chlorubine, rubicholic acid, soranjidol, chrysophanol, phosphorus, magnesium, iron, sodium, glycoside, morindadiol, morindine, resins, rubiadin, and sterols. Moreover, research reports clearly indicate that due the presence of phytochemicals isolated from leaves, roots, flowers and fruits, the noni plant has a diversity of pharmacological activities in the areas of antifungal (Jayaraman et al., 2008), antioxidant (Krishnaiah et al., 2012), antiinflammatory (Palu et al., 2012), antiarthritic (Saraswathi et al., 2012), and anticancer (Lv et al., 2011).
INDUSTRIAL USES M. citrifolia is involved in various green industrial sectors, including juice products, natural preservative for food industry, natural sources of medicine and chemical reagents and green insecticide. In 2003, the fruit juice of M. citrifolia was approved as a novel food by the European commission; however, this approval was limited to Tahitian fruit juice only, no other products (Potterat and Hamburger, 2007). The bioactive screening of the Thai M. citrifolia fermented fruit juice recorded a superior vitamins content (C, B1, B2, B3, B12) in comparison to the vitamin content of the American M. citrifolia fruit, it also contains alkaloids, anthraquinones, antioxidants, essential oils, flavonoids, saponins, scopoletin and sugars, and these results were congruent to the content of the commercial Thai fruit juice content (Nandhasri et al., 2005). M. citrifolia is recognized as a novel food ingredient by the name of Noni fruit puree (Efsa, 2009). The butylated hydroxytoluene, a phenol derivative, act as natural preservative blocking the warmed-over flavor in formerly stewed beef pies, by reducing lipid oxidation, as well as enhancing color stability and the shelf life of the final aerobically wrapped pies (Zin et al., 2002; Nathan et al., 2012). The aqueous root extract of Indian M. citrifolia is used in the nanobiotechnology field for the synthesis of ecological noble metal nanoparticles due to the presence of anthraquinones. Suman et al. (2013) prepared silver nanoparticles by the reduction of silver nitrate into silver ions upon adding M. citrifolia root aqueous extract with a cytotoxic activity against the HeLa cell lines. Acetone extract of Thai M. citrifolia dried roots was reported as a source of natural reagents for the flow injection spectrophotometric technique in quantitative assays. An extract containing anthraquinones such as alizarin acting as a
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complexing agent by reacting with aluminum and forming a reddish complex which could be measured at 499 nm (Tontrong et al., 2012). The Indian M. citrifolia leaf ethanol extract is reported for its larvicidal and pupicidal activities against the malarial vector Anopheles stephensi, or as a combination of M. citrifolia with Metarhizium anisopliae (an entomopathogenic fungi) (Kovendana et al., 2014). The mosquitocidal activity of Indian M. citrifolia was successfully proved at various concentrations range (100500 ppm) on the developing phases of malarial vector, A. stephensi, Dengue vector, Aedes aegypti and Filarial vector culex quinquefasciatus, showing that methanol extract had the highest larval and pupal mortality rate (Kovendan et al., 2012).
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Ca´rdenas-Coronel, W.G., Carrillo-Lo´pez, A., Rocha, R.V., Labavitch, J.M., Ba´ez-San˜udo, M., Heredia, J.B., et al., 2015. Biochemistry and cell wall changes associated to Noni (Morinda citrifolia L.) fruit ripening. J. Agric. Food. Chem. Available from: http://dx.doi.org/10.1021/acs. jafc.5b03681. Cardon, D., 2003. Le Monde des Teintures Naturelles. Belin, Paris. Chan-Blanco, Y., Vaillant, F., Perez, A.M., Reynes, M., Brillouet, J.M., Brat, P., 2006. The noni fruit (Morinda citrifolia L.): a review of agricultural research, nutritional and therapeutic properties. J. Food Compos. Anal. 19, 645654. Chunhieng M.T., 2003. Developpement de nouveaux aliments sante´ tropicale: application a la moix du Bre´sil Bertholettia excelsa et au fruit de Cambodge Morinda citrifolia. Ph.D thesis, INOL, France. Da Silva, A.M., de Souza, A.M., de Paula, F.M., Diniz, A.P., Zan, R.A., Ramos, L.J., et al., 2012. Analysis physical-chemical, mutagenic and antimutagenic of Morinda citrifolia L. 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Pidada—Sonneratia caseolaris Azlen Che Rahim and Mohd Fadzelly Abu Bakar Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Antioxidant Properties
327 327 328 328 329
Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Application Acknowledgment References
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CULTIVAR ORIGIN AND BOTANICAL ASPECTS Sonneratia caseolaris is found from the west coast of India to southern China through to the western islands of the Pacific Ocean. This species is widespread and can be found in Bangladesh, Brunei Darussalam, Cambodia, China, India, Indonesia, Malaysia, Myammar, the Philippines, Thailand, northeast Australia, and Papua New Guinea (Howlader et al., 2012). S. caseolaris is known as mangrove apple or crabapple mangrove. In Malaysia, S. caseolaris (L) Engler or “Pidada” is a common name used by Sabahan, Malaysian Borneo while “berembang”, and “perepat” is used in peninsular Malaysia. Watson (1928) classified the mangroves in peninsular Malaysia into five regions: Avicennia-sonneratia type, Bruguiera cylindrical type, Bruguiera parviflora type, Rhizophora type and Bruguiera gymnorhiza type (Latiff, 2012). Sonneratia caseolaris is derived from family Lythraceae and is one of the native mangrove plants that can grow in the mangrove forests on deep muddy soil and tidal areas with mud banks. In some instances, this tree has also been found growing in fresh water. S. caseolaris can grow up to 20 m tall with a diameter about 50 cm and able to adapt with a salty harsh environment. The unique rooting system, and salt excluders, are in the form of the adaptations to the mangrove area environment. For example, the branches, and cone-shaped pneumatophores are formed in order to support the breathing system (Giesen et al., 2006). The flower of S. caseolaris can grow up to 10 cm in diameter with narrow petals and dark red coloring. The flower is nocturnal, opening late in the evening and lasts for one night only. In addition, according to Giesen et al. (2006) this flower contain edible nectars that attract bats and moths. The total weight of the fruits of S. caseolaris is about 92% consisting of heavy seeds inside it. It has a star shaped stem cap with six edges on the top as the cap of the fruit. The diameter of the fruit can be between 12cm and 20 cm. The fruit of S. caseolaris are shown in Fig. 1.
HARVEST ANNUAL PRODUCTION S. caseolaris is an evergreen, medium to tall tree which can grow up to 10 m in height (Naskar, 2004). The reproductive cycle of the plant takes about 45 months. Flowering season occurrs during the dry period meanwhile fruit fall occurs during the short rainy season. It is estimated that each mangrove tree can produce up to 2 kg of fruits per day (Jariyah et al., 2014). However, this tree has not been planted commercially for fruits. The tree naturally grow in the wild. In Malaysia, during harvesting season, only trees that only meets the maturity criteria is allowed to be cut down with a logging permit issued by the relevant state Forestry Department (The Star, 2009). This is to ensure the sustainability of the forest and conservation of mangrove swamps. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00043-5 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Fruit of Sonneratia caseolaris (A) Fruits on a tree; (B) Whole fruit. FIGURE 2 Cross section of S. caseolaris fruit.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Fruit development is largely dictated by the seed development. The fruit of S. caseolaris is round, made up of a pompom of white stamens in a cup shaped calyx. These turn into globular fruits which are seated on a star-like calyx with the seeds embedded in the fleshy pulp. The fruit is noted for its outward similarity to the persimmon fruit, but is green in color. Fig. 2 shows the cross section of S. caseolaris fruit with a large number of small seeds. The fruits are also able to float in water. An important characteristic of mangrove fruits is the adaptation of seed survival in the harsh environment of mangrove forest. As saline water and soil is not a conducive environment for seeds to germinate, a vivipary propagation has been adopted by the seed (Tomlinson, 1986; Rabinowitz, 1978). Not only that, hydrochory is another way by which mangrove species spread seeds fruits and propagules. The unique viviparous mode enables the embryo to germinate while they are still attached to the parent tree. At the moment of reaching their maturity, about 46 months, the seedlings or “propagules” fall into the water and are dispersed by the tides.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE The phytochemical constituents of S. caseolaris in selected areas have been investigated in detail. A recent study by Simlai et al. (2014) reported that the methanolic extract of stem bark of this species is a good source of phenolics, flavonoids, tannins, alkaloid, and saponins. The phytochemical analysis of stem bark of S. caseolaris are presented in Table 1. Many of the reported composition indicates that species of S. caseolaris may have significant biological activities due to the recognized potent antioxidants.
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TABLE 1 Quantitative Estimation of Phytochemicals From Sonneratia caseolaris Stem Bark Extract Phytochemical
Concentration (μg/g dry weight)
Total phenolics
50.70 6 0.74 mg GAE/g dry weight
Total flavonoids
90.04 6 3.57 mg QE/g dry weight
Total tannin
48.04 6 0.91 mg TAE/g dry weight
Total alkaloid
56.96 6 2.66 mg/g dry weight
Total saponin
8.00 6 1.41 mg/g dry weight
Data are presented as mean 6 standard deviation from three replicates (n 5 3). Source: Adapted from Simlai, A., Rai, A., Mishra, S., Mukherjee, K., Roy, A., 2014. Antimicrobial and antioxidative activities in the bark extracts of Sonneratia caseolaris, A Mangrove plant. EXCLI J. 13, 9971010.
Despite only a few studies regarding their phytochemicals and pharmacology contribution, the outcome of isolation of this plant on different parts yielded identification of major compounds. In the screening of the phytochemicals in the leaves of the plant, both ethanolic and acetone extracts showed the presence of alkaloids, carbohydrates, flavonoids, and cardiac glycosides. Meanwhile, saponin and phenolic compounds are present in ethanol and sterols are found to be active in acetone extract (Varghese et al., 2010). As for the nutritional values for the mangrove species, a study by Patil and Chavan (2013) reported that fruits of S. caseolaris contains about 15.95% carbohydrate, moisture 77.10%, fat 0.86%, ash 3.85%, and protein 2.24%.
Antioxidant Properties The secondary metabolites of plant are closely related to the antioxidant properties. The recent study by Sadhu et al. (2006) reported that the isolation of alcoholic extract of S. caseolaris yielded flavonoid compounds such as flavone and 7-O-β-glucoside (cynaroside) that displayed superior scavenging activities. The fruits of S. caseolaries also have been claimed to possess antidiabetic activity (Rahmatullah et al., 2012). The antioxidant properties of this plant can be explained by the presence of the various phenolic phytochemicals, used as a traditional folk remedy. The above finding is similar to the study by Sadhu et al. (2006) who reported the antioxidant activity of active compounds of two flavonoids, luteolin and luteolin 7-O-β-glucoside, from S. caseolaris extract. The above findings are also similar to the study by Tiwari et al. (2010) who found that luteolin is one of the bioactive compounds that are responsible for intestinal α-glucoside inhibitory action. Quantitative analysis of antioxidant and anticholinesterase activity of phenolic compounds extracted from various part of S. caseolaris were undertaken by Wetwitayaklung et al. (2013). The result (Table 2) showed that methanol seed extract of the S. caseolaris tree displayed low IC50 value which represent the best AChE inhibition as its value is the closest to luteolin. Meanwhile, the extract also present the noncompetitive inhibition effect which suggests that the action of the methanol seed extract are the same as tacrine.
SENSORY CHARACTERISTICS Despite the availability of S. caseolaris, the information and exposure of this mangrove species especially in other parts of the world is limited. Thus, this has hindered the potential to be commercialized and the functionality of the fruit. S. caseolaris is one of the mangrove species that produce edible fruits among the nine most popular species in East Java Province of Indonesia which included Sonneratia, Ceriops, Bruguiera, Avicennia, Xylocarpus, Aegiceras, Lumnitcera, Waru and Bariringtonia asiatica (Noor et al., 2006; Jariyah et al., 2014). Among the species, S. caseolaries fruits have been reported to be nontoxic (Chen et al. ,2009), soft in texture, and producing specific flavors (Jariyah et al., 2014). Additionally, local persons used to utilize the unripe fruits of S. caseolaris as a flavor cooking due to it sour taste or being eaten raw as well. The ripe fruit it has a “cheese-like taste” and is usually eaten raw. Because it has a sour taste, the ripe fruit can be added to the steamed fish to give a sour taste to the dish. The fruits of S. caseolaris appear to be globular in shape and produce abundant seeds per fruit. The flower of S. caseolaris are also eaten as a vegetable with nampriks (spicy dish) (Wetwitayaklung et al., 2013).
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TABLE 2 IC50 Value of Anticholinesterase Activity of Substances and Methanol Extract (Maceration) Type of extract and substance
IC50 (μg/mL)
Tacrine
0.01
Luteolin
9.31
Luteoline glycoside
5.87
Stamen Calyx of flower Meat of fruit Persistent calyxs of fruit Seeds
55.58 140.12 84.74 642.10 10.52
Pneumatophores
126.15
Leaf
146.66
IC50 stands for 50% inhibitory concentration. Source: Adapted from Wetwitayaklung, P., Limmatvapirat, C., and Phaechamud, T., 2013. Antioxidant and anticholinesterase activities in various parts of Sonneratia caseolaris (L). Indian. J. Pharm. Sci. 75(6): 649656.
HARVEST AND POSTHARVEST CONSERVATION The increasing in human population is putting increased pressure on the mangrove species. This is due to the growing demand for timber, fuelwood, nonwood forest products and other building materials for local construction (Latiff, 2012). Thus, to ensure the conservation of the mangroves for environmental benefits, proper management of mangrove ecosystem is needed as well as the awareness of the public towards the protective effort of the tropical mangrove ecosystem. According to Kumar (2000), good management of a mangrove swamp can become a new avenue for selfemployment opportunities such as ecotourism, fishing, beekeeping, and cottage industries such as the production of mangrove based products, which also directly impacts on local community socioeconomics. Not only that, conservation of the mangrove swamp is also known to give protection to the coast by absorbing the energy of storm-driven waves and wind (Miles et al., 1998). According to the statistics from the Forestry Department in 2008, there was a decline of about 1497 ha of mangroves species from 2002 to 2003 (The Star, 2009). Thus, in realizing the importance of the preserving the mangrove swamp forests, the government has taken actions together with the various agencies to replant the mangroves. The replanting of the mangroves species is one of the efforts to restore the biodiversity of the forest in order to provide a balance life cycle in the mangrove swamp. The species of S. caseolaris is listed as least concern category as by the IUCN Red List of Threatened Species (2006). Fig. 3 shows the tree of S. caseolaris which need to be protected to maintain the ecosystem diversity.
INDUSTRIAL APPLICATION OR POTENTIAL APPLICATION Mangrove plants have long been consumed by the society especially those who are living in coastal area in Indonesia, either as food materials or food products (Jariyah et al., 2014). There are a number of products derived from this species. Among others species of mangrove fruits, S. caseolaris is the popular one to be processed as food products including syrups (Abeywickrama and Jayasooriya, 2010), cakes, and pudding (Brown et al., 2006). Meanwhile, according to Kathiresan et al. (2010), S. caseolaris fruits are used as beverages and pickled (mainly in Sri Lanka and Indonesia). In addition to that, a study by Jariyah et al., (2014) investigated mangrove fruits of S. caseolaris and discovered they are rich in mineral sources. The authors also suggested that mangrove fruit flour can be used as food product which supplies a good source of dietary fiber. The other uses of S. caseolaris is the pneumatophores are commercialized as corks and floats for fishing nets. Because the pneumatophores are able to float on water, they are often used to build boats. Other than the pneumatophores, the pulp can also be used for craft paper production. The tree is also valued for its timber which is used for
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FIGURE 3 The habitat of Sonneratia caseolaris.
various construction application and also as fuel (Wetwitayaklung et al., 2013). Not only that, the tree is very important among the coastal swamp community as it provide a tolerable habitat for wildlife and helps to protect the soil from erosion. The mangrove species also have been exploited to serve the local communities by supplying the basic needs of life.
ACKNOWLEDGMENT We would like to thank the editorial board for giving us opportunity to contribute chapters in this book. We also want to thank for those who undertook the research and provided us the data from previous years.
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Kumar, R., 2000. Conservation and management of mangroves in India, with special reference to the state of Goa and the Middle Andaman Islands. Int. J. For. Forest Ind. 51 (203). Latiff, A., 2012. Conservation strategies for endangered mangrove swamp forests in Malaysia. Pak. J. Bot. 44, 2736. Miles, D.H., Kokpol, U., Chittawong, V., Tip-Pyang, S., Tunsuwan, K., Nguyen, C., 1998. Mangrove forests - the importance of conservation as a bioresource for ecosystem diversity and utilization as a source of chemical constituents with potential medicinal and agricultural value. Pure. Appl. Chem. 70 (11). Naskar, K., 2004. Indian Sundarbans. In: Naskar, K. (Ed.), Manual of Indian Mangroves. Daya Publishing House, Delhi, pp. 2937. Noor, Y.R., Khazali, M., Suryadiputra, I.N.N., 2006. Guide of Introduction Mangroves in Indonesia. PHKA/WI-IP, Bogor, pp. 74130. Patil, P.D., Chavan, N.S., 2013. A need conservation of mangrove genus Bruguiera as a famine food. Annals Food Sci. Technol. 14 (2), 294297. Rabinowitz, D., 1978. Dispersal properties of mangrove propagules. Biotropica. 10, 4757. Rahmatullah, M., Azam, M.N.K., Pramanik, S., Sania, Rahman, S., Jahan, R., 2012. Inter. J. Pharm. Technol. Res. 4 (1), 125129. Sadhu, S.K., Ahmed, F., Ohtsuki, T., Ishibashi, M., 2006. Flavonoids from Sonneratia caseolaris. J. Nat. Med. 60, 264265. Simlai, A., Rai, A., Mishra, S., Mukherjee, K., Roy, A., 2014. Antimicrobial and antioxidative activities in the bark extracts of Sonneratia caseolaris, A Mangrove plant. EXCLI J. 13, 9971010. The Star, 2009. Saving the mangroves. Environmental Development in Malaysia. ,https://envdevmalaysia.wordpress.com/2009/10/05/saving-themangroves/. (accessed 25.01.17.). Tomlinson, P.B., 1986. The Botany of Mangroves. Cambridge University Press, Cambridge. Tiwari, A.K., Viswanadh, V., Gowri, P.M., Ali, A.Z., Radhakrishnan, S.V.S., Agawane, S.B., et al., 2010. Oleanolic acid- an α- Glucoside inhibitory and antihyperglycemic active compound from the fruits of Sonneratia caseolaris. Journal of Medicinal and Aromatic Plants. 1 (1), 1923. Varghese, K.J., Belzik, N., Nisha, A.R., Resiya, S., Resmi, S., Silvipriya, K.S., 2010. J. Pharm. Res. 3 (11), 26252627. Watson, J.G., 1928. Mangrove forests of the Malay Peninsula Malayan Forest Records, No 6: pp. 275. Wetwitayaklung, P., Limmatvapirat, C., Phaechamud, T., 2013. Antioxidant and anticholinesterase activities in various parts of Sonneratia caseolaris (L). Indian. J. Pharm. Sci. 75 (6), 649656.
Pitanga—Eugenia uniflora L. Rodrigo C. Franzon1, Silvia Carpenedo1, Maximiliano D. Vin˜oly2 and Maria do C.B. Raseira1 1
Embrapa Temperate Agriculture, Pelotas, Rio Grande do Sul, Brazil, 2Federal University of Pelotas, Pelotas, Rio Grande do Sul, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Chemical Composition and Nutritional Value Sensory Characteristics
333 334 335 336
Harvest and Postharvest Conservation Industrial Potential References
337 337 337
CULTIVAR ORIGIN AND BOTANICAL ASPECTS The pitanga (Eugenia uniflora L.) belongs to the Myrtaceae family, and is native to an area extended from central Brazil through to the north of Argentina. The biodiversity centers within Brazil are located on the northeast/Caatinga, south/southern, central Brazil/Cerrado and Atlantic rainforest. However, due its the easy adaptation, the species is found over almost the entire Brazilian territory, as well various parts of the world. In wild form it usually grows along the banks of streams and on the edge of the forest, but it is also commonly cultivated throughout many areas of Brazil, mainly in the northeast region (Lorenzi et al., 2006). Their common name, pitanga, is from the Tupy indigenous language, “pi’ta˜g”, meaning red, in reference to the fruit color that is most commonly found (Donadio et al., 2002; Lira Ju´nior et al., 2007), although there is variability in skin color, ranging from orange (Fig. 1), red (Fig. 2) to dark purple (Fig. 3). Various botanical names are synonyms of E. uniflora, being the most commonly found Stenocalyx uniflorus (L.) Kausel and E. micheli (Lam.) (Lorenzi et al., 2006; Sobral et al., 2015). In Brazil, Uruguay and parts of Argentina, this species is popularly known as pitangueira, or simply pitanga. On the northeast of Argentina, and possibly in other countries of Spanish language in Latin America, such as Paraguay and ˜ angapirı´ (Tupi-Guarani origin), arraya´n, Capulı´ o Cereza de Cayena. The worldwide Bolivia, this species is known as N literature usually refers to E. uniflora as Surinam cherry or Cayenne cherry, usually in the USA, Spain, and France, possibly wrongly considered as a native bush of Suriname. There are other names; in India, it is known as the Brazil cherry and in Sri Lanka, as the goraka cherry (Ctenas et al., 2000). The basic chromosome number of the species is n 5 11, being a diploid species (2n 5 22). The pitanga occurs predominantly in the Atlantic rainforest as a tree that reaches between 45 m high, sometimes reaching 812 m (Sanchotene, 1989; Lorenzi, 2014), or existing as a bush 0.7 m high in Restinga areas (Salgueiro et al., 2004). The pitanga have a deep root system, formed by a taproot. The stems have light gray spots, and a diameter of up to 40 cm. The canopy has rounded shape, with a projection diameter ranging from 3 to 5 m when in isolated cultivation (Fig. 4) (Sanchotene, 1989; Lorenzi, 2014). Leaves are alternate, simple, elliptic to ovate, margins entire, shortly accuminated to obtuse apex, leaf bases are obtuse to slightly cordate sometimes attenuated or acute, with dimensions ranging from 2.57 cm length and 1.23 cm wide, with a dark green color, glossy, and membranous consistency (Sanchotene, 1989; Lira Ju´nior et al., 2007; Lorenzi, 2014). The flowers are typical of the Myrtaceae family, being white, bisexual, and appear solitary or in clusters at the leaf axils, with petioles ranging from 1 to 3 cm in length. They are mildly fragrant and honey (meliferas), but produce little nectar (Lira Ju´nior et al., 2007). The sepals are oblong, with 34 mm length. The petals, in groups of four, are free, Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00044-7 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Orange pitanga fruits. Photo by Rodrigo Cezar Franzon.
FIGURE 2 Red pitanga fruits. Photo by Rodrigo Cezar Franzon.
puberulent, and white. The style is filiform, approximately 6 mm in length, and stigma is capitated (Sanchotene, 1989). Stamen numbers can reach 50, with yellow small anthers with longitudinal dehiscence. The ovary is inferior, bilocular and the ovules number is greater than 30 (Franzon, 2004). The fruits are globular, crowned by persistent calyx, with flattened poles and seven to eight ribs in the longitudinal direction (Sanchotene, 1989), although there is variability and fruits having from 7 to 10 ribs can be found. When the ripening process begins, the epicarp goes from green to an orange or light red color, until the final coloration, which can be red, orange or dark purple, almost black. There is color variability, both in the skin and flesh. The flavor usually is sweet and acidic, with variations ranging from fruit with low acidity to fruit with high acidity and some astringency, intense and characteristic aroma. Typically, the fruit presents one or two seeds, occasionally three or four and rarely more than that.
HARVEST SEASON In southern Brazil, the flowering time of E. uniflora is between September and October, and the fruit ripens between October and November. However, plants selected by Embrapa Clima Temperado, Pelotas, RS, have a second flowering
Pitanga—Eugenia uniflora L.
335
FIGURE 3 Dark purple pitanga fruits. Photo by Rodrigo Cezar Franzon.
FIGURE 4 Flowering pitanga tree at Embrapa Temperate Agriculture, Pelotas, RS, Brazil, in August 2015. Photo by Rodrigo Cezar Franzon.
cycle, which takes place between February and March and the fruit ripening between April and early May. This is the main fruiting period for these plants.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE The pitanga is well known by the Brazilian population, and has long been used in folk medicine for different purposes. The leaves have been used as an antihypertensive and diuretic (Consolini and Sarubbio, 2001), an astringent, in the treatment of digestive disorders (Bandoni et al., 1972), antipyretic and antirheumatic (Alice et al., 1991) and as an antimicrobial (Souza et al., 2004). More recently, it was found that the extract of E. uniflora leaves has potential inhibitory effects on production of hepatic stellate cells (Denardin et al., 2014). The chemical fruit composition is highly variable and dependent on other factors such as climate and soil condition, management, plant nutrition, fruit ripening stage, and variety, among others. Its composition (average 77% pulp and
336
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TABLE 1 Pitanga composition per 100 g of edible part (UNICAMP, 2011) Composition
Fresh fruit
Frozen pulp
Moisture (%)
88.3
94.6
Calories (Kcal)
41
19
Protein (g)
0.9
0.3
Fat (g)
0.2
0.1
Carbohydrate (g)
10.2
4.8
Fiber (g)
3.2
0.7
Ashes (g)
0.4
0.3
Ca (mg)
18
8
Mg (mg)
12
6
23% seed) is rich in calcium, phosphorus, anthocyanin and flavonoids, carotenoids and vitamin C, indicating its high antioxidant property. The vitamin C content of the pitanga fresh fruit is 24.9 mg/100 g pulp (Universidade de Campinas, UNICAMP, 2011), which is greater than the value found in passionfruit. The pitanga fruit composition is described in Table 1, according to UNICAMP (2011). The pitanga fruits are also rich in carotenoids and the presence of these compounds varies, both in terms of quantity and the type, among the production regions. In hot climates, the pitanga fruit presented higher carotenoids content than those found in fruits produced under mild climate, and presented higher carotenoid content when compared to fruits harvested in cold weather locations (Bagetti et al., 2011; Porcu and Rodriguez-Amaya, 2008). In fruits produced in Sa˜o Paulo, Pernambuco, Parana´ (Cavalcante et al., 2008) and Rio Grande do Sul, the major carotenoids were lycopene, β-cryptoxanthin and β-carotene (Bagetti et al., 2011) however, depending on the origin of the fruit, this composition may be different. The levels of total carotenoid are variable, and are more abundant in red pitanga fruit, followed by purple and orange color fruits, with average content of 153.0, 90.6, and 60.7 μg β-carotene/g of fruit, respectively (Jacques et al., 2009). In addition to carotenoids, antioxidants such as phenolic compounds and anthocyanins are also found. Among the phenolic compounds with antioxidant properties, are the flavonoids that, chemically, include anthocyanin and flavonols (Jacques et al., 2009), which are more concentrated in the skin than in the flesh, and in greater quantity in ripe fruit (Lima et al., 2002). Purple pitangas have a higher concentration of total phenolic than red pitangas due to the presence of higher content of anthocyanin (Lima et al., 2002; Jacques et al., 2009). Bagetti et al. (2011) found higher values for antioxidant activity (DPPH) for the purple fruits (3.1 mmol trolox/100 g fresh pulp) compared to those found in fruits with orange pulp (1.4 mmol trolox/100 g fresh pulp). Similarly, phenolic compounds content found in black fruits was higher than red and orange pitangas, with values ranging from 179 to 799.8 mg GAE/100 g fresh weight (Lima et al., 2002; Jacques et al., 2009; Bagetti et al., 2011; Denardin et al., 2015). The amount of anthocyanins found in fruits of black pitanga (136 mg/100 g) and red (69 mg/ 100 g) (Bagetti et al., 2011) are higher than those found in grape frozen (Vitis vinifera) (30.9 mg/100 g), strawberry (Fragaria vesca) (23.7 mg/100 g) and ac¸aı´ berrie (Euterpe oleracea) (22.8 mg/100 g) (Kuskoski et al., 2006).
SENSORY CHARACTERISTICS The pitanga has the appearance of a small pumpkin, with a green color when immature and, when ripened, it may have an orange, red to dark purple color (Lederman et al., 1992; Lima et al., 2002; Griffis et al., 2013). It is a nonclimacteric fruit, which needs to be harvested ripe for best flavor and appearance. Unripened fruits do not have a good flavor (Griffis et al., 2013). The flavor of ripened fruits is very particular, and hard to compare with other known fruits (Griffis et al., 2012), and this flavor can be very distinct between different plants of the same population.
Pitanga—Eugenia uniflora L.
337
Due to the perishability, pitanga fruits are rarely found in the market as a fresh fruit, being more common in processed form, such as juices, frozen pulp, and jellies. The storage as a frozen pulp retains the characteristics of flavor, color, and aroma for up to 60 days. After this period, it was found that there is a decreasing acceptance of a frozen pitanga pulp based nectar (Lopes et al., 2005). Sensory analyzes of the pitanga-based products such asnectar, juice and soft drink showed a good acceptance (Silva et al., 2014).
HARVEST AND POSTHARVEST CONSERVATION Several biochemical changes occur during the fruit ripening, such as soluble solids increasing and acidity decreasing. So harvesting E. uniflora in an inappropriate stage can accelerate the deterioration process, causing significant postharvest losses. The fruit ripening physiology is still unknown, and it is necessary to establish appropriate parameters to set the harvesting time and methods to prolong the postharvest period (Vizzotto et al., 2011). Besides being a nonclimacteric fruit, the pitanga is highly perishable due to its high metabolism during ripening. Therefore, improper handling at harvest and postharvest can accelerate the process of maturation and senescence, influencing negatively the quality of the fruit and limiting the marketing period (Vizzotto et al., 2011). The harvesting at the proper ripening stage determines the final product quality. Fruits harvested before ideal maturation stage have low quality, higher water loss, and are more susceptible to physiological disorders (Vizzotto et al., 2011), have low levels of soluble solids and higher acidity. Fruits harvested at an advanced ripening stage have a more limited shelf life, reducing the marketing period, which is already quite short.
INDUSTRIAL POTENTIAL The potential uses of pitanga abound. In addition to the fresh market, fruits can be used for industrialization as frozen pulp, juices, nectars, icecream, and jellies. The pitanga juice is very popular in northeastern Brazil, being served in juice houses, restaurants, and coffee shops. Liqueurs are prepared with the fruit in some regions, and also teas, syrups, and fermented beverages are used by Brazilians as medicine. This species is also used by the cosmetic industry for the manufacture of shampoos, hair conditioners, facial and bath creams and perfumes (Vizzotto et al., 2011). In addition to the processing possibilities, therapeutic properties of the pitanga leaves are known and referenced by popular knowledge and in literature for treatment of various diseases, including fever, stomach disorders, and hypertension (Schmeda-Hirschmann et al., 1987; Weyerstahl et al., 1988), rheumatism (Alice et al., 1991), bronchitis (Rivera and Obon, 1995), diabetes and obesity (Arai et al., 1999). There are also reports of cardiovascular activity (Lee et al., 2000), antiinflammatory activity (Schapoval et al., 1994), and diuretics (Consolini et al., 1999). Recent studies have proved the antioxidant activity, which inhibits lipid peroxidation and promotes the removal of free radicals (Velazquez et al., 2003). The essential oil of pitanga leaves has antioxidant activity (Marin et al., 2008), exhibits strong antibacterial effects against Staphylococcus aureus and exhibited an excellent cytotoxic action against cell lines of human tumor PC-3 and Hep G2, and inhibited Hs 578T growth completely (Ogunwande et al., 2005). However, despite all the knowledge on possible uses of fruits, leaves, and wood of this species, its use is still very limited, leaving the commercial exploitation of its fruits restricted to northeast of Brazil, where they are used for pulp and juice production. With regard to the leaves, the essential oil is used in the manufacture of cosmetics. More recently, in southern Brazil, the pitanga has been used in very small amounts for the manufacture of nectars by some small business, and are generally sold only in the local market, mainly at fairs and exhibitions.
REFERENCES Alice, C.B., Vargas, V.M., Silva, G.A., Siqueira, N.C., Schapoval, E.E., Gleye, J., et al., 1991. Screening of plants used in south Brazilian folk medicine. J. Ethnopharmacol. 35, 165171. Arai, I., Amagaya, S., Komatsu, Y., Okada, M., Hayashi, T., Kasaic, M., et al., 1999. Improving effects of the extracts from Eugenia uniflora on hyperglycemia and hypertriglyceridemia in mice. J. Ethnopharmacol. 68, 307314. Bagetti, M., Facco, E.M.P., Piccolo, J., Hirsch, G.E., Rodriguez-Amaya, D., Kobori, C.N., et al., 2011. Physicochemical characterization and antioxidant capacity of pitanga fruits (Eugenia uniflora L.). Cieˆnc. Tecnol. Aliment. 31, 147154. Bandoni, A.L., Mendiondo, M.E., Rondina, R.V., Coussio, J.D., 1972. Survey of Argentine medicinal plants. I. Folklore and phytochemical screening. Lloydia. 35, 6980. Cavalcante, M.L., Rodriguez-Amaya, D.B., 2008. Carotenoid composition of the tropical fruits Eugenia uniflora and Malpighia glabra. In: Charalambous, G. (Ed.), Food Science and Human Nutrition. Elsevier Science Publishers, Amsterdam, pp. 643650.
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Consolini, A.E., Sarubbio, M.G., 2001. Pharmacological effects of Eugenia uniflora (Myrtaceae) aqueous crude extract on rat’s heart. J. Ethnopharmacol. 81, 5763. Consolini, A.E., Baldini, O.A.N., Amat, A.G., 1999. Pharmacological basis for the empirical use of Eugenia uniflora L. (Myrtaceae) as antihypertensive. J. Ethnopharmacol. 66, 3339. Ctenas, M.L.B., Ctenas, A.C., Quast, D., 2000. Frutas das Terras Brasileiras. C2 Editora e consultoria em nutric¸a˜o, Sa˜o Paulo. Denardin, C.C., Parisi, M.M., Martins, L.A.M., Terra, S.R., Borojevic, R., Vizzotto, M., et al., 2014. Antiproliferative and cytotoxic effects of purple pitanga (Eugenia uniflora L.) extract on activated hepatic stellate cells. Cell. Biochem. Funct. 32, 1623. Denardin, C.C., Hirsch, G.E., Rocha, R.F., Vizzotto, M., Henriques, A.T., Moreira, J.C.F., et al., 2015. Antioxidant capacity and bioactive compounds of four Brazilian native fruits. J. Food Drug Anal. 23, 387398. Donadio, L.C., Moˆro, F.V., Servidone, A.A., 2002. Frutas Brasileiras. Novos Talentos, Jaboticabal. Franzon, R.C., Caracterizac¸a˜o de mirta´ceas nativas do Sul do Brasil, 2004. 114f. Dissertac¸a˜o (Mestrado emAgronomia), Faculdade de Agronomia Eliseu Maciel, Universidade Federal de Pelotas, Pelotas. Griffis Jr., J.L., Sams, S.E., Manners, M.M., McDonald, T.G., Radovich, T.J., 2012. Purple-fruited pitanga - antioxidant levels and flavors of mature fruits vary considerably among closely related cultivars. Acta. Hortic. 959, 209215. Griffis Jr., J.L., Manners, M.M., Sams, S.E., McDonald, T.G., Radovich, T.J., 2013. Purple-fruited Pitanga (Eugenia uniflora) crop development and commercialization. Proc. Florida State Hortic. Soc. 126, 3034. Jacques, A.C., Pertuzatti, P.B., Barcia, M.T., Zambiazi, R.C., 2009. Bioactive compounds in small fruits cultivated in the southern region of Brazil. Braz. J. Food Technol. 12, 123127. Kuskoski, E.M., Asuero, A.G., Morales, M.T., Fett, R., 2006. Frutas tropicais silvestres e polpas de frutas congeladas: atividade antioxidante, polifeno´is e antocianinas. Cieˆnc. Rural 36, 12831287. Lee, M.H., Chiou, J.F., Yen, K.Y., Yang, L.L., 2000. EBV DNA polymerase inhibition of tannins from Eugenia uniflora. Cancer. Lett. 154, 131136. Lederman, I.E., Bezerra, J.E.F., Calado, G.A., 1992. Pitangueira em Pernambuco. Empresa Pernambucana de Pesquisa Agropecua´ria, Recife. Lima, V.L.A.G., Me´lo, E.A., Lima, D.E.S., 2002. Feno´licos e caroteno´ides totais em pitanga. Sci. Agric. 59, 447450. Lira Ju´nior, J.S., Bezerra, J.E.F., Lederman, I.E., Silva Ju´nior, J.F., 2007. Pitangueira. Empresa Pernambucana de Pesquisa Agropecua´ria, Recife. Lopes, A.S., Mattietto, R.A., Menezes, H.C., 2005. Estabilidade da polpa de pitanga sob congelamento. Cieˆnc. Tecnol. Aliment. 25, 553559. Lorenzi, H., 2014. sixth ed. A´rvores brasileiras: manual de identificac¸a˜o e cultivo de plantas arbo´reas nativas do Brasil, v. 1. Instituto Plantarum de Estudos da Flora, Sa˜o Paulo. Lorenzi, H., Bacher, L., Lacerda, M., Sartori, S., 2006. Frutas Brasileiras e Exo´ticas Cultivadas. Editora Plantarum, Sa˜o Paulo. Marin, R., Apel, M.A., Limberger, R.P., Raseira, M.C.B., Pereira, J.F.M., Zuanazzi, J.A., 2008. Volatile components and antioxidant activity from some Myrtaceous fruits cultivated in Southern Brazil. Latin Am. J. Pharmacy 27, 172177. Ogunwande, I.A., Olawore, N.O., Ekundayo, O., Walker, T.M., Schmidt, J.M., Setzer, W.N., 2005. Studies on the essential oils composition, antibacterial and cytotoxicity of Eugenia uniflora L. Int. J. Aromatherapy 15, 147152. Porcu, O.M., Rodriguez-Amaya, D.B., 2008. Variation in the carotenoid composition of the lycopene-rich Brazilian fruit Eugenia uniflora L. Plant Foods Hum. Nutr. 63, 195199. Rivera, D., Obon, C., 1995. The ethnopharmacology of Madeira and Porto Santo Island: a review. J. Ethnopharmacol. 46, 7393. Salgueiro, F., Felix, D., Caldas, J.F., Margis-Pinheiro, M., Margis, R., 2004. Even population differentiation for maternal and biparental gene markers in Eugenia uniflora, a widely distributed species from the Brazilian coastal Atlantic rain forest. Divers. Distrib. 10, 201210. Sanchotene, M.C.C., 1989. Frutı´feras nativas u´teis a` fauna na arborizac¸a˜o urbana. 2 ed Porto Alegre, Sagra. Schapoval, E.E.S., Silveira, S.M., Miranda, M.L., Alice, C.B., Henriques, A.T., 1994. Evaluation of some pharmacological activity of Eugenia uniflora leaves. J. Ethnopharmacol. 44, 137142. Schmeda-Hirschmann, G., Theoduloz, C., Franco, L., Ferro, E., Arias, A.R., 1987. Preliminary pharmacological studies on Eugenia uniflora leaves: xanthine oxidase inhibitory activity. Ethnopharmacology 21, 183186. Silva, A.B., Soares, D.J., Oliveira, L.S., Sacramento, C.K., Figueiredo, E.A.T., Sousa, P.H.M., et al., 2014. Evaluation of antioxidant properties and sensory profile of purple Brazilian cherry beverages. Aliment. Hum. 20, 7584. Sobral, M., Proenc¸a, C., Souza, M., Mazine, F., Lucas, E., 2015. Myrtaceae. Lista de Espe´cies da Flora do Brasil. Jardim Botaˆnico do Rio de Janeiro, Disponı´vel em: ,http://floradobrasil.jbrj.gov.br/jabot/florado-brasil/FB10560.. Acesso em: 12 Nov. 2015. Souza, G.C., Haas, A.P., Von Poser, G.L., Schapoval, E.E., Elisabetsky, E., 2004. Ethnopharmacological studies of antimicrobial remedies in the south of Brazil. J. Ethnopharmacol. 90, 135143. UNICAMP-Universidade de Campinas, 2011. Tabela Brasileira de composic¸a˜o dos alimentos. 4 ed. Campinas. Disponı´vel em: ,http://www.unicamp. br/nepa/taco/contar/taco_4_edicao_ampliada_e_rev-isada. Acesso em outubro de 2015. Velazquez, E., Toumier, H.A., Buschiazzo, P.M., Saavedra, G., Schinella, G.R., 2003. Antioxidant activity of Paraguayan plants extracts. Fitoterapia. 74, 9197. Vizzotto, M., Cabral, L., Lopes, A.S., 2011. Pitanga (Eugenia uniflora L.). In: Yahia, E.M. (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruits. Woodhead Publishing, Oxford, pp. 272286. Weyerstahl, P., Marschall-Weyerstahl, H., Christiansen, C., Oguntimein, B.O., Adeoye, A.O., 1988. Volatile constituents of Eugenia uniftora leaf oil. Planta Med. 54, 546549.
Pitaya—Hylocereus undatus (Haw) Edmundo M. Mercado-Silva Autonomous University of Queretaro, Santiago de Quere´taro, Mexico
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value: Vitamins, Mineral, Phenolics, and Antioxidant Compounds Sensory Characteristics
339 340 340 341 342 343
Harvest and Postharvest Conservation Packing Systems Alternative Treatments Pests and Diseases Quarantine Treatments Industrial Application or Potential Industrial Application References
343 344 344 345 345 345 346
CULTIVAR ORIGIN AND BOTANICAL ASPECTS Dragon fruit or pitahayas are native to southern Mexico and Central America. Due to their attractive color and flavor, the world production is increasing quickly and new fruit crops in arid areas are under development (Tel-Zur, 2004; Mizrahi, 2014, 2015). Today it is commercially cultivated in the Bahamas, Bermuda, Indonesia, Colombia, Israel, Philippines, Maymar, Malaysia, Mexico, Nicaragua, northern Australia, Okinawa (Japan), Sri Lanka, southern China, southern Florida, Taiwan, Thailand, Vietnam, and the West Indies. Le Bellec et al. (2011), Lim (2012), and OrtizHernandez and Carrillo-Salazar (2012) have reviewed their taxonomy, botany, nutritive and medicinal properties, geographical distribution, and industrial uses. This plant is one of the most widely distributed members of the cactaceae family, with three species in the genus Hylocereus (Hylocereus guatemalensis, Hylocereus polyrhizus, and Hylocereus undatus) and one species in the genus Selenicereus (S. megalanthus). Bauer (2003) revised its taxonomy and Selenicereus megalanthus species was placed in the Hylocereus genus and renamed to be H. megalanthus. Additionally, the Hylocereus polyrhizus species was renamed to Hylocereus monacanthus. The plant is a cacti climber. There are 18 species (Gunasena et al., 2007) within the groupings of H. undatus (red skin and white flesh fruit), H. monacanthus (red skin and red flesh) and Hylocereus megalanthus (yellow skin and white flesh). All produce aerial roots, which facilitate anchoring in trunks, and have large flowers and fruit. Several pitahaya blooms flows occur in the northern hemisphere from May to October and the daily floral opening time varies with the region; in Mexico, it starts at 18:40 and ends at 23:40 while in Israel occur between 16:00 and 18:30. Bloom is affected by the photosynthetic period, where the process requires 1013 h of light (Gunasena et al., 2007; Jiang et al., 2012). In Vietnam, during September to December, the floral bud formation is induced (Tran et al., 2015) by manipulating the light (4 h of additional light daily using incandescent bulbs of 100 W). This procedure allows the production of fruit in winter. However, in Israel the use of N-(2-chloro-4-pyridinyl)-N-phenylurea (CPPU) promoted precocious flowering in H. undatus, increasing total flower yield, whereas GA3 application delayed the flowering and decreased total flower yield (Khaimov and Mizrahi, 2006). CPPU can be used to obtain early fruit production, and giberellic acid or flower thinning to delay cropping. Khaimov et al. (2012) pointed out that the active forms of endogenous cytokines are involved in the flowering regulation. The high capacity for growth in different environments is associated to the dragon fruit’s high capacity to respond to different stresses (Nie et al., 2015; Qiong et al., 2015). The plant’s reproductive biology can involve self-compatible or self-incompatible pollination (Cohen et al., 2012), with added ability to performing crosses intra specific (inter-clonal Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00045-9 © 2018 Elsevier Inc. All rights reserved.
339
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TABLE 1 Producer Countries, Season Production and Species Produced of Hylocereus sp Country
Season production
Specie or variety
Australia
SeptemberMarch
Hylocereus undatus, Hylocereus monacanthus, Hylocereus megalanthus
Colombia
All year
Hylocereus megalanthus
Honduras
MayNovember
Different clones from Hylocereus monacanthus sp. Lisa orejona, cebra
Chile
DecemberJune
Hylocereus monacanthus and varieties
Florida USA
JuneNovember
Hylocereus undatus
Indonesia
All the year or NovOct
Hylocereus undatus
Israel
JulyMay
Hylocereus polyrhizus, Hylocereus monacanthus Ephephillum
Malaysia
NA
Hylocereus undatus
Me´xico
JuneNovember
Hylocereus undatus
Nicaragua
JuneNovember
Hylocerus costaricenses
Taiwan
MayDecember
Hylocerus monacanthus
Thailand
NA
Hylocereus undatus
Vietnam
Almost all year
Hylocereus undatus
Northern Vietnam
JulyOctober
Hylocereus monacanthus
hybrids), between species (interspecific hybrids) and even between different genera (inter-generic hybrids). This allows the development of hybrids of high productivity (Cisneros and Tel-Hur, 2010). Castillo-Martinez et al. (2005) studied the sexual compatibility of different genotypes of H. undatus in Me´xico. Some genotypes were self-compatible, and others were self-incompatible which had bigger fruits with better color and flavor. In all materials studied, the fruit production was less in relation to the total flowers developed, its main cause was sexual self-incompatibility (Cisneros and Tel-Hur, 2010). The plants with self-compatibility ensures fruit production whereas the plants that have self-incompatibility should be planted alternatively with self-compatibility clones to ensure the fruit production. Mizrahi (2015) highlighted the importance of breeding programs. His program has carried out crosses between clones of the same species, into different species as well as different genera (Tel-Zur et al., 2004). This allows fresh fruit production for most of the year. The problems with growing of these genotypes is the self-incompatibility (Nerd and Mizrahi 1997), therefore, some hybrids need cross-pollination and the grower has to grow at least two compatible clones.
HARVEST SEASON Table 1 shows the different countries producers of Hylocereus fruit, the season of production, and the species produced. Pitahaya is virtually unknown in most European countries. The main supplier of red pitahaya to Europe is Vietnam, but during the year it changes to supply from Israel and South America. Israel supplies the southern part of Europe and UK by sea, which has a lower cost than Vietnam supplying by air. Colombia and Ecuador supply H. megalanthus fruit.
ESTIMATED ANNUAL PRODUCTION Table 2 shows the actual and estimated production and yields per hectare in different countries in 2014. Vietnam is the largest producer, followed by China, Indonesia, Taiwan, Malaysia, and Nicaragua. The total production reached 1,000,000 ton, with Vietnam the principal producer and exporter. The main importer countries are USA 17%; Germany 14%; France 12%; The Netherlands 11%: Russia 10%; UK 9%; Canada 8%. The EU is main importer with 57%.
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TABLE 2 Producer Countries, Production Area and Yields of Hylocereus sp Production Country
Production ton
Yield ton/ha
Australia
NA
NA
China
200,000
14
Colombia
NA
NA
Honduras
NA
NA
Indonesian
36,000
2430
Israel
1000
Summer clones 3540 Winter clones 2530
Malaysiaa
8577
1930
Myanmar
2000
20
a
Me´xico
2496
46
Nicaragua
6160
69
Philippinesa
1574
6
Spain
NA
NA
Taiwan
27,654
2030
Thailand
NA
NA
Vietnam
602,680
4045
a
Estimate production, NA: not available.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The Cactaceae family has a crassulacean acid metabolism or CAM photosynthesis (Ortiz-Herna´ndez et al., 1999; Nobel and De la Barrera, 2004; Andrade et al., 2006; Ortiz-Herna´ndez and Carrillo-Salazar, 2012; Mizrahi, 2015) which allow them to have an efficient system to retain water, controlling the opening and closing stomata during the day. Tropical cacti such as the Hylocereus spp., use this pathway because they have a limited system of roots;their adventitious roots serve mainly to adhere to other plants or supports (epiphytes). For this reason, these plants also have to save water, reducing their day transpiration and capturing CO2 during the night. In addition, these plants live under low light levels due to foliage of other plants. When the environmental conditions do not satisfy the plant requirements, the flowering, fruiting and the fruit quality are altered. Raveh et al. (1995) demonstrated that the CO2 uptake in H. undatus was maximum under shade (10 mol m2/ day of photosynthetic photon flux, PPF). Andrade et al. (2006) indicated that H. undatus plants were photoinhibited when they were grown under direct solar radiation, but showed maximum photosynthetic activity and stem elongation with only 35%45% of PPF. Nobel and De la Barrera (2004) added that total daily net CO2 uptake is maximum at 30 C/ 20 C day/night; but becomes zero at 42 C/32 C, with stem damage at 45 C, or cell death at 1.5 C. The long water stress effects on pattern of CO2 exchange was studied by Ortiz-Herna´ndez et al. (1999); the well-watered plants increased the exchange from 3.9 to 4.7 mmol CO2/m2 per s, whereas these values decreased from 4.3 to 2.9 mmol CO2/m2 per s in plants with no watering. Nobel and De la Barrera (2002) showed similar results under short drought stress. The injection of 100 μM abscisic acid into the stems substantially reduced the gas exchange; and the net CO2 uptake rate was inhibited by 97% 2 days afterwards. The abscisic acid leads to stomatal closure altering the gas exchange. Using suppression subtractive hybridization and cDNA microarray analysis, Fan et al. (2014) described the gene expression to unravel the molecular basis underlying the high tolerance of pitahaya (H. undatus) to drought stress. Thirty six genes were mapped to 47 KEGG pathways, including carbohydrates, lipids, energy, nucleotides, and amino acid metabolism. During the fruit development, there are increases of weight, size and color as well as increases in the total solids soluble (SST), the SST/acidity ratio, total and reducing sugars and betalains content, whereas the titratable acidity and vitamin C decreased (Centurio´n-Yah et al., 2008; Phebe et al., 2009).
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TABLE 3 Nutritional Composition of the Flesh of Three Main Species of Pitahaya Fruit Constituent
Species Hylocereus megacanthus
Hylocereus undatus
Hylocereus megalanthus
Water (%)
83
89
85
Protein (g)
0.160.23
0.5
0.4
Fat (g)
0.210.61
0.1
0.1
Fiber (g)
0.70.9
0.3
0.5
Ash (g)
0.540.68
0.5
0.4
Calcium (mg)
6.38.8
6.0
10.0
Phosphorus (mg)
30.236.1
19.0
16.0
Iron (mg)
0.550.65
Carotene (mg)
0.0050.012
NR
0.4
NR
0.3
Thiamine (mg)
0.280.43
0
0
Riboflavin (mg)
0.280.45
0
0
Niacin (mg)
0.2970.430
Ascorbic acid (mg)
89
0.2 25
0.2 4
Data are expressed in 100 g of fresh pulp
Nerd et al. (1999) studied the fruit growth and ripening, and the effect of various storage temperatures on fruit quality, in H. undatus and H. monacanthus growing in Israel under greenhouse conditions. A sigmoidal pattern of fruit growth was detected with a strong decline in growth rate after the onset of peel color change. H. undatus showed the first color change in peel at 2425 days after anthesis while in H. monacanthus it was at 2627 days. The peel turned fully red 45 days after the first color change. There was a decrease in the proportion of peel concomitant with the increase in the pulp associated with the slow growth phase, as well an increase in the concentration of soluble solids and soluble sugars and a decrease in firmness and starch and mucilage contents. The surge in acidity prior to color change indicated the beginning of the ripening processes. For H. monacanthus, the increase in pulp pigment was concomitant with the development of peel color.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE: VITAMINS, MINERAL, PHENOLICS, AND ANTIOXIDANT COMPOUNDS The pulp represents 60%80% of the total weight of a mature fruit. The total soluble content is variable (1214 Brix) and low acidity (0.20.35 mg malic acid per 100 g of fresh weight). Table 3 summarizes the nutritious composition of the flesh in the principal commercial species. Dembitsky et al. (2011) researched the nutrition properties, active metabolites and their biological activity as well as the total phenolic content, flavonoids, phytosterols and antioxidant activity. Menezes-Cordeiro et al. (2015) pointed out its high fiber content as well as the significant contents of Ca (79 g/kg), K (1113 g/kg) and Fe (307360 mg/kg) in the pulp of H. monacanthus fruit. The betalains of H. monacanthus include 10 betacyanins; five were identified as bougainvillein-r-I, betanin, isobetanin, phyllocactin, and iso-phyllocactin, three were tentatively identified as (60 -O-3-hydroxy-3-methyl-glutaryl)-betanin, its C15-stereoisomer, and (60 -O-3-hydroxy-3-butyryl)-betanin, respectively (Stintzing et al., 2002). In addition, Wybraniec et al. (2007) showed the presence of apiofuranosyl betacyanins in fruit flesh and peel of Hylocereus spp. The pectin of flesh fruit is mainly composed of arabinose and galactose, while the hemicellulose fraction consists of glucose, xylose and galactose (Ramı´rez-Truque et al., 2011). The relative amounts of neutral sugars of these hemicelluloses can be used as a taxonomic tool to distinguish species. The viscous consistency of the flesh might not be
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343
attributed to pectin fractions, because of the limited content of uronic acid (32.3%). On the other hand, Muhammad et al. (2014) indicated that the pectin from Hylocereus polyrhizus peel is constituted of galacturonic acid (39.11%), with moderate concentrations of mannose, rhamnose, galactose, glucose and minor amounts of xylose and arabinose. This pectin has high degree of esterification (63.74%). The total phenolics content was higher (Kugler et al., 2007) in H. monacanthus (61 mg GAE/100 mL) than H. undatus (18) and H. megalanthus (23). Six different flavonoids were separated in different floral parts of H. undatus, and although these compounds were not identified, their content changed with the sample origin (Yi et al., 2012). The antioxidant capacity was higher in H. monacanthus (412 mmol/100 mL TE) than H. undatus (182) and H. megalanthus (202). Only the juice of H. monacanthus showed betacyanins (46 mg/100 mL) where the hylocerenin was the principal betacyanin. This study confirmed that H. monacanthus fruit contains significant amounts of betalains and it is an excellent source of dietary antioxidative phytochemicals. Moo-Huchin et al. (2014) confirmed these result for H. undatus from Mexico. The lipid composition of the seed oil from H. undatus and H. monacanthus showed high oil content (18.33%28.37%) and the three major fatty acids were palmitic, oleic, and linoleic (Lim et al., 2010). The total tocopherol contents in H. undatus and H. monacanthus were 36.70 and 43.50 mg/100 g, respectively. The phytosterol compounds identified were cholesterol, campesterol, stigmasterol, and β-sitosterol. Seven acids phenolic were identified as gallic, vanillic, syringic, protocatechuic, p-hydroxybenzoic, p-coumaric, and caffeic. In addition, Chemah et al. (2010) indicated that the oil seed of H. monacanthus has higher scavenging capacity (46.6%) and high reducing capacity (59.1 mg Trolox/100 g dry weight).
SENSORY CHARACTERISTICS The opportunities for growth in the international market of pitahaya are mainly due to sensory characteristics of the fruit. The high visual quality (given by the skin and flesh color) and its exquisite taste in addition to the nutraceutical properties determine the acceptance in distant markets. However, due to the wide availability of species and hybrids obtained by the breeding programs, it is necessary to conduct sensory evaluations that allow give accurate estimates of the sensory quality of those materials. One also needs to assess storage conditions. Obenland et al. (2016) evaluated six varieties of pitahaya with white, pink, and red flesh, at harvest and after two weeks of storage at 5 C or 10 C. There were substantial varietal differences in sensory and quality attributes, regardless of storage condition. The panelists’ perception of flavor quality was most closely linked with varietal differences in soluble solid content (SSC) and titratable acidity, although there were clear differences in aroma volatiles. There was no correlation between method of storage and panelists liking the color of the fruit skin. In addition, the panelists did not report any significant differences in overall liking, flavor, sweetness, tartness or texture. Storage at 10 C induced a wide variety of measureable changes in pitahaya quality parameters, but these changes did not altered the sensory fruit quality. The nonclimacteric behavior and the maturity stage at the harvest time are key factors to obtain high sensory quality after the storage and during postharvest management. The sensory quality and the flavor increases according to the ripeness (Centurio´n-Yah et al., 2008). The color change was inhibited and the ethanol and acetaldehyde production increased under storage at 4 C for 21 days (Corrales-Garcia and Canche-Canche, 2008) altering the fruit sensory quality.
HARVEST AND POSTHARVEST CONSERVATION The harvest time is a key factor to maintain the fruit quality during the postharvest period; the most common harvest indices are the days after flowering (minimum 2737 days) as well as the red color intensity of the skin (depending on the cultivar and production area). Up to now the epidermis color and fruit firmness are the only practical indexes to harvest fruit. Nerd et al. (1999) indicated that when the epidermis color is completely red; the fruit size and weight, pulp content, total soluble solids, betacyanin content and flavor rating are maximum; while the firmness, mucilage content, starch and total titratable acidity are minimum. The fruit quality indices include the skin color (red or yellow), absence of defects, fruit well shaped, firm, fleshy and green bracts, pulp red or white and a ratio TSS:acidity ratio minimum of 40. The physical, chemical, and biochemical changes of fruit harvested at different maturity stages has been studied by different authors (Nerd et al., 1999; Centurion-Yah et al., 2008; Osuna-Enciso et al., 2011). All studies confirm this nonclimacteric behavior and that its best quality is displayed when the fruit is harvested at full maturity stage. The betalain content in the skin and flesh are highest in full maturity also (Esquivel et al., 2007; Obenland et al., 2016).
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However, the firmness, titratable acidity, total soluble solids (TSS) and vitamin C decreased during storage. The respiration rate is higher in fruit that is completely mature than in early maturity stages. Cold storage maintains the quality of the fruit; however it is sensitive to chilling injuries Nerd et al. (1999) showed that the storage at 6 C is not recommended, because the fruit showed a rapid loss of firmness and a sharp decline in the malic acid content once the fruit was transferred to the environmental conditions. However, in the export markets, storage at 5 C is a common commercial practice. Meanwhile, Corrales-Garcı´a and Canche-Canche (2008) also indicated that the storage at 4 C or 8 C showed external damage, being more intense in fruits stored at 4 C. Fruits stored for 21 days at 4 C did not show color change and maintained a high hue value (37.6 degrees), indicating that the desirable external pinkish-red color development was inhibited. In addition, an increase in the respiration rate was also recorded (28%). They recommended that the hue value and the respiration rate could be used to evaluate the chilling injury in pitahaya fruits. The website of Postharvest Center at UC Davis CA (Freitas et al., 2011) indicates that the optimal temperature to store red pitahayas (H. undatus and H. monacanthus) is 10 C with 5 C for yellow pitayas (Selenicereus megalanthus). The storage of red pitahaya and white flesh at 7 C or 11 C for two weeks did not show chilling injury symptoms, but storage at 3 C for 3 weeks showed internal tissue translucence as a chilling injury symptom (Balois-Morales et al., 2013). Previous studies also showed that storage at 3 C for 21 days decreased the phenolic content and the polyphenol oxidase activity while the peroxidase activity and soluble protein increased (Balaois-Morales et al., 2007). These increases could be associated with the senescence process. As noted above, the correct harvest time is key to have a good quality fruit. The firmness reduction was higher in H. monacanthus fruit harvested 5 weeks after anthesis than fruit harvested after 4 or 3 weeks. In a similar way, the total SSCs were highest in fruit of 5 weeks conserved at 6 C (Punitha et al., 2010). Based on these results, they indicated that to keep the fruit at 6 C is a good storage condition, but is necessary to take into account the optimum harvest time or the maturity stage of the fruit.
Packing Systems For export market, the fruit is packed into cardboard boxes of 5 or 7 kg and the fruit size is determined by count per box (515). Fruit is packed in a single layer tray using a plastic insert. The counts will vary appropriately when using 5 kg produce boxes. Packing into polyethylene bags with 4 L/m2 per hof oxygen transmission rates extended the shelf life until 35 days at 10 C, in fruit harvested 30 days after flowering (To et al., 2002). The wilting of the fruit scales is one of the most important changes that occur during the postharvest period; due to the bracts that contain active stomata that follow the rhythm of stomatal opening of stems (Mizrahi, 2015). The fruit stomata density changes according to species and the fruit surface. H. undatus has a higher density of stomata, and these are found in greater amounts on fruit bracts. Indeed the wilting occurs more rapidly in H. undatus fruit than other species (Mizrahi, 2015). Covering the fruit with IP9 plastic sheets (StePac, Tefen Israel) increased the shelf life. Also, the use of perforated bags of low-density polyethylene maintain the fruit quality, its firmness and titratable acidity while, the decay incidence and weight loss are low for H. undatus fruit, stored 20 days at 5, 7, and 10 C (Freitas and Mitcham, 2013). No matter what type of bags were used, the best temperature observed was 5 C. However, the samples stored at 5 C showed pulp translucency, while the fruit stored at 10 C did not show this change. The use of ethanolic extract of natural glue produced by honeybees, or propolis, at 0.5% delayed the weight loss and maintain the firmness fruit as well the titratable acidity (Zahid et al., 2013). This treatment can be used to extend the storage life without any negative effects on the quality.
Alternative Treatments Independent of its nonclimacteric pattern, Hylocereus spp. may respond favorably to 1-MCP applications. The use of this compound (200 μg/L) maintained the mechanical properties of the slices fruit of Hylocereus megalantus destined for minimal processing (Serna-Cock et al., 2012). The treatment with 600 mg/L for 24 h, significantly decreased the firmness loss, total soluble solids, the weight loss and the respiratory rate in whole fruit from Hylocereus megalanthus (Deaquiz et al., 2014). In a similar way, Li et al. (2016) found that exposure of red pitahaya cv ‘Bilu’ at 1 μL/L of 1-MCP for 24 h at 15 C delayed the bracts senescence as well as its color change after 16 days at 10 C plus 5 days at 20 C. These results indicate that the commercial application of 1-MCP can be used to maintain the fruit quality.
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345
Pests and Diseases Anthracnose is widely distributed in different countries with different species such as Colletotrichum gloesporioides Penz or C. truncatum (Guo et al., 2014). This fungal disease affects fruits and stems. However, a new pathogen has been isolated and identified as Botryosphaeria dothidea in Me´xico (Valencia-Botı´n et al., 2013) which has been previously reported to cause panicle and shoot blight and canker diseases in pistachio, peach, and apple. Bipolaris cactivora (Petrak) responsible for early brown rot was described on fruit in a Japanese market (Taba et al., 2007). Neoscytalidium dimidiatum was responsible for fruit internal brown rot and found on white-fleshed pitahaya (H. undatus) in China (Yi et al., 2015). The use of chitosan dispersions at submicron size of 1.0% with 600 nm droplet size, has potential as antifungal agent; the dispersion delayed the onset of anthracnose disease and maintained the fruit quality up to 28 days at 10 C 6 2 C (Ali et al., 2013). The effects of these coatings were also investigated in field applications by Ali et al. (2014), observing that the lignin contents in cell walls as well as the β-1,3-glucanase and chitinase activities increased 2, 10, and 11 folds respectively. These responses may improve the resistance against the anthracnose and be used as a plant growth enhancer.
Quarantine Treatments Dragon fruit is a host for tephritid fruit flies, therefore is subject to quarantine restrictions. Different countries have different quarantine requirements. Australia prohibits the entry of Hylocereus fruit in its territory, while Singapore and Hong Kong ask for a phytosanitary certificate, but with a statement indicating that the fruit is free of pests and diseases. The European Union allows the entrance of this fruit, but the fruit must be free of pests and diseases. The fruit from Vietnam destined for the USA should be inspected at origin by APHIS inspectors to ensure it is free of pests. After, this fruit will be subjected to gamma or X rays irradiation (4001000 Gy) and packed in insect-proof cartons. Each shipment must have a certificate that ensures that the treatment was made according to protocol. Hawaii can send Hylocereus fruit after irradiation at 400-Gy or 150-Gy and inspection for mealybugs (Dysmicoccus neobrevipes, Maconellicoccus hirsutus, and Pseudococcus crvptus). Irradiation as a quarantine treatment is already used commercially (Ihsanullah et al 2016); in 2014, Vietnam sent 2000 tons of fruit radiated by X-rays (400 Gy) to the US markets. Irradiation treatment at 800 Gy doses or less would ensure visual and compositional quality while providing quarantine security (Wall and Khan, 2008). Combined treatments to control pest and diseases has also been evaluated. A combination of hot water and gamma irradiation treatments (55 C for 5 min and 400 Gy) controlled the decays and fruit fly without affecting the fruit quality and physicochemical properties (Wasantha et al., 2013). Japan and other countries require hot air treatment (46.5 C, 20 min); this ensures the destruction of the Mediterranean fruit fly (Ceratitis capitata) or Bactrocera spp. (Hoa et al., 2006) in shipments from Asia and South America. However, the fruit quality was affected after storage at 5 C indicating that the hot treatment is an additional stress. From 2012, the pitahaya produced under the System Approach in Central America can enter the USA without applying any quarantine treatments. The System includes procedures for monitoring and oversight, establishment of pest-free abodes, and packing procedures.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Le Bellec and Vaillant (2011), Lim (2012), and Ortiz-Hernandez and Carrillo-Salazar (2012) made a general revision of the nutritional and medicinal properties, as well as its industrial uses. The juice is very cloudy and viscous; therefore, the raw pitahaya juice need to be clarified. A treatment with commercial enzymes at 49 C for 40 min seemed to resolve the problem (Nur et al., 2010). The heat treatment increase the viscosity and antioxidative properties of red pitahaya puree, the pasteurization at 90 C can be used to preserve it (Liaotrakoon et al., 2013). The seeds could be source of essential oils due to a high level of functional lipids (Ariffin et al., 2009; Chemah, et al., 2010; Lim et al., 2010). A powder from pitahaya could be used as a natural coloring agent and a health supplement (Yusof et al., 2012).
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Exotic Fruits Reference Guide
As stated above, due to its high contents of mucilaginous material, the pulp is very viscous. A pectin analysis showed a limited uronic acid content (32.3%), but high esterification degree (DE) (Ramirez-Truque et al., 2011). In the other hand, the cell wall polysaccharides from the pericarp also has low content of anhydrouronic acid (,65%), but low DE, indicating that the peel is unsuitable for pectin extraction. However, their high viscosity at low concentrations showed possible uses as commercial thickeners like locus bean gum, and guar gum (Garcia-Cruz et al., 2013; MontoyaArroyo et al., 2013). In addition, Muhammad et al. (2014) indicated that it can also be used as a functional and healthy ingredient in foods and beverages of low viscosity. Based on these properties, the peel can be used to obtain a powder high in dietary fiber, with high swelling capacity, high oil-holding capacity and high glucose retention. This powder can be used as functional ingredient to improve the human health (Zhuang et al., 2012). Betalains pigments maintain its color over a wide pH range (37), which makes them ideal for coloring low-acid foodstuff such as dairy products (Harivaindaran et al., 2008) instead of red beet pigment, overcoming their sensory and nutritious characteristics. The betalains content in Hylocereus spp. depends on the species and variety (Esquivel et al., 2007, Obenland et al., 2016). The flesh of red fruits (H. monacanthus) has the highest contents, while the white flesh fruit (H. undatus) has the lowest. Among different environmental factors that affect their stability, amount of light is the major factor of betalain degradation, while the storage at 4 C is the best condition to preserve the pigment (Woo et al., 2011). Products with betalains must be stable during the storage. The pigments extracted from red pitahaya flesh maintained its betalain content for up to 9 months, when they were treated at high temperature and short time (92 C, 20 s). However, also the ascorbic acid addition affects the stability. The betacyanin losses and color alteration were minimal in a system with the addition of 1% ascorbic acid prior to storage (Herbach et al., 2007). From a medicinal point of view, there are different properties that are worth noting. Different extracts of H. undatus showed wound healing properties on diabetic rats (Perez et al., 2005), as well as a protective effect of triterpenes on the microvascular activity in rabbits (Perez-Gutierrez et al., 2007). Additionally, pitahaya is a potential source of oligosaccharides with prebiotic properties that may be used as an ingredient in functional foods and nutraceutical products (Wichienchot et al., 2010). The peel extracts of white pitahaya may be a rich source of antioxidants and be used as antiproliferative agent against cancer cells (Kim et al., 2011; Lou et al., 2014). The peel could be regarded as a new valueadded ingredient with the potential to assist in the prevention of chronic diseases. The polyphenolic fractions from flesh and peels of H. polyrhizus might be purified to provide extracts and subfractions useful to inhibit the growth of pathogens in foods (Tenore et al., 2012).
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Identification of differentially-expressed genes potentially implicated in drought response in pitaya (Hylocereus undatus) by suppression subtractive hybridization and cDNA microarray analysis. Gene. 533, 322331. Freitas, S.T., Mitcham, E.J., 2013. Quality of pitaya fruit (Hylocereus undatus) as influenced by storage temperature and packaging. Sci. Agric. 70 (4), 257262. Freitas, S.T., Nham, N.T., Mitcham, E.J., 2011. Pitaya (Pitahaya, Dragon Fruit) recommendations for maintaining postharvest quality. Available at: ,http://postharvest.ucdavis.edu/PFfruits/Pitaya/.. Garcia-Cruz, E.E., Rodrı´guez-Ramı´rez, J., Me´ndez Lagunas, L.L., Medina-Torres, L., 2013. Rheological and physical properties of spray-dried mucilage obtained from Hylocereus undatus cladodes. Carbohydr. Polym. 91, 394402. Gunasena, H.P.M., Pushpakumara, D.K.N.G., Kariyawasam, M., 2007. Dragon fruit (Hylocereus undatus (Haw.) Britton and Rose. Chapter 4. In: Pushpakumara, D.K.N.G., Gunasena, H.P.M., Singh, V.P. (Eds.), Underutilized fruit trees in Sri Lanka. World Agroforestry Centre, South Asia Office, New Delhi, pp. 110141. Guo, L.W., Wu, Y.X., Ho, H.H., Su, Y.Y., Mao, Z.C., He, P.F., et al., 2014. First Report of Dragon Fruit (Hylocereus undatus) Anthracnose Caused by Colletotrichum truncatum in China. J. Phytopathol. 162, 272275. Harivaindaran, K.V., Rebecca, O.P.S., Chandran, S., 2008. Study of optimal temperature, pH and stability of drgaon fruit (Hylocereus polyrhizus) peel for use as potential natural colorant. Pakistan J. Biol. Sci. 11 (18), 22592263. Herbach, K.M.C., Stintzing, F.C., Carle, R., 2007. Effects of processing and storage on juice colour and betacyanin stability of purple pitaya (Hylocereus polyrhizus) juice. Eur. Food Res. Technol. 224, 649658. Hoa, T.T., Clark, C.J., Waddell, B.C., Woolf, A.B., 2006. Postharvest quality of Dragon fruit (Hylocereus undatus) following disinfesting hot air treatments. Postharvest. Biol. Technol. 41, 6269. Ihsanullah, I., Rashid, A., 2016. Current activities in food irradiation as a sanitary and phytosanitary treatment in the Asia and the Pacific Region and a comparison with advanced countries. Food. Control.http://dx.doi.org/10.1016/j.foodcont.2016.03.011. Jiang, Y.L., Liao, Y.Y., Lin, T.S., Lee, C.L., Yen, C.R., Yang, W.J., 2012. The Photoperiod-regulated Bud Formation of Red Pitaya (Hylocereus sp.). HortScience. 47 (8), 10631067. Khaimov, A., Mizrahi, Y., 2006. Effects of day-length, radiation, flower thinning and growth regulators on flowering of the vine cacti Hylocereus undatus and Selenicereus megalanthus. J. Hortic. Sci. Biotechnol. 81 (3). Khaimov-Armoza, A., Nova´k, O., Strnad, M., Mizrahi, Y., 2012. The role of endogenous cytokinins and environmental factors in flowering in the vine cactus Hylocereus undatus. Israel J. Plant Sci. 60 (3), 371383. Kim, J., Choi, H.K., Moon, J.Y., Kim, Y.S., Mosaddik, A., Cho, S.K., 2011. Comparative antioxidant and antiproliferative activities of red and white pitayas and their correlation with flavonoid and polyphenol content. J. Food Sci. 76 (1), C38C45. Kugler, F., Stintzing, F.C., Carle, R., 2007. Evaluation of the antioxidant capacity of betalainic fruits and vegetables. J. Appl. Bot. Food Qual. 81, 6976. Le Bellec, F., Vaillant, F., 2011. Chapter 12, Pitahaya (pitaya) (Hylocereus spp). In: Yahia, E. (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruits, vol. 4. Mangosteen to White Sapote. Woodhead Publishing, pp. 247267. Li, L., Lichter, A., Chalupowicz, D., Gamrasni, D., Goldberg, T., Nerya, O., et al., 2016. Effects of the ethylene-action inhibitor 1-methylcyclopropene on postharvest quality of non-climacteric fruit crops. Postharvest Biol. Technol. 111, 322329. Liaotrakoon, W., De Clercq, N., Hoed, V.V., De Walle, D.V., Lewille, B., Dewettinck, K., 2013. Impact of thermal treatment on physicochemical, antioxidative and rheological properties of white-flesh and red-flesh dragon fruit (Hylocereus spp.) purees. Food Bioprocess Technol. 6 (2), 416430. Lim, H.K., Tan, C.P., Karim, R., Ariffin, A.A., Bakar, J., 2010. Chemical composition and DSC thermal properties of two species of Hylocereus cacti seed oil: Hylocereus undatus and Hylocereus polyrhizus. Food Chem. 119, 13261331. Lim, T.K., 2012. Edible medicinal and non-medicinal plants, Fruits, vol. 1. Springer, Dordrecht Heidelberg London New York, pp. 640650. Luo, H., Cai, Y., Peng, Z., Liu, T., Yang, S., 2014. Chemical composition and in vitro evaluation of the cytotoxic and antioxidant activities of supercritical carbon dioxide extracts of pitaya (dragon fruit) peel. Chem. Cent. J. 8, 17. Menezes-Cordeiro, M.H., Mendes da Silva, J., Mizobutsi, G.P., Mizobutsi, E.H., Ferreira da Mota, W., 2015. Physical, chemical and nutritional characterization of pink pitaya of red pulp. Rev. Bras. Frutic. 37 (1), 2026. Mizrahi, Y., 2014. Vine-cacti pitayas-the new crops of the world. Rev. Bras. Frutic. 36 (1), 124138. Mizrahi, Y., 2015. Thirty-one years of research and development in the vine cacti pitaya in israel. In: Jiang, Y.-L., Liu, P.-C., Huang, P.H., (Eds.), Improving Pitaya Production and Marketing: International Workshop Proceedings, September 79, 2015, Kaoshiung, Taiwan, organized by FFTC, TARI and SOFRI. Taipei, Taiwan, ROC: FFTC. 219pp. Montoya-Arroyo, A., Schweiggert, R.M., Pineda-Castro, M.L., Sramek, M., Kohlus, R., Carle, R., et al., 2013. Characterization of cell wall polysaccharides of purple pitaya (Hylocereus sp.) pericarp. Food Hydrocolloids 35, 557564.
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Moo-Huchin, V.M., Estrada-Mota, I., Estrada-Leo´n, R., Cuevas-Glory, L., Ortiz-Va´zquez, E., y Vargas, M.D. L.V., et al., 2014. Determination of some physicochemical characteristics, bioactive compounds and antioxidant activity of tropical fruits from Yucatan, Mexico. Food Chem. 152, 508515. Muhammad, K., Zahari, N.I.M., Gannasin, S.P., Adzahan, N.M., Bakar, J., 2014. High methoxyl pectin from dragon fruit (Hylocereus polyrhizus) peel. Food Hydrocolloids 42, 289297. Nerd, A., Mizrahi, Y., 1997. Reproductive biology of cactus fruit crops. Hortic. Rev. 18, 321346. Nerd, A., Gutman, F., Mizrahi, Y., 1999. Ripening and postharvest behavior of fruits of two Hylocereus species (Cacataceae). Postharvest Biol. Technol. 17, 3945. Nie, Q., Guo-Li, G., Qing-jie, F., Qiao, G., Xiao-Peng, W., Liu, T., et al., 2015. Isolation and characterization of a catalase gene “HuCAT3” from pitaya (Hylocereus undatus) and its expression under abiotic stress. Gene. 563, 63710. Nobel, P.S., De la Barrera, E., 2002. Stem water relations and net CO2 uptake for a hemi epiphytic cactus during short-term drought. Environ. Exp. Bot. 48, 129137. Nobel, P.S., De la Barrera, E., 2004. CO2 uptake by the cultivated hemiepiphytic cactus, Hylocereus undatus. Ann. Appl. Biol. 144, 18. Nur ‘Aliaa, A.R., Siti Mazlina, M.K., Taip, F.S., Liew Abdullah, A.G., 2010. Response surface optimization for clarification of white pitaya juice using a commercial enzyme. J. Food. Process. Eng. 33, 333347. Obenland, D., Cantwell, M., Lobo, R., Collin, S., Sievert, J., Arpaia, M.L., 2016. Impact of storage conditions and variety on quality attributes and aroma volatiles of pitahaya (Hylocereus spp.). Sci. Hortic. (Amsterdam). 199, 1522. Ortiz-Herna´ndez, Y.D., Livera-Mun˜oz, M., Colinas-Leon, M.T., Carrillo-Salazar, J.A., 1999. Water stress and CO2 exchange rate of pitahaya (Hylocereus undatus). Agrociencia 33, 397405. Ortiz-Herna´ndez, Y.D., Carrillo-Salazar, J.A., 2012. Pitahaya (Hylocereus spp.): a short review. Comun. Sci. 3 (4), 220237. Available from: http:// dx.doi.org/10.4067/S0718-34292015000200008. Osuna-Enciso, T., Ibarra-Zazueta, M.E., Muy-Rangel, M.D., Valdez-Torres, J.B., Villarreal-Romero, M., Herna´ndez-Verdugo, S., 2011. Postharvest quality of pitahaya (Hylocereus undatus Haw.) fruits harvested in three maturity stages. Rev. Fitotec. Mex. 34 (1), 6372. Perez, G.R.M., Vargas, R.S., Ortiz, H.Y.D., 2005. Wound Healing Properties of Hylocereus undatus on diabetic rats. Phytother. Res. 19, 665668. Perez-Gutie´rrez, R.M., Vargas-Solı´s, R., Garcı´a-Baez, E., Mota-Flores, J.M., 2007. Microvascular protective activity in rabbits of triterpenes from Hylocereus undatus. J. Nat. Med. 61, 296301. Phebe, D., Chew, M.K., Suraini, A.A., Lai, O.M., Janna, O.A., 2009. Red-fleshed pitaya (Hylocereus polyrhizus) fruit colour and betacyanin content depend on maturity. Int. Food Res. J. 16, 233242. Punitha, V., Boyce, A.N., Chandran, S., 2010. Effect of storage temperatures on the physiological and biochemical properties of Hylocereus polyrhizus. Acta Hortic. 875, 137144. Qiong, C., 2015. Isolation and characterization of a catalase gene “HuCAT3” from pitaya (Hylocereus undatus) and its expression under abiotic stress. Gene. 563, 6371. Ramı´rez-Truque, C., Esquivela, P., Carle, R., 2011. Neutral sugar profile of cell wall polysaccharides of pitaya (Hylocereus sp.) fruits. Carbohydr. Polym. 83, 11341138. Serna-Cock, L., Torres Valenzuela, L.S., Ayala Aponte, A., 2012. Changes in mechanical properties of minimally-processed yellow pitahaya treated with 1-MCP. Dyna. 79 (164), 7178. Stintzing, F.C., Schieber, A., Carle, R., 2002. Betacyanins in fruits from red-purple pitaya, Hylocereus polyrhizus (Weber) Britton & Rose. Food. Chem. 77, 101106. Taba, S., Miyahira, N., Nasu, K., Takushi, T., Moromizato, Z.I., 2007. Fruit rot of Strawberry pear (pitaya) caused by Bipolaris cactivora. J. Gen. Plant Pathol. 73, 374376. 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Pitomba—Talisia esculenta Sueli Rodrigues1, Edy Sousa de Brito2 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Botanical Aspects and Harvest Season Estimated Annual Production Chemical Composition and Nutritional Value Including, Vitamins, Mineral, Phenolics, and Antioxidant Compounds
351 351
Industrial Application or Potential Industrial Application References
353 353
351
BOTANICAL ASPECTS AND HARVEST SEASON The pitomba fruit (Talisia esculenta Radlk), also known as olho-de-boi, bush pitomba and monkey pitomba, is a member of Sapindaceae family and is native to the South American Amazon area. The plant is found in temperate and tropical areas. In Brazil, the fruit is found spread throughout the whole country (Dı´az and Rossini, 2012; Majheni et al., 2007). The pitomba tree grows to 515 m high and is very leafy. The bark is cylindrical, striated with puberulent branches. The leaves are 512 cm long and 25 cm broad and alternately arranged with 511 leaflets. The inflorescence is up to 20 cm in length by 36 cm in width, terminal, axillary and consisted short-styled dicassia. The flowers are small and whiteyellow and produced in a panicle that is 1015 cm long. The fruit is about 1.54 cm in diameter, and the fruit shape might be round or ellipsoid. Beneath the outer peel is the white, translucent, sweetsour pulp with one or two large, elongated seeds (Fig. 1). The pitomba trees are naturally found all over Brazil, and it is well adapted to the Brazilian Cerrado (Mato Grosso and Goias states of Brazil). The plant is also found in Bolivia and Paraguay. The pitombeira flowers from August to October and the maturation of the fruit occurs from there, being more pronounced from January to March, depending on the region. The plant germination is hypogean, whose cotyledons are not raised above the soil, remaining partially buried in the soil. The tree is widely grown in domestic orchards throughout the country. The plant is indicated for planting in degraded areas of permanent preservation. The bark and the leaves contain tannin, and the sap is ichthyotoxic (Neto et al., 2003). The pitomba tree propagation is by seeds, which have short longevity, requiring planting soon after the extraction of the seeds from the fruits (De Almeida Cardoso et al., 2015).
ESTIMATED ANNUAL PRODUCTION The pitomba fruit is usually commercialized in local markets. The fruits are mainly collected from wild trees or domestic orchards, and there is no official data on its annual production. However, it is common to find the fruits in street markets during the harvesting season.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING, VITAMINS, MINERAL, PHENOLICS, AND ANTIOXIDANT COMPOUNDS Pitomba pulp is the fruit edible part presenting a whitepink color and an apricot-like texture. The pitomba composition is presented in Table 1. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00046-0 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Pitomba fruit.
TABLE 1 Pitomba Composition Compound
Content
Energy
56 kcal/100 g
Moisture
83%
Protein
1.15 g/100 g
Lipids
0.19 g/100 g
Carbohydrate
12.5 g/100 g
Fibers
2.40 g/100 g
Ash
0.61 g/100 g
Calcium
26.7 mg/100 g
Zinc
0.84 mg/100 g
Iron
0.60 mg/100 g
Source: Silva, M.R., D.B.C.L. Lacerda, G.G. Santos, and D.M. de Oliveira Martins. 2008. Caracterizac¸a˜o Quı´mica de Frutos Nativos Do Cerrado Cieˆnc. Rural 38 (6), 17901793.
Recent studies reported the antiproliferative and antimutagenic activities of the pitomba pulp, reinforcing the idea that this fruit may be a functional food source (Neri-Numa et al., 2014). Aroma is also an important property of fruits and one of their most appreciated characteristics. Aroma is a combination of volatile organic compounds (VOCs), which are biosynthesized during ripening and characterize a specific fruit or variety (Bicas et al., 2011; Geo˝ cze et al.,
Pitomba—Talisia esculenta
353
TABLE 2 Quantification of the Phenolic Compounds in Pitomba Fruit (µg/g of Dry Pulp) Compound
Content
p-coumaric acid
3.4
Ferulic acid
1.8
Gallic acid
1.1
Catechin
1.4
Epicatechin
2.9
Caffeic acid
0.6
Chlorogenic acid
1.5
Quinic acid
807.8
Source: de Souza, M.P., et al., 2016. Phenolic and Aroma compositions of pitomba fruit (Talisia Esculenta Radlk.) assessed by LC-MS/MS and HS-SPME/GC-MS Food Res. Int. 83, 8794. http://dx.doi.org/10.1016/j.foodres.2016.01.031.
2013). Therefore, the aroma composition is an important tool for further investigations concerning the processing and storage of a fruit pulp. The pitomba flavor was described as a combination of apricot and lemon (Guarim-Neto et al., 2000). It is rich in phenolic compounds such as catechins and flavonoids. A total of 27 volatile organic compounds (VOCs) were reported for pitomba fruit. The esters 2-phenethyl acetate (17.89%) and isopentyl acetate (13.43%) were the main VOCs related to the pitomba characteristic aroma. A more recent study reported the following VOCs in pitomba fruit: hexanal; 2(e)-2-hexenal; hexan-1-ol; isopentyl acetate; furan-2-pentyl; hexyl acetate; d-limonene; 1-octanol; linalool; nonanal; 2-phenylethanol; 1-nonanol; ethyl octanoate; decanal; phenethyl acetate; 1-undecanol; tetradecane; dodecanal; β-ionone; pentadecane; β-bisabolene; dodecanoic acid; e,e-farnesol; methyl palmitate; (e)-11-hexadecenoic acid ethyl ester; ethyl linoleate and ethyl oleate (de Souza et al., 2016). Due to the presence of antioxidant compound,s pitomba is considered a moderately antioxidant fruit. De Souza et al. (2016) studied the phenolic composition of Pitomba fruit and reported the presence of the following compounds: quinic acid; gallic acid; chlorogenic acid; catechin; epicatechin; caffeic acid; syringic acid; p-coumaric acid; rutin; ferulic acid; quercetin eriodictyol and acacetin. Table 2 depicts the major phenolics found in pitomba fruit.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION The pitomba fruits, peels, leaves, and wood can be used. Fruits are edible, marketed in street fairs in the North and Northeast of Brazil. The seeds are considered as antidiarrheals and used as astringents. The tea of the seeds is used to for dehydration treatment, and the leaf tea is indicated for hip pain and kidney problems (Guarim Neto, 1987, 1996). Due to the local production without a large scale market, there is no industrial processing for pitomba, despite its documented healthy benefits. The fruit is usually consumed in natura or used in the local culinary. The pulp is also used to produce jams and home-made sweets (De Almeida Cardoso et al., 2015; Viera e Gusma˜o, 2008)
REFERENCES Bicas, J.L., Molina, G., Dionı´sio, A.P., Barros, F.F.C., Wagner, R., Maro´stica Jr., M.R., et al., 2011. Volatile constituents of exotic fruits from Brazil. Food Res. Int. 44, 18431855. De Almeida Cardoso, E., Ursulino Alves, E., Ursulino Alves, A., 2015. Qualidade de Sementes de Pitombeira Em Func¸a˜o Do Perı´odo E Da Temperatura de Secagem. Sem:Cienc. Agrarias. 36 (1), 716. de Souza, M.P. et al., 2016. Phenolic and Aroma compositions of pitomba fruit (Talisia Esculenta Radlk.) assessed by LC-MS/MS and HS-SPME/GCMS. Food Res. Int. 83, 8794. http://dx.doi.org/10.1016/j.foodres.2016.01.031. Dı´az, M., Rossini, C. 2012. Bioactive natural products from Sapindaceae deterrent and toxic metabolites against insects. In: F. Perveen (Ed.), Insecticides Pest Engineering. Janeza Trdine 9, 5100 Rijeka, Croatia, 555. Ge˝ocze, K.C., Barbosa, L.C.A., Fideˆncio, P.H., Silve´rio, F.O., Lima, C.F., Barbosa, M.C.A., et al., 2013. Essential oils from pequi fruits from the Brazilian Cerrado ecosystem. Food Res. Int. 54, 18. Guarim Neto, G. 1987. Plantas utilizadas na medicina popular do estado de Mato Grosso. Brası´lia, MCT/CNPq. 58 pp.
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Guarim Neto, G., 1996. Plantas medicinais do Estado de Mato Grosso. Brası´lia: Associac¸a˜o Brasileira de Educac¸a˜o Agrı´cola Superior. 72p. Guarim Neto, G., Santana, S.R., Silva, J. V. da, 2000. Notas etnobotaˆnicas de Sapindaceae Jussieu. Acta Bot. Bras. 14 (3), 327334. Guarim Neto, G., Santana, S.R., Valdete, J., Silva, B., 2003. Botanical Repertorium of the ‘Pitombeira’ (Talisia Esculenta). Acta Amazonica 33 (2), 16. Majhenic, L., Skerget, M., Knez, Z., 2007. Antioxidant and antimicrobial activity of guarana seed extracts. Food Chem. 104 (3), 12581268. Neri-Numa, I.A., de Carvalho-Silva, L.B., Macedo Ferreira, J.E., Tomazela Machado, A.R., Malta, L.G., Tasca Gois Ruiz, A.L., et al., 2014. Preliminary evaluation of antioxidant, antiproliferative and antimutagenic activities of pitomba (Talisia esculenta). LWT-Food Sci. Technol. 59, 12331238. Silva, M.R., Lacerda, D.B.C.L., Santos, G.G., de Oliveira Martins, D.M., 2008. Caracterizac¸a˜o Quı´mica de Frutos Nativos Do Cerrado. Cieˆnc. Rural. 38 (6), 17901793. Vieira, F.A., Gusma˜o, E., 2008. Biometria, armazenamento de sementes e emergeˆncia de plaˆntulas de Talisia esculenta Radlk. (Sapindaceae). Cieˆnc. Agrotecnol. 32, 10731079.
Pomegranate/RomaPunica granatum Mustafa Erkan and Adem Dogan Akdeniz University, Antalya, Turkey
Chapter Outline Cultivars, Origin, and Botanical Aspects Harvest Seasons Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Harvest and Postharvest Conservation Controlled Atmosphere/Modified Atmosphere Storage
355 357 357 358 358 358 359
Problems Under Suboptimal Conditions Industrial Application Minimally Processed or Ready-to-Eat Arils Jelly, Beverages, and Other Usage References Further Reading
359 360 360 360 360 361
CULTIVARS, ORIGIN, AND BOTANICAL ASPECTS Pomegranate, one of the oldest known edible fruit, is native to central Asia. It is believed to be among the first cultivated fruit in the Middle East. Pomegranate is classified as a berry and belongs to the Punicaceae family. Punica, the only genus in this family, has a predominant species called Punica granatum (Zarfeshany et al., 2014). Pomegranate is spread out from its origin of what is now Iran and Afghanistan to east India and China and to west Mediterranean basin, USA and the southern hemisphere as well. The primary commercial pomegranate-growing regions in the world are India, the Middle East and Mediterranean basin countries (Erkan and Kader, 2011). Pomegranate has been introduced into Latin America and USA by Spanish settlers and is also being cultivated in parts of California and Arizona. The pomegranate requires a long, hot summer for fruit maturation, but it can withstand, up to certain point, low winter temperatures, drought, and salinity. There are several types of pomegranates including ornamental types; these are double flowers that are largely sterile. The pomegranate plant is a bushy small tree of 38 m high, evergreen in the tropics and deciduous in subtropical and temperate climates. There are dwarf cultivars that do not reach 1.5 m height (Holland et al., 2009). The trunk is covered by redbrown bark which later becomes gray. Branches are stiff, angular, and often spiny. There is a strong tendency to produce suckers from the base, which gives rise to the bushy or shrubby form of growth. In orchards, plants are normally trained to a single trunk, forming a large shrub or small tree. Trees may be trained to multiple trunks in colder areas, to reduce risk of total tree loss. While pomegranates may live as long as 200 years, tree vigor declines after about 15 years and the plant becomes nonproductive. Most pomegranates begin fruiting in their second year, but substantial bearing does not begin until 35 years of age (Glozer and Ferguson, 2011). A pomegranate tree bears two kinds of flowers, male and hermaphroditic, from which fruit are derived. Aril, the edible portion of fruit, is a seed around the juicy pulp formed from ovules present in the ovary of the fertilized fruit (Shulman et al., 1984). The pomegranate fruit develops from the ovary measuring 6.2512.5 cm wide and 200650 g in weight (Fig. 1). Nearly-round pomegranate fruit is crowned by a prominent calyx and connected to the tree by a short stalk (Holland et al., 2009). The fruit has a smooth leathery skin and is divided by thin inedible membranes into a number of sections each of which are filled with angular seeds covered by juicy pulp sacs. The peel color of the fruit varies with green, pink, reddish, or dark red and there are also some cultivars that have a black external color. Peel thickness varies from 1.5 to 4.24 mm and cultivars, genotypes, and cultural practices have an impact on skin thickness (Pekmezci and Erkan, Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00049-6 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Pomegranate fruit at different sizes.
FIGURE 2 Pomegranate arils.
2004). The edible part (arils) of pomegranate fruit is about 55%60% of the total fruit weight and contains 80% juice and 20% seeds (Erkan and Kader, 2011). The fruit contains many arils separated by white pericarp. The arils (Fig. 2) contain a juicy edible layer that developed entirely from outer epidermal cells of the seed and vary in color, size, and hardness. There are some soft seeded cultivars called seedless pomegranates (Holland et al., 2009). In general, the wild genotypes have higher aril hardness as well as higher seed hardness and toughness (Al-Said et al., 2009). There is no consistent correlation between the outer skin color of the rind and the color of the arils. Cultivars are categorized as sweet, sweet/sour, or sour depending on acidity levels (Pekmezci and Erkan, 2004).
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HARVEST SEASONS The harvest season is from September to November in the northern hemisphere, and from March to May in the southern hemisphere. The fruit is classified as nonclimacteric; they do not ripen off the tree and should be harvested when it is reached fully mature stage to ensure their best eating quality (Erkan and Kader, 2011). The fruit reaches full maturity stage within 135180 days after anthesis, depending on genotypes, cultivars, and climatic conditions (Kader, 2006). Maturity indices for pomegranate fruits are cultivar-dependent and include skin and aril color, acidity level, total soluble solids (TSS) content and TSS/acid ratio (Crisosto et al., 2000; Al-Maiman and Ahmad, 2002; Erkan and Kader, 2011). In addition, calyx opening is a good indicator for the harvest determination in some cultivars. Due to the extended blooming period, harvest season lasts almost one month, with an interval of 710 days and 23 times per season. For example, California-grown “Wonderful” pomegranates harvested in mid-October had an average TSS content of 18.1% and the acidity of 1.58%, whereas those harvested in late September averaged 17% and 1.8%, respectively (Kader et al., 1984). In Turkey’s ecological conditions, “Hicaznar” is harvested when TSS content and acidity level reached to 17%18% and 1.4%1.7%, respectively (Selcuk and Erkan, 2015).
ANNUAL PRODUCTION Over the past decade, drastic increases in world production and trading quantities of pomegranate fruit were noticed as a result of the growing awareness to its nutritional and health issue. The total world production of currently estimated pomegranate is about 3 million tons/year. At present 90% of the world’s pomegranate production occurs in the northern hemisphere, but a growing exporting opportunity exists for the countries in the southern hemisphere to provide fruit to the markets during the counter season. South Africa is one of the major producers of pomegranate fruit in the southern hemisphere (Arendse, 2014). The main producers of pomegranate fruit are China, India, Iran, Turkey, USA, and South Africa (Table 1).
TABLE 1 Top Pomegranate Producing Countries in 2012 Countries
Production (31000 tons)
China
1.200i
Iran
1.009a
India
745b
Turkey
315c
USA
282d
South Africa
198e
Azerbaijan
141f
Tunisia
73g
Israel
70i
Afghanistan
62h
Spain
60i
Egypt
43i
Uzbekistan
35i
a
Iran statistical year book (2012). India Ministry of Agriculture (2014). c Turkish Statistical Institute (2012). d Marzolo (2015). e Perishable Products Export Control Board of South Africa (2012). f The State Statistical Committee of the Republic of Azerbaijan (undated). g Annuaire Statistique De La Tunisie (2012). h Afghanistan Statistical Yearbook (2012). i Estimated data (2012). b
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FRUIT PHYSIOLOGY AND BIOCHEMISTRY The developmental period of pomegranate arils extends up to 80 days from fruit set, which is associated with a continuous increase in concentration of total sugars, reducing sugars, and anthocyanin pigments. The period is accompanied by a significant reduction in total phenolics, ascorbic acid, and titrable acidity up to 80 days, followed by a steady-state. The highest titratable acidity (0.56% of citric acid) was recorded in 60 day-old pomegranate fruit arils. This was followed by a continuous decrease to the lowest concentration of 0.33, which was recorded in 140 days old fully mature fruit. During maturation, citric acid, ascorbic acid and juice percentage decreases and TSS content, total and individual sugars, TSS/acid ratio, pH, and red color intensity of the juice increases (Al-Maiman and Ahmad, 2002). The type of organic acids is cultivar-dependant in pomegranates. For example, citric acid is the main organic acid in the “Mollar” cultivar, followed by tartaric acid, whereas the “Assaria” cultivar has almost equal levels of citric, oxalic, and tartaric acids (Miguel et al., 2006). In contrast, considerable variation is found in some of the chemical properties of different ¨ zgen et al., 2008). pomegranate cultivars grown in the Mediterranean region of Turkey (O
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE In recent years, the production, marketing, and consumption of pomegranate fruit is increasing rapidly throughout the world, mainly due to greater awareness of their health-promoting attributes (Selcuk and Erkan, 2015). Pomegranate fruit are rich source of polyphenols, including ellagitannins, gallotannins, ellagic acids, gallagic acids, catechins, anthocyanins, ferulic acids, and quercetins. These polyphenols exhibit various biological activities, such as eliminating free radicals, inhibiting oxidation and microbial growth, and decreasing the risk of cardiovascular and cerebrovascular diseases and some type of cancers (Mena et al., 2011). In addition, pomegranate fruit are good source of nutrients and bioactive compounds, mainly anthocyanins which exhibit strong chemopreventive activities such as antimutagenicity, antihypertension, oxidative potential and reduction of liver injury. The fresh juice contains 85% water and 15% sugar, pectin, ascorbic acid, polyphenolic flavonoids, anthocyanins, and amino acids (Kader, 2006). Pomegranate juice contains fructose and glucose in similar quantities; calcium is 50% of its ash content (Aviram et al., 2004). The juice is also rich in organic acids, vitamins, polysaccharides, and essential minerals (Al-Maiman and Ahmad, 2002). The levels of these compounds vary among cultivars, maturity stage of fruits, environmental conditions, and cultural practices of production. Pomegranate taste is dependent on its TSS content/acid ratio that varies among the cultivars. But TSS content should be above 17% for optimum level of sweetness. There is a strong positive correlation between total phenolics and antioxidant activity of pomegranates. However, above a certain concentration, phenolic compounds can make the juice less desirable because of astringency (Kader, 2006). In general, varieties that have whitish or pinkish arils are usually sweeter than those with purplish or dark crimson arils because the latter varieties contain higher concentrations of organic acids (Gil et al., 1996). Differences in TSS content, juice color, percent of edible portion, and percent of extractable juice were small among fruits of various sizes. Larger fruits (more than 250 g) were generally lower in titratable acidity than smaller fruits (Kader, 2006). The overall sensory sweetness of pomegranate juice depends on sugars types, namely fructose, glucose, sucrose, whereas its acidic tastes is as a result of its organic acids, predominantly; malic, tartaric, citric acids. Sweet cultivars are reported to have high sugar content and low organic acid levels whereas sour cultivars have high organic acid and low sugar content levels (Melgarejo et al., 2000; Arendse, 2014).
HARVEST AND POSTHARVEST CONSERVATION Pomegranate is a nonclimacteric fruit and therefore it must be harvested when it has reached the fully mature stage. Maturity indices for the fruit are cultivar-dependent and include skin and aril color, acidity level, soluble solids content, and TSS/acid ratio (Crisosto et al., 2000; Al-Maiman and Ahmad, 2002; Erkan and Kader, 2011). Care must be taken when harvesting and handling the fruit as most varieties have fine and delicate skin that is susceptible to bruising if not handled properly. Pomegranates do not form abscission layers and therefore should be harvested by clippers and placed gently into picking bags, then transferred to harvest bins destined for the packing houses. The mildly defected fruit may be used for processing into juice, and those with very slight or no defects are marketed for fresh consumption. For fresh markets, pomegranates are washed, size-graded, and packed in shipping containers after treatment with fungicide or wax (Kader, 2006; Ergun, 2012).
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Temperature is the most important factor affecting fruit quality, deterioration rates, and storage duration for pomegranate fruit. Fruit of pomegranates can be stored at 5 C for up to 2 months, but longer storage should be at 7 C to avoid chilling injury (CI) (Kader et al., 1984; Erkan and Kader, 2011). Spanish “Mollar” pomegranates can suffer CI if they are stored for more than 2 months at temperatures below 5 C (Arte´s et al., 2000). Similarly, Hicaznar, a popular Turkish cultivar, can be stored up to 6 months at 6 C in MAP without any CI symptoms (Selcuk and Erkan, 2015). Therefore, the minimum safe temperatures for storing pomegranates varies among cultivars and growing regions and should be 5 C7 C (Erkan and Kader, 2011). The relative humidity (RH) is another important factor for maintaining postharvest quality of pomegranates. The objective of storage is minimizing the weight loss without increasing the microbial development and decay and temperature and RH are the key factors to fulfill this objective.
CONTROLLED ATMOSPHERE/MODIFIED ATMOSPHERE STORAGE Controlled atmosphere (CA) can be defined as a creation of altered atmosphere, in order to provide an appropriate atmosphere for slowing down the respiration, decreasing fungal and physiological deteriorations, and prolonging storage duration. CA storage with different O2 and CO2 levels reduce weight loss, fungal decay, and physiological disorders during storage. Arte´s et al. (1996) reported that CA storage was effective in maintaining fruit quality by reducing CI, weight loss and fungal decay in Spanish “Mollar de Elche” pomegranates. This cultivar could be kept at 5 C in a CA of 5 kPa O2 1 5 kPa CO2 for up to 2 months and at 7.5 C in 5 kPa O2 1 15 kPa CO2 for up to 5 months. In another study, “Hicaznar” pomegranates stored in 1 kPa CO2 1 3 kPa O2, 3 kPa CO2 1 3 kPa O2, or 6 kPa CO2 1 3 kPa O2 had a storage life of 130 days (Ku¨pper et al.,1995). Defilippi et al. (2006) have found that the most effective postharvest decay control on “Wonderful” pomegranates was the combination of prestorage treatment with potassium sorbate followed by storage in an atmosphere of 5 kPa O2 1 15 kPa CO2 at nonchilling temperatures. Modified atmosphere packaging (MAP) is defined as “the packaging of a perishable product in an atmosphere which has been modified so that its composition is other than that of regular atmosphere”. MAP technology offers the possibility to retard respiration rate and extend the shelf life of pomegranates. Water loss from pomegranate peel results in weight loss and shriveling leading to a direct financial loss due to unsaleable stored fruits (Selcuk and Erkan, 2015). Therefore, appropriate packaging and optimal storage conditions should be applied to extend the shelf life of both fresh and ready-to-eat pomegranated. On the other hand, it is important to correlate the permeability properties of the packing films with the respiration rate of the produce, in order to avoid anaerobic conditions which could lead to fermentation of produce and accumulation of ethanol. These techniques are used to support and supplement low temperature storage to delay respiration rated and ripening, to reduce physiological disorders, and to suppress decay during the storage and extension of shelf life in many fresh fruit and vegetables. MAP is a simple and low-cost method that has been proven to maintain postharvest quality of pomegranates up to 6 months after harvest (Selcuk and Erkan, 2015). Porat et al. (2009) reported that crop-specific MAP for pomegranate fruits having different gas permeabilities results in the accumulation of 5kPa O2 1 1214 kPa CO2 within the bags at the end of prolonged storage. These types of bags reduced weight loss from 7% to 3.5% and husk scald development from 38% to 21% in “Wonderful” pomegranates. Similarly, the storage of “Wonderful” pomegranates in MAP using commercial Xtends bags reduced weight loss, decay development, and scald incidence and maintained fruit quality for 3 months after harvest (Porat et al., 2009).
PROBLEMS UNDER SUBOPTIMAL CONDITIONS One of the major problems associated with pomegranate fruit under suboptimal conditions is excessive water loss which may result in weight loss, hardening of the husk, and browning of the rind and arils (Arte´s et al., 2000; Caleb et al., 2012). Even in the absence of shriveling, water loss can cause undesirable textural and flavor changes, ultimately resulting to loss of marketibility. Al-Mughrabi et al. (1995) observed that high storage temperature and duration of storage has increased weight loss on “Taeifi”, “Manfaloti”, “Ganati” pomegranates. The authors reported that higher weight loss was observed on pomegranates stored at 22 C than those stored at 10 C and 5 C (weight losses of 32.83%, 21.93%, and 18.32%, respectively) after 2 months of storage. Pomegranate fruit are very susceptible to CI if they are stored for longer than one month at temperatures between 23 C and 5 C or longer than two months at 5 C (Kader et al., 1984).
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INDUSTRIAL APPLICATION The demand for pomegranate fruit and its byproducts is rising exponentially, especially in the USA and Europe, owing to the growing awareness of the health-promoting benefits of pomegranate. Because of this trend, Iran and India are becoming leaders of the pomegranate market, followed by China, Turkey, and the USA. The trend for cultivation and consumption is enourmously increasing in many countries. These countries process fruit into juice and juice concentrate, exporting the concentrate to the many countries as numerous different juices, products, and functional beverages are formulated using juice concentrate (Borgese and Massini, 2007). Increasing mechanization of aril extraction with minimal damaged fruit and subsequent preparation steps of arils as a ready-to-eat products will increase marketability and profit of minimal damaged fruits. Further development of nutraceuticals derived from the edible and nonedible portions of pomegranates will increase the popularity and profitability of pomegranates.
MINIMALLY PROCESSED OR READY-TO-EAT ARILS In spite of the numerous health benefits, pomegranate consumption is still limited, due to the difficulties of separation the arils from the fruit and the irritation of phenolic metabolites’ which stain the hands and clothes during extraction of the arils. The hard peel of pomegranate fruit makes it difficult to peel and extract the arils, thus limiting its consumption as a fresh fruit. On the other hand, pomegranate is a very sensitive fruit to sunburn, cracking, cuts, or bruises in the husk (Arte´s et al., 2000). Usually, these diverse external defects make the injured fruit unsuitable for fresh marketing and consumption, despite their excellent internal quality. Therefore, the minimally fresh processing of the externally mildly damaged pomegranates could be an excellent way to obtain a commercial profit from discarded pomegranates that are unacceptable for fresh marketing and consumption (Lopez-Rubira, 2005). Therefore, marketing of pomegranate arils in “minimally processed or ready-to-eat” form would be a convenient and alternative method to the consumption of fresh fruits and may further increase pomegranate demand by consumers.
JELLY, BEVERAGES, AND OTHER USAGE Pomegranate fruit is commonly consumed as fresh or fruit juice, but can also be used for making jams, jelly, sauce, grenadine or as flavoring and coloring agents. The peel is a rich source of natural antioxidants and has been used in the Middle East as coloring agents for textiles due to the high tannin and phenolic contents (Al-Said et al., 2009).
REFERENCES Afghanistan Statistical Yearbook, 2012. Available from: ,http://cso.gov.af/Content/files/08%20Agriculture%20Development.pdf.. Al-Maiman, S.A., Ahmad, D., 2002. Changes in physical and chemical properties during pomegranate (Punica granatum L.) fruit maturation. Food Chem. 76, 437441. Al-Mughrabi, M.A., Bacha, M.A., Abdelrahman, A.O., 1995. Effect of storage temperature and duration on fruit quality of three pomegranate cultivars. Agric. Sci. 7 (2), 239248. Al-Said, F.A., Opara, L.U., Al-Yahyai, R.A., 2009. Physico-chemical and textural quality attributes of pomegranate cultivars (Punica granatum L.) grown in the Sultanate of Oman. J. Food Eng. 90, 129134. Annuaire Statistique De La Tunisie, 2012. Available from: ,http://www.ins.tn/sites/default/files/publication/pdf/anunaire_2012.pdf.. Arendse, E., 2014. Determining optimum storage conditions for pomegranate fruit (cv. Wonderful). MSc thesis, Stellenbosch University, 122 pp. Arte´s, F., Marin, J.G., Martinez, J.A., 1996. Controlled atmosphere storage of pomegranate. Z. Lebensm. Unters. Forsch. 203, 3337. Arte´s, F., Villaescusa, R., Tudela, J.A., 2000. Modified atmosphere packaging of Pomegranates. J. Food Sci. 65, 11121116. Aviram, M., Rosenblat, M., Gaitini, D., 2004. Pomegranate juice consumption for 3 years by patients with carotid artery stenosis reduces common carotid intimamedia thickness, blood pressure and LDL oxidation. Clin. Nutr. 23, 423433. Borgese, R., Massini, R., 2007. Pomegranate market, production trend and technology innovation. Fruit Process. 17, 326330. Caleb, O.J., Opara, U.L., Witthuhn, C.R., 2012. Modified atmosphere packaging of pomegranate fruit and arils: a review. Food Bioprocess. Technol. 5, 1530. Crisosto, C.H., Mitcham, E.J., Kader, A.A., 2000. Pomegranates, produce facts. Available from: ,http://postharvest.ucdavis.edu/Produce/ ProduceFacts/Fruit/Pomegranate.shtml.. Defilippi, B.G., Whitaker, B.D., Hess-Pierce, B.M., Kader, A.A., 2006. Development and control of scald on wonderful pomegranates during longterm storage. Postharvest Biol. Technol. 41, 234243. Ergun, M., 2012. Pomegranate. In: Siddiq, M. (Ed.), Tropical and Subtropical Fruits: Postharvest Physiology, Processing and Packaging. John Wiley & Sons, Inc, pp. 529548.
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Erkan, M., Kader, A.A., 2011. Pomegranate (Punica granatum L.). In: Yahia, E.M. (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruits. Woodhead Publishing, New York, pp. 287311. Glozer, K., Ferguson, L., 2011. Pomegranate Production in Afghanistan, UC Davis College of Cultural and Environmental Sciences, Davis Campus. Available from: , http://ucanr.edu/sites/Pomegranates/files/164500.pdf . . Gil, M.I., Arte´s, F., Toma´s-Barbera´n, F.A., 1996. Minimal processing and modified atmosphere packaging effects on pigmentation of pomegranate seeds. J. Food Sci. 61, 161164. Holland, D., Hatib, K., Bar-Ya’akovi, I., 2009. Pomegranate: botany, horticulture, breeding. Hort. Rev. 35, 127191. India Ministry of Agriculture, 2014. HandBook on Horticulture Statistics. Available from: ,http://agricoop.nic.in/imagedefault/handbook2014.pdf.. Iran Statistical Yearbook, 2012. Available from: ,https://www.oparsbooks.com/mn/iran-statistical-yearbook-1391-2012-2013.. Kader, A.A., 2006. Postharvest biology and technology of pomegranates. In: Seeram, N.P., Schulman, R.N., Heber, D. (Eds.), Pomegranates: Ancient Roots to Modern Medicine. CRC Press Taylor & Francis Group, Boca Raton, FL, pp. 211220. Kader, A.A., Chordas, A., Elyatem, S.M., 1984. Responses of pomegranates to ethylene treatment and storage temperature. Calif. Agric. 38 (7&8), 1415. Kupper, W., Pekmezci, M., Henze, J., 1995. Studies on CA-storage of pomegranate (Punica granatum L., cv. Hicaznar). Acta Hortic. 398, 101108. Lopez-Rubira, V., Conesa, A., Allende, A., Artes, F., 2005. Shelf life and overall quality of minimally processed pomegranate arils modified atmosphere packaged and treated with UV-C. Postharvest Biol. Technol. 37, 174185. Marzolo, G., 2015. Pomegranates. Available from: ,http://www.agmrc.org/commodities-products/fruits/pomegranates/.. Melgarejo, P., Salaza, D.M., Artes, F., 2000. Organic acids and sugars composition of harvested pomegranate fruits. Eur. Food Res. Technol. 211, 185190. Mena, P., Garcı´a-Viguera, C., Navarro-Rico, J., Moreno, D.A., Bartual, J., Saura, D., et al., 2011. Phytochemical characterisation for industrial use of pomegranate (Punica granatum L.) cultivars grown in Spain. J. Sci. Food Agric. 91, 18931906. Miguel, G., Fontes, C., Martins, D., Neves, A., Antunes, D., 2006. Effects of post-harvest treatment and storage time on the organic acid content in Assaria and Mollar pomegranate (Punica granatum L.) fruit. Ital. J. Food Sci. 18, 317322. Ozgen, M., Durgac, C., Serce, S., Kaya, C., 2008. Chemical and antioxidant properties of pomegranate cultivars grown in the Mediterranean region of Turkey. Food Chem. 111, 703706. Pekmezci, M., Erkan, M., 2004. Pomegranate, USDA Agricultural Handbook 66. Available from: ,http://www.ba.ars.usda.gov/hb66/index.html.. Porat, R., Weiss, B., Kosto, I., Fuchs, Y., Sandman, A., Ward, G., et al., 2009. Modified atmosphere/modified humidity packaging for preserving pomegranate fruit during prolonged storage and transport. Acta Hortic. 818, 299304. Selcuk, M., Erkan, M., 2015. Changes in phenolic compounds and antioxidant activity of soursweet pomegranates cv. Hicaznar during long-term storage under modified atmosphere packaging. Postharvest Biol. Technol. 109, 3039. Shulman, Y., Fainberstein, L., Lavee, S., 1984. Pomegranate fruit-development and maturation. J. Hortic. Sci. 59, 265274. The State Statistical Committee of the Republic of Azerbaijan, [Undated]. Available from: ,http://www.stat.gov.az/source/agriculture/indexen.php.. Zarfeshany, A., Asgary, S., Javanmard, S.H., 2014. Potent health effects of pomegranate. Adv. Biomed. Res. 3, 100.
FURTHER READING Glozer, K., Ferguson, L., 2008. Pomegranate production in Afghanistan. Available from: ,http://www.ip.ucdavis.edu.. Hand Book on Horticulture Statistics, India ministry of Agriculture. Available from: ,http://agricoop.nic.in/imagedefault/handbook2014.pdf.. Perishable Products Export Control Board (PPECB), 2012. Pomegranate fruit export in South Africa. Internal report, South Africa. Available from: ,http://www.ppecb.com.. Turkish Statistical Institute, 2012. Available from: ,http://rapory.tuik.gov.tr/26-07-2016-17:26:10-212329779719346312751711375835.html..
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Quince—Cydonia oblonga Moˆnica M. de Almeida Lopes1, Alex Guimara˜es Sanches1, Kellina O. de Souza1 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Origin and Botanical Aspects Production Postharvest Physiology and Nutritional Value Postharvest Conservation
363 363 364 366
Industrial Application References Further Reading
366 366 368
ORIGIN AND BOTANICAL ASPECTS The quince fruit (Cydonia oblonga Mill.) is a native of Western Asia, and the origin is considered the Transcaucasus region including Armenia, Azerbaijan, Iran, southwest of Russia and Turkmenistan (Pio et al., 2005a; USDA, 2009). Quince fruits are spread worldwide, called a variety of other names: Arabic: sefarjal; Chinese: wen po; English: quince; French: cognassier or coing; German: quitte or quittenbaum; Portuguese: marmelo; Russian; ajva; Spanish: membrillero; Swedish: kvitten, among others (Postman, 2009; Mir et al., 2015). The quince is a monotypic genus comprising the family Rosaceae, subfamily Maloideae and genus Cydonia (USDA, 2009). The quince plant grows as a shrub or small tree (46 m high) and is rounded by a canopy up to 3 m in diameter. The root presents a superficial and fasciculated system with tortuous trunk. The leaves are green-intense and bright from oval to oblong (510 cm in length). The flowers are white or pink, large and solitary (45 cm), with 5 petals, 20 or more stamens, 5 styles, a lower ovary with many ovules, with a flowering season from September and October (Wertheim, 2002; Al-Snafi, 2016). The fruit quince is globose to elongated (68 cm in diameter) with an average weight of 5080 g. The color of fruit epidermis changes from brown to light-green at the initial development phase to yellow when ripe (Al-Snafi, 2016; Wertheim, 2002). The seeds from the quince are brown, flattened on both sides and adhered to a white mucilage. There can be up to 50 seeds per fruit (Pio et al., 2007a). The pulp is yellowish, consistent, slightly sweet, acidic and astringent, however the pulp is not consumed in natura, but consumed as processed products such as jams, jellies, marmalade, compotes, and cakes (Silva et al., 2006; Alvarenga et al., 2008).
PRODUCTION The quince tree presents a good development in fertile soils and with adequate capacity for retention of water. The multiplication is performed mainly by cuttings and the planting should be carried out with seedlings of up to two years in a spacing of 5 3 3 between plants (Pio et al., 2007b) with cultivars chosen for commercial exploitation (Seifert et al., 2009). The species are tolerant to soil soaking and radical asphyxiation, and due to this factor are used as a rootstock in peach, pear, and apple crops (Manica-Berto et al., 2013). The late frosts and high winds hinder the growth of new branches, flowering, and fertilization. The harvest initiates after the fourth year of planting and occurs between January and March when the fruits are yellow to light-greenish and present an accentuated characteristic odor (Pio et al., 2008) (see also Fig. 1). The quince plant adapts well to temperate climates, being undemanding in cold temperatures (90500 h), and can withstand mild winters. At the vegetative and fruiting phases, the quince plant is demanding to high temperatures and Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00047-2 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Epidermis color of quince fruit during development, (A) unripe, (B) breaker, and (C) ripe. Manica-Berto, R. 2009. Caracterizac¸a˜o fenolo´gica, fı´sico-quı´mica e fitoquı´mica de cultivares de marmeleiro. 70f. Tese (Doutorado em Agronomia). Faculdade de Agronomia Eliseu Maciel. Universidade Federal de Pelotas, Pelotas.
accentuated luminosity (Bettiol Neto et al., 2011; Mora et al., 2015). Excess of moisture in the hot season is harmful due to diseases such as entomosis, which is considered to be the main disease of crop, besides bitter rot, black rot, and leaf spot (Pio et al., 2007a). According to IBGE (2013), the southeast region of Brazil cultivates 67.50% of the national quince area, followed by the south region (22.50%), the northeast (6.25%) and the central west (3.75%), being responsible for a an average of productivity between 8 and 10 t/ha of fruits in adult orchards. In Brazil, Minas Gerais is the largest producer of quince trees with 108 ha cultivated (Fachinello et al., 2011), followed by the states of Rio Grande do Sul, Espirito Santo, Bahia, and Goia´s (Bettiol Neto et al., 2011; Zambon et al., 2014). Despite the interest in the cultivation of quinces in subtropical and tropical regions, only the cultivar ‘Portugal’ has been commercially exploited in these regions (Pio et al., 2008). There are other cultivars with similar productive potential to “Portugal” such as “Smyrna”, “Mendoza INTA37”, “Rea’s mamouth”, “Sheldow” and “Provence” in subtropical regions (Bettiol Neto et al., 2011), and even in colder regions, such as “Lageado” and “De Patras”, possibly because these cultivars need more cold (Fioraranc¸o et al., 2006).
POSTHARVEST PHYSIOLOGY AND NUTRITIONAL VALUE Fruits with a ripening pattern that are denominated as climacteric, such as quince fruit, present intense transpiration, respiration, and ethylene production after removal of the mother plant, triggering rapidly the maturation process (Carneiro et al., 2015), significantly affecting the postharvest quality of fruits through physicochemical, biochemical, and sensorial transformations (Pereira et al., 2008; Prill et al., 2012). According to Silva and Oliveira (2013) the harvest and the postharvest characteristics of the quince fruit are influenced by climatic and edaphic factors of the crop in both temperate and subtropical regions beyond the phenological cycle of each cultivar that may be early, intermediate, or late. Bettiol Neto et al. (2011) and Leonel et al. (2016) determined it is time for a fruit harvest, when the epidermis color changes from deeper green to more yellowish green with values of luminosity (L) between 6570 and yellowish pulp between 8085 and angle hue for epidermis between 95100 and for pulp between 8590. When mature, the average fruit weight varies between 100280 grams, length 6570 mm, with diameter 5565 mm, fruit firmness 7590 N, soluble solids content 11.0013.50 Brix, titratable acidity of 0.680.75 g of malic acid per 100 g, and pH 3.54.2 in different quince cultivars (Bettiol Neto et al., 2011; Beinsan et al., 2015; Leonel et al., 2016). The quince pulp has 81.20% moisture, and other physiochemical components comprises the total protein (0.500.71 g/100 g), lipids (0.212.40 g/100 g), fibers (1.10%2.60%), starch (7.30 g g/100 g), ashes (0.530.70 g/ 100 g), total sugars (10.90 g/100 g), vitamin C (15.32 g/100 g), and total pectin (12.67 g/100 g) plus mineral nutrients such as potassium (189.00 mg/100 mg), calcium (66.00 mg/100 mg), iron (1.10 mg/100 mg), copper (6.00 mg/100 mg), magnesium (2.00 mg/100 mg), and zinc (0.13 mg/100 mg) (Table 1) (Souci et al., 2008; Leonel et al., 2016; Moradi et al., 2017).
Quince—Cydonia oblonga
365
TABLE 1 Nutritional Composition of Quince Pulp Nutrient
Pulp
References
Moisture (%)
76.5081.20
Leonel et al. (2016)
Proteins (g/100 g)
0.470.71
Leonel et al. (2016)
Lipids (g/100 g)
0.212.40
Leonel et al. (2016)
Fiber (%)
1.102.60
Leonel et al. (2016)
Starch
7.30
Leonel et al. (2016)
Ashes (g/100 g)
0.530.70
Leonel et al. (2016)
Total sugar (g/100 g)
10.90
Leonel et al. (2016)
Total Pectin
12.67
Leonel et al. (2016)
Ascorbic acid (mg/100 g)
15.32
Minerals (mg/100 g) Potassium
189.00
Souci et al. (2008)
Phosphorous
25.00
Souci et al. (2008)
Calcium
66.00
Souci et al. (2008)
Iron
1.10
Souci et al. (2008)
Copper
6.00
Souci et al. (2008)
Magnesium
2.00
Souci et al. (2008)
Zinc
0.13
Souci et al. (2008)
Source: Souci, S.W., Fachmann, W., Kraut, H., 2008. Food composition and nutrition tables, seventh revised ed. MedPharm Scientific Publishers, Taylor & Francis, A CRC Press Book, Routledge, London, United Kingdom, 1364p; Leonel, M., Leonel, S., Tecchio, M.A., Mischan, M.M., Moura, M.F., Xavier, D., 2016. Characteristics of quince fruits cultivars’ (Cydonia oblonga Mill.) grown in Brazil. Aust. J. Crop Sci. 10 (5), 711716.
According to Oliveira et al. (2007) due to the presence of phytochemical compounds as phenolic acids and flavonoids, the quince fruit has received great attention for their role in the prevention and treatment of various diseases. In this context, Mir et al. (2016) characterized different phenolic compounds in the quince pulp after processing, such as: quercetin (12.50%) and caffeolic acids, such as 5-O-cafeloquimic acid (36.20%) and rutin (21.10%). Already, total phenolic contents values remained among 79.72 and 243.54 mg/100 mg, these values can be considered as intermediate when compared to other fruits of the rosacea family, such as apple (321474 mg/100 mg), pear (271408 mg/100 mg), plum (471.40 mg/100 mg), grape (117.10 mg/100 mg), and strawberry (132.10 mg/100 mg) (Imeh and Khokhar, 2002). Alesiani et al. (2010) found different phenolics compounds in quince peel, among them: 3β-(18-hydroxylinoleoyl)28-hydroxyurs-12-ene, 3β-linoleoylurs-12-en-28-oic acid, 3β-oleoyl-24-hydroxy-24-ethylcholesta-5,28(29)-diene, tiglic acid 1-O-β-D-glucopyranoside, and 6.9-dihydroxymegastigmasta-5.7-dien-3-one 9-O-β-D-gentiobioside. Magalha˜es et al. (2009) compared the antioxidant and antiproliferative activity of the peel, pulp, and seed of quince fruit, and confirmed that the action against oxidative hemolysis of human erythrocytes is mainly due to 5-O-caffeoylquinic acid compound. The quince pulp is a good source of phenolic compounds which can contribute to a high antioxidant capacity. However, the antioxidant capacity of quince fruit is due not only to the phenolic compounds, but to the other compounds as carotenoids and tocopherols that present a great variation between leaves, epidermis, and pulp (Sabir et al., 2015). Benzarti et al. (2015) identified higher antioxidant capacity in quince leaves in relation to peel and pulp by the DPPH method. Oliveira et al. (2008) showed higher antioxidant properties in quince peel than pulp and the authors justified this effect to the higher accumulation of phenolic compounds in fruit epidermis when compared to pulp. Carotenoids are a group of natural pigments varying from yellow to red and are of great nutritional importance for the human diet. The antioxidant action of carotenoids minimizes the effects of free radicals, contributing to the prevention of diseases such as macular degeneration, and cancers (Mele´ndez-Martı´nez et al., 2007). In quince fruit, the carotenoids are concentrated mainly in peels, as they are synthesized along with the plastids, mainly located in cells of the
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epidermis, such as β-carotene, lycopene, β-cryptoxanthin and lutein plus zeaxanthin (Romorini et al., 2008). Alesiani et al. (2010) detected the presence of carotenoids in quince peel until now unknown by gas chromatography coupled to mass spectrometry, such as: 3β-(18-hydroxylinoleoyl)-28-hydroxy-12-ene (12); 3β-linoleoyl-lurs-12en-28-oic acid (15); 3β-oleoyl-24-hydroxy-24-ethyl-cholest-5.28 (29) diene (24); 1-O-β-D-glucopyranoside (35); 6.9-dihydroxymegastigmasta-5 and 7-dien-3-one 9-O-β-D-gentiobioside.
POSTHARVEST CONSERVATION The quality of the fruit is influenced by external conditions, such as cultivar, temperature, and humidity, and by internal factors related to the fruit structure. A particularly important function is attributed to the structure of the fruit surface layer and to the structure of the parenchymal cells (Thomidis et al., 2004). The best ripening temperature for quince fruit after storage is 20 C (68 F). As quince is a climacteric fruit, the acceleration of ethylene production during ripening is expected, resulting in a reduction of shelf-life (Kader, 1992; Beinsan et al., 2015). Beinsan et al. (2015) evaluated the refrigerated storage of fruits of three quince cultivars at 4 C and 22 C, and found significant differences between the fruits, probably related to the genotype pattern of each cultivar. However, was observed that, independently of the evaluated cultivar, the 4 C temperature preserved the qualitative attributes such as lower degradation of starch and organic acids (titratable acidity) and kept the contents of solids soluble in the pulp of the fruits during 14 days of storage, indicating, therefore, less progress in the fruit ripening process. Low temperatures substantially reduce the rate of metabolic processes, leading to senescence, deterioration, and loss of quality. Temperate fruits such as quince and apple present a longer storage period at low temperatures as their physiological functions are already adapted to these growing conditions (Moradi et al., 2017). According Pio et al. (2005a) and Moradi et al. (2017), the postharvest physiology of quince fruits is not much studied due to the fact of low sensorial attributes (astringent taste) that not favors the in natura consumption, generally being suitable to the industrial processing.
INDUSTRIAL APPLICATION The use of quince fruit in the food industry is already widely used for the production of marmalades, jams, and jellies because of the high nutritional potential (Pio et al., 2005a). The highlight of the quince fruit is the high amount of pectin, which facilitates the production of the most varied sweets. Ferreira et al. (2004) evaluated the sensorial analysis of marmalades elaborated with 18 cultivars of quinces and classified the samples into two groups: one with typical flavor and aroma, attributed to texture with small granules with a shiny surface, in contrast to the other with intense aroma, but less typical, more acid and with more granular texture. Alvarenga et al. (2008) also reported through sensorial analysis there were significant differences in the marmalade elaborated with fruits of different cultivars, nevertheless the mixture of different samples revealed a greater potential of acceptance by the consumer. In agriculture, quince is commonly used as rootstock in apples, improving productivity and fruit quality, as well as being easily propagated (De Paula et al., 2015) and mucilage involving seeds can be used as a coating fruits such as gum arabic (Sharma et al., 2011). According to Sabir et al. (2015) the development of research with quince fruits allowed the identification of phytochemicals, mainly in leaves and fruit peels with promising potential for use in other areas through the development of herbal drugs. Recent research has shown the beneficial effect of extracts produced with quince leaves or peels in areas such as medicine through the control of diabetes mellitus (Aslan and Lu, 2010), in the reduction of cardiovascular complaints (Zhou et al., 2014 Abliz et al., 2014), respiratory (Romero et al., 2009; Minaiyan et al., 2012) and gastrointestinal problems (Ashrafi et al., 2012) and anticarcinogens (Carvalho et al., 2010). In the pharmacology, potential use was detected for microbial control (Fattouch et al., 2007; Silva Oliveira, 2013; De Bruim and Baars, 2001), and as an antiallergic in the control of asthma and rhinitis (De Bruim and Baars, 2001).
REFERENCES Abliz, A., Aji, Q., Abdusalam, E., Sun, X., Abdurahman, A., Zhou, W., et al., 2014. Effect of Cydonia oblonga Mill leaf extract on serum lipids and liver function in a rat model of hyperlipidaemia. J. Ethnopharmacol. 151 (2), 970-944.
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Alesiani, D., Canini, A., D’Abrosca, B., Dellagreca, M., Fiorentino, A., Mastellone, C., et al., 2010. Antioxidant and antiproliferative activities of phytochemicals from Quince (Cydonia vulgaris) peels. Food. Chem. 118, 199207. Alvarenga, A.A., Abraha˜o, E., Pio, R., Assis, F.A., Oliveira, N.C., 2008. Comparac¸a˜o entre doces produzidos a partir de frutos de diferentes espe´cies e cultivares de marmeleiro (Cydonia oblonga Miller e Chaenomeles sinensis Koehne). Cieˆnc. Agrotecnol. 32 (1), 302307. Alsnafi, A.E., 2016. The medical importance of Cydonia oblonga a review. J. Pharmacy 6 (2), 8799. Ashrafi, H., Ghabili, K., Hemmati, A.A., Jouyban, A., Shoja, M.M., Aslanabadi, S., et al., 2012. The effect of quince leaf (Cydonia oblonga Miller) decoction on testes in hypercholesterolemic rabbits: a pilot study. Afr. J. Tradit. Complement. Altern. Med. 10 (2), 277282. Aslan, S., Lu, H., 2010. On the sensitivity of ASL MRI in detecting regional differences in cerebral blood flow. Magn. Reson. Imaging 28 (7), 928935. Beinsan, C., Sumalan, R., Sumalan, R., 2015. Studies on postharvest quality of some quince genotypes. J. Hortic. For. Biotechnol. 19 (1), 193196. Benzarti, S., Hamdi, H., Lahmayer, I., Toumi, W., Kerkeni, A., Belkadhi, K., et al., 2015. Total phenolic compounds and antioxidant potential of quince (Cydonia oblonga Miller) leaf methanol extract. Int. J. Innov. Appl. Stud. 13 (3), 518526. Bettiol Neto, J.E., Pio, R., Sanches, J., Chagas, E.A., Cia, P., Chagas, P.C., et al., 2011. Produc¸a˜o e atributos de qualidade de cultivares de marmeleiro na regia˜o paulista. Rev. Bras. Frutic. 33 (3), 10351042. Carneiro, J.O., Souza, M.A.A., Rodrigues, Y.J.M., Apeli, A.M., 2015. Efeito da temperatura e do uso de embalagem na conservac¸a˜o po´s-colheita de frutos de cagaita (Eugenia dysenterica DC). Rev. Bras. Frutic. 37 (3), 568577. Available from: http://dx.doi.org/10.1590/0100-2945-157/14. Carvalho, M., Silva, B.M., Silva, R., Valenta˜o, P., Andrade, P.B., Bastos, M.L., 2010. First report on Cydonia oblonga Miller anticancer potential: differential antiproliferative effect against human kidney and colon cancer cells. J. Agric. Food Chem. 58 (6), 3663370. De Bruin D., Baars, E., 2001. Citrus/Cydonia comp. use in general practice. A survey among anthroposophic physicians. Driebergen: Louis Bolk Instituut, 31 p. De Paula, L.A., Rufato, A.R., Oliveira, P.R.D., Tallamini, M.R., 2015. Hibridac¸o˜es controladas inter e intraespecı´ficas para o melhoramento gene´tico de porta-enxertos de pereira. Rev. Bras. Frutic. 37 (3), 811818. Fachinello, J.C., Pasa, M.S., Schmtiz, J.D., Betemps, D.L., 2011. Situac¸a˜o e perspectivas da fruticultura de clima temperado no Brasil. Rev. Bras. Frutic. 33, 109120. Fattouch, S., Caboni, P., Coroneo, V., Tuberoso, C.I., Angioni, A., Dessi, S., 2007. Antimicrobial activity of Tunisian quince (Cydonia oblonga Miller) pulp and peel polyphenolic extracts. J. Agric. Food Chem. 55 (3), 963971. Ferreira, M.P.L.V.O., Pestana, N., Alves, M.R., Mota, F.J.M., Reu, C., Cunha, S., et al., 2004. Quince jam quality: microbiological, physicochemical and sensory evaluation. Food. Control. 15 (4), 291295. Fioravanc¸o, J.C., Simonetto, P.R., Grellmann, E.O., 2006. Comportamento fenolo´gico e produtivo de marmeleiros em Verano´polisRS. Cieˆnc. Agrotecnol. 30 (1), 1520. IBGE, Instituto Brasileiro de Geografia e Estatı´sticaIBGE. 2013. Produc¸a˜o agrı´cola: marmelo e peˆra. Available at: ,http://www.ibge.gov.br.. Imeh, U., Khokhar, S., 2002. Distribution of conjugated and free phenols in fruits: antioxidant activity and cultivar variations. J. Agric. Food. Chem. 50 (6), 301306. Kader, A.A., 1992. Postharvest Technology of Horticultural Crops, ed. DANR Pub. n . 3311, University of California, Oakland, CA. Leonel, M., Leonel, S., Tecchio, M.A., Mischan, M.M., Moura, M.F., Xavier, D., 2016. Characteristics of quince fruits cultivars’ (Cydonia oblonga Mill.) grown in Brazil. Aust. J. Crop Sci. 10 (5), 711716. Magalha˜es, A.S., Silva, B.M., Pereira, J.A., Andrade, P.B., Valenta˜o, P., Carvalho, M., 2009. Protective effect of quince (Cydonia oblonga Miller) fruit against oxidative hemolysis of human erythrocytes. Food Chem. Toxicol. 47, 13721377. Manica-Berto, R., 2009. Caracterizac¸a˜o fenolo´gica, fı´sico-quı´mica e fitoquı´mica de cultivares de marmeleiro. 70f. Tese (Doutorado em Agronomia). Faculdade de Agronomia Eliseu Maciel. Universidade Federal de Pelotas, Pelotas. Manica-Berto, R., Pegoraro, C., Mistura, C.C., Bresolin, P.S., Rufato, A.R., Fachinello, J.C., 2013. Similaridade gene´tica entre cultivares de marmeleiro avaliadas por marcadores AFLP. Pesqui. Agropecu. Bras. 48 (5), 568571. Mele´ndez-Ma´rtinez, A.J., Briton, G., Vicario, I.M., Heredia, F.J., 2007. Relationship between the colour and the chemical structure of carotenoides pigments. Food. Chem. 101, 11451150. Minaiyan, M., Ghannadi, A., Etemad, M., Mahzouni, P., 2012. A study of the effects of Cydonia oblonga Miller (Quince) on TNBS-induced ulcerative colitis in rats. Res. Pharmaceut. Sci. 7 (2), 103110. Mir, S.A., Waani, S.M., Ahmad, M., Wani, T.A., Gani, A., Mir, S.A., et al., 2015. Effect of packaging and storage on the physicochemical and antioxidant properties of quince candy. J. Food Sci. Technol. 23 (2), 816821. Mora, D.F., Cerdas, R.C., Marchena, L.A., Du´ran, A.S., Ulloa, C.A., 2015. Enraizamiento de vitroplantas de membrillo (Cydonia oblonga) por medio de inmersio´n temporal automatizada y su aclimatacio´n. Rev. Bras. Frutic. 37 (3), 739747. Moradi, S., Saba, M.K., Mozarafi, A.A., Abdollani, H., 2017. Physical and biochemical changes of some Iranian Quince (Cydonia oblonga Mill) genotypes during cold storage. J. Agric. Sci. Technol. 19, 377388. Oliveira, A.P., Pereira, J.A., Andrade, P.B., Valenta˜o, P., Seabra, R.M., Silva, B.M., 2007. Phenolic profile of Cydonia oblonga Miller leaves. J. Agric. Food Chem. 55, 79267930. Oliveira, A.P., Pereira, J.A., Andrade, P.B., Valenta˜o, P., Seabra, R.M., Silva, B.M., 2008. Organic acids composition of Cydonia oblonga Miller leaf. Food. Chem. 111, 393998. Pereira, G.M., Finger, F.L., Casali, V.W.D., Brommonschenkel, S.H., 2008. Influeˆncia do tratamento com etileno sobre o teor de so´lidos solu´veis e a cor de pimentas. Bragantia 67 (4), 10311036.
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Pio, R., Campo Dall’Orto, F.A., Alvarenga, A.A., Abraha˜o, E., Bueno, S.C.S., Maia, M.L., 2005. A Cultura do marmeleiro. ESALQ/USP, Piracicaba, 53p. (Boletim Te´cnico, 29). Pio, R., Campo Dall’Orto, F.A., Alvarenga, A.A., Abraha˜o, E., Bueno, S.C.S., Maia, M.L., et al., 2007a. Marmelo: do plantio a` marmelada. CATI, Campinas, 49p. (Boletim Te´cnico, 248). Pio, R., Dall’Orto, F.A.C., Alvarenga, A.A., Abraha˜o, E., Chagas, E.A., Sgnorini, G., 2007b. Propagac¸a˜o do marmeleiro ‘Japoneˆs’ por estaquia e alporquia realizadas em diferentes e´pocas. Cieˆnc. Agrotecnol. 31 (2), 570574. Pio, R., Chagas, E.A., Barbosa, W., Signorini, G., Entelmann, F.A., Fioravanc¸o, J.C., et al., 2008. Desenvolvimento de 31 cultivares de marmeleiro enxertadas no porta-enxerto ‘Japoneˆs’. Rev. Bras. Frutic. 30 (2), 466470. Postman, J., 2009. Cydonia oblonga: The unappreciated quince. Arnoldia 67 (1), 29. Prill, M.A.S., Neves, L.C., Tosin, J.M., Chagas, E.A., 2012. Atmosfera modificada e controle de etileno para bananas ‘prata-ana˜’ cultivadas na amazoˆnia setentrional. Rev. Bras. Frutic. 34 (4), 9901003. Remorini, D., Tavarini, S., Degl’Innocenti, E., Loreti, F., Massari, R., Guidi, L., 2008. Effect of rootstocks and harvesting time on the nutritional quality of peel and flesh of peach fruits. Food. Chem. 110, 361367. Romero, M.A., Da´valos, H.N., Astudillo-Va´zquez, A., 2009. Activated gastrointestinal del fruto de Cydonia oblonga Miller. Rev. Latinoam. Quı´m. 37 (2), 115121. Sabir, S., Qureshi, R., Arshad, M., Shoaib, M., Amjad, B., Fatima, S., et al., 2015. Pharmacognostic and clinical aspects of Cydonia oblonga: a review. Asian Pac. J. Trop. Dis. 5 (11), 850855. Seifert, K.E., Pio, R., Celant, V.M., Chagas, E.A., 2009. Mudas de pera produzidas por dupla enxertia em marmeleiro utilizando o porta-enxerto ‘Japoneˆs’. Pesqui. Agropecu. Bras. 44 (12), 16311635. Sharma, R., Joshi, V.K., Rana, J.C., 2011. Nutritional composition and processed products of quince (Cydonia oblonga Mill). Indian J. Nat. Prod. Resour. 2, 354359. Silva, B.M., Andrade, P.B., Martins, R.C., Seabra, R.M., Ferreira, M.A., 2006. Principal component analysis as tool of characterization of quince (Cydonia oblonga Miller) jam. Food. Chem. 94 (4), 504512. Silva, F.G., Oliveira, G.L., 2013. Conhecimento popular e atividade antimicrobiana de Cydonia oblonga Miller (Rosaceae. Rev. Bras. Plant. Med. 15 (1), 98103. Souci, S.W., Fachmann, W., Kraut, H., 2008. Food composition and nutrition tables, MedPharm Scientific Publisshers, seventh revised ed. Taylor & Francis, A CRC Press Book, Routledge, London, United Kingdom, 1364 p. Thomidis, T., Tsipouridis, C., Isaakidis, A., Michailides, Z., 2004. Documentation of field and postharvest performance for a mature collection of quince (Cydonia oblonga) varieties in Imathia, Greece, New Zealand. J. Crop Hortic. Sci. 32 (10), 243247. USDA, 2009. Germplasm Resources Information Network-(GRIN). National Germplasm ResourcesLaboratory, Beltsville, Maryland 2009. Available at: ,http://www.ars-grin.gov/cgi-bin/npgs/html/taxon.pl112779., 2009. Wertheim, S.J., 2002. Rootstocks for European pear: a Review. Acta. Hortic. 596, 299309. Zambon, C.R., Silva, L.F.O., Pio, R., Figueiredo, M.A., Silva, K.N., 2014. Estabelecimento de meio de cultura e quantificac¸a˜o da germinac¸a˜o de gra˜os de po´len de cultivares de marmeleiro. Rev. Bras. Frutic. 36 (2), 400407. Zhou, W., Abdusalam, E., Abliz, P., Reyim, N., Tian, S., Aji, Q., et al., 2014. Effect of Cydonia oblonga Mill fruit and leaf extracts on blood pressure and blood rheology in renal hypertensive rats. J. Ethnopharmacol. 152 (3), 464469.
FURTHER READING Essafi-Benkhadir, K., Refai, A., Riahi, I., Fattouch, S., Karoui, H., Essafi, M., 2012. Quince (Cydonia oblonga Miller) peel polyphenols modulate LPS-induced inflammation in human THP-1-derived macrophages through and Akt inhibition. Biochem. Biophys. Res. Commun. 418 (1), 180185. Simo˜es, C.M.O., Schenkel, E.P., Gosmann, G., Mello, J.C.P., Mentz, L.A., Petrovick, P.R., 2007. Farmacognosia: da planta ao medicamento. 6.ed. Porto Alegre: Editora da UFRGS; Floriano´polis: Editora da UFSC, 1104p.
Rambuta˜n—Nephelium lappaceum Wen Li, Jiaoke Zeng and Yuanzhi Shao Hainan University, Hai Kou, People’s Republic of China
Chapter Outline Origin and Botanical Aspects Origin Morphological Characteristics Cultivars and Harvest Season Cultivation Propagation Growing Behavior and Management Sensory Characteristics Chemical Composition and Nutritional Value Nutritional Component
369 369 369 370 371 371 371 371 371 371
Antioxidant Compounds Polyamine Harvest and Postharvest Conservation Harvest and Postharvest Physiology Postharvest Conservation Industrial Applications Peel Application Seed Application References Further Reading
371 372 372 372 373 373 373 374 374 375
ORIGIN AND BOTANICAL ASPECTS Origin Rambutan (Nephelium lappaceum Linn.) is an exotic fruit closely related to the lychee and longan in the Sapindaceae family. Rambutan originated in the Malaysian2Indonesian region, and has been widely cultivated in southeast Asia areas such as Thailand, Sri Lanka, Malaysia, Indonesia, Singapore, and the Philippines (Tindall et al., 1994). Rambutan is also widely cultivated in Hawaii and Australia. In China, the Taiwan and Hainan provinces have planted a large area of the species, but wild rambutan is found in Sipsongpanna in the Yunnan province.
Morphological Characteristics Rambutan is an evergreen tree growing to a height of 10 m. The branchlet is cylinder-shaped, wrinkled and graybrown, and the twigs are puberulous. The length of leaf and petiole are 1545 cm together, rhachis present as a bit thick. The shape of leaf blade is pinnate, with one to four pair of leaflets, each leaflet is 618 cm long, 47.5 cm wide, elliptic or obovate in shape, and with an entire margin. The leaflet tips are obtuse rounded, slightly orbicular or lanceolate in shape. The base of leaflet is wedge-shaped. The leaf blades have 79 pair of maroon lateral veins, with a bulging back and scrobiculate small vein. The length of petiolule is 5 mm long. The inflorescence contains many branches; the length are almost isometric with leaves, it is covered with rusty short puberulous (see Fig. 1). The peduncles are short. The leathery calyx is about 2 mm long, with ovate shape and puberulous trait. The flower are apetalous, the stamen length is about 3 mm long. Rambutan anthesis is in early Summer. Rambutan fruit are an oval or globose berry, the length of fruit is about 5 cm, the width is 45 cm and they grow in clusters of 1018. The term rambutan is derived from the Malay word “hair”, which describes the reddish or yellow fleshy pliable spinelike protuberances (spinterns), the hair-like spintern length is about 1 cm. The fruit flesh is actually aril, it is translucent and whitish. The seed is brown, length 11.3 cm, with a white basal scar. Rambutan fruits in early fall. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00048-4 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Leaf blade and flower of rambutan.
FIGURE 2 Red rambutan fruit and yellow rambutan fruit.
CULTIVARS AND HARVEST SEASON Rambutan is usually sorted into two groups according to the peel color: red and yellow fruit (Fig. 2). Over 200 cultivars were developed throughout tropical Asia. In the ASEAN region, the general planting cultivars are “R134”, “Muar Gading”, “Oh Heok”, “Chai Tow Cheng”, “Binjai”, “Jitlee” and “Rongrien” in Australia, whereas in Hawaii, cvs. “Binjai”, “Jitlee” and “Rongrien” are preferred. In Singapore, cvs. “Deli cheng” and “Jitlee” are the variety of choice. In Malaysia, “R134”, “Gula Batu”, “Muar Gading”, “Khaw Tow Bak”, “Lee Long”, and “Oh Heok” are widely grown. In Indonesia, “Lebakbulus”, “Binjai”, “Simacan”, and “Rapiah” are preferred. In the Philippines, “Seematjan”, “Seenjonja”, and “Mahalika” cultivars are preferred. In Thailand, “Rongrien”, “Seechompoo”, and “Bangyeekhan” are popular varieties (Pohlan et al., 2008; Kawabata et al., 2007). In China, in the Hainan province, six varieties were cultivated and identified as being good quality, named “Baoyan No.1”, “Baoyan No. 2”, “Baoyan No. 3”, “Baoyan No. 4”, “Baoyan No. 5”, and “Baoyan No. 7”. Within these, “Baoyan No. 2” is yellow oval fruit, “Baoyan Nos. 1, 3, 4” are red oval fruit, “Baoyan Nos. 5, 7” are red round fruit.
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Moreover, “Baoyan No. 7” fruit have higher yield, can bear fruit twice each year, it has a higher stable yield, chilling tolerance, and drought tolerance characteristics. Rambutan usually flowers from February to April, and the fruit ripens from June to August. It is approximately 110 days from fruit set to harvest. A 20-year-old mature tree may produce 100125 kg or more fruit. The skin and spine coloration is the main maturity index of rambutan. Other features such as flavor, taste, physical properties, and fruit weight are all considered to be the determination of maturity (Lye et al., 1987). Ripe fruit have both skin and spines that are red or yellow, depending on the variety.
CULTIVATION Propagation Rambutan is propagated by seedling propagation and vegetative propagation. It can be divided into male, female, and hermaphroditic. Most commercial cultivars are hermaphroditic, cultivars that produce only functionally female flowers requires the presence of male trees. But as the proporation of male trees are only 34.2%, and seldom found, it is adverse to regionalization of fruit tree. Vegetative propagation is most commonly used in production, and rambutan often propagated by grafting and air layering.
Growing Behavior and Management Rambutan is a tropical fruit tree adapted to tropical climate which is characterized by high rainfall, low evaporation rates, and high humidity in low altitude mountainous environment, with average annual temperature of 24 C and 20003000 mm of distributed rainfall. Under these conditions, rambutan thrives well and produces good quality fruit. Seedling stage plants are not drought tolerant, they require good irrigation during fruit development stage. The rambutan tree prefers deep soil, clay loam, or sandy loam rich in organic matter for good drainage and ventilation. The best soil has pH of 4.56.5 and high fertility. On alkaline soils, micronutrient problems often develop. Trees should be planted with 1013 m distances with wind protection. Low relative humidity during fruiting could cause fruit spinterns to have moisture loss and result in poor fruit appearance. Rambutan trees exhibit apical dominance and have a tendency to produce upright growth; early pruning is needed to form an open center shape tree. A mature tree will grow slowly, shooting occuring three or four times a year.
SENSORY CHARACTERISTICS Rambutan fruit is bright red or yellow oval fruit. It is about the size of small hen’s egg with a seed, hairy peel with long, soft spines, edible aril with the texture of juicy, translucent aril and a sweet taste with an acid pulp (Fig. 3).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Nutritional Component Rambutan is rich in vitamins, amino acids, carbohydrates, and a variety of minerals. The edible rate is about 31% 60.2%, and the total soluble solid is about 14%22.2%; the fruit is rich in glucose and sucrose.The citric acid content is about 0.39%1.53%, and the content of vitamin C is about 0.635.5mg/100 g flesh (Pe´rez and Pohlan, 2005).
Antioxidant Compounds The bioactive metabolites include polyphenols, flavonoids, flavanols, tannins, ascorbic acid, anthocyanins, and volatile compounds. The accumulation of phenolic compounds in rambutan peels can increase with the growth of fruit, and reach a maximum of 7331653 mg per fruit at the time of being harvested. The accumulation of ellagic acid, corilagin, and geraniin in the peels increased and reached the maximum at the harvest stage. Geraniin has the potential to be developed into an antihyperglycemic agent(Palanisamy et al., 2011).The major component in the rambutan peels of Rongiren and Seechompoo cultivars was geraniin, the constituent of geraniin could reach 4441011 mg/fruit (Thitilertdecha and Rakariyatham, 2011). Peel extract of rambutan exhibited an extremely high value of IC50 (.100 μg/mL) against both cell types indicating nontoxic activity to the cells (Okonogi et al., 2007). Peel extracts exhibited antibacterial activity against five pathogenic
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FIGURE 3 Sensory characteristics of rambutan fruit.
bacteria. The most sensitive strain, Staphylococcus epidermidis, was inhibited by the methanolic extract (MIC 2.0 mg/mL) (Thitilertdecha et al., 2008). Additionally, peel extract of rambutan has the effect of decreasing blood glucose levels for up to 61.76% 6 4.26% (Muhtadi et al., 2015; Leong and Shui, 2002). Over 100 volatile compounds from the red-skinned cultivar of rambutan were detected by GC/MS. Sixty compounds in the extracts had some odor activity. β-damascenone, ethyl 2-methylbutyrate, 2,6-nonadienal, (E)-2-nonenal, and nonanal were detected as the main compounds among the fruit aroma (Ong et al., 1998). All these data indicated that the peel of rambutan may be considered potentially useful as a source of natural antioxidants for food or drug products because of its high antioxidant activity and nontoxic property to normal cells.
Polyamine Polyamine concentrations were measured in skin, pulp, and seeds of the late harvest cultivar ‘Rongrien’ and the early harvest cultivar ‘Seechompoo’ rambutan fruit. Putrescine (Put) was the major polyamine in the skin, pulp, and seeds of rambutan. The Put was much higher in the pulp than in the skin. These results suggested that Put concentration may be associated with the fruit growth of rambutan (Kondo et al., 2001).
HARVEST AND POSTHARVEST CONSERVATION Harvest and Postharvest Physiology Rambutans are harvested when the fruit have reached optimum visual and organoleptic quality. The fruit are nonclimacteric with little change in total soluble solids or titratable acidity after harvest. Rambutans are exotic tropical fruit with a relatively short shelf life, the fruit browning and decay could occur during 1 to 3 days after harvest and during the storage and transportation. Fresh rambutans are bright red or yellow at harvest, but the peel color and spinterns darken during storage, the browning has close relationship with higher activities of PPO and POD in spinterns (Wall et al., 2011; Yingsanga et al., 2008). Another postharvest physiology for rambutan is chilling injury (CI). Rambutan fruit suffers obvious chilling injury, expressed as an increase in fruit browning and rot. When stored at 8 C or 13 C, chilling injury was detected in the skin of fruit stored 4 days or more at 8 C, and the CI index increased with days of storage (Kondo et al., 2001). Postharvest diseases also limit the successful marketing and export of rambutan fruit (Wall et al., 2011).
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Postharvest Conservation Browning and Disease Control Pericarp browning can be delayed when the fruit are held at 8 C12 C and 95% relative humidity, depending on cultivars. Color deterioration can be retarded (three or four days) by storage under enhanced carbon dioxide atmospheres (9%12%) (O’Hare, 1995). Sulfur dioxide exposure prior to disinfestation treatment resulted in less browning that helped to maintain fruit quality (Paull et al., 1995). The development of browning was preceded by water loss and concomitant declines in water potential of spinterns and skin. There was a strong negative correlation between water potential and browning such that as browning score increased, water potential declined (Landrigan et al., 1996). Rambutan fruits have relatively short storage and shelf life, mostly because of losses to postharvest diseases caused by pathogenic fungi. Cinnamaldehyde (30 ppm) impregnated blotting sheets were used in commercial packaging; incidence and severity of all three postharvest diseases decreased. Treated fruits retained color, overall quality and sensory characteristics at 13.5 C and 95% RH for 14 days (Sivakumara et al., 2002).
Postharvest Handling and Storage Condition Rambutans rapidly deteriorate unless proper handling techniques are employed. Packing materials have a significant impact on storage quality and shelf life of rambutan fruit. Under 10 C, antimoisture polyethylenes bag had the beneficial effects on rambutan fruit quality, however, when fruit was stored at 25 C, packing with regular low density polyethylene proved to be better than that with antimoisture polyethylene bags (Shao et al., 2013). The use of modified atmosphere packaging or enhanced CO2 atmospheres (9%12%) can also maintain the visual quality of rambutans (Wall et al., 2011). To summarise, the suitable condition for rambutan fruit is: 95% relative humidity,7 C10 C storage temperature. Besides this, integrated preharvest and postharvest practices that achieve disease control while reducing desiccation and browning are needed to extend rambutan shelf life beyond two weeks (Wall et al., 2011).
INDUSTRIAL APPLICATIONS Peel Application Antioxidant Agents, Medicine, and Food Industry Fruit peel extracts from rambutan had antioxidant activity and cytotoxicity against human cell lines. The ethyl acetate fraction of rambutan peel is a promising resource for potential novel antioxidant agents whereas the hexane fraction of coconut peel may contain novel anticancer compounds (Khonkarn et al., 2010; Prakash Maran et al., 2013) The methanolic extract of rambutan peels exhibited strong antioxidant properties. The isolated ellagitannins could be further utilized as both a medicine and in the food industry (Thitilertdecha et al., 2008; Dembitsky et al., 2011).
Preparation of Activated Carbons A novel agricultural waste, rambutan peel was used as the precursor for preparation of activated carbon by chemical assisted KOH activation. Microwave heating was employed for activation, and thereby considerably reduced the activation time. The maximum monolayer adsorption capacity of acid yellow 17 (AY 17) was 215.05 mg/g (Njoku et al., 2014; Ahmad and Alrozi, 2011).
Green Synthesis of Nickel Oxide Nanocrystals and Zinc Oxide Nanocrystals From Rambutan Peel Green synthesis of NiO nanocrystals was carried out via nickelellagate complex formation using rambutan wastes. Successful formation of NiO nanocrystals was confirmed (Yuvakkumar et al., 2014b). Yuvakkumar et al. (2014b) reported a sustainable novel green synthetic strategy to synthesize zinc oxide nanocrystals. This is the first report on sustainable biosynthesis of zinc oxide nanocrystals employing rambutan peel extract as a natural ligation agent. Green synthesis of zinc oxide nanocrystals was carried out via zincellagate complex formation using rambutan peel wastes. ZnO nanocrystal-coated cotton showed good antibacterial activity towards Escherichia coli (E. coli), gram negative bacteria and Staphylococcus aureus (S. aureus), gram positive bacteria (Yuvakkumar et al., 2014a, 2015).
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Inhibiting Body Weight Gain Rambutan peel extract (RPE) treatment had obvious effects on physiological characteristics and genes expression of obesity rat model. RPE have antiobesity activity by inhibiting body weight gain, declining size of adipocyte, decreasing triglyceride, decreasing the expression of PPARγ, mRNA level of FABP4 gene (Lestari et al., 2015), and decreasing the expression of Igf-1 and Igf-1R of an obese rat model (Lestari et al., 2014).
Seed Application Antibacterial Activity Bhatand Al-daihan (2014) investigated the seeds’ aqueous extracts for antibacterial activity by disc diffusion method and protein profile from rambutan. Both seed aqueous extracts show moderate inhibition against pathogenic bacteria, both gram positive including Staphylococcus aureus, Streptococcus pyogenes, and Bacilllus subtillis and gram negative bacteria including Escherichia coli and Pseudomonas aeruginosa. The analysis of the antibacterial activity of tested samples revealed that the highest inhibitory activity was produced by rambutan seed.
Seed Fat Composition The chemical composition, the main physicochemical properties, phase behavior and thermal stability of rambutan seed fat were studied by some researchers (Solı´s-Fuentes et al., 2010; Sirisompong et al., 2011). The results showed that the almond-like decorticated seed represents 6.1% of the wet weight fruit and is: 1.22% ash, 7.80% protein, 11.6% crude fiber, 46% carbohydrates, and 33.4% fat (d.b.). The main fatty acids in the drupe fat were 40.3% oleic, 34.5% arachidic, 6.1% palmitic, 7.1% stearic, 6.3% gondoic, and 2.9% behenic. Rambutan seed fat has physicochemical and thermal characteristics that may become interesting for specific applications in several segments of the food industry.
REFERENCES Ahmad, M.A., Alrozi, R., 2011. Optimization of rambutan peel based activated carbon preparation conditions for Remazol Brilliant Blue R removal. Chem. Eng. J. 168, 280285. Bhat, R.S., Al-daihan, S., 2014. Antimicrobial activity of Litchi chinensis and Nephelium lappaceum aqueous seed extracts against some pathogenic bacterial strains. J. King Saud Univers. Sci. 26, 7982. Dembitsky, V.M., Poovarodom, S., Leontowicz, H., Leontowicz, M., Vearasilp, S., Trakhtenberg, S., et al., 2011. The multiple nutrition properties of some exotic fruits: Biological activity andactive metabolites. Food Res. Int. 44, 16711701. Kawabata, A.M., Nagao, M.A., Tsumura, T., Aoki, D.F., Hara, K.Y., Pena, L.K., 2007. Phenology and fruit development of Rambutan (Nephelium lappaceum L.) grown in Hawai’i. J. Hawai. Pac. Agric. 14, 3139. Khonkarn, R., Okonogi, S., Ampasavate, C., Anuchapreeda, S., 2010. Investigation of fruit peel extracts as sources for compounds with antioxidant and antiproliferative activities against human cell lines. Food Chem. Toxicol. 48, 21222129. Kondo, S., Posuya, P., Kanlayanarat, S., 2001. Changes in physical characteristics and polyamines during maturation and storage of rambutans. Sci. Hortic. (Amsterdam) 91, 101109. Landrigan, M., Morris, S.C., Eamus, D., McGlasson, W.B., 1996. Postharvest water relationships and tissue browning of rambutan fruit. Sci. Hortic. (Amsterdam) 66, 201208. Leong, L.P., Shui, G., 2002. An investigation of antioxidant capacity of fruits in Singapore markets. Food Chem. 76, 6975. Lestari, S.R., Djati, M.S., Rudijanto, A., Fatchiyah, F., 2014. The physiological response of obese rat model with rambutan peel extract treatment. Asian Pac. J. Trop. Dis. 4, 780785. Lestari, S.R., Djati, M.S., Rudijanto, A., Fatchiyah, F., 2015. PPARγ expression by rambutan peel extract in obesity rat model-induced high-calorie diet. Asian Pac. J. Trop. Biomed. 5, 852857. Lye, T.T., Laksmi, L.D.S., Maspol, P., Yong, S.K., 1987. Commercial rambutan cultivars in ASEAN. In: Lam, P.F., Kosiyachinda, S. (Eds.), Rambutan Fruit Development Postharvest Physiology & Marketing in Asean. ASEAN Food Handling Bureau, Malaysia, pp. 915. Muhtadi, Primarianti, A.U., Sujono, T.A., 2015. Antidiabetic activity of durian (Duriozibethinus Murr.) and rambutan (Nephelium lappaceum L.) fruit peels in alloxan diabetic rats. Proc. Food Sci. 3, 255261. Njoku, V.O., Foo, K.Y., Asif, M., Hameed, B.H., 2014. Preparation of activated carbons from rambutan (Nephelium lappaceum) peel by microwaveinduced KOH activation for acid yellow 17 dye adsorption. Chem. Eng. J. 250, 198204. O’Hare, T.J., 1995. Postharvest physiology and storage of rambutan. Postharvest. Biol. Technol. 6, 189199. Okonogi, S., Duangrat, C., Anuchpreeda, S., Tachakittirungrod, S., Chowwanapoonpohn, S., 2007. Comparison of antioxidant capacities and cytotoxicities of certain fruit peels. Food Chem. 103, 839846. Ong, P.K.C., Acree, T.E., Lavin, E.H., 1998. Characterization of Volatiles in Rambutan Fruit (Nephelium lappaceum L.). J. Agric. Food Chem. 46, 611615.
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Palanisamy, U.D., Ling, L.T., Manaharan, T., Appleton, D., 2011. Rapid isolation of geraniin from Nephelium lappaceum rind waste and its antihyperglycemic activity. Food. Chem. 127, 2127. Paull, R.E., Reyes, M.E.Q., Reyes, M.U., 1995. Litchi and rambutan insect disinfestation: treatments to minimize induced pericarp browning. Postharvest Biol. Technol. 6, 139148. Pe´rez, R.A., Pohlan, J., 2005. Rambutan fruits (Nephelium lapaceum L.) are no hosts for fruit flies: Anastrepha spp. y Ceratitis capitata (Wied.) results of 10 years in the Soconusco, Chiapas, Mexico. J. Agric. Rural Dev. Trop. Subtrop. 106, 143154. Pohlan, J., Vanderlinden, E.J.M., Janssens, M.J.J., 2008. Harvest maturity, harvesting and field handling of rambutan. Stewart Postharvest Rev. 2, 11. Prakash Maran, J., Manikandan, S., Vigna Nivetha, C., Dinesh, R., 2013. Ultrasound assisted extraction of bioactive compounds from Nephelium lappaceum L. fruit peel using central composite face centered response surface design. Arab. J. Chem. Available from: http://dx.doi.org/10.1016/j. arabjc.2013.02.007. Shao, Y.Z., Xie, J.H., Chen, P., Li, wen, 2013. Changes in some chemical components and in the physiologyof rambutan fruit (Nephelium lappaceum L.) as affectedby storage temperature and packing material. Fruits 68, 1524. Sirisompong, W., Jirapakkul, W., Klinkesorn, U., 2011. Response surface optimization and characteristics of rambutan (Nephelium lappaceum L.) kernel fat by hexane extraction. LWT-Food Sci. Technol. 44, 19461951. Sivakumara, D., Wijeratnama, R.S.W., Wijesunderab, R.L.C., Abeyesekerea, M., 2002. Control of postharvest diseases of rambutan using cinnamaldehyde. Crop Prot. 21, 847852. Solı´s-Fuentes, J.A., Camey-Ortı´z, G., Herna´ndez-Medel, M.D.R., Pe´rez-Mendoza, F., Dura´n-de-Bazu´a, C., 2010. Composition, phase behavior and thermal stability of natural edible fat from rambutan (Nephelium lappaceum L.) seed. Bioresour. Technol. 101, 799803. Thitilertdechaa, N., Rakariyatham, N., 2011. Phenolic content and free radical scavenging activities in rambutan during fruitmaturation. Sci. Hortic. (Amsterdam) 129, 247252. Thitilertdecha, N., Teerawutgulrag, A., Rakariyatham, N., 2008. Antioxidant and antibacterial activities of Nephelium lappaceum L. extracts. LWTFood Sci. Technol. 41, 20292035. Tindall, H.D., Menini, U.G., Hodder, A.J., 1994. Rambutan Cultivation. FAO Plant Production and Protection Paper, Italy. Wall, M.M., Sivakumar, D., Korsten, L., 2011. 15-Rambutan (Nephelium lappaceum L.). In: Yahia, E. (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruits: Mangosteen to White Sapote. Food Science, Technology and Nutrition, USA, pp. 312333. Yingsanga, P., Srilaong, V., Kanlayanarat, S., Noichindab, S., McGlasson, W.B., 2008. Relationship between browning and related enzymes (PAL, PPO and POD) in rambutan fruit (Nephelium lappaceum Linn.) cvs. Rongrien and See-Chompoo. Postharvest. Biol. Technol. 50, 164168. Yuvakkumar, R., Suresh, J., Nathanael, A.J., Sundrarajan, M., Hong, S.L., 2014a. Novel green synthetic strategy to prepare ZnO nanocrystals using rambutan (Nephelium lappaceum L.) peel extract and itsantibacterial applications. Mater. Sci. Eng. C. 41, 1727. Yuvakkumar, R., Suresh, J., JosephNathanael, A., Sundrarajan, M., Hong, S.I., 2014b. Rambutan (Nephelium lappaceum L.) peelextract assisted biomimetic synthesis of nickel oxide nano crystals. Mater. Lett. 128, 170174. Yuvakkumar, R., Suresh, J., Saravanakumar, B., Nathanael, A.J., Hong, S.I., Rajendran, V., 2015. Rambutan peels promoted biomimetic synthesis of bioinspired zinc oxide nanochains for biomedical applications. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 137, 250258.
FURTHER READING O’Hare, T.J., Prasad, A., Cooke, A.W., 1994. Low temperature and controlled atmosphere storage of rambutan. Postharvest Biol. Technol. 4, 147157.
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Safou—Dacryodes edulis Sueli Rodrigues1, Edy Sousa de Brito2 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Cultivar Origin and Botanic Aspects Chemical Composition and Nutritional Value Sensory Aspects
377 377 378
Harvest Season, Postharvest Conservation, Physiology, and Biochemistry Industrial Application or Potential Industrial Application References
380 380 381
CULTIVAR ORIGIN AND BOTANIC ASPECTS Dacryodes species are evergreen; perennial trees belong to the family Buseraseae. Safou Dacryodes edulis, also known as native pear, butterfruit, Ube and Eleme, African Pear or African Plum, is an oliferous fruit tree found in equatorial and humid tropic climates (Anegbeh et al., 2005). The plant originates from central Africa and the Gulf of Guinea and spreads nearly all over the western coast of Africa. The plant is easily planted and found in many parts of Cameroon. Safou has a long history of cultivation in Africa because of its fruits (Daly and Martı´nez-Habibe, 2016). Its natural range extends from southern Nigeria to western Cameroon, and it is found in farmlands in Cameroon, Gabon, Democratic Republic of Congo, Central African Republic, Republic of the Congo, and Equatorial Guinea. This wide range is due to the anthropogenic transfer of planting material (Leakey et al., 2002). The plant is found in home gardens and cocoa farms in Cameroon. In Nigeria, Safou trees are predominantly planted in the compound farm and crop fields (Anegbeh et al., 2005). The cultivated tree reaches about 810 m high, and its multiplication by seed has resulted in a heterogeneous population. Safou tree is a recalcitrant species to vegetative propagation due to the low vitality of its vegetative organs (Ayuk et al., 1999). Increasingly, the species is becoming commercially important. The safou tree is presented in Fig. 1. Although the tree is typically propagated by seed, marcotting (air layering) propagation can be used as well (Mialoundama et al., 2002). Safou plays an important role in alleviating the threats to food security caused by human activities that affect the balance of nature. Safou is an agroforestry tree that benefits people of west and central Africa who are poor and malnourished. As the demand for fruits and other nonwood forest products are increasing, the indigenous fruits from Nigeria’s forests is threatened by increasing deforestation. For rural families, the increasing fruit demand is an opportunity. Small farmers can take part in the development of agroforest technologies and contribute to the selection of the cultivars to be multiplied and planted (Tchoundjeu et al., 2002). Dacryodes edulis trees are also important for the provision of shade (Ayuk et al., 1999)
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE The mesocarp is the edible part of the fruit with a pulp rich in fatty acids, amino acids, and vitamins. The tree is also used as an oil source for the cosmetic and food industries, and the branches are used as firewood. The plant also provides shade for humans, food and other crops (Ayuk et al., 1999). The safou fruit is presented in Fig. 2. The fruits, rich in mineral, vitamins, lipids, vitamins, proteins, and carbohydrate are important for the human diet in west and central Africa (Mbofung et al., 2002). The fruit protein content is higher than that found in maize (10%), rice (8%), sorghum (11%), and wheat (8%13%). The kernels are suitable for use as animal feed. The extracts obtained Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00050-2 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Safou tree.
FIGURE 2 Safou fruit.
from the leaf, fruit and resin present antioxidant, antimicrobial, and anticarcinogenic properties. Safou is also rich in polyphenols, anthocyanins and antioxidant activity (Tee et al., 2014). Tables 1 and 2 present the fruit composition.
SENSORY ASPECTS Pulp samples of untreated, boiled and roasted safou fruits from Cameroon were olfactometrically evaluated by professional perfumers. The aroma characteristics are described below: Untreated pulp: pleasant warm-woody-balsamic (pinene-like), fresh-fruity (citrus-like), sweet-fruity (direction of ripe plum), weak minty-floral and in the background fatty and spicy aroma.
Safou—Dacryodes edulis
TABLE 1 Safou (Dacryodes edulis) Composition Component
Safou Fruit
Safou Pulp
Moisture
44.9%63.1%
12%53%
Protein
3.5%7.3%
4.3%25.9%
Carbohydrate
9.5%11.3%
13.5%38%
Lipid
21.0%72.6%
32%44%
Ash
1.4%4.2%
2%10.8%
Dietary Fiber
1.0%3.1%
2.7%17.9%
Potassium
4432000 mg/100 g
1.12380 mg/100 g
Sodium
0.860 mg/100 g
80375 mg/100 g
Calcium
50690 mg/100 g
0.2690 mg/100 g
Phosphorus
30 mg/100 g
220 mg/100 g
Magnesium
47190 mg/100 g
0.5450 mg/100 g
Iron
1.780 mg/100 g
1.5 mg/100 g
Cooper
0.5 mg/100 g
6.4 mg/100 g
Zinc
0.5 mg/100 g
0.9 mg/100 g
Vitamin C
19.524.5 mg/100 g
22.5164.8 mg/100 g
Vitamin B3
ND
17.3 mg/100 g
Vitamin B6
ND
33.9 mg/100 g
ND, not detected. Adapted from Tee, L.H., Yang, B., Nagendra, K.P., Ramanan, R.N., Sun, J., Chan, E.S., et al., 2014. Nutritional compositions and bioactivities of Dacryodes species: a review. Food Chem. 165, 247255.
TABLE 2 Safou (Dacryodes edulis) Oil Composition in % Dry Weight Basis Component
Safou Fruit
Safou Seeds
Saturated Oil C14:0
014
C16:0
7.247.9
43.261.9
C18:0
2.112.9
4.6
C20:0
0.2
11.6
C16:1
0.10.2
C18:1
2236
18.322.0
Monosaturated Oil
Polyunsaturated Oil C18:2
1624.9
12.619.0
C18:3
0329.1
Saturated fatty acid
24.1.50.9
59.461.9
Unsaturated fatty acid
4775.9
34.637.3
, unknown Adapted from Tee, L.H., Yang, B., Nagendra, K.P., Ramanan, R.N., Sun, J., Chan, E.S., et al., 2014. Nutritional compositions and bioactivities of Dacryodes species: a review. Food Chem. 165, 247255.
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Pulp after boiling: allium-like top-note, sweet-woody (pinene-like), limonene-note, fresh-spicy (camphoraceous and minty note) and green-fatty aroma-notes, spicy and woody. Pulp after roasting: allium-like and green-fatty notes, sweet-woody-balsamic (pinene-like), fresh-limonene-note and weak minty-floral side notes. According to Jirovetz et al. (2003), about 50 volatile compounds were detected, and more than 40 of them were identified in the pulp headspace of untreated, boiled, and roasted fruit from Cameroon. The following main compounds (concentration higher than 3.0%, calculated as percent relative peak area of GC/FID analysis using an apolar RSL-200 column) of the three HS-SPME of safou pulp samples were found: Untreated fruit: a-pinene (20.3%), myrcene (15.0%), b-pinene (8.2%), and limonene (3.6%) Boiled fruits: a-pinene (44.9%), b-pinene (21.1%), myrcene (7.3%), limonene (6.3%), hexanal (4.6%), dimethyl sulfide (4.1%), and sabinene (3.8%) Roasted fruits: a-pinene (37.1%), myrcene (20.9%), b-pinene (16.2%), hexanal (8.1%), dimethyl sulfide (7.0%), and limonene (3.4%)
HARVEST SEASON, POSTHARVEST CONSERVATION, PHYSIOLOGY, AND BIOCHEMISTRY The safou fruits ripen in the rainy season (MayNovember) and are harvested when they change color from whitishgreen to pink or dark bluepurpleblack. The fruits present a relatively short shelf-life when raw. The shelf life can be prolonged by drying using traditional methods. In Cameroon, the fruit are typically roasted while in Nigeria, the fruits are usually boiled in salted water (Anegbeh et al., 2005). The fruit is also prepared as jams and jellies. The fruit oil is extracted for use in margarine, soap, and other industrial products (Sonwa et al., 2002). The safou pulp softens from 28 C to 80 C by the action of endogenous enzymes (cellulase, pectinesterase, and polygalacturonase), as reported by Leenhouts et al. (1952). At 28 C30 C, the fruit wrapped in paper or polyethylene bags may be stored satisfactorily for 38 days. The shelf-life was increased at lower temperatures. At 15 C, fruits were of better quality and retained their firmness for 2 weeks. Storage in moist sawdust, wood shavings, or water was not efficient in extending shelf-life. Moreover, stability variation among fruit types during storage was observed (DzondoGadet et al., 2005).
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION In the fruit season, safou ensures a good dietetic food for African people. During the rest of the year, the interest in safou oils was demonstrated by nursing mothers for infant growth (Omoti and Okiy, 1987; Okafor, 1983). Recently, partial replacement of margarine by safou pulp was carried out as an ingredient in nutritious biscuits (Everham et al., 1996). The stability and the storage of safou oil were not studied for a long time. The safou oil stability can be used as a nutritional complement due to its lipid oxidation, a major problem in processing and storage of fats, oils and fatcontaining food (Kenmegne-Kandem, 1997). Encapsulation by entrapment of the oil in a matrix, which isolates the oil from the environment, has been studied as a way for long term preservation. Among the entrapment processes, the most commonly used are spray drying and freeze drying. However, due to the lower cost, spray drying is the most usual method (Dzondo-Gadet et al., 2005). The oil can be used in cosmetic and food industry but its composition depends on the fruit origin and ripening conditions. The oil can be extracted by several methods using solvents or enzymes. The level of safou oil extracted by enzyme extraction using Viscozym L was 42%. With the solvent chloroform/methanol (2/1 v/v), the extraction level was 42.3%, and the Soxhlet resulted in 47% of extracted oil. The characteristic oil parameters, iodine, acidic, and peroxide values, were low (79.6, 2.3, and 3.2, respectively). The fatty acid composition was 50% saturated, 25% monounsaturated and 25% polyunsaturated. The thermal and rheological properties of safou pulp oil were studied showing a maximum melting point at 15 C. The tree is also used as medicine and dead branches FOR firewood. The trees on farms provide shade for food, tree crops, and humans (Ayuk et al., 1999). Bark and fruits are used to treat a headache, fever, cough and malaria; exudates are used to treat wounds, parasitic skin diseases, and respiratory diseases; leaves are used to treat malaria (Tee et al., 2014). The safou plant is also a source of money. The fruits are widely traded locally, regionally, and even internationally with exports around US$2 million in 1999 in Cameroon. The estimated value of the safou tree is US$161 per tree per year. The producers receive about 75% of the consumer’s price. The income margins can double the minimum wage, which is particularly important to women as it comes at time of year when school fees and associated costs have to be
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paid (Schreckenberg et al. 2002). The safou retail trade is dominated by women, while the wholesale trade is dominated by men (Leakey and Ladipo, 1996). The market of the fruit can increase through the development of D. edulis fruits as an oil crop (Kalenda et al., 2002; Kapseu et al., 2002) and the enhancement of the shelf life of the fresh fruits, by applying appropriate postharvest techniques (Mbofung et al., 2002).
REFERENCES Anegbeh, P.O., Ukafor, V., Usoro, C., Tchoundjeu, Z., Leakey, R.R.B., Schreckenberg, K., 2005. Domestication of Dacryodes edulis: 1. Phenotypic variation of fruit traits from 100 trees in southeast Nigeria. New For. 29 (2), 149160. Ayuk, E.T., Duguma, B., Franzel, S., Kengue, J., Mollet, M., Tiki-Manga, T., et al., 1999. Uses, management, and economic potential of Dacryodes edulis (Burseraceae) in the humid lowlands of Cameroon. Econ. Bot. 53 (3), 292301. Daly, D.C., Martı´nez-Habibe, M.C., 2016. Seven new species of Dacryodes from Western Colombia. Studies in Neotropical Burseraceae XXI. Brittonia. 68 (2), 120137. Dzondo-Gadet, M., Nzikou, J.M., Etoumongo, A., Linder, M., Desobry, S., 2005. Encapsulation and storage of safou pulp oil in 6DE maltodextrins. Process Biochem. 40 (1), 265271. Everham, E.M., Randall, W.M., VanDeGenachte, E., 1996. Effects of light, moisture, temperature, and litter on the regeneration of five tree species in the tropical montane wet forest of Puerto-Rico. Am. J. Bot. 83 (3), 10631068. Jirovetz, L., Buchbauer, G., Geissler, M., Ngassoum, M.B., Parmentier, M., 2003. Pulp aroma compounds of untreated, boiled and roasted African pear [Dacryodes edulis (G. Don) H.J. Lam] fruits from Cameroon by HS-SPME analysis coupled with GC/FID and GC/MS. Eur. Food Res. Technol. 218 (1), 4043. Kalenda, D.T., Missang, C.E., Kinkela, T., Krebs, H.C., Renard, C.M.G.C., 2002. New developments in the chemical characterization of the fruit of Dacryodes edulis (G. Don) H.J. Lam. For. Trees Livelihoods. 12, 119124. Kapseu, C., Avouampo, E., Djeumako, B., 2002. Oil extraction from Dacryodes edulis (G. Don) H.J. Lam fruit. For. Trees Livelihoods. 12, 97104. Kenmegne Kandem, A.T., 1997. Problems associated with the production of safou oil in Cameroon. Fruits 52 (5), 325330. Leakey, R.R.B., Ladipo, D.O., 1996. Trading on genetic variation fruits of Dacryodes edulis. Agrofor. Today 8 (2), 1617. Leakey, R.R.B., Atangana, A.R., Kengni, E., Waruhiu, A.N., Usoro, C., Anegbeh, P.O., et al., 2002. Domestication of Dacryodes edulis in West and CentralAfrica: characterization of genetic variation. For. Trees Livelihoods. 12, 5771. Leenhouts, P.W., Husson, A.M., Lam, H.J., 1952. Revision of the Burseraceae of Malaysian area in a wider sense. 1. Protium. 2. Scutinanthe. 3. Scandent Burseraceae (Dacryodes and canarium). 4. Dacryodes in New Guinea. Blumea. 7 (1), 154170. Mbofung, C.M.F., Silou, T., Mouragadja, I., 2002. Chemical characterization of Safou (Dacryodes edulis) and evaluation of its potential as an ingredient in nutritious biscuits. For. Trees Livelihoods. 12, 105118. Mialoundama, F., Avana, M.-L., Youmbi, P.C., Mampouya, P.C., Tchoundjeu, Z., Mbeuyo, M., et al., 2002. Vegetative propagation of Dacryodes edulis (G. Don) H.J. Lam. by marcots, cuttings, and micropropagation. For. Trees Livelihoods. 12, 8596. Okafor, J.C., 1983. Varietal delimitation in Dacryodes edulis (G. Don) H.J. Lam. (Burseraceae). Int. Tree Crops J. 2, 255265. Omoti, U., Okiy, A.D., 1987. Characteristics and composition of pulp oil and cake of African pear Dacryodes edulis (G. Don) H.J.LAM. J. Sci. Food Agric. 38, 6772. Schreckenberg, K., Degrande, A., Mbosso, C., Boli Baboule, Z., Boyd, C., Enyong, L., et al., 2002. Dacryodes edulis, a neglected non-timber forest species for the agroforestry systems of west and central Africa. For. Trees Livelihoods. 12, 4156. Sonwa, D.J., Okafor, J.C., Mpungi Buyungu, P., Weise, S.F., Tchat, M., Adesina, A.A., et al., 2002. Dacryodes edulis, a neglected non-timber forest species for the agroforestry systems of west and central Africa. For. Trees Livelihoods. 12, 4156. Tchoundjeu, Z., Kengue, J., Leakey, R.R.B., 2002. Domestication of Dacryodes edulis: State-of-the-art. For. Trees Livelihoods. 12, 314. Tee, L.H., Yang, B., Nagendra, K.P., Ramanan, R.N., Sun, J., Chan, E.S., et al., 2014. Nutritional compositions and bioactivities of Dacryodes species: a review. Food Chem. 165, 247255.
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Salak—Salacca zalacca Nur Amalina Ismail and Mohd Fadzelly Abu Bakar Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Chapter Outline Introduction Cultivar Origin and Botanical Description Morphology and Physiology Harvest Season Estimated Annual Production Chemical Composition and Nutritional Value Nutritional Composition Phytochemical Content Antioxidant Activity
383 383 384 385 385 385 385 385 387
Immunostimulatory Activity Antihyperuricemic Activity Antiproliferative Activity Sensory and Physicochemical Characteristics Conservation Current and Potential Industrial Application Acknowledgment References
387 388 388 388 388 388 389 389
INTRODUCTION Salacca zalacca is in the genus of Arecaceae, a palm tree family. Generally, the Arecaceae family consist of approximately 185 genera with 2522 species. In Malaysia, the well-known species in this family are Cocos nucifera (locally known as Kelapa or coconut), Areca catechu (locally known as Pinang), Elaeis guineensis (locally known as Kelapa Sawit or oil palm) and Nypa fruticans (locally known as Nipah or mangrove palm).
CULTIVAR ORIGIN AND BOTANICAL DESCRIPTION S. zalacca (Gaertn.) Voss is a tropical fruit that is native to the Malay archipelago (Indonesia-Kalimantan, Brunei and Malaysia-Peninsular, Sabah and Sarawak) (Aman, 2006). It has also been introduced into New Guinea, the Philippines, Ponape Island and Fiji Island (Smits, 1989). S. zalacca has multiple synonyms, some of which are Salacca edulis Reinw., S. edulis var. amboinensis Becc., S. zalacca var amboinensis (Becc.) Mogea, Salacca rumphii Wall., nom. illeg., Salacca blumeana Mart., Calamus salakka Wild. Ex Steud., Calamus zalacca Gaertn. Globally, S. zalacca is widely known as snake fruit due to its snake skin-like appearance (Figs. 1 and 2). In Malaysia and Indonesia, S. zalacca is called salak, whereas in Thailand, it is known as sala or rakun (Dembitsky et al., 2011). In other languages, Salak is called Fruta Cobra (Brazil); Yingan (Burmese); Ke Shi Sa La Ka Zong, She Pi Guo ´ Peau De Serpent, Fruit De Palmier A ´ Peau De Serpent (Chinese); Slangeskindsfrugt (Danish); Palmier Salak, Fruit A (French); Salakpalmae Schlagenfrucht, Zalak (German); Sarakka Yashi (Japanese) and Salaca (Spanish) (Lim, 2012). There are approximately 18 varieties of Salak such as Salak Bali (indigenous to Bali, Indonesia) and Salak Pondoh (indigenous fruit variety to Yogyakarta, Indonesia) which are being commercialized in Indonesia (Mahendra et al., 2013; Sukewijaya et al., 2009; Thohari et al., 2005). Salak Pondoh has three more variants, which are pondoh super, pondoh hitam and pondoh gading, whereas Salak Bali has a variant, namely Salak Gula Pasir (“Gula Pasir” in English is “sugar”) that has sweet taste and has the highest price (Lim, 2012). This fruit can be freshly eaten and sometimes it is processed into products such as pickles, candies, fruit salad, fruit juice, “dodol,” a sweet toffee-like confection, chips, crackers, wine or jam (Aralas et al., 2009; Gorinstein et al., 2009; Smits, 1989). The kernel of Pondoh variety can be eaten (Smits, 1989). The consumption of these tropical fruits is not only restricted to Asian countries. Snake fruit has become a common ingredient in diets of Europe and North America (Gorinstein et al., 2009). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00051-4 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Salak fruits which have been sold at traditional market in Sabah, Malaysian Borneo.
FIGURE 2 Close up view of Salak fruits that has a snake-like skin.
MORPHOLOGY AND PHYSIOLOGY Most Salak palm grows wild from the seed, sown or through vegetative propagation. A salak palm can reach up to 6 m. It has a short stem and grows in a compact clump formed by successive branching from the stem base (Lim, 2012). Almost all parts of the palm, especially the stem base, contain sharp and long thorns. Salak has pinnate leaves, measuring 38 m in length and the leaf surface is shiny green in color (Zawiah and Othaman, 2012). This palm thrives under the shade of other trees and interestingly, it could be intercropped with other plants such as banana (Musa sp.), durian (Durio sp.), rubber (Hevea brasiliensis), oil palm (E. guineensis), coconut (C. nucifera), and cocoa (Theobroma cacao) (Supapvanich et al., 2011). Salak palm is dioecious, meaning the male and female flowers grow on different trees and are clustered in a clump. Male inflorescence is compactly arranged, consists of 410 flowers in a cluster, and a long shaft. Female inflorescence consists of 420 flowers in a cluster, where the flower size is bigger and wider with a shorter shaft (Zawiah and Othaman, 2012). However, Salak bali is monoecious, where the male and female inflorescence happen in the same tree (Lim, 2012). Usually, the pollination of Salak is through wind and insects. To produce
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the fruit, the pollination should be induced by gently tapping the male flower to the female flower. Without such activity, the female Salak palm will not produce any fruits even when it is fertile (Zawiah and Othaman, 2012). The germination of Salak also can be done by planting the seeds from the fresh fruit and it will readily germinate in less than a week under moist, shady conditions (Smits, 1989). Salak fruit has an oval (egg-like) or nearly round shape, with 312 cm in length and 47 cm in width. Each fruit consist of 13 pieces of seeds cover with flesh (Zawiah and Othaman, 2012). In a study, it was found that pure sand, with a complete nutrition solution, is the best growing medium for Salak seedlings, as compared to peat and peat/sand compost mixture. Thus, sand-containing substrate might be the good option for Salak seedlings as it can provide good aeration for the root zone compared to pure peat (Lestari et al., 2011).
HARVEST SEASON Generally, the flowering and fruiting seasons of S. zalacca happens once a year. Usually, the flowering season is November to March. The fruit will arrive at its maturity stage during August to December (Aman, 2006). However, in Indonesia, the season of this fruit is all year round (Dembitsky et al., 2011). The tree blossoms only on the fourth year and begins to bear fruits a month later. Usually, the peak harvest (on-season period) for Salak bali is December to February, whereas the first and second intermediate harvest season (off-season period) happens in June to August and September to November, respectively.
ESTIMATED ANNUAL PRODUCTION In 2015, the production of Salak in Indonesia was 965,205 metric tonnes per year, with 49% of the production from central Java (Badan Pusat Statistik, 2017). Based on a survey that was done by Department of Agriculture, the total production of Salak in Malaysia for 2015was 3765.3 metric tonnes. In Malaysia, this tree has been planted in 1261.1 ha. The Kelantan and Terengganu states, located at the north-east of Peninsular Malaysia has become the highest producer of Salak in Malaysia (Malaysia, 2015; Zawiah and Othaman, 2012).
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE Nutritional Composition Salak fruit has 80.1 6 0.4% moisture content (Chareoansiri and Kongkachuichai, 2009). This fruit contains a high nutritional value and low calorie count. The edible part of the fruit contains high carbohydrate and fiber contents. However, it contains low protein and fat contents. Sodium (Na), magnesium (Mg), potassium (K), and calcium (Ca) are among the minerals presented in the flesh of Salak (Table 1). S. zalacca contains 0.731.28 mg/100 g vitamin C (ascorbic acid) which considered to be moderate. The nutritional composition of Salak has been tabulated in Table 1 (Chareoansiri and Kongkachuichai, 2009; Haruenkit et al., 2007). The amount of total sugar in Salak is quite similar to lychee (Litchi chinensis), mangosteen (Garcinia mangostana), and sugar apple (Annona squamosal) fruits, but lower than banana (Musa spp.), jackfruit (Artocarpus heterophyllus), and rambutan (Nephelium lappaceum) (Chareoansiri and Kongkachuichai, 2009). Sucrose contents in Salak fruit increased during maturation from stage 1 (4 months after pollination) to stage 4 (5 months after pollination) but decrease in the next stage (stage 5). The glucose and fructose levels increase to the highest level at the end of maturity, which might contribute to the sandy texture of the flesh. Hence, it is suggested to harvest the fruit at stage 4 to get the optimum sweetness of the fruits. The flesh firmness increased during maturation process but the flesh become soft at the end of maturation (Supriyadi et al., 2002).
Phytochemical Content In comparison study of phytochemicals between the core (flesh) and shell (skin) of Salak fruit, it was found that edible part of Salak contained a higher amount of total phenolic, flavonoid and monoterpenoid as compared to its skin (SuicaBunghez et al., 2016). According to Aralas et al. (2009) four Salak varieties, namely SS1, SS2, SS3 and SS4 contain total phenolic (TPC) in the range of 12.615.0 mg gallic acid equivalent/100 g. For total flavonoid content (TFC), Salak varieties consist of 4.97.1 mg catechin equivalent/g of TFC in range. The phenolic content of Salak fruit is also influenced by its maturity stage (young, mature, and ripe). TPC of Salak is highest at young stage (381.23 6 2.52 mg
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TABLE 1 Nutritional Composition of Salak Flesh Component
Concentration
Carbohydrate Sucrose (a)
7.60a
Fructose (a)
5.90a
Glucose (a)
3.90a
Total sugar (a)
17.40a
Fiber Soluble dietary fiber (a,b)
0.300.35a
Insoluble dietary fiber (a,b)
0.751.40a
Total dietary fiber (a,b)
1.101.70a
Minerals (b) Sodium
19.1 6 0.1a
Potassium
191.2 6 12.6a
Magnesium
7.16 6 0.5a
Calcium
6.11 6 0.4a
Trace Elements (b) Iron
301.7 6 11.2b
Manganese
249.9 6 11.7b
Zinc
35.1 6 2.9b
Copper
8.4 6 0.6 b
Data are reported as mean (a) Adapted from Chareoansiri and Kongkachuichai (2009) (n 5 6). (b) Adapted from Haruenkit et al. (2007) (n 5 5). a Concentration unit 5 mg/100 g edible portion/fresh weight. b Concentration unit 5 μg/100 g fresh weight.
gallic acid equivalent per 100 g), but decreases as fruit matured (274.56 6 3.21 mg gallic acid equivalent per 100 g). However, the TPC increasing from mature to ripen stage (324.90 6 3.46 mg gallic acid equivalent per 100 g) (Mokhtar et al., 2014). The same study also demonstrated that Salak contains highest TPC compared to mango (Mangifera indica L.) and rambai (Baccaurea motleyana). The amounts of total and free polyphenols, and total and free flavonoids of Salak fruits were shown in Table 2. Volatile constituents contribute to the aroma of Salak fruits. About 24 odor-active compounds have been identified in 3 Salak varieties (Pondoh, Super and Gading). The typical snake fruit aroma has been contributed by Methyl 3-methylpentanoate. The sweaty odor of the snake fruit is due to the presence of methylbutanoic acid, 3-methylpentanoic acid, and an unknown odorant. The main differences between the aroma of different cultivars could be attributed to the olfactory characteristic (Wijaya et al., 2005). Based on the analysis of volatile compound in the solvent assisted flavor evaporation extract of Salak “Pondoh,” the volatile compounds identified were methyl ester of butanoic acids, 2-methylbutanoic acids, hexanoic acid, pentanoic acid, and corresponding carboxylic acids (Supriyadi et al., 2002). The sweet and fruity character of Salak “Pondoh” are contributed by these ester group (Supriyadi et al., 2003). Furanol, which is widely known to contribute to sweet, caramel-like flavor was also found in minor concentration in Salak fruit. Composition of organic acid is also responsible for the flavor development of fruit and can influence the chemical and sensory characteristic. Malic acid is the dominant organic acid in S. zalacca followed by citric acid, tartaric acid and oxalic acid. The composition of organic acid in Salak fruit is decreased as the maturity increases (Mokhtar et al., 2014).
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TABLE 2 Phytochemicals Content in Salak Fruits Phytochemicals
Concentration
Total polyphenols (mg gallic acid equivalent/100 g fresh weight)
217.1 6 13.2
Free polyphenols (mg gallic acid equivalent/100 g fresh weight
33.2 6 1.7
Total flavonoid (mg catechin equivalent/100 g fresh weight)
61.2 6 4.9
Free flavonoid (mg catechin equivalent/100 g fresh weight)
14.1 6 0.9
Values are means 6 SD (n 5 5). Source: Adapted from Haruenkit, R. et al., 2007. Comparative study of health properties and nutritional value of durian, mangosteen, and snake fruit: experiments in vitro and in vivo. J. Agric. Food Chem. 55, 58425849.
TABLE 3 Antioxidant Activity of Different Varieties of Salak Samples
DPPH Free Radical Scavenging1
FRAP2
SS1
837.8 6 112.9a
100.33 6 1.89b
SS2
922.5 6 32.4
113.33 6 1.60a
SS3
892.7 6 30.1a
91.66 6 0.57c
SS4
691.5 6 36.4b
92.83 6 2.46c
a
Values are presented in mean 6 SD (n 5 3) which with different letters are significantly different at P , .05. 1 DPPH free radical scavenging activity was expressed as mg AEAC in 100 g of dry sample. 2 FRAP was expressed as μM ferric reduction to ferrous in 1 g of dry sample.
Antioxidant Activity Variation in antioxidant activities of different varieties exist even if fruit is from the same species. Aralas et al. (2009) demonstrated that the SS2 salak variety showed the highest antioxidant activities (via DPPH radical scavenging and FRAP reducing ability mechanisms) in comparison with other varieties, SS1, SS3 and SS4 (Table 3). The core of Salak fruit has higher antioxidant activity as compared to its shell (Suica-Bunghez et al., 2016). The edible part of Salak exhibit higher antioxidant capacity as compared to mangosteen (G. mangostana), mango (M. indica), and rambai (B. motleyana) but slightly lower activity than Durian (Durio zibethinus) (Mokhtar et al., 2014; Haruenkit et al., 2007). Young stage S. zalacca fruit showed higher phytochemicals and antioxidant activity compared to its mature and ripe stages (Mokhtar et al., 2014). Thus, the development of antioxidant-rich product from young stages of S. zalacca is recommended as it contains high phytochemicals content and antioxidant activity. The potential of the fruit byproduct (peel and seed) to be developed as natural antioxidant source has been investigated by a few researchers (Deng et al., 2012; Fitri et al., 2016; Kanlayavattanakul et al., 2013). A study by Fitri et al. (2016) demonstrated that Salak peel extract has the highest antioxidant capacity (DPPH scavenging activity) compared to other tropical fruits such as Matoa (Pometia pinnata), Papaya (Carica papaya L.), Soursop (Annona muricata), Kapundang (Baccaurea racemosa) and Rambai (B. motleyana) peel and seed extracts. For lipid peroxidation inhibition assay, Salak peel is in the highest group that exhibit the higher activity along with Soursop peel and Matoa peel. Among the fractions of peel extract, ethyl acetate fraction exhibited the highest antioxidant activity in comparison with 70% ethanolic and aqueous fraction (Kanlayavattanakul et al., 2013). The ethyl acetate fraction of Salak peel has been shown to be noncytotoxic in vero (kidney cells) and normal human fibroblast cells. This evidence suggests that all parts of Salak fruits can be fully utilized as an alternative source of natural antioxidant.
Immunostimulatory Activity Some plants have the ability to promote immune response. Salak fruit peel extract was able to enhance the phagocytotic activity (process to remove and degrade invading microbes) of murine macrophage-like cell line J744.1 (Wijanarti et al., 2015).
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Antihyperuricemic Activity High concentration of uric acid in blood stream may lead to the formation of gout, featured by hyperuricemia and recurrent attacks of arthritis. The xanthine oxidase (XO) enzyme is responsible for oxidizing hypoxanthine to xanthine and xanthine to uric acid (Azmi et al., 2012). Thus, the inhibition of xanthine oxidase indicates the potential of plants or compounds to lower the uric acid level in blood. The ethyl acetate and ethanol extract of S. edulis cv Bongkok has been shown to display xanthine oxidase inhibitory activity with IC50 values of 24.75 and 44.95 μg/mL, respectively. Two compounds, 2-methylester-1-H-pyrrole-4-carboxylic acid and 3β-hydroxy-sitosterol have been isolated from Salak ethyl acetate extract, where the first compound has been found to be active against xanthine oxidase (IC50 5 48.86 μg/mL), while the latter is inactive against the enzyme (Priyanto et al., 2007). In another study, the petiole and seeds of S. zalacca extract did not show any inhibition towards xanthine oxidase. The study investigated the effect of different plant parts in different solvent for xanthine oxidase inhibitory activity. For S. zalacca, the 70% methanolic leaves extract and ethanolic leaves extract showed higher xanthine oxidase inhibition. The in vivo study of antihyperuricemic activity of Salak Bongkok ethanolic extract suggest that the administration of the extract at doses 200 mg/kg body weight was able to decrease serum uric acid level significantly on Wistar male rats (induced with potassium oxonate intraperitoneally simultaneous with uric acid orally) as compared to the control group after 67 h induction (Priyanto et al., 2012).
Antiproliferative Activity Snake fruit (cultivar Sumalee) methanol extract has been found to exhibit antiproliferative activity on human cancer cell lines (Calu-6 for human pulmonary carcinoma and SNU-601 for human gastric carcinoma). In comparison with Hayward conventional kiwi fruit antiproliferative activity, snake fruit methanol extract (2000 μg/mL concentration) displayed similar activity with the kiwi fruit on Calu-6 and SMU-601 cell line in the range 90.5%87.6% and 89.3% 87.1% cell survival, respectively. The snake fruit (cultivar Sumalee) also contain high antioxidant and polyphenol content which might contribute to its antiproliferative activity (Gorinstein et al., 2009).
SENSORY AND PHYSICOCHEMICAL CHARACTERISTICS At stage 1 (3.5 months after pollination) and 2 (4 months after pollination) of fruit development, the flesh of the fruit is white in color and turns yellowishwhite after stage 5 (Supriyadi et al., 2002). The fruit has sweet, sweetsour and sometimes has astringent taste with combinations of pineapple, pear, and banana aromas (Gorinstein et al., 2009). The Pondoh cultivar has a sweet taste even at an immature stage (Supriyadi et al., 2002). Another cultivar, Salak bali, has a moist and crunchy fruit texture.
CONSERVATION Some of the indigenous fruit species are vulnerable to loss of genetic diversity (Normah et al., 2002). Therefore, conservation of this species is important in order to ensure the sustainability of the fruit source and at the same time meet the consumer demand. In Indonesia, S. zalacca has been given first priority in germplasm conservation. The collection of Salak germplasm and plants has been conducted by Research Institute for Fruits, Indonesia and Genetic Resources Garden at Cibinong (Thohari et al., 2005). Salak palm plantation is one of the ex-situ conservation plans to ensure the availability of this rare fruit. Salak Sibetan plantation and RC Fruit Conservation Farm in Indonesia are examples of ex-situ conservation efforts (Budiasa and Ambarawati, 2014; Coronel, 2013). There are about 220 edible fruit species grown in the RC Fruit Conservation Farm, with 124 plant genera and 54 families. S. zalacca is one of the species that has been conserved. Salak Sibetan plantation involves the local community for the conservation and agro-tourism project of Salak. In Malaysia, a field genebank has been established to conserve the tropical fruit species that is at risk of genetic erosion. The Department of Agriculture of Malaysia has established an arboretum to locate 250 species and cultivar of wild and underutilized fruits which include S. edulis (Wong and Senawi, 2005).
CURRENT AND POTENTIAL INDUSTRIAL APPLICATION Edible parts of Salak fruit have been developed into fruit juice, pickles, jam, candies, wine, jams, and other food products (Aralas et al., 2009; Gorinstein et al., 2009; Smits, 1989). The kernel of Salak has been developed into coffee. This exotic fruit has been exported to other countries such as Europe and North America.
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The Salak farm has been seen as a good agro-tourism product. This community-based agro-tourism of Salak Sibetan plantation (located at Sibetan Village, eastern part of Bali) involved local farmers as an innovator, who offer various types of services and agro-tourism products. The activities involve Salak plantation visits and fresh fruit picking, visiting a winery and a crispy chip making demonstration. This effort will not only give positive effects towards tourism in Indonesia, but it will make people learn about the exotic fruit in South East Asia (Budiasa and Ambarawati, 2014). Currently, research has been undertaken to investigate the potential of Salak skin and kernel, usually discarded, being developed into products or applied in industry. Salak fruit has the potential to be incorporated into cosmetic products. The high antioxidant showed by the extract and the stability of Salak peel loaded with liposome consisting lecithin and hydrophobically modified hydroxyethylcellulose in adequate entrapment efficiency should become good characteristic for the development of nature-based cosmetic products (Kanlayavattanakul et al., 2013). Salak waste such as seed has the potential to be utilized as biomedia in biofilter for biogas production. In recent study by Lestari et al. (2016), a biofilter that been attached to Salak seeds was able to remove 97.15% of hydrogen sulfide. Hydrogen sulfide has become major problem in biogas production as it is highly toxic, corrosive, colorless, produces foul odor and could cause corrosion in the engine and pipeline when used as fuel (Lestari et al., 2016). This showed that Salak has potential to be utilized in various fields.
ACKNOWLEDGMENT The authors would like to acknowledge Ministry of Higher Education (MOHE) of Malaysia and Universiti Tun Hussein Onn Malaysia (UTHM) for financial assistance under the Fundamental Research Grant Scheme (FRGS) (Project No: 1560) and Incentive Grant Scheme for Publication (IGSP) (Project No: U673).
REFERENCES Aman, R., 2006. Buah-buahan Nadir Semenanjung Malaysia, third ed. Dewan Bahasa dan Pustaka, Kuala Lumpur. Aralas, S., Mohamed, M., Bakar, M.F.A., 2009. Antioxidant properties of selected salak (Salacca zalacca) varieties in Sabah, Malaysia. Nutr. Food Sci. 39 (3), 243250. Azmi, S.M.N., Jamal, P., Amid, A., 2012. Xanthine oxidase inhibitory activity from potential Malaysian medicinal plant as remedies for gout. Int. Food Res. J. 19 (1), 159165. Badan Pusat Statistik, 2017. Production of Fruits. Badan Pusat Statistik Indonesia. Available at: ,http://www.bps.go.id/site/resultTab. (accessed 03.01.17.). Budiasa, I.W., Ambarawati, I.G.A.A., 2014. Community based Agro-tourism as as an innovative integrated farming system development model towards sustainable agriculture and tourism in Bali. J. ISSAAS. 20 (1), 2940. Chareoansiri, R., Kongkachuichai, R., 2009. Sugar profiles and soluble and insoluble dietary fiber contents of fruits in Thailand markets. Int. J. Food Sci. Nutr. 60 (S4), 126139. Coronel, R.E., 2013. On-farm biodiversity conservation: the RC fruit conservation farm. In: Crops for the Future Beyond Food Security, pp. 559568. Dembitsky, V.M., et al., 2011. The multiple nutrition properties of some exotic fruits: biological activity and active metabolites. Food Res. Int. 44, 16711701. Deng, G., et al., 2012. Potential of fruit wastes as natural resources of bioactive compounds. Int. J. Mol. Sci. 13, 83088323. Fitri, A., et al., 2016. Screening of antioxidant activities and their bioavailability of tropical fruit byproducts from Indonesia. Int. J. Pharm. Pharm. Sci. 8 (6), 96100. Gorinstein, S., et al., 2009. The comparative characteristics of snake and kiwi fruits. Food Chem. Toxicol. 47 (8), 18841891. Haruenkit, R., et al., 2007. Comparative study of health properties and nutritional value of durian, mangosteen, and snake fruit: experiments in vitro and in vivo. J. Agric. Food Chem. 55, 58425849. Kanlayavattanakul, M., et al., 2013. Salak plum peel extract as a safe and efficient antioxidant appraisal for cosmetics. Biosci. Biotechnol. Biochem. 77 (5), 10681074. Lestari, R.A.S., et al., 2016. Hydrogen sulfide removal from biogas using a salak fruit seeds packed bed reactor with sulfur oxidizing bacteria as biofilm. J. Environ. Chem. Eng. 4 (2), 23702377. Lestari, R., Ebert, G., Huyskens-Keil, S., 2011. Growth and physiological responses of Salak cultivars (Salacca zalacca (Gaertn.) Voss) to different growing media. J. Agric. Sci. 3 (4), 261271. Lim, T.K., 2012. Salacca zalacca. Edible Medicinal and Non-Medicinal Plants: Volume 1, Fruits. Springer, Netherlands, pp. 432437. Mahendra, M.S., Rai, I.N., Janes, J., 2013. Current postharvest handling practices of salak and mango fruits in Indonesia. Acta Hortic. 975, 479486. Malaysia, D. of A., 2015. Fruit Crops Statistic Malaysia 2015, Putrajaya. Mokhtar, S.I., et al., 2014. Total phenolic contents, antioxidant activities and organic acids composition of three selected fruit extracts at different maturity stages. J. Trop. Resources Sustainable Sci. 2 (February), 4046. Normah, M.N., et al., 2002. Ex situ conservation of tropical rare fruit species. Acta Hortic. 575, 221230.
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Priyanto, L.H.A., et al., 2007. Xanthine oxidase inhibitor activity of terpenoid and pyrrole compounds isolated from snake fruit (Salacca edulis Reinw.) cv Bongkok. J. Appl. Sci. 7 (20), 31273130. Priyanto, L.H.A., et al., 2012. Antihyperuricemic effect of ethanol extract of snake fruit (Salacca edulis Reinw.) var. Bongkok on Wistar male rat. J. Food Sci. Eng. 2, 271276. Smits, W.T.M., 1989. Salacca zalacca (Gaertner) Voss. In: Westphal, E., Jansen, P.C.M. (Eds.), Plant Resources of South-East Asia: A Selection. Pudoc, Wageningen, pp. 248253. Suica-Bunghez, I.R., et al., 2016. Antioxidant activity and phytochemical compounds of snake fruit (Salacca zalacca). IOP Conference Series: Materials Science and Engineering, 133, 8 pp. Sukewijaya, I.M., Rai, I.N., Mahendra, M.S., 2009. Development of salak bali as an organic fruit. Asian J. Food Agro-Industry, (Special Issue). S37S43. Supapvanich, S., Megia, R., Ding, P., 2011. Salak (Salacca zalacca (Gaertner) Voss). Woodhead Publishing Limited, Cambridge. Supriyadi, et al., 2002. Changes in the volatile compounds and in the chemical and Pondoh during maturation. J. Agric. Food Chem. 50, 76277633. Supriyadi, et al., 2003. Biogenesis of volatile methyl esters in snake fruit (Salacca edulis, Reinw) cv. Pondoh. Biosci. Biotechnol. Biochem. 67 (6), 12671271. Thohari, M., Adisoemarto, S., Kusumo, S., 2005. Plant genetic resources collection in response to early warning system: situation of Indonesia. In: Pandey, A., et al., (Eds.), Wild Relatives of Crop Plants in India Collection and Conservation. National Bureau of Plant Genetic Resources, India, pp. 4754. Wijanarti, S., et al., 2015. Immunostimulatory activity of snake fruit peel extract. Cytotechnology 68 (5), 17371745. Wijaya, C.H., et al., 2005. Identification of potent odorants in different cultivars of snake chromatography 2 olfactometry. J. Agric. Food Chem. 53 (5), 16371641. Wong, L.J., Senawi, M.T.M., 2005. Plant genetic resources and documentation systems in Peninsular Malaysia. In: Pandey, A., et al., (Eds.), Wild Relatives of Crop Plants in India Collection and Conservation. National Bureau of Plant Genetic Resources, India, pp. 7581. Zawiah, N., Othaman, H., 2012. 99 Spesies Buah di FRIM, 2012. Institut Penyelidikan Perhutanan Malaysia Kepong, Selangor, Malaysia.
Soursop—Annona muricata Shuaibu Babaji Sanusi and Mohd Fadzelly Abu Bakar Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Chapter Outline Introduction Cultivar Origin and Distribution Taxonomy and Botanical Description Harvesting Season Estimated Annual Production Physiology and Biochemistry
391 391 391 392 392 393
Sensory Characteristics of Soursop Fruit Harvest and Postharvest Conservation Industrial Application Acknowledgments References
394 394 395 395 395
INTRODUCTION Annona muricata, or soursop, is an exotic commodity which is currently finding its way into commercial markets as it is becoming better known. The harvested yield contains only a small proportion of total global fruit production. Thus, sustainability and improvement of these species in suitable regions, as well as improved application and potential commercial values are needed. This chapter discusses various aspects of soursop, including cultivar origin and distribution, taxonomy and botany, harvest season, estimated annual production, fruit physiology and biochemistry, chemical compositions and nutritional values, sensory characteristics, harvest and postharvest conservation, and industrial applications.
CULTIVAR ORIGIN AND DISTRIBUTION Soursop originates from central America within the lowlands regions. In 1526, a Spanish historian, Gonzalo Ferna´ndez de Oviedo y Valde´s, first described soursop (Love and Paull, 2011). It is grown in the Caribbean as well as equatorial belt of the Americas, mostly in the Bahamas, Bermuda, Cuba, Dominican Republic, Grenada, southern Mexico, Costa Rica, St. Vincent, Puerto Rico, Colombia, Brazil, and Ecuador. Soursop is adaptable to tropical climates, thus distributed throughout the tropics of the world. It is currently cultivated for its fruit in commercial quantity in the Caribbeans, Americas, Africa, and southeast Asia areas such as Malaysia, Indonesia and the Philippines (Pinto et al., 2005; Gajalakshmi et al., 2012).
TAXONOMY AND BOTANICAL DESCRIPTION A. muricata belongs to the Annonaceae family which encompasses about 130 genera and 2300 species (Moghadamtousi et al., 2015). A. muricata L. is called soursop in English. It is also known as guayabano in the Philippines; guanabana by Spanish; the French called it corossol epineux; sirsak in Indonesian; Brazilians called it graviola; thurian thet, thurian-khaek, riannam in Thailand, mang cauxiem (Vietnamese), and in Malaysia, it is known as durian belanda, durian maki (Pinto et al., 2005; Pareek et al., 2011). The soursop tree is around 810 m in height, upright, with low branches when fully mature. The tree is small, slender, and evergreen when domesticated as a garden plant in lowland South America. The stems are rough, and rounded with nut-brown coloration. The leaves are oblongovate to cylindrical with have short petioles, measuring from 14 to even 16 cm in length with the width measuring 57 cm. Their flowers are 3.23.8 cm in length, which open in the early hours. Flowering in this species is a continuous process, and appear everywhere on different branch or trunk Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00053-8 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Whole fruit of Annona muricata.
FIGURE 2 Cross-section of Annona muricata fruit.
(Pinto et al., 2005; Badrie and Schauss, 2010). The tree produces an oval or conical shaped fruit, which it is a dark green in color when unripe and transform to lighter green when fully ripe. It has the average weight of 4 kg in some countries; however, the weight ranges between 0.4 and 1.0 kg in Mexico, Nicaragua, and Venezuela. It has a white and juicy flesh, and the fruit may contain 127170 seeds, depending on the size, distributed in the pulp. The seed sizes differ from 1 to 2 cm in length and their weight ranges between 0.33 and 0.59 g, with a dark-brown coloration (Pinto et al., 2005; Coria-Te´llez et al., 2016). The fruit of A. muricata is shown in Figs. 1 and 2.
HARVESTING SEASON The production of the flowers and fruit of soursop is more or less a continuous process; however each region has a specific ripening period. In Puerto Rico for instance, the ripening season usually starts in March until September, while the harvesting season in Queensland (Australia) commences in April. The ripening season ranges between June and September in southern India, Mexico and Florida; the season progresses to October in the Bahamas. In Hawaii, there is early ripening which begins in January until April; the midseason ripening between June and August, with the highest production in July. Occasionally late harvests do occur in October or November (Sawant and Dongre, 2014).
ESTIMATED ANNUAL PRODUCTION There is limited literature on the soursop with the exception of data from Americas. Mexico is the prime producer of soursop, producing about 35,000 mt of fruit from approximately 5900 ha in 1997. Venezuela in 1987 produced around
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TABLE 1 Chemical and Nutritional Composition of Edible Pulp of Soursop Fruits per 100 g Components
Mean 6 Standard Deviations
Water (g)
81 6 2.5 (77.981.7)
Proteins (g)
1 6 0.55 (0.691.7)
Lipids (g)
0.6 6 0.3 (0.30.8)
Carbohydrates (g)
17.25 6 0.1 (16.318.2)
Fiber (g)
0.86 6 0.1 (0.780.95)
Total acidity (g)
1.0 6 0.3 (0.71.3)
Ash (g)
0.61 6 0.2 (0.40.86)
Energy (calories)
65 6 5 (6471)
Calcium (mg)
15 6 7 (8.80.22)
Phosphorus (mg)
28 6 1 (27.129)
Iron (mg)
0.7 6 0.1 (0.60.82)
Vitamin A (mg)
14.45 6 5.45 (8.920)
Vitamin B1 (mg)
0.07 6 0.01 (0.060.077)
Vitamin B12 (mg)
0.08 6 0.035 (0.050.12)
Vitamin B5 (mg)
1.2 6 0.3 (0.891.52)
Ascorbic acid (mg)
19.4 6 3 (16.422)
Anthocyanin
6.44 6 0.10
Flavonoids
9.32 6 0.45
Tannin
65.98 6 2.11
Alkaloids
1.90 6 0.04
Saponin
0.17 6 0.01
Source: Pinto, A.D.Q., Cordeiro, M.C.R., De Andrade, S.R.M., Ferreira, F.R., Filgueiras, H.A., Alves, R.E. et al., 2005. Annona species. International Centre for Underutilised Crops; University of Southampton; Pareek, S., Yahia, E. M., Pareek, O.P., Kaushik, R.A., 2011. Postharvest physiology and technology of Annona fruits. Food Res. Int. 44, 17411751; Onyechi, A.U., Ibeanu, V.N., Eme, P.E., Kelechi, M., 2015. Nutrient, phytochemical composition and consumption pattern of soursop (Annona muricata) pulp and drink among workers in University of Nigeria, Nsukka Community. Pak. J. Nutr. 14, 866.
10,000 mt on about 3500 ha. Brazil produces about 8000 mt on approximately 2000 ha, virtually all for sale in the internal market. Due to the favorable climate, around 90% of the total Brazilian production emanates from the north-eastern region of the country (Pinto et al., 2005). There are about 500,000 trees of soursop fruit in the Philippines with an estimated annual production of 8500 t (Rieser et al., 1996). The annual fruit production in Hawaii is around 16,000 lb per acre (roughly equal kg/ha) in an established land. In Puerto Rico, there an estimated production of 50008000 lb per acre (roughly equal kg/ha) (Love and Paull, 2011; Sawant and Dongre, 2014) (see also Table 1).
PHYSIOLOGY AND BIOCHEMISTRY Soursop was categorized as climacteric by measuring the rate of respiration. It is climacteric in the sense that, the immature fruits are often harvested and ripened postharvest. Hence, soursop is categorized as a multiple climacteric fruit because the berries that make up the fruit are of different maturities and therefore ripening at different intervals. The well matured soursop fruit produces a biphasic climacteric respiration, yielding 100 and then 350 mL/kg per h of CO2 at the temperature of 2530 C. In between the two respiratory maxima, there exists the peak ethylene production of 250350 mL/kg per h (Badrie and Schauss, 2010). The respiration in immature harvested fruit is higher than in matured ones. During the maturation process, the peel coloration transforms to slight yellowish green from green
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indicating the chlorophyll has lost living carotenoids which are main contributors to the entire peel coloration (Badrie and Schauss, 2010). As the fruit ripening process continues, the peel gradually turns to dark brown, perhaps as a result of chloroplast interruption resulting in the release of polyphenol oxidases leading to the oxidation and polymerization of phenols. The matured fruit is identified by the smooth and soft skin. During the second day of harvesting, variations in starch of soursop have been documented, with a lesser fraction of the starch left at 6 days from harvest. Besides the decrease of ethanol and starch fraction, there is a rise in ascorbate, total soluble sugars, increase in total soluble solids to approximately 16 Brix, as well as increase in total titratable acidity (Badrie and Schauss, 2010). On the other hand, the total sugars start increasing from 1 to 2 days after harvesting the fruit with a concurrent increase in respiration. There is a rapid increase in ethanol-soluble sugars as the ripening process continues. Five days after harvest, the fructose and glucose attains their highest concentration. There is a significant drop in pH from 5.5 to 3.7 within the 3 days of ripening process, which consequently results in an increase in titratable acidity. There is a threefold increase in malic acid content which gives the acidic flavor of the fruit, thus decreasing the pulp pH as well (Badrie and Schauss, 2010). The volatile production in soursop differs during ripening. At the beginning of respiration, there are a few volatiles, which significantly increase as the ethylene production increase. The optimum eating period is realized when the ethylene and volatiles level reach peak (roughly 4 days from harvest). On the other hand, there is slight increase in total ethanol-soluble phenol of about 10% first, and then significantly decrease to around 50% of preclimacteric levels with the extreme decrease after the climactic peak. This consequently results in a loss of astringency which causes a bland flavor of the slightly overripe soursop fruit. The off-flavor of an overripe fruit is a consequence of some fermentation, lower organic acids, and phenols (Badrie and Schauss, 2010). Lima et al. (2006) in Brazil studied the chemical, physical, and biochemical changes associated with the softening of soursop fruits during maturation. The fruits were collected when matured and kept at 26.3 6 0.6 C temperature, and 88 6 12% relative humidity. No significant disparity was observed in the soluble pectin content during 1, 2, 3, 4, and 5 days. Around 5% loss of weight was observed on the fruit in day 5 without shriveling. The decrease in starch and total pectin contents occurred in the course of greatest enzymatic activity of amylase and polygalacturonase respectively.
SENSORY CHARACTERISTICS OF SOURSOP FRUIT Sensory characteristics are the major parameters in evaluating the quality of a product. Currently, sensory evaluation is an irreplaceable tool in the food industry while interacting with the key sectors in food production. Lutchmedial et al. (2004) identified and quantified the key sensory descriptors of soursop using quantitative descriptive analysis. The pulp of the soursop fruit is white with a unique pleasant, subacid and aromatic flavor (Lutchmedial et al., 2004; Baskaran et al., 2016). It has a pleasant blend of sweetness and mild sourness taste (Pinto et al., 2005).
HARVEST AND POSTHARVEST CONSERVATION The quality of fruit largely depends on cultural practices. Moreover, variation exists in both the fruit quality and size as a result of seed propagation. Consequently, the vegetative method of propagation is recommended, as it is an effective method of obtaining highly yield with good quality fruits. Among the major factors affecting the fruit quality of soursop are age of the fruit at harvest and harvesting techniques employed. The soursop fruits in an orchard do not ripen at the same time. Hence, frequent visit is compulsory in order to identify the fruits that have reached harvest point (Lima and Alves, 2011). Harvest of soursop fruit should be early in the morning, thus escaping the sun which may possibly cause browning of the spurs when touched as a result of heat. When harvested, the soursop fruit must be placed in containers shielded with flexible and soft material, and should be kept away from the sun, dust, and rain. When there are many layers of fruits in a container, sponge should be placed in between the fruits (Lima and Alves, 2011). Of all the current conservation practices, refrigeration is the most widely employed and it is effective in conserving quality features such as aroma, firmness, flavor, color, and humidity content (Lima and Alves, 2011). Soursop can be conserved generally using the following strategies; firstly, the planting of soursop tree in small plot of land should be encouraged. Secondly, the soursop species should be collected in an arboretum for research purposes. Thirdly, the network between producers, traders, and consumers should be strengthening (to promote the market). Finally, the general public should be educated about the nutritional benefit of soursop.
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INDUSTRIAL APPLICATION Soursop is the most suitable species of among the genus Annona in terms of industrial potential and commercialization due to its agreeable aroma and taste. The fruit of soursop is extensively used in food industries for making icecream, candies, nectars, yoghurts, syrups, sherbets, canning, and for preparation of beverages. It is also a starting material for flakes, powders, and fruit bars (Pinto et al., 2005; Coeˆlho de Lima and Alves, 2011). In Brazil and Cuba, a refreshing drink is prepared by mixing the soursop pulp with milk and sugar (champola), while it is commonly mixed with water (carato) in Puerto Rico (Badrie and Schauss, 2010). In addition, they possess high medicinal values, for instance, acetogenins from soursop exhibit anticancer properties, although information about the plant part suitable to use for isolation of these secondary products is still unknown. The only organization interested in the industrialization of secondary products so far is Rain Tree, United States. Furthermore, there is a success in using domestically prepared insecticide from extracts of wild soursop in Africa (Pinto et al., 2005).
ACKNOWLEDGMENTS The authors are very grateful to Universiti Tun Hussein Onn Malaysia (UTHM) for providing internal research funding (UTHM Grant Contract No: U555).
REFERENCES Badrie, N., Schauss, A., 2010. Soursop (Annona muricata L.): composition, nutritional value, medicinal uses, and toxicology. In: Watson, R.R., Preedy, V.R. (Eds.), Bioactive Foods in Promoting Health: Fruits and Vegetables. Elsevier Inc, Oxford, pp. 621643. Baskaran, R., Ravi, R., Rajarathnam, S., 2016. Thermal processing alters the chemical quality and sensory characteristics of sweetsop (Annona squamosa L.) and soursop (Annona muricata L.) pulp and nectar. J. Food Sci. 81, S182S188. Coria-Te´llez, A.V., Montalvo-Go´nzalez, E., Yahia, E.M., Obledo-Va´zquez, E.N., 2016. Annona muricata: a comprehensive review on its traditional medicinal uses, phytochemicals, pharmacological activities, mechanisms of action and toxicity. Arab. J. Chem. Gajalakshmi, S., Vijayalakshmi, S., Devi Rajeswari, V., 2012. Phytochemical and pharmacological properties of Annona muricata: a review. Int. J. Pharm. Pharm. Sci. 4, 36. Lima, M.A.C.D., Alves, R.E., 2011. Soursop (Annona muricata L.). In: Yahia, E.M. (Ed.), Postharvest Biology and Technology of Tropical and Subtropical Fruits. Woodhead Publishing Limited, Sawston, Cambridge, UK, pp. 365392. Lima, M.A.C.D., Alves, R.E., Filgueiras, H.A.C., 2006. Changes related to softening of soursop during postharvest maturation. Pesqui. Agropecu. Bras. 41, 17071713. Love, K., Paull, R.E., 2011. Soursop. Honolulu, HI, University of Hawaii. 6 pp. (Fruit, Nut, and Beverage Crops Series; F_N-22). Lutchmedial, M., Ramlal, R., Badrie, N., Chang-Yen, I., 2004. Nutritional and sensory quality of stirred soursop (Annona muricata L.) yoghurt. Int. J. Food Sci. Nutr. 55, 407414. Moghadamtousi, S.Z., Fadaeinasab, M., Nikzad, S., Mohan, G., Ali, H.M., Kadir, H.A., 2015. Annona muricata (Annonaceae): a review of its traditional uses, isolated acetogenins and biological activities. Int. J. Mol. Sci. 16, 1562515658. Onyechi, A.U., Ibeanu, V.N., Eme, P.E., Kelechi, M., 2015. Nutrient, phytochemical composition and consumption pattern of soursop (Annona muricata) pulp and drink among workers in University of Nigeria, Nsukka Community. Pak. J. Nutr. 14, 866. Pareek, S., Yahia, E.M., Pareek, O.P., Kaushik, R.A., 2011. Postharvest physiology and technology of Annona fruits. Food Res. Int. 44, 17411751. Pinto, A.D.Q., Cordeiro, M.C.R., De Andrade, S.R.M., Ferreira, F.R., Filgueiras, H.A., Alves, R.E., et al., 2005. Annona species. International Centre for Underutilised Crops; University of Southampton. Rieser, M.J., Gu, Z.M., Fang, X.P., Zeng, L., Wood, K.V., McLaughlin, J.L., 1996. Five novel mono-tetrahydrofuran ring acetogenins from the seed of Annona muricata. J. Nat. Prod. 59, 100108. Sawant, T.P., Dongre, R.S., 2014. Bio-chemical compositional analysis of Annona muricata: a miracle fruit’s review. Int. J. Univ. Pharm. Bio Sci. 3, 82104.
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Sugar Apple—Annona squamosa Linn. Muhammad Murtala Mainasara, Mohd Fadzelly Abu Bakar, Maryati Mohamed, Alona C. Linatoc and Fatimah Sabran Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Chapter Outline Annona squamosa International Common Names Cultivar Origin Botanical Aspects Description Harvest Season Estimated Annual Production Plant Chemicals
397 397 397 398 398 400 400 400
Fruit Composition Sensory Characteristics Harvest and Postharvest Conservation Industrial Application Economic Value References Further Reading
400 401 401 402 402 402 402
ANNONA SQUAMOSA Preferred Scientific Name: Annona squamosa L. Preferred Common Name: Sugar apple
INTERNATIONAL COMMON NAMES G G G G
English: Atemoya; sugar apple; Sugar-apple; Sweetsop Spanish: Anon; Anona (Blanca); Anona blanca; Chirimoyo French: annone ecailleuse; attiee; attier pomme cannelle; Corossolier a fruits ecailleux. Malaysian: Buah nona; Nona Sri Kaya; Sri Kaya; Sarikaya
Annona squamosa (the sugar apple) is a member of family Annonaceae that is local to the tropical America and broadly developed for its sweet-smelling, succulent, and tasteful fruit, which have more vitamin C than an orange. The Sugar apple is the most developed tropical fruit in the family (Pandey et al., 2014).
CULTIVAR ORIGIN The locality and originality of the plant is not known due to the fact that it is widely developed and naturalized. It is believed that the tree may have started in the West Indies. The date of introduction to the West Indies is also unknown, but it was present by the time of Sir Hans Sloane’s 16871689 voyage to Jamaica (UK Natural History Museum, 2014), during which he collected specimens now present in the British Museum (British Museum specimen BM000594147). A. squamosa grows well in swampy tropical atmospheres around the world, including: Polynesia, Indonesia, southern Mexico, tropical Africa, the Antilles, South and Central and America, and Australia,. It was later made known to India and the Philippines by the Spanish and Portuguese in the sixteenth century, and has been produced from this time. It has been found from north to southern Florida in the United States and south to Bahia in Brazil, and to other Asian countries, and is seen prominently in French Polynesia and a couple of Pacific islands (PIER, 2015). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00054-X © 2018 Elsevier Inc. All rights reserved.
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BOTANICAL ASPECTS Taxonomic Classification: Annona squamosa L. Kingdom: Plantae Sub Kingdom: Tracheobionta Super division: Spermatophyta Division: Magnoliophyta Class: Magnoliopsida Order: Magnoliales Family: Annonaceae Genus: Annona L. Species: Annona squamosa The genus Annona comprises of about 125 species with some species generally cultivated for their edible fruits and often becoming established beyond their native range of tropical America and Africa (Moghadamtousi et al., 2015). The name Annona could be traced from the Latin word “anon,” meaning “yearly produce,” referring to “the fruit production habits of the various species in this genus” an aboriginal name for the tree in tropical America, probably “Santo Domingo.” The species A. squamosa is ordinarily known as “sugar apple” or “sweetsop” in English, but it is also occasionally known as “custard-apple,” especially in Asia (Shenoy et al., 2009).
DESCRIPTION A. squamosa is a robust, half evergreen bush or little tree achieving 8 m (26 ft). Blooming and fruit bearing for the most part begins when the tree is 23 years old. Productive fruit generation is with sufficient rainfall (.70 cm or 27 in. annually), and requires pollinators, which incorporate several types of insect; fertilization by bumble bees (Apis mellifera) occurs due to the profundity of the blooms. Fertilization by hand is used to enhance harvests (Shenoy et al., 2009). Fruits are 610 cm (2.43.9 in.) expansiveness, with a thick, finished, or rough skin that gives them a pinecone appearance. Fruits weigh 100230 g (3.58.1 oz). The fruit tissue is fragrant, sugary, and white to bright yellow, with the surface similar kind of custard; the flavor is viewed as the best among fruits in the family. Natural products are partitioned into 2038 fragments, each for the most part containing a hard, gleaming earthy dark, seed, enmeshed in the substance, albeit a few trees deliver a seedless organic product. The fruits are for the most part eaten crisp, or used in juice making for refreshments or ice, and are a decent wellspring of iron, calcium, and phosphorus (NRCS, 2008) (see also Figs. 1 and 2). Branches have a light chestnut bark and evident leaf scars; internal bark is light yellow; twigs get the opportunity to be particularly cocoa-colored with light cocoa touches (lenticels—little, oval, balanced spots upon the stem or branch of a plant, from which the essential tissues may expand or roots may issue). Thin, clear, substitute leaves happen freely, 5 cm (2 in.) to 17 cm (6.7 in.) long and 2 cm (0.79 in.) to 6 cm (2.4 in.) wide, balanced at the base and pointed at the tip (oval lanceolate). They are bright green on both surfaces and for the most part smooth with slight hairs on the underside when young. The sides from time to time are possibly unequal and the leaf edges are without teeth, unnoticeable bristly when energetic leaf stalks are 0.4 cm (0.16 in.) to 2.2 cm (0.87 in.) long, green, insufficiently pubescent. In the flowers, there are single or in short horizontal groups of 24 around 2.5 cm (0.98 in.) long, greenish-yellow blossoms on a shaggy, slim 2 cm (0.79 in.) long stalk. Three green external petals, purplish at the base, oval, 1.6 cm (0.63 in.) to 2.5 cm (0.98 in.) long, and 0.6 cm (0.24 in.) to 0.75 cm (0.30 in.) wide, three internal petals decreased to moment scales or truant. Extremely various stamens; swarmed, white, under 1.6 cm (0.63 in.) long; ovary light green. Styles are white, swarmed on the raised hub. Every pistil frames a different tubercle (a little adjusted wartlike projection), for the most part 1.3 cm (0.51 in.) to 1.9 cm (0.75 in.) long and 0.6 cm (0.24 in.) to 1.3 cm (0.51 in.) wide which develops into the total organic product. Blooming happens in Spring to early Summer and blossoms are pollinated by nitidulid insects (Bhattacharya and Chakraverty, 2016). Aggregate and soft fruits from the various and approximately joined pistils of a bloom are distinctly extended and develop into fruits (similar to a goliath raspberry). The round or heart-formed greenish yellow, matured total natural product is pendulous on a thickened stalk; 5 cm (2.0 in.) to 10 cm (3.9 in.) in distance across with many round bulges and secured with a fine blossom. Fruits are shaped of freely sticking or free carpels (the matured pistels). The mash is white-tinged yellow, palatable, and sweetly smelling. Every carpel contains an oval, glossy, and smooth, dull chestnut to dark, 1.3 cm (0.51 in.) to 1.6 cm (0.63 in.) seed. A. squamosa is a lowland tropical or marginally subtropical species and native to the warmest and driest places in Central America, growing between latitudes 23 N and S, but also yields well in humid regions and is frequently
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FIGURE 1 Annona squamosa pulp.
FIGURE 2 Annona squamosa pulp with cross section showing seeds.
reported in cultivation in semiarid climates, such as northeastern Brazil (Pinto et al., 2005). In North America the species is reportedly found in “dryish, sandy substrates and dry hammocks” (Flora of North America Editorial Committee, 2015) and in Puerto Rico, “in thickets, on roadsides, and in valleys, in the southern districts” (Liogier and Martorell, 2000); on Saint John, US Virgin Island, this species is naturalized and found along roadsides and secondary forests. In the Bahamas it was reportedly growing in scrublands and similarly, in dry regions of north Queensland, Australia, it is found wild in pastures, forests, and along roadsides. The species occurs in moist tropical forests of Colombia and in coastal regions of Ecuador (NRCS, 2008).
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The matured sugar apple is normally torn open and the tissue sections delighted in while the hard seeds are isolated in the mouth and spat out. It is luscious to the point that it is definitely justified even despite the inconvenience. In Malaya, the tissue is squeezed through a strainer to dispose of the seeds and is then added to dessert or mixed with rain to make a cool drink.
HARVEST SEASON Two particular periods of vegetative flushes are normally found in Annonaceous organic products. Consequently, reap time is hard to judge, in light of the fact that blossoming can happen continuously. Alternately, hand fertilization can change the season of reaping (Pinto et al., 2005). Ripening the fruit starts in midsummer and lasts through Fall, but it can last to midwinter if there is no frost, giving a season from 3 to as long as 6 months. Sugar apple fruits are considered to be matured and ready for reaping when there is change in skin color and also exposing a creamy yellow skin when the segments spread. The fruits split open when permitted to develop on the tree, especially amid the blustery season. Poor organic product quality can happen subsequently of untimely reaping, and natural products left to age on the tree are frequently eaten by fowls and bats, and there is inclination of breaking and rotting when overdeveloped. In order to ensure the pulp mash is firm, fruit should be picked a couple days before achieving full development. The essential development record in sugar apple is the adjustments in shade of the skin from dim green to light green or greenish yellow (Pinto et al., 2005). Other indexes incorporates the presence of cream shading between portions on the skin and expanded surface smoothness of the different organic product carpels. They will mature off the tree in a couple days and can be held for a few more days in an icebox or refrigerated conditions. Being somewhat delicate and perishable, vast majority of the natural product is sold locally (Pinto et al., 2005).
ESTIMATED ANNUAL PRODUCTION Despite the fact that information on sugar apple annual production globally is lacking, the data gathered demonstrates that the possibility for increasing the sugar apple market is high in a certain countries. This species developed economies in the West Indies and Dominican Republic, the USA (Florida), the Middle East, India, Malaysia and Thailand. Despite the fact that the plant it is still viewed as a garden feature, the fruit is the most utilized part in the Philippines. In Brazil, sugar apple generation is gathered in Alagoas and Sa˜o Paulo states. Different ranges of generation are in Mexico, Egypt and India, where most fruits come to showcase from semiwild timberlands of the Deccan Plateau where sugar apple has been allowed to go wild (Pinto et al., 2005).
PLANT CHEMICALS Phytochemical examinations of the plant have demonstrated that they have a wide assortment of mixes such as acetogenins which were hostile to malarial, cytotoxic and the immunosuppressive exercises. Diterpenes discovered in the A. squamosa have counter-HIV rule and the counter platelet total movement. Some lignans and other hydroxyl ketones were likewise observed to be available in this plant. The quantity of alkaloids that was accounted for from this plant has a place within various classes, e.g., aporphine and benzoquinazoline. Squamocenin, annotemoyin, reticulatain-2, squamocin-I, squamocin-B, squamocin, motrilin, squamostatin-D, squamostatin-E, cherimolin-1, and cherimolin-2 were all extracted from the ethyl liquor concentrate of A. squamosa L. Other researchers found squamocenin, Annotemoyin, and reticulatain-2 (Pareek et al., 2011). Finding the above-mentioned chemical constituents in this plant reinforces the plant being used for different therapeutic qualities (Gajalakshmi et al., 2012).
FRUIT COMPOSITION Fruit contains the essential measures of calcium, phosphorus, starches, thiamine, riboflavin, fructose, glucose, sucrose, cellulose, hemi-cellulose, lignin, and peptic substances (Table 1). The sugars are the aftereffect of starch hydrolysis; the essential being glucose (11.75%) and sucrose (9.4%) and the first regular acids are citrus and malic acids. It is critical to pick sugar apple natural items with a high substance of dissolvable solids and ascorbic destructive, and for incite usage, succulent and enormous size and characteristic items are typically supported. The odor is a champion among the most perceived characteristics of the sugar apple and related to the maturing headway (Andrade, 2012). Sugar apple pound is imperceptibly granular, rich yellow or white, sweet with a not too bad flavor and low causticity. It is seen as the sweetest of the annona normal items. The consumable fragment is 28%37% of the total common item weight and seeds identify with 23%40%. Starches show in the squash join fructose (3.5%), sucrose (3.4%),
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401
TABLE 1 Chemical Composition of 100 g of Edible Pulp of Sugar Apple Fruits (Pareek et al., 2011) Components
Value
Water (g)
72.6 6 2.4 (68.675.9)
Proteins (g)
1.68 6 0.8 (1.22.4)
Lipids (g)
0.4 6 0.3 (0.11.1)
Carbohydrates (g)
19.6 6 1 (18.226.2)
Fiber (g)
1.4 6 0.6 (1.12.5)
Total acidity (g)
0.1
Ash (g)
0.7 6 0.1 (0.61.3)
Energy (calories)
96 6 10 (86114)
Calcium (mg)
26.2 6 6 (1744.7)
Phosphorous (mg)
42 6 14 (23.655.3)
Iron (mg)
0.8 6 0.5B (0.31.8)
Vitamin A (mg)
0.005 6 0.001 (0.0040.007)
Vitamin B1 (mg)
0.1 6 0.01 (0.100.11)
Vitamin B12 (mg)
0.13 6 0.05 (0.0570.167)
Vitamin B5 (mg)
0.9 6 0.3 (0.651.28)
Vitamin B6
0.2 mg (15%)
Ascorbic acid (mg)
37.38 6 4.62 (3442.2)
Thiamine (B1)
0.11 mg (10%)
Riboflavin (B2)
0.113 mg (9%)
Niacin (B3)
0.883 mg (6%)
Pantothenic acid (B5)
0.226 mg (5%)
Folate (B9)
14 μg (4%)
glucose (5.1%) and oligosaccharides (1.2%2.5%). volatiles for the most part conveyed by the leucine pathway (Pareek et al., 2011).
SENSORY CHARACTERISTICS Sensory characteristics of A. squamosa are mainly from the fruit in terms of appearance, odor, taste, texture. Sight Appearance: Shape (round or heart-shaped), color (greenish yellow), size (5 centimeters (2.0 in) to 10 centimeters (3.9 in) in diameter) Stimulation: colorful, grainy, foamy, greasy, shiny, transparency, dullness, gloss stringy, crystalline Smell Aroma: flavor, aromatics floral, rotten, acrid, musty, fragrant scented, pungent Taste: mouth feel and taste sweet, cool, bitter, zesty, hot, tangy, sour, sharp, sweet, salt, sour, bitter rich, salty Touch texture: mouth feel brittle, rubbery, gritty, bubbly, sandy, tender
Harvest and Postharvest Conservation A change in fruit surface color is the main maturity index for custard apple fruit harvesting. The farmers prefer harvesting sugar apple fruits in the morning. Manual harvesting and collection is followed by majority of the farmers with lower harvesting capacity 10 kg/person per day and higher harvesting losses 3%6%. During the whole harvesting season, sugar apple growers undertake 35 pickings. No farmers use a fruit picker for harvesting sugar apple. Average
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fruit yield per tree is 25 kg. Manual grading with very low capacity (25 kg/day per person) is undertaken by sugar apple farmers. Fruit size is the main grading criteria and the fruits are classified into three grades, Growers, who do the packaging, pack the fruits in bamboo baskets, boxes and plastic crates, with an average package size of 2025 kg. Sugar apple leaves and neem leaves are use as cushioning material. Postharvest handling losses of sugar apple fruit are in the range of 13%25%. Harvesting, grading, and transportation are the most problematic operations in postharvest handling of sugar apple fruits at the orchard level.
INDUSTRIAL APPLICATION Economic Value A. squamosa is a popular seasonal fruit with great economic importance in a number of tropical countries. It is also used as an agroforestry species, as a source of food and for honeybee cultivation. Some forms have a tendency to be seedy, which apparently deters some people from eating them, and research is needed to find a strain/provenance that produces larger and sweeter fruit containing fewer seeds. A. squamosa is usually grown as a backyard fruit tree. In some instances, A. squamosa is planted in parks or plazas as a shade and ornamental tree due to its attractive fruit color. The fruit of A. squamosa is usually eaten fresh, and is a source of carbohydrates, vitamins, and proteins. The fruit is also utilized commercially as a flavoring for icecream and can also be made into sherbet, and the pulp, after removing the seeds, is passed through a strainer or homogenized to make a delicious and refreshing drink. Sugar apple pulp is slightly granular, creamy yellow or white, sweet, with a good flavor and low acidity, it is believed to be the sweetest of the family. The wood of A. squamosa is used for fuel wood. It is soft, close-grained and grayish-white, with a density of about 600 kg/m3. The leaves, bark, roots, seeds and fruit of A. squamosa have various important medicinal uses. The green fruit and seed have effective vermicidal and insecticidal properties and are used as astringents in diarrhea and dysentery. The seeds contain 45% of a yellow, nondying oil which is an irritant poison for lice. Crushed leaves are applied as an effective cure for ulcers and malignant sores. A poultice from fresh leaves is used for dyspepsia and when mixed with oil is used for diseases of the scalp. Crushed fresh leaves are applied to the nasal area in cases of fainting spells. A decoction of roots is used as a drastic purgative. The astringent bark, leaves, unripe fruit and seed can be used as a source of the alkaloid anonaine.
REFERENCES Andrade, S., 2012. Physical, chemical and biochemical changes of sweetsop (Annona squamosa L.) and golden apple (Spondias citherea Sonner) fruits during ripening. J. Agric. Sci. Technol. B. 2 (11B), 1148. Bhattacharya, A., Chakraverty, R., 2016. The pharmacological properties of Annona squamosa Linn: a review. Int. J. Pharm. Eng. 4 (2), 692699. Flora of North America Editorial Committee, 2015. Flora of North America North of Mexico. Missouri Botanical Garden and Harvard University Herbaria, St. Louis, Missouri and Cambridge, Massachusetts, USA. Gajalakshmi, S., Vijayalakshmi, S., Devi, R.V., 2012. Phytochemical and pharmacological properties of Annona muricata: a review. Int. J. Pharm. Pharm. Sci. 4 (2), 36. Liogier, H.A., Martorell, L.F., 2000. Flora of Puerto Rico and Adjacent Islands: A Systematic Synopsis. 2nd edition revised. La Editorial, University of Puerto Rico, San Juan, Puerto Rico, 382 pp. Moghadamtousi, S.Z., Fadaeinasab, M., Nikzad, S., Mohan, G., Ali, H.M., Kadir, H.A., 2015. Annona muricata (Annonaceae): a review of its traditional uses, isolated acetogenins and biological activities. Int. J. Mol. Sci. 16 (7), 1562515658. Natural Resources Conservation Service (NRCS), 2008. Plants profile Annona squamosa L. The Plants Database. United States Department of Agriculture, United States, pp. 417. Pandey, V., Giri, I., Singh, S., Srivastava, A., 2014. Pharmacognostical and physiochemical study on the leaves of Annona squamosa Linn. Int. J. Res. Pharm. Sci. 4 (2), 812. Pareek, S., Yahia, E.M., Pareek, O., Kaushik, R., 2011. Postharvest physiology and technology of Annona fruits. Food Res. Int. 44 (7), 17411751. PIER, 2015. Pacific Islands Ecosystems at Risk. HEAR, University of Hawaii, Honolulu, USA. Pinto, Ad.Q., Cordeiro, M., De Andrade, S., Ferreira, F., Filgueiras, Hd, Alves, R., et al., 2005. Annona species. International Centre for Underutilised Crops; University of Southampton, Southampton. Shenoy, C., Patil, M., Kumar, R., 2009. Antibacterial and wound healing activity of the leaves of Annona squamosa Linn. (Annonaceae). Res. J. Pharmacogn. Phytochem. 1 (1), 4450. UK Natural History Museum, 2014. Roots and Herbs-Sweetsop. Natural History Museum, London, UK.
FURTHER READING Dash, D., Patro, H., Tiwari, R.C., Shahid, M., 2011. Effect of organic and inorganic sources of N on growth attributes, grain and straw yield of rice (Oryza sativa). Int. J. of Pharm. Life Sci. 2 (4), 655660.
Tamarindo—Tamarindus indica Md. Salim Azad Khulna University, Khulna, Bangladesh
Chapter Outline Introduction Taxonomy Distribution and Habitat General Description Food Value Chemical Composition Harvesting and Storage Cultivars
403 403 404 404 406 406 406 407
Postharvest Uses Household Uses Medicinal Uses Industrial Uses Other Uses Propagation and Conservation Acknowledgment References Further Reading
407 408 408 408 409 409 410 410 412
INTRODUCTION Tamarindus indica L. is commonly known as tamarind. It is assumed that the word tamarind derived from the Arabic “Tamar-u’l-Hind” (Tamere-Hind means date of India) as the pulp of this fruits is similar to dried dates. This species has numerous local names (Ross, 2003; Lim, 2012) (Table 1). People from different countries use varying local names. This is a nontraditional tropical fruit tree species that grows on residential family yards (especially back or front side of the yards), public roads, graveyards, community gardens/orchards, and barren spaces or fallow lands sometimes in institutional and commercial areas. Although it is a nontraditional fruit tree, it has a lot of traditional uses in many countries.
Taxonomy T. indica is a member of Fabaceae family, Caesalpinioideae subfamily. Based on its morphology, it has 58 tribes. It is dicotyledonous diploid species, having chromosome number 2n 5 24 (Purseglove, 1987). The scientific classification of this species is as followed (Sources: Wikipedia and Scientific classification of fruits): Domain: Eukarya Kingdom: Plantae Subkingdom: Tracheobionta Division: Magnoliophyta Class: Liliopsida Subclass: Rosidae Order: Fabales Family: Fabaceae Subfamily: Caesalpiniodeae Genus: Tamarindus Species: Tamarindus indica Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00055-1 © 2018 Elsevier Inc. All rights reserved.
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TABLE 1 Different Local Names of Tamarindus indica in Different Parts of the World Country
Local Names
Bangladesh
Tamarind, Tetul
Brazil
Tamarindo
Canary Islands
Tamarindo
China
Manhan
Cuba
Tamarindo
Fiji
Amli, Imli
Guatemala
Tamarindo
Guinea
Ntemi, Ntomi, Tamarinde, Tamarini
Guyana
Tamarind, Tombi, Tombinyi
India
Ambliki, Ambali, Cheench, Cinca, Imli, Tamarind, Tateli, Tatul
Indonesia
Asam Jawa, Asem, Kaju Asam, Tamarind, Tamarindo
Japan
Tamarid
Madagascar
Tamarindo
Malaysia
Asam Jawa, Pokok asam jawa
Morocco
Timer hendi
Nicaragua
Slim, Tamarindo, Tamparanu, Tamrand
Nigeria
Ajagbon, Icheku oyibo, Tsaniya
Paru
Tamarindo
Puerto Rico
Tamarindo
Rodrigues Island
Tamarin
Saudi Arabia
Hamer
Senegal
Dakhar
Tanzania
Mkwaju
Thailand
Makham
West Indies
Tamarin des indes, Tamarind, Tame tamarind
Distribution and Habitat It is a leguminous tree probably indigenous to fertile areas throughout tropical Africa (Cameroon, Chad, Kenya, Madagascar, Nigeria, Sudan, Tanzania, Uganda, and Zimbabwe). It is cultivated in China, India, Sri Lanka, Nepal, Pakistan, Taiwan, and Bangladesh. It is also widely distributed in northern Australia, Brazil, Mexico, the Philippines, the United States, and Jamaica (Das and Alam, 2001). Tamarind grows well in humid areas where mean annual rainfall is higher than 1500 mm but cannot tolerate continuous frost. It prefers to some extent acidic well-drained loamy soil (pH 56), but can also grow in a huge range of soil types, from alluvial to limestone (rocky) soil (Khan and Alam, 1996).
GENERAL DESCRIPTION G
G
T. indica is an eye-catching tree containing almost a round canopy, can achieve a height of 1825 m with spreading branches (Fig. 1A). Leaves are alternate, even-pinnately compound; consist of 1020 pairs of small opposite leaflets. Leaflets are narrowly oblong, 1232 by 311 mm in size, pink or reddish in color when young, and dark green with reticulate
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405
FIGURE 1 Some pictures of Tamarindus indica: (A) tree containing huge amount of pods, (B) tamarind pod, (C) variation in pod size, (D) variation in sap length, (E) seeds, (F) seedling.
G
G
G
G
G
G
venation at maturity (Fig. 1B and F). The apex is nearly rounded, to some extent notched and asymmetric with a bunch of yellow hairs. A distinguish scar is observed following leaf shedding. Inflorescence raceme is in terminal, small, 510 cm long, yellowish-orange or pale green in color. Flowers are bisexual and 22.5 cm in diameter, fertile stamens—3, ovary linear, about 7 mm long. Pods are oblong (510 cm 3 2 cm), reddish brown, to some extent curved with rounded ends. Seeds are glossy, embedded in a thick, sticky, acid brown pulp adjacent to the seed cavities (Fig. 1B and C) (Coronel, 1991). T. indica is highly cross pollinated (Thimmaraju et al., 1977), takes places through insects. Self pollination is also possible. Seeds are hard and dispersed by man, animals, and other agents (storms). Wood is resistant and durable but having possibility of termite attack. The wood is a very good source of fuel for brick burning having a high calorific value of 4850 kcal/kg (NAS, 1979; Chaturvedi, 1985). The production of tamarind depends on genetic factors as well as environmental factors (Feungchan et al., 1996a). Production is higher in cross pollination compare to open pollination (Usha and Singh, 1996). High yielding varieties can produce 600800 kg fruits/tree per year. Seedling growth shows significant seasonal variation at nursery stages. Height growth and diameter growth showed significant correlation (Azad et al., 2014)
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Food Value T. indica is well documented for its appetizing fruit owing to its brown, sticky, sweet, and sour pulp usually used as aroma in various dishes and drinks. The juicy, soft, succulent, ripened fruit pulp usually is used in confectionery as a component of curries, chutnies, pickles, preserves, sherbets, and beverages (Das and Alam, 2001). Tamarind fruits contain several nutrient values, vitamins, electrolytes, minerals, and phytonutrients. The USDA National nutrient database reported tamarind nutritional value per 100 g as follows: energy—239 kcal, carbohydrates—62.5 g, protein 2.8 g, fat— 0.6 g, cholesterol (nil), and dietary fiber 5.1 g. Tamarind fruits (per 100 g) also contain vitamins (folates—14 μg, niacin—1.94 mg, pantothenic acid—0.143 mg, pyridoxine—0.066 mg, thiamin—0.428 mg, vitamin A—30 IU, vitamin C—3.5 mg, vitamin E—0.1 mg, vitamin K—2.8 μg); electrolytes (sodium—28 mg, potassium—628 mg); minerals (calcium—74 mg, copper—0.86 mg, iron—2.8 mg, magnesium—92 mg, phosphorus—113 mg, selenium—1.3 μg, zinc— 0.1 mg); and phytonutrients (carotene-β—18 μg, crypto xanthin-β—nil, lutein-zeaxanthin—nil).
Chemical Composition Phytochemical and pharmacological studies on T. indica indicate the existence of different components of essential elements, volatile components, phenolic substances, fatty acids, organic acids, antioxidative activities, antimicrobial activities, antibacterial activities, antisnake venom activities, antidiabetic, and antiinflammatory activities. The leaf contains 13 different components (in which linonene and benzyl benzoate predominant); root barks contain n-hexacosane, octacosanyl ferulate, eicosanoic acid, 21-oxobehenic acid, β-sitosterol, (1)-pinitol; seeds contains fatty acids, unsaponifiable matter (from the seed oil), polyphenols; and pulp contains different organic acids. The chemical composition of different elements are summarized below: G
G
G
G
G G G G
G
G G
G G
Essential elements: copper 0.76 mg/kg, iron 14.07 mg/kg, cadmium 3.36 mg/kg, arsenic 54.25 μg/kg, zinc 8.52 mg/kg, lead 0.27 mg/kg, sodium 10.9 mg/kg, potassium 7.16 mg/kg, calcium 20.2 mg/kg, magnesium 60.1 mg/kg, manganese 25.9 mg/kg, phosphorus 20.4 ppm (Khanzada et al., 2008). Volatile components: alpha humulene, alpha murolene, alpha pinene, alpha copaene, beta caryophyllene, beta pinene, beta elemene, gamma cadinene (Sagrero-Nieves et al., 1994). Phenolic components: oligomeric procyanidin tetramer (30.2%), procyanidin hexamer (23.8%), procyanidin trimer (18.1%), procyanidin pentamer (17.6%), procyanidin B2 (5.5%) and (2)-epicatechin (4.8%) (Sudjaroen et al., 2005). Fatty acid component: myristic acid (trace), lauric acid (trace), stearic acid (5.9%), palmitic acid (14.8%), oleic acid (27.0%), linolenic acid (5.6%), linoleic acid (7.5%), behenic acid (12.2%), arachidic acid (4.5%), lignoceric acid (22.3%) (Pitke et al., 1977). Keto acid: Alpha oxo-glutaric acid (Mukherjee and Laloraya, 1974). Ascorbic acid: 0.40.6 mg/100 g (Sulieman et al., 2015). Other organic acid components: lactic acid, citric acid, stearic acid, galacturonic acid, succinic acid, tartaric acid. Antioxidative components: 4-dihydroxyacetophenone, methyl 3,4-dihydroxybenzoate, 3,4-dihydroxy phenyl acetate (Tsuda et al., 1994); α,α-diphenyl-β-picrylhydrazyl (Siddhuraju, 2007). Antimicrobial component: tannins, saponins, sesquiterpenes, alkaloids and phlobatamins (Doughari, 2006); phenols and flavonoids (n-hexane, chloroform, ethyl acetate and n-butanol) (Escalona-Arranz et al., 2013). Antibacterial component: ciprofloxacin, gentamicin, aqueous extracts, hydroalcoholic extracts (Meher et al., 2013). Antisnake venom component: hyaluronidase, protease, 50 -nucleotidase enzyme, l-amino acid oxidase (Ushanandini et al., 2006). Antidiabetic components: mucilage and pectin (Ibrahim et al., 1995); (1)-pinitol (Jain et al., 2007). Antiinflammatory component: (1)-pinitol (Jain et al., 2007).
Harvesting and Storage Harvesting of tamarinds starts at the time of complete maturity. The maturity of tamarind depends on location, cultivars, climatic factors, and interaction amongst them. Ripening of a tamarind is usually considered the starting point for its harvest. Even individual fruits of the same tree become mature at different time. At the time of harvesting the pulp becomes brown to reddish brown. The testa becomes easily broken and cracks without any difficulties. The shells of the fruits slowly change to brown in color. The pulp becomes dehydrated and sticky. The seed becomes harder, dark brown in color, and glossy. Besides, tapping pods with fingers can also identify the maturity of fruits. The shells become easily broken at the time of tapping, if it is ready for harvesting (El-Siddig et al., 2006; Hiwale, 2015). Fruits
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407
TABLE 2 Variation of Chemical Composition Among Different Cultivars of Sweet Tamarind From Thailand (Feungchan et al., 1996a; El-Siddig et al., 2006) Cultivars
Tartaric Acid
Sugar
Acid/Sugar
Fiber
Jaehom
2.79
44.68
1:16
1.33
Kru-in
2.70
39.06
1:14
1.02
Pannanikom
2.34
47.71
1:20
1.10
Piyai
2.01
47.19
1:23
1.97
Praroj
2.70
43.09
1:16
0.88
Sithong
3.18
41.07
1:13
1.44
Sri Chompoo
2.39
42.52
1:18
1.96
TABLE 3 Some Important Cultivars Recognized in Asia (El-Siddig et al., 2006) Country
Cultivars
Thailand
Muen Chong, Sri Tong, Nam Pleung, Jac Hom, Kun Sun, Kru Sen, Nazi Zad, Sri Chompoo
Philippines
Cavite, Batangas, Bulacan and Laguna
India
Prathisthan, Periyakulam (PKM 1) Urigam
are harvested through shaking the trees/branches manually in majority of the countries. Sometimes nets are used to capture the fruits. Often some special mechanical devices are also used for harvesting tamarind. After harvesting, the hard shells are removed and fresh fruits are dried very often in the sun in rural households. The seeds are separated from pulp and pulps are stored in plastic bags or other homemade pots. Before storing pulp, it is processed by removing the fiber strands. The pulp is hard-pressed and preserved in most of the tamarind growing countries in Asia and Africa. The pulp is sold in the markets, small shops by weight basis. Sometimes the pods with shells are also sold in the markets. The price of the pulp depends on quality and condition of the pulp. Usually pulp in dry conditions can be retained for a long time (Feungchan et al., 1996b).
Cultivars Based on sweetness of tamarind pulp, two major types of tamarind were recognized in India, Thailand, and the Philippines (Table 2). They are classified as sweet and sour types. Sometimes cultivars are distinguished by tree form, flowering pattern, pod characteristics (pod length, shell color, weight, shape), pulp characteristics (pulp color, pulp content, pulp shell ratio, pulp sweetness, fiber content), number of seeds per pod, etc. Among the cultivar characters, pulp color is considered the main characteristic because it is an indicator of quality of tamarind. Generally red colored pulp produces the best quality testy tamarind. There are a lot of cultivars in Asia (India, the Philippines, and Thailand) and Africa (Uganda and Kenya). Some important recognized tamarind cultivars are shown in Table 3.
POSTHARVEST USES Tamarind is a multipurpose tree species, with versatile uses. It is used for various household, medicinal, and industrial purposes. The exceptional flavor, taste (sweet/sour) of the pulp is well known for cooking a variety of dishes and drinks. The bark, root, leaves, fruit, and wood (every part of the tree) contribute to the subsistence of rural people. Some commercial applications are also well recognized in industrial uses and there is great potential for further development in different purposes.
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Household Uses Tamarind is familiar for its delicious appetizing fruit because of its sticky, soft, succulent, and sweet/sour tasty brown pulp usually used in various dishes and drinks. Some household applications of tamarind are given below: G G
G G G
G
G
G
G
The immature pods (green) are frequently used by the females as snacks (dipped in salt) in some Asian countries. The brown mature pulp is used for many purposes in households as a constituent in chutnies, pickles, curries, and beverages. Juice, candy, jam, and syrup are also prepared from it (Jayaweera, 1981; Das and Alam, 2001). Tamarind pulp is also used in cooking to detoxify poisonous yams in some African countries. The juice is used to preserved fish in some rural areas of Sri Lanka and some other South Asian countries. Tamarind juice is also used as traditional drink in many Asian, African and South American countries. For example, “Jugo” and “fresco de tamarindo” are popular traditional drinks made with tamarind in South America (FAO, 1988). The seeds are consumed by the rural people after boiling or roasting in some places of India. Sometimes they prepare tamarind flour for bread making, or Indian chapattis/cake making (Purseglove, 1987). The seedlings, immature leaves, flowers, and pods are used as vegetables, salads, and soups in many countries. “Chindar” is a popular dish made of tamarind leaves in some parts of India (Coronel, 1991). The wood is used as charcoal and fuel woods for household utilization by the rural people. It is also used for brick burning purposes due to high calorific value of 4850 kcal/kg (Gohil and Singh, 2003). Tamarind wood is also used for making household furniture, wheels, rice pounders, mortars, tent pegs, cart shafts/ axles, boats, toys, tools, and printing blocks.
Medicinal Uses T. indica has fantastic medicinal properties. Lots of rural people use different parts of this species for folk treatments of different ailments. A lot of medicines/drugs have already been produced by using different parts of this species. Some important medicinal values are listed below. G G
G
G
G
G
G
G
G
G G G
Tamarind is a very good as blood sugar decreasing medicines. It is very popular for cardiac diseases. The fruit is used to cure intestinal ailments, reduce fever, and is efficient against scurvy. Tamarind is also used to assist for the treatment of malarial fever (Timyan, 1996). Tamarind seed powder is commonly used for dysentery, chronic diarrhea, jaundice eye diseases, and ulcers in some Asian countries (Rama Rao, 1975; Jayaweera, 1981). The pulp is used for the treatment of sunstroke, effects of alcohol and “ganja” (Cannabis sativa L.) and Datura poisoning (Gunasena and Hughes, 2000). Tamarind pulp is a very good medicine for paralyzed people to restore sensation. It is also used for treatment of painful and wounded throats (Chaturvedi, 1985). The leaves and pulp are used for softening the skin. Both of them are regarded as a diaphoretic and purgative in some Latin American countries. The pulp is also used for the treatment of leprosy. It is also used as an ointment for rheumatism in some southeast Asian countries. Tamarind seeds mixed with lime juice is used for prevention of pimples formation on face and seed oil is applied for hairdressing in some countries like Indonesia. The pulp and leaves are very useful for liver ailments, cholagogue, urinary troubles, habitual constipation, and throat infections. The bark is also used for the treatment of urinary discharges and gonorrhea. Flowers are used for conjunctivitis and also for the treatment of jaundice and piles. Tamarind has antioxidant, antifungal, antimicrobial, antibacterial, antiinflammatory, antidiabetic and antisnake venom properties (Ray and Majumdar, 1976; Bibitha et al., 2002; Ushanandini et al., 2006; Havinga et al., 2010).
Industrial Uses Tamarind is already used as a raw material for the production of several industrial products like tamarind juice concentrate, tamarind pulp powder, tamarind kernel powder (TKP), pectin, tartaric acid, tartarates, and alcohol (Mathur and Mathur, 2001). It has a lot of potential industrial uses as follows.
Tamarindo—Tamarindus indica
G
G
G
G
G
409
The chief industrial use of the seeds is the production of TKP. It is used as preservatives, paper adhesive, textile sizing, textile printing, and weaving and manufacture of jute products (Shankaracharya, 1998; Khoja and Halbe 2001; Lima et al., 2003). Tamarind seed is also used as adhesive filler in the plywood industry. It is also used as a stabilizer for brick industries that combine sawdust briquettes and as a thickener for a number of explosives. Tamarind gum (stiff gel) is commercially accessible for the improvement of texture and viscosity processed foods which are used for thickening, gelling and stabilizing in food and vegetable processing industries (Sone and Sato, 1994). TKP up to 15% is allowed in bread and biscuits factories. TKP reduces springiness and particular volumes in bread (Bhattacharya et al., 1994). A mixture of TKP and low cost jelly could be used as an alternative to expensive pectin for making jams, jellies, and marmalades. Tamarind polysaccharides obtained from seed kernels can produce gels over a wide range of pH and can be used as an alternative to fruit pectin.
Other Uses G
G G
G
G
G G
G
Tamarind is a well-known fodder species. The leaves and seeds are used to feed domestic animals (cattle and goats). In general, leaves contain higher crude protein than seeds, and required almost no preparation for feeding (Alam et al., 1985). Sometimes trees grown in woodland are browsed by wild elephants in Zambia (Kaitho et al., 1988; Storrs, 1995). This species is considered as a component of agroforestry because of its potential nitrogen fixing ability, tolerance of infertile soil, and erosion control (Das and Alam, 2001). Tamarind is used in farming systems (intercropping) due to its multipurpose uses in many tropical countries. Farmers integrate many species including livestock and agricultural crops with tamarind trees in India to reduce the uncertainty of crop failure. It is a very good ornamental tree usually planted along roadsides, avenues, river banks, and in parks (Meghwal, 1997). It is also used as shade tree, shelter belt, and wind breaks due to its resistance to storms. In some countries tamarind is used as firebreak as grasses cannot grow under heavy shade of this tree (Troup, 1921; Salim et al., 1998). A certain portion of the rural folk and tribes living in the forest have beliefs that tamarind is a highly worshipped and sacred tree (Singha, 1995).
PROPAGATION AND CONSERVATION Seed germination and seedling growth are preconditions for conservation of genetic resources and sustainable uses of different products of specific species which depends on perception of genetic inconsistency, evolutionary forces, and breeding system in tree improvement (Azad et al., 2014). Tamarind is commonly grown from seeds. It can also be grown from vegetative propagation (macrovegetative propagation or micropropagation). Vegetative propagation is useful for conservation of different genotypes. Germination from seed is inexpensive and very important for rural tree breeders. It can be used as root stocks to produce large number of grafted ortet. Tamarind seed germination is influenced by different presowing treatments. Different researchers noticed various responses according to the different methods used. Seed germination required 720 days in controlled conditions (Azad et al., 2013). It can vary by seed sources, climatic requirements, and cultivars as well. On an average, it starts to germinate from 13 days of seed sowing. Sometimes it may take 30 days to complete the germination process. El-Siddig et al. (2001) recommended 45 days to allow for maximum seed germination. Azad et al. (2013) noticed 58% seed germination in the control situation, and noticed that presowing significantly enhanced seed germination. They found almost 82% seed germination in cold water treatment (immersion in cold water for 24 h at 4 C) and scarification with sand paper. El-Siddig et al. (2001) noticed acid treatment (immersion of seeds in 97% sulfuric acid for 45 min at room temperature) is an effective method for rapid and synchronous germination of tamarind. The coppicing ability of tamarind is great. Thus the stem cutting is therefore the cheapest methods for tamarind propagation for small scale plantation. A number of protocols have already developed for rooting of cuttings (Srivasuki et al., 1990; Swaminath et al., 1990). However, Mascarenhas et al. (1987) reported that rooting of a cutting is not successful for this species. Different budding and grafting methods are reliable methods for conservation of specific
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attributes of specific genotypes (Swaminath and Ravindran, 1989; Pathak et al., 1992). Tamarind can also be propagated by tissue culture but only a few literatures report on it due to the callogenic nature of this species. To overcome these problems, cotyledons, cotyledonary nodes, and shoot tips were successfully used as explants for tamarind tissue culture (Splittstoesser and Mohamed, 1991).
ACKNOWLEDGMENT The author acknowledges the students of Forestry and Wood Technology Discipline, Khulna University, Bangladesh for providing their help and cooperation to prepare this chapter.
REFERENCES Alam, M.K., Siddiqi, N.A., Das, S., 1985. Fodder Trees of Bangladesh. Bangladesh Forest Research Institute, Chittagong. Azad, M.S., Nahar, N., Matin, M.A., 2013. Effects of variation in seed sources and pre-sowing treatments on seed germination of Tamarindus indica: a multi-purpose tree species in Bangladesh. Forest Sci. Pract. 15 (2), 121129. Azad, M.S., Nahar, N., Mollick, A.S., Matin, M.A., 2014. Variation in seedling growth of Tamarindus indica (L.): a threatening medicinal fruit tree species in Bangladesh. J. Ecosyst. Available from: http://dx.doi.org/10.1155/2014/270956. Bhattacharya, P.K., Bal, S., Mukherji, R.K., 1994. Studies on the characteristics of some products from tamarind (Tamarindus indica L.) kernels. J. Food Sci. Technol. (India) 31 (5), 372376. Bibitha, B., Jisha, V.K., Salitha, C.V., Mohan, S., Valsa, A.K., 2002. Antibacterial activity of different plant extracts. Ind. J. Microbiol. 42 (4), 361363. Chaturvedi, A.N., 1985. Firewood Farming on the Degraded Lands of Gangetic Plain. Uttar Pradesh Forest Bulletin No. 50, 1. Government of India Press, Lucknow, 286 pp. Coronel, R.E., 1991. Tamarindus indica L. in plant resources of South East Asia. Wageningen; Pudoc. no. 2. In: Verheij, E.W.M., Coronel, R.E. (Eds.), Edible Fruits and Nuts. PROSEA Foundation, Bogor, pp. 298301. Das, D.K., Alam, M.K., 2001. Trees of Bangladesh. Bangladesh Forest Research Institute (BFRI), Chittagong. Doughari, J.H., 2006. Antimicrobial activity of Tamarindus indica Linn. Trop. J. Pharm. Res. 5 (2), 597603. El-Siddig, K., Ebert, G., Ludders, P., 2001. A comparison of pretreatment methods for scarification and germination of Tamarindus indica L. seeds. Seed Sci. Technol. 29 (1), 271274. El-Siddig, K., Gunasena, H.P.M., Prasad, B.A., Pushpakumara, D.K.N.G., Ramana, K.V.R., Vijayanand, P., et al., 2006. Tamarind, Tamarindus indica. Southampton Centre for Underutilised Crops, Southampton. Escalona-Arranz, J.C., Pe´rez-Rose´s, R., Urdaneta-Laffitai, I., Morris-Quevedo, H., Camacho-Pozo, M.I., Rodriguez-Amado, J., et al., 2013. Role of polyphenols in the antimicrobial activity of ethanol Tamarindus indica L leaves fluid extract. Bol. Latinoam. Caribe Plant. Med. Aroma´t. 12 (5), 516522. FAO, 1988. Fruit Bearing Trees. Technical notes. FAO-SIDA Forestry Paper 34, 165167. Feungchan, S., Yimsawat, T., Chindaprasert, S., Kitpowsong, P., 1996a. Tamarind (Tamarindus indica L.) plant genetic resources in Thailand. Thai J. Agric. Sci., Special Issue. 1, 111. Feungchan, S., Yimsawat, T., Chindaprasert, S., Kitpowsong, P., 1996b. Evaluation of tamarind cultivars on the chemical composition of pulp. Thai J. Agric. Sci., Special Issue. 1, 2833. Gohil, D.I., Singh, S.P., 2003. Studies on some multipurpose tree species as a source of rural energy. In: Narain, P., Kathju, S., Kar, A., Singh, M.P., Praveen, K. (Eds.), Human Impact on Desert Environment. Arid Zone Research Association of India, Jodhpur, pp. 426429. Gunasena, H.P.M., Hughes, A., 2000. Tamarind, Tamarindus indica L. International Centre for Underutilised Crops, Southampton. Havinga, R.M., Hartl, A., Putscher, J., Prehsler, S., Buchmann, C., Vogl, C.R., 2010. Tamarindus indica L. (Fabaceae): patterns of use in traditional African medicine. J. Ethnopharmacol. 127, 573588. Hiwale, S., 2015. Tamarind (Tamarindus indica L.). Sustainable Horticulture in Semiarid Dry Land. Book Part II. Springer, India, pp. 197212. Available from: http://dx.doi.org/10.1007/978-81-322-2244-6_13. Ibrahim, N.A., El-Gengaihi, S.E., El-Hamidi, A., Bashandy, S.A.E., Svoboda, D.A., 1995. Chemical and biological evaluation of Tamarindus indica L. growing in Sudan. International Symposium on Medicinal and Aromatic Plants xxiv. International Horticultural Congress. Acta Horticult. 390, 5157. Jain, R., Jain, S., Sharma, A., Ito, H., Hatano, T., 2007. Isolation of (1)-pinitol and other constituents from the root bark of Tamarindus indica Linn. J. Nat. Med. 61, 355356. Jayaweera, D.M.A., 1981. Medicinal Plants (Indigenous and Exotic) Used in Ceylon. Part 111. Flacourtiaceae-Lytharaceae. A publication of the National Science Council of Sri Lanka, pp. 244246. Kaitho, R.J., Nsahlai, I.V., Williams, B.A., Umunna, N.N., Tamminga, S., van Bruchem, J., 1988. Relationships between preference, rumen degradability, gas production and chemical properties of browses. Agroforestry Syst. 39, 129144. Khan, M.S., Alam, M.K., 1996. Homestead Flora of Bangladesh. Forestry Division, Bangladesh Agricultural Research Council (BARC), Dhaka. Khanzada, S.K., Shaikh, W., Shahzadi, S., Kazi, T.G., Usmanghani, K., Kabir, A., 2008. Chemical constituents of Tamarindus indica. Medicinal plant in Sindh. Pak. J. Bot. 40, 25532559.
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Khoja, A.K., Halbe, A.V., 2001. Scope for the use of tamarind kernel powder as a thickener in textile printing. Man-Made Text. India 44 (10), 403407. Lim, T.K., 2012. Tamarindus indica. Edible Medicinal and Non-medicinal Plants. vol. 2, Fruits. Springer, The Netherlands, pp. 879905. Available from: http://dx.doi.org/10.1007/978-94-007-1764-0_95. Lima, D.U., Oliveira, R.C., Buckeridge, M.S., 2003. Seed storage hemicelluloses as wet-end additives in papermaking. Carbohydr. Polym. 52 (4), 367373. Mathur, N.K., Mathur, V., 2001. Industrial polysaccharides-9 tamarind seed polysaccharide and tamarind kernel powder. Chem. Weekly. 46 (51), 143150. Mascarenhas, A., Nair, S., Kulkarni, V.M., Agawal, O.C., Khushpee, S.S., Mehta, V.J., 1987. In: Bonga, J.M., Durzan, D.J. (Eds.), Cell and Tissue Culture in Forestry, vol. 3. Martinus Nijhoff, Dordrecht. Meghwal, P.R., 1997. Exploiting under-utilized fruits of the arid zone. Indian Hortic. 42 (3), 2627. Meher, B., Dash, D.K., Bhoi, B.B., 2013. Evaluation of in vitro antioxidant and antimicrobial properties of hydroalcoholic and aqueous seeds extracts of Tamarindus indica L. World J. Pharm. Pharm. Sci. 3 (1), 436452. Mukherjee, D., Laloraya, M.M., 1974. Keto acids in leaves, developing flowers and fruits of Tamarindus indica. Plant Biochem. J. 1, 53. NAS, 1979. Tropical Legumes: Resources for the Future. NAS, Washington, DC, pp. 117121. Pathak, R.K., Ojha, C.M., Dwivedi, R., 1992. Adopt patch budding for quicker multiplication in tamarind. Indian Hortic. 36 (2), 17. Pitke, P.M., Singh, P.P., Srivastava, H.C., 1977. Fatty acid composition of tamarind kernel oil. J. Am. Oil Chem. Soc. 54, 592. Purseglove, J.W., 1987. Tropical Crops. Dicotyledons. Longman Science and Technology, London, pp. 204206. Rama Rao, M., 1975. Flowering Plants of Travancore. Bishen Singh Mahendra Pal Singh, Dehra Dun, p. 484. Ray, P.G., Majumdar, S.K., 1976. Antimicrobial activity of some Indian plants. Econ. Bot. 30 (4), 317320. Ross, I.A., 2003. Tamarinddus indica. Medicinal Plants of the World. Vol. 1, Chemical Constituents, Traditional and Modern Medicinal Uses. Humana Press, pp. 455463.. Available from: http://dx.doi.org/10.1007/978-1-59259-365-1_27 Sagrero-Nieves, L., Bartley, J.P., Provis-Schwede, A., 1994. Supercritical fluid extraction of the volatile constituents from tamarind (Tamarindus indica L.). J. Essent. Oil Res. 6 (5), 547548. Salim, A., Simons, A., Waruhin, A., Orwa, C., 1998. Agroforestry Tree Database: A Tree Species Reference and Selection Guide and Tree Seed Suppliers Directory. International Council for Research in Agroforestry, Nairobi. Shankaracharya, N.B., 1998. Tamarind chemistry, technology and uses a critical appraisal. J. Food Technol. 35 (3), 193208. Siddhuraju, P., 2007. Antioxidant activity of polyphenolic compounds extracted from defatted raw and dry heated Tamarindus indica seed coat. Food Sci. Technol. 40 (6), 982990. Singha, R.K., 1995. Biodiversity conservation through faith and tradition in India. Some case studies. Int. J. Sustainable Dev. World Ecol. 2 (4), 278284. Sone, Y., Sato, K., 1994. Measurement of oligosaccharides derived from tamarind xyloglucan by competitive ELISA assay. Biosci. Biotechnol. Biochem. 58, 22952296. Splittstoesser, W.E., Mohamed, Y., 1991. In vitro shoot regeneration of tamarind (Tamarindus indica L.) and carob (Ceratonia siliqua) with thidiazuron. In: Proceedings of the Inter-American Society for Tropical Horticulture. 35-37th Ann. Meeting, Vina-del-mar, Chile. 7-12 Oct, pp. 68. Srivasuki, K.P., Reddy, R.D., Reddy, K.K., 1990. Rooting of terminal cuttings of Tamarindus indica Linn. Indian For. 116, 984985. Storrs, A.E.G., 1995. Know Your Trees. Some Common Trees Found in Zambia. Regional Soil Conservation Unit (RSCU), Zambia. Sudjaroen, Y., Haubner, R., Wurtele, G., Hull, W.E., Erben, G., Spiegelhalder, B., et al., 2005. Isolation and structure elucidation of phenolic antioxidants from Tamarind (Tamarindus indica L.) seeds and pericarp. Food Chem. Toxicol. 43, 16731682. Sulieman, A.M.E., Alawad, S.M., Osman, M.A., Abdelmageed, E.A., 2015. Physicochemical characteristics of local varieties of Tamarind (Tamarindus indica L), Sudan. Int. J. Plant Res. 5 (1), 1318. Swaminath, M.H., Ravindran, D.S., 1989. Vegetative propagation of fruit yielding tree species. My Forest. 25 (4), 57360. Swaminath, M.H., Ravindra, D.S., Mumtaz, J., 1990. Propagation of tamarind through stem cuttings. My Forest. 26 (2), 207208. Thimmaraju, K.R., Narayana Reddy, M.A., Swamy, N., Sulladmath, U.V., 1977. Studies on the floral biology of tamarind (Tamarindus indica L.). Mysore J. Agric. Sci. 11, 293298. Timyan, J., 1996. Important Trees in Haiti. Southeast Consortium for International Development, Washington, DC. Troup, R.S., 1921. The Silviculture of Indian Trees, Vol.11. Leguminosae (Caesalpinieae) to Verbenaceae. 7. Tamarindus indica L. Clarendon Press, Oxford, pp. 263363. Tsuda, T., Watanabe, M., Ohshima, K., Yamamoto, A., Kawakishi, S., Osawa, T., 1994. Antioxidative components isolated from the seed of tamarind (Tamarindus indica L.). J. Agric. Food Chem. 42 (12), 26712674. Usha, K., Singh, B., 1996. Influence of open and cross pollination on fruit set and retention in tamarind (Tamarinds indica L.). Rec. Hortic. 3 (1), 6061. Ushanandini, S., Nagaraju, S., Kumar, K.H., Vedavathi, M., Machiah, D.K., Kemparaju, K., et al., 2006. The anti-snake venom properties of Tamarindus indica (leguminosae) seed extract. Phytother. Res. 20 (10), 851858.
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FURTHER READING ,http://www.fruitvs.com/en/scientific-classification-of-tamarind/model-81-5.. ,https://en.wikipedia.org/wiki/Tamarind. available on April 1, 2016. ,https://ndb.nal.usda.gov/ndb/foods/show/2391?fgcd5&manu5&lfacet5&format5&count5&max535&offset5&sort5&qlookup5tamarind. available on April 1, 2016. Prasad, A., 1963. Studies on pollen germination in Tamarindus indica L. Madras Agric. J. 50, 202203.
Tarap—Artocarpus odoratissimus Fazleen Izzany Abu Bakar and Mohd Fadzelly Abu Bakar Universiti Tun Hussein Onn Malaysia (UTHM), Johor, Malaysia
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry Chemical Composition and Nutritional Value Including Vitamins, Mineral, Phenolics and Antioxidant Compounds
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Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgment References
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CULTIVAR ORIGIN AND BOTANICAL ASPECTS Kingdom Order Family Genus Species
Plantae Urticales Moraceae Artocarpus Artocarpus odoratissimus
The Artocarpus genus comprises approximately 50 species that are native to south and southeast Asia. One of the species is Artocarpus odoratissimus, known as tarap or terap (Malay), marang (English), pingan (Iban), timadang (kadazandusun), pi-ien (Bidayuh), marang (Sulu), keiran (Kelabit), madang (Lanao), loloi (Tagalog), and khanun sampalor (Thailand) (Subhadrabandhu, 2001). Its closest relatives are Artocarpus altilis (Breadfruit), Artocarpus integer (Cempedak) and Artocarpus heterophyllus (Jackfruit). In Asia, the genus of Artocarpus has been used extensively by the local community in agriculture, industry, and as a food (Tang et al., 2013). For instance, A. heterophyllus fruit pulp is used as a dessert or preserved in syrup while the leaves of this plant are used as food wrappers in cooking. A. odoratissimus belongs to the family of Moraceae and can be found mainly on Borneo Island especially Brunei, Kalimantan (Indonesia), Sabah, and Sarawak (Malaysia). However, the fruit is now cultivated in other southeast Asian countries such as Thailand and the Philippines (Mindoro, Mindanao, Basilan, and Sulu). Nowadays, it has also been introduced into Australia, Brazil and some other tropical countries. Today it has been cultivated in many areas for its edible fruit. The A. odoratissimus tree cannot tolerate cold temperatures (under 7 C) and it can grow between latitude 15 degees north and south. In the state of Sarawak, Malaysian Borneo, this fruit is found in secondary forests up to 1000 m altitude on sandy clay soils. It is an evergreen tree reaching 25 m in height and 40 cm in diameter (trunk) as shown in Fig. 1. The twigs are 410 mm (thickness) with long yellow to red hair. The dark green leaves are large at 1650 cm (long) and 1128 cm (wide) in size and the shape is round at the stem and narrower at the tip. The male and female flowers grow separately on the same tree and the female flowers grow in inflorescences. It is well known that the fruit is tasty, soft flavored and considered superior to both A. heterophyllus (jackfruit) and A. integer (cempedak).
Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00041-1 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 The Artocarpus odoratissimus tree.
HARVEST SEASON A. odoratissimus (tarap) is one of the seasonal fruits where the harvest season is usually at the beginning of the rainy season between August and January depending on its location. For instance in the Philippines, the harvest season in Luzon is between May and July while in Mindanao, it is between August and December. In Malaysia, specifically Sarawak, the fruiting season lies between October and January, while in northern Queensland, Australia, the fruit is harvested over a two-month period with a peak in February, following flowering in October until November. The fruit is usually harvested green and allowed to ripen off and it becomes hard and brittle as the fruit matures. Normally, the mature fruits are harvested by using a curved knife attached to the end of a long bamboo pole and it must be done in a correct way to ensure the fruit might is not shattered after falling to the ground. After the fruit has been harvested, it must be consumed as soon as possible due to its short shelf life.
ESTIMATED ANNUAL PRODUCTION In the Philippines, A. odoratissimus fruit is reported to produce 45 t of fruits per acre and in 1987, this country had 1700 ha under cultivation with a total production of 7900 t valued at about 15 million pesos (US$750,000). In Thailand, this fruit has low yield when compared to Artocarpus heterophyllus (jackfruit) and mostly it is cultivated as a home garden plant as practiced by some villages in southern Thailand (Subhadrabandhu, 2001). In fact, some people might not know the existence of this fruit as it is categorized as an underutilized fruit tree. In the state of Sarawak, Malaysia Borneo, A. odoratissimus is one of the most highly esteemed fruits and there is a ready local market for the small quantities supplied, while in the state of Sabah, Malaysian Borneo, the nation imported fruits worth RM1.8 billion while exports amounted to RM615 million based on the Agriculture Department statistics in 2012. This could be seen as a motivation to the fruit farmers in Sabah to take the initiative to enhance the production of local fruits. If the fruits can be processed to make them marketable, there might be some possibilities in expanding its plantation.
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FRUIT PHYSIOLOGY AND BIOCHEMISTRY The fruit of A. odoratissimus is large with 16 cm (length), 13 cm (diameter) and up to 2.5 kg (weight) and it can be divided into various parts such as flesh, pulp, skin, and seed where the flesh is a dominant part of the fruit which represents 50%60% of the total weight while the pulp, skin and seed represent 40%50% of the total weight and normally they are discarded (Abu Bakar et al., 2009). The fruit is roundish oblong, regular, and thickly studded with short, greenish yellow spines and has bristles on its skin as well as soft yellowish white flesh attached to a central core (Fig. 2) which is juicy and aromatic (Coronel, 1983), while each segment of the flesh contains a seed about 8 3 15 mm in size (Galang, 1955). In addition, the appearance of the fruit can be considered to have the intermediate shape between Artocarpus heterophyllus (Jackfruit) and Artocarpus altilis (Breadfruit). In terms of the ecology, this fruit grows best in regions with abundant and equally distributed rainfall on loamy or sandy clay under cultivation like in the Philippines but the trees from this genus are sensitive towards changes in the soil acidity and the temperature of surrounding environment. Moreover, it is propagated from the seeds by which the fresh seeds germinate easily and the vegetative propagation by budding, grafting, and inarching can also be done for this fruit. Once the fruit undergoes the ripening process, the outer rind turns from green to brownish-yellow and becomes soft. The softening of the fruit is due to the degradation of pectin by pectinase. Additionally, the volatile compounds synthesized during the fruit ripening may produce the strong sweet aroma while the taste is provided by many nonvolatile compounds such as sugars. Throughout the ripening process, the total soluble solids and total sugars increase significantly. The phenolic compounds present in the fruit might also affect the taste. When the fruit is being opened, the oxidative browning might have occurred and thus it should be consumed within few hours after opening as it deteriorates rapidly in taste whilst it oxidizes.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING VITAMINS, MINERAL, PHENOLICS AND ANTIOXIDANT COMPOUNDS In 2013, Tang et al. reported the proximate analysis of A. odoratissimus flesh and seed (Table 1). Based on the results, the carbohydrate content of the A. odoratissimus flesh (12.025.2 g) was higher than the seed (1.22.3 g) and carbohydrate is the dominant nutrient present in the fruit due to the high sugar contents such as fructose, glucose, and sucrose. Among these three sugars, fructose is the dominant sugar and hence it can be concluded that fructose contributes the most to the sweetness of the fruit. In contrast, the seed contains higher ash, protein, fat, and fiber contents than the flesh with 1.01.5 g, 5.16.6 g, 10.128.1 g, and 3.24.7 g respectively. Ash indicates the total mineral content in the foods and most of the mineral contents in the seed were higher than the flesh of the fruit, such as potassium, magnesium, calcium and iron. The crude fat only obtained in the A. odoratissimus seed ranged from 10.128.1 g/100 g and the fatty acids present were hexanoic acid, octanoic acid, hexadecanoic acid (the most abundant), octadecanoic acid and tetracosanoic acid. The protein content in the flesh and seed of this fruit is affected by the stage of maturity and the growing environment. FIGURE 2 The yellowish white flesh of Artocarpus odoratissimus.
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TABLE 1 The Nutritional Composition of Artocarpus odoratissimus Nutritional Composition
Flesh (nutrients per 100 g)
Seed (nutrients per 100 g)
Ash
0.60.8 g
1.0 1.5 g
Carbohydrate
12.025.2 g
1.2 2.3 g
Crude protein
1.2 1.5 g
5.16.6 g
Crude fiber
0.801.30 g
3.24.7 g
Fat
Nil
10.128.1
Moisture
67.9%73.4%
31.0%55.0%
Potassium
176298 mg
352443 mg
Magnesium
14.831.3 mg
103132 mg
Sodium
1.151.70 mg
0.93.8 mg
Calcium
0.481.35 mg
1.53.0 mg
Iron
0.290.53 mg
0.81.2 mg
Nickel
0.010.06 mg
0.130.29 mg
Cobalt
0.110.26 mg
0.100.15 mg
Manganese
0.020.93 mg
0.278.64 mg
Copper
0.390.67 mg
0.580.83 mg
Zinc
0.170.45 mg
0.711.83 mg
Cadmium
0.01040.0149 mg
0.01250.0172 mg
NIL, not in list. Source: Adapted from Tang, Y.P., Linda, B.L.L., Franz, L.W., 2013. Proximate analysis of Artocarpus odoratissimus (Tarap) in Brunei Darussalam. Int. Food Res. J. 20(1), 409415.
TABLE 2 The Phytochemical Contents of Artocarpus odoratissimus Phytochemical contents
Flesh
Seed
Peel
Total phenolic content
3.53 6 0.33 mg
13.72 6 0.87 mg
42.38 6 0.20 mg
Total flavonoid content
1.23 6 0.09 mg
10.18 6 0.81 mg
36.78 6 0.28 mg
Total anthocyanins content
11.02 6 0.38 mg
3.8 6 0.34 mg
NIL
Total carotenoid content
0.79 6 0.23 mg
0.67 6 0.14 mg
0.86 6 0.04 mg
Note: Total phenolic content is expressed as mg gallic acid equivalents in 1 g of dry sample (mg GAE/g). Total flavonoid content is expressed as mg catechin equivalents in 1 g of dry sample (mg CE/g). Total anthocyanin was expressed as mg cyanidine-3-glucoside equivalent in 100 g of dry sample. Total carotenoid content is expressed as mg β-carotene equivalents in 1 g of dry sample. NIL, not in list Source: Adapted from Abu Bakar, M.F., Mohamed, M., Rahmat, A., Fry, J., 2009. Phytochemicals and antioxidant activity of different parts of bambangan (Mangifera pajang) and tarap (Artocarpus odoratissimus). Food Chem. 113(2), 479483 and Abu Bakar, M.F., Abdul Karim, F., Perisamy, E., 2015. Comparison of phytochemicals and antioxidant properties of different fruit parts of selected Artocarpus species from Sabah, Malaysia. Sains Malays. 44(3), 355363.
A. odoratissimus is also rich in secondary metabolites. Secondary metabolites are chemicals produced by the plants that have a role in ecological function, including defense mechanisms by serving as antibiotics and by producing pigments. Secondary metabolites can be classified based on the chemical structure, composition, and solubility into three main groups: terpenes, phenolics, and nitrogen-containing compounds. Meanwhile for the phytochemical contents, the peel contained higher phenolic, flavonoid, and carotenoid contents than the flesh and the seed as shown in Table 2, with 42.38 6 0.20 mg/g, 36.78 6 0.28 mg/g, and 0.86 6 0.04 mg/g respectively (Abu Bakar et al., 2015). The
Tarap—Artocarpus odoratissimus
417
anthocyanin content of the flesh (11.02 6 0.38 mg/g) was higher than the seed (3.8 6 0.34 mg/g) (Abu Bakar et al., 2009). In addition, based on a study done by Abu Bakar et al. (2010), this fruit contained p-coumaric, caffeic, chlorogenic in both flesh and seed while ferulic was only detected in the seed in terms of phenolic acids composition. Gallic and sinapic acids were not detected in the flesh and seed of A. odoratissimus. For the flavanones compositions, the seed contained naringin and hesperidin but the flesh only contained naringin. For the flavonols compositions, quercetin could be only found in A. odoratissimus flesh but kaempferol was obtained only in the seed. Meanwhile, rutin was not found in both flesh and seed of the fruit and for the flavones compositions, diosmin only could be obtained from the seed. Other studies done by Ee et al. (2010) revealed that this fruit contained a phytochemical compound derived from the flavonoid group, namely artosimmin, which expressed cytotoxic activity against the breast cancer cell (MCF-7) and human promyelocytic leukemia cells (HL-60). Additionally, Abu Bakar et al. (2015) reported that A. odoratissimus peel displayed the highest antioxidant activity for both ferric reduction (FRAP) and ABTS free radical scavenging assays followed by the seed and flesh (Table 3). For the free radical scavenging assay (using DPPH assay), the seed (13.69 6 0.59 mg) showed higher antioxidant activity than the flesh (2.44 6 0.15 mg) (Abu Bakar et al., 2009). It is believed that the phenolic and flavonoid constituents are the phytochemicals that contribute to the antioxidant activity in both the seed and flesh of this fruit while the carotenoid found in the fruit peel contributes to the antioxidant activity. For instance, the phenolic and flavonoid showed a positive correlation with the FRAP assay with r 5 0.983 and r 5 0.977 respectively (Abu Bakar et al., 2015).
SENSORY CHARACTERISTICS Sensory attributes such as sweetness and characteristic aroma may be the most important indicators of the acceptance of the people towards certain fruits. The flesh of Artocarpus odoratissimus is eaten fresh (Abu Bakar et al., 2009) and considered to have delightful fragrant aroma and is more delicious than Artocarpus heterophyllus (jackfruit) and Artocarpus altilis (breadfruit). When it is fully ripened, the smell will be a sharp pungent aroma even when the fruit is unopened. However, when it is not fully ripened, it will have a starchy bitter taste. In terms of the texture, the flesh of this fruit is soft and easy to chew as well as it has a thick peel with soft spines like-texture.
HARVEST AND POSTHARVEST CONSERVATION The decline in forest areas such as in Indonesia can result in the extinction of various plant species, and hence the government together with the public need to immediately take action to conserve the forests. For instance, many conservation efforts have been done by biological resources in Indonesia such as the emergence of government policies regarding flora and fauna identity. Other efforts have been done by the local communities in Kalimantan whereby they plant a variety of forest plant species that are useful in their orchards. Not only that, other activities that can support the conservation efforts include the establishment of botanical gardens (Uji, 2007). Last but not least, this fruit is considered as an underutilized fruit, wasted due to ignorance, lack of postharvest technology and gaps in supply chain systems.
TABLE 3 The Antioxidant Activity of Artocarpus odoratissimus Antioxidant activity
Flesh
Seed
Peel
DPPH Free radical scavenging assay
2.44 6 0.15 mg
13.69 6 0.59 mg
NIL
FRAP assay
17.92 6 0.74 μM
68.06 6 2.93 μM
378.93 6 20.25 μM
ABTS assay
5.34 6 0.22 mg
7.61 6 0.24 mg
226.11 6 0.44 mg
Note: FRAP is expressed as μM ferric reduction to ferrous in 1 g of dry sample. ABTS and DPPH free radical scavenging activities are expressed as mg ascorbic acid equivalent antioxidant capacity (AEAC) in 1 g of dry sample. NIL, not in list Source: Adapted from Abu Bakar, M.F., Mohamed, M., Rahmat, A., Fry, J., 2009. Phytochemicals and antioxidant activity of different parts of bambangan (Mangifera pajang) and tarap (Artocarpus odoratissimus). Food Chem. 113(2), 479483 and Abu Bakar, M.F., Abdul Karim, F., Perisamy, E., 2015. Comparison of phytochemicals and antioxidant properties of different fruit parts of selected Artocarpus species from Sabah, Malaysia. Sains Malays., 44(3), 355363.
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INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION This fruit is believed to have a great demand especially in the food industry with the application of modern processing and preservation techniques due to its short shelf life and being seasonal. Normally this fruit will be consumed fresh but it can be processed to make jam and syrup bases as well as being packaged into cans, thus creating markets for processed fruit during the off-seasons. In addition, the flesh also has been consumed as tarap fritters (mixing of flour and egg batter and frying it) and flavoring in ice cream (Tang et al., 2013). Hence, the manufacturers of icecream can take this opportunity to develop the popsicles with tarap flavor. The seed of the fruit has been commonly consumed by the local people either boiled or roasted as it has a firm texture with a reminiscent taste of chestnut and the young unripe fruits are sometimes eaten as vegetables. These features hold tremendous potential for A. odoratissimus fruit and seeds to be developed into food products. According to Lim et al. (2015), the skin of this fruit showed a great potential as a low-cost biosorbent for the removal of toxic dyes (methylene blue and methyl violet 2B) which could benefit the industries for the wastewater treatment for instance. In terms of the packaging, the active packaging and the combination of atmospheric packaging with natural botanicals can be developed for this particular fruit in order to improve the shelf life especially during the off season. Thus, people can still consume the fruit even though it is not available in the fruiting season.
ACKNOWLEDGMENT We would like to express our gratitude to the editor-in-chief for giving us an opportunity to write a chapter in this book as well as the other editors for the expertise and time in polishing our manuscript. We also want to thank those who undertook the research and provided us the data from previous years.
REFERENCES Abu Bakar, M.F., Mohamed, M., Rahmat, A., Fry, J., 2009. Phytochemicals and antioxidant activity of different parts of bambangan (Mangifera pajang) and tarap (Artocarpus odoratissimus). Food. Chem. 113 (2), 479483. Abu Bakar, M.F., Mohamed, M., Rahmat, A., Burr, S.A., Fry, J.R., 2010. Cytotoxicity and polyphenol diversity in selected parts of Mangifera pajang and Artocarpus odoratissimus fruits. Nutr. Food Sci. 40 (1), 2938. Abu Bakar, M.F., Abdul Karim, F., Perisamy, E., 2015. Comparison of phytochemicals and antioxidant properties of different fruit parts of selected Artocarpus species from Sabah, Malaysia. Sains Malays. 44 (3), 355363. Coronel, R., 1983. Promising Fruits of the Philippines. College of Agriculture, University of the Philippines at Los Banos, Los Banos. Ee, G.C.L., Teo, S.H., Rahmani, M., Lim, Y.M., Boong, C.F.J., 2010. Artosimmin-a potential anti-cancer lead compound from Artocarpus odoratissimus. Lett. Org. Chem. 7 (3), 240244. Galang, F.G., 1955. Fruit and Nut Growing in the Philippines. Araneta Institute of Agriculture, Malabon. Lim, L.B.L., Priyantha, N., Ing, C.H., Dahri, M.K., Tennakoon, D.T.B., Zehra, T., et al., 2015. Artocarpus odoratissimus skin as a potential low-cost biosorbent for the removal of methylene blue and methyl violet 2B. Desalin. Water Treat. 53 (4), 964975. Subhadrabandhu, S., 2001. Under-Utilized Tropical Fruits of Thailand. FAO Fiat Panis, Bangkok. Tang, Y.P., Linda, B.L.L., Franz, L.W., 2013. Proximate analysis of Artocarpus odoratissimus (Tarap) in Brunei Darussalam. Int. Food Res. J. 20 (1), 409415. Uji, T., 2007. Review: Keanekaragaman Jenis Buah-Buahan Asli Indonesia dan Potensinya. Biodiversitas. 8 (2), 157167.
The Tucuma˜ of Amazonas—Astrocaryum aculeatum Roberto C.V. Santos1, Michele R. Sagrillo2, Euler E. Ribeiro3 and Ivana B.M. Cruz1 1
Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil, 2Franciscan University Center, Santa Maria,
Rio Grande do Sul, Brazil, 3University for the Third Age, University of Amazonas State, Manaus, Amazonas, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry
419 419 419 420
Uses and Applications Recent In Vitro Studies References
422 422 424
CULTIVAR ORIGIN AND BOTANICAL ASPECTS There are several Amazon fruits consumed regionally having important effects on human health. This is the case of Astrocaryum aculeatum, popularly known as tucuma, which belongs to Arecaceae family and is also called tucuma-doamazonas, tucumanzeiro, tucuma-grande, or tucuma-açu. This palm tree is native to the Amazon, occurring in northern Bolivia, Colombia, Venezuela, Guyana, Suriname, and Brazil, being found mainly in the state of Amazonas. However, other states such as Para, Roraima, Rondonia, Acre, and Mato Grosso also have the plant (Cavalcante, 1991). The Tucuma is present in upland forest, secondary vegetation (roosts), savannahs, pastures, and clearings, being exceptionally tolerant to poor and degraded soils, and is considered as a pioneer plant of aggressive growth, fireresistant, and able to sprout after extensive fires (FAO, 1987). It invades deforested areas, where there is spontaneous occurrence, forming large and dense areas with various tucuma˜ trees. The spread of tucuma˜ is mainly made by animals (agoutis) that feed from the pulp and bury the seeds in the soil (Kahn and Milla´n, 1992). It is a large palm tree, with an upright stipe of 1030 m, being covered in its upper half by black or brown thorns arranged in rings. The leaves have a feather shape and have thorns on its entire length, measuring 45 m long (Cavalcante, 1991; Souza et al., 1996). It has straight inflorescence and edible fruit. They have a thin and smooth bark, a firm, fibrous, oleaginous, and yellow or orange thick pulp. The seeds are coated by the inside of the fruit, forming an extremely hard core with spherical or oval shape from brown to black.
HARVEST SEASON The harvest should be conducted at the beginning of maturation, from August to December, when the fruits are yellow, straight from the tree or even straight from the ground, after spontaneous fall. The harvest is usually made by women and children if the palms are near the houses, and if the plant is in a distant location, the harvest is performed by men and the transportation is made by animals or bicycles.
ESTIMATED ANNUAL PRODUCTION Most of the harvested fruit comes from wild palms. The tucuma˜-do-Amazonas produces, on average, two to four bunches per year, with an amount of about 200400 fruits per bunch. The fruit is constituted by subglobulus drupes to Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00056-3 © 2018 Elsevier Inc. All rights reserved.
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green coloring ellipsoids that when mature become orange, measuring 4.56 cm long and 3.54.5 cm in diameter, weighing about 6080 g. Its smooth and hard epicarp measures 11.5 mm in thickness; and the pith is slightly fibrous, oleaginous, and yellowish, measuring about 78 mm in thickness and the core is black, consistent, and woody, measuring 25 mm (FAO, 1987; Cavalcante, 1991; Kahn and Milla´n, 1992). The productivity of the palm tree is around 1250 kg/year, which starts slowly and late, when the tree reaches 7 years at least with height between 6 and 9 m (Shanley and Medina, 2005). The tucuma seeds germinate very slowly, from 8 months to 3 years old (Sa´, 1984). However, with heat treatment of 40 C for 60 days, one can reduce this time to 6 months. There are only a few reports of data on annual production. Didonet et al. report that in the year 2012, 367.8 t of tucuma were sold in fairs and markets in the city of Manaus, in the state of Amazonas, Brazil.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The fruit weighs 20100 g and is yellowish-green, with a length of 4.56.0 and 3.54.5 cm in diameter. The pulp has a coloration ranging from yellow to orange and has 9% protein, 55% oil, and represents 22% of the fruit weight (Shanley and Medina, 2005). A number of substances has been identified: carotenoids (62.6 mg/g of fresh pulp), being 21 isoforms, with a predominance of 75% of all-trans β-carotene (ATRA); flavonoids like catechin, quercetin and ascorbic acid (58 mg/100 g) (De Rosso and Mercadante, 2007; Gonc¸alves, 2008). The fruits are used for human and domestic animals’ consumption, of which the mesocarp (pulp) is considered a high-calorie food source due to the high lipid content, a significant amount of vitamin A precursor and a satisfactory content of fiber and other vitamins like vitamin E and C (Gonc¸alves, 2008). In this case, tucuma still presents high potential of provitamin A (carotene). The study conducted by De Rosso and Mercadante (2007) identified and quantified 60 different types of carotenoids in Amazon fruits and described the presence of 21 different types of carotenoids in tucuma, being the most concentrated the ATRA. The yellow oil is considered edible and is extracted from the mesocarp with organoleptic and nutritional characteristics of high value for the food and cosmetic industries. Previous work has already demonstrated that the chemical composition of the fruit tucuma has, on average, 46% humidity, 5% protein, 30% fat, 9% fibers, and 3% minerals. The estimated nutritional value is 247 kcal/100 g tucuma. It presents, on average, 58 6 4 mg/100 g of ascorbic acid and great antioxidant capacity. As the concentration of polyphenols is contradictory and therefore may be dependent on the ontogenetic time of the fruit or the environmental conditions of its cultivation. There is also the presence of catechin (79 6 5 mg/100 g) and quercetin (2.96 6 0.05 mg/ 100 g). However, the author did not observe the presence of other polyphenols such as epicatechin, kaempferol, and cyanidin (Gonc¸alves, 2008). A more recent study conducted by Sagrillo et al. (2015) identified other important bioactive compounds in the pulp and peel of tucuma such as rutin, caffeic acid, and chlorogenic acid in addition to confirming significant concentrations of β-carotene and quercetin. The high potential of provitamin A (carotene) was detected by many authors (De Rosso and Mercadante, 2007). The study conducted by De Rosso and Mercadante (2007) identified and quantified 60 different types of carotenoids in Amazonian fruits; 21 of such compounds in tucuma are shown in Table 1. It is important to highlight the fact that the unit of activity of vitamin A universally accepted is retinol equivalents, based on the activity of 1 μg of all-trans retinol. The international unit, still used in some contexts, is equal to 0.300 μg of all-trans retinol. In this case, the different types of carotenoids have different levels of vitamin activity depending upon the efficiency of absorption and the rate of its conversion to vitamin A. In tucuma, trans-β-carotene was the carotenoid found in highest concentration representing 75% of all identified and quantified carotenoids. From the concentration of carotenoids evaluated, the estimate amount of provitamin A in tucuma was 850 RE/100 g. Compared to the provitamin A found in other fruits such as mango (104127 RE/100 g), papaya (1974 RE/100 g), acerola (148283 RE/100 g), broccoli (131194 RE/100 g), leafy vegetables (429640 RE/100 g), and raw carrots (308625 RE/100 g) tucuma has the highest levels (De Rosso and Mercadante, 2007). A recent study by Sagrillo et al. (2015) identified, besides carotenoids, some other important bioactive compounds both in the flesh and in the skin of tucuma that have antioxidant and anticarcinogenic aspects (Table 2). Considering the carotenes present in tucuma, Chaves and Pechnik (1947) reported that the consumption of 30 g of tucuma pulp would supply three times the daily requirement of vitamin A for a child. Thus, 100 g of pulp are equivalent to 52.000 units of vitamin A.
The Tucuma˜ of Amazonas—Astrocaryum aculeatum
TABLE 1 Composition of the Main Carotenoid Found in the Pulp of Tucuma (Astrocaryum aculeatum) described by De Rosso and Mercadante (2007) Composition
Concentration (μg/g)
Total carotenoid
62.65
All-trans β-carotene
47.36
All-trans-carotene R
1.68
All-trans β-criptoxanthines
1.64
13-cis-β-carotene
1.60
All-trans-R criptoxanthines
1.30
Zeinoxanthine
1.02
All-trans-lutein
0.79
Cis-3 c-Carotene
0.89
15-cis-β-Carotene
0.80
5,8-Epoxy-β-carotene
0.76
Cis-β-Zeacarotene 2
0.65
Cis-β-Zeacarotene 1
0.60
All-trans β-Carotene
0.52
All-trans α-zeacarotene
0.44
All-trans-C-carotene
0.35
All-trans-neoxantina
0.26
Cis-violaxanthin
0.24
Tall-trans-zeaxanthin
0.16
All-trans-u-carotene
0.14
Cis-Lutein
0.04
TABLE 2 Phenolic Composition and Flavonoid of Astrocaryum aculeatum Compounds
Bark Extract
Extract of the Pulp
(mg/g)
(%)
(mg/g)
(%)
Gallic acid
3.79 6 0.01 a
0.38
14.25 6 0.03 a
1.42
Chlorogenic acid
3.04 6 0.03 a
0.30
1.19 6 0.02 b
0.11
Caffeic acid
8.33 6 0.11 b
0.83
0.87 6 0.01 b
0.09
Rutin
30.54 6 0.04 c
3.05
6.19 6 0.04 a
1.91
Quercetin
12.72 6 0.01 d
1.27
6.53 6 0.07 c
0.65
β-Carotene
62.91 6 0.05 e
6.29
27.55 6 0.10 d
2.75
The results are expressed as mean 6 standard deviation (SD) of three determinations. Means followed different letters differ by Tukey’s test at P , .005.
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USES AND APPLICATIONS Tucuma has been used since the times of the Amerindians. It is currently consumed by the Amazon population, with the use of nearly all the plants. The stipe is applied to the construction of houses and furniture. The meristem is used in food. The flesh of the fruit, which is the edible part, is widely used for the production of tucuma wine, icecream, popsicles, soap, as well as animal feed. The core is used for the production of handicrafts, such as rings, bracelets, and necklaces. Furthermore, the core has been widely used to extract an oil to be used in the cosmetic and food industry, and in the production of biodiesel (Costa et al., 2005). The leaves have been used in the production of baskets, hats and tucum (a high-quality fiber for the production of hammocks and bags) is extracted from them. In Manaus, the production of tucuma pulp and its derivatives is a significant and growing economic activity at a regional level. The pulp is appreciated and consumed by the population in natura or as a filling for sandwiches, tapioquinha, creams, and icecreams (FAO, 1987). Both from the pulp and the seed, it is possible to extract various types of edible oils, cosmetics and other products suitable for the manufacturing of biodiesel, the grain also serves as a food supplement for pets. Currently, “X-caboquinho,” a typical sandwich, is popular in the local cuisine, being an important product of regional cafes, street markets, bus terminals and other points of Manaus. In this way, the tucuma pulp is an ingredient of local “fast food” (Costa et al., 2005), the fruit has a growing importance in the state of Amazonas, as well as potential for new markets outside the region (Lopes et al., 2009). This fact led to the increase in demand of this fruit by small farmers of the region to draw from this small trade their livelihoods, as well as the interest of producers for the plant crop to be commercialized (Ramos et al., 2011). However, this increasing demand is coming up on the fact that although the tucuma is undemanding as to soil fertility and does not present phytosanitary problems, it has the same deadpan cultivation in the Amazon region itself. This can be explained by difficulties, among other factors, on seed germination, as tucuma has a germination period that can vary from 2 to 3 years (Sa´, 1984). The “rain” of these seeds is responsible for the primary species dispersion, which usually occurs in a projection distance of 3.5 m from the cup. While, the secondary dispersion is made from other animals by agoutis (Dasyprocta sp.), that spread the seeds around the palm trees, at distances less than 15 m, being this rodent primarily responsible for the spread of the palm tree, since it buries seeds a few centimeters deep to search for them later (Shanley and Medina, 2005). Commercial plantations are still rare and are usually found on farms, ranches, and gardens, by natural dispersion, involuntary anthropic dispersion, and the maintenance of young and adult plants in pastures (Bacelar et al., 2006).
RECENT IN VITRO STUDIES Recent studies conducted by Laborato´rio de Biogenoˆmica da Universidade Federal de Santa Maria suggest that the hydroalcoholic extract of tucuma has an antioxidant capacity that is quite high and also has some action in modulating the production of free radicals in healthy blood exposed to hydrogen peroxide. These results indicate that tucuma may have chemotherapeutic potential. Souza Filho et al. (2013) first described the cytogenotoxic effect of tucuma extracts obtained from the pulp and peel. The fragmentation of DNA by the comet assay and chromosomal instabilities were observed from the display of mononucleated cells of peripheral blood extracts of tucuma particularly at concentrations .500 μg/mL for 24 and 72 h of cell culture. Cell viability also decreased when these cells were treated with the extracts of peel and pulp of tucuma at 1000 μg/mL. Other important findings are related to differences in the genotoxic response depending on tucuma concentrations. From the results, it was observed that tucuma at concentrations between 5 and 100 μg/mL showed a positive effect on cells when compared with higher concentrations, they obtained findings of elevated caspase-1. Activation of caspase-1 results in apoptosis via caspase-7, it is a key molecule in pyroptosis process. Therefore, caspase-1 can work aiming to eliminate malignant precursors through programmed cell death. Moreover, high concentrations of the tucuma extract might not have beneficial effects on healthy cells including change in pathways related to inflammation and planned cellular pathways. On the contrary, lower concentrations of the peel and pulp extracts have proven safe and potentially beneficial on the physiology of cells that could contribute to the prevention of disease. However, these results showed that the beneficial effects of tucuma depend on the concentration and exposure time as these variables are related to increased genotoxic effects observed in mononuclear cells from peripheral blood. A further investigation conducted by Sagrillo et al. (2015) showed that the pulp and extract of tucuma were able to reverse the cytogenoxicity caused in mononuclear cells of peripheral blood exposed to hydrogen peroxide. The results of this research are probably related to antioxidant molecules found in the skin and pulp extracts. The amount of tannins
The Tucuma˜ of Amazonas—Astrocaryum aculeatum
423
and alkaloids found in the extracts derived from tucuma pulp are lower when compared to extracts of other fruits such as red grapes and pomegranate. The lower tannin levels found in the analyzed extracts confer safe consumption of tucuma, as excessive tannins can reduce gastric digestibility and cause enzyme inhibition. Other antioxidant compounds such as quercetin and rutin were identified in the extracts of tucuma and have been associated with numerous biochemical and pharmacological activities including free radical scavenging capacity and protection against ultraviolet light. These molecules also have effects on immune and inflammatory cells. The tucuma pulp extract contains gallic acid concentration greater than the bark extract. Sagrillo et al. (2015) estimated that a daily intake of 100 g of fresh tucuma contains an amount of gallic acid equivalent to the intake of about 130 mL of red grape juice. This juice is considered a major source of gallic acid in the human diet. Although caffeic acid and chlorogenic were found in low concentrations in tucuma, the levels of these compounds were higher in bark extract than the pulp. The bioactive molecules present in tucuma extracts probably contribute to its antioxidant capacity, this fact was confirmed by DDPH tests, which check the scavenger capacity of DPPH radical, and TRAP. The concentration of important antioxidant molecules found in the extracts of tucuma is no guarantee that these extracts are able to reverse the oxidative stress in biological systems exposed to prooxidant molecules, such as the H2O2 molecule. This is a prooxidant molecule, because, together with the superoxide radical and hydroxyl radical, H2O2 is one of three main reactive oxygen species (ROS): metabolic byproducts continuously generated by mitochondria in growing cells, as a result of aerobic metabolism (Halliwell, 1992). However, at low levels, H2O2 must be considered as a signaling molecule in various cellular processes, and at high levels H2O2 causes damage to organelles, particularly the mitochondria. Potentially, oxidative stress can be harmful, generated by excessive ROS and dysfunction can result in depletion of the energy accumulation of cytotoxic mediators and cell death (Lima et al., 2008). This process of cell damage occurs because, at high concentration of ROS, such as H2O2, damage to cellular proteins and lipids or DNA adducts are formed and they can promote the carcinogenic activity (Choquenet et al., 2008). Accordingly, the result of reverse in cellular oxidative stress indicates the potential preventive role of tucuma extracts. It is important to highlight that it has not been found a linear response related to different concentrations of the tucuma extracts in lymphocytes compared to cyto and genotoxic activity caused by H2O2. Two potential explanations were considered for the interpretation of such results. Firstly, with regard to the occurrence of chemical compounds in tucuma, higher concentrations may reduce positive effects of other compounds such as antioxidants molecules present in the extracts. This is the case of the alkaloid compounds. Some alkaloid compounds are toxic to many organisms and others are used as drugs (Castro and Freeman, 2001). In the tested extracts, it was found a concentration of total alkaloids greater in the bark when compared to tucuma pulp extract. Another possible explanation is related to increased concentrations of the antioxidants present in extracts that have been tested. This is the case of the carotenoids are present in high concentrations in fruit tucuma˜ as described in our results and previous studies (Sreevidja and Mehrotra, 2003; Laghari et al., 2012). De Rosso and Mercadante (2007) described 24 carotenoids, of which 21 have been chemically identified in tucuma fruit. All-trans O-β-carotene was found as the major carotenoid, accounting for 75% of the total content of carotenoids in tucuma, followed by 13-cisβ-carotene, all-trans α-carotene acid, and all-trans β-cryptoxanthin, each representing between 2.0% and 2.8% of the total carotenoid content. The other 19 carotenoid represent 15% of the total content. The analysis showed that tucuma provides a higher concentration of provitamin A (β-carotene), with 52 mg/100 g pulp. This concentration is about eight times higher than the one found in carrots (6.6 mg/100 g pulp). The average consumption of 30 g of tucuma pulp can provide three times more vitamin than the daily requirement for an adult. Carotenoids are organic pigments that naturally occur and are precursors of vitamin A, which is indispensable for cellular differentiation, embryonic development, for sight as well as many other functions, including potential therapeutic benefit in the treatment of various morbidities due to their antioxidant properties (Lee et al., 2012). There is little or no question that the carotenoids and their oxidation products have significant biological activity in cell lines and its mechanism of action in cell cultures may well help in the design of clinical trials. However, prospective randomized trials have failed to demonstrate a consistent benefit for the carotenoid β-carotene in patients with cardiovascular disease risk. The basis for this apparent paradox is not well understood, but may be assigned to different antioxidant properties of various carotenoids dependent interactions resulting from its physicalchemical structure with biological membranes (Bo¨hm et al., 2012). Therefore, one cannot rule out the idea that high concentrations of tucuma extract with higher levels of carotenoids could stop the cytoprotective effects observed at lower concentrations. Similar results were observed when the potential protective effect of tucuma bark extract on DNA damage in lymphocytes exposed to H2O2 was analyzed. Treatments with 300 and 600 μg/mL showed a protective action better than treatments with tucuma bark extracts in both lower and higher concentrations. However, all treatments of the pulp
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extract at concentrations .100 mg/mL reversed DNA damage caused by H2O2 at a level similar to that observed in control untreated cells. These results are in agreement with previous studies, which found that some carotenoids such as β-carotene, increased resistance to oxidative DNA damage in relatively low concentrations. However, this protection was lost rapidly with increasing concentration of carotenoids (Lowe et al., 1999). Moreover, compared with the peel, pulp concentration extract is about 50% lower than β-carotene. Perhaps the differences in the concentrations of these and other compounds such as alkaloids, may explain the different results with respect to DNA damage in lymphocytes exposed to H2O2 at the concentration of tucuma .100 μg/mL presenting a genoprotective effect. Regardless of the causes that lead to any differences between extracts of tucuma peel and pulp, the results suggest that the pulp is the part of the fruit that has higher genoprotective properties. H2O2 has the ability to destroy cells, such as neurons, by inducing apoptosis (Chandra et al., 2000). The apoptotic signaling converges mainly in activation of intracellular caspases, also known as proteases or cysteine-dependent aspartate, which is a family of intracellular proteins involved in the initiation and execution of apoptosis. Therefore, the activation of the caspase cascade is a central effector mechanism that promotes apoptosis in response to death inducing signals from cell surface receptors or mitochondria (Toshiyuki et al., 2000). The initiator caspases, such as caspase-8, is able to activate effector caspases such as caspase-1 and -3 (Budihardjo et al., 1999). Studies conducted by Jiang et al. (2000) showed that H2O2 induces apoptosis, triggering via of caspases. The authors demonstrated that the treatment with H2O2 caused a time-dependent increase of the proteolytic activity of caspases 1 and 3. Based on prior evidence, a test was conducted to determine whether tucuma extracts may act on the track of caspases promoting apoptosis by exposure of lymphocytes to H2O2. The results confirm the activation of the caspase in the presence of H2O2 described earlier, and tucuma extracts were capable of reversing the activation totally or partially.
REFERENCES Bacelar, C.G., De Mendonc¸a, M.S., Barbosa, T.C.T.S., December 2006. Floral morphology of one population of Astrocaryum aculeatum Meyer (Arecaceae) in the Central Amazon-Brazil. Acta Amazonica. 36 (4). Bo¨hm, F., Edge, R., Truscott, G., 2012. Interactions of dietary carotenoids with activated (singlet) oxygen and free radicals: potential effects for human health. Mol. Nutr. Food Res. 56, 205216. Budihardjo, I., Oliver, H., Lutter, M., Luo, X., Wang, X., 1999. Biochemical pathways of caspase activation during apoptosis. Rev. Cell Dev. Biol. 15, 269290. Castro, L., Freeman, B.A., 2001. Reactive oxygen species in human health and disease. Nutrition. 17, 163165. Cavalcante, P.B., 1991. Frutas comestı´veis da Amazoˆnia. fifth ed. Edic¸o˜es CEJUP/Museu Paraense Emı´lio Goeldi, Bele´m. Chandra, J., Samali, A., Orrenius, S., 2000. Triggering and modulation of apoptosis by oxidative stress. Free Radic. Biol. Med. 29, 323333. Chaves, J.M., Pechnik, E., 1947. Tucuma˜ (Astrocaryum vulgare Mart.). Rev. Quı´m. Ind. 16 (5), 184191. Choquenet, B., Couteau, C., Paparis, E., Coiffard, L.J., 2008. Development of an in vitro test to determine the water-resistance of sunscreens. Pharmazie 63, 525527. Costa, J.R., Van Leeuwen, J., Costa, J.A., 2005. Tucuma˜-do-amazonas, Astrocaryum tucuma Martius. In: Shanley, P., Medina, G. (Eds.), Frutı´feras e plantas u´teis na vida amazoˆnica. CIFOR, Imazon, Bele´m, pp. 215222. De Rosso, V., Mercadante, A., 2007. Identification and quantification of carotenoids, by HPLC-PDA-MS/MS, from Amazonian Fruits. J. Agric. Food Chem. 55, 50625072. FAO, 1987. Especies forestales productoras de frutas y otros alimentos. 3. Ejemplos de America Latina 44-3. FAO, Rome, 241 pp. Gonc¸alves, A.E.S.S., 2008. Avaliac¸a˜o da capacidade antioxidante de frutas e polpas de frutas nativas e determinac¸a˜o dos teores de flavonoides e vitamina C. Sa˜o Paulo: USP, 2008. Dissertac¸a˜o (Programa de Po´s-graduac¸a˜o em Cieˆncias dos Alimentos), Universidade de Sa˜o Paulo. Halliwell, B., 1992. Reactive oxygen species and the central nervous system. J. Neurochem. 59, 16091623. Jiang, Q., Zhenglin, G., Zhang, G., Guozhang, J., 2000. Diphosphorylation and involvement of extracellular signal-regulated kinases (ERK1/2) in glutamate-induced apoptotic-like death in cultured rat cortical neurons. Brain Res. 887, 285292. Kahn, F., Milla´n, B., 1992. Astrocaryum (Palmae) in Amazonia: a preliminary treatment. Bull. Inst. Franc¸ais d’E´tude Andines. 21 (2), 459531. Laghari, A.H., Ali Memon, A., Memon, S., Nelofar, A., Khan, K.M., et al., 2012. Determination of free phenolic acids and antioxidant capacity of methanolic extracts obtained from leaves and flowers of camel thorn (Alhagi maurorum). Nat. Prod. Res. 26, 173176. Lee, J., Giordano, S., Zhang, J., 2012. Autophagy, mitochondria and oxidative stress: cross-talk and redox signaling. Biochem. J. 441, 523540. Lima, E.C., Paiva, R., Nogueira, R.C., Soares, F.P., Emrich, E.B., Silva, A.A.N., 2008. Callus induction in leaf segments of Croton urucurana Baill. Cieˆnc. Agrotecnol. 32, 1722. Lopes, M.T.G., Maceˆdo, J.L.V., Lopes, R., Van Leeuwen, J., Ramos, S.L.F., Bernardes, L.G., 2009. Domesticac¸a˜o e melhoramento do Tucuma˜-doAmazonas. In: Bore´m, A., Lopes, M.T.G., Clement, C.R. (Eds.), Domesticac¸a˜o e melhoramento.. Universidade Federal de Vic¸osa, Vic¸osa, pp. 424441. Lowe, G.M., Booth, L.A., Young, A.J., Bilton, R.F., 1999. Lycopene and b-carotene protect against oxidative damage in HT29 cells at low concentrations but rapidly lose this capacity at higher doses. Free Rad. Res. 30, 141151.
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Ramos, et al., 2011. Pre-germination treatments and origin of tucuma˜-do-amazonas seeds in the production of seedlings. Rev. Bras. Frutic. 33 (3). Sa´, S.T.V., 1984. Superac¸a˜o da dormeˆncia de sementes de tucuma˜ (Astrocaryum tucuma Mart.). Manaus. 53f. Monografia (Graduac¸a˜o Engenheiro Agroˆnomo), Departamento de Cieˆncias Agra´rias, Universidade do Amazonas. Sagrillo, M.R., et al., 2015. Tucuma˜ fruit extracts (Astrocaryum aculeatum Meyer) decrease cytotoxic effects of hydrogen peroxide on human lymphocytes. Food Chem. 173, 741748. Shanley, P., Medina, G., 2005. Frutı´feras e plantas u´teis na vida amazoˆnica. CIFOR, Bele´m. Souza, A.G.C., Sousa, N.R., Silva, S.E.L., Nunes, C.D.M., Couto, A.C., Cruz, L.A.A., 1996. Fruteiras da Amazoˆnia. Embrapa, Brası´lia. Souza Filho, O.C., Sagrillo, M.R., Garcia, L.F., Machado, A.K., Cadona´, F., Ribeiro, E.E., et al., 2013. The in vitro genotoxic effect of Tucuma (Astrocaryum aculeatum), an Amazonian fruit rich in carotenoids. J. Med. Food. 16 (11), 10131021. Sreevidja, N., Mehrotra, S., 2003. Spectrophotometric method for estimation of alkaloids precipitable with Dragendorff’s reagent in plant materials. J. Assoc. Off. Agric. Chem. 86, 11241127. Toshiyuki, N., Hong, Z., Nobuhiro, M., En, L., Xu, J., Yankner, B.A., et al., 2000. Caspase-12 mediates endoplasmic reticulum specific apoptosis and cytotoxicity by amyloid-b. Nature. 403, 98103.
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Umbu—Spondias tuberosa Maria Auxiliadora C. de Lima1, Silvanda de M. Silva2 and Viseldo R. de Oliveira1 1
Embrapa Semia´rido, Petrolina, Pernambuco, Brazil, 2Federal University of Paraiba State, Areia, Paraiba, Brazil
Chapter Outline Introduction Origin and Botanical Aspects Genetic Variability Harvest Season Estimated Annual Production Fruit Physiology and Biochemistry
427 427 428 429 429 429
Chemical Composition and Nutritional Value Sensory Characteristics Harvest and Postharvest Conservation Industrial Application or Potential Industrial Application Final Remarks References
429 431 431 431 432 432
INTRODUCTION The umbu tree is one of the most representative species of the Caatinga biome, which occupies 11% of the Brazilian territory and 70% of the northeast region of this country. Similar to the other species in the biome, the umbu tree has adaptated to the scarcity and irregularity of rains that happen over the years. These are characteristics of the semiarid region, where there is the occurrence of this species. Compared to other species native to this region of Brazil, the fruits of umbu tree are the most consumed by a local population. Besides the fresh fruit consumption, several products from the umbu fruit are sold, reaching other Brazilian regions and niche markets in Europe. However, the season is restricted to a few months, as the extractive harvest, the genetic variability of the species, the perishability of the fruit, the lack of knowledge and techniques that favor the production, and a more rational postharvest conservation hinder progress which facilitates a greater insertion in the market. Some results were derived from studies that assessed the attributes of the umbu fruit, to support propositions of strategies for better packaging and marketing of the fruit as well as to strengthen the production chain.
ORIGIN AND BOTANICAL ASPECTS The Anacardiaceae family consists of 6074 genera and 400600 species of trees and shrubs, rarely subshrubs and lianas, with occurrence in tropical, subtropical, and limited in temperate regions (Purseglove, 1984). One of the representatives of this family is the umbu tree (Spondias tuberosa Arruda), a native and endemic fruit tree species of the Brazilian semiarid region, which has tuberous roots, xerophilia and characteristic leaf shedding. The tree can reach 57 m high. It has a short and twisted trunk, with a diameter at ranging from 1.3 to 2.0 m, when measured at 20 cm from the soil, and an umbellate canopy of 9.012.5 m in diameter (Santos, 1997). The flowers are small, white, pentamerous, the terminal inflorescences are united in a panicle type, reaching 1015 cm of length by 78 cm in diameter, 40% of the flowers are hermaphroditic and 60% are male flowers in the same plant, what characterizes the species as andromonoecious (Nadia et al., 2007). The compound leaves are disposed in an alternate arrangement, they are imparipinate and petiole, they have 37 membranous leaflets, ovate oblong, obtuse based or cordate, acute or obtuse apex, they measure 24 cm in length, 23 cm wide and are serrate or entirely smooth (Pires, 1990), with hairiness in some accessions (Lima, 1994). The fruit is a drupe, with a diameter generally from 2 to 4 cm and a mass of 1020 g. The endocarp or stone is resistant and has a dense fibrous consistency that contains the seed (Silva and Silva, 1974). Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00057-5 © 2018 Elsevier Inc. All rights reserved.
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GENETIC VARIABILITY Considering the extractive production of the umbu tree and the fact of being an alogamous species that is widely distributed, there is genetic variation within and between natural populations for plant form, size, appearance, mass, and physicochemical properties of the fruits. One of the first studies to evaluate the phenotypic variation for qualitative and quantitative characters in umbu fruits was carried out by Silva et al. (1987). The authors observed a great variation in the total weight of the fruit, the seed mass, the rind, and the pulp mass, with mean values, respectively, of 15.89 6 3.82; 1.62 6 0.41; 3.56 6 0.82 and 10.84 6 2.90 g, which indicates a high level of phenotypic variation (over 20%). The authors also added that the umbu consists on average of 10% of stone, 22% of rind, and 68% of pulp. The study also ^ in the umbu fruit in function of the total mass contributed for the proposition of the estimate of the pulp amount Pp ^ of the fruit (TMF), this is based on the regression equation Pp 5 0.70915TMF 2 0.60587, which showed a correlation coefficient of 0.93 (Table 1). The authors highlighted the high variability between and within families and indicated the need for more detailed evaluation of phenotypic and genetic aspects as well as the use of broader sampling, aiming future breeding programs. In a more comprehensive study of the genetic variability of the umbu tree, Santos et al. (1999) evaluated the total mass, diameter, the mass of the rind, the seed mass, the mass of the pulp, and the soluble solids content of fruit pulp. Samples were collected in 17 ecogeographic regions of several states in the northeast region of Brazil, where 340 plants were sampled. Based on the characterization of fruits of mother plants, the identification of extreme phenotypes and other forms of variability, the cloning of 70 accessions was done for the set up of the Embrapa Semi-Arid Umbu Tree Germplasm Bank. Data in Table 2 emphasizes higher phenotypic variability compared to that reported by Silva et al.
TABLE 1 Relationship Between the Total Mass of the Fruit (TMF), Pulp (MP), the Stone (MS), and Rind (MR) Expressed by the Correlation Coefficient Characteristic
MP
MR
MS
TMF
0.93442
0.84241
0.81810
MP
-
0.72900
0.68520
Source: Adapted from Silva, C.M.M.de.S., Pires, I.E., Silva, H.D.da., 1987. Caracterizac¸a˜o de frutos do umbuzeiro. EMBRAPA-CPATSA, Petrolina, 17 pp. (EMBRAPA-CPATSA. Boletim de Pesquisa, 34).
TABLE 2 Origin and Mass Values, Diameter (DIAM), the Rind Mass (RM), Seed Mass (SM), Mass of Pulp (MP) and Soluble Solids From Pulp Content (SS) in Umbu Fruits Which Were Identified as Promising for the Set Up of the Embrapa Semi-Arid Umbu Tree Germplasm Bank Accession
Origin (Brazilian state)
Mass (g)
DIAM (mm)
RM (g)
SM (g)
MP (g)
SS ( Brix)
68
Bahia
96.70
56.7
24.30
13.30
59.10
10.00
48
Bahia
85.00
52.0
22.50
9.80
52.70
12.70
50
Bahia
75.30
53.0
17.70
10.00
47.60
12.80
67
Bahia
61.00
47.3
17.30
11.70
32.00
10.20
57
Minas Gerais
50.00
44.7
9.80
8.30
31.90
11.10
52
Pernambuco
41.80
41.0
4.80
9.70
27.30
11.50
13
Pernambuco
39.00
39.8
7.80
5.13
26.07
14.80
04
Bahia
22.82
33.0
3.18
1.98
17.66
11.60
01
Bahia
9.97
25.1
1.37
0.64
7.96
11.51
09
Pernambuco
4.88
21.9
0.98
0.30
3.60
11.00
Source: Adapted from Santos, C.A.F., Nascimento, C.E.de.S., Campos, O.C., 1999. Preservac¸a˜o da variabilidade gene´tica e melhoramento do umbuzeiro. Rev. Bras. Frutic. 21, 104109.
Umbu—Spondias tuberosa
429
(1987), due to a bigger sampling and number of evaluated trees, the fruit mass stood out, ranging from 4.88 to 96.70 g. However, there were genotypes with mass greater than 100 g. Another way to evaluate the genetic variability is based on the implementation of field trials in experimental design. Thus, Oliveira et al. (2004) installed 42 progenies and three origins of the umbu tree. At 9 years of age, the plants were characterized as: plant height (HEI), biggest canopy diameter (BCD), smallest canopy diameter (SCD), stem diameter (SD), and number of primary branches (NPB), with average values equivalent to 1.60 6 0.40 m; 3.86 6 1.09 m; 0.97 6 3.35 m; 6.95 6 1.48 cm, and 2.96 6 1.02, respectively. No genetic variability was found for HEI, SD, and NPB. For BCD and SCD characters, the variability among origins was practically nil, which indicates that the selection among origins for plants at that age is not possible. On the other hand, there is significant genetic variability within the population, which leads to estimates of the individual heritability in the narrow sense, ranging from 8% to 14%. The presence of genetic variability for BCD and SCD also disclosed the possibility for breeding the characters TMF and number of fruits per plant, as there are positive correlation involving the aforementioned characters (Santos and Nascimento, 1997). Thus, BCD and SCD can be used as an indirect way of selection for the production of fruits.
HARVEST SEASON The harvesting season of a species is an important step in defining marketing strategies regarding the consumption of the fruit or the products generated and marketed. In the case of the umbu tree, the participation of rural communities is very important in the harvesting, which leads to market supply and income generation for small farmers. The generation of income from these fruits is concentrated from January to March, which is the harvest period (Cavalcanti et al., 2006).
ESTIMATED ANNUAL PRODUCTION Official statistics of the Brazilian production recorded values of 7466 t in 2014 (IBGE, 2014). The picking of the umbu fruit is an additional income for rural families in the Brazilian semiarid area, during the period of harvest. However, it is estimated that only about 20% of the fruits are harvested and are reported in the statistics (Cavalcanti et al., 2001). Most of the production is lost due to natural fall of fruits that ripen on the plant, the difficulty to reach plants located far from communities, to the damage caused by the handling, and the rapid postharvest ripening.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY The fruit development cycle lasts about 120 days and is characterized by a simple sigmoidal growth pattern, defined in three phases. According to Campos (2007), the first phase is accelerated growth, which ends when the fruit is green but the degradation of pigments has started. The second phase corresponds to the slow growth lasting until the fruit reaches physiological maturity. The final stage is a mild decrease in weight. For the umbu fruit, the characterization of maturation still depends on the standardization criteria to identify and define the maturity stages. Some propositions for maturity stages were shown in the studies of Narain et al. (1992), Costa et al. (2004), and Campos (2007). Despite differences between criteria for the proposed scales, it is admitted that firmness of the fruit and rind color, which changes from partially dark-green at physiological maturity (Fig. 1A) to yellowish-green in ripe fruits (Fig. 1B), are important elements to characterize the maturity stages. The weight and the transverse diameter are also commercially important. As maturation evolves, tissues accumulate soluble solids, especially sugars, and degrade organic acids, starch, and pectic compounds. One of the major changes is expressed as firmness loss which is reduced to less than 5 N, when the umbu fruit is ready for consumption (Lopes, 2007; Almeida et al., 2008; Lima et al., 2010). The changes that take place during maturation are influenced by the respiratory behavior of the umbu fruit, which is typically climacteric. Some published reports indicate a respiratory peak of about 150 mg CO2/kg per h, at 24 6 2 C, which happens approximately 24 h after the harvesting in the maturity stage, where the rind color is light green (Lopes, 2007). Similarly, the increase in the ethylene production during the maturation determines the rates where the physical and chemical changes happen in the umbu fruit.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE The combination of sugars, acidity and phenolic compounds in the pulp produce an exotic flavor in the umbu fruit. The acid-sweet taste is the main appeal for the fruit intake. However compounds with nutritional importance, like vitamin C, carotenoids and some minerals, and even some phenolic nutrients, can boost its greater inclusion in the diet (Table 3).
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FIGURE 1 Visual aspect of umbu fruit at physiological maturity (A) and ripe (B). Photos courtesy: Maria Auxiliadora Coeˆlho de Lima (A) and Viseldo Ribeiro Oliveira (B).
TABLE 3 Composition of Ripe Umbu Fruit Component
Rangea
Reference
Dry matter
88 g/100 g
Rufino et al. (2010)
Moisture
8590 g/100 g
Narain et al. (1992), Rufino et al. (2010)
Total carotenoids
1.510.0 μg/g
Melo and Andrade (2010), Rufino et al. (2010), Gondim (2012)
β-Carotene
0.13.0 μg/g
Soluble solids
8.015.0 Brix
Narain et al. (1992), Costa et al. (2004), Lopes (2007), Dantas Ju´nior (2008), Lima et al. (2010), Gondim (2012)
Total soluble sugars
8.010.0 g/100 g
Almeida (1999), Dantas Junior (2008)
Reducing sugars
3.56.0 g/100 g
Narain et al. (1992), Almeida et al. (2008), Dantas Junior (2008)
Starch
0.52.5 g/100 g
Narain et al. (1992), Lopes (2007), Gondim (2012)
Titratable acidity
0.51.5 g citric acid/100 g
Narain et al. (1992), Costa et al. (2004), Lopes (2007), Dantas Junior (2008), Lima et al. (2010)
pH
2.03.0
Narain et al. (1992), Costa et al. (2004), Lopes (2007)
Ascorbic acid (vitamin C)
1040 mg/100 g
Narain et al. (1992), Campos (2007), Dantas Junior (2008), Silva et al. (2009), Melo and Andrade (2010)
Pectin compounds
0.51.0 g/100 g
Narain et al. (1992), Dantas Junior (2008)
Total phenols
1090 mg GAE/ 100 g
Dantas Junior et al. (2008), Melo and Andrade (2010), Rufino et al. (2010), Gondim (2012)
Tannins
120 mg/100 g
Narain et al. (1992)
Yellow flavonoids
740 mg/100 g
Dantas Junior (2008), Rufino et al. (2010)
Protein
0.4 g/100 g
Narain et al. (1992)
Fat
0.9 g/100 g
Crude fiber
1.0 g/100 g
Ash
0.3 g/100 g
Calcium
16 g/100 g
Iron
1.4 g/100 g
Phosphorus
30 g/100 g
GAE, gallic acid equivalent. a Values are expressed as fresh weight.
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431
The antioxidant activity of the umbu fruit, despite being considered low (Melo and Andrade, 2010; Rufino et al., 2010; Gondim, 2012), should be related to phenolic compounds (Dantas Junior et al., 2008; Melo and Andrade, 2010). However, Dantas Junior et al. (2008) noted that some genotypes may have antioxidant activity similar to the protection given by Trolox. This compound is an analog of vitamin E. Moreover, as part of the diet, the umbu fruit may contribute to protect the body from damage caused by free radicals (Melo and Andrade, 2010) through a synergistic effect of the compounds it contains. Another important quality component of the umbu fruit are the volatile compounds. The major volatiles compounds identified in ripe umbu fruits were 1-heptanol, 2-nonanol, 1-octanol, 2-octanol, methyl pyrazine, β-cis-ocimene, 2-butyl thiophene, methyl octanoate, 2-hexyl furan, and (E)-2-cyclohexen-1-one (Galva˜o et al., 2011).
SENSORY CHARACTERISTICS Currently the fruits of the umbu tree have gained space in domestic and international markets due to the pleasant taste and remarkable flavor. Additionally, this fruit has a bioactive compounds that contributes to the diet (Dantas Junior, 2008; Gondim, 2012). A sensory profile of fruits from 58 different genotypes of umbu tree was drawn by quantitative descriptive analysis, in which 32 trained judges evaluated the intensity of characteristics relating to appearance (uniformity of size, hairiness, brightness), flavor (sweetness, acidity, distinctive flavor, stranger flavor, astringency), and texture (tactile sensation, juiciness, fibrousness). The sensory quality differed widely among genotypes (Dantas Junior, 2008; Costa et al., 2015). However, the characteristic bittersweet taste, sweetness, brightness, and yellowing of the rind characterized the most outstanding attributes in the selection of genotypes as most promising in relation to the perception of quality (Schunemann, 2013).
HARVEST AND POSTHARVEST CONSERVATION Umbu must be harvested when well formed in the plant and has reached the mature green stage of maturity or near it (physiological maturity), i.e., as the skin color starts to change from dark green to bright light green to light yellow. At this point, the texture of the rind appears more smooth compared to the immature fruit. In general, the fruits are harvested from the plant and/or collected from the ground without any criterion of selection. Taking into account that the firmness of umbu decreases with advancing maturity, this could became a reliable maturity index for this fruit. However, due to high genetic variability, the color of the fruit is not correlated to the pulp firmness. Thus, the firmness of umbu can be used as a suitable maturity index, as, on a sensory basis, fruit featuring firmness between 10 and 15 N had the characteristic flavor, texture, and taste that were best assessed by the panel for fresh consumption (Schunemann, 2013). For the industry, lower fruit firmness is desired, although, in general, fruits of a wide range of maturity are mixed together for processing. However, knowledge of the postharvest conservation of umbu is quite limited. The fruit, once harvested, and kept under ambient conditions, is conserved for a maximum 3 days (Moura et al., 2013). The use of refrigeration would increase the supply of umbu and reduce losses resulting from the rapid advance of ripening after harvest. For umbu harvested at physiological maturity and stored at 11 C, 14 C, and 25 C, the lowest temperature resulted in chilling injury. At 14 C, umbu fruits maintained good appearance, firm flesh, and light green color of fruits for 13 days (Silva et al., 2009). For mature umbu, refrigerated storage is possible at 5 C for up to 15 days. Combined with refrigeration, the use of modified atmosphere (MA) by the use of polymeric films and coatings can interfere with the respiratory metabolism of the fruit and the physical mechanisms of water vapor transfer. Therefore, this would represent a more rational perspective of use that could increase the participation of this activity in the income of semiarid farmers. Based on that, the use of MA was the determining factor in maintaining the quality of umbu stored at under ambient conditions (23 6 1 C and 83 6 2% RH) by reducing weight loss, keeping its attractive appearance, allowing the color to develop into a deeper yellow, and providing an increase in shelf life for those fruits, harvested when green or turning to yellow, of 2 and 1 days, respectively (Moura et al., 2013). Lopes (2007) concluded that the use of MA by PVC film of 13 μm thick at 10 6 0.5 C and 90 6 1% RH was crucial to the maintenance of commercial quality of umbu harvested when the rind color was light green for 15 days.
INDUSTRIAL APPLICATION OR POTENTIAL INDUSTRIAL APPLICATION Due to the high perishability of the fruit, storage alternatives and conservation have been studied as the use of fruit for processing for frozen pulp, juices, marmalade, jellies, fermented drinks, nectars, icecream, and umbuzadas (umbu pulp
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cooked with milk and sugar), one of the most traditional foods in the Brazilian semiarid lands (Ferreira et al., 2000, Folegatti et al., 2003; Santos et al., 2006; Machado et al., 2007). Many of these products are already produced in small quantities and are mostly restricted to artisanal production. In this regard, efforts should be made for the development and standardization of postharvest and processing umbu technologies. As examples of potential industrial applications, some authors proposed an umbu jam with reduced sugar content (Mendes and Santos, 1998), umbu pulp powder (Galdino et al., 2003), crystallized umbu (Folegatti et al., 2003), fermented milk drink with mozzarella cheese whey 60% plus umbu pulp (Santos et al., 2006), and fermented umbu pulp beverages with different proportions of whey of cheese. Also, a drink based on whey and umbu pulp was developed by Fontan (2008), and Coelho et al. (2007) studied an umbu liquor with sugarcane alcohol. Considering the high acidity of the umbu pulp, which causes high syneresis in this product during storage, studies aimed at its reduction are being carried out (Borges et al., 2011). The extractive activities of umbu are responsible for generating employment and income for the population of the occurrence areas of the Brazilian semiarid region and have a high potential for development of products in agroindustries of communities. In this context, one of the main problems is the lack of standardization of the product. The adequacy or standardization of conventional technologies and the development of new technologies for the processing of umbu fruit could reduce postharvest losses and promote a more profitable use, by adding value.
FINAL REMARKS The studies conducted up to the present moment with umbu fruit are still insufficient to contribute for a more rational commercial use that adds value of the fruit and its derivatives. There is still the need for several initiatives before these goals are achieved. These include the detailing of the chemical composition of the fruit, highlighting the content of compounds with nutritional value and or that protect the consumer’s health; the definition of more accurate indices of maturity; the formalization of quality standards and identity of the product; as well as investment in packaging and postharvest storage technologies suitable for small farmers. More globally, the activity, which is currently only extractive, demands the selection of genotypes with aptitude for the fresh fruit market and or for the industry; the recommendation of propagation methods that allow early yield, the definition of crop management techniques to reduce the impact of changes in production and fruit quality between years. These elements greatly contribute to the productive organization and ensure a greater insertion of products in the market.
REFERENCES Almeida, A.da.S., Alves, R.E., Araga˜o, F.A.S., Soares, D.J., Freitas, S.P.de.A.F., 2008. Caracterı´sticas fı´sicas de frutos de plantas nativas de umbu´ rido piauiense. In: Congresso Brasileiro de Fruticultura, 20, Vito´ria. Anais. . . 1 CD-Rom. zeiro oriundos do Semi-A Almeida, M.M.de., 1999. Armazenagem refrigerada de umbu (Spondias tuberosa Arruda Caˆmara): Alterac¸o˜es das caracterı´sticas fı´sicas e quı´micas de diferentes esta´dios de maturac¸a˜o. 89f. Dissertac¸a˜o (Mestrado em Engenharia Agrı´cola). Universidade Federal da Paraı´ba, Campina Grande. Borges, S.V., Martins, M.L.A., Mesquita, K.S., Ferrua, F.Q., Cavalcanti, N.B., 2011. Efeito de aditivos sobre a cor durante o armazenamento de doces de umbu (Spondias tuberosa Arr. Caˆmera) verde e maduro. Aliment. Nutr. 22, 307313. Campos, C.de.O., 2007. Frutos de umbuzeiro (Spondias tuberosa Arruda): caracterı´sticas fı´sico-quı´micas durante seu desenvolvimento e na po´s-colheita. 113f. Tese. (Doutorado em Produc¸a˜o Vegetal). Universidade do Estado de Sa˜o Paulo, Botucatu. ´ rido. In: Cavalcanti, N.de.B., Resende, G.M.de., Brito, L.T.de.L., 2001. Imbuzeiro (Spondias tuberosa Arr. Cam.): cultivo apropriado para o Semi-A Simposio Brasileiro de Captac¸a˜o de Agua de Chuva no Semi-Arido, 3, 2001, Campina Grande. Anais. . . Campina Grande: Embrapa Algoda˜o; Petrolina, PE: Embrapa Semi-Arido. CD-ROM. Cavalcanti, NdeB., Resende, G.M., Brito, L.TdeL., 2006. Colheita e comercializac¸a˜o de frutos de imbuzeiro pelos agricultores da regia˜o Semia´rida do Nordeste. Rev. Polı´tica Agrı´c. 15, 8188. Coelho, M.I.S., Albuquerque, L.K.S., Mascarenhas, R.J., Coelho, M.C.S.C., Silva Filho, E.D., 2007. Elaborac¸a˜o de licores de umbu com diferentes alcoo´is. In: Anais do II Congresso de Pesquisa e Inovac¸a˜o da Rede Norte Nordeste de Educac¸a˜o Tecnolo´gica. Joa˜o Pessoa-PB. Costa, F.R., Moura, N.F., Neder, D.G., Rego, E.R., Rego, M.M., Silva, S.M., Schunemann, A.P.P., 2015. Ana´lise biome´trica de frutos de umbuzeiro do Semia´rido brasileiro. Biosci. J. 31, 682690. Costa, N.Pda, Luz, T.L.B., Gonc¸alves, E.P., Bruno, RdeL.A., 2004. Caracterizac¸a˜o fı´sico-quı´mica de frutos de umbuzeiro (Spondias tuberosa Arr. Caˆm.), colhidos em quatro esta´dios de maturac¸a˜o. Biosci. J. 20, 6571. Dantas Ju´nior, O.R., 2008. Qualidade e atividade antioxidante total de frutos de geno´tipos de umbuzeiro. 90 f. Tese. (Doutorado em Agronomia). Universidade Federal da Paraı´ba, Areia. Dantas Ju´nior, O.R., Alves, R.E., Silva, S.M., Lima, M.A.Cde, Araga˜o, F.A.Sde, Soares, D.J., et al., 2008. Atividade antioxidante total em frutos de diferentes geno´tipos de umbuzeiro oriundos de Petrolina, PE. LIV Annual Meeting of the International Society for Tropical Horticulture, 2008, Vito´ria. Book of Abstracts. ISTH/Embrapa Agroindu´stria Tropical, Vito´ria, p. 272.
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Ferreira, J.C., Mata, M.E.R., Braga, M.E.D., 2000. Ana´lise sensorial da polpa de umbu submetida a congelamento inicial em temperaturas criogeˆnicas e armazenadas em caˆmaras frigorı´ficas. Rev. Bras. Prod. Agroind. 2, 717. Folegatti, M.I.S., Matsuura, F.C.A.U., Cardoso, R.L., Machado, S.S., Rocha, A.A.S., Lima, R.R., 2003. Aproveitamento industrial do umbu: processamento de gele´ia e compota. Cieˆnc. Agrotecnol. 27, 13081314. Fontan, G.C.R., 2008. Influeˆncia do uso de espessantes nas caracterı´sticas sensoriais e fı´sico-quı´micas de bebida la´ctea com polpa de umbu. 57f. (Mestrado em Engenharia de Alimentos). Universidade Estadual do Sudoeste da Bahia, Itapetinga. Galdino, P.O., Queiroz, A.JdeM., Figueireˆdo, R.M.Fde, Silva, R.N.Gda, 2003. Avaliac¸a˜o da estabilidade da polpa de umbu em po´. Rev. Bras. Prod. Agroind. 5, 7380. Galva˜o, MdeS., Narain, N., Santos, MdoS.Pdos, Nunes, M.L., 2011. Volatile compounds and descriptive odor attributes in umbu (Spondias tuberosa) fruits during maturation. Food Res. Int. 44, 19191926. Gondim, P.J., 2012. Identificac¸a˜o de carotenoides e quantificac¸a˜o de compostos bioativos e atividade antioxidante em frutos do geˆnero Spondias. 119f. Tese (Doutorado em Agronomia). Centro de Cieˆncias Agra´rias, Universidade Federal da Paraı´ba, Areia. IBGE. Instituto Brasileiro de Geografia e Estatı´stica, 2014. Produc¸a˜o da extrac¸a˜o vegetal e da silvicultura, vol. 29. IBGE, Rio de Janeiro, 56 pp. Lima, R.S.de., 1994. Estudo morfo-anatoˆmico do sistema radicular de cinco espe´cies arbo´reas de uma a´rea de caatinga do Municı´pio de AlagoinhaPE. 103f. Dissertac¸a˜o (Mestrado). Universidade Federal Rural de Pernambuco, Recife. Lima, M.A.Cde, Oliveira, A.Bde, Rosatti, S.R., Santos, A.C.Ndos, Arau´jo, A.Ade, Silva, R.Pda, 2010. Armazenamento refrigerado de umbu sob atmosfera modificada com uso de filme de cloreto de polivinila. Congresso Brasileiro de Fruticultura, XXI, 2010, Natal. Anais do XXI Congresso Brasileiro de Fruticultura. Emparn/UFERSA/Embrapa/SBF, Natal. Lopes, M.F., 2007. Fisiologia da maturac¸a˜o e conservac¸a˜o po´s-colheita do acesso umbu-laranja (Spondias tuberosa Arruda Caˆmara). 123 f. Dissertac¸a˜o (Mestrado em Cieˆncia e Tecnologia de Alimentos). Universidade Federal da Paraı´ba, Joa˜o Pessoa. Machado, S.S., Tavares, J.T.Q., Cardoso, R.L., Machado, C.S., Souza, K.E.P., 2007. Caracterizac¸a˜o de polpas de frutas tropicais congeladas comercializadas no Recoˆncavo Baiano. Cieˆnc. Agron. 38, 158163. Melo, E.A., Andrade, R.A.M.S., 2010. Bioactive compounds and antioxidant potential from the “umbuzeiro” fruits. Aliment. Nutr. 21, 453457. Mendes, A.C.R., Santos, R.C.C., 1998. Aproveitamento do umbu na formulac¸a˜o de gele´ia modificada em sua composic¸a˜o glicı´dica. Rev. Hig. Aliment. 12, 4951. Moura, F.T., Silva, S.M.S., Schunemann, A.P., Martins, L.P., 2013. Frutos do umbuzeiro armazenados em diferentes esta´dios de maturac¸a˜o. Cieˆnc. Agron. 47, 131133. Nadia, T.L., de Machado, I.C., Lopes, A.V., 2007. Polinizac¸a˜o de Spondias tuberosa Arruda (Anacardiaceae) e ana´lise da partilha de polinizadores com Ziziphus joazeiro Mart. (Rhamnaceae), espe´cies frutı´feras e endeˆmicas da caatinga. Rev. Bras. Bot. 30, 89100. Narain, N., Bora, P.S., Holschuh, H.J., Vasconcelos, M.AdaS., 1992. Variation in physical and chemical composition during maturation of umbu (Spondias tuberosa) fruits. Food Chem. 44, 255259. Oliveira, V.Rde, Rezende, M.D.Vde, Nascimento, C.EdeS., Drumond, M.A., Santos, C.A.F., 2004. Variabilidade gene´tica de procedeˆncias e progeˆnies de umbuzeiro via metodologia de modelos lineares mistos (REML/BLUP). Rev. Bras. Frutic. 26, 5356. Pires, M.G.M., 1990. Estudo taxonoˆmico e a´rea de ocorreˆncia de Spondias tuberosa Arr. Cam. (umbuzeiro) no Estado de Pernambuco - Brasil. 290 f. Dissertac¸a˜o (Mestrado em Botaˆnica). Universidade Federal Rural de Pernambuco, Recife. Purseglove, J.W., 1984. Anacardiaceae. In: Purseglove, J.W. (Ed.), Tropical Crops Dicotyledons. Longman, London, pp. 1832. Rufino, MdoS.M., Alves, R.E., Brito, E.Sde, Pe´rez-Jime´nez, J., Saura-Calixto, F., Mancini-Filho, J., 2010. Bioactive compounds and antioxidant capacities of 18 non-traditional tropical fruits from Brazil. Food Chem. 121, 9961002. Santos, C.A.F., 1997. Dispersa˜o da variabilidade fenotı´pica do umbuzeiro no Semi-a´rido brasileiro. Pesqui. Agropecu. Bras. 32, 923930. Santos, C.A.F., Nascimento, C.EdeS., 1997. Relac¸a˜o entre caracteres quantitativos do umbuzeiro (Spondias tuberosa A. Camara). Pesqui. Agropecu. Bras. 33, 449456. Santos, C.A.F., Nascimento, C.EdeS., Campos, O.C., 1999. Preservac¸a˜o da variabilidade gene´tica e melhoramento do umbuzeiro. Rev. Bras. Frutic. 21, 104109. Santos, C.T., Marques, G.M.R., Fontan, G.C.R., Fontan, R.C.I., Bonomo, R.C.F., Bonomo, P., 2006. Elaborac¸a˜o e caracterizac¸a˜o de uma bebida la´ctea Fermentada com polpa de umbu (Spondias tuberosa sp.). Rev. Bras. Prod. Agroind. 8, 111116. Schunemann, A.P.P., 2013. Qualidade e perfil sensorial de frutas nativas e na˜o tradicionais do Nordeste do Brasil. Relato´rio Parcial, MCT/CAPES/ PNPD. Silva, A.Qda, Silva, Ada, 1974. Observac¸o˜es morfolo´gicas e fisiolo´gicas sobre Spondias tuberosa Arr. Cam. Congresso Nacional de Botaˆnica, 25. 1974. Mossoro´. Anais. . .. Sociedade de Botaˆnica do Brasil, Recife, pp. 515. Silva, C.M.MdeS., Pires, I.E., Silva, H.Dda, 1987. Caracterizac¸a˜o de frutos do umbuzeiro.. EMBRAPA-CPATSA, Petrolina, 17 pp. (EMBRAPACPATSA. Boletim de Pesquisa, 34). Silva, R.Pda, Lima, M.A.Cde, Santos, A.C.Ndos, Costa, A.C.S., Lima, C.BdaS., 2009. Conservac¸a˜o po´s-colheita de umbu sob diferentes temperaturas ´ rido, IV. Anais. . .. Embrapa Semi-A ´ rido, Petrolina, pp. 211217. de armazenamento. Jornada de Iniciac¸a˜o Cientı´fica da Embrapa Semi-A
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Uvaia—Eugenia pyriformis Cambess Angelo P. Jacomino1, Aline P.G. da Silva1, Thais P. de Freitas1 and Veroˆnica S. de Paula Morais2 1
University of Sa˜o Paulo, Luiz de Queiroz College of Agriculture, Piracicaba, Sa˜o Paulo, Brazil, 2Federal Institute of Education, Science and
Technology of Southern Minas Gerais, IFSULDEMINAS, Inconfidentes, Minas Gerais, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects 435 Harvest Season 435 Estimated Annual Production 436 Fruit Physiology and Biochemistry 436 Chemical Composition and Nutritional Value Including Vitamins, Minerals, Phenolics, and Antioxidant Compounds 436 Sensory Characteristics 436
Harvest and Postharvest Conservation Harvest Postharvest Conservation Industrial Application or Potential Industrial Application Acknowledgments References Further Reading
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CULTIVAR ORIGIN AND BOTANICAL ASPECTS The uvaia (Eugenia pyriformis Cambess) is a plant in the family Myrtaceae, which is one of the most important families in the Brazilian flora due to its large number of genera (23) and species (1034) (Landrum and Kawasaki, 1997; Souza and Lorenzi, 2005, Sobral et al., 2003). The uvaia is native to the Atlantic Forest occurring throughout its extension in south, southeast, and northeast Brazil. However, its occurrence has been reported in central-west Brazil, outside the Atlantic Forest biome (Sobral et al., 2003). The species is known by different names including uvaia, ubaia, uvalha, orvalha, and uvalheira (Landrum and Kawasaki, 1997) and can be found in gardens and domestic orchards, especially in the southeast. The existence of different species and accessions of uvaia has been proposed in some studies. Scalon et al. (2004b) described the existence of two species, E. pyriformis and Eugenia uvalha. However, E. pyriformis has been accepted as the botanical name for uvaia and E. uvalha is considered a synonym of E. pyriformis. Sartori et al. (2010) reported the existence of seven E. pyriformis accessions: Bolı´via, Comum, Doce, Doce de Patos de Minas, Peˆra, Rugosa, and Rugosa Doce. The uvaia is a medium-sized tree (6a13 m) with rounded or elongated crown. Leaves are opposite, glabrous, subcoriaceous, pinkish-red in color when young, and 4a7 cm in length. Flowers are white, solitary, hermaphrodite, tetramerous with great number of stamens. Fruit are berry-type, rounded, with thin, velvety epicarp and yellow or orange fleshy pulp. Trunk are usually erect and the bark tends to peel off in large pieces (Lorenzi, 2002). Seeds are large, 1a3 per fruit, with high germination capacity (Mattos, 1954; Silva et al., 2003, 2005).
HARVEST SEASON In the southeast, the species flowers in the months of August and September and harvest occurs in October and November (Sartori et al., 2010), but it may come early or be delayed depending on climatic conditions, especially rainfall. In the southern state of Rio Grande do Sul, Brazil, flowering occurs in November and December and fruit harvest occurs between January and February (Marchiori and Sobral, 1997). Even though flower and fruit production are highest in those periods, off-season flowering events and the presence of fruits at different stages of development in the same plant are often observed, which may require frequent harvests and favor the occurrence of pests and diseases such as fruit flies and rust. Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00058-7 © 2018 Elsevier Inc. All rights reserved.
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ESTIMATED ANNUAL PRODUCTION Commercial uvaia orchards are rare and fruit production comes predominantly from domestic orchards, which makes it difficult to collect basic data that are essential to estimate crop performance. According to Douglas Bello (personal communication., 2015), a fruit producer in Paraibuna, Sa˜o Paulo, 10-year old plants pruned to a canopy height of 2.5 m produce 5 kg of fruit per plant on average. Nevertheless, some plants may produce up to 50 kg of fruit in a harvest season.
FRUIT PHYSIOLOGY AND BIOCHEMISTRY Studies about the physiology and postharvest technology of uvaia are scarce. Field observations have shown that uvaia fruits, which are usually harvested fully ripe, are highly perishable. Preliminary studies about the optimal harvest time of uvaia in our laboratory reveal that fruits harvested with a green skin show a significant change in skin color, soluble solids, and total titratable acidity along the postharvest period, but do not achieve the same quality as fruits harvested when ripe. Additionally, these studies have also shown a great variation in respiratory activity (40a120 mL CO2/kg per h) and ethylene production (5a40 μL C2H4/kg per h) depending on the time of harvest and the number of days after harvest. Thus, these current findings cannot confirm whether the uvaia are classified as climacteric or nonclimacteric fruits.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING VITAMINS, MINERALS, PHENOLICS, AND ANTIOXIDANT COMPOUNDS Studies of the chemical composition of uvaia show that fruits have high nutritional value (Mattos, 2013), are a good source of vitamin C (73a120 mg ascorbic acid per 100 g), and have high levels of iron and zinc (Pereira et al., 2014). Uvaia are also a natural source of bioactive compounds due to their high contents of phenolic compounds and carotenoids. Silva et al. (2014) reported carotenoid content of 1300 mg/100 g fresh weight, and according to Haminiuk et al. (2011), uvaia fruits are an important source of antioxidants. Acidity is moderate and the pH of the fruit ranges from 2.87 to 3.11 (Scalon et al., 2004a; Miguel et al., 2015). Uvaia fruits maintain their nutritional quality after processing. According to Zillo et al. (2013), fresh uvaia and frozen pulp have similar contents of ascorbic acid (100.73 and 84.74 mg/100 g), total carotenoids (0.91 and 0.366 μg/g), and phenolic compounds (4.89 and 6.07 mg gallic acid/100 mL). Even after pasteurization, the content of ascorbic acid (83.07 mg/100 g) and antioxidants (5.98 mg/mL) remain unaltered (Zillo et al., 2014). These data suggest that uvaia are a nutritious fruits that can potentially be consumed in both fresh and processed form.
SENSORY CHARACTERISTICS The skin color of uvaia fruits ranges from yellow to orange. The skin is thin, highly susceptible to mechanical damage, and may be smooth or velvety. Fruits have a distinctive, intense, and pleasant aroma. The pulp is soft, fleshy, juicy, with acidic flavor, and most fruits have a total titratable acidity of approximately 2%. Nevertheless, studies conducted in our laboratory have shown that some plants produce fruits with lower acidity values. These studies have also revealed that orchards consisting of plants originating from seeds of the same tree may produce fruits that show a great variability in fresh weight (10.9a35.4 g), shape (piriform or flattened), color (yellowish to orange), and soluble solids contents (5.38a8.6 Brix). Miguel et al. (2015) observed that the physicochemical characteristics of fruits varied across uvaia accessions. In addition to high pulp yields, accessions “Rugosa Doce,” “Peˆra,” “Doce de Patos de Minas,” and “Doce” had the highest solids/titratable acidity (SS/TA) ratios (11.21, 9.48, 8.02, and 7.59, respectively), an indicative of pulp quality. Conversely, the accessions “Comum,” “da Bolı´via,” and “Rugosa” had the lowest SS/TA ratios (5.21, 6.99, and 6.84, respectively). Nevertheless, further studies are needed for the characterization of uvaia accessions.
HARVEST AND POSTHARVEST CONSERVATION Harvest Because of the various flowering events and the rapid fruit development at the end of the physiological cycle, fruits should be harvested two or three times per week and the harvest point should be determined individually based on skin color and pulp firmness.
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The fruits are harvested by twisting to detach them from the stem. However, to reduce postharvest damage, clippers can be used to cut the peduncle close to the fruit. Fruits should be harvested in the early hours of day when air and fruit temperatures are cooler. Fruits should be picked and stored carefully into baskets or containers lined with foam blanket, polyethylene blanket (“bubble wrap”), or equivalent.
Postharvest Conservation Few studies have investigated the postharvest conservation of uvaia fruits. Because uvaia is a tropical fruit, exposure to low temperatures may result in chilling injury. Therefore, although refrigeration is one of the most efficient techniques to delay senescence in horticultural products, it should be done with caution for uvaia fruits. The minimum storage temperature for uvaia has not yet been determined. Plastic films can be used for storage to delay senescence and reduce water losses. Many polymers are used for fruit storage, including polyvinyl chloride (PVC), low density polyethylene, polypropylene, nylon, or a mixture of more than one material. Scalon et al. (2004b) evaluated the packaging of uvaia fruit at 13 C and 30 C using PVC packaging and preservative film containing an ethylene absorber and found that packaged fruits retained their appearance and quality for four days at 30 C and 12 days at 13 C. Preliminary tests conducted in our laboratory have shown differences in storage potential between varieties, indicating that some varieties may be best consumed in fresh form.
Industrial Application or Potential Industrial Application Uvaia has large industrial potential for consumption in the form of jams, juices, icecream, liqueurs, compotes, conserves, or added to other processed products such as yogurts (Andersen and Andersen, 1988; Andrade and Ferreira, 2000; Delgado and Barbedo, 2007; Sartori et al., 2010). Because of its acid and distinctive taste and pleasant aroma, uvaia fruits have a large potential that can be exploited by the food and cosmetics industries (Di-Stasi and HirumaLima, 2002). Moreover, uvaia is a promising source of bioactive compounds (Karwowski et al., 2013; Silva et al., 2014) and may cater to a consumer market attracted to new foods. Several studies have reported on the interaction between industrial application and functional quality of bioactive compounds in native fruits. There is a growing interest in combining the sensory attributes and protective effects of fruits against chronic and degenerative diseases. In the case of uvaia, these effects have been attributed to the antioxidant capacity of phenolics and carotenoids found in its pulp. The Federal Institute of Southern Minas Gerais (campus Inconfidentes) has been developing uvaia processing technologies to obtain products that retain the sensory and nutritional attributes of fresh fruit. Products including compotes, jam, liqueur, ratafia, icecream, and icecream bars have been prepared using different methods and amounts of fresh fruit. Acceptability scores were high for all products in sensory analysis, especially for recipes that preserved the fruit taste, such as the icecream bars with high pulp content. Despite the small number of studies, the potential for commercial exploitation of uvaia is comparable to that of other tropical fruits. The physicochemical attributes of uvaia provide opportunities for its use in different sectors, including the food and pharmaceutical industries. Further studies on fruit quality and the dissemination of scientific research about its benefits to consumers may help increase the demand for uvaia fruits. Moreover, the commercial exploitation of uvaia can promote the socioeconomic development of producers and regions suitable for uvaia production, generating investments and diversifying agricultural production.
ACKNOWLEDGMENTS Our thanks to grant #2014/12606-3, #2014/13473-7 and #2016/03024-6 Sa˜o Paulo Research Foundation (FAPESP), to the Coordination for the Improvement of Higher Education Personnel (CAPES) and to the National Council for Scientific and Technological Development (CNPq) for research grant number 458123/2014-5 financial support and for scholarships. Thanks to Dr. Se´rgio Sartori, a physician and collector of fruit specimens, and to Hugo Daibs, rural producer, for providing the fruits. Thanks to researchers Evando Luiz Coelho and Lilian Andrade Vilela of Instituto Federal de Educac¸a˜o, Cieˆncia e Tecnologia do Sul de Minas and to Dr. Horst Bremer Neto of Universidade de Sa˜o Paulo, for their support with this research.
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REFERENCES Andersen, O., Andersen, V.U., 1988. As frutas silvestres brasileiras. second Ed. Edic¸o˜es Globo, Rio de Janeiro. Andrade, R.N.B., Ferreira, A.G., 2000. Germinac¸a˜o e armazenamento de sementes de uvaia (Eugenia pyriformis Camb.) Myrtaceae. Rev. Bras. Sementes. 22, 118125. Delgado, L.F., Barbedo, C.J., 2007. Toleraˆncia a` dessecac¸a˜o de sementes de espe´cies de Eugenia. Pesqui. Agropecu. Bras. 42, 265272. Di-Stasi, L.C., Hiruma-Lima, C.A., 2002. Plantas medicinais na Amazoˆnia e na Mata 206 Atlaˆntica. Editora Universidade Estadual Paulista, Sa˜o Paulo, 604 pp. Haminiuk, C.W.I., Plata-Oviedo, M.S.V., Guedes, A.R., Stafussa, A.P., Bona, E., Carpes, S.T., 2011. Chemical, antioxidant and antibacterial study of Brazilian fruits. Int. J. Food Sci. Technol. 46, 15291537. Karwowski, M., Masson, M., Lenzi, M., Scheer, A., Haminiuk, C., 2013. Characterization of tropical fruits: rheology, stability and phenolic compounds. Acta Aliment. 42, 586598. Landrum, L.R., Kawasaki, M.L., 1997. The genera of Myrtaceae in Brazil an illustrated synoptic treatment and identification keys. Brittonia. 49, 508536. ´ rvores brasileiras. Plantarum, Nova Odessa. Lorenzi, H., 2002. A Marchiori, J.N.C., Sobral, M., 1997. Dendrologia das Angiospermas: Myrtales. Universidade Federal de Santa Maria, Santa Maria. Mattos, J.R., 1954. Estudo pomolo´gico dos frutos indı´genas do Rio Grande do Sul. Oficinas Gra´ficas da Imprensa Oficial Porto Alegre. Mattos, G.D., 2013. Extrac¸a˜o e quantificac¸a˜o de a´cidos feno´licos e flavono´ides de Eugenia pyriformis Cambess usando diferentes solventes. Trabalho de conclusa˜o de curso-Universidade Tecnolo´gica Federal do Parana´, Campus Campo Moura˜o, Parana´, 34 pp. Miguel, A.C.A., Silva, A.P.G., Tokairin, T.O., Jacomino, A.P., 2015. Qualidade de uvaias de distintas variedades produzidas no municı´pio de Rio Claro-SP. In: Congresso Brasileiro de Processamento mı´nimo e Po´s-colheita de frutas, flores e hortalic¸as, 001. Anais. . . Aracaju-SE. Pereira, M.C., Boschetti, W., Rampazzo, R., Celso, P.G., Hertz, P.F., Rios, A.O., et al., 2014. Mineral characterization of native fruits from the southern region of Brazil. Food Sci. Technol. 34, 258266. Sartori, S., Donadio, L.C., Martins, A.B.G., Moro, F.V., 2010. Uvaia. Funep, Jaboticabal, 32 pp.: il.; 21 cm (Se´rie Frutas Nativas, 11). Scalon, S.P.Q., Dell’Olio, P., Fornasieri, J.L., 2004a. Temperatura e embalagens na conservac¸a˜o po´s-colheita de Eugenia uvalha CambessMirtaceae. Cieˆnc. Rural. 34, 19651968. Scalon, S.P.Q., Scalon Filho, H., Rigoni, M.R., 2004b. Armazenamento e germinac¸a˜o de sementes de uvaia Eugenia uvalha Cambess. Cieˆnc. Agrotecnol. 28, 12281234. Silva, C.V., Bilia, D.A., Maluf, A.M., Barbedo, C.J., 2003. Fracionamento e germinac¸a˜o de sementes de uvaia (Eugenia pyriformis Cambess. Myrtaceae). Rev. Bras. Bot. 26, 213221. Silva, C.V., Bilia, D.A.C., Barbedo, C.J., 2005. Fracionamento e germinac¸a˜o de sementes de Eugenia. Rev. Bras. Bot. 27, 8692. Silva, N.Ada, Rodrigues, E., Mercadante, A.Z., Rosso, V.Vde, 2014. Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic Forest. J. Agric. Food Chem. 62, 50725084. Sobral, M., Proenc¸a, C., Souza, M., Mazine, F., Lucas, E., 2003. Myrtaceae in Lista de Espe´cies da Flora do Brasil. Jardim Botaˆnico do Rio de Janeiro. Souza, V.C., Lorenzi, H., 2005. Botaˆnica Sistema´tica: guia ilustrado para a identificac¸a˜o das famı´lias de Angiospermas da flora brasileira, baseado em APG/II. Instituto Plantarum, Nova Odessa. Zillo, R.R., Silva, P.P.Mda, Zanatta, S., Carmo, L.Fdo, Spoto, M.H.F., 2013. Qualidade fı´sico-quı´mica da fruta in natura e da polpa de Uvaia congelada. Rev. Bras. Prod. Agroind. 15, 293298. ́ ́ Zillo, R.R., Silva, P.P.Mda, Zanatta, S., Spoto, M.H.F., 2014. Parâmetros fisico-qui micos e sensoriais de polpa de uvaia (Eugenia pyriformis) submetidas à pasteurizac¸a˜o. Bioenergia em revista: dia´logos. 4, 2033.
FURTHER READING Sampaio, V.R., 1983. Propagac¸a˜o da uvaieira (Eugenia uvalha Cambess. Myrtaceae) atra´ves da enxertia por garfagem. Anais da Escola Superior de Agronomia “Luiz de Queiroz”. 40, 9599.
Wampee—Clausena lansium Sueli Rodrigues1, Edy Sousa de Brito2 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects Harvest Season
439 439
Composition and Uses References
439 441
CULTIVAR ORIGIN AND BOTANICAL ASPECTS Wampee (Clausena lansium (Lour.) Skeels), originated in southern China, is a member of the Rutaceae family and a distant relative of citrus fruit. Wampee has many vernacular names, most derived from the Chinese language. The wampee fruit varieties are different in ripening season, number of seeds, form, size and flavor. The seven Chinese varieties are: “Niu Shen” (“cow’s kidney”)sour in flavor; “Yuan Chung” (“globular variety”)sweet-subacid; “Yeh Sheng” (“wild growing”)sour; “Suan Tsao” (“sour jujube”)is very sour, of poor quality; “Hsiao Chi Hsien” (“small chicken heart”)sweet-subacid; “Chi Hsin” (“chicken heart”)sweet; “best flavor of all”; “Kua Pan” (“melon section”)sweet-subacid. The fruit is commonly cultivated in southern China and the northern part of former French Indochina, especially from north to central Vietnam. It was cultivated in the Philippines before 1837 and reintroduced in 1912. The fruit is also grown in India, Malaysia and Singapore in home gardens. The fruit is also cultivated to a limited extent in Queensland (Australia) and Hawaii. Brought to Florida as an unidentified species in 1908, the tree does well in the greenhouse and is tolerant in several soils, including the deep sand soil in Florida. The plant needs watering in dry periods and good drainage is essential. The propagation is by seedling, which germinates in a few days. Softwood cuttings and air-layers are another way of propagation. The tree can reach 6 m, with long, upward-slanting, flexible branches, and gray-brown bark rough to the touch (Fig. 1). The petiole also is warty and hairy. The sweet-scented, 4- to 5-parted flowers are whitish or yellowish-green, about 1.25 cm wide, and borne in slender, hairy panicles 1050 cm long. The fruits, on 0.61.25 cm stalks, hang in showy, loose clusters of several strands. The wampee may be round, or conicaloblong, up to 2.5 cm long, with five faint, pale ridges extending a short distance down from the apex. The thin, pliable but tough rind is light brownishyellow, minutely hairy and dotted with tiny, raised, brown oil glands. It is easily peeled and too resinous to be eaten. The flesh, faintly divided into five segments, is yellowish-white or colorless, grapelike, mucilaginous, juicy, pleasantly sweet, subacid, or sour. There may be 15 oblong, thickish seeds bright-green with one brown tip. The wampee is not a first-class fruit, and the tree is of only casual interest, even as an ornamental, except in Asia (see Fig. 2).
HARVEST SEASON The wampee fruit ripens from May to July and tastes similar to grapefruit when ripe; resembles a grape, and is about 2.0 cm in diameter. It contains 13 seeds and the pulp is slightly acidic (Chokeprasert et al., 2007).
COMPOSITION AND USES Wampee fruits (C. lansium (Lour.) Skeels) contain a significant amount of coumarins with many health benefits including antioxidant activity against DPPH and superoxide anion. The fruit extract showed to be effective against human Exotic Fruits Reference Guide. DOI: http://dx.doi.org/10.1016/B978-0-12-803138-4.00059-9 © 2018 Elsevier Inc. All rights reserved.
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FIGURE 1 Wampee in tree.
FIGURE 2 Wampee fruit.
hepatocellular liver carcinoma cell line (HepG2), human lung adenocarcinoma epithelial cell line (A549), and human cervical carcinoma cell line (Prasad et al., 2010). The steams of C. lansium presented four coumarins (chalepensin, chalepin, gravelliferone, and angustifolin), together with sitosterol and the carbazole alkaloids, indizoline and the new 2,7dihydroxy-3-formyl-1-(Y-methyl-20 -butenyl)carbazol (Du et al., 2015). The steam also presented antinflammatory effects (Shen et al., 2012). Due to the medicinal properties, wampee roots and fruits are utilized in Chinese and Thailand’s popular medicine. The leaves are also used for the treatment of coughs, asthma, and gastrointestinal diseases. The wampee seeds are used for gastrointestinal diseases such as acute inflammation and ulcers. The fruit has cooling effects and is used ethnomedicinally as a vermifuge and for digestive disorders (Lin, 1989). The halved, sun-dried immature fruits and slices of dried roots and stems are used in Vietnam and oriental countries for bronchitis and malaria treatment (Li et al., 1991; Kumar et al., 1995; Maneerat et al., 2012). Different parts are used in Chinese medicine such as the treatment of acute and chronic viral hepatitis (Adebajo et al., 2009).
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441
The leaves are used in Sri Lanka as a substitute for curry leaf in cooking (false curry). The ripened wampee of subacid type is eaten out-of-hand like a grape. The seeds are discharged. The pulp can be added to fruit cups, gelatins, or other desserts, used to make pies and jams. The jelly is made only from the under-ripe acid types. The seeded fruits are served with meat dishes in China. The fermented fruit juice is consumed as carbonated beverage that resembles champagne in southeast Asia. The fruit can be also eaten with the peel, but the most traditional product is the dried fruit, which is produced in Thailand (Chokeprasert et al., 2007). There is little research on the volatile compounds responsible for the wampee intense aroma. The major compounds responsible for the wampee fruit aroma, determined by volatile headspace components are sabinene, ethanol, acetic acid, α-pinene, α-phenallandiene, myrcene, (1) 4-carene, 1,4-cyclohexadiene, cyclohexadiene, and 3-cyclohexanol (Chokeprasert et al., 2007).
REFERENCES Adebajo, A.C., Iwalemwa, E.O., Obuotor, E.M., Ibikunle, G.F., Omisore, N.O., Adewunmi, C.O., et al., 2009. Pharmacological properties of the extract and some isolated compounds of Clausena lansium stem bark: anti-trichomonal, antidiabetic, anti-inflammatory, hepatoprotective and antioxidant effects. J. Ethnopharmacol. 122 (1), 1019. Chokeprasert, P., Charles, A.L., Sue, K.S., Huang, T.C., 2007. Volatile components of the leaves, fruits and seeds of wampee [Clausena lansium (Lour.) Skeels]. J. Food Comp. Anal. 20 (1), 5256. Du, Y.Q., Liu, H., Li, C.J., Ma, J., Zhang, D., Li, L., et al., 2015. Bioactive carbazole alkaloids from the stems of Clausena lansium. Fitoterapia. 103, 122128. Kumar, V., Vallipuram, K., Adebajo, A.C., Reisch, J., 1995. 1,7-Dihydroxy-3-formyl-1-(30-methyl-20-butenyl) carbazole from Clausena lansium. Phytochemistry. 40, 15631565. Li, W.S., McChesney, J.D., El-Feraly, F.S., 1991. Carbazole alkaloids from Clausena lansium. Phytochemistry 30, 343346. Lin, J.H., 1989. Cinnamamide derivatives from Clausena lansium. Phytochemistry 28, 621622. Maneerat, W., Ritthiwigrom, T., Cheenpracha, S., Laphookhieo, S., 2012. Carbazole alkaloids and coumarins from Clausena lansium roots.” Phytochem. Lett. 5 (1), 2628. Prasad, K.N., Xie, H., Haoam, J., Yanga, B., Qiu, S., Weia, X., et al., 2010. Antioxidant and anticancer activities of 8-hydroxypsoralen isolated from wampee [Clausena lansium (Lour.) Skeels] Peel. Food Chem. 118 (1), 6266. Shen, D.Y., Chao, C.H., Chan, H.H., Huang, G.J., Hwang, T.L., Lai, C.Y., et al., 2012. Bioactive constituents of Clausena lansium and a method for discrimination of aldose enantiomers. Phytochemistry 82, 110117.
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Wood Apple—Limonia acidissima Sueli Rodrigues1, Edy Sousa de Brito2 and Ebenezer de Oliveira Silva2 1
Federal University of Ceara´, Fortaleza, Ceara´, Brazil, 2Embrapa Agroindu´stria Tropical, Fortaleza, Ceara´, Brazil
Chapter Outline Cultivar Origin and Botanical Aspects 443 Fruit Physiology and Biochemistry 443 Chemical Composition and Nutritional Value Including Vitamins, Mineral, Phenolics and Antioxidant Compounds 444 Harvest and Postharvest Conservation 444
Potential Industrial Application Medicinal Use Food Uses References
444 444 446 446
CULTIVAR ORIGIN AND BOTANICAL ASPECTS The wood apple is one of the common names of an edible fruit from several trees, mainly those belonging to genus Limonia acidissima L. (synonyms: Feronia limonia syns, Feronia elephantum Correa; Schinus limonia L.). The fruit from the genus Aegle marmelos, a native tree from India, where the fruit is known as “Bael,” is also known as the wood apple. The fruit shape resembles an apple and the name wood apple is due to the fruit hard shell. Native to India, the tree is cultivated in other countries such in Pakistan, Sri-Lanka, and Bangladesh. The fruit is also known as elephant-apple, monkey fruit or crud fruit. The plant belongs to the Rutaceae family (Muthumperumal and Parthasarathy, 2009), it is deciduous and grows up to 9 m. The bark is rough, and the fruits are woody and rough. The wood apple is common in dry plains and a monsoon climate with a distinct dry season. The tree might grow up to an elevation of 450 m, as in the western Himalayas. The tree is drought tolerant and adapted to light soils. The spines are axillary, short, straight, 25 cm long on some of the zigzag twigs. The leaves are deciduous, alternate, dark green, leathery and 35 in. long with oil glands and slightly lemon-scented when crushed. The flowers are normally bisexual, small numerous, dull-red or greenish, borne in small, loose, terminal or lateral panicles. The berry fruit is globose, the shape is round to oval and 25 in. wide, with a hard, woody rind (Fig. 1). The brown pulp is resinous, astringent, aromatic odorous, acid or sweetish with scattered seeds. The fruit might be large and sweet or small and acid (Vijayvargia and Vijayvergia, 2014).
FRUIT PHYSIOLOGY AND BIOCHEMISTRY According to Lakshmi et al. (2015), the wood apple is a ripening fruit and the changes observed at the three characteristic stages (unripe, semiripe, and ripe) are the increase of total sugars reaching up to about 5 g/100 g, acidity decrease reaching about 3 g/100 g. Sucrose is the predominant sugar in all ripening stages. The major organic acid is citric acid with the highest levels (B2 g/100 g) in the unripe fruits and the lowest (B1.6 g/100 g) in the ripe fruits. The higher level of citric acid is expected because the fruit also belongs to the Rutaceae family. Different from other fruits, the soluble solids reduced due to the fruit ripening from 20 to 14 Brix. On the other hand, the total phenolics and total protein increased in ripe fruit. The phenolics presented in the wood apple are mainly bound with a strong correlation between the reducing power and the phenolic content.
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FIGURE 1 Wood apple fruit.
CHEMICAL COMPOSITION AND NUTRITIONAL VALUE INCLUDING VITAMINS, MINERAL, PHENOLICS AND ANTIOXIDANT COMPOUNDS Three volatile flavor-components are obtained from fresh wood apple fruit, namely, methyl hexanoate, ethyl-3hydroxyhexanoate, and butanoic acid (Qureshi et al., 2010; Patel, 2013). The fruit is used for relief from diarrhea, dysentery, tumors, asthma, wounds, cardiac debility, and hepatitis. The fruit contain flavonoids, saponin, tannins, and glycosides. Coumarins and tyramine derivatives were isolated from the fruits. The leaves present hepatoprotective activity and the fruit shells have antifungal compounds such as psoralene, xanthotoxin, 2,6-dimethoxybenzoquinone, and osthenol (Pradhan et al., 2012). The fruit pulp represents 36% of the whole fruit. The pectin content of the pulp is 3%5%. The seeds contain a bland, non-bitter, oil that is high in unsaturated fatty acids (Morton, 1987). Table 1 depicts the centesimal edible pulp composition.
HARVEST AND POSTHARVEST CONSERVATION The wood apple grows in Thailand, Malaysia, Cambodia, and other parts of Southeast Asia. The tree is resistant to dry conditions and adaptable to several kinds of soil. The fruits are harvested at the green stage and plants starts bearing fruits after 5 years of planting. The season for wood apple planting in India is FebruaryMarch or JulyAugust. In mature fruits the shell is light green and the pulp is deep yellow (Fig. 2). The fruits take 1012 months to ripen on the tree. The fruits should be harvest individually with a portion of the fruit stalk. They should not fall onto the ground. No information on annual production was found because the tree is cultivated by small producers and the fruit is sold in the local marked. The plants, at the age of 1012 years, can yield from 20 to 30 t of fruits per hectares of land. In Sri-Lanka the harvest season is AugustSeptember and the estimated production is 200300 fruits per tree. As a dry-tolerant plant, wood apple can be utilized to improve productivity of marginal rain-fed lands with low investment. The fruit weighs between 130 and 225 g (Vilpulasena et al., 2010).
POTENTIAL INDUSTRIAL APPLICATION Medicinal Use Wood apple fruits are reported to be a tonic for liver and lungs, stomachic stimulant, astringent, aphrodisiac, diuretic, cardiotonic and cures coughs and hiccups, and is good for asthma, tumors, ophthalmia, and leucorrhea. Unripe fruit is astringent while seeds are used in for heart disease. The fruits are used as a substitute for bael (Eagle marmelos) in diarrhea and dysentery. Leaves are astringent and good for vomiting, indigestions, hiccups, and dysentery. The leaves have hepatoprotective activity. The gum is demulcent and constipating, and is useful in diarrhea, dysentery, gastropathy,
TABLE 1 Centesimal Composition and Micronutrients of the Wood Apple Edible Pulp (Patel, 2013) Food value (pulp)
Content
Moisture
74.03%
Protein
1.96%
Fat
3.31%
Ash
1.35 g/100 g
Reducing sugar
1.23 g/100 g
Total sugar
2.12 g/100 g
pH
3.72
Acidity (citric acid)
1.94%
Ascorbic acid
7.00 mg/100 g
Fiber
0.65%
Pectin
2.12%
Total soluble solids
11.56 Brix
Calciuma
15.9 (mg/100 g)
a
3.5 (mg/100 g)
Iron
a
Sodium
8.5 (mg/100 g)
Phosphorusa
46.5 (mg/100 g)
a
386.3 (mg/100 g)
Zinc
a
0.8 (mg/100 g)
Copper
a
Manganese a
Ghosh et al. (2010).
FIGURE 2 Wood apple in tree.
0.7 (mg/100 g)
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hemorrhoids, and diabetes (Vijayvargia and Vijayvergia, 2014). The fruits and leaves are prescribed for vomiting, hiccups, dysentery, indigestion, and slight bowel affections in children (Patel, 2013).
Food Uses Wood apple fruit can be eaten plain or mixed into a variety of beverages and desserts, or preserved as jam (Vidhya and Narain, 2011). The scooped-out pulp is eaten raw with or without sugar, or is blended with coconut milk and palmsugar syrup and frozen as an icecream. In Indonesia, wood apple is mixed with honey and eaten for breakfast (Morton, 1987). In Thailand, leaves are eaten in salads while in India the pulp is used in savory chutneys. The fruit pulp is used for the preparation of jam, jelly, chutney, fruit bars (Vidhya and Narain, 2011), and ready-to-serve beverages (Lande et al., 2010). Wood apple is a highly underutilized and seasonal fruit. The demand for wood apple fruit has increased remarkably in the past few decades. The fruit shell is usually opened with a hammer, and its sticky pulp is removed from shell manually using a stainless steel spoon (Patel, 2013). A bottled nectar is made by diluting the pulp with water, passing through a pulper to remove seeds and fiber, further diluting, straining, and pasteurizing (Patel, 2013). A clear juice for blending with other fruit juices is obtained by clarifying the nectar with pectinases. Pulp sweetened with syrup of cane or palm sugar has been canned and sterilized. The pulp can be freeze-dried for future use but it has not been satisfactorily dried by other methods (Morton, 1987). The juice extraction can be done by using machinery such as presses, decanters, centrifuges, pulpers/finishers. Several types of presses are available such as traditional rack and cloth press, hydraulic press, screw press, horizontal press, and belt press. While selecting a juice extraction machinery, the nature of the material to be treated must be taken into account (Patel, 2013). Patel (2013) studied the wood apple juice processing regarding the pulp extraction, the juice formulation, and pasteurization. The wood apple juice obtained from standardized juice extraction presented 5.6 6 0.21 Brix; 0.71 6 0.16 of titratable acidity, 4.73 6 0.115 mg/100 g of ascorbic acid content. The total sugar and reducing sugar were 1.53 and 1.14 g/100 g respectively. The juice pH was 3.71 6 0.02 and the pectin content 0.51 6 0.05% while clarity at 590 nm was 35.13 6 0.26% T. The sensory evaluation was carried out with the standardized wood apple juice. The score obtained of overall acceptability was of juice 7.45. All evaluated attributes (color and appearance, flavor, taste and overall acceptability) presented mean scores higher than 7.0, and in the acceptance range.
REFERENCES Ghosh, S.N., Banik, A.K., Banik, B.C., 2010. Conservation, multiplication and utilization of wood apple (Feronia limonia) a semi-wild fruit crop in West Bengal (India). In: International Symposium on Minor Fruits and Medicinal Plants, pp. 12081214, 1922 December 2011, West Bengal. Lakshmi, Y., Ushadevi, A., Baskaran, R., 2015. Post-harvest ripening changes in wood apple (Feronia elephantum Corr), an underutilized fruit. Int. J. Fruit Sci. 15 (4), 425441. Lande, S.B., Nirmal, V.S., Kotecha, P.M., 2010. Studies on ready to serve beverages from wood apple pulp. Beverages Food Word. 37 (4), 6970. Morton, J., 1987. Wood-Apple. Fruits of Warm Climates. Julia F. Morton, Miami, FL, pp. 190191. Muthumperumal, C., Parthasarathy, N., 2009. Angiosperms, climbing plants in tropical forests of Southern Eastern Ghats, Tamil Nadu, India. Check List 5 (1), 92111. Patel, H.B., 2013. Master of technology. Production technology of wood apple (Feronia limonia) juice. College of Food Processing Technology & Bioenergy Anand Agricultural University, Anand 388 110 (July), p. 95. Pradhan, D., Tripathy, G., Patanaik, S., 2012. Anticancer activity of Limonia acidissima Linn (Rutaceae) fruit extracts on human breast cancer cell lines. Trop. J. Pharm. Res. 11 (June), 413419. Qureshi, A.A., Kumar, K.E., Omer, S., 2010. Feronia limonia-A path less travelled. Int. J. Res. Ayurveda Pharm. 1 (1), 98106. Vidhya, R., Narain, A., 2011. Formulation and evaluation of preserved products utilizing under exploited fruit, wood apple (Limonia acidissima). American-Eurasian J. Agric. Environ. Sci. 10 (1), 112118. Vijayvargia, P., Vijayvergia, R., 2014. A review on Limonia acidissima L.: multipotential medicinal plant. Int. J. Pharm. Sci. Rev. Res. 28 (1), 191195. Vilpulasena, S.M.P.M., Abeynayake, N.R., Kadupitya, H.K., 2010. Evaluation of potentials and constraints for wood apple (Limonia acidissima L.) cultivation in Sri Lanka using spatio-temporal data. In: Proceedings of 10th Agricultural Research Symposium (2010), 363367.
Author Index Note: Page numbers followed by “f ” and “t” refer to figures and tables, respectively.
A Abbasi, N.A., 286 Abdul Karim, F., 416t, 417t Abe, L.T., 219, 240 Abeywickrama, W.S.S., 330 Abliz, A., 366 Abreu, F.P., 87 Abreu, P.A. de A., 81 Abu Bakar, M.F., 415417, 416t, 417t Acevedo, P.I.C., 148 Achmad, S.A., 124 Acosta, M.A., 319 Adati, R.T., 94 Adebajo, A.C., 440 Adeniran, A.H., 58 Adeniran, H.A., 58 Adriano, E., 11 Ago´cs, A., 275 Agudelo, C., 157 Aguiar, J.C., 261 Aguiar, J.P., 102103 Aguiar, J.P.L., 155t Aguiar, L.P., 49, 51 Aguiar, T.M., 219, 220t Aguiar Filho, S.P., 305, 308 Ahmad, D., 357358 Ahmad, M.A., 373 Ahmad, S., 165 Aimi, M.N.N., 177 Airy Shaw, H.K., 1516 Ajifolokun, O.M., 58 Akachi, T., 99102, 101t Akagi, T., 115 Akbulut, M., 288 Akowuah, G.A., 282t Alam, M.K., 404, 406, 408409 Alberton, J.R., 251252 Albuquerque, C.L.C., 24, 26, 28 Albuquerque, M.B., 307 Albuquerque, U.P., 32, 141 Alcaraz, M.L., 37, 44 Al-daihan, S., 374 Alesiani, D., 365366 Alexandre, R.S., 69, 72, 73t Alezandro, M.R., 240, 242 Algarra, A.M., 252 Ali, A., 345 Alia-Tejacal, I., 142143 Alice, C.B., 335, 337 Allegra, M., 193t
Al-Maiman, S.A., 357358 Almeida, A.da.S., 429, 430t Almeida, C.B., 309 Almeida, J.I.L., 8 Almeida, M.M.B., 145, 308309, 311t Almeida, M.M.de., 430t Almeida, S.P., 77, 8081, 297, 309 Almeyda, N., 107108, 110111 Al-Mughrabi, M.A., 359 Alrozi, R., 373 Al-Said, F.A., 355356, 360 Al-snafi, A.E., 363 Alvarado, M.D., 197t, 198 Alvarenga, A.A., 363, 366 ´ lvarez, C., 7273 A Alves, A.P.C., 242 Alves, A.R., 159 Alves, E., 9t Alves, J.A., 297 Alves, R., 99, 102 Alves, R.E., 9, 393t, 394395 Aman, R., 383, 385 Amarante, C.V.T., 34 Ambarawati, I.G.A.A., 388389 Amin, I., 109t Amornputti, S., 171, 176 Amoro´s, A., 287, 289 An˜abesa, M.S., 173, 176 Ancos, B., 116 Andersen, O., 437 Andersen, V.U., 437 Andrade, A.C.S., 80 Andrade, B.A.G., 91 Andrade, E.H.A., 155t Andrade, J.L., 341 Andrade, J.S., 103 Andrade, R.A.M.S., 430t, 431 Andrade, R.N.B., 437 Andrade, S., 1718, 400401 Anegbeh, P.O., 377, 380 Angelo, P.C.S., 232, 235 Aningsih, S., 282t Anjos, F.C., 9t Anon., 208 Anselmo, G.C.S., 299 Anthony, M., 203 Antoniolli, L.R., 116 Anugweje, K.C., 322 Apak, R., 173174 Apel, M.A., 220t
Aquino, E.N., 191, 193, 194t Arabbi, P.R., 300 Arai, I., 337 Aralas, S., 383, 385388 Arancibia-Avila, P., 173174 Arau´jo, F.M.M.C., 241 Arau´jo, P.G.L., 8 Arayne, M.S., 253254 Arenas, E., 194195 Arendse, E., 357358 Argout, X., 69 Ariffin, A.A., 345 Arnal, L., 117 Arola, F.M., 308t Arpaia, M.L., 274 Arrazola, G., 10, 12t Arrizon, J., 197t, 198 Arshadi, M., 149 Arte´s, F., 196, 359360 Artik, N., 116 Arumughan, C., 251252 Ascheri, D.P.R., 240 Ashrafi, H., 366 Ashton, O.B.O., 40 Asiedu, J.J., 172 Askar, A., 190192 Aslan, S., 366 Asquieri, E.R., 33t, 242 Assis, S.A., 10 Assumpc¸a˜o, C.F., 81, 309311 Assunc¸a˜o, R.B., 87 Atapattu, N.S.B.M., 108109, 111 Atkinson, E., 181184 Atkinson, M.D., 181184 Atroch, A.L., 228229, 233 Atta-Aly, M.A., 170 Augusta, I.M., 245, 247t Augusto, F., 145 Augusto, P.E.D., 149 Augusto, S.C., 7 Aurore, G., 53 Avello, M., 131f, 133135 Avilan, L., 144, 149 Aviram, M., 358 Avitia, G.E., 141143 Ayala-Zavala, J.F., 4446, 103 Ayuk, E.T., 377, 380 Ayyanar, M., 251254, 252t Azad, M.S., 405, 409 Azeveˆdo, J.C., 99102, 101t Azmi, S.M.N., 388
447
448
Author Index
B Baars, E., 366 Babosa, W., 286 Bacelar, C.G., 422 Backer, C., 15 Badrie, N., 20, 57, 391395 Bae, D., 290 Bagetti, M., 336 Bakhuisen, Van den Brink, R.C., 15 Balaois-Morales, R., 344 Baldry, J., 174175 Baliane, A., 23 Baliga, M.S., 251254 Balisteiro, D.M., 34 Baljinder, S., 289 Balois-Morales, R., 344 Baltacioglu, H., 116 Bamroongrugsa, N., 121 Bandoni, A.L., 335 Banerjee, A., 254 Bapat, V.A., 166 Baquedano, F.J., 307 Bar, E., 295t Baraona, M., 143, 149 Barbeau, G., 141142 Barbedo, C.J., 437 Barbera, G., 187191 Barbosa, N., 220t Barcelos, G.R.M., 2628 Barcus, D.E., 85 Bardales, X.I., 9899 Barh, D., 253254 Barney, D.L., 211 Barreca, D., 272273, 275276 Barreto, G.P.M., 287, 288t Barros, R.S., 237241 Bartoo, A., 20 Basanta, A., 246 Basar, S., 323 Baskaran, R., 394 Bataglion, G.A., 6365 Batalha, P.G., 69 Batista, P.F., 10, 12t Bauer, R., 339 Bauer, T., 15, 1718 Bayer, R.J., 204 Beckett, J.R., 69, 72 Beckett, S.T., 72 Beinsan, C., 364, 366 Ben-Arie, R., 117 Benedetti, Sde F., 81 Benherlal, P.S., 251252 Benjamin, T.J., 142 Benkebia, N., 288t Benkeblia, N., 1718 Ben-Yehoshua, S., 273274 Benzarti, S., 365 Bernhard, R.A., 275 Berry, A.D., 8788 Bertoldi, F.C., 220t, 222f, 222t Betaglion, G.A., 12 Bettiol Neto, J.E., 286, 363364 Bezerra, J.E.F., 3132 Bhanuprakash, V., 253254
Bhat, R., 173 Bhat, R.S., 374 Bhattacharya, A., 398 Bhattacharya, P.K., 409 Biale, J.B., 85, 272273 Bianchini, F.G., 93 Bibitha, B., 408 Bicas, J.L., 352353 Biegelmeyer, R., 31 Birmingham, E., 209 Blankenship, S., 176 Bodmer, R.E., 61 Bo¨hm, F., 423 Boleti, A.P.A., 33t Bongiorno, A., 193t Boni, A., 309 Booncherm, P., 170171, 173, 175176 Boonlaksiri, C., 124 Boonphong, S., 125 Borchert, R., 143 Bore´m, A., 234 Borges, M.H.C.B., 242 Borges, S.V., 432 Borgese, R., 360 Borkowska, J., 215 Bosco, J., 308 Boshier D.H., 141142, 144 Bouvier, F., 26 Bower, J.P., 3940, 4344 Branda˜o, G.C., 309 Brasileiro, B.G., 286 Brat, P., 321t Brennan, R., 215 Brennan, R.M., 211 Brillouet, J.M., 321t Brito, E.S., 9t, 87, 253, 320f Brito, M.A., 7781 Brod, F.P.R., 300 Brown, B., 330 Brown, B.I., 282 Browne, J., 20 Bruginski, E.R.D., 33t Brunini, M.A., 241242 Budiasa, I.W., 388389 Budihardjo, I., 424 Bueno, L.C., 233234 Bujang, A.S., 177 Bullock, S.H., 143 Burkill, I.H., 125 Burton, W.G., 172 Bustamante, F., 103 Butera, D., 193194, 193t Buttara, M., 123
C Caballero, P., 285 Ca´ceres Paredes, J.R., 157 Cai, C., 289 Calbo, M.E.R., 307 Caleb, O.J., 359 Calzavara, B.B.G., 4950 Camilo, Y.M.V., 7779 Campbell, C.W., 1516, 20
Campos, C.de.O., 429, 430t Campos, F.R., 33t Campos, J.T., 286, 289 Campos, O.C., 428t Campos, R.E., 149 Canche-Canche, E., 343344 Caˆndido, T.L.N., 6364 Cantu-Jungles, T.M., 63 Cantwell, M., 188191, 196 Canuto, G.A.B., 50, 50t, 322t Cao, S., 287, 289 Cao, S.F., 289 Caod, S., 288t Caprile, L., 133 Ca´rdenas, L.D., 141 Ca´rdenas-Coronel, W.G., 322 Cardon, D., 319 Cardona, J.E., 153, 156 Cardoso, L.D.M., 77 Cardoso, L.M., 32, 33t, 310t, 311t Cardozo, M.S., 87 Carle, R., 187, 194, 194t Carneiro, J. de O., 80 Carneiro, J.O., 364 Carnelossi, M.A.G., 306, 308, 310t Carr, M.K.V., 37 Carrera, L., 63, 66 Carrillo-Salazar, J.A., 339, 341, 345 Carrington, C.M.S., 89 Carvalho, A.V., 45 Carvalho, C.M., 242 Carvalho, D.A., 297 Carvalho, G.G.P., 72 Carvalho, J.D., 49 Carvalho, J.M., 88 Carvalho, M., 366 Carvalho-Silva, L.B., 50 Castillo, F.J., 307 Castillo-Martinez, R., 340 Castro, J.C., 99 Castro, L., 423 Castro, P.R.C., 7 Cavalcante, M.L., 336 Cavalcante, P.B., 1, 49, 257, 259, 419420 Cavalcanti, N.de.B., 429 Cavaletto, C.G., 57 Ceballos, A.M., 299 Cecı´lio, A.B., 258 Centurio´n-Yah, A.R., 341, 343344 Cereda, M.P., 300 Cerezal, P., 197t Cernusca, M., 181183 Cerqueira, M.A., 145147 Ceva-Antunes, P.M.N., 145, 147t, 148t Ceylan-Isik, A.F., 289 Chagas, E.A., 288t Chaiprasart, P., 171 Chakraverty, R., 398 Chalutz, E., 273 Chan, E.S., 379t Chan-Blanco, Y., 321, 321t Chandra, J., 424 Chang, Y.K., 260 Chansiripornchai, N., 174
Author Index
Chansiripornchai, P., 174 Chao-ming, L., 164, 164t Chareoansiri, R., 385, 386t Charoensiri, R., 173174, 300 Chaturvedi, A., 253254 Chaturvedi, A.N., 405, 408 Chavan, M.J., 164t, 165 Chavan, N.S., 329 Chavarrı´a, Y., 194t Chaves, F.C., 32f Chaves, J.M., 420 Chaves, L.J., 78 Cha´vez, J.L., 194t Chemah, T.C., 343, 345 Chen, F.X., 287 Chen, H., 37 Chen, J., 287, 289 Chen, L., 329 Chen, M.H., 275276 Cheng, G., 266 Chepote, R.E., 72 Chew, L.Y., 109t Cheyglinted, S., 175176 Chim, J.F., 1112 Chingsuwanrote, P., 173174 Chinweuba, D.C., 58 Chirinos, R., 99 Chitarra, A.B., 8, 10, 34, 116, 286 Chitarra, A.D., 307 Chitarra, M.I.F., 8, 10, 34, 116, 286, 307 Cho, J.Y., 275 Choi, H.S., 272, 275276 Chokeprasert, P., 439, 441 Chong, C.H., 123 Choquenet, B., 423 Chou, S.K., 299 Chua, K.J., 299 Chunhieng, M.T., 322 Cisneros, A., 339340 Citadin, I., 242 Clarke, K., 203, 205 Clement, C.R., 297 Clerici, M.T.P.S., 50, 305, 311t Coelho, M.I.S., 432 Coelho de Souza, G., 3132 Cohen, H., 339340 Cohen, K.O., 160, 310t Coletti, L.Y., 239 Colla, A.R.S., 222 Consolini, A.E., 335, 337 Conti, A., 7273 Contreras-Gutie´rrez, P.K., 40 Coomes, O.T., 66 Corbelini, D.D., 34t Corbo, M.R., 196 Cordeiro, G.D., 92 Cordeiro, I., 220t Cordeiro, L.C.M., 63 Cordeiro, M.C.R., 393t Cordero, J., 141142, 144 Coria-Avalos, V.M., 4243 Coria-Te´llez, A.V., 391392 Coronel, R., 415 Coronel, R.E., 123, 388, 405, 408
Corrales, J., 197 Corrales-Garcı´a, J., 195196, 343344 Correˆa, L.C., 31 Correˆa, M.O.G., 239240 Costa, A.G.V., 5 Costa, D.S.A., 109 Costa, F.R., 431 Costa, J.P., 300 Costa, J.R., 422 Costa, M.G.C., 23, 28 Costa, M.P., 161 Costa, N.Pda, 429, 430t Costa, T.S.A., 116 Cowan, A.K., 3940 Crane, J.H., 42 Crisosto, C.H., 117, 357358 Crowell, P.L., 275 Crozier, A., 221 Cruz, A.F., 2324 Cruz, C.L.C.V., 72 Cruz, E.D., 258 Ctenas, M.L.B., 333 Cuevas, J.A., 142143 Cunha, A.G., 87 Curi, P.N., 289 Cutting, J.G., 3940, 4344 Cymerys, M., 1, 35
D da, Silva, A.C.M.S., 309, 310t Da Silva, A.M., 320, 322 da Silva, F.C., 99102, 101t da Silva, M.A., 102 Da Silva, R, 254 da Silva, W.P., 32f Dabas, D., 4446 Daengkanit, T., 170171, 174 Dahlen, M., 121122 Dahot, M.U., 253t Daiuto, E´.R., 240241 Daley, O.O., 57 Daly, D.C., 16, 377 Damasceno, L.F., 8687 Damiani, C., 32, 33t, 35 Danadio, L.C., 251 Dantas Ju´nior, O.R., 430t, 431 Das, D.K., 404, 406, 408409 Das, H., 299 Dash, G.K., 164t Daulmerie, S., 15, 1718, 20 Davenport, A.J., 4041 De Almeida Cardoso, E., 351, 353 De Andrade, L.A., 258 De Andrade, S.R.M., 393t De Bruim, D., 366 De la Barrera, E., 341 De Lanerolle, M., 107109, 110t De Laroussilhe, F., 1516 De Melo, M.G.G., 257258 de Mendonc¸a, M.S., 61 de Oliveira Martins, D.M., 352t De Paula, L.A., 366 De Rosso, V., 420, 421t, 423
449
De Souza, A., 257258, 260 De Souza, C.R., 259260 de Souza, M.P., 352353 Deaquiz, Y.A., 344 Defilippi, B.G., 42, 359 Defilippi, E., 98 Del Bubba, M., 116 Del Rio, D., 221 Delgado, L.F., 437 Delort, E., 206, 271 Delucchi, G., 285 Delva, L., 10 Dembitsky, V.M., 1112, 342, 373, 383, 385 Denardin, C.C., 335336 Deng, G., 387 Deng, S., 322 Deshmukh, S.R., 33 Desjardins, R.E., 124 Dessimoni-Pinto, N.A.V., 242 Devalaraja, S., 4041 Devi, S., 265 De-Villiers, E.E., 273274 Di Gaudio, F., 193t Dias, L.S., 260 Dı´az, M., 351 Dib, C.M., 102 Ding, C., 196 Ding, C.K., 286 Ding, H., 4041 Ding, Z., 287, 289 Dishon, E., 295t Di-Stasi, L.C., 437 Dittmar, A., 319 Dixon, A.R., 319 Dixon, R.A., 115 do Amaral, F., 102103 Dole, J.M., 176 Domingues, A.F.N., 4 Domı´nguez-Lo´pez, A., 193t Donadio, L.C., 9192, 333 Dongre, R.S., 392393 ´ lvarez, L., 4344 Dorantes-A dos Santos, M.A.Z., 4446 Doughari, J.H., 406 Dreher, M.L., 4041 Drehmer, A.M.F., 34 Dresch, D.M., 3132 Du, Y.Q., 439440 Duarte, A.R., 77 Duarte, G., 197t Duarte, O., 37, 40, 43, 153157, 237238, 241 Duarte, W.F., 161 Dubery, I.A., 273274 Ducke, A., 226227 Dufour, J.P., 99 Duncan, E.J., 53 Duru, B., 190 Dury, S., 20 Dzondo-Gadet, M., 380
E Edagi, F.K., 116, 286, 289 Ee, G.C.L., 417
450
Author Index
Efraim, P., 7273, 74t Eik, N.M., 298 Eiznhamer, D., 266 Elevitch, C., 54, 5758 Elevitch, C.R., 54, 320 Elkins, R., 323 El-Samahy, S.K., 190192, 197, 197t, 199 Elsayed, A.M., 107109 El-Siddig, K., 406407, 407t, 409 Elwers, S., 72 Emanuel, M.A., 1718 Eme, P.E., 393t Endress, B.A., 61 Engels, C., 145 Ergun, M., 358 Erkan, M., 355359 Erre, P., 190 Escalona-Arranz, J.C., 406 Escamilla, S.H.M., 189t Escriche, I., 63 Espı´ndola, M.C.B., 149 Esquivel, P., 343344, 346 Esteve, C., 40 et Faure, J.-J., 1517 et Le Berre, S., 15 Everham, E.M., 380 Ewaidah, E.H., 198 Ewald, C., 302 Ezura, H., 40, 43
F Fa’Anunu, H.‘O., 17 Faber, M.A., 161 Fabra, M.J., 299 Facciola, S., 272 Fachinello, J.C., 3132, 364 Fachmann, W., 365t Fan, Q.J., 341 Faria, A.F., 288t Faria, W.C.S., 322, 322t Faria Junior, J.E.Q., 77 Farine, J.P., 323 Fattouch, S., 366 Fa´varo, D.I.T., 155t Favier, J.-C., 15, 18, 20 Fellows, P.J., 72, 300 Ferguson, L., 355 Fernandes, F.A., 123 Ferna´ndez, M.A., 285 Ferrari, A.S., 93 Ferrari, C.C., 299300 Ferreira, A.G., 437 Ferreira, C.A.C., 257259 Ferreira, E.G., 311t Ferreira, F.R., 49, 51, 393t Ferreira, J.C., 431432 Ferreira, M., 9t Ferreira, M.E., 232 Ferreira, M.P.L.V.O., 366 Ferreres, F., 288 Ferrucci, M.S., 229 Fetter, M.R., 3233, 33t, 34t Feungchan, S., 405407, 407t
Figueiredo, B.C., 28 Figueiredo, R.W., 85 Figueiredo Neto, A., 9t, 11 Filgueiras, H.A., 393t Filgueiras, H.A.C., 9, 8587 Finn, C.E., 181 Fioravanc¸o, J.C., 364 Fitri, A., 387 Fletcher, H.M., 322 Flores, A., 198 Flores, C.A., 197 Flores, G., 219 Flores, P., 215 Folegatti, M.I.S., 431432 Fonseca, E.T., 50 Fontan, G.C.R., 432 Fonteles, T.V., 88 Foo, K.Y., 177 Foo, L.Y., 213214 Forman, L.L., 1516 Fownes, J.H., 55 Fox, F.W., 293 Fracassetti, D., 101t, 102, 219 Fraga, S.R.G., 18 Franco, C.F.O., 24 Franco, C.M.L., 300 Franco, E.M., 109 Franco, M.R.B., 160 Franquin, S., 1718 Franz, L.W., 416t Franzon, R.C., 333334 Frazon, R.C., 3132 Freeman, B.A., 423 Freitas, C.A.S., 11, 12t Freitas, D.V., 225226, 229, 231 Freitas, S.T., 344 Frenedoso da Silva, R., 157 Fry, J., 416t, 417t Fry, S.C., 240 Fu, L., 20 Fuenzalida, C., 129, 132t Fujita, A., 101t, 102
G Gabrielsen, M., 125 Gajalakshmi, S., 391, 400 Galang, F.G., 415 Galdino, P.O., 432 Galho, A.S., 32, 34 Galindo-Cuspinera, V., 2728 Gallegos-Va´zquez, C., 188190, 189t Galva˜o, MdeS., 431 Gama, L., 141 Gao, H.Y., 289 Garcia, C.G., 252t Garcia, L.G.C., 242 Garcı´a, O., 148 Garcia-Cruz, E.E., 346 Garruti, D.S., 87, 320f Gattuso, G., 275276 Geissler, C., 271 Genovese, M.I., 159160 Ge˝ocze, K.C., 352353
George, C., 58 Geurts, F., 16 Ghosh, S.N., 445t Giesen, W., 327 Gil, M.I., 358 Gilani, A.H., 320 Giridhar, P., 28 Giriwono, P.E., 2628 Giuliano, G., 27f, 28 Giusti, M.M., 253 Glozer, K., 355 Glucina, P.G., 113114 Gohil, D.I., 408 Golukcu, M., 40 Gomes, E.D.B., 309311 Gomes, P.M.A., 300 Gomes, S., 129 Gomes, W.F., 305 Gonc¸alves, A.E.S.S., 32, 93, 420 Gonc¸alves, E., 9t Gondim, C.J.E., 227228 Gondim, P.J., 430t, 431 Gondim, T.M.S., 159161 Gong, R.G., 285 Gonza´les, L., 9899, 102 Gonza´lez, R., 196197 Gonzalez, T.N., 34t Gonzalez Vega, R., 157 Gonzalez-Barrio, R., 220221 Gonza´lez-Garcı´a, A., 141142 Gorinstein, S., 116, 173, 383, 388 Graham, C., 203 Graham, J., 215 Graham, O.S., 1718, 20 Grant, W.C., 4041 Grassi, A.M., 285 Grattapaglia, D., 232, 234 Green, C.L., 2425 Griffis Jr., J.L., 336 Griffith, M.P., 187188 Gross, J., 40 Grover, J.K., 251, 252t, 253254 ´ , 1718 Guadarrama, A Guarim Neto, G., 352353 Guerra, M., 229 Guerrero, R., 142143 Guerrero-Beltra´n, J.A., 145147, 191, 193, 195199 Guilherme, A.A., 88 Guilloteau, M., 72 Gulrajani, M.L., 28 Gunasena, H.P.M., 339, 408 Gu¨ney, M., 275 Guo, L.W., 345 Gurgel-Gonc¸alves, R., 61 Gusma˜o, E., 353 Gutierrez, D., 99102, 101t Gutie´rrez, G.O., 148149 Guzma´n, R.I., 194t
H Haas, L.I.R., 32f Hakim, E.H., 124
Author Index
Halbe, A.V., 409 Halliwell, B., 423 Hamacek, F.R., 32, 33t Hamada, A., 290 Hamburger, M., 323 Hameed, B.H., 177 Hamilton, K.N., 203, 205 Haminiuk, C.W.I., 3132, 242, 436 Han, B.H., 265 Hannes, H., 321 Hardenburg, R.E., 116 Hardy, S., 204, 208209 Harivaindaran, K.V., 346 Harrington, M.G., 226, 229 Hart, D., 203 Hartmann, H.T., 285286 Haruenkit, R., 173, 385, 386t, 387, 387t Hasegawa, P.N., 286287, 288t, 289 Hashim, O.H., 124 Hassan, B.H., 198 Hassimotto, N.M.A.J., 220t, 222f, 222t Havinga, R.M., 408 He, Z.G., 288289 Heinrich, M., 4 Henderson, A., 1, 298 Herbach, K.M., 194t Herbach, K.M.C., 346 Hernandez, C., 109 Herna´ndez-Silva, J., 196 Hevia, F., 132t Heyne, K., 125 Hiane, P.A., 300 Hiruma-Lima, C.A., 437 Hiwale, S., 164, 166, 406407 Hiwasa-Tanase, K., 40, 43 Ho, L.-H., 173 Hoa, T.T., 345 Hoffmann, A., 129130 Hofman, P.J., 4344 Holland, D., 355356 Homma, A., 49, 51 Homma, A.K.O., 159 Hopkins, A.L., 142 Hopp, D.C., 164 Hormaza, J.I., 37, 44 Hou, D., 16 Howlader, M.S.I., 327 Hoyos, J., 141, 143 Huang, D., 282t Huang, G., 271 Huang, W.Y., 283 Huang, Y., 289 Huber, L.S., 300301 Hue, C., 72 Hughes, A., 408 Hulme, A.C., 213214 Hummer, K.E., 211 Hurtado-Ferna´ndez, E., 40
I Iacomini, M., 20 Ibeanu, V.N., 393t Ibrahim, N.A., 406
Ihsanullah, I., 345 Iloki-Assanga, S.B., 322 Ima´n, S., 9798, 102 Imeh, U., 365 Imsabai, W., 171 Inada, K.O.P., 242 Inglese, P., 187 ´ ., 103 Inocente-Camones, M.A Inoue, T., 99102, 101t Ioanonne, F., 72 Irtwange, S.V., 85 Isabelle, M., 173174, 280, 282t Ishak, S.A., 18 Itoo, S., 115 Ittah, Y., 116
J Jackix, M.N.H., 160 Jacques, A.C., 336 Jadhav, V.W., 251252 Jagtap, U.B., 166 Jain, R., 406 Jaliliantabar, F., 272 Janick, B.J., 288t Jansen, P.C.M., 123, 383385, 388 Jansz, E.R., 110t Janzen, D.H., 142143 Jaquier, A., 206 Jariyah, Widjanarko, S.B., 327, 329330 Jaswir, I., 174175 Jaya, S., 299 Jayaprakasam, B., 260 Jayaprakasha, G., 275276 Jayaraman, S.K., 323 Jayasooriya, M.C.N., 330 Jayaweera, D.M.A., 408 Jelani, A., 123 Jensen, M., 121, 125 Jesus, N., 239, 241 Jiang, Q., 424 Jiang, Y.L., 339 Jirovetz, L., 15, 18, 20, 380 Jondiko, I.J.O., 26 Jones, A.M.P., 5455, 5859 Jordheim, M., 215 Jorge, N., 77, 81 Jossang, A., 265 Junardy, F.D., 282t
K Kader, A.A., 355, 357359, 366 Kahn, F., 419 Kaitho, R.J., 409 Kalenda, D.T., 380381 Kaneshima, T., 99102, 101t Kang, E.J., 2728 Kanlayavattanakul, M., 387, 389 Kapseu, C., 380381 Kar, A., 165 Karwowski, M., 437 Kasiolarn, H., 172 Kassim, A., 40, 4244, 272, 274
Katan, M.B., 275 Katerson, A., 20 Kathiresan, K., 330 Kaushik, R.A., 165t, 393t Kawabata, A.M., 370 Kawail, S., 275 Kawasaki, M.L., 92, 9798, 435 Kee, M.E., 282t Keenan, B.M., 215 Keep, E., 211 Kelechi, M., 393t Keller, H., 285 Kempler, G.M., 316 Kenmegne Kandem, A.T., 380 Ketsa, S., 169177 Khaimov, A., 339 Khaimov-Armoza, A., 339 Khan, K., 20 Khan, M.S., 404 Khan, S.A., 345 Khanzada, S.K., 406 Khoja, A.K., 409 Khokhar, S., 365 Khonkarn, R., 373 Khoo, H.E., 109t, 174, 282t Khurnpoon, L., 173, 175 Kiesling, R., 187 Kikuchi, T., 290 Kim, D.S.H.L., 266 Kim, J., 346 Kim, M., 289290 Kim, S.H., 290 King, R.A.G., 89 Kinghorn, A.D., 319 Kissmann, C., 3132 Kitagawa, H., 113114 Kluge, R.A., 7, 116 Knouft, J.H., 141 Ko, H.H., 125 Koblitz, M.G.B., 74t Koh, W.P., 282t Konczak, I., 203, 207t, 208 Kondo, S., 274, 372 Kong, J.M., 253 Kong, K.W., 108109, 109t Kongkachuichai, R., 174, 385, 386t Kongor, J.E., 69 Koolen, H.H.F., 6466 Kosiyachinda, S., 170 Koubala, B.B., 18, 20 Kovendan, K., 324 Kovendana, K., 324 Koyasako, A., 275 Kozioł, M.J., 146t, 147t, 148t Kozlowski, T.T., 307 Kraut, H., 365t Krishnaiah, D., 322 Krolow, A.C.R., 242 Kugler, F., 343 Kumamoto, H., 276 Kumar, R., 330 Kumar, V., 440 Kundu, A.D., 266 Kupper, W., 359
451
452
Author Index
Kurihara, Y., 265 Kuskoski, E.M., 300, 336 Kwang, J.J., 275
L Lacerda, D.B.C.L., 352t Ladaniya, M.S., 271273 Ladipo, D.O., 380381 Lage, F.F., 242 Lage, M.E., 33t Lagefoged, T., 55 Laghari, A.H., 423 Lago, E.S., 254 Lago-Vanzela, E.S., 19t Lagunes Ga´lvez, S., 72 Lai, F.Y., 247 Lajolo, F.M., 220t, 222f, 222t, 288t Lakshmi, Y., 443 Laloraya, M.M., 406 Lam, P.F., 172 Lancaster, F.E., 28 Lande, S.B., 446 Landrigan, M., 373 Landrum, L., 130f Landrum, L.R., 9798, 435 Lannes, S.C.S., 159, 161 Latchoumia, J.N., 55 Latiff, A., 327, 330 Lawrence, J.F., 28 Le Bellec, F., 339 Leakey, C.L.A., 53 Leakey, R.R.B., 377, 380381 Lederman, I.E., 305306, 336 Lee, B.L., 282t Lee, J., 181, 423 Lee, M.H., 290, 337 Lee, P.R., 123 Lee, S., 266 Lee, S.K., 3940, 4243 Lee, S.-P., 198 Leenhouts, P.W., 380 Leite, P.B., 69 Leonel, M., 364, 365t Leonel, S., 365t Leong, C.M., 123 Leong, L.P., 371372 Leontowicz, H., 173174 Leontowicz, M., 173174 Lestari, R., 384385 Lestari, R.A.S., 389 Lestari, S.R., 374 Leterme, P., 18 Leung, W.T.W., 20 Levitt, J., 92 Lewicki, P.P., 300 Lewinsohn, E., 295t Lewis-Luja´n, L.M., 322, 322t Li, B.W., 87 Li, J.-X., 175 Li, L., 344 Li, W.S., 440 Liaotrakoon, W., 345 Liaw, C.C., 163, 165
Lim, H.K., 343, 345 Lim, L.B.L., 418 Lim, M.T., 282t Lim, S.B., 124 Lim, T.K., 97, 107111, 121, 123125, 153154, 156, 275, 339, 345, 383385, 403 Lim, Y.Y., 280 Lima, A.J.B., 240241 Lima, D.U., 409 Lima, E.C., 423 Lima, E.S., 33t Lima, I.C.G.S., 144 Lima, J.P., 305 Lima, J.P.L., 305, 309311, 312t, 316 Lima, L.C.O., 285 Lima, M.A.A., 149 Lima, M.A.C.D., 394395 Lima, M.A.Cde, 429, 430t Lima, M.E.L., 221t Lima, P.C.C., 1011, 12t Lima, R.S.de., 427 Lima, V.L.A.G., 336 Lima Filho, P.J.M., 149 Limmatvapirat, C., 330t Lin, C.C., 276 Lin, J.H., 440 Lin, S., 285 Lincoln, N., 55 Linda, B.L.L., 416t Linnaei, C., 187 Liogier, H.A., 398399 Lira Junior, J.S., 333334 Liu, Y., 55, 56t, 57t, 290 Lizada, M.C.C., 282 Ljubo, J., 184t Lleras, E., 226 Lognay, G., 63 Loison, S., 295t Lopes, A.S., 7273, 337 Lopes, J.C., 259260 Lopes, M.F., 429, 430t, 431 Lopes, M.M.A., 85 Lopes, M.T.G., 422 Lo´pez, J.J., 197t, 198 Lopez-Rubira, V., 360 Lorenzi, G.M.A.C., 297298 Lorenzi, H., 51, 91, 219, 222, 237238, 242, 333, 435 Lota, M.-L., 206 Lou, S.N., 271, 274275 Loureiro, G.A.H.A., 72, 73t Love, K., 391393 Lowe, G.M., 423424 Lozano, A., 142 Lu, H., 366 Luberck, W., 321 Lucas, M.P., 59 Lues, J.F.R., 215 Luna, F., 72 Luo, H., 346 Lutchmedial, M., 394 Lu¨ttge, U., 191 Lutz, M., 93 Luz, D.A., 8687
Lv, L., 323 Lv, X., 275276 Lye, T.T., 371 Lysiak-Szydlowska, W., 174
M Ma, J., 109 Mabberley, D.J., 203204, 209 Maˆcedo, A.S.L., 72 Macedo, J.R., 307 Macedo, S.H.M., 155t Machado, C.A.C., 297 Machado, J.W.B., 307 Machado, N.C., 241 Machado, S.S., 431432 Macı´a, M.J., 146t, 147t, 148t Maciel, M.I.S., 11 Maeda, R.N., 103 Magalha˜es, A.S., 365 Magalha˜es, M.M., 238241 Magness, J.R., 181182 Mahanthesh, M.C., 322 Maharaj, R., 58 Mahendra, M.S., 383 Mahmoud, I.I., 251 Maia, G.A., 309 Maia, J.A.G., 155t Majhenic, L., 351 Majumdar, G.P., 263 Majumdar, S.K., 408 Makinen, K.K., 213214 Malaysia, D., 385 Maldonado, M.F., 141 Maldonado-Astudillo, Y.I., 145, 146t Mamede, R.V.S., 9t Manach, C., 109 Maneerat, W., 440 Manica, I., 7, 31, 49 Manica-Berto, R., 363, 364f Maninang, J.S., 171, 173, 175176 Manzi, M., 66 Marchiori, J.N.C., 237, 435 Maria Netto, F., 260 Mariath, J.G.R., 63 Marin, R., 337 Marinho, S.J.O., 311t Marino Neto, L., 7 Markle, G.M., 181182 Martin, F.W., 107108, 110111, 245 Martine, F., 20 Martı´nez, M., 148149 Martı´nez-Calvo, J., 113 Martı´nez-Habibe, M.C., 377 Martinotto, C., 77, 7981 Martins, F.P., 113 Martins, W., 232 Martorell, L.F., 398399 Marx, F., 99, 102, 153, 155t, 156157 Marzolo, G., 357t Mascarenhas, A., 409410 Massini, R., 360 Mathur, N.K., 408409 Mathur, P.B., 282
Author Index
Mathur, V., 408409 Maticorena, C., 129 Matsuda, H., 265 Matsuo, T., 115 Matsushima, J., 115 Matta, M., 73t Matta, V.M., 242 Mattos, G.D., 436 Mattos, J.R., 31, 237238, 435 Matuda, T.G., 260 Matuo, M.C.S., 2628 Mayorga, M.C., 189t Mazza, G., 253 Mbofung, C.M.F., 377378, 380381 McKay, S., 217 McKee, G.W., 181 Medeiros, M.C., 65 Medeiros de Aguiar, T., 11 Medel, F., 129 Medina, A., 9798 Medina, A.L., 32, 32f, 34 Medina, G., 420, 422 Medina Rivas, M.A., 157 Medrano, H., 307 Meghwal, P.R., 409 Meher, B., 409 Mehrotra, S., 423 Meireles, M.A.A., 24, 26, 28 Mele´ndez-Ma´rtinez, A.J., 365366 Melgarejo, P., 358 Melo, A.A.M., 285 Melo, B., 242 Melo, E.A., 430t, 431 Melo, W.S., 66 Melo Neto, B.A., 4 Mena, P., 358 Mendes, A.C.R., 432 Mendes, A.M.S., 257258 Me´ndez-Toribio, M., 141142 Mendis, A.P.S., 108 Mendonc¸a, R.C., 77 Mendoza Jr., D.B., 85 Menezes, A.G.T., 72 Menezes, A.J.E.A., 49 Menezes-Cordeiro, M.H., 342 Mercadante, A., 420, 421t, 423 Mercadante, A.Z., 26, 33t, 87, 99102, 101t, 220t, 223t, 288t Meyer, M.D., 3940 Mezadri, T., 11, 12t Mialoundama, F., 377 Michodjehoun-Mestres, L., 87 Miguel, A.C.A., 436 Miguel, G., 358 Milanez, J.T., 62 Miles, D.H., 330 Milla´n, B., 419420 Miller, A.J., 141 Minaiyan, M., 366 Miniati, E., 253 Mir, S.A., 363 Miranda, I.P.A., 298 Miranda, M.R.A., 9t Miranda-Cruz, E., 149
Miranda-Vilela, A.L., 32 Mischan, M.M., 365t Mishra, S., 329t Mitcham, E.J., 344 Mitchell, J.D., 16 Mitsuoka, T., 32 Mizrahi, Y., 293, 295, 339341, 344 Mochiutti, S., 12 Moerman, D.E., 181 Moghadamtousi, S.Z., 391, 398 Mohamed, K., 176 Mohamed, M., 416t, 417t Mohamed, S., 283 Mohamed, Y., 409410 Mohammed, M., 1518, 20 Mokhtar, S.I., 385387 Mondrago´n-Jacobo, C., 188190, 189t Monteiro, M.F., 116 Monteiro, M.Y., 225226 Montes, M., 130131 Montiel-Rodrı´guez, S.M., 190191, 190t Montim, M., 7 Montoya-Arroyo, A., 346 Moo-Huchin, V.M., 343 Mora, D.F., 363364 Moradi, S., 364, 366 Moraes, J.A.P.V., 307 Moraes, V.H.D.F., 50t Moreira, L.C., 82 Moreno, C., 153 Moreno, M., 192t Moreno, P.R.H., 219220, 221t Moretti, C.L., 42 Morita, H., 164t, 165 Mors, W.B., 295 Morton, J., 1517, 20, 141143, 163164, 164t, 271272, 280, 444, 446 Morton, J.F., 15, 20, 108111, 110t, 153157, 155t, 319 Mosquera, L.H., 299 Mosshammer, M.R., 194t Moßhammer, M.R., 197t, 198 Mota, W.F., 238t, 241 Moura, C.F.H., 9t, 1011, 88 Moura, F.T., 308, 311t, 431 Moura, M.F., 365t Mowry, H., 165 Moyer, R.A., 215 Msonthi, J.D., 295 Muhammad, K., 342343, 346 Muhtadi, Primarianti, A.U., 371372 Mukherjee, D., 406 Mukherjee, K., 329t Mun˜oz de Ch, M., 146t Mun˜oz-de-Cha´vez, A., 190, 191, 192 Muramoto, K., 290 Murch, S., 56t, 57t Murch, S.J., 58 Muthumperumal, C., 443 Myhaia, E., 288t Myoda, T., 99102, 101t
N Nadia, T.L., 427 Naef, R., 271 Nagahama, K., 276 Nagalingam, S., 323 Nagendra, K.P., 379t Nakasone, H.Y., 123 Nakatsuka, A., 113 Nambour, D., 113 Namdaung, U., 125 Nandhasri, P., 323 Nanthachai, S., 174175 Narain, A., 446 Narain, N., 308, 312t, 316, 429, 430t Nascimento, C.EdeS., 428t, 429 Nascimento, O.V., 99102, 101t Nascimento, R.S.M., 309 Nascimento Filho, F.J., 229, 231233 Nascimento Filho, J.F., 232 Naser, F.A., 306 Naskar, K., 327 Nasrollahzadeh, M., 7273 Nathan, T.W., 323 Natividad Marı´n, L., 157 Naves, R.V., 77 Nelson, S.C., 319321 Nerd, A., 340, 342344 Neri-Numa, I.A., 352353 Neto, L.G.M., 300 Neto, M.A.S., 320f Netzel, M., 207t, 208 Neuwald, D.A., 114 Neves, L.C., 9899, 102 Nie, Q., 339340 Niembro, R.A., 141142, 149 Nijveldt, R.J., 219, 221 Nile, S.H., 242 Nilsson, F., 211 Ninio, R., 295t Nissan, R.J., 113 Njoku, V.O., 373 Nobel, P.S., 190191, 341 Nogueira, A.K.M., 45 Nogueira, L.P., 311316, 312t Nogueira, R.T., 258 Noomrio, M.H., 253t Noor, Y.R., 329 Nora, C.D., 34 Normah, M.N., 388 Nur ‘Aliaa, A.R., 345
O Obenland, D., 42, 343344, 346 Obire, O., 166 Obon, C., 337 Ochoa-Velasco, C.E., 191, 193, 195199 Ochse, J.J., 16 Odoux, E., 193t Oetterer, M., 72 Ogawa, K., 274275 Ogunwande, I.A., 337 O’Hare, T.J., 373 Ojima, M., 285
453
454
Author Index
Okafor, J.C., 380 Okechukwu, P.N., 282t Okigbo, R.N., 166 Okiy, A.D., 380 Okonogi, S., 371372 Okuda, T., 219, 222 Oliveira, A.L., 240241 Oliveira, A.P., 365 Oliveira, A.R.G., 299 Oliveira, D.L., 308309 Oliveira, D.M., 297, 300 Oliveira, G.L., 364, 366 Oliveira, J.R.P., 7 Oliveira, L.S., 9t, 1012, 12t Oliveira, M.do S.P.de, 14 Oliveira, R.A., 33t Oliveira, T.B., 160 Oliveira, V.B., 77 Oliveira, V.Rde, 429 Oliveira, V.S., 299300 Oliveira Sousa, A.G., 33 Omena, C.M.B., 145 Omoti, U., 380 Ong, C.N., 282t Ong, P.K.C., 372 Onyechi, A.U., 393t Ordo´n˜ez, J.A., 301302 Orellana, P., 136f Ortiz, J.M., 271, 274275 ´ vila, O., 4446 Ortı´z-A Ortiz-Herna´ndez, Y.D., 339, 341, 345 Orwa, C., 107109, 111 Osipova, S.V., 307 Osuna-Enciso, T., 343344 Osuna Garcia, J.A., 145147 Othaman, H., 384385 Otsuka, H., 265 Ozdemir, F., 40, 4243 Ozgen, M., 358
P Palanisamy, U.D., 371 Palapol, Y., 171, 173 Palhares, D., 33 Pallardy, S.G., 307 Pallavi, R., 252 Palu, A.K., 322323 Panda, S., 165 Pandey, V., 397 Pangkool, S., 170176 Pantastico, E.B., 172 Pardo Sandoval, M.A., 153, 157 Paredes, O., 197, 197t Pareek, O.P., 165t, 265, 393t Pareek, S., 165t, 166, 287, 288t, 391, 393t, 400401, 401t Parente, T.V., 307 Park, J.K., 299 Park, K.J., 300 Park, M.H., 265 Park, S.W., 242 Parry, M.A.J., 307 Parthasarathy, N., 443 Parvin, K., 28 Passos, M.A.B., 61
Pastene, E., 135 Patel, H.B., 444446, 445t Patel, S., 34 Pathak, R.K., 409410 Patil, P.D., 329 Pattenden, G., 26 Paul, D.K., 253t Paul, V., 85 Paula, S.O., 319 Paull, R., 153157 Paull, R.E., 37, 40, 43, 123, 175, 273, 308, 373, 391393 Pawlowska, A.M., 266 Pawlus, A.D., 319 Pechnik, E., 420 Peixoto, A.M., 122 Pekmezci, M., 355356 Pele, J., 15 Peng, L.W., 275 Penha, E., 73t Penn, J.W., 97 Pennigton T.D., 142143 Pequen˜o, G., 130f Pereira, A.C., 309 Pereira, A.G., 258 Pereira, A.L.F., 88, 161 Pereira, A.V., 309 Pereira, F.M., 113, 286 Pereira, G.M., 364 Pereira, J.C.R., 230 Pereira, M., 237 Pereira, M.C., 436 Pereira, M.C.T., 238t, 240 Pereira, M.E.C., 42 Pereira, T.N.S., 227 Perez, A.M., 321t Perez, G.R.M., 346 Pe´rez, R.A., 371 Pe´rez-Arias, G.A., 142144 Perez-Gutie´rrez, R.M., 346 Pe´rez Lopex, A., 144145 Perisamy, E., 416t, 417t Perosa, J.M.Y., 286 Pesis, E., 117 Pessa, J., 133 Peters, C.M., 9798, 102 Petkowicz, C.L., 160161 Peuckert, Y.P., 103 Phaechamud, T., 330t Phatdiphan, S., 282 Phebe, D., 341 Phillipps, K., 121122 Phillips, K.M., 87 Phutdhawong, W., 174 Pierpaoli, E., 2628 Piga, A., 188192, 194, 196199 Pimienta-Barrios, E., 188192 Pinedo-Espinoza, J.M., 196197 Pinheiro-Sant”Ana, H.M., 33t Pino, J.A., 26, 153, 156, 247, 248t Pintaudi, A.M., 193t Pinto, A.C.D.E.Q., 163, 166 Pinto, Ad.Q., 398400 Pinto, A.D.Q., 391395, 393t Pinto, M.D.S., 215 Pio, R., 285286, 288t, 363364, 366
Pire, S.M.C., 145 Pires, A.J.V., 72 Pires, I.E., 428t Pires, J.L., 69 Pires, M.G.M., 427 Pitke, P.M., 406 Plagemann, I., 241 Plaza, L., 40 Pohlan, J., 370371 Polprasid, P., 169170 Pongsamart, S., 174 Pontillon, J., 72 Pontoh, J., 281 Poovarodom, S., 173174 Popenoe, J., 1516, 20 Popenoe, W., 1617 Porat, R., 359 Porcu, O.M., 336 Porter, L.J., 213214 Postman, J., 363 Potterat, O., 323 Powell, D., 53 Prabhakara Rao, P.G., 2728 Pradhan, D., 444 Prado, L.C. da S., 82 Prakash, N., 203, 205 Prakash Maran, J., 373 Prasad, K.N., 439440 Prasad, N.K., 109t Prasanna, V., 11, 102 Pratt, H.K., 85 Prill, M.A.S., 364 Priyadarshani, A.M., 110t Priyanto, L.H.A., 388 Pugliese, A.G., 160 Punitha, V., 344 Purseglove, J.W., 403, 408, 427 Pushpakumara, D.K.N.G., 108
Q Qiong, C., 339340 Queiroz, J.A.L., 12 Queiroz, V.A.V., 300 Querejeta, J.I., 143 Quezada, M., 129 Quijano, C.E., 153, 156 Quin˜ones-Islas, N., 4446 Qureshi, A.A., 444
R Rabinowitz, D., 328 Radlkofer, L., 226 Ragone, D., 5355, 56t, 5759, 57t Rahman, M.A., 125 Rahman, M.M., 164165, 164t Rahmat, A., 416t, 417t Rahmatullah, M., 329 Rai, A., 329t Rakariyatham, N., 371 Rama Rao, M., 408 Ramalho, R.S., 23 Ramalho, S.A., 145 Ramanan, R.N., 379t Rame´rez-Truque, C., 342343, 346
Author Index
Ramful, D., 275, 309 Ramı´rez, J.G.A., 141 Ramı´rez Hernandez, B.C., 146t Ramos, 422 Ramos, A.S., 32, 33t Ramos, M.I.L., 297, 300 Ramsundar, D., 20 Ranti, A.S., 282t Raseira, A., 3132 Raseira, C.B.M., 31 Raseira, M.C.B., 3132 Rashid, A., 345 Ratanachinakorn, B., 176 Ratti, C., 102 Raupp, D.S., 117 Ravindran, D.S., 409410 Ray, P.G., 408 Raynor, W.C., 55 Razali, B., 280281 Razeto, B., 42 Realini, C.E., 910 Reddy, M.K., 2628 Redfern, T.N., 5455 Reece, P.C., 205 Reis, D.S., 9t Reksodihardjo, W.S., 169 Resende, M.D.V., 229 Reynertson, K.A., 219, 248 Reynes, M., 321t Rezende, C.M., 18 Rezende, J.R., 297 Rezende, L.C.G., 241 Rhodes, M.J.C., 272273 Ribeiro, E.M.G., 80 Ribeiro, S.M.R., 33t Rieser, M.J., 392393 Righetto, A.M., 11 Riley, J.M., 203 Ritter, C.M., 181 Ritzinger, C.H.S.P., 8 Ritzinger, R., 78 Rivera, D., 337 Rivera, G., 143, 149 Roberts, J.A., 173 Roberts-Nkrumah, L.B., 53, 5758 Robins, J., 203 Rocha, C., 81, 308309 Rocha, I.S., 72 Rocha, K.R.A., 311t Rocha, M.S., 7880, 309, 310t, 311t Rodov, V., 273274 Rodrigues, E., 33t, 156, 220t, 223t Rodrigues, R.B., 97, 99, 102 Rodrı´guez, A., 285 Rodrı´guez, S., 188192 Rodriguez-Amaya, D.B., 221, 300301 Rodrı´guez-Fragoso, L., 44 Rodrı´guez-Herna´ndez, G.R., 198 Roehrs, M., 2628 Roesler, R., 33, 80 Rogez, H., 4, 160 Rojas, J., 130f Rojo, R., 197, 197t Romero, M.A., 366 Romorini, D., 365366 Romphophak, T., 176
Ross, I.A., 251252, 319, 403 Rossini, C., 351 Rosso, V.V., 33t, 220t, 223t Rotili, M.C.C., 309 Roulle, P., 203, 208 Roy, A., 329t Rozzi, S., 130 Ruberto, G., 206 Rufino, MdoS.M., 430t, 431 Rufino, M.S.M., 12t, 50, 8687, 305, 310t, 311, 311t Ruiz, L., 99102, 101t Ruiz, M., 133 Rusconi, M., 7273 Ryan, E., 87
S Sa´, S.T.V., 420 Sabaa-Srur, A.U.O., 220t Sabir, S., 365366 Sacramento, C.K., 227 Sadek, E.S., 274276 Sadhu, S.K., 329 Sa´enz, C., 188192, 192t, 197, 197t Sa´enz, E., 192, 192t Sagrero-Nieves, L., 406 Sagrillo, M.R., 420, 422423 Said, O., 289 Saka, J.D.K., 295t Salgado, J.M., 160 Salgueiro, F., 333 Salim, A., 409 Salma, I., 280281 Saloma˜o, L.C.C., 238t Salvador, A., 114, 116117 Salvador, M., 32f Sampaio, A.S., 144145 Sampaio, M.B., 62 Sampaio, P.T.B., 257259 Sampaio, S. de A., 308 Sampaio, S.T., 311316, 312t Samuagam, L., 282t Sanches, J., 286, 289 Sanches, M.C.R., 9293 Sancho, S.O., 87 Sanchotene, M.C.C., 333334 Sang, M.L., 266 Sang, S., 323 Sangiovanni, E., 219, 221 Sangwanangkul, P., 171 Sankat, C.K., 58, 246, 248 Sano, E.E., 32 Sano, S.M., 310t Santana, A.C., 45 Santana, A.C.de, 25 Santiago, M.C.P.A., 223 Santos, A.R.F dos, 305 Santos, A.T., 7273 Santos, C.A.F., 149, 427429, 428t Santos, C.O., 72 Santos, C.T., 431432 Santos, D.T., 240 Santos, G.G., 352t Santos, J.T.S., 310t Santos, L.M.P., 6163, 66
455
Santos, M.D.S.S.A., 50t Santos, M.F.G., 6364 Santos, M.N., 261 Santos, M.N.G. dos, 81 Santos, P.R.G., 33t Santos, P.R.P., 5051 Santos, R.C.C., 432 Santos, R.S., 66 Santos, S.M.L., 7 Santos, T.C., 72, 149 Saraswathi, C.D., 323 Sargent, S.A., 8788 Sari, P., 252253 Sartori, S., 435, 437 Sarubbio, M.G., 335 Sarukha´n, J., 142143 Sato, K., 409 Sauls, J.W., 1516, 20 Sawant, T.P., 392393 Sawaya, W.H., 188192, 197198, 197t Sazan, M.S., 78 Scalon, S.D.P.Q., 89 Scalon, S.P.Q., 3132, 307, 435437 Scaloppi Ju´nior, E.J., 285286 Scariot, A.O., 297 Schaffer, C.C., 219, 222 Schapoval, E.E.S., 337 Schauss, A., 391395 Scherer, R., 8687 Scheuermann, E., 129, 133 Schirra, M., 196, 272275 Schmeda-Hirschmann, G., 337 Schneider, R.G., 10 Schreckenberg, K., 380381 Schreckinger, M.E., 1112 Schuelter, A.R., 157 Schulze, M., 259 Schunemann, A.P.P., 431 Schwartz, G., 257, 259260 Schweiggert, R.M., 87 Scora, R.W., 3940 Scotter, M., 2526 Seifert, K.E., 363 Seifried, H.E., 275276 Selcuk, M., 357359 Sellappan, S., 194t Senawi, M.T.M., 388 Sepu´lveda, E., 188192, 192t, 197198, 197t Serafini, M.R., 323 Serna-Cock, L., 157, 344 Seymour, C., 213215 Seymour, G.B., 40 Shah, A.H., 265 Shaha, R.K., 253t Shahid-ul-Islam, Rather, L.J., 2528 Shajib, M.T.I., 254 Shallenberger, R.S., 123 Shankaracharya, N.B., 409 Shanley, P., 1, 35, 259, 420, 422 Shao, X., 288t Shao, Y.Z., 373 Sharma, R., 366 Sharma, R.R., 196 Sharma, S.B., 252t Shen, D.Y., 439440 Shenoy, C., 398
456
Author Index
Shibamoto, T., 160 Shibamoto, T.A., 275 Shibata, A., 2628 Shigematsu, E., 298 Shin, T.Y., 290 Shoei, S.L., 266 Shui, G., 371372 Shulman, Y., 355 Sia, C.M., 282t Siddhuraju, P., 406 Sievers, A.F., 181 Silva, A.B., 337 Silva, A.C.M.S., 309, 310t, 311t Silva, Ada, 427 Silva, A.N.C. da, 309, 310t, 311t Silva, A.Qda, 427 Silva, B.M., 363 Silva, C.A., 107109 Silva, C.A.A., 141, 149 Silva, C.D.M., 81 Silva, C.M.MdeS., 428429, 428t Silva, C.V., 435 Silva, E.C., 307 Silva, F.A., et al., 33t Silva, F.G., 364, 366 Silva, F.J.F., 242 Silva, H.Dda, 428t Silva, H.G.O., 72 Silva, I.M., 88 Silva, J.A., 7778, 80, 298 Silva, J.A.A., 286 Silva, J.J.M., 11 Silva, L.B.C., 305, 311t Silva, M.A., 102, 299 Silva, M.R., 7980, 258260, 309, 352t Silva, N.A., 3233, 33t, 220221, 220t, 223t Silva, N.Ada, 436437 Silva, P.I., 23, 2526 Silva, Q.J., 145 Silva, R.Pda, 429, 430t Silva, R.S., 6164 Silva, S.A.M., 7273 Silva Filho, D., 155t Silva Filho, D.F., 153157 Silve, E.R., 194t Silveira, C.E.S., 77 Simlai, A., 328, 329t Singh, B., 307, 405 Singh, D.R., 322 Singh, G., 307 Singh, S.P., 164, 408 Singha, R.K., 409 Siondalski, P., 174 Siripanich, J., 170171, 173, 175176 Siriphanich, J., 175176 Sirisompong, W., 374 Sitrit, Y., 293294, 295t Siva, R., 26 Sivakumara, D., 373 Small, E., 276 Smith, J., 2425 Smith, N.J.H., 23 Smith, T.J., 28 Smits, W.T.M., 383385, 388 Soares, E.C., 298 Sobral, M., 220t, 237, 333, 435
So¨derling, E., 213214 Solı´s Neffa, V.G., 229 Solı´s-Fuentes, J.A., 374 Solis-Magallanes, J.A., 143 Soltis, D.E., 229 Soltis, P.S., 229 Sommano, S., 208 Sone, Y., 409 Sonwa, D.J., 380 Souci, S.W., 364, 365t Sousa, A., 320f, 323 Sousa, J., 320f Sousa, L.S., 72 Sousa, N.R., 226, 230, 232 Souza, A.G.C., 227, 419 Souza, A.L., 102 Souza, E.R.B., 7779 Souza, F.G., 305, 310t Souza, G.C., 335 Souza, K.O., 1112, 12t Souza, L.T., 156 Souza, M.C., 308309, 310t Souza, M.J.H., 8 Souza, P.C.A.de, 1 Souza, R.B., 240241 Souza, R.K.D., 258 Souza, R.O.S., 33t Souza, R.P., 307 Souza, V.C., 435 Souza, V.D., 51 Souza Filho, O.C., 422 Souza-Moreira, T.M., 242 Splittstoesser, W.E., 409410 Sreevidja, N., 423 Srivastana, H.C., 282 Srivastava, S.D., 265 Srivastava, S.K., 265 Srivasuki, K.P., 409410 Sriyook, S., 172173 Standley, P.C., 142143 Stange, E.J., 181 Stebbins, G.L., 231 Stepp, J.R., 142 Stewart, K., 215 Steyermark, J.A., 142143 Stintzing, F.C., 187, 191194, 194t, 197t, 199, 342 Storrs, A.E.G., 409 Stringheta, P.C., 23, 2526, 27f, 28 Sua´rez, R., 189t Subash-Babu, P., 251254, 252t Subhadrabandhu, S., 169170, 175, 177, 413414 Sudjaroen, Y., 406 Sugiura, A., 113115 Suguino, E., 219, 222, 237, 239 Suhartati, T., 125 Suica-Bunghez, I.R., 385387 Sukewijaya, I.M., 383 Sulieman, A.M.E., 406 Suman, T.Y., 323 ˇ Sumic, Z.M., 184t Sumithraarachchi, D.B., 110t Sun, G., 289 Sun, J., 379t Sun, Q., 32
Supapvanich, S., 384385 Supriyadi, 385386, 388 Suranant, S., 123 Sutthaphan, S., 174 Suwalsky, M., 133 Suzuki, T., 116 Swaminath, M.H., 409410 Swingle, W.T., 204205, 271 Syah, Y.M., 124125 Sykes, S.R., 209
T Taba, S., 345 Tadeo, F.R., 272 Tadisco, M.K., 145147 Taira, S., 116 Tamayo, L.M.A., 261 Tan, S., 276 Tanaka, K., 290 Tanaka, T., 115 Tang, Y.P., 413, 415, 416t Tansiriyakul, S., 170 Taylor, F.W., 293 Taylor, M.B., 53 Tchoundjeu, Z., 377 Tecchio, M.A., 365t Tee, L.H., 377378, 379t, 380 Teixeira, G.H., 240 Teixeira, G.H.D.A., 50 Teixeira, L.L., 220221, 220t, 222f, 222t Teixeira, M.L.F., 261 Telles, M.P. de C., 78 Tel-Zur, N., 339340 Temiz, H., 289 Temple, L., 17 Tenore, G.C., 346 Terra, F.A.M., 116 Terry, L.A., 40 Tesoriere, L., 192, 193t Tessmer, M.A., 115 Texeira, D.M., 148149 Theron, M.M., 215 Thimmaraju, K.R., 405 Thitilertdecha, N., 371373 Thohari, M., 383, 388 Thomidis, T., 366 Thompson, A.K., 217 Tian, S., 287 Tilaar, M., 282t, 283 Timbola, A.K., 252t Timyan, J., 408 Tindall, H.D., 369 Tirimanna, A.S.L., 26 Tiwari, A.K., 329 To, L., 344 Toledo, F., 173174 Toledo, F.F., 122 Tomlinson, P.B., 328 Tongdee, S., 170, 176 Tongdee, S.C., 170, 174176 Tontrong, S., 323324 Topuz, A., 40, 4243 Torma, P.C.M.R., 4 Torres, A., 129, 132t, 133 Toshiyuki, N., 424
Author Index
Tran, D.H., 339 Tressl, R., 213214 Trevisa, M.T.S., 87 Tripathi, M., 265 Troup, R.S., 409 Trozzi, A., 206 Trugo, L.C., 89, 11 Tschesche, R., 265 Tsuda, T., 252, 406 Tucci, M.L.S., 69 Tucker, N., 190 Turi, C., 55, 56t, 57t
U Uchiyama, H., 9798 Ueda, H., 99102, 101t Uenojo, M., 300 Uji, T., 417 Umano, K., 275 Undurraga, P.L., 286 Unlu, N.Z., 4142 Urbiloa, M.C., 189t Usha, K., 405 Ushanandini, S., 406, 408
V Vaillant, F., 321t Valencia-Botı´n, A.J., 345 Vale´rio, M.A., 26 Valle`s, J., 181 Vallilo, M.I., 9293 Valois, A.C.C., 231232 Van Eck, A., 217 Vanegas, M.J., 142145 Vangdal, E., 102 Vargas-Simo´n, G., 141143 Varghese, K.J., 329 Vasco, C., 93 Vasquez, A., 9798, 102 Va´squez-Ocmı´n, P.G., 63, 6566 Vaughan, J.G., 271 Veberic, R., 116 Veigas, J.M., 252t, 253254 Vekiari, S.A., 4243 Velazquez, E., 337 Vendramini, A.L., 89, 11 Verdalet, I., 194t Verheij, E.W.M., 123 Verı´ssimo, A.J.M., 72 Vicente, A.R., 275276 Vicente, P., 286 Vidhya, R., 446 Vidigal, M.C., 102 Vieira, F.A., 353 Vieira, G., 238t Vieira Neto, R.D., 305, 308309 Vieites, R.L., 241 Vignoni, L., 197198 Vijayvargia, P., 443446 Vijayvergia, R., 443446 Vilar, D., 2628 Vilas-Boas, E.V.B., 33t Vilela, P.A., 78
Vilhena, A.M.G.F., 7 Villachica, H., 50, 9799, 102, 155t Villa-Rodrı´guez, J.A., 40 Vilpulasena, S.M.P.M., 444 Viswanathan, G., 253254 Vivien, J., 1517 Vizzoto, M., 34t Vizzotto, M., 337 Volpato, G., 153154 von der Pahlen, A., 155t Voon, Y.Y., 176177 Vracar, O., 184t Vriesmann, L.C., 74t, 160161 Vulic, J., 183, 184t
W Wagner, H., 164t Wall, M.M., 322, 345, 372373 Wallace, G., 240 Wang, C.Y., 92 Wang, M.Y., 319 Wang, Y.C., 274275 Warrier, P.K., 251 Wasantha, L.P.G., 345 Wasitaatmadja, S.M., 282t Watada, A.E., 3940 Watanapa, A., 177 Watson, J.G., 327 Webster, S.A., 5758 Wehmeyer, A.S., 293 Wehncke, E.V., 141142 Wei, Y., 287, 288t Wertheim, S.J., 363 Westendorf, J., 323 Wetwitayaklung, P., 329331, 330t Weyerstahl, P., 337 Whiley, A.W., 37, 43 Wichienchot, S., 346 Widyawaruyanti, A., 124125 Wih, W.L., 282t Wijanarti, S., 387 Wijaya, C.H., 386 Wilaipon, P., 177 Winsborrow, C., 17 Winton, K.B., 16 Winton, L.A., 16 Wisutiamonkul, A., 171, 172f, 174 Wiyaratn, W., 177 Wong, K.C., 123, 247 Wong, L.J., 388 Woo, K.K., 346 Woo, W.S., 265 Woolf, A., 117 Worrell, D.B., 55, 57 Wrolstad, R.E., 123, 253 Wu, F.Z., 307 Wu, Y.C., 164 Wutscher, H.K., 272 Wybraniec, S., 342
X Xavier, D., 365t Xu, F., 288t
Xu, H., 287 Xu, Z., 266
Y Yaacob, O., 121, 175 Yahia, E., 282 Yahia, E.M., 165t, 393t Yahia, E.Y., 195196 Yakushiji, H., 113 Yamaguchi, K.K.L., 45 Yang, B., 379t Yang, H., 159 Yang, S., 287 Yang, X.L., 323 Yang, Y.L., 165 Yazawa, K., 99102, 101t Ye, Y., 271 Yi, R.H., 345 Yi, W., 194t Yi, Y., 343 Yim, H.S., 282t Yingsanga, P., 372 Yonemori, K., 113115 Yoshikawa, M., 265 Yoshioka, S., 290 Youmbi, E., 1718 Young, M.C.M., 220t Young, R.E., 3940 Youssef, K., 273 Yusof, Y.A., 345 Yuvakkumar, R., 373 Yuyama, K., 155t Yuyama, L.K.O., 155t, 161
Z Zahid, N., 344 Zambiazi, R.C., 32f Zambon, C.R., 364 Zanatta, C.F., 65, 99102, 101t Zapata, S.M., 99 Zar, P.P.K., 289 Zarfeshany, A., 355 Zarringhalami, S., 2728 Zawiah, N., 384385 Zeng, L., 265 Zerega, N., 54 Zerega, N.J.C., 5354 Zhang, M., 307 Zhang, W., 288 Zheng, Y.H., 289 Zhou, C.H., 288 Zhou, W., 366 Zhuang, D.H., 113 Zhuang, H., 323 Zhuang, Y., 346 Zielinski, Q.B., 211 Zillo, R.R., 436 Zin, Z.M., 323 Ziyaev, R., 265 Zizumbo-Villarreal, D., 141142 Zucchi, M.I., 77
457
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Subject Index Note: Page numbers followed by “f ” and “t” refer to figures and tables, respectively.
A Ac¸aı´ (Euterpe oleracea Mart.), 2f in Amazon region, 23 chemical properties and composition, 4 estimated annual production, 34 fruits and seeds of, 1, 3f lipid levels, 4 production, 2 harvest/postharvest conservation, 34 harvest season, 3 industrial application, 45 of pulp, 5 of seeds, 5 of stems, 5 juice, 4 production, 23 uses of, 45 nutritional value, 4 origin, 13 regeneration of, 12 reproduction phase, 3 sensory characteristics, 4 species, 1 varieties of, 1 Acerola (Malpighia emarginata D.C.), 7 chemical composition of, 11, 12t polyphenols, 1112 flavor, 10 flowers of, 7 fruits of, 78 harvesting of, 8 loss of vitamins of, 910 nutritional composition of anthocyanin content, 1112 cyanidin contents, 1112 flavonols, 12 vitamin C content, 11 origin and botanical classification, 78 pectin level, 10 phytochemical constituents of, 11 postharvest of, 810 quality, 1012 production, 8 countries producing, 8 in different developmental stages, 9f ideal climate for, 8 susceptibility to pests, 8 quality attributes of, 9t rate of autoincompatibility, 7 ripening and senescence, 9
physical characteristics, 10t size of, 7 storage life of, 9 volatile compounds of, 11t Acrocomia aculeata. See Macauba palm (Acrocomia aculeata) Aegles marmelus. See Bael (Aegles marmelus) α-cryptoxanthin, 64 Ambarella (Spondias cytherea), 16f, 17f applications as an alternative source of pectin and fibers, 20 as food additive, 20 in fruit processing, 20 pulp and peels, 20 chemical composition, 1820 description, 1617 fruit amino acid content of, 18 biochemical and physicochemical composition, 19t conservation of, 20 development and maturation, 1718 nutritional value, 1820 ripening, 18 sensory characteristics of, 20 vitamins C and A in, 18 harvest and annual production, 17 origin and distribution, 15 taxonomy and colloquial names, 16 Anacardium occidentale. See Caju (Anacardium occidentale) Annatto/Urucum (Bixa orellana L.) biological activities of compounds, 2627 antitumor effects, 27 protective effect of bixin and norbixin, 2627, 27f biosynthesis of compounds, 26 chemical composition of, 2526 structural formulas of bixin, norbixin and norbixin salt, 25f estimated production and trade of, 2425 harvest and annual production, 23 industrial application, 2728 colorants, 2728 pigments, 28 origin and botanical aspects, 23 postharvest conservation, 24 seeds, 24f
Annona muricata. See Soursop (Annona muricata) Annona squamosa L. See Custard apple (Annona squamosa L.) Annona squamosa Linn. See Sugar apple (Annona squamosa Linn.) Anthocyanin, 4 Apis mellifera, 92 Arac¸a´ (Psidium cattleyanum), 32f antimicrobial effects, 34 antioxidant activity, 3234 botanical aspects, 31 cultivars, 31 fruit physiology, 3234 harvest and annual production, 3132 industrial application, 3435 Psidium guinnensis jam, 35 as jams, juices, icecreams, and liqueurs, 34 nutritional value, 3234, 33t origin, 31 phytochemicals content and antioxidant activity of, 34t postharvest conservation, 34 shelf-life, 34 Areca catechu, 383 Artocarpus altilis (Parkinson) Fosberg. See Breadfruit (Artocarpus altilis (Parkinson) Fosberg) Artocarpus camansi Blanco, 53 Artocarpus champeden. See Cempedak (Artocarpus champeden) Artocarpus heterophyllus. See Jackfruit (Artocarpus heterophyllus) Artocarpus odoratissimus. See Tarap (Artocarpus odoratissimus) Artocarpus species A. altilis. See Breadfruit (Artocarpus altilis (Parkinson) Fosberg) A. champeden. See Cempedak (Artocarpus champeden) A. elasticus, 125 A. hirsutus, 122 Astrocaryum aculeatum. See Tucuma˜ of Amazonas (Astrocaryum aculeatum) Australian finger lime. See Finger lime/The Australian Caviar (Citrus australasica) Avocado (Persea americana), 37 appearance of different, 38f botany and origin, 37 as butter fruit, 40
459
460
Subject Index
Avocado (Persea americana) (Continued) chemical composition and nutritional value, 4042, 41t cultivars, 37, 39t different horticultural races of, 38t ecological races of, 37, 42 Eriodaphne family, 37 estimated annual production, 44, 45f harvest and postharvest conservation, 4344 harvest season, 4243 health benefits of, 4142 hybridization, 37 industrial application and other uses, 4446 Lauraceae family, 37 nutritive and nonnutritive substances, 4041 oil content of, 40 parts of, 39f phases of development of, 3940 physiological or harvest maturity, 4243 physiology and biochemistry, 3940 protein level, 40 respiration, 40 ripening of, 40 sensory attributes, 42 world trade, 44
B Baccaurea motleyana. See Rambai (Baccaurea motleyana) Baccaurea racemosa. See Kapundang (Baccaurea racemosa) Bacuri (Platonia insignis) applications, 5051 as a source for culinary products, 50 characteristic flavor, 51 harvest and annual production, 49, 51 origin and botanical aspects, 49 physical and chemical characterization of, 50t postharvest conservation, 50 pulp quality, 50 Bael (Aegles marmelus), 443 Banana (Musa spp.), 385 Barbados cherry tree. See Acerola (Malpighia emarginata D.C.) Betalains pigments, 346 Bixa orellana L. See Annatto/Urucum (Bixa orellana L.) BLUP (best linear unbiased predictor), 234 Breadfruit (Artocarpus altilis (Parkinson) Fosberg), 54f, 122, 415, 417 chemical composition and nutritional value, 5556 cultivars, 5354 estimated annual production, 55 fruit physiology and biochemistry, 55, 56t grading standards, 58 harvest and postharvest conservation, 5758 harvest season, 5455 industrial application, 5859 as breadfruit flour, 58 as livestock feed, 59
processing fruit into chips and other snacks, 58 mineral content, 56t monoecious nature of, 54 origin and botanical aspects, 5354 sensory characteristics, 57 vitamin content, 57t Buriti fruit (Mauritia flexuosa), 62f biological benefits, 65 botanical characteristics, 61 fruit morphology, 6263, 63f ash amount, 63 carbohydrate content, 63 cold pressing procedures, 64 crude fat content, 63 crude protein level, 63 metabolites, 64, 65f nutrient content, 63, 64t pericarp, 6263 water content, 63 harvest and postharvest conservation, 66 harvest season and annual production, 62 industrial applications, 66 in cosmetic industry, 66 in pharmaceutical industry, 66 origin and considerations, 61 sensory characteristics and food application, 66
C Cacao (Theobroma cacao L.), 70f applications in chocolate making, 72 bark, chemical composition of, 74t beans centesimal composition of the fermented and dried, 74t processing, 72 chemical composition, 7274 flowers, 71 fruit, 71, 71f physical characteristics of, 73t harvest of, 72 leaves, 71 moisture content of, 72 nutritional value, 7274 origin and botanical aspects, 6971 physicochemical composition of cocoa pulp, 73, 73t root system, 71 seed, 71 chemical composition of, 74t physical characteristics of, 73t stem, 71 Cagaita (Eugenia dysenterica), 78f, 79f antioxidant activity, 80 botanical aspects, 7778 flowering, 77 fruits, 77, 79, 81 harvest and postharvest conservation, 8082 harvest season and estimated annual production, 7879 industrial applications, 8082
leaves, 77, 82 nectar, 81 origin, 7778 physiology and biochemistry of, 7980 pulp, 81 Recommended Daily Intake (RDI), 80 seeds, 81 flour, 81 water content, 80 Caju (Anacardium occidentale), 86f botanical and agronomical aspects, 85 chemical composition and nutritional value, 8687 fruit physiology and biochemistry, 8586 harvest and postharvest conservation, 8788 industrial application, 88 Cambuci (Campomanesia phaea (O. Berg.) Landrum) antioxidant activity of, 93 ascorbic acid and phenolic compound contents, 93 chemical composition and nutritional value, 9293 estimated annual production, 92 flowers, 92 fruit, 92 physiology and biochemistry of, 92 harvest season, 92 human health benefits, 93 origin, 9192 plant, 91 sensory attributes, 93 tree, 91 tree reproduction, 92 Campomanesia phaea (O. Berg.) Landrum. See Cambuci (Campomanesia phaea (O. Berg.) Landrum) Camu-camu (Myrciaria dubia (Kunth) McVaugh) extracts and bioactive phytochemicals of, 101t fruit, 98f chemical and nutritional compositions, 99 physiology and biochemistry, 9899 harvest and postharvest conservation, 102 harvest season and annual estimated production, 98 health-promoting phytochemicals, 99102, 101t industrial applications, 103 frozen fruit pulp, 103 in pharmaceutical industry, 103 production of vitamin C, 102103 origin and botanical aspects, 9798 sensory characteristics, 102 shrub, 9798 Canistel (Pouteria campechiana (Kunth) Baehni), 108f antioxidant, antinitrosative, and antimitotic qualities, 109 carotenoid content and retinol equivalent (RE) of, 110t chemical composition, 109 estimated annual population, 108
Subject Index
food value for edible portion, 110t fruit distribution and cultivation of, 108 physical properties, 109t physiology and biochemistry, 108109 harvest and postharvest conservation, 110 harvest season, 108 industrial applications, 110111 in chewing gum, 111 as a poultry feed, 111 nutritional value, 109 origin and botanical aspects, 107108 pharmaceutical applications as antipyretic medication, 111 in traditional medicine, 109 sensory characteristics, 109 Caqui (Diopyros kaki) chemical composition and nutritional value, 116 estimated annual production, 114 fruit physiology and biochemistry, 115116 harvest and postharvest conservation, 117 harvest season, 114 industrial application, 117 origin and botanical aspects, 113114 sensory characteristics, 116117 Cashew apple, 85, 86f aroma profile, 87 color, 8586 grading of, 87 juice, 8688 phenolic compound of, 87 storage of, 88 Cashew nut, 88 oil, 87 Cempedak (Artocarpus champeden), 122f anticancer activity, 124 antimalarial activity, 124 against Plasmodium falciparum, 124 bark of, 125 biological activities of, 125 cytotoxicity, 125 leaves of, 125 lectin and cell adhesion activity, 124125 medicinal uses, 125 nutritive and medicinal properties, 123125 origin and botanical aspects, 121123 pulp, 123 seeds, 123, 125 Chilean Guava (Myrtus ugni), 129, 130f, 131f consumption level, 131132 challenges of the murtilla market, 132 ethnic uses, 130 phytochemistry and biological activity, 132133 socioeconomic importance, 130132 storage life, 131132 Chilean wineberry, 133 Ciruela/Mexican plum (Spondias purpurea L.), 142f, 143f, 144f chemical composition and nutritional value, 145, 146t volatile compounds, 145, 148t volatile flavor compounds, 147t
consistency gums of, 148149 estimated annual production, 144 fruit physiology and biochemistry, 144145 harvest and postharvest conservation, 145147 harvest season, 143 industrial applications, 148149 in jams or candies, 148 organic waste capacity of, 149 origin and botanical aspects, 141143 rheological properties of, 149 shelf-life, 145147 way of propagation, 149 Citrus australasica. See Finger lime/The Australian Caviar (Citrus australasica) Citrus species, 203 botanical classification, 204 C. australasica F. Muell, 203 C. australis Planch, 203 C. garrawayae F. M. Bailey, 203 C. glauca (Lindl.) Burkill, 203 C. gracilis Mabb., 203 C. inodora F. M. Bailey, 203 C. maideniana (Domin.) Swingle, 203 C. warburgiana, 203 C. wintersii, 203 harvest season, 204205 physiology, 204205 Clausena lansium. See Wampee (Clausena lansium) Cocoa honey, 72 Cocona (Solanum sessiliflorum), 153, 154f agronomical aspects, 156157 challenges related to production, 157 composition of, 155156, 155t carotenoids and phenolic compounds, 156 volatile compounds, 156 fruit color, 154155 germination of, 156157 origin and distribution, 153155 planting densities for, 157 protective effect of, 157 susceptibility to fungal and bacterial attacks, 157 uses and perspectives, 157 as a component of juices, jelly, liquor, 157 as food additives, 157 juice for cosmetic purposes, 157 Cocos nucifera, 383 Cupuassu (Theobroma grandiflorum), 72, 159, 160f antioxidant properties of, 160 chemical composition and nutritional value, 160 ascorbic acid, 160 pectin content, 161 protein and lipid content, 160 vitamins and minerals, 160 in chocolate products, 161 flowering and fruiting, 159160 harvest and postharvest conservation, 161 industrial applications, 161 industrial process, 161f origin and botanical aspects, 159160
461
pulp, 160161 seeds, 160 liquors of, 160 processing of, 161 Cupulate, 159 Custard apple (Annona squamosa L.), 163 botanical description, 163164 ethnomedicinal uses, 164t antiinflammatory, antimicrobial and cytotoxic activity, 165 antithyroidal activity of, 165 vasorelaxant effect, 165 harvest and postharvest conservation, 166 industrial applications, 166 origin and distribution, 163 phytochemistry, 165166 in production of silver nanoparticles, 166 pulp, 165 nutrient composition of, 165t seeds, 166 storage and shelf life of, 166 total production and market, 164 uses dietary, 164 in traditional medicine, 164165 wine, 166 Cydonia oblonga. See Quince (Cydonia oblonga)
D Dacryodes edulis. See Safou (Dacryodes edulis) Diopyros kaki. See Caqui (Diopyros kaki) Diospyros species D. ebenum, 113 D. kaki. See Caqui (Diopyros kaki) D. oleifera, 113 D. virginiana, 113 Durian (Durio zibethinus), 387 antioxidant properties, 173174 aril, 177 chemical composition and nutritional value carbohydrates of, 174 carotenoids in, 174 fatty acid composition, 173174 vitamins and minerals, 173 volatile compounds in, 175 as a climacteric fruit, 169 cultivar origin and botanical aspects, 169170 estimated annual production, 170 expansin genes in, 171, 173 fruit physiology and biochemistry, 170173 color development, 171, 172f dehiscence, 172173 ethylene production, 170171 respiration, 170 softening of, 171 weight loss, 172 harvesting, 175 harvest season, 175 health properties, 174 industrial application of, 176177
462
Subject Index
Durian (Durio zibethinus) (Continued) fresh fruit, 176 husks, 177 products, 177 1-MCP (1-methylecyclopropene) treatment and, 176 physical and chemical properties, 177 ripening, 175176 sensory properties of, 174175 storage of, 176 sugar content in pulp of, 174 waxing or surface coating of, 176 Durio zibethinus. See Durian (Durio zibethinus)
E Elaeis guineensis, 383 Elderberry (Sambucus nigra L.), 182f allergic reactions of, 185 applications, 184185 as an immune booster, 185 against diabetes, 185 in herbal medicine, 185 to prepare jams, pies, and sauces, 182183 aroma compounds, 183184 biochemical and physiology, 183 amino acid content, 183 sambunigrin and prunasin, 183 titratable acid content, 183 characteristic aroma of, 184 chemical composition and nutritional value, 183184, 184t cultivars, 181 estimated production of, 182183 flowers of, 181, 182f fruits, 183f origin and botanical aspects, 181 postharvest of, 182 Embrapa Western Amazon breeding program, 234 Eriobotrya japonica Lindl. See Loquat/Nispero (Eriobotrya japonica Lindl.) Ethylene, 40 Eugenia brasiliensis Lam. See Grumixama (Eugenia brasiliensis Lam.) Eugenia dysenterica. See Cagaita (Eugenia dysenterica) Eugenia pyriformis Cambess. See Uvaia (Eugenia pyriformis Cambess) Eugenia uniflora L. See Pitanga (Eugenia uniflora L.) Euterpe oleracea Mart. See Ac¸aı´ (Euterpe oleracea Mart.)
F FAPEAM (Amazonas State Research Support Foundation), 232 Figo da india (Opuntia spp.) amino acids, 192 betalains in, 193t, 194t cultivation and harvest, 190
fruit characteristics, 188190 harvesting and conservation process, 195196 industrial applications, 197199 colonche, 198 dehydrated products, 198 fudge and cheese, 198 juice and nectar production, 197 minimal processing, 198199 pigments, 199 prickly pear products, 197t used for jams, jellies, and candies, 197198 minerals, 192 nutraceutical characteristics of cultivars, 194t nutritive characteristics, 191192, 192t origin, 187 phenolic compounds and antioxidant activity, 193, 193t physicochemical characteristics of, 189t physicochemical composition, 191 pigments, 194 postharvest conservation, 196197 modified atmosphere for packaging fruits, 196197 refrigeration, 196 respiration characteristics, 191 sensory characteristics, 195 taxonomy, 187188 vitamins, 192, 193t volatile compounds, 194195, 195t Finger lime/The Australian Caviar (Citrus australasica), 204f, 205f antioxidant capacity, 206208, 207t chemical composition of the peel, 206 cultivated varieties, 208209 harvest season, 204205 hybrids, 209 hydrophilic compounds, 208 lipophilic compounds, 208 nutritional value, 206208 phenol content, 208 physiology, 204205 production and industrial applications, 208209 sensory characteristics and volatile composition, 206 Flavonoid O-glucosides, 64 Fortunella japonica. See Kumquat (Fortunella japonica)
fruit physiology and biochemistry, 213214 harvest and postharvest conservation, 215217 effect of precooling, 217 hand, 217 machine, 217 harvest season, 212213, 213f industrial application, 217 market potential, 217218 origin and botanical aspects, 211212 ripening and physico-chemical changes, 213 sensory characteristics, 215 Grumixama (Eugenia brasiliensis Lam.), 219, 220f antioxidant capacity, 222 bioactive compounds of, 221 carotenoids, 221, 223t chemical composition of purple and yellow, 219, 220t ellagitannin content of, 220221 harvest season and production, 222 industrial applications, 223 as natural dye, 223 medicinal properties of, 222 nutritional composition, 219 phenolic compounds in, 222t phytochemical profile, 220222, 221t plant, 219 Guarana (Paullinia cupana Kunth var. sorbilis (Mart.) Ducke), 225, 227f, 230f breeding, 233 estimated annual production, 228229, 228f flowering and pollination, 227228 future prospects, 235 genetic improvement methods, 233235 clonal selection, 234 Expressed Sequence Tags (EST) for guarana fruits and seeds, 232 mass selection, 233234 plantpathogen interaction pathways, 235 plant selection with progeny testing, 234 recurrent intraspecific selection, 234 sequencing of transcripts, 235 genetic resource conservation, 229230, 231t genomic structure and organization, 229, 233 harvest season, 227228 origin and botanical aspects, 225227 phenotypic variability, 230232 seed productivity, 233
G
H
Garcinia mangostana. See Mangosteen (Garcinia mangostana) Genetic diversity index, 234 Gooseberry (Ribes grossularia L./Ribes uvacrispa), 212f chemical composition and nutritional value, 215, 216t as a natural source of organic acids, 215 classification of, 211212 cultivars, 211212 estimated annual production, 214215, 214t
Hancornia speciosa Gomes. See Mangaba (Hancornia speciosa Gomes) Hylocereus guatemalensis, 339 Hylocereus megalanthus, 343 Hylocereus monacanthus, 342343 Hylocereus polyrhizus, 339 Hylocereus undatus, 339343 Hylocereus undatus (Haw). See Pitaya (Hylocereus undatus (Haw)) Hymenaea courbaril L. See Jatoba (Hymenaea courbaril L.)
Subject Index
J Jabuticaba hı´brida (Myrciaria cauliflora), 238 Jabuticaba (Myrciaria spp.), 238f anthocyanin contents, 240 antimicrobial properties, 242 antioxidant properties, 240 chemical composition and nutritional value, 240241 calcium content, 241 content of, 238t estimated annual production, 239 fruit peel and seed, 240 fruit physiology and biochemistry, 239240 fruit pulp, 240 harvest and postharvest conservation, 241 harvest season, 239 industrial applications, 242 in jellies and jams, 242 origin and botanical aspects, 237238 phenolic compounds, 240 Jabuticaba Sabara´ (Myrciaria jaboticaba), 237238 Jackfruit (Artocarpus heterophyllus), 122, 385, 415, 417 Jambo (Syzygium malaccense), 246f botanical aspects, 245 chemical composition and nutritional value, 247248, 247t anthocyanin content, 248 of skin, 247t volatile constituents, 247, 248t common names, 245 harvest and postharvest conservation, 246 harvest season, 245 industrial application, 248 sensory characteristics, 248 Jambolan (Syzygium jambolanum), 251 astringency aspect of, 254 biological properties, 253254 chemical composition and nutritional value, 252254, 253t anthocyanins, 252253 fruit physiology and biochemistry, 251252 harvest and postharvest conservation, 254 harvest season, 251 industrial applications, 254 as juices, pulps, and jellies, 254 origin and botanical aspects, 251 scientific and popular names, 252f, 252t sensory characteristics, 254 shelf-life, 254 Jatoba (Hymenaea courbaril L.) activities of cyclooxygenase (COX) enzymes and lipid peroxidation, 260 chemical composition and nutritional value, 260 commercial use of, 257258 estimated annual production, 259260 flowering of, 259 fruits, 257259, 259f geographical distribution of, 257 harvest/postharvest conservation, 259260 harvest season of, 259 industrial applications, 260261
flour, 258259 in food conservation and agricultural defensives, 261 inhibitory activity against Escherichia coli, 261 of pulp and seed’s oil, 260 as a medicinal plant, 258 nutritive and sweet fruits of, 257 origin and biological aspects, 257259 seedling, 258f sensory characteristics, 260 Jujuba (Ziziphus jujuba Mill.), 264f chemical composition and nutritional value, 265266 alkaloids, 265 cyclopeptide alkaloids, 265 flavonoids, 266 glycosides, 265 phenolic compounds, 266 saponins, 265 terpenoids, 266 vitamins, 266 estimated annual production, 265 flowers, 263 fruit physiology and biochemistry, 265 harvest and postharvest conservation, 266267 industrial applications, 267268 candied jujube, 267 dry dates, 267 jam, 268 juice, wine, and vinegar, 268 paste, 268 roasted product, 267 smoked product, 267 spirited juice, 267 origin and botanical aspects, 263
K Kapundang (Baccaurea racemosa), 387 Kumquat (Fortunella japonica), 272f, 273f, 274f antiageing activity of, 276 botany and anatomy, 271272 classification, 271 essential oils, 275 free radical scavenging mechanism of, 275276 fresh and processed products, 276 carotenoids composition, 275 in confectionery industry, 276 phenolic and flavonoid contents of, 275, 275 secondary metabolites, 275 vitamin composition, 275 important cultivated species, 271 nutritional composition, 274276 origin and distribution, 271 postharvest physiology and storage, 272274 shelf-life, 273 in ultraviolet (UV) treatment, 274
463
L Langsat (Lansium domesticum), 281f antimicrobial activity, 283 chemical compositions and nutritional values, 280281, 282t estimated annual production, 280 harvest and postharvest conservation, 282 harvest season, 280 industrial application, 282283 as a rich source of limonoids, 283 origin and botanical aspects, 279280 common names, 279 flower, 279 fruit, 280 leaflet, 279 seeds, 280 varieties, 279 sensory characteristics, 281 Lansium domesticum. See Langsat (Lansium domesticum) Lemon caviar. See Finger lime/The Australian Caviar (Citrus australasica) Limonia acidissima L. See Wood apple (Limonia acidissima L.) Litchi chinensis. See Lychee (Litchi chinensis) Loquat/Nispero (Eriobotrya japonica Lindl.) fruits, 285, 287f industrial and medicinal uses, 289290 nutritional composition of, 287, 288t phenolic and antioxidant capacity, 288 physicochemical compounds in, 289 postharvest and nutritional value, 286288 postharvest conservation, 288289 pulp, 287 leaves, 289290 origin and botanical aspects, 285 production, 285286 Lychee (Litchi chinensis), 385
M Maboque/monkey orange (Strychnos spinosa), 294f industrial uses, 295 origin, 293 physicochemical composition, 294, 295t trans-isoeugenol, 294 postharvest and physiology, 293294 sensory characterization, 294 volatile compounds of, 293294, 295t Macauba palm (Acrocomia aculeata), 298f botanical and production aspects of, 298 common names, 297 fruit components of, 300301, 301t flavonoid content, 302 phenolic content, 302 powder, 301 preservation of, 300 pulp and seeds, 299f vitamin C content, 300, 302 fruit pulp and seeds, 297 preservation of, 298300
464
Subject Index
Macauba palm (Acrocomia aculeata) (Continued) drying process, 299302, 302t Magellan barberry, 133 Malpighia emarginata D.C. See Acerola (Malpighia emarginata D.C.) Maltodextrin, 299300 Mangaba (Hancornia speciosa Gomes) antioxidant activity, 309 botanical aspects, 305306 chemical composition and nutrition, 308309, 310t bioactive compounds, 311t phenolic compounds, 309311 vitamin C content, 309, 311t cultivation and harvest, 306 fruit development, 307308 gas exchange and photosynthetic activities of, 307 origin and production, 305 physical characteristics, 308t physiology and biochemistry, 307 volatile compounds, 311316, 312t effects of storage on, 316 water deficit tolerance mechanisms, 307, 307 Mangifera indica L. See Mango (Mangifera indica L.) Mango (Mangifera indica L.), 385386 Mangosteen (Garcinia mangostana), 385, 387 Matoa (Pometia pinnata), 387 Mauritia flexuosa. See Buriti fruit (Mauritia flexuosa) Megalopta sodalis, 92 Megommation insigne, 92 Microencapsulation, 28 Modified atmosphere packaging (MAP), 359 Monkey orange. See Maboque/monkey orange (Strychnos spinosa) Monoecious species, 1. See also Ac¸aı´ (Euterpe oleracea Mart.) Morinda citrifolia Linn. See Noni (Morinda citrifolia Linn) Murtilla fruits, 133134 antioxidant properties, 134 linoleic acid levels, 133 polyphenols level in, 134 Murtilla leaves, 134 antioxidant properties, 134 chemical composition, 134 tannins of, 134 Myrciaria cauliflora. See Jabuticaba hı´brida (Myrciaria cauliflora) Myrciaria dubia (Kunth) McVaugh. See Camucamu (Myrciaria dubia (Kunth) McVaugh) Myrciaria jaboticaba. See Jabuticaba Sabara´ (Myrciaria jaboticaba) Myrciaria spp. See Jabuticaba (Myrciaria spp.) Myrthaceae, 129 Myrtus ugni. See Chilean Guava (Myrtus ugni)
N Nanoencapsulation, 28 National Tropical Botanical Garden (NTBG), 5455 Nephelium lappaceum Linn. See Rambuta˜n (Nephelium lappaceum Linn.) Noni (Morinda citrifolia Linn), 320f, 321f chemical constituents of the leaf, flower, root and bark, 323 cultivation practices and harvest, 319321 (2E,4Z,7Z)-decatrienoic acid (DTA) content of, 323 fruit juice, 322 industrial uses, 323324 against mosquitoes, 324 as a natural preservative, 323 as a source of natural reagents for flow injection spectrophotometric technique, 323324 larvicidal and pupicidal activities, 324 nutritional value, 322323, 322t origin and botanical aspects, 319 recognized varieties of, 319 seeds, 319 skin color and firmness, 321t volatile compounds of, 323 Nypa fruticans, 383
O Oleic acid, 40 Opuntia amyclaea carbon dioxide and ethylene production during respiration rate of, 191t physical and compositional changes, 190t Opuntia spp. See Figo da india (Opuntia spp.)
P Papaya (Carica papaya L.), 387 Paullinia cupana Kunth var. sorbilis (Mart.) Ducke. See Guarana (Paullinia cupana Kunth var. sorbilis (Mart.) Ducke) Persea americana. See Avocado (Persea americana) Persea schiedeana, 37 Persimmon tree, 113, 114f astringency of, 116 cultivars, 114 estimated annual production, 114, 115t fruit chemical composition and nutritional value, 116 physical and chemical changes during fruit ripening, 115 physiology and biochemistry, 115116 harvest and postharvest conservation, 117 harvest season, 114 industrial application, 117 as dry fruit, 117 vinegar and hard liquor production, 117 phenolic and polyphenolic composites, 116 “Rojo Brillante” persimmon species, 116 sensory characteristics, 116117
Pidada (Sonneratia caseolaris), 328f chemical composition and nutritional value, 328329, 329t antidiabetic activity, 329 antioxidant properties, 329, 330t phytochemical constituents of bark, 328 decline of, 330 environmental benefits, 330 fruit physiology and biochemistry, 328 habitat, 331f harvest and postharvest conservation, 330 harvest annual production, 327 industrial application, 330331 origin and botanical aspects, 327 sensory characteristics, 329 types, 327 Pitanga (Eugenia uniflora L.), 335f antioxidant properties of, 337 chemical composition and nutritional value, 335336, 336t carotenoids, 336 vitamin C content, 335336 harvest and postharvest conservation, 337 harvest season, 334335 industrial application, 337 in cosmetic industry, 337 juice and liqueurs of, 337 orange fruit, 334f origin and botanical aspects, 333334 purple fruit, 335f red fruit, 334f sensory characteristics, 336337 therapeutic properties of, 337 Pitaya (Hylocereus undatus (Haw)) chemical composition and nutritional value, 342343, 342t estimated annual production, 340, 341t fruit physiology and biochemistry, 341342 harvest and postharvest conservation, 343345 packing system, 344 from pests and diseases, 345 quarantine requirements, 345 harvest season, 340, 340t industrial applications, 345346 as commercial thickeners, 346 medicinal uses, 346 origin and botanical aspects, 339340 sensory characteristics, 343 Pitomba (Talisia esculenta), 352f antiproliferative and antimutagenic activities of, 352353 botanical aspects, 351 chemical composition and nutritional value, 351353, 352t phenolic compounds, 353t volatile organic compounds of, 352353 estimated annual production, 351 harvest season, 351 industrial applications, 353 Platonia insignis. See Bacuri (Platonia insignis) Plumbago zeylanica, 166 Pneumatophores, 330331
Subject Index
Pomegranate/Roma (Punica granatum), 356f chemical composition and nutritional value, 358 estimated annual production, 357, 357t as flavoring and coloring agents, 360 fruit physiology and biochemistry, 358 harvest and postharvest conservation, 358359 harvest season, 357 industrial applications, 360 for making jams, jelly, and sauce, 360 minimally processed or ready-to-eat, 360 origin and botanical aspects, 355356 problems associated under suboptimal conditions, 359 storage, 359 Pometia pinnata. See Matoa (Pometia pinnata) Pouteria campechiana (Kunth) Baehni. See Canistel (Pouteria campechiana (Kunth) Baehni) Protocatechuic acid, 64 Psidium cattleyanum. See Arac¸a´ (Psidium cattleyanum) Ptiloglossa latecalcarata, 92 Public Health Security and Bioterrorism Preparedness and Response Act of 2002, 58 Punica granatum. See Pomegranate/Roma (Punica granatum)
Q Quince (Cydonia oblonga), 364f cultivates, 364 estimated annual production, 363364 industrial application, 366 in marmalades, jams, and jellies, 366 medicinal properties, 366 origin and botanical aspects, 363 postharvest conservation, 366 postharvest physiology and nutritional value, 364366, 365t carotenoids, 365366 phenolic compounds, 365 phytochemical compounds, 365 pulp, 364
R Rambai (Baccaurea motleyana), 385387 Rambuta˜n (Nephelium lappaceum Linn.), 385 antioxidant compounds, 371372 browning and disease control, 373 cultivars and harvest season, 370371 growing behavior and management, 371 harvest and postharvest physiology, 372 leaf and flower, 370f morphological characteristics, 369 nutritional component, 371 origin, 369 peel application antioxidant activity, 373 green synthetic strategy, 373 preparation of activated carbon, 373
polyamine concentrations, 372 postharvest conservation, 373 postharvest handling and storage condition, 373 seed application antibacterial activity, 374 seed fat composition, 374 seedling propagation and vegetative propagation, 371 sensory characteristics, 371, 372f REALGENE (Legal Amazonia Network for Genomic Research), 232, 235 Ribes grossularia L. See Gooseberry (Ribes grossularia L./Ribes uva-crispa) Ribes uva-crispa. See Gooseberry (Ribes grossularia L./Ribes uva-crispa)
S Safou (Dacryodes edulis), 378f chemical composition and nutritional value, 377378 composition, 379t oil, 379t, 380 volatile compounds of, 380 harvest season, 380 industrial applications, 380381 as a good dietetic food, 380 as jams and jellies, 380 origin and botanical aspects, 377 sensory characteristics, 378380 shelf-life, 380 Salacca zalacca. See Salak (Salacca zalacca) Salak (Salacca zalacca), 384f agro-tourism of Salak Sibetan plantation, 389 antihyperuricemic activity, 388 antioxidant activities, 387, 387t antiproliferative activity, 388 appearance, 383 conservation, 388 estimated annual production, 385 genus, 383 germplasm and plants, 388 harvest season, 385 immunostimulatory activity, 387 industrial applications, 388389 morphology and physiology, 384385 nutritional composition, 385, 386t origin and botanical aspects, 383 phytochemicals, 385386 sensory and physicochemical characteristics, 388 skin and kernel, uses of, 389 volatile constituents, 386, 387t Sambucus canadensis, 181 Sambucus nigra L. See Elderberry (Sambucus nigra L.) Solanum sessiliflorum. See Cocona (Solanum sessiliflorum) Solanum species S. betaceum (tamarillo), 153 S. lycopersicum L. (tomato), 153
465
S. muricatum Alt. (pepino or melon shrub), 153 S. quitoense Lam., 153 S. quitoense Lam. (naranjilla or lulo), 153 S. sessiliflorum. See Cocona (Solanum sessiliflorum) S. tuberosum L. (potato), 153 Sonneratia caseolaris. See Pidada (Sonneratia caseolaris) Soursop (Annona muricata), 72, 387, 392f chemical and nutritional composition, 393394, 393t estimated annual production, 392393 harvest and postharvest conservation, 394 harvest season, 392 industrial applications, 395 medicinal properties, 395 origin and distribution, 391 quality and size, factors influencing, 394 ripening process, 394 sensory characteristics, 394 taxonomy and botanical description, 391392 Spondias cytherea. See Ambarella (Spondias cytherea) Spondias purpurea. See Ciruela/Mexican plum (Spondias purpurea L.) Spondias tuberosa. See Umbu (Spondias tuberosa) Strawberry (Fragaria x annanassa), 213 Strychnos spinosa. See Maboque/monkey orange (Strychnos spinosa) Sugar apple (Annona squamosa Linn.), 385, 397, 399f botanical aspects, 398 chemical composition, 400401, 401t common names, 397 cultivar origin, 397 description, 398400 estimated annual production, 400 harvest and postharvest conservation, 401402 harvest season, 400 industrial application, economic value, 402 fuel wood, 402 phytochemical examinations of, 400 sensory characteristics, 401402 vermicidal and insecticidal properties of, 402 Syzygium cumini species. See Jambolan (Syzygium jambolanum) Syzygium jambolanum. See Jambolan (Syzygium jambolanum) Syzygium malaccense. See Jambo (Syzygium malaccense)
T Talisia esculenta. See Pitomba (Talisia esculenta) Tamarindo (Tamarindus indica L.) chemical composition, 406, 407t coppicing ability of, 409410 cultivars, 407, 407t distribution and habitat, 404
466
Subject Index
Tamarindo (Tamarindus indica L.) (Continued) in farming systems, 409 as firebreak, 409 as fodder species, 409 food value, 406 general description, 404407, 405f harvesting and storage, 406407 household uses, 408 industrial uses, 408409 as adhesive filler, 409 production of TKP, 409 medicinal properties, 408 as a nontraditional fruit tree, 403 pollination of, 405 postharvest uses, 407409 propagation and conservation, 409410 seedling growth, 405 seed germination and, 409 as shade tree, shelter belt, and wind breaks, 409 taxonomy of, 403 local names, 404t Tamarindus indica L. See Tamarindo (Tamarindus indica L.) Tarap (Artocarpus odoratissimus), 414f, 415f antioxidant activity, 417t chemical composition and nutritional value, 415417, 416t estimated annual production, 414 fruit physiology and biochemistry, 415 harvest and postharvest conservation, 417 harvest season, 414 industrial applications, 418 as a flavoring agent in ice cream, 418 in jam and syrup bases, 418 as a low-cost biosorbent for the removal of toxic dyes, 418 metabolites in, 416417 mineral content, 415 origin and botanical aspects, 413 sensory characteristics, 417 Tetraterpenoids, 64 Theobroma cacao L. See Cacao (Theobroma cacao L.)
Theobroma grandiflorum. See Cupuassu (Theobroma grandiflorum) Tucuma˜ of Amazonas (Astrocaryum aculeatum) carotenids in, 421t estimated annual production, 419420 fruit physiology and biochemistry, 420421 harvest season, 419 origin and botanical aspects, 419 phenolic composition and flavonoid of, 421t uses and applications, 422 in vitro studies, 422424 alkaloid compounds, 423 antioxidant properties, 422423 beneficial effects of, 422 genotoxic response, 422 as a major source of gallic acid, 423 protective effect on DNA damage in lymphocytes, 423424
U Ugni molinae Turcz., 129, 132t forms of flavonols, saponins, and tannins, 135 infuses, antioxidant activity of, 135 leaves, antioxidant activity of, 135 oxygen radicals absorption capacity (ORAC) value of, 135 phenol contents, 135 tea elicits, antioxidant activity of, 135137, 136f, 137f, 138f Umbu (Spondias tuberosa), 427, 430f, 430t antioxidant activity, 431 chemical composition and nutritional value, 429431 volatile compounds, 431 estimated annual production, 429 fruit development cycle, 429 genetic variation, 428429, 428t harvest and postharvest conservation, 431 harvesting season, 429 industrial applications, 431432 liquor, 432 origin and botanical aspects, 427
pulp, 432 sensory characteristics, 431 Uvaia (Eugenia pyriformis Cambess) chemical composition, 436 estimated annual production, 436 fruit physiology and biochemistry, 436 harvest and postharvest conservation, 436437 harvest season, 435 industrial application, 437 nutritional quality, 436 origin and botanical aspects, 435 sensory characteristics, 436
W Wampee (Clausena lansium), 440f antinflammatory effects, 439440, 440 aroma of, 441 composition and uses, 439441 fermented fruit juice, 441 harvest season, 439 leaves, 441 medicinal properties, 440 origin and botanical aspects, 439 Wood apple (Limonia acidissima L.), 444f, 445f chemical composition and nutritional value, 444 composition and micronutrients, 445t food uses, 446 as beverages and desserts, 446 as jam, jelly, chutney, fruit bars, 446 juice, 446 fruit physiology and biochemistry, 443 harvest and postharvest conservation, 444 medicinal uses, 444446 origin and botanical aspects, 443
Z Zikanapis seabrai, 92 Ziziphus jujuba Mill. See Jujuba (Ziziphus jujuba Mill.)