Rice insect pests and their management 9781786761965, 1786761963

Table of contents :
Contents
Series list
Introduction
References
Chapter 1 Biology and ecology of rice-feeding insects: root and stem feeders
1.1 Introduction
1.2 Mole cricket, Gryllotalpa africana Palisot de Beauvois (Orthoptera: Gryllotalpidae)
1.3 Root aphids, Tetraneura nigriabdominalis (Sasaki)
1.4 Rice root aphid, Rhopalosiphum rufiabdominale (Sasaki) (Hemiptera: Aphididae)
1.5 Rice mealybug, Brevennia rehi (Lindinger) (Homoptera: Pseudococcidae)
1.6 Black bugs, Scotinophara coarctata (Fabricius), S. lurida (Burmeister) (Fig. 1.5), S. latiuscula Breddin, and S. sorsogonensis Barrion, Joshi, Barrion-Dupo & Sebastian (Hemiptera: Pentatomidae)
1.7 Rice stalk stink bug, Tibraca limbativentris (Stål) (Hemiptera: Pentatomidae)
1.8 Chinch bug, Blissus leucopterus leucopterus (Say) (Hemiptera: Blissidae)
1.9 Rice seed midges, Cricotopus sylvestris (F.), Paralauterborniella subcincta and Paratanytarsus sp. (Diptera: Chironomidae)
1.10 Rice stem maggot, Chlorops oryzae Matsumura (Diptera: Chloropidae)
1.11 Rice seedling flies, Atherigona exigua Stein and Atherigona oryzae Malloch (Diptera: Muscidae)
1.12 Black beetles, Heteronychus mossambicus Peringuey (= H. oryzae Britton); Coleoptera: Scarabaeidae: Dynastinae
1.13 ‘Chafers’ (white grubs), Leucopholis irrorata (Coleoptera: Scarabaeidae, Melolonthinae)
1.14 Colaspis beetles, Colaspis brunnea and Colaspis louisianae (Say) (Coleoptera: Chrysomelidae)
1.15 Rice root weevil, Echinocnemus oryzae Marshall (Coleoptera: Curculionidae)
1.16 Rice plant weevil, Echinocnemus squameus Billberg (Coleoptera: Curculionidae)
1.17 Paddy root weevil, Hydronomidius molitor Faust (Coleoptera: Curculionidae)
1.18 Rice water weevil (Lissorhoptrus oryzophilus Kuschel) (Coleoptera: Curculionidae)
1.19 Gorgulho aquático do arroz (Oryzophagus oryzae)
1.20 Rice water weevil (Afroryzophilus djibai Lyal) (Coleoptera: Curculionidae)
1.21 African subterranean termites, Macrotermes (Macrotermes bellicosus (Smeathman), Pseudacanthotermes militaris (Hagen)); Microtermes (Microcerotermes parvus (Haviland), Armitermes evuncifer Silvestri, Trinervitermes oeconomus (Tragardh)) (Isoptera: Te
1.22 South American root-feeding termites, Procornitermes triacifer, P. araujoi and Syntermes molestus (Isoptera: Termitidae)
1.23 References
1.2 Mole cricket, Gryllotalpa africana Palisot de Beauvois (Orthoptera: Gryllotalpidae)
1.3 Root aphids, Tetraneura nigriabdominalis (Sasaki)
1.4 Rice root aphid, Rhopalosiphum rufiabdominale (Sasaki) (Hemiptera: Aphididae)
1.5 Rice mealybug, Brevennia rehi (Lindinger) (Homoptera: Pseudococcidae)
1.6 Black bugs, Scotinophara coarctata (Fabricius), S. lurida (Burmeister) (Fig. 1.5), S. latiuscula Breddin, and S. sorsogonensis Barrion, Joshi, Barrion-Dupo & Sebastian (Hemiptera: Pentatomidae)
1.7 Rice stalk stink bug, Tibraca limbativentris (Stål) (Hemiptera: Pentatomidae)
1.8 Chinch bug, Blissus leucopterus leucopterus (Say) (Hemiptera: Blissidae)
1.9 Rice seed midges, Cricotopus sylvestris (F.), Paralauterborniella subcincta and Paratanytarsus sp. (Diptera: Chironomidae)
1.10 Rice stem maggot, Chlorops oryzae Matsumura (Diptera: Chloropidae)
1.11 Rice seedling flies, Atherigona exigua Stein and Atherigona oryzae Malloch (Diptera: Muscidae)
1.12 Black beetles, Heteronychus mossambicus Peringuey (= H. oryzae Britton); Coleoptera: Scarabaeidae: Dynastinae
1.13 ‘Chafers’ (white grubs), Leucopholis irrorata (Coleoptera: Scarabaeidae, Melolonthinae)
1.14 Colaspis beetles, Colaspis brunnea and Colaspis louisianae (Say) (Coleoptera: Chrysomelidae)
1.15 Rice root weevil, Echinocnemus oryzae Marshall (Coleoptera: Curculionidae)
1.16 Rice plant weevil, Echinocnemus squameus Billberg (Coleoptera: Curculionidae)
1.17 Paddy root weevil, Hydronomidius molitor Faust (Coleoptera: Curculionidae)
1.18 Rice water weevil (Lissorhoptrus oryzophilus Kuschel) (Coleoptera: Curculionidae)
1.19 Gorgulho aquático do arroz (Oryzophagus oryzae)
1.20 Rice water weevil (Afroryzophilus djibai Lyal) (Coleoptera: Curculionidae)
1.21 African subterranean termites, Macrotermes (Macrotermes bellicosus (Smeathman), Pseudacanthotermes militaris (Hagen)); Microtermes (Microcerotermes parvus (Haviland), Armitermes evuncifer Silvestri, Trinervitermes oeconomus (Trag
1.22 South American root-feeding termites, Procornitermes triacifer, P. araujoi and Syntermes molestus (Isoptera: Termitidae)
1.23 References
Chapter 2 Biology and ecology of rice-feeding insects: stem borers and rice gall midges
2.1 Introduction
2.2 Stalk-eyed borer, Diopsis longicornis Macquart (Diptera: Diopsidae)
2.3 Stalk-eyed fly, Diopsis apicalis Dalman (Diptera: Diopsidae)
2.4 Gold-fringed rice borer, Chilo auricilius Dudgeon (Lepidoptera: Pyralidae)
2.5 Dark-headed stem borer, Chilo polychrysus (Meyrick) (Lepidoptera: Crambidae)
2.6 Spotted stem borer, Chilo partellus (Swinh.) (Lepidoptera: Pyralidae)
2.7 American rice stalk borer, Chilo plejadellus Zincken (Lepidoptera: Pyralidae)
2.8 Rice striped borer, Chilo suppressalis (Walker) (Lepidoptera: Pyralidae)
2.9 African striped rice borer, Chilo zacconius Bleszynski (Lepidoptera: Pyralidae)
2.10 African white borer, Maliarpha separatella Ragonot; (Lepidoptera: Pyralidae)
2.11 Yellow stem borer, Scirpophaga incertulas (Walker) (Lepidoptera: Pyralidae)
2.12 White stem borer, Scirpophaga innotata (Walker) (Lepidoptera: Pyralidae)
2.13 African pink borer, Sesamia calamistis Hampson (Lepidoptera: Noctuidae)
2.14 African pink borer, Sesamia nonagrioides botanephaga Tams and Bowden; (Lepidoptera: Noctuidae)
2.15 Asiatic pink stem borer, Sesamia inferens Walker (Lepidoptera: Noctuidae)
2.16 South American white borer, Rupela albinella (Cram.) (Lepidoptera: Schoenobiidae)
2.17 Sugarcane borer, Diatraea saccharalis (Fabricius) (Lepidoptera: Pyralidae)
2.18 Lesser cornstalk borer (LCB), Elasmopalpus lignosellus (Zeller) (Lepidoptera: Pyralidae)
2.19 Mexican rice borer, Eoreuma loftini (Dyar) (Lepidoptera: Crambidae)
2.20 Asian rice gall midge, Orseolia oryzae (Wood-Mason) (Diptera: Cecidomyiidae)
2.21 African rice gall midge, Orseolia oryzivora Harris and Gagne (Cecidomyiidae: Diptera)
2.22 References
Chapter 3 Biology and ecology of rice-feeding insects: leafhoppers and planthoppers
3.1 Introduction
3.2 White rice leafhoppers, Cofana spectra (Distant) and C. unimaculata (Signoret) (Hemiptera: Cicadellidae)
3.3 Green leafhoppers, Nephotettix spp. (Homoptera: Cicadellidae)
3.4 Nephotettix afer Ghauri and Nephotettix modulatus Melichar (Hemiptera: Cicadellidae)
3.5 Nephotettix nigropictus (Stål) (Hemiptera: Cicadellidae)
3.6 Nephotettix cincticeps (Uhler) (Hemiptera: Cicadellidae)
3.7 Nephotettix virescens (Distant) (Hemiptera: Cicadellidae)
3.8 Nephotettix malayanus Ishihara et Kawase (Hemiptera: Cicadellidae)
3.9 Zigzag leafhopper, Recilia dorsalis (Motschulsky) (Homoptera: Cicadellidae)
3.10 Smaller brown planthopper, Laodelphax striatellus (Fallen) (Homoptera: Delphacidae)
3.11 Brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae)
3.12 White-backed planthopper, Sogatella furcifera (Horvath) (Homoptera: Delphacide)
3.13 Rice delphacid, Tagosodes orizicolus (Muir) (Homoptera: Delphacidae)
3.14 Rice delphacid, Tagosodes cubanus (Crawford) (Hemiptera: Delphacidae)
3.15 Spittlebugs, Locris maculata maculata Fabricius and L. rubra Fabricius (Hemiptera: Cercopidae)
3.16 Spittlebugs (Cigarrinha das pastagens), Deois flavopicta Stål (Hemiptera: Cercopidae)
3.17 References
Chapter 4 Biology and ecology of rice-feeding insects: foliage feeders
4.1 Introduction
4.2 Large rice grasshoppers, Hieroglyphus banian (Fabricius) and Hieroglyphus nigrorepletus  (I. Bol.) (Orthoptera: Acrididae)
4.3 Rice grasshopper, Hieroglyphus daganensis Krauss (Orthoptera: Acrididae) 
4.4 Short-horned grasshoppers, Oxya spp. (Orthoptera: Acrididae)
4.5 Variegated grasshoppers, Zonocerus variegatus (L.) (Orthoptera: Pyrgomorphidae)
4.6 Meadow grasshoppers, Conocephalus spp. (Orthoptera: Tettigoniidae)
4.7 Whitefly, Aleurocybotus indicus David and Subramaniam (Hemiptera: Aleyrodidae)
4.8 Rice whitefly, Aleurocybotus occiduus Maria (Hemiptera: Aleyrodidae) 
4.9 Spider mites, Oligonychus pratensis Banks, O. senegalensis Gutierrez and Etienne, O. oryzae Hirst and Tetranychus neocaledonicus Andre (Acari: Tetranychidae)
4.10 Rice thrips, Stenchaetothrips biformis (Bagnall) (Thysanoptera: Thripidae)
4.11 Rice leaffolder, Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae) 
4.12 Rice leaffolder, Marasmia patnalis (Bradley) (Lepidoptera: Pyralidae)
4.13 Fijian rice leaffolder, Susumia exigua (Butler) (Lepidoptera: Pyralidae) 
4.14 Rice caseworm, Nymphula depunctalis (Guenée) (Lepidoptera: Pyralidae)
4.15 Green horned caterpillar, Melanitis leda ismene Cramer (Lepidoptera: Satyridae)
4.16 Rice skipper, Parnara guttata (Bremer et Grey) (Lepidoptera: Hesperidiae)
4.17 Rice skipper, Pelopidas mathias (F.) (Lepidoptera: Hesperiidae)
4.18 Rice ear-cutting caterpillar, Mythimna separata (Walker) (Lepidoptera: Noctuidae) 
4.19 The fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae)
4.20 Common cutworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae)
4.21 Rice swarming caterpillar, Spodoptera mauritia (Boisd.) (Lepidoptera: Noctuidae) 
4.22 Common armyworm, Mythimna unipuncta (Haworth) (Lepidoptera: Noctuidae) 
4.23 Rice green semiloopers, Naranga aenescens (Moore) and Naranga diffusa Walker (Lepidoptera: Noctuidae)
4.24 Green hairy caterpillars, Rivula atimeta (Swinhoe) (Lepidoptera: Noctuidae)
4.25 Rice whorl maggot, Hydrellia prosternalis Deeming (Diptera: Ephydridae)
4.26 Rice leaf miner, Hydrellia griseola (Fallen) (Diptera: Ephydridae)
4.27 Rice whorl maggot, Hydrellia philippina Ferino (Diptera: Ephydridae) 
4.28 South American rice miner, Hydrellia wirthi Korytkowski (Diptera: Ephydridae) 
4.29 Leaf miner, Cerodontha orbitona (Spencer) (Diptera: Agromyzidae)
4.30 Paddy stem maggot, Hydrellia sasakii Yausa et Isitani (Diptera: Ephydridae) 
4.31 Asian rice hispa, Dicladispa armigera (Oliver) (Coleoptera: Chrysomelidae)
4.32 African rice hispa, Trichispa sericea (Coleoptera: Chrysomelidae)
4.33 Rice blue beetle, Leptispa pygmaea Baly (Coleoptera: Chrysomelidae) 
4.34 Rice leaf beetle, Oulema oryzae (Kuwayama) (Coleoptera: Chrysomelidae) 
4.35 Flea beetles, Chaetocnema spp. (Coleoptera: Chrysomelidae)
4.36 Ladybird beetle, Chnootriba similis (Mulsant) (Coleoptera: Coccinellidae) 
4.37 Foliage feeding aphids
4.38 References
Chapter 5 Biology and ecology of rice-feeding insects: panicle feeders
5.1 Introduction
5.2 Stink bugs
5.3 Alydid bugs, Stenocoris spp., Mirperus spp., Riptortus dentipes (Hemiptera: Alydidae)
5.4 Rice bugs, Leptocorisa spp. (Hemiptera: Alydidae)
5.5 Stink bugs (Aspavia spp.) (Hemiptera: Pentatomidae)
5.6 Southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae)
5.7 Rice stink bugs, Oebalus spp. (Hemiptera: Pentatomidae)
5.8 Earwigs, Diaperasticus erythrocephalus (Olivier) (Dermaptera: Forficulidae)
5.9 Blister beetles (Coleoptera: Meloidae)
5.10 Panicle thrips, Haplothrips spp. (Thysanoptera: Phlaeothripidae)
5.11 References
Chapter 6 Integrated pest management (IPM) of rice
6.1 Concepts and options for rice IPM
6.2 Cultural practices in rice IPM
6.3 Promoting natural enemies of rice pests: conservation biological control
6.4 Augmentative biological control
6.5 Selective insecticides
6.6 Dissemination mechanisms for rice IPM
6.7 References
Index

Citation preview

http://dx.doi.org/10.0000/00000.0000 © Burleigh Dodds Science Publishing Limited, 2016. All rights reserved.

Rice insect pests and their management

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Related titles: Achieving sustainable cultivation of rice Volume 1 Print: (ISBN 978-1-78676-024-1); Online: (ISBN 978-1-78676-026-5, 978-1-78676-027-2) Achieving sustainable cultivation of rice Volume 2 Print: (ISBN 978-1-78676-028-9); Online: (ISBN 978-1-78676-030-2, 978-1-78676-031-9) Chapters are available individually from our online bookshop: https://shop.bdspublishing.com

BURLEIGH DODDS SERIES IN AGRICULTURAL SCIENCE NUMBER 050

Rice insect pests and their management Professor E. A. Heinrichs, University of Nebraska-Lincoln, USA; Dr Francis E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; Professor Michael J. Stout, Louisiana State University, USA; Dr Buyung A. R. Hadi, The International Rice Research Institute (IRRI), The Philippines; Dr Thais Freitas, Universidade Federal do Rio Grande do Sul, Brazil

Published by Burleigh Dodds Science Publishing Limited 82 High Street, Sawston, Cambridge CB22 3HJ, UK www.bdspublishing.com Burleigh Dodds Science Publishing, 1518 Walnut Street, Suite 900, Philadelphia, PA 19102-3406, USA First published 2017 by Burleigh Dodds Science Publishing Limited © Burleigh Dodds Science Publishing, 2017, All rights reserved. This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission and sources are indicated. Reasonable efforts have been made to publish reliable data and information but the authors and the publisher cannot assume responsibility for the validity of all materials. Neither the authors, nor the publisher, nor anyone else associated with this publication, shall be liable for any loss, damage or liability directly or indirectly caused or alleged to be caused by this book. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher. The consent of Burleigh Dodds Science Publishing Limited does not extend to copying for general distribution, for promotion, for creating new works, or for resale. Specific permission must be obtained in writing from Burleigh Dodds Science Publishing Limited for such copying. Permissions may be sought directly from Burleigh Dodds Science Publishing at the above address. Alternatively, please email: [email protected] or telephone (+44) (0) 1223 839365. Trademark notice: Product or corporate names may be trademarks or registered trademarks and are used only for identification and explanation, without intent to infringe. Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of product liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Library of Congress Control Number: 2017940084 British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library ISBN 978-1-78676-196-5 (print) ISBN 978-1-78676-198-9 (online) ISBN: 978-1-78676-199-6 (online) ISSN: 2059-6936 (print) ISSN: 2059-6944 (online) Typeset by Deanta Global Publishing Services, Chennai, India Printed by Lightning Source

Contents Series list

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Introduction xiii 1 Biology and ecology of rice-feeding insects: root and stem feeders 1 E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; and T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 1.1 Introduction 1 1.2 Mole cricket 3 1.3 Root aphids 5 1.4 Rice root aphid 8 1.5 Rice mealybug 10 1.6 Black bugs 12 1.7 Rice stalk stink bug 15 1.8 Chinch bug 17 1.9 Rice seed midges 19 1.10 Rice stem maggot 22 1.11 Rice seedling flies 23 1.12 Black beetles 25 1.13 ‘Chafers’ (white grubs) 26 1.14 Colaspis beetles 28 1.15 Rice root weevil 31 1.16 Rice plant weevil 33 1.17 Paddy root weevil 35 1.18 Rice water weevil 37 1.19 Gorgulho aquático do arroz 41 1.20 Rice water weevil 43 1.21 Termites 44 1.22 Root-feeding termites 49 1.23 References 51 2 Biology and ecology of rice-feeding insects: stem borers and rice gall midges 57 E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; and T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 2.1 Introduction 57 2.2 Stalk-eyed borer 61 2.3 Stalk-eyed fly 65 2.4 Gold-fringed rice borer 68 2.5 Dark-headed stem borer 70 2.6 Spotted stem borer 73 2.7 American rice stalk borer 76 2.8 Rice striped borer 79 2.9 African striped rice borer 83 © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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2.10 African white borer 86 2.11 Yellow stem borer 91 2.12 White stem borer 95 2.13 African pink borer 97 2.14 African pink borer 100 2.15 Asiatic pink stem borer 102 2.16 South American white borer 105 2.17 Sugarcane borer 107 2.18 Lesser cornstalk borer 110 2.19 Mexican rice borer 113 2.20 Asian rice gall midge 116 2.21 African rice gall midge 120 2.22 References 124 3 Biology and ecology of rice-feeding insects: leafhoppers and planthoppers 135 E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; and T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 3.1 Introduction 135 3.2 White rice leafhoppers 138 3.3 Green leafhoppers 140 3.4 Nephotettix afer Ghauri and Nephotettix modulatus Melichar 141 3.5 Nephotettix nigropictus (Stål) 143 3.6 Nephotettix cincticeps (Uhler) 145 3.7 Nephotettix virescens (Distant) 147 3.8 Nephotettix malayanus Ishihara et Kawase 149 3.9 Zigzag leafhopper 151 3.10 Smaller brown planthopper (Laodelphax striatellus Fallen) 153 3.11 Brown planthopper (Nilaparvata lugens Stål) 155 3.12 White-backed planthopper 160 3.13 Rice delphacid (Tagosodes orizicolus Muir) 164 3.14 Rice delphacid (Tagosodes cubanus Crawford) 167 3.15 Spittlebugs (Locris maculata maculata Fabricius) 169 3.16 Spittlebugs (Deois flavopicta Stål) 172 3.17 References 174 4 Biology and ecology of rice-feeding insects: foliage feeders 181 E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; and T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 4.1 Introduction 181 4.2 Large rice grasshoppers (Hieroglyphus banian Fabricius) 186 4.3 Rice grasshopper (Hieroglyphus daganensis Krauss) 189 4.4 Short-horned grasshoppers 191 4.5 Variegated grasshoppers 193 4.6 Meadow grasshoppers 196 4.7 Whitefly 199 © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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4.8 Rice whitefly 201 4.9 Spider mites 202 4.10 Rice thrips 204 4.11 Rice leaffolder (Cnaphalocrocis medinalis Guenée) 207 4.12 Rice leaffolder (Marasmia patnalis Bradley) 212 4.13 Fijian rice leaffolder 214 4.14 Rice caseworm 215 4.15 Green horned caterpillar 218 4.16 Rice skipper (Parnara guttata Bremer et Grey) 221 4.17 Rice skipper (Pelopidas mathias F.) 223 4.18 Rice ear-cutting caterpillar 225 4.19 The fall armyworm (Spodoptera frugiperda J. E. Smith) 228 4.20 Common cutworm 230 4.21 Rice swarming caterpillar 232 4.22 Common armyworm (Mythimna unipuncta Haworth) 235 4.23 Rice green semiloopers 237 4.24 Green hairy caterpillars 240 4.25 Rice whorl maggot (Hydrellia prosternalis Deeming) 242 4.26 Rice leaf miner (Hydrellia griseola Fallen) 244 4.27 Rice whorl maggot (Hydrellia philippina Ferino) 247 4.28 South American rice miner 251 4.29 Leaf miner (Cerodontha orbitona Spencer) 254 4.30 Paddy stem maggot 255 4.31 Asian rice hispa 257 4.32 African rice hispa 261 4.33 Rice blue beetle 264 4.34 Rice leaf beetle 266 4.35 Flea beetles 268 4.36 Ladybird beetle 271 4.37 Foliage feeding aphids 273 4.38 References 274 5 Biology and ecology of rice-feeding insects: panicle feeders 285 E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; and T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 5.1 Introduction 285 5.2 Stink bugs 287 5.3 Alydid bugs 288 5.4 Rice bugs 293 5.5 Stink bugs 299 5.6 Southern green stink bug 301 5.7 Rice stink bugs 303 5.8 Earwigs 309 5.9 Blister beetles 311 5.10 Panicle thrips 313 5.11 References 315

© Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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6 Integrated pest management (IPM) of rice 319 E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; and T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 6.1 Concepts and options for rice IPM 319 6.2 Cultural practices in rice IPM 321 6.3 Promoting natural enemies of rice pests: conservation biological control 325 6.4 Augmentative biological control 328 6.5 Selective insecticides 329 6.6 Dissemination mechanisms for rice IPM 332 6.7 References 335 Index345

© Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Achieving sustainable cultivation of maize - Vol 1 001 From improved varieties to local applications  Edited by: Dr Dave Watson, CGIAR Maize Research Program Manager, CIMMYT, Mexico Achieving sustainable cultivation of maize - Vol 2 002 Cultivation techniques, pest and disease control  Edited by: Dr Dave Watson, CGIAR Maize Research Program Manager, CIMMYT, Mexico Achieving sustainable cultivation of rice - Vol 1 003 Breeding for higher yield and quality Edited by: Prof. Takuji Sasaki, Tokyo University of Agriculture, Japan Achieving sustainable cultivation of rice - Vol 2 004 Cultivation, pest and disease management Edited by: Prof. Takuji Sasaki, Tokyo University of Agriculture, Japan Achieving sustainable cultivation of wheat - Vol 1 005 Breeding, quality traits, pests and diseases Edited by: Prof. Peter Langridge, The University of Adelaide, Australia Achieving sustainable cultivation of wheat - Vol 2 006 Cultivation techniques Edited by: Prof. Peter Langridge, The University of Adelaide, Australia Achieving sustainable cultivation of tomatoes 007 Edited by: Dr Autar Mattoo, USDA-ARS, USA & Prof. Avtar Handa, Purdue University, USA Achieving sustainable production of milk - Vol 1 008 Milk composition, genetics and breeding Edited by: Dr Nico van Belzen, International Dairy Federation (IDF), Belgium Achieving sustainable production of milk - Vol 2 009 Safety, quality and sustainability Edited by: Dr Nico van Belzen, International Dairy Federation (IDF), Belgium Achieving sustainable production of milk - Vol 3 010 Dairy herd management and welfare Edited by: Prof. John Webster, University of Bristol, UK Ensuring safety and quality in the production of beef - Vol 1 011 Safety Edited by: Prof. Gary Acuff, Texas A&M University, USA & Prof. James Dickson, Iowa State University, USA Ensuring safety and quality in the production of beef - Vol 2 012 Quality Edited by: Prof. Michael Dikeman, Kansas State University, USA Achieving sustainable production of poultry meat - Vol 1 013 Safety, quality and sustainability Edited by: Prof. Steven C. Ricke, University of Arkansas, USA Achieving sustainable production of poultry meat - Vol 2 014 Breeding and nutrition Edited by: Prof. Todd Applegate, University of Georgia, USA Achieving sustainable production of poultry meat - Vol 3 015 Health and welfare Edited by: Prof. Todd Applegate, University of Georgia, USA

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Achieving sustainable production of eggs - Vol 1 016 Safety and quality Edited by: Prof. Julie Roberts, University of New England, Australia Achieving sustainable production of eggs - Vol 2 017 Animal welfare and sustainability Edited by: Prof. Julie Roberts, University of New England, Australia Achieving sustainable cultivation of apples 018 Edited by: Dr Kate Evans, Washington State University, USA Integrated disease management of wheat and barley 019 Edited by: Prof. Richard Oliver, Curtin University, Australia Achieving sustainable cultivation of cassava - Vol 1 020 Cultivation techniques Edited by: Dr Clair Hershey, formerly International Center for Tropical Agriculture (CIAT), Colombia Achieving sustainable cultivation of cassava - Vol 2 021 Genetics, breeding, pests and diseases Edited by: Dr Clair Hershey, formerly International Center for Tropical Agriculture (CIAT), Colombia Achieving sustainable production of sheep 022 Edited by: Prof. Johan Greyling, University of the Free State, South Africa Achieving sustainable production of pig meat - Vol 1 023 Safety, quality and sustainability Edited by: Prof. Alan Mathew, Purdue University, USA Achieving sustainable production of pig meat - Vol 2 024 Animal breeding and nutrition Edited by: Prof. Julian Wiseman, University of Nottingham, UK Achieving sustainable production of pig meat - Vol 3 025 Animal health and welfare Edited by: Prof. Julian Wiseman, University of Nottingham, UK Achieving sustainable cultivation of potatoes - Vol 1 026 Breeding, nutritional and sensory quality Edited by: Prof. Gefu Wang-Pruski, Dalhousie University, Canada Achieving sustainable cultivation of oil palm - Vol 1 027 Introduction, breeding and cultivation techniques Edited by: Prof. Alain Rival, Center for International Cooperation in Agricultural Research for Development (CIRAD), France Achieving sustainable cultivation of oil palm - Vol 2 028 Diseases, pests, quality and sustainability Edited by: Prof. Alain Rival, Center for International Cooperation in Agricultural Research for Development (CIRAD), France Achieving sustainable cultivation of soybeans - Vol 1 029 Breeding and cultivation techniques Edited by: Prof. Henry Nguyen, University of Missouri, USA Achieving sustainable cultivation of soybeans - Vol 2 030 Diseases, pests, food and non-food uses Edited by: Prof. Henry Nguyen, University of Missouri, USA Achieving sustainable cultivation of sorghum - Vol 1 031 Genetics, breeding and production techniques Edited by: Prof. Bill Rooney, Texas A&M University, USA

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Series listxi Achieving sustainable cultivation of sorghum - Vol 2 032 Sorghum utilisation around the world Edited by: Prof. Bill Rooney, Texas A&M University, USA Achieving sustainable cultivation of potatoes - Vol 2 033 Production and storage, crop protection and sustainability Edited by: Dr Stuart Wale, Potato Dynamics Ltd, UK Achieving sustainable cultivation of mangoes 034 Edited by: Professor Víctor Galán Saúco, Instituto Canario de Investigaciones Agrarias (ICIA), Spain & Dr Ping Lu, Charles Darwin University, Australia Achieving sustainable cultivation of grain legumes - Vol 1 035 Advances in breeding and cultivation techniques Edited by: Dr Shoba Sivasankar et al., CGIAR Research Program on Grain Legumes, ICRISAT, India Achieving sustainable cultivation of grain legumes - Vol 2 036 Improving cultivation of particular grain legumes Edited by: Dr Shoba Sivasankar et al., CGIAR Research Program on Grain Legumes, ICRISAT, India Achieving sustainable cultivation of sugarcane - Vol 1 037 Cultivation techniques, quality and sustainability Edited by: Prof. Philippe Rott, University of Florida, USA Achieving sustainable cultivation of sugarcane - Vol 2 038 Breeding, pests and diseases Edited by: Prof. Philippe Rott, University of Florida, USA Achieving sustainable cultivation of coffee 039 Breeding and quality traits Edited by: Dr Philippe Lashermes, Institut de Recherche pour le Développement (IRD), France Achieving sustainable cultivation of bananas - Vol 1 040 Cultivation techniques Edited by: Prof. Gert Kema, Wageningen University, The Netherlands & Prof. André Drenth, University of Queensland, Australia Global Tea Science 041 Current status and future needs Edited by: Dr V. S. Sharma, Formerly UPASI Tea Research Institute, India & Dr M. T. Kumudini Gunasekare, Coordinating Secretariat for Science Technology and Innovation (COSTI), Sri Lanka Integrated weed management 042 Edited by: Emeritus Prof. Rob Zimdahl, Colorado State University, USA Achieving sustainable cultivation of cocoa - Vol 1 043 Genetics, breeding, cultivation and quality Edited by: Prof. Pathmanathan Umaharan, Cocoa Research Centre – The University of the West Indies, Trinidad and Tobago Achieving sustainable cultivation of cocoa - Vol 2 044 Diseases, pests and sustainability Edited by: Prof. Pathmanathan Umaharan, Cocoa Research Centre – The University of the West Indies, Trinidad and Tobago Water management for sustainable agriculture 045 Edited by: Prof. Theib Oweis, Formerly ICARDA, Lebanon Improving organic animal farming 046 Edited by: Dr Mette Vaarst, Aarhus University, Denmark & Dr Stephen Roderick, Duchy College, Cornwall, UK Improving organic crop cultivation 047 Edited by: Prof. Ulrich Köpke, University of Bonn, Germany

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Managing soil health for sustainable agriculture - Vol 1 048 Fundamentals Edited by: Dr Don Reicosky, USDA-ARS, USA Managing soil health for sustainable agriculture - Vol 2 049 Monitoring and management Edited by: Dr Don Reicosky, USDA-ARS, USA Rice insect pests and their management 050 E. A. Heinrichs, Francis E. Nwilene, Michael J. Stout, Buyung A. R. Hadi & Thais Freitas Improving grassland and pasture management in temperate agriculture 051 Edited by: Prof. Athole Marshall & Dr Rosemary Collins, University of Aberystwyth, UK Precision agriculture for sustainability 052 Edited by: Dr John Stafford, Silsoe Solutions, UK

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Introduction Rice, the daily food of nearly half of the world’s population, is the foundation of national stability and economic growth in many developing countries. It is the source of onequarter of global food energy and – for the world’s poor – the largest food source. It involves also the single largest use of land for producing food and the biggest employer and income generator for rural people in the developing world. Rice production has been described as the single most important economic activity on Earth. Because rice occupies approximately 9% of the planet’s arable land, it is also a key area of concern – and of opportunity – in environmental protection. Rice, one of the world’s major food crops, has a variety of uses and is adapted to a broad range of climatic, edaphic and cultural conditions. Annual world rice production in 2013 was approximately 745 million tonnes grown on more than 165 million ha (FAO 2016). Over 90% of this area lies in Asia, while the remainder is divided among Latin America, Africa, Australia, Europe and the United States. Annual production in Asia is 675 million tonnes while it is only 36 million tonnes in the Americas and 29 million tonnes in Africa. Rice cultivation involves the dominant land use in Asia, but it is now playing an increasingly important role in Africa as well. In West and Central Africa – the most impoverished regions on Earth according to the Food and Agriculture Organization (FAO) – rice is grown under subsistence conditions by about 20 million smallholder farmers who are shackled to slashand-burn farming and who lack rice varieties that are appropriate to local conditions. FAO statistics show that the demand for rice in these regions is growing by 6% a year (the fastest-growing rice demand in the world), largely because of increasing urbanisation. The increase in rice consumption is not only limited to Africa but also prevalent worldwide. To feed the growing world population rice production must be increased. However, rice farmers face many abiotic and biotic constraints in their quest to increase rice production. In conjunction with the introduction of new high-yielding drought- and flood-tolerant rice varieties, increasing yields will require a reduction in losses to insects and other stresses. As cropping intensity and cultural practices are changed to meet production needs, pest pressure is expected to intensify. The rice plant is an ideal host for many insect species. All of the plant parts are vulnerable to insect attack from the time of sowing till harvest. There are over 800 insect species damaging rice in one way or another, although the majority of them do very little damage. In tropical Asia only about 20 species are of major importance and of regular occurrence (Grist and Lever 1969). In Africa, 15 species of insects are considered major pests of rice (Oteng and Sant’Anna 1999) and in the Americas about 20 species are considered major pests (Stout, pers. comm.). To develop effective pest management strategies, it is essential to properly identify and to understand the biology and ecology of insect pests and the arthropods that help regulate their populations. This chapter effectively utilises the unique knowledge and expertise of leading rice entomologists from Africa, Asia and the Americas to provide the first global coverage of rice insect pests. The discussion includes the geographical distribution, plant hosts other than rice, description and biology, and plant damage and ecology of the important rice insects in Africa, Asia and the Americas. The insects are classified based on feeding type: (1) root and stem feeders, (2) stem borers, (3) rice gall midges, (4) leafhoppers and planthoppers, (5) foliage feeders and

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Introduction

(6) panicle feeders. In addition, the current strategies to manage rice insect pests in an environmentally sustainable manner are discussed.

References FAO. 2016. FAOSTAT. http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor Grist, D. H. and Lever, R. J. A. W. 1969. Pests of Rice. London and Harlow: Longmans, Green and Co. Ltd. Oteng, J. W. and Sant’Anna, R. 1999. Rice production in Africa: current situation and issues. In International Rice Commission Newsletter, Vol. 48. FAO, Roma.

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Chapter 1 Biology and ecology of rice-feeding insects: root and stem feeders E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 1.1 Introduction 1.2 Mole cricket 1.3 Root aphids 1.4 Rice root aphid 1.5 Rice mealybug 1.6 Black bugs 1.7 Rice stalk stink bug 1.8 Chinch bug 1.9 Rice seed midges 1.10 Rice stem maggot 1.11 Rice seedling flies 1.12 Black beetles 1.13 ‘Chafers’ (white grubs) 1.14 Colaspis beetles 1.15 Rice root weevil 1.16 Rice plant weevil 1.17 Paddy root weevil 1.18 Rice water weevil (Lissorhoptrus oryzophilus Kuschel) 1.19 Gorgulho aquático do arroz (Oryzophagus oryzae) 1.20 Rice water weevil (Afroryzophilus djibai Lyal) 1.21 Termites 1.22 Root-feeding termites 1.23 References http://dx.doi.org/10.19103/AS.2017.0038.01 © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

1.1 Introduction There are many insects which feed on the roots and stem of rice plants. Some, such as white grubs and root aphids, attack exclusively the roots, while others (e.g. mealybug and rice stem maggot) infest only the stems, although there are some pests such as mole crickets which damage both roots and stems. The infestation of the rice crop by different insect pests is related also to the growth stage of the plants. Seedlings are prone to attack by pests such as rice seedling flies, rice seed midges and mole crickets. Insect damage at the early stages of crop growth causes seedling death and results in missing plants. Damaged plants may completely disappear from the field by being blown in the wind or by being consumed by saprophytic organisms. Heavily infested fields have many missing hills, leading to low plant density and low yield. The subterranean environment in which root-feeding insects live limits mobility, especially in locating food. As a result, root feeders have adapted by 1) having a long life either as individuals (beetles), as colonies of social insects (termites) or as dependent on social insects (mealybugs and aphids) and 2) having a wide host range (all species) (Litsinger et al. 1987). Root-feeding insects include the mole crickets (family Gryllotalpidae), tobacco cricket (family Gryllidae), root aphids (family Aphididae), mealybugs (family Pseudococcidae), black bugs (family Pentatomidae), stink bug (family Pentatomidae), seed midges (family Chironomidae), stem maggot (family Chloropidae), seedling flies (family Muscidae), white grubs (family Scarabaeidae), grape colaspis (family Chrysomelidae), termites (family Termitidae), root weevils (family Curculionidae), plant weevil (family Curculionidae), black beetles (family Scarabaeidae) and the rice water weevils (family Curculionidae).

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1.2 Mole cricket, Gryllotalpa africana Palisot de Beauvois (Orthoptera: Gryllotalpidae) Distribution: Asia, Africa, Central America and the Caribbean, Europe, Oceania. Host plants other than rice: Panax ginseng L., Helianthus annuus L., Brassica oleracea L. var. capitata L., Acacia confusa Merr., Allium cepa L., Hordeum vulgare L., Populus, Poaceae (grasses), Nicotiana tabacum L., Solanum tuberosum L., Triticum spp., Cola acuminata (Beauvoir) Schott and Endlicher, Camellia sinensis (L.) Kuntze, Corchorus (CABI 2015a). Description and biology: This insect is readily identifiable by its large size and enlarged front legs that are adapted for digging in soil, hence the name 'mole' cricket (Fig. 1.1). Adult mole crickets are strong fliers and are phototropic, being attracted to lights at night. They are large insects, 25–35 mm in length, and are light brown in colour (AgroAtlas 2003). The front legs are enlarged and modified for burrowing in soil. The first segment of the thorax is enlarged, which helps the mole cricket to push its way through the soil. At night, adults make branched burrows by their digging action in the soil or they search for food items such as other insects or seeds above ground. They remain underground during the day. Adults are sometimes seen swimming in flooded fields when the paddy is being puddled as flooding causes them to leave their burrows. Thus, mole cricket populations are low in flooded fields where they are mostly found in the levees. Female mole crickets attract males by chirping. The burrow acts as a resonator of the sound. Each species has a unique calling signal. Males can be attracted by playing back

Figure 1.1 Gryllotalpa africana adult. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

a recording of the mating call. Female crickets burrow in levees of irrigated fields and construct hardened cells below the soil surface in which the eggs are laid. During its lifespan of more than 6 mo., each female may lay several hundred eggs in batches of 30–50. Eggs are laid in cells beneath the soil surface and hatch in about 1 mo. Development of the light brown nymphs occurs in the soil and lasts 3–4 mo. (Reissig et al. 1986, Dale 1994). There is only one generation a year. Adults are highly mobile and can leave a flooded field to locate a more suitable habitat (Litsinger et al. 1987). Adults overwinter in burrows deep in the soil (Dale 1994). Plant damage and ecology: Although mole crickets occur in all rice environments, they are most prevalent in upland rice when fields are damp (Dale 1994). Irrigated fields are generally not attacked, except before flooding or when water supply is irregular or inadequate, causing dry areas to occur (Breniere 1983). When they occur in lowlands, they inhabit rice field levees but leave them when water levels rise. Mole crickets prefer lowlying, moist upland soils with high organic matter (Akinsola 1984a). Sandy or light soils are preferred by mole crickets in India (Chatterjee 1973). Young and newly planted seedlings are most commonly attacked in the early part of the season before the fields are flooded (CABI 2015a). Both nymphs and adults attack stems below ground and close to the roots. Sometimes, only one or two tillers are cut and damage is evident only when the tillers begin to dry a few days later. The entire plant dies if the attack is severe. Dried plants can be seen as patches in the rice field. Normally damage is greatest near the field borders. Unlike field crickets, mole crickets do not take the cut tillers into their burrows (Tripathi and Shri Ram 1968). Mole crickets are polyphagous insects (Dale 1994). Although mole crickets have been reported as predacious on other insects (Chatterjee 1973) and are cannibalistic, they primarily feed on a number of plant species. In addition to rice, they have been reported as serious pests of other agricultural crops (Matsura et al. 1985) and turf and pasture grasses (Nickle and Castner 1984). Mole crickets sometimes feed on germinating seedlings. Severe mole cricket attacks of rice in nursery beds have been reported from West Africa according to field surveys made by entomologists of AfricaRice. In rice fields, the feeding of mole crickets can easily kill seedlings having small root systems. Older plants are more tolerant of injury because of their larger root systems. Mole cricket nymphs and adults dig tunnels and attack stems and roots below the soil level. Sometimes, only the base of one or two tillers of a plant is cut and the damage is only evident when tillers begin to die a few days later. When feeding is severe, the entire plant dies. Dried plants are evident as dead patches in the rice field. In irrigated fields, young and newly planted seedlings are most commonly attacked in the early part of the season before fields are flooded (COPR 1976). Feeding activity most commonly occurs at night.

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Biology and ecology of rice-feeding insects: root and stem feeders

1.3  Root aphids, Tetraneura nigriabdominalis (Sasaki) The aphid species that infest rice roots and their distribution are given in Table 1.1. Some of these aphids are also occasionally found on the aerial parts of plants. Distribution: Cuba, Fiji, India, Indonesia, Japan, Malaysia, New Guinea, Philippines, Sierra Leone, Taiwan, Zambia. Host plants other than rice: Many Gramineae species. Graminaceous weeds such as Eleusine indica (L.), Pennisetum subangustum Stapf and Hubb, Ischaemum rugosum Table 1.1 World distribution of rice root aphids (modified from Yano et al. 1983) Aphid species

Host plants

Distribution

Anoecia corni (Fabricius)

Rice

Japan

Anoecia fulviabdominalis (Sasaki)

Rice, barley, wheat, grasses

Japan

Anoecia sp.

Rice

Japan

Chaetogeoica polychaeta Pal & Raychaudhuri

Rice, grasses

India

Forda sp.

Rice

Japan

Geoica lucifuga (Zehntner)

Rice, sugarcane, grasses, Pistacia

India, Japan, Malaysia, Philippines, Taiwan

Geoica setulosa (Passerini)

Rice

Italy

Geoica sp.

Rice

Japan

Geoica utricularia setariae (Passerini)

Rice

Italy

Paracletus cimiciformis von Heyden

Rice, barley, grasses

Japan

Prociphilus sp.

Rice, plants belonging to Araceae and Liliaceae

Japan

Rhopalosiphum rufiabdominale (Sasaki)

Rice, Prunus sp., grasses

Argentina, Central America, Egypt, Fiji, India, Japan, Malaysia, Morocco, Suriname, Taiwan, Thailand, United States, USSR

Tetraneura akinire (Sasaki)

Rice

Japan

Tetraneura basui Hille Ris Lambers

Rice, grasses

India

Tetraneura nigriabdominalis (Sasaki)

Rice, graminaceous weeds

Cuba, Fiji, India, Indonesia, Japan, Malaysia, New Guinea, Philippines, Sierra Leone, Taiwan, Zambia

Tetraneura radicicola Strand

Rice, grass, Ulmus sp.

India

Tetraneura sp.

Rice

Japan

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Biology and ecology of rice-feeding insects: root and stem feeders

Salisb and Paspalum commersonii scrobiculatum L. serve as alternate hosts for the root aphid in Sierra Leone (Akibo-Betts and Raymundo 1978). These grasses are most common in upland ecosystems and are the most important weed competitors of rice. The root aphid has many additional hosts throughout the world. In India, it is a pest of finger millet or ragi, Eleusine coracana (L.), where up to 200 nymphs and adults may feed on one plant (Gadiyappannavar and Channabasavanna 1973). Description and biology: The root aphids are soft-bodied insects that live in colonies composed of nymphs and adults (Reissig et al. 1986). Eggs develop and remain inside the body of the viviparous females (gives birth to nymphs). A female produces 35–45 nymphs in a lifetime of 2–3 wk. Adult females are 3–5 mm in length, are more or less spherical in shape and are brown. The body of the aphid is usually covered with a thin film of white powder. The females are parthenogenic, producing offsprings without mating. The root aphids are normally composed entirely of females. The nymphs produce honeydew, which attracts ants. In return, ants transport the nymphs from plant to plant, protecting the growing aphids from predators and parasites (IRRI: Rice Knowledge Bank. Root aphids). There are winged and wingless forms of adults. Winged adults fly into the rice field from their alternative plant hosts at the beginning of the rice season and rapidly produce young aphids that become wingless adults. Several generations occur on rice. Winged adults are produced when the crop is near maturity, and at that time, the aphids leave rice fields to seek new plant hosts.

Figure 1.2 Root aphid, Tetraneura nigriabdominalis (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: Root aphids occur in well-drained soils in rainfed environments including upland and rainfed lowlands (Reissig et al. 1986). The adults are found on roots below ground level. They can also be located in cavities made by ants around the root system. T. nigriabdominalis (Fig. 1.2) was observed feeding on rice in Sierra Leone during the early wet season (Akibo-Betts and Raymundo 1978). Adults emerge and infest the roots simultaneously with the peach aphid, Hysteroneura setariae (Thomas), which feeds on the leaves and grain in April and May. Most of the infestations observed in Sierra Leone seem to coincide with the infestation of rice by termites. Both the adults and nymphs remove plant sap with their sucking mouthparts and, as a result, the rice leaves turn yellow and the plants become stunted. In severe cases, which are rare in West Africa, plants wilt and die. Yield loss occurs mainly through reduced tillering of the rice plants (Litsinger et al. 1987). Yield losses due to root aphids in West Africa have not been determined. In Japan, Tanaka (1961) reported that rice root aphids cause yield reductions of up to 50%. In India, T. nigriabdominalis is one of a complex of aphid species that attacks the roots of rice seedlings in nursery beds during the rabi (winter) crop. Populations vary greatly among the various rice cultivars with Jaya having a higher infestation than IR8 (Dani and Majumdar 1978). T. nigriabdominalis is a widely distributed species of root aphid. In Japan, it infests only upland rice but not irrigated fields.

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Biology and ecology of rice-feeding insects: root and stem feeders

1.4 Rice root aphid, Rhopalosiphum rufiabdominale (Sasaki) (Hemiptera: Aphididae) Distribution: Asia, Africa, North America, Central America and the Caribbean, South America, Europe, Oceania. Originally described from Japan, this aphid is thought to be an invasive species worldwide (Kindler et al. 2004). Host plants other than rice: Araceae, Brassicaceae, Cucurbitaceae, Fabaceae, Indiaceae, Malvaceae, Orobanchaceae, Poaceae, Rosaceae, Solanaceae (CABI 2016a). This species is also known to feed on Echinochloa colona, Andropogon bicornis, Soliva pterosperma, Paspalum sp. and red rice (Maziero et al. 2007). Description and biology: Root aphids have a dark green and reddish soft body, with dark red spots close to the siphunculus (Fig. 1.3), in winged and wingless forms. Holocyclic populations (obligate alternation between winter and summer hosts) inhabit East Asian regions only, whilst anholocyclic populations (reproducing by means of obligate parthenogenesis) are distributed in warmer climates worldwide (Blackman and Eastop 2006). In Brazil, females reproduce all year, by thelytokous parthenogenesis, producing only female offspring (Gallo et al. 2002). Nymphs moult four times before becoming adults and then require 1.2–1.8 days to begin reproducing (Hsieh 1970).

Figure 1.3 Rhopalosiphum rufiabdominale (Source: Rajinder Bains).

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Biology and ecology of rice-feeding insects: root and stem feeders

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Plant damage and ecology: It has been reported as an important pest in Brazil, especially in upland rice fields, but also in lowland areas before flooding. Nymphs and adults feed mainly on the roots, but can move to the stem when populations are very high. Direct damage results from removal of sap, causing yellowing and stunted growth of plants (Gallo et al. 2002). Damage is more severe in dry seasons and dry areas such as the top of the levees, but once the area is flooded the populations move out or decline drastically.

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Biology and ecology of rice-feeding insects: root and stem feeders

1.5 Rice mealybug, Brevennia rehi (Lindinger) (Homoptera: Pseudococcidae) Distribution: Australia, Bangladesh, Burma, India, Nepal, Papua New Guinea, Puerto Rico, Southern US. Host plants other than rice: Apluda mutica L., Brachiaria reptans (L.) Gardner & Hubbard, Chloris barbata (Sw.), Cymbopogon caesius (Nees) Stapf, Cynodon dactylon (L.) Pers., Cyperus rotundus L., Dactyloctenium aegyptium (L.) Willd., Dichanthium annulatum (Forssk.) Stapf, Digitaria sanguinalis (L.) Scop., Echinochloa colona (L.) Link, Eleusine coracana (L.) Gaertn., Eragrostis interrupta (Lam.) Doell, Fimbristylis miliacea (L.) Vahl, Fimbristylis tenera Roem. & Schult., Imperata cylindrica (L.) Raeuschel, Ischaemum indicum (Houtt) Merr., Iseilema laxum Hack., Leptochloa chinensis (L.) Nees, Panicum repens L., Paspalum scrobiculatum L., Saccharum spontaneum L., Setaria glauca (L.) Beauv. Description and biology: The adult females are wingless, oblong and 3–4 mm long. They are bulky and remain stationary on the stems behind leaf sheaths at the base of plants. The body is soft, pinkish and covered with white waxy threads (Fig. 1.4). Males, pale yellowish, are seldom found in the colonies. They have a single pair of wings and a style-like process at the end of the abdomen but lack mouthparts. They are slender and much smaller than the females. Males migrate freely from plant to plant. Reproduction is parthenogenetically oviparous as well as viviparous (Alam 1965).

Figure 1.4 Rice mealybug, Brevennia rehi (Source: Kerala Agricultural University, India). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

Biology and ecology of rice-feeding insects: root and stem feeders

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The average pre-oviposition period is 6 days. The female mealybug lays individual eggs, more or less in a chain, inside the waxy threads. A single female can lay 60–280 eggs and nymphs in about 5 days, after which it dies. Eggs are yellowish white and the incubation period varies from 3 to 6 hours. Hatching of eggs usually takes place in the morning hours. Newly hatched nymphs remain crowded within the waxy threads for 6 to 10 hours before they disperse to various parts of the same plant or to adjacent rice plants. Nymphs are first yellowish white but turn dark yellow after a day. They become fixed between the leaf sheath and stem by driving the proboscis into the stem. The body gets covered with a waxy material in about a day. There are three nymphal instars which take 12–18 days to pass and about 12 generations in a year. Plant damage and ecology: The rice mealybug is a sporadic pest causing severe losses to rice in the Indian subcontinent. It is prevalent in rainfed rice and is not found in irrigated rice. Mealybugs occur in colonies attached to the stems and leaf sheaths of rice plants. They suck sap from the plants. White waxy fluff protruding from between the leaf sheath and the stem is the typical indication of the pest’s presence. As a result of infestation, plants become stunted and the older leaves turn yellow. High incidence inhibits panicle emergence and plants may even dry. Infested fields show isolated patches of stunted plants. Damage is severe during drought conditions when plants can least tolerate the removal of plant sap. In 1979, when there was a long and severe drought in Bangladesh, a severe outbreak of mealybugs caused yield losses of up to 100% in some fields (Alam and Karim 1981). Heavy losses caused by mealybugs have been reported from several parts of India (Banerjee 1956, Mammen 1976). Hot, dry weather favours the survival and multiplication of rice mealybugs. But the population drops drastically by the beginning of winter. During winter, the pests survive on weeds and volunteer rice plants.

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Biology and ecology of rice-feeding insects: root and stem feeders

1.6 Black bugs, Scotinophara coarctata (Fabricius), S. lurida (Burmeister) (Fig. 1.5), S. latiuscula Breddin, and S. sorsogonensis Barrion, Joshi, Barrion-Dupo & Sebastian (Hemiptera: Pentatomidae) Distribution: S. coarctata: Bangladesh, Brunei Darussalam, Burma, Cambodia, India, Indonesia, Malaysia, Pakistan, Philippines (Palawan), Sri Lanka, Thailand, Vietnam (CABI 2015b). S. lurida: Bangladesh, China, India, Indonesia, Japan, Kampuchea, Malaysia, Pakistan, Papua New Guinea, Philippines (Mindanao), Sri Lanka, Thailand, Vietnam. S. latiuscula: Indonesia (Sumatra), Philippines (Luzon) (Dale 1994). S. sorsogonensis: Philippines (Joshi et al. 2007). Host plants other than rice: Colocasia esculenta Schott., Hibiscus esculentus L., Hymenachne pseudointerrupta C. Muell., Panicum amplexicaule Rudge Pl. Guian., Scirpus grossus L., Scleria sumatrensis Retz., Vigna unguiculata L., Zea mays L. Description and biology: The following describes S. coarctata but the biology of the other Scotinophara species is similar. Adults are brownish black with a few distinct yellowish

Figure 1.5  Scotinophara lurida adult (Source: Centre for Invasive Species and Ecosystem Health, University of Georgia, USA (https://www.bugwood.org/); photo taken by Natasha Wright, Cook’s Pest Control, USA). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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spots on the thorax which bears spines below the anterior angles. They are 8–9 mm long. Tibiae and tarsi are pinkish. They give off an offensive odour typical of stink bugs when disturbed. Adult bugs live for up to seven months. There is one generation in a year. Female bugs deposit eggs (Fig. 1.6) on the basal parts of rice plants near the water surface. A female lays about 200 eggs during her lifetime and guards them until they hatch. Eggs are laid in masses in parallel rows on lower leaves near the water level (Reissig et al. 1996). Each egg measures 1 mm long, is greenish when laid and turns pinkish as it matures. The incubation period is 4–7 days. Nymphs are light brown, with a yellowish green abdomen and some black spots. They moult 4–5 times and reach the adult stage in 25–30 days. The long-living adults pass the winter or dry season in a dormant state in cracks in the soil in grassy areas. With favourable weather they fly to the rice crop and reproduce over several generations. They return to their resting sites after rice harvest. Adults are capable of migrating over long distances (Reissig et al. 1986). Large numbers of bugs are carried to distant places by strong winds. Adults appear in swarms, and are strongly attracted to light. Ajuk et al. (1981) and Latif et al. (1982) observed that the flight activity of adults to light traps coincides with the lunar cycle. The bugs are able to adapt to a wide variety of conditions and are capable of withstanding adverse conditions. They hide in soil cracks during water stress periods and during the winter. After overwintering they fly to the rice crop and reproduce over several

Figure 1.6  Scotinophara lurida female guarding eggs (Source: https://www.google.com/search?q= rhopalosiphum+rufiabdominale&source=lnms&tbm=isch&sa=X&ved=0ahUKEwjz6_26NLTAhWI24MKHar4DhkQ_AUICigB&biw=1920&bih=971#tbm=isch&q=Scotinophara+latiuscula&i mgrc=PcFN_exYkjMPVM). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

generations. They again return to their resting sites after the harvest of the rice crop. The black bug aestivates in the adult or late nymphal stage in cracks in bunds, in paddy fields or in adjacent higher grounds to a depth of 30 cm where it remains torpid. It is gregarious during periods of rice fallow. Plant damage and ecology: In the 1980s, many outbreaks of black bugs were reported even though the insects were previously considered as minor pests of rice (Reissig et al. 1986). Nymphs and adults feed chiefly at the base of stems where they remove plant sap. When the infestation is at the tillering stage, deadhearts occur but continued feeding results in leaves turning chlorotic or reddish brown colour, and in unfilled grains, decrease in tiller number, fewer grains per panicle and stunting (Heinrichs et al. 1987). Attack during the booting stage results in panicles with empty grains similar to the ‘deadhearts’ caused by stem borers. Direct injury to panicles is also common. Bugs feed on panicles in the milky stage on overcast days and during night. Injured grains have brown spots. Heavy infestations may lead to the death of plants and the whole field appears ‘burned’ similar to that of a hopperburned field. Per cent yield loss at 10 bugs per hill ranged from 14.7% in resistant cultivars to 23.0% in susceptible cultivars (Heinrichs et al. 1987). Populations are generally less on upland than on irrigated and rainfed wetland rice. The insects prefer continuously cropped irrigated fields to a single-cropped field. Heavy damage by the pest is usually observed after the heading stage of the rice crop especially when irrigation has been stopped during the maturation period. In the Philippines, the dry season rice crop is damaged more severely than the wet season crop (Miyamoto et al. 1983). The pest is most abundant in poorly drained rice fields around marshes. Asynchronous double cropping of irrigated rice with high levels of nitrogen seems to favour black bug outbreaks (Joshi et al. 2007). In Malaysia, the relatively small natural enemy complex of S. coarctata and high availability of alternate hosts in the vicinity of rice fields are suggested as possible causes for the frequent black bug outbreaks (Dale 1994).

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1.7 Rice stalk stink bug, Tibraca limbativentris (Stål) (Hemiptera: Pentatomidae) Distribution. This neotropical stink bug was identified using specimens from Rio de Janeiro, Brazil (Stål 1860). It is distributed in all the rice-producing countries in South and Central America, and is a major pest in Argentina, Brazil, Colombia, Dominican Republic, Ecuador, Peru and Venezuela (Pantoja et al. 2007). Host plants other than rice: Andropogon bicornis L., Glycine max (L.) Merr., Solanum lycopersicum L. and Triticum aestivum L. Other economically important crops may also serve as host plants. Description and biology. Adults are brownish with two white spots on the pronotum (Fig. 1.7) and reach 13 mm in length and 7.5 mm in width. Females reach sexual maturity 14 days after adulthood (Silva et al. 2004). The T. limbativentris adults enter the field shortly after rice germination and oviposit on the upper leaf surface. One female oviposits several times for a total of about 500–700 eggs over a period of 30 days. Female adults live for about 65 days and the male for about 30 days (Ferreira 1998).

Figure 1.7 Tibraca limbativentris adult (Source: Centre for Invasive Species and Ecosystem Health, University of Georgia, USA (https://www.bugwood.org/); photo taken by Natasha Wright, Cook’s Pest Control, USA).

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Biology and ecology of rice-feeding insects: root and stem feeders

Eggs are laid in two rows (Agronomia Para Todos 2012), usually on the abaxial surface of older leaves in an average number of 16 per egg mass (Pantoja et al. 1997). Eggs are cylindrical, 1 mm long and 0.8 mm in diameter. Egg colour varies from green, when newly oviposited, to cream or dark brown prior to hatching. The period from oviposition up to hatching is about 6 days. Nymphs pass through five nymphal instars in a period of about 37 days (Ferreira 1998). The duration varies with temperature, and can take up to 55 days. The first instar is gregarious; later instars are distributed on young stems and are located at the base of the plant, near soil level. Nymphal colour varies from deep red in the early instars to dark brown in the last instar. Adults feed on the rice stem, upside down, next to the soil in upland fields or next to the water level in lowland fields. Because of this habit, it is difficult to detect this insect in rice fields, since the insect is hidden and protected by the leaves (Ferreira et al. 1997). After harvest, adults seek shelter to hibernate if there is no food available. Andropogon bicornis L. (Poaceae) is one of the favoured species of host plants (Klein et al. 2012). Plant damage and ecology: Both adults and nymphs feed on plants. Nymphs begin to feed in the second instar. They begin attacking seedling plants starting at 20 days after germination (Ferreira 1998). Feeding on the plant causes partial or total culm necrosis due to injection of toxic saliva. Even in cases of partial necrosis, the plant is damaged because feeding delays development (Ferreira et al. 1997). This results from attack of the stem at the stage of initiation of the floral primordia. Entrance of the insect’s stylus at the last internode and sucking vital plant fluids causes a bottleneck that prevents the passage of nutrients to the panicle. When attack occurs in the vegetative phase, the tiller dies and the symptom is termed ‘deadheart’. When plants are attacked during the heading, spikelets are not filled and the symptom is termed a ‘whitehead’ (Heinrichs and Miller 1991). While Tibraca sucks the sap, it also introduces or injects toxic saliva. The damage is similar to that caused by stem borers, but the damage is at the top of internode rather than from boring within the stem. Plants attacked later in the reproductive phase can also suffer damage in grain quality, if feeding occurs towards the end of grain filling. Distribution is not uniform and spots can reach up to 200 insects m−2, where the damage is 100% (Ferreira 1998). Damage is greatest in rice under dry conditions and low humidity, favoured by the almost permanent absence of the sheet of water, which allows the insects to remain at the base of the plants. As the crop matures, populations of nymphs and adults decrease due to the hardness of the stem, which hinders the penetration of the stylet of the insect for sucking the plant sap. In studies in Colombia (Pantoja et al. 2007), infestation of 15- or 20-day-old plants did not cause yield reductions, thus suggesting that scouting for this pest should be concentrated on 25- to 40-day-old plants. Threshold levels on rice were calculated to be 8.8 and 25.8 T. limbativentris per 10 sweep net strokes for 30- and 40-day old plants, respectively.

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1.8 Chinch bug, Blissus leucopterus leucopterus (Say) (Hemiptera: Blissidae) Distribution: Blissus leucopterus leucopterus is native to North America, and its range now includes much of the United States and southern Canada, Mexico, Central America and South America. Host plants other than rice: Poaceae – Andropogon, Avena sativa L., Digitaria sanguinalis (L.), Hordeum vulgare L., Pennisetum glaucum (L.), Poa pratensis L., Saccharum officinarum L., Secale cereale L., Setaria lutescens (Weigel) F.T. Hubbard, Setaria viridis (L.) P. Beauv., Sorghum bicolor (L.), Urochloa mutica (Forssk.) T.Q. Nguyen, Zea mays L., turfgrasses (CABI 2016b). Description and biology: Chinch bugs are small sucking insects, 4 mm in length, with black bodies and white front wings with triangular black spots near the margins of the wings (Fig. 1.8). Adults overwinter in clumps of grass and emerge in spring to feed on grasses such as wheat, rice and maize. Eggs are elongated, white and very small (0.1 cm). Eggs turn red as they develop and nymphs emerge from eggs about seven to ten days after being laid. First instars are about 1 mm bright red with a yellow or white band on the abdomen. Later instars are black and grey with a white spot on the back. The entire life cycle from egg through five nymphal instars to adult may take five to six weeks. Non-diapausing adults may live three weeks. The insect is bivoltine (Vásquez and Sánchez 1991).

Figure 1.8 Blissus leucopterus adults and nymphs (Source: LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

Plant damage and ecology: Chinch bugs are occasional pests of seedling rice. They prefer hot and dry conditions and are thus most often pests of drill-seeded rice before flooding and under conditions conducive to drought. Adults and nymphs feed on the leaves and stems of rice plants; young nymphs can be found feeding on the roots below the soil line. Feeding on young seedlings causes leaves and stems to turn light brown to red in colour. The plants often take on a flame colour – red at the tip. High numbers of chinch bugs can kill young plants, severely reducing plant stands. Chinch bugs tend to be more problematic in drill-seeded rice until the application of a permanent flood (Saichuk 2012). They use their piercing-sucking mouthparts to feed on rice stems below the soil surface. Leaves and stems of the affected plants turn brown and eventually may wither and die.

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1.9 Rice seed midges, Cricotopus sylvestris (F.), Paralauterborniella subcincta and Paratanytarsus sp. (Diptera: Chironomidae) Distribution: Worldwide. Host plants other than rice: Some weed species. Description and biology: Chironomid midges are distributed worldwide and many species are found in rice fields. However, only a few species cause damage to rice. In California, where most rice is water-seeded and midges can be a significant pest (UC Pest Management Guidelines 2015), over 30 species have been recorded but comparatively few species are associated with seed and seedling injury. The most important pest midges are found in the genera Cricotopus, Paratanytarsus and Paralauterborniella (Clement et al. 1977). Chironomid adults resemble small mosquitoes but lack the elongated, needle-like mouthparts characteristic of mosquitoes (Fig. 1.9). They are often seen swarming above the surface of rice fields and other bodies of water. Masses of eggs are laid on water in strings held together by a sticky, mucilaginous material (gelatin envelope) that swells in contact with water to form a protective covering over the eggs. Eggs hatch in 1 or 2 days. Larvae are long and slender. They burrow through the mud and build characteristic tubes of silk and debris where they feed on organic matter, microorganisms and detritus.

Figure 1.9 Seed midge adult (Source: Jack Kelly Clark, courtesy of University of California Statewide IPM Program, USA. The photo is copyrighted by the Regents of the University of California, USA). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

The tubes serve as larval retreats and also as webs to entrap algae and diatoms for food. Larvae often possess haemoglobin in their ‘blood’ and as a consequence are reddish in colour. They pass through four instars in 7–10 days in the spring when the water is warm. Rice seed midges pupate in the tubes, complete development in 2–3 days and come to the water surface where the adult emerges. The entire life cycle from egg to adult requires about two weeks. Adults are short-lived and do not feed. Three to four generations occur each summer, but only the first two are of economic concern to rice growers in the United States (Anon. 1983). Plant damage and ecology: In North and South America, seed midges affect only waterseeded rice, and this problem aggravates when fields remain flooded for a substantial period before seeding. Injury to rice is limited to germinating seeds and very young seedlings (UC Pest Management Guidelines 2015). Damage to rice is caused mostly by the third and fourth instar larvae. Midge larvae feed on the emerging shoot, leaves or roots, or may hollow out the embryo of germinating seeds (Fig. 1.10) and all parts of seedlings (Clement et al. 1977) and kill the plant. They may also feed on floating leaves, causing small holes that extend completely through the leaves. Midge feeding can kill plants and reduce stands, necessitating replanting in some cases. Damage tends to be localized. Once seedlings are fully established, the plants can withstand damage by the larvae. Larval populations increase daily after flooding because of continued egg laying, and a delay in planting will expose germinating rice seeds to more midge infestations.

Figure 1.10 Seed midge injury to rice seeds (Source: LSU AgCenter).

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Biology and ecology of rice-feeding insects: root and stem feeders

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Tadpole shrimp and seed midge injury to the leaves and roots may be similar but the chewed areas caused by tadpole shrimp will be larger and more irregular because of the larger size of the shrimp mandibles. If the injury is caused by midges, the midge larva and tube are often still on the plant at the time of examination. If the injury is several days old, secondary organisms may invade the plant tissue, and the pest that caused the injury may be difficult to associate with the injury. Numerous other species of Chironomidae have been reported occasionally infesting rice fields in various countries. In Egypt, a Chironomus sp. causes damage to rice seedlings grown in saline soils. The Australian Chironomus tepperi prefers soils with a high organic content following sod seeding. In the USSR, larvae of a Chironomus sp. feed on floating or submerged rice leaves causing a severe reduction in shoot numbers (Dale 1994).

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Biology and ecology of rice-feeding insects: root and stem feeders

1.10 Rice stem maggot, Chlorops oryzae Matsumura (Diptera: Chloropidae) Distribution: Indonesia, Japan, Korea, Vietnam. Host plants other than rice: Alopecurus fulvus J. E. Sm., Hordeum vulgare L., Secale cereale L., Triticum aestivum L. Description and biology: The adult fly which looks like a small housefly is grey with three black longitudinal stripes on the thorax (Fig. 1.11). Female flies lay 50–100 small, white, elongated eggs singly on the leaf blades of rice seedlings in the nursery. The incubation period is 7 days. The adult flies live for a fortnight (Dale 1994). The maggots are white, translucent and about 1 mm long. The anal segment is bifid. The larvae migrate to the central whorl of the rice plant and start feeding. The larval stage lasts about 6 weeks. Pupation takes place between the leaf sheath and stem and the pupal period is 2 weeks. There are remarkable variations in the growth period of the insect in different regions of Japan (Tamura et al. 1959). The number of generations/year is two in the northern part of Japan and three in the south (Hirao 1970). The flies of the later generations oviposit on grasses where the emerging larvae overwinter. Plant damage and ecology: The rice stem maggot is an important pest of rice in Japan and Vietnam where crop losses up to 30% have been reported. In Vietnam, damage is more serious in the colder regions than in the warm areas. Upland rice and early varieties are more prone to infestation than irrigated and late-maturing varieties. The maggots are located near the growing point of the rice plant and feed on leaf blades. Tillering is reduced, and stunting results from early attack. Larvae of later generations feed on developing flowers and this reduces yield considerably. The type of damage differs in north and south Japan. In the north, where there are only two generations, the first brood larvae attack young leaves and growing tips of rice plants. However, in the south, where there are three generations, the first brood maggots infest young leaves while the second brood larvae attack only leaf tips (Uyeda et al. 1962).

Figure 1.11 Chlorops oryzae adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

Biology and ecology of rice-feeding insects: root and stem feeders

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1.11 Rice seedling flies, Atherigona exigua Stein and Atherigona oryzae Malloch (Diptera: Muscidae) Distribution: Asia (Bangladesh, India, Indonesia, Japan, Malaysia, Pakistan, Papua New Guinea, Philippines, Singapore, Sri Lanka, Thailand). Oceania and Africa (Seychelles). Host plants other than rice: Cynodon dactylon (L.) Pers., Panicum repens L., Paspalum sp., Saccharum officinarum L., Sorghum bicolor (L.) Moench., Triticum spp., Zea mays L. Description and biology: Adults resemble houseflies. The adult (Fig. 1.12) is a small fly, 3 to 3.5 mm long (Dale 1994). They have a distinct angular head with deep-set antennae, a grey thorax, yellow-spotted abdomen and yellow legs (Islam and Catling 2012). The adults are strong fliers and are only active during the daytime. The adults are attracted to plants less than a month old for oviposition and a female may lay 100 eggs during its lifetime. Eggs are laid singly on the underside of the leaves 3–5 days after mating, usually in the evening hours. Eggs are pure white, elongated and large in comparison to the adult. The incubation period is 3 days (Dale 1994). Newly emerged larvae are creamy white and move down the leaf blade on a film of dew in the early morning (Reissig et al. 1986). The maggots then burrow in the leaf sheath towards the base of the stalk. They moult three times in 6–10 days and then pupate inside the stem or in the soil within a small yellow puparium. Pupae are barrel-shaped and reddish brown in colour and turn to dark brown at the later stages. The pupal period last 8 days (Dale 1994). Adult emergence can take place any time of the day, but it occurs mostly in the afternoon (Rodriguez 1969). Adult longevity is 10–12 days (Dale 1994). Plant damage and ecology: Seeding maggots have a wide range of hosts including rice (CABI 2015c). They have been reported to be restricted to upland rice and do not occur in flooded wetlands (Reissig et al. 1986). However, Islam and Catling (2012) suspect that A.

Figure 1.12 Atherigona oryzae adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

oryzae is one of several dipterous maggots causing deadhearts in pre-flooded and deepwater rice seedlings in Bangladesh. Adult occurrence is highly seasonal. Damaging infestation levels normally occur during a period of 2–3 months, beginning several months after the onset of the rainy season (Reissig et al. 1986). Peak incidence of the pest in India was reported during the months of July and August (Senapati and Satpathy 1983). In Sri Lanka, the A. oryzae infestation was most serious on rice after a prolonged period of drought (Fernando and Manickavasagar 1957). The legless larvae (maggots) feed within the central shoot of rice seedlings by tunnelling downwards to the base (Dale 1994). Larvae feed by moving their mouth hooks back and forth in a rasping motion (Reissig et al. 1986). Larvae feed on developing tillers and decaying tissues and can kill tillers and form deadhearts similar to those due to lepidopterous stem borers. Severely damaged tillers turn yellow, become stunted and die. Less damaged tillers that survive exhibit discoloured or transparent patches of damaged leaf tissue along the margins and are readily torn by the wind. As a result the leaves become ragged and exhibit symptoms similar to whorl maggot, Hydrellia philippina, damage (Reissig et al. 1986). Maturity of plants that survive is delayed by 7–10 days.

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1.12 Black beetles, Heteronychus mossambicus Peringuey (= H. oryzae Britton); Coleoptera: Scarabaeidae: Dynastinae The Scarabaeidae family is divided into two groups: the ‘chafers’ or ‘white grubs’ (subfamilies Melolonthinae and Rutelinae), in which adults feed on tree leaves and the larvae feed on roots of living plants; and the ‘black beetles’ (subfamily Dynastinae), in which the adults feed on roots of living rice plants and the larvae, or grubs, feed on organic matter in the soil but do not feed on living plants. Other black beetle species from rice in Côte d'Ivoire in the WARDA Arthropod Reference Collection are Onthophagus spp., Geotrupes auratus Motschulsky, G. leaviatriatus Motschulsky, Schizonycha sp., and Bupachytoma sp. (Heinrichs and Barrion 2004). Litsinger et al. (1987) list the following species as occurring in upland rice in Africa: Heteronychus andersoni Jack, H. bituberculatus Kolbe, H. licas (Klug), H. mosambicus, H. arator (Fabricius), H. plebejus (Klug), H. pseudocongoensis Ferriere, H. rugifrons Fairmaire, and H. rusticus niger (Klug). The black beetle H. mosambicus is discussed here and the chafers Leucopholis irrorata in section ‘Chafers’ (white grubs)’. Distribution: Afrotropical – Burkina Faso, Chad, Congo, Ethiopia, Guinea, Mozambique, Nigeria, Senegal, Sierra Leone, Sudan, Tanzania, Togo, Zimbabwe (Global species 2015; Heinrichs and Barrion 2004). Host plants other than rice: Pearl millet, sorghum, maize, groundnut. Description and biology: The larvae of the scarab (Scarabaeidae family) beetles can be distinguished from other soil-inhabiting larvae by the swollen end of their abdomens. The adult black beetle, H. mosambicus, is about 10 mm long and reddish brown to black with reddish brown legs. The beetle breeds in decomposing plant material such as rotting weeds. Eggs are deposited singly. The larvae are typical grubs with a brown head and a white body. Larvae feed only on organic matter in dryland fields and do not feed on rice. The life cycle of this species is long, taking several months to pass through the egg, larval and pupal stages before they become adults. The adult black beetle can live up to 1 yr (Reissig et al. 1986). Plant damage and ecology: Feeding by the adults is restricted to non-flooded environments. Adults are highly mobile and, although sensitive to flooding, invade rice fields soon after they drain (Litsinger et al. 1987). The beetle attacks newly sown rice up to the age of 6 wk (COPR 1976). At Rokupr, Sierra Leone, the adults began feeding on rice at the two-leaf stage. The adults feed on rice stems and roots a few centimetres below the ground level. The first sign of damage is wilting of the central leaves, followed by the progressive wilting of outer leaves. Finally, the entire plant withers, turns brown and dies. The beetles move below the soil surface, leaving behind a raised track as they move from one seedling to another. Severely damaged fields have to be resown. Damage is most severe when the rice plants are exposed to drought when they are less able to replace the eaten roots. Another Heteronychus species, H. arator, causes similar damage to rice in South Africa (COPR 1976). In Madagascar, H. plebejus damages rice growing in humid soil during the dry season and H. mosambicus feeds on rice roots in Malawi (Grist and Lever 1969). An outbreak in Rokupr, Sierra Leone, occurred in direct-seeded rice near a mangrove swamp (Agyen-Sampong 1977). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

1.13 ‘Chafers’ (white grubs), Leucopholis irrorata (Coleoptera: Scarabaeidae, Melolonthinae) Distribution: Asia. Host plants other than rice: Wide range of plant species. Description and biology: Adult chafer beetles are greyish brown and densely mottled with minute, brownish spots (Fig. 1.13). The males are considerably smaller than females (Uichanco 1930). The male Leucopholis irrorata is 25 mm long and 14 mm broad; the corresponding measurements for the female being 30 mm and 16 mm, respectively (Otanes 1924). The beetles feed on leaves and fruits of various trees. Besides being a source of food, these trees serve as mating sites. Beetles, after mating, remain in the trees during the day and at night fly short distances to lay eggs in the nearby fields. Hence, more egg laying and a higher level of infestation are noticed in fields near trees. The beetles are attracted to light traps and light trap catches are the largest during new moon nights. Eggs are laid in the soil at a depth of 5 to 15 cm. They are creamy white and oval when freshly laid and measure on an average 3 mm long and 1.7 mm broad. The total number of eggs laid per female varies from 50 to 60. Colour changes as the development advances and the egg swells up to 4 mm in diameter, one or two days before hatching. Eggs are highly sensitive to dry weather and must be in moist soil to hatch. The egg stage lasts for 1 to 3 weeks. The newly hatched grub is creamy white in colour. The head turns brown and the larva becomes active in a few hours. The first instar larva can feed on the organic matter

Figure 1.13 Leucophilus irrorata adult (Source: not known). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

Biology and ecology of rice-feeding insects: root and stem feeders

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available in the soil but prefers plant roots. The second and third instar grubs require roots as their food for normal development and pupation. Larvae prefer moist soil, where the grubs are seen near the soil surface whereas in dry soil they remain close to a location in the soil where moisture is suitable. The larva can survive for more than 110 days within the earthen cell under low soil moisture levels but cannot survive for more than six days under water-saturated conditions (Veeresh 1977). In nature, continuous rain or a waterlogged condition in fallow land for 3 to 4 days forces the grubs to emerge from the soil where they are exposed to dehydration and predation by birds. The uneven distribution of white grub larvae within a field is due to their strict moisture requirement. There are three larval instars. The stadia are 1 to 2 weeks, 3 to 4 weeks and 4 to 8 weeks for first, second and third instars, respectively. In the tropics, the grubs feed on the roots of host plants from July to September. The maximum damage is usually done from the middle of August to early September when the grubs are fully grown. Mature larvae descend to a depth of 0.3 to 2.0 m in the soil during the dry season where they prepare an earthen cell and pupate. The pupal cells protect the dark brown pupae from drying out. Adult emergence starts by the last week of September and is completed by the end of November. The adult beetles remain inactive within their pupal cells till next April when they begin to leave the soil. There is only one generation of the pest in a year. The life cycle is completed in 11 to 16 weeks in the tropics. In temperate areas 2-year life cycles are common. The larvae are unable to tolerate low temperatures. The third instar grubs kept at constant temperatures of 4, 10, 15, 20, 25 and 30°C did not survive for more than a month except at 20 and 25°C (Veeresh 1977). Plant damage and ecology: The adults feed on leaves and fruits of various trees (Dale 1994). The larvae of chafers feed on roots and other subterranean plant portions of upland rice and many other crop plants (Dale 1994; Project Noah 2013). As the grubs grow they become voracious feeders causing enormous damage to crops. A single white grub is capable of destroying several plants. However, in older crops, plants are not killed outright. In such cases, yellowing followed by withering of the leaves occurs. Clustered distribution is a common feature of white grubs, and infestations often tend to occur in the same fields year after year (Veeresh 1977). Sporadic occurrence of chafers such as Anomala dimidiata, Holotrichia seticollis, H. longipennis and Popillia cupricollis has been reported on rice crops from India. Grubs of P. cupricollis damage roots of rice seedlings while adult beetles chew the rice grains at the dough stage. Rain at the beginning of the rainy season stimulates the overwintering adults of most species to become active and emerge from the soil. However, adults of Leucopholis irrorata in the Philippines revert to normal activity only a month after rains begin (Litsinger et al. 1983). They emerge from the soil leaving behind a small hole on the surface. The beetles then undertake feeding and a mating flight during night and return back to the soil before dawn. They are found in soil up to a depth of 0.3 m (Rai et al. 1969).

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Biology and ecology of rice-feeding insects: root and stem feeders

1.14 Colaspis beetles, Colaspis brunnea and Colaspis louisianae (Say) (Coleoptera: Chrysomelidae) Distribution: Southern USA. Host plants other than rice: Apples, beans, clover, cowpeas, grapes, lespedeza, pasture grasses, maize, potatoes, soybeans, strawberries and timothy grass. Description and biology: There are two species of Colaspis in Louisiana rice fields, Colaspis brunnea and Colaspis louisianae (LSU 2013). Colaspis flavida, reported as a rice pest in Arkansas (Rolston and Rouse 1965), is a synonym of C. brunnea (Kaeb 2006). Adults (Fig. 1.14) are oval-shaped, approximately 5 to 6 mm in length, light gold to light brown in colour, with long antennae and white/gold stripes running lengthwise down their bodies. The wing covers appear striped due to the presence of longitudinal rows of shallow indentations. Adults feed on the leaves of legumes and are occasional defoliating pests of soybean. Adults lay eggs in masses of five to 90, principally in legumes such as soybean or lespedeza. They mate soon after emergence and may mate several times during their life. The average longevities of the males and females are 7.8 and 13.4 days, respectively (Rolston and Rouse 1965). The pre-oviposition period lasts for 3 to 5 days. Eggs are laid in the soil around the roots of host plants. The smooth, white to yellow egg is about 0.6 by 0.25 mm. The incubation period is 6 to 9 days.

Figure 1.14 Colaspis brunnea adult (Source: LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Larvae are cream-coloured, C-shaped, soil-dwelling grubs about 5–7 mm in size in the late instars. Larvae have golden brown head capsules and feed on roots of legumes, rice and grasses. Larvae spend up to 7 months in cells pressed slightly into or on the soil. Pupation occurs in the soil and the pupae remain in the soil for 3 to 7 days until adults emerge. The 4-mm-long pupa is whitish at first, and then gradually darkens. There are probably two to three generations per growing season, and larvae of the last generation overwinter as larvae. These insects cannot complete their life cycles on rice, but larvae remaining in soil from the previous fall will attack rice planted in spring. The Colaspis species overwinter as larvae near the boundary of the subsoil and topsoil. The larvae (Fig. 1.15) suffer considerable mortality from spring tillage. The surviving larvae move upward and start feeding about the first week of May. Pupation begins in late May and continues until late June. The first brood of adults starts ovipositing from about the beginning of June until mid-August. Some larvae may not pupate until the following spring; others pupate in late July or August and produce a second brood of adults. These adults are responsible for the overwintering larvae that develop in late fall. Plant damage and ecology: Damage is mostly confined to dry-seeded fields. Highest larval populations are seen in less compact soils. The larvae will feed on the roots of a plant, such as rice, when it is planted into a field that is already infested with the developing insect from the previous year. The Louisiana species can be found damaging the fields of dry-seeded rice in a soybean–rice rotation. Colaspis will complete a single generation in soybeans, lespedeza or pasture plants.

Figure 1.15 Colaspis brunnea larva (Source: LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

In the spring, the overwintering grubs feed on germinating seeds, roots and seedlings reducing the crop stand and tillering. Damaged plants are observed to be stunted, withering, dying and surrounded by declining plants. Damage is manifested as seedling death and reductions in plant stands, with stand losses reaching as high as 50% in some cases. Because of the feeding and ovipositional habits of this insect, infestations are usually confined to fields that had been planted with soybeans the previous year. Infestations are also more common in higher areas in fields.

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1.15 Rice root weevil, Echinocnemus oryzae Marshall (Coleoptera: Curculionidae) Distribution: India. Host plants other than rice: Fimbristylis tenera Roem. & Schult. and many wild grasses. Description and biology: It is likely that this insect is primarily a pest of grasses and it has only secondarily taken to rice. The distribution of the pest is rather restricted to the deltaic regions of India that have been brought under rice farming (Singh and Kalkat 1956). Clay and heavy loam soils favour the incidence. The insect does not seem to occur in sandy soil (Thirumala Rao 1952). Eggs are laid at the base of plants. The incubation period is 3–4 days. Larvae are translucent white and about 5 mm long with six pairs of prominent tubercles on the dorsal side of the abdomen. These structures serve a respiratory function by taking in oxygen from the roots. The larvae burrow down into deeper layers of soil to remain in a resting condition and later pupate. The grub overwinters in soil at a depth of 25–30 cm, after September. The larval period lasts for 11 months. It pupates during May. The pupal period is 10–12 days (Dale 1994). Adult weevils have an oblong body and are shiny black or piceous and densely covered with grey scales. They lack the white spots on the elytra as seen in E. squameus and the rostrum is shorter (Fig. 1.16). They emerge with the onset of the monsoon towards the end of May. The beetles are usually found on grasses and, after pairing, give rise to a new generation of grubs that can be seen among rice roots from July to September. There are two generations per year.

Figure 1.16 Echinocnemus oryzae adult (Source: IRRI).

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Biology and ecology of rice-feeding insects: root and stem feeders

Plant damage and ecology: The rice root weevil, E. oryzae, was considered a minor pest of paddy (Singh et al. 2012) but it has become an important pest in some river basins in India (Dale 1994). Adults feed on leaves of newly transplanted rice (Reissig et al. 1986), but seldom cause economic damage (Dale 1994). Larvae feed on roots during the wet season http://www.indiaagronet.com/indiaagronet/pest_management/CONTENTS/Pest%20 of%20rice.htm#pestofrice. Grubs devour the fibrous roots of rice plants, and the attacked plants become stunted and tillering is reduced. Presence of dead plants in large patches is a typical symptom. Plants attacked during tillering show more damage symptoms than plants damaged after tillering. Damage is most severe in the newly transplanted crop during July–August. In severe cases, the plants wither and the field has many patches that have to be filled by transplanting fresh seedlings. Once the plant is established, the chances of withering are low. Yield losses are seldom severe (Dale 1994).

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1.16 Rice plant weevil, Echinocnemus squameus Billberg (Coleoptera: Curculionidae) Distribution: China, Indonesia, Japan, Korea, Ryukyu Island, Taiwan. Host plants other than rice: Alisma plantago-aquatica L., Callitriche verna L., Cyperus rotundus L., Echinochloa colona (L.) Link, Potamogeton natans L. Description and biology: The adult weevils have elytra with a pair of whitish oblong spots on the apical one-third of stria 2 and 3 and the rostrum is much longer than wide and more or less cylindrical (Fig. 1.17). The adults emerge from hibernation and migrate to rice fields by the end of May. In Japan migration to the rice fields coincides with the transplanting time. Plants adjacent to levees are most prone to damage by the beetles. The beetles walk on the surface of water and dive under water or swim. Females dive under water and lay their eggs singly on soil close to the rice plant (Reissig et al. 1986). Water is indispensable for the development and hatching of eggs (Kuwayama 1963). The incubation period is 6 to 10 days. The newly hatched grubs burrow into the soil (Dale 1994). The spiracles are modified to six paired dorsal hooks on the lateral side of the larvae, which under flooded conditions are thrust into roots to obtain oxygen. Larval feeding occurs on decayed organic matter and rarely on plant roots. The full-grown grubs usually pupate by the end of September, but are unable to pupate under flooded conditions (Oya and Sato 1978). Overwintering sites are low-lying areas and stubbles in rice fields. But adults often hibernate on the roots of grasses on levees. There is one generation annually. Plant damage and ecology: E. squameus is a sporadic minor pest of rice. Adult weevils feed on the leaves of young rice plants at or near the water surface. Feeding damage is

Figure 1.17 Echinocnemus squameus adult (Source: IRRI).

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Biology and ecology of rice-feeding insects: root and stem feeders

evident by a few longitudinal scars that are visible on the leaves when they open. Maximum damage is caused to plants 3 to 4 weeks after transplanting. The infected plants are stunted and do not tiller normally. Sometimes irregular and delayed flowering also occurs (Kojima et al. 1981). In severe cases, the affected plants break at the site of insect feeding due to wind or submergence. Larval injury on roots is seldom noticed (Kuwayama 1963).

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1.17 Paddy root weevil, Hydronomidius molitor Faust (Coleoptera: Curculionidae) Distribution: India. Host plants other than rice: Fimbristylis sp. Echinochloa sp. and other grasses. Description and biology: The adults start emerging after the first showers in June. The adult weevil (Fig. 1.18) measures 4.5 mm in length and 2.2 mm in width. Freshly emerged weevils are light brown in colour, changing to dark brown to black at later stages. Adults are semi-aquatic and are capable of swimming in water. They mate 3 to 4 hours after emergence and females lay their eggs on the soil near the roots of grasses. The eggs hatch in 7 days (Reissig et al. 1986, Dale 1994). Grubs begin hatching in early July. They are translucent white in colour. Grubs crawl down to the root zone and first feed on the root hairs and later on the roots. The maximum larval population is observed in late July, which coincides with the main transplanting season. The active feeding stage lasts from August to September, after which the larvae move down into deeper layers of soil where they remain in an inactive resting stage during the winter and summer. Most of the grubs occur at a depth of 25 to 30 cm (Singh and Chaudhary 1968). There is a short pupal stage of 10 to 15 days before adult emergence in June. There appears to be only one generation of this insect in a year. Plant damage and ecology: This pest is a serious problem in rainfed wetland and irrigated wetland fields in many parts of Bihar, Gujarat and Haryana in India where damage up to 30 to 50% has been reported (Kushwaha and Sharma 1980). Even though adult weevils have

Figure 1.18 Hydronomidius molitor adult (Source: IRRI).

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Biology and ecology of rice-feeding insects: root and stem feeders

been observed feeding on rice leaves, the damage caused by them is negligible. Grubs feed on the roots of young transplanted rice plants (Talwar 2014). Regenerating roots are also subsequently destroyed by larval feeding. The attacked plants become stunted and tillering is reduced. The leaves turn yellow, develop a rusty appearance and in severe cases, plants are even killed (Kushwaha et al. 1983). But once plants are established, larvae cause little damage.

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1.18 Rice water weevil (Lissorhoptrus oryzophilus Kuschel) (Coleoptera: Curculionidae) Distribution: Lissorhoptrus oryzophilus Kuschel is native to North America east of the Rocky Mountains and north to Canada and is the most important invertebrate pest of rice in the USA. Populations of this species have invaded California (in the 1950s), Japan (1970s), Korea and China (1980s), and, most recently, Italy (2004), and this insect has become a serious pest of rice in all areas where it has been introduced (Aghaee and Godfrey 2015). Various other species in this genus are reported as pests of rice in Central and South America. Lissorhoptrus brevirostris (Fig. 1.19) and L. isthmicus have been reported from Cuba (Carbonell 1983) and Puerto Rico (Pantoja and Medina-Gaud 1988). In South America, L. bosqi is important in Colombia (Pantoja et al. 1997) and L. tibialis is found in Brazil (Ferreira and Martins 1984). Host plants other than rice: Many plants belonging to the families Alismataceae, Commelinaceae, Cyperaceae, Juncaceae and Poaceae. Description and biology: Invasive populations are parthenogenetic, whereas the species is sexual in its native range. Rice water weevils are semi-aquatic weevils that specialize on plants in the Poaceae and Cyperaceae (Tindall and Stout 2003, Lupi et al. 2012, O’Brien and Haseb 2014). The biology of L. oryzophilus is representative of the genus. Adults of L. oryzophilus (Fig. 1.20) are greyish brown and about 3 mm in length; markings are variable but most adults possess a brownish V-shaped area on their backs. In the females, this area is more distinct and the abdomen more swollen. Adult rice water weevils overwinter in bunch grasses, leaf litter and plant debris, often in riparian areas. Adult emergence from overwintering is influenced by temperature (Zou et al. 2004). Adults fly

Figure 1.19 Lissorhoptrus brevirostris adult (Source: Florida A&M University, USA; www.famu.edu). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

to rice fields and feed on leaves of young rice plants and other grassy weeds in proximity to rice fields. Oviposition is triggered by standing water, and larval infestations usually commence when fields are flooded (Stout et al. 2002). The gravid female moves down the stem and lays eggs in or under the basal submerged portion of leaf sheath tissue and, rarely in the roots. Maximum egg laying occurs one or two weeks after flooding. The egg is white, elongate and slightly curved. It is about 0.8 mm long. The egg stadium lasts for 4 to 9 days depending on temperature (Raksarart and Tugwell 1975). Larvae are white, very small and legless. The head is brown, and small in relation to the rest of the body. The first instar grubs mine in the leaf sheath for about a day and then move down the plant to the soil where they start feeding on roots. Larvae possess dorsal hooks that are modified abdominal spiracles. These structures facilitate larval movement in the soil and help in the acquisition of oxygen from the root aerenchyma (Everett 1966). Larvae develop through four larval instars (Cave and Smith 1983) and a pupal stage under flooded conditions in three to six weeks, depending on temperature (Agahee and Godfrey 2014). Larvae attain a maximum length of 8 mm in a period of approximately 21 days. Pupation takes place in oval mud cells lined with a watertight material, which is attached to the roots (Fig. 1.21). The pupa is white and of the same size as the adult weevil. Adults that emerge from pupae may fly to overwintering sites or initiate a new generation. The number of generations per year varies from one in temperate areas to several in tropical and subtropical areas.

Figure 1.20 Lissorhoptrus oryzophilus adult (Source: LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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In Japan, only one or sometimes two generations are recorded in a year (Tsuzuki et al. 1982). But in southern Louisiana, under optimal conditions, up to 4 generations occur. Successive generations take place within the same rice field only when there is no crop in the seedling stage in the area. By the end of August, the weevils move to overwintering sites such as woodland leaf litter, clumps of grass or rice stubbles. Adult overwintering populations are generally higher in moist places than at dry sites. The weevils come out of overwintering areas and start feeding on grasses from late April to early May. They then fly into rice fields that are transplanted in May. The period of oviposition of the water weevil is mostly governed by the duration of day light in the locality. Plant damage and ecology: The rice water weevil is the most important pest of rice in the United States. The adult feeds on the leaf epidermis of young rice plants. Feeding by adult rice water weevils on leaves is rarely damaging enough to warrant treatment. All stages of flooded rice are susceptible to oviposition, although preference is shown for rice in the tillering (vegetative) stage (Stout et al. 2013). Economic losses stem from extensive injury to root systems that result in reductions in vegetative growth, tillering, panicle densities, grains per panicle and grain weights of rice plants. Several analyses of weevil density–rice yield relationships suggest that each larva present on rice roots is associated with an approximate loss in yield of 1% (Agahee and Godfrey 2014). Yield losses up to 75% have been reported (Newsom and Swanson 1962; Grigarick 1963) due to the infestation of the water weevil.

Figure 1.21 Lissorhoptrus oryzophilus pupae on roots (Source: LSU AgCenter).

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Biology and ecology of rice-feeding insects: root and stem feeders

A parthenogenetic strain of the pest is believed to have been introduced into Japan from California in 1976. L. oryzophilus is regarded as one of the most destructive pests of rice in Japan and probably one of the most difficult to control (Okada 1982). The population densities in all stages of the pest are higher in those rice fields with standing water throughout the cropping season than in fields that are only intermittently irrigated (Yasuda et al. 1979). Shimohata and Kano (1982) observed that the weevils feed more and produce more eggs on younger rice seedlings. The critical minimum temperature for adult female survival in Japan was found to be as low as 5 to –10°C (Tsuzuki et al. 1979). This demonstrates the ability of the pest to survive in low-temperature regions and to cause damage to rice crops there.

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1.19  Gorgulho aquático do arroz (Oryzophagus oryzae) Distribution: Oryzophagus oryzae was first identified in Brazil (Costa Lima 1936) where it is distributed throughout the rice-producing regions. It is also present in Argentina, Uruguay and Paraguay (Wibmer and O’Brien 1986). Host plants other than rice: Echinochloa and weedy grasses. Description and biology: Adults (Fig. 1.22) have grey to brown bodies with white spots on the wings and pronotum and teardrop compound eyes. Length ranges from 2.6 to 3.5 mm (Martins and Prando 1980). During winter, the adults hibernate in rice stubble, tussocks and bamboo litter, and fly to rice fields when they are flooded in spring. Weedy grasses such as Echinochloa spp. can serve as alternate hosts for feeding (Martins 2005). Deep water and plants in the tillering stage are preferred for feeding and oviposition (Moreira 2002). During the five larval stages the typical white larvae (Fig. 1.23) cause severe damage to the roots. They pupate and form a cocoon, which is attached to the roots of rice plants. The duration of the life cycle from egg to adult varies according to temperature, but the occurrence of two generations during the rice-growing season is common. In the time between harvests (April–October), the adults hibernate in the rice field or at the base of gramineous or cyperaceous plants or on the ground of forests or eucalyptus and pine trees or even under dry leaves.

Figure 1.22 Oryzophagus oryzae adult (Source: Borges & Consultores Associados, Brazil; http://www. agrolink.com.br). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

Figure 1.23 Oryzophagus oryzae larva (Source: Eduardo Rodrigues Hickel, courtesy of University of California Statewide IPM Program, USA. The photo is copyrighted by the Regents of the University of California, USA).

Plant damage and ecology: O. oryzae is the most damaging insect in flooded rice in southern Brazil. As with Lissorhoptrus species, economic losses result primarily from larvae feeding on roots. Adult damage injury is economically important only in the water-seeded, pre-sprouted cultural systems because seedlings are vulnerable to injury. The first generation is most damaging, because the population density is high and the damage occurs early when the root system has not yet completely developed. The second generation, on the contrary, coincides with the phase of development when the plants are more developed and thus are more tolerant to feeding damage. In flooded rice, with three to four leaves, each larva on the roots is associated with a yield loss of 1–1.5% (SOSBAI 2014).

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1.20 Rice water weevil (Afroryzophilus djibai Lyal) (Coleoptera: Curculionidae) Distribution: Casamance, Senegal. Host plants other than rice: Wild rice species. Description and biology: Afroryzophilus djibai was originally thought to be the rice water weevil, Lissorhoptrus oryzophilus Kuschel, one of the major pests of rice throughout the Southern USA rice belt and in California. However, the West African weevil has proved not to be Lissorhoptrus but, as described by Lyal (1990), is a previously unknown genus and species. The larvae of A. djibai are very similar in appearance to those of Lissorhoptrus species, differing only in having dorsomedial spiracles on abdominal segment I and conical dorsal projections on the terminal abdominal segment. Pupae are similar to those of Lissorhoptrus, differing only in their smaller size and elongate shape. Adult Afroryzophilus differ from all other members of the subfamily Erirhininae in that their mandibles are toothed externally. The biology of A. djibai is not well known; however, Lyal (1990) provides a brief description. In general, it is similar to that of L. oryzophilus, which has been studied extensively in the United States (Bowling 1967) and Japan (Okada 1982). The adults feed on the rice leaves and oviposit within the leaf sheath. Larvae, upon hatching, move down to the rice roots where they feed. The presence of the dorsal spiracular hooks indicates that the method of obtaining oxygen, when submerged in flooded paddies, is similar to that in Lissorhoptrus. Although not confirmed by research, this is most likely accomplished by the piercing of inflated cells of submerged rice roots. Plant damage and ecology: A. djibai lives exclusively in the muddy waters of inland valleys. It has been found in flooded rice fields adjacent to mangrove swamps and the Casamance River in Senegal (Djiba 1991). The harmful stage is the larva, which feeds exclusively on rice roots. It is aquatic as a larva and the larva is only found in flooded fields. The adults make longitudinal feeding scars on the leaves. However, major damage is caused by the larvae that feed on the roots. The reduced root volume affects plant growth and heavy infestations most likely delay maturity and reduce yield (S. Djiba, Institut Senegalais de recherches agricoles, 1996, pers. comm.). Based on yield loss studies and the known economic importance of L. oryzophilus in the United States, Lyal (1990) suggests that A. djibai may have potential to cause serious damage to rice in West Africa.

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Biology and ecology of rice-feeding insects: root and stem feeders

1.21 African subterranean termites, Macrotermes (Macrotermes bellicosus (Smeathman), Pseudacanthotermes militaris (Hagen)); Microtermes (Microcerotermes parvus (Haviland), Armitermes evuncifer Silvestri, Trinervitermes oeconomus (Tragardh)) (Isoptera: Termitidae) Distribution: Various species are distributed throughout Africa. Host plants other than rice: Maize, millet, sorghum, wheat, barley and teff. Description and biology: Subterranean termites, of the family Termitidae (subfamilies Macrotermitinae, Termitinae and Nasutitermitinae), are common pests of upland rice in West Africa, where they may cause serious damage during dry periods. Even though rice fields are small, and surrounded by perennial vegetation that can serve as a food host, African termites seem to prefer rice (Litsinger et al. 1987). Termites are primarily upland feeders but can occur in light-textured soils in rainfed lowland areas. They cannot survive in flooded fields (Reissig et al. 1986). All members of the order Isoptera share certain characteristics. They have pale, elongate bodies and are sometimes called ‘white ants’ because of their appearance. Reproductive

Figure 1.24 Macrotermes bellicosus queen and other castes (Source: Kjell Sandved/Visuals Unlimited, Inc., USA). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

Biology and ecology of rice-feeding insects: root and stem feeders

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individuals have two pairs of membranous wings, all of equal length. Termites shed their wings after mating. Their antennae are roughly the length of their heads. Termites are social insects living in colonies usually composed of a reproductive pair (king and queen) (Fig. 1.24) and many sterile workers (Fig. 1.25) whose activities include foraging, nest building and maintenance, care of eggs and young, and defence. As for the honeybees, the termite queen controls reproduction. However, in the termite world, the male reproductive or king stays with the queen and continues to fertilize her eggs for life. Winged reproductives, called alates, swarm on warm days to find their mates. Successful pairings settle down and begin reproducing. Termites undergo simple metamorphosis. Sterile termite workers perform the hard labour, building and maintaining the nest and caring for the young and the queen. Soldier termites defend the nest. In most species, the soldiers’ specialized defensive structures are found in the head region, making them true ‘muscleheads’. The Trinervitermes (Nasutitermitinae) are characterized by a soldier head, which is extended anteriorly into a tube that emits an adhesive-like repellent for chemical defence. To consume fibrous plant matter, termites have chewing mouthparts. The Macrotermes and Microtermes (Macrotermitinae) lack symbiotic protozoa to help digest plants. Instead, they are fungus-growing termites and depend on the breakdown of plant material in their food through a sophisticated form of symbiosis with a basidiomycete fungus, Termitomyces, which is cultivated within the nests on fungus combs constructed from faecal material (Cowie et al. 1990).

Figure 1.25 Macrotermes bellicosus worker castes (Source: http://www.tier-fotos.eu/; photographer: Professor J. Renoux). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: root and stem feeders

Plant damage and ecology: Of the approximately 2500 termite species in the world, about 300 are recorded as pests (Logan et al. 1990). In Nigeria, 120 species have been identified, but only 20 damage crops and buildings (Logan 1992). Togola et al. (2012) reported 6 species infesting upland rice in Benin. Although most termite species feed on dead plant materials, a few attack living plants in the soil. Under adequate rainfall, termites cause little damage, but they can destroy drought-stricken rice plants. Harris (1969), IITA (1971) and Malaka (1973) have reported that Macrotermes, Microtermes and Trinervitermes feed on upland rice in Nigeria. Nineteen species of termites have been associated with upland rice in Nigeria, of which Macrotermes is the most common and destructive genus (Obasola et al. 1981). Wood and Cowie (1988) considered termites to be the most significant soil pests of crops in Africa. They cited examples of damage to maize, sorghum, wheat, barley, teff and upland rice by Macrotermes and Microtermes. Microtermes feed on the plant's root system, whereas Macrotermes cut seedlings at the base of the stem just below the soil surface or just above the soil surface. Trinervitermes are foragers that feed on green and dry leaves and inflorescences of grasses. In a study conducted in Cotonou, Benin, on specific diversity and damage of termites on upland rice, it was evident that the specific diversity varied not only according to the environment, but also according to rice phenological stage. Microcerotermes parvus, Pseudacanthotermes militaris and Microtermes sp. were the most abundant species at the tillering stage; M. parvus, Armitermes evuncifer, P. militaris and Microtermes sp. were

Figure 1.26  Macrotermes bellicosus mound in Burkina Faso (Source: Guillaume Mazille and Marie Schneider; www.obturations.com). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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the most abundant at the heading stage; and Microtermes sp., M. parvus and A. evuncifer were the most common at maturity (Togola et al. 2012). Logan et al. (1990) mention several generalizations with respect to the severity of termite feeding as affected by ecological conditions. Feeding is generally more severe on exotic or introduced plant species or varieties than on indigenous ones, presumably because the latter have evolved some level of resistance. Feeding is more severe on plants that have been subjected to abiotic and biotic stresses such as drought, diseases, weeds, lack of fertilizer, and mechanical or fire damage. Crops planted at low altitudes are more likely to be attacked than those in highland areas because altitude often limits termite distribution. In Africa, both Trinervitermes and Macrotermes build mounds (Fig. 1.26). Macrotermes build large epigeal nests (mounds), which house many thousands or even up to 2 million termites (Collins 1981), and construct shallow subterranean foraging galleries radiating from the nest for distances up to 50 m (Darlington 1982). The main galleries give rise to a network of smaller galleries from which foraging parties exploit potential food resources over extensive areas. Their usual food is dead wood, grass and dung. They forage on the surface, often under the cover of earthen runways that protect them against desiccation and predators. Normally, crops are not affected, but under dry conditions and when alternative food is scarce, crops can be damaged (Kooyman and Onck 1987). Macrotermes feed on plants at the seedling stage, attacking them at the base of the stem. Usually, the seedlings are completely severed, resulting in low plant populations (Wood and Cowie 1988). Farmers in areas where Macrotermes damage is prevalent use higher than recommended sowing rates to compensate for the expected loss of seedlings. Macrotermes occasionally cut the base of older, well-established plants, but this is insignificant compared with the seedling damage. Microtermes, which are strictly subterranean, do not build mounds. Their nests consist of a diffuse network of galleries and chambers. The chambers, in which the fungus combs are located, have a subspheroidal shape and a diameter of 2–4 cm. Galleries have a circular cross section of 800–1200 cm. Both the chambers and galleries are plastered with clay and saliva, and have a glossy appearance (Kooyman and Onck 1987). A study conducted at AfricaRice, Ibadan, Nigeria showed that termite attack on the plant root predisposes it to fungi attack (Oyetunji et al. 2014). In Benin, Armitermes evuncifer is found in rice fields during the entire crop growing period. It builds nests or makes underground galleries. Pseudacanthotermes militaris is present in rice fields throughout the cropping cycle but is most damaging on the tillering and heading stages. It can stay on the soil surface as well as in underground tunnels. Its damage was observed on dried grasses and lodged rice but caused minor damage to non-lodged rice plants (Togola et al. 2012). Trinervitermes build small mounds from which they forage on a wide range of grass species (Cowie et al. 1990). The Trinervitermes genus in Nigeria is composed of two groups: those that store grass fragments in their mounds and those that do not (Sands 1961). The grass storers are T. ebenerianus Sjostedt, T. carbonarius Sjostedt and T. suspensus Silvestri. The non-storers are T. oeconomus (Tragardh) and T. auriaterrae Sjostedt. T. ebenerianus emerges from holes in the mound or from subterranean tunnels and forages at night in about a 10-m radius around the mound. Foraging in northern Nigeria ceases during the wettest months (July to September) and during the cold, dry months (November to February).

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Biology and ecology of rice-feeding insects: root and stem feeders

Termites also have some positive attributes in enhancing soil fertility. However, there is little information on the overall value of termites to the small-scale farmer and on the extent that the beneficial value of termites outweighs the damage that they cause (Logan 1992). Termites process 8% of the annual litter production in the Sahelian dry savannas of Senegal and 28% of the litter production in the humid savannas of Côte d'Ivoire. In studies conducted in the humid savanna zone in Côte d'Ivoire, the food habits result in the preservation of energy and nutrients from fire damage and thus, termite foraging activities are beneficial for the savanna ecosystem (Lepage et al. 1993).

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1.22 South American root-feeding termites, Procornitermes triacifer, P. araujoi and Syntermes molestus (Isoptera: Termitidae) Distribution: Both genera, Procornitermes and Syntermes, are distributed in South America in regions with hot summers and mild winters. Procornitermes triacifer and P. araujoi are typical from the central regions of Brazil (Mato Grosso, São Paulo and Goiás) (Emerson 1952). Syntermes molestus has a wider distribution, and is also found as a pest in rain forests in the Amazon (Emerson, 1945; Martius 1998). Although these two genera are cited as the most important, the termite fauna is very diverse in upland rice fields in South America. A field study in Goiás, Brazil, showed 13 genera of termites feeding on rice roots (Czepak et al. 1993). Host plants other than rice: Many plant species. Description and biology: These termite species are social insects that nest under or above ground. Three castes are present in termite colonies: nymphs that can become workers, soldiers or reproductive adults. Workers are the caste that is involved in the feeding of nest mates, so it is members of this caste that feed on the rice roots. Termite workers have soft white bodies measuring 5–10 mm in length; are asexual; and lack wings, compound eyes and ocelli. Soldiers are also wingless but differ from workers in possessing larger heads and mandibles. Despite the developed mandibles, soldiers do not forage but only defend

Figure 1.27 Procornitermes araujoi soldier (Source: Christian Jost). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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the nest. Reproductive adults have dark brown to yellowish bodies, and are winged with eyes and ocelli. They leave the colony in the beginning of the rainy season to find a suitable place to mate and start a new colony (Ferreira 1998). Soldiers are the easiest individuals with which to identify the termite genus: Syntermes soldiers have one or more sharped thorax segments, while the other has rounded side segments. Procornitermes soldiers have the bristles on the tibia of the foreleg (Fig. 1.27) as long as the apical spur (Ferreira and Barrigosi 2006). Plant damage and ecology: Termites are serious pests of rice in upland cultural systems, especially in sandy and deep soils and where the crop rotation is with another grass. Termites prune plant roots, often causing plant death, resulting in low plant populations. Young plants are more likely to be attacked, and often show signs of water stress (dry, folded leaves during hottest hour of the day) (Ferreira and Barrigosi 2006).

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Uichanco, L. B. 1930. Biological notes on adult Leucopholis irrorata Chevrolat, with a consideration of beetle collecting campaigns as a method of control against white grubs. Philippine Agriculturist 19(3):133–55. Uyeda, Y., Emura, K., Fujimaki, S. 1962. On the distribution of the rice stem maggot to repeat two or three generations a year in Niigata Prefecture. J. Niigata Agric. Exp. Stn. 13:1–16. Vásquez, J. M. N., Sánchez, G. G. 1991. Biology, habits and hosts of the chinch bug Blissus leucopterus (Say) (Hemiptera: Lygaeidae). Revista Colombiana de Entomología 17(1):8–15. Veeresh, G. K. 1977. Studies on the root grubs in Karnataka with special reference to bionomics and control of Holotrichia serrata Fabricius (Coleoptera, Melolonthinae). Univ. Agric. Sci. Mongr. Ser. 2. Hebbal, Bangalore, India. Wibmer G, O’Brien C. 1986. Annotated checklist of the weevils (Curculionidae sensu lato) of South America (Coleoptera, Curculionidea), American Entomological Institute, 563p. Wood, T. G., Cowie, R. H. 1988. Assessment of on-farm losses in cereals in Africa due to soil insects. Insect Sci. Appl. 9:709–16. Yano, K., Miyake, T. Eastop, V. F. 1983. The biology and economic importance of rice aphids (Hemiptera:Aphididae): a review. Bull. Entomol. Res. 73:539–66. Yasuda, H., Shimohata, T., Umlbuchi, T., Asano, T., Hirose, O., Yatsuhiro, O. 1979. The occurrence of the rice water weevil in late transplanted rice crop in Gihu Prefecture (in Japanese). Proc. Kansai Plant Prot. Soc. 21:52. Zou, L., Stout, M. J., Ring, D. R. 2004. Degree-day models for emergence and development of the rice water weevil (Coleoptera: Curculionidae) in Southwestern Louisiana. Environ. Entomol. 33(6):1541–8.

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Chapter 2 Biology and ecology of rice-feeding insects: stem borers and rice gall midges E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 2.1 Introduction 2.2 Stalk-eyed borer 2.3 Stalk-eyed fly 2.4 Gold-fringed rice borer 2.5 Dark-headed stem borer 2.6 Spotted stem borer 2.7 American rice stalk borer 2.8 Rice striped borer 2.9 African striped rice borer 2.10 African white borer 2.11 Yellow stem borer 2.12 White stem borer 2.13 African pink borer (Sesamia calamistis Hampson) 2.14 African pink borer (Sesamia nonagrioides botanephaga Tams and Bowden) 2.15 Asiatic pink stem borer 2.16 South American white borer 2.17 Sugarcane borer 2.18 Lesser cornstalk borer 2.19 Mexican rice borer 2.20 Asian rice gall midge 2.21 African rice gall midge 2.22 References http://dx.doi.org/10.19103/AS.2017.0038.02 © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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2.1 Introduction Rice stem borers are a key group of insect pests, mostly belonging to the two lepidopteran families of Pyralidae and Noctuidae. According to Pathak (1968), pyralid borers are the most common and destructive of all stem borers and usually exhibit a high degree of host plant specificity. The noctuid borers, on the other hand, are polyphagous and only occasionally cause economic losses. A list of common stem borers is provided in Table 2.1. In Asia, Scirpophaga incertuIas and Chilo suppressalis are the major stem borers and are widely distributed from India to Japan. Although there are a number of species that feed on rice in West Africa, five are considered to be of major importance: the dipterous stalkeyed flies (Diopsis longicornis and D. apicalis) (Togola et al. 2011) and the lepidopterous species including the white stem borer (Maliarpha separatella), the striped stem borer (Chilo zacconius) and the pink stem borer (Sesamia calamistis) (Akinsola 1975, 1979; Alam 1988; Alam et al. 1985a). Various species of lepidopteran stem borers belonging to the families Pyralidae, Noctuidae and Crambidae attack rice in North and South America. The most important stem-boring species are Diatraea saccharalis (Fabricius), the sugarcane borer, which is the most widely distributed stem borer of rice in the New World and occurs from northern part of Argentina to the southern US; Eoreuma loftini, the Mexican rice borer, which is found in parts of northern Central America, Florida, and the Western and Southern US; Rupela albinella (Cramer), the white rice stem borer, which is found from Mexico to Brazil;

Figure 2.1 Deadheart damage (Source: F. Nwilene, Africa Rice Center). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Table 2.1 Global list of common rice stem borer species (Pathak 1975 modified) Scientific name

Common name

Distribution

Ancylolomia chrysographella Koll.

–

Southeast Asia

Chilo agamemnon Blez.

Small purple-lined borer

Africa

Chilo auricilius (Dudgeon)

Gold-fringed rice borer

Indian subcontinent, Southeast Asia

Chilo loftini (Dyar)

–

Mexico, United States

Chilo partellus (Swinhoe)

Pink borer Sorghum stem borer

Oriental and Ethiopian regions

Chilo phaeosoma (Martin)

–

Ethiopian region

Chilo plejadellus (Zinken)

Rice stalk borer American rice stem borer

Mexico, United States

Chilo polychrysus (Meyrick)

Dark-headed stem borer Rice stalk borer

Indian subcontinent, Southeast Asia

Chilo suppressalis(Wlk.)

Striped stem borer Rice striped borer Pale-headed striped borer Asiatic rice borer

Asia, Italy, Spain

Chilo zacconius Bleszynski

African rice borer

Africa

Diatraea saccharalis (Fabricius)

Sugarcane borer American sugarcane borer Small moth borer

Southern US, Central and South America

Diopsis spp.

Stalk-eyed borers

Africa

Elasmopalpus lignosellus (Zeller)

Lesser corn stalk borer

Neotropical, Trinidad, Brazil

Eoreuma loftini (Dyar)

Mexican rice borer

Mexico, United States

Maliarpha separatella (Rogonot)

White borer

Africa

Niphadoses gilviberbis (Zeller)

–

Burma

Niphadoses palleucus Common

–

Australia

Phragmatiphila spp.

–

Australia

Proceras indicus (Kapur)

Internodal borer

Indian subcontinent

Rupela albinella (Cramer)

South American white borer

South America

Scirpophaga incertulas (Wlk.)

Yellow stem borer

Asia

Scirpophaga innotata (Wlk.)

White rice borer White stem borer

Asia, Australia

Sesamia botanephaga (Tams & Bowden)

–

Ethiopian region

Sesamia calamistis (Hampson)

African pink borer Mauritius pink borer

Africa

Sesamia inferens (Walker)

Pink stem borer Ragi stem borer Purple stem borer

Asia

Zeadiataea lineolata (Wlk.)

Neotropical corn borer Maize borer

Venezuela

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and Elasmopalpus lignosellus (Zeller), the lesser cornstalk borer (LCB), a polyphagous insect, which is important as a rice pest in Mexico, Central and South America, especially in upland system regions. In Australia, rice is attacked by a species of Phragmatiphila (Hely 1958). Damage caused by the various lepidopterous stem-boring species is similar. Feeding by early instar stem borers on leaves and within leaf sheaths produces characteristic orange-tan lesions but is not economically damaging. Feeding within the culm on the growing point and vascular tissue can sever the growing portion of the plant from the base of the plant. When feeding occurs during the vegetative stage of plant development, the tiller in which the larva is present often dies and fails to produce a panicle (deadheart) (Fig. 2.1). Rice is capable of partly or fully compensating for losses of tillers because of stem borer attack during vegetative stage by putting forth additional tillers (Lv et al. 2008). When feeding occurs after panicle initiation, feeding by a larva within a stem results in drying of the panicle. Affected panicles may not emerge or, if they do, do not produce grains, remain straight and appear whitish (whitehead) (Fig. 2.2). Some species, however, feed inside the stem without producing visible symptoms of deadhearts or whiteheads. Infestations in rice fields often involve multiple species of borers, and yield losses under severe infestations can reach as high as 60% (Lv et al. 2008). For every per cent of whitehead, 1 to 3% loss in yield may be expected (Pathak 1975). However, yield losses from stem borers have not been adequately characterised. The distribution, bionomics and ecology of the important stem borer pests are discussed herein.

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2.2 Stalk-eyed borer, Diopsis longicornis Macquart (Diptera: Diopsidae) Data collected on various Diopsis spp. indicate that D. longicornis Macquart is the most abundant and most important pest of rice (Vercambre 1982; Cocherau 1978). Distribution: Most of sub-Saharan Africa, including Benin, Botswana, Burkina Faso, Cameroon, Central African Republic, Chad, Côte d’Ivoire, Ethiopia, Gambia, Ghana, Guinea, Guinea-Bissau, Kenya, Liberia, Malawi, Mali, Mozambique, Niger, Nigeria, Senegal, Sierra Leone, Somalia, South Africa, Sudan, Swaziland, Tanzania, Togo, Zambia and Zimbabwe (Feijen and Feijen 2012). Host plants other than rice: Sorghum, millet, Cynodon dactylon, Cyperus difformis, Paspalum orbiculare. In addition to the above, many of the grasses of the Poaceae family have been reported as hosts by Descamps (1957), Zan et al. (1981) and Alghali and Domingo (1982). Description and biology: The adults, the largest of the various Diopsis species observed in rice, have a distinct black thorax and reddish-orange abdomen (Fig. 2.3). The flies are found in lowland areas with water throughout the year and occur in swarms in shady areas near streams and canals and on weeds along levees in fallow lowlands during the dry season. Age of the rice plant affects both the number of eggs laid and the oviposition substrate (Alghali 1983). Gravid females lay eggs singly on the upper surface of young

Figure 2.2 Whitehead damage (Source: F. Nwilene, Africa Rice Center). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: stem borers and rice gall midges

leaves, normally in the midrib groove of the sub-terminal leaf. In older plants, the eggs are placed on the leaf sheath (Alghali and Osisanya 1981; Alghali 1983). The peak oviposition period on the leaf blades occurs about 30 d after transplanting (DT), while oviposition on leaf sheaths occurs about 10 d later. Boat-shaped, striated eggs, 1.7 ± 0.4 mm, with a characteristic anterior projection are attached to the leaf with a glue-like substance that prevents them from being washed off in heavy rains (Hill 1975). Eggs are creamy white when laid but later turn to tan. Each female lays about 30 eggs over a 20-d period at the rate of a maximum of four eggs per day (Breniere 1983). Peak oviposition occurs at 30–40 DT and practically terminates by the end of the tillering stage (Alam 1988; Umeh et al. 1992). Virtually no eggs are laid and no deadhearts develop on 60-d-old plants (Alghali and Osisanya 1981). The eggs hatch 2–3 d after oviposition. The larvae are yellowish maggots, about 18 mm long and 3 mm wide. Two long extensions on the abdomen that end in black hooks pointed forward make the larvae easy to recognise. Upon hatching, they move down inside the leaf sheath and feed above the meristem on the central spindle of young leaves, causing deadhearts. Larvae move readily from one tiller to another. One larva can destroy up to 10 neighbouring tillers (Feijen 1979). Later generations feed on the developing flower head. The larval stage lasts for 25–33 d (Cocherau 1978). Prior to pupation, the larvae move to new tillers within the same rice hill or stay on the damaged tillers and move to the outer leaf sheaths. Pupation normally occurs in the first three leaf sheaths (Alghali 1984) of healthy tillers, generally one pupa per tiller. Pupa-bearing tillers remain healthy. The pupae, which are red with brown dorsal bands, are flat and almost triangular because of the compression

Figure 2.3 Diopsis longicornis adult (Source: © G. Goergen, Biodiversity Centre, IITA; www.iita.org). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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inside the stem. During the later stages, the winged adult can be seen inside the pupal case. After a 10- to 12-d pupation period, adults emerge and mating occurs on the rice plant. About 60 d are required from hatching of the larvae to the maturation and mating of the adults and egg laying for the next generation. Between 15 and 20 d are required after emergence before the females begin laying eggs. Two principal generations occur between June and October and a third less prominent generation during the off-season. Plant damage and ecology: The survey conducted in Côte d’Ivoire in 1995 indicated that Diopsis spp. were the most abundant group in the stem borer complex, based on a total of collections in all climatic zones, ecosystems and plant stages (Heinrichs and Barrion 2004). D. thoracica has been reported to be primarily a rice feeder but may feed on crop plants other than rice such as wild rices and grasses. Cyperus difformis, a weed commonly found in rice fields, on which eggs, larvae, pupae and adults have been found, may be a host plant during non-rice cropping seasons (Alghali 1979). Togola et al. (2011) reported the high contribution of rice ratoons in the sedentarisation of the Diopsis flies in rice fields. Although Diopsis larvae are present in stems throughout the crop growth period, they are most abundant in younger plants (Joshi et al. 1992), possibly because of low silicon deposits. This pest attacks rice plants early in the crop growth stage (usually under 10 cm), shortly after emergence in direct-seeded fields or shortly after transplanting. Adult populations are responsive to toposequence site. Heinrichs and Barrion (2004) reported that adult numbers increased at lower toposequence sites – being most abundant in the lowlands and least abundant in the uplands. Igbinosa et al. (2007) reported that D. longicornis is the most important pest of upland rainfed rice in Ekpoma, Edo State, Nigeria. In irrigated rice in Ibadan, Nigeria, adults appear before 20 DT and peak at 40 DT, at the beginning of panicle initiation (Alam 1988). Alghali (1983) reported oviposition in irrigated rice beginning at 10 DT and peaking at 30 DT. Deadhearts caused by D. longicornis appeared by 10 DT, peaking at 30 DT, and terminating by 60 DT. Oviposition on upland rice at M’be continued from 3 to 10 wk after sowing (WAS) with a peak occurring 4–5 WAS (Dankers 1995). Deadhearts caused by Diopsis spp. feeding were observed to occur by 6 WAS with a peak at 9 WAS. In mangrove rice in Gambia, Diopsis spp. were the most abundant of the five stem borers found in rice stems at the tillering stage, while M. separatella became the most abundant at flowering and maturity (Jobe 1996). In studies conducted in Malawi, Feijen (1979) found that larvae remain in the same stem till pupation, except when small seedlings are attacked. Other authors have reported that 3–10 stems are attacked by one larva. Pollet (1977) reported that larvae leave the stem at the first sign of necrosis and thus only 40% of the deadheart-damaged tillers examined were infested with a larva. Reports of yield losses caused by D. longicornis vary greatly. Several estimates of infestation levels and yield loss have been reported from Ghana. Schröder (1970) reported 35–60% hills were infested in a survey. In a wet season survey, 66% of the tillers and 100% of the hills were infested (Scheibelreiter and Apaloo 1972). Abu (1972) reported that D. longicornis cause 9% yield loss in the Volta Region, Ghana. In a screenhouse test conducted in Badeggi, Nigeria, Akinsola (1980b) reported yield losses of 5–19% when plants were infested at the nursery stage. Morgan (1970) reported severe damage by D. longicornis of rice grown in reclaimed mangrove swamps in Sierra Leone. Alghali and Osisanya (1984) conducted detailed studies on the effect of D. longicornis damage on rice yield components. The feeding of the larva significantly decreased the number of panicles produced (both total and mature); the percentage

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Biology and ecology of rice-feeding insects: stem borers and rice gall midges

of tillers with panicles, grain weight and the total yield of unprotected plants; and increased the number of immature panicles and time to 50% flowering. Compensation occurs through the production of new tillers, so yield reductions may not be directly related to percentage of damaged tillers. Production of new tillers, however, did not fully compensate for damaged tillers in most cultivars tested. Photoperiod-sensitive cultivars were better able to compensate for pest damage than photoperiodinsensitive cultivars. Compensation tillering may not contribute significantly to grain yield because of delayed and heterogeneous maturity within a field (Akinsola and Agyen-Sampong 1984).

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2.3 Stalk-eyed fly, Diopsis apicalis Dalman (Diptera: Diopsidae) Geographical distribution: Benin, Burkina Faso, Cameroon, Chad, Côte d'Ivoire, Gambia, Ghana, Guinea, Guinea-Bissau, Liberia, Mali, Mauritania, Nigeria, Senegal, Sierra Leone, Togo. Host plants other than rice: Sorghum, millet, Cynodon dactylon (L.) Pers., Cyperus difformis L., Paspalum orbiculare G. Forst. Description and biology: D. apicalis only occurs in West Africa where it is the dominant species in the genus with apical wing spots (Fig. 2.4). It is a typical stalk-eyed fly with a distinct red frons (Fig. 2.5). It commonly occurs in fields along with D. longicornis, but it is easily identified, as it is much smaller. Dalman in 1817 originally described and Feigen (1986) re-described the species based on specimens from Burkina Faso and Nigeria. D. apicalis is characterised by apical wing spots. However, there are about 10 apicalis-like Diopsis found in rice according to Feijen (1985). D. apicalis is a polyphagous species that is often seen in rice fields. Adults, larvae and eggs are similar in appearance to D. longicornis, but smaller. Adults have an apical, smoky rounded spot at the tip of each wing (Feijen and Feijen 2012). This character is absent in D. longicornis. According to Abu (1972) and Scheibelreiter (1974), D. apicalis oviposits exclusively on stems infested with D. longicornis. In a similar fashion to D. longicornis, D. apicalis

Figure 2.4  Diopsis apicalis adult on rice leaf (Source: http://animales--asombrosos.blogspot.com/ 2010/04/diopsis-diopsis-apicalis.html). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Biology and ecology of rice-feeding insects: stem borers and rice gall midges

deposits eggs on the last emerged leaf (Pollet 1977). Scheibelreiter (1974) found that three-fourths of the laid eggs were attached to the withering terminal leaf or were laid in the basal groove of the mid-vein of the sub-terminal leaf. The remaining eggs were laid on the stem below. D. apicalis’s life cycle is similar to, but shorter than, that of D. longicornis (Cocherau 1978). In the tropics, days from egg to adult are 15–17 compared with 44 for D. longicornis. Egg, larval and pupal stages are 36 h, 8–10 d and 6 d, respectively, compared with 50 h, 25–33 d and 10–12 d, respectively, for D. longicornis. In contrast to D. longicornis, the larvae complete their development within one stem (Morgan and Abu 1973). Plant damage and ecology: In the dry season, the flies are abundant in wet areas such as along rivers. In the rainy season, they move to rice fields (Feijen 1986). In three 1995 surveys conducted in Côte d’Ivoire, adults were more abundant in the Guinean savanna zone than in the forest zone in July, but were most abundant in the forest zone in August and October (Heinrichs and Barrion 2004). The larvae feed on healthy plants or on decomposed tissue that occurs after stem borer attack. According to Descamps (1957) the larvae exist as phytophages on healthy plants, as saprophytes on damaged plants or as predators of larvae of other species in rice stems. Scheibelreiter (1974) observed D. apicalis feeding on dead larvae of D. longicornis. Therefore, D. apicalis may be considered at times to be a beneficial insect, although Breniere (1983) believes its role as a predator does not make up for the damage it causes to the rice crop.

Figure 2.5  Diopsis apicalis adult front view (Source: http://animales--asombrosos.blogspot.com/ 2010/04/diopsis-diopsis-apicalis.html). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Chiasson and Hill (1993) studied the population density, development and behaviour of D. longicornis and D. apicalis in Guinea. At the beginning of the crop season, the adults of D. apicalis were as abundant as those of D. longicornis. Thereafter, they decreased until the end of the season when the D. apicalis numbers were half those of D. longicornis. Similar to D. longicornis, D. apicalis adult populations in a monthly planting study in Côte d’Ivoire were high in the plots planted in November and lowest in the May planting. In the same study, as based on an average of 12 planting dates (months), flies appeared shortly after transplanting and reached a peak at 6–8 WAT. The highest D. apicalis population occurred during December–January (planted in November), in the middle of the dry season and harmattan period (Heinrichs and Barrion 2004). The ‘harmattan’ is an annually occurring period of strong winds coming from the Sahara Desert and relatively low temperatures. It is possible that adults are brought in with the winds from the north. In Ghana, D. apicalis larvae were found to infest plants later than those of D. longicornis (Morgan and Abu 1973). Adults were found in the fields throughout the cropping period but peaked at about 8 WAT. Eggs and larvae were observed at about 40 DT, with eggs reaching a peak at about 60–70 DT and larvae reaching a peak about 2 weeks later. In studies in Guinea (Chiasson and Hill 1993), transplanted and direct-seeded rice had similar adult populations, but the number of larvae was 10 times greater in the directseeded fields as compared with the transplanted fields. Adult populations in studies at the WARDA M’be Station in Côte d’Ivoire were dependent on the spacing of transplanted seedlings and the seeding rate of direct-seeded fields (Heinrichs and Barrion 2004).

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Biology and ecology of rice-feeding insects: stem borers and rice gall midges

2.4 Gold-fringed rice borer, Chilo auricilius Dudgeon (Lepidoptera: Pyralidae) Distribution: Bangladesh, Bhutan, Burma, Cambodia, China, India, Indonesia, Laos, Malaysia, Nepal, Pakistan, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam (CABI 2015a). Host plants other than rice: Saccharum officinarum L.; Sorghum bicolor (L.) Moench.; many grasses, for example, maize; Sacciolepis; Scirpus; Rottboellia; Setaria; Echinochloa (Reissig et al. 1986). Description and biology: The range of the gold-fringed stem borer C. auricilius is similar to that of the dark-headed stem borer C. polychrysus and their appearance is similar (Reissig et al. 1986). However, there are slight differences between the two species in the markings of the wings. Both species coexist in Bangladesh but C. auricilius is always present in smaller numbers (Islam and Catling 2012). The following description on the bionomics of the stem borer is mostly based on studies conducted by Rao and Rao (1980) in India. Larvae have only four stripes (the dorsal stripe being absent), and their body is proportionately wider than in C. polychrysus; the species is separated from C. suppressalis only by slight differences in the thoracic chaetotaxy. The caterpillar moults six times before becoming a pupa. The larval period is about 30–32 days. Pupation takes place in the affected stems. The postero-lateral and postero-dorsal spines on the cremaster of the pupa are more prominent than on the other Chilo species. The pupal period lasts for 6 days.

Figure 2.6 Chilo auricilius adult (Source: not known). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The adult moth is straw to light brown colour with silver lines in the apical one-fifth of the forewing and several black dots at the tip of the forewing (Fig. 2.6). Moths mate between 8 and 9 pm. Gravid females lay eggs in masses on foliage, mostly on the undersurface of rice leaves. The scale-like pale yellow eggs overlap in the egg mass (Reissig et al. 1986). Occasionally, a few egg masses are laid on the leaf sheaths. Average oviposition period is 3 days and the maximum number of eggs is laid on the first day of egg laying. The average number of eggs laid per female was reported to be 123 during the entire oviposition period in an average of 9.5 egg masses. Eggs hatch in 5–7 days. Four generations occur in Taiwan and China, and 5–7 in India. The insect is active during and just after the monsoon (Dale 1994). Plant damage and ecology: Rice is not the preferred host for C. auricilius (Reissig et al. 1986), and it is a serious pest of sugarcane in India, Taiwan and China. It has become more abundant on rice plants and has become a major pest in the Indian states of Orissa and West Bengal and in Bangladesh. All stages of the rice plant are attacked. Damage by the boring of this pest in the stems of vegetative rice results in deadhearts and reduced tillering. Feeding in the reproductive stage results in whiteheads. C. auricilius was reported to cause around 30% loss in grain yield in Orissa (Rao 1964) and 20% in Bangladesh (Alam et al. 1964). This borer is common in upland rice in the Philippines.

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2.5 Dark-headed stem borer, Chilo polychrysus (Meyrick) (Lepidoptera: Crambidae) Distribution: Bangladesh, Brunei, Cambodia, China, India, Indonesia, Laos, Malaysia, Myanmar, Pakistan, Philippines, Thailand, Vietnam (CABI 2015b). Host plants other than rice: Echinochloa crus-galli (L.) Beauv., Hymenachne acutigluma (Steud.) Gilliland, Saccharum officinarum L., Scirpus grossus L., Setaria pallide-fusca (Schumach.) Stapf and C. E. Hubb., Triticum aestivum L., Zea mays L. Description and biology: Chilo polychrysus is the second most important rice stem borer in Bangladesh after the yellow stem borer Scirpophaga incertulas (Dale 1994). Before 1960, it was the most dominant species in Peninsular Malaysia (Manwan 1977) but since the introduction of double cropping with short-maturing varieties the yellow stem borer gradually took its place (Khoo 1986). In South India, it was first seen attacking the rice crop during the 1955–56 cultivation season and many serious infestations subsequently followed (Dale 1994). The adult moth (Fig. 2.7) is straw to light brown in colour with silver scales at the centre of the forewing with 6–7 tiny black spots at the tip of the forewings. The hindwings are yellowish white. Body length is 10–13 mm and wingspan is 16–25 mm (Islam and Catling 2012). The moths usually live for 2–5 days.

Figure 2.7 Chilo polychrysus adult (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The moths are active during the night and oviposition takes place between 7 and 11 pm. Eggs are laid in batches of 20–150 in longitudinal rows along shallow furrows on both surfaces at the basal portions of the leaves. They overlap each other and are scale-like in appearance. A single female moth can lay up to 480 eggs in 3 days. The egg is white when laid but turns black as it nears hatching. The fully developed embryo eats its way out of the eggshell, usually in the morning hours. The incubation period is 4–7 days (Dale 1994). The newly hatched larvae are greyish white and 1.3 mm long. They are distinguishable from other species by the head and prothoracic shield which are distinctly black. The first instar caterpillar moves down to the leaf base and bores into the outer leaf sheath. Sometimes the larva enters the midrib of a leaf and tunnels down into the leaf sheath. The attacked leaf sheath first appears yellow and then gradually dries up. If the rice plant is thick, stout and succulent, the larval and pupal development is completed within the peripheral leaf sheaths sparing the central culm. On the other hand, if the outer leaf sheaths are thin or dry, the caterpillar bores into the central shoot. One larva is usually found in a single stem. If the host plant is dead as a result of infestation or when it becomes congested with larvae, the larvae migrate to neighbouring plants. In such cases, the points of entry are indicated by plugs of faecal matter. The last instar larva measures about 21 mm in length. The head is brownish black while the body is creamy white with five distinct brown stripes along the back of the body (Fig. 2.8). The head and body are sparsely clothed with inconspicuous hairs. The full-grown caterpillar, just prior to pupation, makes an exit hole below which the feeding tunnel is cleared and lined inside with a loose layer of silken frass. There are six larval instars, and the larval period ranges from 20 to 41 days.

Figure 2.8  Chilo polychrysus larva in rice stem (Source: B.M. Shepard/International Rice Research Institute (IRRI)). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The newly formed pupa is dirty white to light straw coloured with the larval body stripes clearly visible. The colour subsequently turns deep brown to black. The pupal period lasts for 4–6 days. No dormancy or diapause has been reported. The number of generations in a year varies up to 12 depending on the climate and availability of host plants. Overlapping generations may occur throughout the year. The second and succeeding generations are usually more destructive. In the absence of rice plants, the larvae move on to alternate hosts. Plant damage and ecology: C. polychrysus is a polyphagous species attacking several cereal crops including rice, maize, wheat and sugarcane. A large number of plants are alternate hosts (Islam and Catling 2012). All stages of the rice crop are attacked. Adult insects lay eggs on the leaf sheaths. From the leaf sheaths larvae move towards the stems and bore the stems. Larvae enter into the pith and feed on the inner surface of the stem wall (mainly soft tissues of the pith). If larvae attack at the vegetative stage of rice plant growth the central leaf whorl turns into brownish colour and dries off rapidly. This symptom is called ‘deadheart’. Tillers cannot bear panicles and become dry. Sometimes panicles emerge but do not produce grains. As the panicles are empty, they become whitish in colour and remain straight. This symptom, very conspicuous in the rice field, is known as ‘whiteheads’. Rahaman et al. (2014) studied the abundance of the adults of five stem borer species in lowland Boro (winter) rice in Bangladesh. C. polychrysus was second in abundance to the yellow stem borer Scirpophaga incertulas and was most abundant in the tillering stage of the crop growth cycle.

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2.6 Spotted stem borer, Chilo partellus (Swinh.) (Lepidoptera: Pyralidae) Distribution: Asia and Africa (CABI 2015c). Host plants other than rice: Poaceae; Eleusine coracana (L.) Gaertn., Hemarthria altissima (Poir.) Stapf & C.E.Hubb. Hyparrhenia rufa (Nees) Stapf, Megathyrsus maximus, Panicum maximum Jacq., Pennisetum glaucum (L.), Pennisetum purpureum Schumach., Saccharum officinarum L., Setaria italica (L.), Sorghum bicolor (L.) Moench., Triticum aestivum L., Zea mays L., wild grasses. Description and biology: C. partellus, a native of Asia, is a pest that was introduced to Africa, most likely from India, in the early twentieth century. After arriving in Africa, it has spread to nearly all countries in Eastern and Southern Africa, and it is assumed that it has spread to Western Africa. C. partellus became established in East Africa in the 1950s. Since then it has spread to southern and central Africa and there has been an unconfirmed report from Benin in West Africa (CABI 2015c). It occurs in low- to mid-altitude areas (1230 m altitude and below). The insect is primarily a pest of maize and sorghum but as a rice pest it is particularly important in eastern India. It rarely occurs in lowland irrigated conditions, but is abundant in upland rainy conditions.

Figure 2.9  Chilo partellus adult (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Moths are yellowish to yellowish brown with a slender body (Fig. 2.9). The moths are small in size with wing lengths ranging from 7 to 17 mm and a wingspan of 20–25 mm. Forewings terminate with an acute tip and are straw coloured with one or two transverse rows of small dark brown dots. Hindwings are white with a marginal fringe. The hindwings of males are pale straw coloured and in females the hindwings are white. Usually male moths are darker and smaller than the female (CABI 2015c). Eggs are laid in two overlapping rows on all parts of the plant. They are oval, flat and whitish, and about 0.8 mm in length. About 300 eggs are laid by a single female. Hatching begins after 3–5 days. Young larvae feed on leaves for about 5–6 days after which they penetrate the midribs of leaves. The larvae are dirty white with setae borne on each segment. The larvae have four purple brown longitudinal stripes and are usually found with characteristically dark brown spots along the back, therefore giving off a spotted appearance (Fig. 2.10). When the larvae of the spotted stalk borer are fully grown, they produce a conspicuous reddish brown head. It has a plate on the dorsal surface of the thorax which is known as a prothoracic shield and is reddish brown to dark brown and shiny. The larvae enter the stem directly or through the growing point. They feed inside the stem until they become fully grown after 18–30 days (Dale 1994). During winter, in temperate zones the older larvae remain dormant in the stems and stubbles. In the tropics, continuous development occurs during the rainy season. In places where there is a distinct dry season, the pest enters a larval diapause after the rainy season. Diapausing larvae pupate after the first showers and the moths emerge a few days later.

Figure 2.10  Chilo partellus larva (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Pupation takes place within the stem and lasts for 6–12 days. Pupae are slender, 10–15 mm long and shiny. The pupae of C. partellus are light yellowish brown to dark reddish brown in colour. Plant damage and ecology: C. partellus with its wide host range is one of the economically most damaging pests in Asia and Africa, attacking all parts of the plant except the roots. C. partellus is an important pest of cultivated cereals, especially maize, sorghum, sugarcane and pearl millet (Pennisetum glaucum). It has also been recorded from rice, and from many grass hosts (CABI 2015c, Islam and Catling 2012). Young C. partellus larvae feed on leaf whorls, causing characteristic scars and holes. They later feed at the growing point, which may be killed. The dead central leaves then form a characteristic ‘deadheart’, especially in young plants. Older larvae tunnel extensively in stems; damage to inflorescences may interfere with grain formation, causing chaffy heads or ‘whiteheads’ in rice. Most of the information on yield losses due to C. partellus feeding refers to maize. In a yield loss study conducted in an irrigated rice field, in Bangladesh, Rahman et al. (2004) found that yield loss due to C. partellus was similar to that of C. polychrysus and C. suppressalis.

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2.7 American rice stalk borer, Chilo plejadellus Zincken (Lepidoptera: Pyralidae) Distribution: Mexico, the United States (Arkansas, Louisiana, Texas). Host plants other than rice: The host range of the stalk borer is similar to that of the sugarcane borer. Description and biology: Dr. L. O. Howard first observed this pest on rice near Savannah, Georgia, in 1881 and described it as a new species (Riley 1883). The stalk borer has a restricted distribution and serious infestations are only sporadic. The biology and description is given in Dale (1994). Rice stalk borer adults (Fig. 2.11) are about 2.5 cm in length. The forewings are white or pale brown with black scales (small black spots). Forewing edges have a row of metallic gold scales and black dots. The hindwings are white or pale brown; the wingspan is 20–40 mm. Flat, oval, cream-coloured eggs are laid at night on the leaf surface. The eggs are deposited in clusters of 50 or more with the individual eggs overlapping. Larvae emerge and crawl down the leaf towards the plant stem and may feed for a short time on the inside of the leaf sheath before boring into the stem. Larvae (Fig. 2.12) are pale yellowish white with two pairs of stripes running the entire length of the body and have a black head capsule. The larva is about 2.5 cm long when full grown. Larvae of this species resemble Mexican rice borer larvae. They move up and down the stem feeding

Figure 2.11  Chilo plejadellus adult (Source: LSU AgCenter/EOL Bob Paterson Moth Photography Group). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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before moving to the first joint above the waterline, chewing an exit hole in the stem and constructing a silken web in which they pupate. Pupation occurs inside the culm and takes place in the spring, the larvae having spent the winter in the stubble. The pupa is about 1 inch long, light to dark brown, smoothly tapered to a point at the rear and is nearly always found enclosed in a heavy web inside the stem. The pupal stage lasts 7–10 days. There are two to three generations per year in rice. They overwinter as larvae in rice stubble and after pupating adults emerge in May. Plant damage and ecology: The rice stalk borer is a sporadic pest of rice in Louisiana. Injury to rice results from larvae feeding on plant tissue as they tunnel inside the stem. Early instars enter the rice plant stem by chewing a hole either behind the leaf sheath or near the base of the panicle. Several larvae enter the stem from a single hole. Later instars keep feeding on tissues until only a single thin layer of tissue covers a circular hole in the stem above the water line. Injury is often first noticed when the youngest partially unfurled leaf of the plant begins to wither and die, resulting in a condition called ‘deadheart’. Later in the growing season, these rice stems are weakened and may lodge before harvest. Stem feeding that occurs during panicle development causes partial or complete sterility and results in the ‘whitehead’ condition (Dale 1994). The white, empty panicles are light in weight and stand upright. Newly hatched larvae have also been known to attack at the uppermost node after the panicle has already emerged and partially developed. These panicles may break at the point of injury.

Figure 2.12 Chilo plejadellus larva (Source: LSU AgCenter).

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In Louisiana rice stalk borers overwinter as last instar larvae in the stalks of rice and other host plants. Larvae pupate in the spring, and adult moths emerge in early to late June, mate and live on various hosts until rice stem diameter is large enough to support tunnelling larvae. Although egg laying may begin in late May, injurious infestations usually occur from August through September. Severe infestations cause stalk breakage and plant lodging.

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2.8 Rice striped borer, Chilo suppressalis (Walker) (Lepidoptera: Pyralidae) Distribution: Europe: France, Portugal, Spain; Asia: Bangladesh, Burma, Cambodia, China, Hong Kong, India, Indonesia, Iran, Japan, Korea, South Laos, Malaysia, Manchuria, Nepal, Pakistan, Philippines, Ryukyu Islands, Taiwan, Thailand, Vietnam; USSR: Bleszynski; Australasia and Pacific Islands: Australia, Hawaii, Papua New Guinea, Irian Jaya (CABI 2015d). Host plants other than rice: Main hosts: Sorghum bicolor (L.) Moench., Zea mays L.; Many wild hosts (Poaceae grasses) including Echinochloa colona (L.) Link, Echinochloa crus-galli (L.) Beauv., Eleusine indica (L.) Gaertn., Panicum miliaceum L., Phragmites australis (Cav.) Trin.ex Steud., Sclerostachya fusca (Roxb.) A. Camus, Typha latifolia L., Zizania aquatica L. (CABI 2015d). Description and biology: The adult moths (Fig. 2.13) are 13–16 mm long and with straw to light brown forewings. There are a number of silvery scales and usually five black dots at the tip of the forewing; the hindwing is yellowish white (Reissig et al. 1986). The females are lighter in colour than the males. Moths emerge at about 7–8 pm and become active in the early morning. During the day they remain in dense foliage. Moths are capable of flying long distances; sometimes winds carry them to distant places (Dale 1994). Male moths are strongly attracted to virgin females, the attraction being highest on the evening of their emergence but declining as days pass. Mating usually takes place

Figure 2.13 Chilo suppressalis adult (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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during the night of emergence, but egg laying starts only on the next night. The mating frequency is highest among 2- or 3-day-old moths and it then decreases rapidly with age (Kanno and Sato 1978). Through laboratory studies, it has been shown that the threshold light intensity for mating initiation varies with temperature (Kanno 1980). A female moth may lay 100–550 eggs in batches of 50–80, depositing one batch each night over a 3–5 day period. Eggs (Fig. 2.14) are naked and scale-like, pale to dark yellow, laid in masses formed of overlapping rows. Egg masses are found on the basal half of the leaves or occasionally on the leaf sheaths along the midrib of either the upper or lower surface. The eggs hatch in 3–5 days. Maximum hatching takes place in the morning between 5 and 6 am. Generally, all eggs of a mass hatch together (Dale 1994). The larvae live gregariously (Fig. 2.15) during the first three instars (Nozato 1981). If the young larvae are isolated from each other, they suffer high mortality. The newly emerged larvae crawl up the rice plant and then congregate beneath the leaf sheath. All larvae enter the stem through a common hole. Larval feeding generally occurs in the middle of the stem. The fully grown larva is approximately 26 mm long and 2.5 mm wide. It has a yellowish brown head and has three dorsal and two lateral brownish abdominal stripes. The middle dorsal stripe is lighter in colour. Under ideal conditions there are 5–6 larval instars while under adverse conditions, as many as 9 instars have been recorded. The larval stage normally lasts from 20 to 48 days (Dale 1994). Pupation takes place within the stem. The last instar larva makes an exit hole in the internode for the moth to emerge. The pupa is reddish brown in colour and is without a silken cocoon.

Figure 2.14 Chilo suppressalis eggmass (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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In temperate regions, the larvae enter into diapause in the winter and development resumes in the spring with warmer temperatures. Temperature, day length and the stage of growth of rice plants are principal factors inducing diapause. Exposure of larvae to short day lengths (8–14 hours) induces diapause while longer days (14.5–16 hours) prevent it. The rice striped borer is well adapted to a temperate climate. All stages of the pest can withstand low temperatures and development proceeds normally in cold habitats of temperate regions. The optimum temperature for larval development is between 22 and 33°C even though larvae are able to withstand temperatures as low as −14°C for short periods of time. The rate of pupal development increases with temperature from 15 to 30°C. Beyond 35°C, the pupae suffer high mortality and the emerging moths are mostly deformed. The pest can have one to five generations per year depending on the availability of host plants and the occurrence of favourable temperature conditions. The longer the period of host plant availability, the more the population is increased through additional generations in a year. In Japan, distinct ecotypes of C. suppressalis have been reported. They are ‘Shonai’ in the north, ‘Saigoku’ in the southwest and ‘Tosa’ from Kochi prefecture. The Shonai ecotype is more tolerant to lower temperature than the Saigoku ecotype. The stem borer population between the areas distinctly occupied by these ecotypes is intermediate in nature (Dale 1994).

Figure 2.15 Chilo suppressalis larva (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: The rice striped borer, Chilo suppressalis prefers temperate regions and non-flooded conditions (Islam and Catling 2012) and has been considered as one of the most serious pests of rice in temperate and subtropical Asia (Dale 1994). However, its importance has gradually declined in many countries. The pest mainly attacks rice in the middle or late stage of plant growth. In addition to causing deadhearts and whiteheads, larval feeding can also cause reduced plant vigour, fewer tillers, unfilled grains and lodging of plants. High grain yield losses have been reported for this pest; up to 50% grain loss has been reported from the Philippines (Otanes and Sison 1947) and 20% in Taiwan (Ou 1959). In Spain, Chilo suppressalis, coupled with Sesamia spp., produces an estimated crop loss of about 2% (Grist 1965), but in Malaysia, no serious damage has been reported (Dale 1994). It occurs in Bangladesh but is rare there (Islam and Catling 2012).

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2.9 African striped rice borer, Chilo zacconius Bleszynski (Lepidoptera: Pyralidae) Distribution: Benin, Burkina Faso, Cameroon, Cote d'Ivoire, Mali, Niger, Nigeria, Senegal. Host plants other than rice: Echinochloa crus-galli (L.) Beauv., Oryza barthii A. Chev., Sorghum arundinaceum (Desv.) Stapf., E. pyramidalis (Lamarck) Hitchcock and Chase, Pennisetum spp., Rottboellia cochinchinensis (Loureiro) W.D. Clayton, Saccharum officinarum L., Sorghum arundinaceum (Desv.) Stapf., and Zea mays L. (Sampson and Kumar 1986, Akinsola 1990, Dale 1994). Description and biology: Chilo zacconius is a polyphagous pest of rice in West Africa where it is found in rainfed and irrigated lowland environments (Nwilene et al. 2013). Adult moths (Fig. 2.16) have pale yellow forewings with irregular black spots. Males are darker than the females. Moths are nocturnal and hide during the day. Oviposition takes place on the upper or middle leaves. Pale yellow eggs are laid in two or three overlapping longitudinal rows. Eggs are oval, flat and imbricate like fish scales. They hatch after 4 days. The newly hatched larva moves around actively on the plant, feeds a little from the leaf and bores into the stem through the leaf sheath. From flowering, the larvae bore into the flower stalk causing whiteheads. Then they descend into the central stem which they perforate at different levels. The larvae can live for several months without food. The larva has an ivory body with a dark brown head. There are seven longitudinal pink stripes on the body, the ventral ones being incomplete and sometimes indistinct. The larvae pass through 5 instars in a period of 4 weeks before they pupate. Pupation takes place in the stem or in the leaf sheaths. The chrysalis is dark brown; its abdomen ends in a four-pointed crest with another two-pointed crest at the back. The pupal period is 6–7 days. There are 5–7 generations per year. The number is mostly governed by the duration of the dry season and the availability of host plants. Generally, two successive generations occur in the same rice field; the first-generation larvae attack the stem and mainly cause deadheart development whereas the second generation mostly infests the panicle stalks resulting in whiteheads (Heinrichs and Barrion 2004).

Figure 2.16 Chilo zacconius adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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A very similar species, Chilo diffusilineus J. de Joannis, has also been reported from the humid equatorial Sudanese areas (Breniere 1976; Bonzi 1982). It differs from C. zacconius only in the shape of genitalia in both sexes. The habits and appearance of the larvae are identical. C. diffusilineus infests irrigated and rainfed rice plants. Plant damage and ecology: Chilo zacconius is a polyphagous pest of rice attacking both cultivated and wild gramineous plants. The gramineous species serve as alternate hosts on which the larvae survive during the off-season when rice is not available and that serve as a reservoir from which they invade rice fields (Akinsola 1990). Plant damage caused by C. zacconius is similar to that of other lepidopterous stem borers. Feeding inside the stem during the vegetative stage prevents the central leaf whorl from opening; instead, it turns brown and withers. Although the lower leaves remain green, the apical reproductive portion of the tiller is destroyed (deadheart) and the tiller fails to produce a panicle. Larval feeding at the panicle initiation stage or thereafter prevents the development of the panicle, resulting in a whitehead. Although larvae, upon hatching, quickly establish themselves within the stem, the appearance of damage symptoms occurs gradually. Akinsola (1990) reported that when plants were artificially infested with larvae the maximum number of deadhearts occurred at 20 days after infestation. The particular internode in which feeding occurs is a factor in the rate at which damage symptoms appear – the higher the internode, the sooner the appearance of the deadhearts. The number of larvae per tiller also affects the percentage of tillers that show deadheart symptoms. Akinsola (1990) found that four larvae tiller−1 were required to attain 85% deadhearts. In nature, several larvae can be found in one tiller a few days after hatching. However, they disperse to other tillers after a few days and usually only one larva remains in a tiller to maturity. Chilo zacconius occurs in the humid tropical, Guinean and Sudanian savanna zones of West Africa but is most abundant in the latter two zones. C. zacconius occurs in all ecosystems, but is generally most abundant in the uplands. It occurs in the mangrove swamps, but it is of much less importance than M. separatella. Studies in Gambia indicated that C. zacconius made up only 5% of the stem borer composition in irrigated and mangrove swamps while M. separatella (82%) was the most abundant species (Jobe 1996). The per cent stem borer species composition of C. zacconius, M. separatella and S. calamistis throughout 1 yr in upland and irrigated rice ecosystems was determined at Ibadan, Nigeria (Alam 1988). Maliarpha separatella predominated in both ecosystems. Chilo zacconius populations were higher in irrigated rice than in upland rice. Chilo zacconius larvae were present from February to December with the highest percentage occurring in June. In the irrigated Sahel region, C. zacconius is a major stem borer species (Akinsola 1990). Dry season crops grown from December to April are almost free of borers, while the main season crop, grown from July to November, is heavily attacked. During the dry season, larvae may feed on weeds or in off-season rice fields. They can, however, live without food for several months (December to April in the Casamance, Senegal). In a screenhouse experiment, Ukwungwu and Odebiyi (1984) studied the effect of C. zacconius larvae on rice plants. Larval infestation caused a reduction in plant height. Degree of plant height reduction appeared to be related to degree of susceptibility to borers. Larval infestation caused an increase in tiller production in most varieties studied,

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indicating a tendency to compensate for damage to primary tillers. The number of panicles produced per hill by infested and uninfested plants differed little. Damage tends to cause the development of secondary tillers that produce panicles, but these panicles may, or may not, mature, depending on time of harvesting of the primary tillers. Infestation of susceptible varieties resulted in reductions in the number of filled grains per panicle. There was a positive correlation between percentage of deadhearts and reduction in filled grains per panicle and reduction in weight of grains. Thus, varieties that had more deadhearts sustained higher grain yield losses.

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2.10 African white borer, Maliarpha separatella Ragonot; (Lepidoptera: Pyralidae) Maliarpha separatella Ragonot is one of the most common stem borers occurring in rice throughout West Africa and has been extensively studied. Its feeding damage is unique among the rice stem borers as it seldom causes deadhearts or whiteheads (Heinrichs and Barrion 2004). The genus Maliarpha has been revised and what has been referred to in the literature as the African rice borer, M. separatella, is actually a complex of three closely related stem borer species (Cook 1997). Distribution: Africa – Burkina Faso, Cameroon, Comoro Islands, Côte d’Ivoire, Ghana, Kenya, Liberia, Madagascar, Nigeria, Swaziland, Tanzania, Uganda; Asia – China, India, Myanmar; Oceania – Papua New Guinea (CABI 2016a). M. separatella is a stem borer of sub-Saharan and Indian Ocean Islands and it is the only rice stem borer that has widespread distribution in sub-Saharan Africa. It was first reported as a pest when Hall (1955) found it feeding on irrigated rice in Swaziland. It also occurs in the Comoro Islands and Madagascar (Kfir et al. 2002; Dale 1994; Delucchi et al. 1996). Although it has been reported from China, India and Myanmar, it is not considered a rice borer there (Heinrichs and Barrion, 2004). Host plants other than rice: Andropogon tectorum Schum. & Thonn., and wild rices. M. separatella is a rice pest. There have been reports of it attacking sorghum in India (Sandu and Chandler 1976) and sugarcane in Papua New Guinea (Li, 1985). Other host plants for this pest recorded in West Africa are Andropogon tectorum (WARDA 1977), Oryza barthii, Oryza longistaminata and Oryza punctata (Khan et al. 1991). However, Delucchi et al. (1996) considered all hosts other than Oryza spp. in West Africa to be doubtful. Bianchi et al. (1993) also disputed these records and considered M. separatella to be monophagous and restricted to sub-Saharan Africa. Description and biology: Reports on the biology and ecology of M. separatella have been published by Breniere (1969, 1982) and Pollet (1981) in Côte d'Ivoire, Akinsola (1979) and Akinsola and Agyen-Sampong (1984) in Nigeria, Diop (1979) in Mali, and Appert (1970) and Delucchi et al. (1996) in Madagascar. Breniere (1983) has described the eggs, larvae and pupae.

Figure 2.17 Maliarpha separatella adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The slender adult moth has forewings that are yellowish or straw coloured with a prominent reddish brown line along the front edge (Fig. 2.17). The hindwings are pale yellow with a metallic sheen and fringed with long yellow hairs. The body is covered with yellowish scales. At rest, the V-shaped wings cover the body. Body length is 11–13 mm in the male and 13–15 mm in the female. The female produces a sex pheromone, which attracts the male for mating (Ho and Seshu Reddy 1983; Cork et al. 1991). Ho and Seshu Reddy (1983) reported that moths fly at night and that peak flight activity in Kenya was between 2300 and 0300. In West Africa, 82% of the moths were caught between 1900 and 0100 and rainfall appeared to induce flight activity (WARDA 1979). Eggs are laid during the night on preferably large, vertical leaves of tillering plants. Sometimes eggs are deposited in the youngest unfolded leaf. Eggs are laid in parallel rows on the upper side of the leaf and are attached by a cement-like substance that, on drying, causes a characteristic pinching of the leaf lamina, completely enclosing the eggs. Females deposit from one to six egg masses consisting of 30–95 eggs. Total number of eggs laid can reach 300. On the second night after its emergence, the female lays the first egg mass and then may continue for two to three nights more. From two to three egg masses may be deposited each night. After an incubation period of 7–10 d, larvae hatch at about 0700. Newly hatched larvae, which are white with dark brown heads that later turn yellowish with light brown heads (Fig. 2.18), are very active. Some move to the tip of a leaf blade where they suspend themselves from silken threads, which they produce. Suspended from the silken threads, the larvae drift in the wind and attach themselves to adjacent leaves of the same (or a neighbouring) plant. First instar (L1) larvae move down the leaf to the leaf sheath and the stem. After spending about 4–5 d inside the leaf sheath, with their large mandibles they penetrate the stem at the internode. It is believed that the larvae begin feeding in the

Figure 2.18 Maliarpha separatella larva (Source: A. Togola). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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stem about 4–5 days later. The larval stage lasts about 35–50 d during which it passes through five to seven instars. There is usually only 1 larva/stem. Pupation occurs at the internode nearest the plant base (Heinrichs and Barrion 2004). Before pupation, the larva moves from the feeding site towards the upper part of the stem. An exit hole is cut in the stem before the larvae spin a conical silky web channel connecting the inner wall of the stem and the exit hole. The larva then pupates with its head placed upwards 1–2 cm below the exit hole. The pupal period lasts from 32 to 65 d. Diapause occurs during the sixth instar at the base of dried stubble. The larva resumes activity with the return of humid conditions and rapidly completes its life cycle. Larval diapause may last as long as 251 d (Akinsola and Agyen-Sampong 1984). In southern Nigeria, diapause starts in July and lasts until March of the next year. Diapause usually occurs before the rice plant starts drying and – in sub-Saharan Africa – is believed to be triggered by decreasing day length and modulated by temperature (DeLucchi et al. 1996). Diapausing larvae are sluggish, milky white and have a wrinkled body; white nondiapausing larvae are agile, yellowish white and have a smooth body. There are usually 3 or 4 generations per year. Plant damage and ecology: Maliarpha separatella is mainly a rice pest and its alternate hosts are limited. Rice ratoons serve as a residual population between rice crops (Joshi and Ukwungwu 1993). Among the four stem borers usually found attacking rice in Africa, the white borer M. separatella is considered to be the most common and unique. Due to its peculiar habit of remaining at the lower internodes of the rice plant, the larva does not usually produce ‘deadhearts’ or ‘white earheads’. This is a similar situation to that of Rupela albinella (Cramer) in Latin America. The growing apical portion of the plant is not cut off from the base and hence panicles can be initiated at the last node. The infestation mainly leads to a reduction in plant vigour and tiller number and a high percentage of unfilled grains. The level of M. separatella infestation does not correlate with the ultimate damage of the crop. At 75 DT, 97% hills were infested and 71% tillers were damaged by the larvae. However, the incidence of ‘deadheart’ was as low as only 1% (Ho et al. 1983). Bianchi et al. (1993) reported only a slight effect on the number of whiteheads at infestation levels up to 68%. There is a critical period in the rice plant's development – about 42–65 DT, depending on variety (Delucchi et al. 1996) – when M. separatella infestation causes yield loss. Before this period, larval mortality is too high to cause serious damage and the plant compensates for the damage. After this period, the severity of injury caused by the larvae decreases until it becomes negligible. Feeding by M. separatella at the tillering stage causes a reduction in plant height and number of filled grains (Akinsola 1984). When infested at the booting stage, plant height is not affected but total number of grains panicle−1, number of filled grains panicle−1 and grain weight are significantly reduced. In studies of Ho et al. (1983), plants were infested with M. separatella moths at 45 DT and feeding damage by the larvae only caused a reduction in 1000-grain weight and an increase in percentage of empty grains. Harvest index, number of panicles m−2, grains panicle−1 and per cent of reproductive tillers were not significantly affected by the feeding of M. separatella. In addition to the direct damage caused by feeding of the larvae, Pollet (1978a,b) has reported a synergistic relationship between M. separatella and the rice blast fungus, Pyricularia oryzae, where the fungus preferentially attacks plants already infested with the

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stem borer. After M. separatella adults have emerged and left the stems, the fungus attacks the neck of the panicles and affects grain development. This insect–fungus combination can cause a complete grain yield loss. Rice plants are usually attacked during the later stages of their growth cycle. Infestation generally begins in the panicle initiation to booting stages and continues to harvest (Toure 1989). In studies in irrigated rice in Mali, very low larval populations were observed in the early tillering stage (Heinrichs and Hamadoun 1995). Populations peaked at the panicle initiation to booting stages and again near maturity. Low larval populations in Nigeria were observed at 30 DT and increased with crop age, reaching a peak at 90 DT (Ukwungwu 1987a). In Kenya, larval populations were the highest in the ripening stage (Njokah and Kibuka 1982; Njokah et al. 1982). Akinsola and Agyen-Sampong (1984) reported that at the vegetative stage of rice growth larvae are found in the first basal internode. During later crop growth stages, some larvae migrate up to the second or third internode, depending on the height of the plant. No larvae were found at the topmost internode. The larvae complete their development in one or two internodes and do not migrate from one tiller to another once they have lodged themselves within the stem. Maliarpha separatella is abundant in all rice ecosystems (DeLucchi et al. 1996). It is more abundant in the rainfed lowland and irrigated ecosystems than in the uplands and is the most abundant stem borer species in the mangrove swamps. Surveys conducted in Côte d'Ivoire in 1995 indicated that about 35% of the stem borer larvae in the lowlands in the July survey were M. separatella, whereas in the uplands only about 5% were M. separatella. Maliarpha separatella larvae are distributed throughout all toposequence sites in inland valley rice fields at M'be, Côte d’Ivoire (Heinrichs and Barrion 2004). It was the most abundant stem borer species in the drought-prone uplands and in the lowlands, based on percentage species composition. In upland rice, the larvae are located towards the base of the plant while in flooded and swampy fields, the larvae tend to be located in the upper portion of the plant. Once they bore into the first or second internode, larvae feed on the inner stem tissues at a site above the node. Feeding activity of the larvae results in small circular cavities in the stem, which is not pierced. The larvae pass from one internode to another by penetrating the node and, once established, they spend the entire larval stage in one stem and do not migrate from one tiller to another. The larvae generally cannot survive on young plants without elongated internodes. In deep-water rice, initial infestations are believed to occur before flooding. In Mopti, Mali, it was observed that tillers infested with M. separatella were detached at their base (Akinsola 1980a). Plants in deep water have a whitish, fragile portion at the base. Thus, stem borer feeding, plus the water pressure at a 3-m depth, leads to the detachment of the damaged portion of the plant. As a result, M. separatella-infested stems were observed floating on the water surface in the very deep zones (3 m) and 60% of the hills were missing due to M. separatella damage. An increase in cropping intensity is expected to increase the level of damage caused by M. separatella. In studies conducted by Breniere (1969) in Côte d'Ivoire, highest M. separatella populations occurred in Yamoussoukro, where two crops of rice were grown annually. He reports that the same condition exists at the Richard Toll Station in Senegal, where double cropping is practised.

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The economic threshold for M. separatella, as developed in Madagascar (Appert 1970), is based on the number of egg masses. Studies by Delucchi et al. (1996) in Madagascar in the 1980s indicated that the economic threshold for a 2-t ha−1 rice yield should be 8.6 egg masses 100 tillers−1. This is equivalent to an infestation of 59% at the end of the critical period and corresponds to a yield loss of 22%. As the yield increases, the threshold decreases; for a yield of 4 t ha−1, the threshold is 6.6 egg masses 100 tillers−1.

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2.11 Yellow stem borer, Scirpophaga incertulas (Walker) (Lepidoptera: Pyralidae) Distribution: Asia – Afghanistan, Bangladesh, Bhutan, Brunei, Cambodia, China, India, Indonesia, Iraq, Japan, Laos, Malaysia, Myanmar, Nepal, Pakistan, Philippines, Singapore, Sri Lanka, Taiwan, Thailand, Vietnam; Africa – Egypt; Europe – Spain; Oceania – Australia, Papua New Guinea (CABI 2015e). Host plants other than rice: None. S. incertulas is monophagous on rice. Description and biology: The yellow stem borer Scirpophaga incertulas is a serious pest of rice throughout the Orient. It is regarded as monophagous with exclusive host specificity to rice. It is the dominant and the most destructive rice stem borer species in India (Walker 1975; Panda et al. 1976), Sri Lanka (Fernando 1967), Pakistan (Moiz and Rizvi 1971), Bangladesh (Catling and Alam 1977), Thailand (Yasumatsu 1976) and Malaysia (Chang 1981). Adult moths often exhibit sexual dimorphism. The female moth is bigger than the male and its forewings are bright yellowish brown with a distinct black spot in the centre (Fig. 2.19). The abdomen is wide, the tip being covered with tufts of yellowish hairs. The male moth is pale yellow; the abdomen is slender and the anal end has a thin hairy covering dorsally. Spots on the forewing are not conspicuous. The moths are nocturnal (Islam and Catling 2012), emerging between 7 and 9 pm (Dale 1994). They are not active during the daytime, but can be seen resting on stems and

Figure 2.19 Scirpophaga incertulas adult (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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leaves. At dusk, especially on still, warm, humid nights, after a rain, the moths mate. Mating generally occurs between 7 and 9 pm. The female moths lay eggs in 2–3 masses within the first three days of emergence. In the tropics, the moths are short-lived and die 2–3 days after oviposition. But in Taiwan and Japan, they are reported to live longer (Shiraki 1917); the longevity ranges from 5.3 to 8.8 days in females and from 4.5 to 8.6 days in males. Eggs, numbering 100–150, are laid in masses near the tip of leaf blades. They are creamy white, flattened, oval and scale-like and covered with a tuft of tan anal hairs from the female moth (Fig. 2.20). Before hatching in 5–8 days, the eggs darken to a purplish tinge. Although eggs show some development at 13°C, they normally develop only at or above 16°C. The optimum temperature is between 24 and 29°C. The humidity requirement for egg development is between 90 and 100%, and hatching is drastically reduced when it falls below 70% (Doke 1936). Eggs often have a high parasitisation rate. The yellow stem borer usually passes through 6 instars (Islam and Catling 2012). The first instar larvae are about 1.5 mm long and 0.5 mm wide. The body is pale yellow, the prothoracic shield is dark brown and prominent and the head is orange. The newly emerged larvae show a strong tendency to disperse. They move downward and wander about on the plant surface for one or two hours. They can also be seen hanging down by a silken thread to be carried by wind to adjacent rice plants. During this roaming period, many larvae die. The survivors enter between the stem and the leaf sheath and feed on green tissues of the leaf sheath for two to three days. The caterpillars then start boring in the stem, often at the nodal region and feed on the inner tissues of the plant.

Figure 2.20 Scirpophaga incertulas eggmass (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Often the larvae leave the first host plant after a week. Young larvae, in search of other plants, crawl or wriggle about on the water surface, while third and fourth instars sometimes float and drift on the water surface inside cylindrical cases made up of rolled leaf tips (Islam and Catling 2012). After reaching a suitable host plant, the larvae bore in, leaving their cases sticking to the stem at right angles. In mature rice plants, the caterpillars bore into the stalk at the top region just below the earhead. At this stage, a number of larvae are found in the same stalk (Banerjee and Pramanik 1967). The full-grown sixth instar larvae are 25 mm long, white or yellowish white, with a welldivided prothoracic shield and minute black spots (pinaculae) at the base of the setae on the abdomen (Fig. 2.21). They make a thin silken case over themselves inside the stem soon after the pre-pupal moult. The larval period usually lasts for 30 days. Before pupation, the larvae make an exit hole through which the adult moth later escapes. Pupation takes place inside the stem, mostly in the lowest node of the plant or just above the water level. In seedlings, the larvae pupate in the root region only (Puttarudriah 1945). Pupae are pale at first and turn darker brown after some time. They are partly exarate, and the tips of their appendages are free (Isaac and Venkatraman 1941). The pupal period is usually 6–10 days but may be prolonged in cooler months. During periods when there is no rice crop and the temperature is not optimal for larval development, mature larvae diapause in rice stubble. These larvae are vulnerable to low temperature and high moisture. Because the larvae cannot survive in the cut straw, they go down into the stubble to diapause. In Japan, where plant stems are cut near the soil level at harvest, the stubble harbours far fewer borers than in Taiwan, where longer

Figure 2.21 Scirpophaga incertulas larva (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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stubbles are left when rice is harvested. In Japan, as soon as warm weather begins in April–May, the larvae start pupating (Kawada et al. 1934). In single cropping areas of tropical South India, some larvae enter into diapause after harvest in December. These larvae pupate and emerge as moths after the monsoon rains begin in June or July (Perraju and Reddy 1965). S. incertulas occurs year-round in Sri Lanka, South India and Malaysia where rice is cultivated in succession. The number of generations in a year is governed mostly by the ecological conditions and the availability of rice plants and varies from 2 to 6. In temperate countries like Japan, the pest has only three broods (Ishikura and Nakatsuka 1955). The first brood moths appear as early as December–January in subtropical areas such as Hainan Island, China, and Taiwan, where six generations occur annually (Kiritani and Iwao 1967). In the cooler areas of China, the fourth brood is usually partial, whereas in warmer areas such as Chunchi, the fourth brood is the largest (Tsai 1936). Three broods are reported to occur during the 6-month growing season in Sri Lanka (Fernando 1967). Plant damage and ecology: Boring of the larvae in the stem of plants in the vegetative stage causes ‘deadhearts’ (dead central shoots) and boring in plants at the reproductive stage causes the development of ‘whiteheads’ (dead panicles) due to the severing of the reproductive shoot within the stem. Both deadhearts and whiteheads can be removed from within the stem by pulling on the apical portion. The yellow stem borer is most abundant in aquatic habitats where fields are flooded and in locations where multiple rice crops are grown annually (Reissig et al. 1986). The extent of crop losses varies in time and space. S. incertulas was reported to cause 1–19% yield loss in early planted and 38–80% in late-planted rice crops in India (Khan 1967). A loss of 5–10% was reported in the Philippines (Rowan 1923). According to Walker (1975), the stem borer causes 10–30% crop loss in Taiwan. In Malaysia, the yield reduction may amount to 10%. The yellow stem borer is a notorious pest of deep-water rice in the main flooding period (Islam and Catling 2012). In Bangladesh, at harvest, more than 90% of whiteheads were found to be due to S. incertulas (Catling 1980). In Thailand, it comprised more than 95% of the borer population in attacked stems. The average incidence increased with the stage of crop, from early elongation phase to ripening through late elongation and bootingheading stages (Catling 1982). Stem damage and borer activity are apparently very low during the pre-flood stage from May to mid-July. Stem damage increases gradually during the late pre-flooding stage and culminates in maximum damage at harvest. In Bangladesh it is estimated that many deepwater fields sustain yield losses of 20% every year, primarily due to the yellow stem borer (Islam and Catling 2012). A 1% yield loss in deepwater rice was associated with 2% damaged stems at harvest (Catling et al. 1987). A tentative damage threshold of 10% damaged stems at booting/flowering stage and 20% damaged stems at plant maturity was proposed.

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2.12 White stem borer, Scirpophaga innotata (Walker) (Lepidoptera: Pyralidae) Distribution Asia – Indonesia, Malaysia, Philippines; Australasia and Pacific Islands – Australia, Papua New Guinea, Irian Jaya (CABI 2015f). Host plants other than rice: Eleocharis dulcis (Burm. f.) Trin ex Henschel, Eleusine spp., Paspalum spp., Panicum spp., Cyperus spp., Saccharum officinarum L., wild rices. Description and biology: The white stem borer is a major pest of rice in South and Southeast Asia and Australia. It occurs predominantly in areas where there is only one wet season crop per year and the stubble is left undisturbed during the dry season. The pest is especially important in Indonesia, where it occurs in low-lying areas up to 200 m above sea level. It is a dominant species in the upland rice areas of Sarawak. The insect does not occur in regions with high rainfall, as the larvae cannot survive extremely wet situations (Soenardi 1967). The adult white stem borer is similar to the yellow stem borer S. incertulas in appearance. In contrast to the yellow stem borer, the female moth of the white stem borer does not have the characteristic black spot on the wing and adults of the two white stem borer sexes are similar in appearance. The white moth with a broad, flattened, orange anal tuft (Fig. 2.22) is commonly seen in the field, especially in the early stages of the crop. The adult female has a wingspan of 26–30 mm and the male has a wingspan of 18–24 mm (Reissig et al. 1986; Dale 1994). Three disc-like eggs are laid in oval clusters of 70–260 usually on the underside of young leaves. The egg mass is covered with silky hairs from the anal portion of the female moth and is similar to that of the yellow stem borer S. incertulas. The incubation period is 4–9 days. The young larvae have small orange heads and penetrate the leaf sheath and bore down into the stem. The larva is milky white and grows to a length of 25 mm. The age of host plant has a strong effect on the duration of larval period. It varies from 19 to 31 days. The full-grown larva pupates within the stem after making an exit hole for the moth to emerge. Pupae are soft-bodied, pale and 12–15 mm long. They are more white-coloured than those of the yellow stem borer. Pupation is completed in 7–11 days. Larvae undergo diapause during the dry season. After the crop has been harvested, the caterpillars remain inactive in the lowest internodes of the stubble. Pupation does not take

Figure 2.22 Scirpophaga innotata adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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place until the first rains at the beginning of the next season. With the rains, the larvae become active, pupate and the moths emerge. The threshold rainfall which terminates diapause is about 10 mm (Soenardi 1967). Adult moths are seen in rice fields only during the wet season. Three to five generations are produced on the rice crop, depending upon the duration of the variety, time of sowing and transplanting. Plant damage and ecology: The white stem borer differs from the yellow stem borer in that it has a wide host range. In rice the first three generations cause deadhearts in nurseries and in the young crop, while feeding of the two subsequent generations causes whitehead development at the reproductive stage. Heavy losses, however, do not occur every year. The white stem borer is an important biotic factor influencing rice yields in West Java, Indonesia. Prior to 1945 the average area of rice attacked by the white stem borer was ca 15 000 ha (Rubia et al. 1997). The degree of damage in the Indramayu region was around 11%, and in some years as high as 37%. In some areas the harvest failed completely due to heavy infestation, causing famine in several locations. In the late 1980s in the Indramayu region, 2000 ha of rice were attacked by the white stem borer, with a peak in 1990 when 65 040 ha were infested (15 000 ha at 100% infestation) with a yield loss estimated at 210 000 tons of unhulled rice. In West Java, 10 000–20 000 hectares of rice are infested each year (www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsID=55202). Yield losses depend on stem borer populations and the stage of the rice plant. If rice is attacked in the vegetative stage, the yield loss varies, but if the infestation happens during the booting stage the yield loss could be as high as 90–95%. In Australia, yield reduction due to the white stem borer was estimated at 30% in the summer crop, while the winter crop was free from infestation (www.plantwise.org/KnowledgeBank/Datasheet. aspx?dsID=55202).

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2.13 African pink borer, Sesamia calamistis Hampson (Lepidoptera: Noctuidae) Sesamia spp. are the most polyphagous among the rice stem borers. Five Sesamia species have been reported to feed on rice in West Africa: S. calamistis Hampson, S. nonagrioides botanephaga Tams and Bowden, S. nonagrioides penniseti Tams and Bowden, S. cretica Led. and S. poephaga Tams and Bowden. Sesamia calamistis is the most common species and occurs throughout West Africa, East Africa, Madagascar and South Africa (Breniere 1982), and Réunion, Maurice and Comoros Islands in the Indian Ocean (Appert and Ranaivosoa 1970). Sesamia nonagrioides botanephaga is probably the next most common Sesamia species in rice and is limited to the tropical and equatorial areas of Africa. Sauphanor (1985) considers S. calamistis to be the main stem borer of upland rice in Côte d'Ivoire. Distribution: Angola, Benin, Burkina Faso, Burundi, Cameroon, Comoros, Congo, Congo Democratic Republic, Côte d'Ivoire, Eritrea, Ethiopia, Gambia, Ghana, Kenya, Libya, Madagascar, Malawi, Mali, Mauritius, Mozambique, Niger, Nigeria, Réunion, Rwanda, Sierra Leone, South Africa, Sudan, Senegal, Tanzania, Togo, Uganda, Zambia, Zimbabwe (CABI 2016b). Host plants other than rice: Cyperaceae – Carex (sedges); Poaceae (grasses) – Pennisetum glaucum, Pennisetum purpureum Schumach., Rottboellia exaltata L., Saccharum officinarum L., Setaria splendida Stapf, Sorghum bicolor (L.) Moench, Triticum aestivum L., Zea mays L.

Figure 2.23 Sesamia calamistis adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Description and biology: Breniere (1983), Akinsola and Agyen-Sampong (1984), and Dale (1994) have described the various stages and the life cycle of S. calamistis. Appert and Ranaivosoa (1970) have described the morphology of the various stages and Meijerman and Ulenberg (1996) have described the larval morphology, host plants and distribution. The adult moth is light brown with brown stripes. The margin of the forewings is wide, whitish and partly smoky. The rest of the forewings are speckled with dark patches. The hindwings are pearly white with a yellowish margin. The pronotum is covered with long hairs (Fig. 2.23). The moths are nocturnal and are capable of flying long distances. Mating of adults takes place as early as the first night after emergence and oviposition begins the same night. The female lays up to 300 eggs. Eggs are laid loosely between the leaf sheath and the stem surrounding the upper internodes. Eggs are subspherical, flat at the poles and have numerous longitudinal striations. Eggs are yellow and are laid side by side, without any specific alignment. Eggs hatch in 7–10 d after oviposition. Sesamia calamistis larvae are smooth, uniformly yellowish pink on the dorsum, with greyish lateral and dorsal stripes, and a dark brown head (Fig. 2.24). First instar larvae (L1) on hatching are gregarious. Larvae first feed within the tissues of the leaf sheath, causing a brownish yellow discolouration, and then enter the stem through a horizontal cavity and move downward, sometimes through several internodes. The frass, which fills the vertical galleries, is partly pushed out through openings in the leaf sheath. The duration of the larval period is from 28 to 35 d.

Figure 2.24 Sesamia calamistis larva (Source: East African Network for Taxonomy (BIONET-EAFRINET; http://keys.lucidcentral.org/keys/v3/eafrinet/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The larvae pupate within the base of the stem or in folds of withered leaf sheaths. The pupation period is 10–14 d. The reddish brown pupae are about 17 mm long. The tip of the abdomen bears two dorsal horns (cremaster). In wet, tropical regions, the life cycle is practically continuous throughout the year. Drought or cold temperatures may slow development. Mature larvae become inactive from the start of the dry season and remain so until the rains begin. On crops that are irrigated out of season, development continues uninterrupted. Where rice is grown throughout the year, there may be at least six generations annually. Plant damage and ecology: This species is found in sub-Saharan Africa and some of the islands in the Indian Ocean. It commonly occurs in wetter localities at all altitudes from sea level to 2400 m altitude. It is more common in Uganda, with its extensive swampy areas, than in Kenya and Tanzania, where it tends to be limited to the hills, lakesides, rivers and irrigated areas. Sesamia calamistis has many plant hosts in addition to rice. Sesamia calamistis is an important pest of rice, maize, millet and sorghum in Africa and Madagascar (Appert and Ranaivosoa 1970; Khan et al. 1991; Schulthess et al. 1991; Hamadoun 1992; Dale 1994). In Ghana, Echinochloa provides a potential source for the S. calamistis infestation on sugarcane (Sampson and Kumar 1986). In a survey conducted in the rainforest region of Côte d’Ivoire in 1994 (Heinrichs and Schulthess 1994), Sesamia larvae were present in maize as a monocrop and as a mixed crop with rice and in rice when grown as a mixed crop with maize. Infestation of the rice crop by S. calamistis is highest at the latter part of the crop growth stage occurring from the end of the booting stage to maturity. In irrigated rice in the Sahel at Kogoni, Mali, S. calamistis larval numbers in rice stems were first observed in the booting stage. Larval populations in both 1986 and 1987 peaked twice, at the end of the panicle initiation stage and again at maturity (Hamadoun 1992). The surveys in Côte d’Ivoire (Heinrichs and Barrion 2004) indicated that Sesamia spp. larvae were present in rice stems in the vegetative, booting and flowering–ripening stages. Their portion of the total stem borer complex in the flowering–ripening stage was highest in the August and October surveys. In the vegetative stage, Diopsis predominated in the three survey dates. Percentage of stem borer-damaged tillers infested with Sesamia larvae increased with crop age, reaching a peak in the flowering–ripening stage in both the July and August surveys. Both light and pheromone traps have been used to study the seasonal occurrence of S. calamistis moths in irrigated rice at Kogoni, Mali (Hamadoun 1992). Rains in this part of the Sahel begin in June after a long, harsh, dry season and continue to December. In 1987, there were three major flights. Moths began flying in early August, reaching a peak in mid-August, and again peaking in mid-September and mid-October and terminating in early November. Because the rice plants are generally attacked at the later growth stages by Sesamia spp., whiteheads are the primary result. Young larvae occupy the stalk at the base of the panicle causing whitehead development, but they feed lower in the stem as they become older. Rice plant density and fertiliser level effects on rice plant damage caused by S. calamistis were studied under lowland rice conditions in Kenya (Ho and Kibuka 1983). Plant damage was similar at plant spacings of 10 x 20 and 20 x 20 cm, but there were significantly more empty grains that resulted from S. calamistis at 120 kg N than at 0 or 60 kg N ha−1.

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2.14 African pink borer, Sesamia nonagrioides botanephaga Tams and Bowden; (Lepidoptera: Noctuidae) Distribution: Asia – Iran; Africa – Côte d’Ivoire, Ghana, Liberia, Nigeria, Senegal, Togo (Heinrichs and Barrion 2004). Host plants other than rice: Saccharum officinarum L., Zea mays L. (CABI 2016c). Description and biology: Akinsola and Agyen-Sampong (1984) and Pollet (1977) described the life history of S. nonagrioides botanephaga. Eggs are laid on the leaf near ligules. The incubation period is 5–7 d. The L1 larva moves towards the leaf tip upon hatching and hangs from a silken thread. It is then blown to another leaf of the same plant or to another plant. After aerial transport, the L1 moves onto the stem and penetrates the nearest internode and feeds within the stem. The larva is a pinkish colour with a dark brown head (Fig. 2.25). There are six larval instars and the total larval period lasts from 40 to 50 d. Pupation occurs within the lumen of the internode nearest the plant base. There is only one pupa per stem. The pupal period is from 10 to 12 d. The moth is yellowish brown in colour with a narrow band of black scales in the centre of the forewing (Fig. 2.26). Plant damage and ecology: Sesamia nonagrioides botanephaga, next to Sesamia calamistis, is the second most common Sesamia species in rice and is limited to

Figure 2.25 Sesamia nonagriodes botanephaga larva (Source: HYPPZ Database – INRA; http://www7. inra.fr/hyppz/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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the tropical and equatorial areas of Africa. Sauphanor (1985) considers S. calamistis to be the main stem borer of upland rice in Côte d'Ivoire. Sesamia nonagrioides botanephaga is also an important maize pest in West Africa (Shanower et al. 1993). In Ghana, it causes such extensive losses in second-season maize (August–November) in the rainforest zone that farmers are reluctant to plant maize during that season (Tams and Bowden 1953). The effect of feeding damage by S. nonagrioides botanephaga on rice development has been described in detail by Akinsola (1984). Infestation by larvae in the tillering stage of crop growth resulted in the development of deadhearts. Feeding damage caused a significant increase in number of tillers. However, at harvest, uninfested plants had higher numbers of productive tillers. This indicated that the initial increase in tiller numbers in infested plants did not result in a corresponding increase in productive tillers at harvest. Thus, it appeared that the compensatory tillers contributed little to ultimate yield because they do not produce mature panicles at harvest. Feeding of the larvae also caused a significant reduction in the number of filled grains. Larval infestation of plants at the booting stage caused yield loss by reducing the number of productive tillers through the formation of whiteheads. Infestation at this stage also caused the growth of compensatory tillers but these tillers were not able to produce panicles before harvest (Akinsola 1984).

Figure 2.26  Sesamia nonagriodes botanephaga adult (Source: © Diego Regglanti; http://lepidop tera.pro). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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2.15 Asiatic pink stem borer, Sesamia inferens Walker (Lepidoptera: Noctuidae) Distribution: Asia – Bangladesh, Bhutan, Brunei, Cambodia, China, India, Indonesia, Japan, Korea, Laos, Malaysia, Myanmar, Nepal, Pakistan, Philippines, Singapore, Sri Lanka, Taiwan, Thailand, Vietnam; North America – the United States; Oceania – Guam, Papua New Guinea, Solomon Islands (CABI 2016g). Host plants other than rice: Beckmania crucaefonnis (L.) Host., Cymbopogon nardus (L.) Rendle, Cyperus japonicus Houtt., Echinochloa crus-galli (L.) Beauv., Echinochloa frumentacea Link, Eleusine coracana (L.) Gaertn., Hemarthria compressa (L. f.) R. Br., Hordeum vulgare L., Panicum maximum Jacq., Paspalum scrobiculatum L., Paspalum thunbergii Kunth ex Steud., Phragmites karka (Retz.) Trin ex Steud., Polypogon fugax Nees, Saccharum arundinaceum Retz., Saccharum officinarum L., Saccharum spontaneum L., Scirpus maritimus L., Sclerostachya fusca (Roxb.) A. Camus, Setaria italica (L.) Beauv., Sorghum bicolor (L.) Moench., Triticum aestivum L., Zea mays (L.) (Dale et al. 1994). Description and biology: The pink borer, first described in 1894 (Islam and Catling 2012), is probably the least destructive pest among the rice stem borers. This may be due to its extreme polyphagy. Outbreaks in rice usually result from a population spill over from adjacent sugarcane fields or other alternate hosts (Dale 1994). The adult moth (Fig. 2.27) is fawn, the forewings being tan with dark brown markings. From a centred point in the forewing, greyish black lines radiate towards the wing tips ending in a thin terminal line of dark spots. There are tufts of hair on the pronotum. The hindwings are white. The wingspan is 30–35 mm in the female and 20–30 mm in the male. The body length is 14–17 mm. Male and female moths can be easily distinguished by observing their antennae; they are pectinate in the male but filiform in the female (Patel and Rajesh Verma 1980).

Figure 2.27  Sesamia inferens adult (Source: © 2013, ICAR-National Bureau of Agricultural Insect Resources. All Rights Reserved; http://www.nbair.res.in/insectpests/Sesamia-inferens.php).

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Bead-like, depressed, spherical (0.5 x 0.4 mm) eggs are laid in rows between the leaf sheath and stem, at 30 to 100 eggs per batch (Islam and Catling 2012). The female is known to lay over 400 creamy white to dark naked eggs. Eggs hatch in about a week. Larvae feed on a wide range of hosts. The larva (Fig. 2.28) has an orange-red head capsule and its body is purplish pink dorsally and white ventrally (Reissig et al. 1986). The head is relatively large compared to the rest of the body. The body is distinctly segmented with no stripes and it tapers towards the abdominal tip. The caterpillars do not tend to congregate but disperse early. They often come out of the stem of one host plant and bore into neighbouring rice plants thus destroying several plants. The larva becomes full grown in 4–5 weeks undergoing 5–7 moults. At this stage, it is 20–26 mm long. As the larvae are highly polyphagous, they can move to adjacent fields or border areas to complete their development even after the rice has been harvested. Pupation usually takes place inside the larval tunnel within the stem but occasionally occurs outside the stem between the leaf sheath and the stem. The pupa is dark brown with a tinge of purple on the cephalic region. It is 18 mm long and 4 mm wide. The pupal period is about a week. There are up to six generations in a year. Plant damage and ecology: Newly hatched larvae feed in the leaf sheath and then bore directly into the stem (Islam and Catling 2012).The larvae that penetrate a tiller feed on the inner surface of the stem walls and thus interrupt the movement of water and nutrients. The tunnelling caused by the larvae severs the vascular tissue but there are many conduits in a

Figure 2.28  Sesamia inferens larva (Source: Nigel Cattlin, Visuals Unlimited, Inc., USA; http:// visualsunlimited.photoshelter.com/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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stem and reduction in nutrient and assimilate flow can normally be shunted to undamaged vascular bundles unless the stem is completely severed. Tunnelling by the larvae weakens rice stems, which may easily break. If damage occurs when plants are young, the central leaves of the damaged tillers turn brown. This damage is called ‘deadhearts’. If the damage occurs after the spikelets form, panicles turn white and are chaffy (no grain filling occurs). These damaged panicles are called ‘whiteheads’. Whiteheads are a greater contributor than deadhearts to yield loss Tiller damage from ‘kresek’ (bacterial disease of rice) also resembles deadhearts. Drought and neck blast can also cause whiteheads. However, panicles damaged by stem borers differ in that they can easily be pulled out by hand and will show insect feeding damage at the base.

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2.16 South American white borer, Rupela albinella (Cram.) (Lepidoptera: Schoenobiidae) Distribution: Brazil, Colombia, Costa Rica, Ecuador, French Guiana, Guatemala, Guyana, Honduras, Mexico, Nicaragua, Panama, Peru, Surinam, Trinidad, Venezuela. Host plants other than rice: None known. Description and biology: The shining white moths (Fig. 2.29) are commonly seen resting on the uppermost leaf tips or flying near rice plants. The anal tuft is white in the male, while in the female moth it is yellow. The adult of this species has a 40 mm wingspan. Male moths live for 4–6 days and females 5–8 days (Dale 1994). Conspicuous yellow clusters of eggs are laid on the abaxial leaf surface (Ferreira and Martins 1984) leaves. Eggs are oval and yellowish green and are covered with yellow silken hairs (Fig. 2.30) from the anal tuft of the female moth. They are laid in batches of 80–120 and hatch in 8–9 days. Larvae of the white stem borer Rupela albinella are very agile, possess cream-coloured bodies with reddish brown heads, and are usually dispersed by wind. Mature larvae are approximately 30mm long with a head capsule width of 1.5 mm; the head appears reduced relative to the body size (Pessoa and Habeck 1987). There is a longitudinal dorsal brown stripe on the body. The activity of the larvae is mostly restricted to the lower portion of the rice plant. The larvae make characteristic holes in the stem before they pupate. The larval period is 35–50 days.

Figure 2.29 Rupela albinella adult (Source: E. A. Heinrichs). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Pupation takes place inside the stem in a white silken cocoon. The pupa is yellowish brown in colour. The pupal period is 10–13 days. The adult moth comes out through the hole previously cut by the larva. In Surinam, there are two main periods of moth emergence in a year. Diapause occurs only when the plant has flowered and it is also related to temperature. Plant damage and ecology: Damage is similar to that described under D. saccharalis. Rupela albinella is not normally a major pest of irrigated rice even though sometimes high populations occur. It can be a serious problem in upland rice. The damage is caused by the larvae feeding into the leaf sheath and tunnelling into the nodes. Yellowish stained patches below the axis of leaf sheaths indicate the white borer infestation. Yield losses due to this pest are most severe in Central and South America, where the South American white stem borer Rupela albinella is a serious pest of rice (AgriLIFE Res. 2011).

Figure 2.30  Rupela albinella egg mass (Source: Nigel Cattlin, Visuals Unlimited, Inc., USA; http:// visualsunlimited.photoshelter.com/).

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2.17 Sugarcane borer, Diatraea saccharalis (Fabricius) (Lepidoptera: Pyralidae) Distribution: Southern US, Central and South America to Argentina, West Indian Islands. Host plants other than rice: 15 wild grass species, Brachiaria mutica (Forssk.) Stapf, Leptochloa filiformis (Lam.) Beauv., Paspalum urvillei Steud., Saccharum officinarum L., Sorghum halepense (L.) Pers., Vetiveria zizanioides (L.) Nash, Zea mays L. Description and biology: Diatraea saccharalis is the most damaging and the widely distributed stem borer in the Americas. It is a pest of a variety of graminaceous crops in the southern USA, including sugarcane, maize, and rice in Louisiana (Hamm et al. 2012). In Texas it is more abundant than the rice stalk borer Chilo plejadellus (Bowling 1967). As its name suggests, the sugarcane borer is a key pest of sugarcane as well as rice. The adult sugarcane borer (Fig. 2.31) is a straw coloured moth approximately 2–2.5 cm in length. Moths show an inverted V-shaped series of black dots on their front wings. Adult moths have a wingspan of 20–26 mm. The forewings are light brown to grey with less continuous lines and a dark discal dot. During the day the moths hide under foliage. The adult population is highest when the rice plants are at about 30 DT. Rice in the reproductive stages of development (boot and panicle differentiation stages) is preferred over younger rice (tillering stage) for oviposition (Hamm et al. 2012). D. saccharalis prefers to oviposit on the uppermost portions of rice plants, regardless of

Figure 2.31 Diatraea saccharalis adult (Source: Thomas Riley/ LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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plant stage. Females lay their cream-coloured, oval-shaped eggs in clusters of two to 100 at night, although the number of eggs usually found in a single cluster is less than 50 (Dale 1994). Eggs are laid on young leaves on both the upper and lower surfaces. Eggs are creamy white when laid but turn yellowish as the incubation period advances. Larvae emerge in three to five days, and first and second instars feed on leaf blades or in between the leaf sheath and the stem. The newly hatched larvae move about and feed on rice leaves for 24–48 hours. They then crawl into the space between the leaf sheath and stem to make the entry hole and enter the stem and bore within. Sometimes these larvae come out of the initial tunnels and make new attacks on the same plant or search for other plants to infest. Larvae are pale yellowish white, with a brown head capsule and a series of brown spots on the back (Fig. 2.32). In the winter these spots are absent and the colour becomes more deeply yellow. Larvae pass through four or five instars in the stem in four to five weeks. Normally 5–6 larval instars can be distinguished. The fully grown larva is 25–35 mm long and makes an exit hole for the adult moth to emerge. Pupation takes place within the stem (Fig. 2.33). The pupa is light brown and 10–12 mm long. It is naked without being enclosed in a silken web. This insect may pass through four to five generations in a growing season in the cool northern and southern limits of the pest’s distribution. In the tropics, as many as seven generations develop.

Figure 2.32 Diatraea saccharalis larva in rice stem (Source: LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 2.33 Diatraea saccharalis pupa (Source: LSU AgCenter).

The sugarcane borer spends the winter as a larva in the stubble of host plants. The larvae pupate and moths emerge in spring. The insects breed on alternate host plants until rice plants are big enough to feed upon. Plant damage and ecology: Damage caused by the various stem-boring species including D. saccharalis is similar. Feeding by early instar stem borers on leaves and within leaf sheaths produces characteristic orange-tan lesions but is not economically damaging. Feeding within the culm on the growing point and vascular tissue can sever the growing portion of the plant from the base of the plant. When feeding occurs during the vegetative stage of plant development, the tiller in which the larva is present often dies and fails to produce a panicle (deadheart). When feeding occurs after panicle initiation, feeding by a larva within a stem results in drying of the panicle. Affected panicles may not emerge or, if they do, do not produce grains, remain straight and appear whitish (whitehead). Diatraea saccharalis, a major pest of sugarcane, is also an important rice stem borer in Louisiana, USA (Sidhu 2013, Sidhu et al. 2013). In 2002, for example, approximately 1,214 hectares of rice in Concordia Parish, Louisiana were infested with D. saccharalis which damaged 70 to 95 % of the rice crop on some farms (Castro et al. 2004). Diatraea saccharalis can also be a serious pest of rice in Texas, USA (Way et al. 2006, 2010) where rice was grown on 72,843 hectares in 2011 (Sidhu 2013).

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2.18 Lesser cornstalk borer (LCB), Elasmopalpus lignosellus (Zeller) (Lepidoptera: Pyralidae) The LCB, Elasmopalpus lignosellus (Zeller), was described by Zeller in 1848, but it was not considered to be of economic importance until 1881 (Riley 1882). Distribution: Mexico, Central and South America. The LCB occurs widely in the western hemisphere and is known from much of the southern US. It is not an important pest of rice in the United States but attacks rice in Mexico, Central and South America (Luginbill and Ainslie 1917). Because larvae spend considerable time in the soil they are most common in sandy soil and upland rice. Host plants other than rice: The LCB is a polyphagous pest that often attacks several crops. It has a number of weed hosts in the United States, including nutsedge (Cyperus rotundus), watergrass (Hydrochloa caroliniensis), Johnsongrass (Sorghum halepense), crabgrass (Digitaria sanguinalis), wild oats (Avena fatua), Bermudagrass (Cynodon dactylon), wiregrass (Aristida stricta) and goosegrass (Eleusine indica) (Isely and Miner 1994; Gardner and All 1982). Description and biology: The below discussion is based on studies in Southeastern US (http://entnemdept.ufl.edu/creatures/field/lesser_cornstalk_borer.htm) and Brazil (Ferreira 1998), where it is referred to as ‘broca do colo’.

Figure 2.34  Elasmopalpus lignosellus adult (Source: Larry McDaniel; http://porchlightinsects.blog spot.co.uk/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Adults (Fig. 2.34) are small moths about 8.5–10 mm in length with 15–25 mm wingspan and with a distinct eye and ‘horn’ on the head. Sexual dimorphism is pronounced in wing colour and pattern. In males, forewings are brownish yellow in the centre with dark borders. In females, forewings are dark brown or grey and uniform. The hindwings of both sexes are transparent with a silvery tint. The thorax is light in males, but dark in females. Adults are most active at night when the temperature exceeds 27°C, relative humidity is high and there is little air movement. Such conditions are optimal for mating and oviposition. Adult longevity under field conditions is estimated at about 10 days. Oviposition can occur on the stem and leaves, but usually is in the soil. A single female can oviposit about 200 eggs (Capinera 2001), with a report of up to 420 eggs (Ferreira 1998). The eggs are oval, measuring about 0.6 mm in length and 0.4 mm in width. When first deposited, they appear greenish, soon turn pinkish and eventually reddish. The female deposits nearly all her eggs below the soil surface adjacent to the plants. A few, however, are placed on the surface or on leaves and stems. Duration of the egg stage is two to three days. Larvae are strong and active when disturbed and wiggle violently so that in some countries it is called the ‘jumping borer’ (Schaaf 1974). Larvae live in the soil, constructing tunnels from soil and excrement tightly woven together with silk. They leave the tunnel to feed in the basal stalk area or just beneath the soil surface, returning and constructing new tunnels as they mature. Thus, tunnels often radiate out from the stem of the food source, just below the soil surface (Fig. 2.35).

Figure 2.35  Elasmopalpus lignosellus larva and silk tunnel (on soybean) (Source: James Solomon, USDA Forest Service, USA; https://www.forestryimages.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Normally there are six instars, but the number of instars can range from five to nine depending on environmental conditions (Biddle et al. 1992). During the early instars, larvae are yellowish green, with reddish pigmentation dorsally, tending to form transverse bands. As the larvae mature, whitish longitudinal stripes develop, and by the fifth instar they are pronounced (Fig. 2.35). The mature larvae are bluish green, but tend towards reddish brown with fairly distinct yellowish white stripes dorsally. Head capsules are dark in colour, and measure about 0.23, 0.30, 0.44, 0.63, 0.89 and 1.2 mm in width, respectively, for instars one through six. Larval lengths are about 1.7, 2.7, 5.7, 6.9, 8.8 and 16.2 mm, respectively. Mean development time is estimated at 4.2, 2.9, 1.4, 3.1, 2.9 and 8.8 days for instars one through six, respectively. Total larval development time varies widely, but normally averages about 20 days. At larval maturity, caterpillars construct pupal cells of sand and silk at the end of the tunnels. Cocoons measure about 16 mm in length and 6 mm in width. The pupae are yellowish initially turning brown and then almost black just before adults emerge. Pupae are about 8 mm long and 2 mm wide. The tip of the abdomen is marked by a row of six hooked spines. Pupal development time averages about 9–10 days, with a range of 7–13 days. There are three to four generations annually in the Southeast United States. Activity extends from June to November, with the generations overlapping considerably and little evidence of breaks between generations. Overwintering apparently occurs in the larval and pupal stage, and diapause does not occur. A complete life cycle usually requires 30–60 days. Plant damage and ecology: The larval stage causes damage when it feeds upon, and tunnels within, the stems of plants. Normally, the tunnelling is restricted to the basal region of stalks, including the below-ground portion, and girdling may occur. Wilting is one of the first signs of attack in affected plants and stunting and plant deformities are common. In Brazil, during the larval period of 13–39 days, larvae can bore into 5–10 rice stems where the damage results in the formation of deadhearts (Ferreira 1998). Deadheart symptoms are caused by the larva boring into the stalk at the soil level and tunnelling upward. They do not cause the development of whiteheads as most stem borers do. When the larvae become fully grown, they leave the plants and build silken and soil cocoons where they pupate (Ferreira and Barrigosi 2006). LCBs seem to be adapted to hot, xeric conditions, and therefore tend to be more abundant and damaging following unusually warm, dry weather.

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2.19 Mexican rice borer, Eoreuma loftini (Dyar) (Lepidoptera: Crambidae) Distribution: Mexico, the United States The moth is native to Mexico and has become a major pest of sugarcane in the southern United States since it was first discovered there in 1980. Host plants other than rice: Saccharum officinarum L. and numerous gramineae species. Description and biology: The Mexican rice borer, a devastating pest of sugarcane, is a serious pest of rice. The life history of the Mexican rice borer, as described by Saichuk (2012), is similar to that of the sugarcane borer. Mexican rice borer adults (Fig. 2.36) are light tan in colour, with delta-shaped wings. The apex of forewing is acute, and the light veins are edged on each side by a line of fine brown scales, which diffuse in the interspaces. The forewing has a small black discal dot in the centre, a row of terminal black dots in the interspaces which are connected by a slender line, and a brownish fringe. The hindwing has an expanse of 23 mm, is white with a slender brown line on the apical half, and lacks dots. Unlike the sugarcane borer, females prefer to lay eggs in folds on senesced or senescing leaves. Globular, cream-coloured eggs are deposited in clusters of less than 100. Larvae (Fig. 2.37) are whitish, with an orange-brown head capsule, and four purple red stripes

Figure 2.36 Eoreuma loftini adult (Source: LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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running parallel along the dorsal side. Larvae pass through five to six stadia in approximately five weeks in summer temperatures in rice with late instars measuring 2–2.5 cm. Pupation takes place inside the rice stem after mature larvae have constructed an emergence window covered by one or two layers of plant tissue. Emergence holes are smaller than those made by the sugarcane borer. The pupal stage lasts 7–21 days depending on temperature (Saichuk 2012). Mexican rice borers probably use non-crop hosts to a greater degree than sugarcane borers (Beuzelin et al. 2011). Four to six generations occur in the southern areas of the distribution of this insect, and this insect appears to be active year-round in the Gulf Coast region of Texas. Plant damage and ecology: Mexican rice borers overwinter as larvae in the stems of rice and other weedy plants. These larvae pupate in the spring, and adults attack rice when stem diameter is large enough to support larval feeding. Young larvae feed on the tissue inside the leaf sheath and bore into the rice stem after about one week of feeding (Saichuk and Meszaros 2011). Injury to rice results from stem borer larvae feeding on plant tissue as they tunnel inside the stem. Injury is often first noticed when the youngest partially unfurled leaf of the plant begins to wither and die, resulting in a condition called ‘deadheart’. Later in

Figure 2.37 Eoreuma loftini larva (Source: LSU AgCenter).

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the growing season, these rice stems are weakened and may lodge before harvest. Stem feeding that occurs during panicle development causes partial or complete sterility and results in the ‘whitehead’ condition (Saichuk and Meszaros 2011). The white, empty panicles are light in weight and stand upright. Severe infestations cause stalk breakage and plant lodging.

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2.20 Asian rice gall midge, Orseolia oryzae (Wood-Mason) (Diptera: Cecidomyiidae) Distribution: Bangladesh, Burma, Cambodia, China, India, Indonesia, Laos, Malaysia, Myanmar, Nepal, Pakistan, Sri Lanka, Taiwan, Thailand, Vietnam (CABI 2016d). Host plants other than rice: Cynodon dactylon (L.) Pers., Echinochloa colona (L.) Link, Heteropogon contortus (L.) Beauv., Ischaemum aristatum L., Leersia hexandra Sw., Oyza barthii A. Chev., Panicum miliaceum L., Paspalum scrobiculatum L., Sacciolepis interrupta (Willd.) Stapf. Description and biology: The adult gall midge (Fig. 2.38) is similar in appearance to a mosquito. Females have bright red abdomens. Mating takes place soon after emergence and egg laying starts a few hours later. The female flies mate only once and the unmated ones lay sterile eggs. Adults are nocturnal in habit and are highly attracted to light traps. Eggs are laid either singly or in groups on the underside near the base of rice leaves or sometimes on leaf sheaths. A single female lays 100–200 eggs either singly or in groups. The males mostly die in 12–18 hours after emergence; females live up to 3 days (Dale 1994). Eggs are long, tubular, and shiny white; sometimes with pink, red or yellow shades. They turn amber before hatching. Eggs require high humidity for development and hatching. The incubation period is around 3–4 days (Reissig et al. 1986).

Figure 2.38 Orseolia oryzae adult (Source: www.flickr.com). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The newly hatched maggots are greyish white, fairly stout with a pointed anterior end. They wiggle down the leaf blade in a film of dew and move between the leaf sheath and the stem until they reach the opening point of the apical or side bud at a node. The larva feeds inside the developing bud, which is a zone of differentiation for new tillers. A hollow chamber called a ‘gall’ forms around the larva. As the larva feeds the gall enlarges at the base and elongates having the appearance of an onion leaf (Fig. 2.39). There are three larval instars; total larval period is 15–20 days. Generally, only one maggot is found in a tiller. Pupation takes place inside the gall. The male and female pupae can be easily separated by their size and colour of the abdomen (Panda and Mohanty 1970). Male pupae are small and brown while the females are larger and pinkish. The colour turns darker before adult emergence. The pupa has several rows of abdominal spines that enable it to move up to the tip of the gall before adult emergence. The pupa makes a hole at the gall tip with its spines and the midge emerges through this hole leaving the pupal skin behind. Adult emergence generally takes place at night or early morning. The pupal period varies from 2 to 8 days. The entire life cycle is completed in about 25–38 days (Reissig et al. 1986). The gall midge remains inactive as a pre-pupa in wild rice or weeds during the dry season. At the onset of the monsoons, it becomes active and completes one or two generations in grasses before it moves to the rice crop (Reddy 1967). In India, pest incidence is high during July and August if there is rainfall during the daytime. This period coincides with the maximum tillering phase in rice. The population then declines rapidly in December, primarily, because of the limited availability of suitable host plants. In some cases, the pest infests rice stubbles left after the first crop.

Figure 2.39 Galls caused by O. oryzivora larvae (Source: O. E. Oyetunji). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: O. oryzae is primarily a pest of low-land irrigated and rainfed rice, including deepwater rice, but it has occasionally been reported in upland rice (Islam and Catling 2012). This pest was formerly considered a minor pest of rice in Bangladesh. However, there is strong evidence that the more favourable microclimate provided by the high-tillering varieties, and intensive management practices associated with the Green Revolution, has increased the extent and severity of the Asian rice gall midge in Bangladesh. This is also believed to be the case in China, India, Indonesia and Thailand (Islam and Catling 2012). The main external symptom of gall midge attack is a ‘silver shoot’ or ‘gall’ that resembles an onion leaf. A fully developed gall is a silvery white, hollow tube, about 1 cm wide and 10–30 cm long. Larval feeding suppresses leaf primordial differentiation at the growing tip. This, in turn, induces the development of radial ridges from the innermost leaf primordium followed by an elongation of the leaf sheath (Perera and Fernando 1970). Galls appear within a week after the larvae reach the growing point. Gall midge attack of rice seedlings leads to profuse tillering and stunting of the plants. A late infestation of the plants at the reproductive shoot apex causes malformed leaves and panicles. Israel et al. (1959) reported 0.5% loss in yield for every unit per cent increase in incidence. But wide varietal differences exist in the effect of infestation on crop losses. In certain varieties, gall formation is not manifested and instead necrosis of the shoot apex results (Pieris 1977). The gall midge attacks rice from the nursery to the end of tillering stage. Young maggots cannot survive in plants past the vegetative stage as there are no actively growing apical buds for them to infest. The periodicity of infestation and extent of damage caused by the gall midge varies in different countries. In Thailand, the pest has long been reported associated with the rainfed rice of the North, Northeast and Eastern regions, but in the 1970s, outbreaks in the irrigated dry season rice of the Central Plains occurred (Katanyukul et al. 1980a). The Asian rice gall midge, a major insect pest of rice in India (Bentur et al. 2003), was previously a pest only in the wet season crop but later it was observed in the winter crop as well (Kalode and Kasiviswanathan 1976). It has been reported from almost all the states except Uttaranchal, Punjab, Haryana and hill states of Himachal Pradesh and Jammu and Kashmir (Bentur et al. 1992, CABI 2016d) ). In India, crop losses ranging from 10 to 100% have been reported (Siddiq 1991). Average annual yield loss due to the pest in India is estimated to be US$80 million (Ramaswamy and Jatileksono 1996). In Sri Lanka, high infestations of gall midge were observed in the southwest monsoon season (April–July) in the wet zone while in the intermediate and dry zones, they were mostly seen during the northeast monsoon (October–November) (Kudagamage and Nugaliyadde 1981). The extent of damage caused by O. oryzae as reported by various workers is presented in Table 2.2. Wongsiri et al. (1971) reported the ecological conditions that usually prevailed in Thailand at the times when gall midge populations were high. The sky was cloudy most of the days and the relative humidity was 75% on an average; the optimum mean temperature for adult emergence and oviposition ranged from 23 to 27°C. Hidaka et al. (1974) observed that seasonal fluctuations of gall midge populations were closely related to rainfall. Overcast skies and drizzling rains are favourable for rapid build-up of pest populations. Israel et al. (1961) reported an increase in the pest population with high nitrogen levels. The incidence decreased with high levels of phosphate in combination with nitrogenous fertilisers. The infestation generally increased with higher levels of potash (Israel et al. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Table 2.2 Damage caused by O. oryzae in South and Southeast Asia rice Country

Zone

Season

Damage

Reference

India

Tamil Nadu

Late

30% hills

Natarajan and Chandy 1978

India

Uttar Pradesh

Late

65% hills

Rizvi and Singh 1980

India

Madhya Pradesh

Second crop

45% hills

Kaushik et al.1979

India

Karnataka

−

50% yield

Subramanian 1935

India

Nizamabad

−

30% yield

Khan and Murthy 1955

India

−

−

15% yield

Israel 1959

India

−

−

25% yield

Lever 1970

Thailand

−

−

50% yield

Grist 1965

Thailand

Northern

Wet

33% yield

Katanyukul et al. 1980b

Thailand

Northeastern

Wet

27% tillers

Katanyukul et al. 1980b

Sri Lanka

Dry & Intermediate

Maha

44% tillers

Wickremasinghe 1969

Sri Lanka

Dry & Intermediate

Yala

23% tillers

Wickremasinghe 1969

Sri Lanka

Dry & Intermediate

Maha

100% hills

Wickremasinghe 1969

Sri Lanka

Dry & Intermediate

Yala

18% hills

Wickremasinghe 1969

Sri Lanka

Wet

Yala

80% yield

Wickremasinghe 1969

October

60% hills

IRRI 1978

China

1963). Prakasa Rao (1972) observed an increased number of absolute tillers and infested tillers per unit area with the application of increased levels of nitrogen. Close spacing of transplanted rice resulted in a greater number of tillers and more leaves per unit area and an increase in relative humidity within the plant canopy which was suggested as the reason for higher gall midge incidence than under wider spacing (Prakasa Rao 1975). Variable reactions of differential rice varieties to O. oryzae have provided evidence of different biotypes in South and Southeast Asia (Heinrichs and Pathak 1981). The variability of the species is indicated by six biotypes in different regions of India (Bentur et al. 2003). Behura et al. (1999) developed a polymerase chain reaction (PCR)-based assay that distinguished different biotypes of the Asian gall midge (O. oryzae). This assay is faster, more reliable and unaffected by environmental factors as compared to the common use of plant host differentials and midge feeding behaviour for identifying biotypes.

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2.21 African rice gall midge, Orseolia oryzivora Harris and Gagne (Cecidomyiidae: Diptera) Distribution: Benin, Burkina Faso, Cameroon, Chad, Côte d’Ivoire, Ghana, Guinea, Guinea-Bissau, Liberia, Malawi, Mali, Niger, Nigeria, Senegal, Sierra Leone, Sudan, Tanzania, Togo, Uganda, Zambia (CABI 2016e; Nwilene et al. 2006). The occurrence of distinct species of Orseolia on rice in Africa and Asia may be linked to the separate development of African and Asian cultivated rice. The Asian rice species, O.  sativa, probably grew along the foothills of the Himalayas and associated mountain ranges in Southeast Asia and south-western China and has been cultivated for about 9000 yr. The African rice species, O. glaberrima, probably originated in the swampy basin of the upper Niger River about 3500 yr ago (Chang 1976). The African rice gall midge (AfRGM) O. oryzivora was first observed as a pest of rice in Nigeria in the early 1950s, but at that time it was thought to be the Asian species, O.  oryzae (Harris 1960). As a result of the clarification of the taxonomy, Harris (1990) stated that the AfRGM had first been reported in Sudan in 1947, in Malawi in 1973, and in Senegal and Burkina Faso in 1980. He goes on to state that this simply reflects the level of entomological interest and not the spread of the species, which must have been present on rice in Africa for thousands of years. It seems likely that the species originated on O. glaberrima in West Africa and it is therefore endemic to that area. O. oryzivora is widely distributed in West Africa and has also been reported from Zambia (Alam et al. 1985b), Sudan (Harris 1987) and Malawi (Feijen and Schulten 1983). It also occurs in Tanzania where severe outbreaks were reported in the Kapunga Irrigated Rice Project, shortly after rice was first grown in the early 1990s (Heinrichs and Barrion 2004). Host plants other than rice: It occurs in weeds such as Paspalum polystachion (L.), P. scrobiculatum, (K Harris, c/o CABI Biosciences Division, Silwood Park, Ascot, UK, unpublished data), Panicum spp. and wild species of Oryza (C. Williams, c/o CABI Biosciences Division, Silwood Park, Ascot, UK, unpublished data). Description and biology: The AfRGM is similar in appearance, behaviour, biology, and in the plant damage caused, to that of the Asian gall midge O. oryzae. However Harris and Gagne (1982) reported that the two species are morphologically distinct in the larval, pupal and adult stages. They can be separated most easily in the pupal stage by the antennal horns, which are simple and terminate in a point in O. oryzivora but are bifid and terminate in two strong spines in O. oryzae. The description and biology of the AfRGM have been published by Bouchard et al. (1992), Breniere (1983), Umeh and Joshi (1993) and Dale (1994). The adult midge is similar in appearance to a mosquito. It is 4.8 mm in length and has a bright red abdomen; dark antennae, pronotum, and thorax; and black eyes. The adult is attracted to artificial lights and they can be used to increase the level of midge populations in field evaluations of rice germplasm for gall midge resistance. Mating of the adults takes place soon after emergence and oviposition begins within a few hours. The adults live about 2–4 d during which the female lays 100–200 eggs, either isolated, or in groups of three to five at the base of stems, on the ligule, near the base of rice leaves, or on leaf sheaths. Eggs are elongated (cigar-shaped) and shiny white. With development, they turn yellow and then amber with red spots that appear just before hatching. Eggs require © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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extremely high humidity for hatching, which may be a reason that they are pests during the rainy season and are most serious on rainfed lowland and irrigated rice. The incubation period is 3–4 d. Newly hatched larvae are greenish white and stout with a pointed posterior end. Larvae have two pairs of distinct spines, which disappear at the third larval instar, when the larvae become milky white with brown spiracles and distinct mouth hooks. The larvae, upon hatching, wiggle down the leaf blade in a film of dew and move between the leaf sheath and the stem until they reach the opening point of the apical or side bud at a node. Oviposition, egg development and penetration into the stem take about 5 d. The larvae feed within the developing bud, which is a zone of differentiation for new tillers. A hollow chamber called a ‘gall’ forms around each larva. Galls form from 16 to 18 d after hatching. There is only one larva per gall and the entire larval stage is spent within the gall. As the larva feeds, the gall enlarges at the base and elongates, having the tubular appearance of an onion leaf. The gall consists primarily of leaf sheath tissue with a small leaf at the tip. Because the leaf sheath tissue is light green, the gall is sometimes considered to be ‘silvery’, hence the name ‘silver shoot’. There are three larval instars and the larval period is from 15 to 20 d. Pupation occurs within the gall. When a gall is first observed, the insect in the gall is already in the pupal stage. The pupa has several rows of abdominal spines that enable it to move up to the tip of the gall before adult emergence. The pupa makes a hole at the gall tip. The pupal period varies from 2 to 8 d. The adult, upon emergence, exits the gall through the hole, leaving the pupal skin sticking out of the hole. Emergence of the adult takes place at night or in the early morning. The entire life cycle from egg to adult is 25–38 d. There may be several generations within a crop season. In a study conducted in Nigeria, the identification and differentiation of Orseolia species was made possible using SCAR-PCR analysis. Two major Orseolia species genotypes as well as Orseolia species genotype distribution and population structure in Nigeria were revealed by this study. The OSG-1a genotype that covers about 42% of yet unknown Orseolia species in Nigeria needs further investigation to establish their identity either as one new Orseolia species or as two or more new Orseolia species. This finding will further establish the actual number of Orseolia species in Nigeria, their genotype distribution and population structure. This type of information is needed to be able to develop cultivars with durable resistance to the AfRGM (Nwilene et al. 2010). Plant damage and ecology: O. oryzivora shows more extreme variations in abundance, both spatially and temporally, than other rice insect pests in West Africa. O. oryzivora is reported to occur in the humid tropical and Guinean and Sudanian savanna zones of West Africa, but is more abundant in the savannah (Heinrichs and Barrion 2004). In Nigeria, the AfRGM occurs in both the savanna and forest zones, but is most commonly found in the southern Guinean savanna region of the country (Ukwungwu and Joshi 1992). It is the only rice insect pest in West Africa for which there is evidence of a long-term trend of increasing abundance over the last few decades. Even at moderate infestation levels, gall midge attack can result in heavy crop yield loss under rainfed lowland conditions (Williams 1997). In studies conducted in Nigeria (Williams et al. 1994), host plant species important for the dry season survival of the gall midge varied according to locality and cropping pattern. In the forest zone, the insect survived the dry season on rice (O. sativa ratoons) in the rice field, but in the savanna zone, wild perennial rice (O. longistaminata) was the dry

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season host, with O. sativa ratoons providing a bridge between O. longistaminata and the following rice crop. During crop growth, AfRGM attack occurs from the nursery or seedling stage to the end of the tittering stage. Young larvae cannot survive in the plants past the vegetative stage, as there are no actively growing apical buds for them to infest. The rice gall midge produces a distinctly characteristic plant damage symptom – a gall resembling an onion leaf (Fig. 2.39). Size of the gall varies depending on the host plant, but is usually about 3 mm wide and 10–30 cm long. In studies conducted in Nigeria, gall length was reported to be from 26 to 41 mm. Abnormal galls (spiral and twisted) were also observed (Ukwungwu and Joshi 1992). The gall formation process due to the larval feeding of O. oryzivora is similar to that described for O. oryzae (Perera and Fernando 1970). Each gall represents a tiller that will not produce a panicle. After adult emergence, the gall turns yellow and then dries. The plant responds by producing new tillers that may in turn be attacked by the gall midge. If the new tillers are not attacked, they may produce a panicle, but maturity will be severely delayed. O. oryzivora has risen to the status of a major rice pest in certain regions of Nigeria (Ukwungwu et al. 1989). However, surveys have indicated that gall midge infestations in other West African countries are minimal compared to Nigeria. In 1995, when the gall midge was first observed in Sierra Leone, infestations as high as 27% of hills attacked were observed in some farmers’ fields (Taylor et al. 1995). A 1995 wet season survey conducted by Hamadoun (1996) at six sites in the central and southern portion of Mali indicated per cent tiller infestation levels ranging from 0.5% at Klela to 17 and 24% at Longorola and Baguineda, respectively. In a survey conducted in lowland fields of Côte d'Ivoire, Guinea and Guinea-Bissau during the 1995 wet season (Heinrichs et al. 1995), tiller infestation was 1.6, 0.9 and 2.0%, respectively. In West Africa, Nigeria is reported to be the 'hot spot' for gall midge infestations. Since the early 1950s, when the AfRGM was first observed as a pest of rice in Nigeria (Harris 1960), it has continued to increase in importance (Umeh et al. 1992). Severe gall midge incidence in Nigeria was reported in the states of Plateau and Niger (Ukwungwu et al. 1984). In 1988, there was a severe outbreak in the Guinean savanna zone. Most severe damage was in Abakaliki in Anambra states (present Ebonyi State), where up to 80% tiller infestation was observed. About 50 000 ha of rice were damaged and total grain losses were recorded in severely infested fields. Outbreaks also reached catastrophic proportions in the forest zone in Cross River State in 1989 and in Akwa Ibom State. These outbreaks attracted national attention because they came at a time when rice importation had been prohibited. Suggested reasons for the outbreaks were (1) favourable weather with high rainfall, extensive cloud cover and high humidity; (2) staggered planting of highly susceptible varieties that provide a continuity of favourable host plants; (3) the sale and exchange of gall midge-infested rice seedlings; and (4) the application of insecticides that have adverse effects on natural enemies (Ukwungwu et al. 1989). Few experiments to determine grain yield losses due to AfRGM infestation have been reported in Africa. Studies over a 5-yr period using the insecticidal check method were conducted in the irrigated rice area in Karfiguela, south-western Burkina Faso (Nacro and Dakouo 1990). Yield losses in 1982, 1983, 1984, 1986 and 1987 were, respectively, 19, 17, 11, 11 and 3%. Williams (1997) conducted on-station and on-farm AfRGM yield loss trials in Nigeria. In on-station trials, he observed a yield loss of 0.5% for every 1% increase in infested © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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tillers at 84 DT. Results suggested that, under the fertile conditions of experiment station fields, plants compensated well to gall midge attack by producing new tillers. This compensation continued even after the time at which uninfested tillers would have passed the panicle initiation stage. In on-farm trials, yield losses were 2.3 (favourable site) and 3.1% (unfavourable site) per 1% increase in tillers with galls at 63 DT. This was considerably higher than in the on-station trial. Thus, one gall per five tillers at 49–63 DT caused 40 and 60% yield losses, respectively. Nacro et al. (1995) studied the relationship between gall midge adult populations and yield losses in 1-m2 plots of caged rice seedlings in Burkina Faso. Yield losses ranged from 22% at one midge pair to 65% with 25 pairs m−2. The infestation by the insects on the plants resulted in compensatory tillers that developed in response to the damage. However, the compensation was not sufficient to make up for the loss of yield due to the damaged tillers. One per cent of tillers damaged resulted in 2% grain yield loss. Certain cultural practices affect population levels of the Asian gall midge. In Nigeria, nitrogen and close plant spacing increased the number of gall midge-infested tillers (Ukwungwu 1987b). Some antixenotic and antibiotic properties were discovered to be responsible for the level of gall midge infestation. The antixenotic properties include plant leaf length, leaf glossiness and wetness. A study conducted at AfricaRice station in Ibadan, Nigeria, in 2012 and 2013, showed that leaf length is associated with the level of resistance to AfRGM in rice genotypes. A short leaf increases the chance that the newly hatched larva will reach the leaf sheath while a longer leaf decreases the chance of the larva surviving long enough to reach the sheath. The rate of leaf glossiness and leaf wetness are associated with susceptibility to AfRGM. While leaf glossiness accelerates the rate at which larva bore into the stem, leaf surface wetness facilitates larval movement down the sheath. Antibiotic compounds responsible for the level of resistance in rice to the gall midge include silica, salicylic acid, phenol and monoterpenoid content (Oyetunji et al. 2014). High silica content in the epidermal layers gives strength and rigidity to the growing leaf blades and thus deters feeding by insects, thereby preventing the ovipositor on the leaf and the larva from further penetration into the plant. Salicylic acid includes some of the key endogenous chemical mediators of plant defence signal transduction. Phenols contain toxic molecules which disrupt pest/pathogen metabolism or cellular structure but are often pest and pathogen specific in their toxicity. Monoterpenoid is a primary component of the essential oil containing alpha-monoterpenoids and beta-pinene, which are potent insect toxins and repellents (Oyetunji et al. 2014). Parasitism is extremely important in the natural control of the AfRGM (Nacro et al. 1995). Dakouo et al. (1988) reported larval parasitism up to 77% in Burkina Faso. However, parasitism was mainly due to the microhymenopterans, Platygaster oryzae Cameron and Aprostocetus procerae (Risbec), both of which are established late in the crop cycle. Ukwungwu and Joshi (1992) reported P. diplosisae, A. pachydiplosisae and Aphanogmus spp. as parasitoids of the gall midge in Nigeria, with P. diplosisae being the dominant species. Predators of AfRGM include Cyrtorhinus viridis (Heteroptera: Miridae), Conocephalus longipennis (Orthoptera: Tettigoniidae), Anaxipha longipennis (Orthoptera: Gryllidae) and ladybird beetles (Coleoptera: Coccinellidae) (Nwilene et al. 2006). Part of the natural biological control strategy is habitat manipulation to increase the carry over of parasitoids from the ‘paspalum gall midge’ on Paspalum scrobiculatum during the dry season cultivation which pass to AfRGM on rice, early in the wet season (Nwilene et al. 2006). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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2.22 References Abu, J. F. 1972. The bionomics of Diopsis (Diptera: Diopsidae) and Epilachna similis (Coleoptera: Coccinellidae) on Oryza sativa L. in the Accra plains. MS thesis, University of Ghana, Legon. AgriLIFE Res. 2011. Texas Rice (Beaumont, Texas) Vol. XI, No. 4 Akinsola, E. A., Agyen-Sampong, M. 1984. The ecology, bionomics, and control of rice stem-borers in West Africa. Insect Sci. Appl. 5:69–77. Akinsola, E. A. 1975. Present status of different rice stem stem borers in plants of Nigeria. Rice Entomol. Newsl. 3:28. Akinsola, E. A. 1979. The biology and ecology of rice stem borers in Nigeria. PhD thesis, University of Ibadan, Nigeria. Akinsola, E. A. 1980a. Notes on damage caused by Maliarpha separatella on deep-flooded rice in Mal. WARDA Tech. Newsl. 2(2):1. Akinsola, E. A. 1980b. Effets d’infestation de Diopsis thoracica (West.) sur les plants de riz. Bull. Tech. ADRAO 2 (2):3–4. Akinsola, E. A. 1984. Effects of rice stem borer infestation on grain yield and yield components. Insect Sci. Appl. 5:91–4. Akinsola, E. A. 1990. Management of Chilo spp. in rice in Africa. Insect Sci. Appl. 11:815–23. Alam, M. S. 1988. Seasonal abundance of rice stem borer species in upland and irrigated rice in Nigeria. Insect Sci. Appl. 9:191–5. Alam, M. Z., Ahmad, A., Siddique, A. 1964. Field test of insecticides against rice borers in East Pakistan. Pak J. Sci. 16:259–62. Alam, M. S., John, V. T., Zan, K. 1985a. Insect pests and diseases of rice in Africa. In Rice Improvement in Eastern, Central and Southern Africa, pp. 67–82. Manila, Philippines, International Rice Research Institute. Alam, M. S., Zan, K., Alluri, K. 1985b. Gall midge (GM) Orseolia oryzivora H. and G. in Zambia. Int. Rice Res. Newsl. 10(2):15–16. Alghali, A. M. 1979. Weed hosts of diopsid (Diptera) rice stem borers in Southern Nigeria. Int. Rice Res. Newsl. 4(4):21–2. Alghali, A. M. 1983. Relative susceptibility of some rice varieties to the stalk-eyed fly Diopsis thoracica West. Insect Sci. Appl. 4:135–40. Alghali, A. M. 1984. The selection of pupation sites by the stalk-eyed fly Diopsis thoracica (Diptera: Diopsidae) and pupal parasitism in some rice cultivars. Ann. Appl. Biol. 105:189–94. Alghali, A. M., Domingo, J. S. 1982. Weed hosts of some rice pests in Sierra Leone. Int. Rice Res. Newsl. 7(2):10. Alghali, A. M., Osisanya, E. O. 1981. Effects of rice plant age on diopsid oviposition and plant susceptibility. Int. Rice Res. Newsl. 6(6):17–18. Alghali, A. M., Osisanya, E. O. 1984. Effect of damage by the stalk-eyed fly (Diopsis thoracica) on yield components of rice. Exp. Agric. 20:225. Appert, J. 1970. Maliarpha separatella (borer blanc du riz). Observations nouvelles et rappel des problèmes entomologiques du riz à Madagascar. Agron. Trop. 25:329–67. Appert, J., Ranaivosoa, H. 1970. Sesamia calamistis Hampson (Lep. Noctuidae) chenille mineuse des graminées. Bull. Madagascar 20:633–52. Banerjee, S. N., Pramanik, L. M.1967. The lepidopterous stalk borers of rice and their life cycles in the tropics. In International Rice Research Institute (Ed.), The Major Insect Pests of the Rice Plant, pp. 103–24. Proceedings of a symposium at the International Rice Research Institute, September, 1964. Johns Hopkins Press, Baltimore, USA. Behura, S. K., Sahu, S. C., Rajamani, S., Devi, A., Mago, R., Nair, S. and Mohan, M. 1999. Differentiation of Asian rice gall midge, Orseolia oryzae (Wood-Mason), biotypes by sequence characterized amplified regions (SCARs). Insect. Mol. Biol. 8(3):391–7. Bentur, J. S., Pasalu, I. C. and Kalode, M. B. 1992. Inheritance of virulence in rice-gall midge (Orseolia oryzae). Indian J. Agric. Sci. 62:492–3.

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Bentur, J. S., Pasalu, I. C., Sharma, N. P., Prasada Rao, U., Mishra, B. 2003. Gall midge resistance in rice: Current status in India and future strategies. DRR Research Paper Series 01/2003. Directorate of Rice Research, Rajendranagar, Hyderabad, India. Beuzelin, J. M., Meszaros, A., Reagan, T. E., Wilson, L. T., Way, M. O., Blouin, D. C., Showler, A. T. 2011. Seasonal infestations of two stem borers (Lepidoptera: Crambidae) in non-crop grasses of Gulf Coast rice agroecosystems. Environ. Entomol. 40:1036–50. Bianchi, G., Rasoloarison, B., Genini, M. 1993. Noxiousness of the African white stem borer, Maliarpha separatella Rag (Pyralidae: Phycitinae) in irrigated paddy fields at Lake Alaotra (Madagascar). Insect Sci. Appl. 14:667–73. Biddle, A. J., Hutchins, S. H., Wightman, J. A. 1992. Pests living below ground, Elasmopalpus lignosellus: Lesser cornstalk borer. In McKinley, R. G. (Ed.), Vegetable Crop Pests, pp. 202–3. CRC press, Boca Raton, FL. Bonzi, S. M. 1982. Chilo diffusilineus J. de Joannis (Lepidoptera: Pyralidae), a cereal stem borer in irrigated and rainfed crops in Upper Volta. Agronomie Tropicale 37:207–9. Bouchard, D., Ouedraogo, A., Boivin, G., Amadou, K. 1992. Mass rearing and life cycle of the African rice gall midge, Orseolia oryzivora H. & G. in Burkina Faso. Trop. Pest Manage. 38:450–2. Bowling, C. C. 1967. Insect pests of rice in the United States. In International Rice Research Institute (Ed.), The Major Insect Pests of the Rice Plant, pp. 551–70. Proceedings of a symposium at the International Rice Research Institute, September, 1964. Johns Hopkins Press, Baltimore, USA. Brenière J. 1969. Importance des problèmes entomologiques dans le développement de la riziculture de l’Afrique de l’Ouest. Agron. Trop. 24:906–27. Brenière J. 1976. Reconnaissance des principaux lepidopteres du riz de l’Afrique de l’Ouest. Agron. Trop. 31:213–31. Brenière J. 1982. Lepidopterous borers of rice in West Africa: biology, damage and control. In: Integrated pest management in rice in West Africa. Proceedings of a seminar on Concepts, Techniques, and Applications of Integrated Pest Management in Rice in West Africa, 10–28 January 1982. Fendall (Liberia), West Africa Rice Development Association, pp. 20–32. Brenière J. 1983. The principal insect pests of rice in West Africa and their control. Monrovia (Liberia), West Africa Development Association CABI. 2015a. Chilo auricillius (gold-fringed rice borer) Invasive species compendium. http://www. cabi.org/isc/datasheet/18759 CABI. 2015b. Chilo polychrysus (dark-headed striped borer). Invasive species compendium. http:// www.cabi.org/isc/datasheet/44561 CABI. 2015c. Chilo partellus (spotted stem borer) Invasive species compendium. http://www.cabi. org/isc/datasheet/12859 CABI. 2015d. Chilo suppressalis. Distribution Maps of Plant Pests 1977 No. December pp. Map 254 (Revised) http://www.cabdirect.org/abstracts/20056600254.html;jsessionid=763380931F6628 D579D6AA5E0E33DE64 CABI. 2015e. Scirpophaga incertulas (yellow stem borer). Invasive Species Compendium. http://www. cabi.org/isc/datasheet/49009 CABI. 2015f. Scirpophaga innotata. Distribution Maps of Plant Pests 1985 No. December pp. Map 253 (Revised) ISSN 1369-104x http://www.cabdirect.org/abstracts/20056600253.html;jsessioni d=DD72A45D9E2A0E4CD32EDC7F64BA66F3 CABI. 2015g. Sesamia inferens (purple sem borer). Invasive Species Compendium, http://www.cabi. org/isc/datasheet/49751 CABI. 2016a. Maliarpha separatella (African white rice borer). Invasive Species Compendium. http:// www.cabi.org/isc/datasheet/32351 CABI. 2016b. Sesamia calamistis (African pink stem borer). Invasive Species Compendium. http:// www.cabi.org/isc/datasheet/49748 CABI. 2016c. Sesamia nonagrioides botanephaga. Invasive Species Compendium. CABI. 2016d. Orseolia oryzae (rice stem gall midge). Invasive Species Compendium http://www.cabi. org/isc/datasheet/37921

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CABI. 2016e. Orseolia oryzivora (African rice gall midge). Invasive Species Compendium. http://www. cabi.org/isc/datasheet/38391 Capinera J. L. 2001. Handbook of Vegetable Pests. Academic Press, San Diego, p. 729. Castro, B. A., Riley, T. J., Leonard, B. R., Baldwin, J. 2004. Borers Galore: Emerging Pests in Louisiana Corn, Grain Sorghum and Rice. Louisiana Agriculture 46, 4–7. Catling H. D. 1980. Deepwater Rice In Bangladesh: A Survey of Its Fauna With Special Reference to Insect Pests. Overseas Development Administration of the United Kingdom, p. 100. Catling H. D. 1982. Yellow rice borer incidence in deepwater rice in Thailand, 1981. Intl. Rice Res. Newsl. 7(2):11. Catling H. D, Alam S. 1977. Rice stem borers. In: Literature Review of Insect Pests and Diseases of Rice in Bangladesh. Bangladesh Rice Research Institute, pp. 5–29. Catling H. D., Islam Z., Pattrasudhi A. R. 1987. Assessing yield losses in deepwater rice due to yellow stem borer, Scirpophaga incertulas (Walker), in Bangladesh and Thailand. Crop Prot. 6:20–27. Chang T. T. 1976. The origin, evolution, cultivation, dissemination and diversification of Asian and African rices. Euphytica 25:425–41. Chang P. 1981. Insect pests of paddy in Malaysia. International symposium of problems of insect pest management in developing countries. Trop. Agric. Res. Ser. 14:1–11. Chiasson H., Hill S. B. 1993. Population density, development and behaviour of Diopsis longicornis and D. apicalis (Diptera: Diopsidae) on rice in the Republic of Guinee. Bull. Entomol. Res. 83:5–13. Cocherau, P. 1978. Fluctuations des populations imaginales de Diopsis thoracica Westwood et Diopsis apicalis Westwood (Diptera: Diopsidae) en liaison avec la phenologie d’un riz de basfond a Bouake’ (Cote d’Ivoire). Cahier ORSTOM Ser. Biol. 13:45–58. Cook, M. 1997. Revision of the genus Maliarpha (Lepidoptera: Pyralidae), based on adult morphology with descriptions of three new species. Bull. Entomol. Res. 87:25–36. Cork, A., Agyen-Sampong, M., Fannah S. J., Beevor P. S., Hall, D. R. 1991. Sex pheromone of female African white rice stem borer, Maliarpha separatella (Lepidoptera: Pyralidae) from Sierra Leone: identification and field testing. J. Chem. Ecol. 17:1205–19. Dakouo, D., Nacro S., Sie M. 1988. Evolution saisonniere des infestations de la cécidomyie du riz, Orseolia oryzivora H. et G. (Diptera: Cecidomyiidae) dans le sud-ouest du Burkina Faso. Insect Sci. Appl. 9:469–73. Dale, D. 1994. Insect Pests of the Rice Plant-Their Biology and Ecology. In Heinrichs, E. A. (Ed.), Biology and Management of Rice Insects, pp. 363–485. Wiley Eastern Limited, New Delhi and the International Rice Research Institute, Los Baños, Philippines. Dankers, C. 1995. The fear of heights of the stalk-eyed fly. Report on research conducted at WARDA. Netherlands: Departments of Agronomy and Entomology, Agricultural University of Wageningen (mimeo). Delucchi, V., Bianchi, G., Bousse, P., Graf, B., Rahalivavololona, N., Zahner, P. 1996. The biology and control of the African white rice borer, Maliarpha separatella Ragonot (1888) (Lep., Pyralidae, Phycitinae). Agric. Zool. Rev. 7:1–34. Descamps, M. 1957. Contribution de l’etude des diptères Diopsidae nuisibles au riz dans le nord. Agric. Trop. Bot. Appl. Cameroun 4:83–93. Diop, T. 1979. Entomological problems in the rice growing areas supervised by the SAED. WARDA Report, February 1979. Bouaké (Côte d’Ivoire), West Africa Rice Development Association. Doke, N. 1936. On the effect of temperature and moisture on the biology of Chilo simplex Butler. (in Japanese). I. Oyo-Dobuts. Zasshi 8:87–93. Feijen, H.R. 1979. Economic importance of rice stem borer (Diopsis macrophthalma) in Malawi. Exp. Agric. 15:177–86. Feijen, H.R. 1985. The correct names of the African rice stem boring Diopsidae (stalk-eyed flies). Int. Rice Res. Newsl. 10(5):21–2. Feijen, H.R. 1986. A revision of the Diopsidae (Diptera) described by J. W. Dalman. Entomol. Scand. 17:409–22.

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Williams, C. 1997. Final report of the project Management of the African rice gall midge (Orseolia oryzivora) in West Africa. ODA Holdback Project R 5619 (H). Wallingford (UK), Centre for Agriculture and Biosciences International. Williams, C., Heinrichs, E. A., Harris, K., Okhidievbie, O. 1994. Year-round monitoring of African rice gall midge in Nigerian outbreak areas. In Annual Report for 1994. Bouaké (Côte d’Ivoire), West Africa Rice Development Association. Wongsiri, T., Vungsilabutr, P., Hidaka, T. 1971. Study on ecology of the rice gall midge in Thailand. Trop. Agric. 267–90. 19–24 July 1971, Tokyo, Japan. Yasumatsu, K. 1976. Rice stem borers. In Delucchi, V. L. (Ed.), Studies in Biological Control, pp. 121– 37. Cambridge University Press, London. Zan, K., Perez, A. T., Alluri, K., Ng, N. Q. 1981. Problems and approaches on genetic improvement of rice in Sub- Sahelian Africa. IRRI Internal Program Review, 28 January 1981. International Rice Research Institute, Los Baños, Philippines.

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Chapter 3 Biology and ecology of rice-feeding insects: leafhoppers and planthoppers E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 3.1 Introduction 3.2 White rice leafhoppers 3.3 Green leafhoppers 3.4 Nephotettix afer Ghauri and Nephotettix modulatus Melichar 3.5 Nephotettix nigropictus Stål 3.6 Nephotettix cincticeps Uhler 3.7 Nephotettix virescens Distant 3.8 Nephotettix malayanus Ishihara et Kawase 3.9 Zigzag leafhopper 3.10 Smaller brown planthopper (Laodelphax striatellus Fallen) 3.11 Brown planthopper (Nilaparvata lugens Stål) 3.12 White-backed planthopper 3.13 Rice delphacid (Tagosodes orizicolus Muir) 3.14 Rice delphacid (Tagosodes cubanus Crawford) 3.15 Spittlebugs (Locris maculata maculata Fabricius) 3.16 Spittlebugs (Deois flavopicta Stål) 3.17 References

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3.1 Introduction The genera occurring in Asia are also present in West Africa, but the species are different. The West African species are similar in appearance to Asian species, but they are of only minor importance. In Asia, their importance has escalated. with the intensification of rice production, especially the use of insecticides. Asian species not only cause direct plant damage, by removing the sap from leaves and stems, but several are also efficient vectors of rice viruses (Heinrichs and Barrion 2004). Recent studies by Koudalimoro et al. (2015) and Nwilene et al. (2009) have shown that Cofana spectra, C. unimaculata and Nephotettix modulatus are vectors of Rice Yellow Mottle Virus (RYMV) in Africa. Leafhoppers attack all aerial parts of the plant, but planthoppers occur primarily on the basal portion of the plant (Dale 1994). Oman (1949) classified the types of damage caused by leafhoppers and planthoppers into four categories: 1) removal of plant sap from the xylem or phloem, 2) damage to plant tissue and deformation of leaves and stems through oviposition, 3) transmission of pathogens and 4) predisposition of the plants to pathogens that penetrate the oviposition and feeding punctures left by the hoppers in plant tissue. In Asia, leafhoppers are a threat to production mainly because of their efficiency in vectoring rice viruses, but generally do not cause severe direct damage by the removal of plant sap. The brown planthopper, Nilaparvata lugens (Stål), however, is a serious pest because it causes direct damage through the removal of large amounts of plant sap, and as a vector of several serious rice viruses (Heinrichs 1979; Cabauatan et al. 2009). In Asia, the sudden increase in the importance of these pests in the 1970s, was attributed to the changes in cultural practices accompanying the intensification of rice production during the Green Revolution. It appears that high levels of nitrogen fertilizer, monocultures, continuous cropping and mainly the application of insecticides that cause hopper resurgence are some of the intensification practices contributing to leafhopper and planthopper outbreaks (Heinrichs and Mochida 1984; Cabauatan et al. 2009). In West Africa, the hoppers are still considered as only potential pests, which should be closely monitored as production practices are intensified. Intensive surveys of the leafhoppers and planthoppers inhabiting West African rice environments are limited to those of Heinrichs and Barrion (2004) in Côte d’Ivoire. Based on the examination of museum specimens, Wilson and Claridge (1991) described the rice leafhoppers and planthoppers occurring on rice in the region south of the Sahara and have developed taxonomic keys for their identification. Wilson and Claridge (1991) list three planthopper species of the Delphacidae family that occur on rice in West Africa, Nilaparvata maeander Fennah, Tagosodes cubanus (Crawford) and Sogatella kolophon (Kirkaldy). The literature and the WARDA Arthropod Reference Collection add Delphacoides aglauros and Sogatella nigeriensis to the list of delphacid species in West Africa. Closely related species attacking rice in Asia are the brown planthopper (BPH), N. lugens (Stål), and the white-backed planthopper (WBPH), Sogatella furcifera (Horvath). Sogatella kolophon is widely distributed in the world, occurring in West Africa, Australia, the Orient, the Atlantic Islands, the Pacific, the Ethiopian region, the New World and the eastern Palearctic. It is most commonly found in the tropics. Tagosodes cubanus also occurs in South and Central America where it is a vector of the hoja blanca virus of rice, which can cause up to 50% yield loss (King and Saunders 1984). The rice delphacid Tagosodes oryzicolus is a serious pest in tropical Central American, Caribbean

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and South American rice-growing countries where it causes direct damage and transmits hoja blanca virus (Morales and Jennings 2010). This insect migrates and has occasionally been found (but not established) as far north as Texas and Louisiana and as far south as Argentina. Nisia nervosa (Motschulsky) is the only member of the Meenoplidae family attacking rice. The preferred host plant appears to be a sedge species (Cyperaceae) (CABI 2016a), but rice is frequently used as a host (Wilson and Claridge 1991). Grist and Lever (1969) mention it as a minor pest of rice and Huang and Qi (1981) have recorded it on rice and sugarcane in China. Locris spp. (Cercopidae) are confined to Africa and can transmit RYMV (Koudamiloro et al. 2015). They are easily recognized by their large size and red, orange or brown colouration and patterning of the forewings and head. Little is known about the biology of Locris spp. Akingbohungbe (1983) records Locris rubens Erichson, L. maculata maculata F. and L. rubra F. as minor pests of cereals in Nigeria. The most common Locris spp. occurring on rice are L. erythromela (Walker), L. maculata maculata, L. rubra and L. rubens (E.A. Akinsola, WARDA, 1992, pers. comm.). They prefer irrigated and lowland rice to upland rice. Severe plant damage caused by Locris spp. is not common, but leaf bronzing and wilting can occur. Wilson and Claridge (1991) list five species of cicadellids in West Africa. Fourteen Cicadellidae species have been reported in the literature. Nephotettix spp. are severe pests of rice in Asia where N. virescens (Distant), N. cincticeps (Uhler) and N. nigropictus (Stål) are vectors of the virus diseases tungro, rice transitory yellowing, rice dwarf virus, rice gall dwarf and yellow dwarf. In West Africa, N. modulatus Melichar and N. afer Ghauri are, so far, of only minor importance, as they are not known to be virus vectors and populations seldom reach levels where feeding injury causes economic damage to rice. Two other cicadellid species, Cofana spectra (Distant) and C. unimaculata (Signoret), occur on rice in West Africa. Both are widely distributed in the Old World tropics from Africa to Australia. Cofana spp. are not known to be virus vectors in any region of the world. There are several cicadellid species of the genus Recilia that are found on rice throughout the world. Of these, the zigzagged leafhopper, R. dorsalis (Motschulsky), is an important rice pest in Asia where it transmits tungro, rice dwarf virus, rice gall dwarf viruses and orange leaf (Wilson and Claridge 1991). Recilia mica Kramer has only been recorded from West Africa (Kramer 1962) where it has been reported on rice (Zakra et al. 1986), but evidence of crop damage has not been reported. Little is known about the biology and ecology of planthoppers and leafhoppers that occur on rice in West Africa. However, the known literature and research conducted at WARDA on Nephotettix, Cofana, Nilaparvata, Nisia and Locris spp. are reported below (Heinrichs and Barrion 2004). The rice leaf- and planthoppers have gained great economic significance in recent years as their infestations very often assume epidemic proportions. Rice leafhoppers (Cicadellidae) and planthoppers (Delphacidae) have become important pests in Asia where, in recent decades, infestations have assumed epidemic proportions coterminous with the Green Revolution.

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3.2 White rice leafhoppers, Cofana spectra (Distant) and C. unimaculata (Signoret) (Hemiptera: Cicadellidae) Distribution: Africa, Australia and Asia. Host plants other than rice: Cyperus rotundus L., Echinochloa colona (L.) Link., Fimbristylis miliacea (L.) Vahl., Saccharum officinarum L., Scirpus articulatus L., Sorghum bicolor (L.) Moench., Zea mays L. Description and biology: Two species of the Cofana genus, C. spectra and C. unimaculata, are common in West African rice fields. Wilson and Claridge (1991) regard only C. spectra to be a pest. Cofana spectra and C. unimaculata are the largest of the leafhoppers occurring on rice in West Africa. They are easily distinguished. Cofana spectra is characterized by a large central black spot on the posterior margin of the head vertex (Fig. 3.1) and has brown lines on the fore wings, which are absent with C. unimaculata (Koudalimoro et al. 2015). Cofana spectra is the largest among the species of leaf- and planthoppers in West Africa. The female measures about 9.5 mm, while the male is shorter, around 7.5 mm in length. Adult longevity recorded in India for males and females is 7 and 10 days, respectively (Sam and Chelliah 1984). Adults rest on the lower surface of the leaves or on tillers at the base of the plant. They are highly attracted to lights at night. During oviposition, the female makes a cut parallel to the long axis of the leaf sheath with its saw-like ovipositor. Eggs are laid in rows of 10 to 15 across the cut, at the base of the plant, above the paddy water. The number of eggs laid per female averages about 50. They hatch in 5 to 12 days (Dale 1994). Studies in India (Singh et al. 1997) indicate that rice variety significantly affects C. spectra biology.

Figure 3.1 Cofana spectra adult (Source: www.hkwildlife.net). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Adults in West Africa appear in transplanted rice fields in May–June and multiply reaching a peak population during October–November (Heinrichs and Barrion 2004). Then the population declines and is very low from December to April. Adults are most abundant at 6 weeks after transplanting. Many overwinter as eggs, though a few adults can also be seen at this time. The overwintering eggs hatch in the period December–January, develop in grass hosts and the resulting adults appear in the period January–February. Another population peak is reached during March. Then the population again declines gradually. Plant damage and ecology: C. spectra is a minor pest of rice rarely occurring at populations causing yield loss (Dale 1994). In recent studies, both Cofana species have been reported as capable of mechanically transmitting RYMV in Benin (Koudalimoro et al. 2014; Koudalimoro et al. 2015). Generally, adults live on the lower surface of the leaves or at the tiller base. Feeding by a large number of nymphs and adults may, however, cause typical sap loss. Leaf tips first dry up and later the leaf turns orange and curls. The pest causes stunting and yellowing of plants, and severe infestations cause plant death (Sam and Chelliah 1984). In Asia, Reissig et al. (1986) reported a threshold of 30 C. spectra hill–1 from tillering to flowering. C. spectra occurs in all rice environments but is most common in rainfed wetland rice at the end of the rainy season. However, C. spectra was reported among the most prevalent insect species in upland rice in Southeastern Nigeria (Emosairue and Usua 1996). Both Cofana species responded to high rates of N fertilizer in WARDA tests (Heinrichs and Barrion 2004). Cofana spectra and C. unimaculata populations in lowland rice at 250 kg N ha−1 were three times those of plots treated with 100 kg N ha−1. The effect on Cofana populations of the length of the fallow period, prior to planting upland rice, was studied in the forest region of Côte d'Ivoire in 1994. Populations of both C. spectra and C. unimaculata were negatively correlated, with the length of fallow periods ranging from 2 to 35 years (Heinrichs and Barrion 2004). Strepsipteran parasitism can regulate Cofana population levels in West Africa. In lowland rice, on the WARDA Mbè Farm in Côte d’Ivoire, C. spectra parasitism by Halictophagus australensis Perkins reached 100% at 65 DT while C. unimaculata peaked at 45% at 75 DT (Oyediran et al. 2000). In a survey conducted in farmers’ fields throughout Côte d'Ivoire, parasitism of C. spectra averaged 21%, while that of C. unimaculata averaged 12% (Heinrichs 1994). In a survey conducted in Guinea, strepsipteran parasitism of Cofana spp. averaged about 18% (Heinrichs and Barrion 2004).

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3.3 Green leafhoppers, Nephotettix spp. (Homoptera: Cicadellidae) Green leafhoppers are important insect pests of rice throughout Asia. They cause either direct damage to the rice crop by sucking the sap and injecting toxic chemicals or indirect harm by transmitting virus diseases. The genus Nephotettix is widely distributed in Asia and Africa. The important Oriental species are N. nigropictus, N. virescens, N. cincticeps, N. malayanus and N. parvus. Their distribution and the virus diseases they transmit are given in Table 3.1. The genus in Africa and Madagascar has been found to be represented by two species – N. modulatus and N. afer (Ghauri 1968). Both are largely symmetric and widely distributed throughout Africa. Recent studies (Koudalimoro et al. 2014; Koudalimoro et al. 2015) have reported N. modulatus as a vector of RYMV in Central Africa. Feeding by green leafhoppers is confined mostly to the leaf and leaf sheath of rice. Mild infestations may reduce the vigour of the plants and the number of productive tillers. Heavy infestations cause withering and complete drying of the crop. Among the diseases transmitted by Nephotettix spp., tungro is the most destructive. The infection occurs primarily in the early stages of crop growth. It is the only known nonpersistent or transitory rice virus (Ling and Tiongco 1979). When the epidemic is severe, 100% yield loss can occur (Heinrichs 1979). Severe epidemics of tungro occurred in Indonesia, Thailand, Malaysia, Bangladesh and India in the 1970s. An epidemic outbreak of tungro in three districts of West Bengal, India during 2001, caused an unmilled rice production loss of 0.5 mt valued at 2911 million rupees (Muralidharan et al. 2003). In the Philippines, the disease has been a serious threat ever since it first appeared as an epidemic in 1957. In general, epidemics of tungro in South and Southeast Asia have declined since the 1960s and 1970s, but it is still a potential threat to rice (Islam and Catling 2012). Nephotettix spp. were known only as minor pests in Bangladesh until 1955 (Alam and Islam 1959). But since then–80% damage has been reported from different regions of the country. The emergence of green leafhoppers into a major pest has been commonly attributed to the introduction of high-yielding rice cultivars and the accompanying high nitrogen applications (Karim and Pathak 1979) and year-round cropping with irrigation (Reissig et al. 1986).

Table 3.1 Distribution of green leafhopper vectors of rice viruses in Asia and Africa (Dale 1994; Sulochana 1984; Koudalimoro et al. 2014, 2015) Leafhopper

Distribution

Virus disease transmitted

N.nigropictus

Africa

Rice dwarf, transitory yellowing, tungro, yellow dwarf, orange leaf

N.virescens

Asia

Tungro, leaf yellowing, transitory yellowing, yellow dwarf, orange leaf

N.cincticeps

Asia

Transitory yellowing, yellow dwarf, rice dwarf

N.malayanus

Asia

Waika, tungro

N.parvus

Asia

Tungro, yellow dwarf

N. modulatus

Africa

Rice yellow mottle virus

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3.4 Nephotettix afer Ghauri and Nephotettix modulatus Melichar (Hemiptera: Cicadellidae) The Nephotettix genus in West Africa is represented by two species, N. afer and N. modulatus (Ghauri 1968). Nephotettix modulatus has also been recognized as N. africanus Emeljanov (Wilson and Claridge 1991). Distribution: N. afer – Africa: Angola, Congo, Côte d’Ivoire, Ethiopia, Guinea, GuineaBissau, Kenya, Madagascar, Nigeria, South Africa, Sudan, Tanzania, Uganda, Zambia. N. modulatus – Africa (Angola, Benin, Congo, Côte d’Ivoire, Ethiopia, Ghana, Guinea, Guinea-Bissau, Kenya, Madagascar, Malawi, Morocco, Liberia, Nigeria, Senegal, Sudan, Tanzania, Togo, Uganda, Zambia, Egypt) and Israel. Nephotettix modulatus is believed to be widely distributed in sub-Saharan Africa, extending southward to Tanzania and Angola, and in North Africa and the Middle East (Ghauri 1971). Nephotettix afer has a more southerly distribution than N. modulatus, having been found in South Africa. In contrast to N. modulatus, N. afer is not found in North Africa or the Middle East (Ghauri 1971). Like N. modulatus, it has been reported in Angola, Ethiopia, Kenya, Madagascar, Sudan, Tanzania, Uganda and Zambia (Dale 1994). In countries where N. modulatus and N. afer both occur, they may be found together in the same rice fields. Host plants other than rice: N. modulatus – Rottboellia cochinchinensis (Loureiro) Clayton, L., Ischaemum rugosum Salisb. and Paspalum vaginatum Swartz. Alghali and Domingo (1982) reported that N. modulatus nymphs were found on R. cochinchinensis and I. rugosum in the mangrove swamps of Mawir, Sierra Leone, when rice was at the heading stage and on P. vaginatum in mangrove swamps at Rokupr, Sierra Leone, when rice was at the vegetative stage. Description and biology: Information regarding the biology of Nephotettix spp. in Africa is lacking. Nephotettix modulatus (Fig. 3.3) being green with black markings on the wings and head is similar in appearance to N. nigropictus (Fig. 3.4), an Asian species, with which it is often confused. Nephotettix afer (Fig. 3.2) differs from N. modulatus (Fig. 3.3) in that it has a distinct, complete submarginal black band on the vertex of the head, while in N. modulatus, the black band is separated or reduced in the middle (Wilson and Claridge 1991). Also, N. modulatus is lighter in colour than that of N. afer, is slightly larger and its ovipositor is longer; the dorsal setae of male pygofers are longer (Dale 1994). The colour pattern of N. afer is more similar to that of N. nigropictus than to that of N. modulatus. Three transverse marginal and submarginal black bands on the vertex are well developed. Eggs are deposited in groups of 10–25 in slits made by the ovipositor in leaf sheaths of growing rice plants. The incubation period is 4–10 d. Nymphs, upon hatching, suck the sap from leaves. High mortality occurs in the nymphal stage because of the predatory activity of spiders (Heinrichs and Barrion 2004). Nephotettix spp. are present in irrigated rice at WARDA throughout the year (Oyediran and Heinrichs 1999). Populations in monthly plantings were lowest in plots transplanted during the dry season and harmattan period, December to January. Length of the fallow period, prior to the sowing of upland rice, has an effect on leafhopper populations. Studies conducted in the forest region of Côte d’Ivoire indicated that leafhopper populations in rice, planted after a fallow period, increase as the length of the fallow period increases (Heinrichs et al. 1993). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 3.2 Nephotettix afer adult (Source: IRRI).

Figure 3.3 Nephotettix modulatus adult (Source: IRRI).

Plant damage and ecology: Both the nymphs and the adults of Nephotettix afer and N. modulatus suck sap from the leaves and leaf sheaths. Low infestation levels may reduce vigour of the plant and the number of productive tillers. High infestation levels, which are not common, cause withering and complete drying of the crop. N. modulatus has recently been identified as a vector of RYMV in Central Africa (Koudalimoro et al. 2014; Koudalimoro et al. 2015).

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3.5 Nephotettix nigropictus (Stål) (Hemiptera: Cicadellidae) Distribution: Africa – Cameroon; Asia – Bangladesh, Bhutan, Cambodia, China, India, Indonesia, Japan, Korea, Laos, Malaysia, Myanmar, Nepal, Pakistan, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam; Oceania – Australia, Guam, Micronesia, Palau, Papua New Guinea (CABI 2016b; Dale 1994; Reissig et al. 1986). Host plants other than rice: Cyperus, Cynodon dactylon (L.), Echinochloa colona (L.) Link, Echinochloa crus-galli (L.) Beauv., Eleusine indica (L.) Gaertn., Ischaemum indicum (Houtt.) Merr., Leersia hexandra Sw., Panicum (millets), Panicum repens L., Paspalum scrobiculatum L., Saccharum officinarum L., wild rices, Zea mays L. (CABI 2016b; Dale 1994; Reissig et al. 1986). Description and biology: N. nigropictus (Fig. 3.4) is distinguished from N. virescens (Fig. 3.6) by the rounded vertex, and an anterior black band extending beyond the ocelli to the inner margins of the eyes (Islam and Catling 2012). The adult is green, the male possessing a median black wedge-shaped mark on the forewings (Reissig et al. 1986). In the female, this area is brown in colour. Both nymphs and adults are very active in summer, especially on hot sunny days. With the onset of cold weather, they become somewhat sluggish.

Figure 3.4 Nephotettix nigropictus adult (Source: Centre for Invasive Species and Ecosystem Health, University of Georgia, USA (https://www.bugwood.org/); photo taken by Natasha Wright, Cook’s Pest Control, USA). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The pre-mating period ranges between 3 and 5 days after the final moult. Females start laying eggs 1–3 days after mating and prefer to oviposit in the basal portions of leaf sheaths of young rice seedlings. The eggs are laid in batches of 10–15 into the epidermis and cortex and sometimes in the air cavities of the leaf sheath with the saw-like ovipositor (Islam and Catling 2012). They are arranged in a single row, along the length of the leaf sheath. Most eggs are laid during the afternoon hours (Dhawan and Sajjan 1976). The ovipositional sites can be seen as slightly bulged portions and are lighter green in colour. The number of eggs laid starts declining with age after the second week of mating. In India, the average adult longevities for males and females are 56–62 days, respectively, during the months of June to October. But longevity is extended during the winter months (Misra 1980). Eggs are somewhat crescent-shaped, pale yellow and measure 1 × 0.3 mm. Reddish eye spots are visible just before hatching. The incubation period varies from 8 to 14 days depending on the temperature. Nymphs are creamy white at first and later turn green. The colour darkens as the nymphs pass through five successive moults. The nymphal period is 2–3 weeks in summer and longer in winter. Nasu (1967) observed a longer nymphal period in the case of females than in males. Nymphal survival was found higher on the weed Leersia sp. than on rice cultivars (Razzaque 1984). Seasonal occurrence is based on studies conducted in India (Misra 1980). The leafhoppers start appearing in the rice fields in August. They multiply and reach a peak population during October–November. Then, the population declines drastically, mainly because of the fall in temperature. After rice harvest, surviving adults live on grasses found near irrigation canals and levees. The ratoon and self-sown rice also harbour the pest. During the period December–January, the hoppers migrate from grasses to rice nurseries, and then from February to March, to the transplanted rice crop. A rise in population takes place during this time, even though the number is comparatively smaller than that from October to November. Again, at harvest, the hoppers move on to grasses during summer for feeding and egg laying. The adults emerging from these grasses migrate to the rice fields during late July or early August. Plant damage and ecology: Feeding by N. nigropictus is similar to that of other Nephotettix spp. in that both the nymphs and the adults suck sap from the leaves and leaf sheaths of rice plants. Low infestation levels may reduce vigour of the plant and the number of productive tillers. High infestation levels, which are not common, cause withering and complete drying of the crop. N. nigropictus transmits the viruses rice dwarf, transitory yellowing, tungro, yellow dwarf and orange leaf (Dale 1994).

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3.6 Nephotettix cincticeps (Uhler) (Hemiptera: Cicadellidae) Distribution: Asia – China, India, Indonesia, Japan, DPR Korea, Republic of Korea, Laos, Malaysia, Myanmar, Pakistan, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam; Europe – Russian Federation-Far East (CABI 2016c) Host plants other than rice: Alopecurus aequalis Sobol, Avena fatua L., Echinochloa frumentacea Link, Leersia japonica (Honda) Honda, Phalaris arundinacea L., Phragmites australis (Cav.) Trin. ex Steud., Poa annua L. Description and biology: Wilson and Claridge (1991) and CABI (2016c) provide a description of N. cincticeps. Nymphs are pale-green/yellow with small spines on the dorsal surface of abdominal segments, with small, dark-brown or black markings on the dorsal surface. The length of the male adult is 4.30–4.50 mm and that of the female is 5.00–5.60 mm. Males have head with a black submarginal band between the eyes. Some males have black markings adjacent to ocelli. Forewing of male has a distinct spot that does not touch the claval suture, but this spot may be absent or only partially represented. Apical third of tegmen is black in males (Fig. 3.5). Females have unmarked head, pronotum and clavus. Females are similar in colouration to many N. nigropictus females where the submarginal band of the vertex often does not touch the inner margins of the eyes and the forewings are without dark markings.

Figure 3.5 Nephotettix cincticeps adult (Source: Natural History Museum of Wales, UK). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Life history and habits are similar to those given for N. nigropictus, but there are differences in the seasonal occurrence caused primarily due to the ecological differences in the pest habitats (Dale 1994). N. cincticeps is a more northerly distributed species in Asia than any other Nephotettix species. The following description is based on the study of Hirao and Inoue (1978) conducted in Japan. N. cincticeps passes the winter as a half-grown, mostly fourth instar, diapausing nymph. During the off-season of rice cultivation, a winter grass, water foxtail Alopecurus aequalis, serves as the main host plant. This grass is widely seen in fallow fields after rice harvest. Adults migrate from the wild host vegetation to paddy fields in early summer immediately after transplanting. Afterwards, the hoppers spend three generations in paddy fields. The adult emergence of the last generation is interrupted by the nymphal diapause induced by short day length of autumn. There are four generations of the pest in most regions of Japan. However, there may be a fifth or even a partial sixth generation in the warmer southern parts of Kyushu. Plant damage and ecology: N. cincticeps attack all plant growth stages from seedling to flowering (CABI 2015c). Direct damage to rice plants is similar to that described for other Nephotettix species. Feeding symptoms are honeydew and sooty mould on the leaves. Severe damage results in yellowing and dead plants. N. cincticeps transmits transitory yellowing, yellow dwarf and rice dwarf viruses (Reissig et al. 1986). It is the only species related to the incidence of the yellow dwarf disease in Japan. Yield losses as high as 75% have been reported due to this disease (Hirao and Inoue 1978). In Japan, a positive relationship exists between low populations of N. cincticeps and heavy snowfall, although this factor is not the only one in checking pest outbreaks (Otake 1966).There is also a long list of parasites, predators and pathogens that check N. cincticeps populations (CABI 2016c).

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3.7 Nephotettix virescens (Distant) (Hemiptera: Cicadellidae) Distribution: Azerbaijan, Bangladesh, Brunei, Cambodia, China, India, Indonesia, Japan, Laos, Malaysia, Myanmar, Philippines, Sri Lanka, Taiwan, Thailand, Taiwan, Vietnam (CABI 2016d; Dale 1994; Reissig et al. 1986). Host plants other than rice: Cynodon dactylon (L.) Pers., Echinochloa crus-galli (L.) Beauv., Eleusine indica (L.) Gaertn., Leersia hexandra Sw., Panicum ramosum L., Saccharum officinarum L., wild rices, Zea mays L. (Dale 1994). Description and biology: The N. virescens adults are highly mobile and fly when disturbed and are strongly attracted to light (Islam and Catling 2012). Nymphs are pale green/yellow with small spines on the dorsal surface of abdominal segments and with small, dark brown or black markings on the dorsal surface (CABI 2016d).The newly emerged adult is yellowish in colour. It gradually turns yellowish green and then green in about 3 hours after emergence. Most of the adults emerge early in the morning (Dale 1994). The forewing has a distinct spot that does not touch the claval suture (Fig. 3.6), but this spot may be absent or only partially represented (CABI (2016d). The adult green leafhopper is about 4 mm long. It has a pointed vertex and a green head. Males have green forewings with a small dark brown or black band in the middle, while in females there is no such band. The head, pronotum and scutellum are usually green, but some males have black markings adjacent to ocelli.

Figure 3.6 Nephotettix virescens adult (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The pre-mating period ranges from 1 to 2 days. Eggs are laid in small slits made in the soft parts of the leaf sheath. The number of eggs in a batch seldom exceeds 30 and the total eggs laid during the life cycle is around 350. Unmated females lay sterile eggs randomly on the leaf sheaths, while mated females lay fertile eggs which are inserted in the leaf sheath in an arranged manner. Young leaves are preferred for oviposition (Islam and Catling 2012). Newly laid eggs are barely visible and are oblong, bent and pale yellow. The incubation period varies from 6 to 12 days (Dale 1994). Young nymphs are creamy white with black longitudinal stripes on the sides of the body. They turn yellow or yellowish green in about an hour after moulting. First instar nymphs are more numerous on the lower surface of older leaf blades, but from the second instar onwards, they distribute themselves rather evenly on all leaves. Nymphs and adults suck sap from leaf sheaths and blades (Dale 1994). The rate of nymphal development is faster at higher temperatures. Cheng and Pathak (1971) reported that the average larval duration was only 14.1 days at 35°C, while it was 37.3 days at 20°C. The male nymphal period is usually shorter than that of females. Rice plants at the tillering and panicle initiation stages are most favourable for the rapid build-up of pest populations. The nymphal stage is greatly prolonged during winter. The insect can withstand long periods of starvation (Basu et al. 1976). Ho and Chen (1968) observed 8 generations of the pest in Taiwan, whereas in India, occurrence of up to 11 generations has been recorded. Throughout India, the population of N. virescens is higher than that of N. nigropictus (Mathur and Chaturvedi 1980). Leafhoppers move from one rice crop to another and during the intervening periods they feed and breed on grasses found in the rice ecosystem. There are two population peaks in a year – one in March during the first crop season (February to May/June) and another from October to November during the second crop (June to December). Plant damage and ecology: N. virescens is more specific to rice than N. nigropictus (Islam and Catling 2012). N. virescens causes direct damage to rice plants by sucking the sap and plugging vascular bundles with their stylet sheaths. Although N. virescens is the most abundant green leafhopper in irrigated rice ecosystems, their populations are rarely sufficiently high to cause significant yield loss through direct feeding and hopperburn is rare. N. virescens is a major pest because they transmit several viruses, that is, tungro, leaf yellowing, transitory yellowing, yellow dwarf and orange leaf (Dale 1994). Both nymphs and adults transmit viruses and N. virescens is a more efficient transmission agent than N. nigropictus (Islam and Catling 2012). The most important virus is tungro, which causes severe yield losses. Infected plants are stunted and have deformed leaves, increased tillering, gall formation and yellowing. It is a dangerous disease because it can cause total loss of the crop and there are no effective control measures once the plants are infected. Irrigated areas are at most risk, but tungro may also occur in rainfed lowland rice and often in ratoons (Islam and Catling 2012). The optimum temperature for the development of green leafhoppers ranges between 25 and 30°C. Insects exposed to higher temperatures lay less eggs, some of which may not hatch. The high incidence of Nephotettix spp. is attributed to favourable temperature, low rainfall and good sunshine. In Vietnam, it was reported that during a year when there is little rain with low temperature and high humidity, there will be a heavy incidence of green leafhopper (Quyen 1963). Similar conditions lead to sudden N. virescens outbreaks in India (Ghosh et al. 1960).

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3.8 Nephotettix malayanus Ishihara et Kawase (Hemiptera: Cicadellidae) Distribution: Australia (N and SE Queensland), China, India, Indonesia, Japan, Malaysia, Myanmar, Nepal, Philippines, Sri Lanka, Taiwan, Thailand. Host plants other than rice: Echinochloa spp., Leersia hexandra Sw. Description and biology: N. malayanus adults (Fig. 3.7) are mostly greenish, although the head is tinted with yellow (Dale 1994). It is smaller in size than the closely allied species N. cincticeps. Body lengths, including tegmina, of the male and female are 3.8–4.6 mm and 4.3–5.0 mm, respectively. The absence of a transverse black band across the vertex and the lack of the black mark in the centre of the tegmen differentiate this species from N. nigropictus, and the presence of short black marks behind the ocelli and the relatively shorter vertex differentiates it from N. virescens. Adults usually emerge in the morning. Eggs, which are deposited in leaf sheaths, hatch in 7–10 days. The newly hatched nymphs remain on the leaf sheath for about an hour and then disperse to the leaf blades. There are five nymphal instars. The nymphal period varies from 13 to 19 days. The effect of temperature on the development of N. malayanus on L. hexandra was studied by Kim (1985). He found that, at 25°C, the incubation period of the eggs was 10.2

Figure 3.7 Nephotettix malayanus adult female (Source: Natural History Museum of Wales, UK). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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days, while at 33°C, it decreased to 7.1 days. Similarly, the lifespan of the adult hoppers was longest (23.3 days) at 25°C, while it was only 17.3 days at 33°C. Plant damage and ecology: This is one of the two Malayan species of the genus Nephotettix reported by Ishihara and Kawase (1968). N. malayanus is less of a threat to rice cultivation than the other green leafhoppers because a weed, Leersia hexandra, is the most preferred host plant. Nephotettix malayanus is common in both rainfed and irrigated wetland environments. They are not prevalent in upland rice. Similar to other Nephotettix species the nymphs and adults suck the sap of the leaves and the tillers. They prefer to feed on the lateral leaves rather than the leaf sheaths and the middle leaves. Both the nymphs and adults feed on the dorsal surface of the leaf blades rather than the ventral surface. They also prefer rice plants that have been heavily fertilized with nitrogen. Staggered planting encourages population growth of N. malayanus. Affected plants are stunted with deformed leaves and a decreased number of productive tillers. Plants wither, stop growing and dry completely (IRRI http://www.knowledgebank. irri.org). Damaged plants show yellowing or browning of leaves (Pan Germany http:// www.oisat.org/pests/insect_pests/hoppers/glh/general_information.html). N. malayanus is the vector of two virus diseases of rice, waika and tungro. Both adults and nymphs of N. malayanus transmit rice waika virus and transmission efficiency is higher than that of N. cincticeps. But, in the case of tungro, transmission efficiency is generally lower with N. malayanus than with N. virescens (Kim 1985).

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3.9 Zigzag leafhopper, Recilia dorsalis (Motschulsky) (Homoptera: Cicadellidae) Distribution: Australia, Bangladesh, Bhutan, Brunei Darussalam, Cambodia, China, India, Indonesia, Japan, Korea DPR, Korea ROK, Laos, Malaysia, Myanmar, Pakistan, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam (Reissig et al. 1986). Host plants other than rice: Cynodon dactylon (L.) Pers., Cyperus rotundus L., Echinochloa colona (L.) Link., Hordeum vulgare L., Leersia hexandra Sw., Saccharum officinarum L., Triticum aestivum L. (Reissig et al. 1986; CABI 2016e). Description and biology: The adult (Fig. 3.8) is readily identified by the characteristic zigzag (W-shaped) white and brown pattern on the forewings (Islam and Catling 2012). Body length is 3.5–4.0 mm. The pre-mating period, after the final moult, ranges from 2 to 4 days. The white eggs are laid individually in rows within the leaf sheaths (Reissig et al. 1986). The average number of eggs laid per female is 98 (Misra 1980) and eggs hatch in 7–9 days. To lay eggs, the female cuts openings in leaf sheaths with her saw-like ovipositor. The ovipositional sites can be located, with difficulty, as small brownish spots; sometimes micropylar ends of eggs protrude from the leaf surface. There are five nymphal stages lasting for 16 days. The nymphs are yellowish brown in colour varying from 1.0 to 3.0 mm in body length. They are found on leaves in the upper parts of the rice plant and also on tillers near the base (Reissig et al. 1986). The adult

Figure 3.8 Recilia dorsalis adult (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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hoppers live for 10–14 days. R. dorsalis in southern Japan has four generations in a year and hibernates in the egg stage (Dale 1994). Plant damage and ecology: R. dorsalis is present in all rice environments and in Bangladesh it is most abundant during the early rainy season in the early crop growth stages (Islam and Catling 2012). It is considered a minor pest of rice and causes little damage by direct feeding but does transmit rice dwarf, orange leaf and tungro viruses to wetland rice in many parts of Asia. Only the female is viruliferous. Adults are highly mobile and enter rice fields in the early crop growth stages. Both nymphs and adults suck sap from the leaves and leaf sheaths. Leaf tips dry and leaf margins become orange in colour. Later, the entire leaf turns orange and the margins curl. Damage first appears on the older leaves. Young seedlings wilt and die when R. dorsalis is abundant. However, it usually occurs in low population densities and seldom causes significant damage to the rice crop by removal of plant sap. It occurs in all rice environments but transmits virus diseases only to wetland rice. In India, the adults make their first appearance during the rainy season, June–July, in the rice nurseries and newly planted fields. Their number gradually increases to reach a peak during the period August–September. The population then gradually declines in the October–November period. At that time some adults are still found on the plant leaves of paddy fields. These overwintering adults again appear between December and January in the seedbed of the first crop. In the newly transplanted crop, they multiply rapidly and reach a peak during the February–March period. Then the population starts declining.

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3.10 Smaller brown planthopper, Laodelphax striatellus (Fallen) (Homoptera: Delphacidae) Distribution: Asia, Africa, Europe, Oceania (CABI 2016f). Host plants other than rice: Wheat, barley, oats and various other grasses (Poaceae) (CABI 2016f). Description and biology: The description and biology were reported by Dale (1994). Adults have two wing forms: brachypterous (Fig. 3.9) and macropterous (Fig. 3.10). The adult males are usually 3.5 mm long, while the females are smaller, about 2.0 mm long. Sometimes the insects have red eyes. The female lays 60–260 white eggs in masses in the leaf midrib or leaf sheath near the base of the plant. The eggs hatch in 5–15 days. The nymphs are light to dark brown and are usually smaller than those of the other species at corresponding instars. There are five nymphal stages lasting . At a temperature of 25°C, the nymphal period is about two weeks. The hoppers congregate on the lower portions of the plant just above the water level in irrigated fields, and in the interior of the clustered bases of the tillers, strongly suggesting that the insects prefer humid conditions. Close planting and weedy rice fields favour the incidence of the pest.

Figure 3.9  Laodelphax striatellus brachypterous adult (Source: Jean-Laurent Hentz; www.nature dugard.org). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 3.10 Laodelphax striatellus macropterous adult (Source: not known).

There are six to seven generations in a year. In Japan, this species hibernates as last instar nymphs in winter wheat. The emerging adults then move into the transplanted rice in late May and early June. Usually 5% of these hoppers carry stripe virus. By July–August, they infest the second rice crop. The smaller BPH harbours yeast-like symbiotes in the fat body, which are transmitted to the next generation through eggs (Noda 1977). High temperature (35°C) destroys the symbiotes and leads to a poor growth of the host insects (Noda and Saito 1979). Plant damage and ecology: Although the nymphs and adults suck plant sap, feeding damage rarely causes yield losses. Laodelphax striatellus is important as a vector of rice stripe and black-streaked dwarf virus in China and Japan (Anon. 1976). Once it has acquired the virus it remains a vector throughout its life. Rice stripe virus disease can cause high yield losses when severe epidemics occur. The virus is transmitted in a persistent, circulative-propagative manner, mainly by L. striatellus. In Japan, it is also transmitted by three other planthopper species, Unkanodes sapporona (Matsumura), U. albifascia (Matsumura) and Terthron albovittatum (Matsumura). Rice stripe virus disease occurs in the temperate regions of East Asia, specifically China, Japan, Korea and Taiwan. It has also been reported in far-eastern Russia.

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3.11 Brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae) There are two major planthoppers in Asian rice production: the brown planthopper (BPH) N. lugens and the whitebacked planthopper (WBPH) Sogatella furcifera. The BPH is one of the most damaging insect pests in Asian rice because it not only reproduces and multiplies rapidly, causing plant damage known as ‘hopperburn’, but also is an efficient vector of rice grassy stunt (RGSV) and ragged stunt (RRSV) viruses (Cabauatan et al. 2009). A minor pest in tropical Asia until the mid-1960s, it assumed major pest status in the 1970s when it caused severe losses in many Asian countries. Then, after keeping a low profile for a decade or so, the BPH again re-emerged as a major threat to rice in Asia, especially China, Thailand, Vietnam and Indonesia (Islam and Catling 2012). Distribution: Asia – Bangladesh, Bhutan, Brunei Darussalam, Cambodia, China, Fiji, India, Indonesia, Japan, Korea DPR, Korea ROK, Laos, Malaysia, Nepal, Pakistan, Philippines, Singapore, Sri Lanka, Taiwan, Thailand, Vietnam; Oceania – Australia, Fiji, Guam, Micronesia, New Caledonia, Northern Mariana Islands, Palau, Papua New Guinea, Solomon Islands (Dale 1994; CABI 2016g; Reissig et al. 1986). Host plants other than rice: Arthraxon hispidus (Thunb.), Brachiaria mutica (Forssk.) Stapf, Digitaria ciliaris (Retz.) Koeler, Echinochloa crus-galli (L.), Isachne globosa (Thunb.)

Figure 3.11 Nilaparvata lugens adult (Source: Slvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Kuntze, Leersia hexandra Sw., Leersia japonica (Makino ex Honda) Honda, Poa annua L., Saccharum officinarum L., Zizania latifolia (Griseb.) Turcz. ex Stapf (Islam and Catling 2012). Description and biology: Adult emergence takes place at the basal part of the host plant. It begins at dawn and continues for 4–5 hours. The adult planthoppers are ochraceous brown dorsally and brown ventrally (Fig. 3.11). The tegmina are subhyaline with a dull yellowish tint. The female measures about 5 mm and the male 4.5 mm in length. The adults are dimorphic, with fully winged ‘macropterous’ and truncate-winged ‘brachypterous’ forms. The macropters are potentially migrants and are responsible for colonizing new fields. At the time of colonization, the macropterous forms dominate in a rice field both under temperate (Kisimoto 1956, 1965; Kusakabe 1979) and tropical conditions (Dyck et al. 1979). Adults usually mate on the day of emergence and the female starts laying eggs from the day following mating. Brachypterous females lay 300 to 350 eggs, while macropters lay less eggs. The eggs are thrust in a straight line generally along the mid-region of the leaf sheath, although sometimes eggs are laid on the leaf midribs (Fig. 3.12). Eggs are covered with a dome-shaped egg plug secreted by the female. Only the tips of eggs protrude from the plant surface. The egg-laying sites appear as brownish streaks. The number of eggs laid at a site has been reported to vary in different countries – 2–3 in Japan, 4–10 in the Philippines and 2–12 in India. The egg is banana-shaped, about 1.0 X 0.2 mm, constricted towards the egg caps, whitish brown when freshly laid, darkening with age and developing two distinct red eyespots before hatching. Eggs hatch in about 6–9 days (Islam and Catling 2012).

Figure 3.12 Nilaparvata lugens egg mass (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The newly hatched nymph 0.9 X 0.37 is cottony white at first and turns purple brown within an hour. The fully developed nymph is 3.0 X 1.25 mm with a prominent median line from base of vertex to the end of metathorax where it is widest. Feeding on the plant sap, it undergoes five instars to become an adult. The nymphal period varies widely depending on the food conditions, density during development and other environmental factors. In the tropics, it takes about 10–18 days from hatching until the first instar nymph reaches adulthood (Islam and Catling 2012). N. lugens can have several generations during one cropping season on irrigated rice in the Asian tropics depending on the length of the cropping period. It has 5 generations on one rice crop in southern Japan (Mochida 1964), 5–6 in central China (Lei and Wang 1958) and 4–6 in Indonesia (Mochida et al. 1977). There are usually three generations on the modern high-yielding intermediate duration varieties in the tropics (Heinrichs et al. 1986). Plant damage and ecology: The BPH is a serious insect pest of rice, especially in tropical Asia, where rice crops are continuously cultivated throughout the year (Dyck and Thomas 1979). The insect prefers rainfed and irrigated wetland fields to upland rice and directsown fields to transplanted fields. It is known to primarily feed on rice and on the weed Leersia hexandra (Heinrichs and Medrano 1984). It infests the rice crop at all stages of plant growth. Both BPH nymphs and adults damage rice plants through their extensive feeding and transmission of rice viruses (Cabauatan et al. 2009). N. lugens is a phloemfeeding insect. Removal of nutrients from the plant sap reduces the net photosynthate available to the plant for sustenance and storage. The BPH secretes a solid feeding sheath into the phloem tissues blocking the flow of plant sap while their feeding and ovipositional sites expose the plants to fungal and bacterial infection. The honeydew

Figure 3.13 Hopperburn caused by Nilaparvata lugens feeding (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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excreted by the nymphs and adults at the base of the plants is covered with sooty mould. At early infestation, round yellow patches appear in the field, which soon turn brownish because of the drying of the plants. This condition is called ‘hopperburn’ (Fig. 3.13). Then, the patches of infestation may spread out and cover the entire field (Islam and Catling 2012). Hopperburn does not usually appear until the crop reaches the milk or dough stages. The BPH transmits the viruses such as Rice Ragged Stunt Virus (RRSV) and Rice Grassy Stunt Virus (RGSV) (Hibino 1979, 1989, 1996; Cabauatan et al. 2009). Thus, increased levels of BPH occasionally accompany substantial losses of rice crops due to the virus diseases. From 2005 to 2006, more than 485,000 ha of rice production area in Southern Vietnam were severely affected by viral diseases, seemingly spread by the BPH, resulting in the loss of k828,000 tons of rice valued at US$120 million (Du et al. 2007). The rice virus disease widely observed in Southern Vietnam is called ‘yellowing syndrome’, derived from the characteristic symptom of leaf yellowing. Rice yellowing syndrome was found associated with infection by RGSV or co-infection of RGSV with RRSV, both transmitted by the BPH (Du et al. 2007). N. lugens is a long-range migrant. They make wind-assisted migratory flights every year to colonize the summer rice-growing areas of China. By capture of marked hoppers, it is found that the insects migrate to 200 to 300 km in mainland China (Tu 1979). The hoppers are carried to Korea and Japan by prevailing winds from permanent breeding grounds in southern China. Influxes of the BPH occur from late June to mid-July every year, coinciding with the arrival of low-pressure fronts from the south. In the tropics, migrations also occur. Saxena and Justo (1984) collected hopper adults in two successive inter-island voyages, indicating that migrant planthoppers are reaching the Philippine archipelago from certain rice-growing areas lying to the southwest of the Philippines in the Indian Ocean. The inflowing warm and humid air currents facilitate this migration. Observations indicate that the BPHs take off at dusk and that some are capable of continuously flying up to 26h if the temperature is more than 17°C (Rosenberg and Magor 1983). Others may fly for shorter durations, giving the transient population a chance of dispersal and colonization of rice plants on the way. Several biotypes of N. lugens are known to occur throughout tropical Asia. Temporal change of the biotypes of various N. lugens populations indicated that the populations in Asia are grouped into three: the East Asian, Southeast Asian and South Asian (Sogawa 1992). These populations have shown different insecticide susceptibility properties (Nagata 2002), as well as differential feeding on resistant varieties (Sogawa 1992). The populations are distinguishable by their differential virulence, honeydew production and ability to survive on various rice varieties. The susceptibility of IR26 in India, the first BPH-resistant variety released by IRRI, signalled the evolution of biotypes among hopper populations. Breeding for resistance to the BPH and the subsequent commercial release of numerous rice cultivars with genetic resistance to the BPH has not provided a panacea for managing this pest because of the selection for biotypes that are capable of surviving on these cultivars (Pathak and Khush 1979; Claridge and den Hollander 1980). The seasonal prevalence of the pest is mostly dependent on the availability of host plants. In India, in most regions, the peak population is observed during the late rainy season from October to November. Another peak appears during the dry season from April to May in the regions where double cropping is widely practised. In Japan and Korea, © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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macropterous adults immigrate into rice fields from late June to early July every year. Afterwards, the pest spends several generations on rice and moves or dies at the end of the cropping season. Temperature is a critical factor in the life activities of the BPH. The threshold temperatures of embryonic and post-embryonic development of the BPH are 10.8 and 9.8°C, respectively (Suenaga 1963). The hatchability and survival rate are the highest around 25°C. Eggs are very sensitive to desiccation and soon shrivel when the host plant starts wilting (Kisimoto 1977). The temperature conditions in the nymphal stage affect the longevity and oviposition of adult hoppers (Mochida 1964). The population growth of N. lugens is maximum at a temperature range of 28 to 30°C in the daytime and slightly lower at night. In warm and humid climates, the planthoppers remain active throughout the year and their population fluctuates according to the availability of host plants, activity of natural enemies and other environmental factors prevailing in the locality. Many factors have been attributed to the rapid development and widespread outbreaks of BPH populations in Asia. N. lugens is considered a secondary pest which is often induced by the prophylactic use of insecticides that destroy basic ecosystem services that control them (Heong and Schoenly 1998, Gallagher et al. 1994). In fact, insecticides have been suggested as the major factor involved in population explosions (Heinrichs and Medrano 1985, Shepard et al. 1995). The promiscuous use of insecticides has been shown to promote resurgence of the BPH (Heinrichs and Mochida 1984) due to the poor control, destruction of the natural enemies that play a key role in suppressing BPH populations (Kenmore et al. 1984) and reproductive stimulation of the hopper at sub-lethal insecticide rates (Heinrichs and Mochida 1984). In addition, increased fertilizer use in Green Revolution crops has been suggested to benefit BPH population growth. Laboratory studies of Sogawa (1971) have shown that the hoppers prefer and feed more on plants receiving high nitrogen rates. This leads to faster insect development and higher fecundity. These findings were confirmed in the work of Heinrichs and Medrano (1985) where results clearly showed that insect weight, feeding rate and population growth increased with the application of N fertilizer. In addition, observations from the Philippines (IRRI 1979), Indonesia (Mochida et al. 1979) and Taiwan (Cheng 1977) all concur that intensification of rice production through continuous irrigation favours BPH outbreaks.

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3.12 White-backed planthopper, Sogatella furcifera (Horvath) (Homoptera: Delphacide) The WBPH and the BPH are biologically similar and have an almost identical ecological niche, both species attaining major pest status with the intensive cultivation of shortstatured, nitrogen-responsive, high-yielding varieties and the environmental changes associated with modern rice culture (Islam and Catling 2012). Similar to the BPH, the WBPH are also known to migrate across mainland China (Wang et al. 1982) and from China to Japan and Korea (Mochida et al. 1982). Saxena and Justo (1984) collected airborne hoppers in traps set aboard inter-island vessels sailing in the Philippine archipelago. Several other Sogatella spp. are of minor importance in Asian rice fields (Reissig et al. 1984). Distribution: Asia – Afghanistan, Bangladesh, Bhutan, Cambodia, China, India, Indonesia, Japan, Korea DPR, Korea ROK, Laos, Malaysia, Mongolia, Myanmar, Nepal, Pakistan, Papua New Guinea, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam; Oceania – Australia, Fiji, Marshall Islands, Micronesia, New Caledonia, Northern Mariana Islands, Palau, Solomon Islands, Vanuatu (Reissig et al. 1986, CABI 2017a). Host plants other than rice: Digitaria, Echinochloa, Eleusine, Poa (many grass species), Oryza (wild rice species), Sorghum bicolor (L.) Moench., Triticum aestivum L., Zea mays L. (Reissig et al. 1986; Dale 1994).

Figure 3.14 Sogatella furcifera macropterous and brachypterous adults (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Description and biology: Adult forewings are almost uniformly subhyaline with dark veins. There is a prominent white band between the junctures of the wings. The body is creamy white with the mesonotum and abdomen black dorsally and the legs, ochraceous brown. There is a conspicuous black dot at the middle of the posterior margin of each forewing, which meets when the forewings come together. A medial white band passes along the thorax between wing bases (hence ‘white back’) set off by dark brown outer sides (Islam and Catling 2012). A prominent movable spur is present on hind tibia. The adult hopper is 3.5–4.0 mm long. Macropterous males and females and brachypterous females (Fig. 3.14) are commonly found in the rice crop, whereas brachypterous males are very rare. The planthoppers, especially adults, prefer to stay at the upper portion of rice stems. The preoviposition period ranges between 3 and 8 days. Eggs are laid in longitudinal rows within the leaf midribs (Fig. 3.15). On an average, a female hopper laid 164 eggs in tests in India (Vaidya and Kalode 1981). But in Japan, Suenaga (1963) noted that the total number of eggs laid per female ranged between 300 and 350. Eggs are similar in size (0.9mm long), colour (creamy white) and shape (bananashaped) to those of the BPH but have a longer, more pointed, egg plug. The eggs hatch in about 6 days. Neonate nymphs are whitish yellow, 0.8 mm long, with pink to reddish eyes. The fully developed nymph is 2.1 mm long, greyish in colour; thorax with white markings; distinctive white band in older nymphs; conspicuous black and white spots on abdomen. They reach adulthood in 12 to 17 days passing through five instars.

Figure 3.15 Sogatella furcifera eggs (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: Sogatella furcifera has a long history as an insect pest of rice. It was first reported from Japan in 1899 and from India in 1903 (Chaudhary et al. 1968). The WBPH has emerged as a major pest of rice in many Asian countries where it has destroyed sizeable proportions of the crop in certain years. It occurs in both upland and wetland rice environments. Long-winged adults enter the field at about 30 days after sowing and usually complete fewer generations on a crop than does the BPH. The WBPH prefers a young crop and often produces long-winged migratory forms before the plants flower. Both adults and nymphs suck sap primarily at the base of the rice plants, which leads to yellowing of the lower leaves, reduced vigour and stunting of plants. The attacked plants later acquire a rust red appearance, spreading from the leaf tips to the rest of the plants (Dale 1994). S. furcifera can become sufficiently numerous to kill the plants by hopperburn: the tillers dry up and turn brown as a result of excessive removal of plant sap (Reissig et al. 1986). Because seedlings are attacked in the nursery, infestation is often carried through eggs into the transplanted crop. Severely attacked seedlings do not grow, are stunted, wilt and eventually die. If the infestation is at the panicle initiation stage, the number of grains and the panicle length decrease. But when attacked later, during the maturation period, grains do not fill fully and ripening is delayed. When the hoppers are present in large numbers late in the crop growth stage, they are seen infesting the flag leaves and panicles. Gravid females cause additional damage by making oviposition punctures in leaf sheaths. Feeding points and wounds caused by egg laying may later become potential sites for the invasion of bacteria and fungi. Moreover, the honeydew produced by the hoppers serves as a medium for mould growth. The WBPH is only known to transmit one rice virus. A new virus disease transmitted by the WBPH called Southern Rice Black Streak Dwarf Virus (Wang et al. 2014), originally discovered in China in 2005 and endemic to most of China’s southern provinces, has spread northward in China and southwards to the Red River Delta of Vietnam (Islam and Catling 2012). The rice plants affected by the WBPH appear uniformly in large areas throughout the field rather than as localized hopperburned patches as in the damage by the BPH. This may be due to the difference in the distribution patterns of the two planthopper species. Under favourable conditions, the insect produces several generations and inflicts heavy damage on the rice crop. Serious outbreaks of the pest in the tropics have been reported in Bangladesh, India, Indonesia, Malaysia, Nepal, Pakistan and Vietnam (Mochida et al. 1982). In Japan, the grain loss caused by this pest has reached up to 90% in some fields (Suenaga 1971). In May–June 1985, it severely damaged rice for the first time in Assam, India, where heavily infested fields were hopperburned and a range of 800–1400 hoppers per sweep were collected. In southern China and North Vietnam, the WBPH caused serious crop losses in 2009/10, destroying young rice crops and moving to other areas in large numbers (Islam and Catling 2012). Major factors to WBPH outbreaks are 1) excessive use of nitrogen fertilizer, 2) close spacing, 3) continuous submerged conditions in the fields and 4) low populations of natural enemies on account of indiscriminate use of insecticides (Hu et al. 1990 in CABI 2017b). In addition, the population of S. furcifera was affected by temperature in China. The population was low when the weather was cold and overcast, intermediate when it was

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warm and rainy, and high when it was warm and dry (Zhu et al. 1990 in CABI 2017b). Ghauri (1979 in CABI 2017b) reported that in 1952 (prior to the Green Revolution) crop losses in Pakistan amounting to 60% were attributed to S. furcifera infestation. This indicates that there are factors other than the introduction of new varieties that increase the importance of the pest.

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3.13 Rice delphacid, Tagosodes orizicolus (Muir) (Homoptera: Delphacidae) The genus Tagosodes was described to accommodate the majority of the species in the Sogatodes genus (Asche and Wilson 1990, Wilson and Claridge 1991). The species T. cubanus (Crawford), T. orizicolus (Muir) and T. pusanus (Distant) are found on rice. T. pusanus is primarily an Asian pest occurring in China, India, Indonesia (Sulawesi), Micronesia, Pakistan, Philippines, Sri Lanka and Taiwan (http://ag.udel.edu/research/ delphacid/species/tagosodes.htm). Distribution: The rice delphacid, T. orizicolus, common and widely distributed in the Neotropics, is a native of and a serious pest in tropical Central American, Caribbean and South American rice-growing countries such as Bolivia, Brazil, Cayman Islands (Grand Cayman), Colombia, Costa Rica, Cuba, Dominican Republic, Honduras, Guatemala, Guyana, Mexico, Panama, Peru, Puerto Rico, Surinam, Trinidad and Venezuela (http://ag.udel.edu/ research/delphacid/species/tagosodes.htm). This insect is a strong long-distance disperser, and the insect has occasionally been found (but not established) as far north as Texas and Louisiana and as far south as Argentina. It was found in Florida and Louisiana in the late 1950s and early 1960s but then disappeared for about 50 years. In October 2015, this pest was found in ratoon rice fields in seven counties in Texas (Mo Way, pers. comm.). Host plants other than rice: The host range of this insect includes many grasses but not broadleaves (Morales and Jennings 2010): Cocos nucifera L. (coconut palm), grassy weeds such as Echinochloa crus-galli (L.) Beauv., Leptochloa chinensis (L.) Nees. and Digitaria ischaemum (Schreb.) Schreb. ex Muhl. and can survive for a short time on Avena strigosa Schreb., Bromus catharticus Vahl, Triticum aestivum L. and Zea mays L. (http://ag.udel. edu/research/delphacid/species/tagosodes.htm). Description and biology: The rice delphacid, T. orizicolus, like most planthoppers, is small in size (2–5 mm in length) with piercing-sucking mouthparts and membranous wings (Asche and Wilson 1990). Adults (Fig. 3.16) have a movable spur at the distal end of the hind tibia. Males are smaller and darker than the females. The male body is brown overall with a yellow stripe from the vertex to the scutellum, with a dark apical spot on the forewings. The wings are yellowish and the veins are yellow, except for some in the apical area and the white costal veins that form the dorsal stripe when the wings are folded over the body. The female body is yellow with dark brown stripes laterally from the mesothorax to the abdomen, leaving a paler longitudinal dorsal stripe that extends from the vertex to the end of the abdomen. Both alate and brachypterous forms may be found in the populations of T. orizicolus. High temperatures and humidity are required for optimal development. Adults can live as long as five weeks and females may lay as many as 160 eggs. Eggs are less than a millimetre in length, cylindrical and slightly curved, and are deposited in clusters, usually in multiples of seven, on rice leaves or in rice leaf sheaths. About 95% of the eggs are laid on the upper side of the leaves. They are white when laid but darken subsequently. This delphacid can diapause in the egg stage, but nymphs usually hatch in 4–8 days. The first instar nymph emerges on the adaxial surface of the leaf and starts feeding within 24 hours. The nymphal body is transparent white, with large red conical eyes. The second instar is yellowish, and in the third it is yellow with two black stripes running the entire length of the body (Mora et al. 2001). Fourth and fifth instars may reach 2.5 mm in length. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Upon crop flowering, winged individuals tend to leave the plants in search of younger rice plantings. With a life cycle of about a month, two to three generations may develop in a rice field. Plant damage and ecology: The rice delphacid is both a direct and indirect pest. Direct damage is caused by removal of plant sap by the adult and nymphal delphacids. Under heavy infestations, feeding may result in ‘hopperburn’, patches of chlorotic or dead leaves or plants (Fig. 3.17). Additional yield losses may result from colonization by sooty mould and other pathogens on leaves with large amounts of honeydew from delphacid feeding. Indirect damage from delphacid feeding may occur via the transmission of the hoja blanca virus (Morales and Jennings 2010). Hoja blanca is a circulative, propagative and transovarially transmitted tenuivirus. However, only a portion of delphacids in any given population are capable of transmitting the virus. Symptoms of the disease include cream-coloured spots on immature leaves followed by systemic chlorosis of leaves and tillers (Fig. 3.18). Panicles in diseased tillers may be completely sterile. Complete yield losses have been reported. Occurrence of the disease is cyclical. The pest is prevalent in Brazil throughout the year with three population peaks in April–May, September, and December–January (Ferreira and Silveira Neto 1979). Studies conducted in Cuba (Sousa et al. 1977) have shown that the development and multiplication of T. orizicolus is greater on young plants than on mature rice plants.

Figure 3.16 Tagosodes orizicolus adult (Source: Alberto Pantoja, USDA-ARS, USA; Centre for Invasive Species and Ecosystem Health, University of Georgia, USA (https://www.bugwood.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 3.17 Hopperburn caused by the feeding of Tagosodes orizicolus (Source: Thais Freitas).

Figure 3.18 Hoja blanca virus infected rice (Source: FEDEARROZ).

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3.14 Rice delphacid, Tagosodes cubanus (Crawford) (Hemiptera: Delphacidae) Geographical distribution: Caribbean – Bahamas, Bermuda, Cayman Islands, Cuba, Jamaica, Martinique, Puerto Rico, St. Lucia, Trinidad; Central and South America – Belize, Bolivia, Brazil Colombia, Costa Rica, Mexico; West Africa – Liberia, Nigeria, Sierra Leone (Heinrichs and Barrion 2004, http://ag.udel.edu/research/delphacid/species/tagosodes.htm). Host plants other than rice: Cocos nucifera L. (coconut palm), Echinochloa spp. and other Gramineae (Wilson and Claridge 1991, http://ag.udel.edu/research/delphacid/ species/tagosodes.htm). Description and biology: Tagosodes cubanus (Fig. 3.19) is smaller than T. orizicolus, being about 2 mm long. It is generally brown. When the wings are folded, a dark spot on the wings forms a saddle-shaped stigmata. It is a sedentary species and its spread is assisted by strong winds and flowing water. The biology has been briefly described in COPR (1976). Females lay 30–350 eggs in batches of seven on the midribs of rice leaves. Eggs are 0.1 mm long, cylindrical, slightly curved and white when first laid. As the eggs develop, the colour darkens. Diapause can occur during the egg stage, but nymphs usually hatch in 4–8 d. Plant damage and ecology: T. cubanus is a vector of hoja blanca virus of rice in South and Central America where 50% of the yield may be lost to this disease (King and Saunders 1984). Plant damage is similar to that caused by T. orizicolus. Little is known about the plant damage, if any, caused by T. cubanus in West Africa. However, based on the damage caused by the insect in South and Central America, it can be considered at the least a potential pest in West Africa.

Figure 3.19 Tagosodes cubanus adult (Source: Wilson and Claridge, 1991). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Nymphs and adults of T. cubanus suck sap from rice leaves and stems. This pest excretes honeydew, which forms a substrate for the growth of sooty mould on the plant. Stephen (1977) reported high populations of T. cubanus in lowland rice at Suakoko, Liberia, during the middle of the wet season. Rice plants with virus-like symptoms were observed, but no tests were conducted to verify the presence of hoja blanca or any other rice virus. Intercropping experiments conducted in Côte d'Ivoire indicated that upland rice was not a suitable crop for cultivation under or near coconut because of frequent infestations by the delphacids T. cubanus and Sogatella kolophon and the cicadellid Recilia mica, which transmit dry bud rot and blast to coconut (Zakra et al. 1986).

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3.15 Spittlebugs, Locris maculata maculata Fabricius and L. rubra Fabricius (Hemiptera: Cercopidae) Few cercopids have been reported to occur on rice throughout the world. Locris species are the only cercopids recorded on rice in West Africa (Wilson and Claridge 1991) and they are confined to Africa (Akingbohungbe 1983). Locris maculata maculata and L. rubra are the most abundant of the species collected in rice in West Africa. Additional species are L. atra Lallem, L. erythromela (Walker) and L. rubens Erichson. Adenuga (1971) developed a key to the Locris genus in Nigeria. He indicated that there are many colour forms that are intermediate between generally accepted species and that some species may thus be morphs of a single species. For example, L. rubens appears to be the same species as L. rubra. Distribution: L. maculata maculata – Burkina Faso, Côte d'Ivoire, Guinea, Guinea-Bissau, Liberia, Mali, Nigeria, Togo; L. rubra – Benin, Burkina Faso, Cameroon, Côte d'Ivoire, Gambia, Guinea, Guinea-Bissau, Mali, Nigeria, Senegal, Togo. Host plants other than rice: Zea mays L., Sorghum bicolor (L.) Moench, Pennisetum glaucum (L.) R. Br., Saccharum officinarum L. Although the host range is not well known, it is likely that they feed on a wide range of grasses (Egwuatu and Ita 1982), millet, rice, sugarcane and numerous grass species. Akingbohungbe (1983) reported Locris spp. as minor pests on cereals in Nigeria. Egwuatu and Ita (1982) reported on damage in maize caused by L. maculata in Nigeria. Ajayi (2000) stated that L. rubens (=rubra) had a wide host range, including sorghum, maize, millet, rice, sugarcane and numerous grass species. Description and biology: Heinrichs and Barrion (2004) have described that the adults of L. maculata maculata and L. rubra. Locris spp. are distinct from other rice insects by the boat-shaped form of the body, their large size and reddish colouration with characteristic spots. L. maculata maculata adults (Fig. 3.20) have a black pronotum, yellow forewing with a black apical one-third and shades of black spots in basal one-third; tibia III black in basal one-half and red in apical one-half; body length 10.5 mm. L. rubra adults (Fig. 3.21) have a red pronotum with a transverse brown band in the posterior portion; oblique reddish brown band in the forewing; reddish brown spot in inner one-third of corium clavus, head dorsally red and black; tibia III red with black anterior end, dark reddish brown basal onehalf and a spine below mid-length; body length 11 mm. Cercopids generally lay eggs in the stems or leaf sheaths of grasses. The nymphs that hatch feed on the stems of grasses and surround themselves with a frothy, spittle-like mass. After the last moult, the adult leaves the spittle and moves about freely. The spittle is derived from fluid excreted from the anus and from a mucilaginous substance excreted by the epidermal glands on the abdomen. Air bubbles are injected into the spittle by means of caudal appendages on the insect. Spittlebugs generally rest head downward on the plant and, as the spittle forms, it flows down and covers the insect. The spittle provides the nymph with a moist habitat and may provide some protection from natural enemies. The adults do not produce spittle (Borror et al. 1981). Plant damage and ecology: Igbinosa (2007) reported L. maculata maculata as a pest of rainfed rice in Nigeria and Heinrichs and Barrion (2004) reported on its occurrence in irrigated lowland rice in Côte d’Ivoire. In the July and August 1995 surveys in Côte d'Ivoire, L. maculata maculata populations were two times as abundant in the lowlands as © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 3.20 Locris maculata maculata adult (Source: IRRI).

Figure 3.21 Locris rubra adult (Source: IRRI).

in the uplands. Locris rubra populations, however, were three to seven times higher in the uplands than in the lowlands. Both L. maculata maculata and L. rubra are more abundant at the lowland sites on the continuum toposequence on the WARDA Research Farm than at the hydromorphic and upland sites (Heinrichs and Barrion 2004). Also both species are distinctly more abundant in unweeded plots than in weeded plots on the continuum toposequence. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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They are among the most abundant insects in lowland rice during the seedling stage and are easily seen because of their large size and because the adults readily fly from the plants when disturbed. Limited research has been conducted on the type and extent of damage by spittlebugs to rice in West Africa. However, it is known that in addition to direct feeding damage, L. maculata maculata and L. rubra are vectors of RYMV (Koudalimoro et al. 2015). Also, Locris spp. belong to the spittlebug group that suck plant sap at the base of the stems and feeding results in leaf bronzing and wilting of the plant. In Australia, the cercopid, Eoscarta carnifex (F.) causes systemic damage to sugarcane by injecting an unidentified toxin into the plant (Rodman and Miller 1992). Locris maculata maculata populations in a 120-d duration rice crop in irrigated lowland rice in Sierra Leone were present throughout the crop period during both the wet and dry seasons. However, populations were highest during the wet season (Taylor and Kamara 1974). During the wet season, the insect was most abundant from the seedling stage to the end of tillering, peaking at 6 WAT and dropping rapidly thereafter. During the dry season, populations continued to near harvest. Populations of both Locris spp. occur throughout most of the crop period on irrigated lowland rice on the WARDA Research Farm at M'be but distinctly peak at 4 WAT. Populations occurred throughout the year but were low for most monthly transplanting dates. Both species were most abundant in the crop transplanted in November, the sampling of which covered the 12-week period of 14 November to 14 February. These dates include the harmattan period in the middle of the dry season. In contrast, a study by Taylor and Kamara (1974) in Sierra Leone indicated that L. maculata maculata was most abundant during the wet season crop, with populations being three times those of the dry season crop.

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3.16 Spittlebugs (Cigarrinha das pastagens), Deois flavopicta Stål (Hemiptera: Cercopidae) Distribution: The spittlebug Deois flavopicta Stål is a neotropical species distributed throughout the south-east and central-west regions of Brazil (Ferreira 1998) and has been reported from Colombia (Pantoja et al. 1997). Host plants other than rice: Numerous grass species, including the following species in Brazil: Axonopus barbigerus (Kunth) Hitch, A. marginatus (Trin.) Chase, A. siccus (Nees) Kunth, Brachiaria decumbens Stapf, Echinolaena inflexa (Poiret) Chase, Melinis minutiflora Beauv., Mesosetum loliiforme (Hochst.) Chase, Panicum campestre [Nees ex] Trin., Paspalum erianthum Nees ex Trin., P. guenoarum (Hack.) Parodi P. pilosum Lam. and P. plicatulum (Pires et al. 2000, Nilakhe 1985, Cosenza et al. 1989). Description and biology: Nymphs hatch from the eggs at the beginning of the rainy season. They have yellowish bodies and feed in pastures (Cosenza 1989), sucking the roots upside down and producing white foam, which is made of the liquid excreted through the anus and a mucilaginous substance secreted by Batelli glands. Nymphs go through six instars. When they reach adulthood, they move to feed only on rice plants even if pasture is available. Adults (Fig. 3.22) are 10 mm long, black on dorsal side with three yellow spots in each tegmina. Abdomen and legs are red, with two spines on the tibia of the hindlegs.

Figure 3.22 Deois flavopicta adult (Source: http://ruralcentro.uol.com.br). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: Originally, this species fed on a broad range of native grasses and has always exhibited low population densities on the cerrado, the Brazilian savanna. After the introduction of exotic grasses, principally in the genus Brachiaria (Poaceae), D. flavopicta populations increased to outbreak levels in cultivated pastures (Pires et al. 2000). It is a serious rice pest especially in the upland cultivation and in regions where rice is rotated with pastures. The spittlebugs, D. flavopicta (Stål) and D. schach (F.) cause damage to rice fields that are adjacent to pastures in Brazil (Rosseto et al. 1978). These insects have become severe pests of grassland pastures, especially Brachiaria decumbens, where they develop during the warm, humid months. Populations that build up on B. decumbens fly to neighbouring rice fields where they cause severe damage. Rice spittlebugs suck sap fluid from leaves and stems of rice, introducing toxic saliva that causes a ‘burning’ symptom in plants. Five to seven days after being attacked, plants become yellow and dry and subsequently the entire plant is destroyed (Ferreira et al. 2003). In the state of Mato Grosso do Sul, Brazil, 23,000 ha of rice were destroyed by spittlebugs during the 1983–84 growing season (Nilakhe 1985).

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3.17 References Adenuga, A. O. 1971. A key to two families of Nigerian Cercopoidea (Homoptera). Occas. Publ. Entomol. Soc. Nigeria No. 4 . Ajayi, O. 2000. How important are spittle bugs on sorghum? In: Entomology in Nation Building: the Nigerian Experience. Proceedings, ESN 30th Annual Conference, Dike, M. C., Ajayi, O., Okunade, S.O., Okoronkwo, N. O., Abba, A. A. (Eds), 4–7 October 1999. International Crops Research Institute for the Semi-Arid Tropics, Kano, Nigeria, pp. 91–7. Akingbohungbe, A. E. 1983. Nomenclatural problems, biology, host plant and possible vector status of Auchenorryncha associated with crop plants in Nigeria. In Proceedings of the 1st International Workshop on Leafhoppers and Planthoppers of Economic Importance, Knight, W. J., Pant, N. C., Robertson, T. S., Wilson, M. R. (Eds), pp. 365–70. Commonwealth Institute of Entomology, London. Alam, A., Islam, A. 1959. Biology of the rice leafhopper, Nephotettix bipunctatus Fabr. in East Pakistan. J. Pakistan Sci. Res. 2:20–28. Alghali, A. M., Domingo, J. S. 1982. Weed hosts of some rice pests in Sierra Leone. Int. Rice Res. Newsl. 7(2):10. Anonymous. 1976. Pest Control in Rice. PANS Manual No. 3, Centre for Overseas Pest Research, London, pp. 138–9. Asche, M., Wilson, M. R. 1990. The delphacid genus Sogatella and related groups: a revision with special reference to rice associated species (Homoptera: Fulgoroidea). Syst. Entomol. 15:1–42. Basu, S. K., Mishra, M. D., Ghosh, A., Niazi, F. R., Rayachaudhuri, S. P. 1976. Some observations on the overwintering of rice tungro virus and Nephotettix virescens (Distant) in Delhi. Indian J. Entomol. 38:57–62. Borror, D. J., De Long, D. M., Triplehorn, C. A. 1981. An Introduction to the Study of Insects, 5th ed., Saunders College Publishing, New York. Cabauatan, P. Q., Cabunagan, R. C., Il-Ryong, C. 2009. Rice viruses transmitted by the brown planthopper Nilaparvata lugens Stål. In Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia, Heong, K. L., Hardy, B. (Eds), pp. 357–68. International Rice Research Institute, Los Baños (Philippines). CABI. 2016a. Nisia nervosa (gray planthopper) Invasive Species Compendium. http://www.cabi.org/ isc/datasheet/3634 CABI. 2016b. Nephotettix nigropictus (rice green leafhopper) Invasive Species Compendium. http:// www.cabi.org/isc/datasheet/36200 CABI. 2016c. Nephotettix cincticeps (rice green leafhopper). Invasive Species Compendium. http:// www.cabi.org/isc/datasheet/36197 CABI.2016d. Invasives pecies compendium/Nephotettix virescens (green paddy leafhopper). http:// www.cabi.org/isc/datasheet/36198 CABI. 2016e. Recilia dorsalis (zigzag leafhopper). Invasive Species Compendium. http://www.cabi. org/isc/datasheet/46924 CABI. 2016f. Laodelphax striatellus (small brown planthopper). Invasive Species Compendium. http:// www.cabi.org/isc/datasheet/10935 CABI. 2016g. Nilaparvata lugens (brown planthopper). Invasive Species Compendium. http://www. cabi.org/isc/datasheet/36301 CABI. 2017a. Sogatella furcifera. Distribution. Plantwise Knowledge Data Bank. http://www.plantwise. org/KnowledgeBank/PWMap.aspx?speciesID=40151&dsID=50497&loc=global (Accessed 03-05-2017). CABI. 2017b. White-backed planthopper (Sogatella furcifera). Plantwise Technical Factsheet. Plantwise Knowledge Data Bank. http://www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsid=50497 (Accessed 03-05-2017). Chaudhary, J. P., Atwal, A. S., Sohi, B. S. 1968. Delphacid hopper — a serious pest of paddy. Prog. Farming (India) 5:24–5.

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Chapter 4 Biology and ecology of rice-feeding insects: foliage feeders E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; and T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 4.1 Introduction 4.2 Large rice grasshopper (Hieroglyphus banian Fabricius) 4.3 Rice grasshopper (Hieroglyphus daganensis Krauss) 4.4 Short-horned grasshoppers 4.5 Variegated grasshopper 4.6 Meadow grasshoppers 4.7 Whitefly 4.8 Rice whitefly 4.9 Spider mite 4.10 Rice thrips 4.11 Rice leaffolder (Cnaphalocrocis medinalis Guenée) 4.12 Rice leaffolder (Marasmia patnalis Bradley) 4.13 Fijian rice leaffolder 4.14 Rice caseworm 4.15 Green horned caterpillar 4.16 Rice skipper (Parnara guttata Bremer and Grey) 4.17 Rice skipper (Pelopidas mathias F.) 4.18 Rice ear-cutting caterpillar 4.19 The fall armyworm (Spodoptera frugiperda J. E. Smith) 4.20 Common cutworm 4.21 Rice swarming caterpillar 4.22 Common armyworm (Mythimna unipuncta Haworth) http://dx.doi.org/10.19103/AS.2017.0038.04 © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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4.23 Rice green semiloopers 4.24 Green hairy caterpillar 4.25 Rice whorl maggot (Hydrellia prosternalis Deeming) 4.26 Rice leaf miner (Hydrellia griseola Fallen) 4.27 Rice whorl maggot (Hydrellia philippina Ferino) 4.28 South American rice miner 4.29 Leaf miner (Cerodontha orbitona Spencer) 4.30 Paddy stem maggot 4.31 Asian rice hispa 4.32 African rice hispa 4.33 Rice blue beetle 4.34 Rice leaf beetle 4.35 Flea beetle 4.36 Ladybird beetle 4.37 Foliage feeding aphids 4.38 References

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4.1 Introduction There are numerous insect species that feed on the foliage of rice. Many of the species are in the orders Coleoptera, Lepidoptera, and Orthoptera, of which the adult beetles, larvae, and nymphs, respectively, feed on the leaves. In addition, sucking insects such as whiteflies and aphids suck sap from the leaves. Foliage feeding by insects, with chewing mouthparts, causes three types of damage: 1) removal of the chlorophyll layer of the leaves by the scraping-like feeding, 2) actual consumption of portions of a leaf or entire leaves, and 3) leaf mining or feeding between the epidermal layers. Removal of chlorophyll decreases the photosynthetic activity and thus reduces grain development. Extent of yield losses caused by defoliators depends on the age of the plant and extent of green matter removed. Young plants often produce new foliage, recuperate, and grain yields may not be affected. The amount of yield loss to defoliation also depends on the other abiotic stresses that may occur simultaneously (Heinrichs 1988). For example, drought-stressed plants are more susceptible to insect defoliation because they are not able to recuperate from feeding as are non-stressed plants. In addition to direct damage, some beetles mechanically transmit Rice Yellow Mottle Virus (RYMV) that is usually more damaging than the feeding injury itself. Among the arthropods that remove sap from the leaves with their sucking mouthparts are the whiteflies, aphids and spider mites. Two whitefly species, Aleurocybotus indicus and A. occiduus are pests of rice in Asia and Africa and Asia and the Americas, respectively. Extensive feeding and the high amounts of sooty mould growth on the honeydew produced by the aphids may eventually lead to wilting and death of the plants (Alam 1989). Many aphid species infest the aerial parts of rice even though rice is not the primary host plant for most of them. The bird cherry oat aphid, Rhopalosiphum padi, is a vector of the virus disease, ‘gaillume’ (yellow disease or rice yellows) in Italy. The spider mite species (Tetranychidae) are extremely small arthropods that are important pests of rice in in the Sahel area of West Africa (Heinrichs and Barrion 2004). As the common name implies, these mites spin silken webs on the plant. Among the leaf-feeding beetles (Coleoptera), several chrysomelids have potential to cause severe crop losses (Heinrichs and Barrion 2004). The hispids, Dicladispa armigera and Trichispa sericea are major pests in Asia and Africa respectively. Both grubs (larvae) and adult beetles feed on rice plants. Grubs mine the leaves and the adults feed externally. Three additional chrysomelids; the rice blue beetle, Leptispa pygmaea, rice leaf beetle Oulema oryzae and the flea beetles, Chaetocnema spp. are foliage feeders. A coccinellid, the ladybird beetle, Chnootriba similis is a minor pest as a leaf-feeder in Africa. However, C. similis and some Chaetocnema spp. are RYMV vectors in Africa. Numerous lepidopteran leaf feeders are important pests wherever rice is grown. All have a wide host range but some are more restricted to rice. Feeding is restricted to the larval (caterpillar) stage. A number of noctuids are major pests. The noctuid group includes: 1) Ear cutting caterpillar, Mythimna separata; 2) Fall armyworm, Spodoptera frugiperda; 3) Common cutworm, Spodoptera litura; 4) Rice swarming caterpillar, Spodoptera mauritia 5) Rice green semi-looper, Naranga aenescens and 6) Green hairy caterpillar, Rivula atimeta. All are Asian pests except the fall armyworm, S. frujiperda, which is a pest of rice in the Americas.

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Several dipteran species are rice leaf feeders. The most common are the whorl maggots, Hydrellia prosternalis and H. philippina; rice leaf miner, H. griseola; South American rice miner, H. wirthi; paddy stem maggot, H. sasakii, and the leaf miner Cerodontha orbitona. These species cause only minor leaf damage to crops, in the early growth stages, and in the absence of other major abiotic or biotic stresses, the crop often recuperates. A number of species of grasshoppers are occasionally found in rice fields, but rarely cause significant damage other than along the field margins. They chew angular holes in leaves, causing an injury similar to that caused by leaffolders or armyworms. These insects are polyphagous; and besides rice, they feed on maize, sugarcane, millets and many grasses. A list of rice grasshoppers and their general distribution is given in Table 4.1. Nearly 30 grasshopper species, belonging to the short-horned (Acrididae and Pyrgomorphidae) and the long-horned (Tettigoniidae) families, attack rice plants in West Africa. However, most species are not of economic importance on rice because they occur in low populations. Among the most important species of the short-horned Table 4.1 Rice grasshoppers and their distribution Species

General distribution

Acrida turrita Krauss

India

Acrida exaltata Walker

India

Acrotylus humbertianus Saussure.

India

Aeolopus affinis Bol.

India

Aeolopus tamulus F.

South and Southeast Asia

Atractomorpha crenulata F.

India, Malaysia

Chrotogonus sp.

India

Colemania sphenarioides Bol.

India

Gastrimargus spp.

Africa, India, Southeast Asia

Heteropternis respondens Walker

India, Taiwan

Hieroglyphus banian (F.)

South and Southeast Asia, China

Hieroglyphus daganensis Krauss

Africa

Hieroglyphus furcifer Sw.

India

Hieroglyphus nigrorepletus (I. Bol.)

South and Southeast Asia, China

Hieroglyphus oryzivorus Carl

India, Pakistan

Oxya chinensis (Thunberg)

India, Southeast Asia to Japan

Oxya intricata (Stål)

Africa, South and Southeast Asia

Oxya japonica (Thunberg)

South and Southeast Asia, Japan

Pyrgomorpha conica Olivier

Cyprus, India

Conocephalus maculatus (Guillou).

Africa, India

Conocephalus longipennis (de Haan)

Africa, India

Zonocerus variegatus

Africa

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ones are Atractomorpha spp. Chrotogonus spp., Hieroglyphus africanus Uvarov, H. daganensis Krauss, Oxya hyla Serville Zonocerus variegatus (L.) and of the long-horned ones is Conocephalus spp. Nwilene et al. (2009) reported Conocephalus longipennis, Oxya hyla and Zonocerus variegatus as being transmission agents of RYMV in West Africa. In West Africa, grasshoppers are most important on irrigated rice grown in the dry zones of the Sahel. In these regions, rice is a major form of green vegetation during the hot dry season and grasshoppers congregate on these fields. In Asia grasshoppers are of less importance than in Africa. Key species in Asia are Hieroglyphus banian (F.) and Oxya chinensis T.

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4.2 Large rice grasshoppers, Hieroglyphus banian (Fabricius) and Hieroglyphus nigrorepletus (I. Bol.) (Orthoptera: Acrididae) Distribution: Bangladesh, Cambodia, China, India, Laos, Myanmar, Pakistan, Sri Lanka, Thailand, Vietnam (CABI 2016a). Host plants other than rice: Cajanus cajan (L.), Dactyloctenium aegyptium (L.), Gossypium hirsutum L., Lens culinaris Medik, Panicum miliaceum L., Pennisetum glaucum (L.) R. Br., Pennisetum purpureum K. Schumach., Pennisetum typhoides Stapf and C. E. Hubb., Pisum sativum L., Saccharum officinarum L., Sorghum bicolor (L.) Moench Sorghum halepense (L.) Pers., Setaria italic (L.) Beauv., Zea mays L. (CABI 2016a) Description and biology: The adult H. banian (Fig. 4.1) is of medium size, the female measuring 34–54 mm and the male, 28–40 mm in length. It is dull green or yellow brown. The lower body surface is brownish black. Adults of H. nigrorepletus (Fig. 4.2) are more commonly found in the brachypterous than macropterous form. The adults mate after a short pre-copulation period of 1–3 days. Egg pods are laid in soil, each pod containing about 35 eggs. The total number of eggs laid per female ranges from 100 to 150. Individual eggs are yellowish and covered with a gummy substance that hardens into a waterproof coating. In wet sandy soil, eggs are laid at a depth of 3-5 cm, while in dry sandy soil, they are laid on the soil surface. Oviposition

Figure 4.1 Hieroglyphus banian adult (Source: not known). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.2 Hieroglyphus nigrorepletus adult (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in).

Figure 4.3 Hieroglyphus banian feeding on rice (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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occurs from October to December and the eggs remain in soil till rains begin the following June–July (Dale 1994). Nymphs hatch out shortly after the rainy season begins. If the rains are poor, the eggs do not hatch and at temperatures above 40°C, there is heavy egg mortality. Young hoppers are brownish yellow and later change to dull green. Nymphs that hatch from egg pods buried in compact soil at a depth of more than 5 cm are unable to come out (Pradhan 1969). Like the adults, nymphs hide from birds during the day and feed on rice foliage at night. The usual number of instars is 5 to 6 for males and 7 for females. There is only one generation a year. The longevity of the grasshopper ranges from 1 to 8 months. Plant damage and ecology: These grasshoppers occasionally reach economic status, in marshy and humid habitats. Serious outbreaks have been reported from many parts of India (Nair 1978, Singh and Dhamdhere 1982). The nymphs eat newly germinated rice seedlings and cause them to wither. Adult grasshoppers feed on the leaves and shoots. In the earhead stage, the adults attack the ears, nibble at the tender florets or gnaw into the base of the stalks (Fig. 4.3). If the emerging inflorescence is attacked, the resulting grains become chaffy (Fig. 4.4) (Chatterjee and Debgoswami 1981). Large numbers of H. nigropletus can strip all of the leaves from a rice plant in a short period of time. H. banian has been shown to be involved in the mechanical transmission of Xanthomonas oryzae pv. oryzae, although it does not survive within the insect (Murty and Devadath 1981).

Figure 4.4 Chaffy rice grains due to grasshopper damage (Source: LSU Ag Center). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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4.3 Rice grasshopper, Hieroglyphus daganensis Krauss (Orthoptera: Acrididae) Distribution: Cameroon, Ghana, Mali, Niger, Nigeria, Senegal. Host plants other than rice: Andropogon gayanus Kunth, Arachis hypogaea L., Chrysopogon aciculatus (Retz.), Diectomis fastigiata (Sw.), Hyparrhenia chrysargyrea (Stapf), Pennisetum subangustum Stapf and Hubb., Rottboelia exaltata L., Setaria sphacelata (Schumacher) Moss and Sorghum bicolor (L.) Moench (Dale 1994). Description and biology: Agyen-Sampong (1975) described the biology of H. daganensis in Ghana, where it has caused significant damage in rice. The adult is pale greenish yellow or light orange with yellow patches. It has distinct, dark lateral markings on the pronotum that resemble hieroglyphs (Fig. 4.5). The head is ochraceous (dark yellow) with light brown eyes, greenish mandibles and a black band under the back of the genae. The male is 3-4 cm long and the female is longer at 4-6 cm. Short-winged (brachypterous) forms of adults are more common than long-winged (macropterous) ones. In September–October, the grasshopper population is higher in rice fields than on grasses, but the reverse is true during November–December. Mating and oviposition occur from October to early December. Eggs are laid in egg pods in the soil and they hatch at the beginning of the rainy season in July of the following year.

Figure 4.5 Pair of Hieroglyphus daganensis adults (Source: Christiaan Kooyman). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: Hieroglyphus daganensis is found primarily in swampy areas, where it has a wide host range, and it feeds on a number of grassy weeds and gramineous crops. The grasshoppers start appearing in rice fields in August, and the population reaches its peak during September–October, which coincides with booting and panicle initiation stages of the rice plant. At the end of October, when the crop begins to mature and leaves start turning yellow, the grasshoppers leave for other grassy host plants. Both the nymphs and the adults feed on rice leaves. When H. daganensis populations are high, the stems and panicles are also attacked. In Ghana, this insect has appeared in large populations since 1972 and has damaged large areas of rice. Yield losses of about 10% have been estimated in outbreak areas (Dale 1994).

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4.4 Short-horned grasshoppers, Oxya spp. (Orthoptera: Acrididae) Distribution: Several short-horned grasshoppers in the Oxya genus occur on rice throughout the world. Oxya hyla Stal, O. chinensis (Thunberg) and O. velox (F.) occur in both Africa and Asia (Delvi and Pandian 1971, Reissig et al. 1986, Dale 1994, Heinrichs and Kassoum 1996). Oxya hyla intricata (Stal) and O. japonica japonica (Thunberg) are additional Oxya species that occur in Asia (Reissig et al. 1986). Host plants other than rice: Oxya chinensis feeds on Cyperus rotundus L., Saccharum officinarum L. and Zea mays L. (Dale 1994). Information on the other species is lacking but it is presumed that they have a wide host range of crops and wild grasses. Description and biology: Dale (1994) described the biology of Oxya chinensis. Adult Oxya chinensis (Fig. 4.6) and O. hyla intricata (Fig. 4.7) are bright green and have a distinct dark band running laterally from behind each compound eye through the thorax to the base of the wings. The male is about 20 mm long and the female about 30 mm. Eggs are laid in masses or pods consisting of 10 to 30 eggs. The egg masses are covered with a white, froth secretion that hardens to form an ootheca, which protects the eggs from drying. Eggs are laid behind rice leaf sheaths, among rice stems, in rice leaf folds and in grass clumps above the water level. In dry conditions, the eggs are located just below the surface of the soil. Eggs hatch in 2-3 wk. Generally, there are six nymphal instars over a period of about 100 d.

Figure 4.6 Oxya chinensis adult (Source: www.flickr.com/ © Andrew Hardacre Photography). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: Oxya spp. are general feeders (Alam 1992) consuming foliage of grass species in addition to rice. Plant damage in rice is the same as that caused by other grasshopper species previously mentioned. Both the nymphs and adults feed on leaf tissue, consuming large sections from the edges of leaf blades. Nurseries suffer severe damage when attacked by high Oxya populations. According to IRRI (1983), Reckhkaus and Andriamasintseheno (1997) and Koudamiloro et al. (2014 and 2015), Oxya hyla transmit RYMV. Many studies have shown that the virus is vectored by several insect species in a process of a first ingestion of leaf material and subsequent transmission in following feedings. RYMV is the major viral constraint to rice production in Africa. RYMV was first identified in 1966 in Kenya and then later in most African countries where rice is grown (Koudamiloro et al. 2015). Studies on lowland irrigated rice on the WARDA Farm in Côte d’Ivoire showed that Oxya hyla was present throughout the crop period, but populations peaked at 8 WAT. WARDA studies on seasonal occurrence indicated that O. hyla was present throughout the year with peak populations occurring in October and March. In surveys conducted in Côte d'Ivoire and Guinea (Heinrichs and Barrion 2004), Oxya spp. occurred in both the humid forest zone and in the Guinean savanna. Populations were four times as high in Guinea as in Côte d'Ivoire, but were similar in both climatic zones. In the August, 1995 Côte d'Ivoire surveys, these grasshoppers were collected in both upland and lowland fields but the population was highest in the lowland fields. According to Shepard et al. (1995), Oxya spp. are adapted to aquatic environments.

Figure 4.7 Oxya hyla intricata adult (Source: Paul Thompson, Thailand Wildlife; http://thailandwildlife. photoshelter.com/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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4.5 Variegated grasshoppers, Zonocerus variegatus (L.) (Orthoptera: Pyrgomorphidae) The variegated grasshopper, Zonocerus variegatus, commonly called ‘stinking locust’, belongs to the short-horned group and is one of the most common grasshopper species occurring in lowland rice in the forest and Guinean savanna zones of West Africa. It is readily seen because of its large size and striking colours. Another Zonocerus species, Z. elegans (Thunberg), also occurs in Africa. Geographical distribution: Zonocerus elegans occurs between the Equator and the Tropic of Capricorn and is restricted to eastern and southern Africa (Toye 1982). It is distributed throughout West Africa, south of the Sahara and spreads east to Uganda and north to Sudan (Page 1978). Host plants other than rice: Zonocerus variegatus is polyphagous, feeding on a wide range of wild and cultivated plant species. Reports from Nigeria (Page 1978, Toye 1982, Nwana 1984) list its hosts as banana, cassava, citrus, cocoa, cola, cotton, cowpea, citrus, maize, okra, oil palm, pawpaw, pepper, pineapple, plantain, rice, soybean, teak, yam, various green vegetables and Chromolaena odorata. Description and biology: Characterized by a large size (female is between 35 and 52 mm long while male varies between 30 and 45 mm in length). Z. variegatus has a striking colour (Fig. 4.8) and can produce a repugnant protecting smell. The head is vertical to the body with a black clypeus in the dorsal half with six yellow spots. Its ventral half is yellow. The femur has black spots in the apical part and the tibia III has six spines in the outer row and eight spines in the inner row. The biology of Z. variegatus is well documented (Toye 1971, 1982; Page 1978; de Gregorio 1982; McCaffery and Page 1982; Chapman et al. 1986). Intense oviposition follows periods

Figure 4.8 Zonocerus variegatus adult (Source: www.trigobert.net). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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of heavy rainfall. Oviposition sites are usually in shady areas beneath woody plants and are close to cultivated plants such as cassava. The female lays eggs after mating two or three times; an individual might lay up to six egg pods in a lifetime. Egg pods are injected into the soil. There are about 50 eggs per pod, and pod densities may exceed 500 m2. Eggs usually undergo diapause before development of the embryo. Eggs laid in November develop through the dry season and hatch in March. Eggs laid in February develop through the wet season and hatch in September. Eggs only survive when and where the soil remains moist for long periods. Because eggs are clumped together, first instar nymphs, upon hatching, aggregate in large numbers on low, herbaceous vegetation. There are usually six nymphal instars. The nymphs and adults are gregarious and the first through third instars are distinctly so. The nymphs aggregate in the morning and in the early evening, but during the hours of bright sunshine, they disperse to feed on weeds. There is little activity between 2100 and 0600 . Later instars disperse to feed on rice and other crops. They disperse about 500 m or more between hatching and becoming adults. Adults of the dry season population, which appear in February, are dimorphic in wing length, with the long-winged forms being capable of flights exceeding 100 m. The life cycle of Z. variegatus varies with latitude in West Africa (Iheagwam 1983). According to de Gregorio (1988), rainfall and humidity regulate the life cycle of the variegated grasshopper in Togo. In the savanna regions of Cameroon, Mali and Nigeria, where the rainy season is well defined, development is similar to that of other grasshoppers (Chapman et al. 1986). First instar nymphs hatch in April or May, just before rains begin. Nymphal development continues through the wet season and the adults mature. The females mate and lay eggs in the soil in October with the onset of the dry season. The eggs survive the dry season only if the soil remains moist. In the forest region, and associated derived savanna, the life cycle is more complex. Rainfall is bimodal and the dry season is shorter and less defined than in the north. At least in the region extending from the west of Nigeria to Guinea, some eggs hatch from September to April. Insects that hatch early in this period (September to November) develop during the dry season. Nymphs that hatch from eggs in March and April develop wholly in the wet season. Oviposition may occur at any time of the year. Populations in different localities may be at different stages of development even though they are only separated by a few kilometres. In Côte d'Ivoire, populations separated by only 3 km were more than a month out of phase (Vuillaume 1954). Plant damage and ecology: In Nigeria, especially in the more tropical south, Z. variegatus causes considerable damage to crops that are grown during the dry season months of October to March (Nwana 1984). Zonocerus variegatus is polyphagous, feeding on a wide range of wild and cultivated plant species. In southern Nigeria, cassava is the major crop damaged, but serious damage to other crops has also been observed (Page 1978). Feeding on a mixed diet of even relatively poor food-quality species such as the weed Chromolaena odorata (L.) and other plant species is generally more beneficial to Z. variegatus than feeding on a single plant species (Modder and Tamu 1996). Zonocerus variegatus feeds around the clock but is most active during the day, resting a good part of the time from dusk until morning. Modder (1984a) found that, in Nigeria, most feeding activity takes place between 1300 and 1900. In the forest region in the southern portion of its range, Z. variegatus occurs in both the dry and wet seasons, but it is most abundant during the dry season. In the savanna, it is mostly restricted to the wet season (Chapman et al. 1986). Results of seasonal occurrence studies conducted in Ibadan, Nigeria, were similar to those conducted at WARDA in Bouake, Côte © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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d'Ivoire. Zonocerus variegatus populations in lowland irrigated rice were observed from the beginning of the dry season in October to the end of the dry season in April with peak populations occurring at mid-dry season from December to January (Page 1978). The pest status of Z. variegatus appears to have increased in the forest zone of West Africa since the 1960s (Modder 1984b). Three interrelated factors may be involved (Chapman et al. 1986: 1)) a reduction in the dense evergreen forest area, 2) an increase in the growing area of cassava and 3) the spread of the 'Siam weed', Chromolaena odorata L. During the 1976–80 period, the area of closed forest in Nigeria, Côte d'Ivoire and Cameroon decreased at an annual rate of 300,000, 285,000 and 80,000 ha, respectively. Zonocerus variegatus has become an important pest in these countries. Closed forests favour a fungal disease, Entomophaga grylli (Fres.), which normally controls Z. variegatus. Areas cleared of trees become drier and the Z. variegatus population is no longer restricted by the fungus. The reduced forest area is attributed to shifting cultivation, which involves increased cassava production. In the forest regions where cassava is widely grown, it probably contributes to the dry season survival of Z. variegatus. Cassava-fed Z. variegatus have high fertility (Chapman et al. 1986) and this may contribute to the increase in populations. The weed, Chromolaena odorata, which was introduced into West Africa from Sri Lanka in the 1930s, quickly colonizes areas cleared of forest. The spread of this broadleaf in West Africa corresponds to the apparent increase in Z. variegatus populations. Toye (1974) suggested that the spread of this weed in Nigeria might have been at least partly responsible for the increasing occurrence of Z. variegatus outbreaks. Modder (1984b) found that the tops of C. odorata plants, especially the inflorescence, are favoured roosting sites for Z. variegatus nymphs. The genus Chromolaena produces pyrrolizidine alkaloids and it is believed that Z. variegatus uses them for some non-nutritional purpose, such as an attractant pheromone. Thus, Chromolaena spp., being a ready source of the alkaloids, may have contributed to an increase in the populations of this grasshopper (Chapman et al. 1986). Zonocerus variegatus damage in rice is sporadic and depends on the availability of other plant hosts adjacent to rice fields. Nymphs and adults feeding on rice remove large areas of foliage, typical of other grasshopper species. Although damage is usually light, severe attacks can cause plant death. There is a lack of data on the yield losses caused by Z. variegatus in rice and other crops.

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4.6 Meadow grasshoppers, Conocephalus spp. (Orthoptera: Tettigoniidae) Meadow grasshoppers, which belong to the long-horned group of grasshoppers, are minor pests of rice. Geographical distribution: Conocephalus maculatus (Le Guillou) (Fig. 4.9) – The spotted meadow katydid is widely distributed throughout Africa, the Middle East, Southeast Asia and Australasia (http://www.iucnredlist.org/details/summary/20633133/0). Conocephalus longipennis (de Haan) (Fig.4.10) –Distribution probably similar to that of C. maculatus. Host plants other than rice: Grasses. Description and biology: The meadow grasshoppers, also called katydids, are distinguished from other grasshoppers by the long thread-like antennae; the elongated, sickle-shaped ovipositor; and the four-segmented tarsi. Body colour is bright green and wings are brown (Fig. 4.9 and 4.10). Conocephalus is a diurnal, grass-frequenting genus (Key 1970). Conocephalus spp. lay eggs in grass stems and feed on grasses and their seeds (Scholtz and Holm 1985). The stages of development of Conocephalus longipennis were studied in the Philippines. It completed its life cycle in 142–182 days. The peak of abundance in the field occurred at 63–77 days after transplanting (Rubia et al. 1990).

Figure 4.9 Conocephalus maculatus adult (Source: not known). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Plant damage and ecology: Although the host range of Conocephalus spp. has not been reported, grasshoppers, in general, have a wide range of hosts. Conocephalus is considered a grass-frequenting genus (Key 1970). The meadow grasshopper was the most abundant orthopteran occurring in the monthly planting test on the WARDA Farm. Conocephalus spp., at WARDA, occurred in lowland rice throughout the crop growth period. Peak populations were recorded at 8 WAT in 1994–95 (Heinrichs and Barrion 2004). Conocephalus spp. are present throughout the year, but populations vary greatly within the year. Peak populations are observed in rice transplanted in October and November. Conocephalus spp. occur in both the forest (humid tropical) and Guinean savanna climatic zones. In surveys conducted in Côte d'Ivoire and Guinea, it was reported that Conocephalus spp. prefer the more moist habitats of the continuum toposequence. Extremely low populations were observed in the upland sites (Heinrichs and Barrion 1994). On rice, meadow grasshoppers feed on both the foliage and rice panicles (Barrion and Litsinger 1987). Conocephalus spp. eat the highly nutritive rice anthers by cutting through the lemma or palea, thus damaging the rice spikelets. Its damage is distinguished from bird, rat or rice bug damage by the small holes made in each spikelet. Birds and rats strip off many spikelets and bugs feeding on the seeds do not make observable holes. Feeding holes on damaged 1-d-old spikelets are observed to turn from white to brown by the third day. Caged adults can destroy 10-28 spikelets daily (Heinrichs and Barrion 2004). Its role as a predator of other rice pests may be more important than its role as a rice pest itself. Rothschild (1970) reported that C. longipennis is an important predator of rice insects in Malaysia. In laboratory and field observations conducted in Malaysia, Ito et al. (1995) observed C. longipennis feeding on eggs of the rice bug, Leptocorisa oratorius

Figure 4.10 Conocephalus longipennis adult (Source: Ahmad Omar; www.flickr.com/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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(F.). In field tests conducted in the Philippines, C. longipennis destroyed 46% of the egg masses of yellow stem borer, Scirpophaga incertulas (Walker) (Pantua and Litsinger 1984a). In another study conducted in the Philippines, Rubia et al. (1990) reported that Conocephalus longipennis fed on the nymphs and adults of rice pests, viz. brown planthopper, Nilaparvata lugens; white-backed planthopper, Sogatella furcifera; and green leafhopper, Nephotettix virescens. It also fed on adults of the yellow stem borer, Scirpophaga incertulas; striped stem borer, Chilo suppressalis; leaffolder, Marasmia patnalis; whorl maggot, Hydrellia philippina; and rice bug, Leptocorisa oratorius. One meadow grasshopper consumed more than eight yellow stem borer egg masses in 3 d. Conocephalus maculatus is a predator of the striped stem borer, Chilo suppressalis (Walker), in Japan (Miyata and Saito 1982). Conocephalus longipennis has been reported as being a transmission agent of RYMV in West Africa (Abo 1998, Abo et al. 1998, Nwilene 1999). Among the various insects tested by Bakker (1971, 1974) in Kenya, only the chrysomelid beetles and the grasshopper, Conocephalus merumontanus (Sjostedt), transmitted RYMV.

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4.7 Whitefly, Aleurocybotus indicus David and Subramaniam (Hemiptera: Aleyrodidae) Members of the Aleyrodidae family usually appear white on account of the powdery or waxy material that covers their wings, hence the name whitefly. Few species of these small insects have been recorded on rice; however, Williams and Diop (1981) reported Aleurocybotus indicus David and Subramaniam to be an important pest of rice in West Africa. A. occiduus Maria was reported as a pest on rice in Nepal (Pokhrel and Thapa 2011). The only other whitefly species previously recorded on rice is the polyphagous species Bemisia tabaci Gennadius (Fig. 4.11) found at Madras, India, in 1970 (Zoological survey of India 70:133-233 cited in Williams and Diop 1981) and Trialeurodes oryzae (Westwood) reported by Chia-Hwa (1973) on the Chinese Agricultural Mission farms in Bobo-Dioulasso, Burkina Faso. Geographical distribution: West Africa, Asia. In West Africa, A. indicus was first reported on rice in Senegal in 1977 (Alam 1989). It has since been reported from Bobo-Dioulasso in Burkina Faso; Kogoni, Mali; Basse, Georgetown and Kolikunda, Gambia; Kaedi, Lamin, Sapir and Sankuli Kinda, Mauritania; Niger; Ibadan and Badeggi, Nigeria; and Richard-Toll, Fanaye and Guede-Podor, Senegal (Heinrichs and Barrion 2004, Williams and Diop 1981, Abdou 1992, Dingkuhn 1992).

Figure 4.11 Bemisia tabaci (Source: David Riley; Centre for Invasive Species and Ecosystem Health, University of Georgia, USA (https://www.bugwood.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Host plants other than rice: Alternate host plants of A. indicus in West Africa have not been reported. However, reports of the grasses Chloris barbata Swartz and Dactyloctenium aegyptium (L.) Willdenow as being host plants in India indicate that grass species in West Africa are most likely hosts as well. Alternate hosts in China are Zea mays L., Saccharum officinarum L. and 13 Poaceae species (Fu Minglong et al. 2000). Description and biology: Whiteflies are minute insects measuring 2–3 mm in length as adults (Borror et al. 1981). The adults resemble tiny white moths with their wings covered by a white dust or waxy powder (Fig. 4.11). Adults are active and readily fly from leaves of rice when disturbed. Eggs are laid on the plant. Metamorphosis of whiteflies differs from that of other members of the suborder Homoptera. The first instars are active, but subsequent instars are sessile and have the appearance of scales. The scale-like covering is a waxy secretion of the insect. The early instars are called larvae. The next to the last instar is quiescent and is called a pseudopupa. Details on the biology of A. indicus in rice in West Africa have not been published. Plant damage and ecology: Aleurocybotus indicus was first reported on rice in Senegal in 1977. The whitefly is a dry season insect. High temperatures and low humidity favour its build-up. The whitefly occurs on the plant from the seedling to the maturity stage (Alam 1984) and damages plants by sucking sap from the leaves. Whiteflies feed by tapping into the phloem of plants, introducing toxic saliva and decreasing the plants' overall turgor pressure. Since whiteflies congregate in large numbers, susceptible plants can be quickly overwhelmed. Further harm is done by mould growth encouraged by the honeydew whiteflies secrete (https://en.wikipedia.org/wiki/ Whitefly). Honeydew, which is excreted on the leaves by the feeding nymphs and adults, has a high sugar content, and a black sooty mould fungus grows on it. Extensive feeding and high amounts of sooty mould may eventually lead to wilting and death of the plants (Alam 1989). Aleurocybotus indicus is considered a major pest at Fanaye and Ndiaye, Senegal, and in Niger where yield losses attributed to this pest have reached 80% (Abdou 1992). Total destruction of the rice crop at Fanaye, Senegal, was reported during the 1982-83 season (Akinsola and Coly 1984). Whiteflies are rice pests in the Guinean and Sudanian savannas but not in the humid tropical (forest) zone of West Africa. They occur in the irrigated Sahel and the mangrove swamp areas, but are not found in the upland and inland swamp areas of the continuum toposequence (Heinrichs and Barrion 2004).

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4.8 Rice whitefly, Aleurocybotus occiduus Maria (Hemiptera: Aleyrodidae) Distribution: Nepal, the United States, Peru, Mexico and El Salvador. Host plants other than rice: Similar to that of Aleurocybotus indicus this species feeds on numerous cereal crops and was first recorded in Mexico in 2009 (Vejar Cota et al. 2009). Description and biology: Aleurocybotus occiduus is a polyphagous, tiny insect of 1-1.5 mm in size. Adults have two pairs of white wings with prominently longer hindwings. These migratory adults lay up to 120 eggs, which are sub-elliptical in shape, light yellow in colour and are laid singly or in groups of up to 20 on the under surface of the leaves and succulent stems (Pokhrel and Thapa 2011), although sometimes, when abundant, they are found in the sheath (Vejar Cota et al. 2009). Nymphs hatch in 3-7 days and go through four instars, which are stationary. The stationary nymphs, which suck the plant sap from stems and leaves, are the most harmful stage. The last instar nymph is commonly called a ‘pupa’. Pupation ends in 2-8 days. The total life cycle from egg to adult is 14-120 days (Pokhrel and Thapa 2011). Plant damage and ecology: The whitefly occurs on the plant from the seedling to the maturity stage and damages plants by sucking sap from the leaves. Pokhrel and Thapa (2011) reported on an outbreak on main season rice in Chitwan Valley, Nepal, in 2003, which affected a total of 20,601 ha (severely 177 ha, medium 2,787 ha, low 6,945 ha and mild 10,692 ha) land, causing a loss of 9,448 mt in rice yield. In the 2003 outbreak in Nepal a population of up to 1,000 whitefly nymphs/tiller was counted (Pokhrel and Thapa 2011). Damaged plants took on a reddish yellow appearance, which extensionists confused with a nutritional deficiency and bacterial blight. A. occiduus feeding proportionally decreased the tiller number/hill, fertile tillers/hill, grain weight/ panicle and the grain yield/ha. Rice plants infested with a high population of the whitefly (898/tiller) failed to produce grain, whereas a medium population (335/tiller) produced 1287 kg and a low population (103/tiller) produced 3456 kg /ha (30.8% less than the previous year). Use of monoculture, susceptible varieties (Sabitri) and improper cultural operations; excess use of agrochemicals; and unawareness of the population build-up of the pest were suggested to be causes of the outbreak (Pokhrel and Thapa 2011).

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4.9 Spider mites, Oligonychus pratensis Banks, O. senegalensis Gutierrez and Etienne, O. oryzae Hirst and Tetranychus neocaledonicus Andre (Acari: Tetranychidae) Distribution: O. pratensis – A widely distributed species occurring in West Africa; North, Central and South America; Hawaii; Madagascar; and South Africa (Heinrichs and Barrion 2004); O. senegalensis – Senegal (Gutierrez and Etienne 1981a); O. oryzae – India (Radhakrishnan and Ramaraju 2009); Tetranychus neocaledonicus – West Africa (Heinrichs and Barrion 2004), Canary Islands (Pande and Hernandez 1989), Madagascar (Gutierrez and Chazeau 1973) and India (Bharodia and Talati 1976). Host plants other than rice: The spider mite species have different host plants. Oligonychus pratensis and T. neocaledonicus have a wide host range. Oligonychus pratensis feeds on maize, sugarcane, sorghum and wheat, in addition to rice (Gutierrez and Etienne 1981b). It is a pest of cereals in the southern United States and also feeds on pasture and ornamental grasses, such as Bermuda grass, and on weeds (Jeppson et al. 1975). T. neocaledonicus is a polyphagous species and has been reported on 59 botanical families in Madagascar alone (Gutierrez and Etienne 1981b). Oligonychus senegalensis has only been reported

Figure 4.12 Oligonychus pratensis (Source: Jim Kalisch, Dept of Entomology, University of NebraskaLincoln, USA). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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as a pest of rice in Senegal (Gutierrez and Etienne 1981b) and O. oryzae is a pest of rice in India. Description and biology: Radhakrishnan and Ramaraju (2009) have described the biology of O. oyzae in India. Eggs of O. oryzae are minute, spherical or globular in shape and pale whitish yellow. Eggs are deposited on the lower surface of the leaves. Freshly laid eggs are colourless or clear and later turn pale yellow. The incubation periods were significantly different among the temperatures tested. The longest incubation period was 6.3±0.52 days at 20 °C, whereas only 2.58 and 2.61 days were required at 30 and 35 °C, respectively. The newly hatched larva are white with four dark spots. The larvae were active for 2.3– 3.3 days prior to entering the protonymph stage. There was a significant difference in larval development times depending on temperature. At 30°C the development time of protonymph and deutonymph was 1.6 and 1.9 days, respectively. Total life cycle lasted for 8.35 days at 30°C. The adult females were light greyish brown with four prominent dark black spots on the dorsal side and lived for 8.8 days. Males were slightly pinkish and also lived for 8.8 days at 30°C. High temperatures are favourable for the multiplication of this mite. Plant damage and ecology: Leaf-feeding spider mites of the Tetranychidae family are severe pests feeding on the rice crop at all growth stages. Oligonychus oryzae (Hirst), a rice pest in India, begins feeding on plants in the nursery and continues feeding on transplanted seedlings in the field (Jeppson et al. 1975). Oligonychus pratensis (Fig. 4.12) populations are concentrated along the central vein and at the base of the rice leaf (Gutierrez and Etienne 1981b). Mites suck sap from the parenchymatous cells of the leaves and produce large masses of webbing on the leaves. They often feed on the under surface of the leaves. Leaves become discoloured with white patches and dry up starting from the leaf tip. Plants become stunted with deformed panicles and empty spikelets (Heinrichs and Barrion 2004). In seasonal occurrence studies in the Casamance at Djibelor, Senegal, O. pratensis and T. neocaledonicus were collected on rice during the dry season in March and O. senegalensis was collected on rice in March, June and October (Gutierrez and Etienne 1981b). Spider mites generally occur within the same rice ecosystem as the whiteflies. They have pest status in the irrigated Sahel ecosystem but not in the mangrove swamps or the upland/inland swamp continuum (Heinrichs and Barrion 2004). The spider mites are more important constraints to rice production in the Sahel than are the whiteflies.

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4.10 Rice thrips, Stenchaetothrips biformis (Bagnall) (Thysanoptera: Thripidae) Distribution: Afghanistan, Bangladesh, Bhutan, Cambodia, China, Europe, India, Indonesia, Japan, Republic of Korea, Laos, Malaysia, Myanmar, Nepal, Papua New Guinea, Philippines, South America, Sri Lanka, Taiwan, Thailand, Vietnam (Dale 1994). Host plants other than rice: Agropyron kamojo Ohwi, Alopecurus aequalis Sobol., Arundinella hirta Tanaka, Cyperus iria L., Cyperus rotundus L., Digitaria ciliaris (Retz.) Koel., Echinochloa colona (L.) Link, Echinochloa crus-galli (L.) Beauv., Eragrostis ferruginea Beauv., Festuca parvigluma Steud., Imperata cylindrica (L.) Raeuschel. Leersia japonica Honda, Panicum repens L., Paspalum scrobiculatum L., Pennisetum japonicum Trinius, Phragmites australis (Cav.) Trin. ex Steud., Zea mays L., Zoysia japonica Steud. (Dale 1994). Description and biology: Adult thrips (Fig. 4.13) are minute elongate insects, about 1 mm long, brown to dark brown and with pronounced seven-jointed antennae (Dale 1994). Pronotum with two pairs of long posteroangular setae. They can be either winged or apterous. Wings when present are long, narrow and fringed with fine hairs and lie along the insects’ backs (dorsum) when they are at rest. At the base of the forewing is a light spot. The males, which are smaller and more slender than the females, are seldom observed. Reproduction is believed to be parthenogenetic. Adults are day-flying insects and are not attracted to light. Despite their small size and fragile appearance, thrips can travel long distances. They migrate during the day and seek out newly planted rice fields

Figure 4.13 Stenchaetothrips biformis female (Source: not known). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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or other grassy hosts. But they prefer to confine themselves to rolled leaves most of the time (Nugaliyadde and Heinrichs 1984). Adult thrips live for about 20 days. Eggs are reniform and are inserted singly in tissues of the youngest leaves on the side facing the stem (Reissig et al. 1986). They are hyaline when laid but turn pale yellow as they mature. A female lays about 25 eggs in its lifetime. Eggs hatch after 3 days. The newly hatched larvae are almost transparent, but they turn yellowish white after the first moult. The legs, head and antennae are darker. After a brief resting period, the larvae start feeding actively on leaves and on the basal parts of the leaf sheath. If young rice plants are not available, the thrips may even feed on rice flowers. The larvae remain on the same plant in which they hatched. There are three larval instars which last for a total of 6 to 8 days. The pre-pupae are usually seen in groups. Pupation takes place inside rolled leaves. At this stage, the appendages are clearly visible and the wings reach up to the fourth abdominal segment. Pre-pupal and pupal stages together last for 3–4 days. In China, the thrips have 10 generations a year. The threshold temperature for temperate regions is 11.5 ± 12°C; the optimum temperature for development ranges from 15 to 25°C. Adults of the overwintering generation emerge in the middle of April and lay eggs on weeds. During the early half of May, adults of the second generation invade the fields and infest rice plants. Maximum crop damage, however, is caused by the second and fourth generations from the middle of May to the middle of July. The peak population is attained in the middle of June. Seasonal abundance in tropical countries is slightly different probably due to the change in seasons and planting times. In northern India, the thrips appear on rice plants in the first week of August. The population reaches its peak by the third week and declines thereafter. The crop that is planted in early July has less infestation compared to that planted in late July or early August. Older plants, particularly those at 30 days after transplanting, have very low populations (Senapati and Satpathy 1982). Nugaliyadde and Heinrichs (1984) studied the effects of plant age, adult density and temperature on fecundity and population growth of the rice thrips. Plant age did not influence female longevity. However, male longevity was significantly less on the twoleaf-stage plants than on the six-leaf-stage plants. Daily mean fecundity was significantly higher on rice seedlings at the third, fourth and fifth leaf stages than on seedlings at the first, second or sixth leaf stages. Females on plants with low population density levels produced significantly more progeny. The total progeny produced per female over 14 days of the early reproductive period was not affected by the temperatures tested in the study (23, 26, 29 and 32°C). Plant damage and ecology: Stenchaetothrips biformis is a sporadic pest of rice infesting mostly young plants. It can damage large areas of paddy fields within a few days because it builds up high populations due to a comparatively short life cycle. The pest infests both upland and wetland rice crops. In years of a delayed monsoon or low rainfall during June– July, severe outbreaks of rice thrips have often been reported from India (Mammen and Nair 1977, Nath and Sen 1978, Velusamy and Chelliah 1980, Gubbiah 1984), Bangladesh (Husain 1982) and China (Zu-yin et al. 1978). Larvae and adults have rasping mouthparts that lacerate the green tissue of leaves. They have only one mandible that is used to puncture leaf tissue. The maxillae and mouth cone, which form a tube, are used to suck leaf sap. Young plants, usually of 1 to 2 weeks after transplanting (WAT), are the most affected. Damage becomes evident as fine yellowish lines or silvery streaks on the leaves which later curl from the margin towards the midrib.

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The lower leaves are often killed. In severe infestations, the plants become stunted and wither. However, the plants that survive early infestation usually recover and are able to bear normal grains. Cheng (1983) studied the yield loss in rice caused by the rice thrips, Stenchaetothrips biformis, in Xishui Prefecture, Hubei, China, where this pest increased in importance. Yield was significantly correlated with the level of infestation. It was estimated that an increase of 1 insect/plant decreased yield by 98.93 kg/ha, and an increase of 1% in the number of thrips-induced leaf rolls decreased the yield by 36.56 kg/ha. Thrips are normally abundant during the dry season, when there is little or no rainfall. Therefore, plants that are transplanted preceding the rains become the main target of thrips attack. Prolonged rainy periods and heavy rains reduce the pest population (Zu-yin et al. 1978). The outbreak of thrips in Bangladesh in 1982 was attributed to a long winter followed by a summer drought (Husain 1982).

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4.11 Rice leaffolder, Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae) Distribution: Afghanistan, Australia, Bangladesh, Bhutan, Brunei, Cambodia, China, India, Indonesia, Japan, Korea (DPR and R), Laos, Madagascar, Malaysia, Myanmar, Nepal, Pakistan, Papua New Guinea, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam (Dale 1994). Host plants other than rice: Brachiaria mutica (Forssk.) Stapf, Echinochloa colona (L.) Link, Eleusine coracana (L.) Gaertn., Isachne dispar Trin., Leersia hexandra Sw., Pennisetum pedicellatum Trin., Saccharum officinarum L., Sorghum bicolor (L.) Moench., Triticum aestivum L., Zea mays L. (Dale 1994). Description and biology: Adult moths (Fig. 4.14) are yellowish brown in colour, small and 10 to 12 mm long with a wing expanse of 13 to 15 mm. The wings take the shape of an equal-sided triangle when at rest. The forewings have three dark oblique lines of varying lengths. The hindwings have a broad anal area. The tibiae are tufted with black hairs which are prominent in the male, but not in the female. The tip of the abdomen is blunt in the male, but pointed in the female (Lingappa 1972). The female attracts its mate with a pheromone and generally mates between dusk and midnight. Adults hide on the host plants during the day to escape predation by buds and only take short flights when disturbed. Adult longevity is about a week. Moths are nocturnal and in the daytime, they are usually seen resting on the under surface of leaves and on stems. During the early morning hours, moths are often active,

Figure 4.14 Cnaphalocrocis medinalis adult (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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but their activity diminishes as the sun increases in severity. The attraction of moths to light is rather poor. Adult feeding influences the fecundity and subsequent population build-up of the pest. The female moths require an exogenous source of sugar for the production of eggs. The increase in fecundity under laboratory conditions resulting from the utilization of hopperexcreted honeydew indicates that adult moths can use honeydew as a source of sugar in rice fields (Waldbauer et al. 1980). Egg laying starts one or two days after mating. Flat, oval and whitish yellow eggs are laid singly or in rows, parallel to a midrib on both surfaces of young leaves and rarely on stems (Fig. 4.15). The eggs are laid in batches of 10 to 12, the biggest batches being laid on the fourth to seventh nights after the emergence of moths. Each female moth may lay about 300 eggs during its lifetime. The incubation period varies from 3 to 6 days (Heinrichs and Barrion 2004). The newly hatched larva is white, translucent with a light brown head. The body, however, turns green once the larva starts feeding. After hatching, it crawls to the base of the youngest unopened leaf and begins to feed. The second instar migrates to an older leaf and folds the leaf together. Some of the newly hatched larvae suspend themselves by silken threads from the leaf tip and disperse to other plants by wind (Velusamy and Subramaniam 1974). Mostly, only one larva (Fig. 4.16) is found in a leaf fold (Yadava et al. 1972). Leaf tubes are generally made by folding a single leaf but cases are also observed where two or three leaves are used for making one fold. There are generally five larval instars in tropical countries. The frequency of larval moulting is affected more

Figure 4.15 Cnaphalocrocis medinalis eggs (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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by the growth stage of the rice plant than by the temperature in temperate regions (Wada 1979). Details regarding the mode of construction of leaf folds by larvae have been reported by Ramasubbaiah et al. (1980) and Fraenkel and Fallil (l981). The larva selects a point on a leaf about 15 cm from the tip and lines the surface for about 6 cm with a salivary secretion as flooring for the leaf fold. Then the larva swings its head in quick succession between two opposite leaf margins, affixing a silk thread at each touch down (Fig. 4.16). The tiny threads from about 100 such movements fuse together to a firm band which on drying contracts. About ten to 25 such bands are produced on a leaf at a distance of a few millimetres. The entire process requires about 45 minutes, the larva resting several times during the period. The nature of the folds depends on the age of the crop (Rajamma and Das 1969). In rice seedlings and young plants, 3 to 4 leaves of adjacent plants are webbed together longitudinally to make a tubular fold. In the more mature plants, folds are made out of single leaves that are folded either longitudinally or rarely transversely. Only fully grown larvae make a transverse leaf roll. In the earhead stage, the larvae make a shelter by webbing together the bootleaf and the earhead. The full-grown larva is about 16 mm long and 1.7 mm wide across the thorax. It is yellowish green in colour with a dark brown head and prothoracic shield. Mature larvae jump or wiggle rapidly when touched. The larval period lasts for 15 to 25 days. Pupation takes place inside the leaf roll in loosely woven strands of silk. The newly formed pupa is slender and greenish brown and later turns brown. The moth emerges after 6 to 8 days.

Figure 4.16 Cnaphalocrocis medinalis larva (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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In Japan, overwintering has only been confirmed in subtropical Okinawa (Miyahara 1981). As the insect does not hibernate, low temperature in winter affects overwintering survival. Both eggs and larvae cannot survive winter in temperate Japan (Sato and Kishino 1978). The leaffolder moths have been recorded in tropical countries throughout the year, although they are most abundant during the wet season. In countries such as Japan, with a cold winter, moths are first seen in the paddy field in mid-June (Wada et al. 1980). Then their population gradually increases until late August after which the larval density decreases and very few eggs are seen on rice leaves. At the end of the season, the generations overlap each other as indicated by the various instars seen in a field at the same time. C. medinalis moths migrate long distances. In 1977, many moths were captured on a vessel in the East China Sea far from land (Kisimoto 1978). During migration, most of the female moths remain unmated and once they settle on rice plants, they immediately mate and start laying eggs (Miyahara 1980). The insect is believed to take the same migration route from China to Japan and Korea as the planthoppers Sogatella and Nilaparvata do (Miyahara 1981). Plant damage and ecology: The rice leaffolder, Cnaphalocrocis medinalis, earlier considered as a minor and sporadic pest of rice in many Asian countries, appears to have become increasingly important with the spread of high-yielding rice varieties and accompanying changes in cultural practices. Misuse of insecticides and excessive use of nitrogenous fertilizers have been cited as the cause for high leaffolder populations (Dhaliwal et al. 1979). Outbreaks have been reported from India (Yadava et al. 1972, Chatterjee 1979), southern Japan (Hirao 1981) and Vietnam (Bautista et al. 1984). Infestation usually occurs during late growth stages of the rice crop. The larvae fold the leaves and scrape the green tissues of the leaves from within and cause scorching and leaf drying. Each larva is capable of destroying several leaves by its feeding. Under heavy infestation, each rice plant may have several rolled leaves, which severely restricts its photosynthetic activity. When plants are attacked in the bootleaf stage, grains are partially filled. A close correlation between the intensity of leaffolder attack and loss in grain yield very often exists (Upadhyay et al. 1975). Bautista et al. (1984) have clearly shown that yield loss due to rice leaffolder is positively related to the percentage of damaged leaves. In their studies, yield was significantly decreased at 17.5% damaged leaves, resulting in 16.5% yield loss, and a 21.3% yield loss occurred with 26.6% damaged leaves. Sellamal Murugesan and Chelliah (1983) reported that a 10% increase in flag leaf damage by the leaffolder reduces grain yield by 0.13 g per tiller and the number of fully filled grains by 4.5%. However, rice plants sometimes compensate for flag leaf damage by increasing the photosynthesis rate of the leaf adjacent to the flag leaf (Derui 1984). Leaf feeding also predisposes the plants to fungal and bacterial infections. High humidity and optimum temperatures are conducive ecological factors for the rapid multiplication of the leaffolder (Pathak 1975). The threshold temperatures of development for egg, larva and pupa are 12.5, 12.2 and 14.2°C, respectively (Wada and Kobayashi 1980). There are many other factors that play a role in the development and population increase of the rice leaffolder. It has been shown by Hanifa et al. (1974) that silica in host plants plays an important role in the feeding activity of leaffolder larvae. Arrangement of silica chains in the leaf varies in resistant and susceptible cultivars. Closer silica chains, high

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epidermal silica deposition, heavy deposition of silica in the intercostal area and single or double rows of silica in resistant varieties provide a sufficient mechanical barrier to the feeding by caterpillars. There are varying reports on the effect of nitrogenous fertilizers on rice leaffolder incidence. Many workers (Regupathy and Subramanian 1972, Michael Raj and Morachan 1973, Subbaia and Morachan 1974, Chandramohan and Jayaraj 1977, Upadhyay et al. 1981) have shown that the incidence of leaffolder is positively correlated to the level of nitrogenous fertilizers. A combined application of high doses of N, P and K has been shown to alter the mineral metabolism of rice plants in favour of leaffolder development and multiplication (Regupathy and Subramanian 1972). However, when K was applied alone, leaffolder infestation was significantly reduced (Subramanian and Balasubramanian 1976). It is interesting to note that the damage is more severe in shady areas particularly near the levees (Velusamy and Subramaniam 1974). Close crop growth consequent to heavy manuring is also conducive for leaffolder activity.

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4.12 Rice leaffolder, Marasmia patnalis (Bradley) (Lepidoptera: Pyralidae) Two Marasmia species, M. patnalis (Bradley) and M. ruralis (Walker) attack rice. The habits and the biology of these two species are very similar to those of Cnaphalocrocis medinalis. Distribution: India, Indonesia, Malaysia, Philippines, Sri Lanka (CABI 2016b). Host plants other than rice: Three Cyperaceae andb 15 Poaceae species (CABI 2016b). Description and biology: The adult M. patnalis moth is similar in appearance to that of C. medinalis. However, it has three long, dark bands on the forewings (middle one is broken) (Fig. 4.17), while C. medinalis has two long and one short band (Fig. 4.14). Forewings are pale yellow with a greyish marginal band. Hindwings are also pale yellow but whitish basally. The male moth is readily distinguished by the presence of a prominent patch of dark brown and shining conical scales at the middle of the forewing costa. The larva differs from that of C. medinalis in that the apex of the pronotum is angulated while it is straight in M. patnalis and has two pairs of subdorsal spots on the mesonotum whereas C. medinalis (Fig. 4.16) has one pair. The life cycle of M. patnalis was studied in the Philippines by Joshi et al. (1985). Eggs are laid singly or in groups of 2 to 9 on the upper side of the leaves, but sometimes eggs are also seen on leaf sheath. The incubation period is 4 days. First instar larvae scrape the leaf surface. The second instar larvae fold leaves and start feeding from within. The larval period is about 23 days. The pupal period is 9 days and takes place within a silken cocoon, most commonly between leaves that have been stitched together. Adult emergence takes place at night. Plant damage and ecology: Marasmia patnalis was reported as a pest of rice in Southeast Asia in 1981 (Bradley 1981). The species is shade-loving and is considered as a major pest of rice in Sri Lanka. Damage is similar to that described for Cnaphalocrocis medinalis. The

Figure 4.17 Marasmia patnalis adult (Source: IRRI).

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removal of leaf tissue by a larva feeding within a feeding chamber causes longitudinal white, transparent streaks on the leaf blade. Each blade may contain several feeding streaks. When infestations are high each plant may contain many folded leaves. Heavily damaged leaves become dry and highly infested fields appear scorched. Yield loss can be high when many flag leaves are damaged (Reissig et al. 1986).

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4.13 Fijian rice leaffolder, Susumia exigua (Butler) (Lepidoptera: Pyralidae) Distribution: Asia – Bangladesh, Burma, Cambodia, China, India, Indonesia, Japan, Korea, Pakistan, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam; Australasia and Pacific Islands – Caroline Islands, Fiji, Mariana Islands, Marquesas, New Caledonia, Papua New Guinea, Samoa, American, Western Society Islands, Solomon Islands, Irian Jaya (CABI 2016c). Host plants other than rice: Zea mays L., Brachiaria spp., Coix spp. Description and biology: The adult S. exigua moth is about 7 mm long with a wingspan of 13 mm and three bands on the forewings with the central band longer than the other two (Fig. 4.18). Its forewings have light yellow and brown markings. The gravid female moths prefer to lay eggs on the green parts of tall rice plants. Eggs are laid overlapping one another, in a row parallel to the midrib of the leaf. The eggs in a cluster average 3 but may be as high as 11. They are flat and translucent. The incubation period is about 5 days (Dale 1994). The newly hatched larvae tend to be gregarious for some time and then start feeding on the leaves. The second instars draw the leaf margins together and stitch them with contractile silk. Both ends of the leaf roll are left open. The larva feeds on the green tissue leaving conspicuous white scars on the leaf blade. There are six larval instars and development takes approximately 4 weeks. The larva differs from that of C. medinalis in that the apex of the pronotum is convex while it is straight in C. medinalis and has no spots on the mesonotum, whereas C. medinalis has one pair of subdorsal spots. Pupation takes place within the leaf roll. The pupa is not enclosed in a cocoon but is surrounded with silken frass and faecal plugs, Pupae are 8 mm long and 1.7 mm wide. The pupal period is about 9 days (Hinckley 1963). The insect is most abundant in Fiji during April and May. Plant damage and ecology: Damage is similar to that described for Cnaphalocrocis medinalis. The removal of leaf tissue by a larva feeding within a feeding chamber causes longitudinal white and transparent streaks on the leaf blade. Each blade may contain several feeding streaks. When infestations are high each plant may contain many folded leaves. Heavily damaged leaves become dry and highly infested fields appear scorched. Yield loss can be high when many flag leaves are damaged (Reissig et al. 1986).

Figure 4.18 Susumia exigua adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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4.14 Rice caseworm, Nymphula depunctalis (Guenée) (Lepidoptera: Pyralidae) Distribution: Argentina, Bangladesh, Bhutan, Brazil, Burma, China, Gambia, Ghana, India, Indonesia, Kampuchea, Laos, Madagascar, Malaysia, Malawi, Mauritius, Mozambique, Nepal, Nigeria, Papua New Guinea, Philippines, Sri Lanka, Taiwan, Uruguay, Venezuela, Vietnam, Zaire (Dale 1994). Host plants other than rice: Brachiaria murica (Forssk.) Stapf, Brachiaria ramosa (L.) Stapf, Cynodon dactylon (L.) Pers., Cyperus iria L., Cyperus rotundus L., Cyrtococcum patens (L.) A. Camus, Echinochloa colona (L.) Link, Isachne dispar Trin., Leersia hexandra Sw., Panicum repens L., Paspalum conjugatum Berg. (Dale 1994). Description and biology: Many workers have studied the bionomics of the rice caseworm in India (Srivastava et al. 1970, Kittur and Chauhan 1974, Viraktamath et al. 1974, Pillai and Nair 1979) and in the Philippines (Sison 1938). Moths are nocturnal in habit and are attracted to light. They are delicate, white with fuscous markings and black specks on wings (Fig. 4.19). Female moths are larger than the males. Mating mostly takes place during the night; egg laying occurs the next night. Usually all the eggs are laid during a single night. Each female lays about 60 eggs and may die 2–3 days after oviposition. The male moths live for 4-5 days. The freshly laid eggs are light yellow, smooth and spherical and 0.5 mm in diameter (Islam and Catling 2012). They are laid in batches of about 20 on the underside of leaves

Figure 4.19 Nymphula depunctalis adult (Source: Semi Lapiz/Alberto Barrion, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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floating on the water. The eggs turn dark yellow as they mature. The incubation period lasts for 4 days. Larvae are transparent green in colour with light brownish orange heads. The first instar larva starts feeding on the green tissues by scraping the leaf surface. It then moves to the leaf tip and cuts a slit on the margin at a point 2 - 3 cm below the tip and makes a fold. Then the larva makes another cut about 1 cm below the first and rolls the margin with silk to form a tubular case. The inside of the case is lined with silk to hold a thin film of water, which is essential for both respiration and preventing desiccation of the larva. A new case is constructed after every larval moult. The case, which is carried along by the caterpillar whenever it moves, helps the larva to float on the water surface. During the daytime, larvae hide in cases while at night they crawl up rice plants and feed with their head and legs protruding from the case.  Feeding is reduced under dry conditions and the presence of water droplets on the leaves is helpful for larval feeding. Larvae are 20 mm long when fully grown, and are semi-aquatic in habit with lateral, slender, filamentous gills. The larval stage lasts for 15–30 days. Pupation takes place inside the larval case with both ends closed and attached to the rice stem just above the water level. The case has an inner silk lining with a slit-like opening at the anterior end. The fresh pupa is milky white which gradually changes to light yellow. The adult moth emerges in 4–7 days. In South India, moth populations reach two peaks, one during November–December and another in May–June. These peaks coincide with periods of high rainfall and high humidity. Variations in temperature do not appear to be correlated with pest populations (Pillai and Nair 1979). In northern India, the infestation is more severe in the months of August–November (Srivastava et al. 1970).  The insect occurs in overlapping generations and does not hibernate. N. nympheata, commonly called China mark moth, is a related species of N. depunctalis, distributed mainly in Italy and Hungary. Five generations occur per year in Italy, the first being the most important as it attacks very young plants. A smaller rice caseworm, N. vittalis Bremir has been reported from Japan, Korea, Manchuria and USSR. The larvae typically fold leaves of the plant and feed from within (Dale 1994). Plant damage and ecology: The rice caseworm is a major pest in Southeast Asia, and parts of Africa and South America. It was first recorded in rice in India in 1917 (Islam and Catling 2012). Damage is caused by larvae cutting off the leaf tips for making the characteristic leaf cases and by the removal of the green tissue. Defoliation occurs in rice plants before the maximum tillering stage. Plants that have recently been transplanted are preferred but the larvae may infest the nursery. It does not occur after maximum tillering. Larvae scrape the leaf tissues, leaving only the papery upper epidermis (Heinrichs and Viajante 1987). Generally, several larvae attack the same rice plant and cut off most of the leaf tips for constructing larval cases and scrape the remaining leaves. Caseworm damage can be distinguished from that of other pests by the ladder-like appearance of the removed leaf tissue, resulting from the back-and-forth motion of the head during feeding.  Also, the pattern of damage in the field is not uniform because the larvae in the cases are carried to one side of the paddy by winds or water currents.  Attacked plants often become stunted. A grain yield loss of 10% was reported when either 30% of the leaves were cut by larvae or 25% of the leaf area was scraped in the first month after transplanting (Islam and Catling 2012). Damage occurs in patches and

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when damaged patches are not replanted severe weed infestations occur, resulting in further losses. Nymphula depunctalis is an important pest of irrigated and rainfed wetland rice in the Orient. Even though rice is its preferred host plant, the insect infests various other grasses as well. The pest occurs regularly in low populations, but sporadic increases in population result in intense defoliation of plants. An extensive outbreak occurred in Kerala, South India, in 1968 (Joseph 1969). The infestation is most severe on dwarf, compact, heavytillering, high-yielding varieties (Kittur and Chauhan 1974). Nitrogen has an effect on the population and damage caused by N. depunctalis. In a study conducted in Bangladesh the highest infestation was observed from the plots treated with 190 kg urea ha-1 and the minimum from plots with 130 kg urea ha-1 (Das et al. 2001).

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4.15 Green horned caterpillar, Melanitis leda ismene Cramer (Lepidoptera: Satyridae) Distribution: Asia – Bangladesh, Bhutan, Cambodia, China, India, Japan, Korea (Republic of), Laos, Malaysia, Myanmar, Nepal, Pakistan, Philippines, Sri Lanka, Thailand, Vietnam; Africa – Kenya, Mauritius; Oceania – Australia, (CABI 2016d). Host plants other than rice: Wide range of hosts including species of Anacardiaceae, Araceae, Bombacaceae, Bromeliaceae, Cucurbitaceae, Dioscoreaceae, Euphorbiaceae, Fabaceae, Musaceae, Myrtaceae, Poaceae, Sapindaceae and Sterculiaceae (CABI 2016d). Description and biology: The adult is a large, dark brown butterfly, measuring about 7.5 cm across expanded wings and with a body 2.2 cm long. There are two large, round spots on the upper surface of the forewings. The underside is ochreous brown with dark transverse stripes and target-like spots (Fig. 4.20); hindwings have six prominent spots on their ventral side. The wings are folded above the body when the insect is at rest. It flies at dusk, making darting movements among the rice plants (Dale 1994). Pearl-like eggs are laid singly or in rows on rice leaves and are 1 mm in diameter. Each female lays 50-100 eggs in a lifetime of about 2 weeks. They hatch in about 4 days. The yellowish green larva blends into the rice foliage, and is difficult to identify, in spite of its large size. The body is covered with small, yellow bead-like hairs (Fig. 4.21). The head (Fig. 4.22) is flat and quadrangular with a pair of brown horns; at the posterior extremity of the body are two slender processes. Pupation takes place on the rice leaf.

Figure 4.20 Melanitis leda ismene adult (Source: © Khew Sin Khoon). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.21 Melanitis leda ismene larva (Source: Clive Lau).

Figure 4.22 Melanitis leda ismene larva head view (Source: Rundstedt Rovillos; www.flickr.com).

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The pupa is dark green, smooth and hangs by its anal extremity from the leaf. The pupal period lasts for 10 days. In Bangladesh, the pest is observed to reach its peak population during October (Alam 1974). Plant damage and ecology: Melanitis leda ismene is a minor pest of rice. The caterpillars feed on the margins and tips of leaves and remove leaf tissue and veins. Damage in similar to that of grasshoppers and armyworms. The pest occurs in all rice environments but is more prevalent in rainfed areas. Deep-water rice in Bangladesh is also often infested by this insect (Alam 1974).

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4.16 Rice skipper, Parnara guttata (Bremer et Grey) (Lepidoptera: Hesperidiae) Parnara gutatta and Pelopidas mathias (F.) are the most common rice field species of the day-flying skippers. Distribution: Bangladesh, Cambodia, China, India, Indonesia, Japan, Korea, Laos, Malaysia, Pakistan, Philippines, Taiwan, Thailand, Vietnam (Dale 1994). Host plants other than rice: Carex olivacea Boott. and Phragmites communis Trin. (Dale 1994). Description and biology: Adult butterflies are olive brown and 10 to 15 mm long with a wingspan of 20–44 mm. There are 4–9 small whitish specks on the forewings and similar spots, 2 to 4 in number, on the hindwings (Fig. 4.23). The butterflies are swift fliers being active only during the day. The white spherical eggs are glued singly on leaf blades by the female moths. The eggs hatch in 3-4 days. Larvae rest at the base of the plants during the day and feed on leaf blades at night. The full-grown caterpillar is pale green, and has a dark head with a W-shaped black mark on the rear. The mature larvae often move from one rice plant to adjacent plants. There are 5 larval instars in Taiwan, but the fifth instar larvae moult once more in Japan (Ishii 1980). The larval period is about a month. Pupation takes place inside the leaf tubes. The light brown or light green pupa rests in a pad of silk and has a pointed end, which is attached to the folded leaf. Adults emerge after 8 to 10 days.

Figure 4.23 Parnara guttata adult (Source: Yunhyok Choi; www.flickr.com). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Skipper butterflies exhibit adult polymorphism. Hasegawa (1975) has reported that the species has two seasonal forms; the yellowish brown ‘summer form’ and the dark brown ‘autumn form’. Temperature and photoperiod conditions prevailing during the larval stage mostly determine the morphological characters of the adult butterfly. A long photoperiod induces pale wing colouration and small size of adults. But low temperature induces larger size, stronger melanization and more conspicuous spots on the wings (Ishii and Hidaka 1979). The ecological factors such as photoperiod and temperature may also affect the physiology of the migrating butterflies. Females reared under 14-hour photoperiod, which corresponds to the migratory adults in early autumn, have higher flight capacity, lower fecundity and a longer pre-ovipositional period than those under a 16-hour photoperiod, which corresponds to the non-migratory adults in summer (Ono and Nakasuji 1980). Parnara guttata is well known as a migrant butterfly in central and western Japan. Second-generation butterflies fly en masse to the warmer southwest in early autumn for hibernation. Eggs of the third generation are laid on grasses and the larvae develop on those grasses in autumn (Nakasuji et al. 1981). Average migration distance is less than 100 km (Nakasuji and Ishii 1983). However, some of the migrants fly more than 500 km over the Pacific Ocean (Asahina and Turuoka 1969) and may thus reach the southwest islands of Japan or even Taiwan. Plant damage and ecology: The rice skipper, P. gutatta, is the most dominant species among the rice skippers in Japan and China (Masuzawa et al. 1983). It is one of the major pests of rice in China (Chiang 1977) and outbreaks of the pest often occur in the paddy fields of central and western Japan. It occurs in all rice environments, but is mostly a pest of irrigated rice. The caterpillars feed on leaves from the margins inwards and then parallel to the midrib, which is often left uneaten. In addition, the larvae tie, with silken threads, the two edges of the same leaf or two adjacent leaves together to form a tube in which they live. Damage is severe in young transplanted rice seedlings and the attack may continue until the plants mature. In severe cases, the plants do not recover. Grain quality is adversely affected by the pest. In Iksan, Korea, P. guttata have three generations per year. Adults of the first-generation emerged mid- to late May from pupae that developed from overwintered larvae in weeds on banks around rice fields or on hillsides. On emergence, the adults moved to rice fields to lay eggs on rice leaves. The damage to rice by the second-generation larvae began to increase in late July and reached a peak from mid- to late August. There was a significant relationship between the transplanting time and the occurrence of P. guttata in rice fields. P. guttata preferred the rice transplanted in late season (Choi et al. 2005).

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4.17 Rice skipper, Pelopidas mathias (F.) (Lepidoptera: Hesperiidae) Distribution: Widespread in Asia, Africa and Oceania (CABI 2016e). Host plants other than rice: 22 Poaceae species (CABI 2016e). Description and biology: The adult butterfly (Fig. 4.24) differs from P. guttata in being larger and usually having only 2 spots in the discal cell of the wing and 2 groups of 3 white specks, one anterior and one marginal from the first group (CABI 2016e). The hindwings are olive brown, usually without spots. Mating generally takes place during morning hours. Eggs, averaging 90, are laid singly on the upper surface of leaves (Dale 1994). The white eggs are spherical, about 1 mm in diameter and 0.5 mm high with the flat base attached to the leaf. The eggs remain white until they darken when ready to hatch. The incubation period ranges from 3 to 6 days. The newly hatched P. mathias larvae are pale green, becoming yellowish green with age. P. mathias larvae have reddish vertical bands on each side of the head (Fig. 4.25), while the bands of P. guttata are dark brown, closer together and W-shaped. There are five larval instars. The full-grown caterpillar measures 30 mm in length and 3.5 mm across the middle of the body. The larval stage lasts for 13 to 26 days. The pupa is a chrysalis. Pupation takes place in a silken web spun inside the leaf fold. It is light green and stouter and shorter than the larva. The pupa is at first green in colour with stripes clearly visible on the back, but changes to dark brown later. It is cylindrical

Figure 4.24 Pelopidas mathias adult (Source: www.butterflycircle.com). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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and gradually tapering towards the hind end. The pointed end is attached by silk to a leaf. The cremaster is transversely flattened and bears on its posterior margin a number of small spines. The pupal skin is thin and almost transparent. The adult butterfly emerges in 7 to 12 days after pupation. The skippers can frequently be found feeding on nectar from flowers (CABI 2016e). In India, the insect passes through four overlapping generations. The adults of the first generation appear in the fields about the third week of August and those of the second generation, the second week of September. The butterflies of the third and fourth generations appear towards the third week of October and last week of November, respectively. P. mathias is most active from August to November and with the advent of winter a high percentage of the larvae hibernate thereafter. The overwintering pupae remain inside the cocoons in folded leaves. The butterflies emerge from them in the spring when the weather becomes warmer (Dale 1994). Plant damage and ecology: Pelopidas mathias is a minor pest of rice with an extensive distribution in the rice-growing regions of the world. It occurs in all rice environments, but in Japan and Taiwan upland rice is the most affected. Damage caused by the larvae that defoliate the rice plants is similar to that of P. guttata. The newly hatched larvae feed on tender leaves. The large larvae do most of the defoliation. They roll up and stitch together two or more leaves that are eaten from the margin inwards. Feeding edgewise on the margins and tips of the leaves, they remove large sections of leaf tissue to the midrib. Generally, only one larva is found in a fold (Teotia and Siya Nand 1966). A few large larvae on a plant can cause noticeable defoliation viewed while walking through a field or along the field border.

Figure 4.25 Pelopidas mathias larva (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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4.18 Rice ear-cutting caterpillar, Mythimna separata (Walker) (Lepidoptera: Noctuidae) Distribution: Asia – Afghanistan, Australia, Bangladesh, Bhutan, China, India, Indonesia, Japan, Kampuchea, Korea (DPR), Korea (ROK), Laos, Malaysia, Myanmar, Nepal, New Zealand, Pakistan, Papua New Guinea, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam; Europe – Russia; Oceania – Australia, Cook Islands, Fiji, New Caledonia, New Zealand, Norfolk Island, Papua New Guinea, Samoa, Solomon Islands, Tonga, Vanuatu (CABI 2016f). Host plants other than rice: A wide host range including species in the families Brassicaceae, Cannabaceae, Chenopodiaceae, Cyperaceae, Fabaceae, Linaceae, Poaceae, Solanaceae (CABI 2016f). Description and biology: The adult (Fig. 4.26) is a stout, pale reddish brown moth which measures 20 mm long with a wing expanse of 40 mm. The forewings have two pale round spots, and the hindwings are dark reddish brown dorsally and white ventrally. The moths feed on nectar from flowers and honeydew excreted by mealybugs and other Homoptera. The female moths start egg laying in three days. Eggs are laid in batches of about 100 between the leaf sheaths and stems of rice plants or grasses. Eggs are cemented to the plant by a white adhesive fluid secreted by the female. Males live for only 3 days while the female moths live longer (Dale 1994; Islam and Catling 2012). Eggs are spherical, greenish white when fresh, gradually turning pale yellow and finally black. The egg period varies from 5 to 7 days. Newly hatched caterpillars are dull white, but later turn green. The head is orange or brown. Four longitudinal light grey to black stripes

Figure 4.26 Mythimna separata adult (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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run along the body. The larvae are nocturnal in habit and during the day they hide in loose soil, under trash, in stubbles, in leaf sheaths and in whorls. During the night, they become active and resume their feeding activity. The entire larval stage lasts for about 28 days. The head of the larva is orange or brown. Four longitudinal stripes run along the green to pink body (Fig. 4.27). The larvae pupate in the soil. Sometimes naked pupae are also observed among the tillers. Pupae are light amber at first, later becoming shiny dark brown as they mature. Pupae are 17-20 mm long and have two long curved cremastral spines. The pupal period is 8-11 days. There are five annual field generations per year in Bangladesh (Islam and Catling 2012). Plant damage and ecology: The early instar caterpillars first feed on dried leaf tissues and later move on to green leaves for feeding. Consumption increases steadily as the larvae develop, and from the third instar onwards the caterpillar is a voracious feeder, often removing large areas of leaf blade or entire leaves and even completely stripping the plants. They also eat the lemma and palea of the developing grains as well as the anthers of flowers (Papel et al. 1981). The most devastating damage is caused by the sixth and final instar larvae in the grain filling stage when the larvae cut off rice panicles from the peduncle. The grains falling on the ground, however, are not eaten by the caterpillars (Islam and Catling 2012). Damage may be localized in a part of the field, but in serious outbreaks many fields are affected as the larvae, moving in large groups as a marching army, from field to field, cause enormous losses within a few days. In cases of severe infestation, the damage may go up to 60% or even more. Katiyar and Patel (1969) reported grain losses up to 1,640 kg/ha in Madhya Pradesh, India. Besides the direct loss, many farmers, anticipating the pest incidence, are tempted to harvest the crop

Figure 4.27 Mythimna separata larva (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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prematurely. This produces large quantities of chaffy grains, which may reduce the market price of the product. Moreover, a large number of grains and panicles are seen lying in the fields as the result of feeding damage. Experiments with third instar caterpillars indicated that for each increase of 1% leaf area consumed, there is a reduction of 0.058 cm in panicle length, 0.88 grain/panicle and 0.072 g yield/hill at the booting stage of the crop (Alam et al. 1980). But these values are liable to change with the larval instar and rice cultivar used for the study. Khamparia et al. (1981), working with a different variety and fifth instar caterpillars, reported that there was a yield reduction of 0.41 g/hill with an increase of every 1% of foliage loss by the larvae. Islam and Catling (2012) stated that the yield loss caused by a population of 15 larvae/hill was estimated at 38% in the vegetative stage and 93% in the ripening stage. Mythimna separata, formerly considered a minor pest of rice, became a serious pest in several parts of Bangladesh, China and India in the 1970s. Severe outbreaks of this insect have been reported by many workers (Alam and Nurullah 1977, Chaudhary and Singh 1980, Barwal l983). The attacks may be sporadic but if heavy, the entire crop may be lost. The pest occurs in all rice environments but is most abundant in upland and rainfed wetland environments. Many conditions have been reported ideal for outbreaks of this pest in different countries. In India, heavy late rains after a long drought often result in widespread oviposition and larval development. Also, in Bangladesh, major outbreaks are always associated with a long drought followed by wet weather (Alam and Nurullah 1977; Patel 1970). In Bangladesh M. separata is more abundant during the monsoon season due to the abundance of weed hosts (Islam and Catling 2012). Plants with dense foliage coupled with heavy tillering are most commonly attacked by the pest (Patel 1979). Heavy application of nitrogenous fertilizers produces more succulent and green plants and results in increased armyworm populations (Koyama 1966). Survival rate and fresh weight of larvae are both high on these plants. It is interesting to note that plants of the aromatic rice variety ‘Basmati’ are seldom attacked by the pest. In China, the M. separata moths migrate to the north from southern China in the spring and fly back in the autumn. The overwintering boundary is considered between 32 and 34°N latitude (Li Kuang-po et al. 1964; Hong-Qiang Feng et al. 2008). There are four important migrations annually. The first (March–April) and the second (May–June) are from low latitude and low elevation to high elevations; the third and fourth, vice versa. M. separata is also believed to move into Bangladesh from southern and central India during the south-west monsoon (Islam and Catling 2012).

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4.19 The fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) Distribution: The fall armyworm ranges from the United States east of the Rocky Mountains southward to Argentina. In the United States, it overwinters successfully only in southern Texas and Florida and is generally a more serious pest in the south-eastern United States than in other regions of the United States. It has been reported as a pest of rice in the United States, Panama, Brazil, Colombia and Puerto Rico. Host plants other than rice: A total 186 plant species, from 42 different families, are affected by this pest. The plant species most frequently cited in North America were maize, sorghum, peanuts, Bermuda grass, sugarcane and rice. In South America, the plant species were maize, rice, sorghum, beans, cotton and peanuts (Casmuz et al. 2010). Description and biology: The fall armyworm is a polyphagous insect but prefers grasses, and is a serious pest of maize, pasture grasses and several other crops. It is only an occasional pest on rice. Adult moths (Fig. 4.28) are about 2.5 cm long with greyish brown sculptured forewings and whitish hindwings. Females lay masses of 50 to several hundred whitish eggs covered with moth scales (imparting a ‘furry’ appearance) on the leaves of rice and other grasses in and around rice fields. Light green, brown or dark grey larvae with light stripes running the length of the body emerge in less than 10 days and then feed on rice plants for two to three weeks, passing through six instars. Mature larvae are about 2.5 cm long and have a distinctive inverted ‘Y’ on the head (Fig. 4.29). Mature larvae prepare a cocoon and pupate in soil or decomposing plant material. Moths emerge in 10 to 15 days, mate and disperse widely before laying eggs on new plants. Adults are strong

Figure 4.28 Spodoptera frugiperda male (Source: Matthew Bertone). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.29 Spodoptera frugiperda larva (Source: Matthew Bertone).

fliers and can disperse widely. Multiple generations occur per year, with more generations in the tropical and subtropical portions of its range. Plant damage and ecology: Larvae feed on the leaves of rice plants, and can be found in fields throughout the season; however, the insect is most damaging to young rice plants. The young larvae feed on the leaf surfaces from the edge towards the midrib (Dale 1994). As they grow they become voracious. Young rice plants are often cut at ground level while older plants are only defoliated. They consume large amounts of leaf tissue and can enter fields in large numbers, and under severe infestations destroy large amounts of tissue. When large numbers of armyworms are present, entire seedlings can be defoliated, resulting in severe stand loss. Pantoja et al. (1986) studied the effect of S. frujiperda feeding on the yield components of rice. Increased S. frugiperda infestation levels resulted in increased rice defoliation, reduced plant and panicle density, and reduced rice yields. Yield component studies indicated that lower yields on infested plots were the result of reduced plant stand and panicle density. Kernel weight and per cent filled kernels were not affected. Yield reductions were linearly related to S.frugiperda larval density. Fall armyworm infestations generally occur along field borders, levees and in high areas of fields where larvae escape drowning. The most injurious infestations occur in fields of seedling rice that are too young to flood. The pest is generally a problem in upland rice because it needs dry soil for pupation.

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4.20 Common cutworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) Distribution: Widely distributed throughout Asia, Australasia and Pacific Islands (CABI 2016g). Host plants other than rice: Arachis hypogaea L., Beta vulgaris L., Brassica oleracea L., Fragaria virginiana Duchesne, Ipomoea batatas (L.) Lam., Nicotiana tabacum L., Ricinus communis L., Zea mays L. and a wide variety of other plants (CABI 2016g). Description and biology: The adult moth (Fig. 4.30) has a greyish brown body, 15-20 mm long; wingspan 30-38 mm, dark purplish brown forewings with numerous spots and light coloured lines. The hindwings are greyish white with grey margins, often with dark veins, narrowly banded along the outer margin. Moths are nocturnal in habit and hide during the day at the base of rice plants and grassy weeds. Adults are strong flyers and can migrate hundreds of kilometres. Female moths begin ovipositing 2–3 days after emergence. Eggs are laid on leaves in clusters of 200 to 300 and they are covered with buff coloured hairs. The eggs are 0.6 mm in diameter, round and have a ridged surface. They are usually pale orange-brown or pink in colour, laid in batches and covered with hair scales from the tip of the abdomen of the female moth (CABI 2016g).They hatch in 3-4 days. The larva (Fig. 4.31) is hairless, variable in colour (young larvae are light green, the later instars are dark green to brown on their backs, lighter underneath); sides of body with dark and light longitudinal bands; dorsal side with two dark semilunar spots laterally on

Figure 4.30 Spodoptera litura adult (Source: Sandeep Singh, Punjab Agricultural University, India). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.31 Spodoptera litura larva (Source: Don Herbison-Evans; http://www.butterflyhouse.com.au/).

each segment, except for the prothorax; spots on the first and eighth abdominal segments larger than others, interrupting the lateral lines on the first segment. There are black crescent spots next to the stripes. The head is black to dull brown with a yellow V-shaped marking. Though the markings are variable, a bright yellow stripe along the length of the dorsal surface is characteristic of S. litura larvae (CABI 2016g). The larval period is 20–26 days and they pass through 5 instars before they pupate. In upland conditions, pupation takes place in soil in individual earthen cells. In wetland fields, larvae pupate in the rice plants or in grassy areas along field borders. The pupa is reddish brown in colour, 15-20 mm long and tip of abdomen has two small spines. The moth emerges in 6-7 days (Dale 1994). Plant damage and ecology: Spodoptera litura is a highly polyphagous pest infesting rice only sporadically. The young caterpillars feed on leaf surfaces from the edge towards the midrib. As they grow, they become voracious. Young rice plants are often cut at ground level while older plants are only defoliated. The pest is generally a problem on upland rice because it needs dry soil for pupation. Lowland fields also occasionally suffer damage when the larvae move from one field to another grazing over the young rice plants (Dale 1994).

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4.21 Rice swarming caterpillar, Spodoptera mauritia (Boisd.) (Lepidoptera: Noctuidae) Distribution: Widely distributed in Asia, Africa, Australasia and Pacific Islands (CAB International 2015). Host plants other than rice: Agropyron sp., Axonopus compressus (Sw.) Beauv., Brachiaria mutica (Forssk.) Stapf, Fimbristylis acuminata Vahl., Isachne globosa (Thunb.) O. Kuntze, Ischaemum indicum (Houtt.) Merr, Panicum repens L., Paspalum conjugatum Berg., Saccharum sp., Zea mays L. (Dale 1994). Description and biology: The adult moth (Fig. 4.32) is stout with a body length of about 1.6 cm and wing expanse of 3.5–4.0 cm. Forewings of the female moth are greyish brown with wavy lines and a dark spot sub-centrally. Wings of the male moth are more greyish. The hindwings are brownish white with thin black margins. Moths are nocturnal in habit and hide in crevices in the soils or under vegetation during the daytime (Dale 1994). Female moths generally mate on the night following emergence. Egg lying commences on the third night and continues for a week. Peak oviposition is on the first night of egg laying. Eggs are laid on the underside of grass leaves and are covered with a thin layer of brownish grey hairs. Oviposition rarely occurs on rice plants and the first instar larvae usually migrate from grassy vegetation to the rice field. But in the later stages of infestation, eggs may be laid on rice leaves. A single fem ale moth may lay 5 to 6 oblong egg masses each

Figure 4.32 Spodoptera mauritia adult (Source: DW Stock Picture Library (http://www.dwpicture.com. au/); photographer: L. Greenup (HR243/RM)). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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containing 150 to 200 spherical eggs. The egg is cream coloured when laid and acquires a brown tinge as development proceeds. The incubation period ranges from 3 to 9 days. Young larvae are light green with yellowish white lateral and dorsal stripes, later becoming greyish brown. The head is a mottled light brown. Three longitudinal pale brown or red stripes lie along the dark green body (Fig. 4.33). The lateral stripes have a reddish upper margin. The larvae are darker brown when populations are high. First instar larvae prefer succulent young foliage for feeding. The weight of frass produced by the last instar caterpillar is almost five times of that of the previous instar. This feeding pattern explains the cause of sudden, devastating damage by late instar armyworms in the field (Rothschild 1969). The number of larval instars of S. mauritia has been reported from different countries; 4 in the Philippines (Otanes and Sison 1952), 5–6 in India (Ananthanarayanan and Ramakrishna Ayyar 1937, Nair 1978), 7 in Sarawak (Rothschild 1969) and occasionally 8 in Hawaii (Tanada and Beardsley 1958). The larval period is 15–24 days. Pupation is in soil, within an earthen chamber. The pupa is dark brown in colour and measures 16.5 mm long and 5 mm wide. The pupal stage lasts 7–14 days. In Taiwan, 7–8 generations occur per year. Plant damage and ecology: The rice-swarming caterpillar is a sporadic pest occasionally causing up to 20% loss in rice yield. It is also polyphagous and infests various graminaceous plants. Severe outbreaks of this pest have been reported from Sarawak (Rothschild 1969) and India (Sathiyanandam et al. 1984). It occurs in all rice environments, but is least

Figure 4.33  Spodoptera mauritia larva (Source: Science Photo Library (www.sciencephoto.com); photographer: Nigel Cattlin). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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abundant in irrigated fields. The caterpillar damages rice by feeding on the leaves at night. The damage by early instar larvae is negligible and escapes notice. But the older caterpillars are voracious and can devastate a whole field within a short time. They feed mainly on young rice plants in the nurseries or shortly after planting. When a field has been stripped bare, they migrate in large numbers into adjoining fields to continue feeding. Their migration is facilitated by the absence of standing water in the fields. The plants are reduced to mere stumps which may die, or even if they recover, do not bear earheads uniformly. Nurseries situated near ill-drained marshy areas are attacked earlier than those near dry ground. The infestation starts at the onset of the monsoon. Seedlings 4 to 20 days old in wetbed nurseries as well as plants from direct-seeded rice in poorly drained fields suffer the most serious attacks. Rice plants older than 6 to 7 weeks are usually not attacked. The pest infestation is governed by various climatic conditions. In South India, S. mauritia is more prevalent in the ‘punja’ crop during October–December. Oviposition ceases by the end of February when the weather becomes hot and dry. Rothschild (1969) suggested that the 1967 outbreak in Sarawak, Malaysia, was due to a prolonged period of dry weather, followed by heavy rainfall, which led to the abundant growth of young grasses and favoured S. mauritia survival and development.

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4.22 Common armyworm, Mythimna unipuncta (Haworth) (Lepidoptera: Noctuidae) Distribution: Southern Canada, the United States, Central and some South American countries, Southern Europe, West Africa (Dale 1994). Host plants other than rice: Larvae are generalist feeders on many species of plants including alfalfa, maize and other grains, forage grasses, vegetables, many weeds and other wild plants, leaves of fruit trees and ornamentals. Description and biology: The adult (Fig. 4.34) moths are light red to pale brownish and have a hairy body with black spots and patches. They have a wingspan of about 35 to 45 mm. The length of the forewings varies from 18 to 21 mm. There is a distinctive white spot in the middle of each forewing. Hindwing is fuscous grey, paler towards the base, the veins dark. Moths are nocturnal in habit, positively phototropic and remain inactive during daytime. Mating and oviposition usually take place after sunset. Generally, the males die shortly after mating. The female moths lay eggs for about 5 days (Dale 1994). The eggs are laid in several rows, each mass consisting of 90–230 eggs. They are round, pale yellow and 0.6–0.7 mm in diameter. The incubation period is 7–9 days. Larvae are nocturnal and hide under leaves and debris during the day. Freshly hatched larvae are dull white with a brownish black head. There are 6 larval instars. Of the total amount of leaf area consumed, more than 90% is eaten by the fifth and sixth instar caterpillars (Rice et al. 1982a). The full-grown larva (Fig. 4.35) is usually dark or greenish grey in colour and has a yellow stripe just below a line of prominent black spiracles. The

Figure 4.34 Mythimna unipuncta adult (Source: Juha Tyllinen). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.35 Mythimna unipuncta larva (Source: http://www.pyrgus.de/).

head capsule of the larva has two brown bands forming a ‘V’ shape. The larval duration is 24-28 days. Pupation takes place in individual earthen cells in the soil. The pupae are light amber at the beginning and turn dark brown just before adult emergence. The average pupal period lasts for 16 days. There are five generations of the pest in a year; usually only one generation is spent on rice. Plant damage and ecology: Mythimna unipuncta is a cosmopolitan pest of grasses. Rice is not an ideal host for the armyworm. However, it occurs sporadically in epidemic numbers on rice in California (Lange and Grigarick 1970). Armyworm infestations occur relatively late in the growing season, 3 to 4 weeks before heading. During the early instars, larvae skeletonize tender, young leaves or the inside of leaf sheaths. Later, the larvae remove irregular portions of the entire leaf starting from the edge, but leaving the midvein intact (Rice et al. 1982a). Feeding damage is generally found on the distal portion of rice leaves. Rice et al. (1982b) have shown that defoliation averaging 25 to 30% by armyworm larvae resulted in yield reductions up to 50%.

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4.23 Rice green semiloopers, Naranga aenescens (Moore) and Naranga diffusa Walker (Lepidoptera: Noctuidae) Distribution: N. aenescens – China, India, Indonesia, Japan, Korea, Malaysia, Philippines, Taiwan, Vietnam (Dale 1994); N. diffusa – Bangladesh, China, India, Japan, Korea ROK, Korea DPR, Malaysia, Myanmar, Philippines, Taiwan, Thailand, Vietnam (http://www. plantwise.org/KnowledgeBank/Datasheet.aspx?dsID=35720). Host plants other than rice: N. aenescens – Cyperus diffusa L., Echinochloa colona (L.) Link, Leersia hexandra Sw., Leptochloa chinensis (L.) Nees, Paspalum conjugatum Berg., Sorghum bicolor (L.) Moench. (Dale 1994); N. diffusa – Echinochloa colona, Echinochloa crus-galli, Eleusine indica, Leersia hexandra, Leptochloa chinensis, Paspalum conjugatum, Paspalum distichum, Sorghum bicolor (http://www.plantwise.org/KnowledgeBank/ Datasheet.aspx?dsID=35720). Description and biology: Naranga aenescens is an important pest of rice in eastern Asia (Ando et al. 1980) but N. diffusa is only a minor pest. The biology and ecology of N. aenescens and N. diffusa are similar and the biology of N. aenescens, as given in Dale (1994), is herein described. The adult N. aenescens (Fig. 4.36) is a small moth with a wing expanse of 17 mm. The forewings of the female are golden yellow, each with two transverse brown bands; hindwings are dark brown. The male moth is dark purple red. The moths which emerge from overwintering pupae late in spring mate in the daytime. Adults hide in rice fields or

Figure 4.36 Naranga aenescens adult (Source: http://www.jpmoth.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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grassy areas at the base of the plants during the day and become active at night. They are highly attracted to lights. Each female lays 50-100 spherical eggs on leaves, in groups of up to 15 each, during its lifetime of 3 to 5 days. Eggs are yellow when newly laid and later develop purple markings. The larva is a semilooper, light green with white stripes (Fig. 4.37). The population density during the larval stage of N. aenescens is known to be one of the factors responsible for inducing larval diapause (Kishino and Sato 1975). The larva forms a pupal chamber by folding a rice leaf over and securing it with silk. The pupa is light brown and smooth bodied. Development from egg to adult takes 18 to 21 days in the Philippines (Pantua and Litsinger 1984b). There is often a short pupal diapause for the last generation. There are 4–5 generations in a year except in northern Japan where there are only 3–4. Plant damage and ecology: N. aenescens is only found in wetland environments and is abundant in the rainy season. The defoliation caused by N. aenescens and N.diffusa is similar to that caused by other early season leaf-feeding larvae such as Rivula atimeta. First and second instar larvae scrape leaf tissue from the leaf blades, causing them to appear whitish when viewed from a distance. Mature larvae feeding on leaf edges create notches. The larvae prefer actively growing plants, from the seedbed through the tillering stage. Defoliation generally occurs in patches in the field. Defoliation from green semiloopers and other pests that attack the vegetative stage are of greater significance, in terms of yield loss, if the crop is also affected by other insect pests, diseases, weeds or soil problems. These biotic and abiotic stresses act synergistically to increase crop loss (Litsinger et al. 2010). Frequent outbreaks of N.diffusa have been recorded in Japan, even before 1900, and are associated with overcast skies, low temperatures and increased use of nitrogen fertilizer (http:// www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsID=35720). Damage is restricted to

Figure 4.37 Naranga aenescens larva (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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the seedbed and the vegetative stage in the field. Fortunately, a vigorously growing rice crop can tolerate high levels of defoliation (25-50% loss of leaf area). Economic thresholds, based on levels of defoliation by N. diffusa larvae, have been developed by Bandong and Litsinger (1988). These levels are 0.5–1.0 larvae/hill or 10–15% of leaves showing damage and N. diffusa larvae present.

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4.24 Green hairy caterpillars, Rivula atimeta (Swinhoe) (Lepidoptera: Noctuidae) Distribution: Brunei, Philippines, Indonesia (http://www.plantwise.org/KnowledgeBank/ Datasheet.aspx?dsid=47657). Host plants other than rice: Echinochloa spp. and Leersia sp. Description and biology: The description of the pest is based on the paper by Sunio et al. (1983). Adult moths (Fig. 4.38) of both sexes are whitish grey or light brown and are active at night. During the day, they hide under vegetation with their heads pointed down. Spherical, pale green eggs are laid singly in rows on both sides of a leaf. The number of eggs laid per female moth averages 130. The incubation period is 3–5 days. Adult longevity of male and female moths is 4 and 5 days, respectively. The larva (Fig. 4.39) has long thread-like hairs on its pale green body and the average larval period is 13.5 days. When ready to pupate, larvae spin a cocoon of silk on a leaf blade. The pupal period is 5 days. Plant damage and ecology: The hairy caterpillars defoliate rice at the vegetative stage. In addition to rice, R. atimeta feed on grassy weeds. Damage is similar to that of the green semilooper Naranga aenescens. Damaged plants often recover when defoliation is not severe but high populations can kill seedlings, especially when they occur in combination with other insect pests.

Figure 4.38 Rivula atimeta adult (Source: B. Merle Shepard, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.39 Rivula atimeta larva (Source: Sylvia Villareal, IRRI).

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4.25 Rice whorl maggot, Hydrellia prosternalis Deeming (Diptera: Ephydridae) A new species of Hydrellia discovered on rice at the International Institute of Tropical Agriculture in Ibadan, Nigeria, was described and named Hydrellia prosternalis Deeming in 1977 (Deeming 1977). The genus Hydrellia contains more than 100 species that feed on gramineous crops (Deeming 1977). Although at least eight Hydrellia species have been recorded in Africa south of the Sahara, only H. prosternalis feeds on rice in this region. Distribution: West Africa (Burkina Faso, Côte d’Ivoire, Ghana, Nigeria), Egypt (Heinrichs and Barrion 2004). Hydrellia prosternalis may be widely distributed in West Africa, but taxonomic confirmations from several countries have not been published. Although H. prosternalis damage was reported from Liberia and Sierra Leone, no taxonomic identifications were made (Deeming 1977). It is reported as a pest in Egypt (Isa et al. 1979, Ismail 1979, Zatwarnicki 1988, Yanni and Abdallah 1990); thus its distribution in Africa may be broad. Host plants other than rice: Leersia hexandra Swartz and Pennisetum purpureum (Schumacher) (Moyal 1982). Description and biology: Ismail et al. (1979) studied the biology of H. prosternalis in Egypt. Moyal (1982) reported on the biology and ecology of H. prosternalis in Côte d'Ivoire and described the morphological features of the various stages. White, cigar-shaped eggs are laid singly and parallel to the veins on the leaves of young seedlings. Eggs are 0.7–0.8 mm long and 0.2 mm wide. Upon hatching, the larva penetrates the leaf tissue parallel to the veins. In the second instar, the larva moves to the base of the plant to the level of the axillary bud where it enters the leaf sheath. The whitish yellow third instar is 3 mm long and 0.7 mm wide. Two, distinct, black spine-like structures are readily observed protruding from the extremity of the abdomen. The third instar larva moves up the leaf sheath and pupates underneath the ligule. The larvae, when ready to pupate, often leave the mines in which they are feeding and bore into a plant of another species. Thus, rearing an adult specimen from a plant does not mean that the plant is its host plant (Deeming 1977). The duration of one generation from egg to adult is 30–40 d and there is one generation per rice crop. Plant damage and ecology: Moyal (1982) conducted a detailed study of H. prosternalis in three regions of Côte d'Ivoire: Kotiessou in the south, Bouake in the centre and Korhogo in the north. He reported it as a pest occurring at the seedling stage until booting, being most abundant during the tillering phase of crop growth. Detailed studies on the seasonal occurrence of this pest have not been conducted, but it is present in rainfed lowland and irrigated lowland rice throughout most, if not all, of the year. Moyal (1982) reported that it occurred in Côte d'Ivoire, in both the dry and wet seasons, from February to November. According to Yanni and Abdallah (1990), the introduction of indica rice into Egypt intensified the damage caused by H. prosternalis as indica rice is highly susceptible compared with the japonica rice. Damage by H. prosternalis is similar to that of H. philippina, which is a widespread pest in Asia. When larvae hatch, they begin feeding on the foliar tissue. First instar larvae mine in the leaves moving parallel to the leaf veins. Feeding damage by this pest retards plant development, reduces plant vigour and renders the infested plants © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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less competitive with weeds. Effects of this pest in causing yield loss have not yet been determined. It is considered a potentially serious pest whose biology and ecology should be studied more (Moyal 1982). In the Philippines, however, feeding by populations of H. philippina failed to reduce rice yields on the IRRI farm (Shepard et al. 1990). In Egypt, Isa et al. (1979) reported that applications of N fertilizer caused an increase in the percentage of infested tillers and in the number of H. prosternalis mines per tiller. Application of manure, however, had no effect on degree of infestation. Hydrellia prosternalis is reported to occur in both the humid tropical and the Guinean savanna zones in West Africa, with highest populations in the former. In Nigeria, it is present, with equal incidence, in all three climatic zones: the humid tropical, Guinean savanna and the Sudanian savanna (Alam 1992). In Côte d'Ivoire, it is most important in the Korhogo area in the north, which is in the Guinean savanna (Moyal 1982). The whorl maggot occurs in aquatic habitats and thus is a pest of both rainfed lowland and irrigated lowland rice.

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4.26 Rice leaf miner, Hydrellia griseola (Fallen) (Diptera: Ephydridae) Distribution: Information on the distribution of Hydrellia griseola is incomplete, but it is known to be distributed widely (Hesler 1995). It occurs throughout Asia (e.g. the Philippines, India and Japan) and Europe, in the United States and Canada, in Costa Rica and Colombia, and perhaps in Africa and Australia. It is found in ephemeral aquatic and semi-aquatic habitats of various kinds, including rice paddies. Host plants other than rice: Agropyron sp, Agrostis tenuis Sibth., Alisma plantagoaquatica L., Allium cepa L., Avena sativa L., Bellis perennis L., Bromus inennis Leyss., Cynodon dactylon (L.) Pers., Cyperus rotundus L., Dactylis glomerata L., Digitaria sanguinalis (L.) Scop., Echinochloa colona (L.) Link, Festuca parvigluma Steud., Hordeum vulgare L., Hydrocharis morsus-ranae L., Lamium album L., Lemna minor L., Lolium perenne L., Lychnis dioica L., Muhlenbergia mexicana (L.) Trin., Panicum repens L., Paspalum scrobiculatum L., Phalaris arundinacea L., Phleumpaniculatum Huds., Phragmites australis (Cav.) Trin. ex Steud., Poa compressa L., Polygonum lapathifolium L., Polypogon fugax Nees, Sagittaria latifolia Willd., Scirpus grossus L., Secale cereale L., Setaria glauca (L.) Beauv., Stellaria media (L.) Cyr., Siratiotes aloides L., Trifolium pratense L., Triticum aestivum L., Typha latifolia L., Veronica officinalis L., Zea mays L., Zizania aquatica L. (Dale 1994).

Figure 4.40 Hydrellia griseola fly (Source: http://www.diptera.info/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Description and biology: The description and biology are reported in Dale (1994). Rice leaf miner adults (Fig. 4.40) are small flies, less than 6 mm in length, and are metallic grey with clear wings. The newly emerged adult is light grey, and looks like a small housefly. It walks briskly and stops repeatedly to stroke and brush various parts of the body with its front and hind legs. Adults are positively phototropic and are attracted to bright reflecting surfaces. They fly close to the water surface and can be observed resting on leaves. Mating occurs 3 days after emergence. Flies of both sexes are polygamous. Copulation is observed most often on the water surface and floating leaves (Grigarick 1959). Adults are mobile and oviposit throughout the rice field. Adults are long-lived (four months or more) and feed on fungi, algae, leaf tissue and other insects. Leaves lying on or very close to the water surface are the preferred sites for oviposition. A single fly may lay about 50-100 eggs singly on the upper surface of leaves. Eggs are elongate, whitish and approximately 0.6 mm in length. The average incubation period is 5 days. Legless larvae emerge from eggs in 3 to 6 days. They are transparent or cream coloured as early instars but become yellow to light green as they feed. Larvae mine leaves, feeding between the epidermal layers. They feed using their well-developed mouth hooks. Under conditions of limited food supply, crowding or submergence of the infested leaves, the larvae may leave their first mines and migrate to newer leaves. The maggots pass through three larval instars in a period of 7-10 days. Late instars attain a length of about 6 mm, and pupate in the larval mines within 5 to 12 days of beginning to feed. The puparium is ovoid, tapering and light to golden brown in colour. It measures about 3.5 mm long and 1.0 m wide. The pupae can easily be seen inside the transparent mines. Puparia are also occasionally found on soil. The entire life cycle is completed in two to four weeks, and up to 11 generations per year may occur in some parts of the insect’s range (Hesler 1995). Hydrellia griseola, a multivoltine species, overwinters as an adult or pupa. All stages of the life cycle can generally be found after the first generation of the year. It is possible to have 10 generations in a year under California conditions. Kuwayama et al. (1955), in Japan, reported the critical low temperature for the egg stage at 10°C, larval stage at 6°C and pupal stage at 8°C. These temperatures are similar to the threshold temperatures recorded in California by Grigarick (1959). Total developmental time in California, from hatched egg to adult varies from 13 days at 32°C to 94 days at 10°C. Larvae may be killed by extremely high temperatures (44–46°C), especially when they mine upright leaves exposed to the sun (Anon. 1983). Plant damage and ecology: The rice leaf miner is an early season pest of rice in California and in Japan. The pest also attacks other crops such as barley, oats, timothy and wheat in California. Direct-seeded rice is more at risk than transplanted rice. Infestations tend to be more severe in continuously flooded rice where the flood is relatively deep and leaves lie on the water surface. The larvae mine the leaves and rarely leaf sheaths, and feed on the mesophyll tissues. The early mines are usually linear which later widen and coalesce to form big white blotches. The leaves then shrivel and lie on the surface of the water. In severe infestations, the majority of leaves in an area may be mined (Way et al. 1983). The maggots are mobile and move on to new leaves after old ones are completely mined. Serious infestations may result in reductions in photosynthetic capacity, and an increase in leaf abscission, seedling

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death and stand loss. Losses of 10–20% have been reported in California, but the insect is only a sporadic pest of rice. Damage is more severe if the attack occurs at the seedling stage. Also, Manandhar and Grigarick (1983) have shown that feeding effects on younger leaves are more pronounced than on older leaves. Deep water and cool temperatures during the early part of the growing season reduce plant vigour (Kuwayama 1956, Grigarick 1963). These conditions cause the leaves to lay on the water surface which results in increased oviposition and subsequent mining by the larvae. But if the weather becomes warm and conditions become favourable for the growth of leaves in an upright position, the infestation may be drastically reduced due to egg and larval mortality (Grigarick 1959) In Japan, high populations of adult flies are observed in the paddy fields from the middle of June to the end of July. But in the weedy fields, the adults begin to appear earlier (i.e. from April onwards). The peak fly population in Japan is reached in the months of May and July (Murai 1967). In California, the fly population is at its highest during March and April (Grigarick 1959).

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4.27 Rice whorl maggot, Hydrellia philippina Ferino (Diptera: Ephydridae) Distribution: Asia – Bangladesh, Cambodia, China, India, Indonesia, Japan, Korea (DPR), Laos, Myanmar, Philippines, Taiwan, Thailand, Vietnam; Africa – Egypt; South America – Guyana, Suriname; Oceania – Papua New Guinea, Solomon Islands. http://www.plantwise.org/KnowledgeBank/PWMap.aspx?speciesID=21541&dsID=281 04&loc=glo Host plants other than rice: Cynodon dactylon (L.) Pers., Echinochloa colona (L.) Link, Echinochloa crus-galli (L.) Beauv., Eleusine indica (L.) Gaertn., Fimbristylis miliacea (L.) Vahl., Paspalum scrobiculatum L. (Dale 1994). Description and biology: Sain (2000) reviewed the bionomics and pest status of the rice whorl maggots, Hydrellia, philippina, H. griseola and H. sasakii, pests attacking rice in India. The rice whorl maggot (RWM), H. philippina, was discovered as a pest of rice only in 1961. The spread of irrigation and double cropping allowed its density to increase and become noticeable (Litsinger et al. 2013). The morphology and bionomics of H. philippina was first recorded on rice in Thailand (Patanakamjorn 1964). Ferino (1968) studied the taxonomy and bionomics of the whorl maggot in the Philippines. Adults (Fig. 4.41) are dull grey flies. Females are about 1.8 to 2.3 mm long, but the males are slightly smaller. The flies have a definite preference for high moisture conditions and are not found in upland rice fields. The gravid flies prefer flooded fields for oviposition (Viajante and Heinrichs 1985a).They are often found on

Figure 4.41 Hydrellia philippina adult (Source: Philippines Rice Research Institute). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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floating foliage in calm water and prostrate vegetation near slow-flowing drainage and irrigation canals (Karim 1969). The flies move by a combination of walking and hopping in a zigzag pattern. Adults are saprophagous on dead aquatic insects. The peak time of adult emergence is from 7 to 10 a.m. Mating occurs mostly during morning and evening hours from the second day after emergence. Adults locate rice fields by reflected sunlight from the water surface. Once the canopy closes they can no longer find the rice crop, thus direct-seeded fields or seedbeds are not highly attractive to the adults. The white elongate, cigar-shaped eggs are laid singly on either surface of the leaves. Females lay about 100 eggs during the lifetime of 3–7 days. Flies prefer the basal portions of the leaf to the upper half. The maggots emerge after 2–6 days. The larvae move down the leaf into the whorl on a film of dew and feed within developing leaf whorls. The larva is transparent to very light cream during the first instar but later becomes yellow (Fig. 4.42). Larvae mostly remain outside the leaves, and feed on the mesophyll tissues of the foliage. When the leaves emerge from the whorl, damage can be seen as pinholes in the leaves and white and yellowish lesions at the leaf edges (Fig. 4.43). Severely damaged leaves break in the wind. The larva undergoes three instars; the larval period ranges from 8 to 17 days. Pupation takes place between the leaf sheaths where the pupa is loosely attached to the stem. The puparium is light to dark brown, ovoid and sub-cylindrical in shape. The pupal period is 5–9 days. Hydrellia philippina is a multivoltine species with overlapping generations under field conditions. Temperature, humidity and availability of host plants influence the number of generations. It is believed that the whorl maggot has 13–15 generations in a year. The optimum temperature for normal development is between 29 and 33°C, at which the life cycle is about 19 days (Karim 1969). Adult flies have a special preference for high moisture areas. Under natural conditions, environments such as ponds, streams, lakes and irrigated rice fields provide a favourable ecological niche for the breeding of the flies. Plant damage and ecology: Hydrellia philippina differs from other rice-feeding Hydrellia. The other rice-feeding Hydrellia species are leaf miners but the damage from RWM is different as it mines the unfurled leaf before it expands (Litsinger et al. 2013). Conspicuous necrotic linear feeding lesions are visible when the central leaf opens. Damaged leaves

Figure 4.42 Hydrellia phiippina larva (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.43 Plant damage caused by Hydrellia philippina (Source: IRRI).

become distorted and may break off in the wind (Ferino 1968). Injury results in reduced plant height and root length, delaying crop maturity. (Litsinger et al. 2013). The pest can also cause damage to the boot leaf and developing panicles (Sain et al. 1983), which can lead to only partial filling of the grains (Varadharajan et al. 1977). Small punctures appear in the middle of the flag leaf and its margins get discoloured (Basu 1979). The chlorotic effect coupled with disrupted sugar metabolism and poor nutrient uptake is probably the reasons for the manifested effects on infested plants (Ramamurthy et al. 1977). At the International Rice Research Institute, the occurrence of the pest has been recorded throughout the year (Dale 1994). This species is a pest of rice seedlings only under irrigated or rainfed conditions. Rice plants grown with continuous standing water in the first 3 or 4 WAT have more insect damage than plants in fields where the soil is watersaturated, but without standing water. Ferino (1968) reported an estimated yield loss of 1.4 tons per hectare due to the damage of this pest in the Philippines. In South India, Thomas et al. (1971) reported that the whorl maggot could cause 20 to 30% yield loss on the first crop during April to September. However, the infestation was less in the second crop. However, Nurullah (1979) reported that whorl maggot leads to no adverse effect on tiller production and it even increases the number of productive tillers to compensate for possible grain losses. Litsinger et al. (2013) reported that yield losses to the RWM do occur when the crop is under abiotic or biotic stress from any cause during the vegetative stage. Viajante and Heinrichs (1986) conducted six yield loss experiments and found that the whorl maggot did not adversely affect yield of IR36 but did delay maturity. The experiments

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were conducted by comparing yields of artificially infested and non-infested caged plots. The experimental design eliminated the threat of abiotic or biotic stresses. The conflicting reports regarding yield losses are likely due to different experimental conditions. The fly population in the Philippines is at its lowest during the first six months of the year, which also coincides with times of high temperature and low rainfall. The fly population increases in July and continues to increase up to November after which it declines. But in India, the autumn rice (April to mid-July) is reported to be most affected by whorl maggots, with a peak infestation in the first week of June (Sasidharan et al. 1979). Close planting decreases oviposition and subsequent damage by the whorl maggots (Viajante and Heinrichs, 1985b). Similarly, an Azolla cover on the surface of rice fields reduces the egg population and consequently leaf damage by the larvae.

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4.28 South American rice miner, Hydrellia wirthi Korytkowski (Diptera: Ephydridae) Distribution: Hydrellia wirthi is a native of South and Central America and has been reported from Brazil, Peru, Colombia and Costa Rica. The pest is invasive in the United States and was first reported from rice in Texas and Louisiana in 2004 (Mathis et al. 2006). It also occurs in Mississippi. Host plants other than rice: The insect has also been found on other grass genera including Paspalum and Echinochloa (Mathis et al. 2006). Description and biology: Korytkowski (1982) described the South American rice miner (SARM), H. wirthi, and included notes on its behaviour and biology in addition to the first mention of the economic impact of H. wirthi in the neotropical region. Mathis et al. (2006) described the biology in the south-eastern United States. SARM adults are small (approximately 2 mm in length), dark grey flies (Fig. 4.44). SARM eggs (Fig. 4.45) are elongated, ribbed, white or creamy white and approximately 0.5 mm long and 0.2 mm wide. Eggs are laid singly on the upper surface of rice leaves, near the leaf margins. Larvae are legless, yellowish, and translucent and third instars measure about 6 mm in length (Fig. 4.46). Larvae feed by rasping on leaf surfaces or mine plant tissues, and usually enter rice whorls or stems to feed. Pupation occurs within the plant. Pupae are elongated, about 3-4 mm in length and brown (Fig. 4.47).

Figure 4.44 Hydrellia wirthi adult (Source: Michael Seymour; www.insectimages.org). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.45 Hydrellia wirthi eggs (Source: Boris Castro; www.forestryimages.org).

Figure 4.46  Hydrellia wirthi larva (Source: Alberto Pantoja, USDA-ARS; https://www.ipmimages.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 4.47 Hydrellia wirthi pupa (Source: Michael Seymour; www.forestryimages.org).

Plant damage and ecology: Injury to plants resembles that of the RWM, H. philippina, in Asia (Fig. 4.43). Damage results from feeding by the larvae on or in leaves within the whorls or stems. The maggot mines the leaf or rasps the leaf surface before the leaf unfurls. Larval feeding causes elongated yellow lesions on the margins or distal portions of emerging leaves, and affected leaves often break off. Young rice is primarily affected, and damage is usually detected in plants in the tillering stage of development. Multiple larvae are commonly found in a single plant, and plants infested with multiple larvae exhibit a ragged appearance. Under heavy infestations, entire plants may be killed and stand reduced (Mathis et al. 2006). All severely injured fields reported are from lateplanted rice (i.e. planted in May and June in central and south-west Louisiana).This insect is only a sporadic pest in the United States and yield losses have not been quantified.

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4.29 Leaf miner, Cerodontha orbitona (Spencer) (Diptera: Agromyzidae) Cerodontha orbitona (Spencer) is one of the few dipterans that feed on rice foliage. It is a minor feeder of no apparent economic importance. Distribution: Spencer (1985) reported C. orbitona to be widely distributed in South, West and East Africa with its range extending to the Indian Ocean. In West Africa, C. orbitona has been reported from Ghana, where it is widely spread throughout the rice-growing regions (Scheibelreiter 1973). Host plants other than rice: Hyparrhenia cymbaria (L.) Stapf, Zea mays L. and probably other wild grasses (Spencer 1985). Description and biology: Spencer (1960) described Cerodontha orbitona as a new species from South Africa. Scheibelreiter (1973) provided a detailed description of the stages of C. orbitona. The adult is a small fly, with a wing length of 1.9–2.2 mm. The adults copulate shortly after emergence and lay eggs on the upper leaf surface. The egg is inserted into the spongy layer near the epidermis of the lower leaf surface and towards the leaf tip. The size of the egg is 0.2 x 0.12 mm. Females lay up to nine eggs a day. Larvae emerge 3–4 d after oviposition and begin feeding on the parenchymatous cells, tunnelling towards the leaf tip. According to Spencer (1973), the mine is narrow and situated on the upper part of young leaves. As the larvae develop, they enlarge their mines, thus the end where they pupate is the widest. Larvae appear nearly transparent with internal organs and tracheae clearly visible externally. Larvae have conspicuous and characteristic long posterior spiracular processes. The length of a larva varied from 1·8 mm to 2·3 mm. The larval period is 12–16 d. Pupation takes place inside the mine, where the puparia is fixed to the dorsal leaf epidermis by their long posterior spiracular processes, which can be seen with the naked eye from outside of the leaf (Scheibelreiter 1973). The pupa is slightly transparent, light to dark brown and about 2 mm in length and 1 mm in width. It is light to dark brown in colour. Development from oviposition to the emergence of the adult varies from 3 to 4 wk. Plant damage and ecology: Cerodontha orbitona has been reported from lowland irrigated rice fields (Heinrichs and Barrion 2004). The primary host plant for C. orbitona is Oryza sativa but it has been reported to feed on a grass belonging to genus Hyparrhenia in Uganda and Zea mays in Réunion (Spencer 1985). Although plant damage was easily recognizable, this insect was reported to be a pest of no apparent economic importance in fields observed in Ghana (Scheibelreiter 1973). Infestation of hills varied from 0 to 20%. However, 50% of ratooned rice hills were infested at Dawhenya, Ghana. This insect was found on all stages of crop growth, but appeared to have a slight preference for younger plants. Studies on the seasonal occurrence of C. orbitona at Dawhenya showed that it was present on both the wet and dry season crops but was most abundant during the wet season. The population increased during the wet season, reaching 15% hills infested in November and decreasing to about 0.1% of hills infested with mines during the dry season the following April. Symptoms of plant damage are the transparent, light brown mines that are elongated along one side of the midrib, reaching up to 6 cm in length. The mine is narrow at one end and wide at the other.

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4.30 Paddy stem maggot, Hydrellia sasakii Yausa et Isitani (Diptera: Ephydridae) Distribution: India, Japan. Host plants other than rice: Leersia japonica Honda, Leersia oryzoides (L.) Sw. var. japonica Hack., Leptochloa chinensis (L.) Nees (Sain 2000). The pest is particularly important on the late-planted rice crop in Japan. It is most damaging to young rice plants at one month after transplanting. The insect closely resembles the rice stem maggot, Chlorops oryzae, also a pest in Japan, in its biology. Description and biology: The fly (Fig. 4.48) is blackish grey tinged with bronze and 1.8–2.3 mm in size. The halteres are vividly yellow and their bases are orange in colour. The females are usually larger and with a more swollen abdomen than the males. The flies are often seen resting on the leaf tips of rice plants. Rice planted with wide spacing is preferred for oviposition (Dale 1994). White cigar-shaped eggs are laid singly on both sides of the leaf and hatch in about 2 days. Newly hatched larvae are transparent to very light cream in colour but later become milky yellow. The larval stage lasts for 2-3 weeks. Pupation occurs between the leaf sheath and stem. Fresh pupae are light brown and gradually turn to dark brown as they mature. They are ovoid and sub-cylindrical in shape. The average pupation period during summer is 5-8 days, but it is about 17 days during spring. During winter the insect hibernates as larvae on graminaceous weed plants. The maggots are fairly tolerant to fluctuations in temperature from 18 to 39°C (Okamoto and Koshihara 1962). The insect has five overlapping generations in a year. The population is high during July to early September. This period corresponds to the third and fourth generations of the pest.

Figure 4.48 Hydrellia sasakii adult (Source: IRRI).

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Plant damage and ecology: Newly hatched maggots feed on the unopened tender leaves which are marked with small spots and stripes due to the insect attack. The older larvae enter the central whorl to feed on the inner margin of unopened leaves. When leaves emerge from the whorl damage can be seen as pinholes in the leaves and whiteyellowish lesions on the leaf edge (TNAU 2015). Damaged leaves are shrivelled, the plant is stunted and maturity is delayed. Larvae occasionally infect the panicles in the booting stage and damage the developing grains. A heavy attack may stunt the crop and reduce yield. Heavy-tillering varieties, or plants transplanted with several seedlings per hill, are less damaged by the pest. In India, a recommended economic threshold level (ETL) is 25% damaged leaves (TNAU 2015).

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4.31 Asian rice hispa, Dicladispa armigera (Oliver) (Coleoptera: Chrysomelidae) Distribution: Asia – Bangladesh, Bhutan, Cambodia, China, India, Indonesia, Korea DPR, Laos, Malaysia, Myanmar, Nepal, Pakistan, Philippines, Sri Lanka, Taiwan, Thailand, Vietnam; Oceania – Papua New Guinea (CABI 2016h). Host plants other than rice: Cyperaceae – Cyperus rotundus L.; Poaceae – Cynodon dactylon (L.) Pers., Dactyloctenium aegyptium (L.) Willd. Echinochloa colona (L.) Link, Echinochloa crus-galli (L.) Beauv., Eleusine indica (L.) Gaertn., Leersia hexandra Swartz, Panicum repens L., Paspalum distichum L., Saccharum officinarum L., Triticum aestivum L., Zea mays L., Zizania aquatica L.; Pontederiaceae – Monochoria vaginalis (N.L.Burm.) K.Presl.; (CABI 2016h). Description and biology: Adult beetles emerge in early morning and rest on the lower parts of the plant during daytime. They are small, shiny black beetles with light brown legs and about 5.5 mm long (Fig. 4.49). Beetles have long, well-developed spines on prothorax and elytra; four strong spines project from metanotum. Forewings (elytra) have many pits, a row of ten spines along lateral margins and nine dorsolateral spines. The feeding activity of beetles is highest during morning hours. Females live for 20 days while the males’ longevity is only a fortnight. The beetles mate 3-4 days after emergence (Dale 1994).

Figure 4.49 Dicladispa armigera adult (Source: Jacopo Werther; https://commons.wikimedia.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Eggs are laid singly within the epidermal layers of the ventral surface of rice leaves. A single female lays, on an average, about 55 eggs. The minute eggs are usually found towards the leaf tips. The incubation period ranges from 4 to 5 days. The newly hatched larvae are pale yellow, dorso-ventrally flattened and about 2.4 mm long. Larvae (Fig. 4.50) are distinctly segmented and have a light brown head. They start mining from the leaf tip towards the base of the leaf blade. Larval movement inside the leaf is easily seen when it is placed against light. The larval stage lasts for 7–12 days. Pupae are dorso-ventrally flattened, exarate, ca 4.6 mm long, and brown in colour. The pupal stage is completed within the leaf mine and takes 4-5 days. The adult beetles cut their way out of the rice leaf and become external feeders. The number of generations of the pest seems to depend on the nature and number of crops grown. In regions such as Bangladesh where three rice crops are grown in a year, 6 generations of hispa occur. The sequence is: one generation during February in the winter rice (boro), one during April–May in graminaceous weeds, one on upland rainfed rice (aus) and three others in the monsoon crop (aman) from July to November in succession (Sen and Chakravorty 1970). Adult beetles appear in rice fields in February and the population gradually increases until June–July when the larvae as well as adults cause heavy damage to young rice plants. The population declines after August. Adult beetles in small numbers can still be collected from rice fields up to September–October (Pathak 1975).

Figure 4.50  Dicladispa armigera larva in mine (Source: http://visualsunlimited.photoshelter.com/; Photographer: Nigel Cattlin). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Adult beetles prefer to feed and oviposit on rice crops in the vegetative stage (i.e. plants from 25 to 60 days old). After this phase, the leaves become silicified and less succulent perhaps offering mechanical resistance to feeding (Prakasa Rao et al. 1971). Studies conducted by Basu and Banerjee (1957) showed that plants just after transplanting were more prone to damage than those of later stages. Plant damage and ecology: Both grubs and adult beetles feed on rice plants. Grubs mine the leaves (Fig. 4.50) by feeding on the mesophyll between the veins and tunnelling the tissue in the direction of the main axis of the leaf advancing towards the leaf sheath. The damaged area appears burned and the damage area is puffy (Acharya 1967). A single grub was found to consume, on an average, 123 mm2 of rice leaf area in its lifetime (Budhraja et al. 1979). A single adult beetle feeding on the surface of the leaves consumes about 25 mm2 of leaf area per day (Budhraja et al. 1979). They begin feeding mostly from the apical parts of leaves and proceed downward. The adult beetles prefer to feed on tender leaf tissues mostly from the dorsal side of the leaf. Adults first scrape the epidermis removing chlorophyll between the veins of the lamina giving the appearance of white parallel streaks on the leaves (Fig. 4.51). Later, due to feeding on the veins, white irregular blotches appear on the leaves. In severe cases, leaves are brown and the field presents a dried up appearance. Even replanting may not be of much avail as the pests persist in the field and infest the freshly planted rice seedlings. The pest causes heavy crop losses in many Asian countries particularly in Bangladesh. It is most common in wetland environments. Sporadic outbreaks have been reported from

Figure 4.51 Dicladispa armigera adult feeding on rice (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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many parts of India (Budhraja et al. 1980, Das 1980, Chandramohan and Tomar 1984). Infestations of hispa have increased since the introduction of high-yielding varieties and improved agronomic practices (Dhaliwal et al. 1980). The extent of damage in Bangladesh reaches 65% (Alam 1967). Many factors have been reported to influence the incidence of hispa in rice fields. Prakasa Rao et al. (1971) reported that top dressing with high levels of nitrogen during periods of pest abundance resulted in greater susceptibility of the rice crop to the pest. Dhaliwal et al. (1980) found hispa incidence to increase with an increase in nitrogen levels from 0 to 100 kg/ha. However, at 150 kg, the infestation considerably decreased. Date of planting influences the ultimate damage caused by hispa. It was shown by Prakasa Rao et al. (1971) that although the July plantings suffered considerable infestation by the two early broods, they soon recovered and reached a stage of least susceptibility for the two succeeding broods. But plantings in August suffered severe damage with less chance of recovery. Weather conditions prevailing in regions of infestation in South India indicate that high humidity after rains and intermittent bright sunshine seem to favour hispa development. In north-eastern India, rainfall was reported to have a negative effect on the activity of hispa (Ghosh et al. 1960). Heavy rainfall in July followed by unusually low rain in August and September was characteristic of epidemic years.

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4.32 African rice hispa, Trichispa sericea (Coleoptera: Chrysomelidae) Several species belonging to the subfamily Hispinae, commonly referred to as 'hispids’, feed on rice in Africa. The term 'hispa' means spiny and characterizes the adults of this group, which have numerous spines on the thorax and abdomen. As reported by Breniere (1983), this group consists of Trichispa sericea Guerin-Meneville, Dicladispa viridicyanea (Kraatz) and Dactylispa bayoni Gestro. Additional Hispinae in the WARDA Arthropod Reference Collection are Agonita sp., Chysispa viridicyanea Weise, Dactylispa spinigera Gyllenhall, Dicladispa paucispino (Weise) and Dorcathispa bellicosa (Guerin). There are likely additional Hispinae species in rice in West Africa whose taxonomic determinations have not yet been made. Trichispa sericea is the species described in detail below because it is a major pest of rice in West Africa, causing severe defoliation, and because of its potential as a Rice Yellow Mottle Virus (RYMV) vector. Geographical distribution: Trichispa sericea – Burkina, Faso, Cameroon, Côte d'Ivoire, Mali, Nigeria, Senegal, Sierra Leone, Togo. In addition to West Africa, T. sericea occurs in many countries throughout Central, East and South Africa (Dale 1994).

Figure 4.52 Trichispa sericea adult (Source: IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Host plants other than rice: Chloris virgata Sw, Echinochloa holubii (Stapf), Eragrostis aethiopica Chiov., Eragrostis heteromera Stapf, Digitaria zeyheri (Nees Hend.) and Diplachne fusca (L.) ex Stapf (Dale 1994). Description and biology: The T. sericea adult (Fig. 4.52) is a dark grey beetle covered with short spines and is about 3-4 mm long (Koudalimoro et al. 2015). Adult females live for 2 wk and lay about 100 eggs during this period. The eggs are white and boat-shaped and are about 1 mm long. The eggs are laid singly in slits made under the epidermis of the upper portion of the leaf. The wound left by the ovipositor is sometimes covered by a dark spot of excreta by the female. The larvae hatch in 3 or 4 d. Trichispa sericea larvae, which are referred to as 'grubs’, are slender, yellow and about 6 mm long. The grubs mine from within the epidermal layer of the leaf. When infested leaves are held against the light, the dark spot of the larva or the pupa in the mine may be visible. The larval period lasts 10 d. Pupation, which lasts about 6 d, takes place in the last mine bored by the larva and within those portions of the leaf lamina that are not submerged. After pupation, the emerging adults migrate to alternate host plants. In Madagascar, T. sericea completes a generation in about 1 mo (Ravelojaona 1970). Plant damage and ecology: Hispids are serious pests of rice in some countries. In addition to rice, a number of grassy weeds serve as hosts for T. sericea (Zongo 1993). In Swaziland, when rice leaves harden and become unattractive for adult feeding and oviposition, T. sericea adults migrate to other plants such as Chloris virgata Sw, Echinochloa holubii (Stapf), Eragrostis aethiopica Chiov., Eragrostis heteromera Stapf, Digitaria zeyheri (Nees Hend.) and Diplachne fusca (L.) Beauv. ex Stapf (COPR 1978). However, rice is the preferred host plant. Trichispa sericea is generally most abundant during the rainy season. However, obtaining detailed data on the seasonal occurrence of T. sericea on the WARDA M'be Farm has been difficult because of the sporadic nature of its occurrence. Annual populations of T. sericea in the monthly planting experiment have been generally low. However, in 1993, extremely high populations were observed during the rainy months of July and August. Trichispa sericea attacks the rice crop in the early growth stages. In Côte d'Ivoire (Heinrichs and Barrion 2004), adults are observed in the rice field shortly after transplanting when they attack small seedlings. Larval feeding occurs through the tillering phase. Both the adults and the larvae feed on the leaf tissues of young rice plants (COPR 1976, Dale 1994). The first attack in a field is highly localized, but the infested area spreads rapidly. Adults feed on the green portion of the leaves, leaving only the epidermal membranes. Adult feeding damage is evident by the characteristic narrow white streaks, or feeding scars, that run along the long axis of the leaf and the irregular brown patches. The larvae mine into the leaf, between the epidermal membranes, and the mining results in brown, blister-like areas. Feeding results in a loss of chlorophyll and the plants wither and die. The most serious damage occurs in nurseries that may be completely destroyed. Severe infestations sporadically occur on transplanted rice and can kill the plants. When the plants survive, they usually recuperate and produce some grain. However, damaged plants often mature late. Trichispa sericea is not a highly mobile insect and can spend several hours feeding on the same plant. It is able to retain and transmit RYMV for one to two days according to the semi-persistent transmission mode. T. sericea was confirmed as an RYMV vector in Niger, Mali, Cameroon and Côte d’Ivoire (Koudalimoro et al. 2015).Trichispa sericea, along with Dactylispa bayoni and Dicladispa viridicyanea, has been reported to transmit © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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rice RYMV in Kenya in East Africa (Bakker 1971). Reckhaus and Andriamasintseheno (1997) list Dicladispa gestroi (Chapman) and T. sericea as RYMV vectors in Madagascar where the disease has significantly impacted rice yields. RYMV was first reported on rice in West Africa in 1976 (Raymundo and Buddenhagen 1976). Symptoms of the virus disease are pale yellow mottled leaves, stunted growth, reduced tillering, asynchronous flowering, poor panicle exsertion, spikelet discolouration and sterility. RYMV was reported in lowland irrigated rice and in mangrove and inland swamps in Guinea during 1982–86 (Fomba 1990), and in upland rice in Côte d'Ivoire in 1985 and Sierra Leone during 1987 (Awoderu et al. 1987). From a distance, infected fields appear yellow. Symptoms on the leaves are linear, chlorotic mottles that coalesce into broken or continuous pale green to yellowish streaks up to 10 cm long. Later, whole plants become light green and then turn to pale yellow. Observations on the WARDA Farm and in farmers' lowland irrigated fields at Sakassou, near Bouake, Côte d'Ivoire, indicate that high populations of T. sericea are usually associated with high incidence of RYMV (Heinrichs and Barrion 2004). In plots planted at WARDA in July and August of 1993, T. sericea populations and RYMV incidence were high and grain yields were low. However, high incidence of RYMV is not always associated with high T. sericea populations, indicating that other insects may be vectors or other means of mechanical transmission may occur. Populations of T. sericea adults are affected by the spacing of transplanted seedlings. Adults in sweep net collections in lowland rice on the WARDA Farm were higher in close spacings of 10 x 10 cm (100 hills m2) than in wider spacings of 20 x 20 (25 hills m2) or 40 x 40 cm (6 hills m2) (Heinrichs et al. 1993). Hispids are prevalent in wetland environments, especially irrigated lowland fields (Reissig et al. 1986). Studies conducted on the continuum toposequence on the WARDA M'be Farm also indicated that damage caused by T. sericea is most prevalent in the lowlands. Per cent leaf area damaged by T. sericea was about 15% in the lowlands and 1% in the uplands of the toposequence (Heinrichs and Barrion 2004). The effect of soil moisture on the extent of T. sericea damage was studied on the WARDA Farm (Heinrichs 1991a). An upland rice variety (IDSA 6) was planted at various intervals along the continuum toposequence from the valley bottom to the hydromorphic zone. Trichispa sericea damage was significantly (positively) correlated with soil moisture percentage. High leaf damage (100%) occurred only at high soil moisture levels. The results indicated that an upland variety growing in standing water constitutes an attractive host for ovipositing T. sericea adults.

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4.33 Rice blue beetle, Leptispa pygmaea Baly (Coleoptera: Chrysomelidae) Distribution: India. Host plants other than rice: Arundinella metzii Hochst., Ischaemum travancorense Stapf, Paspalum scrobiculatum L., Pennisetum purpureum (Schum.), Saccharum officinarum L., Vetiveria zizanioides (L.) Nash (Dale 1994). Description and biology: The biology of the rice blue beetle was studied under cage conditions at Dharwad, Karnataka, India (Krishna Japur et al. 2013). The adult (Fig. 4.53) is a small, metallic bluish, elongated beetle with rows of pits on the elytra, and measuring about 5 mm in length and 1.5 mm in width. Adult females lay oval-shaped eggs, measuring 0.36 mm x 0.16 mm on both sides of the leaf surface, either single or in parallel rows. The incubation period was 4.5 days. The grub (larva) had five instars with a mean developmental period of 10.9 days. The grub pupated on the leaf surface with its posterior end loosely attached to the leaf. The pupal period was 4.4 d and the entire life cycle was completed in 20 d. Longevity of the adult beetle varied with sex, with the male living 37 d and female living 20 d. Plant damage and ecology: Leptispa pygmaea, a minor pest of rice, assumed serious proportions in poorly drained rice fields of central India in 1978. The pest appeared in an epidemic form for the first time during the second crop (July to November) in Maharashtra. Both adults and grubs feed on the surface tissues of rice leaves, leaving long feeding scars

Figure 4.53 Leptispa pygmaea adult (Source: ICAR – National Bureau of Agricultural Insect Resources (NBAIR), India; http://www.nbaii.res.in). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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on the leaf lamina (Prathapan et al. 2009). Damage by the adult is similar to that of the hispa, but the feeding lesions are narrower and more regular in shape and cause less damage than that caused by the grubs (Dale 1994). The attacked leaves become wafer thin, and dry up. They also roll the leaves inward, which attract other insects to come and take shelter inside. This pest usually appears along with that of the rice hispa, thus aggravating the damage done by it to the rice crop. The pest survives the off-season (November–February) in the adult stage on grasses, volunteer rice plants and ratoon rice or on sugarcane. The activity of the pest is at its lowest during this period. No egg laying has been observed on the alternate hosts during the pest’s inactive stage (Khanvikar et al. 1983).

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4.34 Rice leaf beetle, Oulema oryzae (Kuwayama) (Coleoptera: Chrysomelidae) Distribution: China, Japan, Korea, Ryukyu Islands, eastern Siberia, Taiwan (Dale 1994). Host plants other than rice: Dactylis glomerata L., Glyceria tonglensis C. B. Clarke, Leersia oryzoides (L.) Sw., Phragmites australis (Cav.) Trin. ex Steud., Zizania latifolia (Griseb.) Turez. ex Stapf (Dale 1994). Description and biology: Adult beetles (Fig. 4.54) have shiny black elytra with straight rows of pits, head and antennae are black and the thorax reddish brown. The females deposit cylindrical eggs in masses on the upper surface of leaves. The oviposition period lasts 15 days and incubation varies from 5 to 11 days. The life of the adult extends for one year or more (Dale 1994). The brown larvae are globular in shape and rather heavily sclerotized and with dark brown nodules on a yellow base. They cover their body with dark greenish excreta and appear as mud on leaves. The larval period is 13-19 days. The full-grown larva pupates within an ellipsoidal whitish cocoon mostly on the rice leaves, though in upland fields, pupation sometimes takes place on or under the ground. There is one generation per year and overwintering occurs in the adult stage. In Japan, the increase in the number of leaf beetles often coincides with the transplanting of rice seedlings. The beetles leave their hibernating sites by late May, mate and start laying eggs

Figure 4.54 Oulema oryzae adult (Source: http://www.boujo.net/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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by early June. Oviposition continues until nearly the end of July. Then the adults bury themselves in the debris of mountain bush and under the roots of grasses. O. oryzae is highly adaptable to low temperatures. In the north temperate regions of Japan, female beetles stop depositing eggs early and adult longevity is shortened if the atmospheric temperature rises early in summer. On the other hand, when cooler days continue to prevail in summer, the hibernating adults survive for a longer time in the field and oviposition continues longer (Kuwayama 1966). Plant damage and ecology: Oulema oryzae occurs in upland and wetland environments and is one of the serious pests of rice in northern Japan, Korea and China leading to crop losses of up to 30%. The percentage of yield reduction in Japan is computed as 0.25 of the percentage of injured leaves. In Taiwan, it infests the first crop in the mountain regions. Both adults and larvae feed on the leaf surface causing a scorched appearance of the foliage. Larvae skeletonize leaf blades in a linear fashion. In short-duration rice varieties, plants often do not recover from O. oryzae damage. Retardation of plant growth and decrease in the number of leaves and tillers has been observed (Kojima and Emura 1979). Ripening of grains in infested plants is considerably delayed leading to reduction in both quality and quantity of grain yield. In cases of severe infestation, the plants die and the fields present an appearance of having been burned by fire. In Japan, damage varies from 5% to 10% when slight and 20% to 30% when severe. The tolerable injury level is set at 20% injured leaves in late June (Koyama 1978).

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4.35 Flea beetles, Chaetocnema spp. (Coleoptera: Chrysomelidae) The term 'flea beetle' is applied to a group of small beetles that have enlarged hind legs and jump when disturbed. This group consists of several chrysomelid genera, including Chaetocnema, which make small holes in the leaf when feeding. Although Chaetocnema spp. are extremely abundant in upland rice, in West Africa, the feeding damage that they cause is minimal and they are considered to be minor pests. However, they are vectors of RYMV (Heinrichs and Barrion 2004). Distribution: Chaetocnema pulla Chapuis (= C. zeae Bryant) – Burkina Faso, Côte d'Ivoire, Mali, Kenya, Tanzania; Chaetocnema pusilla Laboissiere – Burkina Faso, Côte d'Ivoire, Mali; Chaetocnema sp.– Burkina Faso, Côte d'Ivoire, Guinea, Guinea-Bissau, Nigeria. Host plants other than rice: Chaetocnema pulla – Zea mays L., Cyperus sp., Pennisetum glaucum (L.). Description and biology: Chaetocnema spp. have metathoracic femora that are enlarged for jumping (Barrion and Litsinger 1994). Chaetocnema pulla (Fig. 4.55) are very small metallic black beetles measuring about 0.2 mm in length and 0.1 mm in width and are also characterized by a tooth on the dorsal side of the intermediate posterior tibiae (Bakker 1971). Biondi and D’Alessandro (2008) revised the Chaetocnema pulla species group from

Figure 4.55 Chaetocnema pulla adult (Source: Mike Adams; http://www.dpvweb.net/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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the Afrotropical region with description of a new species from Central Africa. C. pulla differs from other Chaetocnema spp. in that the pronotum is smooth except for very fine punctures. Also, the apical 5–6 segments of the antenna are brownish to brownish red (Heinrichs and Barrion 2004). Information on the biology of Chaetocnema spp. on rice is lacking (Bakker 1974; Nwilene 1999). Doval et al. (1975) reported on the biology of C. basalis in wheat in India. Eggs are laid singly or in batches of 20–200 in soil crevices or on the upper soil surface during the early morning. After about 5 d, the eggs hatch and the creamy white larvae feed on root hairs. After three moults, during a period of 10–20 d, the larvae pupate in soil crevices 5–7 cm deep or under loose stubble. The pupal period lasts 7–15 d. Adults are active during the day. There are two generations during the crop season. The adult hibernates or migrates to alternate host plants during the dry season. Plant damage and ecology: The feeding of the adult beetle produces distinctive narrow scraped areas on the leaves. The beetle causes plant damage similar to that of the ladybird beetle, Chnootriba similis (Mulsant). However, damage differs from that of C. similis in that the whitish streaks on the leaves, where the green material has been removed, are narrower because of the beetle's small size. Larvae develop on the roots of grasses in fallow upland areas and are not rice pests (Shepard et al. 1995). Several species of Chaetocnema have been recorded as minor feeders of rice throughout the world. Grist and Lever (1969) mention C. obesula Lec., C. basalis (Baly) and C. gregaria Weise. Bakker (1974) reported C. abyssinica Jac., C. concinnipennis Baly, C. kenyensis Bryant, C. pallidipes Fairm., C. pulla and C. pusilla on rice and grasses around rice fields in Kenya. Having numerous host plants, Chaetocnema spp. are polyphagous. According to Bakker (1974), plants belonging to families Polygonaceae and Chenopodiaceae are often preferred host plants, but several species feed on cereals. Chaetocnema pulla, in addition to feeding on rice, is reported as a serious pest of maize and millet in Sierra Leone (Hargreaves 1936 as cited in Bakker 1974). Furth (1985) reported Cyperus sp. as the food plant of C. conducta suturalis Bryant, C. juba Bechyne and C. nigripennis Lab. in East Africa and grasses as hosts of C. wollastoni Baly in Chad, South Africa, Sudan and Zaire. Although flea beetles are often very abundant, they are very small and the amount of feeding damage is usually minimal. Chaetocnema spp. are primarily pests of economic significance because they mechanically transmit RYMV, a serious rice disease. Bakker (1974) mentioned C. abyssinica, C. kenyensis and C. pulla as the Chaetocnema spp. transmitting RYMV in Kenya; Reckhaus and Andriamasintseheno (1997) reported C. pulla as an RYMV vector in Madagascar; and Banwo et al. (2001) reported C. pulla and Chaetocnema sp. as vectors in Tanzania. Koudalimoro et al. (2015) reported that C. pulla was confirmed as an RYMV vector in Sierra Leone, Madagascar, Tanzania, Cameroon and Côte d’Ivoire. C. pulla is a highly mobile insect which has short feeding periods on the same plant, inducing a fast dissemination of the virus. It can acquire and retain the virus for about six days but is unable to transmit the virus for more than three days (Koudalimoro et al. 2015). This insect is more abundant on upland rice than in lowland and irrigated ecologies (Koudalimoro et al. 2015).Studies indicate that Chaetocnema spp. may be present in upland fields throughout the crop but are more abundant at later growth stages. In the 1995 Côte d'Ivoire survey, beetles were present in vegetative, booting and ripening crops with slightly larger populations in the latter. Studies on the continuum toposequence,

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on the WARDA Farm, indicated that the beetles were first collected in sweep nets at 9 weeks after sowing (WAS). Chaetocnema spp., being pests of upland rice, are present during the rainy season when upland rice is grown in West Africa (Heinrichs and Barrion 2004). In three surveys conducted in Côte d'Ivoire and one in Guinea, during the 1995 rainy season, Chaetocnema adults were among the most abundant insect groups in sweep net collections (Heinrichs and Barrion 2004). In both countries, they were equally abundant in the humid tropical (forest) and the savanna zone. In Latin America, intensification of crop management practices, for example, land preparation, high seeding density and high water level have been shown to result in decreasing importance of Chaetocnema spp. in lowland rice (Weber and Parada 1994).

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4.36 Ladybird beetle, Chnootriba similis (Mulsant) (Coleoptera: Coccinellidae) Distribution: Chnootriba similis (Mulsant) occurs in West Africa, East Africa and in the Ethiopian region (Raimundo 1992). It is generally distributed throughout West Africa and probably occurs in all African countries. In West Africa it has been recorded from Benin, Burkina Faso, Cameroon, Chad, Côte d'Ivoire, Ghana, Guinea, Guinea-Bissau, Liberia, Niger, Nigeria, Senegal and Togo. Host plants other than rice: Eragrostis tef (Zucc.), Glycine max (L.) Merr., Hordeum vulgare L., Pennisetum glaucum (L.) R. Br., Pennisetum purpureum Schumach, Solanum tuberosum L., Sorghum bicolor (L.) Moench, Triticum aestivum L., Zea mays L. and several other species. Description and biology: Adults are oval, hemispherical beetles of about 6 mm in length and orange red with six black spots on each elytron (wing cover) (Breniere 1983). There is variability in the arrangement of the spots on the wing cover (Raimundo 1992). Certain spots on the wing cover are isolated or more or less coalesced in some individuals (Fig. 4.56). The adults are very good fliers. The eggs are laid in clusters of 20-50. Usually the eggs are laid on the underside of the leaves in a vertical position. The colour is pale yellow. They are elongate oval and have a hexagonal sculpturing. They are about 0.5 mm long and have an incubation period is 3–4 d. Upon hatching, the young larvae from the same egg batch remain aggregated for a period and then disperse. Their body is covered with stiff, short bristles or spines. The larvae are dark grey to black with white spines when they are young but become whitish

Figure 4.56 Chnootriba similis adult (Source: Guido.Coza.iSpot share nature). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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as they develop. In laboratory studies on maize (Scheibelreiter and Inyang 1974), the larval period was 9–17 d. The pupa is dark yellow. It is found on the leaves of the host plant. Due to temperature differences, time for development from egg to adult takes 4–5 wk. in the dry season and 7–8 wk. in the wet season. Plant damage and ecology: C. similis is one of the most common insect pests of upland rice in West Africa, but the extent of plant damage it causes is generally minimal. Although most species in the family Coccinellidae are predators feeding on other insects, some of the Epilachninae subfamily are phytophagous. Chnootriba similis is polyphagous and, according to Breniere (1983), is particularly attracted to gramineous plants especially rice, sugarcane, maize and sorghum. The adult and larval stages of this beetle are severe pests of nursery rice. They feed on the leaves, scraping off sections along the length of the leaf, leaving white streaks or irregular patches, where the chlorophyll-bearing tissue has been removed. They leave the epidermis and the veins intact. This type of damage is called ‘windowing’. Heavily attacked leaves are skeletonized and eventually dry up. Severely infested nurseries take on a silvery appearance. Feeding studies on maize (Scheibelreiter and Inyang 1974) indicate that one larva can eat a section of leaf 3 cm long (1,000 mm2) in about 12 d. The fourth instar larvae do about 80% of the feeding damage within 4-5 d. Thus, the larvae from four to five egg batches are able to destroy the total leaf surface of 2-3-wk-old maize plants, which often kills them. In addition to the direct feeding damage caused by C. similis on rice, several studies have confirmed that C. similis is also a vector of RYMV (Nwilene et al. 2009; Koudalimoro et al. 2014; Abo et al. 2004). In a study in lowland rice at WARDA, C. similis attacked the crop in the vegetative stage (Heinrichs 1991b). The adult beetle population in sweep net collections was highest in the first 2 WAT and continued at low levels until 5 WAT. Populations of C. similis adults on the continuum toposequence at WARDA, where the insect was most abundant in the upland sites, were highest in the later crop growth stages. The insects were first collected at the panicle initiation stage [9 WAS], and collections continued to near harvest (17 WAS). Chnootriba similis is primarily a pest of upland rice in West Africa. Alam (1992) reports populations in both upland and lowland rice with highest populations in the former. In the 1995 Côte d'Ivoire survey, C. similis populations were 11 per 500 sweeps in the upland fields and 1 per 500 sweeps in lowland fields (Heinrichs and Barrion 2004). Studies on the continuum toposequence on the WARDA M'be Farm indicated a trend similar to that of Chaetocnema. Populations occurred in all ecologies but were highest in the uplands. Nonweeded plots had populations two to three times those of the weeded plots. Chnootriba similis is primarily an upland pest so the insect is present during the rainy season when upland rice is grown. Studies on the length of fallow periods in slash-and-burn agriculture in the forest zone near Gagnoa, Côte d'Ivoire, indicate a weak negative (r= –0.23, p= 0.32) correlation between the length of fallow (1–35 years) and the C. similis populations in upland rice (Heinrichs and Barrion 2004). Chnootriba similis occurs in all climatic zones, from the humid tropical to the Sudanian savanna, in Nigeria (Alam 1992). In the July 1995 survey in Côte d'Ivoire, populations were 10 times higher in the forest (humid tropical) zone than in the Guinean savanna (Heinrichs and Barrion 2004). In the 1995 survey of Guinea, populations were similar in both the forest and savanna zones.

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4.37  Foliage feeding aphids Many aphid species (Homoptera: Aphididae) infest the aerial parts of rice even though rice is not the primary host plant for most of them. A list of aphids reported on rice with their geographical distribution is provided in Table 4.2. The rusty plum aphid Hysteroneura setariae feeds on the leaves and unripened grains of rice. Moderately infested grains show brown necrotic spots. A heavy infestation turns all spikelets brown and chaffy. Severe attacks by this aphid have been reported from countries such as Sierra Leone (Akibo-Betts and Raymundo 1978), India (Garg and Sethi 1979) and Nigeria (Akinlosotu 1980). The wingless adults of H. setariae are 3-4 mm long and are rusty to dark brown in colour. Nymphs are pink. The average nymphal period is 10 days. In Africa, the aphid appears in large numbers with the May rains and remains active on the rice crop until December. However, heavy rains greatly reduce its population during August–October. In India, this aphid is found on rice throughout the season. Rhopalosiphum padi (Fig. 4.57) is known as the bird cherry oat aphid and the apple grain aphid. It is a vector of the virus disease ‘giallume’ (yellow disease or rice yellows) in Italy. The primary host of this aphid species in Italy is the fruit tree Prunus padus. When P. padus is not available, the aphid overwinters on secondary hosts such as rice and various grasses.

Figure 4.57 Rhopalosiphum padi (Source: http://www.forestryimages.org/).

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Table 4.2 Distribution of aphid species feeding on rice foliage (Yano et al 1983) Aphid species

Host plants

Distribution

Aphis craccivora Koch

Rice, many plants

Many countries

Aphis gossypii Glover

Rice, many plants

Cosmopolitan, absent only from the colder parts of Asia and Canada

Brachysiphoniella montana (van der Goot)

Rice

India

Diuraphis noocia (Mordivilko ex Kurdjumov)

Rice, grasses

North Africa

Hysteroneura setariae (Thomas)

Rice

India, Philippines, Thailand, West Africa

Melanaphis sacchari (Zehntner)

Rice, sugarcane, sorghum, maize, wheat, grasses

Japan, Philippines

Metopolophium dirhodum (Walker)

Rice, grasses

Central Asia

Myzus persicae (Sulzer)

Rice, many crop plants, weeds

Virtually cosmopolitan

Rhopalosiphum maidis (Fitch)

Rice, many crop plants, some weeds

Throughout the tropics, subtropics and the warmer temperate regions

Rhopalosiphum nymphaeae (L.)

Rice, Monochoria vaginalis, Saginaria, Trifolia, Prunus spp.

Bangladesh, Fiji, North America, Philippines, Spain, Taiwan

Rhopalosiphum padi (L.)

Rice, many plants belonging to Gramineae and Cyperaceae

Africa, America, Asia, Australia, Europe

Rhopalosiphum sp.

Rice

Japan

Schizaphis graminum (Rondani)

Rice, wheat, barley, oats, Italian Africa, Asia, South America, the millet United States

Sipha glyceriae (Kaltenbach) Rice, grasses

Italy

Sitobion akebiae (Shinji)

Rice, wheat, wild weeds

Japan, Korea

S. avenue (F.)

Rice, grasses

Europe, North America, Taiwan

S. fragariae (Walker)

Rice

Spain

S. graminis (Takahashi)

Rice, grasses

Oriental and Ethiopian regions

S. miscanthi (Takahashi)

Rice, graminaceous plants

Australia, China, New Zealand, Philippines, South Pacific region, Taiwan

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4.38 References Abdou, S. 1992. Report on the status of research on plant protection in rice in Niger [in French]. Paper presented at the IPM Task Force Meeting, 19–20 February 1992, West Africa Rice Development Association, Bouaké, Côte d’Ivoire. Abo, M. E. 1998. Studies on the transmission of rice yellow mottle virus (RYMV). PhD dissertation, Ahmadu Bello University, Zaria, Nigeria, 200p. Abo, M. E., Alegbejo, M. D., Sy, A. A., Sere, Y. 2004. Retention and transmission of Rice yellow mottle virus (RYMV) by beetle vectors in Cote d’Ivoire, Agronomie Africaine 16 :71–6. Abo, M. E., Sy, A. A., Alegbejo, M. D. 1998. Rice yellow mottle virus (RYMV) in Africa: evolution, distribution, economic significance on sustainable production and management strategies. J. Sustainable Agric. 11 (2/3):85–111 Acharya, L. P. 1967. Life history, bionomics and morphology of the rice hispa. Hispa armigera Olivier. M.Sc. (Ag.) thesis, University of Agriculture and Technology, Bhubaneswar, India. Agyen-Sampong, M. 1975. Hieroglyphus daganensis Krauss (Orthoptera: Acrididae), a new pest of rice in northern Ghana. Ghana J. Agric. Sci. 8:249–53. Akibo-Betts, D. T., Raymundo, S. A. 1978. Aphids, Hysteroneura setariae and Tetraneura nigriabdominalis as rice pests in Sierra Leone. Int. Rice Res. Newsl. 3(6):15–16. Akinlosotu, T. A. 1980. Outbreak of the rusty plum aphid, Hysteroneura setariae Th. (Homoptera, Aphididae), on rice (Oryza sativa L.) in Ibadan, Nigeria. Ghana J. Agric. Sci. 10:149–50. Akinsola, E. A., Coly, A. 1984. Irrigated rice pests at Fanaye, Senegal. WARDA Tech Newsl 5(1):21–2. Alam, M. A., Khatri, A. K., Jakhmola, S. S., Rathore, V. S. 1980. Losses caused by Mythimna separata Walker to rice. Indian J. Agric. Sci. 50:709–11. Alam, M. S. 1989. Whitefly (Hemiptera: Aleyrodidae) — a potential pest of rice in West Africa. Int. Rice Res. Newsl. 14(3):38–9. Alam, M. S. 1992. A survey of rice pests in Nigeria. Trop. Pest Manage. 38:115–18. Alam, M. Z. 1967. Insect pests of rice in East Pakistan. In International Rice Research Institute (Ed.), The Major Insect Pests of the Rice Plant, pp. 643–55. Proceedings of a symposium at the International Rice Research Institute, September, 1964. Johns Hopkins Press, Baltimore, USA. Alam, S. 1974. Pests of deep-water rice in Bangladesh. In Deep-water rice in Bangladesh, Bangladesh Rice Research Institute, Dacca, Bangladesh, pp. 140–50. Alam, S., Nurullah, C. M. 1977. Ear-cutting caterpillar. In Literature Review of Insect Pests and Diseases of Rice in Bangladesh, Bangladesh Rice Research Institute, Dacca, Bangladesh, pp. 3–44. Ananthanarayanan, K. P., Ramakrishna Ayyar, T. V. 1937. Bionomics of the swarming caterpillar of paddy rice in South India. Agric. Livestock India 7:725–34. Ando, T., Kishino, K., Tatsuki, S., Takahashi, N. 1980. Sex pheromones of the rice green caterpillar: Chemical identification of three components and field tests with synthetic pheromones. Agric. Biol. Chem. 44:765–75. Anonymous. 1983. Integrated Pest Management for Rice. University of California, Statewide Integrated Pest Management Project, Division of Agricultural Sciences Publication 3280. Asahina, S., Turuoka, Y. 1969. Records of the insects visiting a weather ship located at the Ocean Weather Station ‘Tango’ in the Pacific, III. Kontyu 37:290–304. Awoderu, V. A., Alam, M. S., Thottapilly, G., Alluri, K. 1987. Outbreaks and new records. Ivory Coast. Rice yellow mottle virus in upland rice. FAO Plant Prot. Bull. 35(1):32–3. Bakker, W. 1971. Three new beetle vectors of rice yellow mottle virus in Kenya. Neth. J. Plant Pathol. 77:201–6. Bakker, W. 1974. Characterization and ecological aspects of rice yellow mottle virus in Kenya. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands. Bandong, J. P., Litsinger, J. A. 1988. Development of action control thresholds for major rice pests. In Pesticide Management and Integrated Pest Management in Southeast Asia, Publisher: Consortium for International Crop Protection (CICP), USAID, College Park, MD, P.S. Teng, K.L. Heong (Eds), pp. 95–102.

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Banwo, O. O., Makundi, R. H., Abdallah, R. S., Mbapila, J. C. 2001. Newly recorded species of Chaetocnema, vector of rice yellow mottle virus in Tanzania. New Zealand J. Crop Hortic. 29: 61–5. Barrion, A. T., Litsinger, J. A. 1987. Meadow grasshopper Conocephalus longipennis damage to rice spikelets. Int. Rice Res. Newsl. 12(1):18. Barwal R. N. 1983. Outbreak of rice ear-cutting caterpillar Mythimna separata (Walker) in Manipur, India. Intl. Rice Res. Newsl. 8(5):11–12. Basu, S. K. 1979. Whorl maggot damage on flag leaf. Int. Rice Res. Newsl. 4(3):20–1. Basu, A. C., Banerjee, S. N. 1957. Study on the assessment of damage done by Hispa armigera Ol. to paddy crop. Indian J. Agric. Sci. 27:295–301. Bautista, R. C., Heinrichs, E. A., Rejesus, R. S. 1984. Economic injury levels for the rice leaffolder Cnaphalocrocis medinalis (Lepidoptera: Pyralidae): insect infestation and artificial leaf removal. Environ. Entomol. 13:439–43. Bharodia, R. K., Talati, G. M. 1976. Biology of Tetranychus neocaledonicus Andre (Acarina: Tetranychidae), a pest of Gossypium hirsutum L. Gujarat Agric. Univ. J. 2:15–20. Biondi, M., D’Alessandro, P. 2008. Revision of the Chaetocnema pulla species-group from the Afrotropical region with description of a new species from Central Africa. In Research on Chrysomelidae, Publisher: Brill, Leiden-Boston, Editors: Jolivet P., Santiago-Blay J., Schmitt M., pp. 265–285. Borror, D. J., De Long, D. M., Triplehorn, C. A. 1981. An Introduction To The Study of Insects. 5th ed. Saunders College Publishing, New York. Bradley, J. D. 1981. Marasmia patnalis sp. n. (Lepidoptera: Pyralidae) on rice in SE Asia. Bull. Entomol. Res. 71:323–7. Brenière J. 1983. The Principal Insect Pests of Rice in West Africa and Their Control. West Africa Development Association, Monrovia, Liberia. Budhraja, K., Rawat, R. R., Singh, O. P. 1979. Feeding behavior of Dicladispa armigera. Int. Rice Res. Newsl. 4(6):15–16. Budhraja, K., Rawat, R. R., Singh, O. P. 1980. Extent of recuperation from attack of Dicladispa armigera after insecticidal control in some rice varieties. Int. Rice Res. Newsl. 5(2):6. CABI. 2016a. Invasive Species Compendium. Hieroglyphus banian (rice grasshopper). http://www. cabi.org/isc/datasheet/27164 CABI. 2016b. Marasmia patnalis (rice leafroller). Invasive Species Compendium. http://www.cabi.org/ isc/datasheet/32497 CABI. 2016c. Susumia exigua. [Distribution map]. Invasive Species Compendium. http://www.cabi. org/isc/abstract/20056600365 CABI. 2016d. Melanitis leda ismene (rice butterfly). Invasive Species Compendium. http://www.cabi. org/isc/datasheet/34400 CABI. 2016e. Pelopidas mathias (rice skipper). Invasive Species Compendium. http://www.cabi.org/ isc/datasheet/39504 CABI. 2016f. Mythimna separata (paddy armyworm). Invasive Species Compendium. http://www. cabi.org/isc/datasheet/45093 CABI. 2016g. Spodoptera litura. [Distribution map].Invasive Species Compendium. http://www.cabi. org/isc/abstract/20046600061 CABI. 2016h. Dicladispa armigera (rice hispa) Invasive Species Compendium. http://www.cabi.org/ isc/datasheet/27270 CAB International. 2015. Spodoptera mauritia. [Distribution map]. cabdirect. Distribution Maps of Plant Pests 1973 No. June pp. Map 162 (Revised) http://www.cabdirect.org/abstracts/20056600162. html;jsessionid=7FE20C693CF68D87E8F632EFC9297A30 Casmuz, A., Juárez, M. L., Socias, M. G., Murúa, M. G., Prieto, S., Medna, S., Willink, E., Gastaminza, G. 2010. Revisión de los hospederos del gusano cogollero del maíz, Spodoptera frugiperda (Lepidoptera: Noctuidae). Revista de la Sociedad Entomológica Argentina 69(3–4):209–31. Chandramohan, N., Jayaraj, S. 1977. Effect of different levels of nitrogen and age of the crop on the incidence of rice leaf roller. Madras Agric. J. 64:684–5. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Prakasa Rao, P. S., Israel, P., Rao, Y. S. 1971. Epidemiology and control of the rice hispa Dicladispa armigera Oliver. Oryza 4:345–59. Prathapan, K. D., Chaboo, C. S., Karthikeyan, K. 2009. Natural history and leaf shelter construction of the Asian rice leptispa beetle Leptispa pygmaea Baly (Coleoptera: Chrysomelidae: Cassidinae: Leptispini). Zoological Studies 48:625–31. Radhakrishnan V., Ramaraju K. 2009. Development durations, colonization and insecticide efficacy of leaf mite, Oligonychus oryzae Hirst on rice. Tropical Agric. Res. 21(1):30–8. Raimundo, A. C. 1992. Contribução para o conhecimento dos coccinelideos da Guiné-Bissau (Coleoptera: Coccinellidae). Bolm. Soc. Portuguesa Ent. V-6(138):65–81. Rajamma, P, Das, N. M. 1969. Studies on the biology of the rice leafroller Cnaphalocrocis medinalis Guen. Agric. Res.J. Kerala 7:110–12. Ramamurthy, V. V., Kumaraswami, T., Jayaraj, S. 1977. Effect of whorl maggot damage on the contents of chlorophyll and reduced sugars and uptake of nutrients in rice seedlings. Madras Agric. J. 64:405–6. Ramasubbaiah, K., Sanjeeva Rao, P., Venugopala Rao, N., Ganeswara Rao, A. 1980. Nature of damage and control of rice leaf roller, Cnaphalocrocis medinalis Guen. Indian J. Entomol. 42:214–17. Ravelojaona, G. 1970. Observations sur la dynamique des populations de Trichispa sericea Guerin, Coléoptère Hispinae nuisible au riz à Madagascar. Comptes Rendus Seances Soc. de Biol. de Madagascar 164:474–6. Raymundo,S. A. and Buddenhagen, I. W. 1976. A rice virus disease in West Africa. Int. Rice Comm. Newsl. 25(12):58. Reckhaus, P. M., Andriamasintseheno, H. F. 1997. Rice yellow mottle virus in Madagascar and its epidemiology in the northwest of the Island. Z. Pflanzenkr. Pflanzenschutz 104:289–95. Regupathy, A., Subramanian, A. 1972. Effect of different doses of fertilizers on the mineral metabolism of IR8 rice in relation to its susceptibility to gall fly Pachydiplosis oryzae Wood-Mason and leaf roller, Cnaphalocrocis medinalis Guenee. Oryza 9:81–5. Reissig, W. H., Heinrichs, E. A., Litsinger, J. A., Moody, K., Fiedler, L., Mew, T. W., Barrion, A. T. 1986. Illustrated Guide to Integrated Pest Managment of Rice in Tropical Asia. International Rice Research Institute, Los Baños, Laguna, Philippines, p. 411. Rice, S. R., Grigarick, A. A., Way, M. O. 1982a. Relationship of larval density and instars of Pseudaletia unipuncta to rice leaf feeding. Environ. Entomol. 11:648–51. Rice, S. R., Grigarick, A. A., Way, M. O. 1982b. Effect of the leaf panicle feeding by armyworm (Lepidoptera: Noctuidae) larvae on rice grain yield. J. Econ. Entomol. 75:593–5 Rothschild, G. H. L. 1969. Observations on the armyworm Spodoptera mauritia acronyctoides Gn. (Lep., Noctuidae) in Sarawak Malaysian Borneo. Bull. Entomol. Res. 59:143–60. Rothschild, G. H. L. 1970. Observations on the ecology of the rice ear bug (Leptocorisa oratorius F.) (Hemiptera: Alydidae) in Sarawak (Malaysian Borneo). J. Appl. Ecol. 7:147–67. Rubia, E. G., Ferrer, E. R., Shepard, B. M. 1990. Biology and predatory behaviour of Conocephalus longipennis (de Haan) (Orthoptera: Tettigoniidae), a predator of some rice pests. J. Plant Prot. Trop. 7:47–54. Sain, M. 2000. Bionomics andmanagement of rice whorl maggot-Hydrellia spp. (Diptera: Ephydridae) – a review. Agric. Rev. 21:10–15. Sain, M., Bentur, J. S., Kalode, M. B. 1983. Boot leaf and spikelet damage in rice by whorl maggot Hydrellia philippina Ferino. Int. Rice Res. Newsl. 7(5):18–19. Sasidharan, N. K., Kurup, A. E. S, Vijayan, M, Santha Kumari, S. 1979. Incidence of whorl maggot in Onattukara, Kerala, India. Int. Rice Res. Newsl. 4(5):20. Sathiyananadam, V. K. R., Venugopal, M. S., Kareem, A. A. 1984. Controlling armyworm with synthetic pyrethroids and conventional insecticides. Intl. Rice Res. Newsl. 9(2):20. Sato, T., Kishino, K. 1978. Ecological studies on the occurrence of paddy leaf roller, Cnaphalocrocis medinalis Guenee. Bull. Tohoku Natl. Agric. Exp. Stn. 58:47–80. Scheibelreiter, G. 1973. Notes on the biology of Cerodontha orbitona Spencer (Diptera, Agromyzidae)–a new leaf miner on rice. Ghana J. Agric. Sci. 6:127–31.

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Chapter 5 Biology and ecology of rice-feeding insects: panicle feeders E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 5.1 Introduction 5.2 Stink bugs 5.3 Alydid bugs 5.4 Rice bugs 5.5 Aspavia 5.6 Southern green stink bug 5.7 Rice stink bugs 5.8 Earwigs 5.9 Blister beetles 5.10 Panicle thrips 5.11 References

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5.1 Introduction Insects that attack rice panicles can be classified into those that feed on the floral parts (mostly the pollen) and the stink bugs that suck the milk-like sap from the developing grains. Insects that feed on the floral parts, such as earwigs, blister beetles and panicle thrips, prevent the spikelet from filling and thus it remains empty and aborts. Numerous hemipteran insect species belonging to the Alydidae, Coreidae, Pentatomidae and Pyrrhocoridae families suck the milk-like sap from the developing rice grains. Depending on the time of attack, in relation to stage of grain development, direct damage by milk (liquid endosperm) removal may completely or partially destroy the grain. In addition to the direct damage caused by the feeding of the bugs, secondary pathogens may enter the feeding wounds left by the bugs and cause a staining of the grain that cannot be removed in milling. This is referred to as ‘pecky rice’ that is prone to breakage in milling and lowering of the grain quality. The ‘dirty-panicle’ symptom often observed in rice fields is believed to be caused by a combination of bug feeding and fungal infection (Agyen-Sampong and Fannah 1980). In this section, the grain-sucking bugs are discussed first, followed by the floral feeders.

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5.2  Stink bugs The characteristic foul odour produced by scent glands on the abdomen of these insects has led them to be commonly called ‘stink bugs’. About 60 stink bug species have been reported to infest rice fields and at least half of them are considered pests causing yield loss or pecky rice. ‘Pecky rice’ is referred to as the condition of the grain after being sucked by stink bugs and partially or wholly stained by bacteria or fungi. If a sample of rice contains some pecky grains, the whole lot is considered contaminated and the market price is decreased in some countries. An emphasis on rice has shifted from yield to quality. In Japan, the inspection for rice grain quality has become stricter and the pecky rice problem has assumed increasing importance. The major bug species causing pecky rice are listed in Table 5.1.

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Table 5.1 Bugs that cause pecky rice (Kisimoto 1983, Dale 1994, Heinrichs and Barrion 2004, Pathak and Khan 1994) Family

Species

Distribution

Alydidae

Leptocorisa acuta (Thunb.)

Asia, Australia, Oceania, Central America

L. chinensis (Dallas)

Japan

L. varicornis F.

India

L. oratorius (F.)

Asia, Australia, Oceania

Mirperus jaculus Thunberg

West Africa

Riptortus dentipes (F.)

West Africa

Stenocoris apicalis (Westwood)

West Africa

S. claviformis (Ahmad)

West Africa

S. elegans (Blote)

West Africa

Coreidae

Cletus punctiger Dallas

Japan

Lygaeidae

Nysius plebejus Distant

Japan

Togo hemipterus Scott

Japan

Stenodema sibiricum Bergroth

Japan

Trigonotylus coelestialium Kirkaldy

Japan

Aspavia armigera F.

West Africa

A. acuminata Montandon

West Africa

A. brunnea (Signoret)

West Africa

A. hastator (F.)

West Africa

Dolycoris baccanum L.

Japan

Eysarcoris lewisi Distant

Japan

E. parvus Uhler

Japan

E. ventralis Westwood

Japan

Lagynotomus elongatus Dallas

Japan

Nezara antennata Scott

Japan

N. viridula (L.)

Worldwide

Oebalus pugnax (F.)

United States, Caribbean

O. ornata (Sailer)

Caribbean

O. poecilus Dallas

South America

O. ypsilongresius (De Geer)

Caribbean and northern South America

O. insularis (Stål)

Central America, Mexico, Colombia

Scotinophara lurida Burmeister

Southeast Asia, China, Indonesia, India

Aeschynteles maculatus Fieber

Japan

Miridae Pentatomidae

Ropalidae

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5.3 Alydid bugs, Stenocoris spp., Mirperus spp., Riptortus dentipes (Hemiptera: Alydidae) Various alydid bugs are pests of rice worldwide. The alydids are distinguished from the pentatomids by their long, slender body and lack of a large scutellum. There are several alydids in the genera Riptortus and Stenocoris in rice in West Africa and their biology, ecology and the damage they do to plants are similar (Heinrichs and Barrion 2004). Thus, a representative genus, Stenocoris, which is extremely abundant in Côte d'Ivoire, is primarily discussed herein. Distribution: Mirperus jaculus Thunberg – Benin, Burkina Faso, Côte d'Ivoire, Guinea, Guinea-Bissau, Mali, Nigeria, Togo; Riptortus dentipes (F.) – Benin, Burkina Faso, Côte d'Ivoire, Ghana, Guinea, Guinea-Bissau, Mali, Nigeria, Togo; Stenocoris apicalis (Westwood) – Cameroon, Côte d'Ivoire, Gambia, Togo; S. claviformis – Burkina Faso, Côte d'Ivoire, Liberia, Nigeria, Sierra Leone; S. elegans (Blote) – Côte d’Ivoire, Liberia, Nigeria. The distribution of the alydids on rice in West Africa is likely much more widespread than what the literature indicates. Host plants other than rice: Many grasses serve as hosts for the alydids, with rice and Echinochloa being important (Reissig et al. 1986). Riptortus dentipes is also a pest of soya bean (Ogunwolu 1992) and cowpea (Kaemba and Khamala 1981) in Nigeria. Description and biology: Linnavuori (1987) published notes on the taxonomy, habitats and distribution of the Alydidae in West and Central Africa. Stenocoris spp. (Fig. 5.1) closely resemble the Asian rice stink bugs, Leptocorisa spp. (Hemiptera: Alydidae) (Figs. 5.4, 5.5, 5.8, 5.9). The body is elongated and slender. Nymphs are reddish. The three pairs of legs are similar in shape and size, which distinguishes Stenocoris from some of the other alydid bugs on rice, such as Mirperus jaculus (Fig. 5.2) and Riptortus dentipes (Heinrichs and Barrion 2004). Riptortus (Fig. 5.3) is stout and varies from light to dark brown and has an enlarged third pair of legs. Stenocoris may also be identified by the three white spots on the lateral side. Alydid eggs are laid in small groups on the leaves (Reissig et al. 1986). One female may lay many groups of eggs and each group hatches in about 6 days. During hatching, the upper half of the egg breaks away, leaving a characteristic hole. Nymphs aggregate on the foliage and because they are green, they blend in with the rice foliage. The nymphs pass through five instars (E.A. Akinsola, WARDA 1994 pers. comm.). When adults are disturbed, they give off an offensive odour that is as strong as that given off by the pentatomids. Plant damage and ecology: Many grasses serve as hosts for the alydids, with rice and Echinochloa being important (Reissig et al. 1986). Riptortus dentipes is also a pest of soya bean (Ogunwolu 1992) and cowpea (Kaemba and Khamala 1981) in Nigeria. They occur throughout the crop cycle in irrigated lowland rice at the WARDA Station in Côte d’Ivoire, but peak populations generally occur at 10–12 WAT (Heinrichs and Barrion 2004). October surveys in farmers’ fields in Côte d'Ivoire showed that the population was highest in crops at the flowering stage when they were about six times that of crops in the vegetative or booting stage. Both nymphs and adults prefer to feed on the endosperm of rice grains but will also suck plant sap. The presence of Stenocoris spp. in the crop at the vegetative stage indicates that

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Figure 5.1 Stenocoris apicalis adult (Source: not known).

Figure 5.2 Mirperus jaculus adult (Source: A. C. van Dyk; http://www.treknature.com/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.3 Riptortus dentipes adult (Source: http://www.infonet-biovision.org/).

they may be feeding on the sap from rice leaves or stems, as they have sucking mouthparts. The alydids do not bore a hole through the rice hulls but insert their stylets into the grain through a space between the lemma and the palea. As they feed, they secrete a liquid that forms a stylet sheath that hardens around the feeding point and holds the mouthparts in place. The white stylet sheaths left in the grain are visible to the naked eye. The nymphs and adults both prefer rice at the milk stage but may also feed on soft and hard dough rice grains. Nymphs are more active feeders than adults, but adults cause more damage because they feed over a longer period of time. Removal of the milky white endosperm results in reduced grain size. When feeding on the grain at the soft or hard dough endosperm stage, they inject enzymes to predigest the carbohydrate. This process results in the contamination of the grain with microorganisms that cause grain discolouration or pecky rice. Feeding at this stage reduces grain quality but does not reduce grain weight. According to Agyen-Sampong and Fannah (1980), Stenocoris spp. remove only a portion of the grain milk at one feeding and the grain may be fed upon several times. They report that a few days after the grain is punctured, the glumes begin to change colour, first to light brown and then to dark brown. Severity of the damage depends on the stage of grain development at the time of attack and on the number of times that the grain is fed upon. Plant density appears to have an effect on the Stenocoris spp. population. In a direct seeding experiment, in lowland irrigated rice, Stenocoris spp. populations were significantly higher at wider plant spacings with a seed density of 60 kg ha−', as compared with a more dense spacing at 120 kg ha−1 (Heinrichs and Barrion 2004). Stenocoris spp. are present in both the humid forest zone and Guinean savanna in Côte d'Ivoire. In three surveys conducted in 1995, populations were highest in the savanna in July, but in August and October, they were highest in the forest zone. In an October 1995 survey in Guinea, populations were twice as high in the savanna as in the forest zone (Heinrichs and Barrion 1994). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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The alydid bugs inhabit all rice ecosystems from the uplands to the lowlands. Studies on the continuum toposequence at WARDA (Heinrichs and Barrion 2004) indicated very low populations in the uplands with highest populations occurring in the lowlands, especially in the unweeded plots. Surveys in farmers' fields in Côte d'Ivoire indicated that populations of Stenocoris spp. were distinctly higher in lowland than in upland fields. In July 1995, there were 0.7 per 500 sweeps in the uplands and 4.8 per 500 sweeps in the lowlands, while in August there were 0.7 in the uplands and 13.2 in the lowlands per 500 sweeps (Heinrichs and Barrion 2004).

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5.4  Rice bugs, Leptocorisa spp. (Hemiptera: Alydidae) The rice bugs most commonly found in rice are L. acuta (Thunb.), L. chinensis (Dallas), L. varicornis F. and L. oratorius (F.) Distribution: L. acuta – Asia, Australia, Oceania and several Central American countries; L. chinensis – Japan; L. varicornis – India; L. oratorius – Asia, Australia, Oceania (Hayashi 1997, Dale 1994, Reissig et al. 1986, Schaefer and Panizzi 2000, Litsinger et al. 2015). Host plants other than rice: More than 65 plant species (Srivastava and Saxena 1967). Description and biology: The description and biology of the Leptocorisa spp. are similar. The following describes the life stages and biology of L. acuta (Serrano et al. 2014). Leptocorisa acuta adults (Fig. 5.4) are long (14–17 mm) and slender (3–4 mm wide). They are of light yellowish green to yellowish brown in colour. The head is broad, often similar in length and width to that of the pronotum (upper surface of the first plate on the thorax) and the scutellum (triangle-shaped plate on the thorax, posterior to the pronotum). These bugs have globular, protruding eyes in addition to small ocelli (simple eyes), which are difficult to see. The fourth antennal segment of the Leptocorisa spp. is longer than the third segment. Leptocorisa spp. have long legs and antennae and brownish green bodies (Fig. 5.5). Eggs (Fig. 5.6) are oval with the tops flattened. Females lay eggs in batches of 10–20, symmetrically arranged in 2–3 rows, on the upper surface of the leaf blade. When they are freshly deposited, eggs are of cream yellow colour, turning to a reddish brown after approximately one week.

Figure 5.4 Leptocorisa acuta adult (Source: not known). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.5 Leptocorisa varicornis adult (Source: http://www.srilankawilderness.org/).

Figure 5.6 Leptocorisa oratorius eggs (Source: Sylvia Villareal, IRRI).

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The eggs hatch a week following oviposition. The nymphs congregate around the empty egg cases for 3–4 hours before they disperse for feeding. Nymphs feed voraciously and gregariously until the fourth instar. There are five wingless nymphal instars with a total nymphal period of 25–30 days. Nymphs are mostly pale yellowish green and have long antennae (Fig. 5.7). Each nymphal instar looks remarkably similar to the one before it, except that each successive nymph is larger than the last and wing pad enlargement occurs. The final moulting takes place at night. Nymphs stop feeding about 5 hours prior to selecting a place to moult on the leaves or flowers of the host plant. The nymph then remains motionless in an extended position for about 2 hours before ecdysis. The actual process of moulting takes only 2 minutes. Rice bugs are diurnal but are most active during early morning and evening. During the hotter parts of the day, the bugs are seen taking shelter under the leaves of rice plants or weeds near rice fields. Rice bugs fly short distances when disturbed. The females are stronger fliers than the males. The males are capable of mating shortly after emergence, but the females start mating only one or two weeks after becoming adults. Mating generally takes place in the morning hours and rarely at night. They complete 1–2 generations on grassy weeds before migrating to rice fields. A small number of adults usually appear in the rice fields as soon as the plants start flowering. When about 80% of the grains have ripened, the adults migrate to fields having rice plants of less maturity. In Japan, L. chinensis hibernates on ferns and weeds under humid and shady conditions (Ito 1978). In India, teeming populations of L. acuta have been found to hibernate on trees during the relatively colder and drier months of December to March (Banerjee and Chatterjee 1965).

Figure 5.7 Leptocorisa oratorius nymph (Source: Sylvia Villareal, IRRI).

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Plant damage and ecology: The rice bugs are major pests of rice (Fig. 5.8, 5.9) wherever the crop is grown (Pathak and Khan 1994). Many species share a common distribution but very often differ in their relative abundance. For example, in the Philippines, L. oratorius (Fig. 5.8) is more abundant than L. acuta (Fig. 5.4). Rice bugs are found in all rice environments, but are more prevalent in rainfed wetland or upland rice. Factors that favour high bug populations are adjacent woodlands, extensive weedy areas near rice fields and staggered rice planting (Reissig et al. 1986). Both nymphs and adults are destructive to the crop, even though the damage by nymphs is more severe (Pathak and Khan 1994). Nymphs prefer grains at the milky stage, when the starches within the grains are not yet fully formed, for feeding. They infest rice crops in large numbers at flowering. Leptocorisa adults and nymphs have piercing-sucking mouthparts and feed by sucking fluid from florets, soft (milky) rice grains and plant sap. They do not bore a hole through the rice hull but feed by the insertion of the proboscis at points where the glumes (lemma and palea) meet. During the process, the bug secretes a proteinaceous stylet sheath to form a feeding canal for its sucking mouthparts (Gyawali 1981). The point of insertion may be visible by white exudate that turns into a brown spot. Removal of stored assimilates from the developing grains may result in either unfilled or partially filled grains with damage symptoms. When the bugs feed on soft or hard dough endosperm, they inject enzymes to predigest the carbohydrate. In the process they contaminate the grain with microorganisms that cause grain discolouration or pecky rice, which is more liable to break during milling (Reissig et al. 1986). Feeding enzymes

Figure 5.8 Leptocorisa oratorius female on rice (Source: Sylvia Villareal, IRRI). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.9 Leptocorisa chinensis adult on rice (Source: not known).

and microorganisms enhance feeding damage (Srivastava and Saxena 1967). Damaged florets may drop. The quality of grains is also reduced by the insect attack. Pecky rice in Japan and the United States is downgraded and priced lower than undamaged grains. The smell of the infested grains also lowers market value. Damaged grains, even after cooking, retain the buggy smell. Sometimes even the straw has an off-flavour which is unattractive to cattle. The intensity and type of damage caused by rice bugs depends on the stage of the rice crop, population density of the pest and ecological conditions. In India, on an average, 5–10% of the grains are damaged due to infestations of the rice bug. In years of severe attacks, damage reaches 40–60% (Kalode 1982). In the case of early paddy, maturing in September, the loss is usually greater than in the late maturing varieties. Leptocorisa spp. cause significant damage in Thailand every year. In the Malay Peninsula, the yield loss in certain areas exceeds 25% (Dale 1994). In addition to the direct feeding damage, Leptocorisa acuta is known to transmit Sarocladium oryzae and Sarocladium attenuatum (fungi), the cause of sheath rot disease. Sheath rot disease damages the panicle (branched arrangement of flowers) of the rice plant, which causes the plant to produce underdeveloped or damaged rice grains. In severe cases, the infected plant may not produce rice grains (Serrano et al. 2014). Rice bugs are often seen on flowering wild grasses near canals. In Papua New Guinea, numbers of Leptocorisa were observed to increase enormously when weeds in the adjacent paddies were left unmanaged (Sands 1977).

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Leptocorisa oratorius has been reported to reproduce on a number of wild grasses in Southeast Asia, although, as food plants, wild grasses were inferior to rice (Van Den Berg and SOEHARDI 2000). The bugs are attracted to the rice crop when the plants start flowering. Kainoh et al. (1980) have shown that adult bugs of L. chinensis (Fig. 5.9) can detect the odour of rice plants when they are close to the rice field. But their aggregation on the panicles seems to be due to the arresting effect of the flowers. The bug reacts favourably to high humidity and frequent drizzles prevailing from April to June, the active season of the bugs in India (Singh and Chandra 1967). Srivastava and Saxena (1967) reported that it was the light intermittent rain which favoured the build-up of bug populations, while heavy rains had an adverse effect on the pest. In the Philippines, rice bug activity was at its peak during the rainy period in November–December, and dry season crops which attained the milky stage in the period March–May were less severely attacked (Uichanco 1921).

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5.5  Stink bugs (Aspavia spp.) (Hemiptera: Pentatomidae) Four species of Aspavia have been reported on rice in West Africa. The biology and the damage caused by the various Aspavia species are assumed to be similar. Aspavia armigera F. appears to be the most common species. Distribution: A. armigera – Cameroon, Côte d'Ivoire, Gambia, Ghana, Guinea, GuineaBissau, Liberia, Nigeria, Senegal, Togo; A. acuminata – Côte d'Ivoire, Ghana, Mali; A. brunnea – Côte d'Ivoire, Mali, Senegal; A. hastator – Côte d'Ivoire. Host plants other than rice: The grain-sucking Aspavia spp. that attack rice have a wide host range. In Nigeria, A. armigera is a major pest of soya bean and cowpea in addition to rice (Ewete and Olagbaju 1990, Ogunwolu 1992; Panizzi 1997). It has been reported on cotton in Ghana (Forsyth 1966 as cited in Cobblah 1991). Description and biology: The characteristic odour that is produced by the scent glands, located on the lower side of the body, has given the pentatomids the common name of ‘stink bug’. Adult Aspavia spp. (Fig. 5.10) are brown bugs with a large scutellum (triangular shield) having three yellow spots and a pointed projection or spine at each side of the prothoracic plate. The species of Aspavia can be distinguished by the nature of the three spots on the scutellum. In A. armigera the spots are small and located at each corner of the scutellum (Fig. 5.10). In A. acuminata Montandon the spots are larger and in A. brunnea (Signoret) the spots fuse together to form a t- or v-shape. The spots are not present in A. hastator (Heinrichs and Barrion 2004).

Figure 5.10 Aspavia armigera adult (Source: Robert Taylor; http://www.ispotnature.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Ewete and Olagbaju (1990) studied the development of A. armigera on rice and cowpea in Nigeria. The female lays eggs singly on the plant after a preoviposition period of 12–19 days, depending on the rice variety. Incubation takes about 1 week. Nymphs pass through five instars over a period of 20–25 days. Plant damage and ecology: Agyen-Sampong and Fannah (1980) described damage caused by the feeding of Aspavia spp. Both nymphs and adults attack rice grains as soon as the panicle is exserted and continue to feed until the hard dough stage. Nymphs prefer to feed on grain immediately after flowering and the adults prefer grain in the milk stage. Grains at the hard dough stage are rarely punctured. The glumes are punctured and the bugs suck the contents of the developing grain. Although the alydid bugs, Riptortus and Stenocoris spp., feed on any site on the grain, Aspavia spp. primarily puncture the grain at the apical end. Only part of the milk is sucked out at each feeding and the same grain may be punctured several times. Signs of attack by Riptortus spp. are stylet puncture marks with milk exudate on the outer glumes, but these signs were not observed in feeding by Stenocoris or Aspavia spp. Within 2–3 days after the grain is punctured, the glumes begin to change colour, first to light brown and then gradually darker. In severe cases, the glumes become grey after 1 week. Severity of the damage depends on the stage of grain development and on the number of punctures in the grain. It is believed that Aspavia spp. feeding contributes to the incidence of the ‘dirty-panicle’ syndrome caused by multiple fungus diseases. There appear to be varietal differences in the effect of A. armigera feeding on the extent of grain damage. In studies by Ewete and Olagbaju (1990), four bugs panicle−1 caused significant grain damage in cultivar ITA 257, while eight bugs panicle−1 were required to cause significant grain damage in ITA 128. Mean percentage grain damage at four bugs panicle−1 was 14 and 39% for ITA 128 and ITA 257, respectively. Aspavia armigera occurs in both upland and lowland ecosystems but is more abundant in the latter (Heinrichs and Barrion 2004). Alam and Lowe (1989) studied the relative abundance of A. armigera on irrigated lowland and upland rice in Nigeria. Populations were about five times higher on irrigated rice than on upland rice. Studies on the continuum toposequence at WARDA (Heinrichs and Barrion 2004) indicated very low populations in the upland and high populations in the lowland plots. In a survey of farmers’ fields in Côte d'Ivoire, A. armigera populations were 1.6 and 10.3 per 500 sweeps, respectively, in the uplands and lowlands (Heinrichs and Barrion 2004). Aspavia armigera occurs throughout the rice crop growth cycle but is most abundant at flowering. In studies in lowland fields at WARDA (Heinrichs and Barrion 2004) the A. armigera population was 1.5, 2.4 and 12.9 per 500 sweeps at the vegetative, booting and flowering stages, respectively.

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5.6 Southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae) Distribution: All rice-growing regions of the world. Host plants other than rice: Nezara viridula is a polyphagous pest. It occasionally causes serious losses to rice. Description and biology: The adult (Fig. 5.11) is shield-shaped about ½- to 3/4-inch in length and readily recognized by its green colour. However, phenotypes differing in intensity of colouration may occur in the same population (Pathak 1968). In West Africa, they range from plain green to green with yellow stripes or yellow with green spots. The adult is about 12-mm long (Heinrichs and Barrion 2004). Females start mating about 1 week after emergence as adults and they begin lay eggs 2–3 weeks after mating. Eggs are laid in parallel rows on the lower surface of leaves in masses containing 70–130 each. Each female usually lays 2–8 egg masses. Eggs, which are white to light yellow but turn red or bright orange just before hatching, are often heavily parasitized. Newly hatched nymphs remain aggregated around their empty eggshells before they disperse for feeding. No feeding activity occurs during the first instar stage. Feeding begins in the second instar when the nymphs move away from their empty eggshells. After the fourth instar, the nymphs feed solitarily. Nymphs usually pass through five instars during a

Figure 5.11 Nezara viridula adult (Source: LSU Ag Center). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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35- to 45-day period before becoming adults (Dale 1994).The nymphal population exhibits varied colour patterns, from black for very small nymphs to green for larger nymphs. In Louisiana, as many as five generations per year may occur with greater numbers appearing in the fall before adults overwinter. In southern Japan, the insect has three overlapping generations with a partial fourth. In years that are warm in March–June, the hibernating bugs become active earlier and complete the fourth generation. Adults hibernate in shaded dry places. After hibernation the emerging adults feed on grasses, orchards and other spring and summer crops before they migrate to rice. Among the external conditions influencing mortality of the green stink bug in the overwintering season, weather conditions are the most important. In severe winters, mortality as high as 97.5% has been reported in Japan (Kiritani and Hokyo 1970). Intrinsic factors such as sex, body size and colour type of the adult influence the bug mortality in the overwintering period. Plant damage and ecology: The southern green stink bug has one of the widest host ranges of any insect pest. Not surprisingly then, it is occasionally a pest of rice. Even though the problem is sporadic, when southern green stink bugs feed on rice, they can cause significant damage. In West Africa, N. viridula populations on rice are generally lower than those of the other grain-sucking bugs, such as Aspavia, Stenocoris, Mirperus and Riptortus spp., so N. viridula is considered a minor pest of rice (Heinrichs and Barrion 2004). In addition to rice, N. viridula has many host plants and is especially common on legumes, cotton and tomato (Dale 1994). Rice fields surrounded by wild vegetation are especially vulnerable to N. viridula infestations. Mass migrations of this bug from vegetable fields to rice crops have been observed. The feeding behaviour of the nymphs and adults is similar. Both have piercing-sucking mouthparts, suck the milk from developing grains and cause pecky rice that is partially or wholly stained by bacteria or fungi. Damaged grains are shrivelled and unfilled. When grains are in the milky stage, they are fed upon, but when grains have ripened, the bugs feed on panicle stalks and pedicels. In Malaysia, when restricted to rice stems and leaves, they will feed on these plant parts with a preference for leaves over stems (Lim 1970). In Louisiana, damaged areas are usually localized in a field instead of being uniform throughout. Stunted plants, killed growing points and dead leaves are all signs of stink bug injury. In studies conducted in Japan, one N. viridula adult could produce 1.5 pecky rice grains d−1 (Kisimoto 1983). The pest has assumed great economic significance in Japan since 1956 when the introduction of early transplanting resulted in the flowering of the rice crop at the same time as the emergence of first-generation adults. Adults of N. viridula can fly over a distance of 1 km even if there is a hill in their flight path (Kiritani and Hokyo 1970).

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5.7 Rice stink bugs, Oebalus spp. (Hemiptera: Pentatomidae) Distribution: Rice stink bug O. pugnax (F.) – southern North America, the Caribbean and Central America (Pantoja et al. 1995); O. ornata (Sailer) – northern South America, the Caribbean and Central America (Pantoja et al. 1995); Small rice stink bug O. poecilus (Dallas) – Central and South America and is the most important stink bug infesting rice in Guyana, Brazil and other rice-producing countries in South America (Santos et al. 2006); O. ypsilongresius (De Geer) is found in Florida, the Caribbean and northern South America; O. insularis (Stål) is an important pest in Central America, Mexico and Colombia (Ruelas Ayala and Carrillo Sanchez 1979) and has also been reported from rice fields in Florida, USA (Cherry and Nuessly 2010). Host plants other than rice: Avena sativa L., Cyperus iria L., Digitaria sanguinalis (L). Scop., Echinochloa crus-galli (L.) Beauv., Hordeum vulgare L., Panicum dichotomiforum Michx., Paspalum urvillei Steud., Secale cereale L., Sorghum bicolor (L.) Moench., Triticum aestivum L., Zea mays L. Description and biology: The complex of stink bugs in the genus Oebalus constitutes the most important insect pests of rice from flowering to grain maturity in North, Central and South America. All species are characterized by the ability to emit pungent chemical compounds from scent glands. Oebalus pugnax begins hibernating during the first week of October and overwinters in the adult stage in bunch grass (Nilakhe 1976) and wood trash (Odglen and Warren 1962). The insects start emerging out of hibernation by the first week of April and complete their emergence by the last week. Males emerge first about 10 days before the females. After emergence from overwintering adult bugs are seen voraciously feeding on the flowers of wild grasses and populations may pass through several generations on these alternate weed hosts before moving into rice when panicles emerge (Naresh and Smith 1984). They are usually evenly distributed in rice fields. O. pugnax adults are frequently observed mating in the field (Fig. 5.12) and females lay barrel-shaped eggs in masses of 10–47 eggs on rice leaves, stems and panicles, often immediately after moving into fields. The eggs are arranged in two rows on stems, leaves or panicles. Eggs are bright green when laid but turn red before they hatch. The incubation period is 4–8 days. Host plant quality affects egg production. Females reared on barnyard grass and vasey grass lay significantly fewer eggs than those reared on rice (Nilakhe 1976). The newly hatched O. pugnax nymphs congregate on and around the empty eggshells for about a day (Fig. 5.13) before they disperse to feed. When they hatch, the nymphs have a black thorax, head, legs and antennae and two black spots on the red abdomen. But this colouration fades away with successive nymphal moults (Fig. 5.14). There are five nymphal instars and the nymphal period lasts from 16 to 20 days. Development time from egg to adult ranges from 3–5 weeks, depending on temperature. Oebalus pugnax, the species of greatest importance in North American rice, is a shieldshaped, metallic brown/tan bug approximately 1.2 cm in length with prominent lateral pronotal spines (Fig. 5.12). The antenna is pale red, with the first segment lighter in colour than the others. The legs are yellow with scattered black punctures. The hindwings are iridescent and frequently appear green. The bugs give off a strong, disagreeable odour when disturbed. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.12 Oebalus pugnax mating (Source: LSU Ag Center).

Figure 5.13 Oebalus nymphs at the site of hatching (Source: LSU Ag Center).

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Figure 5.14 Oebalus pugnax nymph (Source: http://bugguide.net/).

Figure 5.15 Oebalus poecilus adult (Source: LSU AgCenter). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.16 Oebalus ypsilongriseus adult (Source: LSU Ag Center).

Figure 5.17 Swarm of Oebalus poecilus adults (Source: Thais Freitas). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.18 Stink bug damaged rice grains (Source: Centre for Insect Bioinformatics, ICAR-NBAIR; http://www.nabg-nbaii.res.in/).

Species of Oebalus found in Central and South Americas are similar to O. pugnax in appearance and life history. O. poecilus (Fig. 5.15) is smaller than O. pugnax; males are 8.1 by 4.1 mm and females are 8.9 by 4.2 mm. This species has seven yellow spots on its body that are easy to identify: two half-moon-shaped spots on the pronotum, three yellow spots on the scutellum, two of which are larger and kidney-shaped and one of which is smaller and on the vertex, and two small spots on the wings. Oebalus ypsilongriseus (Fig. 5.16) has two yellow spots on the pronotum close to the head. Females of O. poecilus ‘swarm’ (Fig. 5.17) to lay thousands of eggs in overlapping layers on plants (Barrigosi 2008). Plant damage and ecology: Nymphs and adults feed on developing rice grains from anthesis until grain hardening. Both use their piercing-sucking mouthparts to remove the contents of developing rice grains. Feeding by rice stink bugs causes both quantitative damage (decrease in rice yield) and qualitative damage (decrease in rice grain quality). Attack of florets during anthesis to early endosperm formation results in losses in yield (blank grains, reduced grain weights and atrophied grains), whereas feeding during milk and dough stages results in dark spots on the lemma (Fig. 5.18) and in reductions in grain quality. Reductions in quality are manifested in various ways, including broken and chalky grains, but the most important form of qualitative damage is increased incidence of bull’s eye-shaped discolourations known as ‘pecky’ grains in milled rice. Pecky rice is caused in part by various species of facultative pathogens that enter through feeding sites of bugs (Lee et al. 1993). ‘Pecky’ grains are structurally weak at the region of insect injury and often break during milling. This results in a reduction in market value and loss of income for producers. Pecky © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.19 Parboiled rice grains with fungal damage (‘pecky rice’) due to stinkbug feeding (Source: http://pragasarroz.xpg.uol.com.br/).

rice, which escapes breakage during milling, is of inferior quality as a finished product owing to its discolouration. Seed quality is also decreased, and germination of seeds damaged by stink bugs is lower (Chaves et al. 2001). Studies in Arkansas, indicated that discolouration in pecky rice (Fig. 5.19) results from fungi that are introduced at the time of feeding by the rice stink bug, O. pugnax (Lee et al. 1993). Similar fungi were cultured from pecky rice grain and from the stylets and saliva of O. pugnax. The fungus, Fusarium oxysporum Schlect., caused the greatest discolouration in pecky rice. Economic losses due to stink bugs vary. O. ornata causes crop losses as high as 50% in the Dominican Republic. Early estimates in the United States put the loss caused by O. pugnax from a negligible amount to 25% (Ingram 1927). Consistent and severe losses in rice yields were reported for infestation levels of 7–8 bugs per 1,000 panicles (Swanson and Newsom 1962).

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5.8 Earwigs, Diaperasticus erythrocephalus (Olivier) (Dermaptera: Forficulidae) The common name, ‘earwig’, was given to these insects because of the superstition that they crawl into the ears of sleeping persons (Little 1963). Their food varies considerably, ranging from living and dead insects to decaying and living plants. Although they are commonly seen on the floral parts of rice, the damage that they cause is minimal, and they are considered as minor pests of rice in West Africa. Distribution: Earwigs occur primarily in the tropics and warmer temperate zones (Giles 1970). Steinmann (1977) reported D. erythrocephalus Olivier to be distributed throughout the Ethiopian region and Madagascar. In West Africa, it has been recorded from Benin, Burkina Faso, Cameroon, Côte d'Ivoire, Liberia and Mali, but it probably occurs in most West African countries (Heinrichs and Barrion 2004). Euboriella annulipes Pallas distribution is worldwide in temperate and tropical areas, except in Australia, and Labidura riparia (Lucas) is a cosmopolitan species primarily in tropical to subtropical regions. Both occur in Côte d'Ivoire. Host plants other than rice: Pennisetum glaucum (L.) R. Br., Sorghum bicolor (L.) Moench., Triticum aestivum L., Zea mays L. Description and biology: Earwigs are elongated, slender insects with a flattened and heavily sclerotized body. They are beetle-like in appearance but are easily distinguished from the Coleoptera by the presence of distinct cerci, or pincers, that appear as forceps

Figure 5.20 Labiduria riparia (Source: Paco Alarcon; http://www.biodiversidadvirtual.org/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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at the tip of the abdomen, as seen in Labidura riparia (Fig. 5.20). The pincers are used in defence; to fold the soft, membranous, fan-shaped, hindwings beneath the forewings; and to catch and hold the prey while it is consumed.’Dermaptera’ means ‘skin wings’, referring to the leather-like texture of the forewings. Female earwigs are maternal in that they protect the eggs that are laid in burrows on the ground and feed the nymphs until they are strong enough to take care of themselves. Metamorphosis is simple and the nymphs are similar in appearance to the adults, except for an increase in the number of antennal segments and the progressive development of the wings until maturity. Nymphs moult four to five times before reaching adulthood. Development takes about 4 weeks (Giles 1970). Plant damage and ecology: Diaperasticus erythrocephalus is found on rice plants at all stages of crop growth. However, it is most abundant during the flowering stage. Earwigs generally hide in dark spaces during the day and feed at night. They are mostly scavengers but also feed on the floral parts, pollen, stamens and pistils of rice when the glumes open. Such feeding damage causes sterility. Diaperasticus erythrocephalus occurs at all sites on the continuum toposequence. However, they appear to be more abundant in the upland/hydromorphic zones than in the lowlands. In studies on the continuum toposequence at WARDA (Heinrichs and Barrion 2004), the D. erythrocephalus population was highest in the lower portion of the uplands and in the hydromorphic zones. In studies conducted in slash-and-burn ecosystems in Côte d'Ivoire (Oyediran et al. 1999), Diaperasticus populations were higher in the upland than in the hydromorphic sites. D. erythrocephalus is predaceous on smaller insects. Alghali (1984) observed the earwig preying on newly emerged adults of the sorghum midge, Contarinia sorghicola Coquillet, in Kenya. It was also recorded as a predator of maize stalk borers in Ethiopia (Abate 2012). Predaceous activity of this earwig in rice is not known.

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5.9  Blister beetles (Coleoptera: Meloidae) Blister beetles are large, distinctly coloured beetles that are general feeders on various plant species. Blister beetle adults are found on flowers and on foliage on which they feed. Meloids produce a body fluid containing cantharidin that is highly toxic and causes large, watery blisters when it comes in contact with human skin. Blister beetles found on rice in West Africa are found in the genera Epicauta, Cylindrothorax and Mylabris (Heinrichs and Barrion 2004) Distribution: Cylindrothorax melanocephala F. – Côte d'Ivoire, Nigeria; C. spurcaticollis F. – Burkina Faso, Cameroon, Côte d'Ivoire, Guinea, Guinea-Bissau, Liberia, Mali; C. westermanni Maklin – Cameroon; Epicauta canescens Klug – Nigeria; Epicauta funebris Horn – the United States; Mylabris sp. – Cameroon, Côte d'Ivoire. Host plants other than rice: Cylindrothorax melanocephala has been reported on Pennisetum glaucum (L.) and Sorghum bicolor Moench in Ghana and Senegal. C. westermanni has been reported on P. glaucum, S. bicolor and Zea mays L. in Côte d'Ivoire, Ghana, Nigeria and Senegal (Selander 1988). Description and biology: Blister beetles vary in colour, with the head and pronotum being yellow or black and the elytra being reddish yellow, bluish or greenish black. Their bodies are cylindrical (Britton 1970). The head is large and constricted to a narrow ‘neck’ where it joins the prothorax. The thorax is narrower than the head or wing covers (Fig. 5.21–5.22).

Figure 5.21 Mylabris sp. (Source: http://www.zin.ru/animalia/coleoptera/eng/). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Figure 5.22 Epicauta funebris on rice in Arkansas, USA (Source: http://www.arkansas-crops.com/).

Cylindrothorax melanocephala is a large, slender beetle approximately 20 mm long. The elytra (forewings) are metallic pine green, while the dorsal portion of the prothorax has a bright orange colour; the head is black. Adults lay eggs in the soil where the larvae and pupae also occur. Larvae generally pass through six instars before pupating. Plant damage and ecology: Blister beetle adults are very mobile and often suddenly appear in large numbers and cause severe damage to the floral parts of the rice plant. In addition to rice, they feed on the flowers of other crops; they are well known to feed on maize tassels. Whereas the adult blister beetles are phytophagous, the larvae are predaceous on grasshopper eggs in the soil. A Cylindrothorax melanocephala outbreak was observed at Keneba, Gambia, during the late rains (October–November) of 1958–62. Outbreak years are partly associated with high rainfall but probably more related to the presence of locust swarms during the previous year, as the newly hatched beetle larvae were able to prey on an abundance of locust eggs in the soil (Giglioli 1965). Okwapam (1971) reported an outbreak of C. melanocephala at the Federal Rice Research Station, Badeggi, Nigeria, in September 1965. The beetle population was high, ranging from 2 to 10 beetles panicle−1. The beetles ravenously ate the developing grains (milk stage), which became empty and white in colour. They destroyed almost 100% of the grains after feeding in a field for 48 hours and then moved on to adjacent fields on the research station.

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5.10 Panicle thrips, Haplothrips spp. (Thysanoptera: Phlaeothripidae) Distribution: Haplothrips ganglbaueri Schmutz – India, Malaysia, Pakistan, Sri Lanka; Haplothrips avenae (Priesner) – Malawi, Nigeria, Senegal; H. gowdeyi Franklin – Globally in tropical and subtropical countries. This section is based on the host plants, description and biology and plant damage caused by Haplothrips ganglbaueri, although it is assumed that it is similar to those of H. avenae and H. gowdeyi. Host plants other than rice: Ageratum conyzoides L., Asytasia gangetica (L.) Aners., Blumea wightiana DC, Bothriochloa pertusa (L.) A. Camms, Celosia argentea L., Chloris barbata Sw., Cyperus rotundus L., Echinochloa crus-galli (L.) Beauv., Eragrostis nigra Nees ex Steud., Hydrolea zeylanica Vahl., Imperata cylindrica (L.) Raeuschel, Ischaemum indicum (Houtt.) Merr., Leucas aspera Sprng., Paspalum scrobiculatum L., Pennisetum typhoides (Burm. F.), Polytrias amaura (Buse) O. Kuntze, Solanum torvum Sw., Sorghum bicolor (L.) Moench., Triticum vulgare Vill. (Dale 1994). Description and biology: The thrips are distinct because of their long, narrow, membranous wings, which are fringed with long hairs and have a pointed abdomen tip (Fig. 5.23). The adult thrips are dark brown with a dominant reddish tinge. The average lengths of males and females are 1.3 and 1.6 mm, respectively. The preoviposition period lasts for 2–3 days. Eggs are laid on the outer surface of the lemma and palea mostly in clusters of 4, 8 and

Figure 5.23 Haplothrips gowdeyi female (Source: Dena Paris). © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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12 (Ananthakrishnan and Thangavelu 1967). Eggs hatch in 2–4 days. There are two larval instars which together last for 8–11 days. There is a short pre-pupal stage of 1 day which then passes to the pupal stage. The pupal period is 3–4 days. Female thrips live for 12–15 days, while males live for only 3–5 days (Dale 1994). Plant damage and ecology: Cereal thrips, Haplothrips ganglbaueri, is a polyphagous species infesting the inflorescence of various cereal crops such as rice, wheat, sorghum and millets. The pest also abounds on several weeds common in and around rice fields. A positive correlation often exists between the thrips populations in the weeds and on the rice plants (Ananthakrishnan and Thangavelu 1967). The population build-up of the insect is very high and outbreaks have been reported from many parts of India (Chaudhary and Ramzan 1971, Abraham et al. 1972). Incidence of H. ganglbaueri in South India is serious during the first fortnight of December when the weather is humid, with occasional drizzles, and the sky is overcast for most of the day (Dale 1994). Thrips have a single functional mandible. Because of the laceration and feeding by larvae and adults of H. ganglbaueri, the rice inflorescence is variously affected. The damage on the lemma and palea causes development of irregularly oval and diffused brownish patches (Abraham et al. 1972). Vidayasagar and Kulshreshtha (1983) reported three distinct types of damage: (1) light brown spots with a perforation at the proximal part of the unopened spikelets, (2) sterile spikelets that retain their green colour throughout their development and (3) oozing of milk over the grain without any external feeding marks. Continuous feeding causes chaffy or malformed grains. Affected panicles turn to premature whitish colour and are erect due to the dropping of damaged grains. Hsieh et al. (1980) reported an association between rice sheath rot caused by Acrocylindrium oryzae Sawada and two rice thrips, Thrips oryzae Williams and Haplothrips aculeatus. The disease infected the leaf sheath, spikelets and grains. About 80% of each of the two thrips species collected from the infected rice plants carried the A. oryzae pathogen. Rice thrips infested with the pathogen were also shown to be able to transmit the disease to the rice plant. Infected panicles were sterile.

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5.11 References Abate, T. 2012. Maize stalk borers of Ethiopia: quantitative data on ecology and management. In Proceedings: Meeting the challenges of global climate change and food security through innovative maize research. Proceedings of the 3rd National Maize Workshop of Ethiopia, Worku, M., Wolde, L., Tadesse, B., Demisie, G., Bogale, G., Wegary, D., Prasanna, B. M., TwumasiAfriyie, S., Wolde, L., Tadesse, B., Demisie, G., Bogale, G., Wegary, D. and Prasanna, B. M. (Eds), Addis Ababa, Ethiopia, 18–20 April 2011, pp. 174–84. Abraham, C. C., Thomas, B., Karunakaran, K., Gopalakrishnan, R. 1972. Occurrence of Haplothrips ganglbaueri Schmutz (Phlaeothripidae: Thysanoptera) as a serious pest of rice earheads in Kerala. Cur. Sci. 41:721. Agyen-Sampong, M., Fannah, S. J. 1980. Dirty panicles and rice yield reduction caused by bugs Stenocoris and Aspavia in West Africa. Int. Rice Res. Newsl. 5(1):11–12. Alam, M. S., Lowe, J. A. 1989. Incidence of two grain suckers in irrigated and upland rice. Int. Rice Res. Newsl. 14 (1):30–1. Alghali, A. M. 1984. Studies on the biology, damage and crop loss assessment of the sorghum midge, Contarinia sorghicola Coq. (Diptera: Cecidomyiidae). Insect Sci. Appl. 5:253–8. Ananthakrishnan, T. N., Thangavelu, K. 1967. The cereal thrips Haplothrips ganglbaueri Schmutz with particular reference to the trends of infestation on Oryza sativa and the weed Echinochloa crusgalli. Proc. Indian Acad. Sci. Sec. B 83:196–201. Banerjee S. N., Chatterjee, P. B. 1965. On the alternate host plants and hibernation of rice bug, Leptocorisa acuta Thunberg in North Bengal. Sci. Cult. 31:259–60. Barrigosi, J. A. F. 2008. Manejo do Percevejo da Panícula em Arroz Irrigado. Embrapa Arroz e Feijão, Circular Técnica 79, 8 pp. Britton, E. B. 1970. Coleoptera (beetles). pp. 495–621. In: Mackerras, I. M. (ed.). p. 1029. The Insects of Australia. A Textbook for Students and Research Workers [1st edition]. Melbourne University Press, Canberra, Australia. Chaudhary, J. P., Ramzan, M. 1971. Chemical control of Haplothrips ganglbaueri Schmutz (Phlaeothripidae: Thysanoptera) on paddy. J. Res. Punjab Agric. Univ. 8:214–16. Chaves, G., Ferreira, E., Garcia, A. H. 2001. Influência da alimentação de Oebalus poecilus (Heteroptera: Pentatomidae) na emergencia de plântulas em genótipos de arroz (Oryza sativa) irrigado. Pesquisa Agropecuária Tropical 31(1):79–85. Cherry, R., Nuessly, G. 2010. Establishment of a new stink bug pest, Oebalus insularis (Hemiptera: Pentatomidae), in Florida rice. Fla. Entomol. 93:291–3. Cobblah, M. A. 1991. Some pod-sucking bugs of cowpea, Vigna unguiculata (L.), in Ghana. Discovery Innovation 3:77–9. Dale, D. 1994. Insect pests of the rice plant-their biology and ecology. p. 363–485. In: Biology and Management of Rice Insects, Heinrichs, E. A. (ed.), p. 779. Wiley Eastern Limited, New Delhi and the International Rice Research Institute, Los Baños, Philippines. Ewete, F. K., Olagbaju, R. A. 1990. The development of Aspavia armigera Fabricius (Hemiptera: Pentatomidae) and its status as a pest of cowpea and rice. Insect Sci. Appl. 11:171–7. Giglioli, M. E. C. 1965. Some observations on blister beetles, family Meloidae, in Gambia, West Africa. Trans. R. Soc. Trop. Med. Hyg. 59:657–63. Giles, E. T. 1970. Dermaptera (earwigs). pp. 306–313. In: Mackerras, I. M. (ed.). p. 1029. The Insects of Australia. A Textbook for Students and Research Workers. [1st edition]. Melbourne University Press, Canberra, Australia. Gyawali, B. K. 1981. Feeding behavior and damage assessment of rice bug, Leptocorisa oratorius (Fabricius) on rice. M.S. thesis, University of the Philippines, Los Baños, Philippines. Hayashi, H. 1997. Historical changes and control of rice stink bug complex causing the pecky rice. Plant Prot. 51:455–61 (in Japanese).

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Heinrichs, E. A., Barrion, A. T. 2004. Rice-Feeding Insects and Selected Natural Enemies in West Africa: Biology, Ecology, Identifcation. Los Baños (Philippines): International Rice Research Institute and Abidjan (Côte d’Ivoire): WARDA-The Africa Rice Center. 242 p. Hsieh, S. P. Y., Hsu, M. F., Liang, W. C. 1980. Etiological studies on the sterility of the rice plant. II. Transmission by tarsonemid mite, Steneotarsonemus spinki, thrips, Thrips oryzae and Haplothrips aculeatus and survival of Acrocylindrium oryzae Sawada, the fungus associated with sterile rice plant. Plant Prot. Bull. (Taiwan) 22:41–6. Ingram, J. W. 1927. Insects injurious to the rice crop. U. S. Dept Agric. Farmers’ Bull. 1543. Ito, K. 1978. Ecology of the stink bugs causing pecky rice. Rev. Plant Prot. Res. (Japan) 2:62–78. Kaemba, B. M., Khamala, C. P. M. 1981. Relation of pod age to the expression of resistance in cowpea Vigna unguiculata (L.) to common pod sucking bugs Riptortus dentipes (F.) and Anoplocnemis curvipes F. (Hemiptera: Coreidae) in Nigeria. Kenya J. Sci. Technol. Ser. B. Biol. Sci. 2:47–52. Kainoh, Y., Shimizu, K., Maru, S., Tamaki, Y. 1980. Host finding behavior of the rice bug, Leptocorisa chinensis Dallas (Hemiptera: Coreidae), with special reference to diet patterns of aggregation and feeding on rice plant. Appl. Entomol. Zool. 15:225–33. Kalode, M. B. 1982. Rice gundhi bug. pp. 22–7. In: Recent advances in the Knowledge of Insect Pests of Paddy: Distribution, Life History and Control. Indian Agricultural Research Institute, New Delhi, India. Kiritani, K., Hokyo, N. 1970. Studies on the population ecology of the southern green stink bug, Nezara viridula L. (Heteroptera: Pentatomidae). Agriculture, Forestry and Fisheries Research Council BL. Secretariat, Japan. Kisimoto, R. 1983. Damage caused by rice stink bugs and their control. Jpn. Pestic. Inf. 43:9–13. Lee, F. N., Tugwell, N. P., Fannah, S. J., Weidemann, G. J. 1993. Role of fungi vectored by rice stink bug (Heteroptera: Pentatomidae) in discoloration of rice kernels. J. Econ. Entomol. 86:549–56. Lim, G. S. 1970. Importance and control of Nezara viridula Linnaeus on the rice crop in West Malaysia. Malays. Agric. J. 47:465–82. Linnavuori, R. E. 1987. Alydidae, Stenocephalidae and Rhopalidae of West and Central Africa. Acta Entomol. Fenn. 49:1–36. Litsinger, J. A., Barrion, A. T., Canapi, B. L., Libetario, E. M., Pantua, P. C., dela Cruz, C. G., Apostol, R. F., Lumaban, M. D., Macatula, R. F. 2015. Leptocorisa rice seed bug (Hemiptera: Alydidae) in Asia: a review. The Philippine Entomologist 29:1–103. Little, V. A. 1963. General and Applied Entomology (2nd ed.). Oxford and IBH Publishing Co., New Delhi. Naresh, J. S., Smith, C. M. 1984. Feeding preference of the rice stink bug on annual grasses and sedges. Entomol. Exp. et Applic. 35:89–92. Nilakhe, S. S. 1976. Overwintering, survival, fecundity, and mating behavior of the rice stink bug. Ann. Entomol. Soc. Am. 69:717–20. Odglen, G., Warren, L. O. 1962. The rice stink hug Oebalus pugnax Fabricius in Arkansas. Arkansas Agric. Exp. Stn. Rep. Ser. 107. Ogunwolu, E. O. 1992. Field infestation and damage to soybean and cowpea by pod-sucking bugs in Benue State, Nigeria. Insect Sci. Appl. 13:801–5. Okwapam, B. A. 1971. Outbreak of blister beetles in ricefields at Badeggi. Nigerian Entomol. Mag. 2(3):100–2. Oyediran, I. O., Heinrichs, E. A., Traore, A. K. A., Johnson, D. 1999. Plant spacing effect on insect pest abundance and yields of irrigated lowland rice in Côte d’Ivoire. J. Plant Prot. Trop. 12:55–67. Panizzi, A. R. 1997. Wild hosts of pentatomids: ecological significance and role in their pest status on crops. Annu. Rev. Entomol. 42:99–122. Pantoja, A., Daza, E., Garcia, C., Mejia, O. I., Rider, D. A. 1995. Relative abundance of stink bugs (Hemiptera: Pentatomidae) in Southwestern Colombia rice fields. J. Entomol. Sci. 30(4): 463–7. Pathak, M. D. 1968. Ecology of common insect pests of rice. Ann. Rev. Entomol. 13:257–94.

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Pathak, M. D., Khan, Z. R. 1994. Insect Pests of Rice. The International Rice Research Institute, Los Baños, Philippines. 89 pp. Reissig, W. H., Heinrichs, E. A., Litsinger, J. A., Moody, K., Fiedler, L., Mew, T. W., Barrion, A. T. 1986. Illustrated Guide to Integrated Pest Managment of Rice in Tropical Asia. International Rice Research Institute, Los Baños, Laguna, Philippines, p. 411. Ruelas Ayala, H., Carrillo Sanchez, J. L. 1979. Parasitismo natural causado por Telenomus sp., sobre la chinche café del arroz, Oebalus insularis (Stål), en Campeche. Agricultura Tecnica en Mexico 4(2):137–42. Sands, D. P. A. 1977. The Biology and Ecology of Leptocorisa (Hemiptera: Alydidae) in Papua New Guinea. Res. Bull. No. 18, Department of Primary Industry, Port Moresby, Papua New Guinea, p. 104. Santos, R. S. S., Redaelli, L. R., Diefenbach, L. M. G., Romanowski, H. P., Prando, H. F., Antochevis, R.C. 2006. Seasonal abundance and mortality of Oebalus poecilus (Dallas) (Hemiptera: Pentatomidae) in a hibernation refuge. Brazilian J. Biol. 66(2A):447–453. Schaefer, C. W., Panizzi, A. R. 2000. Heteroptera of Economic Importance. CRC Press, Boca Raton, p. 856. Selander, R. B. 1988. An anotated catalog and bionomics of blister beetles of the genus Cylindrothorax (Coleoptera, Meloidae). Trans. Am. Entomol. Soc. 114:15–70. Serrano, A. C., Russell, F., Mizell, R. F., Byron, M. A. 2014. Rice Bug (suggested common name) Leptocorisa acuta (Thunberg) (Insecta) EENY614. Entomology and Nematology Department, UF/IFAS Extension, Gainesville, FL 32611. http://edis.ifas.ufl.edu/pdffiles/IN/IN106700.pdf Singh, M. P., Chandra, S. 1967. Population dynamics of rice stink bug (Leptocorisa varicornis Fabr.) in relation to weather factors. Indian J. Agric. Sci. 37:112–19. Srivastava, A. S., Saxena, H. P. 1967. Rice bug Leptocorisa varicornis Fabricius and allied species. In International Rice Research Instititute (Ed), The Major Insect Pests of the Rice Plant, pp. 525–48. Proceedings of a symposium at the International Rice Research Institute, September, 1964. Johns Hopkins Press, Baltimore, USA. Steinmann, H. 1977. A new Diaperasticus Burr species from Sudan (Dermaptera: Forficulidae). Acta Zool. Acad. Sci. Hung. 23:415–20. Swanson, M. C., Newsom, L. D. 1962. Effect of infestation by the rice stink bug Oebalus pugnax on yield and quality in rice. J. Econ. Entomol. 55:877–9. Uichanco, L. B. 1921. The rice bug, Leptocorisa acuta Thunberg in the Philippines. Philipp. Agric. Rev. 14: 87–125. Van Den Berg, H., SOEHARDI. 2000. The influence of the rice bug Leptocorisa oratorius on rice yield. J. Appl. Ecol. 37: 959–70. Vidayasagar, P. S. P. V., Kulshreshtha, J. P. 1983. Observations on the nature of damage to rice earheads by thrips, Haplothrips ganglbaueri Schmutz. Curr. Sci. 52:173–4.

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Chapter 6 Integrated pest management (IPM) of rice E. A. Heinrichs, University of Nebraska-Lincoln, USA; F. E. Nwilene, The Africa Rice Center (AfricaRice), Nigeria; M. Stout, Louisiana State University, USA; B. A. R. Hadi, International Rice Research Institute (IRRI), The Philippines; T. Freitas, Universidade Federal do Rio Grande do Sul, Brazil 6.1 Concepts and options for rice IPM 6.2 Cultural practices in rice IPM 6.3 Promoting natural enemies of rice pests: conservation biological control 6.4 Augmentative biological control 6.5 Selective insecticides 6.6 Dissemination mechanisms for rice IPM 6.7 References

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6.1 Concepts and options for rice IPM Pre-harvest yield losses due to rice insect pests can be significant. This is especially so under pest outbreak scenarios. Irrigated rice has been shown to be an agro-ecosystem with rich biodiversity and a redundant food chain (Schoenly et al. 1996, Wilby et al. 2006). Insecticide abuse negatively affects the natural enemy communities, shortens the food chain length and increases the propensity for pest outbreaks in irrigated rice ecosystems (Heong and Schoenly 1998, Settle et al. 1996, Way and Heong 1994). An alternative framework for insect pest management is needed to address the vulnerability of the rice crop to specific pests, without introducing a higher risk of pest outbreaks. Wyss et al. (2005) and Zehnder et al. (2006) proposed a conceptual framework for arthropod pest management in organic crop production (Fig. 6.1). In this framework, arthropod pest management strategies are classified into four ‘phases’. The framework prioritizes pest management options that will prevent damaging levels of pests (phase 1 and 2) and minimize the need for curative actions (phase 3 and 4). We will adopt and modify this conceptual framework to structure the discussion on various rice insect pest management options in rice ecosystems.

Figure 6.1 Conceptual framework for rice IPM (adapted from Zehnder et al. 2006).

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6.2 Cultural practices in rice IPM Generally, two types of practices are found under the first two phases: 1) cultural practices that directly target insect pest populations (primary practices) and 2) crop husbandry practices with secondary effects on pest populations (secondary practices). Practices that directly target insect pest populations probably form the earliest methods of pest management in rice and include mechanical and physical removal of insect pest populations. These practices are typically labour-intensive in nature. In terms of the optimum spatial scale, these cultural practices can be further classified into two: 1) those that operate in single-field scale and 2) those that operate in community scale (i.e. covers multiple fields within a locale). Litsinger (1994) catalogued a number of cultural practices that prevent the development of economically damaging populations of rice pests and we classify these practices according to their principal intent (e.g. primary and secondary practices) and optimum spatial scale in Table 6.1. Of the cultural practices listed above, deployment of host plant resistance (a primary cultural practice) and fertilizer management (a secondary cultural practice) form basic building blocks in developing a rice ecosystem with reduced vulnerability to insect pests.

Host plant resistance: insect adaptation and deployment strategies Heinrichs et al. (1985) documented standard methods for screening for resistance against multiple insect pests of rice. Much work has been done to identify resistance genes, especially against hemipteran pests, and breed them into elite varieties (Fujita et al. 2013, Jena and Kim 2010). Sources of resistance have been identified for most of rice insect pests (Heinrichs et al. 1985).

Table 6.1 Examples of cultural practices that prevent the development of economically damaging populations of rice insect pests (from Litsinger 1994) Single-field scale

Community scale

Primary practices

•• Deployment of resistant rice varieties against brown planthopper in Asia (Cohen et al 1997) and rice water weevil in North America (e.g. Stout et al 2001)

•• Insect light traps using blue light were used to control stem borer moths, Chilo suppressalis, in paddy fields across Japan during World War II and the post-war years (Shimoda and Honda 2013)

Secondary practices

•• Fertilizer management affects hopper and stem borer populations in Asia (e.g. Lu et al. 2004, Hou and Han 2010) •• Delayed planting date to avoid population peak of small rice stink bug in South America (Albuquerque 1993) •• Water and planting date management affects rice water weevil population in North America (e.g. Morgan et al 1989, Stout et al 2002, Thompson et al 1994)

•• Synchronous planting affects the incidence of tungro, a viral disease vectored by the green leafhopper (Cabunagan et al 2001)

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Resistance durability is the primary challenge in the utilization of host plant resistance for managing rice insect pests. Rice pest populations showed rapid adaptation against the deployed resistant varieties. This is especially well documented in rice brown planthopper systems (e.g. Alam and Cohen 1998). Mundt (2014) listed several general deployment strategies to improve the durability of resistance genes against pests and diseases: gene rotation, field mixture of resistance genes and gene pyramiding. Gene rotation involves a regional deployment of a resistance gene, monitoring of pest virulence/adaptation to the deployed gene within the region and rotation to another resistance gene upon detection of pest adaptation. There is evidence that this deployment scheme is feasible in prolonging durability against rice blast disease (Crill et al. 1981). The challenge lies in the implementation of regional monitoring schemes to detect the target pest’s adaptation to the deployed gene. Such regional monitoring schemes are likely to be expensive. Furthermore, in the event of detected adaptation, it may prove difficult to choose alternative genes to be deployed since cross-adaptation may occur across several resistance genes. While gene rotation subjects the same cropping space to two or more resistance genes over time, field deployment of a mixture of varieties essentially subjects various parts of the cropping space to two or more varieties with different levels of resistance in a given period of time. Large-scale trials in China showed that a mixture of resistant and susceptible varieties suppressed rice blast severity and reduced the need for fungicide application (Zhu et al. 2000). However, the report did not monitor the effect of the strategy in prolonging the durability of resistance against rice blast. Concern has been raised that this particular deployment strategy may select for pathogen race or pest populations that are adapted to multiple resistance genes (Mundt 2014). A number of studies reported that pyramiding two or more resistance loci resulted in higher resistance compared to monogenic lines, as measured by the target pest’s feeding, settling, survivorship, population growth and damage on host plants (e.g. Fujita et al. 2010, Hu et al. 2012, Qiu et al. 2012). However, Sharma et al. (2004) showed that a pyramided line (incorporating Bph1 and bph2) had the same resistance level to introgression lines carrying Bph1 alone, as measured by the effects of brown planthopper infestation on plant heights. None of these studies measured the effects of pyramiding resistance genes to the durability of the resistance. Gene function and resistance mechanisms associated with identified resistance genes against rice pests are not fully understood (Fujita et al. 2013). Moreover, the mechanisms and genetic/physiological basis for pest adaptation to resistant rice varieties are not always clear. Without this information, it is difficult to predict how the different deployment strategies will delay pest adaptation towards resistant rice varieties. Thus, a considerable amount of research is needed to evaluate the effects of deployment strategies described above to the durability of resistance genes against insect pests.

Fertilizer management In general, fertilizer management affects rice insect pest populations by modifying rice plants’ suitability for and attractiveness towards herbivorous insects (Ge et al. 2013, De Kraker et al. 2000, Chantaprapha et al. 1980, Swaminathan et al. 1985, Lu et al. 2004, Jiang and Cheng 2003, Hou and Han 2010, Ranganathan et al. 2006, Hosseini et al. 2012, Djamin and Pathak 1967).

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Increased nitrogen fertilizer rate was associated with a longer larval development duration and higher oviposition rate of the leaffolder (C. medinalis) (Ge et al. 2013). Leaffolder female moths preferred rice plants with higher fertilizer rates to lay their eggs compared to plants with lower fertilizer rates (De Kraker et al. 2000). A small-scale field experiment confirmed that the number of leaffolder eggs found on plots with high fertilizer rate (~150 kg/Ha) was higher than those found on plots with lower fertilizer rates (~0 and 75 kg/Ha). Furthermore, the ratio between the natural enemy and leaffolder larval abundance was correlated negatively with nitrogen fertilizer rate and, consequently, the survivorship of leaffolder larvae was the highest in plots receiving high amounts of nitrogen fertilizer (De Kraker et al. 2000). Other field studies confirmed that higher severity of leaffolder injury was typically observed on plots with high nitrogen fertilizer rates (≥150 kg/Ha) (Chantaraprapha et al. 1980, Swaminathan et al. 1985). Lu et al. (2004) reported a positive correlation between rice leaf nitrogen content and brown planthopper nymphal survivorship, longevity of adult females, female fecundity and egg hatching rate. Additionally, higher leaf nitrogen content was associated with faster nymphal development of brown planthopper. Taken together, these findings indicate that excessive nitrogen fertilization rate may lead to faster population development and higher maximum population levels of brown planthopper. Nitrogen fertilizer regimes may affect brown planthopper population’s ability to grow on resistant or tolerant varieties. Heinrichs and Medrano (1985) recorded a positive correlation between nitrogen fertilizer rate and the number of brown planthopper populations developing on Triveni, a tolerant rice variety with some antibiosis activity, and IR60, a resistant variety with high antibiosis. Nitrogen fertilizer regime affected rice plant’s host suitability for stem borer and the plant’s ability to compensate for tiller loss. In a screenhouse experiment, Jiang and Cheng (2003) reported that striped stem borer’s larval weight gain and development were positively correlated with nitrogen fertilizer rates within a certain range (200–600 mg N/ pot) and started to decrease with additional nitrogen fertilizer. Moreover, nitrogen, as a plant nutritional factor, contributes to the ability of rice to produce new tillers. Therefore, the plants compensated for striped stem borer injury between the low and medium range of nitrogen fertilizer rate (200–400 mg N/pot) but not under high or excessive range of nitrogen rate (600–800 mg N/pot) (Jiang and Cheng 2003). Silicon amendment was associated with a longer time needed for striped stem borer’s penetration into rice stalk, lower larval weight gain and lesser extent of damage (Hou and Han 2010). These effects were even more pronounced in the tested susceptible variety than the resistant variety. In greenhouse experiments, silicon amendment was negatively correlated with whitehead incidence caused by yellow and striped stem borers (Ranganathan et al. 2006, Hosseini et al. 2012). Djamin and Pathak (1967) posit that varietal difference in accumulating silica in the leaves may affect the variety’s suitability for stem borer larvae and partially contribute to their resistance against stem borer. Indeed, they observed a negative correlation between leaf silica content and deadheart incidence caused by striped stem borer. Through an observation of striped stem borer larval mandibles, Djamin and Pathak (1967) further inferred that high leaf silica content decreased stem borer-related damage by mechanically grinding the incisor region of larval mandibles. The form of fertilizer may have an impact on rice herbivorous insects. White-backed planthoppers feeding on rice with poultry manure fertilizer had lower nymphal survivorship,

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reproductive rate and egg hatching rate compared to those feeding on plants with inorganic fertilizer (Kajimura 1995a, b). The same effect of lower nymphal survivorship on organically fertilized rice plants was observed with brown planthopper (Kajimura 1995a). Organically fertilized plants had lower nitrogen content compared to those with inorganic fertilizer. Specifically, the leaves of organically fertilized plants contained significantly lower amounts of asparagine, an amino acid, compared to those with inorganic fertilizer. Asparagine acts as a feeding stimulant for brown planthopper (Sogawa 1982) and its absence or low titre has been associated with planthopper resistance in various indica and japonica rice varieties (Sogawa and Pathak 1970, Shigematsu et al. 1982). Apart from its impact on host plant suitability and attractiveness towards herbivorous insects, fertilizer may have effects on the natural enemy communities exerting a regulation function on pest populations. Jiang and Cheng (2004) reported higher abundance of collembolans in organically manured rice plots compared to those with inorganic fertilizer. While no statistical difference was observed in arthropod predator abundance between the two rice plot types, significantly higher egg predation rate of white-backed planthopper was observed in organically manured rice plots.

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6.3 Promoting natural enemies of rice pests: conservation biological control Natural pest regulation in irrigated rice ecosystems Among cultivated plants, irrigated rice constitutes a complex ecosystem with a relatively high species diversity and redundant food web (Schoenly et al. 1996, Wilby et al. 2006). Various life stages of herbivorous insects in rice ecosystems are preyed upon and parasitized by predators and parasitoids from a number of classes and orders, including araneae (Preap et al. 2001, Sigsgaard 2000), orthopterans (de Kraker et al. 2000), coleopterans (Rubia-Sanchez et al. 1990), aquatic and terrestrial heteropterans (Nakasuji and Dyck 1984, Reyes and Gabriel 1975), hymenopterans, strepsipterans and dipterans (Gurr et al. 2011). Settle et al. (1996) showed that across irrigated rice production fields in Java, generalist predators (e.g. spiders, mirid bug) were always abundant early in the cropping season. An increase in the organic matter before the beginning of the season resulted in the increased decomposer abundance and led to even higher levels of predator populations. These correlations indicated that predators in rice ecosystems utilize decomposer communities as alternative prey before the arrival of phytophagous insects (Settle et al. 1996). The widely practised staggered planting in intensive rice production areas may further ensure the continuous availability of prey and hosts in rice fields and contribute to the abundance of natural enemy populations in this ecosystem (Way and Heong 1994). Conservation biological control in rice ecosystems capitalizes on and enhances the natural pest regulation provided by these prevalent natural enemy communities in rice fields. Annual monoculture cropping systems is often associated with high disturbance regimes on the natural habitat for natural enemies. High usage of pesticides and potential lack of adult food source and shelter are among the disturbances affecting the natural enemy populations in these cropping systems (Landis et al. 2000). Conservation biological control aims to remedy this situation by limiting insecticide use, promoting selective insecticides and altering crop habitats to allow better support for natural enemy populations.

The effects of insecticide application on natural enemy and pest populations In a descriptive work on insect population dynamics as affected by early insecticide application (20–50 days after transplanting), Schoenly et al. (1996) found a stark difference in pest and natural enemy populations between sprayed and unsprayed fields. By midseason, natural enemy abundance was higher in the unsprayed field compared to that in the sprayed field. On the other hand, herbivorous insect populations were higher by mid-season on the field receiving three early insecticide applications. Indeed when food webs were constructed for the two field types, the authors found that the mean length of the food chain was shorter in fields receiving early insecticide application. This food chain shortening continued for about 40 days after the first spray. The abundance of natural enemy population eventually rose in the field receiving early insecticide application, yet the plant damage due to increased herbivore abundance during the mid-season might have already been done.

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At least two mechanisms contribute to this dramatic increase in pest population due to early insecticide applications. Schoenly et al. (1996) linked a reduction in natural enemy population immediately after insecticide application to a quick rise of herbivore abundance. The rise of herbivore population has indeed been attributed to the temporal release of herbivores from natural enemies following early insecticide applications (Heinrichs and Mochida 1984, Fagan et al. 1998). Chelliah et al. (1980) and Chelliah and Heinrichs (1980) reported an increase in the reproductive rate of brown planthopper in response to a sub-lethal dose of insecticide application. This phenomenon in which a sub-lethal dose of select insecticide increases ecological fitness parameters of certain insects, termed ‘hormesis’, has received further attention recently with works published on different rice pest species using various active ingredients (Azzam et al. 2009, Bao et al. 2008, Hu et al. 2010, Ling et al. 2009, Ling et al. 2011, Suri and Singh 2011). Stimulation of ecological fitness parameters by a sub-lethal dose of insecticide forms the second mechanism explaining the rise in pest population as affected by insecticide application (Heinrichs et al. 1982). What factors drive the practice of early insecticide application? In the Philippines, a survey of farmers’ insecticide decision protocols revealed that a significant portion of early insecticide application coincided with fertilizer application, in part to provide an easy-toremember guide to time a prophylactic application (Bandong et al. 2002). Heong et al. (1994) reported that early insecticide application is often driven by farmers’ perception of defoliators’ ability to affect yield. Indeed, defoliator pests which produce conspicuous injuries such as leaffolder often infest rice fields early in the season. Yet, empirical and simulation studies showed that early stage defoliation by leaffolder only resulted in rare occurrence of minor yield loss (Graf et al. 1992, Heong et al. (1994). Consequently, much of the early season application of insecticides was based on exaggerated estimation of plant damage due to leaffolder and likely to be uneconomical (Heong et al. 1994). These observations led to the formulation of a simple rule of thumb: ‘Insecticide spraying for leaffolder control in the first 40 days after sowing is not needed’ (Heong et al. 1998). This simple message, supported by public media and an entertainment education campaign, has been shown to successfully change farmers’ practice in the Mekong Delta, Vietnam (Huan et al. 1999, Heong et al. 2008). A number of caveats need to be taken to complement this simple message. While irrigated rice may be an inherently resilient ecosystem against pests, it is possible that insect pest populations occasionally reach damaging levels early in the season, perhaps due to a particularly high immigration rate or high degree of planting asynchrony. Unfortunately, economic injury levels for early rice stages that take into account natural enemies’ capacity to provide biological control are not available and this lack of knowledge hampers our ability to make judicious pest management decisions. More research is needed to identify these economic injury levels. The effects of different active ingredients on rice natural enemies vary widely (Fabellar and Heinrichs 1986, Preetha et al. 2009, Preetha et al. 2010, Takahashi and Kiritani 1973, Tanaka et al. 2000, Wang et al. 2008). ‘Reduced risk’ insecticides, due to their selectivity against natural enemies and other non-target organisms, have recently been developed. These newer insecticides are not commonly used in rice production, partly due to their relatively expensive costs (Norton et al. 2010). Careful research needs to be conducted to test the effects of these reduced risk insecticides on field populations of natural enemies when applied early in the season. Information from these studies should then be used to evaluate whether these ‘reduced risk’ insecticides may become options for rare occasions of early insecticide application as dictated by pest population levels. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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Habitat management for natural enemy conservation Various habitat management schemes within agricultural fields, for example, by intercropping and introduction of wildflower strips or plants repellent to herbivores, were shown to significantly suppress herbivore populations, enhance natural enemies and reduce crop damage (Letorneau et al. 2011). While the limitation on early insecticide application enhances rice natural enemies by reducing the known effect of a disturbance regime (insecticide), habitat management schemes typically provide resources (e.g. alternative or complementary food sources, shelter) to the natural enemy species. In the Asian rice ecosystem, much effort has been invested in designing a habitat management scheme in which flowering plants are introduced on rice bunds to conserve natural enemies (Gurr et al. 2011, Gurr et al. 2012, Gurr et al. 2016, Zhu et al. 2013, Zhu et al. 2015). Introduction of flowering plants seemed to have a primary benefit of food provisioning (e.g. pollen, floral and extrafloral nectar) to members of the natural enemy community (Lu et al. 2014). Indeed many predators and parasitoids are known to utilize non-prey food sources, usually to satisfy their need for metabolic energy (Lundgren 2009). Laboratory studies showed that, compared to a water control, the presence of sesame flower (Sesamum indicum) as a food source increased the adult longevity of planthopper parasitoids (Anagrus optabilis and Anagrus nilaparvata) (Zhu et al. 2015) and stem borer parasitoids (e.g. Apanteles ruficrus, Cotesia chilonis and Trichogramma chilonis) (Zhu et al. 2015). A similar laboratory study showed that the adult longevity of a predatory mirid bug, Cyrtorhinus lividipennis, was significantly increased in the presence of sesame as well as other flowers (e.g. Tagetes erecta, Trida procumbens and Emilia sonchifolia) compared to water or nil controls (Zhu et al. 2015). Furthermore, these controlled experiments showed that the presence of sesame flowers increased the parasitism and predation rates of the natural enemies compared to water or nil controls (Zhu et al. 2013, Zhu et al. 2014). These benefits, observed in controlled experiments, may not translate to enhancement of natural enemies at the field level. There are a number of further considerations to be taken (Zhu et al. 2015, Lu et al. 2014: 1)) the plant selected for a habitat management scheme will have to provide a resource not already available in the field, 2) the scheme will have to allow for a back-and-forth movement of natural enemies between the flowering plants and the major crop, 3) the availability of food resource provided by the scheme will have to start as early as possible and to last as long as possible across the season to maximize the benefits for natural enemies, and 4) selection of plants to be included in the habitat management scheme must also consider potential adverse effects of the plant’s introduction; for example, some plants may act as alternative food source for pests as well as natural enemies. Yet, in the case of sesame flowers the natural enemy benefits reported in laboratory studies were reproduced at the field scale. In a factorial study with combinations of sesame borders and pesticide applications, fields with sesame borders and no pesticide applications had the highest predator and parasitoid abundances compared to all other combinations (e.g. no sesame border and no pesticide application, no sesame border with pesticide application, with sesame border with no pesticide application) (Gurr et al. 2016). Indeed, the same report contains a multi-country comparison where rice fields with nectar-bearing flowers on their borders had significantly lower pest populations, received less insecticide applications (as guided by farmers’ decision) and produced higher yields compared to control fields (Gurr et al. 2016).

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6.4  Augmentative biological control As mentioned above, while the irrigated rice ecosystem constitutes a redundant food web, it is plausible for the insect pest populations to occasionally reach economically damaging levels. Then, curative actions are needed and, whenever available, augmentative biological control should form the first curative option. In contrast to conservation biological control, the aim of which is to improve the impact of indigenous natural enemy community, augmentative biological control typically aims for a limited time increase in specific natural enemy species to temporally suppress pest populations and activities and avoid economic damage in yield. Augmentative biological control is usually achieved by field releases of predators, parasitoids or pathogens with expected effects to last either season-long (inoculative biological control) or within a short period of time in season (innundative biological control). Rombach et al. (1987) provided a bibliography on pathogens of rice insect pests from 1960 to 1985 and listed members of all major fungal groups, bacteria, viruses and nematodes as potential biological control agents of rice insect pests. Since then, a number of studies have continued to show the efficacy of primarily two entomopathogenic fungal genera, Metarhizium and Beauveria, on rice pests (Aguda et al. 1987, Jin et al. 2008, Jin et al. 2010, Rombach et al. 1987, Li et al. 2012a,b). Additionally, in a laboratory experiment using an artificial diet, toxins produced by Bacillus thuringiensis (Bt) have been shown to inhibit feeding by larvae of the Asiatic stem borer (Rombach et al. 1989). One of the criticisms against the use of invertebrate pathogens as augmentative biocontrol agents in rice production is the relatively long period it takes for control and the limited efficacy at field scale (Way 2003). Rombach et al. (1994), for example, recorded very low level of mortality after field application of five entomopathogenic species (including Beauveria bassiana and Metarhizium anisopliae) seven days after treatment (0–4% mortality rate). Yet, the mortality rate reached 70–100% at 21 days after treatment. In an evaluation of Metarhizium flavoviride against a rice grasshopper, Hieroglyphus daganensis, Thomas et al. (1998) found a field population knocked down to ~40% survivorship 10 days after application but then the mortality rate slowed down significantly afterward. Further development of biological control agents will have to address these criticisms by identifying highly virulent fungal strains, optimizing formulation and, perhaps, considering a mixture of augmentative biocontrol with other control options. There is an obvious variability in biocontrol efficacy among strains of the same fungal species (e.g. Toledo et al. 2008, Jin et al. 2008). An evaluation of 35 global strains of a single species, Metarhizium anisopliae, for example, yielded nymphal mortality rates ranging from 6.5 to 64.2% (Jin et al. 2008). The density of conidia needed to kill 50% of a given target pest population (LC50) also varies with formulation. When prepared as emulsifiable formulation, the LC50 of a virulent strain of Beauveria bassiana was reduced by 38% compared to unformulated conidial solution (Feng and Pu 2005). Finally, combining M. anisopliae application with low-rate buprofezin, an insect growth regulator, increased brown planthopper control rate from ~60% to ~80% (Jin et al. 2010). There are very few reports on the effects of augmentative biological control agents on rice natural enemies. Rombach et al. (1994) noted that while some entomopathogenic fungi infect beneficial insects, natural infection was always observed at low levels. Schoenly et al. (2003) reported no effect of Bt spray on rice natural enemy’s diversity and abundance in field scale. Scant published data signals a need to conduct thorough studies on the effects of augmentative biocontrol on the populations of indigenous beneficial insects. © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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6.5  Selective insecticides Insecticides should be regarded as the last resort in the arsenal of IPM options. There are a number of considerations to guide insecticide application in rice ecosystems: application timing, selectivity of active ingredients and resistance among pest populations associated with insecticide overuse. For the insecticide application to be profitable, the decision as to whether or not to apply an insecticide must be guided by an estimate of economic loss that may be incurred if no curative action is taken. This is usually done by introducing an economic threshold value for pest populations to guide decisions. Furthermore, unfortunate timing of insecticide application may prove harmful to the indigenous natural enemy community and its attendant pest regulation function (Schoenly et al. 1996). Some active ingredients were shown to be more toxic to the natural enemy than the pest species (e.g. Fabellar and Heinrichs 1986). Finally, overuse of insecticides may lead to the development of insecticide resistance among the insect pest populations (e.g. Su et al. 2013, Matsumura and Sanada-Morimura 2010).

Economic action thresholds Economic injury level, defined as ‘the lowest population density that will cause economic damage’, is a keystone of IPM theory (Stern et al. 1959). Economic injury level relates field population of insect pests to pest injuries and pest injuries to economic damage (e.g. yield loss). An economic action threshold to guide the timing of insecticide application is formulated based on the economic injury level. A number of economic injury levels and economic action thresholds against individual rice pests have been developed and tested in Asia (e.g. Bautista et al. 1984, Litsinger et al. 2005, Litsinger et al. 2006a, b, c) and North America (e.g. Morgan et al. 1989). In large-scale testing against rice bug and plant- and leafhoppers in the Philippines, Litsinger et al. 2005 reported that while implementation of action thresholds typically resulted in significantly higher rice yield compared to untreated controls (by about 0.3–0.5 ton/ha), they are not always profitable to farmers. A number of factors may contribute to this result: •• While the development of an economic injury level typically takes into account the commodity market value and the cost of management action, in practice the economic injury level is not adjusted to account for temporal fluctuation and spatial variation in rice price. This means that, at times, the action threshold will overestimate or underestimate the actual economic injury levels for a given season/location. •• Most of the economic injury levels, that have been developed for rice pests, do not take into natural pest regulation potential of indigenous natural enemies. The only exception where the natural enemy population was somehow accounted for (by reducing the number of pest individuals by a certain factor for each natural enemy individual found) was the action threshold tested for brown planthopper (Litsinger et al. 2005). In a large-scale test, the population levels of brown planthopper never crossed this threshold. By not accounting for natural enemy population in formulating action thresholds, we risk affecting the natural enemy community and pest regulation function it provides, which may lead to pest resurgence and total net loss for the farmers (as discussed under section ‘The effects of insecticide application on natural enemy and pest populations’).

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•• Most of the economic injury levels on rice were developed on a limited number of susceptible varieties (e.g. Bautista et al. 1984). Relationship between insect pest population, insect injuries and yield loss differ markedly between resistant and susceptible rice varieties. By basing the economic injury levels on susceptible varieties, we risk overestimating the impact of insect pest populations for rice fields that incorporate resistant and tolerant varieties. Due to the limitations above, the practicality of using action thresholds in rice ecosystems, especially among smallholder farmers, has been questioned (Matteson 2000). Since the available economic threshold values do not typically take into account the local and temporal specifics (in terms of price variability, natural enemy populations and varieties planted, for example), efforts to use economic thresholds may backfire and trigger unnecessary application of insecticides.

Selectivity against natural enemies Studies have shown that insecticidal active ingredients vary in their selectivity against natural enemies in different Asian countries. In the Philippines, Fabellar and Heinrichs (1986) showed that deltamethrin, chlorpyrifos and endosulfan are more toxic to Pardosa pseudoannulata, a common predatory spider, compared to the brown planthopper. Interestingly, one of these active ingredients, deltamethrin, is much more toxic to green leafhopper compared to P. pseudoannulata. Indeed, a number of reports stated that while deltamethrin was associated with brown planthopper resurgence (e.g. Heinrichs et al. 1982, Reissig et al. 1982a,b), no such resurgence was observed for green leafhopper (Fabellar and Heinrichs 1986). Triazophos and carbaryl are shown to be more toxic to Cyrtorhinus lividipennis, a predatory mirid bug, compared to the brown planthopper and green leafhopper (Fabellar and Heinrichs 1986). In Japan, BPMC, a common carbamate insecticide, was found to be more toxic to P. pseudoannulata and Conocephalus maculatus, a predatory grasshopper, compared to the green rice leafhopper Nephotettix cincticeps (Takahashi and Kiritani 1973). Additionally, in Japan, deltamethrin was found to be more toxic to a number of predatory spiders, mirid bugs and Haplogonatopus apicalis, a drynid wasp, compared to the brown planthopper (Tanaka et al. 2000). Using a risk quotient approach (calculated as the ratio between recommended field dose of a given active ingredient and the LC50 of the same active ingredient to a given natural enemy), Zhao et al. (2012) reported that all tested organosphosphates (chlorpyrifos, fenitrothion, phoxim, profenofos and triazophos) and carbamates (carbosulfan, carbaryl, isoprocarb, metolcarb and promecarb) posed high risks against Trichogramma japonicum, a parasitoid of rice lepidopteran pests in China. This means that the recommended field rates of these active ingredients are much higher than their comparative LC50s against T. japonicum, in some cases more than 1000 times higher. In the same study, insect growth regulators (chlorfluazuron, fufenozide, hexaflumuron, tebufenozide) were reported to pose the lowest risk against T. japonicum. Insecticides may also affect the biological control function of natural enemies. In a cage study, Fabellar and Heinrichs (1986) reported a significantly lower predation rate of L. pseudoannulata on plants treated with azinphos ethyl, an organophosphate insecticide, compared to untreated spiders.

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In summary, active ingredients of different members of the organophosphates, pyrethroids, organochlorines and carbamates appear to pose a high risk against various members of natural enemy communities in the rice ecosystem. Thus, screening among the different active ingredients for their risks against rice natural enemies should be taken seriously especially at the insecticide registration phase. Heinrichs et al. (1982) added that such screening needs to be done for potential tendency to induce resurgence, likely caused by hormesis (discussed above), on target insect pests.

Insecticide resistance Insecticide resistance to various active ingredients has been reported among different rice insect pest species across Asia. In 2006, resistance against imidacloprid was detected on brown planthopper populations collected in East Asia (Taiwan, China and Japan) and Vietnam but not on those collected in the Philippines. Additionally, resistance against fipronil was detected among white-backed planthopper populations from East Asia, Vietnam and the Philippines (Matsumura et al. 2008). Resistance against imidacloprid among brown planthopper populations collected in China was also reported by Wen et al. (2009) and Zhang et al. (2014). Moderate resistance against buprofezin, an insect growth regulator, was widespread among white-backed planthopper populations in China collected in 2010–2011 (Su et al. 2013). The same study reported lower frequency (30–60% of the samples) of low-tomoderate resistance to imidacloprid, thiamethoxam and chlorpyrifos among white-backed planthopper populations in China. An eleven-year survey showed a dramatic increase (up to 28-fold) in buprofezin resistance among Chinese brown planthopper populations between 1996 and 2006 (Wang et al. 2008). Development of insecticide resistance is often associated with overuse of a certain active ingredient in a given region over an extended period of time (Matsumura et al. 2008, Wang et al. 2008). Indeed, laboratory selection by constantly subjecting generations of the insect population to a given active ingredient commonly yield an insect strain with over 100-fold resistance compared to susceptible strains (e.g. Ding et al. 2013, Liu and Han 2006, Wang et al. 2008). On the other hand, development of resistance in a given population may carry an ecological fitness cost. For example, a brown planthopper population selected for imidacloprid resistance had significantly lower life table parameters (e.g. fecundity, nymphal survivorship and egg hatchability) compared to an imidacloprid-susceptible population (Liu and Han 2006). If indeed the insecticide-susceptible strain has an ecological fitness advantage, an environment with reduced or no pesticide exposure may lead to selection of susceptible individuals. Indeed, a brown planthopper population collected in China was found to be resistant to imidacloprid, chlorpyrifos, fipronil and fenobucarb when compared to a susceptible strain. This field-collected population was then reared for 15 generations without exposure to any insecticide and their susceptibilities to the four above-mentioned active ingredients were measured routinely. A consistent decrease of LD50 was detected across all tested active ingredients, indicating a reversal of resistance development occurring in the absence of insecticide exposure (Yang et al. 2014). This observation indicates that development of resistance to a given active ingredient may be slowed down or even reversed by drastic exposure reduction of the active ingredient towards the insect population.

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6.6  Dissemination mechanisms for rice IPM Over the last two decades, two major dissemination mechanisms for rice IPM in Asia have taken shape: farmer field school (FFS) and mass media campaign (MMC). FFS is a participatory training approach that utilizes experiential and reflective learning principles. The approach improves farmers’ capacities through a series of regular meetings with highly trained facilitators (typically extension workers or NGO staffers) in which the farmers conduct their own field experiments, learn to diagnose problems and formulate solutions (Van den Berg and Jiggins 2007). The use of FFS as a means for rice IPM dissemination was first developed in the Philippines as a collaboration between the International Rice Research Institute and the Philippines’ Bureau of Plant Industry (Pontius et al. 2002). The FAO later launched a large-scale FFS campaign in Indonesia in the late 1980s. Based on the success in Indonesia, FFS was adopted as a dissemination mechanism for IPM and other best agronomic practices across the globe (Van den Berg and Jiggins 2007). The impact and cost-effectiveness of FFS as a means for IPM dissemination have been contested. Participation in FFS on rice IPM has been shown to reduce insecticide use and increase yield over time (e.g. Pincus 1999). FFS participants used much less pesticide and produced significantly more yield compared to control farmers (e.g. Tripp et al. 2005). Thus, participation in FFS had a significant impact on farmers’ IPM practice and their respective yield. The major criticisms against FFS are its financial sustainability and effectiveness to spread information among non-participants. There are evidences that very limited, if any, diffusion of IPM knowledge and practices occurred between FFS alumnae and neighbouring farmers (e.g. Rola et al. 2002, Tripp et al. 2005). In light of these limited diffusion effects, outscaling of FFS to cover a significant farmer population may be crucial to achieve a large-scale impact of the IPM packages. However, Quizon et al. (2001) observed high upfront and overhead costs of FFS upscaling to cover a meaningful farming population and concluded that FFS was financially unsustainable. As FFSs were launched in Vietnam in 1992, the project focused on farmers living around towns or main roads. Thus, there was a concern that the method may not reach farmers who live in areas outside town proper or with limited road access. MMC was introduced in Vietnam specifically to reach these ‘underserved’ farmers (Rejesus et al. 2009). There has been an evolution of the messages disseminated through MMC in Vietnam. As described under the subsection ‘The effects of insecticide application on natural enemy and pest populations’, a simple rule of thumb, ‘insecticide spraying for leaffolder control in the first 40 days after sowing is not needed (No early spray – NES)’, was formulated. Multimedia materials to communicate this message were designed through a participatory workshop that involved researchers, extension and agricultural communication specialists. The resulting MMC involved distribution of leaflets, posters, roadside billboards and radio dramas broadcast through local stations and played at coffee shops (Heong et al. 1998). After 31 months of the MMC-NES in Long An Province, Vietnam, the proportion of farmers who believed that early season spraying was required dropped from 77% to 23%. Reported spray frequency was also significantly reduced from 3.35 sprays per season to 1.56 sprays per season (Heong et al. 1998). Between 1992 and 1997, both FFS and MMC-NES coincided in Vietnam providing an opportunity to compare the impacts of both interventions. In terms of reach, FFS trained 108,000 farmers in the study sites across Mekong Delta while MMC reached 2.3 million farmer households (Huan et al. 1999). Both FFS and MMC-NES had effects on farmer

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beliefs. The percentage of farmers who believed that killing natural enemies of pests can cause more pests are the highest among those exposed to both FFS and MMC-NES compared to those exposed to only MMC-NES. Furthermore, the percentage of farmers who believed that applying insecticides will increase yield is lower among those exposed to both interventions compared to those exposed only to MMC. An evaluation study of both the FFS and the MMC-NES message was conducted in 2005 in three southern Vietnam provinces. The study showed that farmers exposed to either FFS or MMC-NES are more technically efficient in using pesticide compared to control farmers (i.e. those not exposed to either intervention). However, there is no statistical difference in the amount of insecticides used by farmers receiving MMC-NES compared to control farmers. This may mean that MMC-NES farmers were spraying the same amount of insecticides with better timing compared to control farmers, thus producing better technical efficiency. FFS farmers used statistically less insecticides compared to control farmers; however, there was no difference in spray frequency between FFS and control farmers. This may mean that FFS farmers spray as frequently as control farmers with lower rates, perhaps as the results of following label dosage and better recognition of pest and beneficial insects (Rejesus et al. 2009). The authors posit that the difference between their evaluation results of MMC-NES impact and previous studies (e.g. Heong et al. 1998, Huan et al. 2008) may have stemmed from the chosen evaluation methodologies. Rejesus et al. (2009) pointed out that previous evaluation studies for MMC impacts did not take into account the possible selection bias and endogeneity problem, which might affect the studies’ inferences. In 2002, a large-scale participatory experiment was conducted with 951 farmer collaborators in multiple Vietnamese provinces in the Mekong Delta to evaluate the effects of reducing pesticide, fertilizers and seed rates on rice farming productivity and profitability. This exercise showed that reducing input from the then current practice had no effect on productivity and improved profitability (Huan et al. 2008). This largescale participatory evaluation formed the basis for a message expansion disseminated through MMC in Vietnam. The new campaign, locally termed ‘Ba Giam Ba Tang’ or ‘Three reductions, Three Gains’, promoted a reduction of pesticide, synthetic fertilizer and seed rates (i.e. three reductions) and promised savings in production costs, improved farmers’ health and environmental quality (i.e. three gains). The campaign distributed leaflets and posters. Additionally, a radio drama and a 30-s TV commercial were broadcasted over local radio and TV stations. An evaluation of this MMC was conducted in Can Tho and Tien Gang provinces. Two months after the launch of the campaign, 81% and 56% of surveyed farmers had heard of the campaign in Can Tho and Tien Gang, respectively (Huan et al. 2008). The evaluation programme monitored the changes in farmers’ belief attitudes and input use (self-report) as affected by the campaign. Reductions of insecticide spray (~13–33%), seed rate (~10%) and nitrogen fertilizer rate (~7%) were reported. Additionally, there was an overall change in belief attitudes favouring reduction of the targeted inputs (Huan et al. 2008). Huelgas et al. (2008) found an increase of $92–118/ha in net income from An Giang Province in Vietnam. However, economic assessment data from Can Tho province showed lower net income among ‘Ba Giam Ba Tang’ adopters compared to the non-adopters. In conclusion, FFS is an effective educational tool to improve the farmers’ capacity to manage their agro-ecosystem. This improvement translates into reduction in pesticide use and higher yield. However, the high cost and tendency for low diffusion effects to non-participants are the weaknesses of FFS. MMC is an effective method to communicate simple messages to a large farming audience. When designed correctly, the simple © Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.

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messages work to modify farmers’ attitude and behaviour. Both FFS and MMC increased the technical efficiency of pesticide use by farmers; however, the household-level economic impact of MMC may vary with geographic location. FFS and MMC complement each other by creating a nucleus of farmers with in-depth understanding of agro-ecosystem management and ability to conduct their own field experiments while mass communicating simpler IPM messages towards a larger farming audience.

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Index African pink borer  97–100 African rice gall midge  120–124 African rice hispa  263–266 African striped rice borer  83–85 African subterranean termites  44–48 African white borer  86–90 Alydid bugs  291–294 American rice stalk borer  76–78 Asian rice gall midge  116–119 Asian rice hispa  259–262 Asiatic pink stem borer  102–104 Augmentative biological control  330–331 Black beetles  25–26 Black bugs  12–14 Blister beetles  313–314 Brown planthopper  155–159 ‘Chafers’ (white grubs)  26–28 Chinch bug  17–18 Colaspis beetles  28–30 Common armyworm  237–238 Common cutworm  232–233 Dark-headed stem borer  70–72 Earwigs 311–312 Economic action thresholds  331–332 Fall armyworm  230–231 Farmer field school (FFS)  334–336 Fertilizer management  324–325 FFS. see Farmer field school (FFS) Fijian rice leafflolders  216 Flea beetles  270–272 Foliage feeders African rice hispa  263–266 Asian rice hispa  259–262 common armyworm  237–238 common cutworm  232–233 fall armyworm  230–231 flea beetles  270–272 foliage feeding aphids  275 green hairy caterpillars  242 green horned caterpillar  220–222 ladybird beetle  273–274 large rice grasshoppers  188–190 leaf miner  256 meadow grasshoppers  198–200

overview 146–148 paddy stem maggot  257–258 rice blue beetle  266–267 rice caseworm  217–219 rice ear-cutting caterpillar  227–229 rice grasshoppers  188–190 rice green semiloopers  239–241 rice leaf beetle  268–269 rice leafflolders  214–215 Fijian 216 rice leaf miner  246–248 rice skipper  223–224 rice swarming caterpillar  234–236 rice thrips  206–208 rice whitefly  203 rice whorl maggot  244–245, 249–252 short-horned grasshoppers  193–194 South American rice miner  253–255 spider mites  204–205 variegated grasshopper  195–197 whitefly 201–202 Foliage feeding aphids  275 Gold-fringed rice borer  68–69 Green hairy caterpillars  240 Green horned caterpillar  218–219 Green leafhoppers  140–141 Habitat management  327–328 Host plant resistance  321–323 Insecticide resistance  331 Insect population dynamics  325–326 Integrated pest management (IPM) augmentative biological control  330 dissemination mechanisms for  334–336 fertilizer management  324–326 habitat management  329 host plant resistance  323–324 insect population dynamics  327–328 natural pest regulation  327–331 overview 253–254 selective insecticides economic action thresholds  331–332 insecticide resistance  333 selectivity against natural enemies  332 Ladybird beetle  273–274 Large rice grasshoppers  188–190

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346 LCB. see Lesser cornstalk borer (LCB) Leafhoppers and planthoppers brown planthopper  155–159 green leafhoppers  140–141 Nephotettix afer Ghauri  141–143 Nephotettix cincticeps  145–147 Nephotettix malayanus  149–151 Nephotettix modulatus Melichar  141–143 Nephotettix nigropictus  143–145 Nephotettix virescens  147–150 overview 107–109 rice delphacid  164–167 smaller brown planthopper  153–155 spittlebugs 169–172 white-backed planthopper  160–163 white rice leafhoppers  138–140 zigzag leafhopper  151–152 Leaf miner  254–256 Lesser cornstalk borer (LCB)  110–113 Mass media campaign (MMC)  332–334 Meadow grasshoppers  196–198 Mexican rice borer  113–115 MMC. see Mass media campaign (MMC) Mole cricket  3–5 Natural pest regulation  325–326 Nephotettix afer Ghauri  141–143 Nephotettix cincticeps  145–147 Nephotettix malayanus  149–151 Nephotettix modulatus Melichar  141–143 Nephotettix nigropictus  143–145 Nephotettix virescens  147–150 Oryzophagus oryzae  41–43 Paddy root weevil  35–36 Paddy stem maggot  255–257 Panicle thrips  313–315 Pecky rice  286 Rice blue beetle  266–267 Rice bugs  295–300 Rice caseworm  217–219 Rice delphacid  164–168 Rice ear-cutting caterpillar  227–229 Rice grasshoppers  188–190 Rice green semiloopers  239–241 Rice leaf beetle  268–269 Rice leafflolders  214–215 Fijian 216 Rice leaf miner  246–248

Index Rice mealybug  10–11 Rice panicle feeders alydid bugs  291–294 blister beetles  313–314 earwigs 311–312 overview 227–228 panicle thrips  315–316 rice bugs  295–300 rice stink bugs  305–310 southern green stink bug  303–304 stink bugs  289, 301–302 Rice plant weevil  33–34 Rice root weevil  31–32 Rice seedling flies  23–24 Rice seed midges  19–21 Rice skipper  221–223 Rice stalk stink bug  15–16 Rice stem borers and gall midges African pink borer  97–100 African rice gall midge  120–124 African striped rice borer  83–85 African white borer  86–90 American rice stalk borer  76–78 Asian rice gall midge  116–119 Asiatic pink stem borer  102–104 dark-headed stem borer  70–72 gold-fringed rice borer  68–69 lesser cornstalk borer (LCB)  110–112 Mexican rice borer  113–115 overview 44–46 rice striped borer  79–82 South American white borer  105–107 spotted stem borer  73–75 stalk-eyed borer  61–64 stalk-eyed fly  65–67 sugarcane borer  107–109 white stem borer  95–97 yellow stem borer  91–95 Rice stem maggot  22–23 Rice stink bugs  305–310 Rice striped borer  79–82 Rice swarming caterpillar  232–234 Rice thrips  204–207 Rice water weevil  37–39, 43–44 Rice whitefly  160–161 Rice whorl maggot  242–243, 195–198 Root and stem feeders African subterranean termites  44–48 black beetles  25–26 black bugs  12–15 ‘chafers’ (white grubs)  26–28 chinch bug  17–18

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Index347 colaspis beetles  28–30 mole cricket  3–5 Oryzophagus oryzae  41–43 overview 2 paddy root weevil  35–36 rice mealybug  10–11 rice plant weevil  33–34 rice root weevil  31–32 rice seedling flies  23–24 rice seed midges  19–21 rice stalk stink bug  15–16 rice stem maggot  22–23 rice water weevil  37–39, 43–44 root aphids  5–8 South American root-feeding termites  49–50 Root aphids  5–8 Selective insecticides economic action thresholds  331–332 insecticide resistance  331 selectivity against natural enemies  332 Short-horned grasshoppers  193–194 Smaller brown planthopper  153–155

South American rice miner  253–255 South American root-feeding termites  49–50 South American white borer  105–107 Southern green stink bug  303–304 Spider mites  204–205 Spittlebugs 169–172 Spotted stem borer  73–75 Stalk-eyed borer  61–64 Stalk-eyed fly  65–67 Stink bugs  289, 301–302 Stink bugs  289 Sugarcane borer  107–109 Variegated grasshopper  195–197 White-backed planthopper  160–163 Whitefly 201–202 White rice leafhoppers  138–140 White stem borer  95–97 Yellow stem borer  91–95 Zigzag leafhopper  151–152

© Burleigh Dodds Science Publishing Limited, 2017. All rights reserved.