Animal Diversity and Biogeography of the Cuatro Ciénegas Basin [1st ed.] 978-3-030-11261-5;978-3-030-11262-2
This volume investigates the contemporary fauna that inhabit the Cuatro Ciénegas Basin. Divided into 15 chapters, it add
460 59 7MB
English Pages XV, 231 [240] Year 2019
Polecaj historie
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Table of contents :
Front Matter ....Pages i-xv
The Fauna of the Cuatro Ciénegas Basin, a Unique Assemblage of Species, Habitats, and Evolutionary Histories (Fernando Álvarez, Margarita Ojeda)....Pages 1-10
Helminth Community Structure of Some Freshwater Fishes of the Cuatro Ciénegas Basin: Patterns and Processes (Gerardo Pérez-Ponce de León, Rogelio Aguilar-Aguilar)....Pages 11-27
Abundance and Diversity of the Soil Microarthropod Fauna from the Cuatro Ciénegas Basin (Margarita Ojeda, Jaime Gasca-Pineda)....Pages 29-51
Scorpions (Arachnida: Scorpiones) from the Cuatro Ciénegas Basin (Oscar F. Francke B.)....Pages 53-59
The Spiders of the Churince Region, Cuatro Ciénegas Basin: A Comparison with Other Desert Areas of North America (Pablo Corcuera, María Luisa Jiménez, Marco Antonio Desales-Lara)....Pages 61-75
Crustaceans from the Cuatro Ciénegas Basin: Diversity, Origin, and Endemism (Fernando Álvarez, José Luis Villalobos)....Pages 77-90
Spatial and Temporal Patterns of Diversity of the Lepidoptera (Papilionoidea sensu lato) in the Cuatro Ciénegas Basin (Jessica Hernández-Jerónimo, Uri Omar García-Vázquez, Omar Ávalos-Hernández, Arturo Arellano-Covarrubias, Moisés Armando Luis-Martínez, Marysol Trujano-Ortega)....Pages 91-104
Diversity and Resource Use Patterns of Bees and Flies that Visit Flowers in the Cuatro Ciénegas Basin (Omar Ávalos-Hernández, Marysol Trujano-Ortega, Uri Omar García-Vázquez, Olivia Yánez-Ordóñez)....Pages 105-116
Odonata of the Cuatro Ciénegas Basin (Héctor Ortega-Salas, Enrique González-Soriano)....Pages 117-128
Diversity and Community Structure of Ants in the Cuatro Ciénegas Basin, Coahuila, Mexico (Milan Janda, Madai Rosas-Mejía, Pablo Corcuera, Mario Josué Aguilar-Méndez, Miguel Vásquez-Bolaños, Yuliza Tafoya-Alvarado)....Pages 129-145
Prostigmatid Mites (Arachnida, Acariformes, Prostigmata) Parasitic on Amphibians and Reptiles in the Cuatro Ciénegas Basin (Ricardo Paredes-León)....Pages 147-160
Systematics of the Fish from the Cuatro Ciénegas Basin (Héctor Espinosa-Pérez, Christian Lambarri-Martínez)....Pages 161-173
Diversity of Amphibians and Reptiles in the Cuatro Ciénegas Basin (Uri Omar García-Vázquez, Marysol Trujano-Ortega, Arturo Contreras-Arquieta, Omar Ávalos-Hernández, Omar Osvaldo Escobedo-Correa, Pablo Corcuera)....Pages 175-188
The Birds of the Cuatro Ciénegas Basin, a Wetland Within the Chihuahuan Desert (Pablo Corcuera, Adolfo Navarro-Sigüenza, Omar Suárez-García)....Pages 189-201
Evaluating the Hypothesis of Pleistocene Refugia for Mammals in the Cuatro Ciénegas Basin (Niza Gámez, Gabriela Castellanos-Morales)....Pages 203-224
Back Matter ....Pages 225-231
Citation preview
Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis
Fernando Álvarez Margarita Ojeda Editors
Animal Diversity and Biogeography of the Cuatro Ciénegas Basin
Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis Series Editors: Valeria Souza Ecology Institute Universidad Nacional Autónoma de México Mexico City, Distrito Federal, Mexico Luis E. Eguiarte Ecology Institute Universidad Nacional Autónoma de México Mexico City, Distrito Federal, Mexico
This book series describes the diversity, ecology, evolution, anthropology, archeology and geology of an unusually diverse site in the desert that is paradoxically one of the most phosphorus-poor sites that we know of. The aim of each book is to promote critical thinking and not only explore the natural history, ecology, evolution and conservation of the oasis, but also consider various scenarios to unravel the mystery of why this site is the only one of its kind on the planet, how it evolved, and how it has survived for so long. More information about this series at http://www.springer.com/series/15841
Fernando Álvarez • Margarita Ojeda Editors
Animal Diversity and Biogeography of the Cuatro Ciénegas Basin
Editors Fernando Álvarez Colección Nacional de Crustáceos Instituto de Biologia Universidad Nacional Autónoma de México Mexico City, Mexico
Margarita Ojeda Colección Nacional de Crustáceos Instituto de Biología Universidad Nacional Autónoma de México Mexico City, Mexico
ISSN 2523-7284 ISSN 2523-7292 (electronic) Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis ISBN 978-3-030-11261-5 ISBN 978-3-030-11262-2 (eBook) https://doi.org/10.1007/978-3-030-11262-2 Library of Congress Control Number: 2019934956 © Springer Nature Switzerland AG 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Preface by the Editors
The project to publish a book series on the Cuatro Ciénegas Basin (CCB) came first as an ambitious idea that would need the contributions of many scientists. Valeria Souza and Luis Eguiarte, two Mexican scientists profoundly committed to the study and conservation of this unique site, led the way to organize a vast network of friends and collaborators to crystallize the original idea. After a decade of visiting the area to obtain samples, measurements, and field data, and after a number of specific studies were published, it was time to compile the results of this enormous effort in a series that would update the knowledge that had been accumulating. The series on the “Cuatro Ciénegas Basin: an Endangered Hyperdiverse Oasis,” opened with a first volume Cuatro Ciénegas Ecology, Natural History and Microbiology, followed by the second volume Ecosystem Ecology and Geochemistry of Cuatro Ciénegas. Herein we present the third volume Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, which is a compilation of new studies on the fauna from the CCB that have been conducted in the last decade, updating in most cases previous studies of species inventories and in others presenting completely new information and analyses on systematics, biogeography, and ecology. The volume is composed of 15 chapters that deal with over 20 animal groups: Platyhelminthes, Nematoda, Acanthocephala, Mollusca, Crustacea, Scorpiones, Araneae, Acari, Collembola, Papilionoidea, Diptera, Coleoptera, Hemiptera, Hymenoptera, Psocoptera, Odonata, Pisces, Amphibia, Reptilia, Aves, and Mammalia. Organizing and editing this book was a very rewarding experience, and we enjoyed the support and enthusiasm of all the authors, some of whom have been longtime friends and colleagues. We would like to express our gratitude to Valeria Souza whose leadership has been fundamental to undertake all these projects and to succeed in putting Cuatro Ciénegas in the spotlight. Our gratitude and admiration to Luis Eguiarte who has always shared his intelligence when difficult and interesting questions arise. The funding agencies that supported the research in Cuatro Ciénegas
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all these years, WWF and Carlos Slim Foundation, are gratefully acknowledged. We hope that this book series will become a powerful statement in the continued endeavor to preserve Cuatro Ciénegas. Mexico City, Mexico Fernando Álvarez Margarita Ojeda
Contents
1 The Fauna of the Cuatro Ciénegas Basin, a Unique Assemblage of Species, Habitats, and Evolutionary Histories������������ 1 Fernando Álvarez and Margarita Ojeda 1.1 Introduction�������������������������������������������������������������������������������������� 1 1.2 The Fauna������������������������������������������������������������������������������������������ 3 1.3 This Volume�������������������������������������������������������������������������������������� 3 1.4 The Future���������������������������������������������������������������������������������������� 6 1.5 Conclusions�������������������������������������������������������������������������������������� 6 References�������������������������������������������������������������������������������������������������� 8 2 Helminth Community Structure of Some Freshwater Fishes of the Cuatro Ciénegas Basin: Patterns and Processes������������ 11 Gerardo Pérez-Ponce de León and Rogelio Aguilar-Aguilar 2.1 Introduction�������������������������������������������������������������������������������������� 12 2.2 Diversity of Freshwater Fish Helminth Parasites of the Cuatro Ciénegas Basin������������������������������������������������������������ 13 2.3 Helminth Parasite Community Structure������������������������������������������ 17 2.3.1 Methods of Study������������������������������������������������������������������ 17 2.3.2 Patterns of Community Structure������������������������������������������ 17 2.4 Discussion ���������������������������������������������������������������������������������������� 20 References�������������������������������������������������������������������������������������������������� 24 3 Abundance and Diversity of the Soil Microarthropod Fauna from the Cuatro Ciénegas Basin ������������������������������������������������ 29 Margarita Ojeda and Jaime Gasca-Pineda 3.1 Introduction�������������������������������������������������������������������������������������� 30 3.2 Materials and Methods���������������������������������������������������������������������� 31 3.2.1 Study Area���������������������������������������������������������������������������� 31 3.2.2 Sampling ������������������������������������������������������������������������������ 31 3.2.3 Taxonomic Determination���������������������������������������������������� 32 3.2.4 Data Analysis������������������������������������������������������������������������ 33
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3.3 Results���������������������������������������������������������������������������������������������� 33 3.3.1 Abundance���������������������������������������������������������������������������� 33 3.3.2 Diversity�������������������������������������������������������������������������������� 38 3.4 Discussion ���������������������������������������������������������������������������������������� 46 3.5 Conclusions�������������������������������������������������������������������������������������� 47 References�������������������������������������������������������������������������������������������������� 47 4 Scorpions (Arachnida: Scorpiones) from the Cuatro Ciénegas Basin������������������������������������������������������������������������������������������ 53 Oscar F. Francke B. 4.1 Introduction�������������������������������������������������������������������������������������� 53 4.2 Diversity and Endemism������������������������������������������������������������������ 54 4.3 Origins and Biogeography���������������������������������������������������������������� 54 4.4 Discussion ���������������������������������������������������������������������������������������� 58 References�������������������������������������������������������������������������������������������������� 59 5 The Spiders of the Churince Region, Cuatro Ciénegas Basin: A Comparison with Other Desert Areas of North America�������������������������������������������������������������������������������������� 61 Pablo Corcuera, María Luisa Jiménez, and Marco Antonio Desales-Lara 5.1 Introduction�������������������������������������������������������������������������������������� 62 5.2 Materials and Methods���������������������������������������������������������������������� 63 5.2.1 Study Sites���������������������������������������������������������������������������� 63 5.2.2 Statistical Analyses �������������������������������������������������������������� 66 5.3 Results���������������������������������������������������������������������������������������������� 66 5.4 Discussion ���������������������������������������������������������������������������������������� 70 5.4.1 Species Richness Variation Among Regions������������������������ 70 5.4.2 Differences in Composition�������������������������������������������������� 71 5.4.3 Biogeographical Classification �������������������������������������������� 72 5.4.4 Spider Assemblages and Vegetation Types �������������������������� 73 References�������������������������������������������������������������������������������������������������� 74 6 Crustaceans from the Cuatro Ciénegas Basin: Diversity, Origin, and Endemism ���������������������������������������������������������� 77 Fernando Álvarez and José Luis Villalobos 6.1 Introduction�������������������������������������������������������������������������������������� 77 6.2 Materials and Methods���������������������������������������������������������������������� 78 6.3 Results���������������������������������������������������������������������������������������������� 79 6.3.1 Diversity�������������������������������������������������������������������������������� 79 6.3.2 Lineages�������������������������������������������������������������������������������� 82 6.3.3 Endemism ���������������������������������������������������������������������������� 85 6.4 Discussion ���������������������������������������������������������������������������������������� 86 References�������������������������������������������������������������������������������������������������� 87
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7 Spatial and Temporal Patterns of Diversity of the Lepidoptera (Papilionoidea sensu lato) in the Cuatro Ciénegas Basin �������������������� 91 Jessica Hernández-Jerónimo, Uri Omar García-Vázquez, Omar Ávalos-Hernández, Arturo Arellano-Covarrubias, Moisés Armando Luis-Martínez, and Marysol Trujano-Ortega 7.1 Introduction�������������������������������������������������������������������������������������� 92 7.2 Materials and Methods���������������������������������������������������������������������� 93 7.2.1 Fieldwork������������������������������������������������������������������������������ 94 7.2.2 Taxonomic Determination���������������������������������������������������� 94 7.2.3 Data Analysis������������������������������������������������������������������������ 94 7.3 Results���������������������������������������������������������������������������������������������� 95 7.3.1 Species Richness������������������������������������������������������������������ 95 7.3.2 Similarity������������������������������������������������������������������������������ 96 7.3.3 Complementarity������������������������������������������������������������������ 96 7.3.4 Phenology ���������������������������������������������������������������������������� 97 7.3.5 Feeding Guilds���������������������������������������������������������������������� 98 7.3.6 Biogeographic Affinity��������������������������������������������������������� 99 7.4 Discussion ���������������������������������������������������������������������������������������� 99 References�������������������������������������������������������������������������������������������������� 102 8 Diversity and Resource Use Patterns of Bees and Flies that Visit Flowers in the Cuatro Ciénegas Basin������������������ 105 Omar Ávalos-Hernández, Marysol Trujano-Ortega, Uri Omar García-Vázquez, and Olivia Yánez-Ordóñez 8.1 Introduction�������������������������������������������������������������������������������������� 106 8.2 Materials and Methods���������������������������������������������������������������������� 107 8.2.1 Sampling Sites���������������������������������������������������������������������� 107 8.2.2 Fieldwork������������������������������������������������������������������������������ 108 8.2.3 Taxonomic Determination���������������������������������������������������� 108 8.2.4 Data Analysis������������������������������������������������������������������������ 108 8.3 Results���������������������������������������������������������������������������������������������� 109 8.4 Discussion ���������������������������������������������������������������������������������������� 112 References�������������������������������������������������������������������������������������������������� 115 9 Odonata of the Cuatro Ciénegas Basin�������������������������������������������������� 117 Héctor Ortega-Salas and Enrique González-Soriano 9.1 Introduction�������������������������������������������������������������������������������������� 117 9.2 Diversity�������������������������������������������������������������������������������������������� 118 9.3 Biogeography and Conservation������������������������������������������������������ 119 9.4 Discussion ���������������������������������������������������������������������������������������� 125 References�������������������������������������������������������������������������������������������������� 127
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10 Diversity and Community Structure of Ants in the Cuatro Ciénegas Basin, Coahuila, Mexico�������������������������������������������������������������������������� 129 Milan Janda, Madai Rosas-Mejía, Pablo Corcuera, Mario Josué Aguilar-Méndez, Miguel Vásquez-Bolaños, and Yuliza Tafoya-Alvarado 10.1 Introduction������������������������������������������������������������������������������������ 130 10.2 Materials and Methods�������������������������������������������������������������������� 131 10.2.1 Study Site�������������������������������������������������������������������������� 131 10.2.2 Sampling �������������������������������������������������������������������������� 132 10.2.3 Data Processing and Analysis ������������������������������������������ 132 10.3 Results�������������������������������������������������������������������������������������������� 133 10.3.1 Habitat Preferences ���������������������������������������������������������� 133 10.4 Discussion �������������������������������������������������������������������������������������� 134 10.4.1 Community Structure and Habitat Preferences���������������� 140 10.4.2 Notes About Select Ant Species Occurring in the Cuatro Ciénegas Basin�������������������������������������������� 141 10.4.3 Myrmecocystus wheeleri Snelling, 1971�������������������������� 141 10.4.4 Pogonomyrmex maricopa Wheeler, 1914 ������������������������ 141 10.4.5 Temnothorax paiute Snelling et al. 2014�������������������������� 142 10.4.6 Cyphomyrmex wheeleri Forel, 1900 �������������������������������� 142 10.4.7 Crematogaster laeviuscula Mayr, 1870���������������������������� 142 10.4.8 Camponotus essigi Smith, 1923���������������������������������������� 142 10.4.9 Temnothorax subditivus (Wheeler, 1903) ������������������������ 143 10.4.10 Temnothorax nitens (Emery, 1895) ���������������������������������� 143 10.4.11 Pseudomyrmex pallidus (Smith, 1855) ���������������������������� 143 10.4.12 Neivamyrmex nigrescens (Cresson, 1872)������������������������ 143 References�������������������������������������������������������������������������������������������������� 144 11 Prostigmatid Mites (Arachnida, Acariformes, Prostigmata) Parasitic on Amphibians and Reptiles in the Cuatro Ciénegas Basin������������������������������������������������������������������������������������������ 147 Ricardo Paredes-León 11.1 Introduction������������������������������������������������������������������������������������ 148 11.2 Materials and Methods�������������������������������������������������������������������� 149 11.3 Diversity������������������������������������������������������������������������������������������ 150 11.3.1 Trombiculidae and Leeuwenhoekiidae ���������������������������� 150 11.3.2 Pterygosomatidae�������������������������������������������������������������� 152 11.4 Endemism �������������������������������������������������������������������������������������� 154 11.5 Origin���������������������������������������������������������������������������������������������� 155 11.6 Biogeography���������������������������������������������������������������������������������� 156 11.7 Conservation Status������������������������������������������������������������������������ 156 11.8 Discussion �������������������������������������������������������������������������������������� 157 References�������������������������������������������������������������������������������������������������� 157
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12 Systematics of the Fish from the Cuatro Ciénegas Basin�������������������� 161 Héctor Espinosa-Pérez and Christian Lambarri-Martínez 12.1 Introduction������������������������������������������������������������������������������������ 161 12.2 Diversity and Endemism���������������������������������������������������������������� 163 12.2.1 Cypriniformes ������������������������������������������������������������������ 164 12.2.2 Characiformes ������������������������������������������������������������������ 164 12.2.3 Siluriformes���������������������������������������������������������������������� 165 12.2.4 Cyprinodontiformes���������������������������������������������������������� 165 12.2.5 Cichliformes���������������������������������������������������������������������� 167 12.2.6 Perciformes ���������������������������������������������������������������������� 168 12.3 Conservation Status������������������������������������������������������������������������ 168 12.4 Discussion �������������������������������������������������������������������������������������� 169 References�������������������������������������������������������������������������������������������������� 170 13 Diversity of Amphibians and Reptiles in the Cuatro Ciénegas Basin������������������������������������������������������������������������������������������ 175 Uri Omar García-Vázquez, Marysol Trujano-Ortega, Arturo Contreras-Arquieta, Omar Ávalos-Hernández, Omar Osvaldo Escobedo-Correa, and Pablo Corcuera 13.1 Introduction������������������������������������������������������������������������������������ 176 13.2 Materials and Methods�������������������������������������������������������������������� 177 13.2.1 Fieldwork�������������������������������������������������������������������������� 178 13.2.2 Taxonomic Determination������������������������������������������������ 178 13.2.3 Data Analysis�������������������������������������������������������������������� 178 13.3 Results�������������������������������������������������������������������������������������������� 179 13.3.1 Species Richness�������������������������������������������������������������� 179 13.3.2 Diversity���������������������������������������������������������������������������� 180 13.3.3 Similarity�������������������������������������������������������������������������� 181 13.3.4 Biogeographic Affinity����������������������������������������������������� 181 13.4 Discussion �������������������������������������������������������������������������������������� 184 References�������������������������������������������������������������������������������������������������� 186 14 The Birds of the Cuatro Ciénegas Basin, a Wetland Within the Chihuahuan Desert�������������������������������������������������������������� 189 Pablo Corcuera, Adolfo Navarro-Sigüenza, and Omar Suárez-García 14.1 Introduction������������������������������������������������������������������������������������ 190 14.2 Methods������������������������������������������������������������������������������������������ 191 14.2.1 Study Area������������������������������������������������������������������������ 191 14.2.2 Data Analysis�������������������������������������������������������������������� 192 14.3 Results�������������������������������������������������������������������������������������������� 193 14.3.1 North American Deserts���������������������������������������������������� 193 14.3.2 Cuatro Ciénegas and Other North American Deserts ������ 193 14.3.3 Local Diversity������������������������������������������������������������������ 194 14.4 Discussion �������������������������������������������������������������������������������������� 197 References�������������������������������������������������������������������������������������������������� 199
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15 Evaluating the Hypothesis of Pleistocene Refugia for Mammals in the Cuatro Ciénegas Basin������������������������������������������ 203 Niza Gámez and Gabriela Castellanos-Morales 15.1 Introduction������������������������������������������������������������������������������������ 204 15.2 Methods������������������������������������������������������������������������������������������ 207 15.3 Results�������������������������������������������������������������������������������������������� 208 15.4 Discussion �������������������������������������������������������������������������������������� 220 15.5 Conclusions������������������������������������������������������������������������������������ 221 References�������������������������������������������������������������������������������������������������� 222 Index������������������������������������������������������������������������������������������������������������������ 225
Contributors
Rogelio Aguilar-Aguilar Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Mario Josué Aguilar-Méndez Departamento de Biología, División de Ciencias Naturales y Exactas, Campus Guanajuato, Universidad de Guanajuato, Guanajuato, Guanajuato, Mexico Fernando Álvarez Colección Nacional de Crustáceos, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico Arturo Arellano-Covarrubias Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Omar Ávalos-Hernández Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Gabriela Castellanos-Morales Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur-Villahermosa, Villahermosa, Tabasco, Mexico Arturo Contreras-Arquieta Acuario y Herpetario W. L. Minckley, Cuatro Ciénegas de Carranza, Coahuila, Mexico Pablo Corcuera Laboratorio de Ecología Animal, Departamento de Biología, Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico Marco Antonio Desales-Lara Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico Omar Osvaldo Escobedo-Correa Departamento de Biología, Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico Héctor Espinosa-Pérez Colección Nacional de Peces, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico xiii
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Contributors
Oscar F. Francke B. Colección Nacional de Arácnidos, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Niza Gámez Facultad de Estudios Superiores, Zaragoza, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Uri Omar García-Vázquez Laboratorio de Sistemática Molecular, Unidad de Investigación Multidisciplinaria de Investigación Experimental Zaragoza, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Jaime Gasca-Pineda Departamento de Biología de la Conservación, Centro de Investigación Científica y, Educación Superior de Ensenada, Ensenada, Baja California, Mexico Enrique González-Soriano Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Jessica Hernández-Jerónimo Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Milan Janda Laboratorio Nacional de Análisis y Síntesis Ecológica, Escuela Nacional de Estudios Superiores-Morelia, Universidad Nacional Autónoma de México, Michoacán, Mexico Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech Republic María Luisa Jiménez Laboratorio de Aracnología y Entomología, Centro de Investigaciones Biológicas del Noroeste, Instituto Politécnico Nacional, La Paz, Baja California Sur, Mexico Christian Lambarri-Martínez Colección Nacional de Peces, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Moisés Armando Luis-Martínez Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Adolfo Navarro-Sigüenza Museo de Zoología, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Margarita Ojeda Colección Nacional de Ácaros, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico Héctor Ortega-Salas Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Ricardo Paredes-León Colección Nacional de Ácaros, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico
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Gerardo Pérez-Ponce de León Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Madai Rosas-Mejía Universidad Autónoma de Tamaulipas, Instituto de Ecología Aplicada, Ciudad Victoria, Tamaulipas, Mexico Omar Suárez-García Programa de Doctorado, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Oaxaca, Instituto Politécnico Nacional, Santa Cruz Xoxocotlán, Oaxaca, Mexico Yuliza Tafoya-Alvarado Laboratorio Nacional de Análisis y Síntesis Ecológica, Escuela Nacional de Estudios Superiores-Morelia, Universidad Nacional Autónoma de México, Michoacán, Mexico Marysol Trujano-Ortega Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Miguel Vásquez-Bolaños Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Jalisco, Mexico José Luis Villalobos Colección Nacional de Crustáceos, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Olivia Yáñez-Ordóñez Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico
Chapter 1
The Fauna of the Cuatro Ciénegas Basin, a Unique Assemblage of Species, Habitats, and Evolutionary Histories Fernando Álvarez and Margarita Ojeda
Abstract In this chapter we review some of the main characteristics of the Cuatro Ciénegas Basin, touching upon the physical setting, its geologic history, and animal diversity. We go through all the chapters of the volume summarizing the different interpretations of the authors regarding the origin and structuring of the particular communities. We present a list of animal taxa that have been recorded from the area, noting the number of species and supraspecific taxa that are endemic to the CCB: a total of 885 species are reported for the CCB in this volume, of which 38 (4.3%) are endemic. A brief discussion on the future challenges that the CCB faces is presented. Keywords Chihuahuan Desert · Diversity · Endemism · Conservation
1.1 Introduction It has been mentioned many times that the Cuatro Ciénegas Basin (CCB) is a unique place, surprising the observer with its wealth of life. The CCB constitutes an oasis, which is always somewhat of a contradiction for the biologist, since it represents an aquatic environment within the desert. The CCB lies in the southeastern portion of the Chihuahuan Desert (CD), the largest desert in North America, with over 450,000 km2, and it harbors a diverse biota making it one of the more diverse deserts in the world (Morafka 1977).
F. Álvarez (*) Colección Nacional de Crustáceos, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico e-mail: [email protected] M. Ojeda Colección Nacional de Ácaros, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_1
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Regarding its modern history, the CCB seems to have been a four-swamp system, the reason for the name “Cuatro Ciénegas,” before water started to be canalized out of the valley to be used in a series of towns on the way east to Monclova in the 1880s (Minckley 1992). Several historic accounts describe that large lagoons formed in a few areas within the valley (Alessio-Robles 1938). Canalization started to move water through “La Polilla” canal located in the southeastern section of the CCB (Minckley 1969). Many other canals were later built to drain Laguna de los Anteojos, Laguna Escobeda, Rio Mezquites, Puerto Salado, Tio Candido, Lagunas de Los Fresnos, and Poza de la Becerra (Minckley 1969). The result of water extraction for such a long time can be seen today in the many partially or totally drained swamps. Another result is that the aquatic environment has been largely fragmented with unknown effects on the previous distribution of species or on the genetic exchange among populations. In fact, biologists started studying the CCB fauna once many changes, especially in the hydrology, had occurred. This raises relevant questions about the meaning of current distribution patterns of species and populations, especially of the aquatic ones. Recent studies on the shrimp Palaemon suttkusi and the pupfishes Cyprinodon atrorus and C. bifasciatus examined the genetic variation associated to the fragmentation of the freshwater bodies, due to water extraction, and/or the creation of new contact zones, due to canalization, inside the CCB (Carson et al. 2012; Álvarez et al. 2014). We can hypothesize that the contemporary genetic make-up of these populations are probably different from what they were before the basin started to be exploited. The origin of the basin is quite remarkable since it is possible that it has been in a stable land mass that has had similar climatic conditions possibly for the last 15 million years (Wilson and Pit 2010; Souza et al. 2012). If this is true then the CCB has served as a refuge many times for animal species as dissimilar as copepods and birds, and harboring speciation events in groups that are completely different such as molluscs and reptiles. In addition to its age, the geographic situation of the CCB, lying at the boundary of the Neotropical and Nearctic biogeographic provinces, in the southern portion of the largest desert in North America, makes it an essential crossroads to understand the evolution of many aquatic and terrestrial animal groups. The resulting stage is then the product of a unique combination of geologic history, geographic location, and biological makeup, which is expressed and recognizable through its species richness and degree of endemism. Two impressive volumes precede this, the third volume of the Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis series conceived and led by Valeria Souza and Luis Eguiarte, from the Instituto de Ecología, UNAM, in Mexico City, Mexico. The first one explores the ecology, natural history, and microbiology of the basin (Souza et al. 2018), whereas the second one is on the ecosystem ecology and geochemistry of the CCB (García-Oliva et al. 2018). In light of the scope of these volumes, herein we adopt a more organismic approach to review the state of knowledge about the different zoological groups present in the CCB.
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1.2 The Fauna The fauna that occurs in the CCB is a mixture of species with Neotropical and Nearctic biogeographic affinities. Most of the zoological groups, including many species, that inhabit the CCB today have a very old origin, dating back to Cretaceous times, and the opening of the Tethys Sea. Many groups, either terrestrial or freshwater, reached the CCB through land from populations whose range expanded and contracted with the glaciations and with emergence of new mountain ranges, probably leaving isolated populations in the CCB when these changes occurred. Through land the CCB could have been colonized from the south or from the north, representing for both geographic components the limit of their distributions. It is interesting to note that the CCB could have also been colonized by marine species that reached the area through the Bravo River Basin at several points in time during high sea level periods. Souza et al. (2012) identified microbial communities which have a marine ancestry and a long history of isolation in the CCB. Several copepods occurring in the CCB have their closest relatives in estuarine/marine environments (Álvarez and Villalobos 2019) in addition to several fish species that have also a marine origin (Espinosa-Pérez and Lambarri-Martínez 2019). Recapitulating, the CCB represents a strategic evolutionary location that has acquired species from the northern Nearctic province, from the southern Neotropical province, and from the ancient Gulf of Mexico. That is, the CCB has been for a long period of time at the confluence of three major pathways that have provided species, some of which adapted to the particular conditions of the CCB and got successfully established.
1.3 This Volume The present contribution is a compilation of new studies on the fauna from the CCB that have been conducted in the last decade, updating in most cases previous studies on species inventories and in others presenting completely new information and analyses on systematics, biogeography, and ecology. The volume is composed of 15 chapters. In the second chapter Pérez-Ponce de León and Aguilar-Aguilar (2019) describe the parasitic helminth communities occurring in the fishes of the CCB. They found a helminth community characterized by a low diversity with an important presence of introduced species which, interestingly, occur in good numbers in host species of Nearctic affinity. The soil microarthropods are analyzed in Chap. 3 by Ojeda and Gasca-Pineda (2019), who describe the richness and diversity of mites, insects, and crustaceans from samples associated to the different vegetation types found in the CCB. The mites were the dominant group with the prostigmatids being the most abundant and diverse group. The insects have species of Collembola, Coleoptera, Hemiptera, Hymenoptera, and Psocoptera; and crustaceans were represented by terrestrial
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isopods. The overall diversity of soil microarthropods for this desert environment was lower, as expected, than what is found in mesic soils. The scorpions of the CCB are reviewed in Chap. 4 (Francke 2019). Until now, 2 out of 12 species are endemic to the CCB. As the author comments, it is possible that the two endemics will be found outside the CCB when more regional studies are undertaken; however, it has been over 30 years since both species were described. The scorpion diversity of the CCB is similar to other sites within the CD in Baja California, California, and Nevada (Francke 2019). The spiders of the CCB are reviewed in Chap. 5 by Corcuera et al. (2019a) based on a study that focused on the fauna from Churince. A total of 159 species were identified belonging to 37 families. The diversity found was comparable to other sites in the Chihuahuan and Sonoran Deserts; however, oases from southern Baja California were more diverse. The type of vegetation, traps, and season are variables that need to be considered when large-scale comparisons of the spider fauna among sites are attempted. In Chap. 6, Álvarez and Villalobos (2019) present an updated list of crustaceans that is used to determine what is the level of endemism in this group and how old are the lineages present in the CCB. They recorded 45 species from four different classes, with seven of them being endemic to the CCB. The crustacean diversity is dominated by the copepods followed by the malacostracans. The endemics belong to very distant groups (Cladocera, Copepoda, Amphipoda, Isopoda, Decapoda), suggesting a very long and strong isolation to have promoted speciation in the different lineages. The butterflies (Papilionoidea sensu lato) are dealt with in Chap. 7; Hernández- Jerónimo et al. (2019) present the first systematic listing for this group specifically for the CCB. A total of 59 species were recorded, which included new records for the CCB, for Coahuila and for Mexico. The biogeographic affinities represented in the CCB butterflies are diverse with more Nearctic species than Neotropical ones. The role of bees and flies as pollinators in the CCB is the topic of Chap. 8. Ávalos-Hernández et al. (2019) describe how 169 species of bees and flies pollinate 39 plant species. Variation in the number of visits was influenced by season, but the diversity of some families of pollinators was higher in the dry season. The analysis presented highlights the importance of flies as pollinators in a dry environment as the CCB. The odonate fauna is treated in Chap. 9 by Ortega-Salas and González-Soriano (2019). The chapter on Odonata updates the knowledge of the group for an area, the CCB and northern Mexico, that has been only superficially studied. The authors report on the endemic to the CCB and recently described Libellula coahuiltecana (Ortega-Salas and González-Soriano 2015), which until now has not been collected again. The ants, Chap. 10, of the CCB were studied by Janda et al. (2019) through samplings carried out at Churince Lagoon. Although one third of the species collected were new records for Coahuila, the regional diversity is still very low, compared with what is known for the neighboring states of Nuevo León and Chihuahua. The
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limited area sampled at Churince suggests that the real ant diversity of the whole CCB will be very high. In Chap. 11, Paredes-León (2019) reports on nine species of mites parasitic on amphibians and reptiles from the CCB. All the species reported are new records for the CCB, one for Coahuila, and eight were new host records, including first records of mites parasitic on several species. This new approach to study a specific fauna, once more indicates that the real diversity that we can find in the CCB cannot yet be envisioned. Probably one of the most emblematic groups from the CCB is the fish. In Chap. 12, Espinosa-Pérez and Lambarri-Martínez (2019) go through the 18 species present in the CCB offering comments on their origin, biogeographic affinity, and conservation status. The authors mention the presence of several cryptic species in genera such as Astyanax, Herichthys, and Micropterus, that are in need of more systematic studies. Regarding their conservation status, 11 (61%) of the species present have been classified in a risk category, either in the Nom-059-Semarnat-2010 or in the IUCN Red List. It is indeed a high proportion of the ichthyofauna from the CCB that is now threatened. With the widespread canalization of the valley and the introduction of species like the spotted jewelfish, Hemichromis guttatus, the challenge to preserve this fauna is enormous. Chapter 13 describes the amphibian and reptile diversity. This chapter by García- Vázquez et al. (2019) assesses the diversity of both groups including the most recent findings, such as the description of a new endemic lizard (García-Vázquez et al. 2018). The CCB is the area with highest endemism for herpetofauna within the CD and probably for all of Mexico (Lemos-Espinal and Smith 2016; García-Vázquez et al. 2019). The authors comment on the absence from their samplings of one amphibian and three reptiles which could have already been extirpated from the CCB. The birds of the CCB are treated in Chap. 14 by Corcuera et al. (2019b). One fourth of the species recorded for the entire CD occur in the CCB. The variety of habitats that the CCB harbors attract a considerable number of visitor, transient and migrant species, more than what was expected. Another salient feature of the CCB avifauna is the high proportion of arid environment species present, suggesting that the area has served as a refuge in the past with a number of species adapting to local conditions. Finally, the CCB is an essential element of the “North American Central Migratory Flyway,” giving the area a fundamental importance. The last chapter explores the role of the CCB as a Pleistocene refuge for mammals (Gámez and Castellanos-Morales 2019). Although the current number of species recorded for the CCB is 39 (Contreras-Balderas et al. 2007), the study suggests that a maximum of 59 might occur in the CCB. Several species occurred in the CCB in the past but no longer are found there as evidenced by archeological remains. The authors suggest that altitude is the main factor in the distribution of mammals and that very little sampling has been done in the mountains surrounding the valley, thus underestimating the real diversity of the area.
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1.4 The Future The canalization of several large ponds and lagoons in the CCB started in the 1880s to help in the development of a series of small towns to the east of the valley. In 1960, although water extraction had been operating for about 80 years, the basin with its native vegetation looked intact (Minckley 1992). This observation suggests that it is in the last 60 years when the area started to deteriorate to reach its present state. It was until 1994, when Mexico signed several international agreements to preserve the natural environment that the CCB was declared a natural reserve: “Area de Protección de Flora y Fauna.” It was in 1995 that the CCB was listed as a “Wetland of International Importance” by the Ramsar Convention. Although the area is under the protection of these and other designations, its transformation into an agricultural district and the drying up of ponds and lagoons are happening at a fast pace with no signs of diminishing. The degradation will eventually reach a point in which the recovery of the system will not be possible. The threat of introduced species in the bodies of water of the CCB is a reality. At least three highly invasive aquatic species have been recorded to date. The gastropod Melanoides tuberculata, the red swamp crayfish Procambarus clarkii, and the spotted jewelfish Hemichromis guttatus have been present in the area for several years and will most likely increase their population sizes and outcompete native species. It is possible too that these species will modify the microhabitat conditions, will introduce new parasites and will affect not only their close relatives, but also unrelated species outside their taxonomic group. Until now no known efforts are being undertaken to control these exotics. Another element that has to be considered when designing conservation strategies is the presence of cryptic species. In various, unrelated, completely different animal groups the presence of cryptic species has been detected. In crustaceans, and fishes, for example, taxonomic studies based on molecular data have clearly unveiled the presence of several species complexes. These new taxa will undoubtedly modify, first, the diversity estimates we have for the entire system but also can unveil several more endemic species, increasing the importance for conservation that the region has. As in other ecosystems, for example, coral reefs, it is possible that many species in the CCB could disappear before we have recognized them.
1.5 Conclusions It is clear that the CCB is a special place that still holds wonders to be discovered. Its location, its history, and the life forms that have made their home in it all combine to produce a unique setting that deserves to be protected and preserved for the future. However, the risk of losing it is real. We are seeing how the degradation is advancing and no actions are taken to stop or counteract the water extraction, to protect the native flora, or to prevent the arrival of more introduced species. The account that derives from the results presented in this volume shows that the CCB has up to now 885 species, 38 (4.3%) of which are endemic to the basin (Table 1.1).
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Table 1.1 Number of animal species and endemic taxa recorded in the Cuatro Ciénegas Basin, Coahuila, Mexico
Platyhelminthesa
Species in the CCB 12
Endemic taxa –
Nematodaa
9
–
Acanthocephalaa
3
–
Mollusca
13
Crustacea
45
Scorpiones Araneae
12 159
% of endemism
1 subfamily, 6 genera, 9 spp. 7 spp.
69
2 spp.
16.6
15.5
Acaric Soil microarthropodsd Papilionoidea
9 65
Dipterae
70
Hymenopteraf
99
Hymenopterag Odonata
33 67
1 sp.
1.5
Pisces
18
8 spp.
44.4
Amphibia
11
2 spp.
18.2
Reptilia
61
9 spp.
14.7
59
Aves Mammalia
101 39
Total
885
1 subfamily, 6 genera, 38 species
Parasitic on fish This volume c Prostigmata parasitic on amphibians and reptiles d Prostigmata, Oribatida, Insecta, Myriapoda, Crustacea e Bombyliidae, Syrphidae f Andrenidae, Apidae, Colletidae, Halictidae, Megachilidae g Formicidae a
b
4.3
Source Pérez-Ponce de León and Aguilar-Aguilar (Chap. 2)b Pérez-Ponce de León and Aguilar-Aguilar (Chap. 2)b Pérez-Ponce de León and Aguilar-Aguilar (Chap. 2)b Hershler (1985) Álvarez and Villalobos (Chap. 6)b Francke (Chap. 4)b Bizuet-Flores et al. (2015); Corcuera et al.(Chap. 5)b Paredes-León (Chap. 11)b Ojeda and Gasca-Pineda (Chap. 3)b Hernández-Jerónimo et al. (Chap. 7)b Ávalos-Hernández et al. (Chap. 8)b Ávalos-Hernández et al. (Chap. 8)b Janda et al. (Chap. 10)b Ortega-Salas and González- Soriano (Chap. 9)b Espinosa-Pérez and Lambarri-Martínez (Chap. 12)b García-Vázquez et al. (Chap. 13)b García-Vázquez et al. (Chap. 13)b Corcuera et al. (Chap. 14)b Contreras-Balderas et al. (2007)
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In particular, the radiation of molluscs in the CCB has been extraordinary, producing in addition to the nine endemic species also one endemic subfamily with six genera. It is worth mentioning that the endemics are, in addition to molluscs, crustaceans, scorpions, odonates, but also fishes, amphibians, and reptiles. The isolation and the geologic history of the basin have been so unique and so intense, as to produce speciation in widely different lineages, similar to what is seen in oceanic island. It is natural that as more species are recognized in the area the level of endemism will decrease. In several cases, species that were thought to be endemic to the CCB have been found outside the basin but in adjacent areas. Although no data exist to corroborate this, at a larger scale the area of endemism might be the main CCB plus the adjacent valleys to the east. However, as more groups are studied and with the description of cryptic species the growing diversity found in the CCB could also produce more endemic species. What we see in the CCB, in any case, is that it is a hotspot of biodiversity, but also a hotspot for endemism, a very unique situation since both phenomena are created by different factors and processes. As stated by Minckley (1992) “By all measures, the scientific values of the Cuatro Cienegas basin are profound, far exceeding the monetary value of its land and water supply as resources for typical development.” Acknowledgments Special thanks to V. Souza and L.E. Eguiarte for supporting this research and for inviting us to prepare this volume. We acknowledge the financial support obtained from the WWF - Carlos Slim Foundation Alliance.
References Alessio-Robles V (1938) Coahuila y Texas en la Epoca Colonial. Editorial Cultura, México Álvarez F, Villalobos JL (2019) Chapter 6. Crustaceans from the Cuatro Ciénegas Basin: diversity, origin and endemism. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Álvarez F, Pedraza-Lara C, Villalobos JL (2014) Indetity of freshwater shrimp populatons (Palaemon Weber, 1795) from northern Mexico: genetic variation at local and regional scales. J Crust Biol 34:481–493 Ávalos-Hernández O, Trujano-Ortega M, García-Vázquez UO, Yáñez-Ordoñez O (2019) Chapter 8. Diversity and resource use patterns of bees and flies that visit flowers in the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Bizuet-Flores MY, Jiménez-Jiménez ML, Zavala-Hurtado A, Corcuera P (2015) Diversity patterns of ground dwelling spiders (Arachnida: Araneae) in five prevailing plant communities of the Cuatro Ciénegas Basin, Coahuila, Mexico. Rev Mex Biodivers 86:153–163 Carson EW, Tobler M, Minckley WL, Ainsworth RJ, Dowling TE (2012) Relationships between spatio-temporal environmental and genetic variation reveal an important influence of exogenous selection in a pupfish hybrid zone. Mol Ecol 21:1209–1222 Contreras-Balderas AJ, Hafner DJ, López-Soto JH, Torres-Ayala JM, Contreras-Arqueta S (2007) Mammals of the Cuatro Ciénegas Basin, Coahuila, Mexico. Southwet Nat 52:400–409
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Corcuera P, Jiménez ML, Desales-Lara MA (2019a) Chapter 5. The spiders of the Churince region, Cuatro Ciénegas Basin: a comparison with other desert areas of North America. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Corcuera P, Navarro-Sigüenza A, Suárez-García O (2019b) Chapter 14. The birds of the Cuatro Ciénegas Basin, a wetland within the Chihuahuan Desert. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Espinosa-Pérez H, Lambarri-Martínez C (2019) Chapter 12. Systematics of the fishes from the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Francke OF (2019) Chapter 4. Scorpions (Arachnida: Scorpiones) from the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Gámez N, Castellanos-Morales G (2019) Chapter 15. Evaluating the hypothesis of Pleistocene refugia for mammals in the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham García-Oliva F, Elser J, Souza V (eds) (2018) Ecosystem ecology and geochemistry of Cuatro Ciénegas. Springer Nature, Cham, 171 pp García-Vázquez UO, Contreras-Arquieta A, Trujano-Ortega M, Nieto-Montes de Oca A (2018) A new species of Gerrhonotus (Squamata: Anguidae) from the Cuatro Ciénegas Basin, Coahuila, Mexico. Herpetologica 74:269–278 García-Vázquez UO, Contreras-Arquieta A, Trujano-Ortega M, Ávalos-Hernández O, Escobedo- Correa OO, Corcuera P (2019) Chapter 13. Diversity of amphibians and reptiles in the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Hernández-Jerónimo J, García-Vázquez UO, Ávalos-Hernández O, Arellano-Covarrubias A, Luis- Martínez A, Trujano-Ortega M (2019) Chapter 7. Spatial and temporal patterns of diversity of the Lepidoptera (Papilionoidea sensu lato) in the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Hershler RT (1985) Systematic revision of the Hydrobiidae (Gastropoda: Rissoacea) of the Cuatro Ciénegas Basin, Coahuila, Mexico. Malacologia 26:31–123 Janda M, Rosas-Mejía M, Corcuera P, Aguilar-Méndez MJ, Vázquez-Bolaños M, Tafoya-Alvarado Y (2019) Chapter 10. Diversity and community structure of ants in the Cuatro Ciénegas Basin, Coahuila, Mexico. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Lemos-Espinal JA, Smith GR (2016) Amphibians and reptiles of the state of Coahuila, Mexico, with comparison with adjoining states. ZooKeys 593:117–137 Minckley WL (1969) Environments of the Bolsón of Cuatro Cienegas, Coahuila, Mexico. Texas Western Press, The University of Texas at El Paso, 65 pp Minckley WL (1992) Three decades near Cuatro Ciénegas, Mexico: photographic documentation and a plea for area conservation. J Ariz Nev Acad Sci 26:89–118 Morafka DJ (1977) A biogeographical analysis of the Chihuahuan Desert through its herpetofauna. Biogeographica Hague 9:1–313 Ojeda M, Gasca-Pineda J (2019) Chapter 3. Abundance and diversity of the soil microarthropod fauna from the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Ortega-Salas H, González-Soriano E (2015) A new species of Libellula Linnaeus, 1758, from the Cuatro Ciénegas basin, Coahuila, Mexico (Anisoptera: Libellulidae). Zootaxa 4028:589–594 Ortega-Salas H, González-Soriano E (2019) Chapter 9. Odonata of the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham
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Paredes-León R (2019) Chapter 11. Prostigmatid mites (Arachnida: Acariformes: Prostigmata) parasitic on amphibians and reptiles in the Cuatro Ciénegas Basin. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Pérez-Ponce de León G, Aguilar-Aguilar R (2019) Chapter 2. Helminth community structure of some freshwater fishes of the Cuatro Ciénegas Basin: patterns and processes. In: Álvarez F, Ojeda M (eds) Animal diversity and biogeography of the Cuatro Ciénegas Basin. Springer Nature, Cham Souza V, Olmedo-Alvarez G, Eguiarte LE (eds) (2018) Cuatro Ciénegas Ecology, natural history and microbiology. Springer Nature, Cham, 149 pp Souza V, Siefert JL, Escalante AE, Elser JJ, Eguiarte LE (2012) The Cuatro Ciénegas Basin in Coahuila, Mexico: an astrobiological Precambrian Park. Astrobiology 12:641–647 Wilson JS, Pit JP (2010) Illuminating the lack of consensus among descriptions of earth history data in the North American deserts: a resource for biologists. Progr Phys Geog 34:419–441
Chapter 2
Helminth Community Structure of Some Freshwater Fishes of the Cuatro Ciénegas Basin: Patterns and Processes Gerardo Pérez-Ponce de León and Rogelio Aguilar-Aguilar
Abstract Freshwater fishes are usually infected with a wide array of parasites. In particular, the helminth parasite fauna of these hosts consists of larval forms and/or adults of species included in three major phyla: Platyhelminthes (trematodes, cestodes, and monogeneans), Nematoda, and Acanthocephala. Among vertebrates, helminth parasite communities in freshwater fish are generally depauperate, i.e., communities show low species richness and abundance values. The physicochemical characteristics of the freshwater habitat, the host feeding habits, the parasite life-cycle traits, and the historical biogeography of both members of the association are the main factors that determine the parasite community structure. Patterns of community structure of freshwater fish helminths in Mexico have been described in the last two decades, although most studies were conducted in fish occurring in central and southern Mexico, and just a few were carried out in the northern region, where fish with Nearctic affinities are predominant. Water bodies of the Cuatro Ciénegas Basin (CCB), in the State of Coahuila, a characteristic intermontane desert valley in north Mexico, are inhabited by an interesting fish fauna, where most species are part of the Nearctic component. The freshwater fish helminth parasite fauna was recently described for 15 species and comprises 25 species of helminths of which 9 are digeneans, 3 monogeneans, 1 cestode, 3 acanthocephalans, and 9 nematodes. Here, the patterns and processes that determine the helminth community structure of each fish species are presented at both infracommunity and component community levels. Ecological descriptors of parasite communities, i.e., dominance, diversity, abundance, evenness, and similarity, were estimated for ten fish species for which sample size allows an analysis of their parasite communities; five of these fish species possess a Nearctic affinity, while the others belong to fish G. Pérez-Ponce de León (*) Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico e-mail: [email protected] R. Aguilar-Aguilar Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_2
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families with Neotropical affinity. Our results show that the Black bass Micopterus salmoides is the fish species with the highest diversity values at both levels. Most of the communities are dominated by a single helminth species, usually a trematode or a nematode. Remarkably, the dominant species for three parasite communities is an exotic, anthropogenically introduced helminth species, either the cestode Schizocotyle acheilognathi or the trematode Centrocestus formosanus. The processes that determine the helminth parasite community structure in the area are discussed. Keywords Parasites · Trematodes · Cestodes · Nematodes · Acanthocephalans - fish · Parasite community
2.1 Introduction Parasites are recognized as an important component of global biodiversity (Poulin and Morand 2004); the factors determining the structure of helminth communities of vertebrates have been the focus of several research programs over the past three decades (Poulin 1997, 1998; Navarro et al. 2005); the diversity, richness, and abundance of parasite assemblages in their vertebrate and invertebrate hosts are the result of a variety of environmental and non-environmental factors (Dogiel 1961; Neves et al. 2013, 2015; Tavares-Dias et al. 2014; Pantoja et al. 2015), such as pollution, eutrophication, seasonality, environmental changes, and relationships with other parasitic and free-living species (Tavares-Dias 2017); therefore, parasites may be indicators of environmental changes (Pérez-Ponce de León 2014). Several early studies on the freshwater fish helminth communities carried out in the north temperate regions, allowed their authors to postulate the nature of water bodies, along with host diet, as key factors structuring communities, and were characterized as depauperate and isolationists in character, compared with those described for other, mainly endothermic, vertebrates (Aho and Bush 1993). More recently, historical biogeography and phylogenetic histories of the hosts have been considered to act synergistically with the factors mentioned above, to produce parasite faunas with different features, depending on the different hosts involved in their life-cycle. Helminth communities of freshwater fish of these northern regions are then considered as predictable, species-poor, and usually dominated by a single parasite species. However, factors involved in the structure of helminth communities in fresh- water fish across tropical and sub-tropical regions are currently less known. Mexico has the largest percentage of known freshwater fish species for which parasites have been recorded (Luque and Poulin 2007; Pérez-Ponce de León and Choudhury 2010; Scholz and Choudhury 2014). Some of the published studies have focused on describing the helminth communities in terms of species composition, species richness, diversity, and dominance, at the infracommunity and/or component community levels. Most of these studies were carried out in freshwater fish with a Nearctic affinity occurring in central Mexico, such as Goodeidae (Rojas et al. 1997;
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érez-Ponce de León et al. 2000; Martínez-Aquino et al. 2004, 2007, 2009, 2011), P Atherinopsidae (Espinosa-Huerta et al. 1996; Pérez-Ponce de León et al. 2000), Cyprinidae (Aguilar-Aguilar et al. 2010, 2016), and Cyprinodontidae (Martínez- Aquino and Aguilar-Aguilar 2008). Comparatively, a reduced number of studies have been developed in tropical (Neotropical) Mexico. Despite the great diversity of fish species in southern Mexico, the helminth communities of just a few of them have been studied, for example, Lepisosteidae (Salgado-Maldonado et al. 2004), Poeciliidae (Salgado-Maldonado et al. 2014b), and Cichlidae (Salgado-Maldonado and Kennedy 1997; Violante-González et al. 2008).
2.2 D iversity of Freshwater Fish Helminth Parasites of the Cuatro Ciénegas Basin The intermontane Cuatro Ciénegas Basin (CCB) is located at the edge of the Sierra Madre Oriental in the Mexican state of Coahuila, northern Mexico. The CCB is a desert area of approximately 1000 km2, with the greatest number of endemic species of any place in North America (Stein et al. 2000), holding a large biodiversity and more than 70 endemic species. In the CCB diverse aquatic and semi-aquatic habitats as springs, marshes, rivers, and lakes are found (Marsh 1984). These freshwater ecosystems support an unusually diverse fish fauna for a North American desert region. The fish fauna consists of 16 native fish species, 8 of which are endemic (Minckley 1984). Five out of the 16 species are Neotropical in origin and extend their most northern distribution range up to northern Mexico. The Neotropical component includes three species of cichlids, one poeciliid and one characid. The other 11 species are Nearctic and comprise typical members of this biogeographical region, including centrarchids, cyprinids, ictalurids, and cyprinodontids (Miller et al. 2005). The freshwater fish helminth fauna of the CCB has been scarcely studied. Until 2005 only 10 species had been recorded, including seven species of trematodes, two of monogeneans (Guajardo-Martínez 1984), and one acanthocephalan (Jiménez et al. 1981; Guajardo-Martínez 1984; Meffe 1985). However, Aguilar-Aguilar et al. (2014) conducted a 3-year survey of the helminth parasites of freshwater fish of water bodies within the CCB in which a total of 570 individual fish from 26 localities, comprising 15 species, were analyzed. Aguilar-Aguilar et al. (2014) collected 8324 specimens of helminths. Twenty-five species were identified, including nine trematodes, three monogeneans, one cestode, three acanthocephalans, and nine nematodes (Table 2.1). One of the major conclusions of the aforementioned study was that the inventory of the freshwater fish helminth fauna supported the transitional character of the CCB, where 31% of the fish fauna represented Neotropical components in an area immersed within the Nearctic biogeographical region. The helminth parasite fauna of the Neotropical fish inhabiting the CCB water bodies is characteristic of that geographic region, whereas the same pattern is observed for
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Table 2.1 Freshwater fish helminth fauna of water bodies of Cuatro Ciénegas Helminth taxon (site)/fish species Trematoda Ascocotyle sp. (IW, H) Gambusia marshi
Localities
Canal entre La Vega y el Venado, La Teclita, Camino hacia la Tecla, and Santa Tecla Centrocestus formosanus (Nishigori, 1924) (G) Astyanax mexicanus Canal entre La Vega y el Venado, Río en Celemania, Anteojo San Juan, and Poza La Becerra Cyprinella lutrensis Puente San José de las Águilas Cyprinella xanthicara Canal entre La Vega y el Venado Cyprinodon atrorus x Laguna intermedia bifasciatus Gambusia marshi Puente San José de las Águilas, and Poza La Becerra Lepomis megalotis Río en Celemania Micropterus salmoides Puente San José de las Águilas Notropis sp. Río en Celemania Crassicutis cichlasomae Manter, 1936 (I) [§] Herichthys minckleyi Charcos Prietos, Laguna intermedia, Río Mezquites, and Poza La Becerra Crassicutis sp. (lineage I, sensu Razo-Mendivil et al., 2010) (I) [§] Herichthys Puente San José de las Águilas cyanoguttatus Allocreadiidae gen sp. (I) Gambusia marshi Los Hundidos Homalomentron sp. (I) Gambusia marshi Los Hundidos, Charcos Prietos, Poza Temporal hacia Playitas, Arroyo en La Estación, and Manantial de Churince Creptotrematina aguirrepequenoi (Jiménez-Guzmán, 1973) (I) [§] Astyanax mexicanus Río en Celemania Posthodiplostomum minimum (MacCallum, 1921) (M) Cyprinodon atrorus Poza temporal hacia playitas, and Poza Los Gatos Gambusia marshi Charcos prietos, and Río Mezquites Micropterus salmoides Camino hacia Playitas Microphallus opacus (Ward, 1894) (I) Cyprinodon atrorus Poza Los Gatos, and El Garabatal Monogenea Ancyrocephalinae gen. sp. (G) Herichthys Río en Celemania cyanoguttatus Herichthys minckleyi Charcos Prietos, Poza La Becerra, and Poza Tío Cándidio Salsuginus sp. (G) Cyprinodon atrorus Poza Playitas, and Manantial de Churince (continued)
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Table 2.1 (continued) Helminth taxon (site)/fish species Localities Cyprinodon atrorus x Laguna Intermedia bifasciatus Characithecium costariscensis (Price & Bussing, 1967) (G) Astyanax mexicanus Canal entre La Vega y el Venado, Anteojo San Juan, and Poza La Becerra Cestoda Schizocotyle acheilognathi (Yamaguti, 1934) (I) Cyprinella xanthicara Río Mezquites Gambusia marshi Canal San Juan Boquillas Nematoda Contracaecum sp. (BC) Herichthys minckleyi Santa Tecla, Río Mezquites, and Poza Tío Cándido Eustrongylides sp. (BC) Gambusia marshi Nadadores 1, and Nadadores at Huizachal Herichthys minckleyi Poza La Becerra Lepomis megalotis Río Mezquites Lucania interioris Camino hacia Playitas Procamallanus sp. (I) Ictalurus lupus Charcos prietos Procamallanus neocaballeroi (Caballero-Deloya, 1977) (I) Astyanax mexicanus Río en Celemania Rhabdochona sp. (I) Cyprinella xanthicara Río Mezquites, and Laguna intermedia Ictalurus lupus El Antiojo Lucania interioris Camino hacia Playitas Rhabdochona kidderi (Pearse, 1936) (I) [§] Gambusia marshi Canal entre La Vega y el Venado, and Charcos prietos Herichthys Río en Celemania cyanoguttatus Herichthys minckleyi Canal entre La Vega y el Venado, Charcos prietos, Río Mezquites, and Poza La Becerra Serpinema trispinosum (Leidy, 1852) (I) Lepomis megalotis Río Mezquites, and Manantial en Churince Micropterus salmoides Charcos prietos Spinitectus sp. (I) Micropterus salmoides Río Mezquites Spiroxys sp. (M) Astyanax mexicanus Río en Celemania, Camino hacia La Tecla, Poza La Becerra, and Poza Tío Cándido Cyprinella xanthicara Laguna Intermedia, and Santa Tecla Cyprinodon atrorus Poza Playitas, and Poza temporal hacia playitas Dionda episcopa Los Hundidos (continued)
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Table 2.1 (continued) Helminth taxon (site)/fish species Gambusia marshi Hemichromis bimaculatus Herichthys minckleyi
Localities Canal entre La Vega y el Venado, Poza Playitas, Poza temporal hacia playitas, and La Teclita Manantial en Churince, and Laguna Intermedia Charcos prietos, Río Mezquites, Santa Tecla, Poza La Becerra, and Camino hacia Playitas Río en Celemania, and Río Mezquites Camino hacia Playitas Río en Celemania
Lepomis megalotis Micropterus salmoides Notropis sp. Acanthocephala Atactorhynchus duranguensis Salgado-Maldonado, Aguilar-Aguilar and Cabañas-Carranza, 2005 (I) [§] Cyprinodon atrorus Poza Playitas, Poza temporal hacia playitas, Manantial en Churince, Laguna intermedia, and Poza Los Gatos Cyprinodon atrorus x Laguna intermedia bifasciatus Pomphorhynchus bulbocolli (Van Cleave, 1916) (I) Cyprinella lutrensis Puente San José de las Águilas Leptorhynchoides thecatus Linton, 1891 (I) Cyprinodon atrorus Poza Playitas Gambusia marshi Poza Playitas, Charcos prietos, and Poza temporal hacia playitas Herichthys minckleyi Charcos prietos Ictalurus lupus Charcos prietos Lepomis megalotis Río en Celemania, and Manantial en Churince Micropterus salmoides Charcos prietos, and Camino hacia Playitas BC body cavity, G gills, H heart, I intestine, IC intestinal caeca, IW intestinal wall, L liver, M mesentery, [§] host specialist species
the Nearctic component, and the faunal exchange is nule or very limited, occurring only with generalist parasite species. This has been described as a general pattern of the freshwater fish helminth parasites fauna in Mexico (Pérez-Ponce de León and Choudhury 2005). Three major results were found: (1) no endemic species of parasites, i.e., new species, were described as a result of the inventory work in the area, (2) no species of helminth was found to produce severe damage to the freshwater fish in the area, and (3) two species of helminths, i.e., Centrocestus formosanus and Schizocotyle acheilognathi, are co-invasive species that represent a potential threat to the future survival of the fish populations (see Aguilar-Aguilar et al. 2009; Pérez- Ponce de León et al. 2018). In addition, even though the inventory of the freshwater fish helminths in this geographic area is nearly complete, the parasite community structure patterns have been only characterized in one fish species, i.e., the Bolson pupfish Cyprinodon atrorus (Aguilar-Aguilar et al. 2015). In this study, we present a general description of the helminth parasite communities for 10 fish species occurring in the CCB protected area. Conclusions derived from this study could be
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i mmediately integrated to the current discussion about the processes that determine parasite community assemblages, which represent basic information for numerous ecological and evolutionary studies.
2.3 Helminth Parasite Community Structure 2.3.1 Methods of Study The helminth community structure of each fish species was analyzed at two hierarchical levels: infracommunity, a community of parasite infrapopulations in a single host (Bush et al. 1997), and component community, all infrapopulations of parasites associated to a subset of the host species. Infracommunities are herein expressed as the mean number of parasite species per host, the mean number of individual helminths, and the mean value of the Brillouin diversity index, used for fully censored communities. Numerical dominance was calculated using the Berger-Parker dominance index (Southwood 1978). Infracommunities were compared qualitatively using the Jaccard similarity index, and quantitatively using the Morisita-Horn index, as calculated in Magurran (1988). Component communities are herein described by using total number of individual parasites and total number of species. To determine whether sample size was sufficient to produce an accurate estimate of the pool of parasites, we performed a species richness sample-effort curve for those fish species with sample size higher than 12 individuals. The nonparametric species-richness estimators Chao 1 and Chao 2 were calculated following Colwell and Coddington (1994), and were used to estimate the number of missing species for each component community; the dominance-diversity relationship was calculated with Simpson’s index; also, we grouped helminth species as dominant (high prevalence and abundance) and rare (low prevalence and abundance) after an Olmstead-Tukey corner test of association (Berry et al. 2014).
2.3.2 Patterns of Community Structure The helminth parasite communities of ten fish species were analyzed. Five of these host species have a Nearctic affinity; the other five belong to Neotropical fish families, although the Jewel fish Hemichromis bimaculatus is actually an exotic cichlid, which has been introduced to Mexico as an ornamental species. Mean species richness at infracommunity level is low in all cases, with a single species in five host species, and with a maximum of 1.7 helminth species in the Longear sunfish Lepomis megalotis (Table 2.2). According to the values of the Brillouin and Berger- Parker indices, all the infracommunities analyzed were dominated by a single parasite species. With exception of Cyprinella lutrensis, which showed infracommunities
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Table 2.2 Attributes of the helminth parasite communities in fishes of Cuatro Ciénegas Infracommunities Host Cyprinella lutrensis Cyprinella xanthicara Dionda episcopa Lepomis megalotis Micropterus salmoides Astyanax mexicanus Cyprinodon atrorus Gambusia marshi Herichthys minckleyi
Hemichromis bimaculatus
0.33
1.319
0.05
–
Component Community (S) dmean J/M-H Schao1/Schao2 D/(1 − D) spD/(spr) 0.016 0.851/0.935 (2) 2/2 0.996/0.003 C. formosanus/ (1) 0.05 0.19/0.2 (4) 4/4.25 0.28/0.715 S. acheilognathi/ (1) – – (1) −/− −/− *
1.71
0.32
0.128 0.259/0.219 (5) 5.5/5.25 0.876/0.123 −/(2)
1.25
1.25
0.162 0.17/0.166
(6) 6/8.25
1.01
1.151
0.063 0.322/0.35
(5) 5/5
1.59
0.11
0.11
(7) 7/7.5
Smean HBmean 0.129 0.013
0.279 0.958 0.82
1.481
0.285 –
0.46/0.49
0.401/0.598 C. formosanus/ (3) 0.355/0.644 Spiroxys sp./(2) 0.332/0.668 A. duranguensis/ (4) 0.599/0.4 −/(5)
0.065 0.135/0.147 (10) 10.25/10.25 0.171 0.219/0.28 (7) 7/7 0.27/0.72
–
–
(1) −/−
−/−
R. kidderi, C. cichlasomae, and Spiroxys sp./(4) *
S species richness, HB Brillouin index, d Berger-Parker dominance index, J Jaccard index (qualitative similarity), M-H Morisita-Horn (cuantitative similarity), D Simpson (dominance), (1-D) Simpson (diversity), spD dominant species, spr number of rare species, * = not estimated because a single species was found
with an exceptionally high value of similarity in relation to their very low value of richness, the mean values of similarity among most of the infracommunities for remaining host species were low (Table 2.2). At the component community level, some intuitive patterns can be observed. Species richness of each component is considered low, however, those described for Nearctic hosts varied from 1 to a maximum of 6 helminth species, and were less species-rich than those exhibited by Neotropical fishes (excepting Hemichromis bimaculatus), which had a minimum of 5, reaching the maximum of 10 parasite species in the poecilid Gambusia marshi. The cumulative species curves and the values for the non-parametric species richness estimators show that no more than one missing species remains to be found for most of the component communities, excepting for the Black bass Micropterus salmoides, whose value for the Chao 2 index indicates that at least two additional species remain to be found (Table 2.2). Considering the helminth species richness of this centrarchid in other areas of North America (Hoffman 1999), it is not unexpected to find even more helminth species since the CCB is part of the natural
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distributional range of the species. Most of the analyzed component communities were moderately dominated; however, two fish hosts, Cyprinella lutrensis and Lepomis megalotis, exhibited very high dominance values (Table 2.2). Except for Minckley’s cichlid Herichthys minckleyi, which possess three dominant species, the dominance is exerted by one species, usually a trematode or a nematode. Remarkably, the dominant species for two component communities were host specialist helminth species, the nematode Rhabdochona kidderi, and the trematode Crassicutis cichlasomae in the cichlid Herichthys minckleyi, whereas the acanthocephalan Atactorhynchus duranguensis was the dominant species in the cyprinodontid Cyprinodon atrorus. Instead, the dominant species for three component communities was an exotic, anthropogenically introduced helminth species, the metacercariae of Centrocestus formosanus (in Cyprinella lutrensis and Micropterus salmoides), or the adult cestode Schizocotyle acheilognathi (in Cyprinella xanthicara) (Fig. 2.1).
Fig. 2.1 Microphotographs of some representative helminth species in freshwater fish of Cuatrociénegas. (a) Homalometron cf. pallidum, ventral view (Trematoda) ex Gambusia marshi; (b) Microphallus cf. opacus, ventral view (Trematoda) ex Gambusia marshi; (c) Schizocotyle acheilognathi, scolex (Cestoda) ex Gambusia marshi; and (d) Leptorhynchoides cf thecatus, anterior end showing the proboscis (Acanthocephala) ex Micropterus salmoides; (e) Pomphorhynchus bulbocolli, anterior end showing the bulb and proboscis (Acanthocephala), ex Cyprinella lutrensis
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Fig. 2.2 Similarity (based on the Jaccard index) between component communities analyzed. G.mar = Gambusia marshi; H.min = Herichthys minckleyi; C.atr = Cyprinodon atrorus; A.mex = Astyanax mexicanus; D.epi = Dionda episcopa; C.xan = Cyprinella xanthicara; L.mac = Lepomis macrochirus; M.sal = Micropterus salmoides; C.lut = Cyprinella lutrensis
Based on the shared helminth species, the dendrogram for qualitative similarity shows two main clusters: one conformed by the Nearctic components Dionda episcopa, Cyprinella xanthicara, Lepomis megalotis, and Micropterus salmoides, plus the Neotropical Astyanax mexicanus, and another one with the remaining Neotropical components (Gambusia marshi, Herichthys minckleyi, and Cyprinodon atrorus). A single branch, relatively isolated from the main clusters, contains the component of the Nearctic cyrpinid Cyprinella lutrensis (Fig. 2.2).
2.4 Discussion The fish fauna of the CCB is composed by a core of endemic species, which is complemented with other more widely distributed species with Nearctic and Neotropical affinities representing, in most of the cases, their southernmost or northern-most distribution range, respectively. Notwithstanding the distance with respect to core populations, each fish species keeps their characteristic helminth fauna. In this sense, helminth communities analyzed here are circumscribed to
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higher levels of monophyletic host taxa (family, genus, or species), and they are therefore considered to be part of the biogeographical core helminth fauna (Pérez- Ponce de León and Choudhury 2005), showing a host-specific component of adult worm species, which is the dominant set of species for the cichlid Herichthys minckleyi (whose specific worm species are the trematode Crassicutis cichlasomae and the nematode Rhabdochona kidderi), and for the pupfish Cyprinodon meeki (with the acanthocephalan Atactorhynchus duranguensis). The number of specific helminth species in this Neotropical fish component determines the low similarity among the helminth communities herein studied, which instead is given by sharing generalist larval stages such as Posthodiplostomum sp., Contracaecum sp., and Spiroxys sp.; in this study, these shared larval helminths may explain why Astyanax mexicanus is nested with Nearctic affinity hosts, although Astyanax spp. as a characiform is a typical Neotropical freshwater fish group. Most of the species found in the helminth communities described here infect their host by ingestion of the intermediate host. The three larval stages of digeneans infect their fish host through the free-living larval stage of cercariae. These cercariae are released from the first intermediate host (a snail), and infect fishes by penetrating the body and establishing as metacercariae in different parts of the body of the fish, which represents the second intermediate host. Only six out of the 25 species of helminths are larval forms that require another vertebrate to complete their life cycle, either a fish-eating bird in five of the six species, or a turtle in one case (the nematode Spiroxys sp.). The CCB possesses a wide variety of aquatic invertebrates, such as insects and crustaceans, which are largely consumed by cyprinids, cyprinodontiforms, poecilids, and centrarchids (Hernández et al. 2017). However, a presumably wide set of intermediate hosts is currently missing in the region, which has prevented the completion of the life cycles of several specific helminth taxa, which are absent in the CCB fishes. Furthermore, an ecological-phylogenetic component appears to be operating in structuring the helminth community of the introduced African jewelfish Hemichromis bimaculatus, which is only parasitized by the larvae of the nematode Spiroxys sp. The jewelfish, as well as Herichthys minckleyi and H. cyanoguttatus belong to the family Cichlidae; likewise, these species possess a different trophic spectrum in the ecosystem, and the only food item they share are some aquatic plants (Hernández et al. 2017), which do not constitute intermediate hosts for cichlid helminths. It is also possible that the lack of other helminth taxa such as monogeneans in Hemochromis bimaculatus, or other members of the core helminth fauna of cichlids such as Crassicutis spp., is the result of a phylogenetic component that prevents the establishment of these parasites in their hosts. The patterns of helminth community structure herein described are in concordance with general patterns that have been proposed in previous studies. Infracommunities and component communities of hosts with Nearctic affinities exhibit a low species richness, and are strongly dominated by one single parasite species with low host specificity; instead, helminth infracommunities and component communities of Neotropical hosts are in comparison relatively species-rich, and possess lower numerical dominance values; dominance in Neotropical fish is exerted by a set of specific helminth species. Furthermore, in our study, only fish
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belonging to the families Cyprinidae and Centrarchidae were analyzed. Species richness, dominance values, and the type of dominant species shown by Cyprinella lutrensis, C. xanthicara, and Dionda episcopa are similar to those described for other cyprinids in other areas of Mexico with a Nearctic influence, such as Campostoma ornatum, Codoma ornata, and Gila conspersa (Aguilar-Aguilar et al. 2010, 2016). As a general pattern, most of these helminth communities in northern Mexico are species-poor, usually with less than five helminth species per host species, and are conformed mainly by several species of platyhelminthes, nematodes of the genus Rhabdochona, and complemented by some larval stages of nematodes. Interestingly, the dominance in these communities is exerted by a generalist parasite species such as the metacercariae of Posthodiplostomum minimum, which was remarkably scarce in the CCB considering that it is widely distributed in fish across Mexico and other areas of North America (Hoffman 1999; Pérez-Ponce de León et al. 2007), or numerical dominance is exerted by co-introduced species such as the metacercariae of Centrocestus formosanus or the adult cestode Schizocotyle acheilognathi (Aguilar-Aguilar et al. 2009; Pérez-Ponce de León et al. 2018). In spite of their position within the Nearctic biogeographical zone, the CCB holds some Neotropical fish components that include members of the Cichlidae, Cyprinodontidae, Characidae, and Poeciliidae. In all cases, the CCB represents the northernmost limit of the distribution of these species, probably with the exception of some species of poeciliids that can reach farther north. Even though helminth infracommunities and component communities in Neotropical fish occurring in the area showed higher species richness values with respect to those in typically Nearctic hosts, this community attribute was usually lower than those described for truly Neotropical localities. This is the case of Minckley’s cichlid Herichthys minckleyi, whose helminth species richness is always lower than that described in other cichlids from central and southeastern Mexico (Salgado-Maldonado and Kennedy 1997; Aguilar-Aguilar 2005; Violante-González et al. 2008). As a general pattern, helminth communities of Mexican cichlids are strongly dominated by a core of larval and/or adult helminth species. Apparent exceptions are H. minckleyi in this study, and Vieja fenestrata from Los Tuxtlas in Veracruz (Aguilar-Aguilar 2005), which show a very low value for the Simpson dominance index; however, these component communities are actually dominated by almost 50% of the total of species, thus generating an effect of false increase in the diversity value. Previous studies (Aguilar-Aguilar 2005; Múgica and Caspeta-Mandujano 2010; Salgado-Maldonado et al. 2014a, 2016) describing helminth communities in characid hosts (Astyanax aeneus, A. mexicanus, and Bramocharax caballeroi) in Mexico which are Neotropical components, show species richness values varying from 3 (in communities across central Mexico) to 11 helminth species (in communities across southeastern Mexico). In this sense, the helminth community structure herein described for A. mexicanus shows an intermediate species richness value. The helminth fauna of characids in Mexico appears to be conformed by a wide core of adult helminth species, frequently specialist species, which vary among localities. In this case, the core helminth fauna of A. mexicanus is only determined by the m onogenean Characithecium costaricensis, the trematode Creptotrematina aguirrepequenoi,
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and the nematode Procamallanus neocaballeroi, which contrast with the only previous study on helminth community for this host species, conducted in a river located in a tropical latitude (Salgado-Maldonado et al. 2016). More studies are required to determine if the patterns and the processes that determine the helminth community structure of A. mexicanus are different from other characid fishes occurring in typically Neotropical environments. Pupfishes of the genus Cyprinodon are typical Neotropical fish, with several species inhabiting in northern Mexico and some regions across the United States. To date, descriptions of helminth communities for this fish genus in Mexico have been conducted in northern regions (Martínez-Aquino and Aguilar-Aguilar 2008; Aguilar-Aguilar et al. 2015). Helminth communities in these cyprinodontids, i.e., the Mezquital pupfish Cyprinodon meeki and the Bolson pupfish C. atrorus, exhibit moderate species richness, and are dominated by Atactorhynchus duranguensis, which represents a specialist acantocephalan species. These features must be corroborated for hosts analyzed from tropical localities where pup-fishes inhabit in order to establish valid patterns for helminth communities for cyprinodontids across their entire distributional area. Different members of the family Poeciliidae have been studied for helminth parasites in Mexico; nevertheless, there are relatively few studies of their helminth parasite communities. In these studies, community attributes such as species richness, diversity-dominance relationship, and intercommunity similarity are highly variable (Aguilar-Aguilar 2005; Salgado-Maldonado et al. 2014a, b). For this fish group, it seems that differences are due to the environmental characteristics of each locality. A remarkable feature of the helminth communities described in this study is the presence of the exotic co-invasive species Schizocotyle acheilognathi and Centrocestus formosanus. The presence of these two species in hosts with Nearctic affinities is interesting because of the fact that these hosts possess poor parasite communities, and in consequence they may offer empty niches for this highly invasive species. The Asian fish tapeworm S. acheilognathi is a very successful generalist species, which is currently found in a large number of fish species across Mexico (Pérez-Ponce de León et al. 2018). However, this species is not commonly found in freshwater fish of Cuatro Ciénegas (Aguilar-Aguilar et al. 2014), probably due to the continuous efforts to prevent or eradicate invasive fish species in this protected area, and this could represent a factor that prevents the successful establishment of this species. Likewise, occasional records of carps in the region have been documented (Lozano-Vilano and García-Ramírez 2014). In any case, the Asian fish tapeworm has been documented as a major cause of disease in fish farms because of the effect they produce in the intestine of their hosts (Scholz et al. 2012). Furthermore, the metacercariae of C. formosanus is, in comparison, more commonly found in CCB fish (Aguilar-Aguilar et al. 2014). The introduction of this digenean species to the system, which infects fish-eating birds as adults, was facilitated by the propagation of the first intermediate host in their life-cycle, the snail Melanoides tuberculata, which is frequently found in high abundance in water bodies of the CCB and neighboring areas (Contreras-Arquieta 1998; Dinger et al. 2005; Aguilar-Aguilar et al. 2009). The metacercariae of this species have been recorded as the cause of
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fish mortality in fish maintained for aquaculture purposes (Amaya-Huerta and Almeyda-Artigas 1994; Arguedas et al. 2010). Because of the latter arguments, the presence of both coinvasive species, C. formosanus and S. acheilognathi, could represent a risk for the conservation of fish populations in the Cuatro Ciénegas Basin. Acknowledgments The authors would like to thank Juan Carlos Ibarra Flores of CONANP, Mexico, for permission to sample in some particular areas of Cuatro Ciénegas during the 2008 samplings. We also thank Andres Martínez, Rodolfo Pérez, Omar Lagunas, Alma Islas, Javier Alcantar, Daniel Sepúlveda, Eduardo Villalobos, Christian Lambarri, and Martha Barluenga for their help during fieldwork which is greatly appreciated. The final support and facilities provided by Dra. Valeria Souza to conduct samplings during 2011 within the research project financed by WWF-Fundación Carlos Slim Alliance is greatly appreciated. Fishes were obtained under the collecting permit Pesca de Fomento No. DGOPA.00889.280211.-0349 issued by SAGARPA to H. Espinosa P.
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Múgica E, Caspeta-Mandujano JM (2010) Helmintos parásitos de Astyanax aeneus del Río Cuautla Inventio 12:57–60 Navarro P, Lluch J, Font E (2005) The component helminth community in six sympatric species of Ardeidae. J Parasitol 91:775–779 Neves LR, Pereira FB, Tavares-Dias M et al (2013) Seasonal influence on the parasite fauna of a wild population of Astronotus ocellatus (Perciformes: Cichlidae) from the Brazilian Amazon. J Parasitol 99:718–721 Neves LR, Braga ECR, Tavares-Dias M (2015) Diversity of parasites in Curimata incompta (Curimatidae), a host from Amazon River system in Brazil. J Parasitic Dis 40:1–15 Pantoja WMF, Flores L, Tavares-Días M (2015) Parasites component community in wild population of Pterophyllum scalare Schultze, 1823 and Mesonauta acora Castelnau, 1855, cichlids from the Brazilian Amazon. J App Ichth 31:1043–1048 Pérez-Ponce de León G (2014) Los helmintos parásitos de peces como bioindicadores de la salud de los ecosistemas. In: González Zuarth CA, Vallarino A, Pérez Jiménez JC, Low Pfeng AM (eds) Bioindicadores: Guardianes de nuestro futuro ambiental. El Colegio de la Frontera Sur e Instituto Nacional de Ecología (ECOSUR) y Cambio Climático (INEEC), México, pp 253–272 Pérez-Ponce de León G, Choudhury A (2005) Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. J Biogeogr 32:645–659 Pérez-Ponce de León G, Garcia-Prieto L, León-Régannon V, Choudhury A (2000) Helminth communities of native and introduced fishes in Lake Pátzcuaro, Michoacán, México. J Fish Biol 57:303–325 Pérez-Ponce de León G, García-Prieto L, Mendoza-Garfias B (2007) Trematode parasites (Platy helminthes) of wildlife vertebrates in Mexico. Zootaxa 1534:1–247 Pérez-Ponce de León G, Choudhury A (2010) Parasite inventories and DNA-based taxonomy: lessons from helminths of freshwater fishes in a megadiverse country. J. Parasitol 96:236–244 Pérez-Ponce de León G, Lagunas-Calvo O, García-Prieto L, Briosio-Aguilar R, Aguilar- Aguilar R (2018) Update on the distribution of the co-invasive Schyzocotyle acheilognathi (= Bothriocephalus acheilognathi), the Asian fish tapeworm, in freshwater fishes of Mexico J Helminthol 92:279–290 Poulin R (1997) Species richness of parasite assemblages: evolution and patterns. Ann Rev Ecol Syst 28:341–358 Poulin R (1998) Evolutionary ecology of parasites: from individuals to communities. Chapman & Hall, London. 212 pp Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Books, Washington, D. C.. 216 pp Razo-Mendivil U, Vázquez-Domínguez E, Rosas-Valdez R, Pérez-Ponce de León G, Nadler SA (2010) Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of middle-American cichlids. Int J Parasitol 40:471–486 Rojas EP, Pérez-Ponce de León G, García-Prieto L (1997) Helminth community structure of some freshwater fishes from Patzcuaro, Michoacan, Mexico. Trop Ecol 38:129–131 Salgado-Maldonado G, Kennedy CR (1997) Richness and similarity of helminth communities in the tropical cichlid fish Cichlasoma urophthalmus from the Yucatan Peninsula, Mexico. Parasitology 114:581–590 Salgado-Maldonado G, Moravec F, Cabañas-Carranza G, Aguilar-Aguilar R, Sánchez-Nava P, Báez-Valé R, Scholz T (2004) Helminth parasites of the tropical gar, Atractosteus tropicus Gill, from Tabasco, Mexico. J Parasitol 90:260–265 Salgado-Maldonado G, Caspeta-Mandujano JM, Ramírez-Martínez C, Lozano-Vilano L, García- Ramírez ME, Mendoza-Franco EF (2014a) Helmintos parásitos de los peces del Río Lacantún en la Reserva de la Biósfera Montes Azules, Chiapas. Universidad Autónoma de Nuevo León, Nuevo León. 147 pp Salgado-Maldonado G, Novelo-Turcotte MT, Vázquez G, Caspeta-Mandujano JM, Quiroz- Martínez B, Favila M (2014b) The communities of helminth parasites of Heterandria
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bimaculata (Teleostei: Poeciliidae) from the upper Río La Antigua basin, east-central Mexico show a predictable structure. Parasitology 141:970–980 Salgado-Maldonado G, Novelo-Turcotte MT, Caspeta-Mandujano JM, Vazquez-Hurtado G, Quiroz-Martínez B, Mercado-Silva N, Favila M (2016) Host specificity and the structure of helminth parasite communities of fishes in a Neotropical river in Mexico. Parasite 23:61 Scholz T, Choudhury A (2014) Parasites of freshwater fishes in North America: why so neglected? J Parasitol 100:26–45 Scholz T, Kuchta R, Williams C (2012) Bothriocephalus acheilognathi. In: Woo PT, Buchmann K (eds) Fish parasites: pathobiology and protection. CABI, Wallingford, pp 282–297 Southwood TR (1978) Ecological methods, 2nd edn. Chapman & Hall, London Stein BA, Kutner LS, Adams JS (2000) Precious heritage: the status of biodiversity in the United States. Oxford University Press, Oxford Tavares-Dias M (2017) Community of protozoans and metazoans parasitizing Auchenipterus nuchalis (Auchenipteridae), a catfish from the Brazilian Amazon. Acta Scient Biol Sci 39:123–128 Tavares-Dias M, Oliveira MSB, Goncalves RA et al (2014) Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitol 59:158–164 Violante-González J, Aguirre-Macedo ML, Rojas-Herrera A (2008) Comunidad de parásitos metazoarios de la charra Cichlasoma trimaculatum en la laguna de Tres Palos, Guerrero, México. Rev Mex Biodivers 79:405–412
Chapter 3
Abundance and Diversity of the Soil Microarthropod Fauna from the Cuatro Ciénegas Basin Margarita Ojeda and Jaime Gasca-Pineda
Abstract Soil is one of the less studied resources of terrestrial ecosystems, both in terms of its biodiversity and internal processes. In particular, microarthropods of desert ecosystems have been poorly studied worldwide, and probably less than 10% of the total soil species have been described. Nevertheless, microarthropods are responsible for one of the most important environmental functions: the decomposition of organic matter. In this chapter, we present the results of the first survey of soil microarthropod communities from the CCB. The study was conducted in 2015– 2016 to identify the microarthropods’ diversity in its components of richness and abundance. We collected 6721 organisms of 6 classes, 26 orders, and 60 families. Acari was the most abundant and diverse group and is dominated by Prostigmata (20 families) and Oribatida (16 families). Hexapoda is represented by Collembola, Coleoptera, Hemiptera, Hymenoptera, and Psocoptera. Differences in mite assemblages are attributable to the type of vegetation in the different sites of the CCB. The site’s taxonomic diversity is associated with habitat heterogeneity. The high productivity micro-habitats could produce high levels of biomass and not necessarily more diverse communities. We observed broad similarities in microarthropod composition at familial level among arid-semiarid ecosystems elsewhere in the world. Knowledge of soil microarthropod community will be helpful to understand the network of interactions and the flow of nutrients and energy within this desert ecosystem; all these are crucial elements to assess the health of the soil and to establish appropriate strategies for it use, management, and conservation. Keywords Soil mites · Edaphic · Organic matter · Decomposition · Desert
M. Ojeda (*) Colección Nacional de Ácaros, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico J. Gasca-Pineda Departamento de Biología de la Conservación, Centro de Investigación Científica y, Educación Superior de Ensenada, Ensenada, Baja California, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_3
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3.1 Introduction Soil is a complex ecological system where important processes occur, such as the decomposition of organic matter and the recycling, storage, and release of nutrients. Many of these ecosystem processes are mediated by the biota that inhabit in it, which is composed of the microflora (bacteria, algae, and fungi) and the complex fauna formed by protozoa, nematodes, annelids, and arthropods (Wallwork 1970; Kaczmarek et al. 1995; Powers et al. 1998). The wide variety in body size of the edaphic fauna determines the different levels of participation in the ecological processes that take place in the soil: (1) earthworms, termites, and ants are the ecosystem engineers, since they alter the physical structure of the ecosystem and influence the flow of energy and nutrients; (2) microarthropods (mites, Collembola, and other small insects) are the leaf litter transformers, since they fragment it and make it more available for microorganisms (bacteria and fungi); and (3) the decomposers are bacteria, fungi, and algae that release the necessary nutrients for the plants to develop (Luxton 1972; Dindal 1990; Kampichler and Bruckner 2009). The composition of soil microarthropod communities in arid ecosystems varies considerably because soil temperature, moisture, and texture, as well as the vegetation type, are important factors affecting abundance, species composition, and spatial distribution (Santos et al. 1978; Whitford 1989, 1996; Cepeda-Pizarro and Whitford 1989a, 1989b; Silva et al. 1989). The soils of arid and semi-arid regions have a low density of microarthropods in comparison with mesic ecosystems and these communities are adapted to the extreme climatic characteristics of this particular environment. The biota present in these habitats, due to their predatory and fungivorous habits, act as regulators of the decomposition, crushing of plant matter, vertical transport, and spore dissemination, increasing through these actions the microbial activity (Whitford and Parker 1989; André et al. 2002). Of the terrestrial ecosystems, soil comprises one of the least studied resources (Coleman et al. 2004), both, regarding its biodiversity and its internal processes. Only about 10% of microarthropods have been examined and probably only 10% of the species described (André et al. 2002), and, as a result, the importance of the biota in the soil is commonly underestimated (Coleman et al. 2004), regardless of the services and the key role these provide to humanity and the rest of the edaphic biota (Petersen and Luxton 1982). The knowledge of the diversity and abundance of the species present in the soils are an indicator of the quality and health of the edaphic environment, since these organisms are sensitive to natural and anthropic disturbances (Socarrás 2013). The microarthropod community in desert environments in Mexico has hardly been studied (Estrada et al. 1988; Villarreal-Rosas et al. 2014; Rodríguez-Zaragoza et al. 2008), and especially those from the Chihuahuan Desert (CD) are unknown. The aim of this study was to identify and quantify soil microarthropod communities in the Cuatro Ciénegas Basin (CCB).
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3.2 Materials and Methods 3.2.1 Study Area The CCB is a gypsum-rich environment located in northern Mexico with a unique geological and biological history (Moreno-Letelier et al. 2012). In this basin, groundwater rises to the surface by dissolution of the limestone, forming a great amount of pools surrounded by saline soils rich in calcium sulfates and extremely poor in nutrients. The soil has high alkalinity produced by elevated concentrations of ions, which is a general pattern in desert soils (Titus et al. 2002). The high pH decreases phosphorus (P) availability, which is very scarce in these soils (Elser et al. 2005; Perroni et al. 2014). Vegetation cover and water availability in these soils depend on the degree of proximity to the aquatic systems and rainfall. The vegetation in the CCB is characterized as gypsophile, halophile grasslands, aquatic and subaquatic, and desert shrubs (Challenger 1998). The soil and vegetation sampled in the study are representative of the extensive arid zone occurring in the northern part of Mexico and the southwestern United States, known as CD. Many investigations in the CCB conclude that the particular characteristics of this site and the isolation of the valley have resulted in a high microbial diversity and a high degree of endemism (Souza et al. 2006; Escalante et al. 2008; Cerritos et al. 2011). However, no such studies have addressed the diversity of soil microarthropods.
3.2.2 Sampling Sampling sites were selected at six different locations within the CCB: Churince (with five sites related to the vegetation), Pozas Rojas, Pozas Azules (= Pozas Domos), Poza la Becerra, Ejido El Oso, and CBTA22. For the Churince site, the five main vegetation types established were as follows: (1) shrubland, Mezquital (Prosopis glandulosa); (2) wet grassland, Tular (Sporobolus/Distichlis); (3) desert scrub, Larrea (Larrea tridentata/Fouquieria), (4) desert scrub, Sotol (Dasylirion wheeleri); and (5) Peladero (Sporobolus) surrounded by areas of gypsum desert dunes with no vegetation cover. The sampling was spread between these sites with different vegetation (Fig. 3.1). In order to identify and quantify the edaphic microfauna of the CCB, soil samples were carried out during 2015 and 2016. Soil portions of 250–300 g with a depth of 5–10 cm were taken at each of the different habitats present in the CCB. Each sample was placed in sealed polyethylene bags, individualized, and labeled for transport to the laboratory. Studies involving many different categories of small arthropods have shown that no single extraction procedure is best suited or equally efficient for all groups (Price 1973). Considering this, each soil sample was subdivided to be processed by two
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Fig. 3.1 Churince site: The five vegetation associations established: (a) the shrubland, Mezquital (Prosopis glandulosa); (b) wet grassland, Tular (Sporobolus/Distichlis); (c) desert scrub, Larrea (Larrea tridentata/Fouquieria); (d) desert scrub, Sotol (Dasylirion wheeleri); and, (e) Peladero (Sporobolus) surrounded by areas of gypsum desert dunes with no vegetation cover
methods: firstly, by using modified Berlese-Tullgren funnels for 3 days without heat, followed by a period of 3–5 days with a heat source (standard light 40 W). Microarthropods were collected from the funnels in small tubes with alcohol 80% for preservation and posterior counting and identification; secondly, by a modified flotation technique (Kethley 1991), which uses water and drops of liquid soap to wash and float microarthropods from the bulk soil sample. An advantage of this technique is the recovery of a sufficiently large number of individuals of microarthropod species to ensure representation of all inactive stages.
3.2.3 Taxonomic Determination Due to the size of some of the organisms of various groups such as mites, springtails, and diplurans, these were macerated in lactic acid and mounted in Höyer’s fluid or CMC-10 medium on glass slides for initial identification and storage. Mites were identified with specialized keys (Hughes 1961; Balogh 1972; Balogh and Balogh 1988; Kethley 1990; Krantz and Walter 2009), to family and genus. As for insects and other arthropods, identification was carried out to family level using Dindal (1990) and Palacios-Vargas et al. (2014). Feeding groups were assigned to each Acari family based on the feeding behavior reported in the literature (Walter 1988; Walter et al. 1988; Neher et al. 2009; Walter and Proctor 2013): (1) predators (consuming nematodes and other microarthropods), (2) microphytophages (fungi and algae eaters), and (3) saprophages (Luxton 1972; Walter and Proctor 2013).
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3.2.4 Data Analysis The diversity of sites (i.e., alpha diversity) was evaluated using Shannon diversity index. The equitability (interpreted here as dominance) was estimated using Hill’s ratio from the previous value estimated from the Shannon diversity index. Both estimates were calculated using the package vegan 2.5 (Oksanen et al. 2018) implemented in R 3.5.1 (R Core Team 2018). The differences in composition among sites were evaluated using the relative abundance of taxa per site; graphics were constructed using the package ggplot2 (Wickham 2016) in R. We assessed beta-diversity by constructing a Sorensen similarity plot using the package adespatial 0.2 (Dray et al. 2018).
3.3 Results 3.3.1 Abundance A total of 6721 specimens were collected belonging to the four Arthropoda subphyla, 6 classes, 26 orders, and 60 families (Table 3.1; Fig. 3.2). Among Arachnida, mites constituted the most abundant and diverse group among all microarthropods (68%). Within the Acari, Trombidiformes had the highest richness with the Prostigmata (20 families), followed by Sarcoptiformes, especially Oribatida with 18 families, the latter are the most abundant group in terms of the number of organisms collected from all the sampling sites. Abundance of Mesostigmata (nine families), Opilioacarida, and Astigmata was low. Other orders of arachnids present in the soil were pseudoscorpions, solifuges, and spiders (Figs. 3.3 and 3.4) with very low abundances. Among the hexapods, insects were the most abundant, represented by 11 orders, the most diverse were Coleoptera (five families), Diptera (four families), Hymenoptera (two families), and Psocoptera (Fig. 3.5). Even though the springtails (Collembola: Entognatha) were represented by four families, the number of organisms per sample was very low compared to the mites. The Myriapoda were poorly represented by diplopods of the family Polyxenidae, similar to the crustaceans represented by the terrestrial isopod genus Armadillidium, both contributed with less than 1% of the total number of organisms collected. Major differences in the abundance of the total microarthropod and mite assemblages were recorded between the different vegetation types of the CCB. These differences can be explained by the abiotic and biotic factors that affect this microhabitat. Among the former, the availability of water in this ecosystem is a driving force for soil organisms, some of which are active at a particular time when rainfall is present (Whitford 1989). We must also consider that there are differences in species resistance to desiccation, and that there is an acceleration in reproduction when water is available, and the threshold for entry into a cryptobiotic state.
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Table 3.1 Soil microarthropods of the Cuatro Ciénegas Basin (Classification follows Brusca et al. 2016; Krantz and Walter 2009; Balogh 1972; Subías 2004) Superorder
Parasitiformes
Order Araneae Palpigradi Solifugae Pseudoscorpiones Opilioacarida Mesostigmata
Suborder
Family
Genus
Opilioacaridae Macrochelidae Uropodidae Ameroseiidae Laelapidae
Neoacarus sp. Geholaspis sp.
Trematuridae Parasitidae Ascidae
Acariformes
Trombidiformes
Prostigmata
Rhodacaridae Oplitidae Alycidae Adamystidae Siteroptidae Barbutiidae Bdellidae Caligonellidae Ereynethidae Tarsochelidae Stigmaeidae Cheyletidae Tydeidae Oehserchestidae Cunaxidae
Nanorchestidae Lordalycidae Rhagidiidae Paratydeidae Microtrombidiidae Camerobiidae Caeculidae
Setitympanum sp. Androlaelaps sp. Gaeolaelaps sp. Trichouropoda sp. Pergamasellus sp. Asca sp. Lasioseius sp. Orthadenella sp. Protogamasellus sp. Gamasellodes sp. Rhodacarus sp. Oplitis sp. Adamystis sp.
Neognatus sp.
Hemicheyletia sp. Oehserchestes sp. Cunaxa sp Cunaxoides sp Neocunaxoides sp
Neophyllobius sp Caeculus sp (continued)
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Table 3.1 (continued) Superorder
Order
Suborder
Acariformes
Sarcoptiformes
Oribatida
Family Smaridiidae Stigmaeidae Teneriffidae Alicorhagiidae Eupodidae Acaronychidae Aphelacaridae Amerobelbidae Austrachipetridae Cepheidae Nodocepheidae Cosmochthoniidae Cymbaeremaeidae Epilohmaniidae Haplochthoniidae Haplozetidae Hypochthoniidae Trhypochthoniidae Nothridae Teratoppiidae Damaeidae Oppiidae
Galumnidae Licnodamaeidae Malaconothridae Microzetidae Mochlozetidae Suctobelbidae Oribatulidae
Oripodidae
Genus Smaris sp
Acaronychus sp Aphelacarus sp Amerobelba sp Allozetes sp Sphodrocepheus sp Nemacepheus sp Cosmochthonius sp Phyllozetes sp Scapheraemeus sp Epilohmania sp Haplochthonius sp Rostrozetes sp Peloribates sp Phyllozetes sp Trhrypochthonius sp Novonothrus sp Belba sp Epidamaeus sp Brachioppia sp Striatoppia sp Oxyoppia sp Ramuloppia sp Galumna sp Heterogalumna sp Licnodamaeus sp Malaconothrus sp Kaszabobates sp Podoribates sp Rhynchobelba sp Oribatula sp Zygoribatula sp Phauloppia sp Benoibates sp Calobates sp Campbellobates sp Oripoda sp (continued)
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Table 3.1 (continued) Superorder
Order
Suborder
Sarcoptiformes
Astigmata
Family Phthiracaridae Passalozetidae Tectocepheidae Acaridae
Genus Rhysotritia sp Passalozetes sp Tectocepheus sp Acarus sp Aleuroglyphus sp Caloglyphus sp Rhizoglyphus sp Tyrophagus sp
Arthropoda Unclassified
Symphyla
Class
Malacostraca Abundance 1.00
Insecta
0.75 0.50
Entognatha
0.25 0.00
Diplopoda
Chilopoda
Tular
Sotol
PozasRojas
Pozadomos
PozaLaBecerra
PozaChurince
Peladero
Mezquital
Manantial
Larrea
EjidoELOso
CBTA22
Arachnida
Fig. 3.2 Heatmap of relative OTU abundance for each group studied in the CCB soil
The abundance and diversity of soil microarthropods and their importance in ecosystem processes are closely related to the physical structure of the soil as it affects the ability of various species to move through it (Elliot et al. 1980). Soil porosity and especially pore size are critical factors for the microarthropods, which vary greatly in size and cannot move through spaces smaller than the diameter of their bodies. Some of the largest Mesostigmata mites may be ten times larger than the smallest Prostigmata and Oribatida and hence are restricted to only the largest pore spaces. The varying pore sizes in the soil provide refugia from the larger
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Abundance
Tular
Sotol
PozasRojas
Pozadomos
PozaLaBecerra
Peladero
PozaChurince
Mezquital
Larrea
Manantial
EjidoELOso
0.5 0.4 0.3 0.2 0.1 0.0
CBTA22
Order
Arthropoda Zygentoma Unclassified Trombidiformes Thysanoptera Symplyhpleona Symphypleona Solifugae Sarcoptiformes Pterygota_Unclassified Psocoptera Pseudoscorpionida Polyxenida Poduromorpha Palpigradi Orthoptera Odonata Mesostigmata Lepidoptera Isoptera Isopoda Hymenoptera Hemiptera Entomobryomorpha Diptera Diplura Decapoda Collembola_Unclassified Coleoptera Arthropleona Araneae Acari_Unclassified
Fig. 3.3 Heatmap showing the relative abundance of all soil Arthropoda orders that were collected on the different CCB sites
p redators for smaller microbial feeding forms. Pore size distribution thus affects the relative abundance and species composition of the microarthropod fauna. Some groups with extremely small body size may play an important role in decomposition and/or mineralization processes in soils due to their access to the small pore spaces and because they are probably active in dry soils (André et al. 1994). Plant community structure of the region is influenced by spatial and temporal variability of abiotic (e.g., soil physical characteristics, nutrients, organic matter, moisture, water holding capacity) and biotic (fauna, flora, microbes) components of the ecosystem. This variability has been related to moisture and temperature patterns and the availability of soil nitrogen (Whitford 1989; Fisher et al. 1988). Several studies have suggested that desert microarthropods experience relatively rapid changes in patterns of distribution and abundance in relation to the variability in available N, moisture, and temperature and that microhabitat differences are important in determining the density of soil mites in arid ecosystems (Steinberger et al. 1984; Cepeda-Pizarro and Whitford 1989a, b; Franco et al. 1979). Surface litter and organic matter content in areas with vegetation are positively correlated with abundance and diversity of microarthropods in all the sampled sites along the CCB.
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M. Ojeda and J. Gasca-Pineda Arachnida Trombidiformes
Solifugae
Sarcoptiformes
Abundance 0.6
Pseudoscorpionida
Order
0.4 Palpigradi
0.2 0.0
Mesostigmata
Araneae
Tular
Sotol
PozasRojas
Pozadomos
PozaLaBecerra
Peladero
PozaChurince
Mezquital
Larrea
Manantial
CBTA22
EjidoELOso
Acari_Unclassified
Fig. 3.4 Heatmap depicting abundance of the top seven Arachnida found in the CCB soils
We observed broad similarities in microarthropod composition at familial level in arid-semiarid ecosystems in the Sonoran and Chihuahuan Desert in the United States (Santos et al. 1978; Wallwork et al. 1985) and other deserts around the world, such as in Australia (Noble et al. 1996) and Israel (Steinberger and Wallwork 1985; Steinberger et al. 1988; Steinberger 1990; Wasserstrom et al. 2016).
3.3.2 Diversity Sixty-five taxa of arthropods (mites, insects, myriapods, and crustacean) were found in the soil samples from the CCB. Several of the taxa were found in single samples and/or at single sites and others were often represented by few individuals. Diversity was measured using the number of OTUs and the Shannon and Sorensen index. The analysis reveals that the sites are different among themselves when we compared diversity (Table 3.2). We observed the highest diversity in Peladero, while the lowest was in Poza Churince (Fig. 3.6a). It is worth noting that Peladero was the locality with the lowest number of specimens. Moreover, the
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Insecta Zygentoma Unclassified Thysanoptera Pterygota_Unclassified Psocoptera
Abundance
Order
Orthoptera
0.6
Odonata
0.4
Lepidoptera
0.2 0.0
isoptera Hymenoptera Hemiptera Diptera
Tular
Sotol
PozasRojas
PozaLaBecerra
Pozadomos
Peladero
PozaChurince
Mezquital
Larrea
Manantial
EjidoELOso
CBTA22
Coleoptera
Fig. 3.5 Heatmap showing the realtive abundance of Insects that were collected on the different CCB sites
Table 3.2 Alpha diversity estimates per site Site CBTA22 Ejido El Oso Larrea Manantial Mezquital Peladero Poza Churince Poza domos Poza la Becerra Pozas Rojas Sotol Tular
N 31 20 69 29 78 62 3 11 14 55 77 68
H 3.054049 2.684712 3.374284 2.888343 3.569842 3.821859 0.898137 2.252354 2.511595 3.347462 3.661563 3.587342
N OTU counts, H Shannon diversity index, E Hill’s evenness number
E 0.6839034 0.7326993 0.423237 0.6194315 0.4552688 0.7369205 0.8183417 0.8645544 0.8803263 0.5169178 0.5054821 0.5314397
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M. Ojeda and J. Gasca-Pineda
a
4
Shannon diversity index
3
2
1
PozasRojas
PozaLaBecerra
PozasRojas
Tular
PozaLaBecerra
Pozadomos
Sotol
Pozadomos
PozaChurince
Peladero
PozaChurince
Mezquital
Manantial
Larrea
EjidoELOso
CBTA22
0
b
Shannon evenness number
0.75
0.50
0.25
Tular
Sotol
Peladero
Mezquital
Manantial
Larrea
EjidoELOso
CBTA22
0.00
Fig. 3.6 (a) Shannon diversity index in each site of the CCB; (b) Shannon evenness index in each site of the CCB
h ighest dominance was found in the Larrea site (Fig. 3.6b), while Poza La Becerra had the lowest. These results lead to two notable points: first, the site taxonomic diversity is associated with habitat heterogeneity. In the case of Peladero, the combination of areas with dunes and little vegetation cover lead to the generation of different micro-habitats that support more diverse communities of microarthropods.
3 Abundance and Diversity of the Soil Microarthropod Fauna from the Cuatro…
0
0.1
0.2
0.29
0.39
0.49
0.59
0.68
0.78
0.88
41
0.9
Fig. 3.7 Dissimilarity of soil microarthropods across all sites from the CCB. Beta diversity was estimating using the Sorensen index, and represents dissimilarity of one community to another, with red indicating low dissimilarity and white indicating high dissimilarity (a value of 1 indicates no share species)
Second, the high productivity micro-habitats could produce high levels of biomass; however, this did not necessarily lead to more diverse communities. The Sorensen dissimilarity analysis displayed that in general, Poza La Becerra and Poza Churince were the localities with the most different taxonomic composition (Figs. 3.7 and 3.8). We expected this result since these sites presented the most different micro-habitats, a combination of vegetation cover and mud-like soil, restricting diversity but harboring divergent taxonomic groups. Members of the phylum Arthropoda occur in every soil type throughout the world, from the sandy soils of hot deserts to the richest litter soil of tropical and temperate forests. The phylum has an ubiquitous distribution and its diversity is immense. Crustacea, Myriapoda, Hexapoda (Insecta), and Arachnida often make an appreciable contribution to the total biomass and metabolism of the community (Wallwork 1976) (Fig. 3.9). Crustacea The majority of crustaceans are aquatic and the isopods are one of the few groups of which some members now live on land. Terrestrial isopods or “woodlice” play an important role in the decomposition of plant material through
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Fig. 3.8 Similarity dendrogram (Sorensen’s similarity index) among the CCB sites
echanical and chemical means and by enhancing the activity of microbes. The m desert species are usually nocturnal, spending the day in an underground burrow and emerging at night. Many species can roll themselves into a ball, a behavior used in defense that also conserves moisture, an important factor in the lives of these organisms. Species inhabiting the desert as Armadillidium sp. have developed mechanisms that allow them to resist desiccation and to survive in dry habitats. Isopods are important saprophages; they feed on a wide variety of organic matter, dead wood, or carrion. Most of them can be seen easily, however, they were poorly represented in the samples from the CCB. Myriapoda Members of this group (Chilopoda, Diplopoda, Pauropoda, and Symphyla) are associated with the soil and have a wide range of distribution. They are most abundant in moist forests, where they fulfill an important role in breaking down decaying plant material, although a few live in grasslands, semiarid habitats, or even deserts (Dindal 1990). Except for the pauropods, the other three classes of myriapods were represented in the CCB soils samples. The majority are detritivorous with the exception of centipedes, which are chiefly nocturnal predators. Most of the millipedes are detritivores and feed on decomposing vegetation, feces, or organic matter mixed with soil. Symphylans are the smallest among the myriapods. Particularly, millipedes in the order Polyxenida (flat-backs) graze on algae and are an important group of saprophages. They are not efficient burrowers and are forced to use existing spaces between fallen leaves or beneath decaying wood to live
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Fig. 3.9 Different arthropods extracted from the soil from CCB. (Photographs by M. Ojeda)
(Dindal 1990; Wallwork 1976). However, in the CCB they were observed especially in soils covered with vegetation as the Prosopis shrubland (Mezquital), where they were abundant. Hexapoda (Apterygota-Entognatha) Collembolans, commonly known as “springtails,” are extremely common and ubiquitous in soil; they are found in diverse habitats from tundras to agriculture fields, and moisture is the most important abiotic factor of the soil that influences their populations. They play important roles in the decomposition of organic materials, the cycling of nutrients, and the formation of the soil microstructure. Like most soil invertebrates, they make a relevant contribution to the food web and the health of the soil community. The collembolans in the CCB were represented by several families: Hypogastruridae, Tomoceridae, and Sminthuridae. Some species are adapted to environments with low organic matter and water stress conditions such as the CCB soils. In general, the collembolan fauna shows a vertical stratification of species, where the forms with large body size occur mainly in the upper layers of leaf litter, whereas small-sized forms are concentrated at greater depths. These showed morphological differences that evidence the different microhabitats they are adapted to. Mostly, the species in the CCB show smaller sizes and may be living deeper, characteristics that can explain the low abundance found in the samples. Springtails are
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saprophages, and their food includes decomposing plant material and carrion, among others, but it is the fungi, bacteria, and algae associated with these substrates which are an important part of the diet in many species. Hexapoda (Pterygota) Soil plays an important part in the lives of many insects. For some, it is a permanent home, from egg to adult; in others, it is just a temporary refuge or shelter. There are many insect groups that depend on the soil for only a part of their life cycle, such as a number of Diptera, Lepidoptera, and Coleoptera (Dindal 1990; Wallwork 1976). For the Hymenoptera, especially ants, a group well represented in many parts of the world, hot deserts are not the exception. They are common in the CCB, they produce subterranean nests, and feed on seeds which they collect and store in these underground nests (a full chapter in this book includes the ants). Coleoptera Some families of beetles are usual inhabitants of the soil; in the CCB they were the most abundant group of insects, we found them at all the sites sampled, although in low densities compared to arachnids, specifically mites. Lepidoptera and Diptera Some representatives of these orders were found in the soil samples of the different sites of the CCB. Lepidoptera occurred mainly as larval instars. Arachnida Of the 11 orders comprising this class of arthropods, 5 are represented in the CCB soil, and just 1 is sufficiently diverse and widely distributed: the Acari (Fig. 3.10). The remaining four are rare or scarce: the false scorpions (Pseudoscorpiones), spiders (Araneae, see chapter 3 in this volume), Solifugae and Palpigradi. These last three groups are almost exclusively predators, whereas mites (Acari) are a very diverse group which includes predators, phytophages, saprophages, and parasites. Acari Mites together with collembolans make a major contribution to the total biomass and diversity in a wide range of soil types. Moisture plays a key role on the distribution patterns of these arachnids (MacKay et al. 1986, 1987). Vertical stratification is related to their body size and to their ability to resist desiccation. The larger-sized species occur mainly in the upper litter soil layers and include groups such as the Oribatida (moss-mites or Cryptostigmata) and Mesostigmata, although other smaller mites such as Prostigmata and Astigmata, as well as some species of oribatids can be found deeper in the soil. Oribatids are saprophages in a broad sense, although a distinction between species can be made as some are macrophytic feeders (feed on decomposing litter) and some microphytic feeding on fungi and bacteria (Luxton 1981). They were represented by 18 families; the most abundant were Aphelacaridae, Cosmochthoniidae, Nothridae, Oppiidae, Hypochthoniidae, and Oribatulidae (Fig. 3.10).
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Fig. 3.10 Some of the mites found on the soil samples from CCB. (a) Opilioacarida; (b–d) Prostigmatid mites; (e–h) Mesostigmata; (i) Astigmata and (j–n) Oribatid mites. (Photographs by M. Ojeda)
Prostigmata (sensu lato) is a heterogeneous group that includes some soil- dwellers, plant-feeders (spider mites), and water mites; it was represented by 22 families in the CCB soil. Prostigmatids in desert habitats range from fewer than 1000 to 6000 per square meter and constitute from 40% to nearly 85% of the mite density (Kethley 1990). Dominant species represent the Bdelloidea, Caligonellidae, Nanorchestidae, Pygmephoridae, Tarsonemidae, and Tydeidae in North America (Dindal 1990). The biological plasticity within prostigmatid mites confounds unimodal characterization of feeding types. Walter (1988) reported that these mites are probably generalists and capable of feeding on a variety of fungi and/or nematodes, a characteristic that allows them to survive in desert habitats. Luxton (1981) suggests that populations increase during winter due to the rainy season, stimulating egg hatching, and the emergence of juveniles at the time of the renewed substrate, a general pattern documented for the Mojave Desert (Edney et al. 1976; Franco et al. 1979) and also observed in the CCB. For the Mesostigmata (9 families, 14 genera), the Ascidae was the most diverse family including five species (Fig. 3.10). Mesostigmatids would act as either predators or scavengers on soil nematodes, thus unraveling the complexity of microarthropod food webs. Astigmata occur sporadically and are the least abundant and diverse group of mites in the CCB soils: only one family (Acaridae) was found.
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3.4 Discussion This study represents the first survey of soil microarthropods performed in the CCB. The best represented group was the Acari, 90% of the records for mites are new for the state of Coahuila and also for the CCB. Particularly, oribatid mites have no previous records for Coahuila (Palacios-Vargas and Iglesias 2004); and knowledge and records for other soil mite groups such as Mesostigmata and Prostigmata are very scarce for Coahuila (Hoffmann and López-Campos 2000). The structure of soil microarthropod assemblages is similar in several arid regions of the world, and abundance and diversity are directly related to the quantity of litter accumulations and soil organic matter. Microarthropod densities found in the soil of the CCB sites can be compared with those found in other arid areas of the world (Australia, Wood 1971; Arizona, Whitford 1996; Cepeda-Pizarro and Whitford 1989a, b, 1990) where the organic matter (mainly organic C values) are similar to the CCB soils that we examined and where major acarine densities were found for Prostigmata and Oribatida. Sites with vegetation cover such as Mezquital, Tular, and Larrea had the highest microarthropod densities; this can be explained by the soil water content and the amount of organic matter (leaf litter). Santos et al. (1978) reported that total microarthropod densities were directly related to the amount of litter accumulation. Wallwork et al. (1985) found fewer oribatid mites in areas with physical disturbance from flooding, a factor to which these mites are very sensitive (Holt 1985). However, species richness in these sites was low when compared with zones without vegetation, closer to pools allowing a constant level of humidity in the soils. The relative abundance of these mites depends on the amount and depth of the litter layer or organic matter content (Loots and Ryke 1967; Cepeda-Pizarro and Whitford 1989a). Desert soils are typically characterized by low concentrations of N, P, and organic matter (West 1981; Gallardo and Schlesinger 1990), and the productivity of these ecosystems is primarily water-limited (Noy-Meir 1985; MacKay et al. 1986). Several studies have shown that N may limit production even when water is available (Fisher et al. 1987, 1988; Sharifi et al. 1988). Terrestrial consumer populations (i.e., soil microarthropods and nematodes) are among the many factors thought to affect soil nutrient cycles by altering the equilibrium between immobilization and mineralization of nutrients essential to plants (Kitchell et al. 1979; Ingham et al. 1985; Moore et al. 1988). The importance of soil microfauna in N mineralization has been emphasized in field studies in the CD (Santos and Whitford 1981; Whitford et al. 1983; Parker et al. 1984). No species of mites or of any other soil microarthropod group are listed in the NOM-059 (SEMARNAT, 2010), despite the important role they have in the soil. Climate change and particularly the irrational use of water in the CCB are some factors that directly affect the biodiversity of these organisms in this particular ecosystem.
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3.5 Conclusions This study has focused on the abundance and diversity of soil microarthropods in the CCB, a special and oligotrophic arid ecosystem with a high and different diversity among the studied sites. It should be emphasized that even though soil arthropods are diverse, the total diversity of all groups is lower than in mesic ecosystems. The extreme climatic conditions and unpredictability of the desert climate are such that many species will be surviving at their tolerance limits. Low diversity affects the composition of the functional fraction of the soil biota. Despite the limitations imposed by the abiotic environment, there are several taxa of soil microarthropods that could be considered keystone taxa. There may be many more keystone species among the soil biota that need to be discovered. The unique life histories and behavior characteristics of desert soil microarthropods determine the effects of these organisms on soil properties and soil formation. The soil biota, by affecting the spatial and temporal distribution of essential resources (water and nutrients), is vital for the maintenance of the ecosystem integrity in arid regions. Knowledge of soil microarthropods will be helpful in understanding and identifying the network of interactions and the flow of nutrients and energy within the desert ecosystem in the CCB. All these are crucial elements to evaluate the health status of the soil and to establish the appropriate strategies for it use, management, and conservation. Acknowledgments We would like to thank Valeria Souza and Luis E. Eguiarte for the invitation to participate in the inventory of the animal diversity of the Cuatro Ciénegas Basin as well as for being part of the editors of this volume. To Ana L. Carlos for assistance during field and laboratory work. We also want to thank Dr. Tila M Pérez for allowing us to use installations and equipment of the CNAC-IB, UNAM. We acknowledge the financial support of Alianza WWF-Fundación Carlos Slim.
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Chapter 4
Scorpions (Arachnida: Scorpiones) from the Cuatro Ciénegas Basin Oscar F. Francke B.
Abstract Twelve species of scorpions, belonging to three families and seven genera, have been recorded from the Cuatro Cienegas Basin (CCB). Two are considered endemic, but this might be due to poor sampling efforts in other areas of the state of Coahuila; the other ten species are widely distributed in the Chihuahuan Desert and are not threatened at the time. However, there is concern about the populations inside the Basin because the increasing aridification is causing a loss in primary productivity, which in turn has an impact on the arthropods that scorpions feed upon. Keywords Species richness · Origins and distribution · Conservation status
4.1 Introduction Historically, the scorpion fauna of the Cuatro Ciénegas Basin (CCB) has received little attention, most likely not because they are rare but because the species found there do not represent a threat to public health. In Mexico, scorpions of the genus Centruroides Marx are responsible for over half-a-million stinging accidents annually, creating a very serious threat to human life. However, the single species of Centruroides found in the CCB is not among the most toxic ones; fewer than 1000 stinging accidents were reported during the 10 years of 1997–2006 and no loss of life in the state of Coahuila. The first reports from the area date back to 1964, when Diaz-Nájera reported the presence of Centruroides vittatus (Say) and Diplocentrus whitei (Gervais) in the town of Cuatro Ciénegas de Carranza. Then Williams (1968) described five new species from Coahuila, all collected in the CCB and four presumably endemic to it; however, since then two of those species have been synonymized under older O. F. Francke B. (*) Colección Nacional de Arácnidos, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico e-mail: [email protected] © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_4
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existing names from taxa occurring outside the Basin: Vaejovis gilvus under Paruroctonus globosus by Francke (1977) and Vaejovis pallidus under Paruroctonus gracilior by Haradon (1985). Soleglad (1974) and Haradon (1985) each contributed with one additional new species each from the area. I was fortunate to visit the CCB in 2005, and collections made then have brought the actualized total of scorpions there to 3 families, 7 genera, and 12 species (see González-Santillán and Prendini 2013, for additional records of the four species of Chihuahuanus; Table 4.1). For comparative purposes only, the entire state of Coahuila has also 3 families and has 1 more genus (8 in total) and 19 species. However, all collections at the CCB have been made on the valley floor, and additional species can be expected in the Sierra de la Madera and Sierra San Marcos at higher elevations and in different vegetation zones.
4.2 Diversity and Endemism Only 2 of the 12 species found in the CCB (Table 4.1) are presumed endemics, Paruroctonus coahuilanus and Serradigitus calidus; but they will probably be found outside the Basin when more extensive sampling is done in other regions of the state.
4.3 Origins and Biogeography The fauna is from the Mexican Altiplano, mostly connected biogeographically with the states to the east, west, and north of the state (Table 4.1): 8 of the 12 species are shared with Durango, 7 species each with Chihuahua and Texas, and 6 with Nuevo Leon; the states to the south, Aguascalientes, San Luis Potosí, and Zacatecas, share only 1 or 2 species each, suggesting there is a barrier to dispersal into the CCB by southern elements in the Sierra Madre Oriental in southern Coahuila. The scorpion species present in the CCB (Figs. 4.1 and 4.2) do not appear to be under any threat at present, but climate change could have an impact in the future. Centruroides vittatus (Say) is found in six states in northern Mexico and numerous states in the Midwestern United States and has abundant populations occupying many different types of habitats. Diplocentrus whitei (Gervais) has been reported from four states in Mexico and from Texas; its populations tend to be localized based on the soil type they require to excavate their burrows, but when it is present, they are not rare. Chihuahuanus cazieri (Williams) is known from Coahuila and Nuevo León in desert environments and can be locally abundant. Chihuahuanus coahuilae (Williams) is found in the Mexican states of Chihuahua, Coahuila, and Durango and in the southwestern United States in Arizona, New Mexico, and Texas, and it can be locally abundant.
Genus Centruroides Diplocentrus Chihuahuanus Chihuahuanus Chihuahuanus Chihuahuanus Maaykuyak Paruroctonus Paruroctonus Pseudouroctonus Serradigitus Vaejovis Vaejovis
Species vittatus whitei cazieri coahuilae crassimanus globosus waueri coahuilanus gracilior reddelli calidus intermedius minckleyi 1
•
7
•
•
•
• •
Mexico Ags Chi • • Coa • • • • • • • • • • • • • 13 • • 8
•
• • • •
•
Dgo
6
•
•
•
NL • • •
1
•
SLP
1
Tam •
2
•
Zac •
2
•
•
4
•
• •
United States Az NM •
8
•
• •
•
• •
Tx • •
Ags Aguascalientes, Chi Chihuahua, Coa Coahuila, Dgo Durango, NL Nuevo Leon, SLP San Luis Potosi, Tam Tamaulipas, Zac Zacatecas, AZ Arizona, NM New Mexico, Tx Texas
Family Buthidae Diplocentridae Vaejovidae Vaejovidae Vaejovidae Vaejovidae Vaejovidae Vaejovidae Vaejovidae Vaejovidae Vaejovidae Vaejovidae Vaejovidae No. of species shared
Table 4.1 Scorpions known from the Cuatro Cienegas Basin and their known distributions in neighbouring states in the Chihuahuan Desert, both in Mexico and the United States
4 Scorpions (Arachnida: Scorpiones) from the Cuatro Ciénegas Basin 55
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Fig. 4.1 Representative scorpions from the Cuatro Cienegas Basin. (a) Centruroides vittatus Say (family Buthidae); (b) Diplocentrus whitei (Gervais) (family Diplocentridae); (c) Chihuahuanus cazieri (Williams) (family Vaejovidae); (d) Chihuahuanus coahuilae (Williams) (family Vaejovidae); (e) Chihuahuanus crassimanus (Pocock) (family Vaejovidae); (f) Chihuahuanus globosus (Borelli) (family Vaejovidae)
Chihuahuanus crassimanus (Pocock) has been reported from Chihuahua, Coahuila, Durango, and Nuevo León in Mexico and from New Mexico and Texas in the United States, where it is never very abundant but its wide distribution removes it from any threats. Chihuahuanus globosus (Borelli) has been reported from Coahuila, Durango, and Texas and is locally scarce, with only a few specimens showing up in most samples, but it is widely distributed. Maaykuyak waueri (Gertsch & Soleglad) was originally described from the Chisos Mountains in Big Bend National Park, Texas, but has since been also found in four Mexican states, including the CCB in Coahuila.
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Fig. 4.2 More representative scorpions from the Cuatro Cienegas Basin (a) Maaykuyak waueri (Gertsch & Soleglad) (family Vaejovidae); (b) Paruroctonus gracilior (Hoffmann) (family Vaejovidae); (c) Serradigitus calidus (Soleglad) (family Vaejovidae); (d) Vaejovis intermedius Borelli (family Vaejovidae); (e) Vaejovis minckleyi Williams (family Vaejovidae)
Paruroctonus gracilior (Hoffmann) is known from sandy soils and sand dunes in five states in northern Mexico and three in the southwestern United States; in the right habitat, the populations are dense. Paruroctonus coahuilanus Haradon is presently known only from the original description from the CCB; it requires loose sandy soils, and it is expected to be found in adjacent dune systems when they are properly sampled. Serradigitus calidus (Soleglad) is also known only from the CCB. These are small scorpions that live in cracks in rocks and rock walls and depend on their
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tremendous speed to escape predators, making them difficult to collect. Most species in the genus are rare in collections, and it is expected to be found in adjacent mountain ranges when these are adequately surveyed. Vaejovis intermedius Borelli was originally described from Durango but has since been collected in Chihuahua, Durango, Nuevo León, and Zacatecas in Mexico and in southern Texas in the United States. It prefers loose, gravely habitats such as rock-slides and rail-road tracks, where it can be very abundant and where it finds excellent protection from the elements as well as potential predators. Vaejovis minckleyi Williams was originally described from the CCB but has since been collected in Durango (pers. obs.). This is a large scorpion that lives in cracks and under large boulders and is difficult to collect; it is probably not very rare if the right habitat can be reached in the isolated mountain ranges that dot the Altiplano.
4.4 Discussion The richness in scorpion species found in the CCB is not extraordinary or unexpected, and it compares favourably with other sampling studies in North American deserts; Polis (1990) reported the existence of communities of 9 species in the desert of Nevada, 11 species in one community in California, and 10–13 species in various communities in Baja California Sur. It is doubtful that additional scorpion species will be found in the valley floor and along the lower reaches of the Sierra de San Marcos. However, sampling at the higher elevations in the Sierra de La Madera could yield several additional species, either range extensions of taxa known from the Chisos Mountains in Big Bend National Park, Texas, or from the Sierra Madre Oriental in Coahuila and Nuevo León, or perhaps even new species to science. Regarding their conservation status, although their wide distributions indicate that these species are not endangered, there is concern about their populations in the CCB. Scorpions are top predators in the invertebrate food chain of the area and depend on other arthropods, mostly insects, for food. The increasing aridification of the CCB due to uncontrolled water use for irrigation has lowered the water table significantly, thus affecting primary productivity (= plants) which in turn are consumed by the insects that scorpions prey upon; thus, a decrease in the food supply (= insects) is bound to cause a decrease in the abundance of scorpions locally. Acknowledgements Field work in the CCB in 2006 was financed by the REVSYS project awarded to Dr. Lorenzo Prendini (National Science Foundation grant DEB 0413453). Field assistance by David Sissom, Kari McWest, Brent Hendrixson, Steven Grant, Abigail Jaimes, Milagros Cordova, Edmundo Gonzáles, and Jesús Ballesteros was deeply appreciated. The photographs were taken in the field by Kari McWest, and his permission to use them is greatly acknowledged. Collections were done under Scientific Collector Permit FAUT-0175 from SEMARNAT to O. F. Francke; permission to camp and collect in the CCB was kindly granted by Dean Hendrickson on behalf of the Desert Fishes Council. Finally, I thank the editors of this book for inviting me to participate.
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References Díaz-Nájera A (1964) Alacranes de la República Mexicana. Identificación de ejemplares capturados en 235 localidades. Rev Inst Salub Enferm Trop 24:15–30 Francke OF (1977) Redescription of Vaejovis globosus Borelli (Scorpionida: Vaejovidae). Entomol News 88:45–51 González-Santillán E, Prendini L (2013) Redefinition and generic revision of the North American vaejovid scorpion subfamily Syntropinae Kraepelin, 1905, with descriptions of six new genera. Bull Am Mus Nat Hist 382:1–71 Haradon RM (1985) New groups and species belonging to the nominate subgenus Paruroctonus (Scorpiones, Vaejovidae). J Arachnol 13:19–42 Polis G (1990) The biology of scorpions. In: Stanford University Press. Palo Alto, California Soleglad ME (1974) Vejovis calidus, a new species of scorpion from Coahuila, Mexico (Scorpionida: Vejovidae). Entomol News 85:108–115 Williams SC (1968) Scorpions from northern Mexico: five new species of Vejovis from Coahuila. Mexico Occ Pap Cal Acad Sci 68:1–24
Chapter 5
The Spiders of the Churince Region, Cuatro Ciénegas Basin: A Comparison with Other Desert Areas of North America Pablo Corcuera, María Luisa Jiménez, and Marco Antonio Desales-Lara
Abstract In this study we compare the arachnofauna of the region known as Churince, in the Cuatro Ciénegas Basin (CCB), with the spider communities found in other localities of the North American deserts. We also compare the communities found in the main vegetation types of study site. The spiders of North American deserts were grouped according to biogeographical regions. The only exception was White Sands, which is part of the northern Trans-Pecos subregion of the Chihuahuan Desert (CD) and is an area of gypsum dunes (calcium sulphate). This unique substrate almost certainly determines the species that can be present in the area and suggests that, in addition to biogeographical patterns, local conditions may have a strong influence as filters for the species present in a particular site. Our study site (Churince) had the lowest number of species shared with the other CD sites. The Basin is located in the southern part of the CD in the Mapimí subregion and is the southernmost of all. This partially explains the differences in composition. Furthermore, the CCB probably has more species of spiders than any other of the North American desert regions. The variety of vegetation types within a relatively small area partly explains this since few species are shared among vegetation types. The CCB has a particularly high richness of wandering species of Lycosidae and Gnaphosidae. The latter is typical of the Nearctic North American deserts, but wolf spiders (Lycosidae) are frecuently found in wet environments. The family also includes a number of “supertramp” species which colonize areas after natural or anthropogenic perturbations. The climate of the CCB shows extreme variations, but, more importantly, Churince has been subject to human-induced perturbations that P. Corcuera (*) Laboratorio de Ecología Animal, Departamento de Biología, Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico e-mail: [email protected] M. L. Jiménez Laboratorio de Aracnología y Entomología, Centro de Investigaciones Biológicas del Noroeste, Instituto Politécnico Nacional, La Paz, Baja California Sur, Mexico M. A. Desales-Lara Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_5
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have increased in recent years. Although this can explain the high number of wolf spiders, it also has had a negative influence on the abundance and number of other spider families. Keywords Arthropods · Wetlands · Chihuahuan Desert · Perturbation · Biogeography · Regional diversity
5.1 Introduction In spite of their diversity and their importance as predators of insects and other arthropods (Turnbull 1973; Polis and Yamashita 1991), desert spiders have been scarcely studied. However, Chew (1961), Muma (1975), Gertsch and Riechert (1976), Broussard and Horner (2006), and Richman et al. (2011) have produced valuable information that includes abundances of spiders found in different sites in the CD. Jiménez and collaborators have also contributed considerably to the knowledge of spiders of arid zones and in particular of Baja California (Jiménez 1988; Llinas-Gutiérrez and Jiménez 2004; Jiménez and Navarrete 2010; Jiménez et al. 2015). In the CCB, part of the Mapimí subprovince of the CD, the only published papers on spiders are those by Jiménez et al. (2012), on a new record for Mexico, and Bizuet-Flores et al. (2015), who described the spider diversity and distribution in different vegetation types in the region known as Churince. At a biogeographical scale, Lightfoot et al. (2008) analysed the distribution of spiders and other arthropods in three sites within the southwestern arid region of the United States. The authors found that spider assemblages were more similar between vegetation associations in the same region than between similar vegetation types in different regions. However, the similarity was also low within the plant associations within each region. This confirms that, at least locally, spider distribution is associated with structural and floristic characteristics of the vegetation and this is the reason why spiders are good indicators of habitat variations (Wheater et al. 2000; Jiménez and Navarrete 2010; Oxbrough et al. 2010; Corcuera et al. 2015). In this study, we compared the spiders found in different subprovinces of the Chihuahuan and Sonoran Deserts. We also assessed the spider assemblages between some of the dominant vegetation types of the CCB. The questions we ask are: (1) How many spider species are there in Churince, a region within the CCB, compared to other North American deserts? (2) Is the proportion of species per family similar between regions? Alternatively, is the CCB arachnofauna a subset of the North American deserts spider assemblage? If not, are there some families with more or less species than expected according to what has been found in the other regions? (3) Is there a coincidence between a spider-based classification of the sites included in this study and the biogeographical regions that have been recognized in the literature? (4) How dissimilar are the spider communities among the vegetation types found in the study area? Can the complementarity between vegetation associations partially explain the number of species found in the valley?
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5.2 Materials and Methods 5.2.1 Study Sites We compared the composition and spider richness between the CCB and other eight sites located in the Trans-Pecos subprovince in the CD (Sevilleta Wildlife National Refuge, Jornada del Muerto, White Sands National Park and Dalquest Desert Research Station), Sonora (Comitán and Baja California Sur Oases) Desert, and a subtropical arid region in southern Mexico (Tehuacán-Cuicatlán) (Fig. 5.1, Table 5.1). The CCB is in the Mapimí subprovince of the CD and Dalquest belongs to the Trans-Pecos, but it is in the limit with Mapimí. Precipitation ranges from an annual mean of 150 mm in the CCB to 390 mm in the Tehuacán-Cui- catlán reserve. Sevilleta has the lowest mean annual temperature (14 °C) and Comitán, in Baja California Sur, the highest (25 °C). Pitfalls and direct sampling were used to catch spiders in the CCB, Jornada del Muerto, Valley of Fire, and Comitán. Sampling in White Sands, Dalquest and Sevilleta was done with pitfalls only. In Zapotitlán ramp traps were used, the same method used for ground spiders in the CCB. The lists of
Fig. 5.1 Location of the sites used to compare the spider faunas in the deserts of North America as well as the main vegetation types in Churince, Cuatro Ciénegas. A = Valle of Fires, B = Sevilleta, C = Jornada del Muerto, D = White Sands, E = Dalquest, Big Bend, F = Churince, Cuatro Ciénegas, G = Zapotitlán, Tehuacán-Cuicatlán, 1 = Mezquital, 2 = Larrea scrubland, 3 = Grasland, 4 = Sotol scrubland, 5 = Playas, 6 = Baja California Oases, 7 = Comitán
Mainly pitfalls Can traps
b
a
26°23′34″N 111°49′13″W 24°05′13″N 110°11′19″W 23°55′40″N 110°13′27″ 18°19′55″N 97°27′29″W
San José Buena Mujer El Novillo
San Isidro
Site 1 Site 2 Site 3 Site 4
Coordinates 26°59′10″N 102°03′59″W 32°30′N 106°48″W 32°36′18″N 106°50′51″W 32°36′5″N 106°44′32″W 32°42′32″N 106°49′28″W 32PER′47″N 106LIN′18″W 36°27′22″N 114°31′59″W 33′25.19″N × 103° 47′38.16″W 24°6′31″N 110°22′29″W 26°12′23″N 112°02′54″W
Replicates
Sevilleta National Wildlife Cresosotebush 34°19′58.0″N Refuge (Sev) 106°44′9″W Black gramma 34°20′17″N 106°43′3″W Pine Juniper 34°22′6.3″N 106°32′6″W
Zapotitlán (Zap)
Comitán (Com) Humedales (HS)
White Sands (WhS) Valley of fire (VF) Dalquest (Dal)
Site Cuatro Ciénegas (CC) Jornada (JM)
1736
1500
5 0.333– 180
1291 675 1267
Mean height 740 1325
250
390
c.200 c.200
229 166 380
Mean rainfall 150 294
14
20
25 20
15.4 20.7 22.1
Woodland
Grassland
Oasis Oasis Oasis Scrubland sarcocaulescent scrub Scrubland
Sarcocaulescent scrub Oasis
Dunes grassland Open scrub Scrubland riparian
Mean temperature Vegetation 20 Grassland scrubland wetland 19 Grassland scrubland
Pitfalls
Ramp
Mixedb Golpeo
Pitfalls Mixed Pitfalls
Method Mixed Mixeda
Table 5.1 Coordinates, mean height, rainfall, temperature, main vegetation types, and spider collecting methods in nine sites in the Chihuahan and Sonoran deserts and a subtropical arid region in central Mexico
64 P. Corcuera et al.
5 The Spiders of the Churince Region, Cuatro Ciénegas Basin: A Comparison…
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species were obtained from Lightfoot et al. (2008) (Sevilleta), Muma (1975) (White Sands), Broussard and Horner (2006) (Dalquest), Richman et al. (2011) (Jornada del Muerto and a review of the studies from the previous authors for the CD), Bizuet-Flores et al. (2015) (Cuatro Ciénegas), Jiménez and Navarrete (2010) (Comitán, BCS), and Jiménez et al. (2015) (BCS Oasis). Spiders from Tehuacán- Cuicatlán were identified by the authors of this study. We then compared the composition (see below) and the number of species per family between the CCB and the other sites. The CCB is an enclosed watershed surrounded by more than 3100 m high mountains. The valley includes a system of natural springs, streams, and ponds. The study area, known as Churince, is c. 2000 ha and has five main vegetation associations: (1) Prosopis glandulosa shrubland (Mezquital), (2) Sporobolus/Distichlis spicata wet grasslands (Pastizal), (3) Larrea tridentata/Fouqueria splendens desert scrub (Larrea), (4) Dasylirion wheeleri desert scrub (Sotolera), and (5) Sporobolus tussocks surrounded by areas with no vegetation cover (Playas) (Fig. 5.1). Spiders from Churince were caught weekly from March to May and from September to November 2011, January to May and July to October 2012, May to December 2014, January to December 2015, and January to April 2016. Six replicates (sample units) of five traps each were placed in each vegetation association, separated by 100 m. The five traps in each sample unit site were placed in the centre and extreme ends of a 10 × 10 m2 quadrat. Each trap consisted of a plastic container (15 × 23 × 8 cm3) with two 6 × 6 cm2 lateral openings. A triangular aluminium ramp was placed in the lower part of each opening (Bouchard et al. 2000). Each ramp was previously varnished with a sand texture aerosol. The containers were filled with water and a small quantity of detergent added to lower the surface tension. It has been shown that these traps are efficient to sample ground spider communities (Brennan et al. 1999; Pearce et al. 2005). Direct sampling followed the method implemented by Coddington et al. (1991) and was conducted from 7 to 14 October 2014; 31 March to 6 April and 12–18 June 2014; 8–13 October 2015; and 22–26 and 30 June to 4 July 2016. In each of the five plant associations, we placed two 200 × 3 m quadrats and two people collected all spiders found on and under rocks as well as on the vegetation under and above 50 m for a period of 2 hours. All specimens were preserved in 96% alcohol. The procedure was carried out from 8 to 10 hours and from 17:30 to 19:30 hours. All the adults were identified to species or morphospecies. Specimens were separated into families and identified to genus level according to Ubick et al. (2005) and to species with the taxonomic works of various authors. Scientific names were verified in the World Spider Catalog (2014). The specimens were preserved in 75% ethanol and deposited in the Arachnological Collection (CARCIB) at Centro de Investigaciones Biológicas del Noroeste, La Paz, Baja California Sur, Mexico.
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5.2.2 Statistical Analyses As a first approach, we compared the number of species per family found in Churince with the other sites by means of a goodness of fit test (χ2). The aim of this approach was to test if the spider fauna of our study site was a subset of the spiders found in the North American deserts and of the CD in particular. Since spiders were only sampled with pitfalls in four sites (White Sands, Dalquest, in the Big Bend National Park, Comitán and Zapotitlán) (we used both, direct and pitfall traps in CCB), we repeated the analyses without these sites. The idea was that in these locations foliage and orb and spatial web spiders would be under-represented since pit- falls would have few individuals of these groups. We repeated the analysis with the CD sites and with the Chihuahuan sites where both techniques were used. The compositional similarity between arid regions was assessed with a classification and a similarity matrix with the Jaccard index. The unweighted pair group method (UPGMA) was used for the classification and only the identified species were included. We included the morphospecies that were present only in one site because in that case there was no confusion that it was the same or a different species in two or more locations. In order to compare the spider assemblages between the five vegetation types in Churince, we used the monthly mean abundance of all the study years. We used the Bray-Curtis dissimilarity with the unweighted pair group method UPGMA to classify the vegetation types. A one-way analysis of similarity (ANOSIM), also with the Bray-Curtis index, was used to test if there were significant differences between the spider associations of each site (Clarke 1993). Multivariate analyses were executed in Past v. 3.14 (Hammer et al. 2001).
5.3 Results We found 159 species grouped in 37 families in the Churince region. Gnaphosi- dae, Lycosidae, and Salticidae were represented by 39, 24, and 21 species. Philodromidae and Thomisidae were present with nine and eight species, and the weaver families Araneidae and Theridiidae had seven and six species, respectively. Even though abundances were low (only 1227 specimens in 5 years, 815 collected with pitfalls and 412 by direct sampling), the number of species was second only to the Baja California Oases (199) and was followed by Jornada del Muerto, with 121 species captured in more than 30 years of sampling. The sites in which only pitfalls were used had fewer species, as would be expected (Fig. 5.2). Nonetheless, when comparing only the number of spiders caught with pitfalls, Churince had the highest richness of all (Fig. 5.2). The goodness of fit tests showed that Churince is not a sub-group of the spider fauna found either in all sites or in the four sites with mixed sampling. When all sites were included, CCB had a lower number of species of Theriididae and
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Fig. 5.2 Number of spider species found in eight sites within the main North American deserts with pitfalls and mixed techniques (direct sampling and pitfalls). Results from pitfall and mixed sampling are shown for Baja California Oases (HBCS) and Churince. Mx mixed, Ptf pitfalls
Araneidae and a higher number of Gnaphosidae and Lycosidae with regard to the species set of the other sites. When we compared the CCB with the CD ensemble and with the Chihuahuan sites in which the two sampling techniques were used (as was the case of Churince), the number of species of Gnaphoside did not differ from the other sites. Wolf spiders, on the other hand, still had more species in Churince (Table 5.2; Fig. 5.3). In general, the Jaccard coefficients were higher amongst the Trans-Pecos subprovince sites and between the two Baja sites than among provinces and subprovinces. Churince and specially Zapotitlán had a low similarity with the rest (Table 5.3). With the exception of White Sands, which was separated from the other northern sites, a classification, based on the same coefficients, showed that the locations were grouped according to their respective biogeographic provinces/subprovinces (Fig. 5.4). Zapotitlán, a province on its own, was separated from the rest of the sites on the first level. On a second level, the two Baja California sites were segregated from those belonging to the CD. Churince was then separated from the rest of the Chihuahuan sites (Fig. 5.4). Within the Churince region, a Bray-Curtis classification separated three sites with high soil humidity (grassland, sotol, and playas) from two dry sites (mesquite and Larrea shrubland) (Fig. 5.5). The grassland was the least similar of the three wet sites and the composition amongst the five sites was significantly different according to the analysis of similarities (R = 0.64, p 145 Mya) suggest the antiquity of the subgenera of Daphnia and their coevolution with chaoborid predators. BMC Evol Biol 11:129 Lemos-Espinal JA, Smith GR (2016) Amphibians and reptiles of the state of Coahuila, Mexico, with comparison with adjoining states. Zookeys 593:117–137 Maeda-Martínez A, Obregón-Barboza H, García-Velazco H, Prieto-Salazar MA (2002a) Branchiopoda: Anostraca. In: Llorente-Bousquets J, Morrone JJ (eds) Biodiversidad, taxonomía y biogeografía de artrópodos de México: Hacia una síntesis de su conocimiento. Volumen III. Facultad de Ciencias, UNAM-Conabio-Bayer, Mexico DF. 680 pp Maeda-Martínez A, Obregón-Barboza H, García-Velazco H (2002b) Branchiopoda: Cyclestherida, Laevicaudata, and Spinicaudata. In: Llorente-Bousquets J, Morrone JJ (eds) Biodiversidad, taxonomía y biogeografía de artrópodos de México: Hacia una síntesis de su conocimiento. Volumen III. Facultad de Ciencias, UNAM-Conabio-Bayer, Mexico DF. 680 pp Maeda-Martínez A, Obregón-Barboza H, García-Velazco H, Murugan G (2002c) Branchiopoda: Notostraca. In: Llorente-Bousquets J, Morrone JJ (eds) Biodiversidad, taxonomía y biogeografía de artrópodos de México: Hacia una síntesis de su conocimiento. Volumen III. Facultad de Ciencias, UNAM-Conabio-Bayer, Mexico DF. 680 pp Marrón-Becerra A, Hermoso-Salazar M, Solis-Weiss V (2018) Hyalella maya, a new Hyalellidae species (Crustacea: Amphipoda) from a cenote in the Yucatan Peninsula, Mexico. J Cave Karst Stud 80:1–11 Martens K, Coomans A (1990) Phylogeny and historical biogeography of the Megalocypridinae Rome, 1965; with an updated checklist of the subfamily. In: Whatley RC, Maybury C (eds) Ostracoda and Global events, Proceedings of the 10th Intnl Symp on Ostracoda, Chapmann & Hall Mercado-Salas NF, Suárez-Morales E (2012) Morfología, diversidad y distribución de los Cyclopoida (Copepoda) de zonas áridas del centro-norte de México. II Eucyclopinae y análisis biogeográfico. Hidrobiológica 22:99–124 Metcalfe S, Say A, Black S, McCulloch R, O'Hara S (2002) Wet conditions during the last glaciation in the Chihuahuan Desert, Alta Babicora Basin, Mexico. Quat Res 57:91–101 Minckley WL (1984) Cuatro Cienegas fishes: research review and a local test of diversity versus habitat size. J Ariz Nev Acad Sci 19:13–21 Moreno-Letelier A, Olmedo G, Eguiarte LE, Martínez-Castilla L, Souza V (2011) Parallel evolution and horizontal gene transfer of the pst operon in Firmicutes from oligotrophic environments. Int J Evol Biol 2011:781642 Morvan C, Malard F, Paradis E, Lefebure T, Konecny-Dupré L, Douady CK (2013) Timetree of Asellidea reveals species diversification dynamics in groundwater. Syst Biol 62:512–522 Porter ML, Pérez-Lozada M, Crandall KA (2005) Model-based multi-locus estimation of decapod phylogeny and divergence times. Mol Phylogenet Evol 37:355–369 Reid JW, Hudson PL (2007) Comment on “Rate of species introductions in the Great Lakes via ships’ ballast water and sediments”. Can J Fish Aquat Sci 65:549–553 Rocha-Ramírez A, Álvarez F, Alcocer J, Chávez-López R, Escobar-Briones E (2009) Lista anotada de los isópodos acuáticos epicontinentales de México (Crustacea: Isopoda). Rev Mex Biodivers 80:615–631
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Rodríguez-Almaraz GA, Muñiz R (2008) 7. Conocimiento de los acociles y langostinos del noreste de México: amenazas y propuestas de conservación. In: Álvarez F, Rodríguez-Almaraz GA (eds) Crustáceos de México: Estado actual de su conocimiento. Universidad Autónoma de Nuevo León-Promep, Monterrey, Nuevo León, México Rodríguez-García S (2015) Revisión taxonómica de los Oníscidos (Crustacea: Isopoda) de México. Tesis Licenciatura, Facultad de Ciencias, UNAM, 168 pp Simpson SL, Spadaro DA (2011) Performance and sensitivity of rapid sublethal sediment toxicity tests with the amphipod Melita plumulosa and the copepod Nitocra spinipes. Environ Toxicol Chem 30:2326–2334 Souza V, Siefert JL, Escalante AE, Elser JJ, Eguiarte LE (2012) The Cuatro Ciénegas Basin in Coahuila, Mexico: an astrobiological Precambrian park. Astrobiology 12:641–647 Suárez-Morales E, Reid JW (1998) An updated list of the free-living freshwater copepods (Crustacea) of Mexico. Southwest Nat 43:256–265 Suárez-Morales E, Walsh EJ (2009) Two new species of Eucyclops Claus (Copepoda: Cyclopoida) from the Chihuahuan Desert with a redescription of E. pseudoensifer Dussart. Zootaxa 2206:1–22 Suárez-Morales E, Gutiérrez-Aguirre MA, Walsh EJ (2010) Freshwater Copepoda (Crustacea) from the Chihuahuan Desert with comments on biogeography. Southwest Nat 55:525–531 Thum RA (2004) Using 18S rDNA to resolve diaptomid copepod (Copepoda: Calanoida: Diaptomidae) phylogeny: an example with the North American genera. Hydrobiologia 519:135–141 Thum RA, Derry AM (2008) Taxonomic implications for diaptomid copepods based on contrasting patterns of mitochondrial DNA sequence divergences in four morphospecies. Hydrobiologia 614:197–207 Witt JDS, Hebert PDN (2000) Cryptic species diversity and evolution in the amphipod genus Hyalella within central glaciated North America: a molecular phylogenetic approach. Can J Fish Aquat Sci 57:687–698 Wyngaard GA, Holynska M, Schulte JA (2010) Phylogeny of the freshwater copepod Mesocyclops (Crustacea: Cyclopidae) based on combined molecular and morphological data, with notes on biogeography. Mol Phylogenet Evol 55:753–764 Zamudio-Valdéz JA (1991) Los copépodos de vida libre (Crustacea, Maxillopoda), del Valle de Cuatro Ciénegas, Coahuila, México. Tesis Licenciatura, Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León, 107 pp Zamudio-Valdéz JA, Reid JW (1990) A new species of Leptocaris (Crustacea, Copepoda, Harpacticoida) from inland waters of Mexico. An Inst Cienc Mar Limnol, UNAM 17:47–54
Chapter 7
Spatial and Temporal Patterns of Diversity of the Lepidoptera (Papilionoidea sensu lato) in the Cuatro Ciénegas Basin Jessica Hernández-Jerónimo, Uri Omar García-Vázquez, Omar Ávalos- Hernández, Arturo Arellano-Covarrubias, Moisés Armando Luis-Martínez, and Marysol Trujano-Ortega
Abstract We describe and compare the patterns of species richness, species abundance, and species composition in space and time of butterflies (Papilionoidea sensu lato) in seven localities of the Cuatro Ciénegas Basin (CCB) in northeast Mexico. Although the basin is one of the most important wetlands in Mexico, due to the endemism rate, the knowledge of its fauna, including butterflies, is incomplete or null. This research is the first systematic faunistic study in the basin and includes 5 families, 44 genera, 59 species, and 5429 specimens, from which 33 are new records for the CCB and 10 for Coahuila, and for 1 species its occurrence is confirmed in the country. Nymphalidae, with 30 species, was the most diverse family, while Lycaenidae was the most abundant (1849 specimens), as opposed to Papilionidae and Riodinidae which were the less rich and abundant families. The diversity was higher during the rainy season and in the halophyte and gypsum dunes habitats. Three localities, Río Cañón, Antiguos Mineros del Norte, and Rancho Orozco, were the localities with highest richness and abundance. An analysis of the feeding guilds showed that in this arid habitat, butterflies use flower resources most than any other. We also analysed the biogeographical affinity, where 52% of the species (28 spp.) had a Nearctic affinity and 42% (23 spp.) were Neotropical species. The results highlight the idea of the great diversity of the CCB but also expose the lack of knowledge of insects in the deserts of Mexico.
J. Hernández-Jerónimo · O. Ávalos-Hernández · A. Arellano-Covarrubias M. A. Luis-Martínez · M. Trujano-Ortega (*) Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico U. O. García-Vázquez Laboratorio de Sistemática Molecular, Unidad de Investigación Multidisciplinaria de Investigación Experimental Zaragoza, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México, Ciudad de México, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_7
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Keywords Species richness · Foraging behaviour · Biogeographic affinities · Hotspot · Chihuahuan Desert
7.1 Introduction Lepidoptera is the second most diverse taxa in the world, surpassed only by Coleoptera. Recent estimations predict 23,750 species in Mexico of which 14,500 have been described and recorded (Llorente et al. 2014). Within the order, the butterflies or Papilionoidea (sensu lato) comprise 13% of the species, and 1929 species and subspecies are recorded for Mexico grouped in six families: Hesperiidae (764 sspp.), Nymphalidae (527 sspp.), Lycaenidae (252 sspp.), Riodinidae (205 sspp.), Pieridae (105 sspp.), and Papilionidae (76 sspp.) (Llorente et al. 2014). Because of its great diversity, butterflies are a fundamental biological model for biogeographic, conservation, genetic, and ecologic studies. They also show great predictive power for some other invertebrate and vertebrate taxa, regarding evolutive, coevolutive, ecological, genetic, and spatial distribution processes (Pozo et al. 2015). In Mexico, the butterfly fauna of humid and subhumid habitats are the best known, mainly from the southern and southeastern states. In contrast, desertic and semi-desertic habitats have received less attention, even when these habitats contain most of the endemic species. The largest desertic area in North America is the Chihuahuan Desert (CD) with an area of 450,000 km2 (Morafka 1977), from which 85% is located in northern and central Mexico (Loera 2013). The “Fauna and Flora Protection Area CuatroCiénegas” is the most important wetland in the CD, and it is within the CCB in Coahuila, Mexico. This wetland is also one of the most relevant of Mexico due to the presence of endemic species (Loera 2013), especially in aquatic environments (INE 1999). Research on the insects of the CCB is scarce, with just a few isolated records. Particularly for butterflies, there are only three publications from a decade or more ago, reporting some species (Clench 1968; Contreras 1977; Contreras and Warren 2006); however, none of these works constitute a systematic study or analysis of the butterfly diversity of the area. We present a systematic faunistic study of the butterflies (Papilionoidea s. lato) in the CCB. The diversity, species richness patterns, phenology, feeding preferences, and biogeographical affinities of the butterflies are analysed. Due to the scarcity of data of Hesperiidae at a national scale and for comparative purposes, we excluded this family from the analyses. This study will contribute to the understanding of the insect communities of the arid regions of the country, and particularly of this priority for conservation protected area, which is suffering great human-induced alterations.
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7.2 Materials and Methods Sites were selected following abiotic and biotic criteria. All localities have superficial water, except Río Cañón. Most localities show some degree of perturbation due to the presence of cattle, agriculture, and tourism. Dominant habitat was desertic shrub of the microphyle and rosetophyle variants, but all habitats present in the CCB were included: sotol, mesquite, secondary grassland, and semiaquatic vegetation associated to ponds. Churince pond is the only site with gypsum dune habitat. The climate is desertic dry (BW) (García 1964) with three well-defined seasons: rainy, cold dry, and hot dry. Within seven localities, 16 sites were selected: (1) Churince with five sites, (2) Rancho PRONATURA with four sites, (3) Rancho Orozco with three sites, (4) Antiguos Mineros del Norte, (5) La Poza Azul, (6) Río Cañón, and (7) San José del Anteojo, one site for each of the last four localities. The number of sites was assigned according to the size, environmental heterogeneity, and observed diversity of each locality. Each locality was taken as an independent unit, although fauna interchange is possible but not probable (Fig. 7.1).
Fig. 7.1 Sampling sites in the Cuatro Ciénegas Basin (CCB), Coahuila, Mexico
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7.2.1 Fieldwork Fourteen field trips were made during 2012 and 2013; records from sporadic trips in 2009 and 2010 are also included. Effective sampling effort was 84 days with at least three collectors each day. Sampling spans from 9:00 to 16:00 h covering the three seasons present in the region. Two sampling techniques were applied, entomological net and Van Someren- Rydon traps, due to the vegetation traps that could only be set in Río Cañón and Antiguos Mineros del Norte. All insects observed were collected and prepared for posterior identification.
7.2.2 Taxonomic Determination Butterflies were identified to the species level with specialized literature (e.g. Miller 1974; Turner and Parnell 1985; Prudic et al. 2008; Grishin and Durden 2012) and comparison with specimens from the Lepidopterological Collection of the Zoological Museum “Alfonso L. Herrera” of the Facultad de Ciencias, UNAM, and the images available in the website “Butterflies of America” (Warren et al. 2013).
7.2.3 Data Analysis Species richness estimation was made with species accumulation models using specimens as sampling effort (Jiménez-Valverde and Hortal 2003), with the software EstimateS v.9 (Colwell 2013). Data were adjusted to the Clench model for evaluation of the sampling effort efficiency (Ávalos-Hernández 2007). Similarities between localities with enough sampling effort were estimated with the Bray-Curtis index. Colwell and Coddington’s (1994) coefficient of complementarity was used to estimate the difference in species composition between localities. Adult feeding preferences were analysed using the species richness and abundance in each feeding guild. Species richness and abundances were also analysed by seasons. Foraging is related to climatic conditions and food availability; feeding preferences were divided into three guilds: flower visitors (nectarivorous), wet-sand visitors for water and minerals (mud-puddling), and organic decomposed matter feeders (fruit feeding) (Luis and Llorente 1990). Lastly, biogeographic affinities were determined with specialized literature considering three regions Palearctic, Nearctic, and Neotropical (Halffter 1976; Morrone et al. 2002).
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7.3 Results Fifty-nine taxa at the species level (species and subspecies) and 5429 specimens were collected, from 44 genera of Papilionoidea s. lat., grouped in five families: Nymphalidae (30), Pieridae (14), Lycaenidae (9), Papilionidae (4), and Riodinidae (2). From these families, Pieridae was the most abundant with 1849 specimens, followed by Nymphalidae with 1727, Lycaenidae with 1719, Papilionidae with 75, and finally Riodinidae with 59 specimens. Specifically, Brephidium exilis exilis Boisduval (Lycaenidae) was the most dominant species on both spatial and temporal scales. Forty-three species were recorded for the first time in this study, ten new records for Coahuila, Eurema daira eugenia Wallengren, Apodemia palmerii australis Austin, Megisto rubricata smithorum Wind, Eunica monima Stoll, Hamadryas februa ferentina Godart, Adelpha eulalia Doubleday, Polygonia interrogationis Fabricius, Junonia evarete Cramer, Chlosyne theona bollii Edwards, and Strymon solitario Grishin and Durden, and 33 new records for the CCB. The presence of Strymon solitario in Mexico is confirmed. This species was cited for Tamaulipas (Grishin and Durden 2012) based on photograph records. The specimens of the CCB present all the diagnostic characters of the species and are the first to be collected in the country.
7.3.1 Species Richness The butterfly species list for the CCB was completed in 94% of the estimated richness, which we consider acceptable. According to the Clench model, 100% of the species of Pieridae, Papilionidae, and Riodinidae were recorded, while for Nymphalidae and Lycaenidae, the lists were 90% complete. Species richness estimation was highest for Nymphalidae with 33 taxa, followed by Pieridae (14), Lycaenidae (10), Papilionidae (4), and Riodinidae with two (Table 7.1).
Table 7.1 Species richness estimation of Papilionoidea sensu lato R2, model adjustment (100% = total fit of the model with the observed data) Family Nymphalidae Pieridae Lycaenidae Papilionidae Riodinidae
Clench Observed taxa 30 14 9 4 2
% R2 99 97 94 98 99
Estimated taxa (asymptote) 33 14 10 4 2
% Completeness 91 100 90 100 100
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7.3.2 Similarity Churince and Rancho PRONATURA were the most similar localities (72%). The second group of localities was formed by Rancho PRONATURA-Churince and Rancho Orozco with 67% similarity. In third place, Antiguos Mineros del Norte is added with 63% of shared species. Lastly, Río Cañón is the less similar locality in relation to the others with 52% of similarity (Fig. 7.2).
7.3.3 Complementarity Antiguos Mineros del Norte and Churince are the most complementary localities (54%), meaning that the butterfly faunas between them are the most different and therefore more relevant for its conservation. Together, both localities contain 50 taxa, from which 27 are not shared; 9 species are present only in Churince and 18 species are present only in Antiguos Mineros del Norte (Heraclides ornythion Boisduval, Pyrisitia nise nelphe Felder, Atlides halesus Cramer, Strymon solitario, and Vanessa cardui Linnaeus). Whereas, Antiguos Mineros del Norte and Río Cañón have the lowest complementarity (29%), recording 49 taxa from which 35 are shared and 14 are exclusive of one of these sites, 6 in Antiguos Mineros and 8 in Río Cañón (Pyrisitia proterpia Fabricius, Hemiargus ceraunus Fabricius, Apodemia palmerii australis, and Limenitis arthemis arizonensis Edwards) (Table 7.2). Cñ
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Fig. 7.2 Similarity dendrogram between five localities of the CCV. AM Antiguos Mineros, CHU Churince, RO Rancho Orozco, RPRO Rancho PRO-NATURA, Cñ Río Cañón
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AM 0 54 47 40 29
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7.3.4 Phenology The rainy season has the highest species richness and abundance with 57 species (97%) and 4358 specimens (80%). During the dry season, 33 taxa (56%) were recorded and 1071 specimens (20%). Most specimens during the dry season (90% of the dry season specimens) were collected in the hottest portion of the year. Papilionoidea sensu lato shows a maximum of species richness and abundance in October (rainy season) with 47 species and 1274 specimens. Besides, the hot dry season shows a small peak with 24 species and 874 specimens in April. The lowest species richness and abundance are in the cold dry season, with 12 species and 46 specimens in February (Fig. 7.3). Twenty-six taxa are exclusive of the rainy season, sixteen species of Nymphalidae, five species of Pieridae, three species of Lycaenidae, and two species of Papilionidae. Only two taxa are exclusive of the dry season, Nymphalis antiopa Linnaeus and Zizula cyna Edwards. Four species are present throughout the year in the CCB, a pierid (Nathalis iole Boisduval) and three lycaenids (Leptotes marina Reakirt, Brephidium exilis Boisduval, and Echinargus isola Reakirt).
Fig. 7.3 Phenology of Papilionoidea sensu lato. CD, cold dry, HD, hot dry, R rainy
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7.3.5 Feeding Guilds Feeding preferences were recorded for 39 species and 1223 specimens. Nectarivorous butterflies are the most diverse (60% of the species) and abundant (72% of the specimens), then mud-puddling with 46% of the species and 9% of the specimens, and finally the fruit feeding represents 41% of the taxa and 31% of the specimens (Fig. 7.4). The feeding preferences and resource use vary within each family; Nymphalidae presents 15 fruit feeding and 9 nectarivorous species, Pieridae 10 nectarivorous, and Lycaenidae 4 mud-puddling species with 67 specimens. From all the taxa for which feeding preferences were recorded, 54% are exclusive of a guild, and 46% use at least two different resources. Exclusive species include 13 nectarivorous (v. gr. Phoebis sennae marcellina Cramer, Chlosyne lacinia adjutrix Scudder, Euptoieta claudia daunius Herbst) and 8 fruit feeding (v. gr. Anaea troglodyta aidea Guérin-Méneville, Polygonia interrogationis Fabricius, Vanessa atalanta rubria Fruhstorfer). Generalist species comprise 18 spp., from which 13 feed on two sources, wet-sand and flowers. Asterocampa leilia Edwards and Anartia jatrophae luteipicta Fruhstorfer prefer decomposing fruit or excrement. Finally, five species consume the three resources analysed here; these are the most generalist (Pyrisitia nise nelphe Felder; Kricogonia lyside Godart; Leptotes marina, Brephidium exilis, and Libytheana carinenta mexicana Michener).
Fig. 7.4 Feeding guilds analysed of Papilionoidea sensu lato from the Cuatro Ciénegas Basin
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Table 7.3 Biogeographic affinities by family of Papilionoidea sensu lato in the CCB Family Papilionidae Pieridae Nymphalidae Riodinidae Lycaenidae Total spp. by region % of spp. by region
Palearctic 0 0 0 0 3 3 6
Nearctic 2 5 19 1 1 28 52
Neotropical 2 9 10 1 1 23 42
Total spp. by family 4 14 29 2 5 54 100
Spp., taxa at species taxonomic level
7.3.6 Biogeographic Affinity Data of biogeographic affinity were obtained for 54 species and subspecies; from the other 5 species (mostly Lycaenidae), no data were available. Species that occur in the CCB have affinity with three regions, the Boreal regions being the most represented, Nearctic (52%, 28 species) and Palearctic (6%, three species), which agrees with patterns of other groups as Odonata and Diptera. The rest of the species have an affinity with the Neotropical region (42%, 23 species). It is worth noticing that the affinities vary with each family; Nymphalidae (19 Nearctic species) and Lycaenidae (three Palearctic species) have mainly a Boreal affinity, while Pieridae has mainly a Neotropical affinity with nine species. Papilionidae and Riodinidae show evenly Nearctic and Neotropical affinity (Table 7.3).
7.4 Discussion This is the first systematic study of the Lepidoptera of the CCB; therefore the results affect the diversity at the national, state, and regional levels, showing the lack of systematic studies at different taxonomic, temporal, and spatial scales that would help in the understanding of the diversity, structure, and functioning of communities (Stork et al. 1996). The confirmation of the presence of Strymon solitario (Lycaenidae) in the country increases the list of Papilionoidea sensu lato of Mexico (Llorente et al. 2006, 2014); so now the total is 1166 taxa at the species level. There are no complete butterfly species inventories for the state of Coahuila; a literature review resulted in 105 species recorded (Hoffmann 1940; Clench 1968; Contreras and Warren 2006; Llorente et al. 2006, 2014; Warren et al. 2008). Here we add 10 records for the state, so now Coahuila has 115 species, which is 10% of the national species richness, and this moves Coahuila to the 28th place, over Guanajuato and Aguascalientes, both with 91 species each. Species recorded in the
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CCB increases from 27 taxa (Clench 1968; Contreras 1977, 1984; Contreras and Warren 2006) to 59 species. This is important because insects of arid areas of northern Mexico are scarcely represented in Mexican insect collections (LuisMartínez et al. 2005; Llorente et al. 2014). The butterfly fauna of the CCB has a diversity pattern, at the family level, different from those described by Llorente et al. (2014). Our results and theirs both put Nymphalidae as the richest family, but here we report a higher diversity for Pieridae, Lycaenidae, and Papilionidae in the CCB. Lastly, Riodinidae has just two species of two genera (Calephelis y Apodemia), which was expected since this family has its origin in the Neotropics (Espeland et al. 2015). With this study, along with the studies on Odonata (Ortega 2015; Ortega-Salas and González-Soriano 2015), butterflies and dragonflies are the two best-known groups of insects of the CCB with 94% of their species known, followed by bees and pollinator flies (Diptera, Hymenoptera) with 86% of the species list completed (Ávalos-Hernández et al. 2014; Ávalos-Hernández 2016) followed by the spiders (Arachnida: Araneae) with 64% of its fauna recorded (Bizuet et al. 2015). These studies emphasize the increase in new records in the CCB, Coahuila and Mexico, as well as the description of new species (González-Soriano et al. 2012; Ávalos- Hernández et al. 2014; González-Soriano and Novelo-Gutiérrez 2014; Bizuet et al. 2015; Ortega 2015; Ortega-Salas and González-Soriano 2015; ÁvalosHernández 2016), as a consequence of the poor knowledge we have of northern Mexico. Diversity results show that the species richness of these groups of Arthropoda is higher in the CCB than in other sites with desert environments, like the Sonora Desert of the southern USA which forms part of the CD (González-Soriano et al. 2012; Ávalos-Hernández et al. 2014; González-Soriano and Novelo-Gutiérrez 2014; Bizuet et al. 2015; Ortega 2015; Ortega-Salas and González-Soriano 2015; Ávalos- Hernández 2016). All this makes of the CCB a diversity hotspot within the Nearctic region. At a smaller scale, Churince and Rancho PRONATURA were the most similar localities, even when they are separated by the San Marcos and Pinos Mountain Range; this shows the homogeneity of the environment at the same altitude interval, with the presence of aquatic and semiaquatic habitats around the ponds and halophyte and gypsum habitats in between the ponds. Even if Churince has sotol and gypsum dunes, few species were associated with these habitats, so the effect of these habitats in the similarity analyses is not relevant. On the other hand, Rancho PRONATURA is closer to Rancho Orozco and Antiguos Mineros, but the habitat separating these localities is xeric shrub, which probably limits the exchange of species adapted to more humid habitats and with limited flying capabilities. Río Cañón is the only site outside the Conservation Area and the CCB, located to the north, between La Madera and La Menchaca Mountain Ranges. The spatial distance is reflected in the species composition differences (≈50%) with the other
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localities, a well-known pattern of decaying similarity as distance increases (Calderón et al. 2012). As distances get larger, species interchange decreases because the sites become independent units (Calderón et al. 2012). Other ecological factors, as habitat fragmentation or disturbance, can have an effect on the similarity between two communities (Fagua et al. 1999). Consistent with this idea, Río Cañón presents high levels of disturbance. Species richness and abundance were higher in the rainy than in the dry season. This seasonal pattern is cited by several authors for this and other flower-visiting insect groups, even in sites with distinct habitats from those present in the CCB, such as the cloud or rainforest (Vargas et al. 1992, 1999; Hernández 2005; Hernández-Mejía et al. 2008; Arellano 2013). Temperature and rainfall affect species richness, abundance, and the diversity of each feeding guild. The highest diversity and abundance were recorded in the rainy season, when resource availability and quality are higher (Hernández 2005; Hernández-Mejía et al. 2008). During the hot dry season, richness of fruit feeding and nectarivorous species was higher. Apparently, mud-puddling diversity is low, but abundance is high; the wet-sand resource is not restricted to a specific season, due to the presence of permanent ponds throughout the year and the soil characteristics, a combination that is unique of the CCB. The most used resource by the butterflies of the CCB is nectar and flowers. This is a pattern reported by other authors for butterflies in other environments, which highlights the importance of these insects as pollinators (Vargas et al. 1992, 1999; Hernández 2005; Hernández-Mejía et al. 2008; Arellano 2013) and of flowers as the main resource of the CCB for butterflies, mainly as carbohydrates and water sources (Murphy et al. 1983; Karlsson 1994, 1995). The CCB is located in the Altiplano Mexicano province in the Nearctic region (Halffter 1976; Morrone et al. 2002); this is congruent with the biogeographical affinity of the species collected in this study; however, it also has a great neotropical component. Geographic distribution is determined by ecological factors and historical events but is difficult to distinguish the influence of each. The preliminary approach presented here gives valuable information about the role of the CCB on the butterfly’s biology and distribution. This is the first systematic study on Papilionoidea sensu lato in the CCB and Coahuila and one of the few made in the CD (Fig. 7.5). With more data, diversity in Coahuila and endemism in the CCB are expected to increase due to the large area it represents and its degree of isolation. Acknowledgements Support for fieldwork was provided by grants from CONABIO (JF065) to A. Nieto, from resources of the WWF-Alianza Carlos Slim (L039) and the Theodore Roosevelt Memorial Fund (American Museum of Natural History) provided to M. Trujano-Ortega and U. García-Vázquez. We thank E. Austria, A. Contreras, H. Ortega, PRONATURA A. C., DESUVALLE A.C., and CONANP for their assistance in the fieldwork. We thank C. Mayorga (CNIN-IBUNAM) for allowing access to the collections under their care.
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Fig. 7.5 Papilionoidea of Cuatro Ciénegas Basin: (a). Anaea aidea (Guérin-Méneville), (b). Abaeis niccipe (Cramer), (c). Atlides halesus (Cramer) y, (d). Danaus plexippus plexippus (Linnaeus)
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Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Ser B 345:101–118 Contreras BS (1977) Memoria del primer Congreso Nacional de Zoología, Chapingo. México, pp 106–110 Contreras BS (1984) Environmental impacts in Cuatro Cienegas, Coahuila, Mexico: a commentary. In: Marsh PC (ed) Biota of Cuatro Cienegas, Coahuila, Mexico proceedings of a special symposium. Fourteenth annual meeting, Desert Fish Council, Tempe, Arizona USA 1983. J Ariz-Nev Acad Sci 19:85–88 Contreras BAJ, Warren AD (2006) Cercyonis pegala texana (Lepidoptera: Nymphalidae: Satyrinae): new record from the state of Coahuila, Mexico. Southwest Nat 51:552–553 Espeland M, Hall JP, DeVries PJ, Lees DC, Cornwall M, Hsu YF, Wu LW, Campbell DL, Talavera G, Vila R, Salzman S (2015) Ancient Neotropical origin and recent recolonisation: phylogeny, biogeography and diversification of the Riodinidae (Lepidoptera: Papilionoidea). Mol Phylogenet Evol 93:296–306 Fagua G, Amarillo A, Andrade CG (1999) Las mariposas (Lepidoptera: Rhopalocera) como indicadores del grado de intervención en la cuenca del Río Pato (Caquetá, Colombia). In: Andrade MG, Amat G, Fernández F (eds) Insectos de Colombia. Estudios escogidos. Academia Colombiana de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Colombia, Bogotá, Colombia, pp 285–315 García E (1964) Modificaciones al sistema de clasificación climática de Köppen (para adaptarlo a las condiciones de la República Mexicana) Offset Larios. México DF, pp 1–71 González-Soriano E, Novelo-Gutiérrez R (2014) Biodiversidad de Odonata en México. Rev Mex Biodivers 85:243–251 González-Soriano E, Trujano-Ortega M, Contreras-Arquieta A, García-Vásquez UO (2012) New records of Libellula pulchella (Odonata: Libellulidae) and Phyllogomphoides albrighti (Odonata: Gomphidae) from the Cuatro Ciénegas Basin, Coahuila, Mexico. Rev Mex Biodivers 83:847–849 Grishin NV, Durden CJ (2012) New bromeliad-feeding Strymon species from Big Bend National Park, Texas USA and its vicinity (Lycaenidae: Theclinae). J Lepidopt Soc 66:81–110 Halffter G (1976) Distribución de los insectos en la Zona de Transición Mexicana. Fol Entomol Mex 35:1–64 Hernández MBC (2005) Composición y gremios alimentarios de mariposas diurnas de la Superfamilia Papilionoidea (Insecta: Lepidoptera) en el Municipio de Malinalco, Estado de México. Tesis de Licenciatura, Universidad Autónoma del Estado de México, Toluca, 99 pp Hernández-Mejía C, Llorente-Bousquets J, Vargas-Fernández I, Luis-Martínez A (2008) Las mariposas (Hesperioidea y Papilionoidea) de Malinalco, Estado de México. Rev Mex Biodivers 79:117–130 Hoffmann CC (1940) Catálogo sistemático y zoogeográfico de los lepidópteros mexicanos, primera parte. Papilionoidea. An Inst Biol Univ Nac Auton Mex 11:730–739 Instituto Nacional de Ecología (INE) (1999) Programa de Manejo del Área de Protección de Flora y Fauna Cuatro Ciénegas, México. Unidad de Participación Social, Enlace y Comunicación, 167 pp Jiménez-Valverde A, Hortal J (2003) Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Rev Iber Aracnol 8:151–161 Karlsson B (1994) Feeding habits and change of body composition whit age in three nymphalid butterfly species. Oikos 69:224–230 Karlsson B (1995) Resource allocation and mating systems in butterflies. Evol 49:955–961 Llorente J, Luis A, Vargas I (2006) Apéndice General De Papilionoidea: Lista Sistemática, Distribución Estatal y Provincias Biogeográficas. In: Morrone J, Llorente J (eds) Componentes Bióticos Principales de la Entomofauna Mexicana. Las Prensas de Ciencias, UNAM, México DF, pp 945–1009 Llorente J, Vargas I, Luis A, Trujano M, Hernández BC, Warren AD (2014) Biodiversidad de Lepidoptera en México. Rev Mex Biodivers 85:353–371
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Chapter 8
Diversity and Resource Use Patterns of Bees and Flies that Visit Flowers in the Cuatro Ciénegas Basin Omar Ávalos-Hernández, Marysol Trujano-Ortega, Uri Omar García-Vázquez, and Olivia Yánez-Ordóñez
Abstract We analyse the spatio-temporal diversity patterns of five families of bees (Andrenidae, Apidae, Colletidae, Halictidae and Megachilidae) and two families of flower-visiting flies (Bombyliidae and Syrphidae) in the Cuatro Ciénegas Basin (CCB). Pollination by insects is one of the most important ecological processes in an ecosystem, maintaining plant populations and crop production. Knowing the diversity and resource use patterns of pollinators allows the design of conservation and management strategies. We collected 2310 specimens of 169 species of the 7 families of insects; 1331 plant-insect interactions were recorded in which 39 plant species were involved. We compared the insect diversity and plants visited of four localities within the CCB, considering species diversity of the plants visited by each group of insects by season and locality. More plant species were visited during the rainy season, but three insect families were richer during the dry season. Bombyliidae was the family with more flower visits recorded (426), but Apidae (particularly Apis mellifera) was the group that visited more plant species (Apidae 31 spp., A. mellifera 20 spp.). The abundance of Bombyliidae and the diversity of plants visited by Syrphidae, Megachilidae and Halictidae increases the relevance as pollinators of these groups. We identified the plant species more frequently visited in both seasons. Finally, we discuss how this knowledge can be applied in pollinator conservation strategies specifically in the CCB. Keywords Apoidea · Syrphidae · Bombyliidae · Pollinators · Community structure O. Ávalos-Hernández (*) · M. Trujano-Ortega · O. Yánez-Ordóñez Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico e-mail: [email protected] U. O. García-Vázquez Laboratorio de Sistemática Molecular, Unidad de Investigación Multidisciplinaria de Investigación Experimental Zaragoza, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México, Ciudad de México, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_8
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8.1 Introduction Insects, especially bees, flies and butterflies, are the main pollinators of more than 80% of wild plants and crops (Ollerton et al. 2011). Recently, intensive farming, climate change, invasive species and diseases are reducing the number of pollinator insects (Vanbergen and the Insect Pollinators Initiative 2013). The consequences of this reduction or disappearance of pollinators are not clear. First, the commercial value of pollinator services is not easy to estimate and may be overestimated. This is because crop production does not depend exclusively on pollination. Also, crops pollinated by insects are costly in the stock market, but crops that sustain human populations (corn, rice, wheat) are auto pollinated (Allsopp et al. 2008). Besides its commercial value, pollination by insects is important for wild plants and to sustain plant communities. However, A. mellifera has been introduced in almost all habitats, and together with other generalists, they pollinate most plants (Thomson 2004). Then, how important is maintaining the diversity of pollinator insects? Species and functional diversity of pollinators are the most important factors maintaining plant diversity and crop production (Hoem et al. 2008). Especially in xeric habitats, like the CCB, specialist bees are more diverse and abundant than generalist ones (Minckley et al. 2000; Vergara and Badano 2009). These specialists are more affected by disturbance and land-use changes (Vanbergen and the Insect Pollinators Initiative 2013). Even if A. mellifera could partially substitute native pollinators, this species does not visit all crops (e.g. alfalfa), and pollinators of other crops are not known (Goulson 2003). Also, A. mellifera is not as efficient as other bees (Vergara and Badano 2009). Therefore, diversity of native pollinators and how they use floral resources is relevant in natural resource management. Functional diversity, which is very important, increases with taxonomic diversity (Córdova-Tapia and Zambrano 2015). Taxonomic diversity of pollinators comprise several orders of insects. Bees are considered the most important pollinators, being the main pollen carriers. However, flies have an important role in pollination, making up to 66% of the abundance and 67% of the diversity of flower visitors (Orford et al. 2015). The importance of flies as pollinators has been recognized for some time now (Kearns 2001). However, there is no research on monitoring pollinator flies, regarding their populations and patterns. Therefore, nothing is known about the health of their populations, the effect of human activities on them or their conservation. The diversity of bees and pollinator flies is higher in xeric regions than in tropical wet regions; and the Chihuahuan Desert (CD), where the CCB is located, is an arid region with an exceptionally high diversity of these groups (Hull 1973; Minckley and Ascher 2013). In the latter study, the authors surveyed bee communities in the CD of Arizona. They recorded 540 species in 6 sites, with a mean of 134 species by site; most of these species were specialists and endemic. This agrees with Nabhan et al. (2015) who found 104 species visiting Asclepias L. in the Southeastern USA and Northern Mexico. Meanwhile, McAlister (2012) reported the abundance of bees (643), flies (253) and wasps (251) in a region of Texas part of the CD. To date,
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nothing has been published on these groups of insects from the Mexican portion of the CD. But the diversity found in the USA suggests a high diversity of bees in this part of Mexico. The high diversity combined with the particular environments and geological history of the CCB (Souza et al. 2006; Moreno-Letelier et al. 2012) compels the study of these groups in the region. We present an analysis of the diversity of five bees (Andrenidae, Apidae, Colletidae, Halictidae and Megachilidae) and two fly (Bombyliidae and Syrphidae) families in the CCB. Also, we analyse the flower resource use patterns of each group. We compare the patterns of each family to identify the most active flower visitors and potentially the most important pollinators. Finally, we suggest how the data can be used in conservation programmes of these insects.
8.2 Materials and Methods 8.2.1 Sampling Sites Four sampling sites were selected in the CCB: Churince, Orozco, Pozas Azules and Antiguos Mineros (Fig. 8.1). All sites have a similar vegetation type with aquatic and semiaquatic species near the ponds and a mixture of mezquital and halophile
Fig. 8.1 Map showing the study sites in the Cuatro Ciénegas Basin, Coahuila, Mexico
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vegetation between ponds; Churince also presents gypsum dunes. The altitudinal range is small from 713 m asl in Antiguos Mineros to 768 m asl in Churince. The shortest distances between sites are 4.5 km between Antiguos Mineros and Pozas Azules and 6 km between Churince and Orozco. Churince and Orozco are separated by Sierra de San Marcos and Pinos. Also, between Pozas Azules and Antiguos Mineros, the habitat is xeric shrubland, very different from habitats present in both sites; therefore, each of the four sites can be considered as an independent unit, with low or null faunal exchange among them.
8.2.2 Fieldwork Bees and flies were collected in 2012 and 2013 to sum 35 sampling days distributed in the four sites. During fieldwork, all bees and Syrphidae and Bombyliidae flies were collected with an aerial net from 10:00 to 15:00 hours. The plant species visited by each specimen were recorded. All insects were collected and prepared for posterior identification.
8.2.3 Taxonomic Determination Insects were identified with specialized keys for Apoidea (Michener 2000), Bombyliidae (Hall 1981) and Syrphidae (Vockeroth and Thompson 1981). Plants were determined by expert taxonomists: Gabriel Flores curator of HUMO-UAEM and Ramiro Cruz of FCME-UNAM.
8.2.4 Data Analysis Samples were grouped by site and by season. The rainy season was considered from June to November and the dry season from December to May (García 2003). Species richness was estimated for each family of insects and for plants visited by site and by season. The non-parametric estimator Chao 1 was used for species richness estimation (Colwell and Coddington 1994) with the software SPADE (Chao and Shen 2010). Confidence intervals (95%) of estimations were calculated using a bootstrap technique. Spatio-temporal patterns of species richness of insects and plants visited were recognized by comparing estimations between sites and seasons for each taxonomic group. A principal component analysis was calculated using visit frequency by family in both seasons as ordination variables. Visit frequency data were log- transformed to reduce the effect of abundant species on the analysis. The ordination diagram shows the variation in the composition of plant species visited and the frequency of visits by each family. Also, seasons were included in the diagram as
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categorical variables, showing the differences in the composition of plant species visited in each season.
8.3 Results A total of 2310 specimens belonging to 169 species of insects were collected from 7 families. Bombyliidae was the most abundant (1080 records, 46%) and diverse (70 species, 41%) family. However, Apis mellifera with 213 specimens was the most abundant species, while Copestylum (Syrphidae) was the genera with more species (10). Species richness estimations show that Bombyliidae is significantly richer than other families except for Apidae and Syrphidae, which have similar richness (Fig. 8.2). Because of the proportion of rare species, the estimates suggest a potentially high species richness of Apidae and Syrphidae. Churince was the site with higher abundance with 847 records of insects (37%), followed by Orozco with 720 records (31%). Diversity did not differ significantly among localities (Fig. 8.3). Therefore, no bias for the abundance or diversity spatial distribution was evident, although Pozas Azules presented a lower bee/flies ratio than other sites, where bees and flies were more or less equally diverse. Regarding flower visits, 1331 plant-insect interactions were recorded in which 39 plant species were involved. Bombyliidae and Apidae participated in 63% of the 120 110 100 Estimated species richness
90 80 70 60 50 40 30 20 10 0 Andrenidae
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Colletidae
Halictidae
Megachilidae
Bombyliidae Syrphidae
Insect species - Rainy season
Insect species - Dry season
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Fig. 8.2 Species richness of insects and plants visited by each family in each season
Estimated species richness
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Pozas Azules
Fig. 8.3 Species richness of insects and plants visited by both orders in each site
interactions, 426 and 417 interactions, respectively. Bombyliidae, Apidae and Syrphidae visited more plant species than Andrenidae and Colletidae (Fig. 8.2). Apis mellifera was the insect species with most visits (198) and plant species visited (20). The diversity of plants visited in each site was similar, except in Pozas Azules where it was lower (Fig. 8.3). Also, according to the estimations, bees visit more plant species than flies at all sites. Species richness of insects can be divided into two temporal patterns; firstly, Andrenidae, Apidae and Colletidae are more diverse during the rainy season; the other four families show a similar species richness in both seasons (Fig. 8.2). Meanwhile, species richness of plants visited is higher in the rainy season (31 species) than in the dry season (20 species). Five families visit more species during the rainy season, while two others do not follow this pattern. Andrenidae, although it is more diverse in the rainy season, visit more plant species in the dry season; and Syrphidae, with a higher species richness in the dry season, visit more plant species in this part of the year. Even if Bombyliidae is the most species-rich family, Apidae visit more plant species (36) (Fig. 8.2). This family visited significantly more species than Andrenidae, Colletidae and Megachilidae, but, according to estimations and confidence intervals, the same number of species of Halictidae, Bombyliidae and Syrphidae. The principal component analysis included species composition and visit frequency; therefore, visitation patterns of each family are represented in the diagram
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Isocoma plurifolia
Cirsium coahuilense
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Petalonyx crenatus
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Aster subulatus
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Nama cuatrocienegensis Samolus abracteatus coahuilensis
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Fig. 8.4 Principal component analysis of plant species visited. Taxa point marks the mean value of plants visited by that family. Season markers show the mean value of plants visited in that season. Data of the 10 most visited plants are shown
(Fig. 8.4). Five families showed a similar visitation pattern, especially Halictidae and Megachilidae. Apidae and Bombyliidae got separated from the rest, visiting different plant species and at a higher frequency. Apidae, Halictidae, Megachilidae and Syrphidae showed a slight bias towards rainy season plants, contrary to Andrenidae which preferred dry season plants; Colletidae and Bombyliidae did not show any bias. Plant species visited were separated into two groups, according to
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the season in which they were visited. In the rainy season, Isocoma pluriflora was the most visited species, although Cirsium coahuilense and Cevallia sinuata were also visited frequently in this season. In the dry season, Nama cuatrocienegensis dominated the visit records, followed by Samolus ebracteatus coahuilensis and Prosopis glandulosa; these two were visited almost at the same frequency. Within the 10 most visited plant species, only Euphorbia astyla was visited at the same frequency in both seasons. Noteworthy, dominant plants in the rainy season were visited by Apidae and Bombyliidae at the same frequency or slightly more visited by Apidae, but all dominant plants in the dry season were visited more frequently by Bombyliidae than by Apidae.
8.4 Discussion Temporal diversity patterns are different among families; this modifies the relevance of each family as pollinators. While both fly families are equally rich or richer in species in the dry season, all bee families present more species in the rainy season. The diversity and abundance of flies during the dry season indicate a potential higher visit frequency to flowers and a more important role in pollination in this season than bees. Further, Apidae and Bombyliidae visit with the same frequency the dominant plant species in the rainy season (Isocoma pluriflora, Cirsium coahuilense and Cevallia sinuata), but Bombyliidae visits at a higher frequency the dominant plant species in dry season, especially Nama cuatrocienegensis (Fig. 8.4). If Bombyliidae are abundant flower visitors, even if they are not as efficient pollen transporters, they contribute to pollination equally than efficient but less frequent pollinators (Cane et al. 2005). The high diversity of Bombyliidae makes them important pollinators in the dry season. Diversity patterns also show that less rich families are important pollinators because they visit relatively more plant species than richer families. Syrphidae, Megachilidae (Fig. 8.5) and Halictidae, with fewer species, visit the same number of plant species as Bombyliidae and Apidae (Fig. 8.2). In this regard, Minckley et al. (2003) reported that A. mellifera does not visit all available flowers, only the more abundant ones and of the best quality. For example, Golubov et al. (1999) found that Mesquite, arguably the most important species in the maintenance of the CD ecosystem, is more visited by Colletes (Colletidae) and Ashmeadiella (Megachilidae) than by Apis. The plant species discrimination by A. mellifera has two consequences: first native species are as important as A. mellifera as they visit flowers that Apis ignores (Ollerton et al. 2012) and second, the effect of A. mellifera as alien species on native species of pollinators and plants changes with each species, especially with their specialization degree. Spatial diversity patterns found in the CCB show that species richness and bee/ flies ratios are constant across sites. Plant species visited at each site are also similar. Churince and Orozco present each 61% of the observed species of insects, while Antiguos Mineros and Pozas Azules have 48 and 50% of the species. This implies a
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Fig. 8.5 Some bees and flies that visit flowers in the Cuatro Ciénegas Basin: (a) Geron sp. (Bombyliidae), (b) Exoprosopa sp. (Bombyliidae), (c) Megachile sp. (Megachilidae), (d) Copestylum marginatum (Syrphidae)
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high beta diversity, also found in the Larrea tridentata insect visitors in the CD of Arizona (Cane et al. 2005). High beta diversities are common in deserts where low resource availability prevents species coexistence (Kelt et al. 1996), producing a species replacement at all spatial scales (Minckley et al. 1999). In the CCB, ponds may serve as shelters maintaining their own associated communities, somehow independent from other ponds, therefore increasing beta diversity. Regarding temporal patterns, Martínez-Falcon et al. (2011) reported a higher diversity of Copestylum (Syrphidae) larvae in the rainy season in Metztitlan in central Mexico; however, in the CCB, we found the opposite pattern being more diverse in the dry season. This suggests that flowers, which are the main resource for adults of these flies, are not limiting in the dry season. Pollinator diversity and resource use patterns presented here provide useful data for conservation strategies of pollinator populations in the CCB. Conservation of pollinators generally involves maintenance of wildflowers in crops, shrub walls and reduced pesticide use in crop edges (Goulson 2003). Flowers are necessary for these insects; however, pollinator insects also need shelter, nesting sites and water (Wood et al. 2015). In dry habitats, Apis is associated with water (Minckley et al. 2003). In the CCB ponds are an important source of clean water and must be considered as an important resource maintaining pollinator communities, as well as other communities. Also, not all flowers attract pollinators in the same abundance or diversity. It has been demonstrated that habitats and even organic crops with high abundance but low diversity of flowers present a low diversity of pollinator insects (Wood et al. 2015); even at a smaller scale, pollinators prefer diversity over abundance when selecting flower patches (Jha and Kremen 2013). This means that the mere presence of flowers does not guarantee maintaining pollinator communities and the taxonomic composition of the flowers matters. In the CCB the plant species that are preferred by pollinators are Isocoma pluriflora, Cirsium coahuilense, Cevallia sinuata, Nama cuatrocienegensis, Samolus ebracteatus coahuilensis and Prosopis glandulosa; these are the species suitable for pollinator insects conservation. However, because of the differences between seasons, conservation of pollinators along the year must include plants preferred by these insects during the dry and rainy seasons. Also, as flies are important pollinators in the region, plant species used for conservation must include those visited by bees and flies, contrary to the most common strategy of keeping flowers only visited by Apis, Bombus or the most abundant insect species, which are generally invasive species (Wood et al. 2015). This is a first approach to the study of the pollinator insect communities in the CCB. Long-term studies must be conducted in order to recognize temporal patterns at larger scales. In other arid habitats of the CD, pollinators insects have shown great interannual variations (Cane et al. 2005). In this regard, forthcoming faunistic or ecological studies on these communities should focus their sampling effort on the most diverse insects and most visited plants presented here. Chacoff et al. (2012) found that this sampling strategy works better than standardized sampling for recording most of the plant-insect interactions in a system. Finally, the potential pollination importance of flies and most frequent visitors proposed here should be confirmed with pollen transport and deposition measures or with evaluation of the quantity and quality of seeds produced by visit.
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Acknowledgments We thank A. Arellano, A. Contreras, J. Hernández, H. Ortega, E. Austria, PRONATURA A.C., DESUVALLE A.C. and CONANP for their assistance in the fieldwork. We also thank H. Brailovsky, A. Zaldívar and C. Mayorga for allowing access to the CNIN-IBUNAM and J. Llorente and A. Luis from the MZFC-UNAM for their assistance and for providing part of the collecting and preparation material. Plants were identified by Gabriel Flores curator of the HUMO-UAEM and Ramiro Cruz of the FCME-UNAM. We thank the Posgrado en Ciencias Biológicas UNAM for its support. Support for field work was provided by grants from CONABIO (JF065) to A. Nieto, from CONACyT to OAH (CVU 226224), from Memorial Fund (American Museum of Natural History) to MTO and UGV and from resources of the WWF-Alianza Carlos Slim (L039).
References Allsopp MH, de Lange WJ, Veldtman R (2008) Valuing insect pollination services with cost of replacement. PLoS One 3(9):e3128 Cane JH, Minckley R, Kervin L et al (2005) Temporally persistent patterns of incidence and abundance in a pollinator guild at annual and decadal scales: the bees of Larrea tridentata. Biol J Linn Soc 85:319–329 Chacoff NP, Vázquez DP, Lomáscolo SB et al (2012) Evaluating sampling completeness in a desert plant-pollinator network. J Anim Ecol 81:190–200 Chao A, Shen TJ (2010) Program SPADE (Species Prediction and Diversity Estimation). User guide. (http://chao.stat.nthu.edu.tw) Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Phil Trans R Soc B 345:101–118 Córdova-Tapia F, Zambrano L (2015) La diversidad funcional en la ecología de comunidades. Ecosistemas 24:78–87 García E (2003) Distribución de la precipitación en la República Mexicana. Investigaciones Geográficas. Bol Inst Geog UNAM 50:67–76 Golubov J, Eguiarte LE, Mandujano MC et al (1999) Why be a honeyless honey mesquite? Reproduction and mating system of nectarful and nectarless individuals. Am J Bot 86:955–963 Goulson D (2003) Conserving wild bees for crop pollination. J Food Agric Environ 1:142–144 Hall JC (1981) Bombyliidae. In: McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) Manual of Nearctic Diptera, Monograph 27, vol 1. Research Branch, Agriculture Canada Ottawa Canada, Ottawa, pp 589–602 Hoem P, Tscharntke T, Tylianakis JM et al (2008) Functional group diversity of bee pollinators increases crop yield. Proc Royal Soc B 275:2283–2291 Hull FM (1973) Bee flies of the world. The genera of the family Bombyliidae. Smithsonian Institution Press, Washington, DC, p 687 Jha S, Kremen C (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. PNAS 110:555–558 Kearns CA (2001) North American dipteran pollinators: assessing their value and conservation status. Conserv Ecol 5:5 Kelt D, Brown JH, Heske EJ et al (1996) Community structure of desert small mammals: comparisons across four continents. Ecology 77:746–761 Martínez-Falcón AP, Marcos-García MA, Moreno CE (2011) Temporal shifts and niche overlapping in Copestylum (Diptera, Syrphidae) communities reared in cactus species in a central Mexican scrubland. Ecol Res 26:341–350 McAlister CG (2012) An insect pollinator survey at the Chihuahuan Desert Institute (CDRI), Jeff Davis County, Texas, and a comparison of the native bee diversity of the CDRI’s botanical gardens to the surrounding grasslands using pan traps. Thesis Master of Science Degree. School of Arts and Sciences Sul Ross State University
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Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore, p 913 Minckley RL, Cane JH, Kervin L, Roulston TH (1999) Spatial predictability and resource specialization of bees (Hymenoptera: Apoidea) at a superabundant, widespread resource. Biol J Linn Soc 67:119–147 Minckley RL, Cane JH, Kervin L (2000) Origins and ecological consequences of pollen specialization among desert bees. Proc Royal Soc Lond B 267:265–271 Minckley RL, Cane JH, Kervin L et al (2003) Biological impediments to measures of competition among introduced honey bees and desert bees (Hymenoptera: Apiformes). J Kans Entomol Soc 76:306–319 Minckley RL, Archer JS (2013) Preliminary survey of bee (Hymenoptera: Anthophila) richness in the northwestern Chihuahuan Desert. In: Gottfried GJ, Ffolliott PF, Gebow BS, Eskew LG, Collins LC (comps). Merging science and management in a rapidly changing world: Biodiversity and management of the Madrean Archipelago III; 2012 May 1–5; Tucson, AZ. Proceedings. RMRS-P-67, U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins, CO, pp 138–143 Moreno-Letelier A, Olmedo-Álvarez G, Eguiarte LE et al (2012) Divergence and phylogeny of Firmicutes from Cuatro Ciénegas Basin, Mexico: A window to an ancient ocean. Astrobiology 12:674–684 Nabhan GP, Buckley S, Dial H (2015) Pollinator Plants of the Desert Southwest: Native Milkweeds (Asclepias spp.). USDA-Natural Resources Conservation Service, Tucson Plant Materials Center, Tucson, AZ. TN-PM-16-1-AZ Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326 Ollerton J, Price V, Armbruster WS et al (2012) Overplaying the role of honey bees as pollinators: a comment on Aebi and Neumann (2011). Trends Ecol Evol 27:141–142 Orford KA, Vaughan IP, Memmott J (2015) The forgotten flies: the importance of non-syrphid Diptera as pollinators. Proc Royal Soc B 282:2014–2034 Souza V, Espinosa-Asuar L, Escalante AE et al (2006) An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert. PNAS 103:6565–6570 Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85:458–470 Vanbergen AJ, the Insect Pollinator Initiative (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259 Vergara CH, Badano EI (2009) Pollinator diversity increases fruit production in Mexican coffee plantations: The importance of rustic management systems. Agric Ecosys Environ 129:117–123 Vockeroth JR, Thompson FC (1981) Syrphidae. In: JF MA, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) Manual of Nearctic Diptera, Monograph 27, vol 1. Research Branch, Agriculture Canada, Ottawa, pp 713–743 Wood TJ, Holland JM, Goulson D (2015) Pollinator-friendly management does not increase the diversity of farmland bees and wasps. Biol Conserv 187:120–126
Chapter 9
Odonata of the Cuatro Ciénegas Basin Héctor Ortega-Salas and Enrique González-Soriano
Abstract A summary of the present knowledge on the diversity of Odonata occurring in the Cuatro Ciénegas Basin (CCB) is presented. The work is based on published records, and the results from samplings are carried out between the years 2009 and 2013 in 23 sites. A list of the 67 Odonata species from the CCB is provided including 19 new state records. Finally, the biogeographic affinities, conservation status, and major threats are discussed. Keywords Odonata · Mexico · Diversity · New records
9.1 Introduction The order Odonata is regarded as a monophyletic group; it comprises three suborders: Zygoptera or damselflies, Anisoptera or true dragonflies and a small suborder Anisozygoptera with four species (Suhling et al. 2015). Odonata has a tropical origin (Corbet 1999), and today the highest diversity is found near the equatorial areas (Paulson 2006). Larvae are aquatic inhabiting freshwater habitats with some species occurring in saline waters and only a few with terrestrial habits. Both larvae and adults are predatory. They are top predators of macroinvertebrates in freshwater ecosystems. Adults are easily recognizable by having a stylized body, divided into the head, thorax, and abdomen. Their compound eyes are large and multifaceted and often occupy most of the head. The thorax consists of a small, mobile prothorax,
H. Ortega-Salas (*) Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Ciudad de México, Mexico e-mail: [email protected] E. González-Soriano Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico e-mail: [email protected] © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_9
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and a larger pterothorax where the wings are inserted. The four wings are elongated, membranous, and reticulated. The legs are relatively long and are adapted to perch and capture their prey. The abdomen is long and thin and has ten visible segments (Corbet 1999). Odonates, being elegant and iconic, are high-profile insects. Since they are associated with a scarce resource (freshwater) and are sensitive to landscape alterations and climate change, they play an important role in conservation biology thinking (Samways 2008). Odonates are increasingly used as bioindicators in the assessment of health status of freshwater bodies and their ecological integrity (Bulánková 1997; Oertli 2008; Simaika and Samways 2008).
9.2 Diversity The continental water bodies cover less than 1% of the earth’s surface; however, they harbour 10% of the known animal diversity, of which 60% is composed by aquatic insects, although there are those who estimate that it could well constitute up to 80% of the aquatic animal diversity (Dijkstra et al. 2014). Aquatic insects are grouped into 12 orders, although most of them have only a small proportion of aquatic species. Within the fully aquatic orders, Odonata is the second largest with over 6280 species described until 2018 (Schorr and Paulson 2018). Since 2014, the number of species recorded in Mexico rose from 355 (González-Soriano and Novelo-Gutiérrez 2014) to 360 species (Paulson and González-Soriano 2018), representing 5.7% of the world’s total odonate diversity. Of these species, 49 are considered endemic, which is equivalent to 13% of the species present in the country. In Mexico, very few studies on the biology of Odonata have been carried out in the Nearctic portion of the country, and, besides the study conducted by González- Soriano and Novelo-Gutiérrez (1991), no other taxonomic study has been done in the region. Until very recently, almost nothing was known about the odonate fauna from the northern states. In the last decade, the situation started to change with the publication of a number of studies on this fauna (Behrstock et al. 2004, 2007; Behrstock 2006, 2009; Upson et al. 2007; Bailowitz et al. 2009, 2013, 2015). Coahuila remains one of the least studied states in Mexico. Although it is the third largest state of the country occupying 7.7% of the territory, only 72 species until 2015 had been recorded, making it the 12th state with the least species listed (González-Soriano and Novelo-Gutiérrez 2007, 2014; Behrstock 2009; Ortega- Salas and González-Soriano 2015). The Cuatro Ciénegas Basin (CCB) is one of the most biologically interesting places in North America, due to its great biodiversity and high endemism, for which it has been compared to the Galapagos Islands (Minckley 1969; Souza et al. 2012). The first mention of the odonate from this area was made by Dinger et al. (2005) who collected larvae from 20 sites in the CCB and listed 24 species. Behrstock (2009) listed 65 species for the state, including 19 from the CCB, disregarding the list given by Dinger for “these lists, based entirely on nymphs, are difficult to evalu-
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Fig. 9.1 Libellula coahuiltecana perched at Rancho Orozco, Cuatro Ciénegas Basin
ate, as they contain various taxonomic errors, as well as species unlikely to be found at lower elevations in Chihuahuan Desert habitats, or in Mexico”. Three years later González-Soriano et al. (2012) listed another two species, and finally, Ortega-Salas and González-Soriano (2015) described Libellula coahuiltecana (Fig. 9.1) from material collected in the CCB (Table 9.1). In this work, we provide a list of the 67 Odonata species known from the CCB and Sierra La Madera (Table 9.1), including 19 new state records and 1 new country record (Table 9.2), based on samplings carried out between 2009 and 2013 in 23 sites within the CCB and Sierra La Madera (Fig. 9.2). We also validate 8 of the records previously mentioned by Dinger et al. (2005) increasing the species number of Coahuila to 91. The recorded species belong to 38 genera and 8 families. The family Libellulidae was the richest with 36 species, followed by Coenagrionidae with 18 (Fig. 9.3a, b); Gomphidae (Fig. 9.4a) with 5; Calopterygidae, Lestidae, Aeshnidae, and Corduliidae (Fig. 9.4b) with 2 each; and finally Macromiidae with only 1 species. The richest genus was Argia (Fig. 9.4a) with 11 species, followed by Libellula with 7 and Enallagma, Dythemis, Erythrodiplax, and Tramea with 3 each.
9.3 Biogeography and Conservation The majority of the species present within the CCB are distributed at least in the southern USA and northern Mexico, some even reaching countries in Central and South America. Only Argia mayi and L. coahuiltecana have restricted distributions within Mexico. Since its description in 2015, L. coahuiltecana has not been collected again, so the extent of its distribution outside the CCB is unknown. The species composition in the CCB involves elements of both Nearctic and Neotropical affinity. Forty-three percent of the species (29) are of mainly or exclusive Nearctic affinity, 20% (14) are Neotropical species, and the rest do not have a clear affinity because they are widely distributed in both biogeographic provinces (Table 9.1).
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Table 9.1 List of Odonata species recorded within the Cuatro Ciénegas Basin and Sierra La Madera including the reference of the first record of each species (X), its status in the IUCN Red List (NE not evaluated, LC least concern) and biogeographic affinity (NA, mainly Nearctic; NT, mainly Neotropical; NA-NT, without main affinity) González- Soriano Dinger This et al. Behrstock et al. (2012) study IUCN Affinity (2005) (2009) Zygoptera Lestidae
Archilestes grandis (Rambur, 1842) Lestes alacer Hagen, 1861 Calopterygidae Hetaerina americana (Fabricius, 1798) Hetaerina titia (Drury, 1773) Coenagrionidae Argia fumipennis (Burmeister, 1839) Argia immunda (Hagen, 1861) Argia leonorae Garrison, 1994 Argia mayi González-Soriano, 2012 Argia moesta (Hagen, 1861) Argia nahuana Calvert, 1902 Argia oculata Hagen in Selys, 1865 Argia plana Calvert, 1902 Argia rhoadsi Calvert, 1902 Argia sedula (Hagen, 1861) Argia translata Hagen in Selys, 1865 Enallagma basidens Calvert, 1902 Enallagma civile (Hagen, 1861) Enallagma praevarum Hagen, 1861
X
NE
NA-NT
X
LC
NA-NT
X
LC
NA-NT
X
X
NE
NA-NT
X
X
LC
NA
X
LC
NA
X
LC
NA
X
NE
NT
X
X
LC
NA
X
X
LC
NA
X
NE
NT
X
LC
NA-NT
X
LC
NA
X
LC
NA
X
NE
NA-NT
X
LC
NA
X
LC
NA-NT
X
LC
NA-NT
X
X
X
X
X
X
X
X
X
(continued)
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Table 9.1 (continued)
Ischnura ramburii (Selys, 1850) Nehalennia minuta (Selys in Sagra, 1857) Protoneura cara Calvert, 1903 Telebasis salva (Hagen, 1861) Anisoptera Aeshnidae
Gomphidae
Macromiidae Corduliidae
Libellulidae
González- Soriano Dinger This et al. Behrstock et al. (2012) study IUCN Affinity (2005) (2009) X X LC NA-NT X
Anax junius (Drury, X 1773) Rhionaeschna multicolor (Hagen, 1861) Dromogomphus spoliatus (Hagen in Selys, 1858) Erpetogomphus designatus Hagen in Selys, 1858 Gomphus militaris Hagen in Selys, 1858 Phyllogomphoides albrighti (Needham, 1950) Phyllogomphoides stigmatus (Say, 1839) Macromia annulata X Hagen, 1861 Epitheca petechialis (Muttkowski, 1911) Epitheca princeps Hagen, 1861 Brachymesia furcata (Hagen, 1861) Brechmorhoga mendax (Hagen, 1861) Cannaphila insularis Kirby, 1889
X
X
X
LC
NT
X
LC
NT
X
NE
NA-NT
X
LC
NA-NT
X
LC
NA
X
LC
NA
X
LC
NA
X
LC
NA
X
LC
NA
X
LC
NA
X
LC
NA
X
LC
NA
X
LC
NA
X
LC
NA-NT
X
LC
NA
X
LC
NA-NT
(continued)
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Table 9.1 (continued)
Celithemis eponina (Drury, 1773) Dythemis fugax Hagen, 1861 Dythemis nigrescens Calvert, 1899 Dythemis velox Hagen, 1861 Erythemis simplicicollis (Say, 1839) Erythrodiplax basifusca Calvert, 1895 Erythrodiplax fervida (Erichson, 1848) Erythrodiplax umbrata (Linnaeus, 1758) Idiataphe cubensis (Scudder, 1866) Libellula coahuiltecana Ortega-Salas & González-Soriano, 2015 Libellula comanche Calvert, 1907 Libellula composita (Hagen, 1873) Libellula croceipennis Selys, 1868 Libellula needhami Westfall, 1943 Libellula pulchella Drury, 1773 Libellula saturata Uhler, 1857 Macrodiplax balteata (Hagen, 1861)
González- Soriano Dinger This et al. Behrstock et al. (2012) study IUCN Affinity (2005) (2009) X X NE NA X
LC
NA
X
X
LC
NT
X
X
LC
NA
X
X
LC
NA
X
LC
NA
X
LC
NT
X
LC
NA-NT
X
LC
NT
X
NE
NA
X
LC
NA
X
LC
NA
X
LC
NT
X
LC
NA-NT
X
LC
NA
X
LC
NA-NT
X
NE
NA-NT
X
X
X X X
(continued)
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Table 9.1 (continued) González- Soriano Dinger This et al. Behrstock et al. (2012) study IUCN Affinity (2005) (2009) X LC NT
Macrothemis inacuta Calvert, 1898 Micrathyria aequalis (Hagen, 1861) Orthemis discolor (Burmeister, 1839) Orthemis ferruginea (Fabricius, 1775) X Pachydiplax longipennis (Burmeister, 1839) Paltothemis lineatipes Karsch, 1890 Pantala flavescens (Fabricius, 1798) Pantala hymenaea (Say, 1839) Perithemis tenera (Say, 1839) Plathemis lydia (Drury, 1773) Pseudoleon superbus (Hagen, 1861) Sympetrum corruptum (Hagen, 1861) Tramea insularis Hagen, 1861 Tramea lacerata Hagen, 1861 Tramea onusta Hagen, 1861
X
LC
NT
X
LC
NT
X
LC
NA-NT
X
NE
NA-NT
X
LC
NT
X
LC
NA-NT
X
NE
NA-NT
X
LC
NA
X
LC
NA
X
X
LC
NT
X
X
NE
NA-NT
X
LC
NT
X
NE
NA
X
LC
NA-NT
X
X
Table 9.2 New records of Odonata for Coahuila, Mexico Coenagrionidae
Aeshnidae Gomphidae Corduliidae Libellulidae
Argia leonorae Garrison, 1994 Argia mayi González-Soriano, 2012 Argia oculata Hagen in Selys, 1865 Protoneura cara Calvert, 1903 Rhionaeschna multicolor (Hagen, 1861) Dromogomphus spoliatus (Hagen in Selys, 1858) Gomphus militaris Hagen in Selys, 1858 a Epitheca petechialis (Muttkowski, 1911) Epitheca princeps Hagen, 1861 Brechmorhoga mendax (Hagen, 1861) Dythemis fugax Hagen, 1861 Erythrodiplax fervida (Erichson, 1848) Libellula coahuiltecana Ortega-Salas & González-Soriano, 2015 Libellula croceipennis Selys, 1868 Macrodiplax balteata (Hagen, 1861) Macrothemis inacuta Calvert, 1898 Micrathyria aequalis (Hagen, 1861) Orthemis discolor (Burmeister, 1839) Tramea insularis Hagen, 1861
New country record for Mexico
a
Fig. 9.2 Collecting sites in the CCB and Sierra La Madera. (1) Rancho El Espejo; (2) Rancho La Casita; (3) Ejido El Oso; (4) Río Cañón; (5) Cuatro Ciénegas town; (6) San José del Anteojo; (7) Río Salado de Nadadores; (8) La Poza Azul; (9) Poza Mojarral East; (10) Puente Chiquita; (11) Poza Mojarral West; (12) Río Mezquites, las Palapas; (13) Cueva Minckley; (14) Las Playitas SE shore; (15) Río Garabatal; (16) Los Gatos; (17) Los Hundidos; (18) Poza La Becerra; (19) Rancho Orozco; (20) Churince; (21) Rancho PRONATURA-Pozas Azules; (22) Ejido El Venado; (23) Ejido Antiguos Mineros del Norte
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Fig. 9.3 Damselflies belonging to the family Coenagrionidae in the Cuatro Ciénegas Basin: (a) Argia moesta male and (b) Ischnura ramburii male and female in tandem
Regarding the IUCN Red List, 80% (54) of the species registered in the CCB are evaluated as least concern (LC), and the remaining 13 species have not been evaluated (NE); however, with the exception of Libellula coahuiltaecana (which is only known from three localities within the valley), in all cases they are species of wide distribution, so it is unlikely that they would be placed in a risk category (IUCN 2019). Desert springs, marshes, and rivers are highly vulnerable to anthropogenic disturbance. Water extraction is a primary threat to desert springs, but invasions by non-native species also pose serious threats (Hendrickson et al. 2008). These threats are the main factors of the decline of odonate populations (Suhling et al. 2015) and therefore the main threats to the species that occur in the CCB.
9.4 Discussion The CCB is one of the most odonatological diverse sites in the North American deserts only surpassed in species number by Bitter Lake National Wildlife Refuge in New Mexico (RR Larsen, personal communication). The endemic species
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Fig. 9.4 Dragonflies belonging to the families Corduliidae and Gomphidae in the Cuatro Ciénegas Basin: (a) Epitheca petechialis male and (b) Phyllogomphoides albrighti male
Libellula coahuiltecana, an unexpected recently described species belonging to an apparently well-studied genus, reinforces this statement. However, the area in general is suffering great threats due to water extraction mainly for agricultural use, which has caused the decrease of marshy areas and modified the flood pattern of the valley (INE-SEMARNAP 1999). Furthermore, the construction of drainage infrastructure has interconnected water bodies that were naturally isolated whose effects on the odonate communities are unknown. Research on the conservation status and follow-up of the odonate populations from the CCB could give an insight on the impact that the infrastructure and exploitation of water have on the aquatic species that inhabit the area. Acknowledgements This work was funded by grants from CONABIO (JF065) to A. Nieto and from resources of the WWF-Alianza Carlos Slim (L039) and the Theodore Roosevelt Memorial Fund (American Museum of Natural History) provided to M. Trujano-Ortega and U. García-Vázquez.
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References Bailowitz RA, Danforth D, Deviche P (2009) West Mexico updated. Argia 21:15–18 Bailowitz RA, Danforth D, Upson S (2013) Erpetogomphus molossus, a new species from Sonora, Mexico (Odonata: Anisoptera: Gomphidae). Zootaxa 3734:559–570 Bailowitz RA, Danforth D, Upson S (2015) A Field guide to the Damselflies & Dragonflies of Arizona and Sonora. Nova Granada Publications, Tucson. https://searchworks.stanford.edu/ view/11809907 Behrstock RA (2006) Five new records of Odonata for the state of Tamaulipas, Mexico, including the correction of a previously published Brechmorhoga. Argia 18:17–19 Behrstock RA (2009) An updated list of the Odonata of Coahuila, Mexico, including forty-one new state records and the first Mexican occurrence of Libellula composita (Hagen). Bull Am Odonatol 11:1–7 Behrstock RA, Danforth D, Upson S (2004) Yaqui dancer (Argia carlcooki, Daigle 1995), new distributional records for northern Mexico and the U.S. Argia 16:11–16 Behrstock RA, Danforth D, Upson S (2007) A list of the Odonata of Chihuahua state, Mexico, including new state records and the first Mexican record of Argia alberta, Kennedy, 1918. Bull Am Odonatol 10:52–63 Bulánková E (1997) Dragonflies (Odonata) as bioindicators of environment quality. Biologia, Bratislava 52:177–180 Corbet PS (1999) Dragonflies : behavior and ecology of Odonata. Cornell University Press, Ithaca, United States Dijkstra KDB, Monaghan MT, Pauls SU (2014) Freshwater biodiversity and aquatic insect diversification. Ann Rev Entom 59:143–163 Dinger EC, Cohen AE, Hendrickson D, Marks JC (2005) Aquatic invertebrates of Cuatro Ciénegas, Coahuila, México: natives and exotics. Southwest Nat 50:237–246 González-Soriano E, Novelo-Gutiérrez R (1991) Odonata de la reserva de la biosfera La Michi-lia, Durango, Mexico. Parte I. Imagos. Fol Entomol Mex 81:67–105 González-Soriano E, Novelo-Gutiérrez R (2007) Odonata from México revisited. In: Tyagi BK (ed) Odonata biology of dragonflies. Scientific Publishers, Jodhpur, pp 105–136 González-Soriano E, Novelo-Gutiérrez R (2014) Biodiversidad de Odonata en México. Rev Mex Biodivers 85 (supl:243–251) González-Soriano E, Trujano-Ortega M, Contreras-Arquieta A, García-Vásquez UO (2012) New records of Libellula pulchella (Odonata: Libellulidae) and Phyllogomphoides albrighti (Odonata: Gomphidae) from the Cuatro Ciénegas Basin, Coahuila, Mexico. Rev Mex Biodivers 83:847–849 Hendrickson DA, Marks JC, Moline AB, Dinger E, Cohen AE (2008) Combining ecological research and conservation: a case study in Cuatro Ciénegas, Coahuila, Mexico. In: Stevens LE, Meretsky VJ (eds) Ariland springs in North America: ecology and conservation. The University of Arizona Press, Tucson INE-SEMARNAP (1999) Programa de Manejo del Área de Protección de Flora y Fauna Cuatrociénegas. Instituto Nacional de Ecología, Ciudad de México, 167 pp IUCN (2019) The IUCN Red List of Threatened Species. Version 2018-2. Retrieved January 29, 2019, from www.iucnredlist.org Minckley WL (1969) Environments of the Bolsón of Cuatro Ciénegas, Coahuila, México. With special reference to the aquatic biota. The University of Texas at El Paso: Texas Western Press Oertli B (2008) The use of dragonflies in the assessment and monitoring of aquatic habitats. In: Córdoba-Aguilar A (ed) Dragonflies and damselflies: model organisms for ecological and evolutionary research. Oxford University Press, Oxford, UK, pp 79–95 Ortega-Salas H, González-Soriano E (2015) A new species of Libellula Linnaeus, 1758, from the Cuatro Ciénegas basin, Coahuila, México (Anisoptera: Libellulidae). Zootaxa 4028:589–594
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Paulson DR (2006) The importance of forests to neotropical dragonflies. In: Cordero-Rivera A (ed) Forest and dragonflies: fourth WDA international symposium of odonatology, Pontevedra (Spain), July 2005. Pensoft, Sofia, pp 79–101 Paulson DR, González-Soriano E (2018) Mexican Odonata. Retrieved January 19, 2018, from https:// www.pugetsound.edu/academics/academic-resources/slater-museum/biodiversity-resources/ dragonflies/mexican-odonata/ Samways MJ (2008) Dragonflies as focal organisms in contemporary conservation biology. In: Córdoba-Aguilar A (ed) Dragonflies: model organisms for ecological and evolutionary research. Oxford University Press, Oxford, UK, pp 97–108 Schorr M, Paulson DR (2018) World Odonata list. Retrieved July 7, 2018, from https://www.pugetsound.edu/academics/academic-resources/slater-museum/biodiversity-resources/dragonflies/ world-odonata-list2/ Simaika JP, Samways MJ (2008) Valuing dragonflies as service providers. In: Córdoba-Aguilar A (ed) Dragonflies: model organisms for ecological and evolutionary research. Oxford University Press, Oxford, UK, pp 109–123 Souza V, Siefert JL, Escalante AE, Elser JJ, Eguiarte LE (2012) The Cuatro Ciénegas Basin in Coahuila, Mexico: an astrobiological Precambrian Park. Astrobiology 12:641–647 Suhling F, Sahlén G, Gorb S, Kalkman VJ, Dijkstra KDB, van Tol J (2015) Order Odonata. In: Thorp JH, Rogers DC (eds) Thorp and Covich’s freshwater invertebrates: ecology and general biology: fourth edition, vol 1, 4th edn. Academic Press, London, pp 893–932 Upson S, Danforth D, González-Soriano E, Behrstock RA, Bailowitz RA (2007) A preliminary checklist of the Odonata of Sonora, Mexico. Bull Am Odonatol 10:23–25
Chapter 10
Diversity and Community Structure of Ants in the Cuatro Ciénegas Basin, Coahuila, Mexico Milan Janda, Madai Rosas-Mejía, Pablo Corcuera, Mario Josué Aguilar- Méndez, Miguel Vásquez-Bolaños, and Yuliza Tafoya-Alvarado
Abstract Ants (Hymenoptera: Formicidae) are one of the most conspicuous invertebrates in the arid and semiarid ecosystems. Thanks to their diverse life strategies and high abundance, they take part in many interactions with other plants and animals and can considerably alter the local ecosystem. Here, we surveyed the ant assemblage of Churince in the Cuatro Ciénegas Basin (CCB) for the first time. We describe species diversity, community structure and habitat associations along an environmental gradient between the grasslands and gypsum dunes. The ant fauna in the CCB is typical of semi-desert areas, with several species shared with arid areas of Arizona and Texas. The ant communities are dominated by species from the
M. Janda (*) Laboratorio Nacional de Análisis y Síntesis Ecológica, Escuela Nacional de Estudios Superiores-Morelia, Universidad Nacional Autónoma de México, Michoacán, Mexico Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech Republic e-mail: [email protected] M. Rosas-Mejía Universidad Autónoma de Tamaulipas, Instituto de Ecología Aplicada, Ciudad Victoria, Tamaulipas, Mexico P. Corcuera Laboratorio de Ecología Animal, Departamento de Biología, Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico M. J. Aguilar-Méndez Departamento de Biología, División de Ciencias Naturales y Exactas, Campus Guanajuato, Universidad de Guanajuato, Guanajuato, Guanajuato, Mexico M. Vásquez-Bolaños Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Jalisco, Mexico Y. Tafoya-Alvarado Laboratorio Nacional de Análisis y Síntesis Ecológica, Escuela Nacional de Estudios Superiores-Morelia, Universidad Nacional Autónoma de México, Michoacán, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_10
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genera Crematogaster, Myrmecocystus, Pogonomyrmex and Forelius. The unique environmental settings of the CCB allow the coexistence of several distinct ant communities in a relatively small area. Keywords Hymenoptera · Life strategies · Ant assemblage
10.1 Introduction Ants (Hymenoptera: Formicidae) are among the most conspicuous and abundant insects in subtropical and tropical terrestrial habitats. Thanks to their eusociality and diverse life strategies, they participate in many types of interactions with other organisms and the environment. They are predators, scavengers, and herbivores; and some developed diverse symbiotic relationships. Ants are a conspicuous element in arid and semi-desert habitats across North America. Some of the species have major impact on the communities of plants and animals in these habitats by influencing soil structure and distribution of nutrients, by dispersing and preying on plant seeds, or by exhibiting strong predation pressure. The nest structures of some harvester ants (genus Pogonomyrmex) and fungus-growing ants (genera Acromyrmex, Atta) are often conspicuous structures, visible from large distances which sometimes dominate across arid habitats from the southern USA to southern Mexico. The CCB is located in the Chihuahuan Desert (CD) which is the largest arid region of Mexico. Because of its complex topography and habitat diversity, the whole region harbours a high richness of vertebrate groups including reptiles, amphibians, and birds (Contreras-Balderas et al. 2004; Mendoza-Quijano et al. 2006). The diversity and distribution of the invertebrates are much less known for the region. Although some arthropod groups were studied in the past, including scorpions, thrips, and ants (Sissom and Hendrixson 2006; Williams 1968; Rojas and Fragoso 1999), this vast region is in evident need of more systematic surveys of invertebrates. The distribution and composition of ant assemblages across the CD are still not well documented. There have been several important studies, such as the surveys from the Jornada Basin in the northwest (https://jornada.nmsu.edu/lter/data/species/ants), Mapimi Reserve in the southwest (Rojas and Fragoso 1999), and few others. Several studies from the Sonoran Desert have also provided important insights into the composition of ant assemblages across the arid regions of northern Mexico (Bestelmeyer and Schooley 1999; Wheeler and Wheeler 1973). In the CCB, a high diversity of ground-dwelling spiders was documented (Bizuet-Flores et al. 2015), and selected groups of flies and bees were studied as well (Ávalos-Hernández et al. 2016). However, many other arthropod groups still await investigation. The goal of this study was to (1) survey ant assemblages in the CCB, (2) describe the species richness and community composition, (3) assess their possible associations with various vegetation types, and (4) evaluate the composition of ant fauna in the regional context.
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10.2 Materials and Methods 10.2.1 Study Site The CCB has a unique geological and biological history. The region was isolated from the Atlantic Ocean by the rise of the Sierra Madre Oriental in the Middle Eocene (40 mya). When the ocean withdrew, part of the water remained trapped in the valley (Moreno-Letelier et al. 2012). Today, the subterranean water emerges and forms ponds and streams that distinguish this region from the surrounding desert areas and nearby mountains. The isolation of the valley has also resulted in a high degree of endemism in some vertebrate and invertebrate groups (Souza et al. 2012). Ants were surveyed at the site Churince, located at the western part of the CCB at 780–765 m a.s.l. The whole Churince site extends approximately 2000 ha, and its vegetation has been characterized as gypsophile, halophile, aquatic, and sub-aquatic and desert shrub (Ávalos-Hernández et al. 2016). We recognized five main vegetation associations, here referred to as habitats: (1) Prosopis glandulosa shrubland (Mezquital), (2) Sporobolus spicatus/Distichlis spicata wet grasslands (Tular), (3) Larrea tridentata/Fouquieria splendens desert scrub (Larrea), (4) Dasylirion wheeleri desert scrub (Sotol), and (5) Sporobolus tussocks surrounded by areas of gypsum desert dunes with no vegetation cover (Peladero). The sampling was spread between the hillside of the cordillera limited by Federal Highway 30 at the east and the gypsum dunes site at the west (Fig. 10.1). The sampled area size was 4.3 km (east to west) by 2.5 km (south to north).
Fig. 10.1 Sampled habitats in Cuatro Ciénegas, Coahuila. Lines represent the five pitfall traps transects (T1 to T5), and squares represent the centroid of the square plots (P1 to P7) for the hand collecting method
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10.2.2 Sampling Ants were surveyed between 2011 and 2015. The sampling consisted of two principal approaches: (1) pitfall traps were arranged in five transects in each principal habitat, and (2) seven square plots, placed randomly within all habitats, were actively surveyed for ant colonies using hand collecting and bait traps. In addition to the plot sampling, the locality was directly surveyed for ants outside the plots in 2014 and 2016. The pitfall traps were set in 20 sampling points, distributed in 5 transects across the 5 principal habitats at the site. Each transect contained four sampling points, separated by 100 m. The five traps in each sample unit site were placed in the centre and extreme ends of a 10 × 10 m quadrat. Each trap consisted of a plastic recipient (15 × 23 × 8 cm) with two 6 × 6 cm lateral openings. A triangular aluminium ramp was placed in the lower part of each opening (Bouchard et al. 2000). Each ramp was previously varnished with a sand texture aerosol. Traps contained water and a small quantity of detergent to lower the surface tension, and their content was collected weekly. The traps were exposed from March to May and from September to November 2011 and from January to May and from July to October 2012 (6 months each year). Ants were collected along with other invertebrates and then separated from the sample for follow-up processing. The plots for active collecting were 20 m by 20 m, placed randomly within each main habitat (vegetation) type. At every plot, the ant colonies and foraging individuals were actively searched for between 9 am and 4 pm for 2 person-hours. Every possible microhabitat was surveyed, such as the space under stones, soil, and surface of vegetation. Within each plot, nine bait traps with tuna, honey, and seed mixture were placed and checked after 1 and 2 hours. The specimens were preserved in absolute ethanol for follow-up sorting and identification.
10.2.3 Data Processing and Analysis All specimens were sorted into morphospecies and identified to species or to the lowest possible taxonomic level, using available taxonomic literature and by comparisons with specimens at the University of Guadalajara Ant Collection (curator M. Vasquez Bolaños). High-resolution images for representatives of each species were taken at the Biology Centre, Czech Academy of Sciences, with a Leica APO- 16 imaging system. The species occurrences in pitfall traps for each transect with 4 trap stations (20) were combined for both collecting seasons and collecting years and converted to presence-absence data, for a total of 40 replicates. For the plots with hand collecting and bait traps, we included only the records from hand collecting, as the bait traps did not yield any additional species. The number of colonies/ nest encountered within each plot was used as input data. The occurrence data from the two types of sampling approaches were used separately or combined to calculate
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overview statistics, biodiversity indices, species accumulation curves, and habitat preferences using MS Excel for alpha diversity and EstimateS v. 9.1.0 for beta diversity. Shannon’s diversity index and Shannon’s equitativity index were calculated following Magurran (1988), and the Jaccard index for shared species was calculated following Real and Vargas (1996). We used a correspondence analysis to associate species occurrence with the sampled habitats. The analysis was performed with frequencies without grouping in the Statistica v. 4 and plotted in program Past 3.18 to explore the preferences of the 36 ant species in the 5 habitats.
10.3 Results We recorded 36 species of ants at Churince, 33 of which were recorded in the sampling plots and transect, and the remaining 3 species were encountered during additional hand collecting outside the plots. The species represented 19 genera from 6 subfamilies. Although the accumulation curve for pitfall traps did not fully reach the asymptote, while the curve for hand collecting did, they both signal that a large portion of the fauna was recorded. The species richness estimators (ICE) suggest that additional sampling might yield 11 more species in transects and 3 more species in plots (Fig. 10.1). Species richness recorded per single pitfall transect (both years combined) ranged from 1 to 20 species (mean = 6.65 ± 4.93), while from 5 to 10 (mean = 6.43 ± 1.96) species were collected within a single plot. The most frequent species recorded by hand collecting were Crematogaster cerasi, Forelius pruinosus, Solenopsis aurea, and Myrmecocystus wheeleri. The density of nests recorded in a single plot (400 m2) reached up to 23 nests of Crematogaster cerasi. The species recorded with highest frequencies in pitfall transects were Pheidole sp. 1, Forelius pruinosus, Camponotus festinatus, and Forelius mccooki (Fig. 10.2 and 10.3).
10.3.1 Habitat Preferences The highest species richness was found in Tular and Mezquital (25 and 24 spp., respectively), followed by Larrea, Peladero and Sotol having the lowest species richness (Table 10.1). Interestingly, hand collecting recorded 15 and 14 species less in Tular and Mezquital, respectively, than the pitfall traps. The species numbers in the other three habitats were more balanced among both methods (Table 10.1). There was a considerable species overlap among some habitats; however, the numbers of shared species differed largely between the two types of transects and the collecting methods. In the hand-collected plots, Sotol, Larrea, and Mezquital shared the most species. On the other hand, the pitfall trap plots shared the most species between Tular and Mezquital and Mezquital and Larrea. Both methods combined revealed that there were 17 species shared between Tular and Mezquital and 14 species between Tular and Larrea (Table 10.2). The gypsum dunes (Peladero)
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Fig. 10.2 Species accumulation curve for ant samples collected at Churince site. Two collecting methods (hand collecting and pitfall traps) are plotted separately. The species accumulation curves were calculated using 100 randomizations
and the Sotol habitat had the lowest values of Jaccard index, reflecting their more distinct and less diverse fauna. In the correspondence analysis, the first two canonical axes accounted for 36% and 30.5% of explained variance of species data, respectively (Table 10.3). The habitats with the highest quality scores were Tular (0.97) and Peladero (0.79), respectively. To interpret the relationship between the species and the habitats, we plotted both together (Fig. 10.4). The closer the species and habitat categories are, the more strongly they are associated. Although some species can be observed to prefer certain habitats (Mezquital, Larrea, Tular), there were no large groups of species strongly associated with most of them. The habitats with the highest relative inertia (which represents the proportion of the contribution of that point to the overall inertia) were Tular and Peladero (Fig. 10.4 and Table 10.3).
10.4 Discussion Out of the 36 species encountered in Churince, 13 were recorded for the first time in the state of Coahuila (Guénard et al. 2017). This brings the number of ant species currently registered for the state to 93. The actual diversity of Coahuila is most likely at least twice as high and more similar to the neighbouring states of Nuevo León and Chihuahua in which there are 150 and 160 species reported, respectively (Guénard et al. 2017). However, we should consider that most of northern Mexico remains highly undersampled. Considering that the neighbouring states of Arizona, New Mexico, and Texas have each over 300 ant species reported (Guénard et al.
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Fig. 10.3 Ants recorded in Churince site by two collecting methods. The values in hand collecting represent the number of colonies recorded in the plots, while the values in pitfall traps represent the numbers of traps in which the species was recorded during the two collecting years. The patterns represent the distribution among different vegetation types
2017), we can anticipate at least a similar ant diversity in the Mexican bordering states. This only shows that much more surveys are needed across northern Mexico. Ant species richness in Churince is similar to other semi-desert sites in northern Mexico and the southern USA. For example, Rojas and Fragoso (2000) encountered 32 species from 18 genera at Mapimi Reserve in the CD which has similar types of habitats as Churince. Bestelmeyer and Schooley (1999) recorded 39 species in a 9.7 ha area at Los Horcones in the Sonoran Desert and 29 species in a 10 ha area in
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Table 10.1 Alpha diversity metrics for observed species in each habitat and by each method. Higher diversity was found in Mezquital and Tular Pitfall traps Shannon H’ Shannon E No. of species Hand collecting Shannon H’ Shannon E No. of species Both Shannon H’ Shannon E No. of species
Mezquital
Larrea
Peladero
Sotol
Tular
2.7382 0.7641 20
2.2121 0.6173 12
1.8344 0.5119 7
1.5596 0.4352 5
2.7588 0.7698 20
1.67 0.46 6
2.28 0.63 11
1.67 0.46 8
1.80 0.50 8
0.93 0.26 5
2.89 0.80 24
2.66 0.74 17
2.46 0.68 15
2.28 0.63 12
2.56 0.71 25
Table 10.2 Beta diversity metrics among the sampled habitats. Jaccard index of shared species is shown above the diagonal and the number of shared species below the diagonal Pitfall traps Mezquital Larrea Peladero Sotol Tular Hand collecting Mezquital Larrea Peladero Sotol Tular Both Mezquital Larrea Peladero Sotol Tular
Mezquital
Larrea
Peladero
Sotol
Tular
N/A 10 6 2 12
0.45 N/A 5 3 8
0.28 0.36 N/A 1 7
0.08 0.21 0.09 N/A 3
0.42 0.33 0.35 0.13 N/A
N/A 5 3 5 1
0.41 N/A 4 6 3
0.27 0.26 N/A 4 2
0.55 0.46 0.33 N/A 1
0.10 0.23 0.18 0.08 N/A
N/A 12 10 7 17
0.41 N/A 9 9 14
0.34 0.39 N/A 9 13
0.24 0.45 0.50 N/A 11
0.53 0.50 0.48 0.42 N/A
a CD grassland of southern New Mexico. Wheeler and Wheeler (1973) recorded 27 species from Mojave and Sonoran desert scrub habitats in California. On the other hand, the research site La Jornada in the northern CD has at least 74 ant species documented (https://jornada.nmsu.edu). This seems to be a result of the intense, long-term collecting effort (MacKay and MacKay 2002) and due to the high habitat diversity in the area (https://jornada.nmsu.edu/lter/data/species/ants).
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Table 10.3 Percentage of explained variance and eigenvalues for the correspondence analysis of species’ habitat preferences (Fig. 10.4) Axis 1 2 3 4
Eigenvalue 0.32 0.25 0.16 0.10
% of total 38.60 29.99 19.51 11.89
Cumulative 38.60 68.59 88.11 100
Fig. 10.4 Correspondence analysis of species’ occurrences within the five sampled habitats. The analysis was performed with species occurrence frequencies without grouping
Nevertheless, considering in this study that the sampled area was approximately 10 km2 of which a large part was devoid of vegetation, the overall ant diversity seems relatively high. There is no doubt that a long-term and detailed sampling with more collecting methods would yield several more species. In particular, some of cryptic soil fauna and probably some of the smaller ant species associated with trees and shrubs. There was a considerable difference in the number of species recorded between the pitfall traps and hand collecting. This can be attributed to the much longer exposure of the pitfall traps, compared to the direct and focused collecting in plots which took 8 days in total (although spread over 2 years). Furthermore, in some habitats, the species pool was quite different between the two collecting methods. The main contributing factors were likely the differences between the efficiency of both methods and between the size of the area covered by the transects and the plots. The pitfall traps were recording species from a larger radius, for a longer period, and the transect arrangement likely resulted in entrapping some species from the patches of other habitats.
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Fig. 10.5 Representatives of ant species recorded in the Cuatro Ciénegas Basin, Coahuila. (a) Pogonomyrmex maricopa Wheeler, 1914, (b) Crematogaster cerasi (Fitch, 1855), (c) Solenopsis aurea Wheeler, 1906, (d) Pheidole sp. 1, and (e) Myrmecocystus wheeleri Snelling, 1971
10 Diversity and Community Structure of Ants in the Cuatro Ciénegas Basin… Table 10.4 The list of species recorded at Churince site in the Cuatro Ciénegas Basin between the years 2011 and 2015. The list includes species collected by pitfall traps and by direct hand collecting
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Dolichoderinae Forel, 1878 Dorymyrmex flavus McCook, 1880 Dorymyrmex insanus (Buckley, 1866) Dorymyrmex pyramicus (Roger, 1863) Forelius keiferi Wheeler, 1934 Forelius mccooki (McCook, 1880) Forelius pruinosus (Roger, 1863) Formicinae Latreille, 1809 Brachymyrmex depilis Emery, 1893 Camponotus essigi Smith, 1923 Camponotus festinatus (Buckley, 1866) Myrmecocystus wheeleri Snelling, 1971 Nylanderia terricola (Buckley, 1866) Nylanderia sp. Pseudomyrmecinae Smith, 1952 Pseudomyrmex pallidus (Smith, 1855) Dorylinae Leach, 1815 Neivamyrmex harrisii (Haldeman, 1852) Neivamyrmex nigrescens (Cresson, 1872) Myrmicinae Le Peletier de Saint-Fargeau, 1835 Acromyrmex versicolor (Pergande, 1894) Crematogaster cerasi (Fitch, 1855) Crematogaster laeviuscula Mayr, 1870 Cyphomyrmex wheeleri Forel, 1900 Monomorium compressum Wheeler, 1914 Novomessor cockerelli (André, 1893) Pheidole sp. 1 Pheidole sp. 2 Pheidole sp. 3 Pheidole sp. 4 Pheidole sp. 5 Pogonomyrmex barbatus (Smith, 1858) Pogonomyrmex imberbiculus Wheeler, 1902 Pogonomyrmex maricopa Wheeler, 1914 Solenopsis aurea Wheeler, 1906 Temnothorax nitens (Emery, 1895) Temnothorax paiute Snelling et al. 2014 Temnothorax subditivus (Wheeler, 1903) Temnothorax sp.
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10.4.1 Community Structure and Habitat Preferences Among the main factors influencing the diversity and composition of ant communities in the semi-desert habitats are the annual precipitation and minimum annual temperature. The variation in these conditions is often the main contributor to different levels of ant diversity among various xeric and savannah habitats (Bestelmeyer and Schooley 1999). Furthermore, the distance from the subtropical and tropical forest habitats also seem to have an effect in some areas of northern Mexico. Several tropical ant lineages reach the central and northern regions of the country, tracking the patches of tropical vegetation scattered among the vegetation of temperate affinity. However, these species are mainly present in more forested areas rather than in the CCB . The ant fauna documented at Churince represents an assemblage typical for the semi-desert and savannah habitats from central Mexico to the southern USA. Some of the species are in fact common and cosmopolitan with wide ranges and broad habitat preferences (e.g. Crematogaster cerasi, Dorymyrmex spp., Forelius spp. or Pogonomyrmex barbatus). A large portion of the species are distributed across the southern and central USA to central Mexico, with few species reaching Central and South America. However, for several species, Churince currently represents the southernmost distribution record (Camponotus essigi, Myrmecocystus wheeleri, Temnothorax paiute). Apart from the generalists, the community was dominated by xerothermic species associated with semi-desert habitats, such as Cyphomyrmex wheeleri, Myrmecocystus wheeleri, Pogonomyrmex maricopa, Solenopsis aurea, and others. We did not encounter any regional endemics, although some species have been known only from several records in North America so far. The vegetation structure is among the main factors determining the diversity and composition of ant assemblages. In Churince, Tular and Mezquital harboured the most diverse ant communities. Unsurprisingly, the generalists and widespread species (e.g. Forelius spp., Pheidole sp. 1) were found across all or the majority of habitats. Tular was dominated by Crematogaster cerasi, with Forelius pruinosus and Pheidole sp. 1 being also common. Furthermore, Pheidole sp. 5 was almost exclusively found in this habitat. In Mezquital, the community was more balanced (Table 10.1), with Forelius mccooki and Pheidole sp. 1 as the most frequent species and with Monomorium compressum preferring this habitat. Larrea had also a balanced community but was occupied by species occurring in most of the other habitats. Only Nylanderia sp. 1 and Temnothorax sp. 1 were found exclusively in Larrea. There were several species occupying almost exclusively both the Mezquital and Larrea which included Myrmecocystus wheeleri, Pogonomyrmex barbatus, Camponotus festinatus, and Monomorium compressum. In the least diverse Peladero and Sotol, the most frequent species were Solenopsis aurea and Forelius pruinosus, respectively. Trachymyrmex smithi had the strongest preferences for Peladero, while there was no particular species strongly associated with the Sotol.
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Among the conspicuous and relatively common species were two harvester ants. While Pogonomyrmex barbatus was found mainly in Mezquital and Tular, P. maricopa was most abundant in Peladero. This species was also one of the few which extended in the sparsely vegetated areas, including gypsum dunes where it was able to nest in bare sand patches.
10.4.2 N otes About Select Ant Species Occurring in the Cuatro Ciénegas Basin
10.4.3 Myrmecocystus wheeleri Snelling, 1971 This species is found in dry coastal valleys and desert margins. They can forage during midday hours and move quickly on the sand (Mallis 1941). They feed on small arthropods and regularly visit flowers to obtain nectar, especially from plants of the families Polygonaceae and Euphorbiaceae (AntWiki 2017). Distribution: In the USA it is reported from central California and in Mexico from the state of Baja California. With this first record for Coahuila, its known distribution is extended over 1000 km SE.
10.4.4 Pogonomyrmex maricopa Wheeler, 1914 Species with preference for arid habitats and occurs on sandy, silt and loam soils (Navajo Nature 2018). The nests are in the soil, often in areas fully exposed to sunlight (Cole Jr 1968) forming a dome-shaped mound surrounded by a bare area (Moody and Forster 1979). The workers can be scavengers or feed on seeds and insects (Cole Jr 1968). The foraging activity starts when the surface temperature at the opening of the nest reaches 21–23 °C. The foraging increases until the surface temperature reaches 40–45 °C and decreases sharply at temperatures above 46 °C (Moody and Forster 1979). Unlike other Pogonomyrmex species, Pogonomyrmex maricopa individuals do not seem to use trunk trails for their foraging (Navajo Nature 2018). The venom released by this species is among the most toxic substances known. Distribution: In the USA it is present in western Texas, New Mexico, southern Colorado, southern Utah, Arizona, and southeastern Nevada to southeastern California and in Mexico in Sinaloa, Sonora, northern Chihuahua, northern Baja California, Durango, Coahuila, and San Luis Potosí (Vásquez-Bolaños 2015).
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10.4.5 Temnothorax paiute Snelling et al. 2014 This species has been collected on plants of the genus Ephedra; however, not much is known about its biology. Distribution: In the USA, it is reported from California and Nevada (Snelling et al. 2014). This is the first report for Mexico.
10.4.6 Cyphomyrmex wheeleri Forel, 1900 Species with preference for arid habitats. Its nests are located in the ground or under stones in the creosote bush scrub. Fungal gardens can be found a few centimetres below the soil surface, in small chambers, a few centimetres in diameter (Mackay and Mackay 2002). Distribution: In the USA it is reported for California, Arizona, New Mexico, Texas and Louisiana. In Mexico it has been reported in Baja California, Baja California Sur, Sonora, Durango, Tamaulipas and Veracruz (AntWeb 2017). This species is reported for the first time in Coahuila.
10.4.7 Crematogaster laeviuscula Mayr, 1870 It has been found in forests, meadows and riparian habitats. It is an arboreal species and occasionally nests in trunks, in stumps or under stones (Kaspari 2000; Morgan and Mackay 2017). This species has been attracted to meat baits (Morrison 2004). Distribution: Found from across the USA to Tabasco, Mexico (Guénard et al. 2012; Vásquez-Bolaños 2015). Here we report C. laeviuscula for the first time in Coahuila.
10.4.8 Camponotus essigi Smith, 1923 Species that has been reported in coniferous forests as well as from anthropogenic zones (Wheeler and Wheeler 1986). Distribution: The species occurs throughout western USA and also in the Caribbean and Central America. In Mexico, it was previously reported from Baja California. This is the first record for Coahuila.
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10.4.9 Temnothorax subditivus (Wheeler, 1903) Inhabits small dead branches, in shrubland and open woodland habitats. Distribution: From southern USA throughout Central America to Colombia and Venezuela. It has been collected across most of Mexico (Vásquez-Bolaños 2015); however, this is the first record for Coahuila.
10.4.10 Temnothorax nitens (Emery, 1895) Found nesting under stones and trunks, also associated with termite nests. This species can occur in juniper forests (Mackay 2000). Distribution: Across western and central USA; in Mexico only previously reported in Durango. This is the first record for Coahuila.
10.4.11 Pseudomyrmex pallidus (Smith, 1855) A widespread species that nests in cavities of dead plant stems and branches of trees (Ward 1985). It may feed on extrafloral nectaries and flowers (Sherbrooke and Scheerens 1979). Distribution: Widely distributed in the Nearctic and Neotropical regions. This is the first record for Coahuila.
10.4.12 Neivamyrmex nigrescens (Cresson, 1872) A common, widespread species with a nomadic life cycle. It is usually active at night, hunting for insects including other ant colonies (Snelling and Snelling 2007). Distribution: Occurs across the USA and throughout Central America. This is the first record for Coahuila. Acknowledgements We are grateful to Valeria Souza and Luis Eguiarte for indispensable research and logistic assistance and to Fret Cervantes for field assistance. We thank the Ecological Genomics Laboratory at LANGEBIO, Cinvestav, for logistic support with the project. Funding was provided by the Czech Science Foundation, Centrum of Excellence for Tropical Biology: 14-36098G, CONACYT DICB-2016 No. 282471 and UNAM PAPIIT IN206818.
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References AntWeb (2017) https://www.antweb.org/. Accessed 13 Mar 2018 AntWiki (2017) Species Accounts. http://www.antwiki.org/wiki/Species_Accounts. Accessed 13 Mar 2018 Ávalos-Hernández O, Cano-Santana Z, Trujano-Ortega M, García-Vázquez UO (2016) Diversity and resource use patterns of anthophile insects in Cuatro Ciénegas Coahuila Mexico. Environ Entomol 45:1386–1397 Bestelmeyer BT, Schooley RL (1999) The ants of the southern Sonoran desert: community structure and the role of trees. Biodivers Conserv 8:643–657 Bizuet-Flores YM, Jiménez-Jiménez LM, Zavala-Hurtado A, Corcuera P (2015) Diversity patterns of ground dwelling spiders (Arachnida: Araneae) in five prevailing plant communities of the Cuatro Ciénegas Basin, Coahuila, Mexico. Rev Mex Biodivers 86(1):153–163 Bouchard P, Wheeler TA, Goulet H (2000) Design for a low-cost, covered, ramp pitfall trap. Can Entomol 132:387–389 Cole AC Jr (1968) Pogonomyrmex harvester ants. A study of the genus in North America. University of Tennessee Press, Knoxville, 222 pp Contreras-Balderas AJ, López-Soto JH, Torres-Ayala JM (2004) Additional records of birds from Cuatrociénegas basin, Natural Protected Area, Coahuila México. Southwest Nat 49:103–109 Guénard B, Mccaffrey KA, Lucky A, Dunn RR (2012) Ants of North Carolina: an up-dated list (Hymenoptera: Formicidae). Zootaxa 3552:1–36 Guénard B, Weiser MD, Gomez K, Narula N, Economo EP (2017) The Global Ant Bio-diversity Informatics (GABI) database: synthesizing data on ant species geographic distribution. Myrmecol News 24:83–89 Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton Kaspari M (2000) Do imported fire ants impact canopy arthropods? Evidence from simple arboreal pitfall traps. Southwest Nat 45:118–122 MacKay WP (2000) A review of the New World ants of the subgenus Myrafant (genus Leptothorax). Sociobiol 36:265–444 MacKay WP, MacKay E (2002) The ants of New Mexico. The Edwin Mellen Press, Lewiston Mallis A (1941) A list of the ants of California with notes on their habits and distribution. Bull South Calif Acad Sci 40:61–100 Morgan C, Mackay WP (2017) The North America acrobat ants of the hyperdiverse genus Crematogaster. LAP LAMBERT Academic Publishing, Mauritius, p 540 Morrison LW (2004) Spatiotemporal variation in antlion (Neuroptera: Myrmeleontidae) density and impacts on ant (Hymenoptera: Formicidae) and generalized arthropod foraging. Ann Entomol Soc Am 97:913–922 Mendoza-Quijano F, Arturo GA, Liner EA, Bryson RW Jr (2006) Una sinopsis de la herpetofauna de Coahuila Inventarios herpetofaunísticos de México: avances en el conocimiento de su biodiversidad. Soc Herpetol Mex:24–47 Moody JV, Forster DE (1979) Notes on the bionomics and nest structure of Pogonomyrmex maricopa (Hymenoptera: Formicidae) National parks by. National Park Service region 4:115–121 Moreno-Letelier A, Olmedo-Alvarez G, Eguiarte LE, Souza V (2012) Divergence and phylogeny of Firmicutes from the Cuatro Ciénegas Basin, Mexico: a window to an ancient ocean. Astrobiology 12:674–684 Navajo Nature (2018). http://navajonature.org/. Accessed 13 Mar 2018 Real R, Vargas JM (1996) The probabilistic basis of Jaccard’s index of similarity. Syst Biol 45:380–385 Rojas P, Fragoso C (2000) Composition, diversity, and distribution of a Chihuahuan Desert ant community (Mapimí, México). J Arid Environ 44:213–227 Sherbrooke WC, Scheerens JC (1979) Ant-visited extrafloral (calyx and foliar) nectaries and nectar sugars of Erythrina flabelliformis Kearney in Arizona. Ann Mo Bot Gard 472:481
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Sissom WD, Hendrixson BE (2006) Scorpion biodiversity and patterns of endemism in northern Mexico. In: Cartron JLE, Ceballos G (eds) Biodiversity, ecosystems and conservation in northern Mexico. Oxford University Press, Oxford, pp 122–137 Snelling RR, Borowiec ML, Prebus MM (2014) Studies on California ants: a review of the genus Temnothorax (Hymenoptera, Formicidae). ZooKeys 372:27 Snelling GC, Snelling RR (2007) New synonymy, new species, new keys to Neivamyrmex army ants of the United States. Mem Am Entomol Inst 80:459–550 Souza V, Siefert JL, Escalante AE, Elser JJ, Eguiarte LE (2012) The Cuatro Ciénegas basin in Coahuila, Mexico: an astrobiological precambrian park. Astrobiology 12:641–647 Vásquez-Bolaños M (2015) Taxonomía de Formicidae (Hymenoptera) para México. Métodos en Ecología y Sistemática 10:1–53 Wheeler GC, Wheeler JN (1973) Ants of deep canyon, Colorado Desert, California. Philip L. Boyd Deep Canyon Desert Research Center, University of California Riverside, Riverside Wheeler GC, Wheeler J (1986) The ants of Nevada. Natural History Museum of Los Angeles County, Los Angeles Williams SC (1968) Scorpions from Northern Mexico: five new species of Vejovis from Coahuila, Mexico. Occas Pap Calif Acad Sci 68:1–24
Chapter 11
Prostigmatid Mites (Arachnida, Acariformes, Prostigmata) Parasitic on Amphibians and Reptiles in the Cuatro Ciénegas Basin Ricardo Paredes-León
Abstract Herpetozoa of ten species from the Cuatro Ciénegas Basin (CCB) were inspected in search of parasitic mites. A total of 195 specimens of nine taxa of mites from the suborder Prostigmata (Arachnida: Acariformes: Trombidiformes) were recovered from 27 herps, 25 reptiles and 2 amphibians. The frog Lithobates berlandieri was intradermally parasitized by two species of the genus Hannemania (Leeuwenhoekiidae). Another two species of Leeuwenhoekiidae were found externally on three phrynosomatid lizards: Sceloporus merriami, S. poinsettii and Cophosaurus texanus. Three mite species of the family Trombiculidae were found on the lizards Sceloporus magister, S. merriami and S. poinsettii (Phrynosomatidae); Aspidoscelis gularis septemvittata and A. inornata cienegae (Teiidae); and Gerrhonotus sp. (Anguidae) and on the snake Thamnophis proximus diabolicus (Colubridae). Additionally, two species of the genus Geckobiella (Pterygosomatidae) were found parasitizing the phrynosomatid lizards Sceloporus poinsettii, S. merriami and S. cyanostictus. The prostigmatid mite fauna on herps from the CCB include nine new records of mites for the study area and eight new host records including the first records of parasitic mites for five host species. Keywords Chiggers · Leeuwenhoekiidae · Pterygosomatidae · Trombiculidae · Herpetozoa
R. Paredes-León (*) Colección Nacional de Ácaros, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico e-mail: [email protected] © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_11
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11.1 Introduction The Acari (mites and ticks) is the most diverse group of the class Arachnida and is comprised by two lineages, Parasitiformes and Acariformes. The acariform mites are the largest lineage with approximately 42,230 species (Zhang 2013). The suborder Prostigmata is the most diverse and includes free-living and parasitic mites. Prostigmata includes some of the most important parasites of reptiles, which are either permanent (Pterygosomatidae, Cloacaridae, Harpirrhynchidae) or temporal parasites (Trombiculidae, Leeuwenhoekiidae) (Fajfer 2012); the latter family is also found commonly in amphibians (Paredes-León et al. 2008). The mite fauna in Mexico has been poorly studied, and according to Pérez et al. (2014), Acari is represented by 2625 species, representing only 4.8% of the world’s mite fauna. The majority of this diversity is included in the Acariformes with 2010 species. In Mexican herpetozoa, at least 38 species of parasitic prostigmatic mites have been recorded (Dugès 1888; Paredes-León et al. 2008, 2012; Paredes-León and Morales-Malacara 2009; Paredes-León and Guzmán-Cornejo 2015). In particular, the mite fauna of the Mexican state of Coahuila has not been compiled, but 80 species were mentioned by Hoffmann and López-Campos (2000) for this area. From these, at least six species are endemic to Coahuila: (1) Euschoengastia fronterizae Wrenn, Baccus and Loomis, 1976, (2) Walchioides whartoni (Brennan, 1960) (Trombiculidae, both species ectoparasites on mammals), (3) Brevipalpus celtis Baker, Tuttle and Abbatiello, 1975, (4) B. piniceltis Baker and Tuttle, 1987, (5) B. ruelliae Baker and Tuttle, 1987 (Tenuipalpidae, phytophagous) and (6) Atractides toldomus Cook, 1980 (Hygrobatidae, water mites). Regarding the parasitic mites on lizards, only three species have been recorded from Coahuila: (1) Eutrombicula alfreddugesi (Oudemans, 1910) (Trombiculidae), (2) Acomatacarus arizonensis Ewing, 1942 (Leeuwenhoekiidae) and (3) Bertrandiella otophila (Hunter and Loomis, 1966) (Pterygosomatidae) (Hoffmann 1990; Paredes-León et al. 2008; García-De la Peña et al. 2007, 2010; García-De la Peña 2011). There are no records of mites parasitizing amphibians in the state of Coahuila. The studies in the Chihuahuan Desert (CD) have been carried out only in the northern region, in New Mexico (United States), where 114 mite species were identified from decomposed leaf litter and the underlying mineral soil (Cepeda and Whitford 1990). Whereas for the Mexican portion of the CD and in particular in the surroundings of the Cuatro Ciénegas Basin (CCB), just two scattered records of chiggers (Trombiculidae) on rodents have been published: (1) Euschoengastoides arizonae Loomis, 1971 and (2) Otorhinophila baccusi Loomis and Wrenn, 1973. Some efforts to describe the mite fauna associated to lizards from the Mexican part of the CD and surroundings have been carried out by García-De la Peña and collaborators who have recorded two species, Eutrombicula alfreddugesi and Acomatacarus arizonensis, associated to nine lizard species (García-De la Peña 2011; García-De la Peña et al. 2004, 2007, 2010). In this contribution, I present the
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first account on the parasitic mites associated to amphibians and reptiles from the CCB, including new locality and host records for the area.
11.2 Materials and Methods Amphibians and reptiles from eight localities in the CCB (Fig. 11.1) were inspected in situ searching for parasitic mites. The whole of the body surface was examined from each herpetozoa, using forceps, cotton swabs and entomological needles to collect the mites. These were preserved in glass vials with 80% ethanol and transported to the laboratory. Selected mites were cleared with lactophenol and mounted on microscopic slides using Hoyer’s medium as preserver (Walter and Krantz, 2009). The rest of mites were preserved in 80% ethanol. All the mites are deposited at Colección Nacional de Ácaros (CNAC) of the Instituto de Biología (IB), Universidad Nacional Autónoma de México (UNAM) in Mexico City, Mexico, with catalogue numbers CNAC011116–011192. Two specimens of Acomatacarus arizonensis were processed for micrographs with a Hitachi S-2460 N scanning electron microscope following the technique proposed by Alberti and Nuzzaci (1996). Photographs of mounted specimens were taken with a Zeiss AxioCam MRc 5 camera adapted to a Zeiss Axio Zoom V.16 stereo zoom microscope. Both photography techniques were performed in the Scanning Electron Microscopy (SEM) and Photography Lab of the IB-UNAM.
Fig. 11.1 Study area showing the localities of the prostigmatid mites parasitic on amphibians and reptiles in the Cuatro Ciénegas Basin
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Mites were identified using the taxonomic keys of Brennan and Goff (1977) and Hoffmann (1990) for Trombiculidae and Leeuwenhoekiidae and Paredes-León et al. (2012) and Paredes-León and Guzmán-Cornejo (2015) for Pterygosomatidae. Host names follow The Reptile Database (Uetz, 2018) and The Amphibian Species of the World (Frost 2018). A map of the study area (Fig. 11.1) was generated using Google Earth Pro (ver. 7.3.2).
11.3 Diversity Nine species of mites were found associated to ten species of herpetozoa (n = 27) from eight localities in the CCB (Fig. 11.1). The lizards Sceloporus merriami (canyon lizard) and S. poinsettii (crevice spiny lizard) (Phrynosomatidae) were the hosts with the greatest number of parasites, with five and four mite species, respectively. The lizards S. cyanostictus (blue-spotted spiny lizard) (Phrynosomatidae) and Aspidoscelis gularis septemvittata (Mexican plateau spotted whiptail) (Teiidae) and the frog Lithobates berlandieri (Río Grande leopard frog) (Ranidae) were parasitized by two mite species each, whereas the lizards Sceloporus magister (desert spiny lizard), Cophosaurus texanus (greater earless lizard) (Phrynosomatidae), Aspidoscelis inornata cienegae (little stripped whiptail) (Teiidae) and Gerrhonotus sp. (Anguidae) and the snake Thamnophis proximus diabolicus (arid land ribbon snake) (Colubridae) were parasitized by one mite species each (Table 11.1). All the prostigmatid mite fauna found (nine species) on herps from the CCB are new records of mites for the study area and eight new host records (Sceloporus poinsettii and lizards of the genus Gerrhonotus had already been reported as hosts of A. arizonensis and E. alfreddugesi, respectively), including the first record of parasitic mites for Sceloporus merriami, Cophosaurus texanus, Aspidoscelis inornata cienegae, A. gularis septemvittata and Thamnophis proximus diabolicus in all their distribution range. All the species of mites found are parasites; some of them are permanent ectoparasites in all the active instars of their life cycle (Pterygosomatidae), whereas some species are temporary parasites, only in larval instar. Among the latter, some species are either endoparasites (Leeuwenhoekiidae) or ectoparasites (Leeuwenhoekiidae and Trombiculidae).
11.3.1 Trombiculidae and Leeuwenhoekiidae These families are closely related, and even in some classifications, Leeuwenhoekiidae is considered a subfamily of Trombiculidae (Shatrov and Kudryaashova, 2008). These mites have a complex life cycle including an egg, inactive prelarva, active larva, inactive protonymph, active deutonymph, inactive tritonymph and active adults (Walter et al. 2009). Trombiculidae and
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Table 11.1 Classification of the prostigmatid mites parasitic on herpetozoa from the Cuatro Ciénegas Basin Taxa Host Subclass Acari Superorder Acariformes Order Trombidiformes Suborder Prostigmata Supercohort Anystides Cohort Parasitengonina Subcohort Trombidiae Superfamily Trombiculoidea Family Leeuwenhoekiidae Acomatacarus Sceloporus merriami arizonensis Sceloporus poinsettii Cophosaurus texanus ca. Acomatacarus Sceloporus poinsettii Sceloporus merriami Hannemania ca. Lithobates berlandieri mexicana Hannemania ca. saxicola Lithobates berlandieri Family Trombiculidae Eutrombicula Aspidoscelis inornata alfreddugesi cienegae Aspidoscelis gularis septemvittata Gerrhonotus sp. Sceloporus poinsettii Sceloporus merriami Eutrombicula ca. alfreddugesi
ca. Eutrombicula
Supercohort Eleutherengonides Cohort Raphignathina Superfamily Pterygosomatoidea Family Pterygosomatidae Geckobiella sp. 1
Aspidoscelis gularis septemvittata Thamnophis proximus diabolicus Sceloporus magister Sceloporus merriami
Sceloporus cyanostictus Sceloporus poinsettii
Locality
Ejido El Oso; Ejido El Oso, Ojo de Agua; Santa Teresa Ejido El Oso, Ojo de Agua Ejido El Oso, Ojo de Agua Carr. Ejido El Oso-Ojo de Agua Carr. Ejido El Oso-Ojo de Agua Rancho Pronatura Antiguos Mineros del Norte Poza Churince; Poza de Enmedio Ejido El Oso, Ojo de Agua Poza Churince Rancho La Casita; Ejido El Oso, Ojo de Agua Carr. Ejido El Oso-Ojo de Agua; Santa Teresa Ejido El Oso, Ojo de Agua Rancho Pronatura, Pozas Azules Rancho Pronatura, Pozas Azules Carr. Ejido El Oso-Ojo de Agua; Ejido El Oso, Ojo de Agua
Rancho El Chupadero Rancho La Casita; Rancho El Chupadero (continued)
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Table 11.1 (continued) Taxa Geckobiella sp. 2
Host Sceloporus merriami Sceloporus cyanostictus
Locality Santa Teresa Rancho El Chupadero
Leeuwenhoekiidae are the only ones from the cohort Parasitengonina with larval parasites that attack terrestrial vertebrate hosts: wildlife, domesticated and humans. The larvae, commonly known as “chiggers”, are strongly heteromorphic, very different from the post-larval instars. Deutonymphs and adults are soil dwellers that prey on various insects. The bites of trombiculid chiggers cause skin irritations and itching in their hosts (condition known as trombidiosis or trombiculosis) and serve as vectors of the causative agents of human diseases (Shatrov and Kudryaashova 2006; Walter et al. 2009). Owing to their medical and veterinary importance, larvae have been studied more, and therefore taxonomy is entirely based on this instar. In this study, the most common chigger was the protelean ectoparasite Eutrombicula alfreddugesi found on five species of lizards (Table 11.1). This species has been pointed out as one of the two main responsible species of trombiculosis in North America (Jenkins, 1948). Acomatacarus arizonensis (Fig. 11.2a–c) was found on three host species (Table 11.1). This chigger has been recorded only from the Midwestern United States to western Mexico (Hoffmann 1990). I found also two species of the genus Hannemania (Leeuwenhoekiidae) endoparasites in Lithobates berlandieri. These species were identified as Hannemania ca. mexicana (Fig. 11.2d) and H. ca. saxicola. Both species are endemic to Mexico. Hannemania mexicana is distributed in San Luis Potosí, Puebla and Veracruz in different host species of the genus Lithobates (Hoffmann 1965; Paredes-León et al. 2008; Jacinto-Maldonado et al. 2016), whereas H. saxicola has been recorded in Durango in Eleutherodactylus saxatilis (Welbourn and Loomis 1970). Three of the nine species found were not identified with accuracy because their morphological characteristics did not fit fully with the diagnosis of the taxa, so these were provisionally labelled as (1) Leeuwenhoekiidae ca. Acomatacarus, ectoparasitic on the lizards Sceloporus merriami and S. poinsettii, (2) Trombiculidae ca. Eutrombicula found on S. magister and S. merriami and (3) Eutrombicula ca. alfreddugesi found on Aspidoscelis gularis septemvittata and on the snake Thamnophis proximus diabolicus.
11.3.2 Pterygosomatidae The family Pterygosomatidae is the only representative of the superfamily Pterygosomatoidea. It comprises 11 genera and approximately 180 species; almost all of them are ectoparasitic on lizards of different families around the world, passing their entire life cycle on the skin between the host’s scales, hence, their common name of “scale mites”. However, some species have different kinds of hosts, such as species of the genus Pimeliaphilus that are ectoparasitic on arthropods, as well as
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Fig. 11.2 Representative prostigmatid mites associated to the herpetofauna in the Cuatro Ciénegas Basin. (a–c) Acomatacarus arizonensis; (a) dorsal aspect of the idiosoma; (b) detail of the dorsal scutum and eyes; (c) tarsus II showing solenidion (tarsala II) expanded apically. (d) Hannemania ca. mexicana, ventral aspect of the idiosoma. (e) Geckobiella sp. 1, dorsal aspect of the idiosoma. (f) Geckobiella sp. 2, dorsal aspect of the idiosoma
one species of Geckobia associated to a turtle and the monotypic Bharatoliaphilus found on a dove (Prasad 1975; Bertrand and Pedrono 1999; Paredes-León et al. 2012). The lizards of the CCB are parasitized by two species of the genus Geckobiella, here named Geckobiella sp. 1 (Fig. 11.2e) and Geckobiella sp. 2 (Fig. 11.2f), both found on Sceloporus cyanostictus, and the first one also found on S. poinsettii and S. merriami (Table 11.1).
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11.4 Endemism Mites were found parasitizing herpetozoa from eight localities in the CCB (Fig. 11.1). The locality with the greatest number of records was Ejido El Oso with 16 records of mites on lizards, followed by Rancho El Chupadero and Rancho La Casita with 4 records each; Rancho Pronatura, Poza de Enmedio and Santa Teresa with 3 records each; and Antiguos Mineros del Norte and Poza Churince with 1 record each (Table 11.1). Only two of the nine taxa found are considered endemic to Mexico: Hannemania ca. mexicana and H. ca. saxicola. However, other mite species are ectoparasitic on two endemic lizards: (1) Aspidoscelis inornata cienegae distributed only in the CCB and (2) Sceloporus cyanostictus occurring only in the state of Coahuila (Uetz, 2018). Hannemania ca. mexicana was found only in Rancho Pronatura, while H. ca. saxicola was found in Antiguos Mineros del Norte. These mites are endoparasites in Lithobates berlandieri whose natural distribution comprises central and western Texas and southern New Mexico, USA, through eastern Chihuahua to central Veracruz and Hidalgo, Mexico. It has been introduced to Sonora and Baja California in Mexico and to California and Arizona in the USA (Uetz, 2018). Both species are distributed in the Mexican Plateau Province, although H. mexicana extends to the Sierra Madre Oriental Province. Acomatacarus arizonensis is an ectoparasitic mite specific of lizards and some snakes (Squamata) and has a disjunct distribution from the west and Midwest of the USA, to the Baja California and Mexican Pacific Coast Provinces (Brennan and Beck 1955; Crossley 1960; Allred and Beck 1962; Loomis and Stephens 1973; Hoffmann 1990). Eutrombicula alfreddugesi is considered the species of chiggers with the widest distribution in America, from southern Canada to Argentina. This species can parasitize any terrestrial vertebrate. In Mexico, it has been known since the pre-Hispanic era with the name of “tlalzahuatl” or “tlalzahuate” and recorded throughout Mexico (Hoffmann 1990). Taxonomically, Eutrombicula alfreddugesi belongs to the alfreddugesi group, which includes seven species, two of them occurring in Mexico. However, it is considered that most of the records of E. alfreddugesi are misidentifications. It is estimated that in Mexico, there are at least 13 species of the alfreddugesi group, ten of them being undescribed. Most of these, tentatively, new species are ectoparasitic on lizards of the genus Sceloporus at high elevations (Loomis and Wrenn 1984; Wrenn and Loomis 1984). Species included in the genus Geckobiella have a high host preference for iguanian lizards of the families Iguanidae, Phrynosomatidae and Tropiduridae (Paredes-León et al. 2012). The genus Geckobiella includes three species with hypertrichous idiosoma in adult females and eight oligotrichous species, all distributed in the Americas. The known larvae in this genus retain the oligotrichous idiosomal condition. The taxonomy is entirely based on adult females and only in a few
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species other instars are known. We found two different species of Geckobiella in larval instar; they differ in the size of the dorsal idiosomal setae. One of the larvae found (Geckobiella sp. 2) has short dorsal idiosomal setae (Fig. 11.2f), which implies that it corresponds to one of the species with hypertrichous adults whereas that the other kind of larvae (Geckobiella sp. 1) with long dorsal idiosomal setae (Fig. 11.2e) are more similar to those species with oligotrichous adults (ParedesLeón, unpublished data). Both species were found parasitizing Sceloporus cyanostictus, a species endemic to Coahuila and considered as endangered by the International Union for Conservation of Nature (IUCN) (Vázquez-Díaz et al. 2007). Additionally, Geckobiella sp. 1 was also found on Sceloporus poinsettii and S. merriami.
11.5 Origin The oldest fossil of mites belongs to the Acariformes and is known from the Devonian period, at least 411 million years ago (Dunlop and Selden 2009). However, most ancient acariform mites belong to taxa whose actual descendants feed on fungi and other microbes, dead plant matter or green algae (Walter and Proctor 2013). Unfortunately, there is no paleontological material on trombiculid mites, although representatives of the closely related recent families Erythraeidae and Trombidiidae were recorded in Baltic amber from the Oligocene (Dubinin 1962; Shatrov and Kudryaashova 2006, 2008). Fossilized trombidiform mites, which were aquatic species, are known from the Middle Jurassic, whereas many recent families of terrestrial mites were discovered from the mineral resins of the Upper Cretaceous (Vainstein 1978). On the other hand, the oldest known member of the parasitic mite family Pterygosomatidae was found in the Lower Cretaceous (Albian) from 100 million- year-old amber (Sidorchuk and Khaustov 2018). This mite corresponds to an unattached larva of the genus Pimeliaphilus, whose current species are ectoparasites on gekkotan lizards in the Old World and on arthropods worldwide (Paredes-León et al. 2012). Among the herpetozoa from the CCB, phrynosomatid lizards (n = 18, 67%) are the main hosts of prostigmatid mites (Table 11.1). It has been assumed that the age of the most recent common ancestor of phrynosomatids is on average 55 million years (Wiens et al. 2013). However, the lack of more fossils and of a phylogeny for chiggers and scale mites prevents the establishing of scenarios on the history of these parasitic mites in the region.
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11.6 Biogeography The herpetofauna of Coahuila shares the most species with that of the adjoining states of Nuevo León in Mexico and Texas in the USA (Lemos-Espinal and Smith 2016). Unfortunately, the knowledge on parasitic mites on herpetofauna is very scarce and has not been explored in detail virtually in any region. Previous studies in the CD region were focused on free-living mites (not parasites) (Cepeda and Whitford, 1990). In the CD region and surrounding areas, two species of ectoparasitic mites on some lizards have been recorded, such as (1) Eutrombicula alfreddugesi on Gerrhonotus infernalis (Texas alligator lizard) (Anguidae), Sceloporus jarrovii (Yarrow’s spiny lizard), S. poinsettii and S. grammicus (Phrynosomatidae) from the Sierra de Jimulco, located south of the CD region (García-De la Peña, 2011); on Sceloporus couchii from Santa Catarina, located south-east of the CD region (García-De la Peña et al. 2004); and on Uma exsul (fringe-toed sand lizard) and Uta stansburiana stejnegeri (desert side-blotched lizard) (Phrynosomatidae) from Viesca, south of the CD region (García-De la Peña et al. 2007) and (2) Acomatacarus arizonensis on Sceloporus cyanostictus and Crotaphytus antiquus (venerable collared lizard) (Phrynosomatidae) from the Sierra San Lorenzo and on Sceloporus jarrovii from the Valle de las Piedras Encimadas, both localities from the southern part of the CD (García-De la Peña et al. 2010).
11.7 Conservation Status There are no mite species listed in the NOM-059 (SEMARNAT, 2010), but there are five species listed by the IUCN red list of threatened species (Gerlach 2014a, b, c, d; Pryce and White 2014); however, none of them are from Mexico. Conversely, some of the host species (herpetozoa) are considered to be in risk. The lizard Sceloporus cyanostictus is considered an endangered species according to the IUCN (Vázquez-Díaz et al. 2007). Further, S. cyanostictus is one of the endemic members of the Mexican herpetofauna with the highest environmental vulnerability scores (EVS = 16), which is due to its restricted distribution in a single physiographic region (Johnson et al. 2017). According to the NOM-059, the lizard Cophosaurus texanus and the snake Thamnophis proximus are listed as Threatened, while the frog Lithobates berlandieri is listed as Subject to Special Protection. Curiously, S. cyanostictus is not listed in any category unlike the IUCN red list (SEMARNAT, 2010).
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11.8 Discussion The herpetozoa from the CCB can be parasitized by a relatively high diversity of mites, totaling nine species. These mites exhibit a variety of life cycles and behaviours; chiggers (Leeuwenhoekiidae and Trombiculidae) are parasites only in the larval instar and can be internal (in amphibians) or external (on lizards and snakes), whereas scale mites (Pterygosomatidae) are external parasites in all instars of their life cycle. The prostigmatid mite fauna in the CCB includes only a small proportion of the real parasite diversity associated to the herpetofauna from the region. Despite this, the registered biodiversity includes nine new records of mites for the study area and eight new host records (including the first records of parasitic mites for five host species). Future research should focus on the taxonomic status of the species with morphological variation to define their correct identity. The exploration of more representatives of the herpetofauna of the CCB and their parasitic mites will permit a better approach to the real biodiversity of symbiotic organisms. The knowledge of the parasitic mite fauna allows a better understanding of the host’s biology and some of them (e.g. Pterygosomatidae) can be useful models for co-evolution studies. It is clear that ignoring this biodiversity not only maintains an incomplete checklist for any region but also conservation strategies cannot be completely successful. Failure to protect the herpetofauna entails a major catastrophe considering all their symbionts, a process called co-extinction. Future efforts should be routed to protecting these biological interactions. Acknowledgements I am grateful to M. Trujano Ortega and U. O. García Vázquez for collecting the mites on herpetozoa during field work. Thanks to the graduate student A. L. Carlos Delgado for his help in processing the mites in microscope slides and to T. M. Pérez for granting access to CNAC where the specimens were studied. Also, thanks to A. L. Carlos Delgado as well as B. Mendoza-Garfias and S. Guzmán (Laboratorio de Microscopía Electrónica y Fotografía de la Biodiversidad, IB-UNAM) for their help in obtaining the microphotographs. Thanks to M. Ojeda and M. Trujano Ortega for inviting me to participate in this contribution. Field work was partially supported by Conabio (grant number JF065) and WWF/Alianza Carlos Slim.
References Alberti A, Nuzzaci G (1996) SEM and TEM techniques. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophid mites: their biology, natural enemies and control, vol 6. Elsevier, Amsterdam, pp 399–410. 790 pp Allred DM, Beck DE (1962) Ecological distribution of mites on lizards at the Nevada atomic test site. Herpetologica 18:47–51 Bertrand M, Pedrono M (1999) Euryxenie et stenoxenie du genre Geckobia Mégnin (Actinedida: Pterygosomatidae): recolte de Geckobia enigmatica n. sp. sur une tortue terrestre malgache (Geocehelone yniphora). Acarologia 40:147–153
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Brennan JM, Beck DE (1955) The chiggers of Utah (Acarina: Trombiculidae). Great Basin Nat 15:1–26 Brennan JM, Goff ML (1977) Keys to the genera of chiggers of the western hemisphere (Acarina: Trombiculidae). J Parasitol 63:554–566 Cepeda J, Whitford WG (1990) Microartrópodos edáficos del desierto Chihuahuense, al norte de México. Fol Entomol Mex 78:257–272 Crossley DA Jr (1960) Comparative external morphology and taxonomy of nymphs of the Trombiculidae (Acarina). U Kansas Sci Bull 40:135–321 Dubinin VB (1962) Class Acaromorpha. Acari. In: Rodendorf BB (ed) The bases of paleontology. Arthropods – tracheal and cheliceral. Nauka, Moscow, pp 450–473. (In Russian). Dugès A (1888) Description de Geckobia oblonga nov. sp. Bull Soc Zool France 13:14–16 Dunlop JA, Selden PA (2009) Calibrating the chelicerate clock: a paleontological response to Jeyaprakash and Hoy. Exp Appl Acarol 48:183–197 Fajfer M (2012) Acari (Chelicerata) – parasites of reptiles. Acarina 20:108–129 Frost DR (2018) Amphibian species of the World: an Online Reference. Version 6.0 (May 24, 2018). Electronic database accessible at http://research.amnh.org/herpetology/amphibia/index.html. American Museum of Natural History, New York, USA García-De la Peña C (2011) Eutrombicula alfreddugesi (Acari: Trombiculidae): new host records from four species of lizards in the Sierra de Jimulco, Coahuila, Mexico. Southwest Nat 56:131–133 García-De la Peña C, Contreras-Balderas A, Castañeda G, Lazcano D (2004) Infestación y distribución corporal de la nigua Eutrombicula alfreddugesi (Acari: Trombiculidae) en el lacertilio de las rocas Sceloporus couchii (Sauria: Phrynosomatidae). Acta Zool Mex (n s) 20:159–165 García-De la Peña C, Castañeda G, Barrows CW (2007) Infestation by chigger mites in two lizard species from a dune habitat of northern Mexico. Texas J Sci 59:23–32 García-De la Peña C, Paredes-León R, O'Connor BM, Gadsden-Esparza H, Barrows CW (2010) Acomatacarus arizonensis (Acari: Leeuwenhoekiidae): new records from three species of lizards in the Mexican chihuahuan desert. Southwest Nat 55:278–279 Gerlach J (2014a) Dicrogonatus gardineri. The IUCN Red List of Threatened Species 2014: e.T201462A2706716. https://doi.org/10.2305/IUCN.UK.2014-1.RLTS. T201462A2706716. en. Downloaded on 10 July 2018 Gerlach J (2014b) Dicrogonatus niger. The IUCN Red List of Threatened Species 2014: e.T201461A2706709. https://doi.org/10.2305/IUCN.UK.2014-1.RLTS. T201461A2706709. en. Downloaded on 10 July 2018 Gerlach J (2014c) Michaelothyrus seychellensis. The IUCN Red List of Threatened Species 2014:e. T201464A2706723. https://doi.org/10.2305/IUCN.UK.2014-1.RLTS. T201464A2706723.en. Downloaded on 10 July 2018 Gerlach J (2014d) Sternothyrus braueri. The IUCN Red List of Threatened Species 2014: e.T201466A2706730. https://doi.org/10.2305/IUCN.UK.2014-1.RLTS. T201466A2706730. en. Downloaded on 10 July 2018 Hoffmann A (1965) Contribuciones al conocimiento de los trombicúlidos mexicanos (Acarina: Trombiculidae). 11ª parte. Fol Entomol Mex 9:3–18 Hoffmann A (1990) Los trombicúlidos de México (Acarida: Trombiculidae). Pub Esp I Biol, UNAM 2:1–275 Hoffmann A, López-Campos G (2000) Biodiversidad de los ácaros en México. Universidad Nacional Autónoma de México y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Ciudad de México, México, 230 pp Jacinto-Maldonado M, Paredes-León R, Salgado-Maldonado G, García A, Suzán G (2016) New records of amphibians parasitized by chiggers in Los Tuxtlas Biosphere Reserve, Mexico, and taxonomic notes on Hannemania mexicana (Acariformes: Prostigmata: Leeuwenhoekiidae). Syst Appl Acarol 21:13–20 Jenkins DW (1948) Trombiculid mites affecting man. I. Bionomics with reference to epidemiology in the United States. Am J Hyg 48:22–35
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Johnson JD, Wilson LD, Mata-Silva V, García-Padilla E, DeSantis DL (2017) The endemic herpetofauna of Mexico: organisms of global significance in severe peril. Mesoamerican Herp 4:543–620 Lemos-Espinal JA, Smith GR (2016) Amphibians and reptiles of the state of Coahuila, Mexico, with comparisons with adjoining states. ZooKeys 593:117–137 Loomis RB, Stephens RC (1973) The chiggers (Acarina, Trombiculidae) parasitizing the side- blotched lizard (Uta stansburiana) and other lizards in Joshua Tree National Monument, California. Bull South Cal Acad Sci 72:78–89 Loomis RB, Wrenn WJ (1984) Systematics of the pest chigger genus Eutrombicula (Acari: Trombiculidae). In: Griffiths DA, Bowman CE (eds) Acarology VI, Volume 1. Ellis Horwood Limited, Chichester, pp 152–159. 645 pp Paredes-León R, Guzmán-Cornejo C (2015) A new species of pterygosomatid mite and its phylogenetic position within the genus Geckobiella (Acariformes: Prostigmata: Pterygosomatidae). Int J Acarol 41:19–30 Paredes-León R, Morales-Malacara JB (2009) A new species of the genus Hirstiella (Acari: Prostigmata: Pterygosomatidae) parasitic on Phyllodactylus bordai (Reptilia: Squamata: Gekkonidae) in Mexico. J Med Entomol 46:442–450 Paredes-León R, García-Prieto L, Guzmán-Cornejo C, León-Regàgnon V, Pérez TM (2008) Metazoan parasites of Mexican amphibians and reptiles. Zootaxa 1904:1–166 Paredes-León R, Klompen H, Pérez TM (2012) Systematic revision of the genera Geckobiella Hirst, 1917 and Hirstiella Berlese, 1920 (Acari: Prostigmata: Pterygosomatidae) with description of a new genus for American species parasites on geckos formerly placed in Hirstiella. Zootaxa 3510:1–40 Pérez TM, Guzmán-Cornejo C, Montiel-Parra G, Paredes-León R, Rivas-Lechuga G (2014) Biodiversidad de Ácaros en México. Rev Mex Biodivers 85S:S399–S407 Prasad V (1975) A new genus and species of pterygosomatid mite (Acarina: Pterygosomatidae) from India. Int J Acarol 1:14–17 Pryce D, White L (2014) Scheloribates evanescens. The IUCN Red List of Threatened Species 2014: e.T64304382A64304387. https://doi.org/10.2305/IUCN.UK.2014-3.RLTS. T64304382A64304387.en. Downloaded on 10 July 2018 Semarnat. Secretaría del Medio Ambiente y Recursos Naturales. 2010. Norma Oficial Mexicana, NOM-059-SEMARNAT-2010, Protección ambiental-especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio- Lista de especies en riesgo. Publicada el 30 de diciembre de 2010 en el Diario Oficial de la Federación Shatrov AB, Kudryaashova NI (2006) Taxonomy, life cycles and the origin of parasitism in trombiculid mites. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and macroparasites. From evolutionary ecology to management. Springer, Tokyo. 647 p, pp 119–140. https://doi. org/10.1007/978-4-431-36025-4 Shatrov AB, Kudryaashova NI (2008) Taxonomic ranking of major trombiculid subtaxa with remarks on the evolution of host-parasite relationships (Acariformes: Parasitengona: Trombiculidae). Annales Zoologici (Warszawa) 58:279–287 Sidorchuk EA, Khaustov AA (2018) A parasite without host: The first fossil pterygosomatid mite (Acari: Prostigmata: Pterygosomatidae) from French Lower Cretaceous amber. Cret Res 91:131–139 Uetz P (2018) The Reptile Database. http://www.reptile-database.org. Accessed 11 June 2018. Vainstein BA (1978) System, evolution and phylogeny of trombidiform mites. In: Giljarov MS (ed) The determination keys of the soil-dwelling mites (Trombidiformes). Nauka, Moscow, pp 228–244, (In Russian) Vazquez-Díaz J, Gadsden H, Quintero-Díaz GE, Ponce-Campos P, Lavin P (2007) Sceloporus cyanostictus. The IUCN Red List of Threatened Species 2007: e.T64099A12738104. https:// doi.org/10.2305/IUCN.UK.2007.RLTS.T64099A12738104.en. Downloaded on 28 May 2018
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Chapter 12
Systematics of the Fish from the Cuatro Ciénegas Basin Héctor Espinosa-Pérez and Christian Lambarri-Martínez
Abstract The fish fauna of the Cuatro Ciénegas Basin (CCB) has been widely studied, and many aspects of its populations are known. Previous studies have, for example, clarified genetic identities and discovered new species and their feeding habits. Nevertheless, in the last two decades, there has been a notorious change in fish diversity, together with fluctuations in population numbers throughout seasons and years. It is known that anthropogenic activities have altered water levels and flow, resulting in the swamps’ desertification. Also, the introduction of at least two exotic species that compete with or prey upon native species has triggered its displacement and population decline. As a consequence, the unique and highly endemic fish diversity has drastically changed and is now in peril. We analyse and discuss the fish systematics under biogeographic, historical, ecological, and evolutionary perspectives, to offer a wide view of the ecosystem. The approach used in this study could contribute to the conservation of this desert aquatic environment and its biota. Keywords Diversity · Endemism · Coahuila · North America · Chihuahuan Desert
12.1 Introduction In order to delimit the challenges posed by the aquatic habitats within deserts, Soltz and Naiman (1981) took the definition of Goodall (1976) and interpreted the deserts as “areas where the biological potential is strongly limited by the water scarcity”. These authors stated that several decades of study would be necessary only to begin to approach the questions on the preservation of North American deserts. The problems that water scarcity brings are notorious in this chapter, where the fishes from the Cuatro Ciénegas Basin (CCB) are studied. This desert region, in the Chihuahuan Desert (CD) in Coahuila, is composed of several springs where the H. Espinosa-Pérez (*) · C. Lambarri-Martínez Colección Nacional de Peces, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico e-mail: [email protected] © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_12
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water flows superficially through geological fractures, forming therefore pools or swamps. These swamps are emblematic of this northern region of Mexico, and they join together in streams or rivers, forming important aquatic environments for fish and other organisms. The origin of the North American deserts, especially the CD, goes back to no more than 10,000 or 12,000 years, since the last pluvial period (Axelrod 1979; Smith 1981); therefore, the existence and isolation of aquatic organisms, fish among them, are due to several inter-pluvial periods (Hubbs and Miller 1948; Miller 1981) that resulted in the invasion and slow isolation of watersheds that became the arid region that we now know. Since the late Cretaceous, the CD configuration was formed by tectonic activity in western North America. This desert is then the result of a series of complex events that developed in the middle of North America during the early Cenozoic, between the Sierra Madre Occidental and the Sierra Madre Oriental mountain chains and the Trans-Mexican Volcanic Belt, which were formed since the Miocene (Atwater 1970; Gastril and Jensky 1973). The origin of the freshwater resources in central Mexico can be approached through the current freshwater network existing in the Central Plateau. Many of the contemporary water systems of north-central Mexico originated in the Bravo River watershed. Also, many of these tributaries have endemic fauna, and this endemism is evident in fish (Meek 1902, 1904; Smith and Miller 1986) (Fig. 12.1). There are clear differences regarding the composition of the fish fauna in current watersheds; the Central Plateau, limited to the south by the Trans-Mexican Volcanic Belt, is composed of northern fauna that comes from the Bravo River basin, such as fish of the family Cyprinidae in the Nazas-Aguanaval, Tunal, Mezquital, and Lerma Rivers. These rivers also share unique fish of the family Goodeidae and some singular vicariant species of the family Atherinopsidae, although the two latter ones are not found in the CCB or other regions north from the Bravo River. The CCB was declared a protected area by the Mexican government, a Ramsar site, and a biosphere reserve by UNESCO (Hendrickson et al. 2008; Souza et al. 2008). This rather small valley of about 1500 km2, also known as “Bolsón de Cuatro Ciénegas” because of its bucket shape, is an endorheic watershed that contains many aquatic habitats and at least 70 endemic species. It is surrounded by the Sierra de San Marcos to the south, San Vicente and La Purísima to the east, Sierra de la Fragua to the west, and Sierra de la Madera and Menchaca to the north-east and north-west, respectively. The extremely arid valley is located in the central region of Coahuila, and its endemic fauna inhabits the 200+ pools, rivers, and permanent lakes, whose origin is historically independent from the valley (Hendrickson et al. 2008). The valley’s nearest external drainage is the Salado de los Nadadores River in the Bravo River watershed, but there used to be no natural direct connection to the valley. Nevertheless, there are several man-made channels that take water out from the CCB for agricultural activities (Chavez-Campos et al. 2010). These novel waterways might have been the entrance for non-endemic species such as the longear sunfish Lepomis megalotis, which is now common throughout the valley.
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Fig. 12.1 Common and scientific names of fishes, (a) Cuatro Ciénegas shiner Cyprinella xanthicara (Minckley and Lytle, 1969); (b) Cuatro Ciénegas killifish Lucania interioris Hubbs and Miller, 1965; (c) Cuatro Ciénegas cichlid Herichthys minckleyi (Kornfield and Taylor, 1983); and (d) Tufa darter Etheostoma lugoi Norris and Minckley, 1997
If the importance of the desert’s origin and the water resources is acknowledged, it is imperative to ask the following questions: How is it possible to find fish that inhabit such extreme habitat conditions? Do desert fish have accumulated physiological characteristics that allow them to evolve anywhere? This contribution attempts to explore how the current species are distributed in the CCB, what are their origins, and for how long have they been there.
12.2 Diversity and Endemism The fish group in the CCB comprises 18 species with Nearctic and Neotropical affinities. This group is considered transitional and shows unique characteristics associated to the desert habitat. At least eight species, from the less evolutionarily derived to morphs of recent appearance, are endemic to the CCB. The orders Cypriniformes, Siluriformes, Characiformes, Cyprinodontiformes, Cichliformes, and Perciformes are represented in the area by species whose distribution and appearance in the CCB are analysed.
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12.2.1 Cypriniformes Cyprinidae. This is the most numerous family in freshwater ecosystems in the world and is distributed naturally in Africa, Eurasia, and North America, where they are also the most diverse group of fish, from southern Canada to southern Mexico. The most antique known fossil is from Asia (from the Eocene) and the most recent one from Europe. In North America, all of the fossils are from the Oligocene. Cavender (1991) showed evidence of the absence of the cyprinids in America during the Eocene, when the Catostomidae and Ictaluridae were already present. Cyprinids in North America belong to the non-monophyletic subfamily Leuciscinae, and in the CCB there are two species in two genera. Cyprinella xanthicara (Fig. 12.1a) is a sister species of C. rutila, from which it separated and became isolated vicariantly during the Pleistocene; although it is possible that this species is actually more related to C. panarcys and C. garmani (from Chihuahua and Durango) than to C. rutila (Lambarri-Martínez 2017). There is also the possibility that the CCB specimens represent more than one species that belong to more than one lineage. The type locality of C. xanthicara is the (now gone) Puente Colorado River in the CCB. Within the valley, it was also found in Churince River and Intermedia Lagoon, which dried out. The species remains in La Becerra pool; Garabatal, Mezquites, and Puente Chiquito Rivers; and Juan Santos, Tío Cándido, and Santa Tecla pools. Dionda episcopa has been considered to be a polytypic species distributed in the Colorado, Bravo, Conchos, and Mezquital Rivers. But for more than 50 years, it has been thought to be a sympatric and widespread species complex. Several isolated populations of D. episcopa from Texas, Chihuahua, and Durango have been found to belong to different lineages (Mayden et al. 1992; Schönhuth et al. 2008; Lambarri- Martínez 2017), and it is highly plausible that there are two sympatric species in the CCB. If this is the case, neither one of these species would be Dionda episcopa but would belong to a clade related to other cyprinids in Chihuahua and to the Dionda melanops clade, respectively (Lambarri-Martínez 2017).
12.2.2 Characiformes Characidae. This family of Neotropical origin is quite diverse in Central and South America. It is nominally monophyletic, but relationships among species and genera are still to be clarified. According to Schmitter-Soto (2017), there are two species that inhabit the Nearctic region in the Bravo River and the western slope of the Gulf of Mexico (Burr and Mayden 1992): Astyanax mexicanus, which inhabits adjacent areas to the northeastern coast of Mexico, and A. argentatus, which inhabits the Bravo River basin. The latter species would be the same morph as the one found in the CCB. However Sepúlveda (2012) separated the CCB morph from others outside the basin, based on three loci and several characters that are distinct from A. argentatus.
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Little is known about the origins of the Characidae in North America. Chakrabarty and Albert (2011) revised several Neotropical fish phylogenies and suggested that the southern fish invasion of America is explained by biogeographical events in Central and South America. Schmitter-Soto (2012) stated that the closing of the Isthmus of Panama during the Plio-Pleistocene (2–3 million years ago) allowed fish invasions and faunal exchange, as did a first closure of the Central American Isthmus during the Paleocene (58–60 million years ago) (Iturralde-Vinent 2006). The presence of A. argentatus in the CCB could be explained by these invasions, which allowed it to get into the Bravo River province and later became isolated in the CCB. Once isolated, another morph derived; Sepúlveda (2012) consider this morph to be an undescribed species or a population still in speciation processes.
12.2.3 Siluriformes Ictaluridae. The so-called freshwater catfishes are an endemic family to North America, easily distinguishable by their rostral barbels. The family includes seven genera and over 45 species, including several blind ones. The genus Ictalurus, the one found in the CCB, comprises ten species, five of which are endemic to Mexico; and I. lupus is considered to be native to the Bravo River region. Grande and Lundberg (1988) revised the Eocene North American fossils and found that the fossil genus Astephus is the sister group of all the Ictaluridae that appeared in the Oligocene and that Ictalurus appeared in the last part of the Pliocene (Hubbs and Hilbbard 1951). Ictalurus cf. lupus. This species inhabits the Gulf of Mexico slope from the Pecos and Bravo Rivers to the Nueces River in Texas. It can be found in San Fernando and Soto La Marina Rivers in Tamaulipas, in San Juan and El Salado in Nuevo León, and in Coahuila, although it does not reach the Conchos River. Because of its isolation, the CCB population is thought to be different from I. lupus. The morphs and its taxonomic position, along with others from northeastern Mexico, are currently being discussed.
12.2.4 Cyprinodontiformes Fundulidae. Although the Cyprinodontiformes originated in northern Africa and southern Europe, the family Fundulidae currently inhabits southern Canada, the eastern and southern regions of the United States, Mexico, Cuba, and Bermuda. The relationships within the family are poorly understood; however, Parenti (1981) stated that Fundulus is the sister group to other genera, including Lucania, which forms an unresolved trichotomy with Plancterus (Burr and Mayden 1992). The group’s time of appearance is also poorly known, but it should be related to the
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continental breakup that produced a completely different North American clade. There are three species in Lucania: L. goodie that occurs in the eastern United States, from Massachusetts to Florida; L. parva with the same distribution in the north but also found along the Gulf of Mexico coast, reaching Yucatan, and in the Bravo and Pecos Rivers. L. parva is thought to be the sister group of L. interioris. Lucania interioris (Fig. 12.1b) is known from a few localities within the region. It inhabits pools in the southern portion of the CCB and is considered to be a small (no more than 3.5 cm TL) and rare species in the area (Miller et al. 2005). It is hypothesized that its arrival time to the CCB coincided with that of the family Centrarchidae, as a reminiscence of the fauna of the Mississippi River. Cyprinodontidae. Fish of the order Cyprinodontiformes originated in the Tethys Sea (Parenti 1981), but the present Cyprinodontidae inhabit fresh, estuarine, and marine coastal waters from the United States, through Mexico and Central America, to South America, North Africa, and the Mediterranean. There are several species restricted to continental waters in the southern United States and northern Mexico that are thought to have evolved from coastal species such as Cyprinodon variegatus (Echelle and Echelle 1992); two of them are present in the CCB. These species could have originated from populations in the Bravo River or the Guzmán basin and later became isolated inside the CCB. Cyprinodon atrorus, as described by Miller et al. (2005), finds in the CCB pools a suitable environment, even with the adverse temporal and seasonal variations. This species can hybridize with C. bifasciatus (Minckley and Deacon 1991), and although the latter tends to disappear when C. atrorus is abundant, there are regions of introgressive hybridization and pools where each species still exists independently (Carson and Dowling 2006). Cyprinodon bifasciatus’ habitat is confined to thermal and isolated springs with constant water flow, although in the hot season it moves to ditches, channels, and sulphurous waters. This fish is an active predator and competes with bigger species such as native and exotic cichlids. The so-called pupfish lives in big schools, and juveniles usually stay in sandy bottoms (Miller et al. 2005). It is thought that hybridization has resulted in the loss of several populations of this species, now substituted by C. atrorus-C. bifasciatus hybrids. Populations of C. bifasciatus in other pools, where the jewelfish Hemichromis guttatus has been introduced, have also been reduced or disappeared completely. Poeciliidae. This family is thought to be a monophyletic group (Parenti 1981) and includes the Cyprinodontiformes viviparous group that inhabits waters from North America, the Caribbean, and South America to northern Argentina, and Congo and Madagascar in Africa. This group includes about 220 species, three of which occur in the CCB: two of the genus Gambusia and one of Xiphophorus. These species belong to two different subtribes that arrived from the neotropics to northern and more temperate areas in Mexico and the United States. Together with other species, they have formed a distinct fish fauna that managed to invade the Bravo River basin to later become isolated. Gambusia marshi is a small species closely related to G. senilis, which inhabits several rivers in the Bravo River basin. A sister species to G. marshi occurs also in
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the CCB but cannot be readily differentiated from it. The undescribed species is distributed in almost every pond and can even be found in El Salado River because of its communication with the ponds through artificial channels. This polymorphic complex (Raunchenberger 1989) shows a particular colouration in the eastern ponds, which could be a different species from the one in the western ponds as Churince, where they show colouration and shape variations between males and females (Minckley 1981). Some aspects of the biology of these species were analysed by Hernández et al. (2017), and Moody et al. (2018) revised the nitrogen intake of the species. Gambusia longispinis is an inconspicuous species, sister of G. marshi, distributed only in the CCB (Minckley 1978; Miller et al. 2005). Its habitat, unlike G. marshi, is in clear, shallow, ephemeral waters with little to no flow that tend to dry in the hottest seasons. The disappearance of its habitat is one of the causes why the species is considered seriously endangered. Xiphophorus gordoni is thought to be sister species of X. couchianus, which inhabits the San Juan River basin in Nuevo León, part of the Bravo River basin. It used to be isolated in the southeastern portion of the CCB (Miller et al. 2005) but has now disseminated through the channels up to the Nadadores River (Contreras- Balderas 1987). Carson et al. (2013) documented the phylogeography of the species and recorded the localities and thermal waters where the species occurs.
12.2.5 Cichliformes Cichlidae. The cichlids are one of the most diverse freshwater fish families in the world, mostly because of their tolerance to different salinity conditions. They are defined as a secondary family (Myers 1938). The family includes over 1900 species (Kullander 1998) distributed in Africa, Iran, India, Sri Lanka, and Madagascar, and throughout the American continent, including Cuba and Hispaniola. Stiassny (1981) proposed its monophyly based on four apomorphic characters. Three species inhabit the CCB: the exotic and invasive Hemichromis guttatus and two species of the genus Herichthys (Říčan et al. 2016; Pérez-Miranda et al. 2018). Herichthys cyanoguttatus is the most northern native cichlid in Mexico. It is distributed in the Bravo, Nueces, San Fernando, and Soto La Marina Rivers. Its sympatric distribution within the CCB with H. minckleyi has been associated with the introduction of nonnative species (Miller et al. 2005). Herichthys minckleyi (Fig. 12.1c) is endemic to the CCB and is absent from the Bravo River basin. There are two morphs of this polymorphic species that differ in their pharyngeal teeth; Liem and Kaufman (1984) suggested them to be in an early phase of speciation, and Miller et al. (2005) considered the existence of a third piscivorous form with divergent cranial structure and body shape.
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12.2.6 Perciformes Centrarchidae. The evolutionary relationships among several lineages within the family are not clear yet, resulting in different hypotheses about its internal structure (Burr and Mayden 1992). On the basis of numerous fossils, this group is known to be endemic to North America (Cavender 1986), in particular to eastern North America, except for one species that occurs in the west. There could be up to three sunfish species in the CCB, with two of them still undescribed. Lepomis megalotis inhabits rivers of eastern and central North America, from Canada to the Bravo and Conchos Rivers, in Chihuahua, Coahuila (CCB), Nuevo León, and Tamaulipas. As many other species in the CCB, this species is thought to be an independent lineage from the northern ones and has been isolated for a long time. Several introductions, however, could imperil it through hybridization, predation, and competition (Miller et al. 2005). Micropterus salmoides is also native to North America: being distributed from southern Canada, to the Bravo, San Fernando, and Soto La Marina Rivers and the CCB. However, it has been widely introduced for sport fishing and aquaculture throughout both Mexico and the United States. Again, as most of the species in the CCB, it is thought to be a species complex with one or more undescribed taxa that are in risk of disappearing because of the introduction of northern M. salmoides specimens. Percidae. Johnson (1984) and Wiley (1992) supported this family’s monophyly, but recent molecular studies are now challenging this view. Percidae is a species- rich family, and the genus Etheostoma is the most diverse in North America. E. lugoi occurs in the CCB, and E. segrex was described from the waters just outside the valley. Etheostoma lugoi (Fig. 12.1d) is the only species of the genus and the family that inhabits the CCB, being restricted to the Mezquital River system. Its habitat preferences include gravel bottoms with little or no vegetation (Miller et al. 2005). The valley isolation allowed the separation of E. lugoi from E. segrex; which differ essentially in their distribution, one in the CCB and the other one in the Nadadores River; and in the number and articulation of branchiostegal rays, but these characters also vary greatly within populations of both species. Despite the fact that their evolutionary relationships are still unresolved, it seems that both species are closely related to E. grahami, which inhabits the Bravo River in Coahuila and Texas. E. segrex is apparently extinct, and E. lugoi has disappeared from many areas within its range.
12.3 Conservation Status The conservation status of the fish species from the CCB has been summarized considering both the IUCN Red List (IUCN 2018) and the NOM-059- SEMARNAT-2010 (SEMARNAT 2010) (Table 12.1). Although most of the CCB fish species are in a risk category in both lists, several taxa are undescribed or their populations not studied enough to declare what their conservation status might be.
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Table 12.1 Risk categories of the Cuatro Ciénegas Basin fish species according to the Mexican Red List (NOM-059-SEMARNAT-2010) and the IUCN Red List Species Cyprinella xanthicara (Minckley and Lytle, 1969) Dionda cf. episcopa Girard, 1856 Astyanax argentatus Baird and Girard, 1854 Ictalurus cf. lupus (Girard, 1858)
NOM-059- SEMARNAT-2010 IUCN Red List Endemic Endangered Endangered
Lucania interioris Hubbs and Miller, 1965 Cyprinodon atrorus Miller, 1968
Endemic ND Not endemic Endemic Endemic
Cyprinodon bifasciatus Miller, 1968
Endemic
Gambusia marshi Minckley and Craddock, 1962 Gambusia longispinis Minckley, 1962 Xiphophorus gordoni Miller and Minckley, 1963 Herichthys cyanoguttatus Baird and Girard, 1854 Herichthys minckleyi (Kornfield and Taylor, 1983) Lepomis megalotis (Rafinesque, 1820) Micropterus salmoides (Lacepède, 1802) Etheostoma lugoi Norris and Minckley, 1997
Not endemic Endemic Endemic ND
Endangered Least concern ND Protected Data deficient Endangered Critically endangered Threatened Lower risk/least concern Threatened Lower risk/least concern Threatened ND Threatened Vulnerable Endangered Endangered Least concern
Endemic
Endangered Vulnerable
ND ND Endemic
Least concern Least concern Endangered ND
ND no available data
12.4 Discussion Herein we examined the systematics and biogeography of the fish of the CCB in order to explore when and how they arrived to this basin, which is subject to the extreme environmental conditions of the CD. The pools in the CCB are thought to be, as the stromatolites in some of them (Souza et al. 2008), geologically old and with different and independent histories, such as the fish that inhabit them. Fish origins could be explained by several independent arrivals or invasions of the CCB that were followed by complex orographic events, which formed sierras that isolated the basin, although Axelrod (1979), Smith (1981), Hubbs and Miller (1948), and Miller (1981) proposed that the water and fish fauna arrived through subterranean channels and various pluvial floods. Most of the fish came to the CCB from the Bravo River basin, which apparently was much bigger than it is today and had many large lagoons that reached the center of the state of Jalisco to the south and a wide region of Chihuahua in the Guzmán
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basin (Smith 1981). Some other species came from the Mississippi basin, whereas others are considered to be vicarious (sensu Myers 1966) or peripheral, such as the Cyprinodontiformes that originated from marine populations and were trapped when the continent emerged. Finally, there is another component with a southern affinity that could be older than previously thought in the CCB. The Nearctic fauna, composed of Ictalurus cf. lupus and at least two cyprinids (C. xanthicara and Dionda sp.), came originally from Asia through the Bering Sea to North America in the Oligocene (Cavender 1991), but their arrival to the CCB might have been until the Miocene. The Centrarchidae came along with the Mississippi fauna, between the Miocene and Pleistocene, and occupied large flooded regions that were eventually fragmented by new mountains and later became a desert. The fossil Micropterus relictus, found in Jalisco (Smith 1981), south of the CCB, suggests that the invasion could have been in the late Pleistocene, along with families such as Percidae (Etheostoma spp.). In contrast, the cichlids of the CCB are thought to be the most ancient neotropical fauna in North America (Mejía et al. 2015). Fossils of more tropical fish have not been found, except for some Poeciliidae from the Eocene in Central America (Álvarez and Aguilar 1957); but the isthmus through which the fish must have crossed is proposed to have closed in the Eocene, suggesting that the invasions occurred when the area was occupied by tropical forests that later dried out into a desert. Once in this region, generalist fish adapted and survived the high temperatures and desiccation pressures. However, more of the history of the CCB fish is still to be discovered. Here we highlighted some changes in the alpha taxonomy that new methods of analysis are producing, changing the traditional knowledge on the fish species from the CCB. This paper began with a statement on how long it would still take to propose a hypothesis on the origins of the desert fauna, which is in fact harder to work out regarding the CCB fauna and its relatives. But it is urgent to make progress since anthropogenic activities and pollution are quickly threatening species and ecosystems as unique as these. Acknowledgements We thank Valeria Souza for inviting us to participate in several field trips to Cuatro Ciénegas. We acknowledge the financial support of Alianza WWF-Fundación Carlos Slim.
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Chapter 13
Diversity of Amphibians and Reptiles in the Cuatro Ciénegas Basin Uri Omar García-Vázquez, Marysol Trujano-Ortega, Arturo Contreras- Arquieta, Omar Ávalos-Hernández, Omar Osvaldo Escobedo-Correa, and Pablo Corcuera
Abstract We gathered and analyzed the current knowledge of the amphibians and reptiles of the Cuatro Ciénegas Basin (CCB), including their biogeographical affinities and the historical and ecological importance of the basin to the diversity of these groups in the Chihuahuan Desert (CD). The CCB has a characteristic topography with alternating highlands and basins. The degree of endemicity of the fauna within the CCB is one of the highest in North America. Morphological and genetic differentiation of these taxa suggests a quick speciation due to the isolation of the basin. Further, the restricted distribution within the CCB of some taxa indicates a high ecological dependence on aquatic microhabitats. The herpetofauna present in the CCB is composed of seven amphibian and 46 reptile species, from which 2 amphibians and 9 reptiles are endemic to the basin. Bufonidae and Colubridae are the most diverse families, while Lithobates berlandieri and Aspidoscelis inornata cienegae are the most abundant species of Amphibia and Reptilia, respectively. Twelve of the previously reported species had not been recorded recently, but we recorded five U. O. García-Vázquez (*) Laboratorio de Sistemática Molecular, Unidad de Investigación Multidisciplinaria de Investigación Experimental Zaragoza, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México, Ciudad de México, Mexico M. Trujano-Ortega · O. Ávalos-Hernández Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico A. Contreras-Arquieta Acuario y Herpetario W. L. Minckley, Cuatro Ciénegas de Carranza, Coahuila, Mexico O. O. Escobedo-Correa Departamento de Biología, Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico P. Corcuera Laboratorio de Ecología Animal, Departamento de Biología, Universidad Autónoma Metropolitana-Iztapalapa, Ciudad de México, Mexico © Springer Nature Switzerland AG 2019 F. Álvarez, M. Ojeda (eds.), Animal Diversity and Biogeography of the Cuatro Ciénegas Basin, Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis, https://doi.org/10.1007/978-3-030-11262-2_13
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species for the first time in the CCB. Most of the species are distinctive of the CD; however, the endemic species are more closely related with taxa of the Tamaulipan province, Edwards Plateau, and the Sierra Madre Oriental province. Keywords Amphibian · Reptiles · Endemism · Behavior · Biogeographic affinities · Chihuahuan Desert
13.1 Introduction The diverse herpetofauna is one of the most important elements of the Mexican fauna (Flores-Villela and Gérez 1994). An estimated 864 species of reptiles are distributed in Mexico, described in 159 genera and 40 families, which constitute 8.7% of the reptiles worldwide. Of these 864 species, 417 are lizards, 393 snakes and vipers, 48 turtles, 3 amphisbaenians, and 3 crocodiles. Also, 493 taxa are endemic to Mexico (Flores-Villela and García-Vázquez 2014). On the other hand, amphibians are one of the most diverse groups of vertebrates with 376 species in Mexico, classified into 16 families in three orders; this places Mexico as the country with the fifth highest diversity of this group. The degree of endemism is high, considering that more than 50% of the species in seven families are endemic to Mexico, including seven endemic genera, three anurans, and four salamanders (Parra-Olea et al. 2014). Amphibians and reptiles are key groups in xeric environments, being found in very specific and particular sites. The two groups participate in the natural control of populations of potentially harmful vertebrate and invertebrate species. Amphibians, in particular, are associated with aquatic habitats, which makes them vulnerable to perturbations produced by pollution, desiccation, and global warming. They are considered great bioindicators of the ecosystem health. As for the reptiles, some species are closely associated with specific habitats and, therefore, sensitive to anthropogenic modifications (Kremen 1992; Colwell and Coddington 1994; Fitzgerald et al. 2004). The CCB in Coahuila, Mexico, is a unique region in the CD because of its water reservoirs. It contains one of the most endemic-rich faunas of North America, which includes, among others, aquatic snails, isopod crustaceans, fishes, turtles, and lizards (García-Vázquez et al. 2010). Particularly, amphibians and reptiles are possibly the most studied groups of vertebrates in the CCB, because of their high degree of endemism. Milstead (1960) recognized three amphibian and seven reptile species from the CCB as relicts. These are mesic-adapted species in the CD, existing in the region as apparently disjunct populations considerably apart from the main portion of the range of the species. Later, McCoy (1984) reported 66 native species to the CCB (8 amphibians and 58 reptiles) and 2 introduced reptile species. Of these, 41 were typical desert species, 13 riparian, 6 semiaquatic, and 6 exclusively aquatic. In the last study of the herpetofauna from Coahuila, Lemos-Espinal and Smith (2016) reported 24 species of amphibians and 109 of reptiles, of which 4 species are endemic to the CCB. However, these authors considered Gerrhonotus lugoi McCoy, 1970, as endemic, a species recently reported in Nuevo León (García-Vázquez et al. 2016); additionally, they omitted in their list of endemics Craugastor augusti fuscofemora Zweifel, 1956, Aspidoscelis inornatus cienegae (Wright and Lowe 1993),
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and Aspidoscelis gularis pallidus (Duellman and Zweifel 1962); all of them exclusive to the CCB. Finally, García-Vázquez et al. (2018a) described Gerrhonotus mccoyi García-Vázquez, Contreras-Arquieta, Trujano-Ortega, and Nieto-Montes de Oca, 2018, a new endemic species of the CCB. Previous studies summarize the historical records of the last 70 years; however, there are no recent ecological studies which assess the current diversity of these groups in the CCB. We present a systematic faunistic study of the amphibians and reptiles in the CCB. The diversity, abundance, species richness, origin, and biogeographical affinities are analyzed. This study will contribute to the understanding of the current vertebrate communities of the CCB and particularly of the human activities which are impacting these species.
13.2 Materials and Methods We selected seven sites in three localities: (1) Las Teclas in Antiguos Mineros del Norte; (2) Mezquital, Poza Bonita, Poza Churince, and Poza de en Medio in Churince; and (3) Poza Escobedo and Poza Tío Cándido in Rancho Orozco. These sites were selected according to size, environmental heterogeneity, and previously observed diversity of each locality (Fig. 13.1). All localities have superficial water,
Fig. 13.1 Map of study sites within the Cuatro Ciénegas Basin, Coahuila
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except Mezquital. Most localities present some degree of perturbation due to the presence of cattle, crops, and tourism. The main vegetation types in the CCB are grasslands, sedge marshes, gypsum dunes, desert scrub, and chaparral (Pinkava 1979, 1984). The mean annual temperature is 21.4 °C and ranges from 12 °C in the coldest months to 28 °C in the warm season. Annual seasonal precipitation averages 200 mm, and the rainy season extends from May through December (INEGI 1994). Most habitats present in the CCB were included: sotol, mesquite, secondary grassland, and semiaquatic vegetation associated with ponds.
13.2.1 Fieldwork Fourteen field trips were made from 2012 to 2013 in order to determine and count the amphibians and reptiles found on each site. In addition, we included records from the literature and made sporadic trips in 2009, 2010, 2014, and 2015 to complete the taxonomic composition. Only the field records in 2012 and 2013 were included in the statistical analysis. The sampling effort involved 72 days with at least three collectors each day. To make sure to include diurnal, crepuscular, and nocturnal species, samplings were performed from 9:00 to 16:00 and 19:00 to 23:00 hours. Within each site, we sampled all of the main habitats with a procedure that included opportunistic searching and linear transect surveys that varied in length depending upon the amount of habitat available (Campbell and Christman 1982).
13.2.2 Taxonomic Determination We identified all of the observed amphibians and reptiles with Lemos and Smith (2007) field guide and also verified the correct identifications with the specimens kept in the Herpetological Collection of the Zoological Museum “Alfonso L. Herrera” of the Facultad de Ciencias, UNAM.
13.2.3 Data Analysis We assessed the sampling efficiency with the Jackknife 1 and Chao 1 estimators (Colwell 2006). The two estimators are reliable for relatively small sampling units (i.e., circular plots; Hortal et al. 2006). In addition, they are less dependent on sampling intensity than other estimators (Colwell and Coddington 1994; Hortal et al. 2006). We used rarefaction techniques to compare and to assess if the number of species between years was significantly different. In order to test if there were
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differences of the relative reptile abundance between years among sites, we used an Χ2 goodness of fit test. Dominance, diversity, and evenness were calculated with the Simpson, Shannon-Wiener, and Pielou indexes. Similarities between localities with similar sampling efforts were estimated with the Bray-Curtis index. Lastly, biogeographic affinities were determined with specialized literature considering two regions, Nearctic and Neotropical (Morrone et al. 2002).
13.3 Results The herpetofauna of the CCB is composed of 5 amphibian and 14 reptile families, including 6 genera and 11 species of amphibians and 37 genera and 61 species of reptiles, from which 2 amphibians and 9 reptiles are endemic to the CCB. Colubridae with 23 taxa, Phrynosomatidae with 11 taxa, and Bufonidae and Viperidae with 5 taxa each were the most diverse families. Seven families were represented by only one species. Teiidae was the most abundant family with 413 observed specimens, followed by Phrynosomatidae with 286, Ranidae with 166, and Scincidae with 152; seven families were represented by 10 or fewer organisms. Specifically, Aspidoscelis inornatus cienegae (Teiidae) and Lithobates berlandieri (Baird, 1859) (Ranidae) were the most dominant species on both spatial and temporal scales. We found one taxon that had not been previously recorded in Coahuila (Salvadora grahamiae grahamiae (Baird and Girard,1853)), and three are new to the state and endemic for the CCB (Eleutherodactylus sp. nov., Storeria sp. nov., and Gerrhonotus mccoyi). On the other hand, 12 taxa that had been previously collected in the CCB were not observed in this study.
13.3.1 Species Richness We found from 75 to 89% of the estimated species in 2012 and 74% of the estimated richness in 2013, according to Chao 1 and Jackknife 1 estimators (Table 13.1, Fig. 13.2). Because the confidence intervals between years overlapped, the number of species was not significantly different between the two years (Fig. 13.3). Table 13.1 Number of observed species and percentage of the expected richness in the Cuatro Ciénegas Basin, Coahuila, according to the Chao 1 and Jackknife 1 estimators Year 2012 2013
Observed 21 17
Chao 1 (%) 88.8 74.0
Jack 1 (%) 75.4 73.9
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Fig. 13.2 Species richness of amphibians and reptiles from the Cuatro Ciénegas Basin, Coahuila
Fig. 13.3 Species observed of amphibians and reptiles from the Cuatro Ciénegas Basin, Coahuila
13.3.2 Diversity There was a significant difference in the number of individuals among the seven sites between the two years (X2 = 116.03, 6 df, p