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Insect–Fungal Associations: Ecology and Evolution Fernando E. Vega Meredith Blackwell, Editors OXFORD UNIVERSITY PRESS Insect–Fungal Associations This page intentionally left blank Insect–Fungal Associations Ecology and Evolution Edited by Fernando E. Vega Meredith Blackwell 1 2005 3 Oxford New York Auckland Bangkok Buenos Aires Cape Town Chennai Dar es Salaam Delhi Hong Kong Istanbul Karachi Kolkata Kuala Lumpur Madrid Melbourne Mexico City Mumbai Nairobi São Paulo Shanghai Taipei Tokyo Toronto Copyright © 2005 by Oxford University Press, Inc. Published by Oxford University Press, Inc. 198 Madison Avenue, New York, New York 10016 www.oup.com Oxford is a registered trademark of Oxford University Press All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, without the prior permission of Oxford University Press. Library of Congress Cataloging-in-Publication Data Insect-fungal associations : ecology and evolution / edited by Fernando E. Vega, Meredith Blackwell. p. cm. Includes bibliographical references. ISBN 0-19-516652-3 1. Fungi as biological pest control agents. 2. Insect pests—Biological control. 3. Fungi in agriculture. 4. Insect-fungus relationships. I. Vega, Fernando E. II. Blackwell, Meredith. SB976.F85 I57 2004 987654321 Printed in the United States of America on acid-free paper It is not only poets who are interested in puzzles. All of us live in basic mystery. Science and religion jostle one another in the shadows, throwing in each other’s eyes the dust of beauty, possibilities, distant myths, and approximate truth. Pablo Neruda Passions and Impressions This page intentionally left blank Acknowledgments F.E.V. thanks Pedro Barbosa, Pat Dowd, and Eric Rosenquist. Also, thanks are due to Ann Sidor, Francisco Posada, and Monica Pava-Ripoll for their superb work in the Beltsville laboratory. Special thanks to Wendy and Ian, for being so wonder- ful and for their love. M.B. thanks Sung-Oui Suh and undergraduate students in- cluding Christine Ackerman, Katie Brillhart, Cennet Erbil, Nhu Nguyen, and Amy Whittington, who keep her lab productive. Thanks also to James Kimbrough and Quentin Wheeler, who first showed her the insect fungi, and David Malloch, with whom she pursued the origin of euascomycetes without mycelium. Renée, Elise, David, and Esme provide support. We both thank Kirk Jensen, our initial editor at Oxford University Press, for taking on this project, and Anne Rockwood for helping us to complete it. We also thank Lisa Stallings and Rosanne Hallowell at Oxford University Press for overseeing the copy-editing and production, and Lisa Hamilton for the cover design. Thanks also to Sung-Oui Suh, who helped with proofreading. This page intentionally left blank Contents Introduction: Seven Wonders of the Insect–Fungus World xiii Meredith Blackwell and Fernando E. Vega Part I. Fungi Acting against Insects 1. Phylogenetics of the Insect Pathogenic Genus Beauveria 3 Stephen A. Rehner 2. Phylogeography of Metarhizium, an Insect Pathogenic Fungus 28 Michael J. Bidochka and Cherrie L. Small 3. Interactions between Entomopathogenic Fungi and Arthropod Natural Enemies 51 Michael J. Furlong and Judith K. Pell 4. Ecology and Evolution of Fungal Endophytes and Their Roles against Insects 74 A. Elizabeth Arnold and Leslie C. Lewis 5. The Fungal Roots of Microsporidian Parasites 97 Naomi M. Fast and Patrick J. Keeling 6. Fungal Biotrophic Parasites of Insects and Other Arthropods 119 Alex Weir and Meredith Blackwell x Contents Part II. Fungi Mutualistic with Insects 7. Reciprocal Illumination: A Comparison of Agriculture in Humans and in Fungus-growing Ants 149 Ted R. Schultz, Ulrich G. Mueller, Cameron R. Currie, and Stephen A. Rehner 8. Evolutionary Dynamics of the Mutualistic Symbiosis between Fungus-Growing Termites and Termitomyces Fungi 191 Duur K. Aanen and Jacobus J. Boomsma 9. The Role of Yeasts as Insect Endosymbionts 211 Fernando E. Vega and Patrick F. Dowd 10. The Beetle Gut as a Habitat for New Species of Yeasts 244 Sung-Oui Suh and Meredith Blackwell 11. Ecology and Evolution of Mycophagous Bark Beetles and Their Fungal Partners 257 Thomas C. Harrington Conclusion: Symbioses, Biocomplexity, and Metagenomes 293 Fernando E. Vega and Meredith Blackwell Index 297 Contributors Duur K. Aanen, Department of Population Ecology, Zoological Institute, University of Copenhaguen, Universitetsparken 15, 2100 Copenhagen, Denmark A. Elizabeth Arnold, Department of Biology, Duke University, Durham, North Carolina 27708, USA Michael J. Bidochka, Department of Biological Sciences, Brock University, St. Catharines, Ontario L2S 3A1, Canada Meredith Blackwell, Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, USA Jacobus J. Boomsma, Department of Population Ecology, Zoological Institute, University of Copenhaguen, Universitetsparken 15, 2100 Copenhagen, Denmark Cameron R. Currie, Department of Ecology and Evolutionary Biology, Haworth Hall, University of Kansas, Lawrence, Kansas 66045, USA Patrick F. Dowd, Crop Bioprotection Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Peoria, Illinois 61642, USA Naomi M. Fast, Department of Botany, University of British Columbia, 3529- 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada Michael J. Furlong, Department of Zoology and Entomology, School of Life Sciences, University of Queensland, Brisbane 4072, Queensland, Australia Thomas C. Harrington, Department of Plant Pathology 221 Bessey Hall, Iowa State University, Ames, Iowa 50011, USA Patrick J. Keeling, Department of Botany, University of British Columbia 3529- 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada xi xii Contributors Leslie C. Lewis, Corn Insects and Crop Genetics Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Ames, Iowa 50011, USA Ulrich G. Mueller, School of Biological Sciences, University of Texas, Austin, Texas 78712, USA Judith K. Pell, Division of Plant and Invertebrate Ecology, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, England Stephen A. Rehner, Insect Biocontrol Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Bldg. 011A, Beltsville, Maryland 20705, USA Ted R. Schultz, Department of Systematic Biology, MRC 188, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA Cherrie L. Small, Department of Biological Sciences, Brock University, St. Catharines, Ontario L2S 3A1, Canada Sung-Oui Suh, Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, USA Fernando E. Vega, Insect Biocontrol Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Bldg. 011A, Beltsville, Maryland 20705, USA Alex Weir, Environmental and Forest Biology, SUNY College of Environmental Science and Forestry, 350 Illick Hall, 1 Forestry Drive, Syracuse, New York 13210, USA Introduction: Seven Wonders of the Insect–Fungus World Meredith Blackwell Fernando E. Vega This book first arose out of a passage in Borges, out of the laughter that shattered, as I read the passage, all the familiar landmarks of my thought—our thought, the thought that bears the stamp of our age and our geography—breaking up all the ordered surfaces and all the planes with which we are accustomed to tame the wild profusion of existing things, and continuing long afterwards to disturb and threaten with collapse our age-old distinction between the Same and the Other. This passage quotes a “certain Chinese encyclopaedia” in which it is written that “animals are divided into: (a) belonging to the Emperor, (b) embalmed, (c) tame, (d) sucking pigs, (e) sirens, (f) fabulous, (g) stray dogs, (h) included in the present classification, (i) frenzied, (j) innumerable, (k) drawn with a very fine camelhair brush, (l) etcetera, (m) having just broken the water pitcher, (n) that from a long way off look like flies.” In the wonderment of this taxonomy, the thing we apprehend in one great leap, the thing that, by means of the fable is demonstrated as the exotic charm of another system of thought, is the limitation of our own, the stark impossibility of thinking that. Michel Foucault The Order of Things Insects and fungi share a long history of association in the common habitats where they endure similar environmental conditions. Only relatively recently did mycolo- gists stop killing the fungus-destroying insects they collected with their specimens and entomologists realize the fungal influence on insects. Prompted by an interest in understanding the associations between the two groups of unrelated organisms, an opportunity for people with interests in the interactions between the insects and fungi arose. Quentin Wheeler, a proponent of cladistic analysis, hoped to find new xiii xiv Introduction: Seven Wonders of the Insect–Fungus World disciples for Hennig among mycologists and hoped to encourage entomologists and mycologists to work together to understand the interactions among the speciose groups of organisms. A symposium organized by Wheeler and one of us (M.B.) was held at the Entomological Society of America, Eastern Branch, meeting at Syracuse and then at Ithaca, New York, in 1981. An edited book was an outcome of the gathering (Wheeler and Blackwell 1984). Some people only noticed the book when it hit the remainder tables, and oddly enough a single—although five star— Amazon.com
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  • Survey of Leaf-Cutting Ant Species in Native Vegetation and Monocultures in the State of Goiás, Brazil Levantamento De Espécie

    Survey of Leaf-Cutting Ant Species in Native Vegetation and Monocultures in the State of Goiás, Brazil Levantamento De Espécie

    Bol. Mus. Para. Emílio Goeldi. Cienc. Nat., Belém, v. 15, n. 1, p. 237-241, jan.-abr. 2020 Survey of leaf-cutting ant species in native vegetation and monocultures in the State of Goiás, Brazil Levantamento de espécies de formigas cortadeiras em vegetação nativa e monoculturas no estado de Goiás, Brasil Filipe Viegas de ArrudaI | Marcos Antônio PesqueroII | Marcos Filipe PesqueroIII | João Danillo dos SantosIII IUniversidade Estadual de Goiás. Programa de Pós-Graduação em Recursos Naturais do Cerrado. Anápolis, Goiás, Brasil IIUniversidade Estadual de Goiás. Morrinhos, Goiás, Brasil IIIUniversidade Federal do Tocantins. Porto Nacional, Tocantins, Brasil Abstract: Leaf-cutting ants are distributed exclusively in the Americas. For this study, we sampled different areas of native vegetation and monocultures to survey the leaf-cutting ants that occur in the State of Goiás, and to what environments they are associated. We recorded six species of leaf-cutting ants: Atta sexdens, Atta laevigata, Acromyrmex subterraneus, Acromyrmex disciger, Acromyrmex ambiguus, and Acromyrmex hispidus. The last four were registered for the first time for the State of Goiás. Keywords: Savanna. Colony density. Agriculture. Diversity. Resumo: As formigas cortadeiras apresentam distribuição exclusiva nas Américas. Durante a realização do presente estudo, foram amostradas diferentes áreas de vegetação nativa e de monoculturas, com o intuito de fazer um levantamento das espécies de formigas cortadeiras que ocorrem em Goiás e sobre quais são os ambientes aos quais elas estão associadas. Durante o presente estudo, foram registradas seis espécies de formigas cortadeiras: Atta sexdens, Atta laevigata, Acromyrmex subterraneus, Acromyrmex disciger, Acromyrmex hispidus e Acromyrmex ambiguus, sendo que as últimas quatro foram registradas pela primeira vez para o estado de Goiás.