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FUNGAL DISEASES An Emerging Threat to Human, Animal, and Plant Health Workshop Summary LeighAnne Olsen, Eileen R. Choffnes, David A. Relman, and Leslie Pray, Rapporteurs Forum on Microbial Threats Board on Global Health
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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. Financial support for this project was provided by the U.S. Department of Health and Hu - man Services: National Institutes of Health, National Institute of Allergy and Infectious Diseases, Centers for Disease Control and Prevention, Food and Drug Administration, and the Fogarty International Center; U.S. Department of Defense, Department of the Army: Global Emerging Infections Surveillance and Response System, Medical Research and Materiel Command, and the Defense Threat Reduction Agency; U.S. Department of Veterans Affairs; U.S. Department of Homeland Security; U.S. Agency for International Development; American Society for Microbiology; sanofi pasteur; Burroughs Wellcome Fund; Pfizer, Inc.; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Company Foundation. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the organizations or agencies that provided support for this project. International Standard Book Number-13: 978-0-309-21226-7 International Standard Book Number-10: 0-309-21226-X Additional copies of this report are available from the National Academies Press, 500 Fifth Street, N.W., Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. For more information about the Institute of Medicine, visit the IOM home page at: www. iom.edu. Copyright 2011 by the National Academy of Sciences. All rights reserved. Printed in the United States of America The serpent has been a symbol of long life, healing, and knowledge among almost all cultures and religions since the beginning of recorded history. The serpent adopted as a logotype by the Institute of Medicine is a relief carving from ancient Greece, now held by the Staatliche Museen in Berlin. Cover images: Front (upper): Little brown bats with white-nose syndrome, New York, photo courtesy of New York Department of Environmental Conservation; Front (lower): Yellow stripe rust on wheat, photo courtesy of Stephen A. Harrison, Louisiana State Uni - versity Agricultural Center. Spine: The Panamanian golden frog ( Atelopus zeteki), photo courtesy of Wikimedia Commons, photo by Brian Gratwicke, Smithsonian Conservation Biology Institute. Back: Geomyces destructans, shown in a false-color SEM image (fungus hyphae are yellow, green, and orange; spores are blue), image reprinted from Chaturvedi et al. (2010) Morphological and Molecular Characterizations of Psychrophillic Fungus Geomyces destructans from New York Bats with White Nose Syndrome (WNS). PLoS ONE 5(5): e10783. Doi: 10.1371/journal.pone.0010783. Suggested citation: IOM (Institute of Medicine). 2011. Fungal Diseases: An Emerging Threat to Human, Animal, and Plant Health. Washington, DC: The National Academies Press.
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“Knowing is not enough; we must apply. Willing is not enough; we must do.” — Goethe Advising the Nation. Improving Health.
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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examina - tion of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the Na - tional Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org
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FORUM ON MICROBIAL THREATS1 DAVID A. RELMAN (Chair), Stanford University and Veterans Affairs Palo Alto Health Care System, Palo Alto, California JAMES M. HUGHES (Vice-Chair), Global Infectious Diseases Program, Emory University, Atlanta, Georgia LONNIE J. KING (Vice-Chair), Ohio State University, Columbus KEVIN ANDERSON, Department of Homeland Security, Washington, DC RUTH L. BERKELMAN, Center for Public Health Preparedness and Research, Rollins School of Public Health, Emory University, Atlanta, Georgia DAVID BLAZES,2 Armed Forces Health Surveillance Center, Division of Global Emerging Infectious Surveillance, Silver Spring, Maryland ENRIQUETA C. BOND, Burroughs Wellcome Fund (Emeritus), Marshall, Virginia ROGER BREEZE, Lawrence Livermore National Laboratory, Livermore, California STEVEN J. BRICKNER,3 SJ Brickner Consulting, LLC, Ledyard, Connecticut PAULA R. BRYANT, Defense Threat Reduction Agency, Medical S&T Division, Fort Belvoir, Virginia JOHN E. BURRIS, Burroughs Wellcome Fund, Research Triangle Park, North Carolina ARTURO CASADEVALL,2 Albert Einstein College of Medicine, Bronx, New York PETER DASZAK, EcoHealth Alliance, New York, New York JEFFREY S. DUCHIN, Public Health–Seattle and King County, Seattle, Washington JONATHAN EISEN, Genome Center, University of California, Davis MARK B. FEINBERG, Merck Vaccine Division, Merck & Co., West Point, Pennsylvania JACQUELINE FLETCHER, Oklahoma State University, Stillwater S. ELIZABETH GEORGE,3 Department of Homeland Security, Washington, DC JESSE L. GOODMAN, Food and Drug Administration, Rockville, Maryland EDUARDO GOTUZZO, Instituto de Medicina Tropical–Alexander von Humbolt, Universidad Peruana Cayetano Heredia, Lima, Peru CAROLE A. HEILMAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 1 Institute of Medicine Forums and Roundtables do not issue, review, or approve individual docu - ments. The responsibility for the published workshop summary rests with the workshop rapporteurs and the institution. 2 Forum member since September 1, 2011. 3 Forum member until December 31, 2010. v
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DAVID L. HEYMANN, Health Protection Agency, London, United Kingdom PHILIP HOSBACH, sanofi pasteur, Swiftwater, Pennsylvania STEPHEN ALBERT JOHNSTON, Arizona BioDesign Institute, Arizona State University, Tempe KENT KESTER, Walter Reed Army Institute of Research, Silver Spring, Maryland GERALD T. KEUSCH, Boston University School of Medicine and Boston University School of Public Health, Boston, Massachusetts RIMA F. KHABBAZ, Centers for Disease Control and Prevention, Atlanta, Georgia STANLEY M. LEMON, School of Medicine, University of North Carolina, Chapel Hill EDWARD McSWEEGAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland MARK A. MILLER, Fogarty International Center, Bethesda, Maryland PAUL F. MILLER,4 Pfizer, Inc., Groton, Connecticut STEPHEN S. MORSE,5 Center for Public Health Preparedness, Columbia University, New York, New York GEORGE POSTE, Complex Adaptive Systems Initiative, Arizona State University, Tempe, Arizona JOHN C. POTTAGE, JR., ViiV Healthcare, Collegeville, Pennsylvania DAVID RIZZO,6 Department of Plant Pathology, University of California, Davis GARY A. ROSELLE, Veterans Health Administration, Department of Veterans Affairs, Cincinnati, Ohio ALAN S. RUDOLPH, Defense Threat Reduction Agency, Fort Belvoir, Virginia KEVIN RUSSELL, Armed Forces Health Surveillance Center, Department of Defense, Silver Spring, Maryland JANET SHOEMAKER, American Society for Microbiology, Washington, DC P. FREDERICK SPARLING, University of North Carolina, Chapel Hill, North Carolina TERENCE TAYLOR, International Council for the Life Sciences, Arlington, Virginia MURRAY TROSTLE, U.S. Agency for International Development, Washington, DC MARY E. WILSON, Harvard School of Public Health, Harvard University, Boston, Massachusetts 4 Forum member until July 31, 2011. 5 Forum member until December 31, 2010. 6 Forum member since September 1, 2011. vi
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Staff EILEEN CHOFFNES, Director LEIGHANNE OLSEN, Program Officer KATHERINE McCLURE, Senior Program Associate COLLIN WEINBERGER, Research Associate (until May 2011) REBEKAH HUTTON, Research Associate (from June 2011) ROBERT GASIOR, Senior Program Assistant (until March 2011) PAMELA BERTELSON, Senior Program Assistant (since September 2011) vii
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BOARD ON GLOBAL HEALTH1 Richard Guerrant (Chair), Thomas H. Hunter Professor of International Medicine and Director, Center for Global Health, University of Virginia School of Medicine, Charlottesville Jo Ivey Boufford (IOM Foreign Secretary), President, New York Academy of Medicine, New York Claire V. Broome, Adjunct Professor, Division of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia Jacquelyn C. Campbell, Anna D. Wolf Chair, and Professor, Johns Hopkins University School of Nursing, Baltimore, Maryland Thomas J. Coates, Professor, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California Gary Darmstadt, Director, Family Health Division, Global Health Program, Bill & Melinda Gates Foundation, Seattle, Washington Valentin Fuster, Director, Wiener Cardiovascular Institute Kravis Cardiovascular Health Center Professor, Cardiology, Mount Sinai School of Medicine, Mount Sinai Medical Center, New York, New York James Hospedales, Coordinator, Chronic Disease Project, Health Surveillance and Disease Management Area, Pan American Health Organization/World Health Organization, Washington, DC Peter J. Hotez, Professor and Chair, Department of Microbiology, Immunology, and Tropical Medicine, The George Washington University, Washington, DC Clarion Johnson, Global Medical Director, Medicine and Occupational Medicine Department, Exxon Mobil, Fairfax, Virginia Fitzhugh Mullan, Professor, Department of Health Policy, George Washington University, Washington, DC Guy Palmer, Regents Professor of Pathology and Infectious Diseases, Director of the School for Global Animal Health, Washington State University Jennifer Prah-Ruger, Associate Professor, Division of Health Policy and Administration, Yale University School of Public Health, New Haven, Connecticut Staff Patrick Kelley, Director Angela Mensah, Program Associate 1 Institute of Medicine boards do not review or approve individual workshop summaries. The responsibility for the content of the workshop summary rests with the authors and the institution. viii
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Reviewers This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures ap - proved by the National Research Council’s Report Review Committee. The pur- pose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manu - script remain confidential to protect the integrity of the process. We wish to thank the following individuals for their review of this report: Beth Bell, Centers for Disease Control and Prevention Michael Jeger, Imperial College London Karen Lips, University of Maryland Victoria McGovern, Burroughs Wellcome Fund John W. Taylor, University of California at Berkeley Brett Tyler, Virginia Bioinformatics Institute Although the reviewers listed above have provided many constructive com- ments and suggestions, they were not asked to endorse the final draft of the report before its release. The review of this report was overseen by Dr. Melvin Worth. Appointed by the Institute of Medicine, he was responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution. ix
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Acknowledgments The Forum on Emerging Infections was created by the Institute of Medicine (IOM) in 1996 in response to a request from the Centers for Disease Control and Prevention (CDC) and the National Institutes of Health (NIH). The purpose of the Forum is to provide structured opportunities for leaders from govern- ment, academia, and industry to regularly meet and examine issues of shared concern regarding research, prevention, detection, and management of emerg - ing, reemerging, and novel infectious diseases in humans, plants, and animals. In pursuing this task, the Forum provides a venue to foster the exchange of information and ideas, identify areas in need of greater attention, clarify policy issues by enhancing knowledge and identifying points of agreement, and inform decision makers about science and policy issues. The Forum seeks to illuminate issues rather than resolve them. For this reason, it does not provide advice or recommendations on any specific policy initiative pending before any agency or organization. Its value derives instead from the diversity of its membership and from the contributions that individual members make throughout the activities of the Forum. In September 2003, the Forum changed its name to the Forum on Microbial Threats. The Forum on Microbial Threats and the IOM wish to express their warmest appreciation to the individuals and organizations who gave their valuable time to provide information and advice to the Forum through their participation in the planning and execution of this workshop. A full list of presenters, and their biographical information, may be found in Appendixes B and F, respectively. The Forum gratefully acknowledges the contributions of the members of the xi
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xii ACKNOWLEDGMENTS planning committee1: Gerald Keusch (Boston University), Rima Khabbaz (Cen- ters for Disease Control and Prevention), Lonnie King (Ohio State University), Victoria McGovern (Burroughs Wellcome Fund), Carol Meteyer (United States Geological Service, National Wildlife Health Center), John Perfect (Duke Uni - versity), Erica Rosenblum (University of Idaho), Kevin Russell (Department of Defense), Fred Sparling (University of North Carolina), and James Stack (Kansas State University). The Forum is indebted to IOM staff who tirelessly contributed throughout the planning and execution of the workshop and the production of this workshop summary report. On behalf of the Forum, we gratefully acknowledge these efforts led by Dr. Eileen Choffnes, director of the Forum; Dr. LeighAnne Olsen, program officer; Katherine McClure, senior program associate; Collin Weinberger and Rebekah Hutton, research associates; and Robert Gasior and Pamela Bertelson, senior program assistants, for dedicating much effort and time to developing this workshop’s agenda and for their thoughtful and insightful approach and skill in planning for the workshop and in translating the workshop’s proceedings and discussion into this workshop summary report. We would also like to thank the following IOM staff and consultants for their valuable contributions to this activity: Greta Gorman, Jill Grady, Laura Penny, Heather Phillips, Leslie Pray, Elisabeth Reese, Vilija Teel, and Jordan Wyndelts. Finally, the Forum wishes to recognize the sponsors that supported this ac- tivity. Financial support for this project was provided by the U.S. Department of Health and Human Services: NIH, National Institute of Allergy and Infectious Diseases, CDC, Food and Drug Administration, and the Fogarty International Center2; U.S. Department of Defense, Department of the Army: Global Emerg- ing Infections Surveillance and Response System, Medical Research and Ma - teriel Command, and the Defense Threat Reduction Agency; U.S. Department of Veterans Affairs; U.S. Department of Homeland Security; U.S. Agency for International Development; American Society for Microbiology; sanofi pasteur; Burroughs Wellcome Fund; Pfizer, Inc.; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Company Foundation. The views presented in this workshop summary report are those of the workshop participants and rapporteurs and are not necessarily those of the Forum on Microbial Threats or its sponsors. 1 Institute of Medicine (IOM) planning committees are solely responsible for organizing the work - shop, identifying topics, and choosing speakers. The responsibility for the published workshop sum - mary rests with the workshop rapporteurs and the institution. 2 Sponsor as of October 1, 2010.
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Contents Workshop Overview 1 Workshop Overview References, 84 Appendixes A Contributed Manuscripts 101 A1 The Emergence of Cryptococcus gattii in British Columbia and the Pacific Northwest, 101 Karen H. Bartlett, Sarah E. Kidd, and James W. Kronstad A2 The Good, the Bad, and the Ugly: Fungi Mold Your World, 116 Meredith Blackwell A3 The Fungi: 1, 2, 3 … 5.1 Million Species?, 140 Meredith Blackwell A4 Bat White-Nose Syndrome in North America, 167 David S. Blehert, Jeffrey M. Lorch, Anne E. Ballmann, Paul M. Cryan, and Carol U. Meteyer A5 Mammalian Endothermy Optimally Restricts Fungi and Metabolic Costs, 177 Aviv Bergman and Arturo Casadevall A6 Vertebrate Endothermy Restricts Most Fungi as Potential Pathogens, 181 Vincent A. Robert and Arturo Casadevall xiii
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xiv CONTENTS A7 Surveillance for Emerging Diseases in Wildlife, 188 Peter Daszak, Carlos Zambrana-Torrelio, and Tiffany Bogich A8 Geography, Climate, Dust, and Disease: Epidemiology of Valley Fever (Coccidioidomycosis) and Ways It Might Be Controlled, 196 John N. Galgiani A9 Cryptococcus gattii: An Emerging Pathogen in the United States, 207 Julie R. Harris A10 Sexual Reproduction, Evolution, and Adaptation of Cryptococcus gattii in the Pacific Northwest Outbreak, 226 Joseph Heitman, Edmond J. Byrnes III, and John R. Perfect A11 Yeast Infections—Human Genetics on the Rise, 248 Steven M. Holland and Donald C. Vinh A12 The Increased Risk of Global Wheat Rust Pandemics: Putting Yellow Rust into Perspective, 252 Mogens Støvring Hovmøller A13 Fungal Pathogenesis in Plants and Animals: Similarities and Differences, 264 Barbara Howlett A14 Climate, Globalization, and Trade: Impacts on Dispersal and Invasion of Fungal Plant Pathogens, 273 Michael Jeger, Marco Pautasso, and James Stack A15 Emerging Fungal Diseases of Wild Animal Species, 296 Luis R. Padilla A16 The Emergence of Phytophthora ramorum in North America and Europe, 321 David M. Rizzo, Ross K. Meentemeyer, and Matteo Garbelotto A17 Climate Change, Extreme Weather Events, and Fungal Disease Emergence and Spread, 324 Compton J. Tucker, Karina Yager, Assaf Anyamba, and Kenneth J. Linthicum A18 Host-Pathogen Dynamics of Amphibian Chytridiomycosis: The Role of the Skin Microbiome in Health and Disease, 342 Vance T. Vredenburg, Cheryl J. Briggs, and Reid Harris A19 The Effect of Trade-Mediated Spread of Amphibian Chytrid on Amphibian Conservation, 355 Ché Weldon and Matthew C. Fisher A20 White-Nose Syndrome Fungus (Geomyces destructans) in Bats, Europe, 368 Gudrun Wibbelt, Andreas Kurth, David Hellmann, Manfred Weishaar, Alex Barlow, Michael Veith, Julia Prüger, Tamás Görföl, Lena Grosche, Fabio Bontadina, Ulrich Zöphel, Hans- Peter Seidl, Paul M. Cryan, and David S. Blehert
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xv CONTENTS A21 Pan-European Distribution of White-Nose Syndrome Fungus (Geomyces destructans) Not Associated with Mass Mortality, 380 Sébastien J. Puechmaille, Gudrun Wibbelt, Vanessa Korn, Hubert Fuller, Frédéric Forget, Kristin Mühldorfer, Andreas Kurth, Wieslaw Bogdanowicz, Christophe Borel, Thijs Bosch, Thomas Cherezy, Mikhail Drebet, Tamás Görföl, Anne-Jifke Haarsma, Frank Herhaus, Guénael Hallart, Matthias Hammer, Christian Jungmann, Yann Le Bris, Lauri Lutsar, Matti Masing, Bart Mulkens, Karsten Passior, Martin Starrach, Andrzej Wojtaszewski, Ulrich Zöphel, and Emma C. Teeling B Agenda 403 C Acronyms 409 D Glossary 413 E Forum Member Biographies 427 F Speaker Biographies 455
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Tables, Figures, and Boxes TABLES WO-1 Number of Individual Animals Traded by the United States (2000– 2006), 21 WO-2 Disease Types and Associated Symptoms Caused by P. ramorum, 56 A2-1 Examples of Fungal Associations with Plants, 127 A2-2 Examples of Fungal Associations with Insects, 130 A6-1 Growth Tolerances for Fungi from Soils, Animals, and Plants at 2 Temperatures, 184 A9-1 Characteristics of C. gattii Patients in the United States, 2004–2010, 212 A9-2 Comparison Between Outbreak-Strain (VGIIa/b/c) and Other Genotypes of Infection with C. gattii, United States, 2004–2010, 213 A9-3 Sources and Species of Isolates of Cryptococcus Submitted Following a Request Through ClinMicroNet, United States, October 2010– February 2011, 216 A13-1 General Similarities and Differences Between Fungal Pathogens of Plants and Animals, 266 A13-2 Fungicides Used to Control Plant and Animal Diseases, 269 A14-1 Selected Papers Illustrating the Effects of Climate and Global Change Factors on Specific Pathogen–Host Systems, 280 xvii
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xviii TABLES, FIGURES, AND BOXES A20-1 Bats Tested for Geomyces destructans by Using Microscopy, Fungal Culture, or PCR Analysis, by Country, Europe, 373 A20-2 Fungal Culture and PCR Results for 23 Bats with Evidence of Fungal Colonization Tested by Light or Electron Microscopy, Europe, 374 A21-1 Confirmed Records of Geomyces destructans on Hibernating Bats in Europe and Details of the Culture and Genetic Analyses, 384 A21-2 Suspected Photographic Records of Geomyces destructans on Hibernating Bats in Europe, 385 A21-3 Suspected Visual Records of Geomyces destructans on Hibernating Bats in Europe, 386 FIGURES WO-1 The fungal kingdom, 5 WO-1-1 Leafcutter ants tending their fungal garden, 10 WO-2 Diversity of fungal morphology, 6 WO-3 Depiction of starving Irish children in 1847 potato famine, 13 WO-4 The epidemiological triad, 16 WO-5 Global aviation network, 20 WO-6 Selected dispersal events of fungal pathogens, 22 WO-7 Environmental disturbances and dust storms contribute to the dispersal of fungal spores, 24 WO-8 Change in precipitation between the 1971–2000 average and the 2091–2100 average in inches of liquid water/year, 27 WO-9 Incidence of systemic fungal disease has increased since the 1950s, 30 WO-10 Damage response framework, 31 WO-11 Microbial flora as a host defense, 33 WO-12 Map of the Pacific Northwest, comprising parts of British Columbia, Canada, and the states of Washington and Oregon in the United States, showing human and veterinary Cryptococcus gattii cases, 36 WO-13 Environmental sampling for Cryptococcus gattii in British Columbia (2001–2009), 40 WO-14 Signs of bat white-nose syndrome (WNS), 42 WO-15 Spread of bat white-nose syndrome (WNS) in North America as of April 21, 2011, 44 WO-16 Species affected by bat white-nose syndrome (WNS), 45 WO-17 Global distribution of Bd, 48 WO-18 A chytridiomycosis outbreak in southern mountain yellow-legged frogs, 50 WO-19 Sudden oak death and ramorum blight, 55 WO-20 P. ramorum “migration” pathways, 57 WO-21 Wheat production regions worldwide, 59
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xix TABLES, FIGURES, AND BOXES WO-22 Yellow “stripe” rust on wheat, 61 WO-23 Presence of “trace” and “severe” levels of yellow rust in North America since 2000, 62 WO-24 Roles and responsibilities for monitoring pathogens in humans, animals, plants, food, and the environment in the United States, 65 WO-25 Risk for sudden oak death in the continental United States, based on agreement among five spatially referenced models, 71 WO-26 Mechanisms of action of selected antifungals, 78 WO-27 Frogs in the Sierra Nevada region, being treated in baths containing a fungicidal bacterium in hopes of eliminating infection by the fungal pathogen (Bd) associated with the deadly disease: amphibian chytridiomycosis, 79 WO-28 Panamanian golden frog (Atelopus zeteki), 82 A1-1 Map of the forecasted ecologic niche and region of emergence of C. gattii in British Columbia (BC), 103 A2-1 Diagrammatic representation of relationships of fungal taxa, examples (ex.), and approximate number of species in each group, 120 A2-2 Images of representative fungal groups, 121 A2-3 Saccharomyces cerevisiae (Y-2235), baker’s yeast and model organism, 123 A2-4 Anaptychia ciliaris, 128 A2-5 Ectomycorrhizal root, 129 A2-6 Excavation of deeply entrenched nest of the ant Atta texana requires heavy equipment or, alternatively, ground-penetrating radar to map such nests, 132 A2-7 Hirsutella citriformis (Ophiostomataceae) on a delphacid planthopper, 133 A3-1 Fungal phyla and approximate number of species in each group, 142 A3-2 Lemonniera sp., 144 A3-3 The aero-aquatic ascomycete Helicoon gigantisporum produces distinctive tightly coiled conidia, 144 A3-4 The smut Testicularia sp. develops in the ovary of grasses and (as shown here) sedges, 144 A3-5 Perithecia of Pyxidiophora sp. (Laboulbeniomycetes) developed in moist chamber on moose dung from Meredith Station, New Brunswick, Canada, 144 A3-6 The ca. 8 cm wide basidiomata of Pycnoporus sp., a wide-ranging, brightly colored, wood-decaying polypore, photographed at Barro Colorado Island, Panama, 144
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xx TABLES, FIGURES, AND BOXES A3-7 Peniphorella baculorubrensis, a bark-decaying basidiomycete common on and restricted to living live oak (Quercus virginiana), decays the bark and changes its water-holding capacity, 144 A3-8 Basidiomata of Perenniporia phloiophila on the bark of living Quercus virginiana, 144 A3-9 A basidioma (8 cm diameter) of the wood-decaying fungus, Favolus tenuiculus, a favorite food of several species of mushroom-feeding beetles, 144 A3-10 The small (>10 mm long) brightly colored beetle, Mycotretus sp. (Erotylidae), was collected at Barro Colorado Island, Panama, 144 A3-11 Numbers of known fungi from the Dictionary of the Fungi (editions 1–10, 1950–2008), 146 A4-1 Occurrence of white-nose syndrome and/or Geomyces destructans in the United States (by county) and Canada (by county or district) from winter 2005/2006 through April 2011, 169 A4-2 Micrograph of Geomyces destructans showing distinctive asymmetrically curved conidia either free or borne singly at the tips and sides of branched conidiophores, 170 A4-3A Three little brown bats (Myotis lucifugus) photographed by Alan Hicks (New York State Department of Environmental Conservation) in Graphite Mine, New York in November, 2008, 172 A4-3B Periodic acid-Schiff (PAS) stained microscopic section of wing membrane from a little brown bat with white-nose syndrome collected in Pennsylvania in February, 2009, 172 A4-4 Colony expansion rates of Geomyces destructans when grown on cornmeal agar at 3, 7, 14, and 20°C, 173 A5-1 Organism fitness as a function of body temperature, 180 A6-1 Frequency histogram of thermal growth tolerance for 4802 fungal strains, 184 A7-1 Proportion of emerging infectious diseases caused by different taxonomic groups of pathogens, 190 A8-1 Annual cases of coccidioidomycosis, 199 A9-1 Human infections with C. gattii, United States, December 2004– January 2011, 210 A9-2 U.S. human cases of C. gattii, by year of illness onset, 211
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xxi TABLES, FIGURES, AND BOXES A10-1 The C. gattii outbreak expanded into, and emerged within, the United States, 229 A10-2 Cryptococcus pathogenic species complex, 230 A10-3 Cryptococcus neoformans can reproduce unisexually and bisexually, 235 A10-4 Sexual reproduction and the origin of an outbreak, 240 A11-1 Mechanisms of fungal sensing and control, 250 A12-1 Typical macroscopic symptoms of rust infections on adult wheat plants, 254 A12-2 Map indicating the distribution of global wheat production and regions of recent yellow rust epidemics, 255 The increase in goods (109 tons × km) moved in the United Kingdom A14-1 from the 1930s to the 1990s, 275 A14-2 The world in 1897, with British possessions marked in red, 282 A16-1 Current distribution of Phytophthora ramorum in California and Oregon forests, 316 A17-1 Summary of observations that show the Earth is warming (red arrows) while the Sun has been constant over the same period of time, 326 A17-2 A comparison of the existing four global surface temperature datasets that are used in climate analyses, 327 A17-3 Sea-level rise based on radar altimeters from TOPEX and Jason, with seasonal variations removed, 329 A17-4 A comparison between the total solar irradiance and the NASA/GISS surface temperature data, both from 1979 to 2010, 330 A17-5 Representation of a general circulation model, 331 A17-6 Change in precipitation between the 1971–2000 average and the 2091–2100 average in inches of liquid water/year, 331 A17-7 Rift Valley fever major outbreak events plotted against time and the Southern Oscillation Index, a measure of the phase of El Niño/ Southern Oscillation events, 333 A17-8 Summary Rift Valley fever (RVF) risk maps for (A) Eastern Africa: September 2006–May 2007; (B) Sudan: May 2007–December 2007; (C) Southern Africa: September 2007–May 2008; and (D) Madagascar: September 2007–May 2008, 335 A17-9 Stem rust symptoms on wheat, 336 A17-10 False-color Landsat satellite data (RGB 642) showing glaciers as the blue colors. The green colors represent green vegetation and the red colors represent areas of rock, sand, and soil, 337
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xxii TABLES, FIGURES, AND BOXES A18-1 Decline of (A) Sierra Nevada mountain yellow-legged frog, Rana sierrae, and (B) southern mountain yellow-legged frog, Rana muscosa, in California, USA, 345 A18-2 Maps of the three study metapopulations showing the spread of Bd and frog population status (adults only) during a 4-year period following the initial detection of Bd, 347 A18-3 Frog Bd dynamics in eight intensively sampled populations in Milestone and Sixty Lake basins before and after detection of Bd, 349 A19-1 Maps indicating (A) the global prevalence of Batrachochytrium dendrobatidis. (B) Regional U.S. prevalence of Batrachochytrium dendrobatidis, 361 A20-1 (A) Greater mouse-eared bat (Myotis myotis) with white fungal growth around its muzzle, ears, and wing membranes. (B) Scanning electron micrograph of a bat hair colonized by Geomyces destructans, 371 A20-2 Locations in Europe of bats positive for Geomyces destructans by PCR alone (circles) or by PCR and culture (solid stars) and bats negative for G. destructans but positive for other fungi (square), 375 A21-1 Distribution of confirmed and suspected records of G. destructans on hibernating bats in Europe, 387 A21-2 Photographic evidence showing bats with confirmed or suspected growth of G. destructans, 388 A21-3 Seasonal changes of the number of live bats reported with white fungal growth in Europe, 390 A21-4 Indirect evidence of bats grooming off G. destructans during hibernation, 391 A21-S1 Monitoring of bats at an hibernaculum in Germany during (A) the winter 2006/2007 (September 5, 2006 until April 19, 2007) and (B) the winter 2007/2008 (August 28, 2007 until April 23, 2008), 399 BOXES WO-1 The Fungal Gardens of Leafcutter Ants, 10 WO-2 Factors in the Emergence of Infectious Diseases, 17