|
||||||||||||||||
|
||||||||||||||||
|
||||||||||||||||
|
| ||||||||||||||||||||||||||||||||
|
||||||||||||||||||||||||||||||||
Below are the first 10 and last 10 pages of uncorrected machine-read text (when available) of this chapter, followed by the top 30 algorithmically extracted key phrases from the chapter as a whole.
Intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text on the opening pages of each chapter.
Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.
Do not use for reproduction, copying, pasting, or reading; exclusively for search engines.
OCR for page R1
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
OCR for page R2
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.
OCR for page R3
“Knowing is not enough; we must apply.
Willing is not enough; we must do.”
— Goethe
Advising the Nation. Improving Health.
OCR for page R4
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
OCR for page R5
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
OCR for page R6
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
OCR for page R7
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
OCR for page R8
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
OCR for page R9
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
OCR for page R10
OCR for page R11
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
OCR for page R12
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.
OCR for page R13
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
OCR for page R14
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
OCR for page R15
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
OCR for page R16
OCR for page R17
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
OCR for page R18
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
OCR for page R19
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
OCR for page R20
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
OCR for page R21
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
OCR for page R22
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
