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The Emerging Amphibian Fungal Disease, Chytridiomycosis: Akeyexampleoftheglobal Phenomenon of Wildlife Emerging Infectious Diseases JONATHAN E

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The Emerging Amphibian Fungal Disease, Chytridiomycosis: Akeyexampleoftheglobal Phenomenon of Wildlife Emerging Infectious Diseases JONATHAN E The Emerging Amphibian Fungal Disease, Chytridiomycosis: AKeyExampleoftheGlobal Phenomenon of Wildlife Emerging Infectious Diseases JONATHAN E. KOLBY1,2 and PETER DASZAK2 1One Health Research Group, College of Public Health, Medical, and Veterinary Sciences, James Cook University, Townsville, Queensland, Australia; 2EcoHealth Alliance, New York, NY 10001 ABSTRACT The spread of amphibian chytrid fungus, INTRODUCTION: GLOBAL Batrachochytrium dendrobatidis, is associated with the emerging AMPHIBIAN DECLINE infectious wildlife disease chytridiomycosis. This fungus poses During the latter half of the 20th century, it was noticed an overwhelming threat to global amphibian biodiversity and is contributing toward population declines and extinctions that global amphibian populations had entered a state worldwide. Extremely low host-species specificity potentially of unusually rapid decline. Hundreds of species have threatens thousands of the 7,000+ amphibian species with since become categorized as “missing” or “lost,” a grow- infection, and hosts in additional classes of organisms have now ing number of which are now believed extinct (1). also been identified, including crayfish and nematode worms. Amphibians are often regarded as environmental in- Soon after the discovery of B. dendrobatidis in 1999, dicator species because of their highly permeable skin it became apparent that this pathogen was already pandemic; and biphasic life cycles, during which most species in- dozens of countries and hundreds of amphibian species had already been exposed. The timeline of B. dendrobatidis’s global habit aquatic zones as larvae and as adults become emergence still remains a mystery, as does its point of origin. semi or wholly terrestrial. This means their overall The reason why B. dendrobatidis seems to have only recently health is closely tied to that of the landscape. Amphibian increased in virulence to catalyze this global disease event declines in recent decades are largely attributed to in- remains unknown, and despite 15 years of investigation, creases in habitat destruction, pollution, and commercial this wildlife pandemic continues primarily uncontrolled. Some disease treatments are effective on animals held in Received: 1 September 2015, Accepted: 19 January 2016, captivity, but there is currently no proven method to eradicate Published: 13 May 2016 B. dendrobatidis from an affected habitat, nor have we been able Editors: W. Michael Scheld, Department of Infectious Diseases, to protect new regions from exposure despite knowledge of an University of Virginia Health System, Charlottesville, VA; James M. “ ” B. dendrobatidis Hughes, Division of Infectious Diseases, Department of Medicine, approaching wave of and ensuing disease. Emory University School of Medicine, Atlanta, GA; Richard J. Whitley, International spread of B. dendrobatidis is largely facilitated Department of Pediatrics, University of Alabama at Birmingham, by the commercial trade in live amphibians. Chytridiomycosis Birmingham, AL was recently listed as a globally notifiable disease by the World Citation: Kolby JE, Daszak P. 2016. The emerging amphibian fungal Organization for Animal Health, but few countries, if any, have disease, chytridiomycosis: a key example of the global phenomenon Microbiol Spectrum formally adopted recommended measures to control its spread. of wildlife emerging infectious diseases. 4(3): EI10-0004-2015. doi:10.1128/microbiolspec.EI10-0004-2015. Wildlife diseases continue to emerge as a consequence of Correspondence: Jonathan E. Kolby, [email protected] globalization, and greater effort is urgently needed to protect © 2016 American Society for Microbiology. All rights reserved. global health. ASMscience.org/MicrobiolSpectrum 1 Kolby and Daszak exploitation, but enigmatic declines and mass mortality with normal shedding, damaging the animal’s ability events began to be observed in seemingly healthy envi- to osmoregulate and maintain electrolyte balance. In ronments, suggesting that an additional factor with con- severe infections, this leads to death by cardiac arrest siderable negative impact was also influencing declines (7). Amphibians also sometimes manifest behavioral (2, 3). symptoms of disease such as lethargy, anorexia, and loss of righting reflex, but these are inconsistent and non- Discovery of Batrachochytrium dendrobatidis specific to chytridiomycosis and thus cannot be used In 1998, a mass mortality event occurred in a colony alone to confirm infection. The same applies to the of poison-dart frogs (Dendrobates spp.) held in a col- presence of amphibian skin lesions sometimes caused by lection at the National Zoo in Washington, DC. During B. dendrobatidis. Consequently, diagnosis of chytridio- an autopsy, histological examination revealed an un- mycosis is challenging and nearly impossible under field usual fungal infection of the skin. The fungus was soon conditions. Thus, the presence of seemingly healthy described as B. dendrobatidis, a previously unknown amphibian populations is sometimes misleading. Dead species of parasitic chytrid fungi with a particular ap- amphibians are infrequently observed in the field despite petite for amphibians (4). There are several hundred sometimes high mortality rates (8), because they quickly described species of chytrid fungi, most of which are decompose or become scavenged. important decomposers of nonliving organic material in the environment, such as pollen and rotting vegetation. Chytrid Resistance in Nature A few exceptions infect living plant or animal cells, with While some amphibians readily develop clinical symp- B. dendrobatidis becoming the first known species to toms of chytridiomycosis, others do not express illness. attack living vertebrate hosts. Certain species appear to possess a variable degree of innate resistance to B. dendrobatidis infection and/or Infection with B. dendrobatidis disease. It is not yet fully understood what provides these and Chytridiomycosis species with a greater defense than most others, but it B. dendrobatidis begins life as an aquatic uniflagellated sometimes involves the presence of anti–B. dendrobatidis zoospore released from a mature zoosporangia embed- symbiotic bacteria in the skin and/or the amphibian’s ded in the skin of an amphibian (4, 5). B. dendrobatidis ability to produce certain skin antimicrobial peptides (9). zoospores are commonly shed into the water, where they These species can sometimes resist or clear B. dendro- can swim short distances and/or are carried by water batidis infection or persist with low-intensity infections. currents to reach a new host. Upon contact with an Unfortunately, some of these are species known to be amphibian, B. dendrobatidis zoospores burrow several invasive outside their native ranges, such as the American layers down into the skin, to the area where keratin is bullfrog (Lithobates catesbeianus) and African clawed produced. These zoospores remain there, where they frog (Xenopus laevis), and have established feral popu- grow and mature into new zoosporangia. Through lations around the world (10). These species serve as asexual reproduction, multiple new zoospores are pro- asymptomatic B. dendrobatidis reservoir hosts that can duced within the zoosporangia and, when ready, are transmit B. dendrobatidis infections to more susceptible released from the amphibian’s skin via discharge tu- species sharing a habitat. The presence of tolerant am- bules. If the infected amphibian is in a terrestrial location phibians in a community of B. dendrobatidis–susceptible when zoospores are released, they are likely to reinfect species can maintain pathogen presence even as vulner- that animal and/or be shed onto vegetation or into soil. able species decline and become locally extinct. This growth cycle from zoospore to mature zoosporan- gium normally takes about five days at optimum tem- Detection of B. dendrobatidis peratures and nutrient conditions. Infection versus Disease Infection with B. dendrobatidis has various effects Distinction between B. dendrobatidis presence on a upon an amphibian, ranging from asymptomatic pres- skin swab, B. dendrobatidis infection, and the dis- ence to the often lethal disease, chytridiomycosis (5). ease chytridiomycosis must be made since these terms Low host-species specificity threatens potentially thou- are sometimes used interchangeably, but each has a sands of species with disease. As of 2013, 42% of 1,240 distinct meaning and denotes a different physical pres- amphibian species tested were found to be infected (6). ence. The most widely accepted protocol to identify a In amphibians susceptible to disease, the presence of B. dendrobatidis–infected amphibian is the collection B. dendrobatidis causes hyperkeratosis and interferes of a skin swab sample together with a highly sensitive 2 ASMscience.org/MicrobiolSpectrum The Emerging Amphibian Fungal Disease, Chytridiomycosis and specific quantitative PCR diagnostic test (11). This lation decline attributed to this pathogen has now is effective because B. dendrobatidis grows within the been documented on every continent where amphib- amphibians’ skin and frequently sheds zoospores back ians are found (6). Although all 7,000+ species in the out to the skin surface, where swabbing the highly kera- class Amphibia are potentially vulnerable to infection, tinized regions (i.e., pelvic patch and feet) is likely to B. dendrobatidis seems to cause disease most often in collect B. dendrobatidis particles that are then iden- members of the order Anura,
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