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1

Techangamsuwan, Somporn, Angkana Sommanustweechai, Sumate Kamolnorranart, Boripat Siriaroonrat, Wichase Khonsue, and Nopadon Pirarat. "Emerging Chytrid Fungal Pathogen, Batrachochytrium Dendrobatidis, in Zoo Amphibians in Thailand." Acta Veterinaria 67, no. 4 (December 20, 2017): 525–39. http://dx.doi.org/10.1515/acve-2017-0042.

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AbstractChytridiomycosis, a disease in amphibians caused by Batrachochytrium dendrobatidis (Bd), has led to a population decline and extinction of frog species since 1996. The objective of this study was to determine the prevalence of and the need for establishing a surveillance system for monitoring chytridiomycosis in five national zoos and five free ranging protected areas across Thailand. A total of 492 skin swab samples were collected from live and dead animals and tested by polymerase chain reaction (PCR) for the presence of Bd. The positive specimens were confi rmed by amplicon sequencing and examined by histopathology and immunohistochemistry. From July 2009 to August 2012, the prevalence of Bd from frog skin samples was low (4.27%), monitored by PCR. All samples from live amphibians were negative. The positive cases were only from dead specimens (21/168, 12.5% dead samples) of two non-native captive species, poison dart frog (Dendrobates tinctorius) and tomato frog (Dyscophus antongilii) in one zoo. Immunohistochemistry and histopathology revealed the typical feature of fl ask-shaped zoosporangia and septate thalli, supporting the PCR-based evidence of chytridiomycosis in captive amphibians in Thailand, but detected Bd in only 7/21 of the PCR-positive samples. Although the introduction of a pathogenic strain of Bd from imported carriers might have a serious impact on the native amphibian populations in Thailand, chytridiomycosis has not currently been detected in native Thai amphibians. An active surveillance system is needed for close monitoring of the fungus crossing into Thai amphibian populations
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Kueneman, Jordan G., Douglas C. Woodhams, Reid Harris, Holly M. Archer, Rob Knight, and Valerie J. McKenzie. "Probiotic treatment restores protection against lethal fungal infection lost during amphibian captivity." Proceedings of the Royal Society B: Biological Sciences 283, no. 1839 (September 28, 2016): 20161553. http://dx.doi.org/10.1098/rspb.2016.1553.

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Host-associated microbiomes perform many beneficial functions including resisting pathogens and training the immune system. Here, we show that amphibians developing in captivity lose substantial skin bacterial diversity, primarily due to reduced ongoing input from environmental sources. We combined studies of wild and captive amphibians with a database of over 1 000 strains that allows us to examine antifungal function of the skin microbiome. We tracked skin bacterial communities of 62 endangered boreal toads, Anaxyrus boreas , across 18 time points, four probiotic treatments, and two exposures to the lethal fungal pathogen Batrachochytrium dendrobatidis ( Bd ) in captivity, and compared these to 33 samples collected from wild populations at the same life stage. As the amphibians in captivity lost the Bd -inhibitory bacteria through time, the proportion of individuals exposed to Bd that became infected rose from 33% to 100% in subsequent exposures. Inoculations of the Bd -inhibitory probiotic Janthinobacterium lividum resulted in a 40% increase in survival during the second Bd challenge, indicating that the effect of microbiome depletion was reversible by restoring Bd -inhibitory bacteria. Taken together, this study highlights the functional role of ongoing environmental inputs of skin-associated bacteria in mitigating a devastating amphibian pathogen, and that long-term captivity decreases this defensive function.
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FIEGNA, CATERINA, CHARLOTTE L. CLARKE, DARREN J. SHAW, JOHANNA L. BAILY, FRANCES C. CLARE, ALEXANDRA GRAY, TRENTON W. J. GARNER, and ANNA L. MEREDITH. "Pathological and phylogenetic characterization ofAmphibiothecumsp. infection in an isolated amphibian (Lissotriton helveticus) population on the island of Rum (Scotland)." Parasitology 144, no. 4 (November 22, 2016): 484–96. http://dx.doi.org/10.1017/s0031182016001943.

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SUMMARYOutbreaks of cutaneous infectious disease in amphibians are increasingly being attributed to an overlooked group of fungal-like pathogens, the Dermocystids. During the last 10 years on the Isle of Rum, Scotland, palmate newts (Lissotriton helveticus) have been reportedly afflicted by unusual skin lesions. Here we present pathological and molecular findings confirming that the pathogen associated with these lesions is a novel organism of the order Dermocystida, and represents the first formally reported, and potentially lethal, case of amphibian Dermocystid infection in the UK. Whilst the gross pathology and the parasite cyst morphology were synonymous to those described in a study from infectedL. helveticusin France, we observed a more extreme clinical outcome on Rum involving severe subcutaneous oedema. Phylogenetic topologies supported synonymy between Dermocystid sequences from Rum and France and as well as their distinction fromAmphibiocystidiumspp. Phylogenetic analysis also suggested that the amphibian-infecting Dermocystids are not monophyletic. We conclude that theL. helveticus-infecting pathogen represents a single, novel species;Amphibiothecum meredithae.
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4

Rollins-Smith, Louise A., J. Scott Fites, Laura K. Reinert, Andrea R. Shiakolas, Thomas P. Umile, and Kevin P. C. Minbiole. "Immunomodulatory Metabolites Released by the Frog-Killing Fungus Batrachochytrium dendrobatidis." Infection and Immunity 83, no. 12 (September 14, 2015): 4565–70. http://dx.doi.org/10.1128/iai.00877-15.

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Batrachochytrium dendrobatidisis a fungal pathogen in the phylum Chytridiomycota that causes the skin disease chytridiomycosis. Chytridiomycosis is considered an emerging infectious disease linked to worldwide amphibian declines and extinctions. Although amphibians have well-developed immune defenses, clearance of this pathogen from the skin is often impaired. Previously, we showed that the adaptive immune system is involved in the control of the pathogen, butB. dendrobatidisreleases factors that inhibitin vitroandin vivolymphocyte responses and induce lymphocyte apoptosis. Little is known about the nature of the inhibitory factors released by this fungus. Here, we describe the isolation and characterization of three fungal metabolites produced byB. dendrobatidisbut not by the closely related nonpathogenic chytridHomolaphlyctis polyrhiza. These metabolites are methylthioadenosine (MTA), tryptophan, and an oxidized product of tryptophan, kynurenine (Kyn). Independently, both MTA and Kyn inhibit the survival and proliferation of amphibian lymphocytes and the Jurkat human T cell leukemia cell line. However, working together, they become effective at much lower concentrations. We hypothesize thatB. dendrobatidiscan adapt its metabolism to release products that alter the local environment in the skin to inhibit immunity and enhance the survival of the pathogen.
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Voyles, Jamie, Douglas C. Woodhams, Veronica Saenz, Allison Q. Byrne, Rachel Perez, Gabriela Rios-Sotelo, Mason J. Ryan, et al. "Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation." Science 359, no. 6383 (March 29, 2018): 1517–19. http://dx.doi.org/10.1126/science.aao4806.

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Infectious diseases rarely end in extinction. Yet the mechanisms that explain how epidemics subside are difficult to pinpoint. We investigated host-pathogen interactions after the emergence of a lethal fungal pathogen in a tropical amphibian assemblage. Some amphibian host species are recovering, but the pathogen is still present and is as pathogenic today as it was almost a decade ago. In addition, some species have defenses that are more effective now than they were before the epidemic. These results suggest that host recoveries are not caused by pathogen attenuation and may be due to shifts in host responses. Our findings provide insights into the mechanisms underlying disease transitions, which are increasingly important to understand in an era of emerging infectious diseases and unprecedented global pandemics.
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6

Stoler, Aaron B., Keith A. Berven, and Thomas R. Raffel. "Leaf Litter Inhibits Growth of an Amphibian Fungal Pathogen." EcoHealth 13, no. 2 (March 2, 2016): 392–404. http://dx.doi.org/10.1007/s10393-016-1106-z.

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7

Rothstein, Andrew P., Allison Q. Byrne, Roland A. Knapp, Cheryl J. Briggs, Jamie Voyles, Corinne L. Richards-Zawacki, and Erica Bree Rosenblum. "Divergent regional evolutionary histories of a devastating global amphibian pathogen." Proceedings of the Royal Society B: Biological Sciences 288, no. 1953 (June 23, 2021): 20210782. http://dx.doi.org/10.1098/rspb.2021.0782.

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Emerging infectious diseases are a pressing threat to global biological diversity. Increased incidence and severity of novel pathogens underscores the need for methodological advances to understand pathogen emergence and spread. Here, we use genetic epidemiology to test, and challenge, key hypotheses about a devastating zoonotic disease impacting amphibians globally. Using an amplicon-based sequencing method and non-invasive samples we retrospectively explore the history of the fungal pathogen Batrachochytrium dendrobatidis ( Bd ) in two emblematic amphibian systems: the Sierra Nevada of California and Central Panama. The hypothesis in both regions is the hypervirulent Global Panzootic Lineage of Bd ( Bd GPL) was recently introduced and spread rapidly in a wave-like pattern. Our data challenge this hypothesis by demonstrating similar epizootic signatures can have radically different underlying evolutionary histories. In Central Panama, our genetic data confirm a recent and rapid pathogen spread. However, Bd GPL in the Sierra Nevada has remarkable spatial structuring, high genetic diversity and a relatively older history inferred from time-dated phylogenies. Thus, this deadly pathogen lineage may have a longer history in some regions than assumed, providing insights into its origin and spread. Overall, our results highlight the importance of integrating observed wildlife die-offs with genetic data to more accurately reconstruct pathogen outbreaks.
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8

Zipkin, Elise F., Graziella V. DiRenzo, Julie M. Ray, Sam Rossman, and Karen R. Lips. "Tropical snake diversity collapses after widespread amphibian loss." Science 367, no. 6479 (February 13, 2020): 814–16. http://dx.doi.org/10.1126/science.aay5733.

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Biodiversity is declining at unprecedented rates worldwide. Yet cascading effects of biodiversity loss on other taxa are largely unknown because baseline data are often unavailable. We document the collapse of a Neotropical snake community after the invasive fungal pathogen Batrachochytrium dendrobatidis caused a chytridiomycosis epizootic leading to the catastrophic loss of amphibians, a food source for snakes. After mass mortality of amphibians, the snake community contained fewer species and was more homogeneous across the study site, with several species in poorer body condition, despite no other systematic changes in the environment. The demise of the snake community after amphibian loss demonstrates the repercussive and often unnoticed consequences of the biodiversity crisis and calls attention to the invisible declines of rare and data-deficient species.
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9

Murphy, Peter, Sophie St-Hilaire, and Charles Peterson. "The Effect of Aquatic and Terrestrial Environmental Factors on the Interaction Between Grand Teton Boreal Toads and a Lethal Fungal Pathogen." UW National Parks Service Research Station Annual Reports 31 (January 1, 2008): 125–31. http://dx.doi.org/10.13001/uwnpsrc.2008.3723.

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Batrachochytrium dendrobatidis (Bd), the chytrid fungus which infects keratinized amphibian skin and causes the lethal disease chytridiomycosis, has been linked to population declines and extinctions worldwide (Lips et al. 2006). Amphibians infected with Bd may suffer a variety of outcomes. Individuals of some species have been killed by :S 100 Bd zoospores, while other species, such as the North American bullfrog Rana catesbiana, are highly resistant (Daszak et al. 2004). Within an amphibian species, populations may also respond differently to Bd, with some declining et al. remaining stable (Kriger and Hero 2006). Divergent outcomes among species and populations with respect to Bd may arise from at least three factors, or their interaction.
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10

Holden, Whitney M., Alexander R. Ebert, Peter F. Canning, and Louise A. Rollins-Smith. "Evaluation of Amphotericin B and Chloramphenicol as Alternative Drugs for Treatment of Chytridiomycosis and Their Impacts on Innate Skin Defenses." Applied and Environmental Microbiology 80, no. 13 (April 25, 2014): 4034–41. http://dx.doi.org/10.1128/aem.04171-13.

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ABSTRACTChytridiomycosis, an amphibian skin disease caused by the emerging fungal pathogenBatrachochytrium dendrobatidis, has been implicated in catastrophic global amphibian declines. The result is an alarming decrease in amphibian diversity that is a great concern for the scientific community. Clinical trials testing potential antifungal drugs are needed to identify alternative treatments for amphibians infected with this pathogen. In this study, we quantified the MICs of chloramphenicol (800 μg/ml), amphotericin B (0.8 to 1.6 μg/ml), and itraconazole (Sporanox) (20 ng/ml) againstB. dendrobatidis. Both chloramphenicol and amphotericin B significantly reducedB. dendrobatidisinfection in naturally infected southern leopard frogs (Rana[Lithobates]sphenocephala), although neither drug was capable of complete fungal clearance. Long-term exposure ofR. sphenocephalato these drugs did not inhibit antimicrobial peptide (AMP) synthesis, indicating that neither drug is detrimental to this important innate skin defense. However, we observed that chloramphenicol, but not amphotericin B or itraconazole, inhibited the growth of multipleR. sphenocephalaskin bacterial isolatesin vitroat concentrations below the MIC againstB. dendrobatidis. These results indicate that treatment with chloramphenicol might dramatically alter the protective natural skin microbiome when used as an antifungal agent. This study represents the first examination of the effects of alternative antifungal drug treatments on amphibian innate skin defenses, a crucial step to validating these treatments for practical applications.
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11

Becker, C. Guilherme, Molly C. Bletz, Sasha E. Greenspan, David Rodriguez, Carolina Lambertini, Thomas S. Jenkinson, Paulo R. Guimarães, et al. "Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian." Proceedings of the Royal Society B: Biological Sciences 286, no. 1908 (August 14, 2019): 20191114. http://dx.doi.org/10.1098/rspb.2019.1114.

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Wildlife disease dynamics are strongly influenced by the structure of host communities and their symbiotic microbiota. Conspicuous amphibian declines associated with the waterborne fungal pathogen Batrachochytrium dendrobatidis (Bd) have been observed in aquatic-breeding frogs globally. However, less attention has been given to cryptic terrestrial-breeding amphibians that have also been declining in tropical regions. By experimentally manipulating multiple tropical amphibian assemblages harbouring natural microbial communities, we tested whether Bd spillover from naturally infected aquatic-breeding frogs could lead to Bd amplification and mortality in our focal terrestrial-breeding host: the pumpkin toadlet Brachycephalus pitanga . We also tested whether the strength of spillover could vary depending on skin bacterial transmission within host assemblages. Terrestrial-breeding toadlets acquired lethal spillover infections from neighbouring aquatic hosts and experienced dramatic but generally non-protective shifts in skin bacterial composition primarily attributable to their Bd infections. By contrast, aquatic-breeding amphibians maintained mild Bd infections and higher survival, with shifts in bacterial microbiomes that were unrelated to Bd infections. Our results indicate that Bd spillover from even mildly infected aquatic-breeding hosts may lead to dysbiosis and mortality in terrestrial-breeding species, underscoring the need to further investigate recent population declines of terrestrial-breeding amphibians in the tropics.
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12

Rohr, Jason R., Thomas R. Raffel, Neal T. Halstead, Taegan A. McMahon, Steve A. Johnson, Raoul K. Boughton, and Lynn B. Martin. "Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality." Proceedings of the Royal Society B: Biological Sciences 280, no. 1772 (December 7, 2013): 20131502. http://dx.doi.org/10.1098/rspb.2013.1502.

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Exposure to stressors at formative stages in the development of wildlife and humans can have enduring effects on health. Understanding which, when and how stressors cause enduring health effects is crucial because these stressors might then be avoided or mitigated during formative stages to prevent lasting increases in disease susceptibility. Nevertheless, the impact of early-life exposure to stressors on the ability of hosts to resist and tolerate infections has yet to be thoroughly investigated. Here, we show that early-life, 6-day exposure to the herbicide atrazine (mean ± s.e.: 65.9±3.48 µg l −1 ) increased frog mortality 46 days after atrazine exposure (post-metamorphosis), but only when frogs were challenged with a chytrid fungus implicated in global amphibian declines. Previous atrazine exposure did not affect resistance of infection (fungal load). Rather, early-life exposure to atrazine altered growth and development, which resulted in exposure to chytrid at more susceptible developmental stages and sizes, and reduced tolerance of infection, elevating mortality risk at an equivalent fungal burden to frogs unexposed to atrazine. Moreover, there was no evidence of recovery from atrazine exposure. Hence, reducing early-life exposure of amphibians to atrazine could reduce lasting increases in the risk of mortality from a disease associated with worldwide amphibian declines. More generally, these findings highlight that a better understanding of how stressors cause enduring effects on disease susceptibility could facilitate disease prevention in wildlife and humans, an approach that is often more cost-effective and efficient than reactive medicine.
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Drawert, Brian, Marc Griesemer, Linda R. Petzold, and Cheryl J. Briggs. "Using stochastic epidemiological models to evaluate conservation strategies for endangered amphibians." Journal of The Royal Society Interface 14, no. 133 (August 2017): 20170480. http://dx.doi.org/10.1098/rsif.2017.0480.

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Recent outbreaks of chytridiomycosis, the disease of amphibians caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), have contributed to population declines of numerous amphibian species worldwide. The devastating impacts of this disease have led researchers to attempt drastic conservation measures to prevent further extinctions and loss of biodiversity. The conservation measures can be labour-intensive or expensive, and in many cases have been unsuccessful. We developed a mathematical model of Bd outbreaks that includes the effects of demographic stochasticity and within-host fungal load dynamics. We investigated the impacts of one-time treatment conservation strategies during the disease outbreak that occurs following the initial arrival of Bd into a previously uninfected frog population. We found that for all versions of the model, for a large fraction of parameter space, none of the one-time treatment strategies are effective at preventing disease-induced extinction of the amphibian population. Of the strategies considered, treating frogs with antifungal agents to reduce their fungal load had the greatest likelihood of a beneficial outcome and the lowest risk of decreasing the persistence of the frog population, suggesting that this disease mitigation strategy should be prioritized over disinfecting the environment or reducing host density.
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Becker, Matthew H., Jenifer B. Walke, Shawna Cikanek, Anna E. Savage, Nichole Mattheus, Celina N. Santiago, Kevin P. C. Minbiole, Reid N. Harris, Lisa K. Belden, and Brian Gratwicke. "Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus." Proceedings of the Royal Society B: Biological Sciences 282, no. 1805 (April 22, 2015): 20142881. http://dx.doi.org/10.1098/rspb.2014.2881.

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Symbiotic microbes can dramatically impact host health and fitness, and recent research in a diversity of systems suggests that different symbiont community structures may result in distinct outcomes for the host. In amphibians, some symbiotic skin bacteria produce metabolites that inhibit the growth of Batrachochytrium dendrobatidis (Bd), a cutaneous fungal pathogen that has caused many amphibian population declines and extinctions. Treatment with beneficial bacteria (probiotics) prevents Bd infection in some amphibian species and creates optimism for conservation of species that are highly susceptible to chytridiomycosis, the disease caused by Bd. In a laboratory experiment, we used Bd-inhibitory bacteria from Bd-tolerant Panamanian amphibians in a probiotic development trial with Panamanian golden frogs, Atelopus zeteki , a species currently surviving only in captive assurance colonies. Approximately 30% of infected golden frogs survived Bd exposure by either clearing infection or maintaining low Bd loads, but this was not associated with probiotic treatment. Survival was instead related to initial composition of the skin bacterial community and metabolites present on the skin. These results suggest a strong link between the structure of these symbiotic microbial communities and amphibian host health in the face of Bd exposure and also suggest a new approach for developing amphibian probiotics.
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Parris, Matthew J., and Tommie O. Cornelius. "FUNGAL PATHOGEN CAUSES COMPETITIVE AND DEVELOPMENTAL STRESS IN LARVAL AMPHIBIAN COMMUNITIES." Ecology 85, no. 12 (December 2004): 3385–95. http://dx.doi.org/10.1890/04-0383.

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16

Brannelly, Laura A., Alexandra A. Roberts, Lee F. Skerratt, and Lee Berger. "Epidermal cell death in frogs with chytridiomycosis." PeerJ 5 (February 1, 2017): e2925. http://dx.doi.org/10.7717/peerj.2925.

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Background Amphibians are declining at an alarming rate, and one of the major causes of decline is the infectious disease chytridiomycosis. Parasitic fungal sporangia occur within epidermal cells causing epidermal disruption, but these changes have not been well characterised. Apoptosis (planned cell death) can be a damaging response to the host but may alternatively be a mechanism of pathogen removal for some intracellular infections. Methods In this study we experimentally infected two endangered amphibian species Pseudophryne corroboree and Litoria verreauxii alpina with the causal agent of chytridiomycosis. We quantified cell death in the epidermis through two assays: terminal transferase-mediated dUTP nick end-labelling (TUNEL) and caspase 3/7. Results Cell death was positively associated with infection load and morbidity of clinically infected animals. In infected amphibians, TUNEL positive cells were concentrated in epidermal layers, correlating to the localisation of infection within the skin. Caspase activity was stable and low in early infection, where pathogen loads were light but increasing. In animals that recovered from infection, caspase activity gradually returned to normal as the infection cleared. Whereas, in amphibians that did not recover, caspase activity increased dramatically when infection loads peaked. Discussion Increased cell death may be a pathology of the fungal parasite, likely contributing to loss of skin homeostatic functions, but it is also possible that apoptosis suppression may be used initially by the pathogen to help establish infection. Further research should explore the specific mechanisms of cell death and more specifically apoptosis regulation during fungal infection.
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Vieira, CA, LF Toledo, JE Longcore, and JR Longcore. "Body length of Hylodes cf. ornatus and Lithobates catesbeianus tadpoles, depigmentation of mouthparts, and presence of Batrachochytrium dendrobatidis are related." Brazilian Journal of Biology 73, no. 1 (February 2013): 195–99. http://dx.doi.org/10.1590/s1519-69842013000100021.

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A fungal pathogen Batrachochytrium dendrobatidis (Bd), which can cause morbidity and death of anurans, has affected amphibian populations on a worldwide basis. Availability of pure cultures of Bd isolates is essential for experimental studies to understand the ecology of this pathogen. We evaluated the relationships of body length of Hylodes cf. ornatus and Lithobates catesbeianus tadpoles to depigmentation of mouthparts and determined if dekeratinization indicated an infection by Batrachochytrium dendrobatidis. A strong association existed for both species, one from South America (Brazil: São Paulo) and one from North America (USA: Maine). We believe it prudent not to kill adult amphibians if avoidable, thus obtaining tissue for isolating Bd from tadpoles is reasonable because infected specimens of some species can be selectively collected based on depigmentation of mouthparts.
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Greenspan, Sasha E., Mariana L. Lyra, Gustavo H. Migliorini, Mônica F. Kersch-Becker, Molly C. Bletz, Cybele Sabino Lisboa, Mariana R. Pontes, et al. "Arthropod–bacteria interactions influence assembly of aquatic host microbiome and pathogen defense." Proceedings of the Royal Society B: Biological Sciences 286, no. 1905 (June 26, 2019): 20190924. http://dx.doi.org/10.1098/rspb.2019.0924.

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The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod–bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host–pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod–bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.
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Li, Zhimin, An Martel, Sergé Bogaerts, Bayram Göçmen, Panayiotis Pafilis, Petros Lymberakis, Tonnie Woeltjes, Michael Veith, and Frank Pasmans. "Landscape Connectivity Limits the Predicted Impact of Fungal Pathogen Invasion." Journal of Fungi 6, no. 4 (October 3, 2020): 205. http://dx.doi.org/10.3390/jof6040205.

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Infectious diseases are major drivers of biodiversity loss. The risk of fungal diseases to the survival of threatened animals in nature is determined by a complex interplay between host, pathogen and environment. We here predict the risk of invasion of populations of threatened Mediterranean salamanders of the genus Lyciasalamandra by the pathogenic chytrid fungus Batrachochytrium salamandrivorans by combining field sampling and lab trials. In 494 samples across all seven species of Lyciasalamandra, B. salamandrivorans was found to be absent. Single exposure to a low (1000) number of fungal zoospores resulted in fast buildup of lethal infections in three L. helverseni. Thermal preference of the salamanders was well within the thermal envelope of the pathogen and body temperatures never exceeded the fungus’ thermal critical maximum, limiting the salamanders’ defense opportunities. The relatively low thermal host preference largely invalidates macroclimatic based habitat suitability predictions and, combined with current pathogen absence and high host densities, suggests a high probability of local salamander population declines upon invasion by B. salamandrivorans. However, the unfavorable landscape that shaped intraspecific host genetic diversity, lack of known alternative hosts and rapid host mortality after infection present barriers to further, natural pathogen dispersal between populations and thus species extinction. The risk of anthropogenic spread stresses the importance of biosecurity in amphibian habitats.
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Olivares-Miranda, Mizraim, Vance T. Vredenburg, Julio C. García-Sánchez, Allison Q. Byrne, Erica B. Rosenblum, and Sean M. Rovito. "Fungal infection, decline and persistence in the only obligate troglodytic Neotropical salamander." PeerJ 8 (September 22, 2020): e9763. http://dx.doi.org/10.7717/peerj.9763.

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The fungal pathogen Batrachochytrium dendrobatidis (Bd) is implicated in global mass die-offs and declines in amphibians. In Mesoamerica, the Bd epidemic wave hypothesis is supported by detection of Bd in historic museum specimens collected over the last century, yet the timing and impact of the early stages of the wave remain poorly understood. Chiropterotriton magnipes, the only obligate troglodytic Neotropical salamander, was abundant in its small range in the decade following its description in 1965, but subsequently disappeared from known localities and was not seen for 34 years. Its decline is roughly coincident with that of other populations of Neotropical salamanders associated with the invasion and spread of Bd. To determine the presence and infection intensity of Bd on C. magnipes and sympatric amphibian species (which are also Bd hosts), we used a noninvasive sampling technique and qPCR assay to detect Bd on museum specimens of C. magnipes collected from 1952 to 2012, and from extant populations of C. magnipes and sympatric species of amphibians. We also tested for the presence of the recently discovered Batrachochytrium salamandivorans (Bsal), another fungal chytridiomycete pathogen of salamanders, using a similar technique specific for Bsal. We did not detect Bd in populations of C. magnipes before 1969, while Bd was detected at low to moderate prevalence just prior to and during declines. This pattern is consistent with Bd-caused epizootics followed by host declines and extirpations described in other hosts. We did not detect Bsal in any extant population of C. magnipes. We obtained one of the earliest positive records of the fungus to date in Latin America, providing additional historical evidence consistent with the Bd epidemic wave hypothesis. Genotyping results show that at least one population is currently infected with the Global Panzootic Lineage of Bd, but our genotyping of the historical positive samples was unsuccessful. The lack of large samples from some years and the difficulty in genotyping historical Bd samples illustrate some of the difficulties inherent in assigning causality to historical amphibian declines. These data also provide an important historical baseline for actions to preserve the few known remaining populations of C. magnipes.
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Woeltjes, Tonnie, Matthew Rendle, Annemarieke Spitzen-van der Sluijs, Freddy Haesebrouck, An Martel, Frank Pasmans, Emma Wombwell, Pascale Van Rooij, and Ronald Zollinger. "Clinically healthy amphibians in captive collections and at pet fairs: A reservoir of Batrachochytrium dendrobatidis." Amphibia-Reptilia 32, no. 3 (2011): 419–23. http://dx.doi.org/10.1163/017353711x579830.

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Abstract Batrachochytrium dendrobatidis is the cause of the fungal disease chytridiomycosis, a potentially lethal skin disease of amphibians. Asymptomatically infected amphibians may pose a risk for environmental pathogen pollution. This study therefore assessed the role of healthy, captive amphibians as a reservoir of Batrachochytrium dendrobatidis. Samples were collected from captive amphibians in Belgium, the Netherlands, Germany and France (559 from anurans, 330 from urodelans and 4 from gymnophians) from private owners, zoos, and laboratories. In addition to which, 78 anurans from 19 living collections were sampled during a pet fair in the Netherlands. Nearly 3% of the captive amphibians were infected by B. dendrobatidis, and 13.6% of the collections yielded at least one positive result. At the fair, 7 out of 78 anurans, representing 2 collections were positive. None of the animals that tested positive showed any obvious health problems at the time of sampling. Our results demonstrate the potential of the amphibian pet trade as a vehicle for the spread of B. dendrobatidis.
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Bradley, Paul W., Paul W. Snyder, and Andrew R. Blaustein. "Host age alters amphibian susceptibility to Batrachochytrium dendrobatidis, an emerging infectious fungal pathogen." PLOS ONE 14, no. 9 (September 6, 2019): e0222181. http://dx.doi.org/10.1371/journal.pone.0222181.

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Sabino-Pinto, Joana, Molly Bletz, Ralf Hendrix, R. G. Bina Perl, An Martel, Frank Pasmans, Stefan Lötters, et al. "First detection of the emerging fungal pathogen Batrachochytrium salamandrivorans in Germany." Amphibia-Reptilia 36, no. 4 (2015): 411–16. http://dx.doi.org/10.1163/15685381-00003008.

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The emerging infectious disease chytridiomycosis is one of the major factors triggering global amphibian declines. A recently discovered species of chytrid fungus,Batrachochytrium salamandrivorans(Bsal), likely originated in East Asia, has led to massive declines in populations of fire salamanders (Salamandra salamandra) after its apparent introduction to the Netherlands and Belgium. Here, we report the first detection of this pathogen in Germany where it caused mass mortality of fire salamanders in a captive collection. Salamanders from this collection showed an almost 100% prevalence of infection withBsal. SupposedBsal-induced mortality occurred in multipleSalamandraspecies (S. salamandra,S. algira,S. corsica, andS. infraimmaculata), whileBsalinfection was confirmed in nine subspecies ofS. salamandraand inS. algira. Our study indicates that this pathogen can potentially infect all fire salamander species and subspecies. IfBsalspreads from captive collections to wild populations, then a similar devastating effect associated with high mortality should be expected.
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Jones, Devin K., Trang D. Dang, Jenny Urbina, Randall J. Bendis, Julia C. Buck, Rickey D. Cothran, Andrew R. Blaustein, and Rick A. Relyea. "Effect of Simultaneous Amphibian Exposure to Pesticides and an Emerging Fungal Pathogen, Batrachochytrium dendrobatidis." Environmental Science & Technology 51, no. 1 (December 21, 2016): 671–79. http://dx.doi.org/10.1021/acs.est.6b06055.

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Piovia-Scott, Jonah, Karen Pope, S. Joy Worth, Erica Bree Rosenblum, Thomas Poorten, Jeanine Refsnider, Louise A. Rollins-Smith, et al. "Correlates of virulence in a frog-killing fungal pathogen: evidence from a California amphibian decline." ISME Journal 9, no. 7 (December 16, 2014): 1570–78. http://dx.doi.org/10.1038/ismej.2014.241.

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Piovia-Scott, Jonah, Daniel Rejmanek, Douglas C. Woodhams, S. Joy Worth, Heather Kenny, Valerie McKenzie, Sharon P. Lawler, and Janet E. Foley. "Greater Species Richness of Bacterial Skin Symbionts Better Suppresses the Amphibian Fungal Pathogen Batrachochytrium Dendrobatidis." Microbial Ecology 74, no. 1 (January 7, 2017): 217–26. http://dx.doi.org/10.1007/s00248-016-0916-4.

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Barnett, K. M., S. E. Detmering, T. A. McMahon, and D. J. Civitello. "Asymmetric cross-strain protection for amphibians exposed to a fungal-metabolite prophylactic treatment." Biology Letters 17, no. 8 (August 2021): 20210207. http://dx.doi.org/10.1098/rsbl.2021.0207.

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Chytridiomycosis, an infectious disease of amphibians caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), poses an imminent conservation threat. The global spread of Bd has led to mass mortality events in many amphibian species, resulting in at least 90 species' extinctions to date. Exposure to Bd metabolites (i.e. non-infectious antigenic chemicals released by Bd) partially protects frogs during subsequent challenges with live Bd, suggesting its use as a prophylactic treatment and potential vaccine. However, we do not know whether Bd metabolite exposure protects against strains beyond the one used for treatment. To address this knowledge gap, we conducted a 3 × 2 experiment where we exposed adult Cuban treefrogs, Osteopilus septentrionalis , to one of three treatments (Bd metabolites from California-isolated strain JEL-270, Panamá-isolated strain JEL-419, or an artificial spring water control) and then challenged individuals with live Bd from either strain. We found that exposure to Bd metabolites from the California-isolated strain significantly reduced Bd loads of frogs challenged with the live Panamá-isolated strain, but no other treatments were found to confer protective effects. These findings demonstrate asymmetric cross-protection of a Bd metabolite prophylaxis and suggest that work investigating multiple, diverse strains is urgently needed.
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Adams, Andrea J., Sarah J. Kupferberg, Mark Q. Wilber, Allan P. Pessier, Marcia Grefsrud, Steve Bobzien, Vance T. Vredenburg, and Cheryl J. Briggs. "Extreme drought, host density, sex, and bullfrogs influence fungal pathogen infection in a declining lotic amphibian." Ecosphere 8, no. 3 (March 2017): e01740. http://dx.doi.org/10.1002/ecs2.1740.

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Gauberg, Julia, Nicholas Wu, Rebecca L. Cramp, Scott P. Kelly, and Craig E. Franklin. "A lethal fungal pathogen directly alters tight junction proteins in the skin of a susceptible amphibian." Journal of Experimental Biology 222, no. 3 (December 17, 2018): jeb192245. http://dx.doi.org/10.1242/jeb.192245.

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Searle, Catherine L., Lisa K. Belden, Pang Du, and Andrew R. Blaustein. "Stress and chytridiomycosis: Exogenous exposure to corticosterone does not alter amphibian susceptibility to a fungal pathogen." Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 321, no. 5 (March 9, 2014): 243–53. http://dx.doi.org/10.1002/jez.1855.

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Xie, Gisselle Yang, Deanna H. Olson, and Andrew R. Blaustein. "Projecting the Global Distribution of the Emerging Amphibian Fungal Pathogen, Batrachochytrium dendrobatidis, Based on IPCC Climate Futures." PLOS ONE 11, no. 8 (August 11, 2016): e0160746. http://dx.doi.org/10.1371/journal.pone.0160746.

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Fonner, CW, SA Patel, SM Boord, MD Venesky, and SK Woodley. "Effects of corticosterone on infection and disease in salamanders exposed to the amphibian fungal pathogen Batrachochytrium dendrobatidis." Diseases of Aquatic Organisms 123, no. 2 (March 6, 2017): 159–71. http://dx.doi.org/10.3354/dao03089.

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Flechas, Sandra V., Ailin Blasco-Zúñiga, Andrés Merino-Viteri, Valeria Ramírez-Castañeda, Miryan Rivera, and Adolfo Amézquita. "The effect of captivity on the skin microbial symbionts in three Atelopus species from the lowlands of Colombia and Ecuador." PeerJ 5 (July 31, 2017): e3594. http://dx.doi.org/10.7717/peerj.3594.

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Many amphibian species are at risk of extinction in their natural habitats due to the presence of the fungal pathogen Batrachochytrium dendrobatidis (Bd). For the most highly endangered species, captive assurance colonies have been established as an emergency measure to avoid extinction. Experimental research has suggested that symbiotic microorganisms in the skin of amphibians play a key role against Bd. While previous studies have addressed the effects of captivity on the cutaneous bacterial community, it remains poorly studied whether and how captive conditions affect the proportion of beneficial bacteria or their anti-Bd performance on amphibian hosts. In this study we sampled three amphibian species of the highly threatened genus, Atelopus, that remain in the wild but are also part of ex situ breeding programs in Colombia and Ecuador. Our goals were to (1) estimate the diversity of culturable bacterial assemblages in these three species of Atelopus, (2) describe the effect of captivity on the composition of skin microbiota, and (3) examine how captivity affects the bacterial ability to inhibit Bd growth. Using challenge assays we tested each bacterial isolate against Bd, and through sequencing of the 16S rRNA gene, we identified species from thirteen genera of bacteria that inhibited Bd growth. Surprisingly, we did not detect a reduction in skin bacteria diversity in captive frogs. Moreover, we found that frogs in captivity still harbor bacteria with anti-Bd activity. Although the scope of our study is limited to a few species and to the culturable portion of the bacterial community, our results indicate that captive programs do not necessarily change bacterial communities of the toad skins in a way that impedes the control of Bd in case of an eventual reintroduction.
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Grogan, Laura F., Josephine E. Humphries, Jacques Robert, Chantal M. Lanctôt, Catherine J. Nock, David A. Newell, and Hamish I. McCallum. "Immunological Aspects of Chytridiomycosis." Journal of Fungi 6, no. 4 (October 19, 2020): 234. http://dx.doi.org/10.3390/jof6040234.

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Amphibians are currently the most threatened vertebrate class, with the disease chytridiomycosis being a major contributor to their global declines. Chytridiomycosis is a frequently fatal skin disease caused by the fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). The severity and extent of the impact of the infection caused by these pathogens across modern Amphibia are unprecedented in the history of vertebrate infectious diseases. The immune system of amphibians is thought to be largely similar to that of other jawed vertebrates, such as mammals. However, amphibian hosts are both ectothermic and water-dependent, which are characteristics favouring fungal proliferation. Although amphibians possess robust constitutive host defences, Bd/Bsal replicate within host cells once these defences have been breached. Intracellular fungal localisation may contribute to evasion of the induced innate immune response. Increasing evidence suggests that once the innate defences are surpassed, fungal virulence factors suppress the targeted adaptive immune responses whilst promoting an ineffectual inflammatory cascade, resulting in immunopathology and systemic metabolic disruption. Thus, although infections are contained within the integument, crucial homeostatic processes become compromised, leading to mortality. In this paper, we present an integrated synthesis of amphibian post-metamorphic immunological responses and the corresponding outcomes of infection with Bd, focusing on recent developments within the field and highlighting future directions.
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Loyau, Adeline, Jérémie H. Cornuau, Frances C. Clare, and Dirk S. Schmeller. "Side effects of itraconazole on post-metamorphic Alytes obstetricans after a cold stress." Amphibia-Reptilia 37, no. 4 (2016): 345–57. http://dx.doi.org/10.1163/15685381-00003064.

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Itraconazole is the most widely used treatment against Batrachochytrium dendrobatidis (Bd), the fungal pathogen causing chytridiomycosis, a proximate cause of amphibian declines. Several side effects of itraconazole treatment, ranging in severity from depigmentation to death have been reported in different amphibian species and life stages, and these side effects were observed at commonly used dosages of itraconazole. However, no studies have investigated side-effects of itraconazole in conjunction with environmental stress. Post-metamorphic midwife toads (Alytes obstetricans) that were treated with itraconazole and subsequently exposed to a cold stress (exposure to 4°C cold water) had higher mortality rates compared to untreated individuals. Moreover, adults of booroolong frogs (Litoria booroolongensis) treated with itraconazole had a higher probability to become infected when subsequently exposed to Bd. Our results suggest that a post-metamorphosis itraconazole treatment of infected midwife toads combined with a subsequent release into the wild may be an ineffective disease mitigation strategy, as the cold stress during hibernation and/or exposure to Bd in the wild may reduce the hibernation emergence rate of treated individuals in this species.
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Adams, Andrea J., Allan Pessier, Peggy Cranston, and Robert L. Grasso. "Chytridiomycosis-induced mortality in a threatened anuran." PLOS ONE 15, no. 11 (November 6, 2020): e0241119. http://dx.doi.org/10.1371/journal.pone.0241119.

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Effectively planning conservation introductions involves assessing the suitability of both donor and recipient populations, including the landscape of disease risk. Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), has caused extensive amphibian declines globally and may hamper reintroduction attempts. To determine Bd dynamics in potential source populations for conservation translocations of the threatened California red-legged frog (Rana draytonii) to Yosemite National Park, we conducted Bd sampling in two populations in the foothills of the Sierra Nevada Mountains, California, U.S.A. At one of two sites, we observed lethally high Bd loads in early post-metamorphic life stages and confirmed one chytridiomycosis-induced mortality, the first such report for this species. These results informed source population site selection for subsequent R. draytonii conservation translocations. Conservation efforts aimed at establishing new populations of R. draytonii in a landscape where Bd is ubiquitous can benefit from an improved understanding of risk through disease monitoring and ex situ infection studies.
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Eskew, Evan A., Barbara C. Shock, Elise E. B. LaDouceur, Kevin Keel, Michael R. Miller, Janet E. Foley, and Brian D. Todd. "Gene expression differs in susceptible and resistant amphibians exposed to Batrachochytrium dendrobatidis." Royal Society Open Science 5, no. 2 (February 2018): 170910. http://dx.doi.org/10.1098/rsos.170910.

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Chytridiomycosis, the disease caused by the fungal pathogen Batrachochytrium dendrobatidis ( Bd ), has devastated global amphibian biodiversity. Nevertheless, some hosts avoid disease after Bd exposure even as others experience near-complete extirpation. It remains unclear whether the amphibian adaptive immune system plays a role in Bd defence. Here, we describe gene expression in two host species—one susceptible to chytridiomycosis and one resistant—following exposure to two Bd isolates that differ in virulence. Susceptible wood frogs ( Rana sylvatica ) had high infection loads and mortality when exposed to the more virulent Bd isolate but lower infection loads and no fatal disease when exposed to the less virulent isolate. Resistant American bullfrogs ( R. catesbeiana ) had high survival across treatments and rapidly cleared Bd infection or avoided infection entirely. We found widespread upregulation of adaptive immune genes and downregulation of important metabolic and cellular maintenance components in wood frogs after Bd exposure, whereas American bullfrogs showed little gene expression change and no evidence of an adaptive immune response. Wood frog responses suggest that adaptive immune defences may be ineffective against virulent Bd isolates that can cause rapid physiological dysfunction. By contrast, American bullfrogs exhibited robust resistance to Bd that is likely attributable, at least in part, to their continued upkeep of metabolic and skin integrity pathways as well as greater antimicrobial peptide expression compared to wood frogs, regardless of exposure. Greater understanding of these defences will ultimately help conservationists manage chytridiomycosis.
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Garner, Trenton W. J., Benedikt R. Schmidt, An Martel, Frank Pasmans, Erin Muths, Andrew A. Cunningham, Che Weldon, Matthew C. Fisher, and Jaime Bosch. "Mitigating amphibian chytridiomycoses in nature." Philosophical Transactions of the Royal Society B: Biological Sciences 371, no. 1709 (December 5, 2016): 20160207. http://dx.doi.org/10.1098/rstb.2016.0207.

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Amphibians across the planet face the threat of population decline and extirpation caused by the disease chytridiomycosis. Despite consensus that the fungal pathogens responsible for the disease are conservation issues, strategies to mitigate their impacts in the natural world are, at best, nascent. Reducing risk associated with the movement of amphibians, non-amphibian vectors and other sources of infection remains the first line of defence and a primary objective when mitigating the threat of disease in wildlife. Amphibian-associated chytridiomycete fungi and chytridiomycosis are already widespread, though, and we therefore focus on discussing options for mitigating the threats once disease emergence has occurred in wild amphibian populations. All strategies have shortcomings that need to be overcome before implementation, including stronger efforts towards understanding and addressing ethical and legal considerations. Even if these issues can be dealt with, all currently available approaches, or those under discussion, are unlikely to yield the desired conservation outcome of disease mitigation. The decision process for establishing mitigation strategies requires integrated thinking that assesses disease mitigation options critically and embeds them within more comprehensive strategies for the conservation of amphibian populations, communities and ecosystems. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.
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Brannelly, LA, DP Wetzel, M. West, and CL Richards-Zawacki. "Optimized Batrachochytrium dendrobatidis DNA extraction of swab samples results in imperfect detection particularly when infection intensities are low." Diseases of Aquatic Organisms 139 (June 4, 2020): 233–43. http://dx.doi.org/10.3354/dao03482.

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Accurate detection of the amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd) is critical for wildlife disease research; however, false negatives in detection do occur. Here we compared different DNA extraction methods to determine the threshold for Bd detection and identify an optimal extraction method to improve detection and quantification of the pathogen. We extracted both lab-created cell suspension standards using PrepMan Ultra, Chelex resin, and 3 spin column DNA extraction kits (Qiagen DNeasy Blood and Tissue, Zymo Quick DNA miniprep, and IBI gMAX mini kit), and further compared extraction methods using field-collected samples. We found that when extracting Bd DNA from cells in lab-created culture, the spin column extraction methods and PrepMan Ultra were equivalent, while the resin method detected higher Bd DNA quantities, especially at higher loads. However, when swabs from live animals were analyzed, low Bd quantities were more than twice as likely to be detected using a spin column extraction than with the PrepMan Ultra extraction method. All tested spin column extraction methods performed similarly across both field and lab samples. Samples containing low Bd quantities yielded inconsistent detection and quantification of Bd DNA copies regardless of extraction method. To manage imperfect detection of Bd, we suggest that presence/absence analyses are more informative than attempting to quantify Bd DNA when quantities are low. Overall, we recommend that a cost-benefit analysis of target species susceptibility and epidemiology be taken into consideration when designing an experiment to determine the most appropriate DNA extraction method to be used, because sometimes detecting low Bd quantities is imperative to the study, whereas in other situations, detecting low DNA quantities is less important.
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Romero-Zambrano, Génesis L., Stalin A. Bermúdez-Puga, Alex F. Sánchez-Yumbo, Jomira K. Yánez-Galarza, H. Mauricio Ortega-Andrade, and Leopoldo Naranjo-Briceño. "Amphibian chytridiomycosis, a lethal pandemic disease caused by the killer fungus Batrachochytrium dendrobatidis: New approaches to host defense mechanisms and techniques for detection and monitoring." Bionatura 6, no. 1 (February 15, 2021): 1628–36. http://dx.doi.org/10.21931/rb/2021.06.01.28.

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Chytridiomycosis is a catastrophic disease currently decimating worldwide amphibian populations, caused by the panzootic chytrid fungus Batrachochytrium dendrobatidis. Massive species decline to extinction catalyzes radical changes in ecosystems globally, including the largest continuous rainforest ecosystem on Earth, the Amazon rainforest. Innovative research that aims to propose feasible mechanisms of mitigation and the origins of the disease is vital, including studies addressing climatic effects on the expansion of chytridiomycosis. Thus, this publication aims to provide a comprehensive review of: i) the current technologies used for B. dendrobatidis detection and monitoring, and ii) the known Neotropical amphibian's skin microbiota with anti-fungal properties against B. dendrobatidis. Several immunologic and DNA-based methods are discussed to understand the emerging fungal pathogens and their effects on the biosphere, which can help to mitigate the devastating ecological impacts of mass amphibian morbidity. The establishment of rapid and highly accurate B. dendrobatidis detection techniques and methods for monitoring amphibian's cutaneous microbiome is crucial in the fight against chytridiomycosis.
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Stupar, Milos, Katarina Breka, Imre Krizmanic, Srdjan Stamenkovic, Nikola Unkovic, Zeljko Savkovic, Jelena Vukojevic, and Milica Ljaljevic-Grbic. "First case report on pathogenic fungus Fonsecaea sp. Negroni from skin of Pelophylax kl. esculentus L. in Serbia." Zbornik Matice srpske za prirodne nauke, no. 133 (2017): 307–14. http://dx.doi.org/10.2298/zmspn1733307s.

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Non-harmful adhesive tape method was applied directly on the skin surface of edible frog (Pelophylax kl. esculentus), captured in vernal ponds on the locality ?Stevanove ravnice? within the Special Nature Reserve ?Deliblatska pescara?, in order to detect fungal dwellers of frogs? skin. Light microscopy analyses of Lactophenol Cotton Blue mounted adhesive tape samples taken from frog?s ventrum revealed the presence of melanized septate hyphae, branched conidiophores with chains of single-celled ovoid conidia, arising directly from the skin, which corresponds to morphological features of dematiaceous hyphomycete - Fonsecaea sp. Since members of genus Fonsecaea are frequently cited as causative agents of chromomycosis in amphibians, as well as human phaeohyphomycosis, world?wide, it is of great significance to study the presence of this fungal pathogen on amphibians in Serbia in order to make the basic reference data of the incidence of these pathogens in this region.
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42

Picco, Angela M., and James P. Collins. "Fungal and Viral Pathogen Occurrence in Costa Rican Amphibians." Journal of Herpetology 41, no. 4 (December 2007): 746–49. http://dx.doi.org/10.1670/07-033.1.

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43

Klop-Toker, Kaya L., Jose W. Valdez, Michelle P. Stockwell, Matthew E. Edgar, Loren Fardell, Simon Clulow, John Clulow, and Michael J. Mahony. "Assessing host response to disease treatment: how chytrid-susceptible frogs react to increased water salinity." Wildlife Research 44, no. 8 (2017): 648. http://dx.doi.org/10.1071/wr16145.

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Context The severity and prevalence of the amphibian fungal pathogen, Batrachochytrium dendrobatidis (Bd) is correlated with several environmental variables, including salinity, temperature, and moisture content, which influence the pathogen’s growth and survival. Habitats that contain these environmental variables at levels outside of those optimal for Bd growth and survival may facilitate the survival of susceptible host species. Therefore, manipulation of environmental salinity is a potential management strategy to help conserve Bd-susceptible species. However, host behaviour also influences disease dynamics, and the success of habitat manipulation programs depends on how hosts use this altered habitat. Aims To assess if the Bd-susceptible green and golden bell frog, Litoria aurea, will select waterbodies with a salinity increased to S=3; if this selection is affected by infection; and if a frog’s time in a waterbody of this salinity affects infection load or blood physiology. Methods We conducted a filmed choice experiment and a 3-year field study where infected and uninfected frogs could choose between fresh or saline waterbodies. Key results In both the laboratory experiment and field study, Bd-infected L. aurea spent a significantly greater amount of time in or closer to a waterbody than uninfected frogs. Experimentally infected frogs tended to prefer the saline water over fresh, but their choice of water usage did not differ statistically from uninfected frogs. In the field, frogs began to avoid ponds when salinities rose above S=5. Conclusions Because both wild and captive, and infected and uninfected L. aurea readily selected waterbodies with a salinity of S=3, this salinity could potentially be used as a passive method for reducing the severity of Bd when managing this species. However, further testing is needed to understand the efficacy of this treatment, and care must be taken to prevent salinities rising above S=5, because this level seems to produce an avoidance response and therefore may not be suitable in every location. Implications Manipulation of aquatic habitats may be a worthwhile focus for Bd management in habitats where water level fluctuations are minimal.
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Voyles, Jamie. "Phenotypic profiling of Batrachochytrium dendrobatidis, a lethal fungal pathogen of amphibians." Fungal Ecology 4, no. 3 (June 2011): 196–200. http://dx.doi.org/10.1016/j.funeco.2010.12.003.

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45

Briggs, C. J., R. A. Knapp, and V. T. Vredenburg. "Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians." Proceedings of the National Academy of Sciences 107, no. 21 (May 10, 2010): 9695–700. http://dx.doi.org/10.1073/pnas.0912886107.

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RAFFEL, T. R., T. BOMMARITO, D. S. BARRY, S. M. WITIAK, and L. A. SHACKELTON. "Widespread infection of the Eastern red-spotted newt (Notophthalmus viridescens) by a new species of Amphibiocystidium, a genus of fungus-like mesomycetozoan parasites not previously reported in North America." Parasitology 135, no. 2 (October 12, 2007): 203–15. http://dx.doi.org/10.1017/s0031182007003708.

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SUMMARYGiven the worldwide decline of amphibian populations due to emerging infectious diseases, it is imperative that we identify and address the causative agents. Many of the pathogens recently implicated in amphibian mortality and morbidity have been fungal or members of a poorly understood group of fungus-like protists, the mesomycetozoans. One mesomycetozoan, Amphibiocystidium ranae, is known to infect several European amphibian species and was associated with a recent decline of frogs in Italy. Here we present the first report of an Amphibiocystidium sp. in a North American amphibian, the Eastern red-spotted newt (Notophthalmus viridescens), and characterize it as the new species A. viridescens in the order Dermocystida based on morphological, geographical and phylogenetic evidence. We also describe the widespread and seasonal distribution of this parasite in red-spotted newt populations and provide evidence of mortality due to infection.
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Demori, Ilaria, Zeinab El Rashed, Viola Corradino, Annamaria Catalano, Leila Rovegno, Linda Queirolo, Sebastiano Salvidio, et al. "Peptides for Skin Protection and Healing in Amphibians." Molecules 24, no. 2 (January 18, 2019): 347. http://dx.doi.org/10.3390/molecules24020347.

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Amphibian skin is not to be considered a mere tegument; it has a multitude of functions related to respiration, osmoregulation, and thermoregulation, thus allowing the individuals to survive and thrive in the terrestrial environment. Moreover, amphibian skin secretions are enriched with several peptides, which defend the skin from environmental and pathogenic insults and exert many other biological effects. In this work, the beneficial effects of amphibian skin peptides are reviewed, in particular their role in speeding up wound healing and in protection from oxidative stress and UV irradiation. A better understanding of why some species seem to resist several environmental insults can help to limit the ongoing amphibian decline through the development of appropriate strategies, particularly against pathologies such as viral and fungal infections.
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Cook, KJ, J. Voyles, HV Kenny, KL Pope, and J. Piovia-Scott. "Non-lethal isolation of the fungal pathogen Batrachochytrium dendrobatidis (Bd) from amphibians." Diseases of Aquatic Organisms 129, no. 2 (July 4, 2018): 159–64. http://dx.doi.org/10.3354/dao03238.

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Rumschlag, SL, and MD Boone. "High juvenile mortality in amphibians during overwintering related to fungal pathogen exposure." Diseases of Aquatic Organisms 131, no. 1 (October 16, 2018): 13–28. http://dx.doi.org/10.3354/dao03277.

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Longo, Ana V., Anna E. Savage, Ian Hewson, and Kelly R. Zamudio. "Seasonal and ontogenetic variation of skin microbial communities and relationships to natural disease dynamics in declining amphibians." Royal Society Open Science 2, no. 7 (July 2015): 140377. http://dx.doi.org/10.1098/rsos.140377.

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Abstract:
Recently, microbiologists have focused on characterizing the probiotic role of skin bacteria for amphibians threatened by the fungal disease chytridiomycosis. However, the specific characteristics of microbial diversity required to maintain health or trigger disease are still not well understood in natural populations. We hypothesized that seasonal and developmental transitions affecting susceptibility to chytridiomycosis could also alter the stability of microbial assemblages. To test our hypothesis, we examined patterns of skin bacterial diversity in two species of declining amphibians ( Lithobates yavapaiensis and Eleutherodactylus coqui ) affected by the pathogenic fungus Batrachochytrium dendrobatidis ( Bd ). We focused on two important transitions that affect Bd susceptibility: ontogenetic (from juvenile to adult) shifts in E. coqui and seasonal (from summer to winter) shifts in L. yavapaiensis . We used a combination of community-fingerprinting analyses and 16S rRNA amplicon sequencing to quantify changes in bacterial diversity and assemblage composition between seasons and developmental stages, and to investigate the relationship between bacterial diversity and pathogen load. We found that winter-sampled frogs and juveniles, two states associated with increased Bd susceptibility, exhibited higher diversity compared with summer-sampled frogs and adult individuals. Our findings also revealed that hosts harbouring higher bacterial diversity carried lower Bd infections, providing support for the protective role of bacterial communities. Ongoing work to understand skin microbiome resilience after pathogen disturbance has the potential to identify key taxa involved in disease resistance.
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