The Effect of Aquatic and Terrestrial Environmental Factors on the Interaction Between Grand Teton Boreal Toads and a Lethal Fungal Pathogen

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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Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability

Applied and Environmental Microbiology ◽

10.1128/aem.00186-17 ◽

2017 ◽

Vol 83 (9) ◽

Cited By ~ 12

Author(s):

Carly R. Muletz-Wolz ◽

Graziella V. DiRenzo ◽

Stephanie A. Yarwood ◽

Evan H. Campbell Grant ◽

Robert C. Fleischer ◽

...

Keyword(s):

Fungal Pathogen ◽

Batrachochytrium Dendrobatidis ◽

Bacterial Species ◽

Rrna Gene ◽

Amphibian Skin ◽

Amphibian Species ◽

Protective Function ◽

Content Type ◽

Skin Bacteria ◽

Salamander Species

ABSTRACT Diverse bacteria inhabit amphibian skin; some of those bacteria inhibit growth of the fungal pathogen Batrachochytrium dendrobatidis. Yet there has been no systematic survey of anti-B. dendrobatidis bacteria across localities, species, and elevations. This is important given geographic and taxonomic variations in amphibian susceptibility to B. dendrobatidis. Our collection sites were at locations within the Appalachian Mountains where previous sampling had indicated low B. dendrobatidis prevalence. We determined the numbers and identities of anti-B. dendrobatidis bacteria on 61 Plethodon salamanders (37 P. cinereus, 15 P. glutinosus, 9 P. cylindraceus) via culturing methods and 16S rRNA gene sequencing. We sampled co-occurring species at three localities and sampled P. cinereus along an elevational gradient (700 to 1,000 meters above sea level [masl]) at one locality. We identified 50 anti-B. dendrobatidis bacterial operational taxonomic units (OTUs) and found that the degree of B. dendrobatidis inhibition was not correlated with relatedness. Five anti-B. dendrobatidis bacterial strains occurred on multiple amphibian species at multiple localities, but none were shared among all species and localities. The prevalence of anti-B. dendrobatidis bacteria was higher at Shenandoah National Park (NP), VA, with 96% (25/26) of salamanders hosting at least one anti-B. dendrobatidis bacterial species compared to 50% (7/14) at Catoctin Mountain Park (MP), MD, and 38% (8/21) at Mt. Rogers National Recreation Area (NRA), VA. At the individual level, salamanders at Shenandoah NP had more anti-B. dendrobatidis bacteria per individual (μ = 3.3) than those at Catoctin MP (μ = 0.8) and at Mt. Rogers NRA (μ = 0.4). All salamanders tested negative for B. dendrobatidis. Anti-B. dendrobatidis bacterial species are diverse in central Appalachian Plethodon salamanders, and their distribution varied geographically. The antifungal bacterial species that we identified may play a protective role for these salamanders. IMPORTANCE Amphibians harbor skin bacteria that can kill an amphibian fungal pathogen, Batrachochytrium dendrobatidis. Some amphibians die from B. dendrobatidis infection, whereas others do not. The bacteria that can kill B. dendrobatidis, called anti-B. dendrobatidis bacteria, are thought to influence the B. dendrobatidis infection outcome for the amphibian. Yet how anti-B. dendrobatidis bacterial species vary among amphibian species and populations is unknown. We determined the distribution of anti-B. dendrobatidis bacterial species among three salamander species (n = 61) sampled at three localities. We identified 50 unique anti-B. dendrobatidis bacterial species and found that all of the tested salamanders were negative for B. dendrobatidis. Five anti-B. dendrobatidis bacterial species were commonly detected, suggesting a stable, functional association with these salamanders. The number of anti-B. dendrobatidis bacteria per individual varied among localities but not among co-occurring salamander species, demonstrating that environment is more influential than host factors in structuring the anti-B. dendrobatidis bacterial community. These anti-B. dendrobatidis bacteria may serve a protective function for their salamander hosts.

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Single infection with Batrachochytrium dendrobatidis or Ranavirus does not increase probability of co-infection in a montane community of amphibians

Scientific Reports ◽

10.1038/s41598-020-78196-3 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Jaime Bosch ◽

Camino Monsalve-Carcaño ◽

Stephen J. Price ◽

Jon Bielby

Keyword(s):

Batrachochytrium Dendrobatidis ◽

Disease Outbreaks ◽

Single Infection ◽

Chytrid Fungus ◽

Population Declines ◽

Emerging Pathogens ◽

Amphibian Species ◽

Management Interventions ◽

Amphibian Chytrid Fungus ◽

Common Situation

AbstractUnderstanding the occurrence and consequence of co-infections can be useful in designing disease management interventions. Amphibians are the most highly threatened vertebrates, and emerging pathogens are a serious threat to their conservation. The amphibian chytrid fungus and the viruses of the Ranavirus genus are already widely distributed, causing disease outbreaks and population declines worldwide. However, we lack information about the occurrence and consequences of coinfection with these pathogens across age-classes of amphibian hosts. Here, we analyze the occurrence of infection of the amphibian chytrid fungus and ranaviruses during one season in two susceptible amphibian species at two different locations at which outbreaks have occurred. We found that the co-occurrence of both pathogens in a particular host is not common except in highly susceptible life-stages, and that single infections are the most common situation. Moreover, we found that the occurrence of one pathogen in a particular host did not predict the occurrence of the other. We attribute these results to the niches in which both pathogens proliferate in amphibian hosts.

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Review: Examining the Natural Role of Amphibian Antimicrobial Peptide Magainin

Molecules ◽

10.3390/molecules25225436 ◽

2020 ◽

Vol 25 (22) ◽

pp. 5436

Author(s):

Katelyn A. M. McMillan ◽

Melanie R. Power Coombs

Keyword(s):

Immune System ◽

Batrachochytrium Dendrobatidis ◽

Conservation Strategy ◽

Population Declines ◽

Small Peptides ◽

Amphibian Species ◽

Host Defense Peptides ◽

African Clawed Frog ◽

The North ◽

Clawed Frog

Host defense peptides (HDPs) are a group of antimicrobial peptides (AMPs) that are crucial components of the innate immune system of many different organisms. These small peptides actively kill microbes and prevent infection. Despite the presence of AMPs in the amphibian immune system, populations of these organisms are in decline globally. Magainin is an AMP derived from the African clawed frog (Xenopus laevis) and has displayed potent antimicrobial effects against a wide variety of microbes. Included in this group of microbes are known pathogens of the African clawed frog and other amphibian species. Arguably, the most deleterious amphibious pathogen is Batrachochytrium dendrobatidis, a chytrid fungus. Investigating the mechanism of action of magainin can help understand how to effectively fight off infection. By understanding amphibian AMPs’ role in the frog, a potential conservation strategy can be developed for other species of amphibians that are susceptible to infections, such as the North American green frog (Rana clamitans). Considering that population declines of these organisms are occurring globally, this effort is crucial to protect not only these organisms but the ecosystems they inhabit as well.

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Inhibition of Batrachochytrium dendrobatidis Caused by Bacteria Isolated from the Skin of Boreal Toads, Anaxyrus (Bufo) boreas boreas, from Grand Teton National Park, Wyoming, USA

Microbiology Insights ◽

10.4137/mbi.s13639 ◽

2014 ◽

Vol 7 ◽

pp. MBI.S13639 ◽

Cited By ~ 13

Author(s):

Shawna T. Park ◽

Amanda M. Collingwood ◽

Sophie St-Hilaire ◽

Peter P. Sheridan

Keyword(s):

National Park ◽

Batrachochytrium Dendrobatidis ◽

Chytrid Fungus ◽

Bacterial Isolates ◽

Skin Microbiota ◽

Amphibian Species ◽

Bufo Boreas ◽

Grand Teton National Park ◽

Boreal Toads

The chytrid fungus Batrachochytrium dendrobatidis is a significant cause of the worldwide decline in amphibian populations; however, various amphibian species are capable of coexisting with B. dendrobatidis. Among them are boreal toads ( Anaxyrus ( Bufo) boreas boreas) located in Grand Teton National Park (GTNP) in Wyoming, USA. The purpose of this study was to identify cultivable bacterial isolates from the skin microbiota of boreal toads from GTNP and determine if they were capable of inhibiting B. dendrobatidis in vitro, and therefore might be a factor in the toad's coexistence with this pathogen. Isolates from 6 of 21 genera tested were found to inhibit the growth of B. dendrobatidis. These bacteria represent diverse lineages such as the Gammaproteobacteria, the Betaproteobacteria, and the Bacteroidetes/Chlorobium groups. We propose that these bacteria compete via microbial antagonism with B. dendrobatidis.

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Reproductive phenology of the American Bullfrog in subtropical Brazil: photoperiod as a main determinant of seasonal activity

Anais da Academia Brasileira de Ciências ◽

10.1590/0001-3765201620150694 ◽

2016 ◽

Vol 88 (3 suppl) ◽

pp. 1909-1921 ◽

Cited By ~ 1

Author(s):

CAMILA I. MEDEIROS ◽

CAMILA BOTH ◽

IGOR L. KAEFER ◽

SONIA Z. CECHIN

Keyword(s):

Life Histories ◽

Management Strategies ◽

Reproductive Activity ◽

Ex Situ ◽

Reproductive Phenology ◽

High Fertility ◽

Seasonal Activity ◽

Population Declines ◽

American Bullfrog ◽

The North

ABSTRACT The North American bullfrog Lithobates catesbeianus continues to invade ecosystems worldwide, potentially causing population declines and even extinctions. Within its native distribution, bullfrogs show prolonged reproductive seasons and high fertility. However, data on breeding biology of bullfrogs ex-situ in invaded localities mainly comes from anecdotal reports. Understanding how invasive species are adjusting their life histories to new colonized environments is important for conservation purposes. Here we describe temporal and spatial abundance, calling activity, spawning and tadpole distribution of bullfrogs in southern Brazil. Eighteen samplings occurred during one year. The abundance of individuals was positively related to longer photoperiods and higher temperatures. Reproductive activity was also positively associated with longer photoperiods. Calling sites, spawning and tadpoles were associated with microhabitats presenting hydrophytes, which may provide shelter and thermal stability to bullfrogs. The reproductive seasonal activity of bullfrogs can be highly variable across its growing geographical range, but in subtropical Brazil it is associated with photoperiod, a highly predictable abiotic determinant. In our study area, bullfrogs presented a breeding season twice as long as that observed in some native localities. We suggest that management strategies directed to bullfrog populations must consider the habitat structures and seasonal regimes determined by each invaded environment.

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Establishement of a national monitoring program based on environmental DNA for amphibians and the chytrid fungus Batrachochytrium dendrobatidis

ARPHA Conference Abstracts ◽

10.3897/aca.4.e65362 ◽

2021 ◽

Vol 4 ◽

Author(s):

Omneya Osman ◽

Johan Andersson ◽

Tomas Larsson ◽

Mats Töpel ◽

Alexander Eiler

Keyword(s):

Batrachochytrium Dendrobatidis ◽

National Level ◽

Monitoring Program ◽

12S Rrna ◽

Rrna Gene ◽

Chytrid Fungus ◽

Rana Arvalis ◽

Amphibian Species ◽

National Monitoring ◽

Wide Range

National monitoring programs provide the basis for evaluating the integrity of ecosystems, their responses to disturbances, and the success of actions taken to conserve or recover biodiversity. In this study, we successfully established a national program for the invasive chytrid fungus Batrachochytrium dendrobatidis (Bd) based on dual TaqMan assays. Amphibian diversity based on metabarcoding of the mitochondrial 12S rRNA gene was also performed. Assays were optimized for sensitive detection of target species from a wide range of amphibian ponds with variable potential of inhibitions for eDNA based detection. An amphibian mock community of 5 species was used to validate the metabarcoding approach while internal standards were used in the case of the dual TaqMan assays. First sampling of over 170 ponds in Norway resulted in Bd detection in 12 environmental samples and one swab sample taken over multiple years indicating the establishment of Bd in Norway. Five amphibian species Bufo bufo, Lissotriton vulgaris, Triturus cristatus, Rana arvalis and Rana temporaria as predicted from data in long-term citizen science reporting systems were widely detected in the collected eDNA samples. Our large scale-monitoring program indicates a low risk of a Bd outbreak and amphibian decline caused by chytridiomycosis but continued monitoring is recommended in the future. These findings indicate that eDNA is an effective method to detect invasive species, and to monitor endangered amphibian species. Still, several shortcomings (such as PCR inhibitors and sample volume) were identified that need to be addressed to improve eDNA-based monitoring at the national level.

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Ancestral chytrid pathogen remains hypervirulent following its long coevolution with amphibian hosts

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.0833 ◽

2019 ◽

Vol 286 (1904) ◽

pp. 20190833 ◽

Cited By ~ 3

Author(s):

Minjie Fu ◽

Bruce Waldman

Keyword(s):

Batrachochytrium Dendrobatidis ◽

Population Declines ◽

Amphibian Species ◽

South Korean ◽

Global Pandemic ◽

Litoria Caerulea ◽

Experimental Treatments ◽

Amphibian Chytrid Fungus ◽

Genomic Recombination ◽

Blank Solution

Many amphibian species around the world, except in Asia, suffer morbidity and mortality when infected by the emerging infectious pathogen Batrachochytrium dendrobatidis (Bd). A lineage of the amphibian chytrid fungus isolated from South Korean amphibians (BdAsia-1) is evolutionarily basal to recombinant global pandemic lineages (BdGPL) associated with worldwide amphibian population declines. In Asia, the Bd pathogen and its amphibian hosts have coevolved over 100 years or more. Thus, resilience of Asian amphibian populations to infection might result from attenuated virulence of endemic Bd lineages, evolved immunity to the pathogen or both. We compared susceptibilities of an Australasian amphibian, Litoria caerulea , known to lack resistance to BdGPL, with those of three Korean species, Bufo gargarizans , Bombina orientalis and Hyla japonica , after inoculation with BdAsia-1, BdGPL or a blank solution. Subjects became infected in all experimental treatments but Korean species rapidly cleared themselves of infection, regardless of Bd lineage. They survived with no apparent secondary effects. By contrast, L. caerulea , after infection by either BdAsia-1 or BdGPL, suffered deteriorating body condition and carried progressively higher Bd loads over time. Subsequently, most subjects died. Comparing their effects on L. caerulea , BdAsia-1 induced more rapid disease progression than BdGPL. The results suggest that genomic recombination with other lineages was not necessary for the ancestral Bd lineage to evolve hypervirulence over its long period of coevolution with amphibian hosts. The pathogen's virulence may have driven strong selection for immune responses in endemic Asian amphibian host species.

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Phylogenetic investigation of skin sloughing rates in frogs: relationships with skin characteristics and disease-driven declines

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.2378 ◽

2019 ◽

Vol 286 (1896) ◽

pp. 20182378 ◽

Cited By ~ 4

Author(s):

Michel E. B. Ohmer ◽

Rebecca L. Cramp ◽

Craig R. White ◽

Peter S. Harlow ◽

Michael S. McFadden ◽

...

Keyword(s):

Batrachochytrium Dendrobatidis ◽

Phylogenetic Signal ◽

Interspecific Variation ◽

Phylogenetic Position ◽

Turnover Rates ◽

Amphibian Skin ◽

Amphibian Species ◽

Wide Range ◽

Skin Morphology ◽

And Function

Amphibian skin is highly variable in structure and function across anurans, and plays an important role in physiological homeostasis and immune defence. For example, skin sloughing has been shown to reduce pathogen loads on the skin, such as the lethal fungus Batrachochytrium dendrobatidis ( Bd ), but interspecific variation in sloughing frequency is largely unknown. Using phylogenetic linear mixed models, we assessed the relationship between skin turnover rate, skin morphology, ecological traits and overall evidence of Bd -driven declines. We examined skin sloughing rates in 21 frog species from three continents, as well as structural skin characteristics measured from preserved specimens. We found that sloughing rate varies significantly with phylogenetic group, but was not associated with evidence of Bd -driven declines, or other skin characteristics examined. This is the first comparison of sloughing rate across a wide range of amphibian species, and creates the first database of amphibian sloughing behaviour. Given the strong phylogenetic signal observed in sloughing rate, approximate sloughing rates of related species may be predicted based on phylogenetic position. While not related to available evidence of declines, understanding variation in sloughing rate may help explain differences in the severity of infection in genera with relatively slow skin turnover rates (e.g. Atelopus ).

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Recovery and resiliency of skin microbial communities on the southern leopard frog (Lithobates sphenocephalus) following two biotic disturbances

Animal Microbiome ◽

10.1186/s42523-020-00053-5 ◽

2020 ◽

Vol 2 (1) ◽

Author(s):

Denita M. Weeks ◽

Matthew J. Parris ◽

Shawn P. Brown

Keyword(s):

Microbial Communities ◽

Fungal Pathogen ◽

Bacterial Species ◽

Leopard Frog ◽

Multiple Time ◽

Population Declines ◽

Community Interactions ◽

Amphibian Species ◽

Functional Relationships ◽

Species Specific

Abstract Background Microorganisms have intimate functional relationships with invertebrate and vertebrate taxa, with the potential to drastically impact health outcomes. Perturbations that affect microbial communities residing on animals can lead to dysbiosis, a change in the functional relationship, often associated with disease. Batrachochytrium dendrobatidis (Bd), a fungal pathogen of amphibians, has been responsible for catastrophic amphibian population declines around the globe. Amphibians harbor a diverse cutaneous microbiome, including some members which are known to be antagonistic to Bd (anti-Bd). Anti-Bd microorganisms facilitate the ability of some frog populations to persist in the presence of Bd, where other populations that lack anti-Bd microorganisms have declined. Research suggests disease-antagonistic properties of the microbiome may be a function of microbial community interactions, rather than individual bacterial species. Conservation efforts have identified amphibian-associated bacteria that exhibit anti-fungal properties for use as ‘probiotics’ on susceptible amphibian populations. Probiotic application, usually with a single bacterial species, may benefit from a greater understanding of amphibian species-specific microbiome responses to disturbances (e.g. dysbiosis vs. recovery). We assessed microbiome responses to two microbial disturbance events over multiple time points. Results Exposing Lithobates sphenocephalus (southern leopard frog) adults to the biopesticidal bacteria Bacillus thuringiensis, followed by exposure to the fungal pathogen Bd, did not have long term impacts on the microbiome. After initial shifts, microbial communities recovered and returned to a state that resembled pre-disturbance. Conclusions Our results indicate microbial communities on L. sphenocephalus are robust and resistant to permanent shifts from some disturbances. This resiliency of microbial communities may explain why L. sphenocephalus is not experiencing the population declines from Bd that impacts many other species. Conservation efforts may benefit from studies outlining amphibian species-specific microbiome responses to disturbances (e.g. dysbiosis vs. recovery). If microbial communities on a threatened amphibian species are unlikely to recover following a disturbance, additional measures may be implemented to ameliorate the impacts of physical and chemical stressors on host-associated microbial communities.

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