Locality, time and heterozygosity affect chytrid infection in yellow-bellied toads

2020 ◽  
Vol 142 ◽  
pp. 225-237
Author(s):  
P Oswald ◽  
A Rodríguez ◽  
J Bourke ◽  
N Wagner ◽  
N de Buhr ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Breeding Season ◽  
Batrachochytrium Dendrobatidis ◽  
Infection Intensity ◽  
Sampling Period ◽  
Infection Prevalence ◽  
Infection Status ◽  
Population Declines ◽  
Amphibian Species ◽  
High Genetic Diversity

The chytrid fungus Batrachochytrium dendrobatidis (Bd) infects numerous amphibian species worldwide and is suggested to drive population declines and extinction events. We report a study of Bd infection at the northernmost distribution of the European yellow-bellied toad Bombina variegata. A total of 577 individuals from ponds in 16 study sites were sampled for DNA and Bd throughout the breeding season. Microsatellite genotyping revealed 3 genetic clusters for the host B. variegata with an overall low genetic diversity. One of the clusters displayed a low microsatellite heterozygosity, a high inbreeding coefficient as well as high Bd infection prevalence and intensities. Multi-model estimates identified site, time of sampling, and heterozygosity to be important predictors of an individual’s Bd infection status, and identified a strong effect of site on individual Bd infection intensity. The study site effects are suggestive of localized infection peaks, and the increase of individual Bd infection probabilities towards the end of the sampling period suggests cumulative infection during the breeding season. This study highlights the need for regular monitoring of Bd infection variables at multiple localities and times to gain insights into Bd dynamics. Due to the detected relationship between individual Bd infection status and heterozygosity, conservation measures should focus on the maintenance of high genetic diversity and connectivity within and among amphibian populations.

scholarly journals Fungal infection, decline and persistence in the only obligate troglodytic Neotropical salamander

PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9763
Author(s):  
Mizraim Olivares-Miranda ◽  
Vance T. Vredenburg ◽  
Julio C. García-Sánchez ◽  
Allison Q. Byrne ◽  
Erica B. Rosenblum ◽  
...  
Keyword(s):  
Batrachochytrium Dendrobatidis ◽  
Infection Intensity ◽  
Sampling Technique ◽  
Sympatric Species ◽  
Amphibian Declines ◽  
Small Range ◽  
Museum Specimens ◽  
Amphibian Species ◽  
Extant Population ◽  
Epidemic Wave

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.

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

2019 ◽  
Vol 286 (1904) ◽  
pp. 20190833 ◽  
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.

scholarly journals Body size mediates latitudinal population differences in response to Bd infection in two amphibian species.

2021 ◽  
Author(s):  
Sara Meurling ◽  
Maria Cortazar-Chinarro ◽  
Mattias Siljestam ◽  
David Ahlen ◽  
Erik Agren ◽  
...  
Keyword(s):  
Body Size ◽  
Batrachochytrium Dendrobatidis ◽  
Geographical Origin ◽  
Bufo Bufo ◽  
Northern Region ◽  
Population Declines ◽  
Rana Arvalis ◽  
Amphibian Species ◽  
Survival Difference ◽  
Species Survival

Populations of the same species may differ in their sensitivity to pathogens but the factors behind this variation are poorly understood. Moreover, infections may cause sub-lethal fitness effects even in species resistant or tolerant to disease. The chytrid fungus Batrachochytrium dendrobatidis (Bd), is a generalist pathogen which has caused amphibian population declines worldwide. In many species, Bd infection causes the disease chytridiomycosis, often leading to high mortality. We investigated how geographical origin affects tolerance to Bd by exposing newly metamorphosed individuals of two North European amphibians (moor frog Rana arvalis, common toad Bufo bufo) from two latitudinal regions to two different BdGPL strains. Bd exposure strongly lowered survival in B. bufo, and in both species survival was lower in the northern region, this difference being much stronger in B. bufo. Northern individuals were smaller in both species, and the survival difference between the regions was size-mediated with smaller individuals being more sensitive to Bd. In both species, Bd exposure led to sub-lethal effects in terms of reduced growth suggesting that even individuals surviving the infection may have reduced fitness mediated by smaller body size. Bd strain affected size-dependent mortality differently in the two regions. We discuss the possible mechanisms how body size and geographical origin can contribute to the present results.

scholarly journals Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus

2015 ◽  
Vol 282 (1805) ◽  
pp. 20142881 ◽  
Author(s):  
Matthew H. Becker ◽  
Jenifer B. Walke ◽  
Shawna Cikanek ◽  
Anna E. Savage ◽  
Nichole Mattheus ◽  
...  
Keyword(s):  
Batrachochytrium Dendrobatidis ◽  
Population Declines ◽  
Amphibian Species ◽  
Amphibian Population ◽  
New Approach ◽  
Skin Bacteria ◽  
Probiotic Treatment ◽  
Host Health ◽  
The Face ◽  
Inhibitory Bacteria

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.

scholarly journals Prevalence of the fungal pathogen Batrachochytrium dendrobatidis in amphibians of Costa Rica predated first-known epizootic

2018 ◽  
Author(s):  
Marina E. De León ◽  
Héctor Zumbado-Ulate ◽  
Adrián García-Rodríguez ◽  
Gilbert Alvarado ◽  
Hasan Sulaeman ◽  
...  
Keyword(s):  
Costa Rica ◽  
Fungal Pathogen ◽  
Batrachochytrium Dendrobatidis ◽  
Emerging Infectious Diseases ◽  
Infection Prevalence ◽  
Pcr Assay ◽  
Local Data ◽  
Amphibian Species ◽  
Genetic Lineages ◽  
Quantitative Pcr Assay

AbstractEmerging infectious diseases are a growing threat to biodiversity worldwide. Outbreaks of the infectious disease chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), have caused the decline and extinction of numerous amphibian species. In Costa Rica, a major decline event occurred in 1987, more than two decades before this pathogen was discovered. The loss of many species in Costa Rica is assumed to be due to Bd-epizootics, but there are few studies that provide data from amphibians in the time leading up to the proposed epizootics. In this study, we provide new data on Bd infection rates of amphibians collected throughout Costa Rica, in the decades prior to the epizootics. We used a quantitative PCR assay to test for Bd infection in 1016 specimens collected throughout Costa Rica. We found Bd-infected hosts collected as early as 1964, and a infection prevalence average per decade of just 4%. The infection prevalence remained relatively low and geographically constrained until the 1980s when epizootics are hypothesized to have occurred. After that time, infection prevalence increased three-fold and Bd-infected hosts we collected throughout the entire country. Our results, suggest that Bd may either have invaded Costa Rica earlier than previously known, and spread more slowly than previously reported, or that an endemic lineage of the pathogen may exists. To help visualize areas where future studies should take place, we provide a Bd habitat suitability model trained with local data. Studies that provide information on genetic lineages of Bd are needed to determine whether an endemic lineage of Bd or the Global Panzootic Lineage (identified from mass die off sites globally) was present in Costa Rica and responsible for the epizootics that caused amphibian communities to collapse.

scholarly journals Infectious disease threats to amphibian conservation

2018 ◽  
Vol 27 (Supplement) ◽  
pp. 81-90
Author(s):  
A.A. Cunningham
Keyword(s):  
Infectious Disease ◽  
Batrachochytrium Dendrobatidis ◽  
Biodiversity Loss ◽  
Amphibian Conservation ◽  
Disease Spread ◽  
Population Declines ◽  
Amphibian Species ◽  
Late 20Th Century ◽  
Amphibian Population ◽  
In The Wild

The unexplained decline of amphibian populations across the world was first recognised in the late 20th century. When investigated, most of these “enigmatic” declines have been shown to be due to one of two types of infectious disease: ranavirosis caused by infection with FV3-like ranavirus or with common midwife toad virus, or chytridiomycosis caused by infection with Batrachochytrium dendrobatidis or B. salamandrivorans. In all cases examined, infection has been via the human-mediated introduction of the pathogen to a species or population in which it has not naturally co-evolved. While ranaviruses and B. salamandrivorans have caused regionally localised amphibian population declines in Europe, the chytrid fungus, B. dendrobatidis, has caused catastrophic multi-species amphibian population declines and species extinctions globally. These diseases have already caused the loss of amphibian biodiversity, and over 40% of known amphibian species are threatened with extinction. If this biodiversity loss is to be halted, it is imperative that regulations are put in place – and enforced – to prevent the spread of known and yet-to-be discovered amphibian pathogens. Also, it is incumbent on those who keep or study amphibians to take measures to minimise the risk of disease spread, including from captive animals to those in the wild.

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

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.

scholarly journals Review: Examining the Natural Role of Amphibian Antimicrobial Peptide Magainin

Molecules ◽  
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.

scholarly journals Endemic Infection of Batrachochytrium dendrobatidis in Costa Rica: Implications for Amphibian Conservation at Regional and Species Level

Diversity ◽  
2019 ◽  
Vol 11 (8) ◽  
pp. 129 ◽  
Author(s):  
Héctor Zumbado-Ulate ◽  
Kiersten N. Nelson ◽  
Adrián García-Rodríguez ◽  
Gerardo Chaves ◽  
Erick Arias ◽  
...  
Keyword(s):  
Costa Rica ◽  
Batrachochytrium Dendrobatidis ◽  
Infection Intensity ◽  
Amphibian Conservation ◽  
Conservation Strategies ◽  
Amphibian Species ◽  
Current Impact ◽  
Taxonomic Groups ◽  
Species Descriptions ◽  
Effective Conservation

Batrachochytrium dendrobatidis (Bd) has been associated with the severe declines and extinctions of amphibians in Costa Rica that primarily occurred during the 1980s and 1990s. However, the current impact of Bd infection on amphibian species in Costa Rica is unknown. We aimed to update the list of amphibian species in Costa Rica and evaluate the prevalence and infection intensity of Bd infection across the country to aid in the development of effective conservation strategies for amphibians. We reviewed taxonomic lists and included new species descriptions and records for a total of 215 amphibian species in Costa Rica. We also sampled for Bd at nine localities from 2015–2018 and combined these data with additional Bd occurrence data from multiple studies conducted in amphibian communities across Costa Rica from 2005–2018. With this combined dataset, we found that Bd was common (overall infection rate of 23%) across regions and elevations, but infection intensity was below theoretical thresholds associated with mortality. Bd was also more prevalent in Caribbean lowlands and in terrestrial amphibians with an aquatic larval stage; meanwhile, infection load was the highest in direct-developing species (forest and stream-dwellers). Our findings can be used to prioritize regions and taxonomic groups for conservation strategies.

scholarly journals Genetic assessment reveals no population substructure and divergent regional and sex-specific histories in the Chachapoyas from northeast Peru

PLoS ONE ◽  
2020 ◽  
Vol 15 (12) ◽  
pp. e0244497
Author(s):  
Evelyn K. Guevara ◽  
Jukka U. Palo ◽  
Sanni Översti ◽  
Jonathan L. King ◽  
Maria Seidel ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Gene Flow ◽  
Demographic History ◽  
Population Decline ◽  
Population Substructure ◽  
Gene Pools ◽  
Population Declines ◽  
Montane Forests ◽  
High Genetic Diversity ◽  
Spanish Conquest

Many native populations in South America have been severely impacted by two relatively recent historical events, the Inca and the Spanish conquest. However decisive these disruptive events may have been, the populations and their gene pools have been shaped markedly also by the history prior to the conquests. This study focuses mainly on the Chachapoya peoples that inhabit the montane forests on the eastern slopes of the northern Peruvian Andes, but also includes three distinct neighboring populations (the Jívaro, the Huancas and the Cajamarca). By assessing mitochondrial, Y-chromosomal and autosomal diversity in the region, we explore questions that have emerged from archaeological and historical studies of the regional culture (s). These studies have shown, among others, that Chachapoyas was a crossroads for Coast-Andes-Amazon interactions since very early times. In this study, we examine the following questions: 1) was there pre-Hispanic genetic population substructure in the Chachapoyas sample? 2) did the Spanish conquest cause a more severe population decline on Chachapoyan males than on females? 3) can we detect different patterns of European gene flow in the Chachapoyas region? and, 4) did the demographic history in the Chachapoyas resemble the one from the Andean area? Despite cultural differences within the Chachapoyas region as shown by archaeological and ethnohistorical research, genetic markers show no significant evidence for past or current population substructure, although an Amazonian gene flow dynamic in the northern part of this territory is suggested. The data also indicates a bottleneck c. 25 generations ago that was more severe among males than females, as well as divergent population histories for populations in the Andean and Amazonian regions. In line with previous studies, we observe high genetic diversity in the Chachapoyas, despite the documented dramatic population declines. The diverse topography and great biodiversity of the northeastern Peruvian montane forests are potential contributing agents in shaping and maintaining the high genetic diversity in the Chachapoyas region.

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