An official website of the United States government
Considerable attention has been directed to studying the infection dynamics of the fungal pathogenBatrachochytrium dendrobatidis(Bd) affecting amphibians in the high elevations of the Neotropics. However, lowland forests of the same realm remain comparatively understudied in this context. Herein, we attempt to bridge this gap by measuring the prevalence ofBdvia quantitative polymerase chain reaction (qPCR) in several anuran taxa inhabiting the Amazonian lowlands in the northeast of Ecuador. To this end, we sampled 207 anurans from 10 different families, 25 different genera, and 55 distinct host species originally collected in 2008. Taxonomy (at the family level), morphology (i.e. weight and snout-vent length), and life-long aquatic dependency of hosts (i.e. aquatic index) were also compiled to serve as potential predictors ofBdinfection status. Our findings revealed a relatively highBdprevalence of 58%, with 88% of sampled anuran families testing positive for the fungus at varying proportions. Model selection involving fitting and testing several different linear models, including mixed linear models, revealed a significant negative relationship between host weight andBdinfection status (p < 0.01). However, no significant associations were observed between taxonomy, aquatic dependency, snout-vent length, andBdinfections. In addition, we only detected the global panzootic lineage ofBd(Bd-GPL) and not theBd-Asia-2/Bd-Brazil lineage via qPCR single nucleotide polymorphism (SNP) genotyping. Our findings contribute to the understanding ofBddynamics in the Neotropical lowlands and emphasize the need for future research on the ecological factors influencingBdin the Amazon and their implications for amphibian conservation.
more »
« less
Infection with Batrachochytrium dendrobatidis is common in tropical lowland habitats: Implications for amphibian conservation
Abstract Numerous species of amphibians declined in Central America during the 1980s and 1990s. These declines mostly affected highland stream amphibians and have been primarily linked to chytridiomycosis, a deadly disease caused by the chytrid fungusBatrachochytrium dendrobatidis(Bd). Since then, the majority of field studies on Bd in the Tropics have been conducted in midland and highland environments (>800 m) mainly because the environmental conditions of mountain ranges match the range of ideal abiotic conditions for Bd in the laboratory. This unbalanced sampling has led researchers to largely overlook host–pathogen dynamics in lowlands, where other amphibian species declined during the same period. We conducted a survey testing for Bd in 47 species (n = 348) in four lowland sites in Costa Rica to identify local host–pathogen dynamics and to describe the abiotic environment of these sites. We detected Bd in three sampling sites and 70% of the surveyed species. We found evidence that lowland study sites exhibit enzootic dynamics with low infection intensity and moderate to high prevalence (55% overall prevalence). Additionally, we found evidence that every study site represents an independent climatic zone, where local climatic differences may explain variations in Bd disease dynamics. We recommend more detection surveys across lowlands and other sites that have been historically considered unsuitable for Bd occurrence. These data can be used to identify sites for potential disease outbreaks and amphibian rediscoveries.
more »
« less
- Award ID(s):
- 1633948
- PAR ID:
- 10089586
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 9
- Issue:
- 8
- ISSN:
- 2045-7758
- Page Range / eLocation ID:
- p. 4917-4930
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract To combat the threat of emerging infectious diseases in wildlife, ecoimmunologists seek to understand the complex interactions among pathogens, their hosts, and their shared environments. The cutaneous fungal pathogen Batrachochytrium dendrobatidis (Bd), has led to the decline of innumerable amphibian species, including the Panamanian golden frog (Atelopus zeteki). Given that Bd can evade or dampen the acquired immune responses of some amphibians, nonspecific immune defenses are thought to be especially important for amphibian defenses against Bd. In particular, skin secretions constitute a vital component of amphibian innate immunity against skin infections, but their role in protecting A. zeteki from Bd is unknown. We investigated the importance of this innate immune component by reducing the skin secretions from A. zeteki and evaluating their effectiveness against Bd in vitro and in vivo. Following exposure to Bd in a controlled inoculation experiment, we compared key disease characteristics (e.g., changes in body condition, prevalence, pathogen loads, and survival) among groups of frogs that had their skin secretions reduced and control frogs that maintained their skin secretions. Surprisingly, we found that the skin secretions collected from A. zeteki increased Bd growth in vitro. This finding was further supported by infection and survival patterns in the in vivo experiment where frogs with reduced skin secretions tended to have lower pathogen loads and survive longer compared to frogs that maintained their secretions. These results suggest that the skin secretions of A. zeteki are not only ineffective at inhibiting Bd but may enhance Bd growth, possibly leading to greater severity of disease and higher mortality in this highly vulnerable species. These results differ from those of previous studies in other amphibian host species that suggest that skin secretions are a key defense in protecting amphibians from developing severe chytridiomycosis. Therefore, we suggest that the importance of immune components cannot be generalized across all amphibian species or over time. Moreover, the finding that skin secretions may be enhancing Bd growth emphasizes the importance of investigating these immune components in detail, especially for species that are a conservation priority.more » « less
-
Abstract BackgroundHost microbiomes may differ under the same environmental conditions and these differences may influence susceptibility to infection. Amphibians are ideal for comparing microbiomes in the context of disease defense because hundreds of species face infection with the skin-invading microbeBatrachochytrium dendrobatidis(Bd), and species richness of host communities, including their skin bacteria (bacteriome), may be exceptionally high. We conducted a landscape-scale Bd survey of six co-occurring amphibian species in Brazil’s Atlantic Forest. To test the bacteriome as a driver of differential Bd prevalence, we compared bacteriome composition and co-occurrence network structure among the six focal host species. ResultsIntensive sampling yielded divergent Bd prevalence in two ecologically similar terrestrial-breeding species, a group with historically low Bd resistance. Specifically, we detected the highest Bd prevalence inIschnocnema henseliibut no Bd detections inHaddadus binotatus.Haddadus binotatuscarried the highest bacteriome alpha and common core diversity, and a modular network partitioned by negative co-occurrences, characteristics associated with community stability and competitive interactions that could inhibit Bd colonization. ConclusionsOur findings suggest that community structure of the bacteriome might drive Bd resistance inH. binotatus, which could guide microbiome manipulation as a conservation strategy to protect diverse radiations of direct-developing species from Bd-induced population collapses.more » « less
-
ABSTRACT Studying declining and rare species is inherently challenging, particularly when the cause of rarity is emerging infectious diseases (EIDs). Tracking changes in the distribution of pathogens that cause EIDs, and the species made scarce by them, is necessary for conservation efforts, but it is often a time and resource intensive task. Here, we demonstrate how using environmental DNA (eDNA) to detect rare species—and the pathogens that threaten them—can be a powerful tool to understand disease dynamics and develop effective conservation strategies. Amphibian populations around the world have undergone rapid declines and extinctions due to the emerging fungal pathogen,Batrachochytrium dendrobatidis(Bd). We developed and validated a qPCR assay using eDNA sampling methods for some of the most imperiled amphibian species, harlequin frogs (Atelopus varius,Atelopus zeteki,andAtelopus chiriquiensis), and applied this assay in concert with a standard qPCR assay forBdin rainforest streams of Panamá. We confirmed the presence ofAtelopusat sampling locations across three regions. In addition, we used genomic analysis of eDNA samples to show thatBdin Panamá falls within the Global Panzootic Lineage, a lineage associated with disease‐induced declines. We detectedBdDNA in most of our historic sites, and its concentration in water samples correlated with stream characteristics and the pathogen load of the local amphibian community. These results suggest that some populations ofAtelopuspersist in their historic localities. They also show how eDNA analysis can be effectively used for monitoring species presence, pathogen concentrations, and the distribution and spread of pathogen lineages. EIDs are a growing threat to endangered species around the world. Simultaneous detection of rare and declining host species and their pathogens with eDNA will help to provide key insights for effective conservation management.more » « less
-
Abstract Infectious disease systems frequently exhibit strong seasonal patterns, yet the mechanisms that underpin intra‐annual cycles are unclear, particularly in tropical regions. We hypothesized that host immune function fluctuates seasonally, contributing to oscillations in infection patterns in a tropical disease system. To test this hypothesis, we investigated a key host defense of amphibians against a lethal fungal pathogen,Batrachochytrium dendrobatidis(Bd). We integrated two field experiments in which we perturbed amphibian skin secretions, a critical host immune mechanism, in Panamanian rocket frogs (Colostethus panamansis). We found that this immunosuppressive technique of reducing skin secretions in wild frog populations increasedBdprevalence and infection intensity, indicating that this immune defense contributes to resistance toBdin wild frog populations. We also found that the chemical composition and anti‐Bdeffectiveness of frog skin secretions varied across seasons, with greater pathogen inhibition during the dry season relative to the wet season. These results suggest that the effectiveness of this host defense mechanism shifts across seasons, likely contributing to seasonal infection patterns in a lethal disease system. More broadly, our findings indicate that host immune defenses can fluctuate across seasons, even in tropical regions where temperatures are relatively stable, which advances our understanding of intra‐annual cycles of infectious disease dynamics.more » « less
