The worldwide decline in amphibians has been attributed to several causes, especially habitat loss and disease. We identified a further factor, namely "habitat split"-defined as human-induced disconnection between habitats used by different life history stages of a species-which forces forest-associated amphibians with aquatic larvae to make risky breeding migrations between suitable aquatic and terrestrial habitats. In the Brazilian Atlantic Forest, we found that habitat split negatively affects the richness of species with aquatic larvae but not the richness of species with terrestrial development (the latter can complete their life cycle inside forest remnants). This mechanism helps to explain why species with aquatic larvae have the highest incidence of population decline. These findings reinforce the need for the conservation and restoration of riparian vegetation.
Habitat loss and disease are main drivers of global amphibian declines, yet the interaction between them remains largely unexplored. Here we show that paradoxically, habitat loss is negatively associated with occurrence, prevalence, and infection intensity of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in amphibian populations in the tropics. At a large spatial scale, increased habitat loss predicted lower disease risk in amphibian populations across Costa Rica and eastern Australia, even after jointly considering the effect of potential biotic and abiotic correlates. Lower host-species richness and suboptimal microclimates for Bd in disturbed habitats are potential mechanisms underlying this pattern. Furthermore, we found that anthropogenic deforestation practices biased to lowlands and natural vegetation remaining in inaccessible highlands explain increased Bd occurrence at higher elevations. At a smaller spatial scale, holding constant elevation, latitude, and macroclimate, we also found a negative relationship between habitat loss, and both Bd prevalence and infection intensity in frog populations in two landscapes of the Brazilian Atlantic Forest. Our results indicate that amphibians will be disproportionately affected by emerging diseases in pristine environments, and that, paradoxically, disturbed habitats may act as shelters from disease, but only for the very few species that can tolerate deforestation. Thus, tropical amphibian faunas are threatened both by destruction of natural habitats as well as increased disease in pristine forests. To curb further extinctions and develop effective mitigation and restoration programs we must look to interactions between habitat loss and disease, the two main factors at the root of global amphibian declines.chytridiomycosis | species diversity | anurans | Neotropics | pathogen
The recent global spread of the amphibian-killing fungus [Batrachochytrium dendrobatidis (Bd)] has been closely tied to anthropogenic activities; however, regional patterns of spread are not completely understood. Using historical samples, we can test whether Bd was a spreading or endemic pathogen in a region within a particular time frame, because those two disease states provide different predictions for the regional demographic dynamics and population genetics of Bd. Testing historical patterns of pathogen prevalence and population genetics under these predictions is key to understanding the evolution and origin of Bd. Focusing on the Atlantic Forest (AF) of Brazil, we used qPCR assays to determine the presence or absence of Bd on 2799 preserved postmetamorphic anurans collected between 1894 and 2010 and used semi-nested PCRs to determine the frequency of rRNA ITS1 haplotypes from 52 samples. Our earliest date of detection was 1894. A mean prevalence of 23.9% over time and spatiotemporal patterns of Bd clusters indicate that Bd has been enzootic in the Brazilian AF with no evidence of regional spread within the last 116 years. ITS1 haplotypes confirm the long-term presence of two divergent strains of Bd (BdGPL and Bd-Brazil) and three spatiotemporally broad genetic demes within BdGPL, indicating that Bd was not introduced into southeast Brazil by the bullfrog trade. Our data show that the evolutionary history and pathogen dynamics of Bd in Brazil is better explained by the endemic pathogen hypothesis.
Most amphibian species have biphasic life histories and undergo an ontogenetic shift from aquatic to terrestrial habitats. In deforested landscapes, streams and forest fragments are frequently disjunct, jeopardizing the life cycle of forest-associated amphibians with aquatic larvae. We tested the impact of habitat split--defined as human-induced disconnection between habitats used by different life-history stages of a species--on four forest-associated amphibian species in a severely fragmented landscape of the Brazilian Atlantic Forest. We surveyed amphibians in forest fragments with and without streams (referred to as wet and dry fragments, respectively), including the adjacent grass-field matrix. Our comparison of capture rates in dry fragments and nearby streams in the matrix allowed us to evaluate the number of individuals that engaged in high-risk migrations through nonforested habitats. Adult amphibians moved from dry fragments to matrix streams at the beginning of the rainy season, reproduced, and returned at the end of the breeding period. Juveniles of the year moved to dry fragments along with adults. These risky reproductive migrations through nonforested habitats that expose individuals to dehydration, predation, and other hazards may cause population declines in dry fragments. Indeed, capture rates were significantly lower in dry fragments compared with wet fragments. Declining amphibians would strongly benefit from investments in the conservation and restoration of riparian vegetation and corridors linking breeding and nonbreeding areas.
Animal-associated microbiomes are integral to host health, yet key biotic and abiotic factors that shape host-associated microbial communities at the global scale remain poorly understood. We investigated global patterns in amphibian skin bacterial communities, incorporating samples from 2,349 individuals representing 205 amphibian species across a broad biogeographic range. We analyzed how biotic and abiotic factors correlate with skin microbial communities using multiple statistical approaches. Global amphibian skin bacterial richness was consistently correlated with temperature-associated factors. We found more diverse skin microbiomes in environments with colder winters and less stable thermal conditions, compared to environments with warm winters and less annual temperature variation. We used bioinformatically predicted bacterial growth rates, dormancy genes, and antibiotic synthesis genes, as well as inferred bacterial thermal growth optima to propose mechanistic hypotheses that may explain the observed patterns. We conclude that temporal and spatial characteristics of the host's macro-environment mediate microbial diversity.
The recent increase in emerging fungal diseases is causing unprecedented threats to biodiversity. The origin of spread of the frog-killing fungus () is a matter of continued debate. To date, the historical amphibian declines in Brazil could not be attributed to chytridiomycosis; the high diversity of hosts coupled with the presence of several lineages predating the reported declines raised the hypothesis that a hypervirulent genotype spread from Brazil to other continents causing the recent global amphibian crisis. We tested for a spatio-temporal overlap between and areas of historical amphibian population declines and extinctions in Brazil. A spatio-temporal convergence between and declines would support the hypothesis that Brazilian amphibians were not adapted to prior to the reported declines, thus weakening the hypothesis that Brazil was the global origin of emergence. Alternatively, a lack of spatio-temporal association between and frog declines would indicate an evolution of host resistance in Brazilian frogs predating 's global emergence further supporting Brazil as the potential origin of the panzootic. Here, we-screened over 30 000 museum-preserved tadpoles collected in Brazil between 1930 and 2015 and overlaid spatio-temporal data with areas of historical amphibian declines. We detected an increase in the proportion of-infected tadpoles during the peak of amphibian declines (1979-1987). We also found that clusters of -positive samples spatio-temporally overlapped with most records of amphibian declines in Brazil's Atlantic Forest. Our findings indicate that Brazil is post epizootic for chytridiomycosis and provide another piece to the puzzle to explain the origin of globally.
The 'dilution effect' (DE) hypothesis predicts that diverse host communities will show reduced disease. The underlying causes of pathogen dilution are complex, because they involve non-additive (driven by host interactions and differential habitat use) and additive (controlled by host species composition) mechanisms. Here, we used measures of complementarity and selection traditionally employed in the field of biodiversity-ecosystem function (BEF) to quantify the net effect of host diversity on disease dynamics of the amphibian-killing fungus Batrachochytrium dendrobatidis (Bd). Complementarity occurs when average infection load in diverse host assemblages departs from that of each component species in uniform populations. Selection measures the disproportionate impact of a particular species in diverse assemblages compared with its performance in uniform populations, and therefore has strong additive and non-additive properties. We experimentally infected tropical amphibian species of varying life histories, in single-and multi-host treatments, and measured individual Bd infection loads. Host diversity reduced Bd infection in amphibians through a mechanism analogous to complementarity (sensu BEF), potentially by reducing shared habitat use and transmission among hosts. Additionally, the selection component indicated that one particular terrestrial species showed reduced infection loads in diverse assemblages at the expense of neighbouring aquatic hosts becoming heavily infected. By partitioning components of diversity, our findings underscore the importance of additive and non-additive mechanisms underlying the DE.
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