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Fragile coexistence of a global chytrid pathogen with amphibian populations is mediated by environment and demography.

ABSTRACT: Unravelling the multiple interacting drivers of host-pathogen coexistence is crucial in understanding how an apparently stable state of endemism may shift towards an epidemic and lead to biodiversity loss. Here, we investigate the apparent coexistence of the global amphibian pathogen Batrachochytrium dendrobatidis (Bd) with Bombina variegata populations in The Netherlands over a 7-year period. We used a multi-season mark-recapture dataset and assessed potential drivers of coexistence (individual condition, environmental mediation and demographic compensation) at the individual and population levels. We show that even in a situation with a clear cost incurred by endemic Bd, population sizes remain largely stable. Current environmental conditions and an over-dispersed pathogen load probably stabilize disease dynamics, but as higher temperatures increase infection probability, changing environmental conditions, for example a climate-change-driven rise in temperature, could unbalance the current fragile host-pathogen equilibrium. Understanding the proximate mechanisms of such environmental mediation and of site-specific differences in infection dynamics can provide vital information for mitigation actions.

SUBMITTER: Spitzen-van der Sluijs A

PROVIDER: S-EPMC5647299 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Fragile coexistence of a global chytrid pathogen with amphibian populations is mediated by environment and demography.

Spitzen-van der Sluijs Annemarieke A Canessa Stefano S Martel An A Pasmans Frank F

Proceedings. Biological sciences 20171001 1864

Unravelling the multiple interacting drivers of host-pathogen coexistence is crucial in understanding how an apparently stable state of endemism may shift towards an epidemic and lead to biodiversity loss. Here, we investigate the apparent coexistence of the global amphibian pathogen <i>Batrachochytrium dendrobatidis</i> (Bd) with <i>Bombina variegata</i> populations in The Netherlands over a 7-year period. We used a multi-season mark-recapture dataset and assessed potential drivers of coexisten ...[more]

PMID: 28978729

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Project description:The rapid worldwide emergence of the amphibian pathogen Batrachochytrium dendrobatidis (Bd) is having a profound negative impact on biodiversity. However, global research efforts are fragmented and an overarching synthesis of global infection data is lacking. Here, we provide results from a community tool for the compilation of worldwide Bd presence and report on the analyses of data collated over a four-year period. Using this online database, we analysed: 1) spatial and taxonomic patterns of infection, including amphibian families that appear over- and under-infected; 2) relationships between Bd occurrence and declining amphibian species, including associations among Bd occurrence, species richness, and enigmatic population declines; and 3) patterns of environmental correlates with Bd, including climate metrics for all species combined and three families (Hylidae, Bufonidae, Ranidae) separately, at both a global scale and regional (U.S.A.) scale. These associations provide new insights for downscaled hypothesis testing. The pathogen has been detected in 52 of 82 countries in which sampling was reported, and it has been detected in 516 of 1240 (42%) amphibian species. We show that detected Bd infections are related to amphibian biodiversity and locations experiencing rapid enigmatic declines, supporting the hypothesis that greater complexity of amphibian communities increases the likelihood of emergence of infection and transmission of Bd. Using a global model including all sampled species, the odds of Bd detection decreased with increasing temperature range at a site. Further consideration of temperature range, rather than maximum or minimum temperatures, may provide new insights into Bd-host ecology. Whereas caution is necessary when interpreting such a broad global dataset, the use of our pathogen database is helping to inform studies of the epidemiology of Bd, as well as enabling regional, national, and international prioritization of conservation efforts. We provide recommendations for adaptive management to enhance the database utility and relevance.

Project description:Anthropogenic and natural stressors often interact to affect organisms. Amphibian populations are undergoing unprecedented declines and extinctions with pesticides and emerging infectious diseases implicated as causal factors. Although these factors often co-occur, their effects on amphibians are usually examined in isolation. We hypothesized that exposure of larval and metamorphic amphibians to ecologically relevant concentrations of pesticide mixtures would increase their post-metamorphic susceptibility to the fungus Batrachochytrium dendrobatidis (Bd), a pathogen that has contributed to amphibian population declines worldwide. We exposed five anuran species (Pacific treefrog, Pseudacris regilla; spring peeper, Pseudacris crucifer; Cascades frog, Rana cascadae; northern leopard frog, Lithobates pipiens; and western toad, Anaxyrus boreas) from three families to mixtures of four common insecticides (chlorpyrifos, carbaryl, permethrin, and endosulfan) or herbicides (glyphosate, acetochlor, atrazine, and 2,4-D) or a control treatment, either as tadpoles or as newly metamorphic individuals (metamorphs). Subsequently, we exposed animals to Bd or a control inoculate after metamorphosis and compared survival and Bd load. Bd exposure significantly increased mortality in Pacific treefrogs, spring peepers, and western toads, but not in Cascades frogs or northern leopard frogs. However, the effects of pesticide exposure on mortality were negligible, regardless of the timing of exposure. Bd load varied considerably across species; Pacific treefrogs, spring peepers, and western toads had the highest loads, whereas Cascades frogs and northern leopard frogs had the lowest loads. The influence of pesticide exposure on Bd load depended on the amphibian species, timing of pesticide exposure, and the particular pesticide treatment. Our results suggest that exposure to realistic pesticide concentrations has minimal effects on Bd-induced mortality, but can alter Bd load. This result could have broad implications for risk assessment of amphibians; the outcome of exposure to multiple stressors may be unpredictable and can differ between species and life stages.

Dataset Information

Fragile coexistence of a global chytrid pathogen with amphibian populations is mediated by environment and demography.

Publications

Fragile coexistence of a global chytrid pathogen with amphibian populations is mediated by environment and demography.

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