Abstract
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.
Highlights
As ecosystems are increasingly threatened by anthropogenic factors, ecologists attempt to understand the impacts of these stressors on sensitive organisms
Pacific treefrogs, spring peepers, northern leopard frogs, and western toads in this pesticide treatment could not be exposed to Batrachochytrium dendrobatidis (Bd) and are excluded from analyses (Figs 1 and 2)
Mortality of western toads exposed to pesticides after metamorphosis was sufficiently high to allow us to test for interactive effects between pesticides and Bd
Summary
As ecosystems are increasingly threatened by anthropogenic factors, ecologists attempt to understand the impacts of these stressors on sensitive organisms. Instead, anthropogenic stressors such as contaminants can interact with natural stressors such as pathogens to produce unpredictable effects [1,2]. When organisms are exposed to contaminants, their ability to launch effective immune responses may be compromised, rendering them susceptible to disease [3,4,5]. Contaminants may affect the pathogen itself, for example, by inhibiting production of the infective stage [3]. Environmental influences on host-pathogen dynamics are complex, context-dependent, and require continued examination [6,7]
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