title: Effects of Pesticide Mixtures on Host-Pathogen Dynamics of the Amphibian Chytrid Fungus.
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.
authors.affiliation: Texas Research Institute for Environmental Studies, Sam Houston State University, Huntsville, Texas, United States of America; Department of Integrative Biology, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Julia C
authors.initials: JC
authors.lastname: Buck
authors.affiliation: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
authors.forename: Jessica
authors.initials: J
authors.lastname: Hua
authors.affiliation: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
authors.forename: William R
authors.initials: WR
authors.lastname: Brogan
authors.affiliation: Department of Integrative Biology, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Trang D
authors.initials: TD
authors.lastname: Dang
authors.affiliation: Environmental Sciences Graduate Program, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Jenny
authors.initials: J
authors.lastname: Urbina
authors.affiliation: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
authors.forename: Randall J
authors.initials: RJ
authors.lastname: Bendis
authors.affiliation: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
authors.forename: Aaron B
authors.initials: AB
authors.lastname: Stoler
authors.affiliation: Department of Integrative Biology, Oregon State University, Corvallis, Oregon, United States of America; Environmental Sciences Graduate Program, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Andrew R
authors.initials: AR
authors.lastname: Blaustein
authors.affiliation: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
authors.forename: Rick A
authors.initials: RA
authors.lastname: Relyea
mesh_terms: D015084:2,4-Dichlorophenoxyacetic Acid / Q000494:pharmacology; D000818:Animals; D001001:Anura / Q000254:growth & development / Q000382:microbiology*; D001280:Atrazine / Q000494:pharmacology; D012721:Carbaryl / Q000494:pharmacology; D004390:Chlorpyrifos / Q000494:pharmacology; D008411:Chytridiomycota / Q000472:pathogenicity* / Q000502:physiology; D015169:Colony Count, Microbial; D004338:Drug Combinations; D004726:Endosulfan / Q000494:pharmacology; D005998:Glycine / Q000031:analogs & derivatives / Q000494:pharmacology; D006540:Herbicides / Q000494:pharmacology*; D054884:Host-Pathogen Interactions; D007306:Insecticides / Q000494:pharmacology*; D007814:Larva / Q000187:drug effects / Q000254:growth & development / Q000382:microbiology; D008675:Metamorphosis, Biological / Q000187:drug effects* / Q000502:physiology; D026023:Permethrin / Q000494:pharmacology; D013045:Species Specificity; D016019:Survival Analysis; D014052:Toluidines / Q000494:pharmacology; D000097797:Glyphosate
chemical_list: D015084:2,4-Dichlorophenoxyacetic Acid; D001280:Atrazine; D012721:Carbaryl; D004390:Chlorpyrifos; D004338:Drug Combinations; D004726:Endosulfan; D005998:Glycine; D006540:Herbicides; D007306:Insecticides; D026023:Permethrin; D014052:Toluidines; D000097797:Glyphosate; C043377:acetochlor