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.

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Understanding how ecological interactions mitigate the impacts of perturbations such as pesticides in biological communities is an important basic and applied question for ecologists. In aquatic ecosystems, new evidence from microcosm experiments suggests that submerged macrophytes can buffer cladocerans from pulse exposures to the widely used insecticide malathion, and that mitigation increases with macrophyte density. However, whether these results scale up to more complex aquatic communities where ecological interactions such as competition can alter toxicity is unknown. Further, macrophyte abilities to mitigate different insecticide exposure scenarios (i.e. single versus repeated pulses) have never been tested. To address these gaps, we performed a factorial mesocosm experiment examining the influence of four macrophyte treatments (0, 10, 50, or 100 Elodea Canadensis shoots planted per mesocosm) crossed with three malathion exposure scenarios (no insecticide, single pulse, repeated pulses) on aquatic communities containing zooplankton, phytoplankton, periphyton, two snail species, and larval amphibians. In the absence of macrophytes, single malathion pulses caused short-term declines in cladoceran abundance followed by their rapid recovery, which precluded any indirect effects (i.e. trophic cascades). However, repeated malathion pulses caused cladoceran extinctions, resulting in persistent phytoplankton blooms and reduced abundance of one snail species. In contrast, with macrophytes present, even at low density, malathion had no effect on any taxa. We also discovered novel effects of macrophytes on the benthic food web. In the two highest macrophyte treatments, we observed trends of reduced periphyton biomass, decreased abundance of one snail species, and decreased amphibian time to and mass at metamorphosis. To our knowledge, this is the first evidence of negative submerged macrophyte effects on amphibians, a taxa of global conservation concern. Our findings suggest that facilitating macrophytes could be an important strategy for buffering freshwater communities from insecticides, though consideration of their impacts on animal species is necessary.

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Abstract-In ecotoxicology, appreciation is growing for the influence that ecological interactions have on the toxicity of contaminants, such as insecticides, to sensitive species. Most previous studies, however, have focused on factors that exacerbate insecticide effects on species, while factors that may mitigate these effects have been relatively ignored. In aquatic habitats, a small number of studies have shown that submersed macrophytes can remove some insecticides from the water column via sorption. Although examining sorption dynamics is important for understanding the environmental fate of insecticides, whether and to what extent macrophytes actually mitigate insecticide effects on aquatic species remains unknown. In the present study, the authors examined how much and how quickly several realistic densities of the macrophyte Elodea canadensis decreased the toxicity of the insecticide malathion to Daphnia magna, a keystone aquatic herbivore. To do this, the authors quantified Daphnia survival in outdoor test systems (0.95 L) exposed to a factorial combination of five Elodea densities crossed with five malathion concentrations. The authors discovered that malathion's lethality to Daphnia decreased with increasing Elodea density. Furthermore, the rate at which Elodea reduced malathion's toxicity in the water column increased with macrophyte density. These results provide strong evidence that submersed macrophytes can mitigate the ecological impacts of a popular insecticide and further support that ecological interactions can strongly influence contaminant environmental effects. Environ. Toxicol. Chem. 2013;32:699-706. # 2012 SETAC

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Some submersed macrophyte species rapidly sorb some insecticides from the water, potentially reducing exposure for aquatic species. The rates at which macrophytes remove insecticides, however, can differ widely among plant species. Furthermore, few studies have examined how much macrophytes actually influence insecticide toxicity to sensitive animals. The authors quantified the ability of several macrophyte species to mitigate insecticide toxicity by comparing the survival of the aquatic herbivore, Daphnia magna, following exposure to a factorial combination of 3 malathion concentrations (0 µg/L, 3 µg/L, and 24 µg/L) and 7 macrophyte treatments (no macrophytes, 4 different macrophyte monocultures, and 2 inert substrates: plastic plants and polypropylene rope). The authors also quantified the rate that different macrophytes reduced malathion's toxicity by exposing D. magna to water samples collected from each treatment after 2 h, 8 h, and 48 h of exposure. The results revealed that whereas 3 µg/L and 24 µg/L of malathion decimated D. magna in the no-macrophyte, plastic plant, and rope treatments, all 4 macrophyte species strongly mitigated these effects. When the authors compared the rate at which malathion's toxicity decreased, they found that all macrophytes negated malathion's toxicity within 2 h, whereas it took more than 8 h in the absence of macrophytes or in the presence of inert substrates. These results demonstrate that numerous macrophyte species can equally and strongly mitigate insecticide toxicity, whereas inert substrates cannot.