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.

Long term effects of carbaryl exposure on antiviral immune responses in Xenopus laevis

“…Indeed, carbaryl appears to be more toxic for fish (rainbow trout) with an LC 50 of 1.4 mg/L (1.4 ppm) for a 96 hr exposure time. Exposure to a sublethal dose of carbaryl has been shown to reduce host skin peptide defenses of several anurans species, which may increase susceptibility to infection by skin pathogens such as the chytrid fungus ( Batrachochytrium dendrobatidis ) [17–19]. To examine in more detail the potential immunomodulatory effects of carbaryl, we took advantage of the X. laevis /FV3 model system [20–22].…”

A pesticide paradox: Fungicides indirectly increase fungal infections

“…Corresponding Editor: Trenton W. J. Garner. 6 E-mail: jasonrohr@gmail.com (Gahl et al 2011, Buck et al 2015, Jones et al 2017, insecticides (Davidson et al 2007, Gaietto et al 2014, Buck et al 2015, Jones et al 2017, fungicides (Johnson et al 2003, Woodhams et al 2012, Gaietto et al 2014, Hudson et al 2016, and agricultural disinfectants (Johnson et al 2003, Bosch et al 2015. Additionally, many researchers are exploring biocides as management tools to control Bd (Woodhams et al 2011).…”

“…Indeed, many pesticides are known to be immunomodulators (Voccia et al 1999, Rohr et al 2008b, Rohr and McCoy 2010 and thus might have unfavorable effects on amphibian disease risk. Given the complexity of these direct and indirect effects, it is not surprising that studies exploring the effects of pesticides on Bd infections have produced mixed results (Davidson et al 2007, Buck et al 2015, Jones et al 2017.…”

Effects of Emerging Infectious Diseases on Amphibians: A Review of Experimental Studies

“…Rohr et al [173] found that early-life exposure to atrazine decreased survival post-metamorphosis when combined with Bd in Osteopilus septentrionalis. Likewise, Buck et al [163] demonstrated that exposure to pesticides in tadpoles resulted in higher Bd loads and increased mortality in post-metamorphic individuals from three species, but not for two other species. A possible reason for findings with little or no interactive effects may be that certain compounds can inhibit or diminish the growth or integrity of Bd, as was demonstrated outside of the host species [162,167,170].…”

“…Some studies examining this interaction investigate if pesticides and contaminants play a role in decreasing amphibian immune response, rendering amphibians more susceptible to infectious disease [159][160][161]. However, few experimental studies support this hypothesis [118,[162][163][164][165][166][167][168][169][170][171][172]. Rohr et al [173] found that early-life exposure to atrazine decreased survival post-metamorphosis when combined with Bd in Osteopilus septentrionalis.…”