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Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs

Environmental Studies Program, San Francisco State University, 1600 Holloway Avenue, San Francisco CA 94132, USA.
Environmental Science and Technology (Impact Factor: 5.48). 03/2007; 41(5):1771-6. DOI: 10.1021/es0611947
Source: PubMed

ABSTRACT Environmental contaminants and disease may synergistically contribute to amphibian population declines. Sub-lethal levels of contaminants can suppress amphibian immune defenses and, thereby, may facilitate disease outbreaks. We conducted laboratory experiments on newly metamorphosed foothill yellow-legged frogs (Rana boylii) to determine whether sublethal exposure to the pesticide carbaryl would increase susceptibility to the pathogenic chytrid fungus Batrachochytrium dendrobatidis that is widely associated with amphibian declines. We examined the effect of carbaryl alone, chytrid alone, and interactions of the two on individual survival, growth, and antimicrobial skin defenses. We found no effect of chytrid, carbaryl, or their interaction on survival. However, chytrid infection reduced growth by approximately one-half. This is the first report of suppressed growth in post-metamorphic amphibians due to infection with chytrid. Rana boylii skin peptides strongly inhibited chytrid growth in vitro, which may explain why chytrid exposure did not result in significant mortality. Skin peptide defenses were significantly reduced after exposure to carbaryl suggesting that pesticides may inhibit this innate immune defense and increase susceptibility to disease.

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    • "Population declines due to fatal amphibian chytridiomycosis are selective, with some species being highly susceptible to lethal infection, whereas others either appear to be resistant or have limited mortality following infection (reviewed in Rollins-Smith 2009; Conlon 2011). Among the Amerana species group, documented resistance to fatal disease has been provided for R. boylii (Davidson et al. 2007) and R. draytonii (Padgett-Flohr 2008), whereas R. muscosa (Rachowicz and Vredenburg 2004) and R. sierrae (Briggs et al. 2010) are particularly susceptible and have suffered major population declines due to chytridiomycosis. Although once relatively widespread over an area from northeastern California to southwestern British Columbia, R. pretiosa has disappeared from most of its geographical range (Pearl and Hayes 2005) and is listed as vulnerable in the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (Hammerson and Pearl 2012). "
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    ABSTRACT: Population declines due to amphibian chytridiomycosis among selected species of ranid frogs from western North America have been severe, but there is evidence that the Oregon spotted frog, Rana pretiosa Baird and Girard, 1853, displays resistance to the disease. Norepinephrine-stimulated skin secretions were collected from a non-declining population of R. pretiosa that had been exposed to the causative agent Batrachochytrium dendrobatidis. Peptidomic analysis led to identification and isolation, in pure form, of a total of 18 host-defense peptides that were characterized structurally. Brevinin-1PRa, -1PRb, -1PRc, and -1PRd, esculentin-2PRa and -PRb, ranatuerin-2PRa, -2PRb, -2PRc, and -2PRe, temporin-PRb and -PRc were identified in an earlier study of skin secretions of frogs from a different population of R. pretiosa known to be declining. Ranatuerin-2PRf, -2PRg, -2PRh, temporin-PRd, -PRe, and -PRf were not identified in skin secretions from frogs from the declining population, whereas temporin-PRa and ranatuerin-2PRd, present in skin secretions from the declining population, were not detected in the current study. All purified peptides inhibited the growth of B. dendrobatidis zoospores. Peptides of the brevinin-1 and esculentin-2 families displayed the highest potency (minimum inhibitory concentration = 6.25-12.5 μM). The study provides support for the hypothesis that the multiplicity and diversity of the antimicrobial peptide repertoire in R. pretiosa and the high growth-inhibitory potency of certain peptides against B. dendrobatidis are important in conferring a measure of resistance to fatal chytridiomycosis.
    Journal of Chemical Ecology 05/2013; 39(6). DOI:10.1007/s10886-013-0294-z · 2.24 Impact Factor
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    • "Davidson et al.'s (2007) study differed from ours in that carbaryl was applied as a 'pulse treatment' (a single high-dose application) rather than a 'press treatment' (multiple applications of lower concentration) (Relyea & Diecks, 2008). To explain the absence of interactive effects of carbaryl and Bd, Davidson et al. (2007) hypothesised that (1) while immune function may have been reduced by carbaryl, it may not have been reduced to the extent that susceptibility to Bd increased, (2) immune function may have recovered after a one-time application of carbaryl or (3) carbaryl and Bd may have affected different aspects of immune function. Hypotheses 1 and 3 seem plausible in terms of the results of our study, but carbaryl was applied on a weekly basis in our experiment, so recovery of immune function after a carbaryl dose seems unlikely. "
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    ABSTRACT: Summary1. Anthropogenic effects have propelled us into what many have described as the sixth mass extinction, and amphibians are among the most affected groups. The causes of global amphibian population declines and extinctions are varied, complex and context-dependent and may involve multiple stressors. However, experimental studies examining multiple factors contributing to amphibian population declines are rare.2. Using outdoor mesocosms containing zooplankton, phytoplankton, periphyton and tadpoles, we conducted a 2 × 2 × 3 factorial experiment that examined the separate and combined effects of an insecticide and the fungal pathogen Batrachochytrium dendrobatidis (Bd) on three different assemblages of larval pacific treefrogs (Pseudacris regilla) and Cascades frogs (Rana cascadae).3. Larval amphibian growth and development were affected by carbaryl and the amphibian assemblage treatment, but only minimally by Bd. Carbaryl delayed metamorphosis in both amphibian species and increased the growth rate of P. regilla. Carbaryl also reduced cladoceran abundance, which, in turn, had positive effects on phytoplankton abundance but no effect on periphyton biomass. Substituting 20 intraspecific competitors with 20 interspecific competitors decreased the larval period but not the growth rate of P. regilla. In contrast, substituting 20 intraspecific competitors with 20 interspecific competitors had no effect on R. cascadae. Results of real-time quantitative polymerase chain reaction (qPCR) analysis confirmed infection of Bd-exposed animals, but exposure to Bd had no effects on either species in univariate analyses, although it had significant or nearly significant effects in several multivariate analyses. In short, we found no interactive effects among the treatments on amphibian growth and development.4. We encourage future research on the interactive effects of pesticides and pathogens on amphibian communities.
    Freshwater Biology 10/2012; 57(1):61 - 73. DOI:10.1111/j.1365-2427.2011.02695.x · 2.91 Impact Factor
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    • "The disease chytridiomycosis, caused by infection by the fungal pathogen Batrachochytrium dendrobatidis (hereafter ''Bd''), has been identified as a proximate cause of both amphibian population declines and species extinctions, but the factors underlying its recent emergence and varying virulence remain under investigation (Fisher et al., 2009). With respect to virulence, one hypothesis states that an interaction between environmental contaminants, such as pesticides, and Bd may contribute to susceptibility to infection (Carey et al., 1999; Parris and Baud, 2004; Davidson et al., 2007). The prevalence of pesticides in aquatic environments combined with observations that amphibians exhibit immune suppression and increased parasitism following pesticide exposure (e.g. "
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    ABSTRACT: Effects of exposure to contaminants such as pesticides along with exposure to pathogens have been listed as two major contributors to the global crisis of declining amphibian populations. These two factors have also been linked in explanations of the causes of these population declines. We conducted a combined exposure experiment to test the hypothesis that exposure to two agricultural herbicides would increase the susceptibility of post-metamorphic northern leopard frogs (Lithobates pipiens) to the amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd). We assessed the independent and interactive effects of these exposures on the health and survival of the frogs. Wild-caught frogs underwent a 21-day exposure to a nominal concentration of either 2.1 μg/L atrazine (Aatrex(®) Liquid 480) or 100 μg a.e./L glyphosate (Roundup(®) Original), followed by Bd, and then were observed until 94 days post-initial exposure to the herbicides. Actual levels of atrazine were between 4.28 ± 0.04 μg/L and 1.70 ± 0.26 μg/L while glyphosate degraded from 100 μg a.e./L to approximately 7 μg a.e./L within 6 days of initial exposure to the herbicides. Compared to controls, the glyphosate formulation reduced the snout-vent length of frogs during the pesticide exposure (at Day 21), and the atrazine formulation reduced gain in mass up to Day 94. No treatment affected survival, splenosomatic or hepatosomatic indices, the densities and sizes of hepatic and splenic melanomacrophage aggregates, the density and size of hepatic granulomas, proportions of circulating leucocytes, the ratio of neutrophils to lymphocytes, or the ratio of leucocytes to erythrocytes. Histological assessment of samples collected at Day 94 revealed no evidence of Bd infection in any Bd-exposed frogs, while real-time PCR detected only one case of light infection in a single atrazine- and Bd-exposed frog. Frogs exposed to Bd shed their skin significantly more frequently than Bd-unexposed frogs, which may have helped them resist or clear infection, and could explain why no interaction between the herbicides and Bd was detected. The results suggest that these frogs were resistant to Bd infection and that pre-exposure to the herbicides did not alter this resistance. The effects seen on the growth following herbicide exposure is a concern, as reduced growth can lower the reproductive success and survival of the amphibians.
    Ecotoxicology and Environmental Safety 04/2012; 80:372-80. DOI:10.1016/j.ecoenv.2012.04.006 · 2.48 Impact Factor