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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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    • "As a consequence, in species exhibiting apparent resistance to Bd, we might also expect there to be sub-lethal costs of infection and for such costs to influence populations. In support, a number of studies in frogs and toads have reported subclinical effects of Bd on tadpole growth [25-28], as well as adult body size [29] and body condition [30]. Nevertheless, in such cases, tests of the consequences of Bd infection for traits important in reproduction (morphology, behaviour) of resistant amphibians are generally lacking. "
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    ABSTRACT: Batrachochytrium dendrobatidis (Bd), the causative agent of chytridiomycosis, is decimating amphibians worldwide. Unsurprisingly, the majority of studies have therefore concentrated on documenting morbidity and mortality of susceptible species and projecting population consequences as a consequence of this emerging infectious disease. Currently, there is a paucity of studies investigating the sub-lethal costs of Bd in apparently asymptomatic species, particularly in controlled experimental conditions. Here we report the consequences of a single dose of B. dendrobatidis zoospores on captive adult palmate newts (Lissotriton helveticus) for morphological and behavioural traits that associate with reproductive success. A single exposure to ~2000 zoospores induced a subclinical Bd infection. One week after inoculation 84% of newts tested positive for Bd, and of those, 98% had apparently lost the infection by the day 30. However, exposed newts suffered significant mass loss compared with control newts, and those experimental newts removing higher levels of Bd lost most mass. We found no evidence to suggest that three secondary sexual characteristics (areas of dorsal crest and rear foot webbing, and length of tail filament) were reduced between experimental versus control newts; in fact, rear foot webbing was 26% more expansive at the end of the experiment in exposed newts. Finally, compared with unexposed controls, exposure to Bd was associated with a 50% earlier initiation of the non-reproductive terrestrial phase. Our results suggest that Bd has measureable, but sub-lethal effects, on adult palmate newts, at least under the laboratory conditions presented. We conclude that the effects reported are most likely to be mediated through the initiation of costly immune responses and/or tissue repair mechanisms. Although we found no evidence of hastened secondary sexual trait regression, through reducing individual body condition and potentially, breeding season duration, we predict that Bd exposure might have negative impacts on populations of palmate newts through reducing individual reproductive success and adult recruitment.
    BMC Ecology 07/2013; 13(1):27. DOI:10.1186/1472-6785-13-27 · 2.36 Impact Factor
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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: 1. 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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