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: 5.33). 03/2007; 41(5):1771-6. DOI: 10.1021/es0611947
Source: PubMed


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 agricultural landscapes encroach on amphibian habitats , interactions likely occur between environmental pressures such as disease and contamination. While research has focused on Bd host-pathogen interactions in tadpoles and adult frogs (e.g., Davidson et al. 2007; Responsible editor: Cinta Porte "
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    ABSTRACT: Background/Question/Methods Chytridiomycosis, an emerging infectious amphibian disease caused by the pathogenic fungus Batrachochytrium dendrobatidis (Bd), has played a major roll in amphibian declines. Studies have also shown that widespread pesticide use contributes to declines in amphibian health. These causes are not mutually exclusive; thus, studies must examine the effects of multiple concurrent perturbations on amphibian declines. We conducted a field study to determine the effects of the fungicide thiophanate-methyl (TM) and Bd on Southern Leopard frog (Lithobates sphenocephalus) tadpoles and aquatic ecosystems. We exposed tadpoles to Bd in the lab and then placed them in aquatic mesocosms, which were then exposed to TM (at three environmentally relevant concentrations) on a weekly basis. Aquatic community measures were recorded weekly. Frogs were collected upon metamorphosis and life history traits were measured. Based on previous studies, we predicted that Bd and TM would act in opposition to directly affect amphibian health, while TM would alter aquatic community composition, possibly negating the direct effects of either pressure on the amphibians. Results/Conclusions Counter to our predictions, Bd mitigated the effects of TM by “protecting” tadpoles from TM-induced mortality, and both Bd and TM altered aquatic community composition. However, we conclude that alterations to the measured aquatic community variables were not the cause of tadpole mortality, as has been recorded in previous studies. TM also interacted with Bd to affect the size of new metamorphs. Bd-unexposed tadpoles that were exposed to the low and high levels of TM metamorphosed larger than those exposed to the mid level of TM, results that were not observed in Bd-exposed individuals. Moreover, TM altered aquatic community composition, resulting in trophic cascades and dramatic aquatic community alterations. This research illustrates that interactions between multiple perturbations such as pesticides and disease impact amphibian health and aquatic community composition and further research is necessary to elucidate such effects.
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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.
    Full-text · Article · Jul 2013 · BMC Ecology
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    • "Similarly, in several cases, peaks containing as yet uncharacterized peptides are present in the chromatogram of secretions from one species that are not present in the chromatograms of secretions from either of the other species. It is worthwhile to point out that the expression pattern of the antimicrobial peptides in skin secretions of a particular frog species is not constant but can vary with season, age of the frog, and environmental influences such as exposure to microbial pathogens and pesticides (Davidson et al., 2007; Tennessen et al., 2009). The data suggest that the three species may be closely related but are not conspecific. "
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    ABSTRACT: Peptidomic analysis was used to compare the distribution of host-defense peptides in norepinephrine-stimulated skin secretions from Xenopus victorianusAhl, 1924 (also described as the subspecies X. laevis victorianus) and Xenopus laevis sudanensisPerret, 1966 with the previously determined distributions in Xenopus laevis (Daudin, 1802) and Xenopus petersii Bocage, 1895. Peptides belonging to the magainin, peptide glycine-leucine-amide (PGLa), and caerulein precursor fragment (CPF) families were purified by reversed-phase HPLC and characterized by electrospray mass spectrometry. Magainin-P2, PGLa-P1, CPF-P1, CPF-P2, and CPF-P3 previously isolated from X. petersii and structurally different from orthologous peptides from X. laevis, were identified in X. victorianus and X. laevis sudanensis skin secretions whereas the corresponding X. laevis peptides were absent. Magainin-1, identical in X. petersii and X. laevis, was also identified in the secretions. Xenopsin-precursor fragment (XPF) peptides, absent from X. petersii but present in X. laevis skin secretions, were not identified in the X. victorianus and X. laevis sudanensis secretions. The data indicate that X. victorianus and X. laevis sudanensis are more closely related to X. petersii than to X. laevis and support separate species status. The study illustrates the value of analysis of host-defense peptides in the evaluation of taxonomic and phylogenetic relationships between closely related frog species.
    Full-text · Article · Jul 2013 · Comparative Biochemistry and Physiology Part D Genomics and Proteomics
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