Banning JL, Weddle AL, Wahl GW, Simon MA, Lauer A, Walters RL et al.. Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum. Oecologia 156: 423-429

California State University Bakersfield Department of Biology 9001 Stockdale Highway Bakersfield CA 93311-1099 USA
Oecologia (Impact Factor: 3.09). 05/2008; 156(2):423-429. DOI: 10.1007/s00442-008-1002-5


We examined a novel hypothesis for the maintenance of communal nesting in the salamander, Hemidactylium scutatum, namely that communal nests are more likely than solitary nests to be associated with cutaneous antifungal bacteria, which
can inhibit fungal infections of embryos. A communal nest contains eggs of two or more females of the same species. The nesting
behavior of H. scutatum females and survival of embryos were determined by frequent nest surveys at three ponds. For communal nests, embryonic survival
tended to be higher and catastrophic nest failure was lower. Pure bacterial cultures of resident species were obtained from
the salamanders’ skins by swabbing and tested against a fungal pathogen of embryos (Mariannaea sp.) in laboratory assays. We found that 27% of females had skin bacteria inhibitory to Mariannaea sp. Communal nests were more likely to have at least one female with antifungal bacteria than were solitary nests. Using
a culture-independent assay (denaturing gradient gel electrophoresis of 16S rRNA gene fragments), we found that bacterial
species on females and embryos were more similar to each other than they were to bacterial species found in soil within the
nest, suggesting that females transmitted skin bacteria to embryos. The presence of anti-Mariannaea skin bacteria identified from the laboratory assays did not prevent fungal presence in field nests. However, once a nest
was visibly infected with fungi, presence of anti-Mariannaea bacteria was positively correlated with survival of embryos. Microbe transmission is usually thought to be a cost of group
living, but communal nesting in H. scutatum may facilitate the transmission of antifungal bacteria to embryos.

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    • "The potential for using symbiotic bacteria for probiotic treatments against chytridiomycosis is currently being investigated (reviewed by Bletz et al., 2013), and on-going research has identified symbiotic bacteria that inhibit the growth of the chytridiomycosis fungus, Batrachochytrium dendrobatidis, from a number of amphibian species (e.g. Harris et al., 2006; Culp et al., 2007; Lauer et al., 2007; Banning et al., 2008; Brucker et al., 2008; Flechas et al., 2012; Loudon et al., 2013; Roth et al., 2013). "
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    ABSTRACT: Amphibians possess innate immune defences, including antimicrobial peptides and symbiotic bacterial communities, that can protect them from infectious diseases, including chytridiomycosis. On-going research is attempting to use amphibian symbiotic bacteria to develop probiotic treatments that can protect hosts from the causative agent of chytridiomycosis, the fungal pathogen Batrachochytrium dendrobatidis. Events that cause disruption of symbiotic bacterial communities or deplete peptide stores could increase the susceptibility of individuals to disease and may have implications for amphibians involved in probiotic trials or time course studies that investigate symbiotic bacterial communities. It has previously been shown that passive integrated transponder tagging of frogs causes a rapid (within 24 h) and major proliferation of micro-organisms on the skin. Here, we show that marking of red-eyed tree frogs (Agalychnis callidryas) with visible elastomer has no effect on adrenal response (represented by faecal glucocorticoid metabolite concentrations) or peptide production, although there was evidence of a slightly greater microbial abundance associated with the skin of marked frogs 2 weeks after tagging. The results indicate that visible elastomer may be a preferable marking technique to passive integrated transponder tagging, particularly in the context of probiotic trials or time course studies that investigate symbiotic bacterial communities. More work is required to determine the effects of different marking techniques on physiological responses of amphibians, whether these physiological responses are consistent across host species and whether such ‘non-invasive’ marking methods affect the susceptibility of amphibians to infectious pathogens, such as B. dendrobatidis.
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    ABSTRACT: Host-microbe symbioses rely on the successful transmission or acquisition of symbionts in each new generation. Amphibians host a diverse cutaneous microbiota, and many of these symbionts appear to be mutualistic and may limit infection by the chytrid fungus, Batrachochytrium dendrobatidis, which has caused global amphibian population declines and extinctions in recent decades. Using bar-coded 454 pyrosequencing of the 16S rRNA gene, we addressed the question of symbiont transmission by examining variation in amphibian skin microbiota across species and sites and in direct relation to environmental microbes. Although acquisition of environmental microbes occurs in some host-symbiont systems, this has not been extensively examined in free-living vertebrate-microbe symbioses. Juvenile bullfrogs (Rana catesbeiana), adult red-spotted newts (Notophthalmus viridescens), pond water and pond substrate were sampled at a single pond to examine host-specificity and potential environmental transmission of microbiota. To assess population level variation in skin microbiota, adult newts from two additional sites were also sampled. Cohabiting bullfrogs and newts had distinct microbial communities, as did newts across the three sites. The microbial communities of amphibians and the environment were distinct; there was very little overlap in the amphibians' core microbes and the most abundant environmental microbes, and the relative abundances of OTUs that were shared by amphibians and the environment were inversely related. These results suggest that, in a host species-specific manner, amphibian skin may select for microbes that are generally in low abundance in the environment.
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    • "Given the current lack of knowledge about amphibian resistance to emerging diseases, it may be important to consider the diversity and stability of the symbiotic skin bacterial community when reintroducing captive amphibians to the wild. Amphibians gain bacteria through interaction with conspecifics and via transmission from the environment – both of which are controlled by husbandry protocols in captivity [18], [21]–[23]. Captive husbandry may also affect symbiotic bacteria by altering the abiotic environment to which the amphibian and the bacteria are exposed, including temperature, humidity and ultraviolet radiation levels. It has previously been shown that captive diet (carotenoid-enriched and carotenoid-free diets) has a significant effect on the bacterial communities of red-eyed tree frogs (Agalychnis callidryas), and therefore other facets of captive husbandry may do so too [24]. "
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