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Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum

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Abstract

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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Acknowledgements

We thank E. André and T. Nelms for assistance with field and lab work, J. Kastendiek and G. Wyngaard for helpful comments on the manuscript, and R. Domangue for invaluable statistical advice, including providing us with a program to calculate power of Wilcoxon tests. T. Slater gave us permission to work in the George Washington National Forest; Virginia Department of Game and Inland Fisheries permit 026187 allowed us to handle salamanders in this study. JMU’s Animal Care and Use Committee approved our protocol that involves swabbing salamanders and releasing them (06-09-01), and these experiments comply with the current laws of the state of Virginia and the United States of America in which they were performed. This study was funded by Jeffress Foundation grant J-738 and by NSF grant 0413981.

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Correspondence to Reid N. Harris.

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Communicated by Steven Kohler.

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Banning, J.L., Weddle, A.L., Wahl III, G.W. et al. Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum . Oecologia 156, 423–429 (2008). https://doi.org/10.1007/s00442-008-1002-5

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  • DOI: https://doi.org/10.1007/s00442-008-1002-5

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