, Volume 156, Issue 2, pp 423–429 | Cite as

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

  • Jenifer L. Banning
  • Anna L. Weddle
  • George W. Wahl III
  • Mary Alice Simon
  • Antje Lauer
  • Robert L. Walters
  • Reid N. Harris
Community Ecology - Original Paper


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.


Disease resistance Fungal pathogen Group living Mutualism Parental care 


  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  2. Austin RM Jr (1997) The cutaneous bacterial flora of the eastern zigzag salamander, Plethodon dorsalis (Amphibia: Plethodontidae). PhD dissertation, University of MississippiGoogle Scholar
  3. Austin RM Jr (2000) Cutaneous microbial flora and antibiosis in Plethodon ventralis. In: Bruce RC, Jaeger RG, Houck LD (eds) The biology of plethodontid salamanders. Kluwer, Plenum, New York, pp 451–462Google Scholar
  4. Bilde T, Coates KS, Birkhofer K, Bird T, Maklakov AA, Lubin Y, Aviles L (2007) Survival benefits select for group living in a social spider despite reproductive costs. J Evol Biol 20:2412–2426PubMedCrossRefGoogle Scholar
  5. Blanchard FN (1934) The relation of the female four-toed salamander to her nest. Copeia 1934:137–138CrossRefGoogle Scholar
  6. Brown CR, Brown MB (1996) Ectoparasitism. In: Coloniality in the cliff swallow: the effect of group size on social behavior. University of Chicago Press, Chicago, pp 68–117Google Scholar
  7. Côté IM, Gross MR (1993) Reduced disease in offspring: a benefit of coloniality in sunfish. Behav Ecol Sociobiol 33:269–274CrossRefGoogle Scholar
  8. Culp CE, Falkinham JO, Belden LK (2007) Identification of the natural bacterial microflora on the skin of eastern newts, bullfrog tadpoles and redback salamanders. Herpetologica 63:66–71CrossRefGoogle Scholar
  9. Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ant. Science 311:81–83PubMedCrossRefGoogle Scholar
  10. Duellman WE, Trueb L (1986) Biology of amphibians. McGraw–Hill, New YorkGoogle Scholar
  11. Eggert AK, Müller JK (1992) Joint breeding in female burying beetles. Behav Ecol Sociobiol 31:237–242CrossRefGoogle Scholar
  12. Farrelly V, Rainey FA, Stackebrandt E (1995) Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl Environ Microbiol 61:2798–2801PubMedGoogle Scholar
  13. Forester DC (1979) The adaptiveness of parental care in Desmognathus ochrophaeus (Urodela: Plethodontidae). Copeia 1979:332–341CrossRefGoogle Scholar
  14. Green AJ (1999) Implications of pathogenic fungi for life-history evolution in amphibians. Funct Ecol 13:573–575CrossRefGoogle Scholar
  15. Harris RN (2005) Hemidactylium scutatum. In: Lannoo M (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 780–781Google Scholar
  16. Harris RN (2008) Body condition and order of arrival affect cooperative nesting behaviour in four-toed salamanders Hemidactylium scutatum. Anim Behav 75:229–233 CrossRefGoogle Scholar
  17. Harris RN, Gill DE (1980) Communal nesting, brooding behavior, and embryonic survival of the four-toed salamander, Hemidactylium scutatum. Herpetologica 36:141–144Google Scholar
  18. Harris RN, Hames WW, Knight IT, Carreño CA, Vess TJ (1995) An experimental analysis of joint nesting in the salamander Hemidactylium scutatum (Caudata: Plethodontidae): the effects of population density. Anim Behav 50:1309–1316CrossRefGoogle Scholar
  19. Harris RN, James TY, Lauer A, Simon MA, Patel A (2006) Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3:53–56CrossRefGoogle Scholar
  20. Hess ZJ, Harris RN (2000) Eggs of Hemidactylium scutatum (Caudata: Plethodontidae) are unpalatable to insect predators. Copeia 2000:597–600CrossRefGoogle Scholar
  21. Hughes WOH, Eilenberg J, Boomsma JJ (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc Lond B Biol Sci 269:1811–1819CrossRefGoogle Scholar
  22. Jockusch EL, Mahoney MJ (1997) Communal oviposition and lack of parental care in Batrachoseps nigriventris (Caudata: Plethodontidae) with a discussion of the evolution of breeding behavior in plethodontid salamanders. Copeia 1997:697–705CrossRefGoogle Scholar
  23. Kéry M, Hatfield JS (2003) Normality of raw data in general linear models: the most widespread myth in statistics. Bull Ecol Soc Am 84:92–94CrossRefGoogle Scholar
  24. Koenig WD, Mumme RL (1987) Population ecology of the cooperatively breeding acorn woodpecker. Princeton University Press, PrincetonGoogle Scholar
  25. Koford LL, Bowen BS, Vehrencamp SL (1990) Groove-billed anis: joint nesting in a tropical cuckoo. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds. Cambridge University Press, Cambridge, pp 335–355Google Scholar
  26. Lauer A, Simon MA, Banning JL, André E, Duncan K, Harris RN (2007) Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007:630–640CrossRefGoogle Scholar
  27. Lauer A, Simon MA, Banning JL, Lam BA, Harris RN (2008) Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. ISME J 2:145–157PubMedCrossRefGoogle Scholar
  28. Rosengaus RB, Maxmen AB, Coates LE, Traniello JFA (1998) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav Ecol Sociobiol 44:125–134CrossRefGoogle Scholar
  29. Smith P, Davey S (1993) Evidence for the competitive exclusion of Aeromonas salmonicida from fish with stress-inducible furunculosis by a fluorescent pseudomonad. J Fish Dis 16:521–524CrossRefGoogle Scholar
  30. Tallamy DW (1985) “Egg-dumping” in lace bug (Gargaphia solani, Hemiptera: Tingidae). Behav Ecol Sociobiol 17:357–362CrossRefGoogle Scholar
  31. Traniello JFA, Rosengaus RB, Savoie K (2002) The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc Natl Acad Sci USA 99(10):6838–6842Google Scholar
  32. Villa J (1979) Two fungi lethal to frog eggs in Central America. Copeia 1979:650–655CrossRefGoogle Scholar
  33. Wahl GW III, Harris RN, Nelms T (2008) Nest site selection and embryonic survival in four-toed salamanders, Hemidactylium scutatum (Caudata:Plethodontidae). Herpetologica 64:12–19CrossRefGoogle Scholar
  34. Warkentin KM, Currie CR, Rehner SA (2001) Egg-killing fungus induces early hatching of red-eyed treefrog eggs. Ecology 82:2860–2869CrossRefGoogle Scholar
  35. Woodhams DC, Rollins-Smith LA, Alford RA, Simon MA, Harris RN (2007) Response - Innate immune defenses of amphibian skin: antimicrobial peptides and more. Anim Conserv 10:425–428CrossRefGoogle Scholar
  36. Zehnder LD (2002) Maternal care in four-toed salamander joint nests: how prevalent is alloparental care? B.S. honors project thesis, James Madison UniversityGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Jenifer L. Banning
    • 1
  • Anna L. Weddle
    • 1
  • George W. Wahl III
    • 1
  • Mary Alice Simon
    • 1
  • Antje Lauer
    • 1
    • 2
  • Robert L. Walters
    • 1
  • Reid N. Harris
    • 1
  1. 1.Department of BiologyJames Madison UniversityHarrisonburgUSA
  2. 2.Department of BiologyCalifornia State University BakersfieldBakersfieldUSA

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