Behavioral Ecology and Sociobiology

, Volume 69, Issue 3, pp 407–413 | Cite as

Larval deposition behaviour and maternal investment of females reflect differential habitat adaptation in a genetically diverging salamander population

  • Barbara A. Caspers
  • Sebastian Steinfartz
  • E. Tobias Krause
Original Paper


Illuminating the ability of individuals to react to different selective forces caused by environmental differences is crucial to understand population divergence and speciation in the context of habitat adaptation. In a common environment experiment performed under standardised laboratory conditions, we examined whether female fire salamanders (Salamandra salamandra) originating from a recently adaptively diverged population displayed behavioural phenotype differences related to larval deposition behaviour. Females of this species typically deposit their larvae in small first-order streams; however, in our study population, females also use temporary ponds. These two habitat types display major ecological differences that strongly influence larval growth and survival. We observed that females differed in larval deposition behaviour and maternal investment. Pond-type females extended larval deposition over an increased time period and tended to exhibit more deposition events compared with stream-type females. Over successive deposition events, the body condition of larvae deposited by stream-type females decreased faster than that of larvae deposited by pond-type females. These differences in larval deposition behaviour may represent a bet-hedging strategy, given that ponds are more constrained in terms of desiccation and food availability than streams. The lengthened deposition period enabled pond-type females to deposit larger larvae towards the end of the deposition period, compared with stream-type females. Although the studied population only diverged recently, we observed significant behavioural differences between differentially adapted females, demonstrating the importance of behavioural differences in habitat adaptation in the context of speciation processes.


Habitat adaptation Behavioural differences Larval deposition Natural selection Fire salamander Speciation 



We thank Timm Reinhardt, Ralf Hendrix, Terry Morley and Annika Keller for field assistance and Fritz Trillmich for providing logistical support. We are very grateful to two anonymous referees and the editor for constructive comments. We thank Tobias Roth for statistical advice. This research was supported by a research grant from the Deutsche Forschungsgemeinschaft (DFG) to BAC (CA 889/1) and partially supported by the Wilhelm-Peters Fund of the DGHT to ETK, BAC and SS.

Ethical standards

With the permission of the ‘Untere Landschaftsbehörde’ in Bonn, we collected potentially pregnant female fire salamanders (Salamandra salamandra) in the Kottenforst near Bonn, Germany (N 50°41.321′; E 007°07.012′) and brought them to the Department of Animal Behaviour at Bielefeld University, Germany. Experiments comply with the current laws of Germany. After the experiment, the females and larvae were released at the site of capture and the nearest water body, respectively.

Supplementary material

265_2014_1853_MOESM1_ESM.docx (15 kb)
ESM 1 (DOCX 14 kb)


  1. Alcobendas M, Buckley D, Tejedo M (2004) Variability in survival, growth and metamorphosis in the larval fire salamander (Salamandra salamandra): effects of larval birth size, sibship and environment. Herpetologica 60:232–245CrossRefGoogle Scholar
  2. Alford RA, Wilbur HM (1985) Priority effects in experimental pond communities: competition between Bufo and Rana. Ecology 66: 1097–1105Google Scholar
  3. Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882PubMedCrossRefGoogle Scholar
  4. Boag PT, Grant PR (1981) Intense natural-selection in a population of Darwin finches (Geospizinae) in the Galapagos. Science 214:82–85PubMedCrossRefGoogle Scholar
  5. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225PubMedCrossRefGoogle Scholar
  6. Caspers BA, Junge C, Weitere M, Steinfartz S (2009) Habitat adaptation rather than genetic distance correlates with female preference in fire salamanders (Salamandra salamandra). Front Zool 6:13PubMedCentralPubMedCrossRefGoogle Scholar
  7. Caspers BA, Krause ET, Hendrix R, Kopp M, Rupp O, Rosentreter K, Steinfartz S (2014) The more the better—polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra). Mol Ecol 23:239–250PubMedCrossRefGoogle Scholar
  8. Crawley MJ (2013) The R book, 2nd edn. Wiley, New YorkGoogle Scholar
  9. Crump ML (1983) Opportunistic cannibalism by amphibian larvae in temporary aquatic environments. Am Nat 121:281–289Google Scholar
  10. Degani G, Goldenberg S, Warburg MR (1980) Cannibalistic phenomena in Salamandra salamandra larvae in certain water bodies and under experimental conditions. Hydrobiologia 75:123–128Google Scholar
  11. Eitam A, Blaustein L, Mangel M (2005) Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146:36–42Google Scholar
  12. Grant PR, Grant BR (2011) How and why species multiply: the radiation of Darwin’s finches. Princeton University Press, PrincetonGoogle Scholar
  13. Hanski I, Erälahti C, Kankare M, Ovaskainen O, Sirén H (2004) Variation in migration propensity among individuals maintained by landscape structure. Ecol Lett 7:958–966CrossRefGoogle Scholar
  14. Hendrix R, Hauswaldt JS, Veith M, Steinfartz S (2010) Strong correlation between cross-amplification success and genetic distance across all members of ‘True salamander’(Amphibia: Salamandridae) revealed by Salamandra salamandra-specific microsatellite loci. Mol Ecol Resour 10:1038–1047PubMedCrossRefGoogle Scholar
  15. Hoffman EA, Pfennig DW (1999) Proximate causes of cannibalistic polyphenism in larval tiger salamanders. Ecology 80:1076–1080Google Scholar
  16. Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485PubMedCrossRefGoogle Scholar
  17. Hopey ME, Petranka JW (1994) Restriction of wood frogs to fish-free habitats: how important is adult choice? Copeia 1994:1023–1025CrossRefGoogle Scholar
  18. Kleindorfer S, Chapman TW, Winkler H, Sulloway FJ (2006) Adaptive divergence in contiguous populations of Darwin’s small ground finch (Geospiza fuliginosa). Evol Ecol Res 8:357–372Google Scholar
  19. Kokko H, López-Sepulcre A (2006) From individual dispersal to species ranges: perspectives for a changing world. Science 313:789–791PubMedCrossRefGoogle Scholar
  20. Kraus F, Petranka JW (1989) A new sibling species of Ambystoma from the Ohio River drainage. Copeia 1989:94–110CrossRefGoogle Scholar
  21. Krause ET, Caspers BA (2015) The influence of a water current on the larval deposition pattern of females of a diverging fire salamander population (Salamandra salamandra). Salamandra (in press)Google Scholar
  22. Krause ET, Steinfartz S, Caspers BA (2011) Poor nutritional conditions during the early larval stage reduce risk‐taking activities of fire salamander larvae (Salamandra salamandra). Ethology 117:416–421CrossRefGoogle Scholar
  23. Lawler SP, Morin PJ (1993) Temporal overlap, competition, and priority effects in larval anurans. Ecology 74:174–182Google Scholar
  24. Lips KR (2001) Reproductive trade-offs and bet-hedging in Hyla calypsa, a Neotropical treefrog. Oecologia 128:509–518CrossRefGoogle Scholar
  25. Manenti R, Ficetola GF, De Bernardi F (2009) Water, stream morphology and landscape: complex habitat determinants for the fire salamander Salamandra salamandra. Amphibia-Reptilia 30:7–15CrossRefGoogle Scholar
  26. Marchetti K (1993) Dark habitats and bright bird illustrate the role of the environment in species divergence. Nature 362:149–152CrossRefGoogle Scholar
  27. McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17:480–488CrossRefGoogle Scholar
  28. Nagel L, Schluter D (1998) Body size, natural selection, and speciation in sticklebacks. Evolution 52:209–218CrossRefGoogle Scholar
  29. Nyman S, Wilkinson RF, Hutcherson JE (1993) Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma annulatum). J Herpetol 27:78–84Google Scholar
  30. Ogden R, Thorpe RS (2002) Molecular evidence for ecological speciation in tropical habitats. Proc Natl Acad Sci U S A 99:13612–13615PubMedCentralPubMedCrossRefGoogle Scholar
  31. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42PubMedCrossRefGoogle Scholar
  32. Petranka JW, Sih A (1987) Habitat duration, length of larval period, and the evolution of a complex life cycle of a salamander, Ambystoma texanum. Evolution 41:1347–1356CrossRefGoogle Scholar
  33. Price T (1991) Morphology and ecology of breeding warblers along an altitudinal gradient in Kashmir, India. J Anim Ecol 60:643–664CrossRefGoogle Scholar
  34. Primmer CR, Koskinen MT, Piironen J (2000) The one that did not get away: individual assignment using microsatellite data detects a case of fishing competition fraud. Proc R Soc Lond B 267:1699–1704CrossRefGoogle Scholar
  35. Quinn GGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  36. Reinhardt T (2014) New home, new life: the effect of shifts in the habitat choice of salamander larvae on population performance and their effect on pond invertebrate communities. Dissertation, Technische Universität-Dresden, GermanyGoogle Scholar
  37. Reinhardt T, Steinfartz S, Paetzold A, Weitere M (2013) Linking the evolution of habitat choice to ecosystem functioning: direct and indirect effects of pond-reproducing fire salamanders on aquatic-terrestrial subsidies. Oecologia 173:281–291PubMedCrossRefGoogle Scholar
  38. Rice WR (1987) Speciation via habitat specialization: the evolution of reproductive isolation as a correlated character. Evol Ecol 1:301–314CrossRefGoogle Scholar
  39. Rivera G (2008) Ecomorphological variation in shell shape of the freshwater turtle Pseudemys concinna inhabiting different aquatic flow regimes. Integr Comp Biol 48:769–787PubMedCrossRefGoogle Scholar
  40. Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427CrossRefGoogle Scholar
  41. Ryan PG, Bloomer P, Moloney CL, Grant TJ, Delport W (2007) Ecological speciation in South Atlantic island finches. Science 315:1420–1423PubMedCrossRefGoogle Scholar
  42. Sadeh A, Mangel M, Blaustein L (2009) Context-dependent reproductive habitat selection: the interactive roles of structural complexity and cannibalistic conspecifics. Ecol Lett 12:1158–1164PubMedCrossRefGoogle Scholar
  43. Schmidt BR, Feldmann R, Schaub M (2007) Demographic processes underlying population growth and decline in Salamandra salamandra. Conserv Biol 19:1149–1156CrossRefGoogle Scholar
  44. Schulte U, Kusters D, Steinfartz S (2007) A PIT tag based analysis of annual movement patterns of adult fire salamanders (Salamandra salamandra) in a Middle European habitat. Amphibia-Reptilia 28:531–536CrossRefGoogle Scholar
  45. Schulte LM, Yeager J, Schulte R, Veith M, Werner P, Beck LA, Lötters S (2011) The smell of success: choice of larval rearing sites by means of chemical cues in a Peruvian poison frog. Anim Behav 81:1147–1154CrossRefGoogle Scholar
  46. Segev O, Mangel M, Wolf N, Sadeh A, Kershenbaum A, Blaustein L (2011) Spatiotemporal reproductive strategies in the fire salamander: a model and empirical test. Behav Ecol 22:670–678CrossRefGoogle Scholar
  47. Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192CrossRefGoogle Scholar
  48. Steinfartz S, Küsters D, Tautz D (2004) Isolation of polymorphic tetranucleotide microsatellite loci in the Fire salamander Salamandra salamandra (Amphibia: Caudata). Mol Ecol Notes 4:626–628CrossRefGoogle Scholar
  49. Steinfartz S, Weitere M, Tautz D (2007) Tracing the first step to speciation—ecological and genetic differentiation of a salamander population in a small forest. Mol Ecol 16:4550–4561PubMedCrossRefGoogle Scholar
  50. Thiesmeier B (2004) Der Feuersalamander. Laurenti Verlag, GermanyGoogle Scholar
  51. Touchon JC, Warkentin KM (2008) Reproductive mode plasticity: aquatic and terrestrial oviposition in a treefrog. Proc Natl Acad Sci U S A 105:7495–7499PubMedCentralPubMedCrossRefGoogle Scholar
  52. Walls SC (1998) Density dependence in a larval salamander: the effects of interference and food limitation. Copeia 4:926–935Google Scholar
  53. Weitere M, Tautz D, Neumann D, Steinfartz S (2004) Adaptive divergence vs. environmental plasticity: tracing local genetic adaptation of metamorphosis traits in salamanders. Mol Ecol 13:1665–1677PubMedCrossRefGoogle Scholar
  54. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  55. Wolf JBW, Harrod C, Brunner S, Salazar S, Trillmich F, Tautz D (2008) Tracing early stages of species differentiation: ecological, morphological and genetic divergence of Galápagos sea lion populations. BMC Evol Biol 8:150PubMedCentralPubMedCrossRefGoogle Scholar
  56. Ziemba RE, Myers MT, Collins JP (2000) Foraging under the risk of cannibalism leads to divergence in body size among tiger salamander larvae. Oecologia 124:225–231CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Barbara A. Caspers
    • 1
  • Sebastian Steinfartz
    • 2
  • E. Tobias Krause
    • 1
    • 3
  1. 1.Department of Animal BehaviourBielefeld UniversityBielefeldGermany
  2. 2.Zoological Institute, Department of Evolutionary Biology, Unit Molecular EcologyTechnische Universität BraunschweigBraunschweigGermany
  3. 3.Behavioural Ecology Group, Department of Animal SciencesWageningen UniversityWageningenThe Netherlands

Personalised recommendations