Skip to main content
Log in

Drought survival and reproduction impose contrasting selection pressures on maximum body size and sexual size dimorphism in a snake, Seminatrix pygaea

  • Population ecology - Original paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The causes and consequences of body size and sexual size dimorphism (SSD) have been central questions in evolutionary ecology. Two, often opposing selective forces are suspected to act on body size in animals: survival selection and reproductive (fecundity and sexual) selection. We have recently identified a system where a small aquatic snake species (Seminatrix pygaea) is capable of surviving severe droughts by aestivating within dried, isolated wetlands. We tested the hypothesis that the lack of aquatic prey during severe droughts would impose significant survivorship pressures on S. pygaea, and that the largest individuals, particularly females, would be most adversely affected by resource limitation. Our findings suggest that both sexes experience selection against large body size during severe drought when prey resources are limited, as nearly all S. pygaea are absent from the largest size classes and maximum body size and SSD are dramatically reduced following drought. Conversely, strong positive correlations between maternal body size and reproductive success in S. pygaea suggest that females experience fecundity selection for large size during non-drought years. Collectively, our study emphasizes the dynamic interplay between selection pressures that act on body size and supports theoretical predictions about the relationship between body size and survivorship in ectotherms under conditions of resource limitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arak A (1988) Sexual dimorphism in body size: a model and a test. Evolution 42:820–825

    Article  Google Scholar 

  • Beaupre SJ (2002) Modeling time-energy allocation in vipers: individual responses to environmental variation and implications for populations. In: Schuett GW, Höggren M, Douglas ME, Greene HW (eds) Biology of the vipers. Eagle Mountain Publishing, Eagle Mountain, pp 463–481

    Google Scholar 

  • Beaupre SJ, Duvall D (1998) Variation in oxygen consumption of the western diamondback rattlesnake (Crotalus atrox): implications for sexual size dimorphism. J Comp Physiol B 168:497–506

    Article  Google Scholar 

  • Bennett AF (1982) The energetics of reptilian activity. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 12. Academic Press, New York, pp 155–199

    Google Scholar 

  • Bennett AF, Dawson WR (1976) Metabolism. In: Gans C (ed) Biology of the reptilia. Physiology A, vol 5. Academic Press, London, pp 127–223

    Google Scholar 

  • Blouin-Demers G, Prior KA, Weatherhead PJ (2002) Comparative demography of black rat snakes (Elaphe obsoleta) in Ontario and Maryland. J Zool 256:1–10

    Google Scholar 

  • Boback SM (2003) Body size evolution in snakes: evidence from island populations. Copeia 2003:81–94

    Article  Google Scholar 

  • Bonnet X, Naulleau G, Shine R, Lourdais O (2000) Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis. Oikos 89:509–518

    Article  Google Scholar 

  • Brown GP, Weatherhead PJ (1997) Effects of reproduction on survival and growth of female northern water snake, Nerodia sipedon. Can J Zool 75:424–432

    Article  Google Scholar 

  • Case TJ (1978) General explanation for insular body size trends in terrestrial vertebrates. Ecology 59:1–18

    Article  Google Scholar 

  • Clutton-Brock TH, Harvey PH, Rudder B (1977) Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269:797–800

    Article  CAS  PubMed  Google Scholar 

  • Cox RM, Butler MA, John-Alder HB (2007) The evolution of sexual size dimorphism in reptiles. In: Fairbairn DJ, Blanckenhorn WU, Szekely T (eds) Sex, size & gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford, pp 38–49

    Google Scholar 

  • Darwin C (1871) The decent of man and selection in relation to sex. Murray, London

    Google Scholar 

  • Dodd CK Jr (1993) Population structure, body mass, activity, and orientation of an aquatic snake (Seminatrix pygaea) during a drought. Can J Zool 71:1281–1288

    Article  Google Scholar 

  • Forsman A (1991) Variation in sexual size dimorphism and maximum body size among adder populations: effects of prey size. J Anim Ecol 60:253–267

    Article  Google Scholar 

  • Forsman A (1996) Body size and net energy gain in gape-limited predators: a model. J Herpetol 30:307–319

    Article  Google Scholar 

  • Gibbons JW, Dorcas ME (2004) North American watersnakes: a natural history. University of Oklahoma Press, Norman

    Google Scholar 

  • Gibbons JW, Semlitsch RD (1991) Guide to the reptiles and amphibians of the Savannah River Site. University of Georgia Press, Athens, GA

  • Gibbons JW, Winne CT, Scott DE, Willson JD, Glaudas X, Andrews KM, Todd BD, Fedewa LA, Wilkinson L, Tsaliagos RN, Harper SJ, Greene JL, Tuberville TD, Metts BS, Dorcas ME, Nestor JP, Young CA, Akre T, Reed RN, Buhlmann KA, Norman J, Croshaw DA, Hagen C, Rothermel BB (2006) Remarkable amphibian biomass and abundance in an isolated wetland: implications for wetland conservation. Conserv Biol 20:1457–1465

    Article  PubMed  Google Scholar 

  • Hedrick AV, Temeles EJ (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol 4:136–138

    Article  Google Scholar 

  • Jessop TS, Madsen T, Sumner J, Rudiharto H, Phillips JA, Ciofi C (2006) Maximum body size among insular Komodo dragon populations covaries with large prey density. Oikos 112:422–429

    Article  Google Scholar 

  • Keogh JS, Scott IAW, Hayes C (2005) Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes. Evolution 59:226–233

    PubMed  Google Scholar 

  • King RB, Bittner TD, Queral-Regil A, Cline JH (1999) Sexual dimorphism in neonate and adult snakes. J Zool 247:19–28

    Article  Google Scholar 

  • Kissner KJ, Weatherhead PJ (2005) Phenotypic effects on survival of neonatal northern watersnakes Nerodia sipedon. J Anim Ecol 74:259–265

    Article  Google Scholar 

  • Kissner KJ, Weatherhead PJ, Gibbs HL (2005) Experimental assessment of ecological and phenotypic factors affecting male mating success and polyandry in northern watersnakes, Nerodia sipedon. Behav Ecol Sociobiol 59:207–214

    Article  Google Scholar 

  • Luiselli L (2005) Snakes don’t shrink, but ‘shrinkage’ is an almost inevitable outcome of measurement error by the experimenters. Oikos 110:199–202

    Article  Google Scholar 

  • Luiselli L, Capula M, Shine R (1996) Reproductive output, costs of reproduction, and ecology of the smooth snake, Coronella austriaca, in the eastern Italian Alps. Oecologia 106:100–110

    Google Scholar 

  • Madsen T, Shine R (1993a) Costs of reproduction in a population of European adders. Oecologia 94:488–495

    Article  Google Scholar 

  • Madsen T, Shine R (1993b) Male mating success and body size in European grass snakes. Copeia 1993:561–564

    Article  Google Scholar 

  • Madsen T, Shine R (1993c) Phenotypic plasticity in body sizes and sexual size dimorphism in European grass snakes. Evolution 47:321–325

    Article  Google Scholar 

  • Madsen T, Shine R (1994) Costs of reproduction influence the evolution of sexual size dimorphism in snakes. Evolution 48:1389–1397

    Article  Google Scholar 

  • Madsen T, Shine R (2000a) Energy versus risk: costs of reproduction in free-ranging pythons in tropical Australia. Austral Ecol 25:670–675

    Google Scholar 

  • Madsen T, Shine R (2000b) Silver spoons and snake body sizes: prey availability early in life influences long-term growth rates of free-ranging pythons. J Anim Ecol 69:952–958

    Article  Google Scholar 

  • Madsen T, Shine R (2001) Do snakes shrink? Oikos 92:187–188

    Article  Google Scholar 

  • Madsen T, Shine R (2002) Short and chubby or long and slim? Food intake, growth and body condition in free-ranging pythons. Austral Ecol 27:672–680

    Article  Google Scholar 

  • Madsen T, Stille B (1988) The effect of size dependent mortality on colour morphs in male adders, Vipera berus. Oikos 52:73–78

    Article  Google Scholar 

  • McNab BK (1971) On the ecological significance of Bergmann’s rule. Ecology 52:845–854

    Article  Google Scholar 

  • McNab BK (1999) On the comparative ecological and evolutionary significance of total and mass-specific rates of metabolism. Physiol Biochem Zool 72:642–644

    Article  CAS  PubMed  Google Scholar 

  • Moen DS, Winne CT, Reed RN (2005) Habitat-mediated shifts and plasticity in the evaporative water loss rates of two congeneric pit vipers (Squamata, Viperidae, Agkistrodon). Evol Ecol Res 7:759–766

    Google Scholar 

  • Parker WS, Plummer MV (1987) Population ecology. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. Blackburn Press, Caldwell, pp 253–301

    Google Scholar 

  • Pearson D, Shine R, Williams A (2002) Geographic variation in sexual size dimorphism within a single species (Morelia spilota, Pythonidae). Oecologia 131:418–426

    Article  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

    Google Scholar 

  • Preziosi RF, Fairbairn DJ (1997) Sexual size dimorphism and selection in the wild in the waterstrider Aquarius remigis: lifetime fecundity selection on female total length and its components. Evolution 51:467–474

    Article  Google Scholar 

  • Saint Girons H, Naulleau G (1981) Poids des nouveau-nés et stratégies reproductrices de vipèrs européennes. Terre Vie 35:597–616

    Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment, 5th edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Seigel RA, Ford NB (1987) Reproductive ecology. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. Macmillan, New York, pp 210–249

    Google Scholar 

  • Seigel RA, Gibbons JW, Lynch TK (1995a) Temporal changes in reptile populations: effects of a severe drought on aquatic snakes. Herpetol 51:424–434

    Google Scholar 

  • Seigel RA, Loraine RK, Gibbons JW (1995b) Reproductive cycles and temporal variation in fecundity in the black swamp snake, Seminatrix pygaea. Am Midl Nat 134:371–377

    Article  Google Scholar 

  • Semlitsch RD, Gibbons JW (1982) Body size dimorphism and sexual selection in two species of water snakes. Copeia 1982:974–976

    Article  Google Scholar 

  • Sever DM, Ryan TJ, Morris T, Patton D, Swafford S (2000) Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). II. Annual oviducal cycle. J Morphol 245:146–160

    Article  CAS  PubMed  Google Scholar 

  • Shine R (1994) Sexual size dimorphism in snakes revisited. Copeia 1994:326–346

    Article  Google Scholar 

  • Shine R (2003) Reproductive strategies in snakes. Proc R Soc B 270:995–1004

    Article  PubMed  Google Scholar 

  • Shine R, Wall M (2005) Ecological divergence between the sexes in reptiles. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, Cambridge, pp 221–253

    Google Scholar 

  • Shine R, Olsson MM, Moore IT, LeMaster MP, Mason RT (2000) Body size enhances mating success in male garter snakes. Anim Behav 59:F4–F11

    Article  PubMed  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Turner FB (1977) The dynamics of populations of squamates, crocodilians, and rhynchocephalians. In: Gans C, Tinkle DW (eds) Biology of the reptilia, vol 7. Academic Press, London, pp 157–264

    Google Scholar 

  • Weatherhead PJ, Prosser MR, Gibbs HL, Brown GP (2002) Male reproductive success and sexual selection in northern water snakes determined by microsatellite DNA analysis. Behav Ecol 13:808–815

    Article  Google Scholar 

  • Wikelski M (2005) Evolution of body size in Galapagos marine iguanas. Proc R Soc B 272:1985–1993

    Article  PubMed  Google Scholar 

  • Wikelski M, Thom C (2000) Marine iguanas shrink to survive El Niño. Nature 403:37–38

    Article  CAS  PubMed  Google Scholar 

  • Wikelski M, Trillmich F (1997) Body size and sexual size dimorphism in marine iguanas fluctuate as a result of opposing natural and sexual selection: an island comparison. Evolution 51:922–936

    Article  Google Scholar 

  • Willson JD, Winne CT, Fedewa LA (2005) Unveiling escape and capture rates of aquatic snakes and salamanders (Siren spp. and Amphiuma means) in commercial funnel traps. J Freshwater Ecol 20:397–403

    Google Scholar 

  • Willson JD, Winne CT, Dorcas ME, Gibbons JW (2006) Post-drought responses of semi-aquatic snakes inhabiting an isolated wetland: insights on different strategies for persistence in a dynamic habitat. Wetlands 26:1071–1078

    Article  Google Scholar 

  • Willson JD, Winne CT, Keck MB (2008) Empirical tests of biased body size distributions in aquatic snake captures. Copeia 2008:401–408

    Article  Google Scholar 

  • Winne CT (2005) Increases in capture rates of an aquatic snake (Seminatrix pygaea) using naturally baited minnow traps: evidence for aquatic funnel trapping as a measure of foraging activity. Herpetol Rev 36:411–413

    Google Scholar 

  • Winne CT, Ryan TJ, Leiden Y, Dorcas ME (2001) Evaporative water loss in two natricine snakes, Nerodia fasciata and Seminatrix pygaea. J Herpetol 35:129–133

    Google Scholar 

  • Winne CT, Dorcas ME, Poppy SM (2005) Population structure, body size, and seasonal activity of black swamp snakes (Seminatrix pygaea). Southeast Nat 4:1–14

    Article  Google Scholar 

  • Winne CT, Willson JD, Andrews KM, Reed RN (2006a) Efficacy of marking snakes with disposable medical cautery units. Herpetol Rev 37:52–54

    Google Scholar 

  • Winne CT, Willson JD, Gibbons JW (2006b) Income breeding allows an aquatic snake Seminatrix pygaea to reproduce normally following prolonged drought-induced aestivation. J Anim Ecol 75:1352–1360

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Luke Fedewa for field assistance. Richard Seigel and Ray Loraine graciously provided population data from the 1980s. Brian Todd provided insightful comments on earlier versions of this manuscript. All procedures used in the study were approved by the University of Georgia Animal Care and Use Committee (no. A2003-10024) and by the South Carolina Department of Natural Resources (collection permits no. 56-2003). This research was supported in part by the US Department of Energy through Financial Assistance Award no. DE-FC09-07SR22506 to the University of Georgia Research Foundation. This study complies with the current laws of the United States of America.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher T. Winne.

Additional information

Communicated by Raoul Van Damme.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Winne, C.T., Willson, J.D. & Whitfield Gibbons, J. Drought survival and reproduction impose contrasting selection pressures on maximum body size and sexual size dimorphism in a snake, Seminatrix pygaea . Oecologia 162, 913–922 (2010). https://doi.org/10.1007/s00442-009-1513-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1513-8

Keywords

Navigation