Skip to main content
SpringerLink
Log in

Effects of early postnatal environment on phenotype and survival of a lizard

  • Physiological ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Nutritional and thermal regimes experienced early in life can strongly influence offspring quality and ultimately adult life histories, especially in ectotherms. However, the importance of the interaction between diet and temperature during postnatal development and the effect on offspring quality are unknown. We compared offspring quality (size, shape, speed, behavior, and survival) of juvenile McCann’s skinks (Oligosoma maccanni) housed outdoors under variable thermal conditions (under shelter, but exposed to daily and seasonal variations in light and temperature) with those housed indoors under more stable thermal conditions (controlled temperatures providing 30–40% more basking opportunity) and with a control group (open field conditions). For those caged in captivity (indoors and outdoors), we also compared outcomes between those fed a restricted diet and those fed ad libitum. By comparing individuals raised under different environmental regimes, we aimed to determine whether direct effects of temperature or indirect effects of food supply are more important for offspring quality. Individuals provided with food ad libitum grew faster, and attained larger sizes than those raised on a restricted diet or in the field. Activity rates were higher in individuals exposed to stable rather than variable thermal conditions. Survival post release in the field was highest for larger neonates, and lowest in individuals raised under stable thermal conditions and a restricted diet. We found little evidence for effects of an interaction between feeding and thermal regimes on most factors measured. However, the conditions experienced by young animals (especially diet) do influence important traits for population persistence, such as survival, and may influence key reproductive parameters (e.g., age and size at maturity), which could have implications for conservation management. Further research, including the ultimate influence of early environmental conditions on fecundity and life expectancy, is urgently needed.

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

Access this article

Log in via an institution

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
Fig. 5

Similar content being viewed by others

References

  • Abe AS, Mendes EG (1980) Effect of body temperature on oxygen uptake in the water snakes Helicops modestus and Liophis miliaris. Comp Biochem Physiol 65A:367–370

    Article  Google Scholar 

  • Avery RA (1994) Growth in reptiles. Gerontology 40:193–199

    Article  PubMed  CAS  Google Scholar 

  • Barbraud T, Weimerskirch H (2001) Emperor penguins and climate change. Nature 411:183–186

    Article  PubMed  CAS  Google Scholar 

  • Bennett AF, Huey RB (1990) Studying the evolution of physiological performance. Oxf Surv Evol Biol 7:251–284

    Google Scholar 

  • Chamaillé-Jammes S, Massot M, Aragón P, Clobert J (2006) Global warming and positive fitness response in mountain populations of common lizards Lacerta vivipara. Glob Change Biol 12:392–402

    Article  Google Scholar 

  • Civantos E (2000) Home-range ecology, aggressive behaviour, and survival in juvenile lizards, Psammodromus algirus. Can J Zool 78:1681–1685

    Google Scholar 

  • Clobert J, Oppliger A, Sorci G, Ernande B, Swallow JG, Garland TJ (2000) Trade-offs in phenotypic traits: endurance at birth, growth, survival, predation and susceptability to parasitsm in a lizard, Lacerta vivipara. Funct Ecol 14:675–684

    Article  Google Scholar 

  • Congdon JD, Nagle RD, Dunham AE, Beck CW, Kinney OM, Yeomans SR (1999) The relationship of body size to survivorship of hatchling snapping turtles (Chelydra serpentina): an evaluation of the “bigger is better” hypothesis. Oecologia 121:224–235

    Article  Google Scholar 

  • Connolly JD, Cree A (2008) Risks of a late start to captive management for conservation: phenotypic differences between wild and captive individuals of a viviparous endangered skink (Oligosoma otagense). Biol Conserv 141:1283–1292

    Article  Google Scholar 

  • Deeming DC (2004) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham

    Google Scholar 

  • Diaz JA (1993) Breeding coloration, mating opportunities, activity, and survival in the lacertid lizard Psammodromus algirus. Can J Zool 71:1104–1110

    Article  Google Scholar 

  • Du WG (2006) Phenotypic plasticity in reproductive traits induced by food availability in a lacertid lizard, Takydromus septentrionalis. Oikos 112:363–369

    Article  Google Scholar 

  • Du W, Ji X, Shine R (2005) Does body-volume constrain reproductive output in lizards? Biol Lett 1:98–100

    Article  PubMed  Google Scholar 

  • Ferguson GW, Fox SF (1984) Annual variation of survival advantage of large juvenile sideblotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution 38:342–349

    Google Scholar 

  • Fernandez-Teruel A et al (2002) A quantitative trait locus influencing anxiety in the laboratory rat. Genome Res 12:618–626

    PubMed  CAS  Google Scholar 

  • Freeman AB (1997) Comparative ecology of two Oligosoma skinks in coastal Canterbury: a contrast with central Otago. NZ J Ecol 21:153–160

    Google Scholar 

  • Gaby MJ et al (2011) Thermal dependence of locomotor performance in two cool-temperate lizards. J Comp Physiol A 197:869–875

    Article  Google Scholar 

  • Garland TJ, Hankins E, Huey RB (1990) Locomotor capacity and social dominance in male lizards. Funct Ecol 4:243–250

    Google Scholar 

  • Hare KM, Cree A (2010a) Exploring the consequences of climate-induced changes in cloud cover on offspring of a cool-temperate viviparous lizard. Biol J Linn Soc 101:844–851

    Article  Google Scholar 

  • Hare KM, Cree A (2010b) Incidence, causes and consequences of pregnancy failure in viviparous lizards: implications for research and conservation settings. Reprod Fertil Dev 22:761–770

    Article  PubMed  Google Scholar 

  • Hare KM, Cree A (2011) Maternal and environmental influences on reproductive success of a viviparous grassland lizard. NZ J Ecol 35:254–260

    Google Scholar 

  • Hare JR, Holmes KM, Wilson JL, Cree A (2009) Modelling exposure to selected temperature during pregnancy: the limitations of reptilian viviparity in a cool-climate environment. Biol J Linn Soc 96:541–552

    Article  Google Scholar 

  • Hare KM, Hare JR, Cree A (2010) Parasites, but not palpation, are associated with pregnancy failure in a captive viviparous lizard. Herpetol Conserv Biol 5:563–570

    Google Scholar 

  • Heilbronn LK, Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr 78:361–369

    PubMed  CAS  Google Scholar 

  • Holmes KM, Cree A (2006) Annual reproduction in females of a viviparous skink (Oligosoma maccanni) in a subalpine environment. J Herpetol 40:141–151

    Article  Google Scholar 

  • Huey RB (1982) Temperature, physiology and ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the reptilia, vol 12. Academic, London, pp 25–92

  • Huntingford FA (2004) Implications of domestication and rearing conditions for the behaviour of cultivated fishes. J Fish Biol 65:122–142

    Article  Google Scholar 

  • Husak JF (2006) Does speed help you survive? A test with collared lizards of different ages. Funct Ecol 20:174–179

    Article  Google Scholar 

  • Husak JF, Fox SF, Lovern MB, van den Bussche RA (2006) Faster lizards sire more offspring: sexual selection on whole-animal performance. Evolution 60:2122–2130

    Google Scholar 

  • Jayne BC, Bennett AF (1990) Selection on locomotor performance capacity in a natural population of garter snakes. Evolution 44:1204–1229

    Google Scholar 

  • Kortet R, Hedrick A (2007) A behavioural syndrome in the field cricket Gryllus integer: intrasexual aggression is correlated with activity in a novel environment. Biol J Linn Soc 91:475–482

    Article  Google Scholar 

  • Kubicka L, Kratochvíl L (2009) First grow, then breed and finally get fat: hierarchical allocation to life-history traits in a lizard with invariant clutch size. Funct Ecol 23:595–601

    Article  Google Scholar 

  • Le Galliard J-F, Clobert J, Ferrière R (2004) Physical performance and darwinian fitness in lizards. Nature 432:502–505

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Marana T, Põdra M, Põlma M, Macdonald DW (2009) The survival of captive-born animals in restoration programmes—case study of the endangered European mink Mustela lutreola. Biol Conserv 142:1685–1692

    Article  Google Scholar 

  • Martín J, López P (1999) When to come out from a refuge: risk-sensitive and state-dependent decisions in an alpine lizard. Behav Ecol 10:487–492

    Article  Google Scholar 

  • McConnachie S, Alexander GJ (2004) The effect of temperature on digestive and assimilation efficiency, gut passage time and appetite in an ambush foraging lizard, Cordylus melanotus melanotus. J Comp Physiol B 174:99–105

    Article  PubMed  CAS  Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  • Olsson M, Shine R (2002) Growth to death in lizards. Evolution 56:1867–1870

    PubMed  Google Scholar 

  • Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915

    Article  PubMed  CAS  Google Scholar 

  • Pike DA, Pizzatto L, Pike BA, Shine R (2008) Estimating survival rates of uncatchable animals: the myth of high juvenile mortality in reptiles. Ecology 89:607–611

    Article  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rose B (1981) Factors affecting activity in Sceloporus virgatus. Ecology 62:706–716

    Article  Google Scholar 

  • Roy DB, Sparks TH (2000) Phenology of British butterflies and climate change. Glob Change Biol 6:407–416

    Article  Google Scholar 

  • Santos T, Pérez-Tris J, Carbonell R, Tellería JL, Díaz JA (2009) Monitoring the performance of wild-born and introduced lizards in a fragmented landscape: implications for ex situ conservation programmes. Biol Conserv 142:2923–2930

    Article  Google Scholar 

  • Schwarzkopf L, Shine R (1992) Costs of reproduction in lizards: escape tactics and susceptibility to predation. Behav Ecol Sociobiol 31:17–26

    Article  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Sinervo B, Doughty P (1996) Interactive effects of offspring size and timing of reproduction on offspring reproduction: experimental, maternal, and quantitative genetic aspects. Evolution 50:1314–1327

    Article  Google Scholar 

  • Sonesson M et al (2002) Growth of two peat-forming mosses in subarctic mires: species interactions and effects of simulated climate change. Oikos 99:151–160

    Article  Google Scholar 

  • Taborsky B (2006) The influence of juvenile and adult environments on life-history trajectories. Proc R Soc Lond Ser B 273:741–750

    Article  Google Scholar 

  • Verbeek MEM, Drent PJ, Wiepkena PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121

    Article  Google Scholar 

  • Warner DA, Andrews RM (2002) Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards. Biol J Linn Soc 76:105–124

    Article  Google Scholar 

  • Warner DA, Shine R (2007) Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154:65–73

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Anne Besson, Matthew Downes, Mya Gaby, Kim Garrett, Jo Hoare, Clément Lagrue, Les Judd, Simon Madill, Riki Mules, Sophie Penniket, Robert Trought, Laura Weir, Nathan Whitmore, Cynthia Winkworth, and especially Murray McKenzie for their assistance in the field and/or laboratory. Thanks also to Amy Armstrong for supplying live insects, Greg Hand, Marjorie and Jonathan Hay, Keith and Margaret Philip, and the New Zealand Department of Conservation (DOC) for allowing us access to their land to capture skinks, to DOC field staff for continued mammal trapping, and researchers from Landcare Research for the use of their pens. We thank David Sinn and Shinichi Nakagawa for statistical advice and two anonymous reviewers and members of the Cree Lab for useful comments on drafts of the manuscript. Temperature data were provided by Oceana Gold (Macraes) and the Energy Studies Programme at the University of Otago. Financial support was provided by the Foundation for Research Science and Technology, New Zealand Science and Technology Postdoctoral Fellowship to KMH. Research was carried out following consultation with Ngāi Tahu and approval from DOC and the University of Otago Animal Ethics Committee.

Author information

Author notes

  1. Amanda J. Caldwell

    Present address: School of Zoology, University of Tasmania, Private Bag 05, Tasmania, 7001, Australia

Authors and Affiliations

  1. Department of Zoology, University of Otago, PO Box 56, Dunedin, 9054, New Zealand

    Kelly M. Hare, Amanda J. Caldwell & Alison Cree

Authors
  1. Kelly M. Hare
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda J. Caldwell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alison Cree
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kelly M. Hare.

Additional information

Communicated by Lin Schwarzkopf.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hare, K.M., Caldwell, A.J. & Cree, A. Effects of early postnatal environment on phenotype and survival of a lizard. Oecologia 168, 639–649 (2012). https://doi.org/10.1007/s00442-011-2145-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2145-3

Keywords

Search

Navigation