, Volume 171, Issue 1, pp 83–91 | Cite as

Detrimental influence on performance of high temperature incubation in a tropical reptile: is cooler better in the tropics?

Physiological ecology - Original research


Global temperatures have risen over the last century, and are forecast to continue rising. Ectotherms may be particularly sensitive to changes in thermal regimes, and tropical ectotherms are more likely than temperate species to be influenced by changes in environmental temperature, because they may have evolved narrow thermal tolerances. Keelback snakes (Tropidonophis mairii) are tropical, oviparous reptiles. To quantify the effects of temperature on the morphology and physiology of hatchling keelbacks, clutches laid by wild-caught females were split and incubated at three temperatures, reflecting the average minimum, overall average and average maximum temperatures recorded at our study site. Upon hatching, the performance of neonates was examined at all three incubation temperatures in a randomized order over consecutive days. Hatchlings from the ‘hot’ treatment had slower burst swim speeds and swam fewer laps than hatchlings from the cooler incubation temperatures in all three test temperatures, indicating a low thermal optimum for incubation of this tropical species. There were no significant interactions between test temperature and incubation temperature across performance variables, suggesting phenotypic differences caused by incubation temperature did not acclimate this species to post-hatching conditions. Thus, keelback embryos appear evolutionarily adapted to development at cooler temperatures (relative to what is available in their habitat). The considerable reduction in hatchling viability and performance associated with a 3.5 °C increase in incubation temperature, suggests climate change may have significant population-level effects on this species. However, the offspring of three mothers exposed to the hottest incubation temperature were apparently resilient to high temperature, suggesting that this species may respond to selection imposed by thermal regime.


Climate change Developmental acclimation Ectotherm Performance Phenotype 


  1. Ackerman R, Lott D (2004) Thermal, hydric and respiratory climate of nests. Reptilian incubation. In: Deeming D (ed) Environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 15–43Google Scholar
  2. Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol Evol 12:235–239PubMedCrossRefGoogle Scholar
  3. Baayen RH (2011) languageR: Data sets and functions with “Analyzing Linguistic Data: A practical introduction to statistics”. R package version 1.4. http://CRAN.R-project.org/package=languageR
  4. Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4
  5. Birchard G (2004) Effects of incubation temperature. Reptilian incubation. In: Deeming D (ed) Environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 103–123Google Scholar
  6. Blouin-Demers G, Kissner K, Weatherhead P (2000) Plasticity in preferred body temperature of young snakes in response to temperature during development. Copeia 2000:841–845CrossRefGoogle Scholar
  7. Bogert C (1949) Thermoregulation in reptiles, a factor in evolution. Evolution 3:195–211PubMedCrossRefGoogle Scholar
  8. Booth D (2006) Influence of incubation temperature on hatchling phenotype in reptiles. Physiol Biochem Zool 79:274–281PubMedCrossRefGoogle Scholar
  9. Bradshaw WE, Holzapfel CM (2006) Evolutionary response to rapid climate change. Science 312:1477–1478PubMedCrossRefGoogle Scholar
  10. Brodie ED III, Garland T Jr (1993) Quantitative genetics of snake populations. In: Seigel RA, Collins JT (eds) Snakes; ecology and behaviour. McGraw-Hill, New York, pp 315–362Google Scholar
  11. Bronikowski A (2000) Experimental evidence for the adaptive evolution of growth rate in the garter snake Thamnophis elegans. Evolution 54:1760–1767PubMedGoogle Scholar
  12. Brown G, Shine R (2002) Reproductive ecology of a tropical natricine snake, Tropidonophis mairii (Colubridae). J Zool 258:63–72CrossRefGoogle Scholar
  13. Brown G, Shine R (2004) Maternal nest-site choice and offspring fitness in a tropical snake (Tropidonophis mairii, Colubridae). Ecology 85:1627–1634CrossRefGoogle Scholar
  14. Brown G, Shine R (2006) Effects of nest temperature and moisture on phenotypic traits of hatchling snakes (Tropidonophis mairii, Colubridae) from tropical Australia. Biol J Linn Soc 89:159–168CrossRefGoogle Scholar
  15. Burger J, Zappalorti R, Gochfield M (1987) Developmental effects of incubation temperature on hatchling pine snakes Pituophis melanoleucus. Comp Biochem Physiol A Comp Physiol 87:727–732CrossRefGoogle Scholar
  16. Caley M, Schwarzkopf L (2004) Complex growth rate evolution in a latitudinally widespread species. Evolution 58:862–869PubMedGoogle Scholar
  17. Cogger H (1986) Reptiles and amphibians of Australia. Reed New Holland, SydneyGoogle Scholar
  18. Deeming D (2004) Post-hatching phenotypic effects of incubation in reptiles. Reptilian incubation. In: Deeming D (ed) Environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 229–251Google Scholar
  19. Deere JA, Chown SL (2006) Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. Am Nat 168:630–644PubMedCrossRefGoogle Scholar
  20. Du W, Ji X (2008) The effects of incubation temperature on hatching success, embryonic use of energy and hatchling morphology in the Stripe-tailed Ratsnake Elaphe taeniura. Asiatic Herpetol Res 11:24–30Google Scholar
  21. Geister TL, Fischer K (2007) Testing the beneficial acclimation hypothesis; temperature effects on mating success in a butterfly. Behavioural Ecol 18:658–664CrossRefGoogle Scholar
  22. Goodman BA, Krockenberger AK, Schwarzkopf L (2007) Master of them all: performance specialization does not result in trade-offs in tropical lizards. Evol Ecol Res 9:527–546Google Scholar
  23. Gutzke W, Packard G (1987) Influence of the hydric and thermal environments on eggs and hatchlings of bull snakes Pituophis melanoleucus. Physiol Zool 60:9–17Google Scholar
  24. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biomet J 50(3):346–363CrossRefGoogle Scholar
  25. Huey RB, Dunham AE, Overall KL, Newman RA (1990) Variation in locomotor performance in demographically known populations of the lizard Sceloporus merriami. Physiol Zool 63:845–872Google Scholar
  26. Huey RB, Hertz PE, Sinervo B (2003) Behavioural drive versus behavioural inertia in evolution: a null model approach. Am Nat 161:357–366PubMedCrossRefGoogle Scholar
  27. Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Alvarez Perez HJ, Garland T (2009) Why tropical forest lizards are vulnerable to climate warming. Proc R Soc Lond B 1664:1939–1948CrossRefGoogle Scholar
  28. IPCC (2007) Climate Change 2007: The Physical Science Basis Working Group I Contribution to the IPCC Fourth Assessment Report. IPCC, GenevaGoogle Scholar
  29. Ji X, Gao J, Han J (2007) Ecology-phenotypic responses of hatchlings to constant versus fluctuating incubation temperatures in the multi-banded krait, Bungarus multicintus (Elapidae). Zool Sci 24:384–390PubMedCrossRefGoogle Scholar
  30. Kearney M, Porter WP, Williams C, Ritchie S, Hoffmann AA (2009) Integrating biophysical models and evolutionary theory to predict climatic impacts on species’ ranges: the dengue mosquito Aedes aegypti in Australia. Funct Ecol 23:528–538CrossRefGoogle Scholar
  31. Kolbe JJ, Janzen FJ (2002) Impact of nest-site selection on nest success and nest temperature in natural and disturbed habitats. Ecology 83:269–281CrossRefGoogle Scholar
  32. Leroi AM, Bennett AF, Lenski RE (1994) Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc Natl Acad Sci USA 91:1917–1921PubMedCrossRefGoogle Scholar
  33. Lin Z, Ji X, Luo L, Ma X (2005) Incubation temperature affects hatching success, embryonic expenditure of energy and hatchling phenotypes of a prolonged egg-retaining snake, Deinagkistrodon acutus (Viperidae). J Therm Biol 30:289–297CrossRefGoogle Scholar
  34. Lowenborg K, Shine R, Karvemo S, Hagman M (2010) Grass snakes exploit anthropogenic heat sources to overcome the distributional limits imposed by oviparity. Funct Ecol 24:1095–1102CrossRefGoogle Scholar
  35. Partridge L, Barrie B, Barton NH, Fowler K, French V (1995) Rapid laboratory evolution of adult life history traits in Drosophila melanogaster in response to temperature. Evolution 49:538–544CrossRefGoogle Scholar
  36. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
  37. Secor SM, Jayne BC, Bennett AF (1992) Locomotor performance and energetic cost of sidewinding by the snake Crotalus cerastes. J Exp Biol 163:1–14CrossRefGoogle Scholar
  38. Seebacher F (2005) A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility? J Comp Physiol B 175:453–461PubMedCrossRefGoogle Scholar
  39. Shine R (1999) Egg-laying reptiles in cold climates: determinants and consequences of nest temperatures in montane lizards. J Evol Biol 12:918–926CrossRefGoogle Scholar
  40. Shine R, Bonnet X (2000) Snakes: a new ‘model organism’ in ecological research? Trends Ecol Evol 15:221–222PubMedCrossRefGoogle Scholar
  41. Shine R, Thompson M (2006) Did embryonic responses to incubation conditions drive the evolution of reproductive modes in squamate reptiles? Herpetol Monogr 20:159–171CrossRefGoogle Scholar
  42. Shine R, Langkilde T, Wall M, Mason R (2005) The fitness correlates of scalation asymmetry in garter snakes Thamnophis sirtalis parietalis. Ecology 19:306–314Google Scholar
  43. Sinervo BS, Mendez-De-La-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagran-Santa Cruz M, Lara-Resendiz R, Martinez-Mendez N, Calderon-Espinosa ML, Meza-Lazaro RN, Gadsden H, Avila LJ, Morando M, De La Riva IJ, Sepulveda PV, Rocha CFD, Ibarguengoytia N, Puntriano CA, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW Jr (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899PubMedCrossRefGoogle Scholar
  44. Sorci G, Swallow JG, Garland T Jr, Clobert J (1995) Quantitative genetics of locomotor speed and endurance in the lizard Lacerta vivipara. Physiol Zool 68:698–720Google Scholar
  45. Stillwell RC, Fox CW (2005) Complex patterns of phenotypic plasticity: interactive effects of temperature during rearing and ovisposition. Ecology 86:924–934CrossRefGoogle Scholar
  46. Sunday JM, Bates AE, Dulvy NK (2010) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc Lond B 1295:1–9Google Scholar
  47. Vanhooydonck B, Van Damme R, Aerts P (2001) Speed and stamina trade-off in lacertid lizards. Evolution 55:1040–1048PubMedCrossRefGoogle Scholar
  48. Webb J, Brown G, Shine R (2001) Body size, locomotor speed and antipredator behaviour in a tropical snake (Tropidonophis mairii, Colubridae): the influence of incubation environments and genetic factors. Funct Ecol 15:561–568CrossRefGoogle Scholar
  49. Wilson DS (1998) Nest-site selection: microhabitat variation and its effects on the survival of turtle embryos. Ecology 79:1884–1892CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  2. 2.School of Biological SciencesThe University of QueenslandBrisbaneAustralia

Personalised recommendations