Your PDF has successfully downloaded.

You may be interested in finding more content on these topics:


You are not currently logged in.

Access JSTOR through your library or other institution:


Log in through your institution.

The Behavior-Physiology Nexus: Behavioral and Physiological Compensation Are Relied on to Different Extents between Seasons

Christine H. Basson and Susana Clusella-Trullas
Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches
Vol. 88, No. 4 (July/August 2015), pp. 384-394
DOI: 10.1086/682010
Stable URL:
Page Count: 11
  • Download PDF
  • Add to My Lists
  • Cite this Item
We're having trouble loading this content. Download PDF instead.


AbstractEnvironmental variability occurring at different timescales can significantly reduce performance, resulting in evolutionary fitness costs. Shifts in thermoregulatory behavior, metabolism, and water loss via phenotypic plasticity can compensate for thermal variation, but the relative contribution of each mechanism and how they may influence each other are largely unknown. Here, we take an ecologically relevant experimental approach to dissect these potential responses at two temporal scales: weather transients and seasons. Using acclimation to cold, average, or warm conditions in summer and winter, we measure the direction and magnitude of plasticity of resting metabolic rate (RMR), water loss rate (WLR), and preferred body temperature (Tpref) in the lizard Cordylus oelofseni within and between seasons. In summer, lizards selected lower Tpref when acclimated to warm versus cold but had no plasticity of either RMR or WLR. By contrast, winter lizards showed partial compensation of RMR but no behavioral compensation. Between seasons, both behavioral and physiological shifts took place. By integrating ecological reality into laboratory assays, we demonstrate that behavioral and physiological responses of C. oelofseni can be contrasting, depending on the timescale investigated. Incorporating ecologically relevant scenarios and the plasticity of multiple traits is thus essential when attempting to forecast extinction risk to climate change.

Notes and References

This item contains 77 references.

Literature Cited
  • ['Angilletta M.J. 2009. Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, New York.']
  • ['Angilletta M.J., A.F. Bennett, H. Guderley, C.A. Navas, F. Seebacher, and R.S. Wilson. 2006. Coadaptation: a unifying principle in evolutionary thermal biology. Physiol Biochem Zool 79:282–294.']
  • ['Angilletta M.J., T. Hill, and M.A. Robson. 2002. Is physiological performance optimized by thermoregulatory behavior? a case study of the eastern fence lizard, Sceloporus undulatus. J Therm Biol 27:199–204.']
  • ['Bentley P.J. and K. Schmidt-Nielsen. 1966. Cutaneous water loss in reptiles. Science 151:1547–1549.']
  • ['Burnham K.P. and D.R. Anderson. 2001. Kullback-Leiber information as a basis for strong inference in ecological studies. Wildl Res 28:111–119.']
  • ['Burton T., S.S. Killen, J.D. Armstrong, and M.B. Metcalfe. 2011. What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B 278:3465–3473.']
  • ['Case T.J. 1976. Seasonal aspects of thermoregulatory behaviour in the chuckwalla, Sauromalus obesus (Reptilia, Lacertilia, Iguanidae). J Herpetol 10:5–95.']
  • ['Chevin L.-M., R. Lande, and G.M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8(4):e1000357.']
  • ['Christian K. and B. Green. 1994. Seasonal energetics and water turnover of the frillneck lizard (Chlamydosaurus kingii) in the wet-dry tropics of Australia. Herpetologica 50:274–281.']
  • ['Clarke A. 1993. Seasonal acclimatization and latitudinal compensation in metabolism: do they exist? Funct Ecol 7:139–149.']
  • ['———. 2003. Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581.']
  • ['Clarke A. and K.P.P. Fraser. 2004. Why does metabolism scale with temperature? Funct Ecol 18:243–251.']
  • ['Claussen D.L. 1967. Studies of water loss in two species of lizards. Comp Biochem Physiol 20:115–130.']
  • ['Clusella-Trullas S. and A. Botes. 2007. Faecal analysis suggests generalist diets in three species of Western Cape cordylids. Afr Zool 43:125–130.']
  • ['Clusella-Trullas S. and S.L. Chown. 2014. Lizard thermal trait variation at multiple scales: a review. J Comp Physiol B 184:5–21.']
  • ['Clusella-Trullas S., J.S. Terblanche, and S.L. Chown. 2010. Phenotypic plasticity of locomotion performance in the seed harvester Messor capensis (Formicidae). Physiol Biochem Zool 83:519–530.']
  • ['Clusella-Trullas S., J.H. van Wyk, and J.R. Spotila. 2009. Thermal benefits of melanism in cordylid lizards: a theoretical and field test. Ecology 90:2297–2312.']
  • ['Congdon J.D., R.E. Ballinger, and K.A. Nagy. 1979. Energetics, temperature and water relations in winter aggregated Sceloporus jarrovi (Sauria: Iguanidae). Ecology 60:30–35.']
  • ['Congdon J.D., A.E. Dunham, and D.W. Tinkle. 1982. Energy budgets and life histories of reptiles. Pp. 233–271 in C. Gans, ed. Biology of the Reptilia. Academic Press, New York.']
  • ['Cowles R.B. and C.M. Bogert. 1944. A preliminary study of the thermal requirements of desert reptiles. Bull Am Mus Nat Hist 83:261–296.']
  • ['Crawley M. J. 2007. The R book. Wiley, West Sussex.']
  • ['Davies P.M.C., J.W. Patterson, and E.L. Bennett. 1981. Metabolic coping strategies in cold tolerant reptiles. J Therm Biol 6:321–330.']
  • ['Deutsch C.A., J.J. Tewksbury, R.B. Huey, K.S. Sheldon, C.K. Ghalambor, D.C. Haak, and P.R. Martin. 2008. Impact of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672.']
  • ['DeWitt T.J., A. Sih, and D. Sloan Wilson. 1998. Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81.']
  • ['Dillon M.E., L.R.Y. Cahn, and R.B. Huey. 2007. Life history consequences of temperature transients in Drosophila melanogaster. J Exp Biol 210:2897–2904.']
  • ['Dmi’el R., G. Perry, and J. Lazell. 1997. Evaporative water loss in nine insular populations of the lizard Anolis cristatellus group in the British Virgin Isles. Biotropica 29:111–116.']
  • ['Dunham A.E., B.W. Grant, and K.L. Overall. 1989. Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectotherms. Physiol Zool 62:335–355.']
  • ['Dutton R.H. and L.C. Fitzpatrick. 1974. Metabolic compensation to seasonal temperatures in the rusty lizard, Sceloporus olivaceus. Comp Biochem Physiol A 51:309–318.']
  • ['Fogel G. 2003. The art of armadillo lizards (Cordylus cataphractus): fifteen years of captive observations. Bull Chic Herpetol Soc 38:113–119.']
  • ['Glanville E.J. and F. Seebacher. 2006. Compensation for environmental change by complementary shifts of thermal sensitivity and thermoregulatory behaviour in an ectotherm. J Exp Biol 209:4869–4877.']
  • ['Guderley H. 2004. Metabolic responses to low temperature in fish muscle. Biol Rev 79:409–427.']
  • ['Gvoždík L. 2012. Plasticity of preferred body temperatures as means of coping with climate change? Biol Lett 8:262–265.']
  • ['Hadamová M. and L. Gvoždík. 2011. Seasonal acclimation of preferred body temperature improves the opportunity for thermoregulation in newts. Physiol Biochem Zool 84:166–174.']
  • ['Hare K.M., S. Pledger, M.B. Thompson, J.H. Miller, and C.H. Daugherty. 2010. Nocturnal lizards from a cool-temperate environment have high metabolic rates at low temperatures. J Comp Physiol B 180:1173–1181.']
  • ['Heatwole H. 1976. Reptile ecology. University of Queensland Press, St. Lucia.']
  • ['Hertz P.E., R.B. Huey, and E. Nevo. 1983. Homage to Santa Anita: thermal sensitivity of sprint speed in agamid lizards. Evolution 37:1075–1084.']
  • ['Hertz P.E., R.B. Huey, and R.D. Stevenson. 1993. Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. Am Nat 142:796–818.']
  • ['Hochachka P.W. and G.N. Somero. 2002. Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York.']
  • ['Huey R.B. and A.F. Bennett. 1987. Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance. Evolution 41:1098–1115.']
  • ['———. 1990. Physiological adjustments to fluctuating thermal environments: an ecological and evolutionary perspective. Pp. 37–59 in R. I. Morimoto, A. Tissieres, and C. Georgopoulos, eds. Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, New York.']
  • ['Huey R.B., C.A. Deutsch, J.J. Tewksbury, L.J. Vitt, P.E. Hertz, H.J. Álvarez Pérez, and T. Garland. 2009. Why tropical forest lizards are vulnerable to climate warming. Proc R Soc B 276:1939–1948.']
  • ['Huey R.B., P.E. Hertz, and B. Sinervo. 2003. Behavioural drive versus behavioural inertia in evolution: a null model approach. Am Nat 161:357–366.']
  • ['Huey R.B. and M. Slatkin. 1976. Costs and benefits of lizard thermoregulation. Q Rev Biol 51:363–384.']
  • ['Kaufmann J.S. and A.F. Bennett. 1989. The effect of temperature and thermal acclimation on locomotor performance in Xantusia vigilis, the desert night lizard. Physiol Zool 62:1047–1058.']
  • ['Kingsolver J.G. and R.B. Huey. 1998. Evolutionary analyses of morphological and physiological plasticity in thermally variable environments. Am Zool 38:545–560.']
  • ['Lee J.C. 1980. Comparative thermal ecology of two lizards. Oecologia 44:171–176.']
  • ['Leroi A., A.F. Bennett, and R.E. Lenski. 1994. Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc Natl Acad Sci USA 91:1917–1921.']
  • ['Li H., Z. Wang, W. Mei, and X. Ji. 2009 Temperature acclimation affects thermal preference and tolerance in three Eremias lizards (Lacertidae). Curr Zool 17:258–265.']
  • ['Licht P. 1964. The temperature dependence of myosin-adenosinetriphosphatase and alkaline phosphatase in lizards. Comp Biochem Physiol 12:331–340.']
  • ['Lighton J.R.B. 2008. Measuring metabolic rates: a manual for scientists. Oxford University Press, New York.']
  • ['Lillywhite H.B. 2006. Review: water relations of tetrapod integument. J Exp Biol 209:202–226.']
  • ['Little A.G., T. Kunisue, K. Kannan, and F. Seebacher. 2013. Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish (Danio rerio). BMC Biol 11:26.']
  • ['Losos B.L., T.W. Schoener, and D.A. Spiller. 2004. Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432:505–508.']
  • ['Martin T.L. and R.B. Huey. 2008. Why “suboptimal” is optimal: Jensen’s inequality and ectotherm thermal preferences. Am Nat 171:E102–E118.']
  • ['Mautz W.J. 1982. Correlations of both respiratory and cutaneous water losses of lizards with habitat aridity. J Comp Physiol B 149:25–30.']
  • ['McNab B.K. 2002. The physiological ecology of vertebrates: a view from energetics. Cornell University Press, Ithaca, NY.']
  • ['Mouton P.F.N. and J.H. van Wyk. 1990. Taxonomic status of the melanistic forms of the Cordylus cordylus complex (Reptilia: Cordylidae) in the south-western Cape, South Africa. S Afr J Zool 25:31–38.']
  • ['Paaijmans K.P., R.L. Heinig, R.A. Seliga, J.I. Blanford, S. Blanford, C.C. Murdock, and M.B. Thomas. 2013. Temperature variation makes ectotherms more sensitive to climate change. Global Change Biol 19:2373–2380.']
  • ['Pinheiro J., D. Bates, S. DebRoy, D. Sarkar, and the R Development Core Team. 2013. nlme: linear and nonlinear mixed effects models. R package. Version 3.1–111.']
  • ['Precht H. 1958. Concepts of temperature adaptation of unchanging reaction systems of cold-blooded animals. Pp. 50–78 in C.L. Prosser, ed. Physiological adaptation. American Physiological Society, Washington, DC.']
  • ['R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.']
  • ['Reed T.E., D.E. Schindler, and R.S. Waples. 2011. Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conserv Biol 25:56–63.']
  • ['Roberts L.A. 1968. Oxygen consumption in the lizard Uta stansburiana. Ecology 49:809–819.']
  • ['Rogers K.D., M.B. Thompson, and F. Seebacher. 2007. Beneficial acclimation: sex specific thermal acclimation of metabolic capacity in the striped marsh frog (Limnodynastes peronii). J Exp Biol 210:2932–2938.']
  • ['Seebacher F. 2005. A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility? J Comp Physiol B 175:453–461.']
  • ['Seebacher F., M.D. Brand, P.L. Else, H. Guderley, A.J. Hulbert, and C.D. Moyes. 2010. Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiol Biochem Zool 83:721–732.']
  • ['Sinervo B., F. Méndez-de-la-Cruz, D.B. Miles, B. Heulin, E. Bastiaans, M.V.-S. Cruz, R. Lara-Resendiz, et al. 2010. Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899.']
  • ['Somero G.N. 1978. Temperature adaptations of enzymes: biological optimisation through structure-function compromises. Annu Rev Ecol Syst 9:1–29.']
  • ['———. 2010. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. J Exp Biol 213:912–920.']
  • ['Tattersall G.J., V. Cadena, and M.C. Skinner. 2006. Respiratory cooling and thermoregulatory coupling in reptiles. Respir Physiol Neurobiol 154:302–318.']
  • ['Tsuji J.S. 1988a. Seasonal profiles of standard metabolic rate of lizards (Sceloporus occidentalis) in relation to latitude. Physiol Zool 61:230–240.']
  • ['———. 1988b. Thermal acclimation of metabolism in Sceloporus lizards from different latitudes. Physiol Zool 61:241–253.']
  • ['Wheeler P.E. 1986. Thermal acclimation of metabolism and preferred body temperature in lizards. J Therm Biol 11:161–166.']
  • ['Wilhoft D.C. and J.D. Anderson. 1960. Effect of acclimation on the preferred body temperature of the lizard, Sceloporus occidentalis. Science 131:610–611.']
  • ['Woods H.A. and J.F. Harrison. 2001. The beneficial acclimation hypothesis versus acclimation of specific traits: physiological change in water-stressed Manduca sexta caterpillars. Physiol Biochem Zool 74:32–44.']
  • ['Zuur A.F., E.N. Ieno, N.J. Walker, A.A. Saveliev, and G.M. Smith. 2009. Mixed effects models and extensions in ecology with R. Springer, New York.']
  • ['Zytynska S.E., M.F. Fay, D. Penney, and R.F. Preziosi. 2011. Genetic variation in a tropical tree species influences the associated epiphytic plant and invertebrate communities in a complex forest ecosystem. Philos Trans R Soc B 366:1329–1336.']