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Thermal strategies and energetics in two sympatric colubrid snakes with contrasted exposure

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Abstract

The thermoregulatory strategy of reptiles should be optimal if ecological costs (predation risk and time devoted to thermoregulation) are minimized while physiological benefits (performance efficiency and energy gain) are maximized. However, depending on the exact shape of the cost and benefit curves, different thermoregulatory optima may exist, even between sympatric species. We studied thermoregulation in two coexisting colubrid snakes, the European whipsnake (Hierophis viridiflavus, Lacépède 1789) and the Aesculapian snake (Zamenis longissimus, Laurenti 1768) that diverge markedly in their exposure, but otherwise share major ecological and morphological traits. The exposed species (H. viridiflavus) selected higher body temperatures (~30°C) than the secretive species (Z. longissimus, ~25°C) both in a laboratory thermal gradient and in the field. Moreover, this difference in body temperature was maintained under thermophilic physiological states such as digestion and molting. Physiological and locomotory performances were optimized at higher temperatures in H. viridiflavus compared to Z. longissimus, as predicted by the thermal coadaptation hypothesis. Metabolic and energetic measurements indicated that energy requirements are at least twice higher in H. viridiflavus than in Z. longissimus. The contrasted sets of coadapted traits between H. viridiflavus and Z. longissimus appear to be adaptive correlates of their exposure strategies.

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References

  • Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268

    Article  Google Scholar 

  • Angilletta MJ, Bennett AF, Guderley H, Navas CA, Seebacher F, Wilson RS (2006) Coadaptation: a unifying principle in evolutionary thermal biology. Physiol Biochem Zool 79(2):282–294

    Article  PubMed  Google Scholar 

  • Bakken GS (1992) Measurement and application of operative and standard operative temperatures in ecology. Am Zool 32:194–216

    Google Scholar 

  • Belliure J, Carrascal LM, Diaz JA (1996) Covariation of thermal biology and foraging mode in two Mediterranean lacertid lizards. Ecology 77(4):1163–1173

    Article  Google Scholar 

  • Ben Ezra E, Bulté G, Blouin-Demers G (2008) Are locomotor performances coadapted to preferred basking temperature in the Northern Map Turtle (Graptemys geographica)? J Herpetol 42(2):322–331

    Article  Google Scholar 

  • Bennett AF, Hicks JW, Cullum AJ (2000) An experimental test of the thermoregulatory hypothesis for the evolution of endothermy. Evolution 54(5):1768–1773

    CAS  PubMed  Google Scholar 

  • Blouin-Demers G, Nadeau P (2005) The cost-benefit model of thermoregulation does not predict lizard thermoregulatory behaviour. Ecology 86(3):560–566

    Article  Google Scholar 

  • Blouin-Demers G, Weatherhead PJ (2001a) An experimental test of the link between foraging, habitat selection and thermoregulation in a black rat snakes Elaphe obsoleta obsoleta. J Anim Ecol 70:1006–1013

    Article  Google Scholar 

  • Blouin-Demers G, Weatherhead PJ (2001b) Thermal ecology of black rat snakes (Elaphe obsoleta) in a thermally challenging environment. Ecology 82(11):3025–3043

    Google Scholar 

  • Blouin-Demers G, Weatherhead PJ (2002) Habitat-specific behavioral thermoregulation by black rat snake (Elaphe obsoleta obsoleta). Oikos 97(1):59–68

    Article  Google Scholar 

  • Blouin-Demers G, Weatherhead PJ, McCracken HA (2003) A test of the thermal coadaptation hypothesis with black rat snakes (Elaphe obsoleta) and northern water snakes (Nerodia sipedon). J Therm Biol 28:331–340

    Article  Google Scholar 

  • Bonnet X, Naulleau G, Shine R (1999) The dangers of leaving home: dispersal and mortality in snakes. Biol Conserv 89:39–50

    Article  Google Scholar 

  • Brown GP, Weatherhead PJ (2000) Thermal ecology and sexual size dimorphism in northern water snakes, Nerodia sipedon. Ecol Monogr 70(2):311–330

    Google Scholar 

  • Bulté G, Blouin-Demers G (2006) Cautionary notes on the descriptive analysis of performance curves in reptiles. J Therm Biol 31(4):287–291

    Article  Google Scholar 

  • Capizzi D, Luiselli L (1996) Feeding relationships and competitive interactions between phylogenetically unrelated predators (owls and snakes). Acta Oecol 17(4):265–284

    Google Scholar 

  • Capizzi D, Luiselli L, Capula M, Rugiero L (1995) Feeding habits of a mediterranean community of snakes in relation to prey availability. Revue d’Ecologie-la Terre et la Vie 50(4):353–363

    Google Scholar 

  • Carfagno GLF, Weatherhead PJ (2006) Intraspecific and interspecific variation in use of forest-edge habitat by snakes. Can J Zool 84(10):1440–1452

    Article  Google Scholar 

  • Carfagno GLF, Weatherhead PJ (2008) Energetics and space use: intraspecific and interspecific comparisons of movements and home ranges of two colubrid snakes. J Anim Ecol 77:416–424

    Article  PubMed  Google Scholar 

  • Christian KA, Weavers BW (1996) Thermoregulation of monitor lizards in Australia: an evaluation of methods in thermal biology. Ecol Monogr 66:139–167

    Article  Google Scholar 

  • Cooper WE (1998) Risk factors and emergence from refuge in the lizard Eumeces laticeps. Behaviour 135:1065–1076

    Google Scholar 

  • Downes S (2001) Trading heat and food for safety: costs of predator avoidance in a lizard. Ecology 82(10):2870–2881

    Article  Google Scholar 

  • Du WG, Shou L, Shen JY (2006) Habitat selection in two sympatric Chinese skinks, Eumeces elegans and Sphenomorphus indicus: do thermal preferences matter? Can J Zool 84(9):1300–1306

    Article  Google Scholar 

  • Dubois Y, Blouin-Demers G, Shipley B, Thomas D (2009) Thermoregulation and habitat selection in wood turtles Glyptemys insculpta: chasing the sun slowly. J Anim Ecol 78(5):1023–1032

    Article  CAS  PubMed  Google Scholar 

  • Filippi E, Luiselli L (2006) Changes in community composition, habitats and abundance of snakes over 10+ years in a protected area in Italy: conservation implications. Herpetol J 16(1):29–36

    Google Scholar 

  • Fitzgerald M, Shine R, Lemckert F (2003) A reluctant heliotherm: thermal ecology of the arboreal snake Hoplocephalus stephensii (Elapidae) in dense forest. J Therm Biol 28:515–524

    Article  Google Scholar 

  • Garland T Jr, Adolph SC (1994) Why not to do 2-species comparative studies—limitations on inferring adaptation. Physiol Zool 67(4):797–828

    Google Scholar 

  • Gibson AR, Smucny DA, Kollar J (1989) The effects of feeding and ecdysis on temperature selection by young garter snakes in a simple thermal mosaic. Can J Zool 67(1):19–23

    Article  Google Scholar 

  • Goldsbrough CL, Hochuli DF, Shine R (2004) Fitness benefits of retreat site selection: spiders, rocks and thermal cues. Ecology 85(6):1635–1641

    Article  Google Scholar 

  • Gregory PT, Crampton LH, Skebo KM (1999) Conflicts and interactions among reproduction, thermoregulation and feeding in viviparous reptiles: are gravid snakes anorexic? J Zool 248:231–241

    Article  Google Scholar 

  • Grover MC (1996) Microhabitat use and thermal ecology of two narrowly sympatric Sceloporus (Phrynosomatidae) lizards. J Herpetol 30(2):152–160

    Article  Google Scholar 

  • Gvoždík L (2002) To heat or to save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: Lacertidae) in different thermal environments along altitudinal gradient. Can J Zool 80:479–492

    Article  Google Scholar 

  • Hertz PE, Huey RB, Nevo E (1982) Fight versus flight: body temperature influences defensive responses of lizards. Anim Behav 30:676–679

    Article  Google Scholar 

  • Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. Am Nat 142(5):796–818

    Article  CAS  PubMed  Google Scholar 

  • Huey RB (1991) Physiological consequences of habitat selection. Am Nat 137:91–115

    Article  Google Scholar 

  • Huey RB, Bennett AF (1987) Phylogenetic studies of coadaptation—preferred temperatures versus optimal performance temperatures of lizards. Evolution 41(5):1098–1115

    Article  Google Scholar 

  • Huey RB, Hertz PE (1984) Is a-jack-of-all temperatures a master of none? Evolution 38(2):441–444

    Article  Google Scholar 

  • Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4(5):131–135

    Article  Google Scholar 

  • Huey RB, Slatkin M (1976) Costs and benefits of lizard thermoregulation. Q Rev Biol 51:363–384

    Article  CAS  PubMed  Google Scholar 

  • Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366

    Google Scholar 

  • Kearney M (2002) Hot rocks and much-too-hot rocks: seasonal patterns of retreat-site selection by a nocturnal ectotherm. J Therm Biol 27(3):205–218

    Article  Google Scholar 

  • Kearney M, Predavec M (2000) Do nocturnal ectotherms thermoregulate? A study of the temperate gecko Christinus marmoratus. Ecology 81(11):2984–2996

    Google Scholar 

  • Kery M (2002) Inferring the absence of a species—a case study of snakes. J Wildl Manage 66(2):330–338

    Article  Google Scholar 

  • Knies JL, Kingsolver JG, Burch CL (2009) Hotter is better and broader: thermal sensitivity of fitness in a population of bacteriophages. Am Nat 173(4):419–430

    Article  PubMed  Google Scholar 

  • Lasiewski RC, Acosta AL, Bernstein ML (1966) Evaporative water loss in birds. I. Characteristics of the open flow method of determination and their relation to estimates of thermoregulatory ability. Comp Biochem Physiol 19:445–457

    Article  Google Scholar 

  • Lenk P, Joger U, Wink M (2001) Phylogenetic relationships among European ratsnakes of the genus Elaphe Fitzinger based on mitochondrial DNA sequence comparisons. Amphib-reptil 22(3):329–339

    Article  Google Scholar 

  • Luiselli L (2006) Ecological modelling of convergence patterns between European and African ‘whip’ snakes. Acta Oecol 30(1):62–68

    Article  Google Scholar 

  • Luiselli L, Capizzi D (1997) Influences of area, isolation and habitat features on distribution of snakes in Mediterranean fragmented woodlands. Biodivers Conserv 6(10):1339–1351

    Article  Google Scholar 

  • Luiselli L, Filippi E, Di Lena E (2007) Ecological relationships between sympatric Vipera aspis and Vipera ursinii in high-altitude habitats of central Italy. J Herpetol 41(3):378–384

    Article  Google Scholar 

  • Martin J (2001) When hiding from predators is costly: optimization of refuge use in lizards. Etologia 9:9–13

    Google Scholar 

  • Martin J, Lopez P (1999) When to come out from a refuge: risk-sensitive and state-dependent decisions in a alpine lizard. Behav Ecol 10(5):487–492

    Article  Google Scholar 

  • Nagy KA (1983) Ecological energetics. In: Huey RB, Pianka ER, Schoener TW (eds) Lizard ecology: studies of a model organism. Harvard University Press, Cambridge, pp 24–54

    Google Scholar 

  • Naulleau G (1984) Les serpents de France, Revue Française d’Aquariologie, Paris

  • Naulleau G (1997) Coluber viridiflavus (Lacepède, 1789) Atlas of Amphibians and Reptiles in Europe. Societas Herpetologica et Muséum National d’Histoire Naturelle Paris, pp 342–343

  • Nevo E, Rashkovetsky E, Pavlicek T, Korol A (1998) A complex adaptive syndrome in Drosophila caused by microclimatic contrasts. Heredity 80(1):9–16

    Article  PubMed  Google Scholar 

  • Pearson DJ, Shine R, Williams A (2003) Thermal biology of large snakes in cool climates: a radio-telemetric study of carpet pythons (Morelia spilota imbricata) in southwestern Australia. J Therm Biol 28:117–131

    Article  Google Scholar 

  • Pianka ER, Pianka HD (1970) Ecology of Moloch horridus (Lacertilia Agamidae) in western Australia. Copeia 1970:90–103

  • Pierce JB, Fleet RR, McBrayer L, Rudolph DC (2008) Use of trees by the Texas ratsnake (Elaphe obsoleta) in eastern Texas. Southeast Nat 7(2):359–366

    Article  Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing

  • Ratkowsky DA, Lowry RK, McMeekin TA, Stokes AN, Chandler RE (1983) Model for bacterial growth rate throughout the entire biokinetic temperature range. J Bacteriol 154:1222–1226

    CAS  PubMed  Google Scholar 

  • Reinert HK (1984) Habitat variation within sympatric snake populations. Ecology 65(5):1673–1682

    Article  Google Scholar 

  • Reinert HR, Cundall D (1982) An improved surgical implantation method for radio-tracking snakes. Copeia 1982(3):702–705

    Article  Google Scholar 

  • Robert KA, Thompson MB (2003) Reconstructing thermochron iButtons to reduce size and weight as a new technique in the study of small animal thermal biology. Herpetol Rev 34(2):130–132

    Google Scholar 

  • Row J, Blouin-Demers G (2007) Thermal quality influences effectiveness of thermoregulation, habitat use, and behaviour in milksnakes. Oecologia 148:1–11

    Article  Google Scholar 

  • Rugiero L, Capizzi D, Luiselli L (2002) Interactions between sympatric snakes, Coluber viridiflavus and Elaphe longissima: are there significant inter-annual differences in coexistence patterns? Ecol Mediterr 28(2):75–91

    Google Scholar 

  • Sartorius SS, do Amaral JPS, Durtsche RD, Deen CM, Lutterschmidt WI (2002) Thermoregulatory accuracy, precision, and effectiveness in two sand-dwelling lizards under mild environmental conditions. Can J Zool 80:1966–1976

    Article  Google Scholar 

  • Scheers H, Van Damme R (2002) Micro-scale differences in thermal habitat quality and a possible case of evolutionary flexibility in the thermal physiology of lacertid lizards. Oecologia 132(3):323–331

    Article  Google Scholar 

  • Secor SM, Nagy KA (1994) Bioenergetic correlates of foraging mode for the snakes Crotalus cerastes and Masticophis flagellum. Ecology 75(6):1600–1614

    Article  Google Scholar 

  • Shine R (1980) Ecology of eastern Australian whipsnakes of the genus Demansia. J Herpetol 14(4):381–389

    Article  Google Scholar 

  • Shine R, Elphick MJ, Harlow PS (1997) The influence of natural incubation environments on the phenotypic traits of hatchling lizards. Ecology 78(8):2559–2568

    Article  Google Scholar 

  • Sievert LM, Jones DM, Puckett MW (2005) Postprandial thermophily, transit rate, and digestive efficiency of juvenile cornsnakes, Pantherophis guttatus. J Therm Biol 30(5):354–359

    Article  Google Scholar 

  • Singh S, Smyth AK, Blomberg SP (2002) Thermal ecology and structural habitat use of two sympatric lizards (Carlia vivax and Lygisaurus foliorum) in subtropical Australia. Aust Ecol 27:616–623

    Article  Google Scholar 

  • Sperry JH, Weatherhead PJ (2009) Sex differences in behavior associated with sex-biased mortality in an oviparous snake species. Oikos 118(4):627–633

    Google Scholar 

  • Stevenson RD, Peterson CR, Tsuji J (1985) The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiol Zool 58:46–57

    Google Scholar 

  • Tattersall GJ, Milsom WK, Abe AS, Brito SP, Andrade DV (2004) The thermogenesis of digestion in rattlesnakes. J Exp Biol 207:579–585

    Article  PubMed  Google Scholar 

  • Tsai TS, Tu MC (2005) Postprandial thermophily of Chinese green tree vipers, Trimeresurus s. stejnegeri: Interfering factors on snake temperature selection in a thigmothermal gradient. J Therm Biol 30(6):423–430

    Article  Google Scholar 

  • Whitaker PB, Shine R (2002) Thermal biology and activity patterns of the eastern brownsnake (Pseudonaja textilis): a radiotelemetric study. Herpetologica 58(4):436–452

    Article  Google Scholar 

  • Whitaker PB, Shine R (2003) A radiotelemetric study of movements and shelter-site selection by free-ranging brownsnakes (Pseudonaja textilis, Elapidae). Herpetol Monogr 17:130–144

    Article  Google Scholar 

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Acknowledgments

We thank Julien Farsy and Pierre Surre for assistance in the field. Dale DeNardo and Ty Hoffman provided invaluable support in calorimetric chamber installation. David Pinaud gave precious help on statistical analyses. We thank Xavier Bonnet who initiated the snake population monitoring in Chizé. This research was made possible by the financial support of the Conseil Général des Deux-Sèvres, the Région Poitou-Charentes, and the ANR (ECTOCLIM project).

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Correspondence to Hervé Lelièvre.

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Communicated by I. D. Hume.

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Lelièvre, H., Le Hénanff, M., Blouin-Demers, G. et al. Thermal strategies and energetics in two sympatric colubrid snakes with contrasted exposure. J Comp Physiol B 180, 415–425 (2010). https://doi.org/10.1007/s00360-009-0423-8

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  • DOI: https://doi.org/10.1007/s00360-009-0423-8

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