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Thermal ecology of three coexistent desert lizards: Implications for habitat divergence and thermal vulnerability

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Abstract

How ectotherms exploit thermal resources has important implications for their habitat utilization and thermal vulnerability to climate warming. To address this issue, we investigated thermal relations of three sympatric lizard species (Eremias argus, Eremias multiocellata, and Phrynocephalus przewalskii) in the desert steppe of Inner Mongolia, China. We determined the thermoregulatory behavior, body temperature (T b), operative temperature (T e), selected body temperature (T sel), and critical thermal maximum (CTmax) of adult lizards. Based on these physiological parameters, we quantified the accuracy and effectiveness of thermoregulation as well as thermal-safety margin for these species. The three species were accurate and effective thermoregulators. The P. przewalskii preferred open habitats, and had a higher T b than the two Eremias lizards, which preferred shade habitats and shuttled more frequently between the shade and sun. This indicated that the three sympatric lizards have different thermoregulatory behavior and thermal physiology, which might facilitate their coexistence in the desert steppe ecosystem. In addition, the P. przewalskii had higher T sel and CTmax, and a wider thermal-safety margin than the two Eremias lizards, suggesting that the two Eremias lizards would be more vulnerable to climate warming than P. przewalskii.

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References

  • Adolph SC (1990) Influence of behavioral thermoregulation on microhabitat use by two Sceloporus lizards. Ecology 71:315–327

    Article  Google Scholar 

  • Angiletta MJ (2009) Thermal adaptation: a theoretical and empiricial synthesis. Oxford University Press, New York

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet PA, Valladares F, Chown SL (2013) Heat freezes niche evolution. Ecol lett 16:1206–1219

    Article  PubMed  Google Scholar 

  • Bakken GS, Angilletta MJ (2014) How to avoid errors when quantifying thermal environments. Funct Ecol 28(1):96–107

    Article  Google Scholar 

  • Bauwens D, Hertz PE, Castilla AM (1996) Thermoregulation in a lacertid lizard: the relative contributions of distinct behavioral mechanisms. Ecology 77:1818–1830

    Article  Google Scholar 

  • Bauwens D, Castilla AM, Mouton PlFN (1999) Field body temperatures, activity levels and opportunities for thermoregulation in an extreme microhabitat specialist. J Zool 249:11–18

    Article  Google Scholar 

  • Bennett AF (1980) The thermal-dependence of lizard behavior. Anim Behav 28:752–762

    Article  Google Scholar 

  • Bennett AF, Johnalder H (1986) Thermal relations of some Australian skinks (Sauria: Scincidae). Copeia 1986:57–64

    Article  Google Scholar 

  • Besson AA, Cree A (2010) A cold-adapted reptile becomes a more effective thermoregulator in a thermally challenging environment. Oecologia 163:571–581

    Article  PubMed  Google Scholar 

  • Blouin-Demers G, Weatherhead PJ (2001a) An experimental test of the link between foraging, habitat selection and thermoregulation in black rat snakes Elaphe obsoleta obsoleta. J Anim Ecol 70(6):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 82:3025–3043

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bogert CM (1949) Thermoregulation in reptiles, a factor in evolution. Evolution Int J org Evolution 3(3):195–211

    Article  CAS  Google Scholar 

  • Bowker RG (1984) Precision of thermoregulation of some African lizards. Physiol Zool 57:401–412

    Article  Google Scholar 

  • Clusella-Trullas S, Blackburn TM, Chown SL (2011) Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am Nat 177:738–751

    Article  PubMed  Google Scholar 

  • Corbalan V, Debandi G, Kubisch E (2013) Thermal ecology of two sympatric saxicolous lizards of the genus Phymaturus from the Payunia region (Argentina). J Therm Biol 38:384–389

    Article  Google Scholar 

  • Cowles RB, Bogert CM (1944) A preliminary study of the thermal requirements of desert reptiles. Bull Am Mus Nat Hist 83:263–296

    Google Scholar 

  • Daly BG, Dickman CR, Crowther MS (2008) Causes of habitat divergence in two species of agamid lizards in arid central Australia. Ecology 89:65–76

    Article  PubMed  Google Scholar 

  • Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • do Amaral JPS, Marvin GA, Hutchison VH (2002) Thermoregulation in the box turtles Terrapene carolina and Terrapene ornata. Can J Zool 80(5):934–943

    Article  Google Scholar 

  • Du WG, Yan SJ, Ji X (2000) Selected body temperature, thermal tolerance and thermal dependence of food assimilation and locomotor performance in adult blue-tailed skinks, Eumeces elegans. J Therm Biol 25:197–202

    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 84:1300–1306

    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 78:1023–1032

    Article  CAS  PubMed  Google Scholar 

  • Grant BW, Dunham AE (1988) Thermally imposed time constraints on the activity of the desert lizard Sceloporus merriami. Ecology 69:167–176

    Article  Google Scholar 

  • Grigg JW, Buckley LB (2013) Conservatism of lizard thermal tolerances and body temperatures across evolutionary history and geography. Biol Lett 9:20121056

    Article  PubMed  PubMed Central  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 

  • Gunderson AR, Stillman JH (2015) Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc R Soc B 282(1808):20150401

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo X, Wang Y (2007) Partitioned Bayesian analyses, dispersal–vicariance analysis, and the biogeography of Chinese toad-headed lizards (Agamidae: Phrynocephalus): a re-evaluation. Mol Phylogenet Evol 45:643–662

    Article  CAS  PubMed  Google Scholar 

  • Heatwole H (1970) Thermal ecology of the desert dragon Amphibolurus inermis. Ecol Monogr 40:425–457

    Article  Google Scholar 

  • Hertz PE (1992a) Evaluating thermal resource partitioning by sympatric lizards Anolis cooki and A. cristatellus: a field test using null hypotheses. Oecologia 90:127–136

    Article  CAS  PubMed  Google Scholar 

  • Hertz PE (1992b) Temperature regulation in Puerto Rican Anolis lizard: A field test using null hypotheses. Ecology 73:1405–1417

    Article  Google Scholar 

  • Hertz PE, Huey RB, Nevo E (1983) Homage to Santa-Anita—thermal sensitivity of sprint speed in Agamid lizards. Evol Int J org Evolution 37:1075–1084

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hertz PE, Arima Y, Harrison A, Huey RB, Losos JB, Glor RE (2013) Asynchronous evolution of physiology and morphology in Anolis lizards. Evolution Int J org Evol 67:2101–2113

    Article  Google Scholar 

  • Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of reptilia, vol 12. Academic, London, pp 25–91

    Google Scholar 

  • Huey RB, Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae: Mabuya). Ecology 58:119–128

    Article  Google Scholar 

  • Huey RB, Tewksbury JJ (2009) Can behavior douse the fire of climate warming? Proc Natl Acad Sci USA 106:3647–3648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huey RB, Pianka ER, Egan ME, Coons LW (1974) Ecological shifts in sympatry—Kalahari fossorial lizards (Typhlosaurus). Ecology 55:304–316

    Article  Google Scholar 

  • Huey RB, Pianka ER, Hoffman JA (1977) Seasonal variation in thermoregulatory behavior and body temperature of diurnal Kalahari lizards. Ecology 58:1066–1075

    Article  Google Scholar 

  • Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Alvarez Perez HJ, Garland T Jr (2009) Why tropical forest lizards are vulnerable to climate warming. Proc R Soc B 276:1939–1948

    Article  PubMed  PubMed Central  Google Scholar 

  • Huey RB, Kearney MR, Krockenberger A, Holtum JA, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc Lond B Biol Sci 367:1665–1679

    Article  PubMed  PubMed Central  Google Scholar 

  • Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc Natl Acad Sci USA 106:3835–3840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lara-Resendiz RA, Gadsden H, Rosen PC, Sinervo B, Mendez-De La Cruz FR (2015) Thermoregulation of two sympatric species of horned lizards in the Chihuahuan Desert and their local extinction risk. J Therm Biol 48:1–10

    Article  PubMed  Google Scholar 

  • Lelievre H, Blouin-Demers G, Pinaud D, Lisse H, Bonnet X, Lourdais O (2011) Contrasted thermal preferences translate into divergences in habitat use and realized performance in two sympatric snakes. J Zool 284:265–275

    Article  Google Scholar 

  • Li H, Wang Z, Mei W, Ji X (2009) Temperature acclimation affects thermal preference and tolerance in three Eremias lizards. Curr Zool 55:258–265

    Google Scholar 

  • Lixia W, Shihong S, Yuanting J, Yongfeng Y, Naifa L (2007) Molecular phylogeography of the Chinese lacertids of the genus Eremias (Lacertidae) based on 16 S rRNA mitochondrial DNA sequences. Amphibia-Reptilia 28:33–41

    Article  Google Scholar 

  • Lopez P, Martin J (2013) Effects of microhabitat-dependent predation risk on vigilance during intermittent locomotion in Psammodromus algirus Lizards. Ethology 119(4):316–324

    Article  Google Scholar 

  • Luo LG, Qu YF, Ji X (2005) Thermal dependence of food assimilation and sprint speed in a lacertid lizard (Eremias argus) from northern China. Dong wu xue bao.[Acta zoologica Sinica] 52:256–262

    Google Scholar 

  • Magnuson JJ, Crowder LB, Medvick PA (1979) Temperature as an ecological resource. Am Zool 19:331–343

    Article  Google Scholar 

  • Martinvallejo J, Garciafernandez J, Perezmellado V, Vicentevillardon JL (1995) Habitat selection and thermal ecology of the sympatric lizards Podarcis muralis and Podarcis hispanica in a mountain region of central spain. Herpetol J 5(1):181–188

    Google Scholar 

  • Melville J, Schulte JA (2001) Correlates of active body temperatures and microhabitat occupation in nine species of central Australian agamid lizards. Austral Ecol 26:660–669

    Article  Google Scholar 

  • Middleton N, Thomas D (1997) World atlas of desertification, 2nd edn. Arnold, London

    Google Scholar 

  • Pachauri RK et al (2014) Climate change 2014: Synthesis report. Contribution of working groups I, II and III to the fifth assessment report. Intergovernmental Panel on Climate Change, Geneva, Switzerland

  • Pianka ER (1971) Comparative ecology of two lizards. Copeia 1971:129–138

    Article  Google Scholar 

  • Pianka ER (1986) Ecology and natural history of desert lizards: analyses of the ecological niche and community structure. Princeton University Press, Princeton

    Book  Google Scholar 

  • Pianka ER (1989) Desert lizard diversity: additional comments and some data. Am Nat 134(3):344–364

    Article  Google Scholar 

  • Qu YF, Li H, Gao JF, Xu XF, Ji X (2011) Thermal preference, thermal tolerance and the thermal dependence of digestive performance in two coexisting Phrynocephalus lizards. Curr Zool 57:684–700

    Article  Google Scholar 

  • Rocha CFD, Vrcibradic D (1996) Thermal ecology of two sympatric skinks (Mabuya macrorhyncha and Mabuya agilis) in a Brazilian restinga habitat. Aust J Ecol 21(1):110–113

    Article  Google Scholar 

  • Row JR, Blouin-Demers G (2006) Thermal quality influences effectiveness of thermoregulation, habitat use, and behaviour in milk snakes. Oecologia 148:1–11

    Article  PubMed  Google Scholar 

  • Ruibal R (1960) Thermal relations of five species of tropical lizards. Evol Int J org Evol 15:98–111

    Article  Google Scholar 

  • Rummel JD, Roughgarden J (1985) Effects of reduced perch-height separation on competition between two Anolis lizards. Ecology 66(2):430–444

    Article  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 132:323–331

    Article  PubMed  Google Scholar 

  • Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39

    Article  CAS  PubMed  Google Scholar 

  • Sears MW, Angilletta MJ (2015) Costs and benefits of thermoregulation revisited: both the heterogeneity and spatial structure of temperature drive energetic costs. Am Nat 185:E94–E102

    Article  PubMed  Google Scholar 

  • Sears MW, Angilletta MJ Jr, Schuler MS, Borchert J, Dilliplane KF, Stegman M, Rusch TW, Mitchell WA (2016) Configuration of the thermal landscape determines thermoregulatory performance of ectotherms. Proc Natl Acad Sci USA 113:10595–11060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen JW, Pike DA, Du WG (2010) Movements and microhabitat use of translocated big-headed turtles (Platysternon megacephalum) in southern China. Chel Cons Biol 9:154–161

    Article  Google Scholar 

  • Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, Huey RB (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Natl Acad Sci USA 111:5610–5615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang XL, Yue F, He JZ, Wang NB, Ma M, Mo JR, Chen Q (2013) Ontogenetic and sexual differences of thermal biology and locomotor performance in a lacertid lizard, Eremias multiocellata. Zoology 116:331–335

    Article  PubMed  Google Scholar 

  • Vandamme R, Bauwens D, Verheyen RF (1991) The thermal dependence of feeding behavior, food consumption and gut passage time in the lizard Lacerta vivipara Jacquin. Funct Ecol 5:507–517

    Article  Google Scholar 

  • Wang Y, Zeng ZG, Li SR, Bi JH, Du WG (2016) Low precipitation aggravates the impact of extreme high temperatures on lizard reproduction. Oecologia 182:961–971

    Article  PubMed  Google Scholar 

  • Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644

    Article  PubMed  Google Scholar 

  • Zeng ZG Bi JH, Li SR, Wang Y, Robbins TR, Chen SY, Du WG (2016) Habitat alteration influences a desert steppe lizard community: implications of species-specific preferences and performance. Herpetol Monogr 30:34–48

    Article  Google Scholar 

  • Zhao KT (1999) Lacertidae. In: Zhao EM, Zhou KY (eds) Sinica Fauna, Reptilia (Squamata: Lacertilia). Science, Beijing, pp 219–242

    Google Scholar 

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Acknowledgements

We thank Peng Cao and Shao-Yong Chen for assistance in the field. We are grateful to the staffs at Shierliancheng Field Station, Institute of Grassland Research of the Chinese Academy of Agricultural Sciences for logistic support. Funding was supported by the National Key Research and Development Program of China (2016YFC0503200).

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Authors and Affiliations

  1. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China

    Shu-Ran Li, Yang Wang, Liang Ma, Zhi-Gao Zeng & Wei-Guo Du

  2. University of Chinese Academy of Sciences, Beijing, People’s Republic of China

    Shu-Ran Li, Yang Wang & Liang Ma

  3. College of Life Sciences, Inner Mongolia Normal University, Hohhot, 010022, Inner Mongolia, People’s Republic of China

    Jun-Huai Bi

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  1. Shu-Ran Li
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  2. Yang Wang
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Correspondence to Wei-Guo Du.

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Research was performed under approvals from the Animal Ethics Committee at the Institute of Zoology, Chinese Academy of Sciences (IOZ14001).

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Communicated by G. Heldmaier.

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Li, SR., Wang, Y., Ma, L. et al. Thermal ecology of three coexistent desert lizards: Implications for habitat divergence and thermal vulnerability. J Comp Physiol B 187, 1009–1018 (2017). https://doi.org/10.1007/s00360-017-1087-4

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  • DOI: https://doi.org/10.1007/s00360-017-1087-4

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