Skip to main content

Are viviparous lizards more vulnerable to climate warming because they have evolved reduced body temperature and heat tolerance?

Abstract

Lizards may experience population declines and extinctions on a similar scale to that experienced by amphibians, and climate warming is one hypothesis proposed to explain these declines and extinctions. Within lizards, viviparous species are hypothesized to be more vulnerable to climate warming, because they have evolved reduced body temperature and heat tolerance, but this idea remains untested. To test this hypothesis, we conducted three temperatures (20, 24, and 28 °C) × two species [Phrynocephalus przewalskii (oviparous) and P. putjatia (viviparous)] factorial design experiment that simulated warming on oviparous versus viviparous lizards. Our manipulation of ambient temperature affected activity and thermal preference in both species, birth date in P. putjatia, and egg mass in P. przewalskii; other examined traits (fecundity, reproductive output, and size, morphology, and sprint speed of offspring) were not affected. Neither in P. putjatia nor in P. przewalskii behavioral responses to rising temperatures differ between the sexes. The viviparous species thermoregulated more actively than did the oviparous species, but the two species did not differ in thermal preference. Warming reduced the activity time allotted for thermoregulation in both species, but the effect was more dramatic in the viviparous species. Our data support one of the central predictions that lead to the hypothesis that viviparous lizards are more vulnerable to climate warming; however, this is not because viviparous lizards have evolved reduced body temperature and heat tolerance, but, because warming constrains activity more dramatically in viviparous species.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Andrews RM, Mathies T (2000) Natural history of reptilian development: constraints on the evolution of viviparity. Bioscience 50:227–238

    Article  Google Scholar 

  2. Angilletta MJ Jr, Hill T, Robson MA (2002a) Is physiological performance optimized by thermoregulatory behavior?: a case study of the eastern fence lizard, Sceloporus undulatus. J Therm Biol 27:199–204

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. Barabanov AV, Ananjeva NB (2007) Catalogue of the available scientific species group names for lizards of the genus Phrynocephalus Kaup, 1825 (Reptilia, Sauria, Agamidae). Zootaxa 1399:1–57

    Article  Google Scholar 

  6. Bauwens D, Thoen C (1981) Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara. J Anim Ecol 50:733–743

    Article  Google Scholar 

  7. Bennett AF, John-Alder HB (1986) Thermal relations of some Australian skinks (Sauria: Scincidae). Copeia 1986:57–64

    Article  Google Scholar 

  8. Beuchat CA (1988) Temperature effects during gestation in a viviparous lizard. J Therm Biol 13:135–142

    Article  Google Scholar 

  9. Bickford D, Howard SD, Ng DJJ, Jennifer A (2010) Impacts of climate change on the amphibians and reptiles of Southeast Asia. Biodivers Conserv 19:1043–1062

    Article  Google Scholar 

  10. Blackburn DG (2000) Reptilian viviparity: past research, future directions, and appropriate models. Comp Biochem Physiol A 127:391–409

    CAS  Article  Google Scholar 

  11. Braña F (1993) Shifts in body temperature and escape behaviour of female Podarcis muralis during pregnancy. Oikos 66:216–222

    Article  Google Scholar 

  12. Cadby CD, While GM, Hobday AJ, Uller T, Erik Wapstra E (2010) Multi-scale approach to understanding climate effects on offspring size at birth and date of birth in a reptile. Integr Zool 5:164–175

    Article  PubMed  Google Scholar 

  13. Carey C (2009) The impacts of climate change on the annual cycles of birds. Phil Trans R Soc B 364:3321–3330

    Article  PubMed  PubMed Central  Google Scholar 

  14. Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Divers Distrib 9:111–121

    Article  Google Scholar 

  15. 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 

  16. Clusella-Trullas S, Chown SL (2011) Comment on ‘‘Erosion of lizard diversity by climate change and altered thermal niches’’. Science 332:537

    Article  PubMed  Google Scholar 

  17. Clusella-Trullas S, Chown SL (2014) Lizard thermal trait variation at multiple scales: a review. J Comp Physiol B 184:5–21

    Article  PubMed  Google Scholar 

  18. Congdon JD, Dunham AE, Tinkle DW (1982) Energy budgets and life histories of reptiles. In: Gans C, Pough FH (eds) Biology of reptilia, vol 13. Academic, London, pp 233–271

    Google Scholar 

  19. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Dubois Y, Blouin-Demers G, Thomas D (2008) Temperature selection in wood turtles (Glyptemys insculpta) and its implications for energetics. Ecoscience 15:398–406

    Article  Google Scholar 

  21. Dufaure JP, Hubert J (1961) Table de développement du lézard vivipare: Lacerta (Zootoca) vivipara Jacquin. Arch Anat Micr Morph Exp 50:309–328

    Google Scholar 

  22. Feldman A, Bauer AM, Castro-Herrera F, Chirio L, Das I, Doan TM, Maza E, Meirte D, de Campos Nogueira C, Nagy ZT, Torres-Carvajal O, Uetz P, Meiri S (2015) The geography of snake reproductive mode: a global analysis of the evolution of snake viviparity. Glob Ecol Biogeogr 24:1433–1442

    Article  Google Scholar 

  23. Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjà vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  24. Grant BW, Dunham AE (1990) Elevational covariation in environmental constraints and life histories of the desert lizard Sceloporus merriami. Ecology 71:1765–1776

    Article  Google Scholar 

  25. Guo XG, Wang YZ (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

    CAS  Article  PubMed  Google Scholar 

  26. Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of reptilia, vol 13. Academic, London, pp 25–91

    Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Pérez HJÁ, 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 

  29. Huey RB, Losos JB, Moritz C (2010) Are lizards toast? Science 328:832–833

    CAS  Article  PubMed  Google Scholar 

  30. Hutchison VH (1976) Factors influencing thermal tolerances of individual organisms. In: Esch GW, McFarlane RW (eds) Thermal ecology 11. Proceedings of the 2nd SREL thermal ecology symposium. US National Technical Information Service, Oak Ridge, TN, pp 10–26

  31. Ji X, Lin LH, Luo LG, Lu HL, Gao JF, Han J (2006) Gestation temperature affects sexual phenotype, morphology, locomotor performance and growth of neonatal brown forest skink, Sphenomorphus indicus. Biol J Linn Soc 88:453–463

    Article  Google Scholar 

  32. Ji X, Lin CX, Lin LH, Qiu QB, Du Y (2007) Evolution of viviparity in warm-climate lizards: an experimental test of the maternal manipulation hypothesis. J Evol Biol 20:1037–1045

    CAS  Article  PubMed  Google Scholar 

  33. Ji X, Wang YZ, Wang Z (2009) New species of Phrynocephalus (Squamata, Agamidae) from Qinghai, Northwest China. Zootaxa 1988:61–68

    Google Scholar 

  34. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Kubička L, Kratochvíl L (2009) First growth, 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 

  36. Lambert SM, Wiens JJ (2013) Evolution of viviparity: a phylogenetic test of the cold-climate hypothesis in Phrynosomatid lizards. Evolution 67:2614–2630

    Article  PubMed  Google Scholar 

  37. Li H, Qu YF, Hu RB, Ji X (2009a) Evolution of viviparity in cold-climate lizards: testing the maternal manipulation hypothesis. Evol Ecol 23:777–790

    Article  Google Scholar 

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

    Google Scholar 

  39. Li H, Zhou ZS, Wu T, Wu YQ, Ji X (2013) Do fluctuations in incubation temperature affect hatchling quality in the Chinese soft-shelled turtle Pelodiscus sinensis? Aquaculture 406–407:91–96

    Article  Google Scholar 

  40. Lucas A (1996) Bioenergetics of aquatic animals. Taylor and Francis Ltd, London

    Google Scholar 

  41. Luo LG, Ding GH, Ji X (2010) Income breeding and temperature-induced plasticity in reproductive traits in lizards. J Exp Biol 213:2073–2078

    Article  PubMed  Google Scholar 

  42. Lynch VJ (2009) Live-birth in vipers (Viperidae) is a key innovation and adaptation to global cooling during the Cenozoic. Evolution 63:2457–2465

    Article  PubMed  Google Scholar 

  43. Martin TL, Huey RB (2008) Why suboptimal is optimal: Jensen’s inequality and ectotherm thermal preferences. Am Nat 171:E102–E118

    Article  PubMed  Google Scholar 

  44. Mathies T, Andrews RM (1997) Influence of pregnancy on thermal biology of the lizard, Sceloporus jarrovi: why do pregnant females exhibit low body temperatures? Funct Ecol 11:498–507

    Article  Google Scholar 

  45. McNab BK (2002) The physiological ecology of vertebrates: a view from energetics, vol 1. Comstock, Cornell

    Google Scholar 

  46. Miles DB, Sinervo B, Frankino WA (2000) Reproductive burden, locomotor performance, and the cost of reproduction in free ranging lizards. Evolution 54:1386–1395

    CAS  Article  PubMed  Google Scholar 

  47. 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 

  48. Noble D, Qi Y, Fu JZ (2010) Species delineation using Bayesian model-based assignment tests: a case study using Chinese toad-headed agamas (genus Phrynocephalus). BMC Evol Biol 10:197

    Article  PubMed  PubMed Central  Google Scholar 

  49. Pang JF, Wang YZ, Zhong Y, Hoelzel AR, Papenfuss TJ, Zeng XM, Ananjeva NB, Zhang YP (2003) A phylogeny of Chinese species in the genus Phrynocephalus (Agamidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 27:398–409

    CAS  Article  PubMed  Google Scholar 

  50. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  51. Patterson JW (1991) Emergence, basking behaviour, mean selected temperature and critical thermal minimum in high and low altitude subspecies of the tropical lizard Mabuya striata. Afr J Ecol 37:330–339

    Article  Google Scholar 

  52. Pincheira-Donoso D, Tregenza T, Witt MJ, Hodgson DJ (2013) The evolution of viviparity opens opportunities for lizard radiation but drives it into a climatic cul-de-sac. Global Ecol Biogeogr 22:857–867

    Article  Google Scholar 

  53. Porter WP, Tracy CR (1983) Biophysical analyses of energetics, time-space utilization, and distributional limits. In: Huey RB, Pianka ER, Schoener TW (eds) Lizard ecology: studies of a model organism. Harvard University Press, Cambridge, pp 55–83

    Google Scholar 

  54. Post E, Pedersen C, Wilmers CC, Forchhammer MC (2008) Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proc R Soc B 275:2005–2013

    Article  PubMed  PubMed Central  Google Scholar 

  55. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sánchez-Azofeifa GA, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167

    CAS  Article  PubMed  Google Scholar 

  56. Pyron RA, Burbrink FT (2014) Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecol Lett 17:13–21

    Article  PubMed  Google Scholar 

  57. Qu YF, Li H, Gao JF, Ji X (2011a) Embryonic thermosensitivity and hatchling morphology differ between two coexisting lizards. Acta Oecol 37:375–380

    Article  Google Scholar 

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

    Article  Google Scholar 

  59. Qualls CP, Andrews RM (1999) Maternal body volume constrains water uptake by lizard eggs in utero. Funct Ecol 13:845–851

    Article  Google Scholar 

  60. Qualls CP, Shine R (1995) Maternal body-volume as a constraint on reproductive output in lizards: evidence from the evolution of viviparity. Oecologia 103:73–78

    Article  PubMed  Google Scholar 

  61. Shine R (1985) The evolution of viviparity in reptiles: an ecological analysis. In: Gans C, Billet F (eds) Biology of the reptilia, vol 15. Wiley, New York, pp 605–694

    Google Scholar 

  62. Shine R (1992) Relative clutch mass and body shape in lizards and snakes: is reproductive investment constrained or optimized? Evolution 46:828–833

    Article  PubMed  Google Scholar 

  63. Shu L, Zhang QL, Qu YF, Ji X (2010) Thermal tolerance, selected body temperature and thermal dependence of food assimilation and locomotor performance in the Qinghai toad-headed lizard Phrynocephalus vlanglii. Acta Ecol Sin 30:2036–2042

    Google Scholar 

  64. Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Cruz MVS, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Avila LJ, Morando M, De la Riva IJ, Sepulveda PV, Rocha CFD, Ibargüengoytía 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 328:894–899

    CAS  Article  PubMed  Google Scholar 

  65. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    CAS  Article  PubMed  Google Scholar 

  66. Tang XL, Yue F, Ma M, Wang NB, He JZ, Chen Q (2012) Effects of thermal and hydric conditions on egg incubation and hatchling phenotypes in two Phrynocephalus lizards. Asian Herpetol Res 3:184–191

    Article  Google Scholar 

  67. Telemeco RS, Elphick MJ, Shine R (2009) Nesting lizards (Bassiana duperreyi) compensate partly, but not completely, for climate change. Ecology 90:17–21

    Article  PubMed  Google Scholar 

  68. Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297

    CAS  Article  PubMed  Google Scholar 

  69. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, Ferreira de Siqueira M, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148

    CAS  Article  PubMed  Google Scholar 

  70. Tinkle DW, Gibbons JW (1977) The distribution and evolution of viviparity in reptiles. Misc Publ Univ Mich Mus Zool 154:1–55

    Google Scholar 

  71. Urban MC, Richardson JL, Freidenfelds NA (2014) Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change. Evol Appl 7:88–103

    Article  PubMed  Google Scholar 

  72. Visser ME, Both C, Lambrechts MM (2004) Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35:89–110

    Article  Google Scholar 

  73. Wang YZ, Zeng XM, Fang ZL, Wu GF, Liu ZJ, Papenfuss TJ, Macey JR (2002) A valid species of the genus Phrynocephalus: P. putjatia and a discussion on taxonomy of Phrynocephalus hongyuanensis (Sauria: Agamidae). Acta Zootax Sin 27:372–383

    Google Scholar 

  74. Wang Z, Lu HL, Ma L, Ji X (2013a) Differences in thermal preference and tolerance among three Phrynocephalus lizards (Agamidae) with different body sizes and habitat use. Asian Herpetol Res 4:214–220

    Article  Google Scholar 

  75. Wang Z, Ma L, Shao M, Ji X (2013b) Differences in incubation length and hatchling morphology among five oviparous Phrynocephalus lizards (Agamidae) from China. Asian Herpetol Res 4:225–232

    Google Scholar 

  76. Wang Z, Lu HL, Ma L, Ji X (2014) Viviparity in high-altitude Phrynocephalus lizards is adaptive because embryos cannot fully develop without maternal thermoregulation. Oecologia 174:639–649

    Article  PubMed  Google Scholar 

  77. Watson CM, Makowsky R, Bagley JC (2014) Reproductive mode evolution in lizards revisited: updated analyses examining geographic, climatic and phylogenetic effects support the cold-climate hypothesis. J Evol Biol 27:2767–2780

    CAS  Article  PubMed  Google Scholar 

  78. Yang J, Sun YY, An H, Ji X (2008) Northern grass lizards (Takydromus septentrionalis) from different populations do not differ in thermal preference and thermal tolerance when acclimated under identical thermal conditions. J Comp Physiol B 178:343–349

    Article  PubMed  Google Scholar 

  79. Zhao KT (1999) Phrynocephalus przewalskii Strauch, 1876. In: Zhao EM, Zhao KT, Zhou KY (eds) Fauna Sinica, Reptilia, vol 2. Science, Beijing, pp 182–184

    Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Natural Science Foundation of China (Projects 31672277, 31470471, 31200282 and 31071910) and the Priority Academic Program Development of Jiangsu Higher Education Institutions. We thank Ce Chen, Ya-Qing Liu, and Zhu-Yuan Zhang for help during this research.

Author information

Affiliations

Authors

Contributions

ZW and XJ conceived and designed the experiments. ZW, LM, and MS performed the experiments. ZW, LM, and XJ analyzed the data. ZW and XJ wrote the manuscript; LM and MS provided editorial advice.

Corresponding author

Correspondence to Xiang Ji.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All experimental procedures complied with the current laws on animal welfare and research in China, and were approved by the Animal Research Ethics Committee of Nanjing Normal University (AREC2010-05-006).

Additional information

Communicated by Raoul Van Damme.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 259 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, Z., Ma, L., Shao, M. et al. Are viviparous lizards more vulnerable to climate warming because they have evolved reduced body temperature and heat tolerance?. Oecologia 185, 573–582 (2017). https://doi.org/10.1007/s00442-017-3979-0

Download citation

Keywords

  • Climate warming
  • Extinction risk
  • Lizards
  • Reproductive mode
  • Reproductive trait