Are lizards sensitive to anomalous seasonal temperatures? Long-term thermobiological variability in a subtropical species

Autoři: André Vicente Liz aff001;  Vinicius Santos aff001;  Talita Ribeiro aff002;  Murilo Guimarães aff001;  Laura Verrastro aff001
Působiště autorů: Programa de Pós–Graduação em Biologia Animal, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil aff001;  Programa de Pós–Graduação em Ecologia, Departamento de Ecologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226399


Alterations in thermal niches have been widely associated with the Anthropocene erosion of reptiles’ diversity. They entail potential physiological constraints for organisms’ performance, which can lead to activity restrictions and impact fitness and demography. Reptiles are ectotherms which rely on seasonal periodicity to maximize the performance of biological functions. Despite it, the ecological implications of shifts in local temperatures are barely explored at the seasonal scale. This study aims to assess how changes in air temperature and substrate temperature affect the activity, body temperature (Tb) and thermoregulation patterns of the sand lizard, Liolaemus arambarensis (an endangered, microendemic species from southern Brazil), throughout a four-year period. Field surveys were conducted monthly on a restricted population in a sand-dune habitat. The annual fluctuations of the seasonal temperatures led to significant changes in the activity and Tb of L. arambarensis and shaped thermoregulation trends, suggesting biological plasticity as a key factor in the face of such variability. Lizards tended to maintain seasonal Tb in mild and harsh seasons through increased warming/cooling efforts. Anomalous winter conditions seemed especially critical for individual performance due to their apparent high impact favouring/constraining activity. Activity and thermoregulation were inhibited in frigid winters, probably due to a vulnerable physiology to intense cold spells determined by higher preferred body temperatures than Tb. Our results warn of a complex sensitivity in lizards to anomalous seasonal temperatures, which are potentially enhanced by climate change. The current work highlights the importance of multiannual biomonitoring to disentangle long-term responses in the thermal biology of reptiles and, thereby, to integrate conservation needs in the scope of global change.

Klíčová slova:

Body temperature – Foraging – Lizards – Reptiles – Seasons – Spring – Winter – Reptile biology


1. Gibbons J, Scott D, Ryan TJ, Buhlmann K, Tuberville T, Metts B, et al. The Global Decline of Reptiles, Déjà Vu Amphibians. Bioscience. 2000;50: 653–666. doi: 10.1641/0006-3568(2000)050[0653:TGDORD]2.0.CO;2

2. Whitfield SM, Bell KE, Philippi T, Sasa M, Bolaños F, Chaves G, et al. Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proc Natl Acad Sci. 2007;104: 8352–8356. doi: 10.1073/pnas.0611256104 17449638

3. Angilletta MJ Jr.. Thermal Adaptation. Oxford University Press; 2009.

4. Huey RB. Temperature, Physiology, and the Ecology of Reptiles. In: C G, FH P, editors. Biology of the Reptilia, Vol 12, Physiology (C). Academic Press; 1982. pp. 25–91.

5. Fitzgerald LA, Walkup D, Chyn K, Buchholtz E, Angeli N, Parker M. The Future for Reptiles: Advances and Challenges in the Anthropocene. Encyclopedia of the Anthropocene. Elsevier Inc.; 2018.

6. Powers RP, Jetz W. Global habitat loss and extinction risk of terrestrial vertebrates under future land-use-change scenarios. Nat Clim Chang. Springer US; 2019;9: 323–329. doi: 10.1038/s41558-019-0406-z

7. Adolph SC, Porter WP. Temperature, Activity, and Lizard Life Histories. Am Nat. 1993;142: 273–295. doi: 10.1086/285538 19425979

8. Bestion E, Teyssier A, Richard M, Clobert J, Cote J. Live Fast, Die Young: Experimental Evidence of Population Extinction Risk due to Climate Change. PLoS Biol. 2015;13: 1–19. doi: 10.1371/journal.pbio.1002281 26501958

9. Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE. Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc B Biol Sci. 2012;367: 1665–1679. doi: 10.1098/rstb.2012.0005 22566674

10. Piantoni C, Navas CA, Ibargüengoytía NR. A real tale of Godzilla: impact of climate warming on the growth of a lizard. Biol J Linn Soc. 2019;126: 768–782. doi: 10.1093/biolinnean/bly216

11. Rutschmann A, Miles DB, Le Galliard JF, Richard M, Moulherat S, Sinervo B, et al. Climate and habitat interact to shape the thermal reaction norms of breeding phenology across lizard populations. J Anim Ecol. 2016;85: 457–466. doi: 10.1111/1365-2656.12473 26589962

12. Böhm M, Collen B, Baillie JEM, Bowles P, Chanson J, Cox N, et al. The conservation status of the world’s reptiles. Biol Conserv. 2013;157: 372–385. doi: 10.1016/j.biocon.2012.07.015

13. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, et al. Extinction risk from climate change. Nature. 2004;427: 145–148. doi: 10.1038/nature02121 14712274

14. Sinervo B, Mendez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagran-Santa Cruz M, et al. Erosion of Lizard Diversity by Climate Change and Altered Thermal Niches. Science (80). 2010;328: 894–899. doi: 10.1126/science.1184695 20466932

15. Diele-Viegas LM, Rocha CFD. Unraveling the influences of climate change in Lepidosauria (Reptilia). Journal of Thermal Biology. Elsevier Ltd; 2018. pp. 401–414.

16. Maxwell SL, Butt N, Maron M, McAlpine CA, Chapman S, Ullmann A, et al. Conservation implications of ecological responses to extreme weather and climate events. Divers Distrib. 2018;25: 613–625. doi: 10.1111/ddi.12878

17. Meiri S, Bauer AM, Chirio L, Colli GR, Das I, Doan TM, et al. Are lizards feeling the heat? A tale of ecology and evolution under two temperatures. Glob Ecol Biogeogr. 2013;22: 834–845. doi: 10.1111/geb.12053

18. Kirchhof S, Hetem RS, Lease HM, Miles DB, Mitchell D, Müller J, et al. Thermoregulatory behavior and high thermal preference buffer impact of climate change in a Namib Desert lizard. Ecosphere. 2017;8: e02033. doi: 10.1002/ecs2.2033

19. Ortega Z, Mencía A, Pérez-Mellado V. Behavioral buffering of global warming in a cold-adapted lizard. Ecol Evol. 2016;6: 4582–4590. doi: 10.1002/ece3.2216 27386098

20. Garcia RA, Cabeza M, Rahbek C, Araujo MB. Multiple Dimensions of Climate Change and Their Implications for Biodiversity. Science. 2014;344: 1247579–1247579. doi: 10.1126/science.1247579 24786084

21. Ummenhofer CC, Meehl GA. Extreme weather and climate events with ecological relevance: a review. Philos Trans R Soc B Biol Sci. 2017;372: 20160135. doi: 10.1098/rstb.2016.0135 28483866

22. Cohen J, Pfeiffer K, Francis JA. Warm Arctic episodes linked with increased frequency of extreme winter weather in the United States. Nat Commun. Springer US; 2018;9: 1–12. doi: 10.1038/s41467-018-02992-9 29535297

23. Santer BD, Po-Chedley S, Zelinka MD, Cvijanovic I, Bonfils C, Durack PJ, et al. Human influence on the seasonal cycle of tropospheric temperature. Science. 2018;361: eaas8806. doi: 10.1126/science.aas8806 30026201

24. Wallace JM, Held IM, Thompson DWJ, Trenberth KE, Walsh JE. Global Warming and Winter Weather. Science. 2014;343: 729–730. doi: 10.1126/science.343.6172.729 24531953

25. IPCC. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker, T.F., D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia VB and PMM, editor. Cambridge, United Kingdom and New York: Cambridge University Press; 2013.

26. Díaz JA, Iraeta P, Monasterio C. Seasonality provokes a shift of thermal preferences in a temperate lizard, but altitude does not. J Therm Biol. 2006;31: 237–242. doi: 10.1016/j.jtherbio.2005.10.001

27. Huey RB, Pianka ER. Seasonal Variation in Thermoregulatory Behavior and Body Temperature of Diurnal Kalahari Lizards. Ecology. 1977;58: 1066–1075. doi: 10.2307/1936926

28. Ortega Z, Pérez-Mellado V. Seasonal patterns of body temperature and microhabitat selection in a lacertid lizard. Acta Oecologica. 2016;77: 201–206. doi: 10.1016/j.actao.2016.08.006

29. Kubisch EL, Corbalán V, Ibargüengoytía NR, Sinervo B. Local extinction risk of three species of lizard from Patagonia as a result of global warming. Can J Zool. 2015;94: 49–59. doi: 10.1139/cjz-2015-0024

30. Vicenzi N, Corbalán V, Miles D, Sinervo B, Ibargüengoytía N. Range increment or range detriment? Predicting potential changes in distribution caused by climate change for the endemic high-Andean lizard Phymaturus palluma. Biol Conserv. Elsevier Ltd; 2017;206: 151–160. doi: 10.1016/j.biocon.2016.12.030

31. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, et al. Ecological responses to recent climate change. Nature. 2002;416: 389–395. doi: 10.1038/416389a 11919621

32. Huey RB, Losos JB, Moritz C. Are Lizards Toast? Science. 2010;328: 832–833. doi: 10.1126/science.1190374 20466909

33. Zani PA, Rollyson ME. The Effects of Climate Modes on Growing-Season Length and Timing of Reproduction in the Pacific Northwest as Revealed by Biophysical Modeling of Lizards. Am Midl Nat. 2011;165: 372–388. doi: 10.1674/0003-0031-165.2.372

34. Berriozabal-Islas C, Rodrigues JFM, Ramírez-Bautista A, Becerra-López JL, Nieto-Montes de Oca A. Effect of climate change in lizards of the genus Xenosaurus (Xenosauridae) based on projected changes in climatic suitability and climatic niche conservatism. Ecol Evol. 2018;8: 6860–6871. doi: 10.1002/ece3.4200 30073050

35. Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Pérez HJÁ, et al. Why tropical forest lizards are vulnerable to climate warming. Proc R Soc B Biol Sci. 2009;276: 1939–1948. doi: 10.1098/rspb.2008.1957 19324762

36. Roll U, Feldman A, Novosolov M, Allison A, Bauer AM, Bernard R, et al. The global distribution of tetrapods reveals a need for targeted reptile conservation. Nat Ecol Evol. 2017;1: 1677–1682. doi: 10.1038/s41559-017-0332-2 28993667

37. Sears MW, Angilletta MJ, Schuler MS, Borchert J, Dilliplane KF, Stegman M, et al. Configuration of the thermal landscape determines thermoregulatory performance of ectotherms. Proc Natl Acad Sci. 2016;113: 10595–10600. doi: 10.1073/pnas.1604824113 27601639

38. Huey RB. Behavioral thermoregulation in lizards: importance of associated costs. Science. 1974;184: 1001–1003. doi: 10.1126/science.184.4140.1001 4826166

39. Huey RB, Slatkin M. Cost and Benefits of Lizard Thermoregulation. Q Rev Biol. 1976;51: 363–384. doi: 10.1086/409470 981504

40. Tan WC, Schwanz LE. Thermoregulation across thermal environments in a nocturnal gecko. J Zool. 2015;296: 208–216. doi: 10.1111/jzo.12235

41. Bonino MF, Moreno Azócar DL, Schulte JA, Abdala CS, Cruz FB. Thermal sensitivity of cold climate lizards and the importance of distributional ranges. Zoology. Elsevier GmbH.; 2015;118: 281–290.

42. Uetz, P., Freed, P., Hošek J. The Reptile Database [Internet]. 2018 [cited 30 May 2019].

43. Labra A, Pienaar J, Hansen TF. Evolution of Thermal Physiology in Liolaemus Lizards: Adaptation, Phylogenetic Inertia, and Niche Tracking. Am Nat. 2009;174: 204–220. doi: 10.1086/600088 19538089

44. Medina M, Scolaro A, Méndez-De la Cruz F, Sinervo B, Miles DB, Ibargüengoytía N. Thermal biology of genus Liolaemus: A phylogenetic approach reveals advantages of the genus to survive climate change. J Therm Biol. 2012;37: 579–586. doi: 10.1016/j.jtherbio.2012.06.006

45. Rodríguez-Serrano E, Navas CA, Bozinovic F. The comparative field body temperature among Liolaemus lizards: Testing the static and the labile hypotheses. J Therm Biol. 2009;34: 306–309. doi: 10.1016/j.jtherbio.2009.04.002

46. Catullo RA, Llewelyn J, Phillips BL, Moritz CC. The Potential for Rapid Evolution under Anthropogenic Climate Change. Curr Biol. Elsevier BV; 2019;29: R996–R1007. doi: 10.1016/j.cub.2019.08.028 31593684

47. Verrastro L, Veronese L, Bujes C, Dias Filho MM. A new species of Liolaemus arambarensis from southern Brasil (Iguania: Tropiduridae). Herpetologica. 2003;59: 105–118. doi: 10.1655/0018-0831(2003)059[0105:ANSOLF]2.0.CO;2

48. Espinoza R. Liolaemus arambarensis. IUCN Red List Threat Species 2010. 2010;8235.

49. Martins LF, Guimarães M, Verrastro L. Population Estimates for the Sand Lizard, Liolaemus arambarensis : Contributions to the Conservation of an Endemic Species of Southern Brazil. Herpetologica. 2017;73: 55–62. doi: 10.1655/herpetologica-d-16-00046.1

50. Craugastor SF, Rican C, Forest TD, Bolan F, Puschendorf R, Zhu W, et al. The novel and endemic pathogen hypotheses: Competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol. 2006;8: 141–148. doi: 10.1111/j.1523-1739.2005.00255.x

51. Suguio K, Tessler MG. Planícies de cordões litorâneos quaternários do Brasil: origem e nomenclatura. In: Lacerda L, editor. Restingas, origem, estrutura, processos. 1984. pp. 32–56.

52. Kuinchtner A, Buriol GaA. Clima do Estado do Rio Grande do Sul segundo a classificação climática de Kóppen e Thornthwaite. Discip Sci Série Ciências Exatas. 2001;2: 171–182. Available:

53. Crump M, Scott N Jr.. Measuring and monitoring biological diversity: Standard methods for amphibians. In: Heyer W.R., Donnelly M.A., McDiarmid R.W., Hayek L.C. and F MS, editor. Visual encounter surveys. Smithsonian Institution Press; 1994. p. 364.

54. Di-Bernardo M., Borges-Martins M., Oliveira R.D., Pontes GMF. Taxocenoses de serpentes de regiões temperadas do Brasil. In: Nascimento L.B., Oliveira E, editor. Herpetologia no Brasil II. 2007. p. 354.

55. Borges-Landáez PA, Shine R. Influence of Toe-Clipping on Running Speed in Eulamprus quoyii, an Australian Scincid Lizard. J Herpetol. 2003;37: 592–595. doi: 10.1670/26-02N

56. Langkilde T, Shine R. How much stress do researchers inflict on their study animals? A case study using a scincid lizard, Eulamprus heatwolei. J Exp Biol. 2006;209: 1035–1043. doi: 10.1242/jeb.02112 16513929

57. Paulissen MA, Meyer HA. The Effect of Toe-Clipping on the Gecko Hemidactylus turcicus. J Herpetol. 2000;34: 282–285. doi: 10.2307/1565425

58. Matthiopoulos J. How to be a Quantitative Ecologist [Internet]. Chichester, UK: John Wiley & Sons, Ltd; 2011.

59. Akaike H. Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika. 1973;60: 255–265. doi: 10.1093/biomet/60.2.255

60. Kiefer MC, Van Sluys M, Rocha CFD. Thermoregulatory behaviour in Tropidurus torquatus (Squamata, Tropiduridae) from Brazilian coastal populations: an estimate of passive and active thermoregulation in lizards. Acta Zool. 2006;88: 81–87. doi: 10.1111/j.1463-6395.2007.00254.x

61. Maia-Carneiro T, Rocha CFD. Seasonal variations in behaviour of thermoregulation in juveniles and adults Liolaemus lutzae (Squamata, Liolaemidae) in a remnant of Brazilian restinga. Behav Processes. 2013;100: 48–53. doi: 10.1016/j.beproc.2013.08.001 23941976

62. Vrcibradic D, Rocha CFD. The Ecology of the Skink Mabuya frenata in an Area of Rock Outcrops in Southeastern Brazil. J Herpetol. 1998;32: 229–237. doi: 10.2307/1565302

63. Pianka ER, Vitt LJ. Lizards: windows to the evolution of diversity. University of California Press; 2003.

64. Porter WP, Gates DM. Thermodynamic Equilibria of Animals with Environment. Ecol Monogr. Wiley; 1969;39: 227–244. doi: 10.2307/1948545

65. Maia-Carneiro T, Rocha CFD. Influences of sex, ontogeny and body size on the thermal ecology of Liolaemus lutzae (Squamata, Liolaemidae) in a restinga remnant in southeastern Brazil. J Therm Biol. 2013;38: 41–46. doi: 10.1016/j.jtherbio.2012.10.004 24229803

66. Ruby DE. Winter Activity in Yarrow’s Spiny Lizard, Sceloporus jarrovi. Herpetologica. Allen PressHerpetologists’ League; 1977;33: 322–333.

67. Verrastro L, Ely I. Diet of the lizard Liolaemus occipitalis in the coastal sand dunes of southern Brazil (Squamata-Liolaemidae). Brazilian J Biol. Instituto Internacional de Ecologia; 2015;75: 289–299. doi: 10.1590/1519-6984.11013 26132010

68. Rocha CFD. Ecologia Termal de Liolaemus Lutzae (Sauria: Tropiduridae) em uma área de Restinga do Sudesde do Brasil. Rev Bras Biol. 1995;55: 481–489.

69. Bujes CS, Verrastro L. Thermal biology of Liolaemus occipitalis (Squamata, Tropiduridae) in the coastal sand dunes of Rio Grande do Sul, Brazil. Brazilian J Biol. 2006;66: 945–954. doi: 10.1590/s1519-69842006000500021 17119843

70. Maia-Carneiro T, Dorigo TA, Rocha CFD. Influences of Seasonality, Thermal Environment and Wind Intensity on the Thermal Ecology of Brazilian Sand Lizards In A Restinga Remnant. South Am J Herpetol. 2012;7: 241–251. doi: 10.2994/057.007.0306

71. Marquet PA, Ortíz JC, Bozinovié F, Jaksié FM. Ecological aspects of thermoregulation at high altitudes: the case of andean Liolaemus lizards in northern Chile. Oecologia. Springer-Verlag; 1989;81: 16–20. doi: 10.1007/BF00377003 28312150

72. Etheridge R. A Review of Lizards of the Liolaemus wiegmannii Group (Squamata, Iguania, Tropiduridae), and a History of Morphological Change in the Sand-Dwelling Species. Herpetol Monogr. 2000;14: 293–352. doi: 10.2307/1467049

73. Kiefer MC, Van Sluys M, Rocha CFD. Body temperatures of Tropidurus torquatus (Squamata, Tropiduridae) from coastal populations: Do body temperatures vary along their geographic range? J Therm Biol. 2005;30: 449–456. doi: 10.1016/j.jtherbio.2005.05.004

74. Martori R, Aun L, Orlandini S. Relaciones térmicas temporales en una población de Liolaemus koslowskyi. Cuad Herpetol. 1998;16: 33–45. Available:

75. Wang L, Chen W. The East Asian winter monsoon: Re-amplification in the mid-2000s. Chinese Sci Bull. 2014;59: 430–436. doi: 10.1007/s11434-013-0029-0

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