Skip to main content

Advertisement

SpringerLink
Log in

Turn up the heat: thermal tolerances of lizards at La Selva, Costa Rica

  • Highlighted Student Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Global temperature increases over the next century are predicted to contribute to the extinction of a number of taxa, including up to 40 % of all lizard species. Lizards adapted to living in lowland tropical areas are especially vulnerable because of their dependence on specific microhabitats, low vagility, and a reduced capacity to physiologically adjust to environmental change. To assess the potential effects of climate change on lizards in the lowland tropics, we measured the critical thermal maximum (CTmax) of ten species from La Selva, Costa Rica. We also examined how well body size, microhabitat type, and species predicted the CTmax. We used current temperature data along with projected temperature increases for 2080 to predict which species may be at the greatest risk at La Selva. Of the ten species sampled, four are at serious risk of lowland extirpation and three others might also be at risk under the highest predicted temperature-increase models. Forest floor lizards at La Selva have already experienced significant population declines over the past 40 years, and we found that each of the forest floor species we studied is at serious risk of local extirpation. We also found that microhabitat type is the strongest predictor of CTmax, demonstrating the profound impact habitat specialization has on the thermal limits of tropical lizards.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc R Soc Lond B 267:739–745. doi:10.1098/rspb.2000.1065

    Article  CAS  Google Scholar 

  • Andrews RM, Schwarzkopf L (2012) Thermal performance of squamate embryos with respect to climate, adult life history, and phylogeny. Biol J Linn Soc 106:851–864. doi:10.1111/j.1095-8312.2012.01901.x

    Article  Google Scholar 

  • 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. doi:10.1016/S0306-4565(01)00084-5

    Article  Google Scholar 

  • Angilletta MJ Jr, Niewiarowski PH, Navas CA (2002b) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268. doi:10.1016/S0306-4565(01)00094-8

    Article  Google Scholar 

  • Angilletta MJ Jr, Huey RB, Frazier MR (2010) Thermodynamic effects on organismal performance: is hotter better? Physiol Biochem Zool 83:197–206. doi:10.1086/648567

    Article  PubMed  Google Scholar 

  • Asbury DA, Angilletta MJ Jr (2010) Thermodynamic effects on the evolution of performance curves. Am Nat 176:40–49. doi:10.1086/653659

    Article  Google Scholar 

  • Becker CG, Zamudio KR (2011) Tropical amphibian populations experience higher disease risk in natural habitats. Proc Natl Acad Sci USA 108:9893–9898. doi:10.1073/pnas.1014497108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Belliure J, Carrascal LM, Diaz JA (1996) Covariation of thermal biology and foraging mode in two Mediterranean lacertid lizards. Ecology 77:1163–1173. doi:10.2307/2265585

    Article  Google Scholar 

  • Cadby CD, While GM, Hobday AJ, Uller T, 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. doi:10.1111/j.1749-4877.2010.00201.x

    Article  PubMed  Google Scholar 

  • Chown SL (2012) Trait-based approaches to conservation physiology: forecasting environmental change risks from the bottom up. Philos Trans R Soc B Biol Sci 367:1615–1627. doi:10.1098/rstb.2011.0422

    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. doi:10.1086/660021

    Article  PubMed  Google Scholar 

  • Colwell RK, Brehm G, Cardelús CL, Gilman AC, Longino JT (2008) Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322:258–261. doi:10.1126/science.116254

    Article  CAS  PubMed  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679. doi:10.1126/science.292.5517.673

    Article  CAS  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. doi:10.1073/pnas.0709472105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467:704–706. doi:10.1038/nature09407

    Article  CAS  PubMed  Google Scholar 

  • Donnelly MA (1994) The biology of La Selva amphibians. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: ecology and natural history of a Neotropical rain forest. University of Chicago, Chicago, pp 380–381

    Google Scholar 

  • Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139. doi:10.1016/S0169-5347(98)01554-7

    Article  PubMed  Google Scholar 

  • Dzialowski EM (2005) Use of operative temperature and standard operative temperature models in thermal biology. J Therm Biol 30:317–334. doi:10.1016/j.jtherbio.2005.01.005

    Article  Google Scholar 

  • Feder ME (1978) Environmental variability and thermal acclimation in Neotropical and temperate zone salamanders. Physiol Zool 51:7–16

    Article  CAS  Google Scholar 

  • Feder ME, Lynch JF (1982) Effects of latitude, season, elevation, and microhabitat on field body temperatures of Neotropical and temperate zone salamanders. Ecology 63:1657–1664. doi:10.2307/1940107

    Article  Google Scholar 

  • Feeley KJ, Silman MR (2010) Biotic attrition from tropical forests correcting for truncated temperature niches. Glob Change Biol 16:1830–1836. doi:10.1111/j.1365-2486.2009.02085.x

    Article  Google Scholar 

  • Frazier MR, Huey RB, Berrigan D (2006) Thermodynamics constrains the evolution of insect population growth rates: “warmer is better”. Am Nat 168:512–520. doi:10.1086/506977

    Article  CAS  PubMed  Google Scholar 

  • Ghalambor CK, Huey RB, Martin PR, Tewksbury JJ, Wang G (2006) Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integr Comp Biol 46:5–17. doi:10.1093/icb/icj003

    Article  PubMed  Google Scholar 

  • Grover MC (1996) Microhabitat use and thermal ecology of two narrowly sympatric Sceloporus (Phrynosomatidae) lizards. J Herpetol 30:152–160. doi:10.2307/1565506

    Article  Google Scholar 

  • Gunderson AR, Leal M (2012) Geographic variation in vulnerability to climate warming in a tropical Caribbean lizard. Funct Ecol 26:783–793. doi:10.1111/j.1365-2435.2012.01987.x

    Article  Google Scholar 

  • Guyer C (1994) The biology of La Selva reptiles. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: ecology and natural history of a Neotropical rain forest. University of Chicago, Chicago, pp 382–383

    Google Scholar 

  • Han D, Zhou K, Bauer AM (2004) Phylogenetic relationships among gekkotan lizards inferred from C-mos nuclear DNA sequences and a new classification of the Gekkota. Biol J Linn Soc 83:353–368. doi:10.1111/j.1095-8312.2004.00393.x

    Article  Google Scholar 

  • Hasegawa M, Susuki Y, Wada S (2005) Design and performance of a wet sponge model for amphibian thermal biology. Curr Herpetol 24:27–32. doi:10.3105/1345-5834(2005)24[27:DAPOAW]2.0.CO;2

    Article  Google Scholar 

  • Huey RB, Slatkin M (1976) Cost and benefits of lizard thermoregulation. Q Rev Biol 51:363–384. doi:10.1086/409470

    Article  CAS  PubMed  Google Scholar 

  • Huey RB, Niewiarowski PH, Kaufmann J, Herron JC (1989) Thermal biology of nocturnal ectotherms: is sprint performance of geckos maximal at low body temperatures? Physiol Zool 62:488–504

    Article  Google Scholar 

  • Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Pérez HJÁ, Garland T (2009) Why tropical forest lizards are vulnerable to climate warming. Proc R Soc Lond B Biol 276:1939–1948. doi:10.1098/rspb.2008.1957

    Article  Google Scholar 

  • Huey RB, Losos JB, Moritz C (2010) Are lizards toast? Science 328:832–833. doi:10.1126/science.1190374

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part A. Global and sectoral aspects. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Contribution of Working Group II to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University, Cambridge, pp 1039–1101

    Google Scholar 

  • Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249

    Article  Google Scholar 

  • Jenssen TA, Hovde KA, Taney KG (1998) Size-related habitat use by nonbreeding Anolis carolinensis lizards. Copeia 1998:774–779. doi:10.2307/1447814

    Article  Google Scholar 

  • Kearney M, Porter WP (2004) Mapping the fundamental niche: physiology, climate, and the distribution of a nocturnal lizard. Ecology 85:3119–3131. doi:10.1890/03-0820

    Article  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. doi:10.1073/pnas.0808913106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leal M, Gunderson AR (2012) Rapid change in the thermal tolerance of a tropical lizard. Am Nat 180:815–822. doi:10.1086/668077

    Article  PubMed  Google Scholar 

  • Lutterschmidt WI, Hutchison VH (1997) The critical thermal maximum: data to support the onset of spasms as the definitive end point. Can J Zool 75:1553–1560. doi:10.1139/z97-782

    Article  Google Scholar 

  • Maes D, Titeux N, Hortal J, Anselin A, Decleer K, Knijf GD, Fichefet V, Luoto M (2010) Predicted insect diversity declines under climate change in an already impoverished region. J Insect Conserv 14:485–498. doi:10.1007/s10841-010-9277-3

    Article  Google Scholar 

  • Magrin G, García CG, Choque DC, Giménez JC, Moreno AR, Nagy GJ, Nobre C, Villamizar A (2007) Climate change 2007: impacts, adaptation and vulnerability: Latin America. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson SE (eds) Contribution of Working Group II to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University, Cambridge, pp 581–615

    Google Scholar 

  • McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (1994) La Selva: ecology and natural history of a Neotropical rain forest, 1st edn. University of Chicago, Chicago

    Google Scholar 

  • Meiri S (2008) Evolution and ecology of lizard body sizes. Global Ecol Biogeogr 17:724–734. doi:10.1111/j.1466-8238.2008.00414.x

    Article  Google Scholar 

  • Miles DB (1994) Population differentiation in locomotor performance and the potential response of a terrestrial organism to global environmental change. Am Zool 34:422–436

    Article  Google Scholar 

  • Munguia-Vega A, Rodriguez-Estrella R, Shaw WW, Culver M (2013) Localized extinction of an arboreal desert lizard caused by habitat fragmentation. Biol Conserv 157:11–20. doi:10.1016/j.biocon.2012.06.026

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Method Ecol Evol 4:133–142. doi:10.1111/j.2041-210x.2012.00261.x

    Article  Google Scholar 

  • Navas CA (1996) Implications of microhabitat selection and patterns of activity on the thermal ecology of high elevation Neotropical anurans. Oecologia 108:617–626. doi:10.1007/BF00329034

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Development Core Team R (2013) nlme: linear and nonlinear mixed effects models. R package version 3:1–110

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/

  • Seebacher F, Franklin CE (2005) Physiological mechanisms of thermoregulation in reptiles: a review. J Comp Physiol B 175:533–541. doi:10.1007/s00360-005-0007-1

    Article  PubMed  Google Scholar 

  • Sheldon KS, Yang S, Tewksbury JJ (2011) Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure. Ecol Lett 14:1191–1200. doi:10.1111/j.1461-0248.2011.01689.x

    Article  PubMed  Google Scholar 

  • Shine R, Kearney M (2001) Field studies of reptile thermoregulation: how well do physical models predict operative temperatures? Funct Ecol 15:282–288. doi:10.1046/j.1365-2435.2001.00510.x

    Article  Google Scholar 

  • Sinervo B, Mendez-De-La-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz R, Martinez-Mendez N, Calderon-Espinosa ML, Meza-Lazaro RN, Gadsden H, Avila LJ, Morando M, De la Riva IJ, Sepulveda PV, Rocha CFD, Ibarguengoytia N, Puntriano CA, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899. doi:10.1126/science.1184695

    Article  CAS  PubMed  Google Scholar 

  • Solís F, Ibáñez R, Chaves G, Bolaños F, Wilson LD (2012) Grant T (2010) IUCN 2012. IUCN Red List of Threatened Species

    Google Scholar 

  • Stevenson RD (1985) Body size and limits to the daily range of body temperature in terrestrial ectotherms. Am Nat 125:102–117. doi:10.1086/284330

    Article  Google Scholar 

  • Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65. doi:10.1126/science.1083073

    Article  CAS  PubMed  Google Scholar 

  • Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Ferreira Siqueira M, Grainger A, Hannah L, Hughes L, Huntley B, Jaarsveld AS, Midgley GF, Miles L, Oretga-Huerta MA, Peterson AT, Philips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148. doi:10.1038/nature02121

    Article  CAS  PubMed  Google Scholar 

  • Townsend TM, Mulcahy DG, Noonan BP, Sites JW, Kuczynski CA, Wiens JJ, Reeder TW (2011) Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation. Mol Phylogenet Evol 61:363–380. doi:10.1016/j.ympev.2011.07.008

    Article  PubMed  Google Scholar 

  • van Berkum FH (1988) Latitudinal patterns of the thermal sensitivity of sprint speed in lizards. Am Nat 132:327–343. doi:10.1086/284856

    Article  Google Scholar 

  • Vasconcelos R, Santos X, Carretero MA (2012) High temperatures constrain microhabitat selection and activity patterns of the insular Cape Verde wall gecko. J Arid Environ 81:18–25. doi:10.1016/j.jaridenv.2012.01.013

    Article  Google Scholar 

  • Vickers M, Manicom C, Schwarzkopf L (2011) Extending the cost-benefit model of thermoregulation: high-temperature environments. Am Nat 177:452–461. doi:10.1086/658150

    Article  PubMed  Google Scholar 

  • Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci USA 105:11466–11473. doi:10.1073/pnas.0801921105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Walters RJ, Blanckenhorn WU, Berger D (2012) Forecasting extinction risk of ectotherms under climate warming: an evolutionary perspective. Funct Ecol 26:1324–1338. doi:10.1111/j.1365-2435.2012.02045.x

    Article  Google Scholar 

  • Whitfield SM, Bell KE, Philippi T, Sasa M, Bolaños F, Chaves G, Savage JM, Donnelly MA (2007) Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proc Natl Acad Sci USA 104:8352–8356. doi:10.1073/pnas.0611256104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zeh JA, Bonilla MM, Su EJ, Padua MV, Anderson RV, Kaur D, Yang D, Zeh DW (2012) Degrees of disruption: projected temperature increase has catastrophic consequences for reproduction in a tropical ectotherm. Glob Change Biol 18:1833–1842. doi:10.1111/j.1365-2486.2012.02640.x

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation and the Organization for Tropical Studies Research Experience for Undergraduates. This manuscript was greatly improved by the suggestions and support of Dr Diego Salazar, the 2013 Research Experience for Undergraduates undergrad group at La Selva, and Tony Frazier. All applicable institutional and/or national guidelines for the care and use of animals were followed.

Author contribution statement

G. A. B. and S. M. W. conceived and designed the experiments. G. A. B. and S. M. W. conducted fieldwork and performed the experiments. G. A. B. and E. N. T. analyzed the data. G. A. B., E. N. T., and S. M. W. wrote the manuscript.

Author information

Authors and Affiliations

  1. School of Life Sciences, Arizona State University, 427 East Tyler Mall, Tempe, AZ, 85287, USA

    George A. Brusch IV

  2. Department of Biological Sciences, California Polytechnic State University, San Luis Obispo, CA, 93407, USA

    Emily N. Taylor

  3. Conservation and Research Department, Zoo Miami, Miami, FL, 33177, USA

    Steven M. Whitfield

Authors
  1. George A. Brusch IV
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emily N. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Steven M. Whitfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to George A. Brusch IV.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Lin Schwarzkopf.

This study and paper represent my senior undergraduate thesis, and gave me the opportunity to experience the scientific process, from start to finish, first hand. I am extremely proud of this work and believe it should be considered for the “Highlighted Student Research” section. I am eternally grateful to my coauthors and the Organization for Tropical Studies Research Experience for Undergraduates program for giving me this opportunity.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brusch, G.A., Taylor, E.N. & Whitfield, S.M. Turn up the heat: thermal tolerances of lizards at La Selva, Costa Rica. Oecologia 180, 325–334 (2016). https://doi.org/10.1007/s00442-015-3467-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3467-3

Keywords

Search

Navigation