pp 1–10 | Cite as

Ontogenetic reduction in thermal tolerance is not alleviated by earlier developmental acclimation in Rana temporaria

  • Urtzi Enriquez-UrzelaiEmail author
  • Martina Sacco
  • Antonio S. Palacio
  • Pol Pintanel
  • Miguel Tejedo
  • Alfredo G. Nicieza
Physiological ecology – original research


Complex life-histories may promote the evolution of different strategies to allow optimal matching to the environmental conditions that organisms can encounter in contrasting environments. For ectothermic animals, we need to disentangle the role of stage-specific thermal tolerances and developmental acclimation to predict the effects of climate change on spatial distributions. However, the interplay between these mechanisms has been poorly explored. Here we study whether developmental larval acclimation to rearing temperatures affects the thermal tolerance of subsequent terrestrial stages (metamorphs and juveniles) in common frogs (Rana temporaria). Our results show that larval acclimation to warm temperatures enhances larval heat tolerance, but not thermal tolerance in later metamorphic and juvenile stages, which does not support the developmental acclimation hypothesis. Further, metamorphic and juvenile individuals exhibit a decline in thermal tolerance, which would confer higher sensitivity to extreme temperatures. Because thermal tolerance is not enhanced by larval developmental acclimation, these ‘risky’ stages may be forced to compensate through behavioural thermoregulation and short-term acclimation to face eventual heat peaks in the coming decades.


Amphibian Complex life-cycle Global warming Niche shifts Vulnerability 



We thank Florentino Braña, Miguel Carretero, Silvia Matesanz, and Ross Alford (editor) and two anonymous reviewers for helpful comments that improved previous versions of the manuscript. We thank the staff from the Principality of Asturias and the Governing Council of Castile-León for providing the permits to conduct this investigation. We are also grateful to two anonymous reviewers for their helpful comments.

Author contribution statement

UEU and AGN designed the study; AGN collected the experimental animals, UEU, MS, and ASP performed the experiment; UEU and MS analysed data; all authors contributed to the writing.


This research was supported by MINECO (CGL2012-40246) and MEC (CGL2017-86924-P) Grants. U.E.U. was supported by a Ph.D. award (BES-2013-063203) from MEC.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. Field work was carried out under the Government of the Principality of Asturias Permit No. 2015/008130 and 2016/001092. Experiments were carried out under the Ethics Board for Animal Experimentation of the University of Oviedo Permit No. 8-INV-2012. The members of the research team have approved licenses by the Service of Animal Welfare and Production of the Principality of Asturias to design (license type C; A.G.N) and execute (license type B; U.E.U.) experimental protocols with animals.

Data accessibility

Data supporting this article are available from the Dryad Digital Repository:

Supplementary material

442_2019_4342_MOESM1_ESM.docx (99 kb)
Supplementary material 1 (DOCX 99 kb)


  1. Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268. CrossRefGoogle Scholar
  2. Araújo MB, Ferri-Yañez F, Bozinovic F, Marquet PA, Valladares F, Chown SL (2013) Heat freezes niche evolution. Ecol Lett 16:1206–1219. CrossRefGoogle Scholar
  3. Araújo MB, Thuiller W, Pearson RG (2006) Climate warming and the decline of amphibians and reptiles in Europe. J Biogeogr 33:1712–1728. CrossRefGoogle Scholar
  4. Bartelt PE, Klaver RW, Porter WP (2010) Modeling amphibian energetics, habitat suitability, and movements of western toads, Anaxyrus (= Bufo) boreas, across present and future landscapes. Ecol Model 221:2675–2686. CrossRefGoogle Scholar
  5. Beaman JE, White CR, Seebacher F (2016) Evolution of plasticity: mechanistic link between development and reversible acclimation. Trends Ecol Evol 31:237–249. CrossRefGoogle Scholar
  6. Berven KA (1981) Mate choice in the Wood frog, Rana sylvatica. Evolution 35:707–722. CrossRefGoogle Scholar
  7. Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol Rev 83:339–355. CrossRefGoogle Scholar
  8. Bozinovic F, Bastías DA, Boher F et al (2011a) The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiol Biochem Zool 84:543–552. CrossRefGoogle Scholar
  9. Bozinovic F, Calosi P, Spicer JI (2011b) Physiological correlates of geographic range in animals. Annu Rev Ecol Evol Syst 42:155–179. CrossRefGoogle Scholar
  10. Bozinovic F, Medina NR, Alruiz JM et al (2016a) Thermal tolerance and survival responses to scenarios of experimental climatic change: changing thermal variability reduces the heat and cold tolerance in a fly. J Comp Physiol B 186:581–587. CrossRefGoogle Scholar
  11. Bozinovic F, Sabat P, Rezende EL, Canals M (2016b) Temperature variability and thermal performance in ectotherms: acclimation, behaviour, and experimental considerations. Evol Ecol Res 17:111–124Google Scholar
  12. Brattstrom BH (1968) Thermal acclimation in anuran amphibians as a function of latitude and altitude. Comp Biochem Physiol 24:93–111. CrossRefGoogle Scholar
  13. Briscoe NJ, Handasyde KA, Griffiths SR et al (2014) Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals. Biol Let 10:20140235. CrossRefGoogle Scholar
  14. Briscoe NJ, Porter WP, Sunnucks P, Kearney MR (2012) Stage-dependent physiological responses in a butterfly cause non-additive effects on phenology. Oikos 121:1464–1472. CrossRefGoogle Scholar
  15. Buckley LB, Ehrenberger JC, Angilletta MJ Jr (2015) Thermoregulatory behaviour limits local adaptation of thermal niches and confers sensitivity to climate change. Funct Ecol 29:1038–1047. CrossRefGoogle Scholar
  16. Cavieres G, Bogdanovich JM, Bozinovic F (2016) Ontogenetic thermal tolerance and performance of ectotherms at variable temperatures. J Evol Biol 29:1462–1468. CrossRefGoogle Scholar
  17. Chevin L-M, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8:e1000357. CrossRefGoogle Scholar
  18. Coyne JA, Bundgaard J, Prout T (1983) Geographic-variation of tolerance to environmental-stress in Drosophila pseudoobscura. Am Nat 122:474–488. CrossRefGoogle Scholar
  19. Cupp PV Jr (1980) Thermal tolerance of five salientian amphibians during development and metamorphosis. Herpetologica 36:234–244Google Scholar
  20. Donelson JM, Munday PL, McCormick MI, Nilsson GE (2011) Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish. Glob Change Biol 17:1712–1719. CrossRefGoogle Scholar
  21. Duarte H, Tejedo M, Katzenberger M et al (2012) Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Glob Change Biol 18:412–421. CrossRefGoogle Scholar
  22. Enriquez-Urzelai U, San Sebastián O, Garriga N, Llorente GA (2013) Food availability determines the response to pond desiccation in anuran tadpoles. Oecologia 173:117–127. CrossRefGoogle Scholar
  23. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. CrossRefGoogle Scholar
  24. Floyd RB (1983) Ontogenetic change in the temperature tolerance of larval Bufo marinus (Anura: Bufonidae). Comp Biochem Physiol Part A 75:267–271. CrossRefGoogle Scholar
  25. Floyd RB (1984) Variation in temperature preference with stage of development of Bufo marinus larvae. J Herpetol 18:153–158. CrossRefGoogle Scholar
  26. Fretwell SD (1972) Populations in a seasonal environment. Princeton University Press, PrincetonGoogle Scholar
  27. Gerick AA, Munshaw RG, Palen WJ et al (2014) Thermal physiology and species distribution models reveal climate vulnerability of temperate amphibians. J Biogeogr 41:713–723. CrossRefGoogle Scholar
  28. Gomez-Mestre I, Saccoccio VL, Iijima T et al (2010) The shape of things to come: linking developmental plasticity to post-metamorphic morphology in anurans. J Evol Biol 23:1364–1373. CrossRefGoogle Scholar
  29. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica. Google Scholar
  30. Groffman PM, Driscoll CT, Fahey TJ et al (2001) Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry 56:135–150. CrossRefGoogle Scholar
  31. Gunderson AR, Dillon ME, Stillman JH (2017) Estimating the benefits of plasticity in ectotherm heat tolerance under natural thermal variability. Funct Ecol. Google Scholar
  32. Gunderson AR, Stillman JH (2015) Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc R Soc B Biol Sci 282(2015):0401. Google Scholar
  33. Gutiérrez-Pesquera LM, Tejedo M, Olalla-Tárraga MÁ et al (2016) Testing the climate variability hypothesis in thermal tolerance limits of tropical and temperate tadpoles. J Biogeogr. Google Scholar
  34. Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–216. CrossRefGoogle Scholar
  35. Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366. CrossRefGoogle Scholar
  36. Kearney M, Porter W (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol Lett 12:334–350. CrossRefGoogle Scholar
  37. Kellermann V, van Heerwaarden B, Sgrò CM (2017) How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster. Proc Biol Sci 284:20170447. CrossRefGoogle Scholar
  38. Kingsolver JG, Arthur Woods H, Buckley LB et al (2011) Complex life cycles and the responses of insects to climate change. Integr Comp Biol 51:719–732. CrossRefGoogle Scholar
  39. Klockmann M, Günter F, Fischer K (2016) Heat resistance throughout ontogeny: body size constrains thermal tolerance. Global Change Biol 23:686–696. CrossRefGoogle Scholar
  40. Levy O, Buckley LB, Keitt TH et al (2015) Resolving the life cycle alters expected impacts of climate change. Proc R Soc B Biol Sci 282:20150837. CrossRefGoogle Scholar
  41. Levy O, Buckley LB, Keitt TH, Angilletta MJ (2016) Ontogeny constrains phenology: opportunities for activity and reproduction interact to dictate potential phenologies in a changing climate. Ecol Lett 19:620–628. CrossRefGoogle Scholar
  42. Lockwood BL, Gupta T, Scavotto R (2018) Disparate patterns of thermal adaptation between life stages in temperate vs. tropical Drosophila melanogaster. J Evol Biol 31:323–331. CrossRefGoogle Scholar
  43. Lutterschmidt WI, Hutchison VH (1997) The critical thermal maximum: history and critique. Can J Zool 75:1561–1574. CrossRefGoogle Scholar
  44. MacLean HJ, Higgins JK, Buckley LB, Kingsolver JG (2016) Geographic divergence in upper thermal limits across insect life stages: does behavior matter? Oecologia 181:107–114. CrossRefGoogle Scholar
  45. Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. Ann N Y Acad Sci 1206:35–55. CrossRefGoogle Scholar
  46. Maynard Smith J (1957) Temperature tolerance and acclimatization in Drosophila subobscura. J Exp Biol 34:85–96Google Scholar
  47. McDermott Long O, Warren R, Price J et al (2016) Sensitivity of UK butterflies to local climatic extremes: which life stages are most at risk? J Anim Ecol 86:108–116. CrossRefGoogle Scholar
  48. Mitton JB, Ferrenberg SM (2012) Mountain pine beetle develops an unprecedented summer generation in response to climate warming. Am Nat 179:E163–E171. CrossRefGoogle Scholar
  49. Muir AP, Biek R, Thomas R, Mable BK (2014) Local adaptation with high gene flow: temperature parameters drive adaptation to altitude in the common frog (Rana temporaria). Mol Ecol 23:561–574. CrossRefGoogle Scholar
  50. Newman RA (1989) Developmental plasticity of Scaphiopus couchii tadpoles in an unpredictable environment. Ecology 70:1775–1787. CrossRefGoogle Scholar
  51. Nyamukondiwa C, Terblanche JS (2010) Within-generation variation of critical thermal limits in adult Mediterranean and Natal fruit flies Ceratitis capitata and Ceratitis rosa: thermal history affects short-term responses to temperature. Physiol Entomol 35:255–264. CrossRefGoogle Scholar
  52. Oromí N, Camarasa S, Sanuy I, Sanuy D (2015) Variation of growth rate and survival in embryos and larvae of Rana temporaria populations from the Pyrenees. Acta Herpetol 10:85–91. Google Scholar
  53. Ospina AF, Mora C (2004) Effect of body size on reef fish tolerance to extreme low and high temperatures. Environ Biol Fishes 70:339–343. CrossRefGoogle Scholar
  54. Overgaard J, Tomčala A, Sørensen JG et al (2008) Effects of acclimation temperature on thermal tolerance and membrane phospholipid composition in the fruit fly Drosophila melanogaster. J Insect Physiol 54:619–629. CrossRefGoogle Scholar
  55. Pechenik JA (2006) Larval experience and latent effects–metamorphosis is not a new beginning. Integr Comp Biol 46:323–333. CrossRefGoogle Scholar
  56. Peck LS, Clark MS, Morley SA et al (2009) Animal temperature limits and ecological relevance: effects of size, activity and rates of change. Funct Ecol 23:248–256. CrossRefGoogle Scholar
  57. Pincebourde S, Casas J (2015) Warming tolerance across insect ontogeny: influence of joint shifts in microclimates and thermal limits. Ecology 96:986–997. CrossRefGoogle Scholar
  58. Potter KA, Davidowitz G, Arthur Woods H (2010) Cross-stage consequences of egg temperature in the insect Manduca sexta. Funct Ecol 25:548–556. CrossRefGoogle Scholar
  59. Quintero I, Wiens JJ (2013) Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species. Ecol Lett 16:1095–1103. CrossRefGoogle Scholar
  60. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 5 Dec 2016
  61. Ragland GJ, Kingsolver JG (2008) Evolution of thermotolerance in seasonal environments: the effects of annual temperature variation and life-history timing in Wyeomyia smithii. Evolution 62:1345–1357. CrossRefGoogle Scholar
  62. Reques R, Tejedo M (1995) Negative correlation between length of larval period and metamorphic size in natural populations of natterjack toads (Bufo calamita). J Herpetol 29:311–314. CrossRefGoogle Scholar
  63. Ribeiro PL, Camacho A, Navas CA (2012) Considerations for assessing maximum critical temperatures in small ectothermic animals: insights from leaf-cutting ants. PLoS One 7:e32083. CrossRefGoogle Scholar
  64. Richter-Boix A, Katzenberger M, Duarte H et al (2015) Local divergence of thermal reaction norms among amphibian populations is affected by pond temperature variation. Evolution 69:2210–2226. CrossRefGoogle Scholar
  65. Richter-Boix A, Tejedo M, Rezende EL (2011) Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis. Ecol Evol 1:15–25. CrossRefGoogle Scholar
  66. Ruiz-Aravena M, Gonzalez-Mendez A, Estay SA et al (2014) Impact of global warming at the range margins: phenotypic plasticity and behavioral thermoregulation will buffer an endemic amphibian. Ecol Evol 4:4467–4475. CrossRefGoogle Scholar
  67. Rutledge PS, Spotila JR, Easton DP (1987) Heat hardening in response to two types of heat shock in the lungless salamanders Eurycea bislineata and Desmognathus ochrophaeus. J Therm Biol 12:235–241. CrossRefGoogle Scholar
  68. Scott GR, Johnston IA (2012) Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. Proc Natl Acad Sci USA 109:14247–14252. CrossRefGoogle Scholar
  69. Sgrò CM, Terblanche JS, Hoffmann AA (2016) What can plasticity contribute to insect responses to climate change? Annu Rev Entomol 61:433–451. CrossRefGoogle Scholar
  70. Sinclair BJ, Marshall KE, Sewell MA et al (2016) Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecol Lett. Google Scholar
  71. Slotsbo S, Schou MF, Kristensen TN et al (2016) Reversibility of developmental heat and cold plasticity is asymmetric and has long-lasting consequences for adult thermal tolerance. J Exp Biol 219:2726–2732. CrossRefGoogle Scholar
  72. Smith DC (1987) Adult recruitment in Chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350. CrossRefGoogle Scholar
  73. Smith-Gill SJ, Berven KA (1979) Predicting amphibian metamorphosis. Am Nat 113:563–585. CrossRefGoogle Scholar
  74. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. J Exp Biol 213:912–920. CrossRefGoogle Scholar
  75. Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annu Rev Mar Sci 4:39–61. CrossRefGoogle Scholar
  76. Spotila JR, Oconnor MP, Bakken GS (1992) Biophysics of heat and mass transfer. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. The University of Chicago Press, Chicago, pp 59–80Google Scholar
  77. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65. CrossRefGoogle Scholar
  78. Stuhldreher G, Hermann G, Fartmann T (2014) Cold-adapted species in a warming world—an explorative study on the impact of high winter temperatures on a continental butterfly. Entomol Exp Appl 151:270–279. CrossRefGoogle Scholar
  79. Sunday JM, Bates AE, Kearney MR et al (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Natl Acad Sci USA 111:5610–5615. CrossRefGoogle Scholar
  80. Sørensen JG, Kristensen TN, Loeschcke V, Schou MF (2015) No trade-off between high and low temperature tolerance in a winter acclimatized Danish Drosophila subobscura population. J Insect Physiol 77:9–14. CrossRefGoogle Scholar
  81. Tejedo M, Marangoni F, Pertoldi C et al (2010) Contrasting effects of environmental factors during larval stage on morphological plasticity in post-metamorphic frogs. Clim Res. Google Scholar
  82. Terblanche JS, Chown SL (2006) The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae). J Exp Biol 209:1064–1073. CrossRefGoogle Scholar
  83. Valladares F, Matesanz S, Guilhaumon F et al (2014) The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol Lett 17:1351–1364. CrossRefGoogle Scholar
  84. Vences M, Galan P, Palanca A et al (2000) Summer microhabitat use and diel activity cycles in a high altitude Pyrenean population of Rana temporaria. Herpetol J 10:49–56Google Scholar
  85. Vázquez DP, Gianoli E, Morris WF, Bozinovic F (2015) Ecological and evolutionary impacts of changing climatic variability. Biol Rev 92:22–42. CrossRefGoogle Scholar
  86. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93.;subPage:string:Access CrossRefGoogle Scholar
  87. Williams SE, Shoo LP, Isaac JL et al (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol 6:e325. CrossRefGoogle Scholar
  88. Wollmuth LP, Crawshaw LI, Forbes RB, Grahn DA (1987) Temperature selection during development in a montane anuran species, Rana cascadae. Physiol Zool 60:472–480. CrossRefGoogle Scholar
  89. Álvarez D, Nicieza AG (2002a) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195. CrossRefGoogle Scholar
  90. Álvarez D, Nicieza AG (2002b) Effects of temperature and food quality on anuran larval growth and metamorphosis. Funct Ecol 16:640–648. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Biología de Organismos y SistemasUniversidad de Oviedo UOOviedoSpain
  2. 2.UMIB, Unidad Mixta de Investigación en Biodiversidad (UO-CSIC-PA)MieresSpain
  3. 3.Department of Evolutionary EcologyEstación Biológica de Doñana, CSICSevilleSpain

Personalised recommendations