Skip to main content

Individual variation in thermal performance curves: swimming burst speed and jumping endurance in wild-caught tropical clawed frogs

Oecologia volume 175, pages 471–480 (2014)Cite this article

Abstract

The importance of studying individual variation in locomotor performance has long been recognized as it may determine the ability of an organism to escape from predators, catch prey or disperse. In ectotherms, locomotor performance is highly influenced by ambient temperature (T a), yet several studies have showed that individual differences are usually retained across a T a gradient. Less is known, however, about individual differences in thermal sensitivity of performance, despite the fact that it could represent adaptive sources of phenotypic variation and/or additional substrate for selection to act upon. We quantified swimming and jumping performance in 18 wild-caught tropical clawed frogs (Xenopus tropicalis) across a T a gradient. Maximum swimming velocity and acceleration were not repeatable and individuals did not differ in how their swimming performance varied across T a. By contrast, time and distance jumped until exhaustion were repeatable across the T a gradient, indicating that individuals that perform best at a given T a also perform best at another T a. Moreover, thermal sensitivity of jumping endurance significantly differed among individuals, with individuals of high performance at low T a displaying the highest sensitivity to T a. Individual differences in terrestrial performance increased with decreasing T a, which is opposite to results obtained in lizards at the inter-specific and among-individual levels. To verify the generality of these patterns, we need more studies on individual variation in thermal reaction norms for locomotor performance in lizards and frogs.

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

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

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

    Article  Google Scholar 

  • Angilletta MJ Jr, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240

    Article  Google Scholar 

  • Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361

    Google Scholar 

  • Arnold SJ, Bennett AF (1984) Behavioral variation in natural populations. III. Antipredator displays in the garter snake Thamnophis radix. Anim Behav 32:1108–1118

    Article  Google Scholar 

  • Artacho P, Jouanneau I, Le Galliard J-F (2013) Interindividual variation in thermal sensitivity of maximal sprint speed, thermal behavior, and resting metabolic rate in a lizard. Physiol Biochem Zool 86:458–469

    PubMed  Article  Google Scholar 

  • Baumann H, Conover DO (2011) Adaptation to climate change: contrasting patterns of thermal-reaction-norm evolution in Pacific vs Atlantic silversides. Proc R Soc Lond Ser B Biol Sci 278:2265–2273

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Boake CR (1989) Repeatability: its role in evolutionary studies of mating behavior. Evol Ecol 3:173–182

    Article  Google Scholar 

  • Braña F (2003) Morphological correlates of burst speed and field movement patterns: the behavioural adjustment of locomotion in wall lizards (Podarcis muralis). Biol J Linn Soc 80:135–146

    Article  Google Scholar 

  • Brodie ED III, Russell NH (1999) The consistency of individual differences in behaviour: temperature effects on antipredator behaviour in garter snakes. Anim Behav 57:445–451

    PubMed  Article  Google Scholar 

  • Brommer JE (2013) Phenotypic plasticity of labile traits in the wild. Curr Zool 59:485–505

    Google Scholar 

  • Butler D, Cullis BR, Gilmour AR, Gogel DJ (2009) ASReml-R reference manual Release 3.0 (draft copy). VSN, Hemel Hempstead

  • Careau V, Garland T Jr (2012) Performance, personality, and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85:543–571

    PubMed  Article  Google Scholar 

  • Careau V, Gifford ME, Biro PA (2014) Individual (co)variation in thermal reaction norms of standard and maximal metabolic rates in wild-caught slimy salamanders. Funct Ecol. doi:10.1111/1365-2435.12259

    Google Scholar 

  • Casterlin ME, Reynolds WW (1980) Diel activity and thermoregulatory behavior of a fully aquatic frog: Xenopus laevis. Hydrobiologia 75:189–191

    Article  Google Scholar 

  • Conover DO, Duffy TA, Hice LA (2009) The covariance between genetic and environmental influences across ecological gradients reassessing the evolutionary significance of countergradient and cogradient variation. Ann NY Acad Sci 1168:100–129

    PubMed  Article  Google Scholar 

  • Djawdan M, Garland T Jr (1988) Maximal running speeds of bipedal and quadrupedal rodents. J Mammal 69:765–772

    Article  Google Scholar 

  • Dominicus A, Skrondal A, Gjessing HK, Pedersen NL, Palmgren J (2006) Likelihood ratio tests in behavioral genetics: problems and solutions. Behav Genet 36:331–340

    PubMed  Article  Google Scholar 

  • Elnitsky MA, Claussen DL (2006) The effects of temperature and inter-individual variation on the locomotor performance of juvenile turtles. J Comp Physiol B 176:497–504

    PubMed  Article  Google Scholar 

  • Friedman WA, Garland T Jr, Dohm MR (1992) Individual variation in locomotor behavior and maximal oxygen consumption in mice. Physiol Behav 52:97–104

    CAS  PubMed  Article  Google Scholar 

  • Garland T Jr (1988) Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42:335–350

    Article  Google Scholar 

  • Garland T Jr, Losos JB (1994) Ecological morphology of locomotor performance in squamate reptiles. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 240–302

    Google Scholar 

  • Gilchrist GW (1996) A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidius ervi. Evolution 50:1560–1572

    Article  Google Scholar 

  • Hadfield JD, Nakagawa S (2010) General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J Evol Biol 23:494–508

    Google Scholar 

  • Henderson CR (1982) Analysis of covariance in the mixed model—higher-level, non-homogeneous, and random regressions. Biometrics 38:623–640

    PubMed  Article  Google Scholar 

  • Herrel A, Bonneaud C (2012) Temperature dependence of locomotor performance in the tropical clawed frog, Xenopus tropicalis. J Exp Biol 215:2465–2470

    PubMed  Article  Google Scholar 

  • Herrel A, Gonwouo LN, Fokam EB, Ngundu WI, Bonneaud C (2012) Intersexual differences in body shape and locomotor performance in the aquatic frog, Xenopus tropicalis. J Zool 287:311–316

    Article  Google Scholar 

  • Huey RB, Dunham AE (1987) Repeatability of locomotor performance in natural populations of the lizard Sceloporus merriami. Evolution 41:1116–1120

    Article  Google Scholar 

  • Huey RB, Hertz PE (1984) Is a jack-of-all-temperatures a master of none? Evolution 38:441–444

    Article  Google Scholar 

  • Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: discussion of approaches. Am Zool 19:357–366

    Google Scholar 

  • Husak JF (2006) Does survival depend on how fast you can run or how fast you do run? Funct Ecol 20:1080–1086

    Article  Google Scholar 

  • Husak JF, Fox SF (2006) Field use of maximal sprint speed by collared lizards (Crotaphytus collaris): compensation and sexual selection. Evolution 60:1888–1895

    PubMed  Article  Google Scholar 

  • Irschick DJ (2003) Measuring performance in nature: implications for studies of fitness within populations. Integr Comp Biol 43:396–407

    PubMed  Article  Google Scholar 

  • Irschick DJ, Garland T Jr (2001) Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annu Rev Ecol Syst 32:367–396

    Article  Google Scholar 

  • Irschick DJ, Herrel AV, Vanhooydonck B, Huyghe K, Van Damme R (2005) Locomotor compensation creates a mismatch between laboratory and field estimates of escape speed in lizards: a cautionary tale for performance-to-fitness studies. Evolution 59:1579–1587

    PubMed  Article  Google Scholar 

  • Izem R, Kingsolver JG (2005) Variation in continuous reaction norms: quantifying directions of biological interest. Am Nat 166:277–289

    PubMed  Article  Google Scholar 

  • John-Alder HB, Morin PJ, Lawler S (1988) Thermal physiology, phenology, and distribution of tree frogs. Am Nat 132:506–520

    Article  Google Scholar 

  • Kenward MG, Roger JH (1997) The precision of fixed effects estimates from restricted maximum likelihood. Biometrics 53:983–997

    CAS  PubMed  Article  Google Scholar 

  • Knies JL, Kingsolver JG, Burch CL (2009) Hotter is better and broader: thermal sensitivity of fitness in a opulation of bacteriophages. Am Nat 173:419–430

    PubMed  Article  Google Scholar 

  • Knowles TW, Weigl PD (1990) Thermal dependence of anuran burst locomotor performance. Copeia 1990:796–802

  • Latimer CAL, Wilson RS, Chenoweth SF (2011) Quantitative genetic variation for thermal performance curves within and among natural populations of Drosophila serrata. J Evol Biol 24:965–975

    CAS  PubMed  Article  Google Scholar 

  • Londos PL, Brooks RJ (1988) Effect of temperature acclimation on locomotory performance curves in the toad, Bufo woodhousii woodhousii. Copeia 1:26–32

    Article  Google Scholar 

  • Lynch M, Walsh JB (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland

    Google Scholar 

  • Martin JGA, Nussey DH, Wilson AJ, Réale D (2011) Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol Evol 2:362–374

    Article  Google Scholar 

  • Miller K (1982) Effect of temperature on sprint performance in the frog Xenopus laevis and the salamander Necturus maculosus. Copeia 3:695–698

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Navas CA, Gomes FR, Carvalho JE (2008) Thermal relationships and exercise physiology in anuran amphibians: integration and evolutionary implications. Comp Biochem Physiol A 151:344–362

    Article  Google Scholar 

  • Niehaus AC, Wilson RS, Seebacher F, Franklin CE (2011) Striped marsh frog (Limnodynastes peronii) tadpoles do not acclimate metabolic performance to thermal variability. J Exp Biol 214:1965–1970

    PubMed  Article  Google Scholar 

  • Preest MR, Pough FH (1989) Interaction of temperature and hydration on locomotion of toads. Funct Ecol 3:693–699

    Article  Google Scholar 

  • Putnam RW, Bennett AF (1981) Thermal dependence of behavioural performance of anuran amphibians. Anim Behav 29:502–509

    Article  Google Scholar 

  • Rödel MO (2000) Herpetofauna of West Africa. Chimaira, Frankfurt am Main

    Google Scholar 

  • Šamajová P, Gvoždík L (2010) Inaccurate or disparate temperature cues? Seasonal acclimation of terrestrial and aquatic locomotor capacity in newts. Funct Ecol 24:1023–1030

    Article  Google Scholar 

  • Singer JD, Willett JB (2003) Applied longitudinal data analysis: modeling change and event occurrence. Oxford University Press, New York

    Book  Google Scholar 

  • Stinchcombe JR, Function-valued_Traits_Working_Group, Kirkpatrick M (2012) Genetics and evolution of function-valued traits: understanding environmentally responsive phenotypes. Trends Ecol Evol 27:637–647

    PubMed  Article  Google Scholar 

  • Van Berkum FH, Huey RB, Tsuji JS, Garland T Jr (1989) Repeatability of individual differences in locomotor performance and body size during early ontogeny of the lizard Sceloporus occidentalis (Baird & Girard). Funct Ecol 3:97–105

    Article  Google Scholar 

  • Walton M (1988) Relationships among metabolic, locomotory, and field measures of organismal performance in the Fowler’s toad (Bufo woodhousei fowleri). Physiol Zool 61:107–118

    Google Scholar 

  • Whitehead PJ, Puckridge JT, Leigh CM, Seymour RS (1989) Effect of temperature on jump performance of the frog Limnodynastes tasmaniensis. Physiol Zool 62:937–949

    Google Scholar 

  • Wilson RS (2001) Geographic variation in thermal sensitivity of jumping performance in the frog Limnodynastes peronii. J Exp Biol 204:4227–4236

    CAS  PubMed  Google Scholar 

  • Wilson RS, James RS, Johnston IA (2000) Thermal acclimation of locomotor performance in tadpoles and adults of the aquatic frog Xenopus laevis. J Comp Physiol B 170:117–124

    CAS  PubMed  Article  Google Scholar 

  • Winter D (2004) Biomechanics and motor control of human movement. Wiley, New York

    Google Scholar 

Download references

Acknowledgments

We would like to thank L. N. Gonwouo for his valuable help in the field, J. Rodriguez for help with animal husbandry, and M. Antoine for logistical support. This research was supported by the Agence Nationale de la Recherche MOBIGEN (ANR-09-PEXT-003 to A. H. and C. B.), a Muséum National d’Histoire Naturelle Action transversale du Muséum (ATM) grant of the Biodiversité actuelle et fossile programme to A. H., a Marie Curie reintegration grant to C. B. (FP7-PEOPLE-IRG-2008 no. 239257), an Alfred Deakin postdoctoral research fellowship to V. C., and an ARC Future Fellowship to P. A. B. We thank two anonymous reviewers for their constructive comments on a previous draft.

Author information

Authors and Affiliations

  1. Centre for Integrative Ecology, School of Life and Environmental Science, Deakin University, 75 Pigdons Road, Waurn Ponds, VIC, 3216, Australia

    Vincent Careau & Peter A. Biro

  2. Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Cornwall, Penryn, TR10 9FE, UK

    Camille Bonneaud

  3. Department of Plant and Animal Sciences, University of Buea, 63, Buea, Cameroon

    Eric B. Fokam

  4. Département d’Ecologie et de Gestion de la Biodiversité, UMR 7179 CNRS/MNHN, 57 rue Cuvier, 75231 Cedex 5, Paris, France

    Anthony Herrel

  5. Evolutionary Morphology of Vertebrates, Ghent University, K. L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Anthony Herrel

Authors
  1. Vincent Careau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter A. Biro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Camille Bonneaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric B. Fokam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anthony Herrel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vincent Careau.

Additional information

Communicated by Jean-François Le Galliard.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 34 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Careau, V., Biro, P.A., Bonneaud, C. et al. Individual variation in thermal performance curves: swimming burst speed and jumping endurance in wild-caught tropical clawed frogs. Oecologia 175, 471–480 (2014). https://doi.org/10.1007/s00442-014-2925-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-2925-7

Keywords

  • Anura
  • Climate change
  • Random regression
  • Repeatability
  • Silurana