Running in cold weather: morphology, thermal biology, and performance in the southernmost lizard clade in the world (Liolaemus lineomaculatus section: Liolaemini: Iguania)
Marcelo Fabián Bonino
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Search for more papers by this authorDébora Lina Moreno Azócar
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Search for more papers by this authorMaría José Tulli
CONICET-Instituto de Herpetologia (FML), Tucumán, Argentina
Search for more papers by this authorCristian Simón Abdala
CONICET-Instituto de Herpetologia (FML), Tucumán, Argentina
Facultad de Ciencias Naturales e I. M. Lillo (UNT), Tucumán, Argentina
Search for more papers by this authorMaría Gabriela Perotti
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Search for more papers by this authorCorresponding Author
Félix Benjamín Cruz
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, 8400 - Bariloche, Rio Negro, Argentina===Search for more papers by this authorMarcelo Fabián Bonino
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Search for more papers by this authorDébora Lina Moreno Azócar
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Search for more papers by this authorMaría José Tulli
CONICET-Instituto de Herpetologia (FML), Tucumán, Argentina
Search for more papers by this authorCristian Simón Abdala
CONICET-Instituto de Herpetologia (FML), Tucumán, Argentina
Facultad de Ciencias Naturales e I. M. Lillo (UNT), Tucumán, Argentina
Search for more papers by this authorMaría Gabriela Perotti
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Search for more papers by this authorCorresponding Author
Félix Benjamín Cruz
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, Bariloche, Argentina
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) CONICET-UNCOMA, 8400 - Bariloche, Rio Negro, Argentina===Search for more papers by this authorAbstract
The integration or coadaptation of morphological, physiological, and behavioral traits is represented by whole-organism performance traits such as locomotion or bite force. Additionally, maximum sprint speed is a good indicator of whole-organism performance capacity as variation in sprinting ability can affect survival. We studied thermal biology, morphology, and locomotor performance in a clade of Liolaemus lizards that occurs in the Patagonian steppe and plateaus, a type of habitat characterized by its harsh cold climate. Liolaemus of the lineomaculatus section display a complex mixture of conservative and flexible traits. The phylogenetically informed analyses of these ten Liolaemus species show little coevolution of their thermal traits (only preferred and optimum temperatures were correlated). With regard to performance, maximum speed was positively correlated with optimum temperature. Body size and morphology influenced locomotor performance. Hindlimbs are key for maximal speed, but forelimb length was a better predictor for sustained speed (i.e. average speed over a total distance of 1.2 m). Finally, sustained speed differed among species with different diets, with herbivores running on average faster over a long distance than omnivores. J. Exp. Zool. 315:495–503, 2011. © 2011 Wiley-Liss, Inc.
Supporting Information
Additional Supporting Information may be found in the online version of this article
Filename | Description |
---|---|
jez_697_sm_SuppInfo.pdf30.5 KB | Supplementary Materials |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
LITERATURE CITED
- Abdala CS, Quinteros S, Espinoza RE. 2008. Two new species of Liolaemus (Iguania: Liolaemidae) from northwestern Argentina. Herpetologica 64: 458–471.
- Adolph SC. 1990. Influence of behavioral thermoregulation on microhabitat use by two Sceloporus lizards. Ecology 71: 315–327.
- Aguilar R, Cruz F. 2010. Refuge use in a Patagonian nocturnal lizard, Homonota darwini: the role of temperature. J Herpetol 44: 236–241.
- Andrews RM. 1998. Latitudinal and elevational variation in body temperatures of Sceloporus lizards. J Thermal Biol 23: 329–334.
- Angilletta MJ. 2006. Estimating and comparing thermal performance curves. J Therm Biol 31: 541–545.
- Angilletta MJ. 2009a. Looking for answers to questions about heat stress: researchers are getting warmer. Funct Ecol 23: 231–232.
- Angilletta MJ. 2009b. Thermal adaptation: a theoretical and empirical synthesis. Oxford: Oxford University Press.
10.1093/acprof:oso/9780198570875.001.1 Google Scholar
- Angilletta MJ, Niewiarowski PH, Navas CA. 2002. The evolution of thermal physiology in ectotherms. J Therm Biol 27: 249–268.
- Arnold SJ. 1983. Morphology, performance and fitness. Am Zool 23: 347–361.
- Bauwens D, Garland Jr T, Castilla AM, Van Damme R. 1995 Evolution of sprint speed in lacertid lizards: morphological, physiological and behavioral covariation. Evolution 49: 848–863.
- Bennett AF, Huey RB. 1990. Studying the evolution of physiological performance. In: DJ Futuyma, J Antonovics, editors. Oxford surveys in evolutionary biology. Oxford: Oxford University Press. p 250–284.
- Blomberg SP, Garland Jr T, Ives AR. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745.
- Bonine KE, Garland Jr T. 1999. Sprint performance of phrynosomatid lizards, measured on a high–speed treadmill, correlates with hindlimb length. J Zool 248: 255–265.
- Breitman MF, Avila LJ, Sites JW, Morando M. 2011. Lizards from the end of the world: Phylogenetic relationships of the Liolaemus lineomaculatus section (Squamata: Iguania: Liolaemini). Mol Phylogenet Evol 59: 364–376.
- Carothers JH, Fox SF, Marquet PA, Jaksic FM. 1997. Thermal characteristics of ten Andean lizards of the genus Liolaemus in central Chile. Rev Chil Hist Nat 70: 297–309.
- Christian KA, Tracy CR. 1981. The effect of the thermal environment on the ability of hatchling Galapagos land iguanas to avoid predation during dispersal. Oecologia 49: 218–223.
- Crowley SR. 1985. Thermal sensitivity of sprint–running in the lizard Sceloporus undulatus: support for a conservative view of thermal physiology. Oecologia 66: 219–225.
- Cruz FB, Fitzgerald LA, Espinoza RE, Schulte II JA. 2005. The importance of phylogenetic scale in tests of Bergmann's and Rapoport's rules: lessons from a clade of South American lizards. J Evol Biol 18: 1559–1578.
- Cruz FB, Belver L, Acosta JC, Villavicencio HJ, Blanco G, Canovas MG. 2009. Thermal biology of Phymaturus lizards: evolutionary constraints or lack of environmental variation? Zoology 112: 425–432.
- Cruz FB, Antenucci D, Luna F, Abdala CS, Vega LE. 2011. Energetics in Liolaemini lizards: implications of a small body size and ecological conservatism. J Comp Physiol B 181: 373–382.
- Díaz-Uriarte R, Garland Jr T. 1998. Effects of branch length errors on the performance of phylogenetically independent contrasts. Syst Biol 47: 654–672.
- Dorcas ME, Peterson CR, Flint ME. 1997. The thermal biology of digestion in rubber boas (Charina bottae): physiology, behavior, and environmental constraints. Physiol Zool 70: 292–300.
- Espinoza RE, Wiens JJ, Tracy CR. 2004. Recurrent evolution of herbivory in small, cold–limate lizards: breaking the ecophysiological rules of reptilian herbivory. Proc Natl Acad Sci USA 101: 16819–16824.
- Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat 126: 1–25.
- Fernandez JB, Smith Jr J, Scolaro A, Ibargüengoytía NR. 2011. Performance and thermal sensitivity of the southernmost lizards in the world, Liolaemus sarmientoi and Liolaemus magellanicus. J Therm Biol 36: 15–22.
- Garland Jr T. 1985. Ontogenetic and individual variation in size, shape, and speed in the Australian agamid lizard Amphibolurus nuchalis. J Zool 207: 425–439.
- Garland Jr T, Kelly SA. 2006. Phenotypic plasticity and experimental evolution. J Exp Biol 209: 2344–2361.
- Garland Jr T, Losos JB. 1994. Ecological morphology of locomotor performance in squamate reptiles. In: PC Wainwright, SM Reilly, editors. Ecological morphology: integrative organismal biology. Chicago: University of Chicago Press. p 240–302.
- Garland Jr T, Huey RB, Bennett AF. 1991. Phylogeny and thermal physiology in lizards: a reanalysis. Evolution 45: 1969–1975.
- Garland Jr T, Harvey PH, Ives AR. 1992. Procedures for the analysis of comparative data using phylogenetic independent contrasts. Syst Biol 41: 18–32.
- Garland Jr T, Dickerman AW, Janis CM, Jones JA. 1993. Phylogenetic analysis of covariance by computer simulation. Syst Biol 42: 265–292.
- Gaston KJ, Blackburn TM. 2000. Pattern and process in macroecology. Malden, MA: Blackwell Science.
10.1002/9780470999592 Google Scholar
- Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology. Oxford: Oxford University Press.
10.1093/oso/9780198546412.001.0001 Google Scholar
- Hertz PE, Huey RB, Nevo E. 1983. Homage to Santa Anita: thermal sensitivity of sprint speed in agamid lizards. Evolution 37: 1075–1084.
- Hertz PE, Huey RB, Stevenson RD. 1993. Evaluating temperature regulation by field–active ectotherms: the fallacy of the inappropriate question. Am Nat 142: 796–818.
- Huey RB. 1982. Temperature, physiology, and the ecology of reptiles. In: C Gans, FH Pough, editors. Biology of reptilia, vol. 12. New York: Academic Press. p 25–74.
- Huey RB, Bennettt AF. 1987. Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance temperatures of lizards. Evolution 41: 1098–1115.
- Huey RB, Hertz PE. 1982. Effects of body size and slope on sprint speed of a lizard (Stellio (Agama) stellio). J Exp Biol 97: 401–409.
- Huey RB, Kingsolver JG. 1989. Evolution of thermal sensitivity of ectotherms. TREE 4: 131–135.
- Huey RB, Kingsolver JG. 1993. Evolution of resistance to high temperature in ectotherms. Am Nat 142: S21–S46.
- Huey RB, Stevenson RD. 1979. Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Integr Comp Biol 19: 357–366.
- Irschick DJ, Jayne BC. 1998. Effects of incline on acceleration, body posture, and hindlimb kinematics in two species of lizard, Callisaurus draconoides and Uma scoparia. J Exp Biol 201: 273–287.
- Jayne BC, Bennett AF. 1990. Selection on locomotor performance capacity in a natural–population of garter snakes. Evolution 44: 1204–1229.
- Ji X, Zheng XZ, Xu YG, Sun RM. 1995. Several aspects of the thermal biology of the skink Eumeces chinensis. Acta Zool Sin 41: 268–285.
- Ji X, Du WG, Sun PY. 1996. Body temperature, thermal tolerance and influence of temperature on sprint speed and food assimilation in adult grass lizards, Takydromus septentrionsalis. J Therm Biol 21: 155–161.
- Ji X, Sun PY, Du WG. 1997. Selected body temperature, thermal tolerance and food assimilation in a viviparous skink, Sphenomorphus indicus. Neth J Zool 47: 103–110.
- Kingsolver JG. 2009. The well–temperatured biologist. Am Nat 174: 755–768.
- Kingsolver J, Huey R. 2003. Introduction: the evolution of morphology, performance, and fitness. Int Comp Biol 43: 361–366.
- Kingsolver JG, Watt WB. 1983. Thermoregulatory strategies in Colias butterflies: thermal stress and the limits to adaptation in temporally varying environments. Am Nat 121: 32–55.
- Kohlsdorf T, Navas CA. 2006. Ecological constraints on the evolutionary association between field and preferred temperatures in Tropidurinae lizards. Evol Ecol 20: 549–564.
- Koumoundouros G, Divanach P, Kentouri M. 2001: Osteological development of Dentex dentex (Osteichthyes: Sparidae): dorsal, anal, paired fins and squamation. Mar Biol 138: 399–406.
- Labra A. 1998. Selected body temperatures of seven species of chilean Liolaemus lizards. Rev Chil Hist Nat 71: 349–358.
- Lobo F, Espinoza RE, Quinteros S. 2010. A critical review and systematic discussion of recent classification proposals for liolaemid lizards. Zootaxa 2549: 1–30.
10.11646/zootaxa.2549.1.1 Google Scholar
- Losos JB. 1990. The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. Evolution 44: 1189–1203.
- Losos JB, Creer D, Schulte II JA. 2002. Cautionary comments on use of maximal sprint performance. J Zool 258: 57–61.
- Maddison WP, Maddison DR. 2010. Mesquite: a modular system for evolutionary analysis. Version 2.74. Available at: http://mesquiteproject.org.
- Marsh RL, Bennett AF. 1986. Thermal–dependence of sprint performance of the lizard Sceloporus occidentalis. J Exp Biol 126: 79–87.
- Martin TL, Huey RB. 2008. Why “suboptimal” is optimal: Jensen's inequality and ectotherm thermal preferences. Am Nat 171: E102–E118.
- Martins EP, Garland Jr T. 1991. Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution 45: 534–557.
- Martins EP, Labra A, Halloy MP, Thompson JT. 2004. Large–scale patterns of signal evolution: an interspecific study of Liolaemus lizard headbob displays. Anim Behav 68: 453–463.
- Midford PE, Garland Jr T, Maddison WP. 2003. PDAP Package. Version 1.15. Available at: http://mesquiteproject.org
- Nicieza AG, Metcalfe NB. 1997 Growth compensation in juvenile Atlantic salmon: responses to depressed temperature and food availability. Ecology 78: 2385–2400.
- Okafor AL. 2010. The influence of body temperature on sprint speed and anti–predatory defensive responses of the North African monitor lizard, Varanus griseus. Afr J Biotech 9: 778–781.
- Petriek AG, Walker RS, Novaro AJ. 2009. Susceptibility of lizards to predation under two levels of vegetative cover. J Arid Environ 73: 574–577.
- Rodríguez–Serrano E, Navas CA, Bozinovic F. 2010. The comparative field body temperature among Liolaemus lizards: testing the staticand the labile hypotheses. J Therm Biol 34: 306–309.
- Schulte II JA, Macey JR, Espinoza RE, Larson A. 2000. Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biol J Linn Soc 69: 75–102.
- Scolaro JA. 2005. Reptiles patagónicos Sur, Una guía de campo, Ed. Univ. Nac. de la Patagonia, Trelew.
- Sinervo B, Losos JB. 1991. Walking the tight rope: arboreal sprint performance among Sceloporus occidentalis lizard populations. Ecology 72: 1225–1233.
- Sinervo B, Hedges R, Adolph SC. 1991. Decreased sprint speed as a cost of reproduction in the lizard Sceloporus occidentalis: variation among populations. J Exp Biol 155: 323–336.
- Snell HL, Jennings RD, Snell HM, Harcourt S. 1988. Intrapopulational variation in predator–avoidance performance of Galápagos lava lizards: the interaction of sexual and natural selection. Evol Ecol 2: 353–369.
- Tulli MJ, Cruz FB, Herrel A, Vanhooydonck B, Abdala V. 2009. The interplay between claw morphology and habitat use in neotropical iguanian lizards. Zoology 112: 379–392.
- Tulli MJ, Abdala V, Cruz FB. 2011. Relationships among morphology, clinging performance and habitat use in Liolaemini lizards. J Evol Biol 24: 843–855.
- van Berkum FH. 1986. Evolutionary patterns of the thermal sensitivity of sprint speed in Anolis lizards. Evolution 40: 594–604.
- van Berkum FH. 1988. Latitudinal patterns of the thermal sensitivity of sprint speed in lizards. Am Nat 132: 327–343.
- Van Damme R, Vanhooydonck B. 2001. Origins of interspecific variation in lizard sprint capacity. Funct Ecol 15: 186–202.
- Van Damme R, Bauwens D, Castilla AM, Verheyen RF. 1989. Altitudinal variation of the thermal biology and running performance in the lizard Podarcis tiliguerta. Oecologia 80: 516–524.
- Van Damme R, Bauwens D, Castilla AM, Verheyen RF. 1990. Comparative thermal ecology of the sympatric lizards Podarcis tiliguerta and Podarcis sicula. Acta Oecol 11: 503–512.
- Wall M, Shine R. 2008. Post–feeding thermophily in lizards (Lialis burtonis Gray, Pygopodidae): Laboratory studies can provide misleading results. J Therm Biol 33: 274–279.