Abstract
Achieving optimal body temperature maximizes animal fitness. Since ambient temperature may limit ectotherm thermal performance, it can be constrained in too cold or hot environments. In this sense, elevational gradients encompass contrasting thermal environments. In thermally pauperized elevations, ectotherms may either show adaptations or suboptimal body temperatures. Also, reproductive condition may affect thermal needs. Herein, we examined different thermal ecology and physiology capabilities of the lizard Psammodromus algirus along a 2200-m elevational gradient. We measured field (Tb) and laboratory-preferred (Tpref) body temperatures of lizards with different reproductive conditions, as well as ambient (Ta) and copper-model operative temperature (Te), which we used to determine thermal quality of the habitat (de), accuracy (db), and effectiveness of thermoregulation (de–db) indexes. We detected no Tb trend in elevation, while Ta constrained Tb only at high elevations. Moreover, while Ta decreased more than 7 °C with elevation, Tpref dropped only 0.6 °C, although significantly. Notably, low-elevation lizards faced excess temperature (Te > Tpref). Notably, de was best at middle elevations, followed by high elevations, and poorest at low elevations. Nonetheless, regarding microhabitat, high-elevation de was more suitable in sun-exposed microhabitats, which may increase exposition to predators, and at midday, which may limit daily activity. As for gender, db and de–db were better in females than in males. In conclusion, P. algirus seems capable to face a wide thermal range, which probably contributes to its extensive corology and makes it adaptable to climate changes.
Similar content being viewed by others
References
Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142:273–295
Aguado S, Braña F (2014) Thermoregulation in a cold-adapted species (Cyren’s Rock Lizard, Iberolacerta cyreni): influence of thermal environment and associated costs. Can J Zool 92:955–964
Alford JG, Lutterschmidt WI (2012) Modeling energetic and theoretical costs of thermoregulatory strategy. J Biol Dyn 6:63–69
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis, 1st edn. Oxford University Press, Oxford
Bakken GS, Angilletta MJ (2014) How to avoid errors when quantifying thermal environments. Funct Ecol 28:96–107
Belliure J, Carrascal LM (2002) Influence of heat transmission mode on heating rates and on the selection of patches for heating in a Mediterranean lizard. Physiol Biochem Zool 75:369–376
Beuchat CA (1986) Reproductive influences on the thermoregulatory behavior of a live-bearing lizard. Copeia 1986:971–979
Blouin-Demers G, Nadeau P (2005) The cost-benefit model of thermoregulation does not predict lizard thermoregulation behavior. Ecology 86:560–566
Blouin-Demers G, Weatherhead PJ (2001) Thermal ecology of black rat snakes (Elaphe obsoleta) in a thermally challenging environment. Ecology 82:3025–3043
Braña F (1993) Shifts in body temperature and escape behaviour of female Podarcis muralis during pregnancy. Oikos 66:216–222
Brewster CL, Sikes RS, Gifford ME (2013) Quantifying the cost of thermoregulation: thermal and energetic constraints on growth rates in hatchling lizards. Funct Ecol 27:490–497
Brown RP, Au T (2009) The influence of metabolic heat on body temperature of a small lizard, Anolis carolinensis. Comp Biochem Physiol A 153:181–184
Carrascal LM, López P, Martín J, Salvador A (1992) Basking and antipredator behaviour in a high altitude lizard: implications of heat-exchange rate. Ethology 92:143–154
Carter AJ, Goldizen AW, Tromp SA (2010) Agamas exhibit behavioral syndromes: bolder males bask and feed more but may suffer higher predation. Behav Ecol 21:655–661
Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026
Clusella-Trullas S, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245
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
Díaz JA (1997) Ecological correlates of the thermal quality of an ectotherm’s habitat: a comparison between two temperate lizard populations. Funct Ecol 11:79–89
Díaz JA, Cabezas-Díaz S (2004) Seasonal variation in the contribution of different behavioural mechanisms to lizard thermoregulation. Funct Ecol 18:867–875
Díaz JA, Iraeta P, Monasterio C (2006) Seasonality provokes a shift of thermal preferences in a temperate lizard, but altitude does not. J Therm Biol 31:237–242
Du W, Lu Y, Shen J (2005) The influence of maternal thermal environments on reproductive traits and hatchling traits in a Lacertid lizard. J Therm Biol 30:153–161
Dzialowski EM (2005) Use of operative temperature and standard operative temperature models in thermal biology. J Therm Biol 30:317–334
Fei T, Skidmore AK, Venus V, Wang T, Schlerf M, Toxopeus B, van Overjijk S, Bian M, Liu Y (2012) A body temperature model for lizards as estimated from the thermal environment. J Therm Biol 37:56–64
Gilchrist GW (1995) Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. Am Nat 146:252–270
Grant BW, Dunham AE (1990) Elevational covariation in environmental constraints and life histories of the desert lizard Sceloporus merriami. Ecology 71:1765–1776
Gvoždík L (2002) To heat or to save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: Lacertidae) in different thermal environments along an altitudinal gradient. Can J Zool 80:479–492
Herczeg G, Gonda A, Saarikivi J, Merilä J (2006) Experimental support for the cost–benefit model of lizard thermoregulation. Behav Ecol Sociobiol 60:405–414
Herczeg G, Saarikivi J, Gonda A, Perälä J, Tuomola A, Merilä J (2007) Suboptimal thermoregulation in male adders (Vipera berus) after hibernation imposed by spermiogenesis. Biol J Linn Soc 92:19–27
Hertz PE (1992) Temperature regulation in Puerto Rican Anolis lizards: a field test using null hypotheses. Ecology 73:1405–1417
Hertz PE, Huey RB (1981) Compensation for altitudinal changes in the thermal environment by some Anolis lizards on Hispaniola. Ecology 62:515–521
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, Slatkin M (1976) Costs and benefits of lizard thermoregulation. Quart Rev Biol 51:363–384
Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366
Ibargüengoytía NR, Acosta JC, Boretto JM, Villavicencio HJ, Marinero JA, Krenz JD (2008) Field thermal biology of Phymaturus lizards: comparisons from the Andes to the Patagonian steppe in Argentina. J Arid Environ 72:1620–1630
Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. PNAS 106:3835–3840
Lara-Reséndiz RA, Larraín-Barrios BC, Díaz de la Vega-Pérez AH, Méndez-de la Cruz FR (2014) Calidad térmica a través de un gradiente altitudinal para una comunidad de lagartijas en la sierra del Ajusco y el Pedregal de San Ángel, México. Rev Mex Biodiv 85:885–897
Le Galliard JF, Le Bris M, Clobert J (2003) Timing of locomotor impairment and shift in thermal preferences during gravidity in a viviparous lizard. Funct Ecol 17:877–885
Lin CX, Zhang L, Ji X (2008) Influence of pregnancy on locomotor and feeding performances of the skink, Mabuya multifasciata: why do females shift thermal preferences when pregnant? Zoology 111:188–195
Marler CA, Walsberg G, White ML, Moore M (1995) Increased energy expenditure due to increased territorial defense in male lizards after phenotypic manipulation. Behav Ecol Sociobiol 37:225–231
Martín J, López P (2000) Fleeing to unsafe refuges: effects of conspicuousness and refuge safety on the escape decisions of the lizard Psammodromus algirus. Can J Zool 78:265–270
Mathies T, Andrews RM (1997) Influence of pregnancy on the thermal biology of the lizard, Sceloporus jarrovi: why do pregnant females exhibit low body temperatures? Funct Ecol 11:498–507
McConnachie S, Alexander GJ (2004) The effect of temperature on digestive and assimilation efficiency, gut passage time and appetite in an ambush foraging lizard, Cordylus melanotus melanotus. J Comp Physiol B 174:99–105
Moreno Azócar DL, Bonino MF, Perotti MG, Abdala CS, Schulte JA, Cruz FB (2013) Chasing the Patagonian sun: comparative thermal biology of Liolaemus lizards. Oecologia 171:773–788
Moreno-Rueda G, Pleguezuelos JM, Alaminos E (2009) Climate warming and activity period extension in the Mediterranean snake Malpolon monspessulanus. Clim Chang 92:235–242
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. 1st ed. Cambridge University Press
R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reguera S, Zamora-Camacho FJ, Moreno-Rueda G (2014) The lizard Psammodromus algirus (Squamata: Lacertidae) is darker at high altitudes. Biol J Linn Soc 112:132–141
Rodríguez-Serrano E, Navas CA, Bozinovic F (2009) The comparative field body temperature among Liolaemus lizards: testing the static and the labile hypotheses. J Therm Biol 34:306–309
Salvador A (2011) Lagartija colilarga—Psammodromus algirus (Linnaeus, 1758). In Salvador A, Marco A (eds) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org/
Schwarzkopf L, Shine R (1991) Thermal biology of reproduction in viviparous skinks, Eulamprus tympanum: why do gravid females bask more? Oecologia 88:562–569
Shine R (2003) Locomotor speed of gravid lizards: placing ‘costs of reproduction’ within an ecological context. Funct Ecol 17:526–533
Shine R, Harlow PS (1993) Maternal thermoregulation influences offspring viability in a viviparous lizard. Oecologia 96:122–127
Shine R, Harlow PS, Elphick MJ, Olsson MM, Mason RT (2000) Conflicts between courtship and thermoregulation: the thermal ecology of amorous male garter snakes (Thamnophis sirtalis parietalis, Colubridae). Physiol Biochem Zool 73:508–516
Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans B, Villagrán-Santa Cruz M, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Ávila LJ, Morando M, De la Riva IJ, Sepúlveda PV, Duarte Rocha CF, Ibargüengoytía 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
Stevens GC (1992) The elevational gradient in altitudinal range: an extension of Rapoport’s latitudinal rule to altitude. Am Nat 140:893–911
Sun Y, Du Y, Yang J, Lin C, Ji X (2012) Climatic correlates of female and male reproductive cycles and plasma steroid hormone levels in the many-lined sun skink Eutropis multifasciata. Gen Comp Endocrinol 178:363–371
Sunday JM, Bates AE, Dulvy NK (2010) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B 278:1823–1830
Truter JC, van Wyk JH, Mouton PFN (2014) An evaluation of daily, seasonal and population-level variation in the thermal preference of a group-living lizard, Ouroborus cataphractus (Sauria: Cordylidae). Amphibia-Reptilia 35:391–403
Valdecantos S, Martínez V, Lobo F, Cruz FB (2013) Thermal biology of Liolaemus lizards from the high Andes: being efficient despite adversity. J Therm Biol 38:126–134
Verwaijen D, Van Damme R (2007) Correlated evolution of thermal characteristics and foraging strategy in lacertid lizards. J Therm Biol 32:388–395
Vickers M, Manicom C, Schwarzkopf L (2011) Extending the cost-benefit model of thermoregulation: high-temperature environments. Am Nat 177:452–461
Xiang J, Weiguo D, Pingyue S (1996) Body temperature, thermal tolerance and influence of temperature on sprint speed and food assimilation in adult grass lizards, Takydromus septentrionalis. J Therm Biol 21:155–161
Yu D, Guo-Hua D, Yan-Yan S, Xiang J (2008) Northern grass lizard (Takydromus septentrionalis; Lacertidae) shift thermal preferences when fasted. Acta Zool Sin 54:739–743
Zamora-Camacho FJ, Reguera S, Moreno-Rueda G, Pleguezuelos JM (2013) Patterns of seasonal activity in a Mediterranean lizard along a 2200 m altitudinal gradient. J Therm Biol 38:64–69
Zamora-Camacho FJ, Reguera S, Moreno-Rueda G (2014a) Bergmann’s Rule rules body size in an ectotherm: heat conservation in a lizard along a 2200-meter elevational gradient. J Evol Biol 27:2820–2828
Zamora-Camacho FJ, Reguera S, Rubiño-Hispán MV, Moreno-Rueda G (2014b) Effects of limb length, body mass, gender, gravidity, and elevation on escape speed in the lizard Psammodromus algirus. Evol Biol 41:509–517
Zamora-Camacho FJ, Rubiño-Hispán MV, Reguera S, Moreno-Rueda G (2015) Thermal dependence of sprint performance in the lizard Psammodromus algirus along a 2200-meter elevational gradient: cold-habitat lizards do not perform better at low temperatures. J Therm Biol 52:90–96
Acknowledgments
This study was funded by the Ministerio de Ciencia e Innovación (project CGL2009-13185) and performed according to permits issued to the authors by Junta de Andalucía (references GMN/GyB/JMIF and ENSN/JSG/JEGT/MCF). FJZC and SR were supported by two pre-doctoral grants from the Ministerio de Ciencia e Innovación (FPU program). We thank the personnel from the Espacio Natural de Sierra Nevada for their constant support. María Virtudes Rubiño Hispán, MariCruz Tuset Arcas, Miguel Leandro López Gracia, Susana Silva González, Elena Melero Martínez, and Laureano González González-Granda helped us during field work. Comments by Juan Manuel Pleguezuelos and three anonymous reviewers improved the manuscript. David Nesbitt revised the English.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This article does not contain any studies with human participants performed by any of the authors. The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 327 kb)
Rights and permissions
About this article
Cite this article
Zamora-Camacho, F.J., Reguera, S. & Moreno-Rueda, G. Thermoregulation in the lizard Psammodromus algirus along a 2200-m elevational gradient in Sierra Nevada (Spain). Int J Biometeorol 60, 687–697 (2016). https://doi.org/10.1007/s00484-015-1063-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-015-1063-1