Skip to main content
Log in

Seasonal and altitudinal variation in dorsal skin reflectance and thermic rates in a high-altitude montane lizard

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

Abstract

Temperature is one of the most important factors in the life histories of ectotherms, as body temperature has an undeniable effect on growth, activity, and reproduction. Lizards have a wide variety of strategies to acquire and maintain body temperature in an optimal range. The “Thermal Melanism Hypothesis” proposes that individuals with lower skin reflectance can heat up faster as a result of absorbing more solar radiation compared to lighter conspecifics. Therefore, having a darker coloration might be advantageous in cold habitats. Dorsal skin reflectance has been found to change rapidly with body temperature in several lizard species, and it can also vary over longer, seasonal time scales. These variations may be important in thermoregulation, especially in lizards that inhabit areas with a large temperature variation during the year. Here, we study how dorsal reflectance fluctuates with body temperature and varies among seasons. We compared dorsal skin reflectance at three body temperature treatments, and measured thermal rates (i.e., heat and cool rate, thermic lapse, and net heat gain) by elevation (2500–4100 m) and seasons (spring, summer, and autumn) in the mesquite lizard, Sceloporus grammicus. Our results show that lizards were darker at high elevations and during the months with the lowest environmental temperatures. The rate of obtaining and retaining heat also varied during the year and was highest during the reproductive season. Our results indicate that the variation of dorsal skin reflectance and thermal rates follows a complex pattern in lizard populations and is affected by both elevation and season.

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

Access this article

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

Similar content being viewed by others

References

  • Adolph SC (1990) Influence of behavioral thermoregulation on microhabitat use by two Sceloporus lizards. Ecology 71:315–327

    Article  Google Scholar 

  • Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142:273–295

    Article  CAS  Google Scholar 

  • Aguado S, Clusella-Trullas S (2021) Intra-specific variation of thermal performance, skin reflectance and body size partially co-vary with climate in a lizard. Biol J Linn Soc 134:111–125

    Article  Google Scholar 

  • Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis, first ed. Oxford University Press, Oxford

    Book  Google Scholar 

  • Bagnara JT, Hadley ME (1973) Chromatophores and Color Change, the Comparative Physiology of Animal Pigmentation. Inc. Englewood Cliffs, New Yersey

    Google Scholar 

  • Bagnara JT, Taylor JD, Hadley ME (1968) The dermal chromatophore unit. J Cell Biol 38(1):67–79

    Article  CAS  Google Scholar 

  • Bastiaans E, Bastiaans MJ, Moringa G, Castañeda-Gaytan JG, Marshall JC, Bane B, Méndez-de la Cruz FR, Sinervo B (2014) Female preference for sympatric vs allopatric male throat color morphs in the mesquite lizard (Sceloporus grammicus) species complex. Plos One: e93197

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bauwens D, Hertz PE, Castilla AM (1996) Thermoregulation in a lacertid lizard: the relative contributions of distinct behavioral mechanisms. Ecology 77:1818–1830

    Article  Google Scholar 

  • Bittner TD, King RB, Kerfin JM (2002) Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis). Copeia 2002: 477–482

  • 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

    Article  Google Scholar 

  • Cadena V, Rankin K, Smith KR, Endler J, Stuart-Fox D (2018) Temperature induced colour change varies seasonally in bearded dragon lizards. Biol J Linn Soc 123:422–430

    Article  Google Scholar 

  • Chang C, Zheng R (2003) Effects of ultraviolet B on epidermal morphology, shedding, lipid peroxide, and antioxidant enzymes in Cope’s rat snake (Elaphe Taeniura). J Photochem Photobiol B Biol 72:79–85

    Article  CAS  Google Scholar 

  • Clusella-Trullas S, Van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245

    Article  Google Scholar 

  • Clusella-Trullas S, Terblanche JS, Blackburn TM, Chown SL (2008) Testing the thermal melanism hypothesis: a macrophysiological approach. Funct Ecol 22:232–238

    Article  Google Scholar 

  • Clusella-Trullas S, Van Wyk JH, Spotila JR (2009) Thermal benefits of melanism in cordylid lizards: a theoretical and field test. Ecology 90:2297–2312

    Article  Google Scholar 

  • CONANP (2016) Programa De Manejo, área de protección de flora y fauna del Nevado De Toluca. SEMARNAT, México

    Google Scholar 

  • Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251

  • Crisp M, Cook LM, Hereward FV (1979) Color and heat balance in the lizard Lacerta dugesii. Copeia 1979: 250–258

  • Cuadrado M (2000) Body colors indicate the Reproductive Status of Female Common chameleons: experimental evidence for the Intersex Communication Function. Ethology 106:79–91

    Article  Google Scholar 

  • Delhey K (2018) Darker where cold and wet: Australian birds follow their own version of Gloger’s rule. Ecography 41:673–683

    Article  Google Scholar 

  • Díaz JA, Cabezas-Díaz S (2004) Seasonal variation in the contribution of different behavioural mechanisms to lizard thermoregulation. Func Ecol 18:867–875

    Article  Google Scholar 

  • Díaz de la Vega-Pérez AH, Barrios-Montiel R, Jiménez-Arcos VH, Bautista A, Bastiaans E (2019) High-mountain altitudinal gradient influences thermal ecology of the Mesquite Lizard (Sceloporus grammicus). Can J Zool 97:659–668

  • Escudero PC, Minoli I, González-Marín MA, Morando M, Avila IJ (2016) Melanism and ontogeny: a case of study in lizards from Liolaemus fitzingerii group (Squamata: Liolaemini). Can J Zool 94:199–206

    Article  Google Scholar 

  • Geen MRS, Johnston GR (2014) Coloration affects heating and cooling in three color morphs of the Australian bluetongue lizard, Tiliqua scincoides. J Therm Biol 43:54–60

    Article  Google Scholar 

  • González-Morales JC, Beamonte-Barrientos R, Bastiaans E, Guevara-Fiore P, Quintana E, Fajardo V (2017) A mountain or a plateau? Hematological traits vary nonlinearly with altitude in a highland lizard. Physiol Biochem Zool 90:638–645

    Article  Google Scholar 

  • González-Morales JC, Rivera-Rea J, Moreno-Rueda G, Bastiaans E, Castro-López M, Fajardo V (2021a) Fast and dark: the case of Mezquite lizards at extreme altitude. J Therm Biol 102:103115

    Article  Google Scholar 

  • González-Morales JC, Rivera-Rea J, Moreno-Rueda G, Bastiaans E, Díaz-Albiter H, Díaz de la Vega-Pérez, Bautista AH, Fajardo A (2021b) V To be small and dark is advantageous for gaining heat in in mesquite lizard, Sceloporus grammicus (Squamata: Phynosomatidae). Biol J Linn Soc 132: 93–103

  • González-Morales JC, de la Díaz AH, Barrios-Montiel R, Quintana E, Moreno-Rueda G, Rivera-Rea J, Bastiaans E, Fajardo V (2023) Elevations and blood traits in mesquite lizard: are patterns repeatable among mountains? Comp Biochem Physiol A 276:111338

    Article  Google Scholar 

  • Green JP (1964) Morphological color change in the fiddler crab, Uca pugnax. Biol Bull 127:239–254

    Article  Google Scholar 

  • Guillette LJ, Casas-Andreu G (1980) Fall reproductive activity in the high altitude Mexican lizard, Sceloporus grammicus microlepidotus. J Herpetol 14:143–147

    Article  Google Scholar 

  • Gvozdík L (1999) Colour polymorphism in a population of the common lizard, Zootoca vivipara (Squamata: Lacertidae). Folia Zool 48:131–136

    Google Scholar 

  • Gvozdík 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

    Article  Google Scholar 

  • Harlow P, Grigg G (1984) Shivering thermogenesis in a brooding diamond python, Python spilotes spilites. Copeia 1984:959–965

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Huey RB (1974) Behavioural thermoregulation in lizards: importance of associated costs. Science 184:1001–1003

    Article  Google Scholar 

  • INEGI (2009) Instituto Nacional de Estadística, Geografía e Informática, Prontuario de información geográfica municipal de los Estados Unidos Mexicanos. Geostatistical key 15098 and 15004. http://www3.inegi.org.mx/contenidos/app/mexicocifras/datos_geograficos/15/15098.pdf

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

    Article  Google Scholar 

  • Kearny MR, Porter WP (2017) NichemapR- and R package for biophysical modelling: the microclimatic model. Ecography 40:664–674

    Article  Google Scholar 

  • Keller I, Alexander JM, Holderegger R, Edwards PJ (2013) Widespread phenotypic and genetic divergence along altitudinal gradients in animals. J Evol Biol 26:2527–2543

    Article  CAS  Google Scholar 

  • Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574

    Article  Google Scholar 

  • Langkilde T, Boronow KE (2012) Hot boys are blue: temperature-dependent color change in male eastern fence lizards. J Herpetol 2012: 46–465

  • Lembrechts JJ, Nijs I, Lenoir J (2019a) Incorporating microclimate into species distribution models. Ecography 42:1267–1279

  • Lembrechts JJ, Lenoir J, Roth N, Hattab T, Milbau A, Haider S, Pellissier L, Pauchard A, Ratier A, Dimarco RD, Nuñez MA, Aalto J, Nijs I (2019b) Comparing temperature data sources for use in species distribution models: from in-situ logging to remote sensing. Glob Ecol Biogeogr 28:1578–1596

    Article  Google Scholar 

  • Lemos-Espinal JA, Ballinger RE (1995) Comparative thermal ecology of the high-altitude lizard Sceloporus grammicus on the eastern slope of the Iztaccihuatl volcano, Puebla, Mexico. Can J Zool 73:2184–2191

    Article  Google Scholar 

  • Lenth R (2018) emmeans: estimated marginal means, aka least-squares means. v 1.2.2

  • Mackintosh JA (2001) The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J Theor Biol 211:101–113

    Article  CAS  Google Scholar 

  • Macotela L, Naya DE, González-Morales JC, Anaya M, Fajardo V, Manjarrez J (2023) Altitudinal variation in organ mass from three mountain system: the case of the mesquite lizard Sceloporus grammicus. Comp Biochem Physiol A 281:111426

    Article  CAS  Google Scholar 

  • Martín J, López P, Carrascal LM, Salvador A (1995) Adjustment of basking postures in the high-altitude Iberian rock lizard (Lacerta Monticola). Can J Zool 73:1065–1068

    Article  Google Scholar 

  • Medica PA, Hoddenbach GA, Lannom JR (1971) Lizard sampling techniques: Rock Valley. Misc Publs 1:1–55

    Google Scholar 

  • Megía-Palma R, Martínez J, Merino S (2016) A structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. Sci Nat 103:52

    Article  Google Scholar 

  • Moreno Azócar DL, Bonino MF, Perotti MG, Schulte JA, Abdala CS, Cruz FB (2016) Effect of body mass and melanism on heat balance in Liolaemus lizards of the Goetschi clade. J Exp Biol 219:1162–1171

    Google Scholar 

  • Moreno-Rueda G, González-Granda LG, Reguera S, Zamora-Camacho FJ, Melero E (2019) Crypsis decreases with elevation in a lizard. Diversity 11:236

    Article  Google Scholar 

  • Moreno-Rueda G, Reguera S, Zamora-Camacho FJ, Comas M (2021) Inter-individual differences in ornamental colouration in a mediterranean lizard in relation to altitude, season, sex, age, and body traits. Diversity 13:158

    Article  Google Scholar 

  • Muñoz MM, Bodensteiner BL (2019) Janzen’s hypothesis meets the Bogert effect: connecting climate variation, thermoregulatory behavior, and rates of physiological evolution. Integr Org Biol 1:oby002

    Article  Google Scholar 

  • Norris KS (1967) Color adaptation in desert reptiles and its thermal relationships. In Lizard ecology: a symposium (pp. 162–229)

  • Ortega Z, Mencía A, Pérez-Mellado V (2016) Behavioral buffering of global warming in a cold-adapted lizard. Ecol Evol 6:4582–4590

    Article  Google Scholar 

  • Porter WP, Norris KS (1969) Lizard reflectivity change and its effect on light transmission through body wall. Science 163:482–484

    Article  CAS  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • R Development Core Team (2017) A language and environment for statistical computing. R Foundation for Statistical Computing. R Development Core Team, Vienna, Austria

    Google Scholar 

  • Ravanat JL, Douki T, Cadet J (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B 63:88–102

    Article  CAS  Google Scholar 

  • Reguera S, Zamora-Camacho FJ, Moreno-Rueda G (2014a) The lizard Psammodromus Algirus (Squamata: Lacertidae) is darker at high altitudes. Biol J Linn Soc 112:132–141

    Article  Google Scholar 

  • Reguera S, Zamora-Camacho FJ, Trenzado CE, Sanz A, Moreno-Rueda G (2014b) Oxidative stress decreases with elevation in the lizard Psammodromus Algirus. Comp Biochem Physiol A 172:52–56

    Article  CAS  Google Scholar 

  • Rivera-Rea J, Macotela L, Moreno-Rueda G, Suárez-Varón G, Bastiaans E, Quintana E, González-Morales JC (2023) Thermoregulatory behavior varies with altitude and season in the sceloporine mesquite lizard. J Therm Biol 114:103539

    Article  CAS  Google Scholar 

  • Sanders CE, Tattersall GJ, Reichert M, Andrade DV, Abe AS, Milsom WK (2015) Daily and annual cycles in thermoregulatory behaviour and cardio-respiratory physiology of black and white tegu lizards. J Comp Physiol B 185:905–915

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass–size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Sears MW (2005) Resting metabolic expenditure as a potential source of variation in growth rates of the sagebrush lizard. Comp Biochem Physiol A 140:171–177

    Article  Google Scholar 

  • Sheehan G, Farrel G, Kavanagh K (2020) Immune priming: the secret weapon of the insect world. Virulence 11:238–246

    Article  CAS  Google Scholar 

  • Sherbrooke WC (1997) Physiological (rapid) change of color in Horned lizards. Amphib-Reptil 18:155–175

  • Sites JW, Archie JW, Cole CJ, Villela OF (1992) A review of phylogenetic hypotheses of the genus Sceloporus (Phrynosomatidae): implications for ecological and evolutionary studies. Bull Amer Mus Nat Hist 213:1–110

    Google Scholar 

  • Smith KR, Cadena V, Endler JA, Kearney MR, Porter WP, Stuart-Fox D (2016) Color change for thermoregulation versus camouflage in free-ranging lizards. Am Nat 188:668–678

    Article  Google Scholar 

  • Stephenson BP, Ihász N, Byrd DC, Swierk J, Swierk L (2017) Temperature-dependent colour change is a function of sex and directionality of temperature shift in the eastern fence lizard (Sceloporus undulatus). Biol J Linn Soc 120:396–409

    Google Scholar 

  • Stuart-Fox DM, Moussalli A, Johnston GR, Owens IPF (2004) Evolution of color variation in dragon lizards: quantitative tests of the role of crypsis and local adaptation. Evolution 58:1549–1559

    Google Scholar 

  • Stuart-Fox D, Whiting MJ, Moussalli A (2006) Camouflage and colour change: antipredator responses to bird and snake predators across multiple populations in a dwarf chameleon. Biol J Linn Soc 88:437–446

    Article  Google Scholar 

  • Stuart-Fox D, Newton E, Clusella-Trullas S (2017) Thermal consequences of color and near-infrared reflectance. Philos Trans R Soc Lond B Biol Sci 372:20160345

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tanaka K (2005) Thermal aspects of melanistic and striped morphs of the snake Elaphe quadrivirgata. Zool Sci 22:1173–1179

    Article  Google Scholar 

  • Tattersall GJ, Leite CA, Sanders CE, Cadena V, Andrade DV, Abe AS, Milsom WK (2016) Seasonal reproductive endothermy in tegu lizards. Sci Adv 2:e1500951

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zamora-Camacho FJ, Reguera S, Moreno-Rueda G (2014) Bergmann’s rule rules body size in an ectotherm: heat conservation in a lizard along a 2200-metre elevational gradient. J Evol Biol 27:2820–2828

    Article  CAS  Google Scholar 

  • Zamora-Camacho FJ, Reguera S, Moreno-Rueda G (2016) Thermoregulation in the lizard Psammodromus algirus along a 2200-m elevational gradient in Sierra Nevada (Spain). Int J Biometeorol 60:687–697

    Article  Google Scholar 

  • Zúñiga-Vega JJ, Méndez-de la Cruz FR, Cuellar O (2008) Body growth in one montane population of Sceloporus grammicus (Sauria, Phrynosomatidae) in Central Mexico. Amphib-Reptil 29:127–134

    Article  Google Scholar 

Download references

Funding

We are grateful to the Consejo Nacional de Ciencia y Tecnologí (Ph.D. degree scholarship JRR and JCGM).

Author information

Authors and Affiliations

Authors

Contributions

JRR and JCGM conceived and designed the experiments. JRR, EQ and, JCGM performed the experiments. JCGM, GMR, EB analyzed the data. JRR, JCGM, MP, and, GMR wrote the manuscript; other authors provided editorial advice.

Corresponding author

Correspondence to J. Carlos González-Morales.

Ethics declarations

Ethical approval

All experimental procedures were carried out following the guidelines of the Universidad Autónoma del Estado de México (UAEMéx), as well as the Mexican Federal Regulation for Animal Experimentation and Care (NOM-062-ZOO-2001; governmental approval SGPA/DGVS/ 02407/13).

Conflict of interest

the authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Supplementary Material 2

Supplementary Material 3

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Morales, J.C., Rivera-Rea, J., Moreno-Rueda, G. et al. Seasonal and altitudinal variation in dorsal skin reflectance and thermic rates in a high-altitude montane lizard. Int J Biometeorol (2024). https://doi.org/10.1007/s00484-024-02677-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00484-024-02677-7

Keywords

Navigation