The Science of Nature

, 103:97 | Cite as

An ecophysiological background for biogeographic patterns of two island lizards?

  • Miguel A. CarreteroEmail author
  • Evandro P. Lopes
  • Raquel Vasconcelos
Original Paper


Distributions of sedentary ectotherms are dependent on temperature and humidity due to their low homeostatic and dispersal abilities. Lizards are strongly conditioned by temperature, but hydric environment may be also important, at least in arid environments. Biotic interactions may also play a role in range patterns, but they are of minor importance in islands where native species monopolize well-delimited niche spaces. On the arid island of São Vicente (Cabo Verde), two endemic lizards display different spatial patterns. While the gecko Tarentola substituta is widely distributed across the island, the skink Chioninia stangeri is restricted to the NE, which is cooler, more humid, and vegetated. We hypothesized that this is due to differences in the fundamental niche, specifically in ecophysiology. We predict that C. stangeri should select for lower temperatures and lose more water by evaporation than T. substituta. We submitted adults of each species to standard experiments to assess preferred body temperatures (Tp) and evaporative water loss (EWL) rates, and examined the variation between species and through time using repeated-measures AN(C)OVAs. Results only partially supported our expectations. Contrary to the prediction, skinks attained higher Tp than geckos but in the long term showed a trend for higher EWL as predicted. Thus, while ecophysiology certainly contributes to functional interpretation of species distributions, it needs to be combined with other evidence such as habitat use and evolutionary history. These findings will be useful to perform mechanistic models to better understand the impact of climate change and habitat disturbance on these endemic species.


Reptiles Preferred temperatures Water loss rates Biogeography Arid systems 



This article is the output number 1 from the Twin-lLb CIBIO/InBIO-UniCV’s protocol. We thank the Departamento de Engenharias e Ciencias do Mar of the University of Cabo Verde for logistic support. This work was funded by Cabeólica S.A. and FEDER funds through the Operational Programme for Competitiveness Factors – COMPETE and by National Funds through Foundation for Science and Technology (FCT, Portugal) under the UID/BIA/50027/2013, POCI-01-0145-FEDER-006821, and FCOMP-01-0124-FEDER-008929 PTDC/BIA-BEC/101256/2008. RV was supported by a post-doctoral grant (SFRH⁄BPD⁄79913/2012) from FCT under the Programa Operacional Potencial Humano – Quadro de Referência Estratégico Nacional funds from the European Social Fund and Portuguese Ministério da Educação e Ciência. We also thank S. Delgado, P. Vasconcelos, Z. Monteiro, R. Monteiro, J. Ramos, S. da Luz, S. Delgado, M. Lourenço, E. Fernandes, M. Fortes, M dos Santos, and K. Delgado for field assistance.

Compliance with ethical standards

Ethical standards

Experiments followed the ethical guidelines of Universities of Cabo Verde and Porto. Study permit (no. 07/2016) was provided by Direcção Geral do Ambiente, Ministério do Ambiente, Habitação e Ordenamento do Território of Cabo Verde.


  1. Angilletta MJ Jr (2010) Thermal adaptation. Oxford University Press, OxfordGoogle Scholar
  2. Angilletta MJ Jr, Werner YL (1998) Australian geckos do not display diel variation in thermoregulatory behavior. Copeia 1998:736–742CrossRefGoogle Scholar
  3. Arad Z, Schwarzbaum A, Werner YL (1997) Temperature selection and thermoregulation in the Moorish gecko, Tarentola mauritanica. Amphibia-Reptilia 69:269–282CrossRefGoogle Scholar
  4. Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  5. Barroso FM, Carretero MA, Silva F, Sannolo M (2016) Using thermography to infer internal body temperatures of lizards. J. Therm Biol 62:90–96Google Scholar
  6. Bauwens D, Garland T Jr, Castilla AM, Van Damme R (1995) Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral Covariation. Evolution 49:848–863CrossRefGoogle Scholar
  7. Bocourt MF (1870) Description de quelques sauriens nouveaux originaires de l´Amérique méridionale. Nouvelles archives du Muséum d'histoire naturelle. 6:11–18Google Scholar
  8. Bowker RG (1993) The thermoregulation of the lizards Cnemidophorus exanguis and C. velox: some consequences of high body temperature. In: Wright JW, Vitts LJ (eds) Biology of whiptail lizards (genus Cnemidophorus). Oklahoma Museum Natural History, Norman, pp. 117–132Google Scholar
  9. Bowker RG, Bowker GE, Wright CL (2013) Thermoregulatory movement patterns of the lizard Podarcis carbonelli (Lacertilia: Lacertidae). J Therm Biol 38:454–457CrossRefGoogle Scholar
  10. Carneiro D, García-Muñoz E, Kalionzopoulou A, Llorente GA, Carretero MA (2015) Comparing ecophysiological traits in two Podarcis Wall lizards with overlapping ranges. Salamandra 51:335–344Google Scholar
  11. Carneiro D, García-Muñoz E, Žagar A, Pafilis P, Carretero MA (2017) Is ecophysiology congruent with the present-day relictual distribution of a lizard group? Evidence from preferred temperatures and water loss rates. Herpetol J 27:47–56Google Scholar
  12. Carretero MA (2008a) An integrated assessment of the specific status in a group with complex systematics: the Iberomaghrebian lizard genus Podarcis (Squamata, Lacertidae). Integr Zool 4:247–266CrossRefGoogle Scholar
  13. Carretero MA (2008b) Preferred temperatures of Tarentola mauritanica in spring. Acta Herpetol 3:57–64Google Scholar
  14. Carretero MA (2012) Measuring body temperatures in small lacertids: infrared vs. contact thermometers. Basic Appl Herpetol 26:99–105Google Scholar
  15. Carretero MA, Sillero N (2016) Evaluating how species niche modelling is affected by partial distributions with an empirical case. Acta Oecol 77:207–216Google Scholar
  16. Carretero MA, Roig JM, Llorente GM (2005) Variation in preferred body temperature in an oviparous population of Lacerta (Zootoca) vivipara. Herpetological J 15:51–55Google Scholar
  17. Davis MB, Shaw RG, Etterson JR (2005) Evolutionary responses to changing climate. Ecology 86:1704–1714CrossRefGoogle Scholar
  18. Dell Inc. (2015) Dell statistica (data analysis software system), version 13. Scholar
  19. Diniz AC, Matos GC (1994) Carta de zonagem Agro-Ecológica e da Vegetação de Cabo Verde VI e VII – Ilha de S. Vicente. Garcia de Orta. Série Botânica 12:69–100Google Scholar
  20. Eynan M, Dmi’el R (1993) Skin resistance to water loss in agamid lizards. Oecologia 95:290–294CrossRefGoogle Scholar
  21. Ferreira CC, Santos X, Carretero MA (2016) Does ecophysiology mediate reptile responses to fire regimes? Evidence from Iberian lizards. Peer J 4:e2107CrossRefPubMedPubMedCentralGoogle Scholar
  22. Ficetola GF, Thuiller W, Miaud C (2007) Prediction and validation of the potential global distribution of a problematic alien invasive species: the American bullfrog. Divers Distrib 13:476–485CrossRefGoogle Scholar
  23. García-Muñoz E, Carretero MA (2013) Comparative ecophysiology of two sympatric lizards. Laying the groundwork for mechanistic distribution models. Acta Herpetol 8:123–128Google Scholar
  24. Gil MJ, Guerrero F, Pérez-Mellado V (1994) Seasonal variation in the diet composition and prey selection of the Mediterranean gecko Tarentola mauritanica. Israel J Zool 40:61–74Google Scholar
  25. Gray JE (1845) Catalogue of the specimens of lizards in the collection of the British Museum. Trustees of the British Museum: LondonGoogle Scholar
  26. Hertz PE, Arima Y, Harrison A, Huey RB, Losos JB, Glor RE (2014) Asychronous evolution of physiology and morphology in Anolis lizards. Evolution 67:2101–2113CrossRefGoogle Scholar
  27. Hidalgo-Galiana A, Sánchez-Fernández D, Bilton DT, Cieslak A, Ribera I (2014) Thermal niche evolution and geographical range expansion in a species complex of western Mediterranean diving beetles. PLoS One 14:187Google Scholar
  28. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  29. Hódar JA, Pleguezuelos JM, Villafranca C, Fernández-Cardenete JR (2006) Foraging mode of the Moorish gecko Tarentola mauritanica in an arid environment: inferences from abiotic setting, prey availability and dietary composition. J Arid Environ 65:83–93CrossRefGoogle Scholar
  30. Huey RB, Bennett AF (1987) Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance temperatures of lizards. Evolution 41:1098–1115CrossRefGoogle Scholar
  31. Huey RB, Niewiaroswski PH, Kaufmann J, Herron JC (1989a) Thermal biology of nocturnal ectotherms: is sprint performance of geckos maximal at low body temperatures? Physiol Zool 62:488–504CrossRefGoogle Scholar
  32. Huey RB, Peterson CR, Arnold SJ, Porter WP (1989b) Hot rocks and not-so-hot rocks: retreat-site selection by garter snakes and its thermal consequences. Ecology 70:931–944CrossRefGoogle Scholar
  33. Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B: Biological Sciences 367 (1596):1665–1679Google Scholar
  34. Joger U (1984) Die radiation der gattung Tarentola in Makaronesien (Reptilia: Sauria: Gekkonidae). Courier Forschungsinstitut Senckenberg 71:91–111Google Scholar
  35. Kearney M, Porter WP (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species ranges. Ecol Lett 12:334–350CrossRefPubMedGoogle Scholar
  36. Kratochvíl L, Frynta D (2005) Egg shape and size allometry in geckos (Squamata: Gekkota), lizards with contrasting eggshell structure: why lay spherical eggs? J Zool Sys Evol Res 44:217–222CrossRefGoogle Scholar
  37. Labra A (2009) Evolution of thermal physiology in Liolaemus lizards: adaptation, phylogenetic inertia, and niche tracking. Am Nat 174:204–220CrossRefPubMedGoogle Scholar
  38. Lara-Reséndiz RA, Gadsden H, Rosen PC, Sinervo B, Méndez-de-la-Cruz FR (2015) Thermoregulation of two sympatric species of horned lizards in the Chihuahuan Desert and their local extinction risk. J Therm Biol 48:1–10CrossRefPubMedGoogle Scholar
  39. Lomolino MV, Riddle BR, Whittaker RJ, Brown JH (2010) Biogeography. 4th Edition. Sinauer Associates, SunderlandGoogle Scholar
  40. Lorenzon P, Clobert J, Oppliger A, John-Alder HB (1999) Effect of water constraint on growth rate, activity and body temperature of yearling common lizard (Lacerta vivipara). Oecologia 118:423–430CrossRefGoogle Scholar
  41. Mautz WJ (1982a) Patterns of evaporative water loss. In: Gans C, Pough FH (eds) Biology of the Reptilia Vol. 12. Academic Press, New York, pp. 443–481Google Scholar
  42. Mautz WJ (1982b) Correlation of both respiratory and cutaneous water losses of lizards with habitat aridity. J Comp Physiol B 149:25–30CrossRefGoogle Scholar
  43. Medina A, Brêthes J, Sévigny J, Zakardjian B (2007) How geographic distance and depth drive ecological variability and isolation of demersal fish communities in an archipelago system (Cape Verde, Eastern Atlantic Ocean). Mar Ecol 3:404–417CrossRefGoogle Scholar
  44. Medina M, Scolaro A, Méndez-de-la-Cruz FR, Sinervo B, Miles DB, Ibargüengoytía NR (2012) Thermal biology of genus Liolaemus: a phylogenetic approach reveals advantages of the genus to survive climate change. J Therm Biol 37:579–586CrossRefGoogle Scholar
  45. Miralles A, Vasconcelos R, Harris DJ, Perera A, Carranza S (2010) An integrative taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae). Zool Scripta 40:16–44CrossRefGoogle Scholar
  46. Neilson KA (2002) Evaporative water loss as a restriction on habitat use in endangered New Zealand endemic skinks. J Herpetol 36:342–348CrossRefGoogle Scholar
  47. Osojnik N, Žagar A, Carretero MA, García-Muñoz E, Vrezec A (2013) Ecophysiological dissimilarities of two sympatric lizards. Herpetologica 69:445–454CrossRefGoogle Scholar
  48. Pianka ER, Vitt LJ (2006) Lizards: windows to the evolution of diversity. University of California Press, BerkeleyGoogle Scholar
  49. Porter WP, Tracy CR (1983) Biophysical analyses of energetics, time-space utilization, and distributional limits. In: Huey RB, Pianka ER, Schoener TW (eds) Lizard ecology studies on a model organism. Harvard University Press, Cambridge, pp. 55–83Google Scholar
  50. Pulliam HR (2000) On the relationship between niche and distribution. Ecol Lett 3:349–361CrossRefGoogle Scholar
  51. Rato C, Carretero MA (2015) Ecophysiology tracks phylogeny and meets ecological models in an Iberian gecko. Physiol Biochem Zool 88:564–575CrossRefPubMedGoogle Scholar
  52. Ribeiro R, Santos X, Sillero N, Carretero MA, Llorente GA (2009) Biodiversity and land uses: is agriculture the biggest threat for reptiles’ assemblages? Acta Oecol 35:327–334CrossRefGoogle Scholar
  53. Sannolo M, Mangiacotti M, Sacchi R, Scali S (2014) Keeping a cool mind: head-body temperature differences in the common wall lizard. J Zool 293:71–79CrossRefGoogle Scholar
  54. Schmidt-Nielsen K (1984) Scaling: why is animal size so important? Cambridge University Press, New YorkCrossRefGoogle Scholar
  55. Sears MW, Angilletta MJ Jr (2015) Costs and benefits of thermoregulation revisited: both the heterogeneity and spatial structure of temperature drive energetic costs. Am Nat 185:e94–102CrossRefPubMedGoogle Scholar
  56. Sears MW, Angilletta MJ Jr, Schuler MS, Borchert GM, Dilliplane KL, Stegman M, Rusch TW, Mitchell WA (2016) Configuration of the thermal landscape determines thermoregulatory performance of ectotherms. Proc Natl Acad Sci U S A 113:10595–10600CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sillero N (2011) What does ecological modelling model? A proposed classification of ecological niche models based on their underlying methods. Ecol Model 222:1343–1346CrossRefGoogle Scholar
  58. Sinervo B, Méndez-de-la-Cruz FR, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz RA, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Avila LJ, Morando M, de la Riva I, Sepúlveda PV, Rocha CFD, Ibargüengoytía NR, Aguilar Puntriano C, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW Jr (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899CrossRefPubMedGoogle Scholar
  59. Soberon J, Nakamura M (2009) Niches and distributional areas: concepts, methods, and assumptions. Proc Natl Acad Sci U S A 106:19644–19650CrossRefPubMedPubMedCentralGoogle Scholar
  60. Templeton AR (2002) Out of Africa again and again. Nature 416:45–51CrossRefPubMedGoogle Scholar
  61. Valenzuela-Ceballos S, Castañeda G, Rioja-Paradela T, Carrillo-Reyes A, Bastiaans E (2015) Variation in the thermal ecology of an endemic iguana from Mexico reduces its vulnerability to global warming. J Therm Biol 48:56–64CrossRefPubMedGoogle Scholar
  62. Vasconcelos R, Brito JC, Carvalho SB, Carranza S, Harris DJ (2012a) Identifying priority areas for island endemics using genetic versus specific diversity—the case of terrestrial reptiles of the Cape Verde Islands. Biol Conserv 153:276–286CrossRefGoogle Scholar
  63. Vasconcelos R, Perera A, Geniez P, Harris DJ, Carranza S (2012b) An integrative taxonomic revision of the Tarentola geckos (Squamata, Phyllodactylidae) of the Cape Verde islands. Zool J Linnean Soc 164:328–360CrossRefGoogle Scholar
  64. Vasconcelos R, Santos X, Carretero MA (2012c) High temperatures constrain microhabitat selection and activity patterns by the insular Cape Verde wall gecko. J Arid Environ 81:18–25CrossRefGoogle Scholar
  65. Vasconcelos R, Brito JC, Carranza S, Harris DJ (2013) Review of the distribution and conservation status of the terrestrial reptiles of the Cape Verde Islands. Oryx 47:77–87CrossRefGoogle Scholar
  66. Veríssimo CV, Carretero MA (2009) Preferred temperatures of Podarcis vaucheri from Morocco: intraspecific variation and interspecific comparisons. Amphibia-Reptilia 30:17–23CrossRefGoogle Scholar
  67. Vitt LJ, Pianka ER (2005) Deep history impacts present-day ecology and biodiversity. Proc Natl Acad Sci U S A 102:7877–7881CrossRefPubMedPubMedCentralGoogle Scholar
  68. Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography: ecology, evolution, and conservation. Oxford University Press, OxfordGoogle Scholar
  69. Wiens JA, Stralberg D, Jongsomjit D, Howell CA, Snyder MA (2009) Niches, models, and climate change: assessing the assumptions and uncertainties. Proc Natl Acad Sci U S A 106:19729–19736CrossRefPubMedPubMedCentralGoogle Scholar
  70. Zheng Y, Wiens JJ (2016) Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol Phylogenet Evol 94:537–547CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.CIBIO Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIOUniversidade do PortoVila do CondePortugal
  2. 2.UniCV, Faculdade de Engenharias e Ciências do MarUniversidade de Cabo Verde, São VicenteMindeloCabo Verde
  3. 3.Institute of Evolutionary Biology (CSIC-UPF)BarcelonaSpain

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