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Disentangling the role of heat sources on microhabitat selection of two Neotropical lizard species

Published online by Cambridge University Press:  22 April 2019

Zaida Ortega*
Affiliation:
Programa de Pós-Graduação em Ecologia e Conservação, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, ZIP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil
Abraham Mencía
Affiliation:
Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências, Universidade Federal do Mato Grosso do Sul, ZIP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil
Kleber Martins
Affiliation:
Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências, Universidade Federal do Mato Grosso do Sul, ZIP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil
Priscilla Soares
Affiliation:
Programa de Pós-Graduação em Ecologia e Conservação, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, ZIP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil
Vanda Lúcia Ferreira
Affiliation:
Instituto de Biociências, Universidade Federal do Mato Grosso do Sul, ZIP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil
Luiz Gustavo Oliveira-Santos
Affiliation:
Instituto de Biociências, Universidade Federal do Mato Grosso do Sul, ZIP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil

Abstract

Our aim was to disentangle the effects of different heat sources and the non-thermal properties of the substrate in the microhabitat choices of two lizard species living in savanna habitats of central-western Brazil: the teiid Ameivula aff. ocellifera (N = 43) and the tropidurid Tropidurus oreadicus (N = 23). To this end, a mixed structural resource selection function (mixed-SRSF) approach was used, modelling the probability of finding a lizard on a certain microhabitat based on environmental variables of used and simultaneously available places. First, we controlled for the effects of solar radiation, convection and the physical thermal properties of the substrate on substrate temperature. Then we assessed the effects of solar radiation, convection, conduction and the non-thermal properties of the substrate in the probability of use of a certain microhabitat. Results confirmed that substrate temperature was mediated by: air convection > solar radiation > physical thermal properties of the substrates. Moreover, the mixed-SRSF revealed that direct solar radiation and the non-thermal properties of the substrates were the only drivers of microhabitat selection for both species, with approximately the same strength. Our novel approach allowed splitting of the effect of different mechanisms in the microhabitat selection of lizards, which makes it a powerful tool for assessing the conformation of the interactions between different environmental variables mediating animal behaviour.

Type
Research Article
Copyright
© Cambridge University Press 2019 

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References

Literature cited

Addo-Bediako, AA, Chown, SL and Gaston, KJ (2000) Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society B 267, 739745.10.1098/rspb.2000.1065CrossRefGoogle ScholarPubMed
Allen, KE, Rodríguez, KJA, Eifler, DA and Powell, R (2015) Social and environmental factors influence microhabitat selection in the brown-speckled sphaero, Sphaerodactylus notatus (Squamata: Sphaerodactylidae). Journal of Herpetology 49, 165169.10.1670/13-120CrossRefGoogle Scholar
Angilletta, MJ (2009) Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford: Oxford University Press, 302 pp.10.1093/acprof:oso/9780198570875.001.1CrossRefGoogle Scholar
Arias, F, Carvalho, CM, Rodrigues, M and Zaher, H (2011a) Two new species of Cnemidophorus (Squamata: Teiidae) of the C. ocellifer group, from Bahia, Brazil. Zootaxa 3022, 121.10.11646/zootaxa.3022.1.1CrossRefGoogle Scholar
Arias, F, Carvalho, CM, Rodrigues, FS and Zaher, H (2011b) Two new species of Cnemidophorus (Squamata: Teiidae) from the Caatinga, Northwest Brazil. Zootaxa 2787, 3754.10.11646/zootaxa.2787.1.3CrossRefGoogle Scholar
Arias, FJ, Recoder, R, Álvarez, BB, Ethcepare, E, Quipildor, M, Lobo, F and Rodrigues, MT (2018) Diversity of teiid lizards from Gran Chaco and Western Cerrado (Squamata: Teiidae). Zoologica Scripta 47, 144158.10.1111/zsc.12277CrossRefGoogle Scholar
Belliure, J and Carrascal, LM (2002) Influence of heat transmission mode on heating rates and on the selection of patches for heating in a Mediterranean lizard. Physiological and Biochemical Zoology 75, 369376.10.1086/342768CrossRefGoogle Scholar
Bergier, I and Assine, M (2016) Dynamics of the Pantanal Wetland in South America. New York, NY: Springer International Publishing, 243 pp.10.1007/978-3-319-18735-8CrossRefGoogle Scholar
Blouin-Demers, G and Weatherhead, PJ (2001) An experimental test of the link between foraging, habitat selection and thermoregulation in black rat snakes Elaphe obsoleta obsoleta. Journal of Animal Ecology 70, 10061013.10.1046/j.0021-8790.2001.00554.xCrossRefGoogle Scholar
Brusch, GA, Taylor, EN and Whitfield, SM (2016) Turn up the heat: thermal tolerances of lizards at La Selva, Costa Rica. Oecologia 180, 325334.10.1007/s00442-015-3467-3CrossRefGoogle Scholar
Carrascal, LM, López, P, Martín, J and Salvador, A (1992) Basking and antipredator behaviour in a high altitude lizard: implications of heat-exchange rate. Ethology 92, 143154.10.1111/j.1439-0310.1992.tb00955.xCrossRefGoogle Scholar
Castilla, AM and Bauwens, D (1991) Thermal biology, microhabitat selection, and conservation of the insular lizard Podarcis hispanica atrata. Oecologia 85, 366374.10.1007/BF00320612CrossRefGoogle ScholarPubMed
Compton, BW, Rhymer, JM and McCollough, M (2002) Habitat selection by Wood Turtles (Clemmys insculpta): an application of paired logistic regression. Ecology 83, 833843.10.2307/3071885CrossRefGoogle Scholar
Da Silva, RG, Maia, ASC and Macedo-Costa, LL (2014) Index of thermal stress for cows (ITSC) under high solar radiation in tropical environments. International Journal of Biometeorology 59, 551559.10.1007/s00484-014-0868-7CrossRefGoogle ScholarPubMed
Díaz, JA and Cabezas-Díaz, S (2004) Seasonal variation in the contribution of different behavioural mechanisms to lizard thermoregulation. Functional Ecology 18, 867875.10.1111/j.0269-8463.2004.00916.xCrossRefGoogle Scholar
Doody, JS, Guarino, E, Georges, A, Corey, B, Murray, G and Ewert, M (2006) Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evolutionary Ecology 20, 307330.10.1007/s10682-006-0003-2CrossRefGoogle Scholar
Duchesne, T, Fortin, D and Courbin, N (2010) Mixed conditional logistic regression for habitat selection studies. Journal of Animal Ecology 79, 548555.10.1111/j.1365-2656.2010.01670.xCrossRefGoogle ScholarPubMed
Grbac, I and Bauwens, D (2001) Constraints on temperature regulation in two sympatric Podarcis lizards during autumn. Copeia 2001, 178186.10.1643/0045-8511(2001)001[0178:COTRIT]2.0.CO;2CrossRefGoogle Scholar
Heatwole, H (2009) Grand challenges. Integrative and Comparative Biology 49, 6.10.1093/icb/icp042CrossRefGoogle ScholarPubMed
Hertz, PE, Fleishman, LT and Armsbury, C (1994) The influence of light intensity and temperature on microhabitat selection in two Anolis lizards. Functional Ecology 8, 720729.10.2307/2390231CrossRefGoogle Scholar
Hillebrand, H (2004) On the generality of the latitudinal diversity gradient. American Naturalist 163, 192211.10.1086/381004CrossRefGoogle ScholarPubMed
Holst, KK and Budtz-Jørgensen, E (2013) Linear latent variable models: the lava-package. Computational Statistics 28, 13851452.10.1007/s00180-012-0344-yCrossRefGoogle Scholar
Huey, RB (1991) Physiological consequences of habitat selection. American Naturalist 137, S91S115.10.1086/285141CrossRefGoogle Scholar
Huey, RB, Deutsch, CA, Tewksbury, JJ, Vitt, LJ, Hertz, PE, Pérez, HJÁ and Garland, T (2009) Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society of London B: Biological Sciences 276, 19391948.10.1098/rspb.2008.1957CrossRefGoogle ScholarPubMed
Jaksić, FM, Núnez, H and Ojeda, FP (1980) Body proportions, microhabitat selection, and adaptive radiation of Liolaemus lizards in central Chile. Oecologia 45, 178181.10.1007/BF00346457CrossRefGoogle ScholarPubMed
Janzen, DH (1967) Why mountain passes are higher in the tropics. American Naturalist 101, 233249.10.1086/282487CrossRefGoogle Scholar
Kearney, M, Shine, R and Porter, WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proceedings of the National Academy of Sciences USA 106, 38353840.10.1073/pnas.0808913106CrossRefGoogle ScholarPubMed
Kearney, MR, Isaac, AP and Porter, WP (2014a) microclim: global estimates of hourly microclimate based on long-term monthly climate averages. Science Data 1, 140006.10.1038/sdata.2014.6CrossRefGoogle ScholarPubMed
Kearney, MR, Shamakhy, A, Tingley, R, Karoly, DJ, Hoffmann, AA, Briggs, PR and Porter, WP (2014b) Microclimate modelling at macro scales: a test of a general microclimate model integrated with gridded continental-scale soil and weather data. Methods in Ecology and Evolution 5, 273286.10.1111/2041-210X.12148CrossRefGoogle Scholar
Kottek, M, Grieser, J, Beck, C, Rudolf, B and Rubel, F (2006) World map of the Köppen–Geiger climate classification updated. Meteorologische Zeitschrift 15, 259263.10.1127/0941-2948/2006/0130CrossRefGoogle Scholar
Maia-Carneiro, T, Dorigo, TA and Rocha, CFD (2012) Influences of seasonality, thermal environment and wind intensity on the thermal ecology of Brazilian sand lizards in a restinga remnant. South American Journal of Herpetology 7, 241251.10.2994/057.007.0306CrossRefGoogle Scholar
Manly, BFJ, McDonald, LL, Thomas, DL, McDonald, TL and Erickson, WP (2002) Resource Selection by Animals: Statistical Design and Analysis for Field Studies. New York, NY: Springer, 233 pp.Google Scholar
Marshall, KLA, Philpot, KE and Stevens, M (2016) Microhabitat choice in island lizards enhances camouflage against avian predators. Science Reports 6, 110.Google ScholarPubMed
Martín, J and Salvador, A (1997) Microhabitat selection by the Iberian rock lizard Lacerta monticola: effects on density and spatial distribution of individuals . Biological Conservation 79, 303307.10.1016/0006-3207(95)00110-7CrossRefGoogle Scholar
Menezes, VA, Sluys Van, M, Fontes, AF and Rocha, CFD (2011) Living in a caatinga-rocky field transitional habitat: ecological aspects of the whiptail lizard Cnemidophorus ocellifer (Teiidae) in northeastern Brazil. Zoologia (Curitiba) 28, 816.10.1590/S1984-46702011000100002CrossRefGoogle Scholar
Mesquita, D and Colli, GR (2003) The ecology of Cnemidophorus ocellifer (Squamata, Teiidae) in a neotropical savanna. Journal of Herpetology 37, 498509.10.1670/179-02ACrossRefGoogle Scholar
Newbold, TAS and MacMahon, JA (2014) Determinants of habitat selection by desert horned lizards (Phrynosoma platyrhinos): the importance of abiotic factors associated with vegetation structure. Journal of Herpetology 48, 306316.10.1670/10-141CrossRefGoogle Scholar
Ortega, Z and Pérez-Mellado, V (2016) Seasonal patterns of body temperature and microhabitat selection in a lacertid lizard. Acta Oecologica 77, 201206.10.1016/j.actao.2016.08.006CrossRefGoogle Scholar
Ortega, Z and Pérez-Mellado, V (2017) The effect of thermal requirements on microhabitat selection and activity of Podarcis lilfordi (Squamata: Lacertidae). Salamandra 53, 351358.Google Scholar
Ortega, Z, Mencía, A and Pérez-Mellado, V (2017) Wind constraints on the thermoregulation of high mountain lizards. International Journal of Biometeorology 61, 19.10.1007/s00484-016-1233-9CrossRefGoogle ScholarPubMed
Paterson, JE and Blouin-Demers, G (2018) Density-dependent habitat selection predicts fitness and abundance in a small lizard. Oikos 127, 448459.10.1111/oik.04758CrossRefGoogle Scholar
Pianka, ER, Vitt, LJ, Pelegrin, N, Fitzgerald, DB and Winemiller, KO (2017) Toward a periodic table of niches, or exploring the lizard niche hypervolume. American Naturalist 190, 601616.10.1086/693781CrossRefGoogle ScholarPubMed
Pontes-da-Silva, E, Magnusson, WE, Sinervo, B, Caetano, GH, Miles, DB, Colli, GR, Diele-Viegas, LM, Fenker, J, Santos, JC and Werneck, FP (2018) Extinction risks forced by climatic change and intraspecific variation in the thermal physiology of a tropical lizard. Journal of Thermal Biology 73, 5060.10.1016/j.jtherbio.2018.01.013CrossRefGoogle ScholarPubMed
Porter, WP and Gates, DM (1969) Thermodynamic equilibria of animals with environment. Ecological Monographs 39, 227244.10.2307/1948545CrossRefGoogle Scholar
Porter, WP, Mitchell, JW, Beckman, WA and DeWitt, CB (1973) Behavioral implications of mechanistic ecology. Oecologia 13, 154.10.1007/BF00379617CrossRefGoogle ScholarPubMed
Quirt, KC, Blouin-Demers, G, Howes, BJ and Lougheed, SC (2006) Microhabitat selection of five-lined skinks in northern peripheral populations. Journal of Herpetology 40, 335342.10.1670/0022-1511(2006)40[335:MSOFSI]2.0.CO;2CrossRefGoogle Scholar
Ribeiro, LB, Gomides, SC, Santos, AO and Sousa, BM (2008) Thermoregulatory behavior of the saxicoious lizard, Tropidurus torquatus (Squamata, Tropiduridae), in a rocky outcrop in Minas Gerais, Brazil. Herpetological Conservation and Biology 3, 6370.Google Scholar
Rocha, CFD and Siqueira, CC (2008) Feeding ecology of the lizard Tropidurus oreadicus Rodrigues 1987 (Tropiduridae) at Serra dos Carajás, Pará state, northern Brazil. Brazilian Journal of Biology 68, 109113.10.1590/S1519-69842008000100015CrossRefGoogle ScholarPubMed
Ruibal, R (1961) Thermal relations of five species of tropical lizards. Evolution 15, 98111.10.1111/j.1558-5646.1961.tb03132.xCrossRefGoogle Scholar
Sathe, EA and Husak, JF (2018) Substrate-specific locomotor performance is associated with habitat use in six-lined racerunners (Aspidoscelis sexlineata). Biological Journal of the Linnean Society 124, 165173.10.1093/biolinnean/bly039CrossRefGoogle Scholar
Schwenk, K, Padilla, DK, Bakken, GS and Full, RJ (2009) Grand challenges in organismal biology. Integrative and Comparative Biology 49, 714.10.1093/icb/icp034CrossRefGoogle ScholarPubMed
Sears, MW and Angilletta, MJ (2015) Costs and benefits of thermoregulation revisited: both the heterogeneity and spatial structure of temperature drive energetic costs. American Naturalist 185, E94E102.10.1086/680008CrossRefGoogle ScholarPubMed
Sears, MW, Angilletta, MJ, Schuler, MS, Borchert, J, Dilliplane, KF, Stegman, M, Rusch, TW and Mitchell, WA (2016) Configuration of the thermal landscape determines thermoregulatory performance of ectotherms. Proceedings of the National Academy of Sciences USA 113, 1059510600.10.1073/pnas.1604824113CrossRefGoogle ScholarPubMed
Shipley, B (2016) Cause and Correlation in Biology: A User’s Guide to Path Analysis, Structural Equations and Causal Inference with R. Cambridge: Cambridge University Press, 315 pp.10.1017/CBO9781139979573CrossRefGoogle Scholar
Smith, GR and Ballinger, RE (2001) The ecological consequences of habitat and microhabitat use in lizards: a review. Contemporary Herpetology 2001, 113.Google Scholar
Tewksbury, JJ, Huey, RB and Deutsch, CA (2008) Putting the heat on tropical animals. Science 320, 1296.10.1126/science.1159328CrossRefGoogle ScholarPubMed
Vickers, M, Manicom, C and Schwarzkopf, L (2011) Extending the cost-benefit model of thermoregulation: high-temperature environments. American Naturalist 177, 452461.10.1086/658150CrossRefGoogle ScholarPubMed