Behavioral compensation buffers body temperatures of two Liolaemus lizards under contrasting environments from the temperate Pampas: a Bogert effect?

REFERENCES

• Abdala CS, Quinteros AS. 2014. Los últimos 30 años de estudios de la familia de lagartijas más diversa de Argentina: actualización taxonómica y sistemática de Liolaemidae. [The last 30 years of study of the most diverse family of lizards in Argentina: a taxonomic and systematic update of Liolaemidae]. Cuad Herpetol. 28:55–82. Spanish.
   Google Scholar
• Adolph SC. 1990. Influence of behavioral thermoregulation on microhabitat use by two Sceloporus lizards. Ecology. 71:315–327.
   Web of Science ®Google Scholar
• Andrews RM. 1998. Geographic variation in field body temperature of Sceloporus lizards. J Therm Biol. 23:329–334.
   Web of Science ®Google Scholar
• Andrews RM, Méndez de la Cruz FR, Villagrán-Santa Cruz M, Rodríguez-Romero F. 1999. Field and selected body temperatures of the lizards Sceloporus aeneus and Sceloporus bicanthalis. J Herpetol. 33:93–100.
   Web of Science ®Google Scholar
• Artacho P, Saravia J, Perret S, Bartheld JL, Le Galliard JF. 2017. Geographic variation and acclimation effects on thermoregulation behavior in the widespread lizard Liolaemus pictus. J Therm Biol. 63:78–87.
   PubMed Web of Science ®Google Scholar
• Austin M. 2007. Species distribution models and ecological theory: a critical assessment and some possible new approaches. Ecol Modell. 200:1–19.
   Web of Science ®Google Scholar
• Avery RA. 1982. Field studies of body temperatures and thermoregulation. In: Gans C, Pough FH, editors. Biology of the Reptilia: physiological ecology. London (UK): Academic Press; p. 93–l66.
   Google Scholar
• Bakken GS. 1989. Arboreal perch properties and the operative temperature experienced by small animals. Ecology. 70:922–930.
   Web of Science ®Google Scholar
• Basson CH 2013. Thermal adaptation in the lizard Cordylus oelofseni: physiological and behavioural responses to temperature variation [ Master Thesis]. South Africa: Stellenbosch University.
   Google Scholar
• Basson CH, Clusella-Trullas S. 2015. The behavior-physiology nexus: behavioral and physiological compensation are relied on to different extents between seasons. Physiol Biochem Zool. 88:384–394.
   PubMed Web of Science ®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.
   Web of Science ®Google Scholar
• Block C, Stellatelli OA, García GO, Vega LE, Isacch JP. 2013. Factors affecting the thermal behavior of the sand lizard Liolaemus wiegmannii in natural and modified grasslands of temperate coastal dunes from Argentina. J Therm Biol. 38:560–569.
   Web of Science ®Google Scholar
• Bogert CM. 1949. Thermoregulation in reptiles, a factor in evolution. Evolution. 3:195–211.
   PubMed Web of Science ®Google Scholar
• Bogert CM. 1959. How reptiles regulate their body temperature. Sci Am. 200:105–120.
   Web of Science ®Google Scholar
• Bonino MF, Moreno Azócar DL, Tulli MJ, Abdala CS, Perotti MG, Cruz FB. 2011. Running in cold weather: morphology, thermal biology and performance in the southernmost lizard clade in the world (Liolaemus lineomaculatus section: Liolaemini: Iguania). J Exp Zool. 315:495–503.
   Google Scholar
• Bouazza A, Slimani T, El Mouden H, Blouin-Demers G, Lourdais O. 2016. Thermal constraints and the influence of reproduction on thermoregulation in a high-altitude gecko (Quedenfeldtia trachyblepharus). J Zool. 300:36–44.
   Web of Science ®Google Scholar
• Bujes CS, Verrastro L. 2006. Thermal biology of Liolaemus occipitalis (Squamata, Tropiduridae) in the coastal sand dunes of Rio Grande do Sul, Brazil. Braz J Biol. 66:945–954.
   PubMedGoogle Scholar
• Bujes CS, Verrastro L. 2008. Annual activity of the lizard Liolaemus occipitalis (Squamata, Liolaemidae) in the coastal sand dunes of southern Brazil. Iheringia Sér Zool. 98:156–160.
   Web of Science ®Google Scholar
• Burger J, Gochfeld M. 1993. The importance of the human face in risk perception by black iguanas Ctenosaura similis. J Herpetol. 27:426–430.
   Web of Science ®Google Scholar
• Burgos JJ, Vidal AL. 1995. Los climas de la República Argentina según la nueva clasificación de Thornthwaite. [The climates of the Argentine Republic according to the new Thornthwaite classification]. Meteoros. 1:3–32. Spanish.
   Google Scholar
• Burkart R, Bárbaro NO, Sánchez RO, Gómez DA. 1999. Eco-regiones de la Argentina. [Eco-regions of Argentina]. Buenos Aires (BA): Administración de Parques Nacionales. Spanish.
   Google Scholar
• Burnham KP, Anderson DR, editors. 2002. Model selection and multimodel inference: a practical information-theoretic approach. New York (NY): Springer-Verlag.
   Google Scholar
• Cabrera AL. 1976. Regiones fitogeográficas argentinas. [Argentinian phytogeographical regions]. Enciclopedia Argentina de Agricultura y Jardinería. Buenos Aires (BA): ACME. Spanish.
   Google Scholar
• Cadena V, Tattersall GJ. 2009. The effect of thermal quality on the thermoregulatory behavior of the Bearded Dragon Pogona vitticeps: influences of methodological assessment. Physiol Biochem Zool. 82:203–217.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Carothers JH, Jaksic FM, Marquet PA. 2001. Altitudinal zonation among lizards of the genus Liolaemus: questions answered and unanswered questions. Rev Chil Hist Nat. 74:313–316.
   Web of Science ®Google Scholar
• Carothers JH, Marquet PA, Jaksic FM. 1998. Thermal ecology of a Liolaemus lizard assemblage along an Andean altitudinal gradient in Chile. Rev Chil Hist Nat. 71:39–50.
   Web of Science ®Google Scholar
• Castilla AM, Van Damme R, Bauwens D. 1999. Field body temperatures, mechanisms of thermoregulation and evolution of thermal characteristics in lacertid lizards. Nat Croat. 8:253–274.
   Google Scholar
• Cei JM. 1993. Reptiles del centro, centro oeste y sur de la Argentina. Monogr. IV. [Reptiles of the Center, Central-West and South of Argentina. Monogr. IV]. Torino: Museo Regionale di Scienze Naturali. Spanish.
   Google Scholar
• Corbalán V, Debandi G. 2013. Basking behaviour in two sympatric herbivorous lizards (Liolaemidae: Phymaturus) from the Payunia volcanic region of Argentina. J Nat Hist. 47:1365–1378.
   Web of Science ®Google Scholar
• Crawley MJ. 2007. The R book. Chichester (UK): John Wiley and Sons.
   Google Scholar
• Cruz FB, Fitzgerald LA, Espinoza RE, Schulte JAII. 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. 18:1559–1574.
   PubMed Web of Science ®Google Scholar
• Cruz FB, Moreno Azócar DL, Bonino MF, Schulte JA II, Abdala CS, Perotti MG. 2014. Clima, distribución geográfica y viviparismo en especies de Liolaemus (Reptilia; Squamata): cuando las hipótesis se ponen a prueba. [Climate, geographic distribution and viviparism in Liolaemus species (Reptilia; Squamata): when the hypotheses are tested]. Ecosistemas. 23:37–45. Spanish.
   Google Scholar
• Díaz JA, Cabezas-Díaz S. 2004. Seasonal variation in the contribution of different behavioural mechanisms to lizard thermoregulation. Funct Ecol. 18:867–875.
   Web of Science ®Google Scholar
• Díaz JA, Díaz-Uriarte R, Rodríguez A. 1996. Influence of behavioral thermoregulation on the use of vertical surfaces by Iberian wall lizards Podarcis hispanica. J Herpetol. 30:548–552.
   Web of Science ®Google Scholar
• Downes S, Shine R. 1998. Heat, safety or solitude? Using habitat selection experiments to identify a lizard’s priorities. Anim Behav. 55:1387–1396.
   PubMed Web of Science ®Google Scholar
• Duran F, Kubisch EL, Boretto JM. 2017. Thermal physiology of three sympatric and syntopic Liolaemidae lizards in cold and arid environments of Patagonia (Argentina). J Comp Physiol B. doi:10.1007/s00360-017-1116-3
   PubMedGoogle Scholar
• Etheridge R. 2000. A review of lizards of the L. wiegmannii group (Squamata, Iguania, Tropiduridae) and a history of morphological change in the sand-dwelling species. Herpetol Monogr. 14:293–352.
   Web of Science ®Google Scholar
• Grbac I, Bauwens D. 2001. Constraints on temperature regulation in two sympatric Podarcis lizards during autumn. Copeia. 1:178–186.
   Google Scholar
• Gutiérrez JA, Krenz JD, Ibargüengoytía NR. 2010. Effect of altitude on thermal responses of Liolaemus pictus argentinus in Argentina. J Therm Biol. 35:332–337.
   Web of Science ®Google Scholar
• Hadamová M, Gvoždík L. 2011. Seasonal acclimation of preferred body temperatures improves the opportunity for thermoregulation in newts. Physiol Biochem Zool. 84:166–174.
   PubMed Web of Science ®Google Scholar
• Hertz PE, Huey RB. 1981. Compensation for altitudinal changes in the thermal environment by some Anolis lizards on Hispaniola. Ecology. 62:515–521.
   Web of Science ®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.
   PubMed Web of Science ®Google Scholar
• Huey RB, Hertz PE, Sinervo B. 2003. Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat. 161:357–366.
   PubMed Web of Science ®Google Scholar
• Huey RB, Pianka ER. 1977. Seasonal variation in thermoregulatory behavior and body temperature of diurnal Kalahari lizards. Ecology. 58:1066–1075.
   Web of Science ®Google Scholar
• Ibargüengoytía NR, Medina M, Fernández JB, Gutiérrez JA, Tappari F, Scolaro A. 2010. Thermal biology of the southernmost lizards in the world: Liolaemus sarmientoi and Liolaemus magellanicus from Patagonia. Argentina J Therm Biol. 35:21–27.
   Web of Science ®Google Scholar
• Kubisch EL, Fernández JB, Ibargüengoytía NR. 2016. Vulnerability to climate warming of Liolaemus pictus (Squamata, Liolaemidae), a lizard from the cold temperate climate in Patagonia, Argentina. J Comp Physiol B. 186:243–253.
   PubMed Web of Science ®Google Scholar
• Labra A, Pienaar J, Hansen T. 2009. Evolution of thermal physiology in Liolaemus lizards: adaptation, phylogenetic inertia, and niche tracking. Am Nat. 174:204–220.
   PubMed Web of Science ®Google Scholar
• Labra A, Soto-Gamboa M, Bozinovic F. 2001. Behavioral and physiological thermoregulation of Atacama desert-dwelling Liolaemus lizards. Ecoscience. 8:413–420.
   Web of Science ®Google Scholar
• Labra A, Vidal MA, Solís R, Penna M. 2008. Ecofisiología de anfibios y reptiles. [Ecophysiology of amphibians and reptiles]. In: Vidal-Maldonado MS, Labra A, editors. Herpetología de Chile. Spanish. Santiago de Chile (MS): Science Verlag; p. 483–516.
   Google Scholar
• Lennon JJ. 1999. Resource selection functions: taking space seriously? Trends Ecol Evol. 14:399–400.
   PubMed Web of Science ®Google Scholar
• Lobo F, Espinoza RE, Quinteros S. 2010. A critical review and systematic discussion of recent classification proposals for liolaemid lizards. Zootaxa. 2549:1–30.
   Google Scholar
• Losos JB. 1987. Postures of the military dragon (Ctenophorus isolepis) in relation to substrate temperature. Amphibia-Reptilia. 8:419–423.
   Google Scholar
• Maia-Carneiro T, Dorigo TA, Rocha CFD. 2012. Influences of seasonality, thermal environment and wind intensity on the thermal ecology of Brazilian sand lizards in a Restinga remnant. South Am J Herpetol. 7:241–251.
   Google Scholar
• Maia-Carneiro T, Rocha CFD. 2013. Seasonal variations in behaviour of thermoregulation in juveniles and adults Liolaemus lutzae (Squamata, Liolaemidae) in a remnant of Brazilian restinga. Behav Processes. 100:48–53.
   PubMed Web of Science ®Google Scholar
• Marquet PA, Ortiz JC, Bozinovic F, Jaksik FM. 1989. Ecological aspects of thermoregulation at high altitudes: the case of Andean Liolaemus lizards in northern Chile. Oecologia. 81:16–20.
   PubMed Web of Science ®Google Scholar
• Martín J, López P, Carrascal LM, Salvador A. 1995. Adjustment of basking postures in the high-altitude lberian rock lizard (Lacerta monticola). Can J Zool. 73:1065–1068.
   Web of Science ®Google Scholar
• Martins LS, Verrastro L, Tozetti AM. 2014. The influences of habitat on body temperature control in a southern population of Liolaemus occipitalis (Boulenger 1885) in Brazil. South Am J Herpetol. 9:9–13.
   Web of Science ®Google Scholar
• Martori R, Aun L. 1997. Reproductive and fat body cycle of Liolaemus wiegmannii in Central Argentina. J Herpetol. 31:578–581.
   Web of Science ®Google Scholar
• McConnachie Z, Graham JA, Whiting MJ. 2009. Selected body temperature and thermoregulatory behavior in the sit-and-wait foraging lizard Pseudocordylus melanotus melanotus. Herpetol Monogr. 23:108–122.
   Web of Science ®Google Scholar
• McGinnis SM. 1970. Flexibility of thermoregulatory behavior in the western fence lizard Sceloporus occidentalis. Herpetologica. 26:70–76.
   Google Scholar
• Medina M, Gutiérrez J, Scolaro A, Ibargüengoytía NR. 2009. Thermal responses to environmental constraints in two population of the viviparous lizard Liolaemus bibronii in Patagonia, Argentina. J Therm Biol. 34:32–40.
   Web of Science ®Google Scholar
• Medina M, Scolaro A, Méndez-De La Cruz F, Sinervo B, Ibargüengoitia N. 2011. Thermal relationships between body temperature and environment conditions set upper distributional limits on oviparous species. J Therm Biol. 36:527–534.
   Web of Science ®Google Scholar
• Medina M, Scolaro A, Méndez-De La Cruz F, Sinervo B, Miles DB, Ibarguengoytía N. 2012. Thermal biology of genus Liolaemus: a phylogenetic approach reveals advantages of the genus to survive climate change. J Therm Biol. 37:579–586.
   Web of Science ®Google Scholar
• Moreno Azócar DL, Vanhooydonck B, Bonino MF, Perotti MG, Abdala CS, Schulte JA II, Cruz FB. 2013. Chasing the Patagonian sun: comparative thermal biology of lizards. Oecologia. 171:773–788.
   PubMed Web of Science ®Google Scholar
• Muth A. 1977. Thermoregulatory postures and orientation to the sun: a mechanistic evaluation for the zebra-tailed lizard, Callisaurus draconoides. Copeia. 4:10–720.
   Google Scholar
• NASA. 2000–2016. Prediction of worldwide energy resource (POWER): climatology resource for agroclimatology. Available from: https://power.larc.nasa.gov/cgi-bin/cgiwrap/solar/agro.cgi [Accessed 11 Nov 2015].
   Google Scholar
• Nicholls AO. 1989. How to make biological surveys go further with generalised linear models. Biol Conserv. 50:51–75.
   Web of Science ®Google Scholar
• Niewiarowski PH. 2001. Energy budget, growth rates and thermal constraints: toward an integrative approach to the study of life history variation. Am Nat. 157:421–433.
   PubMed Web of Science ®Google Scholar
• Plummer MV, Ferner JW. 2012. Marking reptiles. In: McDiarmid RW, et al., editors. Reptile biodiversity: standard methods for inventory and monitoring. California: University of California Press; p. 143–150.
   Google Scholar
• Porter WP, Mitchell JW, Beckman WA, DeWitt CB. 1973. Behavioral implications of mechanistic ecology: thermal and behavioral modeling of desert ectotherms and their microenvironment. Oecologia. 13:1–54.
   PubMed Web of Science ®Google Scholar
• Pough FH, Gans C. 1982. The vocabulary of reptilian thermoregulation. In: Gans C, Pough FH, editors. Biology of the Reptilia. London (UK): Academic Press; p. 17–23.
   Google Scholar
• Quinteros AS. 2012. Taxonomy of the Liolaemus alticolor-bibronii group (Iguania: Liolaemidae) with descriptions of two new species. Herpetologica. 68:100–120.
   Web of Science ®Google Scholar
• R Development Core Team. 2015. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: http://www.R-project.org [Accessed 11 Nov 2015].
   Google Scholar
• 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.
   Web of Science ®Google Scholar
• Row JR, Blouin-Demers G. 2006. Thermal quality influences effectiveness of thermoregulation, habitat use and behaviour in milk snakes. Oecologia. 148:1–11.
   PubMed Web of Science ®Google Scholar
• Scheers H, Van Damme R. 2002. Micro-scale differences in thermal habitat quality and a possible case of evolutionary flexibility in the thermal physiology of lacertid lizards. Oecologia. 132:323–331.
   PubMed Web of Science ®Google Scholar
• Stellatelli OA, Block C, Vega LE, Cruz FB. 2014. Responses of two sympatric sand lizards to exotic forestations in the coastal dunes of Argentina: some implications for conservation. Wildl Res. 41:480–489.
   Web of Science ®Google Scholar
• Stellatelli OA, Block C, Vega LE, Cruz FB. 2015. Nonnative vegetation induces changes in predation pressure and escape behavior of two sand lizards (Liolaemidae: Liolaemus). Herpetologica. 71:136–142.
   Web of Science ®Google Scholar
• Stellatelli OA, Block C, Vega LE, Isacch JP, Cruz FB. 2016. Factors affecting the spatial ecology of the lizard Liolaemus wiegmannii in the pampasic coastal dunes of Argentina. Herpetol J. 26:11–19.
   Web of Science ®Google Scholar
• Stellatelli OA, Vega LE, Block C, Cruz FB. 2013. Effects on the thermoregulatory efficiency of two native lizards as a consequence of the habitat modification by the introduction of the exotic tree Acacia longifolia. J Therm Biol. 38:135–142.
   Web of Science ®Google Scholar
• Stevenson RD. 1985. The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am Nat. 126:362–386.
   Web of Science ®Google Scholar
• Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, Huey RB. 2014. Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Natl Acad Sci USA. 111:5610–5615.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Vega LE 1999. Ecología de saurios arenícolas de las dunas costeras bonaerenses. [Ecology of arenicolous saurians from the coastal dunes of Buenos Aires] [ PhD Thesis]. Mar del Plata (BA): Universidad Nacional de Mar del Plata. Spanish.
   Google Scholar
• Vega LE. 2001. Herpetofauna: diversidad, ecología e historia natural. [Herpetofauna: diversity, ecology and natural history]. In: Iribarne O, editor. Reserva de Biosfera Mar Chiquita: características físicas, biológicas y ecológicas. Mar del Plata (BA): Editorial Martín; p. 213–226. Spanish.
   Google Scholar
• Vega LE, Bellagamba PJ, Lobo F. 2008. New endemic species of Liolaemus (Iguania: Liolaemidae) from the mountain range of Tandilia, Buenos Aires province, Argentina. Herpetologica. 64:81–91.
   Web of Science ®Google Scholar
• Vidal MA, Ortíz JC, Labra A. 2008. Intraspecific variation in a physiological thermoregulatory mechanism: the case of the lizard Liolaemus tenuis (Liolaeminae). Rev Chil Hist Nat. 81:171–178.
   Web of Science ®Google Scholar
• Villalba A 2016. Ecología térmica de la lagartija endémica Liolaemus tandiliensis en las sierras del Partido de General Pueyrredón (Buenos Aires, Argentina). [Thermal ecology of the endemic lizard Liolaemus tandiliensis in the sierras of the district of General Pueyrredón (Buenos Aires, Argentina)] [ Bachellor´s Thesis]. Mar del Plata (BA): Universidad Nacional de Mar del Plata. Spanish.
   Google Scholar
• Villavicencio HJ, Acosta JC, Marinero JA, Cánovas MG. 2007. Thermal ecology of a population of the lizard, Liolaemus pseudoanomalus in western Argentina. Amphibia-Reptilia. 28:163–165.
   Web of Science ®Google Scholar
• Vitt LJ, Sartorius SS. 1999. HOBOs, Tidbits and lizard models: the utility of electronic devices in field studies of ectotherm thermoregulation. Funct Ecol. 13:670–674.
   Web of Science ®Google Scholar
• Zar JH. 1984. Biostatistical analysis. New Jersey (NJ): Prentice Hall.
   Google Scholar