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Daily and annual cycles in thermoregulatory behaviour and cardio-respiratory physiology of black and white tegu lizards

Journal of Comparative Physiology B volume 185, pages 905–915 (2015)Cite this article

Abstract

This study was designed to determine the manner in which metabolism is suppressed during dormancy in black and white tegu lizards (Tupinambis merianae). To this end, heart rate (f H), respiration rate (f R), and deep body temperature (T b) were continuously monitored in outdoor enclosures by radio-telemetry for nine months. There was a continuous decline in nighttime breathing and heart rate, at constant T b, throughout the late summer and fall suggestive of an active metabolic suppression that developed progressively at night preceding the entrance into dormancy. During the day, however, the tegus still emerged to bask. In May, when the tegus made a behavioural commitment to dormancy, T b (day and night) fell to match burrow temperature, accompanied by a further reduction in f H and f R. Tegus, under the conditions of this study, did arouse periodically during dormancy. There was a complex interplay between changes in f H and T b associated with the direct effects of temperature and the indirect effects of thermoregulation, activity, and changes in metabolism. This interplay gave rise to a daily hysteresis in the f H/T b relationship reflective of the physiological changes associated with warming and cooling as preferred T b alternated between daytime and nighttime levels. The shape of the hysteresis curve varied with season along with changes in metabolic state and daytime and nighttime body temperature preferences.

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References

  • Abe AS (1983) Observations on dormancy in tegu lizards—Tupinambis teguixim (Reptilia, Teiidae). Naturalia 8:235–239

    Google Scholar 

  • Abe AS (1993) Effect of the environment on ventilation in reptiles. In: Bicudo JEPW (ed) The vertebrate gas transport cascade: adaptations to environment and mode of life. CRC Press Inc., Boca Raton, pp 87–93

    Google Scholar 

  • Abe AS (1995) Estivation in South American amphibians and reptiles. Braz J Med Biol Res 28:1241–1247

    CAS  PubMed  Google Scholar 

  • Andrade DV, Abe AS (1999) Gas exchange and ventilation during dormancy in the tegu lizard Tupinambis merianae. J Exp Biol 202:3677–3685

    PubMed  Google Scholar 

  • Andrade DV, Brito SP, Toledo LF, Abe AS (2004) Seasonal changes in blood oxygen transport and acid-base status in the tegu lizard, Tupinambis merianae. Respir Physiol Neurobiol 140:197–208

    Article  CAS  PubMed  Google Scholar 

  • Ávila-Pires TCS (1995) Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen 1995:3–706

    Google Scholar 

  • Barnes BM, Omtzigt C, Daan S (1993) Hibernators periodically arouse in order to sleep. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 555–558

    Google Scholar 

  • Bartholomew GA, Tucker VA (1963) Control of changes in body temperature, metabolism, and circulation by the agamid lizard, Amphibolurus barbatus. Physiol Zool 36:199–218

    Google Scholar 

  • Beuchat CA (1986) Reproductive influences on the thermoregulatory behavior of a live-bearing lizard. Copeia 1986:971–979

    Article  Google Scholar 

  • Butler PJ, Woakes AJ, Bevan RM, Stephenson R (2000) Heart rate and rate of oxygen consumption during flight of the barnacle goose, Branta leucopsis. Comp Biochem Physiol A 126:379–385

    Article  CAS  Google Scholar 

  • Butler PJ, Frappell PB, Wang T, Wikelski M (2002) The relationship between heart rate and rate of oxygen consumption in Galapagos marine iguanas (Amblyrhynchus cristatus) at two different temperatures. J Exp Biol 205:1917–1924

    PubMed  Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    Article  CAS  PubMed  Google Scholar 

  • Clark TD, Butler PJ, Frappell PB (2004) Digestive state influences the heart rate hysteresis and rates of heat exchange in the varanid lizard Varanus rosenbergi. J Exp Biol 208:2269–2276

    Article  Google Scholar 

  • Clark TD, Butler PJ, Frappell PB (2006) Factors influencing the prediction of metabolic rate in a reptile. Funct Ecol 20:105–113

    Article  Google Scholar 

  • Crossley DA, Wearing OH, Platzack B, Hartzler LK, Hicks JW (2015) Acute and chronic temperature effects on cardiovascular regulation in the red-eared slider (Trachemys scripta). J Comp Physiol B 185:401–411

    Article  CAS  PubMed  Google Scholar 

  • de Souza SCR, de Carvalho JE, Abe AS, Bicudo JEPW, Bianconcini MSC (2004) Seasonal metabolic depression, substrate utilisation and changes in scaling patterns during the first year cycle of tegu lizards (Tupinambis merianae). J Exp Biol 207:307–318

    Article  PubMed  Google Scholar 

  • Donohoe PH, West TG, Boutilier RG (1998) Respiratory, metabolic, and acid-base correlates of aerobic metabolic rate reduction in overwintering frogs. Am J Physiol 274:R704–R710

    CAS  PubMed  Google Scholar 

  • Ellis DJ, Firth BT, Belan I (2008) Interseasonal variation in the circadian rhythms of locomotor activity and temperature selection in sleepy lizards, Tiliqua rugosa. J Comp Physiol [A] 194:701–712

    Article  Google Scholar 

  • Firth BT, Belan I (1998) Daily and seasonal rhythms in selected body temperatures in the Australian lizard Tiliqua rugosa (Scincidae): field and laboratory observations. Physiol Zool 71:303–311

    Article  CAS  PubMed  Google Scholar 

  • Galli G, Taylor EW, Wang T (2004) The cardiovascular responses of the freshwater turtle Trachemys scripta to warming and cooling. J Exp Biol 207:1471–1478

    Article  PubMed  Google Scholar 

  • Garrick LD (1974) Reproductive influences on behavioral thermoregulation in the lizard, Sceloporus cyanogenys. Physiol Behaviour 12:85–91

    Article  CAS  Google Scholar 

  • Glanville EJ, Seebacher F (2006) Compensation for environmental change by complementary shifts of thermal sensitivity and thermoregulatory behaviour in an ectotherm. J Exp Biol 209:4869–4877

    Article  CAS  PubMed  Google Scholar 

  • Green JA, Frappell PB, Clark TD, Butler PJ (2008) Predicting rate of oxygen consumption from heart rate while little penguins work rest and play. Comp Biochem Physiol 150A:222–230

    Article  CAS  Google Scholar 

  • Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74:1–40

    Article  CAS  PubMed  Google Scholar 

  • Heldmaier G, Ruf T (1992) Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol B 162(8):696–706

    Article  CAS  PubMed  Google Scholar 

  • Heller HC, Colliver GW, Beard J (1977) Thermoregulation during entrance into hibernation. Pflug Arch Eur J Phy 369:55–59

    Article  CAS  Google Scholar 

  • Hicks JW, Wang T (2004) Hypometabolism in reptiles: behavioural and physiological mechanisms that reduce aerobic demands. Resp Physiol Neurobiol 141:261–271

    Article  CAS  Google Scholar 

  • Huey RB, Bennett AF (1987) Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance temperatures of lizards. Evolution 41:1098–1115

    Article  Google Scholar 

  • Huey RB, Pianka ER (1977) Seasonal variation in thermoregulatory behavior and body temperature of diurnal Kalahari lizards. Ecology 58:1066–1075

    Article  Google Scholar 

  • Köhler G, Langerwerf B (2000) Tejus: Lebensweise, Plege, Zucht. Herpeton, Offenbach

  • Langille BL, Crisp B (1980) Temperature dependence of blood viscosity in frogs and turtles: effect on heat exchange with environment. Am J Physiol 239:R248–R253

    CAS  PubMed  Google Scholar 

  • Luiselli L, Akani GC (2002) Is thermoregulation really unimportant for tropical reptiles? Comparative study of four sympatric snake species from Africa. Acta Oecol 23:59–68

    Article  Google Scholar 

  • Lyman CP (1982) Entering Hibernation. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 37–53

    Chapter  Google Scholar 

  • Mayhew WW (1965) Hibernation in the Horned Lizard, Phrynosoma m’calli. Comp Biochem Physiol 16:103–119

    Article  CAS  PubMed  Google Scholar 

  • Milsom WK, Andrade DV, Brito SP, Toledo LF, Wang T, Abe AS (2008) Seasonal changes in daily metabolic patterns of tegu lizards (Tupinambis merianae) placed in the cold (17°C) and dark. Physiol Biochem Zool 81:165–175

    Article  CAS  PubMed  Google Scholar 

  • Milstead WW (1961) Notes on the Teiid lizards in southern Brazil. Copeia 1961:493–495

    Article  Google Scholar 

  • Morgareidge K, White FN (1969) Cutaneous vascular changes during heating and cooling in the Galápagos marine iguana. Nature 223:587–591

    Article  CAS  PubMed  Google Scholar 

  • Nedergaard J, Cannon B, Jaenicke R (1990) Mammalian hibernation. Phil Trans R Soc Lond B 326:669–686

    Article  CAS  Google Scholar 

  • Patterson JW, Davies PMC (1978) Energy expenditure and metabolic adaptation during winter dormancy in the lizard Lacerta vivipara Jacquin. J Therm Biol 3:183–186

    Article  Google Scholar 

  • Piercy J, Rogers K, Andrade D, Abe AS, Tattersall G, Milsom WK (2015). The relationship between body temperature, heart rate, breathing rate, and the rate of oxygen consumption in the tegu lizard (Tupinambis merianae) at various levels of activity. J Comp Physiol B (Submitted)

  • Revel FG, Herwig A, Garidou ML, Dardente H, Menet JS, Masson-Pevet M, Simonneux V, Saboureau M, Pevet P (2007) The circadian clock stops ticking during deep hibernation in the European hamster. Proc Natl Acad Sci 104:13816–13820

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rismiller PD, Heldmaier G (1982) The effect of photoperiod on temperature selection in the European green lizard, Lactera viridis. Occologia 53:222–226

    Article  Google Scholar 

  • Rismiller PD, Heldmaier G (1991) Seasonal changes in daily metabolic patterns of Lacerta viridis. J Comp Physiol B 161:482–488

    Article  Google Scholar 

  • Rismiller PD, McKelvey MW (2000) Spontaneous arousal in reptiles? Body temperature ecology of Rosenberg’s Goanna, Varanus rosenbergi. In: Heldmaier G, Klingenspor M (eds) Life in the Cold. Springer-Verlag, New York, pp 57–64

    Chapter  Google Scholar 

  • Rollinson N, Tattersall GJ, Brooks RJ (2008) Overwintering habitats of a northern population of Painted Turtles (Chrysemys picta): winter temperature selection and dissolved oxygen concentrations. J Herpetol 42:312–321

    Article  Google Scholar 

  • Seebacher F (2000) Heat transfer in a microvascular network: the effect of heart rate on heating and cooling in reptiles (Pogona barbata and Varanus varius). J Theor Biol 203:97–109

    Article  CAS  PubMed  Google Scholar 

  • Seebacher F, Franklin CE (2001) Control of heart rate during thermoregulation in the heliothermic lizard Pogona barbata: importance of cholinergic and adrenergic mechanisms. J Exp Biol 204:4361–4366

    CAS  PubMed  Google Scholar 

  • Seebacher F, Franklin CE (2005) Physiological mechanisms of thermoregulation in reptiles: a review. J Comp Physiol B 175:533–541

    Article  PubMed  Google Scholar 

  • Stewart GR (1965) Thermal ecology of the garter snake Thamnophis sirtalis concinnus (Hallowell) and Thamnophis orfinoides (Baird and Girard). Herpetologica 21:81–102

    Google Scholar 

  • Stewart JR (1984) Thermal biology of the live bearing lizard Gerrhonotus coeruleus. Herpetologica 40:349–355

    Google Scholar 

  • Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65:145–174

    Article  CAS  PubMed  Google Scholar 

  • Tattersall GJ, Boutilier RG (1997) Balancing hypoxia and hypothermia in cold-submerged frogs. J Exp Biol 200:1031–1038

    CAS  PubMed  Google Scholar 

  • Tattersall GJ, Boutilier RG (1999) Behavioural oxy-regulation by cold-submerged frogs in heterogeneous oxygen environments. Can J Zool 77:843–850

    Article  Google Scholar 

  • Tøien Ø, Blake J, Barnes BM (2015) Thermoregulation and energetics in hibernating black bears: metabolic rate and the mystery of multi-day body temperature cycles. J Comp Physiol B 185:447–461

    Article  PubMed  Google Scholar 

  • Toledo LF, Brito SP, Milsom WK, Abe AS, Andrade DV (2008) Effects of season, temperature and body mass on the standard metabolic rate of tegu lizards (Tupinambis merianae). Physiol Biochem Zool 81:158–164

    Article  PubMed  Google Scholar 

  • Twente JW, Twente JA (1967) Seasonal variation in the hibernating behaviour of Citellus lateralis. In: Fisher KC, Dawe AR, Lyman CP, Schöbaum E, South FE Jr (eds) Mammalian Hibernation III. Elsevier Inc., New York, pp 47–63

    Google Scholar 

  • Van Breukelen F, Martin SL (2002) Reversible depression of transcription during hibernation. J Comp Physiol B 172:355–361

    Article  PubMed  Google Scholar 

  • Wang LCH (1993) Neurochemical regulation of arousal from hibernation. In: Carey C, Florant GL, Wunder BA Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 559–561

  • Werner YL, Whitaker AH (1978) Observations and comments on the body temperatures of some New Zealand reptiles. N Z J Zool 5:375–393

    Article  Google Scholar 

  • Willis JS (1982) The mystery of the periodic arousal. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 92–103

    Google Scholar 

  • Winck GR, Cechin SZ (2008) Hibernation and emergence pattern of Tupinambis merianae (Squamata: Teiidae) in the Taim Ecological Station, southern Brazil. J Nat Hist 42:239–247

    Article  Google Scholar 

  • Zaar M, Larsen E, Wang T (2004) Hysteresis of heart rate and heat exchange of fasting and postprandial savannah monitor lizards (Varanus exanthematicus). Comp Biochem Phys A 137:675–682

    Article  Google Scholar 

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Acknowledgements

This research was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) to ASA, from the Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) and Fundação para o Desenvolvimento da Unesp (FUNDUNESP) to DVA, and the Natural Sciences and Engineering Research Council of Canada to WKM and GJT.

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Authors and Affiliations

  1. Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada

    Colin E. Sanders, Michelle Reichert & William K. Milsom

  2. Department of Biological Sciences, Brock University, St. Catharines, ON, Canada

    Glenn J. Tattersall

  3. Depto de Zoologia, Instituto Nacional de Ciência e Tecnologia em Fisiologia Comparada, Univ Estadual Paulista, Rio Claro, SP, 13506-900, Brazil

    Denis V. Andrade & Augusto S. Abe

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  1. Colin E. Sanders
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  2. Glenn J. Tattersall
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  4. Denis V. Andrade
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  5. Augusto S. Abe
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  6. William K. Milsom
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Correspondence to William K. Milsom.

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Communicated by G. Heldmaier.

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Sanders, C.E., Tattersall, G.J., Reichert, M. et al. Daily and annual cycles in thermoregulatory behaviour and cardio-respiratory physiology of black and white tegu lizards. J Comp Physiol B 185, 905–915 (2015). https://doi.org/10.1007/s00360-015-0928-2

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