Advertisement

Journal of Comparative Physiology B

, Volume 183, Issue 5, pp 663–673 | Cite as

Performance correlates of resting metabolic rate in garden skinks Lampropholis delicata

  • Lucy Merritt
  • Philip G. D. Matthews
  • Craig R. White
Original Paper

Abstract

Resting metabolic rates can vary greatly between individuals of the same species. These differences are generally repeatable and show moderate-to-high heritability, suggesting that they could be a target for natural selection. The present study therefore aimed to determine if inter-individual differences in resting metabolic rates (RMR) in garden skinks Lampropholis delicata were associated with inter-individual differences in a suite of physiological and behavioural variables: aerobic capacity, burst sprinting speed and thermal preference. Whole-animal measures of aerobic capacity and RMR were significantly positively correlated, but mass-independent measures were not. Burst sprinting speed and thermal preference were also not correlated with RMR.

Keywords

Thermal preference Aerobic capacity Sprint speed 

Notes

Acknowledgments

Cameron Schofield, Natalie Schimpf, Daniel Hancox, Benjamin Barth, Candice Bywater and Skye Cameron provided help with animal capture; Roberto Nespolo and an anonymous reviewer provided comments that helped us improve an earlier version of the manuscript. This research was supported by the Australian Research Council (projects DP0879605 and DP0987626).

References

  1. Alibardi L (1995) Muscle differentiation and morphogenesis in the regenerating tail of lizards. J Anat 186:143–151PubMedGoogle Scholar
  2. Alton LA, White CR, Seymour RS (2007) Effect of aerial oxygen content on bimodal gas exchange and air-breathing behaviour in Trichogaster leeri. J Exp Biol 210:2311–2319PubMedCrossRefGoogle Scholar
  3. Andrews RM, Pough FH (1985) Metabolism of squamate reptiles—allometric and ecological relationships. Physiol Zool 58:214–231Google Scholar
  4. Angilletta MJ (2001) Thermal and physiological constraints on energy assimilation in a widespread lizard (Sceloporus undulatus). Ecology 82:3044–3056Google Scholar
  5. Angilletta MJ, Hill T, Robson MA (2002) Is physiological performance optimized by thermoregulatory behavior?: a case study of the eastern fence lizard, Sceloporus undulatus. J Therm Biol 27:199–204CrossRefGoogle Scholar
  6. Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361Google Scholar
  7. Artacho P, Nespolo RF (2009) Natural selection reduces energy metabolism in the garden snail, Helix aspersa (Cornu aspersum). Evolution 63:1044–1050PubMedCrossRefGoogle Scholar
  8. Bartholomew GA, Tucker VA, Lee AK (1965) Oxygen consumption, thermal conductance, and heart rate in the Australian skink, Tiliqua scincoides. Copeia 1965:169–173CrossRefGoogle Scholar
  9. Bauwens D, Garland T, Castilla AM, Vandamme R (1995) Evolution of sprint speed in lacertid lizards—morphological, physiological and behavioural covariation. Evolution 49:848–863CrossRefGoogle Scholar
  10. Beck DD, Dohm MR, Garland T, Ramirez Bautista A, Lowe CH (1995) Locomotor performance and activity energetics of helodermatid lizards. Copeia 1995(3):577–585CrossRefGoogle Scholar
  11. Bell GP, Bartholomew GA, Nagy KA (1986) The roles of energetics, water economy, foraging behavior, and geothermal refugia in the distribution of the bat, Macrotus californicus. J Comp Physiol B Biochem Syst Environ Physiol 156:441–450CrossRefGoogle Scholar
  12. Ben-Ezra E, Bulte G, Blouin-Demers G (2008) Are locomotor performances coadapted to preferred basking temperature in the northern map turtle (Graptemys geographica)? J Herpetol 42:322–331CrossRefGoogle Scholar
  13. Bennett AF (1982) Energetics of activity in reptiles. In: Gans C, Pough FH (eds) Biol Reptil. Academic Press, New York, pp 155–199Google Scholar
  14. Bennett AF (1991) The evolution of activity capacity. J Exp Biol 160:1–23PubMedGoogle Scholar
  15. Bennett AF, Gleeson TT (1979) Metabolic expenditure and the cost of foraging in the lizard Cnemidophorus murinus. Copeia 1979(4):573–577CrossRefGoogle Scholar
  16. Bennett AF, John-Alder HB (1984) The effect of body temperature on the locomotory energetics of lizards. J Comp Physiol B Biochem Syst Environ Physiol 155:21–27CrossRefGoogle Scholar
  17. Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654PubMedCrossRefGoogle Scholar
  18. Bennett AF, Huey RB, John-Alder H (1984) Physiological correlates of natural activity and locomotor capacity in two species of lacertid lizards. J Comp Physiol 154:113–118CrossRefGoogle Scholar
  19. Berteaux D, Thomas DW, Bergeron JM, Lapierre H (1996) Repeatability of daily field metabolic rate in female meadow voles (Microtus pennsylvanicus). Funct Ecol 10:751–759CrossRefGoogle Scholar
  20. Billerbeck JM, Lankford TE, Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates. I. Trade-offs with swimming performance in Menidia menidia. Evolution 55:1863–1872PubMedGoogle Scholar
  21. Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659PubMedCrossRefGoogle Scholar
  22. Bishop CM (1999) The maximum oxygen consumption and aerobic scope of birds and mammals: getting to the heart of the matter. Proc R Soc Lond Series B: Biol Sci 266:2275–2281CrossRefGoogle Scholar
  23. Blackmer AL, Mauck RA, Ackerman JT, Huntington CE, Nevitt GA, Williams JB (2005) Exploring individual quality: basal metabolic rate and reproductive performance in storm-petrels. Behav Ecol 16:906–913CrossRefGoogle Scholar
  24. Boratyński Z, Koteja P (2009) The association between body mass, metabolic rates and survival of bank voles. Funct Ecol 23:330–339CrossRefGoogle Scholar
  25. Bundle MW, Hoppeler H, Vock R, Tester JM, Weyand PG (1999) High metabolic rates in running birds. Nature 397:31–32CrossRefGoogle Scholar
  26. Burgin S (1993) Lampropholis: the new “laboratory” animals. R Zool Soc N S W, NSWGoogle Scholar
  27. Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B Biol Sci 278:3465–3473CrossRefGoogle Scholar
  28. Christian KA, Bedford GS, Schultz TJ (1999) Energetic consequences of metabolic depression in tropical and temperate zone lizards. Aust J Zool 47:133–141CrossRefGoogle Scholar
  29. Clarke A, Pörtner HO (2010) Temperature, metabolic power and the evolution of endothermy. Biol Rev 85:703–727PubMedGoogle Scholar
  30. Clusella-Trullas S, Terblanche JS, van Wyk JH, Spotila JR (2007) Low repeatability of preferred body temperature in four species of Cordylid lizards: temporal variation and implications for adaptive significance. Evol Ecol 21:63–79CrossRefGoogle Scholar
  31. Cortes P, Quijano SA, Nespolo RF (2009) Bioenergetics and inter-individual variation in physiological capacities in a relict mammal—the Monito del Monte (Dromiciops gliroides). J Exp Biol 212:297–304PubMedCrossRefGoogle Scholar
  32. Dohm MR, Garland T, Cole CJ, Townsend CR (1998) Physiological variation and allometry in Western whiptail lizards (Cnemidophorus tigris) from a transect across a persistent hybrid zone. Copeia 1998(1):1–13CrossRefGoogle Scholar
  33. Downes S, Hoefer AM (2007) An experimental study of the effects of weed invasion on lizard phenotypes. Oecologia 153:775–785PubMedCrossRefGoogle Scholar
  34. Farmer CG (2000) Parental care: the key to understanding endothermy and other convergent features in birds and mammals. Am Nat 155:326–334PubMedCrossRefGoogle Scholar
  35. Frappell PB, Butler PJ (2004) Minimal metabolic rate, what it is, its usefulness, and its relationship to the evolution of endothermy: a brief synopsis. Physiol Biochem Zool 77:865–868PubMedCrossRefGoogle Scholar
  36. Garland T (1988) Genetic basis of activity metabolism-1. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42:335–350CrossRefGoogle Scholar
  37. Gomes FR, Chauí-Berlinck JG, Bicudo JEPW, Navas CA (2004) Intraspecific relationships between resting and activity metabolism in anuran amphibians: influence of ecology and behavior. Physiol Biochem Zool 77:197–208PubMedCrossRefGoogle Scholar
  38. Grigg GC, Beard LA, Augee ML (2004) The evolution of endothermy and its diversity in mammals and birds. Physiol Biochem Zool 77:982–997PubMedCrossRefGoogle Scholar
  39. Hayes JP (2010) Metabolic rates, genetic constraints, and the evolution of endothermy. J Evol Biol 23:1868–1877PubMedCrossRefGoogle Scholar
  40. Hayes JP, Garland T (1995) The evolution of endothermy—testing the aerobic capacity model. Evolution 49:836–847CrossRefGoogle Scholar
  41. Hinds DS, Baudinette RV, MacMillen RE, Halpern EA (1993) Maximum metabolism and the aerobic factorial scope of endotherms. J Exp Biol 182:41–56PubMedGoogle Scholar
  42. Hochachka PW, Burelle Y (2004) Control of maximum metabolic rate in humans: dependence on performance phenotypes. Mol Cell Biochem 256–257:95–103PubMedCrossRefGoogle Scholar
  43. Hochscheid S, McMahon CR, Bradshaw CJA, Maffucci F, Bentivegna F, Hays GC (2007) Allometric scaling of lung volume and its consequences for marine turtle diving performance. Comp Biochem Physiol A Mol Integr Physiol 148:360–367PubMedCrossRefGoogle Scholar
  44. Howard R, Williamson I, Mather P (2003) Structural aspects of microhabitat selection by the skink Lampropholis delicata. J Herpetol 37:613–617CrossRefGoogle Scholar
  45. Huey RB, Bennett AF, John-Alder H, Nagy KA (1984) Locomotor capacity and foraging behaviour of Kalahari lacertid lizards. Anim Behav 32:41–50CrossRefGoogle Scholar
  46. Hulbert AJ, Else PL (2000) Mechanisms underlying the cost of living in animals. Ann Rev Physiol 62:207–235CrossRefGoogle Scholar
  47. Huyghe K, Vanhooydonck B, Scheers H, Molina-Borja M, Van Damme R (2005) Morphology, performance and fighting capacity in male lizards, Gallotia galloti. Funct Ecol 19:800–807CrossRefGoogle Scholar
  48. Jackson DM, Trayhurn P, Speakman JR (2001) Associations between energetics and over-winter survival in the short-tailed field vole Microtus agrestis. J Anim Ecol 70:633–640CrossRefGoogle Scholar
  49. Jayne BC, Bennett AF (1990) Selection on locomotor performance capacity in a natural population of garter snakes. Evolution 44:1204–1229CrossRefGoogle Scholar
  50. Ji X, Sun PY, Du WG (1997) Selected body temperature, thermal tolerance and food assimilation in a viviparous skink, Sphenomorphus indicus. Neth J Zool 47:103–110Google Scholar
  51. John-Alder HB, Garland T, Bennett AF (1986) Locomotory capacities, oxygen consumption and the cost of locomotion of the shingle-back lizard (Trachydosaurus rugosus). Physiol Zool 59:523–531Google Scholar
  52. Joss JMP, Minard JA (1985) On the reproductive cycles of Lampropholis guichenoti and Lampropholis delicata (Squamata, Scincidae) in the Sydney region. Aust J Zool 33:699–704CrossRefGoogle Scholar
  53. Konarzewski M, Książek A (2013) Determinants of intra-specific variation in basal metabolic rate. J Comp Physiol B 183:27–41PubMedCrossRefGoogle Scholar
  54. Koteja P (1987) On the relation between basal and maximum metabolic rate in mammals. Comp Biochem Physiol A 87:205–208PubMedCrossRefGoogle Scholar
  55. Koteja P (1996) Measuring energy metabolism with open flow respirometric systems: which design to choose? Funct Ecol 10:675–677CrossRefGoogle Scholar
  56. Koteja P (2000) Energy assimilation, parental care and the evolution of endothermy. Proc R Soc Lond B Biol Sci 267:479–484CrossRefGoogle Scholar
  57. Labocha MK, Sadowska ET, Baliga K, Semer AK, Koteja P (2004) Individual variation and repeatability of basal metabolism in the bank vole, Clethrionomys glareolus. Proc R Soc Lond B Biol Sci 271:367–372CrossRefGoogle Scholar
  58. Le Galliard JF, Ferriere R (2008) Evolution of maximal endurance capacity: natural and sexual selection across age classes in a lizard. Evol Ecol Res 10:157–176Google Scholar
  59. Lichtenbelt W, Vogel JT, Wesselingh RA (1997) Energetic consequences of field body temperatures in the green iguana. Ecology 78:297–307CrossRefGoogle Scholar
  60. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, OxfordCrossRefGoogle Scholar
  61. Lighton JRB, Fielden LJ (1995) Mass scaling of standard metabolism in ticks: a valid case of low metabolic rates in sit-and-wait strategists. Physiol Zool 68:43–62Google Scholar
  62. Lighton JRB, Brownell PH, Joos B, Turner RJ (2001) Low metabolic rate in scorpions: implications for population biomass and cannibalism. J Exp Biol 204:607–613PubMedGoogle Scholar
  63. Litzgus JD, Brooks RJ (2000) Habitat and temperature selection of Clemmys guttata in a Northern population. J Herpetol 34:178–185CrossRefGoogle Scholar
  64. Lovegrove BG (2011) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biological Rev. Doi: 10.1111/j.1469-1185X.2011.00188.x
  65. Marras S, Claireaux G, McKenzie DJ, Nelson JA (2010) Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax. J Exp Biol 213:26–32PubMedCrossRefGoogle Scholar
  66. Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life history strategies in Atlantic salmon. Anim Behav 49:431–436CrossRefGoogle Scholar
  67. Moon BR, Tullis A (2006) The ontogeny of contractile performance and metabolic capacity in a high-frequency muscle. Physiol Biochem Zool 79:20–30PubMedCrossRefGoogle Scholar
  68. Nagy KA (2005) Field metabolic rate and body size. J Exp Biol 208:1621–1625PubMedCrossRefGoogle Scholar
  69. Nespolo RF, Franco M (2007) Whole-animal metabolic rate is a repeatable trait: a meta-analysis. J Exp Biol 210:3877–3878CrossRefGoogle Scholar
  70. Nespolo RF, Bustamante DM, Bacigalupe LD, Bozinovic F (2005) Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini. Evolution 59:1829–1837PubMedGoogle Scholar
  71. Nespolo RF, Bacigalupe LD, Figueroa CC, Koteja P, Opazo JC (2011) Using new tools to solve an old problem: the evolution of endothermy in vertebrates. Trends Ecol Evol 26:414–423PubMedCrossRefGoogle Scholar
  72. Nilsson JA, Akesson M, Nilsson JF (2009) Heritability of resting metabolic rate in a wild population of blue tits. J Evol Biol 22:1867–1874PubMedCrossRefGoogle Scholar
  73. Noren DP (2002) Thermoregulation of weaned Northern elephant seal (Mirounga angustirostris) pups in air and water. Physiol Biochem Zool 75:513–523PubMedCrossRefGoogle Scholar
  74. Novinger DC, Coon TG (2000) Behavior and physiology of the redside dace, Clinostomus elongatus, a threatened species in Michigan. Environ Biol Fishes 57:315–326CrossRefGoogle Scholar
  75. Owerkowicz T, Baudinette RV (2008) Exercise training enhances aerobic capacity in juvenile estuarine crocodiles (Crocodylus porosus). Comp Biochem Physiol A Mol Integr Physiol 150:211–216PubMedCrossRefGoogle Scholar
  76. Porter SD, Tschinkel WR (1993) Fire ant thermal preferences—behavioural control of growth and metabolism. Behav Ecol Sociobiol 32:321–329CrossRefGoogle Scholar
  77. Reidy SP, Kerr SR, Nelson JA (2000) Aerobic and anaerobic swimming performance of individual Atlantic cod. J Exp Biol 203:347–357PubMedGoogle Scholar
  78. Rixon RH, Stevenson JAF (1957) Factors influencing survival of rats in fasting metabolic rate and body weight loss. Am J Physiol 188:332–336PubMedGoogle Scholar
  79. Roe JH, Hopkins WA, Talent LG (2005) Effects of body mass, feeding and circadian cycles on metabolism in the lizard Sceloporus occidentalis. J Herpetol 39:595–603CrossRefGoogle Scholar
  80. Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758PubMedGoogle Scholar
  81. Ronning B, Jensen H, Moe B, Bech C (2007) Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch. J Evol Biol 20:1815–1822PubMedCrossRefGoogle Scholar
  82. Ruben JA, Battalia DE (1979) Aerobic and anaerobic metabolism during activity in small rodents. J Exp Zool 208:73–76PubMedCrossRefGoogle Scholar
  83. Sadowska ET, Labocha MK, Baliga K, Stanisz A, Wróblewska AK, Jagusiak W, Koteja P (2005) Genetic correlations between basal and maximum metabolic rates in a wild rodent: consequences for evolution of endothermy. Evolution 59:672–681PubMedGoogle Scholar
  84. Sadowska ET, Baliga-Klimczyk K, Labocha MK, Koteja P (2009) Genetic correlations in a wild rodent: grass-eaters and fast-growers evolve high basal metabolic rates. Evolution 63:1530–1539PubMedCrossRefGoogle Scholar
  85. Schimpf NG, Matthews PGD, White CR (2012a) Cockroaches that exchange respiratory gases discontinuously survive food and water restriction. Evolution 66:597–604PubMedCrossRefGoogle Scholar
  86. Schimpf NG, Matthews PGD, White CR (2012b) Standard metabolic rate is associated with gestation duration, but not clutch size, in speckled cockroaches Nauphoeta cinerea. Biol Open. doi: 10.1242/bio.20122683 PubMedGoogle Scholar
  87. Schimpf NG, Matthews PGD, White CR (2013) Discontinuous gas exchange exhibition is a heritable trait in speckled cockroaches Nauphoeta cinerea J Evol Biol: in pressGoogle Scholar
  88. Sears MW (2005) Resting metabolic expenditure as a potential source of variation in growth rates of the sagebrush lizard. Comp Biochem Physiol A Mol Integr Physiol 140:171–177PubMedCrossRefGoogle Scholar
  89. Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56PubMedCrossRefGoogle Scholar
  90. Seebacher F (2005) A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility? J Comp Physiol B Biochem Syst Environ Physiol 175:453–461CrossRefGoogle Scholar
  91. Sieg AE, O’Connor MP, McNair JN, Grant BW, Agosta SJ, Dunham AE (2009) Mammalian metabolic allometry: do intraspecific variation, phylogeny and regression models matter? Am Nat 174:720–733PubMedCrossRefGoogle Scholar
  92. Sogard SM, Olla BL (1996) Food deprivation affects vertical distribution and activity of a marine fish in a thermal gradient: potential energy-conserving mechanisms. Mar Ecol Prog Ser 133:43–55CrossRefGoogle Scholar
  93. Speakman JR (2000) The cost of living: field metabolic rates of small mammals. Adv Ecol Res 30:176–297Google Scholar
  94. Swallow JG, Hayes JP, Koteja P, Garland T Jr (2009) Selection experiments and experimental evolution of performance and physiology. In: Garland T Jr, Rose MR (eds) Experimental evolution: concepts, methods, and applications of selection experiments. University of California Press, Berkeley, pp 301–351Google Scholar
  95. Tattersall GJ, Boutilier RG (1997) Balancing hypoxia and hypothermia in cold-submerged frogs. J Exp Biol 200:1031–1038PubMedGoogle Scholar
  96. Tattersall GJ, Boutilier RG (1999) Does behavioural hypothermia promote post-exercise recovery in cold-submerged frogs? J Exp Biol 202:609–622PubMedGoogle Scholar
  97. Taylor CR, Maloiy GMO, Weibel ER, Langman VA, Kamau JMZ, Seeherman HJ, Heglund NC (1981) Design of the mammalian respiratory system. 3. Scaling maximum aerobic capacity to body mass—wild and domestic mammals. Resp Physiol 44:25–37CrossRefGoogle Scholar
  98. Terblanche JS, Klok CJ, Chown SL (2004) Metabolic rate variation in Glossina pallidipes (Diptera : Glossinidae): gender, ageing and repeatability. J Insect Physiol 50:419–428PubMedCrossRefGoogle Scholar
  99. Thompson MB, Speake BK, Russell KJ, McCartney RJ (2001) Utilisation of lipids, protein, ions and energy during embryonic development of Australian oviparous skinks in the genus Lampropholis. Comp Biochem Physiol A-Mol Integr Physiol 129:313–326PubMedCrossRefGoogle Scholar
  100. 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 80:516–524CrossRefGoogle Scholar
  101. Vanhooydonck B, Van Damme R, Aerts P (2000) Ecomorphological correlates of habitat partitioning in Corsican lacertid lizards. Funct Ecol 14:358–368CrossRefGoogle Scholar
  102. Vanhooydonck B, Van Damme R, Aerts P (2001) Speed and stamina trade-off in lacertid lizards. Evolution 55:1040–1048PubMedCrossRefGoogle Scholar
  103. Walton M (1988) Relationships amongst metabolic, locomotory and field measures of organismal performance in the Fowlers toad (Bufo woodhousei fowleri). Physiol Zool 61:107–118Google Scholar
  104. Weibel ER, Bacigalupe LD, Schmidt B, Hoppeler H (2004) Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as a determinant factor. Respir Physiol Neurobiol 140:115–132PubMedCrossRefGoogle Scholar
  105. Weinstein RB, Full RJ (1999) Intermittent locomotion increases endurance in a gecko. Physiol Biochem Zool 72:732–739PubMedCrossRefGoogle Scholar
  106. Wheeler PE (1986) Thermal acclimation of metabolism and preferred body temperature in lizards. J Therm Biol 11:161–166CrossRefGoogle Scholar
  107. White CR, Kearney MR (2013) Determinants of inter-specific variation in basal metabolic rate. J Comp Physiol B 183:1–26PubMedCrossRefGoogle Scholar
  108. White CR, Seymour RS (2005) Allometric scaling of mammalian metabolism. J Exp Biol 208:1611–1619PubMedCrossRefGoogle Scholar
  109. White CR, Matthews PGD, Seymour RS (2006a) Balancing the competing requirements of saltatorial and fossorial specialisation: burrowing costs in the spinifex hopping mouse, Notomys alexis. J Exp Biol 209:2103–2113PubMedCrossRefGoogle Scholar
  110. White CR, Phillips NF, Seymour RS (2006b) The scaling and temperature dependence of vertebrate metabolism. Biol Lett 2:125–127PubMedCrossRefGoogle Scholar
  111. White CR, Cassey P, Blackburn TM (2007) Allometric exponents do not support a universal metabolic allometry. Ecology 88:315–323PubMedCrossRefGoogle Scholar
  112. White CR, Terblanche JS, Kabat AP, Blackburn TM, Chown SL, Butler PJ (2008) Allometric scaling of maximum metabolic rate: the influence of temperature. Funct Ecol 22:616–623CrossRefGoogle Scholar
  113. Withers PC (2001) Design, calibration and calculation for flow-through respirometry systems. Aust J Zool 49:445–461CrossRefGoogle Scholar
  114. Wolf BO, Walsberg GE (1996) Thermal effects of radiation and wind on a small bird and implications for microsite selection. Ecology 77:2228–2236CrossRefGoogle Scholar
  115. Wone B, Sears MW, Labocha MK, Donovan ER, Hayes JP (2009) Genetic variances and covariances of aerobic metabolic rates in laboratory mice. Proc R Soc B 276:3695–3704PubMedCrossRefGoogle Scholar
  116. Zhan X, Li Y, Wang D (2009) Effects of fasting and refeeding on body mass, thermogenesis and serum leptin in Brandt’s voles (Lasiopodomys brandtii). J Therm Biol 34:237–243CrossRefGoogle Scholar
  117. Zhang YP, Ji XA (2004) The thermal dependence of food assimilation and locomotor performance in southern grass lizards, Takydromus sexlineatus (Lacertidae). J Therm Biol 29:45–53CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Lucy Merritt
    • 1
  • Philip G. D. Matthews
    • 1
  • Craig R. White
    • 1
  1. 1.School of Biological SciencesThe University of QueenslandSt LuciaAustralia

Personalised recommendations