Restricted access
Phenotypic plasticity in the scaling of avian basal metabolic rate
Published:17 January 2006https://doi.org/10.1098/rspb.2005.3415
Abstract
Many birds exhibit short-term, reversible adjustments in basal metabolic rate (BMR), but the overall contribution of phenotypic plasticity to avian metabolic diversity remains unclear. The available BMR data include estimates from birds living in natural environments and captive-raised birds in more homogenous, artificial environments. All previous analyses of interspecific variation in BMR have pooled these data. We hypothesized that phenotypic plasticity is an important contributor to interspecific variation in avian BMR, and that captive-raised populations exhibit general differences in BMR compared to wild-caught populations. We tested this hypothesis by fitting general linear models to BMR data for 231 bird species, using the generalized least-squares approach to correct for phylogenetic relatedness when necessary. The scaling exponent relating BMR to body mass in captive-raised birds (0.670) was significantly shallower than in wild-caught birds (0.744). The differences in metabolic scaling between captive-raised and wild-caught birds persisted when migratory tendency and habitat aridity were controlled for. Our results reveal that phenotypic plasticity is a major contributor to avian interspecific metabolic variation. The finding that metabolic scaling in birds is partly determined by environmental factors provides further support for models that predict variation in scaling exponents, such as the allometric cascade model.
References
-
Ambrose S.J& Bradshaw S.D . 1988 Seasonal changes in standard metabolic rates in the white-browed scrubwren Sericornis frontalis (Acanthizidae) from arid, semi-arid and mesic environments. Comp. Biochem. Physiol. A. 89, 79–83.doi:10.1016/0300-9629(88)91142-5. . Crossref, Web of Science, Google Scholar -
Anderson K.J& Jetz W . 2005 The broad-scale ecology of energy expenditure of endotherms. Ecol. Lett. 8, 310–318.doi:10.1111/j.1461-0248.2005.00723.x. . Crossref, Web of Science, Google Scholar -
Banavar J.R, Damuth J, Maritan A& Rinaldo A . 2002 Supply–demand balance and metabolic scaling. Proc. Natl Acad. Sci. USA. 99, 1056–1059.doi:10.1073/pnas.162216899. . Crossref, Web of Science, Google Scholar -
Bartholomew G.A& Trost C.H . 1970 Temperature regulation in the speckled mousebird, Colius striatus. Condor. 72, 141–146. Crossref, Web of Science, Google Scholar -
Battley P.F, Dekinga A, Dietz M.W, Piersma T, Tang S& Hulsman K . 2001 Basal metabolic rate declines during long-distance migratory flight in great knots. Condor. 103, 838–845. Crossref, Web of Science, Google Scholar -
Broggi J, Hohtola E, Orell M& Nilsson J.-Å . 2005 Local adaptation to winter conditions in a passerine spreading north: a common-garden approach. Evolution. 59, 1600–1603. Crossref, PubMed, Web of Science, Google Scholar -
Daan S, Masman D& Groenewold A . 1990 Avian basal metabolic rates: their association with body compostition and energy expenditure in nature. Am. J. Physiol. R333, R340. Google Scholar -
Darveau C.-A, Suarez R.K, Andrews R.D& Hochachka P.W . 2002 Allometric cascade as a unifying principle of body mass effects on metabolism. Nature. 417, 166–170.doi:10.1038/417166a. . Crossref, PubMed, Web of Science, Google Scholar -
Dawson W.R& O'Conner T.P Energetic features of avian thermoregulatory responses. Avian energetics and nutritional ecology& Carey C . 1996pp. 85–124. Eds. New York:Chapman & Hall. Crossref, Google Scholar -
Dekinga A, Dietz M.W, Koolhaas A& Piersma T . 2001 Time course and reversability of changes in the gizzards of red knots alternately eating hard and soft food. J. Exp. Biol. 204, 2167–2173. Crossref, PubMed, Web of Science, Google Scholar -
Felsenstein J . 1985 Phylogenies and the comparative method. Am. Nat. 125, 1–15.doi:10.1086/284325. . Crossref, Web of Science, Google Scholar -
Freckleton R.P, Harvey P.H& Pagel M . 2002 Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726.doi:10.1086/343873. . Crossref, PubMed, Web of Science, Google Scholar -
Garland T& Ives A.R . 2000 Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155, 346–364.doi:10.1086/303327. . Crossref, PubMed, Web of Science, Google Scholar -
Garland T, Harvey P.H& Ives A.R . 1992 Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18–32. Crossref, Web of Science, Google Scholar -
Garland T, Dickerman A.W, Janis C.M& Jones J.A . 1993 Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42, 265–292. Crossref, Web of Science, Google Scholar -
Hochachka P.W, Darveau C.-A, Andrews R.D& Suarez R.K . 2003 Allometric cascade: a model for resolving body mass effects on metabolism. Comp. Biochem. Physiol. A. 134, 675–691.doi:10.1016/S1095-6433(02)00364-1. . Crossref, PubMed, Web of Science, Google Scholar -
Karasov W.H Digestive plasticity in avian energetics and feeding ecology. Avian energetics and nutritional ecology& Carey C . 1996pp. 61–84. Eds. New York, NY:Chapman & Hall. Crossref, Google Scholar -
Klaassen M, Oltrogge M& Trost L . 2004 Basal metabolic rate, food intake, and body mass in cold- and warm-acclimated Garden Warblers. Comp. Biochem. Physiol. A. 137, 639–647.doi:10.1016/j.cbpb.2003.12.004. . Crossref, PubMed, Web of Science, Google Scholar -
Kvist A& Lindström Å . 2001 Basal metabolic rate in migratory waders: intra-individual, intraspecific, interspecific and seasonal variation. Funct. Ecol. 15, 465–473.doi:10.1046/j.0269-8463.2001.00549.x. . Crossref, Web of Science, Google Scholar -
Lasiewski R.C& Dawson W.R . 1967 A re-examination of the relation between standard metabolic rate and body weight in birds. Condor. 69, 13–23. Crossref, Web of Science, Google Scholar -
Levey D.J, Place A.R, Rey P.J& Martinez del Rio C . 1999 An experimental test of dietary enzyme modulation in pine warblers Dendroica pinus. Physiol. Biochem. Zool. 72, 576–587.doi:10.1086/316689. . Crossref, PubMed, Web of Science, Google Scholar -
Lindström Å . 1997 Basal metabolic rates of migrating waders in the Eurasian Arctic. J. Avian Biol. 28, 87–92. Crossref, Web of Science, Google Scholar -
Lindström Å& Klaassen M . 2003 High basal metabolic rates of shorebirds while in the Arctic: a circumpolar view. Condor. 105, 420–427. Crossref, Web of Science, Google Scholar -
Lovegrove B.G . 2000 The zoogeography of mammalian basal metabolic rate. Am. Nat. 156, 201–219.doi:10.1086/303383. . Crossref, PubMed, Web of Science, Google Scholar -
Lovegrove B.G . 2003 The influence of climate on the basal metabolic rate of small mammals: a slow–fast metabolic continuum. J. Comp. Physiol. B. 173, 87–112. Crossref, PubMed, Web of Science, Google Scholar -
Lovegrove B.G . 2005 Seasonal thermoregulatory responses in mammals. J. Comp. Physiol. B. 175, 231–247.doi:10.1007/s00360-005-0477-1. . Crossref, PubMed, Web of Science, Google Scholar -
Martinez del Rio C, Brugger K.W, Rios J.L, Vergara M.E& Witmer M.C . 1995 An experimental and comparative study of dietary modulation of intestinal enzymes in the European starling. Physiol. Zool. 68, 490–511. Crossref, Google Scholar -
Martins E.P . 2000 Adaptation and the comparative method. Trends Ecol. Evol. 15, 296–299.doi:10.1016/S0169-5347(00)01880-2. . Crossref, PubMed, Web of Science, Google Scholar -
Martins E.P& Hansen T.F . 1997 Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646–667.doi:10.1086/286013. . Crossref, Web of Science, Google Scholar -
Martins E.P, Diniz-Filho J.A.F& Housworth E.A . 2002 Adaptive constraints and the phylogenetic comparative method: a computer simulation test. Evolution. 56, 1–13. Crossref, PubMed, Web of Science, Google Scholar -
McKechnie, A. E. 2001 Patterns, mechanisms and evolution of avian facultative hypothermic responses: a southern African perspective. Ph.D. thesis, University of Natal, Pietermaritzburg. Google Scholar
-
McKechnie A.E& Lovegrove B.G Heterothermic responses in the speckled mousebird (Colius striatus). J. Comp. Physiol. B. 171, 2001a 507–518.doi:10.1007/s003600100201. . Crossref, PubMed, Web of Science, Google Scholar -
McKechnie A.E& Lovegrove B.G Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius). Physiol. Biochem. Zool. 74, 2001b 238–249.doi:10.1086/319669. . Crossref, PubMed, Web of Science, Google Scholar -
McKechnie A.E& Lovegrove B.G . 2003 Facultative hypothermic responses in an Afrotropical arid-zone passerine, the red-headed finch (Amadina erythrocephala). J. Comp. Physiol. B. 173, 339–346.doi:10.1007/s00360-003-0341-0. . Crossref, PubMed, Web of Science, Google Scholar -
McKechnie A.E& Wolf B.O The allometry of avian basal metabolic rate: good predictions need good data. Physiol. Biochem. Zool. 77, 2004a 502–521.doi:10.1086/383511. . Crossref, PubMed, Web of Science, Google Scholar -
McKechnie A.E& Wolf B.O Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation. J. Exp. Biol. 207, 2004b 203–210.doi:10.1242/jeb.00757. . Crossref, PubMed, Web of Science, Google Scholar -
McNab B.K . 1986 The influence of food habits on the energetics of eutherian mammals. Ecol. Monogr. 56, 1–19. Crossref, Web of Science, Google Scholar -
McNab B.K . 1988 Complications inherent in scaling the basal rate of metabolism in mammals. Q. Rev. Biol. 63, 25–54.doi:10.1086/415715. . Crossref, PubMed, Web of Science, Google Scholar -
McNab B.K . 1997 On the utility of uniformity in the definition of basal rates of metabolism. Physiol. Zool. 70, 718–720. Crossref, PubMed, Google Scholar -
McNab B.K . 2001 Energetics of toucans, barbets and a hornbill: implications for avian frugivory. Auk. 118, 916–933. Crossref, Web of Science, Google Scholar -
McNab B.K . 2003 Ecology shapes bird bioenergetics. Nature. 426, 620–621.doi:10.1038/426620b. . Crossref, PubMed, Web of Science, Google Scholar -
Merola-Zwartjes M& Ligon J.D . 2000 Ecological energetics of the Puerto Rican tody: heterothermy, torpor and intra-island variation. Ecology. 81, 990–1002. Crossref, Web of Science, Google Scholar -
Moss R . 1972 Effects of captivity on gut lengths in red grouse. J. Wildl. Manage. 36, 99–104. Crossref, Web of Science, Google Scholar -
Mueller P& Diamond J . 2001 Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc. Natl Acad. Sci. USA. 98, 12 550–12 554.doi:10.1073/pnas.221456698. . Crossref, Web of Science, Google Scholar -
Pagel M . 1994 Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. B. 255, 37–45. Link, Web of Science, Google Scholar -
Pagel M . 1999 Inferring the historical patterns of biological evolution. Nature. 401, 877–884.doi:10.1038/44766. . Crossref, PubMed, Web of Science, Google Scholar -
Piersma T& Drent J . 2003 Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18, 228–233.doi:10.1016/S0169-5347(03)00036-3. . Crossref, Web of Science, Google Scholar -
Piersma T, Cadée N& Daan S . 1995 Seasonality in basal metabolic rate and thermal conductance in a long distance migrant shorebird, the knot (Calidris canutus). J. Comp. Physiol. 165, 37–45. Crossref, Web of Science, Google Scholar -
Reynolds P.S& Lee R.M . 1996 Phylogenetic analysis of avian energetics: passerines and non-passerines do not differ. Am. Nat. 147, 735–759.doi:10.1086/285877. . Crossref, Web of Science, Google Scholar -
Rezende E.L, Swanson D.L, Novoa F.F& Bozinovic F . 2002 Passerines versus nonpasserines: so far, no statistical differences in the scaling of avian energetics. J. Exp. Biol. 205, 101–107. Crossref, PubMed, Web of Science, Google Scholar -
Sakamoto Y, Ishiguro M& Kitagawa G Akaike information criterion statistics. 1986 Dordrecht, The Netherlands:D. Reidel. Google Scholar -
Savage V.M, Gillooly J.F, Woodruff W.H, West G.B, Allen A.P, Enquist B.J& Brown J.H . 2004 The predominance of quarter-power scaling in biology. Funct. Ecol. 18, 257–282.doi:10.1111/j.0269-8463.2004.00856.x. . Crossref, Web of Science, Google Scholar -
Schleucher E . 2002 Metabolism, body temperature and thermal conductance of fruit-doves (Aves: Columbidae, Treronidae). Comp. Biochem. Physiol. A. 131, 417–428.doi:10.1016/S1095-6433(01)00499-8. . Crossref, PubMed, Web of Science, Google Scholar -
Schleucher E& Withers P.C . 2002 Metabolic and thermal physiology of doves and pigeons. Physiol. Biochem. Zool. 75, 439–450.doi:10.1086/342803. . Crossref, PubMed, Web of Science, Google Scholar -
Schlichting C.D& Pigliucci M Phenotypic evolution: a reaction norm perspective. 1998 Sunderland, MA:Sinauer Associates. Google Scholar -
Scholander P.F, Hock R, Walters V& Irving L . 1950 Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation and basal metabolic rate. Biol. Bull. 99, 259–271. Crossref, PubMed, Web of Science, Google Scholar -
Sibley C.G& Ahlquist J.E Phylogeny and classification of birds. 1990 New Haven, CT:Yale University Press. Google Scholar -
Starck J.M . 1999 Phenotypic flexibility of the avian gizzard: rapid, reversible and repeated changes of organ size in response to changes in dietary fibre content. J. Exp. Biol. 202, 3171–3179. Crossref, PubMed, Web of Science, Google Scholar -
Swanson, D. L. In press. Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr. Ornithol. 17. Google Scholar
-
Swanson D.L& Olmstead K.L . 1999 Evidence for a proximate influence of winter temperatures on metabolism in passerine birds. Physiol. Biochem. Zool. 72, 566–575.doi:10.1086/316696. . Crossref, PubMed, Web of Science, Google Scholar -
Tieleman B.I& Williams J.B . 2000 The adjustment of avian metabolic rates and water fluxes to desert environments. Physiol. Biochem. Zool. 73, 461–479.doi:10.1086/317740. . Crossref, PubMed, Web of Science, Google Scholar -
Tieleman B.I& Williams J.B . 2002 Cutaneous and respiratory water loss in larks from arid and mesic environments. Physiol. Biochem. Zool. 75, 590–599.doi:10.1086/344491. . Crossref, PubMed, Web of Science, Google Scholar -
Tieleman B.I, Williams J.B& Buschur M.E . 2002 Physiological adjustments to arid and mesic environments in larks (Alaudidae). Physiol. Biochem. Zool. 75, 305–313.doi:10.1086/341998. . Crossref, PubMed, Web of Science, Google Scholar -
Tieleman B.I, Williams J.B, Buschur M.E& Brown C.R . 2003 Phenotypic variation of larks along an aridity gradient: are desert birds more flexible?. Ecology. 84, 1800–1815. Crossref, Web of Science, Google Scholar -
Weathers W.W . 1979 Climatic adaptation in avian standard metabolic rate. Oecologia. 42, 81–89. Crossref, PubMed, Web of Science, Google Scholar -
Weathers W.W, Weathers D.L& van Riper C . 1983 Basal metabolism of the apapane: comparison of freshly caught birds with long-term captives. Auk. 100, 977–978. Crossref, Web of Science, Google Scholar -
West G.B, Brown J.H& Enquist B . 1997 A general model for the origin of allometric scaling laws in biology. Science. 276, 122–126.doi:10.1126/science.276.5309.122. . Crossref, PubMed, Web of Science, Google Scholar -
West G.B, Savage V.M, Gillooly J.F, Enquist B, Woodruff W.H& Brown J.H . 2003 Why does metabolic rate scale with body size?. Nature. 421, 713 doi:10.1038/421713a. . Crossref, PubMed, Web of Science, Google Scholar -
White C.R& Seymour R.S . 2003 Mammalian basal metabolic rate is proportional to body mass2/3. Proc. Natl Acad. Sci. USA. 100, 4046–4049.doi:10.1073/pnas.0436428100. . Crossref, PubMed, Web of Science, Google Scholar -
Wikelski M, Spinney L, Schelsky W, Scheuerlein A& Gwinner E . 2003 Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc. R. Soc. B. 270, 2383–2388.doi:10.1098/rspb.2003.2500. . Link, Web of Science, Google Scholar
