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Causes and significance of variation in mammalian basal metabolism

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Abstract

Mammalian basal metabolic rates (BMR) increase with body mass, whichs explains approximately 95% of the variation in BMR. However, at a given mass, there remains a large amount of variation in BMR. While many researchers suggest that the overall scaling of BMR with body mass is due to physiological constraints, variation at a given body mass may provide clues as to how selection acts on BMR. Here, we examine this variation in BMR in a broad sample of mammals and we test the hypothesis that, across mammals, body composition explains differences in BMR at a given body mass. Variation in BMR is strongly correlated with variation in muscle mass, and both of these variables are correlated with latitude and ambient temperature. These results suggest that selection alters BMR in response to thermoregulatory pressures, and that selection uses muscle mass as a means to generate this variation.

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References

  • Artacho P, Nespolo RF (2009) Natural selection reduces energy metabolism in the garden snail, Helix aspersa (Cornu aspersum). Evolution 63:1044–1050

    Article  CAS  PubMed  Google Scholar 

  • 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 16:906–913

    Article  Google Scholar 

  • Blanco RE, Gambini R (2007) Maximum running speed limitations on terrestrial mammals: a theoretical approach. J Biomech 40:2517–2522

    Article  PubMed  Google Scholar 

  • Bozinovic F, Muñoz JLP, Cruz-Neto AP (2007) Intraspecific variability in the basal metabolic rate: testing the food habits hypothesis. Physiol Biochem Zool 80:452–460

    Article  PubMed  Google Scholar 

  • Bozinovic F, Rojas JM, Broitman BR, Vásquez RA (2009) Basal metabolism is correlated with habitat productivity among populations of degus (Octodon degus). Comp Biochem Physiol A 152:560–564

    Article  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Calder WA (1984) Size, function, and life history. Harvard University Press, Cambridge

    Google Scholar 

  • Careau V, Morand-Ferron J, Thomas D (2007) Basal metabolic rate of canidae from hot deserts to cold arctic climates. J Mammal 88:394–400

    Article  Google Scholar 

  • Chown SL, Addo-Bediako A, Gaston KJ (2003) Physiological diversity: listening to the large-scale signal. Funct Ecol 17:568–572

    Article  Google Scholar 

  • Crile G, Quiring D (1940) A record of the body weight and certain organ and glad weights of 3690 animals. Ohio J Sci 40:219–259

    Google Scholar 

  • Daan S, Masman D, Groenewold A (1990) Avian basal metabolic rates: their association with body composition and energy expenditure. Am J Physiol 259:R333–R340

    CAS  PubMed  Google Scholar 

  • Darveau CA, Suarez RK, Andrews RD, Hochachka PW (2002) Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417:166–170

    Article  CAS  PubMed  Google Scholar 

  • Eisentraut M (1961) Beobachtugen uber den warmehaushalt bei halbaffen. Biol Zbl 80:319–325

    Google Scholar 

  • Field J, Belding HS, Martin AW (1939) An analysis of the relation between basal metabolism and summated tissue respiration in the rat. I. The post-pubertal albino rat. J Cell Comp Physiol 14:143–157

    Article  CAS  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Grafen A (1989) The phylogenetic regression. Philos Trans R Soc Lond B Biol Sci 326:119–157

    Article  CAS  PubMed  Google Scholar 

  • Grand TI (1977) Body weight: its relation to tissue composition, segment distribution, and motor function. I. Interspecific comparisons. Am J Phys Anthropol 47:211–240

    Article  CAS  PubMed  Google Scholar 

  • Grand TI (1983) Body-weight—its relationship to tissue composition, segmental distribution of mass, and motor function. 3. The didelphidae of French-Guyana. Aust J Zool 31:299–312

    Article  Google Scholar 

  • Grand TI (1990) Body composition and the evolution of the Macropodidae (Potorous, Dendrolagus and Macropus). Anat Embryol 182:85–92

    Article  CAS  PubMed  Google Scholar 

  • Grand TI, Barboza F (2001) Anatomy and development of the koala, Phascolarctes cinereus: an evolutionary perspective on the superfamily Vombatoidea. Anat Embryol 203:211–223

    Article  CAS  PubMed  Google Scholar 

  • Hodkinson ID (2003) Metabolic cold adaptation in arthropods: a smaller-scale perspective. Funct Ecol 17:562–567

    Article  Google Scholar 

  • Holliday MA (1986) Body composition and energy needs during growth. In: Falkner P, Tanner JM (eds) Human growth: a comprehensive treatise. Plenum Press, New York, pp 101–117

    Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Article  Google Scholar 

  • Isler K, van Schaik CP (2006) Metabolic costs of brain size evolution. Biol Lett 2:557–560

    Article  PubMed  Google Scholar 

  • 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 70:633–640

    Article  Google Scholar 

  • Kleiber M (1932) Body size and metabolism. Hilgardia 6:315–353

    CAS  Google Scholar 

  • Konarzewski M, Diamond J (1995) Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 49:1239–1248

    Article  Google Scholar 

  • Kozłowski J, Konarzewski M (2004) Is West, Brown and Enquist’s model of allometric scaling mathematically correct and biologically relevant? Funct Ecol 18:283–289

    Article  Google Scholar 

  • Kozłowski J, Konarzewski M, Gawelczyk AT (2003) Intraspecific body size optimization produces intraspecific allometries. In: Blackburn TM, Gaston KJ (eds) Macroecology: concepts and consequences. Blackwell Science Ltd, Malden, pp 299–320

    Google Scholar 

  • Kurland JA, Pearson JD (1986) Ecological significance of hypometabolism in nonhuman primates: allometry, adaptation, and deviant diets. Am J Phys Anthropol 71:445–457

    Article  CAS  PubMed  Google Scholar 

  • Leonard WR, Sorenson MV, Galloway VA, Spencer GJ, Mosher MJ, Osipova L, Spitsyn VA (2002) Climatic influences on basal metabolic rates among circumpolar populations. Am J Hum Biol 14:609–620

    Article  PubMed  Google Scholar 

  • Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219

    Article  PubMed  Google Scholar 

  • Lovegrove BG (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

    CAS  PubMed  Google Scholar 

  • Lovegrove BG (2004) Locomotor mode, maximum running speed, and basal metabolic rate in placental mammals. Physiol Biochem Zool 77:916–928

    Article  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis version 2.6. http://www.mesquiteproject.org

  • Martin AW, Fuhrman FA (1955) The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Zool 28:18–34

    Google Scholar 

  • McNab BK (1969) The economics of temperature regulation in neotropical bats. Comp Biochem Physiol 31:227–268

    Article  CAS  PubMed  Google Scholar 

  • McNab BK (1978) Energetics of arboreal folivores: physiological problems and ecological consequences of feeding on an ubiquitous food supply. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, pp 153–162

    Google Scholar 

  • McNab BK (1986) The influence of food habits on the energetics of eutherian mammals. Ecol Monogr 56:1–19

    Article  Google Scholar 

  • McNab BK (1994) Energy conservation and the evolution of flightlessness in birds. Am Nat 144:628–642

    Article  Google Scholar 

  • McNab BK (2000) The standard energetics of mammalian carnivores: Felidae and Hyaenidae. Can J Zool 78:2227–2239

    Article  Google Scholar 

  • McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, Ithica

    Google Scholar 

  • McNab BK (2007) The evolution of energetics in birds and mammals. Univ Calif Publ Zool 137:67–110

    Google Scholar 

  • McNab BK, Ellis HI (2006) Flightless rails endemic to islands have lower energy expenditures and clutch sizes than flighted rails on islands and continents. Comp Biochem Physiol 145:295–311

    Article  Google Scholar 

  • McNab BK, Morrison P (1963) Body temperature and metabolism in subspecies of Peromyscus from arid and mesic environments. Ecol Monogr 33:63–82

    Article  Google Scholar 

  • Midford PE, Garland T Jr, Maddison WP (2003) PDAP package

  • Muchlinski MN, Snodgrass JJ, Terranova CJ (2003) Scaling of muscle mass in primates. Am J Phys Anthropol Suppl 36:155

    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 98:12550–12554

    Article  CAS  PubMed  Google Scholar 

  • Nevill AM, Markovic G, Vucetic V, Holder R (2004) Can greater muscularity in larger individuals resolve the 3/4 power-law controversy when modelling maximum oxygen uptake? Ann Hum Biol 31:436–445

    Article  CAS  PubMed  Google Scholar 

  • Pitts GC, Bullard TR (1968) Some interspecific aspects of body composition in mammals. In: Council NR (ed) Body composition in animals and man. National Academy of Sciences, Washington, pp 45–79

    Google Scholar 

  • Rezende EL, Bozinovic F, Garland T (2004) Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents. Evolution 58:1361–1374

    PubMed  Google Scholar 

  • Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071

    Article  Google Scholar 

  • Roberts DF (1978) Climate and human variability. Cummings, Menlo Park

    Google Scholar 

  • Rolfe D, Brown G (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    CAS  PubMed  Google Scholar 

  • Savage VM, Gillooly JF, Woodruff WH, West GB, Allen AP, Enquist BJ, Brown JH (2004) The predominance of quarter-power scaling in biology. Funct Ecol 18:257–282

    Article  Google Scholar 

  • Schkolnik A, Schmidt-Nielsen K (1976) Temperature regulation in hedgehogs from temperate and desert environments. Physiol Zool 49:56–64

    Google Scholar 

  • Schmidt-Nielsen K (1984) Scaling: why is animal size so important. Cambridge University Press, Cambridge

    Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology. Cambridge University Press, Cambridge

    Google Scholar 

  • Selman C, Lumsden S, Bünger L, Hill WG, Speakman JR (2001) Resting metabolic rate and morphology in mice (Mus musculus) selected for high and low food intake. J Exp Biol 204:777–784

    CAS  PubMed  Google Scholar 

  • Snodgrass JJ, Leonard WR, Tarskaia LA, Alekseev VP, Krivoshapkin VG (2005) Basal metabolic rate in the Yakut (Sakha) of Siberia. Am J Hum Biol 17:155–172

    Article  PubMed  Google Scholar 

  • Snodgrass JJ, Leonard WR, Robertson ML (2007) Primate bioenergetics: an evolutionary perspective. In: Ravosa MJ, Dagosto M (eds) Primate origins: adaptations and evolution. Springer, New York, pp 703–737

    Chapter  Google Scholar 

  • Swanson DL, Liknes ET (2006) A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Biol 209:466–474

    Article  PubMed  Google Scholar 

  • Terranova CJ, Coffman BS (1998) Body weights of wild and captive lemurs. Zoo Biol 16:17–30

    Article  Google Scholar 

  • Wang Z, O’Connor TP, Heshka S, Heymsfield SB (2001) The reconstruction of Kleiber’s law at the organ-tissue level. J Nutr 131:2967–2970

    CAS  PubMed  Google Scholar 

  • Weibel ER, Hoppeler H (2005) Exercise-induced maximal metabolic rate scales with muscle aerobic capacity. J Exp Biol 208:1635–1644

    Article  PubMed  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126

    Article  CAS  PubMed  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1999) The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284:1677–1679

    Article  CAS  PubMed  Google Scholar 

  • White CR, Seymour RS (2003) Mammalian basal metabolic rate is proportional to body mass2/3. Proc Natl Acad Sci USA 100:4046–4049

    Article  CAS  PubMed  Google Scholar 

  • Withers PC, Cooper CE, Larcombe AN (2006) Environmental correlates of physiological variables in marsupials. Physiol Biochem Zool 79:437–453

    Article  CAS  PubMed  Google Scholar 

  • Zihlman AL (1984) Body build and tissue composition in Pan paniscus and Pan troglodytes, with comparisons to other hominoids. In: Susman RL (ed) The pygmy chimpanzee: evolutionary biology and behavior. Plenum Press, New York, pp 179–200

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Acknowledgments

We thank C.J. Terranova for access to primate cadavers and B. Enquist and A. Foster for helpful discussions. We also thank Ian Hume and two anonymous reviewers for their comments and suggestions. Muscle mass data collection was funded partially by a University of Texas Liberal Arts Graduate Research Grant awarded to MNM.

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Authors and Affiliations

  1. Department of Anthropology, University of Arizona, 1009 E. South Campus Drive, Tucson, AZ, 85721, USA

    David A. Raichlen

  2. Department of Anthropology, University at Albany, SUNY, Albany, NY, USA

    Adam D. Gordon

  3. Department of Anatomy and Pathology, Marshall University, School of Medicine, Huntington, VA, USA

    Magdalena N. Muchlinski

  4. Department of Anthropology, University of Oregon, Corvallis, OR, USA

    J. Josh Snodgrass

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  1. David A. Raichlen
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  2. Adam D. Gordon
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  3. Magdalena N. Muchlinski
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  4. J. Josh Snodgrass
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Correspondence to David A. Raichlen.

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Communicated by I. D. Hume.

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Raichlen, D.A., Gordon, A.D., Muchlinski, M.N. et al. Causes and significance of variation in mammalian basal metabolism. J Comp Physiol B 180, 301–311 (2010). https://doi.org/10.1007/s00360-009-0399-4

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  • DOI: https://doi.org/10.1007/s00360-009-0399-4

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