Skip to main content
SpringerLink
Log in

Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Metabolic rate is commonly thought to scale with body mass (M) to the 3/4 power. However, the metabolic scaling exponent (b) may vary with activity state, as has been shown chiefly for interspecific relationships. Here I use a meta-analysis of literature data to test whether b changes with activity level within species of ectothermic animals. Data for 19 species show that b is usually higher during active exercise (mean ± 95% confidence limits = 0.918 ± 0.038) than during rest (0.768 ± 0.069). This significant upward shift in b to near 1 is consistent with the metabolic level boundaries hypothesis, which predicts that maximal metabolic rate during exercise should be chiefly influenced by volume-related muscular power production (scaling as M 1). This dependence of b on activity level does not appear to be a simple temperature effect because body temperature in ectotherms changes very little during exercise.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

b :

Metabolic scaling exponent (slope of log metabolic rate in relation to log body mass)

AMR:

Maximal or near maximal metabolic rate during activity

L :

Metabolic level or elevation of a scaling relationship

M :

Live body mass

RMR:

Resting or standard metabolic rate

T B :

Body temperature

References

  • Apol MEF, Etienne RS, Olff H (2008) Revisiting the evolutionary origin of allometric metabolic scaling in biology. Funct Ecol 22:1070–1080

    Article  Google Scholar 

  • Armstrong JD, Priede IG, Lucas MC (1992) The link between respiratory capacity and changing metabolic demands during growth of northern pike, Esox lucius L. J Fish Biol 41(Suppl B):65–75

    Article  Google Scholar 

  • Banavar JR, Maritan A, Rinaldo A (1999) Size and form in efficient transport networks. Nature 399:130–134

    Article  PubMed  CAS  Google Scholar 

  • Banavar JR, Damuth J, Maritan A, Rinaldo A (2006) Comment on “Revising the distributive networks models of West, Brown and Enquist (1997) and Banavar, Maritan and Rinaldo (1999): metabolic inequity of living tissues provides clues for the observed allometric scaling rules” by Makarieva, Gorshkov and Li. J Theor Biol 239:391–393

    Article  PubMed  Google Scholar 

  • Barbosa LA, Garcia GJM, da Silva JKL (2006) The scaling of maximum and basal metabolic rates of mammals and birds. Physica A 359:547–554

    Article  CAS  Google Scholar 

  • Bartholomew GA (1982) Body temperature and energy metabolism. In: Gordon MS, Bartholomew GA, Grinnell AD, Jørgensen CB, White FN (eds) Animal physiology: principles and adaptations, 4th edn. Macmillan, New York, pp 333–406

    Google Scholar 

  • Bokma F (2004) Evidence against universal metabolic allometry. Funct Ecol 18:184–187

    Article  Google Scholar 

  • Brett JR (1965) The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon (Oncorhynchus nerka). J Fish Bd Canada 22:1491–1501

    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 

  • Brown JH, West GB, Enquist BJ (2005) Yes, West, Brown and Enquist’s model of allometric scaling is both mathematically correct and biologically relevant. Funct Ecol 19:735–738

    Article  Google Scholar 

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

    Google Scholar 

  • Chaui-Berlinck JG (2006) A critical understanding of the fractal model of metabolic scaling. J Exp Biol 209:3045–3054

    Article  PubMed  Google Scholar 

  • Chaui-Berlinck JG (2007) Response to ‘Comment on “A critical understanding of the fractal model of metabolic scaling”‘. J Exp Biol 210:3875–3876

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ferguson RA, Krustrup P, Kjær M, Mohr M, Ball D, Bangsbo J (2006) Effect of temperature on skeletal muscle energy turnover during dynamic knee-extensor exercise in humans. J Appl Physiol 101:47–52

    Article  PubMed  CAS  Google Scholar 

  • Garland T (1984) Physiological correlates of locomotory performance in a lizard: an allometric approach. Am J Physiol 247:R806–R815

    PubMed  CAS  Google Scholar 

  • Garland T, Else PL (1987) Seasonal, sexual, and individual variation in endurance and activity metabolism in lizards. Am J Physiol 252:R439–R449

    PubMed  CAS  Google Scholar 

  • Gatten RE, Miller K, Full RJ (1992) Energetics at rest and during locomotion. In: Feder ME, Burggren WW (eds) Environmental physiology of the Amphibia. University of Chicago Press, Chicago, pp 314–377

    Google Scholar 

  • Gillooly JF, Allen AP (2007) Changes in body temperature influence the scaling of VO2max and aerobic scope in mammals. Biol Lett 3:99–102

    Article  PubMed  Google Scholar 

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  PubMed  CAS  Google Scholar 

  • Glazier DS (2005) Beyond the ‘3/4-power law’: variation in the intra- and interspecific scaling of metabolic rate in animals. Biol Rev 80:611–662

    Article  PubMed  Google Scholar 

  • Glazier DS (2006) The 3/4-power law is not universal: evolution of isometric, ontogenetic metabolic scaling in pelagic animals. BioScience 56:325–332

    Article  Google Scholar 

  • Glazier DS (2008) Effects of metabolic level on the body-size scaling of metabolic rate in birds and mammals. Proc R Soc Lond B 275:1405–1410

    Article  Google Scholar 

  • Glazier DS (2009a) A unifying explanation for diverse metabolic scaling in animals and plants. Biol Rev (in press)

  • Glazier DS (2009b) Metabolic level and size scaling of rates of respiration and growth in unicellular organisms. Funct Ecol (in press)

  • Glazier DS (2009c) Ontogenetic body-mass scaling of resting metabolic rate covaries with species-specific metabolic level and body size in spiders and snakes. Comp Biochem Physiol A. doi:10.1016/j.cbpa.2009.03.020

  • Gunn DL (1942) Body temperature in poikilothermal animals. Biol Rev 17:293–314

    Article  Google Scholar 

  • Heinrich B (1974) Thermoregulation in endothermic insects. Science 185:747–756

    Article  PubMed  CAS  Google Scholar 

  • Heinrich B (1993) The hot-blooded insects. Harvard University Press, Cambridge, Massachusetts

    Google Scholar 

  • Hemmingsen AM (1960) Energy metabolism as related to body size and respiratory surfaces, and its evolution. Rep Steno Memorial Hospital Nordisk Insulin Laboratorium 9:1–110

    Google Scholar 

  • Hughes GM, Gaymer R, Moore M, Woakes AJ (1971) Respiratory exchange and body size in the Aldabra giant tortoise. J Exp Biol 55:651–665

    PubMed  CAS  Google Scholar 

  • John-Adler HB (1984) Seasonal variations in activity, aerobic energetic capacities, and plasma thyroid hormones (T3 and T4) in an iguanid lizard. J Comp Physiol B 154:409–419

    Article  Google Scholar 

  • Killen SS, Costa I, Brown JA, Gamperl AK (2007) Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. Proc R Soc Lond B 274:431–438

    Article  Google Scholar 

  • Killen SS, Atkinson D, Glazier DS (2008) Ecological factors contributing to variation in the scaling of metabolic rate with body mass in fishes. Comp Biochem Physiol 150A:S111

    Google Scholar 

  • Koga S, Shiojiri T, Kondo N, Barstow TJ (1997) Effect of increased muscle temperature on oxygen uptake kinetics during exercise. J Appl Physiol 83:1333–1338

    PubMed  CAS  Google Scholar 

  • Kotiaho JS, Alatalo RV, Mappes J, Nielsen MG, Parri S, Rivero A (1998) Energetic costs of size and sexual signaling in a wolf spider. Proc R Soc Lond B 265:2203–2209

    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 (2005) West, Brown and Enquist’s model of allometric scaling again: the same questions remain. Funct Ecol 19:739–743

    Article  Google Scholar 

  • Lane N (2005) Power, sex, suicide: mitochondria and the meaning of life. Oxford University Press, Oxford

    Google Scholar 

  • Lyman CP (1968) Body temperature of exhausted salmon. Copeia 1968:631–633

    Article  Google Scholar 

  • Makarieva AM, Gorshkov VG, Li B-L (2005) Revising the distributive networks models of West, Brown & Enquist (1997) and Banavar, Maritan & Rinaldo (1999): metabolic inequity of living tissues provides clues for the observed allometric scaling rules. J Theor Biol 237:291–307

    Article  PubMed  Google Scholar 

  • Makarieva AM, Gorshkov VG, Li B-L (2006) Distributive network model of Banavar, Damuth, Maritan & Rinaldo (2002): Critique and perspective. J Theor Biol 239:394–397

    Article  PubMed  Google Scholar 

  • Marden JH, Allen LR (2002) Molecules, muscles, and machines: universal performance characteristics of motors. Proc Nat Acad Sci USA 99:4161–4166

    Article  PubMed  CAS  Google Scholar 

  • Mukai K, Hiraga A, Eto D, Takahashi T, Hada T, Tsubone H, Jones JH (2008) Effects of warm-up intensity on oxygen transport during supramaximal exercise in horses. Am J Vet Res 69:690–696

    Article  PubMed  Google Scholar 

  • Nagy KA (2005) Field metabolic rate and body size. J Exp Biol 208:1621–1625

    Article  PubMed  Google Scholar 

  • Niven JE, Scharlemann JP (2005) Do insect metabolic rates at rest and during flight scale with body mass? Biol Lett 1:346–349

    Article  PubMed  Google Scholar 

  • Ohlberger J, Staaks G, Hölker F (2007) Effects of temperature, swimming speed and body mass on standard and active metabolic rate in vendace (Coregonus albula). J Comp Physiol B 177:905–916

    Article  PubMed  Google Scholar 

  • Painter PR (2005) Allometric scaling of the maximum metabolic rate of mammals: oxygen transport from the lungs to the heart is a limiting step. Theor Biol Med Modelling 2:31. doi:10.1186/1742-4682-2-31

    Article  Google Scholar 

  • Pough FH, Andrews RM (1984) Individual and sibling-group variation in metabolism of lizards: the aerobic capacity model for the origin of endothermy. Comp Biochem Physiol 79A:415–419

    Article  CAS  Google Scholar 

  • Prange HD, Jackson DC (1976) Ventilation, gas exchange and metabolic scaling of a sea turtle. Resp Physiol 27:369–377

    Article  CAS  Google Scholar 

  • Rajagopal PK, Kramer RH (1974) Respiratory metabolism of Utah chub, Gila atraria (Girad) and speckled dace, Rhinichthyes osculus (Girard). J Fish Biol 6:215–222

    Article  Google Scholar 

  • Rao GMM (1968) Oxygen consumption of rainbow trout (Salmo gairdneri) in relation to activity and salinity. Can J Zool 46:781–786

    Article  PubMed  CAS  Google Scholar 

  • Reich PB, Tjoelker MG, Machado J-L, Oleksyn J (2006) Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439:457–461

    Article  PubMed  CAS  Google Scholar 

  • Robinson WR, Peters RH, Zimmermann J (1983) The effects of body size and temperature on metabolic rate of organisms. Can J Zool 61:281–288

    Article  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 

  • Savage VM, Enquist BJ, West GB (2007) Comment on “A critical understanding of the fractal model of metabolic scaling”‘. J Exp Biol 210:3873–3874

    Article  PubMed  Google Scholar 

  • Savage VM, Deeds EJ, Fontana W (2008) Sizing up allometric scaling theory. PLoS Comput Biol 4:e1000171. doi:10.1371/journal.pcbi.1000171

    Article  PubMed  CAS  Google Scholar 

  • Simpson S (1908) The body-temperature of fishes and other marine animals. Proc R Soc Edinburgh 28:66–84

    Google Scholar 

  • Taigen TL, Pough FH (1981) Activity metabolism of the toad (Bufo americanus): ecological consequences of ontogenetic change. J Comp Physiol 144:247–252

    Google Scholar 

  • Tarby MJ (1981) Metabolic expenditure of walleye (Stizostedion vitreum vitreum) as determined by rate of oxygen consumption. Can J Zool 59:882–889

    Article  Google Scholar 

  • Thompson GG, Withers PC (1997) Standard and maximal metabolic rates of goannas (Squamata: Varanidae). Physiol Zool 70:307–323

    PubMed  CAS  Google Scholar 

  • Wallace JC (1972) Activity and metabolic rate in the shore crab, Carcinus maenas (L.). Comp Biochem Physiol 41A:523–533

    Article  Google Scholar 

  • Walton M (1988) Relationships among metabolic, locomotory, and field measures of organismal performance in the Fowler’s toad (Bufo woodhousei fowleri). Physiol Zool 61:107–118

    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 

  • Weibel ER, Bacigalupe LD, Schmitt B, Hoppeler H (2004) Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Resp Physiol Neurobiol 140:115–132

    Article  Google Scholar 

  • West GB, Brown JH (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592

    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  PubMed  CAS  Google Scholar 

  • White CR, Seymour RS (2005) Allometric scaling of mammalian metabolism. J Exp Biol 208:1611–1619

    Article  PubMed  CAS  Google Scholar 

  • White CR, Phillips NF, Seymour RS (2006) The scaling and temperature dependence of vertebrate metabolism. Biol Lett 2:125–127

    Article  PubMed  Google Scholar 

  • White CR, Cassey P, Blackburn TM (2007) Allometric exponents do not support a universal metabolic allometry. Ecology 88:315–323

    Article  PubMed  Google Scholar 

  • 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 22:616–623

    Article  Google Scholar 

  • Wood TG, Lawton JH (1973) Experimental studies on the respiratory rates of mites (Acari) from beech-woodland leaf litter. Oecologia 12:169–191

    Article  Google Scholar 

Download references

Acknowledgments

I thank Shaun S. Killen for providing me with unpublished data on study temperatures and body-mass ranges for Cyclopterus lumpus L., Macrozoarces americanus (Bloch and Schneider) and Myoxocephalus scorpius (L.), Jan Ohlberger for providing me with unpublished data on active metabolic rates in relation to body mass in the vendace Coregonus albula (L.), James H. Jones, Hans Hoppeler and Ewald R. Weibel for kindly allowing me to see their unpublished data on temporal changes in metabolic rate and body temperature in running horses, and two anonymous reviewers for providing helpful comments on a previous version of this paper.

Author information

Authors and Affiliations

  1. Department of Biology, Juniata College, Huntingdon, PA, 16652, USA

    Douglas Stewart Glazier

Authors
  1. Douglas Stewart Glazier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Douglas Stewart Glazier.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Glazier, D.S. Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals. J Comp Physiol B 179, 821–828 (2009). https://doi.org/10.1007/s00360-009-0363-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-009-0363-3

Keywords

Search

Navigation