Skip to main content
SpringerLink
Log in

Is BMR repeatable in deer mice? Organ mass correlates and the effects of cold acclimation and natal altitude

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

Abstract

Basal metabolic rate (BMR) is probably the most studied aspect of energy metabolism in vertebrate endotherms. Numerous papers have explored its mass allometry, phylogenetic and ecological relationships, and ontogeny. Implicit in many of these studies (and explicit in some) is the view that BMR responds to selection, which requires repeatability and heritability. However, BMR is highly plastic in response to numerous behavioral and environmental factors and there are surprisingly few data on its repeatability. Moreover, the mechanistic underpinnings of variation in BMR are unclear, despite considerable research. We studied BMR repeatability in deer mice (Peromyscus maniculatus) across intervals of 30–60 days, and also examined the influence of birth altitude (3,800 m versus 340 m) and temperature acclimation (to ∼5 or ∼20°C) on BMR, and the relationship between BMR and organ size. Neither acclimation temperature nor natal altitude alone influenced BMR, but the combination of birth at high altitude and cold acclimation significantly increased BMR. Few visceral organ masses were correlated to BMR and most were inconsistent across natal altitudes and acclimation temperatures, indicating that no single organ ‘controls’ variation in BMR. In several treatment groups, the mass of the ‘running motor’ (combined musculoskeletal mass) was negatively correlated to BMR and the summed mass of visceral organs was positively correlated to BMR. We found no repeatability of BMR in any treatment group. That finding—in sharp contrast to high repeatability of BMR in several other small endotherms—suggests little potential for direct selection to drive BMR evolution in deer mice.

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
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

BMR:

Basal metabolic rate

FMR:

Field metabolic rate

RMR:

Resting metabolic rate

\( \ifmmode\expandafter\dot\else\expandafter\.\fi{V}{\text{O}}_{{{2} }} \) :

Rate of oxygen consumption

\( \ifmmode\expandafter\dot\else\expandafter\.\fi{V}{\text{O}}_{{{{2\,{\text{max}}}} }} \) :

Maximal \( \ifmmode\expandafter\dot\else\expandafter\.\fi{V}{\text{O}}_{{{2} }} \) in exercise

\( \ifmmode\expandafter\dot\else\expandafter\.\fi{V}{\text{O}}_{{{{2\;{\text{sum}}}} }} \) :

Maximal \( \ifmmode\expandafter\dot\else\expandafter\.\fi{V}{\text{O}}_{{{2} }} \) during cold exposure

TNZ:

Thermal neutral zone

References

  • Bech C, Langseth I, Gabrielsen GW (1999) Repeatability of basal metabolism in breeding female kittiwakes Rissa tridactyla. Proc R Soc Lon B 266:2161–2167

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bennett AF (1987) Inter-individual variability: an underutilized resource. In: Feder ME, Bennett AF, Burggren WW, Huey RB (eds) New directions in ecological physiology. Cambridge University Press, Cambridge, pp 11–37

    Google Scholar 

  • Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654

    Article  PubMed  CAS  Google Scholar 

  • Berteaux D, Thomas DW, Bergeron J-M, Lapierre H (1996) Repeatability of daily field metabolic rate in female meadow voles (Microtus pennsylvanicus). Funct Ecology 10:751–759

    Article  Google Scholar 

  • Bozinovic F (1992) Scaling of basal and maximum metabolic-rate in rodents and the aerobic capacity model for the evolution of endothermy. Physiol Zool 65:921–932

    Google Scholar 

  • Burness GP, Ydenberg RC, Hochachka PW (1998) Interindividual variability in body composition and resting oxygen consumption rates in breeding tree swallows, Tachycineta bicolor. Physiol Zool 71:247–256

    PubMed  CAS  Google Scholar 

  • Campbell KL, MacArthur RA (1998) Nutrition and the energetic tactics of muskrats (Ondatra zibethicus): morphological and metabolic adjustments to seasonal shifts in diet quality. Can J Zool 76:163–174

    Article  Google Scholar 

  • Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359

    Article  PubMed  CAS  Google Scholar 

  • Chappell MA, Hammond KA (2004) Maximal aerobic performance of deer mice in combined cold and exercise challenges. J Comp Physiol B 174:41–48

    Google Scholar 

  • Chappell MA, Holsclaw DS (1984) Effects of wind on thermoregulation and energy balance in deer mice (Peromyscus maniculatus). J Comp Physiol 154B:619–625

    Google Scholar 

  • Chappell MA, Snyder LRG (1984) Biochemical and physiological correlates of deer mouse a-chain hemoglobin polymorphisms. Proc Natl Acad Sci USA 81:5484–5488

    Article  PubMed  CAS  Google Scholar 

  • Chappell MA, Bachman GC, Odell JP (1995) Repeatability of maximal aerobic performance in Belding’s ground squirrels, Spermopholis beldingi. Funct Ecol 9:498–504

    Article  Google Scholar 

  • Chappell MA, Zuk M, Johnsen TS (1996) Repeatability of aerobic performance in red junglefowl: effects of ontogeny and nematode infection. Funct Ecol 10:578–585

    Article  Google Scholar 

  • Chappell MA, Bech C, Buttemer WA (1999) The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows. J Exp Biol 202:2269–2279

    PubMed  Google Scholar 

  • Chappell MA, Rezende EL, Hammond KA (2003) Age and aerobic performance in deer mice. J Exp Biol 206:1221–1231

    Article  PubMed  Google Scholar 

  • Cruz-Neto AP, Bozinovic F (2004) The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analysis. Physiol Biochem Zool 77:877–889

    Article  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Daan S, Masman D, Strijkstra A, Verhulst S (1990b) Intraspecific allometry of basal metabolic rate: relations with body size, temperature, composition and circadian phase in the kestrel (Falco tinnunculus). J Biol Rhythms 4:11–23

    Google Scholar 

  • Dawson TJ, Olson JM (1988) Thermogenic capabilities of the opossum Monodelphis domestica when warm and cold acclimated: similarities between American and Australian marsupials. Comp Biochem Physiol 89A:85–91

    Article  Google Scholar 

  • Dohm MR (2002) Repeatability estimates do not always set an upper limit to heritability. Funct Ecol 16:273–280

    Article  Google Scholar 

  • Frappell P, Westwood K, Maskrey MJ (1995) Ventilatory and metabolic responses to hypoxia during moderate hypothermia in anesthetized rats. J Appl Physiol 79:256–260

    PubMed  CAS  Google Scholar 

  • Garland T, Bennett AF (1990) Quantitative genetics of maximal oxygen consumption in a garter snake. Am J Physiol 259:R986–R992

    PubMed  Google Scholar 

  • Geluso K, Hayes JP (1999) Effects of dietary quality on basal metabolic rate and internal morphology of European starlings (Sturnus vulgaris). Physiol Zool 72:189–197

    Article  CAS  Google Scholar 

  • Hammond KA, Chappell MA, Cardullo RA, Lin RS, Johnsen TS (2000) The mechanistic basis of aerobic performance variation in red junglefowl. J Exp Biol 203:2053–2064

    PubMed  CAS  Google Scholar 

  • Hammond KA, Chappell MA, Kristan DM (2002) Developmental plasticity in aerobic performance in deer mice (Peromyscus maniculatus). Comp Biochem Physiol 133A:213–224

    CAS  Google Scholar 

  • Hart JS (1971) Rodents. In: Whittow GC (eds) Comparative physiology of thermoregulation, vol II. Academic, New York, pp 1–149

    Google Scholar 

  • Hayes JP (1989a) Altitudinal and seasonal effects on aerobic metabolism of deer mice. J Comp Physiol 159B:453–459

    Google Scholar 

  • Hayes JP (1989b) Field and maximal metabolic rates of deer mice (Peromyscus maniculatus) at low and high altitudes. Physiol Zool 62:732–744

    Google Scholar 

  • Hayes JP, Chappell MA (1986) Effects of cold acclimation on maximum oxygen consumption during cold exposure and treadmill exercise in deer mice, Peromyscus maniculatus. Physiol Zool 59:473–481

    Google Scholar 

  • Hayes JP, Chappell MA (1990) Individual consistency of maximal oxygen consumption in deer mice. Funct Ecol 4:495–503

    Article  Google Scholar 

  • Hayes JP, O’Connor CS (1999) Natural selection on thermogenic capacity of high-altitude deer mice. Evolution 53:1280–1287

    Article  Google Scholar 

  • Hayes JP, Bible CA, Boone JD (1998) Repeatability of mammalian physiology: evaporative water loss and oxygen consumption of Dipodomys merriami. J Mammal 79:475–485

    Article  Google Scholar 

  • Heldmaier G, Boeckler H, Buchberger A, Klaus S, Puchalski W, Steinlacher S, Wiesinger H (1986) Seasonal variation of thermogenesis. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold. Elsevier, New York, pp 361–372

    Google Scholar 

  • Hill RW (1983) Thermal physiology and energetics of Peromyscus: ontogeny, body temperature, metabolism, insulation, and microclimatology. J Mammal 64:19–37

    Article  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  • Horak P, Saks L, Ots I, Kollist H (2002) Repeatability of condition indices in captive greenfinches (Carduelis chloris). Can J Zool 80:636–643

    Article  Google Scholar 

  • Huey RB, Dunham AT (1987) Repeatability of locomotor performance in natural populations of the lizard, Sceloporus merriami. Evolution 41:1116–1120

    Article  Google Scholar 

  • IUPS Thermal Commission (1987) Glossary of terms for thermal physiology. Pflugers Arch 410:567–587

    Article  Google Scholar 

  • Jones JH (1998) Optimization of the mammalian respiratory system: symmorphosis versus single species adaptation. Comp Biochem Physiol 120B:125–138

    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 

  • Koteja P (1996a) Limits to the energy budget in a rodent, Peromyscus maniculatus: the central limitation hypothesis. Physiol Zool 69:981–993

    Google Scholar 

  • Koteja P (1996b) Limits to the energy budget in a rodent, Peromyscus maniculatus: does gut capacity set the limit? Physiol Zool 69:994–1020

    Google Scholar 

  • Krebs HA (1950) Body size and tissue respiration. Biochim Biophys Acta 4:249–269

    Article  PubMed  CAS  Google Scholar 

  • 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 271:367–372

    Article  Google Scholar 

  • Li X-S, Wang D-H (2005) Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J Comp Physiol 175B:593–600

    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 173B:87–112

    Google Scholar 

  • MacMillen RE, Garland T Jr (1989) Adaptive physiology. In: Layne JN, Kirkland GL Jr (eds) Advances in the study of Peromyscus. Texas Tech University Press, Lubbock, pp 143–168

    Google Scholar 

  • Mathias ML, Nunes AC, Marques CC, Sousa I, Ramalhinho MG, Auffray JC, Catalan J, Britton-Davidian J (2004) Adaptive energetics in house mice, Mus musculus domesticus, from the island of Porto Santo (Madeira archipelago, North Atlantic). Comp Biochem Physiol 137A:703–709

    CAS  Google Scholar 

  • McLean JA, Speakman JR (2000) Effects of body mass and reproduction on the basal metabolic rate of brown long-eared bats (Plecotus auritus). Physiol Biochem Zool 73:112–121

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Meagher S, O’Connor TP (2001) Population variation in the metabolic response of deer mice to infection with Capillaria hepatica (Nematoda). Can J Zool 79:554–561

    Article  Google Scholar 

  • Meerlo P, Bolle L, Visser GH, Masman D, Daan S (1997) Basal metabolic rate in relation to body composition and daily energy expenditure in the field vole, Microtus agrestis. Physiol Zool 70:362–369

    PubMed  CAS  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 58:12550–12554

    Article  Google Scholar 

  • Nespolo RF, Bacigalupe LD, Sabat P, Bozinovic F (2002) Interplay among energy metabolism, organ mass and digestive enzyme activity in the mouse-opossum Thylamys elegans: the role of thermal acclimation. J Exp Biol 205:2697–2703

    PubMed  Google Scholar 

  • Piersma T, Bruinzeel L, Drent R, Kersten M, Van der Meer J, Wiersma P (1996) Variability in basal metabolic rate of a long-distance migrant shorebird (red knot Calidris canutus) reflects shifts in organ size. Physiol Zool 69:191–217

    Google Scholar 

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

    Article  Google Scholar 

  • Rezende EL, Chappell MA, Hammond KA (2004b) Cold-acclimation in Peromyscus: temporal effects and individual variation in maximum metabolism and ventilatory rates. J Exp Biol 207:295–305

    Article  Google Scholar 

  • Rodriquez-Duran A (1995) Metabolic rates and thermal conductance in four species of neotropical bats roosting in hot caves. Comp Biochem Physiol 110A:347–355

    Article  CAS  Google Scholar 

  • Rønning B, Moe B, Bech C (2005) Long-term repeatability makes basal metabolic rate a likely heritable trait in the zebra finch Taeniopygia guttata. J Exp Biol 208:4663–4669

    Article  PubMed  Google Scholar 

  • Rose RW, West AK, Ye JM, McCormack GH, Colquhoun EQ (1999) Nonshivering thermogenesis in a marsupial, the Tasmanian bettong (Bettongia gaimardi) is not attributable to brown adipose tissue. Physiol Biochem Zool 72:699–704

    Article  PubMed  CAS  Google Scholar 

  • Schaeffer PJ, Villarin JJ, Lindstedt SL (2003) Chronic cold exposure increases skeletal muscle oxidative structure and function in Monodelphis domestica, a marsupial lacking brown adipose tissue. Physiol Biochem Zool 76:877–887

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Nielsen K (1985) Scaling why is animal size so important? Cambridge University Press, Cambridge

    Google Scholar 

  • Selman C, Lumsden S, Bunger 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

    PubMed  CAS  Google Scholar 

  • Speakman JR, Johnson MS (2000) Relationships between resting metabolic rate and morphology in lactating mice: what tissues are the major contributors to resting metabolism? In: Heldmaier G, Klingenspor M (eds) Life in the cold: eleventh international hibernation symposium. Springer, Berlin Heidelberg New York, pp 479–486

    Google Scholar 

  • Speakman JR, McQueenie J (1996) Limits to sustained metabolic rate: the link between food intake, basal metabolic rate, and morphology in reproducing mice, Mus musculus. Physiol Zool 69:746–769

    Google Scholar 

  • Spicer JI, Gaston KJ (1999) Physiological diversity and its ecological implications. Blackwell Sciences, Oxford

    Google Scholar 

  • Storey JD (2003) The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Stat 31:2013–2035

    Article  Google Scholar 

  • Swift RW, Forbes RM (1939) The heat production of the fasting rat in relation to environmental temperature. J Nutr 18:307–318

    CAS  Google Scholar 

  • Szewczak J (1998) Hypoxic hypometabolism in heterothermic mammals. Am Zool 38:9A

    Google Scholar 

  • Tolley EA, Notter DR, Marlowe TJ (1983) Heritability and repeatability of speed of 2- and 3-year old standardbred racehorses. J Anim Sci 56:1295–1305

    Google Scholar 

  • Van Berkum FH, Huey RB, Tsuji JS, Garland T (1989) Repeatability of differences in locomotor performance and body size during early ontogeny of the lizard, Sceloporus occidentalis (Baird and Girard). Funct Ecol 3:97–105

    Article  Google Scholar 

  • Vezina F, Williams TD (2005) The metabolic cost of egg production is repeatable. J Exp Biol 208:2533–2538

    Article  PubMed  Google Scholar 

  • Weber TP, Piersma T (1996) Basal metabolic rate and the mass of tissues differing in metabolic scope: migration-related covariation between individual knots Calidris canutus. J Avian Biol 27:215–224

    Google Scholar 

  • White CR, Seymour RS (2004) Does basal metabolic rate contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological, and life-history variables. Physiol Biochem Zool 77:929–941

    Article  PubMed  Google Scholar 

  • Williams JB, Tieleman BI (2000) Flexibility in basal metabolic rate and evaporative water loss among Hoopoe Larks exposed to different environmental temperatures. J Exp Biol 203:3153–3159

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Jack Hayes provided the initial cohort of deer mice to establish our captive colony, which is supported by National Science Foundation grant # IBN-0073229 to Kimberly A. Hammond and M.A. Chappell. The staff at the Barcroft Laboratory of the WMRS provided indispensable help and hospitality during our stays and while the HB mice were under their care. Husbandry at WMRS was supported in part by a WMRS minigrant to G.A. Russell. Finally, we thank E. Hice and J. Urrutia in the UCR Biology machine shop for constructing the metabolism chambers and environmental cabinet. All of the experiments and methods listed in this paper comply with the laws of the country in which they were performed.

Author information

Authors and Affiliations

  1. Department of Biology, University of California, Riverside, CA, 92521, USA

    G. A. Russell & M. A. Chappell

Authors
  1. G. A. Russell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Chappell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. A. Russell.

Additional information

Communicated by G. Heldmaier

Rights and permissions

Reprints and permissions

About this article

Cite this article

Russell, G.A., Chappell, M.A. Is BMR repeatable in deer mice? Organ mass correlates and the effects of cold acclimation and natal altitude. J Comp Physiol B 177, 75–87 (2007). https://doi.org/10.1007/s00360-006-0110-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-006-0110-y

Keywords

Search

Navigation