Skip to main content
Log in

Quadrupedal locomotor performance in two species of arboreal squirrels: predicting energy savings of gliding

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

Abstract

Gliding allows mammals to exploit canopy habitats of old-growth forests possibly as a means to save energy. To assess costs of quadrupedal locomotion for a gliding arboreal mammal, we used open-flow respirometry and a variable-speed treadmill to measure oxygen consumption and to calculate cost of transport, excess exercise oxygen consumption, and excess post-exercise oxygen consumption for nine northern flying squirrels (Glaucomys sabrinus) and four fox squirrels (Sciurus niger). Our results indicate that oxygen consumption during exercise by flying squirrels was 1.26–1.65 times higher than predicted based on body mass, and exponentially increased with velocity (from 0.84 ± 0.03 ml O2 kg−1 s−1 at 0.40 m s−1 to 1.55 ± 0.03 ml O2 kg−1 s−1 at 0.67 m s−1). Also, cost of transport in flying squirrels increased with velocity, although excess exercise oxygen consumption and excess post-exercise oxygen consumption did not. In contrast, oxygen consumption during exercise for fox squirrels was similar to predicted, varying from 0.51 (±0.02) ml O2 kg−1 s−1 at 0.63 m s−1 to 0.54 (±0.03) ml O2 kg−1 s−1 at 1.25 m s−1. In addition, the cost of transport for fox squirrels decreased with velocity, while excess exercise oxygen consumption and excess post-exercise oxygen consumption did not. Collectively, these observations suggest that unlike fox squirrels, flying squirrels are poorly adapted to prolonged bouts of quadrupedal locomotion. The evolution of skeletal adaptations to climbing, leaping, and landing and the development of a gliding membrane likely has increased the cost of quadrupedal locomotion by >50% while resulting in energy savings during gliding and reduction in travel time between foraging patches.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

COT:

Cost of transport

EEOC:

Excess exercise oxygen consumption

EPOC:

Excess post-exercise oxygen consumption

M b :

Body mass

RMR:

Resting metabolic rate

v g :

Speed

\( \dot{V}_{{O_{2} }} \) :

Rate of oxygen consumption

References

  • Abrams PA (1984) Foraging time optimization and interactions in food webs. Am Nat 124:80–96

    Article  Google Scholar 

  • Adler FR, Kotar M (1999) Departure time versus departure rate: how to forage optimally when you are stupid. Evol Ecol Res 1:411–421

    Google Scholar 

  • Alexander RMcN (1968) Animal mechanics. Sidgwick and Jackson, London

    Google Scholar 

  • Animal Care and Use Committee (1998) Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. J Mammal 79:1416–1431

    Article  Google Scholar 

  • Baker EJ, Gleeson TT (1998) EPOC and the energetics of brief locomotor activity in Mus domesticus. J Exp Biol 280:114–120

    CAS  Google Scholar 

  • Baker EJ, Gleeson TT (1999) The effects of intensity on the energetics of brief locomotor activity. J Exp Biol 202:3081–3087

    CAS  PubMed  Google Scholar 

  • Ben-David M, Williams TM, Ormseth OA (2000) Effects of oiling on exercise physiology and diving behavior of river otters: a captive study. Can J Zool 78:1380–1390

    Article  Google Scholar 

  • Biewener AA (2003) Animal locomotion. Oxford University Press, Oxford

    Google Scholar 

  • Blaxter K (1989) Energy metabolism in animals and man. Cambridge University Press, Cambridge

    Google Scholar 

  • Carey AB (1995) Sciurids in Pacific Northwest managed and old-growth forests. Ecol Appl 5:648–661

    Article  Google Scholar 

  • Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9:129–136

    Article  CAS  PubMed  Google Scholar 

  • Dial R (2003) Energetic savings and the body size distributions of gliding mammals. Evol Ecol Res 5:1151–1162

    Google Scholar 

  • Dudley R, Byrnes G, Yanoviak SP, Borrell B, Brown RM, McGuire JA (2007) Gliding and the functional origins of flight: biomechanical novelty or necessity? Annu Rev Ecol Evol Syst 38:179–201

    Article  Google Scholar 

  • Emmons LH, Gentry AH (1983) Tropical forest structure and the distribution of gliding prehensile-tail vertebrates. Am Nat 121:513–524

    Article  Google Scholar 

  • Essner RL (2008) Morphology, locomotor behavior and microhabitat use in North American squirrels. J Zool 272:101–109

    Article  Google Scholar 

  • Essner RL, Scheibe JS (2000) A comparison of scapular shape in flying squirrels (Rodentia: Sciuridae) using relative warp analysis. In: Goldingay R, Scheibe J (eds) Biology of gliding mammals. Filander Press, Furth, pp 135–148

    Google Scholar 

  • Fedak MA, Rome L, Seeherman HJ (1981) One-step N2 dilution technique for calibrating open-circuit O2 measuring systems. J Appl Physiol 51:772–776

    CAS  PubMed  Google Scholar 

  • Fish FE, Baudinette RV (1999) Energetics of locomotion by the Australian water rat (Hydromys chrysogaster): a comparison of swimming and running in a semi-aquatic mammal. J Exp Biol 202:353–363

    CAS  PubMed  Google Scholar 

  • Flaherty EA, Smith WP, Pyare S, Ben-David M (2008) Experimental trials of the northern flying squirrel (Glaucomys sabrinus) traversing managed rainforest landscapes: perceptual range and fine-scale movements. Can J Zool 86:1050–1058

    Article  Google Scholar 

  • Flaherty EA, Ben-David M, Smith WP (2010) Diet and food availability of the endemic Prince of Wales flying squirrel (Glaucomys sabrinus griseifrons) in Southeast Alaska: implications for dispersal across managed landscapes. J Mammal 91:79–91

    Article  Google Scholar 

  • Fournier RA, Weber JM (1994) Locomotory energetics and metabolic fuel reserves of the Virginia opossum. J Exp Biol 197:1–16

    CAS  PubMed  Google Scholar 

  • Gaesser GA, Brooks GA (1984) Metabolic bases of excess post-exercise oxygen consumption: a review. Med Sci Sports Exerc 16:29–43

    CAS  PubMed  Google Scholar 

  • Garland T, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828

    Google Scholar 

  • Geiser F, Stapp P (2000) Energetics and thermal biology of gliding mammals. In: Goldingay R, Scheibe J (eds) Biology of gliding mammals. Filander Press, Furth, pp 149–166

    Google Scholar 

  • Gleeson TT (1996) Post-exercise lactate metabolism: a comparative review of sites, pathways, and regulation. Ann Rev Phys 58:565–581

    Article  CAS  Google Scholar 

  • Gleeson TT, Hancock TV (2002) Metabolic implications of a ‘run now, pay later’ strategy in lizards: an analysis of post-exercise oxygen consumption. Comp Biochem Physiol A 133:259–267

    Article  Google Scholar 

  • Goldingay RL (2000) Gliding mammals of the world: diversity and ecological requirements. In: Goldingay R, Scheibe J (eds) Biology of gliding mammals. Filander Press, Furth, pp 135–148

    Google Scholar 

  • Kilpatrick AM (2003) The impact of thermoregulatory costs on foraging behaviour: a test with American Crows (Corvus brachyrhynchos) and eastern grey squirrels (Sciurus carolinensis). Evol Ecol Res 5:781–786

    Google Scholar 

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

    CAS  Google Scholar 

  • Koprowski JL (1994) Sciurus niger. Mammal Species 479:1–9

    Google Scholar 

  • Kramer DL, McLaughlin RL (2001) The behavioral ecology of intermittent locomotion. Am Zool 41:137–153

    Article  Google Scholar 

  • Mace GM, Harvey PH (1983) Energetic constraints on home-range size in mammals. Ecology 67:120–132

    Google Scholar 

  • McAdam AG, Kramer DL (1998) Vigilance as a benefit of intermittent locomotion in small mammals. Anim Behav 55:109–117

    Article  PubMed  Google Scholar 

  • Mowrey RA, Zasada JC (1982) Den tree use and movements of northern flying squirrels in interior Alaska and implications for forest management. In: Meehan WR, Merrell TR Jr, Hanley TA (eds) Fish and wildlife relationships in old growth forests. Bookmasters, Ohio, pp 351–356

    Google Scholar 

  • Neter JM, Kutner H, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models. Irwin, Chicago

    Google Scholar 

  • Norberg RA (1977) An ecological theory on foraging time and energetics and choice of optimal food-searching method. J Anim Ecol 46:511–529

    Article  Google Scholar 

  • Norberg UM (1985) Evolution of vertebrate flight: an aerodynamic model for the transition from gliding to active flight. Am Nat 126:303–327

    Article  Google Scholar 

  • Nupp TE, Swihart RK (2000) Landscape-level correlates of small-mammal assemblages in forest fragments of farmland. J Mammal 81:512–526

    Article  Google Scholar 

  • Paskins KE, Bowyer A, Megill WM, Scheibe JS (2007) Take-off and landing forces and the evolution of controlled gliding in northern flying squirrels Glaucomys sabrinus. J Exp Biol 210:1413–1423

    Article  PubMed  Google Scholar 

  • Peterka HE (1936) A study of the mycology and osteology of tree sciurids with regard to adaptation to arboreal, glissant, and fossorial habits. Trans Kans Acad Sci 39:313–332

    Article  Google Scholar 

  • Pyare S, Longland WS (2001) Mechanisms of truffle detection by northern flying squirrels. Can J Zool 79:1007–1015

    Article  Google Scholar 

  • Rosenblatt DL, Heske EJ, Nelson SL, Barber DM, Miller MA, MacAllister B (1999) Forest fragments in east-central Illinois: islands or habitat patches for mammals? Am Midl Nat 141:115–123

    Article  Google Scholar 

  • Scheibe JS, Essner RL (2000) Pelvic shape in gliding rodents: implications for the launch. In: Goldingay R, Scheibe J (eds) Biology of gliding mammals. Filander Press, Furth, pp 135–148

    Google Scholar 

  • Scheibe JS, Robbins JH (1998) Morphological and performance attributes of gliding mammals. In: Steele MA, Merritt JF, Zegers DA (eds) Ecology and evolutionary biology of tree squirrels. Special publication of the Virginia Museum of Natural History 6:131–144

  • Scheibe JS, Smith WP, Bassham J, Magness D (2006) Locomotor performance and cost of transport in the northern flying squirrel Glaucomys sabrinus. Acta Theriol 51:169–178

    Google Scholar 

  • Scheibe JS, Paskins KE, Ferdous S, Birdsill D (2007) Kinematics and functional morphology of leaping, landing, and branch use in Glaucomys sabrinus. J Mammal 88:850–861

    Article  Google Scholar 

  • Scholey K (1986) The climbing and gliding locomotion of the giant red flying squirrel Petaurista petaurista (Sciuridae). In: Nachtigall W (ed) Bat Flight-Fledermausflug Biona-report 5. Gustav-Fischer Verlag, Stuttgart, pp 187–204

    Google Scholar 

  • Selonen V, Hanski IK (2003) Movements of the flying squirrels Pteromys volans in corridors and in matrix habitat. Ecography 26:641–651

    Article  Google Scholar 

  • Selonen V, Hanski IK (2004) Young flying squirrels (Pteromys volans) dispersing in fragmented landscapes. Behav Ecol 15:564–571

    Article  Google Scholar 

  • Smith WP, Nichols JV (2003) Demography of the Prince of Wales flying squirrel (Glaucomys sabrinus griseifrons): an endemic of southeastern Alaska temperate rain forest. J Mammal 84:144–158

    Article  Google Scholar 

  • Steele MA (1998) Tamiasciurus hudsonicus. Mammal Species 586:1–9

    Article  Google Scholar 

  • Strahan R (1998) The mammals of Australia, Revised 2nd ed. New Holland publishers, Sydney

    Google Scholar 

  • Swihart RN, Slade NA, Bergstrom BJ (1988) Relating body size to the rate of home range use in mammals. Ecology 69:393–399

    Article  Google Scholar 

  • Taylor CR, Caldwell SL, Rowntree VJ (1972) Running up and down hills: some consequences of size. Science 178:1096–1097

    Article  CAS  PubMed  Google Scholar 

  • Taylor CR, Heglund NC, Maloiy GMO (1982) Energetics and mechanics of terrestrial locomotion I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J Exp Biol 97:1–21

    CAS  PubMed  Google Scholar 

  • Thorington RW, Heaney LR (1981) Body proportions and gliding adaptations of flying squirrels. J Mammal 62:101–114

    Article  Google Scholar 

  • Tucker VA (1970) The energetic cost of locomotion in animals. Comp Biochem Physiol 34:841–846

    Article  CAS  PubMed  Google Scholar 

  • Vernes K (2001) Gliding performance of the northern flying squirrel (Glaucomys sabrinus) in mature mixed forests of eastern Canada. J Mammal 82:1026–1033

    Article  Google Scholar 

  • Volz K (1986) Habitat requirements of northern flying squirrels in west-central Oregon. M.S. thesis, Washington State University, Pullman, WA, USA

  • Ward S, Bishop CM, Woakes AJ, Butler PJ (2002) Heart rate and the rate of oxygen consumption of flying and walking barnacle geese (Branta leucopsis) and bar-headed geese (Anser indicus). J Exp Biol 205:3347–3356

    CAS  PubMed  Google Scholar 

  • Williams TM (1983) Locomotion in the North American mink, a semi-aquatic mammal II. The effect of an elongate body on running energetics and gait patterns. J Exp Biol 105:283–295

    CAS  PubMed  Google Scholar 

  • Williams TM, Ben-David M, Noren S, Rutishauser M, McDonald K (2002) Running energetics of the North American river otter: do short legs necessarily reduce efficiency on land? Comp Biochem Physiol A 133:203–212

    Article  Google Scholar 

  • Withers PC (1977) Measurements of \( \dot{V}_{{{\text{O}}_{2} }} \), \( \dot{V}_{{{\text{CO}}_{2} }} \), and evaporative water loss with a flow through mask. J Appl Physiol 42:120-123

  • Woodworth CJ, Bollinger EK, Nelson TA (2000) The effects of forest fragmentation size, isolation, and microhabitat variables on nest box use by southern flying squirrels (Glaucomys volans) in southern Illinois. In: Goldingay R, Scheibe J (eds) Biology of gliding mammals. Filander Press, Furth, pp 135–148

    Google Scholar 

  • Wunder BA, Morrison PA (1974) Red squirrel metabolism during incline running. Comp Biochem Physiol 48A:153–161

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, New Jersey

    Google Scholar 

  • Zollner PA (2000) Comparing the landscape level perceptual abilities of forest sciurids in fragmented agricultural landscape. Landscape Ecol 15:523–533

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank R. Carroll for his assistance caring for the captive squirrels. Sable Systems, Inc. answered many questions and provided assistance with our respirometry equipment. Drs. H. J. Harlow, C. Martinez del Rio, and T. M. Williams provided helpful insights in the early planning stages of this project. We thank S. W. Buskirk, R. L. Essner, Jr., G. Hayward, S. Miller, T. M. Williams and two anonymous reviewers for helpful comments on earlier drafts of the manuscript. Funding for this work was provided by the United States Fish and Wildlife Service, United States Forest Service, and the University of Wyoming.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elizabeth A. Flaherty.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Flaherty, E.A., Ben-David, M. & Smith, W.P. Quadrupedal locomotor performance in two species of arboreal squirrels: predicting energy savings of gliding. J Comp Physiol B 180, 1067–1078 (2010). https://doi.org/10.1007/s00360-010-0470-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-010-0470-1

Keywords

Navigation