Gait-specific energetics contributes to economical walking and running in emus and ostriches
Open accessAbstract
A widely held assumption is that metabolic rate (Ėmet) during legged locomotion is linked to the mechanics of different gaits and this linkage helps explain the preferred speeds of animals in nature. However, despite several prominent exceptions,Ėmet of walking and running vertebrates has been nearly uniformly characterized as increasing linearly with speed across all gaits. This description of locomotor energetics does not predict energetically optimal speeds for minimal cost of transport (Ecot). We tested whether large bipedal ratite birds (emus and ostriches) have gait-specific energetics during walking and running similar to those found in humans. We found that during locomotion, emus showed a curvilinear relationship between Ėmet and speed during walking, and both emus and ostriches demonstrated an abrupt change in the slope of Ėmet versus speed at the gait transition with a linear increase during running. Similar to human locomotion, the minimum net Ecot calculated after subtracting resting metabolism was lower in walking than in running in both species. However, the difference in net Ecot between walking and running was less than is found in humans because of a greater change in the slope of Ėmet versus speed at the gait transition, which lowers the cost of running for the avian bipeds. For emus, we also show that animals moving freely overground avoid a range of speeds surrounding the gait-transition speed within which the Ecot is large. These data suggest that deviations from a linear relation of metabolic rate and speed and variations in transport costs with speed are more widespread than is often assumed, and provide new evidence that locomotor energetics influences the choice of speed in bipedal animals. The low cost of transport for walking is probably ecologically important for emus and ostriches because they spend the majority of their active day walking, and thus the energy used for locomotion is a large part of their daily energy budget.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A U-shaped curve during walking locomotion has also been observed in another large cursorial bird, the emu (Dromaius novaehollandiae), and field observations revealed that the self-selected speeds preferred by emu were tightly clustered around the lowest point of the curve in line with predictions they chose this speed to minimize the CoT.
“A U-shaped curve during walking locomotion has also been observed in another large cursorial bird, the emu (Dromaius novaehollandiae), and field observations revealed that the self-selected speeds preferred by emu were tightly clustered around the lowest point of the curve in line with predictions they chose this speed to minimize the CoT34.”
From The peacock train does not handicap cursorial locomotor performance (2016) · cites this paper as [34]
The curvilinear relationship between metabolic power consumption (Pmet) and speed (U) during walking in peacocks is also seen in other animals including some species of large bird, but deviates from the more common linear relationship found in many species.
“the relationship between metabolic power consumption (Pmet) and speed (U) for walking during both experimental periods was curvilinear, which is also seen in other animals including some species of large bird”
From The peacock train does not handicap cursorial locomotor performance (2016) · cites this paper as [34]
Cites
Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure
Cavagna, G., Heglund, N. C., & Taylor, C. R. (1977) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1977.233.5.r243 · Cited by 1,425 · see citing works
Gait and the energetics of locomotion in horses
Hoyt, D. F., & Taylor, C. R. (1981) · Nature · doi:10.1038/292239a0 · Cited by 1,072 · see citing works
Self-citationMeasurement of VO2, VCO2, and evaporative water loss with a flow-through mask
Withers, P. C. (1977) · Journal of Applied Physiology · doi:10.1152/jappl.1977.42.1.120 · Cited by 874 · see citing works
Energetics of running: a new perspective
Kram, R., & Taylor, C. R. (1990) · Nature · doi:10.1038/346265a0 · Cited by 821 · see citing works
Optimization and gaits in the locomotion of vertebrates
Alexander, R. M. (1989) · Physiological Reviews · doi:10.1152/physrev.1989.69.4.1199 · Cited by 709 · see citing works
Margaria, R., Cerretelli, P., Aghemo, P., & Sassi, G. (1963) · Journal of Applied Physiology · doi:10.1152/jappl.1963.18.2.367 · Cited by 666 · see citing works
Taylor, C. R., Heglund, N. C., & Maloiy, G. M. O. (1982) · Journal of Experimental Biology · doi:10.1242/jeb.97.1.1 · Cited by 650 · see citing works
Scaling of energetic cost of running to body size in mammals
Taylor, C., Schmidt‐Nielsen, K., & Raab, J. (1970) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1970.219.4.1104 · Cited by 600 · see citing works
Energy expenditures for locomotion by mule deer and elk.
Parker, K. L., Robbins, C. T., & Hanley, T. A. (1984) · The Journal of Wildlife Management · doi:10.2307/3801180 · Cited by 577 · see citing works
Biomechanical and physiological aspects of legged locomotion in humans
Saibene, F., & Minetti, A. E. (2003) · European Journal of Applied Physiology · doi:10.1007/s00421-002-0654-9 · Cited by 437 · see citing works
Energetic Cost of Locomotion in Kangaroos
Dawson, T. J., & Taylor, C. R. (1973) · Nature · doi:10.1038/246313a0 · Cited by 435 · see citing works
Energetics of Bipedal Running: I. Metabolic Cost of Generating Force
Roberts, T. J., Kram, R., Weyand, P. G., & Taylor, C. R. (1998) · Journal of Experimental Biology · doi:10.1242/jeb.201.19.2745 · Cited by 293 · see citing works
On the Running of the GNU (Connochaetes Taurinus) and other Animals
Pennycuick, C. J. (1976) · Journal of Experimental Biology · doi:10.1242/jeb.63.3.775 · Cited by 218 · see citing works
Effective limb length and the scaling of locomotor cost in terrestrial animals
Pontzer, H. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.002246 · Cited by 189 · see citing works
Rubenson, J., Heliams, D. B., Lloyd, D. G., & Fournier, P. A. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2702 · Cited by 184 · see citing works
Self-citationEnergy expenditures for locomotion by barren-ground caribou
Fancy, S. G., & White, R. G. (1987) · Canadian Journal of Zoology · doi:10.1139/z87-018 · Cited by 166 · see citing works
Field Metabolism, Water Requirements, and Foraging Behavior of Wild Ostriches in the Namib
Williams, J. B., Siegfried, W. R., Milton, S. J., et al. (1993) · Ecology · doi:10.2307/1939301 · Cited by 162 · see citing works
Relating mechanics and energetics during exercise.
Cr, T. (1994) · PubMed · Cited by 158 · see citing works
Fedak, M. A., & Seeherman, H. J. (1979) · Nature · doi:10.1038/282713a0 · Cited by 146 · see citing works
Biomechanical and energetic determinants of the walk–trot transition in horses
Griffin, T. M., Kram, R., Wickler, S. J., & Hoyt, D. F. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.01277 · Cited by 146 · see citing works
Self-citationOxygen Consumption and Respiratory Evaporation of the Emu and Rhea
Crawford, E. C., & Lasiewski, R. C. (1968) · Ornithological Applications · doi:10.2307/1365927 · Cited by 143 · see citing works
Energy cost of bipedal running
Fedak, M. A., Pinshow, B., & Schmidt‐Nielsen, K. (1974) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1974.227.5.1038 · Cited by 126 · see citing works
Optimal running speed and the evolution of hominin hunting strategies
Steudel‐Numbers, K., & Wall‐Scheffler, C. M. (2009) · Journal of Human Evolution · doi:10.1016/j.jhevol.2008.11.002 · Cited by 124 · see citing works
Rubenson, J., Lloyd, D. G., Heliams, D. B., Besier, T. F., & Fournier, P. A. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2010.0466 · Cited by 113 · see citing works
Self-citationMoving Cheaply: Energetics of Walking in the African Elephant
Langman, V. A., Roberts, T. J., Black, J. D., Maloiy, G. M. O., Heglund, N. C., Weber, J., Kram, R., & Taylor, C. R. (1995) · Journal of Experimental Biology · doi:10.1242/jeb.198.3.629 · Cited by 110 · see citing works
(2001) · Choice Reviews Online · doi:10.5860/choice.38-4519 · Cited by 101 · see citing works
Preferred Speeds in Terrestrial Vertebrates: Are They Equivalent?
Perry, A. K., Blickhan, R., Biewener, A. A., Heglund, N. C., & Taylor, C. R. (1988) · Journal of Experimental Biology · doi:10.1242/jeb.137.1.207 · Cited by 97 · see citing works
Energetic cost of running and heat balance in a large bird, the rhea
Taylor, C., Dmi’el, R., Fedak, M. A., & Schmidt‐Nielsen, K. (1971) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1971.221.2.597 · Cited by 79 · see citing works
Williams, T. M. (1983) · Journal of Experimental Biology · doi:10.1242/jeb.105.1.283 · Cited by 77 · see citing works
Reappraisal of the comparative cost of human locomotion using gait-specific allometric analyses.
Rubenson, J., Heliams, D. B., Maloney, S. K., Withers, P. C., Lloyd, D. G., & Fournier, P. A. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.000992 · Cited by 76 · see citing works
Self-citationBiomechanics of Running Indicates Endothermy in Bipedal Dinosaurs
Pontzer, H., Allen, V. R., & Hutchinson, J. R. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007783 · Cited by 73 · see citing works
Energetic cost of locomotion in the tammar wallaby
Baudinette, R. V., Snyder, G. K., & Frappell, P. B. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.262.5.r771 · Cited by 70 · see citing works
Effect of load on preferred speed and cost of transport
Wickler, S. J., Hoyt, D. F., Cogger, E. A., et al. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.4.1548 · Cited by 60 · see citing works
Self-citationSeasonal Variation in Daily Activity Patterns, Water Relations and Diet of Emus
Dawson, T. J., Read, D., RUSSELL, E. M., et al. (1984) · Emu - Austral Ornithology · doi:10.1071/mu9840093 · Cited by 46 · see citing works
Hoyt, D. F., & Kenagy, G. J. (1988) · Physiological Zoology · doi:10.1086/physzool.61.1.30163734 · Cited by 45 · see citing works
Self-citationWhat are the relations between mechanics, gait parameters, and energetics in terrestrial locomotion?
Hoyt, D. F., Wickler, S. J., Dutto, D. J., Catterfeld, G. E., & Johnsen, D. (2006) · Journal of Experimental Zoology Part A Comparative Experimental Biology · doi:10.1002/jez.a.335 · Cited by 41 · see citing works
Self-citationTriggers for the transition between human walking and running.
Hanna, A., Abernethy, A. B., Neal, R. J., et al. (2000) · Cited by 29 · see citing works
Overground vs. treadmill walk-to-run transition
Caekenberghe, I. V., Smet, K. D., Segers, V., et al. (2010) · Gait & Posture · doi:10.1016/j.gaitpost.2010.01.011 · Cited by 26 · see citing works
Comparative vertebrate exercise physiology : unifying physiological principles
Jones, J. H. (1994) · Academic Press eBooks · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ijspeert, A. J., & Daley, M. A. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.245784 · Cited by 79 · see citing works
The peacock train does not handicap cursorial locomotor performance
Thavarajah, N. K., Tickle, P. G., Nudds, R. L., & Codd, J. R. (2016) · Scientific Reports · doi:10.1038/srep36512 · Cited by 25 · see citing works
- Authors
- Watson, R. R., Rubenson, J., Coder, L., Hoyt, D. F., Propert, M. W. G., & Marsh, R. L.
- Affiliations
- California State Polytechnic University (US)
- The University of Western Australia (AU)
- Northeastern University (US)
- Corresponding author
- Marsh, Richard L.
- Venue
- Proceedings of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2010-12
- Volume
- 278
- Issue
- 1714
- Pages
- 2040-2046
- ISSN
- 0080-4649 (ISSN-L)
- 0962-8452
- 1471-2954
- PMC
- PMC3107644
- OpenAlex
- W2123151273
- Cited by
- 70
- References
- 39
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 4 · 2019: 2 · 2018: 4 · 2017: 16 · 2016: 11 · 2015: 8 · 2014: 3 · 2013: 3 · 2012: 1
- FWCI
- 1.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- Funders
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR 47337, R01AR047337)
- Topics
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Physical Sciences › Engineering › Biomedical Engineering › Robotic Locomotion and Control
- Physical Sciences › Environmental Science › Ecology › Avian ecology and behavior
- Keywords
- locomotion energetics, cost of transport, metabolic rate, walking, running, gait transition, emu, ostrich, bipedalism, speed choice, overground locomotion
- MeSH terms
- Animals, California, Energy Metabolism, Female, Gait, Male, Running, Walking, Struthioniformes, Dromaiidae
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review