Hummingbird flight: Sustaining the highest mass-specific metabolic rates among vertebrates
Abstract
Resting and maximal mass-specific metabolic rates scale inversely with body mass. Small hummingbirds achieve the highest known mass-specific metabolic rates among vertebrate homeotherms. Maximal capacities for O2 and substrate delivery to muscle mitochondria, as well as mitochondrial oxidative capacities in these animals may be at the upper limits of what are structurally and functionally possible given the constraints inherent in vertebrate design. Such constraints on the evolutionary design of functional capacities may play an important role in determining the lower limits to vertebrate homeotherm size and the upper limits to mass-specific metabolic rate.
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Hummingbird flight requires the highest mass-specific oxygen consumption of any vertebrate locomotor mode.
“Hummingbird flight requires the highest massspecific oxygen consumption of any vertebrate locomotor mode (Suarez, 1992), but these birds nevertheless inhabit high elevations throughout the New World (Schuchmann, 1999), with some taxa residing up to 5000 m (Carpenter, 1976;Rahbek and Graves, 2000).”
From The physiology and biomechanics of avian flight at high altitude (2006) · cites this paper as Suarez, 1992
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“Moreover, the high metabolic rate of hummingbirds (Suarez, 1992) makes them relentless foragers in a broad range of outdoor weather conditions, requiring them to utilize a variety of flight control strategies to contend with the airflow conditions they encounter in natural habitats.”
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Gregory, T. R., Andrews, C. B., McGuire, J. A., & Witt, C. C. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.1004 · Cited by 51 · see citing works
“Hummingbirds correspondingly possess the highest relative heart volumes, lung volumes, mitochondrial volume densities, mitochondrial respiration rates and capillary volume densities compared with any vertebrates (Suarez et al. 1991; Suarez 1992).”
BackgroundAdipose energy stores, physical work, and the metabolic syndrome: lessons from hummingbirds
Hargrove, J. L. (2005) · Nutrition Journal · doi:10.1186/1475-2891-4-36 · Cited by 50 · see citing works
“Adding 2 g of water of hydration for each g of glycogen, the birds would have to increase their body weight to above 10 g! The flight is possible only because the energy yield per gram of fat is 10 fold higher than for hydrated glycogen [19].”
BackgroundFalk, J. J., Webster, M. S., & Rubenstein, D. R. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.043 · Cited by 50 · see citing works
Spaargaren, D. H. (1994) · Acta Biotheoretica · doi:10.1007/bf00707392 · Cited by 50 · see citing works
McWilliams, S. R., & Karasov, W. H. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.0308 · Cited by 48 · see citing works
Energetics of hummingbird foraging at low ambient temperature
Gass, C. L., Romich, M. T., & Suarez, R. K. (1999) · Canadian Journal of Zoology · doi:10.1139/cjz-77-2-314 · Cited by 46 · see citing works
Self-citationGaleotti, P., Sacchi, R., Fasola, M., Pellitteri‐Rosa, D., Marchesi, M., & Ballasina, D. (2005) · Canadian Journal of Zoology · doi:10.1139/z05-130 · Cited by 44 · see citing works
Animal Flight Mechanics in Physically Variable Gas Mixtures
Dudley, R., & Chai, P. (1996) · Journal of Experimental Biology · doi:10.1242/jeb.199.9.1881 · Cited by 44 · see citing works
Quantifying the dynamic wing morphing of hovering hummingbird
Maeda, M., Nakata, T., Kitamura, I., Tanaka, H., & Liu, H. (2017) · Royal Society Open Science · doi:10.1098/rsos.170307 · Cited by 43 · see citing works
Elements of episodic-like memory in free-living hummingbirds, energetic consequences
González‐Gómez, P. L., Bozinovic, F., & Vásquez, R. A. (2011) · Animal Behaviour · doi:10.1016/j.anbehav.2011.03.014 · Cited by 43 · see citing works
“In hummingbirds, foraging success is vital because of the extremely high mass specific rates of aerobic metabolism (Suarez 1992; Suarez & Gass 2002).”
Dietary protein level affects iridescent coloration in Anna's hummingbirds, Calypte anna
Meadows, M. G., Roudybush, T. E., & McGraw, K. J. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.069351 · Cited by 42 · see citing works
“Hummingbirds hover while hawking for protein-rich insects, and this is the most energetically expensive activity known among vertebrates (Suarez, 1992).”
BackgroundPeterson, C. C. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-021 · Cited by 49 · see citing works
Comparative skeletal muscle fibre morphometry among wild birds with different locomotor behaviour
Torrella, J. R., Fouces, V., Palomeque, J., & Viscor, G. (1998) · Journal of Anatomy · doi:10.1046/j.1469-7580.1998.19220211.x · Cited by 41 · see citing works
The sugar oxidation cascade: aerial refueling in hummingbirds and nectar bats
Suarez, R. K., M., L., & Welch, K. C. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.047936 · Cited by 45 · see citing works
“It is likely that, when in flight, 90% or more of their whole-body VO2 and VCO2 (rate of CO2 production) values are accounted for by flight muscles (Suarez, 1992; Taylor, 1987).”
Self-citationFat metabolism in exercise – with special reference to training and growth hormone administration
Lange, K. H. W. (2004) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2004.381.x · Cited by 39 · see citing works
“Among homeotherm vertebrates, small humming birds achieve the highest known rates of mass-specific aerobic metabolism of 670mLO2 kg 1 min 1, both during hovering and during forward flight (Suarez, 1992, 1998).”
BackgroundSugar Metabolism in Hummingbirds and Nectar Bats
Suarez, R. K., & Welch, K. C. (2017) · Nutrients · doi:10.3390/nu9070743 · Cited by 32 · see citing works
“Small hummingbirds in routine hovering flight display wingbeat frequencies of 30–60 Hz [21,22] and, in the process, sustain the highest mass-specific rates of aerobic metabolism among vertebrates that are about tenfold higher than the maximum rates measured in human athletes [2].”
BackgroundSelf-citationGans, C., Gaunt, A. S., & Webb, P. W. (1997) · Comprehensive physiology · doi:10.1002/cphy.cp130103 · Cited by 38 · see citing works
Integration of demand and supply sides in the ATP energy economics of cells
Nath, S. (2019) · Biophysical Chemistry · doi:10.1016/j.bpc.2019.106208 · Cited by 37 · see citing works
Suarez, R. K., Welch, K. C., Hanna, S. K., & M., L. G. H. (2009) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2009.01.015 · Cited by 37 · see citing works
“glucoseflux andhexokinase data arebasedon Suarez et al. (1990); CPTdata are fromTables 1”
BackgroundInfluentialSelf-citationHummingbirds can fuel expensive hovering flight completely with either exogenous glucose or fructose
Chen, C., & Welch, K. C. (2014) · Functional Ecology · doi:10.1111/1365-2435.12202 · Cited by 41 · see citing works
“When sustaining true hovering flight hummingbirds have some of the highest mass-specific metabolic rates among vertebrates (Suarez 1992).”
BackgroundDNA sequence diversity and the efficiency of natural selection in animal mitochondrial DNA
James, J., Castellano, D., & Eyre‐Walker, A. (2016) · Heredity · doi:10.1038/hdy.2016.108 · Cited by 35 · see citing works
Dynamic energy and time budgets in hummingbirds: a study in Sephanoides sephaniodes
López-Calleja, M. V., & Bozinovic, F. (2003) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(02)00263-5 · Cited by 35 · see citing works
“Considering that at low ambient temperatures, the energetic cost of thermoregulation at rest may increase to a significant fraction of the cost of flight (Marsh and Dawson, 1989; Chai et al., 1998), and that hovering birds display the highest known mass-specific metabolic rates among vertebrates ( Suarez, 1992 ), the…”
BackgroundThe integration of diet, physiology, and ecology of nectar-feeding birds
McWhorter, T. J., & López-Calleja, M. V. (2000) · Revista chilena de historia natural · doi:10.4067/s0716-078x2000000300008 · Cited by 35 · see citing works
Use of Metabolic Substrates in the Gray Treefrog Hyla versicolor. Implications for Calling Behavior
Grafe, T. U. (1997) · Copeia · doi:10.2307/1447755 · Cited by 34 · see citing works
Neuromuscular control of wingbeat kinematics in Anna's hummingbirds (Calypte anna)
Altshuler, D. L., Welch, K. C., Cho, B. H., Welch, D. B., Lin, A. F., Dickson, W. B., & Dickinson, M. H. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.043497 · Cited by 33 · see citing works
“The muscles that power hummingbird flight are composed exclusively of fast oxidative-glycolytic (FOG or IIA) fibers (Suarez, 1992; Welch and Altshuler, 2009).”
BackgroundBakken, B. H., McWhorter, T. J., Tsahar, E., & del Rio, C. M. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.01238 · Cited by 33 · see citing works
“Hummingbirds, because of their small body sizes (Dunning, 1992) and high mass-specific metabolisms (Suarez, 1992), are particularly challenged by this dilemma (Beuchat et al., 1990).”
BackgroundAraya‐Salas, M., González‐Gómez, P. L., Wojczulanis‐Jakubas, K., López, V., & Wright, T. F. (2018) · Scientific Reports · doi:10.1038/s41598-018-20441-x · Cited by 32 · see citing works
Integrating metabolic pathway fluxes with gene-to-enzyme expression rates
Hochachka, P. W., McClelland, G. B., Burness, G., Staples, J. F., & Suarez, R. K. (1998) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/s0305-0491(98)00019-4 · Cited by 32 · see citing works
Self-citationWelch, K. C., Allalou, A., Sehgal, P., Cheng, J., & Ashok, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077003 · Cited by 38 · see citing works
“While hovering at flowers, feeding on sugar-rich nectar, hummingbirds sustain some of the highest aerobic metabolic rates observed among vertebrates [1].”
BackgroundBandivadekar, R. R., Pandit, P., Sollmann, R., Thomas, M. J., Logan, S. M., Brown, J. C., Klimley, A. P., & Tell, L. A. (2018) · PLoS ONE · doi:10.1371/journal.pone.0208057 · Cited by 31 · see citing works
“Hummingbirds have the highest known metabolic rates among vertebrates and therefore require a high energy diet [5].”
BackgroundDolan, E., Saunders, B., Dantas, W. S., Murai, I. H., Roschel, H., Artioli, G. G., Harris, R. C., Bicudo, J. E. P. W., Sale, C., & Gualano, B. (2018) · Scientific Reports · doi:10.1038/s41598-018-32636-3 · Cited by 30 · see citing works
Hedges, C. P., Wilkinson, R. T., Devaux, J. B. L., & Hickey, A. J. (2019) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2019.01.002 · Cited by 29 · see citing works
Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds
Osipova, E., Barsacchi, R., Brown, T., Sadanandan, K. R., Gaede, A. H., Monte, A. A., Jarrells, J., Moebius, C., Pippel, M., Altshuler, D. L., et al. (2023) · Science · doi:10.1126/science.abn7050 · Cited by 29 · see citing works
“hovering flight is the most energy-demanding locomotion type and hummingbirds have the highest mass-specific metabolic rate measured for vertebrates (1, 2).”
BackgroundComparative Energetics of the Giant Hummingbird (Patagona gigas)
Fernández, M. J., Dudley, R., & Bozinovic, F. (2011) · Physiological and Biochemical Zoology · doi:10.1086/660084 · Cited by 29 · see citing works
The power of feeder-mask respirometry as a method for examining hummingbird energetics
Welch, K. C. (2010) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2010.07.014 · Cited by 29 · see citing works
“, 2004; Welch and Suarez, 2007), it's likely that the costs of imbibing nectar can be largely ignored (Suarez, 1992).”
Maina, J. N. (2022) · Frontiers in Animal Science · doi:10.3389/fanim.2022.851574 · Cited by 28 · see citing works
“…and physiological specializations (Maina, 2000b) that allow the body weight to be wholly supported by power generated by flapping light muscles (Suarez, 1992; Wells, 1993; Winter, 1998; Clark and Dudley, 2010); and the African rock martin is a small highly energetic passerine bird (Irwin,…”
BackgroundBuilding a mechanistic understanding of climate-driven elevational shifts in birds
Neate‐Clegg, M. H. C., & Tingley, M. W. (2023) · PLOS Climate · doi:10.1371/journal.pclm.0000174 · Cited by 27 · see citing works
Groom, D. J. E., de Toledo, M. C. B., Powers, D. R., Tobalske, B. W., & Welch, K. C. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.2011 · Cited by 24 · see citing works
The metabolic rate of the biosphere and its components
Hoehler, T. M., Mankel, D., Girguis, P. R., McCollom, T. M., Kiang, N. Y.-L., & Jørgensen, B. B. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2303764120 · Cited by 23 · see citing works
“For example, among animals with the highest known MSPs (e.g., hummingbirds), cardiac output and mitochondrial enzyme packing very likely constrain the absolute upper limit of aerobic respiration (25, 26).”
Oxygen efficient design of cephalopod muscle metabolism
Hochachka, P. W. (1995) · Marine and Freshwater Behaviour and Physiology · doi:10.1080/10236249409378908 · Cited by 24 · see citing works
Mahalingam, S., & Welch, K. C. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.089383 · Cited by 24 · see citing works
“The pectoralis and the supracoracoideus are both composed 541 exclusively of type IIa (fast twitch oxidative-glycolytic) fibers (Suarez, 1992; Welch and 542 Altshuler, 2009).”
BackgroundReiser, P. J., Welch, K. C., Suarez, R. K., & Altshuler, D. L. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.068825 · Cited by 23 · see citing works
“Hummingbirds can sustain aerobic metabolism at some of the highest rates observed in vertebrates when hovering under benign conditions and can substantially increase metabolism to meet greater power output demands during hovering under more taxing conditions, such as at high elevation or in reduced density gas mixture…”
BackgroundSelf-citationMorphological adaptations for relatively larger brains in hummingbird skulls
Ocampo, D., Barrantes, G., & Uy, J. A. C. (2018) · Ecology and Evolution · doi:10.1002/ece3.4513 · Cited by 23 · see citing works
“In addition, hummingbirds have the highest mass- specific metabolic rate among vertebrates, which likely represents the upper evolutionary metabolic limit (Suarez, 1992).”
BackgroundThermoregulatory cost affects territorial behavior in hummingbirds: a model and its application
González‐Gómez, P. L., Ricote, N., Razeto‐Barry, P., Cotorás, I. S., & Bozinovic, F. (2011) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-011-1222-2 · Cited by 22 · see citing works
“Moreover, hummingbird hovering is an energetically expensive flight style ( Suarez 1992 ), and the convective cooling it produces due to wing and air movements could further exacerbate energy drain (Chai et al. 1998).”
BackgroundDNA metabarcoding reveals broadly overlapping diets in three sympatric North American hummingbirds
Spence, A. R., Rankin, E. W. W., & Tingley, M. (2021) · Ornithology · doi:10.1093/ornithology/ukab074 · Cited by 19 · see citing works
“…E. E. Wilson Rankin, and M. W. Tingley Dietary overlap in North American hummingbirds families, instead of specializing on 1 or 2, ensures that hummingbirds can obtain enough nectar to fulfill their high metabolic needs from spatiotemporally variable resources (Powers and Nagy 1988, Suarez 1992).”
BackgroundVariable evidence for convergence in morphology and function across avian nectarivores
Hewes, A. E., Cuban, D., Groom, D. J. E., Sargent, A. J., Beltrán, D. F., & Rico‐Guevara, A. (2022) · Journal of Morphology · doi:10.1002/jmor.21513 · Cited by 21 · see citing works
“…that many factors play large roles in shaping bill morphology, including development (Bhullar et al., 2012), allometry (Bright et al., 2016), thermoregulation (Ryeland et al., 2017; Tattersall et al., 2017), and competition for mates (Rico‐Guevara & Araya‐ Salas, 2015; Rico‐Guevara & Hurme, 2019).”
BackgroundHummingbird blood traits track oxygen availability across space and time
Williamson, J. L., Linck, E. B., Bautista, E., Smiley, A., McGuire, J. A., Dudley, R., & Witt, C. C. (2023) · Ecology Letters · doi:10.1111/ele.14235 · Cited by 21 · see citing works
Oxygen, Homeostasis, and Metabolic Regulation
Hochachka, P. W. (2002) · Advances in experimental medicine and biology · doi:10.1007/0-306-46825-5_30 · Cited by 21 · see citing works
Sugar flux through the flight muscles of hovering vertebrate nectarivores: a review
Welch, K. C., & Chen, C. (2014) · Journal of Comparative Physiology □ B · doi:10.1007/s00360-014-0843-y · Cited by 20 · see citing works
Hovering Energetics and Thermal Balance in Anna’s Hummingbirds (Calypte anna)
Evangelista, D., Fernández, M. J., Berns, M. S., Hoover, A., & Dudley, R. (2010) · Physiological and Biochemical Zoology · doi:10.1086/651460 · Cited by 18 · see citing works
Hou, L., & Welch, K. C. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.08.019 · Cited by 18 · see citing works
“Hummingbirds have high mass-specific metabolic rates (Lasiewski, 1963; Suarez, 1992), high thermoregulatory costs due to their small size (Welch & Suarez, 2008), and must sustain high metabolic rates to power hovering and forward flight (Chai, 1997; Chen & Welch, 2014; Clark & Dudley, 2010; Suarez et al.”
Background
- Authors
- Suarez, R. K.
- Affiliations
- Simon Fraser University (CA)
- Corresponding author
- Suarez, R. K.
- ORCID
- Suarez, R. K.
- Venue
- Experientia
- Published
- 1992-06
- Volume
- 48
- Issue
- 6
- Pages
- 565-570
- ISSN
- 1420-682X (ISSN-L)
- 0014-4754
- 1420-9071
- OpenAlex
- W2075619721
- Cited by
- 193
- References
- 52
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 5 · 2023: 15 · 2022: 11 · 2021: 5 · 2020: 7 · 2019: 7 · 2018: 9 · 2017: 7 · 2016: 7 · 2015: 7 · 2014: 6 · 2013: 7 · 2012: 5
- FWCI
- 0.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cellular and Molecular Life Sciences (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- hummingbird flight, mass-specific metabolic rate, body mass scaling, homeotherms, mitochondrial oxidative capacity, muscle oxygen delivery, substrate supply, muscle mitochondria, flight energetics
- MeSH terms
- Animals, Birds, Energy Metabolism, Flight, Animal, Kinetics, Microscopy, Electron, Mitochondria, Muscles, Oxygen Consumption
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