Solving the conundrum of intra-specific variation in metabolic rate: A multidisciplinary conceptual and methodological toolkit: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species.
ATP
energetics
energy
mitochondria
nutrition
physiology
respirometry
Journal
BioEssays : news and reviews in molecular, cellular and developmental biology
ISSN: 1521-1878
Titre abrégé: Bioessays
Pays: United States
ID NLM: 8510851
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
24
03
2023
received:
09
02
2023
accepted:
27
03
2023
medline:
17
5
2023
pubmed:
13
4
2023
entrez:
12
4
2023
Statut:
ppublish
Résumé
Researchers from diverse disciplines, including organismal and cellular physiology, sports science, human nutrition, evolution and ecology, have sought to understand the causes and consequences of the surprising variation in metabolic rate found among and within individual animals of the same species. Research in this area has been hampered by differences in approach, terminology and methodology, and the context in which measurements are made. Recent advances provide important opportunities to identify and address the key questions in the field. By bringing together researchers from different areas of biology and biomedicine, we describe and evaluate these developments and the insights they could yield, highlighting the need for more standardisation across disciplines. We conclude with a list of important questions that can now be addressed by developing a common conceptual and methodological toolkit for studies on metabolic variation in animals.
Identifiants
pubmed: 37042115
doi: 10.1002/bies.202300026
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2300026Subventions
Organisme : Medical Research Council
ID : MC_UU_00014/4
Pays : United Kingdom
Informations de copyright
© 2023 The Authors. BioEssays published by Wiley Periodicals LLC.
Références
Pettersen, A. K., White, C. R., Bryson-Richardson, R. J., & Marshall, D. J. (2019). Linking life-history theory and metabolic theory explains the offspring size-temperature relationship. Ecology Letters, 22, 518-526.
Kozłowski, J., Konarzewski, M., & Czarnołęski, M. (2020). Coevolution of body size and metabolic rate in vertebrates: A life-history perspective. Biological Reviews, 95, 1393-1417.
White, C. R., Alton, L. A., Bywater, C. L., Lombardi, E. J., & Marshall, D. J. (2022). Metabolic scaling is the product of life-history optimization. Science, 377, 834-839.
Hood, W. R., Austad, S. N., Bize, P., Jimenez, A. G., Montooth, K. L., Schulte, P. M., Scott, G. R., Sokolova, I., Jason, R. T., Salin, K., & Salin, K. (2018). The mitochondrial contribution to animal performance, adaptation, and life-history variation: Introduction. Integrative and Comparative Biology, 58, 480-485.
Mathot, K. J., Dingemanse, N. J., & Nakagawa, S. (2019). The covariance between metabolic rate and behaviour varies across behaviours and thermal types: Meta-analytic insights. Biological Reviews, 94, 1056-1074.
Arnold, P. A., Delean, S., Cassey, P., & White, C. R. (2021). Meta-analysis reveals that resting metabolic rate is not consistently related to fitness and performance in animals. Journal of Comparative Physiology B: Biochemical Systems and Environmental Physiology, 191, 1097-1110.
Waters, J. S., Ochs, A., Fewell, J. H., & Harrison, J. F. (2017). Differentiating causality and correlation in allometric scaling: ant colony size drives metabolic hypometry. Proceedings of the Royal Society B: Biological Sciences, 284, 20162582.
Burton, T., Killen, S. S., Armstrong, J. D., & Metcalfe, N. B. (2011). What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proceedings of the Royal Society B: Biological Sciences, 278, 3465-3473.
Konarzewski, M., & Książek, A. (2013). Determinants of intra-specific variation in basal metabolic rate. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology, 183, 27-41.
Pettersen, A. K., Marshall, D. J., & White, C. R. (2018). Understanding variation in metabolic rate. Journal of Experimental Biology, 221, jeb166876.
White, C. R., & Kearney, M. R. (2013). Determinants of inter-specific variation in basal metabolic rate. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology, 183, 1-26.
Salin, K., Auer, S. K., Rey, B., Selman, C., & Metcalfe, N. B. (2015). Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance. Proceedings of the Royal Society B: Biological Sciences, 282, 20151028.
Vézina, F., Gerson, A. R., Guglielmo, C. G., & Piersma, T. (2017). The performing animal: Causes and consequences of body remodeling and metabolic adjustments in red knots facing contrasting thermal environments. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 313, R120-R131.
Glazier, D. S. (2022). How metabolic rate relates to cell size. Biology, 11, 1106.
Nilsson, J. F., & Nilsson, J.-Å. (2016). Fluctuating selection on basal metabolic rate. Ecology and Evolution, 6, 1197-1202.
Pettersen, A. K., Hall, M. D., White, C. R., & Marshall, D. J. (2020). Metabolic rate, context-dependent selection, and the competition-colonization trade-off. Evolution Letters, 4, 333-344.
Amberson, W. R., Mayerson, H. S., & Scott, W. J. (1924). The influence of oxygen tension upon metabolic rate in invertebrates. Journal of General Physiology, 7, 171-176.
Dawson, N. J., Ivy, C. M., Alza, L., Cheek, R., York, J. M., Chua, B., Milsom, W. K., McCracken, K. G., & Scott, G. R. (2016). Mitochondrial physiology in the skeletal and cardiac muscles is altered in torrent ducks, Merganetta armata, from high altitudes in the Andes. Journal of Experimental Biology, 219, 3719-3728.
Acin-Perez, R., Benador, I. Y., Petcherski, A., Veliova, M., Benavides, G. A., Lagarrigue, S., Caudal, A., Vergnes, L., Murphy, A. N., Karamanlidis, G., Tian, R., Reue, K., Wanagat, J., Sacks, H., Amati, F., Darley-Usmar, V. M., Liesa, M., Divakaruni, A. S., Stiles, L., & Shirihai, O. S. (2020). A novel approach to measure mitochondrial respiration in frozen biological samples. The EMBO Journal, 39, e104073.
Underwood, E., Redell, J. B., Zhao, J., Moore, A. N., & Dash, P. K. (2020). A method for assessing tissue respiration in anatomically defined brain regions. Scientific Reports, 10, 13179.
Suarez, R. K. (2012). Energy and metabolism. Comprehensive Physiology, 2, 2527-2540.
Ikeda, T. (2016). Routine metabolic rates of pelagic marine fishes and cephalopods as a function of body mass, habitat temperature and habitat depth. Journal of Experimental Marine Biology and Ecology, 480, 74-86.
Palacios, M. M., Killen, S. S., Nadler, L. E., White, J. R., & McCormick, M. I. (2016). Top predators negate the effect of mesopredators on prey physiology. Journal of Animal Ecology, 85, 1078-1086.
Deutsch, C., Penn, J. L., & Seibel, B. (2020). Metabolic trait diversity shapes marine biogeography. Nature, 585, 557-562.
Glazier, D. S. (2008). Effects of metabolic level on the body size scaling of metabolic rate in birds and mammals. Proceedings of the Royal Society B: Biological Sciences, 275, 1405-1410.
Aschoff, J., & Pohl, H. (1970). Rhythmic variations in energy metabolism. Federation Proceedings, 29, 1541-1552.
Piersma, T. (2011). Why marathon migrants get away with high metabolic ceilings: Towards an ecology of physiological restraint. Journal of Experimental Biology, 214, 295-302.
Weiner, J. (1992). Physiological limits to sustainable energy budgets in birds and mammals - ecological implications. Trends in Ecology & Evolution, 7, 384-388.
Thurber, C., Dugas, L. R., Ocobock, C., Carlson, B., Speakman, J. R., & Pontzer, H. (2019). Extreme events reveal an alimentary limit on sustained maximal human energy expenditure. Science Advances, 5, eaaw0341.
Williams, T. M. (2022). Racing time: Physiological rates and metabolic scaling in marine mammals. Integrative and Comparative Biology, icac054.
Westerterp, K. R. (2013). Energy balance in motion. Springer.
Drent, R., & Daan, S. (1980). The prudent parent: Energetic adjustments in avian breeding. Ardea, 68, 225-252.
Westerterp, K. R., Saris, W. H. M., Vanes, M., & Tenhoor, F. (1986). Use of the doubly labeled water technique in humans during heavy sustained exercise. Journal of Applied Physiology, 61, 2162-2167.
Treberg, J. R., Killen, S. S., MacCormack, T. J., Lamarre, S. G., & Enders, E. C. (2016). Estimates of metabolic rate and major constituents of metabolic demand in fishes under field conditions: Methods, proxies, and new perspectives. Comparative Biochemistry and Physiology A - Molecular & Integrative Physiology, 202, 10-22.
Chung, M. T., Trueman, C. N., Godiksen, J. A., & Grønkjaer, P. (2019). Otolith delta C-13 values as a metabolic proxy: Approaches and mechanical underpinnings. Marine and Freshwater Research, 70, 1747-1756.
Chung, M. T., Jørgensen, K. E. M., Trueman, C. N., Knutsen, H., Jorde, P. E., & Grønkjaer, P. (2021). First measurements of field metabolic rate in wild juvenile fishes show strong thermal sensitivity but variations between sympatric ecotypes. Oikos, 130, 287-299.
Westerterp, K. R., & Speakman, J. R. (2008). Physical activity energy expenditure has not declined since the 1980s and matches energy expenditures of wild mammals. International Journal of Obesity, 32, 1256-1263.
Jansson, J. O., Palsdottir, V., Hägg, D. A., Schéle, E., Dickson, S. L., Anesten, F., Bake, T., Montelius, M., Bellman, J., Johansson, M. E., Cone, R. D., Drucker, D. J., Wu, J., Aleksic, B., Törnqvist, A. E., Sjögren, K., Gustafsson, J.-Å., Windahl, S. H., & Ohlsson, C. (2018). Body weight homeostat that regulates fat mass independently of leptin in rats and mice. Proceedings of the National Academy of Sciences of the United States of America, 115, 427-432.
Marlatt, K. L., Chen, K. Y., & Ravussin, E. (2018). Is activation of human brown adipose tissue a viable target for weight management? American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 315, R479-R483.
Vats, P., Singh, S. N., Singh, V. K., Shyam, R., Upadhyay, T. N., Singh, S. B., & Banerjee, P. K. (2005). Appetite regulatory peptides in Indian Antarctic expeditioners. Nutritional Neuroscience, 8, 233-238.
Westerterp-Plantenga, M. S. (2016). Sleep, circadian rhythm and body weight: Parallel developments. Proceedings of the Nutrition Society, 75, 431-439.
Bennett, A. F., & Ruben, J. A. (1979). Endothermy and activity in vertebrates. Science, 206, 649-654.
Sadowska, E. T., Labocha, M. K., Baliga, K., Stanisz, A., Wróblewska, A. K., Jagusiak, W., & Koteja, P. (2005). Genetic correlations between basal and maximum metabolic rates in a wild rodent: Consequences for evolution of endothermy. Evolution, 59, 672-681.
Wone, B. W. M., Madsen, P., Donovan, E. R., Labocha, M. K., Sears, M. W., Downs, C. J., Sorensen, D. A., & Hayes, J. P. (2015). A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate. Heredity, 114, 419-427.
Swanson, D. L., Thomas, N. E., Liknes, E. T., & Cooper, S. J. (2012). Intraspecific correlations of basal and maximal metabolic rates in birds and the aerobic capacity model for the evolution of endothermy. PLoS ONE, 7, e34271.
Careau, V., Gifford, M. E., & Biro, P. A. (2014). Individual (co)variation in thermal reaction norms of standard and maximal metabolic rates in wild-caught slimy salamanders. Functional Ecology, 28, 1175-1186.
Auer, S. K., Killen, S. S., & Rezende, E. L. (2017). Resting vs. active: A meta-analysis of the intra- and inter-specific associations between minimum, sustained, and maximum metabolic rates in vertebrates. Functional Ecology, 31, 1728-1738.
Fiedler, A., & Careau, V. (2021). Individual (co)variation in resting and maximal metabolic rates in wild mice. Physiological and Biochemical Zoology, 94, 338-352.
Nespolo, R. F., & Franco, M. (2007). Whole-animal metabolic rate is a repeatable trait: A meta-analysis. Journal of Experimental Biology, 210, 2000-2005.
Auer, S. K., Bassar, R. D., Salin, K., & Metcalfe, N. B. (2016). Repeatability of metabolic rate is lower for animals living under field versus laboratory conditions. Journal of Experimental Biology, 219, 631-634.
Barceló, G., Love, O. P., & Vézina, F. (2017). Uncoupling basal and summit metabolic rates in White-throated sparrows: Digestive demand drives maintenance costs, but changes in muscle mass are not needed to improve thermogenic capacity. Physiological and Biochemical Zoology, 90, 153-165.
Brand, M. D., & Nicholls, D. G. (2011). Assessing mitochondrial dysfunction in cells. Biochemical Journal, 435, 297-312.
Brand, M. D. (2005). The efficiency and plasticity of mitochondrial energy transduction. Biochemical Society Transactions, 33, 897-904.
Koch, R. E., Buchanan, K. L., Casagrande, S., Crino, O. L., Dowling, D. K., Hill, G. E., Hood, W. R., McKenzie, M., Mariette, M. M., Noble, D. W. A., Pavlova, A., Seebacher, F., Sunnucks, P., Udino, E., White, C. R., Salin, K., & Stier, A. (2021). Integrating mitochondrial aerobic metabolism into ecology and evolution. Trends in Ecology & Evolution, 36, 321-332.
Walsberg, G. E., & Hoffman, T. C. M. (2005). Direct calorimetry reveals large errors in respirometric estimates of energy expenditure. Journal of Experimental Biology, 208, 1035-1043.
Müller, M. J., Geisler, C., Hübers, M., Pourhassan, M., Braun, W., & Bosy-Westphal, A. (2018). Normalizing resting energy expenditure across the life course in humans: Challenges and hopes. European Journal of Clinical Nutrition, 72, 628-637.
Salmón, P., Millet, C., Selman, C., Monaghan, P., & Dawson, N. J. (2023). Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata. Geroscience, 45, 265-276.
West, A. P., Shadel, G. S., & Ghosh, S. (2011). Mitochondria in innate immune responses. Nature Reviews Immunology, 11, 389-402.
Bahat, A., MacVicar, T., & Langer, T. (2021). Metabolism and innate immunity meet at the mitochondria. Frontiers in Cell and Developmental Biology, 9, 720490.
Sousa, A. P., Amaral, A., Baptista, M., Tavares, R., Campo, P. C., Peregrin, P. C., Freitas, A., Paiva, A., Almeida-Santos, T., & Ramalho-Santos, J. (2011). Not all sperm are equal: Functional mitochondria characterize a subpopulation of human sperm with better fertilization potential. PLoS ONE, 6, e18112.
Boratyński, Z., & Koteja, P. (2010). Sexual and natural selection on body mass and metabolic rates in free-living bank voles. Functional Ecology, 24, 1252-1261.
Fletcher, Q. E., Speakman, J. R., Boutin, S., Lane, J. E., McAdam, A. G., Gorrell, J. C., Coltman, D. W., & Humphries, M. M. (2015). Daily energy expenditure during lactation is strongly selected in a free-living mammal. Functional Ecology, 29, 195-208.
Rønning, B., Broggi, J., Bech, C., Moe, B., Ringsby, T. H., Pärn, H., Hagen, I. J., Saether, B., & Jensen, H. (2016). Is basal metabolic rate associated with recruit production and survival in free-living house sparrows? Functional Ecology, 30, 1140-1148.
Wiersma, P., Salomons, H. M., & Verhulst, S. (2005). Metabolic adjustments to increasing foraging costs of starlings in a closed economy. Journal of Experimental Biology, 208, 4099-4108.
Brown, J. C. L., & Staples, J. F. (2011). Mitochondrial metabolic suppression in fasting and daily torpor: Consequences for reactive oxygen species production. Physiological and Biochemical Zoology, 84, 467-480.
Willmer, P., Stone, G., & Johnston, I. A. (2005). Environmental physiology of animals (2nd ed.). Blackwell Science Ltd.
Stier, A., Romestaing, C., Schull, Q., Lefol, E., Robin, J. P., Roussel, D., & Bize, P. (2017). How to measure mitochondrial function in birds using red blood cells: A case study in the king penguin and perspectives in ecology and evolution. Methods in Ecology and Evolution, 8, 1172-1182.
Salin, K., Auer, S. K., Rudolf, A. M., Anderson, G. J., Selman, C., & Metcalfe, N. B. (2016). Variation in metabolic rate among individuals is related to tissue-specific differences in mitochondrial leak respiration. Physiological and Biochemical Zoology, 89, 511-523.
Chausse, B., Vieira-Lara, M. A., Sanchez, A. B., Medeiros, M. H. G., & Kowaltowski, A. J. (2015). Intermittent fasting results in tissue-specific changes in bioenergetics and redox state. PLoS ONE, 10, e0120413.
Farhat, E., Cheng, H., Romestaing, C., Pamenter, M., & Weber, J. M. (2021). Goldfish response to chronic hypoxia: Mitochondrial respiration, fuel preference and energy metabolism. Metabolites, 11, 187.
Hill, G. E. (2019). Mitonuclear ecology. Oxford University Press.
Consuegra, S., John, E., Verspoor, E., & de Leaniz, C. G. (2015). Patterns of natural selection acting on the mitochondrial genome of a locally adapted fish species. Genetics Selection Evolution, 47, 58.
Shen, Y. Y., Liang, L., Zhu, Z. H., Zhou, W. P., Irwin, D. M., & Zhang, Y. P. (2010). Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proceedings of the National Academy of Sciences of the United States of America, 107, 8666-8671.
Pichaud, N., Chatelain, E. H., Ballard, J. W. O., Tanguay, R., Morrow, G., & Blier, P. U. (2010). Thermal sensitivity of mitochondrial metabolism in two distinct mitotypes of Drosophila simulans: Evaluation of mitochondrial plasticity. Journal of Experimental Biology, 213, 1665-1675.
Teulier, L., Weber, J. M., Crevier, J., & Darveau, C. A. (2016). Proline as a fuel for insect flight: Enhancing carbohydrate oxidation in hymenopterans. Proceedings of the Royal Society B: Biological Sciences, 283, 20160333.
Blier, P. U., Lemieux, H., & Pichaud, N. (2014). Holding our breath in our modern world: Will mitochondria keep the pace with climate changes? Canadian Journal of Zoology, 92, 591-601.
Gyllenhammer, L. E., Entringer, S., Buss, C., & Wadhwa, P. D. (2020). Developmental programming of mitochondrial biology: A conceptual framework and review. Proceedings of the Royal Society B: Biological Sciences, 287, 20192713.
Zhang, Y. F., & Farrell, A. P. (2022). Testing the hypoxia tolerance and hypoxic performance of fishes: A two-tier screening approach. Frontiers in Marine Science, 9, 939239.
Williams, T. M., Blackwell, S. B., Tervo, O., Garde, E., Sinding, M. H. S., Richter, B., & Heide-Jørgensen, M. P. (2022). Physiological responses of narwhals to anthropogenic noise: A case study with seismic airguns and vessel traffic in the Arctic. Functional Ecology, 36, 2251-2266.
Zupa, W., Alfonso, S., Gai, F. C., Gasco, L., Spedicato, M. T., Lembo, G., & Carbonara, P. (2021). Calibrating accelerometer tags with oxygen consumption rate of Rainbow trout (Oncorhynchus mykiss) and their use in aquaculture facility: A case study. Animals, 11, 1496.
Malkoc, K., Casagrande, S., & Hau, M. (2021). Inferring whole-organism metabolic rate from red blood cells in birds. Frontiers in Physiology, 12, 691633.
Quéméneur, J. B., Danion, M., Cabon, J., Collet, S., Zambonino-Infante, J. L., & Salin, K. (2022). The relationships between growth rate and mitochondrial metabolism varies over time. Scientific Reports, 12, 16066.
Pérez-Rodríguez, M., Huertas, J. R., Villalba, J. M., & Casuso, R. A. (2023). Mitochondrial adaptations to calorie restriction and bariatric surgery in human skeletal muscle: A systematic review with meta-analysis. Metabolism, 138, 155336.
Kingma, B., Frijns, A., & van Marken Lichtenbelt, W. (2012). The thermoneutral zone: Implications for metabolic studies. Frontiers in Bioscience, 4, 1975-1985.
Sadler, D. G., Treas, L., Sikes, J. D., & Porter, C. (2022). A modest change in housing temperature alters whole body energy expenditure and adipocyte thermogenic capacity in mice. American Journal of Physiology - Endocrinology & Metabolism, 323, E517-E528.
Halsey, L. G., Fahlman, A., Handrich, Y., Schmidt, A., Woakes, A. J., & Butler, P. J. (2007). How accurately can we estimate energetic costs in a marine top predator, the king penguin? Zoology, 110, 81-92.
Schultner, J., Welcker, J., Speakman, J. R., Nordøy, E. S., & Gabrielsen, G. W. (2010). Application of the two-sample doubly labelled water method alters behaviour and affects estimates of energy expenditure in black-legged kittiwakes. Journal of Experimental Biology, 213, 2958-2966.
Butler, P. J., Green, J. A., Boyd, I. L., & Speakman, J. R. (2004). Measuring metabolic rate in the field: The pros and cons of the doubly labelled water and heart rate methods. Functional Ecology, 18, 168-183.
Bourne, A. R., McKechnie, A. E., Cunningham, S. J., Ridley, A. R., Woodborne, S. M., & Karasov, W. H. (2019). Non-invasive measurement of metabolic rates in wild, free-living birds using doubly labelled water. Functional Ecology, 33, 162-174.
Bryce, C. M., Dunford, C. E., Pagano, A. M., Wang, Y. W., Borg, B. L., Arthur, S. M., & Williams, T. M. (2022). Environmental correlates of activity and energetics in a wide-ranging social carnivore. Animal Biotelemetry, 10, 1.
Green, J. A. (2011). The heart rate method for estimating metabolic rate: Review and recommendations. Comparative Biochemistry and Physiology A - Molecular & Integrative Physiology, 158, 287-304.
Mitchell, S. E., Tang, Z. H., Kerbois, C., Delville, C., Derous, D., Green, C. L., Wang, Y., Han, J. J. D., Chen, L., Douglas, A., Lusseau, D., Promislow, D. E. L., & Speakman, J. R. (2017). The effects of graded levels of calorie restriction: VIII. Impact of short term calorie and protein restriction on basal metabolic rate in the C57BL/6 mouse. Oncotarget, 8, 17453-17474.
Levine, J. A. (2005). Measurement of energy expenditure. Public Health Nutrition, 8, 1123-1132.
Norin, T., & Metcalfe, N. B. (2019). Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change. Philosophical Transactions of the Royal Society B: Biological Sciences, 374, 20180180.
Anderson, J. M., Spurgeon, E., Stirling, B. S., May, J., Rex, P. T., Hyla, B., McCullough, S., Thompson, M., & Lowe, C. G. (2022). High resolution acoustic telemetry reveals swim speeds and inferred field metabolic rates in juvenile white sharks (Carcharodon carcharias). PLoS ONE, 17, e0268914.
Chen, C. C. W., & Welch, K. C. (2014). Hummingbirds can fuel expensive hovering flight completely with either exogenous glucose or fructose. Functional Ecology, 28, 589-600.
Krystal, A. D., Schopler, B., Kobbe, S., Williams, C., Rakatondrainibe, H., Yoder, A. D., & Klopfer, P. (2013). The relationship of sleep with temperature and metabolic rate in a hibernating primate. PLoS ONE, 8, e69914.
White, C. R., Marshall, D. J., Alton, L. A., Arnold, P. A., Beaman, J. E., Bywater, C. L., Condon, C., Crispin, T. S., Janetzki, A., Pirtle, E., Winwood-Smith, H. S., Angilletta, M. J., Chenoweth, S. F., Franklin, C. E., Halsey, L. G., Kearney, M. R., Portugal, S. J., & Ortiz-Barrientos, D. (2019). The origin and maintenance of metabolic allometry in animals. Nature Ecology & Evolution, 3, 598-603.
Czarnołęski, M., Kozłowski, J., Dumiot, G., Bonnet, J. C., Mallard, J., & Dupont-Nivet, M. (2008). Scaling of metabolism in Helix aspersa snails: Changes through ontogeny and response to selection for increased size. Journal of Experimental Biology, 211, 391-400.
Hatton, I. A., Dobson, A. P., Storch, D., Galbraith, E. D., & Loreau, M. (2019). Linking scaling laws across eukaryotes. Proceedings of the National Academy of Sciences of the United States of America, 116, 21616-21622.
Pontzer, H., Yamada, Y., Sagayama, H., Ainslie, P. N., Andersen, L. F., Anderson, L. J., Arab, L., Baddou, I., Bedu-Addo, K., Blaak, E. E., Blanc, S., Bonomi, A. G., Bouten, C. V. C., Bovet, P., Buchowski, M. S., Butte, N. F., Camps, S. G., Close, G. L., Cooper, J. A., … IAEA DLW Database Consortium. (2021). Daily energy expenditure through the human life course. Science, 373, 808-812.
Pottier, P., Burke, S., Drobniak, S. M., & Nakagawa, S. (2022). Methodological inconsistencies define thermal bottlenecks in fish life cycle: A comment on Dahlke et al. 2020. Evolutionary Ecology, 36, 287-292.
Divakaruni, A. S., & Jastroch, M. (2022). A practical guide for the analysis, standardization and interpretation of oxygen consumption measurements. Nature Metabolism, 4, 978-994.
Kumar, V., Chang, H., Reiter, D. A., Bradley, D. P., Belury, M., McCormack, S. E., & Raman, S. V. (2017). Phosphorus-31 Magnetic Resonance Spectroscopy: A tool for measuring in vivo mitochondrial oxidative phosphorylation capacity in human skeletal muscle. JoVE - Journal of Visualized Experiments, e54977.
Bartlett, M. F., Fitzgerald, L. F., Nagarajan, R., Hiroi, Y., & Kent, J. A. (2020). Oxidative ATP synthesis in human quadriceps declines during 4 minutes of maximal contractions. Journal of Physiology, 598, 1847-1863.
Cheng, M. H., Chicco, A. J., Ball, D., & Chen, T. W. (2022). Analysis of mitochondrial oxygen consumption and hydrogen peroxide release from cardiac mitochondria using electrochemical multi-sensors. Sensors and Actuators B: Chemical, 360, 131641.
Lighton, J. R. B. (2019). Measuring metabolic rates: A manual for scientists (2nd ed.). Oxford University Press.
Killen, S. S., Christensen, E. A. F., Cortese, D., Závorka, L., Norin, T., Cotgrove, L., Crespel, A., Munson, A., Nati, J. J. H., Papatheodoulou, M., & McKenzie, D. J. (2021). Guidelines for reporting methods to estimate metabolic rates by aquatic intermittent-flow respirometry. Journal of Experimental Biology, 224, jeb242522.
Schoffelen, P. F. M., & Plasqui, G. (2018). Classical experiments in whole-body metabolism: Open-circuit respirometry-diluted flow chamber, hood, or facemask systems. European Journal of Applied Physiology, 118, 33-49.
Sandstrom, D. J., & Offord, B. W. (2022). Measurement of oxygen consumption in Tenebrio molitor using a sensitive, inexpensive, sensor-based coulometric microrespirometer. Journal of Experimental Biology, 225, jeb243966.
Harrison, X. A. (2021). A brief introduction to the analysis of time-series data from biologging studies. Philosophical Transactions of the Royal Society B: Biological Sciences, 376, 20200227.
Siutz, C., Ammann, V., & Millesi, E. (2018). Shallow torpor expression in free-ranging common hamsters with and without food supplements. Frontiers in Ecology and Evolution, 6, 190.
Reider, K. E., Zerger, M., & Whiteman, H. H. (2022). Extending the biologging revolution to amphibians: Implantation, extraction, and validation of miniature temperature loggers. Journal of Experimental Zoology Part A - Ecological and Integrative Physiology, 337, 403-411.
Doherty, C. L. J., Fisk, A. T., Cooke, S. J., Pitcher, T. E., & Raby, G. D. (2022). Exploring relationships between oxygen consumption and biologger-derived estimates of heart rate in two warmwater piscivores. Journal of Fish Biology, 100, 99-106.
Song, S. R., & Beissinger, S. R. (2020). Environmental and ecological correlates of avian field metabolic rate and water flux. Functional Ecology, 34, 811-821.
Rodríguez, E., Weber, J. M., Pagé, B., Roubik, D. W., Suarez, R. K., & Darveau, C. A. (2015). Setting the pace of life: Membrane composition of flight muscle varies with metabolic rate of hovering orchid bees. Proceedings of the Royal Society B: Biological Sciences, 282, 20142232.
Post, J. R., & Lee, J. A. (1996). Metabolic ontogeny of teleost fishes. Canadian Journal of Fisheries and Aquatic Sciences, 53, 910-923.
Videlier, M., Careau, V., Wilson, A. J., & Rundle, H. D. (2021). Quantifying selection on standard metabolic rate and body mass in Drosophila melanogaster. Evolution, 75, 130-140.
Gienapp, P., Fior, S., Guillaume, F., Lasky, J. R., Sork, V. L., & Csilléry, K. (2017). Genomic quantitative genetics to study evolution in the wild. Trends in Ecology & Evolution, 32, 897-908.
Kurbalija Novičić, Z., Immonen, E., Jelić, M., Anđelković, M., Stamenković-Radak, M., & Arnqvist, G. (2015). Within-population genetic effects of mtDNA on metabolic rate in Drosophila subobscura. Journal of Evolutionary Biology, 28, 338-346.
Schaum, C. E., Team, S. R., ffrench-Constant, R., Lowe, C., Ólafsson, J. S., Padfield, D., & Yvon-Durocher, G. (2018). Temperature-driven selection on metabolic traits increases the strength of an algal-grazer interaction in naturally warmed streams. Global Change Biology, 24, 1793-1803.