Hummingbirds pay a high cost for a warm drink
Abstract
Endotherms must warm ingested food to body temperature. Food warming costs may be especially high for nectar-feeding birds, which can ingest prodigious volumes. We formulated a mathematical model to predict the cost of warming nectar as a function of nectar temperature and sugar concentration. This model predicts that the cost of warming nectar should: (1) decrease as a power function of nectar concentration, and (2) increase linearly with the difference between body temperature and nectar temperature. We tested our model on rufous hummingbirds (Selasphorus rufus). A typical experiment consisted of feeding birds nectar of a given concentration at 39 degrees C (equivalent to body temperature) and then at 4 degrees C, and vice versa. We used the percentage change in metabolic rate between the two food temperatures to estimate the cost of warming nectar. The model's predictions were accurately met. When birds had to hover rather than perch during feeding bouts, estimated food-warming costs were only slightly lower. The cost of warming nectar to body temperature appears to be an important yet overlooked aspect of the energy budgets of nectar-feeding birds. Hummingbirds feeding on 5% sucrose solutions at 4 degrees C have to increase their metabolic rate by an amount equivalent to that elicited by a 15 degrees C drop in ambient temperature.
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Lower nectar temperatures will impose additional energetic costs on meal acquisition by hummingbirds.
“lower nectar temperatures will impose additional energetic costs on meal acquisition by hummingbirds (Lotz et al., 2003)”
From The physiology and biomechanics of avian flight at high altitude (2006) · cites this paper as Lotz et al., 2003
Cites
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“The effects of meal temperature are most evident for endotherms living in cold environments that consume food that may be more than 30 C lower than their body temperature (Battam et al. 2008; Lotz et al. 2003; Wilson and Culik 1991).”
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Self-citationThe physiology and biomechanics of avian flight at high altitude
Altshuler, D. L. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icj008 · Cited by 141 · see citing works
“For example, lower nectar temperatures will impose additional energetic costs on meal acquisition by hummingbirds (Lotz et al., 2003).”
BackgroundConcentration and temperature effects on sugar intake and preferences in a sunbird and a hummingbird
Fleming, P. A., Bakken, B. H., Lotz, C. N., & Nicolson, S. W. (2004) · Functional Ecology · doi:10.1111/j.0269-8463.2004.00818.x · Cited by 83 · see citing works
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“Warmth from flowers can provide an energetic benefit to visiting pollinators [4,5,10], and modelling suggests this may allow plants to provide the same energetic reward with less nectar production [11].”
BackgroundResultHoneybees prefer warmer nectar and less viscous nectar, regardless of sugar concentration
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“The first is energetic, as demonstrated by differences in the metabolic rate of hummingbirds drinking cool and warm nectar [29].”
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Martin, V., Schaeffer, R., & Fukami, T. (2022) · Philosophical Transactions of the Royal Society of London. Biological Sciences · doi:10.1098/rstb.2021.0155 · Cited by 64
“Given that some pollinators may prefer warmer nectar [60], perhaps because warmer nectar is easier to digest (but see [61]), nectar microbes may exert their influences on pollinator health through nectar warming.”
A review of the energetics of pollination biology
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The sugar oxidation cascade: aerial refueling in hummingbirds and nectar bats
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“At low Ta, thermogenic mechanisms are activated (Bicudo et al., 2002), resulting in elevation of rates of energy expenditure (Lasiewski, 1963; Lopez-Calleja and Bozinovic, 1995; Lotz et al., 2003).”
BackgroundFleming, P. A., & Nicolson, S. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00351 · Cited by 38
“It is possible that this posture was a response to warming large volumes of cold food to body temperature (Lotz et al., 2003), or else the increased water flux, and potentially greater evaporative losses, increased P. A. Fleming and S. W. Nicolson 1853Diet and osmoregulation in an avian…”
BackgroundSelf-citationDrinking problems on a ‘simple’ diet: physiological convergence in nectar-feeding birds
Nicolson, S. W., & Fleming, P. A. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.054387 · Cited by 32 · see citing works
“The combination of low temperature and dilute food is particularly stressful because birds have to warm ingested food to body temperature, shown by the increased metabolic rate of hummingbirds consuming dilute nectar in the cold (Lotz et al., 2003).”
BackgroundSelf-citationMata, A., & Bosque, C. (2004) · Comparative biochemistry and physiology. Part A, Molecular & integrative physiology · doi:10.1016/j.cbpb.2004.10.012 · Cited by 32
“Cost of food warming, energy expenditure in recovering solutes, and electrolyte losses increase with food dilution (Fleming and Nicolson, 2003; Lotz et al., 2003; Lotz and Nicolson, 2002).”
BackgroundGonzález-Gómez, P. L., Vásquez, R., & Bozinovic, F. (2011) · doi:10.1525/auk.2011.10024 · Cited by 30
“In order to meet these high energy demands, hummingbirds must ingest large quantities of high-quality nectar (Lotz et al. 2003).”
BackgroundRegulation of nutrient intake in nectar-feeding birds: insights from the geometric framework
Köhler, A., Raubenheimer, D., & Nicolson, S. (2012) · Journal of Comparative Physiology □ B · doi:10.1007/s00360-011-0639-2 · Cited by 27 · see citing works
“ingested nectar to body temperature increase with decreasing nectar temperature (Lotz et al. 2003).”
BackgroundInfluentialSelf-citationEvidence of ‘sickness behaviour’ in bats with white-nose syndrome
Bohn, S. J., Turner, J. M., Warnecke, L., Mayo, C., McGuire, L., Misra, V., Bollinger, T., & Willis, C. (2016) · doi:10.1163/1568539x-00003384 · Cited by 26
“Crawling or flying is also energetically costly for bats and, when combined with conductive heat loss from climbing across cold surfaces to get to a water source, or drinking cold water (Lotz et al., 2003), its effect on energy stores could be dramatic.”
BackgroundTan, K., Latty, T., Hu, Z., Wang, Z.-W., Yang, S., Chen, W.-W., & Oldroyd, B. (2013) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-013-1617-3 · Cited by 22
“Even endotherms like hummingbirds pay a significant metabolic cost when they imbibe cold nectar (Lotz et al. 2003).”
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Self-citationHovering 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
Seasonal intake responses in the nectar-feeding bat Glossophaga soricina
Ayala‐Berdón, J., Schondube, J. E., & Stoner, K. E. (2009) · Journal of Comparative Physiology B · doi:10.1007/s00360-008-0335-z · Cited by 20 · see citing works
Thermoregulatory 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
“Hence, to cope with low temperatures, hummingbirds must ingest large quantities of nectar (Lotz et al. 2003; López-Calleja and Bozinovic 2003).”
BackgroundA nectar-feeding mammal avoids body fluid disturbances by varying renal function
Bakken, B. H., M., L. G. H., Carroll, R. M., Ayala‐Berdón, J., Schondube, J. E., & del Rio, C. M. (2008) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.90349.2008 · Cited by 14 · see citing works
Köhler, A., Verbürgt, L., Fleming, P. A., & Nicolson, S. W. (2008) · Journal of Comparative Physiology B · doi:10.1007/s00360-008-0269-5 · Cited by 13 · see citing works
Self-citationTjørve, K., Underhill, L. G., & Visser, G. (2007) · doi:10.1111/j.1474-919x.2007.00752.x · Cited by 16
“We used the same experimental protocol employed by Lotz et al. (2003), with some modifications to ambient temperature and flow rate.”
MethodSucrose Hydrolysis Does Not Limit Food Intake by Pallas’s Long‐Tongued Bats
M., L., & G, C. A. M. (2007) · Physiological and Biochemical Zoology · doi:10.1086/522904 · Cited by 13
Drinking made easier: honey bee tongues dip faster into warmer and/or less viscous artificial nectar
Shi, L., Nicolson, S. W., Yang, Y., Wu, J., Yan, S., & Wu, Z. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.229799 · Cited by 15 · see citing works
Self-citationTjørve, K., Underhill, L., & Visser, G. (2007) · Zoology · doi:10.1016/j.zool.2007.01.002 · Cited by 12
“After the oxygen analyser, the air passed through the pump and finally into a bubble flow metre for accurate measure of flow rate (Lotz et al., 2003).”
MethodInfluentialMata, A. (2010) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2010.07.018 · Cited by 8 · see citing works
Nicolson, S., Hoffmann, D., & Fleming, P. A. (2005) · Functional Ecology · doi:10.1111/j.1365-2435.2005.01042.x · Cited by 9 · see citing works
Self-citationIs energy in nectar a good predictor of hummingbird activity at landscape scale?
Ortiz-Pulido, R., & Rodríguez, C. (2012) · doi:10.1080/11250003.2011.602367 · Cited by 8
“…temperature was 17.7◦C, with a variation from 15.2 to 19.7◦C. Hummingbird metabolic rate change in this temperature range has been reported as less than 2.5% (sensu figure 1 in Lotz et al. 2003), so we supposed that metabolic cost in the recorded hummingbirds remained similar in our study period.”
ResultInfluentialAdded salt helps sunbirds and honeyeaters maintain energy balance on extremely dilute nectar diets
Purchase, C., Fleming, P. A., & Nicolson, S. W. (2010) · Journal of Comparative Physiology B · doi:10.1007/s00360-010-0493-7 · Cited by 7 · see citing works
“the increased energetic costs of electrolyte and glucose recovery, and steeply increasing costs of warming food to body temperature (Beuchat et al. 1990; Fleming and Nicolson 2003; Lotz et al. 2003).”
BackgroundSelf-citationTestosterone levels in feces predict risk-sensitive foraging in hummingbirds
Chávez-Zichinelli, C. A., Gómez, L., Ortiz-Pulido, R., Lara, C., Valdez, R., & Romano, M. (2014) · doi:10.1111/jav.00387 · Cited by 7
Evaporative water loss and dehydration during the night in hummingbirds
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Premigratory fat metabolism in hummingbirds: A Rumsfeldian approach
Suarez, R. K. (2013) · Current Zoology · doi:10.1093/czoolo/59.3.371 · Cited by 3 · see citing works
“Low ambient temperature also elevates the energetic cost of foraging flight (Schuchmann, 1979; Chai et al., 1998; Welch and Suarez, 2008) as well as the cost of warming up cold nectar (Lotz et al., 2003).”
BackgroundTjørve, K., Underhill, L. G., & Visser, G. (2007) · Emu - Austral Ornithology · doi:10.1071/mu06033 · Cited by 3 · see citing works
“…rate Resting metabolic rates (RMRs) was determined for free-living Spotted Thick-knee chicks at different ages during the prefledging period using the experimental protocol of Lotz et al. (2003), with some modifications to ambient temperature and flow rate appropriate to the size of the chicks.”
MethodGroom, D. J. E., Bayram, N., Shehata, M., M., L. G. H., & Welch, K. C. (2019) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2019.110559 · Cited by 3 · see citing works
Köhler, A., Verbürgt, L., Fleming, P. A., McWhorter, T. J., & Nicolson, S. (2011) · doi:10.1071/mu10032 · Cited by 2
“Why did the birds not feed at maximal rates the entire afternoon and evening to compensate for the lost foraging time? Warming large amounts of ingested nectar to body temperature is energetically costly, and costs of food warming increase with increasing temperature difference between body and nectar (Lotz et al. 200…”
BackgroundSelf-citationGowland, F. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.00749 · Cited by 2
Bradley, T. H., & Melby, C. L. (2016) · Journal of Energy Resources Technology · doi:10.1115/1.4033628 · Cited by 2 · see citing works
“Under these conditions, the energy required to warm this volume of nectar can lead to a 2% weight loss per day [15,16].”
BackgroundFirst record of meso- and microplastics ingestion in hummingbirds (Trochilidae)
Moreno, J., Sarquis, J. A., Garello, N., Cappelletti, A. L., & Blettler, M. C. M. (2026) · Chemosphere · doi:10.1016/j.chemosphere.2026.145119
Crestani, A. C., Pizo, M. A., Fontanella, A. B. A., M., L., & Cruz-Neto, A. (2021) · Journal of Avian Biology · doi:10.1111/jav.02873/v2/decision1
- Authors
- Lotz, C. N., Mart�nez del Rio, C., & Nicolson, S. W.
- Affiliations
- University of Wyoming (US)
- University of Pretoria (ZA)
- ORCID
- Nicolson, S. W.
- Venue
- Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology
- Published
- 2003-08-01
- Volume
- 173
- Issue
- 6
- Pages
- 455-462
- ISSN
- 0174-1578 (ISSN-L)
- 1432-136X
- OpenAlex
- W2131122595
- Cited by
- 66
- References
- 0
- Citations by year
- 2026: 1 · 2022: 1 · 2021: 1 · 2020: 1 · 2019: 1 · 2016: 2 · 2015: 1 · 2014: 2 · 2013: 4 · 2012: 1
- FWCI
- 2.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Comparative Physiology B (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Physical Sciences › Environmental Science › Ecology › Avian ecology and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
- Keywords
- hummingbirds, nectar feeding, endothermy, metabolic rate, sugar content, Rufous hummingbird, Selasphorus rufus, energy balance, hover feeding, mathematical model
- MeSH terms
- Administration, Oral, Animals, Electronic Data Processing, Birds, Body Temperature, Body Temperature Regulation, Calorimetry, Indirect, Drinking, Eating, Energy Metabolism, Exercise Test, Models, Theoretical, Oxygen Consumption, Sucrose, Water, Thermogenesis
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