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We provide the first direct quantification of the metabolic cost of floral buzzing in bumblebees and evaluate its ecological significance. Using flow-through respirometry synchronized with laser vibrometry, we measured carbon dioxide production during floral buzzing by Bombus terrestris and compared it with flight take-off, which is powered by the same thoracic muscles. Floral buzzing required high muscular effort compared with other behaviours, with approximately 0.10 J per event and mass-specific power approximately 293 W\/kg. Overall costs were comparable to take-off because floral buzzing bouts are longer despite a lower metabolic rate. Metabolic rate scaled with body mass, whereas intertegular span did not, implying that transient load rather than structural size better explains energetic demand in short, high-intensity behaviours. Metabolic traits were highly repeatable within individuals, but variable between individuals, and colony identity also explained additional variance. Converting costs to nectar equivalents showed that floral buzzing required slightly more nectar than take-off and that requirements rose as nectar sugar concentration declined. We conclude that floral buzzing is a major, previously unquantified component of bee energy budgets that is likely to shape nectar demands, flower visitation patterns and generally plant\u2013pollinator interactions.<\/jats:p>","DOI":"10.1098\/rspb.2026.0206","type":"journal-article","created":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T00:20:56Z","timestamp":1779236456000},"source":"Crossref","is-referenced-by-count":5,"title":["First direct quantification of floral handling costs in bees"],"prefix":"10.1098","volume":"293","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3631-9019","authenticated-orcid":false,"given":"Natacha","family":"Rossi","sequence":"first","affiliation":[{"name":"University of Sussex 1 , ,","place":["Brighton, UK, BN1 9RH"],"department":["Ecology and Evolution"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5663-8025","authenticated-orcid":false,"given":"Mario","family":"Vallejo-Marin","sequence":"additional","affiliation":[{"name":"Uppsala Universitet 2 , ,","place":["Uppsala, Sweden, 752 36"],"department":["Department of Ecology and Genetics"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3697-0223","authenticated-orcid":false,"given":"Elizabeth","family":"Nicholls","sequence":"additional","affiliation":[{"name":"University of Sussex 1 , ,","place":["Brighton, UK, BN1 9RH"],"department":["Ecology and Evolution"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2026,5,20]]},"reference":[{"key":"2026051920205389800_R1","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.86176","article-title":"How honey bees make fast and accurate decisions","volume":"12","author":"MaBouDi","year":"2023","journal-title":"eLife"},{"key":"2026051920205389800_R2","doi-asserted-by":"crossref","first-page":"4279","DOI":"10.1016\/j.cub.2022.07.062","article-title":"Ecology dictates the value of memory for foraging bees","volume":"32","author":"Pull","year":"2022","journal-title":"Curr. 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Insect Behav."},{"key":"2026051920205389800_R26","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1093\/beheco\/arx058","article-title":"How a generalist bee achieves high efficiency of pollen collection on diverse floral resources","volume":"28","author":"Russell","year":"2017","journal-title":"Behav. Ecol."},{"key":"2026051920205389800_R27","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1086\/318112","article-title":"Energy metabolism during insect flight: biochemical design and physiological performance","volume":"73","author":"Suarez","year":"2000","journal-title":"Physiol. Biochem. 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Zool."},{"key":"2026051920205389800_R47","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.3390\/agriculture12081132","article-title":"Nectar abundance and nectar composition in selected Rubus idaeus L. varieties","volume":"12","author":"Kostryco","year":"2022","journal-title":"Agriculture"},{"key":"2026051920205389800_R48","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1051\/agro:19900305","article-title":"Genetical studies of nectar and pollen production in sunflower","volume":"10","author":"Vear","year":"1990","journal-title":"Agronomie"},{"key":"2026051920205389800_R49","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2021.755843","article-title":"Climate change-induced stress reduce quantity and alter composition of nectar and pollen from a bee-pollinated species (Borago officinalis, Boraginaceae)","volume":"12","author":"Descamps","year":"2021","journal-title":"Front. 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Lett."},{"key":"2026051920205389800_R55","doi-asserted-by":"crossref","DOI":"10.1126\/sciadv.aay3115","article-title":"Kinematic flexibility allows bumblebees to increase energetic efficiency when carrying heavy loads","volume":"6","author":"Combes","year":"2020","journal-title":"Sci. Adv."},{"key":"2026051920205389800_R56","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1146\/annurev.es.06.110175.001035","article-title":"Energetics of pollination","volume":"6","author":"Heinrich","year":"1975","journal-title":"Annu. Rev. Ecol. Syst."},{"key":"2026051920205389800_R57","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1007\/BF00693012","article-title":"Flight of the honey bee - IV. Respiratory quotients and metabolic rates during sitting, walking and flying","volume":"158","author":"Rothe","year":"1989","journal-title":"J. Comp. Physiol. B"},{"key":"2026051920205389800_R58","first-page":"476","volume-title":"The biomechanics of insect flight: form, function, evolution","author":"Dudley","year":"2002"},{"key":"2026051920205389800_R59","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1242\/jeb.187.1.315","article-title":"Correlation of sound generation and metabolic heat flux in the bumblebee Bombus lapidarius","volume":"187","author":"Schultze-Motel","year":"1994","journal-title":"J. Exp. Biol."},{"key":"2026051920205389800_R60","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1007\/s000400050148","article-title":"Foraging costs in bumblebees: field conditions cause large individual differences","volume":"46","author":"Wolf","year":"1999","journal-title":"Insectes Soc."},{"key":"2026051920205389800_R61","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1007\/BF00706595","article-title":"Thermoregulation in bumblebees","volume":"96","author":"Heinrich","year":"1975","journal-title":"J. Comp. 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Biol."},{"key":"2026051920205389800_R65","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1086\/665568","article-title":"Morphological and physiological idiosyncrasies lead to interindividual variation in flight metabolic rate in worker bumblebees (Bombus impatiens)","volume":"85","author":"Skandalis","year":"2012","journal-title":"Physiol. Biochem. Zool."},{"key":"2026051920205389800_R66","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1098\/rstb.1984.0052","article-title":"The aerodynamics of hovering insect flight. IV. Aerodynamic mechanisms","volume":"305","author":"Ellington","year":"1984","journal-title":"Phil. Trans. R. Soc. Lond. B"},{"key":"2026051920205389800_R67","volume-title":"The hot-blooded insects: strategies and mechanisms of thermoregulation","author":"Heinrich","year":"1993"},{"key":"2026051920205389800_R68","doi-asserted-by":"crossref","first-page":"2317","DOI":"10.1242\/jeb.199.10.2317","article-title":"Activity of asynchronous flight muscle from two bee families during sonication (buzzing)","volume":"199","author":"King","year":"1996","journal-title":"J. Exp. Biol."},{"key":"2026051920205389800_R69","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1007\/s00442-012-2535-1","article-title":"Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers","volume":"172","author":"De Luca","year":"2013","journal-title":"Oecologia"},{"key":"2026051920205389800_R70","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.tree.2009.07.013","article-title":"Behavioural reaction norms: animal personality meets individual plasticity","volume":"25","author":"Dingemanse","year":"2010","journal-title":"Trends Ecol. Evol."},{"key":"2026051920205389800_R71","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1111\/j.1420-9101.2007.01300.x","article-title":"The evolutionary ecology of individual phenotypic plasticity in wild populations","volume":"20","author":"Nussey","year":"2007","journal-title":"J. Evol. 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