{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,15]],"date-time":"2026-09-15T20:36:26Z","timestamp":1789504586505,"version":"build-2803163510"},"reference-count":48,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2025,11,9]],"date-time":"2025-11-09T00:00:00Z","timestamp":1762646400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32272650"],"award-info":[{"award-number":["32272650"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Natural Science Foundation of Changchun Normal University","award":["2017-008"],"award-info":[{"award-number":["2017-008"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Bumblebees are important pollinating insects in crop pollination. Chemical attractants can effectively improve the flower-visiting efficiency of bumblebees, thereby increasing blueberry yields. To identify volatile compounds that attract bumblebees, we collected volatile compounds from blueberry flowers using headspace extraction. Gas chromatography\u2013 mass spectrometry (GC\u2013MS) identified 32 volatile compounds, with Linalool and Styrene being the primary substances that accounted for 25.93% and 14.28%, respectively. The olfactory threshold of bumblebee antennae was assessed using electroantennography (EAG), and the behavioral responses from bumblebees were investigated using a Y-tube olfactometer. Results indicate that among the six classes of volatiles\u2014alcohols, aldehydes, esters, ketones, aromatic compounds, and olefins\u2014alcohols constituted the predominant proportion. Among these, six compounds\u2014benzaldehyde, phenylpropylaldehyde, citral, linalool, \u03b1-terpineol, and geraniol\u2014induced significant antennal responses in bumblebees. Our assays showed that geraniol, linalool, and \u03b1-terpineol at concentrations of 0.1 \u03bcg\/\u03bcL, 1 \u03bcg\/\u03bcL, and 10 \u03bcg\/\u03bcL elicited attraction, whereas higher concentrations of benzaldehyde, benzenepropanal, and citral had repellent effects.<\/jats:p>","DOI":"10.3390\/biology14111570","type":"journal-article","created":{"date-parts":[[2025,11,10]],"date-time":"2025-11-10T10:35:31Z","timestamp":1762770931000},"page":"1570","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Behavioral Responses of the Bumblebee Bombus terrestris to Volatile Compounds from Blueberries"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0009-0002-7664-8420","authenticated-orcid":false,"given":"Yun","family":"He","sequence":"first","affiliation":[{"name":"School of Life Sciences, Changchun Normal University, 677 Changjibei Road, Changchun 130032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiaru","family":"Zhang","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Changchun Normal University, 677 Changjibei Road, Changchun 130032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-3466-8839","authenticated-orcid":false,"given":"Ziyang","family":"Hu","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Changchun Normal University, 677 Changjibei Road, Changchun 130032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-3049-6808","authenticated-orcid":false,"given":"Yingxue","family":"Cao","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Changchun Normal University, 677 Changjibei Road, Changchun 130032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5399-6719","authenticated-orcid":false,"given":"Kevin H.","family":"Mayo","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Molecular Biology & Biophysics, University of Minnesota Health Sciences Center, 6-155 Jackson Hall, Minneapolis, MN 55455, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-0467-8482","authenticated-orcid":false,"given":"Duo","family":"Liu","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Changchun Normal University, 677 Changjibei Road, Changchun 130032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7108-9098","authenticated-orcid":false,"given":"Mingju","family":"E","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Changchun Normal University, 677 Changjibei Road, Changchun 130032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,11,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Zhao, X., Jiang, J., Pang, Z., Ma, W., Jiang, Y., Fu, Y., and Liu, Y. (2024). Tracking existing factors directly affecting the reproduction of bumblebees: Current knowledge. Insects, 15.","DOI":"10.3390\/insects15090654"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Zhang, H., Huang, J., Williams, P.H., Vaissi\u00e8re, B.E., Zhou, Z., Gai, Q., Dong, J., and An, J. (2015). Managed bumblebees outperform honeybees in increasing peach fruit set in China: Different limiting processes with different pollinators. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0121143"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e10914","DOI":"10.1002\/ece3.10914","article-title":"Strawberry varieties differ in pollinator-relevant floral traits","volume":"14","author":"Symington","year":"2024","journal-title":"Ecol. Evol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"170102","DOI":"10.1098\/rsos.170102","article-title":"Sensitivity of commercial pumpkin yield to potential decline among different groups of pollinating bees","volume":"4","author":"Pfister","year":"2017","journal-title":"R. Soc. Open Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1386","DOI":"10.1126\/science.aan0826","article-title":"Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter","volume":"356","author":"Adebesin","year":"2017","journal-title":"Science"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1007\/s00049-019-00297-x","article-title":"Does the orchid Luisia teres attract its male chafer pollinators (Scarabaeidae: Protaetia pryeri pryeri) by sexual deception?","volume":"30","author":"Wakamura","year":"2020","journal-title":"Chemoecology"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1111\/j.1461-0248.2010.01451.x","article-title":"The evolution of floral scent and insect chemical communication","volume":"13","author":"Schiestl","year":"2010","journal-title":"Ecol. Lett."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1936","DOI":"10.1111\/pce.12314","article-title":"Floral volatiles: From biosynthesis to function","volume":"37","author":"Muhlemann","year":"2014","journal-title":"Plant Cell Environ."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1146\/annurev-ento-120220-124357","article-title":"Chemical ecology of floral resources in conservation biological control","volume":"68","author":"Colazza","year":"2023","journal-title":"Annu. Rev. Entomol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1949","DOI":"10.1093\/jee\/toad204","article-title":"Exploratory comparison of flower visiting behavior and pollination ability of mason bees, bumble bees, and honey bees","volume":"116","author":"Lyu","year":"2023","journal-title":"J. Econ. Entomol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1086\/697220","article-title":"Dispensing pollen via catapult: Explosive pollen release in mountain laurel (Kalmia latifolia)","volume":"191","author":"Switzer","year":"2018","journal-title":"Am. Nat."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1111\/ele.12386","article-title":"Bees use honest floral signals as indicators of reward when visiting flowers","volume":"18","author":"Knauer","year":"2015","journal-title":"Ecol. Lett."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"111468","DOI":"10.1016\/j.foodres.2022.111468","article-title":"Terpene volatiles mediates the chemical basis of blueberry aroma and consumer acceptability","volume":"158","author":"Sater","year":"2022","journal-title":"Food Res. Int."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Sanchez-Ballesta, M.T., Marti-Anders, C., \u00c1lvarez, M.D., Escribano, M.I., Merodio, C., and Romero, I. (2023). Are the blueberries we buy good quality? comparative study of berries purchased from different outlets. Foods, 12.","DOI":"10.3390\/foods12132621"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Ma, L., Sun, Z., Zeng, Y., Luo, M., and Yang, J. (2018). Molecular mechanism and health role of functional ingredients in blueberry for chronic disease in human beings. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19092785"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Cromie, J., Ternest, J.J., Komatz, A.P., Adunola, P.M., Azevedo, C., Mallinger, R.E., and Mu\u00f1oz, P.R. (2024). Genotypic variation in blueberry flower morphology and nectar reward content affects pollinator attraction in a diverse breeding population. BMC Plant Biol., 24.","DOI":"10.1186\/s12870-024-05495-6"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Mi\u00f1arro, M., and Garc\u00eda, D. (2021). Complementary contribution of wild bumblebees and managed honeybee to the pollination niche of an introduced blueberry crop. Insects, 12.","DOI":"10.3390\/insects12070595"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1093\/jee\/tox344","article-title":"Pollen foraging differences among three managed pollinators in the highbush blueberry (Vaccinium corymbosum) agroecosystem","volume":"111","author":"Bobiwash","year":"2018","journal-title":"J. Econ. Entomol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Estravis-Barcala, M.C., Palottini, F., Macri, I., Nery, D., and Farina, W.M. (2021). Managed honeybees and South American bumblebees exhibit complementary foraging patterns in highbush blueberry. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-87729-3"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Zhang, J., Liu, J., Gao, F., Chen, M., Jiang, Y., Zhao, H., and Ma, W. (2022). Electrophysiological and behavioral responses of apis mellifera and bombusterrestris to melon flower volatiles. Insects, 13.","DOI":"10.3390\/insects13110973"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1139\/Z10-031","article-title":"The chemical ecology and evolution of bee flower interactions: A review and perspectives","volume":"88","author":"Vereecken","year":"2010","journal-title":"Can. J. Zool."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1111\/j.1469-8137.2010.03410.x","article-title":"Pollinators exert natural selection on flower size and floral display in Penstemon digitalis","volume":"188","author":"Parachnowitsch","year":"2010","journal-title":"New Phytol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1111\/j.1365-2435.2009.01627.x","article-title":"The evolution of floral scent: The influence of olfactory learning by insect pollinators on the honestsignalling of floral rewards","volume":"23","author":"Wright","year":"2009","journal-title":"Funct. Ecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/j.anbehav.2006.11.012","article-title":"Osmia bees (Hymenoptera: Megachilidae) can detect nectar-rewarding flowers using olfactory cues","volume":"74","author":"Howell","year":"2007","journal-title":"Anim. Behav."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"104920","DOI":"10.1016\/j.bse.2024.104920","article-title":"Chemical mimicry in the corpse flower: Floral odor and phytochemical profiles of Amorphophallus titanum (becc.) becc","volume":"118","author":"Raman","year":"2025","journal-title":"Biochem. Syst. Ecol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.tree.2013.01.019","article-title":"Pollinator-mediated evolution of floral signals","volume":"28","author":"Schiestl","year":"2013","journal-title":"Trends Ecol. Evol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1111\/j.1365-2435.2008.01517.x","article-title":"The sweet smell of success: Floral scent affects pollinator attraction and seed fitness inHesperis matronalis","volume":"23","author":"Majetic","year":"2009","journal-title":"Funct. Ecol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1007\/s00114-007-0251-1","article-title":"Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers","volume":"94","author":"Spaethe","year":"2007","journal-title":"Die Naturwissenschaften"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1111\/plb.12957","article-title":"Nectar yeasts enhance the interaction between Clematis akebioides and its bumblebee pollinator","volume":"21","author":"Yang","year":"2019","journal-title":"Plant Biol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Liu, J., Zhang, J., Shen, J., Zhao, H., Ma, W., and Jiang, Y. (2022). Differences in EAG response and behavioral choices between honey bee and bumble bee to tomato flower volatiles. Insects, 13.","DOI":"10.3390\/insects13110987"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1016\/j.jnutbio.2012.12.010","article-title":"Wild blueberry (Vaccinium angustifolium) consumption improves inflammatory status in the obese zucker rat model of the metabolic syndrome","volume":"24","author":"Vendrame","year":"2013","journal-title":"J. Nutr. Biochem."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1111\/nph.14809","article-title":"Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator","volume":"220","author":"Rering","year":"2017","journal-title":"New Phytol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/S1369-5266(02)00251-0","article-title":"The formation and function of plant volatiles: Perfumes for pollinator attraction and defense","volume":"5","author":"Pichersky","year":"2002","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.1093\/aob\/mcr077","article-title":"Variation in highbush blueberry floral volatile profiles as a function of pollination status, cultivar, time of day and flower part: Implications for flower visitation by bees","volume":"107","author":"Parra","year":"2011","journal-title":"Ann. Bot."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1007\/s10337-018-3550-0","article-title":"Evaluation of Headspace Solid-Phase Microextraction Gas Chromatography-MassSpectrometry for the characterization of volatile organic compounds from Melon (Cucumis melo L.) Flowers","volume":"81","author":"Silva","year":"2018","journal-title":"Chromatographia"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1127\/entomologia\/2023\/2096","article-title":"Bumblebees\u2019 flower preferences are associated with floral abundance and buzz frequency when buzz-pollinating co-flowering plants","volume":"44","author":"Huang","year":"2024","journal-title":"Entomol. Gen."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Kreiman, G., MaBouDi, H., Shimazaki, H., Giurfa, M., and Chittka, L. (2017). Olfactory learning without the mushroom bodies: Spiking neural network models of the honeybee lateral antennal lobe tract reveal its capacities in odour memory tasks of varied complexities. PLoS Comput. Biol., 13.","DOI":"10.1371\/journal.pcbi.1005551"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"L\u00f6sel, P.D., Monchanin, C., Lebrun, R., Jayme, A., Relle, J.J., Devaud, J.M., Heuveline, V., and Lihoreau, M. (2023). Natural variability in bee brain size and symmetry revealed by micro-CT imaging and deep learning. PLoS Comput. Biol., 19.","DOI":"10.1371\/journal.pcbi.1011529"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1038\/387285a0","article-title":"Representations of odours and odour mixtures visualized in the honeybee brain","volume":"387","author":"Joerges","year":"1997","journal-title":"Nature"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1016\/S0959-4388(00)00109-4","article-title":"Odour perception in honeybees: Coding information in glomerular patterns","volume":"10","author":"Galizia","year":"2000","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1007\/s004410051245","article-title":"A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy","volume":"295","author":"Galizia","year":"1999","journal-title":"Cell Tissue Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1111\/1365-2745.14242","article-title":"Insect herbivory but not plant pathogen infection drive floral volatile-mediated indirect effects on pollinators and plant fitness in Brassica rapa","volume":"112","author":"Moreira","year":"2024","journal-title":"J. Ecol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"267","DOI":"10.2135\/cropsci1965.0011183X000500030023x","article-title":"Flower color, a factor in attractiveness of alfalfa clones for honeybees","volume":"5","author":"Clement","year":"1965","journal-title":"Crop Sci."},{"key":"ref_44","unstructured":"Kauffeld, N.M., and Sorensen, E.L. (1971). Interrelations of Honeybee Preference and Alfalfa Clones and Flower Color, Aroma, Nectar Volume and Sugar Concentration, Agricultural Experiment Station, Kansas State University of Agriculture and Aplied Science."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1007\/s00359-011-0673-2","article-title":"Behavioural plasticity and sex differences in host finding of a specialized bee species","volume":"197","author":"Milchreit","year":"2011","journal-title":"J. Comp.Physiol. A"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1007\/s00359-005-0081-6","article-title":"The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth","volume":"192","author":"Balkenius","year":"2006","journal-title":"J. Comp. Physiol. A"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e09708","DOI":"10.1111\/oik.09708","article-title":"Range-wide floral trait variation reflects shifts in pollinator assemblages, consistent with pollinator-mediated divergence despite generalized visitation","volume":"2023","author":"Wenzell","year":"2023","journal-title":"Oikos"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"D\u00f6tterl, S., Gl\u00fcck, U., J\u00fcrgens, A., Woodring, J., and Aas, G. (2014). Floral reward, advertisement and attractiveness to honey bees in dioecious Salix caprea. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0093421"}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/14\/11\/1570\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,14]],"date-time":"2025-11-14T10:40:55Z","timestamp":1763116855000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/14\/11\/1570"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,9]]},"references-count":48,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["biology14111570"],"URL":"https:\/\/doi.org\/10.3390\/biology14111570","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,9]]}}}