{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T18:13:03Z","timestamp":1788459183870,"version":"build-2803163510"},"reference-count":50,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T00:00:00Z","timestamp":1788393600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005363","name":"University of Buenos Aires","doi-asserted-by":"publisher","award":["PIDAE 2025, PIDAE Estructural 1-33-6-1"],"award-info":[{"award-number":["PIDAE 2025, PIDAE Estructural 1-33-6-1"]}],"id":[{"id":"10.13039\/501100005363","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005363","name":"University of Buenos Aires","doi-asserted-by":"publisher","award":["UBACYT 2026, 20020250100069BA"],"award-info":[{"award-number":["UBACYT 2026, 20020250100069BA"]}],"id":[{"id":"10.13039\/501100005363","id-type":"DOI","asserted-by":"publisher"}]},{"award":["PIDAE 2025, PIDAE Estructural 1-33-6-1"],"award-info":[{"award-number":["PIDAE 2025, PIDAE Estructural 1-33-6-1"]}],"id":[{"id":"https:\/\/ror.org\/0081fs513","id-type":"ROR","asserted-by":"publisher"}]},{"award":["UBACYT 2026, 20020250100069BA"],"award-info":[{"award-number":["UBACYT 2026, 20020250100069BA"]}],"id":[{"id":"https:\/\/ror.org\/0081fs513","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Within the framework of animal learning theory, information transfer refers to the generalization or transmission of acquired knowledge to novel situations, individuals, or environments. In pollinators, this process is critical for adaptive foraging and ecological success. Although olfactory information transfer has been demonstrated in bumblebees through classical conditioning or colony exposure, the influence of reward type (nectar vs. pollen) remains poorly understood. Here, we evaluated olfactory information transfer and decision-making in the South American bumblebee Bombus pauloensis using complementary laboratory and colony-based experiments. Under laboratory conditions, bees were either classically conditioned through the proboscis extension reflex (PER) paradigm using scented sucrose solution or exposed overnight to scented pollen and subsequently tested in a four-arm arena. In a more natural context, colonies were exposed to scented sucrose solution or scented pollen through in-nest feeders, after which foraging choices were assessed in a flight cage. Sucrose-conditioned bees exhibited an odor-contingent preference in the four-arm arena, consistent with associative learning under our conditions. In contrast, pollen exposure produced odor-associated trends. Linalool exhibited a bias, although airborne volatile concentrations were not directly quantified, representing a methodological limitation. Moreover, linalool-scented pollen induced intense feeder manipulation and increased mortality during overnight exposure, highlighting substantial physiological costs. Under colony conditions, 24-h exposure to scented pollen promoted significant odor-guided search preferences, particularly with linalool, whereas no significant effect of scented sucrose was detected under our 24 h in-nest exposure; individual feeder contact was not verified. Overall, behavioral responses varied jointly with odor identity and the combined operational framework; the salience of pollen-associated odors observed here is consistent with reward-specific effects but cannot be fully disentangled from differences in protocol structure between the sucrose and pollen experiments.<\/jats:p>","DOI":"10.3390\/insects17090924","type":"journal-article","created":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T17:13:25Z","timestamp":1788455605000},"page":"924","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Olfactory Information Transfer in Bumblebees and Its Variation According to the Food Resource"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0009-0007-0689-5764","authenticated-orcid":false,"given":"Tom\u00e1s Eloy","family":"Gonz\u00e1lez-Chinnici","sequence":"first","affiliation":[{"name":"Laboratorio de Insectos Sociales, Departamento de Biodiversidad y Biolog\u00eda Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires 1428, Argentina"},{"name":"Instituto de Fisiolog\u00eda, Biolog\u00eda Molecular y Neurociencias (IFIBYNE), CONICET-Universidad de Buenos Aires, Buenos Aires 1428, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mateo","family":"Mir\u00f3","sequence":"additional","affiliation":[{"name":"Laboratorio de Insectos Sociales, Departamento de Biodiversidad y Biolog\u00eda Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires 1428, Argentina"},{"name":"Instituto de Fisiolog\u00eda, Biolog\u00eda Molecular y Neurociencias (IFIBYNE), CONICET-Universidad de Buenos Aires, Buenos Aires 1428, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-5283-4360","authenticated-orcid":false,"given":"Camila Bel\u00e9n","family":"Salda\u00f1a","sequence":"additional","affiliation":[{"name":"Laboratorio de Insectos Sociales, Departamento de Biodiversidad y Biolog\u00eda Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires 1428, Argentina"},{"name":"Instituto de Fisiolog\u00eda, Biolog\u00eda Molecular y Neurociencias (IFIBYNE), CONICET-Universidad de Buenos Aires, Buenos Aires 1428, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6411-489X","authenticated-orcid":false,"given":"Walter Marcelo","family":"Farina","sequence":"additional","affiliation":[{"name":"Laboratorio de Insectos Sociales, Departamento de Biodiversidad y Biolog\u00eda Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires 1428, Argentina"},{"name":"Instituto de Fisiolog\u00eda, Biolog\u00eda Molecular y Neurociencias (IFIBYNE), CONICET-Universidad de Buenos Aires, Buenos Aires 1428, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1890\/130330","article-title":"From research to action: Enhancing crop yield through wild pollinators","volume":"12","author":"Garibaldi","year":"2014","journal-title":"Front. Ecol. Environ."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3516","DOI":"10.1111\/gcb.14736","article-title":"Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification","volume":"25","author":"Aizen","year":"2019","journal-title":"Glob. Change Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"259","DOI":"10.17584\/rcch.2015v9i2.4182","article-title":"Comportamiento y eficiencia de polinizaci\u00f3n de Bombus atratus Franklin en piment\u00f3n (Capsicum annum L.) sembrado bajo invernadero","volume":"9","author":"Pacateque","year":"2016","journal-title":"Rev. Colomb. De Cienc. Hort\u00edcolas"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Cavigliasso, P., Phifer, C.C., Adams, E.M., Flaspohler, D., Gennari, G.P., Licata, J.A., and Chacoff, N.P. (2020). Spatio-temporal dynamics of landscape use by the bumblebee Bombus pauloensis (Hymenoptera: Apidae) and its relationship with pollen provisioning. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0216190"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"8187","DOI":"10.1038\/s41598-021-87729-3","article-title":"Managed honeybees and South American bumblebees exhibit complementary foraging patterns in highbush blueberry","volume":"11","author":"Palottini","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1007\/s00114-006-0176-0","article-title":"Floral odor learning within the hive affects honeybees\u2019 foraging decisions","volume":"94","author":"Arenas","year":"2007","journal-title":"Naturwissenschaften"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1016\/j.anbehav.2012.01.026","article-title":"Learned olfactory cues affect pollen-foraging preferences in honeybees, Apis mellifera","volume":"83","author":"Arenas","year":"2012","journal-title":"Anim. Behav."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1101\/lm.38801","article-title":"Searching for the Memory Trace in a Mini-Brain, the Honeybee","volume":"8","author":"Menzel","year":"2001","journal-title":"Learn. Mem."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Palottini, F., Barcala, M.C.E., and Farina, W.M. (2018). Odor Learning and Its Experience-Dependent Modulation in the South American Native Bumblebee Bombus atratus (Hymenoptera: Apidae). Front. Psychol., 9.","DOI":"10.3389\/fpsyg.2018.00603"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1093\/cz\/zoaa073","article-title":"Classical olfactory conditioning promotes long-term memory and improves odor-cued flight orientation in the South American native bumblebee Bombus pauloensis","volume":"67","author":"Nery","year":"2021","journal-title":"Curr. Zool."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Pellettieri, J., and Farina, W.M. (2026). Combined nectar nonsugar compounds enhance bumblebee cognition. Sci. Rep.","DOI":"10.1038\/s41598-026-61182-6"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1080\/10635150801898912","article-title":"Historical Biogeography, Divergence Times, and Diversification Patterns of Bumble Bees (Hymenoptera: Apidae: Bombus)","volume":"57","author":"Hines","year":"2008","journal-title":"Syst. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1111\/j.1095-8312.2007.00784.x","article-title":"A comprehensive phylogeny of the bumble bees (Bombus): Bumble bee phylogeny","volume":"91","author":"Cameron","year":"2007","journal-title":"Biol. J. Linn. Soc."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1093\/aesa\/say031","article-title":"Ecology and Evolution of Cuckoo Bumble Bees","volume":"112","author":"Lhomme","year":"2019","journal-title":"Ann. Entomol. Soc. Am."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Farina, W.M., Arenas, A., Estravis-Barcala, M.C., and Palottini, F. (2023). Targeted crop pollination by training honey bees: Advances and perspectives. Front. Bee Sci., 1.","DOI":"10.3389\/frbee.2023.1253157"},{"key":"ref_16","unstructured":"Mackintosh, N.J. (1994). Animal Learning and Cognition. Handbook of Perception and Cognition, Academic Press. [2nd ed.]."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1007\/s00114-008-0465-x","article-title":"How floral odours are learned inside the bumblebee (Bombus terrestris) nest","volume":"96","author":"Molet","year":"2009","journal-title":"Naturwissenschaften"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1007\/s00040-008-1022-5","article-title":"Does pollen function as a reward for honeybees in associative learning?","volume":"55","author":"Arenas","year":"2008","journal-title":"Insectes Soc."},{"key":"ref_19","first-page":"2783","article-title":"Bees associate colour cues with differences in pollen rewards","volume":"217","author":"Nicholls","year":"2014","journal-title":"J. Exp. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.anbehav.2014.12.024","article-title":"Trading off short-term costs for long-term gains: How do bumblebees decide to learn morphologically complex flowers?","volume":"101","author":"Muth","year":"2015","journal-title":"Anim. Behav."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.anbehav.2015.09.029","article-title":"Bees remember flowers for more than one reason: Pollen mediates associative learning","volume":"111","author":"Muth","year":"2016","journal-title":"Anim. Behav."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1093\/beheco\/arv213","article-title":"Bees learn preferences for plant species that offer only pollen as a reward","volume":"27","author":"Russell","year":"2016","journal-title":"Behav. Ecol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/0022-1910(92)90117-V","article-title":"Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): Dependence on individual age and function","volume":"38","author":"Crailsheim","year":"1992","journal-title":"J. Insect Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"20252103","DOI":"10.1098\/rspb.2025.2103","article-title":"Flower constancy in pollinators: A bouquet of agendas shapes interactions among mutualistic partners","volume":"293","year":"2026","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_25","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":"ref_26","doi-asserted-by":"crossref","unstructured":"Nery, D., Palottini, F., and Farina, W.M. (2024). The South American Black Bumblebee (Bombus pauloensis) as a Potential Pollinator of Alfalfa (Medicago sativa). Agriculture, 14.","DOI":"10.3390\/agriculture14122192"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1006\/anbe.2000.1395","article-title":"Olfactory information transfer in the honeybee: Compared efficiency of classical conditioning and early exposure","volume":"59","author":"Sandoz","year":"2000","journal-title":"Anim. Behav."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/0031-9422(93)85502-I","article-title":"Floral scents\u2014A checklist of volatile compounds isolated by head-space techniques","volume":"33","author":"Knudsen","year":"1993","journal-title":"Phytochemistry"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1046\/j.1442-1984.1999.00014.x","article-title":"New Perspectives in Pollination Biology: Floral Fragrances. A day in the life of a linalool molecule: Chemical communication in a plant-pollinator system. Part 1: Linalool biosynthesis in flowering plants","volume":"14","author":"Raguso","year":"1999","journal-title":"Plant Species Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1111\/2041-210X.12584","article-title":"BORIS: A free, versatile open-source event-logging software for video\/audio coding and live observations","volume":"7","author":"Friard","year":"2016","journal-title":"Methods Ecol. Evol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/0022-1910(61)90060-9","article-title":"Classical conditioned response in the honey bee","volume":"6","author":"Takeda","year":"1961","journal-title":"J. Insect Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"20160333","DOI":"10.1098\/rspb.2016.0333","article-title":"Proline as a fuel for insect flight: Enhancing carbohydrate oxidation in hymenopterans","volume":"283","author":"Teulier","year":"2016","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_33","unstructured":"R Core Team (2026, August 29). R: The R Project for Statistical Computing. Available online: https:\/\/www.r-project.org\/."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2409","DOI":"10.1002\/sim.1047","article-title":"A solution to the problem of separation in logistic regression","volume":"21","author":"Heinze","year":"2002","journal-title":"Stat. Med."},{"key":"ref_35","unstructured":"Fox, J., Weisberg, S., and Price, B. (2026, August 29). car: Companion to Applied Regression, Version 3.1-5. Available online: https:\/\/CRAN.R-project.org\/package=car."},{"key":"ref_36","unstructured":"Piaskowski, J.L.R. (2026, August 29). emmeans: Estimated Marginal Means, Aka Least-Squares Means. R Package Version 2.0.3. Available online: https:\/\/rvlenth.github.io\/emmeans\/."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3139","DOI":"10.21105\/joss.03139","article-title":"Performance: An R Package for Assessment, Comparison and Testing of Statistical Models","volume":"6","author":"Patil","year":"2021","journal-title":"J. Open Source Softw."},{"key":"ref_38","unstructured":"Wickham, H., Fran\u00e7ois, R., Henry, L., M\u00fcller, K., Vaughan, D., and Posit Software, PBC (2026, August 29). dplyr: A Grammar of Data Manipulation. Available online: https:\/\/cran.r-project.org\/web\/packages\/dplyr\/index.html."},{"key":"ref_39","unstructured":"Bolker, B., Robinson, D., Menne, D., Gabry, J., Buerkner, P., Hua, C., Petry, W., Wiley, J., Kennedy, P., and Sz\u00f6cs, E. (2026, August 29). broom.mixed: Tidying Methods for Mixed Models. Available online: https:\/\/cran.r-project.org\/web\/packages\/broom.mixed\/index.html."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis, Springer. Available online: https:\/\/ggplot2.tidyverse.org.","DOI":"10.1007\/978-3-319-24277-4_9"},{"key":"ref_41","unstructured":"Elff, M. (2026, August 29). mclogit: Multinomial Logit Models for Categorical Responses and Discrete Choices. R Package Version 0.9.17.1. Available online: http:\/\/melff.github.io\/mclogit\/."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.lmot.2014.11.001","article-title":"Honeypot visitation enables scent learning and heightens forager response in bumblebees (Bombus impatiens)","volume":"50","author":"McAulay","year":"2015","journal-title":"Learn Motiv. Bee Insect Learn. Cogn."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1642","DOI":"10.1111\/ejn.12539","article-title":"Odor memories regulate olfactory receptor expression in the sensory periphery","volume":"39","author":"Claudianos","year":"2014","journal-title":"Eur. J. Neurosci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2879","DOI":"10.1093\/gbe\/evw202","article-title":"Identification of Complete Repertoire of Apis florea Odorant Receptors Reveals Complex Orthologous Relationships with Apis mellifera","volume":"8","author":"Karpe","year":"2016","journal-title":"Genome. Biol. Evol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"10823","DOI":"10.1038\/s41598-017-11098-z","article-title":"Computational genome-wide survey of odorant receptors from two solitary bees Dufourea novaeangliae (Hymenoptera: Halictidae) and Habropoda laboriosa (Hymenoptera: Apidae)","volume":"7","author":"Karpe","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"10947","DOI":"10.1038\/s41598-021-90400-6","article-title":"Olfactory coding in the antennal lobe of the bumble bee Bombus terrestris","volume":"11","author":"Mertes","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1051\/apido:2004001","article-title":"Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera)","volume":"35","author":"Scheiner","year":"2004","journal-title":"Apidologie"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3961","DOI":"10.1038\/s41598-019-40275-5","article-title":"Toxicity and neurophysiological impacts of plant essential oil components on bed bugs (Cimicidae: Hemiptera)","volume":"9","author":"Gaire","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1111\/j.1570-7458.2008.00683.x","article-title":"Start making scents: The challenge of integrating chemistry into pollination ecology","volume":"128","author":"Raguso","year":"2008","journal-title":"Entomol. Exp. Appl."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1111\/j.1365-2435.2009.01643.x","article-title":"Floral scent in a whole-plant context: Moving beyond pollinator attraction","volume":"23","author":"Raguso","year":"2009","journal-title":"Funct. Ecol."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/9\/924\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T17:19:02Z","timestamp":1788455942000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/9\/924"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,3]]},"references-count":50,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["insects17090924"],"URL":"https:\/\/doi.org\/10.3390\/insects17090924","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,3]]}}}