Honey Bee Nutrition

Current Knowledge, Challenges, and Future Research Directions

Authors

DOI:

https://doi.org/10.31285/AGRO.30.1818

Keywords:

colony nutritional supplementation, Eucalyptus grandis, landscape composition, nutritional value, pollen

Abstract

Honey bees (Apis mellifera) play a major ecological role since they are the main pollinators worldwide. In addition, these insects have been managed for commercial purposes for a long time due to the products obtained from their colonies. However, based on the number of published scientific studies, honey bee nutrition is a topic that has received increasing attention during the last years, likely due to land use intensification, which has decreased the diversity and/or quality of pollen available for honey bees, impacting their health. Moreover, there is an increase in inquiries from beekeepers regarding strategies to mitigate nutritional stress, suggesting that the information available is not enough. This gap might be related to the fact that honey bee nutrition is closely dependent on the environment in which the honey bees are. In this revision, we first review the information regarding honey bees' nutritional resources and requirements. Secondly, we analyze the flow of these nutritional resources within the honey bee colony and their effect at the individual and colony level. Thirdly, we analyze the impact of nutritional stress on honey bee colonies, explore the availability of strategies for colony supplementation, and discuss their effects on colonies' strength and productivity. Fourthly, we analyze the interaction between the infection level with pathogens and nutritional stress, considering the Eucalyptus grandis plantations, a common scenario in Uruguay in which those stressors interact. Finally, we aimed to identify research directions that could contribute to improving honey bee health through nutrition. Understanding the complex interactions between honey bee colonies, their environment and beekeeping management practices is key to achieving a sustainable productive activity.

Downloads

Download data is not yet available.

References

Alaux, C., Dantec, C., Parrinello, H., & Le Conte, Y. (2011). Nutrigenomics in honey bees: Digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees. BMC Genomics, 12, Article 496. https://doi.org/10.1186/1471-2164-12-496

Alaux, C., Ducloz, F., Crauser, D., & Le Conte, Y. (2010). Diet effects on honeybee immunocompetence. Biology Letters, 6(4), 562-565. https://doi.org/10.1098/rsbl.2009.0986

Al-Tikrity, W. S., Benton, A. W., Hillman, R. C., & Clarke, W. W. (1972). The relationship between the amount of unsealed brood in honeybee colonies and their pollen collection. Journal of Apicultural Research, 11(1), 9-12. https://doi.org/10.1080/00218839.1972.11099693

Alarcón, M., Castelli, L., Branchiccela, B., Invernizzi, C., & Antúnez, K. (2026). Mitigating the impacts of nutritional stress on honey bee colonies located in monoculture Eucalyptus plantations. Apidologie, 57, Article 7. https://doi.org/10.1007/s13592-025-01242-4

Amdam, G. V., & Omholt, S. W. (2002). The regulatory anatomy of honeybee lifespan. Journal of Theoretical Biology, 216(2), 209-228. https://doi.org/10.1006/jtbi.2002.2545

Amdam, G. V., & Omholt, S. W. (2003). The hive bee to forager transition in honeybee colonies: The double repressor hypothesis. Journal of Theoretical Biology, 223(4), 451-464. https://doi.org/10.1016/s0022-5193(03)00121-8

Amdam, G. V., Csondes, A., Fondrk, M. K., & Page, R. E., Jr. (2006). Complex social behaviour derived from maternal reproductive traits. Nature, 439(7072), 76-78. https://doi.org/10.1038/nature04340

Ament, S. A., Corona, M., Pollock, H. S., & Robinson, G. E. (2008). Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proceedings of the National Academy of Sciences of the United States of America, 105(11), 4226-4231. https://doi.org/10.1073/pnas.0800630105

Ament, S. A., Wang, Y., & Robinson, G. E. (2010). Nutritional regulation of division of labor in honey bees: Toward a systems biology perspective. Wiley Interdisciplinary Reviews Systems Biology and Medicine, 2(5), 566-576. https://doi.org/10.1002/wsbm.73

Amro, A., Omar, M., & Al-Ghamdi, A. (2016). Influence of different proteinaceous diets on consumption, brood rearing, and honey bee quality parameters under isolation conditions. Turkish Journal of Veterinary & Animal Sciences, 40(4), 468-475. https://doi.org/10.3906/vet-1507-28

Anderson, K. E., Carroll, M. J., Sheehan, T., Lanan, M. C., Mott, B. M., Maes, P., & Corby-Harris, V. (2014). Hive-stored pollen of honey bees: Many lines of evidence are consistent with pollen preservation, not nutrient conversion. Molecular Ecology, 23(23), 5904-5917. https://doi.org/10.1111/mec.12966

Anjos, O., Paula, V., Delgado, T., & Estevinho, L. (2019). Influence of the storage conditions on the quality of bee pollen. Zemdirbyste-Agriculture, 106(1), 87-94. https://doi.org/10.13080/z-a.2019.106.012

Anjum, S. I., Ullah, A., Gohar, F., Raza, G., Khan, M. I., Hameed, M., Ali, A., Chen, C. C., & Tlak Gajger, I. (2024). Bee pollen as a food and feed supplement and a therapeutic remedy: Recent trends in nanotechnology. Frontiers in Nutrition, 11, Article 1371672. https://doi.org/10.3389/fnut.2024.1371672

Antúnez, K., Anido, M., Branchiccela, B., Harriet, J., Campa, J., Invernizzi, C., Santos, E., Higes, M., Martín-Hernández, R., & Zunino, P. (2015). Seasonal variation of honeybee pathogens and its association with pollen diversity in Uruguay. Microbial Ecology, 70(2), 522-533. https://doi.org/10.1007/s00248-015-0594-7

Arenas, A., Lajad, R., & Farina, W. (2021). Selective recruitment for pollen and nectar sources in honeybees. The Journal of Experimental Biology, 224(16), Article jeb242683. https://doi.org/10.1242/jeb.242683

Arien, Y., Dag, A., & Shafir, S. (2018). Omega-6:3 ratio more than absolute lipid level in diet affects associative learning in honey bees. Frontiers in Psychology, 9, Article 1001. https://doi.org/10.3389/fpsyg.2018.01001

Arien, Y., Dag, A., Yona, S., Tietel, Z., Lapidot Cohen, T., & Shafir, S. (2020). Effect of diet lipids and omega-6:3 ratio on honey bee brood development, adult survival and body composition. Journal of Insect Physiology, 124, Article 104074. https://doi.org/10.1016/j.jinsphys.2020.104074

Arien, Y., Dag, A., Zarchin, S., Masci, T., & Shafir, S. (2015). Omega-3 deficiency impairs honey bee learning. Proceedings of the National Academy of Sciences of the United States of America, 112(51), 15761-15766. https://doi.org/10.1073/pnas.1517375112

Azzouz-Olden, F., Hunt, A., & DeGrandi-Hoffman, G. (2018). Transcriptional response of honey bee (Apis mellifera) to differential nutritional status and Nosema infection. BMC Genomics, 19(1), Article 628. https://doi.org/10.1186/s12864-018-5007-0

Babendreier, D., Kalberer, N., Romeis, J., Fluri, P., & Bigler, F. (2004). Pollen consumption in honey bee larvae: A step forward in the risk assessment of transgenic plants. Apidologie, 35, 293-300. https://doi.org/10.1051/apido:2004016

Badisco, L., Van Wielendaele, P., & Vanden Broeck, J. (2013). Eat to reproduce: A key role for the insulin signaling pathway in adult insects. Frontiers in Physiology, 4, Article 202. https://doi.org/10.3389/fphys.2013.00202

Baky, M. H., Abouelela, M. B., Wang, K., & Farag, M. A. (2023). Bee pollen and bread as a super-food: A comparative review of their metabolome composition and quality assessment in the context of best recovery conditions. Molecules (Basel), 28(2), Article 715. https://doi.org/10.3390/molecules28020715

Barker, R. J. (1977). Considerations in selecting sugars for feeding to honey bees. American Bee Journal, 117, 76-77.

Black, J. L. (2006). Honeybee nutrition: Review of research and practices: A report for the Rural Industries Research and Development Corporation. RIRDC.

Bogdanov, S., Haldimann, M., Luginbühl, W., & Gallmann, P. (2007). Minerals in honey: Environmental, geographical and botanical aspects. Journal of Apicultural Research, 46(4), 269-275. https://doi.org/10.1080/00218839.2007.11101407

Bonvehí, J. S., & Jordà, R. E. (1997). Nutrient composition and microbiological quality of honeybee-collected pollen in Spain. Journal of Agricultural and Food Chemistry, 45(3), 725-732. https://doi.org/10.1021/jf960265q

Bordenstein, S. R., & Theis, K. R. (2015). Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biology, 13(8), Article e1002226. https://doi.org/10.1371/journal.pbio.1002226

Botías, C., Martín-Hernández, R., Barrios, L., Meana, A., & Higes, M. (2013). Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Veterinary Research, 44(1), Article 25. https://doi.org/10.1186/1297-9716-44-25

Branchiccela, B. (2020). Rol de la nutrición de la abeja Apis mellifera en la infección con los patógenos de mayor importancia apícola [Doctoral dissertation, Universidad de la República]. Colibri. https://hdl.handle.net/20.500.12008/30745

Branchiccela, B., Antúnez, K., Invernizzi, C., & Coll, F. (2020). Apicultura en montes de Eucalyptus spp. Revista INIA, (62), 60-72. https://ainfo.inia.uy/digital/bitstream/item/14737/1/Revista-INIA-62-Setiembre-2020-p-60-72.pdf

Branchiccela, B., Castelli, L., Corona, M., Díaz-Cetti, S., Invernizzi, C., Martínez de la Escalera, G., Mendoza, Y., Santos, E., Silva, C., Zunino, P., & Antúnez, K. (2019). Impact of nutritional stress on the honeybee colony health. Scientific Reports, 9(1), Article 10156. https://doi.org/10.1038/s41598-019-46453-9

Branchiccela, B., Castelli, L., Díaz-Cetti, S., Invernizzi, C., Mendoza, Y., Santos, E., Silva, C., Zunino, P., & Antúnez, K. (2023). Can pollen supplementation mitigate the impact of nutritional stress on honey bee colonies? Journal of Apicultural Research, 62(2), 294-302. https://doi.org/10.1080/00218839.2021.1888537

Brodschneider, R., & Crailsheim, K. (2010). Nutrition and health in honey bees. Apidologie, 41(3), 278-294. https://doi.org/10.1051/apido/2010012

Brooker, M. I. H. (2000). A new classification of the genus Eucalyptus L’Hér. (Myrtaceae). Australian Systematic Botany, 13(1), 79-148. https://doi.org/10.1071/SB98008

Camazine, S., Crailsheim, K., Hrassnigg, N., Robinson, G. E., Leonhard, B., & Kropiunigg, H. (1998). Protein trophallaxis and the regulation of pollen foraging by honey bees (Apis mellifera L.). Apidologie, 29, 113-126. https://doi.org/10.1051/apido:19980107

Cappellari, A., Malagnini, V., Fontana, P., Zanotelli, L., Tonidandel, L., Angeli, G., Ioriatti, C., & Marini, L. (2024). Impact of landscape composition on honey bee pollen contamination by pesticides: A multi-residue analysis. Chemosphere, 349, Article 140829. https://doi.org/10.1016/j.chemosphere.2023.140829

Carroll, M. J., Brown, N., Goodall, C., Downs, A. M., Sheenan, T. H., & Anderson, K. E. (2017). Honey bees preferentially consume freshly-stored pollen. PloS One, 12(4), Article e0175933. https://doi.org/10.1371/journal.pone.0175933

Castelli, L., Branchiccela, B., Garrido, M., Invernizzi, C., Porrini, M., Romero, H., Santos, E., Zunino, P., & Antúnez, K. (2020). Impact of nutritional stress on honeybee gut microbiota, immunity, and nosema ceranae Infection. Microbial Ecology, 80(4), 908-919. https://doi.org/10.1007/s00248-020-01538-1

Charistos, L., Parashos, N., & Hatjina, F. (2015). Long term effects of a food supplement HiveAliveTM on honey bee colony strength and Nosema ceranae spore counts. Journal of Apicultural Research, 54(5), 420-426. https://doi.org/10.1080/00218839.2016.1189231

Chen, Y., Evans, J., & Feldlaufer, M. (2006). Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. Journal of Invertebrate Pathology, 92(3), 152-159. https://doi.org/10.1016/j.jip.2006.03.010

Cilia, G., Garrido, C., Bonetto, M., Tesoriero, D., & Nanetti, A. (2020). Effect of Api-Bioxal® and ApiHerb® treatments against Nosema ceranae infection in Apis mellifera Investigated by two qPCR methods. Veterinary Sciences, 7(3), Article 125. https://doi.org/10.3390/vetsci7030125

Clermont, A., Eickermann, M., Kraus, F., Hoffmann, L., & Beyer, M. (2015). Correlations between land covers and honey bee colony losses in a country with industrialized and rural regions. The Science of the Total Environment, 532, 1-13. https://doi.org/10.1016/j.scitotenv.2015.05.128

Cook, S. M., Sandoz, J. C., Martin, A. P., Murray, D. A., Poppy, G. M., & Williams, I. H. (2005). Could learning of pollen odours by honey bees (Apis mellifera) play a role in their foraging behaviour? Physiological Entomology, 30, 164-174. https://doi.org/10.1111/j.1365-3032.2005.00445.x

Corby-Harris, V., Snyder, L., Meador, C., & Ayotte, T. (2018). Honey bee (Apis mellifera) nurses do not consume pollens based on their nutritional quality. PloS One, 13(1), Article e0191050. https://doi.org/10.1371/journal.pone.0191050

Corona, M., Branchiccela, B., Alburaki, M., Palmer-Young, E. C., Madella, S., Chen, Y., & Evans, J. D. (2023). Decoupling the effects of nutrition, age, and behavioral caste on honey bee physiology, immunity, and colony health. Frontiers in Physiology, 14, Article 1149840. https://doi.org/10.3389/fphys.2023.1149840

Corona, M., Libbrecht, R., & Wheeler, D. E. (2016). Molecular mechanisms of phenotypic plasticity in social insects. Current Opinion in Insect Science, 13, 55-60. https://doi.org/10.1016/j.cois.2015.12.003

Corona, M., Velarde, R. A., Remolina, S., Moran-Lauter, A., Wang, Y., Hughes, K. A., & Robinson, G. E. (2007). Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences of the United States of America, 104(17), 7128-7133. https://doi.org/10.1073/pnas.0701909104

Crailsheim, K. (1988). Regulation of food passage in the intestine of the honeybee. Journal of Insect Physiology, 34(2), 85-90. https://doi.org/10.1016/0022-1910(88)90158-8

Crailsheim, K. (1998). Trophallactic interactions in the adult honeybee (Apis mellifera L.). Apidologie, 29, 97-112. https://doi.org/10.1051/apido:19980106

Crailsheim, K., Schneider, L. H. W., Hrassnigg, N., Buhlmann, G., Brosch, U., Gmeinbauer, R., Schöffmann, B. (1992). Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): Dependence on individual age and function. Journal of Insect Physiology, 38(6), 409-419. https://doi.org/10.1016/0022-1910(92)90117-V

Cremonez, T. M., De Jong, D., & Bitondi, M. M. G. (1998). Quantification of hemolymph proteins as a fast method for testing protein diets for honey bees (Hymenoptera: Apidae). Journal of Economic Entomology, 91(6), 1284-1289. https://doi.org/10.1093/jee/91.6.1284

Danihlík, J., Škrabišová, M., Lenobel, R., Šebela, M., Omar, E., Petřivalský, M., Crailsheim, K., & Brodschneider, R. (2018). Does the pollen diet influence the production and expression of antimicrobial peptides in individual honey bees? Insects, 9(3), Article 79. https://doi.org/10.3390/insects9030079

Day, S., Beyer, R., Mercer, A., & Ogden, S. (1990). The nutrient composition of honeybee-collected pollen in Otago, New Zealand. Journal of Apicultural Research, 29(3), 138-146. https://doi.org/10.1080/00218839.1990.11101210

de Groot, A. P. (1953). Protein and amino acid requirements of the honeybee. Physiologia Comparata et Oecologia, 3, 197-285.

DeGrandi-Hoffman, G., Chen, Y., Huang, E., & Huang, M. H. (2010). The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). Journal of Insect Physiology, 56(9), 1184-1191. https://doi.org/10.1016/j.jinsphys.2010.03.017

DeGrandi-Hoffman, G., Chen, Y., Rivera, R., Carroll, M., Chambers, M., & Hidalgo, G. (2016). Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements. Apidologie, 47(2), 186-196. https://doi.org/10.1007/s13592-015-0386-6

DeGrandi-Hoffman, G., Corby-Harris, V., Carroll, M., Toth, A. L., Gage, S., Watkins deJong, E., Graham, H., Chambers, M., Meador, C., & Obernesser, B. (2021). The importance of time and place: Nutrient composition and utilization of seasonal pollens by European honey bees (Apis mellifera L.). Insects, 12(3), Article 235. https://doi.org/10.3390/insects12030235

DeGrandi-Hoffman, G., Corby-Harris, V., Chen, Y., Graham, H., Chambers, M., Watkins deJong, E., Ziolkowski, N., Kang, Y., Gage, S., Deeter, M., Simone-Finstrom, M., & de Guzman, L. (2020). Can supplementary pollen feeding reduce varroa mite and virus levels and improve honey bee colony survival? Experimental & Applied Acarology, 82(4), 455-473. https://doi.org/10.1007/s10493-020-00562-7

DeGrandi-Hoffman, G., Gage, S. L., Corby-Harris, V., Carroll, M., Chambers, M., Graham, H., Watkins deJong, E., Hidalgo, G., Calle, S., Azzouz-Olden, F., Meador, C., Snyder, L., & Ziolkowski, N. (2018). Connecting the nutrient composition of seasonal pollens with changing nutritional needs of honey bee (Apis mellifera L.) colonies. Journal of Insect Physiology, 109, 114-124. https://doi.org/10.1016/j.jinsphys.2018.07.002

Descamps, C., Boubnan, N., Jacquemart, A. L., & Quinet, M. (2021). Growing and flowering in a changing climate: Effects of higher temperatures and drought stress on the bee-pollinated species Impatiens glandulifera Royle. Plants (Basel), 10(5), Article 988. https://doi.org/10.3390/plants10050988

Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L. P., Decourtye, A., Kretzschmar, A., Suchail, S., Brunet, J. L., & Alaux, C. (2013). Influence of pollen nutrition on honey bee health: Do pollen quality and diversity matter? PloS One, 8(8), Article e72016. https://doi.org/10.1371/journal.pone.0072016

Dolezal, A. G., Carrillo-Tripp, J., Miller, W. A., Bonning, B. C., & Toth, A. L. (2016). Intensively cultivated landscape and varroa mite infestation are associated with reduced honey bee nutritional state. PloS One, 11(4), Article e0153531. https://doi.org/10.1371/journal.pone.0153531

Doner, L. W. (1977). The sugars of honey: A review. Journal of the Science of Food and Agriculture, 28(5), 443-456. https://doi.org/10.1002/jsfa.2740280508

Donkersley, P., Rhodes, G., Pickup, R. W., Jones, K. C., & Wilson, K. (2014). Honeybee nutrition is linked to landscape composition. Ecology and Evolution, 4(21), 4195-4206. https://doi.org/10.1002/ece3.1293

Dreller, C., & Tarpy, D. R. (2000). Perception of the pollen need by foragers in a honeybee colony. Animal Behaviour, 59(1), 91-96. https://doi.org/10.1006/anbe.1999.1303

Fewell, J. H., & Winston, M. L. (1992). Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behavioral Ecology and Sociobiology, 30, 387-393. https://doi.org/10.1007/BF00176173

Flores, J. M., Gutiérrez, I., & Espejo, R. (2005). The role of pollen in chalkbrood disease in Apis mellifera: Transmission and predisposing conditions. Mycologia, 97(6), 1171-1176. https://doi.org/10.3852/mycologia.97.6.1171

Food and Agriculture Organization of the United Nations & World Health Organization. (2019). Codex standard for honey (CODEX STAN 12–1981, Rev. 2001, Amd. 2022). Codex Alimentarius Commission. https://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https://workspace.fao.org/sites/codex/Standards/CXS%2B12-1981/CXS_012e.pdf

Free, J. B., & Williams, I. H. (1971). The effect of giving pollen and pollen supplement to honeybee colonies on the amount of pollen collected. Journal of Apicultural Research, 10(2), 87-90. https://doi.org/10.1080/00218839.1971.11099676

Frigero, M. L. P., Boaro, C. S. F., Galetto, L., Tunes, P., & Guimarães, E. (2025). Extreme events induced by climate change alter nectar offer to pollinators in cross pollination-dependent crops. Scientific Reports, 15(1), Article 10852. https://doi.org/10.1038/s41598-025-94565-2

García-Vicente, E. J., Martín, M., Rey-Casero, I., Pérez, A., Martín, J., García, A., Alonso, J. M., & Risco, D. (2024). Effects of feeding with a protein liquid supplement on productivity, mortality and health of Apis mellifera hives in southwestern Spain. Research in Veterinary Science, 169, Article 105173. https://doi.org/10.1016/j.rvsc.2024.105173

Garrido, P. M., Porrini, M. P., Alberoni, D., Baffoni, L., Scott, D., Mifsud, D., Eguaras, M. J., & Di Gioia, D. (2024). Beneficial bacteria and plant extracts promote honey bee health and reduce nosema ceranae infection. Probiotics and Antimicrobial Proteins, 16(1), 259-274. https://doi.org/10.1007/s12602-022-10025-7

Giampieri, F., Quiles, J. L., Cianciosi, D., Forbes-Hernández, T. Y., Orantes-Bermejo, F. J., Alvarez-Suarez, J. M., & Battino, M. (2022). Bee products: An emblematic example of underutilized sources of bioactive compounds. Journal of Agricultural and Food Chemistry, 70(23), 6833-6848. https://doi.org/10.1021/acs.jafc.1c05822

Gilliam, M. (1979). Microbiology of pollen and bee bread: The yeasts. Apidologie, 10(1), 43-53. https://doi.org/10.1051/apido:19790106

Gilliam, M., & Bee, C. H. (1979). Microbiology of pollen and bee bread: The genus Bacillus. Apidologie, 10, 269-274. https://doi.org/10.1051/apido:19790304

Goulson, D., Nicholls, E., Botías, C., & Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229), Article 1255957. https://doi.org/10.1126/science.1255957

Guidugli, K. R., Nascimento, A. M., Amdam, G. V., Barchuk, A. R., Omholt, S., Simões, Z. L., & Hartfelder, K. (2005). Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Letters, 579(22), 4961-4965. https://doi.org/10.1016/j.febslet.2005.07.085

Haszonits, O., & Crailsheim, K. (1990). Uptake of L-leucine into isolated enterocytes of the honeybee (Apis mellifera L.) depending on season. Journal of Insect Physiology, 36(11), 835-842. https://doi.org/10.1016/0022-1910(90)90170-K

Haydak, M. H. (1945). Value of pollen substitutes for brood rearing of honeybees. Journal of Economic Entomology, 38(4), 484-487. https://doi.org/10.1093/jee/38.4.484

Haydak, M. H. (1970). Honey bee nutrition. Annual Review Entomology, 15,143-156. https://doi.org/10.1146/annurev.en.15.010170.001043

Haydak, M. H., & Tanquary, M. C. (1943). Pollen and pollen substitutes in the nutrition of the honeybee. University of Minnesota.

Herbert, E. W., & Miller-Ihli, N. J. (1987). Seasonal variation of seven minerals in honey bee-collected pollen. American Bee Journal, 127(5), 367-369.

Herbert, E. W., Jr., & Shimanuki, H. (1978). Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie, 9, 33-40. https://doi.org/10.1051/apido:19780103

Higes, M., Meana, A., Bartolomé, C., Botías, C., & Martín-Hernández, R. (2013). Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environmental Microbiology Reports, 5(1), 17-29. https://doi.org/10.1111/1758-2229.12024

Hrassnigg, N., & Crailsheim, K. (2005). Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie, 36, 255-277. https://doi.org/10.1051/apido:2005015

Hsu, P. S., Wu, T. H., Huang, M. Y., Wang, D. Y., & Wu, M. C. (2021). Nutritive value of 11 bee pollen samples from major floral sources in Taiwan. Foods (Basel), 10(9), Article 2229. https://doi.org/10.3390/foods10092229

Invernizzi, C., Branchiccela, B., Mendoza, Y., Castelli, L., Viera, N., Santos, E., Díaz-Cetti, S., & Antúnez, K. (2023). Apicultura en forestaciones de eucaliptos: Una oportunidad con muchos problemas a resolver. In A. Brazeiro (Ed.), Biodiversidad en paisajes forestados en Uruguay (pp. 155-175). CSIC. https://hdl.handle.net/20.500.12008/47650

Invernizzi, C., Santos, E., García, E., Daners, G., Di Landro, R., Saadoun, A., & Cabrera, C. (2011). Sanitary and nutritional characterization of honeybee colonies in Eucalyptus grandis plantations. Archivos de Zootecnia, 60(232), 1303-1314. https://dx.doi.org/10.4321/S0004-05922011000400045

Johansson, T. S. K., & Johansson, M. P. (1977). Feeding honeybees pollen and pollen substitutes. Bee World, 58(3), 105-118. https://doi.org/10.1080/0005772X.1977.11097658

Johnson, B. R. (2010). Division of labor in honeybees: Form, function, and proximate mechanisms. Behavioral Ecology and Sociobiology, 64(3), 305-316. https://doi.org/10.1007/s00265-009-0874-7

Johnson, K. D. (2000). Systematic studies in the eucalypts: 10. New tropical and subtropical eucalypts from Australia and New Guinea (Eucalyptus, Myrtaceae). Telopea, 8(4), 503-540. https://doi.org/10.7751/telopea20002007

Juri, P., Nogueira, E., Salvarrey, S., Branchiccela, B., Mendoza, Y., Bonora, E., & Invernizzi, C. (2025). Honey bees colonies in Eucalyptus grandis plantation: when the excess of nectar and pollen limits the queen’s oviposition. Journal of Apicultural Research. Advance online publication. https://doi.org/10.1080/00218839.2025.2483012

Kapahi, P., Chen, D., Rogers, A. N., Katewa, S. D., Li, P. W., Thomas, E. L., & Kockel, L. (2010). With TOR, less is more: A key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metabolism, 11(6), 453-465. https://doi.org/10.1016/j.cmet.2010.05.001

Kleinschmidt, G. J. (1976). Influence of crude protein levels on colony production in relation to the pollen nutrition of Apis mellifera. The Australasian Beekeeper, 78, 36-39.

Knapp, J. L., Nicholson, C. C., Jonsson, O., de Miranda, J. R., & Rundlöf, M. (2023). Ecological traits interact with landscape context to determine bees' pesticide risk. Nature Ecology & Evolution, 7(4), 547-556. https://doi.org/10.1038/s41559-023-01990-5

Lamontagne-Drolet, M., Samson-Robert, O., Giovenazzo, P., & Fournier, V. (2019). The impacts of two protein supplements on commercial honey bee (Apis mellifera L.) colonies. Journal of Apicultural Research, 58(5), 800-813. https://doi.org/10.1080/00218839.2019.1644938

Leoncini, I., Le Conte, Y., Costagliola, G., Plettner, E., Toth, A. L., Wang, M., Huang, Z., Bécard, J. M., Crauser, D., Slessor, K. N., & Robinson, G. E. (2004). Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proceedings of the National Academy of Sciences of the United States of America, 101(50), 17559-17564. https://doi.org/10.1073/pnas.0407652101

Leonhardt, S. D., Blüthgen, N., & Leonhardt, S. D. (2012). The same, but different: Pollen foraging in honeybee and bumblebee colonies. Apidologie, 43(4), 449-464. https://doi.org/10.1007/s13592-011-0112-y

Maes, P. W., Rodrigues, P. A., Oliver, R., Mott, B. M., & Anderson, K. E. (2016). Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Molecular Ecology, 25(21), 5439-5450. https://doi.org/10.1111/mec.13862

Manning, R. (2001a). Fatty acids in pollen: A review of their importance for honey bees. Bee World, 82(2), 60-75. https://doi.org/10.1080/0005772X.2001.11099504

Manning, R. (2001b). Pollen analysis of eucalypts in western Australia. RIRDC. https://agrifutures.com.au/wp-content/uploads/publications/01-053.pdf

Manning, R. (2018). Artificial feeding of honeybees based on an understanding of nutritional principles. Animal Production Science, 58, 689-703. https://doi.org/10.1071/AN15814

Manning, R., & Harvey, M. (2002). Fatty acids in honeybee-collected pollens from six endemic Western Australian eucalypts and the possible significance to the Western Australian beekeeping industry. Australian Journal of Experimental Agriculture, 42(2), 217-223. https://doi.org/10.1071/EA00160

Marco Antonio, D. S., Guidugli-Lazzarini, K. R., do Nascimento, A. M., Simões, Z. L., & Hartfelder, K. (2008). RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Die Naturwissenschaften, 95(10), 953-961. https://doi.org/10.1007/s00114-008-0413-9

Matilla, H. R., & Otis, G. W. (2006). The effects of pollen availability during larval development on the behaviour and physiology of spring-reared honey bee workers. Apidologie, 37(5), 533-546. https://doi.org/10.1051/apido:2006037

Mendoza, Y., Antúnez, K., Branchiccela, B., Anido, M., Santos, E., & Invernizzi, C. (2014). Nosema ceranae and RNA viruses in European and Africanized honeybee colonies (Apis mellifera) in Uruguay. Apidologie, 45(2), 224-234. https://doi.org/10.1007/s13592-013-0241-6

Mendoza, Y., Díaz, S., Ramallo, G., & Invernizzi, C. (2012). Incidencia de Nosema ceranae durante el invierno en colonias de abejas melíferas retiradas de una forestación de Eucalyptus grandis. Veterinaria (Montevideo), 48(188), 13-18. https://www.revistasmvu.com.uy/index.php/smvu/article/view/209

Michalczyk, M., Sokol, R., & Koziatek, S. (2016). Evaluation of the effectiveness of selected treatments of Nosema spp. infections by the homecytometric method and duplex PCR. Acta Veterinaria Beograd, 66(1), 115-124. https://doi.org/10.1515/acve-2016-0009

Moayed Saffari, A. (2008). Effects of feeding honeybees with pollen substitutes and natural pollen on brood rearing, population, and honey production [Master’s thesis, University of Guelph]. University of Guelph. https://hdl.handle.net/10214/22232

Moritz, B., & Crailsheim, K. (1987). Physiology of protein digestion in the midgut of the honeybee (Apis mellifera L.). Journal of Insect Physiology, 33(12), 923-931. https://doi.org/10.1016/0022-1910(87)90004-7

Mortensen, A. N., Jack, C. J., Bustamante, T. A., Schmehl, D. R., & Ellis, J. D. (2019). Effects of supplemental pollen feeding on honey bee (Hymenoptera: Apidae) colony strength and Nosema spp. infection. Journal of Economic Entomology, 112(1), 60-66. https://doi.org/10.1093/jee/toy341

Motta, E. V. S., & Moran, N. A. (2024). The honeybee microbiota and its impact on health and disease. Nature Reviews Microbiology, 22(3), 122-137. https://doi.org/10.1038/s41579-023-00990-3

Nässel, D. R., & Vanden Broeck, J. (2016). Insulin/IGF signaling in Drosophila and other insects: Factors that regulate production, release and post-release action of the insulin-like peptides. Cellular and Molecular Life Sciences, 73(2), 271-290. https://doi.org/10.1007/s00018-015-2063-3

Naug, D. (2009). Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation, 142(10), 2369-2372. https://doi.org/10.1016/j.biocon.2009.04.007

Nielsen, N., Grommer, J., & Lunden, R. (1955). Investigations on the chemical composition of pollen from some plants. Acta Chemica Scandinavica, 9(7), 1100-1106.

Noordyke, E. R., & Ellis, J. D. (2021). Reviewing the efficacy of pollen substitutes as a management tool for improving the health and productivity of western honey bee (Apis mellifera) colonies. Frontiers in Sustainable Food Systems, 5, Article 772897. https://doi.org/10.3389/fsufs.2021.772897

Oertel, E. (1980). History of beekeeping in the United States. In Beekeeping in the United States (pp. 2-9). USDA.

Oroian, M., Dranca, F., & Ursachi, F. (2022). Characterization of Romanian bee pollen-an important nutritional source. Foods (Basel), 11(17), Article 2633. https://doi.org/10.3390/foods11172633

Pankiw, T., Page, R. E., & Fondrk, M. K. (1998). Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behavioral Ecology and Sociobiology, 44, 193-198. https://doi.org/10.1007/s002650050531

Pavlin, A., Marinč, A., & Prešern, J. (2025). Go with the flow: A case study of migratory beekeeping and its associated costs. Journal of Economic Entomology, 118(4), 1485-1494. https://doi.org/10.1093/jee/toaf119

Peirson, M., Ibrahim, A., Ovinge, L. P., Hoover, S. E., Guarna, M. M., Melathopoulos, A., & Pernal, S. F. (2024). The effects of protein supplementation, fumagillin treatment, and colony management on the productivity and long-term survival of honey bee (Apis mellifera) colonies. PloS One, 19(3), Article e0288953. https://doi.org/10.1371/journal.pone.0288953

Pernal, S., & Currie, R. (2000). Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees. Apidologie, 31, 387-409. https://doi.org/10.1051/apido:2000130

Pernal, S. F., & Currie, R. W. (2001). The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behavioral Ecology and Sociobiology, 51(1), 53-68. https://doi.org/10.1007/s002650100412

Phillips, B. B., Shaw, R. F., Holland, M. J., Fry, E. L., Bardgett, R. D., Bullock, J. M., & Osborne, J. L. (2018). Drought reduces floral resources for pollinators. Global Change Biology, 24(7), 3226-3235. https://doi.org/10.1111/gcb.14130

Pilati, L., & Prestamburgo, M. (2016). Sequential relationship between profitability and sustainability: The case of migratory beekeeping. Sustainability, 8(1), Article 94. https://doi.org/10.3390/su8010094

Pita-Calvo, C., & Vázquez, M. (2017). Differences between honeydew and blossom honeys: A review. Trends in Food Science & Technology, 59, 79-87. https://doi.org/10.1016/j.tifs.2016.11.015

Powell, J. E., Martinson, V. G., Urban-Mead, K., & Moran, N. A. (2014). Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Applied and Environmental Microbiology, 80(23), 7378-7387. https://doi.org/10.1128/AEM.01861-14

Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., Lim, D., Joklik, J., Cicero, J. M., Ellis, J. D., Hawthorne, D., & vanEngelsdorp, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences of the United States of America, 116(5), 1792-1801. https://doi.org/10.1073/pnas.1818371116

Raymann, K., & Moran, N. A. (2018). The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science, 26, 97-104. https://doi.org/10.1016/j.cois.2018.02.012

Ricigliano, V. A., Williams, S. T., & Oliver, R. (2022). Effects of different artificial diets on commercial honey bee colony performance, health biomarkers, and gut microbiota. BMC Veterinary Research, 18(1), Article 52. https://doi.org/10.1186/s12917-022-03151-5

Robinson, G. E. (1992). Regulation of division of labor in insect societies. Annual Review of Entomology, 37, 637-665. https://doi.org/10.1146/annurev.en.37.010192.003225

Rotjan, R. D., Calderone, N. W., & Seeley, T. D. (2002). How a honey bee colony mustered additional labor for the task of pollen foraging. Apidologie, 33(4), 367-373. https://doi.org/10.1051/apido:2002026

Roulston, T. H., & Cane, J. H. (2000). Pollen nutritional content and digestibility for animals. Plant Systematics and Evolution, 222, 187-209. https://doi.org/10.1007/BF00984102

Rudelli, C., Galuppi, R., Cabbri, R., Dalmonte, T., Fontanesi, L., Andreani, G., & Isani, G. (2024). Field application of an innovative approach to assess honeybee health and nutritional status. Animals, 14(15), Article 2183. https://doi.org/10.3390/ani14152183

Ruedenauer, F. A., Wöhrle, C., Spaethe, J., & Leonhardt, S. D. (2018). Do honeybees (Apis mellifera) differentiate between different pollen types? PloS One, 13(11), Article e0205821. https://doi.org/10.1371/journal.pone.0205821

Santos, E., Invernizzi, C., García, E., Cabrera, C., Di Landro, R., Saadoun, A., & Daners, G. (2009). Contenido de proteína cruda del polen de las principales especies botánicas utilizadas por las abejas melíferas en Uruguay. Agrociencia Uruguay, 13(2), 9-13. https://doi.org/10.31285/AGRO.13.714

Saraiva, M. A., Zemolin, A. P., Franco, J. L., Boldo, J. T., Stefenon, V. M., Triplett, E. W., de Oliveira Camargo, F. A., & Roesch, L. F. (2015). Relationship between honeybee nutrition and their microbial communities. Antonie van Leeuwenhoek, 107(4), 921-933. https://doi.org/10.1007/s10482-015-0384-8

Schmehl, D. R., Teal, P. E., Frazier, J. L., & Grozinger, C. M. (2014). Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera). Journal of Insect Physiology, 71, 177-190. https://doi.org/10.1016/j.jinsphys.2014.10.002

Schmickl, T., & Crailsheim, K. (2004). Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply. Apidologie, 35, 249-263. https://doi.org/10.1051/apido:2004019

Schmidt, J. O., Thoenes, S. C., & Levin, M. D. (1987). Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Annals of the Entomological Society of America, 80, 176-183. https://doi.org/10.1093/aesa/80.2.176

Schulz, D. J., Huang, Z. Y., & Robinson, G. E. (1998). Effects of colony food shortage on behavioral development in honey bees. Behavioral Ecology and Sociobiology, 42(5), 295-303. https://doi.org/10.1007/s002650050442

Simopoulos, A. P. (2002). The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomedicine & Pharmacotherapy, 56(8), 365-379. https://doi.org/10.1016/s0753-3322(02)00253-6

Simopoulos, A. P. (2008). The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Experimental Biology and Medicine, 233(6), 674-688. https://doi.org/10.3181/0711-MR-311

Singh, S., Saini, K., & Jain, K. L. (1999). Quantitative comparison of lipids in some pollens and their phagostimulatory effects in honey bees. Journal of Apicultural Research, 38(1-2), 87-92. https://doi.org/10.1080/00218839.1999.11100999

Smart, M. D., Pettis, J. S., Euliss, N., & Spivak, M. S. (2016). Land use in the Northern Great Plains region of the U.S. influences the survival and productivity of honey bee colonies. Agriculture, Ecosystems & Environment, 230, 139-149. https://doi.org/10.1016/j.agee.2016.05.030

Smart, M., Pettis, J., Rice, N., Browning, Z., & Spivak, M. (2016). Linking measures of colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use. PloS One, 11(3), Article e0152685. https://doi.org/10.1371/journal.pone.0152685

Somerville, D. (2000). Honey bee nutrition and supplementary feeding. NSW Agriculture.

Somerville, D. C. (2001). Nutritional value of bee collected pollens: A report for the Rural Industries Research and Development Corporation. RIRDC. https://www.nbba.ca/wp-content/uploads/2013/12/Nutritional_Value_of_Bee_Collected_Pollens.pdf

Somerville, D. C., & Nicol, H. I. (2006). Crude protein and amino acid composition of honey bee-collected pollen pellets from south-east Australia and a note on laboratory disparity. Australian Journal of Experimental Agriculture, 46(1), 141-149. https://doi.org/10.1071/EA03188

South, W., Nicolle, D., & Phillips, G. P. (2024). The identity and taxonomic status of the rare Angophora/Eucalyptus exul (Myrtaceae) from the Northern Tablelands of New South Wales. Telopea, 27, 197-201. https://doi.org/10.7751/telopea19867

Spencer-Booth, Y. (1960). Feeding pollen, pollen substitutes and pollen supplements to honeybees. Bee World, 41(10), 253-263. https://doi.org/10.1080/0005772X.1960.11096810

Stanley, R. G., & Linskens, H. F. (1974). Carbohydrates and cell walls. In Robert G. Stanley & H. F. Linskens (Eds.), Pollen: Biology, biochemistry, management (pp. 129-144). Springer. https://doi.org/10.1007/978-3-642-65905-8_9

Steinmann, N., Corona, M., Neumann, P., & Dainat, B. (2015). Overwintering is associated with reduced expression of immune genes and higher susceptibility to virus infection in honey bees. PloS One, 10(6), Article e0129956. https://doi.org/10.1371/journal.pone.0129956

Tapia-Rivera, J. C., Tapia-González, J. M., Alburaki, M., Chan, P., Sánchez-Cordova, R., Macías-Macías, J. O., & Corona, M. (2025). The effects of artificial diets containing free amino acids versus intact proteins on biomarkers of nutrition and deformed wing virus levels in the honey bee. Insects, 16(4), Article 375. https://doi.org/10.3390/insects16040375

Thakur, M., & Nanda, V. (2020). Composition and functionality of bee pollen: A review. Trends in Food Science & Technology, 98, 82-106. https://doi.org/10.1016/j.tifs.2020.02.001

Toth, A. L., & Robinson, G. E. (2005). Worker nutrition and division of labour in honeybees. Animal Behaviour, 69(2), 427-435. https://doi.org/10.1016/j.anbehav.2004.03.017

Toth, A. L., Kantarovich, S., Meisel, A. F., & Robinson, G. E. (2005). Nutritional status influences socially regulated foraging ontogeny in honey bees. The Journal of Experimental Biology, 208(Pt 24), 4641-4649. https://doi.org/10.1242/jeb.01956

Tsuruda, J. M., Chakrabarti, P., & Sagili, R. R. (2021). Honey bee nutrition. The Veterinary Clinics of North America Food Animal Practice, 37(3), 505-519. https://doi.org/10.1016/j.cvfa.2021.06.006

Van Bilsen, D. G. J. L., van Roekel, T., & Hoekstra, F. A. (1994). Declining viability and lipid degradation during pollen storage. Sexual Plant Reproduction, 7(5), 303-310. https://doi.org/10.1007/BF00227714

Vaudo, A. D., Patch, H. M., Mortensen, D. A., Tooker, J. F., & Grozinger, C. M. (2016). Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of the National Academy of Sciences of the United States of America, 113(28), E4035-E4042. https://doi.org/10.1073/pnas.1606101113

Vaughan, D. M., & Calderone, N. W. (2002). Assessment of pollen stores by foragers in colonies of the honey bee, Apis mellifera L. Insectes Sociaux, 49(1), 23-27. https://doi.org/10.1007/s00040-002-8273-3

Viera López, N. (2021). Administración de polen polifloral como estrategia para mejorar la salud y productividad de colonias de abejas melíferas [Master’s thesis, Universidad de la República]. Colibri. https://hdl.handle.net/20.500.12008/31627

Watkins de Jong, E., DeGrandi-Hoffman, G., Chen, Y., Graham, H., & Ziolkowski, N. (2019). Effects of diets containing different concentrations of pollen and pollen substitutes on physiology, Nosema burden, and virus titers in the honey bee (Apis mellifera L.). Apidologie, 50(6), 845-858. https://doi.org/10.1007/s13592-019-00695-8

White, B., & Day, C. (2022). The economic value of honey bee flora in Western Australia. CRC for Honey Bee Products.

Wu, Q., & Brown, M. R. (2006). Signaling and function of insulin-like peptides in insects. Annual Review of Entomology, 51, 1-24. https://doi.org/10.1146/annurev.ento.51.110104.151011

Downloads

Published

2026-03-02

How to Cite

Branchiccela, B., Antúnez, K., & Invernizzi, C. (2026). Honey Bee Nutrition: Current Knowledge, Challenges, and Future Research Directions. Agrociencia Uruguay, 30, e1818. https://doi.org/10.31285/AGRO.30.1818

Issue

Section

Review

Altmetric

Article metrics
Abstract views
Galley views
PDF Views
HTML views
Other views
Escanea para compartir
QR Code

Most read articles by the same author(s)