A mini review on the abiotic factors that disrupt honeybee behavior and impede plant pollination


Hossam Abou-Shaara
Martin Staron
Περίληψη

Honeybees, Apis mellifera, play a crucial role in pollinating various plants. During their foraging age, many stressors can directly disrupt their ability to collect food from flowers. These behavioral disruptions can hamper the foragers' ability to perform round trips between the hive and the flowers, and to visit flowers for collecting food, leading to pollination failure. Stressful environments with poor air quality, pesticide contamination, microplastics, high electromagnetic fields, high wind speeds, and temperature extremes can affect foraging round trips and flower visitation ability. Despite the importance of successful flight trips until landing on flowers for pollination, no specific studies have comprehensively discussed these environmental stressors in the light of behavioral disruptions. Therefore, this mini-review considers abiotic stressors with or without human interference that can cause such behavioral disruptions in the context of recent studies, and suggests new avenues for future research, which are crucial for pollination studies and global food security. Understanding pollination failure due to behavioral disruptions in forager honeybees caused by abiotic factors, even when the bees are seemingly healthy, is emphasized. This article provides a synthesis of important bodies of work related to the foraging ecology of honeybees.

Λεπτομέρειες άρθρου
  • Ενότητα
  • Articles
Λήψεις
Τα δεδομένα λήψης δεν είναι ακόμη διαθέσιμα.
Αναφορές
Abou-Shaara, H.F. 2014. The foraging behaviour of honey bees, Apis mellifera: a review. Vet. Med. 59: 1-10.
Abou-Shaara, H.F. 2019. Geographical information system for beekeeping development. J. Apic. Sci. 63: 5-16.
Abou-Shaara, H.F. 2024. The response of heat shock proteins in honey bees to abiotic and biotic stressors. J. Ther. Biol. 103784.
Abou-Shaara, H.F. 2025. Competition for resources: What factors lead honey bees to outcompete other insect competitors?. Acta Oecol. 127: 104077.
Abou-Shaara, H.F., A.A. Al-Ghamdi and A.A. Mohamed. 2013. Honey bee colonies performance enhance by newly modified beehives. J. Apic. Sci. 57: 45-57.
Agathokleous, E., Z. Feng and J. Peñuelas. 2022. Ozone pollution disrupts plant–pollinator systems. Trends Ecol. Evol. 37: 939-941.
Alma, A.M., G.S. de Groot and M. Buteler. 2023. Microplastics incorporated by honeybees from food are transferred to honey, wax and larvae. Environ. Pollut. 320: 121078.
Amdam, G.V., O. Rueppell, M.K. Fondrk, R.E. Page and C.M. Nelson 2009. The nurse’s load: early-life exposure to brood-rearing affects behavior and lifespan in honey bees (Apis mellifera). Exp. Gerontol. 44: 467-471.
Arenas, A., R. Lajad, T. Peng, C. Grüter and W. Farina. 2021. Correlation between octopaminergic signalling and foraging task specialisation in honeybees. Gen. Brain. Behav. 20: e12718.
Balmori, A. 2022. Effects of man-made and especially wireless communication electromagnetic fields on wildlife. Electromagnetic Fields of Wireless Communications: Biological and Health Effects 393-446.
Balzani, P., G. Galeotti, S. Scheggi, A. Masoni, G. Santini and D. Baracchi. 2022. Acute and chronic ingestion of polyethylene (PE) microplastics has mild effects on honey bee health and cognition. Env. Pollu. 305: 119318.
Barascou, L., F. Requier, D. Sené, D. Crauser, Y. Le Conte and C. Alaux. 2022. Delayed effects of a single dose of a neurotoxic pesticide (sulfoxaflor) on honeybee foraging activity. Sci. Total Environ. 805: 150351.
Begna, T. and C. Jung. 2021. Effects of sequential exposures of sub-lethal doses of amitraz and thiacloprid on learning and memory of honey bee foragers, Apis mellifera. J. Asia-Pacific Entomol. 24: 77-83.
Bisrat, D. and C. Jung. 2022. Roles of flower scent in bee–flower mediations: a review. J. Ecol. Env. 46.
Black, T.E., K.L.N. Stauch, H. Wells and C.I. Abramson. 2021. Effects of ethanol ingestion on aversive conditioning in honey bees (Apis mellifera L.). J. Comp. Psychol. 135: 559.
Bonoan, R.E., J. Gonzalez and P.T. Starks. 2020. The perils of forcing a generalist to be a specialist: lack of dietary essential amino acids impacts honey bee pollen foraging and colony growth. J. Apic. Res. 59: 95-103.
Burden, C.M., M.O. Morgan, K.R. Hladun, G.V. Amdam, J.J. Trumble and B.H. Smith. 2019. Acute sublethal exposure to toxic heavy metals alters honey bee (Apis mellifera) feeding behavior. Sci. Rep. 9: 4253.
Buteler, M., A.M. Alma, T. Stadler, A.C. Gingold, M.C. Manattini and M. Lozada. 2022. Acute toxicity of microplastic fibers to honeybees and effects on foraging behavior. Sci. Total Env. 822: 153320.
Buteler, M., E. Villalobos, A.M. Alma, L. Silva and J.P. Tomba. 2023. Management practice for small hive beetle as a source of microplastic contamination in honey and honeybee colonies. Env. Pollu. 334: 122151.
Capela, N., A. Sarmento, S. Simões, H.M. Azevedo-Pereira and J.P. Sousa. 2022. Sub-lethal doses of sulfoxaflor impair honey bee homing ability. Sci. Total Env. 837: 155710.
Cassano, J. and D. Naug. 2022. Metabolic rate shapes differences in foraging efficiency among honeybee foragers. Behav. Ecol. 33: 1188-1195.
Cho, Y., S. Jeong, D. Lee, S.W. Kim, R.J. Park, L. Gibson, C. Zheng and C.R. Park. 2021. Foraging trip duration of honeybee increases during a poor air quality episode and the increase persists thereafter. Ecol. Evol. 11: 1492-1500.
Choudhary, A., B. Mohindru, R. Kaur, J. Singh and P.K. Chhuneja. 2021. Effect of partial solar eclipse on the activity of Apis mellifera Linnaeus. In proceedings of virtual national conference on strategic reorientation for climate smart agriculture, 2:103.
Coallier, N., L. Perez, M. F. Franco, Y. Cuellar and J. Vadnais. 2025. Poor air quality raises mortality in honey bees, a concern for all pollinators. Commun. Earth Environ. 6: 126.
Colin, T., W.G. Meikle, X. Wu and A.B. Barron. 2019. Traces of a neonicotinoid induce precocious foraging and reduce foraging performance in honey bees. Env. Sci. Technol. 53: 8252-8261.
Conti, G.O., M. Ferrante, M. Banni, C. Favara, I. Nicolosi, A. Cristaldi, M. Fiore, P. Zuccarello. 2020. Micro-and nano-plastics in edible fruit and vegetables. The first diet risks assessment for the general population. Env. Res. 187: 109677.
Cruz, C.P., B. Ratoni, F. Villalobos, R. Ayala, I. Hinojoza-Díaz and W. Dáttilo. 2024. Drivers of flower visit and resource sharing between the honeybee and native bees in Neotropical coastal sand dunes. Sci. Nat. 111: 2. https://doi.org/10.1007/s00114-024-01888-7
Démares, F., L. Gibert, P. Creusot, B. Lapeyre and M. Proffit. 2022. Acute ozone exposure impairs detection of floral odor, learning, and memory of honey bees, through olfactory generalization. Sci. Total Env. 827: 154342.
Démares, F., L. Gibert, B. Lapeyre, P. Creusot, D. Renault and M. Proffit. 2023. Ozone exposure induces metabolic stress and olfactory memory disturbance in honey bees. Chemosphere 140647.
Deng, Y., X. Jiang, H. Zhao, S. Yang, J. Gao, Y. Wu, Q. Diao and C. Hou. 2021. Microplastic polystyrene ingestion promotes the susceptibility of honeybee to viral infection. Env. Sci. Technol. 55: 11680-11692.
Di Trani, J.C., V.M. Ramírez, Y. Añino and A. Barba. 2022. Environmental conditions and bee foraging on watermelon crops in Panama. J. Anim. Behav. Biometeorol. 10: 2234-2234.
Dreyer, D., B. Frost, H. Mouritsen, A. Günther, K. Green, M. Whitehouse, S. Johnsen, S. Heinze and E. Warrant. 2018. The Earth’s magnetic field and visual landmarks steer migratory flight behavior in the nocturnal Australian Bogong moth. Curr. Biol. 28: 2160-2166.
Eeraerts, M., R. Vanderhaegen, G. Smagghe and I. Meeus. 2020. Pollination efficiency and foraging behaviour of honey bees and non‐Apis bees to sweet cherry. Agri. Forest Entomol. 22: 75-82.
Farina, W.M., M.S. Balbuena, L.T. Herbert, C. Mengoni Goñalons and D.E. Vázquez. 2019. Effects of the herbicide glyphosate on honey bee sensory and cognitive abilities: Individual impairments with implications for the hive. Insects 10: 354.
Favre, D. 2011. Mobile phone-induced honeybee worker piping. Apidologie 42: 270-279.
Fei, C.J., K.M. Williamson, , R.T. Woodward, , B.A. McCarl, , and J. Rangel. 2021. Honey bees, almonds, and colony mortality: An economic simulation of the US pollination market. Land Econom. 97: 688-703.
Ferenczi, A.F., I. Szűcs and A.B. Gáthy. 2023. Evaluation of the pollination ecosystem service of the honey bee (Apis mellifera) based on a beekeeping model in Hungary. Sustainability 15: 9906.
Ferrari, T.E. 2014. Magnets, magnetic field fluctuations and geomagnetic disturbances impair the homing ability of honey bees (Apis mellifera). J. Apic. Res. 53: 452-465.
Galen, C., Z. Miller, A. Lynn, M. Axe, S. Holden, L. Storks, E. Ramirez, E. Asante, D. Heise, S. Kephart and J. Kephart. 2019. Pollination on the dark side: Acoustic monitoring reveals impacts of a total solar eclipse on flight behavior and activity schedule of foraging bees. Ann. Entomol. Soci. Am. 112: 20-26.
Ghosh, S., H. Jeon and C. Jung. 2020. Foraging behaviour and preference of pollen sources by honey bee (Apis mellifera) relative to protein contents. J. Ecol. Env. 44: 1-7.
Girling, R.D., I. Lusebrink, E. Farthing, T.A. Newman and G.M. Poppy. 2013. Diesel exhaust rapidly degrades floral odours used by honeybees. Sci. Rep. 3: 2779.
Gong, Z., G. Gu, Y. Wang, S. Dong, K. Tan and J.C. Nieh. 2021. Floral tea polyphenols can improve honey bee memory retention and olfactory sensitivity. J. Insect Physiol. 128: 104177.
Guo, Y., Q.Y. Diao, P.L. Dai, Q. Wang, C.S. Hou, Y.J. Liu, L. Zhang, Q.-H. Luo, Y.-Y. Wu and J. Gao. 2021. The effects of exposure to flupyradifurone on survival, development, and foraging activity of honey bees (Apis mellifera L.) under field conditions. Insects 12: 357.
Hains, B.C. and H. Gamper. 2017. Disruption in honey bee (Apis mellifera) foraging flight activity during a partial solar eclipse shown by individual flight path tracking. Bull. Insectol. 70: 315-320.
Hendriksma, H.P., A.L. Toth and S. Shafir. 2019. Individual and colony level foraging decisions of bumble bees and honey bees in relation to balancing of nutrient needs. Front. Ecol. Evol. 7: 177.
Hennessy, G., C. Harris, C. Eaton, P. Wright, E. Jackson, D. Goulson and F.F. Ratnieks. 2020. Gone with the wind: effects of wind on honey bee visit rate and foraging behaviour. Anim. Behav. 161: 23-31.
Hennessy, G., C. Harris, L. Pirot, A. Lefter, D. Goulson and F.L. Ratnieks. 2021. Wind slows play: Increasing wind speed reduces flower visiting rate in honey bees. Anim. Behav. 178: 87-93.
Horna Lowell, E.S., J.A. Morris, M.C. Vidal, C.S. Durso and S.M. Murphy. 2019. The effect of conspecific cues on honey bee foraging behavior. Apidologie 50: 454-462.
Juddin, A.S.S., N. Ngah, R. Umar, K. Asante and M.G. Abdullahi. 2023. A review influence of light on insect activity and behaviour: sustainable lighting and light pollution. J. Sustainabil. Sci. Manag. 18: 231-247.
Kheradmand, B., J. Cassano, S. Gray and J.C. Nieh 2020. Influence of visual targets and landmarks on honey bee foraging and waggle dancing. Insect Sci. 27: 349-360.
Kietzman, P.M. and P.K. Visscher. 2021. The influence of available comb storage space on the performance of honey bee communication signals that regulate foraging. Apidologie 52: 133-140.
Koelmans, A.A., N.H.M. Nor, E. Hermsen, M. Kooi, S.M. Mintenig and J. De France. 2019. Microplastics in freshwaters and drinking water: Critical review and assessment of data quality. Water Res. 155: 410-422.
Lambinet, V., M.E. Hayden, K. Reigl, S. Gomis and G. Gries. 2017. Linking magnetite in the abdomen of honey bees to a magnetoreceptive function. Proc. Royal. Soc. B: Biol. Sci. 284: 20162873.
Lan, J., G. Ding, W. Ma, Y. Jiang and J. Huang. 2021. Pollen source affects development and behavioral preferences in honey bees. Insects 12: 130.
Landaverde, R., M.T. Rodriguez and J.A. Parrella. 2023. Honey production and climate change: beekeepers’ perceptions, farm adaptation strategies, and information needs. Insects 14: 493.
Langford, B., J.M. Ryalls, N.J. Mullinger, P. Hayden, E. Nemitz, C. Pfrang, A. Robins, D. Touhami, L.M. Bromfield and R.D. Girling. 2023. Mapping the effects of ozone pollution and mixing on floral odour plumes and their impact on plant-pollinator interactions. Environ. Pollu. 336: 122336.
Le Conte, Y. and M. Navajas. 2008. Climate change: impact on honey bee populations and diseases. Revue Scientifique et Technique-Office International des Epizooties 27: 499-510.
Lee, H. and H. Kang. 2018. Temperature-driven changes of pollinator assemblage and activity of Megaleranthis saniculifolia (Ranunculaceae) at high altitudes on Mt. Sobaeksan, South Korea. J. Ecol. Environ. 42: 1-7.
Leonard, R.J., T.J. Pettit, P. Irga, C. McArthur and D.F. Hochuli. 2019a. Acute exposure to urban air pollution impairs olfactory learning and memory in honeybees. Ecotoxicol. 28: 1056-1062.
Leonard, R.J., V. Vergoz, N. Proschogo, C. McArthur and D.F. Hochuli. 2019b. Petrol exhaust pollution impairs honey bee learning and memory. Oikos 128: 264-273.
Liga, D., G. Stancher and E. Frasnelli. 2024. Visuo-motor lateralization in Apis mellifera: flight speed differences in foraging choices. Sci. Rep. 14: 660.
Ludicke, J.C. and J.C. Nieh. 2020. Thiamethoxam impairs honey bee visual learning, alters decision times, and increases abnormal behaviors. Ecotoxicol. Environ. Safet. 193: 110367.
Lusebrink, I., R.D. Girling, L. Dobrindt, C.W. Jackson, T.A. Newman and G.M. Poppy. 2023. Investigating the effects of diesel exhaust and flower color on flower visitation by free-flying honey bees. Arth-Plant Inter. 17: 11-17.
Lusebrink, I., R.D. Girling, E. Farthing, T.A. Newman, C.W. Jackson and G.M. Poppy. 2015. The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction. J. Chem. Ecol. 41: 904-912.
Ma, W., D. Long, Y. Wang, X. Li, J. Huang, J. Shen, W. Su, Y. Jiang and J. Li. 2021. Electrophysiological and behavioral responses of Asian and European honeybees to pear flower volatiles. J. Asia-Pacific Entomol. 24: 221-228.
Mas, F., R.M. Horner, S. Brierley, R.C. Butler and D.M. Suckling. 2020. Selection of key floral scent compounds from fruit and vegetable crops by honey bees depends on sensory capacity and experience. J. Insect Physiol. 121: 104002.
Migdał, P., E. Berbeć, P. Bieńkowski, M. Plotnik, A. Murawska and K. Latarowski. 2022. Exposure to magnetic fields changes the behavioral pattern in Honeybees (Apis mellifera L.) under laboratory conditions. Animals 12: 855.
Molina-Montenegro, M.A., I.S. Acuña-Rodríguez,
Molina-Montenegro, M.A., I.S. Acuña-Rodríguez, G.I. Ballesteros, M. Baldelomar, C. Torres-Díaz, B.R. Broitman and D.P. Vázquez. 2023. Electromagnetic fields disrupt the pollination service by honeybees. Sci. Adv. 9: eadh1455.
Morfin, N., P.H. Goodwin, A. Correa-Benitez and E. Guzman-Novoa. 2019. Sublethal exposure to clothianidin during the larval stage causes long-term impairment of hygienic and foraging behaviours of honey bees. Apidologie 50: 595-605.
Mustard, J.A., A. Gott, J. Scott, N.L. Chavarria and G.A. Wright. 2020. Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide. J. Exp. Biol. 223: jeb217174.
Neumann, P. and L. Straub. 2023. Beekeeping under climate change. J Apic Res 62: 963-968.
Ngo, T.N., D.J.A. Rustia, E.C. Yang and T.T. Lin. 2021. Automated monitoring and analyses of honey bee pollen foraging behavior using a deep learning-based imaging system. Comp. Elect. Agri. 187: 106239.
Nicewicz, Ł., A.W. Nicewicz, A. Kafel and M. Nakonieczny. 2021. Set of stress biomarkers as a practical tool in the assessment of multistress effect using honeybees from urban and rural areas as a model organism: a pilot study. Env. Sci. Pollu. Res. 28: 9084-9096.
Odemer, R. and F. Odemer. 2019. Effects of radiofrequency electromagnetic radiation (RF-EMF) on honey bee queen development and mating success. Sci. Total Env. 661: 553-562.
Ohlinger, B.D., R. Schürch, S. Durzi, P.M. Kietzman, M.R. Silliman and M.J. Couvillon. 2022. Honey bees (Hymenoptera: Apidae) decrease foraging but not recruitment after neonicotinoid exposure. J. Insect Sci. 22: 16.
Okubo, S., M. Yoshiyama, A. Nikkeshi, N. Morimoto and K. Kimura. 2020. Effect of cold narcosis on foraging behavior of European honey bees (Apis mellifera ligustica) tracked using a radio-frequency identification (RFID) system. J. Apic. Res. 59: 1027-1032.
Paray, B.A., I. Kumari, Y.A. Hajam, B. Sharma, R. Kumar, M.F. Albeshr, M.A Farah, J.M. Khan. 2021. Honeybee nutrition and pollen substitutes: A review. Saudi J. Biol. Sci. 28: 1167-1176.
Pasquini, E., F. Ferrante, L. Passaponti, F.S. Pavone, I. Costantini and D. Baracchi. 2023. Microplastics reach the brain and interfere with honey bee cognition. Sci. Total Env. 169362.
Pătruică, S., E. Simiz, I. Peț and L. Ștef. 2019. Some correlations between environmental parameters and the foraging behavior of honeybees (Apis mellifera) on oilseed rape (Brassica napusoleifera), Scientific Papers, Series D. Anim. Sci. 2: 180-184.
Paudel, Y.P., R. Mackereth, R. Hanley and W. Qin. 2015. Honey bees (Apis mellifera L.) and pollination issues: Current status, impacts, and potential drivers of decline. J. Agri. Sci. 7: 93-109.
Peter, C.I. and S.D. Johnson. 2008. Mimics and magnets: the importance of color and ecological facilitation in floral deception. Ecol. 89:1583–1595.
Puškadija, Z., E. Štefanić, A. Mijić, Z. Zdunić, N. Parađiković, T. Florijančić and A. Opačak. 2007. Influence of weather conditions on honey bee visits (Apis mellifera carnica) during sunflower (Helianthus annuus L.) blooming period. Poljoprivreda, 13(1), 230-233.
Quinlan, G., M. Milbrath, C. Otto, A. Smart, D. Iwanowicz, R.S. Cornman and R. Isaacs. 2021. Honey bee foraged pollen reveals temporal changes in pollen protein content and changes in forager choice for abundant versus high protein flowers. Agri. Ecosyst. Env. 322: 107645.
Rahman, A., A. Sarkar, O.P. Yadav, G. Achari and J. Slobodnik. 2021. Potential human health risks due to environmental exposure to nano-and microplastics and knowledge gaps: a scoping review. Sci. Total Env. 757: 143872.
Ratnayake, M.N., A.G. Dyer and A. Dorin. 2021. Tracking individual honeybees among wildflower clusters with computer vision-facilitated pollinator monitoring. Plos One 16: e0239504.
Romero-González, J.E., C. Solvi and L. Chittka. 2020. Honey bees adjust colour preferences in response to concurrent social information from conspecifics and heterospecifics. Anim. Behav. 170: 219-228.
Ryalls, J.M., B. Langford, N.J. Mullinger, L.M. Bromfield, E. Nemitz, C. Pfrang and R.D. Girling. 2022. Anthropogenic air pollutants reduce insect-mediated pollination services. Env. Pollu. 297: 118847.
Shepherd, S., M.A.P. Lima, E.E. Oliveira, S.M. Sharkh, C.W. Jackson and P.L. Newland. 2018. Extremely low frequency electromagnetic fields impair the cognitive and motor abilities of honey bees. Sci. Rep. 8: 1-9.
Shi, J., H. Yang, L. Yu, C. Liao, Y. Liu, M. Jin, W. Yan, X.B. Wu. 2020. Sublethal acetamiprid doses negatively affect the lifespans and foraging behaviors of honey bee (Apis mellifera L.) workers. Sci. Total. Env. 738: 139924.
Shi, L., S.W. Nicolson, Y. Yang, J. Wu, S. Yan and Z. Wu, 2020. Drinking made easier: honey bee tongues dip faster into warmer and/or less viscous artificial nectar. J. Exp. Biol. 223: jeb229799.
Smith, M.L., J.D. Davidson, B. Wild, D.M. Dormagen, T. Landgraf and I.D. Couzin. 2022. Behavioral variation across the days and lives of honey bees. Iscience 25.
Stec, D. and K. Kuszewska. 2020. CO2 narcosis influences the memory of honey bees. J. Apic. Res. 59: 663-668.
Su, W., W. Ma, Q. Zhang, X. Hu, G. Ding, Y. Jiang and J. Huang. 2022. Honey bee foraging decisions influenced by pear volatiles. Agriculture 12: 1074.
Tait, C., A. Mattise-Lorenzen, A. Lark and D. Naug. 2019. Interindividual variation in learning ability in honeybees. Behav. Proc. 167: 103918.
Tison, L., A. Duer, V. Púčiková, U. Greggers and R. Menzel. 2020. Detrimental effects of clothianidin on foraging and dance communication in honey bees. PLoS One 15: e0241134.
Toribio, D., W. Joseph and A. Thielens. 2021. Near field radio frequency electromagnetic field exposure of a western honey bee. IEEE Transactions on Antennas and Propagation 70: 1320-1327.
Tsuruda, J.M., P. Chakrabarti and R.R. Sagili. 2021. Honey bee nutrition. Veterinary Clinics: Food Animal Practice 37: 505-519.
Waiker, P., S. Baral, A. Kennedy, S. Bhatia, A. Rueppell, K. Le, E. Amiri, J. Tsuruda and O. Rueppell. 2019. Foraging and homing behavior of honey bees (Apis mellifera) during a total solar eclipse. Sci. Nat. 106: 1-10.
Walker, M.M. and M.E. Bitterman. 1985. Conditioned responding to magnetic fields by honeybees. J. Comp. Physiol. A 157: 67-71.
Weidenmüller, A. and J. Tautz. 2002. In‐hive behavior of pollen foragers (Apis mellifera) in honey bee colonies under conditions of high and low pollen need. Ethol. 108: 205-221.
Xu, J., W. Pan, Y. Zhang, Y. Li, G. Wan, F. Chen, G.A. Sword and W. Pan. 2017. Behavioral evidence for a magnetic sense in the oriental armyworm, Mythimna separata. Biol. Open 6: 340-347.