Skip to main content

Advertisement

SpringerLink
Log in

Global honeybee health decline factors and potential conservation techniques

  • Review
  • Published:
Food Security Aims and scope Submit manuscript

A Correction to this article was published on 15 February 2023

This article has been updated

Abstract

Pesticide exposure, heavy metal pollution, and biological stressors drive a worldwide, ongoing, and rapid population decline of the crucial pollinator honeybee. Drastic colony loss of honeybees may well precipitate a food security crisis. Here a systematic review was conducted, examining reports on a global scale to propose a bench line for common pesticides and potentially toxic element (PTE) residue levels in plant rewards and honeybees and to assess the health risk of chemical residues via oral exposure to honeybees. Relevant articles were retrieved from Scopus, PubMed, ISI Web of Science, and Embase. Recent findings on how chemical and biological stressors cripple honeybee health, and conservation techniques were also summarized. We identified a number of chemical residues at lethal or sublethal risk to honeybees based on their average concentrations, as well as primary evidence pertaining to the bio-accumulative propensity of certain substances. Moreover, combinations of pesticide stressors (“pesticide cocktails”), which are frequently encountered in agricultural landscapes, often interact synergistically with honeybee health via detoxification suppression. Finally, we discuss and describe the relevance of novel, biotechnology-based, approaches to counteract agrochemical and PTE poisoning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

All data generated or analysed during this study are included in this published article (and its supplementary information files).

Change history

References

  • Aldgini, H. M. M., Abdullah Al-Abbadi, A., Abu-Nameh, E. S. M., & Alghazeer, R. O. (2019). Determination of metals as bio indicators in some selected bee pollen samples from Jordan. Saudi Journal of Biological Sciences, 26(7), 1418–1422. https://doi.org/10.1016/j.sjbs.2019.03.005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alejo-González, K., Hanson-Viana, E., & Vazquez-Duhalt, R. (2018). Enzymatic detoxification of organophosphorus pesticides and related toxicants. Journal of Pesticide Science, 43(1), 1–9 https://doi.org/10.1584/jpestics.D17-078

  • Amiri Andi, M., & Ahmadi, A. (2014). Influence of vitamin C in sugar syrup on brood area, colony population, body weight and protein in honey bees. International Journal of Biosciences (IJB), 4(6), 32–36. https://doi.org/10.12692/ijb/4.6.32-36

  • Andrey, R. (2017). Autoclaved Nosema ceranae spores immune adult Apis mellifera against future infection [University of California, San Diego]. California Digital Library. Retrieved February 11, 2022, from https://escholarship.org/uc/item/8t2694nh

  • Annoscia, D., Di Prisco, G., Becchimanzi, A., Caprio, E., Frizzera, D., Linguadoca, A., & Pennacchio, F. (2020). Neonicotinoid Clothianidin reduces honey bee immune response and contributes to Varroa mite proliferation. Nature Communications, 11(1), Article 5887. https://doi.org/10.1038/s41467-020-19715-8

  • Ataide de Oliveira, F., de Abreu, A. T., Nascimento, N., & d. O., Froes, R. E. S., Nalini, H. A., Jr., & Antonine, Y. (2020). Mineral content in honey and pollen from native stingless bees Tetragonisca angustula (Latreille, 1811) in the Iron Quadrangle. Brazil. Journal of Apicultural Research, 59(4), 378–389. https://doi.org/10.1080/00218839.2020.1730578

    Article  Google Scholar 

  • Bell, H. C., Montgomery, C. N., Benavides, J. E., & Nieh, J. C. (2021). Effects of Nosema ceranae (Dissociodihaplophasida: Nosematidae) and Flupyradifurone on olfactory learning in honey bees, Apis mellifera (Hymenoptera: Apidae). Journal of Insect Science, 20(6), Article 29. https://doi.org/10.1093/jisesa/ieaa130

  • Belsky, J., & Joshi, N. K. (2019). Impact of biotic and abiotic stressors on managed and feral bees. Insects, 10(8), Article 233. https://doi.org/10.3390/insects10080233

  • Bird, G., Wilson, A. E., Williams, G. R., & Hardy, N. B. (2021). Parasites and pesticides act antagonistically on honey bee health. Journal of Applied Ecology, 58(5), 997–1005. https://doi.org/10.1111/1365-2664.13811

    Article  Google Scholar 

  • Bolisetty, S., Peydayesh, M., & Mezzenga, R. (2019). Sustainable technologies for water purification from heavy metals: Review and analysis. Chemical Society Reviews, 48, 463–487. https://doi.org/10.1039/c8cs00493e

    Article  CAS  PubMed  Google Scholar 

  • Bosancic, B., Zabic, M., Mihajlovic, D., Samardzic, J., & Mirjanic, G. (2020). Comparative study of toxic heavy metal residues and other properties of honey from different environmental production systems. Environmental Science and Pollution Research, 27, 38200–38211. https://doi.org/10.1007/s11356-020-09882-y/Published

    Article  CAS  PubMed  Google Scholar 

  • Bovi, T. S., Zaluski, R., & Orsi, R. O. (2018). Toxicity and motor changes in Africanized honey bees (Apis mellifera L.) exposed to fipronil and imidacloprid. Anais da Academia Brasileira de Ciencias, 90(1), 239–245. https://doi.org/10.1590/0001-3765201820150191

  • Budge, G. E., Simcock, N. K., Holder, P. J., Shirley, M. D. F., Brown, M. A., Van Weymers, P. S. M., & Rushton, S. P. (2020). Chronic bee paralysis as a serious emerging threat to honey bees. Nature Communications, 11(1), Article 2164. https://doi.org/10.1038/s41467-020-15919-0

  • Burden, C. M., Elmore, C., Hladun, K. R., Trumble, J. T., & Smith, B. H. (2016). Acute exposure to selenium disrupts associative conditioning and long-term memory recall in honey bees (Apis mellifera). Ecotoxixology and Environmental Safety, 127, 71–79. https://doi.org/10.1016/j.ecoenv.2015.12.034

    Article  CAS  Google Scholar 

  • Burnham, A. J. (2019). Scientific advances in controlling Nosema ceranae (Microsporidia) infections in honey bees (Apis mellifera). Frontiers in Veterinary Science, 6, Article 79. https://doi.org/10.3389/fvets.2019.00079

  • Buszewski, B., Bukowska, M., Ligor, M., & Staneczko-Baranowska, I. (2019). A holistic study of neonicotinoids neuroactive insecticides-properties, applications, occurrence, and analysis. Environmental Science and Pollution Research, 26(34), 34723–34740. https://doi.org/10.1007/s11356-019-06114-w

    Article  CAS  PubMed  Google Scholar 

  • Calatayud-Vernich, P., Calatayud, F., Simo, E., Pascual Aguilar, J. A., & Pico, Y. (2019). A two-year monitoring of pesticide hazard in-hive: High honey bee mortality rates during insecticide poisoning episodes in apiaries located near agricultural settings. Chemosphere, 232, 471–480. https://doi.org/10.1016/j.chemosphere.2019.05.170

    Article  CAS  PubMed  Google Scholar 

  • Cameron, S. A., & Sadd, B. M. (2020). Global Trends in Bumble Bee Health. Annual Review of Entomology, 65, 209–232. https://doi.org/10.1146/annurev-ento-011118-111847

    Article  CAS  PubMed  Google Scholar 

  • Carnesecchi, E., Svendsen, C., Lasagni, S., Grech, A., Quignot, N., Amzal, B., & Dorne, J. (2019). Investigating combined toxicity of binary mixtures in bees: Meta-analysis of laboratory tests, modelling, mechanistic basis and implications for risk assessment. Environment International, 133(Pt B), Article 105256. https://doi.org/10.1016/j.envint.2019.105256

  • Castilhos, D., Bergamo, G. C., Gramacho, K. P., & Gonçalves, L. S. (2019). Bee colony losses in Brazil: A 5-year online survey. Apidologie, 50, 263–272. https://doi.org/10.1007/s13592-019-00642-7

    Article  Google Scholar 

  • Cevat, N., Ahmet, G., Neslihan, O., & Sena, C. (2018). Preventive action of zinc against heavy metals toxicity in honeybee. African Journal of Biochemistry Research, 12, 1–6. https://doi.org/10.5897/ajbr2016.0921

    Article  CAS  Google Scholar 

  • Chaimanee, V., & Pettis, J. S. (2019). Gene expression, sperm viability, and queen (Apis mellifera) loss following pesticide exposure under laboratory and field conditions. Apidologie, 50(3), 304–316. https://doi.org/10.1007/s13592-019-00645-4

    Article  CAS  Google Scholar 

  • Chakrabarti, P., Sarkar, S., & Basu, P. (2019). Pesticide induced visual abnormalities in Asian honey bees (Apis cerana L.) in intensive agricultural landscapes. Chemosphere, 230, 51–58. https://doi.org/10.1016/j.chemosphere.2019.05.050

    Article  CAS  PubMed  Google Scholar 

  • Chauzat, M. P., Faucon, J. P., Martel, A. C., Lachaize, J., Cougoule, N., & Aubert, M. (2006). A survey of pesticide residues in pollen loads collected by honey bees in France. Journal of Economic Entomology, 99(2), 253–262. https://doi.org/10.1603/0022-0493-99.2.253

    Article  CAS  PubMed  Google Scholar 

  • Chen, J., Webb, J., Shariati, K., Guo, S., Montclare, J.-K., McArt, S., & Ma, M. (2021). Pollen-inspired enzymatic microparticles to reduce organophosphate toxicity in managed pollinators. Nature Food, 2(5), 339–347. https://doi.org/10.1038/s43016-021-00282-0

    Article  CAS  PubMed  Google Scholar 

  • Colin, T., Meikle, W. G., Paten, A. M., & Barron, A. B. (2019). Long-term dynamics of honey bee colonies following exposure to chemical stress. Science of the Total Environment, 677, 660–670. https://doi.org/10.1016/j.scitotenv.2019.04.402

    Article  CAS  PubMed  Google Scholar 

  • Coulon, M., Dalmon, A., Di Prisco, G., Prado, A., Arban, F., Dubois, E., & Le Conte, Y. (2020). Interactions Between Thiamethoxam and Deformed Wing Virus Can Drastically Impair Flight Behavior of Honey Bees. Frontiers in Microbiology, 11, Article 766. https://doi.org/10.3389/fmicb.2020.00766

  • Coulon, M., Schurr, F., Martel, A.-C., Cougoule, N., Begaud, A., Mangoni, P., & Dubois, E. (2019). Influence of chronic exposure to thiamethoxam and chronic bee paralysis virus on winter honey bees. PLoS One, 14(8), Article e0220703. https://doi.org/10.1371/journal.pone.0220703

  • Dabour, K., Al Naggar, Y., Masry, S., Naiem, E., & Giesy, J. P. (2019). Cellular alterations in midgut cells of honey bee workers (Apis millefera L.) exposed to sublethal concentrations of CdO or PbO nanoparticles or their binary mixture. Science of the Total Environment, 651, 1356–1367. https://doi.org/10.1016/j.scitotenv.2018.09.311

    Article  CAS  PubMed  Google Scholar 

  • Dara, S. K. (2019). The New Integrated Pest Management Paradigm for the Modern Age. Journal of Integrated Pest Management, 10(1), Article 12. https://doi.org/10.1093/jipm/pmz010

  • David, A., Botias, C., Abdul-Sada, A., Nicholls, E., Rotheray, E. L., Hill, E. M., & Goulson, D. (2016). Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environment International, 88, 169–178. https://doi.org/10.1016/j.envint.2015.12.011

    Article  CAS  PubMed  Google Scholar 

  • del Mar Gomez-Ramos, M., Gomez Ramos, M. J., Martinez Galera, M., Gil Garcia, M. D., & Fernandez-Alba, A. R. (2018). Analysis and evaluation of (neuro)peptides in honey bees exposed to pesticides in field conditions. Environmental Pollution, 235, 750–760. https://doi.org/10.1016/j.envpol.2017.12.091

    Article  CAS  Google Scholar 

  • Di, N., Hladun, K. R., Zhang, K., Liu, T. X., & Trumble, J. T. (2016). Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere, 152, 530–538. https://doi.org/10.1016/j.chemosphere.2016.03.033

    Article  CAS  PubMed  Google Scholar 

  • Dively, G. P., & Kamel, A. (2012). Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. Journal of Agricultural and Food Chemistry, 60(18), 4449–4456. https://doi.org/10.1021/jf205393x

    Article  CAS  PubMed  Google Scholar 

  • Egan, P. A., Dicks, L. V., Hokkanen, H. M. T., & Stenberg, J. A. (2020). Delivering Integrated Pest and Pollinator Management (IPPM). Trends in Plant Science, 25(6), 577–589. https://doi.org/10.1016/j.tplants.2020.01.006

  • El-Nahhal, Y. (2020). Pesticide residues in honey and their potential reproductive toxicity. Science of the Total Environment, 741, Article 139953. https://doi.org/10.1016/j.scitotenv.2020.139953

  • European, C., Directorate-General for, H., & Consumers. (2013). Toxicity and assessment of chemical mixtures. European Commission. https://doi.org/10.2772/21444

  • European Food Safety, A. (2013). Guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal, 11(7), Article 3295. https://doi.org/10.2903/j.efsa.2013.3295

  • Feldhaar, H., & Otti, O. (2020). Pollutants and Their Interaction with Diseases of Social Hymenoptera. Insects, 11(3), Article 153. https://doi.org/10.3390/insects11030153

  • Gajic, B., Munoz, I., De la Rua, P., Stevanovic, J., Lakic, N., Kulisic, Z., & Stanimirovic, Z. (2019). Coexistence of genetically different Varroa destructor in Apis mellifera colonies. Experimental and Applied Acarology, 78(3), 315–326. https://doi.org/10.1007/s10493-019-00395-z

    Article  PubMed  Google Scholar 

  • Galajda, R., Valencakova, A., Sucik, M., & Kandracova, P. (2021). Nosema Disease of European Honey Bees. Journal of Fungi, 7(9), Article 714. https://doi.org/10.3390/jof7090714

  • Garibaldi, L. A., Requier, F., Rollin, O., & Andersson, G. K. (2017). Towards an integrated species and habitat management of crop pollination. Current Opinion in Insect Science, 21, 105–114. https://doi.org/10.1016/j.cois.2017.05.016

    Article  PubMed  Google Scholar 

  • Gashout, H. A., Goodwin, P. H., & Guzman-Novoa, E. (2018). Lethality of synthetic and natural acaricides to worker honey bees (Apis mellifera) and their impact on the expression of health and detoxification-related genes. Environmental Science and Pollution Research International, 25(34), 34730–34739. https://doi.org/10.1007/s11356-018-3205-6

    Article  CAS  PubMed  Google Scholar 

  • Gashout, H. A., Guzman-Novoa, E., Goodwin, P. H., & Correa-Benítez, A. (2020). Impact of sublethal exposure to synthetic and natural acaricides on honey bee (Apis mellifera) memory and expression of genes related to memory. Journal of Insect Physiology, 121, Article 104014. https://doi.org/10.1016/j.jinsphys.2020.104014

  • Gierer, F., Vaughan, S., Slater, M., Thompson, H. M., Elmore, J. S., & Girling, R. D. (2019). A review of the factors that influence pesticide residues in pollen and nectar: Future research requirements for optimising the estimation of pollinator exposure. Environmental Pollution, 249, 236–247. https://doi.org/10.1016/j.envpol.2019.03.025

    Article  CAS  PubMed  Google Scholar 

  • Gong, Y., & Diao, Q. (2017). Current knowledge of detoxification mechanisms of xenobiotic in honey bees. Ecotoxicology, 26(1), 1–12. https://doi.org/10.1007/s10646-016-1742-7

    Article  CAS  PubMed  Google Scholar 

  • Gray, A., Adjlane, N., Arab, A., Ballis, A., Brusbardis, V., Charrière, J.-D., & Williams, A. (2020). Honey bee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018–2019, and the effects of a new queen on the risk of colony winter loss. Journal of Apicultural Research, 59(5), 744–751. https://doi.org/10.1080/00218839.2020.1797272

  • Green, K. K., Stenberg, J. A., & Lankinen, Å. (2020). Making sense of Integrated Pest Management (IPM) in the light of evolution. Evolutionary Applications, 13(8), 1791–1805. https://doi.org/10.1111/eva.13067

  • Grozinger, C. M., & Flenniken, M. L. (2019). Bee Viruses: Ecology, Pathogenicity, and Impacts. Annual Review of Entomology, 64, 205–226. https://doi.org/10.1146/annurev-ento-011118-111942

    Article  CAS  PubMed  Google Scholar 

  • Haber, A. I., Steinhauer, N. A., & vanEngelsdorp, D. (2019). Use of Chemical and Nonchemical Methods for the Control of Varroa destructor (Acari: Varroidae) and Associated Winter Colony Losses in U.S. Beekeeping Operations. Journal of Economic Entomology, 112(4), 1509–1525. https://doi.org/10.1093/jee/toz088

  • Harwood, G. P., & Dolezal, A. G. (2020). Pesticide–virus interactions in honey bees: Challenges and opportunities for understanding drivers of bee declines. Viruses, 12(5), Article 566. https://doi.org/10.3390/v12050566

  • Hladun, K. R., Di, N., Liu, T. X., & Trumble, J. T. (2016). Metal contaminant accumulation in the hive: Consequences for whole-colony health and brood production in the honey bee (Apis mellifera L.). Environmental Toxicology and Chemistry, 35, 322–329. https://doi.org/10.1002/etc.3273

    Article  CAS  PubMed  Google Scholar 

  • Hladun, K. R., Kaftanoglu, O., Parker, D. R., Tran, K. D., & Trumble, J. T. (2013). Effects of selenium on development, survival, and accumulation in the honeybee (Apis mellifera L.). Environmental Toxicology and Chemistry, 32(11), 2584–2592. https://doi.org/10.1002/etc.2357

  • Holder, P. J., Jones, A., Tyler, C. R., & Cresswell, J. E. (2018). Fipronil pesticide as a suspect in historical mass mortalities of honey bees. Proceedings of the National Academy of Sciences of the United States of America, 115(51), 13033–13038. https://doi.org/10.1073/pnas.1804934115

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hristov, P., Shumkova, R., Palova, N., & Neov, B. (2020). Factors Associated with Honey Bee Colony Losses: A Mini-Review. Veterinary Sciences, 7(4), Article 166. https://doi.org/10.3390/vetsci7040166

  • Huang, Y., Chen, Q., Deng, M., Japenga, J., Li, T., Yang, X., & He, Z. (2018). Heavy metal pollution and health risk assessment of agricultural soils in a typical peri-urban area in southeast China. Journal of Environmental Management, 207, 159–168. https://doi.org/10.1016/j.jenvman.2017.10.072

    Article  CAS  PubMed  Google Scholar 

  • Johnson, R. M., Pollock, H. S., & Berenbaum, M. R. (2009). Synergistic interactions between in-hive miticides in Apis mellifera. Journal of Economic Entomology, 102(2), 474–479. https://doi.org/10.1603/029.102.0202

    Article  CAS  PubMed  Google Scholar 

  • Jonker, M. J., Svendsen, C., Bedaux, J. J. M., Bongers, M., & Kammenga, J. E. (2005). Significance testing of synergistic antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environmental Toxicology and Chemistry, 24(10), 2701–2713. https://doi.org/10.1897/04-431R.1

  • Kadlikova, K., Vaclavikova, M., Halesova, T., Kamler, M., Markovic, M., & Erban, T. (2021). The investigation of honey bee pesticide poisoning incidents in Czechia. Chemosphere, 263, Article 128056. https://doi.org/10.1016/j.chemosphere.2020.128056

  • Kahlon, S. K., Sharma, G., Julka, J. M., Kumar, A., Sharma, S., & Stadler, F. J. (2018). Impact of heavy metals and nanoparticles on aquatic biota. Environmental Chemistry Letters, 16, 919–946. https://doi.org/10.1007/s10311-018-0737-4

    Article  CAS  Google Scholar 

  • Kairo, G., Biron, D. G., Ben Abdelkader, F., Bonnet, M., Tchamitchian, S., Cousin, M., & Brunet, J. -L. (2017a). Nosema ceranae, Fipronil and their combination compromise honey bee reproduction via changes in male physiology. Scientific Reports, 7, Article 8556. https://doi.org/10.1038/s41598-017-08380-5

  • Kairo, G., Poquet, Y., Haji, H., Tchamitchian, S., Cousin, M., Bonnet, M., & Brunet, J. L. (2017b). Assessment of the toxic effect of pesticides on honey bee drone fertility using laboratory and semifield approaches: A case study of fipronil. Environmental Toxicology and Chemistry, 36(9), 2345–2351. https://doi.org/10.1002/etc.3773

  • Kammoun, S., Mulhauser, B., Aebi, A., Mitchell, E. A. D., & Glauser, G. (2019). Ultra-trace level determination of neonicotinoids in honey as a tool for assessing environmental contamination. Environmental Pollution, 247, 964–972. https://doi.org/10.1016/j.envpol.2019.02.004

    Article  CAS  PubMed  Google Scholar 

  • Kimura-Kuroda, J., Komuta, Y., Kuroda, Y., Hayashi, M., & Kawano, H. (2012). Nicotine-like effects of the neonicotinoid insecticides acetamiprid and imidacloprid on cerebellar neurons from neonatal rats. PLoS One, 7(2), Article e32432. https://doi.org/10.1371/journal.pone.0032432

  • Kogan, M. (1998). Integrated Pest Management: Historical Perspectives and Contemporary Developments. Annual Review of Entomology, 43(1), 243–270. https://doi.org/10.1146/annurev.ento.43.1.243

    Article  CAS  PubMed  Google Scholar 

  • Kulhanek, K., Steinhauer, N., Rennich, K., Caron, D. M., Sagili, R. R., Pettis, J. S., & Dennis. (2017). A national survey of managed honey bee 2015–2016 annual colony losses in the USA. Journal of Apicultural Research, 56, 328–340. https://doi.org/10.1080/00218839.2017.1344496

  • Lambert, O., Piroux, M., Puyo, S., Thorin, C., L'Hostis, M., Wiest, L., & Pouliquen, H. (2013). Widespread Occurrence of Chemical Residues in Beehive Matrices from Apiaries Located in Different Landscapes of Western France. PLoS One, 8(6), Article e67007. https://doi.org/10.1371/journal.pone.0067007

  • Lambert, O., Piroux, M., Puyo, S., Thorin, C., Larhantec, M., Delbac, F., & Pouliquen, H. (2012). Bees, honey and pollen as sentinels for lead environmental contamination. Environmental Pollution, 170, 254–259. https://doi.org/10.1016/j.envpol.2012.07.012

    Article  CAS  PubMed  Google Scholar 

  • Leonard, S. P., Powell, J. E., Perutka, J., Geng, P., Heckmann, L. C., Horak, R. D., & Moran, N. A. (2020). Engineered symbionts activate honey bee immunity. Science, 367, 573–576.

  • Leponiemi, M., Amdam, G. V., & Freitak, D. (2021). Exposure to Inactivated Deformed Wing Virus Leads to Trans-Generational Costs but Not Immune Priming in Honeybees (Apis mellifera). Frontiers in Ecology and Evolution, 9, 1–9. https://doi.org/10.3389/fevo.2021.626670

    Article  Google Scholar 

  • Lin, C. H., Sponsler, D. B., Richardson, R. T., Watters, H. D., Glinski, D. A., Henderson, W. M., & Johnson, R. M. (2021). Honey Bees and Neonicotinoid-Treated Corn Seed: Contamination, Exposure, and Effects. Environmental Toxicology and Chemistry, 40(4), 1212–1221. https://doi.org/10.1002/etc.4957

  • Lippert, C., Feuerbacher, A., & Narjes, M. (2021). Revisiting the economic valuation of agricultural losses due to large-scale changes in pollinator populations. Ecological Economics, 180, Article 106860. https://doi.org/10.1016/j.ecolecon.2020.106860

  • Liu, Y. J., Qiao, N. H., Diao, Q. Y., Jing, Z., Vukanti, R., Dai, P. L., & Ge, Y. (2020). Thiacloprid exposure perturbs the gut microbiota and reduces the survival status in honeybees. Journal of Hazardous Materials, 389, Article 121818. https://doi.org/10.1016/j.jhazmat.2019.121818

  • Locke, B., Forsgren, E., Fries, I., & de Miranda, J. R. (2012). Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control. Applied and Environmental Microbiology, 78(1), 227–235. https://doi.org/10.1128/aem.06094-11

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lunardi, J. S., Zaluski, R., & Orsi, R. O. (2017). Evaluation of motor changes and toxicity of insecticides Fipronil and imidacloprid in Africanized Honey bees (Hymenoptera: Apidae). Sociobiology, 64(1), 50–56. https://doi.org/10.13102/sociobiology.v64i1.1190

  • Lundin, O., Rundlöf, M., Jonsson, M., Bommarco, R., & Williams, N. M. (2021). Integrated pest and pollinator management – expanding the concept. Frontiers in Ecology and the Environment, 19(5), 283–291. https://doi.org/10.1002/fee.2325

  • Mao, W., Schuler, M. A., & Berenbaum, M. R. (2011). CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America, 108(31), 12657–12662. https://doi.org/10.1073/pnas.1109535108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martin, S. J., & Brettell, L. E. (2019). Deformed Wing Virus in Honeybees and Other Insects. Annual Review of Virology, 6(1), 49–69. https://doi.org/10.1146/annurev-virology-092818-015700

    Article  CAS  PubMed  Google Scholar 

  • Mc Carthy, U., Uysal, I., Badia-Melis, R., Mercier, S., & O’donnell, C., & Ktenioudaki, A. (2018). Global food security-Issues, challenges and technological solutions. Trends in Food Science & Technology, 77, 11–20. https://doi.org/10.1016/j.tifs.2018.05.002

    Article  CAS  Google Scholar 

  • McRobert, N., Hughes, G., & Savary, S. (2003). Integrated approaches to understanding and control of diseases and pests in field crops. Australasian Plant Pathology, 32(2), 167–180. https://doi.org/10.1071/AP03026

    Article  Google Scholar 

  • Milivojević, T., Glavan, G., Božič, J., Sepčić, K., Mesarič, T., & Drobne, D. (2015). Neurotoxic potential of ingested ZnO nanomaterials on bees. Chemosphere, 120, 547–554. https://doi.org/10.1016/j.chemosphere.2014.07.054

    Article  CAS  PubMed  Google Scholar 

  • Millán-Leiva, A., Marín, Ó., De la Rúa, P., Muñoz, I., Tsagkarakou, A., Eversol, H., & González-Cabrera, J. (2021). Mutations associated with pyrethroid resistance in the honey bee parasite Varroa destructor evolved as a series of parallel and sequential events. Journal of Pest Science, 94, 1505–1517. https://doi.org/10.1007/s10340-020-01321-8

  • Milone, J. P., Chakrabarti, P., Sagili, R. R., & Tarpy, D. R. (2021). Colony-level pesticide exposure affects honey bee (Apis mellifera L.) royal jelly production and nutritional composition. Chemosphere, 263, Article 128183. https://doi.org/10.1016/j.chemosphere.2020.128183

  • Moffat, C., Buckland, S. T., Samson, A. J., McArthur, R., Chamosa Pino, V., Bollan, K. A., & Connolly, C. N. (2016). Neonicotinoids target distinct nicotinic acetylcholine receptors and neurons, leading to differential risks to bumblebees. Scientific Reports, 6, Article 24764. https://doi.org/10.1038/srep24764

  • Monchanin, C., Drujont, E., Devaud, J.-M., Lihoreau, M., & Barron, A. B. (2021). Metal pollutants have additive negative effects on honey bee cognition. Journal of Experimental Biology, 224(12), Article jeb241869. https://doi.org/10.1242/jeb.241869

  • Morfin, N., Goodwin, P. H., & Guzman-Novoa, E. (2020). Interaction of field realistic doses of clothianidin and Varroa destructor parasitism on adult honey bee (Apis mellifera L.) health and neural gene expression, and antagonistic effects on differentially expressed genes. PLoS One, 15(2), Article e0229030. https://doi.org/10.1371/journal.pone.0229030

  • Morse, R. A., & Calderone, N. W. (2003). The Value of Honey Bees As Pollinators of U.S. Crops in 2000. Bee Culture, 128(3), 1–15.

  • Mullin, C. A., Frazier, M., Frazier, J. L., Ashcraft, S., Simonds, R., Vanengelsdorp, D., & Pettis, J. S. (2010). High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One, 5(3), Article e9754. https://doi.org/10.1371/journal.pone.0009754

  • Narjes, M. E., & Lippert, C. (2018). The Optimal Supply of Crop Pollination and Honey From Wild and Managed Bees: An Analytical Framework for Diverse Socio-Economic and Ecological Settings. Ecological Economics, 157, 278–290. https://doi.org/10.1016/j.ecolecon.2018.11.018

    Article  Google Scholar 

  • Nicodemo, D., Maioli, M. A., Medeiros, H. C., Guelfi, M., Balieira, K. V., De Jong, D., & Mingatto, F. E. (2014). Fipronil and imidacloprid reduce honeybee mitochondrial activity. Environmental Toxicology and Chemistry, 33(9), 2070–2075. https://doi.org/10.1002/etc.2655

    Article  CAS  PubMed  Google Scholar 

  • Nikolic, T. V., Kojic, D., Orcic, S., Batinic, D., Vukasinovic, E., Blagojevic, D. P., & Purac, J. (2016). The impact of sublethal concentrations of Cu, Pb and Cd on honey bee redox status, superoxide dismutase and catalase in laboratory conditions. Chemosphere, 164, 98–105. https://doi.org/10.1016/j.chemosphere.2016.08.077

    Article  CAS  PubMed  Google Scholar 

  • Nikolić, T. V., Kojić, D., Orčić, S., Vukašinović, E. L., Blagojević, D. P., & Purać, J. (2019). Laboratory bioassays on the response of honey bee (Apis mellifera L.) glutathione S-transferase and acetylcholinesterase to the oral exposure to copper, cadmium, and lead. Environmental Science and Pollution Research, 26, 6890–6897. https://doi.org/10.1007/s11356-018-3950-6

    Article  CAS  PubMed  Google Scholar 

  • Pablo Porrini, M., Melisa Garrido, P., Laura Umpierrez, M., Pablo Porrini, L., Cuniolo, A., Davyt, B., & Rossini, C. (2020). Effects of synthetic acaricides and Nosema ceranae (Microsporidia: Nosematidae) on molecules associated with chemical communication and recognition in honey bees. Veterinary Sciences, 7(4), Article 199. https://doi.org/10.3390/vetsci7040199

  • Panseri, S., Catalano, A., Giorgi, A., Arioli, F., Procopio, A., Britti, D., & Chiesa, L. M. (2014). Occurrence of pesticide residues in Italian honey from different areas in relation to its potential contamination sources. Food Control, 38(1), 150–156. https://doi.org/10.1016/j.foodcont.2013.10.024

    Article  CAS  Google Scholar 

  • Peng, Y. S., & Marston, J. M. (1986). Filtering mechanism of the honey bee proventriculus. Physiological Entomology, 11, 433–439. https://doi.org/10.1111/j.1365-3032.1986.tb00434.x

    Article  Google Scholar 

  • Pettis, J. S., Lichtenberg, E. M., Andree, M., Stitzinger, J., Rose, R., & Vanengelsdorp, D. (2013). Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS One, 8(7), Article e70182. https://doi.org/10.1371/journal.pone.0070182

  • Polykretis, P., Delfino, G., Petrocelli, I., Cervo, R., Tanteri, G., Montori, G., & Gulisano, M. (2016). Evidence of immunocompetence reduction induced by cadmium exposure in honey bees (Apis mellifera). Environmental Pollution, 218, 826–834. https://doi.org/10.1016/j.envpol.2016.08.006

  • Potts, S. G., Roberts, S. P. M., Dean, R., Marris, G., Brown, M. A., Jones, R., & Settele, J. (2010). Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research, 49, 15–22. https://doi.org/10.3896/IBRA.1.49.1.02

  • Purać, J., Nikolić, T. V., Kojić, D., Ćelić, A. S., Plavša, J. J., Blagojević, D. P., & Petri, E. T. (2019). Identification of a metallothionein gene in honey bee Apis mellifera and its expression profile in response to Cd, Cu and Pb exposure. Molecular Ecology, 28, 731–745. https://doi.org/10.1111/mec.14984

    Article  CAS  PubMed  Google Scholar 

  • Qi, S., Niu, X., Wang, D. H., Wang, C., Zhu, L., Xue, X., & Wu, L. (2020). Flumethrin at sublethal concentrations induces stresses in adult honey bees (Apis mellifera L.). Science of the Total Environment, 700, Article 134500. https://doi.org/10.1016/j.scitotenv.2019.134500

  • Quignot, N., Grech, A., & Amzal, B. (2015). Data collection on Combined Toxicity of Multiple Chemicals for Animal Health and Ecological Risk Assessment. EFSA Supporting Publications, 12(7), 861E. https://doi.org/10.2903/sp.efsa.2015.EN-861

  • Rademacher, E., Harz, M., & Schneider, S. (2017). Effects of oxalic acid on Apis mellifera (Hymenoptera: Apidae). Insects, 8(3), Article 84. https://doi.org/10.3390/insects8030084

  • Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., & 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

  • Robinson, A., Hesketh, H., Lahive, E., Horton, A. A., Svendsen, C., Rortais, A., & Spurgeon, D. J. (2017). Comparing bee species responses to chemical mixtures: Common response patterns? PLoS One, 12(6), Article e0176289. https://doi.org/10.1371/journal.pone.0176289

  • Rothman Jason, A., Leger, L., Kirkwood Jay, S., McFrederick Quinn, S., & Stabb Eric, V. (2019). Cadmium and Selenate Exposure Affects the Honey Bee Microbiome and Metabolome, and Bee-Associated Bacteria Show Potential for Bioaccumulation. Applied and Environmental Microbiology, 85(21), e01411-01419. https://doi.org/10.1128/AEM.01411-19

    Article  PubMed Central  PubMed  Google Scholar 

  • Ru, Q.-M., Feng, Q., He, J.-Z., & Carlo, M. (2013). Risk assessment of heavy metals in honey consumed in Zhejiang province, southeastern China. Food and Chemical Toxicology, 53, 256–262. https://doi.org/10.1016/j.fct.2012.12.015

    Article  CAS  PubMed  Google Scholar 

  • Salmela, H., Amdam, G. V., & Freitak, D. (2015). Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin. PLOS Pathogens, 11(7), Article e1005015. https://doi.org/10.1371/journal.ppat.1005015

  • Sanchez-Bayo, F., & Goka, K. (2014). Pesticide Residues and Bees – A Risk Assessment. PLoS One, 9(4), Article e94482. https://doi.org/10.1371/journal.pone.0094482

  • Sanchez-Bayo, F., Goulson, D., Pennacchio, F., Nazzi, F., Goka, K., & Desneux, N. (2016). Are bee diseases linked to pesticides? - A brief review. Environment International, 89–90, 7–11. https://doi.org/10.1016/j.envint.2016.01.009

    Article  CAS  PubMed  Google Scholar 

  • Sharma, A., Kumar, V., Shahzad, B., Tanveer, M., Sidhu, G. P. S., Handa, N., & Thukral, A. K. (2019). Worldwide pesticide usage and its impacts on ecosystem. SN Applied Sciences, 1, Article 1446. https://doi.org/10.1007/s42452-019-1485-1

  • Sivakoff, F. S., & Gardiner, M. M. (2017). Soil lead contamination decreases bee visit duration at sunflowers. Urban Ecosystems, 20, 1221–1228. https://doi.org/10.1007/s11252-017-0674-1

    Article  Google Scholar 

  • Siviter, H., Bailes, E. J., Martin, C. D., Oliver, T. R., Koricheva, J., Leadbeater, E., & Brown, M. J. F. (2021). Agrochemicals interact synergistically to increase bee mortality. Nature, 596(7872), 389–392. https://doi.org/10.1038/s41586-021-03787-7

    Article  CAS  PubMed  Google Scholar 

  • Stout, M. J. (2014). Chapter 1 - Host-Plant Resistance in Pest Management. In D. P. Abrol (Ed.), Integrated Pest Management (pp. 1–21). Academic Press. https://doi.org/10.1016/B978-0-12-398529-3.00002-6

  • Tang, J., Ma, C., Shi, W., Chen, X., Liu, Z., Wang, H., & Chen, C. (2020). A National Survey of Managed Honey Bee Colony Winter Losses (Apis mellifera) in China (2013–2017). Diversity, 12(9), Article 318. https://doi.org/10.3390/d12090318

  • Thomas, J. M., & Simmons, M. A. (1991). Population dynamics of honey bee nucleus colonies exposed to industrial pollutants. Apidologie, 22, 359–369. https://doi.org/10.1051/apido:19910401

    Article  Google Scholar 

  • Traynor, K. S., Tosi, S., Rennich, K., Steinhauer, N., Forsgren, E., Rose, R., & vanEngelsdorp, D. (2021). Pesticides in honey bee colonies: Establishing a baseline for real world exposure over seven years in the USA. Environmental Pollution, 279, Article 116566. https://doi.org/10.1016/j.envpol.2021.116566

  • Ullah, A., Tlak Gajger, I., Majoros, A., Dar, S. A., Khan, S., & Kalimullah, … Anjum, S. I. (2021). Viral impacts on honey bee populations: A review. Saudi Journal of Biological Sciences, 28(1), 523–530. https://doi.org/10.1016/j.sjbs.2020.10.037

    Article  CAS  PubMed  Google Scholar 

  • Vanegas, M. (2017). The silent beehive: How the decline of honey bee populations shifted the environmental protection agency's pesticide policy towards pollinators. Ecology Law Quarterly, 44(2), 311–341. https://doi.org/10.15779/Z38GQ6R199

  • Vanengelsdorp, D., & Meixner, M. D. (2009). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, 103, S80–S95. https://doi.org/10.1016/j.jip.2009.06.011

    Article  PubMed  Google Scholar 

  • Veres, A., Wyckhuys, K. A. G., Kiss, J., Toth, F., Burgio, G., Pons, X., & Furlan, L. (2020). An update of the Worldwide Integrated Assessment (WIA) on systemic pesticides. Part 4: Alternatives in major cropping systems. Environmental science and pollution research international, 27(24), 29867–29899. https://doi.org/10.1007/s11356-020-09279-x

  • Vilarem, C., Piou, V., Vogelweith, F., & Vetillard, A. (2021). Varroa destructor from the Laboratory to the Field: Control, Biocontrol and IPM Perspectives-A Review. Insects, 12(9), Article 800. https://doi.org/10.3390/insects12090800

  • Vu, P. D., Rault, L. C., Jenson, L. J., Bloomquist, J. R., & Anderson, T. D. (2020). Voltage-gated chloride channel blocker DIDS as an acaricide for Varroa mites. Pesticide Biochemistry and Physiology, 167, Article 104603. https://doi.org/10.1016/j.pestbp.2020.104603

  • Wang, D., Wang, S., Bai, L., Nasir, M. S., Li, S., & Yan, W. (2020a). Mathematical modeling approaches for assessing the joint toxicity of chemical mixtures based on luminescent bacteria: a systematic review. Frontiers in Microbiology, 11, Article 1651. https://doi.org/10.3389/fmicb.2020.01651

  • Wang, Y., Zhu, Y. C., & Li, W. (2020b). Comparative examination on synergistic toxicities of chlorpyrifos, acephate, or tetraconazole mixed with pyrethroid insecticides to honey bees (Apis mellifera L.). Environmental Science and Pollution Research International, 27(7), 6971–6980. https://doi.org/10.1007/s11356-019-07214-3

  • Wang, Y., Zhu, Y.-C., Li, W., Yao, J., Reddy, G. V. P., & Lv, L. (2021). Binary and ternary toxicological interactions of clothianidin and eight commonly used pesticides on honey bees (Apis mellifera). Ecotoxicology and Environmental Safety, 223, 112563–112563. https://doi.org/10.1016/j.ecoenv.2021.112563

    Article  CAS  PubMed  Google Scholar 

  • Wernecke, A., Frommberger, M., Forster, R., & Pistorius, J. (2019). Lethal effects of various tank mixtures including insecticides, fungicides and fertilizers on honey bees under laboratory, semi-field and field conditions. Journal of Consumer Protection and Food Safety, 14(3), 239–249. https://doi.org/10.1007/s00003-019-01233-5

    Article  Google Scholar 

  • Williams, N. M., Gaines, H., Ascher, J. S., & Kremen, C. (2008). Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. Journal of Applied Ecology, 45, 793–802. https://doi.org/10.1111/j.1365-2664.2007.01418.x

    Article  Google Scholar 

  • Wu, S., Nomura, Y., Du, Y., Zhorov, B. S., & Dong, K. (2017). Molecular basis of selective resistance of the bumblebee BiNav1 sodium channel to tau-fluvalinate. Proceedings of the National Academy of Sciences of the United States of America, 114(49), 12922–12927. https://doi.org/10.1073/pnas.1711699114

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xun, E., Zhang, Y., Zhao, J., & Guo, J. (2017). Translocation of heavy metals from soils into floral organs and rewards of Cucurbita pepo: Implications for plant reproductive fitness. Ecotoxicology and Environmental Safety, 145, 235–243. https://doi.org/10.1016/j.ecoenv.2017.07.045

    Article  CAS  PubMed  Google Scholar 

  • Yanez, O., Piot, N., Dalmon, A., de Miranda, J. R., Chantawannakul, P., Panziera, D., & Chejanovsky, N. (2020). Bee Viruses: Routes of Infection in Hymenoptera. Frontiers in Microbiology, 11, Article 943. https://doi.org/10.3389/fmicb.2020.00943

  • Yao, J., Zhu, Y. C., & Adamczyk, J. (2018a). Responses of Honey Bees to Lethal and Sublethal Doses of Formulated Clothianidin Alone and Mixtures. Journal of Economic Entomology, 111(4), 1517–1525. https://doi.org/10.1093/jee/toy140

    Article  CAS  PubMed  Google Scholar 

  • Yao, J., Zhu, Y. C., Adamczyk, J., & Luttrell, R. (2018b). Influences of acephate and mixtures with other commonly used pesticides on honey bee (Apis mellifera) survival and detoxification enzyme activities. Comparative Biochemistry and Physiology Part c: Toxicology & Pharmacology, 209, 9–17. https://doi.org/10.1016/j.cbpc.2018.03.005

    Article  CAS  Google Scholar 

  • Zaluski, R., Kadri, S. M., Alonso, D. P., Martins Ribolla, P. E., & de Oliveira Orsi, R. (2015). Fipronil promotes motor and behavioral changes in honey bees (Apis mellifera) and affects the development of colonies exposed to sublethal doses. Environmental Toxicology and Chemistry, 34(5), 1062–1069. https://doi.org/10.1002/etc.2889

    Article  CAS  PubMed  Google Scholar 

  • Zhang, G., Ma, L., Zhang, W., Liu, F., & Xu, B. (2015). Effects of calcium, magnesium, iron and zinc on the viability of honeybees. Journal of Bee, 6, 1–4.

    Google Scholar 

  • Zwolak, A., Sarzyńska, M., Szpyrka, E., & Stawarczyk, K. (2019). Sources of Soil Pollution by Heavy Metals and Their Accumulation in Vegetables: a Review. Water, Air, & Soil Pollution, 230, Article 164. https://doi.org/10.1007/s11270-019-4221-y

Download references

Acknowledgements

This work was supported by Distinguished Professor Grant in Nanjing University of Chinese Medicine (No. 013038019015).

Funding

Distinguished Professor Grant in Nanjing University of Chinese Medicine,013038019015,Jing Chen

Author information

Authors and Affiliations

  1. School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, 210023, China

    Yinying Yang, Yuzheng Wu, Hexuan Long, Xuelin Ma, Liang Guo, Yang Pan, Peng Cao & Jing Chen

  2. Department of Biological and Environmental Engineering, Cornell University, Ithaca, NY, 14853, USA

    Kaavian Shariati & Minglin Ma

  3. Beemmunity Inc, Boulder, CO, 80304, USA

    James Webb

  4. Science, Biomedical Polymers Laboratory, College of Chemistry, Chemical Engineering and Materials, Soochow University, Suzhou, 215123, China

    Chao Deng

  5. Affiliated Hospital of Integrated Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing, 210028, China

    Peng Cao

Authors
  1. Yinying Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuzheng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hexuan Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xuelin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kaavian Shariati
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. James Webb
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Liang Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yang Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Minglin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Chao Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Peng Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Peng Cao or Jing Chen.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

The original online version of this article was revised: In this article the author name Xuelin Ma was incorrectly written as Xueling Ma.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Wu, Y., Long, H. et al. Global honeybee health decline factors and potential conservation techniques. Food Sec. 15, 855–875 (2023). https://doi.org/10.1007/s12571-023-01346-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12571-023-01346-8

Keywords

Search

Navigation