Biotic and abiotic stresses on honeybee health

Abstract

Honeybees are the most critical pollinators providing key ecosystem services that underpin crop production and sustainable agriculture. Amidst a backdrop of rapid global change, this eusocial insect encounters a succession of stressors during nesting, foraging, and pollination. Ectoparasitic mites, together with vectored viruses, have been recognized as central biotic threats to honeybee health, while the spread of invasive giant hornets and small hive beetles also increasingly threatens colonies worldwide. Cocktails of agrochemicals, including acaricides used for mite treatment, and other pollutants of the environment have been widely documented to affect bee health in various ways. Additionally, expanding urbanization, climate change, and agricultural intensification often result in the destruction or fragmentation of flower-rich bee habitats. The anthropogenic pressures exerted by beekeeping management practices affect the natural selection and evolution of honeybees, and colony translocations facilitate alien species invasion and disease transmission. In this review, the multiple biotic and abiotic threats and their interactions that potentially undermine bee colony health are discussed, while taking into consideration the sensitivity, large foraging area, dense network among related nestmates, and social behaviors of honeybees.

Keywords

abiotic stressor / Apis / biotic stressor / colony losses / interaction effect / pollinator decline

References

[1] Acosta-Reyes F, Neupane R, Frank J, Fernández IS (2019). The Israeli acute paralysis virus IRES captures host ribosomes by mimicking a ribosomal state with hybrid tRNAs. The EMBO Journal 38, e102226.

[2] Aizen MA, Aguiar S, Biesmeijer JC et al. (2019). Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification. Global Change Biology 25, 3516–27.

[3] Al Naggar Y, Dabour K, Masry S, Sadek A, Naiem E, Giesy JP (2020). Sublethal effects of chronic exposure to CdO or PbO nanoparticles or their binary mixture on the honey bee (Apis millefera L.). Environmental Science and Pollution Research 27, 19004–15.

[4] Alonso-Salces RM, Cugnata NM, Guaspari E et al. (2017). Natural strategies for the control of Paenibacillus larvae, the causative agent of American foulbrood in honey bees: a review. Apidologie 48, 387–400.

[5] Amdam GV, Norberg K, Hagen A, Omholt SW (2003). Social exploitation of vitellogenin. PNAS 100, 1799–802.

[6] Anbumani S, Kakkar P (2018). Ecotoxicological effects of microplastics on biota: A review. Environmental Science and Pollution Research 25, 14373–96.

[7] Annoscia D, Di Prisco G, Becchimanzi A et al. (2020). Neonicotinoid clothianidin reduces honey bee immune response and contributes to Varroa mite proliferation. Nature Communications 11, 5887.

[8] Arrese EL, Soulages JL (2010). Insect fat body: Energy, metabolism, and regulation. Annual Review of Entomology 55, 207–25.

[9] Aufauvre J, Biron DG, Vidau C et al. (2012). Parasite-insecticide interactions: A case study of Nosema ceranae and fipronil synergy on honeybee. Scientific Reports 2, 326.

[10] Balzani P, Galeotti G, Scheggi S, Masoni A, Santini G, Baracchi D (2022). Acute and chronic ingestion of polyethylene (PE) microplastics has mild effects on honey bee health and cognition. Environmental Pollution 305, 119318.

[11] Barbet-Massin M, Rome Q, Muller F, Perrard A, Villemant C, Jiguet F (2013). Climate change increases the risk of invasion by the yellow-legged hornet. Biological Conservation 157, 4–10.

[12] Bargańska Ż, Ślebioda M, Namieśnik J (2016). Honey bees and their products: Bioindicators of environmental contamination. Critical Reviews in Environmental Science and Technology 46, 235–48.

[13] Beaurepaire A, Piot N, Doublet V et al. (2020). Diversity and global distribution of viruses of the western honey bee, Apis mellifera. Insects 11, 239.

[14] Ben Abdelkader F, Çakmak İ, Çakmak SS et al. (2021). Toxicity assessment of chronic exposure to common insecticides and bee medications on colony development and drones sperm parameters. Ecotoxicology 30, 806–17.

[15] Britton NF, Jane White KA (2021). The effect of covert and overt infections on disease dynamics in honey-bee colonies. Bulletin of Mathematical Biology 83, 67.

[16] Brown A, Rodriguez V, Pfister J, Perreten V, Neumann P, Retschnig G (2022). The dose makes the poison: feeding of antibiotic-treated winter honey bees. Apis mellifera, with probiotics and b-vitamins. Apidologie 53, 19.

[17] Buawangpong N, De Guzman LI, Khongphinitbunjong K, Frake AM, Burgett M, Chantawannakul P (2015). Prevalence and reproduction of Tropilaelaps mercedesae and Varroa destructor in concurrently infested Apis mellifera colonies. Apidologie 46, 779–86.

[18] Buteler M, Alma AM, Stadler T, Gingold AC, Manattini MC, Lozada M (2022). Acute toxicity of microplastic fibers to honeybees and effects on foraging behavior. Science of the Total Environment 822, 153320.

[19] Büchler R, Berg S, Le Conte Y (2010). Breeding for resistance to Varroa destructor in Europe. Apidologie 41, 393–408.

[20] Bąk B, Wilde J (2015). Grooming behavior by worker bees of various subspecies of honey bees to remove Varroa destructor mites. Journal of Apicultural Research 54, 207–15.

[21] Burden CM (2016). Sublethal effects of heavy metal and metalloid exposure in honey bees: behavioral modifications and potential mechanisms (Thesis). Arizona State University, Phoenix, Arizona.

[22] Capitani G, Papa G, Pellecchia M, Negri I (2021). Disentangling multiple PM emission sources in the Po Valley (Italy) using honey bees. Heliyon 7, e06194.

[23] Castelli L, Branchiccela B, Garrido M et al. (2020). Impact of nutritional stress on honeybee gut microbiota, immunity, and Nosema ceranae Infection. Microbial Ecology 80, 908–19.

[24] Cebotari V, Buzu I, Postolachi O (2019). Impact of climate change of air temperature on vital activity of the bee families. Scientific Papers Series D Animal Science 62, 249–55.

[25] Chaimanee V, Evans JD, Chen Y, Jackson C, Pettis JS (2016). Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. Journal of Insect Physiology 89, 1–8.

[26] Chantawannakul P, Ramsey S, Vanengelsdorp D, Khongphinitbunjong K, Phokasem P (2018). Tropilaelaps mite: An emerging threat to European honey bee. Current Opinion in Insect Science 26, 69–75.

[27] Chen Y, Evans J, Feldlaufer M (2006a). Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. Journal of Invertebrate Pathology 92, 152–9.

[28] Chen Y, Evans JD, Smith IB, Pettis JS (2008). Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology 97, 186–8.

[29] Chen YP, Pettis JS, Collins A, Feldlaufer MF (2006b). Prevalence and transmission of honeybee viruses. Applied and Environmental Microbiology 72, 606–11.

[30] Cho Y, Jeong S, Lee D et al. (2021). Foraging trip duration of honeybee increases during a poor air quality episode and the increase persists thereafter. Ecology and Evolution 11, 1492–500.

[31] Cilia G, Bortolotti L, Albertazzi S, Ghini S, Nanetti A (2022). Honey bee (Apis mellifera L.) colonies as bioindicators of environmental SARS-CoV-2 occurrence. Science of The Total Environment 805, 150327.

[32] Cornelissen B, Neumann P, Schweiger O (2019). Global warming promotes biological invasion of a honey bee pest. Global Change Biology 25, 3642–55.

[33] Costa A, Veca M, Barberis M et al. (2019). Heavy metals on honeybees indicate their concentration in the atmosphere. A proof of concept. Italian Journal of Animal Science 18, 309–15.

[34] Costa CP, Leza M, Duennes MA et al. (2022). Pollen diet mediates how pesticide exposure impacts brain gene expression in nest-founding bumble bee queens. Science of the Total Environment 833, 155216.

[35] Cox KD, Covernton GA, Davies HL, Dower JF, Juanes F, Dudas SE (2019). Human consumption of microplastics. Environmental Science & Technology 53, 7068–74.

[36] Crowl TA, Crist TO, Parmenter RR, Belovsky G, Lugo AE (2008). The spread of invasive species and infectious disease as drivers of ecosystem change. Frontiers in Ecology and the Environment 6, 238–46.

[37] Cunningham MM, Tran L, Mckee CG et al. (2022). Honey bees as biomonitors of environmental contaminants, pathogens, and climate change. Ecological Indicators 134, 108457.

[38] Dargas JHF, Chaves SR, Fischer E (2016). Pollination of lark daisy on roadsides declines as traffic speed increases along an Amazonian highway. Plant Biology 18, 542–4.

[39] De Guzman LI, Williams GR, Khongphinitbunjong K, Chantawannakul P (2017). Ecology, life history, and management of Tropilaelaps mites. Journal of Economic Entomology 110, 319–32.

[40] De Jong D, Morse RA, Eickwort GC (1982). Mite pests of honey bees. Annual Review of Entomology 27, 229–52.

[41] De Jongh EJ, Harper SL, Yamamoto SS et al. (2022). One Health, One Hive: A scoping review of honey bees, climate change, pollutants, and antimicrobial resistance. PLoS ONE 17, e0242393.

[42] De León-Door AP, Pérez-Ordóñez G, Romo-Chacón A et al. (2020). Pathogenesis, epidemiology and variants of Melissococcus plutonius, the causal agent of European foulbrood. Journal of Apicultural Science 64, 173–88.

[43] Deng Y, Jiang X, Zhao H et al. (2021). Microplastic polystyrene ingestion promotes the susceptibility of honeybee to viral infection. Environmental Science & Technology 55, 11680–92.

[44] Deng Y, Yang S, Zhao H, Luo J, Yang W, Hou C (2022). Antibiotics-induced changes in intestinal bacteria result in the sensitivity of honey bee to virus. Environmental Pollution 314, 120278.

[45] Deroost K, Pham T-T, Opdenakker G, Van Den Steen PE (2015). The immunological balance between host and parasite in malaria. FEMS Microbiology Reviews 40, 208–57.

[46] Desneux N, Decourtye A, Delpuech J-M (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52, 81–106.

[47] Devi S, Rana K, Negi N, Sharma HK, Thakur M (2021). Seasonal incidence of brood diseases in hives of Asian honey bee (Apis cerana F.) correlates with colony and weather parameters. The Pharma Innovation Journal 10, 1945–51.

[48] Di Prisco G, Annoscia D, Margiotta M et al. (2016). A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. PNAS 113, 3203–8.

[49] Di Prisco G, Cavaliere V, Annoscia D et al. (2013). Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. PNAS 110, 18466–71.

[50] Di Prisco G, Pennacchio F, Caprio E, Boncristiani HF Jr, Evans JD, Chen Y (2011). Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. Journal of General Virology 92, 151–5.

[51] Diaz-Basantes MF, Conesa JA, Fullana A (2020). Microplastics in honey, beer, milk and refreshments in Ecuador as emerging contaminants. Sustainability 12, 5514.

[52] Dickel F, Bos NMP, Hughes H et al. (2022). The oral vaccination with Paenibacillus larvae bacterin can decrease susceptibility to American Foulbrood infection in honey bees-A safety and efficacy study. Frontiers in Veterinary Science 9, 946237.

[53] Dietemann V, Pflugfelder J, Anderson D et al. (2012). Varroa destructor: Research avenues towards sustainable control. Journal of Apicultural Research 51, 125–32.

[54] Dolezal AG, Toth AL (2018). Feedbacks between nutrition and disease in honey bee health. Current Opinion in Insect Science 26, 114–9.

[55] DÈmares FJ, Crous KL, Pirk CWW, Nicolson SW, Human H (2016). Sucrose sensitivity of honey bees is differently affected by dietary protein and a neonicotinoid pesticide. PLoS ONE 11, e0156584.

[56] Edo C, Fernández-Alba AR, Vejsnæs F, Van Der Steen JJM, Fernández-Piñas F, Rosal R (2021). Honeybees as active samplers for microplastics. Science of The Total Environment 767, 144481.

[57] Eiri DM, Nieh JC (2012). A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. Journal of Experimental Biology 215, 2022–9.

[58] Evans JD, Lopez DL (2004). Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 97, 752–6.

[59] Evans JD, Mckenna D, Scully E et al. (2018). Genome of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae), a worldwide parasite of social bee colonies, provides insights into detoxification and herbivory. GigaScience 7, giy138.

[60] Feldhaar H, Otti O (2020). Pollutants and their interaction with diseases of social hymenoptera. Insects 11, 153.

[61] Fijen TPM, Scheper JA, Boom TM, Janssen N, Raemakers I, Kleijn D (2018). Insect pollination is at least as important for marketable crop yield as plant quality in a seed crop. Ecology Letters 21, 1704–13.

[62] Fisher A, Rangel J (2018). Exposure to pesticides during development negatively affects honey bee (Apis mellifera) drone sperm viability. PLoS ONE 13, e0208630.

[63] Flores JM, Gil-Lebrero S, Gámiz V, Rodríguez MI, Ortiz MA, Quiles FJ (2019). Effect of the climate change on honey bee colonies in a temperate Mediterranean zone assessed through remote hive weight monitoring system in conjunction with exhaustive colonies assessment. Science of The Total Environment 653, 1111–9.

[64] Forrest JRK (2015). Plant–pollinator interactions and phenological change: What can we learn about climate impacts from experiments and observations? Oikos 124, 4–13.

[65] Gajda AM, Mazur ED, Bober AM, Czopowicz M (2021). Nosema ceranae interactions with Nosema apis and black queen cell virus. Agriculture 11, 963.

[66] Gao J, Ma S, Wang X et al. (2021). Tropilaelaps mercedesae parasitism changes behavior and gene expression in honey bee workers. PLoS Pathogens 17, e1009684.

[67] Garibaldi LA, Sáez A, Aizen MA, Fijen T, Bartomeus I (2020). Crop pollination management needs flower–visitor monitoring and target values. Journal of Applied Ecology 57, 664–70.

[68] Geslin B, Gauzens B, Baude M et al. (2017). Chapter Four—Massively introduced managed species and their consequences for plant–pollinator interactions. Advances in Ecological Research 57, 147–99.

[69] Ghazoul J (2005). Buzziness as usual? Questioning the global pollination crisis. Trends in Ecology & Evolution 20, 367–73.

[70] Gleadow R, Hanan J, Dorin A (2019). Averting robo-bees: Why free-flying robotic bees are a bad idea. Emerging Topics in Life Sciences 3, 723–9.

[71] Gong H, Chen X, Chen Y et al. (2016). Evidence of Apis cerana Sacbrood virus infection in Apis mellifera. Applied and Environmental Microbiology 82, 2256–62.

[72] Goretti E, Pallottini M, Rossi R et al. (2020). Heavy metal bioaccumulation in honey bee matrix, an indicator to assess the contamination level in terrestrial environments. Environmental Pollution 256, 113388.

[73] Goulson D, Nicholls E (2022). Anthropogenic influences on bee foraging. Science 375, 970–2.

[74] Goulson D, Nicholls E, Botías C, Rotheray EL (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957.

[75] Grindrod I, Martin SJ (2021). Spatial distribution of recapping behaviour indicates clustering around Varroa infested cells. Journal of Apicultural Research 60, 707–16.

[76] Grozinger CM, Flenniken ML (2019). Bee viruses: Ecology, pathogenicity, and impacts. Annual Review of Entomology 64, 205–26.

[77] Guo Y, Goodman CL, Stanley DW, Bonning BC (2020). Cell lines for honey bee virus research. Viruses 12, 236.

[78] Gutiérrez M, Molero R, Gaju M, Van Der Steen J, Porrini C, Ruiz JA (2020). Assessing heavy metal pollution by biomonitoring honeybee nectar in Córdoba (Spain). Environmental Science and Pollution Research 27, 10436–48.

[79] Hassler EE, Cazier JA, Hopkins B, Wilkes JT, Smith K, Rünzel M (2021). A century of discovery: Mining 100 years of honey bee research. Journal of Apicultural Research 60, 3–12.

[80] Hegland SJ, Nielsen A, Lázaro A, Bjerknes A-L, Totland Ø (2009). How does climate warming affect plant-pollinator interactions? Ecology Letters 12, 184–95.

[81] Henry M, Beguin M, Requier F et al. (2012). A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–50.

[82] Herrero-Latorre C, Barciela-García J, García-Martín S, Peña-Crecente RM (2017). The use of honeybees and honey as environmental bioindicators for metals and radionuclides: A review. Environmental Reviews 25, 463–80.

[83] Higes M, Martín-Hernández R, Botías C et al. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology 10, 2659–69.

[84] Hopkins BK, Herr C, Sheppard WS (2012). Sequential generations of honey bee (Apis mellifera) queens produced using cryopreserved semen. Reproduction, Fertility and Development 24, 1079–83.

[85] Hristov P, Shumkova R, Palova N, Neov B (2020). Factors associated with honey bee colony losses: A mini-review. Veterinary Sciences 7, 166.

[86] Hulme PE (2014). Invasive species challenge the global response to emerging diseases. Trends in Parasitology 30, 267–70.

[87] Idrissou FO, Huang Q, Yañez O, Neumann P (2019). International beeswax trade facilitates small hive beetle invasions. Scientific Reports 9, 10665.

[88] Jaffé R, Veiga JC, Pope NS et al. (2019). Landscape genomics to the rescue of a tropical bee threatened by habitat loss and climate change. Evolutionary Applications 12, 1164–77.

[89] Jamal ZA, Abou-Shaara HF, Qamer S et al. (2021). Future expansion of small hive beetles, Aethina tumida, towards North Africa and South Europe based on temperature factors using maximum entropy algorithm. Journal of King Saud University - Science 33, 101242.

[90] Kairo G, Provost B, Tchamitchian S et al. (2016). Drone exposure to the systemic insecticide Fipronil indirectly impairs queen reproductive potential. Scientific Reports 6, 319.

[91] Kakumanu ML, Reeves AM, Anderson TD, Rodrigues RR, Williams MA (2016). Honey bee gut microbiome is altered by in-hive pesticide exposures. Frontiers in Microbiology 7, 1255.

[92] Kalynych S, Füzik T, Přidal A, De Miranda J, Plevka P (2017). Cryo-EM study of slow bee paralysis virus at low pH reveals iflavirus genome release mechanism. PNAS 114, 598–603.

[93] Keeler AM, Rose-Person A, Rafferty NE (2021). From the ground up: Building predictions for how climate change will affect belowground mutualisms, floral traits, and bee behavior. Climate Change Ecology 1, 100013.

[94] Khalifa SAM, Elshafiey EH, Shetaia AA et al. (2021). Overview of bee pollination and its economic value for crop production. Insects 12, 688.

[95] Kraus B, Page RE Jr (1995). Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral Apis mellifera (Hymenoptera: Apidae) in California. Environmental Entomology 24, 1473–80.

[96] Kwong WK, Moran NA (2016). Gut microbial communities of social bees. Nature Reviews Microbiology 14, 374–84.

[97] Le Conte Y, Meixner MD, Brandt A et al. (2020). Geographical distribution and selection of european honey bees resistant to Varroa destructor. Insects 11, 873.

[98] Leclercq G, Pannebakker B, Gengler N, Nguyen BK, Francis F (2017). Drawbacks and benefits of hygienic behavior in honey bees (Apis mellifera L.): A review. Journal of Apicultural Research 56, 366–75.

[99] Leong M, Ponisio LC, Kremen C, Thorp RW, Roderick GK (2016). Temporal dynamics influenced by global change: Bee community phenology in urban, agricultural, and natural landscapes. Global Change Biology 22, 1046–53.

[100] Lin Z, Page P, Li L et al. (2016). Go east for better honey bee health: Apis cerana is faster at hygienic behavior than A. mellifera. PLoS ONE 11, e0162647.

[101] Lin Z, Qin Y, Page P et al. (2018). Reproduction of parasitic mites Varroa destructor in original and new honeybee hosts. Ecology and Evolution 8, 2135–45.

[102] Lin Z, Wang S, Neumann P et al. (2021a). Population genetics and host specificity of Varroa destructor mites infesting eastern and western honeybees. Journal of Pest Science 94, 1487–504.

[103] Lin Z, Zhang N, Wang Z et al. (2022). Acute and chronic viruses mediated by an ectoparasite targeting different developmental stages of honeybee (Apis mellifera and Apis cerana) brood. Frontiers in Veterinary Science 9, 951159.

[104] Lin Z, Zhao L, Cao L et al. (2021b). A survey of common pathogens of Apis spp. In wild non-cave honeybees in Southwest China. Journal of Wildlife Diseases 57, 932–5.

[105] Lindgren E, Andersson Y, Suk JE, Sudre B, Semenza JC (2012). Monitoring EU emerging infectious disease risk due to climate change. Science 336, 418–9.

[106] Locke B (2016). Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 47, 467–82.

[107] Lin Z, Zhu Z, Zhuang M et al. (2023). Effects of local domestication warrant attention in honey bee population genetics. Science Advances 9, eade7917.

[108] Mallinger RE, Gaines-Day HR, Gratton C (2017). Do managed bees have negative effects on wild bees?: A systematic review of the literature. PLoS ONE 12, e0189268.

[109] Mammo FK, Amoah ID, Gani KM et al. (2020). Microplastics in the environment: Interactions with microbes and chemical contaminants. Science of The Total Environment 743, 140518.

[110] Mao W, Schuler MA, Berenbaum MR (2013). Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. PNAS 110, 8842–6.

[111] Marshman J, Blay-Palmer A, Landman K (2019). Anthropocene crisis: Climate change, pollinators, and food security. Environments 6, 22.

[112] Martin SJ, Highfield AC, Brettell L et al. (2012). Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–6.

[113] Martín-Hernández R, Bartolomé C, Chejanovsky N et al. (2018). Nosema ceranae in Apis mellifera: A 12 years postdetection perspective. Environmental Microbiology 20, 1302–29.

[114] Mcafee A, Chapman A, Higo H et al. (2020). Vulnerability of honey bee queens to heat-induced loss of fertility. Nature Sustainability 3, 367–76.

[115] Mccabe LM, Aslan CE, Cobb NS (2022). Decreased bee emergence along an elevation gradient: Implications for climate change revealed by a transplant experiment. Ecology 103, e03598.

[116] Mcdermott A (2021). To understand the plight of insects, entomologists look to the past. PNAS 118, e2018499117.

[117] Mcmenamin AJ, Flenniken ML (2018). Recently identified bee viruses and their impact on bee pollinators. Current Opinion in Insect Science 26, 120–9.

[118] Medrzycki P, Sgolastra F, Bortolotti L et al. (2010). Influence of brood rearing temperature on honey bee development and susceptibility to poisoning by pesticides. Journal of Apicultural Research 49, 52–9.

[119] Millard J, Outhwaite CL, Kinnersley R et al. (2021). Global effects of land-use intensity on local pollinator biodiversity. Nature Communications 12, 2902.

[120] Molina-Montenegro MA, Acuña-Rodríguez IS, Ballesteros GI et al. (2023). Electromagnetic fields disrupt the pollination service by honeybees. Science Advances 9, eadh1455.

[121] Mondet F, Alaux C, Severac D, Rohmer M, Mercer AR, Le Conte Y (2015). Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees. Scientific Reports 5, 10454.

[122] Morales MM, Ramos MJG, Vázquez PP et al. (2020). Distribution of chemical residues in the beehive compartments and their transfer to the honeybee brood. Science of The Total Environment 710, 136288.

[123] Moritz RFA, Härtel S, Neumann P (2005). Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Ecoscience 12, 289–301.

[124] Motta EV, Raymann K, Moran NA (2018). Glyphosate perturbs the gut microbiota of honey bees. PNAS 115, 10305–10.

[125] Muth F, Francis JS, Leonard AS (2019). Modality-specific impairment of learning by a neonicotinoid pesticide. Biology Letters 15, 20190359.

[126] Muth F, Leonard A (2019). A neonicotinoid pesticide impairs foraging, but not learning, in free-flying bumblebees. Scientific Reports 9, 4764.

[127] Nazzi F, Le Conte Y (2016). Ecology of Varroa destructor, the major ectoparasite of the western honey bee, Apis mellifera. Annual Review of Entomology 61, 417–32.

[128] Neumann P, Blacquière T (2017). The Darwin cure for apiculture? Natural selection and managed honeybee health. Evolutionary Applications 10, 226–30.

[129] Neumann P, Carreck N (2010). Honey bee colony losses. Journal of Apicultural Research 49, 1–6.

[130] Neumann P, Pettis JS, Schäfer MO (2016). Quo vadis Aethina tumida? Biology and control of small hive beetles. Apidologie 47, 427–66.

[131] Nganso BT, Fombong AT, Yusuf AA, Pirk CWW, Stuhl C, Torto B (2017). Hygienic and grooming behaviors in African and European honeybees—New damage categories in Varroa destructor. PLoS ONE 12, e0179329.

[132] Nganso BT, Fombong AT, Yusuf AA, Pirk CWW, Stuhl C, Torto B (2018). Low fertility, fecundity and numbers of mated female offspring explain the lower reproductive success of the parasitic mite Varroa destructor in African honeybees. Parasitology 145, 1633–9.

[133] O'neal ST, Anderson TD, Wu-Smart JY (2018). Interactions between pesticides and pathogen susceptibility in honey bees. Current Opinion in Insect Science 26, 57–62.

[134] Oddie MA, Dahle B, Neumann P (2017). Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection. PeerJ 5, e3956.

[135] Oddie MAY, Burke A, Dahle B, Le Conte Y, Mondet F, Locke B (2021). Reproductive success of the parasitic mite (Varroa destructor) is lower in honeybee colonies that target infested cells with recapping. Scientific Reports 11, 9133.

[136] Odemer R, Alkassab AT, Bischoff G et al. (2020). Chronic high glyphosate exposure delays individual worker bee (Apis mellifera L.) development under field conditions. Insects 11, 664.

[137] Oldroyd BP (2007). What's killing American honey bees? PLoS Biology 5, e168.

[138] Page P, Lin Z, Buawangpong N et al. (2016). Social apoptosis in honey bee superorganisms. Scientific Reports 6, 27210.

[139] Papa G, Capitani G, Capri E, Pellecchia M, Negri I (2021). Vehicle-derived ultrafine particulate contaminating bees and bee products. Science of The Total Environment 750, 141700.

[140] Paray BA, Kumari I, Hajam YA et al. (2021). Honeybee nutrition and pollen substitutes: A review. Saudi Journal of Biological Sciences 28, 1167–76.

[141] Paris L, El Alaoui H, Delbac F, Diogon M (2018). Effects of the gut parasite Nosema ceranae on honey bee physiology and behavior. Current Opinion in Insect Science 26, 149–54.

[142] Paris L, Peghaire E, Moné A et al. (2020). Honeybee gut microbiota dysbiosis in pesticide/parasite co-exposures is mainly induced by Nosema ceranae. Journal of Invertebrate Pathology 172, 107348.

[143] Phillips BB, Bullock JM, Gaston KJ et al. (2021). Impacts of multiple pollutants on pollinator activity in road verges. Journal of Applied Ecology 58, 1017–29.

[144] Phillips BB, Wallace C, Roberts BR et al. (2020). Enhancing road verges to aid pollinator conservation: A review. Biological Conservation 250, 108687.

[145] Piot N, Schweiger O, Meeus I et al. (2022). Honey bees and climate explain viral prevalence in wild bee communities on a continental scale. Scientific Reports 12, 1904.

[146] Pirk CWW, Crewe RM, Moritz RFA (2017). Risks and benefits of the biological interface between managed and wild bee pollinators. Functional Ecology 31, 47–55.

[147] Pirk CWW, Strauss U, Yusuf A, Démares F, Human H (2016). Honeybee health in Africa—A review. Apidologie 47, 276–300.

[148] Porto RG, De Almeida RF, Cruz-Neto O et al. (2020). Pollination ecosystem services: A comprehensive review of economic values, research funding and policy actions. Food Security 12, 1425–42.

[149] Posada-Florez F, Sonenshine DE, Egekwu NI, Rice C, Lupitskyy R, Cook SC (2019). Insights into the metabolism and behaviour of Varroa destructor mites from analysis of their waste excretions. Parasitology 146, 527–32.

[150] Potts SG, Imperatriz-Fonseca V, Ngo HT et al. (2016). Safeguarding pollinators and their values to human well-being. Nature 540, 220–9.

[151] Potts SG, Neumann P, Vaissière B, Vereecken NJ (2018). Robotic bees for crop pollination: Why drones cannot replace biodiversity. Science of The Total Environment 642, 665–7.

[152] Preston DL, Mischler JA, Townsend AR, Johnson PTJ (2016). Disease ecology meets ecosystem science. Ecosystems 19, 737–48.

[153] Procházková M, FüZik T, Škubník K et al. (2018). Virion structure and genome delivery mechanism of sacbrood honeybee virus. PNAS 115, 7759–64.

[154] Procházková M, Škubník K, Füzik T, Mukhamedova L, Přidal A, Plevka P (2020). Virion structures and genome delivery of honeybee viruses. Current Opinion in Virology 45, 17–24.

[155] Pusceddu M, Cini A, Alberti S et al. (2021). Honey bees increase social distancing when facing the ectoparasite Varroa destructor. Science Advances 7, eabj1398.

[156] Quigley TP, Amdam GV, Harwood GH (2019). Honey bees as bioindicators of changing global agricultural landscapes. Current Opinion in Insect Science 35, 132–7.

[157] Ramsey S, Gulbronson CJ, Mowery J, Ochoa R, Vanengelsdorp D, Bauchan G (2018). A multi-microscopy approach to discover the feeding site and host tissue consumed by Varroa destructor on host honey bees. Microscopy and Microanalysis 24, 1258–9.

[158] Ramsey SD, Ochoa R, Bauchan G et al. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. PNAS 116, 1792–801.

[159] Rangel J, Tarpy DR (2015). The combined effects of miticides on the mating health of honey bee (Apis mellifera L.) queens. Journal of Apicultural Research 54, 275–83.

[160] Raven PH, Wagner DL (2021). Agricultural intensification and climate change are rapidly decreasing insect biodiversity. PNAS 118, e2002548117.

[161] Raymann K, Motta EV, Girard C, Riddington IM, Dinser JA, Moran NA (2018). Imidacloprid decreases honey bee survival rates but does not affect the gut microbiome. Applied and Environmental Microbiology 84, e00545–18.

[162] Requier F, Rome Q, Chiron G et al. (2019). Predation of the invasive Asian hornet affects foraging activity and survival probability of honey bees in Western Europe. Journal of Pest Science 92, 567–78.

[163] Rigaud T, Perrot-Minnot M-J, Brown MJF (2010). Parasite and host assemblages: Embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society B: Biological Sciences 277, 3693–702.

[164] Ryabov EV, Posada-Florez F, Rogers C et al. (2022). The vectoring competence of the mite Varroa destructor for deformed wing virus of honey bees is dynamic and affects survival of the mite. Frontiers in Insect Science 2, 931352.

[165] Sales K, Vasudeva R, Dickinson ME et al. (2018). Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nature Communications 9, 4771.

[166] Sayğı H (2020). Adverse effects of climate change on agriculture: An evaluation of fruit and honey bee farming. Asian Journal of Agriculture and Rural Development 10, 504–14.

[167] Seeley TD, Smith ML (2015). Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie 46, 716–27.

[168] Seibold S, Gossner MM, Simons NK et al. (2019). Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–4.

[169] Simeunovic P, Stevanovic J, Cirkovic D et al. (2014). Nosema ceranae and queen age influence the reproduction and productivity of the honey bee colony. Journal of Apicultural Research 53, 545–54.

[170] Siviter H, Bailes EJ, Martin CD et al. (2021). Agrochemicals interact synergistically to increase bee mortality. Nature 596, 389–92.

[171] Smith KE, Weis D (2022). Metal and Pb isotope characterization of particulates encountered by foraging honeybees in Metro Vancouver. Science of the Total Environment 826, 154181.

[172] Spurny R, Přidal A, Pálková L, Kiem HKT, De Miranda JR, Plevka P (2017). Virion structure of black queen cell virus, a common honeybee pathogen. Journal of Virology 91, e02100–16.

[173] Stanisavljević L, Partap U, IPBES (2016). Assessment report on pollinators, pollination and food production. IPBES, Bonn, Germany. https://digitallibrary.un.org/record/3794027.

[174] Steinhauer N, Kulhanek K, Antúnez K et al. (2018). Drivers of colony losses. Current Opinion in Insect Science 26, 142–8.

[175] Straub L, Villamar-Bouza L, Bruckner S, Chantawannakul P, Gauthier L, Khongphinitbunjong K (2016). Neonicotinoid insecticides can serve as inadvertent insect contraceptives. Proceedings of the Royal Society B: Biological Sciences 283, 20160506.

[176] Straub L, Villamar-Bouza L, Bruckner S, Chantawannakul P, Kolari E, Maitip J (2021). Negative effects of neonicotinoids on male honeybee survival, behaviour and physiology in the field. Journal of Applied Ecology 58, 2515–28.

[177] Straub L, Williams GR, Vidondo B, Khongphinitbunjong K, Retschnig G, Schneeberger A (2019). Neonicotinoids and ectoparasitic mites synergistically impact honeybees. Scientific Reports 9, 8159.

[178] Strauss U, Dietemann V, Human H, Crewe RM, Pirk CWW (2016). Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destructor. Parasitology 143, 374–87.

[179] Sánchez-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, 7–11.

[180] Škubník K, Nováček J, Füzik T, Přidal A, Paxton RJ, Plevka P (2017). Structure of deformed wing virus, a major honey bee pathogen. PNAS 114, 3210–5.

[181] Škubník K, Sukeník L, Buchta D et al. (2021). Capsid opening enables genome release of iflaviruses. Science Advances 7, eabd7130.

[182] Tabor JA, Koch JB (2021). Ensemble models predict invasive bee habitat suitability will expand under future climate scenarios in Hawai'i. Insects 12, 443.

[183] Tan K, Radloff SE, Li JJ et al. (2007). Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera. Naturwissenschaften 94, 469–72.

[184] Tan K, Wang C, Dong S, Li X, Nieh JC (2017). The pesticide flupyradifurone impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Scientific Reports 7, 17772.

[185] Teeters BS, Johnson RM, Ellis MD, Siegfried BD (2012). Using video-tracking to assess sublethal effects of pesticides on honey bees (Apis mellifera L.). Environmental Toxicology and Chemistry 31, 1349–54.

[186] Theisen-Jones H, Bienefeld K (2016). The Asian honey bee (Apis cerana) is significantly in decline. Bee World 93, 90–7.

[187] Thimmegowda GG, Mullen S, Sottilare K et al. (2020). A field-based quantitative analysis of sublethal effects of air pollution on pollinators. PNAS 117, 20653–61.

[188] Tihelka E (2018). Effects of synthetic and organic acaricides on honey bee health: A review. Slovenian Veterinary Research 55, 114–40.

[189] Tong L, Nieh JC, Tosi S (2019). Combined nutritional stress and a new systemic pesticide (flupyradifurone, Sivanto®) reduce bee survival, food consumption, flight success, and thermoregulation. Chemosphere 237, 124408.

[190] Traynor KS, Mondet F, De Miranda JR et al. (2020). Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends in Parasitology 36, 592–606.

[191] Tritschler M, Vollmann JJ, Yañez O, Chejanovsky N, Crailsheim K, Neumann P (2017). Protein nutrition governs within-host race of honey bee pathogens. Scientific Reports 7, 14988.

[192] Tsuruda JM, Chakrabarti P, Sagili RR (2021). Honey bee nutrition. Veterinary Clinics: Food Animal Practice 37, 505–19.

[193] Ullah A, Tlak Gajger I, Majoros A et al. (2021). Viral impacts on honey bee populations: A review. Saudi Journal of Biological Sciences 28, 523–30.

[194] Ulrich J, Bucher SF, Eisenhauer N et al. (2020). Invertebrate decline leads to shifts in plant species abundance and phenology. Frontiers in Plant Science 11, 542125.

[195] Van Der Sluijs JP (2020). Insect decline, an emerging global environmental risk. Current Opinion in Environmental Sustainability 46, 39–42.

[196] Vanbergen AJ, Espíndola A, Aizen MA (2018). Risks to pollinators and pollination from invasive alien species. Nature Ecology & Evolution 2, 16.

[197] Varela M, Spencer TE, Palmarini M, Arnaud F (2009). Friendly viruses: the special relationship between endogenous retroviruses and their host. Annals of the New York Academy of Sciences 1178, 157–72.

[198] Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015). Bee nutrition and floral resource restoration. Current Opinion in Insect Science 10, 133–41.

[199] Vercelli M, Novelli S, Ferrazzi P, Lentini G, Ferracini C (2021). A qualitative analysis of beekeepers’ perceptions and farm management adaptations to the impact of climate change on honey bees. Insects 12, 228.

[200] Villa JD, Danka RG, Harris JW (2009). Simplified methods of evaluating colonies for levels of Varroa Sensitive Hygiene (VSH). Journal of Apicultural Research 48, 162–7.

[201] Walsh BS, Parratt SR, Hoffmann AA et al. (2019). The impact of climate change on fertility. Trends in Ecology & Evolution 34, 249–59.

[202] Walsh EM, Sweet S, Knap A, Rangel J (2020). Queen honey bee (Apis mellifera) pheromone and reproductive behavior are affected by pesticide exposure during development. Behavioral Ecology and Sociobiology 74, 33.

[203] Wang K, Cai M, Sun J et al. (2023). Atrazine exposure can dysregulate the immune system and increase the susceptibility against pathogens in honeybees in a dose-dependent manner. Journal of Hazardous Materials 452, 131179.

[204] Wang K, Chen H, Fan RL et al. (2022). Effect of carbendazim on honey bee health: Assessment of survival, pollen consumption, and gut microbiome composition. Ecotoxicology and Environmental Safety 239, 113648.

[205] Wang K, Chen H, Lin ZG et al. (2021a). Carbendazim exposure during the larval stage suppresses major royal jelly protein expression in nurse bees (Apis mellifera). Chemosphere 266, 129011.

[206] Wang K, Li J, Zhao L et al. (2021b). Gut microbiota protects honey bees (Apis mellifera L.) against polystyrene microplastics exposure risks. Journal of Hazardous Materials 402, 123828.

[207] Wang S, Chen G, Lin Z, Wu Y, Hu F, Zheng H (2019). Occurrence of multiple honeybee viruses in the ectoparasitic mites Varroa spp. in Apis cerana colonies. Journal of Invertebrate Pathology 166, 107225.

[208] Wang S, Lin Z, Chen G et al. (2020). Reproduction of ectoparasitic mites in a coevolved system: Varroa spp.-Eastern honey bees, Apis cerana. Ecology and Evolution 10, 14359–71.

[209] Wei R, Cao L, Feng Y, Chen Y, Chen G, Zheng H (2022). Sacbrood virus: A growing threat to honeybees and wild pollinators. Viruses 14, 1871.

[210] Werenkraut V, Arbetman MP, Fergnani PN (2022). The Oriental hornet (Vespa orientalis L.): A threat to the Americas? Neotropical Entomology 51, 330–8.

[211] Wheeler MM, Robinson GE (2014). Diet-dependent gene expression in honey bees: Honey vs. sucrose or high fructose corn syrup. Scientific Reports 4, 5726.

[212] Wickramasinghe K, Mathers JC, Wopereis S, Marsman DS, Griffiths JC (2020). From lifespan to healthspan: The role of nutrition in healthy ageing. Journal of Nutritional Science 9, e33.

[213] Williams GR, Troxler A, Retschnig G et al. (2015). Neonicotinoid pesticides severely affect honey bee queens. Scientific Reports 5, 14621.

[214] Wilson CJ, Jamieson MA (2019). The effects of urbanization on bee communities depends on floral resource availability and bee functional traits. PLoS ONE 14, e0225852.

[215] Woolhouse ME, Taylor LH, Haydon DT (2001). Population biology of multihost pathogens. Science 292, 1109–12.

[216] Wu JY, Anelli CM, Sheppard WS (2011). Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS ONE 6, e14720.

[217] Young HS, Parker IM, Gilbert GS, Sofia Guerra A, Nunn CL (2017). Introduced species, disease ecology, and biodiversity–disease relationships. Trends in Ecology & Evolution 32, 41–54.

[218] Zhang Y, Kang S, Allen S, Allen D, Gao T, Sillanpää M (2020). Atmospheric microplastics: A review on current status and perspectives. Earth-Science Reviews 203, 103118.

[219] Zheng H, Lin Z, Huang S, Sohr A, Wu L, Chen YP (2014). Spore loads may not be used alone as a direct indicator of the severity of Nosema ceranae Infection in honey bees Apis mellifera (Hymenoptera:Apidae). Journal of Economic Entomology 107, 2037–44.

[220] Zhu G, Gutierrez Illan J, Looney C, Crowder DW (2020). Assessing the ecological niche and invasion potential of the Asian giant hornet. PNAS 117, 24646–8.

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