Honey bee colony losses: Why are honey bees disappearing?

Peter Hristov, Rositsa Shumkova, Nadezhda Palova, Boyko Neov

Abstract


The Western honey bee (Apis mellifera L., Hymenoptera: Apidae) is a species of crucial economic, agricultural and environmental importance.

In the last ten years, some regions of the world have suffered from a significant reduction of honey bee colonies. In fact, honey bee losses are not an unusual phenomenon, but in many countries worldwide there has been a notable decrease in honey bee families. The cases in the USA, in many European countries, and in the Middle East have received considerable attention, mostly due to the absence of an easily identifiable cause.

It has been difficult to determine the main factors leading to colony losses because of honey bees’ diverse social behavior. Moreover, in their daily routine, they make contact with many agents of the environment and are exposed to a plethora of human activities and their consequences. Nevertheless, a number of different factors are considered to be contributing to honey bee losses, and recent investigations have established some of the most important ones, in particular, pests and diseases, bee management, including bee keeping practices and breeding, the change in climatic conditions, agricultural practices, and the use of pesticides. The global picture highlights the ectoparasitic mite Varroa destructor as a major factor in colony loss. Last but not least, microsporidian parasites, mainly Nosema ceranae, also contribute to the problem.

Thus, it is obvious that many factors are involved in honey bee colony losses globally. Increased monitoring and scientific research should throw new light on the factors involved in recent honey bee colony losses.

This review focuses on the main factors which have been found to have an impact on the increase in honey bee colony losses.


Keywords


honey bee losses; colony collapse disorder; Varroa destructor, viral diseases, nosematosis, negative pressures

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References


Neumann, P.; Carreck, N.L. Honey bee colony losses. J. Apic. Res. 2010, 49, 1–6.

Taniguchi, T.; Kita, Y.; Matsumoto, T.; Kimura, K. Honeybee Colony Losses during 2008~2010 Caused by Pesticide Application in Japan. J. Apic. 2012, 27, 15-27.

Liu, Z.; Chen, C.; Niu, Q.; Qi, W.; Yuan, C.; Su, S.; Liu, S.; Zhang, Y.; Zhang, X.; Ji, T.; et al. Survey results of honey bee (Apis mellifera) colony losses in China (2010–2013). J. Apic. Res. 2016, 55, 29-37.

Al-Ghamdi, A.; Adgaba, N.; Getachew, A.; Tadesse, Y. New approach for determination of an optimum honeybee colony’s carrying capacity based on productivity and nectar secretion potential of bee forage species. Saudi J. Biol. Sci. 2016, 23, 92-100.

FAO. FAOSTAT Database. Food and Agriculture Organization of the United Nations 2009. Retrieved from http://www.fao.org/faostat/en/#home.

Potts, S.G.; Roberts, S.P.; Dean, R.; Marris, G.; Brown, M.A.; Jones, R.; Neumann, P.; Settele, J. Declines of managed honey bees and beekeepers in Europe. J. Apic. Res. 2010, 49, 15-22.

Sammataro, D.; Gerson, U.; Needham, G. Parasitic mites of honey bees: life history, implications, and impact. Annu. Rev. Entomol. 2000, 45, 519-548.

Dhooria, M.S. Parasitic Mites on Honeybees. In: Fundamentals of Applied Acarology. Springer, Singapore, 2016.

Shen, M.; Cui, L.; Ostiguy, N.; Cox-Foster, D. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. J. Gen. Virol. 2005, 86, 2281–2289.

Iwasaki, J.M.; Barratt, B.I.; Lord, J.M.; Mercer, A.R.; Dickinson, K.J. The New Zealand experience of varroa invasion highlights research opportunities for Australia. Ambio 2015, 44, 694–704.

Medina Flores, C.A.; Guzmán Novoa, E.; Hamiduzzaman, M.; Aréchiga Flores, C.F.; López Carlos, M.A. Africanized honey bees (Apis mellifera) have low infestation levels of the mite Varroa destructor in different ecological regions in Mexico. Genet. Mol. Res. 2014, 13, 7282-7293.

Oddie, M.; Büchler, R.; Dahle, B.; Kovacic, M.; Le Conte, Y.; Locke, B.; de Miranda, J.R.; Mondet, F.; Neumann, P. Rapid parallel evolution overcomes global honey bee parasite. Sci. Rep. 2018, 8, 7704.

Ramsey, S.D.; Ochoa, R.; Bauchan, G.; Gulbronson, C.; Mowery, J.D.; Cohen, A.; Lim, D.; Joklik, J.; Cicero, J.M.; Ellis, J.D.; et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. PNAS 2019, 116, 1792-1801.

Rinkevich, F.D.; Danka, R.G.; Healy, K.B. Influence of Varroa Mite (Varroa destructor) Management Practices on Insecticide Sensitivity in the Honey Bee (Apis mellifera). Insects 2017, 8, 9.

Peck, D.T.; Smith, M.L.; Seeley, T.D. Varroa destructor Mites Can Nimbly Climb from Flowers onto Foraging Honey Bees. PloS One 2016, 11, e0167798.

Oddie, M.; Dahle, B.; Neumann, P. Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection. PeerJ 2017, 5, e3956.

Floris, I.; Cabras, P.; Garau, V.L.; Minelli, E.V.; Satta, A.; Troullier, J. Persistence and effectiveness of pyrethroids in plastic strips against Varroa jacobsoni (Acari: Varroidae) and mite resistance in a Mediterranean area. J. Econ. Entomol. 2001, 94, 806-810.

Macedo, P.A.; Wu, J.; Ellis, M.D. Using inert dusts to detect and assess varroa infestations in honey bee colonies. J. Apic. Res. 2002, 41, 3-7.

Mozes-Koch, R.; Slabezki, Y.; Efrat, H.; Kalev, H.; Kamer, Y.; Yakobson, B.A.; Dag, A. First detection in Israel of fluvalinate resistance in the varroa mite using bioassay and biochemical methods. Exp. Appl. Acarol. 2000, 24, 35-43.

Rodríguez-Dehaibes, S.R.; Otero-Colina, G.; Sedas, V.P.; Jiménez, J.A.V. Resistance to amitraz and flumethrin in Varroa destructor populations from Veracruz, Mexico. J. Apic. Res. 2005, 44, 124-125.

Büchler, R.; Berg, S.; Le Conte, Y. Breeding for resistance to Varroa destructor in Europe. Apidologie 2010, 41, 393-408.

Elzen, P.J.; Westervelt, D. Detection of coumaphos resistance in Varroa destructor in Florida. Am. Bee J. 2002, 142, 291-292.

Spreafico, M.; Eördegh, F.R.; Bernardinelli, I.; Colombo, M. First detection of strains of Varroa destructor resistant to coumaphos. Results of laboratory tests and field trials. Apidologie 2001, 32, 49-55.

Elzen, P.J.; Baxter, J.R.; Spivak, M.; Wilson, W.T. Control of Varroa jacobsoni Oud. resistant to fluvalinate and amitraz using coumaphos. Apidologie 2000, 31, 437-441.

Gisder, S.; Genersch, E. Special issue: honey bee viruses. Viruses 2015, 7, 5603–5608.

Locke, B. Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 2016, 47, 467-482.

Tentcheva, D.; Gauthier, L.; Zappulla, N.; Dainat, B.; Cousserans, F.; Colin, M.E.; Bergoin, M. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol. 2004, 70, 7185–7291.

Nielsen, S.L.; Nicolaisen M.; Kryger, P. Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie 2008, 39, 310–314.

Levin, S.; Sela, N.; Chejanovsky, N. Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Sci. Rep. 2016, 6, 37710.

Francis, R. M.; Nielsen, S.L.; Kryger, P Patterns of viral infection in honey bee queens. J. Gen. Virol. 2013, 94, 668–676.

Paris, L.; El Alaoui, H.; Delbac, F.; Diogon, M. Effects of the gut parasite Nosema ceranae on honey bee physiology and behavior. Curr. Opin. Insect. Sci. 2018, 26, 149-154.

Fries, I.; Feng, F.; Da Silva, A.; Slemenda, S.B.; Pieniazek, N.J. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol. 1996, 32, 356-365.

Klee, J.; Besana, A.M.; Genersch, E.; Gisder, S.; Nanetti, A.; Tam, D.Q.; Chinh, T.X.; Puerta, F.; Ruz, J.M.; Kryger, P.; et al. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 2007, 96, 1-10.

Paxton, R.J.; Klee, J.; Korpela, S.; Fries, I. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007, 38, 558-565.

Chen, Y.P.; Evans, J.D.; Smith, I.B.; Pettis, J.S. Nosema ceranae is a long-present and widespread microsporidean infection of the European honey bee (Apis mellifera) in the United States. J. Invertebr. Pathol. 2008, 97, 186-188.

Invernizzi, C.; Abud, C.; Tomasco, I.H.; Harriet, J.; Ramallo, G.; Campa, J.; Katz, H.; Gardiol, G.; Mendoza, Y. Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. J. Invertebr. Pathol. 2009, 101, 150-153.

Stevanovic, J.; Stanimirovic, Z.; Genersch, E.; Kovacevic, S.R.; Ljubenkovic, J.; Radakovic, M.; Aleksic, N. Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie 2011, 42, 49-58.

Papini, R.; Mancianti, F.; Canovai, R.; Cosci, F.; Rocchigiani, G.; Benelli, G.; Canale, A. Prevalence of the microsporidian Nosema ceranae in honeybee (Apis mellifera) apiaries in Central Italy. Saudi J. Biol. Sci. 2017, 24, 979–982.

Botías, C.; Martín-Hernández, R.; Barrios, L.; Meana, A.; Higes, M. Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet. Res. 2013, 44, 25.

Vejsnaes, F.; Neilsen, S.L.; Kryger, P. Factors involved in the recent increase in colony losses in Denmark. J. Apic. Res. 2010, 49, 109-110.

Higes, M.; Martín-Hernandez, R.; Garrido-Bailon, E.; Gonzalez-Porto, A.V.; García-Palencia, P.; Meana, A.; Del Nozal, M.J.; Mayo, R.; Bernal, J.L. Honey bee colony collapse due to Nosema ceranae in professional apiaries. Environ. Microbiol. Rep. 2009, 1, 110-113.

Higes, M.; Nozal, M.J.; Alvaro, A.; Barrios, L.; Meana, A.; Martín-Hernández, R.; Bernal, J.L.; Bernal, J. The stability and effectiveness of fumagillin in controlling Nosema ceranae (Microsporidia) infection in honey bees (Apis mellifera) under laboratory and field conditions. Apidologie 2011, 42, 364–377.

Pajuelo, A.G.; Torres, C.; Bermejo F.J.O. Colony losses: a double blind trial on the influence of supplementary protein nutrition and preventative treatment with fumagillin against Nosema ceranae. J. Apic. Res. 2008, 47, 84–86.

Huang, W.F.; Solter, L.F.; Yau, P.M.; Imai, B.S. Nosema ceranae escapes fumagillin control in honey bees. PLoS Pathog. 2013, 9, e1003185.

van den Heever, J.P.; Thompson, T.S.;, Curtis, J.M.; Pernal, S.F. Stability of dicyclohexylamine and fumagillin in honey. Food Chem. 2015, 179, 152–158.

Toplak, I.; Jamnikar Ciglenečki, U.; Aronstein, K.; Gregorc, A. Chronic bee paralysis virus and Nosema ceranae experimental co-infection of winter honey bee workers (Apis mellifera L.). Viruses 2013, 5, 2282–2297

Costa, C.; Tanner, G.; Lodesani, M.; Maistrello, L.; Neumann, P. Negative correlation between Nosema ceranae spore loads and deformed wing virus infection levels in adult honey bee workers. J. Invertebr. Pathol. 2011, 108, 224–225

Bahreini, R.; Currie, R.W. The influence of Nosema (Microspora: Nosematidae) infection on honey bee (Hymenoptera: Apidae) defense against Varroa destructor (Mesostigmata: Varroidae). J. Invertebr. Pathol. 2015, 132, 57–65.

Rubanov, A.; Russell, K.A.; Rothman, J.A.; Nieh, J.C.; McFrederick, Q.S. Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure. Sci. Rep. 2019, 9, 3820.

Fewell, J.H.; Winston, M.L. Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behav. Ecol. Sociobiol. 1992, 30, 387–393.

Oldroyd, B.P. What’s killing American honey bees? PLoS Biol. 2007, 5, e168.

Groh, C.; Tautz, J.; Rössler, W. Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 4268–4273.

Jones, J.C.; Helliwell, P.; Beekman, M.; Maleszka, R.; Oldroyd, B.P. The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 2005, 191, 1121–1129.

Nürnberger, F.; Härtel, S.; Steffan-Dewenter, I. The influence of temperature and photoperiod on the timing of brood onset in hibernating honey bee colonies. PeerJ 2018, 6, e4801.

Wang, Q.; Xu, X.; Zhu, X.; Chen, L.; Zhou, S.; Huang, Z.Y.; Zhou, B. Low-Temperature Stress during Capped Brood Stage Increases Pupal Mortality, Misorientation and Adult Mortality in Honey Bees. PloS One 2016, 11, e0154547.

VanEngelsdorp, D.; Speybroeck, N.; Evans, J.D.; Kim Nguyen, B.; Mullin, C.; Frazier, M.; Frazier, J.; Cox-Foster, D.; Chen, Y,; Tarpy, D.R.; et al. Weighing risk factors associated with bee colony collapse disorder by classification and regression tree analysis. J. Econ. Entomol. 2010, 103, 1517-1523.

Memmott, J.; Craze, P.G.; Waser, N.M.; Price, M.V. Global warming and the disruption of plant-pollinator interactions. Ecol. Lett. 2007, 10, 710-717.

Thomson, J.D. Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365, 3187-3199.

Goulson, D.; Lye, G.C.; Darvill, B. Decline and conservation of bumble bees. Annu. Rev. Entomol. 2008, 53, 191–208.

Brown, M.J.F.; Paxton, R.J. The conservation of bees: A global perspective. Apidologie 2009, 40, 410–416.

Goulson, D.; Nicholls, E.; Botías, C.; Rotheray, E.L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015, 347, 1255957.

Kovács-Hostyánszki, A.; Földesi, R.; Mózes, E.; Szirák, Á.; Fischer, J.; Hanspach, J.; Báldi, A. Conservation of Pollinators in Traditional Agricultural Landscapes - New Challenges in Transylvania (Romania) Posed by EU Accession and Recommendations for Future Research. PloS ONE 2016, 11, e0151650.

Belsky, J.; Joshi, N.K. Impact of Biotic and Abiotic Stressors on Managed and Feral Bees. Insects 2019, 10, 233.

Patrício-Roberto, G.B.; Campos, M.J.O. Aspects of Landscape and Pollinators—What is Important to Bee Conservation? Diversity 2014, 6, 158-175.

Rollin, O.; Benelli, G.; Benvenuti, S.; Decourtye, A.; Wratten, S.D.; Canale, A.; Desneux, N. Weed-insect pollinator networks as bio-indicators of ecological sustainability in agriculture. A review. Agron. Sustain. Dev. 2016, 36, 8.

Sponsler, D.B.; Grozinger, C.M.; Hitaj, C.; Rundlöf, M.; Botías, C.; Code, A.; Lonsdorf, E.V.; Melathopoulos, A.P.; Smith, D.J.; Suryanarayanan, S.; et al. Pesticides and pollinators: A socioecological synthesis. Sci. Total. Environ. 2019, 662, 1012–1027.

Földesi, R.; Kovács‐Hostyánszki, A.; Kőrösi, Á.; Somay, L.; Elek, Z.; Markó, V.; Sárospataki, M.; Bakos, R.; Varga, Á.; Nyisztor, K.; et al. Relationships between wild bees, hoverflies and pollination success in apple orchards with different landscape contexts. Agr. Forest. Entomol. 2016, 18, 68-75.

Lee, H.; Sumner, D.A.; Champetier, A. Pollination Markets and the Coupled Futures of Almonds and Honey Bees: Simulating Impacts of Shifts in Demands and Costs. Am. J. Agric. Econ. 2019, 101, 230–249.

Potts, S.; Biesmeijer, J.; Kremen, C.; Neumann, P.; Schweiger, O.; Kunin, W. Global pollinator declines: trends impacts and drivers. Trends Ecol. Evol. 2010, 256, 345–353.

vanEngelsdorp, D.; Evans, J.D.; Donovall, L.; Mullin, C.; Frazier, M.; Frazier, J.; Tarpy, D.R.; Hayes, J.; Pettis, J.S. Entombed pollen: a new condition in honey bee colonies associated with increased risk of colony mortality. J. Invertebr. Pathol. 2009, 101, 147–149.

London-Shafir, I.; Shafir, S.; Eisikowitch, D. Amygdalin in almond nectar and pollen-facts and possible roles. Plant Syst. Evol. 2003, 238, 87–95.

United Nations Environment Programme (UNEP). UNEP Emerging Issues: Global Honey Bee Colony Disorder and Other Threats to Insect Pollinators 2010, p. 16 .http://www.unep.org/dewa/Portals/67/pdf/Global_Bee_Colony_Disorder_and_Threats_insect_pollinators.pdf.

Tilman, D.; Fargione, J.; Wolff, B.; D'Antonio, C.; Dobson, A.; Howarth, R.; Schindler, D.; Schlesinger, W.H.; Simberloff, D,; Swackhamer D. Forecasting Agriculturally Driven Global Environmental Change. Science 2001, 292, 281–284.

Drinkwater, L.E.; Wagoner, P.; Sarrantonio, M. Legume-based cropping systems have reduced carbon and nitrogen losses. Nature 1998, 396, 262–265.

Havlin, J.L.; Beaton, J.D.; Tisdale, S.L.; Nelson, W.L. Soil Fertility and Fertilizers: An Introduction to Nutrient Management. Saddle River 1999, NJ: Prentice–Hall.

Fox, J. E., Gulledge, J., Engelhaupt, E., Burow, M. E., & McLachlan, J. A. (2007). Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proceedings of the National Academy of Sciences of the United States of America, 104(24), 10282–10287.

Schierow, L-J.; Johnson, R.; Corn, M.L. Bee health: the role of pesticides, Congressional Research Service (CRS) 2012, Reports for Congress, pp. 26. https://www.fas.org/sgp/crs/misc/R42855.pdf

Capri, E.; Marchis, A. Bee Health in Europe: Facts and Figures 2013. Compendium of the latest information on bee health in Europe. OPERA Research Centre, Università Cattolica del Sacro Cuore , pp. 64.

Johnson, R.; Corn, M.L. Bee Health: The Role of Pesticides. Congressional Research Service (CRS) 2015. Reports for Congress, pp. 47. http://fas.org/sgp/crs/misc/R43900.pdf.

USDA-Biotech Crop Data. Adoption of genetically engineered crops in the U.S. 2009. http://www.ers.usda.gov/Data/BiotechCrops/#2009-7-1.

Johnson, R.M.; Ellis, M.D.; Mullin, C.A.; Frazier, M. Pesticides and honey bee toxicity—USA. Apidologie 2010, 41, 312–331.

Johnson, R.M. Honey Bee Toxicology. Annu. Rev. Entomol. 2015, 60, 415–434.




DOI: http://dx.doi.org/10.13102/sociobiology.v68i1.5851

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