Skip to main content

Pathogens, Pests, and Economics: Drivers of Honey Bee Colony Declines and Losses

Abstract

The Western honey bee (Apis mellifera) is responsible for ecosystem services (pollination) worth US$215 billion annually worldwide and the number of managed colonies has increased 45% since 1961. However, in Europe and the U.S., two distinct phenomena; long-term declines in colony numbers and increasing annual colony losses, have led to significant interest in their causes and environmental implications. The most important drivers of a long-term decline in colony numbers appear to be socioeconomic and political pressure on honey production. In contrast, annual colony losses seem to be driven mainly by the spread of introduced pathogens and pests, and management problems due to a long-term intensification of production and the transition from large numbers of small apiaries to fewer, larger operations. We conclude that, while other causal hypotheses have received substantial interest, the role of pests, pathogens, and management issues requires increased attention.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Aizen, M. A. and L. D. Harder (2009). “The global stock of domesticated honey bees is growing slower than agricultural demand for pollination.” Current Biology 19: 915-918.

    CAS  PubMed  Article  Google Scholar 

  • Al-Afaleq, A. I. and M. F. Hussein (2011). “The status of Rift Valley fever in animals in Saudi Arabia: a mini review.” Vector-Borne and Zoonotic Diseases 11(12): 1513-1520.

    PubMed  Article  Google Scholar 

  • Alaux, C., F. Ducloz, D. Crauser and Y. Le Conte (2010). “Diet effects on honeybee immunocompetence.” Biology Letters 6(4): 562-565.

    PubMed Central  PubMed  Article  Google Scholar 

  • Anderson, P. K., A. A. Cunningham, N. G. Patel, F. J. Morales, P. R. Epstein and P. Daszak (2004). “Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers.” Trends in Ecology & Evolution 19(10): 535-544.

    Article  Google Scholar 

  • Aston, D. (2010). “Honey bee winter loss survey for England, 2007-8.” Journal of Apicultural Research 49: 111–112.

    Article  Google Scholar 

  • Aufauvre, J., D. G. Biron, C. Vidau, R. Fontbonne, M. Roudel, M. Diogon, B. Vigues, L. P. Belzunces, F. Delbac and N. Blot (2012). “Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee.” Scientific Reports 2: 326.

    PubMed Central  PubMed  Article  Google Scholar 

  • Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, H. B. Hines, K. R. Lips, G. Marantelli and H. Parkes (1998). “Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.” Proceedings of the National Academy of Sciences of the United States of America 95(15): 9031-9036.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Blackburn, T. and K. Gaston (2004). “Special Feature: Macroecology.” Basic and Applied Ecology 385-387.

  • Blaustein, A. R. and D. B. Wake (1990). “Declining amphibian populations: a global phenomenon.” Trends in Ecology & Evolution 5: 203–204.

    Article  Google Scholar 

  • Brodschneider, R. and K. Crailsheim (2010). “Nutrition and health in honey bees.” Apidologie 41: 278–294.

    Article  Google Scholar 

  • Burnham, K. P. and D. R. Anderson (2002). “Model selection and multimodel inference: a practical information-theoretic approach.” Springer, New York.

    Google Scholar 

  • Champetier A, Sumner D, Wilen JE (2010) The Bioeconomics of Honeybees and Pollination.

  • Chauzat, M. P., A. C. Martel, S. Zeggane, P. Drajnudel, F. Schurr, M. C. Clement, M. Ribiere-Chabert, M. Aubert and J. P. Faucon (2010). “A case control study and a survey on mortalities of honey bee colonies (Apis mellifera) in France during the winter of 2005-6.” Journal of Apicultural Research 49(1): 40-51.

    Article  Google Scholar 

  • Chen, Y., J. D. Evans, B. I. Smith and J. S. Pettis (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: 186-188.

    PubMed  Article  Google Scholar 

  • Creswell, J. E. (2011). “A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees.” Ecotoxicology 20: 149–157.

    Article  Google Scholar 

  • Cunningham, A. A., P. Daszak and J. P. Rodríguez (2003). “Pathogen pollution: defining a parasitological threat to biodiversity conservation.” Journal of Parasitology 89: S78-S83.

    Google Scholar 

  • Currie, R. W., S. F. Pernal and E. Guzmán-Novoa (2010). “Honey bee colony losses in Canada.” Journal of Apicultural Research 49: 104–106.

    Article  Google Scholar 

  • Cutler, G. C. and C. D. Scott-Dupree (2007). “Exposure to clothianidin seed-treated canola has no long-term impact on honey bees.” Journal of Economic Entomology 100: 765–772.

    CAS  PubMed  Article  Google Scholar 

  • Daberkow, S., P. Korb and F. Hoff (2009). “Structure of the US beekeeping industry: 1982-2002.” Journal of Economic Entomology 102(3): 868-886.

    PubMed  Article  Google Scholar 

  • Daszak, P., A. A. Cunningham and A. D. Hyatt (2000). “Emerging infectious diseases of wildlife - threats to biodiversity and human health.” Science 287: 443-449.

    CAS  PubMed  Article  Google Scholar 

  • Daszak, P., A. A. Cunningham and A. D. Hyatt (2003). “Infectious disease and amphibian population declines.” Diversity and Distributions 9: 141–150.

    Article  Google Scholar 

  • Davidson, C., H. B. Shaffer and M. R. Jennings (2001). “Declines of the California red-legged frog: Climate, UV-B, habitat, and pesticides hypotheses.” Ecological Applications 11(2): 464-479.

    Article  Google Scholar 

  • Desneux, N., A. Decourtye and J. M. Delpuech (2007). “The sublethal effects of pesticides on beneficial arthropods.” Annual Review of Entomology 52: 81–106.

    CAS  PubMed  Article  Google Scholar 

  • Evans, J. D. and M. Spivak (2010). “Socialized medicine: Individual and communal disease barriers in honey bees.” Journal of Invertebrate Pathology 103: S62-S72.

    PubMed  Article  Google Scholar 

  • Fevre, E. M., B. M. D. C. Bronsvoort, K. A. Hamilton and S. Cleaveland (2006). “Animal movements and the spread of infectious diseases.” Trends in Microbiology 14(3): 125-131.

    CAS  PubMed  Article  Google Scholar 

  • Fisher, M. C., D. A. Henk, C. J. Briggs, J. S. Brownstein, L. C. Madoff, S. L. McCraw and S. J. Gurr (2012). “Emerging fungal threats to animal, plant and ecosystem health.” Nature 484(7393): 186-194.

    CAS  PubMed  Article  Google Scholar 

  • Gajger, I. T., Z. Tomljanovic and Z. Petrinec (2010). “Monitoring health status of Croatian honey bee colonies and possible reasons for winter losses.” Journal of Apicultural Research 49: 107–108.

    Article  Google Scholar 

  • Gallai, N., J. M. Salles, J. Settele and B. E. Vaissiere (2009). “Economic valuation of the vulnerability of world agriculture confronted with pollinator decline.” Ecological Economics 68(3): 810-821.

    Article  Google Scholar 

  • Garibaldi, L. A., I. Steffan-Dewenter, R. Winfree, M. A., Aizen, R. Bommarco, S. A. Cunningham, C. KKremen, L. G. Carvalheiro, L.D. Harder, O. Afik, I. Bartomeus, F. Benjamin, V. Boreux, D. Cariveau, N. P. Chacoff, J. H. Dudenhöffer, B. M. Freitas, J. Ghazoul, S. Greenleaf, J. Hipólito, A. Holzschuh, B. Howlett, R. Isaacs, S. K. Javorek, C. M. Kennedy, K. M. Krewenka, S. Srishnan, Y. Mandelik, M. M. Mayfield, I. Motzke, T. Munyuli, B. A. Nault, M. Otieno, J. Petersen, G. Pisanty, S. G. Potts, R. Rader, T. H. Ricketts, M. Rundlöf, C. L. Seymour, C. Schüepp, H. Szentgyörgyi, H. Taki, T. Tscharntke, C. H. Vergara, B. F. Viana, T. C. Wanger, C. Westphal, N. Williams, and A. M. Klein (2013). “Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance”. Science 339(6127): 1608-1611.

    CAS  PubMed  Article  Google Scholar 

  • Gaston, K. J. and T. M. Blackburn (2000). Pattern and process in macroecology, Wiley- Blackwell.

    Book  Google Scholar 

  • Genersch, E. and M. Aubert (2010). “Emerging and re-emerging viruses of the honey bee (Apis mellifera L.).” Veterinary Research 41(6): 54

    PubMed Central  PubMed  Article  Google Scholar 

  • Genersch, E., W. von der Ohe, H. Kaatz, A. Schroeder, C. Otten, R. Buchler, S. Berg, W. Ritter, W. Muhlen, S. Gisder, M. Meixner, G. Liebig and P. Rosenkranz (2010b). “The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies.” Apidologie 41(3): 332-352.

    CAS  Article  Google Scholar 

  • Gill, R. J., O. Ramos-Rodriguez and N. E. Raine (2012). “Combined pesticide exposure severely impacts individual- and colony-level traits in bees.” Nature 491: 105-109.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Girolami, V., L. Mazzon, A. Squartini, N. Mori, M. Marzaro, A. Di Bernardo, M. Greatti, C. Giorio and A. Tapparo (2009). “Translocation of Neonicotinoid Insecticides From Coated Seeds to Seedling Guttation Drops: A Novel Way of Intoxication for Bees.” Journal of Economic Entomology 102(5): 1808-1815.

    CAS  PubMed  Article  Google Scholar 

  • Gisder, S., P. Aumeier and E. Genersch (2009). “Deformed wing virus: replication and viral load in mites (Varroa destructor).” Journal of General Virology 90(2): 463-467.

    CAS  PubMed  Article  Google Scholar 

  • Gisder, S., K. Hedtke, N. Möckel, M.-C. Frielitz, A. Linde and E. Genersch (2010). “Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae?” Applied and Environmental Microbiology 76(9): 3032-3038.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Guzman-Novoa, E., L. Eccles, Y. Calvete, J. McGowan, P. G. Kelly and A. Correa-Benitez (2010). “Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada.” Apidologie 41(4): 443-450.

    Article  Google Scholar 

  • Hawthorne, D. J. and G. P. Dively (2011). “Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey bees.” PLoS ONE 6(11): e26796.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Henry, M., M. Beguin, F. Requier, O. Rollin, J. F. Odoux, P. Aupinel, J. Aptel, S. Tchamitchian and A. Decourtye (2012). “A Common Pesticide Decreases Foraging Success and Survival in Honey Bees.” Science 336(6079): 348-350.

    CAS  PubMed  Article  Google Scholar 

  • Higes, M., P. García-Palencia, R. Martín-Hernández and A. Meana (2007). “Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia).” Journal of Invertebrate Pathology 94: 211-217.

    PubMed  Article  Google Scholar 

  • Higes, M., R. Martin-Hernandez, C. Botias, E. Garrido Bailon, A. V. Gonzalez-Porto, L. Barrios, M. Jesus del Nozal, J. L. Bernal, J. J. Jimenez, P. Garcia Palencia and A. Meana (2008). “How natural infection by Nosema ceranae causes honeybee colony collapse.” Environmental Microbiology 10(10): 2659-2669.

    PubMed  Article  Google Scholar 

  • Highfield, A. C., A. El Nagar, L. C. M. Mackinder, L. M. L. J. Noel, S. J. Martin and D. C. Schroeder (2009). “Deformed Wing Virus Implicated in Overwintering Honeybee Colony Losses.” Applied and Environmental Microbiology 75(22): 7212-7220.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Hosseini, P., S. H. Sokolow, K. J. Vandegrift, A. M. Kilpatrick and P. Daszak (2010). “Predictive power of air travel and socio-economic data for early pandemic spread.” PLoS ONE 5(9): e12763.

    PubMed Central  PubMed  Article  Google Scholar 

  • Johnson, J. B. and K. S. Omland (2004). “Model selection in ecology and evolution.” Trends in Ecology & Evolution 19(2): 101-108.

    Article  Google Scholar 

  • Johnson, R. M. (2009). “Managed pollinator CAP Coordinated Agricultural Project: A national research and extension initiative to reverse pollinator decline when varroacides interact.” American Bee Journal 149: 1157–1159.

    Google Scholar 

  • Johnson, R. M., M. D. Ellis, C. A. Mullin and M. Frazier (2010). “Pesticides and honey bee toxicity - USA.” Apidologie 41(3): 312-331.

    CAS  Article  Google Scholar 

  • Johnson, R. M., L. Dahlgren, B. D. Siegfried, and M. D. Ellis (2012). “Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS ONE 8(1): e54092.

    Article  Google Scholar 

  • Karesh, W. B., R. A. Cook, E. L. Bennett and J. Newcomb (2005). “Wildlife trade and global disease emergence.” Emerging Infectious Diseases 11(7): 1000-1002.

    PubMed Central  PubMed  Article  Google Scholar 

  • Keppler, J., R. Becker, R. Spatz and F. Dechet (2010). Systemische insektizide Beizmittel – Auftreten und Relevanz von Guttation für die Entwicklung von Honigbienenkolonien. Deutsche Pflanzenschutztagung. J. K.-I. BfKeVG. Quedlinburg, Germany.

    Google Scholar 

  • Kiesecker, J. M. and A. R. Blaustein (1995). “Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature.” Proceedings of the National Academy of Sciences of the United States of America 92: 11049–11052.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kilpatrick, A. M., A. A. Chmura, D. W. Gibbons, R. C. Fleischer, P. P. Marra and P. Daszak (2006a). “Predicting the global spread of H5N1 avian influenza.” Proceedings of the National Academy of Sciences of the United States of America 103: 19368-19373.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kilpatrick, A. M., L. D. Kramer, M. J. Jones, P. P. Marra and P. Daszak (2006b). “West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior.” PloS Biology 4(4): e82.

    PubMed Central  PubMed  Article  Google Scholar 

  • Klee, J., A. M. Besana, E. Genersch, S. Gisder, A. Nanetti, D. Q. Tam, T. X. Chinh, F. Puerta, J. M. Ruz, P. Kryger, D. Message, F. Hatjina, S. Korpela, I. Fries and R. J. Paxton (2007). “Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera.” Journal of Invertebrate Pathology 96(1): 1-10.

    PubMed  Article  Google Scholar 

  • Krupke, C. H., G. J. Hunt, B. D. Eitzer, G. Andino and K. Given (2012). “Multiple routes of pesticide exposure for honey bees living near agricultural fields.” PLoS ONE 7(1): e29268.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Laycock, I., K. M. Lenthall, A. T. Barratt and J. E. Creswell (2012). “Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris).” Ecotoxicology 21(7): 1937-1945.

    CAS  PubMed  Article  Google Scholar 

  • Le Conte, Y., M. Ellis and W. Ritter (2010). “Varroa mites and honey bee health: can Varroa explain part of the colony losses?” Apidologie 41(3): 353-363.

    Article  Google Scholar 

  • Le Conte, Y. and M. Navajas (2008). “Climate change: impact on honey bee populations and diseases.” Revue scientifique et technique (International Office of Epizootics) 27: 485-497, 499-510.

    Google Scholar 

  • Levine, J. M. and C. M. D’Antonio (2003). “Forecasting biological invasions with increasing international trade.” Conservation Biology 17(1): 322-326.

    Article  Google Scholar 

  • Mao, W., M. A. Shuler and M. R. Berenbaum (2013). “Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera.” Proceedings of the National Academy of Sciences of the United States of America 110(22): 8763-8764.

    Article  Google Scholar 

  • Martin, S. J., A. C. Highfield, L. Brettell, E. M. Villalobos, G. E. Budge, M. Powell, S. Nikaido and D. C. Schroeder (2012). “Global honey bee viral landscape altered by a parasitic mite.” Science 336(6086): 1304-1306.

    CAS  PubMed  Article  Google Scholar 

  • Mendelson, J. R., K. R. Lips, R. W. Gagliardo, G. B. Rabb, J. P. Collins, J. E. Diffendorfer, P. Daszak, R. Ibanez, K. C. Zippel, D. P. Lawson, K. M. Wright, S. N. Stuart, C. Gascon, H. R. da Silva, P. A. Burrowes, R. L. Joglar, E. La Marca, S. Lotters, L. H. du Preez, C. Weldon, A. Hyatt, J. V. Rodriguez-Mahecha, S. Hunt, H. Robertson, B. Lock, C. J. Raxworthy, D. R. Frost, R. C. Lacy, R. A. Alford, J. A. Campbell, G. Parra-Olea, F. Bolanos, J. J. C. Domingo, T. Halliday, J. B. Murphy, M. H. Wake, L. A. Coloma, S. L. Kuzmin, M. S. Price, K. M. Howell, M. Lau, R. Pethiyagoda, M. Boone, M. J. Lannoo, A. R. Blaustein, A. Dobson, R. A. Griffiths, M. L. Crump, D. B. Wake and E. D. Brodie (2006). “Biodiversity - Confronting amphibian declines and extinctions.” Science 313(5783): 48.

    CAS  PubMed  Article  Google Scholar 

  • Mullin C. A., M. Frazier, J. L. Frazier, S. Ashcraft, R. Simonds, D. vanEngelsdorp, J. S. Pettis. (2010). “High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS ONE 5(3): e9754.

    PubMed Central  PubMed  Article  Google Scholar 

  • Mutinelli, F. (2011). “The spread of pathogens through trade in honey bees and their products (including queen bees and semen): overview and recent developments.” Revue Scientifique et Technique - Office International des Epizooties 30: 257–271.

    CAS  Google Scholar 

  • Mutinelli, F., C. Costa, M. Lodesani, A. Baggio, P. Medrzycki, G. Formato and C. Parrini (2010). “Honey bee colony losses in Italy.” Journal of Apicultural Research 49: 119–120.

    Article  Google Scholar 

  • Neumann, P. and N. L. Carreck (2010). “Honey bee colony losses.” Journal of Apicultural Research 49: 1–6.

    Article  Google Scholar 

  • Nguyen, B. K., C. Saegerman, C. Pirard, J. Mignon, J. Widart, B. Tuirionet, F. J. Verheggen, D. Berkvens, E. De Pauw and E. Haubruge (2009). “Does imidacloprid seed-treated maize have an impact on honey bee mortality?” Journal of Economic Entomology 102(2): 616-623.

    CAS  PubMed  Article  Google Scholar 

  • Ollerton, J., V. Price, W. S. Armbruster, J. Memmott, S. Watts, N. M. Waser, O. Totland, D. Goulson, R. Alarcon, J. C. Stout and S. Tarrant (2012). “Overplaying the role of honey bees as pollinators: a comment on Aebi and Neumann (2011).” Trends in Ecology & Evolution 27(3): 141-142.

    Article  Google Scholar 

  • OPERA (2011). Bee health in Europe - Facts & figures. U. C. d. S. Cuore. Italy.

    Google Scholar 

  • Palmer MJ, Moffat C, Saranzewa N, Harvey J, Wright GA, Connolly CN (2013) Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nature Communications 4(1634). doi:10.1038/ncomms2648

  • Pettis, J. S., D. vanEngelsdorp, J. Johnson and G. Dively (2012). “Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema.” Naturwissenschaften 99(2): 153-158.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Plowright, R. K., S. H. Sokolow, M. E. Gorman, P. Daszak and J. E. Foley (2008). “Causal inference in disease ecology: investigating ecological drivers of disease emergence.” Frontiers in Ecology and the Environment 6(8): 420-429.

    Article  Google Scholar 

  • Potts, S. G., J. C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger and W. E. Kunin (2010a). “Global pollinator declines: trends, impacts and drivers.” Trends in Ecology & Evolution 25(6): 345-353.

    Article  Google Scholar 

  • Potts, S. G., S. P. M. Roberts and R. Dean (2010b). “Declines of managed honey bees and beekeepers in Europe.” Journal of Apicultural Research 49: 15–22.

    Article  Google Scholar 

  • Pounds, J. A. (2001). “Climate and amphibian declines.” Nature 410(6829): 639-640.

    CAS  PubMed  Article  Google Scholar 

  • Ribiere M, Ball B, Aubert M (2008) Natural history and geographic distribution of honey bee viruses. In: Virology and the Honey Bee, Aubert M, Ball B, Fries I et al. (editors), Luxembourg: European Communities, pp 15–84.

  • Rosenkranz, P., P. Aumeier and B. Ziegelmann (2010). “Biology and control of Varroa destructor.” Journal of Invertebrate Pathology 103: S96-S119.

    PubMed  Article  Google Scholar 

  • Schloegel, L. M., P. Daszak, A. A. Cunningham, R. Speare and B. Hill (2010). “Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment.” Diseases of Aquatic Organisms 92(2-3): 101-108.

    PubMed  Article  Google Scholar 

  • Smolinski, M. S., M. A. Hamburg, J. Lederberg and Committee on Emerging Microbial Threats to Health in the 21st Century (2003). Microbial threats to health: Emergence, detection, and response. Washington D.C., The National Academies Press

    Google Scholar 

  • Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman and R. W. Waller (2004). “Status and trends of amphibian declines and extinctions worldwide.” Science 306(5702): 1783-1786.

    CAS  PubMed  Article  Google Scholar 

  • Sumner, D. A. and H. Boriss (2006). Bee-conomics and the leap in pollination fees. Agricultural and Resource Economics Update, University of California Gianni Foundation of Agricultural Economics. 9: 9-11.

    Google Scholar 

  • Tapparo, A., D. Marton and C. Gioro (2012). “Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seeds.” Environmental Science & Technology 46: 2592–2599.

    CAS  Article  Google Scholar 

  • Thompson, H. (2010). “Risk assessment for honey bees and pesticides - recent developments and ‘new issues’.” Pest Management Science 66: 1157–1162.

    CAS  PubMed  Article  Google Scholar 

  • Thompson, H. M. (2003). “Behavioural effects of pesticides in bees - Their potential for use in risk assessment.” Ecotoxicology 12(1-4): 317-330.

    CAS  PubMed  Article  Google Scholar 

  • van der Zee, R., L. Pisa, S. Andonov, R. Brodschneider, J. D. Charriere, R. Chlebo, M. F. Coffey, K. Crailsheim, B. Dahle, A. Gajda, A. Gray, M. M. Drazic, M. Higes, L. Kauko, A. Kence, M. Kence, N. Kezic, H. Kiprijanovska, J. Kralj, P. Kristiansen, R. M. Hernandez, F. Mutinelli, B. K. Nguyen, C. Otten, A. Ozkirim, S. F. Pernal, M. Peterson, G. Ramsay, V. Santrac, V. Soroker, G. Topolska, A. Uzunov, F. Vejsnaes, S. Wei and S. Wilkins (2012). “Managed honey bee colony losses in Canada, China, Europe, Israel and Turkey, for the winters of 2008-9 and 2009-10.” Journal of Apicultural Research 51(1): 91-114.

    Article  Google Scholar 

  • vanEngelsdorp, D., D. Caron, J. Hayes, R. Underwood, M. Henson, K. Rennich, A. Spleen, M. Andree, R. Snyder, K. Lee, K. Roccasecca, M. Wilson, J. Wilkes, E. Lengerich, J. Pettis and Bee Informed Partnership (2012). “A national survey of managed honey bee 2010-11 winter colony losses in the USA: results from the Bee Informed Partnership.” Journal of Apicultural Research 51(1): 115-124

    Article  Google Scholar 

  • vanEngelsdorp, D., J. D. Evans, L. Donovall, C. Mullin, M. Frazier, J. Frazier, D. R. Tarpy, J. Hayes and J. S. Pettis (2009a). “Entombed pollen”: A new condition in honey bee colonies associated with increased risk of colony mortality.” Journal of Invertebrate Pathology 101(2): 147-149.

    PubMed  Article  Google Scholar 

  • vanEngelsdorp, D., J. D. Evans, C. Saegerman, C. Mullin, E. Haubruge, B. K. Nguyen, M. Frazier, J. Frazier, D. Cox-Foster, Y. P. Chen, R. Underwood, D. R. Tarpy and J. S. Pettis (2009b). “Colony Collapse Disorder: A descriptive study.” PLoS ONE 4(8): e6481.

    PubMed Central  PubMed  Article  Google Scholar 

  • vanEngelsdorp, D., J. Hayes, R. M. Underwood, D. Caron and J. Pettis (2011). “A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010.” Journal of Apicultural Research 50(1): 1-10.

    Article  Google Scholar 

  • vanEngelsdorp, D., J. Hayes, R. M. Underwood and J. Pettis (2008). “A survey of honey bee colony losses in the US, fall 2007 to spring 2008.” PLoS ONE 3(12): e4071.

    PubMed Central  Article  Google Scholar 

  • vanEngelsdorp, D., J. J. Hayes, R. Underwood and J. S. Pettis (2010). “A survey of honey bee colony losses in the United States, fall 2008 to spring 2009.” Journal of Apicultural Research 49(1): 7-14.

    Article  Google Scholar 

  • vanEngelsdorp, D. and M. D. Meixner (2010). “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.

    PubMed  Article  Google Scholar 

  • vanEngelsdorp, D., R. Underwood, D. Caron and J. Hayes (2007). “An estimate of managed colony losses in the winter of 2006-2007: A report commissioned by the Apiary Inspectors of America.” American Bee Journal 147(7): 599-603.

    Google Scholar 

  • Vejsnaes, F., S. L. Nielsen and P. Kryger (2010). “Factors involved in the recent increase in colony losses in Denmark.” Journal of Apicultural Research 49: 109–110.

    Article  Google Scholar 

  • Vidau, C., M. Diogon, J. Aufauvre, R. Fontbonne, B. Vigues, J. L. Brunet, C. Texier, D. G. Biron, N. Blot, H. El Alaoui, L. P. Belzunces and F. Delbac (2011). “Exposure to Sublethal Doses of Fripronil and Thiacloprid Highy lncreases Mortality of Honeybees Previously Infected by Nosema ceranae.” PLoS ONE 6(6).

  • Whitehorn, P. R., S. O’Connor, F. L. Wackers and D. Goulson (2012). “Neonicotinoid pesticide reduces bumblebee colony growth and queen production.” Science 336(6079): 351-352.

    CAS  PubMed  Article  Google Scholar 

  • Williams, G. R., D. R. Tarpy, D. VanEngelsdorp, M. P. Chauzat, D. L. Cox-Foster, K. S. Delaplane, P. Neumann, J. S. Pettis, R. E. L. Rogers and D. Shutler (2010). “Colony Collapse Disorder in context.” Bioessays 32(10): 845-846.

    PubMed Central  PubMed  Article  Google Scholar 

  • Williamson, S. M. and G. A. Wright (2013). “Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees.” Journal of Experimental Biology 216(10): 1799-1807.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Winfree, R., N. M. Williams, J. Dushoff and C. Kremen (2007). “Native bees provide insurance against ongoing honey bee losses.” Ecology Letters 10(11): 1105-1113.

    PubMed  Article  Google Scholar 

  • Yang, E. C., Y. C. Chuang, L. Chen and L. H. Chang (2008). “Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae).” Journal of Economic Entomology 101: 1743–1748.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

We acknowledge the beekeepers who took our survey as well as Jordan Levinson and Chia-Yi Hou of EcoHealth Alliance for assistance. Research was supported by a National Science Foundation Human and Social Dynamics “Agents of Change” award (SES-HSD-AOC “Human-related factors affecting emerging infectious diseases,” BCS—0826779), and by funding from the MARS Foundation, the Margaret A. Cargill Foundation, and Bayer Crop Science. Funders had no role in the data collection, analysis, nor in the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter Daszak.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Smith, K.M., Loh, E.H., Rostal, M.K. et al. Pathogens, Pests, and Economics: Drivers of Honey Bee Colony Declines and Losses. EcoHealth 10, 434–445 (2013). https://doi.org/10.1007/s10393-013-0870-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-013-0870-2

Keywords

  • honey bee
  • colony loss
  • Varroa
  • management
  • pollinator