Open Access
Review
Issue
Apidologie
Volume 41, Number 3, May-June 2010
Honey bee health
Page(s) 353 - 363
DOI https://doi.org/10.1051/apido/2010017
Published online 12 April 2010
  • Alaux C., Brunet J.-L., Dussaubat C., Mondet F., Tchamitchan S., Cousin M., Brillard J., Baldy A., Belzunces L.P., Le Conte Y. (2009) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera), Environ. Microbiol., DOI: 10.1111/j.1462-2920.2009.02123.x. [Google Scholar]
  • Allen M., Ball B. (1996) The incidence and world distribution of honey bee viruses, Bee World 77, 141–162 [Google Scholar]
  • Anderson D.L. (2000) Variation in the parasitic bee mite Varroa jacobsoni Oud., Apidologie 31, 281–292 [CrossRef] [EDP Sciences] [Google Scholar]
  • Ball B.V. (1985) Acute paralysis virus isolated from honeybee colonies infested with Varroa jacobsoni., J. Apic. Res. 24, 115–119 [Google Scholar]
  • Ball B.V., Allen M.F. (1988) The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni, Ann. Appl. Biol. 113, 237–244 [CrossRef] [Google Scholar]
  • Berthoud H., Imdorf A., Haueter M., Radloff S., Neumann P. (2010) Virus infections and winter losses of honey bee colonies (Apis mellifera), J. Apic. Res. 49, 60–65 [CrossRef] [Google Scholar]
  • Boecking O., Genersch E. (2008) Varroosis – the ongoing crisis in bee keeping, J. Verbrauch. Lebensm. 3, 221–228 [CrossRef] [Google Scholar]
  • Bogdanov S. (2006) Contaminants of bee products, Apidologie 37, 1–18 [CrossRef] [EDP Sciences] [Google Scholar]
  • Bowen-Walker P.L., Gunn A. (2001) The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels, Entomol. Exp. Appl. 101, 207–217 [CrossRef] [Google Scholar]
  • Bowen-Walker P.L., Martin S.J., Gunn A. (1999) The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud., J. Invertebr. Pathol. 73, 101–106 [CrossRef] [PubMed] [Google Scholar]
  • Büchler R., Berg S., Le Conte Y. (2010) Breeding for mite resistance in Europe, Apidologie 41, 393–408. [CrossRef] [EDP Sciences] [Google Scholar]
  • Calis J.N.M., Fries I., Ryrie S.C. (1999) Population modelling of Varroa jacobsoni Oud., Apidologie 30, 111–124 [CrossRef] [EDP Sciences] [Google Scholar]
  • Carreck N.L., Ball B.V., Martin S.J. (2010a) The epidemiology of cloudy wing virus infection in the honey bee colonies in the UK, J. Apic. Res. 49, 66–71 [CrossRef] [Google Scholar]
  • Carreck N.L., Ball B.V., Martin S.J. (2010b) Honey bee colony collapse and changes in viral prevalence associated with Varroa destructor, J. Apic. Res. 49, 93–94 [CrossRef] [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, J. Econ. Entomol. 99, 253–262 [CrossRef] [PubMed] [Google Scholar]
  • Chen Y.P., Evans J., Feldlaufer M. (2006) Horizontal and vertical transmission of viruses in the honeybee, Apis mellifera, J. Invertebr. Pathol. 92, 152–159 [CrossRef] [PubMed] [Google Scholar]
  • Chen Y.P., Pettis J.S., Evans J.D., Kramer M., Feldlaufer M.F. (2004) Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor, Apidologie 35, 441–448 [CrossRef] [EDP Sciences] [Google Scholar]
  • Chen Y.P., Pettis J.S., Feldlaufer M.F. (2005) Detection of multiple viruses in queens of the honey bee Apis mellifera L., J. Invertebr. Pathol. 90, 118–121 [CrossRef] [PubMed] [Google Scholar]
  • Colin M.E., Belzunces L.P. (1992) Evidence of synergy between prochloraz and deltamethrin in Apis mellifera L.: A convenient biological approach, Pestic. Sci. 36, 115–119 [CrossRef] [Google Scholar]
  • Cornuet J.M., Beaumont M.A., Estoup A., Solignac M. (2006) Inference on microsatellite mutation processes in the invasive mite, Varroa destructor, using reversible jump Markov chain Monte Carlo, Theor. Popul. Biol. 69, 129–144 [CrossRef] [PubMed] [Google Scholar]
  • Correa-Marques M.H., Medina L.M., Martin S.J., de Jong D. (2003) Comparing data on the reproduction of Varroa destructor, Genet. Mol. Res. 2, 1–6 [PubMed] [Google Scholar]
  • Cox-Foster D.L., Conlan S., Holmes E.C., Palacios G., Evans J.D., Moran N.A., Quan P.L., Briese T., Hornig M., Geiser D.M., Martinson V., vanEngelsdorp D., Kalkstein A.L., Drysdale A., Hui J., Zhai J.H., Cui L.W., Hutchison S.K., Simons J.F., Egholm M., Pettis J.S., Lipkin W.I. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder, Science 318, 283–287 [CrossRef] [PubMed] [Google Scholar]
  • Currie R.W., Gatien P. (2006) Timing acaricide treatments to prevent Varroa destructor (Acari: Varroidae) from causing economic damage to honey bee colonies, Can. Entomol. 138, 238–252 [CrossRef] [Google Scholar]
  • Dahle B. (2010) The role of Varroa destructor for honey bee colony losses in Norway, J. Apic. Res. 49, 124–125 [CrossRef] [Google Scholar]
  • Delaplane K.S., Hood W.M. (1997) Effects of delayed acaricide treatment in honey bee colonies parasitized by Varroa jacobsoni and a late-season treatment threshold for the southeastern USA, J. Apic. Res. 36, 125–132 [Google Scholar]
  • Downey D.L., Winston M.L. (2001) Honey bee colony mortality and productivity with single and dual infestations of parasitic mite species, Apidologie 32, 567–575 [CrossRef] [EDP Sciences] [Google Scholar]
  • Downey D.L., Higo T.T., Winston M.L. (2000) Single and dual parasitic mite infestations on the honey bee, Apis mellifera, Insect. Soc. 47, 171–176 [CrossRef] [Google Scholar]
  • Drescher W., Schneider P. (1987) The effect of the Varroa mite upon the fat body of worker bees and their tolerance of pesticides, In Africanized Honey Bees and Bee Mites, in: Needham G.R. et al. (Eds.), Ellis Horwood ltd, Chichester, England, UK, pp. 452–456. [Google Scholar]
  • Elzen P.J., Baxter J.R., Spivak M., Wilson W.T. (2000) Control of Varroa jacobsoni Oud. resistant to fluvalinate and amitraz using coumaphos, Apidologie 31, 437–441 [CrossRef] [EDP Sciences] [Google Scholar]
  • Floris I., Satta A., Cabras P., Garau V.L., Angioni A. (2004) Comparison between two thymol formulations in the control of Varroa destructor: Effectiveness, persistence, and residues, J. Econ. Entomol. 97, 187–191 [CrossRef] [PubMed] [Google Scholar]
  • Fries I., Camazine S., Sneyd J. (1994) Population Dynamics of Varroa jacobsoni – A Model and a Review, Bee World 75, 5–28 [Google Scholar]
  • Fries I., Imdorf A., Rosenkranz P. (2006) Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate, Apidologie 37, 564–570 [CrossRef] [EDP Sciences] [Google Scholar]
  • Garedew A., Schmolz E., Lamprecht I. (2004) The energy and nutritional demand of the parasitic life of the mite Varroa destructor, Apidologie 35, 419–430 [CrossRef] [EDP Sciences] [Google Scholar]
  • Gauthier L., Tentcheva D., Tournaire M., Dainat B., Cousserans F., Colin M.E., Bergoin M. (2007) Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique, Apidologie 38, 426–435 [CrossRef] [EDP Sciences] [Google Scholar]
  • Genersch E. (2005) Development of a rapid and sensitive RT-PCR method for the detection of deformed wing virus, a pathogen of the honeybee (Apis mellifera), Vet. J. 169, 121–123 [CrossRef] [PubMed] [Google Scholar]
  • Gilliam M. (1997) Identification and roles of non-pathogenic microflora associated with honey bees, Fems Microbiol. Lett. 155, 1–10 [CrossRef] [Google Scholar]
  • Guzman-Novoa E., Eccles L., Calvete Y., McGowan J., Kelly P.G., Correa A. (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada, Apidologie, DOI: 10.1051/apido/2009076. [Google Scholar]
  • Harris J.W., Harbo J.R. (1999) Low sperm counts and reduced fecundity of mites in colonies of honey bees (Hymenoptera : Apidae) resistant to Varroa jacobsoni (Mesostigmata : Varroidae), J. Econ. Entomol. 92, 83–90 [Google Scholar]
  • Hendrikx P., Chauzat M.P., Debin M., Neuman P., Fries I., Ritter W., Brown M., Mutinelli F., Le Conte Y., Gregorc A. (2009) Bee Mortality and Bee Surveillance in Europe, EFSA-Report, http://www.efsa.europa.eu. [Google Scholar]
  • Higes M. (2005) El sîndrome de despoblamiento de las colmenas en Espana, Vida Apicola 15–21. [Google Scholar]
  • Highfield A.C., El Nagar A., Mackinder L.C.M., Noel L., Hall M.J., Martin S.J., Schroeder D.C. (2009) Deformed Wing Virus Implicated in Overwintering Honeybee Colony Losses, Appl. Environ. Microbiol. 75, 7212–7220 [CrossRef] [PubMed] [Google Scholar]
  • Hillesheim E., Ritter W., Bassand D. (1996) First data on resistance mechanisms of Varroa jacobsoni (OUD.) against tau-fluvalinate, Exp. Appl. Acarol. 20, 283–296 [NASA ADS] [CrossRef] [EDP Sciences] [MathSciNet] [PubMed] [Google Scholar]
  • Johnson R.M., Ellis M.D., Mullin C.A., Frazier M. (2010) Pesticides and Bee Toxicity – USA, Apidologie 41, 312–331. [CrossRef] [EDP Sciences] [Google Scholar]
  • Johnson R.M., Evans J.D., Robinson G.E., Berenbaum M.R. (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera), Proc. Natl. Acad. Sci. USA 106, 14790–14795 [CrossRef] [Google Scholar]
  • Johnson R.M., Pollock H.S., Berenbaum M.R. (2009) Synergistic Interactions Between In-Hive Miticides in Apis mellifera, J. Econ. Entomol. 102, 474–479 [CrossRef] [PubMed] [Google Scholar]
  • Kaplan K. (2008) Colony collapse disorder: a complex buzz, Agriculture Research Magazine, <ars.usda.gov/is/br/ccd>. [Google Scholar]
  • Kefuss J., Vanpoucke J., De Lahitte J.D., Ritter W. (2004) Varroa tolerance in France of intermissa bees from Tunisia and their naturally mated descendants: 1993–2004, Am. Bee J. 144, 563–568 [Google Scholar]
  • Koch W., Ritter W. (1991) Experimental Examinations Concerning the Problem of Deformed Emerging Bees After Infestation with Varroa jacobsoni, Zentralbl. Veterinarmed. B 38, 337–344 [PubMed] [Google Scholar]
  • Kovac H., Crailsheim K. (1988) Lifespan of Apis mellifera carnica Pollm. infested by Varroa jocobsoni Oud. in relation to season and extent of infestation, J. Apic. Res. 27, 230–238 [Google Scholar]
  • Kralj J., Fuchs S. (2006) Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers, Apidologie 37, 577–587 [CrossRef] [EDP Sciences] [Google Scholar]
  • Le Conte Y., Arnold G. (1987) The effects of the age and temperature of honeybees on the behaviour of Varroa jacobsoni, Apidologie 18, 305–320 [CrossRef] [EDP Sciences] [Google Scholar]
  • Le Conte Y., Navajas M. (2008) Climate change : impact on bee populations and their illnesses, Rev. Sci. Tech. Off. Int. Epizoot. 27, 485–497 [Google Scholar]
  • Le Conte Y., De Vaublanc G., Crauser D., Jeanne F., Rousselle J.C., Becard J.M. (2007) Honey bee colonies that have survived Varroa destructor, Apidologie 38, 566–572 [CrossRef] [EDP Sciences] [Google Scholar]
  • Martel A.C., Zeggane S., Aurieres C., Drajnudel P., Faucon J.P., Aubert M. (2007) Acaricide residues in honey and wax after treatment of honey bee colonies with Apivar® or Asuntol® 50, Apidologie 38, 534–544 [CrossRef] [EDP Sciences] [Google Scholar]
  • Martin S. (1998) A population model for the ectoparasitic mite Varroa jacobsoni in honey bee (Apis mellifera) colonies, Ecol. Model. 109, 267–281 [CrossRef] [Google Scholar]
  • Martin S., Holland K., Murray M. (1997) Non-reproduction in the honeybee mite Varroa jacobsoni, Exp. Appl. Acarol. 21, 539–549 [NASA ADS] [CrossRef] [EDP Sciences] [MathSciNet] [PubMed] [Google Scholar]
  • Martin S.J. (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach, J. Appl. Ecol. 38, 1082–1093 [CrossRef] [Google Scholar]
  • Martin S.J., Ball B.V., Carreck N.L. (2010) Prevalence and persistance of deformed wing virus (DWV) in untreated or acaricide-treated Varroa destructor infested honey bees (Apis mellifera) colonies, J. Apic. Res. 49, 72–79 [CrossRef] [Google Scholar]
  • Milani N. (1995) The resistance of Varroa jacobsoni Oud. to pyrethroids: A laboratory assay, Apidologie 26, 415–429 [CrossRef] [EDP Sciences] [Google Scholar]
  • Milani N. (1999) The resistance of Varroa jacobsoni Oud. to acaricides, Apidologie 30, 229–234 [CrossRef] [EDP Sciences] [Google Scholar]
  • Moritz R.F.A., de Miranda J., Fries I., Le Conte Y., Neumann P., Paxton R. (2010) Research Strategies to Improve Honeybee Health in Europe, Apidologie, 227–242. [CrossRef] [EDP Sciences] [Google Scholar]
  • Munoz I., Garrido-Bailon E., Martin-Hernandez R., Meana A., Higes M., De la Rua P. (2008) Genetic profile of Varroa destructor infesting Apis mellifera iberiensis colonies, J. Apic. Res. 47, 310–313 [CrossRef] [Google Scholar]
  • Navajas M., Anderson D.L., L.I. D.G., Huang Z.-Y., J.C., Zhou T., Le Conte Y. (2009) New Asian types of Varroa destructor: a potential new threat for world apiculture, Apidologie, DOI: 10.1051/apido/2009068. [Google Scholar]
  • Nazzi F., Milani N. (1996) The presence of inhibitors of the reproduction of Varroa jacobsoni Oud. (Gamasida: Varroidae) in infested cells, Exp. Appl. Acarol. 20, 617–623 [NASA ADS] [CrossRef] [EDP Sciences] [MathSciNet] [PubMed] [Google Scholar]
  • Oldroyd B.P. (1999) Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees, Trends Ecol. Evol. 14, 312–315 [CrossRef] [PubMed] [Google Scholar]
  • Ongus J.R., Peters D., Bonmatin J.M., Bengsch E., Vlak J.M., van Oers M.M. (2004) Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor, J. Gen. Virol. 85, 3747–3755 [CrossRef] [PubMed] [Google Scholar]
  • Peng Y.S., Fang Y., Xu S., Ge L. (1987) The resistance Mecanism of the Asian Honey Bee, Apis cerana Fabr., to an Ectoparasitic Mite, Varroa jacobsoni Oudemans, J. Invertebr. Pathol. 49, 54–60 [CrossRef] [Google Scholar]
  • Pettis J.S., Delaplane K.S. (2010) Coordinated Responses to Honey Bee Decline in the USA, Apidologie 41, 256–263. [CrossRef] [EDP Sciences] [Google Scholar]
  • Rinderer T., Harris J.W., Hunt G., de Guzman L. (2010) Breeding for resistance to Varroa destructor in North America, Apidologie 41, 409–424. [CrossRef] [EDP Sciences] [Google Scholar]
  • Ritter W. (1988) Varroa jacobsoni in Europe, the tropics, and subtropics, in: Needham, G.R., Page R.E., Delfinado-Baker M., Bowman C.E. (Eds.), Africanized Honey bees and bee mites, John Wiley, New York, pp. 349–359. [Google Scholar]
  • Ritter W. (1993) New results of the development of tolerance to Varroa jacobsoni in bee colonies in Tunisia, Wicwas Press, Cheshire, USA, pp. 463–467. [Google Scholar]
  • Ritter W., Perschil F. (1982) Controlling Varroa Disease with Folbex Va Neu, Apidologie 13, 323–324 [Google Scholar]
  • Ritter W., Leclercq E., Koch W. (1984) Observations on Bee and Varroa Mite Populations in Infested Honey Bee Colonies, Apidologie 15, 389–399 [CrossRef] [EDP Sciences] [Google Scholar]
  • Romero-Vera C., Otero-Colina G. (2002) Effect of single and successive infestation of Varroa destructor and Acarapis woodi on the longevity of worker honey bees Apis mellifera, Am. Bee J. 142, 54–57 [Google Scholar]
  • Schneider P., Drescher W. (1987) The influence of Varroa jacobsoni Oud. on weight; development on weight and hypopharyngeal glands; and longevity of Apis mellifera L., Apidologie 18, 101–110. [CrossRef] [EDP Sciences] [Google Scholar]
  • Seeley T.D. (2007) Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States, Apidologie 38, 19–29 [CrossRef] [EDP Sciences] [Google Scholar]
  • Shen M.Q., Yang X.L., Cox-Foster D., Cui L.W. (2005) The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees, Virology 342, 141–149 [CrossRef] [PubMed] [Google Scholar]
  • Solignac M., Cornuet J.M., Vautrin D., Le Conte Y., Anderson D., Evans J., Cros-Arteil S., Navajas M. (2005) The invasive Korea and Japan types of Varroa destructor, ectoparasitic mites of the Western honeybee (Apis mellifera), are two partly isolated clones, Proc. R. Soc. Lond. Ser. B-Biol. Sci. 272, 411–419 [CrossRef] [Google Scholar]
  • Sumpter D.J.T., Martin S.J. (2004) The dynamics of virus epidemics in Varroa-infested honey bee colonies, J. Anim. Ecol. 73, 51–63 [CrossRef] [Google Scholar]
  • Tentcheva D., Gauthier L., Zappulla N., Dainat B., Cousserans F., Colin M.E., Bergoin M. (2004) Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France, Appl. Environ. Microbiol. 70, 7185–7191 [CrossRef] [PubMed] [Google Scholar]
  • Tentcheva D., Gauthier L., Bagny L., Fievet J., Dainat B., Cousserans F., Colin M.E., Bergoin M. (2006) Comparative analysis of deformed wing virus (DWV) RNA in Apis mellifera and Varroa destructor, Apidologie 37, 41–50 [CrossRef] [EDP Sciences] [Google Scholar]
  • Trouiller J., Milani N. (1999) Stimulation of Varroa jacobsoni Oud. oviposition with semiochemicals from honeybee brood, Apidologie 30, 3–12 [CrossRef] [EDP Sciences] [Google Scholar]
  • Vandame R., Palacio M.A. (2010) Preserved honey bee health in Latin America: a fragile equilibrium due to low-intensity agriculture and beekeeping? Apidologie 41, 243–255. [CrossRef] [EDP Sciences] [Google Scholar]
  • vanEngelsdorp D., Evans J.D., Saegerman C., Mullin C., Haubruge E., Nguyen B.K., Frazier M., Frazier J., Cox-Foster D., Chen Y., Underwood R., Tarpy D.R., Pettis J.S. (2009) Colony collapse disorder: a descriptive study, PLoS One 4, DOI: 10.1371/journal.pone.0006481. [Google Scholar]
  • Vasquez A., Olofsson T.C., Sammataro D. (2009) A scientific note on the lactic acid bacterial flora in honeybees in the USA – A comparison with bees from Sweden, Apidologie 40, 26–28 [CrossRef] [EDP Sciences] [Google Scholar]
  • Wallner K. (1999) Varroacides and their residues in bee products, Apidologie 30, 235–248 [CrossRef] [EDP Sciences] [Google Scholar]
  • Yang X., Cox-Foster D. (2007) Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge, Parasitology 134, 405–412 [CrossRef] [PubMed] [Google Scholar]
  • Yang X.L., Cox-Foster D.L. (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification, Proc. Natl. Acad. Sci. USA 102, 7470–7475 [CrossRef] [Google Scholar]
  • Yue C., Schroder M., Bienefeld K., Genersch E. (2006) Detection of viral sequences in semen of honeybees (Apis mellifera): Evidence for vertical transmission of viruses through drones, J. Invertebr. Pathol. 92, 105–108 [CrossRef] [PubMed] [Google Scholar]
  • Yue C., Schroder M., Gisder S., Genersch E. (2007) Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera), J. Gen. Virol. 88, 2329–2336 [CrossRef] [PubMed] [Google Scholar]