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Challenges for developing pathogen-based biopesticides against Varroa destructor (Mesostigmata: Varroidae)

Abstract

Control of the major pest of apiculture, the ectoparasitic mite Varroa destructor using pathogen-based biopesticides would resolve many of the problems experienced with other forms of control, such as chemical control, hive manipulation, or selection of resistant honeybee strains. Several research groups have developed and tested fungus-based biopesticides in laboratory and field experiments, with varying results. While biopesticides have many desirable qualities, including much lower risk of honey contamination and of pest resistance, future research needs to focus on: (1) identification of the sub-population(s) of V. destructor affected by biopesticides and the duration and impact of the application on mite population dynamics; (2) development of an effective, easily applied formulation, and (3) evaluation of possible side or sublethal effects on bees themselves. Biopesticides need to be evaluated on the field (colony) level in addition to the laboratory level. Researchers should consider providing data that can be easily used to evaluate effect, such as mite drop counts onto sticky boards coupled with assessments of phoretic mite density or brood cell mite density. Exploration for naturally occurring pathogens should be conducted in the native range of V. destructor in Asia.

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References

  • Anderson, D.L., Trueman, J.W.H. (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. Appl. Acarol. 24, 165–189

    Article  CAS  PubMed  Google Scholar 

  • Bugeme, D.M., Knapp, M., Boga, H.I., Wanjoya, A.K., Maniania, N.K. (2010) Influence of temperature on virulence of fungal isolates of Metarhizium anisopliae and Beauveria bassiana to the two-spotted spider mite Tetranychus urticae. Mycologia 167, 221–227

    Google Scholar 

  • Burges, H.D. (1998) Chapter 4. Formulation of mycoinsecticides. In: Burges, H.D. (ed.) Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments, pp. 131–185. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Calderón, R.A., Rivera, G., Sánchez, L.A., Zamora, L.G. (2004) Chalkbrood (Ascosphaera apis) and some other fungi associated with Africanized honey bees (Apis mellifera) in Costa Rica. J. Apic. Res. 43, 187–188

    Google Scholar 

  • Calderone, N.W., Lin, S. (2001) Behavioural responses of Varroa destructor (Acari: Varroidae) to extracts of larvae, cocoons and brood food of worker and drone honey bees, Apis mellifera (Hymenoptera: Apidae). Physiol. Entomol. 26(4), 341–350

    Article  CAS  Google Scholar 

  • Chandler, D., Davidson, G., Pell, J.K., Ball, B.V., Shaw, K., Sunderland, K.D. (2000) Fungal biocontrol of Acari. Biocontr. Sci. Technol. 10, 357–384

    Article  Google Scholar 

  • Chandler, D., Sunderland, K.D., Ball, B.V., Davidson, G. (2001) Prospective biological control agents for Varroa destructor n. sp., an important pest of the European honey bee, Apis mellifera. Biocontr. Sci. Technol. 11, 429–448

    Article  Google Scholar 

  • Chen, Y., Evans, J., Feldlaufer, M. (2006) Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J. Invert. Pathol. 92, 152–159

    Article  Google Scholar 

  • Chernov, K.S. (1981) Transmission of mycoses, an aspect of Varroa infestations. Byulletin Vsesoyuznogo Instituta Eksperimental noi Veternarii 41, 59–60 (in Russian)

    Google Scholar 

  • Cherry, A., Jenkins, N., Heviefo, G., Bateman, R.P., Lomer, C. (1999) A West African pilot scale production plant for aerial conidia of Metarhizium sp. for use as a mycoinsecticide against locusts and grasshoppers. Biocontr. Sci. Technol. 9, 35–51

    Article  Google Scholar 

  • Damiani, N., Gende, L.B., Maggi, M.D., Palacios, S., Marcangeli, J.A., Eguaras, M.J. (2010) Repellent and acaricidal effects of botanical extracts on Varroa destructor. Parasitol. Res. 108, 79–86

    Article  PubMed  Google Scholar 

  • Davidson, G., Phelps, K., Sunderland, K.D., Pell, J.K., Ball, B.V., Shaw, K.E., Chandler, D. (2003) Study of temperature–growth interactions of entomopathogenic fungi with potential for control of Varroa destructor (Acari: Mesostigmata) using a nonlinear model of poikilotherm development. J. Appl. Microbiol. 94, 816–825

    Article  CAS  PubMed  Google Scholar 

  • Delaplane, K.S., Berry, J.A., Skinner, J.A., Parkman, J.P., Hood, W.M. (2005) Integrated pest management against Varroa destructor reduces colony mite levels and delays treatment threshold. J. Apic. Res. 44(4), 157–162

    Google Scholar 

  • Dogan, B., Boor, K.J. (2003) Genetic diversity and spoilage potentials among Pseudomonas spp. isolated from fluid milk products and dairy processing plants. Appl. Environ. Microbiol. 69, 130–138

    Article  CAS  PubMed  Google Scholar 

  • Donovan, B.J., Paul, F. (2005) Pseudoscorpions: the forgotten beneficials inside beehives and their potential for management for control of varroa and other arthropod pests. Bee World 86(4), 83–87

    Google Scholar 

  • Eguaras, M.J., Fuselli, S., Gende, L., Fritz, R., Ruffinengo, S.R., Clemente, G., Gonzalez, A., Bailac, P.N., Ponzi, M.I. (2005) An in vitro evaluation of Tagetes minuta essential oil for the control of the honeybee pathogens Paenibacillus larvae and Ascosphaera apis, and the parasitic mite Varroa destructor. J. Essent. Oil Res. 17(3), 336–340

    Article  CAS  Google Scholar 

  • Ellis, J.D., Munn, P.A. (2005) The worldwide health status of honey bees. Bee World 86, 88–101

    Google Scholar 

  • Ellis, A.M., Hayes, G.W., Ellis, J.D. (2009) The efficacy of dusting honey bee colonies with powdered sugar to reduce Varroa mite populations. J. Apic. Res. 48(1), 72–76

    Article  Google Scholar 

  • Evans, J.D., Spivak, M. (2010) Socialized medicine: individual and communal disease barriers in honey bees. J. Invert. Pathol. 103, S62–S72

    Article  Google Scholar 

  • Fakhimzadeh, K. (2001) Effectiveness of confectioner sugar dusting to knock down Varroa destructor from adult honey bees in laboratory trials. Apidologie 32, 139–148

    Article  Google Scholar 

  • Farenhorst, M., Mouatcho, J.C., Kikankie, C.K., Brooke, B.D., Hunt, R.H., Thomas, M.B., Koekemoer, L.L., Knols, B.G.J., Coetzee, M. (2009) Fungal infection counters insecticide resistance in African malaria mosquitoes. Proc. Natl. Acad. Sci. USA 106, 17443–17447

    Article  CAS  PubMed  Google Scholar 

  • Fargues, J., Maniania, N.K., Delmas, J.C., Smits, N. (1992) Influence de la température sur la croissance in vitro d’hyphomycètes entomopathogènes. Agronomie 12, 557–564

    Article  Google Scholar 

  • Fries, I., Camazine, S., Sneyd, J. (1994) Population dynamics of Varroa jacobsoni: a model and a review. Bee World 75, 4–28

    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

    Article  Google Scholar 

  • García-Fernández, P., Santiago-Álvarez, C., Quesada-Moraga, E. (2008) Pathogenicity and thermal biology of mitosporic fungi as potential microbial control agents of Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of honey bee, Apis mellifera (Hymenoptera: Apidae). Apidologie 39, 662–673

    Article  Google Scholar 

  • Gutierrez, A.P., Caltagirone, L., Meikle, W. (1999) Evaluation of results: economics of biological control. In: Bellows, T.S., Fisher, T.W. (eds.) Handbook of biological control, pp. 243–252. Academic Press, San Diego, CA

    Chapter  Google Scholar 

  • Guzmán-Novoa, E., Eccles, L., Calvete, Y., Mcgowan, J., Kelly, P.G., Correa-Benítez, 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 41, 443–450

    Article  Google Scholar 

  • Haas, D., Dèfago, G. (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Rev. Microbiol. 3, 307–319. PMID 15759041

    Article  CAS  Google Scholar 

  • Harbo, J.R., Harris, J.W. (2004) Effect of screen floors on populations of honey bees and parasitic mites (Varroa destructor). J. Apic. Res. 43, 114–117

    Google Scholar 

  • Hayek, A., Delalibera, I. (2010) Fungal pathogens as classical biological control agents against arthropods. BioControl 55, 147–158

    Article  Google Scholar 

  • Herbert Jr., E.W. (1992) Chapter 6. Honey bee nutrition. In: Graham, J.M. (ed.) The hive and the honey bee, pp. 197–233. Dadant & Sons, Hamilton, IL

    Google Scholar 

  • Holder, D.J., Kirkland, B.H., Lewis, M.W., Keyhani, N.O. (2007) Surface characteristics of the entomopathogenic fungus Beauveria (Cordyceps) bassiana. Microbiology 153, 3448–3457

    Article  CAS  PubMed  Google Scholar 

  • Hong, T.D., Gunn, J., Ellis, R.H., Jenkins, N.E., Moore, D. (2001) The effect of storage environment on the longevity of conidia of Beauveria bassiana. Mycol. Res. 105, 597–602

    Article  Google Scholar 

  • Human, H., Nicolson, S.W., Dietemann, V. (2006) Do honeybees, Apis mellifera scutellata, regulate humidity in their nest? Naturwissenschaften 93, 397–401

    Article  CAS  PubMed  Google Scholar 

  • Illies, I., Mühlen, W., Dücker, G., Sachser, N. (2002) The influence of different bee traps on undertaking behaviour of the honey bee (Apis mellifera) and development of a new trap. Apidologie 33(3), 315–326

    Article  Google Scholar 

  • Islam, M., Castle, T., Ren, S.J. (2010) Compatibility of the insect pathogenic fungus Beauveria bassiana with neem against sweetpotato whitefly, Bemisia tabaci, on eggplant. Entomol. Exp. Appl. 134, 28–34

    Article  Google Scholar 

  • James, R.R. (2009) Microbial control for invasive arthropod pests in honey bees. In: Hajek, A.E., Glare, T.R., O’Callahan, M. (eds.) Use of microbes for control and eradication of invasive arthropods, pp. 271–288. Springer, Dordrecht, The Netherlands

    Chapter  Google Scholar 

  • James, R.R., Hayes, G. (2007) Microbial control of varroa: misadventures in the field. J. Anhui Agric. Univ. 34(2), 162–166

    Google Scholar 

  • James, R.R., Hayes, G., Leland, J.E. (2006) Field trials on the microbial control of varroa with the fungus Metarhizium anisopliae. Am. Bee J. 146(11), 968–972

    Google Scholar 

  • Jaronski, S.T. (2010) Ecological factors in the inundative use of fungal entomopathogens. BioControl 55, 159–185

    Article  Google Scholar 

  • Kanga, L.H.B., James, R.R., Boucias, D.G. (2002) Hirsutella thompsonii and Metarhizium anisopliae as potential microbial control agents of Varroa destructor, a honey bee parasite. J. Invertebr. Pathol. 81, 175–184

    Article  CAS  PubMed  Google Scholar 

  • Kanga, L.H.B., Jones, W.A., James, R.R. (2003) Field trials using the fungal pathogen, Metarhizium anisopliae (Deuteromycetes: Hyphomycetes) to control the ectoparasitic mite, Varroa destructor (Acari: Varroidae) in honey bee, Apis mellifera (Hymenoptera: Apidae) colonies. J. Econ. Entomol. 96, 1091–1099

    Article  PubMed  Google Scholar 

  • Kanga, L.H.B., Jones, W.A., James, R.R. (2005) Enlisting fungi to protect the honey bee. Biologist 52(2), 88–94

    Google Scholar 

  • Kanga, L.H.B., Adamczyk, J., Patt, J., Gracia, C., Cascino, J. (2010) Development of a user-friendly delivery method for the fungus Metarhizium anisopliae to control the ectoparasitic mite Varroa destructor in honey bee, Apis mellifera, colonies. Exp. Appl. Acarol. 52, 327–342

    Article  PubMed  Google Scholar 

  • Kleespies, R.G., Radtke, J., Bienefeld, K. (2000) Virus-like particles found in the ectoparasitic bee mite Varroa jacobsoni Oudemans. J. Invertebr. Pathol. 75(1), 87–90

    Article  CAS  PubMed  Google Scholar 

  • Korpela, S., Aarhus, A., Fries, I., Hansen, H. (1992) Varroa jacobsoni Oud. in cold climates: population growth, winter mortality and influence on the survival of honey bee colonies. J. Apic. Res. 31, 157–164

    Google Scholar 

  • Kraus, B., Page, R.E. (1995) Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral Apis mellifera (Hymenoptera: Apidae) in California. Environ. Entomol. 24, 1473–1480

    Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Maggi, M.D., Ruffinengo, S.R., Gende, L.B., Sarlo, E.G., Eguaras, M.J., Bailac, P.N., Ponzi, M.I. (2010) Laboratory evaluations of Syzygium aromaticum (L.) Merr. et Perry essential oil against Varroa destructor. J. Essential Oil Res. 22(2), 119–122

    Article  CAS  Google Scholar 

  • Martin, S.J. (1998) A population model for the ectoparasitic mite Varroa jacobsoni in honey bee (Apis mellifera) colonies. Ecol. Modelling 109, 267–281

    Article  Google Scholar 

  • Meikle, W.G., Jaronski, S., Mercadier, G., Quimby, P.C. (2003) A distributed delay routine-based simulation model of Beauveria bassiana conidial stability in response to environmental stressors. BioControl 48, 561–578

    Article  Google Scholar 

  • Meikle, W.G., Mercadier, G., Girod, V., Derouané, F., Jones, W.A. (2006) Evaluation of Beauveria bassiana (Balsamo) Vuillemin (Deuteromycota: Hyphomycetes) strains isolated from varroa mites in southern France. J. Apic. Res. 45, 219–220

    Article  Google Scholar 

  • Meikle, W.G., Mercadier, G., Holst, N., Nansen, C., Girod, V. (2007) Duration and spread of an entomopathogenic fungus, Beauveria bassiana (Deuteromycota: Hyphomycetes), used to treat varroa mites, Varroa destructor (Acari: Varroidae), in honeybee hives (Hymenoptera: Apidae). J. Econ. Entomol. 100(1), 1–10

    Article  CAS  PubMed  Google Scholar 

  • Meikle, W.G., Mercadier, G., Holst, N., Girod, V. (2008a) Impact of two treatments of a formulation of Beauveria bassiana (Deuteromycota: Hyphomycetes) conidia on Varroa mites (Acari: Varroidae) and on honeybee (Hymenoptera: Apidae) colony health. Exp. Appl. Acarol. 46, 105–117

    Article  PubMed  Google Scholar 

  • Meikle, W.G., Mercadier, G., Holst, N., Nansen, C., Girod, V. (2008b) Impact of a treatment of Beauveria bassiana (Deuteromycota: Hyphomycetes) on honeybee (Hymenoptera: Apidae) colony health and on varroa mites (Acari: Varroidae). Apidologie 39, 1–13

    Article  Google Scholar 

  • Meikle, W.G., Mercadier, G., Annas, F., Holst, N. (2009) Effects of multiple applications of a Beauveria-based biopesticide on Varroa destructor (Acari: Varroidae) densities in honey bee (Hymenoptera: Apidae) colonies. J. Apic. Res. 48, 220–222

    Article  CAS  Google Scholar 

  • Meikle, W.G., Mercadier, G., Guermache, F., Bon, M.-C. (2012) Pseudomonas contamination of a fungus-based biopesticide: implications for honey bee (Hymenoptera: Apidae) health and varroa mite (Acari: Varroidae) control. Biol. Contr. (in press)

  • Mitchell, C.E., Power, A.G. (2003) Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627

    Article  CAS  PubMed  Google Scholar 

  • Moritz, R.F.A., Kraus, B.F., Kryger, P., Crewe, R.M. (2007) The size of wild honeybee populations (Apis mellifera) and its implications for the conservation of honeybees. Insect Conserv. 11, 391–397

    Article  Google Scholar 

  • Muerrle, T.M., Neumann, P., Dames, J.F., Hepburn, H.R., Hill, M.P. (2006) Susceptibility of adult Aethina tumida (Coleoptera: Nitidulidae) to entomopathogenic fungi. J. Econ. Entomol. 99(1), 1–6

    Article  CAS  PubMed  Google Scholar 

  • Neumann, P., Carreck, N. (2010) Honey bee colony losses. J. Apic. Res. 49, 1–6

    Article  Google Scholar 

  • Niu, G., Johnson, R.M., Berenbaum, M.R. (2011) Toxicity of mycotoxins to honeybees and its amelioration by propolis. Apidologie 42(1), 79–87

    Article  CAS  Google Scholar 

  • Ostiguy, N., Sammataro, D. (2000) A simplified technique for counting Varroa jacobsoni Oud. on sticky boards. Apidologie 31, 707–716

    Article  Google Scholar 

  • Perkins, J.H., Garcia, R. (1999) Social and economic factors affecting research and implementation of biological control. In: Bellows, T.S., Fisher, T.W. (eds.) Handbook of biological control, pp. 993–1009. Academic Press, San Diego, CA

    Chapter  Google Scholar 

  • Rath, W. (1999) Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie 30, 97–110

    Article  Google Scholar 

  • Rath, A.C. (2000) The use of entomopathogenic fungi for control of termites. Biocontr. Sci. Technol. 10, 563–581

    Article  Google Scholar 

  • Reber, A., Purcell, J., Buechel, S.D., Buri, P., Chapuisat, M. (2011) The expression and impact of antifungal grooming in ants. J. Evol. Biol. 24, 954–964

    Article  CAS  PubMed  Google Scholar 

  • Reddy, G.V.P., Guerrero, A. (2010) New pheromones and insect control strategies. Vitamins and Hormones 83(C), 493–519

    Article  CAS  PubMed  Google Scholar 

  • Rehner, S.A., Minnis, A.M., Sung, G.-H., Luangsa-ard, J.J., Devotto, L., Humber, R.A. (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103(5), 1055–1073

    Article  PubMed  Google Scholar 

  • Rodríguez, M., Gerding, M., France, A. (2009a) Selection of entomopathogenic fungi to control Varroa destructor (Acari: Varroidae). Chil. J. Agric. Res. 69, 534–540

    Google Scholar 

  • Rodríguez, M., Gerding, M., France, A., Ceballos, R. (2009b) Evaluation of Metarhizium anisopliae var. anisopliae qu-M845 isolate to control Varroa destructor (Acari: Varroidae) in laboratory and field trials. Chil. J. Agric. Res. 69(4), 541–547

    Google Scholar 

  • Rosengaus, R.B., Cornelisse, T., Guschanski, K., Traniello, J.F.A. (2007) Inducible immune proteins in the dampwood termite Zootermopsis angusticollis. Naturwissenschaften 94, 25–33

    Article  CAS  PubMed  Google Scholar 

  • Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010) Biology and control of Varroa destructor. J. Invert. Pathol. 103, S96–S119

    Article  Google Scholar 

  • Ruffinengo, S.R., Eguaras, M.J., Cora, D., Rodriguez, E., Bedascarrasbure, E., Bailac, P.N., Ponzi, M.I. (2002) Biological activity of Heterotheca latifolia essential oil against Varroa jacobsoni. J. Essential Oil Res. 14, 462–464

    Article  CAS  Google Scholar 

  • Sacchetti, R., De Luca, G., Zanetti, F. (2007) Influence of material and tube size on DUWLs contamination in a pilot plant. New Microbiologica 30, 29–34

    PubMed  Google Scholar 

  • Sammataro, D., Arlinghaus, S.L. (2011) The quest to save honey: tracking bee pests using mobile technology, www.mylovedone.com/image/solstice/win10/SammataroandArlinghaus

  • Schäfer, M., Ritter, W., Pettis, J.S., Neumann, P. (2010) Winter losses of honeybee colonies (Hymenoptera: Apidae): the role of infestations with Aethina tumida (Coleoptera: Nitidulidae) and Varroa destructor (Parasitiformes: Varroidae). J. Econ. Entomol. 103, 10–16

    Article  PubMed  Google Scholar 

  • Shaw, K.E., Davidson, G., Clark, S.J., Ball, B.V., Pell, J.K., Chandler, D., Sunderland, K.D. (2002) Laboratory bioassays to assess the pathogenicity of mitosporic fungi to Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of the honeybee, Apis mellifera. Biol. Contr. 24, 266–276

    Article  Google Scholar 

  • Stafford III, K.C., Allan, S.A. (2011) Field applications of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae F52 (Hypocreales: Clavicipitaceae) for the control of Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 47, 1107–1115

    Article  Google Scholar 

  • Steenberg, T., Kryger, P., Holst, N. (2010) A scientific note on the fungus Beauveria bassiana infecting Varroa destructor in worker brood cells in honey bee hives. Apidologie 41, 127–128

    Article  Google Scholar 

  • Stow, A., Briscoe, D., Gillings, M., Holley, M., Smith, S., Leys, R., Silberbauer, T., Turnbull, C., Beattie, A. (2007) Antimicrobial defenses increase with sociality in bees. Biol. Lett. 3, 422–424

    Article  PubMed  Google Scholar 

  • Strasser, H., Vey, A., Butt, T.M. (2000) Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species? Biocontr. Sci. Technol. 10, 717–735

    Article  Google Scholar 

  • Su, N.-Y., Hillis-Starr, Z., Ban, P.M., Scheffrahn, R.H. (2003) Protecting historic properties from subterranean termites: a case study with Fort Christiansvaern, Christiansted National Historic Site, United States Virgin Islands. Am. Entomol. 49, 20–32

    Google Scholar 

  • Swanson, J.A.I., Torto, B., Kells, S.A., Mesce, K.A., Tumlinson, J.H., Spivak, M. (2009) Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. J. Chem. Ecol. 35, 1108–1116

    Article  CAS  PubMed  Google Scholar 

  • Tanada, Y., Kaya, H.K. (1993) Insect pathology. Academic Press, San Diego, CA, USA

    Google Scholar 

  • Thomas, M.B., Wood, S.N., Lomer, C.J. (1995) Biological control of locusts and grasshoppers using a fungal pathogen: the importance of secondary cycling. Proceedings of the Royal Society B: Biological Sciences 259, 265–270

    Article  Google Scholar 

  • Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J., Kuris, A.M. (2003) Introduced species and their missing parasites. Nature 421, 628–630

    Article  CAS  PubMed  Google Scholar 

  • Tsagou, V., Lianou, A., Lazarakis, D., Emmanouel, N., Aggelis, G. (2004) Newly isolated bacterial strains belonging to Bacillaceae (Bacillus sp.) and Micrococcaceae accelerate death of the honey bee mite, Varroa destructor (V. jacobsoni), in laboratory assays. Biotechnol. Lett. 26(6), 529–532

    Article  CAS  PubMed  Google Scholar 

  • Tu, S., Qiu, X., Cao, L., Han, R., Zhang, Y., Liu, X. (2010) Expression and characterization of the chitinases from Serratia marcescens GEI strain for the control of Varroa destructor, a honey bee parasite. J. Invert. Pathol. 104(2), 75–82

    Article  CAS  Google Scholar 

  • Van der Geest, L.P.S., Elliot, S.L., Breeuwer, J.A.J., Beerling, E.A.M. (2000) Diseases of mites. Exp. Appl. Acarol. 24, 497–560

    Article  PubMed  Google Scholar 

  • Vargas, R.I., Piñero, J.C., Mau, R.F.L., Jang, E.B., Klungness, L.M, McInnis, D.O., Harris, E.B., McQuate, G.T., Bautista, R.C., Wong, L. (2010) Area-wide suppression of the mediterranean fruit fly, Ceratitis capitata, and the oriental fruit fly, Bactrocera dorsalis, in Kamuela, Hawaii. J. Ins. Sci. 10:135

  • Wantuch, H.A., Tarpy, D.R. (2009) Removal of drone brood from Apis mellifera (Hymenoptera: Apidae) colonies to control Varroa destructor (Acari: Varroidae) and retain adult drones. J. Econ. Entomol. 102(6), 2033–2040

    Article  PubMed  Google Scholar 

  • Winston, M.L. (1992) The honey bee colony: life history. In: Graham, J.M. (ed.) The hive and the honey bee, pp. 197–234. Dadant & Sons, Hamilton, IL

    Google Scholar 

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Acknowledgements

We thank J.J. Adamczyk, R.R. James, P. Moran, and two anonymous reviewers for their help in improving the manuscript. Financial support was given by the Montagu foundation to JP and the FP7 projects BEEDOC and STEP to PN.

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Correspondence to William Grems Meikle.

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Manuscript Editor: David Tarpy

Défis à relever pour le développement de biopesticides à base de pathogènes contre Varroa destructor (Mesostigmata: Varroidae).

Apis mellifera / Varroa destructor / lutte biologique / champignons entomopathogènes

Anforderungen für die Entwicklung von Biopestiziden auf Pathogenbasis gegen Varroa destructor (Mesostigmata: Varroidae).

Apis mellifera / Varroa destructor / biologische Kontrollle / entomopathogene Pilze

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Meikle, W.G., Sammataro, D., Neumann, P. et al. Challenges for developing pathogen-based biopesticides against Varroa destructor (Mesostigmata: Varroidae). Apidologie 43, 501–514 (2012). https://doi.org/10.1007/s13592-012-0118-0

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Keywords

  • Apis mellifera
  • Varroa destructor
  • biological control
  • entomopathogenic fungi