Entomopathogenic Fungi for Pests and Predators Control in Beekeeping
Abstract
:1. Introduction
2. Entomopathogenic Fungi (EPF)
2.1. Infection and Pathogenic Mechanisms
2.2. Host Defense Mechanisms
3. Detection and Preparation of Entomopathogenic Fungi for Experimental Assays
4. Laboratory Assay and Field Studies for Varroa destructor, Aethina tumida and Vespidae Control
4.1. Use of Fungal Entomopathogens in the Control of Varroa destructor Infestation
4.2. Susceptibility of Honey Bee to Entomopathogenic Fungi
4.3. Use of Fungal Entomopathogens in the Control of Aethina tumida Infestation
4.4. Use of Fungal Entomopathogens in the Control of Vespidae
5. Biotic and Abiotic Factors Affecting the Activity of Fungi
6. Formulations and Methods of Application
7. Conclusions and Outlook
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Corbet, S.A.; Williams, I.H.; Osborne, J.L. Bees and the Pollination of Crops and Wild Flowers in the European Community. Bee World 2015, 72, 47–59. [Google Scholar] [CrossRef]
- Morse, R.A.; Calderone, N.W. The value of honey bees as pollinators of US crops in 2000. Bee Cult. 2000, 128, 1–15. [Google Scholar]
- Balica, G.; Vostinaru, O.; Stefanescu, C.; Mogosan, C.; Iaru, I.; Cristina, A.; Pop, C.E. Potential Role of Propolis in the Prevention and Treatment of Metabolic Diseases. Plants 2021, 10, 883. [Google Scholar] [CrossRef]
- Nagai, T.; Inoue, R. Preparation and the functional properties of water extract and alkaline extract of royal jelly. Food Chem. 2004, 84, 181–186. [Google Scholar] [CrossRef]
- Eteraf-Oskouei, T.; Najafi, M. Traditional and modern uses of natural honey in human diseases: A review. Iran. J. Basic Med. Sci. 2013, 16, 731. [Google Scholar] [CrossRef]
- Neumann, P.; Carreck, N.L. Honey bee colony losses. J. Apic. Res. 2015, 49, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Goblirsch, M. Nosema ceranae disease of the honey bee (Apis mellifera). Apidologie 2018, 49, 131–150. [Google Scholar] [CrossRef] [Green Version]
- Dietemann, V.; Nazzi, F.; Martin, S.J.; Anderson, D.L.; Locke, B.; Delaplane, K.S.; Wauquiez, Q.; Tannahill, C.; Frey, E.; Ziegelmann, B.; et al. Standard methods for Varroa research. J. Apic. Res. 2013, 52, 1–54. [Google Scholar] [CrossRef] [Green Version]
- Neumann, P.; Pettis, J.S.; Schäfer, M.O. Quo vadis Aethina tumida? Biology and control of small hive beetles. Apidologie 2016, 47, 427–466. [Google Scholar] [CrossRef] [Green Version]
- Bogdanov, S.; Liebefeld, A. Contaminants of bee products. Apidologie 2006, 37, 1–18. [Google Scholar] [CrossRef] [Green Version]
- Mullin, C.A.; Frazier, M.; Frazier, J.L.; Ashcraft, S.; Simonds, R.; vanEngelsdorp, D.; Pettis, J.S. High levels of miticides and agrochemicals in north american apiaries: Implications for honey bee health. PLoS ONE 2010, 5, e9754. [Google Scholar] [CrossRef] [Green Version]
- Higes, M.; Martín-Hernández, R.; Sara Hernández-Rodríguez, C.; González-Cabrera, J. Assessing the resistance to acaricides in Varroa destructor from several Spanish locations. Parasitol. Res. 2020, 119, 3595–3601. [Google Scholar] [CrossRef]
- Daniel Maggi, M.; RuYnengo, S.R.; Damiani, N.; Sardella, N.H.; Eguaras, M.J. First detection of Varroa destructor resistance to coumaphos in Argentina. Exp. Appl. Acarol. 2009, 47, 317–320. [Google Scholar] [CrossRef]
- Pettis, J.S. Scientific note A scientific note on Varroa destructor resistance to coumaphos in the United States. Apidologie 2004, 35, 91–92. [Google Scholar] [CrossRef] [Green Version]
- Lodesani, M.; Costa, C.; Serra, G.; Colombo, R.; Sabatini, A.G. Acaricide residues in beeswax after conversion to organic beekeeping methods*. Apidologie 2008, 39, 324–333. [Google Scholar] [CrossRef]
- Pietropaoli, M.; Skerl, M.S.; Cazier, J.; Riviere, M.-P.; Tiozzo, B.; Eggenhoeffner, R.; Gregorc, A.; Haefeker, W.; Higes, M.; Ribarits, A.; et al. BPRACTICES Project: Towards a sustainable european beekeeping. Bee World 2020, 97, 66–69. [Google Scholar] [CrossRef]
- 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. Fungal infection counters insecticide resistance in African malaria mosquitoes. Proc. Natl. Acad. Sci. USA 2009, 106, 17443–17447. [Google Scholar] [CrossRef] [Green Version]
- Farenhorst, M.; Knols, B.G.J.; Thomas, M.B.; Howard, A.F.V.; Takken, W.; Rowland, M.; N’Guessan, R. Synergy in efficacy of fungal entomopathogens and permethrin against west african insecticide-resistant anopheles gambiae mosquitoes. PLoS ONE 2010, 5, e12081. [Google Scholar] [CrossRef]
- Wu, S.; Toews, M.D.; Oliveira-Hofman, C.; Behle, R.W.; Simmons, A.M.; Shapiro-Ilan, D.I. Environmental Tolerance of Entomopathogenic Fungi: A new strain of Cordyceps javanica isolated from a whitefly epizootic versus commercial fungal strains. Insects 2020, 11, 711. [Google Scholar] [CrossRef]
- Bamisile, B.S.; Akutse, K.S.; Siddiqui, J.A.; Xu, Y. Model application of entomopathogenic fungi as alternatives to chemical pesticides: Prospects, challenges, and insights for next-generation sustainable agriculture. Front. Plant Sci. 2021, 12, 2132. [Google Scholar] [CrossRef]
- Vandenberg, J.D. Safety of four entomopathogens for caged adult honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 1990, 83, 755–759. [Google Scholar] [CrossRef]
- Al Mazra’awi, M. Impact of the entomopathogenic fungus Beauveria bassiana on the honey bees, Apis mellifera (Hymenoptera: Apidae). World J. Agric. Sci. 2007, 3, 7–11. [Google Scholar]
- Meikle, W.G.; Mercadier, G.; Girod, V.; Derouané, F.; Jones, W.A. Evaluation of Beauveria bassiana (balsamo) vuillemin (deuteromycota: Hyphomycetes) strains isolated from varroa mites in southern France. J. Apic. Res. 2006, 45, 219–220. [Google Scholar] [CrossRef]
- Houssou, L.; Kanga, B.; Jones, W.A.; James, R.R. 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. 2003, 96, 1091–1099. [Google Scholar] [CrossRef]
- Lord, J.C. Response of the wasp Cephalonomia tarsalis (Hymenoptera: Bethylidae) to Beauveria bassiana (Hyphomycetes: Moniliales) as free conidia or infection in its host, the sawtoothed grain beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Biol. Control 2001, 21, 300–304. [Google Scholar] [CrossRef] [Green Version]
- Aumeier, P. Bioassay for grooming effectiveness towards Varroa destructor mites in Africanized and Carniolan honey bees. Apidologie 2001, 32, 81–90. [Google Scholar] [CrossRef] [Green Version]
- Liu, L.; Zhao, X.-Y.; Tang, Q.-B.; Lei, C.-L.; Huang, Q.-Y. The mechanisms of social immunity against fungal infections in eusocial insects. Toxins 2019, 11, 244. [Google Scholar] [CrossRef] [Green Version]
- McConnaughey, M. Physical Chemical Properties of Fungi. In Reference Module in Biomedical Sciences; Elsevier: Amsterdam, The Netherlands, 2014; pp. 1–4. [Google Scholar] [CrossRef]
- Hillel, D. Encyclopedia of Soils in the Environment; Elsevier: Amsterdam, The Netherlands, 2004; Volume 4. [Google Scholar]
- Petersen, R.H.; Hughes, K.W. Species and speciation in mushrooms development of a species concept poses difficulties. Bioscience 1999, 49, 440–452. [Google Scholar] [CrossRef] [Green Version]
- Mora, M.A.E.; Castilho, A.M.C.; Fraga, M.E. Classification and infection mechanism of entomopathogenic fungi. Arq. Inst. Biológico 2018, 84, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Baron, N.C.; Rigobelo, E.C.; Zied, D.C.; Baron, N.C.; Rigobelo, E.C.; Zied, D.C. Filamentous fungi in biological control: Current status and future perspectives. Chil. J. Agric. Res. 2019, 79, 307–315. [Google Scholar] [CrossRef] [Green Version]
- Islam, W.; Adnan, M.; Shabbir, A.; Naveed, H.; Abubakar, Y.S.; Qasim, M.; Tayyab, M.; Noman, A.; Nisar, M.S.; Khan, K.A.; et al. Insect-fungal-interactions: A detailed review on entomopathogenic fungi pathogenicity to combat insect pests. Microb. Pathog. 2021, 159, 105122. [Google Scholar] [CrossRef] [PubMed]
- Roberts, D.W. Toxins of entomopathogenic fungi. In Microbial Control of Pests and Plant Disease; Academic Press: Cambridge, MA, USA, 1981. [Google Scholar]
- Zimmermann, G. Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci. Technol. 2007, 17, 879–920. [Google Scholar] [CrossRef]
- Goettel, M.S.; Hajek, A.E.; Siegel, J.P.; Evans, H.C. Safety of fungal biocontrol agents. In Fungi as Biocontrol Agents: Progress, Problems and Potential; CABI: Wallingford, UK, 2009. [Google Scholar]
- Goettel, M.S.; Eilenberg, J.; Glare, T. Entomopathogenic Fungi and their Role in Regulation of Insect Populations. In Comprehensive Molecular Insect Science; Elsevier: Amsterdam, The Netherlands, 2005; Volume 6. [Google Scholar]
- Ortiz-Urquiza, A.; Keyhani, N.O. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects 2013, 4, 357–374. [Google Scholar] [CrossRef] [PubMed]
- Zacharuk, R.Y. Penetration of the cuticular layers of elaterid larvae (Coleoptera) by the fungus Metarrhizium anisopliae, and notes on a bacterial invasion. J. Invertebr. Pathol. 1973, 21, 101–106. [Google Scholar] [CrossRef]
- Boucias, D.G.; Pendland, J.C. Attachment of mycopathogens to cuticle: The initial event of mycoses in arthropod hosts. In The Fungal Spore and Disease Initiation in Plants and Animals; Spring: Berlin/Heidelberg, Germany, 1991. [Google Scholar]
- Samuels, R.I.; Paterson, I.C. Cuticle degrading proteases from insect moulting fluid and culture filtrates of entomopathogenic fungi. Comp. Biochem. Physiol. Part B Biochem. 1995, 110, 661–669. [Google Scholar] [CrossRef]
- de Carolina Sánchez-Pérez, L.; Barranco-Florido, J.E.; Rodríguez-Navarro, S.; Cervantes-Mayagoitia, J.F.; Ramos-López, M.Á. Enzymes of Entomopathogenic Fungi, Advances and Insights. Adv. Enzym. Res. 2014, 2, 46652. [Google Scholar] [CrossRef] [Green Version]
- Liaud, N.; Giniés, C.; Navarro, D.; Fabre, N.; Crapart, S.; Herpoël-Gimbert, I.; Levasseur, A.; Raouche, S.; Sigoillot, J.-C. Exploring fungal biodiversity: Organic acid production by 66 strains of filamentous fungi. Fungal Biol. Biotechnol. 2014, 1, 1. [Google Scholar] [CrossRef] [Green Version]
- Hepburn, H.R. Structure of the Integument. In Integument, Respiration and Circulation; Elsevier: Amsterdam, The Netherlands, 1985. [Google Scholar]
- St. Leger, R.J. The role of cuticle-degrading proteases in fungal pathogenesis of insects. Can. J. Bot. 1995, 73 (Suppl. S1), 1119–1125. [Google Scholar] [CrossRef]
- Hajek, A.E.; St Leger, R.J. Interactions between fungal pathogens and insect hosts. Annu. Rev. Entomol. 1994, 39, 293–322. [Google Scholar] [CrossRef]
- Vega, F.E.; Posada, F.; Aime, M.C.; Pava-Ripoll, M.; Infante, F.; Rehner, S.A. Entomopathogenic fungal endophytes. Biol. Control 2008, 46, 72–82. [Google Scholar] [CrossRef] [Green Version]
- Cito, A.; Barzanti, G.P.; Strangi, A.; Francardi, V.; Zanfini, A.; Dreassi, E. Cuticle-degrading proteases and toxins as virulence markers of Beauveria bassiana (Balsamo) Vuillemin. J. Basic Microbiol. 2016, 56, 941–948. [Google Scholar] [CrossRef] [PubMed]
- Vey, A.; Hoagland, R.E.; Butt, T.M. Toxic metabolites of fungal biocontrol agents. In Fungi as Biocontrol Agents: Progress, Problems and Potential; CABI: Wallingford, UK, 2009. [Google Scholar]
- Bradfisch, G.A.; Harmer, S.L. ω-Conotoxin GVIA and nifedipine inhibit the depolarizing action of the fungal metabolite, destruxin B on muscle from the tobacco budworm (Heliothis virescens). Toxicon 1990, 28, 1249–1254. [Google Scholar] [CrossRef]
- Charnley, A.K. Fungal pathogens of insects: Cuticle degrading enzymes and toxins. Adv. Bot. Res. 2003, 40, 241–321. [Google Scholar]
- Pedrini, N.; Crespo, R.; Juárez, M.P. Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comp. Biochem. Physiol.-C Toxicol. Pharmacol. 2007, 146, 124–137. [Google Scholar] [CrossRef] [PubMed]
- Sosa-Gomez, D.R.; Boucias, D.G.; Nation, J.L. Attachment of Metarhizium anisopliae to the southern green stink bug Nezara viridula cuticle and fungistatic effect of cuticular lipids and aldehydes. J. Invertebr. Pathol. 1997, 69, 31–39. [Google Scholar] [CrossRef]
- Altinok, H.H.; Altinok, M.A.; Koca, A.S. Modes of action of entomopathogenic fungi. Curr. Trends Nat. Sci. 2019, 8, 117–124. [Google Scholar]
- Lu, H.L.; Leger, R.J.S. Insect Immunity to entomopathogenic fungi. Adv. Genet. 2016, 94, 251–285. [Google Scholar] [CrossRef]
- Lemaitre, B.; Hoffmann, J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25, 697–743. [Google Scholar] [CrossRef] [Green Version]
- Williams, M.J. Drosophila hemopoiesis and cellular immunity. J. Immunol. 2007, 178, 4711–4716. [Google Scholar] [CrossRef] [Green Version]
- González-Santoyo, I.; Córdoba-Aguilar, A. Phenoloxidase: A key component of the insect immune system. Entomol. Exp. Appl. 2012, 142, 1–16. [Google Scholar] [CrossRef]
- Tang, H. Regulation and function of the melanization reaction in Drosophila. Fly 2009, 3, 105–111. [Google Scholar] [CrossRef]
- Nappi, A.J.; Vass, E.; Frey, F.; Carton, Y. Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur. J. Cell Biol. 1995, 68, 450–456. [Google Scholar]
- Nappi, A.J.; Ottaviani, E. Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 2000, 22, 469–480. [Google Scholar] [CrossRef]
- Ganesan, S.; Aggarwal, K.; Paquette, N.; Silverman, N. Nf-κB/Rel proteins and the humoral immune responses of Drosophila melanogaster. Curr. Top. Microbiol. Immunol. 2011, 349, 25–60. [Google Scholar] [CrossRef] [PubMed]
- Haine, E.R.; Moret, Y.; Siva-Jothy, M.T.; Rolff, J. Antimicrobial defense and persistent infection in insects. Science 2008, 322, 1257–1259. [Google Scholar] [CrossRef] [PubMed]
- Meister, M.; Hetru, C.; Hoffmann, J.A. The antimicrobial host defense of Drosophila. Curr. Top. Microbiol. Immunol. 2000, 248, 17–36. [Google Scholar] [PubMed]
- Fehlbaum, P.; Bulet, P.; Michaut, L.; Lagueux, M.; Broekaert, W.F.; Hetru, C.; Hoffmann, J.A. Insect immunity: Septic injury of Drosophila induces the synthesis of a potent antifungal peptide with sequence homology to plant antifungal peptides. J. Biol. Chem. 1994, 269, 33159–33163. [Google Scholar] [CrossRef]
- Il’iasov, R.A.; Gaǐfullina, L.R.; Saltykova, E.S.; Poskriakov, A.V.; Nikolenko, A.G. Defensins in the honeybee antinfectious protection. Zh. Evol. Biokhim. Fiziol. 2012, 48, 425–432. [Google Scholar]
- Girardin, S.E.; Philpott, D.J. Mini review: The role of peptidoglycan recognition in innate immunity. Eur. J. Immunol. 2004, 34, 1777–1782. [Google Scholar] [CrossRef]
- Leulier, F.; Parquet, C.; Pili-Floury, S.; Ryu, J.H.; Caroff, M.; Lee, W.J.; Mengin-Lecreulx, D.; Lemaitre, B. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat. Immunol. 2003, 4, 478–484. [Google Scholar] [CrossRef]
- Carruthers, R.I.; Larkin, T.S.; Firstencel, H. Influence of thermal ecology on the mycosis of a rangeland grasshopper. Ecology 1992, 73, 190–204. [Google Scholar] [CrossRef]
- Jiang, H.; Vilcinskas, A.; Kanost, M.R. Immunity in lepidopteran insects. Adv. Exp. Med. Biol. 2010, 708, 181–204. [Google Scholar] [CrossRef]
- Hou, R.F.; Chang, J.K. Cellular Defense Response to Beauveria Bassiana in the Silkworm, Bombyx mori. Appl. Entomol. Zool. 1985, 20, 118–125. [Google Scholar] [CrossRef] [Green Version]
- Hung, S.Y.; Boucias, D.G.; Vey, A.J. Effect of Beauveria bassiana and Candida albicans on the cellular defense response of Spodoptera exigua. J. Invertebr. Pathol. 1993, 61, 179–187. [Google Scholar] [CrossRef]
- Butt, T.M.; Hajek, A.E.; Humber, R.A. Gypsy moth immune defenses in response to hyphal bodies and natural protoplasts of entomophthoralean fungi. J. Invertebr. Pathol. 1996, 68, 278–285. [Google Scholar] [CrossRef]
- Tuininga, A.R.; Miller, J.L.; Morath, S.U.; Daniels, T.J.; Falco, R.C.; Marchese, M.; Sahabi, S.; Rosa, D.; Stafford, K.C. Isolation of entomopathogenic fungi from soils and Ixodes scapularis (Acari: Ixodidae) ticks: Prevalence and methods. J. Med. Entomol. 2009, 46, 557–565. [Google Scholar] [CrossRef] [Green Version]
- Goettel, M.S.; Douglas Inglis, G. Fungi: Hyphomycetes. Manual of Techniques in Insect Pathology; Elsevier: Amsterdam, The Netherlands, 1997. [Google Scholar]
- Muniz, E.R.; Ribeiro-Silva, C.S.; Arruda, W.; Keyhani, N.O.; Fernandes, E.K.K. The Msn2 transcription factor regulates acaricidal virulence in the fungal pathogen Beauveria bassiana. Front. Cell. Infect. Microbiol. 2021, 11, 604. [Google Scholar] [CrossRef]
- Briggs, L.L.; Colwell, D.D.; Wall, R. Control of the cattle louse Bovicola bovis with the fungal pathogen Metarhizium anisopliae. Vet. Parasitol. 2006, 142, 344–349. [Google Scholar] [CrossRef]
- Hamiduzzaman, M.M.; Sinia, A.; Guzman-Novoa, E.; Goodwin, P.H. Entomopathogenic fungi as potential biocontrol agents of the ecto-parasitic mite, Varroa destructor, and their effect on the immune response of honey bees (Apis mellifera L.). J. Invertebr. Pathol. 2012, 111, 237–243. [Google Scholar] [CrossRef]
- Peng, C.Y.S.; Zhou, X.; Kaya, H.K. Virulence and site of infection of the fungus, Hirsutella thompsonii, to the honey bee ectoparasitic mite, Varroa destructor. J. Invertebr. Pathol. 2002, 81, 185–195. [Google Scholar] [CrossRef]
- García-Fernández, P.; Santiago-Álvarez, C.; Quesada-Moraga, E. 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 2008, 39, 662–673. [Google Scholar] [CrossRef]
- Luxton, M. Principles of acarology. By Gwilym O. Evans. Wallingford, Oxon: CAB International, 1992. Bull. Entomol. Res. 1992, 84, 142–143. [Google Scholar] [CrossRef]
- Gerritsen, L.; Cornelissen, B. Biological control of Varroa destructor by fungi. Proc. Netherlands Entomol. Soc. Meet. 2006, 17, 125–132. [Google Scholar]
- Kanga, L.H.B.; James, R.R.; Boucias, D.G. Hirsutella thompsonii and Metarhizium anisopliae as potential microbial control agents of Varroa destructor, a honey bee parasite. J. Invertebr. Pathol. 2002, 81, 175–184. [Google Scholar] [CrossRef]
- Poinar, G.; Poinar, R. Parasites and pathogens of mites. Annu. Rev. Entomol. 1998, 43, 449–469. [Google Scholar] [CrossRef]
- Zhioua, E.; Browning, M.; Johnson, P.W.; Ginsberg, H.S.; LeBrun, R.A. Pathogenicity of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) to Ixodes scapularis (Acari: Ixodidae). J. Parasitol. 1997, 83, 815–818. [Google Scholar] [CrossRef]
- Zhioua, E.; Ginsberg, H.S.; Humber, R.A.; Lebrun, R.A. Preliminary survey for entomopathogenic fungi associated with Ixodes scapularis (Acari: Ixodidae) in southern New York and New England, USA. J. Med. Entomol. 1999, 36, 635–637. [Google Scholar] [CrossRef]
- Frazzon, A.P.G.; Vaz Junior, I.D.S.; Masuda, A.; Schrank, A.; Vainstein, M.H. In vitro assessment of Metarhizium anisopliae isolates to control the cattle tick Boophilus microplus. Vet. Parasitol. 2000, 94, 117–125. [Google Scholar] [CrossRef]
- Davidson, G.; Phelps, K.; Sunderland, K.D.; Pell, J.K.; Ball, B.V.; Shaw, K.E.; Chandler, D. 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. 2003, 94, 816–825. [Google Scholar] [CrossRef] [Green Version]
- Rodríguez, M.; Gerding, M.; France, A. Selection of entomopathogenic fungi to control Varroa destructor (Acari: Varroidae). Chil. J. Agric. Res. 2009, 69, 534–540. [Google Scholar] [CrossRef] [Green Version]
- Shaw, K.E.; Davidson, G.; Clark, S.J.; Ball, B.V.; Pell, J.K.; Chandler, D.; Sunderland, K.D. Laboratory bioassays to assess the pathogenicity of mitosporic fungi to Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of the honeybee, Apis mellifera. Biol. Control 2002, 24, 266–276. [Google Scholar] [CrossRef]
- James, R.R.; Hayes, G.; Leland, J.E. Field trials on the microbial control of varroa with the fungus Metarhizium anisopliae. Am. Bee J. 2006, 146, 968–972. [Google Scholar]
- James, R.R.; Hayes, G. Microbial control of Varroa: Misadventures in the field. J. Anhui Agric. Univ. 2007, 32, 162–166. [Google Scholar]
- Meikle, W.G.; Mercadier, G.; Holst, N.; Nansen, C.; Girod, V. Impact of a treatment of Beauveria bassiana (Deuteromycota: Hyphomycetes) on honeybee (Apis mellifera) colony health and on Varroa destructor mites (Acari: Varroidae). Apidologie 2008, 39, 247–259. [Google Scholar] [CrossRef]
- Meikle, W.G.; Mercadier, G.; Holst, N.; Girod, V. 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. 2008, 46, 105–117. [Google Scholar] [CrossRef]
- Meikle, W.G.; Mercadier, G.; Holst, N.; Nansen, C.; Girod, V. Duration and spread of an entomopathogenic fungus, Beauveria bassiana (Deuteromycota: Hyphomycetes), used to treat Varroa mites (Acari: Varroidae) in honey bee (Hymenoptera: Apidae) hives. J. Econ. Entomol. 2007, 100, 1–10. [Google Scholar] [CrossRef]
- Walstad, J.D.; Anderson, R.F.; Stambaugh, W.J. Effects of environmental conditions on two species of muscardine fungi (Beauveria bassiana and Metarrhizium anisopliae). J. Invertebr. Pathol. 1970, 16, 221–226. [Google Scholar] [CrossRef]
- Hywel-Jones, N.L.; Gillespie, A.T. Effect of temperature on spore germination in Metarhizium anisopliae and Beauveria bassiana. Mycol. Res. 1990, 94, 389–392. [Google Scholar] [CrossRef]
- James, R.R.; Croft, B.A.; Shaffer, B.T.; Lighthart, B. Impact of temperature and humidity on host-pathogen interactions between Beauveria bassiana and a Coccinellid. Environ. Entomol. 1998, 27, 1506–1513. [Google Scholar] [CrossRef] [Green Version]
- Meikle, W.G.; Sammataro, D.; Neumann, P.; Pflugfelder, J. Challenges for developing pathogen-based biopesticides against Varroa destructor (Mesostigmata: Varroidae). Apidologie 2012, 43, 501–514. [Google Scholar] [CrossRef] [Green Version]
- Steenberg, T.; Kryger, P.; Holst, N. A scientific note on the fungus Beauveria bassiana infecting Varroa destructor in worker brood cells in honey bee hives. Apidologie 2010, 41, 127–128. [Google Scholar] [CrossRef]
- Rodríguez, M.; Gerding, M.; France, A.; Ceballos, R. Evaluation of Metarhizium anisopliae var. anisopliae Qu-M845 isolate to control Varroa destructor (Acari: Varroidae) In laboratory and field trials. Chil. J. Agric. Res. 2009, 69, 541–547. [Google Scholar] [CrossRef]
- Sinia, A.; Guzman-Novoa, E. Evaluation of the entomopathogenic fungi Beauveria bassiana GHA and Metarhizium anisopliae UAMH 9198 alone or in combination with thymol for the control of Varroa destructor in honey bee (Apis mellifera) colonies. J. Apic. Res. 2018, 57, 308–312. [Google Scholar] [CrossRef]
- Lodesani, M.; Costa, C.; Franceschetti, S.; Bergomi, P.; Galaverna, G.; Dall’Asta, C. Toxicity of destruxins against the parasitic mite Varroa destructor and its host Apis mellifera. J. Apic. Res. 2017, 56, 278–287. [Google Scholar] [CrossRef]
- Han, J.O.; Naeger, N.L.; Hopkins, B.K.; Sumerlin, D.; Stamets, P.E.; Carris, L.M.; Sheppard, W.S. Directed evolution of Metarhizium fungus improves its biocontrol efficacy against Varroa mites in honey bee colonies. Sci. Rep. 2021, 11, 10582. [Google Scholar] [CrossRef] [PubMed]
- Alves, S.B.; Marchini, L.C.; Pereira, R.M.; Baumgratz, L.L. Effects of some insect pathogens on the Africanized honey bee, Apis mellifera L. (Hym., Apidae). J. Appl. Entomol. 1996, 120, 559–564. [Google Scholar] [CrossRef]
- Ahmed, A.A.; Abd-Elhady, H.K. Efficacy of two fungus-based biopesticide against the honeybee ectoparasitic mite, Varroa destructor. Pakistan J. Biol. Sci. 2013, 16, 819–825. [Google Scholar] [CrossRef] [Green Version]
- Kanga, L.H.B.; Adamczyk, J.; Patt, J.; Gracia, C.; Cascino, J. 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. 2010, 52, 327–342. [Google Scholar] [CrossRef]
- Voigt, K.; Rademacher, E. Effect of the propolis components, cinnamic acid and pinocembrin, on Apis mellifera and Ascosphaera apis. J. Apic. Sci. 2015, 59, 89–95. [Google Scholar] [CrossRef] [Green Version]
- Wilson, M.B.; Brinkman, D.; Spivak, M.; Gardner, G.; Cohen, J.D. Regional variation in composition and antimicrobial activity of US propolis against Paenibacillus larvae and Ascosphaera apis. J. Invertebr. Pathol. 2015, 124, 44–50. [Google Scholar] [CrossRef]
- Niu, G.; Johnson, R.M.; Berenbaum, M.R. Toxicity of mycotoxins to honeybees and its amelioration by propolis. Apidologie 2011, 42, 79–87. [Google Scholar] [CrossRef] [Green Version]
- Cappa, F.; Petrocelli, I.; Dani, F.R.; Dapporto, L.; Giovannini, M.; Silva-Castellari, J.; Turillazzi, S.; Cervo, R. Natural biocide disrupts nestmate recognition in honeybees. Sci. Rep. 2019, 9, 3171. [Google Scholar] [CrossRef] [Green Version]
- Jaime, E.A.; Josefina, M.; Francisco, Z. Behavior of nursing Apis mellifera after application of entomopathogenic fungi to control Varroa destructor. African J. Agric. Res. 2019, 14, 2075–2080. [Google Scholar] [CrossRef]
- Omuse, E.R.; Niassy, S.; Wagacha, J.M.; Ong’amo, G.O.; Michael, H.; Lattorff, G.; Kiatoko, N.; Mohamed, S.A.; Subramanian, S.; Akutse, K.S.; et al. Susceptibility of the Western Honey Bee Apis mellifera and the African Stingless Bee Meliponula ferruginea (Hymenoptera: Apidae) to the Entomopathogenic Fungi Metarhizium anisopliae and Beauveria bassiana. J. Econ. Entomol. 2021, 2021, 3171. [Google Scholar] [CrossRef] [PubMed]
- Vega, F.E.; Dowd, P.F.; Bartelt, R.J. Dissemination of microbial agents using an autoinoculating device and several insect species as vectors. Biol. Control 1995, 5, 545–552. [Google Scholar] [CrossRef]
- Ellis, J.D.; Neumann, P.; Hepburn, R.; Elzen, P.J. Longevity and reproductive success of Aethina tumida (Coleoptera: Nitidulidae) fed different natural diets. J. Econ. Entomol. 2002, 95, 902–907. [Google Scholar] [CrossRef]
- Lundie, A.E. The Small Hive Beetle, Aethina túmida. Sci. Bull. Dep. Agric. For. Union S. Africa 1940, 220, 1–30. [Google Scholar]
- Ellis, J.D.; Rong, I.H.; Hill, M.P.; Hepburn, H.R.; Elzen, P.J. The susceptibility of small hive beetle (Aethina tumida Murray) pupae to fungal pathogens. Am. Bee J. 2004, 144, 486–488. [Google Scholar]
- Richards, C.S.; Hill, M.P.; Dames, J.F. The susceptibility of small hive beetle (Aethina tumida Murray) pupae to Aspergillus niger (van Tieghem) and A. flavus (Link:Grey). Am. Bee J. 2005, 145, 748–751. [Google Scholar]
- Cuthbertson, A.G.S.; Wakefield, M.E.; Powell, M.E.; Marris, G.; Anderson, H.; Budge, G.E.; Mathers, J.J.; Blackburn, L.F.; Brown, M.A. The small hive beetle Aethina tumida. Sci. Bull. 2013, 59, 13. [Google Scholar]
- Mürrle, T.; Neumann, P. Mass production of small hive beetles (Aethina tumida, Coleoptera: Nitidulidae). J. Apic. Res. 2004, 43, 144–145. [Google Scholar] [CrossRef]
- Muerrle, T.M.; Neumann, P.; Dames, J.F.; Hepburn, H.R.; Hill, M.P. Susceptibility of Adult Aethina tumida (Coleoptera: Nitidulidae) to Entomopathogenic Fungi. J. Econ. Entomol. 2006, 99, 1–6. [Google Scholar] [CrossRef]
- Leemon, D.M.; McMahon, J. Feasibility Study into In-Hive Fungal Bio-Control of Small Hive Beetle. Report for the Rural Industries Research and Development Corporation Publication no. 09/090. 2009. Available online: http://era.daf.qld.gov.au/id/eprint/2405/ (accessed on 24 December 2021).
- Ibrahim, S.A.M.; Salem, H.H.A.; Taha, M.A. Dual application of entomopathogenic nematodes and fungi on immune and antioxidant enzymes of the greater wax moth, Galleria mellonella L. Egypt. J. Biol. Pest Control 2019, 29, 20. [Google Scholar] [CrossRef] [Green Version]
- Fergani, Y.A.; Yehia, R.S. Isolation, molecular characterization of indigenous Beauveria bassiana isolate, using ITS-5.8 s rDNA region and its efficacy against the greatest wax moth, Galleria mellonella L. (Lepidoptera: Pyralidae) as a model insect. Egypt. J. Biol. Pest Control 2020, 30, 96. [Google Scholar] [CrossRef]
- El-Ghany AT, M.; El-Sheikh, H.H.; El-Rahman AG, A.; El-Nasser, A. Biodiversity of entomopathogenic fungi in new cultivated soil with their using to control of. Int. J. Resaerch Rev. 2012, 4, 17–31. [Google Scholar]
- Harris, R.J.; Harcourt, S.J.; Glare, T.R.; Rose, E.A.F.; Nelson, T.J. Susceptibility of Vespula vulgaris (Hymenoptera: Vespidae) to generalist entomopathogenic fungi and their potential for wasp control. J. Invertebr. Pathol. 2000, 75, 251–258. [Google Scholar] [CrossRef]
- Haxaire, J.; Tamisier, J.-P.; Bouguet, J.-P. Vespa velutina Lepeletier, 1836, une redoutable nouveauté pour la faune de France (Hym., Vespidae). Bull. la Société Entomol. Fr. 2006, 111, 194. [Google Scholar] [CrossRef]
- Merino, L.; France, A.; Gerding, M. Selection of native fungi strains pathogenic to Vespula germanica (Hymenoptera: Vespidae). Agric. Tec. 2007, 67, 335–342. [Google Scholar] [CrossRef]
- Brownbridge, M.; Toft, R.; Rees, J.; Nelson, T.L.; Bunt, C. Towards better mitigation technologies for invasive wasps Vespula spp. New Zeal. Plant Prot. 2009, 62, 395. [Google Scholar] [CrossRef]
- Poidatz, J.; López Plantey, R.; Thiéry, D. Indigenous strains of Beauveria and Metharizium as potential biological control agents against the invasive hornet Vespa velutina. J. Invertebr. Pathol. 2018, 153, 180–185. [Google Scholar] [CrossRef] [Green Version]
- Poidatz, J.; Lopez Plantey, R.J.; Thiéry, D. A Beauveria bassiana strain naturally parasitizing the bee predator Vespa Velutina in France. Entomol. Gen. 2019, 39, 73–79. [Google Scholar] [CrossRef]
- Abou-Shaara, H.F.; Owayss, A.A.; Ibrahim, Y.Y.; Basuny, N.K. A review of impacts of temperature and relative humidity on various activities of honey bees. Insectes Soc. 2017, 64, 455–463. [Google Scholar] [CrossRef]
- Stabentheiner, A.; Pressl, H.; Papst, T.; Hrassnigg, N.; Crailsheim, K. Endothermic heat production in honeybee winter clusters. J. Exp. Biol. 2003, 206, 353–358. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fahrenholz, L.; Lamprecht, I.; Schricker, B. Thermal investigations of a honey bee colony: Thermoregulation of the hive during summer and winter and heat production of members of different bee castes. J. Comp. Physiol. B 1989, 159, 551–560. [Google Scholar] [CrossRef]
- Calovi, M.; Grozinger, C.M.; Miller, D.A.; Goslee, S.C. Summer weather conditions influence winter survival of honey bees (Apis mellifera) in the northeastern United States. Sci. Rep. 2021, 11, 1553. [Google Scholar] [CrossRef]
- Ouedraogo, A.; Fargues, J.; Goettel, M.S.; Lomer, C.J. Effect of temperature on vegetative growth among isolates of Metarhizium anisopliae and M. flavoviride. Mycopathologia 1997, 137, 37–43. [Google Scholar] [CrossRef]
- Guzmán-Franco, A.W.; Clark, S.J.; Alderson, P.G.; Pell, J.K. Effect of temperature on the in vitro radial growth of Zoophthora radicans and Pandora blunckii, two co-occurring fungal pathogens of the diamondback moth Plutella xylostella. BioControl 2008, 53, 501–516. [Google Scholar] [CrossRef]
- Cabanillas, H.E.; Jones, W.A. Effects of temperature and culture media on vegetative growth of an entomopathogenic fungus Isaria sp. (Hypocreales: Clavicipitaceae) naturally affecting the whitefly, bemisia tabaci in Texas. Mycopathologia 2009, 167, 263–271. [Google Scholar] [CrossRef]
- Kikankie, C.K.; Brooke, B.D.; Knols, B.G.; Koekemoer, L.L.; Farenhorst, M.; Hunt, R.H.; Thomas, M.B.; Coetzee, M. The infectivity of the entomopathogenic fungus Beauveria bassiana to insecticide-resistant and susceptible Anopheles arabiensis mosquitoes at two different temperatures. Malar. J. 2010, 9, 71. [Google Scholar] [CrossRef] [Green Version]
- Evans, B.G.; Jordan, K.S.; Brownbridge, M.; Hallett, R.H. Effect of temperature and host life stage on efficacy of soil entomopathogens against the swede midge (Diptera: Cecidomyiidae). J. Econ. Entomol. 2015, 108, 473–483. [Google Scholar] [CrossRef]
- Bouamama, N.; Vidal, C.; Fargues, J. Effects of fluctuating moisture and temperature regimes on the persistence of quiescent conidia of Isaria fumosorosea. J. Invertebr. Pathol. 2010, 105, 139–144. [Google Scholar] [CrossRef] [PubMed]
- Smits, N.; Brière, J.F.; Fargues, J. Comparison of non-linear temperature-dependent development rate models applied to in vitro growth of entomopathogenic fungi. Mycol. Res. 2003, 107, 1476–1484. [Google Scholar] [CrossRef] [PubMed]
- Kramm, K.R.; West, D.F.; Rockenbach, P.G. Termite pathogens: Transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes sp. termites. J. Invertebr. Pathol. 1982, 40, 1–6. [Google Scholar] [CrossRef]
- Kim, J.S.; Je, Y.H.; Choi, J.Y. Complementary effect of Phloxine B on the insecticidal efficacy of Isaria fumosorosea SFP-198 wettable powder against greenhouse whitefly, Trialeurodes vaporariorum West. Pest Manag. Sci. 2010, 66, 1337–1343. [Google Scholar] [CrossRef]
- Burges, H.D. Formulation of Mycoinsecticides. In Formulation of Microbial Biopesticides; Springer Science & Business Media: Berlin/Heidelberg, Germany, 1998. [Google Scholar]
- Kim, J.S.; Je, Y.H.; Woo, E.O.; Park, J.S. Persistence of Isaria fumosorosea (Hypocreales: Cordycipitaceae) SFP-198 Conidia in Corn Oil-Based Suspension. Mycopathologia 2011, 171, 67–75. [Google Scholar] [CrossRef] [PubMed]
- Chantawannakul, P.; de Guzman, L.I.; Li, J.; Williams, G.R. Parasites, pathogens, and pests of honeybees in Asia. Apidologie 2016, 47, 301–324. [Google Scholar] [CrossRef]
- De La Rúa, P.; Jaffé, R.; Dall’Olio, R.; Muñoz, I.; Serrano, J. Biodiversity, conservation and current threats to European honeybees. Apidologie 2009, 40, 263–284. [Google Scholar] [CrossRef] [Green Version]
- Carreck, N.; Neumann, P. Honey bee colony losses. J. Apic. Res. 2010, 49, 1–6. [Google Scholar]
- Lozano, A.; Hernando, M.D.; Uclés, S.; Hakme, E.; Fernández-Alba, A.R. Identification and measurement of veterinary drug residues in beehive products. Food Chem. 2019, 274, 61–70. [Google Scholar] [CrossRef]
- Hernández-Rodríguez, C.S.; Marín, Ó.; Calatayud, F.; Mahiques, M.J.; Mompó, A.; Segura, I.; Simó, E.; González-Cabrera, J. Large-Scale Monitoring of Resistance to Coumaphos, Amitraz, and Pyrethroids in Varroa destructor. Insects 2021, 12, 27. [Google Scholar] [CrossRef]
- Klátyik, S.; Bohus, P.; Darvas, B.; Székács, A. Authorization and toxicity of veterinary drugs and plant protection products: Residues of the active ingredients in food and feed and toxicity problems related to adjuvants. Front. Vet. Sci. 2017, 4, 146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bernardes, M.F.F.; Pazin, M.; Pereira, L.C.; Dorta, D.J. Impact of pesticides on environmental and human health. In Toxicology Studies-Cells, Drugs and Environment; BoD–Books on Demand: Norderstedt, Germany, 2015. [Google Scholar]
- Semalulu, S.S.; MacPherson, J.M.; Schiefer, H.B.; Khachatourians, G.G. Pathogenicity of Beauveria bassiana in Mice. J. Vet. Med. Ser. B 1992, 39, 81–90. [Google Scholar] [CrossRef] [PubMed]
- Zimmermann, G. Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci. Technol. 2007, 17, 553–596. [Google Scholar] [CrossRef]
- Weng, Q.; Zhang, X.; Chen, W.; Hu, Q. Secondary metabolites and the risks of Isaria fumosorosea and Isaria farinosa. Molecules 2019, 24, 664. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ebani, V.V.; Mancianti, F. Entomopathogenic fungi and bacteria in a veterinary perspective. Biology 2021, 10, 479. [Google Scholar] [CrossRef]
- Maggi, M.D.; Damiani, N.; Ruffinengo, S.R.; Brasesco, M.C.; Szawarski, N.; Mitton, G.; Mariani, F.; Sammataro, D.; Quintana, S.; Eguaras, M.J. The susceptibility of Varroa destructor against oxalic acid: A study case. Bull. Insectol. 2017, 70, 39–44. [Google Scholar]
- Pietropaoli, M.; Formato, G. Formic acid combined with oxalic acid to boost the acaricide efficacy against Varroa destructor in Apis mellifera. J. Apic. Res. 2021, 26, 1–9. [Google Scholar] [CrossRef]
- Bava, R.; Castagna, F.; Piras, C.; Palma, E.; Cringoli, G.; Musolino, V.; Lupia, C.; Perri, M.R.; Statti, G.; Britti, D.; et al. In vitro evaluation of acute toxicity of five Citrus spp. Essential oils towards the parasitic mite Varroa destructor. Pathogens 2021, 10, 1182. [Google Scholar] [CrossRef]
- Conti, B.; Bocchino, R.; Cosci, F.; Ascrizzi, R.; Flamini, G.; Bedini, S. Essential oils against Varroa destructor: A soft way to fight the parasitic mite of Apis mellifera. J. Apic. Res. 2020, 59, 774–782. [Google Scholar] [CrossRef]
- Sinha, K.K.; Choudhary, A.K.; Kumari, P. Entomopathogenic Fungi. In Ecofriendly Pest Management for Food Security; Omkar, B.T., Ed.; Academic Press: Cambridge, MA, USA, 2016; pp. 475–505. [Google Scholar] [CrossRef]
- Sharma, H.C. Biotechnological Approaches for Pest Management and Ecological Sustainability; CRC Press: Boca Raton, FL, USA, 2008. [Google Scholar]
- Winder, R.S.; Wheeler, J.J.; Conder, N.; Otvos, I.S.; Nevill, R.; Duan, L. Microencapsulation: A strategy for formulation of inoculum. Biocontrol Sci. Technol. 2003, 13, 155–169. [Google Scholar] [CrossRef]
EPF Species | Formulation Type | Application Method | Reference |
---|---|---|---|
Beauveria bassiana, Hirsutella spp., Metarhizium spp., Paecilomyces spp., Tolypocladium spp., Verticillium lecanii | Spore solution | Immersion for a few seconds | Shaw et al. [90] |
Hirsutella thompsonii, Metarhizium anisopliae | Liquid | Sprayed frames | Kanga et al., 2002 [83] |
Hirsutella thompsonii (laboratory test) | Fungal culture | Walk for a few minutes | Peng et al., 2002 [79] |
Metarhizium anisopliae Metarhizium anisopliae | Powder Liquid | Dusted between frames/strips between frames Sprayed frames | Kanga et al., 2003 [91] James et al., 2006 [110] |
Metarhizium anisopliae Lecanicillium lecanii | Liquid | Sprayed frames | Gerritsen% Cornelissen [82] |
Beauveria bassiana | Powder | Blown between frames | Meikle et al., 2007 [100] |
Beauveria bassiana | Powder/Flour/carnauba wax powder | Blown between frames | Meikle et al., 2007 [95] |
Lecanicillium lecanii, Beauveria bassiana, Metarhizium anisopliae, Hirsutella kirchneri, Hirsutella nodulosa (laboratory test) | Fungal culture | Walk for a few minutes | Fernandez et al., 2008 [80] |
Metarhizium anisopliae | Powder/Liquid | Filter paper between frames/sprinkled between frames/dispenser path hive entrance | Rodriguez et al., 2009 [103] |
Beauveria bassiana and Metarhizium anisopliae | Powder Dispenser tray | Sinia & Guzman-Novoa, 2018 [104] | |
Metarhizium anisopliae/Beauveria bassiana/ Clonostachys rosea (laboratory test) | Spore solution | Immersion for a few seconds | Hamiduzzaman et al., 2012 [78] |
Metarhiziumanisopliae, Beauvaria bassiana | Commercial preparation suspended in water | Sprayed frames | Abdelaal & Hany, 2013 [108] |
Destruxins (laboratory test) | Crude and purified destruxins | Lodesani et al., 2017 [105] | |
Metarhizium brunneum | 120 g of colonized grain bearing 2.63 × 108 spores per gram. | Han et al., 2021 [106] |
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Bava, R.; Castagna, F.; Piras, C.; Musolino, V.; Lupia, C.; Palma, E.; Britti, D.; Musella, V. Entomopathogenic Fungi for Pests and Predators Control in Beekeeping. Vet. Sci. 2022, 9, 95. https://doi.org/10.3390/vetsci9020095
Bava R, Castagna F, Piras C, Musolino V, Lupia C, Palma E, Britti D, Musella V. Entomopathogenic Fungi for Pests and Predators Control in Beekeeping. Veterinary Sciences. 2022; 9(2):95. https://doi.org/10.3390/vetsci9020095
Chicago/Turabian StyleBava, Roberto, Fabio Castagna, Cristian Piras, Vincenzo Musolino, Carmine Lupia, Ernesto Palma, Domenico Britti, and Vincenzo Musella. 2022. "Entomopathogenic Fungi for Pests and Predators Control in Beekeeping" Veterinary Sciences 9, no. 2: 95. https://doi.org/10.3390/vetsci9020095