318
Views
8
CrossRef citations to date
0
Altmetric
Pathology and parasitology

Do Beauveria bassiana and Metarhizium anisopliae affect worker survival and the production of Africanized Apis mellifera queens?

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 260-269 | Received 05 Jun 2020, Accepted 15 Sep 2020, Published online: 14 Oct 2020

References

  • Ahmed, A. A., & Abd-Elhady, H. K. (2013). Efficacy of two fungus-based biopesticide against the honeybee ectoparasitic mite, Varroa destructor . Pakistan Journal of Biological Sciences : PJBS, 16(16), 819–825. https://doi.org/10.3923/pjbs.2013.819.825
  • Akyol, E., Yeninar, H., Kaftanoglu, O., & Ag, A. (2008). Live weight of queen honey bees (Apis mellifera L.) predicts reproductive characteristics. Journal of the Kansas Entomological Society, 81(2), 92–100. https://doi.org/10.2317/JKES-705.13.1
  • Al Mazra’awi, M. (2007). Impact of the entomopathogenic fungus Beauveria bassiana on the honey bees, Apis mellifera (Hymenoptera: Apidae). World Journal of Agricultural Sciences, 3, 7–11.
  • Al Mazra’awi, M. S., Shipp, J. L., Broadbent, A. B., & Kevan, P. G. (2006). Dissemination of Beauveria bassiana by honey bees (Hymenoptera: Apidae) for control of tarnished plant bug (Hemiptera: Miridae) on canola. Environmental Entomology, 35(6), 1569–1577. https://doi.org/10.1603/0046-225x(2006)35[1569:dobbbh]2.0.co;2
  • Alves, S. B. (1998). Controle microbiano de insetos (2nd ed.). FEALQ.
  • Alves, S. B., Marchini, L. C., Pereira, R. M., & Baumgratz, L. L. (1996). Effects of some insect pathogens on the Africanized honey bee, Apis mellifera L. (Hym., Apidae). Journal of Applied Entomology, 120(1–5), 559–564. https://doi.org/10.1111/j.1439-0418.1996.tb01652.x
  • Amiri, B., Ibrahim, L., & Butt, T. M. (1999). Antifeedant properties of destruxins and their potential use with the entomogenous fungus Metarhizium anisopliae for improved control of crucifer pests. Biocontrol Science and Technology, 9(4), 487–498. https://doi.org/10.1080/09583159929451
  • Annett, R., Habibi, H. R., & Hontela, A. (2014). Impact of glyphosate and glyphosate-based herbicides on the freshwater environment. Journal of Applied Toxicology: JAT, 34(5), 458–479. https://doi.org/10.1002/jat.2997
  • Baptista, A. P. M., Carvalho, G. A., Carvalho, S. M., Carvalho, C. F., & Bueno Filho, J. S. S. (2009). Toxicidade de produtos fitossanitários utilizados em citros para Apis mellifera. Ciência Rural, 39(4), 955–961. https://doi.org/10.1590/S0103-84782009005000049
  • Bienefeld, K., Ehrhardt, K., & Reinhardt, F. (2007). Genetic evaluation in the honey bee considering queen and worker effects – A BLUP-Animal Model approach. Apidologie, 38(1), 77–85. https://doi.org/10.1051/apido:2006050
  • Brighenti, D. M., Carvalho, C. F., Carvalho, G. A., Brighenti, C. R. G., & Carvalho, S. M. (2007). Bioatividade do Bacillus thuringiensis var. kurstaki (Berliner, 1915) para adultos de Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae). Ciência e Agrotecnologia, 31(2), 279–289. https://doi.org/10.1590/S1413-70542007000200003
  • Carvalho, S. M., Carvalho, G. a., Carvalho, C. F., Bueno Filho, J. S. S., & Baptista, a P. M. (2009). Toxicidade De Acaricidas/Inseticidas Empregados Na Citricultura Para a Abelha Africanizada Apis mellifera L., 1758 (Hymenoptera : Apidae). Arquivos Do Instituto Biológico, São Paulo, 76(4), 597–606.
  • Catae, A. F., Menegasso, A. R., da, S., Pratavieira, M., Palma, M. S., Malaspina, O., & Roat, T. C. (2019). MALDI-imaging analyses of honeybee brains exposed to a neonicotinoid insecticide. Pest Management Science, 75(3), 607–615. https://doi.org/10.1002/ps.5226
  • Catae, A. F., Roat, T. C., Pratavieira, M., Menegasso, A. R., da, S., Palma, M. S., & Malaspina, O. (2018). Exposure to a sublethal concentration of imidacloprid and the side effects on target and nontarget organs of Apis mellifera. Ecotoxicology (London, England), 27(2), 109–113. https://doi.org/10.1007/s10646-017-1874-4
  • Costa, E. M., Araujo, E. L., Maia, A. V. P., Silva, F. E. L., Bezerra, C. E. S., & Silva, J. G. (2014). Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory conditions. Apidologie, 45(1), 34–44. https://doi.org/10.1007/s13592-013-0226-5
  • De Souza, D. A., Bezzera-Laure, M. A. F., Francoy, T. M., & Gonçalves, L. S. (2013). Experimental evaluation of the reproductive quality of Africanized queen bees (Apis mellifera) on the basis of body weight at emergence. Genetics and Molecular Research : GMR, 12(4), 5382–5391. https://doi.org/10.4238/2013.November.7.13
  • De Souza, D. A., Wang, Y., Kaftanoglu, O., De Jong, D., Amdam, G. V., Gonçalves, L. S., & Francoy, T. M. (2015). Morphometric identification of queens, workers, intermediates in in vitro reared honey bees (Apis mellifera). PLoS One, 10(4), e0123663. https://doi.org/10.1371/journal.pone.0123663
  • Ding, J., & Chi, D.-F. (2018). Ultrastructural observations of Beauveria bassiana infection in Xylotrechus rusticus larvae. Entomological Research, 48(3), 204–213. https://doi.org/10.1111/1748-5967
  • Doolitle, G. M. (1889). Scientific queen-rearing as practically applied (p. 168). Alpha Editions.
  • Facchini, E., Bijma, P., Pagnacco, G., Rizzi, R., & Brascamp, E. W. (2019). Hygienic behaviour in honeybees: A comparison of two recording methods and estimation of genetic parameters. Apidologie, 50(2), 163–172. https://doi.org/10.1007/s13592-018-0627-6
  • Faquinello, P., De Arnaut De Toledo, V. A., Martins, E. N., De Oliveira, C. A. L., Sereia, M. J., Costa-Maia, F. M., & Ruvolo-Takasusuki, M. C. C. (2011). Parameters for royal jelly production in Africanized honeybees. Sociobiology, 57(3), 495–510. https://doi.org/10.12795/spal.2002.i11.21
  • Farooqui, T. (2013). A potential link among biogenic amines-based pesticides, learning and memory, and colony collapse disorder : A unique hypothesis. Neurochemistry International, 62(1), 122–136. https://doi.org/10.1016/j.neuint.2012.09.020
  • Fell, R. D., & Morse, R. A. (1984). Emergency queen cell production in the honey bee colony. Insectes Sociaux, 31(3), 221–237. https://doi.org/10.1007/BF02223608
  • 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(6), 662–673. https://doi.org/10.1051/apido:2008049
  • Gupta, S., & Dikshit, A. K. (2010). Biopesticides: An ecofriendly approach for pest control. Journal of Biopesticides, 3(1), 186–188. https://doi.org/10.4172/2168-9881.S1.012
  • Hamiduzzaman, M. M., Sinia, A., Guzman-Novoa, E., & Goodwin, P. H. (2012). 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.). Journal of Invertebrate Pathology, 111(3), 237–243. https://doi.org/10.1016/j.jip.2012.09.001
  • Harrington, D. (2005). Linear rank tests in survival analysis. Encyclopedia of biostatistics. 1, 1–10. https://doi.org/10.1002/0470011815.b2a11047
  • Harrington, D. P., & Fleming, T. R. (1982). A class of rank test procedures for censored survival data. Biometrika, 69(3), 553–566. https://doi.org/10.1093/biomet/69.3.553
  • Howard, P. H., & Allen, P. (2010). Beyond organic and fair trade?An analysis of ecolabel preferences in the United States. Rural Sociology, 75(2), 244–269. https://doi.org/10.1111/j.1549-0831.2009.00009.x
  • James, R. R., McGuire, M. R., & Leland, J. E. (2012). Susceptibility of adult alfalfa leafcutting bees and honey bees to a microbial control agent, Beauveria bassiana. Southwestern Entomologist, 37(1), 13–21. https://doi.org/10.3958/059.037.0102
  • Johnson, R. A., & Wichern, D. W. (2007). Applied multivariate statistical analysis (6th ed.). Pearson Educational Inc.
  • 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. Experimental & Applied Acarology, 52(4), 327–342. https://doi.org/10.1007/s10493-010-9369-5
  • Kanga, L. H. B., Jones, W. A., & Gracia, C. (2006). Efficacy of strips coated with Metarhizium anisopliae for control of Varroa destructor (Acari: Varroidae) in honey bee colonies in Texas and Florida. Experimental & Applied Acarology, 40(3–4), 249–258. https://doi.org/10.1007/s10493-006-9033-2
  • Kanga, L. H. B., Jones, W., & 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. Journal of Economic Entomology, 96(4), 1091–1099. https://doi.org/10.1603/0022-0493-96.4.1091
  • Kurwadkar, S., & Evans, A. (2016). Neonicotinoids: Systemic insecticides and systematic failure. Bulletin of Environmental Contamination and Toxicology, 97(6), 745–748. https://doi.org/10.1007/s00128-016-1968-3
  • Leclercq, G., Francis, F., Gengler, N., & Blacquière, T. (2018). Bioassays to quantify hygienic behavior in honey bee (Apis mellifera L.) bioassays to quantify hygienic behavior in honey bee (Apis mellifera L.) colonies: A review. Journal of Apicultural Research, 57(5), 663–611. https://doi.org/10.1080/00218839.2018.1494916
  • Lodesani, M., Costa, C., Franceschetti, S., Bergomi, P., Galaverna, G., & Dall’Asta, C. (2017). Toxicity of destruxins against the parasitic mite Varroa destructor and its host Apis mellifera. Journal of Apicultural Research, 56(3), 278–287. https://doi.org/10.1080/00218839.2017.1304611
  • Lorencetti, G. A. T., Potrich, M., Mazaro, S. M., Lozano, E. R., Barbosa, L. R., Menezes, M. J. S., & Gonçalves, T. E. (2018). Eficiência de Beauveria bassiana Vuill. e Isaria sp para o controle de Thaumastocoris peregrinus Carpintero & Dellapé (Hemiptera: Thaumastocoridae). Ciência Florestal, 28(1), 403–411.
  • Mallebrera, B., Prosperini, A., Font, G., & Ruiz, M. J. (2018). In vitro mechanisms of Beauvericin toxicity : A review. Food and Chemical Toxicology : An International Journal Published for the British Industrial Biological Research Association, 111, 537–545. https://doi.org/10.1016/j.fct.2017.11.019
  • Mascarin, G. M., Lopes, R. B., Delalibera, Í., Fernandes, É. K. K., Luz, C., & Faria, M. (2019). Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil. Journal of Invertebrate Pathology, 165, 46–53. https://doi.org/10.1016/j.jip.2018.01.001
  • 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 (Acari: Varroidae) in honey bee (Hymenoptera: Apidae) hives. Journal of Economic Entomology, 100(1), 1–10. https://doi.org/10.1603/0022-0493(2007)100[1:DASOAE]2.0.CO;2
  • Meikle, W. G., Mercadier, G., Holst, N., Nansen, C., & Girod, V. (2008). Impact of a treatment of Beauveria bassiana (Deuteromycota: Hyphomycetes) on honeybee (Apis mellifera) colony health and on Varroa destructor mites (Acari: Varroidae). Apidologie, 39(2), 247–259. https://doi.org/10.1051/apido:2007057
  • Metorima, F. N., Costa-Maia, F. M., Halak, A. L., Parpinelli, R. S., & Toledo, V. d A. (2015). Morphometric measurements of Africanized honeybee queens kept in an incubator or in queen banking. Acta Scientiarum. Animal Sciences, 37(1), 91–96. https://doi.org/10.4025/actascianimsci.v37i1.24006
  • Oldroyd, B. P., Goodman, R. D., & Allaway, M. A. (1990). On the relative importance of queens and workers to honey production. Apidologie, 21(2), 153–159. https://doi.org/10.1051/apido:19900209
  • Pires, C. S. S., Pereira, F., de, M., Lopes, M. T., do, R., Nocelli, R. C. F., Malaspina, O., Pettis, J. S., & Teixeira, E. W. (2016). Enfraquecimento e perda de colônias de abelhas no Brasil: há casos de CCD? Pesquisa Agropecuária Brasileira, 51(5), 422–442. https://doi.org/10.1590/S0100-204X2016000500003
  • Portilla, M., Luttrell, R., Snodgrass, G., Zhu, C., & Riddick, E. (2017). Lethality of the Entomogenous Fungus Beauveria bassiana Strain NI8 on Lygus lineolaris (Hemiptera: Miridae) and its Possible Impact on Beneficial Arthropods. Journal of Entomological Science, 52(4), 352–369. https://doi.org/10.18474/JES17-15.1
  • Potrich, M., Silva, R. T. L. d., Maciel, R. M. A., Costa-Maia, F. M., Lozano, E. R., Rossi, R. M., Martins, J. R., & Dallacort, S. (2020). Are plant extracts safe for honey bees (Apis mellifera)? Journal of Apicultural Research, 59(5), 844–848. https://doi.org/10.1080/00218839.2020.1735733
  • Potrich, M., Silva, R. T. L d., Maia, F. M. C., Lozano, E. R., Rossi, R. M., Colombo, F. C., Tedesco, F. G., & Gouvea, A. d. (2018). Effect of entomopathogens on Africanized Apis mellifera L. (Hymenoptera: Apidae). Revista Brasileira de Entomologia, 62(1), 23–12. https://doi.org/10.1016/j.rbe.2017.12.002
  • Potts, S., Biesmeijer, K., Bommarco, R., Breeze, T., Carvalheiro, L., Franzen, M., Gonzalez-Varo, J. P., Holzschuh, A., Kleijn, D., Klein, A.-M., Kunin, B., Lecocq, T., Lundin, O., Michez, D., Neumann, P., Nieto, A., Penev, L., Rasmont, P., Ratamaki, O., … Schweiger, O. (2015). Status and trends of European pollinators - Key findings from the STEP project. Pensoft Publishers.
  • Qi, S., Niu, X., Wang, D. h., Wang, C., Zhu, L., Xue, X., Zhang, Z., & Wu, L. (2019). Flumethrin at sublethal concentrations induces stresses in adult honey bees (Apis mellifera L.). Science of the Total Environment, 664, 1–18. https://doi.org/10.1016/j.scitotenv.2019.134500
  • Qu, S., & Wang, S. (2018). Interaction of entomopathogenic fungi with the host immune system. Developmental and Comparative Immunology, 83, 96–103. https://doi.org/10.1016/j.dci.2018.01.010
  • Samuels, R. I., Reynolds, S. E., & Charnley, A. K. (1988). Calcium channel activation of insect muscle by destruxins, insecticidal compounds produced by the entomopathogenic fungus Metarhizium anisopliae. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 90(2), 403–412. https://doi.org/10.1016/0742-8413(88)90018-7
  • Sánchez-Bayo, F., Goulson, D., Pennacchio, F., Nazzi, F., Goka, K., & Desneux, N. (2016). Are bee diseases linked to pesticides? A brief review. Environment International, 89–90, 7–11. https://doi.org/10.1016/j.envint.2016.01.009
  • Santos, T. S., Freitas, A. C. d., Poderoso, J. C. M., Hernandez-Macedo, M. L., Ribeiro, G. T., da Costa, L. P., & Mendonça, M. d C. (2018). Evaluation of Isolates of Entomopathogenic Fungi in the Genera Metarhizium, Beauveria, and Isaria, and Their Virulence to Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). Florida Entomologist, 101(4), 597–602. https://doi.org/10.1653/024.101.0421
  • Tarpy, D., Hatch, S., & Fletcher, D. (2000). The influence of queen age and quality during queen replacement in honeybee colonies. Animal Behaviour, 59(1), 97–101. https://doi.org/10.1006/anbe.1999.1311
  • Thany, S. H., Bourdin, C. M., Graton, J., Laurent, A. D., Mathé-Allainmat, M., Lebreton, J., & Le Questel, J. Y. (2015). Similar comparative low and high doses of deltamethrin and acetamiprid differently impair the retrieval of the proboscis extension reflex in the forager honey bee (Apis mellifera). Insects, 6(4), 805–814. https://doi.org/10.3390/insects6040805
  • Tofilski, A., & Czekonska, K. (2004). Emergeny queen rearing in honeybee colonies with brood of known age. Apidologie, 35(3), 275–282. https://doi.org/10.1051/apido
  • Tomasetto, F., Tylianakis, J. M., Reale, M., Wratten, S., & Goldson, S. L. (2017). Intensified agriculture favors evolved resistance to biological control. Proceedings of the National Academy of Sciences of the United States of America, 114(15), 3885–3890. https://doi.org/10.1073/pnas.1618416114
  • Uchôa, F. D. A. B., Souza, D. C., Alves, A. A., Silva, F. A., Nunes, J. R. A., de Lima, C. J., & da Silva Sousa, J. (2012). Effect of weight of Africanized queens (Apis mellifera L.) at birth in honey production in semi-arid Piauiense. Agropecuária Científica No Semiárido, 8(1), 1–6.
  • Valero-Jiménez, C. A., Wiegers, H., Zwaan, B. J., Koenraadt, C. J. M., & Kan, J. A. L. V. (2016). Genes involved in virulence of the entomopathogenic fungus Beauveria bassiana. Journal of Invertebrate Pathology, 133, 41–49. https://doi.org/10.1016/j.jip.2015.11.011
  • van Engelsdorp, D., & Otis, G. W. (2000). Application of a modified selection index for honey bees (Hymenoptera: Apidae) application of a modified selection index for honey bees (Hymenoptera: Apidae). Journal of Economic Entomology, 93(6), 1606–1612. https://doi.org/10.1603/0022-0493-93.6.1606
  • Van Lenteren, J. C., Bolckmans, K., Köhl, J., Ravensberg, W. J., & Urbaneja, A. (2018). Biological control using invertebrates and microorganisms: Plenty of new opportunities. BioControl, 63(1), 39–59. https://doi.org/10.1007/s10526-017-9801-4
  • VanEngelsdorp, D., Traynor, K. S., Andree, M., Lichtenberg, E. M., Chen, Y., Saegerman, C., & Cox-Foster, D. L. (2017). Colony Collapse Disorder (CCD) and bee age impact honey bee pathophysiology. PLoS One, 12(7), e0179535. https://doi.org/10.1371/journal.pone.0179535
  • Wang, C., & Leger, R. J. S. (2007). The MAD1 Adhesin of Metarhizium anisopliae Links Adhesion with Blastospore Production and Virulence to Insects, and the MAD2 Adhesin Enables Attachment to Plants. Eukaryotic Cell, 6(5), 808–816. https://doi.org/10.1128/EC.00409-06
  • Woyke, J. (1971). Correlations between the age at which honeybee brood was grafted, characteristics of the resultant queens, and results of insemination. Journal of Apicultural Research, 10(1), 45–55. https://doi.org/10.1080/00218839.1971.11099669
  • Yu, Q., & Powles, S. (2014). Metabolism-based herbicide resistance and cross-resistance in crop weeds: A threat to herbicide sustainability and global crop production. Plant Physiology, 166(3), 1106–1118. https://doi.org/10.1104/pp.114.242750

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.