Occurrence and distribution of the microsporidium Vairimorpha (Nosema) spp. in apiaries in Brazil - Systematic review

Authors

DOI:

https://doi.org/10.33448/rsd-v13i11.47482

Keywords:

Bees; Apiculture; Microsporidia; Nosemosis; Beekeeping health.

Abstract

Nosemosis is one of the main diseases of bees, caused by microsporidia of the genus Vairimorpha (Nosema). The main etiologic agents are Vairimorpha apis and Vairimorpha ceranae. These pathogens are widely distributed around the world, and in Brazil, they have already been reported in some states, but these data have never been gathered in a review. The objective of this study was to perform a systematic review of the occurrence and distribution of the microsporidium Vairimorpha spp. in apiaries in Brazil. The search was done in the SciELO, PubMed, DOAJ, and Capes Journals (Scopus) databases. 14 articles were selected and published in English and Portuguese. In the included publications, only eight Brazilian states were referred (Bahia, Espírito Santo, Goiás, Minas Gerais, Piauí, Rio Grande do Sul, Santa Catarina, and São Paulo). No work was conducted in the northern of the country, and most of the publications are concentrated in the southern and southeastern. Regarding the Vairimorpha species, only V. apis and V. ceranae were investigated, and V. ceranae was predominantly detected. Most of the studies were done only with the Africanized bee Apis mellifera. This review showed which Brazilian regions have never been explored in terms of incidence and distribution of these pathogens, revealing a gap to be filled by the country's beekeeping surveillance and health systems. In addition, because of the great Brazilian biodiversity, it is evident that the occurrence and distribution of these pathogens also need to be investigated with other bee species.

References

Baena-Díaz, F.; Chévez, E.; Merced, F. R. & Porter-Bolland, L. (2022). Apis mellifera in Mexico: honey production, melliferous flora and pollination aspects. Review. Revista Mexicana de Ciências Pecuárias, 13(2), 1-24.

Bizotto, L. A.; Santos, R. S. S. & Boff, M. I. C. (2018). Parasitism by Varroa and Nosema sp. in beehives used for apple tree pollination. Revista Caatinga, 31(3), 773-778.

Braglia, C.; Daniele, A.; Garrido, P. M.; Porrini, M. P.; Baffoni,L.; Scott, D.; Eguaras, M. J.; Di Gioia, D. & Mifsud, D. (2024). Vairimorpha (Nosema) ceranae can promote Serratia development in honeybee gut: an underrated threat for bees? Frontiers in Cellular and Infection Microbiology, 14(1), 1-11.

Castelli, L.; Branchiccela, B.; Garrido, M.; et al. (2020). Impact of Nutritional Stress on Honeybee Gut Microbiota, Immunity, and Nosema ceranae Infection. Invertebrate Microbiology, 80(4), 908-919.

Chagas, D. B.; Monteiro, F .L.; Barcelos, L. S.; Frühauf, M. I.; Ribeiro, L. C.; Lima, M.; Hübner, S. O. & Fischer, G. (2020). Black queen cell virus and Nosema ceranae coinfection in Africanized honey bees from southern Brazil. Pesquisa Veterinária Brasileira, 40(11), 892-897.

Dias, A .C.; Ferreira, J. T.; Teixeira, E. W. & Lourenço, A. P. (2024). Honey bee viruses in solitary bees in South America: simultaneous detection and prevalence. Journal of Apicultural Research, 63(1), 122-127.

Faita, M. R.; Cardozo, M. M.; Amandio, D. T. T.; Orth, A. I. & Nodari, R. O. (2020). Glyphosate-based herbicides and Nosema sp. microsporidia reduce honey bee (Apis mellifera L.) survivability under laboratory conditions. Journal of Apicultural Research, 59(4), 332-342.

Fernández, J. M.; Puerta, F.; Cousinou, M.; Dios-Palomares, R.; Campano, F. & Redondo, L. (2012). Asymptomatic presence of Nosema sp. in Spanish commercial apiaries. Journal of Invertebrate Pathology, 111(2), 106-110.

Frazier, M.; Muli, E. & Patch, H. (2024). Ecology and Management of African Honey Bees (Apis mellifera L.). Annual Review of Entomology, 69, 439-453.

Freitas, C. D.; Oki, Y.; Resende, F. M.; Zamudio, F.; Freitas, S.G., Rezende, K. M. & Fernandes, G. W. (2023). Impacts of pests and diseases on the decline of managed bees in Brazil: a beekeeper perspective. Journal of Apicultural Research, 62(5), 969-982.

Fries, I.; Chauzat, M. P.; Chen, Y. P.; Doublet, V.; Genersch, E.; Gisder, S.; & Williams, G. R. (2013). Standard methods for Nosema research. Journal of Apicultural Research, 52(1), 1-28.

Georgi, I.; Didaras, N. A.; Nikolaidis, M.; Dimitriou, T. G.; Charistos, L.; Hatjina, F.; Amoutzias, G. D. & Mossialos, D. (2022). The Impact of Vairimorpha (Nosema) ceranae Natural Infection on Honey Bee (Apis mellifera) and Bee Bread Microbiota. Applied Sciences, 12(22), 1-12.

Gomes, I. S. & Caminha, I. O. (2014). Guia para estudos de revisão sistemática: uma opção metodológica para as Ciências do Movimento Humano. Movimento. 20(1), 395-411. Autores, coloquem em itálico o nome da revista "Movimento".

Guimarães-Cestaro, L.; Alves, M. L. T. M. F.; Message, D.; Silva, M. V. G. B. & Teixeira, E. W. (2017). Honey Bee (Apis mellifera) Health in Stationary and Migratory Apiaries. Sociobiology, 64(1), 42-49.

Guimarães-Cestaro, L.; Maia, T.S.; Martins, R.; Alves, M. L. T. M. F.; Otsuk, I. P.; Message, D. & Teixeira, E. W. (2020). Nosema ceranae (Microsporidia: Nosematidae) Does Not Cause Collapse of Colonies of Africanized Apis mellifera (Hymenoptera: Apidae) in Tropical Climate. Sociobiology, 67(3), 408-416, 2020.

IBGE - Instituto Brasileiro de Geografia e Estatística. (2022). Produção de mel de abelha. https://www.ibge.gov.br/explica/producao-agropecuaria/mel-de-abelha/br

Khalifa, S. A. M.; Elshafiey, E. H.; Shetaia, A. A.; et al. (2021). Overview of Bee Pollination and Its Economic Value for Crop Production. Insects, 12(8), 1-23.

Klee, J.; Besana, A. M.; Genersch, E.; et al. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96(1), 1-10.

Lage, V. M. G. B.; Santana, C. D.; Patrocínio, E.; Noronha, R. P.; Melo, R. L.; Barbosa, C. J. & Lima S. T. C. (2022). Prevalence of Nosema ceranae in apiculture regions of Bahia State, Brazil. Ciência Rural, 52(9), e20210473.

Manlik, O.; Mundra, S.; Schmid-Hempel, R. & Schmid-Hempel, P. (2022). Impact of climate change on parasite infection of an important pollinator depends on host genotypes. Global Change Biology, 29(1), 69-80.

Martínez, J.; Leal, G. & Conget, P. (2012). Nosema ceranae an emergent pathogen of Apis mellifera in Chile. Parasitology Research, 111(2), 601–607.

Mazur, E. D. & Gajda, A. M. (2022). Nosemosis in Honeybees: A Review Guide on Biology and Diagnostic Methods. Applied Sciences, 12(12), 1-14.

Nascimento, J. J. S.; Ferreira, M. B. S.; Melquíades, C .C. V. & Bendini, J. N. (2022). Infestation levels of Varroa destructor and Nosema spp. in africanized bee (Apis mellifera) colonies during the dry season in the semiarid region of Piauí state. Acta Veterinaria Brasilica, 16(1), 78-83.

Neves, V. S. L.; Peixoto, C. M.; Sodré, G. S. & Carvalho, C. A. L. (2023). Identificação molecular e nível de infecção de Vairimorpha ceranae em Apis mellifera (Hymenoptera: Apidae). Scientia Plena, 19(9), 090201.

Nikita; Grover, A.; Kalia, P.; Sinha, R. & Garg, P. (2022). Colony collapse disorder: A peril to apiculture. Journal of Applied and Natural Science, 14(3), 729-739.

Nunes-Silva, P.; Piot, N.; Meeus, I.; Blochtein, B. & Smagghe, G. (2016). Absence of Leishmaniinae and Nosematidae in stingless bees. Scientific Reports, 6, 32547.

Pacini, A.; Molineri, A.; Antúnez, K.; et al. (2021). Environmental conditions and beekeeping practices associated with Nosema ceranae presence in Argentina. Apidologie, 52, 400-417.

Parrella, P.; Elikan, A. B. & Snow, J. W. (2024). Pathogen- and host-directed pharmacologic strategies for control of Vairimorpha (Nosema) spp. infection in honey bees. The Journal of Eukaryotic Microbiology, 71(5), e13026.

Pires, C. S. S.; Pereira, F. M.; Lopes, M. T. 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.

Porrini, M. P.; Porrini, L .P.; Garrido, P. M.; Silva Neto, C. M.; Porrini, D. P.; Muller, F.; Nuñez, L. A.; Alvarez, L.; Iriarte, P. F. & Eguaras, M. J. (2017). Nosema ceranae in South American Native Stingless Bees and Social Wasp. Microbial Ecology, 74, 761-764.

Sabolová, B.; Kandrácová, P. & Sucik, M. (2024). Stress Factors Affecting the Development of Vairimorpha (Nosema) spp. Disease in Bee Colonies. Preprints, 2024080118.

Santos, L. G.; Alves, M. L. T. M. F.; Message, D.; Pinto, F. A.; Silva, M. V. G. B. & Teixeira, E .W. (2014). Honey Bee Health in Apiaries in the Vale do Paraíba, São Paulo State, Southeastern Brazil. Sociobiology, 61(3), 307-312.

Silveira, F. A.; Melo, G. A. R. & Almeida, E. A. B. (2002). Abelhas brasileiras Sistemática e identificação. Fundação Araucária.

Spiesman, B .J.; Gratton, C.; Gratton, E. & Hines, H. (2024). Deep learning for identifying bee species from images of wings and pinned specimens. Plos One, 19(5), e0303383.

Teixeira, E. W.; Santos, L. G.; Sattler, A.; Message, D.; Alves, M. L. T. M. F.; Martins, M. F.; Grassi-Sella, M. L. & Francoy, T. M. (2013). Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. Journal of Invertebrate Pathology, 114(3), 250-254.

Teixeira, E. W.; Guimarães-Cestaro, L.; Alves, M. L. T. M. F.; Message, D.; Martins, M. F.; Luz, C. F. P. & Serrão, J. E. (2018). Spores of Paenibacillus larvae, Ascosphaera apis, Nosema ceranae and Nosema apis in bee products supervised by the Brazilian Federal Inspection Service. Revista Brasileira de Entomologia, 62(3), 188-194.

Teixeira, E. W.; Ferreira, E. A.; Luz, C. F. P.; Martins, M. F.; Ramos, T. A. & Lourenço, A. P. (2020). European Foulbrood in stingless bees (Apidae: Meliponini) in Brazil: Old disease, renewed threat. Journal of Invertebrate Pathology, 172, 107357.

Tokarev, Y. S.; Huang, W-F.; Solter, L. F.; Malysh, J. M.; Becnel, J. J. & Vossbrinck, C. R. (2020). A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. Journal of Invertebrate Pathology, 169, 107279.

Truong, A-T.; Sevin, S.; Kim, S.; Yoo, M. S.; Cho, Y. S. & Yoon, B. (2021). Rapidly quantitative detection of Nosema ceranae in honeybees using ultra-rapid real-time quantitative PCR. Journal of Veterinary Science, 22(3), e40.

Webster, V. L.; Hemmings, S.; Pérez, M.; Fisher, M. C.; Brown, M. J. F. & Farrer, R. A. (2024). Revealing the genome of the microsporidian Vairimorpha bombi, a potential driver of bumble bee declines in North America. G3: Gene, Genomes, Genetics, 14(4), 1-8.

Zhang, Y.; Su, M.; Wang, L.; Huang, S.; Su, S. & Huang, W-F. (2021). Vairimorpha (Nosema) ceranae Infection Alters Honey Bee Microbiota Composition and Sustains the Survival of Adult Honey Bees. Biology, 10(9), 1-14.

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Published

19/11/2024

How to Cite

LAGE, V. M. G. B. .; SANTANA, C. D. .; NORONHA, R. P. .; BARBOSA, C. de J. .; LIMA, S. T. da C. . Occurrence and distribution of the microsporidium Vairimorpha (Nosema) spp. in apiaries in Brazil - Systematic review. Research, Society and Development, [S. l.], v. 13, n. 11, p. e123131147482, 2024. DOI: 10.33448/rsd-v13i11.47482. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/47482. Acesso em: 26 nov. 2024.

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Review Article