La relevancia de evaluar los efectos adversos potenciales de los biopesticidas en las abejas
DOI:
https://doi.org/10.33240/rba.v20i3.57874Palabras clave:
agentes de control biológico, polinizadores, evaluación de riesgos, organismos no alvoResumen
El uso de bioinsumos en las actividades agrícolas en Brasil está aumentando, como los “agentes de control biológico” (Ley nº 15.070/2024), también llamados pesticidas biológicos o biopesticidas. Aunque se utilizan indiscriminadamente, se sabe poco acerca de sus posibles riesgos para organismos no objetivo. Así, el objetivo del trabajo fue investigar datos relacionados con el comercio de biopesticidas, reguladores de crecimiento y microbiológicos, entre otros; sus fabricantes, los efectos sobre las abejas de los biopesticidas ya registrados; y la relevancia de la evaluación de los potenciales efectos adversos sobre las abejas. Estudios ya realizados indican la existencia de riesgos por los biopesticidas para los polinizadores y los ecosistemas. De esta investigación se desprenden dos necesidades: la primera es el desarrollo urgente evaluar y ampliar normas legales que establezcan y regulen la evaluación de riesgos de los biopesticidas; La segunda es la cautela en el uso de biopesticidas, particularmente en la producción orgánica y agroecológica, hasta que se evalúen sus riesgos.
Referencias
Agência Nacional de Vigilância Sanitária (ANVISA). Monografias autorizadas: lista em ordem alfabética. Brasília, DF: ANVISA, 2025b. Disponível em: https://www.gov.br/anvisa/pt-br/setorregulado/regularizacao/agrotoxicos/monografias/monografias-autorizadas-por-letra. Acesso em 14 fev. 2025.
______. Monografias de agrotóxicos. Brasília, DF: ANVISA, 2025a. Disponível em: https://www.gov.br/anvisa/pt-br/acessoainformacao/dadosabertos/informacoes-analiticas/monografias-de-agrotoxicos. Acesso em 14 fev. 2025.
AGROFIT. Ministério da Agricultura e Pecuária (MAPA). Consulta aberta. Brasília, DF: MAPA, c2024. Disponível em: https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Acesso em: 02 jan. 2025.
ALKASSAB, Abdulrahim et al. Exposure of honey bees to mixtures of microbial biopesticides and their effects on bee survival under laboratory conditions. Environmental Science and Pollution Research, v. 31, p. 26618–26627, 2024. Doi: 10.1007/s11356-024-32753-9.
ALMEIDA, Felipe et al. Side effects of a fungus-based biopesticide on stingless bee guarding behaviour. Chemosphere, v. 287 (Pt 2), e132147, 2022. Doi: 10.1016/j.chemosphere.2021.132147.
ANTUNES, Sara C.; CASTRO, Bruno B. Pulgas-de-água (Daphnia spp.). Revista de Ciência Elementar, v. 5, n. 4, e050, 2017. Doi: 10.24927/rce2017.050.
AUGUSTO, Lia et al. (Org.). Dossiê danos dos agrotóxicos na saúde reprodutiva: conhecer e agir em defesa da vida. Rio de Janeiro: ABRASCO/ENSP, 2024. 200p.
AYILARA, Modupe S. et al. Biopesticides as a promising alternative to synthetic pesticides: A case for microbial pesticides, phytopesticides, and nanobiopesticides. Frontiers in Microbiology, v. 14, e1040901, 2023. Doi: 10.3389/fmicb.2023.1040901
BARBOSA, Wagner et al. Biopesticide-induced behavioral and morphological alterations in the stingless bee Melipona quadrifasciata. Environmental Toxicology and Chemistry, v. 34, n. 9, p. 2149-2158, 2015. Doi: 10.1002/etc.3053.
BERNARDES, Rodrigo et al. The reduced-risk insecticide azadirachtin poses a toxicological hazard to stingless bee Partamona helleri (Friese, 1900) queens. Chemosphere, v. 201, p. 550-556, 2018. Doi: 10.1016/j.chemosphere.2018.03.030.
BRASIL. Lei Nº 15.070, de 23 de dezembro de 2024. Disponível em: https://www.planalto.gov.br/ccivil_03/_ato2023-2026/2024/Lei/L15070.htm#art40. Acesso em: 30 dez. 2024.
BROCK, Ryan E.; CINI, Alessandro; SUMNER, Seirian. Ecosystem services provided by aculeate wasps. Biological Reviews. 96, 1645–1675. 2021. Doi: 10.1111/brv.12719.
CAPPA, Federico; BARACCHI, David; CERVO, Rita. Biopesticides and insect pollinators: Detrimental effects, outdated guidelines, and future directions, Science of The Total Environment, v. 837, e155714, 2022. Doi: 10.1016/j.scitotenv.2022.155714.
CAPPA, Federico et al. Adverse effects of the fungal biopesticide Beauveria bassiana on a predatory social wasp, Science of The Total Environment, v. 908, e168202, 2024. Doi: 10.1016/j.scitotenv.2023.168202.
CAPPA, Federido et al. Natural biocide disrupts nestmate recognition in honeybees. Scientific Reports, v. 9, n. 1, e3171, 2019. Doi: 10.1038/s41598-019-38963-3.
CARLESSO, Daniele et al. Exposure to a biopesticide interferes with sucrose responsiveness and learning in honey bees. Scientific Reports, v. 10, n. 1, e19929, 2020. Doi: 10.1038/s41598-020-76852-2.
CHALLA, Giriah K.; FIRAKE, Dnyaneshwar M.; BEHERE, Genesh T. Bio-pesticide applications may impair the pollination services and survival of foragers of honey bee, Apis cerana Fabricius in oilseed brassica. Environmental Pollution, v. 249, p. 598-609, 2019. Doi: 10.1016/j.envpol.2019.03.048.
CHAVES, Adriana; FAITA, Marcia R.; NODARI, Rubens O. Effects of fungicides on the ultrastructure of the hypopharyngeal glands and the strength of the hives of Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae). Toxicology and Applied Pharmacology, v. 459, e116340, 2023. Doi: 10.1016/j.taap.2022.116340.
CHRISTEN, Verena, et al. Biopesticide spinosad induces transcriptional alterations in genes associated with energy production in honey bees (Apis mellifera) at sublethal concentrations. Journal of Hazardous Materials, v. 378, e120736, 2019. DOI:10.1016/j.jhazmat.2019.06.013
CUNNINGHAM, Margan M. et al. Honey bees as biomonitors of environmental contaminants, pathogens, and climate change. Ecological Indicators, 134, 108457, 2022. Doi:10.1016/j.ecolind.2021.108457.
DEMIROZER, Ozan; UZUN, Asye; GOSTERIT, Ayhan. Lethal and sublethal effects of different biopesticides on Bombus terrestris (Hymenoptera: Apidae). Apidologie, 53, 24, 2022. Doi: 10.1007/s13592-022-00933-6.
ENGEL, Michael S. et al. Stingless bee classification and biology (Hymenoptera, Apidae): a review, with an updated key to genera and subgenera. Zookeys, 1172:239-312, 2023. Doi: 10.3897/zookeys.1172.104944.
FAITA, Marcia R.; CHAVES, Adriana; NODARI, Rubens O. The expansion of agribusiness: harmful impacts of deforestation, pesticides and transgenics on bees. Desenvolvimento e Meio Ambiente, v.57, p.79-105, 2021. Doi: 10.5380/dma.v56i0.76157.
FAITA, Marcia R.; PEREIRA, Erick; POLTRONIERI, Alex S. Effect of entomopathogenic fungus-formulated bioinsecticides on stingless bees (Hymenoptera: Apidae: Meliponini) in the laboratory. Journal of Apicultural Research, v. 63, n. 5, p. 924–931, 2024.
GIANNINI, Tereza C. et al. Crop pollinators in Brazil: a review of reported interactions. Apidologie, v. 46, n. 2, p. 209-223, 2015. Doi: 10.1007/s13592-014-0316-z.
GOMES, Ingrid N. et al. Honeybee survival and flight capacity are compromised by insecticides used for controlling melon pests in Brazil. Ecotoxicology, v. 29, n. 1, p. 97-107, 2020. Doi: 10.1007/s10646-019-02145-8.
HADDI, Khalid et al. Rethinking biorational insecticides for pest management: unintended effects and consequences. Pest Management Science, v. 76, n. 7, p. 2286-2293, 2020. Doi: 10.1002/ps.5837.
HESS, Sonia C.; Nodari, Rubens O.; LOPES-FERREIRA Monica. Agrotóxicos: críticas à regulação que permite o envenenamento do país. Desenvolvimento e Meio Ambiente (UFPR), v. 57, p. 106-134, 2021. Doi: 10.5380/dma.v57i0.76169
Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA). Relatórios de comercialização de agrotóxicos. Brasília: IBAMA, c2024. Disponível em: https://www.gov.br/ibama/pt-br/assuntos/quimicos-e-biologicos/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos. Acesso em 14 fev. 2025.
Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO). Portaria nº 665, de 3 de novembro de 2021. ICMbio institui catálogo nacional de abelhas nativas sem ferrão. p. 1-2, 2021, Disponível em: https://jusdecisum.com.br/icmbio-institui-catalogo-nacional-de-abelhas-nativas-sem-ferrao/. Acesso em: 14 fev. 2025.
KLEIN, Alexandra-Maria et al. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, v. 274, n. 1608, p.303-313, 2007. Doi: 10.1098/rspb.2006.3721.
LEITE, Mariana O. G. et al. Laboratory risk assessment of three entomopathogenic fungi used for pest control toward social bee pollinators. Microorganisms, v. 10, n. 9, e.1800, 2022. Doi: 10.3390/microorganisms10091800.
MARANHO, L. A. et al. Testing the Neem Biopesticide (Azadirachta indica A. Juss) for Acute Toxicity with Danio rerio and for Chronic Toxicity with Daphnia magna. JAST, v. 16, n. 1. P. 105-111, 2014. Disponível em: http://jast.modares.ac.ir/article-23-6440-en.html. Acesso em: 14 fev. 2025.
MICHENER, Charles D. The bees of the world. Baltimore: Johns Hopkins University Press, 2007. 953p.
MOMMAERTS, Veerle et al. A laboratory evaluation to determine the compatibility of microbiological control agents with the pollinator Bombus terrestris. Pest Management Science, v. 65, n. 9, p. 949-955, 2009. Doi: 10.1002/ps.1778.
MORITZ, Robin F. A.; FUCHS, Stefan. Organization of honeybee colonies: characteristics and consequences of a superorganism concept. Apidologie, v. 29, n. 1-2, p. 7-21, 1998. Doi: 10.1051/apido:19980101.
MOURE, Jesus S., URBAN, Danúncia; MELO, Gabriel A. R. (Orgs). (2008). Catálogo de Abelhas (Hymenoptera, Apoidea) na Região Neotropical - versão online. Disponível em https://moure.cria.org.br/catalogue. Acesso em: 24/05/2025.
NODARI, Rubens O.; HESS, Sonia C. A pulverização aérea de agrotóxicos desordenada em cinco microrregiões com altas taxas de mortalidade por neoplasias e suicídio, Estado de São Paulo, Brasil. Ciencia Digna, v. 3, p. 39-52, 2023.
NOVAIS, Samuel M. et al. Effects of a possible pollinator crisis on food crop production in Brazil. Plos One, v. 11, n. 11, p. e0167292, 2016. Doi: 10.1371/journal.pone.0167292.
Organisation for Economic Co-operation and Development (OECD). OECD guidelines for the testing of chemicals section 2: Effects on biotic systems test No 213 test. Honeybees. Acute oral toxicity test. Paris, France: Organization for Economic Cooperation and Development. 1998a. Acesso em: 14 fev. 2025.
______. OECD guidelines for the testing of chemicals section 2: Effects on biotic systems test No 214 test. Honeybees. Acute contact toxicity test. Paris, France: Organization for Economic Cooperation and Development, 1998b. Acesso em: 14 fev. 2025.
______. OECD guidelines for the testing of chemicals section 2: Effects on biotic systems test No 237 test. Honey Bee (Apis Mellifera) Larval Toxicity Test, Single Exposure. Paris, France: Organization for Economic Cooperation and Development, 2013. Acesso em: 14 fev. 2025.
______. OECD guidelines for the testing of chemicals section 2: Effects on biotic systems test No 245 test. Honey Bee (Apis mellifera L.), Chronic Oral Toxicity Test (10-Day Feeding). Paris, France: Organization for Economic Cooperation and Development. 2017. Acesso em: 14 fev. 2025.
OMUSE, Evanson R. 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. Journal of Economic Entomology, v. 115, n. 1, p. 46-55, 2022. Doi: 10.1093/jee/toab211.
Organização das Nações Unidas para a Alimentação e Agricultura (FAO). Guidelines for the registration of microbial, botanical and semiochemical pest control agents for plant protection and public health uses. Genebra: WHO, 2017. 86p.
POTTS, Simon G. et al. Global pollinator declines: trends, impacts and drivers. Trends In Ecology & Evolution, v. 25, n. 6, p. 345-353, 2010. Doi: 10.1016/j.tree.2010.01.007.
POTTS, Simon G.; IMPERATRIZ-FONSECA, Vera; NGO, Hien T. (eds). Intergovernamental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES). The assessment report on pollinators, pollination and food production. Bonn: Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, 2016. 552p. Disponível em: https://ipbes.net/sites/default/files/downloads/pdf/individual_chapters_pollination_20170305.pdf. Acesso em: 14 fev. 2025.
QIU, Yi-Lei et al. Application of indigenous honeybees in dispersing Trichoderma harzianum spores for control of the strawberry grey mould. Biocontrol Science and Technology, v. 31, n. 4, p. 418-429, 2021. Doi: 10.1080/09583157.2020.1865269
RAMANAIDU, Krilen; CUTLER, G. Christopher. Different toxic and hormetic responses of Bombus impatiens to Beauveria bassiana, Bacillus subtilis and spirotetramat. Pest Management Science, v. 69, n. 8, p. 949-954, 2013. Doi: 10.1002/ps.3456.
RODGER, James G. et al. Widespread vulnerability of flowering plant seed production to pollinator declines. Science Advances, v. 7, n. 42, p. 15, 2021. Doi:10.1126/sciadv.abd3524.
ROSA, Annelise S. et al. The stingless bee species, Scaptotrigona aff. depilis, as a potential indicator of environmental pesticide contamination. Environmental Toxicology and Chemistry, v. 34, n. 8, p. 1851-1853, 2015. Doi: 10.1002/etc.2998.
ROUBIK, David W. Feral African Bees Augment Neotropical Coffee Yield. In KEVAN, Peter G.; IMPERATRIZ-FONSECA, Vera L. (Eds.), POLLINATING BEES - THE CONSERVATION LINK BETWEEN AGRICULTURE AND NATURE. Proceedings of the Workshop on the Conservation and Sustainable Use of Pollinators in Agriculture, with an Emphasis on Bees, 2019, São Paulo. Brasília: Ministério do Meio Ambiente, 2022, p.255-266.
SANTOS, Sircio A. Impacto de um biopesticida na sobrevivência, perfil químico cuticular e reconhecimento social na abelha Scaptotrigona aff. depilis (Hymenoptera, Apidae, Meliponini). 2023. Dissertação (Mestrado) – Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, 2023. Disponível em: https://www.teses.usp.br/teses/disponiveis/59/59131/tde-03072023-135726/. Acesso em: 31 dez. 2024.
SABO, Ratislav et al. Sublethal effects of commercial plant protection product containing spores Bacillus amyloliquefaciens QST 713 (formerly subtilis) on winter adult honeybees. Apidologie, v. 51, p. 226-239, 2020. Doi: 10.1007/s13592-019-00705-9.
SHAFIR, Sharoni et al. Honey bee dispersal of the biocontrol agent Trichoderma harzianum T39: effectiveness in suppressing Botrytis cinerea on strawberry under field conditions. European Journal of Plant Pathology, 116, 119–128, 2006. Doi: 10.1007/s10658-006-9047-y.
SIVITER, Harry et al. Wild bees are exposed to low levels of pesticides in urban grasslands and community gardens. Science of The Total Environment, v. 858, e159839, 2023. doi: 10.1016/j.scitotenv.2022.159839.
STEINIGEWEG, Charlotte et al. Assessment of the impacts of microbial plant protection products containing Bacillus thuringiensis on the survival of adults and larvae of the honeybee (Apis mellifera). Environmental Science and Pollution Research, v. 28, n. 23, p. 29773-29780, 2021. Doi: 10.1007/s11356-021-12446-3.
______. Impact of a microbial pest control product containing Bacillus thuringiensis on brood development and gut microbiota of Apis mellifera worker honey bees. Microbial Ecology, v. 85, n. 4, p. 1300-1307, 2023. Doi: 10.1007/s00248-022-02004-w.
TELLES AMANDIO, Dylan T., FAITA, Márcia R., POLTRONIERI, Alex S. Effect of commercial bioinsecticides formulated from entomopathogenic fungi on Apis mellifera (Hymenoptera: Apidae). Journal of Apicultural Research, v. 64, n. 3, p. 879-887, 2024. Doi: 10.1080/00218839.2023.2295154.
TOLEDO-HERNÁNDEZ, Ricardo A. et al. Effect of three entomopathogenic fungi on three species of stingless bees (Hymenoptera: Apidae) under laboratory conditions. Journal of Economic Entomology, v. 109, n. 3, p. 1015-1019, 2016. Doi: 10.1093/jee/tow064.
UNIÃO EUROPEIA. Regulamento (CE) n.o 1107/2009 do Parlamento Europeu. Official Journal of the European Union, 300/1, 2009. Disponível em: https://eur-lex.europa.eu/eli/reg/2009/1107/oj. Acesso em 15 mar. 2025.
UNIÃO EUROPEIA. Regulamento Regulamento (UE) n. ° 283/2013. Official Journal of the European Union, L 93/1, 2013. Disponível em: https://eur-lex.europa.eu/legal-content/PT/ALL/?uri=CELEX%3A32013R0283. Acesso em 15 mar. 2025.
UNIÃO EUROPEIA. Regulamento (UE) n.o 284/2013. Official Journal of the European Union, L 93/85, 2013. Disponível em: https://eur-lex.europa.eu/legal-content/PT/TXT/?uri=celex:32013R0284. Acesso em 15 mar. 2025.
UNIÃO EUROPEIA. Active substances, safeners and synergists. 2025. Disponível em: https://ec.europa.eu/food/plant/pesticides/eu-pesticides-database/start/screen/active-substances. Acesso em: 18 jan 2025
USEPA - UNITED STATES ENVIRONMENTAL PROTECTION AGENCY. Pesticide Registration Manual: Chapter 3 - Additional Considerations for Biopesticide Products. 1996. Disponível em https://www.epa.gov/pesticide-registration/pesticide-registration-manual-chapter-3-additional-considerations. Acesso em 15 mar. 2025.
USEPA – UNITED STATES ENVIRONMENTAL PROTECTION AGENCY. Pesticide Assessment Guidelines–Subdivision M: Biorational Pesticides. Research Triangle Park, NC: EPA, 1982. 317p.
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