Is glyphosate toxic to bees? A meta-analytical review

Science of The Total Environment - Tập 767 - Trang 145397 - 2021
Lucas Battisti1, Michele Potrich2, Amanda Roberta Sampaio2, Nédia de Castilhos Ghisi3, Fabiana Martins Costa-Maia4, Raiza Abati2, Claudia Bueno dos Reis Martinez1, Silvia Helena Sofia1
1Universidade Estadual de Londrina (UEL), Programa de Pós-Graduação em Ciências Biológicas, Rodovia Celso Garcia Cid, PR 445 km 380, Campus Universitário, 86057-970 Londrina, PR, Brazil
2Universidade Tecnológica Federal do Paraná, UTFPR, Campus Dois Vizinhos, LABCON, Estrada para Boa Esperança, km 04, Comunidade São Cristóvão, 86660-000 Dois Vizinhos, PR, Brazil
3Universidade Tecnológica Federal do Paraná, Campus Dois Vizinhos, UTFPR, Programa de Pós-Graduação em Biotecnologia, Estrada para Boa Esperança, km 04, Comunidade São Cristóvão, 86660-000 Dois Vizinhos, PR, Brazil
4Universidade Tecnológica Federal do Paraná, UFTPR, Campus Dois Vizinhos, UNEPE Apicultura, Estrada para Boa Esperança, km 04, Comunidade São Cristóvão, 86660-000 Dois Vizinhos, PR, Brazil

Tài liệu tham khảo

Abou-Shaara, 2018, Effects of two herbicides on healthy and Nosema infected honey bee workers, Arthropods, 7, 31 Abraham, 2018, Commercially formulated glyphosate can kill non-target pollinator bees under laboratory conditions, Entomol. Exp. Appl., 166, 695, 10.1111/eea.12694 Almasri, 2020, Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees, Ecotoxicol. Environ. Saf., 203, 10.1016/j.ecoenv.2020.111013 Amarante Junior, 2002, Glifosato: propriedades, toxicidade, usos e legislação, Quim Nova, 25, 589, 10.1590/S0100-40422002000400014 Andrea, M.M., Peres, T.B., Luchini, L.C.,Bazrin, S., Papini, S., Matallo, B.F., Savoy, V.L.T. 2003. Influence of repeated applications of glyphosate on its persistence and soil bioactivity. Pesq. Agropec. Bras. 38, 1329-1335. doi.org/10.1590/S0100-204X2003001100012. Balayiannis, 2008, Bee honey as an environmental bioindicator of pesticides’ occurrence in six agricultural areas of Greece, Arch. Environ. Contam. Toxicol., 55, 462, 10.1007/s00244-007-9126-x Balbuena, 2015, Effects of sublethal doses of glyphosate on honeybee navigation, J. Exp. Biol., 218, 2799, 10.1242/jeb.117291 Benbrook, 2016, Trends in glyphosate herbicide use in the United States and globally, Environ. Sci. Eur., 28, 1, 10.1186/s12302-016-0070-0 Beringer, J., 2019. O declínio populacional das abelhas: causas, potenciais soluções e perspectivas futuras. Rev. Eletrônica Científica da UERGS 5, 18–27. doi:10.21674/2448-0479.51.18-27 Blake, 2018, The environmental fate and ecotoxicity of glyphosate, Outlooks Pest Manag., 29, 266, 10.1564/v29_dec_08 Blot, 2019, Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota, PLoS One, 14, 1, 10.1371/journal.pone.0215466 Boily, 2013, Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments, Environ. Sci. Pollut. Res., 20, 5603, 10.1007/s11356-013-1568-2 Boily, 2017, Foraging in maize field areas: a risky business?, Sci. Total Environ., 601–602, 1522, 10.1016/j.scitotenv.2017.06.014 Borenstein, 2009 Botina, 2020, Toxicological assessments of agrochemical effects on stingless bees (Apidae, Meliponini), MethodsX, 7, 10.1016/j.mex.2020.100906 Calderone, 2012, Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992-2009, PLoS One, 7, 24, 10.1371/journal.pone.0037235 Casida, 2013, Neuroactive insecticides: targets, selectivity, resistance, and secondary effects, Annu. Rev. Entomol., 58, 99, 10.1146/annurev-ento-120811-153645 Cullen, 2019, Fungicides, herbicides and bees: a systematic review of existing research and methods, PLoS One, 14, 1, 10.1371/journal.pone.0225743 Cuschieri, 2019, The STROBE guidelines. Saudi J. Anaesth., 13, S31, 10.4103/sja.SJA_543_18 Dai, 2018, The herbicide glyphosate negatively affects midgut bacterial communities and survival of honey bee during larvae reared in vitro, J. Agric. Food Chem., 66, 7786, 10.1021/acs.jafc.8b02212 Desneux, 2007, The sublethal effects of pesticides on beneficial arthropods, Annu. Rev. Entomol., 52, 81, 10.1146/annurev.ento.52.110405.091440 Dill, G.M., Sammons, R.D., Feng, P.C., Kohn, F., Kretzmer, K., Mehrsheikh, A., Bleeke, M., Honegger, J.L., Farmer, D., Wright, D., Haupfear, E.A., 2010. Glyphosate: discovery, development, applications, and properties, in: Nandula, V.K. (ed) Glyphosate Resistance in Crops and Weeds: History, Development, and Management. Wiley, Hoboken ISBN 978-0-470-41031-8. Doner, 1977, The sugars of honey—a review, J. Sci. Food Agric., 28, 443, 10.1002/jsfa.2740280508 El Agrebi, 2020, Honeybee and consumer’s exposure and risk characterisation to glyphosate-based herbicide (GBH) and its degradation product (AMPA): residues in beebread, wax, and honey, Sci. Total Environ., 704, 135312, 10.1016/j.scitotenv.2019.135312 Fagard, 1996, Advantages and disadvantages of the meta-analysis approach, J. Hypertens., 14, 9, 10.1097/00004872-199609002-00004 Faghani, 2018, Effect of glyphosate on honey bee (Apis mellifera) performance, Arthropods., 7, 77 Faita, 2020, Glyphosate-based herbicides and Nosema sp. microsporidia reduce honey bee (Apis mellifera L.) survivability under laboratory conditions, J. Apic. Res., 59, 332, 10.1080/00218839.2020.1736782 FAO, 2013, Edible insects Filho, 2014, O que é, para que serve e como se faz uma meta-análise?, Teor. e Pesqui., 23, 205, 10.4322/tp.2014.018 Gallo, D.O., Nakano, S., Silveira Neto, R.P.L., Carvalho, G.C., Baptista, E., Berti Filho, J.R.P., Parra, R.A., Zucchi, S.B., Alves, J.D., Vendramim, L.C., 2002. Entomologia Agrícola, FEALQ. ed. 2002, Piracicaba, SP. Ghisi, N. de C., Oliveira, E.C. de, Prioli, A.J., 2016. Does exposure to glyphosate lead to an increase in the micronuclei frequency? A systematic and meta-analytic review. Chemosphere 145, 42–54. doi:https://doi.org/10.1016/j.chemosphere.2015.11.044. Giesy, 2000, Ecotoxicological risk assessment for Roundup® herbicide, Rev. Environ. Contam. Toxicol., 167, 35 Gill, 2018, Glyphosate toxicity for animals, Environ. Chem. Lett., 16, 401, 10.1007/s10311-017-0689-0 Gonalons, 2018, Impaired associative learning after chronic exposure to pesticides in young adult honey bees, J. Exp. Biol., 221 González-Santoyo, 2012, Phenoloxidase: a key component of the insect immune system, Entomol. Exp. Appl., 142, 1, 10.1111/j.1570-7458.2011.01187.x Goulson, 2003, Conserving wild bees for crop pollination. Food, Agric. Environ., 1, 142 Goulson, 2015, Bee declines driven by combined stress from parasites, pesticides, and lack of flowers, Science, 347, 1255957, 10.1126/science.1255957 Gregorc, 2012, Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor), J. Insect Physiol., 58, 1042, 10.1016/j.jinsphys.2012.03.015 Hedges, L. V, 1981. Distribution Theory for Glass ’ s Estimator of Effect Size and Related Estimators Author ( s ): Larry V . Hedges Published by: American Educational Research Association and American Statistical Association Journaet o Educational Statis6tiL Key Words : Me 6, 107–128. Helmer, 2015, Effects of realistic doses of atrazine, metolachlor, and glyphosate on lipid peroxidation and diet-derived antioxidants in caged honey bees (Apis mellifera), Environ. Sci. Pollut. Res., 22, 8010, 10.1007/s11356-014-2879-7 Herbert, 2014, Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour, J. Exp. Biol., 217, 3457 Higgins, 2008, Commentary: heterogeneity in meta-analysis should be expected and appropriately quantified, Int. J. Epidemiol., 37, 1158, 10.1093/ije/dyn204 Julian P T Higgins, Simon G Thompson, Jonathan J Deeks, D.G.A., 2006. Measuring inconsistency in knowledgebases. J. Intell. Inf. Syst. 27, 159–184. doi:https://doi.org/10.1007/s10844-006-2974-4. Hua, 2012, Exploring the possibility of quantifying the effects of plant protein ingredients in fish feeds using meta-analysis and nutritional model simulation-based approaches, Aquaculture, 356–357, 284, 10.1016/j.aquaculture.2012.05.003 IARC, International Agency for Research on Cancer, 2017. Some organophosphate insecticides and herbicides. International Agency for Research on Cancer, Lyon, France. http://monographs.iarc.fr/ENG/Monographs/vol112/mono112.pdf. p. 32. IBAMA, Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais e Renováveis, 2020. Relatórios de comercialização de agrotóxicos. 2020. [WWW Document]. 2020. URL http://ibama.gov.br/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos#boletinsanuais Johnson, 2015, Honey bee toxicology, Annu. Rev. Entomol., 60, 415, 10.1146/annurev-ento-011613-162005 Jumarie, 2017, Mixtures of herbicides and metals affect the redox system of honey bees, Chemosphere, 168, 163, 10.1016/j.chemosphere.2016.10.056 Kwong, 2016, Gut microbial communities of social bees, Nat. Rev. Microbiol., 14, 374, 10.1038/nrmicro.2016.43 Ledoux, 2020, Penetration of glyphosate into the food supply and the incidental impact on the honey supply and bees, Food Control, 109, 10.1016/j.foodcont.2019.106859 Lee, 1991, Glutathione S-transferase activities in phytophagous insects: induction and inhibition by plant phototoxins and phenols, Insect Biochem., 21, 353, 10.1016/0020-1790(91)90001-U Leoci, R., Ruberti, M., 2020. Glyphosate in agriculture: environmental persistence and effects on animals. A Review. J. Agric. Environ. Int. Dev. 114, 99–122. doi:10.12895/jaeid.20201.1167. Lewis, 2016, An international database for pesticide risk assessments and management, Hum. Ecol. Risk. Assess., 22, 1050, 10.1080/10807039.2015.1133242 Li, 2007, Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics, Annu. Rev. Entomol., 52, 231, 10.1146/annurev.ento.51.110104.151104 Lovatto, 2007, Meta-análise em pesquisas científicas: enfoque em metodologias, Rev. Bras. Zootec., 36, 285, 10.1590/S1516-35982007001000026 Maleszka, 2014, The social honey bee in biomedical research: realities and expectations, Drug Discov. Today Dis. Model., 12, 7, 10.1016/j.ddmod.2014.06.001 Mamy, 2016, Glyphosate fate in soils when arriving in plant residues, Chemosphere, 154, 425, 10.1016/j.chemosphere.2016.03.104 McHugh, 2009, The odds ratio: calculation, usage, and interpretation, Biochem. Medica, 19, 120, 10.11613/BM.2009.011 Michener, C., 2007. The Bees of the World. Baltimore, The John Hopkins University Press, 2nd ed., 953p. Motta, 2018, Glyphosate perturbs the gut microbiota of honey bees, Proc. Natl. Acad. Sci. U. S. A., 115, 10305, 10.1073/pnas.1803880115 Motta, 2020, Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees, Appl. Environ. Microbiol., 86, 10.1128/AEM.01150-20 Nocelli, 2019, Effects of herbicides on the survival of the brazilian native bee Melipona scutellaris Latreille, 1811 (hymenoptera: apidae), Planta Daninha, 2016, 1 Orr, 2020, Global patterns and drivers of bee distribution, Curr. Biol., 31, 1 Orwin, 1982, RRT meets RDD: statistical strategies for assuring response privacy in telephone surveys, Public Opin. Q., 46, 560, 10.1086/268752 Pérez, L., Solange, M., Mir, L., 2011. Effects of herbicide glyphosate and glyphosate-based formulations on aquatic ecosystems. pp. 343–368, in: Herbicides and Environment, Kortekamp, A. (ed). InTech, ISBN: 978-953-307-476-4. doi: https://doi.org/10.5772/12877. Pires, 2016, Weakness and collapse of bee colonies in Brazil: are there cases of CCD?, Pesqui. Agropecu. Bras., 51, 422, 10.1590/S0100-204X2016000500003 PPDB, Pesticides Properties Database, 2020. A to Z List of Pesticide Active Ingredients. URL: http://sitem.herts.ac.uk/aeru/ppdb/en/atoz.htm. Acceessed at November 3, 2020. PRISMA - Transparent reporting of systematic reviews and meta-analyses, 2015. Principais itens para relatar Revisões Sistemáticas e Meta-análises: A recomendação PRISMA. Epidemiol. e Serviços Saúde 24, 335–342. doi:https://doi.org/10.5123/s1679-49742015000200017 Quigley, 2019, Honey bees as bioindicators of changing global agricultural landscapes, Curr. Opin. Insect Sci., 35, 132, 10.1016/j.cois.2019.08.012 R Core Team, 2020. R: a language and environment for statistical computing., http://www.R-project.org/. Richmond, 2018, Glyphosate: a review of its global use, environmental impact, and potential health effects on humans and other species, J. Environ. Stud. Sci., 8, 416, 10.1007/s13412-018-0517-2 Rolando, 2017, The risks associated with glyphosate-based herbicide use in planted forests, Forests, 8, 1, 10.3390/f8060208 Rosenberg, M.S., Adam, D.C., Gurevitch, J., 2000. MetaWin: Statistic Software for Meta-Analysis (version 2)., Sinauer As. ed. Sunderland, Massachusetts. Rubio, 2014, Survey of glyphosate residues in honey, corn and soy products, J. Environ. Anal. Toxicol., 05, 1000249 Ruiz-Toledo, 2014, Effect of the concentration of glyphosate present in body waters near transgenic soybean fields on the honeybee Apis mellifera, and the stingless bee Tetragonisca angustula, Acta zoológica Mex., 30, 408, 10.21829/azm.2014.302114 Sanchez-Bayo, 2016 Seide, 2018, Glyphosate is lethal and cry toxins alter the development of the stingless bee Melipona quadrifasciata, Environ. Pollut., 243, 1854, 10.1016/j.envpol.2018.10.020 Szumilas, 2010, Explaining odds ratios, J. Can. Acad. Child Adolesc. Psychiatry, 19, 227 Thompson, 2014, Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example, Integr. Environ. Assess. Manag., 10, 463, 10.1002/ieam.1529 Tomé, 2020, Frequently encountered pesticides can cause multiple disorders in developing worker honey bees, Environ. Pollut., 256, 10.1016/j.envpol.2019.113420 Van Bruggen, 2018, Environmental and health effects of the herbicide glyphosate, Sci. Total Environ., 616–617, 255, 10.1016/j.scitotenv.2017.10.309 Van Maele-Fabry, 2011, Residential exposure to pesticides and childhood leukaemia: a systematic review and meta-analysis, Environ. Int., 37, 280, 10.1016/j.envint.2010.08.016 Vázquez, 2018, Glyphosate affects the larval development of honey bees depending on the susceptibility of colonies, PLoS One, 13, 1, 10.1371/journal.pone.0205074 Vázquez, 2020, Sleep in honey bees is affected by the herbicide glyphosate, Sci. Rep., 10, 1, 10.1038/s41598-020-67477-6 Vázquez, 2020, Chronic exposure to glyphosate induces transcriptional changes in honey bee larva: a toxicogenomic study, Environ. Pollut., 261, 114148, 10.1016/j.envpol.2020.114148 Viechtbauer, W., 2010. Conducting meta-analyses in R with the metafor. J. Stat. Softw. 36, 1–48. URL: http://www.jstatsoft.org/v36/i03/. doi: 10.18637/jss.v036.i03. Viechtbauer, W., 2017. Meta-Analysis package for R - Package “metafor.” URL: http://www.metafor-project.org/doku.php. WebPlotDigitizer, 2020. WebPlotDigitizer 4.3 [WWW Document]. 2020. URL https://apps.automeris.io/wpd/ WHO, World Health Organization, 2017, Some organophosphate insecticides and herbicides, IARC Monographs Volume, 112 Zhang, 2015, Degradation dynamics of glyphosate in different types of citrus orchard soils in China, Molecules, 20, 1161, 10.3390/molecules20011161 Zhao, 2020, Transcriptomic and metabolomic landscape of the molecular effects of glyphosate commercial formulation on Apis mellifera ligustica and Apis cerana cerana, Sci. Total Environ., 744, 140819, 10.1016/j.scitotenv.2020.140819 Zhu, 2015, Spray toxicity and risk potential of 42 commonly used formulations of row crop pesticides to adult honey bees (Hymenoptera: Apidae), J. Econ. Entomol., 108, 2640, 10.1093/jee/tov269 Zhu, 2017, Feeding toxicity and impact of imidacloprid formulation and mixtures with six representative pesticides at residue concentrations on honey bee physiology (Apis mellifera), PLoS One, 12, 1 Zhu, 2017, Synergistic toxicity and physiological impact of imidacloprid alone and binary mixtures with seven representative pesticides on honey bee (Apis mellifera), PLoS One, 12, 1 Zhukovskaya, 2013, Grooming behavior as a mechanism of insect disease defense, Insects, 4, 609, 10.3390/insects4040609