Amazonian stingless bees: lethal concentration and mortality after exposure to insecticide in Melipona interrupta Latreire, 1811 (Hymenoptera: Apidae)
DOI:
https://doi.org/10.12741/ebrasilis.v17.e1065Keywords:
Environmental Impact, Insecticide, Mortality, Thiamethoxam, ToxicologyAbstract
Neonicotinoid insecticides can cause a reduction in feeding rate, locomotion, and behavioral changes such as a reduction in flight speed and distance traveled by adult bees. Chronic exposure to sublethal concentrations can result in behavioral disorders and memory loss. This study investigated the effects of insecticides on Amazonian stingless bees, evaluated whether Melipona interrupta Latreire, 1811, is sensitive and does not reject food contaminated with Thiamethoxam, and compared the effects on native stingless bees from the northern region to Apis mellifera. Mortality was evaluated in these bees when exposed to Tiamethoxam (absolute standard AS and Actara 250 WG - commercial product) and Dimethoate AS as a positive control, thus verifying the lethal concentration 50 (LC50) for the species M. interrupta, popularly known as jupará. The mortality of forager workers exposed to active ingredient formulations indicated an LC50 of 24.77 ng/μL for Dimethoate, validating the tests, and 1.28 ng/μL for Tiamethoxam AS and 1.22 ng/μL for Actara 250 WG, values much lower than those found for A. mellifera bees, which were 4.28 ng i.a./µL of Tiamethoxam. Therefore, we concluded that formulations with the active ingredients Dimethoate and Tiamethoxam are highly toxic to Amazonian bees of the species M. interrupta.
References
A.b.e.l.h.a. (2015). Agricultura e Polinizadores. Associação Brasileira de Estudos das Abelhas.
Aranha, A & Rocha, L (2019). Detecção e concentração de agrotóxicos de 2014 a 2017 de acordo com dados de Controle do Sistema de Informação de Vigilância da Qualidade da Água para Consumo Humano (SISAGUA), do Ministério da Saúde. Agência Pública/Repórter Brasil. URL: <https://portrasdoalimento.info/2019/04/15/coquetel-com-27-agrotoxicos-foi-achado-na-agua-de-1-em-cada-4-municipios/>. Access: 03.iii.2022
Arena, M, & Sgolastra, F (2014). A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology, 23: 1-11. https://doi.org/10.1007/s10646-014-1190-1
Ascher, JS & Pickering, J (2020). Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). URL: <http://www.discoverlife.org/mp/20q?guide=Apoidea_species>. Access: 01.x.2023.
Aupinel, P; Fortini, D; Dufour, H; Michaud, B; Marolleau, F; Tasei, JN & Odoux, JF (2007). Toxicity of Dimethoate and Fenoxycarb to honey bee brood Apis mellifera, using a new in vitro standardized feeding method. Pest Manangement Science, 63(11): 1090-1094. https://doi.org/10.1002/ps.1446
Bombardi, LM (2017). Geografia do uso de agrotóxicos no Brasil e conexões com a União Europeia. FFLCH-USP.
Bortolotti, L; Montanari, R; Marcelino, J; Medrzycki, JP; Maini, S & Porrini, C (2003). Effects of sub-lethal imidacloprid doses on honey bees’ homing rate and foraging activity. Bulletin of Insectology, 56(1): 63-68.
Brigante, J; Costa, JO; Espíndola, EL & Daam, MA (2021). Acute toxicity of the insecticide abamectin and the fungicide difenoconazole (individually and in mixture) to the tropical stingless bee Melipona scutellaris. Ecotoxicology, 30(9): 1872-1879. https://doi.org/10.1007/s10646-021-02458-7
Brittain, C & Potts, SG (2011). The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic and Applied Ecology, 12(4): 321-331. https://doi.org/10.1016/j.baae.2010.12.004
Brown, JC & Oliveira, ML (2014). The impact of agricultural colonization and deforestation on stingless bee (Apidae: Meliponini) composition and richness in Rondônia, Brazil. Apidologie, 45: 172-188. https://doi.org/10.1007/s13592-013-0236-3
Camargo, JMF & Pedro, SRM (2013). Meliponini Lepeletier, 1836. In: Moure, JS, Urban, D & Melo, GAR (Eds.). Catalogue of bees (Hymenoptera, Apoidea) in the neotropical region. online version. Sociedade Brasileira de Entomologia. URL: <http://moure.cria.org.br/index>.
Carneiro, FF (2015). Dossiê ABRASCO: um alerta sobre os impactos dos agrotóxicos na saúde. EPSJV/Expressão Popular. URL: <https://abrasco.org.br/download/dossie-abrasco-um-alerta-sobre-os-impactos-dos-agrotoxicos-na-saude/>
Carvalho-Zilse, GA & Nunes-Silva, CG (2012). Threats to the Stingless Bees in the brazilian Amazon: How to deal with scarce biological data and an increasing rate of destruction, pp. 147-168. In: Florio, RM (Ed.). Bees: Biology, Threats and Colonies. Nova Science Publishers
Castro, AS & Andrade, DC (2016). O custo econômico do desmatamento da Floresta Amazônica brasileira (1988-2014). Perspectiva Econômica, 12(1): 1-15. https://doi.org/10.4013/pe.2016.121.01
Costa, LM; Grella, TC; Barbosa, RA; Malaspina, O & Nocelli, RCF (2015). Determination of acute lethal doses (LD50 and LC50) of imidacloprid for the native bee Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae). Sociobiology, 62(4): 578-582. https://doi.org/10.13102/sociobiology.v62i4.792
Cresswell, JE; Page, CJ; Uygun, MB; Holmbergh, M; Li, Y; Wheeler, JG; Laycock, I; Pook, CJ; Ibarra, NH, Smirnoff, N; et al. (2012). Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology, 115(6): 365-371. https://doi.org/10.1016/j.zool.2012.05.003
Desneux, N; Decourtye, A & Delpuech, JM (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review Entomology, 52: 81-106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Faria, ABC (2009). Revisão sobre alguns grupos de inseticidas utilizados no manejo Integrado de pragas florestais. Ambiência, 5(2): 345-358.
Fraxe, TDJP; Pinheiro, JAC; Costa, MSB; Gonçalves, VVC; Oka, JM; Sena, GM & Pereira, CF (2020). Uso de agrotóxicos e seus impactos socioambientais nos municípios de Rio Preto da Eva e Careiro da Várzea, Amazonas-Brasil. Brazilian Journal of Development, 6(5): 31429-31451. https://doi.org/10.34117/bjdv6n5-558
Gallo, DO, Nakano, O; Silvera Neto, S; Carvalho, RPL; Baptista, GC; Berti Filho, E; Parra, JRP; Zucchi, RA; Alves, SB; Vendramin, JD; et al. (2002). Entomologia Agrícola. FEALQ.
Godfray, HCJ, Blacquiere, T; Field, LM; Hails, RS; Petrokofsky, G; Potts, SG; Raine, NE; Vanbergen, AJ & McLean, AR (2014). A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences, 281(1786): 20140558. https://doi.org/10.1098/rspb.2014.0558
Gough, HJ; McIndoe, EC & Lewis, GB (1994). The use of dimethoate as a reference compound in laboratory acute toxicity tests on honey bees (Apis mellifera L.) 1981-1992. Journal of Apicultural research, 33(2): 119-125. https://doi.org/10.1080/00218839.1994.11100859
Goulson, D (2013). Review: An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology, 50(4): 977-987. https://doi.org/10.1111/1365-2664.12111
Hardstone, MC & Scott, JC (2010). A review of the interactions between multiple insecticide resistance loci. Pesticide Biochemistry and Physiology, 97(2): 123-128. https://doi.org/10.1016/j.pestbp.2009.07.010
Henry, M; Beguin, M; Requier, F; Rollin, O; Odoux, JF; Aupinel, P; Aptel, J; Tchamitchian, S & Decourtye, A (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336(6079): 348-350. https://doi.org/10.1126/science.1215039
Hood, M, (2021). Colony collapse disorder. Encyclopedia Britannica. URL: <https://www.britannica.com/science/colony-collapse-disorder>. Access: 28.ix.2023.
IBGE (Instituto Brasileiro de Geografia e Estatística) (2022). Fronteira Agrícola - Amazônia Legal, URL: <https://www.ibge.gov.br/geociencias/cartas-e-mapas/mapas-regionais/15976-fronteira-agricola-amazonia-legal.html?=t=o-que-e>. Access: 28.ix.2022.
Inhuma, YG; Paula Cabral, L; Gonçalves, GS & Clemente, FAS (2020). Produtores rurais do distrito de novo remanso/amazonas: caracterização e percepção dos riscos relacionados ao uso de agrotóxicos na cultura do abacaxi. Nexus - Revista de Extensão do IFAM, 6(10): 105-115. URL: <https://nexus.ifam.edu.br/index.php/revista-nexus/article/view/123>
Jacob, CRO; Zanardi, OZ; Malaquias, JB; Silva, CAS & Yamamoto, PT (2019a). The impact of four widely used neonicotinoid insecticides on Tetragonisca angustula (Latreille) (Hymenoptera: Apidae). Chemosphere, 224, 65-70. https://doi.org/10.1016/j.chemosphere.2019.02.105
Jacob, CRO; Malaquias, JB; Zanardi, OZ; Silva, CA; Jacob, JF & Yamamoto, PT (2019b). Oral acute toxicity and impact of neonicotinoids on Apis mellifera L. and Scaptotrigona postica Latreille (Hymenoptera: Apidae). Ecotoxicology, 28(7): 744-753. https://doi.org/10.1007/s10646-019-02070-w
Jiang, J; Ma, D; Zou, N; Yu, X; Zhang, ZQ; Liu, F & Mu, W (2018). Concentrations of imidacloprid and thiamethoxam in pollen, nectar and leaves from seeddressed cotton crops and their potential risk to honeybees (Apis mellifera L.). Chemosphere, 201: 159-167. https://doi.org/10.1016/j.chemosphere.2018.02.168
Lopes, M; Ferreira, JB & Santos, GD (2005). Abelhas sem-ferrão: a biodiversidade invisível. Agriculturas, 2(4): 1-3. URL: <http://aspta.org.br/article/abelhas-sem-ferrao-a-biodiversidade-invisivel/>. Access 28.ix.2023.
Ludicke, JC & Nieh, JC (2020). Thiamethoxam impairs honey bee visual learning, alters decision times, and increases abnormal behaviors. Ecotoxicology and Environmental Safety, 193: 110367. https://doi.org/10.1016/j.ecoenv.2020.110367
Miotelo, L; Mendes dos Reis, AL; Malaquias, JB; Malaspina, O & Roat, TC (2021). Apis mellifera and Melipona scutellaris exhibit differential sensitivity to thiamethoxam. Environmental Pollution, 268: 115770. https://doi.org/10.1016/j.envpol.2020.115770
Mitchell, EA; Mulhauser, B; Mulot, M; Mutabazi, A; Glauser, G & Aebi, A (2017). A worldwide survey of neonicotinoids in honey. Science, 358(6359): 109-111. https://doi.org/10.1126/science.aan3684
Moraes, SS; Bautista, ARL & Viana, BF (2000). Avaliação da toxicidade aguda (DL50 e CL50) de inseticidas para Scaptotrigona tubiba (Smith) (Hymenoptera: Apidae): via de contato. Anais da Sociedade Entomológica do Brasil, 29(1): 31-37. https://doi.org/10.1590/S0301-80592000000100004.
Moreira, DR; Gigliolli, AAS; Falco, JR; Julio, AHF; Volnistem, EA; Chagas, FD & Ruvolo-Takasusuki, MCC (2018). Toxicity and effects of the neonicotinoid thiamethoxam on Scaptotrigona bipunctata Lepeletier, 1836 (Hymenoptera: Apidae). Environmental Toxicology, 33(4): 463-475. https://doi.org/10.1002/tox.22533
Mullin, CA; Fine, JD; Reynolds, RD & Frazier, MT (2016). Toxicological risks of agrochemical spray adjuvants: organosilicone surfactants may not be safe. Frontiers in Public Health, 4. https://doi.org/10.3389/fpubh.2016.00092
Nogueira, DS (2023). Overview of Stingless Bees in Brazil (Hymenoptera: Apidae: Meliponini). EntomoBrasilis, 16: e1041. https://doi.org/10.12741/ebrasilis.v16.e1041
Nogueira-Neto, P (1997). Vida e criação de abelhas indígenas sem ferrão. Nogueirapis.
OECD (Organization for Economic Co-operation and Development) (1998a). Guidelines for the testing of chemicals: honeybees, acute oral toxicity test. Environmental health safety division, organization for economic co-operation and development. Number 213.
OECD (Organization for Economic Co-operation and Development) (1998b). Guidelines for the testing of chemicals: honeybees, acute contact toxicity test. Environmental health safety division, organization for economic co-operation and development. Number 214.
Oliveira, RA; Roat, TC; Carvalho, SM & Malaspina, O (2014). Side-effects of thiamethoxam on the brain andmidgut of the africanized honeybee Apis mellifera (Hymenopptera: Apidae). Environmental Toxicology, 29(10): 1122-1133. https://doi.org/10.1002/tox.21842
Pacífico da Silva, I; Oliveira, FAZ; Pedroza, HP; Gadelha, ICN; Melo, MM & Soto-Blanco, B (2015). Pesticide exposure of honeybees (Apis mellifera) pollinating melon crops. Apidologie, 46(6): 703-715. https://doi.org/10.1007/s13592-015-0360-3
Pedro, SRM (2014). The stingless bee fauna in Brazil (Hymenoptera: Apidae). Sociobiology, 61(4): 348-354. https://doi.org/10.13102/sociobiology.v61i4.348-354
Piovesan, B; Padilha, AC; Morais, MC; Botton, M; Grützmacher, AD & Zotti, MJ (2020). Effects of insecticides used in strawberries on stingless bees Melipona quadrifasciata and Tetragonisca fiebrigi (Hymenoptera: Apidae). Environmental Science and Pollution Research, 27(34): 42472-42480. https://doi.org/10.1007/s11356-020-10191-7
Prado, RB (2021). Serviços ecossistêmicos: estado atual e desafios para a pesquisa na Amazônia. Revista Terceira Margem Amazônia, 6(16): 11-22. https://doi.org/10.36882/2525-4812.2021v6i16.ed.esp.p11-22
Queiroz, AA; Martins, JAS & Cunha, JPAR (2008). Adjuvantes e qualidade da água na aplicação de agrotóxicos. Bioscience Journal, 24(4): 8-19. URL: <https://seer.ufu.br/index.php/biosciencejournal/article/view/6923>.
Quiroga-Murcia, DE; Zotti, MJ; Polanía, IZ & Pech-Pech, EE (2017). Toxicity evaluation of two insecticides on Tetragonisca angustula and Scaptotrigona xanthotricha (Hymenoptera: Apidae). Agronomía Colombiana, 35(3): 340-349. https://doi.org/10.15446/agron.colomb.v35n3.65447
R Development Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. URL: <https://www.R-project.org>.
Rigitano, RLO (2001). Toxicologia e seletividade de inseticidas. UFLA/FAEPE.
Ritz, C & Streibig, JC (2005). Bioassay analysis using R. Journal of Statistical Software,12(5): 1-22. https://doi.org/10.18637/jss.v012.i05
Rodrigues, AS (2006). Até quando o etnoconhecimento sobre as abelhas sem ferrão (Hymenoptera, Apidae, Meliponinae) será transmitido entre gerações pelos índios Guarani M’byá da Aldeia Morro da Saudade, localizada na cidade de São Paulo, Estado de São Paulo, Brasil. Sitientibus. Série Ciências Biológicas, 6(4):343-350. https://doi.org/10.13102/scb8201
Rosa-Fontana, ADS; Dorigo, AS; Soares-Lima, HM; Nocelli, RCF & Malaspina, O (2020). Is the Water Supply a Key Factor in Stingless Bees’ Intoxication? Journal of Insect Science, 20(6). https://doi.org/10.1093/jisesa/ieaa127
Sanchez-Bayo, F & Goka, K (2014). Pesticide Residues and Bees-A Risk Assessment. PloS ONE, 9(4): e94482. https://doi.org/10.1371/journal.pone.0094482
Sanchez-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
Sandrock, C; Tanadini, M; Tanadini, LG; Fauser-Misslin, A; Potts, SG & Neumann, P (2014). Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLOS ONE, 9(8): e103592. https:/doi.org/10.1371/journal.pone.0103592
Souza, JC; Reis, PR; Rigitano, RLO & Ciociola Júnior, AI (2006). Eficiência de tiametoxam no controle do bichomineiro do cafeeiro: I, influência da modalidade de aplicação. Coffee Science, 1(2): 143-149. URL: <http://www.sbicafe.ufv.br:80/handle/123456789/3891>.
Tomizawa, M & Casida, JE (2003). Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annual Review of Entomology, 48: 339-364. https://doi.org/10.1146/annurev.ento.48.091801.112731
Tomizawa, M & Casida, JE (2005). Neonicotinoid insecticide toxicology: mechanisms of Selective Action. Annual Review of Pharmacology and Toxicology, 45: 247-268. https://doi.org/10.1146/annurev.pharmtox.45.120403.095930
Torres, FZV; Rigitano, RLDO & Torres, LC (2010). Ocorrência de tiametoxam em folhas e frutos de cafeeiro (Coffea arabica L.) após aplicação na modalidade de esguicho no solo. Coffee Science, 5(2): 148-153. URL: <http://www.sbicafe.ufv.br:80/handle/123456789/3915>
Williams, GR; Troxler, A; Retschnig, G; Roth, K; Yañez, O; Shutler, D; Neumann, P & Gauthier, L (2015). Neonicotinoid pesticides severely affect honey bee queens. Scientific Reports, 5(1): 1-8. https://doi.org/10.1038/srep14621
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Author(s)
This work is licensed under a Creative Commons Attribution 4.0 International License.
Access is unrestricted and the documentation available on the Creative Commons License (BY) (http://creativecommons.org/licenses/by/4.0/ ).
I declare for proper purposes that the copyright of the submitted text is now licensed in the form of the Creative Commons License, as specified above.
The copyright of the article belongs to the authors
Funding data
-
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Grant numbers Finance Code 001 -
Conselho Nacional de Desenvolvimento Científico e Tecnológico