Abstract
The conservation of terrestrial ecosystems depends largely on the preservation of pollinators, mainly bees. Stingless bees are among the main pollinators of native plants and crops in tropical regions, where they can be exposed to agrochemicals while foraging on contaminated flowers. In the present study, we investigated the effects on stingless bees of both a commonly used insecticide and herbicide in Brazil. Plebeia lucii Moure, 2004 (Apidae: Meliponini) foragers were orally chronically exposed to food contaminated with different concentrations of commercial formulations of the insecticide acephate or the herbicide glyphosate. Bee mortality increased with increasing agrochemical concentrations. Depending on its concentration, the acephate-based formulation reduced the lifespan and impaired the flight ability of bees. The glyphosate-based formulation was toxic only under unrealistic concentrations. Our results demonstrate that realistic concentrations of acephate-based insecticides harm the survival and alter the mobility of stingless bees. The ingestion of glyphosate-based herbicides was safe for forager bees under realistic concentrations.
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References
Abraham J, Benhotons GS, Krampah I, Tagba J, Amissah C, Abraham JD (2018) Commercially formulated glyphosate can kill non-target pollinator bees under laboratory conditions. Entomol Exp Appl 166(8):695–702. https://doi.org/10.1111/eea.12694
Agathokleous E, Calabrese EJ (2019) Hormesis: the dose response for the 21st century: the future has arrived. Toxicology 425:152249. https://doi.org/10.1016/j.tox.2019.152249
Araújo RS, Bernardes RC, Martins GF (2021) A mixture containing the herbicides Mesotrione and Atrazine imposes toxicological effects on workers of Partamona helleri. Sci Total Environ 763:142980. https://doi.org/10.1016/j.scitotenv.2020.142980
Arena M, Sgolastra F (2014) A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23:324–334. https://doi.org/10.1007/s10646-014-1190-1
Bagheri S, Mirzaie M (2019) A mathematical model of honey bee colony dynamics to predict the effect of pollen on colony failure. PLoS ONE 14(11):e0225632. https://doi.org/10.1371/journal.pone.0225632
Batista MA, Ramalho M, Soares AEE (2003) Nesting sites and abundance of Meliponini (Hymenoptera: Apidae) in heterogeneous habitats of the Atlantic Rain Forest, Bahia, Brazil. Lundiana 4(1):19–23. https://doi.org/10.35699/2675-5327.2003.21830
Battisti L, Potrich M, Sampaio AR, Ghisi NC, Costa-Maia FM, Abati R, Martinez CBR, Sofia SH (2021) Is glyphosate toxic to bees? A meta-analytical review. Sci Total Environ 767:145397. https://doi.org/10.1016/j.scitotenv.2021.145397
Behrend JE, Rypstra AL (2018) Contact with a glyphosate-based herbicide has long-term effects on the activity and foraging of an agrobiont wolf spider. Chemosphere 194:714–721. https://doi.org/10.1016/j.chemosphere.2017.12.038
Belsky J, Joshi NK (2020) Effects of fungicide and herbicide chemical exposure on Apis and Non-Apis bees in agricultural landscape. Front Environ Sci 8:81. https://doi.org/10.3389/fenvs.2020.00081
Berg CJ, King HP, Delenstarr G, Kumar R, Rubio F, Glaze T (2018) Glyphosate residue concentrations in honey attributed through geospatial analysis to proximity of large-scale agriculture and transfer off-site by bees. PLoS ONE 13(7):e0198876. https://doi.org/10.1371/journal.pone.0198876
Bernardes RC, Botina LL, Araújo RDS, Guedes RNC, Martins GF, Lima MAP (2022b) Artificial intelligence-aided meta-analysis of toxicological assessment of agrochemicals in bees. Front Ecol Evol 10:845608. https://doi.org/10.3389/fevo.2022.845608
Bernardes RC, Botina LL, Silva FP, Fernandes KM, Lima MAP, Martins GF (2022a) Toxicological assessment of agrochemicals on bees using machine learning tools. J Hazard Mater 424:127344. https://doi.org/10.1016/j.jhazmat.2021.127344
Berry R, López-Martínez G (2020) A dose of experimental hormesis: when mild stress protects and improves animal performance. Comp Biochem Physiol A Mol Integr Physiol 242:110658. https://doi.org/10.1016/j.cbpa.2020.110658
Boily M, Sarrasin B, Deblois C, Aras P, Chagnon M (2013) Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments. Environ Sci Pollut Res Int 20(8):5603–5614. https://doi.org/10.1007/s11356-013-1568-2
Bombardi LM (2019) A Geography of Agrotoxins use in Brazil and its Relations to the European Union. FFLCH – USP, São Paulo
Borges RC, Padovani K, Imperatriz-Fonseca VL, Giannini TC (2020) A dataset of multi-functional ecological traits of Brazilian bees. Sci Data 7:120. https://doi.org/10.1038/s41597-020-0461-3
Botina LL, Bernardes RC, Barbosa WF, Lima MAP, Guedes RNC, Martins GF (2020) Toxicological assessments of agrochemical effects on stingless bees (Apidae, Meliponini). MethodsX 7:100906. https://doi.org/10.1016/j.mex.2020.100906
Castilhos D, Dombroski JLD, Bergamo GC, Gramacho KP, Gonçalves LS (2019) Neonicotinoids and fipronil concentrations in honeybees associated with pesticide use in Brazilian agricultural areas Apidologie 50:657–668. https://doi.org/10.1007/s13592-019-00676-x
Cham KO, Nocelli RCF, Borges LO, Viana-Silva FEC, Tonelli CAM, Malaspina O, Menezes C, Rosa-Fontana AS, Blochtein B, Freitas BM, Pires CSS, Oliveira FF, Contrera FAL, Torezani KRS, Ribeiro MF, Siqueira MAL, Rocha MCLSA (2019) Pesticide exposure assessment paradigm for stingless bees. Environ Entomol 48(1):36–48. https://doi.org/10.1093/ee/nvy137
Čolović MB, Krstić DZ, Lazarević-Pašti TD, Bondžić AM, Vasić VM (2013) Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11(3):315–335. https://doi.org/10.2174/1570159X11311030006
Contardo-Jara V, Klingelmann E, Wiegand C (2009) Bioaccumulation of glyphosate and its formulation Roundup Ultra in Lumbriculus variegatus and its effects on biotransformation and antioxidant enzymes. Environ Pollut 157(1):57–63. https://doi.org/10.1016/j.envpol.2008.07.027
Cullen MG, Thompson LJ, Carolan JC, Stout JC, Stanley DA (2019) Fungicides, herbicides and bees: a systematic review of existing research and methods. PLoS ONE 14(12):e0225743. https://doi.org/10.1371/journal.pone.0225743
Cutler GC, Rix RR (2015) Can poisons stimulate bees? Appreciating the potential of hormesis in bee-pesticide research. Pest Manag Sci 71(10):1368–1370. https://doi.org/10.1002/ps.4042
Cutler GC, Amichot M, Benelli G, Guedes RNC, Qu Y, Rix RR, Ullah F, Desneux N (2022) Hormesis and insects: effects and interactions in agroecosystems. Sci Total Environ 825:153899. https://doi.org/10.1016/j.scitotenv.2022.153899
de Souza APF, Rodrigues NR, Reyes FGR (2021) Glyphosate and aminomethylphosphonic acid (AMPA) residues in Brazilian honey. Food Addit Contam Part B Surveill 14(1):40–47. https://doi.org/10.1080/19393210.2020.1855676
Devillers J, Decourtye A, Budzinski H, Pham-Delgue MH, Cluzeau S, Maurin G (2003) Comparative toxicity and hazards of pesticides to Apis and non-Apis bees. A chemometrical study. SAR QSAR Environ Res 14(5-6):389–403. https://doi.org/10.1080/10629360310001623980
Diniz TO, Pereira NC, Pizzaia WCS, Gigliolli AAS, Silva BG, Borges YM, Guedes TA, Ruvolo-Takasusuki MCC (2020) Toxicity and genetic analysis of bees Scaptotrigona bipunctata after contamination with insecticide acephate. Sci Electron Arch 13(8):8–17. https://doi.org/10.36560/13820201157
Domingues CEC, Inoue LVB, Silva-Zacarin ECM, Malaspina O (2020) Fungicide pyraclostrobin affects midgut morphophysiology and reduces survival of Brazilian native stingless bee Melipona scutellaris. Ecotoxicol Environ Saf 206:111395. https://doi.org/10.1016/j.ecoenv.2020.111395
El-Nahhal Y (2020) Pesticide residues in honey and their potential reproductive toxicity. Sci Total Environ 741:139953. https://doi.org/10.1016/j.scitotenv.2020.139953
Fiedler L (1987) Acephate residues after pre-blossom treatments: effects on small colonies of honey bees. Bull Environ Contam Toxicol 38(4):594–601. https://doi.org/10.1007/BF01608591
Friedrich K, Silveira GR, Amazonas JC, Gurgel AM, Almeida VES, Sarpa M (2021) International regulatory situation of pesticides authorized for use in Brazil: potential for damage to health and environmental impacts. Cad Saude Publica 37(4):e00061820. https://doi.org/10.1590/0102-311X00061820
Garibaldi LA, Carvalheiro LG, Vaissière BE, Gemmill-Herren B, Hipólito J, Freitas BM, Ngo HT, Azzu N, Saez A, Åström J, An J, Blochtein B, Buchori D, García FJC, Silva FO, Devkota K, Ribeiro MF, Freitas L, Gaglianone MC, Goss M, Irshad M, Kasina M, Pacheco Filho AJS, Kiill LHP, Kwapong P, Parra GN, Pires C, Pires V, Rawal RS, Rizali A, Saraiva AM, Veldtman R, Viana BF, Witter S, Zhang H (2016) Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 351(6271):388–391. https://doi.org/10.1126/science.aac7287
Giannini TC, Boff S, Cordeiro GD, Cartolano JrEA, Veiga AK, Imperatriz-Fonseca VL, Saraiva AM (2015) Crop pollinators in Brazil: a review of reported interactions. Apidologie (Celle) 46:209–223. https://doi.org/10.1007/s13592-014-0316-z
Gonçalves RB, Brandão CRF (2008) Diversity of bees (Hymenoptera, Apidae) along a latitudinal gradient in the Atlantic Forest. Biota Neotrop 8(4):51–61. https://doi.org/10.1590/S1676-06032008000400004
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957. https://doi.org/10.1126/science.1255957
Guedes RNC, Rix RR, Cutler GC (2022) Pesticide-induced hormesis in arthropods: towards biological systems. Curr Opin Toxicol 29:43–50. https://doi.org/10.1016/j.cotox.2022.02.001
Guimarães-Cestaro L, Martins MF, Martínez LC, Alves MLTMF, Guidugli-Lazzarini KR, Nocelli RCF, Malaspina O, Serrão JE, Teixeira ÉW (2020) Occurrence of virus, microsporidia, and pesticide residues in three species of stingless bees (Apidae: Meliponini) in the field. Sci Nat 107(3):16. https://doi.org/10.1007/s00114-020-1670-5
Halcroft M, Haigh AM, Spooner-Hart R (2013) Ontogenic time and worker longevity in the Australian stingless bee, Austroplebeia australis. Insect Soc 60:259–264. https://doi.org/10.1007/s00040-013-0291-9
Holder PJ, Jones A, Tyler CR, Cresswell JE (2018) Fipronil pesticide as a suspect in historical mass mortalities of honey bees. Proc Natl Acad Sci USA 115(51):13033–13038. https://doi.org/10.1073/pnas.1804934115
Hussain MA (1987) Anticholinesterase properties of methamidophos and acephate in insects and mammals. Bull Environ Contam Toxicol 38(1):131–138. https://doi.org/10.1007/BF01606570
IBAMA (2021) Relatórios de comercialização de agrotóxicos. https://www.ibama.gov.br/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos. Accessed 15 May 2022
Ivantsova E, Wengrovitz AS, Souders CL, Martyniuk CJ (2022) Developmental and behavioral toxicity assessment of glyphosate and its main metabolite aminomethylphosphonic acid (AMPA) in zebrafish embryos/larvae. Environ Toxicol Pharmacol 93:103873. https://doi.org/10.1016/j.etap.2022.103873
Iwasaki JM, Hogendoorn K (2021) Non-insecticide pesticide impacts on bees: a review of methods and reported outcomes. Agric Ecosyst Environ 314:107423. https://doi.org/10.1016/j.agee.2021.107423
Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity – USA. Apidologie (Celle) 41(3):312–331. https://doi.org/10.1051/apido/2010018
Karise R, Raimets R, Bartkevics V, Pugajeva I, Pihlik P, Keres I, Williams IH, Viinalass H, Mänd M (2017) Are pesticide residues in honey related to oilseed rape treatments? Chemosphere 188:389–396. https://doi.org/10.1016/j.chemosphere.2017.09.013
Kassambara A, Kosinski M, Biecek P (2020) survminer: Drawing Survival Curves using ‘ggplot2’. R package version 0.4.8. https://CRAN.R-project.org/package=survminer. Accessed 15 February 2021
Khoury DS, Myerscough MR, Barron AB (2011) A quantitative model of honey bee colony population dynamics. PLoS One 6(4):e18491. https://doi.org/10.1371/journal.pone.0018491
Khoury DS, Barron AB, Myerscough MR (2013) Modelling food and population dynamics in honey bee colonies. PLoS One 8(5):e59084. https://doi.org/10.1371/journal.pone.0059084
Ledoux ML, Hettiarachchy N, Yu X, Howard L, Lee S-O (2020) Penetration of glyphosate into the food supply and the incidental impact on the honey supply and bees. Food Control 109:106859. https://doi.org/10.1016/j.foodcont.2019.106859
Lima MAP, Martins GF, Oliveira EE, Guedes RNC (2016) Agrochemical‑induced stress in stingless bees: peculiarities, underlying basis, and challenges. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 202(9-10):733–747. https://doi.org/10.1007/s00359-016-1110-3
Macieira OJD, Hebling-Beraldo MJA (1989) Laboratory toxicity of insecticides to workers of Trigona spinipes (F., 1793) (Hymenoptera, Apidae). J Apic Res 28(1):3–6. https://doi.org/10.1080/00218839.1989.11100813
MacInnis G, Forrest JLK (2019) Pollination by wild bees yields larger strawberries than pollination by honey bees. J Appl Ecol 56:824–832. https://doi.org/10.1111/1365-2664.13344
Main AR, Hladik ML, Webb EB, Goyne KW, Mengel D (2020) Beyond neonicotinoids – Wild pollinators are exposed to a range of pesticides while foraging in agroecosystems. Sci Total Environ 742:140436. https://doi.org/10.1016/j.scitotenv.2020.140436
MAPA (2021) Ministério da Agricultura, Pecuária e Abastecimento. http://extranet.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 20 January 2021
Marques MF, Deprá MS, Gaglianone MC (2018) Seasonal variation in bee-plant interactions in an inselberg in the Atlantic Forest in Southeastern Brazil. Sociobiology 65(4):612–620. https://doi.org/10.13102/sociobiology.v65i4.3473
Marques RD, Lima MAP, Marques RD, Bernardes RC (2020) A spinosad-based formulation reduces the survival and alters the behavior of the stingless bee Plebeia lucii. Neotrop Entomol 49:578–585. https://doi.org/10.1007/s13744-020-00766-x
Michener CD (2007) The bees of the world. Johns Hopkins University Press, Baltimore
Motta EVS, Mak M, De Jong TK, Powell JE, O’Donnell A, Suhr KJ, Riddington IM, Moran NA (2020) Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. Appl Environ Microbiol 86:e01150-20. https://doi.org/10.1128/AEM.01150-20
Moure JS (2004) Duas espécies novas de Plebeia Schwarz do Brasil (Hymenoptera, Apidae, Meliponinae). Rev Bras Entomol 48(2):199–202. https://doi.org/10.1590/S0085-56262004000200007
Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, VanEngelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in North American Apiaries: implications for honey bee health. PLoS One 5(3):e9754. https://doi.org/10.1371/journal.pone.0009754
Nocelli RCF, Soares SMM, Monquero PA (2019) Effects of herbicides on the survival of the Brazilian Native Bee Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae). Planta Daninha 37:1–8. https://doi.org/10.1590/S0100-83582019370100156
Orso D, Floriano L, Ribeiro LC, Bandeira NMG, Prestes OD, Zanella R (2016) Simultaneous determination of multiclass pesticides and antibiotics in honey samples based on ultra-high performance liquid chromatography-tandem mass spectrometry. Food Anal Methods 9:1638–1653. https://doi.org/10.1007/s12161-015-0339-8
Osterman J, Theodorou P, Radzevičiūtė R, Schnitker P, Paxton RJ (2021) Apple pollination is ensured by wild bees when honey bees are drawn away from orchards by a mass co-flowering crop, oilseed rape. Agric Ecosyst Environ 315:107383. https://doi.org/10.1016/j.agee.2021.107383
Owagboriayea F, Dedekeb G, Bamideleb J, Aladesidab A, Isiborc P, Feyisolad R, Adelekea M (2020) Biochemical response and vermiremediation assessment of three earthworm species (Alma millsoni, Eudrilus eugeniae and Libyodrilus violaceus) in soil contaminated with a glyphosate-based herbicide. Ecol Indic 108:105678. https://doi.org/10.1016/j.ecolind.2019.105678
Patil VK, David M (2010) Behavioral and morphological endpoints: as an early response to sublethal malathion intoxication in the freshwater fish, Labeo rohita. Drug Chem Toxicol 33(2):160–165. https://doi.org/10.3109/01480540903196816
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
Pohanka M (2011) Cholinesterases, a target of pharmacology and toxicology. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 155(3):219–230. https://doi.org/10.5507/bp.2011.036
Prado FSR, Santos DM, Oliveira TMA, Burgarelli JAM, Castele JB, Vieira EM (2020) Determination and uptake of abamectin and difenoconazole in the stingless bee Melipona scutellaris Latreille, 1811 via oral and topic acute exposure. Environ Pollut 265:114313. https://doi.org/10.1016/j.envpol.2020.114313
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 15 February 2021
Ramalho M (2004) Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Acta bot bras 18(1):37–47. https://doi.org/10.1590/S0102-33062004000100005
Ribeiro MF, Taura TA (2019) Presence of Plebeia aff. flavocincta Nests in Urban Areas. Sociobiology 66(1):66–74. https://doi.org/10.13102/sociobiology.v66i1.3474
Russell S, Barron AB, Harris D (2013) Dynamic modelling of honey bee (Apis mellifera) colony growthand failure. Ecol Modell 265:158–169. https://doi.org/10.1016/j.ecolmodel.2013.06.005
Sánchez D, Solórzano EJ, Liedo P, Vandame R (2012) Effect of the natural pesticide spinosad (Gf-120 Formulation) on the foraging behavior of Plebeia moureana (Hymenoptera: Apidae). J Econ Entomol 105(4):1234–1237. https://doi.org/10.1603/EC12047
Schmolke A, Galic N, Feken M, Thompson H, Sgolastra F, Pitts-Singer T, Elston C, Pamminger T, Hinarejos S (2021) Assessment of the Vulnerability to Pesticide Exposures Across Bee Species. Environ Toxicol Chem 40(9):2640–2651. https://doi.org/10.1002/etc.5150
Seide VE, Bernardes RC, Pereira EJG, Lima MAP (2018) Glyphosate is lethal and Cry toxins alter the development of the stingless bee Melipona quadrifasciata. Environ Pollut 243:1854–1860. https://doi.org/10.1016/j.envpol.2018.10.020
Sikorski JA, Gruys KJ (1997) Understanding Glyphosate’s molecular mode of action with EPSP synthase: evidence favoring an allosteric inhibitor model. Acc Chem Res 30(1):2–8. https://doi.org/10.1021/ar950122+
Therneau T (2020) A Package for Survival Analysis in R. R package version 3.2-7. https://CRAN.R-project.org/package=survival. Accessed 15 February 2021
Therneau TM, Grambsch PM (2000) Modeling Survival Data: Extending the Cox Model. Springer, New York
Thompson HM, Levine SL, Doering J, Norman S, Manson P, Sutton P, Von Mérey G (2014) Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integr Environ Assess Manag 10(3):463–470. https://doi.org/10.1002/ieam.1529
Toledo-Hernández E, Peña-Chora G, Hernández-Velázquez VM, Lormendez CC, Toribio-Jiménez J, Romero‑Ramírez Y, León‑Rodríguez R (2022) The stingless bees (Hymenoptera: Apidae: Meliponini): a review of the current threats to their survival. Apidologie 53:8. https://doi.org/10.1007/s13592-022-00913-w
Tomé HVV, Barbosa WF, Martins GF, Guedes RNC (2015a) Spinosad in the native stingless bee Melipona quadrifasciata: Regrettable non-target toxicity of a bioinsecticide. Chemosphere 124:103–109. https://doi.org/10.1016/j.chemosphere.2014.11.038
Tomé HVV, Martins GF, Lima MAP, Campos LAO, Guedes RNC (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS ONE 7(6):e38406. https://doi.org/10.1371/journal.pone.0038406
Tomé HVV, Barbosa WF, Corrêa AS, Gontijo LM, Martins GF, Guedes RNC (2015b) Reduced-risk insecticides in Neotropical stingless bee species: impact on survival and activity. Ann Appl Biol 167(2):186–196. https://doi.org/10.1111/aab.12217
Tomé HVV, Ramos GS, Araújo MF, Santana WC, Santos GR, Guedes RNC, Maciel CD, Newland PL, Oliveira EE (2017) Agrochemical synergism imposes higher risk to Neotropical bees than to honeybees. R Soc Open Sci 4(1):160866. https://doi.org/10.1098/rsos.160866
Toumi K, Vleminckx C, van Loco J, Schiffers B (2016) Pesticide residues on three cut flower species and potential exposure of florists in Belgium. Int J Environ Res Public Health 13(10):943. https://doi.org/10.3390/ijerph13100943
Tschoeke PH, Oliveira EE, Dalcin MS, Silveira-Tschoeke MCAC, Sarmento RA, Santos GR (2019) Botanical and synthetic pesticides alter the flower visitation rates of pollinator bees in Neotropical melon fields. Environ Pollut 251:591–599. https://doi.org/10.1016/j.envpol.2019.04.133
Vázquez DE, Balbuena MS, Chaves F, Gora J, Menzel R, Farina WM (2020) Sleep in honey bees is affected by the herbicide glyphosate. Sci Rep 10:10516. https://doi.org/10.1038/s41598-020-67477-6
Wickham H, François R, Henry L, Müller K (2020) dplyr: a grammar of data manipulation. R package version 1.0.2. https://CRAN.R-project.org/package=dplyr. Accessed 15 February 2021
Williamson SM, Moffat C, Gomersall MA, Saranzewa N, Connolly CN, Wright GA (2013) Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. Front Physiol 4:13. https://doi.org/10.3389/fphys.2013.00013
Acknowledgements
We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Finance Code 001) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), for funding. We acknowledge the Brazilian Biodiversity Fund (Funbio) and Instituto Humanize (via the program “FUNBIO Grants—Conserving the Future”; Grant number: 107/2019), and the Rufford Foundation (via the Rufford Small Grants Program; Application ID: 30578-1) which also supported this research. We also thank Wagner Faria Barbosa, Gustavo Ferreira Martins, and Italo Salvatore de Castro Pecci Maddalena for their valuable comments which improved this manuscript.
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This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) (Finance Code 001) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). Author Lívia Maria Negrini Ferreira has received research support from the Brazilian Biodiversity Fund (Funbio) and Instituto Humanize via the program “FUNBIO Grants—Conserving the Future” (Grant number: 107/2019), and from The Rufford Foundation via the Rufford Small Grants Programme (Application ID: 30578-1).
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Study conception and design were established by Lívia Maria Negrini Ferreira, Michael Hrncir, and Maria Augusta Pereira Lima. Material preparation was performed by Lívia Maria Negrini Ferreira and Maria Augusta Pereira Lima. Data collection was performed by Lívia Maria Negrini Ferreira and Danilo Vieira de Almeida. Statistical analyses were performed by Lívia Maria Negrini Ferreira, Rodrigo Cupertino Bernardes, and Michael Hrncir. The fundings were acquired by Lívia Maria Negrini Ferreira and Maria Augusta Pereira Lima. The first draft of the manuscript was written by Lívia Maria Negrini Ferreira and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Plebeia lucii is found in degraded and urban areas in Brazil. It is neither a protected nor an endangered species. According to Brazilian legislation, we acquired two permissions to perform the present study (SISBIO permit no. 71998-0 and SISGEN permit no. AE230B3) and ethics approval is not necessary in researches conducted with invertebrates. In addition, our methods are consistent with commonly accepted norms of animal welfare. “The authors have no relevant financial or non-financial interests to disclose.”
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Ferreira, L.M.N., Hrncir, M., de Almeida, D.V. et al. Effects of acephate and glyphosate-based agrochemicals on the survival and flight of Plebeia lucii Moure, 2004 (Apidae: Meliponini). Ecotoxicology 32, 926–936 (2023). https://doi.org/10.1007/s10646-023-02698-9
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DOI: https://doi.org/10.1007/s10646-023-02698-9