Abstract
The decline in bee populations worldwide has been associated with the use of pesticides in crop systems where these insects forage. The use of biopesticides, like spinosad, is preferred as an alternative method to control pests, because it is considered safer to non-target insects. In this study, we evaluated the lethal and sublethal effects of the spinosad-based formulation Tracer® on foragers of the stingless bee Plebeia lucii Moure (Apidae: Meliponini). Groups of bees were fed a pure diet (negative control) or a diet at different concentrations of spinosad. Positive control groups consisted of bees orally exposed to a diet with the neonicotinoid imidacloprid. Next, flight behavior, body mass, and respiration rate were evaluated in surviving bees. The results showed that bees´ survival was reduced by all concentrations of spinosad, when compared with the negative control. Bee locomotion—walking and flight—was reduced in accordance with the increase in spinosad concentrations; however, body mass and respiration rate were not altered. Our results show that the use of Tracer® in ecosystems visited by P. lucii can reduce forager bee survival and reduce their locomotion, generating a negative impact on pollination services provided by these bees.
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References
Araujo R d S, Bernardes RC, Fernandes KM et al (2019a) Spinosad-mediated effects in the post-embryonic development of Partamona helleri (Hymenoptera: Apidae: Meliponini). Environ Pollut 253:11–18. https://doi.org/10.1016/j.envpol.2019.06.087
Araujo R d S, Lopes MP, Barbosa WF et al (2019b) Spinosad-mediated effects on survival, overall group activity and the midgut of workers of Partamona helleri (Hymenoptera: Apidae). Ecotoxicol Environ Saf 175:148–154. https://doi.org/10.1016/j.ecoenv.2019.03.050
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
Barbosa WF, Smagghe G, Guedes RNC (2015) Pesticides and reduced-risk insecticides, native bees and pantropical stingless bees: pitfalls and perspectives. Pest Manag Sci 71:1049–1053. https://doi.org/10.1002/ps.4025
Bernardes RC, Tomé HVV, Barbosa WF, Guedes RNC, Lima MAP (2017) Azadirachtin-induced antifeeding in Neotropical stingless bees. Apidologie 48:275–285. https://doi.org/10.1007/s13592-016-0473-3
Bernardes RC, Barbosa WF, Martins GF, Lima MAP (2018) The reduced-risk insecticide azadirachtin poses a toxicological hazard to stingless bee Partamona helleri (Friese, 1900) queens. Chemosphere 201:550–556. https://doi.org/10.1016/J.CHEMOSPHERE.2018.03.030
Biondi A, Mommaerts V, Smagghe G et al (2012) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536. https://doi.org/10.1002/ps.3396
Brown MJF, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416. https://doi.org/10.1051/apido/2009019
Caro A, Moo-Valle H, Alfaro R, Quezada-Euán JJG (2017) Pollination services of Africanized honey bees and native Melipona beecheii to buzz-pollinated annatto ( Bixa orellana L.) in the neotropics. Agric For Entomol 19:274–280. https://doi.org/10.1111/afe.12206
Casida JE, Quistad GB (1998) Golden age of insecticide research: past, present, or future? Annu Rev Entomol 43:1–16. https://doi.org/10.1146/annurev.ento.43.1.1
Cisneros J, Goulson D, Derwent LC et al (2002) Toxic effects of Spinosad on predatory insects. Biol Control 23:156–163. https://doi.org/10.1006/BCON.2001.1000
Crawley MJ (2012) The R book, 2nd edn. Wiley, Chichester
dos Santos CF, Acosta AL, Dorneles AL, dos Santos PDS, Blochtein B (2016) Queens become workers: pesticides alter caste differentiation in bees. Sci Rep 6:31605–31609. https://doi.org/10.1038/srep31605
Drumond PM, Zucchi R, Oldroyd BP (2000) Description of the cell provisioning and oviposition process of seven species of Plebeia Schwarz (Apidae, Meliponini), with notes on their phylogeny and taxonomy. Insect Soc 47:99–112. https://doi.org/10.1007/PL00001703
Garibaldi LA, Steffan-Dewenter I, Winfree R et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science (80- ) 339:1608–1611. https://doi.org/10.1126/science.1230200
Giannini TC, Boff S, Cordeiro GD et al (2015) Crop pollinators in Brazil: a review of reported interactions. Apidologie 46:209–223. https://doi.org/10.1007/s13592-014-0316-z
Gómez-Escobar E, Liedo P, Montoya P, Vandame R, Sánchez D (2014) Behavioral response of two species of stingless bees and the honey bee (Hymenoptera: Apidae) to GF-120. J Econ Entomol 107:1447–1449. https://doi.org/10.1603/EC13490
Greenleaf SS, Kremen C (2006) Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc Natl Acad Sci 103:13890–13895. https://doi.org/10.1073/pnas.0600929103
Hilário SD, Ribeiro M de F, Imperatriz-Fonseca VL (2012) Can climate shape flight activity patterns of Plebeia remota Hymenoptera, Apidae)? Iheringia Série Zool 102:269–276. https://doi.org/10.1590/S0073-47212012000300004
ICMBio. Instituto Chico Mendes de Conservação da Biodiversidade (2018) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Volume I. Brasília, Brasil
Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66. https://doi.org/10.1146/annurev.ento.51.110104.151146
Jacob CRO, Soares HM, Carvalho SM, Nocelli RC, Malaspina O (2013) Acute toxicity of Fipronil to the stingless bee Scaptotrigona postica Latreille. Bull Environ Contam Toxicol 90:69–72. https://doi.org/10.1007/s00128-012-0892-4
Kerr WE, Carvalho GA, Nascimento VA et al (1996) Abelha urucu : biologia, manejo e conservacao. Fundacao Acangau
Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One 7:e29268. https://doi.org/10.1371/journal.pone.0029268
Kuhn-Neto B, Contrera FAL, Castro MS, Nieh JC (2009) Long distance foraging and recruitment by a stingless bee, Melipona mandacaia. Apidologie 40:472–480. https://doi.org/10.1051/apido/2009007
Lima MAP, Martins GF, Oliveira EE, Guedes RNC (2016) Agrochemical-induced stress in stingless bees: peculiarities, underlying basis, and challenges. J Comp Physiol A 202:733–747. https://doi.org/10.1007/s00359-016-1110-3
MAPA (2019) Ministério da Agricultura, Pecuária e Abastecimento. http://extranet.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 7 Nov 2019
Melo GAR (2016) Plectoplebeia, a new Neotropical genus of stingless bees (Hymenoptera: Apidae). Zool 33. https://doi.org/10.1590/S1984-4689zool-20150153
Michener CD (2000). The bees of the world. University of Kansas Natural History Museum and Department of Entomology, USA.
Morandin LA, Winston ML, Franklin MT, Abbott VA (2005) Lethal and sub-lethal effects of spinosad on bumble bees (Bombus impatiens Cresson). Pest Manag Sci 61:619–626. https://doi.org/10.1002/ps.1058
Moure JS (2004) Duas espécies novas de Plebeia Schwarz do Brasil (Hymenoptera, Apidae, Meliponinae). Rev Bras Entomol 48:199–202. https://doi.org/10.1590/S0085-56262004000200007
Nauen R, Bretschneider T (2002) New modes of action of insecticides. Pestic Outlook 13:241–245. https://doi.org/10.1039/b211171n
Pedro SRM, de Camargo JMF (2013) Stingless Bees from Venezuela. In: Pot-honey. Springer New York, New York, pp 73–86. https://doi.org/10.1007/978-1-4614-4960-7_4
Powney GD, Carvell C, Edwards M, Morris RKA, Roy HE, Woodcock BA, Isaac NJB (2019) Widespread losses of pollinating insects in Britain. Nat Commun 10:1018. https://doi.org/10.1038/s41467-019-08974-9
R Core Team (2018). R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
Ramalho M, Imperatriz-Fonseca VL, Kleinekt-Giovannini A, Cortopassl-Laurino M (1985) Exploitation of floral resources by Plebeia remota Holmberg (Apidae, Meliponinae). Apidologie 16:307–330
Ramalho M, Kleinert-Giovannini A, Imperatriz-Fonseca VL (1990) Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review. Apidologie 21:469–488. https://doi.org/10.1051/apido:19900508
Rasmussen C, Cameron SA (2009) Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol J Linn Soc 99:206–232. https://doi.org/10.1111/j.1095-8312.2009.01341.x
Ribeiro MDF, Taura TA (2019) Presence of Plebeia aff. flavocincta nests in urban areas. Sociobiology 66:66. https://doi.org/10.13102/sociobiology.v66i1.3474
Roldão-Sbordoni YS, Nascimento FS, Mateus S (2018) Estimating colonies of Plebeia droryana (Friese, 1900) (Hymenoptera, Apidae, Meliponini): adults, brood and nest structure. Sociobiology 65:280. https://doi.org/10.13102/sociobiology.v65i2.2345
Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143. https://doi.org/10.1051/apido:2006026
Salgado VL (1998) Studies on the mode of action of Spinosad: insect symptoms and physiological correlates. Pestic Biochem Physiol 60:91–102. https://doi.org/10.1006/PEST.1998.2332
Sánchez D, De J, Solórzano E, 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 105:1234–1237. https://doi.org/10.1603/ec12047
Sarfraz M, Dosdall LM, Keddie BA (2005) Spinosad: a promising tool for integrated Pest management. Outlooks Pest Manag 16:78–84. https://doi.org/10.1564/16apl09
Silva-Neto CM, Bergamini LL, Elias MAS et al (2016) High species richness of native pollinators in Brazilian tomato crops. Brazilian. J Biol 77:506–513. https://doi.org/10.1590/1519-6984.17515
Sparks TC, Crouse GD, Durst G (2001) Natural products as insecticides: the biology, biochemistry and quantitative structure-activity relationships of spinosyns and spinosoids. Pest Manag Sci 57:896–905. https://doi.org/10.1002/ps.358
Tomé HVV, Martins GF, Lima MAP et al (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS One 7:e38406. https://doi.org/10.1371/journal.pone.0038406
Tomé HVV, Barbosa WF, Corrêa AS et al (2015a) Reduced-risk insecticides in Neotropical stingless bee species: impact on survival and activity. Ann Appl Biol 167:186–196. https://doi.org/10.1111/aab.12217
Tomé HVV, Barbosa WF, Martins GF, Guedes RNC (2015b) 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
Tschoeke PH, Oliveira EE, Dalcin MS et al (2015) Diversity and flower-visiting rates of bee species as potential pollinators of melon (Cucumis melo L.) in the Brazilian Cerrado. Sci Hortic (Amsterdam) 186:207–216. https://doi.org/10.1016/J.SCIENTA.2015.02.027
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
Valdovinos-Núñez GR, Quezada-Euán JJG, Ancona-Xiu P et al (2009) Comparative toxicity of pesticides to stingless bees (Hymenoptera: Apidae: Meliponini). J Econ Entomol 102:1737–1742. https://doi.org/10.1603/029.102.0502
Van Nieuwstadt MGL, Ruano Iraheta CE (1996) Relation between size and foraging range in stingless bees (Apidae, Meliponinae). Apidologie 27:219–228. https://doi.org/10.1051/apido:19960404
Acknowledgments
We are especially grateful to Eugênio Eduardo Oliveira and Khalid Haddi for their valuable comments which helped to improve this manuscript.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. We also thank Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig, CBB-APQ-00247-14) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for funding. We are especially grateful to Eugênio Eduardo Oliveira and Khalid Haddi for their valuable comments which helped to improve this manuscript.
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Conceived and designed the experiments: Rodrigo CB; Maria APL and Rafaela DM. Performed the experiments: Raquel DM and Rafaela DM. Analyzed the data: Rodrigo CB. Contributed reagents/materials/analysis tools: Maria APL and Rodrigo CB. Wrote the paper: Raquel DM; Maria APL; Rafaela DM and Rodrigo CB. Maintained stingless bees colonies for the study: Raquel DM and Rafaela DM. Requested the license: Maria APL.
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Marques, R.D., Lima, M.A.P., Marques, R.D. et al. A Spinosad-Based Formulation Reduces the Survival and Alters the Behavior of the Stingless Bee Plebeia lucii. Neotrop Entomol 49, 578–585 (2020). https://doi.org/10.1007/s13744-020-00766-x
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DOI: https://doi.org/10.1007/s13744-020-00766-x