Abstract
Use of pesticides in agroecosystems is considered a major cause of bees diversity losses in the Neotropics, where Plebeia emerina (Friese) and Tetragonisca fiebrigi (Schwarz) (Hymenoptera: Apidae: Meliponini) are wild pollinators of native and crop plants. The aim of this study was to know the acute lethal toxicity of acetamiprid, malathion, phosmet and spinosad insecticides on P. emerina and T. fiebrigi. We obtained the mean concentration and mean lethal dose (LC50 and LD50) and the mean survival of workers after oral and topical exposure to insecticides, respectively. The LC50 values (ng a.i./μl of diet) and the decreasing order of toxicity for P. emerina was spinosad (4.96) > malathion (18.75) > phosmet (97.33) > acetamiprid (4204.06), and for T. fiebrigi also was spinosad (5.65) > malathion (8.39) > phosmet (53.91) > acetamiprid (9841.32), when orally exposed. The LD50 values (ng a.i./bee) and the decreasing order of toxicity for P. emerina was spinosad (1.90) > malathion (10.90) > phosmet (19.54) > acetamiprid (6216.55) and for T. fiebrigi was malathion (29.29) ≥ spinosad (29.79) > phosmet (41.95) > acetamiprid (1421.23), when topically exposed. The mean survival (hours) of contaminated bees by malathion, phosmet, and spinosad, was 11.81, 7.20, and 12.32 for P. emerina and 8.55, 7.20, and 13.34 for T. fiebrigi when orally exposed; and was 4.87, 9.87 and 11.17 for P. emerina, and 4.87, 4.76, and 19.05 for T. fiebrigi when topically exposed. Malathion, phosmet, and spinosad were highly toxic, while acetamiprid was moderately toxic. Our results indicated that the insecticides tested, mainly malathion, phosmet, and spinosad may be harmful to P. emerina and T. fiebrigi, making it essential to propose measures to minimize their impact on wild pollinators.
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References
Abdalla FC, Jones GR, Morgan ED, Cruz-Landim CD (2003) Comparative study of the cuticular hydrocarbon composition of Melipona bicolor Lepeletier, 1836 (Hymenoptera, Meliponini) workers and queens. Genet Mol Res 2:191–199
Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2:1–12. https://doi.org/10.2478/v10102-009-0001-7
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
Bacci L, Pereira EJ, Fernandes FL, Picanço MC, Crespo ALB, Campos MR (2006) Seletividade fisiológica de inseticidas a vespas predadoras (Hymenoptera: Vespidae) de Leucoptera coffeella (Lepidoptera: Lyonetiidae). BioAssay 1:1–7. https://doi.org/10.14295/BA.v1.0.38
Bailey J, Scott-Dupree C, Harris R, Tolman J, Harris B (2005) Contact and oral toxicity to honey bees (Apis mellifera) of agents registered for use for sweet corn insect control in Ontario, Canada. Apidologie 36:623–633. https://doi.org/10.1051/apido:2005048
Becher MA, Osborne JL, Thorbek P, Kennedy PJ, Grimm V (2013) Towards a systems approach for understanding honeybee decline: a stock taking and synthesis of existing models. J Appl Ecol 50:868–880. https://doi.org/10.1111/1365-2664.12112
Berenbaum MR, Johnson RM (2015) Xenobiotic detoxification pathways in honey bees. Curr Opin Insect Sci 10:51–58. https://doi.org/10.1016/j.cois.2015.03.005
Blomquist GJ, Bagnères AG (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology Cambridge University Press, New York, NY
Brasil (2018) Ministério da Agricultura, Pecuária e Abastecimento. Agrofit. http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons
Brittain C, Potts SG (2011) The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl Ecol 12:321–331. https://doi.org/10.1016/j.baae.2010.12.004
Brunet JL, Badiou A, Belzunces LP (2005) In vivo metabolic fate of [14C]‐acetamiprid in six biological compartments of the honeybee, Apis mellifera L. Pest Manag Sci 61:742–748. https://doi.org/10.1002/ps.1046
Camargo JMF, Pedro SEM (2013) Meliponini Lepeletier, 1836. In Moure JS, Urban D, Melo GAR (Orgs). Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical Region—online version. http://www.moure.cria.org.br/catalogue
Carvalho SM, Carvalho GA, Carvalho CF, Bueno Filho JSS, Baptista APM (2009) Toxicidade de acaricidas/inseticidas empregados na citricultura para a abelha africanizada Apis mellifera L., 1758 (Hymenoptera: Apidae). Arq Inst Biol 76:597–606
Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117. https://doi.org/10.1146/annurev-ento-120811-153645
Cortopassi-Laurino M, Imperatriz-Fonseca VL, Roubik DW, Dollin A, Heard T, Aguilar I, Venturieri GC, Eardley C, Nogueira-Neto P (2006) Global meliponiculture: challenges and opportunities. Apidologie 37:275–292. https://doi.org/10.1051/apido:2006027
Decourtye A, Devillers J (2010) Ecotoxicity of neonicotinoid insecticides to bees. In: Thany SH (ed) Insect nicotinic acetylcholine receptors. Adv Exp Med Biol 85–95. https://doi.org/10.1007/978-1-4419-6445-8_8
Decourtye A, Henry M, Desneux N (2013) Environment: overhaul pesticide testing on bees. Nature 497:188. https://doi.org/10.1038/497188a
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Dively GP, Kamel A (2012) Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J Agric Food Chem 60:4449–4456. https://doi.org/10.1021/jf205393x
Dorneles AL, de Souza Rosa A, Blochtein B (2017) Toxicity of organophosphorus pesticides to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi. Apidologie 48:612–620. https://doi.org/10.1007/s13592-017-0502-x
Felton JC, Oomen PA, Stevenson JH (1986) Toxicity and hazard of pesticides to honeybees: harmonization of the test methods. Bee World 67:114–124. https://doi.org/10.1080/0005772X.1986.11098883
Fletcher M, Barnett L (2003) Bee pesticide poisoning incidents in the United Kingdom. Bull Insectology 56:141–145
Fukuto TR (1990) Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245–254. https://doi.org/10.1289/ehp.9087245
Garratt MP, Breeze TD, Jenner N, Polce C, Biesmeijer JC, Potts SG (2014) Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agric Ecosyst Environ 184:34–40. https://doi.org/10.1016/j.agee.2013.10.032
Giannini TC, Cordeiro GD, Freitas BM, Saraiva AM, Imperatriz-Fonseca VL (2015a) The dependence of crops for pollinators and the economic value of pollination in Brazil. J Econ Entomol 108:849–857. https://doi.org/10.1093/jee/tov093
Giannini TC, Boff S, Cordeiro GD, Cartolano EA, Veiga AK, Imperatriz-Fonseca VL, Saraiva AM (2015b) Crop pollinators in Brazil: a review of reported interactions. Apidologie 46:209–223. https://doi.org/10.1007/s13592-014-0316-z
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. Proc R Soc B 281:20140558. https://doi.org/10.1098/rspb.2014.0558
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. https://doi.org/10.1126/science.1255957
Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62. https://doi.org/10.1146/annurev-ento-010715-023646
Hardstone MC, Scott JG (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag Sci 66:1171–1180. https://doi.org/10.1002/ps.2001
Henry M, Beguin M, Requier F, Rollin O (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336:348–350. https://doi.org/10.1126/science.1215039
Imperatriz-Fonseca VL, Saraiva AM, De Jong D (2006) Bees as pollinators in Brazil. In: Workshop on São Paulo Declaration on Pollinators plus 5 Forum. Holos Editora, São Paulo
Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23:371–378. https://doi.org/10.1016/j.cropro.2003.08.018
Jeschke P, Nauen R, Sparks TC, Loso MR, Watson GB, Babcock JM, Kramer JV, Zhu Y, Nugent BM, Thomas JD, Crouse GD, Dripps JE, Waldron C, Salgado VL, Schnatterer S, Holmes KA, Pitterna T (2011) Nervous system. In: Modern crop protection compounds 1127–1326. https://doi.org/10.1002/9783527644179.ch32
Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity – USA. Apidologie 41:312–331. https://doi.org/10.1051/apido/2010018
Klatt BK, Burmeister C, Westphal C, Tscharntke T, von Fragstein M (2013) Flower volatiles, crop varieties and bee responses. PLoS ONE 8:e72724. https://doi.org/10.1371/journal.pone.0072724
Kirst HA (2010) The spinosyn family of insecticides: realizing the potential of natural products research. J Antibiot 63:101. https://doi.org/10.1038/ja.2010.5
Laycock I, Lenthall KM, Barratt AT, Cresswell JE (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21:1937–1945. https://doi.org/10.1007/s10646-012-0974-4
Leite GLD, Picanco M, Guedes RNC, Gusmão MR (2012) Selectivity of insecticides with and without mineral oil to Brachygastra lecheguana (Hymenoptera: Vespidae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ceiba 39:191–194
Leonhardt SD, Wallace HM, Blüthgen N, Wenzel F (2015) Potential role of environmentally derived cuticular compounds in stingless bees. Chemoecology 25:159–167. https://doi.org/10.1007/s00049-015-0185-6
Magalhães TL, Venturieri GC (2010) Aspectos econômicos da criação de abelhas indígenas sem ferrão (Apidae: Meliponini) no Nordeste paraense. Embrapa Amazônia Oriental, Belém
McBride DK (2011) Protecting honeybees from pesticides. North Dakota University, Fargo
Medrzycki P, Giffard H, Aupinel P, Belzunces LP et al. (2013) Standard methods for toxicology research in Apis mellifera. J Apic Res 52:1–60. https://doi.org/10.3896/IBRA.1.52.4.14
Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins, Baltimore
Michener CD (2013) The meliponini. In Pot-honey. Springer, New York, NY
Miles M (2003) The effects of spinosad, a naturally derived insect control agent to the honeybee. Bull Insectol 56:119–124
Milhome MAL, Sousa DOB, Lima FDA, Nascimento RD (2009) Avaliação do potencial de contaminação de águas superficiais e subterrâneas por pesticidas aplicados na agricultura do Baixo Jaguaribe, CE. Eng Sanit Ambient 14:363–372
Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, VanEngelsdorp D et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5:e9754. https://doi.org/10.1371/journal.pone.0009754
Nicholls CI, Altieri MA (2013) Plant biodiversity enhances bees and other insect pollinators in agroecosystems: a review. Agron Sustain Dev 33:257–274. https://doi.org/10.1007/s13593-012-0092-y
Nocelli RCF, Malaspina O, Carvalho SM, Lourenço CT, Roat TC, Pereira AM, Silva-Zacarin ECM (2011) As abelhas e os defensivos agrícolas. In: Imperatriz-Fonseca VL, Canhos DAL, Saraiva AM (eds) Polinizadores no Brasil: contribuição e perspectivas para a biodiversidade, uso sustentável, conservação e serviços ambientais. EDUSP, São Paulo
Oliveira EE, Aguiar RW, de S, Sarmento R, de A, Tuelher E, de S, Guedes RNC (2002) Seletividade de inseticidas a Theocolax elegans parasitoide de Sitophilus zeamais. Biosci J 18:11–16
Oliveira KAM, Ribeiro LS, De Oliveira GV (2013) Caracterização microbiológica, físico-química e microscópica de mel de abelhas Canudo (Scaptotrigona depilis) e Jataí (Tetragonisca angustula). Rev Brasileira de Produtos Agroindustriais 15:239–248
OECD (1998) Organization for economic co-operation and development. guidelines for the testing of chemicals: honeybees, acute oral toxicity test. Environmental health safety division, organisation for economic co-operation and development, Paris, France, Number 213
OECD (1998) Organization for Economic Co-Operation and Development. Guidelines for the testing of chemicals: Honeybees, acute contact toxicity test. Environmental health safety division, organisation for economic co-operation and development, Paris, France, Number 214
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Orth AI (1984) Levantamento das abelhas nativas (Hym., Apoidea) associadas às flores da macieira (‘Pyrus malus’ L.). Anais do V Congresso Brasileiro de Apicultura, Florianópolis, Santa Catarina, Brasil, pp 280–287
Ortolan SMLS, Laroca S (1996) Melissocenótica em áreas de cultivo de macieira (Pyrus malus L.) em Lages (Santa Catarina), com notas comparativas e experimento de polinização com Plebeia emerina (Friese) (Hymenoptera, Apoidea). Acta Biol Parana 25:1–113
PIC (2018) Lista PIC—Produção Integrada de Citrus. Grade de inseticidas, acaricidas, fungicidas da produção integrada de citrus—PIC BRASIL. Disponível em https://www.fundecitrus.com.br/pdf/Grade_de_Agrotoxicos_03.12.18_PT.pdf. Accessed 28 Nov 2018
PIM (2018) Produção Integrada de Maçã—PIM. Grade de agrotóxicos e agroquímicos ciclo 2018/2019. Disponível em http://agapomi.com.br/wp-content/uploads/Grade-de-Agroqu%C3%ADmicos-ciclo-2018-19-1.pdf. Accessed 28 Nov 2018
Pires CSS, Pereira FDM, Lopes MTDR, Nocelli RCF, Malaspina O, Pettis JS, Teixeira ÉW (2016) Weakness and collapse of bee colonies in Brazil: are there cases of CCD? Pesqui Agropecuária Brasileira 51:422–442. https://doi.org/10.1590/S0100-204X2016000500003
Piovesan B (2018) Inventário de visitantes florais na cultura do morangueiro e efeitos de inseticidas sobre as abelhas nativas Melipona quadrifasciata e Tetragonisca fiebrigi. Federal University of Pelotas, Dissertation, Pelotas, Rio Grande do Sul, Brasil
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
Rinkevich FD, Margotta JW, Pittman JM, Danka RG et al. (2015) Genetics, synergists, and age affect insecticide sensitivity of the honey bee, Apis mellifera. PLoS ONE 10:e0139841. https://doi.org/10.1371/journal.pone.0139841
Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22. https://doi.org/10.18637/jss.v012.i05
Salgado VL, Saar R (2004) Desensitizing and non-desensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. J Insect Physiol 50:867–879. https://doi.org/10.1016/j.jinsphys.2004.07.007
Sanchez-Bayo F, Goka K (2014) Pesticide residues and bees–a risk assessment. PloS ONE 9:e94482. https://doi.org/10.1371/journal.pone.0094482
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
Schreinemachers P, Tipraqsa P (2012) Agricultural pesticides and land use intensification in high, middle and low income countries. Food Policy 37:616–626. https://doi.org/10.1016/j.foodpol.2012.06.003
Slaa EJ, Chaves LAS, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315. https://doi.org/10.1051/apido:2006022
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
Stanley J, Sah K, Jain SK, Bhatt JC, Sushil SN (2015) Evaluation of pesticide toxicity at their field recommended doses to honeybees, Apis cerana and A. mellifera through laboratory, semi-field and field studies. Chemosphere 119:668–674. https://doi.org/10.1016/j.chemosphere.2014.07.039
Stevenson JH (1978) The acute toxicity of unformolated pesticides to worker honey bees (Apis mellifera L.). Plant Pathol 27:38–40. https://doi.org/10.1111/j.1365-3059.1978.tb01070.x
Sylvia M (2010) Pesticide safety 2010—insecticides update, bee toxicity and management decisions. http://scholarworks.umass.edu/cranberry_extension
Thompson HM, Hunt LV (1999) Extrapolating from honeybees to bumblebees in pesticide risk assessment. Ecotoxicology 8:147–166. https://doi.org/10.1023/A:1026444029579
Thompson GD, Dutton R, Sparks TC (2000) Spinosad–a case study: an example from a natural products discovery programme Pest Manag Sci 56:696–702. https://doi.org/10.1002/1526-4998(200008)56:83.0.CO;2-5
Tomé HVV, Barbosa WF, Martins GF, Guedes RNC (2015) 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
Urbaneja A, Chueca P, Montón H, Pascual-Ruiz S et al. (2009) Chemical alternatives to malathion for controlling Ceratitis capitata (Diptera: Tephritidae), and their side effects on natural enemies in Spanish citrus orchards. J Econ Entomol 102:144–151. https://doi.org/10.1603/029.102.0121
Venturieri GC, Alves DA, Villas-Bôas JK, Carvalho CA et al. (2011) Meliponicultura no Brasil: Situação atual e perspectivas futuras para o uso na polinização. In: Imperatriz-Fonseca VL, Canhos DAL, Saraiva AM (eds) Polinizadores no Brasil: contribuição e perspectivas para a biodiversidade, uso sustentável, conservação e serviços ambientais. EDUSP, São Paulo
Vossler FG, Fagúndez GA, Blettler DC (2014) Variability of food stores of Tetragonisca fiebrigi (Schwarz) (Hymenoptera: Apidae: Meliponini) from the Argentine Chaco based on pollen analysis. Sociobiology 61:449–460
Witter S, Nunes-Silva P, Blochtein B, Lisboa BB, Imperatriz-Fonseca VL (2014) As abelhas e a agricultura. EDIPUCRS, Porto Alegre
Wiest L, Buleté A, Giroud B, Fratta F et al. (2011) Multi-residue analysis of 80 environmental contaminants in honeys, honeybees and pollens by one extraction procedure followed by liquid and gas chromatography coupled with mass spectrometric detection. J Chromatogr A 1218:5743–5756. https://doi.org/10.1016/j.chroma.2011.06.079
Yasuda M, Sakamoto Y, Goka K, Nagamitsu T, Taki H (2017) Insecticide susceptibility in Asian honey bees (Apis cerana (Hymenoptera: Apidae)) and implications for wild honey bees in Asia. J Econ Entomol 110:447–452. https://doi.org/10.1093/jee/tox032
Zhu YC, Adamczyk J, Rinderer T, Yao J, Danka R, Luttrell R, Gore J (2015) Spray toxicity and risk potential of 42 commonly used formulations of row crop pesticides to adult honey bees (Hymenoptera: Apidae). J Econ Entomol 108:2640–2647. https://doi.org/10.1093/jee/tov269
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This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and to Brazilian Agricultural Research Corporation (EMBRAPA)—Embrapa Grape & Wine. The authors also thank financial supported by the National Council for Scientific and Technological Development (CNPq—Grand numbers: 140328/2016-5; 310407/2017-6; 302557/2017-2).
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Padilha, A.C., Piovesan, B., Morais, M.C. et al. Toxicity of insecticides on Neotropical stingless bees Plebeia emerina (Friese) and Tetragonisca fiebrigi (Schwarz) (Hymenoptera: Apidae: Meliponini). Ecotoxicology 29, 119–128 (2020). https://doi.org/10.1007/s10646-019-02150-x
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DOI: https://doi.org/10.1007/s10646-019-02150-x