Differential insecticide susceptibility of the Neotropical stingless bee Melipona quadrifasciata and the honey bee Apis mellifera

Apidologie

Volumn 45, Issue 5, 2014, Pages 626-636

  Del Sarto, Mário César L ^a   Oliveira, Eugênio E ^a   Guedes, Raul Narciso C ^a   Campos, Lúcio Antônio O ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

acute toxicity; buzz pollinators; insecticide exposure; wild bees

Indexed keywords

ABAMECTIN; CULTIVATION; DELTAMETHRIN; HONEYBEE; INSECTICIDE; POLLINATOR; POLLUTION EXPOSURE; TOXICITY;

EID: 84906262382     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1007/s13592-014-0281-6     Document Type: Article

References (51)

1. Antonini, Y., Costa, R.G., Martins, R.P. (2006) Floral preferences of a neotropical stingless bee, Melipona quadrifasciata Lepeletier (Apidae: Meliponina) in an urban forest fragment. Braz. J. Biol. 66, 463-471
2. Becher, M.A., Osborne, J.L., Thorbek, P., Kennedy, P.J., Grimm, V. (2013) Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models. J. Appl. Ecol. 50(4), 868-880
3. Biddinger, D.J., Robertson, J., Mullin, C., Frazier, J., Ashcraft, S., Rajotte, E.G., Joshi, N.K., Vaughn, M. (2013) Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS ONE 8(9), e72587
4. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313(5785), 351-354
5. Bispo dos Santos, S., Roselino, A., Hrncir, M., Bego, L. (2009) Pollination of tomatoes by the stingless bee Melipona quadrifasciata and the honey bee Apis mellifera (Hymenoptera: Apidae). Genet. Mol. Res. 8, 751-757
6. Brittain, C., Potts, S.G. (2011) The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl. Ecol. 12, 321-331
7. Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F., Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. U. S. A. 108(2), 662-667
8. Cornman, R., Tarpy, D., Chen, Y., Jeffreys, L., Lopez, D., Pettis, J.S., vanEngelsdorp, D., Evans, D. (2012) Pathogen webs in collapsing honey bee colonies. PLoS ONE 7(8), e43562
9. Cresswell, J.E., Page, C.J., Uygun, M.B., Holmbergh, M., Li, Y., et al. (2012) Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology 115(6), 365-371
10. Cruz, D., Freitas, B., Silva, L., EMS, S., Bomfim, I. (2005) Pollination efficiency of the stingless bee Melipona subnitida on greenhouse sweet pepper. Pesq. Agrop. Brasileira 40(12), 1197-1201
11. Decourtye, A., Henry, M., Desneux, N. (2013) Overhaul pesticide testing on bees. Nature 497, 188
12. Del Sarto, M.C.L., Peruquetti, R.C., Campos, L.A.O. (2005) Evaluation of the Neotropical stingless bee Melipona quadrifasciata (Hymenoptera: Apidae) as pollinator of greenhouse tomatoes. J. Econ. Entomol. 98(2), 260-266
13. Devillers, J., Pham-Delègue, M., Decourtye, A., Budzinski, H., Cluzeau, S., et al. (2003) Modeling the acute toxicity of pesticides to Apis mellifera. Bull. Insectol. 56(1), 103-109
14. EPA (2014) ECOTOX database (http://cfpub.epa.gov/ecotox/), United States Environmental Protection Agency (Accessed on 20th Jan 2014)
15. Felton, J., Oomen, P., Stevenson, J. (1986) Toxicity and Hazard of pesticides to honeybees: harmonization of test methods. Bee World 67, 114-124
16. Freitas, B.M., Paxton, R.J. (1998) A comparison of two pollinators: the introduced honey bee Apis mellifera and an indigenous bee Centris tarsata on cashew Anacardium occidentale in its native range of NE Brazil. J. Appl. Ecol. 35(1), 109-121
17. Freitas, B.M., Imperatriz-Fonseca, V.L.C., Medina, L.M., Kleinert, A.D.M.P., Galetto, L., Nates-Parra, G., Quezada-Euan, J.J.G. (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40(3), 332-346
18. Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., et al. (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339(6127), 1608-1611
19. Gill, R., Ramos-Rodriguez, O., Raine, N. (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105-109
20. Hardstone, Scott, J. (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag. Sci. 66(66), 1171-1180
21. IUCN (2013) IUCN red list of endangered species. In: International Union for Conservation of Nature and Natural Resources (Ed.), pp. http://www. iucnredlist.org/ [Accessed 2 Oct 2013]
22. Jha, S., Kremen, C. (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. Proc. Natl. Acad. Sci. U. S. A. 110(2), 555-558
23. Johnson, R.M., Ellis, M.D., Mullin, C.A., Frazier, M. (2010) Pesticides and honey bee toxicity - USA. Apidologie 41(3), 312-331
24. Kevan, P.G. (1999) Pollinators as bioindicators of the state of the environment: species, activity and diversity. Agric. Ecosyst. Environ. 74(1-3), 373-393
25. Kremen, C., Williams, N.M., Thorp, R.W. (2002) Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. U. S. A. 99(26), 16812-16816
26. Krupke, C., Hunt, G., Eitzer, B., Andino, G., Given, K. (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7(1), e29268
27. Lautenbach, S., Seppelt, R., Liebscher, J., Dormann, C.F. (2012) Spatial and temporal trends of global pollination benefit. PLoS ONE 7(4), e35954
28. Liu, Z., Williamson, M.S., Lansdell, S.J., Denholm, I., Han, Z., Millar, N.S. (2005) A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc. Natl. Acad. Sci. U. S. A. 102(24), 8420-8425
29. Lourenço, C., Carvalho, S.M., Malaspina, O., Nocelli, R.C.F. (2012) Oral toxicity of fipronil insecticide against the stingless bee Melipona scutellaris (Latreille, 1811). Bull. Environ. Contam. Toxicol. 89(4), 921-924
30. Luz, C., Fernandes-Salomão, T., Lage, L., Resende, H., Tavares, M. et al. (2011) Pollen sources for Melipona capixaba Moure & Camargo: an endangered Brazilian stingless bee. Psyche 2011(Article ID 107303), 1-7
31. Maeta, Y., Kitamura, T. (1981) Pollinating efficiency by Osmia cornifrons (Radoszkowski) in relation to required number of nesting bees for economic fruit production. Honeybee Sci 2, 65-72 (in Japanese)
32. MAPA (2013) AGROFIT: Sistema de Agrotóxicos Fitossanitários - MAPA/CGAF/DFIA/DAS. In: Ministério da Agricultura Pecuária e Abastecimento (Ed.), Brasilia, Brazil, pp. http://extranet.agricultura.gov.br/ agrofit-cons/principal-agrofit-cons [Accessed on October 2nd, 2013]
33. 50) de insecticidas para Scaptotrigona tubida (Smith) (Hymenoptera: Apidae): via de contacto. Ann. Soc. Entomol. Bras 29, 31-37
34. Morandin, L.A., Winston, M.L., Franklin, M.T., Abbott, V.A. (2005) Lethal and sub-lethal effects of spinosad on bumble bees (Bombus impatiens Cresson). Pest Manag. Sci. 61(7), 619-626
35. Mullin, C., Frazier, M., Frazier, J., Ashcraft, S., Simonds, R., vanEngelsdorp, D., Pettis, J.S. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5(3), e9754
36. Nunes-Silva, P., Hrncir, M., Silva, C.I., Roldão, Y., Imperatriz-Fonseca, V. (2013) Stingless bees, Melipona fasciculata, as efficient pollinators of eggplant (Solanum melongena) in greenhouses. Apidologie 44(5), 537-546
37. OECD (1998a) Guidelines for the testing of chemicals. Number 213, Honeybees, acute oral toxicity test. In: OECD Environmental Health and Safety Division (ed.), Paris
38. OECD (1998b) Guidelines for the testing of chemicals. Number 214. Honeybees, acute contact toxicity test. In: OECD Environmental Health and Safety Division (Ed.)
39. Osborne, J.L. (2012) Bumblebees and pesticides. Nature 491, 43-45
40. Pettis, J., Lichtenberg, E., Andree, M., Stitzinger, J., Rose, R., vanEngelsdorp, D. (2013) Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8(7), e70182
41. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25(6), 345-353
42. Resende, H., Barros, F., Campos, L.A.O., Fernandes-Salomão, T. (2008) Visitação de orquídea por Melipona capixaba Moure & Camargo (Hymenoptera: Apidae), abelha ameaçada de extinção. Neotropical Entomol. 37, 609-611
43. Robertson, J.L., Preisler, H.K. (1992) Pesticide bioassays with arthropods. CRC, Boca Raton, FL, USA
44. SAS Institute (2008) SAS/STAT user's guide. SAS Institute Inc, Cary
45. Silveira, A.V.T., Antoniosi-Filho, N.R. (2013) Proposta de alternativas menos tóxicas para ingredientes ativos de agrotóxicos no mercado brasileiro. Pestic. R. Ecotoxicol. Meio Amb. 23, 11-24
46. Thompson, Wilkins, S., Battersby, A., Waite, R., Wilkinson, D. (2007) Modelling long-term effects of IGRs on honey bee colonies. Pest Manag. Sci. 63, 1081-1084
47. Tirado, R., Simon, G., Johnston, P., A. Greenpeace International, The Netherlands. (2013) Bees in declilne - a review of factors that put pollinators and agriculture in Europe at risk. In: Greenpeace International (ed.), Greenpeace Research Laboratories Technical Report (Review) 01/2013, Amsterdam
48. Tomé, H., Martins, G., Lima, M., Campos, L.A.O., Guedes, R. (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS ONE 7(6), e38406
49. Valdovinos-Núñez, G.R., Quezada-Euán, J.J.G., Ancona-Xiu, P., Moo-Valle, H., Carmona, A., Sanchez, E.R. (2009) Comparative toxicity of pesticides to stingless bees (Hymenoptera: Apidae: Meliponini). J. Econ. Entomol. 102(5), 1737-1742
50. vanEngelsdorp, D., Meixner, M.D. (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 103, S80-S95
51. Winfree, R., Williams, N.M., Dushoff, J., Kremen, C. (2007) Native bees provide insurance against ongoing honey bee losses. Ecol. Lett. 10(11), 1105-1113