Ecotoxicology

, Volume 23, Issue 3, pp 324–334 | Cite as

A meta-analysis comparing the sensitivity of bees to pesticides

Article

Abstract

The honey bee Apis mellifera, the test species used in the current environmental risk assessment procedure, is generally considered as extremely sensitive to pesticides when compared to other bee species, although a quantitative approach for comparing the difference in sensitivity among bees has not yet been reported. A systematic review of the relevant literature on the topic followed by a meta-analysis has been performed. Both the contact and oral acute LD50 and the chronic LC50 reported in laboratory studies for as many substances as possible have been extracted from the papers in order to compare the sensitivity to pesticides of honey bees and other bee species (Apiformes). The sensitivity ratio R between the endpoint for the species a (A. mellifera) and the species s (bees other than A. mellifera) was calculated for a total of 150 case studies including 19 bee species. A ratio higher than 1 indicated that the species s was more sensitive to pesticides than honey bees. The meta-analysis showed a high variability of sensitivity among bee species (R from 0.001 to 2085.7), however, in approximately 95 % of the cases the sensitivity ratio was below 10. The effect of pesticides in domestic and wild bees is dependent on the intrinsic sensitivity of single bee species as well as their specific life cycle, nesting activity and foraging behaviour. Current data indicates a need for more comparative information between honey bees and non-Apis bees as well as separate pesticide risk assessment procedures for non-Apis bees.

Keywords

Toxicity Environmental risk assessment Apis mellifera Apiformes Pollinators Comparative ecotoxicology 

Supplementary material

10646_2014_1190_MOESM1_ESM.doc (626 kb)
Supplementary material 1 (DOC 626 kb)

References

  1. Ahmad Z, Johansen C (1973) Selective toxicity of carbophenothion and trichlorfon to the honey bee and the alfalfa leafcutting bee. Environ Entomol 2(1):27–30Google Scholar
  2. Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85(9):2408–2421CrossRefGoogle Scholar
  3. 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(4):623–633CrossRefGoogle Scholar
  4. Biesmeijer JC, Roberts SP, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313(5785):351–354CrossRefGoogle Scholar
  5. Blacquiere T, Smagghe G, van Gestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21(4):973–992CrossRefGoogle Scholar
  6. Bosch J, Sgolastra F, Kemp WP (2008) Life cycle ecophysiology of Osmia mason bees used as crop pollinators. In: James RR, Pitts-Singer TL (eds) Bee pollination in agricultural ecosystems. Oxford University Press, OxfordGoogle Scholar
  7. 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(4):321–331CrossRefGoogle Scholar
  8. Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339(6127):1611–1615CrossRefGoogle Scholar
  9. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, Feyereisen R, Oakeshott JG (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15(5):615–636CrossRefGoogle Scholar
  10. Committee on the Status of Pollinators in North America NRC, (2007) Status of Pollinators in North America. National Academies Press, Washington, DCGoogle Scholar
  11. Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:693–702CrossRefGoogle Scholar
  12. Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20(1):149–157CrossRefGoogle Scholar
  13. Cresswell JE, Laycock I (2011) Towards the comparative ecotoxicology of bees: the response–response relationship. In: 11th International symposium of the ICP-BR Bee Protection Group, Wageningen, 2–4 November 2011Google Scholar
  14. Cresswell JE, Page CJ, Uygun MB, Holmbergh M, Li YR, Wheeler JG, Laycock I, Pook CJ, de Ibarra NH, Smirnoff N, Tyler CR (2012) Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology 115(6):365–371CrossRefGoogle Scholar
  15. Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, Cluzeau S, Pham-Delegue MH (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Contam Toxicol 48(2):242–250CrossRefGoogle Scholar
  16. Devillers J, Decourtye A, Budzinski H, Pham-Delegue 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):389–403CrossRefGoogle Scholar
  17. EFSA (2010) Application of systematic review methodology to food and feed safety assessments to support decision making. EFSA J 8(6):1637Google Scholar
  18. EFSA (2012) Scientific opinion on the science behind the development of a risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J 10(5):2668Google Scholar
  19. EPPO/OEPP (2010) PP 3/10 (3): chapter 10: honeybees. EPPO Bull 40(3):323–331Google Scholar
  20. European Commission (2002) SANCO/10329/2002 Rev 2 guidance document on terrestrial ecotoxicology under Council Directive 91/414/EECGoogle Scholar
  21. Gallai N, Salles JM, Settele J, Vaissiere BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68(3):810–821CrossRefGoogle Scholar
  22. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhoffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipolito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlof M, Seymour CL, Schuepp C, Szentgyorgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339(6127):1608–1611CrossRefGoogle Scholar
  23. Hardstone MC, Scott JG (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag Sci 66(11):1171–1180CrossRefGoogle Scholar
  24. Helson BV, Barber KN, Kingsbury PD (1994) Laboratory toxicology of 6 forestry insecticides to 4 species of bee (Hymenoptera, Apoidea). Arch Environ Contam Toxicol 27(1):107–114CrossRefGoogle Scholar
  25. 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):348–350CrossRefGoogle Scholar
  26. Johansen CA (1972) Toxicity of field-weathered insecticide residues to four kinds of bees. Environ Entomol 1(3):393–394Google Scholar
  27. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 274(1608):303–313CrossRefGoogle Scholar
  28. Kwak MM, Velterop O, van Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1(1):37–54CrossRefGoogle Scholar
  29. Ladurner E, Bosch J, Maini S, Kemp WP (2003) A method to feed individual bees (Hymenoptera: Apiformes) known amount of pesticides. Apidologie 34:594–602CrossRefGoogle Scholar
  30. 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(7):1937–1945CrossRefGoogle Scholar
  31. Maini S, Medrzycki P, Porrini C (2010) The puzzle of honey bee losses: a brief review. Bull Insectology 63(1):153–160Google Scholar
  32. Matsumoto T (2013) Reduction in homing flights in the honey bee Apis mellifera after a sublethal dose of neonicotinoid insecticides. Bull Insectology 66(1):1–9Google Scholar
  33. Michener CD (2007) The bees of the world, 2nd edn. The John Hopkins University Press, BaltimoreGoogle Scholar
  34. Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G (2010) Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19(1):207–215CrossRefGoogle Scholar
  35. Neumann P, Carreck NL (2010) Honey bee colony losses. J Apic Res 49(1):1–6CrossRefGoogle Scholar
  36. Porrini C, Sabatini AG, Girotti S, Fini F, Monaco L, Celli G, Bortolotti L, Ghini S (2003) The death of honey bees and environmental pollution by pesticides: the honey bees as biological indicators. Bull Insectology 56(1):147–152Google Scholar
  37. Potts SG, Roberts SPM, Dean R, Marris G, Brown MA, Jones R, Neumann P, Settele J (2010) Declines of managed honey bees and beekeepers in Europe. J Apic Res 49(1):15–22CrossRefGoogle Scholar
  38. Regulation (EC) 544/2011. Commission Regulation (EU) No 544/2011 of June 2011 implementing Regulation (EC) No 1107/2009 of the European Parliament and of the Council as regards to the data requirements for active substancesGoogle Scholar
  39. Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7(1):e30023CrossRefGoogle Scholar
  40. Scott-Dupree CD, Conroy L, Harris CR (2009) Impact of currently used or potentially useful insecticides for canola agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae). J Econ Entomol 102(1):177–182CrossRefGoogle Scholar
  41. Tasei JN (2002) Impact of agrochemicals on non-Apis bees. Honey bees: estimating the environmental impact of chemicals. Taylor & Francis, LondonGoogle Scholar
  42. Thompson HM (2001) Assessing the exposure and toxicity of pesticides to bumblebees (Bombus sp.). Apidologie 32(4):305–321CrossRefGoogle Scholar
  43. Thompson HM, Hunt LV (1999) Extrapolating from honeybees to bumblebees in pesticide risk assessment. Ecotoxicology 8(3):147–166CrossRefGoogle Scholar
  44. van der Steen JJM (1994) Method development for the determination of the contact LD 50 of pesticides for bumble bees (Bombus terrestris L.). Apidologie 25(5):463–465Google Scholar
  45. Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336(6079):351–352CrossRefGoogle Scholar
  46. Williams IH (1994) The dependence of crop production within the European Union on pollination by honey bees. Agric Sci Rev 6:229–257Google Scholar
  47. Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10(11):1105–1113CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Pesticides UnitEuropean Food Safety Authority (EFSA)ParmaItaly
  2. 2.Dipartimento di Scienze Agrarie, Area EntomologiaUniversità di BolognaBolognaItaly
  3. 3.Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Unità di Ricerca in Apicoltura e Bachicoltura (CRA-API)BolognaItaly

Personalised recommendations