A meta-analysis comparing the sensitivity of bees to pesticides
- 2.7k Downloads
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.
KeywordsToxicity Environmental risk assessment Apis mellifera Apiformes Pollinators Comparative ecotoxicology
We are very grateful to the EFSA Bee Working group (Robert Luttik, Franz Streissl, Csaba Szentes, Agnes Rortais, Gèrard Arnold, Jos Boesten, Mark Clook, Jacoba Wassenberg) for their comments and suggestions and to Stephanie Bopp and Sotirios Vasileiadis for reviewing part of the manuscript. We very much appreciate the constructive and helpful comments of Rachel Sharp (EFSA) and the three anonymous reviewers.
The publication was drafted under the sole responsibility of the authors and is not considered as an EFSA output. The positions and opinions presented are those of the authors alone and are not intended to represent the views of EFSA.
Conflict of interest
The authors declare that they have no conflict of interest.
- 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
- 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
- Committee on the Status of Pollinators in North America NRC, (2007) Status of Pollinators in North America. National Academies Press, Washington, DCGoogle Scholar
- 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
- EFSA (2010) Application of systematic review methodology to food and feed safety assessments to support decision making. EFSA J 8(6):1637Google Scholar
- 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
- EPPO/OEPP (2010) PP 3/10 (3): chapter 10: honeybees. EPPO Bull 40(3):323–331Google Scholar
- European Commission (2002) SANCO/10329/2002 Rev 2 guidance document on terrestrial ecotoxicology under Council Directive 91/414/EECGoogle Scholar
- 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
- Johansen CA (1972) Toxicity of field-weathered insecticide residues to four kinds of bees. Environ Entomol 1(3):393–394Google Scholar
- Maini S, Medrzycki P, Porrini C (2010) The puzzle of honey bee losses: a brief review. Bull Insectology 63(1):153–160Google Scholar
- 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
- Michener CD (2007) The bees of the world, 2nd edn. The John Hopkins University Press, BaltimoreGoogle Scholar
- 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
- 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
- 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
- Tasei JN (2002) Impact of agrochemicals on non-Apis bees. Honey bees: estimating the environmental impact of chemicals. Taylor & Francis, LondonGoogle Scholar
- 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
- Williams IH (1994) The dependence of crop production within the European Union on pollination by honey bees. Agric Sci Rev 6:229–257Google Scholar