A meta-analysis comparing the sensitivity of bees to pesticides

Maria Arena1, Fabio Sgolastra2,3
1Pesticides Unit, European Food Safety Authority (EFSA), Parma, Italy
2Dipartimento di Scienze Agrarie, Area Entomologia, Università di Bologna, Bologna, Italy
3Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Unità di Ricerca in Apicoltura e Bachicoltura (CRA-API), Bologna, Italy

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Ahmad Z, Johansen C (1973) Selective toxicity of carbophenothion and trichlorfon to the honey bee and the alfalfa leafcutting bee. Environ Entomol 2(1):27–30

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):2408–2421

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):623–633

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):351–354

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):973–992

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, Oxford

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):321–331

Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339(6127):1611–1615

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):615–636

Committee on the Status of Pollinators in North America NRC, (2007) Status of Pollinators in North America. National Academies Press, Washington, DC

Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:693–702

Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20(1):149–157

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 2011

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):365–371

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):242–250

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):389–403

EFSA (2010) Application of systematic review methodology to food and feed safety assessments to support decision making. EFSA J 8(6):1637

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):2668

EPPO/OEPP (2010) PP 3/10 (3): chapter 10: honeybees. EPPO Bull 40(3):323–331

European Commission (2002) SANCO/10329/2002 Rev 2 guidance document on terrestrial ecotoxicology under Council Directive 91/414/EEC

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):810–821

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):1608–1611

Hardstone MC, Scott JG (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag Sci 66(11):1171–1180

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):107–114

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):348–350

Johansen CA (1972) Toxicity of field-weathered insecticide residues to four kinds of bees. Environ Entomol 1(3):393–394

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):303–313

Kwak MM, Velterop O, van Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1(1):37–54

Ladurner E, Bosch J, Maini S, Kemp WP (2003) A method to feed individual bees (Hymenoptera: Apiformes) known amount of pesticides. Apidologie 34:594–602

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):1937–1945

Maini S, Medrzycki P, Porrini C (2010) The puzzle of honey bee losses: a brief review. Bull Insectology 63(1):153–160

Matsumoto T (2013) Reduction in homing flights in the honey bee Apis mellifera after a sublethal dose of neonicotinoid insecticides. Bull Insectology 66(1):1–9

Michener CD (2007) The bees of the world, 2nd edn. The John Hopkins University Press, Baltimore

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):207–215

Neumann P, Carreck NL (2010) Honey bee colony losses. J Apic Res 49(1):1–6

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):147–152

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):15–22

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 substances

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):e30023

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):177–182

Tasei JN (2002) Impact of agrochemicals on non-Apis bees. Honey bees: estimating the environmental impact of chemicals. Taylor & Francis, London

Thompson HM (2001) Assessing the exposure and toxicity of pesticides to bumblebees (Bombus sp.). Apidologie 32(4):305–321

Thompson HM, Hunt LV (1999) Extrapolating from honeybees to bumblebees in pesticide risk assessment. Ecotoxicology 8(3):147–166

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):463–465

Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336(6079):351–352

Williams IH (1994) The dependence of crop production within the European Union on pollination by honey bees. Agric Sci Rev 6:229–257

Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10(11):1105–1113