Risk assessment of pesticides and other stressors in bees: Principles, data gaps and perspectives from the European Food Safety Authority

Science of the Total Environment

Volumn 587-588, Issue , 2017, Pages 524-537

  Rortais, Agnès ^a   Arnold, Gérard ^b   Dorne, Jean Lou ^a   More, Simon J ^c   Sperandio, Giorgio ^d   Streissl, Franz ^a   Szentes, Csaba ^a   Verdonck, Frank ^a  

^a EUROPEAN FOOD SAFETY AUTHORITY   (Italy)

^b CNRS   (France)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Data collection; Honeybee colony health; Indicator; Modelling; Multiple stressors; Research needs

Indexed keywords

BIOHAZARDS; CHEMICAL ANALYSIS; CHEMICAL CONTAMINATION; DATA ACQUISITION; FOOD SAFETY; INDICATORS (INSTRUMENTS); MODELS; PESTICIDES; PLANTS (BOTANY); UNCERTAINTY ANALYSIS;

DATA COLLECTION; EUROPEAN FOOD SAFETY AUTHORITIES; HONEYBEE COLONIES; INVASIVE ALIEN SPECIES; MULTIPLE STRESSORS; PESTICIDE RISK ASSESSMENT; PLANT PROTECTION PRODUCTS; RESEARCH NEEDS;

RISK ASSESSMENT;

PESTICIDE;

BEE; COLONY; ENVIRONMENTAL INDICATOR; ENVIRONMENTAL STRESS; HOLISTIC APPROACH; MODEL VALIDATION; PESTICIDE; RISK ASSESSMENT; SURVIVAL;

ADULT; AETHINA TUMIDA; ARTICLE; BEETLE; CONTROLLED STUDY; ENVIRONMENTAL MANAGEMENT; LANDSCAPE; LIMIT OF DETECTION; LIMIT OF QUANTITATION; MEASUREMENT ACCURACY; MEASUREMENT PRECISION; NONHUMAN; RISK ASSESSMENT; VALIDATION PROCESS; VESPA; VESPA VELUTINA; ANALYSIS; ANIMAL; BEE; EUROPEAN UNION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; POLLUTANT;

AETHINA TUMIDA; APIS MELLIFERA; APOIDEA; VESPA VELUTINA;

ANIMALS; BEES; ENVIRONMENTAL POLLUTANTS; EUROPEAN UNION; PESTICIDES; RISK ASSESSMENT; STRESS, PHYSIOLOGICAL;

EID: 85028274079     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2016.09.127     Document Type: Article

References (144)

1. Alaux, C., Brunet, J.L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., Brillard, J., Belzunces, L.P., Le Conte, Y., Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12:3 (2010), 774–782, 10.1111/j.1462-2920.2009.02123.x.
2. Alaux, C., Dantec, C., Parrinello, H., Le Conte, Y., Nutrigenomics in honeybees: digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees. BMC Genomics, 12(1), 2011, 496, 10.1186/1471-2164-12-496.
3. ANSES (Agence Nationale de Sécurité Sanitaire Alimentation, Environnement, Travail), Co-exposition des abeilles aux facteurs de stress. Avis de l'ANSES Saisine n° 2012-SA-0176. Rapport d'expertise collective, 2015 (252 pp.).
4. Arca, M., Papachristoforou, A., Mougel, F., Rortais, A., Monceau, K., Bonnard, O., Tardy, P., Thiéry, D., Silvain, J.-F., Arnold, G., Defensive behaviour of Apis mellifera against Vespa velutina in France: testing whether European honeybees can develop an effective collective defence against a new predator. Behav. Process. 106 (2014), 122–129, 10.1016/j.beproc.2014.05.002.
5. Arena, M., Sgolastra, F., A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23:3 (2014), 324–334, 10.1007/s10646-014-1190-1.
6. Barbet-Massin, M., Rome, Q., Muller, F., Perrard, A., Villemant, C., Jiguet, F., Climate change increases the risk of invasion by the yellow-legged hornet. Biol. Conserv. 157 (2013), 4–10, 10.1016/j.biocon.2012.09.015.
7. Becher, M.A., Osborne, J.L., Thorbek, P., Kennedy, P.J., Grimm, V., Review: towards a system approach for understanding honeybee decline: a stocktaking and synthesis of existing models. J. Appl. Ecol. 50:4 (2013), 868–880, 10.1111/1365-2664.12112.
8. Becher, M.A., Grimm, V., Thorbek, P., Horn, J., Kennedy, P.J., Osborne, J.L., BEEHAVE: a systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure. J. Appl. Ecol. 51:2 (2014), 470–482, 10.1111/1365-2664.12222.
9. Beggs, J.R., Brockerhoff, E.G., Corley, J.C., Kenis, M., Masciocchi, M., Muller, F., Rome, Q., Villemant, C., Ecological effects and management of invasive alien Vespidae. BioControl 56:4 (2011), 505–526, 10.1007/s10526-011-9389-z.
10. Biddinger, D.J., Robertson, J.L., Mullin, C., Frazier, J., Ashcraft, S.A., Rajotte, E.G., Joshi, N.K., Vaughn, M., Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS One, 8(9), 2013, e72587, 10.1371/journal.pone.0072587.
11. Boncristiani, H., Underwood, R., Schwarz, R., Evans, J.D., Pettis, J., Direct effect of acaricides on pathogen loads and gene expression levels in honeybees Apis mellifera. J. Insect Physiol. 58:5 (2012), 613–620, 10.1016/j.jinsphys.2011.12.011.
12. Botías, C., David, A., Horwood, J., Abdul-Sada, A., Nicholls, E., Hill, E., Goulson, D., Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environ. Sci. Technol. 49:21 (2015), 12731–12740, 10.1021/acs.est.5b03459.
13. Chauzat, M.P., Laurent, M., Rivière, M.P., Saugeon, C., Hendrikx, P., Ribiere-Chabert, M., A pan-European epidemiological study on honeybee colony losses 2012–2013. 32 pp. Available online: http://ec.europa.eu/food/animals/live_animals/bees/docs/bee-report_en.pdf, 2014 (accessed 13.09.2016).
14. Claudianos, C., Ranson, H., Johnson, R.M., Biswas, S., Schuler, M.A., Berenbaum, M.R., Feyereisen, R., Oakeshott, J.G., A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol. Biol. 15:5 (2006), 615–636, 10.1111/j.1365-2583.2006.00672.x.
15. Colin, M., Belzunces, L., Evidence of synergy between prochloraz and deltamethrin in Apis mellifera L.: a convenient biological approach. Pestic. Sci. 36:2 (1992), 115–119, 10.1002/ps.2780360206.
16. Couto, A., Lapeyre, B., Thiéry, D., Sandoz, J.C., Olfactory pathway of the hornet Vespa velutina: new insights into the evolution of the hymenopteran antennal lobe. J. Comp. Neurol. 524:11 (2016), 2335–2359, 10.1002/cne.23975.
17. Crailsheim, K., Schneider, L.H.W., Hrassnigg, N., Buhlmann, G., Brosch, U., Gmeinbauer, R., Schoffmann, B., Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. J. Insect Physiol. 38:6 (1992), 409–419, 10.1016/0022-1910(92)90117-v.
18. Cresswell, J.E., A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honeybees. Ecotoxicology 20:1 (2011), 149–157, 10.1007/s10646-010-0566-0.
19. Cuthbertson, A.G., Wakefield, M.E., Powell, M.E., Marris, G., Anderson, H., Budge, G.E., Mathers, J.J., Blackburn, L.F., Brown, M.A., The small hive beetle Aethina tumida: a review of its biology and control measures. Curr. Zool. 59:5 (2013), 644–653, 10.1093/czoolo/59.5.644.
20. Devillers, J., silico bees. 2014, CRC Press, Taylor and Francis Group Ed. (292 pp.).
21. Devos, Y., Gaugitsch, H., Gray, A.J., Maltby, L., Martin, J., Pettis, J.S., Romeis, J., Rortais, A., Schoonjans, R., Smith, J., Streissl, F., Suter, G.W. II, Special issue: advancing environmental risk assessment of regulated products under EFSA's remit. EFSA J., 14(S1), 2016, s0508, 10.2903/j.efsa.2016.s0508 (14 pp.).
22. EC (European Commission), Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 Laying Down the General Principles and Requirements of Food Law, Establishing the European Food Safety Authority and Laying Down Procedures in Matters of Food Safety. OJ L 31/1, 01.02.2002. 2002, 1–24.
23. EC (European Commission), Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 Concerning the Placing of Plant Protection Products on the Market and Repealing Council Directives 79/117/EEC and 91/414/EEC. OJ L 309/1, 24.11.2009. 2009, 1–50.
24. EC (European Commission), Commission Regulation (EU) No 415/2013 of 6 May 2013 Laying Down Additional Responsibilities and Tasks for the EU Reference Laboratories for Rabies, Bovine Tuberculosis and Bee Health, Amending Regulation (EC) No 737/2008 and Repealing Regulation (EU) No 87/2011. 2013.
25. EC (European Commission), Evaluation of Measures for the Beekeeping Sector. Framework Contract No 30-CE-0219319/00-20. 2013 (170 pp.).
26. EC (European Commission), Regulation (EU) No 1308/2013 of the European Parliament and of the Council of 17 December 2013 Establishing a Common Organisation of the Markets in Agricultural Products and Repealing Council Regulations (EEC) No 922/72, (EEC) No 234/79, (EC) No 1037/2001 and (EC) No 1234/2007. OJ L 317, 01.11.2014. 2013 (35 pp.).
27. EC (European Commission), Commission Delegated Regulation (EU) 2015/1366 of 11 May 2015 Supplementing Regulation (EU) No 1308/2013 of the European Parliament and of the Council with Regard to Aid in the Apiculture Sector. OJ L 211, 8.8.2015. 2015, 3–6.
28. EC (European Commission), Commission implementing Regulation (EU) 2016/1141 of 13 July 2016 Adopting a List of Invasive Alien Species of Union Concern Pursuant to Regulation (EU) No 1143/2014 of the European Parliament and of the Council. OJ L 317, 4.11.2014. 2016 (35 pp.).
29. EFSA (European Food Safety Authority), Bee mortality and bee surveillance in Europe—a report from the Assessment Methodology Unit in response to Agence Francaise de Sécurité Alimentaire des Aliments (AFSSA). EFSA J. 154 (2008), 1–28, 10.2903/j.efsa.2008.154r.
30. EFSA (European Food Safety Authority), Inventory of EFSA's Activities on Bees. Supporting Publications 2012;EN-358. 2012 (89 pp.).
31. EFSA (European Food Safety Authority), Towards holistic approaches to the risk assessment of multiple stressors in bees. Summary Report of the EFSA Scientific Colloquium XVIII, Parma, Italy, 2013 (76 pp.).
32. EFSA (European Food Safety Authority), EFSA Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J., 11(7), 2013, 3295, 10.2903/j.efsa.2013.3295 (268 pp.).
33. EFSA (European Food Safety Authority), International framework dealing with human risk assessment of combined exposure to multiple chemicals. EFSA J., 11(7), 2013, 3313, 10.2903/j.efsa.2013.3313EFSA (69 pp.).
34. EFSA (European Food Safety Authority), Towards an integrated environmental risk assessment of multiple stressors on bees: review of research projects in Europe, knowledge gaps and recommendations. EFSA J., 12(3), 2014, 3594, 10.2903/j.efsa.2014.3594 (102 pp.).
35. EFSA (European Food Safety Authority), A Small Application Developed in R for the Estimation of the Residue Intake Rate for Certain Bee Species under Given Conditions: The SHVAL Tool. EFSA Supporting Publication 2014;EN-623. 2014 (15 pp.).
36. EFSA (European Food Safety Authority), The 2013 European Union report on pesticide residues in food. EFSA J., 13(3), 2015, 4038, 10.2903/j.efsa.2015.4038 (169 pp.).
37. EFSA (European Food Safety Authority), EFSA Strategy 2020 Trusted Science for Safe Food. 2015, 10.2805/397609 (Available online: http://www.efsa.europa.eu/en/corporate/pub/strategy2020 (accessed 13.09.2016)).
38. EFSA (European Food Safety Authority), Small hive beetle diagnosis and risk management options. EFSA J., 13(3)), 2015, 4048, 10.2903/j.efsa.2015.4048.
39. EFSA (European Food Safety Authority), Survival, spread and establishment of the small hive beetle (Aethina tumida). EFSA J., 13(12), 2015, 4328, 10.2903/j.efsa.2015.4328.
40. EFSA (European Food Safety Authority), A Mechanistic Model to Assess Risks to Honeybee Colonies from Exposure to Pesticides Under Different Scenarios of Combined Stressors and Factors. EFSA Supporting Publication 2016:EN-1069. 2016, 10.2903/sp.efsa.2016.EN-1069 (116 pp.).
41. EFSA (European Food Safety Authority), Workshop “The health Status of a Managed Honeybee Colony”. EFSA Supporting Publication 2016:EN-1055. 2016 (14 pp.).
42. EFSA (European Food Safety Authority) and EC DG-AGRI (European Commission's Directorate General for Agriculture and Rural Development), EU Scientific Workshop on Bee Health and Sustainable Pollination. EFSA Supporting Publication 2016:EN-1026. 2016 (75 pp.).
43. EFSA Panel on Animal Health and Welfare (AHAW), Scientific opinion on the risk of entry of Aethina tumida and Tropilaelaps spp. in the EU. EFSA J., 11(3), 2013, 3128, 10.2903/j.efsa.2013.3128 (127 pp.).
44. EFSA AHAW Panel, (EFSA Panel on Animal Health and Welfare), 2016. Assessing the health status of managed honeybee colonies (HEALTHY-B): a toolbox to facilitate harmonised data collection. EFSA J., 14(10), 2016, 4578, 10.2903/j.efsa.2016.4578 (246 pp.).
45. EFSA Panel on Plant Protection Products and their Residues (PPR), Scientific opinion of the Panel on Plant Protection Products and their Residues on a request from EFSA on the development of specific protection goal options for environmental risk assessment of pesticides, in particular in relation to the revision of the Guidance Documents on Aquatic and Terrestrial Ecotoxicology (SANCO/3268/2001 and SANCO/10329/2002). EFSA J., 8(10), 2010, 1821, 10.2903/j.efsa.2010.1821 (55 pp.).
46. EFSA Panel on Plant Protection Products and their Residues (PPR), 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), 2012, 2668, 10.2903/j.efsa.2012.2668 (275 pp.).
47. EFSA Panel on Plant Protection Products and their Residues (PPR), Scientific opinion on good modelling practice in the context of mechanistic effect models for risk assessment of plant protection products. EFSA J., 12(3), 2014, 3589, 10.2903/j.efsa.2014.3589 (92 pp.).
48. EFSA Panel on Plant Protection Products and their Residues (PPR), Statement on the suitability of the BEEHAVE model for its potential use in a regulatory context and for the risk assessment of multiple stressors in honeybees at the landscape level. EFSA J., 13(6), 2015, 4125.
49. EFSA Panel of the Scientific Committee (SC), Use of the benchmark dose approach in risk assessment. Guidance of the Scientific Committee. EFSA J. 1150 (2009), 1–72, 10.2903/j.efsa.2009.115.
50. EFSA Panel of the Scientific Committee (SC), Scientific report on principles and process for dealing with data and evidence in scientific assessments. EFSA J., 13(5), 2015, 4121, 10.2903/j.efsa.2015.4121 (35 pp.).
51. EFSA Panel of the Scientific Committee (SC), Guidance to develop specific protection goals options for environmental risk assessment at EFSA, in relation to biodiversity and ecosystem services. EFSA J., 14(6), 2016, 4499, 10.2903/j.efsa.2016.4499 (50 pp.).
52. EFSA Panel of the Scientific Committee (SC), Scientific opinion on coverage of endangered species in environmental risk assessments at EFSA. EFSA J., 14(2), 2016, 4312, 10.2903/j.efsa.2016.4312 (124 pp.).
53. FAO (Food Agriculture Organization)/WHO (World Health Organization), Codex Alimentarius Commission Procedural Manual. Rome, Food and Agriculture Organization of the United Nations, Codex Alimentarius Commission, 18th ed., 2008 ( ftp://ftp.fao.org/codex/Publications/ProcManuals/).
54. FAOSTAT, Dataset 2013. Available online: http://faostat.fao.org, 2013 (accessed 13.09.2016).
55. Garthwaite, D., Sinclair, C.J., Glass, R., Pote, A., Trevisan, M., Sacchettini, G., Spanoghe, P., Ngoc, K.D., Fevery, D., Machera, K., Charistou, A., Nikolopoulou, D., Aarapaki, N., Tskirakis, A., Gerritsen-Ebben, R., Spaan, S., González, F.E., Stobiecki, S., Śliwiński, W., Stobiecki, T., Hakaite, P., Collection of Pesticide Application Data in View of Performing Environmental Risk Assessments for Pesticides. EFSA Supporting Publication 2015:EN-846. 2015 (246 pp.).
56. Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Buchler, R., Berg, S., Ritter, W., Muhlen, W., Gisder, S., Meixner, M., Liebig, G., Rosenkranz, P., The German bee monitoring project: a long term study to understand periodically high winter losses of honeybee colonies. Apidologie 41:3 (2010), 332–352, 10.1051/apido/2010014.
57. Gilioli, G., Schrader, G., Baker, R.H.A., Ceglarska, E., Kertész, V.K., Lövei, G., Navajas, M., Rossi, V., Tramontini, S., van Lenteren, J.C., Environmental risk assessment for plant pests: a procedure to evaluate their impacts on ecosystem services. Sci. Total Environ. 468 (2014), 475–486, 10.1016/j.scitotenv.2013.08.068.
58. Gregorc, A., Silva-Zacarin, E.C., Carvalho, S.M., Kramberger, D., Teixeira, E.W., Malaspina, O., Effects of Nosema ceranae and thiametoxam in Apis mellifera: a comparative study in Africanized and Carniolan honeybees. Chemosphere 147 (2016), 328–336, 10.1016/j.chemosphere.2015.12.030.
59. Hatjina, F., Papaefthimiou, C., Charistos, L., Dogaroglu, T., Bouga, M., Emmanouil, C., Arnold, G., Sublethal doses of imidacloprid decreased size of hypopharyngeal glands and respiratory rhythm of honeybees in vivo. Apidologie 44:4 (2013), 467–480, 10.1007/s13592-013-0199-4.
60. Hawthorne, D.J., Dively, G.P., Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honeybees. PLoS One, 6(11), 2011, e26796, 10.1371/journal.pone.0026796.
61. Hendrikx, P., Chauzat, M.P., Debin, M., Neuman, P., Fries, I., Ritter, W., Brown, M., Mutinelli, F., Le Conte, Y., Gregorc, A., Bee mortality and bee surveillance in Europe. Scientific Report of EFSA, 2009 (217 pp.).
62. Heylen, K., Gobin, B., Arckens, L., Huybrechts, R., Billen, J., The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera. Apidologie 42:1 (2010), 103–116, 10.1051/apido/2010043.
63. Holmstrup, M., Bindesbøl, A.M., Oostingh, G.J., Duschl, A., Scheil, V., Köhler, H.R., Loureiro, S., Soares, A.M., Ferreira, A.L., Kienle, C., Gerhardt, A., Laskowski, R., Kramarz, P.E., Bayley, M., Svendsen, C., Spurgeon, D.J., Interactions between effects of environmental chemicals and natural stressors: a review. Sci. Total Environ. 408:18 (2010), 3746–3762, 10.1016/j.scitotenv.2009.10.067.
64. Hrassnigg, N., Crailsheim, K., The influence of brood on the pollen consumption of worker bees (Apis mellifera L.). J. Insect Physiol. 44:5 (1998), 393–404, 10.1016/s0022-1910(98)00022-5.
65. IPBES (Intergovernmental Platform on Biodiversity and Ecosystem Services), Summary for policymakers of the assessment report of the Intergovernmental Platform on Biodiversity and Ecosystem Services (IPBES) on pollinators, pollination and food production. Potts, S.G., Imperatriz-Fonseca, V.L., Ngo, H.T., Biesmeijer, J.C., Breeze, T.D., Dicks, L.V., Garibaldi, L.A., Hill, R., Settele, J., Vanbergen, A.J., Aizen, M.A., Cunningham, S.A., Eardley, C., Freitas, B.M., Gallai, N., Kevan, P.G., Kovács-Hostyánszki, A., Kwapong, P.K., Li, J., Li, X., Martins, D.J., Nates-Parra, G., Pettis, J.S., Rader, R., Viana, B.F., (eds.) Secretariat of the Intergovernmental Science-policy Platform on iodiversity and Ecosystem Services, Bonn, Germany, 2016 (36 pages. Available online: http://www.ipbes.net/sites/default/files/downloads/pdf/SPM_Deliverable_3a_Pollination.pdf (accessed 13.09.2016)).
66. Jacques, A., Laurent, M., Ribiere-Chabert, M., Saussac, M., Bougeard, S., Hendrikx, P., Chauzat, M.P., Statistical Analysis on the EPILOBEE Dataset: Explanatory Variables Related to Honeybee Colony Mortality in EU During a 2 year Survey. External Supporting Publication 2016:EN-883. 2016, 10.2903/sp.efsa.2016.EN-883 (328 pp.).
67. Joachimsmeier, I., Pistorius, J., Heimbach, U., Schenke, D., Zwerger, P., Kirchner, W., Details on occurrence and frequency of guttation in different crops in Germany. Poster Presentation on the 11th ICPBR Symposium Hazards of Pesticides to Bees, Wageningen, The Netherlands, 2011.
68. Johnson, R.M., Pollock, H.S., Berenbaum, M.R., Synergistic interactions between in-hive miticides in Apis mellifera. J. Econ. Entomol. 102 (2009), 474–479, 10.1603/029.102.0202.
69. Johnson, R.M., Mao, W., Pollock, H.S., Niu, G., Schuler, M.A., Berenbaum, M.R., Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLoS One, 7(2), 2012, e31051, 10.1371/journal.pone.003105.
70. Johnson, R.M., Dahlgren, L., Siegfried, B.D., Ellis, M.D., Acaricide, fungicide and drug interactions in honeybees (Apis mellifera). PLoS One, 8(1), 2013, e54092, 10.1371/journal.pone.0054092.
71. Johnson, R.M., Honeybee toxicology. Annu. Rev. Entomol. 60:1 (2015), 415–434, 10.1146/annurev-ento-011613-162005.
72. Ken, T., Hepburn, H.R., Radloff, S.E., Yusheng, Y., Yiqiu, L., Danyin, Z., Neumann, P., Heat-balling wasps by honeybees. Naturwissenschaften 92:10 (2005), 492–495, 10.1007/s00114-005-0026-5.
73. Khoury, D.S., Myerscough, M.R., Barron, A.B., A quantitative model of honeybee colony population dynamics. PLoS One, 6(4), 2011, e18491, 10.1371/journal.pone.0018491.
74. Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T., Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274:1608 (2007), 303–313, 10.1098/rspb.2006.3721.
75. Laurent, M., Hendrikx, P., Ribiere-Chabert, M., Chauzat, M.P., A pan-European epidemiological study on honeybee colony losses 2012–2014. 44 pp. Available online: http://ec.europa.eu/food/animals/live_animals/bees/docs/beereport_2012_2014_en.pd, 2015 (accessed 13.09.2016).
76. Lodesani, M., Medrzycki, P., Bortolotti, L., Project “APENET”: monitoring and research in apiculture. 11th International Symposium of the ICP-BR Bee Protection Group, Wageningen (The Netherlands), November 2–4, 2011 Julius-Kühn-Archiv, 437, 2012.
77. Long, E.Y., Krupke, C.H., Non-cultivated plants present a season-long route of pesticide exposure for honeybees. Nat. Commun., 7, 2016, 11629, 10.1038/ncomms11629.
78. Luck, G.W., Daily, G.C., Ehrlich, P.R., Population diversity and ecosystem services. Trends Ecol. Evol. 18:7 (2003), 331–336, 10.1016/S0169-5347(03)00100-9.
79. Mao, W., Schuler, M.A., Berenbaum, M.R., CYP9Q-mediated detoxification of acaricides in the honeybee (Apis mellifera). Proc. Natl. Acad. Sci. U. S. A. 108:31 (2011), 12657–12662, 10.1073/pnas.1109535108.
80. Maurizio, A., Pollen: its composition, collection, utilization and identification. Bee World 35:3 (1954), 49–50.
81. Milanesio, D., Saccani, M., Maggiora, R., Laurino, D., Porporato, M., Design of an harmonic radar for the tracking of the Asian yellow-legged hornet. Ecol. Evol. 6:7 (2016), 2170–2178, 10.1002/ece3.2011.
82. Monceau, K., Thiéry, D., Vespa velutina nest distribution at a local scale: an 8-year survey of the invasive honeybee predator. Instr. Sci., 2016, 10.1111/1744–7917.12331.
83. Monceau, K., Bonnard, O., Thiéry, D., Vespa velutina: a new invasive predator of honeybees in Europe. J. Pest. Sci. 87:1 (2014), 1–16, 10.1007/s10340-013-0537-3.
84. Moran, N.A., Genomics of the honeybee microbiome. Curr. Opin. Insect Sci. 10 (2015), 22–28, 10.1016/j.cois.2015.04.003.
85. Munns, W.R. Jr., Assessing risks to wildlife populations from multiple stressors: overview of the problem and research needs. Ecol. Soc., 11(1), 2006, 23.
86. Mutinelli, F., Montarsi, F., Federico, G., Granato, A., Ponti, A.M., Grandinetti, G., Ferre, N., Franco, S., Duquesnes, V., Riviere, M.P., Thiery, R., Henrikx, P., Ribiere-Chabert, M., Chauzat, M.P., Detection of Aethina tumida Murray (Coleoptera: Nitidulidae.) in Italy: outbreaks and early reaction measures. J. Apic. Res. 53:5 (2014), 569–575, 10.3896/ibra.1.53.5.13.
87. Negri, I., Jablonka, E., Editorial: epigenetics as a deep intimate dialogue between host and symbionts. Front. Genet., 7, 2016, 7, 10.3389/fgene.2016.0000.
88. Negri, I., Mavris, C., Di Prisco, G., Caprio, E., Pellecchia, M., Honeybees (Apis mellifera, L.) as active samplers of airborne particulate matter. PLoS One, 10(7), 2015, e0132491, 10.1371/journal.pone.0132491.
89. Nienstedt, K.M., Brock, T.C.M., van Wensem, J., Montforts, M., Hart, A., Aagaard, A., Alix, A., Boesten, J., Bopp, S.K., Brown, C., Capri, E., Forbes, V., Kopp, H., Liess, M., Luttik, R., Maltby, L., Sousa, J.P., Streissl, F., Hardy, A.R., Development of a framework based on an ecosystem services approach for deriving specific protection goals for environmental risk assessment of pesticides. Sci. Total Environ. 415 (2011), 31–38, 10.1016/j.scitotenv.2011.05.057.
90. NRC (National Research Council), Status of Pollinators in North America. 2007, The National Academies Press, Washington, DC, USA (322 pp.).
91. Odoux, J., Aupinel, P., Gateff, S., Requier, F., Henry, M., Bretagnolle, V., ECOBEE: a tool for long-term honeybee colony monitoring at the landscape scale in West European intensive agroecosystems. J. Apic. Res. 53:1 (2014), 57–66, 10.3896/ibra.1.53.1.05.
92. OECD (Organization for Economic Cooperation and Development), Guidance for the testing of chemicals. Honeybees Acute Oral Toxicty test Test Guidelines 213, 1998.
93. OECD (Organization for Economic Cooperation and Development), Guidance for the testing of chemicals. Honeybees Acute Contact Toxicity Test Test Guidelines 214, 1998.
94. OECD (Organization for Economic Cooperation and Development), Test no. 237: honeybee larval toxicity test, single exposure. OECD Guidelines for the Testing of Chemicals, Section 2, 2013, OECD Publishing, Paris, 10.1787/9789264203723-en.
95. OECD (Organization for Economic Cooperation and Development), Draft TG: HoneyBee (Apis mellifera) Chronic Oral Toxicity Test 10 day Feeding Test in the Laboratory. Draft Guideline February 2016. 2016.
96. OEPP/EPPO (European and Mediterranean Plant Protection Organization), PP 1/170 (4): Side-effects on honeybees. EPPO Bull. 40 (2010), 313–319.
97. OEPP/EPPO (European and Mediterranean Plant Protection Organization), PP 3/10 (3). Environmental Risk Assessment Scheme for Plant Protection Products. (Chapter 10: honeybees), 2010, 323–331.
98. Palmeri, V., Scirtὸ, G., Malacrinὸ, A., Laudani, F., Campolo, O., A Scientific Note on A New Pest for European Honeybees: First Report of Small Hive Beetle Aethina tumida, (Coleoptera: Nitidulidae) in Italy, 46(4), 2015, Apidologie, Springer Verlag, 527–529, 10.1007/s13592-014-0343-9.
99. Papachristoforou, A., Rortais, A., Zafeiridou, G., Theophylidis, G., Garnery, L., Thrasyvoulou, A., Arnold, G., Smothered to death: hornets asphyxiated by honeybees. Curr. Biol. 17:18 (2007), R795–R796, 10.1016/j.cub.2007.07.033.
100. Papachristoforou, A., Rortais, A., Sueur, J., Arnold, G., Attack or retreat: contrasted defensive tactics used by Cyprian honeybee colonies under attack from hornets. Behav. Process. 86:2 (2011), 236–241, 10.1016/j.beproc.2010.12.012.
101. PCN (Pest Control News), Asian hornet identified for the first time in the Channel Islands. 12 July 2016. Available online: https://www.pestcontrolnews.com/asian-hornet-identified-first-time-alderney-channel-islands/, 2016 (accessed 13.09.2016).
102. Penev, D., European bee week: what the EU should do for bees and biodiversity. Available online: http://www.euractiv.com/section/agriculturefood/opinion/european-bee-week-what-the-eu-should-do-for-bees-and-biodiversity/, 2016 (accessed 13.09.2016).
103. Pettis, J.S., Lichtenberg, E.M., Andree, M., Stitzinger, J., Rose, R., Crop pollination exposes honeybees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS One, 8(7), 2013, e70182, 10.1371/journal.pone.0070182.
104. Pistorius, J., Brobyn, T., Lorsch, J.A., Suzuki, H., Maus, C., Lückmann, J., Wallner, K., Campbell, P., Forster, R., Morellau, F., Presentation of the ICPBR Working group on assessment of risks posed by guttation. Oral Presentation on the 11th ICPBR Symposium Hazards of Pesticides to Bees, Wageningen, The Netherlands, 2011.
105. Pistorius, J., Wallner, K., Joachimsmeier, I., Reetz, J., Schenke, D., von der Ohe, W., Illies, I., Review on activities in Germany to assess the occurrence, residues and possible risk of guttation for honeybees. Poster Presentation on the 11th ICPBR Symposium Hazards of Pesticides to Bees, Wageningen, The Netherlands, 2011.
106. Porrini, C., Lodesani, M., Libertà, A., Bortolotti, L., Gallina, A., Colombo, R., Sgolastra, F., Medrzycki, P., Bozza, M., Mutinelli, F., BeeNet: Italian beekeeping monitoring network. Proceedings of the XXXXIII Apimondia International Congress, 29 Sept.–4 Oct. 2013, Kiev, Ukraine, 2013.
107. Posthuma, L., Suter, G.W., Traas, T.P., Species Sensitivity Distributions in Ecotoxicology. 2002, CRC Press Taylor & Francis Group (616 pp.).
108. Quignot, N., Audrey, G., Amzal, B., Data Collection on Combined Toxicity of Multiple Chemicals for Animal Health and Ecological Risk Assessment. EFSA Supporting Publication 2015:EN-861. 2015 (112 pp.).
109. Reetz, J., Zühlke, S., Spiteller, M., Wallner, K., Neonicotinoid insecticides translocated in guttated droplets of seed-treated maize and wheat: a threat to honeybees?. Apidologie 42:5 (2011), 596–606, 10.1007/s13592-011-0049-1.
110. Renzi, M.T., Rodriguez-Gasol, N., Medrzycki, P., Porrini, C., Martini, A., Burgio, G., Maini, S., Sgolastra, F., Combined effect of pollen quality and thiamethoxam on hypopharyngeal gland development and protein content in Apis mellifera. Apidologie, 2016, 1–10, 10.1007/s13592-016-0435-9.
111. Requier, F., Odoux, J.F., Tamic, T., Moreau, N., Henry, M., Decourtye, A., Bretagnolle, V., Floral resources used by honeybees in agricultural landscapes. The Bull. Ecol. Soc. Am. 96 (2015), 487–491, 10.1890/0012-9623-96.3.487.
112. Robinet, C., Suppo, C., Darrouzet, E., Rapid spread of the invasive yellow-legged hornet in France: the role of human-mediated dispersal and the effects of control measures. J. Appl. Ecol., 2016, 10.1111/1365-2664.12724.
113. Rumkee, J.C., Becher, M.A., Thorbek, P., Kennedy, P.J., Osborne, J.L., Predicting honeybee colony failure: using the BEEHAVE model to simulate colony responses to pesticides. Environ. Sci. Technol. 49:21 (2015), 12879–12887, 10.1021/acs.est.5b03593.
114. SANCO/10329/2002, Guidance Document on Terrestrial Ecotoxicology Under Council Directive 91/414/EEC Rev.2 Final, 17.10.2002. 2002, 1–39.
115. SANCO/10553/2012, Draft Guidance Document for the Authorisation of Plant Protection Products for Seed Treatment (Member States Commenting Phase). (in preparation), 2016.
116. SCHER/SCENIHR/SCC (Scientific Committees on Health and Environmental Risks, on Emerging and Newly Identified Health Risks and on Consumer Safety), Opinion on the Toxicity and Assessment of Chemical Mixtures. 2012, 10.2772/21444 (50 pp. Available online: http://ec.europa.eu/health/scientific_committees/environmental_risks/docs/scher_o_155.pdf (accessed 13.09.2016)).
117. SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks), Memorandum on the use of the scientific literature for human health risk assessment purposes – weighing of evidence and expression of uncertainty. Available online: http://www.ec.europa.eu, 2012 (accessed 13.09.2016).
118. Schenke, D., Joachimsmeier, I., Pistorius, J., Heimbach, U., Pesticides in guttation droplets following seed treatment - preliminary results from greenhouse experiments. Poster Presentation on the SETAC Europe 20th Annual Meeting, Seville, Spain, 2010.
119. Schenke, D., Joachimsmeier, I., Pistorius, J., Heimbach, U., Pesticides in guttation droplets following seed treatment-field studies. Oral Presentation on SETAC North America 32nd Annual Meeting, Boston, MA, 2011.
120. SFS-16-2017, online, Bee Health and Sustainable Pollination “Sustainable Food Security – Resilient and Resource-efficient Value Chains” Work-Programme 2016–2017 of Societal Challenge “Food security, Sustainable Agriculture and Forestry, MARIne and Maritime and Inland Water Research and the Bioeconomy” (SC2). 2017, 37–39 (Available online: https://ec.europa.eu/research/participants/data/ref/h2020/wp/2016_2017/main/h2020-wp1617-food_en.pdf (accessed 13.09.2016)).
121. Smodiš Škerl, M.I., Gregorc, A., Heat shock proteins and cell death in situ localisation in hypopharyngeal glands of honeybee (Apis mellifera carnica) workers after imidacloprid or coumaphos treatment. Apidologie 41:1 (2010), 73–86, 10.1051/apido/2009051.
122. Spurgeon, D., Hesketh, H., Lahive, E., Svendsen, C., Baas, J., Robinson, A., Horton, A., Heard, M., Chronic Oral Lethal and Sub-lethal Toxicities of Different Binary Mixtures of Pesticides and Contaminants in Bees (Apis mellifera, Osmia bicornis and Bombus terrestris). EFSA Supporting Publication 2016:EN-1076. 2016.
123. Steinhauer, N., Rennich, K., Caron, D.M., Delaplane, K., Rangel, J., Rose, R., Sagili, R., Skinner, J., Wilkes, J.T., Wilson, M.E., Pettis, J., van Engelsdorp, D., Colony loss 2015–2016: preliminary results. Available online: http://pnwhoneybeesurvey.com/wp-content/uploads/2016/06/PNW-SURVEY-posting-CanadaUS-Europe-losses.pdf, 2016 (accessed 13.09.2016).
124. Tan, K., Radloff, S.E., Li, J.J., Hepburn, H.R., Yang, M.X., Zhang, L.J., Neumann, P., Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A.mellifera. Naturwissenschaften 94:6 (2007), 469–472, 10.1007/s00114-006-0210-2.
125. Tan, K., Li, H., Yang, M.X., Hepburn, H.R., Radloff, S.E., Wasp hawking induces endothermic heat production in guard bees. J. Insect Sci., 10(1), 2010, 142, 10.1673/031.010.14102.
126. Tan, K., Wang, Z., Li, H., Yang, S., Hu, Z., Kastberger, G., Oldroyd, B.P., An “I see you” prey–predator signal between the Asian honeybee, Apis cerana, and the hornet, Vespa velutina. Anim. Behav. 83:4 (2012), 879–882, 10.1016/j.anbehav.2011.12.031.
127. Tan, K., Yang, M.X., Wang, Z.W., Li, H., Zhang, Z.Y., Radloff, S.E., Hepburn, H.R., Cooperative wasp-killing by mixed-species colonies of honeybees, Apis cerana and Apis mellifera. Apidologie 43:2 (2012), 195–200, 10.1007/s13592-011-0098-5.
128. Tan, K., Wang, Z., Chen, W., Hu, Z., Oldroyd, B.P., The “I see you” prey–predator signal of Apis cerana is innate. Naturwissenschaften 100:3 (2013), 245–248, 10.1007/s00114-013-1019-4.
129. Tapparo, A., Marton, D., Giorio, C., Zanella, A., Soldà, L., Marzaro, M., Vivan, L., Girolami, V., Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seeds. Environ. Sci. Technol. 46:5 (2012), 2592–2599, 10.1021/es2035152.
130. Thompson, H.M., Interaction Between Pesticides and Other Factors in Effects on Bees. Supporting Publications 2012:EN-340. 2012 (204 pp.).
131. Thompson, H.M., Fryday, S.L., Harkin, S., Milner, S., Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie 45:5 (2014), 545–553, 10.1007/s13592-014-0273-6.
132. Thompson, H.M., Extrapolation of acute toxicity across bee species. Integr. Environ. Assess. Manag., 2015, 10.1002/ieam.1737.
133. Thorbek, P., Campbell, P.J., Sweeney, P.J., Thompson, H.M., Using BEEHAVE to explore pesticide protection goals for European honeybee (Apis melifera L.) worker losses at different forage qualities. Environ. Toxicol. Chem., 2016, 10.1002/etc.3504.
134. Topping, C.J., Dalby, L., Skov, F., Landscape structure and management alter the outcome of a pesticide ERA: evaluating impacts of endocrine disruption using the ALMaSS European Brown Hare model. Sci. Total Environ. 541 (2016), 1477–1488, 10.1016/j.scitotenv.2015.10.042.
135. US-EPA (United States Environmental Protection Agency), Guidance for assessing pesticide risks to bees. 54 pp. Available online: https://www.epa.gov/sites/production/files/2014-06/documents/pollinator_risk_assessment_guidance:06_19_14.pdf, 2014 (accessed 13.09.2016).
136. van den Brink, P.J., Baird, D., Baveco, H.J.M., Focks, A., The use of traits-based approaches and eco(toxico)logical models to advance the ecological risk assessment framework for chemicals. Integr. Environ. Assess. Manag. 9:3 (2013), e47–e57, 10.1002/ieam.1443.
137. vanEngelsdorp, D., Tarpy, D.R., Baylis, K., Spivak, M., Caron, D.M., Connell, J., Delaplane, K.S., Donohue, S., Esaias, W., Gross, B., Hayes, J. Jr., Lengerich, E.J., Pettis, J., Rennich, K., Underwood, R., Rose, R., Skinner, J., Wilkes, J., The bee informed partnership: using beekeeper's real-world experience to solve beekeepers’ real-world problems. Am. Entomol. 58:2 (2012), 116–118.
138. Van Gestel, C.A.M., Jonker, M., Kammenga, J.E., Laskowski, R., Svendsen, C., Mixture Toxicity: Linking Approaches from Ecological and Human Toxicology. 2010, SETAC, Pensecola, FL, USA.
139. Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Viguès, B., Brunet, J.L., Texier, C., Biron, D.G., Blot, N., El Aloui, H., Belzunces, L.P., Delbac, F., Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One, 6(6), 2011, e21550, 10.1371/journal.pone.0021550.
140. Villemant, C., Barbet-Massin, M., Perrard, A., Muller, F., Gargominy, O., Jiguet, F., Rome, Q., Predicting the invasion risk by the alien bee-hawking yellow-legged hornet Vespa velutina nigrithorax across Europe and other continents with niche models. Biol. Conserv. 144:9 (2011), 2142–2150, 10.1016/j.biocon.2011.04.009.
141. Villemant, C., Muller, F., Haubois, S., Perrard, A., Darrouzet, E., Rome, Q., Bilan des travaux (MNHN et IRBI) sur l'invasion en France de Vespa velutina, le frelon asiatique prédateur d'abeilles. Barbançon, J.-M., L'Hostis, M., (eds.) Proceedings of the Journée Scientifique Apicole, Arles. ONIRIS-FNOSAD, Nantes, 11 February 2011, 2011, 3–12 (Available online: https://inpn.mnhn.fr/fichesEspece/Vespa_velutina_fichiers/2011_02_11_Bilan_Invasion_Vespa_velutina_JSA.pdf (accessed 13.09.2016)).
142. Wang, M., Reduction of uncertainty and variability in honeybee trials for the ecological risk assessment. Poster 249 (p128). Shaping the future of food safety, together. Proceedings of the 2nd EFSA Scientific Conference. Milan, Italy, 14–16 October 2015. EFSA J., 13(10), 2015, s1310, 10.2903/j.efsa.2015.s1310 (137 pp.).
143. Woodcock, B.A., Heard, M.S., Jitlal, M.S., Rundlöf, M., Bullock, J.M., Shore, R.F., Pywell, R.F., Replication, effect sizes and identifying the biological impacts of pesticides on bees under field conditions. J. Appl. Ecol., 2016, 10.1111/1365-2664.12676.
144. WHO (World Health Organization), Principles and methods for the risk assessment of chemicals in food. Environmental Health Criteria 240 - Annex 1 Glossary of terms, 2009.