Are honeybees suitable surrogates for use in pesticide risk assessment for non-Apis bees?
Apis mellifera
non-Apis
pesticides
risk assessment
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
Oct 2019
Oct 2019
Historique:
received:
22
03
2019
revised:
13
05
2019
accepted:
21
05
2019
pubmed:
28
5
2019
medline:
18
12
2019
entrez:
25
5
2019
Statut:
ppublish
Résumé
Historically, bee regulatory risk assessment for pesticides has centred on the European honeybee (Apis mellifera), primarily due to its availability and adaptability to laboratory conditions. Recently, there have been efforts to develop a battery of laboratory toxicity tests for a range of non-Apis bee species to directly assess the risk to them. However, it is not clear whether the substantial investment associated with the development and implementation of such routine screening will actually improve the level of protection of non-Apis bees. We argue, using published acute toxicity data from a range of bee species and standard regulatory exposure scenarios, that current first-tier honeybee acute risk assessment schemes utilised by regulatory authorities are protective of other bee species and further tests should be conducted only in cases of concern. We propose similar analysis of alternative exposure scenarios (chronic and developmental) once reliable data for non-Apis bees are available to expand our approach to these scenarios. In addition, we propose that in silico (simulation) approaches can then be used to address population-level effects in more field-realistic scenarios. Such an approach could lead to a protective, but also workable, risk assessment for non-Apis species while contributing to pollination security in agricultural landscapes around the globe. © 2019 Society of Chemical Industry.
Substances chimiques
Pesticides
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2549-2557Informations de copyright
© 2019 Society of Chemical Industry.
Références
Pascual U, Balvanera P, Díaz S, Pataki G, Roth E, Stenseke M et al., Valuing nature's contributions to people: the IPBES approach. Curr Opin Env Sust 26:7-16 (2017).
Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA et al., Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608-1611 (2013).
Grab H, Branstetter MG, Amon N, Urban-Mead KR, Park MG, Gibbs J et al., Agriculturally dominated landscapes reduce bee phylogenetic diversity and pollination services. Science 363:282-284 (2019).
Mathiasson ME and Rehan SM, Status changes in the wild bees of North-Eastern North America over 125 years revealed through museum specimens. Insect Conserv Divers (2019). https://doi.org/10.1111/icad.12347.
Burkle LA, Marlin JC and Knight TM, Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611-1615 (2013).
Carvalheiro LG, Kunin WE, Keil P, Aguirre-Gutierrez J, Ellis WN, Fox R et al., Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett 16:870-878 (2013).
Biesmeijer JC, Roberts SP, Reemer M, Ohlemüller R, Edwards M, Peeters T et al., Parallel declines in pollinators and insect-pollinated plants in Britain and The Netherlands. Science 313:351-354 (2006).
Goulson D, Nicholls E, Botías C and Rotheray EL, Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957 (2015).
Auteri D, Arena M, Barmaz S, Ippolito A, Linguadoca A, Molnar T et al., Neonicotinoids and bees: the case of the European regulatory risk assessment. Sci Total Environ 579:966-971 (2017).
Pisa L, Amaral-Rogers V, Belzunces L, Bonmatin J, Downs C, Goulson D et al., Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68-102 (2014).
IPBES. Summary for policymakers of the assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. In Thematic Assessment of Pollinators, Pollination and Food Production, ed. by Potts S, et al.. Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services: Bonn, pp. 36 (2016).
EFSA, Guidance on the risk assessment of plant protection products on bees ( Apis mellifera, Bombus spp. and solitary bees). EFSA J 11:3295-3295 (2013).
EPPO, Chapter 10: honeybees. EPPO Bull 40:323-331 (2010).
OECD, Test No 213: Honeybees, Acute Oral Toxicity Test. OECD Publishing, Paris (1998).
OECD, Test No. 214: Honey bees, Acute Contact Toxicity Test. OECD Publishing, Paris (1998).
OECD, Test 245: Honey Bee (Apis mellifera) Chronic Oral Toxicity Test (10-Day Feeding). OECD, Paris (2017).
OECD, Guidance Document 239: Honey Bee (Apis mellifera) Larval Toxicity Test. Repeated Exposure. OECD, Paris (2016).
OECD, Test No. 247: Bumblebee, Acute Oral Toxicity Test. OECD, Paris (2017).
OECD, Test No. 246: Bumblebee, Acute Contact Toxicity Test. OECD, Paris (2017).
Handewald N, Exeler N, Kelein O, Knaebe S, Nocelli RCF, Roat T et al., Progress of working group non-Apis testing. Julius-Kuhn Archiv 462:142-145 (2017).
Roessink I, Handewald N, Schnieider C, Exeler N, Schnurr A, Molitor A-M et al., A method for a solitary bee (Osmia sp.) first tier acute contact and oral labortaory test: an update. Julius-Kuhn Archiv 462:158 (2017).
USEPA, Guidance for Assessing Pesticide Risks to Bees (2014). Available: https://www.epa.gov/sites/production/files/2014-06/documents/pollinator_risk_assessment_guidance_06_19_14.pdf [accessed 30 April 2019]
Boyle NK, Cox-Foster DL, Pitts-Singer TL, Abbott J, Alix A, Hinarejos S et al., Workshop on pesticide exposure assessment paradigm for non-Apis bees: foundation and summaries. Environ Entomol 48:4-11 (2018).
KdO C, Rebelo RM, RdP O, Ferro AA, VFEd C, LdO B et al., Manual de avaliação de risco ambiental de agrotóxicos para abelhas. Ibama/Diqua, Brasília (2017).
Michener CD, The Bees of the World. Johns Hopkins University Press, Baltimore, MD (2000).
Arena M and Sgolastra F, A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23:324-334 (2014).
Banks JE, Stark JD, Vargas RI and Ackleh AS, Deconstructing the surrogate species concept: a life history approach to the protection of ecosystem services. Ecol Appl 24:770-778 (2014).
Thompson H, Extrapolation of acute toxicity across bee species. Integr Environ Assess Manage 12:622-626 (2016).
Hardstone MC and Scott JG, Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag Sci 66:1171-1180 (2010).
Couvillon MJ, Jandt J, Duong N and A D, Ontogeny of worker body size distribution in bumble bee (Bombus impatiens) colonies. Ecol Entomol 35:424-435 (2010).
West GB, Brown JH and Enquist BJ, The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284:1677-1679 (1999).
Sample B and Arenal C, Allometric models for interspecies extrapolation of wildlife toxicity data. Bull Environ Contam Toxicol 62:653-663 (1999).
Pamminger T, Hanewald N, Schneider C, Becker R and Bergtold M, Predicting wild bee sensitivity to acetylcholine-esterase (AChE) inhibitors utilizing a trait based & phylogenetically controlled approach, In SETAC Europe 28th Annual Meeting, Rome 2018). https://doi.org/10.13140/rg.2.2.17425.94563 [accessed 30 April 2019]
Kim W, Gilet T and Bush JW, Optimal concentrations in nectar feeding. Proc Natl Acad Sci U S A 108:16618-16621 (2011).
Sadd BM, Barribeau SM, Bloch G, De Graaf DC, Dearden P, Elsik CG et al., The genomes of two key bumblebee species with primitive eusocial organization. Genome Biol 16:76 (2015).
Johnson RM, Comparative toxicogenomics of bees important to agriculture in Ohio, in SEEDS: The OARDC Research Enhancement Competitive Grants Program Report of Progress for Calendar Year. The Ohio State University, Columbus, OH, p. 29 (2013, 2014).
Manjon C, Troczka BJ, Zaworra M, Beadle K, Randall E, Hertlein G et al., Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr Biol 28:e1137 (2018).
Berenbaum MR and Johnson RM, Xenobiotic detoxification pathways in honey bees. Curr Opin Insect Sci 10:51-58 (2015).
Johnson RM, Harpur BA, Dogantzis KA, Zayed A and Berenbaum MR, Genomic footprint of evolution of eusociality in bees: floral food use and CYPome “blooms”. Insectes Soc 65:445-454 (2018).
Beadle K, Singh KS, Troczka BJ, Randall E, Zaworra M, Zimmer CT et al., Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLoS Genet 15:e1007903 (2019).
Tomizawa M and Casida JE, Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247-268 (2005).
Dahlgren L, Johnson R, Siegfried B and Ellis M, Comparative toxicity of Acaricides to honey bee (Hymenoptera: Apidae) workers and Queens. J Econ Entomol 105:1895-1902 (2012).
Hinarejos S, Abbott J, Alix A, Bibek S, Cabrera A, Joseph T et al., Non-Apis bee exposure workshop: industry participants' view. Environ Entomol 48:49-52 (2018).
Uhl P, Awanbor O, Schulz RS and Brühl CA, Osmia bicornis is rarely an adequate regulatory surrogate species. Comparing its acute sensitivity towards multiple insecticides with regulatory Apis mellifera endpoints. bioRxiv 366237 (2018).
Gretenkord C and Drescher W, Effects of four pesticides (Decis, Metasystox, Pirimor, Rubitox) on the bumblebee Bombus terrestris L.: determination of the oral LD50 and preliminary results with semi-field tests. Apidologie 24:519-520 (1993).
Marletto F, Patetta A and Manino A, Laboratory assessment of pesticide toxicity to bumble bees. Bull Insectol 56:155-158 (2003).
EFSA, Conclusion on the peer review of the pesticide risk assessment for bees for the active substance thiamethoxam considering all uses other than seed treatments and granules. EFSA J 13:4212-4282 (2015).
Heard MS, Baas J, Dorne J-L, Lahive E, Robinson AG, Rortais A et al., Comparative toxicity of pesticides and environmental contaminants in bees: are honey bees a useful proxy for wild bee species? Sci Total Environ 578:357-365 (2017).
Sgolastra F, Medrzycki P, Bortolotti L, Renzi MT, Tosi S, Bogo G et al., Synergistic mortality between a neonicotinoid insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Manag Sci 73:1236-1243 (2017).
Jacob CRO, Zanardi OZ, Malaquais JB, Silva CAS and Yamamoto PT, The impact of four widely used neonicotinoid insecticides on Tetragonisca angustula (Latreille) (Hymenoptera: Apidae). Chemosphere 224:65-70 (2019).
Sgolastra F, Arnan X, Cabbri R, Isani G, Medrzycki P, Teper D et al., Combined exposure to sublethal concentrations of an insecticide and a fungicide affect feeding, ovary development and longevity in a solitary bee. Proc R Soc Biol Sci Ser B 285:20180887 (2018).
Soares HM, Jacob CRO, Carvalho SM, Nocelli RCF and Malaspina O, Toxicity of imidacloprid to the stingless bee Scaptotrigona postica Latreille, 1807 (Hymenoptera: Apidae). Bull Environ Contam Toxicol 94:675-680 (2015).
Jacob CRO, Soares HM, Carvalho SM, Nocelli RCF and Malaspina O, Acute toxicity of fipronil to the stingless bee Scaptotrigona postica Latreille. Bull Environ Contam Toxicol 90:69-72 (2013).
Thompson H, Risk assessment for honey bees and pesticides - recent developments and ‘new issues’. Pest Manag Sci 66:1157-1162 (2010).
Holder PJ, Jones AK, Tyler CR and Cresswell JE, Fipronil pesticide as a suspect in historical mass mortalities of honey bees. Proc Natl Acad Sci USA 115:13033-13038 (2018).
Bohme F, Bischoff G, Zebitz CPW, Rosenkranz P and Wallner K, From field to fork - will pesticide-contaminated pollen diet lead to contaminated royal jelly? Apidologie 49:112-119 (2018).
Nicholls E, Fowler R, Niven JE, Gilbert JD and Goulson D, Larval exposure to field-realistic concentrations of clothianidin has no effect on development rate, over-winter survival or adult metabolic rate in a solitary bee, Osmia bicornis. Peer J 5:e3417 (2017).
Becher M, Grimm V, Thorbek P, Horn J, Kennedy P and Osborne J, BEEHAVE: a systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure. J Appl Ecol 51:470-482 (2014).
Becher MA, Twiston-Davies G, Penny TD, Goulson D, Rotheray EL and Osborne JL, Bumble-BEEHAVE: a systems model for exploring multifactorial causes of bumblebee decline at individual, colony, population and community level. J Appl Ecol 55:2790-2801 (2018).
Everaars J, Settele J and Dormann CF, Fragmentation of nest and foraging habitat affects time budgets of solitary bees, their fitness and pollination services, depending on traits: results from an individual-based model. PLoS One 13:e0188269 (2018).