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ORIGINAL ARTICLES

Repellency of insecticides and the effect of thiacloprid on bumble bee colony development in red clover (Trifolium pratense L.) seed crops

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Pages 439-451 | Received 29 Nov 2018, Accepted 28 Feb 2019, Published online: 20 Mar 2019

References

  • Aamlid TS. 2018. Frøavl av rødkløver. Dyrkingsveiledning Mai 2018. [Seed production of red clover. Grower manual May 2018]. Http://froavl.no. Norwegian.
  • Aamlid TS, Andersen A, Lindemark PO, Øverland JI, Breivik L, Kise S, Jørgensen S, Susort Å, Steensohn AA. 2010. Bekjemping av snutebiller i frøeng av rødkløver. [Control of weevils in red clover seed crops]. Bioforsk Fokus. 1:212–217. Norwegian.
  • Blacquière T, Smagghe G, van Gestel CAM, Mommaerts V. 2012. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology. 21:973–992. doi: 10.1007/s10646-012-0863-x
  • Bommarco R, Lundin O, Smith HG, Rundlöf M. 2012. Drastic historic shifts in bumble-bee community composition in Sweden. Proc Royal Soc B Biol Sci. 279:309–315. doi: 10.1098/rspb.2011.0647
  • Brødsgård CJ, Hansen H. 2002. Bi-bestøvning af rødkløver. [Honey bee pollination of red clover]. Grøn Viden. Markbrug nr. 257. Juni 2002. 4 pp. Danish.
  • Christiansen A. 2016. Handbook of analytical methods for pesticide residues. Ås: Norwegian Institute of Bioeconomy Research.
  • Decourtye A, Devillers J. 2010. Ecotoxicity of neonicotinoid insecticides to bees. In: Thany SH, editor. Insect nicotinic acetylcholine receptors. 1st ed. New York: Springer; p. 85–95.
  • Dupont YL, Damgaard C, Simonsen V. 2011. Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields. PLoS ONE. 6(9):e25172. doi:10.1371/journal.pone.0025172.
  • Eklima. 2019. Meteorological data collected from http://eklima.met.no/.
  • Ellis C P, Whitehorn P KJ, David A, Goulson D. 2017. The neonicotinoid insecticide thiacloprid impacts upon bumble bee colony development under field conditions. Environ Sci Technol. 51:1727–1732. doi: 10.1021/acs.est.6b04791
  • EN15662. 2008. Foods of plant origin – Determination of pesticide residues using GC-MS and/or LC-MS/MS following acetonitrile extraction/partitioning and clean-up by dispersive SPE – QuEChERS-method. ISBN 9780580584411. 84 pp.
  • Goulson D. 2010. Bumble bees behaviour, ecology and conservation. Second ed. Oxford: Oxford university press.
  • Goulson D, Lye GC, Darvill B. 2008. Decline and conservation of bumble bees. Annu Rev Entomol. 53:191–208. doi: 10.1146/annurev.ento.53.103106.093454
  • Goulson D, Nicholls E, Botías C, Rotheray EL. 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 347:1255957. doi: 10.1126/science.1255957
  • Havstad LT, Åström J, Øverland JI, Valand S, Hetland O, Susort Å. 2015. Bedre pollinering av rødkløver [Improved pollination of red clover]. Jord- og plantekultur. Bioforsk Fokus. 10(1):224–232. Norwegian.
  • Henry M, Beguin M, Requier F, Rollin O, Odoux J, Aupinel P, Aptel J, Tchamitchian S, Decourtye AA. 2012. A common pesticide Decreases Foraging Success and Survival in honey bees. Science. 336:348–350. doi: 10.1126/science.1215039
  • Iwasa T, Motoyama N, Ambrose JT, Roe JR. 2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot. 23:371–378. doi: 10.1016/j.cropro.2003.08.018
  • Jeschke P, Nauen R, Schindler M, Elbert A. 2011. Overview of the status and global strategy for neonicotinoids. J Agric Food Chem. 59:2897–2908. doi: 10.1021/jf101303g
  • Karise R, Viik E, Mänd M. 2007. Impact of alpha-cypremethrin on honey bees foraging on spring oilseed rape Brassica napus flowers in field conditions. Pest Manage Sci. 63:1085–1089. doi: 10.1002/ps.1445
  • Kolařík P, Rotrekl J. 2013. Regulation of the abundance of clover seed weevils, Apion spp. (Coleoptera: Curculionidae) in a seed stand of red clover (Trifolium pratense L.). J Entomol Acarol Res. 45:105–109. doi: 10.4081/jear.2013.e19
  • Konzmann S, Lunau K. 2014. Divergent rules for pollen and nectar foraging bumblebees – a laboratory study with artificial flowers offering diluted nectar substitute and pollen surrogate. PLoS ONE. 9(3):e91900. doi:10.1371/journal.pone.0091900.
  • Laycock I, Lenthall KM, Barratt AT, Cresswell JE. 2012. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology. 21:1937–1945. doi: 10.1007/s10646-012-0927-y
  • LMT. 2019. Meteorological data collected from http://lmt.nibio.no.
  • Lundin O. 2013. Ecology and management of crop pollination and pest control. Insights from red clover seed production. Doctoral Thesis. Swedish University of Agricultural Sciences. SLU Service/Repro. 54 pp.
  • Lundin O, Rundlöf M, Smith HG, Bommarco R. 2012. Towards integrated pest management in red clover seed production. J Econ Entomol. 105:1620–1628. doi: 10.1603/EC12179
  • Maloof JE, Inouye DW. 2000. Are nectar robbers cheaters or mutualists? Ecology, 81(10): 2651–2661. doi: 10.1890/0012-9658(2000)081[2651:ANRCOM]2.0.CO;2
  • Mayer DF, Lunden JD. 1997. Effects of imidacloprid insecticide on three bee pollinators. Horticultur Sci. 29:93–97.
  • Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G. 2010. Risk assessment for side-effects of neonicotinoids against bumble bees with and without impairing foraging behaviour. Ecotoxicology. 19:207–215. doi: 10.1007/s10646-009-0406-2
  • Mueller-Beilschmidt D. 1990. Toxicology and environmental fate of synthetic pyrethroids. J Pestic Reform. 10:32–37.
  • Norli HR, Christiansen A, Deribe E. 2011. Application of QuEChERS method for extraction of persistent organic pollutants in fish tissue and analysis by gas chromatography mass spectrometry. J Chromatogr A. 1218: 7234–7241. doi: 10.1016/j.chroma.2011.08.050
  • Norsk frøavlerlag. 2018. Tilleggsetikett Off-label. Biscaya OD 240 – tiakloprid [Additional label. Biscaya OD 240 – thiacloprid]. https://www.froavlerlaget.no/Off_label/Tilleggsetikett/Biscaya_OD_240_godkjent_tilleggsetikett.pdf. Norwegian.
  • Öberg S, Gjershaug JO, Staverløkk A, Åström J, Ødegaard F. 2013. Framdriftsrapport 2012 fra utviklingsprosjekt: Naturindeks; videreutvikling av kunnskapsgrunnlaget for humler og sommerfugler [Progress report 2012 from development project: Nature Index; extending the knowledge base for bumble bees and butterflies]. NINA Minirapport 418. 18 s. Norwegian.
  • Ødegaard F, Gjershaug JO, Öberg S, Mjelde A. 2009. Status for humler (Hymenoptera, Apidae, Bombus spp.) i Norge i 2010 [Status of bumble bees (Hymenoptera, Apidae, Bombus spp.) in Norway in 2010]. Fauna. 62(4):94–104. Norwegian.
  • Pedersen TR. 2010. Bekämpa och reglera i vallfrö [control and regulation in seed production]. Svensk Frötidning. 3(10):35–36. Swedish.
  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. 2010. Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol. 25:345–353. doi: 10.1016/j.tree.2010.01.007
  • Ratnieks FLW. 2000. How far do bees forage. Bee Improv. 6:10–11.
  • Rundlöf M, Lundin O, Bommarco R. 2018. Annual flower strips support pollinators and potentially enhance red clover seed yield. Ecol Evol. 8:7974–7985. doi: 10.1002/ece3.4330
  • SAS Institute. 2015. Base SAS® 9.4 procedures guide. Cary (NC): SAS Institute Inc.
  • Schmuck R, Stadler T, Schmidt HW. 2003. Field relevance of a synergistic effect observed in the laboratory between an EBI fungicide and a chloronicotinyl insecticide in the honeybee (Apis mellifera L, Hymenoptera). Pest Manage Sci. 59:279–286. doi: 10.1002/ps.626
  • Shires SW, Le Blanc J, Murray A, Forbes S, Debray P. 1984. A field trial to assess the effects of a new pyrethroid insecticide, WL85871, on foraging honeybees in oilseed rape. J Apic Res. 23:217–226. doi: 10.1080/00218839.1984.11100636
  • Stanley DA, Garratt MPD, Wickens JB, Wickens VJ, Potts SG, Raine NE. 2015. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumble bees. Nature. 528:548–550. doi: 10.1038/nature16167
  • Stout JC, Allen JA, Goulson D. 2000. Nectar robbing, forager efficiency and seed set: bumble bees foraging on the self-incompatible plant Linaria vulgaris (Scrophulariaceae). Acta Oecol. 21:277–283. doi: 10.1016/S1146-609X(00)01085-7
  • Tison L, Hahn ML, Holtz S, Rößner A, Greggers U, Bischoff G, Menzel R. 2016. Honey bees’ Behavior Is impaired by Chronic exposure to the neonicotinoid thiacloprid in the field. Environ Sci Technol. 50:7218–7227. doi: 10.1021/acs.est.6b02658
  • Thompson HM. 2001. Assessing the exposure and toxicity of pesticides to bumble bees (Bombus sp. Apidologie. 32:305–321. doi: 10.1051/apido:2001131
  • Thompson HM. 2003. Behavioural effects of pesticides in bees – their potential for use in risk assessment. Ecotoxicology. 12:317–330. doi: 10.1023/A:1022575315413
  • Wermuth KH, Dupont YL. 2010. Effects of field characteristics on abundance of bumblebees (Bombus spp.) and seed yield in red clover fields. Apidologie. 41:657–666. doi: 10.1051/apido/2010038
  • 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. doi: 10.1126/science.1215025
  • Williams RD. 1931. Methods and technique of breeding red clover, white clover and lucerne. Imperial Bureau of Plant Genetics. Herbage Plants. 3:46–77.
  • Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG, Redhead J, Ridding L, Dean H, Sleep D, Henrys P, et al. 2017. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science. 356:1393–1395. doi: 10.1126/science.aaa1190
  • Woodcock BA, Isaac NJ, Bullock JM, Roy DB, Garthwaite DG, Crowe A, Pywell RF. 2016. Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat Commun. 7:12459. doi: 10.1038/ncomms12459
  • Wratt EC. 1968. The pollinating activities of bumble bees and honey bees in relation to temperature, competing forage plants, and competition from other foragers. J Apic Res. 7(2):61–66. doi: 10.1080/00218839.1968.11100190

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