Skip to main content
SpringerLink
Log in

Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Bumblebees and other pollinators provide a vital ecosystem service for the agricultural sector. Recent studies however have suggested that exposure to systemic neonicotinoid insecticides in flowering crops has sub-lethal effects on the bumblebee workforce, and hence in reducing queen production. The mechanism behind reduced nest performance, however, remains unclear. Here we use Radio Frequency Identification (RFID) technology to test whether exposure to a low, field realistic dose (0.7 ppb in sugar water and 6 ppb in pollen) of the neonicotinoid imidacloprid, reduces worker foraging efficiency. Whilst the nectar foraging efficiency of bees treated with imidacloprid was not significantly different than that of control bees, treated bees brought back pollen less often than control bees (40 % of trips vs 63 % trips, respectively) and, where pollen was collected, treated bees brought back 31 % less pollen per hour than controls. This study demonstrates that field-realistic doses of these pesticides substantially impacts on foraging ability of bumblebee workers when collecting pollen, and we suggest that this provides a causal mechanism behind reduced queen production in imidacloprid exposed colonies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Article  Google Scholar 

  • Aliouane Y, El Hassani AK, Gary V, Armengaud C, Lambin M, Gauthier M (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behaviour. Environ Toxicol Chem 28:113–122

    Article  CAS  Google Scholar 

  • Bonmatin JM, Moineau I, Charvet R, Fléché C, Colin ME, Bengsch ER (2003) A LC/APCI-MS/MS method for analysis of imidacloprid in soils, in plants and in pollens. Anal Chem 75:2027–2033

    Article  CAS  Google Scholar 

  • Bortolotti L, Montanari R (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull Insectol 56:63–67

    Google Scholar 

  • Carvell C, Roy DB, Smart SM, Pywell RF, Preston CD, Goulson D (2006) Declines in forage availability for bumblebees at a national scale. Biol Conserv 132:481–489

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delègue MH (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419

    Article  CAS  Google Scholar 

  • DEFRA (2012) Farming statistics: final crop areas, yields, livestock populations and agricultural workforce. Farming Statistics, Department for Environment, Food and Rural Affairs, London

    Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The Sublethal Effects of Pesticides on Beneficial Arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  Google Scholar 

  • Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F, Gargiulo G, Pennacchio F (2013) Neonicotinoid clothianidin affects insect immunity and promotes replication of a viral pathogen in honey bees. PNAS 201314923 110(46):18466–18471. doi:10.1073/pnas.1314923110

    Article  Google Scholar 

  • EFSA (2012) Statement on the findings in recent studies investigating sub-lethal effects in bees of some neonicotinoids in consideration of the uses currently authorised in Europe. EFSA J 10:2752

    Google Scholar 

  • Elston C, Thompson HM, Walters KFA (2013) Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies. Apidologie 44:563–574

    Article  CAS  Google Scholar 

  • European Commission (2013) Bee health: EU-wide restrictions on pesticide use to enter into force. European Commission, Brussels

    Google Scholar 

  • Garthwaite DG, Barker I, Parrish G, Smith L, Chippindale C, Pietravalle S (2010) Pesticide usage survey report 235-Arable crops in the United Kingdom. DEFRA, London

    Google Scholar 

  • Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual and colony-level traits in bees. Nature 491:105–108. doi:10.1038/nature11585

    Article  CAS  Google Scholar 

  • Goulson D (2010) Bumblebees: behaviour, ecology and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Goulson D, Peat J, Stout JC, Tucker J, Darvill B, Derwent LC, Hughes WOH (2002) Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? Anim Behav 64:123–130

    Article  Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumblebees. Annu Rev Entomol 53:191–208

    Article  CAS  Google Scholar 

  • Goulson D, Lepais O, O’Connor S, Osborne JL, Sanderson R, Cussans J, Goffe L, Darvill B (2010) Effects of land use at a landscape scale on bumblebee nest density and survival. J Appl Ecol 47:1207–1215

    Article  Google Scholar 

  • Harder LD (1990) Behavioural responses by bumble bees to variation in pollen availability. Oecologia 85:41–47

    Article  Google Scholar 

  • Hayter KE, Cresswell JE (2006) The influence of pollinator abundance on the dynamics and efficiency of pollination in agricultural Brassica napus: implications for landscape-scale gene dispersal. J Appl Ecol 43:1196–1202

    Article  Google Scholar 

  • Henry M, Béguin 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 336:348–350

    Article  CAS  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313

    Article  Google Scholar 

  • Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields. PLoS ONE 7. doi:10.1371/journal.pone.0029268

  • 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

    Google Scholar 

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

    Google Scholar 

  • McGregor SE (1976) USDA Agriculture Handbook No. 496. Insect pollination of cultivated crops. USDA, Washington DC

    Google Scholar 

  • Molet M, Chittka L, Stelzer RJ, Streit S, Raine NE (2008) Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris. Behav Ecol Sociobiol 62:1919–1926

    Article  Google Scholar 

  • Müller C, Schmid Hempel P (1992) Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites. Ecolo Entomol 17:343–353

    Article  Google Scholar 

  • Nauen R, Ebbinghaus-Kintscher U, Salgado VL, Kaussmann M (2003) Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pestic Biochem Physiol 76:55–69

    Article  CAS  Google Scholar 

  • Ohashi K, D’Souza D, Thomson JD (2010) An automated system for tracking and identifying individual nectar foragers at multiple feeders. Behav Ecol Sociobiol 64:891–897

    Article  Google Scholar 

  • Peat J, Goulson D (2005) Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee, Bombus terrestris. Behav Ecol Sociobiol 58:152–156

    Article  Google Scholar 

  • Pollak P (2011) Fine chemicals: the industry and the business. Wiley, Hoboken

    Book  Google Scholar 

  • Raine NE, Chittka L (2007) Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris). Die Naturwissenschaften 94:459–464

    Article  CAS  Google Scholar 

  • Robinson EJH, Richardson TO, Sendova-Franks AB, Feinerman O, Franks NR (2009) Radio tagging reveals the roles of corpulence, experience and social information in ant decision making. Behav Ecol Sociobiol 63:627–636

    Article  Google Scholar 

  • Stelzer RJ, Chittka L, Carlton M, Ings TC (2010) Winter active bumblebees (Bombus terrestris) achieve high foraging rates in Urban Britain. PLoS ONE 5. doi:10.1371/journal.pone.0009559

  • Streit S, Bock F, Pirk CWW, Tautz J (2003) Automatic life-long monitoring of individual insect behaviour now possible. Zoology 106:169–171

    Article  Google Scholar 

  • Sumner S, Lucas E, Barker J, Isaac N (2007) Radio-tagging technology reveals extreme nest-drifting behaviour in a eusocial insect. Curr Biol 17:140–145

    Article  CAS  Google Scholar 

  • Thompson H, Harrington P, Wilkins W, Pietravalle S, Sweet D, Jones A (2013) Effects of neonicotinoid seed treatments on bumble bee colonies. Food Environ Res Agency Rep. http://fera.co.uk/ccss/documents/defraBumbleBeeReportPS2371V4a.pdf. Accessed 29 Oct 2013

  • Van Der Steen JJM (2008) Intection and transmission of Nosema bombie in Bombus terrestris colonies and its effect on hibernation, mating and colony founding. Apidologie 39:273–282

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216:1799–1807

    Article  CAS  Google Scholar 

  • Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behaviour induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101:1743–1748

    Article  CAS  Google Scholar 

  • Yang EC, Chang HC, Wu WY, Chen YW (2012) Impaired olfactory associative behaviour of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS ONE 7. doi:10.1371/journal.pone.0049472

Download references

Acknowledgments

We would like to thank Aaron Hamilton and Stephan Hamilton for their assistance in data collection. We would also like to thank Jeroen Minderman and Timothy Paine for their advice on analysis and James Weir for his technical support. Finally we would like to thank the Natural Environment Research Council and the Economic and Social Research Council for their financial support.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. School of Natural Sciences, University of Stirling, Stirling, FK9 4LA, UK

    Hannah Feltham & Kirsty Park

  2. School of Life Sciences, University of Sussex, Brighton, BN1 9RH, UK

    Dave Goulson

Authors
  1. Hannah Feltham
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kirsty Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dave Goulson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hannah Feltham.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feltham, H., Park, K. & Goulson, D. Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23, 317–323 (2014). https://doi.org/10.1007/s10646-014-1189-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-014-1189-7

Keywords

Search

Navigation