, Volume 8, Issue 3, pp 147–166 | Cite as

Extrapolating from Honeybees to Bumblebees in Pesticide Risk Assessment


Bumblebees are important pollinators of many crops and wild flowers and there are both conservation and economic reasons for taking action to assess the impact of pesticides on bumblebees. Pesticide risk assessments for honeybees are based on hazard ratios which rely on application rates and toxicity data and are unlikely to be appropriate for bumblebees. Bumblebees are active at different times and on different crop species and are, therefore, likely to have different exposure profiles. Unlike honeybees, deaths of bumblebees due to pesticides are unlikely to be reported, since the bees are not kept domestically and will die in small numbers. This paper highlights the differences in the potential risk posed by pesticides to bumblebees from that of honeybees. This is based on their exposure through use of crops and flowering weeds and on available data on toxicity of pesticides. This information is also intended as a source document for information on the foraging behavior and phenology of bumblebees for use in risk assessment for pesticides.

Pesticides risk assessment bumblebees 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Acker, R.C.V. and Lutman, P.J.W. (1995). Weed interference in autumn-sown field beans (Vicia faba L.). In Proceedings of the Brighton Crop Protection Conference—Weeds, 20–23 November 1995, pp. 907–12. Farnham: BCPC.Google Scholar
  2. Alford, D.V. (1975). Bumblebees. London: Davis-Poynter Ltd.Google Scholar
  3. Banaszak, J. (1984). The occurrence and number of bees (Apodea) on some cultivated crop plants in the Wielkopolska region (W. Poland). Entomologiczne 53, 623–31.Google Scholar
  4. Barker, R.J., Lehner, Y. and Kunzmann, M.R. (1980). Pesticides and honeybees: nectar and pollen contamination in alfalfa treated with dimethoate. Arch. Environ. Contam. Toxicol. 9, 125–33.Google Scholar
  5. Barr, C.J., Bunce, R.G.H., Clarke, R.T., Fuller, R.M., Fuse, M.T., Gillespie, M.K., Broom, G.B., Hallam, C.J., Hornung, M., Howard, D.C. and Ness, M.J. (1996). The Countryside Survey—Main Report. London: Department of the Environment.Google Scholar
  6. Barrow, D.A. (1983). Ecological Studies on Bumblebees in South Wales with Special Reference to Resource Partitioning and Bee Size Variation. PhD Thesis, University College, Cardiff.Google Scholar
  7. Batra, S.W.T. (1993). Male-fertile potato flowers are selectively buzz-pollinated only by Bombus terricola Kirby in upstate New York. J. Kansas Entomol. Soc. 66, 252–4.Google Scholar
  8. Bhalla, O.P., Verma, A.K. and Dhaliwal, H.S. (1983). Foraging activity of insect pollinators visiting stone fruits. J. Entomol. Res. 7, 91–4.Google Scholar
  9. Bishop, J.A. (1994). Bumblebees (Bombus hypnorum) collect aphid honeydew on stone pine (Pinus pumila) in the Russian far-east. J. Kansas Entomol. Soc. 67, 220–2.Google Scholar
  10. Bohart, G.E. (1957). Pollination of alfalfa and red clover. Annu. Rev. Entomol. 2, 355–80.Google Scholar
  11. Bohart, G.E. (1960). Insect pollination of forage legumes. Bee World 41, 51–64.Google Scholar
  12. Brian, A.D. (1957). Differences in the flowers visited by four species of bumblebees and their causes. J. Animal Ecol. 26, 69–96.Google Scholar
  13. Clarke, J.H., Bowerman, P., Young, J.E.B., Cook, S.K., Jones, A.E., Groves, S.J. and Green, M. (1993). Effects of recommended and reduced rate herbicides on weed number, yield and gross margin in TALISMAN: report on the first two years. In Proceedings of the Brighton Crop Protection Conference-Weeds, 22–25 November 1993, pp. 1009–14. Farnham: BCPC.Google Scholar
  14. Corbet, S.A., Williams, I.H. and Osborne, J.L. (1991). Bees and pollination of crops and wild flowers in the European Community. Bee World 72, 47–59.Google Scholar
  15. Corbet, S.A., Fussell, M., Ake, R., Fraser, A., Gunson, C., Savage, A. and Smith, K. (1993). Temperature and pollinating activity of social bees. Ecol. Entomol. 18, 17–30.Google Scholar
  16. Crane, E. (1990). Bees and Beekeeping; Science Practice and World Resources. Oxford: Heinemann Newnes.Google Scholar
  17. Davis, A.R. and Shuel, R.W. (1988). Distribution of carbofuran and dimethoate in flowers and their secretion in nectar as related to nectary vascular supply. Can. J. Bot. 66, 1248–55.Google Scholar
  18. Delbrassinne, S. and Rasmont, P. (1988). Contribution a l'etude de la pollinisation du colza Brassica napus L. var. oleifera (Moench) Delle, en Belgique. Bull. Rech. Agron. Gembloux 23, 123–52.Google Scholar
  19. Doorn, A.V. (1993). Bumblebees breaking through as crop pollinators. In Pollination in Tropics, pp. 195–201. IUSSI.Google Scholar
  20. Dramstad, W. and Fry, G. (1995). Foraging activity in bumblebees in relation to flower resources on arable land. Agric. Ecosystems Environ. 53, 123–35.Google Scholar
  21. Drescher, W. and Geusen-Pfister, H. (1991). Comparative testing of the oral toxicity of acephate, dimethoate and methomyl to honeybees, bumblebees and syrphidae. Acta Horticulturae 288, 133–6.Google Scholar
  22. Ellenberg, H. (1988). Vegetation Ecology of Central Europe, 4th ed. Cambridge: Cambridge University Press.Google Scholar
  23. Emmet, B.J. (1971). Insect visitors to pear blossom. Plant Pathol. 20, 36–40.Google Scholar
  24. EPPO (1993). Decision making scheme for the environmental risk assessment of plant protection products—honeybees. Bull. OEPP / EPPO Bull. 23, 151–65.Google Scholar
  25. Firbank, L.G. (1990). Interactions between weeds and crops. In: Firbank, L.G., Carter, N., Darbyshire, J.F. and Potts, G.R. (eds) The Ecology of Temperate Cereal Fields, pp. 469. Oxford: Blackwell Scientific Publications.Google Scholar
  26. Free, J.B. (1968a). The behaviour of bees visiting runner beans (Phaseolus multiflorus). J. Appl. Ecol. 5, 631–8.Google Scholar
  27. Free, J.B. (1968b). The foraging behaviour of honeybees (Apis mellifera) and bumblebees (Bombus spp.) on blackcurrant (Ribes nigrum), raspberry (Rubus idaeus) and strawberry (Fragaria x ananassa) flowers. J. Appl. Ecol. 5, 157–68.Google Scholar
  28. Free, J.B. (1993). Insect Pollination of Crops, 2nd ed. London: Academic Press.Google Scholar
  29. Fussell, M., Osborne, J.L. and Corbet, S.A. (1991). Seasonal and diurnal patterns of insect visitors to winter sown field bean flowers in Cambridge. Aspects Appl. Biol. 27, 95–9.Google Scholar
  30. Fussell, M. and Corbet, S.A. (1991). Forage for bumblebees and honeybees in farmland; a case study. J. Apic. Res. 30, 87–97.Google Scholar
  31. Fussell, M. and Corbet, S.A. (1992). Flower usage by bumblebees: a basis for forage plant management. J. Appl. Ecol. 29, 451–65.Google Scholar
  32. Fussell, M. and Corbet, S.A. (1993). Bumblebee (Hym. Apidae) forage plants in the United Kingdom. Entomologists Monthly Magazine 129, 1–14.Google Scholar
  33. Glasgow, J.L., Dicks, J.W. and Hodgson, D.R. (1976). Competition by, and chemical control of, natural weed populations in spring-sown field beans (Vicia faba). Ann. Appl. Biol. 84, 259–69.Google Scholar
  34. Goodwin, S.G. (1995). Seasonal phenology and abundance of early-, mid-and late-season bumblebees in Southern England 1985–1989. J. Apic. Res. 34, 79–89.Google Scholar
  35. Greig-Smith, P.W., Thompson, H.M., Hardy, A.R., Bew, M.H., Findlay, E. and Stevenson, J.H. (1994). Incidents of poisoning of honeybees (Apis mellifera) by agricultural pesticides in Great Britain 1981–1991. Crop Protection 13, 567–81.Google Scholar
  36. Gretenkord, C. and Drescher, W. (1993). 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, 519–20.Google Scholar
  37. Griffiths, D. and Robberts, E.J. (1996). Bumblebees as pollinators of glasshouse crops. In Matheson, A. (ed.) Bumble ees for Pleasure and Profit, pp. 33–9. Cardiff: IBRA.Google Scholar
  38. Gubin, A.F. (1945). Cross-pollination of fibre flax. Bee World 26, 30–1.Google Scholar
  39. Gurr, L. (1975). The role of bumblebees as pollinators of red clover and lucerne in New Zealand; a review and prospect. Proc. N.Z. Grassland Association 36, 111–22.Google Scholar
  40. Gwynne, D.C. and Murray, R.B. (1985). Weed Biology and Control in Agriculture and Horticulture. London: Batsford Technical.Google Scholar
  41. Gyan, K.Y. and Woodell, S.R.J. (1987). Analysis of insect pollen loads and pollination efficiency of some common insect visitors of woody Rosaceae. Functional Ecol. 1, 269–74.Google Scholar
  42. Harder, L.D. (1983). Functional differences of the proboscides of the short-and long-tongued bees (Hymenoptera, Apoidae). Can. J. Zool. 61, 1580–6.Google Scholar
  43. Heinrich, B. (1979). “Majoring” and “minoring” by foraging bumblebees, Bombus vagans; an experimental analysis. Ecology 60, 245–55.Google Scholar
  44. Heinrich, B. (1993). The Hot-Blooded Insects, Berlin: Springer-Verlag.Google Scholar
  45. Herrera, C. (1990). Daily patterns of pollinator activity, differential pollinating effectiveness and floral resource availability in a summer flowering Mediterranean shrub. Oikos 58, 277–88.Google Scholar
  46. Holm, N. (1966). The utilization and management of bumblebees for red clover and alfalfa seed production. Annu. Rev. Entomol. 11, 155–77.Google Scholar
  47. Hurd, P.D. (1964). The pollination of pumpkins, gourds and squashes (genus Curcubita). Bee World 47, 97–8.Google Scholar
  48. Inglesfield, C. (1989). Pyrethroids and terrestrial non-target organisms. Pestic. Sci. 27, 387–428.Google Scholar
  49. Jaycox, E.R. (1964). Effect on honeybees of nectar from systemic insecticide-treated plants. J. Econ. Entomol. 57, 31–5.Google Scholar
  50. Kendall, D.A. and Smith, B.D. (1976). The pollinating efficiency of honeybee and bumblebee visits to flowers of the runner bean Phaseolus coccineus L. J. Appl. Ecol. 13, 749–52.Google Scholar
  51. Kendall, D.A. and Solomon, M.E. (1973). Quanitites of pollen on the bodies of insects visiting apple blossom. J. Appl. Ecol. 10, 627–34.Google Scholar
  52. Kevan, P.G., Straver, W.A., Offer, M. and Laverty, T.M. (1993). Pollination of greenhouse tomatoes by bumblebees in Ontario, Canada. Proc. Entomol. Soc. Ontario 3, 4–6.Google Scholar
  53. Knott, C.M., May, M.J. and Ward, J.T. (1995). Weed control in potatoes, oilseed rape, pulses and sugar beet—trends and prospects. In Proceedings of the Brighton Crop Protection Conference—Weeds, 20–23 November 1995, pp. 1193–202. Farnham: BCPC.Google Scholar
  54. Koch, H. and Weiber, P. (1997). Exposure of honeybees during pesticide application under field conditions. Apidologie 28, 439–47.Google Scholar
  55. Legeun, J., Mesquida, J., Pierre, J.S., Morin, G., Tasei, J.N. and Carre, S. (1993). Efficiency of pollinating treatments on 2 lines of spring faba bean (Vicia faba L. var equina Steudel) with different levels of self fertility and using three species of Bombus Latr. (Hymenoptera, Apidae). Apidologie 24, 129–45.Google Scholar
  56. Longley, M. and Sotherton, N.W. (1997). Factors determining the effects of pesticides upon butterflies inhabiting arable farmland. Agric. Ecosystems Environ. 61, 1–12.Google Scholar
  57. Lord, K.A., May, M.A. and Stevenson, J.H. (1968). The secretion of the systemic insecticides dimethoate and phorate into nectar. Ann. Appl. Biol. 61, 19–27.Google Scholar
  58. Lundberg, H. (1980). Effects of weather on foraging flights of bumblebees Hymenoptera, Apidae in subalpine/alpine area. Holarctic Ecol. 3, 104–10.Google Scholar
  59. Lutman, P.J.W., Bowerman, P., Palmer, G.M. and Whytock, G.P. (1995). A comparison of the competitive effects of eleven weed species on the growth and yield of winter oilseed rape. In Proceedings of the Brighton Crop Protection Conference—Weeds, 20–23 November 1995, pp. 877–82. Farnham: BCPC.Google Scholar
  60. Macdonald, M.A. (1998). The feeding ecology of some Bombus and Psithyrus bees in North Scotland and the importance to them of native and exotic plants. In preparation.Google Scholar
  61. Macfarlane, R.P., Griffin, R.P. and Read, P.E.C. (1983). Bumblebee management options to improve “Grasslands Pawera” red clover seed yields. Proc. N.Z. Grassland Association 44, 47–53.Google Scholar
  62. Macfarlane, R.P., Ende, H.J. and Griffin, R.P. (1991). Pollination needs of “Grasslands Pawera” red clover. Acta Horticulturae 288, 399–404.Google Scholar
  63. MAFF (1997). (General Agricultural Statistics Section).Google Scholar
  64. Marshall, E.J.P. (1989). Distribution patterns of plants associated with arable field edges. J. Appl. Ecol. 26, 247–57.Google Scholar
  65. Mayer, D.F. (1983). Behaviour of pollinators on Malus. In Proceedings of the 5th International Pollination Symposium, Versailles, pp. 387–390.Google Scholar
  66. McGregor, S.E. (1976). Insect Pollination of Cultivated Crop Plants. Washington DC: Agricultural Research Service, USDA.Google Scholar
  67. Michaelson-Yeates, T.P.T., Marshall, A.H., Williams, I.H., Carreck, N.L. and Simpkins, J.R. (1997). The use of isoenzyme markers to determine pollen flow and seed paternity mediated by Apis mellifera and Bombus spp. in Trifolium repens, a self-compatible plant species. J. Apic. Res. 36, 57–62.Google Scholar
  68. Mortimer, A.M. (1990). The biology of weeds. In Hance, R.J. and Holly, K. (eds) Weed Control Handbook: Principles, 8th ed, pp. 582. Farnham: BCPC/Blackwell.Google Scholar
  69. Mountford, J., Parish, T. and Sparks, T.H. (1994). The flora of field margins in relation to land use and boundary features. In Boatman, N. (ed) Field Margins; Integrating Agriculture and Conservation, Monograph 58, pp. 105–10. Farnham: BCPC.Google Scholar
  70. Nye, W.P. and Andersen, J.L. (1974). Insect pollinators frequenting strawberry blossoms and effect of honeybees on yield and fruit quality. J. Amer. Soc. Hortic. Sci. 99, 40–4.Google Scholar
  71. Olgivy, S.E., Green, M.R., Groves, S.J. and Jones, A.E. (1993). SCARAB—the impact of less intensive herbicide use on the diversity and distribution of weed species in three arable rotations. In Proceedings of the Brighton Crop Protection Conference—Weeds, 22–25 November 1993, pp. 1241–6. Farnham: BCPC.Google Scholar
  72. Osborne, J.L. (1994). Evaluating a Pollination System: Borago officinalis and bees. PhD Thesis, University of Cambridge.Google Scholar
  73. Pallutt, B. (1993). Population dynamics and competition of weeds depending on crop rotation and mechanical and chemical control measures in cereals. In Proceedings of the Brighton Crop Protection Conference—Weeds, 22–25 November 1993, pp. 1197–204. Farnham: BCPC.Google Scholar
  74. Patten, K.D., Shanks, C.H. and Mayer, D.F. (1993). Evaluation of herbaceous plants for attractiveness to bees for use near cranberry farms. J. Apic. Res. 32, 73–9.Google Scholar
  75. Pinchinat, B., Bilinski, M. and Ruszkowski, A. (1979). Possibilities of applying bumblebees as pollen vectors in tomato F1 hybrid seed production. In Proceedings of the 4th International Symposium on Pollination, Maryland, pp. 73–90.Google Scholar
  76. Plowright, R.C. and Laverty, T.M. (1984). The ecology and sociobiology of bumblebees. Annu. Rev. Entomol. 29, 175–99.Google Scholar
  77. Pojar, J. (1973). Pollination of typically anemophilous salt marsh plants by bumblebees, Bombus terricola occidentalis Grne. Amer. Midland Naturalist 89, 448–51.Google Scholar
  78. Proctor, M., Yeo, P. and Lack, A. (1996). The Natural History of Pollination. London: Harper Collins.Google Scholar
  79. Prys-Jones, O.E. (1982). Ecological Studies of Foraging and Life History in Bumblebees. PhD Thesis, Cambridge University.Google Scholar
  80. Prys-Jones, O.E. and Corbet, S.A. (1991). Bumblebees, 2nd ed. Slough: Richmond Publishing.Google Scholar
  81. Reader, R.J. (1977). Bog ericad flowers: self compatibility and attractiveness to bees. Can. J. Botany 55, 2279–87.Google Scholar
  82. Richards, K.W. and Edwards, P.D. (1988). Density, diversity and efficiency of pollinators of sainfoin, Onobrychis viciifolia sp. Can. Entomoloist 120, 1085–100.Google Scholar
  83. Sanford, J.C. and Hannemann, R.E. (1981). The use of bees for the purpose of inter-mating in potato. Amer Potato J. 58, 481–5.Google Scholar
  84. Saville, N.M. (1993). Bumble Bee Ecology in Woodlands and Arable Farmland. PhD Thesis, Cambridge University.Google Scholar
  85. Seeley, T.D. (1985). Honeybee Ecology, Princeton NJ: Princeton University Press. Shipp, J.L., Whitfield, G.H. and Papadopoulos, A.P. (1994). Effectiveness of the bumblebee, Bombus impatiens Cr. (Hymenoptera, Apidae) as a pollinator of the greenhouse sweet pepper. Scientia Horticulturae 57, 29–39.Google Scholar
  86. Stace, C.A. (1997). New Flora of the British Isles, 2nd ed. Cambridge: Cambridge University Press.Google Scholar
  87. Stevenson, J.H. and Racey, P.A. (1966). Toxicity of Insecticides to Bumblebees. Report Rothamsted Experimental Station 176.Google Scholar
  88. Stoddard, F.L. and Bond, D.A. (1987). The pollination requirements of the faba bean. Bee World 68, 144–52.Google Scholar
  89. Stone, G.N. and Willmer, P.G. (1989). Warm-up rates and body temperature in bees; the importance of body-size, thermal regime and phylogeny. J. Exp. Biol. 147, 303–28.Google Scholar
  90. Tasei, J.N., Sabik, H. and Pirastru, L. (1994). Effects of sublethal doses of deltamethrin (Decis ce) on Bombus terrestris. J. Apic. Res. 33, 129–35.Google Scholar
  91. Teras, I. (1976). Bumblebees, Bombus Latr. (Hymenoptera, Apidae) on red clover in South Savo, Finland. Ann. Agric. Fenniae 15, 116–27.Google Scholar
  92. Teras, I. (1985). Food plants and flower visits of bumblebees (Bombus: Hymenoptera, Apidea) in Southern Finland. Acta Zool. Fennica 179, 1–120.Google Scholar
  93. van der Steen, J.J.M. (1994). Method development for the determination of the contact LD50 of pesticides to bumblebees (Bombus terrestris L.). Apidologie 25, 463–5.Google Scholar
  94. Voloshin, M., Voloshina, T. and Valter, V. (1995). Use of wild bees for alfalfa pollination. In Banaszak, J. (ed) Changes in Fauna of Wild Bees in Europe, pp. 220. Bydgoszez: Pedagogical University.Google Scholar
  95. Walton, C.L. (1927). Note on the activities of bumblebees (Bombus) in North Wales. Ann. Appl. Biol. 14, 465–9.Google Scholar
  96. Watkinson, A.R. and Bo, L. (1993). Patterns of abundance in the weed seed bank. In Proceedings of the Brighton Crop Protection Conference—Weeds, 22–25 November 1993, pp. 293–298. Farnham: BCPC.Google Scholar
  97. Williams, C.S. (1997). Foraging Ecology of Nectar-Collecting Bumblebees and Honeybees. PhD Thesis, University of Cambridge.Google Scholar
  98. Williams, I.H. (1985). The pollination of swede rape (Brassica napus L.). Bee World 66, 16–22.Google Scholar
  99. Williams, I.H. (1987). The pollination of lupins. Bee World 68, 10–6.Google Scholar
  100. Williams, I.H. (1988). The pollination of linseed and flax. Bee World 69, 145–52.Google Scholar
  101. Williams, I.H., Martin, A.P., Ferguson, A.W. and Clark, S.J. (1990). Effect of pollination on flower, pod and seed production in the white lupin (Lupinus albus). J. Agric. Sci. 115, 67–73.Google Scholar
  102. Williams, I.H., Carreck, N. and Little, D.J. (1993). Nectar sources for honeybees and the movement of honeybee colonies for crop pollination and honey production in England. Bee World 74, 160–75.Google Scholar
  103. Williams, I.H. and Free, J.B. (1974). The pollination of onion (Allium cepa L.) to produce hybrid seed. J. Appl. Ecol. 11, 409–18.Google Scholar
  104. Willmer, P.G. (1983). Thermal constraints on activity patterns in nectar feeding insects. Ecol. Entomol. 8, 455–69.Google Scholar
  105. Willmer, P.G., Bataw, A.A.M. and Hughes, J.P. (1994). The superiority of bumblebees to honeybees as pollinators; insect visits to raspberry flowers. Ecol. Entomol. 19, 271–84.Google Scholar
  106. Wilson, G.F. (1929). Pollination of hardy fruits: insect visitors to fruit blossoms. Ann. Appl. Biol. 16, 602–29.Google Scholar
  107. Yalden, P.E. (1982). Pollen collected by the bumblebee Bombus monticola (Smith) in the peak district, England. J. Natural History 16, 823–32.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  1. 1.National Bee UnitCentral Science LaboratoryYorkUnited Kingdom
  2. 2.Department of ZoologyUniversity of CambridgeCambridgeUnited Kingdom

Personalised recommendations