Skip to main content
Log in

The pollination potential of free-foraging bumblebee (Bombus spp.) males (Hymenoptera: Apidae)

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

Bumblebee workers are efficient pollinators. However, despite their flower visits and less intense grooming the role of males as pollen vectors is largely unexplored. We compared the quantity and diversity of pollen on the bodies (pollination-active pollen) of free-foraging workers and males of two bumblebee species (Bombus lapidarius and Bombus terrestris) to assess their pollination potential. In both species, males exhibit worker-like flower constancy, but differ significantly from workers in the predominantly collected pollen types. Mean pollen loads of approximately 10,000 grains/individual suggest that males can contribute to the colony pollination service. Bumblebee males add to the diversity of pollinators, associated to increased crop pollination and facilitate pollen flow in specific ways, worthwhile further investigation.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.

Similar content being viewed by others

References

  • Abbott, K.R. (2006) Bumblebees avoid flowers containing evidence of past predation events. Can. J. Zool. 84, 1240–1247

    Article  Google Scholar 

  • Ackerman, J.D., Mesler, M.R., Lu, K.L., Montalvo, A.M. (1982) Food-foraging behaviour of male Euglossini (Hymenoptera: Apidae)—vagabonds or trap-liners? Biotropica 14(4), 241–248

    Article  Google Scholar 

  • Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y., Lobo, J. (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol. Ecol. 17, 5177–5188

    Article  PubMed  Google Scholar 

  • Alcock, J., Barrows, E.M., Gordh, G., Hubbard, L.J., Kirkendall, L., Pyle, D.W., Ponder, T.L., Zalom, F.G. (1978) The ecology and evolution of male reproductive behaviour in the bees and wasps. Zool. J. Linn. Soc. 64, 293–326

    Article  Google Scholar 

  • Ayasse, M., Paxton, R.J., Tengö, J. (2001) Mating behaviour and chemical communication in the order Hymenoptera. Annu. Rev. Entomol. 46, 31–78

    Article  CAS  PubMed  Google Scholar 

  • Benatar, S.T., Cobey, S., Smith, B.H. (1995) Selection on a haploid genotype for discrimination learning performance: Correlation between drone honeybees (Apis mellifera) and their worker progeny (Hymenoptera: Apidae). J. Insect Behav. 8(5), 637–652

    Article  Google Scholar 

  • Bergman, R., Bergström, G. (1996) Scent marking, scent origin, and species specificity in male premating behaviour of two Scandinavian bumblebees. J. Chem. Ecol. 23(5), 1235–1251

    Article  Google Scholar 

  • Bertsch, A. (1984) Foraging in male bumblebees (Bombus lucorum L.): maximizing energy or minimizing water load? Oecologia 62, 325–336

    Article  Google Scholar 

  • Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354

    Article  CAS  PubMed  Google Scholar 

  • Bingham, R.A., Orthner, A.R. (1998) Efficient pollination of alpine plants. Nature 391, 238–239

    Article  Google Scholar 

  • Campbell, D.R. (1991) Comparing pollen dispersal and gene flow in a natural population. Evolution 45(8), 1965–1968

    Article  Google Scholar 

  • Carré, S., Badenhausser, I., Taséi, J.N., Le Guen, J., Mesquida, J. (1994) Pollen deposition by Bombus terrestris L. between male-fertile and male-sterile plants in Vicia faba L. Apidologie 25, 338–349

    Article  Google Scholar 

  • Cartar, R.V. (1991) A test of risk-sensitive foraging in wild bumblebees. Ecology 72(3), 888–895

    Article  Google Scholar 

  • Cartar, R.V., Dill, L.M. (1990) Colony energy requirements affect the foraging currency of bumblebees. Behav. Ecol. Sociobiol. 27, 377–383

    Article  Google Scholar 

  • Chase, M.R., Moller, C., Kesseli, R., Bawa, K.S. (1996) Distant gene-flow in tropical trees. Nature 383, 398–399

    Article  CAS  Google Scholar 

  • Chittka, L., Gumbert, A., Kunze, J. (1997) Foraging dynamics of bumblebees: correlates of movements within and between plant species. Behav. Ecol. 8(3), 239–249

    Article  Google Scholar 

  • Courtney, S.P., Hill, C.J., Westerman, A. (1982) Pollen carried for long periods by butterflies. Oikos 38(2), 260–263

    Article  Google Scholar 

  • Couvet, D. (2002) Deleterious effects of restricted gene flow in fragmented populations. Conserv. Biol. 16(2), 369–376

    Article  Google Scholar 

  • Darwin, C.R. (1886) Über die Wege der Hummelmännchen. In: Krause, E. (ed.) Gesammelte kleinere Schriften von Charles Darwin, 2nd edn, pp. 84–88. Germany, Leipzig

    Google Scholar 

  • Dukas, R. (2001) Effects of predation risk on pollinators and plants. In: Chittka, L., Thomson, J.D. (eds.) Cognitive Ecology of Pollination—Animal Behaviour and Floral Evolution, pp. 214–236. Cambridge University Press, Cambridge

    Chapter  Google Scholar 

  • Durrer, S., Schmid-Hempel, P. (1994) Shared use of flowers lead to horizontal pathogen transmission. Proc. R. Soc. Lond. B 258, 299–302

    Article  Google Scholar 

  • Duvoisin, N., Baer, B., Schmid-Hempel, P. (1999) Sperm transfer and male competition in a bumblebee. Anim. Behav. 58, 743–749

    Article  PubMed  Google Scholar 

  • Eickwort, G.C., Ginsberg, H.S. (1980) Foraging and mating behaviour in Apoidea. Annu. Rev. Entomol. 25, 421–446

    Article  Google Scholar 

  • Free, J.B., Williams, I.H. (1972) The transport of pollen on the body hairs of honeybees (Apis mellifera L.) and bumblebees (Bombus spp. L.). J. Appl. Ecol. 9(2), 609–615

    Article  Google Scholar 

  • Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., et al. (2013) Wild pollinators enhance fruit set of crops regardless of honeybee abundance. Science 339, 1608–1611

    Article  CAS  PubMed  Google Scholar 

  • Gegear, R.J., Laverty, T.M. (2005) Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim. Behav. 69, 939–949

    Article  Google Scholar 

  • GenStat for Windows 14th Edition. VSN International, Hemel Hempstead, UK. Web page: genstat.co.uk.

  • Ghazoul, J. (2005) Pollen and seed dispersal among dispersed plants. Biol. Rev. 80, 413–443

    Article  PubMed  Google Scholar 

  • Gögler, J., Stökl, J., Sramkova, A., Twele, R., Francke, W., Cozzolino, S., Cortis, P., Scrugli, A., Ayasse, M. (2009) Menage à Trois—two endemic species of deceptive orchids and one pollinator species. Evolution 63(9), 2222–2234

    Article  PubMed  Google Scholar 

  • Goulson, D. (2003) Bumblebees—Behaviour and Ecology. United Kingdom, Oxford University Press, Oxford

    Google Scholar 

  • Goulson, D., Hawson, S.A., Stout, J.C. (1997) Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Anim. Behav. 55, 199–206

    Article  Google Scholar 

  • Haas, A. (1949) Arttypische Flugbahnen von Hummelmännchen. Z. Vergl. Physiol. 31, 381–387

    Article  Google Scholar 

  • Hagbery, J., Nieh, J.C. (2012) Individual lifetime pollen and nectar foraging preferences in bumblebees. Naturwissenschaften 99, 821–832

    Article  CAS  PubMed  Google Scholar 

  • Harder, L.D. (1985) Morphology as a predictor of flower choice by bumblebees. Ecology 66(1), 198–210

    Article  Google Scholar 

  • Heinrich, B. (1976) The foraging specializations of individual bumblebees. Ecol. Monogr. 46, 105–128

    Article  Google Scholar 

  • Heinrich, B. (1979a) “Majoring” and “minoring” by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology 60(2), 245–255

    Article  Google Scholar 

  • Heinrich, B. (1979b) Bumblebee Economics. Harvard Univ. Press, Cambridge

    Google Scholar 

  • Herrera, C.M. (1987) Components of pollinator “quality”: comparative analysis of a diverse insect assemblage. Oikos 50, 79–90

    Article  Google Scholar 

  • Inouye, D.W. (1980) The effect of proboscis and corolla tube length son patterns and rates of flower visitation by bumblebees. Oecologia 45, 197–201

    Article  Google Scholar 

  • Kevan, P.G., Baker, H.G. (1983) Insects as flower visitors and pollinators. Ann. Rev. Entomol. 28, 407–453

    Google Scholar 

  • Klein, A.M., Steffan-Dewenter, I., Tschantke, T. (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc. R. Soc. Lond. B 270, 955–961

    Article  Google Scholar 

  • Kraus, F.B., Wolf, S., Moritz, R.F.A. (2009) Male flight distance and population substructure in the bumblebee Bombus terrestris. J. Anim. Ecol. 78, 247–252

    Article  CAS  PubMed  Google Scholar 

  • Kwak, M.M., Velterop, O., Andel, J. (1998) Pollen and gene flow in fragmented habitats. Appl. Veg. Sci. 1, 37–54

    Article  Google Scholar 

  • Laloi, D., Sandoz, J.C., Picard-Nizou, A.L., Marchesi, A., Pouvreau, A., Taséi, J.N., Poppy, G., Pham-Delègue, M.H. (1999) Olfactory conditioning of the proboscis extension in bumblebees. Entomol. Exp. Appl. 90, 123–129

    Article  Google Scholar 

  • Lihoreau, M., Chittka, L., Raine, N.E., Kudo, G. (2011) Trade-off between travel distance and prioritization of high-reward sites in traplining bumblebees. Funct. Ecol. 25(6), 1284–1292

    Article  PubMed Central  PubMed  Google Scholar 

  • Lihoreau, M., Raine, N.E., Reynolds, A.M., Stelzer, R.J., Lim, K.S., Smith, A.D., Osborne, J.L., Chittka, L. (2012) Radar tracking and motion-sensitive cameras on flowers reveal the development of pollinator multi-destination routes over large spatial scales. PLoS Biol. 10(9), e1001392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mauss V. (1994) Bestimmungsschlüssel für Hummeln. Hamburg, Germany. Deutscher Jugendbund für Naturbeobachtungen (DJN)

  • Menzel, R. (2001) Behavioural and neural mechanisms of learning and memory as determinants of flower constancy. In: Chittka, L., Thomson, J.D. (eds.) Cognitive Ecology of Pollination—Animal Behaviour and Floral Evolution, pp. 21–40. Cambridge University Press, Cambridge

    Chapter  Google Scholar 

  • Midgley, J.J., Bond, W.J. (1991) Ecological aspects of the rise of angiosperms: a challenge to the reproductive superiority hypotheses. Biol. J. Linn. Soc. 44, 81–92

    Article  Google Scholar 

  • Moeller, D.A. (2005) Pollinator community structure and sources of spatial variation in plant–pollinator interactions in Clarkia xantiana spp. xantiana. Oecologia 142, 28–37

    Article  PubMed  Google Scholar 

  • Nilsson, L.A., Johnsson, L., Ralison, L., Randrianjohany, E. (1987) Angraecoid Orchids and Hawkmoths in Central Madagascar: Specialized Pollination Systems and Generalist Foragers. Biotropica 19(4), 310–318

    Article  Google Scholar 

  • Osborne, J.L., Martin, A.P., Carreck, N.L., Swain, J.L., Knight, M.E., Goulson, D., Hale, R.J., Sanderson, R.A. (2008) Bumblebee flight distances in relation to the forage landscape. J. Anim. Ecol. 77, 406–415

    Article  PubMed  Google Scholar 

  • Ostervik, K.L., Manson, J.S., Thomson, J.D. (2010) Pollination potential of male bumblebees (Bombus impatiens): Movement patterns and pollen transfer efficiency. J. Poll. Ecol. 2(4), 21–26

    Google Scholar 

  • Pyke, G.H. (1978) Optimal foraging: movement patterns of bumblebees between inflorescences. Theor. Popul. Biol. 13, 72–98

    Article  CAS  PubMed  Google Scholar 

  • Raine, N.E., Chittka, L. (2005) Comparison of flower constancy and foraging performance in three bumblebee species (Hymenoptera: Apidae: Bombus). Entomol. Gen. 28(2), 81–89

    Article  Google Scholar 

  • Raine, N.E., Chittka, L. (2007) Flower constancy and memory dynamics in bumblebees (Hymenoptera: Apidae: Bombus). Entomol. Gen. 29(2/4), 179–199

    Google Scholar 

  • Raine, N.E., Chittka, L. (2008) The correlation of learning speed and natural foraging success in bumblebees. Proc. R. Soc. Lond. B 275, 803–808

    Article  Google Scholar 

  • Ranta, E., Lundberg, H. (1981) Resource utilization by bumblebee queens, workers and males in a subarctic area. Hol. Ecol. 4, 145–154

    Google Scholar 

  • Real, L.A. (1991) Animal choice behaviour and the evolution of cognitive architecture. Science 253(5023), 980–986

    Article  CAS  PubMed  Google Scholar 

  • Sargent, R.D., Ackerly, D.D. (2008) Plant–pollinator interactions and the assembly of plant communities. Trends Ecol. Evol. 23(3), 123–130

    Article  PubMed  Google Scholar 

  • Sork, V.L., Nason, J., Campbell, D.R., Fernandez, J.F. (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol. Evol. 14(6), 219–224

    Article  PubMed  Google Scholar 

  • Spaethe, J., Weidenmüller, A. (2002) Size variation and foraging rate in bumblebees (Bombus terrestris). Insectes Soc. 49(2), 142–146

    Article  Google Scholar 

  • Svensson, B.G. (1979) Patrolling behaviour of bumblebee males (Hymenoptera: Apidae) in a Subalpine/Alpine Area, Swedish Lapland. Zoon. 7, 67–94

    Google Scholar 

  • Thomson, J.D. (1986) Pollen transport and deposition by bumblebees in Erythronium: Influences of floral nectar and bee grooming. J. Ecol. 74(2), 29–341

    Article  Google Scholar 

  • Thomson, J.D., Plowright, R.C. (1980) Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46, 68–74

    Article  Google Scholar 

  • Thorp, R.W. (1979) Structural, behavioural and physiological adaptations of bees (Apoidea) for collecting pollen. Ann. Missouri Bot. Gard. 66(4), 788–812

    Article  Google Scholar 

  • Von der Ohe, K., von der Ohe, W. (2003) Celle’s Melissiopalynological collection, 2nd edn. Niedersächsisches Landesinstitut für Bienenkunde Celle, Celle

    Google Scholar 

  • Waddington, K.D. (2001) Subjective evaluation and choice behaviour by nectar- and pollen collecting bees. In: Chittka, L., Thomson, J.D. (eds.) Cognitive Ecology of Pollination—Animal Behaviour and Floral Evolution, pp. 41–60. Cambridge University Press, Cambridge

    Chapter  Google Scholar 

  • Waser, N.M. (1986) Flower constancy: definition, cause and measurement. Am. Nat. 27(5), 593–603

    Article  Google Scholar 

  • Weiss, M.R. (2001) Vision and learning in beetles, flies, moth and butterflies. In: Chittka, L., Thomson, J.D. (eds.) Cognitive Ecology of Pollination—Animal Behaviour and Floral Evolution, pp. 171–190. Cambridge University Press, Cambridge

    Chapter  Google Scholar 

  • Westerkamp, C. (1991) Honeybees are poor pollinators—why? Plant Syst Evol. 177, 71–75

    Article  Google Scholar 

  • Wolf, S., Moritz, R.F.A. (2008) Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae). Apidologie 39, 419–427

    Article  Google Scholar 

  • Wolf, S., Toev, T., Moritz, R.V., Moritz, R.F.A. (2012) Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae). Popul. Ecol. 54(1), 115–124

    Article  Google Scholar 

  • Wolfe, L.M., Barrett, S.C.H. (1989) Patterns of pollen removal and deposition in tristylous Pontederia cordata (Pontederiaceae). Biol. J. Linn. Soc. 36, 317–329

    Article  Google Scholar 

Download references

Acknowledgments

We like to thank Susan Brich, Stephanie Gerschke, Diana Oelschlägel, Olga Skljar and Maria Tauber for valuable help during field work. Thanks to F. B. Kraus and two anonymous reviewers for constructive comments that clearly improved the manuscript. This study was funded by the EU—Project ALARM (Assessing LArge scale Risks for biodiversity with tested Methods; Pollinator Module, EU Contract No.: 506675). Rothamsted Research is a national institute of bioscience strategically funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephan Wolf.

Additional information

Le potentiel de pollinisation des bourdons mâles, Bombus spp. (Hymenoptera: Apidae) butinant pour eux-mêmes

Bourdon / mâle / charge pollinique / rôle pollinisateur d’une colonie/fidélité florale

Das Bestäubungspotential von freifliegenden Hummelmännchen (Bombus spp., Hymenoptera: Apidae)

Hummelmännchen / Pollenladungen / Bestäubungsservice / Blütenstetigkeit

Manuscript editor: James Nieh

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wolf, S., Moritz, R.F.A. The pollination potential of free-foraging bumblebee (Bombus spp.) males (Hymenoptera: Apidae). Apidologie 45, 440–450 (2014). https://doi.org/10.1007/s13592-013-0259-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0259-9

Keywords

Navigation