Skip to main content
SpringerLink
Log in

Pollen and nectar quality drive the major and minor floral choices of bumble bees

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

Abstract

To investigate whether floral resource quality impacts on bumble bee floral choices, we determined the pollen foraging constancy and floral choices of four bumble bee species commonly occurring in peaty, wet meadows in South Belgium. We subsequently analyzed the chemical contents of pollen and nectar, as well as the nectar production of the major host plant species. Individuals of B. lapidarius and B. pascuorum collected high-quality pollen (i.e., having high essential amino acid and phytosterol content) on Comarum palustre and Trifolium pratense, whereas individuals of B. terrestris s.l. and B. hypnorum enlarged their diet breadth to less valuable pollen resources (Cirsium palustre and Valeriana repens). Since Persicaria bistorta and Comarum palustre offer abundant and concentrated nectar, these plant species might represent major nectar sources for bumble bee species in peaty, wet meadows. The present study demonstrated the role of pollen composition on differences in foraging strategies among bumble bee species.

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.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

REFERENCES

  • Ayasse, M., Stökl, J., Francke, W. (2011) Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. Phytochemistry, Plant-Insect Interact. 72, 1667–1677

    CAS  Google Scholar 

  • Baker, H.G., Baker, I. (1990) The predictive value of nectar chemistry to the recognition of pollinator types. Isr. J. Bot. 39, 157–166

    CAS  Google Scholar 

  • Behmer, S.T., Nes, W.D. (2003) Insect sterol nutrition and physiology: a global overview. Adv. Insect Physiol. 31, 1–72

  • Benton, T. (2006) Bumblebees: the natural history & identification of the species found in Britain. Collins, London

    Google Scholar 

  • Beug, H.-J. (2004) Leitfaden der Pollenbestimmung für Mitteleuropa und angrenzende Gebiete. Friedrich Pfeil, München, Germany

    Google Scholar 

  • Canavoso, L.E., Jouni, Z.E., Karnas, K.J., Pennington, J.E., Wells, M.A. (2001) Fat metabolism in insects. Annu. Rev. Nutr. 21, 23–46

    Article  CAS  PubMed  Google Scholar 

  • Carolan, J.C., Murray, T.E., Fitzpatrick, Ú., Crossley, J., Schmidt, H., Cederberg, B., McNally, L., Paxton, R.J., Williams, P.H., Brown, M.J.F. (2012) Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex. PLoS ONE 7, e29251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carter, C., Shafir, S., Yehonatan, L., Palmer, R.G., Thornburg, R. (2006) A novel role for proline in plant floral nectars. Naturwissenschaften 93, 72–79

    Article  CAS  PubMed  Google Scholar 

  • Carvalheiro, L.G., Kunin, W.E., Keil, P., Aguirre-Gutiérrez, J., Ellis, W.N., Fox, R., Groom, Q., Hennekens, S., Van Landuyt, W., Maes, D., et al. (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol. Lett. 16, 870–878

    Article  PubMed Central  PubMed  Google Scholar 

  • Carvell, C. (2002) Habitat use and conservation of bumblebees (Bombus spp.) under different grassland management regimes. Biol. Conserv. 103, 33–49

    Article  Google Scholar 

  • Carvell, C., Westrich, P., Meek, W.R., Pywell, R.F., Nowakowski, M. (2006) Assessing the value of annual and perennial forage mixtures for bumblebees by direct observation and pollen analysis. Apidologie 37, 326–340

    Article  Google Scholar 

  • Chapman, R.F. (2012) The insects: structure and function, 5th edn. Cambridge University Press, USA

  • Cnaani, J., Thomson, J.D., Papaj, D.R. (2006) Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112, 278–285

    Article  Google Scholar 

  • Cohen, A.C. (2004) Insect diets: science and technology. CRC Press, Boca Raton

    Google Scholar 

  • Comba, L., Corbet, S.A., Hunt, L., Warren, B. (1999) Flowers, nectar and insect visits: evaluating British plant species for pollinator-friendly gardens. Ann. Bot. 83, 369–383

    Article  Google Scholar 

  • Connop, S., Hill, T., Steer, J., Shaw, P. (2010) The role of dietary breadth in national bumblebee (Bombus) declines: simple correlation? Biol. Conserv. 143, 2739–2746

    Article  Google Scholar 

  • Cook, S.M., Awmack, C.S., Murray, D.A., Williams, I.H. (2003) Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol. Entomol. 28, 622–627

    Article  Google Scholar 

  • Corbet, S.A. (2003) Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34, 1–10

    Article  CAS  Google Scholar 

  • Day, S., Beyer, R., Mercer, A., Odgen, S. (1990) The nutrient composition of honeybee-collected pollen in Otago, New Zealand. J. Apic. Res. 29, 138–146

    Google Scholar 

  • De Groot, A.P. (1953) Protein and amino acid requirements of the honeybee (Apis mellifera L.). Physiol Comp Oecologia 3, 197–285

    Google Scholar 

  • Dufrêne, M., Legendre, P. (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366

    Google Scholar 

  • Erdtman, G. (1960) The acetolysis method. A revised description. Svensk Botanisk Tidskrift 54, 561–564

    Google Scholar 

  • Fontaine, C., Collin, C.L., Dajoz, I. (2008) Generalist foraging of pollinators: diet expansion at high density. J. Ecol. 96, 1002–1010

    Article  Google Scholar 

  • Frankard, P., Ghiette, P., Hindryckx, M.-N., Schumacker, R., Wastiaux, C. (1998) Peatlands of Wallony (S-Belgium). Suoseura - Finnish Peatland Society 49, 33–47

    Google Scholar 

  • Génissel, A., Aupinel, P., Bressac, C., Tasei, J.-N., Chevrier, C. (2002) Influence of pollen origin on performance of Bombus terrestris micro-colonies. Entomol. Exp. Appl. 104, 329–336

    Article  Google Scholar 

  • Gibbs, J.P. (2000) Pérdida de Humedales y Conservación de la Biodiversidad. Conserv. Biol. 14, 314–317

    Article  Google Scholar 

  • Gonzalez-Teuber, M., Heil, M. (2009) Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal. Behav. 4, 809–813

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goslee, S., Urban, D. (2007) The ecodist package for dissimilarity-based analysis of ecological data. J. Stat. Softw. 22, 1–19

    Google Scholar 

  • Goulson, D. (2009) Bumblebees: behaviour, ecology, and conservation, 2nd edn. Oxford University Press, USA

    Google Scholar 

  • Goulson, D., Darvill, B. (2004) Niche overlap and diet breadth in bumblebees: are rare species more specialized in their choice of flowers? Apidologie 35, 9

    Google Scholar 

  • Goulson, D., Lye, G.C., Darvill, B. (2008) Decline and conservation of bumble bees. Annu. Rev. Entomol. 53, 191–208

    Article  CAS  PubMed  Google Scholar 

  • Gruter, C., Ratnieks, F.L.W. (2011) Flower constancy in insect pollinators. Commun. Integr. Biol. 4, 633–636

    Article  PubMed Central  PubMed  Google Scholar 

  • Guillén, A., Rico, E., Castroviejo, S. (2005) Reproductive biology of the Iberian species of Potentilla L. (Rosaceae). Reprod. Biol. 62, 9–21

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hanley, M.E., Franco, M., Pichon, S., Darvill, B., Goulson, D. (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct. Ecol. 22, 592–598

    Article  Google Scholar 

  • Harder, L.D. (1986) Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69, 309–315

    Article  Google Scholar 

  • Human, H., Nicolson, S.W., Strauss, K., Pirk, C.W.W., Dietemann, V. (2007) Influence of pollen quality on ovarian development in honeybee workers (Apis mellifera scutellata). J. Insect Physiol. 53, 649–655

    Article  CAS  PubMed  Google Scholar 

  • Ishii, H.S. (2005) Analysis of bumblebee visitation sequences within single bouts: implication of the overstrike effect on short-term memory. Behav. Ecol. Sociobiol. 57, 599–610

    Article  Google Scholar 

  • Janson, E.M., Grebenok, R.J., Behmer, S.T., Abbot, P. (2009) Same host-plant, different sterols: variation in sterol metabolism in an insect herbivore community. J. Chem. Ecol. 35, 1309–1319

    Article  CAS  PubMed  Google Scholar 

  • Juillet, N., Scopece, G. (2010) Does floral trait variability enhance reproductive success in deceptive orchids? Perspect. Plant Ecol. Evol. Syst. 12, 317–322

    Article  Google Scholar 

  • Kindt, R., Coe, R. (2005) Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi. ISBN 92-9059-179-X

  • Kitaoka, T.K., Nieh, J.C. (2009) Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav. Ecol. Sociobiol. 63, 625–625

    Article  Google Scholar 

  • Kleijn, D., Raemakers, I. (2008) A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89, 1811–1823

    Article  PubMed  Google Scholar 

  • Leonhardt, S.D., Blüthgen, N. (2012) The same, but different: pollen foraging in honeybee and bumblebee colonies. Apidologie 43, 449–464

    Article  Google Scholar 

  • Liao, K., Gituru, R.W., Guo, Y.-H., Wang, Q.-F. (2011) The presence of co-flowering species facilitates reproductive success of Pedicularis monbeigiana (Orobanchaceae) through variation in bumble-bee foraging behaviour. Ann. Bot. 108, 877–884

    Article  PubMed Central  PubMed  Google Scholar 

  • Lognay, G., Severin, M., Boenke, A., Wagstaffe, P.J. (1992) Edible fats and oils reference materials for sterols analysis with particular attention to cholesterol. Part 1. Investigation of some analytical aspects by experienced laboratories. Analyst 117, 1093–1097

    Article  CAS  Google Scholar 

  • Mayer, C., Michez, D., Chyzy, A., Brédat, E., Jacquemart, A.-L. (2012) The abundance and pollen foraging behaviour of bumble bees in relation to population size of whortleberry (Vaccinium uliginosum). PLoS ONE 7, e50353

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Michener, C.D. (2007) The bees of the world. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Nicolson, S.W. (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr. Zool. 46, 197–204

    Article  Google Scholar 

  • Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H. (2013) Vegan: Community Ecology Package. R package version 1.17-0. Available: http://CRAN.R-project.org/package=vegan

  • Ollerton, J., Winfree, R., Tarrant, S. (2011) How many flowering plants are pollinated by animals? Oikos 120, 321–326

    Article  Google Scholar 

  • Pelletier, L., McNeil, J.N. (2003) The effect of food supplementation on reproductive success in bumblebee field colonies. Oikos 103, 688–694

    Article  Google Scholar 

  • Percival, M.S. (1961) Types of nectar in Angiosperms. New Phytol. 60, 235–281

    Article  Google Scholar 

  • Proctor, M., Yeo, P., Lack, A. (1996) The natural history of pollination. Timber Press Inc., Oregon, USA

  • Prys-Jones, O.E., Corbet, S.A. (2011) Bumblebees: 6, 3rd edn. Pelagic Publishing, Exeter, England

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. [WWW Document]. URL http://www.R-project.org

  • Raguso, R.A. (2004) Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. Curr. Opin. Plant Biol. 7, 434–440

    Article  PubMed  Google Scholar 

  • Rasmont, P., Regali, A., Ings, T.C., Lognay, G., Baudart, E., Marlier, M., Delcarte, E., Viville, P., Marot, C., Falmagne, P., Verhaeghe, J.-C., Chittka, L. (2005) Analysis of pollen and nectar of Arbutus unedo as a food source for Bombus terrestris (Hymenoptera: Apidae). J. Econ. Entomol. 98, 656–663

    Article  CAS  PubMed  Google Scholar 

  • Roberts, D.W. (2012) labdsv: Ordination and Multivariate Analysis for Ecology. R package version 1.4-1. Available: http://CRAN.R-project.org/package=labdsv

  • Robertson, A.W., Mountjoy, C., Faulkner, B.E., Roberts, M.V., Macnair, M.R. (1999) Bumble bee selection of Mimulus guttatus flowers: the effects of pollen quality and reward depletion. Ecology 80, 2594–2606

    Article  Google Scholar 

  • Roulston, T.H., Cane, J.H. (2000) Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222, 187–209

    Article  CAS  Google Scholar 

  • Roulston, T.H., Cane, J.H., Buchmann, S.L. (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol. Monogr. 70, 617–643

    Google Scholar 

  • Roulston, T.H., Goodell, K. (2011) The Role of Resources and Risks in Regulating Wild Bee Populations. Annu. Rev. Entomol. 56, 293–312

  • Schlindwein, C., Wittmann, D., Martins, C.F., Hamm, A., Siqueira, J.A., Schiffler, D., Machado, I.C. (2005) Pollination of Campanula rapunculus L. (Campanulaceae): how much pollen flows into pollination and into reproduction of oligolectic pollinators? Plant Syst. Evol. 250, 147–156

    Google Scholar 

  • Sedivy, C., Müller, A., Dorn, S. (2011) Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: evidence for physiological adaptations to digest pollen. Funct. Ecol. 25, 718–725

    Article  Google Scholar 

  • Somme, L., Mayer, C., Jacquemart, A.-L. (2014) Multilevel spatial structure impacts on the pollination services of Comarum palustre (Rosaceae). PLoS ONE 9, e99295

    Article  PubMed Central  PubMed  Google Scholar 

  • Southwick, E.E., Loper, G.M., Sadwick, S.E. (1981) Nectar production, composition, energetics and pollinator attractiveness in spring flowers of Western New York. Am. J. Bot. 68, 994–1002

    Article  CAS  Google Scholar 

  • Sowig, P. (1989) Effects of flowering plant’s patch size on species composition of pollinator communities, foraging strategies, and resource partitioning in bumblebees (Hymenoptera: Apidae). Oecologia 78, 550–558

    Article  Google Scholar 

  • Standifer, L.N., McCaughey, W.F., Dixon, S.E., Gilliam, M., Loper, G.M. (1980) Biochemistry and microbiology of pollen collected by honey bees (Apis mellifera L.) from almond, Prunus dulcis. II. Protein, amino acids and enzymes. Apidologie 11, 163–171

    Article  CAS  Google Scholar 

  • Stout, J.C., Goulson, D. (2002) The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behav. Ecol. Sociobiol. 52, 239–246

    Article  Google Scholar 

  • Svoboda, J.A., Thompson, M.J., Herbert, E.W., Shimanuki, H. (1980) Sterol utilization in honey bees fed a synthetic diet: analysis of prepupal sterols. J. Insect Physiol. 26, 291–294

    Article  CAS  Google Scholar 

  • Tasei, J.-N., Aupinel, P. (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera: Apidae). Apidologie 39, 397–409

    Article  CAS  Google Scholar 

  • Vanderplanck, M., Leroy, B., Wathelet, B., Wattiez, R., Michez, D. (2014a) Standardized protocol to evaluate pollen polypeptides as bee food source. Apidologie 45, 192–204

    Article  CAS  Google Scholar 

  • Vanderplanck, M., Michez, D., Vancraenenbroeck, S., Lognay, G. (2011) Micro-quantitative method for analysis of sterol levels in honeybees and their pollen loads. Anal. Lett. 44, 1807–1820

    Article  CAS  Google Scholar 

  • Vanderplanck, M., Moerman, R., Rasmont, P., Lognay, G., Wathelet, B., Wattiez, R., Michez, D. (2014b) How does pollen chemistry impact development and feeding behaviour of polylectic bees? PLoS ONE 9, e86209

    Article  PubMed Central  PubMed  Google Scholar 

  • Verté, P. (2007) Les marais de la Haute-Semois, 40 années de conservation d’un site de très grand intérêt biologique. Echo des Réserves 3, 4–9

    Google Scholar 

  • Waser, N.M. (1986) Flower constancy: definition, cause, and measurement. Am. Nat. 127, 593–603

    Article  Google Scholar 

  • Waser, N.M., Ollerton, J. (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago

    Google Scholar 

  • Waters, J., Darvill, B., Lye, G.C., Goulson, D. (2011) Niche differentiation of a cryptic bumblebee complex in the Western Isles of Scotland. Insect Conserv. Divers. 4, 46–52

    Article  Google Scholar 

  • Weiner, C.N., Hilpert, A., Werner, M., Linsenmair, K.E., Blüthgen, N. (2010) Pollen amino acids and flower specialisation in solitary bees. Apidologie 41, 476–487

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank the Belgian Fund for Scientific Research (FNRS contract 2.4540.09) for funding this study. LS holds a FRIA fellowship (Funds for training in Industry and Agriculture Research) and MV holds an aspirant FNRS fellowship. The study was conducted in accordance with current Belgian laws. We thank the “Département de la Nature et des Forêts” (DNF, Région Wallonne, Belgium) for the derogation concerning the sampling of plant and insect individuals in nature reserves, the DNF and Natagora for granting access to their properties, and Christel Buyens and Isabelle Van de Vreken for technical assistance.

Author information

Authors and Affiliations

  1. Earth and Life Institute – Research group Genetics, Reproduction, Populations, Université catholique de Louvain (UCL), Croix-du-Sud 2, Box L7.05.14, 1348, Louvain-la-Neuve, Belgium

    Laurent Somme, Isabelle Lombaerde & Anne-Laure Jacquemart

  2. Laboratory of Zoology, University of Mons - UMONS, Place du Parc 20, 7000, Mons, Belgium

    Maryse Vanderplanck, Denis Michez & Romain Moerman

  3. Industrial Biological Chemistry unit, Gembloux Agro-Bio Tech, University of Liège, Passage des Déportés 2, 5030, Gembloux, Belgium

    Bernard Wathelet

  4. Department of Proteomic and Protein Biochemistry, University of Mons - UMONS, Place du parc 20, 7000, Mons, Belgium

    Ruddy Wattiez

  5. Unit of Analytical Chemistry, Gembloux Agro-Bio Tech, University of Liège, Passage des Déportés 2, 5030, Gembloux, Belgium

    Georges Lognay

  6. Evolutionary Biology & Ecology, Université Libre de Bruxelles (ULB), Avenue F.D. Roosevelt 50, 1050, Brussels, Belgium

    Romain Moerman

Authors
  1. Laurent Somme
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maryse Vanderplanck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Denis Michez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabelle Lombaerde
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Romain Moerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bernard Wathelet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ruddy Wattiez
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Georges Lognay
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anne-Laure Jacquemart
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laurent Somme.

Additional information

Manuscript editor: James Nieh

La qualité du pollen et du nectar conditionne les choix, prioritaires ou secondaires, des fleurs par les bourdons

Acides aminés / récompense / sucre du nectar / phytostéroles / polyectisme

Die Pollen- und Nektarqualität beeinflusst die Blütenauswahl bei Hummeln

Aminosäuren / Blütenbelohnung / Nektarzucker / Phytosterole / Polylektie

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOC 174 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Somme, L., Vanderplanck, M., Michez, D. et al. Pollen and nectar quality drive the major and minor floral choices of bumble bees. Apidologie 46, 92–106 (2015). https://doi.org/10.1007/s13592-014-0307-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-014-0307-0

Keywords

Search

Navigation