Abstract
Like many other bees worldwide, honeybees and bumblebees are threatened by human-induced disturbances. Yet some species decline and others thrive, likely due to different foraging strategies. As little is known about how resource intake translates into nutrients available to colonies, our study aimed to better understand how differences in foraging strategies may affect colony health by relating differences in pollen spectra collected to differences in nutrient composition. The Apis and Bombus colonies studied were all located at the same site, but nevertheless differed in the spectra of plant species visited for pollen collection and the quality of pollen collected. Bumblebees generally collected pollen with significantly higher pollen protein content and more essential amino acids. Unlike honeybees that tend to exploit large resource patches, bumblebees thus seem to select the “better” pollen and to focus on quality instead of quantity.
Similar content being viewed by others
References
Aizen, M.A., Feinsinger, P. (2003) Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. In: Bradshaw, G., Marquet, P., Mooney, H.A. (eds.) How Landscapes Change: Human Disturbance and Ecosystem Disruption in the Americas, pp. 111–129. Springer, New York
Banaszak, J. (1995) Changes in Fauna of Wild Bees in Europe. Pedagogical University, Bydgoszcz
Benton, T. (2006) Bumble Bees: The Natural History and Identification of the Species Found in Britain. Collins, London
Beug H.-J. (2004) Leitfaden der Pollenbestimmung: für Mitteleuropa und angrenzende Gebiete, Dr. Friedrich Pfeil, München, Germany
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354
Blüthgen, N., Menzel, F., Blüthgen, N. (2006) Measuring specialization in species interaction networks. BMC Ecol. 6, 9
Bommarco, R., Biesmeijer, J.C., Meyer, B., Potts, S.G., Pöyry, J., Roberts, S.P.M., Steffan-Dewenter, I., Öckinger, E. (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc. R. Soc. Lond. B 277, 2075–2082
Bommarco, R., Lundin, O., Smith, H.G., Rundlöf, M. (2011) Drastic historic shifts in bumble-bee community composition in Sweden. Proc. R. Soc. Lond. B. doi:10.1098/rspb.2011.0647
Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F., Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. U. S. A 108, 662–667
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
Crawley, M.J. (2008) The R Book. Wiley, Chichester
Darvill, B., Knight, M.E., Goulson, D. (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107, 471–478
de Groot, A.P. (1953) Protein and amino acid requirements of the honey bee (Apis mellifera L.). Physiol. Comp. Oecol. 3, 197–285
Devictor, V., Julliard, R., Jiguet, F. (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117, 507–514
Dietz, A. (1992) Nutrition of the adult honeybee. In: Graham, J.M. (ed.) The Hive and the Honeybee, pp. 125–156. Dadant and Sons, Hamilton
Dormann, C.F. (2008) Angewandte Statistik für die biologischen Wissenschaften. Helmholtz Zentrum für Umweltforschung-UFZ, Leipzig
Fitzpatrick, U., Murray, T.E., Paxton, R.J., Breen, J., Cotton, D., Santorum, V., Brown, M.J.F. (2007) Rarity and decline in bumblebees—a test of causes and correlates in the Irish fauna. Biol. Conserv. 136, 185–194
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
Goulson, D., Darvill, B. (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35, 55–63
Goulson, D., Hanley, M.E., Darvill, B., Ellis, J.S., Knight, M.E. (2005) Causes of rarity in bumblebees. Biol. Conserv. 122, 1–8
Goulson, D., Lye, G.C., Darvill, B. (2008) Decline and conservation of bumblebees. Annu. Rev. Entomol. 53, 191–208
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
Haydak, M.H. (1970) Honey bee nutrition. Annu. Rev. Entomol. 15, 146–156
Heinrich, B. (1976) The foraging specializations of individual bumblebees. Ecol. Monogr. 46, 105–128
Heinrich, B. (1979) Majoring and minoring by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology 60, 245–255
Heinrich, B., Mudge, P.R., Deringis, P.G. (1977) Laboratory analysis of flower constancy in foraging bumblebees: Bombus ternarius and B. terricola. Behav. Ecol. Sociobiol. 2, 247–265
Herbert, E.W. (1992) Honey bee nutrition. In: Graham, J.E. (ed.) The Hive and the Honey Bee. Dadant and Sons, Hamilton
Herbert, E.W.J., Miller-Ihli, N.J. (1987) Seasonal variation of seven minerals in honey bee collected pollen. Am. Bee J. 127, 367–369
Hines, H.M., Hendrix, S.D. (2005) Bumble bee (Hymenoptera: Apidae) diversity and abundance in tallgrass prairie patches: effects of local and landscape floral resources. Environ. Entomol. 34, 1477–1484
Johnson, S.D., Steiner, K.E. (2000) Generalization versus specialization in plant pollination systems. Trends Ecol. Evol. 15, 140–143
Keller, I., Fluri, P., Imdorf, A. (2005) Pollen nutrition and colony development in honey bees: part I. Bee World 86, 3–10
Kitaoka, T.K., Nieh, J.C. (2009) Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav. Ecol. Sociobiol. 63, 501–510
Kleijn, D., Raemakers, I. (2008) A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89, 1811–1823
Klein, A.M. (2011) Plant–pollinator interactions in changing environments. Basic Appl. Ecol. 12, 279–281
Klein, A.M., Vaissiere, B.E., Cane, J.H., Cunningham, S., Kremen, C., Tscharntke, T. (2007a) The role of pollinators for global crop production. Ecol. Soc. Am. Annu. Meet. Abstracts
Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T. (2007b) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. Lond. B 274, 303–313
Kosior, A., Celary, W., Olejniczak, P., Fijal, J., Król, W., Solarz, W., Plonka, P. (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of western and central Europe. Oryx 41, 79–88
Kratochwil, A., Kohl, A. (1988) Pollensammel-Präferenzen bei Hummeln - ein Vergleich mit der Honigbiene, Mittelbadischer Landesverb. Nat.kd. Nat.schutz 3, 697–715
Leonhardt, S.D., Dworschak, K., Eltz, T., Blüthgen, N. (2007) Foraging loads of stingless bees and utilisation of stored nectar for pollen harvesting. Apidologie 38, 125–135
Leonhardt, S.D., Schmitt, T., Blüthgen, N. (2011) Tree resin composition, collection behavior and selective filters shape chemical profiles of tropical bees (Apidae: Meliponini). PLoS One 6, e23445
Michener, C.D. (2007) The Bees of the World. Johns Hopkins University Press, Baltimore
Munidasa, D.T., Toquenaga, Y. (2010) Do pollen diets vary among adjacent bumble bee colonies? Ecol. Res. 25, 639–646
National Research Council (2007) Status of Pollinators in North America. The National Academics Press, Washington
Parker, R.L. (1926) The collection and utilization of pollen by the honeybee. University Agricultural Experiment Station, Memoir Cornell
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
Peat, J., Tucker, J., Goulson, D. (2005) Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers? Ecol. Entomol. 30, 176–181
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353
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
Roulston, T.H., Cane, J.H. (2000) Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222, 187–209
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
Rundlöf, M., Nilsson, H., Smith, H.G. (2008) Interacting effects of farming practice and landscape context on bumblebees. Biol. Conserv. 141, 417–426
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
Steffan-Dewenter, I., Tscharntke, T. (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121, 432–440
Steffan-Dewenter, I., Klein, A.M., Gaebele, V., Alfert, T., Tscharntke, T. (2006) Bee diversity and plant–pollinator interactions in fragmented landscapes. In: Waser, N.M., Ollerton, J. (eds.) Plant–Pollinator Interactions: From Specialization to Generalization, pp. 387–407. University of Chicago Press, Chicago
Teräs, I. (1985) Food plants and flower visits of bumblebees (Bombus: Hymenoptera, Apidae) in southern Finland. Acta Zool. Fenn. 179, 1–120
Walther-Hellwig, K., Frankl, R. (2000) Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., apidae), in an agricultural landscape. J. Appl. Entomol.-Z. Angew. Entomol. 124, 299–306
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
Westphal, C., Steffan-Dewenter, I., Tscharntke, T. (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149, 289–300
Wille, H., Wille, M. (1984) Die Pollenversorgung des Bienenvolkes: Die wichtigsten Pollenarten bewertet nach ihrem Eiweissgehalt und ihrer Häufigkeit im Pollensammelgut. Schweiz. Bienen-Ztg 2, 64–80
Williams, P.H. (1982) The distribution and decline of British bumble bees (Bombus Latr). J. Apic. Res. 21, 236–245
Williams, P.H. (1986) Environmental change and the distributions of British bumble bees (Bombus Latr). Bee World 67, 50–61
Williams, P.H. (1989) Why are there so many species of bumble bees at Dungeness? Bot. J. Linn. Soc. 101, 31–44
Williams, P.H. (2005) Does specialization explain rarity and decline among British bumblebees? A response to Goulson et al. Biol. Conserv. 122, 33–43
Williams, P.H., Araujo, M.B., Rasmont, P. (2007) Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth? Biol. Conserv. 138, 493–505
Williams, P., Colla, S., Xie, Z.H. (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conserv. Biol. 23, 931–940
Williams, G.R., Tarpy, D.R., vanEngelsdorp, D., Chauzat, M.-P., Cox-Foster, D.L., Delaplane, K.S., Neumann, P., Pettis, J.S., Rogers, R.E.L., Shutler, D. (2010) Colony collapse disorder in context. Bioessays 32, 845–846
Winfree, R. (2010) The conservation and restoration of wild bees. Ann. N. Y. Acad. Sci. 1195, 169–197
Winfree, R., Aguilar, R., Vazquez, D.P., LeBuhn, G., Aizen, M.A. (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076
Xie, Z., Williams, P.H., Tang, Y. (2008) The effect of grazing on bumblebees in the high rangelands of the eastern Tibetan Plateau of Sichuan. J. Insect Conserv. 12, 695–703
Acknowledgements
Marcus Ulbrich as well as Susan Oppermann assisted with the data collection. Linda-Maria Jung and Andrea Hilpert greatly helped with the processing of samples and chemical analyses. Dirk Ahrens-Lagast and Jürgen Tautz kindly provided the honeybee colonies and pollen traps for this study. The comments of two anonymous reviewers greatly improved a previous version of our manuscript. Sara Leonhardt is funded by the Deutsche Forschungs-Gemeinschaft (DFG project: LE 2750/1-1).
Author information
Authors and Affiliations
Corresponding author
Additional information
Manuscript editor: James Nieh
Semblable mais cependant différente: la récolte du pollen chez les colonies d’abeilles et celles de bourdons.
Pollinisateurs généralistes / acides aminés / ressources florales / qualité du pollen
Gleich, und doch verschieden. Wie Honigbienenvölker und Hummelvölker Pollen sammeln.
generalistische Bestäuber / Aminosäuren / florale Ressourcen
Rights and permissions
About this article
Cite this article
Leonhardt, S.D., Blüthgen, N. The same, but different: pollen foraging in honeybee and bumblebee colonies. Apidologie 43, 449–464 (2012). https://doi.org/10.1007/s13592-011-0112-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13592-011-0112-y