Biodiversity and Conservation

, Volume 24, Issue 14, pp 3469–3489 | Cite as

Bumble bees show trait-dependent vulnerability to landscape simplification

  • Anna S. Persson
  • Maj Rundlöf
  • Yann Clough
  • Henrik G. Smith
Original Paper


Agricultural intensification has resulted in large-scale loss of bee pollinators, but while some species have been negatively affected others seem to endure changed conditions. It has been suggested that certain morphological, ecological and life-history traits make some species more vulnerable to landscape changes. Information on which traits make species vulnerable and why may aid conservation of declining species. We performed a comprehensive analysis of how multiple traits related to diet breadth, movement and nesting habits moderate vulnerability of bumble bees to landscape simplification. We surveyed bumble bees in flower-rich non-crop habitats in either complex landscapes (with small crop fields bordered by non-crop habitats), or simple landscapes (with larger fields and therefore less non-crop habitats). We analysed if landscape type interacted with colony size, queen emergence date, colony life-cycle length, nesting habitat, thorax width, proboscis length or variability in thorax and proboscis, to explain bumble bee abundances. Workers and males of species with above-ground nests, small sized colonies and long colony cycle were relatively less abundant in simple compared to in complex landscapes. Simple landscapes hosted fewer males of late emerging species and species with highly variable proboscis length. This suggests that both nesting habitat and spatio-temporal availability of food resources act as ecological filters for bumble bees. Colony size correlated with nesting habitat and queen emergence when correcting for phylogenetic correlations, suggesting that landscape simplification acts through effects on combinations of traits. Our results have consequences for conservation by suggesting that declining bumble bee species can be supported by providing adequate nesting habitats and preferred plant species throughout the season and within short distance from nesting habitats, to allow utilisation also by species having colonies with few workers.


Bombus Intra-specific variation Life-history traits Nesting habitat Phenology Phylogeny 



Y. Hanell and A. Jönsson assisted in the field, Y.H. and M. Johansson performed lab-work. S. Cameron kindly provided bumble bee phylogenetic distance data. The project was financed by a Grant from FORMAS to H.G.S. The studies performed comply with Swedish law.

Supplementary material

10531_2015_1008_MOESM1_ESM.pdf (92 kb)
ESM is available for this article online and consists of methods and results, including table of results, from phylogenetic analyses of bumble bee traits, ESM, Table A (PDF 91 kb)


  1. Banaszak J (1992) Strategy for conservation of wild bees in an agricultural landscape. AGEE 40:179–192. doi: 10.1016/0167-8809(92)90091-O Google Scholar
  2. Benton T (2006) Bumblebees: the natural history & identification of the species found in Britain. Collins, LondonGoogle Scholar
  3. Bommarco R, Lundin O, Smith HG, Rundlöf M (2012) Drastic historic shifts in bumble-bee community composition in Sweden. Proc R Soc Lond Ser B 279:309–315. doi: 10.1098/rspb.2011.0647 CrossRefGoogle Scholar
  4. Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Lin Soc 91:161–188. doi: 10.1111/j.1095-8312.2007.00784.x CrossRefGoogle Scholar
  5. Cariveau DP, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci 10:104–109. doi: 10.1016/j.cois.2015.05.004 CrossRefGoogle Scholar
  6. 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. doi: 10.1016/j.biocon.2006.05.008 CrossRefGoogle Scholar
  7. Carvell C, Jordan WC, Bourke AFG, Pickles R, Redhead JW, Heard MS (2012) Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumble bee species. Oikos 121:734–742. doi: 10.1111/j.1600-0706.2011.19832.x CrossRefGoogle Scholar
  8. 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. doi: 10.1016/j.biocon.2010.07.021 CrossRefGoogle Scholar
  9. Dormann C, Elith J, Buchmann S, Carsten C, Carre G et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. doi: 10.1111/j.1600-0587.2012.07348.x CrossRefGoogle Scholar
  10. Duchateau MJ, Velthuis HHW, Boomsma JJ (2003) Sex ratio variation in the bumblebee Bombus terrestris. Behav Ecol 15:71–82. doi: 10.1093/beheco/arg087 CrossRefGoogle Scholar
  11. Dupont YL, Damgaard C, Simonsen V (2011) Quantitative historical change in Bumblebee (Bombus spp.) Assemblages of red clover fields. Plos One. doi: 10.1371/journal.pone.0025172 Google Scholar
  12. Fitzpatrick U, Murray TE, Paxton RJ, Breen J, Cotton D, Santorum V, Brown MJF (2007) Rarity and decline in bumblebees—a test of causes and correlates in the Irish fauna. Biol Cons 136:185–194. doi: 10.1016/j.biocon.2006.11.012 CrossRefGoogle Scholar
  13. Fussell M, Corbet SA (1992) The nesting places of some British bumble bees. J Apic Res 31:32–41Google Scholar
  14. Goulson D, Peat J, Stout J, 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. doi: 10.1006/anbe.2002.3041 CrossRefGoogle Scholar
  15. Goulson D, Hanley ME, Darvill B, Ellis J, Knight M (2005) Causes of rarity in bumblebees. Biol Conserv 122:1–8. doi: 10.1016/j.biocon.2004.06.017 CrossRefGoogle Scholar
  16. Goulson D, Lye GC, Darvill B (2008a) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208. doi: 10.1146/annurev.ento.53.103106.093454 CrossRefPubMedGoogle Scholar
  17. Goulson D, Lye GC, Darvill B (2008b) Diet breadth, coexistence and rarity in bumblebees. Biodivers Conserv 17:3269–3288. doi: 10.1007/s10531-008-9428-y CrossRefGoogle Scholar
  18. Goulson D et al (2010) Effects of land use at a landscape scale on bumblebee nest density and survival. J Appl Ecol 47:1207–1215. doi: 10.1111/j.1365-2664.2010.01872.x CrossRefGoogle Scholar
  19. Greenleaf S, Williams N, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. doi: 10.1007/s00442-007-0752-9 CrossRefPubMedGoogle Scholar
  20. Heard MS, Carvell C, Carreck NL, Rothery P, Osborne JL, Bourke AFG (2007) Landscape context not patch size determines bumble-bee density on flower mixtures sown for agri-environment schemes. Biol Lett 3:638–641. doi: 10.1098/rsbl.2007.0425 PubMedCentralCrossRefPubMedGoogle Scholar
  21. Heinrich B (1979) Bumblebee economics. Harvard University Press, CambridgeGoogle Scholar
  22. Holmström G (2007) Humlor—Alla Sveriges arter, så känner du igen dem i naturen och i trädgården. Symposion, Stockholm, SwedenGoogle Scholar
  23. Inoue MN, Yokoyama J (2006) Morphological variation in relation to flower use in bumblebees. Entomol Sci 9:147–159. doi: 10.1111/j.1479-8298.2006.00162.x CrossRefGoogle Scholar
  24. Jha S, Kremen C (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. PNAS 110:555–558. doi: 10.1073/pnas.1208682110 PubMedCentralCrossRefPubMedGoogle Scholar
  25. Kleijn D, Raemakers I (2008) A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89:1811–1823. doi: 10.1890/07-1275.1 CrossRefPubMedGoogle Scholar
  26. Kleijn D, Winfree R, Bartomeus I et al (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat Commun. doi: 10.1038/ncomms8414 PubMedCentralPubMedGoogle Scholar
  27. Lagerlöf J, Stark J, Svensson B (1992) Margins of agricultural fields as habitats for pollinating insects. AGEE 40:117–124. doi: 10.1016/0167-8809(92)90087-R Google Scholar
  28. Löken A (1973) Studies on scandinavian bumble bees (Hymenoptera, Apidae). Nor J Entomol 20:1–218Google Scholar
  29. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717. doi: 10.1111/j.1461-0248.2007.01061.x CrossRefPubMedGoogle Scholar
  30. Mossberg B, Cederberg B (2012) Humlor i Sverige. 40 arter att älska och förundras över. Bonnier fakta, SwedenGoogle Scholar
  31. Osborne JL et al (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77:406–415. doi: 10.1111/j.1365-2656.2007.01333.x CrossRefPubMedGoogle Scholar
  32. 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. doi: 10.1111/j.0307-6946.2005.00676.x CrossRefGoogle Scholar
  33. Pelletier L, McNeil JN (2003) The effect of food supplementation on reproductive success in bumblebee field colonies. Oikos 103:688–694. doi: 10.1034/j.1600-0706.2003.12592.x CrossRefGoogle Scholar
  34. Persson AS, Smith HG (2013) Seasonal persistence of bumblebee populations is affected by landscape context. AGEE 165:201–209. doi: 10.1016/j.agee.2012.12.008 Google Scholar
  35. Persson AS, Olsson O, Rundlöf M, Smith HG (2010) Land use intensity and landscape complexity-analysis of landscape characteristics in an agricultural region in Southern Sweden. AGEE 136:169–176. doi: 10.1016/j.agee.2009.12.018 Google Scholar
  36. Prŷs-Jones OE, Corbet SA (1987) Naturalist’s handbooks 6. Bumble bees. Naturalists’ handbooks. Cambridge University Press, CambridgeGoogle Scholar
  37. Ricotta C, Moretti M (2011) CWM and Rao’s quadratic diversity: a unified framework for functional ecology. Oecologia 167:181–188. doi: 10.1007/s00442-011-1965-5 CrossRefPubMedGoogle Scholar
  38. Roulston TAH, Goodell K (2010) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56:293–312. doi: 10.1146/annurev-ento-120709-144802 CrossRefGoogle Scholar
  39. Rundlöf M, Nilsson H, Smith HG (2008) Interacting effects of farming practice and landscape context on bumblebees. Biol Conserv 141:417–426. doi: 10.1016/j.biocon.2007.10.011 CrossRefGoogle Scholar
  40. Rundlöf M, Persson AS, Smith HG, Bommarco R (2014) Late-season mass-flowering red clover increases bumble bee queen and male densities. Biol Conserv 172:138–145. doi: 10.1016/j.biocon.2014.02.027 CrossRefGoogle Scholar
  41. Sladen FWL (1912) The humle-bee. MacMillan & CO., LondonGoogle Scholar
  42. Stoate C, Boatman ND, Borralho RJ, Carvalho CR, Snoo GR, Eden P (2001) Ecological impacts of arable intensification in Europe. J Environ Manag 63:337–365. doi: 10.1006/jema.2001.0473 CrossRefGoogle Scholar
  43. Westphal C, Steffan-Dewenter I, Tscharntke T (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol Lett 6:961–965. doi: 10.1046/j.1461-0248.2003.00523.x CrossRefGoogle Scholar
  44. Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149:289–300. doi: 10.1007/s00442-006-0448-6 CrossRefPubMedGoogle Scholar
  45. Williams NM, Kremen C (2007) Resource distribution among habitats determine solitary bee offspring production in a mosaic landscape. Ecol Appl 17:910–921. doi: 10.1890/06-0269 CrossRefPubMedGoogle Scholar
  46. Williams PH, Osborne J (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–387. doi: 10.1051/apido/2009025 CrossRefGoogle Scholar
  47. Williams PH, Colla S, Xie Z (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conserv Biol 23:931–940. doi: 10.1111/j.1523-1739.2009.01176.x CrossRefPubMedGoogle Scholar
  48. Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291. doi: 10.1016/j.biocon.2010.03.024 CrossRefGoogle Scholar
  49. Williams NM, Regetz J, Kremen C (2012a) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058. doi: 10.1890/11-1006.1 CrossRefPubMedGoogle Scholar
  50. Williams PH et al (2012b) Unveiling cryptic species of the bumble bee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae). System Biodiv 10:21–56. doi: 10.1080/14772000.2012.664574 CrossRefGoogle Scholar
  51. Winfree R (2010) The conservation and restoration of wild bees. Ann NY Acad Sci 1195:169–197. doi: 10.1111/j.1749-6632.2010.05449.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Anna S. Persson
    • 1
  • Maj Rundlöf
    • 1
  • Yann Clough
    • 2
  • Henrik G. Smith
    • 1
    • 2
  1. 1.Department of BiologyLund UniversityLundSweden
  2. 2.Centre of Environmental and Climate ResearchLund UniversityLundSweden

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