Drastic shifts in the Belgian bumblebee community over the last century

Abstract

Bumblebees are undergoing strong declines in Europe caused by habitat loss and fragmentation, agricultural intensification, and climate change. Long-term records are necessary to estimate population trends precisely and to propose appropriate mitigation strategies. Based on an original database of 173,788 specimens from museum collections, scientific monitoring, and opportunistic citizen data from 1810 to 2016, we compared changes in species richness and area of occupancy of Belgian bumblebee species through three time-periods (1910–1930, 1970–1989, and 1990–2016). We also assessed if the observed trends are related to species-specific ecological traits and spatial scales (local, regional and national). Overall, species richness decreased over the last century in Belgium, but some regions retained relatively species-rich communities. A strong shift in community composition occurred. Three species remained among the “top five” in terms of species occurrence (area of occupancy) between the three time-periods (B. pascuorum, B. lapidarius, and B. pratorum), but several species that were once widespread declined drastically (B. muscorum, B. humilis, B. ruderatus, and B. veteranus), while a few species increased their distribution (e.g. B. hypnorum and B. terrestris). Habitat preferences significantly explained the observed trends, with declining species preferring open habitats and increasing species preferring wooded habitats.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Aguirre-Gutiérrez J, Biesmeijer JC, van Loon EE et al (2015) Susceptibility of pollinators to ongoing landscape changes depends on landscape history. Divers Distrib 21:1129–1140. https://doi.org/10.1111/ddi.12350

    Article  Google Scholar 

  2. Aguirre-Gutiérrez J, Kissling WD, Carvalheiro LG et al (2016) Functional traits help to explain half-century long shifts in pollinator distributions. Sci Rep. https://doi.org/10.1038/srep24451

    Article  PubMed  PubMed Central  Google Scholar 

  3. Baessler C, Klotz S (2006) Effects of changes in agricultural land-use on landscape structure and arable weed vegetation over the last 50 years. Agric Ecosyst Environ 115:43–50. https://doi.org/10.1016/j.agee.2005.12.007

    Article  Google Scholar 

  4. Ball JF (1914) Les bourdons de la Belgique. Ann de la Soc Entomol de Belg 58:77–108

    Google Scholar 

  5. Ball JF (1920) Notes supplémentaires sur les bourdons de la Belgique. Bull Ann de la Soc Entomol de Belg 60:31–43

    Google Scholar 

  6. Batáry P, Dicks LV, Kleijn D, Sutherland WJ (2015) The role of agri-environment schemes in conservation and environmental management. Conserv Biol 4:1006–1016. https://doi.org/10.1111/cobi.12536

    Article  Google Scholar 

  7. Bees Wasps and Ants Recording Society (2019) Bombus hypnorum. In: Bees, wasps & ants recording society. https://www.bwars.com/index.php?q=bee/apidae/bombus-hypnorum. Accessed 10 Nov 2019

  8. Belgian Federal government (2017) Statistics Belgium—statistiques & chiffres. https://economie.fgov.be/fr/statistiques/chiffres/. Accessed 15 Feb 2017

  9. Benton T (2006) Chapter 9: the British species. In: Bumblebees. Harper Collins Publishers, London

  10. Bommarco R, Biesmeijer JC, Meyer B et al (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc R Soc B 277:2075–2082. https://doi.org/10.1098/rspb.2009.2221

    Article  PubMed  Google Scholar 

  11. Bommarco R, Lundin O, Smith HG, Rundlof M (2012) Drastic historic shifts in bumble-bee community composition in Sweden. Proc R Soc B 279:309–315. https://doi.org/10.1098/rspb.2011.0647

    Article  PubMed  Google Scholar 

  12. Bommarco R, Lindborg R, Marini L, Öckinger E (2014) Extinction debt for plants and flower-visiting insects in landscapes with contrasting land use history. Divers Distrib 20:591–599

    Article  Google Scholar 

  13. Brian AD (1957) Differences in the flowers visited by four species of bumble bees and their causes. J Anim Ecol 26:71–98. https://doi.org/10.2307/1782

    Article  Google Scholar 

  14. Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460. https://doi.org/10.1016/j.tree.2008.03.011

    Article  PubMed  Google Scholar 

  15. Cameron SA, Lozier JD, Strange JP et al (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci 108:662–667. https://doi.org/10.1073/pnas.1014743108

    Article  PubMed  Google Scholar 

  16. Carvalheiro LG, Kunin WE, Keil P et al (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett 16:870–878. https://doi.org/10.1111/ele.12121

    Article  PubMed  PubMed Central  Google Scholar 

  17. Carvalheiro LG, Biesmeijer JC, Franzén M et al (2019) Soil eutrophication shaped the composition of pollinator assemblages during the past century. Ecography. https://doi.org/10.1111/ecog.04656

    Article  Google Scholar 

  18. Carvell C, Meek WR, Pywell RF, Nowakowski M (2004) The response of foraging bumblebees to successional change in newly created arable field margins. Biol Conserv 118:327–339. https://doi.org/10.1016/j.biocon.2003.09.012

    Article  Google Scholar 

  19. Carvell C, Roy DB, Smart SM et al (2006) Declines in forage availability for bumblebees at a national scale. Biol Conserv 132:481–489. https://doi.org/10.1016/j.biocon.2006.05.008

    Article  Google Scholar 

  20. Carvell C, Meek WR, Pywell RF et al (2007) Comparing the efficacy of agri-environment schemes to enhance bumble bee abundance and diversity on arable field margins. J Appl Ecol 44:29–40. https://doi.org/10.1111/j.1365-2664.2006.01249.x

    Article  Google Scholar 

  21. Casey LM, Rebelo H, Rotheray E, Goulson D (2015) Evidence for habitat and climatic specializations driving the long-term distribution trends of UK and Irish bumblebees. Divers Distrib 21:864–875. https://doi.org/10.1111/ddi.12344

    Article  Google Scholar 

  22. Christians C (1998) Quarante ans de politique agricole européenne commune et d’agriculture en Belgique. Bull de la Soc Géogr de Liège 35:41–55

  23. 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

    Article  Google Scholar 

  24. Crowther LP, Hein P-L, Bourke AFG (2014) Habitat and forage associations of a naturally colonising insect pollinator, the tree bumblebee Bombus hypnorum. PLoS ONE 9:e107568. https://doi.org/10.1371/journal.pone.0107568

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Croxton PJ, Carvell C, Mountford JO, Sparks TH (2002) A comparison of green lanes and field margins as bumblebee habitat in an arable landscape. Biol Conserv 107:365–374. https://doi.org/10.1016/S0006-3207(02)00074-5

    Article  Google Scholar 

  26. De Palma A, Kuhlmann M, Roberts SPM et al (2015) Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. J Appl Ecol 52:1567–1577. https://doi.org/10.1111/1365-2664.12524

    Article  PubMed  PubMed Central  Google Scholar 

  27. Debaille F, Rasmont P (1997) Redécouverte de Bombus wurfleini Radoskowski, 1859 (Hymenoptera, Apidae) auparavant considéré comme disparu de Belgique. Bull et Ann de la Soc R Belge d’Entomol 117:1–4

    Google Scholar 

  28. Drossart M, Rasmont P, Vanormelingen P et al (2018) Belgian Red List of bees. BRAIN-be—(Belgian research action through interdisciplinary networks). Presse universitaire de l’Université de Mons, Mons, p 140

    Google Scholar 

  29. Dufrene M, Legendre P (1991) Geographic structure and potential ecological factors in Belgium. J Biogeogr 18:257–266. https://doi.org/10.2307/2845396

    Article  Google Scholar 

  30. Dupont YL, Damgaard C, Simonsen V (2011) Quantitative historical change in Bumblebee (Bombus spp.) assemblages of red clover fields. PLoS ONE 6:e25172. https://doi.org/10.1371/journal.pone.0025172

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Edwards M, Williams P (2004) Where have all the bumblebees gone, and could they ever return. Br Wildl 15:305–312

    Google Scholar 

  32. Fitzpatrick Ú, Murray TE, Paxton RJ et al (2007) Rarity and decline in bumblebees—a test of causes and correlates in the Irish fauna. Biol Conserv 136:185–194. https://doi.org/10.1016/j.biocon.2006.11.012

    Article  Google Scholar 

  33. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x

    Article  Google Scholar 

  34. Goulson D (2010) Bumblebees: behaviour, ecology, and conservation. Oxford University Press, Oxford

    Book  Google Scholar 

  35. 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. https://doi.org/10.1051/apido:2003062

    Article  Google Scholar 

  36. Goulson D, Williams P (2001) Bombus hypnorum (Hymenoptera: Apidae), a new British bumblebee? Br J Entomol Nat Hist 14:129–131

    Google Scholar 

  37. Goulson D, Hanley ME, Darvill B et al (2005) Causes of rarity in bumblebees. Biol Conserv 122:1–8

    Article  Google Scholar 

  38. Goulson D, Lepais O, O’Connor S et al (2010) Effects of land use at a landscape scale on bumblebee nest density and survival. J Appl Ecol 47:1207–1215. https://doi.org/10.1111/j.1365-2664.2010.01872.x

    Article  Google Scholar 

  39. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. https://doi.org/10.1126/science.1255957

    CAS  Article  PubMed  Google Scholar 

  40. Graham L, Jones KN (1996) Resource partitioning and per-flower foraging efficiency in two bumble bee species. Am Midl Nat 136:401–406. https://doi.org/10.2307/2426743

    Article  Google Scholar 

  41. Isaac NJB, Pocock MJO (2015) Bias and information in biological records: bias and information in biological records. Biol J Lin Soc 115:522–531. https://doi.org/10.1111/bij.12532

    Article  Google Scholar 

  42. Iserbyt S, Vray S, Dendoncker N et al (2015) High-resolution distribution of bumblebees (Bombus spp.) in a mountain area marked by agricultural decline. Ann de la Soc Entomol de France (NS) 51:375–391. https://doi.org/10.1080/00379271.2016.1141664

    Article  Google Scholar 

  43. Institut Royal Météorologique - Normales mensuelles (IRM) (2017). http://www.meteo.be/meteo/view/fr/360955-Normales+mensuelles.html#ppt_5238244.

  44. IUCN (2019) The IUCN Red List of threatened species. https://www.iucnredlist.org. Accessed 26 Nov 2019

  45. Kells AR, Goulson D (2003) Preferred nesting sites of bumblebee queens (Hymenoptera: Apidae) in agroecosystems in the UK. Biol Conserv 109:165–174. https://doi.org/10.1016/S0006-3207(02)00131-3

    Article  Google Scholar 

  46. Kerr JT, Pindar A, Galpern P et al (2015) Climate change impacts on bumblebees converge across continents. Science 349:177–180. https://doi.org/10.1126/science.aaa7031

    CAS  Article  PubMed  Google Scholar 

  47. Kleijn D, Raemakers I (2008) A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89:1811–1823. https://doi.org/10.1890/07-1275.1

    Article  PubMed  Google Scholar 

  48. Kleijn D, Sutherland WJ (2003) How effective are European agri-environment schemes in conserving and promoting biodiversity? J Appl Ecol 40:947–969. https://doi.org/10.1111/j.1365-2664.2003.00868.x

    Article  Google Scholar 

  49. Kosior A, Celary W, Olejniczak P et al (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41:79–88. https://doi.org/10.1017/S0030605307001597

    Article  Google Scholar 

  50. Kosior A, Celary W, Solarz W et al (1850s) Long-term changes in the species composition and distribution of Bombini (Apidae) in Cracow since the mid 1850s. Ann de la Soc Entomol de France (NS) 44:393–407. https://doi.org/10.1080/00379271.2008.10697576

    Article  Google Scholar 

  51. Kuussaari M, Bommarco R, Heikkinen RK et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571. https://doi.org/10.1016/j.tree.2009.04.011

    Article  PubMed  Google Scholar 

  52. Løken A (1984) Scandinavianspeciesof the genus Psithyrus lepeletier (HymenopteraA: pidae). Entomol Scand 23:1–45

    Google Scholar 

  53. Maebe K, Meeus I, Vray S et al (2016) A century of temporal stability of genetic diversity in wild bumblebees. Sci Rep. https://doi.org/10.1038/srep38289

    Article  PubMed  PubMed Central  Google Scholar 

  54. Maes D, Isaac NJB, Harrower CA et al (2015) The use of opportunistic data for %3eIUCN Red List assessments. Biol J Lin Soc 3:690–706. https://doi.org/10.1111/bij.12530

    Article  Google Scholar 

  55. Mazoyer M, Roudart L (2006) A history of world agriculture: from the neolithic age to the current crisis. NYU Press, New York

    Google Scholar 

  56. Nieto A, Roberts SPM, Kemp J et al (2014) European red list of bees. Publications Office, Luxembourg

    Google Scholar 

  57. Oksanen J, Blanchet FG, Kindt R, et al (2011) Vegan: community ecology package

  58. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x

    Article  Google Scholar 

  59. Peeters TMJ, Raemakers IP, Smith J (1999) European Invertebrate Survey Nederland. Netherlands

  60. Potts SG, Biesmeijer JC, Kremen C et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007

    Article  PubMed  Google Scholar 

  61. Pywell RF, Warman EA, Hulmes L et al (2006) Effectiveness of new agri-environment schemes in providing foraging resources for bumblebees in intensively farmed landscapes. Biol Conserv 129:192–206. https://doi.org/10.1016/j.biocon.2005.10.034

    Article  Google Scholar 

  62. QGIS Development Team (2019) QGIS geographic information system. Open Source Geospatial Foundation

  63. R Development Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  64. Ranta E, Lundberg H (1980) Resource partitioning in bumblebees: the significance of differences in proboscis length. Oikos 35:298–302. https://doi.org/10.2307/3544643

    Article  Google Scholar 

  65. Rasmont P (1982) Pyrobombus cullumanus (KIRBY) espèce de bourdon nouvelle pour la Belgique (Hymenoptera, Apidea). Bull et Ann de la Soc R Belge d’Entomol 118:21–23

    Google Scholar 

  66. Rasmont P (1988) Monographie écologique et zoogéographique des bourdons de France et de Belgique (Hymenoptera, Apidae, Bombinae. Faculté des Sciences agronomiques de l’Eta

  67. Rasmont P, Mersch P (1988) First estimation of faunistic drift by bumblebees of Belgium, (Hymenoptera: Apidae). Ann de la Soc R Zool de Belg 118:141–147

    Google Scholar 

  68. Rasmont P, Leclercq J, Jacob-Remacle A et al (1993) The faunistic drift of Apoidea in Belgium. In: E. Bruneau (ed) Bee for pollination. Brussels, pp 65–87

  69. Rasmont P, Franzén M, Lecocq T et al (2015) Climatic risk and distribution atlas of European Bumblebees. Pensoft Publishers, Sofia

    Book  Google Scholar 

  70. Robinson RA, Sutherland WJ (2002) Post-war changes in arable farming and biodiversity in Great Britain. J Appl Ecol 39:157–176. https://doi.org/10.1046/j.1365-2664.2002.00695.x

    Article  Google Scholar 

  71. Sárospataki M, Novák J, Molnár V (2005) Assessing the threatened status of bumble bee species (Hymenoptera: Apidae) in Hungary, Central Europe. Biodivers Conserv 14:2437–2446. https://doi.org/10.1007/s10531-004-0152-y

    Article  Google Scholar 

  72. Schleuning M, Fründ J, Schweiger O et al (2016) Ecological networks are more sensitive to plant than to animal extinction under climate change. Nat Commun. https://doi.org/10.1038/ncomms13965

    Article  PubMed  PubMed Central  Google Scholar 

  73. Schweiger O, Biesmeijer JC, Bommarco R et al (2010) Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol Rev 85:777–795. https://doi.org/10.1111/j.1469-185X.2010.00125.x

    Article  PubMed  Google Scholar 

  74. Service Public Fédéral Belge (2019) Utilisation du sol: Chiffres. https://statbel.fgov.be/fr/themes/environnement/sol/utilisation-du-sol. Accessed 10 June 2019

  75. Société Royale Forestière de Belgique (2018) Les forêts de Belgique. In: Société Royale Forestière de Belgique. https://www.srfb.be/fr/les_forets_belgique. Accessed 7 Aug 2018

  76. Svensson B, Lagerlöf J, Svensson GB (2000) Habitat preferences of nest-seeking bumble bees (Hymenoptera: Apidae) in an agricultural landscape. Agric Ecosyst Environ 77:247–255. https://doi.org/10.1016/S0167-8809(99)00106-1

    Article  Google Scholar 

  77. Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66

    Article  Google Scholar 

  78. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x

    Article  PubMed  Google Scholar 

  79. van Strien AJ, van Swaay CAM, Termaat T, Computational Geo-Ecology (IBED, FNWI) (2013) Opportunistic citizen science data of animal species produce reliable estimates of distribution trends if analysed with occupancy models. J Appl Ecol 50:1450–1458. https://doi.org/10.1111/1365-2664.12158

    Article  Google Scholar 

  80. von Hagen E, Aichhorn A (2014) Hummeln: bestimmen, ansiedeln, vermehren, schützen, 6th edn. Fauna Verlag, Germany

    Google Scholar 

  81. Vray S, Lecocq T, Roberts SPM, Rasmont P (2017) Endangered by laws: potential consequences of regulations against thistles on bumblebee conservation. Ann de la Soc Entomol de France (NS) 53:33–41. https://doi.org/10.1080/00379271.2017.1304831

    Article  Google Scholar 

  82. Vray S, Rollin O, Rasmont P et al (2019) A century of local changes in bumblebee communities and landscape composition in Belgium. J Insect Conserv. https://doi.org/10.1007/s10841-019-00139-9

    Article  Google Scholar 

  83. Williams P (2005) Does specialization explain rarity and decline among British bumblebees? A response to Goulson et al. Biol Conserv 122:33–43. https://doi.org/10.1016/j.biocon.2004.06.019

    Article  Google Scholar 

  84. Williams PH, Osborne JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–387. https://doi.org/10.1051/apido/2009025

    Article  Google Scholar 

  85. Williams NM, Crone EE, Roulston TH et al (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291. https://doi.org/10.1016/j.biocon.2010.03.024

    Article  Google Scholar 

  86. Wood TJ, Gibbs J, Graham KK, Isaacs R (2019) Narrow pollen diets are associated with declining Midwestern bumble bee species. Ecology 100:e02697. https://doi.org/10.1002/ecy.2697

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

This research was mainly supported by the Belgian Science Policy (project BR/132/A1/BELBEES). This work was also partly supported by the "Fonds de la Recherche Scientifique—FNRS" and the Fonds "Wetenschappelijk Onderzoek—Vlaanderen (FWO)" under EOS Project (n°3094785). OR was supported by Fundação para Ciência e Tecnologia (FCT) via the programa operacional regional de Lisboa 2014/2020 (EUCLIPO-028360). We thank the Royal Belgian Institute of Natural Sciences of Brussels, more precisely J.-L. Boeve, W. Dekoninck, and Y. Gerard, for the access to the F. J. Ball’s collection of bumblebees. We are grateful to the many people who helped to complete our database, particularly R. Barone, S. Brinckman, D. Camerlinck, E. De Tré, W. Deleus, C. Deschepper, J. Devalez, J. D'Haeseleer, D. D'Hert, S. De Rycke, P. Grootaert, J. Lambrechts, K. Maebe, F. Marlière, L. Marshall, A. Pauly, A.S. Popeler, J. Reyniers, M. Rogghe, M. Terzo, W. Vandemaele, P. Vanormelingen, H. Wallays, with a special thanks to the members of the association Natuurpunt, more precisely the group Aculea. We also would like to thank T.J. Wood for his proofreading and the two anonymous reviewers for their input to our manuscript.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Orianne Rollin or Sarah Vray.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Louise Amy Ashton.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 3301 kb)

Supplementary file2 (XLSX 75 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rollin, O., Vray, S., Dendoncker, N. et al. Drastic shifts in the Belgian bumblebee community over the last century. Biodivers Conserv 29, 2553–2573 (2020). https://doi.org/10.1007/s10531-020-01988-6

Download citation

Keywords

  • Bombus
  • Species richness change
  • Area of occupancy
  • Habitat preference
  • Nesting strategy