Biodiversity and Conservation

, Volume 24, Issue 5, pp 1195–1214 | Cite as

Habitat, spatial and temporal drivers of diversity patterns in a wild bee assemblage

  • Orianne Rollin
  • Vincent Bretagnolle
  • Laura Fortel
  • Laurent Guilbaud
  • Mickaël Henry
Original Paper


Across Europe conservation actions have been implemented to mitigate the decline of pollinators in agricultural landscapes. However, recent concerns have appeared about their efficiency to promote pollinator diversity. To increase the efficiency of these interventions, one must acquire a better knowledge of the target species diversity patterns and its sources of variations at different spatial and temporal scales. This study sets out to identify the main sources of variation in wild bee assemblages at a regional scale (450 km2) in mass-flowering crops and semi-natural habitats. During three consecutive sampling years, we monitored bee diversity and its temporal and spatial turnovers. We show that an intensive agricultural landscape in western France can hold nearly 200 wild bee species at a regional scale, i.e. 20 % of the whole bee fauna known in mainland France. Wild bee diversity was 3–4 times lower in oleaginous crops than in semi-natural habitats, with a substantial number of these being social and gregarious species. Spatial and seasonal species turnover in semi-natural habitats explained 28.6 and 34.3 %, respectively, of regional species richness. Given the importance of the spatial component of the bee diversity turnover, we suggest wild bee conservation efforts should be carried out at relevant spatial scales. The spatial turnover was estimated to be steeper within 50 km2 scales. This provides an order of magnitude for the spatial extent of relevant conservation units within which one may concentrate conservation efforts in order to optimise the number of species promoted per surface area.


Apoidea Additive partitioning Flowering habitats Species richness Species accumulation curve Functional trait 



Special thanks go to J. Knapp and J. Osborne for thorough text correction and improvement. B. Vaissière provided expert support at all stages of the study, including the design and conception of the survey and the management of specimen collection and identification. We are also grateful to J. Aptel, M. Chabirand, A. Haefflinger, C. Maffre and C. Toulet for field assistance; H. Dathe, E. Dufrêne, R. Fonfria, D. Genoud, M. Kuhlmann, G. Le Goff, D. Michez, A. Pauly, S. Risch for bee identification to specie level; F. Herzog, D. Michez and I. Dajoz for helpful comments on earlier versions of the manuscript. We also thank the farmers of the study area for allowing us to carry out surveys in their fields. This work was funded by the French Ministry of Agriculture (POLINOV, CASDAR Program no 9035) and an ANRT CIFRE Ph.D. grant allocated to OR. This paper is dedicated in memoriam of Robert Fonfria.

Supplementary material

10531_2014_852_MOESM1_ESM.doc (270 kb)
Supplementary material 1 (DOC 269 kb)


  1. Amiet F, Müller A, Neumeyer R (1999) Apidae 2: Colletes, Dufourea, Hylaeus, Nomia, Nomioides, Rhophitoides, Rophites, Sphecodes, Systropha. Centre Suisse de Cartographie de la Faune, NeuchâtelGoogle Scholar
  2. Amiet F, Herrmann M, Müller A, Neumeyer R (2001) Apidae 3: Halictus, Lasioglossum. Centre Suisse de Cartographie de la Faune, NeuchâtelGoogle Scholar
  3. Amiet F, Herrmann M, Müller A, Neumeyer R (2004) Apidae 4. Anthidium, Chelostoma, Coelioxys, Dioxys, Heriades, Lithurgus, Megachile, Osmia, Stelis. Centre Suisse de Cartographie de la Faune, NeuchâtelGoogle Scholar
  4. Amiet F, Herrmann M, Müller A, Neumeyer R (2007) Apidae 5. Ammobates, Ammobatoides, Anthophora, Biastes, Ceratina, Dasypoda, Epeoloides, Epeolus, Eucera, Macropis, Melecta, Melitta, Nomada, Pasites, Tetralonia, Thyreus, Xylocopa. Centre Suisse de Cartographie de la Faune, NeuchâtelGoogle Scholar
  5. Amiet F, Herrmann M, Müller A, Neumeyer R (2010) Apidae 6: Andrena, Melitturga, Panurginus, Panurgus. Centre Suisse de Cartographie de la Faune, NeuchâtelGoogle Scholar
  6. Biesmeijer JC, Roberts SPM, Reemer M et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354. doi: 10.1126/science.1127863 CrossRefPubMedGoogle Scholar
  7. 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. doi: 10.1073/pnas.1014743108 CrossRefPubMedCentralPubMedGoogle Scholar
  8. Carvalheiro LG, Seymour CL, Veldtman R, Nicolson SW (2010) Pollination services decline with distance from natural habitat even in biodiversity-rich areas. J Appl Ecol 47:810–820. doi: 10.1111/j.1365-2664.2010.01829.x CrossRefGoogle Scholar
  9. Chase JM (2011) Ecological niche theory. the theory of ecology. University of Chicago Press, Chicago, p 416Google Scholar
  10. Chave J (2004) Neutral theory and community ecology. Ecol Lett 7:241–253. doi: 10.1111/j.1461-0248.2003.00566.x CrossRefGoogle Scholar
  11. Colwell RK (2013) Estimates: statistical estimation of species richness and shared species from samples. Divers Distrib 14:1–10Google Scholar
  12. Crist TO, Veech JA (2006) Additive partitioning of rarefaction curves and species–area relationships: unifying α-, β- and γ-diversity with sample size and habitat area. Ecol Lett 9:923–932. doi: 10.1111/j.1461-0248.2006.00941.x CrossRefPubMedGoogle Scholar
  13. Crist TO, Veech JA, Gering JC, Summerville KS (2003) Partitioning species diversity across landscapes and regions: A hierarchical analysis of α, β, and γ diversity. Am Nat 162:734–743CrossRefPubMedGoogle Scholar
  14. Dengler J (2009) Which function describes the species–area relationship best? A review and empirical evaluation. J Biogeogr 36:728–744. doi: 10.1111/j.1365-2699.2008.02038.x CrossRefGoogle Scholar
  15. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  16. Dicks LV, Showler DA, Sutherland WJ (2010) Bee conservation: Evidence for the effects of interventions, exeter. Pegasus Publishing, CambridgeGoogle Scholar
  17. Duelli P, Obrist MK (2003) Regional biodiversity in an agricultural landscape: the contribution of seminatural habitat islands. Basic Appl Ecol 4:129–138. doi: 10.1078/1439-1791-00140 CrossRefGoogle Scholar
  18. Gering JC, Crist TO, Veech JA (2003) Additive partitioning of species diversity across multiple spatial scales: implications for regional conservation of biodiversity. Conserv Biol 17:488–499. doi: 10.1046/j.1523-1739.2003.01465.x CrossRefGoogle Scholar
  19. 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. doi: 10.1111/j.1365-2664.2010.01872.x CrossRefGoogle Scholar
  20. Greenleaf SS, Williams NM, 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
  21. Hoehn P, Steffan-Dewenter I, Tscharntke T (2010) Relative contribution of agroforestry, rainforest and openland to local and regional bee diversity. Biodivers Conserv 19:2189–2200. doi: 10.1007/s10531-010-9831-z CrossRefGoogle Scholar
  22. Holzschuh A, Dormann CF, Tscharntke T, Steffan-Dewenter I (2013) Mass-flowering crops enhance wild bee abundance. Oecologia 172:477–484. doi: 10.1007/s00442-012-2515-5 CrossRefPubMedCentralPubMedGoogle Scholar
  23. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  24. Jauker F, Peter F, Wolters V, Diekötter T (2012) Early reproductive benefits of mass-flowering crops to the solitary bee Osmia rufa outbalance post-flowering disadvantages. Basic Appl Ecol 13:268–276. doi: 10.1016/j.baae.2012.03.010 CrossRefGoogle Scholar
  25. Jauker B, Krauss J, Jauker F, Steffan-Dewenter I (2013) Linking life history traits to pollinator loss in fragmented calcareous grasslands. Landscape Ecol 28:107–120. doi: 10.1007/s10980-012-9820-6 CrossRefGoogle Scholar
  26. Kirk WDJ, Howes FN (2012) Plants for bees: a guide to the plants that benefit the bees of the british isles. IBRA, p 280Google Scholar
  27. Kleijn D, Sutherland WJ (2003) How effective are European agri-environment schemes in conserving and promoting biodiversity? J Appl Ecol 40:947–969. doi: 10.1111/j.1365-2664.2003.00868.x CrossRefGoogle Scholar
  28. Kleijn D, Berendse F, Smit R, Gilissen N (2001) Agri-environment schemes do not effectively protect biodiversity in Dutch agricultural landscapes. Nature 413:723–725. doi: 10.1038/35099540 CrossRefPubMedGoogle Scholar
  29. Knop E, Kleijn D, Herzog F, Schmid B (2006) Effectiveness of the Swiss agri-environment scheme in promoting biodiversity. J Appl Ecol 43:120–127. doi: 10.1111/j.1365-2664.2005.01113.x CrossRefGoogle Scholar
  30. Lande R (1996) Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos 76:5–13. doi: 10.2307/3545743 CrossRefGoogle Scholar
  31. Le Féon V, Schermann-Legionnet A, Delettre Y et al (2010) Intensification of agriculture, landscape composition and wild bee communities: a large scale study in four European countries. Agric Ecosyst Environ 137:143–150. doi: 10.1016/j.agee.2010.01.015 CrossRefGoogle Scholar
  32. Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410CrossRefPubMedGoogle Scholar
  33. Kuhlmann et al M (2013) Checklist of the western palaearctic bees (Hymenoptera: Apoidea: Anthophila). Accessed 10 Sep 2013
  34. Magurran AE (2004) Measuring biological diversity. Blackwell Pub, MaldenGoogle Scholar
  35. Michener CD (2007) The Bees of the World, 2nd Revised Edition. Johns Hopkins University Press, HopkinsGoogle Scholar
  36. Müller J, Goßner MM (2010) Three-dimensional partitioning of diversity informs state-wide strategies for the conservation of saproxylic beetles. Biol Conserv 143:625–633. doi: 10.1016/j.biocon.2009.11.027 CrossRefGoogle Scholar
  37. Munyuli MBT, Nyeko P, Potts S et al (2013) Patterns of bee diversity in mosaic agricultural landscapes of central Uganda: implication of pollination services conservation for food security. J Insect Conserv 17:79–93. doi: 10.1007/s10841-012-9488-x CrossRefGoogle Scholar
  38. New TR (1999) Limits to species focusing in insect conservation. Ann Entomol Soc Am 92:853–860CrossRefGoogle Scholar
  39. Öckinger E, Smith HG (2007) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59. doi: 10.1111/j.1365-2664.2006.01250.x CrossRefGoogle Scholar
  40. Oertli S, Mueller A, Dorn S (2005) Ecological and seasonal patterns in the diversity of a species-rich bee assemblage (Hymenoptera: Apoidea: Apiformes). Euro J Entomol 102:53–63CrossRefGoogle Scholar
  41. Oksanen J, Blanchet FG, Kindt R et al (2011) Vegan: community ecology package. Blackwell Publishing, OxfordGoogle Scholar
  42. Palmer MW (1995) How should one count species? Natural Areas Journal 15:124–135Google Scholar
  43. Potts SG, Vulliamy B, Dafni A et al (2003) Linking bees and flowers: How do floral communities structure pollinator communities? Ecology 84:2628–2642CrossRefGoogle Scholar
  44. Potts SG, Vulliamy B, Roberts S et al (2005) Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecological Entomol 30:78–85. doi: 10.1111/j.0307-6946.2005.00662.x CrossRefGoogle Scholar
  45. Potts S, Roberts S, Dean R et al (2010a) Declines of managed honey bees and beekeepers in Europe. J Apic Res 49:15. doi: 10.3896/IBRA. CrossRefGoogle Scholar
  46. Potts SG, Biesmeijer JC, Kremen C et al (2010b) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. doi: 10.1016/j.tree.2010.01.007 CrossRefPubMedGoogle Scholar
  47. Pouvreau A (2004) Les insectes pollinisateurs. Delachaux et Niestlé, ParisGoogle Scholar
  48. Ranta E, Lundberg H (1980) Resource partitioning in bumblebees: the significance of differences in proboscis length. Oikos 35:298–302. doi: 10.2307/3544643 CrossRefGoogle Scholar
  49. Rollin O, Bretagnolle V, Decourtye A et al (2013) Differences of floral resource use between honey bees and wild bees in an intensive farming system. Agric Ecosyst Environ 179:78–86. doi: 10.1016/j.agee.2013.07.007 CrossRefGoogle Scholar
  50. Roubik DW (2001) Ups and downs in pollinator populations: When is there a decline? Conserv Ecol 5. URL:
  51. Scheiner SM (2003) Six types of species-area curves. Glob Ecol Biogeogr 12:441–447. doi: 10.1046/j.1466-822X.2003.00061.x CrossRefGoogle Scholar
  52. Steffan-Dewenter I, Tscharntke T (2001) Succession of bee communities on fallows. Ecography 24:83–93. doi: 10.1034/j.1600-0587.2001.240110.x CrossRefGoogle Scholar
  53. Summerville KS, Crist TO (2005) Temporal patterns of species accumulation in a survey of Lepidoptera in a beech-maple forest. Biodivers Conserv 14:3393–3406. doi: 10.1007/s10531-004-0546-x CrossRefGoogle Scholar
  54. Tylianakis JM, Klein A-M, Tscharntke T (2005) Spatiotemporal variation in the diversity of Hymenoptera across a tropical habitat gradient. Ecology 86:3296–3302. doi: 10.1890/05-0371 CrossRefGoogle Scholar
  55. VanEngelsdorp D, Hayes J, Underwood RM, Pettis J (2008) A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS ONE 3:e4071. doi: 10.1371/journal.pone.0004071 CrossRefPubMedCentralGoogle Scholar
  56. Walther BA, Morand S (1998) Comparative performance of species richness estimation methods. Parasitology 116:395–405CrossRefPubMedGoogle Scholar
  57. 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
  58. Westphal C, Bommarco R, Carré G et al (2008) Measuring bee diversity in different european habitats and biogeographical regions. Ecol Monogr 78:653–671. doi: 10.1890/07-1292.1 CrossRefGoogle Scholar
  59. Westrich P (1989) Die Wildbienen Baden-Württemburgs: Spezieller Teil—Die Gattungen und Arten. Eugen Ulmer, StuttgartGoogle Scholar
  60. Williams NM, Minckley RL, Silveira FA (2001) Variation in native bee faunas and its implications for detecting community changes. Conserv Ecol 5. URL:
  61. Zurbuchen A, Cheesman S, Klaiber J et al (2010a) Long foraging distances impose high costs on offspring production in solitary bees. J Anim Ecol 79:674–681. doi: 10.1111/j.1365-2656.2010.01675.x CrossRefPubMedGoogle Scholar
  62. Zurbuchen A, Landert L, Klaiber J et al (2010b) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143:669–676. doi: 10.1016/j.biocon.2009.12.003 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Orianne Rollin
    • 1
    • 2
  • Vincent Bretagnolle
    • 4
    • 5
  • Laura Fortel
    • 3
  • Laurent Guilbaud
    • 2
    • 3
  • Mickaël Henry
    • 2
    • 3
  1. 1.ITSAP-Institut de l’abeille - UMT PrADEAvignon Cedex 9France
  2. 2.UMT Protection des Abeilles dans l’EnvironnementAvignon Cedex 9France
  3. 3.INRA, UR 406 Abeilles et EnvironnementAvignonFrance
  4. 4.Centre d’Etudes Biologiques de ChizéCNRS & Université de la Rochelle, UMR 7372Beauvoir-Sur-NiortFrance
  5. 5.LTER « Zone Atelier Plaine & Val de Sèvre »Centre d’Etudes Biologiques de Chizé, CNRSVilliers-En-BoisFrance

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