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Ecological Research

, Volume 26, Issue 5, pp 969–983 | Cite as

Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques

  • Anders Nielsen
  • Ingolf Steffan-Dewenter
  • Catrin Westphal
  • Olivia Messinger
  • Simon G. Potts
  • Stuart P. M. Roberts
  • Josef Settele
  • Hajnalka Szentgyörgyi
  • Bernard E. Vaissière
  • Michalis Vaitis
  • Michal Woyciechowski
  • Ioannis Bazos
  • Jacobus C. Biesmeijer
  • Riccardo Bommarco
  • William E. Kunin
  • Thomas Tscheulin
  • Ellen Lamborn
  • Theodora Petanidou
Original Article

Abstract

The decline of bees has raised concerns regarding their conservation and the maintenance of ecosystem services they provide to bee-pollinated wild flowers and crops. Although the Mediterranean region is a hotspot for bee species richness, their status remains poorly studied. There is an urgent need for cost-effective, reliable, and unbiased sampling methods that give good bee species richness estimates. This study aims: (a) to assess bee species richness in two common Mediterranean habitat types: semi-natural scrub (phrygana) and managed olive groves; (b) to compare species richness in those systems to that of other biogeographic regions, and (c) to assess whether six different sampling methods (pan traps, variable and standardized transect walks, observation plots and trap nests), previously tested in other European biogeographic regions, are suitable in Mediterranean communities. Eight study sites, four per habitat type, were selected on the island of Lesvos, Greece. The species richness observed was high compared to other habitat types worldwide for which comparable data exist. Pan traps collected the highest proportion of the total bee species richness across all methods at the scale of a study site. Variable and standardized transect walks detected the highest total richness over all eight study sites. Trap nests and observation plots detected only a limited fraction of the bee species richness. To assess the total bee species richness in bee diversity hotspots, such as the studied habitats, we suggest a combination of transect walks conducted by trained bee collectors and pan trap sampling.

Keywords

Hymenoptera Apoidea Sampling methods Pan traps Transect walks Abundance-based Coverage Estimator (ACE) Subunit-based rarefaction curves Olive groves Phrygana Mediterranean scrub Biodiversity hotspot 

Notes

Acknowledgments

Our cordial thanks to all taxonomists for their great help with bee identification: Holger Dathe, Andreas Ebmer, George Else, Andrew Grace, Peter Hartmann, Andreas Müller, Andrew Polaszek, Stephan Risch, Erwin Scheuchl, Max Schwarz, and Paul Williams. Many thanks also to Hjalmar Dahm, Michael Greenwell, and Marios Apostolopoulos for fieldwork assistance and all those that sporadically helped during the collection period. We acknowledge Aristeidis Sifnaios and Aliki Mitsou for allowing fieldwork in their properties. Financial support for all authors was received through the EU FP 6 Integrated Project “ALARM” (Assessing LArge scale environmental Risks for biodiversity with tested Methods: GOCE-CT-2003-506675; http://www.alarmproject.net (Settele et al. 2005), the EU FP7 project “SCALES” (Securing the Conservation of biodiversity across Administrative Levels and spatial, temporal and Ecological Scales: 226852), the EU FP7 project “STEP” (Status and Trends of European Pollinators, http://www.step-project.net, 244090–STEP–CP–FP), and by the Swedish Research Council for Environment, Agricultural Sciences and Spatial planning (FORMAS).

Supplementary material

11284_2011_852_MOESM1_ESM.doc (461 kb)
Supplementary material 1 (DOC 461 kb)

References

  1. Allen HD, Randall RE, Amable GS, Devereux BJ (2006) The impact of changing olive cultivation practices on the ground flora of olive groves in the Messara and Psiloritis regions, Crete, Greece. Land Degrad Dev 17:249–273. doi: 10.1002/ldr.716 CrossRefGoogle Scholar
  2. Atmar W, Patterson BD (1993) The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96:373–382CrossRefGoogle Scholar
  3. Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387PubMedCrossRefGoogle Scholar
  4. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354PubMedCrossRefGoogle Scholar
  5. Cane JH, Minckley RL, Kervin LJ (2000) Sampling bees (Hymenoptera: Apiformes) for pollinator community studies: pitfalls of pan-trapping. J Kansas Entomol Soc 73:225–231Google Scholar
  6. Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159CrossRefGoogle Scholar
  7. Chao A, Chazdon RL, Colwell RK, Shen TJ (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371PubMedCrossRefGoogle Scholar
  8. Colwell RK (2005) EstimateS: Statistical estimation of species richness and shared species from samples. Version 7.5. User’s Guide and application published at: http://purl.oclc.org/estimates
  9. Colwell RK, Chang XM, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727CrossRefGoogle Scholar
  10. Committee on the Status of Pollinators in North America (2007) Status of pollinators in North America. The National Academies Press, Washington, DCGoogle Scholar
  11. Dafni A, Kevan PG, Husband BC, editors (2005) Practical pollination ecology. Enviroquest, Cambridge, Ontario, CanadaGoogle Scholar
  12. Detsis V, Diamantopoulos J, Kosmas C (2000) Collembolan assemblages in Lesvos, Greece. Effects of differences in vegetation and precipitation. Acta Oecologica 21(2):149–159CrossRefGoogle Scholar
  13. Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biology 4:129–135CrossRefGoogle Scholar
  14. Gathmann A, Greiler HJ, Tscharntke T (1994) Trap-nesting bees and wasps colonizing set-aside fields: succession and body-size, management by cutting and sowing. Oecologia 98:8–14CrossRefGoogle Scholar
  15. Ghazoul J (2005) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol Evol 20:367–373PubMedCrossRefGoogle Scholar
  16. Guimarães PR, Guimarães P (2006) Improving the analyses of nestedness for large sets of matrices. Environm Modell Softw 21:1512–1513CrossRefGoogle Scholar
  17. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant–pollinator interactions. Annu Rev Ecol Syst 29:83–112CrossRefGoogle Scholar
  18. Kizos T, Dalaka A, Petanidou T (2010) Farmers’ attitudes and landscape change: evidence from the abandonment of terraced cultivations on Lesvos, Greece. Agric Hum Values 27:199–212CrossRefGoogle Scholar
  19. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274:303–313. doi: 10.1098/rspb.2006.3721 CrossRefGoogle Scholar
  20. Krauss J, Steffan-Dewenter I, Tscharntke T (2003) How does landscape context contribute to effects of habitat fragmentation on diversity and population density of butterflies? J Biogeogr 30:889–900CrossRefGoogle Scholar
  21. Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vazquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein AM, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314PubMedCrossRefGoogle Scholar
  22. Leong JM, Thorp RW (1999) Colour-coded sampling: the pan trap colour preferences of oligolectic and nonoligolectic bees associated with a vernal pool plant. Ecol Entomol 24:329–335CrossRefGoogle Scholar
  23. Magurran AE (2004) Measuring biological diversity. Blackwell Publ, MaldenGoogle Scholar
  24. Marathianou M, Kosmas C, Gerontidis S, Detsis V (2000) Land-use evolution and degradation in Lesvos (Greece): a historical approach. Land Degrad Develop 11:63–73CrossRefGoogle Scholar
  25. Mayer C (2005) Does grazing influence biodiversity? Afr Biodivers Mol Org Ecosyst 173–179Google Scholar
  26. Michener CD (2007) The bees of the world. John Hopkins University Press, BaltimoreGoogle Scholar
  27. Nielsen A, Ims RA (2000) Bumble bee pollination of the sticky catchfly in a fragmented agricultural landscape. Ecoscience 7:157–165Google Scholar
  28. O’Toole C, Raw A (2004) Bees of the world. Facts On File, New YorkGoogle Scholar
  29. Packer L (1991) The evolution of social behavior and nest architecture in sweat bees of the subgenus Evylaeus (Hymenoptera : Halictidae): a phylogenetic approach. Behav Ecol Sociobiol 29:153–160CrossRefGoogle Scholar
  30. Petanidou T, Ellis WN (1996) Interdependence of native bee faunas and floras in changing Mediterranean communities. In: Matheson A, Buchmann SL, O’Toole C, Westrich P, Williams IH (eds) The conservation of bees. Academic press, London, pp 201–226Google Scholar
  31. Petanidou T, Lamborn E (2005) A land for flowers and bees: studying pollination ecology in Mediterranean communities. Plant Biosyst 139:279–294Google Scholar
  32. Petanidou T, Kizos T, Soulakellis N (2008) Socioeconomic dimensions of changes in the agricultural landscape of the Mediterranean basin: a case study of the abandonment of cultivation terraces on Nisyros Island, Greece. Environ Manag 41:250–266. doi: 10.1007/s00267-007-9054-6 CrossRefGoogle Scholar
  33. Pinheiro JC, Bates DM (2000) Mixed-effect models in S and S-PLUS. Springer, New YorkCrossRefGoogle Scholar
  34. Potts SG, Vulliamy B, Dafni A, Ne’eman G, O’Toole C, Roberts S, Willmer P (2003a) Response of plant-pollinator communities to fire: changes in diversity, abundance and floral reward structure. Oikos 101:103–112CrossRefGoogle Scholar
  35. Potts SG, Vulliamy B, Dafni A, Ne’eman G, Willmer P (2003b) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84:2628–2642CrossRefGoogle Scholar
  36. Potts SG, Vulliamy B, Roberts S, O’Toole C, Dafni A, Ne’eman G, Willmer PG (2004) Nectar resource diversity organises flower-visitor community structure. Entomol Exp Appl 113:103–107CrossRefGoogle Scholar
  37. Potts SG, Vulliamy B, Roberts S, O’Toole C, Dafni A, Ne’eman G, Willmer P (2005) Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecol Entomol 30:78–85CrossRefGoogle Scholar
  38. Potts SG, Petanidou T, Roberts SPM, O’Toole C, Hulbert A, Willmer P (2006) Plant-pollinator biodiversity and pollination services in a complex Mediterranean landscape. Biol Conserv 129:519–529CrossRefGoogle Scholar
  39. Potts SG, Roberts SPM, Dean R, Marris G, Brown MA, Jones R, Neumann P, Settele J (2010) Declines of managed honey bees and beekeepers in Europe. J Apic Res 49:15–22. doi: 10.3896/ibra.1.49.1.02 CrossRefGoogle Scholar
  40. R Development Core Team (2008) R: A language and environment for statistical computing. The R foundation for statistical computing. Vienna, AustriaGoogle Scholar
  41. Roulston TH, Smith SA, Brewster AL (2007) Short communication: a comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. J Kansas Entomol Soc 80:179–181CrossRefGoogle Scholar
  42. Settele J, Hammen V, Hulme P, Karlson U, Klotz S, Kotarac M, Kunin W, Marion G, O’Connor M, Petanidou T, Peterson K, Potts S, Pritchard H, Pysek P, Rounsevell M, Spangenberg J, Steffan-Dewenter I, Sykes M, Vighi M, Zobel M, Ku?hn I (2005) ALARM—Assessing LArge-scale environmental Risks for biodiversity with tested Methods. GAIA 14:69–72Google Scholar
  43. Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. TREE 20:651–652PubMedGoogle Scholar
  44. Stephen WP, Rao S (2005) Unscented color traps for non-Apis bees (Hymenoptera: Apiformes). J Kansas Entomol Soc 78:373–380CrossRefGoogle Scholar
  45. Toler TR, Evans EW, Tepedino VJ (2005) Pan-trapping for bees (Hymenoptera: Apiformes) in Utah’s west desert: the importance of color diversity. Pan-Pacific Entomol 81:103–113Google Scholar
  46. Totland Ø, Nielsen A, Bjerknes AL, Ohlson M (2006) Effects of an exotic plant and habitat disturbance on pollinator visitation and reproduction in a boreal forest herb. Am J Bot 93:868–873PubMedCrossRefGoogle Scholar
  47. Vulliamy B, Potts SG, Willmer PG (2006) The effects of cattle grazing on plant-pollinator communities in a fragmented Mediterranean landscape. Oikos 114:529–543CrossRefGoogle Scholar
  48. Westphal C, Bommarco R, Carré G, Lamborn E, Morison N, Petanidou T, Potts SG, Roberts SPM, Szentgyörgyi H, Tscheulin T, Vaissière BE, Woyciechowski M, Biesmeijer JC, Kunin WE, Settele J, Steffan-Dewenter I (2008) Measuring bee biodiversity in different European habitats and biogeographical regions. Ecol Monogr 78:653–671CrossRefGoogle Scholar
  49. Wilson JS, Griswold T, Messinger OJ (2008) Sampling bee communities (Hymenoptera: Apiformes) in a desert landscape: are pan traps sufficient? J Kansas Entomol Soc 81:288–300. doi: 10.2317/JKES-802.06.1 CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2011

Authors and Affiliations

  • Anders Nielsen
    • 1
    • 2
    • 13
  • Ingolf Steffan-Dewenter
    • 3
  • Catrin Westphal
    • 3
    • 4
  • Olivia Messinger
    • 1
    • 5
  • Simon G. Potts
    • 6
  • Stuart P. M. Roberts
    • 6
  • Josef Settele
    • 7
  • Hajnalka Szentgyörgyi
    • 8
  • Bernard E. Vaissière
    • 9
  • Michalis Vaitis
    • 1
  • Michal Woyciechowski
    • 8
  • Ioannis Bazos
    • 10
  • Jacobus C. Biesmeijer
    • 11
  • Riccardo Bommarco
    • 12
  • William E. Kunin
    • 11
  • Thomas Tscheulin
    • 1
  • Ellen Lamborn
    • 1
    • 9
  • Theodora Petanidou
    • 1
  1. 1.Laboratory of Biogeography and Ecology, Department of GeographyUniversity of the AegeanMytileneGreece
  2. 2.Department of Ecology and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway
  3. 3.Population Ecology, Department of Animal Ecology IUniversity of BayreuthBayreuthGermany
  4. 4.Agroecology, Department of Crop ScienceGeorg-August-University GöttingenGöttingenGermany
  5. 5.Department of Plant BiologySouthern Illinois UniversityCarbondaleUSA
  6. 6.Centre for Agri-Environmental Research, School of Agriculture, Policy and DevelopmentUniversity of ReadingReadingUK
  7. 7.Department of Community EcologyHelmholtz-Centre for Environmental Research, UFZHalleGermany
  8. 8.Institute of Environmental SciencesJagiellonian UniversityKrakówPoland
  9. 9.INRA (Institut National de la Recherche Agronomique), UMR 406 Abeilles et Environnement INRA-UAPVAvignon Cedex 9France
  10. 10.Department of Ecology and Taxonomy, Faculty of BiologyUniversity of AthensAthensGreece
  11. 11.Institute of Integrative and Comparative Biology and Earth and Biosphere InstituteUniversity of LeedsLeedsUK
  12. 12.Department of EcologySwedish University of Agricultural SciencesUppsalaSweden
  13. 13.Department of Biology, Centre for Ecological end Evolutionary Synthesis (CEES)University of OsloOsloNorway

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