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.
References
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
Atmar W, Patterson BD (1993) The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96:373–382
Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387
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 313:351–354
Cane JH, Minckley RL, Kervin LJ (2000) Sampling bees (Hymenoptera: Apiformes) for pollinator community studies: pitfalls of pan-trapping. J Kansas Entomol Soc 73:225–231
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 8:148–159
Chao A, Chazdon RL, Colwell RK, Shen TJ (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371
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
Colwell RK, Chang XM, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727
Committee on the Status of Pollinators in North America (2007) Status of pollinators in North America. The National Academies Press, Washington, DC
Dafni A, Kevan PG, Husband BC, editors (2005) Practical pollination ecology. Enviroquest, Cambridge, Ontario, Canada
Detsis V, Diamantopoulos J, Kosmas C (2000) Collembolan assemblages in Lesvos, Greece. Effects of differences in vegetation and precipitation. Acta Oecologica 21(2):149–159
Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biology 4:129–135
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 98:8–14
Ghazoul J (2005) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol Evol 20:367–373
Guimarães PR, Guimarães P (2006) Improving the analyses of nestedness for large sets of matrices. Environm Modell Softw 21:1512–1513
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant–pollinator interactions. Annu Rev Ecol Syst 29:83–112
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 27:199–212
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
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 30:889–900
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 10:299–314
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 24:329–335
Magurran AE (2004) Measuring biological diversity. Blackwell Publ, Malden
Marathianou M, Kosmas C, Gerontidis S, Detsis V (2000) Land-use evolution and degradation in Lesvos (Greece): a historical approach. Land Degrad Develop 11:63–73
Mayer C (2005) Does grazing influence biodiversity? Afr Biodivers Mol Org Ecosyst 173–179
Michener CD (2007) The bees of the world. John Hopkins University Press, Baltimore
Nielsen A, Ims RA (2000) Bumble bee pollination of the sticky catchfly in a fragmented agricultural landscape. Ecoscience 7:157–165
O’Toole C, Raw A (2004) Bees of the world. Facts On File, New York
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 29:153–160
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 201–226
Petanidou T, Lamborn E (2005) A land for flowers and bees: studying pollination ecology in Mediterranean communities. Plant Biosyst 139:279–294
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
Pinheiro JC, Bates DM (2000) Mixed-effect models in S and S-PLUS. Springer, New York
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 101:103–112
Potts SG, Vulliamy B, Dafni A, Ne’eman G, Willmer P (2003b) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84:2628–2642
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 113:103–107
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 30:78–85
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 129:519–529
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
R Development Core Team (2008) R: A language and environment for statistical computing. The R foundation for statistical computing. Vienna, Austria
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 80:179–181
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 14:69–72
Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. TREE 20:651–652
Stephen WP, Rao S (2005) Unscented color traps for non-Apis bees (Hymenoptera: Apiformes). J Kansas Entomol Soc 78:373–380
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 81:103–113
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 93:868–873
Vulliamy B, Potts SG, Willmer PG (2006) The effects of cattle grazing on plant-pollinator communities in a fragmented Mediterranean landscape. Oikos 114:529–543
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 78:653–671
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
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).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Nielsen, A., Steffan-Dewenter, I., Westphal, C. et al. Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques. Ecol Res 26, 969–983 (2011). https://doi.org/10.1007/s11284-011-0852-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11284-011-0852-1