MEASURING BEE DIVERSITY IN DIFFERENT EUROPEAN HABITATS AND BIOGEOGRAPHICAL REGIONS

Bee pollinators are currently recorded with many different sampling methods. However, the relative performances of these methods have not been systematically evaluated and compared. In response to the strong need to record ongoing shifts in pollinator diversity and abundance, global and regional pollinator initiatives must adopt standardized sampling protocols when developing large-scale and long-term monitoring schemes. We systematically evaluated the performance of six sampling methods (observation plots, pan traps, standardized and variable transect walks, trap nests with reed internodes or paper tubes) that are commonly used across a wide range of geographical regions in Europe and in two habitat types (agricultural and seminatural). We focused on bees since they represent the most important pollinator group worldwide. Several characteristics of the methods were considered in order to evaluate their performance in assessing bee diversity: sample coverage, observed species richness, species richness estimators, collector biases (identified by subunit-based rarefaction curves), species composition of the samples, and the indication of overall bee species richness (estimated from combined total samples). The most efficient method in all geographical regions, in both the agricultural and seminatural habitats, was the pan trap method. It had the highest sample coverage, collected the highest number of species, showed negligible collector bias, detected similar species as the transect methods, and was the best indicator of overall bee species richness. The transect methods were also relatively efficient, but they had a significant collector bias. The observation plots showed poor performance. As trap nests are restricted to cavity-nesting bee species, they had a naturally low sample coverage. However, both trap nest types detected additional species that were not recorded by any of the other methods. For large-scale and long-term monitoring schemes with surveyors with different experience levels, we recommend pan traps as the most efficient, unbiased, and cost-effective method for sampling bee diversity. Trap nests with reed internodes could be used as a complementary sampling method to maximize the numbers of collected species. Transect walks are the principal method for detailed studies focusing on plant-pollinator associations. Moreover, they can be used in monitoring schemes after training the surveyors to standardize their collection skills.

[1]  Marco Vighi,et al.  ALARM: Assessing LArge-scale environmental Risks for biodiversity with tested Methods , 2005 .

[2]  Teja Tscharntke,et al.  Mass flowering crops enhance pollinator densities at a landscape scale , 2003 .

[3]  W. P. Stephen,et al.  Unscented Color Traps for Non-Apis Bees (Hymenoptera: Apiformes) , 2005 .

[4]  Lynn V. Dicks,et al.  Compartmentalization in plant–insect flower visitor webs , 2002 .

[5]  C. Zachariades,et al.  Effects of Habitat Fragmentation on Pollinator Diversity and Plant Reproductive Success in Renosterveld Shrublands of South Africa , 2002 .

[6]  D. A. Moeller Geographic structure of pollinator communities, reproductive assurance, and the evolution of self-pollination. , 2006, Ecology.

[7]  J. Neff Bees, pollination systems and plant diversity , 1993 .

[8]  A. Klein,et al.  SPATIOTEMPORAL VARIATION IN THE DIVERSITY OF HYMENOPTERA ACROSS A TROPICAL HABITAT GRADIENT , 2005 .

[9]  J. Cane,et al.  Sampling Bees (Hymenoptera: Apiformes) for Pollinator Community Studies: Pitfalls of Pan-trapping , 2000 .

[10]  T. Tscharntke,et al.  Bumblebees experience landscapes at different spatial scales: possible implications for coexistence , 2006, Oecologia.

[11]  T. Tscharntke,et al.  Bioindication using trap‐nesting bees and wasps and their natural enemies: community structure and interactions , 1998 .

[12]  L. Chittka,et al.  Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks , 2004, Journal of Comparative Physiology A.

[13]  M. L. Buschini Species diversity and community structure in trap-nesting bees in Southern Brazil , 2006 .

[14]  K. Delaplane,et al.  Crop Pollination by Bees , 2000 .

[15]  Rebecca E. Irwin,et al.  TEMPORAL AND SPATIAL VARIATION IN POLLINATION OF A MONTANE HERB: A SEVEN-YEAR STUDY , 2005 .

[16]  Michel Loreau,et al.  Functional Diversity of Plant–Pollinator Interaction Webs Enhances the Persistence of Plant Communities , 2005, PLoS biology.

[17]  S. Potts,et al.  Pollinator diversity and crop pollination services are at risk. , 2005, Trends in ecology & evolution.

[18]  Robert K. Colwell,et al.  A new statistical approach for assessing similarity of species composition with incidence and abundance data , 2004 .

[19]  W. D. J. Kirk Ecologically seIective coIoured traps , 1984 .

[20]  T. Tscharntke,et al.  How does landscape context contribute to effects of habitat fragmentation on diversity and population density of butterflies? , 2003 .

[21]  C. Romão,et al.  Interpretation manual of European Union habitats. , 1996 .

[22]  Neal M. Williams,et al.  The area requirements of an ecosystem service: crop pollination by native bee communities in California , 2004 .

[23]  B. Rathcke,et al.  Habitat fragmentation and plant-pollinator interactions , 1993 .

[24]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[25]  Robert K. Colwell,et al.  Estimating terrestrial biodiversity through extrapolation. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[26]  Michael L. Rosenzweig,et al.  Species Diversity in Space and Time , 1997 .

[27]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[28]  L. Packer,et al.  Changes in the bee fauna (Hymenoptera: Apoidea) of an old field site in southern Ontario, revisited after 34 years , 2006, The Canadian Entomologist.

[29]  David W. Inouye,et al.  Techniques for Pollination Biologists , 1993 .

[30]  Robert K. Colwell,et al.  Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness , 2001 .

[31]  I. Steffan‐Dewenter Importance of Habitat Area and Landscape Context for Species Richness of Bees and Wasps in Fragmented Orchard Meadows , 2003 .

[32]  Neal M Williams,et al.  Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. , 2006, Ecological applications : a publication of the Ecological Society of America.

[33]  A. Klein,et al.  Importance of pollinators in changing landscapes for world crops , 2007, Proceedings of the Royal Society B: Biological Sciences.

[34]  C. Michener The Bees of the World , 2000 .

[35]  J. Hanula,et al.  Effects of prescribed fire and fire surrogates on floral visiting insects of the blue ridge province in North Carolina , 2007 .

[36]  E. Evans,et al.  Pan-trapping for bees (Hymenoptera: Apiformes) in Utah’s west desert: the importance of color diversity , 2005 .

[37]  O. Phillips,et al.  Extinction risk from climate change , 2004, Nature.

[38]  Stephen A. Smith,et al.  A Comparison of Pan Trap and Intensive Net Sampling Techniques for Documenting a Bee (Hymenoptera: Apiformes) Fauna , 2007 .

[39]  Robert K. Colwell,et al.  INTERPOLATING, EXTRAPOLATING, AND COMPARING INCIDENCE-BASED SPECIES ACCUMULATION CURVES , 2004 .

[40]  N. Williams,et al.  Variation in Native Bee Faunas and its Implications for Detecting Community Changes , 2001 .

[41]  David W. Inouye,et al.  ENDANGERED MUTUALISMS: The Conservation of Plant-Pollinator Interactions , 1998 .

[42]  J. Banaszak Studies on methods of censusing the numbers of bees (Hymenoptera, Apoidea). , 1980 .

[43]  J. Tautz,et al.  Visual constraints in foraging bumblebees: Flower size and color affect search time and flight behavior , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. Cane Habitat Fragmentation and Native Bees: a Premature Verdict? , 2001 .

[45]  S. Cunningham,et al.  Depressed pollination in habitat fragments causes low fruit set , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  Jaboury Ghazoul,et al.  Buzziness as usual? Questioning the global pollination crisis. , 2005, Trends in ecology & evolution.

[47]  M. Aizen,et al.  HABITAT FRAGMENTATION, NATIVE INSECT POLLINATORS, AND FERAL HONEY BEES IN ARGENTINE, "CHACO SERRANO"' , 1994 .

[48]  Michael J. Crawley,et al.  Statistical Computing: An Introduction to Data Analysis using S-Plus , 2002 .

[49]  Robert K. Colwell,et al.  Abundance‐Based Similarity Indices and Their Estimation When There Are Unseen Species in Samples , 2006, Biometrics.

[50]  William J. Sutherland,et al.  Ecological Census Techniques: Contents , 1996 .

[51]  J. Barthell,et al.  Monitoring Solitary Bees in Modified Wildland Habitats: Implications for Bee Ecology and Conservation , 1998 .

[52]  T. Tscharntke,et al.  Local species immigration, extinction, and turnover of butterflies in relation to habitat area and habitat isolation , 2003, Oecologia.

[53]  Gretchen C Daily,et al.  Economic value of tropical forest to coffee production. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Teja Tscharntke,et al.  Foraging trip duration of bumblebees in relation to landscape‐wide resource availability , 2006 .

[55]  J. Cane The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields , 1997 .

[56]  W. Wcislo,et al.  Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. , 1996, Annual review of entomology.

[57]  O. Hoegh‐Guldberg,et al.  Ecological responses to recent climate change , 2002, Nature.

[58]  A. P. Schaffers,et al.  Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands , 2006, Science.

[59]  E. Pollard A method for assessing changes in the abundance of butterflies , 1977 .

[60]  L. Chittka,et al.  Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study , 2004, Journal of Comparative Physiology A.

[61]  Teja Tscharntke,et al.  SCALE‐DEPENDENT EFFECTS OF LANDSCAPE CONTEXT ON THREE POLLINATOR GUILDS , 2002 .

[62]  Neal M. Williams,et al.  Crop pollination from native bees at risk from agricultural intensification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Cane,et al.  Substrates and Materials Used for Nesting by North American Osmia Bees (Hymenoptera: Apiformes: Megachilidae) , 2007 .

[64]  J Memmott,et al.  The structure of a plant-pollinator food web. , 1999, Ecology letters.

[65]  T. Tscharntke,et al.  Trap-nesting bees and wasps colonizing set-aside fields: succession and body size, management by cutting and sowing , 1994, Oecologia.

[66]  R. B. Roberts Trap-nesting wasps and bees : life histories, nests and associates , 1967 .

[67]  Paul H. Williams,et al.  What to protect?—Systematics and the agony of choice , 1991 .

[68]  A. Magurran,et al.  Measuring Biological Diversity , 2004 .

[69]  Pat Willmer,et al.  LINKING BEES AND FLOWERS: HOW DO FLORAL COMMUNITIES STRUCTURE POLLINATOR COMMUNITIES? , 2003 .

[70]  Ola Jennersten Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set , 1988 .

[71]  P. Williams The Distribution and Decline of British Bumble Bees (Bombus Latr.) , 1982 .

[72]  R. Thorp,et al.  Colour‐coded sampling: the pan trap colour preferences of oligolectic and nonoligolectic bees associated with a vernal pool plant , 1999 .

[73]  J. A. Thomas Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[74]  T. Ricketts,et al.  Confronting a biome crisis: global disparities of habitat loss and protection , 2004 .

[75]  J. Free Insect pollination of crops , 1970 .