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Pollinator communities in strawberry crops – variation at multiple spatial scales

Published online by Cambridge University Press:  24 April 2015

E.J. Ahrenfeldt ,
B.K. Klatt ,
J. Arildsen ,
N. Trandem ,
G.K.S. Andersson ,
T. Tscharntke ,
H.G. Smith  and
L. Sigsgaard
E.J. Ahrenfeldt*
Affiliation:
Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
B.K. Klatt
Affiliation:
Agroecology, Georg-August-University Göttingen, Grisebachstraße 6, 37077 Göttingen, Germany Department of Biology, Lund University, Ecology building, 223 62 Lund, Sweden Centre for Environmental and Climate Research, Lund University, Ecology building, 223 62 Lund, Sweden
J. Arildsen
Affiliation:
Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
N. Trandem
Affiliation:
Norwegian Institute for Agricultural and Environmental Research (Bioforsk), Høgskoleveien 7, 1432 Ås, Norway
G.K.S. Andersson
Affiliation:
Department of Biology, Lund University, Ecology building, 223 62 Lund, Sweden Centre for Environmental and Climate Research, Lund University, Ecology building, 223 62 Lund, Sweden
T. Tscharntke
Affiliation:
Agroecology, Georg-August-University Göttingen, Grisebachstraße 6, 37077 Göttingen, Germany
H.G. Smith
Affiliation:
Department of Biology, Lund University, Ecology building, 223 62 Lund, Sweden Centre for Environmental and Climate Research, Lund University, Ecology building, 223 62 Lund, Sweden
L. Sigsgaard
Affiliation:
Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
*
*Author for correspondence Phone: (+45) 22 82 26 69 E-mail: ericajuel@plen.ku.dk
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Abstract

Predicting potential pollination services of wild bees in crops requires knowledge of their spatial distribution within fields. Field margins can serve as nesting and foraging habitats for wild bees and can be a source of pollinators. Regional differences in pollinator community composition may affect this spill-over of bees. We studied how regional and local differences affect the spatial distribution of wild bee species richness, activity-density and body size in crop fields. We sampled bees both from the field centre and at two different types of semi-natural field margins, grass strips and hedges, in 12 strawberry fields. The fields were distributed over four regions in Northern Europe, representing an almost 1100 km long north-south gradient. Even over this gradient, daytime temperatures during sampling did not differ significantly between regions and did therefore probably not impact bee activity. Bee species richness was higher in field margins compared with field centres independent of field size. However, there was no difference between centre and margin in body-size or activity-density. In contrast, bee activity-density increased towards the southern regions, whereas the mean body size increased towards the north. In conclusion, our study revealed a general pattern across European regions of bee diversity, but not activity-density, declining towards the field interior which suggests that the benefits of functional diversity of pollinators may be difficult to achieve through spill-over effects from margins to crop. We also identified dissimilar regional patterns in bee diversity and activity-density, which should be taken into account in conservation management.

Keywords

activity-densitybody sizepollinationstrawberrywild bee diversity
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 4 , August 2015 , pp. 497 - 506
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Copyright © Cambridge University Press 2015 

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References

Albano, S., Salvado, E., Borges, P. & Mexia, A. (2009 a) Floral visitors, their frequency, activity rate and index of visitation rate in the strawberry fields of Ribatejo, Portugal: selection of potential pollinators. Part 1. Advances in Horticultural Sciences 23, 238–245.Google Scholar
Albano, S., Salvado, E., Duarte, S., Mexia, A. & Borges, P. (2009 b) Pollination effectiveness of different strawberry floral visitors in Ribatejo, Portugal: selection of potential pollinators. Part 2. Advances in Horticultural Sciences 23, 246–253.Google Scholar
Amiet, F., Herrmann, M., Müller, A. & Neumeyer, R. (2001) Fauna Helvetica 6. pp. 208 in Anonymous (Ed.) Apidae 3: Halictus, Lasioglossum. Centre Suisse de Cartographie de la Faune (CSCF/SEG).Google Scholar
Amiet, F., Herrmann, M., Müller, A. & Neumeyer, R. (2004) Fauna Helvetica 9. pp. 273 in Anonymous (Ed.) Apidae 4: Anthidium, Chelostoma, Coelioxys, Dioxys, Heriades, Lithurgus, Megachile, Osmia, Stelis. Centre Suisse de Cartographie de la Faune (CSCF/SEG).Google Scholar
Amiet, F., Herrmann, M., Müller, A. & Neumeyer, R. (2007) Fauna Helvetica 20, Apidae 5. pp. 356 Ammobates, Ammobatoides, Anthophora, Biastes, Ceratina, Dasypoda, Epeoloides, Epeolus, Eucera, Macropis, Melecta, Melitta, Nomada, Pasites, Tetralonia, Thyreus, Xylocopa. Centre Suisse de Cartographie de la Faune (CSCF/SEG).Google Scholar
Andersson, G.K., Rundlöf, M. & Smith, H.G. (2012) Organic farming improves pollination success in strawberries. PLoS ONE 7, e31599.Google ScholarPubMed
Bailey, S., Requier, F., Nusillard, B., Roberts, S.P., Potts, S.G. & Bouget, C. (2014). Distance from forest edge affects bee pollinators in oilseed rape fields. Ecology and Evolution 4, 370–380.Google Scholar
Barrow, D. & Pickard, R. (1984) Size-related selection of food plants by bumblebees. Ecological Entomology 9, 369–373.Google Scholar
Bell, W.J. (1990) Central place foraging. pp. 171–187. in Anonymous (Ed.) Searching Behaviour. Netherlands, Springer.Google Scholar
Berg, Ø. (2000) Aculeata of Norway. 3. Eleven species of bees new to Norway (Hymenoptera: Apoidea). Norwegian Journal of Entomology 47, 177–181.Google Scholar
Bibby, B.M., Martinussen, T. & Skovgaard, I.M. (2004) Experimental design in agricultural sciences. pp. 218 in Anonymous (Ed.) Copenhagen, Royal Veterinary and Agricultural University.Google Scholar
Bommarco, R., Marini, L. & Vaissière, B.E. (2012) Insect pollination enhances seed yield, quality, and market value in oilseed rape. Oecologia 1–8.Google Scholar
Cane, J.H. (1996) Ground-nesting bees: the neglected pollinator resource for agriculture, pp. 309–324 in VII International Symposium on Pollination, vol 437.Google Scholar
Cappelen, J. & Jensen, J.J. (2001) Jordens Klima – Guide til vejr og Klima i 156 Lande (Update). Trafikministeriet, Danmarks Meteorologiske Institut.Google Scholar
Chagnon, M., Ingras, J. & Oliveira, D.D.E. (1993) Complementary aspects of strawberry pollination by honey and indigenous bees (Hymenoptera). Journal of Economic Entomology 86, 416–420.Google Scholar
Charney, N. & Record, S. (2009) Vegetarian – an R Package: Jost Diversity Measures for Community Data. 1.2.Google Scholar
Corbet, S.A., Fussell, M., Ake, R., Fraser, A., Gunson, C., Savage, A. & Smith, K. (1993) Temperature and the pollinating activity of social bees. Ecological Entomology 18, 17–30.Google Scholar
Cresswell, J.E., Osborne, J.L. & Goulson, D. (2000) An economic model of the limits to foraging range in central place foragers with numerical solutions for bumblebees. Ecological Entomology 25, 249–255.Google Scholar
Cumming, G., Fidler, F. & Vaux, D.L. (2007) Error bars in experimental biology. Journal of Cell Biology 177, pp. 7–11.Google Scholar
De Oliveira, D., Savoie, L. & Vincent, C. (1990) Pollinators of cultivated strawberry in Quebec. pp. 420–424 in VI International Symposium on Pollination, vol. 288.Google Scholar
Delaplane, K.S. & Mayer, D.F. (2000) Crop pollination by bees. pp. 352 in Anonymous (Ed.) Wallingford, Oxfordshire, UK and Wallingford England, New York. CABI Publishing.Google Scholar
Duelli, P., Blank, E. & Frech, M. (1991) The contribution of seminatural habitats to arthropod diversity in agricultural areas. pp. 29–38 in Conference Proceeding.Google Scholar
Ekroos, J., Piha, M. & Tiainen, J. (2008) Role of organic and conventional field boundaries on boreal bumblebees and butterflies. Agriculture, Ecosystems and Environment 124, 155–159.Google Scholar
Fontaine, C., Dajoz, I., Meriguet, J. & Loreau, M. (2005) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biology 4, e1.Google Scholar
Free, J.B. (1968) The foraging behaviour of honeybees (Apis mellifera) and bumblebees (Bombus spp.) on blackcurrant (Ribes nigrum), raspberry (Rubus idaeus) and strawberry (Fragaria x ananassa) flowers. Journal of Applied Ecology 157–168.Google Scholar
Free, J. & Williams, I.H. (1976) Pollination as a factor limiting the yield of field beans (Vicia faba L.). Journal of Agricultural Science 87(2), 395–399.Google Scholar
Fussell, M. & Corbet, S.A. (1992) Flower usage by bumble-bees: a basis for forage plant management. Journal of Applied Ecology, 451–465.Google Scholar
Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., Morales, J.M., Bommarco, R., Cunningham, S.A., Carvalheiro, L.G., Chacoff, N.P., Dudenhöffer, J.H., Greenleaf, S.S., Holzschuh, A., Isaacs, R., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L.A., Potts, S.G., Ricketts, T.H., Szentgyörgyi, H., Viana, B.F., Westphal, C., Winfree, R., Klein, A.M. (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters 14, 1062–1072.Google Scholar
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A., Kremen, C., Carvalheiro, L.G., Harder, L.D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N.P., Dudenhöffer, J.H., Freitas, B.M., Ghazoul, J., Greenleaf, S.S., Hipólito, J., Holzschuh, A., Howlett, B., Isaacs, R., Javorek, S.K., Kennedy, C.M., Krewenka, K., Krishnan, S., Mandelik, Y., Mayfield, M.M., Motzke, I., Munyuli, T., Nault, B.A., Otieno, M., Petersen, J., Pisanty, G., Potts, S.G., Rader, R., Ricketts, T.H., Rundlöf, M., Seymour, C.L., Christof Schüepp, C., Szentgyörgyi, H., Taki, H., Tscharntke, T., Vergara, C.H., Viana, B.F., Wanger, T.C., Westphal, C., Williams, N., Klein, A.M. (2013) Wild pollinators enhance fruit set of crops regardless of honeybee abundance. Science 339, 1608–1611.Google Scholar
Gathmann, A. & Tscharntke, T. (2002) Foraging ranges of solitary bees. Journal of Animal Ecology 71, 757–764.Google Scholar
Goulson, D. (2003) Conserving wild bees for crop pollination. Journal of Food Agriculture and Environment 1, 142–144.Google Scholar
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.Google Scholar
Grundel, R., Frohnapple, K.J., Jean, R.P. & Pavlovic, N.B. (2011) Effectiveness of bowl trapping and netting for inventory of a bee community. Environmental Entomology 40, 374–380.Google Scholar
Hammer, K. & Nørgaard Holm, S. (1970) Danske humlebier og snyltehumler. Natur Og Museum 14, 4.Google Scholar
Hannon, L.E. & Sisk, T.D. (2009) Hedgerows in an agri-natural landscape: potential habitat value for native bees. Biological Conservation 142, 2140–2154.Google Scholar
Heinrich, B. (2004) Bumblebee economics. pp. 245 in Anonymous (Ed.) Cambridge, Mass. Harvard University Press.Google Scholar
Heinrich, B. & Heinrich, M.J.E. (1983) Size and caste in temperature regulation by bumblebees. Physiological Zoology, 552–562.Google Scholar
Hoehn, P., Tscharntke, T., Tylianakis, J.M. & Steffan-Dewenter, I. (2008) Functional group diversity of bee pollinators increases crop yield. Proceedings of the Royal Society B: Biological Sciences 275, 2283.Google Scholar
Holzschuh, A., Steffan Dewenter, I. & Tscharntke, T. (2008) Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 117, 354–361.Google Scholar
Holzschuh, A., Steffan-Dewenter, I. & Tscharntke, T. (2010) How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids? Journal of Animal Ecology 79, 491–500.CrossRefGoogle ScholarPubMed
Jauker, F., Diekötter, T., Schwarzbach, F. & Wolters, V. (2009) Pollinator dispersal in an agricultural matrix: opposing responses of wild bees and hoverflies to landscape structure and distance from main habitat. Landscape Ecology 24, 547–555.Google Scholar
Klatt, B.K. (2013) Bee pollination of strawberries on different spatial scales–from crop varieties and fields to landscapes . Dissertation, Niedersächsische Staats- und Universitätsbibliothek, Göttingen.Google Scholar
Klein, A., Steffan-Dewenter, I. & Tscharntke, T. (2003) Pollination of Coffea canephora in relation to local and regional agroforestry management. Journal of Applied Ecology 40, 837–845.Google Scholar
Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C. & Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274, 303.Google Scholar
Krebs, C.J. (1999) Ecological methodology. pp. 620 in Anonymous (Ed.) New York, Addison Wesley Longman.Google Scholar
Kremen, C., Williams, N.M. & Thorp, R.W. (2002) Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences of the United States of America 99, 16812.Google Scholar
Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P. & Thorp, R.W. (2004) The area requirements of an ecosystem service: crop pollination by native bee communities in california. Ecology Letters 7, 1109–1119.Google Scholar
Lagerlöf, J., Stark, J. & Svensson, B. (1992) Margins of agricultural fields as habitats for pollinating insects. Agriculture, Ecosystems and Environment 40, 117–124.Google Scholar
Le Feon, V., Schermann-Legionnet, A., Delettre, Y., Aviron, S., Billeter, R., Bugter, R., Hendrickx, F. & Burel, F. (2010) Intensification of agriculture, landscape composition and wild bee communities: a large scale study in four European countries. Agriculture, Ecosystems and Environment 137, 143–150.Google Scholar
Loken, A. (1973) Studies on Scandinavian bumblebees (Hymenoptera, Apidae). Norsk Entomologisk Tidsskrift 20, 1–218.Google Scholar
Lomolino, M.V., Riddle, B.R. & Brown, J.H. (2006) Biogeography. Sunderland Massachusetts, Sinauer Associates, Inc. Google Scholar
Lonsdorf, E., Kremen, C., Ricketts, T., Winfree, R., Williams, N. & Greenleaf, S. (2009) Modelling pollination services across agricultural landscapes. Annals of Botany 103, 1589–1600.Google Scholar
Madsen, H.B. & Calabuig, I. (2012) Kommenteret checkliste over danmarks bier–Del 5: Apidae (hymenoptera, apoidea). Entomologiske Meddelelser 80, 7–52.Google Scholar
Magurran, A.E. (2004) Measuring biological diversity. African Journal of Aquatic Science 29, 285–286.Google Scholar
Marshall, E.J.P., West, T.M. & Kleijn, D. (2006) Impacts of an agri-environment field margin prescription on the flora and fauna of arable farmland in different landscapes. Agriculture, Ecosystems and Environment 113, 36–44.Google Scholar
Martin, H. (2014) http://www.wildbienen.de/. 2014.Google Scholar
Michener, C.D. (2000) The bees of the world. pp. 913 in Anonymous (Ed.) Baltimore, Md: Johns Hopkins University Press.Google Scholar
Morandin, L.A. & Kremen, C. (2013) Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecological Applications 23, 829–839.Google Scholar
Morandin, L.A. & Winston, M.L. (2005) Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecological Applications 15, 871–881.Google Scholar
Obrist, M. & Duelli, P. (2010) Rapid biodiversity assessment of arthropods for monitoring average local species richness and related ecosystem services. Biodiversity and Conservation 19, 2201–2220.Google Scholar
Patiny, S., Rasmont, P. & Michez, D. (2009) A survey and review of the status of wild bees in the West-Palaearctic region. Apidologie 40, 313–331.Google Scholar
Paydas, S., Eti, S., Kaftanoglu, O., Yasa, E. & Derin, K. (1998) Effects of pollination of strawberries grown in plastic greenhouses by honeybees and bumblebees on the yield and quality of the fruits. pp. 443–452 in XXV International Horticultural Congress, Part 3: Culture Techniques with Special Emphasis on Environmental Implications vol. 513.CrossRefGoogle Scholar
Pinheiro, J.C. & Bates, D.M. (2000) Mixed effects models in S and S-PLUS. pp. 544 in Anonymous (Ed.) New York, Springer.Google Scholar
Popic, T.J., Davila, Y.C. & Wardle, G.M. (2013) Evaluation of common methods for sampling invertebrate pollinator assemblages: net sampling out-perform pan traps. PLoS ONE 8, e66665.Google Scholar
Potts, S.G., 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. Ecological Entomology. 30, 78–85.Google Scholar
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25, 345–353.Google Scholar
R Development Core Team. (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. ISBN 3-900051-07-0 Google Scholar
Ricketts, T.H., Regetz, J., Steffan Dewenter, I., Cunningham, S.A., Kremen, C., Bogdanski, A., Gemmill Herren, B., Greenleaf, S.S., Klein, A.M. & Mayfield, M.M. (2008) Landscape effects on crop pollination services: are there general patterns? Ecology Letters 11, 499–515.Google Scholar
Rundlöf, M., Nilsson, H. & Smith, H.G. (2008) Interacting effects of farming practice and landscape context on bumble bees. Biological Conservation 141, 417–426.Google Scholar
Scheuchel, E. (2000) Schlüssel der arten der familie anthophoridae. Illustrierte Bestimmungstabellen Der Wildbienen Deutschlands Und Österreichs. Band II.Google Scholar
Schleuning, M., Fründ, J., Klein, A., Abrahamczyk, S., Alarcón, R., Albrecht, M., Andersson, G.K., Bazarian, S., Böhning-Gaese, K. & Bommarco, R. (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology 22, 1925–1931.Google Scholar
Stone, G. & Willmer, P. (1989) Warm-up rates and body temperatures in bees: the importance of body size, thermal regime and phylogeny. Journal of Experimental Biology 147, 303.Google Scholar
Stout, J.C. (2000) Does size matter? Bumblebee behaviour and the pollination of Cytisus scoparius L. (fabaceae). Apidologie 31, 129–140.Google Scholar
Vahl, M. & Humlum, J. (1949). Vahl's Climatic Zones and Biochores. Univ. Forl, Aarhus University Press.Google Scholar
Vázquez, D.P., Morris, W.F. & Jordano, P. (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecology Letters 8, 1088–1094.Google Scholar
Walther-Hellwig, K. & Frankl, R. (2000) Foraging habitats and foraging distances of bumblebees, Bombus spp.(Hym., Apidae), in an agricultural landscape. Journal of Applied Entomology 124, 299–306.Google Scholar
Westphal, C., Bommarco, R., Carré, G., Lamborn, E., Morison, N., Petanidou, T., Potts, S.G., Roberts, S.P., Szentgyörgyi, H. & Tscheulin, T. (2008) Measuring bee diversity in different European habitats and biogeographical regions. Ecological. Monographs 78, 653–671.CrossRefGoogle Scholar
Wilkaniec, Z. & Radajewska, B. (1996) Solitary bee Osmia rufa L.(Apoidea, Megachilidae) as pollinator of strawberry cultivated in an unheated plastic tunnel. III International Strawberry Symposium 439, 489–494.Google Scholar
Wolda, H. (1981) Similarity indices, sample size and diversity. Oecologia 50, 296–302.Google Scholar
Zurbuchen, A., Bachofen, C., Müller, A., Hein, S. & Dorn, S. (2010 a) Are landscape structures insurmountable barriers for foraging bees? A mark-recapture study with two solitary pollen specialist species. Apidologie 41, 497–508.Google Scholar
Zurbuchen, A., Cheesman, S., Klaiber, J., Müller, A., Hein, S. & Dorn, S. (2010 b) Long foraging distances impose high costs on offspring production in solitary bees. Journal of Animal Ecology 79, 674–681.Google Scholar
Zurbuchen, A., Landert, L., Klaiber, J., Müller, A., Hein, S. & Dorn, S. (2010 c) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biological Conservation 143, 669–676.Google Scholar