REVIEW AND SYNTHESIS

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Stability of pollination services decreases with isolation from natural areas despite honey bee visits

  1. Lucas A. Garibaldi1,2,*,
  2. Ingolf Steffan-Dewenter3,
  3. Claire Kremen4,
  4. Juan M. Morales1,
  5. Riccardo Bommarco5,
  6. Saul A. Cunningham6,
  7. Luísa G. Carvalheiro7,8,9,10,†,
  8. Natacha P. Chacoff11,
  9. Jan H. Dudenhöffer12,
  10. Sarah S. Greenleaf4,
  11. Andrea Holzschuh3,12,
  12. Rufus Isaacs13,
  13. Kristin Krewenka12,
  14. Yael Mandelik14,
  15. Margaret M. Mayfield15,
  16. Lora A. Morandin4,
  17. Simon G. Potts16,
  18. Taylor H. Ricketts17,
  19. Hajnalka Szentgyörgyi18,
  20. Blandina F. Viana19,
  21. Catrin Westphal12,
  22. Rachael Winfree20,
  23. Alexandra M. Klein21

Article first published online: 1 AUG 2011

DOI: 10.1111/j.1461-0248.2011.01669.x

Issue

Ecology Letters

Ecology Letters

Volume 14, Issue 10, pages 1062–1072, October 2011

Additional Information

How to Cite

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. and Klein, A. M. (2011), Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters, 14: 1062–1072. doi: 10.1111/j.1461-0248.2011.01669.x

Author Information

  1. 1

    Laboratorio de Ecotono, INIBIOMA-CONICET and CRUB-UNCOMA, Quintral 1250, 8400 Bariloche, Río Negro, Argentina

  2. 2

    Departamento de Métodos Cuantitativos y Sistemas de Información, Facultad de Agronomía, Universidad de Buenos Aires, Av. San Martín 4453, 1417 Buenos Aires, Argentina

  3. 3

    Department of Animal Ecology and Tropical Biology, Biozentrum, University of Würzburg, Am Hubland, 97074 Würzburg, Germany

  4. 4

    Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720-3114, USA

  5. 5

    Department of Ecology, Swedish University of Agricultural Sciences, PO Box 7044, 75007 Uppsala, Sweden

  6. 6

    CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601, Australia

  7. 7

    South African National Biodiversity Institute, Kirstenbosch Research Centre, Private Bag X7, Claremont 7735, South Africa

  8. 8

    Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa

  9. 9

    Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK

  10. 10

    NCB-Naturalis, postbus 9517, 2300 RA, Leiden, The Netherlands

  11. 11

    Instituto de Argentino de Investigaciones de las Zonas Aridas, CCT CONICET Mendoza, CC 507, 5500 Mendoza, Argentina

  12. 12

    Agroecology, Georg August University Göttingen, Grisebachstr. 6, D-37077 Göttingen, Germany

  13. 13

    Department of Entomology, Michigan State University, East Lansing, MI 48824, USA

  14. 14

    Department of Entomology, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel

  15. 15

    The University of Queensland, School of Biological Sciences, Goddard Building, St Lucia Campus, Brisbane, QLD 4072, Australia

  16. 16

    Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, RG6 6AR, UK

  17. 17

    Conservation Science Program, WWF, Washington D.C., USA

  18. 18

    Institute of Environmental Sciences, Jagiellonian University, ul. Gronostajowa 7, 30-387, Kraków, Poland

  19. 19

    Instituto de Biologia, Universidade Federal da Bahia, 40170-210, Ondina, Salvador, Bahia, Brazil

  20. 20

    Department of Entomology, Rutgers University, New Brunswick, NJ 08901, USA

  21. 21

    Institute of Ecology, Section Ecosystem Functions, Leuphana University of Lüneburg, Scharnhorststraße 1, 21335 Lüneburg, Germany

  1. †

    Between Luísa Carvalheiro and Rachael Winfree, we choose an alphabetical order of authors, as they contributed equally to this synthesis.

*E-mail: garibald@agro.uba.ar

  1. †

    Between Luísa Carvalheiro and Rachael Winfree, we choose an alphabetical order of authors, as they contributed equally to this synthesis.

Publication History

  1. Issue published online: 12 SEP 2011
  2. Article first published online: 1 AUG 2011
  3. Editor, Yvonne Buckley Manuscript received 5 June 2011 Manuscript accepted 29 June 2011

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Keywords:

  • Apis mellifera;
  • Bombus spp.;
  • ecosystem services;
  • flower visitors;
  • landscape management;
  • pollinator services;
  • richness;
  • spatial stability;
  • sustainable agricultural landscapes;
  • temporal stability

Ecology Letters (2011) 14: 1062–1072

Abstract

Sustainable agricultural landscapes by definition provide high magnitude and stability of ecosystem services, biodiversity and crop productivity. However, few studies have considered landscape effects on the stability of ecosystem services. We tested whether isolation from florally diverse natural and semi-natural areas reduces the spatial and temporal stability of flower-visitor richness and pollination services in crop fields. We synthesised data from 29 studies with contrasting biomes, crop species and pollinator communities. Stability of flower-visitor richness, visitation rate (all insects except honey bees) and fruit set all decreased with distance from natural areas. At 1 km from adjacent natural areas, spatial stability decreased by 25, 16 and 9% for richness, visitation and fruit set, respectively, while temporal stability decreased by 39% for richness and 13% for visitation. Mean richness, visitation and fruit set also decreased with isolation, by 34, 27 and 16% at 1 km respectively. In contrast, honey bee visitation did not change with isolation and represented > 25% of crop visits in 21 studies. Therefore, wild pollinators are relevant for crop productivity and stability even when honey bees are abundant. Policies to preserve and restore natural areas in agricultural landscapes should enhance levels and reliability of pollination services.

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