Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

David Kleijn^{1

2}, Rachael Winfree³, Ignasi Bartomeus⁴, Luísa G Carvalheiro^{5

6}, Mickaël Henry^{7

8}, Rufus Isaacs⁹, Alexandra-Maria Klein¹⁰, Claire Kremen¹¹, Leithen K M'Gonigle¹¹, Romina Rader¹², Taylor H Ricketts¹³, Neal M Williams¹⁴, Nancy Lee Adamson, John S Ascher¹⁵, András Báldi¹⁶, Péter Batáry¹⁷, Faye Benjamin³, Jacobus C Biesmeijer⁶, Eleanor J Blitzer¹⁸, Riccardo Bommarco¹⁹, Mariëtte R Brand^{20

21

22}, Vincent Bretagnolle²³, Lindsey Button²⁴, Daniel P Cariveau³, Rémy Chifflet²⁵, Jonathan F Colville²⁰, Bryan N Danforth¹⁸, Elizabeth Elle²³, Michael P D Garratt²⁶, Felix Herzog²⁷, Andrea Holzschuh²⁸, Brad G Howlett²⁹, Frank Jauker³⁰, Shalene Jha³¹, Eva Knop³², Kristin M Krewenka¹⁷, Violette Le Féon⁷, Yael Mandelik³³, Emily A May⁹, Mia G Park¹⁸, Gideon Pisanty³³, Menno Reemer³⁴, Verena Riedinger²⁸, Orianne Rollin^{7

8

35}, Maj Rundlöf³⁶, Hillary S Sardiñas¹¹, Jeroen Scheper¹, Amber R Sciligo¹¹, Henrik G Smith^{36

37}, Ingolf Steffan-Dewenter²⁸, Robbin Thorp¹⁴, Teja Tscharntke¹⁷, Jort Verhulst, Blandina F Viana³⁸, Bernard E Vaissière^{7

8}, Ruan Veldtman^{20

21}, Kimiora L Ward¹⁴, Catrin Westphal¹⁷, Simon G Potts²⁶

Affiliations

¹ Animal Ecology Team, Center for Ecosystem Studies, Alterra, Wageningen UR, PO Box 47, 6700AA Wageningen, The Netherlands.
² Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708 PB Wageningen, The Netherlands.
³ Department of Ecology, Evolution and Natural Resources, Rutgers University, 14 College Farm Road, New Brunswick, New Jersey 08901, USA.
⁴ Departmento Ecología Integrativa, Estación Biológica de Doñana (EDB-CSIC), Avenida Américo Vespucio s/n, 41092 Sevilla, Spain.
⁵ School of Biology, University of Leeds, Miall Building, Clarendon Road, Leeds LS2 9JT, UK.
⁶ Department of Terrestrial Zoology, Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands.
⁷ UR 406 Abeilles et Environnement, INRA, CS 40509, F-84914 Avignon, France.
⁸ UMT Protection des Abeilles dans l'Environnement, INRA, CS 40509, F-84914 Avignon, France.
⁹ Department of Entomology, Michigan State University, 578 Wilson Road, East Lansing, Michigan 48824, USA.
¹⁰ Nature Conservation and Landscape Ecology Group, Earth and Environmental Sciences, University of Freiburg, Freiburg D-79106, Germany.
¹¹ Department of Environmental Science, Policy and Management, University of California, 130 Mulford Hall, Berkeley, California 94720-3114, USA.
¹² School of Environmental and Rural Science, University of New England, Armidale, New South Wales 2350, Australia.
¹³ Gund Institute for Ecological Economics, University of Vermont, 617 Main Street, Burlington, Vermont 05405, USA.
¹⁴ Department of Entomology and Nematology, University of California, Davis, 1 Shields Avenue, Davis, California 95616, USA.
¹⁵ Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Singapore.
¹⁶ Institute of Ecology and Botany, MTA Centre for Ecological Research, Alkotmány u. 2-4, Vácrátót 2163, Hungary.
¹⁷ Agroecology Group, Department of Crop Sciences, Georg-August-University, Grisebachstr. 6, 37077 Göttingen, Germany.
¹⁸ Department of Entomology, Cornell University, Ithaca, New York 14853, USA.
¹⁹ Department of Ecology, Swedish University of Agricultural Sciences, Uppsala 75007, Sweden.
²⁰ South African National Biodiversity Institute, Kirstenbosch Research Centre, Private Bag X7, Claremont 7735, South Africa.
²¹ Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa.
²² Iziko South African Museum, 25 Queen Victoria Street, Cape Town 8000, South Africa.
²³ Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS and Université La Rochelle, F-79360 Beauvoir-sur-Niort, France.
²⁴ Department of Biological Sciences, Simon Fraser University,8888 University Drive, Burnaby, British Columbia, Canada V5A 1S6.
²⁵ Plateforme Régionale d'Innovation "Agriculture Biologique et Périurbaine Durable", EPLEFPA du Lycée Nature, Allée des Druides, 85000 La Roche-sur-Yon, France.
²⁶ Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading RG6 6AR, UK.
²⁷ Agricultural Landscapes and Biodiversity, Agroscope, Reckenholzstr. 191, CH-8046 Zurich, Switzerland.
²⁸ Department of Animal Ecology and Tropical Biology, Biocenter, University of Würzburg, Am Hubland, 97074 Würzburg, Germany.
²⁹ Sustainable Production, The New Zealand Institute for Plant and Food Research Limited, Private Bag 4704, Christchurch 8140, New Zealand.
³⁰ Department of Animal Ecology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany.
³¹ Department of Integrative Biology, University of Texas at Austin, 401 Biological Laboratories, Austin, Texas 78712, USA.
³² Community Ecology Group, University of Bern, Baltzerstr. 6, 3012 Bern, Switzerland.
³³ Department of Entomology, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel.
³⁴ EIS Kenniscentrum Insecten, Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands.
³⁵ ITSAP - Institut de l'abeille, 149 rue de Bercy, F-75012 Paris, France.
³⁶ Department of Biology, Lund University, S-223 62 Lund, Sweden.
³⁷ Centre of Environmental and Climate Research, Lund University, S-223 62 Lund, Sweden.
³⁸ Biology Institute, Federal University of Bahia, Rua Barão de Jeremoabo, s/n, Campus Universitário de Ondina, Salvador, Bahia 40170-290, Brazil.

PMID: 26079893
PMCID: PMC4490361
DOI: 10.1038/ncomms8414

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

David Kleijn et al. Nat Commun. 2015.

. 2015 Jun 16:6:7414.

doi: 10.1038/ncomms8414.

Authors

Affiliations

¹ Animal Ecology Team, Center for Ecosystem Studies, Alterra, Wageningen UR, PO Box 47, 6700AA Wageningen, The Netherlands.
² Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708 PB Wageningen, The Netherlands.
³ Department of Ecology, Evolution and Natural Resources, Rutgers University, 14 College Farm Road, New Brunswick, New Jersey 08901, USA.
⁴ Departmento Ecología Integrativa, Estación Biológica de Doñana (EDB-CSIC), Avenida Américo Vespucio s/n, 41092 Sevilla, Spain.
⁵ School of Biology, University of Leeds, Miall Building, Clarendon Road, Leeds LS2 9JT, UK.
⁶ Department of Terrestrial Zoology, Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands.
⁷ UR 406 Abeilles et Environnement, INRA, CS 40509, F-84914 Avignon, France.
⁸ UMT Protection des Abeilles dans l'Environnement, INRA, CS 40509, F-84914 Avignon, France.
⁹ Department of Entomology, Michigan State University, 578 Wilson Road, East Lansing, Michigan 48824, USA.
¹⁰ Nature Conservation and Landscape Ecology Group, Earth and Environmental Sciences, University of Freiburg, Freiburg D-79106, Germany.
¹¹ Department of Environmental Science, Policy and Management, University of California, 130 Mulford Hall, Berkeley, California 94720-3114, USA.
¹² School of Environmental and Rural Science, University of New England, Armidale, New South Wales 2350, Australia.
¹³ Gund Institute for Ecological Economics, University of Vermont, 617 Main Street, Burlington, Vermont 05405, USA.
¹⁴ Department of Entomology and Nematology, University of California, Davis, 1 Shields Avenue, Davis, California 95616, USA.
¹⁵ Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Singapore.
¹⁶ Institute of Ecology and Botany, MTA Centre for Ecological Research, Alkotmány u. 2-4, Vácrátót 2163, Hungary.
¹⁷ Agroecology Group, Department of Crop Sciences, Georg-August-University, Grisebachstr. 6, 37077 Göttingen, Germany.
¹⁸ Department of Entomology, Cornell University, Ithaca, New York 14853, USA.
¹⁹ Department of Ecology, Swedish University of Agricultural Sciences, Uppsala 75007, Sweden.
²⁰ South African National Biodiversity Institute, Kirstenbosch Research Centre, Private Bag X7, Claremont 7735, South Africa.
²¹ Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa.
²² Iziko South African Museum, 25 Queen Victoria Street, Cape Town 8000, South Africa.
²³ Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS and Université La Rochelle, F-79360 Beauvoir-sur-Niort, France.
²⁴ Department of Biological Sciences, Simon Fraser University,8888 University Drive, Burnaby, British Columbia, Canada V5A 1S6.
²⁵ Plateforme Régionale d'Innovation "Agriculture Biologique et Périurbaine Durable", EPLEFPA du Lycée Nature, Allée des Druides, 85000 La Roche-sur-Yon, France.
²⁶ Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading RG6 6AR, UK.
²⁷ Agricultural Landscapes and Biodiversity, Agroscope, Reckenholzstr. 191, CH-8046 Zurich, Switzerland.
²⁸ Department of Animal Ecology and Tropical Biology, Biocenter, University of Würzburg, Am Hubland, 97074 Würzburg, Germany.
²⁹ Sustainable Production, The New Zealand Institute for Plant and Food Research Limited, Private Bag 4704, Christchurch 8140, New Zealand.
³⁰ Department of Animal Ecology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany.
³¹ Department of Integrative Biology, University of Texas at Austin, 401 Biological Laboratories, Austin, Texas 78712, USA.
³² Community Ecology Group, University of Bern, Baltzerstr. 6, 3012 Bern, Switzerland.
³³ Department of Entomology, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel.
³⁴ EIS Kenniscentrum Insecten, Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands.
³⁵ ITSAP - Institut de l'abeille, 149 rue de Bercy, F-75012 Paris, France.
³⁶ Department of Biology, Lund University, S-223 62 Lund, Sweden.
³⁷ Centre of Environmental and Climate Research, Lund University, S-223 62 Lund, Sweden.
³⁸ Biology Institute, Federal University of Bahia, Rua Barão de Jeremoabo, s/n, Campus Universitário de Ondina, Salvador, Bahia 40170-290, Brazil.

PMID: 26079893
PMCID: PMC4490361
DOI: 10.1038/ncomms8414

Erratum in

Corrigendum: Delivery of crop pollination services is an insufficient argument for wild pollinator conservation.
Kleijn D, Winfree R, Bartomeus I, Carvalheiro LG, Henry M, Isaacs R, Klein AM, Kremen C, M'Gonigle LK, Rader R, Ricketts TH, Williams NM, Adamson NL, Ascher JS, Báldi A, Batáry P, Benjamin F, Biesmeijer JC, Blitzer EJ, Bommarco R, Brand MR, Bretagnolle V, Button L, Cariveau DP, Chifflet R, Colville JF, Danforth BN, Elle E, Garratt MP, Herzog F, Holzschuh A, Howlett BG, Jauker F, Jha S, Knop E, Krewenka KM, Le Féon V, Mandelik Y, May EA, Park MG, Pisanty G, Reemer M, Riedinger V, Rollin O, Rundlöf M, Sardiñas HS, Scheper J, Sciligo AR, Smith HG, Steffan-Dewenter I, Thorp R, Tscharntke T, Verhulst J, Viana BF, Vaissiére BE, Veldtman R, Ward KL, Westphal C, Potts SG. Kleijn D, et al. Nat Commun. 2016 Feb 18;7:10841. doi: 10.1038/ncomms10841. Nat Commun. 2016. PMID: 26887922 Free PMC article. No abstract available.

Abstract

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.

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Figures

**Figure 1. The relative contribution of individual species in wild bee communities to crop pollination.**
(a) The rank distribution of the contribution of wild bee species to crop production value in their biogeographical area. Dominant species, contributing at least 5% of all visits within a given study, are indicated in blue. Bars indicate 95% confidence intervals. (b) The cumulative number of bee species known to exist in the countries in which the studies were done, compared with an asymptotic estimate of the number of species that visit the flowers of the studied crops (Chao1 estimator), and the number of dominant crop-visiting wild bee species. Lightly dashed lines indicate estimates±s.e.

**Figure 2. The relation between dominant crop-visiting bee species and cover of semi-natural habitats in agricultural landscapes.**
(a) The proportion of dominant crop-visiting bee species in bee communities in habitats other than flowering crops is negatively related to the proportion of semi-natural habitat within a 1,000-m radius (F_1,14=14.47, P=0.002). (b) The relation between the proportion of semi-natural habitat in agricultural landscapes and bee abundance differs between dominant crop-visiting species and all other bee species (interaction type of bee and cover semi-natural habitat: X²_1,31=8.20, P=0.004). Lines indicate back-transformed model predictions for dominant (dashed) and all other bee species (solid). (c) The relation between the proportion of semi-natural habitat in agricultural landscapes and the bee species richness differs between dominant crop-visiting species and all other species (interaction type of bee and cover semi-natural habitat: X²_1,31=7.84, P=0.005). Lines indicate back-transformed model predictions for dominant (dashed) and all other bee species (solid).

**Figure 3. The effect of measures mitigating biodiversity loss on dominant crop-visiting bee species.**
Bars indicate mean pooled abundance (±s.e.) of dominant crop-visiting bee species on sites with management measures mitigating biodiversity loss compared with control sites in nine different studies. Abbreviations and test statistics: DE—Germany, F_1,40=12.69, P<0.001; HU—Hungary, F_1,38=1.13, P=0.295; NL—Netherlands, F_1,39=0.36, P=0.553; CH—Switzerland, F_1,39=1.29, P=0.263; UK—United Kingdom, F_1,39=4.97, P=0.032; CA1—California study 1, F_1,37=6.97, P=0.012; CA2—California study 2, F_1,9=29.83, P<0.001; MI—Michigan, F_1,5.6=15.10, P=0.009; NJ—New Jersey; F_1,10=10.06, P=0.010. *P<0.05, **P<0.01, ***P<0.001.

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References

1. Green R. E., Cornell S. J., Scharlemann J. P. W. & Balmford A. Farming and the fate of wild nature. Science 307, 550–555 (2005). - PubMed
1. Butchart S. H. M. et al. Global biodiversity: indicators of recent declines. Science 328, 1164–1168 (2010). - PubMed
1. TEEB. The Economics of Ecosystems and Biodiversity: Mainstreaming the Economics of Nature: A synthesis of the approach, conclusions and recommendations of TEEB http://www.teebweb.org/our-publications/teeb-study-reports/synthesis-rep... (2010).
1. Balvanera P. et al. Conserving biodiversity and ecosystem services. Science 291, 2047–2047 (2001). - PubMed
1. Balmford A. et al. Economic reasons for conserving wild nature. Science 297, 950–953 (2002). - PubMed

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Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

Affiliations

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

Authors

Affiliations

Erratum in

Abstract

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources