Review Article | Published:

Safeguarding pollinators and their values to human well-being

Nature volume 540, pages 220229 (08 December 2016) | Download Citation

Abstract

Wild and managed pollinators provide a wide range of benefits to society in terms of contributions to food security, farmer and beekeeper livelihoods, social and cultural values, as well as the maintenance of wider biodiversity and ecosystem stability. Pollinators face numerous threats, including changes in land-use and management intensity, climate change, pesticides and genetically modified crops, pollinator management and pathogens, and invasive alien species. There are well-documented declines in some wild and managed pollinators in several regions of the world. However, many effective policy and management responses can be implemented to safeguard pollinators and sustain pollination services.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313 (2007)

  2. 2.

    Discover Life’s Bee Species Guide and World Checklist; (Ascher and Pickering 2014)

  3. 3.

    et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611 (2013). This study is the first to show consistent benefits from wild insects to crop pollination across the globe and that those benefits cannot be replaced by increasing the abundance of a single managed species such as honeybees

  4. 4.

    , , & Spatial and temporal trends of global pollination benefit. PLoS One 7, e35954 (2012). This study is the most comprehensive and spatially explicit assessment of the direct economic benefits of pollination to global agriculture and accounts for differences in the effective spending power of different countries

  5. 5.

    et al. IPBES. The Assessment Report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on Pollinators, Pollination and Food Production; (2016)

  6. 6.

    Convention on Biological Diversity (CBD). UNEP Decisions Adopted by the Conference of the Parties to the Convention on Biological Diversity at its Fifth Meeting (UNEP/CBD/COP/5/23/Annex III), Decision V/5; (Nairobi, 2000)

  7. 7.

    , , & Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 (2009)

  8. 8.

    , , & How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 103, 1579–1588 (2009). This study is the first to take into account the partial dependence of most crops on pollinators in quantifying the effect of total loss of pollinators on global agricultural production, cultivated area and crop production diversity

  9. 9.

    , , , & Global growth and stability of agricultural yield decrease with pollinator dependence. Proc. Natl Acad. Sci. USA 108, 5909–5914 (2011)

  10. 10.

    , , & Effects of decreases of animal pollinators on human nutrition and global health: a modelling analysis. Lancet 386, 1964–1972 (2015)

  11. 11.

    et al. Global malnutrition overlaps with pollinator-dependent micronutrient production. Proc. R. Soc. B 281, 20141799 (2014)

  12. 12.

    & The macroeconomic cost of catastrophic pollinator declines. Ecol. Econ. 126, 1–13 (2016). This study represents the most complete assessment of the consumer welfare impacts of pollinator losses both within and beyond crop markets

  13. 13.

    , , & Measuring the economic value of pollination services: principles, evidence and knowledge gaps. Ecosyst. Serv. 14, 124–132 (2015)

  14. 14.

    Agroecology: the science of natural resource management for poor farmers in marginal environments. Agric. Ecosyst. Environ. 93, 1–24 (2002)

  15. 15.

    The World Bank. Agriculture and rural development; (2015)

  16. 16.

    et al. Pollination and biological control research: are we neglecting two billion smallholders. Agric. Food Security 3, 5 (2014)

  17. 17.

    et al. Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 351, 388–391 (2016)

  18. 18.

    et al. Benefits of biotic pollination for non-timber forest products and cultivated plants. Conserv. Soc. 7, 213–219 (2009)

  19. 19.

    et al. Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe. PLoS One 9, e82996 (2014)

  20. 20.

    , , & Beekeeping for Poverty Alleviation and Livelihood Security. Vol. 1: Technological Aspects of Beekeeping (Springer, 2014)

  21. 21.

    The World History of Beekeeping and Honey Hunting (Routledge, 1999)

  22. 22.

    , & Beekeeping and sustainable livelihoods. Food and Agriculture Organisation of the United Nations. Rural Infrastructure and Agro-Industries Division, Rome, Italy. (2011)

  23. 23.

    et al. Honey as a topical treatment for wounds. Cochrane Database Syst. Rev. 3, CD005083 (2015)

  24. 24.

    , , , & Aesthetic quality of agricultural landscape elements in different seasonal stages in Switzerland. Landsc. Urban Plan. 133, 67–77 (2015)

  25. 25.

    , , & Mutualism disruption threatens global plant biodiversity: a systematic review. PLoS One 8, e66993 (2013)

  26. 26.

    et al. European Red List of Bees (Luxembourg: Publication Office of the European Union, Belgium, 2014)

  27. 27.

    et al. European Red List of Butterflies (Luxembourg: Publication Office of the European Union, Spain, 2010)

  28. 28.

    et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354 (2006)

  29. 29.

    et al. Patterns of widespread decline in North American bumble bees. Proc. Natl Acad. Sci. USA 108, 662–667 (2011)

  30. 30.

    , , & Drastic historic shifts in bumble-bee community composition in Sweden. Proc. R. Soc. B 279, 309–315 (2012)

  31. 31.

    et al. Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc. Natl Acad. Sci. USA 110, 4656–4660 (2013)

  32. 32.

    et al. Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol. Lett. 16, 870–878 (2013). This study uses 32 million data points to assess shifts in diversity of pollinator groups and plants in the Netherlands, the United Kingdom and Belgium over the last 80 years

  33. 33.

    et al. Modeling the status, trends, and impacts of wild bee abundance in the United States. Proc. Natl Acad. Sci. USA 113, 140–145 (2016)

  34. 34.

    et al. Climate change impacts on bumblebees converge across continents. Science 349, 177–180 (2015)

  35. 35.

    & The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19, 915–918 (2009)

  36. 36.

    & Honey bee colony losses. J. Apic. Res. 49, 1–6 (2010)

  37. 37.

    et al. Declines of managed honeybees and beekeepers in Europe. J. Apic. Res. 49, 15–22 (2010)

  38. 38.

    , , & The sudden collapse of pollinator communities. Ecol. Lett. 17, 350–359 (2014)

  39. 39.

    , , & Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18, 1572–1575 (2008)

  40. 40.

    , & How many flowering plants are pollinated by animals? Oikos 120, 321–326 (2011)

  41. 41.

    et al. Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in the Netherlands. Proc. Natl Acad. Sci. USA 111, 17552–17557 (2014)

  42. 42.

    & Reconstruction of historical pollination rates reveals linked declines of pollinators and plants. Oikos 120, 344–349 (2011)

  43. 43.

    et al. Protecting an ecosystem service: approaches to understanding and mitigating threats to wild insect pollinators. Adv. Ecol. Res 54, 135–206 (2016)

  44. 44.

    , & Plant–pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339, 1611–1615 (2013)

  45. 45.

    et al. The impact of over 80 years of land cover changes on bee and wasp pollinator communities in England. Proc. R. Soc. B 282, 20150294 (2015)

  46. 46.

    et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010)

  47. 47.

    & the Insect Pollinators Initiative. Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Environ 11, 251–259 (2013)

  48. 48.

    et al. Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530, 85–88 (2016)

  49. 49.

    et al. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599 (2013). This study is based on detailed spatial modelling of data from 39 crop systems globally to understand the relative influence of landscape composition, landscape configuration, farm management and their interactions on wild bee abundance and richness

  50. 50.

    , , & Interactive effects of pesticide exposure and pathogen infection on bee health – a critical analysis. Biol. Rev. Camb. Philos. Soc. 91, 1006–1019 (2016)

  51. 51.

    et al. Gains to species diversity in organically farmed fields are not propagated at the farm level. Nat. Commun. 5, 4151 (2014)

  52. 52.

    , , & Effects of an agri-environment scheme on bumblebee reproduction at local and landscape scales. Basic Appl. Ecol. 16, 519–530 (2015)

  53. 53.

    et al. Sown flower strips in southern Sweden increase abundances of wild bees and hoverflies in the wider landscape. Biol. Conserv. 184, 51–58 (2015)

  54. 54.

    , , & Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context. J. Appl. Ecol. 44, 41–49 (2007)

  55. 55.

    et al. Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis. J. Appl. Ecol. 51, 746–755 (2014)

  56. 56.

    et al. Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss–a meta-analysis. Ecol. Lett. 16, 912–920 (2013). This is the first study to provide an overview of the effectiveness of a range of agri-environment options for supporting local pollinator richness and abundance

  57. 57.

    & Flower plantings increase wild bee abundance and the pollination services provided to a pollination-dependent crop. J. Appl. Ecol. 51, 890–898 (2014)

  58. 58.

    et al. Diversification practices reduce organic to conventional yield gap. Proc. R. Soc. B 282, 20141396 (2015)

  59. 59.

    & Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol. Appl. 15, 871–881 (2005)

  60. 60.

    , & Organic farming improves pollination success in strawberries. PLoS One 7, e31599 (2012)

  61. 61.

    et al. Wildlife-friendly farming increases crop yield: evidence for ecological intensification. Proc. R. Soc. B 282, 20151740 (2015). The first to test farm-scale ‘ecological intensification’, this study found no decrease in the crop yield over a five year rotation cycle on a large English farm, despite taking up to 8% of land out of production to support ecological functions

  62. 62.

    Peasant-driven agricultural growth and food sovereignty. J. Peasant Stud. 41, 999–1030 (2014)

  63. 63.

    et al. Defining biocultural approaches to conservation. Trends Ecol. Evol. 30, 140–145 (2015)

  64. 64.

    & Reinterpreting change in traditional ecological knowledge. Hum. Ecol. 41, 643–647 (2013)

  65. 65.

    , , & Indigenous and Local Knowledge about Pollination and Pollinators Associated with Food Production: Outcomes from the Global Dialogue Workshop ((Panama 1–5 December 2014) UNESCO: Paris, 2015)

  66. 66.

    et al. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. B 281, 20140558 (2014)

  67. 67.

    et al. Conclusions of the Worldwide Integrated Assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning. Environ. Sci. Pollut. Res. 22, 148–154 (2015)

  68. 68.

    , , , & Negative effects of pesticides on wild bee communities can be buffered by landscape context. Proc. R. Soc. B 282, 20150299 (2015)

  69. 69.

    & Insect pollinated plants benefit from organic farming. Agric. Ecosyst. Environ. 118, 43–48 (2007)

  70. 70.

    et al. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ. Sci. Pollut. Res 22, 68–102 (2015)

  71. 71.

    et al. A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. Lond. B 282, 20151821 (2015)

  72. 72.

    et al. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528, 548–550 (2015)

  73. 73.

    et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521, 77–80 (2015). In a landscape experiment consisting of eight farms paired with controls, this study showed that actual field exposure to a neonicotinoid–pyrethroid seed treatment reduced wild bee densities, nesting success, bumblebee colony growth and reproduction, but did not measurably affect honeybee colony strength

  74. 74.

    , & Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012)

  75. 75.

    et al. Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat. Commun. 7, 12459 (2016)

  76. 76.

    & Pesticide Risk Assessment for Pollinators (John Wiley & Sons, 2014)

  77. 77.

    Pesticide hazard trends in orchard fruit production in Great Britain from 1992 to 2008: a time-series analysis. Pest Manag. Sci. 69, 768–774 (2013)

  78. 78.

    & Pest control in agro-ecosystems: an ecological approach. Crit. Rev. Plant Sci. 30, 74–94 (2011)

  79. 79.

    , & How to Reduce Bee Poisoning from Pesticides (Oregon State Univ. Extension Service, 2013)

  80. 80.

    et al. Farmer field schools for improving farming practices and farmer outcomes in low- and middle-income countries: a systematic review. Campbell Syst. Rev. 10, 1–335 (2014)

  81. 81.

    & Comparative analysis of pesticide action plans in five European countries. Pest Manag. Sci. 67, 1481–1485 (2011)

  82. 82.

    & Can the IOMC revive the ‘FAO code’ and take stakeholder initiatives to the developing world? Outlooks Pest Manag. 21, 125–131 (2010)

  83. 83.

    , & Impact of Bacillus thuringiensis strains on survival, reproduction and foraging behaviour in bumblebees (Bombus terrestris). Pest Manag. Sci. 66, 520–525 (2010)

  84. 84.

    et al. Effects on weed and invertebrate abundance and diversity of herbicide management in genetically modified herbicide-tolerant winter-sown oilseed rape. Proc. R. Soc. B 272, 463–474 (2005)

  85. 85.

    , , & A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316, 1475–1477 (2007)

  86. 86.

    et al. Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328, 1151–1154 (2010)

  87. 87.

    & Key global environmental impacts of genetically modified (GM) crop use 1996–2012. GM Crops Food 5, 149–160 (2014)

  88. 88.

    et al. An ecologically-based method for selecting ecological indicators for assessing risks to biological diversity from genetically-engineered plants. J. Biosaf. 22, 141–156 (2013)

  89. 89.

    et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351, 594–597 (2016)

  90. 90.

    , & Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Ecoscience 12, 289–301 (2005)

  91. 91.

    & Impacts of alien bees on native plant–pollinator relationships: a review with special emphasis on plant reproduction. Appl. Entomol. Zool. (Jpn.) 45, 37–47 (2010)

  92. 92.

    , , , & Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366 (2014). This paper sampled Apis and Bombus across 26 geographically dispersed sites in the United Kingdom revealing the co-prevalence of deformed wing virus (DWV) infections and evidence of local transmission, suggesting disease spill-over from managed honeybees to wild bumblebee species

  93. 93.

    , & Impact of managed honey bee viruses on wild bees. Curr. Opin. Virol. 19, 16–22 (2016)

  94. 94.

    , & Meliponiculture in México: problems and perspective for development. Bee World 82, 160–167 (2001)

  95. 95.

    , , , & Predicting the economic impact of an invasive species on an ecosystem service. Ecol. Appl. 17, 1832–1840 (2007)

  96. 96.

    et al. Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae). PLoS Pathogens 6, e1001160 (2010)

  97. 97.

    , & Invasive species management restores a plant–pollinator mutualism in Hawaii. J. Appl. Ecol. 50, 147–155 (2013)

  98. 98.

    & Mutualistic interactions and biological invasions. Annu. Rev. Ecol. Evol. Syst. 45, 89–113 (2014)

  99. 99.

    , , & Rapid ecological replacement of a native bumble bee by invasive species. Front. Ecol. Environ 11, 529–534 (2013)

  100. 100.

    , , & Extremely frequent bee visits increase pollen deposition but reduce drupelet set in raspberry. J. Appl. Ecol. 51, 1603–1612 (2014)

  101. 101.

    et al. in Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds et al.) 271–359 (Cambridge Univ. Press, 2014)

  102. 102.

    , , , & How does climate warming affect plant–pollinator interactions? Ecol. Lett. 12, 184–195 (2009)

  103. 103.

    , , , & Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011)

  104. 104.

    , , , & Climate change can cause spatial mismatch of trophically interacting species. Ecology 89, 3472–3479 (2008)

  105. 105.

    et al. Identifying the areas to preserve passion fruit pollination service in Brazilian Tropical Savannas under climate change. Agric. Ecosyst. Environ. 171, 39–46 (2013)

  106. 106.

    et al. Climate-driven spatial mismatches between British orchards and their pollinators: increased risks of pollination deficits. Glob. Change Biol. 20, 2815–2828 (2014)

  107. 107.

    , & Climate change impacts on pollination. Nat. Plants 2, 16092 (2016)

  108. 108.

    et al. Compounded effects of climate change and habitat alteration shift patterns of butterfly diversity. Proc. Natl Acad. Sci. USA 107, 2088–2092 (2010)

  109. 109.

    et al. Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414, 65–69 (2001)

  110. 110.

    & Achieving adequate adaptation in agriculture. Clim. Change 70, 191–200 (2005)

  111. 111.

    , , & Dynamics of insect pollinators as influenced by cocoa production systems in Ghana. J. Pollinat. Ecol. 5, 74–80 (2011)

  112. 112.

    & Ecosystem services in biologically diversified versus conventional farming systems: benefits, externalities, and trade-offs. Ecol. Soc. 17, 40 (2012)

  113. 113.

    , & Effectiveness of bats as pollinators of Stenocereus stellatus (Cactaceae) in wild, managed in situ, and cultivated populations in La Mixteca Baja, central Mexico. Am. J. Bot. 93, 1675–1683 (2006)

  114. 114.

    & Saving slash-and-burn to save biodiversity. Biotropica 42, 550–552 (2010)

  115. 115.

    , , & Sustainability of the traditional management of Agave genetic resources in the elaboration of mezcal and tequila spirits in western Mexico. Genet. Resour. Crop Evol. 60, 33–47 (2013)

  116. 116.

    , & Ecology of urban bees: a review of current knowledge and directions for future study. Cities Environ. 2, 3 (2009)

  117. 117.

    , , , & Long-term erosion of tree reproductive trait diversity in edge-dominated Atlantic forest fragments. Biol. Conserv. 142, 1154–1165 (2009)

  118. 118.

    , , , & Butterflies in semi-natural pastures and power-line corridors – effects of flower richness, management, and structural vegetation characteristics. Insect Conserv. Divers. 6, 639–657 (2013)

  119. 119.

    , & Do linear landscape elements in farmland act as biological corridors for pollen dispersal? J. Ecol. 98, 178–187 (2010)

  120. 120.

    et al. Corridors restore animal-mediated pollination in fragmented tropical forest landscapes. Proc. R. Soc. B 283, 20152347 (2016)

Download references

Acknowledgements

We thank Y. Estrada for preparing the figures and the authors of the original articles for providing the data that underpin them. We are grateful to the authors and reviewers of ref. 5 for their contributions to the report.

Author information

Affiliations

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

    • Simon G. Potts
    •  & Thomas D. Breeze
  2. Ecology Department, Biosciences Institute, S. Paulo University, 05508-090 S. Paulo Brazil and Vale Institute of Technology Sustainable Development, Belém 66055-090, Brazil

    • Vera Imperatriz-Fonseca
  3. Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES), IPBES Secretariat, UN Campus, Platz der Vereinten Nationen 1, Bonn D-53113, Germany

    • Hien T. Ngo
  4. Laboratorio Ecotono, INIBIOMA-CONICET and Centro Regional Bariloche, Universidad Nacional del Comahue, Quintral 1250, 8400 San Carlos de Bariloche, Rio Negro, Argentina

    • Marcelo A. Aizen
  5. Naturalis Biodiversity Center, PO Box 9517, Leiden 2300 RA, The Netherlands.

    • Jacobus C. Biesmeijer
  6. Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam P.O. Box 94248, The Netherlands

    • Jacobus C. Biesmeijer
  7. School of Biological Sciences, University of East Anglia, Norwich NR4 7TL, UK

    • Lynn V. Dicks
  8. Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural (IRNAD), Sede Andina, Universidad Nacional de Río Negro (UNRN), and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mitre 630, CP 8400, San Carlos de Bariloche, Río Negro, Argentina

    • Lucas A. Garibaldi
  9. CSIRO Land and Water and James Cook University Division of Tropical Environments and Societies, Box 12139, Earlville BC, Cairns, Queensland 4870, Australia

    • Rosemary Hill
  10. Helmholtz Centre for Environmental Research—UFZ, Department of Community Ecology, Theodor-Lieser-Strasse 4, 06210 Halle, Germany

    • Josef Settele
  11. iDiv, German Centre for Integrative Biodiversity Research, Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany

    • Josef Settele
  12. NERC Centre for Ecology and Hydrology, Bush Estate, Penicuik, Edinburgh EH26 0QB, UK

    • Adam J. Vanbergen

Authors

  1. Search for Simon G. Potts in:

  2. Search for Vera Imperatriz-Fonseca in:

  3. Search for Hien T. Ngo in:

  4. Search for Marcelo A. Aizen in:

  5. Search for Jacobus C. Biesmeijer in:

  6. Search for Thomas D. Breeze in:

  7. Search for Lynn V. Dicks in:

  8. Search for Lucas A. Garibaldi in:

  9. Search for Rosemary Hill in:

  10. Search for Josef Settele in:

  11. Search for Adam J. Vanbergen in:

Contributions

All authors contributed equally to the planning, evaluation of the literature and writing of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Simon G. Potts.

Reviewer Information Nature thanks R. Gill, R. Paxton and N. Raine for their contribution to the peer review of this work.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature20588

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.