SpringerLink
Log in

Insufficient pollinator visitation often limits yield in crop systems worldwide

  • Article
  • Published:

From Nature Ecology & Evolution

View current issue Submit your manuscript

Abstract

Declining pollinator populations could threaten global food production, especially if current crop yields are limited by insufficient pollinator visitation to flowers, in a phenomenon referred to as ‘pollinator limitation’. Here, we assess the global prevalence of pollinator limitation, explore the risk factors, such as crop type or geographic region, that predict where pollinator limitation is more likely and ask by how much increases in pollinator visitation could improve crop yields. We address these questions using 198,360 plant–pollinator interactions and 2,083 yield measurements from 32 crop species grown in 120 study systems. We find that 28–61% of global crop systems are pollinator limited and that this limitation most frequently occurs in blueberry, coffee and apple crops. For a few datasets, we note that the probability of pollinator limitation decreases with greater forest land cover surrounding a crop field at 1 km, although average effect sizes are small. Finally, we estimate that for those crops we identify as pollinator limited, increasing pollinator visitation at all farms to existing levels observed in the 90th percentile of each study system would close 63% of yield gaps between high- and low-yielding fields. Our findings show variations in sensitivity to pollinator limitation across diverse crop systems and indicate that realistic increases in pollinator visitation could mitigate crop yield shortfalls attributable to pollinator limitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1: Our global dataset represents 198,360 plant–pollinator interactions and 2,083 yield measurements.
Fig. 2: Three hypothetical relationships between crop yield and insect visitation, resulting in unique pollinator limitation scenarios.
Fig. 3: We estimate that 28–61% of global crops exhibit some pollinator limitation.
Fig. 4: Predicted effects of a range of forested land cover on the probability of pollinator limitation for 79 datasets.
Fig. 5: Illustrative example of yield gap due to changes in pollinator density.

Similar content being viewed by others

Data availability

The CropPol data33 used to generate the results of this study are publicly available and continually updated on Zenodo via https://zenodo.org/doi/10.5281/zenodo.4311291 (ref. 76).

Code availability

The datafiles, R code and custom Bayesian scripts used to generate the results of this study are available on Figshare via https://doi.org/10.6084/m9.figshare.24878868.v2 (ref. 77).

References

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

    Article  PubMed  Google Scholar 

  2. Dicks, L. V. et al. A global-scale expert assessment of drivers and risks associated with pollinator decline. Nat. Ecol. Evol. 5, 1453–1461 (2021).

    Article  PubMed  Google Scholar 

  3. Potts, S. et al. (eds). The Assessment Report on Pollinators, Pollination and Food Production (IPBES, 2017).

  4. Aizen, M. A., Garibaldi, L. A., Cunningham, S. A. & Klein, A. M. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18, 1572–1575 (2008).

    Article  CAS  PubMed  Google Scholar 

  5. Aizen, M. A., Garibaldi, L. A., Cunningham, S. A. & Klein, A. M. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 103, 1579–1588 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Aizen, M. A., Garibaldi, L. A. & Harder, L. D. Myth and reality of a global crisis for agricultural pollination. Ecol. Austral 32, 698–715 (2022).

    Article  Google Scholar 

  7. DeVetter, L. W. et al. Toward evidence-based decision support systems to optimize pollination and yields in highbush blueberry. Front. Sustain. Food Syst. 6, 1006201 (2022).

    Article  Google Scholar 

  8. Haig, D. & Westoby, M. On limits to seed production. Am. Nat. 131, 757–759 (1988).

    Article  Google Scholar 

  9. Bennett, J. M. et al. GloPL, a global data base on pollen limitation of plant reproduction. Sci. Data 5, 180249 (2018).

  10. Bennett, J. M. et al. Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene. Nat. Commun. 11, 3999 (2020).

  11. Rosenheim, J. A., Williams, N. M., Schreiber, S. J. & Rapp, J. M. Modest pollen limitation of lifetime seed production is in good agreement with modest uncertainty in whole-plant pollen receipt: (a reply to Burd). Am. Nat. 187, 397–404 (2016).

    Article  PubMed  Google Scholar 

  12. Aizen, M. A. & Harder, L. D. Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88, 271–281 (2007).

    Article  PubMed  Google Scholar 

  13. Ashman, T.-L. et al. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421 (2004).

    Article  Google Scholar 

  14. Reilly, J. R. et al. Crop production in the USA is frequently limited by a lack of pollinators. Proc. R. Soc. B 287, 20200922 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Osterman, J. et al. Global trends in the number and diversity of managed pollinator species. Agric. Ecosyst. Environ. 322, 107653 (2021).

    Article  Google Scholar 

  16. Sáez, A. et al. Managed honeybees decrease pollination limitation in self-compatible but not in self-incompatible crops. Proc. R. Soc. B 289, 20220086 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Knight, T. M. et al. Pollen limitation of plant reproduction: pattern and process. Annu. Rev. Ecol. Evol. Syst. 36, 467–497 (2005).

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  19. Estravis-Barcala, M. C. et al. Evaluating honey bee foraging behaviour and their impact on pollination success in a mixed almond orchard. Apidologie 52, 860–872 (2021).

    Article  Google Scholar 

  20. Isaacs, R. & Kirk, A. K. Pollination services provided to small and large highbush blueberry fields by wild and managed bees. J. Appl. Ecol. 47, 841–849 (2010).

    Article  Google Scholar 

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

    Article  Google Scholar 

  22. Delaney, A. et al. Local-scale tree and shrub diversity improves pollination services to shea trees in tropical West African parklands. J. Appl. Ecol. 57, 1504–1513 (2020).

    Article  Google Scholar 

  23. Forbes, S. J. & Northfield, T. D. Increased pollinator habitat enhances cacao fruit set and predator conservation. Ecol. Appl. 27, 887–899 (2017).

    Article  PubMed  Google Scholar 

  24. Kremen, C., Williams, N. M. & Thorp, R. W. Crop pollination from native bees at risk from agricultural intensification. Proc. Natl Acad. Sci. USA 99, 16812–16816 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  27. Kennedy, C. M. et al. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599 (2013).

    Article  PubMed  Google Scholar 

  28. Ricketts, T. H. et al. Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11, 499–515 (2008).

    Article  PubMed  Google Scholar 

  29. Cusser, S., Neff, J. L. & Jha, S. Natural land cover drives pollinator abundance and richness, leading to reductions in pollen limitation in cotton agroecosystems. Agric. Ecosyst. Environ. 226, 33–42 (2016).

    Article  Google Scholar 

  30. Lundin, O. & Raderschall, C. A. Landscape complexity benefits bumble bee visitation in faba bean (Vicia faba minor L.) but crop productivity is not pollinator-dependent. Agric. Ecosyst. Environ. 314, 107417 (2021).

    Article  Google Scholar 

  31. Fijen, T. P. M., Scheper, J. A., Boekelo, B., Raemakers, I. & Kleijn, D. Effects of landscape complexity on pollinators are moderated by pollinators’ association with mass-flowering crops. Proc. R. Soc. B 286, 20190387 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Chatterjee, A., Chatterjee, S., Smith, B., Cresswell, J. E. & Basu, P. Predicted thresholds for natural vegetation cover to safeguard pollinator services in agricultural landscapes. Agric. Ecosyst. Environ. 290, 106785 (2020).

    Article  Google Scholar 

  33. Allen‐Perkins, A. et al. CropPol: a dynamic, open and global database on crop pollination. Ecology 103, e3614 (2022).

    Article  PubMed  Google Scholar 

  34. Urban-Mead, K. R. et al. Early spring orchard pollinators spill over from resource-rich adjacent forest patches. J. Appl. Ecol. 60, 553–564 (2023).

    Article  Google Scholar 

  35. Proesmans, W., Bonte, D., Smagghe, G., Meeus, I. & Verheyen, K. Importance of forest fragments as pollinator habitat varies with season and guild. Basic Appl. Ecol. 34, 95–107 (2019).

    Article  Google Scholar 

  36. Proesmans, W. et al. Small forest patches as pollinator habitat: oases in an agricultural desert? Landsc. Ecol. 34, 487–501 (2019).

    Article  Google Scholar 

  37. Devkota, K., dos Santos, C. F. & Blochtein, B. Mustard plants distant from forest fragments receive a lower diversity of flower-visiting insects. Basic Appl. Ecol. 47, 35–43 (2020).

    Article  Google Scholar 

  38. Smith, C., Harrison, T., Gardner, J. & Winfree, R. Forest-associated bee species persist amid forest loss and regrowth in eastern North America. Biol. Conserv. 260, 109202 (2021).

    Article  Google Scholar 

  39. Mola, J. M., Hemberger, J., Kochanski, J., Richardson, L. L. & Pearse, I. S. The importance of forests in bumble bee biology and conservation. Bioscience 71, 1234–1248 (2021).

    Article  Google Scholar 

  40. Garibaldi, L. A., Sáez, A., Aizen, M. A., Fijen, T. & Bartomeus, I. Crop pollination management needs flower-visitor monitoring and target values. J. Appl. Ecol. 57, 664–670 (2020).

    Article  Google Scholar 

  41. Knapp, J. L. & Osborne, J. L. Courgette production: pollination demand, supply and value. J. Econ. Entomol. 110, 1973–1979 (2017).

    Article  PubMed  Google Scholar 

  42. Gazzea, E., Batáry, P. & Marini, L. Global meta-analysis shows reduced quality of food crops under inadequate animal pollination. Nat. Commun. 14, 4463 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Albrecht, M. et al. The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis. Ecol. Lett. 23, 1488–1498 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Rollin, O. & Garibaldi, L. A. Impacts of honeybee density on crop yield: a meta-analysis. J. Appl. Ecol. 56, 1152–1163 (2019).

    Article  Google Scholar 

  45. Eeraerts, M. et al. Landscape-level honey bee hive density, instead of field-level hive density, enhances honey bee visitation in blueberry. Landsc. Ecol. 38, 583–595 (2023).

    Article  Google Scholar 

  46. Mallinger, R., Ternest, J. J. & Naranjo, S. M. Blueberry yields increase with bee visitation rates, but bee visitation rates are not consistently predicted by colony stocking densities. J. Econ. Entomol. 114, 1441–1451 (2021).

    Article  CAS  PubMed  Google Scholar 

  47. Gibbs, J., Elle, E., Bobiwash, K., Haapalainen, T. & Isaacs, R. Contrasting pollinators and pollination in native and non-native regions of highbush blueberry production. PLoS ONE 11, e0158937 (2016).

  48. Benjamin, F. E. & Winfree, R. Lack of pollinators limits fruit production in commercial blueberry (Vaccinium corymbosum). Environ. Entomol. 43, 1574–1583 (2014).

    Article  PubMed  Google Scholar 

  49. Kleijn, D. et al. Ecological intensification: bridging the gap between science and practice. Trends Ecol. Evol. 34, 154–166 (2019).

    Article  PubMed  Google Scholar 

  50. Zamorano, J., Bartomeus, I., Grez, A. A. & Garibaldi, L. A. Field margin floral enhancements increase pollinator diversity at the field edge but show no consistent spillover into the crop field: a meta-analysis. Insect Conserv. Divers. 13, 519–531 (2020).

    Article  Google Scholar 

  51. Krimmer, E., Martin, E. A., Krauss, J., Holzschuh, A. & Steffan-Dewenter, I. Size, age and surrounding semi-natural habitats modulate the effectiveness of flower-rich agri-environment schemes to promote pollinator visitation in crop fields. Agric. Ecosyst. Environ. 284, 106590 (2019).

    Article  Google Scholar 

  52. Martin, E. A. et al. The interplay of landscape composition and configuration: new pathways to manage functional biodiversity and agroecosystem services across Europe. Ecol. Lett. 22, 1083–1094 (2019).

    Article  PubMed  Google Scholar 

  53. Lichtenberg, E. M. et al. A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes. Glob. Change Biol. 23, 4946–4957 (2017).

    Article  Google Scholar 

  54. Harder, L. D. & Thomson, J. D. Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am. Nat. 133, 323–344 (1989).

    Article  Google Scholar 

  55. Chacoff, N. P., Aizen, M. A. & Aschero, V. Proximity to forest edge does not affect crop production despite pollen limitation. Proc. R. Soc. B 275, 907–913 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Harrison, T., Gibbs, J. & Winfree, R. Forest bees are replaced in agricultural and urban landscapes by native species with different phenologies and life-history traits. Glob. Change Biol. 24, 287–296 (2018).

    Article  Google Scholar 

  57. Bartual, A. M., Bocci, G., Marini, S. & Moonen, A. C. Local and landscape factors affect sunflower pollination in a Mediterranean agroecosystem. PLoS ONE 13, e0203990 (2018).

  58. Castle, D., Grass, I. & Westphal, C. Fruit quantity and quality of strawberries benefit from enhanced pollinator abundance at hedgerows in agricultural landscapes. Agric. Ecosyst. Environ. 275, 14–22 (2019).

    Article  Google Scholar 

  59. MacInnis, G., Buddle, C. M. & Forrest, J. R. K. Small wild bee abundance declines with distance into strawberry crops regardless of field margin habitat. Basic Appl. Ecol. 44, 14–23 (2020).

    Article  Google Scholar 

  60. Lemanski, N. J., Williams, N. M. & Winfree, R. Greater bee diversity is needed to maintain crop pollination over time. Nat. Ecol. Evol. 6, 1516–1523 (2022).

    Article  PubMed  Google Scholar 

  61. Aldercotte, A. H., Simpson, D. T. & Winfree, R. Crop visitation by wild bees declines over an 8-year time series: a dramatic trend, or just dramatic between-year variation? Insect Conserv. Divers. 15, 522–533 (2022).

    Article  Google Scholar 

  62. Fijen, T. P. M. et al. Insect pollination is at least as important for marketable crop yield as plant quality in a seed crop. Ecol. Lett. 21, 1704–1713 (2018).

    Article  PubMed  Google Scholar 

  63. Reilly, J. et al. Wild insects and honey bees are equally important to crop yields in a global analysis. Glob. Ecol. Biogeogr. 33, e13843 (2024).

  64. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).

  65. Stan Development Team. RStan: the R interface to Stan. R package version 2.32.3 https://mc-stan.org/ (2023).

  66. Srikanth, C. D., Kuberappa, G. C. & Shweatha, B. V. Role of attractants on insect pollinators diversity with special reference to pollination in increasing the productivity of bottle gourd, Lagenaria siceraria L. Mysore J. Agric. Sci. 47, 16–21 (2013).

    Google Scholar 

  67. Thu, M. K. Pollination ecology of ridged gourd (Luffa acutangula Roxb.) in VFRDC, Hlegu. First Myanmar-Korea Conf. 1, 1–10 (2018).

  68. Deyto, R. C. & Cervancia, C. R. Floral biology and pollination of ampalaya (Momordica charantia L.). Philipp. Agric. Sci. 92, 8–18 (2009).

    Google Scholar 

  69. Murtaugh, P. A. Performance of several variable-selection methods applied to real ecological data. Ecol. Lett. 12, 1061–1068 (2009).

    Article  PubMed  Google Scholar 

  70. Sutherland, C. et al. Practical advice on variable selection and reporting using Akaike information criterion. Proc. R. Soc. B 290, 20231261 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Tredennick, A. T., Hooker, G., Ellner, S. P. & Adler, P. B. A practical guide to selecting models for exploration, inference and prediction in ecology. Ecology 102, e03336 (2021).

    Article  PubMed  Google Scholar 

  72. Bivand, R., Keitt, T. & Rowlingson, B. rgdal: Bindings for the ‘Geospatial’ data abstraction library. R package version 1.6-3 https://cran.r-project.org/package=rgdal (2022).

  73. Hijmans, R. J. & van Etten, J. raster: Geographic analysis and modeling with raster data. R package version 3.6-26 http://cran.r-project.org/package=raster (2022).

  74. Kendall, L. K. et al. The potential and realized foraging movements of bees are differentially determined by body size and sociality. Ecology 103, e3809 (2022).https://doi.org/10.1002/ecy.3809

  75. Giménez-García, A. et al. Pollination supply models from a local to global scale. Web Ecol. 23, 99–129 (2023).

    Article  Google Scholar 

  76. Bartomeus, I. & Allen-Perkins, A. ibartomeus/OBservData: Blueberry. Zenodo https://zenodo.org/doi/10.5281/zenodo.4311291 (2023).

  77. Turo, K. J., Reilly, J. R, Fijen, T. P. M., Magrach, A. & Winfree, R. Insufficient pollinator visitation often limits yield in crop systems worldwide: Datafiles, R code, and custom Bayesian scripts. Figshare https://doi.org/10.6084/m9.figshare.24878868.v2 (2023).

Download references

Acknowledgements

We are indebted to D.T. Simpson for his independent statistical review of our custom Bayesian script and feedback on our analyses and manuscript. This research was funded by the United States Department of Agriculture National Institute of Food and Agriculture grant no. 2021- 67012-35153 to K.J.T., and the 2017–2018 Belmont Forum and BiodivERsA joint call for research proposals, under the BiodivScen ERA-Net COFUND programme and with the funding organizations Agencia Estatal de Investigación, Spain (AEI), Dutch Research Council (NWO), Ministerio de Educación, Cultura, Ciencia y Tecnología, Argentina (ECCyT) and the United States National Science Foundation (NSF) to R.W. Additional funding was provided from Programme NWO-Green, which is jointly funded by NWO and Nunhems Netherlands BV (BASF) under project no. 870.15.030 to T.P.M.F. and from the Spanish Ministry of Science and Innovation and the European Social Fund through the Ramón y Cajal Program (RYC2021-032351-I) to A.M.

Author information

Authors and Affiliations

  1. Department of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ, USA

    Katherine J. Turo, James R. Reilly & Rachael Winfree

  2. Plant Ecology and Nature Conservation Group, Department of Environmental Sciences, Wageningen University & Research, Wageningen, The Netherlands

    Thijs P. M. Fijen

  3. Basque Centre for Climate Change (BC3), Leioa, Spain

    Ainhoa Magrach

  4. IKERBASQUE, Basque Foundation for Science, Bilbao, Spain

    Ainhoa Magrach

Authors
  1. Katherine J. Turo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James R. Reilly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thijs P. M. Fijen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ainhoa Magrach
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rachael Winfree
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

K.J.T. conceived the project, conducted statistical analyses, created figures and tables and wrote and revised the manuscript. J.R.R. conceived the project, conducted statistical analyses, created figures and revised the manuscript. T.P.M.F. provided data, contributed to analyses and revised the manuscript. A.M. provided data and revised the manuscript. R.W. conceived the project and revised the manuscript.

Corresponding author

Correspondence to Katherine J. Turo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Parthiba Basu, Liam Kendall, Deepa Senapathi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1, 3 and 5 and Tables 2 and 4.

Reporting Summary

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Turo, K.J., Reilly, J.R., Fijen, T.P.M. et al. Insufficient pollinator visitation often limits yield in crop systems worldwide. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02460-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41559-024-02460-2

  • Springer Nature Limited

Search

Navigation