Avoiding the ecological limits of forage fish for fed aquaculture

Abstract

Aquaculture is supporting demand and surpassing wild-caught seafood. Yet, most fed aquaculture species (finfish and crustacea) rely on wild-captured forage fish for essential fatty acids and micronutrients, an important but limited resource. As the fastest growing food sector in the world, fed aquaculture demand will eventually surpass ecological supply of forage fish, but when and how best to avoid this ecological boundary is unclear. Using global production data, feed use trends, and human consumption patterns, we show how combined actions of fisheries reform, reduced feed use by non-carnivorous aquaculture and agricultural species, and greater consistent inclusion of fish by-products in China-based production can circumvent forage fish limits by mid-century. However, we also demonstrate that the efficacies of such actions are diminished if global diets shift to more seafood-heavy (that is, pescatarian) diets and are further constrained by possible ecosystem-based fisheries regulations in the future. Long-term, nutrient-equivalent alternative feed sources are essential for more rapid and certain aquaculture sustainability.

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Fig. 1: Animal production (livestock, poultry and fed aquaculture species) and forage fish use trends.
Fig. 2: Historical and projected potential of forage fish supply and use.
Fig. 3: Current (baseline) modelled average use of forage fish.

References

  1. 1.

    The State of World Fisheries and Aquaculture 2016 (SOFIA) (FAO, 2016).

  2. 2.

    Martin, C. Not so many fish in the sea. Curr. Biol. 27, R439–R443 (2017).

    Article  CAS  Google Scholar 

  3. 3.

    Naylor, R. & Burke, M. Aquaculture and ocean resources: Raising tigers of the sea. Annu. Rev. Environ. Resour. 30, 185–218 (2005).

    Article  Google Scholar 

  4. 4.

    Troell, M. et al. Does aquaculture add resilience to the global food system? Proc. Natl Acad. Sci. USA 111, 13257–13263 (2014).

    Article  CAS  Google Scholar 

  5. 5.

    Tacon, A. G. J. & Metian, M. Feed matters: Satisfying the feed demand of aquaculture. Rev. Fish. Sci. Aquac. 23, 1–10 (2015).

    Article  Google Scholar 

  6. 6.

    Naylor, R. L. et al. Feeding aquaculture in an era of finite resources. Proc. Natl Acad. Sci. USA 106, 15103–15110 (2009).

    Article  CAS  Google Scholar 

  7. 7.

    Pikitch, E. K. et al. The global contribution of forage fish to marine fisheries and ecosystems. Fish Fish. 15, 43–64 (2014).

    Article  Google Scholar 

  8. 8.

    Koehn, L. E. et al. Developing a high taxonomic resolution food web model to assess the functional role of forage fish in the California Current ecosystem. Ecol. Model. 335, 87–100 (2016).

    Article  Google Scholar 

  9. 9.

    Alder, J., Campbell, B., Karpouzi, V., Kaschner, K. & Pauly, D. Forage fish: From ecosystems to markets. Annu. Rev. Environ. Resour. 33, 153–166 (2008).

    Article  Google Scholar 

  10. 10.

    Tacon, A. G. J. & Metian, M. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: Trends and future prospects. Aquaculture 285, 146–158 (2008).

    Article  CAS  Google Scholar 

  11. 11.

    Tilman, D. & Clark, M. Global diets link environmental sustainability and human health. Nature 515, 518–522 (2014).

    Article  CAS  Google Scholar 

  12. 12.

    Machovina, B., Feeley, K. J. & Ripple, W. J. Biodiversity conservation: The key is reducing meat consumption. Sci. Total Environ. 536, 419–431 (2015).

    Article  CAS  Google Scholar 

  13. 13.

    Gephart, J. A. et al. The environmental cost of subsistence: Optimizing diets to minimize footprints. Sci. Total Environ. 553, 120–127 (2016).

    Article  CAS  Google Scholar 

  14. 14.

    Springmann, M., Godfray, H. C. J., Rayner, M. & Scarborough, P. Analysis and valuation of the health and climate change cobenefits of dietary change. Proc. Natl Acad. Sci. USA 113, 4146–4151 (2016).

    Article  CAS  Google Scholar 

  15. 15.

    Aleksandrowicz, L., Green, R., Joy, E. J. M., Smith, P. & Haines, A. The impacts of dietary change on greenhouse gas emissions, land use, water use, and health: A systematic review. PloS ONE 11, e0165797 (2016).

    Article  CAS  Google Scholar 

  16. 16.

    Smith, A. D. M. et al. Impacts of fishing low-trophic level species on marine ecosystems. Science 333, 1147–1150 (2011).

    Article  CAS  Google Scholar 

  17. 17.

    Pikitch, E. et al. Little Fish, Big Impact: Managing a Crucial Link in Ocean Food Webs (Lenfest Ocean Program, 2012).

  18. 18.

    Kristofersson, D. & Anderson, J. L. Is there a relationship between fisheries and farming? Interdependence of fisheries, animal production and aquaculture. Mar. Policy 30, 721–725 (2006).

    Article  Google Scholar 

  19. 19.

    Shepherd, C. J. & Jackson, A. J. Global fishmeal and fish-oil supply: Inputs, outputs and markets. J. Fish. Biol. 83, 1046–1066 (2013).

    CAS  Google Scholar 

  20. 20.

    Fish to 2030: Prospects for Fisheries and Aquaculture (World Bank, 2013).

  21. 21.

    Watson, R. A. et al. Marine foods sourced from farther as their use of global ocean primary production increases. Nat. Commun. 6, 7365 (2015).

    Article  CAS  Google Scholar 

  22. 22.

    Merino, G. et al. Can marine fisheries and aquaculture meet fish demand from a growing human population in a changing climate? Glob. Environ. Change 22, 795–806 (2012).

    Article  Google Scholar 

  23. 23.

    Essington, T. E. et al. Fishing amplifies forage fish population collapses. Proc. Natl Acad. Sci. USA 112, 6648–6652 (2015).

    Article  CAS  Google Scholar 

  24. 24.

    Chiu, A. et al. Feed and fishmeal use in the production of carp and tilapia in China. Aquaculture 414, 127–134 (2013).

    Article  Google Scholar 

  25. 25.

    Bimbo, A. P. & Crowther, J. B. Fish meal and oil: Current uses. J. Am. Oil Chem. Soc. 69, 221–227 (1992).

    Article  Google Scholar 

  26. 26.

    Olsen, R. L., Toppe, J. & Karunasagar, I. Challenges and realistic opportunities in the use of by-products from processing of fish and shellfish. Trends Food Sci. Technol. 36, 144–151 (2014).

    Article  CAS  Google Scholar 

  27. 27.

    Sarker, P. K. et al. Towards sustainable aquafeeds: Complete substitution of fish oil with marine microalga Schizochytrium sp. improves growth and fatty acid deposition in juvenile Nile tilapia (Oreochromis niloticus). PloS ONE 11, e0156684 (2016).

    Article  CAS  Google Scholar 

  28. 28.

    Olsen, R. L. & Hasan, M. R. A limited supply of fishmeal: Impact on future increases in global aquaculture production. Trends Food Sci. Technol. 27, 120–128 (2012).

    Article  CAS  Google Scholar 

  29. 29.

    Olson, J., Clay, P. M. & Pinto da Silva, P. Putting the seafood in sustainable food systems. Mar. Policy 43, 104–111 (2014).

    Article  Google Scholar 

  30. 30.

    Cao, L. et al. China’s aquaculture and the world’s wild fisheries. Science 347, 133–135 (2015).

    Article  CAS  Google Scholar 

  31. 31.

    Mo, W. Y., Man, Y. B. & Wong, M. H. Use of food waste, fish waste and food processing waste for China’s aquaculture industry: Needs and challenge. Sci. Total Environ. 613–614, 635–643 (2018).

    Article  CAS  Google Scholar 

  32. 32.

    Waite, R. et al. Improving Productivity and Environmental Performance of Aquaculture (WRI, 2014).

  33. 33.

    Lindegren, M., Checkley, D. M., Rouyer, T., MacCall, A. D. & Stenseth, N. C. Climate, fishing, and fluctuations of sardine and anchovy in the California Current. Proc. Natl Acad. Sci. USA 110, 13672–13677 (2013).

    Article  Google Scholar 

  34. 34.

    Tacon, A. G. J. & Metian, M. Fish matters: Importance of aquatic foods in human nutrition and global food supply. Rev. Fish. Sci. 21, 22–38 (2013).

    Article  CAS  Google Scholar 

  35. 35.

    Plagányi, É. E. & Essington, T. E. When the SURFs up, forage fish are key. Fish. Res. 159, 68–74 (2014).

    Article  Google Scholar 

  36. 36.

    Cury, P. M. et al. Global seabird response to forage fish depletion—One-third for the birds. Science 334, 1703–1706 (2011).

    Article  CAS  Google Scholar 

  37. 37.

    Szuwalski, C. S., Burgess, M. G., Costello, C. & Gaines, S. D. High fishery catches through trophic cascades in China. Proc. Natl Acad. Sci. USA 114, 717–721 (2017).

    Article  CAS  Google Scholar 

  38. 38.

    Checkley, D., Alheit, J., Oozeki, Y. & Roy, C. Climate Change and Small Pelagic Fish (Cambridge Univ. Press, Cambridge, 2009).

  39. 39.

    Barange, M. et al. Impacts of climate change on marine ecosystem production in societies dependent on fisheries. Nat. Clim. Change 4, 211–216 (2014).

    Article  Google Scholar 

  40. 40.

    Cheung, W. W. L., Watson, R. & Pauly, D. Signature of ocean warming in global fisheries catch. Nature 497, 365–368 (2013).

    Article  CAS  Google Scholar 

  41. 41.

    Laufkötter, C. et al. Drivers and uncertainties of future global marine primary production in marine ecosystem models. Biogeosciences 12, 6955–6984 (2015).

    Article  Google Scholar 

  42. 42.

    Tacon, A. & Metian, M. G. J. T. M. Fishing for feed or fishing for food: Increasing global competition for small pelagic forage fish. AMBIO 38, 294–302 (2009).

    Article  Google Scholar 

  43. 43.

    Cashion, T., Le Manach, F., Zeller, D. & Pauly, D. Most fish destined for fishmeal production are food-grade fish. Fish Fish. 8, 837–844 (2017).

    Article  Google Scholar 

  44. 44.

    Isaacs, M. The humble sardine (small pelagics): Fish as food or fodder. Agric. Food Secur. 5, 27 (2016).

    Article  Google Scholar 

  45. 45.

    Olsen, Y. Resources for fish feed in future mariculture. Aquac. Environ. Interact. 1, 187–200 (2011).

    Article  Google Scholar 

  46. 46.

    Froese, R. & Pauly, D. (eds) FishBase (2018); www.fishbase.org.

  47. 47.

    Martell, S. & Froese, R. A simple method for estimating MSY from catch and resilience. Fish Fish. 14, 504–514 (2013).

    Article  Google Scholar 

  48. 48.

    Tolkamp, B., Wall, E., Roehe, R., Newbold, J. & Zaralis, K. Review of Nutrient Efficiency in Different Breeds of Farm Livestock (UK Department for Environment, Food and Rural Affairs, 2010).

  49. 49.

    Wilkinson, J. M. Re-defining efficiency of feed use by livestock. Animal 5, 1014–1022 (2011).

    Article  CAS  Google Scholar 

  50. 50.

    The State of Food and Agriculture 2016: Climate Change, Agriculture, and Food Security (FAO, 2016).

  51. 51.

    FAOSTAT Database Collections (FAO, 2013).

  52. 52.

    Alexandratos, N. & Bruinsma, J. World Agriculture Towards 2030/2050: The 2012 Revision (ESA Rome, FAO, 2012).

  53. 53.

    Hunter, M. C., Smith, R. G., Schipanski, M. E., Atwood, L. W. & Mortensen, D. A. Agriculture in 2050: Recalibrating targets for sustainable intensification. BioScience 67, 386–391 (2017).

    Article  Google Scholar 

  54. 54.

    RCoreTeam R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  55. 55.

    Index Mundi (International Fish Meal and Fish Oil Organization, 2017).

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Acknowledgements

This research and H.E.F. were supported by the Science for Nature and People Partnership, a partnership of The Nature Conservancy, the Wildlife Conservation Society and the National Center for Ecological Analysis and Synthesis (SNP015). N.S.J. was supported by VILLUM FONDEN (grant VKR023371). T.C. acknowledges support by the Waitt Foundation.

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H.E.F. conceived the initial study. H.E.F., N.S.J. and T.E.E. developed the research and methodology with critical input and insight from T.C. and B.S.H. H.E.F. and N.S.J. collected and analysed the data. All authors interpreted the results and implications. H.E.F. and N.S.J. made the figures. H.E.F. drafted the manuscript with significant input and revisions from all authors.

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Correspondence to Halley E. Froehlich.

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Supplementary Methods, Supplementary Tables 1,2, Supplementary Figs 1–4, Supplementary References 1–8

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Froehlich, H.E., Jacobsen, N.S., Essington, T.E. et al. Avoiding the ecological limits of forage fish for fed aquaculture. Nat Sustain 1, 298–303 (2018). https://doi.org/10.1038/s41893-018-0077-1

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