Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Increasing CO2 threatens human nutrition

An Author Correction to this article was published on 01 October 2019

Abstract

Dietary deficiencies of zinc and iron are a substantial global public health problem. An estimated two billion people suffer these deficiencies1, causing a loss of 63 million life-years annually2,3. Most of these people depend on C3 grains and legumes as their primary dietary source of zinc and iron. Here we report that C3 grains and legumes have lower concentrations of zinc and iron when grown under field conditions at the elevated atmospheric CO2 concentration predicted for the middle of this century. C3 crops other than legumes also have lower concentrations of protein, whereas C4 crops seem to be less affected. Differences between cultivars of a single crop suggest that breeding for decreased sensitivity to atmospheric CO2 concentration could partly address these new challenges to global health.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Percentage change in nutrients at elevated [CO2] relative to ambient [CO2].
Figure 2: Percentage change (with 95% confidence intervals) in nutrients at elevated [CO2] relative to ambient [CO2], by cultivar.

References

  1. Tulchinsky, T. H. Micronutrient deficiency conditions: global health issues. Public Health Rev. 32, 243–255 (2010)

    Article  Google Scholar 

  2. Caulfield, L. E. & Black, R. E. in Comparative Quantification of Health Risks: Global and Regional Burden of Disease Attribution to Selected Major Risk Factors (eds Ezzati, M., Lopez, A. D., Rodgers, A. & Murray, C. J. L. ) Vol. 1, Ch. 5 (World Health Organization, 2004)

    Google Scholar 

  3. Stoltzfus, R. J., Mullany, L. & Black, R. E. in Comparative Quantification of Health Risks: Global and Regional Burden of Disease Attribution to Selected Major Risk Factors (eds Ezzati, M., Lopez, A. D., Rodgers, A. & Murray, C. J. L. ) Vol. 1, Ch. 3 (World Health Organization, 2004)

    Google Scholar 

  4. De la Puente, L. S., Pérez, P. P., Martinez-Carrasco, R., Morcuende, R. M. & Del Molino, I. M. M. Action of elevated CO2 and high temperatures on the mineral chemical composition of two varieties of wheat. Agrochimica 44, 221–230 (2000)

    CAS  Google Scholar 

  5. Manderscheid, R., Bender, J., Jäger, H. J. & Weigel, H. J. Effects of season long CO2 enrichment on cereals. II. Nutrient concentrations and grain quality. Agric. Ecosyst. Environ. 54, 175–185 (1995)

    Article  CAS  Google Scholar 

  6. Fangmeier, A., Grüters, U., Högy, P., Vermehren, B. & Jäger, H.-J. Effects of elevated CO2, nitrogen supply and tropospheric ozone on spring wheat. II. Nutrients (N, P, K, S, Ca, Mg, Fe, Mn, Zn). Environ. Pollut. 96, 43–59 (1997)

    Article  CAS  Google Scholar 

  7. Pleijel, H. et al. Effects of elevated carbon dioxide, ozone and water availability on spring wheat growth and yield. Physiol. Plant. 108, 61–70 (2000)

    Article  CAS  Google Scholar 

  8. Seneweera, S. P. & Conroy, J. P. Growth, grain yield and quality of rice (Oryza sativa L.) in response to elevated CO2 and phosphorus nutrition. Soil Sci. Plant Nutr. 43, 1131–1136 (1997)

    Article  CAS  Google Scholar 

  9. Lieffering, M., Kim, H.-Y., Kobayashi, K. & Okada, M. The impact of elevated CO2 on the elemental concentrations of field-grown rice grains. Field Crops Res. 88, 279–286 (2004)

    Article  Google Scholar 

  10. Prior, S. A., Runion, G. B., Rogers, H. H. & Torbert, H. A. Effects of atmospheric CO2 enrichment on crop nutrient dynamics under no-till conditions. J. Plant Nutr. 31, 758–773 (2008)

    Article  CAS  Google Scholar 

  11. Högy, P. & Fangmeier, A. Atmospheric CO2 enrichment affects potatoes. 2. Tuber quality traits. Eur. J. Agron. 30, 85–94 (2009)

    Article  Google Scholar 

  12. Högy, P. et al. Effects of elevated CO2 on grain yield and quality of wheat: results from a 3-year free-air CO2 enrichment experiment. Plant Biol. 11, 60–69 (2009)

    Article  Google Scholar 

  13. Erbs, M. et al. Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation. Agric. Ecosyst. Environ. 136, 59–68 (2010)

    Article  CAS  Google Scholar 

  14. Ainsworth, E. A. & Long, S. P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2 . New Phytol. 165, 351–372 (2005)

    Article  Google Scholar 

  15. Curtis, P. S. & Wang, X. A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113, 299–313 (1998)

    Article  ADS  Google Scholar 

  16. Duval, B. D., Blankinship, J. C., Dijkstra, P. & Hungate, B. A. CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis. Plant Ecol. 213, 505–521 (2012)

    Article  Google Scholar 

  17. Miller, L. V., Krebs, N. F. & Hambidge, M. K. A mathematical model of zinc absorption in humans as a function of dietary zinc and phytate. J. Nutr. 137, 135–141 (2007)

    Article  CAS  Google Scholar 

  18. Fisher, B. S. et al. in Climate Change 2007: Mitigation. Contribution of Working Group III to the Fourth Assessment Report of the Inter-governmental Panel on Climate Change (eds Metz, B. et al.) 169–250 (Cambridge Univ. Press, 2007)

  19. Appel, L. J. et al. Effects of protein, monounsaturated fat, and carbohydrate intake on blood pressure and serum lipids: results of the OmniHeart randomized trial. J. Am. Med. Assoc. 294, 2455–2464 (2005)

    Article  CAS  Google Scholar 

  20. Millward, D. Joe. Identifying recommended dietary allowances for protein and amino acids: a critique of the 2007 WHO/FAO/UNU report. Br. J. Nutr. 108, S3–S21 (2012)

    Article  CAS  Google Scholar 

  21. Swaminathan, S., Vaz, M. & Kurpad, A. V. Protein intakes in India. Br. J. Nutr. 108, S50–S58 (2012)

    Article  CAS  Google Scholar 

  22. Leakey, A. Rising atmospheric carbon dioxide concentration and the future of C4 crops for food and fuel. Proc. R. Soc. Lond. B 276, 2333–2343 (2009)

    Article  CAS  Google Scholar 

  23. Rogers, A., Ainsworth, E. A. & Leakey, A. D. Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol. 151, 1009–1016 (2009)

    Article  CAS  Google Scholar 

  24. Bloom, A. J. et al. CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93, 355–367 (2012)

    Article  Google Scholar 

  25. Leakey, A. D. et al. Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60, 2859–2876 (2009)

    Article  CAS  Google Scholar 

  26. Gifford, R., Barrett, D. & Lutze, J. The effects of elevated [CO2] on the C:N and C:P mass ratios of plant tissues. Plant Soil 224, 1–14, 10.1023/A:1004790612630. (2000)

    Article  CAS  Google Scholar 

  27. McGrath, J. M. & Lobell, D. B. Reduction of transpiration and altered nutrient allocation contribute to nutrient decline of crops grown in elevated CO2 concentrations. Plant Cell Environ. 36, 697–705, 10.1111/pce.12007. (2013)

    Article  CAS  Google Scholar 

  28. Monasterio, I. & Graham, R. D. Breeding for trace minerals in wheat. Food Nutr. Bull. 21, 392–396 (2000)

    Article  Google Scholar 

  29. Searle, S. R., Casella, G. & McCulloch, C. E. Variance Components (Wiley, 1992)

    Book  Google Scholar 

  30. Schenker, N. & Gentleman, J. F. On judging the significance of differences by examining the overlap between confidence intervals. Am. Stat. 55, 182–186 (2001)

    Article  MathSciNet  Google Scholar 

  31. Hasegawa, T. A. et al. Rice cultivar responses to elevated CO2 at two free-air CO2 enrichment (FACE) sites in Japan. Funct. Plant Biol. 40, 148–159 (2013)

    Article  CAS  Google Scholar 

  32. Mollah, M., Norton, R. & Huzzey, J. Australian Grains Free Air Carbon dioxide Enrichment (AGFACE) facility: design and performance. Crop Pasture Sci. 60, 697–707 (2009)

    Article  CAS  Google Scholar 

  33. Markelz, R., Strellner, R. & Leakey, A. Impairment of C4 photosynthesis by drought is exacerbated by limiting nitrogen and ameliorated by elevated CO2 in maize. J. Exp. Bot. 62, 3235–3246 (2011)

    Article  CAS  Google Scholar 

  34. Gillespie, K. et al. Greater antioxidant and respiratory metabolism in field-grown soybean exposed to elevated O3 under both ambient and elevated CO2 . Plant Cell Environ. 35, 169–184 (2012)

    Article  CAS  Google Scholar 

  35. Ottman, M. J. et al. Elevated CO2 increases sorghum biomass under drought conditions. New Phytol. 150, 261–273 (2001)

    Article  Google Scholar 

  36. Sah, R. N. & Miller, R. O. Spontaneous reaction for acid dissolution of biological tissues in closed vessels. Anal. Chem. 64, 230–233 (1992)

    Article  CAS  Google Scholar 

  37. AOAC. Official Method 972.43. in Official Methods of Analysis of AOAC International, 18th edition, Revision 1, 2006 Ch. 12 5–6 (AOAC International, 2006)

  38. Mosse, J. Nitrogen to protein conversion factor for ten cereals and six legumes or oilseeds. A reappraisal of its definition and determination. Variation according to species and to seed protein content. J. Agric. Food Chem. 38, 18–24 (1990)

    Article  CAS  Google Scholar 

  39. Haug, W. & Lantzsch, H. J. Sensitive method for the rapid determination of phytate in cereals and cereal products. J. Sci. Food Agric. 34, 1423–1426 (1983)

    Article  CAS  Google Scholar 

  40. Raboy, V. et al. Origin and seed phenotype of maize low phytic acid 1-1 and low phytic acid 2-1. Plant Physiol. 124, 355–368 (2000)

    Article  CAS  Google Scholar 

  41. Wuehler, S. E., Peerson, J. M. & Brown, K. H. Use of national food balance data to estimate the adequacy of zinc in national food supplies: methodology and regional estimates. Public Health Nutr. 8, 812–819 (2005)

    Article  Google Scholar 

Download references

Acknowledgements

We thank L. S. De la Puente, M. Erbs, A. Fangmeier, P. Högy, M. Lieffering, R. Manderscheid, H. Pleijel and S. Prior for sharing data from their groups with us; H. Nakamura, T. Tokida, C. Zhu and S. Yoshinaga for contributions to the rice FACE project; and M. Hambidge, W. Willett, D. Schrag, K. Brown, R. Wessells, N. Fernando, J. Peerson and B. Kimball for reviews of earlier drafts or conceptual contributions to this project. V.R. thanks A. L. Harvey for her efforts in producing the phytate data included here. The National Agriculture and Food Research Organization (Japan) provided the grain samples of some rice cultivars. We thank the following for financial support of this work: the Bill & Melinda Gates Foundation; the Winslow Foundation; the Commonwealth Department of Agriculture (Australia), the International Plant Nutrition Institute, (Australia), the Grains Research and Development Corporation (Australia), the Ministry of Agriculture, Forestry and Fisheries (Japan); the National Science Foundation (NSF IOS-08-18435); USDA NIFA 2008-35100-044459; research at SoyFACE was supported by the US Department of Agriculture Agricultural Research Service; Illinois Council for Food and Agricultural Research (CFAR); Department of Energy’s Office of Science (BER) Midwestern Regional Center of the National Institute for Climatic Change Research at Michigan Technological University, under Award Number DEFC02- 06ER64158; and the National Research Initiative of Agriculture and Food Research Initiative Competitive Grants Program Grant no. 2010–65114–20343 from the USDA National Institute of Food and Agriculture. Early stages of this work received support from Harvard Catalyst | The Harvard Clinical and Translational Science Center (National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health Award 8UL1TR000170-05).

Author information

Authors and Affiliations

Authors

Contributions

S.S.M. conceived the overall project and drafted the manuscript. A.Z., I.K., J.S. and P.H. performed statistical analyses. P.H. and A.D.B.L. provided substantial input into methods descriptions. A.J.B., E.C. and V.R. analysed grain samples for nutrient content. G.F., T.H., A.D.B.L., R.L.N., M.J.O., H.S., S.S., M.T. and Y.U. conducted FACE experiments and supplied grain for analysis. N.M.H. and P.H. assisted with elements of experimental design. K.A.S. and L.H.D. assisted with data collection and analysis. All authors contributed to manuscript preparation.

Corresponding author

Correspondence to Samuel S. Myers.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Table 1 Percentage change in nutrient content at elevated [CO2] relative to ambient [CO2]
Extended Data Table 2 Original data combined with previously published FACE data from studies 3, 4, 6 and 7
Extended Data Table 3 Original data combined with previously published FACE and chamber data from studies 1–10
Extended Data Table 4 Percentage change in nutrient content at elevated [CO2] compared with ambient [CO2] for all nutrients
Extended Data Table 5 Countries whose populations receive at least 60% of dietary iron and/or zinc from C3 grains and legumes
Extended Data Table 6 Literature reporting nutrient changes in the edible portion of crops grown at elevated and ambient [CO2]

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Myers, S., Zanobetti, A., Kloog, I. et al. Increasing CO2 threatens human nutrition. Nature 510, 139–142 (2014). https://doi.org/10.1038/nature13179

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature13179

This article is cited by

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing