Skip to main content

Thank you for visiting 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.

Food web changes under ocean acidification promote herring larvae survival


Ocean acidification—the decrease in seawater pH due to rising CO2 concentrations—has been shown to lower survival in early life stages of fish and, as a consequence, the recruitment of populations including commercially important species. To date, ocean-acidification studies with fish larvae have focused on the direct physiological impacts of elevated CO2, but largely ignored the potential effects of ocean acidification on food web interactions. In an in situ mesocosm study on Atlantic herring (Clupea harengus) larvae as top predators in a pelagic food web, we account for indirect CO2 effects on larval survival mediated by changes in food availability. The community was exposed to projected end-of-the-century CO2 conditions (~760 µatm pCO2) over a period of 113 days. In contrast with laboratory studies that reported a decrease in fish survival, the survival of the herring larvae in situ was significantly enhanced by 19 ± 2%. Analysis of the plankton community dynamics suggested that the herring larvae benefitted from a CO2-stimulated increase in primary production. Such indirect effects may counteract the possible direct negative effects of ocean acidification on the survival of fish early life stages. These findings emphasize the need to assess the food web effects of ocean acidification on fish larvae before we can predict even the sign of change in fish recruitment in a high-CO2 ocean.

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

Access options

Rent or buy this article

Prices vary by article type



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

Fig. 1: Chronology of major events during the experiment.
Fig. 2: Development over time in ambient and high CO2 treatments.
Fig. 3: Relationship between larval survival and the abundance of food items in the ten mesocosms.

Similar content being viewed by others


  1. Haigh, R., Ianson, D., Holt, C. A., Neate, H. E. & Edwards, A. M. Effects of ocean acidification on temperate coastal marine ecosystems and fisheries in the northeast Pacific. PLoS ONE 10, e0117533 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Houde, E. D. Emerging from Hjort’s shadow. J. Northwest Atl. Fish. Sci. 41, 53–70 (2008).

    Article  Google Scholar 

  3. Baumann, H., Talmage, S. C. & Gobler, C. J. Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nat. Clim. Change 2, 38–41 (2011).

    Article  Google Scholar 

  4. Munday, P. L. et al. Effects of elevated CO2 on early life history development of the yellowtail kingfish. ICES J. Mar. Sci. 73, 641–649 (2015).

    Article  Google Scholar 

  5. Stiasny, M. H. et al. Ocean acidification effects on Atlantic cod larval survival and recruitment to the fished population. PLoS ONE 11, e0155448 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Nagelkerken, I., Russell, B. D., Gillanders, B. M. & Connell, S. D. Ocean acidification alters fish populations indirectly through habitat modification. Nat. Clim. Change 6, 89–95 (2015).

    Article  Google Scholar 

  7. Goldenberg, S. U., Nagelkerken, I., Ferreira, C. M., Ullah, H. & Connell, S. D. Boosted food web productivity through ocean acidification collapses under warming. Glob. Change Biol. 23, 4177–4184 (2017).

  8. Schulz, K. G. et al. Phytoplankton blooms at increasing levels of atmospheric carbon dioxide: experimental evidence for negative effects on prymnesiophytes and positive on small picoeukaryotes. Front. Mar. Sci. 4, 64 (2017).

    Article  Google Scholar 

  9. Nagelkerken, I. & Connell, S. D. Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions. Proc. Natl Acad. Sci. USA 112, 13272–13277 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bach, L. T. T. et al. Influence of ocean acidification on a natural winter-to-summer plankton succession: first insights from a long-term mesocosm study draw attention to periods of low nutrient concentrations. PLoS ONE 11, e0159068 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  11. IPCC: Summary for Policymakers. In Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, Cambridge, 2013).

  12. Sswat, M., Boxhammer, T., Jutfelt, F., Clemmesen, C. & Riebesell, U. Performance of Herring Larvae in a Simulated Future Ocean Food Web, Using the ‘Kiel Off-Shore Mesocosms for Future Ocean Simulations’ (GEOMAR, 2016);

  13. Algueró-Muñiz, M. et al. KOSMOS 2013 Gullmar Fjord Long-Term Mesocosm Study: Mesozooplankton Abundance (PANGAEA, 2017);

  14. Paulsen, M. et al. Nutritional situation for larval Atlantic herring (Clupea harengus L.) in two nursery areas in the western Baltic Sea. ICES J. Mar. Sci. 71, 991–1000 (2013).

    Article  Google Scholar 

  15. Cushing, D. H. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol. 26, 249–293 (1990).

    Article  Google Scholar 

  16. Harrell, F. E. Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis 465–507 (Springer, New York, 2001).

  17. Franke, A. & Clemmesen, C. Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.). Biogeosciences 8, 3697–3707 (2011).

    Article  CAS  Google Scholar 

  18. Frommel, A. Y. et al. Organ damage in Atlantic herring larvae as a result of ocean acidification. Ecol. Appl. 24, 1131–1143 (2014).

    Article  PubMed  Google Scholar 

  19. Maneja, R. et al. The swimming kinematics and foraging behavior of larval Atlantic herring, Clupea harengus L., are resilient to elevated pCO2. J. Exp. Mar. Biol. Ecol. 466, 42–48 (2015).

    Article  Google Scholar 

  20. Maneja, R. H. et al. The proteome of Atlantic herring (Clupea harengus L.) larvae is resistant to elevated pCO2. Mar. Pollut. Bull. 86, 154–160 (2014).

    Article  CAS  PubMed  Google Scholar 

  21. Sswat, M., Stiasny, M. H., Jutfelt, F., Riebesell, U. & Clemmesen, C. Growth performance and survival of larval Atlantic herring, under the combined effects of elevated temperatures and CO2. PLoS ONE 13, e0191947 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Eberlein, T. et al. Effects of ocean acidification on primary production in a coastal North Sea phytoplankton community. PLoS ONE 12, e0172594 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Algueró-Muñiz, M. et al. Ocean acidification effects on mesozooplankton community development: results from a long-term mesocosm experiment. PLoS ONE 12, e0175851 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Taucher, J. et al. Influence of ocean acidification on plankton community structure during a winter-to-summer succession: an imaging approach indicates that copepods can benefit from elevated CO2 via indirect food web effects. PLoS ONE 12, e0169737 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Denis, J. et al. Feeding strategy of Downs herring larvae (Clupea harengus L.) in the English Channel and North Sea. J. Sea Res. 115, 33–46 (2016).

    Article  Google Scholar 

  26. Horn, H. G. et al. Low CO2 sensitivity of microzooplankton communities in the Gullmar Fjord, Skagerrak: evidence from a long-term mesocosm study. PLoS ONE 11, e0165800 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Rossoll, D. et al. Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7, e34737 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Checkley, D. M. Selective feeding by Atlantic herring (Clupea harengus) larvae on zooplankton in natural assemblages. Mar. Ecol. Prog. Ser. 9, 245–253 (1982).

    Article  Google Scholar 

  29. Thomsen, J., Casties, I., Pansch, C., Körtzinger, A. & Melzner, F. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Glob. Change Biol. 19, 1017–1027 (2013).

    Article  Google Scholar 

  30. Bach, L. T., Alvarez-Fernandez, S., Hornick, T., Stuhr, A. & Riebesell, U. Simulated ocean acidification reveals winners and losers in coastal phytoplankton. PLoS ONE 12, e0188198 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Frommel, A. Y. et al. Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nat. Clim. Change 2, 42–46 (2011).

    Article  Google Scholar 

  32. Pimentel, M. S. et al. Defective skeletogenesis and oversized otoliths in fish early stages in a changing ocean. J. Exp. Biol. 217, 2062–2070 (2014).

    Article  PubMed  Google Scholar 

  33. Bignami, S., Enochs, I. C., Manzello, D. P., Sponaugle, S. & Cowen, R. K. Ocean acidification alters the otoliths of a pantropical fish species with implications for sensory function. Proc. Natl Acad. Sci. USA 110, 7366–7370 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Nagelkerken, I. et al Species interactions drive fish biodiversity loss in a high-CO2 world. Curr. Biol. 27, 2177–2184.e4 (2017).

    Article  CAS  PubMed  Google Scholar 

  35. Riebesell, U. et al. Technical note: a mobile sea-going mesocosm system—new opportunities for ocean change research. Biogeosciences 2, 1835–1847 (2013).

    Article  Google Scholar 

  36. Boxhammer, T., Bach, L. T., Czerny, J. & Riebesell, U. Technical note: sampling and processing of mesocosm sediment trap material for quantitative biogeochemical analysis. Biogeosciences 13, 2849–2858 (2016).

    Article  Google Scholar 

  37. Purcell, J. E. & Grover, J. J. Predation and food limitation as causes of mortality in larval herring at a spawning ground in British Columbia. Mar. Ecol. Prog. Ser. 59, 55–61 (1990).

    Article  Google Scholar 

  38. Gorsky, G. et al. Digital zooplankton image analysis using the ZooScan integrated system. J. Plankton Res. 32, 285–303 (2010).

    Article  Google Scholar 

  39. Hufnagl, M. & Peck, M. A. Physiological individual-based modelling of larval Atlantic herring (Clupea harengus) foraging and growth: insights on climate-driven life-history scheduling. ICES J. Mar. Sci. 68, 1170–1188 (2011).

    Article  Google Scholar 

Download references


We thank the Sven Lovén Centre for Marine Sciences, Kristineberg for providing the facilities to conduct this experiment. We acknowledge Yngve Elling Nicolaisen and the Marine Biological Station Drøbak for help obtaining the fish. We are grateful to the members of the ‘KOSMOS team’ for their enduring efforts to conduct this experiment. We are also thankful for the support of F. Dahlke and D. Storch, who provided us with the specifically designed ‘egg cages’. We thank the captain and crew of RV ALKOR for help with transporting and setting up the mesocosms (cruises AL406 and AL420). We acknowledge R. Erven, S. Schorr and D. Unverricht for designing the illustrations. The study was jointly funded by the Association of European Marine Biological Laboratories (; ASSEMBLE grant number 227799 to C.C. and M.S.), Swedish Academy of Sciences (to M.A.-M.) and German Federal Ministry of Education and Research (FKZ 03F06550) in the framework of BIOACID II (, and by the Leibniz Prize 2012 of the German Research Foundation (awarded to U.R.).

Author information

Authors and Affiliations



M.S., U.R. and C.C. designed the experiment. M.S., M.H.S., F.J., L.T.B., M.A.-M., U.R. and C.C. performed the experiment. M.S. performed the survival analysis. M.A.-M. performed the zooplankton analysis. J.T. performed the particle analysis. L.T.B. performed the chlorophyll a analysis. M.S. and C.C. analysed the data. M.S., C.C. and U.R. wrote the paper. All authors discussed the results and implications, and commented on the manuscript at all stages.

Corresponding author

Correspondence to Catriona Clemmesen.

Ethics declarations

Competing interests

The authors declare no competing interests.

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 Figures 1–2; Supplementary Table 1

Life Sciences Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sswat, M., Stiasny, M.H., Taucher, J. et al. Food web changes under ocean acidification promote herring larvae survival. Nat Ecol Evol 2, 836–840 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


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