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Toxic algal bloom induced by ocean acidification disrupts the pelagic food web

Abstract

Ocean acidification, the change in seawater carbonate chemistry due to the uptake of anthropogenic CO2, affects the physiology of marine organisms in multiple ways1. Diverse competitive and trophic interactions transform the metabolic responses to changes in community composition, seasonal succession and potentially geographical distribution of species. The health of ocean ecosystems depends on whether basic biotic functions are maintained, ecosystem engineers and keystone species are retained, and the spread of nuisance species is avoided2. Here, we show in a field experiment that the toxic microalga Vicicitus globosus has a selective advantage under ocean acidification, increasing its abundance in natural plankton communities at CO2 levels higher than 600 µatm and developing blooms above 800 µatm CO2. The mass development of V. globosus has had a dramatic impact on the plankton community, preventing the development of the micro- and mesozooplankton communities, thereby disrupting trophic transfer of primary produced organic matter. This has prolonged the residence of particulate matter in the water column and caused a strong decline in export flux. Considering its wide geographical distribution and confirmed role in fish kills3, the proliferation of V. globosus under the IPCC4 CO2 emission representative concentration pathway (RCP4.5 to RCP8.5) scenarios may pose an emergent threat to coastal communities, aquaculture and fisheries.

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Data availability

The data of this mesocosm study are archived in the World Data Centre MARE/PANGAEA and can be downloaded using the following link: https://www.pangaea.de/?q=campaign%3A%22KOSMOS_2014%22.

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References

  1. 1.

    Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19, 1884–1896 (2013).

  2. 2.

    Hall-Spencer, J. M. & Allen, R. The impact of CO2 emissions on ‘nuisance’ marine species. Res. Rep. Biodivers. Stud. 4, 33–46 (2015).

  3. 3.

    Chang, F. H. Cytotoxic effects of Vicicitus globosus (Class Dictyochophyceae) and Chattonella marina (Class Raphidophyceae) on rotifers and other microalgae. J. Mar. Sci. Eng. 3, 401–411 (2015).

  4. 4.

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

  5. 5.

    Le Quéré, C. et al. Global Carbon Budget 2016. Earth Syst. Sci. Data 8, 605–649 (2016).

  6. 6.

    Beardall, J. & Raven, J. A. The potential effects of global climate change on microbial photosynthesis, growth and ecology. Phycologia 43, 26–40 (2004).

  7. 7.

    Giordano, M., Beardall, J. & Raven, J. A . CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56, 99–131 (2005).

  8. 8.

    Riebesellsbe, U. & Tortell, P. D. in Ocean Acidification (eds Gattuso, J. P. & Hansson, L.) 99–121 (Oxford Univ. Press, New York, 2013).

  9. 9.

    Riebesell, U. et al. Competitive fitness of a predominant pelagic calcifier impaired by ocean acidification. Nat. Geosci. 10, 19–23 (2017).

  10. 10.

    Wells, M. L. et al. Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49, 68–93 (2015).

  11. 11.

    Sala, M. M. et al. Contrasting effects of ocean acidification on the microbial food web under different trophic conditions. ICES J. Mar. Sci. 73, 670–679 (2016).

  12. 12.

    Bach, L. 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).

  13. 13.

    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).

  14. 14.

    Taucher, J. et al. Influence of ocean acidification and deep water upwelling on oligotrophic plankton communities in the subtropical North Atlantic: insights from an in situ mesocosm study. Front. Mar. Sci. 4, 85 (2017).

  15. 15.

    Arístegui, J. et al. The influence of island-generated eddies on chlorophyll distribution: a study of mesoscale variation around Gran Canaria. Deep Sea Res. Pt I 44, 71–96 (1997).

  16. 16.

    Pelegrí, J. L. et al. Coupling between the open ocean and the coastal upwelling region off northwest Africa: water recirculation and offshore pumping of organic matter. J. Mar. Syst. 54, 3–37 (2005).

  17. 17.

    Chang, F. H., McVeagh, M., Gall, M. & Smith, P. Chattonella globosa is a member of Dictyochophyceae: reassignment to Vicicitus gen. nov., based on molecular phylogeny, pigment composition, morphology and life history. Phycologia 51, 403–420 (2012).

  18. 18.

    Algueró-Muñiz, M. et al. Impacts of ocean acidification on the development of a subtropical zooplankton community during oligotrophic conditions and simulated upwelling. Front. Mar. Sci. (in the press).

  19. 19.

    Tatters, A. O., Fu, F. X. & Hutchins, D. A. High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS ONE 7, e32116 (2012).

  20. 20.

    Tatters, A. O., Flewelling, L. J., Fu, F., Granholm, A. A. & Hutchins, D. A. High CO2 promotes the production of paralytic shellfish poisoning toxins by Alexandrium catenella from Southern California waters. Harmful Algae 30, 37–43 (2013).

  21. 21.

    Danovaro, R. et al. Marine viruses and global climate change. FEMS Microbiol. Rev. 35, 993–1034 (2011).

  22. 22.

    Bidle, K. D. Programmed cell death in unicellular phytoplankton. Curr. Biol. 26, R594–R607 (2016).

  23. 23.

    Eberlein, T., Van den Waal, D. B. & Rost, B. Differential effects of ocean acidification on carbon acquisition in two bloom-forming dinoflagellate species. Physiol. Plant. 151, 468–479 (2014).

  24. 24.

    Rost, B., Richter, K. U., Riebesell, U. & Hansen, P. J. Inorganic carbon acquisition in red tide dinoflagellates. Plant Cell Environ. 29, 810–822 (2006).

  25. 25.

    Bach, L. T., Alvarez-FernandezS., HornickT., StuhrA. & Riebesell, U. Simulated ocean acidification reveals winners and losers in coastal phytoplankton. PLoS ONE 12, e0188198 (2017).

  26. 26.

    Stange, P. et al. Ocean acidification-induced restructuring of the plankton food web can influence the degradation of sinking particles. Front. Mar. Sci. 5, 140 (2018).

  27. 27.

    Zark, M. et al. Ocean acidification experiments in large-scale mesocosms reveal similar dynamics of dissolved organic matter production and biotransformation. Front. Mar. Sci. 4, 271 (2017).

  28. 28.

    Zingone, A. & Oksfeldt Enevoldsen, H. The diversity of harmful algal blooms: a challenge for science and management. Ocean Coast. Manag. 43, 725–748 (2000).

  29. 29.

    Glibert, P. M. et al. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model analysis. Glob. Change Biol. 20, 3845–3858 (2014).

  30. 30.

    Hiroshi, S., Okada, H., Imai, I. & Yoshida, T. High toxicity of the novel bloom-forming species Chattonella ovata (Raphidophyceae) to cultured fish. Harmful Algae 4, 783–787 (2005).

  31. 31.

    Imai, I. & Itoh, K. Annual life cycle of Chattonella spp., causative flagellates of noxious red tides in the Inland Sea of Japan. Mar. Biol. 94, 287–292 (1987).

  32. 32.

    Hallegraeff, G. M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 46, 220–235 (2010).

  33. 33.

    Sathyendranath, S. et al. Carbon-to-chlorophyll ratio and growth rate of phytoplankton in the sea. Mar. Ecol. Prog. Ser. 383, 73–84 (2009).

  34. 34.

    Putt, M. & Stoecker, D. K. An experimentally determined carbon:volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol. Oceanogr. 34, 1097–1103 (1989).

  35. 35.

    Lehette, P. & Hernández‐León, S. Zooplankton biomass estimation from digitized images: a comparison between subtropical and Antarctic organisms. Limnol. Oceanogr. Methods 7, 304–308 (2009).

  36. 36.

    Kiørboe, T. Zooplankton body composition. Limnol. Oceanogr. 58, 1843–1850 (2013).

  37. 37.

    Arístegui, J., Hernández-León, S., Montero, M. F. & Gómez, M. The seasonal planktonic cycle in coastal waters of the Canary Islands. Sci. Mar. 65, 51–58 (2001).

  38. 38.

    Riebesell, U. et al. Technical note: a mobile sea-going mesocosm system—new opportunities for ocean change research. Biogeosciences 10, 1835–1847 (2013).

  39. 39.

    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).

  40. 40.

    Sharp, J. H. Improved analysis for “particulate” organic carbon and nitrogen from seawater. Limnol. Oceanogr. 19, 984–989 (1974).

  41. 41.

    Barlow, R. G., Cummings, D. G. & Gibb, S. W. Improved resolution of mono- and divinyl chlorophylls a and b and zeaxanthin and lutein in phytoplankton extracts using reverse phase C-8 HPLC. Mar. Ecol. Prog. Ser. 161, 303–307 (1997).

  42. 42.

    Mackey, M. D., Mackey, D. J., Higgins, H. W. & Wright, S. W. CHEMTAX: a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar. Ecol. Prog. Ser. 144, 265–283 (1996).

  43. 43.

    Schunck, H. et al. Giant hydrogen sulfide plume in the oxygen minimum zone off Peru supports chemolithoautotrophy. PLoS ONE 8, e68661 (2013).

  44. 44.

    Nurk S. et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In Proc. RECOMB 2013: Research in Computational Molecular Biology (eds Deng, M. et al.) 158–170 (Springer, 2013).

  45. 45.

    Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31, 3350–3352 (2015).

  46. 46.

    Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987).

  47. 47.

    Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

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Acknowledgements

We thank the Oceanic Platform of the Canary Islands (Plataforma Oceánica de Canarias) for their hospitality and outstanding support and the Marine Science and Technology Park (Parque Científico Tecnológico Marino) for providing access to their facilities. We are grateful to the captains and crews of ESPS RV Hesperides for deploying and recovering the mesocosms (cruise 29HE20140924), and of RV Poseidon for transporting the mesocosms and for their support in testing the deep water collector during cruise POS463. The manuscript greatly benefited from the comments of two anonymous reviewers. This project was funded by the German Federal Ministry of Education and Research (BMBF) in the framework of the coordinated project BIOACID—Biological Impacts of Ocean Acidification, phase 2 (FKZ 03F06550). U.R. received additional funding from the Leibniz Prize 2012 by the German Research Foundation (DFG).

Author information

Experiment conception and design: U.R., J.T. and L.T.B. Experiment performance: all authors. Data analysis: J.T., L.T.B., T.B., M.A.-M., J.A., W.G., C.R.L., H.G.H. and P.S. Manuscript writing: U.R. with input from all co-authors.

Competing interests

The authors declare no competing interests.

Correspondence to Ulf Riebesell.

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Fig. 1: Phytoplankton bloom development and contribution of the HAB species for the individual \({p_{\mathrm{CO_2}}}\) treatments.
Fig. 2: Temporal development of phytoplankton, and micro- and mesozooplankton biomass averaged for three \({p_{{{\rm{CO}}_2}}}\) ranges.
Fig. 3: Temporal development of total particulate carbon (TPC) for the individual \({p_{{{\rm{CO}}_2}}}\) treatments.