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Short-term effects of winter warming and acidification on phytoplankton growth and mortality: more losers than winners in a temperate coastal lagoon

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Abstract

Changes in temperature and CO2 are typically associated with climate change, but they also act on shorter time scales, leading to alterations in phytoplankton physiology and community structure. Interactions among stressors may cause synergistic or antagonistic effects on phytoplankton dynamics. Therefore, the main goal of this work is to understand the short-term isolated and interactive effects of warming and high CO2 on phytoplankton nutrient consumption, growth, production, and community structure in the Ria Formosa coastal lagoon (southern Portugal). We performed microcosm experiments with temperature and CO2 manipulation, and dilution experiments under temperature increase, using winter phytoplankton assemblages. Phytoplankton responses were evaluated using inverted and epifluorescence microscopy. Overall, phytoplankton growth and microzooplankton grazing on phytoplankton decreased with warming. Negative antagonist interactions with CO2 alleviated the negative effect of temperature on phytoplankton and cryptophytes. In contrast, higher temperature benefited smaller-sized phytoplankton, namely cyanobacteria and eukaryotic picophytoplankton. Diatom growth was not affected by temperature, probably due to nutrient limitation, but high CO2 had a positive effect on diatoms, alleviating the effect of nutrient limitation. Results suggest that this winter phytoplankton assemblage is well acclimated to ambient conditions, and short-term increases in temperature are detrimental, but can be alleviated by high CO2.

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References

  • Aberle, N., B. Bauer, a. Lewandowska, U. Gaedke & U. Sommer, 2012. Warming induces shifts in microzooplankton phenology and reduces time-lags between phytoplankton and protozoan production. Marine Biology 159: 2441–2453. http://link.springer.com//10.1007/s00227-012-1947-0.

    Article  Google Scholar 

  • Aberle, N., K. Lengfellner & U. Sommer, 2007. Spring bloom succession, grazing impact and herbivore selectivity of ciliate communities in response to winter warming. Oecologia 150: 668–681.

    Article  CAS  PubMed  Google Scholar 

  • Aberle, N., A. Malzahn, A. Lewandowska & U. Sommer, 2015. Some like it hot: the protozooplankton-copepod link in a warming ocean. Marine Ecology Progress Series 519: 103–113. http://www.int-res.com/abstracts/meps/v519/p103-113/.

  • Agawin, N. S. R., C. M. Duarte & S. Agustí, 2000. Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. Limnology and Oceanography 45: 591–600.

    Article  CAS  Google Scholar 

  • Albers, C. & D. Lakens, 2018. When power analyses based on pilot data are biased: inaccurate effect size estimators and follow-up bias. Journal of Experimental Social Psychology 74: 187–195.

    Article  Google Scholar 

  • Andrade, C., M. C. Freitas, J. Moreno & S. C. Craveiro, 2004. Stratigraphical evidence of Late Holocene barrier breaching and extreme storms in lagoonal sediments of Ria Formosa. Marine Geology 210: 339–362.

    Article  Google Scholar 

  • Bach, L. T. & J. Taucher, 2019. CO2 effects on diatoms: a synthesis of more than a decade of ocean acidification experiments with natural communities. Ocean Science 15: 1159–1175.

    Article  CAS  Google Scholar 

  • Barbosa, A. B., 2006. Estrutura e dinâmica da teia alimentar microbiana na Ria Formosa. PhD Thesis. University of Algarve.

  • Barbosa, A. B., 2010. Seasonal and interanual variability of planktonic microbes in a mesotidal coastal lagoon (Ria Formosa , SE Portugal). Impact of climatic changes and local human influences In Kennish, M. J. & H. W. Paerl (eds), Coastal Lagoons: Critical Habitats of Environmental Change. CRC Press: 334–366.

    Google Scholar 

  • Beardall, J. & J. A. Raven, 2004. The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia The International Phycological Society 43: 26–40. http://www.phycologia.org/doi/abs/10.2216/i0031-8884-43-1-26.1.

  • Behrenfeld, M. J. & E. S. Boss, 2014. Resurrecting the ecological underpinnings of ocean plankton blooms. Annual review of marine science 6: 167–194. http://www.ncbi.nlm.nih.gov/pubmed/24079309.

  • Behrenfeld, M. J., R. T. O’Malley, E. S. Boss, T. K. Westberry, J. R. Graff, K. H. Halsey, A. J. Milligan, D. A. Siegel & M. B. Brown, 2015. Revaluating ocean warming impacts on global phytoplankton. Nature Climate Change. http://www.nature.com/doifinder/10.1038/nclimate2838.

  • Berge, T., N. Daugbjerg, B. Andersen & P. Hansen, 2010. Effect of lowered pH on marine phytoplankton growth rates. Marine Ecology Progress Series 416: 79–91. http://www.int-res.com/abstracts/meps/v416/p79-91/.

  • Biswas, H., J. Jie, Y. Li, G. Zhang, Z. Y. Zhu, Y. Wu, G. L. Zhang, Y. W. Li, S. M. Liu & J. Zhang, 2015. Response of a natural phytoplankton community from the Qingdao coast (Yellow Sea, China) to variable CO2 levels over a short-term incubation experiment. Current Science 108: 1901–1909.

    CAS  Google Scholar 

  • Boyd, P. W., R. Strzepek, F. Fu & D. A. Hutchins, 2010. Environmental control of open-ocean phytoplankton groups: Now and in the future. Limnology and Oceanography 55: 1353–1376. http://www.aslo.org/lo/toc/vol_55/issue_3/1353.html.

  • Calbet, A. & E. Saiz, 2013. Effects of trophic cascades in dilution grazing experiments: from artificial saturated feeding responses to positive slopes. Journal of Plankton Research 35: 1183–1191. http://www.plankt.oxfordjournals.org/cgi/doi/10.1093/plankt/fbt067.

  • Calbet, A. & E. Saiz, 2018. How much is enough for nutrients in microzooplankton dilution grazing experiments?. Journal of Plankton Research 40: 109–117.

    Article  Google Scholar 

  • Calbet, A., K. Riisgaard, E. Saiz, S. Zamora, S. Stedmon & T. G. Nielsen, 2011a. Phytoplankton growth and microzooplankton grazing along a sub-Arctic fjord (Godthåbsfjord, west Greenland). Marine Ecology Progress Series 442: 11–22.

    Article  CAS  Google Scholar 

  • Calbet, A., E. Saiz, R. Almeda, J. I. Movilla & M. Alcaraz, 2011b. Low microzooplankton grazing rates in the Arctic Ocean during a Phaeocystis pouchetii bloom (Summer 2007): fact or artifact of the dilution technique?. Journal of Plankton Research 33: 687–701.

    Article  CAS  Google Scholar 

  • Caron, D. A. & D. A. Hutchins, 2013. The effects of changing climate on microzooplankton grazing and community structure: drivers, predictions and knowledge gaps. Journal of Plankton Research 35: 235–252. http://www.plankt.oxfordjournals.org/cgi/doi/10.1093/plankt/fbs091.

  • Chavez, F. P., M. Messié & J. T. Pennington, 2011. Marine primary production in relation to climate variability and change. Annual Review of Marine Science 3: 227–260.

    Article  PubMed  Google Scholar 

  • Chen, B., H. Liu, M. R. Landry, M. DaI, B. Huang & J. Sune, 2009. Close coupling between phytoplankton growth and microzooplankton grazing in the western South China Sea. Limnology and Oceanography 54: 1084–1097.

    Article  CAS  Google Scholar 

  • Chen, B., M. R. Landry, B. Huang & H. Liu, 2012. Does warming enhance the effect of microzooplankton grazing on marine phytoplankton in the ocean?. Limnology and Oceanography 57: 519–526. http://www.aslo.org/lo/toc/vol_57/issue_2/0519.html.

  • Cloern, J. E., P. C. Abreu, J. Carstensen, L. Chauvaud, R. Elmgren, J. Grall, H. Greening, J. O. R. Johansson, M. Kahru, E. T. Sherwood, J. Xu & K. Yin, 2016. Human activities and climate variability drive fast-paced change across the world’s estuarine-coastal ecosystems. Global Change Biology 22: 513–529.

    Article  PubMed  Google Scholar 

  • Coello-Camba, A., S. Agustí, J. Holding, J. M. Arrieta & C. M. Duarte, 2014. Interactive effect of temperature and CO2 increase in Arctic phytoplankton. Frontiers in Marine Science 1: 1–10, http://journal.frontiersin.org/article/10.3389/fmars.2014.00049/abstract.

  • Collos, Y., J. Husseini-Ratrema, B. Bec, A. Vaquer, T. L. Hoai, C. Rougier, V. Pons & P. Souchu, 2005. Pheopigment dynamics, zooplankton grazing rates and the autumnal ammonium peak in a Mediterranean lagoon. Hydrobiologia 550: 83–93. http://link.springer.com/10.1007/s10750-005-4365-1.

  • Cornwall, C. E., C. D. Hepburn, C. M. Mcgraw, K. I. Currie, C. A. Pilditch, K. A. Hunter, P. W. Boyd & C. L. Hurd, 2013. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proceedings of the Royal Society B 280: 20132201. http://rspb.royalsocietypublishing.org.

  • Cravo, A., S. Cardeira, C. Pereira, M. Rosa, P. Alcântara, M. Madureira, F. Rita, J. Luis & J. Jacob, 2014. Exchanges of nutrients and chlorophyll a through two inlets of Ria Formosa, South of Portugal, during coastal upwelling events. Journal of Sea Research 93: 63–74. http://linkinghub.elsevier.com/retrieve/pii/S1385110114000768.

  • Cravo, A., A. Rosa, J. Jacob & C. Correia, 2020. Dissolved oxygen dynamics in Ria Formosa Lagoon (South Portugal) – aA real time monitoring station observatory. Marine Chemistry. https://doi.org/10.1016/j.marchem.2020.103806.

    Article  Google Scholar 

  • Daufresne, M., K. Lengfellner & U. Sommer, 2009. Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106: 12788–12793. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2722360&tool=pmcentrez&rendertype=abstract.

  • De Bodt, C., N. Van Oostende, J. Harlay, K. Sabbe & L. Chou, 2010. Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size. Biogeosciences 7: 1401–1412.

    Article  CAS  Google Scholar 

  • Dix, N. & M. D. Hanisak, 2015. Microzooplankton grazing experiments in the subtropical Indian River Lagoon, Florida challenge assumptions of the dilution technique. Journal of Experimental Marine Biology and Ecology 465: 1–10. http://linkinghub.elsevier.com/retrieve/pii/S0022098114003256.

  • Dokulil, M. T. & K. Teubner, 2000. Cyanobacterial dominance in lakes. Hydrobiologia 438: 1–12.

    Article  CAS  Google Scholar 

  • Dolan, J. R., C. L. Gallegos & A. Moigis, 2000. Dilution effects on microzooplankton in dilution grazing experiments. Marine Ecology Progress Series 200: 127–139.

    Article  CAS  Google Scholar 

  • Domingues, R. B., T. P. Anselmo, A. B. Barbosa, U. Sommer & H. M. Galvão, 2011a. Nutrient limitation of phytoplankton growth in the freshwater tidal zone of a turbid, Mediterranean estuary. Estuarine, Coastal and Shelf Science 91: 282–297. http://www.linkinghub.elsevier.com/retrieve/pii/S0272771410003756.

  • Domingues, R. B., A. B. Barbosa, U. Sommer & H. M. Galvão, 2011b. Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquatic Sciences 73: 331–343. http://www.link.springer.com/10.1007/s00027-011-0180-0.

  • Domingues, R. B., C. C. Guerra, A. B. Barbosa, V. Brotas & H. M. Galvão, 2014. Effects of ultraviolet radiation and CO2 increase on winter phytoplankton assemblages in a temperate coastal lagoon. Journal of Plankton Research 36: 672–684, http://www.plankt.oxfordjournals.org/cgi/doi/10.1093/plankt/fbt135.

  • Domingues, R. B., C. C. Guerra, A. B. Barbosa & H. M. Galvão, 2015. Are nutrients and light limiting summer phytoplankton in a temperate coastal lagoon?. Aquatic Ecology 49: 127–146. http://link.springer.com/10.1007/s10452-015-9512-9.

  • Domingues, R. B., C. C. Guerra, A. B. Barbosa & H. M. Galvão, 2017a. Will nutrient and light limitation prevent eutrophication in an anthropogenically-impacted coastal lagoon?. Continental Shelf Research 141: 11–25. http://linkinghub.elsevier.com/retrieve/pii/S0278434317300699.

  • Domingues, R. B., C. C. Guerra, H. M. Galvão, V. Brotas & A. B. Barbosa, 2017b. Short-term interactive effects of ultraviolet radiation, carbon dioxide and nutrient enrichment on phytoplankton in a shallow coastal lagoon. Aquatic Ecology 51: 91–105, http://link.springer.com/10.1007/s10452-016-9601-4.

  • Dutkiewicz, S., J. R. Scott & M. J. Follows, 2013. Winners and losers: ecological and biogeochemical changes in a warming ocean. Global Biogeochemical Cycles 27: 463–477.

    Article  CAS  Google Scholar 

  • Dutkiewicz, S., J. J. Morris, M. J. Follows, J. Scott, O. Levitan, S. T. Dyhrman & I. Berman-Frank, 2015. Impact of ocean acidification on the structure of future phytoplankton communities. Nature Climate Change. https://doi.org/10.1038/nclimate2722.

    Article  Google Scholar 

  • Eilers, P. H. C. & J. C. H. Peeters, 1988. A model for the relationship between light and intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling 42: 199–215.

    Article  Google Scholar 

  • Endo, H., K. Sugie, T. Yoshimura & K. Suzuki, 2016. Response of spring diatoms to CO2 availability in the western North Pacific as determined by next-generation sequencing. PLoS ONE 11: 1–22.

    Article  CAS  Google Scholar 

  • Eppley, R. W., 1972. Temperature and phytoplankton growth in the sea. Fishery Bulletin 70: 1063–1085.

    Google Scholar 

  • Eriander, L., A.-L. Wrange & J. N. Havenhand, 2016. Simulated diurnal pH fluctuations radically increase variance in – but not the mean of – growth in the barnacle Balanus improvisus. ICES Journal of Marine Science 73: 596–603.

    Article  Google Scholar 

  • Feng, Y., C. E. Hare, K. Leblanc, J. M. Rose, Y. Zhang, G. R. DiTullio, P. A. Lee, S. W. Wilhelm, J. M. Rowe, J. Sun, N. Nemcek, C. Gueguen, U. Passow, I. Benner, C. Brown & D. A. Hutchins, 2009. Effects of increased pCO2 and temperature on the north atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Marine Ecology Progress Series 388: 13–25.

    Article  CAS  Google Scholar 

  • Feng, Y., C. E. Hare, J. M. Rose, S. M. Handy, G. R. DiTullio, P. A. Lee, W. O. Smith, J. Peloquin, S. Tozzi, J. Sun, Y. Zhang, R. B. Dunbar, M. C. Long, B. Sohst, M. Lohan & D. A. Hutchins, 2010. Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton. Deep-Sea Research Part I: Oceanographic Research Papers 57: 368–383.

    Article  CAS  Google Scholar 

  • Fisher, T. R., L. W. Harding, D. W. Stanley & L. G. Ward, 1988. Phytoplankton, nutrients, and turbidity in the Chesapeake, Delaware, and Hudson estuaries. Estuarine, Coastal and Shelf Science 27: 61–93.

    Article  CAS  Google Scholar 

  • Flores, E. & A. Herrero, 2005. Nitrogen assimilation and nitrogen control in cyanobacteria. Biochemical Society transactions 33: 164–167. http://www.ncbi.nlm.nih.gov/pubmed/15667295.

  • Fu, F.-X., M. E. Warner, Y. Zhang, Y. Feng & D. A. Hutchins, 2007. Effects of Increased Temperature and CO2 on Photosynthesis, Growth, and Elemental Ratios in Marine Synechococcus and Prochlorococcus (Cyanobacteria). Journal of Phycology 43: 485–496. http://doi.wiley.com/10.1111/j.1529-8817.2007.00355.x.

  • Fu, F., A. Tatters & D. Hutchins, 2012. Global change and the future of harmful algal blooms in the ocean. Marine Ecology Progress Series 470: 207–233. http://www.int-res.com/abstracts/meps/v470/p207-233/.

  • Fu, F. X., Y. Zhang, M. E. Warner, Y. Feng, J. Sun & D. A. Hutchins, 2008. A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7: 76–90.

    Article  CAS  Google Scholar 

  • Gallegos, C., 1989. Microzooplankton grazing on phytoplankton in Rhode River, Maryland: noninear feeding kinetics. Marine Ecology Progress Series 57: 23–33.

    Article  Google Scholar 

  • Gao, K. & D. A. Campbell, 2014. Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Functional Plant Biology 41: 449–459.

    Article  CAS  PubMed  Google Scholar 

  • Gao, K., E. Helbling, D.-P. Häder & D. Hutchins, 2012. Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Marine Ecology Progress Series 470: 167–189. http://www.int-res.com/abstracts/meps/v470/p167-189/.

  • Gattuso, J.-P., K. Gao, K. Lee, B. Rost & K. G. Schulz, 2010. Approaches and tools to manipulate the carbonate chemistry In Riebesell, U., V. J. Fabry, L. Hansson & J.-P. Gattuso (eds), Guide to Best Practices for Ocean Acidification Research and Data Reporting. Publications Office of the European Union: 41–52.

  • Giordano, M., J. Beardall & J. a Raven, 2005. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56: 99–131. http://www.ncbi.nlm.nih.gov/pubmed/15862091.

  • Goela, P. C., S. Danchenko, J. D. Icely, L. M. Lubian, S. Cristina & A. Newton, 2014. Using CHEMTAX to evaluate seasonal and interannual dynamics of the phytoplankton community off the South-west coast of Portugal. Estuarine, Coastal and Shelf Science 151: 112–123. http://apps.webofknowledge.com/full_record.do?product=WOS&search_mode=GeneralSearch&qid=12&SID=W1nP4i9eaabP6SGhOzF&page=1&doc=10&cacheurlFromRightClick=no.

  • Grasshoff, K., M. Ehrhardt & K. Kremling, 1999. Methods of Seawater Analysis. WILEY‐VCH Verlag GmbH, Weinheim. https://onlinelibrary.wiley.com/doi/book/10.1002/9783527613984.

  • Grinienė, E., S. Šulčius & H. Kuosa, 2016. Size-selective microzooplankton grazing on the phytoplankton in the Curonian Lagoon (SE Baltic Sea). Oceanologia 58: 292–301.

    Article  Google Scholar 

  • Guiry, M. D. & G. M. Guiry, 2021. AlgaeBase. World-wide electronic publication. National University of Ireland, Galway.

    Google Scholar 

  • Haas, L. W., 1982. Improved epifluorescence microscopy for observing planktonic micro-organisms. Annales de l’Institut Oceanographique 58: 261–266.

    Google Scholar 

  • Halac, S. R., S. D. Guendulain-García, V. E. Villafañe, E. W. Helbling & A. T. Banaszak, 2013. Responses of tropical plankton communities from the Mexican Caribbean to solar ultraviolet radiation exposure and increased temperature. Journal of Experimental Marine Biology and Ecology 445: 99–107. http://linkinghub.elsevier.com/retrieve/pii/S0022098113001652.

  • Hare, C. E., K. Leblanc, G. R. DiTullio, R. M. Kudela, Y. Zhang, P. A. Lee, S. Riseman & D. A. Hutchins, 2007. Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Marine Ecology Progress Series 352: 9–16. http://www.int-res.com/abstracts/meps/v352/p9-16/.

  • Henson, S. A., C. Beaulieu & R. Lampitt, 2016. Observing climate change trends in ocean biogeochemistry: when and where. Global Change Biology 22: 1561–1571.

    Article  PubMed  PubMed Central  Google Scholar 

  • Henson, S. A., C. Beaulieu, T. Ilyina, J. G. John, M. Long, R. Séférian, J. Tjiputra & J. L. Sarmiento, 2017. Rapid emergence of climate change in environmental drivers of marine ecosystems. Nature Communications 8: 1–9.

    Article  Google Scholar 

  • Holding, J. M., C. M. Duarte, M. Sanz-Martín, E. Mesa, J. M. Arrieta, M. Chierici, I. E. Hendriks, L. S. García-Corral, A. Regaudie-De-Gioux, A. Delgado, M. Reigstad, P. Wassmann & S. Agustí, 2015. Temperature dependence of CO2-enhanced primary production in the European Arctic Ocean. Nature Climate Change 5: 1079–1082.

    Article  CAS  Google Scholar 

  • Hoppe, C. J. M., K. K. E. Wolf, N. Schuback, P. D. Tortell & B. Rost, 2018. Compensation of ocean acidification effects in Arctic phytoplankton assemblages. Nature Climate Change 8: 529–533.

    Article  CAS  Google Scholar 

  • Horn, H. G., M. Boersma, J. Garzke, U. Sommer & N. Aberle, 2020. High CO2 and warming affect microzooplankton food web dynamics in a Baltic Sea summer plankton community. Marine Biology 167: 1–17.

    Article  CAS  Google Scholar 

  • IPCC, 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva.

  • Jiang, S., F. Hashihama & H. Saito, 2021. Phytoplankton growth and grazing mortality through the oligotrophic subtropical North Pacific. Journal of Oceanography 77: 505–521.

    Article  CAS  Google Scholar 

  • Justíc, D., N. N. Rabalais, R. E. Turner & Q. Dortch, 1995. Changes in nutrient structure of river dominated coastal waters: stoichiometric nutrient balance and its consequences. Estuarine, Coastal and Shelf Science 40: 339–356.

    Article  Google Scholar 

  • Keys, M., G. Tilstone, H. S. Findlay, C. E. Widdicombe & T. Lawson, 2018. Effects of elevated CO2 and temperature on phytoplankton community biomass, species composition and photosynthesis during an experimentally induced autumn bloom in the western English Channel. Biogeosciences 15: 3203–3222. https://bg.copernicus.org/articles/15/3203/2018/.

  • Kroeker, K. J., R. L. Kordas, R. Crim, I. E. Hendriks, L. Ramajo, G. S. Singh, C. M. Duarte & J.-P. Gattuso, 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology. http://doi.wiley.com/10.1111/gcb.12179.

  • Landry, M. R. & R. P. Hassett, 1982. Estimating the grazing impact of marine micro-zooplankton. Marine Biology 67: 283–288. http://link.springer.com/10.1007/BF00397668.

  • Lewandowska, A. M., D. G. Boyce, M. Hofmann, B. Matthiessen, U. Sommer & B. Worm, 2014. Effects of sea surface warming on marine plankton. Ecology Letters . http://www.ncbi.nlm.nih.gov/pubmed/24575918.

  • Liu, X., Y. Li, Y. Wu, B. Huang, M. Dai, F. Fu, D. A. Hutchins & K. Gao, 2017. Effects of elevated CO2 on phytoplankton during a mesocosm experiment in the southern eutrophicated coastal water of China. Scientific Reports 7: 1–14.

    CAS  Google Scholar 

  • Lomas, M., B. Hopkinson, J. Losh, D. Ryan, D. Shi, Y. Xu & F. Morel, 2012. Effect of ocean acidification on cyanobacteria in the subtropical North Atlantic. Aquatic Microbial Ecology 66: 211–222.

    Article  Google Scholar 

  • López-Urrutia, A., E. S. Martin, R. P. Harris & X. Irigoien, 2006. Scaling the metabolic balance of the oceans. Proceedings of the National Academy of Sciences of the United States of America 103: 8739–8744. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1482648&tool=pmcentrez&rendertype=abstract.

  • Lv, H., J. Yang, L. Liu, X. Yu, Z. Yu & P. Chiang, 2014. Temperature and nutrients are significant drivers of seasonal shift in phytoplankton community from a drinking water reservoir, subtropical China. Environmental Science and Pollution Research International 21: 5917–5928. http://apps.webofknowledge.com/full_record.do?product=UA&search_mode=GeneralSearch&qid=3&SID=X1PxQbuYNMjPY5PkCIh&page=1&doc=3&cacheurlFromRightClick=no.

  • Machado, L. M., 2010. A radiação UV-B na Ria Formosa: incidência e impactes biológicos. University of Algarve.

  • Maugendre, L., J.-P. Gattuso, J. Louis, A. de Kluijver, S. Marro, K. Soetaert & F. Gazeau, 2015. Effect of ocean warming and acidification on a plankton community in the NW Mediterranean Sea. ICES Journal of Marine Science 72: 1744–1755.

    Article  Google Scholar 

  • Menden-Deuer, S., C. Lawrence & G. Franzè, 2018. Herbivorous protist growth and grazing rates at in situ and artificially elevated temperatures during an Arctic phytoplankton spring bloom. PeerJ 6: e5264.

  • Mendes, C. R. B., V. M. Tavano, M. C. Leal, M. S. Souza, V. Brotas & C. A. E. Garcia, 2013. Shifts in the dominance between diatoms and cryptophytes during three late summers in the Bransfield Strait (Antarctic Peninsula). Polar Biology 36: 537–547. http://link.springer.com/10.1007/s00300-012-1282-4.

  • Meyer, J. & U. Riebesell, 2015. Reviews and syntheses: Responses of coccolithophores to ocean acidification: A meta-analysis. Biogeosciences 12: 1671–1682.

    Article  Google Scholar 

  • Montagnes, D. J. S. & D. J. Franklin, 2001. Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: reconsidering some paradigms. Limnology and Oceanography 46: 2008–2018. http://www.aslo.org/lo/toc/vol_46/issue_8/2008.html.

  • Morán, X. A. G., Á. López-Urrutia, A. Calvo-Díaz & W. K. W. Li, 2010a. Increasing importance of small phytoplankton in a warmer ocean. Global Change Biology 16: 1137–1144.

    Article  Google Scholar 

  • Morán, X. A. G., Á. López-Urrutia, A. Calvo-Díaz & W. K. W. Li, 2010b. Increasing importance of small phytoplankton in a warmer ocean. Global Change Biology 16: 1137–1144.

    Article  Google Scholar 

  • Morison, F. & S. Menden-Deuer, 2017. Doing more with less? Balancing sampling resolution and effort in measurements of protistan growth and grazing-rates. Limnology and Oceanography: Methods 15: 794–809.

    Google Scholar 

  • Nejstgaard, J., I. Gismervik & P. Solberg, 1997. Feeding and reproduction by Calanus finmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Marine Ecology Progress Series 147: 197–217.

    Article  Google Scholar 

  • Newton, A. & S. M. Mudge, 2003. Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuarine, Coastal and Shelf Science 57: 73–85. http://linkinghub.elsevier.com/retrieve/pii/S0272771402003323.

  • Newton, A., J. D. Icely, M. Falcao, A. Nobre, J. P. Nunes, J. G. Ferreira & C. Vale, 2003. Evaluation of eutrophication in the Ria Formosa coastal lagoon, Portugal. Continental Shelf Research 23: 1945–1961. http://linkinghub.elsevier.com/retrieve/pii/S0278434303001584.

  • Nielsen, L., G. Hallegraeff, S. Wright & P. Hansen, 2012. Effects of experimental seawater acidification on an estuarine plankton community. Aquatic Microbial Ecology 65: 271–286. http://www.int-res.com/abstracts/ame/v65/n3/p271-286/.

  • Nogueira, P., R. B. Domingues & A. B. Barbosa, 2014. Are microcosm volume and sample pre-filtration relevant to evaluate phytoplankton growth?. Journal of Experimental Marine Biology and Ecology 461: 323–330. http://linkinghub.elsevier.com/retrieve/pii/S0022098114002494.

  • O’Connor, M. I., M. F. Piehler, D. M. Leech, A. Anton & J. F. Bruno, 2009. Warming and resource availability shift food web structure and metabolism. PLoS Biology 7: e1000178. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2723928&tool=pmcentrez&rendertype=abstract.

  • Olejnik, S. & J. Algina, 2003. Generalized eta and omega squared statistics: measures of effect size for some common research designs. Psychological Methods 8: 434–447.

    Article  PubMed  Google Scholar 

  • Parsons, T. R., Y. Maita & C. M. Lalli, 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford.

    Google Scholar 

  • Pequin, B., V. Mohit, T. Poisot, R. Tremblay & C. Lovejoy, 2017. Wind drives microbial eukaryote communities in a temperate closed lagoon. Aquatic Microbial Ecology 78: 187–200.

    Article  Google Scholar 

  • Pereira, M. G., J. Icely, S. Mudge, A. Newton & R. Rodrigues, 2007. Temporal and spatial variation of phytoplankton pigments in the Western Part of Ria Formosa Lagoon, Southern Portugal. Environmental Forensics 8: 205–220.

    Article  CAS  Google Scholar 

  • Piggott, J. J., C. R. Townsend & C. D. Matthaei, 2015. Reconceptualizing synergism and antagonism among multiple stressors. Ecology and Evolution 5: 1538–1547.

    Article  PubMed  PubMed Central  Google Scholar 

  • Platt, T. & S. Sathyendranath, 2008. Ecological indicators for the pelagic zone of the ocean from remote sensing. Remote Sensing of Environment 112: 3426–3436. http://www.sciencedirect.com/science/article/pii/S0034425708001272.

  • R Core Team, 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org/.

  • Racault, M.-F., C. Le Quéré, E. Buitenhuis, S. Sathyendranath & T. Platt, 2012. Phytoplankton phenology in the global ocean. Ecological Indicators 14: 152–163. http://linkinghub.elsevier.com/retrieve/pii/S1470160X11002160.

  • Rae, B. D., B. Forster, M. R. Badger & G. D. Price, 2011. The CO2-concentrating mechanism of Synechococcus WH5701 is composed of native and horizontally-acquired components. Photosynthesis Research 109: 59–72.

    Article  CAS  PubMed  Google Scholar 

  • Raven, J. A. & J. Beardall, 2014. CO2 concentrating mechanisms and environmental change. Aquatic Botany 118: 24–37. http://linkinghub.elsevier.com/retrieve/pii/S0304377014000734.

  • Raven, J. A., J. Beardall & M. Giordano, 2014. Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynthesis Research 121: 111–124.

    Article  CAS  PubMed  Google Scholar 

  • Revilla, T. & F. J. Weissing, 2008. Nonequilibrium coexistence in a competition model with nutrient storage. Ecology 89: 865–877.

    Article  PubMed  Google Scholar 

  • Richier, S., E. P. Achterberg, C. Dumousseaud, A. J. Poulton, D. J. Suggett, T. Tyrrell, M. V. Zubkov & C. M. Moore, 2014. Phytoplankton responses and associated carbon cycling during shipboard carbonate chemistry manipulation experiments conducted around Northwest European shelf seas. Biogeosciences 11: 4733–4752.

    Article  Google Scholar 

  • Riebesell, U., 2004. Effects of CO2 Enrichment on Marine Phytoplankton. Journal of Oceanography 60: 719–729. http://link.springer.com/10.1007/s10872-004-5764-z.

  • Rose, J. M. & D. A. Caron, 2007. Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnology and Oceanography 52: 886–895. http://www.aslo.org/lo/toc/vol_52/issue_2/0886.html.

  • Rose, J. M., Y. Feng, C. Gobler, R. Gutierrez, C. Hare, K. Leblanc & D. Hutchins, 2009. Effects of increased pCO2 and temperature on the North Atlantic spring bloom. II. Microzooplankton abundance and grazing. Marine Ecology Progress Series 388: 27–40. http://www.int-res.com/abstracts/meps/v388/p27-40/.

  • Santos, F. D., K. Forbes & R. Moita, 2002. Climate Change in Portugal. Scenarios, impacts and adaptation measures. Gradiva.

  • Schippers, P., M. Lurling & M. Scheffer, 2004. Increase of atmospheric CO2 promotes phytoplankton productivity. Ecology Letters 7: 446–451. http://www.blackwell-synergy.com/links/doi/10.1111%2Fj.1461-0248.2004.00597.x.

  • Schmidt, K., A. J. Birchill, A. Atkinson, R. J. W. Brewin, J. R. Clark, A. E. Hickman, D. G. Johns, M. C. Lohan, A. Milne, S. Pardo, L. Polimene, T. J. Smyth, G. A. Tarran, C. E. Widdicombe, E. M. S. Woodward & S. J. Ussher, 2020. Increasing picocyanobacteria success in shelf waters contributes to long-term food web degradation. Global Change Biology 26: 5574–5587.

    Article  PubMed  Google Scholar 

  • Schmoker, C., S. Hernandez-Leon & A. Calbet, 2013. Microzooplankton grazing in the oceans: impacts, data variability, knowledge gaps and future directions. Journal of Plankton Research 35: 691–706. http://www.plankt.oxfordjournals.org/cgi/doi/10.1093/plankt/fbt023.

  • Seifert, M., R. Bjorn, S. Trimborn & J. Hauck, 2020. Meta-analysis of multiple driver effects on marine phytoplankton highlights modulating role of p CO2. Global Change Biology 1–62.

  • Sherman, E., J. K. Moore, F. Primeau & D. Tanouye, 2016. Temperature influence on phytoplankton community growth rates. Global Biogeochemical Cycles 30: 550–559.

    Article  CAS  Google Scholar 

  • Sobrino, C., M. L. Ward & P. J. Neale, 2008. Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnology and Oceanography 53: 494–505.

    Article  CAS  Google Scholar 

  • Sommer, U., N. Aberle, K. Lengfellner & A. Lewandowska, 2012. The Baltic Sea spring phytoplankton bloom in a changing climate: an experimental approach. Marine Biology 159: 2479–2490. http://link.springer.com/10.1007/s00227-012-1897-6.

  • Sommer, U., C. Paul & M. Moustaka-Gouni, 2015. Warming and ocean acidification effects on phytoplankton - From species shifts to size shifts within species in a mesocosm experiment. PLoS ONE 10: 1–17.

    Article  Google Scholar 

  • Song, C., F. Ballantyne IV & V. H. Smith, 2014. Enhanced dissolved organic carbon production in aquatic ecosystems in response to elevated atmospheric CO2. Biogeochemistry 118: 49–60.

    Article  CAS  Google Scholar 

  • Steeman-Nielsen, E., 1952. The use of radio-active carbon (C14) for measuring organic production in the sea. Journal du Counseil International pour l’Exploration de la Mer 18: 117–140.

    Article  Google Scholar 

  • Stramma, L., P. Cornillon, R. A. Weller, J. F. Price & M. G. Briscoe, 1986. Large diurnal sea surface temperature variability: satellite and in situ measurements. Journal of Physical Oceanography 56: 345–358.

    Google Scholar 

  • Strom, S. L., M. A. Brainard, J. L. Holmes & M. B. Olson, 2001. Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Marine Biology 138: 355–368.

    Article  CAS  Google Scholar 

  • Strom, S. L., E. L. Macri & M. B. Olson, 2007. Microzooplankton grazing in the coastal Gulf of Alaska: Variations in top-down control of phytoplankton. Limnology and Oceanography 52: 1480–1494.

    Article  Google Scholar 

  • Stuart-Menteth, A. C., I. S. Robinson & P. G. Challenor, 2003. A global study of diurnal warming using satellite-derived sea surface temperature. Journal of Geophysical Research 108: 3155. http://onlinelibrary.wiley.com/doi/10.1029/2002JC001534/full.

  • Suzuki, K., A. Tsuda, H. Kiyosawa, S. Takeda, J. Nishioka, T. Saino, M. Takahashi & C. S. Wong, 2002. Grazing impact of microzooplankton on a diatom bloom in a mesocosm as estimated by pigment-specific dilution technique. Journal of Experimental Marine Biology and Ecology 271: 99–120.

    Article  Google Scholar 

  • Tatters, A. O., M. Y. Roleda, A. Schnetzer, F. Fu, C. L. Hurd, P. W. Boyd, D. A. Caron, A. A. Y. Lie, L. J. Hoffmann & D. A. Hutchins, 2013. Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 368: 20120437. http://www.ncbi.nlm.nih.gov/pubmed/23980240.

  • Teixeira, I. G. & F. G. Figueiras, 2009. Feeding behaviour and non-linear responses in dilution experiments in a coastal upwelling system. Aquatic Microbial Ecology 55: 53–63.

    Article  Google Scholar 

  • Teixeira, I. G., F. G. Figueiras, B. G. Crespo & S. Piedracoba, 2011. Microzooplankton feeding impact in a coastal upwelling system on the NW Iberian margin: the Ría de Vigo. Estuarine, Coastal and Shelf Science 91: 110–120.

    Article  Google Scholar 

  • Teixeira, I. G., B. G. Crespo, T. G. Nielsen & F. G. Figueiras, 2012. Role of microzooplankton during a Phaeocystis sp. bloom in the Oosterschelde (SW Netherlands). Journal of Marine Systems 94: 97–106.

    Article  Google Scholar 

  • Teixeira, I. G., B. G. Crespo, T. G. Nielsen & F. G. Figueiras, 2014. Stratification-mixing cycles and plankton dynamics in a shallow estuary (Limfjord, Denmark). Journal of Plankton Research 36: 475–489.

    Article  CAS  Google Scholar 

  • Torstensson, A., M. Chierici & A. Wulff, 2012. The influence of increased temperature and carbon dioxide levels on the benthic/sea ice diatom Navicula directa. Polar Biology 35: 205–214.

    Article  Google Scholar 

  • Tortell, P. D., G. R. DiTullio, D. M. Sigman & F. M. M. Morel, 2002. CO2 effects on taxonomic composition and nutrient utilization in an Equatorial Pacific phytoplankton assemblage. Marine Ecology Progress Series 236: 37–43.

    Article  Google Scholar 

  • Tortell, P. D., C. D. Payne, Y. Li, S. Trimborn, B. Rost, W. O. Smith, C. Riesselman, R. B. Dunbar, P. Sedwick & G. R. DiTullio, 2008. CO2 sensitivity of Southern Ocean phytoplankton. Geophysical Research Letters 35: 1–5.

    Article  CAS  Google Scholar 

  • Trombetta, T., F. Vidussi, S. Mas, D. Parin, M. Simier & B. Mostajir, 2019. Water temperature drives phytoplankton blooms in coastal waters. PLoS ONE 14.

  • Tsai, A. Y., G.-C. Gong & W. Shiau, 2015. Viral lysis and nanoflagellate grazing on prokaryotes: effects of short-term warming in a coastal subtropical marine system. Hydrobiologia 751: 43–54. http://link.springer.com/10.1007/s10750-014-2170-4.

  • Tsai, A., G. Gong & W. Shiau, 2016. Impact of short-term warming on seasonal variations in bacterial growth, grazing, and viral lysis in coastal waters of Taiwan. Aquatic Microbial Ecology 76: 195–205. http://www.int-res.com/abstracts/ame/v76/n3/p195-205/.

  • Twiss, M. R. & D. E. Smith, 2012. Size-fractionated phytoplankton growth and microzooplankton grazing rates in the upper St. Lawrence River. River Research and Applications 28: 1047–1053.

    Article  Google Scholar 

  • Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt. Internationale Ver. Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Valiela, I., 1995. Marine Ecological Processes. Springer, New York.

    Book  Google Scholar 

  • Venrick, E. L., 1978. How many cells to count? In Sournia, A. (ed), Phytoplankton Manual. UNESCO, Paris: 167–180.

    Google Scholar 

  • Vidussi, F., B. Mostajir, E. Fouilland, E. Le Floc’h, J. Nouguier, C. Roques, P. Got, D. Thibault-Botha, T. Bouvier & M. Troussellier, 2011. Effects of experimental warming and increased ultraviolet B radiation on the Mediterranean plankton food web. Limnology and Oceanography 56: 206–218. http://www.aslo.org/lo/toc/vol_56/issue_1/0206.html.

  • Williams, O. J., R. E. Beckett & D. L. Maxwell, 2016. Marine phytoplankton preservation with Lugol’s: a comparison of solutions. Journal of Applied Phycology Journal of Applied Phycology 28: 1705–1712.

    Article  CAS  Google Scholar 

  • Worden, A. & B. Binder, 2003. Application of dilution experiments for measuring growth and mortality rates among Prochlorococcus and Synechococcus populations in oligotrophic environments. Aquatic Microbial Ecology 30: 159–174.

    Article  Google Scholar 

  • Wu, Y., D. A. Campbell, A. J. Irwin, D. Suggett & Z. Finkel, 2014. Ocean acidification enhances the growth rate of larger diatoms. Limnology and Oceanography 59: 1027–1034. http://www.aslo.org/lo/toc/vol_59/issue_3/1027.html.

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Funding

This work was financially supported by the Portuguese Foundation for Science and Technology (FCT) through projects PTDC/AAC-CLI/103348/2008 and UIDP/00350/2020. FCT provided funding for RBD through a postdoctoral fellowship and a researcher contract (SFRH/BPD/68688/2010, DL57/2016/CP1361/CT0017).

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Domingues, R.B., Barreto, M., Brotas, V. et al. Short-term effects of winter warming and acidification on phytoplankton growth and mortality: more losers than winners in a temperate coastal lagoon. Hydrobiologia 848, 4763–4785 (2021). https://doi.org/10.1007/s10750-021-04672-0

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