DOI QR코드

DOI QR Code

Thermal plasticity of growth and chain formation of the dinoflagellates Alexandrium affine and Alexandrium pacificum with respect to ocean acidification

  • Lee, Chung Hyeon (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • Min, Juhee (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • Lee, Hyun-Gwan (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • Kim, Kwang Young (Department of Oceanography, College of Natural Sciences, Chonnam National University)
  • Received : 2021.10.03
  • Accepted : 2021.12.01
  • Published : 2021.12.15

Abstract

The amount of CO2 absorbed by the oceans continues to rise, resulting in further acidification, altering some functional traits of phytoplankton. To understand the effect of elevated partial pressures of CO2 (pCO2) on functional traits of dinoflagellates Alexandrium affine and A. pacificum, the cardinal temperatures and chain formation extent were examined under two pCO2 (400 and 1,000 µatm) over the range of temperature expected to be associated with growth. The growth rate and chain formation extent of A. affine increased with higher pCO2, showing significant changes in cardinal temperatures and a substantial increase in middle chain-length (4-8 cells) fractionation under elevated pCO2 condition. By contrast, there were no significant differences in specific growth rate and any chain-length fractionation of A. pacificum between ambient and elevated pCO2 conditions. The observed interspecies variation in the functional traits may reflect differences in ability of species to respond to environmental change with plasticity. Moreover, it allows us to understand the shifting biogeography of marine phytoplankton and predict their phenology in the Korea Strait.

Keywords

Acknowledgement

We would like to thank Professor MG Park of Chonnam National University for kindly offering Alexandrium strains. This research was supported by a National Research Foundation (NRF) grant funded by the Korean government (MSIT) (NRF-2016R1A6A1A03012647, NRF-2020R1A2C3005053) to KYK.

References

  1. Bagby, S. C. & Chisholm, S. W. 2015. Response of Prochlorococcus to varying CO2:O2 ratios. ISME J. 9:2232-2245. https://doi.org/10.1038/ismej.2015.36
  2. Basti, L., Nagai, S., Go, J., Okano, S., Nagai, K., Watanabe, R., Suzuki, T. & Tanaka, Y. 2015. Differential inimical effects of Alexandrium spp. and Karenia spp. on cleavage, hatching, and two larval stages of Japanese pearl oyster Pinctada fucata martensii. Harmful Algae 43:1-12. https://doi.org/10.1016/j.hal.2014.12.004
  3. Basu, S. & Mackey, K. R. 2018. Phytoplankton as key mediators of the biological carbon pump: their responses to a changing climate. Sustainability 10:869. https://doi.org/10.3390/su10030869
  4. Bausch, A. R., Juhl, A. R., Donaher, N. A. & Cockshutt, A. M. 2019. Combined effects of simulated acidification and hypoxia on the harmful dinoflagellate Amphidinium carterae. Mar. Biol. 166:80. https://doi.org/10.1007/s00227-019-3528-y
  5. Beardall, J., Allen, D., Bragg, J., Finkel, Z. V., Flynn, K. J., Quigg, A., Rees, T. A. V., Richardson, A. & Raven, J. A. 2009. Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. New Phytol. 181:295-309. https://doi.org/10.1111/j.1469-8137.2008.02660.x
  6. Benard, R., Levasseur, M., Scarratt, M., Blais, M. -A., Mucci, A., Ferreyra, G., Starr, M., Gosselin, M., Tremblay, J. -E. & Lizotte, M. 2018. Experimental assessment of the sensitivity of an estuarine phytoplankton fall bloom to acidification and warming. Biogeosciences 15:4883-4904. https://doi.org/10.5194/bg-15-4883-2018
  7. Bergkvist, J., Thor, P., Jakobsen, H. H., Wangberg, S. -A. & Selander, E. 2012. Grazer-induced chain length plasticity reduces grazing risk in a marine diatom. Limnol. Oceanogr. 57:318-324. https://doi.org/10.4319/lo.2012.57.1.0318
  8. Bjaerke, O., Jonsson, P. R., Alam, A. & Selander, E. 2015. Is chain length in phytoplankton regulated to evade predation? J. Plankton Res. 37:1110-1119. https://doi.org/10.1093/plankt/fbv076
  9. Brandenburg, K. M., Krock, B., Klip, H. C. L., Sluijs, A., Garbeva, P. & Van de Waal, D. B. 2021. Intraspecific variation in multiple trait responses of Alexandrium ostenfeldii towards elevated pCO2. Harmful Algae 101:101970. https://doi.org/10.1016/j.hal.2020.101970
  10. Brondizio, E., Diaz, S., Settele, J. & Ngo, H. T. 2019. IPBES: Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. IPBES Secretariat, Bonn, pp. 680-681.
  11. Cai, W. -J., Hu, X., Huang, W. -J., Murrell, M. C., Lehrter, J. C., Lohrenz, S. E., Chou, W. -C., Zhai, W., Hollibuagh, J. T., Wang, Y., Zhao, P., Guo, X., Gundersen, K., Dai, M. & Gong, G. -C. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4:766-770. https://doi.org/10.1038/ngeo1297
  12. Carstensen, J. & Duarte, C. M. 2019. Drivers of pH variability in coastal ecosystems. Environ. Sci. Technol. 53:4020-4029. https://doi.org/10.1021/acs.est.8b03655
  13. Comeau, S., Carpenter, R. C. & Edmunds, P. J. 2013. Coral reef calcifiers buffer their response to ocean acidification using both bicarbonate and carbonate. Proc. R. Soc. B 280:20122374. https://doi.org/10.1098/rspb.2012.2374
  14. Cornwall, C. E. & Hurd, C. L. 2016. Experimental design in ocean acidification research: problems and solutions. ICES J. Mar. Sci. 73:572-581. https://doi.org/10.1093/icesjms/fsv118
  15. Dai, L., Geng, H. -X., Yu, R. -C., Liu, Y., Zhao, J. -Y., Wang, J. -X., Zhang, Q. -C., Kong, F. -Z. & Zhou, M. -J. 2020. Distribution of Alexandrium pacificum cysts in the area adjacent to the Changjiang River estuary, China. Mar. Pollut. Bull. 156:111206. https://doi.org/10.1016/j.marpolbul.2020.111206
  16. Ding, D., Xing, J., Wang, S., Chang, X. & Hao, J. 2019. Impacts of emissions and meteorological changes on China's ozone pollution in the warm seasons of 2013 and 2017. Front. Environ. Sci. Eng. 13:76. https://doi.org/10.1007/s11783-019-1160-1
  17. Doney, S. C., Balch, W. M., Fabry, V. J. & Feely, R. A. 2009. Ocean acidification: a critical emerging problem for the ocean sciences. Oceanography 22:16-25.
  18. Farrell, A. P. 2009. Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J. Exp. Biol. 212:3771-3780. https://doi.org/10.1242/jeb.023671
  19. Feng, Y., Hare, C. E., Leblanc, K., Rose, J. M., Zhang, Y., DiTullio, G. R., Lee, P. A., Wilhelm, S. W., Rowe, J. M., Sun, J., Nemcek, N., Gueguen, C., Passow, U., Benner, I., Brown, C. & Hutchins, D. A. 2009. Effects of increased pCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Mar. Ecol. Prog. Ser. 388:13-25. https://doi.org/10.3354/meps08133
  20. Fraga, S., Gallager, S. M. & Anderson, D. M. 1989. Chain-forming dinoflagellates: an adaptation to red tides. In Okaichi, T., Anderson, D. M. & Nemoto, T. (Eds.) Red Tides: Biology, Environmental Science, and Toxicology. Elsevie, Amsterdam, pp. 281-284.
  21. Fu, F. X., Tatters, A. O. & Hutchins, D. A. 2012. Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser. 470:207-233. https://doi.org/10.3354/meps10047
  22. Fu, F. -X., Zhang, Y., Warner, M. E., Feng, Y., Sun, J. & Hutchins, D. A. 2008. A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7:76-90. https://doi.org/10.1016/j.hal.2007.05.006
  23. Gao, G., Liu, Y., Li, X., Feng, Z. & Xu, J. 2016. An ocean acidification acclimatised green tide alga is robust to changes of seawater carbon chemistry but vulnerable to light stress. PLoS ONE 11:e0169040. https://doi.org/10.1371/journal.pone.0169040
  24. Gao, K., Zhang, Y. & Hader, D. -P. 2018. Individual and interactive effects of ocean acidification, global warming, and UV radiation on phytoplankton. J. Appl. Phycol. 30:743-759. https://doi.org/10.1007/s10811-017-1329-6
  25. Gattuso, J. -P., Magnan, A., Bille, R., Cheung, W. W. L., Howes, E. L., Joos, F., Allemand, D., Bopp, L., Cooley, S. R., Eakin, C. M., Hoegh-Guldberg, O., Kelly, R. P., Portner, H. -O., Rogers, A. D., Baxer, J. M., Laffoley, D., Osborna, D., Rankovic, A., Rochette, J., Sumaila, U. R., Treyer, S. & Turley, C. 2015. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349:aac4722. https://doi.org/10.1126/science.aac4722
  26. Genovesi, B., Berrebi, P., Nagai, S., Reynaud, N., Wang, J. & Masseret, E. 2015. Geographic structure evidenced in the toxic dinoflagellate Alexandrium pacificum Litaker (A. catenella-group IV (Whedon & Kofoid) Balech) along Japanese and Chinese coastal waters. Mar. Pollut. Bull. 98:95-105. https://doi.org/10.1016/j.marpolbul.2015.07.009
  27. Genty, B., Briantais, J. -M. & Baker, N. R. 1989. The relationship between the quantum yield of photosynthesis electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta Gen. Subj. 990:87-92. https://doi.org/10.1016/S0304-4165(89)80016-9
  28. Guinotte, J. M. & Fabry, V. J. 2008. Ocean acidification and its potential effects on marine ecosystems. Ann. N. Y. Acad. Sci. 1134:320-342. https://doi.org/10.1196/annals.1439.013
  29. Guiry, M. D. & Guiry, G. M. 2021. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: https://www.algaebase.org. Accessed Jan 14, 2021.
  30. Hattenrath-Lehmann, T. K., Smith, J. L., Wallace, R. B., Merlo, L., Koch, F., Mittelsdorf, H., Goleski, J. A., Anderson, D. M. & Gobler, C. J. 2015. The effects of elevated CO2 on the growth and toxicity of field populations and cultures of the saxitoxin-producing dinoflagellate, Alexandrium fundyense. Limnol. Oceanogr. 60:198-214. https://doi.org/10.1002/lno.10012
  31. He, Q. & Silliman, B. R. 2019. Climate change, human impacts, and coastal ecosystems in the Anthropocene. Curr. Biol. 29:R1021-R1035. https://doi.org/10.1016/j.cub.2019.08.042
  32. Hennon, G. M. M., Hernandez Limon, M. D., Haley, S. T., Juhl, A. R. & Dyhrman, S. T. 2017. Diverse CO2-induced responses in physiology and gene expression among eukaryotic phytoplankton. Front. Microbiol. 8:2547. https://doi.org/10.3389/fmicb.2017.02547
  33. Hurd, C. L., Hepburn, C. D., Currie, K. I., Raven, J. A. & Hunter, K. A. 2009. Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. J. Phycol. 45:1236-1251. https://doi.org/10.1111/j.1529-8817.2009.00768.x
  34. Hutchins, D. A. & Fu, F. 2017. Microorganisms and ocean global change. Nat. Microbiol. 2:17058. https://doi.org/10.1038/nmicrobiol.2017.58
  35. Iglesias-Rodriguez, M. D., Halloran, P. R., Rickaby, R. E. M., Hall, I. R., Colmenero-Hidalgo, E., Gittins, J. R., Green, D. R. H., Tyrrell, T., Gibbs, S. J., von Dassow, P., Rehm, E., Armbrust, E. V. & Boessenkool, K. P. 2008. Phytoplankton calcification in a high-CO2 world. Science 320:336-340. https://doi.org/10.1126/science.1154122
  36. Jang, S. H. & Jeong, H. J. 2020. Spatio-temporal distributions of the newly described mixotrophic dinoflagellate Yihiella yeosuensis (Suessiaceae) in Korean coastal waters and its grazing impact on prey populations. Algae 35:45-59. https://doi.org/10.4490/algae.2020.35.2.24
  37. Ji, X., Verspagen, J. M. H., Stomp, M. & Huisman, J. 2017. Competition between cyanobacteria and green algae at low versus elevated CO2: who will win, and why? J. Exp. Bot. 68:3815-3828. https://doi.org/10.1093/jxb/erx027
  38. Joint, I., Doney, S. C. & Karl, D. M. 2011. Will ocean acidification affect marine microbes? ISME J. 5:1-7. https://doi.org/10.1038/ismej.2010.79
  39. Kang, H. C., Jeong, H. J., Jang, S. H. & Lee, K. H. 2019a. Feeding by common heterotrophic protists on the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) compared to that of other suessioid dinoflagellates. Algae 34:127-140. https://doi.org/10.4490/algae.2019.34.5.29
  40. Kang, H. C., Jeong, H. J., Lim, A. S., Ok, J. H., You, J. H., Park, S. A., Lee, S. Y. & Eom, S. H. 2020. Effects of temperature on the growth and ingestion rates of the newly described mixotrophic dinoflagellate Yihiella yeosuensis and its two optimal prey species. Algae 35:263-275. https://doi.org/10.4490/algae.2020.35.8.20
  41. Kang, H. C., Jeong, H. J., Ok, J. H., You, J. H., Jang, S. H., Lee, S. Y., Lee, K. H., Park, J. Y. & Rho, J. -R. 2019b. Spatial and seasonal distributions of the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) in Korea: quantification using qPCR. Algae 34:111-126. https://doi.org/10.4490/algae.2019.34.5.25
  42. Kim, H. M., Jo, J., Park, C., Choi, B. -J., Lee, H. -G. & Kim, K. Y. 2019. Epibionts associated with floating Sargassum horneri in the Korea Strait. Algae 34:303-313. https://doi.org/10.4490/algae.2019.34.12.10
  43. Kim, J. -H., Kim, K. Y., Kang, E. J., Lee, K., Kim, J. -M., Park, K. -T., Shin, K., Hyun, B. & Jeong, H. J. 2013. Enhancement of photosynthetic carbon assimilation efficiency by phytoplankton in the future coastal ocean. Biogeosciences 10:7525-7535. https://doi.org/10.5194/bg-10-7525-2013
  44. Kim, J. -M., Lee, K., Han, I. -S., Lee, J. -S., Choi, Y. -H., Lee, J. H. & Moon, J. -Y. 2020. Anthropogenic nitrogen-induced changes in seasonal carbonate dynamics in a productive coastal environment. Geophys. Res. Lett. 47:e2020GL088232.
  45. Kim, S. -Y., Lee, Y. -H., Kim, Y. -S., Shim, J. -H., Ye, M. -J., Jeon, J. -W., Hwang, J. -R. & Jeon, S. -H. 2012. Characteristics of marine environmental in the hypoxic season at Jinhae Bay in 2010. Korean J. Nat. Conserv. 6:115-129. https://doi.org/10.11624/KJNC.2012.6.2.115
  46. Kottmeier, D. M., Rokitta, S. D. & Rost, B. 2016. H+-driven increase in CO2 uptake and decrease in HCO3- uptake explain coccolithophores' acclimation responses to ocean acidification. Limnol. Oceanogr. 61:2045-2057. https://doi.org/10.1002/lno.10352
  47. Kroeker, K. J., Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L., Singh, G. S., Duarte, C. M. & Gattuso, J. -P. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19:1884-1896. https://doi.org/10.1111/gcb.12179
  48. Kruk, C., Piccini, C., Devercelli, M., Nogueira, L., Accattatis, V., Sampognaro, L. & Segura, A. M. 2021. A trait-based approach predicting community assembly and dominance of microbial invasive species. Oikos 130:571-586. https://doi.org/10.1111/oik.07694
  49. Laws, E. A., Bidigare, R. R. & Popp, B. N. 1997. Effect of growth rate and CO2 concentration on carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum. Limnol. Oceanogr. 42:1552-1560. https://doi.org/10.4319/lo.1997.42.7.1552
  50. Lee, H. -G., Kim, H. M., Min, J., Park, C., Jeong, H. J., Lee, K. & Kim, K. Y. 2020a. Quantification of the paralytic shellfish poisoning dinoflagellate Alexandrium species using a digital PCR. Harmful Algae 92:101726. https://doi.org/10.1016/j.hal.2019.101726
  51. Lee, K. H., Jeong, H. J., Kang, H. C., Ok, J. H., You, J. H. & Park, S. A. 2019a. Growth rates and nitrate uptake of co-occurring red-tide dinoflagellates Alexandrium affine and A. fraterculus as a function of nitrate concentration under light-dark and continuous light conditions. Algae 34:237-251. https://doi.org/10.4490/algae.2019.34.8.28
  52. Lee, S. Y., Jeong, H. J., Kwon, J. E., You, J. H., Kim, S. J., Ok, J. H., Kang, H. C. & Park, J. Y. 2019b. First report of the photosynthetic dinoflagellate Heterocapsa minima in the Pacific Ocean: morphological and genetic characterizations and the nationwide distribution in Korea. Algae 34:7-21. https://doi.org/10.4490/algae.2019.34.2.28
  53. Lee, S. Y., Jeong, H. J., Ok, J. H., Kang, H. C. & You, J. H., 2020b. Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters. Algae 35:225-236. https://doi.org/10.4490/algae.2020.35.8.25
  54. Lewis, E. R. & Wallace, D. W. R. 1998. Program developed for CO2 system calculations. Carbon Dioxide Information Center. Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, 38 pp.
  55. Lim, A. S., Jeong, H. J. & Ok, J. H. 2019. Five Alexandrium species lacking mixotrophic ability. Algae 34:289-301. https://doi.org/10.4490/algae.2019.34.11.21
  56. Lim, M. H., Lee, C. H., Min, J., Lee, H. -G. & Kim, K. Y. 2020. Effect of elevated pCO2 on thermal performance of Chattonella marina and Chattonella ovata (Raphidophyceae). Algae 35:375-388. https://doi.org/10.4490/algae.2020.35.12.8
  57. Listmann, L., LeRoch, M., Schluter, L., Thomas, M. K. & Reusch, T. B. H. 2016. Swift thermal reaction norm evolution in a key marine phytoplankton species. Evol. Appl. 9:1156-1164. https://doi.org/10.1111/eva.12362
  58. Lovecchio, S., Climent, E., Stocker, R. & Durham, W. M. 2019. Chain formation can enhance the vertical migration of phytoplankton through turbulence. Sci. Adv. 5:eaaw7879. https://doi.org/10.1126/sciadv.aaw7879
  59. Maugendre, L., Gattuso, J. -P., Louis, J., De Kluijver, A., Marro, S., Soetaert, K. & Gazeau, F. 2015. Effect of ocean warming and acidification on a plankton community in the NW Mediterranean Sea. ICES J. Mar. Sci. 72:1744-1755. https://doi.org/10.1093/icesjms/fsu161
  60. Millero, F. J., Zhang, J. -Z., Lee, K. & Campbell, D. M. 1993. Titration alkalinity of seawater. Mar. Chem. 44:153-165. https://doi.org/10.1016/0304-4203(93)90200-8
  61. NOAA/GML (ESRL's Global Monitoring Laboratory of the National Oceanic and Atmospheric Administration). 2021. Trends in atmospheric carbon dioxide. Available from: https://gml.noaa.gov/ccgg/trends/. Accessed Sep 30, 2021.
  62. NOAA/NCEI (National Centers for Environmental Information of the National Oceanic and Atmospheric Administration). 2021. Global climate report. Available from: https://www.ncdc.noaa.gov/sotc/global/. Accessed Sep 30, 2021.
  63. O'Donnell, D. R., Hamman, C. R., Johnson, E. C., Kremer, C. T., Klausmeier, C. A. & Litchman, E. 2018. Rapid thermal adaptation in a marine diatom reveals constraints and trade-offs. Glob. Change Biol. 24:4554-4565. https://doi.org/10.1111/gcb.14360
  64. Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R. M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R. G., Plattner, G. -K., Rodgers, K. B., Sabine, C. L., Sarmiento, J. L., Schlitzer, R., Slater, R. D., Totterdell, I. J., Weirig, M. -F., Yamanaka, Y. & Yool, A. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681-686. https://doi.org/10.1038/nature04095
  65. Pahlow, M., Riebesell, U. & Wolf-Gladrow, D. A. 1997. Impact of cell shape and chain formation on nutrient acquisition by marine diatoms. Limnol. Oceanogr. 42:1660-1672. https://doi.org/10.4319/lo.1997.42.8.1660
  66. Pang, M., Xu, J., Qu, P., Mao, X., Wu, Z., Xin, M., Sun, P., Wang, Z., Zhang, X. & Chen, H. 2017. Effect of CO2 on growth and toxicity of Alexandrium tamarense from the East China Sea, a major producer of paralytic shellfish toxins. Harmful Algae 68:240-247. https://doi.org/10.1016/j.hal.2017.08.008
  67. Paul, C., Sommer, U., Garzke, J., Moustaka-Gouni, M., Paul, A. & Matthiessen, B. 2016. Effects of increased CO2 concentration on nutrient limited coastal summer plankton depend on temperature. Limnol. Oceanogr. 61:853-868. https://doi.org/10.1002/lno.10256
  68. Portner, H. -O., Bock, C. & Mark, F. C. 2017. Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology. J. Exp. Biol. 220:2685-2696. https://doi.org/10.1242/jeb.134585
  69. Raven, J. A., Beardall, J. & Sanchez-Baracaldo, P. 2017. The possible evolution and future of CO2-concentrating mechanisms. J. Exp. Bot. 68:3701-3716. https://doi.org/10.1093/jxb/erx110
  70. Reinfelder, J. R. 2011. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Ann. Rrev. Mar. Sci. 3:291-315. https://doi.org/10.1146/annurev-marine-120709-142720
  71. Reusch, T. B. H. & Boyd, P. W. 2013. Experimental evolution meets marine phytoplankton. Evolution 67:1849-1859. https://doi.org/10.1111/evo.12035
  72. Riebesell, U. & Gattuso, J. -P. 2015. Lessons learned from ocean acidification research. Nat. Clim. Chang. 5:12-14. https://doi.org/10.1038/nclimate2456
  73. Rosso, L., Lobry, J. R. & Flandrois, J. P. 1993. An unexpected correlation between cardinal temperatures of microbial growth highlighted by a new model. J. Theor. Biol. 162:447-463. https://doi.org/10.1006/jtbi.1993.1099
  74. Rost, B., Zondervan, I. & Wolf-Gladrow, D. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar. Ecol. Prog. Ser. 373:227-237. https://doi.org/10.3354/meps07776
  75. Ryan, J. P., McManus, M. A. & Sullivan, J. M. 2010. Interacting physical, chemical and biological forcing of phytoplankton thin-layer variability in Monterey Bay, California. Cont. Shelf Res. 30:7-16. https://doi.org/10.1016/j.csr.2009.10.017
  76. Selander, E., Jakobsen, H. H., Lombard, F. & Kiorboe, T. 2011. Grazer cues induce stealth behavior in marine dinoflagellates. Proc. Natl. Acad. Sci. U. S. A. 108:4030-4034. https://doi.org/10.1073/pnas.1011870108
  77. Shin, H. H., Li, Z., Kim, E. S., Park, J. -W. & Lim, W. A. 2017. Which species, Alexandrium catenella (Group I) or A. pacificum (Group IV), is really responsible for past paralytic shellfish poisoning outbreaks in Jinhae-Masan Bay, Korea? Harmful Algae 68:31-39. https://doi.org/10.1016/j.hal.2017.07.006
  78. Smayda, T. J. 2010. Adaptations and selection of harmful and other dinoflagellate species in upwelling systems. 2. Motility and migratory behaviour. Prog. Oceanogr. 85:71-91. https://doi.org/10.1016/j.pocean.2010.02.005
  79. Sobrino, C., Ward, M. L. & Neale, P. J. 2008. Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol. Oceanogr. 53:494-505. https://doi.org/10.4319/lo.2008.53.2.0494
  80. van de Poll, W. H., Abdullah, E., Visser, R. J. W., Fischer, P. & Buma, A. G. J. 2020. Taxon-specific dark survival of diatoms and flagellates affects Arctic phytoplankton composition during the polar night and early spring. Limnol. Oceanogr. 65:903-914. https://doi.org/10.1002/lno.11355
  81. van de Waal, D. B., Brandenburg, K. M., Keuskamp, J., Trimborn, S., Rokitta, S., Kranz, S. A. & Rost, B. 2019. Highest plasticity of carbon-concentrating mechanisms in earliest evolved phytoplankton. Limnol. Oceanogr. Lett. 4:37-43. https://doi.org/10.1002/lol2.10102
  82. Xu, Z., Gao, G., Xu, J. & Wu, H. 2017. Physiological response of a golden tide alga (Sargassum muticum) to the interaction of ocean acidification and phosphorus enrichment. Biogeosciences 14:671-681. https://doi.org/10.5194/bg-14-671-2017
  83. You, J. H., Jeong, H. J., Kang, H. C., Ok, J. H., Park, S. A. & Lim, A. S. 2020. Feeding by common heterotrophic protist predators on seven Prorocentrum species. Algae 35:61-78. https://doi.org/10.4490/algae.2020.35.2.28
  84. Zeebe, R. E., Zachos, J. C., Caldeira, K. & Tyrrell, T. 2008. Carbon emissions and acidification. Science 321:51-52. https://doi.org/10.1126/science.1159124
  85. Zunino, S., Libralato, S., Canu, D. M., Prato, G. & Solidoro, C. 2021. Impact of ocean acidification on ecosystem functioning and services in habitat-forming species and marine ecosystems. Ecosystems 24:1561-1575. https://doi.org/10.1007/s10021-021-00601-3