DOI QR코드

DOI QR Code

Differential responses of diatom and phototrophic dinoflagellate species to five oxygen concentrations: growth, photosynthesis, and respiration rates

  • Se Hee Eom (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Hae Jin Jeong (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Ji Hyun You (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Sang Ah Park (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Minji Kwon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2026.01.15
  • Accepted : 2026.05.26
  • Published : 2026.06.19

Abstract

While phytoplankton are a major component of coastal ecosystems and experience a wide range of oxygen conditions, the survival and physiological responses of common phytoplankton species under hypoxia remain insufficiently understood. To explore these effects, cell densities of the two dinoflagellate species Prorocentrum triestinum and Amphidinium carterae, and the two diatom species Cylindrotheca closterium and Chaetoceros curvisetus-isolated from waters with a dissolved oxygen (DO) concentration of 1.5 mg O2 L-1-were measured under target DO concentrations of 0.5, 1.0, 1.5, 4.0, and >7.0 mg O2 L-1. Using these data, the growth rate, net photosynthesis rate, and dark respiration rate of each species were determined. While A. carterae, Cy. closterium, and Ch. curvisetus survived at all tested DO concentrations, P. triestinum survived only at ≥1.0 mg O2 L-1. The two dinoflagellate species examined here, which possess active swimming ability, exhibited the highest growth rates at >7.0 mg O2 L-1, whereas the two diatom species examined here showed peak growth rate at 1.5 mg O2 L-1. Net photosynthesis rates of all four species peaked at 1.5 mg O2 L-1, while dark respiration rates were highest at >7.0 mg O2 L-1. These findings suggest that although these phytoplankton species can grow under hypoxic conditions, dinoflagellate species achieve maximal growth at higher oxygen concentrations, possibly due to the energetic demands of motility. This study provides a useful basis for understanding species-specific responses of phytoplankton to varying oxygen conditions in coastal environments.

Keywords

Acknowledgement

This research was supported by the National Research Foundation (NRF) funded by the Ministry of Science and ICT (RS-2026-25548794) award to Hae Jin Jeong.

References

  1. Abdel-Tawwab, M., Monier, M. N., Hoseinifar, S. H. & Faggio, C. 2019. Fish response to hypoxia stress: growth, physiological, and immunological biomarkers. Fish Physiol. Biochem. 45:997–1013. doi.org/10.1007/s10695-019-00614-9
  2. Anneville, O., Dur, G., Rimet, F. & Souissi, S. 2018. Plasticity in phytoplankton annual periodicity: an adaptation to longterm environmental changes. Hydrobiologia 824:121–141. doi.org/10.1007/s10750-017-3412-z
  3. Apoya-Horton, M. D., Yin, L., Underwood, G. J. C. & Gretz, M. R. 2006. Movement modalities and responses to environmental changes of the mudflat diatom Cylindrotheca closterium (Bacillariophyceae). J. Phycol. 42:379–390. doi.org/10.1111/j.1529-8817.2006.00194.x
  4. Baig, H. S., Saifullah, S. M. & Dar, A. 2006. Occurrence and toxicity of Amphidinium carterae Hulburt in the North Arabian Sea. Harmful Algae 5:133–140. doi.org/10.1016/j.hal.2005.06.010
  5. Banti, V., Giuntoli, B., Gonzali, S., et al. 2013. Low oxygen response mechanisms in green organisms. Int. J. Mol. Sci. 14:4734–4761. doi.org/10.3390/ijms14034734
  6. Batziakas, S., Frangoulis, C., Tsiola, A., Nikolioudakis, N., Tsagaraki, T. M. & Somarakis, S. 2020. Hypoxia changes the shape of the biomass size spectrum of planktonic communities: a case study in the eastern Mediterranean (Elefsina Bay). J. Plankton Res. 42:752–766. doi.org/10.1093/plankt/fbaa055
  7. 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. doi.org/10.1007/s00227-019-3528-y
  8. Breitburg, D., Levin, L. A., Oschlies, A., et al. 2018. Declining oxygen in the global ocean and coastal waters. Science 359:eaam7240. doi.org/10.1126/science.aam7240
  9. Burlacot, A. & Peltier, G. 2023. Energy crosstalk between photosynthesis and the algal CO2-concentrating mechanisms. Trends Plant Sci. 28:795–807. doi.org/10.1016/j.tplants.2023.03.018
  10. Chabot, D. & Dutil, J.-D. 1999. Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J. Fish Biol. 55:472–491. doi.org/10.1111/j.1095-8649.1999.tb00693.x
  11. Chen, B., Liu, J., Song, H., Xu, G., Zhao, W. & Li, G. 2024. Decreasing available O2 interacts with light to alter the growth and fatty acid content in a marine diatom. Environ. Exp. Bot. 220:105667. doi.org/10.1016/j.envexpbot.2024.105667
  12. Chen, B., Liu, J., Xu, G. & Li, G. 2021. Lowering pO2 interacts with photoperiod to alter physiological performance of the coastal diatom Thalassiosira pseudonana. Microorganisms 9:2541. doi.org/10.3390/microorganisms9122541
  13. Chen, B., Song, H., Xu, G., Ji, H., Yang, X. & Li, G. 2025. Hypoxia lowers cell carbon and nitrogen content and accelerates sinking of a marine diatom Thalassiosira pseudonana. Front. Mar. Sci. 12:1529163. doi.org/10.3389/fmars.2025.1529163
  14. Chen, C.-C., Gong, G.-C. & Shiah, F.-K. 2007. Hypoxia in the East China Sea: one of the largest coastal low-oxygen areas in the world. Mar. Environ. Res. 64:399–408. doi.org/10.1016/j.marenvres.2007.01.007
  15. Cockroft, A. C., Schoeman, D. S., Pitcher, G. C., Bailey, G. W. & van Zyl, D. L. 2000. A mass stranding, or 'walk out' of west coast rock lobster, Jasus lalandii, in Elands Bay, South Africa: causes, results and applications. In von Kaupel Klein, J. C. & Schram, F. R. (Eds.) The Biodiversity Crises and Crustaceans, Crustacean Issues. Balkema, Rotterdam, pp. 673–688.
  16. Crawford, D. W. 1992. Metabolic cost of motility in planktonic protists: theoretical considerations on size scaling and swimming speed. Microb. Ecol. 24:1–10. doi.org/10.1007/BF00171966
  17. De Luca, D., Kooistra, W. H. C. F., Sarno, D., Gaonkar, C. C. & Piredda, R. 2019. Global distribution and diversity of Chaetoceros (Bacillariophyta, Mediophyceae): integration of classical and novel strategies. PeerJ 7:e7410. doi.org/10.7717/peerj.7410
  18. Diaz, R. J. & Rosenberg, R. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33:245–303.
  19. Diaz, R. J. & Rosenberg, R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926–929. doi.org/10.1126/science.1156401
  20. Edwards, K. F., Thomas, M. K., Klausmeier, C. A. & Litchman, E. 2016. Phytoplankton growth and the interaction of light and temperature: a synthesis at the species and community level. Limnol. Oceanogr. 61:1232–1244. doi.org/10.1002/lno.10282
  21. Eom, S. H., Jeong, H. J., Ok, J. H., et al. 2021. Interactions between common heterotrophic protists and the dinoflagellate Tripos furca: implication on the long duration of its red tides in the South Sea of Korea in 2020. Algae 36:25–36. doi.org/10.4490/algae.2021.36.2.22
  22. Eom, S. H., Jeong, H. J., Ok, J. H., Park, S. A., Kang, H. C. & You, J. H. 2024. Combined effects of hypoxia and starvation on the survival and growth rates of autotrophic, mixotrophic, and heterotrophic dinoflagellates. Mar. Biol. 171:42. doi.org/10.1007/s00227-023-04363-5
  23. Eom, S. H., Ok, J. H., You, J. H., et al. 2025. Temporal changes in the structure of protist communities incubated under normoxic and hypoxic conditions: a metabarcoding analysis. Algae 40:127–146. doi.org/10.4490/algae.2025.40.4.18
  24. Fenchel, T. 1988. Marine plankton food chains. Annu. Rev. Ecol. Syst. 19:19–38. doi.org/10.1146/annurev.es.19.110188.000315
  25. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240. doi.org/10.1126/science.281.5374.237
  26. Flynn, K. J. & Skibinski, D. O. 2020. Exploring evolution of maximum growth rates in plankton. J. Plankton Res. 42:497–513. doi.org/10.1093/plankt/fbaa038
  27. Forbes, T. L. & Lopez, G. R. 1990. The effect of food concentration, body size, and environmental oxygen tension on the growth of the deposit-feeding polycheate, Capitella species. Limnol. Oceanogr. 35:1535–1544. doi.org/10.4319/lo.1990.35.7.1535
  28. Galic, N., Hawkins, T. & Forbes, V. E. 2019. Adverse impacts of hypoxia on aquatic invertebrates: a meta-analysis. Sci. Total Environ. 652:736–743. doi.org/10.1016/j.scitotenv.2018.10.225
  29. Gao, K. 2021. Approaches and involved principles to control pH/pCO2 stability in algal cultures. J. Appl. Phycol. 33:3497–3505. doi.org/10.1007/s10811-021-02585-y
  30. Gao, K. & Campbell, D. A. 2014. Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Funct. Plant Biol. 41:449–459. doi.org/10.1071/FP13247
  31. Gao, S., Edmundson, S. & Huesemann, M. 2022. Oxygen stress mitigation for microalgal biomass productivity improvement in outdoor raceway ponds. Algal Res. 68:102901. doi.org/10.1016/j.algal.2022.102901
  32. Gilbert, D., Rabalais, N. N., Díaz, R. J. & Zhang, J. 2010. Evidence for greater oxygen decline rates in the coastal ocean than in the open ocean. Biogeosciences 7:2283–2296. doi.org/10.5194/bg-7-2283-2010
  33. Graham, A. M. & Barreto, F. S. 2019. Loss of the HIF pathway in a widely distributed intertidal crustacean, the copepod Tigriopus californicus. Proc. Natl. Acad. Sci. U. S. A. 116:12913–12918. doi.org/10.1073/pnas.1819874116
  34. Grantham, B. A., Chan, F., Nielsen, K. J., et al. 2004. Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429:749–754. doi.org/10.1038/nature02605
  35. Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8:229–239. doi.org/10.1139/m62-029
  36. Harris, J. O., Maguire, G. B., Edwards, S. J. & Johns, D. R. 1999. Low dissolved oxygen reduces growth rate and oxygen consumption rate of juvenile greenlip abalone, Haliotis laevigata Donovan. Aquaculture 174:265–278. doi.org/10.1016/S0044-8486(99)00022-8
  37. Intarasit, S. & Inwongwan, S. 2026. Coordinating photosynthesis and respiration: evolution and functional integration of mitochondria and chloroplasts in algae. Plant Physiol. 200:kiag054. doi.org/10.1093/plphys/kiag054
  38. Jacobson, D. M. & Anderson, D. M. 1986. Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J. Phycol. 22:249–258. doi.org/10.1111/j.1529-8817.1986.tb00021.x
  39. Jeong, H. J., Kang, H. C., Lim, A. S., et al. 2021. Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance. Sci. Adv. 7:eabe4214. doi.org/10.1126/sciadv.abe4214
  40. Jeong, H. J., Kang, H., Shim, J. H., et al. 2001. Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp. Mar. Ecol. Prog. Ser. 218:77–86. doi.org/10.3354/meps218077
  41. Kang, H. C., Jeong, H. J., Park, S. A., et al. 2020. Feeding by the newly described heterotrophic dinoflagellate Gyrodinium jinhaense: comparison with G. dominans and G. moestrupii. Mar. Biol. 167:156. doi.org/10.1007/s00227-020-03769-9
  42. Kitaya, Y., Xiao, L., Masuda, A., Ozawa, T., Tsuda, M. & Omasa, K. 2008. Effects of temperature, photosynthetic photon flux density, photoperiod and O2 and CO2 concentrations on growth rates of the symbiotic dinoflagellate, Amphidinium sp. J. Appl. Phycol. 20:737–742. doi.org/10.1007/s10811-008-9331-7
  43. Kruskal, W. H. & Wallis, W. A. 1952. Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47:583–621. doi.org/10.1080/01621459.1952.10483441
  44. Langdon, C. 1993. The significance of respiration in production measurements based on oxygen. ICES Mar. Sci. Symp. 197:69–78.
  45. Levin, L. A., Ekau, W., Gooday, A. J., et al. 2009. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6:2063–2098. doi.org/10.5194/bg-6-2063-2009
  46. Li, Z., Song, S., Li, C. & Yu, Z. 2018. The sinking of the phytoplankton community and its contribution to seasonal hypoxia in the Changjiang (Yangtze River) estuary and its adjacent waters. Estuar. Coast. Shelf Sci. 208:170–179. doi.org/10.1016/j.ecss.2018.05.007
  47. Lobus, N. V. & Kulikovskiy, M. S. 2023. The co-evolution aspects of the biogeochemical role of phytoplankton in aquatic ecosystems: a review. Biology 12:92. doi.org/10.3390/biology12010092
  48. López-Sandoval, D. C., Rodríguez-Ramos, T., Cermeño, P., Sobrino, C. & Marañón, E. 2014. Photosynthesis and respiration in marine phytoplankton: relationship with cell size, taxonomic affiliation, and growth phase. J. Exp. Mar. Biol. Ecol. 457:151–159. doi.org/10.1016/j.jembe.2014.04.013
  49. Mann, H. B. & Whitney, D. R. 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18:50–60. doi.org/10.1214/aoms/1177730491
  50. National Institute of Fisheries Science. 2015–2025. Breaking news: hypoxic water mass. National Institute of Fisheries Science, Busan. Available from: https://www.nifs.go.kr/board/actionBoard0056List.do. Accessed Apr 15, 2026 (in Korean).
  51. Naustvoll, L.-J. 2000. Prey size spectra and food preferences in thecate heterotrophic dinoflagellates. Phycologia 39:187–198. doi.org/10.2216/i0031-8884-39-3-187.1
  52. Ok, J. H., Jeong, H. J., Kang, H. C., et al. 2023. Protists in hypoxic waters of Jinhae Bay and Masan Bay, Korea, based on metabarcoding analyses: emphasizing surviving dinoflagellates. Algae 38:265–281. doi.org/10.4490/algae.2023.38.12.6
  53. Orizar, I. D. S. & Lewandowska, A. M. 2025. Interspecific trait variability and plasticity of the Baltic Sea phytoplankton species along a salinity gradient. J. Plankton Res. 47:fbaf015. doi.org/10.1093/plankt/fbaf015
  54. Peng, X., Lin, Q., Liu, B., et al. 2022. Effect of submerged plant coverage on phytoplankton community dynamics and photosynthetic activity in situ. J. Environ. Manage. 301:113822. doi.org/10.1016/j.jenvman.2021.113822
  55. Pierella Karlusich, J. J., Cosnier, K., Zinger, L., et al. 2025. Patterns and drivers of diatom diversity and abundance in the global ocean. Nat. Commun. 16:3452. doi.org/10.1038/s41467-025-58027-7
  56. Pitcher, G. C. & Probyn, T. A. 2016. Suffocating phytoplankton, suffocating waters: red tides and anoxia. Front. Mar. Sci. 3:186. doi.org/10.3389/fmars.2016.00186
  57. Pruder, G. D. & Bolton, E. T. 1980. Differences between cell division and carbon fixation rates associated with light intensity and oxygen concentration: implications in the cultivation of an estuarine diatom. Mar. Biol. 59:1–6. doi.org/10.1007/BF00396976
  58. Rabalais, N. N., Diaz, R. J., Levin, L. A., Turner, R. E., Gilbert, D. & Zhang, J. 2010. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7:585–619. doi.org/10.5194/bg-7-585-2010
  59. Rabalais, N. N., Turner, R. E., Sen Gupta, B. K., Boesch, D. F., Chapman, P. & Murrell, M. C. 2007. Hypoxia in the northern Gulf of Mexico: does the science support the plan to reduce, mitigate, and control hypoxia? Estuaries Coasts 30:753–772. doi.org/10.1007/BF02841332
  60. Raven, J. A. & Larkum, A. W. D. 2007. Are there ecological implications for the proposed energetic restrictions on photosynthetic oxygen evolution at high oxygen concentrations? Photosynth. Res. 94:31–42. doi.org/10.1007/s11120-007-9211-z
  61. Repak, A. J. 1983. Suitability of selected marine algae for growing the marine heterotrich ciliate Fabrea salina. J. Protozool. 30:52–54. doi.org/10.1111/j.1550-7408.1983.tb01032.x
  62. Richmond, C., Marcus, N. H., Sedlacek, C., Miller, G. A. & Oppert, C. 2006. Hypoxia and seasonal temperature: short-term effects and long-term implications for Acartia tonsa Dana. J. Exp. Mar. Biol. Ecol. 328:177–196. doi.org/10.1016/j.jembe.2005.07.004
  63. Rizzo, P. J. 2003. Those amazing dinoflagellate chromosomes. Cell Res. 13:215–217 doi.org/10.1038/sj.cr.7290166
  64. Rocke, E. & Liu, H. 2014. Respiration, growth and grazing rates of three ciliate species in hypoxic conditions. Mar. Pollut. Bull. 85:410–417. doi.org/10.1016/j.marpolbul.2014.04.050
  65. Rocke, E., Jing, H. & Liu, H. 2013. Phylogenetic composition and distribution of picoeukaryotes in the hypoxic northwestern coast of the Gulf of Mexico. MicrobiologyOpen 2:130–143. doi.org/10.1002/mbo3.57
  66. Rodrigues, R. V. & Patil, J. S. 2022. Response of benthic dinoflagellates Amphidinium carterae and Bysmatrum gregarium to salinity changes and prolonged darkness: elucidation through laboratory experiments. Aquat. Ecol. 56:1113–1126. doi.org/10.1007/s10452-022-09960-y
  67. Santoferrara, L. F., McManus, G. B., Greenfield, D. I. & Smith, S. A. 2022. Microbial communities (bacteria, archaea and eukaryotes) in a temperate estuary during seasonal hypoxia. Aquat. Microb. Ecol. 88:61–79. doi.org/10.3354/ame01982
  68. Schmidtko, S., Stramma, L. & Visbeck, M. 2017. Decline in global oceanic oxygen content during the past five decades. Nature 542:335–339. doi.org/10.1038/nature21399
  69. Shi, Z., Liu, K., Zhang, S., Xu, H. & Liu, H. 2019. Spatial distributions of mesozooplankton biomass, community composition and grazing impact in association with hypoxia in the Pearl River estuary. Estuar. Coast. Shelf Sci. 225:106237. doi.org/10.1016/j.ecss.2019.05.019
  70. Sobral, P. & Widdows, J. 1997. Influence of hypoxia and anoxia on the physiological responses of the clam Ruditapes decussatus from southern Portugal. Mar. Biol. 127:455–461. doi.org/10.1007/s002270050033
  71. Staker, R. D. & Bruno, S. F. 1980. Diurnal vertical migration in marine phytoplankton. Bot. Mar. 23:167–172. doi. org/10.1515/botm.1980.23.3.167
  72. Stauffer, B. A., Schnetzer, A., Gellene, A. G., Oberg, C., Sukhatme, G. S. & Caron, D. A. 2013. Effects of an acute hypoxic event on microplankton community structure in a coastal harbor of Southern California. Estuaries Coasts 36:135–148. doi.org/10.1007/s12237-012-9551-6
  73. Stock, W., Vanelslander, B., Rüdiger, F., Sabbe, K., Vyverman, W. & Karsten, U. 2019. Thermal niche differentiation in the benthic diatom Cylindrotheca closterium (Bacillariophyceae) complex. Front. Microbiol. 10:1395. doi.org/10.3389/fmicb.2019.01395
  74. Sun, J.-Z., Wang, T., Huang, R., et al. 2022. Enhancement of diatom growth and phytoplankton productivity with reduced O2 availability is moderated by rising CO2. Commun. Biol. 5:54. doi.org/10.1038/s42003-022-03006-7
  75. Sunrise-Sunset. 2026. Sunrise and sunset times in Tongyeong-si, South Gyeongsangnam-do, South Korea. Available from: https://sunrise-sunset.org/search?location=Tongyeong. Accessed Apr 15, 2026.
  76. Taylor, J. C. & Miller, J. M. 2001. Physiological performance of juvenile southern flounder, Paralichthys lethostigma (Jordan and Gilbert, 1884), in chronic and episodic hypoxia. J. Exp. Mar. Biol. Ecol. 258:195–214. doi.org/10.1016/S0022-0981(01)00215-5
  77. Thomas, L. C., Padmakumar, K. B., Smitha, B. R., Devi, C. R. A., Nandan, S. B. & Sanjeevan, V. N. 2013. Spatio-temporal variation of microphytoplankton in the upwelling system of the south-eastern Arabian Sea during the summer monsoon of 2009. Oceanologia 55:185–204. doi.org/10.5697/oc.55-1.185
  78. Tukey, J. W. 1949. Comparing individual means in the analysis of variance. Biometrics 5:99−114. doi.org/10.2307/3001913
  79. Vaquer-Sunyer, R. & Duarte, C. M., 2008. Thresholds of hypoxia for marine biodiversity. Proc. Natl. Acad. Sci. U. S. A. 105:15452–15457. doi.org/10.1073/pnas.0803833105
  80. Ward, B. A., Dutkiewicz, S., Jahn, O. & Follows, M. J. 2012. A size-structured food-web model for the global ocean. Limnol. Oceanogr. 57:1877–1891. doi.org/10.4319/lo.2012.57.6.18771877
  81. Wei, H., Zhao, L., Zhang, H., Lu, Y., Yang, W. & Song, G. 2021. Summer hypoxia in Bohai Sea caused by changes in phytoplankton community. Anthr. Coasts 4:77–86. doi.org/10.1139/anc-2020-0017
  82. Whitney, M. M. 2022. Observed and projected global warming pressure on coastal hypoxia. Biogeosciences 19:4479–4497. doi.org/10.5194/bg-19-4479-2022
  83. Wong, J. C. Y., Raven, J. A., Aldunate, M., et al. 2023. Do phytoplankton require oxygen to survive? A hypothesis and model synthesis from oxygen minimum zones. Limnol. Oceanogr. 68:1417–1437. doi.org/10.1002/lno.12367
  84. Worden, A. Z., Follows, M. J., Giovannoni, S. J., Wilken, S., Zimmerman, A. E. & Keeling, P. J. 2015. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347:1257594. doi.org/10.1126/science.1257594
  85. Wu, R. S. S., Wo, K. T. & Chiu, J. M. Y. 2012. Effects of hypoxia on growth of the diatom Skeletonema costatum. J. Exp. Mar. Biol. Ecol. 420–421:65–68. doi.org/10.1016/j.jembe.2012.04.003
  86. 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. doi.org/10.4490/algae.2020.35.2.28
  87. Zaitsev, Y. P. 1992. Recent changes in the trophic structure of the Black Sea. Fish. Oceanogr. 1:180–189. doi.org/10.1111/j.1365-2419.1992.tb00036.x
  88. Zhao, P., Wu, Q., Xia, X., et al. 2022. Metabolomic and proteomic responses of Phaeodactylum tricornutum to hypoxia. J. Ocean. Limnol. 40:1963–1973. doi.org/10.1007/s00343-021-1232-5
  89. Zhu, Z.-Y., Hu, J., Song, G.-D., Wu, Y., Zhang, J. & Liu, S.-M. 2016. Phytoplankton-driven dark plankton respiration in the hypoxic zone off the Changjiang Estuary, revealed by in vitro incubations. J. Mar. Syst. 154:50–56. doi.org/10.1016/j.jmarsys.2015.04.009