ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Effect of elevated pCO2 on thermal performance of Chattonella marina and Chattonella ovata (Raphidophyceae)

  • Lim, Myeong Hwan (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • 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 : 2020.10.03
  • Accepted : 2020.12.08
  • Published : 2020.12.15
Download PDF
⟨ Previous Next ⟩

Abstract

Ocean acidification and warming, identified as environmental concerns likely to be affected by climate change, are crucial determinants of algal growth. The ichthyotoxic raphidophytes Chattonella species are responsible for huge economic losses and environmental impact worldwide. In this study, we investigated the impact of CO2 on the thermal performance curves (TPCs) of Chattonella marina and Chattonella ovata grown under temperatures ranging from 13 to 34℃ under ambient pCO2 (350 μatm) and elevated pCO2 (950 μatm). TPCs were comparable between the species or even between pCO2 levels. With the exception of the critical thermal minimum (CTmin) for C. ovata, CTmin for C. marina and the thermal optimum (Topt) and critical thermal maximum (CTmax) for both species did not change with elevation of pCO2 levels. While CO2 enrichment increased the maximum photosynthetic rates (Pmax) up to 125% at the Totp of 30℃, specific growth rates were not significantly different under elevated pCO2 for the two species. Overall, C. ovata is likely to benefit from climate change, potentially widening its range of thermal tolerance limit in highly acidic waters and contributing to prolonged phenology of future phytoplankton assemblages in coastal waters.

Keywords

Acknowledgement

We would like to thank Professor Hae Jin Jeong for kindly offering Chattonella ovata strain and the Culture Collection of KIOST for providing Chattonella marina strain. This research was supported by a National Research Foundation (NRF) grant funded by the Korean government (MSIT) (NRF-2016R1A6A1A03012647, NRF-2020R1A2C3005053) to K.Y.K.

References

  1. Allakhverdiev, S. I., Kreslavski, V. D., Klimov, V. V., Los, D. A., Carpentier, R. & Mohanty, P. 2008. Heat stress: an overview of molecular responses in photosynthesis. Photosynth. Res. 98:541-550. https://doi.org/10.1007/s11120-008-9331-0
  2. Angilletta, M. J. Jr. 2006. Estimating and comparing thermal performance curves. J. Therm. Biol. 31:541-545. https://doi.org/10.1016/j.jtherbio.2006.06.002
  3. Beardall, J., Stojkovic, S. & Larsen, S. 2009. Living in a high CO2 world: impacts of global climate change on marine phytoplankton. Plant Ecol. Divers. 2:191-205. https://doi.org/10.1080/17550870903271363
  4. Bernhardt, J. R., Sunday, J. M., Thompson, P. L. & O'Connor, M. I. 2018. Nonlinear averaging of thermal experience predicts population growth rates in a thermally variable environment. Proc. R. Soc. B 285:20181076.
  5. Bestion, E., Schaum, C. E. & Yvon-Durocher, G. 2018. Nutrient limitation constrains thermal tolerance in freshwater phytoplankton. Limnol. Oceanogr. Lett. 3:436-443. https://doi.org/10.1002/lol2.10096
  6. Boatman, T. G., Lawson, T. & Geider, R. J. 2017. A key marine diazotroph in a changing ocean: the interacting effects of temperature, CO2 and light on the growth of Trichodesmium erythraeum IMS101. PLoS ONE 12:e0168796. https://doi.org/10.1371/journal.pone.0168796
  7. Boyd, P. W., Rynearson, T. A., Armstrong, E. A., Fu, F., Hayashi, K., Hu, Z., Hutchins, D. A., Kudela, R. M., Litchman, E., Mulholland, M. R., Passow, U., Strzepek, R. F., Whittaker, K. A., Yu, E. & Thomas, M. K. 2013. Marine phytoplankton temperature versus growth responses from polar to tropical waters: outcome of a scientific communitywide study. PLoS ONE 8:e63091. https://doi.org/10.1371/journal.pone.0063091
  8. Brandenburg, K. M., Velthuis, M. & Van de Waal, D. B. 2019. Meta-analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels. Glob. Chang. Biol. 25:2607-2618. https://doi.org/10.1111/gcb.14678
  9. Clusella-Trullas, S., Blackburn, T. M. & Chown, S. L. 2011. Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am. Nat. 177:738-751. https://doi.org/10.1086/660021
  10. Core Writing Team, Pachauri, R. K. & Meyer, L. 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, 151 pp.
  11. Coyne, K. J., Handy, S. M., Demir, E., Whereat, E. B., Hutchins, D. A., Portune, K. J., Doblin, M. A. & Cary, S. C. 2005. Improved quantitative real-time PCR assays for enumeration of harmful algal species in field samples using an exogenous DNA reference standard. Limnol. Oceanogr. Methods 3:381-391. https://doi.org/10.4319/lom.2005.3.381
  12. Daufresne, M., Lengfellner, K. & Sommer, U. 2009. Global warming benefits the small in aquatic ecosystems. Proc. Natl. Acad. Sci. U. S. A. 106:12788-12793. https://doi.org/10.1073/pnas.0902080106
  13. Demura, M., Noel, M. -H., Kasai, F., Watanabe, M. M. & Kawachi, M. 2009. Taxonomic revision of Chattonella antiqua, C. marina and C. ovata (Raphidophyceae) based on their morphological characteristics and genetic diversity. Phycologia 48:518-535. https://doi.org/10.2216/08-98.1
  14. Dickson, A. G. 1993. The measurement of sea water pH. Mar. Chem. 44:131-142. https://doi.org/10.1016/0304-4203(93)90198-W
  15. Eberlein, T., Van de Waal, D. B., Brandenburg, K. M., John, U., Voss, M., Achterberg, E. P. & Rost, B. 2016. Interactive effects of ocean acidification and nitrogen limitation on two bloom-forming dinoflagellate species. Mar. Ecol. Prog. Ser. 543:127-140. https://doi.org/10.3354/meps11568
  16. Flynn, K. J., Clark, D. R., Mitra, A., Fabian, H., Hansen, P. J., Glibert, P. M., Wheeler, G. L., Stoecker, D. K., Blackford, J. C. & Brownlee, C. 2015. Ocean acidification with (de) eutrophication will alter future phytoplankton growth and succession. Proc. R. Soc. B 282:20142604.
  17. 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
  18. Garcia-Mendoza, E., Caceres-Martinez, J., Rivas, D., Fimbres-Martinez, M., Sanchez-Bravo, Y., Vasquez-Yeomans, R. & Medina-Elizalde, J. 2018. Mass mortality of cultivated northern bluefin tuna Thunnus thynnus orientalis associated with Chattonella species in Baja California, Mexico. Front. Mar. Sci. 5:454. https://doi.org/10.3389/fmars.2018.00454
  19. Gattuso, J. -P., Gao, K., Lee, K., Rost, B. & Schulz, K. 2010. Approaches and tools to manipulate the carbonate chemistry. In Riebesell, U., Fabry, V. J., Hansson, L. & Gattuso, J. -P. (Eds.) Guide to Best Practices for Ocean Acidification Research and Data Reporting. Publications Office of the European Union, Luxembourg, pp. 41-52.
  20. 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., Baxter, J. M., Laffoley, D., Osborn, 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.
  21. 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
  22. Giordano, M., Beardall, J. & Raven, J. A. 2005. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56:99-131. https://doi.org/10.1146/annurev.arplant.56.032604.144052
  23. Hallegraeff, G. M. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 46:220-235. https://doi.org/10.1111/j.1529-8817.2010.00815.x
  24. Hazen, E. L., Jorgensen, S., Rykaczewski, R. R., Bograd, S. J., Foley, D. G., Jonsen, I. D., Shaffer, S. A., Dunne, J. P., Costa, D. P., Crowder, L. B. & Block, B. A. 2013. Predicted habitat shifts of Pacific top predators in a changing climate. Nat. Clim. Chang. 3:234-238. https://doi.org/10.1038/nclimate1686
  25. Hennon, G. M. M. & Dyhrman, S. T. 2020. Progress and promise of omics for predicting the impacts of climate change on harmful algal blooms. Harmful Algae 91:101587. https://doi.org/10.1016/j.hal.2019.03.005
  26. Hennon, G. M. M., Williamson, O. M., Limon, M. D. H., Haley, S. T. & Dyhrman, S. T. 2019. Non-linear physiology and gene expression responses of harmful alga Heterosigma akashiwo to rising CO2. Protist 170:38-51. https://doi.org/10.1016/j.protis.2018.10.002
  27. Imai, I. & Yamaguchi, M. 2012. Life cycle, physiology, ecology and red tide occurrences of the fish-killing raphidophyte Chattonella. Harmful Algae 14:46-70. https://doi.org/10.1016/j.hal.2011.10.014
  28. Jeong, H. J. 2011. Mixotrophy in red tide algae Raphidophytes. J. Eukaryot. Microbiol. 58:215-222. https://doi.org/10.1111/j.1550-7408.2011.00550.x
  29. Jeong, H. J., Seong, K. A., Kang, N. S., Yoo, Y. D., Nam, S. W., Park, J. Y., Shin, W., Glibert, P. M. & Johns, D. 2010. Feeding by raphidophytes on the cyanobacterium Synechococcus sp. Aquat. Microb. Ecol. 58:181-195. https://doi.org/10.3354/ame01354
  30. Jeong, H. J., Yoo, Y. D., Lim, A. S., Kim, T. -W., Lee, K. & Kang, C. K. 2013. Raphidophyte red tides in Korean waters. Harmful Algae 30(Suppl. 1):S41-S52. https://doi.org/10.1016/j.hal.2013.10.005
  31. Jin, P. & Agusti, S. 2018. Fast adaptation of tropical diatoms to increased warming with trade-offs. Sci. Rep. 8:17771. https://doi.org/10.1038/s41598-018-36091-y
  32. Kahn, S., Arakawa, O. & Onoue, Y. 1998. Physiological investigations of a neurotoxin‐producing phytoflagellate, Chattonella marina (Raphidophyceae). Aquac. Res. 29:9-17. https://doi.org/10.1046/j.1365-2109.1998.00928.x
  33. Kibler, S. R., Tester, P. A., Kunkel, K. E., Moore, S. K. & Litaker, R. W. 2015. Effects of ocean warming on growth and distribution of dinoflagellates associated with ciguatera fish poisoning in the Caribbean. Ecol. Modell. 316:194-210. https://doi.org/10.1016/j.ecolmodel.2015.08.020
  34. Kim, J. -H., Kang, E. J., Kim, K. & Kim, K. Y. 2018. A continuous-flow and on-site mesocosm for ocean acidification experiments on benthic organisms. Algae 33:359-366. https://doi.org/10.4490/algae.2018.33.11.10
  35. Kim, S. Y., Seo, K. S., Lee, C. G. & Lee, Y. 2007. Diurnal modification of a red-tide causing organism, Chattonella antiqua (Raphidophyceae) from Korea. Algae 22:95-106. https://doi.org/10.4490/ALGAE.2007.22.2.095
  36. Kingsolver, J. G. 2009. The well-temperatured biologist (American Society of Naturalists presidential address). Am. Nat. 174:755-768. https://doi.org/10.1086/648310
  37. Kontopoulos, D. -G., Van Sebille, E., Lange, M., Yvon‐Durocher, G., Barraclough, T. G. & Pawar, S. 2020. Phytoplankton thermal responses adapt in the absence of hard thermodynamic constraints. Evolution 74:775-790. https://doi.org/10.1111/evo.13946
  38. Kremp, A., Godhe, A., Egardt, J., Dupont, S., Suikkanen, S., Casabianca, S. & Penna, A. 2012. Intraspecific variability in the response of bloom‐forming marine microalgae to changed climate conditions. Ecol. Evol. 2:1195-1207. https://doi.org/10.1002/ece3.245
  39. 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.
  40. Lewitus, A. J., Brock, L. M., Burke, M. K., De Mattio, K. A. & Wilde, S. B. 2008. Lagoonal stormwater detention ponds as promoters of harmful algal blooms and eutrophication along the South Carolina coast. Harmful Algae 8:60-65. https://doi.org/10.1016/j.hal.2008.08.012
  41. Marshall, J. A. & Hallegraeff, G. M. 1999. Comparative ecophysiology of the harmful alga Chattonella marina (Raphidophyceae) from South Australian and Japanese waters. J. Plankton Res. 21:1809-1822. https://doi.org/10.1093/plankt/21.10.1809
  42. 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
  43. Noh, I. H. 2009. Physiological and ecological studies on the harmful algae Chatttonella spp. (Raphidophyceae) in the coastal waters of Korea. Ph.D. dissertation, Chonnam National University, Gwangju, Korea, 130 pp.
  44. Onitsuka, G., Yamaguchi, M., Sakamoto, S., Shikata, T., Nakayama, N., Kitatsuji, S., Itakura, S., Sakurada, K., Ando, H., Yoshimura, N., Mukai, H. & Yamashita, H. 2020. Interannual variations in abundance and distribution of Chattonella cysts, and the relationship to population dynamics of vegetative cells in the Yatsushiro Sea, Japan. Harmful Algae 96:101833. https://doi.org/10.1016/j.hal.2020.101833
  45. Platt, T., Gallegos, C. L. & Harrison, W. G. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38:687-701.
  46. Qiu, X., Mukai, K., Shimasaki, Y., Wu, M., Chen, C., Lu, Y., Ichinose, H., Nakashima, T., Kato-Unoki, Y. & Oshima, Y. 2020. Diurnal variations in expression of photosynthesis-related proteins in the harmful Raphidophyceae Chattonella marina var. antiqua. J. Exp. Mar. Biol. Ecol. 527:151361. https://doi.org/10.1016/j.jembe.2020.151361
  47. Raven, J. A. 2017. The possible roles of algae in restricting the increase in atmospheric CO2 and global temperature. Eur. J. Phycol. 52:506-522. https://doi.org/10.1080/09670262.2017.1362593
  48. Raven, J. A., Gobler, C. J. & Hansen, P. J. 2020. Dynamic CO2 and pH levels in coastal, estuarine, and inland waters: theoretical and observed effects on harmful algal blooms. Harmful Algae 91:101594. https://doi.org/10.1016/j.hal.2019.03.012
  49. Rosso, L., Lobry, J. R., Bajard, S. & Flandrois, J. P. 1995. Convenient model to describe the combined effects of temperature and pH on microbial growth. Appl. Environ. Microbiol. 61:610-616. https://doi.org/10.1128/aem.61.2.610-616.1995
  50. 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
  51. 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
  52. Satta, C. T., Padedda, B. M., Sechi, N., Pulina, S., Loria, A. & Luglie, A. 2017. Multiannual Chattonella subsalsa Biecheler (Raphidophyceae) blooms in a Mediterranean lagoon (Santa Giusta Lagoon, Sardinia Island, Italy). Harmful algae 67:61-73. https://doi.org/10.1016/j.hal.2017.06.002
  53. Schulz, K., Barcelos e Ramos, J., Zeebe, R. E. & Riebesell, U. 2009. CO2 perturbation experiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations. Biogeosciences 6:2145-2153. https://doi.org/10.5194/bg-6-2145-2009
  54. Seto, D. S., Karp-Boss, L. & Wells, M. L. 2019. Effects of increasing temperature and acidification on the growth and competitive success of Alexandrium catenella from the Gulf of Maine. Harmful Algae 89:101670. https://doi.org/10.1016/j.hal.2019.101670
  55. Shikata, T., Takahashi, F., Nishide, H., Shigenobu, S., Kamei, Y., Sakamoto, S., Yuasa, K., Nishiyama, Y., Yamasaki, Y. & Uchiyama, I. 2019. RNA-seq analysis reveals genes related to photoreception, nutrient uptake, and toxicity in a noxious red-tide raphidophyte Chattonella antiqua. Front. Microbiol. 10:1764. https://doi.org/10.3389/fmicb.2019.01764
  56. Singh, S. P. & Singh, P. 2015. Effect of temperature and light on the growth of algae species: a review. Renew. Sustain. Energy Rev. 50:431-444. https://doi.org/10.1016/j.rser.2015.05.024
  57. Stacca, D., Satta, C. T., Casabianca, S., Penna, A., Padedda, B. M., Sechi, N. & Luglie, A. 2016. Identification of Chattonella (Raphidophyceae) species in long-term phytoplankton samples from Santa Giusta Lagoon, Italy. Sci. Mar. 80:17-25.
  58. Tatters, A. O., Roleda, M. Y., Schnetzer, A., Fu, F., Hurd, C. L., Boyd, P. W., Caron, D. A., Lie, A. A. Y., Hoffman, L. J. & Hutchins, D. A. 2013. Short and long-term conditioning of temperate marine diatom community to acidification and warming. Philos. Trans. R. Soc. B 368:20120437.
  59. Thomas, M. K., Aranguren‐Gassis, M., Kremer, C. T., Gould, M. R., Anderson, K., Klausmeier, C. A. & Litchman, E. 2017. Temperature-nutrient interactions exacerbate sensitivity to warming in phytoplankton. Glob. Chang. Biol. 23:3269-3280. https://doi.org/10.1111/gcb.13641
  60. Thomas, M. K., Kremer, C. T., Klausmeier, C. A. & Litchman, E. 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338:1085-1088. https://doi.org/10.1126/science.1224836
  61. Thomas, M. K., Kremer, C. T. & Litchman, E. 2016. Environment and evolutionary history determine the global biogeography of phytoplankton temperature traits. Glob. Ecol. Biogeogr. 25:75-86. https://doi.org/10.1111/geb.12387
  62. Thoms, S., Pahlow, M. & Wolf‐Gladrow, D. A. 2001. Model of the carbon concentrating mechanism in chloroplasts of eukaryotic algae. J. Theor. Biol. 208:295-313. https://doi.org/10.1006/jtbi.2000.2219
  63. Tilney, C. L., Hoadley, K. D. & Warner, M. E. 2015. Comparing the diel vertical migration of Karlodinium veneficum (Dinophyceae) and Chattonella subsalsa (Raphidophyceae): PSII photochemistry, circadian control, and carbon assimilation. J. Photochem. Photobiol. B 143:107-119. https://doi.org/10.1016/j.jphotobiol.2014.12.023
  64. Tortell, P. D., Rau, G. H. & Morel, F. M. M. 2000. Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol. Oceanogr. 45:1485-1500. https://doi.org/10.4319/lo.2000.45.7.1485
  65. 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
  66. Vidyarathna, N. K., Papke, E., Coyne, K. J., Cohen, J. H. & Warner, M. E. 2020. Functional trait thermal acclimation differs across three species of mid-Atlantic harmful algae. Harmful Algae 94:101804. https://doi.org/10.1016/j.hal.2020.101804
  67. Vrieling, E. G., Koeman, R. P. T., Nagasaki, K., Ishida, Y., Pererzak, L., Gieskes, W. W. C. & Veenhuis, M. 1995. Chattonella and Fibrocapsa (Raphidophyceae): first observation of, potentially harmful, red tide organisms in Dutch coastal waters. Neth. J. Sea Res. 33:183-191. https://doi.org/10.1016/0077-7579(95)90005-5
  68. Wang, B., Wu, D., Chu, K. H., Ye, L., Yip, H. Y., Cai, Z. & Wong, P. K. 2017. Removal of harmful alga, Chattonella marina, by recyclable natural magnetic sphalerite. J. Hazard. Mater. 324:498-506. https://doi.org/10.1016/j.jhazmat.2016.11.018
  69. Wang, Z. -H., Qi, Y. -Z., Chen, J. -F. & Xu, N. 2006. Population dynamics of Chattonella in spring in Daya Bay, the South China Sea and the cause of its blooms. Acta Hydrobiol. Sin. 30:394-398. https://doi.org/10.3321/j.issn:1000-3207.2006.04.004
  70. Watanabe, M., Kohata, K. & Kimura, T. 1991. Diel vertical migration and nocturnal uptake of nutrients by Chattonella antiqua under stable stratification. Limnol. Oceanogr. 36:593-602. https://doi.org/10.4319/lo.1991.36.3.0593
  71. Yamaguchi, H., Mizushima, K., Sakamoto, S. & Yamaguchi, M. 2010. Effects of temperature, salinity and irradiance on growth of the novel red tide flagellate Chattonella ovata (Raphidophyceae). Harmful Algae 9:398-401. https://doi.org/10.1016/j.hal.2010.02.001
  72. Yamaguchi, H., Tanimoto, Y., Hayashi, Y., Suzuki, S., Yamaguchi, M. & Adachi, M. 2018. Bloom dynamics of noxious Chattonella spp. (Raphidophyceae) in contrastingly enclosed coastal environments: a comparative study of two coastal regions. J. Mar. Biol. Assoc. U. K. 98:657-663. https://doi.org/10.1017/S0025315417000017
  73. Yamochi, S. 1984. Effects of temperature on the growth of six species of red-tide flagellates occurring in Osaka Bay. Bull. Plankton Soc. Jpn. 3l:5-22.
  74. Yoshimatsu, S. & Ono, C. 1986. The seasonal appearance of the red tide organisms and flagellates in the southern Harima-Nada, Inland Sea of Seto. Bull. Akashiwo Res. Inst. Kagawa Pref. 2:1-42.
  75. Zhang, Y., Fu, F. -X., Whereat, E., Coyne, K. J. & Hutchins, D. A. 2006. Bottom-up controls on a mixed-species HAB assemblage: a comparison of sympatric Chattonella subsalsa and Heterosigma akashiwo (Raphidophyceae) isolates from the Delaware Inland Bays, USA. Harmful Algae 5:310-320. https://doi.org/10.1016/j.hal.2005.09.001
  76. Zingone, A., Escalera, L., Aligizaki, K., Fernandez-Tejedor, M., Ismael, A., Montreso, M., Mozetic, P., Tas, S. & Totti, C. 2020. Toxic marine microalgae and noxious blooms in the Mediterranean Sea: a contribution to the Global HAB Status Report. Harmful Algae. Advanced online publication. https://doi.org/10.1016/j.hal.2020.101843.