REGULAR PAPER
Full Access
Diversity and geographical distribution of resting stages of eukaryotic algae in the surface sediments from the southern Chinese coastline based on metabarcoding partial 18S rDNA sequences
Lei Liu,
Zhaohui Wang,
Songhui Lu,
Lei Liu
College of Life Science and Technology, Jinan University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Zhaohui Wang
College of Life Science and Technology, Jinan University, Guangzhou, China
Correspondence
Zhaohui Wang, Department of Ecology, College of Life Science and Technology, Jinan University, Guangzhou 510632, China.
Email: [email protected]
Search for more papers by this authorSonghui Lu
College of Life Science and Technology, Jinan University, Guangzhou, China
Search for more papers by this authorLei Liu,
Zhaohui Wang,
Songhui Lu,
Lei Liu
College of Life Science and Technology, Jinan University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Zhaohui Wang
College of Life Science and Technology, Jinan University, Guangzhou, China
Correspondence
Zhaohui Wang, Department of Ecology, College of Life Science and Technology, Jinan University, Guangzhou 510632, China.
Email: [email protected]
Search for more papers by this authorSonghui Lu
College of Life Science and Technology, Jinan University, Guangzhou, China
Search for more papers by this authorAbstract
Surface sediment samples were collected from sixteen sites of the southern Chinese coastline in this study. Diversity of eukaryotic microalgae was examined using high-throughput sequencing of 18S rDNA to understand the community structure and geological distribution of microalgal resting stages. A total of 218 operational taxonomic units (OTUs) were detected for eukaryotic algae, and only 75 OTUs (34.40%) were detected into species level. The algal communities were composed of sixty-four genera belonged to twelve classes of four phyla. Dinoflagellates were the most abundant and diversified group, which accounted for the average of 56.26% and 53.70% DNA reads and OTUs, respectively. Dinoflagellates were dominated by Protoperidinium, Euduboscquella, Amylax, and Paragymnodinium. Chaetoceros, Thalassiosira, and Skeletonema were abundant in diatoms, while Pedospumella and Paraphysomonas in Chrysophyceae were the most abundant genera due to their massive occurrence in some particular sites. The high abundance of Protoperidinium sequences suggested the high nutrient levels in the southern Chinese coastline. Nineteen of the detected OTUs were assigned to harmful and/or bloom-forming microalgae. The wide occurrence of the toxic dinoflagellate Azadinium poporum and high abundance of Alexandrium pacificum in some particular sites suggested the potential risk of human poisoning.
Supporting Information
| Filename | Description |
|---|---|
| maec12585-sup-0001-TableS1-S3.docxapplication/docx, 104.6 KB | Supplementary Material |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Ajani, P., Hallegraeff, G., & Pritchard, T. (2001). Historic overview of algal blooms in marine and estuarine waters of New South Wales, Australia. Proceedings of the Linnean Society of New South Wales, 123, 1–22.
- Anderson, D. M., Cembella, A. D., & Hallegraeff, G. M. (2012). Progress in understanding harmful algal blooms: Paradigm shifts and new technologies for research, monitoring, and management. Annual Review of Marine Science, 4, 143–176. https://doi.org/10.1146/annurev-marine-120308-081121
- Anderson, D. M., Kulis, D. M., Qi, Y. Z., Zheng, L., Lu, S., & Lin, Y. T. (1996). Paralytic shellfish poisoning in southern China. Toxicon, 34, 579–590. https://doi.org/10.1016/0041-0101(95)00158-1
- Bergesch, M., Odebrecht, C., & Moestrup, Ø. (2008). Nanoflagellates from coastal waters of southern Brazil (32ºS). Botanica Marina, 51, 35–50.
- Bråte, J., Logares, R., Berney, C., Ree, D. K., Klaveness, D., Jakobsen, K. S., & Shalchian-Tabrizi, K. (2010). Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. The ISME Journal, 4, 1144–1153. https://doi.org/10.1038/ismej.2010.3910.1038/ismej.2010.39
- Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., … Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336. https://doi.org/10.1038/nmeth.f.303
- Cavalier-Smith, T., Lewis, R., Chao, E. E., Oates, B., & Bass, D. (2009). Helkesimastix marina n. sp. (Cercozoa: Sainouroidea superfam. n.) a gliding zooflagellate of novel ultrastructure and unusual ciliary behaviour. Protist, 160, 452–479. https://doi.org/10.1016/j.protis.2009.03.003
- Chariton, A. A., Stephenson, S., Morgan, M. J., Steven, A. D. L., Colloff, M. J., Court, L. N., & Hardy, C. M. (2015). Metabarcoding of benthic eukaryote communities predicts the ecological condition of estuaries. Environmental Pollution, 203, 165–174. https://doi.org/10.1016/j.envpol.2015.03.04710.1016/j.envpol.2015.03.047
- Dai, X. F., Lu, D. D., Guan, W. B., Wang, H. X., He, P. X., Xia, P., & Yang, H. J. (2014). Newly recorded Karlodinium veneficum dinoflagellate blooms in stratified water of the East China Sea. Deep Sea Research Part II: Topical Studies in Oceanography, 101(SI), 237–243. https://doi.org/10.1016/j.dsr2.2013.01.01510.1016/j.dsr2.2013.01.015
- Dale, B. (1983). Dinoflagellate resting cysts: ‘benthic plankton’. In G. A. Fryxell (Ed.), Survival strategies of the algae (pp. 69–136). Cambridge: Cambridge University Press.
- Dale, B. (2009). Eutrophication signals in the sedimentary record of dinoflagellate cysts in coastal waters. Journal of Sea Research, 61, 103–113. https://doi.org/10.1016/j.seares.2008.06.007
- de Vargas, C., Audic, S., Henry, N., Decelle, J., Mahe, F., Logares, R., … Velayoudon, D. (2015). Eukaryotic plankton diversity in the sunlit ocean. Science, 348(6237), 1261605. https://doi.org/10.1126/science.1261605
- de Vernal, A., Rochon, A., Turon, J. L., & Matthiessen, J. (1997). Organic-walled dinoflagellate cysts: Palynological tracers of sea-surface conditions in middle and high latitude marine environments. Geobios, 30, 905–920.
- Decelle, J., Romac, S., Stern, R. F., Bendif, E. M., Zingone, A., Audic, S., … Christen, R. (2015). PhytoREF: A reference database of the plastidial 16S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Molecular Ecology Resources, 15, 1435–1445. https://doi.org/10.1111/1755-0998.12401
- Deeds, J. R., & Place, A. R. (2006). Sterol-specific membrane interactions with the toxins from Karlodinium micrum (Dinophyceae)-a strategy for self-protection? African Journal of Marine Science, 28, 421–425.
- Dzhembekova, N., Moncheva, S., Ivanova, P., Slabakova, N., & Nagai, S. (2018). Biodiversity of phytoplankton cyst assemblages in surface sediments of the Black Sea based on metabarcoding. Biotechnology & Biotechnological Equipment, 32, 1507–1513. https://doi.org/10.1080/13102818.2018.1532816
- Edgar, R. C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10), 996–998. https://doi.org/10.1038/nmeth.260410.1038/nmeth.2604
- Eland, L. E., Davenport, R., & Mota, C. R. (2012). Evaluation of DNA extraction methods for freshwater eukaryotic microalgae. Water Research, 46, 5355–5364. https://doi.org/10.1016/j.watres.2012.07.023
- Findenig, B. M., Chatzinotas, A., & Boenigk, J. (2010). Taxonomic and ecological characterization of stomatocysts of Spumella-like flagellates (Chrysophyceae). Journal of Phycology, 46, 868–881.
- Finlay, B. J., & Clarke, K. J. (1999). Apparent global ubiquity of species in the protist genus Paraphysomonas. Protist, 150, 419–430. https://doi.org/10.1016/S1434-4610(99)70042-8
- Forster, D., Dunthorn, M., Mahé, F., Dolan, J. R., Audic, S., Bass, D., … Stoeck, T. (2016). Benthic protists: The under-charted majority. FEMS Microbiology Ecology, 92, fiw120. https://doi.org/10.1093/femsec/fiw120
- Gao, Y., Dong, Y., Li, H., & Zhan, A. (2019). Influence of environmental factors on spatial–temporal distribution patterns of dinoflagellate cyst communities in the South China Sea. Marine Biodiversity, 49, 769–781. https://doi.org/10.1007/s12526-018-0850-4
- Gao, Y., Fang, H., Dong, Y., Li, H., Pu, C., & Zhan, A. (2017). An improved method for molecular identification of single dinoflagellate cysts. Peer J, 5, e3224.
- Garces, E., Fernandez, M., Penna, A., Van Lenning, K., Gutierrez, A., Camp, J., & Zapata, M. (2006). Characterization of NW mediterranean Karlodinium spp. (Dinophyceae) strains using morphological, molecular, chemical, and physiological methodologies. Phycology, 42, 1096–1112.
- Genovesi, B., Laabir, M., Masseret, E., Collos, Y., Vaquer, A., & Grzebyk, D. (2009). Dormancy and germination features in resting cysts of Alexandrium tamarense species complex (Dinophyceae) can facilitate bloom formation in a shallow lagoon (Thau, southern France). Journal of Plankton Research, 31, 1209–1224. https://doi.org/10.1093/plankt/fbp066
- Gilbert, P. M. (2017). Eutrophication, harmful algae and biodiversity - Challenging paradigms in a world of complex nutrient changes. Marine Pollution Bulletin, 124(2SI), 591–606. https://doi.org/10.1016/j.marpolbul.2017.04.027
- Gu, H. F., Zeng, N., Liu, T. T., Yang, W. D., Muller, A., & Krock, B. (2013). Morphology, toxicity, and phylogeny of Alexandrium (Dinophyceae) species along the coast of China. Harmful Algae, 27, 68–81. https://doi.org/10.1016/j.hal.2013.05.008
- Guiry, M. D., & Guiry, G. M. (2019). AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Retrieved from http://www.algaebase.org; searched on 09 September 2019.
- Harada, A., Ohtsuka, S., & Horiguchi, T. (2007). Species of the parasitic genus Duboscquella are members of the enigmatic marine alveolate group I. Protist, 158, 337–347. https://doi.org/10.1016/j.protis.2007.03.005
- Head, M. J. (1996). Modern Dinofalgelate cysts and their biological affinities. In J. Jansonius, & D. C. McGregory (Eds.), Palynology: Principles and applications (pp. 1197–1248). Dallas: American Association of Stratigraphic Palynologists Foundation.
- Heiri, O., Lotter, A. F., & Lemcke, G. (2001). Loss on ignition as a method for estimating organic and carbonate content in sediments: Reproducibility and comparability of results. Journal of Paleolimnology, 25, 101–110.
- Heisler, J., Glibert, P. M., Burkholder, J. M., Anderson, D. M., Cochlan, W., Dennison, W. C., … Suddleson, M. (2008). Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae, 8(SI), 3–13. https://doi.org/10.1016/j.hal.2008.08.006
- John, U., Litaker, R. W., Montresor, M., Murray, S., Brosnahan, M. L., & Anderson, D. M. (2014). Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: The introduction of five species with emphasis on molecular-based (rDNA) classification. Protist, 165, 779–804. https://doi.org/10.1016/j.protis.2014.10.00110.1016/j.protis.2014.10.001
- Jung, J. H., Choi, J. M., Coats, D. W., & Kim, Y. O. (2016). Euduboscquella costata n. sp (Dinoflagellata, Syndinea), an Intracellular Parasite of the Ciliate Schmidingerella arcuata: Morphology, Molecular Phylogeny, Life Cycle, Prevalence, and Infection Intensity. Journal of Eukaryotic Microbiology, 63, 3–15.
- Kang, N. S., Jeong, H. J., Moestrup, Ø., Shin, W., Nam, S. W., Park, J. Y., … Noh, J. H. (2010). Description of a new planktonic mixotrphi dinoflagellate Paragymnodinium shiwhaense n. gen., n. sp. from the coastal waters off western Korea: Morphology, pigments, and ribosomal DNA gene sequence. Journal of Eukaryotic Microbiology, 57, 121–144.
- Kang, N. S., Jeong, H. J., Yoo, Y. D., Yoon, E. Y., Lee, K. H., Lee, K., & Kim, G. (2011). Mixotrophy in the newly described phototrophic dinoflagellate Woloszynskia cincta from Western Korean waters: Feeding mechanism, prey species and effect of prey concentration. Journal of Eukaryotic Microbiology, 58, 152–170. https://doi.org/10.1111/j.1550-7408.2011.00531.x
- Kang, N. S., Lee, K. H., Jeong, H. J., Yoo, Y. D., Seong, K. A., Potvin, É., … Yoon, E. Y. (2013). Red tides in Shiwha Bay, western Korea: A huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae, 30, S114–S130. https://doi.org/10.1016/j.hal.2013.10.011
- Kataoka, T., Yamaguchi, H., Sato, M., Watanabe, T., Taniuchi, Y., Kuwata, A., & Kawachi, M. (2017). Seasonal and geographical distribution of near-surface small photosynthetic eukaryotes in the western North Pacific determined by pyrosequencing of 18S rDNA. FEMS Microbiology Ecology, 93, fiw229. https://doi.org/10.1093/femsec/fiw229
- Kociolek, J. P., Sabbe, K., Vandepitte, L., Decock, W., & Vanhoorn, B. (2016). Catalogue of diatom names resurrected: DiatomBase will be the new authority resource for diatom names and more. 24th International Diatom Symposium, 100.
- Kremp, A. (2001). Effects of cyst resuspension on germination and seeding of two bloom-forming dinoflagellates in the Baltic Sea. Marine Ecology Progress Series, 216, 57–66. https://doi.org/10.3354/meps216057
- Krock, B., Tillmann, U., Witt, M., & Gu, H. F. (2014). Azaspiracid variability of Azadinium poporum (Dinophyceae) from the China Sea. Harmful Algae, 36, 22–28. https://doi.org/10.1016/j.hal.2014.04.012
- Li, Y., Tang, Y. N., Shen, P. P., Li, G., & Tan, Y. H. (2019). Distribution of harmful dinoflagellate cysts in the surface sediments of Daya Bay of the South China Sea and their relationship to environmental factors. International Biodeteriatation and Biodegradation, 139, 44–53. https://doi.org/10.1016/j.ibiod.2019.02.006
- Liang, C. Y. (2018). Distribution of biogenic elements and germinated phytoplankton community structure in the surface sediments from the Beibu Gulf Rim. Master Thesis, Jinan University, Guangzhou, China.
- Lu, S. G., Tang, D. L., Guan, X. B., Cen, J. Y., & Lu, S. H. (2016). Identification of susceptibility of harmful algal blooms and determining the key monitoring zones in the coastal water of Hainan Island. Marine Environmetnal Science, 35, 580–586.
- Lu, X. X., Wang, Z. H., Gu, Y. G., Guo, X., Liang, W. B., & Liu, L. (2017). Impacts of metal contamination and eutrophication on dinoflagellate cyst assemblages along the Guangdong coast of southern China. Marine Pollution Bulletin, 120, 239–249. https://doi.org/10.1016/j.marpolbul.2017.05.032
- Luna, G. M., Dell'Anno, A., Pietrangeli, B., & Danovaro, R. (2012). A new molecular approach based on qPCR for the quantification of fecal bacteria in contaminated marine sediments. Journal of Biotechnology, 157, 446–453. https://doi.org/10.1016/j.jbiotec.2011.07.033
- Luo, Z. H., Yang, W. D., Xu, B., & Gu, H. F. (2013). First record of Biecheleria cincta (Dinophyceae) from Chinese coasts, with morphological and molecular characterization of the strains. Chinese Journal of Oceanology and Limnology, 31, 835–845. https://doi.org/10.1007/s00343-013-2315-8
- Malviya, S., Scalco, E., Audic, S., Vincent, F., Veluchamy, A., Poulain, J., … Bowler, C. (2016). Insights into global diatom distribution and diversity in the world's ocean. Proceedings of the National Academy of Sciences of the United States of America, 113, E1516–E1525. https://doi.org/10.1073/pnas.1509523113
- Matsuoka, K. (2001). Further evidence for a marine dinoflagellate cyst as an indicator of eutrophication in Yokohama port, Tokyo Bay, Japan. Comments on a discussion by B. Dale. Science of the Total Environment, 264, 221–233. https://doi.org/10.1016/S0048-9697(00)00718-X
- McQuiod, M. R. (2002). Pelagic and benthic environment controls on the spatial distribution of a viable diatom propagate bank on the Swedish west coast. Journal of Phycology, 38, 881–893.
- McQuoid, M. R., & Hobson, L. A. (1996). Diatom resting stages. Journal of Phycology, 32, 889–902. https://doi.org/10.1111/j.0022-3646.1996.00889.x
- Montresor, M., Prisco, C. D., Sarno, D., Margiotta, F., & Zingone, A. (2013). Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Marine Ecology Progress Series, 484, 79–95. https://doi.org/10.3354/meps10236
- Mortlock, R. A., & Froelich, P. N. (1989). A simple method for the rapid determination of biogenic opal in pelagic marine sediments. Deep Sea Research Part A, 36, 1415–1426. https://doi.org/10.1016/0198-0149(89)90092-7
- Orlova, T. Y., & Morozova, T. V. (2009). Resting stages of microalgae in recent marine sediments of Peter the Great Bay, Sea of Japan. Russian Journal of Marine Biology, 35, 313–322. https://doi.org/10.1134/S1063074009040063
- Park, M. G., Kim, M., & Kang, M. (2013). A dinoflagellate Amylax triacantha with plastids of the Cryptophyte origin: Phylogeny, feeding mechanism, and growth and grazing Responses. Journal of Eukaryotic Microbiology, 60, 363–376.
- Patil, J. S., & Anil, A. C. (2008). Temporal variation of diatom benthic propagules in a monsoon-influenced tropical estuary. Continental Shelf Research, 28, 2404–2416. https://doi.org/10.1016/j.csr.2008.06.001
- Pawlowski, J., Audic, S., Adl, S., Bass, D., Belbahri, L., Berney, C., … de Vargas, C. (2012). CBOL Protist Working Group: Barcoding Eukaryotic Richness beyond the Animal, Plant, and Fungal Kingdoms. PLoS Biology, 10(11), e1001419. https://doi.org/10.1371/journal.pbio.1001419
- Penna, A., Casabianca, S., Guerra, A. F., Vernesi, C., & Scardi, M. (2017). Analysis of phytoplankton assemblage structure in the Mediterranean Sea based on high-throughput sequencing of partial 18S rRNA sequences. Marine Genomics, 36, 49–55. https://doi.org/10.1016/j.margen.2017.06.001
- Piredda, R., Sarno, D., Lange, C. B., Tomasino, M. P., Zingone, A., & Montresor, M. (2017). Diatom resting stages in surface sediments: A pilot study comparing next generation sequencing and serial dilution cultures. Cryptogam Algologie, 38, 31–46. https://doi.org/10.7872/crya/v38.iss1.2017.31
- Place, A. R., Bowers, H. A., Bachvaroff, T. R., Adolf, J. E., Deeds, J. R., & Sheng, J. (2012). Karlodinium veneficum-the little dinoflagellate with a big bite. Harmful Algae, 14, 179–195. https://doi.org/10.1016/j.hal.2011.10.021
- Pospelova, V., & Kim, S. J. (2010). Dinoflagellate cysts in recent estuarine sediments from aquaculture sites of southern South Korea. Marine Micropaleontology, 76, 37–51. https://doi.org/10.1016/j.marmicro.2010.04.003
- Qi, Y., Chen, J., Wang, Z., Xu, N., Wang, Y., Shen, P., … Hodgkiss, I. J. (2004). Some observations on harmful algal bloom (HAB) events along the coast of Guangdong, southern China in 1998. Hydrobiologia, 512, 209–214. https://doi.org/10.1023/B:HYDR.0000020329.06666.8c
- Qiao, X., Wang, B., Sun, X., & Liang, S. (2014). Numerical simulation of nutrient and phytoplankton dynamics in Guangxi Coastal Bays, China. Journal of Ocean University of China, 13, 338–346. https://doi.org/10.1007/s11802-014-2072-0
- Qiu, D. J., Huang, L. M., Zhang, J. L., & Lin, S. J. (2010). Phytoplankton dynamics in and near the highly eutrophic Pearl River Estuary, South China Sea. Continental Shelf Research, 30, 177–186. https://doi.org/10.1016/j.csr.200910.015
- Radi, T., & de Vernal, A. (2008). Last glacial maximum (LGM) primary productivity in the northern North Atlantic Ocean. Canadian Journal of Earth Sciences, 45, 1299–1316.
- Rhodes, L. L., Smith, K. F., MacKenzie, L., & Moisan, C. (2019). Checklist of the planktonic marine dinoflagellates of New Zealand. New Zealand Journal of Marine and Freshwater Research, 54(1), 86–101. https://doi.org/10.1080/00288330.2019.1626746
- Rimet, F., Vasselon, V., Keszte, B. A., & Bouchez, A. (2018). Do we similarly assess diversity with microscopy and high-throughput sequencing? Case of microalgae in lakes. Organisms Diversity and Evolution, 18, 51–62. https://doi.org/10.1007/s13127-018-0359-5
10.1007/s13127-018-0359-5 Google Scholar
- Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., … Weber, C. F. (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541. https://doi.org/10.1128/AEM.01541-09
- Scoble, J. M., & Cavalier-Smith, T. (2013). Molecular and morphological diversity of Paraphysomonas (Chrysophyceae, order Paraphysomonadida); a short review. Nova Hedwigia, 142, 117–126.
- Seyfettin, T., Noyan, Y., & Erdogan, O. (2009). Phytoplankton as an indicator of improving water quality in the Golden Horn Estuary. Estuaries and Coasts, 32, 1205–1224. https://doi.org/10.1007/s12237-009-9207-3
- Sildever, S., Kremp, A., Enke, A., Buschmann, F., Maljutenko, I., & Lips, I. (2017). Spring bloom dinoflagellate cyst dynamics in three eastern sub-basins of the Baltic Sea. Continental Shelf Research, 137, 46–55. https://doi.org/10.1016/j.csr.2016.11.012
- Sildever, S., Ribeiro, S., Mertens, K. N., Andersen, T. J., Moros, M., & Kuijpers, A. (2019). Reconstructing salinity changes and environmental influence on dinoflagellate cysts in the central Baltic Sea since the late 19th century. Estuarine Coastal and Shelf Science, 219, 384–394. https://doi.org/10.1016/j.ecss.2019.02.034
- Smayda, T. J. (2002). Turbulence, watermass stratification and harmful algal blooms: An alternative view and frontal zones as pelagic seed banks. Harmful Algae, 1, 95–112. https://doi.org/10.1016/S1568-9883(02)00010-0
10.1016/S1568-9883(02)00010-0 Google Scholar
- Sun, Z., Li, G., Wang, C., Jing, Y., Zhu, Y., Zhang, S., & Liu, Y. (2014). Community dynamics of prokaryotic and eukaryotic microbes in an estuary reservoir. Scientific Reports, 4, 6966. https://doi.org/10.1038/srep06966
- Takahashi, K., Sarai, C., & Iwataki, M. (2014). Morphology of two marine woloszynskioid dinoflagellates Biecheleria brevisulcata sp. nov. and Biecheleriopsis adriatica (Suessiaceae, Dinophyceae) from Japanese coasts. Phycology, 53, 407–407.
- Tang, Y., & Gobler, C. J. (2012). The toxic dinoflagellate Cochlodinium polykrikoides (Dinophyceae) produces resting cysts. Harmful Algae, 20, 71–80. https://doi.org/10.1016/j.hal.2012.08.001
- Von Dassow, P., & Montresor, M. (2011). Unveiling the mysteries of phytoplankton life cycles: Patterns and opportunities behind complexity. Journal of Plankton Research, 33, 3–12. https://doi.org/10.1093/plankt/fbq137
- Wang, J. J., & Tang, D. L. (2014). Phytoplankton patchiness during spring intermonsoon in western coast of South China Sea. Deep-Sea Research Part II, 101, 120–128. https://doi.org/10.1016/j.dsr2.2013.09.020
- Wang, Z., Fu, Y., Kang, W., Liang, J., Gu, Y., & Jiang, X. (2013). Germination of phytoplankton resting cells from surface sediments in two areas of the Southern Chinese coastal waters. Marine Ecology, 34, 218–232. https://doi.org/10.1111/maec.12009
- Wang, Z., Matsuoka, K., Qi, Y., & Chen, J. (2004). Dinoflagellate cysts in recent sediments from Chinese coastal waters. Marine Ecology, 25, 289–311. https://doi.org/10.1111/j.1439-0485.2004.00035.x
- Wang, Z., Matsuoka, K., Qi, Y., Chen, J., & Lu, S. (2004). Dinoflagellate cyst records in recent sediments from Daya Bay, South China Sea. Phycological Research, 52, 396–407. https://doi.org/10.1111/j.1440-1835.2004.tb00348.x
- Wang, Z.-H., Nie, X.-P., Jiang, S.-J., Zhao, J.-G., Cao, Y. U., Zhang, Y.-J., & Wang, D.-Z. (2011). Source and profile of paralytic shellfish poisoning toxins in shellfish in Daya Bay, South China Sea. Marine Environmental Research, 72, 53–59. https://doi.org/10.1016/j.marenvres.2011.04.007
- Wang, Z., Qi, Y., & Yang, F. (2007). Cyst formation: An important mechanism for the termination of Scrippsiella trochoidea (Dinophyceae) bloom. Journal of Plankton Research, 29, 209–218. https://doi.org/10.1093/plankt/fbm008
- Wang, Z., Zhao, J., Zhang, Y., & Cao, Y. (2009). Phytoplankton community structure and environmental parameters in aquaculture areas of Daya Bay, South China Sea. Journal of Environmental Science China, 21, 1268–1275. https://doi.org/10.1016/S1001-0742(08)62414-6
- Wei, N., Satheeswaran, T., Jenkinsone, I. R., Xue, B., Wei, Y. Q., Liu, H. J., & Sun, J. (2018). Factors driving the spatiotemporal variability in phytoplankton in the Northern South China Sea. Continental Shelf Research, 162, 48–55. https://doi.org/10.1016/j.csr.2018.04.009
- 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. https://doi.org/10.1126/science.1257594
- Yu, Y., Song, J. M., Li, X. G., & Duan, L. Q. (2012). Geochemical records of decadal variations in terrestrial input and recent anthropogenic eutrophication in the Changjiang Estuary and its adjacent waters. Applied Geochemistry, 27, 1556–1566. https://doi.org/10.1016/j.apgeochem.2012.05.002
