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The impact of biotic and abiotic factors on the distribution of surface sediment dinoflagellate cyst assemblages on the Nanji Island in the East China Sea

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Abstract

The dinoflagellate cyst assemblages on the Nanji Island in the East China Sea, are documented at the first time to construct a quantitative overview of the cyst bank from 2014 to 2015. Thirty-four morphotypes from six groups are identified and quantified at eight sampling sites around the island, including a high proportion of potentially toxigenic species (14%). Autotrophic dinocysts constitute 74% of the total cyst counts, which is relatively low (two to thirty-three per millilitre sediment) compared with previous studies in adjacent areas. Scrippsiella trochoidea and Protoperidinium avellana are the most abundant autotrophic and heterotrophic species, respectively. A multivariate analysis is performed to assess associations between dinocysts and abiotic or biotic variables. Differentiation among seasons is evident in the detrended correspondence analysis (DCA) ordination plot, while a spatial pattern is not clearly revealed despite heterogeneity of the hydrodynamic conditions between sampling sites. Soluble reactive phosphate, the ratio of nitrogen to phosphorus concentrations and Karenia mikimotoi bloom are the three factors significantly (P<0.05) related to surface sediment cyst assemblage defined by the canonical correspondence analysis (CCA), highlighting the importance of nutrient regime to a dinocyst distribution in this area. Although attempts to address the origin of HAB events in recent years using seed banks have failed, knowledge can be valuable for further investigation of dinocyst dynamics and potential toxin threats on the Nanji Island.

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References

  • Accoroni S, Romagnoli T, Pichierri S, et al. 2016. Effects of the bloom of harmful benthic dinoflagellate Ostreopsis cf. ovata on the microphytobenthos community in the northern Adriatic Sea. Harmful Algae, 55: 179–190

    Article  Google Scholar 

  • Bogus K, Mertens K N, Lauwaert J, et al. 2014. Differences in the chemical composition of organic–walled dinoflagellate resting cysts from phototrophic and heterotrophic dinoflagellates. Journal of Phycology, 50(2): 254–266, doi: 10.1111/jpy.12170

    Article  Google Scholar 

  • Braak C J F, Šmilauer P. 2012. Canoco Reference Manual and User’s guide: Software for Ordination (Version 5. 0). Ithca, NY: Microcomputer power.

    Google Scholar 

  • Bravo I, Figueroa R I. 2014. Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms, 2(1): 11–32, doi: 10.3390/microorganisms2010011

    Article  Google Scholar 

  • Dai Xinfeng, Lu Douding, Xia Ping, et al. 2012. A 50–year temporal record of dinoflagellate cysts in sediments from the Changjiang estuary, East China Sea, in relation to climate and catchment changes. Estuarine, Coastal and Shelf Science, 112: 192–197, doi: 10.1016/j.ecss.2012.07.016

    Article  Google Scholar 

  • Dale B. 1976. Cyst formation, sedimentation, and preservation: Factors affecting dinoflagellate assemblages in recent sediments from trondheimsfjord, Norway. Review of Palaeobotany and Palynology, 22(1): 39–60, doi: 10.1016/0034–6667(76) 90010–5

    Article  Google Scholar 

  • Dale B. 1983. Dinoflagellate resting cysts: “benthic plankton”. In: Fryxell G A, ed. Survival Strategies of the Algae. Cambridge: Cambridge University Press, 69–136.

    Google Scholar 

  • Dale B. 2009. Eutrophication signals in the sedimentary record of dinoflagellate cysts in coastal waters. Journal of Sea Research, 61(1–2): 103–113, doi: 10.1016/j.seares.2008.06.007

    Article  Google Scholar 

  • Dale B, Dale A L, Jansen J H F. 2002. Dinoflagellate cysts as environmental indicators in surface sediments from the Congo deepsea fan and adjacent regions. Palaeogeography, Palaeoclimatology, Palaeoecology, 185(3–4): 309–338, doi: 10.1016/S0031–0182(02)00380–2

    Article  Google Scholar 

  • Dale B, Fjellså A. 1994. Dinoflagellate cysts as paleoproductivity indicators: state of the art, potential, and limits. In: Zahn R, Ped–ersen T F, Kaminski M A, et al., eds. Carbon Cycling in the Glacial Ocean: Constraints on the Ocean’s Role in Global Change. Berlin. Heidelberg: Springer, 521–537

    Google Scholar 

  • De Jorge V N, van Beusekom J E E. 1995. Wind–and tide–induced resuspension of sediment and microphytobenthos from tidal flats in the Ems estuary. Limnology and Oceanography, 40(4): 776–778, doi: 10.4319/lo.1995.40.4.0776

    Article  Google Scholar 

  • Devillers R, De Vernal A. 2000. Distribution of dinoflagellate cysts in surface sediments of the northern North Atlantic in relation to nutrient content and productivity in surface waters. Mar Geol, 166(1–4): 103–124, doi: 10.1016/S0025–3227(00)00007–4

    Article  Google Scholar 

  • Díaz P A, Molinet C, Seguel M, et al. 2014. Coupling planktonic and benthic shifts during a bloom of Alexandrium catenella in southern Chile: Implications for bloom dynamics and recurrence. Harmful Algae, 40: 9–22, doi: 10.1016/j.hal.2014.10.001

    Article  Google Scholar 

  • Fertouna–Bellakhal M, Dhib A, Béjaoui B, et al. 2014. Driving factors behind the distribution of dinocyst composition and abundance in surface sediments in a western Mediterranean coastal lagoon: report from a high–resolution mapping study. Marine Pollution Bulletin, 84(1–2): 347–362, doi: 10.1016/j.marpolbul. 2014.04.041

    Article  Google Scholar 

  • Figueroa R I, Bravo I. 2005. Sexual reproduction and two different encystment strategies of Lingulodinium polyedrum (Dinophyceae) in culture. Journal of Phycology, 41(2): 370–379, doi: 10.1111/(ISSN)1529–8817

    Article  Google Scholar 

  • Figueroa R I, Bravo I, Garcés E. 2005. Effects of nutritional factors and different parental crosses on the encystment and excystment of Alexandrium catenella (Dinophyceae) in culture. Phycologia, 44 (6): 658–670, d o i: 1 0. 2 2 1 6 /0 0 3 1–8 8 8 4 ( 2 0 0 5 ) 4 4 [ 6 5 8: EONFAD]2.0.CO;2

    Google Scholar 

  • Fistarol G O, Legrand C, Rengefors K, et al. 2004. Temporary cyst formation in phytoplankton: a response to allelopathic competitors. Environmental Microbiology, 6(8): 791–798, doi: 10.1111/emi. 2004.6.issue–8

    Article  Google Scholar 

  • Fujii R, Matsuoka K. 2006. Seasonal change of dinoflagellates cyst flux collected in a sediment trap in Omura Bay, West Japan. Journal of Plankton Research, 28(2): 131–147, doi: 10.1093/plankt/fbi106

    Article  Google Scholar 

  • Furio E F, Azanza R V, Fukuyo Y, et al. 2012. Review of geographical distribution of dinoflagellate cysts in Southeast Asian coasts. Coastal Marine Science, 35(1): 20–33

    Google Scholar 

  • Godhe A, McQuoid M R. 2003. Influence of benthic and pelagic environmental factors on the distribution of dinoflagellate cysts in surface sediments along the Swedish west coast. Aquatic Microbial Ecology, 32(2): 185–201

    Article  Google Scholar 

  • González C, Dupont L M, Mertens K, et al. 2008. Reconstructing marine productivity of the Cariaco Basin during marine isotope stages 3 and 4 using organic–walled dinoflagellate cysts. Paleoceanography, 23: PA3215, doi: 10.1029/2008PA001602

    Book  Google Scholar 

  • Gu Haifeng, Liu Tingting, Lan Dongzhao. 2011. Progress of dinoflagellate cyst research in the China seas. Biodiversity Science, 19(6): 779–786

    Google Scholar 

  • Gu Haifeng, Luo Zhaohe, Mertens K N, et al. 2015. Cyst–motile stage relationship, morphology, ultrastructure, and molecular phylogeny of the gymnodinioid dinoflagellate Barrufeta resplendens comb. Journal of Phycology, 51: 990–999

    Article  Google Scholar 

  • Hallegraeff G M, Bolch C J. 1992. Transport of diatom and dinoflagellate resting spores in ships’ ballast water: implications for plankton biogeography and aquaculture. Journal of Plankton Research, 14(8): 1067–1084, doi: 10.1093/plankt/14.8.1067

    Article  Google Scholar 

  • Harland R, Nordberg K, Filipsson H L. 2004. The seasonal occurrence of dinoflagellate cysts in surface sediments from Koljö Fjord, west coast of Sweden–a note. Review of palaeobotany and pal y n o l o gy, 128 (1–2): 107–117, d o i: 1 0. 1 0 1 6 /S 0 0 3 4–6667(03)00115–5

    Google Scholar 

  • Head M J. 1996. Modern dinoflagellate cysts and their biological affinities. In: Palynology: Principles and Applications, (Vol. 3): 1197–1248

    Google Scholar 

  • Ishikawa A, Hattori M, Ishii K I, et al. 2014. In situ dynamics of cyst and vegetative cell populations of the toxic dinoflagellate Alexandrium catenella in Ago Bay, central Japan. J Plankton Res, 36(5): 1333–1343, doi: 10.1093/plankt/fbu048

    Article  Google Scholar 

  • Ishikawa A, Taniguchi A. 1996. Contribution of benthic cysts to the population dynamics of Scrippsiella spp. (Dinophyceae) in Onagawa Bay, northeast Japan. Marine Ecology Progress Series, 140(1–3): 169–178

    Article  Google Scholar 

  • Jansson I M, Mertens K N, Head M J, et al. 2014. Statistically assessing the correlation between salinity and morphology in cysts produced by the dinoflagellate Protoceratium reticulatum from surface sediments of the North Atlantic Ocean, Mediterranean–Marmara–Black Sea region, and Baltic–Kattegat–Skagerrak estuarine system. Palaeogeography, Palaeoclimatology, Palaeoecology, 399: 202–213, doi: 10.1016/j.palaeo.2014.01.012

    Article  Google Scholar 

  • Jeong H J, Yoo Y D, Seong K A, et al. 2005. Feeding by the mixotrophic red–tide dinoflagellate Gonyaulax polygramma: mechanisms, prey species, effects of prey concentration, and grazing impact. Aquatic Microbial Ecology, 38: 249–257, doi: 10.3354/ame038249

    Article  Google Scholar 

  • Jiang Tao, Xu Yixiao, Li Yang, et al. 2014a. Seasonal dynamics of Alexandrium tamarense and occurrence of paralytic shellfish poisoning toxins in bivalves in Nanji Islands, East China Sea. Marine and Freshwater Research, 65(4): 350–358, doi: 10.1071/MF13001

    Article  Google Scholar 

  • Jiang Tao, Xu Yixiao, Li Yang, et al. 2014b. Dinophysis caudata generated lipophilic shellfish toxins in bivalves from the Nanji Islands, East China Sea. Chinese Journal of Oceanology and Limnology, 32(1): 130–139, doi: 10.1007/s00343–014–2290–8

    Article  Google Scholar 

  • Joyce L B, Pitcher G C, du Randt A, et al. 2005. Dinoflagellate cysts from surface sediments of Saldanha Bay, South Africa: an indication of the potential risk of harmful algal blooms. Harmful Algae, 4(2): 309–318, doi: 10.1016/j.hal.2004.08.001

    Article  Google Scholar 

  • Kremp A, Anderson D M. 2000. Factors regulating germination of resting cysts of the spring bloom dinoflagellate Scrippsiella hangoei from the northern Baltic Sea. Journal of Plankton Research, 22(7): 1311–1327, doi: 10.1093/plankt/22.7.1311

    Article  Google Scholar 

  • Krock B, Borel C M, Barrera F, et al. 2015. Analysis of the hydrographic conditions and cyst beds in the San Jorge Gulf, Argentina, that favor dinoflagellate population development including toxigenic species and their toxins. Journal of Marine Systems, 148: 86–100, doi: 10.1016/j.jmarsys.2015.01.006

    Article  Google Scholar 

  • Leira M, Sabater S. 2005. Diatom assemblages distribution in Catalan Rivers, NE Spain, in relation to chemical and physiographical factors. Water Research, 39(1): 73–82, doi: 10.1016/j.watres. 2004.08.034

    Article  Google Scholar 

  • Li Yang, Li Huan, Lü Songhui, et al. 2010. Species diversity and distribution of phytoplankton in Nanji Islands national nature reserve. Acta Hydrobiologica Sinica (in Chinese), 34(3): 618–628

    Article  Google Scholar 

  • Liu Dongyan, Shi Yajun, Di Baoping, et al. 2012. The impact of different pollution sources on modern dinoflagellate cysts in Sishili Bay, Yellow Sea, China. Marine Micropaleontology, 84–85: 1–13, doi: 10.1016/j.marmicro.2011.11.001

    Google Scholar 

  • Matsuoka K. 1999. Eutrophication process recorded in dinoflagellate cyst assemblages—a case of Yokohama Port, Tokyo Bay, Japan. Science of the Total Environment, 231(1): 17–35, doi: 10.1016/S0048–9697(99)00087–X

    Article  Google Scholar 

  • Matsuoka K, Joyce L B, Kotani Y, et al. 2003. Modern dinoflagellate cysts in hypertrophic coastal waters of Tokyo Bay, Japan. Journal of Plankton Research, 25(12): 1461–1470, doi: 10.1093/plankt/fbg111

    Article  Google Scholar 

  • Morquecho L, Lechuga–Devéze C H. 2004. Seasonal occurrence of planktonic dinoflagellates and cyst production in relationship to environmental variables in subtropical Bahía Concepción, Gulf of California. Botanica Marina, 47(4): 313–322

    Article  Google Scholar 

  • Nagai S, Matsuyama Y, Oh S J, et al. 2004. Effect of nutrients and temperature on encystment of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) isolated from Hiroshima Bay, Japan. Plankton Biology &Ecology, 51(2): 103–109

    Google Scholar 

  • Neely T, Campbell L. 2006. A modified assay to determine hemolytic toxin variability among Karenia clones isolated from the Gulf of Mexico. Harmful Algae, 5(5): 592–598, doi: 10.1016/j.hal. 2005.11.006

    Article  Google Scholar 

  • Persson A, Godhe A, Karlson B. 2000. Dinoflagellate cysts in recent sediments from the west coast of Sweden. Botanica Marina, 43:69–79

    Book  Google Scholar 

  • Pospelova V, Chmura G L, Boothman W S, et al. 2002. Dinoflagellate cyst records and human disturbance in two neighboring estuaries, New Bedford Harbor and Apponagansett Bay, Massachusetts (USA). Science of The Total Environment, 298(1–3): 81–102, doi: 10.1016/S0048–9697(02)00195–X

    Article  Google Scholar 

  • Pospelova V, Chmura G L, Boothman W S, et al. 2005. Spatial distribution of modern dinoflagellate cysts in polluted estuarine sediments from Buzzards Bay (Massachusetts, USA) embayments. Marine Ecology Progress Series, 292: 23–40, doi: 10.3354/meps292023

    Article  Google Scholar 

  • Pospelova V, de Vernal A, Pedersen T F. 2008. Distribution of dinoflagellate cysts in surface sediments from the northeastern Pacific Ocean (43°–25°N) in relation to sea–surface temperature, salinity, productivity and coastal upwelling. Marine Micropaleontology, 68(1–2): 21–48, doi: 10.1016/j.marmicro.2008.01.008

    Article  Google Scholar 

  • Prebble J G, Crouch E M, Carter L, et al. 2013. An expanded modern dinoflagellate cyst dataset for the Southwest Pacific and Southern Hemisphere with environmental associations. Marine Micropaleontology, 101: 33–48, doi: 10.1016/j.marmicro.2013. 04.004

    Article  Google Scholar 

  • Price A M, Pospelova V. 2011. High–resolution sediment trap study of organic–walled dinoflagellate cyst production and biogenic silica flux in Saanich Inlet (BC, Canada). Marine Micropaleontology, 80(1–2): 18–43, doi: 10.1016/j.marmicro.2011.03.003

    Article  Google Scholar 

  • Radi T, Pospelova V, de Vernal A, et al. 2007. Dinoflagellate cysts as indicators of water quality and productivity in British Columbia estuarine environments. Marine Micropaleontology, 62(4): 269–297, doi: 10.1016/j.marmicro.2006.09.002

    Article  Google Scholar 

  • Sætre M M L, Dale B, Abdullah M I, et al. 1997. Dinoflagellate cysts as potential indicators of industrial pollution in a Norwegian Fjord. Marine Environmental Research, 44(2): 167–189, doi: 10.1016/S0141–1136(96)00109–2

    Article  Google Scholar 

  • Sherr E B, Sherr B F. 2007. Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Marine Ecology Progress Series, 352: 187–197, doi: 10.3354/meps07161

    Article  Google Scholar 

  • Shin H H, Jung S W, Jang M C, et al. 2013a. Effect of pH on the morphology and viability of Scrippsiella trochoidea cysts in the hypoxic zone of a eutrophied area. Harmful Algae, 28: 37–45, doi: 10.1016/j.hal.2013.05.011

    Article  Google Scholar 

  • Shin H H, Lim D, Park S Y, et al. 2013b. Distribution of dinoflagellate cysts in Yellow Sea sediments. Acta Oceanologica Sinica, 32(9): 91–98, doi: 10.1007/s13131–013–0356–7

    Article  Google Scholar 

  • Uchida T, Toda S, Matsuyama Y, et al. 1999. Interactions between the red tide dinoflagellates Heterocapsa circularisquama and Gymnodinium mikimotoi in laboratory culture. Journal of Experimental Marine Biology and Ecology, 241(2): 285–299, doi: 10.1016/S0022–0981(99)00088–X

    Article  Google Scholar 

  • Verleye T J, Louwye S. 2010. Recent geographical distribution of organic–walled dinoflagellate cysts in the southeast Pacific (25°–53°S) and their relation to the prevailing hydrographical conditions. Palaeogeography, Palaeoclimatology, Palaeoecology, 298(3–4): 319–340, doi: 10.1016/j.palaeo.2010.10.006

    Article  Google Scholar 

  • Wang You, Tang Xuexi. 2008. Interactions between Prorocentrum donghaiense Lu and Scrippsiella trochoidea (Stein) Loeblich III under laboratory culture. Harmful Algae, 7(1): 65–75, doi: 10.1016/j.hal.2007.05.005

    Article  Google Scholar 

  • Wang Zhaohui, Qi Yuzao, Lu Songhui, et al. 2004. Seasonal distribution of dinoflagellate resting cysts in surface sediments from Changjiang River Estuary. Phycological Research, 52(4): 387–395, doi: 10.1111/pre.2004.52.issue–4

    Article  Google Scholar 

  • Xu Zhifang, Chen Ying, Meng Xi, et al. 2016. Phytoplankton community diversity is influenced by environmental factors in the coastal East China Sea. European Journal of Phycology, 51(1): 107–118, doi: 10.1080/09670262.2015.1107138

    Article  Google Scholar 

  • You Shengpao, Gao Han, Lei Xiangdong, et al. 2016. Biodiversity and distribution of dinoflagellate resting cysts in the sediments of Nanji Island, East China Sea. Oceanologia et Limnologia Sinica (in Chinese), 47(2): 460–468

    Google Scholar 

  • Zhou Mingjiang. 2010. Environmental settings and harmful algal blooms in the sea area adjacent to the Changjiang River Estuary. In: Ishimatsu A, Lie H J, eds. Coastal Environmental and Ecosystem Issues of the East China Sea. Okusawa, Setagaya–ku, Tokyo: TERRAPUB and Nagasaki University, 133–149

    Google Scholar 

  • Zhou Weihua, Yin Kedong, Zhu Dedi. 2006. Phytoplankton biomass and high frequency of Prorocentrum donghaiense harmful algal bloom in Zhoushan sea area in spring. Chinese Journal of Applied Ecology (in Chinese), 17(5): 887–893

    Google Scholar 

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  1. Ocean College, Zhejiang University, Zhoushan, 316000, China

    Han Gao, Yunpu Xiao & Mengmeng Tong

  2. Nanji Marine Environment Monitoring Station, Ministry of Natural Resources, Pingyang, 325400, China

    Shengpao You & Xiangdong Lei

  3. Pingyang County Marine and Fisheries Bureau, Pingyang, 325400, China

    Yunpu Xiao

  4. Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, China

    Haifeng Gu

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  1. Han Gao
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Correspondence to Mengmeng Tong.

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Foundation item: The Zhejiang Public Welfare Technology Research and Social Development Project of 2013 of China under contract Nos 2013C33081 and 2013C32040; the National Natural Science Foundation of China under contract No. 41306095; the Doctoral Fund of Ministry of Education of China under contract No. J20130101.

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Gao, H., You, S., Lei, X. et al. The impact of biotic and abiotic factors on the distribution of surface sediment dinoflagellate cyst assemblages on the Nanji Island in the East China Sea. Acta Oceanol. Sin. 38, 160–171 (2019). https://doi.org/10.1007/s13131-019-1375-9

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