Home > 2019, 38(1) > 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

Citation: Han GAO, Shengpao YOU, Xiangdong LEI, Yunpu XIAO, Haifeng GU, Mengmeng TONG. 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 OCEANOLOGICA SINICA, 2019, 38(1): 160-171. doi: 10.1007/s13131-019-1375-9

2019, 38(1): 160-171. doi: 10.1007/s13131-019-1375-9

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

1.  Ocean College, Zhejiang University, Zhoushan 316000, China
2.  Nanji Marine Environment Monitoring Station, Ministry of Natural Resources, Pingyang 325400, China
3.  Pingyang County Marine and Fisheries Bureau, Pingyang 325400, China
4.  Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China

Corresponding author: Mengmeng TONG, mengmengtong@zju.edu.cn

Received Date: 2017-08-03
Web Publishing Date: 2019-01-01

Fund Project: 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.

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 avellanaare 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.

Key words: dinoflagellate cyst , Nanji Island , nutrients , harmful algal blooms

[1]

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

[2]

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

[3]

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

[4]

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

[5]

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

[6]

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

[7]

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

[8]

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

[9]

Dale B, Dale A L, Jansen J H F. 2002. Dinoflagellate cysts as environmental indicators in surface sediments from the Congo deep-sea fan and adjacent regions. Palaeogeography, Palaeoclimatology, Palaeoecology, 185(3–4): 309–338

[10]

Dale B, Fjellså A. 1994. Dinoflagellate cysts as paleoproductivity indicators: state of the art, potential, and limits. In: Zahn R, Pedersen 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

[11]

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

[12]

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

[13]

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

[14]

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

[15]

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

[16]

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

[17]

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

[18]

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

[19]

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

[20]

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

[21]

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

[22]

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

[23]

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

[24]

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

[25]

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 palynology, 128(1–2): 107–117

[26]

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

[27]

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

[28]

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

[29]

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

[30]

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

[31]

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

[32]

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

[33]

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

[34]

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

[35]

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

[36]

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

[37]

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

[38]

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

[39]

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

[40]

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

[41]

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

[42]

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

[43]

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

[44]

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

[45]

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

[46]

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

[47]

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

[48]

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

[49]

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

[50]

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

[51]

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

[52]

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

[53]

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

[54]

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

[55]

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

[56]

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

[57]

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

[58]

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

[59]

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

[60]

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

[61]

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

[62]

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

[1]

Yanpei ZHUANG, Haiyan JIN, Fan GU, Yang ZHANG, Youcheng BAI, Zhongqiang JI, Yong LU, Jianfang CHEN. Composition of algal pigments in surface freshen layer after ice melt in the central Arctic. ACTA OCEANOLOGICA SINICA, 2017, 36(8): 122-130. doi: 10.1007/s13131-017-1024-0

[2]

Jinglong YAO, Lei YANG, Yeqiang SHU, Lili ZENG, Rui SHI, Ju CHEN, Tingting ZU, Chuqun CHEN. Comparison of summer chlorophyll a concentration in the South China Sea and the Arabian Sea using remote sensing data. ACTA OCEANOLOGICA SINICA, 2017, 36(11): 61-67. doi: 10.1007/s13131-017-1138-4

[3]

Halim Aytekin ERGÜL, Serdar AKSAN, Merve İPŞİROĞLU. Assessment of the consecutive harmful dinoflagellate blooms during 2015 in the Izmit Bay (the Marmara Sea). ACTA OCEANOLOGICA SINICA, 2018, 37(8): 91-101. doi: 10.1007/s13131-018-1191-7

[4]

Yanzhao Yang, Zexun Wei, Guanlin Wang, Zhan Lian, Liwei Wang. The Island Rule with lateral and bottom friction. ACTA OCEANOLOGICA SINICA, 2019, 38(4): 146-153. doi: 10.1007/s13131-019-1394-6

[5]

Yaping WANG, Benwei SHI, Liang ZHANG, Jianjun JIA, Xiaomin XIA, Liang ZHOU, Rui YU, Yang YANG, Jianhua GAO. Assessing the vulnerability of changing coasts, Hainan Island, China. ACTA OCEANOLOGICA SINICA, 2017, 36(4): 114-120. doi: 10.1007/s13131-017-0972-8

[6]

Yuhang LI, Tamotsu NAGUMO, Kuidong XU. Morphology and molecular phylogeny of Pleurosira nanjiensis sp. nov., a new marine benthic diatom from the Nanji Islands, China. ACTA OCEANOLOGICA SINICA, 2018, 37(10): 33-39. doi: 10.1007/s13131-018-1298-x

[7]

Zhangxi HU, Yunyan DENG, Yuhang LI, Ying Zhong TANG. The morphological and phylogenetic characterization for the dinoflagellate Margalefidinium fulvescens (=Cochlodinium fulvescens) isolated from the Jiaozhou Bay, China. ACTA OCEANOLOGICA SINICA, 2018, 37(10): 11-17. doi: 10.1007/s13131-018-1295-0

[8]

Jian ZHOU, Jingjing SONG, Qianling BAI, Chengyue LIU, Zhipeng ZHANG, Haitian TANG. Habitat suitability of Scapharca subcrenata (Lischke) inthe shallow water of the Xiaoheishan Island. ACTA OCEANOLOGICA SINICA, 2016, 35(12): 51-57. doi: 10.1007/s13131-016-0958-y

[9]

Peng BAI, Jingling YANG, Shuwen ZHANG, Lingling XIE, Junshan WU. Upwelling off the west coast of Hainan Island: sensitivity to wave-mixing. ACTA OCEANOLOGICA SINICA, 2019, 38(10): 1-9.

[10]

Jie XIAO, Na SUN, Yiwen ZHANG, Ping SUN, Yan LI, Min PANG, Ruixiang LI. Heterocapsa bohaiensis sp. nov. (Peridiniales: Dinophyceae): a novel marine dinoflagellate from the Liaodong Bay of Bohai Sea, China. ACTA OCEANOLOGICA SINICA, 2018, 37(10): 18-27. doi: 10.1007/s13131-018-1296-z

[11]

Ke SUN, Zhongfeng QIU, Yijun HE, Wei FAN, Zexun WEI. Succession of causative species during spring blooms in the East China Sea: coupled biophysical numerical modeling. ACTA OCEANOLOGICA SINICA, 2016, 35(12): 1-11. doi: 10.1007/s13131-016-0964-0

[12]

Liang ZHAO, Yajun XU, Ye YUAN. The estimation of a critical shear stress based on a bottom tripod observation in the southwest off Jeju Island, the East China Sea. ACTA OCEANOLOGICA SINICA, 2016, 35(11): 105-112. doi: 10.1007/s13131-016-0953-3

[13]

Yang YANG, Shu GAO, Liang ZHOU, Yunwei WANG, Gaocong LI, Yaping WANG, Zhuochen HAN, Peihong JIA. Classifying the sedimentary environments of the Xincun Lagoon, Hainan Island, by system cluster and principal component analyses. ACTA OCEANOLOGICA SINICA, 2017, 36(4): 64-71. doi: 10.1007/s13131-016-0939-1

[14]

Li ZHAO, Yanchu ZHAO, Yi DONG, Yuan ZHAO, Wuchang ZHANG, Jianhong XU, Ying YU, Guangtao ZHANG, Tian XIAO. Influence of the northern Yellow Sea Cold Water Mass on picoplankton distribution around the Zhangzi Island, northern Yellow Sea. ACTA OCEANOLOGICA SINICA, 2018, 37(5): 96-106. doi: 10.1007/s13131-018-1149-9

[15]

Mingming LI, Lingling XIE, Xiaolong ZONG, Shuwen ZHANG, Lei ZHOU, Junyi LI. The cruise observation of turbulent mixing in the upwelling region east of Hainan Island in the summer of 2012. ACTA OCEANOLOGICA SINICA, 2018, 37(9): 1-12. doi: 10.1007/s13131-018-1260-y

[16]

Dawei Li, Zexun Wei, Yonggang Wang, Shujiang Li, Tengfei Xu, Guanlin Wang, Fei Teng. Characteristics and temporal variations of near-bottom currents near the Dongsha Island in the northern South China Sea. ACTA OCEANOLOGICA SINICA, 2019, 38(4): 80-89. doi: 10.1007/s13131-019-1415-5

[17]

Li Zou, Aimin Wang, Zhen Wang, Yuguo Pei, Xiaolong Liu. Experimental study of freak waves due to three-dimensional island terrain in random wave. ACTA OCEANOLOGICA SINICA, 2019, 38(6): 92-99. doi: 10.1007/s13131-019-1390-x

Metrics
  • PDF Downloads()
  • Abstract Views()
  • HTML Views()
Catalog

Figures And Tables

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

Han GAO, Shengpao YOU, Xiangdong LEI, Yunpu XIAO, Haifeng GU, Mengmeng TONG