Effect of dissolved organic nitrogen on the bloom of <i>Prorocentrum donghaiense</i> and <i>Karenia</i> spp. in the East China Sea coastal waters

Xiaoru Cui; Guangming Zhen; Jing Zhao; Keqiang Li; Xiulin Wang

doi:10.1007/s13131-023-2308-9

Volume 43 Issue 6

Jun. 2024

Turn off MathJax

Article Contents

Article Navigation > Acta Oceanologica Sinica > 2024 > 43(6): 71-85

Xiaoru Cui, Guangming Zhen, Jing Zhao, Keqiang Li, Xiulin Wang. Effect of dissolved organic nitrogen on the bloom of Prorocentrum donghaiense and Karenia spp. in the East China Sea coastal waters[J]. Acta Oceanologica Sinica, 2024, 43(6): 71-85. doi: 10.1007/s13131-023-2308-9

Citation:

Xiaoru Cui, Guangming Zhen, Jing Zhao, Keqiang Li, Xiulin Wang. Effect of dissolved organic nitrogen on the bloom of Prorocentrum donghaiense and Karenia spp. in the East China Sea coastal waters[J]. Acta Oceanologica Sinica, 2024, 43(6): 71-85. doi: 10.1007/s13131-023-2308-9

Citation:

PDF( 2839 KB)

Effect of dissolved organic nitrogen on the bloom of Prorocentrum donghaiense and Karenia spp. in the East China Sea coastal waters

doi: 10.1007/s13131-023-2308-9

Xiaoru Cui^{1, 2},
Guangming Zhen³,
Jing Zhao^{1
,
,},
Keqiang Li^{1, 3
,
,},
Xiulin Wang^{1, 3}

1.
Key Laboratory of Marine Chemistry Theory and Technology/Frontiers Science Center for Deep Ocean Multispheres and Earth System of Ministry of Education, Ocean University of China, Qingdao 266100, China
2.
College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
3.
College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, China

Funds: The National Natural Science Foundation of China under contract No. 42130403; the Fundamental Research Funds for the Central Universities under contract No. 202362003; the National Key Research & Development Program of China under contract No. 2017YFC1404300.

More Information

Corresponding author: E-mail: zhaojing8095@ouc.edu.cn; likeqiang@ouc.edu.cn
Received Date: 2023-08-31
Accepted Date: 2024-01-15

Available Online: 2024-04-29

Publish Date: 2024-06-30

Abstract

Abstract

Understanding the mechanism of harmful algal bloom formation is vital for effectively preventing algal bloom outbreaks in coastal environments. Karenia spp. blooms in the East China Sea show a significant correlation with nutrient regimes. However, the impact of key components of nutrients, especially dissolved organic nitrogen (DON), on the blooms of Karenia spp. is not clear. Quantitative research is still lacking. In this study, the cruise observations, field mesocosm-flask culture experiments, and a multinitrogen-tri-phytoplankton-detritus model (NTPD) are combined to reveal the quantitative influence of nutrient regimes on the shift of Prorocentrum donghaiense and Karenia spp. in the East China Sea. It has a synchronism rhythm of diatom-P. donghaiense-Karenia spp.-diatom loop in the field culture experiment, which is consistent with the results of the cruise observation. The results showed that the processes of terrigenous DON (TeDON) and dissolved inorganic nitrogen (DIN: $\mathrm{NO}_{3}^{-} $-N, $\mathrm{NH}_{4}^{+} $-N) absorption promoted P. donghaiense to become the dominant algae in the community; whereas the processes of DON from P. donghaiense absorption promoted Karenia spp. to become the dominant algae in ambient DIN exhaustion. In addition, the three-dimensional fluorescence components of humus C, tyrosine and fulvic acid can indicate the processes of growth and extinction of P. donghaiense and Karenia spp., respectively. This study infers that P. donghaiense and Karenia spp. regime shift mechanism associated with the nutrient regime in coastal waters, which provides a scientific basis for the environmental management of coastal ecosystem health.
- Karenia spp.,
- Prorocentrum donghaiense,
- nutrients,
- multinitrogen-tri-phytoplankton-detritus model,
- three-dimensional fluorescence

FullText(HTML)

References(73)

References

An Xinlong, Li Xuemei, Yao Qiang. 2011. Two new recorded species of Alexandrium tamarense in Hebei Province-Karenia mikimotoi Hansen and Protoperidinium leonis Balech. Journal of Anhui Agricultural Sciences (in Chinese), 39(2): 631

Anderson D M, Glibert P M, Burkholder J M. 2002. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries, 25(4): 704–726, doi: 10.1007/BF02804901

Antia N J, Harrison P J, Oliveira L. 1991. The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology. Phycologia, 30(1): 1–89, doi: 10.2216/i0031-8884-30-1-1.1

Boyer J N, Kelble C R, Ortner P B, et al. 2009. Phytoplankton bloom status: Chlorophyll a biomass as an indicator of water quality condition in the southern estuaries of Florida, USA. Ecological Indicators, 9(6): S56–S67, doi: 10.1016/j.ecolind.2008.11.013

Brand L E, Compton A. 2007. Long-term increase in Karenia brevis abundance along the Southwest Florida Coast. Harmful Algae, 6(2): 232–252, doi: 10.1016/j.hal.2006.08.005

Buchan A, LeCleir G R, Gulvik C A, et al. 2014. Master recyclers: Features and functions of bacteria associated with phytoplankton blooms. Nature Reviews Microbiology, 12(10): 686–698, doi: 10.1038/nrmicro3326

Carlsson P, Granéli E, Tester P, et al. 1995. Influences of riverine humic substances on bacteria, protozoa, phytoplankton, and copepods in a coastal plankton community. Marine Ecology Progress Series, 127: 213–221, doi: 10.3354/meps127213

Cen Jingyi, Wang Jianyan, Huang Lifen, et al. 2020. Who is the “murderer” of the bloom in coastal waters of Fujian, China, in 2019?. Journal of Oceanology and Limnology, 38(3): 722–732, doi: 10.1007/s00343-019-9178-6

Chen Kan, Li Keqiang, Gao Peiyi, et al. 2022. Was dissolved nitrogen regime driving diatom to dinoflagellate shift in the Bohai Sea? Evidences from microcosm experiment and modeling reproduction. Journal of Geophysical Research: Biogeosciences, 127(6): e2021JG006737, doi: 10.1029/2021JG006737

Chen Baohong, Wang Kang, Guo Huige, et al. 2021. Karenia mikimotoi blooms in coastal waters of China from 1998 to 2017. Estuarine, Coastal and Shelf Science, 249: 107034, doi: 10.1016/j.ecss.2020.107034

Ding Guangmao, Zhang Shufeng. 2018. Ecological characteristics and the causes of Karenia mikimotoi bloom in the Sansha Bay in 2012. Haiyang Xuebao (in Chinese), 40(6): 104–112, doi: 10.3969/j.issn.0253-4193.2018.06.010

Fujian Provincial Department of Ocean and Fisheries. 2019. Fujian’s Ocean Disaster Report, http://hyyyj.fujian.gov.cn/(in Chinese [2020-09-07/2022-06-21]

Glibert P M, Burkholder M J. 2011. Harmful algal blooms and eutrophication: “strategies” for nutrient uptake and growth outside the Redfield comfort zone. Chinese Journal of Oceanology and Limnology, 29(4): 724–738, doi: 10.1007/s00343-011-0502-z

Glibert P M, Wilkerson F P, Dugdale R C, et al. 2014. Phytoplankton communities from San Francisco Bay Delta respond differently to oxidized and reduced nitrogen substrates-even under conditions that would otherwise suggest nitrogen sufficiency. Frontiers in Marine Science, 1: 17, doi: 10.3389/fmars.2014.00017

Harrison P J, Furuya K, Glibert P M, et al. 2011. Geographical distribution of red and green Noctiluca scintillans. Chinese Journal of Oceanology and Limnology, 29(4): 807–831, doi: 10.1007/s00343-011-0510-z

Heil C A, Dixon L K, Hall E, et al. 2014. Blooms of Karenia brevis (Davis) G. Hansen & Ø. Moestrup on the West Florida Shelf: Nutrient sources and potential management strategies based on a multi-year regional study. Harmful Algae, 38: 127–140, doi: 10.1016/j.hal.2014.07.016

Heisler J, Glibert P M, Burkholder J M, et al. 2008. Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae, 8(1): 3–13, doi: 10.1016/j.hal.2008.08.006

Hu Chuanmin, Muller-Karger F E, Swarzenski P W. 2006. Hurricanes, submarine groundwater discharge, and Florida’s red tides. Geophysical Research Letters, 33(11): L11601, doi: 10.1029/2005GL025449

Huang Bangqin, Ou Linjian, Hong Huasheng, et al. 2005. Bioavailability of dissolved organic phosphorus compounds to typical harmful dinoflagellate Prorocentrum donghaiense Lu. Marine Pollution Bulletin, 51(8−12): 838–844, doi: 10.1016/j.marpolbul.2005.02.035

Huang C, Qi Y. 1997. The abundance cycle and influence factors on red tide phenomena of Noctiluca scintillans (Dinophyceae) in Dapeng Bay, the South China Sea. Journal of Plankton Research, 19(3): 303–318, doi: 10.1093/plankt/19.3.303

Imai I, Yamaguchi M, Hori Y. 2006. Eutrophication and occurrences of harmful algal blooms in the Seto Inland Sea, Japan. Plankton and Benthos Research, 1(2): 71–84, doi: 10.3800/pbr.1.71

Jeong H J, Lim A S, Lee K, et al. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. Temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae, 32(2): 101–130, doi: 10.4490/algae.2017.32.5.30

Killberg-Thoreson L, Mulholland M R, Heil C A, et al. 2014. Nitrogen uptake kinetics in field populations and cultured strains of Karenia brevis. Harmful Algae, 38: 73–85, doi: 10.1016/j.hal.2014.04.008

Kwon H K, Kim G, Han Yongjin, et al. 2019. Tracing the sources of nutrients fueling dinoflagellate red tides occurring along the coast of Korea using radium isotopes. Scientific Reports, 9(1): 15319, doi: 10.1038/s41598-019-51623-w

Lai Junxiang, Yu Zhiming, Song Xiuxian, et al. 2011. Responses of the growth and biochemical composition of Prorocentrum donghaiense to different nitrogen and phosphorus concentrations. Journal of Experimental Marine Biology and Ecology, 405(1−2): 6–17, doi: 10.1016/j.jembe.2011.05.010

Li Xiaodong, Yan Tian, Yu Rencheng, et al. 2019. A review of Karenia mikimotoi: Bloom events, physiology, toxicity and toxic mechanism. Harmful Algae, 90: 101702, doi: 10.1016/j.hal.2019.101702

Lin Jianing, Yan Tian, Zhang Qingchun, et al. 2014. In situ detrimental impacts of Prorocentrum donghaiense blooms on zooplankton in the East China Sea. Marine Pollution Bulletin, 88(1−2): 302–310, doi: 10.1016/j.marpolbul.2014.08.026

Lin Jianing, Yan Tian, Zhang Qingchun, et al. 2016. Impact of several harmful algal bloom (HAB) causing species, on life history characteristics of rotifer Brachionus plicatilis Müller. Chinese Journal of Oceanology and Limnology, 34(4): 642–653, doi: 10.1007/s00343-016-5065-6

Liu Chunqiang. 2012. Effects of nutrient on the community succession of six marine microalgae (in Chinese)[dissertation]. Qingdao: Ocean University of China

Liu Zhiqiang, Gan Jianping, Hu Jianyu, et al. 2021. Progress on circulation dynamics in the East China Sea and southern Yellow Sea: Origination, pathways, and destinations of shelf currents. Progress in Oceanography, 193: 102553, doi: 10.1016/j.pocean.2021.102553

Liu Gang, Janowitz G S, Kamykowski D. 2001. A biophysical model of population dynamics of the autotrophic dinoflagellate Gymnodinium breve. Marine Ecology Progress Series, 210: 101–124, doi: 10.3354/meps210101

Long Hua, Du Qi, 2005. Primary research on Karenia mikimotoi bloom in Fujian coast. Journal of Fisheries Research (in Chinese), (4): 22–26, doi: 10.14012/j.cnki.fjsc.2005.04.006

Lv Songhui, Cen Jingyi, Wang Jianyan, et al. 2019. The research status quo, hazard, and ecological mechanisms of Karenia mikimotoi red tide in coastal waters of China. Oceanologia et Limnologia Sinica (in Chinese), 50(3): 487–494, doi: 10.11693/hyhz2018 1000255

Lv Honggang, Zhang Xihui, Gong Chunying, et al. 2005. Studies on the algorithm and identification of three dimensional fluorescence spectroscopy of algae. China Environmental Science (in Chinese), 25(5): 581–584

Marques A C, Veras C E, Kumpel E, et al. 2024. Assessment of nutrients and conductivity in the Wachusett Reservoir watershed: An investigation of land use contributions and trends. International Soil and Water Conservation Research, 12(2): 337–350, doi: 10.1016/j.iswcr.2023.07.004

Massi L, Frittitta L, Melillo C, et al. 2020. Seasonal dynamic of CDOM in a shelf site of the South-Eastern Ligurian sea (Western Mediterranean). Journal of Marine Science and Engineering, 8(9): 703, doi: 10.3390/jmse8090703

Mathew T, Prakash S, Baliarsingh S K, et al. 2021. Response of phytoplankton biomass to nutrient stoichiometry in coastal waters of the western Bay of Bengal. Ecological Indicators, 131: 108119, doi: 10.1016/j.ecolind.2021.108119

Medina M, Huffaker R, Jawitz J W, et al. 2020. Seasonal dynamics of terrestrially sourced nitrogen influenced Karenia brevis blooms off Florida’s southern gulf coast. Harmful Algae, 98: 101900, doi: 10.1016/j.hal.2020.101900

Mulholland M R, Bernhardt P W, Heil C A, et al. 2006. Nitrogen fixation and release of fixed nitrogen by Trichodesmium spp. in the Gulf of Mexico. Limnology and Oceanography, 51(4): 1762–1776, doi: 10.4319/lo.2006.51.4.1762

Nielsen T, Ekelund N G A. 1993. Effect of UV-B radiation and humic substances on growth and motility of Gyrodinium aureolum. Limnology and Oceanography, 38(7): 1570–1575, doi: 10.4319/lo.1993.38.7.1570

O’Neil J M, Heil C A. 2014. Nutrient dynamics of Karenia brevis red tide blooms in the eastern Gulf of Mexico. Harmful Algae, 38: 1–140, doi: 10.1016/j.hal.2014.08.004

Park J, Kim G, Kwon H K, et al. 2022. Origins and characteristics of dissolved organic matter fueling harmful dinoflagellate blooms revealed by δ¹³C and D/L-Amino acid compositions. Scientific Reports, 12(1): 15052, doi: 10.1038/s41598-022-19168-7

Parker A E, Hogue V E, Wilkerson F P, et al. 2012. The effect of inorganic nitrogen speciation on primary production in the San Francisco Estuary. Estuarine, Coastal and Shelf Science, 104–105: 91–101, doi: 10.1016/j.ecss.2012.04.001

Parsons T R, Maita Y, Lalli C M. 1984. Determination of chlorophylls and total carotenoids: spectrophotometric method. In: Parsons T R, Maita Y, Lalli C M, eds. A Manual of Chemical & Biological Methods for Seawater Analysis. Amsterdam: Elsevier, 101–104, doi: 10.1016/B978-0-08-030287-4.50032-3

Stedmon C A, Bro R. 2008. Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial. Limnology and Oceanography: Methods, 6(11): 572–579, doi: 10.4319/lom.2008.6.572

Steidinger K A. 2009. Historical perspective on Karenia brevis red tide research in the Gulf of Mexico. Harmful Algae, 8(4): 549–561, doi: 10.1016/j.hal.2008.11.009

Strickland J D H, Parsons T R. 1970. A Practical Handbook of Seawater Analysis. Ottawa: Fisheries Research Board of Canada, doi: 10.1002/iroh.19700550118

Tester P A, Shea D, Kibler S R, et al. 2008. Relationships among water column toxins, cell abundance and chlorophyll concentrations during Karenia brevis blooms. Continental Shelf Research, 28(1): 59–72, doi: 10.1016/j.csr.2007.04.007

Tilney C L, Shankar S, Hubbard K A, et al. 2019. Is Karenia brevis really a low-light-adapted species?. Harmful Algae, 90: 101709, doi: 10.1016/j.hal.2019.101709

van de Poll W H, Kulk G, Timmermans K R, et al. 2013. Phytoplankton chlorophyll a biomass, composition, and productivity along a temperature and stratification gradient in the northeast Atlantic Ocean. Biogeosciences, 10(6): 4227–4240, doi: 10.5194/bg-10-4227-2013

Vargo G A, Heil C A, Fanning K A, et al. 2008. Nutrient availability in support of Karenia brevis blooms on the central West Florida Shelf: what keeps Karenia blooming?. Continental Shelf Research, 28(1): 73–98, doi: 10.1016/j.csr.2007.04.008

Wang Xuejing. 2015. Effects of urea on the growth of typical algae in the East China Sea (in Chinese)[dissertation]. Qingdao: Ocean University of China

Wang Yan, Liu Yongjian, Guo Hao, et al. 2022. Long-term nutrient variation trends and their potential impact on phytoplankton in the southern Yellow Sea, China. Acta Oceanologica Sinica, 41(6): 54–67, doi: 10.1007/s13131-022-2031-3

Wang Yujue, Liu Dongyan, Xiao Wupeng, et al. 2021. Coastal eutrophication in China: trend, sources, and ecological effects. Harmful Algae, 107: 102058, doi: 10.1016/j.hal.2021.102058

Wang Jinhui, Qin Yutao, Liu Caicai, et al. 2006. The preliminary investigation of potentially toxic algae and bio-toxin in Changjiang Estuary. Marine Environmental Science (in Chinese), 25(S1): 52–61

Wasmund N, Kownacka J, Göbel J, et al. 2017. The diatom/dinoflagellate index as an indicator of ecosystem changes in the Baltic Sea 1. Principle and handling instruction. Frontiers in Marine Science, 4: 22, doi: 10.3389/fmars.2017.00022

Wilkerson F P, Dugdale R C, Hogue V E, et al. 2006. Phytoplankton blooms and nitrogen productivity in San Francisco Bay. Estuaries and Coasts, 29(3): 401–416, doi: 10.1007/BF02784989

Xia Wei. 2016. Study on molecular response mechanism of Prorocentrum donghaiense Lu and Karenia mikimotoi Hansen grown into nitrogen limitation or phosphorus limitation (in Chinese)[dissertation]. Guangzhou: Jinan University

Xiao Xi, Agustí S, Pan Yaoru, et al. 2019. Warming amplifies the frequency of harmful algal blooms with eutrophication in Chinese coastal waters. Environmental Science & Technology, 53(22): 13031–13041, doi: 10.1021/acs.est.9b03726

Xiao Wupeng, Liu Xin, Irwin A J, et al. 2018a. Warming and eutrophication combine to restructure diatoms and dinoflagellates. Water Research, 128: 206–216, doi: 10.1016/j.watres.2017.10.051

Xiao Wupeng, Wang Lei, Laws E, et al. 2018b. Realized niches explain spatial gradients in seasonal abundance of phytoplankton groups in the South China Sea. Progress in Oceanography, 162: 223–239, doi: 10.1016/j.pocean.2018.03.008

Yan Tian, Zhou Mingjiang. 2004. Environmental and health effects associated with Harmful Algal Bloom and marine algal toxins in China. Biomedical and Environmental Sciences, 17(2): 165–176

Yao Weimin, Pan Xiaodong, Hua Dandan. 2007. A preliminary study on the origin of red tide of Karenia mikimotoi in Zhejiang waters. Reservoir Fisheries (in Chinese), 27(6): 57–58,76

Yih W, Kim H S, Jeong H J, et al. 2004. Ingestion of cryptophyte cells by the marine photosynthetic ciliate Mesodinium rubrum. Aquatic Microbial Ecology, 36(2): 165–170, doi: 10.3354/ame 036165

Yin Kedong, Song Xiuxian, Liu Sheng, et al. 2008. Is inorganic nutrient enrichment a driving force for the formation of red tides? A case study of the dinoflagellate Scrippsiella trochoidea in an embayment. Harmful Algae, 8(1): 54–59, doi: 10.1016/J.HAL.2008.08.004

Yin Gaofang, Zhao Nanjing, Hu Li, et al. 2014. Classified measurement of Phytoplankton based on characteristic fluorescence of photosynthetic pigments. Acta Optica Sinica (in Chinese), 34(9): 0930005, doi: 10.3788/AOS201434.0930005

Zhang Jinfeng, Gao Xuelu, Li Peimiao, et al. 2015. Nutrient distribution characteristics and long-term trends in the southwest of the Laizhou Bay and its adjacent rivers. Marine Science Bulletin (in Chinese), 34(2): 222–232, doi: 10.11840/j.issn.1001-6392.2015.02.015

Zhang Xiansheng, Zhen Guangming, Cui Xiaoru, et al. 2023. Effect of dissolved organic nutrients on the bloom of Prorocentrum donghaiense in the East China Sea coastal waters. Marine Environmental Research, 183: 105841, doi: 10.1016/j.marenvres.2022.105841

Zhao Congjiao, Liu Xizhen, Fu Shengjing, et al. 2020. Variation characteristics of the evolution of Karenia mikimotoi bloom and environmental factors based on online monitoring buoy data. Journal of Tropical Oceanography (in Chinese), 39(2): 88–97, doi: 10.11978/2019027

Zhao Yanmin, Qin Yanwen, Zhang Lei, et al. 2021. Temporal and spatial distribution of red tides in the Chang-jiang Estuary and in adjacent waters from 1989 to 2019. Marine Sciences (in Chinese), 45(12): 39–46, doi: 10.11759/hykx20210220001

Zhao Nanjing, Zhang Xiaoling, Yin Gaofang, et al. 2018. On-line analysis of algae in water by discrete three-dimensional fluorescence spectroscopy. Optics Express, 26(6): A251–A259, doi: 10.1364/OE.26.00A251

Zhou Mingjiang, Shen Zhiliang, Yu Rencheng. 2008. Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research, 28(12): 1483–1489, doi: 10.1016/j.csr.2007.02.009

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

Relative Articles

Supplements(0)

Cited By

Proportional views