Effect of dissolved organic nitrogen on the bloom of Prorocentrum donghaiense and Karenia spp. in the East China Sea coastal waters
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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. -
Figure 6. Growth and death curves of three species of algae in the field culture experiments (a. MDON, b. TeDON, c.
$\mathrm{PO}_{4}^{3-} $ -P, d.${\mathrm{NO}}_3^- $ -N, e.${\mathrm{NH}}_4^+ $ -N; dots represent the in situ concentration in the field experiment, and dash lines represent the model fitting curves).Figure 7. Variations in nutrient concentrations in the field culture experiments (a. MDON, b. TeDON, c.
$\mathrm{PO}_{4}^{3-} $ -P, d.${\mathrm{NO}}_3^- $ -N, e.${\mathrm{NH}}_4^+ $ -N; dots represent the in situ concentration in the field experiment, and dash lines represent the model fitting curves).Figure 10. The mechanism diagram of Prorocentrum donghaiense and Karenia spp. blooms. Nutrients are discharged from sewage treatment plants and aquaculture tailwater and transported from southwest to northeast with the Taiwan Strait Current, which promotes the dinoflagellate blooms and diatom-dinoflagellate regime shifts. The dinoflagellate regime shift loop is P. donghaiense dominant in phase Ⅰ for the ambient eutrophic DIN and TeDON, whereas Karenia spp. was dominant in phase Ⅱ for the exhaust of DIN and MDON released from P. donghaiense in the coastal waters of the East China Sea.
Table 1. Nutrient concentration (μmol·L−1) setting for the field cultivation experiment
Number Add $\mathrm{NH}_{4}^{+} $-N $\mathrm{NO}_{3}^{-} $-N $\mathrm{NO}_{2}^{-} $-N DON PN $\mathrm{PO}_{4}^{3-} $-P DOP PP Blank group / 1.34 5.84 1.07 32.85 7.95 0.21 0.42 1.71 Control group $\mathrm{NH}_{4}^{+} $-N 5.81 5.03 1.27 37.33 10.66 0.19 1.34 1.78 A MDON 4.38 10.64 0.1 50.67 16.64 0.26 2.74 0.92 B TeDON 3.91 10.79 1.78 42.43 16.26 0.23 2.51 1.18 C $\mathrm{PO}_{4}^{3-} $-P 3.87 7.45 0.47 35.21 16.87 1.29 1.34 1.76 D $\mathrm{NO}_{3}^{-} $-N 3.87 34.61 0.47 35.21 16.83 0.28 1.30 1.71 E $\mathrm{NH}_{4}^{+} $-N 26.77 5.65 1.18 33.26 16.14 0.24 1.32 1.85 Note: The microalgae were filtered through a 0.45 μm glass fiber filter membrane in the blank group. Table 2. Parameters of the NTPD model maximum growth, death, uptake of diatoms and dinoflagellates (P. donghaiense and K. mikimotoi); half-saturation constants of dissolved nitrogen of diatoms and dinoflagellates (P. donghaiense and K. mikimotoi); ammonium oxidation rate constants
Parameter Description Unit P. donghaiense K. mikimotoi Diatom KG maximum growth rate constant d−1 0.60 0.50 0.20 KD maximum death rate constant d−1 0.20 0.10 0.01 Kup_$\mathrm{NH}_{4}^{+} $ maximum uptake rate constants for $\mathrm{NH}_{4}^{+} $-N d−1 0.40 0.10 0.20 Kup_$\mathrm{NO}_{3}^{-} $ maximum uptake rate constants for $\mathrm{NO}_{3}^{-} $-N d−1 0.50 0.20 0.30 Kup_DON maximum uptake rate constants for DON d−1 0.075 0.30 0.18 Ks_$\mathrm{NH}_{4}^{+} $ half-saturation coefficients for $\mathrm{NH}_{4}^{+} $-N uptake μmol/L 0.25 0.90 0.50 Ks_$\mathrm{NO}_{3}^{-} $ half-saturation coefficients for $\mathrm{NO}_{3}^{-} $-N uptake μmol/L 0.75 0.60 0.16 Ks_DON half-saturation coefficients for DON uptake μmol/L 0.50 0.90 0.50 K${\mathrm{NH}}_4^+\_{\mathrm{NO}}_3^- $ maximum ammonium oxidation rate constant d−1 0.05 0.05 0.05 -
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 -