Skip to main content

Advertisement

SpringerLink
Log in

Predicting Ecological Distribution of the Toxic Dinoflagellate Alexandrium minutum in China Sea Using Ecological Niche Modeling

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

Alexandrium minutum from the China Sea produces a range of toxins and causes damage to the local ecosystems and aquaculture. This is essential to understand environmental factors affecting potential distribution. Potential distributions of A. minutum in the China Sea were predicted based on maximum entropy modeling, and dominant environmental variables were studied through analyses of variable contributions and response curves. The results showed that highly suitable areas were mainly located in the southwest of the Yellow Sea, the Laizhou Bay, and north of Haizhou Bay. The coast of the South China Sea was predicted as a low-suitability area, and the coast of the East China Sea as an unsuitable area. Mean temperature of the coldest month (T_min) had the largest drop in permutation importance but a low percent contribution. The probability of presence of A. minutum increased with increasing concentration of nitrate (NO −3 ) and annual mean temperature (T_ann) over a wide range of them. The response curves decreased with increasing concentration of phosphate (PO 3−4 ) and ratio of NO −3 to PO 3−4 (N_P_ratio) when PO 3−4 is above 0.049 µmol L−1 and N_P_ratio above 4, indicating that low values of PO 3−4 concentration and N_P_ratio favour the occurrence of A. minutum. As a predictor, the variance of annual temperature (T_Var) had the highest percent contribution and gains. PO 3−4 was predicted to have much more information than the other variables, and exhibited the second largest drop in permutation importance and percent contribution. The T_Var and PO 3−4 are the most important dominant predictor variables.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Altmann, A., Toloşi, L., Sander, O., and Lengauer, T., 2010. Permutation importance: An unbiased feature importance measure. Bioinformatics, 26 (10): 1340–1347, DOI: https://doi.org/10.1093/bioinformatics/btq134, PMID20385727.

    Article  Google Scholar 

  • Bertram, J., Newman, E. A., and Dewar, R. C., 2019. Comparison of two maximum entropy models highlights the metabolic structure of metacommunities as a key determinant of local community assembly. Ecological Modelling, 407: 108720.

    Article  Google Scholar 

  • Caroppo, C., Pagliara, P., Azzaro, F., Miserocchi, S., and Azzaro, M., 2017. Late summer phytoplankton blooms in the changing polar environment of the Kongsfjorden (Svalbard, Arctic). Cryptogamie Algologie, 38 (1): 53–72.

    Article  Google Scholar 

  • Chang, F. H., and Mcclean, M., 1997. Growth responses of Alexandrium minutum (Dinophyceae) as a function of three different nitrogen sources and irradiance. New Zealand Journal of Marine and Freshwater Research, 31 (1): 1–7.

    Article  Google Scholar 

  • Chen, T., Song, S., Liu, Y., and Liu, C., 2019. The 2015–2016 annual variation of dinoflagellate community and Amoebophrya infections in the Changjiang (Yangtze) River Estuary and adjacent waters. Oceanologia et Limnologia Sinica, 50 (1): 143–152.

    Google Scholar 

  • Duan, J. Q., and Zhou, G. S., 2011. Potential distribution of rice in China and its climate characteristics. Acta Ecologica Sinica, 31 (22): 6659–6668.

    Google Scholar 

  • Elith, J., Phillips, S. J., Hastie, T., Dudík, M., Chee, Y. E., and Yates, C. J., 2011. A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17 (1): 43–57.

    Article  Google Scholar 

  • Fahnenstiel, G., Hong, Y., Millie, D., Doblin, M., Johengen, T., and Reid, D., 2009. Marine dinoflagellate cysts in the ballast. International Association of Theoretical and Applied Limnology, 30: 1035–1038.

    Google Scholar 

  • Glibert, P. M., Landsberg, J. H., Evans, J. J., Al-Sarawi, M. A., Faraj, M., Al-Jarallah, M. A., et al., 2002. A fish kill of massive proportion in Kuwait Bay, Arabian Gulf, 2001: The roles of bacterial disease, harmful algae, and eutrophication. Harmful Algae, 1 (2): 215–231.

    Article  Google Scholar 

  • Gu, H., Wu, Y., Lu, S., Lu, D., Tang, Y., and Qi, Y., 2022. Emerging harmful algal bloom species over the last four decades in China. Harmful Algae, 111: 102059, DOI: https://doi.org/10.1016/j.hal.2021.102059.

    Article  Google Scholar 

  • Gu, H., Zeng, N., Liu, T., Yang, W., Müller, A., and Krock, B., 2013. Morphology, toxicity, and phylogeny of Alexandrium (Dinophyceae) species along the coast of China. Harmful Algae, 27: 68–81.

    Article  Google Scholar 

  • Hallegraeff, G., 1993. A review of harmful blooms and their apparent global increase. Phycologia, 32: 79–99.

    Article  Google Scholar 

  • Hao, S., Liu, L., Chen, J., He, X., and Lian, Z., 2021. Effects of acidification and high N/P ratios on toxin production in Alexandrium minutum. Marine Science, 45 (2): 1–10.

    Google Scholar 

  • Huang, S., Wang, X., and Zhang, L., 2012. Effects of phosphorus concentration on growth and toxin production of two species of toxic Alexandrium. Journal of Hydroecology, 33 (1): 107–111.

    Google Scholar 

  • Huang, S., Wang, X., and Zhang, L., 2015. Effects of different temperatures on tiny Alexandria algae growth and algae virulence. Scientific Fish Farming, 31 (11): 59–60.

    Google Scholar 

  • Hwang, D. F., and Lu, Y. H., 2000. Influence of environmental and nutritional factors on growth, toxicity, and toxin profile of dinoflagellate alexandrium minutum. Toxicon, 38 (11): 1491–1503.

    Article  Google Scholar 

  • Ignatiades, L., Gotsis-Skretas, O., and Metaxatos, A., 2007. Field and culture studies on the ecophysiology of the toxic dinoflagellate Alexandrium minutum (Halim) present in Greek coastal waters. Harmful Algae, 6 (2): 153–165.

    Article  Google Scholar 

  • IPCC, 2019. Summary for policymakers (M/OL). In: IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. 2019 (2020-02-10). https://www.ipcc.ch/srocc/IPCC.

  • Jiang, B., Song, L., Shi, M., Song, G., and Wang, Y., 2015. Invasion status of marine microalgae related to Red Tide in Liaoning inshore. Fisheries Science, 34 (12): 795–800.

    Google Scholar 

  • Lewis, A. M., Coates, L. N., Turner, A. D., Percy, L., and Lewis, J., 2018. A review of the global distribution of Alexandrium minutum (Dinophyceae) and comments on ecology and associated paralytic shellfish toxin profiles, with a focus on northern Europe. Journal of Phycology, 54 (5): 581–598.

    Article  Google Scholar 

  • Li, H., Zhang, Y., Tang, H., Shi, X., Rivkin, R. B., and Legendre, L., 2017. Spatiotemporal variations of inorganic nutrients along the Jiangsu coast, China, and the occurrence of macroalgal blooms (green tides) in the southern Yellow Sea. Harmful Algae, 63: 164–172.

    Article  Google Scholar 

  • Li, J., Chang, H., Liu, T., and Zhang, C., 2019. The potential geographical distribution of haloxylon across Central Asia under climate change in the 21st century. Agricultural and Forest Meteorology, 275: 243–254.

    Article  Google Scholar 

  • Li, P., Ma, Q., Xu, S., Liu, W., Ma, Z., and Ni, G., 2021. Opposite growth responses of Alexandrium minutum and Alexandrium catenella to photoperiods and temperatures. Plants, 10 (6): 1056.

    Article  Google Scholar 

  • Li, R., and Wu, Y., 2010. Effects of unbalance nitrate and phosphate ratios on toxin production of Alexandrium minutum. Marine Environmental Science, 29: 504–508.

    Google Scholar 

  • Lim, P. T., Leaw, C. P., Usup, G., Kobiyama, A., and Ogata, T., 2010. Effects of light and temperature on growth, nitrate uptake, and toxin production of two tropical dinoflagellates: Alexandrium tamiyavanichii and Alexandrium minutum (Dinophyceae). Journal of Phycology, 42 (4): 786–799.

    Article  Google Scholar 

  • Lim, P. T., Sato, S., Chu, V. T., Tu, P. T., and Ogata, T., 2007. Toxic Alexandrium minutum (Dinophyceae) from Vietnam with new gonyautoxin analogue. Harmful Algae, 6 (3): 321–331.

    Article  Google Scholar 

  • Lippemeier, S., Frampton, D. M., Blackburn, S. I., Stute, S. C., and Negri, A. P., 2003. Influence of phosphorus on toxicity and photosynthesis of Alexandrium minutum (Dinophyceae) monitored by in-line detection of variable chlorophyll fluorescence. Journal of Phycology, 39 (2): 320–331.

    Article  Google Scholar 

  • Liu, L. Y., 2020. Effects of eutrophication and acidification environment on the growth and toxin production of Alexandrium minutum based on liquid chromatography-mass spectrometry. PhD thesis, Shandong University, China.

    Google Scholar 

  • Liu, M. L., Krock, B., Yu, R. C., Leawd, C. P., Lim, P. T., Ding, G. M., et al., 2022. Co-occurrence of Alexandrium minutum (Dinophyceae) ribotypes from the Chinese and Malaysian coastal waters and their toxin production. Harmful Aalgae, 115: 102238.

    Article  Google Scholar 

  • Luckett, D. J., Laber, E. B., El-Kamary, S. S., Fan, C., Jhaveri, R., Perou, C. M., et al., 2020. Receiver operating characteristic curves and confidence bands for support vector machines. Biometrics, (2): 13365, DOI: https://doi.org/10.1111/biom.13365, PMID 328 65820.

  • Melo-Merino, S. M., Reyes-Bonilla, H., and Lira-Noriega, A., 2020. Ecological niche models and species distribution models in marine environments: A literature review and spatial analysis of evidence. Ecological Modelling, (1): 415, DOI: https://doi.org/10.1016/j.ecolmodel.2019.108837, PMID 108837.

  • Meshgi, B., Majidi-Rad, M., Hanafi-Bojd, A. A., and Fathi, S., 2019. Ecological niche modeling for predicting the habitat suitability of fascioliasis based on maximum entropy model in southern Caspian Sea littoral, Iran. Acta Trop, 198: 105079, DOI: https://doi.org/10.1016/j.actatropica.2019.105079.

    Article  Google Scholar 

  • Mi, T., Yao, Q., Meng, J., Zhang, X., and Liu, S., 2012. Distributions of nutrients in the southern Yellow Sea and East China Sea in spring and summer 2011. Oceanologia et Limnologia Sinica, 43 (3): 678–688.

    Google Scholar 

  • Narale, D. D., and Anil, A. C., 2017. Spatial distribution of dinoflagellates from the tropical coastal waters of the South Andaman, India: Implications for coastal pollution monitoring. Marine Pollution Bulletin, 115 (1/2): 498–506.

    Article  Google Scholar 

  • Narale, D. D., Patil, J. S., and Anil, A. C., 2013. Dinoflagellate cyst distribution in recent sediments along the south-east coast of India. Oceanologia, 55: 979–1003.

    Article  Google Scholar 

  • Orlova, T. Y., Morozova, T. V., Gribble, K. E., Kulis, D. M., and Anderson, D. M., 2004. Dinoflagellate cysts in recent marine sediments from the east coast of Russia. Botanica Marina, 47 (3): 184–201.

    Article  Google Scholar 

  • Pei, L., Hu, W., Wang, P., Kang, J., Mohamed, H. F., Wang, C., et al., 2022. Morphologic and phylogenic characterization of two bloom-forming planktonic Prorocentrum (Dinophyceae) species and their potential distribution in the China Sea. Algal Research, 66: 102788.

    Article  Google Scholar 

  • Phillips, S. J., and Dudík, M., 2008. Modeling of species distributions with MaxEnt: New extensions and a comprehensive evaluation. Ecography, 31: 161–175.

    Article  Google Scholar 

  • Phillips, S. J., Anderson, R. P., and Schapire, R. E., 2004. A maximum entropy approach to species distribution modeling. Proceedings of the Twenty-First International Conference on Machine Learning. Banff, Alberta, 655–662.

  • Phillips, S. J., Anderson, R. P., and Schapire, R. E., 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190 (3–4): 231–59, DOI: https://doi.org/10.1016/j.ecolmodel.2005.03.026.

    Article  Google Scholar 

  • Phillips, S. J., Anderson, R. P., Dudík, M., Schapire, R. E., and Blair, M. E., 2017. Opening the black box: An open-source release of MaxEnt. Ecography, 40: 887–893.

    Article  Google Scholar 

  • Ranston, E. R., Webber, D. F., and Larsen, J., 2007. The first description of the potentially toxic dinoflagellate, Alexandrium minutum in Hunts Bay, Kingston Harbour, Jamaica. Harmful Algae, 6 (1): 29–47.

    Article  Google Scholar 

  • Sara, M. M., Héctor, R., and Andrés, L., 2020. Ecological niche models and species distribution models in marine environments: A literature review and spatial analysis of evidence. Ecological Modelling, 415: 108837.

    Article  Google Scholar 

  • Saupe, E. E., Barve, V., Myers, C. E., Soberón, J., Barve, N., Hensz, C. M., et al., 2012. Variation in niche and distribution model performance: The need for a priori assessment of key causal factors. Ecological Modeling, 237–238: 11–22, DOI: https://doi.org/10.1016/j.ecolmodel.2012.04.001.

    Article  Google Scholar 

  • Shi, Y., Liu, D., Shao, H., Di, B., and Dong, Z., 2011. Distribution of dinoflagellate cysts in the surface sediments from the northern Yellow Sea, China. Marine Science Bulletin, 30 (3): 320–327.

    Google Scholar 

  • Shumway, S. E., 1990. A review of the effects of algal blooms on shellfish and aquaculture. Journal of the World Aquaculture Society, 21: 65–104.

    Article  Google Scholar 

  • Tang, X., Yu, R., Zhou, M., and Yu, Z., 2012. Application of rRNA probes and fluorescence in situ hybridization for rapid detection of the toxic dinoflagellate Alexandrium minutum. Chinese Journal of Oceanologia and Limnologia, 30 (2): 256–263.

    Article  Google Scholar 

  • Vila, M., Giacobbe, M. G., Maso, M., Gangemi, E., Penna, A., Sampedro, N., et al., 2005. A comparative study on recurrent blooms of Alexandrium minutum in two Mediterranean coastal areas. Harmful Algae, 4 (4): 673–695.

    Article  Google Scholar 

  • Wang, R., Li, F. C., and Shi, Z., 2017. Predicting potential ecological distribution of Locusta migratoria tibetensis in China using MaxEnt ecological niche modeling. Acta Ecologica Sinica, 37 (24): 8556–8566.

    Google Scholar 

  • Wang, Y., Yu, X., Fang, L., Liu, Q., Ren, B., and Luo, H., 2017. Influences of nutrient environment on growth and toxin productivity of Alexandrium minutum C4. Journal of Fisheries of China, 41 (10): 1588–1598.

    Google Scholar 

  • Xie, P., Gu, Y., Sui, W., Tao, G., and Sun, S., 2019. Big data challenges for species distribution models in predicting potential distribution of marine species. Marine Information, 34 (1): 51–61.

    Google Scholar 

  • Xu, Y., He, X., Li, H., Zhang, T., Lei, F., Gu, H., et al., 2021. Molecular identification and toxin analysis of Alexandrium spp. in the Beibu Gulf: First report of toxic A. tamiyavanichii in Chinese coastal waters. Toxins, 13 (2): 161.

    Article  Google Scholar 

  • Yan, P., Feng, L., Zhao, Y., Feng, L., Zhu, Z., Qu, Y., et al., 2020. Predicting the potential distribution of an invasive species, Erigeron canadensis L., in China with a maximum entropy model. Global Ecology and Conservation, 21: e00822.

    Article  Google Scholar 

  • Yang, S., Xiong, H., Chen, Y., Ma, Q., Yang, H., Xing, X., et al., 2004. Risk analysis of red tidal algae imported into Xiamen port by ship ballast water. Inspection and Quarantine Science, 14: 96–99.

    Google Scholar 

  • Yang, X. L., Yang, C. J., Hu, C. Y., and Zhang, X. M., 2017. Application of species distribution models in the prediction of marine potential habitat: A review. Yingyong Shengtai Xuebao, 28 (6): 2063–2072, DOI: https://doi.org/10.13287/j.1001-9332.201706.006, PMID 29745172.

    Google Scholar 

  • Yi, X., Zhang, K., Liu, R., Giesy, J. P., Li, Z., Li, W., et al., 2020. Transcriptomic responses of Artemia salina exposed to an environmentally relevant dose of Alexandrium minutum cells or Gonyautoxin2/3. Chemosphere, 238: 124661, DOI: https://doi.org/10.1016/j.chemosphere.2019.124661.

    Article  Google Scholar 

  • Yoshida, M., 2008. Alexandrium spp. (Dinophyceae) in the western North Pacific. Fisheries Science, 68 (2): 511–514.

    Google Scholar 

  • Yu, R. C., and Zhou, M. J., 1998. Advances in research of paralytic shellfish poisoning. Oceanologia et Limnologia Sinica, 29 (3): 330–338.

    Google Scholar 

  • Zhang, D. H., Hu, Y. M., and Liu, M., 2019. Potential distribution of Spartinal alterniflora in China coastal areas based on Maxent niche model. Yingyong Shengtai Xuebao, 30 (7): 2329–2337, DOI: https://doi.org/10.13287/j.1001-9332.201907.014, PMID 314 18236.

    Google Scholar 

  • Zhang, Q., 2004. Effects of nutrients and microorganisms on the growth and toxin production of Alexandrium minutum. PhD thesis, Graduate School of the Chinese Academy of Sciences (Institute of Oceanography), Qingdao, China.

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and the Development Program of China (No. 2019YFE 0124700), the China National Key Research and Development Program (No. 2022YFC3106002), the National Natural Science Foundation of China (No. U1901215), and the Startup Foundation for Introducing Talent of NUIST (No. 2020r028).

Author information

Authors and Affiliations

  1. School of Marine Sciences, Nanjing University of Information Science and Technology, Nanjing, 210044, China

    Changyou Wang, Ping Zheng, Haifeng Gu, Zhaohe Luo, Zhuhua Luo, Longjiang Mao & Yuanzhi Zhang

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

    Haifeng Gu & Zhuhua Luo

  3. Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, China

    Zhuhua Luo

Authors
  1. Changyou Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ping Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haifeng Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhaohe Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhuhua Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Longjiang Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuanzhi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Changyou Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Zheng, P., Gu, H. et al. Predicting Ecological Distribution of the Toxic Dinoflagellate Alexandrium minutum in China Sea Using Ecological Niche Modeling. J. Ocean Univ. China 22, 1119–1128 (2023). https://doi.org/10.1007/s11802-023-5422-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-023-5422-y

Key words

Search

Navigation