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Decreasing nitrogen loading and climate change promotes the occurrence of nitrogen-fixing cyanobacteria in a restored city lake

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Abstract

External loading reduction has been implemented to improve water quality in China since the 2000s. To evaluate the effects of nutrient reduction on phytoplankton, long-term monitoring data for Lake Wuli from 1998 to 2017 were analyzed. After the restoration since 2003, nitrogen decreased significantly from 8 to 2 mg/l until 2008 and then remained stable until 2017, while total phosphorus declined progressively from 0.2 mg/l to approximately 0.08 mg/l during 2003 and 2017. Biological data indicated that phytoplankton biovolume decreased after restoration until 2010 and then increased slightly from 2010 to 2017, mainly due to increasing of cyanobacterial biovolume. The dominant taxa shifted from cryptophyta to cyanobacteria since 2009. The results of both nonmetric multidimensional scaling and random forest regression showed that changes in nutrients, especially decreases in nitrogen, were the main drivers for phytoplankton community variation and increasing of cyanobacterial biovolume to the total phytoplankton biovolume ratio in summer and autumn. In addition to nutrients reduction, climatic variables such as wind speed decrease also played vital roles in increasing of cyanobacterial dominance in Lake Wuli. Our study confirmed that phytoplankton community respond strongly to nitrogen reduction in the subtropics and that climate change mediates the response.

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References

  • Barone, R. & L. Naselli-Flores, 2003. Distribution and seasonal dynamics of Cryptomonads in Sicilian water bodies. Hydrobiologia 502: 325–329.

    Article  Google Scholar 

  • Borics, G., L. Nagy, S. Miron, I. Grigorszky, Z. László-Nagy, B. A. Lukács, G. László & G. Várbíró, 2013. Which factors affect phytoplankton biomass in shallow eutrophic lakes? Hydrobiologia 714: 93–104.

    Article  CAS  Google Scholar 

  • Breiman, L., 2001. Random forests. Machine Learning 45: 5–32.

    Article  Google Scholar 

  • Budd, J. W., A. M. Beeton, R. P. Stumpf, D. A. Culver & W. Charles Kerfoot, 2001. Satellite observations of Microcystis blooms in western Lake Erie. SIL Proceedings 1922–2010(27): 3787–3793.

    Google Scholar 

  • Bürgi, H. & P. Stadelmann, 2002. Change of phytoplankton composition and biodiversity in Lake Sempach before and during restoration. Hydrobiologia 469: 33–48.

    Article  Google Scholar 

  • Cai, L. L., G. W. Zhu, Y. P. Wang, G. Gao & B. Q. Qin, 2011. Influences of comprehensive treatment on water quality in Wuli Bay of Taihu Lake. Journal of Hohai University (Natural Sciences) 39: 482–488.

    CAS  Google Scholar 

  • Carpenter, S. R., 2008. Phosphorus control is critical to mitigating eutrophication. Proceedings of the National Academy of Sciences 105: 11039–11040.

    Article  CAS  Google Scholar 

  • Chaffin, J. D., T. B. Bridgeman & D. L. Bade, 2013. Nitrogen constrains the growth of late summer cyanobacterial blooms in Lake Erie. Advances in Microbiology 3: 16.

    Article  CAS  Google Scholar 

  • Chen, Y., B. Qin, K. Teubner & M. T. Dokulil, 2003. Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. Journal of Plankton Research 25: 445–453.

    Article  Google Scholar 

  • Chen, K. N., C. H. Bao & W. P. Zhou, 2009. Ecological restoration in eutrophic Lake Wuli: a large enclosure experiment. Ecological Engineering 35: 1646–1655.

    Article  Google Scholar 

  • Cronberg, G., 1982. Changes in the phytoplankton of Lake Trummen induced by restoration. In Lakes and Water Management. Springer, Dordrecht: 185–193.

  • Dai, P., M. Yan, Y. Zhou, Y. Zhou, M. Xiong, J. Lu & K. Liu, 2018. Ecological characteristics of phytoplankton community structure in the littoral zone of Lake Wuli, Lake Taihu in 2014-2015. Resources and Environment in the Yangtze Basin 27: 2348–2357.

    Google Scholar 

  • Daley, R. D. & F. R. Pick, 1990. Phytoplankton biomass and composition of Kootenay Lake, British Columbia, following reductions in phosphorus loading. SIL Proceedings 1922–2010(24): 314–318.

    Google Scholar 

  • Deng, J. M., B. Q. Qin, H. W. Paerl, Y. L. Zhang, J. R. Ma & Y. W. Chen, 2014a. Earlier and warmer springs increase cyanobacterial (Microcystis spp.) blooms in subtropical Lake Taihu, China. Freshwater Biology 59: 1076–1085.

    Article  Google Scholar 

  • Deng, J. M., B. Q. Qin, H. W. Paerl, Y. L. Zhang, P. Wu, J. R. Ma & Y. W. Chen, 2014b. Effects of nutrients, temperature and their interactions on spring phytoplankton community succession in Lake Taihu, China. PLoS ONE 9: e113960.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deng, J. M., H. W. Paerl, B. Q. Qin, Y. Zhang, G. Zhu, E. Jeppesen, Y. Cai & H. Xu, 2018a. Climatically-modulated decline in wind speed may strongly affect eutrophication in shallow lakes. Science of the Total Environment 645: 1361–1370.

    Article  CAS  PubMed  Google Scholar 

  • Deng, J. M., W. Zhang, B. Q. Qin, Y. L. Zhang, H. W. Paerl & N. Salmaso, 2018b. Effects of climatically-modulated changes in solar radiation and wind speed on spring phytoplankton community dynamics in Lake Taihu, China. PLoS ONE 13: e0205260.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deng, J. M., N. Salmaso, E. Jeppesen, B. Q. Qin & Y. L. Zhang, 2019. The relative importance of weather and nutrients determining phytoplankton assemblages differs between seasons in large Lake Taihu, China. Aquatic Sciences 81: 48.

    Article  CAS  Google Scholar 

  • Duan, H., R. Ma, X. Xu, F. Kong, S. Zhang, W. Kong, J. Hao & L. Shang, 2009. Two-decade reconstruction of algal blooms in China’s Lake Taihu. Environmental Science & Technology 43: 3522–3528.

    Article  CAS  Google Scholar 

  • Fei, L., J. M. Deng, B. Q. Qin, G. W. Zhu, S. P. Zuo, J. Sarvala, A. M. Ventela & T. Kirkkala, 2016. Phytoplankton community response to the increasing summer daily minimum temperature in Lake Pyhäjärvi, Finland. Journal of Lake Sciences 28: 592–598.

    Article  Google Scholar 

  • Harding, L., C. Gallegos, E. Perry, W. Miller, J. Adolf, M. Mallonee & H. Paerl, 2016. Long-term trends of nutrients and phytoplankton in Chesapeake Bay. Estuaries Coasts 39: 664.

    Article  CAS  Google Scholar 

  • Hu, H. J., R. Y. Li & Y. X. Wei, 1980. Freshwater Algae in China. Shanghai Science and Technology Press, Shanghai.

    Google Scholar 

  • Jeppesen, E., M. Søndergaard, J. P. Jensen, K. E. Havens, O. Anneville, L. Carvalho, M. F. Coveney, R. Deneke, M. T. Dokulil & B. Foy, 2005. Lake responses to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.

    Article  CAS  Google Scholar 

  • Jeppesen, E., M. Søndergaard, M. Meerhoff, T. L. Lauridsen & J. P. J. H. Jensen, 2007. Shallow lake restoration by nutrient loading reduction – some recent findings and challenges ahead. Hydrobiologia 584: 239–252.

    Article  CAS  Google Scholar 

  • Jin, X. C. & Q. Y. Tu, 1990. The Standard Methods for Observation and Analysis of Lake Eutrophication. China Environmental Science Press, Beijing.

    Google Scholar 

  • Jöhnk, K. D., J. Huisman, J. Sharples, B. Sommeijer, P. M. Visser & J. M. Stroom, 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology 14: 495–512.

    Article  Google Scholar 

  • Kozak, A., K. Kowalczewska-Madura, R. Gołdyn & A. Czart, 2014. Phytoplankton composition and physicochemical properties in Lake Swarzędzkie (midwestern Poland) during restoration: preliminary results. Archives of Polish Fisheries 22: 17–28.

    Article  CAS  Google Scholar 

  • Li, X. Y., B. Li & X. L. Sun, 2014. Effects of a coastal power plant thermal discharge on phytoplankton community structure in Zhanjiang Bay, China. Marine Pollution Bulletin 81: 210–217.

    Article  CAS  PubMed  Google Scholar 

  • Lorenzen, C. J., 1967. Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnology and Oceanography 12(2): 343–346.

    Article  CAS  Google Scholar 

  • Nõges, P., T. Nõges, M. Ghiani, F. Sena, R. Fresner, M. Friedl & J. Mildner, 2011. Increased nutrient loading and rapid changes in phytoplankton expected with climate change in stratified South European lakes: sensitivity of lakes with different trophic state and catchment properties. Hydrobiologia 667: 255–270.

    Article  CAS  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2008. Blooms like it hot. Science 320: 57–58.

    Article  CAS  PubMed  Google Scholar 

  • Paerl, H. W., N. S. Hall & E. S. Calandrino, 2011. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Science of the Total Environment 409: 1739–1745.

    Article  CAS  PubMed  Google Scholar 

  • Peng, Y., L. Liu, L. Jiang & L. Xiao, 2017. The roles of cyanobacterial bloom in nitrogen removal. Science of the Total Environment 609: 297–303.

    Article  CAS  PubMed  Google Scholar 

  • Peñuelas, J., J. Sardans, A. Rivas-ubach & I. A. Janssens, 2012. The human-induced imbalance between C, N and P in Earth’s life system. Global Change Biology 18: 3–6.

    Article  Google Scholar 

  • Peñuelas, J., B. Poulter, J. Sardans, P. Ciais, M. Van Der Velde, L. Bopp, O. Boucher, Y. Godderis, P. Hinsinger & J. Llusia, 2013. Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications 4: 2934.

    Article  PubMed  CAS  Google Scholar 

  • Qin, B. Q., G. Gao, G. W. Zhu, Y. L. Zhang, Y. Z. Song, X. M. Tang, H. Xu & J. M. Deng, 2013. Lake eutrophication and its ecosystem response. Chinese Science Bulletin 58: 961–970.

    Article  CAS  Google Scholar 

  • Qin, B. Q., H. W. Paerl, J. D. Brookes, J. Liu, E. Jeppesen, G. W. Zhu, Y. L. Zhang, H. Xu, K. Shi & J. M. Deng, 2019. Why Lake Taihu continues to be plagued with cyanobacterial blooms through 10 years (2007–2017) efforts. Science Bulletin 64: 354–356.

    Article  CAS  Google Scholar 

  • Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Melo, 2002. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24: 417–428.

    Article  Google Scholar 

  • Rosińska, J., A. Kozak, R. Dondajewska & R. Gołdyn, 2017. Cyanobacteria blooms before and during the restoration process of a shallow urban lake. Journal of Environmental Management 198: 340–347.

    Article  PubMed  CAS  Google Scholar 

  • Salmaso, N. & J. Padisák, 2007. Morpho-functional groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578: 97–112.

    Article  Google Scholar 

  • Salmaso, N., L. Naselli-Flores & J. Padisák, 2015. Functional classifications and their application in phytoplankton ecology. Freshwater Biology 60: 603–619.

    Article  Google Scholar 

  • Schindler, D. W., 1977. Evolution of phosphorus limitation in lakes. Science 195: 260–262.

    Article  CAS  PubMed  Google Scholar 

  • Schindler, D. W., 2012. The dilemma of controlling cultural eutrophication of lakes. Proceedings of the Royal Society B: Biological Sciences 279(1746): 4322–4333.

    Article  CAS  PubMed  Google Scholar 

  • Schindler, D. W., R. E. Hecky, D. L. Findlay, M. P. Stainton, B. R. Parker, M. J. Paterson, K. G. Beaty, M. Lyng & S. E. M. Kasian, 2008. Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proceedings of the National Academy of Sciences 105(32): 11254–11258.

    Article  CAS  Google Scholar 

  • Seip, K. L., 1994. Phosphorus and nitrogen limitation of algal biomass across trophic gradients. Aquatic Sciences 56: 16–28.

    Article  Google Scholar 

  • Shatwell, T. & J. Köehler, 2019. Decreased nitrogen loading controls summer cyanobacterial blooms without promoting nitrogen-fixing taxa: long-term response of a shallow lake. Limnology and Oceanography 64: S166–S178.

    Article  CAS  Google Scholar 

  • Smith, V. H., 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221: 669–671.

    Article  CAS  PubMed  Google Scholar 

  • Smith, V. H., 2003. Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science Pollution Research 10: 126–139.

    Article  CAS  PubMed  Google Scholar 

  • Song, X., Z. Liu, H. Pan, G. Yang & Y. Chen, 2007. Phytoplankton community structure in Meiliang Bay and Lake Wuli of Lake Taihu. Journal of Lake Science 19: 643–651.

    Article  CAS  Google Scholar 

  • Sotero-Santos, R. B., E. G. Carvalho, M. J. Dellamano-Oliveira & O. Rocha, 2008. Occurrence and toxicity of an Anabaena bloom in a tropical reservoir (Southeast Brazil). Harmful Algae 7: 590–598.

    Article  CAS  Google Scholar 

  • Straub, C., P. Quillardet, J. Vergalli, N. T. De Marsac & J.-F. Humbert, 2011. A day in the life of Microcystis aeruginosa strain PCC 7806 as revealed by a transcriptomic analysis. PLoS ONE 6: e16208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong, Y., W. Zhang, X. Wang, R.-M. Couture, T. Larssen, Y. Zhao, J. Li, H. Liang, X. Liu, X. Bu, W. He, Q. Zhang & Y. Lin, 2017. Decline in Chinese lake phosphorus concentration accompanied by shift in sources since 2006. Nature Geoscience 10: 1–6.

    Article  CAS  Google Scholar 

  • Vrede, T., A. Ballantyne, C. Mille-Lindblom, G. Algesten, C. Gudasz, S. Lindahl & A. K. Brunberg, 2009. Effects of N:P loading ratios on phytoplankton community composition, primary production and N fixation in a eutrophic lake. Freshwater Biology 54(2): 331–344.

    Article  CAS  Google Scholar 

  • Wang, J., Z. Fu, H. Qiao & F. Liu, 2019. Assessment of eutrophication and water quality in the estuarine area of Lake Wuli, Lake Taihu, China. Science of the Total Environment 650: 1392–1402.

    Article  CAS  PubMed  Google Scholar 

  • Wood, S. N., 2006. Generalized Additive Models: An Introduction with R. Chapman & CRC Press, Boca Raton.

    Book  Google Scholar 

  • Xie, Y., 2015. Grey relational analysis of algae density and water quality factors in Lake Wuli. Journal of Green Science and Technology 12: 193–196.

    Google Scholar 

  • Xu, H., H. W. Paerl, G. Zhu, B. Qin, N. S. Hall & M. Zhu, 2017. Long-term nutrient trends and harmful cyanobacterial bloom potential in hypertrophic Lake Taihu, China. Hydrobiologia 787: 229–242.

    Article  CAS  Google Scholar 

  • Zhang, B., Y. F. Li, X. Jiang, S. H. Wang & J. C. Hu, 2013. Influences of environmental governance project on spatial distribution of phosphorus in Lihu Lake. Chinese Environmental Science 33: 1271–1279.

    Google Scholar 

  • Zhang, Y., B. Qin, G. Zhu, K. Shi & Y. Zhou, 2018. Profound changes in the physical environment of Lake Taihu from 25 years of long-term observations: implications for algal bloom outbreaks and aquatic macrophyte loss. Water Resources Research 54: 4319–4331.

    Article  Google Scholar 

  • Zhou, Y. Q., J. R. Ma, Y. L. Zhang, B. Q. Qin, E. Jeppesen, K. Shi, J. D. Brookes, R. G. M. Spencer, G. W. Zhu & G. Gao, 2017. Improving water quality in China: environmental investment pays dividends. Water Research 118: 152–159.

    Article  CAS  PubMed  Google Scholar 

  • Zhuang, Y., X. Tang, Y. Sheng, Y. Peng, Z. Dongyun & H. Zou, 2014. The study on water environmental improvement of Lihu Lake for 10 years comprehensive treatment projects. Arid Environmental Monitoring 28: 49–54.

    Google Scholar 

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Acknowledgements

The study was jointly supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA23040201), the Major Science and Technology Program for Water Pollution Control and Treatment (Grant No. 2017ZX07203-004), the National Natural Science Foundation of China (Grant No. 41621002), the Key Research Program of Frontier Sciences, CAS (Grant No. QYZDB-SSW-DQC016), the Natural Science Foundation of Jiangsu Province, China (Grant No. BK20171517), and “One-Three-Five” Strategic Planning of Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences (Grant No. Y7SL061003). We would like to thank the Taihu Laboratory for Lake Ecosystem Research (TLLER) for providing long-term monitoring data on Lake Wuli. Phytoplankton data from 1998 to 2010 were provided by Dr. Yuwei Chen. We also appreciate Erik Jeppesen from Aarhus University for his helpful comments and suggestion on our manuscript and two anonymous reviewers for their useful comments and constructive suggestions for this manuscript.

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Deng, J., Tang, X., Qin, B. et al. Decreasing nitrogen loading and climate change promotes the occurrence of nitrogen-fixing cyanobacteria in a restored city lake. Hydrobiologia 847, 2963–2975 (2020). https://doi.org/10.1007/s10750-020-04299-7

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