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Density-dependent effects of omnivorous bitterling (Acheilognathus macropterus) on nutrient and plankton communities: implications for lake management and restoration

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Abstract

Shallow lakes are dominated by small omnivorous fish, but the roles of these small fish in aquatic ecosystems are not well-known. A small omnivorous bitterling (Acheilognathus macropterus) has been found to be dominant after lake restoration in shallow lakes. We conducted a mesocosm experiment to examine the effects of bitterling on water quality and plankton communities. Bitterling significantly increased the concentrations of nutrients, chlorophyll a (Chla) and suspended solids (TSS), and decreased the light intensity. The abundance and biomass of phytoplankton in the fish-present treatment were significantly higher than the controls, with Microcystis spp. and Dolichospermum spp. dominating the phytoplankton community. However, bitterling did not significantly affect the abundance and biomass of zooplankton, although the presence of bitterling shifted the community structure to dominance by small-sized species. Density-dependent effects of bitterling were observed on the concentrations of nutrient, TSS, organic suspended solids and Chla and on light intensity, but were not found for plankton and ratio of zooplankton to phytoplankton biomass. Our study indicates that A. macropterus can negatively affect water quality and facilitate the dominance of cyanobacteria. Therefore, monitoring and control of these small omnivorous species should be emphasized when restoring or managing shallow lakes.

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References

  • Attayde, J. L. & L.-A. Hansson, 2001. The relative importance of fish predation and excretion effects on planktonic communities. Limnology and Oceanography 46: 1001–1012.

    Google Scholar 

  • Azim, M. E., M. C. J. Verdegem, M. Singh, A. A. V. Dam & M. C. M. Beveridge, 2003. The effects of periphyton substrate and fish stocking density on water quality, phytoplankton, periphyton and fish growth. Aquaculture Research 34: 685–695.

    Google Scholar 

  • Breukelaar, A. W., E. H. R. R. Lammens, J. G. P. K. Breteler & I. Tátrai, 1994. Effects of benthivorous bream (Abramis brama) and carp (Cyprinus carpio) on sediment resuspension and concentrations of nutrients and chlorophyll a. Freshwater Biology 32: 113–121.

    Google Scholar 

  • Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and composition of plankton. Science 150: 28–35.

    CAS  PubMed  Google Scholar 

  • Cai, X., S. Ye, W. Li, H. Fan, Z. Li, T. Zhang & J. Liu, 2019. Spatio-temporal variability of small fishes related with environmental factors in a typical domestic tap water lake, Eastern China. Journal of Oceanology and Limnology 37: 278–289.

    Google Scholar 

  • Carpenter, S. R. & D. M. Lodge, 1986. Effects of submersed macrophytes on ecosystem processes. Aquatic Botany 26: 341–370.

    Google Scholar 

  • Chen, J., H. Su, G. Zhou, Y. Dai, J. Hu, Y. Zhao, Z. Liu, T. Cao, L. Ni, M. Zhang & P. Xie, 2020. Effects of benthivorous fish disturbance and snail herbivory on water quality and two submersed macrophytes. Science of the Total Environment 713: 136734.

    CAS  PubMed  Google Scholar 

  • Chiang, S. C. & N. S. Du, 1979. Fauna Sinica, Crustacea. Science Press, Beijing, Freshwater Cladocera.

    Google Scholar 

  • DeMott, W. R., R. D. Gulati & E. Van Donk, 2001. Daphnia food limitation in three hypereutrophic Dutch lakes: evidence for exclusion of large-bodied species by interfering filaments of cyanobacteria. Limnology and oceanography 46: 2054–2060.

    Google Scholar 

  • Dumont, H. J., I. Van de Velde & S. Dumont, 1975. The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19: 75–97.

    PubMed  Google Scholar 

  • González-Bergonzoni, I., M. Meerhoff, T. A. Davidson, F. Teixeira-de Mello, A. Baattrup-Pedersen & E. Jeppesen, 2012. Meta-analysis shows a consistent and strong latitudinal pattern in fish omnivory across ecosystems. Ecosystems 15: 492–503.

    Google Scholar 

  • Gu, J., H. Jin, H. He, X. Ning, J. Yu, B. Tan, E. Jeppesen & K. Li, 2016. Effects of small-sized crucian carp (Carassius carassius) on the growth of submerged macrophytes: implications for shallow lake restoration. Ecological engineering 95: 567–573.

    Google Scholar 

  • Gu, J., H. He, H. Jin, J. Yu, E. Jeppesen, R. W. Nairn & K. Li, 2018. Synergistic negative effects of small-sized benthivorous fish and nitrogen loading on the growth of submerged macrophytes–relevance for shallow lake restoration. Science of the Total Environment 610: 1572–1580.

    PubMed  Google Scholar 

  • Guiry, M. D. & G. M. Guiry, 2020. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. 2017. http://www.algaebase.org

  • Han, Y., J. Gu, Q. Li, Y. Zhang, H. He, R. Shen & K. Li, 2019. Effects of juvenile crucian carp (Carassius carassius) removal on submerged macrophyte growth—implications for subtropical shallow lake restoration. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-019-07217-0.

    Article  PubMed  Google Scholar 

  • He, H., E. Hu, J. Yu, X. Luo, K. Li, E. Jeppesen & Z. Liu, 2017. Does turbidity induced by Carassius carassius limit phytoplankton growth? A mesocosm study. Environmental Science and Pollution Research 24: 5012–5018.

    CAS  PubMed  Google Scholar 

  • He, H., H. Jin, E. Jeppesen, K. Li, Z. Liu & Y. Zhang, 2018. Fish-mediated plankton responses to increased temperature in subtropical aquatic mesocosm ecosystems: implications for lake management. Water Research 144: 304–311.

    CAS  PubMed  Google Scholar 

  • He, H., Y. Han, Q. Li, E. Jeppesen, K. Li, J. Yu & Z. Liu, 2019. Crucian carp (Carassius carassius) strongly affect C/N/P stoichiometry of suspended particulate matter in shallow warm water eutrophic lakes. Water 11: 524.

    CAS  Google Scholar 

  • Holopainen, I. J., W. M. Tonn & C. A. Paszkowski, 1992. Effects of fish density on planktonic communities and water quality in a manipulated forest pond. Hydrobiologia 243(244): 311–321.

    Google Scholar 

  • Hu, H., 2006. The Freshwater Algae of China: Systematics. Science Press, Beijing, Taxonomy and Ecology.

    Google Scholar 

  • Huang, X. F., 1999. Survey Observation and Analysis of Lake Ecology. Standards Press of China, Beijing.

    Google Scholar 

  • Jeppesen, E., T. L. Lauridsen, T. Kairesalo & M. R. Perrow, 1998. Impact of submerged macrophytes on fish-zooplankton interactions in lakes. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 91–114.

    Google Scholar 

  • Jeppesen, E., J. P. Jensen, C. Jensen, B. Faafeng, D. O. Hessen, M. Søndergaard, T. Lauridsen, P. Brettum & K. Christoffersen, 2003. The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: a study of 466 lakes from the temperate zone to the arctic. Ecosystems 6: 313–325.

    CAS  Google Scholar 

  • Jeppesen, E., P. Nõges, T. A. Davidson, J. Haberman, T. Nõges, K. Blank, T. L. Lauridsen, M. Søndergaard, C. Sayer, R. Laugaste, L. S. Johansson, R. Bjerring & S. L. Amsinck, 2011. Zooplankton as indicators in lakes: a scientific-based plea for including zooplankton in the ecological quality assessment of lakes according to the European Water Framework Directive (WFD). Hydrobiologia 676: 279.

    CAS  Google Scholar 

  • Jeppesen, E., M. Søndergaard, T. L. Lauridsen, T. A. Davidson, Z. Liu, N. Mazzeo, C. Trochine, K. Özkan, H. S. Jensen, D. Trolle, F. Starling, X. Lazzaro, L. S. Johansson, R. Bjerring, L. Liboriussen, S. E. Larsen, F. Landkildehus, S. Egemose & M. Meerhoff, 2012. Biomanipulation as a restoration tool to combat eutrophication: recent advances and future challenges. Advances in Ecological Research 47: 411–488.

    Google Scholar 

  • Jin, X. & Q. Tu, 1990. The standard methods for observation and analysis in lake eutrophication. Environmental Science, Beijing.

    Google Scholar 

  • Koutrakis, E. T., A. K. Kokkinakis, A. C. Tsikliras & E. A. Eleftheriadis, 2003. Characteristics of the European bitterling Rhodeus amarus (Cyprinidae) in the Rihios river, Greece. Journal of Freshwater Ecology 18: 615–624.

    Google Scholar 

  • Liu, Z., J. Hu, P. Zhong, X. Zhang, J. Ning, S. E. Larsen, D. Chen, Y. Gao, H. He & E. Jeppesen, 2018. Successful restoration of a tropical shallow eutrophic lake: strong bottom-up but weak top-down effects recorded. Water Research 146: 88–97.

    CAS  PubMed  Google Scholar 

  • Qiu, X., X. Mei, V. Razlutskij, L. G. Rudstam, Z. Liu, C. Tong, & X. Zhang, 2019. Effects of common carp (Cyprinus carpio) on water quality in aquatic ecosystems dominated by submerged plants: a mesocosm study. Knowledge & Management of Aquatic Ecosystems 28.

  • Reynolds, R. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.

    Google Scholar 

  • Roozen, F. C. J. M., M. Lürling, H. Vlek, E. A. J. Van Der Pouw Kraan, B. W. Ibelings & M. Scheffer, 2007. Resuspension of algal cells by benthivorous fish boosts phytoplankton biomass and alters community structure in shallow lakes. Freshwater Biology 52: 977–987.

    CAS  Google Scholar 

  • Schaus, M. H. & M. J. Vanni, 2000. Effects of gizzard shad on phytoplankton and nutrient dynamics: role of sediment feeding and fish size. Ecology 81: 1701–1719.

    Google Scholar 

  • SEPA, 2002. Analytical methods for water and wastewater monitor. Chinese Environmental Science Press, Beijing.

    Google Scholar 

  • Shen, J. R. & N. S. Du, 1979. Fauna Sinica, Crustacea. Science Press, Beijing, Freshwater Copepoda.

    Google Scholar 

  • Shormann, D. E. & J. B. Cotner, 1997. The effects of benthivorous smallmouth buffalo (Ictiobus bubalus) on water quality and nutrient cycling in a shallow floodplain lake. Lake and Reservoir Management 13: 270–278.

    Google Scholar 

  • Usui, S., K. Kanou & M. Sano, 2018. Food habits of fishes in a freshwater reed belt in Lake Kitaura, eastern Japan, in summer. Fisheries Science 84: 469–476.

    CAS  Google Scholar 

  • Vanni, M. J., A. M. Bowling, E. M. Dickman, R. S. Hale, K. A. Higgins, M. J. Horgan, L. B. Knoll, W. H. Renwick & R. A. Stein, 2006. Nutrient cycling by fish supports relatively more primary production as lake productivity increases. Ecology 87: 1696–1709.

    PubMed  Google Scholar 

  • Ye, S., Z. Li, S. Lek-Ang, G. Feng, S. Lek & W. Cao, 2006. Community structure of small fishes in a shallow macrophytic lake (Niushan Lake) along the middle reach of the Yangtze River, China. Aquatic Living Resources 19: 349–359.

    Google Scholar 

  • Yu, J., Z. Liu, H. He, W. Zhen, B. Guan, F. Chen, K. Li, P. Zhong, F. Teixeira-de Mello & E. Jeppesen, 2016a. Submerged macrophytes facilitate dominance of omnivorous fish in a subtropical shallow lake: implications for lake restoration. Hydrobiologia 775: 97–107.

    CAS  Google Scholar 

  • Yu, J., Z. Liu, K. Li, F. Chen, B. Guan, Y. Hu, P. Zhong, Y. Tang, X. Zhao, H. He, H. Zeng & E. Jeppesen, 2016b. Restoration of shallow lakes in subtropical and tropical China: response of nutrients and water clarity to biomanipulation by fish removal and submerged plant transplantation. Water 8: 438.

    Google Scholar 

  • Yuan, D., Y. Yi, A. Yakupitiyage, K. Fitzimmons & J. S. Diana, 2010. Effects of addition of red tilapia (Oreochromis spp.) at different densities and sizes on production, water quality and nutrient recovery of intensive culture of white shrimp (Litopenaeus vannamei) in cement tanks. Aquaculture 298: 226–238.

    CAS  Google Scholar 

  • Zhang, Z. S. & X. F. Huang, 1991. Methods in Freshwater Plankton Study (Book in Chinese). Science Press, Beijing.

    Google Scholar 

  • Zhang, X., Z. Liu, E. Jeppesen, W. D. Taylor & L. G. Rudstam, 2016. Effects of benthic-feeding common carp and filter-feeding silver carp on benthic-pelagic coupling: implications for shallow lake management. Ecological Engineering 88: 256–264.

    Google Scholar 

  • Zhu, Y. & H. Liu, 2007. Genetic diversity and the biogeographical process of Acheilognathus macropterus revealed by sequence variations of mitochondrial cytochrome b gene. Frontiers of Biology in China 2: 450–455.

    Google Scholar 

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Acknowledgements

We are grateful to Xiaoxia Chen and Xiumei Zhang for their help in the field and laboratory assistance. The paper was improved by suggestions from 2 anonymous reviewers. This study was supported by the National Natural Science Foundation of China (41877415), National Key Research and Development Project (2017YFA0605201), and the NIGLAS 135 Project (NIGLAS2018GH01). JY was supported by the Chinese Academy of Sciences (CAS) Scholarship for a one-year research visit at the Flathead Lake Biological Station, University of Montana, United States of America.

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Authors and Affiliations

  1. State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing, 210008, Jiangsu, China

    Jinlei Yu, Ruijie Shen, Hu He, Baohua Guan & Zhengwen Liu

  2. Department of Ecology and Institute of Hydrobiology, Jinan University, 601 Huangpu Avenus West, Guangzhou, 510630, China

    Manli Xia & Zhengwen Liu

  3. Wuhan Zhiyue Water Ecological Technology Limited Company, 1208 Jiefang Avenue, Wuhan, 430020, China

    Wei Zhen

  4. Flathead Lake Biological Station, University of Montana, 32125 Bio Station Ln, Polson, Montana, 59860, USA

    James J. Elser

  5. Sino-Danish Centre for Education and Research (SDC), University of Chinese Academy of Sciences, 380 Huaibeizhuang, Huairou District, Beijing, 100190, China

    Zhengwen Liu

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  1. Jinlei Yu
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Correspondence to Jinlei Yu.

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Yu, J., Xia, M., Zhen, W. et al. Density-dependent effects of omnivorous bitterling (Acheilognathus macropterus) on nutrient and plankton communities: implications for lake management and restoration. Hydrobiologia 847, 3309–3319 (2020). https://doi.org/10.1007/s10750-020-04335-6

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