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Consumer-driven nutrient release to the water by a small omnivorous fish enhanced ramet production but reduced the growth rate of the submerged macrophyte Vallisneria denseserrulata (Makino) Makino

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Abstract

Small fish are highly associated with submerged macrophytes but may potentially hamper their growth due to nutrient excretion that stimulate growth of phytoplankton and periphyton growth. We conducted a mesocosm experiment to elucidate the effects of the small omnivore Chinese bitterling Acheilognathus macropterus on the growth of phytoplankton, periphyton and the submerged macrophyte Vallisneria denseserrulata. The treatments were fishless as well as low (LF) and high (HF) fish density. We found that the concentrations of nutrients and the phytoplankton biomass increased substantially in both fish treatments, leading to a significantly higher light attenuation compared with the control. Moreover, bitterling substantially enhanced the biomass of periphyton on plant leaves. Consequently, the relative growth rate (RGR) of V. denseserrulata was significantly suppressed in HF, while RGR in the LF treatment did not differ significantly from the controls. However, the bitterling also stimulated the ramet production of V. denseserrulata, significantly. Our results indicate that Chinese bitterling reduce the RGR of V. denseserrulata under high fish density condition. Therefore, the density of Chinese bitterling should be kept low in order to reduce the negative effects of the fish on the RGR of submerged macrophytes (e.g. V. denseserrulata), when restoring lakes by plant transplantation.

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References

  • Bajer, P. G. & P. W. Sorensen, 2015. Effects of common carp on phosphorus concentrations, water clarity, and vegetation density: a whole system experiment in a thermally stratified lake. Hydrobiologia 746: 303–311.

    Article  CAS  Google Scholar 

  • Best, M. D. & K. E. Mantai, 1978. Growth of Myriophyllum: sediment or lake water as the source of nitrogen and phosphorus. Ecology 59: 1075–1080.

    Article  CAS  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.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chambers, P. A. & J. Kalff, 1987. Light and nutrients in the control of aquatic plant community structure. I. in situ experiments. Journal of Ecology 75: 611–619.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chen, Z., D. Zhao, M. Li, W. Tu, X. Luo & X. Liu, 2020b. A field study on the effects of combined biomanipulation on the water quality of a eutrophic lake. Environmental Pollution 265: 15091.

    Article  CAS  PubMed  Google Scholar 

  • Cronin, G. & D. M. Lodge, 2003. Effects of light and nutrient availability on the growth, allocation, carbon/nitrogen balance, phenolic chemistry, and resistance to herbivory of two freshwater macrophytes. Oecologia 137: 32–41.

    Article  PubMed  Google Scholar 

  • Denny, P., 1972. Sites of nutrient absorption in aquatic macrophytes. Journal of Ecology 60: 819–829.

    Article  Google Scholar 

  • Duarte, C. M., 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41: 87–112.

    Article  Google Scholar 

  • Duarte, C. M., J. Kalff & R. H. Peters, 1986. Patterns in biomass and cover of aquatic macrophytes in lakes. Canadian Journal of Fisheries and Aquatic Sciences 43: 1900–1908.

    Article  Google Scholar 

  • Gao, J., Z. Liu & E. Jeppesen, 2014. Fish community assemblages changed but biomass remained similar after lake restoration by biomanipulation in a Chinese tropical eutrophic lake. Hydrobiologia 724: 127–140.

    Article  CAS  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.

    Article  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.

    Article  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.

    Article  CAS  PubMed  Google Scholar 

  • Han, Y., J. Gu, Q. Li, Y. Zhang, H. He, R. Shen & K. Li, 2020. Effects of juvenile crucian carp (Carassius carassius) removal on submerged macrophyte growth—implications for subtropical shallow lake restoration. Environmental Science and Pollution Research 27: 42198–42209.

    Article  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.

    Article  CAS  Google Scholar 

  • Hilt, S., K. V. Weyer, A. de Köhler & I. Chorus, 2010. Submerged macrophyte responses to reduced phosphorus concentrations in two peri-urban lakes. Restoration Ecology 18: 452–461.

    Article  Google Scholar 

  • Hilt, S., M. M. Alirangues Nuñez, E. S. Bakker, I. Blindow, T. A. Davidson, M. Gillefalk, L. A. Hansson, J. H. Janse, A. B. G. Janssen, E. Jeppesen, T. Kabus, A. Kelly, J. Köhler, T. L. Lauridsen, W. M. Mooij, R. Noordhuis, G. Phillips, J. Rücker, H.-H. Schuster, M. Søndergaard, S. Teurlincx, K. van de Weyer, E. van Donk, A. Waterstraat, N. Willby & C. D. Sayer, 2018. Response of submerged macrophyte communities to external and internal restoration measures in north temperate shallow lakes. Frontiers in Plant Science 9: 194.

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang, Y., X. Mei, L. G. Rudstam, W. D. Taylor, J. Urabe, E. Jeppesen, Z. Liu & X. Zhang, 2020. Effects of crucian carp (Carassius auratus) on water quality in aquatic ecosystems: an experimental mesocosm study. Water 12: 1444.

    Article  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, Ecological Studies. Springer, New York: 91–114.

    Chapter  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.

    Article  Google Scholar 

  • Jin, X. & Q. Tu, 1990. The Standard Methods for Observation and Analysis in Lake Eutrophication, 2nd ed. Environmental Science, Beijing.

    Google Scholar 

  • Jones, J. I. & C. D. Sayer, 2003. Does the fish–invertebrate–periphyton cascade precipitate plant loss in shallow lakes? Ecology 84: 2155–2167.

    Article  Google Scholar 

  • Jones, J. I., J. O. Young, J. W. Eaton & B. Moss, 2002. The influence of nutrient loading, dissolved inorganic carbon and higher trophic levels on the interaction between submerged plants and periphyton. Journal of Ecology 90: 12–24.

    Article  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.

    Article  CAS  PubMed  Google Scholar 

  • Lougheed, V. L., B. Crosbie & P. Chow-Fraser, 1998. Predictions on the effect of common carp (Cyprinus carpio) exclusion on water quality, zooplankton, and submergent macrophytes in a Great Lakes wetland. Canadian Journal of Fisheries and Aquatic Sciences 55: 1189–1197.

    Article  Google Scholar 

  • Lu, J., Z. Wang, W. Xing & G. Liu, 2013. Effects of substrate and shading on the growth of two submerged macrophytes. Hydrobiologia 700: 157–167.

    Article  Google Scholar 

  • Meerhoff, M., J. M. Clemente, F. Teixeira de Mello, C. Iglesias, A. R. Pedersen & E. Jeppesen, 2007. Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Global Change Biology 13: 1888–1897.

    Article  Google Scholar 

  • Moss, B., 2010. Climate change, nutrient pollution and the bargain of Dr Faustus. Freshwater Biology 55: 175–187.

    Article  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 420: 28.

    Article  Google Scholar 

  • Roberts, E., J. Kroker, S. Körner & A. Nicklisch, 2003. The role of periphyton during the re-colonization of a shallow lake with submerged macrophytes. Hydrobiologia 506: 525–530.

    Article  Google Scholar 

  • Sand-Jensen, K. & J. Borum, 1991. Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquatic Botany 41: 137–175.

    Article  Google Scholar 

  • Sand-Jensen, K. & T. V. Madsen, 1991. Minimum light requirements of submerged freshwater macrophytes in laboratory growth experiments. Journal of Ecology 79: 749–764.

    Article  Google Scholar 

  • Sayer, C. D., A. Burgess, K. Kari, T. A. Davidson, S. Peglar, H. Yang & N. Rose, 2010. Long-term dynamics of submerged macrophytes and algae in a small and shallow, eutrophic lake: implications for the stability of macrophyte-dominance. Freshwater Biology 55: 565–583.

    Article  CAS  Google Scholar 

  • Scheffer, M., S. H. Hosper, M.-L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275–279.

    Article  CAS  Google Scholar 

  • SEPA, 2002. Analytical Methods for Water and Wastewater Monitor, 4th ed. Chinese Environmental Science Press, Beijing.

    Google Scholar 

  • Søndergaard, M., L. S. Johansson, T. L. Lauridsen, T. B. Jørgensen, L. Liboriussen & E. Jeppesen, 2010. Submerged macrophytes as indicators of the ecological quality of lakes. Freshwater Biology 55: 893–908.

    Article  Google Scholar 

  • Stevens, J. P., 2012. Applied Multivariate Statistics for the Social Sciences, 5th ed. Routledge, London.

    Book  Google Scholar 

  • Tang, Y., B. Fu, X. Zhang & Z. Liu, 2019. Nutrient addition delivers growth advantage to Hydrilla verticillata over Vallisneria natans: a mesocosm study. Knowledge & Management of Aquatic Ecosystems 420: 12.

    Article  Google Scholar 

  • Xiao, K., D. Yu & J. Wang, 2006. Habitat selection in spatially heterogeneous environments: a test of foraging behaviour in the clonal submerged macrophyte Vallisneria spiralis. Freshwater Biology 51: 1552–1559.

    Article  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.

    Article  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.

    Article  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.

    Article  Google Scholar 

  • Yu, J., M. Xia, M. Kong, H. He, B. Guan, Z. Liu & E. Jeppesen, 2020a. A small omnivorous bitterling fish (Acheilognathus macropterus) facilitates dominance of cyanobacteria, rotifers and Limnodrilus in an outdoor mesocosm experiment. Environmental Science and Pollution Research 27: 23862–23870.

    Article  CAS  PubMed  Google Scholar 

  • Yu, J., M. Xia, W. Zhen, H. He, R. Shen, B. Guan & Z. Liu, 2020b. A small omnivore fish (Acheilognathus macropterus) reduces both growth and biomass of submerged macrophytes: implications for shallow lake restoration. Knowledge & Management of Aquatic Ecosystems 421: 34.

    Article  Google Scholar 

  • Yu, J., M. Xia, W. Zhen, R. Shen, H. He, B. Guan, J. J. Elser & Z. Liu, 2020c. Density-dependent effects of omnivorous bitterling (Acheilognathus macropterus) on nutrient and plankton communities: implications for lake management and restoration. Hydrobiologia 847: 3309–3319.

    Article  Google Scholar 

  • Yu, J., L. Yang, M. Xia, Y. Hou, H. He, B. Guan & Z. Liu, 2020d. Effects of bitterling fish on the relationships between submerged macrophytes and mussel. Journal of Lake Sciences 32: 1817–1826.

    Article  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.

    Article  Google Scholar 

  • Zhang, X., X. Mei & R. D. Gulati, 2017. Effects of omnivorous tilapia on water turbidity and primary production dynamics in shallow lakes: implications for ecosystem management. Reviews in Fish Biology and Fisheries 27: 245–254.

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to Yuanzhang Hou, Liu Yang, Mingfei Wang, Wei Zhen and Ruijie Shen for their help in the field and the laboratory and to Anne Mette Poulsen for her linguistic assistance. This study was supported by the National Natural Science Foundation of China (41877415), National Key Research and Development Project (2017YFA0605201), Natural Science Foundation of Jiangsu Province (Grant No. BK20170109) and the NIGLAS 135 Project (NIGLAS2018GH03). 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, USA. EJ was supported by AQUACOSM (Network of Leading European AQUAtic MesoCOSM Facilities Connecting Mountains to Oceans from the Arctic to the Mediterranean), AnaEE Denmark (anaee.dk) and the TÜBITAK outstanding researcher program BIDEB 2232 (Project 118C250).

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Yu, J., Xia, M., Zhao, Y. et al. Consumer-driven nutrient release to the water by a small omnivorous fish enhanced ramet production but reduced the growth rate of the submerged macrophyte Vallisneria denseserrulata (Makino) Makino. Hydrobiologia 848, 4335–4346 (2021). https://doi.org/10.1007/s10750-021-04643-5

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