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Impact of eutrophication on root morphological and topological performance in free-floating invasive and native plant species

  • Xiaolong Huang
  • Xuan Xu
  • Shuailing Liu
  • Shuli Song
  • Shaowei Chang
  • Chunhua LiuEmail author
  • Dan Yu
Primary Research Paper

Abstract

Three free-floating species that normally co-occur in the natural waters of southern China were studied—two globally introduced invasive species, Eichhornia crassipes and Pistia stratiotes, and a native counterpart, Hydrocharis dubia. The responses of the three species to different phosphorus and nitrogen levels were determined using root morphological parameters and topological indices. The results showed that P concentration levels had a significant effect on all of the root traits, except for the shoot/root ratio of P. stratiotes, whereas nitrogen had less impacts on the root traits. The root parameters consisting of lateral root number, root altitude, root length, total root length, root area, total root area, relative growth rate and root relative growth rate of E. crassipes were the highest among the three species. We found that the root branching of E. crassipes can be considered as a peculiar poly-herringbone branching system according to a new root topological structure model. The predominant root growth traits and root branching structure of E. crassipes and P. stratiotes help to explain their high absorption ability and fast growth, so the spread of these invasive species may be exacerbated as eutrophication intensifies in the future.

Keywords

Biological invasions Eutrophication Free-floating plants Root topology 

Notes

Acknowledgements

The authors acknowledge funding support from the Special Foundation of the National Science and Technology Basic Research Program (2013FY112300), the Major Science and Technology Program for Water Pollution Control and Treatment (2015ZX07503-005 and 2017ZX07203-005), and the Introducing Talent Starting Project (NIGLAS2018QD01) of the Nanjing Institute of Geography and Limnology (NIGLAS), Chinese Academy of Sciences. We are grateful to reviewers for providing helpful feedback on our work.

References

  1. Adebayo, A., E. Briski, O. Kalaci, M. Hernandez, S. Ghabooli, B. Beric, F. Chan, A. Zhan, E. Fifield, T. Leadley & H. MacIsaac, 2011. Water hyacinth (Eichhornia crassipes) and water lettuce (Pistia stratiotes) in the Great Lakes: playing with fire? Aquatic Invasions 6: 91–96.CrossRefGoogle Scholar
  2. Bai, X., K. Chen, H. Zhao & X. Chen, 2015. Impact of water depth and sediment type on root morphology of the submerged plant Vallisneria natans. Journal of Freshwater Ecology 30: 75–84.CrossRefGoogle Scholar
  3. Beklioglu, M., M. Meerfhoff, M. Søndergaard & E. Jeppesen, 2013. Eutrophication and restoration of shallow lakes from a cold temperate to a warm mediterranean and a (sub) tropical climate. In Ansari, A. A., S. S. Gill, G. R. Lanza & W. Rast (eds), Eutrophication: Causes, Consequences and Control. Springer, Dordrecht: 103.Google Scholar
  4. Berntson, G. M., 1995. The characterization of topology: a comparison of four topological indices for rooted binary trees. Journal of Theoretical Biology 177: 271–281.CrossRefGoogle Scholar
  5. Bouma, T. J., K. L. Nielsen, J. Van Hal & B. Koutstaal, 2001. Root system topology and diameter distribution of species from habitats differing in inundation frequency. Functional Ecology 15: 360–369.CrossRefGoogle Scholar
  6. Brundu, G., 2015. Plant invaders in European and Mediterranean inland waters: profiles, distribution, and threats. Hydrobiologia 746: 61–79.CrossRefGoogle Scholar
  7. Buller, L. S., I. Bergier, E. Ortega & S. M. Salis, 2013. Dynamic energy valuation of water hyacinth biomass in wetlands: an ecological approach. Journal of Cleaner Production 54: 177–187.CrossRefGoogle Scholar
  8. Bulut, Y. & H. Aydın, 2006. A kinetics and thermodynamics study of methylene blue adsorption on wheat shells. Desalination 194: 259–267.CrossRefGoogle Scholar
  9. Carpenter, S. R., 2005. Eutrophication of aquatic ecosystems: Bistability and soil phosphorus. Proceedings of the National Academy of Sciences 102: 10002–10005.CrossRefGoogle Scholar
  10. Chambers, P. A., P. Lacoul, K. J. Murphy & S. M. Thomaz, 2008. Global diversity of aquatic macrophytes in freshwater. Hydrobiologia 595: 9–26.CrossRefGoogle Scholar
  11. Coetzee, J. A. & M. P. Hill, 2012. The role of eutrophication in the biological control of water hyacinth, Eichhornia crassipes, in South Africa. Biocontrol 57: 247–261.CrossRefGoogle Scholar
  12. Comas, L. H. & D. M. Eissenstat, 2004. Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Functional Ecology 18: 388–397.CrossRefGoogle Scholar
  13. Csathó, P., I. Sisák, L. Radimszky, S. Lushaj, H. Spiegel, M. T. Nikolova, N. Nikolov, P. Čermák, J. Klir, A. Astover, A. Karklins, S. Lazauskas, J. Kopiński, C. Hera, E. Dumitru, M. Manojlovic, D. Bogdanović, S. Torma, M. Leskošek & A. Khristenko, 2007. Agriculture as a source of phosphorus causing eutrophication in Central and Eastern Europe. Soil Use and Management 23: 36–56.CrossRefGoogle Scholar
  14. Dannowski, M. & A. Block, 2005. Fractal geometry and root system structures of heterogeneous plant communities. Plant and Soil 272: 61–76.CrossRefGoogle Scholar
  15. Dawson, W., M. Fischer & M. van Kleunen, 2011. The maximum relative growth rate of common UK plant species is positively associated with their global invasiveness. Global Ecology and Biogeography 20: 299–306.CrossRefGoogle Scholar
  16. Eid, E. M. & K. H. Shaltout, 2017. Growth dynamics of water hyacinth (Eichhornia crassipes): a modeling approach. Rendiconti Lincei 28: 169–181.CrossRefGoogle Scholar
  17. Elser, J. J., M. E. S. Bracken, E. E. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin & J. E. Smith, 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1135–1142.CrossRefGoogle Scholar
  18. Engelhardt, K. A. M., 2011. Eutrophication, aquatic. In Simberloff, D. & M. Rejmánek (eds), Encyclopedia of Biological Invasions. University of California Press, Berkeley and Los Angeles: 209–210.Google Scholar
  19. Finlay, J. C., G. E. Small & R. W. Sterner, 2013. Human influences on nitrogen removal in lakes. Science 342: 247–250.CrossRefGoogle Scholar
  20. Fitter, A. H., 1986. The topology and geometry of plant root systems: influence of watering rate on root system topology in Trifolium pratese. Annals of Botany 58: 91–101.CrossRefGoogle Scholar
  21. Fitter, A. H., 1987. An architectural approach to comparative ecology of plant root systems. New Phytologist 106: 61–77.CrossRefGoogle Scholar
  22. Fitter, A. H., 2002. Characteristics and functions of root systems. In Waisel, Y., A. Eshel & U. Kafkafi (eds), Plant Roots: The Hidden Half. CRC Press, New York: 15–32.CrossRefGoogle Scholar
  23. Fitter, A. H. & T. R. Stickland, 1991. Architectural analysis of plant root systems 2. Influence of nutrient supply on architecture in contrasting plant species. New Phytologist 118: 383–389.CrossRefGoogle Scholar
  24. Fitter, A. H., T. R. Stickland, M. L. Harvey & G. W. Wilson, 1991. Architectural analysis of plant root systems 1. Architectural correlates of exploitation efficiency. New Phytologist 118: 375–382.CrossRefGoogle Scholar
  25. Gamage, N. P. D. & T. Asaeda, 2004. Population dynamics of water hyacinth (Eichhornia crassipes). Research report of the Research and Education Center for Inlandwater Environment Shinshu University 2: 35–40.Google Scholar
  26. Glass, A. D. M., 2002. Nutrient absorption by plant roots: regulation of uptake to match plant demand. In Waisel, Y., A. Eshel & U. Kafkafi (eds), Plant Roots: The Hidden Half. CRC Press, New York: 571–586.CrossRefGoogle Scholar
  27. Glimskär, A., 2000. Estimates of root system topology of five plant species grown at steady-state nutrition. Plant and Soil 227: 249–256.CrossRefGoogle Scholar
  28. Grantz, E. M., B. E. Haggard & J. T. Scott, 2014. Stoichiometric imbalance in rates of nitrogen and phosphorus retention, storage, and recycling can perpetuate nitrogen deficiency in highly-productive reservoirs. Limnology and Oceanography 59: 2203–2216.CrossRefGoogle Scholar
  29. He, H., H. Gao, G. Chen, H. Li, H. Lin & Z. Shu, 2013. Effects of perchlorate on growth of four wetland plants and its accumulation in plant tissues. Environmental Science and Pollution Research 20: 7301–7308.CrossRefGoogle Scholar
  30. Heathwaite, A. L., 2010. Multiple stressors on water availability at global to catchment scales: understanding human impact on nutrient cycles to protect water quality and water availability in the long term. Freshwater Biology 55: 241–257.CrossRefGoogle Scholar
  31. Henry-Silva, G. G., A. F. M. Camargo & M. M. Pezzato, 2008. Growth of free-floating aquatic macrophytes in different concentrations of nutrients. Hydrobiologia 610: 153–160.CrossRefGoogle Scholar
  32. Hodge, A., 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162: 9–24.CrossRefGoogle Scholar
  33. Huang, J., C. Xu, B. G. Ridoutt, X. Wang & P. Ren, 2017. Nitrogen and phosphorus losses and eutrophication potential associated with fertilizer application to cropland in China. Journal of Cleaner Production 159: 171–179.CrossRefGoogle Scholar
  34. Hussner, A., I. Stiers, M. J. J. M. Verhofstad, E. S. Bakker, B. M. C. Grutters, J. Haury, J. L. C. H. van Valkenburg, G. Brundu, J. Newman, J. S. Clayton, L. W. J. Anderson & D. Hofstra, 2017. Management and control methods of invasive alien freshwater aquatic plants: a review. Aquatic Botany 136: 112–137.CrossRefGoogle Scholar
  35. Ismail, Z., S. Z. Othman, K. H. Law, A. H. Sulaiman & R. Hashim, 2015. Comparative performance of water hyacinth (Eichhornia crassipes) and water lettuce (Pista stratiotes) in preventing nutrients build-up in municipal wastewater. Clean: Soil, Air, Water 43: 521–531.Google Scholar
  36. IUCN, 2013. Global Invasive Species Database. http://www.iucngisd.org/gisd/100_worst.php.
  37. Janssen, A. B. G., V. C. L. de Jager, J. H. Janse, X. Kong, S. Liu, Q. Ye & W. M. Mooij, 2017. Spatial identification of critical nutrient loads of large shallow lakes: Implications for Lake Taihu (China). Water Research 119: 276–287.CrossRefGoogle Scholar
  38. Jeppesen, E., M. Sondergaard, J. P. Jensen, K. E. Havens, O. Anneville, L. Carvalho, M. F. Coveney, R. Deneke, M. T. Dokulil, B. Foy, D. Gerdeaux, S. E. Hampton, S. Hilt, K. Kangur, J. Kohler, E. H. H. R. Lammens, T. L. Lauridsen, M. Manca, M. R. Miracle, B. Moss, P. Noges, G. Persson, G. Phillips, R. Portielje, S. Romo, C. L. Schelske, D. Straile, I. Tatrai, E. Willen & M. Winder, 2005. Lake responses to reduced nutrient loading: an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.CrossRefGoogle Scholar
  39. Ji, N., S. Wang & L. Zhang, 2017. Characteristics of dissolved organic phosphorus inputs to freshwater lakes: a case study of Lake Erhai, southwest China. Science of the Total Environment 601–602: 1544–1555.CrossRefGoogle Scholar
  40. Laboski, C. A. M., R. H. Dowdy, R. R. Allmaras & J. A. Lamb, 1998. Soil strength and water content influences on corn root distribution in a sandy soil. Plant and Soil 203: 239–247.CrossRefGoogle Scholar
  41. Le, C., Y. Zha, Y. Li, D. Sun, H. Lu & B. Yin, 2010. Eutrophication of lake waters in China: cost, causes, and control. Environmental Management 45: 662–668.CrossRefGoogle Scholar
  42. Low, K. S., C. K. Lee & K. K. Tan, 1995. Biosorption of basic dyes by water hyacinth roots. Bioresource Technology 52: 79–83.CrossRefGoogle Scholar
  43. McCully, M., 1995. How do real roots work? Some new views of root structure. Plant Physiology 109: 1–6.CrossRefGoogle Scholar
  44. Michelan, T. S., M. S. Dainez Filho & S. M. Thomaz, 2018. Aquatic macrophyte mats as dispersers of one invasive plant species. Brazilian Journal of Biology 78: 169–171.CrossRefGoogle Scholar
  45. Mishra, S. & A. Maiti, 2017. The efficiency of Eichhornia crassipes in the removal of organic and inorganic pollutants from wastewater: a review. Environmental Science and Pollution Research 24: 7921–7937.CrossRefGoogle Scholar
  46. OECD., 1982. Eutrophication of Waters, Monitoring, Assessment and Control. Final Report, OECD Cooperative Program on Monitoring of Inland Waters (Eutrophication Control), Environment Di- rectorate, OECD, Paris.Google Scholar
  47. Oppelt, A. L., W. Kurth & D. L. Godbold, 2001. Topology, scaling relations and Leonardo’s rule in root systems from African tree species. Tree Physiology 21: 117–128.CrossRefGoogle Scholar
  48. Pan, X., A. M. Villamagna & B. Li, 2012. Eichhornia crassipes Mart. (Solms-Laubach) (water hyacinth). In Francis, R. A. (ed.), A Handbook of Global Freshwater invasive Species. Taylor & Francis Group, London and New York: 47–56.Google Scholar
  49. Qiu, D., Z. Wu, B. Liu, J. Deng, G. Fu & F. He, 2001. The restoration of aquatic macrophytes for improving water quality in a hypertrophic shallow lake in Hubei Province, China. Ecological Engineering 18: 147–156.CrossRefGoogle Scholar
  50. Qin, B., G. Gao, G. Zhu, Y. Zhang, Y. Song, X. Tang, H. Xu & J. Deng, 2013. Lake eutrophication and its ecosystem response. Chinese Science Bulletin 58: 961–970.CrossRefGoogle Scholar
  51. Qin, H., Z. Zhang, M. Liu, H. Liu, Y. Wang, X. Wen, Y. Zhang & S. Yan, 2016. Site test of phytoremediation of an open pond contaminated with domestic sewage using water hyacinth and water lettuce. Ecological Engineering 95: 753–762.CrossRefGoogle Scholar
  52. Quilliam, R. S., M. A. van Niekerk, D. R. Chadwick, P. Cross, N. Hanley, D. L. Jones, A. J. A. Vinten, N. Willby & D. M. Oliver, 2015. Can macrophyte harvesting from eutrophic water close the loop on nutrient loss from agricultural land? Journal of Environmental Management 152: 210–217.CrossRefGoogle Scholar
  53. Ru, J., M. Liu, X. Cheng & C. Wang, 2015. The morphological study of the fruit, seed and seedling of Hydrocharis dubia (Hydrocharitaceae). Pakistan Journal of Botany 47: 1467–1472.Google Scholar
  54. Schindler, D. W., 2006. Recent advances in the understanding and management of eutrophication. Limnology and Oceanography 51: 356–363.CrossRefGoogle Scholar
  55. Schindler, D. W., 2012. The dilemma of controlling cultural eutrophication of lakes. Proceedings of the Royal Society B 279: 4322–4333.CrossRefGoogle Scholar
  56. 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: 11254–11258.CrossRefGoogle Scholar
  57. Smart, J. S., 1978. The analysis of drainage network composition. Earth Surface Processes and Landforms 3: 129–170.CrossRefGoogle Scholar
  58. Smith, V. H. & D. W. Schindler, 2009. Eutrophication science: where do we go from here? Trends in Ecology & Evolution 24: 201–207.CrossRefGoogle Scholar
  59. Smith, V. H., G. D. Tilman & J. C. Nekola, 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100: 179–196.CrossRefGoogle Scholar
  60. Tamada, K., K. Itoh, Y. Uchida, S. Higuchi, D. Sasayama & T. Azuma, 2015. Relationship between the temperature and the overwintering of water lettuce (Pistia stratiotes) at Kowataike, a branch of Yodogawa River, Japan. Weed Biology and Management 15: 20–26.CrossRefGoogle Scholar
  61. Taub, D. R. & D. Goldberg, 1996. Root system topology of plants from habitats differing in soil resource availability. Functional Ecology 10: 258–264.CrossRefGoogle Scholar
  62. Tsuchiya, T., 1989. Growth and biomass turnover of Hydrocharis dubia L. cultured under different nutrient conditions. Ecological Research 4: 157–166.CrossRefGoogle Scholar
  63. van Kleunen, M., E. Weber & M. Fischer, 2010. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecology Letters 13: 235–245.CrossRefGoogle Scholar
  64. van Pelt, J. & R. W. H. Verwer, 1983. The exact probabilities of branching patterns under terminal and segmental growth hypotheses. Bulletin of Mathematical Biology 45: 269–285.CrossRefGoogle Scholar
  65. Villamagna, A. M. & B. R. Murphy, 2010. Ecological and socio-economic impacts of invasive water hyacinth (Eichhornia crassipes): a review. Freshwater Biology 55: 282–298.CrossRefGoogle Scholar
  66. Wang, H., Q. Wang, P. Bowler & W. Xiong, 2016. Invasive aquatic plants in China. Aquatic Invasions 11: 1–9.CrossRefGoogle Scholar
  67. Wang, T., J. Hu, C. Liu & D. Yu, 2017. Soil type can determine invasion success of Eichhornia crassipes. Hydrobiologia 788: 281–291.CrossRefGoogle Scholar
  68. Waranusantigul, P., P. Pokethitiyook, M. Kruatrachue & E. S. Upatham, 2003. Kinetics of basic dye (methylene blue) biosorption by giant duckweed (Spirodela polyrrhiza). Environmental Pollution 125: 385–392.CrossRefGoogle Scholar
  69. Werner, C. & J. S. Smart, 1973. Some new methods of topologic classification of channel networks. Geographical Analysis 5: 271–295.CrossRefGoogle Scholar
  70. Wilson, J. R., N. Holst & M. Rees, 2005. Determinants and patterns of population growth in water hyacinth. Aquatic Botany 81: 51–67.CrossRefGoogle Scholar
  71. Xia, C., D. Yu, Z. Wang & D. Xie, 2014. Stoichiometry patterns of leaf carbon, nitrogen and phosphorous in aquatic macrophytes in eastern China. Ecological Engineering 70: 406–413.CrossRefGoogle Scholar
  72. Xie, Y. & D. Yu, 2003. The significance of lateral roots in phosphorus (P) acquisition of water hyacinth (Eichhornia crassipes). Aquatic Botany 75: 311–321.CrossRefGoogle Scholar
  73. Xu, H., H. W. Paerl, B. Qin, G. Zhu, N. S. Hall & Y. Wu, 2015. Determining critical nutrient thresholds needed to control harmful cyanobacterial blooms in eutrophic Lake Taihu, China. Environmental Science & Technology 49: 1051–1059.CrossRefGoogle Scholar
  74. Yan, Z., W. Han, J. Peñuelas, J. Sardans, J. J. Elser, E. Du, P. B. Reich & J. Fang, 2016. Phosphorus accumulates faster than nitrogen globally in freshwater ecosystems under anthropogenic impacts. Ecology Letters 19: 1237–1246.CrossRefGoogle Scholar
  75. You, W., D. Yu, D. Xie, L. Yu, W. Xiong & C. Han, 2014. Responses of the invasive aquatic plant water hyacinth to altered nutrient levels under experimental warming in China. Aquatic Botany 119: 51–56.CrossRefGoogle Scholar
  76. Zhang, Y., D. Zhang & S. C. H. Barrett, 2010. Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Molecular Ecology 19: 1774–1786.CrossRefGoogle Scholar
  77. Zhang, Y., E. Jeppesen, X. Liu, B. Qin, K. Shi, Y. Zhou, S. M. Thomaz & J. Deng, 2017. Global loss of aquatic vegetation in lakes. Earth-Science Reviews 173: 259–265.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.The National Field Station of the Freshwater Ecosystem of Liangzi Lake, Department of Ecology, College of Life SciencesWuhan UniversityWuhanPeople’s Republic of China
  2. 2.State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and LimnologyChinese Academy of SciencesNanjingPeople’s Republic of China

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