Journal of Oceanology and Limnology

, Volume 37, Issue 2, pp 665–674 | Cite as

Antioxidant systems of aquatic macrophytes in three life forms: a case study in Lake Erhai, China

  • Changbo Yuan
  • Tianshun Zhu
  • Te Cao
  • Yilong Xi
  • Xiaolin ZhangEmail author
  • Leyi Ni


Antioxidant systems are vital in life activities of macrophytes. Species with different life forms need to cope with distinct environments by modifying physiological characters, especially antioxidant systems. In order to find differences among life forms and consequence of lake eutrophication, we studied three antioxidant enzymes activity (superoxide dismutase SOD, ascorbate oxidase APX and catalase CAT) and total soluble phenolics (TP) content in leaves of 26 macrophyte species in September 2013 in Lake Erhai, China. We found that antioxidation varied accordingly with life forms. The activities of SOD and APX in emergent macrophytes (EM) and floating-leaved macrophytes (FM) were much lower than those of submerged macrophytes (SM). On the contrary, TP content was much higher in EM and FM species. There was a negative correlation between TP and antioxidant enzyme activities (CAT and APX). The results suggested that EM and FM species rely on phenolics might to adapt to adverse environments (higher herbivores predation pressure and UV radiation intensity), while SM species more rely on antioxidant enzymes possibly due to lower demand for antioxidation and/or lack of light and inorganic C availability for phenolics synthesis. We also found FM species represent highest fitness in term of antioxidant system, which would lead to overgrowth of FM species and littoral zone bogginess during lake eutrophication. Finally, it is necessary to carry out the verification experiment under the control condition in the later stage, especially for the dominant ones in eutrophic lakes, to understand the exact adaptive mechanisms of them.


macrophytes life forms phenolics antioxidant enzymes eutrophication 


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  1. Almeselmani M, Deshmukh P S, Sairam R K, Kushwaha S R, Singh T P. 2006. Protective role of antioxidant enzymes under high temperature stress. Plant Science, 171 (3): 382–388, Scholar
  2. Anderson D M, Glibert P M, Burkholder J M. 2002. Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences. Estuaries, 25 (4): 704–726, Scholar
  3. Barko J W, Smart R M. 1981. Comparative influences of light and temperature on the growth and metabolism of selected submersed freshwater macrophytes. Ecological Monographs, 51 (2): 219–236, Scholar
  4. Bixenmann C, López–Perea J J, Viñuela J, Florín M, Feliu J, Chicote Á, Cirujano S, Mateo R. 2016. Effects of invasive fish and quality of water and sediment on macrophytes biomass, and their consequences for the waterbird community of a Mediterranean floodplain. Science of the Total Environment, 551: 513–521, Scholar
  5. Bowes G. 1985. Pathways of CO 2 fixation by aquatic organisms. In: Lucas W J, Berry J A eds. Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms. American Society of Plant Physiologists, Rockville, Maryland. p.187–210.Google Scholar
  6. Bowler C, Van Montagu M, Inzé D. 1992. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology, 43: 83–116, Scholar
  7. Boyd C E. 1968. Fresh–water plants–a potential source of protein. Economic Botany, 22 (4): 359–368, https://doi. org/10.1007/Bf02908132.CrossRefGoogle Scholar
  8. Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry, 72 (1–2): 248–254,–2697(76)90527–3.CrossRefGoogle Scholar
  9. Bryant J P, Chapin F S, Klein D R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos, 40 (3): 357–368, Scholar
  10. Cao T, Ni L Y, Xie P. 2004. Acute biochemical responses of a submersed macrophyte, Potamogeton crispus L., to high ammonium in an aquarium experiment. Journal of Freshwater Ecology, 19 (2): 279–284, 080/02705060.2004.9664542.CrossRefGoogle Scholar
  11. Cao T, Xie P, Li Z Q, Ni L Y, Zhang M, Xu J. 2009. Physiological stress of high NH 4 + concentration in water column on the submersed macrophyte Vallisneria natans L. Bulletin of Environmental Contamination and Toxicology, 82 (3): 296–299,–008–9531–5.CrossRefGoogle Scholar
  12. Cao T, Xie P, Ni L Y, Wu A P, Zhang M, Wu S K, Smolders A J P. 2007. The role of NH 4 + toxicity in the decline of the submersed macrophyte Vallisneria natans in lakes of the Yangtze River basin, China. Marine and Freshwater Research, 58 (6): 581–587, Scholar
  13. Cao T, Xie P, Ni L Y, Wu A P, Zhang M, Xu J. 2008. Relationships among the contents of total phenolics, soluble carbohydrate, and free amino acids of 15 aquatic macrophytes. Journal of Freshwater Ecology, 23 (2): 291–296, Scholar
  14. Chance B, Maehly A C. 1955. [136] Assay of catalases and peroxidases: Catalase: 2H 2 O 2 ?2H 2 O + O 2 (1), Catalase and Peroxidase: ROOH + AH 2 ?H 2 O + ROH + A (2). Methods in Enzymology, 2: 764–775, https://doi. org/10.1016/S0076–6879(55)02300–8.CrossRefGoogle Scholar
  15. Close D C, McArthur C. 2002. Rethinking the role of many plant phenolics–protection from photodamage not herbivores? Oikos, 99 (1): 166–172, 1034/j.1600–0706.2002.990117.x.CrossRefGoogle Scholar
  16. Conley D J, Paerl H W, Howarth R W, Boesch D F, Seitzinger S P, Havens K E, Lancelot C, Likens G E. 2009. Controlling eutrophication: nitrogen and phosphorus. Science, 323 (5917): 1 014–1 015, Scholar
  17. Cronin G, Lodge D M. 2003. Effects of light and nutrient availability on the growth, allocation, carbon/nitrogen balance, phenolic chemistry, and resistance to herbivory of twofreshwater macrophytes. Oecologia, 137 (1): 32–41,–003–1315–3.CrossRefGoogle Scholar
  18. Dai Y R, Wu J, Ma X H, Zhong F, Cui N X, Cheng S P. 2017. Increasing phytoplankton–available phosphorus and inhibition of macrophyte on phytoplankton bloom. Science of the Total Environment, 579: 871–880, Scholar
  19. Dudt J F, Shure D J. 1994. The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology, 75 (1): 86–98, Scholar
  20. Frew A, Powell J R, Sallam N, Allsopp P G, Johnson S N. 2016. Trade–offs between silicon and phenolic defenses may explain enhanced performance of root herbivores on phenolic–rich plants. Journal of Chemical Ecology, 42 (8): 768–771,–016–0734–7.CrossRefGoogle Scholar
  21. Fryer G, Gaevaskaya N S, Muller D G M, Mann K H. 1970. The role of higher aquatic plants in the nutrition of the animals of freshwater basins. The Journal of Applied Ecology, 7 (2): 388–389, Scholar
  22. Hall A. 1999. Induced responses to herbivory. Plant Pathology, 48 (2): 294,–3059.1999.00340.x.CrossRefGoogle Scholar
  23. He L, Zhu T S, Cao T, Li W, Zhang M, Zhang X L, Ni L Y, Xie P. 2015. Characteristics of early eutrophication encoded in submerged vegetation beyond water quality: a case study in Lake Erhai, China. Environmental Earth Sciences, 74 (5): 3 701–3 708,–015–4202–4.CrossRefGoogle Scholar
  24. Hutchinson G E. 1957. Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology, 22: 415–427, Scholar
  25. Ibáñez C, Alcaraz C, Caiola N, Rovira A, Trobajo R, Alonso M, Duran C, Jiménez P J, Munné A, Prat N. 2012. Regime shift from phytoplankton to macrophyte dominance in a large river: top–down versus bottom–up effects. Science of the Total Environment, 416: 314–322, 1016/j.scitotenv.2011.11.059.CrossRefGoogle Scholar
  26. Klancnik K, Iskra I, Gradinjan D, Gaberšcik A. 2018. The quality and quantity of light in the water column are altered by the optical properties of natant plant species. Hydrobiologia, 812 (1): 203–212,–017–3148–9.CrossRefGoogle Scholar
  27. Larson R A. 1988. The antioxidants of higher plants. Phytochemistry, 27 (4): 969–978,–9422(88)80254–1.CrossRefGoogle Scholar
  28. Leopoldini M, Marino T, Russo N, Toscano M. 2004. Density functional computations of the energetic and spectroscopic parameters of quercetin and its radicals in the gas phase and in solvent. Theoretical Chemistry Accounts, 111 (2–6): 210–216,–003–0544–1.CrossRefGoogle Scholar
  29. Leopoldini M, Russo N, Chiodo S, Toscano M. 2006. Iron chelation by the powerful antioxidant flavonoid quercetin. Journal of Agricultural and Food Chemistry, 54 (17): 6 343–6 351, Scholar
  30. Lodge D M. 1991. Herbivory on freshwater macrophytes. Aquatic Botany, 41 (1–3): 195–224, 1016/0304–3770(91)90044–6.CrossRefGoogle Scholar
  31. Metcalfe N B, Alonso–Alvarez C. 2010. Oxidative stress as a life–history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Functional Ecology, 24 (5): 984–996, 1111/j.1365–2435.2010.01750.x.CrossRefGoogle Scholar
  32. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7 (9): 405–410,–1385(02)02312–9.CrossRefGoogle Scholar
  33. Mole S, Waterman P G. 1987. A critical analysis of techniques for measuring tannins in ecological studies. Oecologia, 72 (1): 137–147, Scholar
  34. Monferrán M V, Sánchez Agudo J A, Pignata M L, Wunderlin D A. 2009. Copper–induced response of physiological parameters and antioxidant enzymes in the aquatic macrophyte Potamogeton pusillus. Environmental Pollution, 157 (8–9): 2 570–2 576, envpol.2009.02.034.CrossRefGoogle Scholar
  35. Ostrofsky M L, Zettler E R. 1986. Chemical defences in aquatic plants. Journal of Ecology, 74 (1): 279–287, Scholar
  36. Ozimek T, Kowalczewski A. 1984. Long–term changes of the submerged macrophytes in eutrophic lake Mikolajskie (North Poland). Aquatic Botany, 19 (1–2): 1–11,–3770(84)90002–0.CrossRefGoogle Scholar
  37. Pakdel F M, Sim L, Beardall J, Davis J. 2013. Allelopathic inhibition of microalgae by the freshwater stonewort, Chara australis, and a submerged angiosperm, Potamogeton crispus. Aquatic Botany, 110: 24–30, Scholar
  38. Phillips G, Willby N, Moss B. 2016. Submerged macrophyte decline in shallow lakes: what have we learnt in the last forty years? Aquatic Botany, 135: 37–45, https://doi. org/10.1016/j.aquabot.2016.04.004.CrossRefGoogle Scholar
  39. Qin B Q, Li W, Zhu G W, Zhang Y L, Wu T F, Gao G. 2015. Cyanobacterial bloom management through integrated monitoring and forecasting in large shallow eutrophic Lake Taihu (China). Journal of Hazardous Materials, 287: 356–363, 047.CrossRefGoogle Scholar
  40. Rout N P, Shaw B P. 2001. Salt tolerance in aquatic macrophytes: possible involvement of the antioxidative enzymes. Plant Science, 160 (3): 415–423, https://doi. org/10.1016/S0168–9452(00)00406–4.CrossRefGoogle Scholar
  41. Schindler D W, Curtis P J, Parker B R, Stainton M P. 1996. Consequences of climate warming and lake acidification for UV–B penetration in North American boreal lakes. Nature, 379 (6567): 705–708, Scholar
  42. Shao H B, Chu L Y, Shao M A, Jaleel C A, Mi H M. 2008. Higher plant antioxidants and redox signaling under environmental stresses. Comptes Rendus Biologies, 331 (6): 433–441, 011.CrossRefGoogle Scholar
  43. Smolders A J P, Vergeer L H T, Van Der Velde G, Roelofs J G M. 2000. Phenolic contents of submerged, emergent and floating leaves of aquatic and semi–aquatic macrophyte species: why do they differ? Oikos, 91 (2): 307–310,–0706.2000.910211.x.CrossRefGoogle Scholar
  44. Song J Q, Smart R, Wang H, Dambergs B, Sparrow A, Qian M C. 2015. Effect of grape bunch sunlight exposure and UV radiation on phenolics and volatile composition of Vitis vinifera L. cv. Pinot noir wine. Food Chemistry, 173: 424–431, Scholar
  45. Su H J, Wu Y, Xie P, Chen J F, Cao T, Xia W L. 2016. Effects of taxonomy, sediment, and water column on C:N:P stoichiometry of submerged macrophytes in Yangtze floodplain shallow lakes, China. Environmental Science and Pollution Research, 23 (22): 22 577–22 585,–016–7435–1.CrossRefGoogle Scholar
  46. Vergeer L H T, Van Der Velde G. 1997. Phenolic content of daylight–exposed and shaded floating leaves of water lilies (Nymphaeaceae) in relation to infection by fungi. Oecologia, 112 (4): 481–484, Scholar
  47. Watson S B, Miller C, Arhonditsis G, Boyer G L, Carmichael W, Charlton M N, Confesor R, Depew D C, Höök T O, Ludsin S A, Matisoff G, McElmurry S P, Murray M W, Richards R P, Rao Y R, Steffen M M, Wilhelm S W, 2016. The re–eutrophication of Lake Erie: harmful algal blooms and hypoxia. Harmful Algae, 56: 44–66, Scholar
  48. Wetzel R G. 2001. Structure and productivity of aquatic ecosystems. In: Wetzel R G ed. Limnology. 3 rd edn. Academic Press, San Diego, p.129–150.CrossRefGoogle Scholar
  49. Wium–Andersen S, Anthoni U, Christophersen C, Houen G. 1982. Allelopathic effects on phytoplankton by substances isolated from aquatic macrophytes (Charales). Oikos, 39 (2): 187–190, Scholar
  50. Yuan C B, Cao T, Zhou C Y, Ni L Y, Zhang X L. 2016. Contents of C, N and total phenols in leaves of aquatic macrophytes in lake Erhai, China. Acta Hydrobiologica Sinica, 40 (5): 1 025–1 032, (in Chinese with English abstract)Google Scholar
  51. Zhang M, Cao T, Ni L Y, Xie P, Li Z Q. 2010. Carbon, nitrogen and antioxidant enzyme responses of Potamogeton crispus to both low light and high nutrient stresses. Environmental and Experimental Botany, 68 (1): 44–50, Scholar
  52. Zhang M, Wang Z Q, Xu J, Liu Y Q, Ni L Y, Cao T, Xie P. 2011. Ammonium, microcystins, and hypoxia of blooms in eutrophic water cause oxidative stress and C–N imbalance in submersed and floating–leaved aquatic plants in Lake Taihu, China. Chemosphere, 82 (3): 329–339, Scholar
  53. Zhu G R, Yuan C B, Di G L, Zhang M, Ni L Y, Cao T, Fang R T, Wu G G. 2018. Morphological and biomechanical response to eutrophication and hydrodynamic stresses. Science of the Total Environment, 622–623: 421–435, Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Changbo Yuan
    • 1
    • 4
  • Tianshun Zhu
    • 3
    • 4
  • Te Cao
    • 1
    • 2
  • Yilong Xi
    • 2
  • Xiaolin Zhang
    • 1
    • 2
    Email author
  • Leyi Ni
    • 1
    • 2
  1. 1.Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  2. 2.Collaborative Innovation Center of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang City Belt, Anhui Province; College of Life SciencesAnhui Normal UniversityWuhuChina
  3. 3.College of Life SciencesZaozhuang UniversityZaozhuangChina
  4. 4.University of Chinese Academy of SciencesBeijingChina

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