Bioaccumulation and growth characteristics of Vallisneria natans (Lour.) Hara after chronic exposure to metal-contaminated sediments

  • Yu Qian
  • Changlei Cheng
  • Ken Drouillard
  • Qingzhi Zhu
  • Huan Feng
  • Shuzhuang He
  • Yuhong Fang
  • Shinan Qiao
  • Marek Kolenčíka
  • Xuexiu ChangEmail author
Research Article


Metal-contaminated sediments in lakes is a global concern that poses toxicological risk to aquatic organisms. This study performed bioassays using the submerged macrophyte, Vallisneria natans (Lour.) Hara, exposed to contaminated sediments collected from five locations in Dianchi Lake, Yunnan, China. Among the sediments collected, Igeo showed enrichment of As and Cd in Dianchi Lake sediments. In spite of enriched toxic metals at some locations, laboratory bioassays found no significant difference in leaf biomass or leaf photosynthesis rate between the sites. Root biomass and root activity showed significant differences between locations and were negatively correlated with the concentration of As, Cd, Hg, and Pb in sediment but not related to Cr. The above correlations were strongest for Hg and As, respectively. Accumulation of Cd and Pb to leaves of bioassay plants was observed, but this was not evident for As and Cr. Overall, the results indicate that V. natans can be used as a bioassay organism and measures of root toxicity are sensitive to metal concentrations present in Dianchi Lake sediments. Furthermore, the study species holds promise for use as a biomonitor of Cd and Pb sediment metal content.


Metals Sediment Vallisneria natans (Lour.) Hara Chronic exposure Toxicity Risk assessment 



We wish to thank Professor Nanlan Peng for metal analysis.

Funding information

This work was supported in part by the Joint Grant of Yunnan Provincial Science and Technology Department – Yunnan University Major Project (2018FY001-007), the National Natural Science Foundation of China for Young Scientist (Grant No. 3170040), and the Provincial Natural Science Foundation of Yunnan for Young Scientist (Grant No. 2017FD066) and Yunnan Science and Technology Major Project (2018BC002).


  1. Al ME, Kaiser K, Williams JR, Dellapenna TM, Louchouarn P, Santschi PH (2018) Centennial record of anthropogenic impacts in Galveston Bay: evidence from trace metals (Hg, Pb, Ni, Zn) and lignin oxidation products. Environ Pollut 237:887–899CrossRefGoogle Scholar
  2. Ali B, Vajpayee P, Tripathi RD, Rai UN, Kumar A, Singh N, Behl HM, Singh SP (2000) Mercury bioaccumulation induces oxidative stress and toxicity to submerged Macrophyte Potamogeton crispus L. Bull Environ Contam Toxicol 65:573–582Google Scholar
  3. Alloway BJ (2013) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. SpringerGoogle Scholar
  4. Andresen E, Mattusch J, Wellenreuther G, Thomas G, Arroyo Abad U, Kupper H (2013a) Different strategies of cadmium detoxification in the submerged macrophyte Ceratophyllum demersum L. Metallomics 5:1377–1386CrossRefGoogle Scholar
  5. Andresen E, Opitz J, Thomas G, Stark HJ, Dienemann H, Jenemann K, Dickinson BC, Kupper H (2013b) Effects of Cd & Ni toxicity to Ceratophyllum demersum under environmentally relevant conditions in soft & hard water including a German lake. Aquat Toxicol 142-143:387–402CrossRefGoogle Scholar
  6. Andresen E, Kappel S, Stark HJ, Riegger U, Borovec J, Mattusch J, Heinz A, Schmelzer CE, Matouskova S, Dickinson B, Kupper H (2016) Cadmium toxicity investigated at the physiological and biophysical levels under environmentally relevant conditions using the aquatic model plant Ceratophyllum demersum. New Phytol 210:1244–1258CrossRefGoogle Scholar
  7. Arts GH, Belgers JD, Hoekzema CH, Thissen JT (2008) Sensitivity of submersed freshwater macrophytes and endpoints in laboratory toxicity tests. Environ Pollut 153:199–206CrossRefGoogle Scholar
  8. ATSDR Agency for Toxic Substance and Disease Registry (2017) Substance priority list. Access 18 March 2019
  9. Bakhat HF, Zia Z, Fahad S, Abbas S, Hammad HM, Shahzad AN, Abbas F, Alharby H, Shahid M (2017) Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ Sci Pollut Res Int 24:9142–9158CrossRefGoogle Scholar
  10. Chen J, Hu X, Cao T, Zhang X, Xi Y, Wen X, Su H, de Silva W, Zhu T, Ni L, Xie P (2017) Root-foraging behavior ensures the integrated growth of Vallisneria natans in heterogeneous sediments. Environ Sci Pollut Res 24:8108–8119CrossRefGoogle Scholar
  11. Cheng C (2017) The distribution of heavy metals in Dianchi Lake and ecological risk assessment. Yunnan University, KunmingGoogle Scholar
  12. Cheng H, Li M, Zhao C, Yang K, Li K, Peng M, Yang Z, Liu F, Liu Y, Bai R, Cui Y, Huang Z, Li L, Liao Q, Luo J, Jia S, Pang X, Yang J, Yin G (2015) Concentrations of toxic metals and ecological risk assessment for sediments of major freshwater lakes in China. J Geochem Explor 157:15–26CrossRefGoogle Scholar
  13. CNSMC China National Standardization Management Committee, GAQSIQ General Administration of Quality Supervision, Inspection and Quarantine (2007) The specification for marine monitoring - part 6: organism analysis (GB17378.6–2007), ChinaGoogle Scholar
  14. Concas S, Ardau C, Bonito MD, Lattanzi P, Vacca A (2015) Field sampling of soil pore water to evaluate the mobile fraction of trace elements in the Iglesiente area (SW Sardinia, Italy). J Geochem Explor 158:82–94CrossRefGoogle Scholar
  15. Coquery M, Welbourn P (1994) Mercury uptake from contaminated water and sediment by the rooted and submerged aquatic macrophyte Eriocaulon septangulare. Arch Environ Contam Toxicol 26:335–341CrossRefGoogle Scholar
  16. Eckley CS, Luxton TP, Goetz J, Mckernan J (2017) Water-level fluctuations influence sediment porewater chemistry and methylmercury production in a flood-control reservoir. Environ Pollut 222:32–41CrossRefGoogle Scholar
  17. EPD EPD (2012) Soil-determination of total phosphorus by alkali fusion-Mo-Sb anti spectrophotometric method (HJ632-2011), China, 1–8 ppGoogle Scholar
  18. EPD EPD (2014) Soil quality - determination of total nitrogen - modified Kjeldahl method (HJ717–2014), ChinaGoogle Scholar
  19. Ghrefat HA, Aburukah Y, Rosen MA (2011) Application of geoaccumulation index and enrichment factor for assessing metal contamination in the sediments of Kafrain Dam, Jordan. Environ Monit Assess 178:95–109CrossRefGoogle Scholar
  20. Giddings JM, Arts G, Hommen U (2013) The relative sensitivity of macrophyte and algal species to herbicides and fungicides: an analysis using species sensitivity distributions. Integr Environ Assess Manag 9:308–318CrossRefGoogle Scholar
  21. Gu J, Xu Z, Jin H, Ning X, He H, Yu J, Jeppesen E, Li K (2016) Response of Vallisneria natans to increasing nitrogen loading depends on sediment nutrient characteristics. Water 8:563CrossRefGoogle Scholar
  22. Guilizzoni P (1991) The role of heavy metals and toxic materials in the physiological ecology of submersed. Aquat Bot 41:87–109CrossRefGoogle Scholar
  23. Gupta M, Chandra P (1994) Lead accumulation and toxicity in Vallisneria spiralis (L.) and Hvdrilla vertieillata (lf) Royle. J Environ Sci Health A 29:503–516Google Scholar
  24. Gupta M, Chandra P (1998) Bioaccumulation and toxicity of mercury in rooted-submerged macrophyte Vallisneria spiralis. Environ Pollut 103:327–333CrossRefGoogle Scholar
  25. Gupta M, Tripathi BD, Rai PK, Chandra P (1998) Role of glutathione and phytochelatin in Hydrilla verticillata (I.f.) Royle and Vallisneria spiralis L. under mercury stress. Chemosphere 37:785–800CrossRefGoogle Scholar
  26. Hakanson L (1980) An ecological risk index for aquatic pollution control.a sedimentological approach. Water Res 14:975–1001CrossRefGoogle Scholar
  27. Jiang HS, Zhang Y, Yin L, Li W, Jin Q, Fu W, Zhang T, Huang W (2018) Diurnal changes in photosynthesis by six submerged macrophytes measured using fluorescence. Aquat Bot 149:33–39CrossRefGoogle Scholar
  28. Juncos R, Campbell L, Arcagni M, Daga R, Rizzo A, Arribere M, Ribeiro Guevara S (2017) Variations in anthropogenic silver in a large Patagonian lake correlate with global shifts in photographic processing technology. Environ Pollut 223:685–694CrossRefGoogle Scholar
  29. Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defence system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634CrossRefGoogle Scholar
  30. Kroflic A, Germ M, Golob A, Stibilj V (2018) Does extensive agriculture influence the concentration of trace elements in the aquatic plant Veronica anagallis aquatica? Ecotoxicol Environ Saf 150:123–128CrossRefGoogle Scholar
  31. Lai WL, Zhang Y, Chen ZH (2012) Radial oxygen loss, photosynthesis, and nutrient removal of 35 wetland plants. Ecol Eng 39:24–30CrossRefGoogle Scholar
  32. Lewis MA (1995) Use of freshwater plants for phytotoxicity testing: a review. Environ Pollut 87:19–336CrossRefGoogle Scholar
  33. Lewis M, Thursby G (2018) Aquatic plants: test species sensitivity and minimum data requirement evaluations for chemical risk assessments and aquatic life criteria development for the USA. Environ Pollut 238:270–280CrossRefGoogle Scholar
  34. Li HB, Yu S, Li GL, Deng H, Xu B, Ding J, Gao JB, Hong YW, Wong MH (2013) Spatial distribution and historical records of mercury sedimentation in urban lakes under urbanization impacts. Sci Total Environ 445-446:117–125CrossRefGoogle Scholar
  35. Li B, Gu B, Yang Z, Zhang T (2018a) The role of submerged macrophytes in phytoremediation of arsenic from contaminated water: a case study on Vallisneria natans (Lour.) Hara. Ecotoxicol Environ Saf 165:224–231CrossRefGoogle Scholar
  36. Li Y, Zhou S, Zhu Q, Li B, Wang J, Wang C, Chen L, Wu S (2018b) One-century sedimentary record of heavy metal pollution in western Taihu Lake, China. Environ Pollut 240:709–716CrossRefGoogle Scholar
  37. Liu H, Cao Y, Li W, Zhang Z, Jeppesen E, Wang W (2017) The effects of cadmium pulse dosing on physiological traits and growth of the submerged macrophyte Vallisneria spinulosa and phytoplankton biomass: a mesocosm study. Environ Sci Pollut Res Int 24:15308–15314CrossRefGoogle Scholar
  38. Lv S, Yang B, Kou Y, Zeng J, Wang R, Xiao Y, Li F, Lu Y, Mu Y, Zhao C (2018) Assessing the difference of tolerance and phytoremediation potential in mercury contaminated soil of a non-food energy crop, Helianthus tuberosus L. (Jerusalem artichoke). Peer J 6:1–18Google Scholar
  39. Macdonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39:20–31CrossRefGoogle Scholar
  40. Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55:64–69CrossRefGoogle Scholar
  41. Manahan SE, Manahan SE (2001) Fundamentals of environmental chemistry. Lewis Publishers 163-163 ppGoogle Scholar
  42. NFB NFB (1999) Determination of organic matter in forest soil and calculatin carbon-nitrogen ratio, pp 1–4Google Scholar
  43. Peng K, Luo C, Lou L, Li X, Shen Z (2008) Bioaccumulation of heavy metals by the aquatic plants Potamogeton pectinatus L. and Potamogeton malaianus Miq. and their potential use for contamination indicators and in wastewater treatment. Sci Total Environ 392:22–29CrossRefGoogle Scholar
  44. Qian Y, Gallagher FJ, Feng H, Wu M (2012) A geochemical study of toxic metal translocation in an urban brownfield wetland. Environ Pollut 166:23–30CrossRefGoogle Scholar
  45. Qian Y, Gallagher FJ, Feng H, Wu M, Zhu Q (2014) Vanadium uptake and translocation in dominant plant species on an urban coastal brownfield site. Sci Total Environ 476-477:696–704CrossRefGoogle Scholar
  46. Qian Y, Gallagher F, Deng Y, Wu M, Feng H (2017) Risk assessment and interpretation of heavy metal contaminated soils on an urban brownfield site in New York metropolitan area. Environ Sci Pollut Res Int 24:23549–23558CrossRefGoogle Scholar
  47. Richter AK, Frossard E, Brunner I (2007) Polyphenols in the woody roots of Norway spruce and European beech reduce TTC. Tree Physiol 27:155–160CrossRefGoogle Scholar
  48. Saygideger S, Dogan M (2004) Lead and cadmium accumulation and toxicity in the presence of EDTA in Lemna minor L. and Ceratophyllum demersum L. Bull Environ Contam Toxicol 73:182–189CrossRefGoogle Scholar
  49. Shao X (2003) Study of spatial distribution of heavy metal element in the sediment of Dianchi Lake, Yunnan, Nanjing Normal UniversityGoogle Scholar
  50. Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110CrossRefGoogle Scholar
  51. Singh KP, Mohan D, Sinha S, Dalwani R (2004) Impact assessment of treated/untreated wastewater toxicants discharged by sewage treatment plants on health, agricultural, and environmental quality in the wastewater disposal area. Chemosphere 55:227–255CrossRefGoogle Scholar
  52. Sivaci A, Sivaci ER, Sokmen M (2007) Changes in antioxidant activity, total phenolic and abscisic acid constituents in the aquatic plants Myriophyllum spicatum L. and Myriophyllum triphyllum Orchard exposed to cadmium. Ecotoxicology 16:423–428CrossRefGoogle Scholar
  53. Soana E, Naldi M, Bartoli M (2012) Effects of increasing organic matter loads on pore water features of vegetated ( Vallisneria spiralis L.) and plant-free sediments. Ecol Eng 47:141–145CrossRefGoogle Scholar
  54. Tamas L, Zelinova V (2017) Mitochondrial complex II-derived superoxide is the primary source of mercury toxicity in barley root tip. J Plant Physiol 209:68–75CrossRefGoogle Scholar
  55. Tripathi RD, Singh R, Tripathi P, Dwivedi S, Chauhan R, Adhikari B, Trivedi PK (2014) Arsenic accumulation and tolerance in rootless macrophyte Najas indica are mediated through antioxidants, amino acids and phytochelatins. Aquat Toxicol 157:70–80CrossRefGoogle Scholar
  56. Wang J, Yu D (2007) Influence of sediment fertility on morphological variability of Vallisneria spiralis L. Aquat Bot 87:127–133CrossRefGoogle Scholar
  57. Wang C, Sun Q, Wang L (2009) Cadmium toxicity and phytochelatin production in a rooted-submerged macrophyte Vallisneria spiralis exposed to low concentrations of cadmium. Environ Toxicol 24:271–278CrossRefGoogle Scholar
  58. Wang Z, Yao L, Liu G, Liu W (2014) Heavy metals in water, sediments and submerged macrophytes in ponds around the Dianchi Lake, China. Ecotoxicol Environ Saf 107:200–206CrossRefGoogle Scholar
  59. Xing W, Wu H, Hao B, Liu G (2013) Metal accumulation by submerged macrophytes in eutrophic lakes at the watershed scale. Environ Sci Pollut Res Int 20:6999–7008CrossRefGoogle Scholar
  60. Xing W, Bai G, Wu H, Liu H, Liu G (2017) Effect of submerged macrophytes on metal and metalloid concentrations in sediments and water of the Yunnan Plateau lakes in China. J Soils Sediments 17:2566–2575CrossRefGoogle Scholar
  61. Yang J, Chen L, Steele JC, Chen RS, Meng XZ (2016) An extended study on historical mercury accumulation in lake sediment of Shanghai: the contribution of socioeconomic driver. Environ Pollut 219:612–619CrossRefGoogle Scholar
  62. Yi Y, Yang Z, Zhang S (2011) Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ Pollut 159:2575–2585CrossRefGoogle Scholar
  63. Zhang X, Huang G, Bian X, Zhao Q (2013) Effects of root interaction and nitrogen fertilization on the chlorophyll content, root activity, photosynthetic characteristics of intercropped soybean and microbial quantity in the rhizosphere. Plant Soil Environ 59:80–88Google Scholar
  64. Zhao P, Zhu Y, Wang W (2010) Evaluation and improvement of spectrophotometric assays of TTC reduction: maize (Zea mays) embryo as an example. Acta Physiol Plant 32:815–819CrossRefGoogle Scholar
  65. Zheng N, Wang Q, Liang Z, Zheng D (2008) Characterization of heavy metal concentrations in the sediments of three freshwater rivers in Huludao City, Northeast China. Environ Pollut 154:135–142CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yu Qian
    • 1
  • Changlei Cheng
    • 2
  • Ken Drouillard
    • 3
  • Qingzhi Zhu
    • 4
  • Huan Feng
    • 5
  • Shuzhuang He
    • 1
  • Yuhong Fang
    • 1
  • Shinan Qiao
    • 1
  • Marek Kolenčíka
    • 6
  • Xuexiu Chang
    • 1
    Email author
  1. 1.School of Ecology and Environmental SciencesYunnan UniversityKunmingChina
  2. 2.Analysis and Measurements Center of Yunnan Provincial Non-ferrous Geology BureauKunmingChina
  3. 3.Great Lakes Institute for Environmental ResearchUniversity of WindsorWindsorCanada
  4. 4.School of Marine and Atmospheric ScienceState University of New YorkStony BrookUSA
  5. 5.Department of Earth and Environmental StudiesMontclair State UniversityMontclairUSA
  6. 6.Department of Soil Science and Geology, Faculty of Agrobiology and Food ResourcesSlovak University of Agriculture in NitraNitraSlovak Republic

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