Environmental Science and Pollution Research

, Volume 24, Issue 18, pp 15308–15314 | Cite as

The effects of cadmium pulse dosing on physiological traits and growth of the submerged macrophyte Vallisneria spinulosa and phytoplankton biomass: a mesocosm study

  • Hui Liu
  • Yu Cao
  • Wei Li
  • Zhao Zhang
  • Erik Jeppesen
  • Wei Wang
Research Article


Pulse inputs of heavy metals are expected to increase with a higher frequency of extreme climate events (heavy rain), leading to stronger erosion of contaminated and fertilized farmland soils to freshwaters, with potentially adverse effects on lake ecosystems. We conducted a 5-month mesocosm study to elucidate the responses of the submerged macrophyte Vallisneria spinulosa and phytoplankton to four different doses of cadmium (Cd): 0 (control), 0.05, 0.5, and 5 g m−2 (CK, I, II, and III, respectively) under mesotrophic conditions. We found that total phosphorus concentrations were larger in the three Cd pulse treatments, whereas total nitrogen concentrations did not differ among the four treatments. The contents of chlorophyll a and soluble sugar in macrophyte leaves decreased in III, and total biomass, ramet number, plant height, and total stolon length of macrophytes were lower in both II and III. In contrast, abundances of the three main phytoplankton taxa—Cyanophyta, Chlorophyta, and Bacillariophyta—did not differ among treatments. Total phytoplankton biomass was, however, marginally lower in CK than in the Cd treatments. We conclude that exposure to strong Cd pulses led to significantly reduced growth of macrophytes, while no obvious effect appeared for phytoplankton.


Extreme events Cd Submerged macrophyte Phytoplankton Pulse loading Heavy metal 



This study was supported by the National Natural Science Foundation of China (31601824, 51379133), CRES (Danish Strategic Research Council), CLEAR (a Villum Kann Rasmussen Centre of Excellence project), and the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No.: 603378 ( We thank Anne Mette Poulsen for valuable editorial comments.


  1. Andresen E, Mattusch J, Wellenreuther G, Thomas G, Arroyo Abad U, Kupper H (2013) Different strategies of cadmium detoxification in the submerged macrophyte Ceratophyllum demersum L. Metallomics 5:1377–1386. doi: 10.1039/C3MT00088E CrossRefGoogle Scholar
  2. Andresen E et al (2016) Cadmium toxicity investigated at the physiological and biophysical levels under environmentally relevant conditions using the aquatic model plant Ceratophyllum demersum. New Phytol 210:1244–1258. doi: 10.1111/nph.13840 CrossRefGoogle Scholar
  3. Brand LE, Sunda WG, Guillard RRL (1986) Reduction of marine phytoplankton reproduction rates by copper and cadmium. J Exp Mar Bio Ecol 96:225–250. doi: 10.1016/0022-0981(86)90205-4 CrossRefGoogle Scholar
  4. Cao T, Xie P, Li ZQ, Ni LY, Zhang M, Xu J (2009) Physiological stress of high NH4 + concentration in water column on the submersed macrophyte Vallisneria natans L. Bull Environ Contam Toxicol 82:296–299. doi: 10.1007/s00128-008-9531-5 CrossRefGoogle Scholar
  5. Communique of the National Soil Pollution Survey (2014) URL:
  6. Cullen JT, Maldonado MT (2013) Biogeochemistry of cadmium and its release to the environment. In: Sigel A, Sigel H, Sigel RKO (eds) Cadmium: from toxicity to essentiality. Springer Netherlands, Dordrecht, pp 31–62. doi: 10.1007/978-94-007-5179-8_2 CrossRefGoogle Scholar
  7. Dalla Vecchia F, Rocca NL, Moro I, De Faveri S, Andreoli C, Rascio N (2005) Morphogenetic, ultrastructural and physiological damages suffered by submerged leaves of Elodea canadensis exposed to cadmium. Plant Sci 168:329–338. doi: 10.1016/j.plantsci.2004.07.025 CrossRefGoogle Scholar
  8. Deng G, Li M, Li H, Yin LY, Li W (2014) Exposure to cadmium causes declines in growth and photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides). Aquat Bot 112:23–32. doi: 10.1016/j.aquabot.2013.07.003 CrossRefGoogle Scholar
  9. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. doi: 10.1021/ac60111a017
  10. Duc Phuc H et al (2016) A 28-year observational study of urinary cadmium and β2-microglobulin concentrations in inhabitants in cadmium-polluted areas in Japan. J Appl Toxicol 36:1622–1628. doi: 10.1002/jat.3327 CrossRefGoogle Scholar
  11. Echeveste P, Agustí S, Tovar-Sánchez A (2012) Toxic thresholds of cadmium and lead to oceanic phytoplankton: cell size and ocean basin–dependent effects. Environ Toxicol Chem 31:1887–1894. doi: 10.1002/etc.1893 CrossRefGoogle Scholar
  12. Fathi AA, El-Shahed AM, Shoulkamy MA, Ibraheim HA, Abdel Rahman OM (2008) Response of Nile water phytoplankton to the toxicity of cobalt, copper and zinc. Research Journal of Environmental Toxicology 2:67–76CrossRefGoogle Scholar
  13. Field CB, Barros VR, Mach K, Mastrandrea M (2014) Climate change 2014: impacts, adaptation, and vulnerability. Contribution of working group II to the 5th assessment report of the intergovernmental panel on climate change. Cambridge University Press, New YorkGoogle Scholar
  14. Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Med Toxicol (London, England) 1:22. doi: 10.1186/1745-6673-1-22 CrossRefGoogle Scholar
  15. Huang XF, Chen WM, Cai QM (1999) Survey, observation and analysis of lake ecology. Standards Press of China, Beijing (in Chinese) Google Scholar
  16. Jain CK, Sharma MK (2002) Adsorption of cadmium on bed sediments of river Hindon: adsorption models and kinetics. Water Air Soil Pollut 137:1–19. doi: 10.1023/a:1015530702297 CrossRefGoogle Scholar
  17. Jensen A, Bro-Rasmussen F (1992) Environmental cadmium in Europe. In: Ware GW (ed) Reviews of environmental contamination and toxicology: continuation of residue reviews. Springer New York, New York, pp 101–181. doi: 10.1007/978-1-4612-2890-5_3 CrossRefGoogle Scholar
  18. Jeppesen E, Sondergaard M, Sondergaard M, Christofferson K (1998) The structuring role of submerged macrophytes in lakes. Ecological studies. Springer New York, New YorkCrossRefGoogle Scholar
  19. John R, Ahmad P, Gadgil K, Sharma S (2008) Effect of cadmium and lead on growth, biochemical parameters and uptake in Lemna polyrrhiza L. Plant Soil Environ 54:262–270Google Scholar
  20. Kabata-Pendias A (2010) Trace elements in soils and plants, 4th edn. Taylor & Francis, Boca RatonCrossRefGoogle Scholar
  21. Kirkham MB (2006) Cadmium in plants on polluted soils: effects of soil factors, hyperaccumulation, and amendments. Geoderma 137:19–32. doi: 10.1016/j.geoderma.2006.08.024 CrossRefGoogle Scholar
  22. Küpper H, Kochian LV (2010) Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population). New Phytol 185:114–129. doi: 10.1111/j.1469-8137.2009.03051.x CrossRefGoogle Scholar
  23. Leung HM et al (2016) Monitoring and assessment of heavy metal contamination in a constructed wetland in Shaoguan (Guangdong Province, China): bioaccumulation of Pb, Zn, Cu and Cd in aquatic and terrestrial components. Environ Sci Pollut Res 24(10):9079–9088. doi: 10.1007/s11356-016-6756-4 CrossRefGoogle Scholar
  24. Li W, Zhang Z, Jeppesen E (2008) The response of Vallisneria spinulosa (Hydrocharitaceae) to different loadings of ammonia and nitrate at moderate phosphorus concentration: a mesocosm approach. Freshwat Biol 53:2321–2330. doi: 10.1111/j.1365-2427.2008.02053.x CrossRefGoogle Scholar
  25. Miao AJ, Wang WX (2006) Cadmium toxicity to two marine phytoplankton under different nutrient conditions. Aquat Toxicol 78:114–126. doi: 10.1016/j.aquatox.2006.02.008 CrossRefGoogle Scholar
  26. Mishra S, Tripathi RD, Srivastava S, Dwivedi S, Trivedi PK, Dhankher OP, Khare A (2009) Thiol metabolism play significant role during cadmium detoxification by Ceratophyllum demersum L. Bioresour Technol 100:2155–2161. doi: 10.1016/j.biortech.2008.10.041 CrossRefGoogle Scholar
  27. Mishra S, Wellenreuther G, Mattusch J, Stärk H-J, Küpper H (2013) Speciation and distribution of arsenic in the nonhyperaccumulator macrophyte Ceratophyllum demersum. Plant Physiol 163:1396–1408. doi: 10.1104/pp.113.224303 CrossRefGoogle Scholar
  28. Nawrot T et al (2006) Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncol 7:119–126. doi: 10.1016/S1470-2045(06)70545-9 CrossRefGoogle Scholar
  29. Payne CD, Price NM (1999) Effects of cadmium toxicity on growth and elemental compostion of marine phytoplankton. J Phycol 35:293–302. doi: 10.1046/j.1529-8817.1999.3520293.x CrossRefGoogle Scholar
  30. Prozialeck WC, Edwards JR (2012) Mechanisms of cadmium-induced proximal tubule injury: new insights with implications for biomonitoring and therapeutic interventions. J Pharmacol Exp Ther 343:2–12. doi: 10.1124/jpet.110.166769 CrossRefGoogle Scholar
  31. Ruangsomboon S, Wongrat L (2006) Bioaccumulation of cadmium in an experimental aquatic food chain involving phytoplankton (Chlorella vulgaris), zooplankton (Moina macrocopa), and the predatory catfish Clarias macrocephalus × C. gariepinus. Aquat Toxicol 78:15–20. doi: 10.1016/j.aquatox.2006.01.015 CrossRefGoogle Scholar
  32. Søndergaard M, Johansson LS, Lauridsen TL, Jørgensen TB, Liboriussen L, Jeppesen E (2010) Submerged macrophytes as indicators of the ecological quality of lakes. Freshwat Biol 55:893–908. doi: 10.1111/j.1365-2427.2009.02331.x CrossRefGoogle Scholar
  33. Wagner GJ (1993) Accumulation of cadmium in crop plants and its consequences to human health. In: Donald LS (ed) Advances in agronomy. Academic, Cambridge, pp 173–212. doi: 10.1016/S0065-2113(08)60593-3 Google Scholar
  34. Wang HJ, Wang HZ, Liang XM, Wu SK (2014) Total phosphorus thresholds for regime shifts are nearly equal in subtropical and temperate shallow lakes with moderate depths and areas. Freshwat Biol 59:1659–1671. doi: 10.1111/fwb.12372 CrossRefGoogle Scholar
  35. Xie LQ, Xie P, Li SX, Tang HJ, Liu H (2003) The low TN:TP ratio, a cause or a result of Microcystis blooms? Water Res 37:2073–2080. doi: 10.1016/S0043-1354(02)00532-8 CrossRefGoogle Scholar
  36. Xing W, Wu HP, Hao BB, Huang WM, Liu GH (2013) Bioaccumulation of heavy metals by submerged macrophytes: looking for hyperaccumulators in eutrophic lakes. Environ Sci Technol 47:4695–4703. doi: 10.1021/es303923w CrossRefGoogle Scholar
  37. Yabanli M, Yozukmaz A, Sel F (2014) Heavy metal accumulation in the leaves, stem and root of the invasive submerged macrophyte Myriophyllum spicatum L. (Haloragaceae): an example of Kadin Creek (Mugla, Turkey). Braz Arch Biol Technol 57:434–440CrossRefGoogle Scholar
  38. Yang ZF, Wang Y, Shen ZY et al (2009) Distribution and speciation of heavy metals in sediments from the mainstream, tributaries, and lakes of the Yangtze River catchment of Wuhan, China. J Hazard Mater 166:1186–1194CrossRefGoogle Scholar
  39. Zhang Z, Cao Y, Jeppesen E, Li W (2016) The response of Vallisneria spinulosa (Hydrocharitaceae) and plankton to pulse addition of inorganic nitrogen with different loading patterns. Hydrobiologia 767:175–184. doi: 10.1007/s10750-015-2494-8 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Key Laboratory of Ecological Impacts of Hydraulic-Projects and Restoration of Aquatic Ecosystem of Ministry of Water Resources, Institute of Hydroecology, Ministry of Water ResourcesChinese Academy of SciencesWuhanChina
  2. 2.Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  3. 3.Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  4. 4.Sino-Danish Centre for Education and Research (SDC)BeijingChina
  5. 5.Xi’an Botanical Garden of Shaanxi ProvinceInstitute of Botany of Shaanxi ProvinceXi’anChina
  6. 6.Lake Ecology Section, Department of BioscienceAarhus UniversitySilkeborgDenmark

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