, Volume 23, Issue 3, pp 385–395 | Cite as

Impacts of major cations (K+, Na+, Ca2+, Mg2+) and protons on toxicity predictions of nickel and cadmium to lettuce (Lactuca sativa L.) using exposure models

  • Yang Liu
  • Martina G. Vijver
  • Willie J. G. M. Peijnenburg


Biotic ligand models (BLM) explicitly accounting for hypothetical interactions with biotic ligands and bioavailability as dictated by water chemistry have been developed for various metals and different organisms. It is only recently that BLMs for plants have received increasing attention. Lettuce is one of the most important vegetable crops in the world. This study investigated the impacts of Ca2+, Mg2+, K+, Na+ and pH, on acute toxicity of Ni and Cd to butter-head lettuce seedlings (Lactuca sativa L.). 4-day assays with the root elongation inhibition (REI) as the endpoint were performed in hydroponic solutions. Magnesium was found to be the sole cation significantly enhancing the median inhibition concentration (IC50) of Ni2+ with increasing concentration. By incorporating the competitive effects of Mg2+, the Ni-toxicity prediction was improved significantly as compared to the total metal model (TMM) and the free ion activity model (FIAM). The conditional stability constants derived from the Ni-BLM were log KMgBL = 2.86, log KNiBL = 5.1, and fNiBL50% = 0.57. A slight downtrend was observed in the 4-d IC50 of Cd2+ at increasing H+ concentrations, but this tendency was not consistent and statistically significant (p = 0.07) over the whole range. The overall variations of Cd-toxicity within the tested Na+, K+, Ca2+ and Mg2+ concentration ranges were relatively small and not statistically significant. 80 % of lettuce REI by Cd could be explained using both TMM and FIAM instead of BLM in the present study. Thus, the mechanistically underpinned models for soil quality guidelines should be developed on a metal-specific basis across different exposure conditions.


Root elongation Nickel Cadmium Biotic ligand model Toxicity 

Supplementary material

10646_2014_1202_MOESM1_ESM.docx (818 kb)
Supplementary material 1 (DOCX 819 kb)


  1. Andriolo JL, Luz GL, Witter MH, Godoi RDS, Barros GT, Bortolotto OC (2005) Growth and yield of lettuce plants under salinity. Hortic Bras 23:931–934CrossRefGoogle Scholar
  2. Antunes PMC, Kreager NJ (2009) Development of the terrestrial biotic ligand model for predicting nickel toxicity to barley (Hordeum Vulgare): ion effects at low pH. Environ Toxicol Chem 28:1704–1710CrossRefGoogle Scholar
  3. Antunes PMC, Hale BA, Ryan AC (2007) Toxicity versus accumulation for barley plants exposed to copper in the presence of metal buffers: progress towards development of a terrestrial biotic ligand model. Environ Toxicol Chem 26:2282–2289CrossRefGoogle Scholar
  4. Cabrera D, Young SD, Rowell DL (1988) The toxicity of cadmium to barley plants as affected by complex formation with humic acid. Plant Soil 105:195–204CrossRefGoogle Scholar
  5. Charles J, Sancey B, Morin-Crini N, Badot PM, Degiorgi F, Trunfio G, Crini G (2011) Evaluation of the phytotoxicity of polycontaminated industrial effluents using the lettuce plant (Lactuca sativa) as a bioindicator. Ecotoxicol Environ Saf 74:2057–2064CrossRefGoogle Scholar
  6. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719CrossRefGoogle Scholar
  7. Clifford M, McGeer JC (2010) Development of a biotic ligand model to predict the acute toxicity of cadmium to Daphnia pulex. Aquat Toxicol 98:1–7CrossRefGoogle Scholar
  8. Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36CrossRefGoogle Scholar
  9. De Schamphelaere KAC, Janssen CR (2002) A biotic ligand model predicting acute copper toxicity for Daphnia magna: the effects of calcium, magnesium, sodium, potassium, and pH. Environ Sci Technol 36:48–54CrossRefGoogle Scholar
  10. Deleebeeck NME, De Schamphelaere KAC, Janssen CR (2009) Effects of Mg2+ and H+ on the toxicity of Ni2+ to the unicellular green alga Pseudokirchneriella subcapitata: model development and validation with surface waters. Sci Total Environ 407:1901–1914CrossRefGoogle Scholar
  11. Di Toro DM, Allen HE, Bergman HL, Meyer JS, Paquin PR, Santore RC (2001) Biotic ligand model of the acute toxicity of metals. 1 Technical basis. Environ Toxicol Chem 20:2383–2396CrossRefGoogle Scholar
  12. Dixon RK (1988) Response of ectomycorrhizal Quercus rubra to soil cadmium, nickel and lead. Soil Biol Biochem 20:555–559CrossRefGoogle Scholar
  13. Dong J, Mao WH, Zhang GP, Wu FB, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity—a review. Plant Soil Environ 53:193–200Google Scholar
  14. Fodor F (2002) Physiological responses of vascular plants to heavy metals. In: Prasad MNV, Strzalka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer Academic Publishers, Dordrecht, pp 149–177CrossRefGoogle Scholar
  15. François L, Fortin C, Campbell PGC (2007) PH modulates transport rates of manganese and cadmium in the green alga Chlamydomonas reinhardtii through non-competitive interactions: implications for an algal BLM. Aquat Toxicol 84:123–132CrossRefGoogle Scholar
  16. Garate A, Ramos I, Manzanares M, Lucena JJ (1993) Cadmium uptake and distribution in three cultivars of Lactuca sp. Bull Environ Contam Toxicol 50:709–716Google Scholar
  17. Gopalapillai Y, Hale B, Vigneault B (2013) Effect of major cations (Ca2+, Mg2+, Na+, K+) and anions (SO4 2−, Cl, NO3 ) on Ni accumulation and toxicity in aquatic plant (Lemna minor L.): implications for Ni risk assessment. Environ Toxicol Chem 32:810–821CrossRefGoogle Scholar
  18. Gupta DK, Huang HG, Nicoloso FT, Schetinger MR, Farias JG, Li TQ, Razafindrabe BHN, Aryal N, Inouhe M (2013) Effect of Hg, As and Pb on biomass production, photosynthetic rate, nutrients uptake and phytochelatin induction in Pfaffia glomerata. Ecotoxicology 22:1403–1412CrossRefGoogle Scholar
  19. Hagemeyer J (2004) Ecophysiology of plant growth under heavy metal stress. In: Prasad MNV (ed) Heavy metal stress in plants, 2nd edn. Springer, Berlin, pp 201–222CrossRefGoogle Scholar
  20. Haghiri F (1974) Plant uptake of cadmium as influenced by cation exchange capacity, organic matter, zinc and soil temperature. J Environ Qual 3:180–183CrossRefGoogle Scholar
  21. Hatano A, Shoji R (2010) A new model for predicting time course toxicity of heavy metals based on Biotic Ligand Model (BLM). Comp Biochem Physiol C 151:25–32Google Scholar
  22. Heijerick DG, De Schamphelaere KAC, Janssen CR (2002) Predicting acute zinc toxicity for Daphnia magna as a function of key water chemistry characteristics: development and validation of a biotic ligand model. Environ Toxicol Chem 21:1309–1315CrossRefGoogle Scholar
  23. Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37Google Scholar
  24. Läuchi A, Epstein E (1984) Mechanisms of salt tolerance in plants. Calif Agric 38:18–20Google Scholar
  25. Le TT (2012) Modeling bioaccumulation and toxicity of metal mixtures. Dissertation, Radboud University NijmegenGoogle Scholar
  26. Le TT, Peijnenburg WJGM, Hendriks AJ, Vijver MG (2012) Predicting effects of cations on copper toxicity to lettuce (Lactuca sativa) by the biotic ligand model. Environ Toxicol Chem 31:355–359CrossRefGoogle Scholar
  27. Lei LP, Chen SB, Sun C, Xu ZL, Wang AY, Chai JR (2012) Influence of Ca, K concentration and pH value in solution on Cd toxicity to tobacco in solution culture. Chin Tob Sci 33:79–84Google Scholar
  28. Lexmond TM, Vorm PDJ (1981) The effect of soil pH on copper toxicity to hydroponically grown maize. Neth J Agric Sci 29:209–230Google Scholar
  29. Li B, Zhang X, Ma YB (2009) Refining a biotic ligand model for nickel toxicity to barley root elongation in solution culture. Ecotoxicol Environ Saf 72:1760–1766CrossRefGoogle Scholar
  30. Lock K, Van Eeckhout H, De Schamphelaere KAC, Criel P, Janssen CR (2007) Development of a biotic ligand model (BLM) predicting nickel toxicity to barley (Hordeum vulgare). Chemosphere 66:1346–1352CrossRefGoogle Scholar
  31. Meyer JS, Santore RC, Bobbitt JP, DeBrey LD, Boese CJ, Paquin PR, Allen HE, Bergman HL, Di Toro DM (1999) Binding of nickel and copper to fish gills predicts toxicity when water hardness varies, but free-ion activity does not. Environ Sci Technol 33:913–916CrossRefGoogle Scholar
  32. Morel F, Hering JG (1993) Principles and applications of aquatic chemistry. Wiley, New YorkGoogle Scholar
  33. OECD (2006) OECD Test Guideline 208: Terrestrial plant test—seedling emergence and seedling growth test. OECD Guidelines for the Testing of Chemicals, ParisCrossRefGoogle Scholar
  34. Paquin PR, Gorsuch JW, Apte S, Batley GE, Bowles KC, Campbell PGC, Delos CG, Di Toro DM, Dwyer RL, Galvez F, Gensemer RW, Goss GG, Hogstrand C, Janssen CR, McGeer JC, Naddy RB, Playle RC, Santore RC, Schneider U, Stubblefield WA, Wood CM, Wu KB (2002) The biotic ligand model: a historical overview. Comp Biochem Physiol C 133:3–35Google Scholar
  35. Peijnenburg W, Baerselman R, de Groot A, Jager T, Leenders D, Posthuma L, Van Veen R (2000) Quantification of metal bioavailability for Lettuce (Lactuca sativa L.) in field soils. Arch Environ Contam Toxicol 39:420–430CrossRefGoogle Scholar
  36. Rooney CP, Zhao FJ, McGrath SP (2007) Phytotoxicity of nickel in a range of European soils: influence of soil properties, Ni solubility and speciation. Environ Pollut 145:596–605CrossRefGoogle Scholar
  37. Shannon MC, Grieve CM (1999) Tolerance of vegetable crops to salinity. Sci Hortic 78:5–38CrossRefGoogle Scholar
  38. Snavely MD, Gravina SA, Cheung TT, Miller CG, Maguire ME (1991) Magnesium transport in Salmonella typhimurium. Regulation of mgtA and mgtB expression. J Biol Chem 266:824–829Google Scholar
  39. Steiner AA (1961) A universal method for preparing nutrient solutions of a certain desired composition. Plant Soil 15:134–154CrossRefGoogle Scholar
  40. Stevens DP, McLaughlin MJ, Heinrich T (2003) Determining toxicity of lead and zinc runoff in soils: salinity effects on metal partitioning and on phytotoxicity. Environ Toxicol Chem 22:3017–3024CrossRefGoogle Scholar
  41. Thakali S, Allen HE, Di Toro DM, Ponizovsky AA, Rooney CP, Zhao FJ, McGrath SP (2006a) A terrestrial biotic ligand model. 1. Development and application to Cu and Ni toxicities to barley root elongation in soils. Environ Sci Technol 40:7085–7093CrossRefGoogle Scholar
  42. Thakali S, Allen HE, Di Toro DM, Ponizovsky AA, Rooney CP, Zhao FJ, McGrath SP, Criel P, Van Eeckhout H, Janssen CR, Oorts K, Smolders E (2006b) Terrestrial biotic ligand model. 2. Application to Ni and Cu toxicities to plants, invertebrates, and microbes in soil. Environ Sci Technol 40:7094–7100CrossRefGoogle Scholar
  43. US EPA (1985) Guidelines for deriving numerical national water quality criteria for the protection of aquatic organisms and their uses. PB85-227049. United States Environmental Protection Agency, Office of Research and Development, WashingtonGoogle Scholar
  44. US EPA (1988) Protocols for short term toxicity screening of hazardous waste sites. EPA600/3-88/029. United States Environmental Protection Agency, Office of Water, WashingtonGoogle Scholar
  45. Valerio ME, García JF, Peinado FM (2007) Determination of phytotoxicity of soluble elements in soils, based on a bioassay with lettuce (Lactuca sativa L.). Sci Total Environ 378:63–66CrossRefGoogle Scholar
  46. Van Wyk BE (2005) Food plants of the world: an illustrated guide. Timber Press, PortlandGoogle Scholar
  47. Voigt A, Hendershot WHH, Sunahara GI (2006) Rhizotoxicity of cadmium and copper in soil extracts. Environ Toxicol Chem 25:692–701CrossRefGoogle Scholar
  48. Wang P, Zhou DM, Li LZ, Luo XS (2010a) Evaluating the biotic ligand model for toxicity and the alleviation of toxicity in terms of cell membrane surface potential. Environ Toxicol Chem 29:1503–1511CrossRefGoogle Scholar
  49. Wang P, Zhou DM, Peijnenburg WJGM, Li LZ, Weng NY (2010b) Evaluating mechanisms for plant-ion (Ca2+, Cu2+, Cd2+ or Ni2+) interactions and their effectiveness on rhizotoxicity. Plant Soil 334:277–288CrossRefGoogle Scholar
  50. Wildner GF, Henkel J (1979) The effect of divalent metal ions on the activity of Mg2+ depleted ribulose-1, 5-bisphosphate oxygenase. Planta 146:223–228CrossRefGoogle Scholar
  51. Worms IAM, Wilkinson KJ (2007) Ni uptake by a green alga. 2. Validation of equilibrium models for competition effects. Environ Sci Technol 41:4264–4270CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Yang Liu
    • 1
  • Martina G. Vijver
    • 1
  • Willie J. G. M. Peijnenburg
    • 1
    • 2
  1. 1.Institute of Environmental Sciences (CML)Leiden UniversityLeidenThe Netherlands
  2. 2.National Institute of Public Health and the Environment (RIVM)BilthovenThe Netherlands

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