Assessment of toxicity of heavy metal-contaminated soils toward Collembola in the paddy fields supported by laboratory tests

  • Manping Liu
  • Jie Xu
  • Paul Henning Krogh
  • Jing Song
  • Longhua Wu
  • Yongming Luo
  • Xin Ke
Research Article

Abstract

Effects on soil Collembola of Cu, Zn, Pb, and Cd pollution from Cu smelters over 40 years were investigated in paddy fields from an area of Eastern China. We compared the field effects to those observed in single-species laboratory tests employing the hemiedaphic collembolan Folsomia candida and the epedaphic Sinella curviseta obtained from laboratory cultures and exposed to field-collected polluted soil. The results indicated that different collembolan species responded differently to the pollution in the fields and could be divided into sensitive, indifferent, and tolerant types accordingly. The abundance of sensitive species decreased as the pollution increased, but this was not the same for indifferent and tolerant species. The dominant species changed from sensitive to tolerant species as the pollution increased. The reproduction of F. candida and S. curviseta was most sensitive to the contaminated soil compared to growth and survival; the sensitivity of the two species was similar. The growth was more sensitive than the survival for F. candida but not for S. curviseta. The growth and survival of F. candida were much more sensitive than those of S. curviseta. Sensitivity of field populations of F. candida (EC10 31 [15–46]) and hemiedaphic species Folsomia quadrioculata (EC10 52 [0.7–102]) were comparable with sensitivity of the reproduction of F. candida in the single-species tests (EC10 21 [14–27]), suggesting that single-species test based on laboratory cultures and field soil could be used to link laboratory and field data and then reflect the field situation. S. curviseta could be used as an epedaphic species in single-species tests and F. quadrioculata as an indicator species for assessment of field effect.

Keywords

Pollution Cu/Zn/Pb/Cd Springtail Species composition Sensitivity Single-species test 

Notes

Acknowledgements

We thank Dr. Yan Gao for Collembola identification.

References

  1. Ardestani MM, van Straalen NM, van Gestel CAM (2014) Uptake and elimination kinetics of metals in soil invertebrates: a review. Environ Pollut 193:277–295CrossRefGoogle Scholar
  2. Austruy A, Laplanche C, Mombo S, Dumat C, Deola F, Gers C (2016) Ecological changes in historically polluted soils: metal(loid) bioaccumulation in microarthropods and their impact on community structure. Geoderma 271:181–190CrossRefGoogle Scholar
  3. Bengtsson J (1998) Which species? What kind of diversity? Which ecosystem function? Some problems in studies of relations between biodiversity and ecosystem function. Appl Soil Ecol 10:191–199CrossRefGoogle Scholar
  4. Bengtsson G, Rundgren S (1988) The Gusum case—a brass mill and the distribution of soil Collembola. Can J Zool Rev Can Zool 66:1518–1526CrossRefGoogle Scholar
  5. Bressan M, Paoletti MG (1997) Leaf litter decomposition and soil microarthropods affected by sulphur dioxide fallout. Land Degrad Dev 8:189–199CrossRefGoogle Scholar
  6. Bruce LJ, McCracken DI, Foster GN, Aitken MN (1997) The effects of cadmium and zinc-rich sewage sludge on epigeic Collembola populations. Pedobiologia 41:167–172Google Scholar
  7. Bruce L, McCracken D, Foster G, Aitken M (1999) The effects of sewage sludge on grassland euedaphic and hemiedaphic collembolan populations. Pedobiologia 43:209–220Google Scholar
  8. Chagnon M, Hebert C, Pare D (2000) Community structures of Collembola in sugar maple forests: relations to humus type and seasonal trends. Pedobiologia 44:148–174CrossRefGoogle Scholar
  9. Christiansen K, Bellinger P (1980–1981) The Collembola of North America north of the Rio Grande. Grinnell College, GrinnellGoogle Scholar
  10. Crouau Y, Moia C (2006) The relative sensitivity of growth and reproduction in the springtail, Folsomia candida, exposed to xenobiotics in the laboratory: an indicator of soil toxicity. Ecotoxicol Environ Saf 64:115–121CrossRefGoogle Scholar
  11. Dai W, Ke X, Li Z, Gao M, Wu L, Chiristie P, Luo Y (2018) Antioxidant enzyme activities of Folsomia candida and avoidance of soil metal contamination. Environ Sci Pollut Res.  https://doi.org/10.1007/s11356-017-0489-x
  12. Fava F, Di Gioia D, Marchetti L (2000) Role of the reactor configuration in the biological detoxification of a dump site-polychlorobiphenyl-contaminated soil in lab-scale slurry phase conditions. Appl Microbiol Biotechnol 53:243–248CrossRefGoogle Scholar
  13. Fiera C (2009) Biodiversity of Collembola in urban soils and their use as bioindicators for pollution. Pesq Agrop Bras 44:868–873CrossRefGoogle Scholar
  14. Filser J (1995) Collembola as indicators for long-term effects of intensive management. Acta Zool Fenn 196:326–328Google Scholar
  15. Filser J, Wittmann R, Lang A (2000) Response types in Collembola towards copper in the microenvironment. Environ Pollut 107:71–78CrossRefGoogle Scholar
  16. Fjellberg A (1998) The Collembola of Fennoscandia and Denmark, part I, Poduromorpha. Fauna Entomologica Scandinavica. Brill Academic, Brill, LeidenGoogle Scholar
  17. Fountain MT, Hopkin SP (2001) Continuous monitoring of Folsomia candida (Insecta : Collembola) in a metal exposure test. Ecotoxicol Environ Saf 48:275–286CrossRefGoogle Scholar
  18. Hågvar S (1994) Log-normal distribution of dominance as an indicator of stressed soil microarthropod communities. Acta Zool Fenn 195:71–80Google Scholar
  19. Haimi J, SiiraPietikainen A (1996) Decomposer animal communities in forest soil along heavy metal pollution gradient. Fresenius J Anal Chem 354:672–675Google Scholar
  20. Holland JM, Winder L, Perry JN (2000) The impact of dimethoate on the spatial distribution of beneficial arthropods in winter wheat. Ann Appl Biol 136:93–105CrossRefGoogle Scholar
  21. Hopkin SP, Spurgeon DJ (2001) Forecasting the environmental effects of zinc, the metal of benign neglect in soil ecotoxicology. Forecast Environ Fate Eff Chem, Ecological and Environmental Toxicology Series 91–96Google Scholar
  22. ISO (2014) Soil quality—inhibition of reproduction of Collembola (Folsomia candida) by soil contaminants (ISO 11267:2014) vol ISO/TC 190/SC 4. International Organization for Standardization, GenevaGoogle Scholar
  23. Joosse ENG, Buker JB (1979) Uptake and excretion of lead by litter-dwelling Collembola. Environ Pollut 18:235–240CrossRefGoogle Scholar
  24. Juvonen R, Martikainen E, Schultz E, Joutti A, Ahtiainen J, Lehtokari M (2000) A battery of toxicity tests as indicators of decontamination in composting oily waste. Ecotoxicol Environ Saf 47:156–166.  https://doi.org/10.1006/eesa.2000.1943 CrossRefGoogle Scholar
  25. Krogh PH (1991) Perturbation of the soil microarthropod community with the pesticides benomyl and isofenphos: I. Population changes. Pedobiologia 35:71–88Google Scholar
  26. Kuznetsova NA (2009) Soil-dwelling Collembola in coniferous forests along the gradient of pollution with emissions from the Middle Ural Copper Smelter. Russ J Ecol 40:415–423CrossRefGoogle Scholar
  27. Lock K, Janssen CR (2001) Test designs to assess the influence of soil characteristics on the toxicity of copper and lead to the oligochaete Enchytraeus albidus. Ecotoxicology 10:137–144CrossRefGoogle Scholar
  28. Lock K, Janssen CR (2003) Comparative toxicity of a zinc salt, zinc powder and zinc oxide to Eisenia fetida, Enchytraeus albidus and Folsomia candida. Chemosphere 53:851–856CrossRefGoogle Scholar
  29. McGrath SP, Cunliffe CH (1985) A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sewage sludges. J Sci Food Agric 36:794–798CrossRefGoogle Scholar
  30. Naeem S, Thompson LJ, Lawler SP, Lawton JH, Woodfin RM (1994) Declining biodiversity can alter the performance of ecosystems. Nature 368:734–737CrossRefGoogle Scholar
  31. Nursita AI, Singh B, Lees E (2005) The effects of cadmium, copper, lead, and zinc on the growth and reproduction of Proisotoma minuta Tullberg (Collembola). Ecotoxicol Environ Saf 60:306–314CrossRefGoogle Scholar
  32. OECD (2004) Test no. 222: earthworm reproduction test (Eisenia fetida/Eisenia andrei). Organization for Economic Cooperation and Development, FranceCrossRefGoogle Scholar
  33. OECD (2009) Guidelines for the testing of chemicals. Test no. 232, Collembolan reproduction test in soil. Organisation for Economic Cooperation and Development, ParisGoogle Scholar
  34. Pedersen MB, van Gestel CAM (2001) Toxicity of copper to the collembolan Folsomia fimetaria in relation to the age of soil contamination. Ecotoxicol Environ Saf 49:54–59CrossRefGoogle Scholar
  35. Peveling R, Rafanomezantsoa JJ, Razafinirina R, Tovonkery R, Zafimaniry G (1999) Environmental impact of the locust control agents fenitrothion, fenitrothion-esfenvalerate and triflumuron on terrestrial arthropods in Madagascar. Crop Prot 18:659–676CrossRefGoogle Scholar
  36. Rusek J, Marshall VG (2000) Impacts of airborne pollutants on soil fauna. Annu Rev Ecol Syst 31:395–423CrossRefGoogle Scholar
  37. Russell DJ, Alberti G (1998) Effects of long-term, geogenic heavy metal contamination on soil organic matter and microarthropod communities, in particular Collembola. Appl Soil Ecol 9:483–488CrossRefGoogle Scholar
  38. SAS Institute Inc.(2004) Institute Inc., Cary, NCGoogle Scholar
  39. Salminen J, Haimi J (1998) Responses of the soil decomposer community and decomposition processes to the combined stress of pentachlorophenol and acid precipitation. Appl Soil Ecol 9:475–481CrossRefGoogle Scholar
  40. Santorufo L, Carotenuto R, Rocco A, Picione FD, Maisto G (2012a) Orthonychiurus pseudostachianus (collembola) as a toxicity test organism and selection of an ecotoxicological test battery to assess soil quality. Appl Soil Ecol 54:49–54CrossRefGoogle Scholar
  41. Santorufo L, Van Gestel CAM, Rocco A, Maisto G (2012b) Soil invertebrates as bioindicators of urban soil quality. Environ Pollut 161:57–63CrossRefGoogle Scholar
  42. Smit CE, Van Gestel CAM (1996) Comparison of the toxicity of zinc for the springtail Folsomia candida in artificially contaminated and polluted field soils. Appl Soil Ecol 3:127–136CrossRefGoogle Scholar
  43. Sørensen TS, Holmstrup M (2005) A comparative analysis of the toxicity of eight common soil contaminants and their effects on drought tolerance in the collembolan Folsomia candida. Ecotoxicol Environ Saf 60:132–139CrossRefGoogle Scholar
  44. Tranvik L, Bengtsson G, Rundgren S (1993) Relative abundance and resistance traits of 2 Collembola species under metal stress. J Appl Ecol 30:43–52CrossRefGoogle Scholar
  45. van Gestel CAM, van der Waarde JJ, Derksen JGM(A), van der Hoek EE, Veul MFXW, Bouwens S, Rusch B, Kronenburg R, Stokman GNM (2001) The use of acute and chronic bioassays to determine the ecological risk and bioremediation efficiency of oil-polluted soils. Environ Toxicol Chem 20:1438–1449CrossRefGoogle Scholar
  46. Wiles JA, Krogh PH (1998) Tests with the collembolans Isotoma viridis, Folsomia candida and Folsomia fimetaria. In: Løkke H, van Gestel CAM (eds) Handbook of soil invertebrate toxicity tests. Wiley, Chichester, pp 131–156Google Scholar
  47. Xu J, Ke X, Krogh PH, Wang Y, Luo YM, Song J (2009a) Evaluation of growth and reproduction as indicators of soil metal toxicity to the Collembolan, Sinella curviseta. Insect Sci 16:57–63CrossRefGoogle Scholar
  48. Xu J, Wang Y, Luo YM, Song J, Ke X (2009b) Effects of copper, lead and zinc in soil on egg development and hatching of Folsomia candida. Insect Sci 16:51–55CrossRefGoogle Scholar
  49. Yin WY (2000) Soil animals in China. Science Press, BeijingGoogle Scholar
  50. Yosii R (1977) Critical check list of the Japanese species of Collembola. Contrib Biol Lab Kyoto Univ 25:141–170Google Scholar
  51. Zhu D, Ke X, Wu L, Li Z, Christie P, Luo Y (2016) Ecotoxicity of cadmium in a soil collembolan-predatory mite food chain: can we use the 15N labeled litter addition method to assess soil functional change? Environ Pollut 219:37–46CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Manping Liu
    • 1
  • Jie Xu
    • 2
  • Paul Henning Krogh
    • 3
  • Jing Song
    • 4
  • Longhua Wu
    • 4
  • Yongming Luo
    • 5
  • Xin Ke
    • 2
  1. 1.Natural History Research Center, Shanghai Natural History MuseumShanghai Science and Technology MuseumShanghaiChina
  2. 2.Institute of Plant Physiology and EcologyChinese Academy of SciencesShanghaiChina
  3. 3.Department of BioscienceAarhus UniversitySilkeborgDenmark
  4. 4.Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil ScienceChinese Academy of SciencesNanjingChina
  5. 5.Yantai Institute of Coastal Zone ResearchChinese Academy of SciencesYantaiChina

Personalised recommendations