, Volume 27, Issue 5, pp 590–604 | Cite as

The behaviour of the nematode, Steinernema feltiae (Nematoda: Steinernematidae) in sand contaminated with the industrial pollutant chromium VI

  • Stephen Boyle
  • Thomais Kakouli-Duarte


This study set out to determine the suitability of the nematode Steinernema feltiae as a bioindicator for heavy metal pollution, specifically chromium VI. Nematodes were introduced into sand contaminated with concentrations of Cr VI+, in a range between 10 and 100 ppm, in increments of 10. Reproductive potential, development times and infectivity vs exposure times to Cr VI were employed as endpoints. It was observed that infective juveniles (IJ) from this nematode can survive and successfully infect host insects in the presence of Cr VI for as much as 13 days, and that the nematode increases its reproductive potential at concentrations up to 100 ppm Cr VI+. Conversely, development times (time in days taken for progeny to emerge after larval host death) and IJ infectivity rates were observed to reduce with increasing concentrations of Cr VI. The ability of this nematode to survive in the presence of high concentrations of Cr VI, and its ability to increase progeny numbers at the early stages of Cr VI exposure may provide a survival advantage for this nematode at contaminated sites. It may also demonstrate potential for development as a model species for toxicological assessment in in-situ field sampling.


Nematode EPN Chromium VI Soil Pollution Bioindicator Mutagen 



This project was funded by the Environmental Protection Agency (EPA) Ireland under the ERTDI Postdoctoral Fellowship Programme, Ref No: 2008-FS-28-M1 and the STRIVE programme 2006–2013. The authors would like to thank Ms. Laura Mestre Alvarez for her invaluable assistance with the laboratory work. We also wish to thank the anonymous reviewers for the interesting and challenging comments.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

No informed consent was required for this reported work.


  1. American society of testing and materials - ASTM E2172-01 (2014). Standard guide for conducting laboratory soil toxicity tests with the nematode Caenorhabditis elegans. ASTM International, West Conshohocken, PA, USA, 2014.
  2. Anderson GL, Boyd WA, Williams PL (2001) Assessment of sub-lethal endpoints for toxicity testing with the nematode Caenorhabditis elegans. Environ Toxicol Chem 20(4):833–838CrossRefGoogle Scholar
  3. Bakonyi G, Nagy P, Kadar In (2003) Long term affects of heavy metals and microelements on nematode assemblages. Toxicol Lett 140-141:391–401CrossRefGoogle Scholar
  4. Balasubramanian S, Pugalenthi V (1999) Determination of total chromium in tannery waste water by inductivity coupled with plasma-atomic emission spectrometry, flame atomic absorption spectrometry and UV-visible spectrophotometric methods. Talanta 50:457–467CrossRefGoogle Scholar
  5. Barceloux D (1999) Chromium. Clinic Toxicol 37(2):173–194Google Scholar
  6. Black MC, Williams PL (2001) Preliminary assessment of metal toxicity in the middle Tisza River (Hungary) flood plain. J Soils Sed 1(4):213–216CrossRefGoogle Scholar
  7. Boemare NE, Akhurst RJ (1990) Physiology of phase variation in Xenorhabdus pp. Proc Int Colloq Invert Pathol Micro Control 5:208–212Google Scholar
  8. Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Evol Ecol 14:224–228CrossRefGoogle Scholar
  9. Boyd WA, Stringer VA, Williams PL (2001) Metal LC50’s of a soil nematode compared to published earthworm data. In: Greenberg BM, Hull RN, Roberts Jr. MH, Gensemer RW Eds Environmental toxicology and risk assessment: science, policy, and standardisation—implications for environmental decisions: tenth volume, ASTM STP 1403. American Society for Testing and Materials, West Conshohocken, PA, p 2001Google Scholar
  10. Boyd WA, Williams PL (2003a) Availability of metals to the nematode Caenorhabditis elegans: toxicity based on total concentrations in soil and extracted fractions. Environ Toxicol Chem 22(5):1100–1106CrossRefGoogle Scholar
  11. Boyd WA, Williams PL (2003b) Comparison of the sensitivity of three nematode species to copper and their utility in aquatic and soil toxicity species. Environ Toxicol Chem 22(11):2768–2774CrossRefGoogle Scholar
  12. Boyle S, Kakouli-Duarte T (2008) The effects of chromium VI on the fitness and on the beta-tubulin genes during in-vivo development of the nematode Steinernema feltiae. Sci Total Environ 404:56–67CrossRefGoogle Scholar
  13. Brown RL, Bowman RS, Kieft TL (1994) Microbial effects of nickel and cadmium sorption and transport in vocanic tuff. J Environ Qual 23:723–729CrossRefGoogle Scholar
  14. Coleman RN (1988) Chromium toxicity: effects in microorganisms with special reference to the soil matrix. In: Nriagu JO, Nieboer E (Eds) Chromium in natural and human environments. Wiley-InterScience, New York, NY, pp 335–350Google Scholar
  15. Dhawan R, Dusenbery DB, Williams PL (1999) Comparison of lethality, reproduction and behaviour as toxicological endpoints in the nematode Caenorhabditis elegans. J Toxicol Environ Health, Part A 58:451–462CrossRefGoogle Scholar
  16. Dillon A, Griffin C, Downes M (1999) Hylobius Interest Group activity report No. 2. Second meeting of the Hylobius Interest Group. National University of Ireland, MaynoothGoogle Scholar
  17. Donkin SG, Dusenbery DB (1994) Using the Caenorhabditis elegans soils toxicity test to identify factors affecting toxicity of four metal ions in intact soil. Water Air Soil Pollut 78:359–373CrossRefGoogle Scholar
  18. Eagon GR (1984) The resistance characteristics of Pseudomonads. Developments in industrial microbiology 25:337–348Google Scholar
  19. Farag AM, May T, Marty GD, Easton M, Harper DD, Little EE, Cleveland L (2006) The effects of chronic chromium exposure on the health of Chinook salmon (Oncorhynchus tshawytscha). Aquat Toxicol 76:246–257CrossRefGoogle Scholar
  20. Grewal P, Converse V, Georgis R (1999) Influence of production and bioassay methods on infectivity of two ambush foragers (Nematoda: Steinernematidae). J Invertebr Pathol 73:40–44CrossRefGoogle Scholar
  21. Griffin C, Moore J, Downes M (1991) Occurrence of insect-parasitic nematodes (Heterorhabditidae, Steinernematidae) in the Republic of Ireland. Nematologica 37:92–100CrossRefGoogle Scholar
  22. Gyedu-Ababio TK, Baird D (2006) Response of meiofauna and nematode communities to increased levels of contaminants in a laboratory microcosm experiment. Ecotoxicol Environ Saf 63:443–450CrossRefGoogle Scholar
  23. Harmon SM, Wyatt DE (2008) Evaluation of post-Katrina flooded soils for contaminants and toxicity to the soil invertebrates Eisenia fetida and Caenorhabditis elegans. Chemosphere 70:1857–1864CrossRefGoogle Scholar
  24. Hazir S, Stock P, Kaya H, Koppenhofer A, Keskin N (2001) Developmental temperature effects on five geographic isolates of the entomopathogenic nematode Steinernema feltiae (Nematoda: Steinernematidae). J Invertebr Pathol 77:243–250CrossRefGoogle Scholar
  25. Hitchcock DR, Black MC, Williams PL (1997) Investigations into using the nematode Caenorhabditis elegans for municipal and industrial wastewater toxicity testing. Arch Environ Contam Toxicol 33:252–260CrossRefGoogle Scholar
  26. Jaworska M, Gorczyca A (2000) The effects of metal ions on mortality, pathogenicity and reproduction of entomopathogenic nematodes Steinernema feltiae Filipjev (Rhabditida, Steinernematidae). Pol J Environ Stud 11:517–519Google Scholar
  27. Kammenga JE, Riksen JAG (1996) Comparing differences in species sensitivity to toxicants: phenotypic plasticity versus concentration—response relationships. Environ Toxicol Chem 15:1649–1653CrossRefGoogle Scholar
  28. Kammenga JE, Vankoert PHG, Riksen JAG, Korthals GW, Bakker JA (1996) A toxicity test in artificial soil based on the life history strategy of the nematode Plectus acuminates. Environ Toxicol Chem 15:722–727CrossRefGoogle Scholar
  29. Khanna N, Cressman III CP, Tatara CP, Williams PL (1997) Tolerance of the nematode Caenorhabditis elegans to pH, salinity and hardness in aquatic media. Arch Environ Contam Toxicol 32:110–114CrossRefGoogle Scholar
  30. Korthals GW, van der Ende A, van Megen H, Lexmond TM, Kammenga JE, Bongers T (1996) Short term effects of cadmium, copper, nickel and zinc on soil nematodes from different feeding and life history strategy groups. Appl Soil Ecol 4:107–117CrossRefGoogle Scholar
  31. Lewis EE, Shapiro-Ilan DI (2002) Host cadavers protect entomopathogenic nematodes during freezing. J Invert Pathol 81:25–32CrossRefGoogle Scholar
  32. Lind DA, Marchal WG, Wathen SA (2006) Basic statistics in business and economics. McGraw-Hill/Irwin, Boston, USAGoogle Scholar
  33. Lokke H, van Gestel CAM (1998) Handbook of soil invertebrate toxicity tests. John Wiley & Sons, ChichesterGoogle Scholar
  34. Malakhov VV (1994) Nematodes, structure, development, classification and phylogeny. Smithsonian Institution Press, Washington, DCGoogle Scholar
  35. McGrath D, Carton O, Diamond S, O’Sullivan A, Murphy W, Rogers P, Parle P, Byrne E (2001) Investigation of animal health problems at Askeaton, Co. Limerick: soil, herbage, feed and water. EPA, Johnstown Castle Estate, Wexford, IrelandGoogle Scholar
  36. Millward RN, Carman KR, Fleeger JW, Gambrell RP, Rodney TP, Rouse M-AM (2001) Linking ecological impact to metal concentrations and speciation: a microcosm experiment using a salt marsh meiofaunal community. Environ Toxicol Chem 20(9):2029–2037CrossRefGoogle Scholar
  37. Nagy P, Bakonyi G, Bongers T, Kadar I, Fabian M, Kiss I (2004) Effects of microelements on soil nematode assemblages seven years after contaminating an agricultural field. Sci Environ 320:131–143Google Scholar
  38. Norseth T (1981) The carcinogenicity of chromium. Eviron Health Perspect 40:121–130CrossRefGoogle Scholar
  39. O’Brien TJ, Fornsaglio JL, Patierno SR (2002) Effects of hexavalent chromium on the survival and cell cycle distribution of DNA repair-deficient S. cerevisiae. DNA Repair 1:617–627CrossRefGoogle Scholar
  40. Parameswari E, Lakshmanan A, Thilagavathi T (2009) Bioasorption of chromium VI and nickel (II) by bacterial isolates from an aqueous solution. Electron J Environ, Agric Food Chem 8(3):150–156Google Scholar
  41. Peredney CL, Williams PL (2000) Utility of Caenorhabditis elegans for assessing heavy metal contamination in artificial soil. Arch Environ Contam Toxicol 39:113–8Google Scholar
  42. Perez E, Lewis E, Shapiro-Ilan D (2004) Effect of application method on fitness of entomopathogenic nematodes emerging at different times. J Nem 36:534–539Google Scholar
  43. Perez-Benito JF (2006) Effects of chromium VI and vanadium V in the lifespan of fish. J Trace Elem Med Biol 20:161–170CrossRefGoogle Scholar
  44. Pionar G (1990) Taxonomy and biology of Steinernematidae and Heterhabditidae. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control, CRC Press Boca Raton, FL, USA, pp 23–61Google Scholar
  45. Richard FC, Bourg ACM (1991) Aqueous geochemistry of chromium: a review. Water Res 25:807–816CrossRefGoogle Scholar
  46. Rocchetta I, Mazzuca M, Conforti V, Ruiz L, Balzaretti V, del Carmen Rios de Molina M (2006) Effects of chromium on the fatty acid composition of two strains of Euglena gracilis. Environ Pollut 141:353–358CrossRefGoogle Scholar
  47. Rolston A (2004) Distribution, relatedness, fitness and behaviour of entomopathogenic nematodes from Bull Island, Dublin. PhD thesis. National University of Ireland, Maynooth, IrelandGoogle Scholar
  48. Ruppert EE, Barnes RD (1994). Invertebrate Zoology, 6th edn. Saunders College Publishing, Harcourt Brace and Company. Orlando, Florida, USAGoogle Scholar
  49. Shrivastava R, Upreti RK, Seth PK, Chaturvedi UV (2002) Effects of chromium on the immune system. FEMS Immun Med Micro 34:1–7CrossRefGoogle Scholar
  50. Sochova I, Hofman J, Holoubek I (2007) Effects of seven organic pollutants on soils nematode Caenorhabditis elegans. Environ Intern 33:798–804CrossRefGoogle Scholar
  51. Sorensen MA, Jensen PD, Walton WE, Trumble JT (2006) Acute and chronic activity of perchlorate and hexavalent chromium contamination on the survival and development of Culex quinquefasciatus Say (Diptera: Culicidae). Environ Pollut 144:759–764CrossRefGoogle Scholar
  52. Sivakumar S, Subbhuraam V (2005) Toxicity of chromium(III) and chromium(VI) to the earthworm Eisenia fetida. Ecotoxicol Environ Saf 62:93–98CrossRefGoogle Scholar
  53. Van Gestel CAM, van Straalen NM (1994) Ecotoxicological test systems for terrestrial invertebrates. In: Donker MH, Eijsackers H, Heimback F (eds) Ecotoxicology of soil organisms. CRC Press, Inc., Boca Ranton, pp 205–228Google Scholar
  54. van Straalen NM, Van Gestel CAM (1993) Soil invertebrates and microorganisms. In: Calow P (ed) Handboook of ecotoxicology, Vol. 1. Blackwell Publishing. Oxford, UK, pp 251–276Google Scholar
  55. Vasanthy M (2004) An investigation on removal of chromium VI using bacterial strains. Asian J Microbiol Biotech Env Sci 7(1):38–46Google Scholar
  56. van Vliet CJ, de Goede GM (2008) Nematode-based risk assessment of mixture toxicity in a moderately polluted river floodplain in the Netherlands. Sci Total Environ 406:449–454CrossRefGoogle Scholar
  57. Velma v, Vutukuru S, Tchounwou p (2009) Ecotoxicology of Hexavalent Chromium in Freshwater Fish: A Critical Review. Rev Envrion Health 24(2):129–145Google Scholar
  58. Wang DY, Wang Y (2008) Phenotypic and behavioural defects caused by Barium exposure in nematode Caenorhabditis elegans. Arch Environ Contam Toxicol 54:447–453CrossRefGoogle Scholar
  59. Weiss B, Larink O (1991) Influence of sewage sludge and heavy metals on nematodes in an arable soil. Biol Fert Soils 12:5–9CrossRefGoogle Scholar
  60. Williams P, Dusenbery D (1990) Aquatic toxicity testing using the nematode Caenorhabditis elegans. Environ Toxicol Chem 9:1285–1290CrossRefGoogle Scholar
  61. WHO Document (2000) Chapter 6.4; chromium. Air Quality Guidelines. World Health Organsiation Regional Office for Europe, Copenhagen, DenmarkGoogle Scholar
  62. Womersley CZ (1993) Factors affecting physiological fitness and modes of survival employed by dauer juveniles and their relationship to pathogenicity. In: Bedding R, Akhurst R, Kaya H (eds.) Nematodes and the biological control of insect pests. CSIRO, East Melbourne, Victoria, Australia, pp 79–88Google Scholar
  63. White G (1927) A method for obtaining infective nematode larvae from cultures. Science 66:302CrossRefGoogle Scholar
  64. Yoder C, Grewal P, Taylor A (2004) Rapid age-related changes in infection behaviour of entomopathogenic nematodes. J Parasitol 90:1229–1234CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Science and Health, enviroCORE, Molecular Ecology and Nematode Research GroupInstitute of Technology CarlowCarlowIreland

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