Environmental Monitoring and Assessment

, Volume 116, Issue 1–3, pp 245–262 | Cite as

Ecotoxicological Assessment of the Impact of Residual Heavy Metals on Soil Nematodes in the Guadiamar River Basin (Southern Spain)

  • Sara Sánchez-MorenoEmail author
  • Julio A. Camargo
  • Alfonso Navas


On 25 April 1998, as a consequence of the breaking of a dam containing the tailings of a pyrite mine, a land strip of approximately 43 km in length was covered with a layer of black sludge, containing high levels of heavy metals, along the Guadiamar River Basin (southern Spain). In this investigation we carried out an ecotoxicological assessment (field and laboratory studies) of the impact of residual heavy metals (Cu, Pb, Zn, Ni) on soil nematodes in the impacted riparian zone, two years after the huge mine spillage. Concentrations of residual heavy metals were significantly (P<0.05) higher at the impacted sampling sectors (S-2, S-3, S-4, S-5) than at the unpolluted (reference) sampling sector (S-1). Nickel however exhibited the lowest increases at the impacted sectors. As a consequence, correlation coefficients between concentrations of heavy metals and values of ecological indices were not significant for Ni. In contrast, copper, lead and zinc exhibited significant (P<0.05) negative correlation coefficients with ecological indices, particularly with diversity indices (including the~number of taxa). In addition, the toxicity of Cu and Pb to nematode test species (Aphelenchus avenae and Cephalobus persegnis) during short-term toxicity bioassays was much higher than the toxicity of Zn and Ni. We conclude that residual heavy metals were still influencing adversely the community of soil nematodes in the impacted riparian zone of the Guadiamar River Basin. Cu, Pb and, to a lesser extent, Zn would be major responsible for the observed impact.


ecotoxicological assessment environmental impact Guadiamar river basin heavy metals soil nematodes 


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  1. Anderson, R. V., Coleman, D. C., Cole, C. V. and Elliot, E. T.: 1981, ‘Effects of the nematodes Acrobeloides spp. and Mesodiplogaster lherithieri on substrate utilization and nitrogen and phosphorus mineralization in soil’, Ecology 62, 549–555.CrossRefGoogle Scholar
  2. Anderson, G. L., Boyd, W. A. and Williams, P. L.: 2001, ‘Assessment of sublethal endpoints for toxicity testing with the nematode Caenorhabditis elegans’, Environ. Toxicol. Chem. 20(4), 833–838.CrossRefGoogle Scholar
  3. Bääth, E., Lohm, U., Lundgren, B., Rosswall, T., Söderström, B. and Sohlenius, B.: 1981, ‘Impact of microbial-feeding animals on total soil activity and nitrogen dynamics: A soil microcosm experiment’, Oikos 37, 257–264.Google Scholar
  4. Bengtsson, J.: 2002, ‘Disturbance and resilience in soil animal communities’, Eur. J. Soil Biol. 38, 119–125.CrossRefGoogle Scholar
  5. Bernard, E. C.: 1992, ‘Soil nematode biodiversity’, Biol. Fertil. Soils 14, 99–103.CrossRefGoogle Scholar
  6. Bongers, T.: 1990: ‘The maturity index: An ecological measure of environmental disturbance based on nematode species composition’, Oecologia 83, 14–19.CrossRefGoogle Scholar
  7. Bongers, T. and Bongers, M.: 1998, ‘Functional diversity of nematodes’, Appl. Soil Ecol. 10, 239–251.CrossRefGoogle Scholar
  8. Bongers, T. and Ferris, H.: 1999, ‘Nematode community structure as a bioindicator in environmental monitoring’, Trends Ecol. Evol. 14, 224–228.CrossRefGoogle Scholar
  9. Bongers, T., Ilieva-Makulec, K. and Ekschmitt, K.: 2001, ‘Acute sensitivity of nematode taxa to CuSO4 and relationships with feeding-type and life-history classification’, Environ. Toxicol. Chem. 20, 1511–1516.CrossRefGoogle Scholar
  10. Cabrera, F., Clemente, L., Díaz-Barrientos, E., López, R. and Murillo, J. M.: 1999, ‘Heavy metal pollution of soils affected by the Guadiamar toxic flood’, Sci. Total Environ. 242, 117–129.CrossRefGoogle Scholar
  11. Camargo, J. A.: 1992, ‘Temporal and spatial variations in dominance, diversity and biotic indices along a limestone stream receiving a trout farm effluent’, Water Air Soil Pollut. 63, 343–359.CrossRefGoogle Scholar
  12. Camargo, J. A.: 1995, ‘On measuring species evenness and other associated parameters of community structure’, Oikos 74, 538–542.Google Scholar
  13. Camargo, J. A., Nombela, G., Muñiz, M. and Navas, A.: 1998, ‘Age specific sensitivity of the nematode Aphelenchus avenae to mercury toxicity’, Bull. Environ. Contam. Toxicol. 61, 149–153.CrossRefGoogle Scholar
  14. Cañizares-Villanueva, R. O., Martínez-Jerónimo, F. and Espinosa Chávez, F.: 2000, ‘Acute toxicity to Daphnia magna of effluents containing Cd, Zn, and a mixture Cd—Zn, after metal removal by Chlorella vulgaris’, Environ. Toxicol. 15(3), 160–164.CrossRefGoogle Scholar
  15. Cheung, S. G., Tai, K. K., Leung, C. K. and Siu, Y. M.: 2002, ‘Effects of heavy metals on the survival and feeding behaviour of the sandy shore scavenging gastropod Nassarius festivus (Powys)’, Mar. Pollut. Bull. 1(12), 107–113.CrossRefGoogle Scholar
  16. Cioci, L. K., Qiu, L. and Freedman, H.: 2000, ‘Transgenic strains of the nematode Caenorhabditis elegans as biomonitors of metal contamination’, Environ. Toxicol. Chem. 19, 2122–2129.CrossRefGoogle Scholar
  17. Cragg, R. G. and Bardgett, R. D.: 2001, ‘How changes in soil faunal diversity and composition within a trophic group influence decomposition processes’, Soil Biol. Biochem. 33, 2073–2081.CrossRefGoogle Scholar
  18. De Deyn, G. B., Raaijmakers, C. E., Zoomer, H. R., Berg, M. P., Rulter, P. C., Verhoef, H. A., Bezemer, T. M. and Van der Putten, W. H.: 2003, ‘Soil invertebrate fauna enhances grassland succession and diversity’, Nature 422, 711–713.CrossRefGoogle Scholar
  19. De Goede, R. G. M. and Dekker, H. H.: 1993, ‘Effects of liming and fertilization on nematode communities in coniferous forest soils’, Pedobiologia 37, 193–209.Google Scholar
  20. De Goede, R. G. M. and Bongers, T.: 1994, ‘Nematode community structure in relation to soil and vegetation characteristics’, Appl. Soil Ecol. 1, 29–44.CrossRefGoogle Scholar
  21. De Grise, A. T.: 1969, ‘Vergelijking van resultan bekomen met de opspoewattenfiltermethode (OWFM) en met de suiker-centrifuge-drijmethode (SCDM)’, in: Voor de extractie van plantenparasitaire nematoden vit de badem. Meded. Rijksfa. Landbouwwetenschappen Gent. Vol. 34, 57–69.Google Scholar
  22. Dean, J. A.: 1995, Analytical Chemistry Handbook, McGraw-Hill, New York.Google Scholar
  23. Donkin, S.G. and Dusenbery, D.B.: 1993, ‘A soil toxicity test using the nematode Caenorhabditis elegans and an effective method of recovery’, Arch. Environ. Contam. Toxicol. 25(2), 145–151.CrossRefGoogle Scholar
  24. Edwards, C. and Bohlen, P. J.: 1995, ‘The effects of contaminants on the structure and function of soil communities’, Acta Zool. Fenn. 196, 284–289.Google Scholar
  25. Ettema, C. H. and Bongers, T.: 1993, ‘Characterization of nematode colonization and succession in disturbed soil using the maturity index’, Biol. Fert. Soils 16, 79–85.CrossRefGoogle Scholar
  26. Ferris, H., Bongers, T. and De Goede, R. G. M.: 1999, ‘Nematode faunal indicators of soil food web condition’, J. Nematol. 31, 534–535.Google Scholar
  27. Freckman, D. W.: 1988, ‘Bacterivorous nematodes and organic-matter decomposition’, Agric. Ecosyst. Environ. 24, 195–217.CrossRefGoogle Scholar
  28. Freckman, D. W. and Ettema, C. H.: 1993, ‘Assessing nematode communities in agroecosystems of varying human intervention’, Agric. Ecosyst. Environ. 45, 239–261.CrossRefGoogle Scholar
  29. Georgieva, S. S., McGrath, S. P., Hooper, D. J. and Chambers, B. S.: 2002, ‘Nematodes communities under stress: The long-term effects of heavy metals in soil treated with sewage sludge’, Appl. Soil Ecol. 20, 27–42.CrossRefGoogle Scholar
  30. Grimalt, J. O., Ferrer, M. and Macpherson, E.: 1999, ‘The mine tailing accident in Aznalcollar’, Sci. Total Environ. 242, 3–11.CrossRefGoogle Scholar
  31. Haight, M., Mudry, T. and Pasternak, J.: 1982, ‘Toxicity of seven heavy metals on Panagrellus silusiae: The efficacy of the free-living nematode as an in vivo toxicological bioassay’, Nematologica 28, 1–11.CrossRefGoogle Scholar
  32. Haimi, J. and Mätäsniemi, L.: 2001, ‘Soil decomposer animal community in heavy-metal contaminated coniferous forest with and without living’, Eur. J. Soil Biol. 38, 131–136.CrossRefGoogle Scholar
  33. Heip, C., Herman, P. M. J. and Soetaert, K.: 1988, ‘Data processing, evaluation and analysis’, in: R. P. Higgins and H. Thiel (eds), Introduction to the Study of Meiofauna, Smithsonian Institution Press, Washington, DC, pp. 197–231.Google Scholar
  34. Holdway, D. A., Lok, K. and Semaan, M.: 2001, ‘The acute and chronic toxicity of cadmium and zinc to two hydra species’, Environ. Toxicol. 16(6), 557–565.CrossRefGoogle Scholar
  35. Höss, S., Henschel, T., Haitzer, M., Traunspurger, W. and Steinberg, C. E. W.: 2001, ‘Toxicity of Cd to Caenorhabditis elegans (nematoda) in whole sediment and pore water—The ambiguous role of organic matter’, Environ. Toxicol. Chem. 20, 2794–2801.CrossRefGoogle Scholar
  36. Junta Andalucía (ed.): 2000, Programa de Investigación del Corredor Verde del Guadiamar, 1999-2002, Consejería de Medio Ambiente, Junta de Andalucía, Sevilla, Spain.Google Scholar
  37. Kammenga, J. E. and Riksen, J. A. G.: 1998, ‘Test on the competition between the nematodes Plectus acuminatus and Heterocephalobus pauciannulatus’, in: H. Ló kke and C. A. M. van Gestel (eds), Handbook of Soil Invertebrate Toxicity Tests, John Wiley and Sons, Chichester, pp. 227–237.Google Scholar
  38. Kammenga, J. E., van Koert, P. H. G., Riksen, J. A. G., Korthals, G. W. and Bakker, J.: 1996, ‘A toxicity tests in artificial soil based on the life-history strategy of the nematode Plectus acuminatus’, Environ. Toxicol. Chem. 15, 722–727.CrossRefGoogle Scholar
  39. Karntanut, W. and Pascoe, D.: 2000, ‘A comparison of methods for measuring acute toxicity to Hydra vulgaris’, Chemosphere 41(10), 1543–1548.CrossRefGoogle Scholar
  40. Korthals, G. W., Alexiev, A. D., Lexmond, T. M., Kammenga, J. E. and Bongers, T.: 1996a, ‘Long-term effects of copper and pH on the nematode community in an agroecosystem’, Environ. Toxicol. Chem. 15, 979–985.CrossRefGoogle Scholar
  41. Korthals, G. W., van der Ende, A., van Megen, H., Lexmond, T. M., Kammenga, J. E. and Bongers, T.: 1996b, ‘Short-term effects of cadmium, copper, nickel and zinc on soil nematodes from different feeding and life-history strategy groups’, Appl. Soil Ecol. 4, 107–117.CrossRefGoogle Scholar
  42. Korthals, G. W., Popovici, I., Iliev, I. and Lexmond, T. M.: 1998, ‘Influence of perennial ryegrass on copper and zinc affected terrestial nematode community’, Appl. Soil Ecol. 10, 73–85.CrossRefGoogle Scholar
  43. Korthals, G. W., Bongers, M., Fokkema, M., Dueck, Th. A. and Lexmond, Th. A.: 2000, ‘Join toxicity of copper and zinc to a terrestial nematode community in an agroecosistem’, Ecotoxicology 9, 219–228.CrossRefGoogle Scholar
  44. Ladislav, H.: 2003, ‘Recovery of soil nematode populations from cropping stress by natural secondary succession to meadow land’, Appl. Soil Ecol. 22(3), 255–270.CrossRefGoogle Scholar
  45. Lee, G., Ellersieck, M. R., Mayer, F. L. and Krause, G. F.: 1995, ‘Predicting chronic lethality of chemicals to fishes from acute toxicity test data: Multifactor probit analysis’, Environ. Toxicol. Chem. 14, 345–349.Google Scholar
  46. Ló kke, H. and van Gestel, C. A. M. (eds), 1998, Handbook of Soil Invertebrate Toxicity Tests, John Wiley and Sons, Chichester.Google Scholar
  47. MacArthur, R. H.: 1972, Geographical Ecology: Patterns in the Distribution of Species, Harper and Row Publishers, New York.Google Scholar
  48. MAPA: 1994, Métodos Oficiales de Análisis, Ministerio de Agricultura Pesca y Alimentación, Madrid.Google Scholar
  49. Nagy, P.: 1999, ‘Effect of an artificial metal pollution on nematode assemblage of a calcareous loamy chernozem soil’, Plant Soil 212, 35–43.CrossRefGoogle Scholar
  50. Neher, D. A., Peck, S. L., Rawlings, J. O. and Campbell, C. L.: 1995, ‘Measures of nematode community structure and sources of variability among and within agricultural fields’, Plant Soil 170, 167–181.CrossRefGoogle Scholar
  51. Nombela, G., Navas, A. and Bello, A.: 1999, ‘Nematodes as bioindicators of dry pasture recovery after temporary rye cultivation’, Soil Biol. Biochem. 31, 535–541.CrossRefGoogle Scholar
  52. Popovici, I.: 1993, ‘Soil nematodes used in detection of habitat disturbance due to industrial pollution’, Studia Univ. Babes-Bolyai, Biologia XXXVII(2), 15–27.Google Scholar
  53. Ruess, L. and Funke, W.: 1992, ‘Effects of experimental acidification on nematode populations in soil cultures’, Pedobiologia 36, 231–239.Google Scholar
  54. Simon, M., Ortiz, L., Garcia, I., Fernandez, J., Fernandez, E., Dorronsoro, C. and Aguilar, J.: 1999, ‘Pollution of soils by the toxic spill of a pyrite mine (Aznalcollar, Spain)’, Sci. Total Environ. 242, 105–115.CrossRefGoogle Scholar
  55. Simpson, E. H.: 1949, ‘Measurement of diversity’, Nature 163, 688.Google Scholar
  56. Smit, C. E., Schouten, A. J., Van den Brink, P. J., van Esbroek, M. L. P. and Posthuma L.: 2002, ‘Effects of zinc contamination on a natural nematode community in outdoor soil mesocosms’, Arch. Environ. Contam. Toxicol. 42(2), 205–216.CrossRefGoogle Scholar
  57. Sohlenius, B.: 1980, ‘Abundance, biomass and contribution to energy flow by soil nematodes in terrestrial ecosystems’, Oikos 34, 186–194.Google Scholar
  58. Talavera, M. and Navas, A.: 2002, ‘Incidence of plant parasitic nematodes in natural and semi-natural mountain grassland and the host status of some common grass species’, Nematology 4, 541–552.CrossRefGoogle Scholar
  59. U. S. Environmental Protection Agency: 1991, Multifactor Probit Analysis, USEPA 600/X-91-101, Washington, DC.Google Scholar
  60. Urzelai, A., Hernández, A. J. and Pastor, J.: 2000, ‘Biotic indices based on soil nematode communities for assessing soil quality in terrestrial ecosystems’, Sci. Total Environ. 247, 253–261.CrossRefGoogle Scholar
  61. Wah Chu, K. and Chow, K. L.: 2002, ‘Synergetic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative’, Aquatic Toxicol. 61, 53–64.CrossRefGoogle Scholar
  62. Wall, J. W., Skene, K. R. and Neilson, R.: 2001, ‘Nematode community and trophic structure along a sand dune succession’, Biol. Fert. Soils 35, 293–301.CrossRefGoogle Scholar
  63. Wasilewska, L.: 1997, ‘Soil invertebrates as bioindicators, with special reference to soil-inhabiting nematodes’, Russ. J. Nematol. 5(2), 113–126.Google Scholar
  64. Weiss, B. and Larink, O.: 1991, ‘Influence of sewage sludge and heavy metals on nematodes in arable soil’, Biol. Fert. Soils 12, 5–9.CrossRefGoogle Scholar
  65. Williams, P. and Dusenbery, D. B.: 1990, ‘ Aquatic toxicity testing usign the nematode Caenorhabditis elegans’, Environ. Toxicol. Biochem. 9, 1285–1290.Google Scholar
  66. Willuhn, J., Otto, A., Koewius, H. and Wunderlich, F.: 1996, ‘Subtoxic cadmium-concentrations reduce copper toxicity in the earthworm Enchytraeus buchholzi’, Chemosphere 32(11), 2205–2210.CrossRefGoogle Scholar
  67. Wolters, V.: 2001, ‘Biodiversity of soil animals and its function’, Eur. J. Soil Biol. 37, 221–227.CrossRefGoogle Scholar
  68. Yeates, G. W.: 1987, ‘How plant affects nematodes’, Adv. Ecol. Res. 17, 61–105.CrossRefGoogle Scholar
  69. Yeates, G. W.: 1990, ‘Effect of three tillage regimes on plant and soil nematodes in oats/maize rotation’, Pedobiologia 34, 379–387.Google Scholar
  70. Yeates, G. W.: 1994, ‘Modification and qualification of the nematode maturity index’, Pedobiologia 38, 97–101.Google Scholar
  71. Yeates, G. W.: 2003, ‘Nematodes as soil indicators: Functional and biodiversity aspects’, Biol. Fertil. Soils 37, 199–210.Google Scholar
  72. Yeates, G. W., Bongers, T., De Goede, R. G. M., Freckman, D. W. and Georgieva, S. S.: 1993, ‘Feeding habits in nematode families and genera: An outline for soil ecologists’, J. Nemat. 25, 315–331.Google Scholar
  73. Yeates, G. W. and Coleman, D. C.: 1982, ‘Role of nematodes in decomposition’, in: D. W. Freckman (ed), Nematodes in Soil Ecosystems, University of Texas Press, Austin, pp. 55–80.Google Scholar
  74. Yeates, G. W., Orchard, V. A., Speir, T. W., Hunt, J. L. and Hermans, M. C. C.: 1994, ‘Impact of pasture contamination by copper, chromium, arsenic timber preservative on soil biological activity’, Biol. Fertil. Soils 18, 200–208.CrossRefGoogle Scholar
  75. Zar, J. H.: 1984, Biostatistical Analysis, 2nd ed., Prentice-Hall International, New Jersey.Google Scholar
  76. Zullini, A. and Peretti, E.: 1986, ‘Lead pollution and moss-inhabiting nematodes of an industrial area’, Water Air Soil Pollut. 27, 403–410.CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Sara Sánchez-Moreno
    • 1
    • 2
    • 3
    Email author
  • Julio A. Camargo
    • 1
  • Alfonso Navas
    • 2
  1. 1.Departamento de Ecología, Facultad de BiologíaUniversidad de AlcaláAlcalá de Henares (Madrid)Spain
  2. 2.Departamento de Biodiversidad y Biología EvolutivaMuseo Nacional de Ciencias Naturales, C.S.I.C.MadridSpain
  3. 3.Department of NematologyUniversity of California, DavisDavisUSA

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