Biology and Fertility of Soils

, Volume 43, Issue 1, pp 39–50 | Cite as

Effects of sewage sludge and copper enrichment on both soil mesofauna community and decomposition of oak leaves (Quercus suber) in a mesocosm

  • Céline Pernin
  • Jean-Paul Ambrosi
  • Jérôme Cortet
  • Richard Joffre
  • Jean Le Petit
  • Elisabeth Tabone
  • Franck Torre
  • Paul Henning Krogh
Original Paper


A laboratory mesocosm experiment was performed to study the effects of copper-enriched sewage sludge application on a mesofauna community. For 12 weeks, characteristics and changes in this defined and artificial mesofauna community structure were monitored as well as the dynamics of leaf litter decomposition. The mesofauna community comprised six species of Collembola (Folsomia fimetaria, Isotomurus prasinus, Lepidocyrtus cyaneus, Mesaphorura macrochaeta, Parisotoma notabilis, Protaphorura armata), two species of acari Oribatida (Achipteria coleoptrata, Adoristes sp.), one species of acari Gamasida (Hypoaspis aculeifer) and one species of enchytraeid (Enchytraeus crypticus). Three treatments included the addition of 22 g dry weight (DW) sludge spiked with 0, 200 and 1,000 mg Cu kg−1 DW sludge in each mesocosm, and one treatment had 66 g DW sludge spiked with 1,000 mg Cu kg−1 DW sludge added in each mesocosm. Copper, complexed with sludge due to a favourable pH, had no effect on community and litter parameters when added to low amount of sludge. In contrast, tripling the sludge dose in addition to a high dose of Cu changed in time the sludge and leaf chemical composition as well as mesofauna community structure. Responses of the mesofauna to this treatment differed between species. The abundance of species such as I. prasinus, L. cyaneus, M. macrochaeta and P. notabilis decreased, whereas the abundance of H. aculeifer increased and became dominant.


Copper Decomposition Mesocosm Mesofauna Sewage sludge 


  1. Aber JD, Melillo JM (1980) Litter decomposition: measuring relative contributions of organic matter and nitrogen to forest soils. Can J Bot 58:416–421Google Scholar
  2. Achazi RK (2002) Invertebrates in risk assessment. Development of a test battery and a short term biotest for ecological risk assessment of soil. J Soils Sediments 2:174–178CrossRefGoogle Scholar
  3. Achazi RK, Fröhlich E, Henneken M, Pilz C (1999) The effect of soil from former irrigation fields and of sewage sludge on dispersal activity and colonizing success of the annelid Enchytraeus crypticus Westheide and Graefe, 1992 (Enchytraeidae, Oligochaeta). Newsl Enchytraeidae 6:117–126Google Scholar
  4. ADEME (2001) Les boues chaulées des stations d’épuration municipales: production, qualité et valeur agronomique. Col. Données et Références no 3831. ADEME, ParisGoogle Scholar
  5. Anderson JM, Ingram JSI (eds) (1993) Tropical soil biology and fertility. A handbook of methods. CAB, OxonGoogle Scholar
  6. Banerjee MR, Burton DL, Depoe S (1997) Impact of sewage sludge application on soil biological characteristics. Agric Ecosyst Environ 66:241–249CrossRefGoogle Scholar
  7. Bengtsson G, Ohlsson L, Rundgren S (1985) Influence of fungi on growth and survival of Onychiurus armatus (Collembola) in a metal polluted soil. Oecologia 68:63–68CrossRefGoogle Scholar
  8. Berti WR, Jacobs LW (1998) Distribution of trace elements in soil from repeated sewage sludge applications. J Environ Qual 27:1280–1286CrossRefGoogle Scholar
  9. Bogomolov DM, Chen SK, Parmelee RW, Subler S, Edwards CA (1996) An ecosystem approach to soil toxicity testing: a study of copper contamination in laboratory soil microcosms. Appl Soil Ecol 4:95–105CrossRefGoogle Scholar
  10. Bourrelier P-H, Berthelin J (eds) (1998) Contamination des sols par les éléments en traces: les risques et leur gestion. Rapport de l’Académie des Sciences no 42 Lavoisier Tec and Doc, ParisGoogle Scholar
  11. 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
  12. Bruce LJ, McCracken DI, Foster GN, Aitken MN (1999) The effects of sewage sludge on grassland euedaphic and hemiedaphic collembolan populations. Pedobiologia 43:209–220Google Scholar
  13. Bruus Pedersen M, Axelsen JA, Strandberg B, Jensen J, Attrill MJ (1999) The impact of a copper gradient on a microarthropods field community. Ecotoxicology 8:467–483CrossRefGoogle Scholar
  14. Bruus Pedersen M, Van Gestel CAM, Elmegaard N (2000) Effects of copper on reproduction of two collembolan species exposed through soil, food, and water. Environ Toxicol Chem 19:2579–2588CrossRefGoogle Scholar
  15. Cole LJ, McCracken DI, Foster GN, Aitken MN (2001) Using collembola to access the risks of applying metal-rich sewage sludge to agricultural land in western Scotland. Agric Ecosyst Environ 83:177–189CrossRefGoogle Scholar
  16. Cortet J, Joffre R, Elmholt S, Krogh PH (2003) Increasing species and trophic diversity of mesofauna affects fungal biomass, mesofauna community structure and organic matter decomposition processes. Biol Fertil Soils 37:302–312Google Scholar
  17. Cortez J, Aber JD, Melillo JM, McClaugherty CA (1990) Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Can J Bot 68:2201–2208CrossRefGoogle Scholar
  18. Coûteau M-M, Bottner P, Berg B (1995) Litter decomposition, climate and litter quality. Tree 10:63–66Google Scholar
  19. Cragg RG, Bardgett RD (2001) How changes in soil fauna diversity and composition within a trophic group influence decomposition processes. Soil Biol Biochem 33:2073–2081CrossRefGoogle Scholar
  20. Crouau Y, Gisclard C, Perotti P (2002) The use of Folsomia candida (collembola, Isotomidae) in bioassays of waste. Appl Soil Ecol 19:65–70CrossRefGoogle Scholar
  21. Cuppen JGM, Van den Brink PJ, Camps E, Uil KF, Brock TCM (2000) Impact of the fungicide carbendazim in freshwater microcosms. I. Water quality, breakdown of particulate organic matter and responses of macroinvertebrates. Aquat Toxicol 48:233–250CrossRefPubMedGoogle Scholar
  22. Denneman CAJ, van Straalen NM (1991) The toxicity of lead and copper in reproduction tests using the oribatid mite Platynothrus peltifer. Pedobiologia 35:305–311Google Scholar
  23. Edwards CA, Bohlen PJ (1995) The effects of contaminants on the structure and function of soil communities. Acta Zool Fenn 196:284–289Google Scholar
  24. Edwards CA, Reichle DE, Crossley DA Jr (1970) The role of soil invertebrates in turnover of organic matter and nutrients. In: Reichle DE (ed) Analysis of temperate forest ecosystems. Springer, Berlin Heidelberg New York, pp 147–172Google Scholar
  25. Filser J, Hölscher G (1997) Experimental studies on the reactions of collembola to copper contamination. Pedobiologia 41:173–178Google Scholar
  26. Filser J, Krogh PH (2002) Interactions between Enchytraeus crypticus, collembolans, gamasid mites and barley plants—a greenhouse experiment. Newsl Enchytraeidae 2:32–42Google Scholar
  27. Filser J, Wittman R, Tang A (2000) Responses type in collembolan towards copper in the microenvironment. Environ Pollut 107:71–78CrossRefPubMedGoogle Scholar
  28. Fioretto A, Di Nardo C, Papa S, Fuggi A (2005) Lignin and cellulose degradation and nitrogen dynamics during decomposition of three leaf litter species in a Mediterranean ecosystem. Soil Biol Biochem 37:1083–1091CrossRefGoogle Scholar
  29. Fountain MT, Hopkin SP (2001) Continuous monitoring of Folsomia candida (insecta:Collembola) in a metal exposure test. Ecotoxicol Environ Saf 48:275–286CrossRefPubMedGoogle Scholar
  30. Gallardo A, Merino J (1999) Control of leaf decomposition rate in a Mediterranean shrubland as indicated by N, P and lignin concentrations. Pedobiologia 43:64–72Google Scholar
  31. Gillon D, Joffre R, Ibrahima A (1999) Can litter decomposability be predicted by near infrared reflectance spectroscopy? Ecology 80:175–186CrossRefGoogle Scholar
  32. Gobat J-M, Aragno M, Matthey W (eds) (1998). Le sol vivant, base de pédologie, biologie des sols, 1st edn. Collection gérer l’environnement. Presses Polytechniques et Universitaires Romandes, LausanneGoogle Scholar
  33. Goering HK, Van Soest PJ (eds) (1970) Forage fibre analysis (apparatus, reagents, procedures and some applications). In: Agricultural handbook no 379. USDA, Washington, DC, pp 1–19Google Scholar
  34. Hopkin SP (1997) Biology of the springtails (Insecta: collembola). Oxford University Press, Inc., New YorkGoogle Scholar
  35. Joffre R, Gillon D, Dardenne P, Agneessens R, Biston R (1992) The use of near-infrared reflectance spectroscopy in litter decomposition studies. Ann Sci For 49:481–488CrossRefGoogle Scholar
  36. Kloster MB (1974) Determination of tannin and lignin. J Am Water Works Assoc 66:44–51Google Scholar
  37. Koehler H (1999) Predatory mites. Agric Ecosyst Environ 74:395–410CrossRefGoogle Scholar
  38. Korthals GW, Alexiev AD, Lexmond TM, Kammenga JE, Bongers T (1996a) Long-term effects of copper and pH on the nematode community in an agroecosystem. Environ Toxicol Chem 15:979–985CrossRefGoogle Scholar
  39. Korthals GW, van de Ende A, van Megen H, Lexmond TM, Kammenga JE, 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 4:107–117CrossRefGoogle Scholar
  40. Kurcheva GF (1960) Role of invertebrates in the decomposition of oak litter. Pochvovedenie 4:16–23Google Scholar
  41. Leonard AW, Hyne RV, Lim RP, Pablo F, Van den Brink PJ (2000) Riverine endosulfan concentrations in the Namoi river, Australia: link to cotton field runoff and macroinvertebrate population densities. Environ Toxicol Chem 19:1540–1551CrossRefGoogle Scholar
  42. Lübben B (1989) Influence of sewage sludge and heavy metals on the abundance of collembola on two agricultural soils. In: Dallai R (ed) Third International Seminar on Apterygota, University of Sienna, Sienna, pp 419–428Google Scholar
  43. Mitchell MJ, Hartenstein R, Swift BL, Neuhauser EF, Abrams BI, Mulligan RM, Brown BA, Craig D, Kaplan D (1978) Effects of different sewage sludges on some chemical and biological characteristics of soil. J Environ Qual 7:5591–5598Google Scholar
  44. O’Connor FB (1962) The extraction of Enchytraeidae from soil. In: Murphy PW (ed) Soil zoology. Butterworths, London, pp 279–285Google Scholar
  45. Parmelee RW, Wentsel RS, Philipps CT, Simini M, Checkai RT (1993) Soil microcosm for testing the effects of chemical pollutants on soil fauna communities and trophic structure. Environ Toxicol Chem 12:1477–1486CrossRefGoogle Scholar
  46. Parmelee RW, Philipps CT, Checkai RT, Bohlen PJ (1997) Determining the effects of pollutants on soil fauna communities and trophic structure using a refined microcosm system. Environ Toxicol Chem 16:1212–1217CrossRefGoogle Scholar
  47. Pimentel D, Warneke A (1989) Ecological effects of manure, sewage sludge and other organic wastes on arthropod populations. Agric Zool Rev 3:1–30Google Scholar
  48. Posthuma L, Baerselman R, Van Veen RPM, Dirven-Van Breemen EM (1997) Single and joint toxic effects of copper and zinc on reproduction of Enchytraeus crypticus in relation to sorption of metals in soils. Ecotoxicol Environ Saf 38:108–121CrossRefPubMedGoogle Scholar
  49. Potapow M (ed) (2001) Synopses on paleoarctic collembola. Isotomidae. Staatliches Museum für Naturkunde Görlitz, GörlitzGoogle Scholar
  50. Salminen J, Haimi J (1999) Horizontal distribution of copper, nickel and enchytraeid worms in polluted soil. Environ Pollut 104:351–358CrossRefGoogle Scholar
  51. Sandifer RD, Hopkin SP (1997) Effects of temperature on the relative toxicities of Cd, Cu, Pb, and Zn to Folsomia candida (collembola). Ecotoxicol Environ Saf 37:125–130CrossRefPubMedGoogle Scholar
  52. Scott-Fordsmand JJ, Krogh PH, Weeks JM (1997) Sublethal toxicity of copper to a soil-dwelling springtail (Folsomia fimetaria). Environ Toxicol Chem 16:2538–2542CrossRefGoogle Scholar
  53. Scott-Fordsmand JJ, Krogh PH, Weeks JM (2000) Responses of Folsomia Fimetaria (Collembola: Isotomidae) to copper under different soil copper contamination histories in relation to risk assessment. Environ Toxicol Chem 19:1297–1303CrossRefGoogle Scholar
  54. Seastedt TR (1984) The role of microarthropods in decomposition and mineralization processes. Annu Rev Entomol 29:25–46CrossRefGoogle Scholar
  55. Shenk JS, Westerhaus MO (1991) ISI-NIRS-2. Software for near-infrared instruments. Infrasoft International, Port Matilda, PAGoogle Scholar
  56. Statsoft (1998) Statistica for Windows, 5.1. Tulsa, OK, USAGoogle Scholar
  57. Streit B (1984) Effects of high copper concentrations on soil invertebrates (earthworms and oribatid mites): experimental results and a model. Oecologia 64:381–388CrossRefGoogle Scholar
  58. Ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination. Microcomputer Power, 4.5, Ithaca, NYGoogle Scholar
  59. Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate metals. Anal Chem 51:844–851CrossRefGoogle Scholar
  60. Van Amelsvoort PAM, Dongen M, Werff A (1988) The impact of collembola on humification and mineralization of soil organic matter. Pedobiologia 31:103–111Google Scholar
  61. Van den Brink PJ (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18:138–148CrossRefGoogle Scholar
  62. Van den Brink PJ, Ter Braak CJF (1998) Multivariate analysis of stress in experimental ecosystems by Principal Response Curves and similarity analysis. Aquat Ecol 32:163–178CrossRefGoogle Scholar
  63. Van den Brink PJ, Hattink J, Bransen F, Van Donk E, Brock TCM (2000) Impact of the fungicide carbendazim in freshwater microcosms. II. Zooplancton, primary producers and final conclusions. Aquat Toxicol 48:251–264CrossRefPubMedGoogle Scholar
  64. Van Wesemael B (1993) Litter decomposition and nutrient distribution in humus profiles in some Mediterranean forests in southern Tuscany. For Ecol Manag 57:99–114CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Céline Pernin
    • 1
  • Jean-Paul Ambrosi
    • 3
  • Jérôme Cortet
    • 4
  • Richard Joffre
    • 5
  • Jean Le Petit
    • 1
  • Elisabeth Tabone
    • 6
  • Franck Torre
    • 1
  • Paul Henning Krogh
    • 2
  1. 1.Institut Mediterraneen d’Ecologie et de Paleoecologie, Faculte des Sciences de St JeromeMarseille Cedex 20France
  2. 2.Department of Terrestrial EcologyNational Environmental Research InstituteSilkeborgDenmark
  3. 3.IRD-CEREGE UMR 161 et CNRS UMR 6635, Centre IRDNouméa cedexNew Caledonia
  4. 4.Institut National Polytechnique de Lorraine (ENSAIA)Vandoeuvre-lès-nancyFrance
  5. 5.Centre d’Ecologie Fonctionnelle et Evolutive CNRSMontpellier cedex 05France
  6. 6.INRA-centre de recherches d’Antibes, Entomologie et lutte biologiqueValbonneFrance

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