Skip to main content
SpringerLink
Log in

Effects of nonylphenol on a soil community using microcosms

  • SOILS, SEC 4 • ECOTOXICOLOGY • RESEARCH ARTICLE
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Nonylphenol polyethoxylates (NPEOs) are a group of surfactants known to be toxic and able to mimic estrogen compounds and thus interfere with the action of an animal’s endogenous hormones. NPEOs are easily biodegraded in the environment, but the last end product, nonylphenol (NP), is the most toxic and recalcitrant form and hence can have a longer half-life in the environment. Despite the fact that most NP is finally degraded, a small fraction may remain in soil for longer periods. In soils, the application of sewage sludge is the main source of NPEOs. The aim of this study is to provide data on the effects of NP on a simplified soil invertebrate community since only a few studies using single-species bioassays are available for terrestrial ecosystems in comparison with aquatic ecosystems.

Materials and methods

In our study, we assessed the effect of increasing NP concentrations (0, 10, 30, 90, and 270 mg NP kg–1) in soil microcosms containing a simplified soil community consisting of natural microorganisms, a primary producer (an oat seedling of Avena sativa), several consumers (the isopod Porcellionides sexfasciatus, the enchytraeid Enchytraeus crypticus, and the collembolans Folsomia candida, Ceratophysella (Hypogastrura) denticulata, and Proisotoma minuta), and a predator species (the mite Hypoaspis aculeifer). The effects on the different taxa of the different NP concentrations were assessed over three sampling dates (28, 56, and 112 days) using the principal response curves method.

Results and discussion

The soil community did not change significantly at concentrations below 90 mg NP kg–1, which was selected as the nonobserved effect concentration (NOEC). The highest concentration (270 mg NP kg–1) changed the community significantly after 28 and 56 days, but this effect disappeared after 112 days, in accordance with the known rapid biodegradation of this compound in soil.

Conclusions

Taking into account the usual NP concentrations in soils with repeated applications of sludge, the environmental risk of NP to soils seems to be limited because the derived NOEC was clearly above the usual concentrations in soil reported in the literature. However, the use of highly polluted sludges or accidental spillages, together with the possible pollution exportation by runoff to aquatic ecosystems, which are highly sensitive to NP pollution, recommend the careful monitoring of this chemical in the environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahel M, Scully FE, Hoigné J, Giger W (1994a) Photochemical degradation of nonylphenol and nonylphenol polyethoxylates in natural waters. Chemosphere 28:1361–1368

    Article  CAS  Google Scholar 

  • Ahel M, Giger W, Koch M (1994b) Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment: I. Occurrence and transformation in sewage treatment. Water Res 28:1131–1142

    Article  CAS  Google Scholar 

  • Ahel M, Giger W, Koch M (1994c) Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment: II. Occurrence and transformation in rivers. Water Res 28:1143–1152

    Article  CAS  Google Scholar 

  • Baatrup E, Bayley M, Axelsen JA (2006) Predation of the mite Hypoaspis aculeifer on the springtail Folsomia fimetaria and the influence of sex, size, starvation, and poisoning. Entomol Exp Appl 118:61–70

    Article  Google Scholar 

  • Berndt O, Meyhöffer Hans-Michael P (2003) Propensity towards cannibalism among Hypoaspis aculeifer and H. miles, two soil-dwelling predatory mite species. Exp Appl Acarol 31:1–14

    Article  Google Scholar 

  • Beyers RJ, Odum HT (1993) Ecological microcosms. Springer, New York

    Google Scholar 

  • Brun LA, Maillet J, Hinsinger P, Pépin M (2001) Evaluation of copper availability to plants in copper-contaminated vineyard soils. Environ Pollut 111:293–302

    Article  CAS  Google Scholar 

  • Burrows LA, Edwards CA (2002) The use of integrated soil microcosms to predict effects of pesticides on soil ecosystems. Eur J Soil Biol 38:245–249

    Article  CAS  Google Scholar 

  • Campbell P (2002) Alternatives to nonylphenol ethoxylates. Review of toxicity, biodegradation and technical-economic aspects. ToxEcology Environmental Consulting, Vancouver, B.C. Canada. Report for Environment Canada

  • Carpenter SR (1996) Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77:677–680

    Article  Google Scholar 

  • 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 37:302–312

    Google Scholar 

  • Croce V, De Angelis S, Patrolecco L, Polesello S, Valsechi S (2005) Uptake and accumulation of sediment-associated 4-nonylphenol in a benthic invertebrate (Lumbricus variegatus, freshwater oligochaete). Environ Toxicol Chem 24:1165–1171

    Article  CAS  Google Scholar 

  • de Jager C, Ms B, Wandrag S, Sharp VW (1999) The effect of p-nonylphenol, an environmental toxicant with oestrogenic properties, on fertility potential in adult male rats. Andrologia 31:99–106

    Article  Google Scholar 

  • Dettenmaier E, Doucette WJ (2007) Mineralization and plant uptake of 14C-labeled nonylphenol, nonylphenol tetraethoxylate and nonylphenol nonylethoxylate in biosolids/soil systems planted with crested wheatgrass. Environ Toxicol Chem 26:193–200

    Article  CAS  Google Scholar 

  • Domene X, Ramírez W, Solà L, Alcañiz JM, Andrés P (2009) Soil pollution by nonylphenol and nonylphenol ethoxylates and their effects to plants and invertebrates. J Soils Sediments 9(6):555–569

    Article  CAS  Google Scholar 

  • Drake JA, Huxel GR, Hewitt CJ (1996) Microcosms as models for generating and testing community theory. Ecology 77:670–677

    Article  Google Scholar 

  • Edwards CA (2002) Assessing the effects of environmental pollutants on soil organisms, communities, processes and ecosystems. Eur J Soil Biol 38:225–231

    Article  CAS  Google Scholar 

  • European Parliament, Council of the European Union (2009) Directive 2003/53/EC of the European Parliament and the Council of 18 June 2003 amending for the 26th time Council Directive 76/769/EEC relating to restrictions on the marketing and use of certain dangerous substances and preparations (nonylphenol, nonylphenol ethoxylate and cement). Official Journal of the European Union 17.7.2003. L 178/24

  • Ferguson SA, Flynn KM, Delclos KB, Newbold RR (2000) Maternal and offspring toxicity but few sexually dimorphic behavioural alterations result from nonylphenol exposure. Neurotoxicol Teratol 15:281–292

    Google Scholar 

  • Fraser LH, Keddy P (1997) The role of experimental microcosms in ecological research. Trends Ecol Evol 12:478–481

    Article  Google Scholar 

  • Fries E, Puttmann W (2004) Occurrence of 4-nonylphenol in rain and snow. Atmos Environ 38:2013–2006

    Article  CAS  Google Scholar 

  • Gabriel FLP, Routledge EJ, Heidlberger A, Rentsch D, Guenther K, Giger W, Sumpter JP, Kohler H-PE (2008) Isomer-specific degradation and endocrine disrupting activity of nonylphenols. Environ Sci Technol 42:6399–6408

    Article  CAS  Google Scholar 

  • Gejlsbjerg B, Klinge C, Samsøe-Petersen L, Madsen T (2001) Toxicity of linear alkyl benzene sulfonates and nonylphenol in sludge-amended soil. Environ Toxicol Chem 20:2709–2716

    Article  CAS  Google Scholar 

  • Greenslade P, Vaughan GT (2003) A comparison of Collembola species for toxicity testing of Australian soils. Pedobiologia 47:171–179

    Article  CAS  Google Scholar 

  • Hamers T, Krogh PH (1997) Predator–prey relationship in a two-species toxicity test system. Ecotoxicol Environ Saf 37:230–212

    Article  Google Scholar 

  • Heckmann L-H, Ruf A, Nienstedt KM, Krogh PH (2007) Reproductive performance of the generalist predator Hypoaspis aculeifer (Acari: Gamasida) when foraging on different invertebrate preys. Appl Soil Ecol 36:130–135

    Article  Google Scholar 

  • Hedlund K, Sjögren-Öhrn M (2000) Tritrophic interactions in a soil community enhance decomposition rates. Oikos 88:585–591

    Article  Google Scholar 

  • Hood TE, Calabrese EJ, Zuckerman BM (2000) Detection of an estrogen receptor in two nematode species and inhibition of binding and development by environmental chemicals. Ecotoxicol Environ Saf 47:74–81

    Article  CAS  Google Scholar 

  • Jacobsen AM, Mortensen GK, Hansen HCB (2004) Degradation and mobility of linear alkyl benzene sulfonate and nonylphenol in sludge-amended soil. J Environ Qual 33:232–240

    CAS  Google Scholar 

  • Jänsch S, Frampton GK, Römbke J, Van Den Brink PJ, Scott-Fordsmand JJ (2006) Effects of pesticides on soil invertebrates: a review and comparison with laboratory toxicity data. Environ Toxicol Chem 25:2490–2501

    Article  Google Scholar 

  • Janssen MPM, Traas TP, Rila J-P, van Vlaardingen PLA (2004) Guidance for deriving Dutch Environmental Risk Limits from EU-Risk Assessment Reports of existing substances. RIVM report 601501020/2004. http://www.rivm.nl/bibliotheek/rapporten/601501020.pdf. Accessed 28 Sept 1999

  • Kampichler C, Bruckner A, Kandeler E (2001) Use of enclosed model ecosystems in soil ecology: a bias towards laboratory research. Soil Biol Biochem 33:269–275

    Article  CAS  Google Scholar 

  • Larsen T, Luxhøi J, Magid J, Jensen LS, Krogh PH (2007) Properties of anaerobically digested and composted municipal solid waste assessed by linking soil mesofauna dynamics and nitrogen modelling. Biol Fertil Soils 44:59–68

    Article  Google Scholar 

  • Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge

    Google Scholar 

  • Liiri M, Setälä H, Haimi J, Fritze H (2002) Relationship between soil microarthropod species diversity and plant growth does not change when the system is disturbed. Oikos 96:137–149

    Article  Google Scholar 

  • Lock K, Janssen CR (2003) Influence of aging on copper bioavailability in soils. Environ Toxicol Chem 22:1162–1166

    CAS  Google Scholar 

  • Luckinbill LS (1979) Regulation, stability, and diversity in a model experimental microcosm. Ecology 60:1098–1102

    Article  Google Scholar 

  • Lussier SM, Champlin D, LiVolsi J, Pucher S, Pruell RJ (2000) Acute toxicity of para-nonylphenol to saltwater animals. Environ Toxicol Chem 19:617–621

    CAS  Google Scholar 

  • Mortensen GK, Kure LK (2003) Degradation and plant uptake of nonylphenol in spiked soils and in soils treated with organic waste products. Environ Toxicol Chem 22:718–721

    Article  CAS  Google Scholar 

  • Moser T, Römbke J, Schallnass H-J, Van Gestel CAM (2007) The use of the multivariate principal response curve (PRC) for community level analysis: a case study on the effects of carbendazim on enchytraeids in terrestrial model ecosystems (TME). Ecotoxicology 16:573–583

    Article  CAS  Google Scholar 

  • Nowak KM, Kouloumbos VN, Schäffer A, Corvini PF-X (2008) Effect of sludge treatment on the bioaccumulation of nonylphenol in grass grown on sludge-amended soil. Environ Chem Lett 6:53–58

    Article  CAS  Google Scholar 

  • Patureau D, Laforie M, Lichtfouse E, Caria G, Denaix L, Schmidt JE (2007) Fate of organic pollutants after sewage sludge spreading on agricultural soils: a 30-years field-scale recording. Water Pract Technol. doi:10.2166/WPT.2007008

  • 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 49:54–59

    Article  CAS  Google Scholar 

  • Pedersen MB, Van Gestel CAM, Elmegaard N (2000) Effects of copper on the reproduction of two collembolan species exposed through soil, food and water. Environ Toxicol Chem 19:2579–258

    Article  CAS  Google Scholar 

  • Pernin C, Ambrosi J-P, Cortet J, Joffre R, Le Petit J, Tabone E, Torre F, Korgh PH (2006) Effects of sewage sludge and copper enrichment on both soil mesofauna community and decomposition of oak leaves (Quercus suber) in a mesocosm. Bio Fertil Soils 43:39–50

    Article  Google Scholar 

  • Peters RJB, Beeltje H, van Delft RJ (2008) Xeno-estrogenic compounds in precipitation. J Environ Qual 10:760–769

    CAS  Google Scholar 

  • Petersen SO, Henriksen K, Mortensen GK, Krogh PH, Brandt KK, Sørensen J, Madsen T, Petersen J, Grøn C (2003) Recycling of sewage sludge and household compost to arable land: fate and effects of organic contaminants, and impact on soil fertility. Soil Tillage Res 72:139–152

    Article  Google Scholar 

  • Preuss TG, Gehrhardt J, Schirmer K, Coors A, Rubach M, Russ A, Jones PD, Giesy JP, Ratte HT (2006) Nonylphenol isomers differ in estrogenic activity. Environ Sci Technol 40:5147–5153

    Article  CAS  Google Scholar 

  • Preuss TG, Telscher M, Ratte HT (2008) Life stage-dependent bioconcentration of a nonylphenol isomer in Daphnia magna. Environ Pollut 156:1211–1217

    Article  CAS  Google Scholar 

  • Quinn B, Ggné F, Blaise C, Castello MJ, Wilson JG, Mothersill C (2006) Evaluation of the lethal and sub-lethal toxicity and potential endocrine disrupting effect of nonylphenol on the zebra mussel (Dreissena polymorpha). Comp Biochem Physiol Part C: Toxicol Pharmacol 142:118–127

    Article  CAS  Google Scholar 

  • Roberts P, Roberts JP, Jones DL (2006) Behaviour of the endocrine disrupting chemical nonylphenol in soil: assessing the risk associated with spreading contaminated waste to land. Soil Biol Biochem 38:1812–1822

    Article  CAS  Google Scholar 

  • Salminen JE, Sulkava PO (1997) Decomposer communities in contaminated soil: is altered community regulation a proper tool in ecological risk assessment of toxicants? Environ Pollut 97:45–53

    Article  CAS  Google Scholar 

  • Scott-Fordsmand JJ, Krogh PH (2004) The influence of application form on the toxicity of nonylphenol to Folsomia fimetaria (Collembola: Isotomidae). Ecotoxicol Environ Saf 58:294–299

    Article  CAS  Google Scholar 

  • 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 19:1297–1303

    CAS  Google Scholar 

  • Scott-Fordsmand JJ, Maraldo K, Van den Brink PJ (2008) The toxicity of copper contaminated soil using a gnotobiotic Soil Multi-species Test System (SMS). Environ Int 34:524–530

    Article  CAS  Google Scholar 

  • Sjöström ǺE, Collins CD, Smith SR, Shaw G (2008) Degradation and plant uptake of nonylphenol (NP) and nonylphenol-12-ethoxylate (NP12EO) in four contrasting agricultural soils. Environ Pollut 156:1284–1289

    Article  CAS  Google Scholar 

  • Soares A, Guieysse B, Jefferson B, Cartmell E, Lester JN (2008) Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ Int 34:1033–1049

    Article  CAS  Google Scholar 

  • Staples CA, Naylor CG, Williams JB (2001) Ultimate biodegradation of alkylphenol ethoxylate surfactants and their biodegradation intermediates. Environ Toxicol Chem 20:2450–2455

    Article  CAS  Google Scholar 

  • Staples C, Mihaich E, Carbone J, Woodburn K, Klecka G (2004) A weight of evidence analysis of the chronic ecotoxicity of nonylphenol ethoxylates, nonylphenol ether carboxylates, and nonylphenol. Hum Ecol Risk Assess 10:999–1017

    Article  CAS  Google Scholar 

  • Topp E, Starratt A (2000) Rapid mineralization of the endocrine-disrupting chemical 4-nonylphenol in soil. Environ Toxicol Chem 19:313–318

    CAS  Google Scholar 

  • Usher MB, Davis PR (1983) The biology of Hypoaspis aculeifer (Canestrini) (Mesostigmata): is there a tendency towards social behaviour? Acarologia 24:243–250

    Google Scholar 

  • Van den Brink PJ, Ter Braak CJF (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18:138–148

    Article  Google Scholar 

  • Van den Brink PJ, Van den Brink N, Ter Braak CJF (2003) Multivariate analysis of ecotoxicological data using ordination: demonstrations of utility on the basis of various examples. Australas J Ecotoxicol 9:141–156

    Google Scholar 

  • Verhoef HA (1996) The role of soil microcosms in the study of ecosystem processes. Ecology 77:685–690

    Article  Google Scholar 

  • Vilkesøe J, Thomsen M, Carlsen L (2002) Phtalates and nonylphenols in profiles of differently dressed soils. Sci Total Environ 296:105–116

    Article  Google Scholar 

  • Widarto TH, Krogh PH, Forbes VE (2004) Nonylphenol stimulates fecundity but not population growth rate (λ) of Folsomia candida. Ecotoxicol Environ Saf 67:369–377

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study has been supported by a postdoctoral fellowship held by the corresponding author (Programa José Castillejo, JC2007-00099) and the TOXIFENOL project (CTM2006-14163-C02-01/TECNO), both funded by the Spanish Ministry of Education and Science. We would also like to thank Tiago Natal-da-Luz and Dalila Costa for their help in conducting the experimental work and Eduardo Mateos for collembolan species identification.

Author information

Authors and Affiliations

  1. Center for Ecological Research and Forestry Applications (CREAF), Facultat de Biociències, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, 08193, Barcelona, Spain

    Xavier Domene & Xavier Domene

  2. IMAR-CMA, Department of Life Sciences, University of Coimbra, 3004-517, Coimbra, Portugal

    Xavier Domene, Sónia Chelinho & José Paulo Sousa

Authors
  1. Xavier Domene
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sónia Chelinho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Paulo Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xavier Domene.

Additional information

Responsible editor: Jörg Römbke

Rights and permissions

Reprints and permissions

About this article

Cite this article

Domene, X., Chelinho, S. & Sousa, J.P. Effects of nonylphenol on a soil community using microcosms. J Soils Sediments 10, 556–567 (2010). https://doi.org/10.1007/s11368-009-0167-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-009-0167-9

Keywords

Search

Navigation