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Soil pollution by nonylphenol and nonylphenol ethoxylates and their effects to plants and invertebrates

  • Xavier DomeneEmail author
  • Wilson Ramírez
  • Laura Solà
  • Josep M. Alcañiz
  • Pilar Andrés
SOILS, SEC 4 * ECOTOXICOLOGY * RESEARCH ARTICLE

Abstract

Background, aim, and scope

Nonylphenol polyethoxylates (NPEOs) are a widely used class of nonionic surfactants known to be toxic and endocrine-disrupting contaminants. Their use and production have been banned in the European Union and substituted by other surfactants considered as environmentally safer. However, their use continues in many countries without any legal control. Discharges of effluents from wastewater treatment plants and the application of sewage sludge application, landfilling, and accidental spillage to soils are the major sources of NPEOs in the environment. The biodegradation of these surfactants is relatively easy, leading to the accumulation of the simplest chemical forms of nonylphenol ethoxylates (NP, NP1EO, and NP2EO) and nonylphenol carboxy acids (NP2EC or NP1EC). However, these are also the most toxic end-products and have a higher environmental persistence. Compared to aquatic ecosystems, not much is known about the effects of NPEOs in terrestrial organisms, with few studies mainly centered on the effects on plants and soil microorganisms. The main aim of this study is to provide the range of concentrations of NPEOs with ecotoxicological effects on different plants and soil invertebrate species. In addition, we aim to identify the main soil properties influencing their toxicity.

Materials and methods

Two natural soils collected and OECD artificial soil were used in toxicity bioassays. Two different NPEO formulations were tested. On the one hand, a technical mixture of NPEOs containing chain isomers and oligomers with an average of eight ethoxy units was used for the experiments and is referred to herein as NP8EO. On the other hand, technical-grade 4-nonylphenol 95% purity was also used and called NP in this study. The chemicals were applied and mixed with soil as an acetone solution. The toxicity of NP8EO and NP was assessed in different taxonomical groups (plants, earthworms, enchytraeids, and collembolans) according to their respective standardized methods. The effect on lethal and sublethal endpoints was assessed and, by means of linear and non-linear regression models, the NPEO concentration causing 10% and 50% inhibition was estimated. The influence of soil properties on the toxicity was assessed using generalized linear models (GLM).

Results

The chemicals tested showed contrasting toxicities, NP being clearly more toxic than NP8EO. There were also substantial differences in the sensitivity of the species and endpoints, together with clearly different toxicities in different soils. Plants were the least affected group compared to soil invertebrates, since plant endpoints were unaffected or only slightly inhibited. In soil invertebrates, reproduction was the most affected endpoint compared to growth or survival. Toxicity was the lowest in OECD artificial soil in comparison to natural soils, with a lower organic matter content.

Discussion

The higher toxicity of NP, both in plant and soil invertebrate bioassays, is consistent with previously published studies and its relatively high persistence in soil. The low phytotoxicity of NP8EO and NP, unaffected at concentrations over 1 g NP kg−1, also accords with the known low uptake in plants. The effects on soil invertebrates appeared at lower concentrations than observed in plants, enchytraeids being less affected by NP8EO than earthworms and collembolans. Drastic inhibition in the invertebrate’s endpoints generally appeared over 1 g kg−1 for NP8EO and below 1 g kg−1 for NP. The range of concentrations with effects is in agreement with the few similar studies published to date. Generally, the lowest toxicity values were obtained in OECD soil, with the highest organic matter content, while the highest toxicity was found in the PRA soil, with the lowest content. However, few of the models developed by GLM identified organic carbon as a significant factor in decreasing the bioavailability and toxicity of NPEO. The probable explanation for this is the simultaneous contribution of other soil properties and in particular the limited number of soils used in the bioassays.

Conclusions

A low ecotoxicological risk of NPEOs might be expected for plants and soil invertebrates, since the usual concentrations in soils (below 2.6 mg kg−1) are clearly less than the lowest concentrations reported to be toxic in our study.

Recommendations and perspectives

Although the apparent risk of NPEOs for soil ecosystems is limited, such risks should not be neglected since significant concentrations in soil could be reached with elevated application rates or when highly polluted sludges are used. More importantly, NPEO concentrations in soils should be maintained low given the extremely high toxicity for aquatic organisms. Despite the reduced leaching of NPEOs, runoff events might transport NP attached to soil particles and affect adjacent aquatic ecosystems.

Keywords

Collembolans Earthworms Enchytraeids Nonylphenol ethoxylates Plants Soil toxicity 

Notes

Acknowledgments

This study has been supported by the TOXIFENOL project (CTM2006-14163-C02-01/TECNO), funded by the Spanish Ministry of Education and Science (MEC).

References

  1. Ahel M, Scully FE, Hoigné J, Giger W (1994a) Photochemical degradation of nonylphenol and nonylphenol polyethoxylates in natural waters. Chemosphere 28:1361–1368CrossRefGoogle Scholar
  2. 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 28:1131–1142CrossRefGoogle Scholar
  3. Ahel M, Giger W, Koch M (1994c) Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment: II. Occurrence and transformation in rivers. Water Res 28:1143–1152CrossRefGoogle Scholar
  4. Brix R, Hvidt S, Carlsen L (2001) Solubility of nonylphenol and nonylphenol ethoxylates. On the possible role of micelles. Chemosphere 44:759–763CrossRefGoogle Scholar
  5. Burgess RM, Pelletier MC, Gundersen JL, Perron MM, Ryba SA (2005) Effects of different forms of organic carbon on the partitioning and bioavailability of nonylphenol. Environ Toxic Chem 24:1609–1617CrossRefGoogle Scholar
  6. Campbell P (2002) Alternatives to nonylphenol ethoxylates. Review of toxicity, biodegradation and technical-economic aspects. ToxEcology Report for Environment Canada. Environmental Consulting, VancouverGoogle Scholar
  7. Chapman HD (1965) Cation-exchange capacity. In: Black CA (ed) Methods of soil analysis, Part 1. Chemical and microbiological properties. American Society of Agronomy, Madison, pp 891–901Google Scholar
  8. Collins CD, Fryer M, Grosso A (2006) Plant uptake of non-ionic organic chemicals. Environ Sci Technol 40:45–52CrossRefGoogle Scholar
  9. Corvini PFX, Schaffer A, Schlosser D (2006) Microbial degradation of nonylphenol and other alkylphenols: our evolving view. Appl Microbiol Biotechnol 72:223–243CrossRefGoogle Scholar
  10. Das KC, Xia K (2008) Transformation of 4-nonylphenol isomers during biosolids composting. Chemosphere 70:761–768CrossRefGoogle Scholar
  11. 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, Brussels, Belgium, L 178, pp 24–27Google Scholar
  12. Domene X, Alcañiz JM, Andrés P (2007) Ecotoxicological assessment of organic wastes using the soil collembolan Folsomia candida. Appl Soil Ecol 35:461–472CrossRefGoogle Scholar
  13. 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 26:193–200CrossRefGoogle Scholar
  14. Fries E, Puttmann W (2004) Occurrence of 4-nonylphenol in rain and snow. Atmos Environ 38:2013–2006CrossRefGoogle Scholar
  15. Gejlsbjerg B, Klinge C, Samsøe-Petersen L, Madsen T (2001) Toxicity of linear alkylbenzene sulfonates and nonylphenol in sludge-amended soil. Environ Toxicol Chem 20:2709–2716CrossRefGoogle Scholar
  16. Gejlsbjerg B, Madsen T, Andersen TT (2003) Comparison of biodegradation of surfactants in soils and sludge–soil mixtures by use of 14C-labelled compounds and automated respirometry. Chemosphere 50:321–331CrossRefGoogle Scholar
  17. Harms HH (1992) In-vitro systems for studying phytotoxicity and metabolic fate of pesticides and xenobiotics in plants. Pestic Sci 35:277–281CrossRefGoogle Scholar
  18. Hernandez-Raquet G, Soef A, Delgenès N, Balaguer O (2007) Removal of the endocrine disrupter nonylphenol and its estrogenic activity in sludge treatment processes. Water Res 41:2643–2651CrossRefGoogle Scholar
  19. ISO (1996) Water quality—determination of 33 elements by inductively coupled plasma atomic emission spectroscopy. Guideline no. 11885. International Organization for Standardization, Geneva, pp 1–22Google Scholar
  20. ISO (1998) Soil quality—effects of pollutants on earthworms. Part 2: Determination of effects on reproduction. Guideline no. 11268-2. International Organization for Standardization, Geneva, pp 1–38Google Scholar
  21. ISO (1999) Soil quality—inhibition of reproduction of Collembola (Folsomia candida) by soil pollutants. Guideline no. 11267. International Organization for Standardization, Geneva, pp 1–16Google Scholar
  22. ISO (2003) Soil quality—effects of pollutants on Enchytraeidae (Enchytraeus sp.)—determination of effects on survival and reproduction. Guideline no. 16387. International Organization for Standardization, Geneva, pp 1–22Google Scholar
  23. Jacobsen AM, Mortensen GK, Hansen HCB (2004) Degradation and mobility of linear alkylbenzene sulfonate and nonylphenol in sludge-amended soil. J Environ Qual 33:232–240Google Scholar
  24. Jänsch S, Amorim M, Römbke J (2005) Identification of the ecological requirements of important terrestrial ecotoxicological test species. Environ Rev 13:51–83CrossRefGoogle Scholar
  25. Jensen D, Bayley M, Holmstrup M (2009) Synergistic interaction between 4-nonylphenol and high but not low temperatures in Dendrobaena octaedra. Ecotoxicol Environ Safety 72:10–16CrossRefGoogle Scholar
  26. John DM, White GF (1998) Mechanism for biotransformation of nonylphenol polyethoxylates to xenoestrogens in Pseudomonas putida. J Bacteriol 180:4332–4338Google Scholar
  27. Kelsey JW, Kottler BD, Alexander M (1997) Selective chemical extractants to predict bioavailability of soil-aged organic chemicals. Environ Sci Technol 31:214–217CrossRefGoogle Scholar
  28. Kirchmann H, Tengsved A (1991) Organic pollutants in sewage sludge. 2. Analysis of barley grains grown on sludge-fertilized soil. Swedish J Agric Res 21:115–119Google Scholar
  29. Krogh PH, Holmstrup M, Jensen J, Petersen SO (1996) Økologisk vurdering af spildevandsslam i landbrugsjord [Ecological assessment of sewage sludge on farm land]. Arbejdsrapport Nr. 43. Miljø- og Energiministeriet, Miljøstyrelsen [Danish EPA]Google Scholar
  30. Kuperman RG, Checkai RT, Simini M, Phillips CT, Anthony JS, Kolakowski JE, Davis EA (2006) Toxicity of emerging energetic soil contaminant CL-20 to potworm Enchytraeus crypticus in freshly amended or weathered and aged treatments. Chemosphere 62:1282–1293CrossRefGoogle Scholar
  31. Langford KH, Lester JN (2002) Fate and behaviour of endocrine disrupters in wastewater treatment processes. In: Birkett JW, Lester JN (eds) Endocrine disrupters in wastewater and sludge treatment processes. CRC, Boca Raton, pp 103–144Google Scholar
  32. Lock K, Janssen CR (2003) Influence of aging on copper bioavailability in soils. Environ Toxicol Chem 22:1162–1166CrossRefGoogle Scholar
  33. Madsen T, Winther-Nielsen M, Samsøe-Petersen L (1998) Effects of organic chemicals in sludge applied to soil: degradation and toxicity to organisms living in soil. Danish Environmental Protection Agency, Ministry of Environment and Energy, København, DenmarkGoogle Scholar
  34. 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 22:718–721CrossRefGoogle Scholar
  35. Ney RE (1990) Where did that chemical go: a practical guide to chemical fate and transport in the environment. Van Nostrand Reinhold, New YorkGoogle Scholar
  36. 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 6:53–58CrossRefGoogle Scholar
  37. OECD (1984) OECD Guidelines for the Testing of Chemicals/Section 2: Effects on Biotic Systems, Test No. 207: Earthworm, Acute Toxicity Tests. Guideline no. 207. Organization for Economic Co-operation and Development, Paris, pp 1–9Google Scholar
  38. OECD (2006) OECD Guidelines for the Testing of Chemicals/Section 2: Effects on Biotic Systems, Test No. 208: Terrestrial Plant Test: Seedling Emergence and Seedling Growth Test. Guideline no. 208. Organization for Economic Co-operation and Development, Paris, pp 1–17Google Scholar
  39. Oman C, Hynning PA (1993) Identification of organic-compounds in municipal landfill leachates. Environ Pollut 80:265–271CrossRefGoogle Scholar
  40. Pakou C, Kornaros M, Stamatelatou K, Lyberatos G (2009) On the fate of LAS, NPEOs and DEHP in municipal sewage sludge during composting. Biores Technol 100:1634–1642CrossRefGoogle Scholar
  41. Peters RJB, Beeltje H, van Delft RJ (2008) Xeno-estrogenic compounds in precipitation. J Environ Qual 10:760–769Google Scholar
  42. 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 72:139–152CrossRefGoogle Scholar
  43. Scott-Fordsmand JJ, Krogh PH (2004) The influence of application form on the toxicity of nonylphenol to Folsomia fimetaria (Collembola: Isotomidae). Ecotoxicol Environ Saf 58:294–299CrossRefGoogle Scholar
  44. Shang DY, Macdonald RW, Ikonomou MG (1999) Persistence of nonylphenol ethoxylate surfactants and their primary degradation products in sediments from near a municipal outfall in the strait of Georgia, British Columbia, Canada. Environ Sci Technol 33:1366–1372CrossRefGoogle Scholar
  45. Sjöström ǺE (2004) Uptake of nonylphenols by crops following agricultural use of sewage sludge. PhD thesis. Imperial College London, UKGoogle Scholar
  46. 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 Pollution 156:1284–1289CrossRefGoogle Scholar
  47. Smit CE, van Gestel CAM (1998) Effects of soil type, prepercolation, and ageing on bioaccumulation and toxicity of zinc for the springtail Folsomia candida. Environ Toxicol Chem 17:1132–1141CrossRefGoogle Scholar
  48. 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 34:1033–1049CrossRefGoogle Scholar
  49. Staples CA, Naylor CG, Williams JB (2001) Ultimate biodegradation of alkylphenol ethoxylate surfactants and their biodegradation intermediates. Environ Toxicol Chem 20:2450–2455CrossRefGoogle Scholar
  50. 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 10:999–1017CrossRefGoogle Scholar
  51. Topp E, Starratt A (2000) Rapid mineralization of the endocrine-disrupting chemical 4-nonylphenol in soil. Environ Toxicol Chem 19:313–318CrossRefGoogle Scholar
  52. Trocme M, Tarradellas J, Vedy JC (1988) Biotoxicity and persistence on nonylphenol during incubation in a compost–sandstone mixture. Biol Fert Soils 5:299–303CrossRefGoogle Scholar
  53. Vilkesøe J, Thomsen M, Carlsen L (2002) Phtalates and nonylphenols in profiles of differently dressed soils. Sci Total Environ 296:105–116CrossRefGoogle Scholar
  54. Vogel D, Gehring M, Tennhardt L, Weltin D, Bilitewski B (2003) Mobility and fate of endocrine disrupting compounds (EDCs) in soil after application of sewage sludge to agricultural land. In: Pullammanappallil Pr, McComb A, Diaz LF, Bidlingmaier W (eds) Proceedings of the 4th International Conference on Biological Processing of Organics: Advances for a Sustainable Society—ORBIT 2003, 30 April–2 May, Perth, Australia, vol 1, pp 241–250Google Scholar
  55. Widarto TH, Holmstrup M, Forbes VE (2004) The influence of nonylphenol on life-history of the earthworm Dendrobaena octaedra Savigny: linking effects from the individual- to the population-level. Ecotox Environ Saf 58:147–159CrossRefGoogle Scholar
  56. Widarto TH, Krogh PH, Forbes VE (2007) Nonylphenol stimulates fecundity but not population growth rate (λ) of Folsomia candida. Ecotox Environ Saf 67:369–377CrossRefGoogle Scholar
  57. Wild SR, Jones KC (1992) Organic chemicals entering agricultural soils in sewage sludges: screening for their potential to transfer to crop plants and livestock. Sci Total Environ 119:85–119CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Xavier Domene
    • 1
    Email author
  • Wilson Ramírez
    • 1
  • Laura Solà
    • 1
  • Josep M. Alcañiz
    • 1
  • Pilar Andrés
    • 1
  1. 1.Center for Ecological Research and Forestry Applications (CREAF), Facultat de BiociènciesUniversitat Autònoma de BarcelonaBarcelonaSpain

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