Abstract
Lanestosa is a chronically polluted site (derelict mine) where the soil (Lanestosa (LA) soil) exceeds screening values (SVs) of regulatory policies in force (Basque Country; Europe) for Zn, Pb and Cd. A scenario-targeted toxicity assessment was carried out on the basis of a multi-endpoint bioassay approach. Acute and chronic toxicity bioassays were conducted with selected test species (Vibrio fischeri, Dictyostelium discoideum, Lactuca sativa, Raphanus sativus and Eisenia fetida) in combination with chemical analysis of soils and elutriates and with bioaccumulation studies in earthworms. Besides, the toxicity profile was compared with that of the mine runoff (RO) soil and of a fresh artificially polluted soil (LAAPS) resembling LA soil pollutant profile. Extractability studies in LA soil revealed that Pb, Zn and Cd were highly available for exchange and/or release into the environment. Indeed, Pb and Zn were accumulated in earthworms and LA soil resulted to be toxic. Soil respiration, V. fischeri, vegetative and developmental cycles of D. discoideum and survival and juvenile production of E. fetida were severely affected. These results confirmed that LA soil had unacceptable environmental risk and demanded intervention. In contrast, although Pb and Zn concentrations in RO soil revealed also unacceptable risk, both metal extractability and toxicity were much lower than in LA soil. Thus, within the polluted site, the need for intervention varied between areas that posed dissimilar risk. Besides, since LAAPS, with a high exchangeable metal fraction, was the most toxic, ageing under in situ natural conditions seemingly contributed to attenuate LA soil risk. As a whole, combining multi-endpoint bioassays with scenario-targeted analysis (including leaching and ageing) provides reliable risk assessment in soils posing unacceptable environmental risk according to SVs, which is useful to optimise the required intervention measures.
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Achazi R (2002) Invertebrates in risk assessment development of a test battery and of short term biotests for ecological risk assessment of soil. J Soils Sediments 2:174–178
Alef K, Nannipieri P (1995) Estimation of microbial activities. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, London, pp 193–270
Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ Sci Technol 34:4259–4265
Alvarenga P, Palma P, Gonçalves A, Fernandes R, de Varennes A, Vallini G, Duarte E, Cunha-Queda A (2008) Evaluation of tests to assess the quality of mine-contaminated soils. Environ Geochem Health 30:95–99
Alvarez-Curto E (2007) Developmental regulation and evolution of cAMP signalling in Dictyostelium. PhD Dissertation, Fac Science, Leiden University
Asensio V, Rodríguez-Ruiz A, Garmendia L, Andre J, Kille P, Morgan AJ, Soto M, Marigómez I (2013) Towards an integrative soil health assessment strategy: a three tier (integrative biomarker response) approach with Eisenia fetida applied to soils subjected to chronic metal pollution. Sci Total Environ 442:344–365
Asensio V (2009) Health assessment of polluted soils after Eisenia foetida ex situ bioassays based on conventional and in vitro cellular biomarkers and microarray technology. PhD Dissertation, Univ Basque Country (UPV/EHU)
Azur Environmental (1995a) Microtox acute toxicity basic test procedures (basic SPT). Carlsbad, CA
Azur Environmental (1995b) Microtox acute toxicity solid-phase test procedures (solid-phase SPT). Carlsbad, CA
Balbo A, Bozzaro S (2008) A novel bioassay for evaluating soil bio-hazards using Dictyostelium as biosensor: validation and application to the Bio-Bio Project. Fresenius Environ Bull 17:1137–1143
Barrutia O, Garbisu C, Hernandez-Allica J, Garcia-Plazaola JI, Becerril JM (2010) Differences in EDTA-assisted metal phytoextraction between metallicolous and non-metallicolous accessions of Rumex acetosa L. Environ Pollut 158:1710–1715
Beeby A (1991) Toxic metal uptake and essential metal regulation in terrestrial invertebrates: a review. In: Newman MC, McIntosh AW (eds) Metal ecotoxicology: concepts and applications. Lewis, Chelsea, pp 65–89
Bierkens J, Klein G, Corbisier P, Van Den Heuvel R, Verschaeve L, Weltens R, Schoeters G (1998) Comparative sensitivity of 20 bioassays for soil quality. Chemosphere 37:2935–2947
Brown RB (2003) Soil texture. Univ Florida, IFAS Extension. Available: http://ufdc.ufl.edu/IR00003107/00001 (last access, 11/03/2014)
Carlon C (2007) Derivation methods of soil screening values in Europe. A review and evaluation of national procedures towards harmonisation. European Commission, Joint Research Centre, Ispra, EUR 22805 EN: 306
Chang LW, Meier JR, Smith MK (1997) Application of plant and earthworm bioassays to evaluate remediation of a lead-contaminated soil. Arch Environ Contam Toxicol 32:166–171
Conder JM, Lanno RP (2000) Evaluation of surrogate measures of cadmium, lead and zinc bioavailability to Eisenia fetida. Chemosphere 41:1659–1668
Cook SV, Chu A, Goodman RH (2002) Leachability and toxicity of hydrocarbons, metals and salt contamination from flare pit soil. Water Air Soil Pollut 133:297–314
Critto A, Torresan S, Semenzin E, Giove S, Mesman M, Schouten AJ, Rutgers M, Marcomini A (2007) Development of a site-specific ecological risk assessment for contaminated sites: part I. A multi-criteria based system for the selection of ecotoxicological tests and ecological observations. Sci Total Environ 379:16–33
Davies NA, Hodson ME, Black S (2003) The influence of time on lead toxicity and bioaccumulation determined by the OECD earthworm toxicity test. Environ Pollut 121:55–61
Diez M, Simon M, Martin F, Dorronsoro C, Garcia I, Van Gestel CAM (2009) Ambient trace element background concentrations in soils and their use in risk assessment. Sci Total Environ 407:4622–4632
DIN (1984) DIN 38414-S4 Deutsche Einheitsverfahren zur Wasser-Abwasser- und Schlammuntersuchung-Schlamm und Sedimente-Bestimmung der Eluierbarkeit mit Wasser. Deutsches Institut für Normung e.V, Berlin
Dondero F, Jonsson H, Rebelo M, Pesce G, Berti E, Pons G, Viarengo A (2006) Cellular responses to environmental contaminants in amoebic cells of the slime mould Dictyostelium discoideum. Comp Biochem Physiol 143C:150–157
Environment Canada (2002) Biological test method: reference method for determining the toxicity of sediment using luminescent bacteria in a solid-phase test EPS 1/RM/42.
Eom IC, Rast C, Veber AM, Vasseur P (2007) Ecotoxicity of a polycyclic aromatic hydrocarbon (PAH)-contaminated soil. Ecotoxicol Environ Saf 67:190–205
Epelde L, Becerril JM, Barrutia O, Gonzalez-Oreja JA, Garbisu C (2010) Interactions between plant and rhizosphere microbial communities in a metalliferous soil. Environ Pollut 158:1576–1583
Epelde L, Mijangos I, Becerril JM, Garbisu C (2009) Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol Biochem 41:1788–1794
Escoto Valerio M, Fernandez Garcia J, Martin Peinado F (2007) Determination of phytotoxicity of soluble elements in soils, based on a bioassay with lettuce (Lactuca sativa L.). Sci Total Environ 378:63–66
Eusko Jaurlaritza/Gobierno Vasco (2007) Plan de suelos contaminados del Pais Vasco (2007–2012). 1–149
Fernández MD, Tarazona JV (2008) Complementary approaches for using ecotoxicity data in soil pollution evaluation: risk based versus direct toxicity assessment. In: Dominguez, J. V. (ed) Soil contamination research trends, pp 1–50
Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414
Gleyzes C, Tellier S, Astruc M (2002) Fractionation studies of trace elements in contaminated soils and sediments: a review of sequential extraction procedures. TrAC Trends Anal Chem 21:451–467
Gray NF, O’Neill C (1997) Acid mine-drainage toxicity testing. Environ Geochem Health 19:165–171
Greene JC, Bartels CL, Warren-Hicks WJ, Parkhurst BR, Linder GL, Peterson SA, Miller WE (1989) Protocols for short term toxicity screening of hazardous waste sites, USEPA, Corvallis, OR, 1989, EPA 600/3-88/029
Gross JD (1994) Developmental decisions in Dictyostelium discoideum. Microbiol Mol Biol Rev 58:330–351
Hankard PK, Svendsen C, Wright J, Wienberg C, Fishwick SK, Spurgeon DJ, Weeks JM (2004) Biological assessment of contaminated land using earthworm biomarkers in support of chemical analysis. Sci Total Environ 330:9–20
Hoekstra NJ, Bosker T, Lantinga EA (2002) Effects of cattle dung from farms with different feeding strategies on germination and initial root growth of cress (Lepidium sativum L.). Agric Ecosyst Environ 93:189–196
Hønsi TG, Stubberud HE, Andersen S, Stenersen J (2003) Lysosomal fragility in earthworms (Eisenia veneta) exposed to heavy metal contaminated soils from two abandoned pyrite ore mines in southern Norway. Water Air Soil Pollut 142:27–37
Hund-Rinke K, Kördel W, Hennecke D, Achazi R, Warnecke D, Wilke BM, Winkel B, Heiden S (2002a) Bioassays for the ecotoxicological and genotoxicological assessment of contaminated soils (results of a round robin test). Part II. Assessment of the habitat function of soils—tests with soil microflora and fauna. J Soils Sediments 2:83–90
Hund-Rinke K, Kördel W, Hennecke D, Eisenträger A, Heiden S (2002b) Bioassays for the ecotoxicological and genotoxicological assessment of contaminated soils (results of a round robin test). Part I. Assessment of a possible groundwater contamination: ecotoxicological and genotoxicological tests with aqueous soil extracts. J Soils Sediments 2:43–50
Ihobe SA (1998a) Valores indicativos de evaluación (VIE-A). Nivel de referencia. Eusko Jaurlaritza/Gobierno Vasco Vitoria-Gasteiz, Autonomous Community of the Basque Country (Spain), 45 pp
Ihobe SA (1998b) Valores indicativos de evaluación (VIE-B, VIE-C) para la protección de los ecosistemas. Eusko Jaurlaritza/Gobierno Vasco. Vitoria-Gasteiz, Autonomous Community of the Basque Country (Spain), 104 pp
INIA, IGME, Ministerio de Medio Ambiente (2007) Anexo E: Metodología para la caracterización toxicológica de una muestra de suelo. Version Web Guía metodológica de aplicación del RD 9/2005, de 14 de enero, por el que se establece la relación de actividades potencialmente contaminantes del suelo y los criterios y estándares para la declaración de suelos contaminados (BOE núm. 15, de 18 enero 2005). 114–119
ISO (1993) Soil quality—determination of dry matter and water content on a mass basis—gravimetric method. ISO 11465
ISO (2005) Soil quality—determination of pH. International Standard. 10390, 1–7
ISO (2012) Soil quality—effects of pollutants on earthworms—part 2: determination of effects on reproduction of Eisenia fetida/Eisenia andrei. 11268–2
Lock K, Janssen CR (2001a) Zinc and cadmium body burdens in terrestrial oligochaetes: use and significance in environmental risk assessment. Environ Toxicol Chem 20:2067–2072
Lock K, Janssen CR (2001b) Cadmium toxicity for terrestrial invertebrates: taking soil parameters affecting bioavailability into account. Ecotoxicology 10:315–322
Lukkari T, Aatsinki M, Väisänen A, Haimi J (2005) Toxicity of copper and zinc assessed with three different earthworm tests. Appl Soil Ecol 30:133–146
Maisto G, Manzo S, De Nicola F, Carotenuto R, Rocco A, Alfani A (2011) Assessment of the effects of Cr, Cu, Ni and Pb soil contamination by ecotoxicological tests. J Environ Monit 13:3049–3056
Maity S, Roy S, Chaudhury S, Bhattacharya S (2008) Antioxidant responses of the earthworm Lampito mauritii exposed to Pb and Zn contaminated soil. Environ Pollut 151:1–7
Margesin R, Walder G, Schinner F (2000) The impact of hydrocarbon remediation (diesel oil and polycyclic aromatic hydrocarbons) on enzyme activities. Acta Biotechnol 20:313–333
Meers E, Du Laing G, Unamuno V, Ruttens A, Vangronsveld J, Tack FMG, Verloo MG (2007) Comparison of cadmium extractability from soils by commonly used single extraction protocols. Geoderma 141:247–259
Meima M, Schaap P (1999) Dictyostelium development—socializing through cAMP. Semin Cell Dev Biol 10:567–576
Nahmani J, Hodson ME, Black S (2007) Effects of metals on life cycle parameters of the earthworm Eisenia fetida exposed to field-contaminated, metal-polluted soils. Environ Pollut 149:44–58
Nahmani J, Hodson ME, Devin S, Vijver MG (2009) Uptake kinetics of metals by the earthworm Eisenia fetida exposed to field-contaminated soils. Environ Pollut 157:2622–2628
NEN (1994) Determination of organic matter content in soil as loss-on-ignition. NEN 5754
NEN (1997) Soil—determination of mineral oil content in soil and sediments with gas chromatography. NEN 5733
OECD (1984) Earthworm, acute toxicity tests. OECD guideline for the testing of chemicals No. 207: 1–9
OECD (2004) Earthworm reproduction test (Eisenia fetida/andrei). OECD guideline for the testing of chemicals No. 222: 1–18
Oleszczuk P, Jośko I, Kuśmierz M, Futa B, Wielgosz E, Ligęza S, Pranagal J (2014) Microbiological, biochemical and ecotoxicological evaluation of soils in the area of biochar production in relation to polycyclic aromatic hydrocarbon content. Geoderma 213:502–511
Peijnenburg WJGM, Baerselman R, de Groot AC, Jager T, Posthuma L, Van Veen RPM (1999) Relating environmental availability to bioavailability: soil-type-dependent metal accumulation in the oligochaete Eisenia andrei. Ecotoxicol Environ Saf 44:294–310
Peijnenburg WJGM, Vijver MG (2009) Earthworms and their use in eco(toxico)logical modeling. In: Devillers, J. (ed) Ecotoxicology modeling. Emerging topics in ecotoxicology: principles, approaches and perspectives 2, pp 177–204
Pietrantonio M, Calace N, Petronio BM, Pietroletti M (2003) Laboratory-polluted soils: a methodological approach to establish equilibrium conditions for different metal chemical forms in soils. J Environ Monit 5:451–454
Plaza G, Nalecz-Jawecki G, Ulfig K, Brigmon RL (2005) The application of bioassays as indicators of petroleum-contaminated soil remediation. Chemosphere 59:289–296
Ponte E, Rivero F, Fechheimer M, Noegel A, Bozzaro S (2000) Severe developmental defects in Dictyostelium null mutants for actin-binding proteins. Mech Dev 91:153–161
Pueyo M, Sastre J, Hernandez E, Vidal M, Lopez-Sanchez JF, Rauret G (2003) Prediction of trace element mobility in contaminated soils by sequential extraction. J Environ Qual 32:2054–2066
Rauret G, Lopez-Sanchez JF, Sahuquillo A, Rubio R, Davidson C, Ure A, Quevauviller P (1999) Improvement of the BCR three step sequential extraction procedure prior to the certification of new sediment and soil reference materials. J Environ Monit 1:57–61
Reijnders L (2009) Are soil pollution risks established by governments the same as actual risks? Appl Environ Soil Sci 237038. doi:10.1155/2009/237038
Renoux AY, Sunahara GI (2002) Introduction. In: Renoux GI, Thellen AY, Gaudet, CL and Pilon A (ed) Environmental analysis of contaminated sites, Wiley, pp 3–8
Rodríguez-Ruiz A, Asensio V, Zaldibar B, Soto M, Marigómez I (2014) Toxicity assessment through multiple endpoint bioassays in soils posing environmental risk according to regulatory screening values. Environ Sci Pollut Res. doi:10.1007/s11356-014-2915-7
Rodríguez-Ruiz A, Marigómez I, Boatti L, Viarengo A (2013) Dictyostelium discoideum developmental cycle (DDDC) assay: a tool for Hg toxicity assessment and soil health screening. Sci Total Environ 450–451:39–50
Rodríguez-Ruiz A (2010) Risk assessment in real soils from the Basque Country after soil health screening through toxicity profiles based on standard and novel multiple endpoint bioassays. PhD Dissertation, Univ Basque Country
Scaps P, Grelle C, Descamps M (1997) Cadmium and lead accumulation in the earthworm Eisenia fetida (Savigny) and its impact on cholinesterase and metabolic pathway enzyme activity. Comp Biochem Physiol 116C:233–238
Sforzini S, Dagnino A, Torrielli S, Dondero F, Fenoglio S, Negri A, Boatti L, Viarengo A (2008) Use of highly sensitive sublethal stress responses in the social amoeba Dictyostelium discoideum for an assessment of freshwater quality. Sci Total Environ 395:101–108
Singh J, Gupta S (1977) Plant decomposition and soil respiration in terrestrial ecosystems. Bot Rev 43:449–528
Smolders E, Oorts K, Van Sprang P, Schoeters I, Janssen CR, McGrath SP, McLaughlin MJ (2009) Toxicity of trace metals in soil as affected by soil type and aging after contamination: using calibrated bioavailability models to set ecological soil standards. Environ Toxicol Chem 28:1633–1642
Spurgeon DJ, Hopkin SP (1995) Extrapolation of the laboratory-based OECD earthworm toxicity test to metal-contaminated field sites. Ecotoxicology 4:190–205
Spurgeon DJ, Hopkin SP (1996a) Effects of metal-contaminated soils on the growth, sexual development, and early cocoon production of the earthworm Eisenia fetida, with particular reference to zinc. Ecotoxicol Environ Saf 35:86–95
Spurgeon DJ, Hopkin SP (1996b) Risk assessment of the threat of secondary poisoning by metals to predators of earthworms in the vicinity of a primary smelting works. Sci Total Environ 187:167–183
Spurgeon DJ, Hopkin SP, Jones DT (1994) Effects of cadmium, copper, lead and zinc on growth, reproduction and survival of the earthworm Eisenia fetida (Savigny): assessing the environmental impact of point-source metal contamination in terrestrial ecosystems. Environ Pollut 84:123–130
Sroka J, Madeja Z, Galanty A, Michalik M, Przestalski S, Rakoczy L, Korohoda W (2001) Trimethyltin inhibits the chemotaxis of Dictyostelium discoideum amoebae. Eur J Protistol 37:313–326
Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851
Urzelai A, Vega M, Angulo E (2000) Deriving ecological risk-based soil quality values in the Basque Country. Sci Total Environ 247:279–284
USEPA (1996a) Microwave assisted acid digestion of siliceous and organically based matrices. Method 3052:1–20
USEPA (1996b) Ultrasonic extraction. Method 3550B:1–11
USEPA (2007) Inductively coupled plasma-atomic emission spectrometry. Method 6010C:1–34
Van Gestel CAM, Van der Waarde JJ, Derksen JGM, van der Hoek EE, Veul MFXW, Bouwens S, Rusch B, Kronenburg R, Stokman GNM (2001) The use of acute and chronic bioassays to determine the ecological risk and bioremediation efficiency of oil-polluted soils. Environ Toxicol Chem 20:1438–1449
Vasseur P, Bonnard M, Palais F, Eom IC, Morel J-L (2008) Bioavailability of chemical pollutants in contaminated soils and pitfalls of chemical analyses in hazard assessment. Environ Toxicol 23:652–656
Velimirovic MB, Prica MD, Dalmacija BD, Roncevic SD, Dalmacija MB, Becelic MD, Trickovic JS (2010) Characterisation, availability, and risk assessment of the metals in sediment after aging. Water Air Soil Pollut 214:219–229
Wang W (1987) Root elongation method for toxicity testing of organic and inorganic pollutants. Environ Toxicol Chem 6:409–414
Acknowledgments
Authors are indebted to Prof. Aldo Viarengo (DISIT, University of Piemonte Orientale) for his excellent support and valuable scientific discussions. This research was funded by Basque Government (UE09+/58, IE03-110 and IE06-179 Research Projects; Grant to Consolidated Research Group, GIC07/26-IT-393-07), UPV/EHU Research & Formation Unit in “Ecosystem Health Protection” (UFI 11/37) and Spanish Ministry of Science and Education (C6L-2006-06154). ARR was recipient of a pre-doctoral fellowship from Fundación Centros Tecnológicos Iñaki Goenaga.
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Additional information on ATT and RT assays. Physicochemical characteristics, soil metal concentrations, bioaccumulation in earthworms and toxicity (Microtox® and earthworm ATT and RT) of the LA soil dilutions and the control (OECD) and reference (DE) soils employed in the ATT and RT earthworm assays. (DOCX 40.9 kb)
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Rodriguez-Ruiz, A., Etxebarria, J., Boatti, L. et al. Scenario-targeted toxicity assessment through multiple endpoint bioassays in a soil posing unacceptable environmental risk according to regulatory screening values. Environ Sci Pollut Res 22, 13344–13361 (2015). https://doi.org/10.1007/s11356-015-4564-x
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DOI: https://doi.org/10.1007/s11356-015-4564-x