Abstract
A cross-transplantation field experiment was performed to investigate about possible adaptation/acclimatization to metal pollution in common garden snail Cantareus aspersus (ex-Helix aspersa) and brown-lipped grove snail Cepaea nemoralis populations. Adults were collected from an area surrounding a former smelter (ME), highly polluted by trace metals (TMs) for decades, and from an unpolluted site (BE). Subadults of first generation (F1) were exposed in microcosms in a 28-day kinetic study. Four exposure sites were chosen around the smelter along a soil pollution gradient (vegetation and soil otherwise comparable). Bioaccumulation in snail soft tissues globally increased with soil contamination, with Cd, Pb and Zn concentrations reaching 271, 187, 5527 μg g−1, respectively. Accumulation kinetic patterns were similar between snail species but C. nemoralis showed greater TM levels than C. aspersus. Some inter-population differences were revealed in TM accumulation (bioaccumulation factors, accumulation kinetics) but did not suggest consistent adaptive responses. We did not detect negative effects of TM exposure on snail condition (body weight, shell size, shell weight). ME C. aspersus snails produced heavier shells than BE snails under exposure to TMs at the highest level, suggesting an adaptive response. The protocol used in this study, however, did not allow unambiguously distinguishing whether this response was due to genetic adaptation or to maternal effects. Abnormal but reversible shell development of adult ME C. nemoralis suggested physiological acclimatization. Differences in responses to TMs between populations are observed for conchological parameters, not for bioaccumulation, with different strategies according to the species (acclimatization or adaptation/maternal effects).
Similar content being viewed by others
References
AFNOR (1996) Qualité des sols—Méthodes chimiques—sols sédiments, mise en solution totale par attaque acide—NF X31–147. Association Française de Normalisation, Paris
AFNOR (1999) Qualité des sols—Méthodes chimiques—Détermination de la capacité d’échange cationique (CEC) et des cations extractibles—NF X31–130. Association Française de Normalisation, Paris
AFNOR (2003) Qualité des sols—determination de la distribution granulométrique des particules du sol - Méthode à la pipette—NF X31–107. Association Française de Normalisation, Paris
Arnaud JF, Madec L, Guiller A, Bellido A (2001) Spatial analysis of allozyme and microsatellite DNA polymorphisms in the land snail Helix aspersa (Gastropoda : Helicidae). Mol Ecol 10:1563–1576. doi:10.1046/j.1365-294X.2001.01292.x
Baur A, Baur B (1993) Daily movement patterns and dispersal in the land snail Arianta arbustorum. Malacologia 35:89–98
Beeby A (1993) The interaction of Pb and Ca assimilation in Helix aspersa with wounded shells. Pol J Environ Stud 2:9–13
Beeby A (2001) What do sentinels stand for? Environ Pollut 112:285–298. doi:10.1016/S0269-7491(00)00038-5
Beeby A, Richmond L (1988) Calcium metabolism in two populations of the snail Helix aspersa on a high-lead diet. Arch Environ Contam Toxicol 17:507–511. doi:10.1007/BF01055516
Beeby A, Richmond L (1998) Variation in the mineral composition of eggs of the snail, Helix aspersa between populations exposed to different levels of metal contamination. Environ Pollut 101:25–31. doi:10.1016/S0269-7491(98)00040-2
Beeby A, Richmond L (2001a) Intraspecific competition in populations of Helix aspersa with different histories of exposure to lead. Environ Pollut 114:337–344. doi:10.1016/S0269-7491(00)00241-4
Beeby A, Richmond L (2001b) Calcium provision to eggs in two populations of Helix aspersa by parents fed a diet high in lead. J Mollusc Stud 67:1–6. doi:10.1093/mollus/67.1.1
Beeby A, Richmond L (2002) Evaluating Helix aspersa as a sentinel for mapping metal pollution. Ecol Indicators 1:261–270. doi:10.1016/S1470-160X(02)00022-5
Beeby A, Richmond L (2003) Do the soft tissues of Helix aspersa serve as a quantitative sentinel of predicted free lead concentrations in soils? Appl Soil Ecol 22:159–165. doi:10.1016/S0929-1393(02)00130-0
Beeby A, Richmond L (2010) Magnesium and the regulation of lead in three populations of the garden snail Cantareus aspersus. Environ Pollut (in press) Corrected proof doi:10.1016/j.envpol.2010.02.002
Beeby A, Richmond L, Herpe F (2002) Lead reduces shell mass in juvenile garden snails (Helix aspersa). Environ Pollut 120:283–288. doi:10.1016/S0269-7491(02)00151-3
Belfiore NM, Anderson SL (1998) Genetic patterns as a tool for monitoring and assessment of environmental impacts: The example of genetic ecotoxicology. Environ Monit Assess 51:465–479. doi:10.1023/A:1005971132502
Berger B, Dallinger R (1993) Terrestrial snails as quantitative indicators of environmental metal pollution. Environ Monit Assess 25:65–84. doi:10.1007/BF00549793
Bonneris E, Giguere A, Perceval O, Buronfosse T, Masson S, Hare L, Campbell PGC (2005) Sub-cellular partitioning of metals (Cd, Cu, Zn) in the gills of a freshwater bivalve, Pyganodon grandis: role of calcium concretions in metal sequestration. Aquat Toxicol 71:319–334. doi:10.1016/j.aquatox.2004.11.025
Brown BE (1982) The form and function of metal-containing granules in invertebrate tissues. Biol Rev Camb Philos Soc 57:621–667. doi:10.1111/j.1469-185X.1982.tb00375.x
Cameron RAD, Williamson P (1977) Estimating migration and effects of disturbance in mark-recapture studies on snail Cepaea nemoralis L. J Anim Ecol 46:173–179
Chevalier L, Desbuquois C, Le Lannic J, Charrier M (2001) Poaceae in the natural diet of the snail Helix aspersa Müller (Gasteropoda, Pulmonata). Compte Rendu de l’Académie des Sciences. Paris 324:979–987
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719. doi:10.1016/j.biochi.2006.07.003
Coeurdassier M, Gomot-de Vaufleury A, Lovy C, Badot P-M (2002) Is the cadmium uptake from soil important in bioaccumulation and toxic effects for snails. Ecotoxicol Environ Saf 53:425–431. doi:10.1016/S0147-6513(02)00004-0
Crawley MJ (2007) The R book. John Wiley & Sons, Ltd, Chichester
Dallinger R, Rainbow PS (1993) Ecotoxicology of metals in invertebrates. Lewis Publishers, Boca raton
Dallinger R, Lagg B, Egg M, Schipflinger R, Chabicovsky M (2004) Cd accumulation and Cd-metallothionein as a biomarker in Cepaea hortensis (Helicidae, Pulmonata) from laboratory exposure and metal-polluted habitats. Ecotoxicology 13:757–772. doi:10.1007/s10646-003-4474-4
de Vaufleury A, Coeurdassier M, Pandard P, Scheifler R, Lovy C, Crini N, Badot P-M (2006) How terrestrial snails can be used in risk assessment of soils. Environ Toxicol Chem 25:797–806. doi:10.1897/04-560R.1
Douay F, Pruvot C, Roussel H, Ciesielski H, Fourrier H, Proix N, Waterlot C (2008) Contamination of urban soils in an area of Northern France polluted by dust emissions of two smelters. Water Air Soil Pollut 188:247–260. doi:10.1007/s11270-007-9541-7
Douay F, Pruvot C, Waterlot C, Fritsch C, Fourrier H, Loriette A, Bidar G, Grand C, de Vaufleury A, Scheifler R (2009) Contamination of woody habitat soils around a former lead smelter in the North of France. Sci Total Environ 407:5564–5577. doi:10.1016/j.scitotenv.2009.06.015
Fairbrother A, Wenstel R, Sappington K, Wood W (2007) Framework for metals risk assessment. Ecotoxicol Environ Saf 68:145–227. doi:10.1016/j.ecoenv.2007.03.015
Fritsch C, Scheifler R, Beaugelin-Seiller K, Hubert P, Coeurdassier M, de Vaufleury A, Badot P-M (2008) Biotic interactions modify the transfer of cesium-137 in a soil-earthworm-plant-snail food web. Environ Toxicol Chem 27:1698–1707. doi:10.1897/07-416.1
Fritsch C, Cosson RP, Coeurdassier M, Raoul F, Giraudoux P, Crini N, de Vaufleury A, Scheifler R (2010a) Responses of wild small mammals to a pollution gradient: host factors influence metal and metallothionein levels. Environ Pollut 158:827–840. doi:10.1016/j.envpol.2009.09.027
Fritsch C, Giraudoux P, Coeurdassier M, Douay F, Raoul F, Pruvot C, Waterlot C, Vaufleury Ad, Scheifler R (2010b) Spatial distribution of metals in smelter-impacted soils of woody habitats: Influence of landscape and soil properties, and risk for wildlife. Chemosphere 81:141–155. doi:10.1016/j.chemosphere.2010.06.075
Gimbert F (2006) Cinétiques de transfert de polluants métalliques du sol à l’escargots. Dissertation, University of Franche-Comté
Gimbert F, de Vaufleury A, Douay F, Scheifler R, Coeurdassier M, Badot P-M (2006) Modelling chronic exposure to contaminated soil: a toxicokinetic approach with the terrestrial snail Helix aspersa. Environ Int 32:866–875. doi:10.1016/j.envint.2006.05.006
Gimbert F, de Vaufleury A, Douay F, Coeurdassier M, Scheifler R, Badot P-M (2008a) Long-term responses of snails exposed to cadmium-contaminated soils in a partial life-cycle experiment. Ecotoxicol Environ Saf 70:138–146. doi:10.1016/j.ecoenv.2007.05.014
Gimbert F, Mench M, Coeurdassier M, Badot P-M, de Vaufleury A (2008b) Kinetic and dynamic aspects of soil-plant-snail transfer of cadmium in the field. Environ Pollut 152:736–745. doi:10.1016/j.envpol.2007.06.044
Gimbert F, Vijver MG, Coeurdassier M, Scheifler R, Peijnenburg WJGM, Badot PM, de Vaufleury A (2008c) How subcellular partitioning can help to understand heavy metal accumulation and elimination kinetics in snails. Environ Toxicol Chem 27:1284–1292. doi:10.1897/07-503.1
Gomot A (1997) Dose-dependent effects of cadmium on the growth of snails in toxicity bioassays. Arch Environ Contam Toxicol 33:209–216. doi:10.1007/s002449900245
Gomot A, Pihan F (1997) Comparison of the bioaccumulation capacities of copper and zinc in two snail subspecies (Helix). Ecotoxicol Environ Saf 38:85–94. doi:10.1006/eesa.1997.1566
Gomot A, Gomot L, Boukraa S, Bruckert S (1989) Influence of soil on the growth of the land snail Helix aspersa. An experimental study of the absorption route for the stimulating factors. J Mollusc Stud 55:1–7. doi:10.1093/mollus/55.1.1-a
Gomot-de Vaufleury A (2000) Standardized growth toxicity testing (Cu, Zn, Pb, and Pentachlorophenol) with Helix aspersa. Ecotoxicol Environ Saf 46:41–50. doi:10.1006/eesa.1999.1872
Gomot-de Vaufleury A, Bispo A (2000) Methods for toxicity assessment of contaminated soil by oral or dermal uptake in land snails. 1. Sublethal effects on growth. Environ Sci Technol 34:1865–1870. doi:10.1021/es9907212
Gomot-de Vaufleury A, Pihan F (2000) Growing snails used as sentinels to evaluate terrestrial environment contamination by trace elements. Chemosphere 40:275–284. doi:10.1016/S0045-6535(99)00246-5
Harmsen J (2007) Measuring bioavailability: from a scientific approach to standard methods. J Environ Qual 36:1420–1428. doi:10.2134/jeq2006.0492
Hendrickx F, Maelfait J-P, Bogaert N, Tojal C, Du Laing G, Tack FMG, Verloo MG (2004) The importance of biological factors affecting trace metal concentration as revealed from accumulation patterns in co-occurring terrestrial invertebrates. Environ Pollut 127:335–341. doi:10.1016/j.envpol.2003.09.001
Hispard F, Schuler D, de Vaufleury A, Scheifler R, Badot PM, Dallinger R (2008) Metal distribution and metallothionein induction after cadmium exposure in the terrestrial snail Helix aspersa (gastropoda, pulmonata). Environ Toxicol Chem 27:1533–1542. doi:10.1897/07-232.1
Hobbelen PHF, Koolhaas JE, van Gestel CAM (2006) Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environ Pollut 144:639–646. doi:10.1016/j.envpol.2006.01.019
ISO (1994) Soil quality—Determination of pH—ISO 10390:1994. International Organization for Standardization, Geneva
ISO (1995a) Soil quality—Determination of carbonate content. Volumetric method—ISO 10693:1995. International Organization for Standardization, Geneva
ISO (1995b) Soil quality—Determination of organic and total carbon after dry combustion (elementary analysis)—ISO 10694:1995. International Organization for Standardization, Geneva
ISO (2006) Soil quality—Effects of pollutants on juvenile land snails (Helicidae). Determination of the effects on growth by soil contamination—ISO 15952:2006. International Organization for Standardization, Geneva
ISO (2008) Soil quality—requirements and guidance for the selection and application of methods for the assessment of bioavailability of contaminants in soil and soil materials. ISO 17402:2008. International Organization for Standardization, Geneva
Jordaens K, De Wolf H, Van Houtte N, Vandecasteele B, Backeljau T (2006a) Genetic variation in two land snails, Cepaea nemoralis and Succinea putris (Gastropoda, Pulmonata), from sites differing in heavy metal content. Genetica 128:227–239. doi:10.1007/s10709-005-5705-9
Jordaens K, De Wolf H, Vandecasteele B, Blust R, Backeljau T (2006b) Associations between shell strength, shell morphology and heavy metals in the land snail Cepaea nemoralis (Gastropoda, Helicidae). Sci Total Environ 363:285–293. doi:10.1016/j.scitotenv.2005.12.002
Kammenga J, Laskowski R (2000) Demography in ecotoxicology. Ecological an environmental toxicology Series. John Wiley & Sons, Chichester
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi:10.1111/j.1461-0248.2004.00684.x
Kleewein D (1999) Population size, density, spatial distribution and dispersal in an Austrian population of the land snail Arianta arbustorum styriaca (Gastropoda: Helicidae). J Mollusc Stud 65:303–315. doi:10.1093/mollus/65.3.303
Lagisz M, Laskowski R (2008) Evidence for between-generation effects in carabids exposed to heavy metals pollution. Ecotoxicology 17:59–66. doi:10.1007/s10646-007-0176-7
Laskowski R, Hopkin SP (1996) Effect of Zn, Cu, Pb, and Cd on fitness in snails (Helix aspersa). Ecotoxicol Environ Saf 34:59–69. doi:10.1006/eesa.1996.0045
Lindstrom M, Bates DM (1990) Nonlinear mixed effects models for repeated measures data. Biometrics 46:673–687
Meers E, Samson R, Tack FMG, Ruttens A, Vandegehuchte M, Vangronsveld J, Verloo MG (2007) Phytoavailability assessment of heavy metals in soils by single extractions and accumulation by Phaseolus vulgaris. Environ Exp Bot 60:385–396. doi:10.1016/j.envexpbot.2006.12.010
Menta C, Parisi V (2001) Metal concentrations in Helix pomatia, Helix aspersa and Arion rufus: a comparative study. Environ Pollut 115:205–208. doi:10.1016/S0269-7491(01)00110-5
Monteiro MS, Santos C, Soares A, Mann RM (2008) Does subcellular distribution in plants dictate the trophic bioavailability of cadmium to Porcellio dilatatus (Crustacea, Isopoda)? Environ Toxicol Chem 27:2548–2556. doi:10.1897/08-154.1
Morgan AJ, Kille P, Stürzenbaum SR (2007) Microevolution and ecotoxicology of metals in invertebrates. Environ Sci Technol 41:1085–1096. doi:10.1021/es061992x
Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407. doi:10.1016/S0169-5347(98)01472-4
Mulvey M, Newman MC, Beeby AN (1996) Genetic and conchological comparison of snails (Helix aspersa) differing in shell deposition of lead. J Mollusc Stud 62:213–223. doi:10.1093/mollus/62.2.213
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. doi:10.1016/j.envpol.2009.05.002
Notten MJM, Oosthoek AJP, Rozema J, Aerts R (2005) Heavy metal concentrations in a soil-plant-snail food chain along a terrestrial soil pollution gradient. Environ Pollut 138:178–190. doi:10.1016/j.envpol.2005.01.011
Notten MJM, Oosthoek AJP, Rozema J, Aerts R (2006) Heavy metal pollution affects consumption and reproduction of the landsnail Cepaea nemoralis fed on naturally polluted Urtica dioica leaves. Ecotoxicology 15:295–304. doi:10.1007/s10646-006-0059-3
Peijnenburg WJGM, Jager T (2003) Monitoring approaches to assess bioaccessibility and bioavailability of metals: Matrix issues. Ecotoxicol Environ Saf 56:63–77. doi:10.1016/S0147-6513(03)00051-4
Pfenninger M (2002) Relationship between microspatial population genetic structure and habitat heterogeneity in Pomatias elegans (OF Muller 1774) (Caenogastropoda, Pomatiasidae). Biol J Linn Soc 76:565–575. doi:10.1046/j.1095-8312.2002.00080.x
Pihan F, de Vaufleury A (2000) The snail as a target organism for the evaluation of industrial waste dump contamination and the efficiency of its remediation. Ecotoxicol Environ Saf 46:137–147. doi:10.1006/eesa.1999.1891
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag, New York
Posthuma L, van Straalen NM (1993) Heavy metal adaptation in terrestrial invertebrates—A review of occurrence, genetics, physiology and ecological consequences. Comp Biochem Physiol C 106:11–38. doi:10.1016/0742-8413(93)90251-F
Quensen JF, Woodruff DS (1997) Associations between shell morphology and land crab predation in the land snail Cerion. Funct Ecol 11:464–471. doi:10.1046/j.1365-2435.1997.00115.x
R Development Core Team (2006) R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Regoli F, Gorbi S, Fattorini D, Tedesco S, Notti A, Machella N, Bocchetti R, Benedetti M, Piva F (2006) Use of the land snail Helix aspersa as sentinel organism for monitoring ecotoxicologic effects of urban pollution: an integrated approach. Environ Health Perspect 114:63–69. doi:10.1289/ehp.8397
Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer-Verlag, New York
Roelofs D, Janssens TKS, Timmermans MJTN, Nota B, Marien J, Bochdanovits Z, Ylstra B, Van Straalen NM (2009) Adaptive differences in gene expression associated with heavy metal tolerance in the soil arthropod Orchesella cincta. Mol Ecol 18:3227–3239. doi:10.1111/j.1365-294X.2009.04261.x
Rozen A (2006) Effect of cadmium on life-history parameters in Dendrobaena octaedra (Lumbricidae: Oligochaeta) populations originating from forests differently polluted with heavy metals. Soil Biol Biochem 38:489–503. doi:10.1016/j.soilbio.2005.06.003
Russell LK, de Haven JJ, Botts RP (1981) Toxic effects of cadmium on the garden snail (Helix aspersa). Bull Environ Contam Toxicol 26:634–640
Scheifler R, Ben Brahim M, Gomot-de Vaufleury A, Carnus J-M, Badot P-M (2003) A field method using microcosms to evaluate transfer of Cd, Cu, Ni, Pb and Zn from sewage sludge amended forest soils to Helix aspersa snails. Environ Pollut 122:343–350. doi:10.1016/S0269-7491(02)00333-0
Scheifler R, de Vaufleury A, Coeurdassier M, Crini N, Badot PM (2006) Transfer of Cd, Cu, Ni, Pb, and Zn in a soil-plant-invertebrate food chain: A microcosm study. Environ Toxicol Chem 25:815–822. doi:10.1897/04-675R.1
Schilthuizen M, Van Til A, Salverda M, Liew TS, James S, Bin Elahan B, Vermeulen JJ (2006) Microgeographic evolution of snail shell shape and predator behavior. Evolution 60:1851–1858. doi:10.1554/06-114.1
Schweiger O, Frenzel M, Durka W (2004) Spatial genetic structure in a metapopulation of the land snail Cepaea nemoralis (Gastropoda : Helicidae). Mol Ecol 13:3645–3655. doi:10.1111/j.1365-294X.2004.02357.x
Sidoumou Z, GnassiaBarelli M, Romeo M (1997) Cadmium and calcium uptake in the mollusc Donax rugosus and effect of a calcium channel blocker. Bull Environ Contam Toxicol 58:318–325. doi:10.1007/s001289900337
Smith R, Pollard SJT, Weeks JM, Nathanail CP (2006) Assessing harm to terrestrial ecosystems from contaminated land. Soil Use Manage 21:527–540. doi:10.1079/SUM2005345
Spurgeon DJ, Hopkin SP (2000) The development of genetically inherited resistance to zinc in laboratory-selected generations of the earthworm Eisenia fetida. Environ Pollut 109:193–201. doi:10.1016/S0269-7491(99)00267-5
Sterckeman T, Douay F, Proix N, Fourrier H, Perdrix E (2002) Assessment of the contamination of cultivated soils by eighteen trace elements around smelters in the North of France. Water Air Soil Pollut 135:173–194. doi:10.1023/A:1014758811194
Van Gestel CAM (2008) Physico-chemical and biological parameters determine metal bioavailability in soils. Sci Total Environ 406:385–395. doi:10.1016/j.scitotenv.2008.05.050
Veltman K, Huijbregts MAJ, Hendriks AJ (2008) Cadmium bioaccumulation factors for terrestrial species: Application of the mechanistic bioaccumulation model OMEGA to explain field data. Sci Total Environ 406:413–418. doi:10.1016/j.scitotenv.2008.05.049
Viard W, Pihan F, Promeyrat S, Pihan JC (2004) Integrated assessment of heavy metal (Pb, Zn, Cd) highway pollution: bioaccumulation in soil, Graminaceae and land snails. Chemosphere 55:1349–1359. doi:10.1016/j.chemosphere.2004.01.003
Vijver MG, Van Gestel CAM, Lanno RP, Van Straalen NM, Peijnenburg WJGM (2004) Internal metal sequestration and its ecotoxicological relevance: a review. Environ Sci Technol 38:4705–4712. doi:10.1021/es040354g
Williamson P (1980) Variables affecting body burdens of lead, zinc and cadmium in a roadside population of the snail Cepaea hortensis Müller. Oecologia 44:213–220. doi:10.1007/BF00572682
Williamson P, Cameron RAD (1976) Natural diet of landsnail Cepaea nemoralis. Oikos 27:493–500
Wood SN (2006) Generalized additive models—an introduction with R. Chapman et Hall/CRC Press - Taylor & Francis Group, Boca Raton
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions with R. Springer, New York
Acknowledgments
We gratefully thank Cécile Grand from the Agence De l’Environnement et de la Maîtrise de l’Energie (ADEME) for many fruitful scientific discussions. We also warmly thank Elie Dhivert, Willy Gerbaud, Jean-Claude Lambert, Dominique Rieffel and Nicolas Tête for their technical assistance, and Peter Winterton for the review of the English language. The STARTT programme was financially supported by the Agence Nationale de la Recherche (ANR, contract n°ANR-05-ECCO-004) and the ADEME (contract n°0572C0058). Clémentine Fritsch was financially supported by a grant from the ADEME and the Conseil Régional de Franche-Comté. The authors are indebted to two anonymous Reviewers for improving the manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Fritsch, C., Coeurdassier, M., Gimbert, F. et al. Investigations of responses to metal pollution in land snail populations (Cantareus aspersus and Cepaea nemoralis) from a smelter-impacted area. Ecotoxicology 20, 739–759 (2011). https://doi.org/10.1007/s10646-011-0619-z
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-011-0619-z