Spatially Explicit Analysis of Metal Transfer to Biota: Influence of Soil Contamination and Landscape

Concepts and developments for a new field in ecotoxicology, referred to as “landscape ecotoxicology,” were proposed in the 1990s; however, to date, few studies have been developed in this emergent field. In fact, there is a strong interest in developing this area, both for renewing the concepts and tools used in ecotoxicology as well as for responding to practical issues, such as risk assessment. The aim of this study was to investigate the spatial heterogeneity of metal bioaccumulation in animals in order to identify the role of spatially explicit factors, such as landscape as well as total and extractable metal concentrations in soils. Over a smelter-impacted area, we studied the accumulation of trace metals (TMs: Cd, Pb and Zn) in invertebrates (the grove snail Cepaea sp and the glass snail Oxychilus draparnaudi) and vertebrates (the bank vole Myodes glareolus and the greater white-toothed shrew Crocidura russula). Total and CaCl2-extractable concentrations of TMs were measured in soils from woody patches where the animals were captured. TM concentrations in animals exhibited a high spatial heterogeneity. They increased with soil pollution and were better explained by total rather than CaCl2-extractable TM concentrations, except in Cepaea sp. TM levels in animals and their variations along the pollution gradient were modulated by the landscape, and this influence was species and metal specific. Median soil metal concentrations (predicted by universal kriging) were calculated in buffers of increasing size and were related to bioaccumulation. The spatial scale at which TM concentrations in animals and soils showed the strongest correlations varied between metals, species and landscapes. The potential underlying mechanisms of landscape influence (community functioning, behaviour, etc.) are discussed. Present results highlight the need for the further development of landscape ecotoxicology and multi-scale approaches, which would enhance our understanding of pollutant transfer and effects in ecosystems.

[1]  Peter B Woodbury,et al.  Dos and don'ts of spatially explicit ecological risk assessments , 2003, Environmental toxicology and chemistry.

[2]  C. S. Boring,et al.  The development of a spatially explicit model to estimate radiocaesium body burdens in raccoons (Procyon lotor) for ecological risk assessment. , 2005, The Science of the total environment.

[3]  R. Smith,et al.  Quantifying Fine-Scale Variability in Pollutant Deposition in Complex Terrain using 210Pb Inventories in Soil , 1998 .

[4]  F. Burel,et al.  Landscape Ecology : Concepts, Methods, and Applications , 2003 .

[5]  A. Kozakiewicz,et al.  Use of space by bank voles (Clethrionomys glareolus) in a polish farm landscape , 1993, Landscape Ecology.

[6]  Françoise Burel,et al.  Differential response of selected taxa to landscape context and agricultural intensification , 2004 .

[7]  M. Vijver,et al.  Internal metal sequestration and its ecotoxicological relevance: a review. , 2004, Environmental science & technology.

[8]  K. Sawicka-Kapusta,et al.  Histopathological changes in the liver, kidneys, and testes of bank voles environmentally exposed to heavy metal emissions from the steelworks and zinc smelter in Poland. , 2004, Environmental research.

[9]  William G. Wallace,et al.  Subcellular compartmentalization of Cd and Zn in two bivalves. II. Significance of trophically available metal (TAM) , 2003 .

[10]  M. Coeurdassier,et al.  Investigations of responses to metal pollution in land snail populations (Cantareus aspersus and Cepaea nemoralis) from a smelter-impacted area , 2011, Ecotoxicology.

[11]  Ł. Sobczyk,et al.  Species diversity and spatial distribution of enchytraeid communities in forest soils: effects of habitat characteristics and heavy metal contamination , 2003 .

[12]  Anne Fairbrother,et al.  Framework for metals risk assessment. , 2007, Ecotoxicology and environmental safety.

[13]  Joop Harmsen,et al.  Measuring bioavailability: from a scientific approach to standard methods. , 2007, Journal of environmental quality.

[14]  J. Rozema,et al.  Heavy metal concentrations in a soil-plant-snail food chain along a terrestrial soil pollution gradient. , 2005, Environmental pollution.

[15]  R. F. Shore,et al.  Ecotoxicology of wild mammals , 2000 .

[16]  P. Williamson.  Variables affecting body burdens of lead, zinc and cadmium in a roadside population of the snailCepaea hortensis Müller , 2004, Oecologia.

[17]  S. J. Turner.  Landscape Ecology Concepts, Methods and Applications , 2005, Landscape Ecology.

[18]  P. Badot,et al.  Is the cadmium uptake from soil important in bioaccumulation and toxic effects for snails? , 2002, Ecotoxicology and environmental safety.

[19]  A. Sánchez-Chardi,et al.  Bioaccumulation of metals and effects of landfill pollution in small mammals. Part I. The greater white-toothed shrew, Crocidura russula. , 2007, Chemosphere.

[20]  R. Samson,et al.  Phytoavailability assessment of heavy metals in soils by single extractions and accumulation by Phaseolus vulgaris , 2007 .

[21]  W. Dimmers,et al.  Effects of soil properties on food web accumulation of heavy metals to the wood mouse (Apodemus sylvaticus). , 2010, Environmental pollution.

[22]  C. Pruvot,et al.  Contamination of Urban Soils in an Area of Northern France Polluted by Dust Emissions of Two Smelters , 2008 .

[23]  P. Badot,et al.  Comparison of transfer and effects of Cd on rats exposed in a short experimental snail-rat food chain or to CdCl2 dosed food. , 2008, Environment international.

[24]  W. Klein,et al.  Underlying issues including approaches and information needs in risk assessment. , 2003, Ecotoxicology and environmental safety.

[25]  P. Badot,et al.  Transfer of Cd, Cu, Ni, Pb, and Zn in a soil‐plant‐invertebrate food chain: A microcosm study , 2006, Environmental toxicology and chemistry.

[26]  Conceição Santos,et al.  Does subcellular distribution in plants dictate the trophic bioavailability of cadmium to Porcellio dilatatus (crustacea, isopoda)? , 2008, Environmental toxicology and chemistry.

[27]  B. Hope.  An examination of ecological risk assessment and management practices. , 2006, Environment international.

[28]  T. Sterckeman,et al.  Assessment of the Contamination of Cultivated Soils by Eighteen Trace Elements Around Smelters in the North of France , 2002 .

[29]  Tina M Carlsen,et al.  The spatial extent of contaminants and the landscape scale: An analysis of the wildlife, conservation biology, and population modeling literature , 2004, Environmental toxicology and chemistry.

[30]  A. Sánchez-Chardi,et al.  Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Doñana. , 2009, Chemosphere.

[31]  J. Harmsen.  Soil quality - Requirements and guidance for the selection and application of methods for the assessment of bioavailability of contaminants in soil and soil materials , 2008 .

[32]  C. P. Nathanail,et al.  Assessing significant harm to terrestrial ecosystems from contaminated land , 2005 .

[33]  P. Williamson,et al.  Estimating Migration and the Effects of Disturbance in Mark-Recapture Studies on the Snail Cepaea nemoralis L. , 1977 .

[34]  E. Pollard,et al.  Hedges. V. A Study of Small Mammals in Hedges and Cultivated Fields , 1970 .

[35]  Paweł Koteja,et al.  Laboratory Model of Adaptive Radiation: A Selection Experiment in the Bank Vole , 2008, Physiological and Biochemical Zoology.

[36]  Larry Kapustka,et al.  Limitations of the Current Practices Used to Perform Ecological Risk Assessment , 2008, Integrated environmental assessment and management.

[37]  T. Sterckeman,et al.  Vertical distribution of Cd, Pb and Zn in soils near smelters in the North of France. , 2000, Environmental pollution.

[38]  C. A. V. van Gestel,et al.  Effects of spatial and temporal variation in metal availability on earthworms in floodplain soils of the river Dommel, The Netherlands. , 2007, Environmental pollution.

[39]  J. Tramper,et al.  Modeling zinc regulation in small mammals , 2009, Environmental toxicology and chemistry.

[40]  I. Udina,et al.  RESTRICTION FRAGMENT LENGTH POLYMORPHISM (RFLP) OF EXON 2 OF THE MHCBIBO-DRB3 GENE IN EUROPEAN BISON BISON BONASUS , 1998 .

[41]  B. T. Walton,et al.  Small mammals as monitors of environmental contaminants. , 1991, Reviews of environmental contamination and toxicology.

[42]  Joanna Burger,et al.  Methodologies to examine the importance of host factors in bioavailability of metals. , 2003, Ecotoxicology and environmental safety.

[43]  J. Burger,et al.  Methodologies for assessing exposure to metals: speciation, bioavailability of metals, and ecological host factors. , 2003, Ecotoxicology and environmental safety.

[44]  K. D. Reynolds,et al.  Contaminant exposure in terrestrial vertebrates. , 2007, Environmental pollution.

[45]  J. Cairns,et al.  Developing a Field of Landscape Ecotoxicology , 1996 .

[46]  Pierre Fontanillas,et al.  Landscape structure affects dispersal in the greater white-toothed shrew : Inference between genetic and simulated ecological distances , 2007 .

[47]  Lawrence Barnthouse,et al.  Population-Level Ecological Risk Assessment , 2007 .

[48]  A. Baur,et al.  Daily movement patterns and dispersal in the land snail Arianta arbustorum , 1993 .

[49]  C. A. V. van Gestel.  Physico-chemical and biological parameters determine metal bioavailability in soils. , 2008, The Science of the total environment.

[50]  M. Marinussen,et al.  Conceptual approach to estimating the effect of home-range size on the exposure of organisms to spatially variable soil contamination , 1996 .

[51]  F. Raoul,et al.  Responses of wild small mammals to a pollution gradient: host factors influence metal and metallothionein levels. , 2010, Environmental pollution.

[52]  J. Frangi,et al.  Heavy metal soil pollution cartography in northern France , 1997 .

[53]  S. Luoma,et al.  Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM) , 2003 .

[54]  W. Peijnenburg,et al.  Monitoring approaches to assess bioaccessibility and bioavailability of metals: matrix issues. , 2003, Ecotoxicology and environmental safety.

[55]  N. Minoretti,et al.  Effects of Soil Type and Adult Size on Mating Propensity and Reproductive Output in Two Populations of the Land Snail Arianta arbustorum (Linnaeus) , 2009 .

[56]  V. Ettler,et al.  Contrasting lead speciation in forest and tilled soils heavily polluted by lead metallurgy. , 2005, Chemosphere.

[57]  F M Danson,et al.  Multi-scale spatial analysis of human alveolar echinococcosis risk in China , 2003, Parasitology.

[58]  M. J. López-Fuster,et al.  Bioaccumulation of lead, mercury, and cadmium in the greater white-toothed shrew, Crocidura russula, from the Ebro Delta (NE Spain): sex- and age-dependent variation. , 2007, Environmental pollution.

[59]  A. Zweep,et al.  The role of food in the dynamics of populations of the landsnail Cepaea nemoralis , 1971, Oecologia.

[60]  F. Burel,et al.  Response of the small mammal community to changes in western French agricultural landscapes , 2003, Landscape Ecology.

[61]  R. Leuven,et al.  Modelling Recolonisation of Heterogeneous River Floodplains by Small Mammals , 2006, Hydrobiologia.

[62]  M. Kozakiewicz.  The weight of eye lens as the proposed age indicator of the bank vole , 1976 .

[63]  David F. Ludwig,et al.  An approach to quantifying spatial components of exposure for ecological risk assessment , 1995 .

[64]  Aafke M Schipper,et al.  Modeling the influence of environmental heterogeneity on heavy metal exposure concentrations for terrestrial vertebrates in river floodplains , 2008, Environmental toxicology and chemistry.

[65]  Reinhard Dallinger,et al.  Terrestrial snails as quantitative indicators of environmental metal pollution , 1993, Environmental monitoring and assessment.

[66]  C. Mason.  Food, feeding rates and assimilation in woodland snails , 1970, Oecologia.

[67]  R. Dallinger,et al.  Cd Accumulation and Cd–Metallothionein as a Biomarker in Cepaea hortensis (Helicidae, Pulmonata) from Laboratory Exposure and Metal-polluted Habitats , 2004, Ecotoxicology.

[68]  B K Hope.  Generating probabilistic spatially-explicit individual and population exposure estimates for ecological risk assessments. , 2000, Risk analysis : an official publication of the Society for Risk Analysis.

[69]  F. Hendrickx,et al.  The importance of biological factors affecting trace metal concentration as revealed from accumulation patterns in co-occurring terrestrial invertebrates. , 2004, Environmental pollution.

[70]  P. Williamson,et al.  Natural diet of the landsnail Cepaea nemoralis , 1976 .

[71]  C. A. V. van Gestel,et al.  Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. , 2006, Environmental pollution.

[72]  J. Ares.  Time and space issues in ecotoxicology: Population models, landscape pattern analysis, and long‐range environmental chemistry , 2003, Environmental toxicology and chemistry.

[73]  A. Gomot de Vaufleury,et al.  Growing snails used as sentinels to evaluate terrestrial environment contamination by trace elements. , 2000, Chemosphere.

[74]  K. Abt,et al.  Seasonal variations of diet composition in farmland field mice Apodemus spp. and bank voles Clethrionomys glareolus , 1998 .

[75]  C. Pruvot,et al.  Contamination of woody habitat soils around a former lead smelter in the North of France. , 2009, The Science of the total environment.

[76]  P. Bergers,et al.  Landscape approach to bank vole ecology , 2000 .

[77]  J. Zawadzki,et al.  Using of high-resolution topsoil magnetic screening for assessment of dust deposition: comparison of forest and arable soil datasets , 2007, Environmental monitoring and assessment.

[78]  R M Sibly,et al.  Risk Assessment of UK Skylark Populations Using Life-History and Individual-Based Landscape Models , 2005, Ecotoxicology.

[79]  W. Z. Lidicker,et al.  Levels of organization in biology: on the nature and nomenclature of ecology’s fourth level , 2007, Biological reviews of the Cambridge Philosophical Society.

[80]  U. Kitron,et al.  Upscale or downscale: applications of fine scale remotely sensed data to Chagas disease in Argentina and schistosomiasis in Kenya. , 2006, Geospatial health.

[81]  F. Raoul,et al.  Spatial distribution of metals in smelter-impacted soils of woody habitats: influence of landscape and soil properties, and risk for wildlife. , 2010, Chemosphere.

[82]  Kenichi Takahashi,et al.  Transmission Ecology of Echinococcus multilocularis in Wildlife : What Can Be Learned from Comparative Studies and Multiscale Approaches? , 2002 .

[83]  M. Johnson,et al.  Accumulation of Lead, Zinc, and Cadmium in a Wild Population of Clethrionomys glareolus from an Abandoned Lead Mine , 2003, Archives of environmental contamination and toxicology.

[84]  A. Butet,et al.  Spatial dynamics of the bank vole (Clethrionomys glareolus) in a fragmented landscape , 1996 .

[85]  R. Stewart,et al.  Use of habitat-contamination spatial correlation to determine when to perform a spatially explicit ecological risk assessment , 2007 .

[86]  B K Hope.  A case study comparing static and spatially explicit ecological exposure analysis methods. , 2001, Risk analysis : an official publication of the Society for Risk Analysis.

[87]  J. Levinton,et al.  Cadmium resistance in an oligochaete and its effect on cadmium trophic transfer to an omnivorous shrimp , 1998 .

[88]  M. Huijbregts,et al.  Spatial variability and uncertainty in ecological risk assessment: a case study on the potential risk of cadmium for the little owl in a Dutch river flood plain. , 2005, Environmental science & technology.

[89]  R. Blust,et al.  Transfer and accumulation of metals in a soil-diet-wood mouse food chain along a metal pollution gradient. , 2007, Environmental pollution.

[90]  R. Leuven,et al.  Heavy-Metal Concentrations in Small Mammals from a Diffusely Polluted Floodplain: Importance of Species- and Location-Specific Characteristics , 2007, Archives of environmental contamination and toxicology.

[91]  D. Blaudez,et al.  Metal Accumulation by Woody Species on Contaminated Sites in the North of France , 2009 .

[92]  M. Farago,et al.  Heavy metal pollution in the vicinity of a secondary lead smelter in the Czech Republic , 1996 .

[93]  L. Buydens,et al.  A Procedure for Incorporating Spatial Variability in Ecological Risk Assessment of Dutch River Floodplains , 2001, Environmental management.