Published: July 19, 2011

r 2011 American Chemical Society 7497 dx.doi.org/10.1021/es200872p | Environ. Sci. Technol. 2011, 45, 7497–7502

ARTICLE

pubs.acs.org/est

Cadmium Accumulation in Small Mammals: Species Traits, SoilProperties, and Spatial Habitat UseNico W. van den Brink,* Dennis R. Lammertsma, Wim J. Dimmers, and Marie Claire Boerwinkel

Alterra, Wageningen UR, PO-Box 47, 6700 AA Wageningen, The Netherlands

’ INTRODUCTION

To assess risks that environmental contaminants may pose towildlife it is essential to get insight into the degree to whichanimals are exposed. In terrestrial ecosystems, wildlife is mainlyexposed to contaminants from the soil, and to a lesser extent toatmospheric or aquatic sources. Soil contaminants are accumu-lated by terrestrial receptors through the diet, or by directingestion of soil.1�3 Several studies have assessed relationshipsbetween concentrations in wildlife and concentrations in the soil,with varying success.4�8 This variable success in relating soilconcentrations directly to concentrations in the organisms is dueto the fact that several other factors may interfere with theaccumulation of environmental contaminants. First, soil proper-ties may affect the bioavailability of, for instance, metals,9,10

which can affect uptake in wildlife.7 Second, age of the animalsmay also influence internal concentrations.11,12 Furthermore,since environmental chemicals are generally accumulated throughthe diet, food web dynamics and diet composition may affectaccumulation patterns significantly.13,14 Factors affecting accu-mulation may vary in time and space (seasonality), so traits ofspecies that govern their spatial and temporal (foraging) behaviormay affect accumulation patterns.15�19

Several modeling studies have focused on the integration ofthese confounding factors in accumulation processes.16,20�22

However, only a few experimental laboratory or field studiesare available in which detailed information on soil concentrationsand properties, diet composition, and spatial habitat use of thereceptors are integrated in an assessment of accumulation ofenvironmental contaminants in terrestrial wildlife.15,23 To over-come this, a study was designed in which accumulation of

cadmium (Cd) from soil to small mammals was related to theirspecies-specific spatial habitat use and diet composition, and tosoil concentrations and properties. Cd accumulation was as-sessed in three different small mammalian species, wood mouse(Apodemus sylvaticus), bank vole (Myodes glareolus) and commonvole (Microtus arvalis), known to have different diet preferencesand spatial habitat use.17,24�27 Spatial habitat use was assessedusing injectable transponders and automated receivers, while dietpreferences were assessed using stable isotope signals of nitrogenand carbon (δ-15N and δ-13C).28

’EXPERIMENTAL SECTION

Study Area. The study area is situated near the village ofRenkum, The Netherlands (51�95058.9200 N, 5�45016.6200 E).The landscape consisted of a mosaic of hedgerows, arable land,forest, and pastures on a sandy soil. Crops grown on the arableland were maize and wheat. Forest was coniferous dominated byScotch-pine (Pinus sylvestris) without a shrub layer, or deciduousforest, dominated by oak (Quercus robur) and birch (Betulapendula). The farmed pastures were abandoned about 10 yearsago and were transformed into meadows with vegetation domi-nated by long grass and herbs (e.g., Holcus lanatus, Taraxacumofficinalis, Rumex acetosella, Senecio jacobea, Agrostis spp., andTrifolium repens).

Received: March 16, 2011Accepted: July 19, 2011Revised: June 21, 2011

ABSTRACT: In this study, the impact of species-specific spatialhabitat use, diet preferences, and soil concentrations and proper-ties on the accumulation of cadmium in small mammals wasinvestigated. The results show that for the woodmouse (Apodemussylvaticus), a mobile species with a large range in diet composition,accumulation of cadmium was not related to local soil concentra-tions or soil properties, but to diet preferences. For the commonvole (Microtus arvalis), a nonmobile, specific feeding species,accumulation of cadmium was related to local soil concentrationsor properties. For the bank vole (Myodes glareolus), a species with asmaller home range than the wood mouse but a broader dietspectrum than the common vole, both local soil properties anddiet appeared to affect the cadmium accumulation in the kidneys.The results of this field study show that species-specific traits of small mammals are important determinants of accumulation ofcadmium on a local scale. For site-specific assessment of risks of contaminants, such information is essential in order to understandexposure dynamics.

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Collection of SmallMammals.Three studies were performedto assess (1) spatial extent of habitat use by the species, (2)habitat preferences of the species, and (3) diet and accumulationassessment.Spatial Extent of Habitat Use. To assess the spatial habitat use

by small mammals, 187 wood mice and 44 bank voles werecaptured in a hedgerow (May 8, 2006�July 17 2007) usingLongworth live traps.29 Only a single common vole could becaptured in this habitat and will not be discussed in thisexperiment. Traps were baited with peanut butter and cat food,and contained hay as bedding. Animals were caught alive in thesetraps and marked individually with a transponder (TROVAN,Identify UK Ltd., Yorkshire, UK). Spatial habitat use wasdetermined by placing receivers at 0, 5, 10, or 15 m from thehedgerow (total 10 receivers) from June 16, 2006 until Novem-ber 29, 2007. Customized single-loop, ring-shaped antennaswith a diameter of 50 cm and height of 10 cm were usedto automatically detect marked animals within close distance(< 20 cm), and the data were stored in a logger (LID650, EIDAalten bv, Aalten, The Netherlands). Per receiver, the totalnumber of animals per day (24 h) could be calculated. Animalsthat were recorded more than once per day were regarded as asingle reading. For each receiver the total number of animals perreceiver per day (no./receiver/day) was calculated per species.

Habitat Preferences. To determine the habitat preferences ofthe small mammals, 32 additional wood mice and 7 bank voleswere captured at different trap lines in different habitats. Animalswere also marked with a transponder and tracked with the similarreceivers as the former experiment, placed in different habitattypes around the trap lines. Animals were detected similarly tothe other experiment.Accumulation Assessment. Twenty-seven wood mice, 13

bank voles, and 7 common voles from the same locations, withan additional location on arable land, were sacrificed in order toassess the cadmium concentrations in their kidneys ([Cd]kidney)and stable isotopes of carbon and nitrogen in the muscles of thehind leg. Only adult specimens were used in order to minimizeage-related variation. Animals were sedated with CO2, andsacrificed by cervical dislocation. All procedures involving thehandling of animals were conducted by certified persons, andreviewed by an Animal Ethics Committee according to Dutchlegislation on the protection and welfare of vertebrate animalsused for experimental and other scientific purposes.At each sampling location, soil samples were collected to assess

the Cd concentrations in the soil ([Cd]soil). Furthermore, dietitems (grass (vegetative parts and seeds), acorn, and earthworm)were collected at random locations for stable isotope analyses.Metal Analysis.Metal analyses were performed according to

ref 7. In short, soil was dried at 40 �C and the kidneys were freeze-dried prior to chemical analysis. Samples were digested withaqua-regia in a microwave in Teflon vessels. Samples wereanalyzed for Cd using inductively coupled plasma atomic emis-sion spectrometer (ICP-AES). When concentrations were belowdetection limits, analyses were performed with inductivelycoupled plasma mass spectrometry (ICP-MS). Limits of detec-tion were 0.012 mg/kg dry weight for the soil and 0.075 mg/kgdry weight for kidney samples. Recoveries were in range of95�111%. All concentrations are reported as dry weight con-centrations, unless stated otherwise. For quality assurance,reference samples from clay and sandy soils were analyzedaccording to criteria of WEPAL (ISE 989, ISE 949, WEPAL,www.wepal.nl). Furthermore, reference liver tissue (BCR-185R,Community Bureau of Reference, the former reference materialsprogram of the European Commission) was analyzed as qualityassurance for the kidneys.DietAssessmentUsingStable IsotopeAnalysis.All samples

were freeze-dried, ground by a ball mill (Retsch MM 2000, RetschGmbH & Co., Haan, Germany) and 13C and 15N enrichment was

Figure 1. Number of observations of animals per receiver at differentdistances of the hedgerow where the animals were caught. (A) woodmouse;(B) bank vole (n/receiver; for 0, 5, and 10 m n = 3 antennas, for 15 m n = 1antenna). (Spring: April�June; Summer: July�September; Fall: October�December; Winter January�March, too low numbers in winter for detailedanalyses). Total number of wood mouse caught: 187; bank voles: 44.

Table 1. Statistical Output for Relationships between Oc-currence ofWoodMice and Bank Vole in Relation toDistanceto Hedgerow, Season, and Species (Figure 1)a

parameter estimate tprob

constant 2.369 p < 0.001

season spring 1.306 p = 0.005

season summer 2.014 p < 0.001

distance �0.4143 p < 0.001

wood mouse �0.524 p = 0.040

distance*wood mouse 0.1974 p = 0.026aGLM-analysis with Poisson as link function;31 significant dependentvariable: occurrence (n/receiver); independent variables: season (Spring(April�June), Summer (July�September), Fall (October�December)),distance, species and interaction distance (m)*species (wood mouse andbank vole); reference: season: Fall, species: bank vole).

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measured after combustion in an elemental analyzer with a con-tinuous flow isotope ratio mass spectrometer (Delta C, FinniganMAT, Bremen, Germany). Data were expressed as atom percent(atom %). As standard for C-enrichment, the VPDB standard wasused, a redefined standard in relation to the PeeDee Belemniteformation (South Carolina, USA).30 For N-enrichment, standardssupplied by the International Atomic Energy Agency (IAEA,Vienna) were used. All reference gases used in the analyseswere obtained directly from IAEA. Isotope ratios are expressed as

δ-values in per mill (%) deviations from the standards. All analyseswere carried out in duplicate.Statistical Analysis. All statistical analyses were performed

with GenStat, version 13 (www.genstat.co.uk). Relationshipsbetween occurrence of small mammals and distance to thehedgerow were analyzed with General Linear Models (GLMs)with a Poisson link function.31 Differences between habitat typesand species in [Cd kidney] δ-

13C and δ-15N and ratios between[Cd]kidney and [Cd]soil were analyzed with Analysis of Variance(ANOVA), with Least Significant Differences (LSD) as posthoctest. Homogeneity of variance was checked with Bartlett’s test,which is rather sensitive for departures from normality; wetherefore also checked residuals posthoc for deviations. Relation-ships between factors governing [Cd]kidney and [Cd]soil wereanalyzed with GLMs. [Cd]kidney and [Cd]soil were log10-trans-formed prior to statistical analyses, but the signals for δ-13C andδ-15N were not.

’RESULTS AND DISCUSSION

Spatial Habitat Use. In Figure 1, the relationship between theoccurrence of marked animals and the distance to the hedgerowin which they were caught is shown. Too few common voles werecaptured for detailed assessment, so data on this species are notincluded in the following analysis. Statistical analysis revealedsignificant effects of distance, season, and species (Table 1). Bankvoles were detected in higher numbers, especially considering thelower number of bank voles captures in this experiment. This ismost pronounced within the hedgerow. Numbers of detectionare lowest in fall, which is likely related to the fact that in springand summer the arable habitat provided more cover and possiblyfood in comparison to fall. In a study on small-scale movementsof wood mice, both cover and food availability were importantdrivers of local spatial habitat use.27 It is evident that numbers ofdetection of marked animals were lower at greater distance fromthe hedgerow. The interaction between species and distance issignificant (p = 0.026) indicating that the wood mouse and bankvole showed different relationships between occurrence anddistance from the hedgerow (Figure 1). Wood mice occurredat relatively higher numbers at greater distance in comparison tothe bank vole. Furthermore, marked wood mice were detected atlower frequency than bank voles, which would imply that a higherproportion of the captured wood mice were outside the area

Figure 2. Number of wood mice (A) and bank voles (B) caught indifferent habitat types in different seasons in different habitat types (n/receiver/day; note different scales between A and B).

Figure 3. Biplot of δ-13C and δ-15N (%; averages and standarddeviations) of the three small mammal species (filled dots) and somemajor diet items (open dots).

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covered by the receivers. Woodmice were detected in all habitats(Figure 2), while bank voles only showed up in habitats withcover: long grass, shrubs, open forest, and hedgerow (arable sitesnot included in this experiment). The total number of woodmicemarked in this experiment was greater than bank voles, which isreflected in the number of detection of marked animals. Withinhedgerows, bank vole numbers were in the same range as those ofthe wood mouse; for the other habitat types the number of bankvoles wasmuch lower in comparison to the woodmouse (note thedifferent scales in the two figures). The results show that woodmice appeared to occupy larger areas and are less strict in theirhabitat preferences. This is in confirmation with refs 32 and 33who deduced larger home ranges for wood mouse in comparisonto the bank vole in similar habitats. The common vole was onlydetected in two habitats, short grass and arable land, indicating arestricted distribution, which is in agreement with ref 33. Thesefindings indicate species-specific use of the habitat, which mayaffect the potential of the different species to accumulate Cd.20

Species-Specific Diet. Accumulation patterns may be relatedto the diet of the animals in the different habitats, because preyspecies and vegetation may show habitat-specific availability.34

Because accumulation efficiency can differ among soil inverte-brate species in different habitats,35 habitat-specific diets, re-flected in the stable isotope signal, may have a big impact on theaccumulation patterns. Figure 3 shows the biplot of δ-13Cand δ-15N in the muscles of the small mammal species and somediet items. There are significant differences between species andhabitats in δ-15N and δ-13C (Table 2; δ-15N: Species Fprob =0.005, habitat: Fprob < 0.001;δ-13C: Species Fprob < 0.001,Habitat Fprob = 0.003, ANOVA). Species are separated byδ-13C (common vole versus wood mouse and bank vole) andalso by δ-15N (bank vole versus common vole and wood mouse,Figure 3). Trophic transfer of diet items results in enrichment ofthe δ-13C and δ-15N signals,36,37 on average 0.5�1% for δ-13Cand 3.5% for δ-15N. When applying an average increase of 0.75for δ-13C and 3.5 for δ-15N it becomes evident that the isotopesignal in common voles indicates vegetative grass as a major dietitem (Figure 3). For the woodmouse, the isotope signal indicatesacorn and earthworm as potential diet items, while grass seedsand/or earthworm appear to be important in the diet of the bankvole. For the bank vole and wood mouse the variation in theisotope signal was rather high (Table 2), indicating high variancein diet composition for these species. This is in agreement withWatts,24 who reports for both the wood mouse and bank vole inwoodland edge habitat, a wide range of diet items includinganimals, but a preference of the wood mouse for seeds and thebank vole for vegetative parts. The common vole showed littlevariation in both δ-13C and δ-15N indicating a narrow diet.Accumulation of Cadmium and Relationships with Soil

Concentrations, Soil Properties, and Stable Isotopes. [Cd]soilranged from 0.06 to 0.44 mg/kg dry weight (mean: 0.26, standard

deviation: 0.14mg/kg), kidney concentrations variedmore than 2orders of magnitude (range: 0.08�14.4 mg/kg dry weight, mean4.0, standard deviation: 3.1 mg/kg). Cadmium concentrationswere significantly lower in kidneys of the common vole incomparison to the other species (ANOVA, p < 0.001). Kidneyconcentrations are similar to the ones found in small mammalsfrom Dutch river floodplains,7,15 although in the latter study theconcentrations in the bank vole were somewhat lower. Whencombining all species, log([Cd]kidney) was positively related toδ-13C, and negativelyrelated toδ-15N (GLM, p< 0.001, Figure 4).This is most likely related to a relative high proportion ofearthworm in the diet, a diet item with relatively high Cdconcentrations7, and a relatively high δ-13C but low δ-15N signal(Figure 3). Habitat type, log([Cd]soil), and pH were droppedfrom the analyses because their effects were not significant.Average [Cd]kidney in the wood mouse was highest at the

meadow locations in comparison to forest and arable land,resulting in high ratios between [Cd]kidney and [Cd]soil for thatspecies in the meadow (Table 3). This was similar for the bankvole, which indicates that accumulation patterns differed among

Table 2. δ-C and δ-N % in Different Small Mammal Species in Different Habitats (%)a

δ-15N (%) δ-13C (%)

wood mouse bank vole common vole wood mouse bank vole common vole

arable 2.87( 3.09 2.40 20.24( 0.23 �25.56( 1.76 �30.21 �29.75( 0.52

forest 1.00( 2.69 �1.72( 1.64 �25.87 ( 1.18 �26.72( 1.29

meadow �0.41( 1.3 �3.78( 0.77 �25.34( 0.79 �26.78( 0.21aAverage ( standard deviation, in case of lacking standard deviation just one observation is available.

Figure 4. Relationships between [Cd]kidney and δ-C (A) and δ-N(B) (mg/kg dry weight). All species and habitat types included inregression line.

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habitats. Within the arable habitat, the accumulation of Cd issignificantly higher in the wood mouse in comparison to thecommon vole (Table 3), indicating additional species specificaccumulation patterns, irrespective of [Cd]soil. In meadows with highCd accumulation, the δ-15N signal in wood mice and bank voles wassignificantly lower than in the other habitats. Similarly, the δ-15Nsignal in wood mice from arable was also lower than in the commonvole,whichwas also related to an increased accumulationof cadmium.Apparently, cadmium accumulation was most efficient on a diet withlow δ-15N, i.e., with grass seeds or earthworm (Figure 3). Sinceearthworm generally contain much higher [Cd] in comparison tograss seeds,7 it is likely that effects of the decrease in δ-15N in themeadow on the increase in [Cd]kidney was caused by an increase ofearthworms in the diet. However, it should be noted that the currentstudy was not focused on a full analysis of the diet of the differentspecies, but merely uses stable isotopes as a proxy of the diet, withreference to samples of diet items. Hence, the focus was on a fewgeneral food items (acorns, vegetation, and seeds24,25) and on anitemwith relatively high Cd concentrations (earthworms). But, forinstance, insects and fruits and berries were not included, althoughthese items may also be important in the diets.25 The fact thatδ-15N relates well with accumulation efficiency does imply aneffect of diet composition on the accumulation of cadmium.However, the conclusion on which diet item causes this relation-shipmay not be conclusive without further study. Additionally, thepH is low in the soils from the forest locations (3.9 in forestcompared to 4.4 in meadow and 5.8 in arable land), which maycause the availability of Cd to increase,10,38 resulting in a relativelyhigh ratio between [Cd]soil and [Cd]kidney in forest habitat.When analyzing data for the individual species, different factors

affect [Cd]kidney in a species specific way. [Cd]kidney in commonvoles was significantly lower than in the other two species,and significantly negatively related to log([Cd]soil) and to pH(ANOVA for both: p = 0.010, 72% explained variance) but not toeither δ-13C or δ-15N. This species was caught at only two traplocations, with different [Cd]soil and pH. Because [Cd]soil and pHwere confounded, it is impossible to separate these factorsstatistically. Since a negative relationship between [Cd]kidney andpH can be explained by an increase of the bioavailability ofCd at lower pH,39 it is likely that this was the most importantfactor regulating [Cd]kidney in common voles. In case of the woodmouse, δ-13C and δ-15N were significantly related to [Cd]kidney(Multiple linear regression: δ-13C: p = 0.002, δ-15N: p < 0.001,percentage variance accounted for 55%), indicating a majorinfluence of the diet on the accumulation patterns in this species.For the bank vole, [Cd]kidney was significantly related to δ-

15Nand pH (multiple linear regression, pH: = p 0.017, δ-15N: p <0.001), indicating influence of both diet and soil properties. Theresults show that [Cd]soil or soil properties are not indicative for

kidney concentrations in mobile species like the wood mouse.This species spatially integrates cadmium over a larger area, andconsumes a wider range of diet, which varies among habitats. Incase of the bank vole, an intermediate mobile species with asimilar range in diet to the wood mouse, both diet and pH are ofimportance. This indicates that for this less mobile species, local soilproperties affect [Cd]kidney, combined with the habitat specific diet.The common vole is least mobile, and shows a very narrow range indiet. For this species, local soil properties (likely pH) were govern-ing [Cd]kidney. However, for this species sampleswere only analyzedfrom animals from arable land, which may account for the narrowrange in diet. This may possibly lead to an underestimation of theimportance of diet in this species. However, if only woodmice fromarable locations are used in the statistical analyses, just δ-15N andδ-13C are significantly related to [Cd]kidney (poverall: 0.042, pδ-N:0.019, pδ-C: 0.038, linear regression, percentage variance accountedfor: 48%), similar to the results based on full data set on woodmice.The significance of the relationship is somewhat lower in compar-ison to the full data set, which is related to the lower degree offreedom, the percentage accounted is similar (55% versus 48%).This illustrates the importance of diet on the accumulation ofcadmium to the wood mouse, even in single habitats.The results of this study clearly illustrate that accumulation ofCd is

affected by species traits in a logical manner. Local soil properties aremost important for predicting Cd accumulation in the nonmobilespecies, while diet composition predicted Cd accumulation for thespecies with a variable diet. However, it should be noted that this isscale dependent, and depending on the variation in [Cd]soil and soilproperties.On a larger spatial scale for instance, it has been shown that[Cd]soil may be predictive for Cd levels in kidneys and liver of smallmammals,8,40 although this can be hampered by differences inavailability of cadmium.7 It has also been suggested that differencesin feeding behavior of animals among sites may be of importance.41

The current study experimentally validates this finding, and it may beconcluded that in addition to soil concentrations and soil properties,species traits affecting the habitat use of small mammals and their dietpreferences can be of prime importance when assessing exposure ofsmall mammals to cadmium.

’AUTHOR INFORMATION

Corresponding Author*E-mail: nico.vandenbrink@wur.nl.

’ACKNOWLEDGMENT

Field work of this study was funded by Ministry of EconomicAffairs, Agriculture and Innovation, coordinated by Bas Volkers(project BO-02-011-007). Further funding was obtained fromthe INSPECT project funded by the SNOWMAN network(www.snowmannetwork.com) and Ministry of Economic Af-fairs, Agriculture and Innovation (project KB-01-015-014-ALT).Leon de Jonge (Wageningen University) analyzed the stableisotope. We are grateful to the Dutch State Forestry Servicefor access to their properties and to Dick Belgers (Alterra,Wageningen UR) for his support.

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