a comparison of cadmium in ecosystems on metalliferous mine tailings in wales and ireland

A COMPARISON OF CADMIUM IN ECOSYSTEMS ONMETALLIFEROUS MINE TAILINGS IN WALES AND IRELAND

A. MILTON1, J. A. COOKE2∗ and M. S. JOHNSON1

1 School of Biological Sciences, Life Sciences Building, University of Liverpool, Liverpool, UnitedKingdom; 2 School of Life and Environmental Sciences, University of Natal, Durban, South Africa

(∗ author for correspondence, e-mail: [email protected], Fax: +27 312 602 029)

(Received 6 August 2002; accepted 7 October 2003)

Abstract. A comparative study of the concentrations of cadmium in ecosystems developed ontailings from lead/zinc mines was undertaken. Mine soils, vegetation, ground-dwelling invertebratesand Apodemus sylvaticus from nine historic and abandoned mines in Wales and a modern Irish minesite were sampled in order to evaluate and compare exposure risks to wildlife. There were three highsoil cadmium sites (155–300 mg kg−1) all from north-east Wales sites, one intermediate site (21 mgkg−1) the Irish mine tailings, with the other sites having low (background) cadmium levels. Thecadmium levels reflected differences in ore minerology and in particular the presence of the zinc ore,sphalerite. The highest plant and invertebrate cadmium levels generally occurred in the three high soilcadmium sites. However, occasional high levels were found in plant and invertebrate samples fromone or more of the low cadmium sites. Of particular significance was, despite the relatively highsoil cadmium, the very low cadmium concentrations in the plants and invertebrates from the Irishtailings. Evidence of food-chain transfer and even biomagnification in invertebrates did not lead tohigh cadmium levels in kidneys of A. sylvaticus. Only at one high site were the kidney cadmiumresidues significantly higher than the reference site.

Keywords: Apodemus sylvaticus, cadmium, ecotoxicology, food chains, invertebrates, mine tailings

1. Introduction

Anthropogenic cadmium derives from a variety of sources including metal smelt-ing, use of sewage sludge on land, burning of fossil fuels, rock phosphate fertilisersand waste disposal (Nriagu, 1979; Hutton, 1983; Jackson and Alloway, 1992; Shoreand Douben, 1994). Mining wastes remaining after the recovery of target metalsare also important sources of environmental cadmium and can contain residualconcentrations of cadmium that, in some cases, reach environmentally toxic levelsand pose an environmental hazard (Johnson et al., 1994). The stabilisation of tail-ings is therefore essential to prevent dispersal of the material on to adjacent land orinto local watercourses, and is generally the main objective of mine waste reclam-ation (Johnson et al., 1994). One widely used and successful method of tailingsreclamation is the establishment of grassland which, with proper management, willstabilise the tailings and reduce the visual impact (Johnson et al., 1994).

The concentration of cadmium has been measured in contaminated ecosystemsincluding mine tailings, and the areas around smelters and metal works (Johnson

Water, Air, and Soil Pollution 153: 157–172, 2004.© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

158 A. MILTON ET AL.

et al., 1978; Andrews and Cooke, 1984; Hunter et al., 1987a–d; Cooke et al.,1990). Cadmium is taken up from contaminated soil by plants and translocatedto the shoots. Transfer through the food chain occurs and exposure to animals ismainly via the diet. Cadmium reaches plant concentrations of concern becauseof the consequences of animal toxicity through exposure via the food chain. Thephytotoxicity threshold is often much greater (McLaughlin et al., 2000). Mammalsand birds eliminate cadmium slowly and bioaccumulation in target organs, espe-cially kidney and liver occurs. Critical concentrations in kidney and liver can helpthe toxicological interpretation of data derived from field samples when comparedwith critical concentrations derived experimentally (Talmage and Walton, 1991;Shore and Douben, 1994; Cooke and Johnson, 1996; Furness, 1996). However,such an approach must take into account the environmental factors to which wildanimals are exposed as these can modify the toxicological responses observedunder laboratory conditions (Dodds-Smith et al., 1992).

This study compares the environmental significance of cadmium at nine historicand abandoned Welsh lead/zinc mine sites and a typical modern tailings facility ata lead/zinc mine in the Republic of Ireland (WDA, 1978; Brady, 1993; Milton etal., 2002). The primary aim was to determine the ecotoxicological cadmium riskin the context of these sites being colonised by wildlife and the potential effect ofcadmium on ecological processes such as decomposition. A second aim was thecomparison of the modern site in Ireland with the much older abandoned sites.This sought to inform the restoration practice currently in operation at the modernsite, in terms of the production of a sustainable low-maintenance grassland and thepotential impacts residual cadmium may have in realising this goal. Lead is alsoa significant zootoxic contaminant of these mine sites and wastes and has beenconsidered in a separate paper (Milton et al., 2002).

2. Materials and Methods

Full details of the sampling sites, methods of sampling and chemical analysis aregiven in Milton et al., (2002). Field sampling was conducted in the late summerand autumn of 1995. Surface spoil (0–10 cm) samples were collected, dried, sieved(1 mm) and sequentially extracted with 10 mL of double distilled water (DDW),0.5 M ethanoic acid and concentrated nitric acid. A range of vegetation sampleswere collected from the Welsh mine sites, including the dominant grasses, com-posite ground cover vegetation, plant litter and seeds of herbaceous and woodyspecies. Invertebrates were collected using pitfall traps. The terrestrial gastropods,Arion ater and Cepaea nemoralis, and adult (5th instar) common field grasshoppers(Chorithippus brunneus), were collected manually from each site. Vegetation andlitter were collected as small (2–15 g wet wt.) bulk samples, oven-dried (48 hr,80 ◦C), then ground to pass a 0.5 mm screen. Gastropods were allowed to passivelyevacuate their alimentary tract, bulked to give three replicates of six specimens

CADMIUM IN MINE WASTE ECOSYSTEMS 159

of each species, and then homogenised before acid digestion. Grasshoppers weredigested individually after oven drying. Only species of invertebrate present atseveral sites, and in sufficient numbers for statistical analysis, had their metal con-centrations determined. Adult specimens of woodmice, Apodemus sylvaticus, werecollected using baited live traps, killed and immediately frozen. The liver, kidney,muscle and bone (femur) were excised and analysed as well as the residual carcass.A. sylvaticus was the commonest small mammal and present at all sites except one,Rhosesmor.

All biological samples were subjected to acid digestion, involving overnightcold dissolution in concentrated HNO3, followed by boiling at 120 ◦C for 2 hr. Soilextracts and acid digests were analysed for metals using flame atomic absorptionspectrometry (AAS), matrix-matched calibration standards and deuterium back-ground correction for non-atomic absorption. Seed, invertebrate and small mammaltissue digests were analysed by graphite furnace atomic absorption spectrometry(GFAAS) (Varian 600AA spectrophotometer with a GTA 100 graphite furnace andPSD 100 autosampler), using the L’vov platform furnace technique (Milton et al.,1998; Milton et al., 2002). All glassware was acid-washed and Quality Assurancewas provided by running double blanks and certified reference materials (CRMs)within all sample batches (Milton et al., 2002). Mammal tissue results were conver-ted from wet to dry weight concentrations using pre-determined conversion factors(carcass, 2.72; kidney, 3.69; liver, 3.67; muscle, 3.83). Gastropod concentrations ofcadmium were similarly converted to dry weight using a factor of 6.8.

Arithmetic means and the Standard Error of the Mean (SEM) for each datasetwere calculated using Microsoft EXCEL. Where appropriate, datasets were sub-jected to One Way Analysis of Variance (ANOVA), using site as the effect factor.Datasets that demonstrated skewness or had a large heterogeneity of variance werenormalised with a log10 transformation prior to ANOVA and are indicated in theresults tables. A Tukeys-Kramer test was used for comparison between sites foreach sample type (Day and Quinn, 1989). Values of half the sample detection limit,under the operating conditions of the instrument (FAAS = 0.05 µg g−1; GFAAS =0.37 ng g−1), were substituted in statistical analysis where necessary. All data fromthe present study and research referenced for comparative purposes are presentedon a dry weight basis unless stated otherwise.

3. Results

3.1. SOIL

Concentrations of cadmium in mine waste extracts are shown in Table I. The ref-erence site values were similar to or lower than those reported previously for soilsfrom other unpolluted sites (Jackson and Alloway, 1992; Shore, 1995). The totalconcentration of cadmium for the Irish tailings derived as the sum of the sequential


TABLE I

Concentration of cadmium in surface soilsa (mg kg−1 dry wt. ± SEM) from the referenceand mine sites

Site n Double distilled H2O 0.5 M CH3COOH Concentrated HNO3

Reference 7 <0.01 <0.01 0.3 ± 0.05

Cwmerfin 4 0.03 ± 0.02 0.38 ± 0.14 0.8 ± 0.13

Grogwnion 4 <0.01 0.10 ± 0.04 2.1 ± 0.27

Cwmsymlog 5 <0.01 0.16 ± 0.07 1.5 ± 0.29

Frongoch 4 <0.01 0.23 ± 0.07 0.9 ± 0.17

Cwmrheidol 4 0.03 ± 0.02 <0.01 1.1 ± 0.24

Ystum Tuen 4 0.03 ± 0.02 0.07 ± 0.01 1.2 ± 0.10

Rhosesmor 4 0.33 ± 0.10 39 ± 6.0∗∗∗ 260 ± 27∗∗∗Trelogan 4 1.5 ± 0.26∗∗∗ 48 ± 2.5∗∗∗ 221 ± 20∗∗∗East Halkyn 4 0.47 ± 0.21 28 ± 11.1∗∗∗ 126 ± 44∗∗∗Irish tailings 10 <0.01 6.5 ± 0.50∗∗∗ 15 ± 1.9∗∗∗

a ANOVA computed on log10 transformed data.∗∗∗ Denotes significant difference from reference site at p < 0.001.

extractions (21.5 mg kg−1) was very similar to that reported previously (19–36 mgkg−1) for the same site (Brady, 1993). Cadmium concentrations indicate a geo-graphically based separation of the Welsh sites, with those in the north-east of thecountry (Rhosesmor, Trelogan and East Halkyn) exhibiting the highest concentra-tions of cadmium in all extracts, with total concentrations in the range 155–300 mgkg−1. Mine sites in west Wales were not significantly different from the referencesite (p > 0.05).

Statistically, only Trelogan contained significantly elevated levels of water sol-uble cadmium compared to the reference site. The ethanoic and nitric acid extract-able fractions generated very similar ranking of sites with Trelogan, Rhosesmor,East Halkyn and the Irish tailings having very significantly elevated values withrespect to the reference site (p < 0.001). These same three sites from north-eastWales also recorded significantly higher cadmium levels than the Irish tailings(p < 0.001) whereas all the other sites were significantly lower than the Irishtailings (p < 0.001).

3.2. VEGETATION AND LITTER

The concentrations of cadmium in vegetation and litter are summarised in Table II.Reference site values for cadmium in a range of plant materials have been reportedas 0.44–0.63 mg kg−1 (Hunter et al., 1987a). The concentrations of cadmium re-ported here for vegetation from the Irish tailings were much lower (<0.01 mg kg−1)


TABLE II

Concentration of cadmium in plants and litter from the reference and mine sites (mg kg−1 drywt. ± SEM)

Site Festuca rubra Agrostis spp. Composite Litter Composite

ground cover seeds

Reference 0.09 ± 0.08 0.25 ± 0.001 0.01 ± 0.0 <0.01 0.04 ± 0.01

(3) (3) (9) (6) (14)

Cwmerfin 0.01 ± 0.0 0.17 ± 0.08 0.12 ± 0.07 0.42 ± 0.19 0.08 ± 0.03

(3) (3) (9) (5) (12)

Grogwnion 0.17 ± 0.08 0.17 ± 0.16 1.3 ± 0.30 1.6 ± 0.54 0.13 ± 0.06

(3) (3) (6) (6) (9)

Cwmsymlog 0.25 ± 0.001 0.17 ± 0.06 1.0 ± 0.52 0.08 ± 0.04 0.11 ± 0.03

(4) (4) (8) (8) (12)

Frongoch 0.17 ± 0.08 0.09 ± 0.08 3.1 ± 1.2∗∗ 0.71 ± 0.08 0.13 ± 0.06

(3) (3) (9) (6) (9)

Cwmrheidol 0.13 ± 0.07 0.76 ± 0.14 0.77 ± 0.19 1.3 ± 0.13 0.28 ± 0.03

(4) (4) (12) (8) (3)

Ystum Tuen 0.18 ± 0.17 0.01 ± 0.0 1.2 ± 0.17 <0.01 0.24 ± 0.08

(3) (3) (4) (6) (4)

Rhosesmor 0.09 ± 0.08 0.17 ± 0.16 3.7 ± 1.0∗∗ 3.1 ± 0.12 0.71 ± 0.24∗(3) (3) (4) (4) (9)

Trelogan 1.4 ± 0.19∗∗∗ 1.3 ± 0.43∗∗∗ 6.4 ± 1.6∗∗∗ 23 ± 10∗∗∗ 0.93 ± 0.31∗∗∗(3) (3) (4) (4) (12)

East Halkyn 0.50 ± 0.001 0.33 ± 0.08 3.1 ± 1.2∗∗ 1.6 ± 0.23 0.17 ± 0.09

(3) (3) (6) (6) (12)

Irish Tailings <0.01 <0.01 <0.01 <0.01 <0.01

(6) (3) (8) (4) (9)

Replication (n) in parentheses.∗, ∗∗ and ∗∗∗ denote significant difference from reference site at p < 0.05, p < 0.01 and p <

0.001, respectively.

than reported previously for the same site (0.14–0.43 mg kg−1) (Brady, 1993), aswell as being very low by comparison with reported values for clean sites.

The levels of cadmium within the various vegetation components of the mineecosystems were variable with either litter or composite ground cover having thehighest values with Festuca rubra, Agrostis spp. or composite seeds the lowestvalues. Substrate levels of cadmium were, in general, reflected in values for ve-getation with the highest concentrations found in samples from sites in north-eastWales (Rhosesmor, Trelogan and East Halkyn). Trelogan was the only site whereall the categories of vegetation collected were significantly elevated with respect tothe reference site (p < 0.05). Composite ground cover from Frongoch, Rhosesmor


TABLE III

Concentration of cadmium in herbivorous and detritivorous invertebratesfrom the reference and mine sites (mg kg−1 dry wt. ± SEM)

Site A. aulica C. brunneus A. ater C. nemoralis

Reference 0.2 ± 0.1 0.1 ± 0.02 1.6 ± 0.3 2.3 ± 0.2

(6) (5) (3) (3)

Cwmerfin 0.5 ± 0.1 0.2 ± 0.06 0.7 ± 0.3 1.9 ± 0.4

(5) (8) (4) (3)

Grogwnion NT 0.2 ± 0.02 NT 2.2 ± 0.1

(4) (3)

Cwmsymlog NT 0.2 ± 0.02 1.0 ± 0.1 1.8 ± 0.4

(11) (5) (4)

Frongoch 0.8 ± 0.4 0.2 ± 0.02 2.2 ± 0.3 2.1 ± 1.0

(5) (7) (5) (6)

Cwmrheidol 2.7 ± 0.6 0.3 ± 0.04 3.3 ± 0.9 13 ± 0.2∗∗∗(7) (8) (4) (3)

Ystum Tuen NT 0.2 ± 0.05 1.2 ± 0.2 NT

(4) (3)

Rhosesmor NT 1.1 ± 0.2∗∗∗ 4.0 ± 0.3 NT

(5) (3)

Trelogan 38 ± 9∗∗∗ 0.8 ± 0.1∗∗∗ NT 13 ± 1.8∗∗∗(5) (8) (3)

East Halkyn 3.9 ± 0.6 1.4 ± 0.3∗∗∗ 6.6 ± 1.1∗∗ 6.9 ± 0.8∗∗∗(6) (4) (3) (4)

Irish Tailings 0.3 ± 0.06 0.3 ± 0.04 2.9 ± 1.4 2.2 ± 0.3

(8) (10) (5) (9)

NT = Not trapped or biomass too low for analysis.Replication (n) in parentheses.∗∗ and ∗∗∗ denote significant difference from reference site at p < 0.01 andp < 0.001, respectively.

and East Halkyn, and composite seeds from Rhosesmor, were also elevated withrespect to the reference site.

3.3. INVERTEBRATES

Table III summarises the concentrations of cadmium in herbivorous and detritivor-ous invertebrates. Overall the cadmium concentrations in these invertebrates weregenerally only higher from the three north-east Wales sites. All the three speciesfound at Trelogan (Amara aulica, Chorithippus brunneus and Cepaea nemoralis)were significantly elevated with respect to the reference site (p < 0.001). C.


TABLE IV

Concentration of cadmium in carnivorous invertebrates from thereference and mine sites (mg kg−1 dry wt. ± SEM)

Site F. nigrita P. mirabilus O. parietinus

Reference 0.8 ± 0.2 NT 2.5 ± 0.1

(22) (5)

Cwmerfin 2.2 ± 1.2 NT 3.8 ± 1.3

(6) (4)

Grogwnion 1.1 ± 0.5 27 ± 9.8 NT

(5) (8)

Cwmsymlog NT 5.2 ± 1.3 4.5 ± 2.8

(7) (3)

Frongoch 0.7 ± 0.02 3.5 ± 0.5 3.9 ± 1.3

(3) (11) (3)

Cwmrheidol 9.3 ± 3.6∗∗∗ 29 ± 8.9 NT

(7) (5)

Ystum Tuen 0.6 ± 0.2 12 ± 3.6 NT

(4) (5)

Rhosesmor NT NT NT

Trelogan NT 77 ± 25 NT

(3)

East Halkyn 3.6 ± 0.8 47 ± 25 NT

(4) (6)

Irish Tailings 0.5 ± 0.07 1.8 ± 0.4 2.0 ± 0.2

(22) (6) (3)

NT = Not trapped or biomass too low for analysis.Replication (n) in parentheses.∗∗∗ Denotes significant difference from reference site at p <

0.001.

brunneus from Rhosesmor and East Halkyn, and C nemoralis from Cwmrheidoland East Halkyn, also showed elevated cadmium with respect to the reference site(p < 0.001). Only at East Halkyn did Arion ater record levels of cadmium abovethe reference site (p < 0.01).

The concentrations of cadmium in grasshoppers were similar to those reportedpreviously for control animals with only those taken from the north-east Walessites approaching levels for animals from contaminated sites elsewhere (Hunter etal., 1987d). In general, grasshopper concentrations from the Welsh and Irish minesites were lower than those reported previously for metal contaminated sites, albeitsmelter as opposed to mine sites (Hunter et al., 1987b; Rabitsch, 1995a, b).


TABLE V

Cadmium concentrations in tissues of Apodemus sylvaticus from contaminated andreference sites (mg kg−1 dry wt. ± SEM)a

Site n Liver Kidney Bone Muscle

Reference 8 0.30 ± 0.11 1.1 ± 0.45 0.18 ± 0.02 0.02 ± 0.004

Cwmerfin 6 0.25 ± 0.09 0.7 ± 0.17 0.30 ± 0.10 0.01 ± 0.002

Grogwnion 5 0.42 ± 0.04 1.9 ± 0.42 0.25 ± 0.06 0.03 ± 0.009

Cwmsymlog 4 0.54 ± 0.15 1.4 ± 0.43 0.16 ± 0.07 0.02 ± 0.005

Frongoch 4 0.72 ± 0.10 1.7 ± 0.31 0.22 ± 0.07 0.02 ± 0.003

Cwmrheidol 5 0.83 ± 0.35 4.8 ± 2.2 0.19 ± 0.05 0.02 ± 0.003

Ystum Tuen 5 0.44 ± 0.04 1.8 ± 0.83 0.13 ± 0.02 0.01 ± 0.001

Trelogan 8 0.67 ± 0.11 2.7 ± 0.36 0.39 ± 0.05 0.01 ± 0.001

East Halkyn 8 3.0 ± 1.7∗ 13 ± 10∗ 0.21 ± 0.13 0.02 ± 0.008

Irish tailings 11 0.22 ± 0.05 0.95 ± 0.32 0.27 ± 0.07 0.02 ± 0.004

a Excluding Rhosesmor mine where no animals were caught.∗ Denotes significant difference from reference site at p < 0.05.

A similar picture to the herbivorous/detritivorous invertebrates was also prob-ably the case for the data set for three carnivorous invertebrates. However, theabsence of Pisaura mirabilus from the reference site and the absence of all threespecies from Rhoesmor and two of the species from Trelogan makes meaning-ful comparisons difficult (Table IV). The wolf spider, Pisaura mirabilus, fromTrelogan and East Halkyn had the highest cadmium levels which were consid-erably higher than Irish tailings (p < 0.01). F. nigrita and Pisaura mirabilusfrom Cwmrheidol were also elevated compared to the reference or Irish tailingssites (p < 0.001). There were no significant between-site differences in cadmiumfor the common harvestman Opilione parietinus (p > 0.05) although this spe-cies was trapped at only five locations and these excluded the highest cadmiumcontaminated sites in north-east Wales.

3.4. Apodemus sylvaticus

Cadmium concentrations in the tissues of A. sylvaticus are summarised in Table V.The pattern of tissue accumulation was: kidney > liver > bone > muscle. The cad-mium concentrations in the liver and kidney of A. sylvaticus from the referencesite were within ranges reported previously for animals from uncontaminated sites,namely 0.5–0.9 and 1.7–2.2 mg kg−1 (dry wt.) respectively (Talmage and Walton,1991). These quoted ranges encompass all animals from sites used in this studyexcept for those from East Halkyn in respect of liver and kidney, and those fromCwmrheidol and Trelogan in respect of kidney cadmium concentrations. Liverand kidney cadmium concentrations for animals trapped at East Halkyn showed


TABLE VI

Estimated daily cadmium intake by A.sylvaticus (µg day−1 ± SEM)

Site n Cd intake

Reference 8 0.5 ± 0.03

Cwmerfin 6 0.9 ± 0.1

Grogwnion 5 1.1 ± 0.1

Cwmsymlog 4 1.0 ± 0.04

Frongoch 4 1.0 ± 0.05

Cwmrheidol 5 3.8 ± 0.6

Ystum Tuen 5 1.2 ± 0.1

Trelogan 8 27 ± 1.9∗∗∗East Halkyn 8 7.0 ± 0.6∗∗∗Irish Tailings 11 1.3 ± 0.2

∗∗∗ Denotes significant difference fromreference site at p < 0.001.

the only significant between-site differences within the dataset, with the valueselevated with respect to the reference site (p < 0.05).

In view of the similarities in vegetation at the Welsh mine and reference sitea common dietary component model was adopted. However, the very differentflora colonising the Irish tailings dam meant that a separate model was needed toaccommodate the reduced floristic diversity. For the reference site and the Welshmine sites, the diet model advocated by Hunter et al. (1987c) (60% seed, 30% grassand 10% invertebrate material) was adopted. A similar, predominantly grass-baseddiet, was assumed for animals on the revegetated Irish tailings (45% seed, 50%grass and 5% invertebrate material) based on the diet of A. sylvaticus describedby Rogers and Gorman (1995), and Halle (1993). In addition to the three foodcomponents of the diet (seeds, grass, and invertebrates) incidental soil ingestioncan comprise a significant proportion (ca. 2%) of the diet (Beyer et al., 1994; Erryet al., 2000). An estimate of Cd intake from soil was also included into the dietarymodel. The intake of all four dietary components was based on body weight.

These models were then used to estimate the daily dietary intake of cadmium foranimals feeding exclusively at the sites (Table VI). Estimates of cadmium intakewere significantly greater for animals inhabiting the north-east Wales sites than forboth the reference and Irish tailings sites (p < 0.001).


4. Discussion

Of the sites sampled there were three high soil cadmium sites (155–300 mg kg−1)all from north-east Wales sites (Rhosesmor, Trelogan and East Halkyn), one inter-mediate site (21 mg kg−1) the Irish mine tailings, with the other sites having low(background) cadmium levels. The distinct geographic grouping of the Welsh minesites, with high cadmium concentrations in north-east Wales and low values in westWales, can be attributed to the regional mineralogy of the target ores (Johnson etal., 1978). These four high/intermediate cadmium sites had concentrations con-siderably greater than the Dutch critical soil concentrations for grasslands (2–3 mgkg−1) and ecotoxicity (12 mg kg−1) although these are calculated for a standard soil(25% clay and 10% organic matter) rather than mine wastes (De Vries and Bakker,1996; McLaughlin et al., 2000). The ethanoic acid extractable cadmium concen-trations, which followed the same site pattern as the total values, were higher thanthese ‘thresholds’ at the north-east Wales sites (28–48 mg kg−1).

The highest plant values occurred in samples from the high soil sites in north-east Wales. However, occasionally the ‘low’ soil cadmium sites had high plantconcentrations. For example the range of values for composite ground cover was3.1–6.4 mg kg−1 at the ‘high’ sites yet Frongoch, a ‘low’ site, had 3.1 mg kg−1.Perhaps the most significant finding was the extremely low values of plant cad-mium at the Irish tailings site. The section of the tailings surface investigatedwas undergoing zero-maintenance although initial management had been intensewith regular application of fertilisers and mushroom compost (Brady, 1993). Theseamendments may have imposed changes in the speciation and behaviour of cad-mium (Livens, 1991). Even though critical concentrations for cadmium in planttissue have been quoted as in the range 3–10 mg kg−1 (Balsberg Pählsson, 1989),cadmium phytotoxicity is thought unlikely to be a factor in the plant populationdynamics of these mine sites, nor a cause of the typically poor vegetative cover ofthe abandoned Welsh mine sites.

In sustainable land revegetation terms the important effects of cadmium areprobably through accumulation in soil invertebrates and effects on the processesof decomposition of plant litter. A recent investigation into decomposer basidio-mycetes and toxic elements found that cadmium was the most toxic of the suiteof metals tested (Hoiland, 1995). Reduced biomass and species diversity have alsobeen reported in cadmium-contaminated soils (Tyler et al., 1989). In general terms,live vegetation standing crop cadmium concentrations greater than 3 mg kg−1 andlitter values greater than 5 mg kg−1 have been associated with significant foodchain transfer of cadmium to invertebrates (Hunter and Johnson, 1982; Andrewsand Cooke 1984). Critical concentrations in litter and soil humus layers of 3.5 mgkg−1 and 10 mg kg−1 for microbiota and invertebrates respectively, have beengiven for forest soils (Bengtsson and Tranvik, 1989; De Vries and Bakker, 1996).The three north-east Wales sites would be at the most ecological risk on this basisparticularly Trelogan.


TABLE VII

C. brunneus: Diet cadmium concentra-tion ratios (CR)

Site CR

Reference 0.71

Cwmerfin 1.67

Grogwnion 1.41

Cwmsymlog 0.71

Frongoch 1.15

Cwmrheidol 0.61

Ystum Tuen 2.3

Rhosesmor 8.5

Trelogan 0.57

East Halkyn 3.37

Irish tailings 10.6

Overall, from an incomplete data set across the sites, the concentrations ofcadmium in invertebrates in this study are similar to other studies of contamin-ated sites (Andrews and Cooke, 1984; Hunter et al., 1987b; Rabitsch 1995a, b).The animals from the three ‘high’ sites in north-east Wales sites generally hadthe highest cadmium levels although Cwmrheidol ( a ‘low’ site based on soil andplant levels) showed some relatively high concentrations in all feeding categoriesof invertebrates (Tables III and IV). There is some evidence of food-chain trans-fer and biomagnification (animal/:food ratios > 1). The carnivorous invertebratesanalysed in this study show concentrations of cadmium that are higher than intheir potential prey. The highest concentrations measured were in the carnivorousspider, P. mirabilus, where the mean values at Trelogan (77 mg kg−1) and EastHalkyn (47 mg kg−1) are similar to the range 30–100 mg kg−1 given for spidersfrom contaminated sites (Andrews and Cooke, 1984; Hunter et al., 1987b).

The phytophagous grasshoppers, with their grass based diet, constitute a sim-plified food chain situation in which animal: diet concentration ratios can be cal-culated. These are shown in Table VII for C. brunneus. There was no direct correl-ation between concentrations of cadmium in grasshoppers and their grass diet (1:1w/w; Festuca:Agrostis) (p > 0.05), although in most cases the ratio of animal:grass concentration is greater than 1.0. This lack of correlation contrasts with thefindings of Hunter et al. (1987d) who identified a near linear relationship betweengrasshopper and food concentrations of cadmium in closed, smelter-contaminatedgrasslands.


TABLE VIII

Estimated intake of cadmium (µg day−1) by gastropodsa

Site Diet composition

F. rubra Agrostis spp. 50:50 Composite Litter

mixed grass ground cover

Reference 0.08 0.23 0.15 0.01 0.01

Cwmerfin 0.01 0.15 0.08 0.11 0.38

Grogwnion 0.15 0.15 0.15 1.17 1.44

Cwmsymlog 0.23 0.15 0.19 0.90 0.72

Frongoch 0.15 0.08 0.12 2.79 0.64

Cwmrheidol 0.12 0.68 0.40 0.69 1.15

Ystum Tuen 0.16 0.01 0.09 1.08 0.01

Rhosesmor 0.08 0.15 0.12 3.33 2.79

Trelogan 1.26 1.17 1.22 5.76 20.7

East Halkyn 0.45 0.30 0.37 0.01 1.44

Irish Tailings 0.01 0.05 0.03 0.01 0.01

a Based on food intake of 0.9 g day−1 (Williamson, 1975).

A possible reason for this difference in cadmium dynamics between smelterand mine site populations of grasshoppers concerns the relatively smaller size ofthe contaminated area at the mine sites. Female C. brunneus select bare patches ofground for oviposition, and these are common at mine sites. Soon after hatching theearly instar nymphs migrate to areas with adequate food supplies (Brown, 1983),and this may involve desertion of the contaminated area. Adult females then needto re-aggregate on bare ground to deposit the next generation of eggs. All animalsanalysed in this investigation were of the 5th instar, captured during July/August.They, therefore, represent animals returning to the contaminated area after feedingelsewhere. It is assumed that males follow the same migration patterns on the basisthat the underlying causes of local movement are food availability and reproductivedrive.

Terrestrial molluscs have been promoted as environmental bioindicators (Rus-sell et al., 1981; Greville and Morgan, 1987); but evidence of the effects of cad-mium on normal gastropod activity are contradictory. For example, Russell et al.(1981) found that increased levels of dietary cadmium caused a reduction in foodintake by Helix aspersa although Berger et al. (1993) found no such decrease.Laskowski and Hopkin (1996) also found a reduction in food consumption, alongwith reduced fecundity, in animals exposed to dietary cadmium. Estimated foodconsumption by C. nemoralis is in the region of 0.8–1.0 g day−1 (Williamson,1975) and by using this value in the present study it is possible to estimate dailycadmium intake based on different diet compositions (Table VIII). A positive re-


lationship exists between the daily intake of cadmium based solely on Agrostisspecies and body concentrations of C. nemoralis (r2 = 0.84; n = 9; p < 0.001).This may reflect a prominent role for the Agrostis genus in the diet of mine sitepopulations of C. nemoralis, which is consistent with the high relative abundanceof Agrostis spp. in the plant communities of toxic sites. Similar relationships wereapparent between cadmium in A. ater and in F. rubra, litter and composite groundcover (r2 = 0.50, 0.47 and 0.49, respectively; n = 9; p < 0.05). It is not known ifthese distinct significant relations reflect dietary niche separation between the twogastropods.

The only significantly high level of cadmium in kidney tissue of A. sylvaticuswas from animals captured at East Halkyn which had the second highest estimateddaily intake at the cadmium-rich sites. However, over all the sites there was norelationship between the estimated daily dietary intake of cadmium (Table VI) andthe kidney or liver residues of A. sylvaticus (p > 0.05). This finding supportsthe review of published data by Shore and Douben (1994) as regards A. sylvaticusthough these authors reported significant positive regressions between concentra-tions of cadmium in the organs of the common shrew (Sorex araneus) and the fieldvole (Microtus agrestis), and their estimated dietary exposure. The diets of theshrew and vole are less diverse than that of A. sylvaticus enabling a more accuratedetermination of dietary cadmium intake (Hunter et al., 1987c). Further, althoughA. sylvaticus is described as granivorous this description has been derived mainlyfrom studies in woodland environments (e.g. Smal and Fairley, 1980), where treeand shrub seeds dominate the diet. In grasslands and disturbed ecosystems whereproductivity is lower, A. sylvaticus is likely to be more strongly omnivorous se-lecting a wide variety of other food items including fungi, green vegetation andinvertebrates (Hunter et al., 1987c; Halle, 1993; Rogers and Gorman, 1995).

It has been suggested that soil concentrations of cadmium can be used to predictresidual levels in small mammal tissues, and significant relationships have beenfound for wood mice and common shrews (Talmage and Walton, 1991; Shore,1995). However, the data presented here contrast with these findings with no sig-nificant relationships detected between either the liver or kidney residues and thelevels of total or available cadmium in mine wastes (p > 0.05). The lack of a signi-ficant relationship between tissue residues and dietary intake by A. sylvaticus at themost contaminated sites may also be a function of the size of the sites investigated.Animals trapped even at the centre of a large contaminated area may only be takingpart of their food from highly polluted terrain (Attuquayefio et al., 1986; Milton etal., 2002).

There is no evidence that concentrations of cadmium in the kidneys of thesemine site animals, even from East Halkyn, are sufficient to induce toxic responses.Reviews of the critical concentrations with regards to the onset of clinical symp-toms for whole kidney cadmium residues in wild small mammals are in the range100–300 mg kg−1 wet weight or 350–1000 mg kg−1 dry wt (Shore and Douben,1994; Cooke and Johnson, 1996). Statements concerning lower thresholds e.g.


30 µg g−1 fresh weight (119 µg g−1 dry weight) have been reported as inducingsub-clinical histopathological changes (Chmielnicka et al., 1989). However, theselower thresholds represent direct (acute) doses administered through subcutaneousinjection and not through chronic dietary exposure which is more realistic in assess-ing ecological risk (Beyer, 2000). Indeed, the results presented in this paper concurwith the views of Beyer (2000) that although high soil cadmium can be the basis offood chain transport of cadmium and even biomagnification, in overall ecologicalrisk assessment terms the toxicity of cadmium especially to small mammals can beoverstated.

References

Andrews, S. M. and Cooke, J. A.: 1984, ‘Cadmium within a Contaminated Grassland EcosystemEstablished on Metalliferous Mine Waste’, in D. Osborn (ed.), Metals in Animals, Institute ofTerrestrial Ecology, Huntingdon Cambs, pp. 11–15.

Attuquayefio, D. K., Gorman, M. L. and Wolton, R. J.: 1986, ‘Home range sizes in the Wood mouseApodemus sylvaticus: Habitat, sex and seasonal differences’, J. Zool. Lond. 210, 45–53.

Balsberg Pählsson, A.-M.: 1989, ‘Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Aliterature review’, Water, Air and Soil Pollut. 47, 287–319.

Bengtsson, G. and Tranvik, L.: 1989, ‘Critical metal concentrations for forest soil invertebrates; Areview of limitations’, Water, Air, and Soil Pollut. 47, 381–417.

Berger, B., Dallinger, R., Felder, E. and Moser, J.: 1993, ‘Budgeting the Flow of Cadmium and ZincThrough the Terrestrial Gastropod, Helix pomatia L., in R. Dallinger and S. P. Rainbow (eds),Ecotoxicology of Metals in Invertebrates, Lewis, Boca Raton, pp. 291–314.

Beyer, W. N., Connor, E. E. and Gerould, S.: 1994, ‘Estimates of soil ingestion by wildlife’, J.Wildlife Manage. 58, 375–382.

Beyer, W. N.: 2000, ‘Hazards to wildlife for soil-borne cadmium reconsidered’, J. Environ. Qual. 29,1380–1384.

Brady, E.: 1993, ‘Revegetation and Environmental Management of Lead-Zinc Mine Tailings’,M.Phil. Thesis, University of Liverpool, England, pp. 201.

Brown, V. K.: 1983, Grasshoppers, Cambridge University, Cambridge, pp. 65.Chmielnicka. J., Halatek, T. and Jedlinska, U.: 1989, ‘Correlation of cadmium-induced nephropathy

and the metabolism of endogenous copper and zinc in rats’, Ecotox. Environ. Safety 18, 268–276.Cooke, J. A, and Johnson, M. S.: 1996, ‘Cadmium in Small Mammals’, in N. Beyer, G. Heinz and A.

Redmond-Norwood (eds), Environmental Contaminants in Wildlife: Interpreting Tissue Concen-trations, Society of Environmental Toxicology and Chemistry Special Publication, Lewis, BocaRaton, pp. 377–388.

Cooke, J. A., Andrews, S. M. and Johnson, M. S.: 1990, ‘Lead, zinc, cadmium and fluoride in smallmammals from contaminated grassland established on fluorspar tailings’, Water, Air, and SoilPollut. 51, 43–54.

Day, R. W. and Quinn, G. P.: 1989, ‘Comparisons of treatments after analysis of variance in ecology’,Ecol. Monographs 59, 433–463.

De Vries, W. and Bakker, D. J.: 1996, ‘Manual for Calculating Critical Loads of Heavy Metals forSoils and Surface Waters. Preliminary Guidelines for Environmental Quality Criteria, CalculationMethods and Input Data’, Wageningen, DLO Winand Staring Centre Report 114, pp. 173.

Dodds-Smith, M. E., Johnson, M. S. and Thompson, D. J.: 1992, ‘Trace metal accumulation by theshrew Sorex araneus. 2. Tissue distribution in kidney and liver’, Ecotox. Environ. Safety 24, 1–13.


Furness, R. W.: 1996, ‘Cadmium in Birds’, in N. Beyer, G. Heinz and A. Redmond-Norwood(eds), Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations, Society ofEnvironmental Toxicology and Chemistry Special Publication, Lewis, Boca Raton, pp. 389–404.

Erry, B. V., Macnair, M. R., Meharg, A. A. and Shore, R. F.: 2000, ‘Arsenic contamination in woodmice (Apodemus sylvaticus) and bank voles (Clethrionomys glareous) on abandoned mine sitesin southwest Britain’, Environ. Pollut. 110, 179–187

Greville, R. W. and Morgan, A. J.: 1987, ‘The Accumulation and Effects of Heavy Metal Assimil-ation on Selected Terrestrial Slug Species’, in Heavy Metals in the Environment, New Orleans,Vol II, CEP Consultants, Edinburgh, U.K., pp. 48–51.

Halle, S.: 1993, ‘Wood mice (Apodemus sylvaticus) as pioneers of recolonization in a reclaimedarea’, Oecologia 94, 120–127.

Hoiland, K.: 1995, ‘Reaction of some decomposer Basidiomycetes to toxic elements’, Nordic J. Bot.15, 305–318.

Hunter, B. A. and Johnson, M. S.: 1982, ‘Food chain relationships of copper and cadmium incontaminated grassland ecosystems’, Oikos 38, 108–117.

Hunter, B. A., Johnson, M. S. and Thompson, D. J.: 1987a, ‘Ecotoxicology of copper and cadmiumin a contaminated grassland ecosystem. 1. Soil and vegetation contamination’, J. Appl. Ecol. 24,573–586.

Hunter, B. A, Johnson, M. S. and Thompson D. J.: 1987b, ‘Ecotoxicology of copper and cadmiumin a contaminated grassland ecosystem. 2. Invertebrates’, J. Appl. Ecol. 24, 587–599.

Hunter, B. A., Johnson, M. S. and Thompson, D. J.: 1987c, ‘Ecotoxicology of copper and cadmiumin a contaminated grassland ecosystem. 3. Small mammals’, J. Appl. Ecol. 24, 601–614.

Hunter, B. A., Hunter, L. M., Johnson, M. S. and Thompson, D. J.: 1987d, ‘Dynamics of metal accu-mulation in the grasshopper Chorthippus brunneus in contaminated grasslands’, Arch. Environ.Contam. Toxicol. 16, 711–716.

Hutton, M.: 1983, ‘Sources of cadmium in the environment’, Ecotox. Environ. Safety 7, 9–24.Jackson, A. P. and Alloway, B. J.: 1992, ‘The Transfer of Cadmium from Agricultural Soils to the

Human Food Chain’, in D. C. Adriano (ed.), Biogeochemistry of Trace Elements, Lewis, BocaRaton, pp. 109–158.

Johnson, M. S., Roberts, R. D., Hutton, M. and Inskip, M. J.: 1978, ‘Distribution of lead, zinc andcadmium in small mammals from polluted environments’, Oikos, 30, 153–159.

Johnson, M. S., Cooke, J. A. and Stevenson, J.: 1994, ‘Revegetation of Metalliferous Wastes andLand Associated with Metal Mining’, in R. E. Hester and R. M. Harrison (eds), Issues in En-vironmental Science and Technology, Vol. 1, Royal Society of Chemistry, Cambridge, U.K.,pp. 31–48

Laskowski, R. and Hopkin, S. P.: 1996, ‘Effect of Zn, Cu, Pb, and Cd on fitness in snails (Helixaspersa’, Ecotox. Environ. Safety 34, 59–69.

Livens, F. R.: 1991, ‘Chemical reactions of metals with humic materials’, Environ. Pollut. 70, 183–208.

McLaughlin, M. J., Hamon, R. E., McLaren, R. G., Speir, T. W. and Rogers S. L.: 2000, ‘Review: Abioavailability-based rationale for controlling metal and metalloid contamination of agriculturalland in Australia and New Zealand’, Aust. J. Soil Res. 38, 1037–1086.

Milton, A. M., Collings, S. E. and Johnson, M. S.: 1998, ‘The determination of lead and cadmium inbiota by electrothermal atomic absorption spectrometry’, Anales de Quimica 94, 349–353.

Milton, A. M, Johnson, M. S. and Cooke, J. A.: 2002, ‘Lead within ecosystems on metalliferousmine tailings in Wales and Ireland’, Sci Tot. Environ. 292, 177–190.

Nriagu, J. O.: 1979, ‘Global inventory of natural and anthrogenic sources of metals in theatmosphere’, Nature 279, 409–411.

Rabitsch, W. B: 1995a, ‘Metal accumulation in arthropods near a lead/zinc smelter in Arnoldstein,Austria. 1’, Environ. Pollut. 90, 221–237.


Rabitsch, W. B.: 1995b, ‘Metal accumulation in arthropods near a lead/zinc smelter in Arnoldstein,Austria. 3. Arachnida’, Environ. Pollut. 90, 249–257.

Rogers, L. M. and Gorman, M. L.: 1995, ‘The diet of the wood mouse Apodemus sylvaticus onset-aside land’, J. Zool. Lond. 235, 77–83.

Russell, L. K., Dehaven, J. I. and Botts, R. P.: 1981, ‘Toxic effects of cadmium in the garden snail(Helix aspersa)’, Bull. Environ. Contam. Toxicol. 26, 634–640.

Shore, R. F.: 1995, ‘Predicting cadmium, lead and fluoride levels in small mammals from soilresidues and by species-species extrapolation’, Environ. Pollut. 88, 333–340.

Shore, R. F. and Douben. P. E. T.: 1994, ‘The ecotoxicological significance of cadmium intake andresidues in terrestrial small mammals’, Ecotox. Environ. Safety 26, 104–112.

Smal, C. M. and Fairley, J. S.: 1980, ‘Food of wood mice (Apodemus sylvaticus) and bank voles(Clethrionomys glareolus) in Oak and Yew woods at Killarney, Ireland’, J. Zool. Lond. 191,413–418.

Talmage, S. S. and Walton, B. T.: 1991, ‘Small mammals as monitors of environmental contamin-ants’, Rev. Environ. Contam. Toxicol. 119, 47–145.

Tyler, G, Balsberg Pöhlsson, A. M., Bengtsson, G, Bääth E. and Tranvik, L.: 1989, Heavy-metalecology of terrestrial plants, micro-organisms and invertebrates’, Water, Air, and Soil Pollut. 47,189–215.

WDA: 1978, Survey of Abandoned Metalliferous Mines in Wales, Welsh Development Agency,Cardiff, U.K., pp. 90.

Williamson, P.: 1975, ‘The Feeding Ecology and Energetics of a Grassland Population of the Snail,Cepaea nemoralis L., Ph.D. Thesis, Portsmouth Polytechnic, England, 1975.

a comparison of cadmium in ecosystems on metalliferous mine tailings in wales and ireland

Documents