lead within ecosystems on metalliferous mine tailings in wales and ireland

The Science of the Total Environment 299(2002) 177–190

0048-9697/02/$ - see front matter� 2002 Elsevier Science B.V. All rights reserved.PII: S0048-9697Ž02.00253-X

Lead within ecosystems on metalliferous mine tailings in Walesand Ireland

Adrian Milton , Michael S. Johnson , John A. Cooke *a a b,

School of Biological Sciences, Life Sciences Building, University of Liverpool, Liverpool, L69 7ZB, UKa

School of Life and Environmental Sciences, George Campbell Building, University of Natal, Durban 4041, South Africab

Received 9 December 2001; accepted 5 June 2002

Abstract

A comparative study of the concentrations of lead in ecosystems developed on metalliferous mine tailings wasundertaken. Mine soils, vegetation, ground-dwelling invertebrates andApodemus sylvaticus from nine abandonedmines in Wales and a modern Irish mine site were sampled in order to evaluate and compare exposure risks towildlife. The mine sites had a wide range of relatively high concentrations of total lead in their tailings(from 1058to 46 630 mg kg ) but the extractable lead fractions were extremely variable and not clearly related or proportionaly1

to the total values. The high soil concentrations were reflected in vegetation collected from most of the sites with theexception of the modern mine, but there was no statistical relationship, on a site basis, between available soil leadand that in plant leaf samples. The highest plant concentrations were found in litter, which in all but one of theWelsh sites exceeded the threshold guideline value of 150 mg kg . Food-chain transfer was shown by highy1

concentrations of lead in invertebrates andA. sylvaticus from the abandoned Welsh mines. A highly significantrelationship existed between lead in grass and the grasshopper,Chorthippus brunneus. Adverse effects on soilinvertebrates, essential to the decomposition processes and cycling of essential nutrients, were identified as probablythe major obstacle to natural ecosystem development on the abandoned Welsh sites. Toxicological risk of lead to thesmall mammals from the Welsh sites, but not the modern Irish tailings, is indicated given the high lead concentrationsin dietary items and the resultant residues in kidney with some evidence of renal oedema in animals from two sites.The absence of a significant relationship between the estimated dietary lead concentration, calculated on a site basis,and the total body concentration inA. sylvaticus, was attributed, in part, to the large size of the home range and thepartial feeding of individual animals off the contaminated mine site.� 2002 Elsevier Science B.V. All rights reserved.

Keywords: Lead; Food chains; Ecotoxicological risk; Mine tailings; Invertebrates;Apodemus sylvaticus

*Corresponding author. Tel.:q27-312-603-192; fax:q27-312-602-029.E-mail address: [email protected](J.A. Cooke).

178 A. Milton et al. / The Science of the Total Environment 299 (2002) 177–190

Table 1Characteristics of Welsh mine sites(WDA, 1978)

Site Ordinance Date last Area Pba Cda Zna

name survey worked (ha) (mg kg )y1 (mg kg )y1 (mg kg )y1

Grid Ref. dry wt. dry wt. dry wt.

Cwmerfin SN 703824 1889 0.5 7800 14 2500Grogwnion SN 714725 1889 1 7100 10 625Cwmsymlog SN 700837 1901 2 14 000 8 7850Frongoch SN 721744 1901 4 7600 6 7200Cwmrheidol SN 730782 1924 2 4219 35 6600Ystum Tuen SN 733788 1919 0.75 7800 18 9870Rhosesmor SJ 214684 1866 0.8 138 500 165 40 320Trelogan SJ 127802 1909 2.3 13 800 131 46 200East Halkyn SJ 211698 1910 0.5 5500 135 39 000

Total concentrations in fine tailings(-2 mm).a

1. Introduction

The main contemporary uses of lead are batterymanufacture, cable sheathing, solders, bearings,radiation shielding, plastics, ceramics and evencosmetics(Stewart, 1994). As with other metalsthe major increase in lead consumption and asso-ciated pollution events came with the IndustrialRevolution, and the mining and smelting of met-alliferous ores has resulted in approximately 4000km of agricultural land being contaminated in the2

UK alone (Thornton, 1980). Concerns about theenvironmental impacts of technogenic lead havecaused it to be one of the most investigated ofpollutants. Special attention has been given to theenvironmental and human health issues surround-ing alkyl-lead additives to motor fuels, in particularthe neurological and developmental defects exhib-ited by children living in areas of dense traffic(Lansdown, 1986). Another area of environmentalconcern has been the exposure of birds to leadused as fishing weights or gun shot, sources towhich bird mortalities have been linked(Pain,1996; Scheuhammer and Norris, 1996).Ecosystem distribution of lead has been inves-

tigated in mining and related refining industries(Roberts and Johnson, 1978; Andrews et al., 1989;Purcell et al., 1992), road verges(Purcell et al.,1992) and aquatic systems(Gerhardt, 1993). How-ever, mine tailings, the waste from the processingof mineral ores, represent an exceptional source ofmetal contamination since other anthropogenic or

natural sources rarely cause such elevated levelsof lead in the substrate(Andrews et al., 1989).This study compares the environmental signifi-

cance of lead at a selection of historic and aban-doned Welsh mine sites last worked between 1866and 1924(WDA, 1978), and a typical moderntailings facility at a leadyzinc mine in the Republicof Ireland(Brady, 1993). The primary aim was toassess the potential ecotoxicological risk associatedwith lead at a range of mine sites in the contextof these sites being colonised by wildlife. A secondaim was the comparison of the modern site inIreland with the much older abandoned sites. Thissought to inform the restoration practice currentlyin operation at the modern site, in terms of theproduction of a sustainable low-maintenance grass-land and the potential impacts residual lead mayhave in realising this goal. Cadmium was also asignificant contaminant of these wastes and willbe considered in a separate paper.

2. Materials and methods

Site selection was based on the results of anearlier study of metal mines in Wales(WDA,1978), using the criteria of size()0.5 ha) andsoil levels of residual metals to ensure comparisonsacross a broad range of contamination levels(Table 1). A reference site(OS Grid Ref: SN665734), with a similar grass flora to the Welshmine sites, was also selected. The modern tailingsdam, located in the Republic of Ireland, covers

179A. Milton et al. / The Science of the Total Environment 299 (2002) 177–190

some 78 ha to an average tailings depth of 14 m.It is covered by a sown and managed, predomi-nantly grass, sward dominated by red fescue(Fes-tuca rubra), creeping bent(Agrostis stolonifera)and white clover(Trifolium repens) (Brady, 1993).Field sampling was conducted in the late sum-

mer and autumn of 1995. Bulk samples(500 g)of surface soil(0–10 cm) were collected from atleast four densely vegetated areas at each minesite, but with selectivity towards the core area soas to avoid the margins and boundaries. Driedsamples(0.5 g) of tailings were sieved(1 mm)and sequentially extracted with 10 ml of doubledistilled water(DDW), 0.5 M ethanoic acid andconcentrated nitric acid(Davies, 1971). Soil sus-pensions were agitated for 1 h and centrifuged at10 000 rev. min for 30 min with each extractanty1

before decanting and diluting to 25 ml with DDW.A range of vegetation samples was collected

from the Welsh mine sites, including the leaves ofdominant grasses, red fescue(Festuca rubra) andcommon bent(Agrostis capillaris). In order todetermine dietary lead intake by the wood mouse,Apodemus sylvaticus, the principal food items werealso collected including grass seeds, blackberries(Rubus fruticosus), seeds of rowan(Sorbus aucu-paria), gorse (Ulex europaeus) and sycamore(Acer pseudoplatanus) trees, young heather(Cal-luna vulgaris) shoots and flowers, and a compositesample of the leaves and flowers of young forbs(Smal and Fairley, 1980; Hunter et al., 1987a;Rogers and Gorman, 1995). Invertebrates werealso sampled since this provides a seasonal foodsource of A. sylvaticus. The estimated dietarycomposition took account of the food items avail-able at each site and was adapted accordingly.Invertebrates were collected using pitfall traps

containing 2% formalin positioned in each of thevegetation zones. Traps were exposed for 12 weeksin late summer and autumn, animals were sorted,identified to species level and then oven-dried toconstant weight. The terrestrial gastropods,Arionater andCepaea nemoralis, and adult(5th instar)common field grasshoppers(Chorithippus brun-neus), were also collected manually from eachsite.Vegetation and plant litter were collected as

small (2–15 g wet wt.) bulk samples, each com-

prising pooled, randomly selected material froman area of 100 m to 0.5 ha according to the total2

area of the mine site. Samples were oven-dried(48 h, 80 8C), then ground to pass a 0.5-mmscreen. Gastropods were allowed to passively evac-uate their alimentary tract, bulked to give threereplicates of six animals of each species per site,and then homogenised before acid digestion.Grasshoppers were not depurated, digested in acidindividually after oven drying. Only invertebratespecies present at several sites, and in sufficientnumbers for statistical analysis, had their metalconcentrations determined.Adult specimens ofA. sylvaticus ()15-22 g

wet wt.) were caught in late summer using baitedlive traps located selectively in the densest areasof vegetation. The sparse population density ofmammals was addressed by an intensive campaignusing 150 traps set for 2–5 days, with twice dailyinspection. Animals were killed and immediatelyfrozen to prevent tissue lysis and metal redistri-bution. The liver, kidney, muscle and bone(femur)were analysed as well as the residual carcass fromwhich the gut contents were removed and discard-ed. Muscle tissue was manually removed from thefemurs, which were then cleaned enzymically withpapain solution and oven-dried(Pankakoski andHanski, 1989).All biological samples were subjected to acid

digestion, involving overnight cold dissolution inconcentrated HNO , followed by boiling at 1208C3

for 2 h. MERCK ‘Analar’ grade acid was used forsoil analysis, whereas ‘Aristar’ grade was used forvegetation, invertebrate and mammal samples. Soilextracts and acid digests were analysed for metalsusing flame atomic absorption spectrometry(AAS), matrix-matched calibration standards anddeuterium background correction for non-atomicabsorption. Seed, invertebrate and small mammaltissue digests were analysed by graphite furnaceatomic absorption spectrometry(GFAAS), usingthe L’vov platform furnace technique(Voth-Beach,1985). Zeeman background correction and a mixedchemical modifier of reduced palladium, magne-sium nitrate and ammonium dihydrogen phosphatesolution was used to minimise interference for allGFAAS analyses. Operational conditions are givenin more detail in Milton et al.(1998).


Table 2Concentration(mg kg dry wt."S.E.M.) of lead in surface soils from the reference and mine sitesy1 ‡

Site n Double distilled 0.5 M ConcentratedH O2 CH COOH3 HNO3

Reference 7 0.07"0.03 7.6"2.0††† 31"7.3†††

Cwmerfin 4 4.8"1.3**†† 5800"1788*** † 12 550"3620*** ††

Grogwnion 4 18"11** †† 7440"2866*** † 8930"2634*** ††

Cwmsymlog 5 11"4.6**†† 4500"1292*** † 24 470"12003***††

Frongoch 4 5.8"1.1**† 1294"460*** 4160"1202*** †

Cwmrheidol 4 34"21*** ††† 174"83*** † 9510"3882*** ††

Ystum Tuen 4 24"12*** ††† 558"130*** 5740"811*** ††

Rhosesmor 4 8.3"1.8**†† 4420"649*** † 46 630"11070***†††

Trelogan 4 3.4"1.0*† 5970"333*** † 13 780"4115*** ††

East Halkyn 4 4.7"1.4*† 2510"2405*** 17 410"12849***††

Irish tailings 10 -0.05 912"167*** 1058"173***

*, ** and *** denote significant difference from reference site atP-0.05,-0.01 and-0.001, respectively. , and denote† †† †††

significant difference from Irish tailings atP-0.05,-0.01 and-0.001, respectively. ANOVA computed on log transformed‡10

data.

All glassware was acid-washed and qualityassurance was provided by running double blanksand certified reference materials(CRMs) with allsample batches. BCR 142(light sandy soil), BCR277 (estuarine sediment) and IAEA soil 7 wereincluded in each batch of tailings samples andrecoveries of lead were between 88 and 96% ofthe certified value. The CRMs included with veg-etation samples were BCR 60(aquatic plant,Lagarosiphon major), BCR 279(sea lettuce,Ulvalactuca) and NIST 1573a(tomato leaves). Recov-eries of lead were between 88 and 114%. Forinvertebrates, the CRM used was TORT-1(lobsterhepatopancreas) for which lead recoveries werebetween 90 and 97%. The CRMs adopted formammal tissues were BCR 185(bovine liver) andBCR 186(pig kidney). Recoveries were between83 and 118%.Mammal tissue results were converted from wet

to dry weight using pre-determined conversionfactors (carcass, 2.72; kidney, 3.69; liver, 3.67;muscle, 3.83). Total body lead concentrations(TBC) were calculated by adding individual tissueburdens to residual carcass values. Gastropod con-centrations of lead were similarly converted to dryweight using a factor of 6.8.Due to variations in site area and the abundance

of animals, replication(n) for each site varied,and is given in Tables 2–7. All data sets arepresented using arithmetic means and standard

errors and were log transformed and subjected10

to a one-way analysis of variance(ANOVA), usingsite as the effect factor. Probability data thereforerelate to analyses undertaken on normalised distri-butions. A Tukey’s–Kramer test was used forcomparison between sites for each sample type(Day and Quinn, 1989). Values of half the detec-tion limit (FAASs0.05mg g ) were substitutedy1

in statistical analysis for samples with lead levelsbelow machine detection limits. All data from thepresent study are presented on a dry weight basisunless stated otherwise.

3. Results

3.1. Soil

Concentrations of lead in the mine wastes aresummarised in Table 2. With the exception of theIrish tailings, all sites had significantly more waterextractable lead than the reference site(P-0.05).For the Irish tailings, water soluble lead was belowa detection limit of 0.05mg g for all replicatesy1

(ns10). The ethanoic- and nitric acid extractablelead for all mine sites were significantly elevatedwith respect to the reference site(P-0.001).Similarly, most of the old Welsh mine wastescontained more lead than the Irish tailings(P-0.05), the exceptions being the ethanoic acidextractable fraction at Frongoch, Ystum Tuen and


Table 3Concentration of lead in plants and litter from the reference and mine sites(mg kg dry wt."S.E.M.)y1

Site F. rubra‡ Agrostis spp‡ Composite Litter‡ Compositeground seedscover‡

Reference 3.6"1.6 4.3"0.2 2.3"0.4 10"1.3††† 2.0"0.5(3) (3) (9) (6) (14)

Cwmerfin 29"4.6*** ††† 156"41*** ††† 87"34*** ††† 1925"595*** ††† 6.4"1.8(3) (3) (9) (5) (12)

Grogwnion 48"10*** ††† 89"3.7*** ††† 121"19*** ††† 790"285*** ††† 2.2"0.6(3) (3) (6) (6) (9)

Cwmsymlog 49"12*** ††† 281"69*** ††† 16"2.3*** ††† 382"74*** ††† 2.4"0.5(4) (4) (8) (8) (12)

Frongoch 88"30*** ††† 161"38*** ††† 156"18*** ††† 896"308*** ††† 46"15*** †††

(3) (3) (9) (6) (9)Cwmrheidol 14"3.6*** ††† 21"11*†† 8.3"4.5 72"19*** 1.5"0.1

(4) (4) (12) (8) (3)Ystum Tuen 48"5.6*** ††† 81"7.6*** ††† 61"10*** ††† 346"55*** ††† 0.8"0.8

(3) (3) (4) (6) (4)Rhosesmor 87"13*** ††† 58"27*** ††† 136"15*** ††† 523"29*** ††† 14"4.3**†

(3) (3) (4) (4) (9)Trelogan 178"46*** ††† 131"36*** ††† 177"39*** ††† 1890"1220*** ††† 16"3.8**†

(3) (3) (4) (4) (12)East Halkyn 68"4.2*** ††† 53"2.6*** ††† 158"22*** ††† 163"25*** † 21"5.0*** ††

(3) (3) (6) (6) (12)Irish tailings 1.3"0.2 -0.50** 1.4"0.2 60"4.3*** 3.1"0.3

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

ANOVA performed on log transformed data. Replication(n) in parentheses. *, ** and *** denote significant difference from‡10

reference site atP-0.05,-0.01 and-0.001, respectively. , and denote significant difference from Irish tailings atP-0.05,† †† †††

-0.01 and-0.001, respectively.

East Halkyn where there were no differences(P)0.05), and the same fraction at Cwmrheidol whichwas lower than for the Irish material(P-0.05).The extractable and total concentrations of lead

in soils from the reference site were within thenormal ranges for British soils of: 0.13–16 mgkg and 10.9–145 mg kg , respectively(Archer–1 y1

and Hodgson, 1987), and the total value was verysimilar to the baseline of 30 mg kg calculatedy1

for soils worldwide(Kabata-Pendias and Pendias,1992). Combining the sequentially extracted frac-tions gave a total lead concentration in the Irishtailings similar to the 2320 mg kg reportedy1

previously for the same site(Brady, 1993). Totallead levels from the Welsh mine sites were alsosimilar to those previously reported(Table 1)(WDA, 1978).

3.2. Vegetation and litter

Lead concentrations in vegetation and litter sam-ples are summarised in Table 3. The concentration

in litter samples was always considerably higherthan any other vegetation sample type, and at allsites, except the Irish tailings, composite seedsshowed the lowest levels of lead contamination.The grassesF. rubra andAgrostis spp had signif-icantly elevated levels of lead at all the Welshmine sites compared to both the reference andIrish sites(P-0.05). Similarly, concentrations oflead in composite ground cover vegetation weresignificantly higher(P-0.001) at all Welsh minesites except Cwmrheidol, whilst there was nodifference between the Irish and reference sites(P)0.05). Litter showed a similar pattern, withall Welsh sites and the Irish tailings dam signifi-cantly elevated with respect to the reference site(P-0.001) and all Welsh sites except Cwmrheidolhigher than the Irish tailings(P-0.05). The con-centrations of lead in composite seeds showed lessdifferences between sites with only samples fromFrongoch, Rhosesmor, Trelogan and East Halkyn,


Table 4Concentration of lead in herbivorous and detritivorous invertebrates from the reference and mine sites(mg kg dry wt."S.E.M.)y1

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

Reference 0.7"0.1††† 2.6"0.5†† 12"1.0 9.5"0.3††

(6) (5) (3) (3)Cwmerfin 5.1"0.9*** 33"4.7*** 109"19** ††† 108"19*** ††

(5) (8) (4) (3)Grogwnion NT 48"9.3*** †† NT 63"12***

(4) (3)Cwmsymlog NT 30"4.0*** † 65"29† 14"5.0††

(11) (5) (4)Frongoch 222"56*** ††† 61"18*** †† 109"23** ††† 126"21*** †††

(5) (7) (5) (6)Cwmrheidol 136"32*** ††† 13"4.7** 5.6"4.1*††† 8.0"0.4††

(7) (8) (4) (3)Ystum Tuen NT 34"14*** 22"1.4 NT

(4) (3)Rhosesmor NT 77"15*** ††† 38"5.3† NT

(5) (3)Trelogan 41 133"8644*** ††† 63"15*** †† NT 25"4.5*

(5) (8) (3)East Halkyn 3847"583*** ††† 72"23*** †† 79"10** †† 44"3.1***

(6) (4) (3) (4)Irish Tailings 8.6"2.9*** 12"2.0** 9.2"0.7 32"5.2**

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

NT, not trapped or biomass too low for comparison. Replication(n) in parentheses. *, ** and *** denote significant differencefrom reference site atP-0.05,-0.01 and-0.001, respectively. , and denote significant difference from Irish tailings atP-† †† †††

0.05,-0.01 and-0.001, respectively.

being significantly higher than the reference andIrish sites(P-0.05).The concentrations of lead in plant material

followed the pattern described previously for veg-etation on a fluorspar tailings lagoon surface(Andrews et al., 1989), with the highest concen-trations being found in the plant litter. This islikely to reflect both a genuine increase in internalmetal burden, and also some degree of surfacecontamination. Levels of lead in reference sitevegetation were all similar to those reported pre-viously for clean sites(Andrews et al., 1989).Seasonal variation in vegetation concentrations oflead have been described for contaminated sites,and the summer is when lowest values occur, inresponse to growth dilution(Hunter et al., 1987b).The samples reported here were collected duringthe summer and so may represent lower dietaryexposure conditions for consumers than thoseexperienced at other times of the year. Seasonalfluctuations may have implications for the inter-

pretation of animal tissue concentrations of leadsince the composition of the diet itself, and alsothe metal loadings, will cause changes in metalintake, tissue- and total body burdens.

3.3. Invertebrates

Table 4 summarises the lead concentrations inherbivorous invertebrates. Concentrations of leadin the beetleAmara aulica and the grasshopperChorthippus brunneus, varied greatly between siteswith all mine waste animals showing significantlyhigher values than the reference site(P-0.01).Animals taken from all the historic Welsh minesites, except Cwmerfin, Cwmrheidol and YstumTuen, were also significantly higher than thosefrom the Irish tailings(P-0.05).Specimens ofArion ater from Cwmerfin, Fron-

goch, and East Halkyn had elevated levels of leadcompared to the reference site, whilst animals fromCwmrheidol were significantly lower(P-0.05).


Table 5Concentration of lead in carnivorous invertebrates from the reference and mine sites(mg kg dry wt."S.E.M.)y1

Site F. nigrita P. mirabilus O. parietinus

Reference 0.6"0.1 NT 17"1.7(22) (5)

Cwmerfin 14"0.9*** NT 1998"860*** †††

(6) (4)Grogwnion 160"39*** ††† 61"25 NT

(5) (8)Cwmsymlog NT 2755"696††† 207"107*

(7) (3)Frongoch 175"44*** ††† 326"97 755"216*** ††

(3) (11) (3)Cwmrheidol 60"18 241"52††† NT

(7) (5)Ystum Tuen 159"36*** ††† 48"24 NT

(4) (5)Rhosesmor NT NT NTTrelogan NT 1594"21††† NT

(3)East Halkyn 1532"65*** ††† 3253"1775††† NT

(4) (6)Irish Tailings 16"2.1*** 75"14 48"8.1*

(22) (6) (3)

NT, not trapped or biomass too low for analysis. Replication(n) in parentheses. * and *** denote significant difference fromreference site atP-0.05, and-0.001, respectively. and denote significant difference from Irish tailings atP-0.01 and-†† †††

0.001, respectively.

Table 6Lead concentrations in tissues ofApodemus sylvaticus from the reference and mine sites(mg kg dry wt."S.E.M.)y1 a

Site n Liver Kidney Bone Muscle

Reference 8 0.4"0.1 1.2"0.2 2.2"0.3††† 0.04"0.02†

Cwmerfin 6 4.4"2.0** 15"1.4*** ††† 531"162*** ††† 1.5"0.3***Grogwnion 5 3.2"0.9** 14"1.7*** ††† 165"21*** †† 1.4"0.4***Cwmsymlog 4 3.4"0.7** 43"7.5*** ††† 573"84*** ††† 0.6"0.4Frongoch 4 4.4"1.8** 40"12*** ††† 603"305*** ††† 0.8"0.1*Cwmrheidol 5 4.3"0.9**† 9.6"3.6*** † 123"62*** † 0.6"0.2Ystum Tuen 5 2.7"0.7** 10"2.5*** † 158"59*** † 0.4"0.1Trelogan 8 2.7"0.5** 14"3.8*** †† 111"31*** † 0.6"0.1East Halkyn 8 4.7"0.6*** † 6.8"0.6*** † 84"26*** 0.3"0.1Irish tailings 11 1.3"0.5 3.2"0.7 27"8.0*** 0.8"0.2*

Excluding Rhosesmor mine where no animals were caught.a

*, ** and *** denote significant difference from reference site atP-0.05,-0.01 and-0.001, respectively. , and denote† †† †††

significant difference from Irish tailings atP-0.05,-0.01 and-0.001, respectively.

Animals from all the Welsh sites were higher thanthe Irish tailings, except Ystum Tuen(P)0.05),and Cwmrheidol where animals were significantlylower (P-0.05). A similar pattern was found forC. nemoralis with all sites except Cwmsymlog andCwmrheidol higher than the reference site(P-

0.05). Cwmerfin and Frongoch were the only siteswith a higher lead concentration than the Irish site(P-0.01), while Cwmsymlog and Cwmrheidolwere significantly lower(P-0.01).Lead concentrations in carnivorous invertebrates

are summarised in Table 5. The beetle,Ferona


Table 7Total body concentration(TBC) and estimated daily leadintake byA. sylvaticus (mean"S.E.M.)

Site N TBC Pb intake(mg kg )y1 (mg day )y1

Reference 8 0.73"0.3 12.5"0.8Cwmerfin 6 29.4"11.3 1380"167Grogwnion 5 3.9"0.8 1934"193Cwmsymlog 4 23.3"5.0 1491"66Frongoch 4 37.5"19.8 774"39Cwmrheidol 5 2.1"0.8 117"17Ystum Tuen 5 1.6"0.4 351"25Trelogan 8 7.6"2.5 16 571"1151East Halkyn 8 5.6"2.0 1179"104Irish tailings 11 3.4"0.8 178"23

nigrita, had significantly elevated lead levels at allmine sites when compared with reference animals(P-0.001). For the wolf spider,Pisaura mirabi-lus, only animals from Cwmsymlog, Trelogan andEast Halkyn had concentrations significantly high-er than the Irish site(P-0.001). Similarly, for theharvestman,Opilione parietinus, all Welsh minesites recorded concentrations higher than the ref-erence site(P-0.05).

3.4. Apodemus sylvaticus

Mean body wet weights(g"S.E.M.) rangedfrom 21"2.4 for the Irish tailings to 26.7"1.3 forFrongoch, with a predominant weight range forindividuals of 20–24 g. There was no significantdifference between sites in terms of mean bodywet weights(P)0.05).Concentrations of lead in the tissues ofA.

sylvaticus are summarised in Table 6. Values forthe reference animals are similar to or lower thanthose reported previously for clean sites(Talmageand Walton, 1991; Purcell et al., 1992). The patternof tissue accumulation: bone)kidney)liver)muscle, was the same at all sites and the same asthat reported previously(Roberts et al., 1978;Andrews et al., 1989; Purcell et al., 1992). For thewhole data set, there was a significant relationshipbetween concentrations of lead in the total bodyand in the kidney(r s0.71; ns64; P-0.001)2

and bone(r s0.62; ns64; P-0.001) reflecting2

the importance of these two tissues as the maindepositories for absorbed lead.

Liver, kidney, and bone(femur) lead concentra-tions in animals from all Welsh mine sites werehigher (P-0.01) than the reference site, althoughonly bone(P-0.001) and muscle(P-0.05) fromthe Irish site were elevated above the levels at thereference site. Kidney and bone concentrationsfrom all the Welsh sites were also higher than theIrish tailings (P-0.05). Only animals trapped atCwmrheidol and East Halkyn had lead levels inliver that were higher than for the Irish site(P-0.05). Muscle showed a variable role in its contri-bution to body lead burden with Cwmerfin,Grogwnion, Frongoch and the modern Irish tailingssignificantly higher than the reference site(P-0.05). However, all liver values were lower thanconcentrations reported previously for small mam-mals from both contaminated and clean sites(Rob-erts et al., 1978; Storm et al., 1994). Muscle tissueis not known to have a prominent role in thestorage of lead in the mammalian body other thanthrough its higher proportional contribution to totalbody weight than that made by most other tissues.

3.5. Diet estimation

In view of the similarities in vegetation at theWelsh mine sites and reference site, at least asregards species present, a common dietary com-ponent model was adopted. However, the differentvegetation of the Irish tailings dam meant that aseparate model was needed to accommodate thereduced floristic diversity. Hunter et al.(1987a)described the seed part of the diet ofA. sylvaticusinhabiting a contaminated grassland as comprisingthe seeds ofR. fruticosus, rose bay willow herb(Epilobium angustifolium) andU. europaeus, sup-plemented by wind-blown tree seeds(A. pseudo-platanus) from surrounding areas. This collectionof species is very similar to that encountered atthe Welsh mine sites, and the diet model advocatedby Hunter et al.(1987a) (60% seed, 30% grassand 10% invertebrate material) was adoptedaccordingly. The diet ofA. sylvaticus has also beendescribed for animals living in ‘set-aside’ grasslandand on revegetated lignite mining waste wheregrass and seeds account for over 95% of the foodconsumed (Halle, 1993; Rogers and Gorman,1995). A similar, predominantly grass-based, diet


was assumed for animals on the revegetated Irishtailings surface(45% seed, 50% grass and 5%invertebrate material).In addition to the three food components of the

diet (seeds, grass, and invertebrates) incidentalsoil ingestion can comprise a significant proportion(approx. 2%) of the diet(Beyer et al., 1994; Erryet al., 2000). An estimate of Pb intake from soilwas also included into the dietary model. Theintake of all four dietary components was basedon body weight.There were no significant correlations(P)0.05)

between estimated dietary intake of lead(Table 7)and the calculated total body concentration or anyindividual tissue value. However, high diet levelswere generally associated with increased tissue andwhole body burdens.

4. Discussion

There have been few investigations into theimpact and biological transfer of lead to wildlifewhere the lead has been derived from soils andvegetation associated with mine tailings(Robertsand Johnson, 1978; Andrews et al., 1989; Purcellet al., 1992). Most of the research into soil leadpollution originating from the metals industry hasfocused on smelter deposition from the atmosphereto normal soils(e.g. Strojan, 1978; Ma et al.,1991; Storm et al., 1994; Rabitsch, 1995a,b).In this study, bioavailable lead, represented by

the water and ethanoic acid extractable metal,showed a large variation in the percentage of thetotal lead it represents; for example available leadfrom Cwmrheidol was approximately 2% of thetotal while for Grogwnion and the Irish tailings85% of the total was available. The bioavailabilityof heavy metals is influenced by many factors inunpolluted soils including substrate surface area asa function of particle size, pH, clay content,calcium carbonate, organic matter and levels ofiron and manganese(Hughes et al., 1980; Sillan-paa and Jansson, 1992; McLaughlin et al., 2000).¨ ¨In polluted soils the chemical and physical natureof the soil lead itself will also be important(Rieuwerts et al., 2000) and in mine tailings thiswill also included the physical and chemical natureof discrete high lead particles(Davis et al., 1992).

Relationships between substrate levels of metalsand those in vegetation growing on mine wasteare also strongly influenced by plant factors suchas transpiration rates, root growth rates and archi-tecture, root exudate production and root surfacelead precipitation, and the presence of associatedmycorrhizal fungi. Thus, the complex interactionsbetween the geochemistry of the wastes and plantspecies or ecotype influence plant uptake of lead.In this study, there was no correlation betweeneither the total or available lead in mine waste andthe concentrations in vegetation growing on them(P)0.05). The concentration in vegetation itselfappears to be the only reliable indicator of thepotential for lead transfer from the substratethrough the trophic levels of the ecosystem devel-oped on the mining wastes.Animals play an important role in ecosystem

functioning. In the context of ecosystem develop-ment on mine wastes these roles, inter alia, include(Majer, 1989): decomposition and nutrient cycling;improvement in soil structure; and plant pollinationand seed dispersal. The detrimental effects ofheavy metals on the invertebrate communitiesresponsible for decomposition have been well doc-umented and the lead levels present in soils andlitter from all the mine sites in this study generallyexceed those reported to impact upon decomposi-tion processes(see below and Babich and Stotzky,1985; Bengtsson et al., 1988). Inhibited incorpo-ration of organic matter into the substrate can alsohave long term implications since the adhesion ofmineral particles to organic matter is essential forthe development of the soil crumb structure thatdetermines aeration and drainage.Conservative threshold concentrations of soil

lead above which adverse effects may be expectedin soil-dwelling invertebrates are surprisingly low,and range from 25 to 300 mg kg (De Vries andy1

Bakker, 1996; McLaughlin et al., 2000). Using thelowest observed effect concentration(LOEC) fromfield and laboratory studies 150 mg kg is ay1

consensus critical threshold value for leaf litterand soil humus horizons(Bengtsson and Tranvik,1989; De Vries and Bakker, 1996). Given thehigher values of substrate and litter lead values inrelation to these critical values, in this study, thismay partly explain why pitfall catches of inverte-


brates were so reduced in diversity and abundanceat all mine sites. Heavy metals have also beenassociated with the total absence of earthworms(Genus-Scherotheca) from metal contaminatedsoils (Rida and Bouche, 1995) and such was thecase for the majority of pitfall traps located atmine sites in the present study, though earthwormswere encountered frequently in pitfalls at the ref-erence site. However, pitfall traps are not a partic-ularly efficient way of assessing earthwormabundance.Terrestrial gastropods, represented byArion ater

and Cepaea nemoralis, are responsible for theinitial breakdown of a significant proportion of thelitter pool and so form an important part of thedetritivorous as well as herbivorous fauna(Rus-sell-Hunter, 1983; Laskowski and Hopkin, 1996).However, though slugs and snails have beenreported as being relatively insensitive to elevatedlevels of metals in laboratory exposures(Las-kowski and Hopkin, 1996), they are often absentfrom highly polluted sites. This absence has beenattributed to delayed reproduction causing eventualextinction, although starvation-induced mortalitiesdue to the avoidance of contaminated foods is alsoan important factor (Laskowski and Hopkin,1996). Laskowski and Hopkin(1996) also high-light the importance of synergistic impacts frominteractions between metals in polymetallic wastewhen assessing the ecotoxicological risk to terres-trial molluscs. All mine tailings in this studydisplay this polymetallic character with relativelyhigh levels of cadmium and zinc.Given the importance of ground and soil-living

invertebrates to decomposition and nutrientcycling, the high levels of metals in the substratacould, through their impact upon invertebratediversity and abundance, emphasise deficiencies inthe labile pool of nutrients in the grassland eco-systems. This would add to the inherited problemscaused by the initially low concentrations of plantnutrients in the mine wastes at the time of depo-sition, especially in respect of nitrogen and phos-phorus. The net effect of retarded decompositionrates will be to further reduce the prospect ofdiversification through plant recruitment into thesystem at unmanaged sites. Along with the require-ment for metal tolerance, this must partly explain

the largely barren nature of historic abandonedmine sites, even 100 years after the termination ofwaste disposal.Members of the Carabidae family are thought

not to accumulate metals, and they have even beentermed ‘deconcentrators’(Dallinger, 1993). Levelsof lead greater than 20 mg kg have beeny1

recorded only rarely in field-caught animals(Hop-kin, 1989; Rabitsch, 1995a), although high con-centrations()600 mg kg ) have been reportedy1

in adult Carabidae, and also in Staphylinidae()1000 mg kg ) (Rabitsch, 1995a). The potentialy1

to bioaccumulate lead to very high concentrationsis evident in the present study. Specimens ofA.aulica with the highest concentrations of leadoriginated from the most contaminated sites butthere was no overall significant relationshipwr s2

0.45 (soil), r s0.15 (litter), ns7; P)0.05x2

between the lead burden of the beetles and soilylitter concentrations. The metal detoxificationmechanism that may enable beetles to survive insuch extreme habitats is the local accumulation oflead in cells or vesicles which are then excretedvia the faeces(Dallinger, 1993). In addition, Car-abids have also been found with 63–82% of totalbody lead deposited in the mainly chitinous exo-skeleton(Roberts and Johnson, 1978). Immobilis-ation of lead in this manner may constitute asecondary detoxification system that is broughtinto being when the primary mechanisms areoverloaded by extreme dietary lead intake.It is difficult to estimate the natural diet com-

ponents and therefore the intake–excretion dynam-ics of invertebrates. One exception is thegrasshopperChorithippus brunneus because of itssimple, grass dominated diet()90%). Moreover,C. brunneus forms an important part of the dietsof birds, small mammals and some larger inverte-brates so the metal accumulation dynamics of thisanimal are significant to food chain transfer atcontaminated sites(Hunter et al., 1987c). A sig-nificant relationship(r s0.60; ns11; P-0.05)2

was found between the concentration of lead inthe combined and averaged(1:1 wyw; Festuca:Agrostis; Table 3) grass diet and the whole bodiesof C. brunneus (Table 4).Carnivorous invertebrates are exposed to levels

of lead that reflect environmental levels as miti-


gated by the ability of their prey to physiologicallyregulate absorption and retention of the metal.Spiders assimilate only the soft tissues of theirprey, where most metals are stored preferentially,and are thus exposed to higher dietary concentra-tions of lead than other species(Hopkin, 1989).This is reflected inP. mirabilus which showedhigher lead concentrations than the herbivorousinvertebrates at all but one site.P. mirabilus feedson small, soft-chitinised insects including the Col-lembola and Isopoda which, although not analysedin this study, accumulate metals in line withenvironmental exposure(Hopkin, 1989). There isevidence thatP mirabilus and other lycosid spidersare sensitive to high soil metal contamination(Read et al., 1998). The harvestmanO. parietinusalso feeds on similar prey(Adams, 1984) and thiswas reflected in the body lead burdens being higherthan for any of the herbivorous invertebrates(Tables 4 and 5). This trophic pattern is similar tothat described elsewhere in respect of cadmiumfor which carnivorous taxa generally had higherconcentrations than species from lower trophiclevels(Hunter et al., 1987d).Tissue concentrations of lead in wild small

mammals are very much dietary dependant whichin turn means that exposure is via the transfer oflead in food chains(Ma, 1996). Generally, as inApodemus sylvaticus in this study, animals fromthe more contaminated sites showed the highestlevels of lead in soft tissues and, in some cases,concentrations were sufficient to induce clinicalsymptoms of lead toxicity based on precedent.Lead administered in drinking water has beenshown to induce the formation of renal nuclearinclusion bodies, increasedd-aminolevulinic acidexcretion, reticolocytosis, renal oedema, reducedsperm counts, irregular dioestrous, growth retar-dation and impaired learning in laboratory miceand rats, and similar observations have been report-ed for small mammals taken from contaminatedareas(Shore and Douben, 1994).Clinical signs of lead toxicosis appear to be

associated with relatively low concentrations of 5and 15 mg kg dry wt. in liver and kidneys,y1

respectively(Ma, 1996). Histological changes inkidney include altered proximal kidney tubularcells, oedema and nuclear inclusion bodies. In a

study by Ma(1989) the critical value of lead inthe kidneys of small mammals as regards nuclearinclusion bodies was 25 mg kg dry wt. Thisy1

figure was only exceeded at two of the historicWelsh mine sites suggesting a low probable inci-dence of lead poisoning on this criterion alone.However, another sensitive indicator of toxicolog-ical risk is the organ-to-body weight ratio(Ma,1989) and a comparison of the kidney weight asa proportion of total body weight(renal oedema)indicated that animals from Cwmsymlog(1.8%"0.1) and Frongoch(1.9%"0.1) were sig-nificantly different from the reference site(1.3%"0.0) (P-0.01). Cwmsymlog and Fron-goch were the sites with the highest kidney leadconcentrations both in excess of the 25-mg kgy1

‘threshold’ level. Roberts et al.(1978) also foundevidence of renal oedema in animals with a kidneylead concentration of 35–55 mg kg . Neithery1

Cwmsymlog nor Frongoch animals had elevatedkidney cadmium or zinc concentrations comparedto the reference site.In laboratory feeding trials, rats fed 200 mg

kg of lead in their diets exhibited increasedy1

relative kidney weight, along with the developmentof intranuclear inclusion bodies, although the kid-ney lead concentration was only 10.8 mg kgy1

(Mahaffey et al., 1981). These apparent conflictsin critical values for renal inclusion bodies andoedema highlight the large number of factors thatinfluence trace element metabolism including thedietary concentrations of other metals, total metalburden, age, period of exposure, and metaboliccondition.This study also confirms the importance of bone

and kidney as the major repositories for absorbedlead. For the reference site and Irish tailings, only4 and 6%, respectively, of the total body leadburden was located in these two tissues combined.However, at the most contaminated Welsh sitesthe bone and kidney account for between 16 and52%, respectively, of the body burden. Lead depos-ited in the skeleton of mammals poses a relativelylow toxicological risk as it is bound within thehydroxyapatiteycollagen bone matrix and is phys-iologically inert. Immobilisation of lead inhibitstranslocation within the body to metabolically


active centres where a toxicological response couldresult.Liver is the ‘first’ organ to encounter absorbed

dietary lead distributed via the bloodstream. Incontrast to kidney there is greater regulation ofhepatic lead in small mammals and, in a reviewof a number of studies, the lead concentrations inliver did not exceed 15 mg kg even when kidneyy1

values in the same individual animal were as highas 60 mg kg (Shore and Douben, 1994). How-y1

ever, concentrations of lead in liver found in thisstudy did not exceed 5 mg kg even when kidneyy1

values were of the order of 40 mg kg and thusy1

liver values here were lower than in most previousinvestigations at contaminated sites, and indeedsimilar to some reported reference site concentra-tions (Talmage and Walton, 1991). The reason forthese low liver values is not known and it isimprobable that the lead concentrations reportedhere would cause any disruption to normal hepaticfunctioning.Animals trapped, even at the centre of a large

contaminated area, may only be taking part oftheir food from highly polluted terrain. Attuquay-efio et al. (1986) found that small mammalsinhabiting unproductive but unpolluted ecosystemshad significantly larger(P-0.001) home ranges(12 290–36 499 m) than those inhabiting produc-2

tive and species-rich woodland(1719–6276 m).2

The low primary productivity of mine sites prob-ably means that animals may be forced to foragein adjacent areas of lower contamination, wherethe abundance of food is greater. The consequentialdilution of lead intake, as compared with exposureestimated by the analysis of dietary items takenonly from the contaminated site itself, may explainthe lack of correlation between dietary lead intakeand bodyytissue concentrations. A similar reduc-tion in metal loading when home ranges areincreased has been conceptualised for cadmium(Marinussen and Vanderzee, 1996).The data presented here indicate that lead is an

influential component of the mine tailings ecosys-tem. The interaction between lead and nutrientcycling is likely to be a major obstacle to whatnatural colonisation can be achieved on historicabandoned sites and even to the long-term sustain-ability of any reclamation scheme on modern sites.

For the modern Irish tailings, where an agriculturalend use for the reclaimed land has been tested andverified as an option(Brady, 1993), fertiliser inputwould be a normal management practise and wouldcircumvent problems of inhibited decompositionprocesses. For lower maintenance end uses includ-ing wildlife habitat, it may be that the regularinput of fertilisers to build-up a nutrient capital isall that is needed to achieve a sustainable ecosys-tem, albeit one with suppressed nutrient dynamicsand litter decomposition. Many species of inver-tebrate, fungi and bacteria have been reported astolerant to elevated levels of heavy metals(Tyleret al., 1989), and it might be possible to introduceselected species and populations from elsewhereto promote decomposition. This approach wouldparallel the use of tolerant grasses for providingan initial vegetation cover on metal-contaminatedmine wastes(Johnson et al., 1994).The concentrations of lead in tissues ofA.

sylvaticus provide evidence that there may be atoxicological risk associated with inhabiting someof the historic mine sites. Tissue concentrationsare certainly consistent with conditions that inducethe clinical symptoms of plumbism in small mam-mals. However, given the uncertainties in quanti-fying the many factors that determine whether thepotential for lead poisoning is realised in practice,and the fact that animals can emigrate from con-taminated areas to feed, the overall hazard to theviability of indigenous populations across themany hundreds of disused and abandoned sites isconsidered to be low. Moreover, the improvedmineral processing technology which is expressedin the lower levels of lead in tailings and mammalsfrom the modern Irish mine, suggests that thebenefits of technological change may eventuallybe reflected in the diversity, structure and function-ing of ecosystems established on mine wastes inthe future.

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