Ecological and Toxicological Effects of Exposure to an Acidic, Radioactive Tailings Storage

ECOLOGICAL AND TOXICOLOGICAL EFFECTS OF EXPOSURE TOAN ACIDIC, RADIOACTIVE TAILINGS STORAGE

JOHN READ and ROBYN PICKERINGEnvironmental Department, WMC Resources Ltd (Olympic Dam Corporation), P.O. Box 150,

Roxby Downs, South AustraliaE-mail: [email protected]

(Received 10 September, 1997; accepted in revised form 22 December, 1997)

Abstract. The persistence of an island of remnant vegetation within a tailings retention systemprovided an opportunity to conduct a pilot study to develop hypothesis concerning the impacts ofacid spray and radiation on arid zone flora and fauna. Ecological changes were investigated by com-paring species abundance and condition on both the study island and remote control areas. Hopbush(Dodonaea viscosa),geckos and a common ant species,Iridomyrmex rufonigersp. B were abundantin control regions but absent from the study region, whereas densities of colonising plant species,Heleabeetles and scorpions were unusually high at the impacted site. These disparities are proba-bly attributable to acid spray at the impacted site and hence are potentially useful bioindicators ofthese impacts. Dragon and skink populations were apparently unaffected by the polluted ecosystem,althoughCtenophorus nuchalisproved to be a significant bioaccumulator of radionuclides. Bioaccu-mulation of the radionuclides,238U, 230Th, 210Pb and particularly210Po were significantly greaterthan that reported elsewhere in the literature. Further radionuclide monitoring of herbivorous dragonspecies, possibly concentrating upon210Po levels, was the suggested outcome of this pilot study.

Keywords: ecological effects, radionuclide analysis

1. Introduction

Airborne acid is a major environmental problem in urban and industrial regions(Roberts, 1982; Barker and Tingey, 1992). Numerous studies have shown thatairborne acid can cause major physiological impacts upon organisms and resultin ecological effects to ecosystems (Newman and Schreiber, 1988; Armentanoand Bennett, 1992; Newmanet al., 1992; Kapusta and Reporter, 1993; Klumppet al., 1994). The identification of bioindicators of contamination in environmentswhere industries operate is particularly valuable since organisms integrate totalpollution levels over time better than spot-check measurements of atmosphericconcentrations (Napier, 1992; Hopkin, 1993).

Exposure to elevated radiation levels can also impact the health of terrestrialecosystems (Woodwell, 1963), although the nature of these impacts are often diffi-cult to measure and are subject to great variability (Woodheadet al., 1983). Effectson biota may be expressed as aberrations to behaviour (Brower, 1966; McMahan1970), reproduction (Maslovet al., 1966; Turneret al., 1971; Turner, 1975; French,

Environmental Monitoring and Assessment54: 69–85, 1999.© 1999Kluwer Academic Publishers. Printed in the Netherlands.

70 J. READ AND R. PICKERING

1965; French and Kaaz, 1968; Woodhead, 1977), pathology (Maslovet al., 1966;Ahmad and Taqawi, 1978; Jordanet al., 1978) or morphology (Maslovet al., 1966;Hanson, 1980). In extreme cases, exposure to high levels of radiation may resultin the death of individuals (Schnell 1964; Turner and Gist, 1970; Woodwell, 1962;Frenchet al., 1974; Dugle, 1985).

In some cases, populations of sensitive species may not exhibit detectable re-sponses to contamination (Arthuret al., 1986; Musselmanet al., 1992), particularlywhen other environmental conditions are favourable (French and Kaaz, 1968).Alternatively, impacts of increased exposure to radioactivity may be beneficialthrough enhancement of an organism’s immune system (Cohenet al., 1983) orgrowth rate (Cooley and Miller, 1971). Some tolerant plants and animals mayprosper in toxic environments (Turner, 1975; Alstadet al., 1982; Lang, 1989;Heliovaaraet al., 1990; Ying Pinget al. 1994). The abundance and conditionof different taxa may therefore be useful indicators of the extent and degree ofenvironmental impact from elevated levels of acid spray or radioactivity.

Environmental impacts of elevated levels of radiation from the nuclear energyindustry have attracted much attention (Halford and Markham, 1978; Miera andHakonson, 1978; Dreeson and Marple, 1979; Arthur and Markham, 1984; Koper-ski and Bywater, 1985; Cristaldiet al., 1985; Arthuret al., 1986; Cloutieret al.,1986; Read and Tyler, 1994). The major pathways of radiation into the biologicalenvironment are from direct exposure to external gamma radiation, inhalation ofradon daughters and radioactive particulates, and ingestion of radioactive particu-lates (ICRP 1965; 1978). Alpha, beta and gamma radiation is released when238Udecays through intermediate products to form stable206Pb.210Pb and210Po, whichare products of this process, also occur naturally through the decay of atmospheric222Rn gas, and hence natural systems are exposed to background levels of radiation.Radionuclide accumulation rates vary in different species (Dreeson and Marple,1979) and may biomagnify through trophic levels. Determination of uptake lev-els in different taxa may identify bioindicators which can be used to assess thecondition of contaminated ecosystems.

1.1. STUDY SITE

This study investigated the ecosystem response and radionuclide levels in an iso-lated community subjected to acid spray and elevated radiation levels at the OlympicDam copper, uranium, gold and silver mine, 520 km north of Adelaide in arid SouthAustralia. The Olympic Dam region experiences hot summers and low erratic rain-fall with an annual average of 168 mm (Read, 1995a). Ore is processed on siteand tailings are deposited in a Tailings Retention System (TRS). The TRS is asignificant source of radon emissions (Harris and Chandler, 1992) and a source ofacid spray due to the low pH of the tailings liquor. The standard man equivalentradiation dose within the TRS of 12.4 mSv y−1∗ is within the range of doses from

∗ Derived from data reported in ODO, 1994.

ECOLOGICAL AND TOXICOLOGICAL EFFECTS 71

large regions of elevated natural radiation but is high in comparison to the averageworldwide background of 2.4 mSv y−1 (UNSCEAR, 1988). Contamination at a siteone km to the south-east of the TRS is minimal, with a standard man equivalentdose of 0.2 mSv y−1above a local background of only 1.5 mSv y−1∗. Therefore,typical radiation doses at Olympic Dam beyond the TRS, are lower than averageworldwide doses and probably have no impact upon the ecosystem.

In April 1994 a 2.5 ha vegetated linear sand dune, which had been isolatedin the 185 ha TRS for approximately 15 months, was removed. The island wasseparated from surrounding vegetation by at least 100 m of wet tailings and the10 m wide rock wall of the tailings dam which formed an effective dispersal bar-rier for invertebrates, reptiles and small mammals. The plants on this island hadbeen exposed to windborne acid spray and elevated levels of radionuclides fromthe tailings. Acid spray, with a pH of 0.7–1.0, was particularly prevalent whenwindspeed exceeded 22 kph, which occurred on 13% of the half hour recordingsfrom a nearby weather station. The entire island was exposed to this spray due toits narrow, low topography. Fauna radiation doses were probably even higher thanvegetation doses because ingestion of radionuclides in dust on their food is a majorradiation exposure pathway (ICRP, 1965; 1978).

1.2. AIMS

The removal of the TRS island provided a timely opportunity to develop hypothe-ses concerning the ecological and biological effects of acid spray and elevatedradiation levels in an arid environment. Because a range of complimentary indi-cators is usually required for comprehensive monitoring programs (Landreset al.,1988; Noss, 1990; Kremenet al., 1993), we hoped to identify several taxa whichcould be developed as bioindicators. In addition, we document the radionuclidesampling, separation and analyses methods used at Olympic Dam and place thelocal environmental radionuclide levels in perspective with global levels.

2. Methods

2.1. SAMPLING

A composite soil sample from the top 10 cm, was collected along with four plantspecies from three sites on the island within the TRS and from three control sites,at least five km from the TRS. The top 10 cm of soil was considered to be themost representative soil exposure source to both the burrowing and feeding zone ofanimals and the surface root systems of plants. Four plant species,Acacia ligulata,Crotalaria eremaea, Sida ammophilaand Paractaenum novae-hollandiae, werechosen for radionuclide analysis because they were common on the TRS islandand they represented a variety of plant forms which potentially differ in uptake ofradionuclides. At least five plants were used to produce a composite 50 g sample for


each species, per site. Airborne dust was collected continuously, at a site one kmsouth-east of the TRS and at a control site 6.3 km south-east of the TRS, usinghigh volume dust samplers and sampled at monthly intervals. Data were averagedover the time period between commissioning of the TRS and when the dune wasremoved. These high volume dust samplers were installed primarily to measuredust levels at the average human breathing height, hence only provide indirectevidence of ground level dust dispersion from the TRS.

Animals were hand caught on the island by active searching during the day andnight. In addition 15 pitfall traps and 25 baited Elliot mammal traps were set onthe island for 14 days in March 1994, when maximum temperatures ranged from31–36 ◦C and minimum temperatures ranged from 13–21◦C. Where possible,replicates of each species trapped within the TRS island were collected oppor-tunistically from remote control sites. The control individuals were trapped in theOlympic Dam region but in all cases further than 3 km from the TRS. The TRSisland ant community was sampled with nine rows of four micro-pitfall traps, onequarter filled with ethylene glycol. Ants were sorted to species level, counted, andthe data transformed to abundance classes. Full details of trapping and analyticalmethods as well as the taxonomy of the ants is presented elsewhere (Read, 1996).

2.2. SAMPLE PREPARATION

Soil samples were dried in an oven at 105◦C. A 5 g sub-sample was taken andtracers and lead carrier added. The sample was digested in hydrofluoric acid andthen nitric acid for five days. The resulting solution was evaporated and made tovolume in a solution of dilute hydrochloric acid in a volumetric flask.

With the exception of theS. ammophila, all of the vegetation was thoroughlywashed prior to drying to remove radioactive dust that may have contaminated thesamples.Sida ammophilaleaves are important to the diet of herbivorous agamids(pers. obs.) and dust trapped on the leaves may be an important radionuclide expo-sure pathway for these species. Vegetation samples were dried in an oven at 55◦C.Radioactive tracers and lead carrier were added to a 5 g sub-sample. The sampleswere digested in nitric acid, filtered and then further digested in a mixture of nitricand perchloric acids for six days. The solution was then evaporated and made tovolume in a volumetric flask.

Reptiles were weighed to the nearest 0.1 g, measured and checked for defor-mities. Sand-sliders (Lerista labialis) were not measured due to the difficulties inaccurately measuring and weighing these small lizards. The snout-vent length toweight ratio of all other species was used as an indication of their body condition(Schwarzkopf, 1991) or health. This ratio was compared with control reptile in-formation, gathered at Olympic Dam from 1989 to 1995, using t-tests. Specimenswere either released on a nearby dune or euthanised by cold necrosis, after a twoday period to clear their digestive tract of insoluble radionuclides, and preparedfor laboratory analysis. TheMus domesticusand most skinks and dragons were


prepared whole so that reasonable radionuclide detection limits could be obtained.The largeCtenophorus nuchalistails were analysed separately to the rest of thebody to determine relative radionuclides accumulation in organs and bone/flesh.Tiliqua rugosaspecimens, being even larger, were dissected into bone and liversamples. Previous analyses at Olympic Dam showed that these areas of the bodyaccumulated larger amounts of radionuclides than flesh. All samples were weighedand washed before tracers and lead carrier were added and treated as per thevegetation samples.

2.3. RADIONUCLIDE ANALYSIS

All digested samples were prepared and counted in the same manner using thestandard techniques of the Olympic Dam Corporation (ODC) Environmental Lab-oratory. An aliquot was taken for226Ra analysis by the radon de-emanation method(APHA et al., 1985). Another aliquot was taken for210Po,210Pb,238U and230Thseparation and analyses. Separation of the radionuclides of interest was undertakenusing a combination of precipitation, organic extraction, and ion exchange. Theseparation method was derived from the work of Brown and Ring (1988), Lowsonand Short (1986), Grimaldi (1961), and Talvitie (1972). The radionuclides of inter-est were then auto-deposited (210Po), electro-deposited (238U, 230Th) or precipitatedonto disks (210Pb) for counting. Alpha spectroscopy was used to analyse210Po,238U and230Th, while 210Bi was analysed by beta counting to determine the210Pbactivity.

Trophic level concentration factors from soil to vegetation (CFsv) and from soilto fauna (CFsf) were calculated using the following equations:

CFsv = (Activity of isotope in vegetation)/(Acitivity of isotope in soil) (1)

CFsf = (Activity of isotope in fauna)/(Activity of isotope in soil) (2)

Concentration factors for226Ra were not calculated, as the radionuclide activitywas below detectable limits in all cases.

2.4. OTHER DATA COLLECTED

Dust collected from high-volume air samplers and tailings liquor samples was rou-tinely collected from the TRS area as part of ODC’s Environmental ManagementProgramme (ODO, 1994). Data from these two sampling schemes were used toprovide information on the characteristics of the contaminants at the TRS.


TABLE I

Vertebrates recorded from the island within the OlympicDam Operations TRS

Species Number

Reptiles Ctenophorus fordi 1 (2)

Ctenophorus nuchalis 2

Varanus gouldii (1)

Ctenotus brooksi 1

Ctenotus leae 1

Ctenotus regius 2

Eremiascincus richardsonii 1

Lerista labialis 8

Tiliqua rugosa 1

Mammals Oryctolagus cuniculus (1)

Felis catus (1)

Mus domesticus 1

Birds Poephila guttata (5)

Malurus lamberti (3)

Tringa stagnatilis (1)

N.B.: Numbers in parentheses represent individuals that wereobserved but not captured.

3. Results

3.1. ECOLOGICAL IMPACTS

The dominant vegetation on the island wasAcacia ligulatawith an understoreyof Salsola kali, Nicotiana velutina, Sida ammophila, Boerhavia dominii, Parac-taenum novae-hollandiaeand scatteredLycium australe. All specimens ofDodon-aea viscosa,a dominant shrub on the dune prior to inclusion within the TRS, haddied prior to sampling. The remaining vegetation appeared to be healthy and notimpacted by the proximity of the tailings.

Nine reptile, three mammal and three bird species were recorded on the TRSisland (Table I). The most striking feature of the reptile community was the absenceof geckos, which are usually second only to skinks as the dominant reptile groupin the region (Read, 1992; 1995b). All mammals recorded were exotic, and thebird fauna were extremely depauperate, considering that 160 species have beenrecorded from the Olympic Dam region (Read, 1994).


TABLE II

Snout-vent length/weight ratios for TRS specimens and controlspecimens of equivalent length

Species TRS SVL/ Control SVL/ Control

WT ratio WT ratio mean number

E. richardsonii 13.16 (∗) 8.93 9

C. regius #1 12.45 (ns) 12.48 187

C. regius #2 11.92 (ns) 12.74 222

T. rugosa 0.59 (ns) 0.52 7

C. leae 23.63 (ns) 19.28 6

C. nuchalis #1 5.17 (ns) 3.77 11

C. nuchalis #2 4.13 (ns) 4.41 16

C. brooksi 26.47 (ns) 26.93 18

C. fordi 13.43 (ns) 13.73 45

∗ = Significantly different from controls at p = 0.05%, ns = notsignificantly different from controls.

The snout-vent length/weight ratio of eight of the sampled reptiles was notsignificantly different (p>0.05) from the mean control snout-vent length/weightratio of individuals of the same species from elsewhere in the Olympic Dam region(Table II). Only theEremiascincus richardsoniispecimen from the TRS islandwas significantly lighter than control specimens of similar length. Morphologi-cal aberrations amongst the TRS reptiles were restricted to one Ford’s Dragon(Ctenophorus fordi) which was missing ten claws and a Central Netted Dragon(Ctenophorus nuchalis)with a missing toe. Several other toes on the same indi-viduals were also withered. Since less than 1% of the 700 dragons caught in thecontrol region had missing toes (pers. obs.), the two abnormal dragons from threecaught on the island are unlikely to be attributable to chance.

In excess of 250 tenebrionid Pie-dish beetles (Heleasp.), along with 10 scorpi-ons (Lycas alexandrinus) were recorded in the large pitfall traps, making them themost abundant invertebrates sampled with the exception of ants. Eighteen speciesof ants were recorded in the micro-pitfall traps (Table III). An additional species,Camponotus aurocincta, was observed on the island but not recorded in the sample.

3.2. RADIONUCLIDE ACTIVITIES

The tailings liquor surrounding the island was highly acidic and contained highconcentrations of radionuclides, particularly238U and 230Th (Table V). Airbornedust in the area was characterised by radionuclide activities 2–6 times that mea-sured at control sites (Table V). Radionuclide exposures from airborne dust areexacerbated at the TRS because the average dust concentration in the vicinity of


TABLE III

Total abundance score of ant species recorded from the islandwithin the Olympic Dam Operations TRS

Subfamily Species Abundance

score

Ponerinae Rhytidoponera metallica 2

Myrmicinae Pheidole G 7

Tetramorium C 2

Monomorium C 3

Monomorium sordidumgp 26

Monomorium F 2

Monomorium H 3

Dolichoderinae Iridomyrmex rufonigersp C 5

Iridomyrmex rufonigersp D 13

Iridomyrmex discors 42

Iridomyrmex rufonigersp C 2

Iridomyrmex dromus 3

Iridomyrmex bicknellisp G 30

Iridomyrmex bicknellisp SA 1

Iridomyrmex viridiaeneus 3

Formicinae Melophorus B 36

Melophorus DE 28

Melophorus I 4

Camponotus aurocincta ∗

∗ = Observed on the TRS but not represented in samples.

the TRS was 43µg m−3 compared with 31µg m−3 at control sites.226Ra activitiesin all samples were below detectable limits and will not be discussed further.

Soils on the TRS island were slightly enriched in230Th and238U, but not in theother measured radionuclides (Table IV). Vegetation samples from the TRS exhib-ited a two to ten fold increase in activity of all radionuclides compared to controls(Table IV). Activities of 238U and 230Th in unwashedSida ammophila, sampledfrom the island, was an order of magnitude higher than those from control sites.Most of the reptile radionuclide activities from the TRS were undetectably differentor only marginally higher than control levels (Table IV). A notable exception wasCtenophorus nuchaliswhich was a significant accumulator of all radionuclides.Activities of 238U, 230Th and210Po in the tail samples ofC. nuchaliswere higher


TABLE IV

Means and counting errors for radionuclide analyses

Nr. of 238U 230Th 226Ra 210Pb 210Po

samples

(Bq kg−1)

Soil Control 3 2.3±0.5 7.9±1.7 <17 7.2±2.3 5.9±1.7

Tailings 3 3.5±0.04 17±5 <17 5.9±0.8 5.1±2.4

Acacia Control 3 <2 <5 <18 13±1.3 <3

Tailings 3 5.2±0.5 23±5 <18 40±16 8.7±1.6

Crotalaria Control 3 <2 <5 <18 <10 <2

Tailings 3 14±12 21±16 <18 30±12 6.3±6.8

Paractaenum Control 3 <2 <5 <18 11±8 1.2±1.7

Tailings 3 15±11 31±24 <18 22±4 6.0±8

Sida Control 3 <2 <5 <18 10±8 <2

Tailings 3 32±4 54±10 <18 28±7 15±3

C. nuchalis Control 2 <4 <3 <17 <6 6.0±2.7

(body) Tailings 2 21±0.2 14±7 <17 9.9±6.5 110±20

C. nuchalis Control 2 <4 <3 <17 <6 13±6

(tail) Tailings 2 56±0.2 33±7 <17 38±7 550±20

T. rugosa Control 1 <1 <1 <17 34 35

(bone) Tailings 1 4 0.6 <17 13 12

T. rugosa Control 1 <1 0.1 <17 <3 11

(liver) Tailings 1 <1 0.1 <17 6.7 3.1

C. regius Control 1 <4 <1 <17 <3 2.3

Tailings 2 4±2 <3 <17 <3 <7

C. fordi Control 1 <4 <3 <45 <6 <7

Tailings 1 9 2 <17 <3 19

C. brooksi Tailings 1 7 5 45 <6 <20

C. leae Tailings 1 1.3 <3 <45 <6 <20

Mus Control 1 <5 <5 <6 <3 4.1

Tailings 1 1.5 0.5 <6 <6 4.4

Note: Activities in flora are expressed as Bq kg−1 dry weight and activities in fauna areexpressed as Bq kg−1 wet weight.

than other activities recorded in the biological samples in this survey and were morethan an order of magnitude higher than control samples. Radionuclide activities intheMus domesticussample were low and not detectably different from the controlsample (Table IV). Polonium to lead ratios were much higher than one in theC.nuchalissamples but were less than parity for all plant samples.


TABLE V

Analyses of tailings liquor and mean airborne dust activities

Tailings Tailings site Control site

liquor airborne dust airborne dust

pH 0.7–1.0 – –

SO2−4 96–140 g L−1 – –

238U 1100 Bq L−1 500 Bq kg−1 120 Bq kg−1

230Th 3400 Bq L−1 830 Bq kg−1 110 Bq kg−1

226Ra 2.2 Bq L−1 500 Bq kg−1 130 Bq kg−1

210Pb 280 Bq L−1 21 000 Bq kg−1 13 000 Bq kg−1

210Po 85 Bq L−1 17 000 Bq kg−1 5 100 Bq kg−1

Total dust – 43µg m−3 31µg m−3

TABLE VI

Calculated concentration factors from soil to vegetation (sv) and soil to fauna (sf) and factors thathave appeared in other publications

Radionuclide CFsv CFsf

This study Published data This study Published data

238U 2.3–9.1 0.05–0.08 (M) 0.37–10.9 4×10−5–2×10−3 (L)230Th 1.2–3.2 – 0.02–1.4 2×10−5–4×10−4 (L)210Pb 1.4–5.6 8×10−4 (V)–0.3 (Mc) 1.70–4.1 –210Po 0.2–2.9 0.03–0.56 (A) 0.39–43 0.02 – 0.22 (A)

(L) = Linsulataet al.1991, (V) = Vasconcelloset al.1987, (W) = Whitehead and Brooks 1971, (A)= Arthur and Markham 1984, (M) = Mieraet al.1980, (Mc) = McDowell-Boyeret al.1980.

3.3. TROPHIC LEVEL CONCENTRATION FACTORS

The concentration factors from soil to both vegetation and fauna were typicallyin the range from 0.2 to 10 for all radionuclides (Table VI). These figures wereconsiderably higher than most trophic level concentrations reported in the literature(Table VI). With the exception of210Po, which was greatly magnified in some faunasamples, there was little evidence of biomagnification of other radionuclide levelsin fauna samples in relation to vegetation samples.


4. Discussion

4.1. ECOLOGICAL IMPACTS

The dramatic decline ofDodonaea viscosawas the most obvious impact to thevegetation on the TRS island. The death of severalD. viscosaindividuals due toleaf necrosis has been recorded at other sites at Olympic Dam with elevated SO2

concentrations (Fatchen and Associates, 1989) and the demise of this species wastherefore probably due to exposure to acid spray rather than elevated radionuclidelevels. All other species on the island, with the exception ofLycium australeandSida ammophila, were characteristic colonisers of disturbed sand habitats in theregion. Studies elsewhere have suggested that ‘weedy’ communities are consider-ably more tolerant to radiation exposure than more stable communities (Woodwell,1963).

The persistence of a lizard community on the contaminated island indicatesthat certain species exhibit tolerance to acid spray and elevated levels of radionu-clides. The agamid community is particularly noteworthy.Ctenophorus fordiandC. nuchalisseldom live longer than one year (Cogger, 1969; Bradshaw, 1965) andhence probably hatched and developed to maturity on the TRS island. The shortlifespan of the agamids tends to protect these species from long-term cumulativeeffects of radiation (Frenchet al., 1974). However, whileC. nuchaliswas tolerantof elevated radiation levels, the sampled individuals accumulated significant lev-els of radionuclides, and hence this species is potentially a useful biomonitor ofenvironmental radiation levels.

The missing toes in the two dragon specimens are unlikely to represent devel-opmental abnormalities, since although the remaining digits were also affected,their bone structure was normal. Therefore, the digits were apparently impactedfollowing bone development via an external perturbation. The most likely cause ofthese missing claws and withered, brittle toes is the acidic environment in which thedragons lived. An alternative scenario was that radium may have partially replacedcalcium in the bones, thus rendering them brittle (Cember, 1983). This hypothesiscould not be tested since the degree of replacement of calcium by radium wasnot investigated in this study. Maslovet al. (1966) reported that the fatness ofanimals decreased with increasing radiation dose. The low fat levels, indicated bya low snout-vent length/weight ratio, which was evident in one of the TRS lizards,may therefore imply that the dose received was sufficient to affect the individual’shealth. Alternatively, low body condition in this individual may have resulted fromunconnected health problems or reduced food availabilty on the island. Geckoswere apparently absent from the island, despite being common constituents ofthe local herpetofauna. Temperatures during the study period were warm to hotand hence the activity of no reptiles was limited by temperature. The absence ofgeckos was likely to be a result of the elevated levels of acidic mist in the regionwhich would impact soft-skinned nocturnal lizards with large eyes more readily


than small-eyed diurnal skinks and dragons with tougher skin. Geckos regularlylick their eyes and face (Bustard, 1963), especially prior to and following feeding(Greer, 1989; pers. obs.), which would also increase their exposure and aversion toairborne noxious substances.

The paucity of birds in the TRS is likely to result from a lack of suitable habitator drinking water. Due to the utilisation of contaminated grit in their gizzards,many bird species can be significant accumulators of radionuclides (Mellinger andSchultz, 1975), but their mobility renders them unsuitable for radionuclide analysisbecause their exposure time is difficult to establish. Unlike less mobile terrestrialvertebrates, the absence of bird species within the TRS does not indicate an intol-erance to prolonged exposure to elevated radionuclide levels. Therefore, birds areunlikely to be useful indicators of relatively confined environmental contamination.

Mus domesticusis relatively resistant to chronic radiation (Turner, 1975) andhas been used extensively as a biological indicator of environmental stress includ-ing elevated radiation levels (Cristaldiet al., 1985). However, due to the low levelsof radionuclides in the sampled individual and natural variability in population size(Read, 1992),M. domesticusare unlikely to be useful ecological or radionuclidebioaccumulating indicators at Olympic Dam.

The TRS ant community was relatively diverse, and most of the common dunetaxa recorded at other localities at Olympic Dam (ODO, 1994) were represented.A notable anomaly in the TRS ant community was the absence ofIridomyrmex ru-fonigersp. B, the dominant ant species at many undisturbed dune sites at OlympicDam (Read, 1996). This supports the finding of an earlier study thatI. rufonigersp. B is replaced by opportunistic or generalised species in chemically-stressedenvironments (Read, 1996). Since ants are relatively radioinsensitive insects (Coleet al., 1959), acid spray is likely to be the major factor suppressingI. rufoniger sp.B populations, possibly due to impacts to their homopteran food source.

The exceptionally high numbers ofHelea beetles and scorpions suggest thatthese invertebrates may be useful positive indicators of chemically stressed sitesat Olympic Dam. Alternatively, densities ofHeleaand scorpions may have beena result of the apparent absence of Central Knob-tailed Geckos (Nephrurus levis),which are normally relatively common on dunes in the region and are a predator ofthese invertebrates (pers. obs.). Alstadet al. (1982) and Yingpinget al. (1994)reported several different cases where insect populations increased in pollutedregions, either because predator numbers were reduced or because stressed vege-tation was susceptible to insect attack. Therefore, the acidic environment probablyeither directly or indirectly influenced populations of beetles and scorpions.

4.2. RADIATION SOURCES

Emissions from the anode furnace stacks of the ODC processing plant increased210Pb and210Po levels at the TRS above natural background (Table V). The elevatedlevels of 238U and 230Th at the study site are a result of TRS dust resuspension


from the dry tailings surface and containment in acid droplets which mist from thetailings liquor (Table V).

4.3. CONCENTRATION COMPARISONS AND ACCUMULATION

Radionuclide levels determined in this study were generally comparable with thosereported in the literature from both contaminated and natural regions (Holtzman,1966; Arthur and Markham, 1984; Koperski and Bywater, 1975; Read and Tyler,1994). Only the210Pb and210Po activities inCtenophorus nuchalissamples ex-ceeded reported activities with the exception of those in caribou (Holtzman, 1966;Thomaset al., 1994). Elevated levels of radionuclides, particularly210Po in C.nuchalis, indicate that this species may be a considerable bioaccumulator of ra-dionuclides. Although dietary preferences can have a major influence on the in-gestion and exposure of particular species to toxic elements (Hunteret al., 1989),intraspecific differences in activity, behaviour and home range also influence ra-dionuclide accumulation (Osborn, 1966; Halford and Markham, 1978). Most ofthe radionuclides probably originated from the diet ofC. nuchaliswhich consistspredominantly of the fruit, flowers and leaves of green plants, includingSida am-mophila,and insects (pers. obs.). Another local dragon species with a similar dietto C. nuchalisis the Bearded Dragon (Pogona vitticeps). Although not sampled inthis study,P. vitticepsis likely to be an important bio-indicator of low-level radia-tion because individuals live for over four years, and long-lived lizards potentiallyaccumulate more radionuclides (Turner, 1975) and receive a larger cumulative dosethan short-lived species.

Trophic level concentration factors for this study were considerably higher thanin other studies (Table VI), which may be attributable to the acidic soil or thephysiological condition of the local plants McDowell-Boyeret al. (1980). Theplants with low concentration factors studied by Mieraet al. (1980) and Vascon-celloset al. (1987) were vegetable crops, which would have higher water uptakeand transpiration rates than the arid-adapted plants in this study (Burrows, 1986).Similarly, the farm animals studied by Linsalataet al. (1991) in Brazil would havehad less physiological adaptations to reduce water loss and hence a higher potentialto flush radionuclides than the fauna at Olympic Dam. The210Po to210Pb ratio ofgreater than one recorded in the TRSC. nuchalissamples, is comparable to ratiosreported elsewhere (Arthur and Markham, 1984; Holtzman, 1966; Thomaset al.,1994), which provides further evidence that210Po is not flushed as readily as210Pbfrom the body.

5. Conclusions

This pilot study identified several interesting trends which can be used to generatehypotheses which can be tested with sufficient replication and control to permit


statistical verification. The negative response ofDodonaea viscosa, geckos andIridomyrmex rufonigersp B, along with the increase inHeleaand scorpions war-rant further research as bioindicators of SO2 impacts at Olympic Dam. Digit andweight loss in reptiles in the contaminated environment were inconclusive in thisstudy but should be noted in further studies. Bioaccumulation of radionuclidesby herbivorous agamids suggest that this group is more likely to provide usefulinformation on the degree and extent of environmental radionuclide contaminationthan soil, plants or other fauna. Finally, Polonium was identified as the radionuclidemost likely to be accumulated by fauna.

Acknowledgements

This study was supported by WMC Resources Ltd (Olympic Dam Corporation).Tim Harrington and Nick Reid provided useful comments on an earlier draft of thismanuscript. Thanks also to Colin Nicholls who prepared the samples and separatedthe radionuclides of interest for analysis.

References

Ahmad, M. and Taqawi, I. H.: 1978, ‘Radiation induced leukemia and leucopenia in the lizardUromastix hardwickii’, Radiobiology and Radiotherapy3, 353.

Alstad, D. N., Edmunds Jr., G. F. and Weinsein, L. H.: 1982, ‘Effects of air pollutants on insectpopulations’,Ann. Rev. Ent.27, 369.

American Public Health Association: 1985, ‘American Water Works Association and Water PollutionControl Federation’,Standard Methods for the Examination of Water and Wastewater, AmericanPublic Health Association.

Armentano, T. V. and Bennet, J. P.: 1992, ‘Air Pollution Effects on the Diversity and Structureof Communities (Ch. 9)’, in: Barker, J. R. and Tingey, D. T. (eds.),Air Pollution Effects onBiodiversity, Van Nostrand Reinhold, New York.

Arthur, W. J. and Markham, O. D.: 1984, ‘Polonium-210 in the environment around a radioactivewaste disposal area and phosphate ore processing plant’,Health Physics46, 793.

Arthur, W. J., Markham, O. D., Groves, C. R., Keller, B. L. and Halford, D. K.: 1986, ‘Radiationdose to small mammals inhabiting a solid waste disposal area’,J. Appl. Ecol. 23, 13.

Barker, J. R. and Tingey, D. T.: 1992,Air pollution effects on biodiversity, Van Nostrand Reinhold,New York.

Bradshaw, S. D.: 1965,The Comparative Ecology of Lizards of the Genus Amphibolurus, PhD. thesis.Univ. of West. Australia, Nedlands, W.A.

Broadway, J. A. and Strong, A. B.: 1983, ‘Radionuclides in human bone samples’,Health Physics45, 765.

Brower, J. H.: 1966, ‘Behavioural changes in an ant colony exposed to chronic gamma irradiation’,American Midland Naturalist75, 530.

Brown, S. A. and Ring, R. J.: 1988,Analytical Methods for the Determination of Lead-210 andPolonium-210 in Feed and Product Materials from the Olympic Dam Project, A report to RoxbyManagement Services, ANSTO.

Burrows, W. H.: 1986, ‘Potential Ecosystem Productivity’, in: Sattler, P. S. (ed.),The Mulga Lands,Royal Society of Queensland.

Bustard, H. R.: 1963, ‘Gecko behavioural trait: tongue wiping spectacle’,Herpetologica16, 1.


Cember, H.: 1983,Introduction to Health Physics, second ed. Pergamon Press.Cloutier, N. R., Clulow, F. V., Lim, T. P. and Dave, N. K.: 1986, ‘Transfer coefficient of Ra226 from

vegetation to Meadow Voles,Microtus pennsylvanicus, on U mill tailings’, Health Physics50,775.

Cogger, H. G.: 1969,A study of the ecology and biology of the Mallee Dragon (Amphibolourus fordi)and its adaptions to survival in an arid environment, PhD. Thesis. Macquarie Univ.

Cohen, J. J., Smith, C. F. and Luckey, T. D.: 1983, ‘Indicators of Possible Beneficial Effects of Low-Level Radiation’, in:Biological Effects of Low-Level Radiation, International Atomic EnergyAgency. Vienna, pp. 611–612.

Cole, M. M., LaBrecque, G. C. and Burden, G. S.: 1959, ‘Effects of gamma radiation on some insectsaffecting man’,J. of Economic Entomology52, 448.

Cooley J. L. and Miller, F. L.: 1971, ‘Effects of chronic irradiation on laboratory populations of theaquatic snailPhysa heterostropha’, Radiation Research47, 716.

Cristaldi, M., Ieradi, L. A., Licastro, E., Lombardi Boccia, G. and Simeone, G.: 1985, ‘Environmentalimpact of nuclear power plants on wild rodents’,Acta Zool. Fennica173, 205.

Dreesen, D. R. and Marple, M. L.: 1979, ‘Uptake of trace elements and radionuclides from Ura-nium mill tailings by Four-wing Saltbush (Atriplex canescens) and Alkali Sacaton (Sporobolusairoides)’, Symposium on Uranium Mill Tailings Management, Fort Collins, Colorado, ColoradoState University.

Dugle, J. R.: 1985, ‘Growth and morphology in Balsam Fir: effects of gamma radiation’,CanadianJ. Botany64, 1484.

Fatchen and Associates: 1989, ‘Olympic Dam vegetation monitoring’ General Report, November1989 – December 1990. Olympic Dam Operations, Olympic Dam.

French, N. R.: 1965, ‘Radiation and animal populations: problems, progress and projections’,HealthPhysics11, 1557.

French, N. R. and Kaaz, H. W.: 1968, ‘The intrinsic rate of natural increase of irradiatedPeromyscusin the laboratory’,Ecology49, 1172.

French, N. R., Maza, B. G., Hill, H. O., Aschwanden, A. P. and Kaaz, H. W.: 1974, ‘A populationstudy of irradiated desert rodents’,Ecological Management44, 45.

Greer, A. E.: 1989,The biology and evolution of Australian lizards, Surrey Beatty, Chipping Norton,Australia.

Grimaldi, F. S.: 1961, ‘Thorium’ in: Kothoff, I. M. and Elving, P. J. (eds.),Treatise on AnalyticalChemistry Part II Analytical Chemistry of the Elements, Interscience,5.

Halford, D. K. and Markham, O. D.: 1978, ‘Radiation dosimetry of small mammals inhabiting aliquid radioactive waste disposal area’,Ecology59, 1047.

Hanson, W. C.: 1980, ‘Ecological Considerations of Natural and Depleted Uranium’, in: Gesell, T.F. and Lowder, W. M. (eds.),Natural Radiation Environment III. Technical Information Center.U.S. Department of Energy, pp. 1682–1697.

Harris, F. F. and Chandler, W. P.: 1992, ‘Release of airborne radionuclides from Olympic DamOperations and exposure assessment for members of the public’,Rad. Prot. Aust.10, 15.

Holtzman, R. B.: 1966, ‘Natural levels of lead-210, polonium-210 and radium-226 in humans andbiota of the Arctic’,Nature210, 1094.

Hopkin, S. P.: 1993, ‘In Situ Biological Monitoring of Pollution in Terrestrial and Aquatic Ecosys-tems (Ch. 20)’, in: Calow, P. (ed.),Handbook of Ecotoxicology, Blackwell Scientific Publications,Oxford.

Hunter, B. A., Johnson, M. S. and Thompson, D. J.: 1989, ‘Ecotoxicology of Copper and Cadmiumin a contaminated grassland ecosystem’,J. Appl. Ecol.8(26), 89.

ICRP: 1965, Principles of environmental monitoring relating to the handling of radioactivematerials, Publication 7, International Committee on Radiation Protection.

ICRP: 1978,Radioactive release into the environment: Assessment of doses to man, Publication 29,International Committee on Radiation Protection.


Jordan, S. W., Yuhas, J. W. and Key, C. R.: 1978, ‘Late effects of unilateral radiation on the mousekidney’ Radiation Research76, 429.

Kapusta, L. A. and Reporter, M.: 1993, ‘Terrestrial Primary Producers (Ch. 14)’, in: Calow, P. (ed.),Handbook of Ecotoxicology, Blackwell Scientific Publications, Oxford.

Klumpp, A., Klumpp, G. and Domingos, M.: 1994, ‘Plants as bioindicators of air pollution at theSerra Do Mar near the industrial complex of Cubatao, Brazil’,Environmental Pollution85, 109.

Koperski, J. and Bywater, J.: 1985, ‘Radionuclide analysis of bush food’,Rad. Prot. Aust.3, 80.Kremen, C., Colwell, R. K., Erwin, T. L., Murphy, D. D., Noss, R. F. and Sanjayan, M. A.: 1993,

‘Terrestrial arthropod assemblages: their role in conservation planning’,Conserv. Biol.7, 796.Landres, P. B., Verner, J. and Thomas, J. W.: 1988, ‘Ecological uses of vertebrate indicator species:

A critique’, Conserv. Biol.2, 316.Linsalata, P.: 1991, ‘Th, U, Ra and rare earth element distributions in farm animal tissues from an

elevated natural radiation background environment’,J. Environ. Radioactivity14, 233.Lowson, R. T. and Short, S. A.: 1986, ‘Analysis for the Radionuclides of the Uranium and Thorium

Decay Chains with Special Reference to Uranium Mine Tailings’, Australian Atomic EnergyCommission report e611.

Maslov, V. I., Maslova, K. I. and Verkhovskaya, I. N.: 1966, ‘Characteristics of the RadioecologicalGroups of Mammals and Birds of Biogeocoenoses with High Natural Radiation’, in: Aberg, B.and Hungate, F. P. (eds.),Radioecological Concentration Processes, Permagon Press. Oxford,pp. 561–571.

McDowell-Boyer, L. M., Watson, A. P. and Travis, C. C.: 1980, ‘A Review of Parameters DescribingTerrestrial Food-Chain Transport of Lead-210 and Radium-226’,Nuclear Safety2, 486.

McMahan, E. A.: 1970, ‘Radiation and the Termites at El Verde (Ch. E8)’, in: Odum, H. T. andPigeon, R. F. (eds.),A Tropical Rainforest. A Study of Irradiation and Ecology at El Verde,Peurto Rico, Division of technical information. U.S. Atomic Energy Commission, Tennessee.

Mellinger, P. J. and Schultz, V.: 1975, ‘Ionizing radiation and wild birds: A review’CRC Criticalreviews in environmental control, 397.

Miera, F. R. and Hakonson, T. E.: 1978, ‘Radiation doses to rodents inhabiting a radioactive wastereceiving area’,Health Physics34, 603.

Miera, F. R., Hanson, W. C., Gladney, E. S. and Jose, P.: 1980, ‘Mobility of Elevated Levels ofUranium in the Environment’, in: Gesell, T. F. and Lowder, W. M. (eds.),Natural RadiationEnvironment III, TF Gesell and WM Lowder, US Dept of Energy, p. 681.

Musselman, R. C., Douglas, G. F., Shaw, C. G. and Moir, W. H.: 1992, ‘Monitoring AtmosphericEffects on Biological Diversity (Ch. 4)’, in: Barker, J. R. and Tingey, D. T. (eds.),Air PollutionEffects on Biodiversity, Van Nostrand Reinhold, New York.

Napier, G. M.: 1992,Application of laboratory derived data to natural aquatic ecosystems, PhDThesis, Macquarie.

Newman, J. R. and Schreiber, R. K.: 1988, ‘Air pollution and wildlife toxicology: An overlookedproblem’,Environ. Toxicol. and Chem.7, 381.

Newman, J. R., Schreiber, R. K. and Novakova, E.: 1992, ‘Air Pollution Effects on Terrestrial andAquatic Animals (Ch. 10), in: Barker, J. R. and Tingey, D. T. (eds.),Air Pollution Effects onBiodiversity, Van Nostrand Reinhold, New York.

Noss, R. F.: 1990, ‘Indicators for monitoring biodiversity: A hierarchical approach’,Conserv. Biol.4, 355.

Olympic Dam Operations: 1994, ‘Environmental Radiation Programme’, Annual Report June 1993– May 1994. Olympic Dam, South Australia.

Osburn, W. S.: 1966, ‘Ecological Concentration of Nuclear Fallout in a Colorado Mountain Wa-tershed’, in: Aberg, B. and Hungate, F. P. (eds.),Radioecological Concentration Processes,Permagon Press, Oxford, pp. 675–709.

Read, J. L.: 1992, ‘Influence of habitats, climate, grazing and mining on the small terrestrialvertebrates at Olympic Dam, South Australia’,Rangel. J. 14, 143.


Read, J. L.: 1994, ‘A retrospective view of the quality of the fauna component of the Olympic DamProject Environmental Impact Statement’,J. Env. Manage. 41, 167.

Read, J. L.: 1995a, ‘Recruitment characteristics of the White Cypress Pine (Callitris glaucophylla)in arid South Australia’,Rangel. J. 17, 228.

Read, J. L.: 1995b, ‘Subhabitat variability: A key to the high reptile diversity in chenopodshrublands’,Aust. J. Ecol. 20, 494.

Read, J. L.: 1996, ‘Use of ants to monitor environmental impacts of salt spray from a mine in aridAustralia’,Biodiv and Conserv. 5, 1533.

Read, J. L. and Tyler, M. J.: 1994, ‘Natural levels of abnormalities in the Trilling Frog (Neobatrachuscentralis) at the Olympic Dam Mine’,Bull. Environ. Contam. Toxicol. 53, 25.

Roberts, L.: 1982, ‘California’s fog is far more polluted than acid rain’,Biosci. 32, 778.Schnell, J. H.: 1964, ‘Some effects of neutron-gamma radiation on late summer bird populations’,

Auk. 81, 528.Schwarzkopf, L.: 1991,Costs of reproduction in the Viviparous Skink (Eulamprus tympanum),

unpubl. PhD Thesis, University of Sydney.Simon, S. L. and Ibrahim, S. A.: 1990, ‘Biological Uptake of Radium by Terrestrial Plants’, in:

The Environmental Behavior of Radium, Vol. 1, Published by IAEA in Technical Reports SeriesNo. 310, Vienna, pp. 545.

Talvitie, N. A.: 1972, ‘Electrodeposition of Actinides for Alpha Spectrometric Determination’,Analytical Chemistry44, 280.

Thomas, P.A., Sheard, J.W. and Swanson, S.: 1994, ‘Transfer of210Po and210Pb through the Lichen-Caribou-Wolf food chain of northern Canada’,Health Phys. 66, 666.

Turner, F. B.: 1975, ‘Effects of continuous irradiation on animal populations’,Advances in RadiationBiology5, 83.

Turner, F. B. and Gist, C. S.: 1970, ‘Observations of Lizards and Tree Frogs in an Irradiated PeurtoRican Forest (Ch. E-2)’, in: Odum, H. T. and Pigeon, R. F. (eds.),A Tropical Rainforest. A Studyof Irradiation and Ecology at El Verde, Peurto Rico, Division of Technical Information. U.S.Atomic Energy Commission, Tennessee.

Turner, F. B., Licht, P., Thrasher, J. D., Medica, P. A. and Lannom, J. R.: 1971, ‘Radiation inducedsterility in natural populations of lizards (Crotaphytus wislizeniiandCnemidophorus tigris)’, in:Nelson, D. J. (ed.),Proc. 3rd Natl Symp. on Radioecology, Oak Ridge, TN, U.S.A.

UNSCEAR: 1988,Sources, effects and risks of ionising radiation, United Nations ScientificCommittee on the Effects of Atomic Radiation.

Vasconcellos, L. M. H., Amaral, E. C. S., Vianna, M. E. and Penna Franca, E.: 1987, ‘Uptake ofRa226 and210Pb by food crops cultivated in a region of high natural radioactivity in Brazil’,J.Environ. Radioact.5, 287.

Whitehead, N. E. and Brooks, R. R.: 1971, ‘Gamma Radiation of some plants and soils from auraniferous area in New Zealand’,N. Z. J. Sci. 14, 66.

Woodhead, D. S.: 1977, ‘The effects of chronic irradiation on the breeding performance of the guppy,Poecilia reticulata(Osteichthyes: Teleostei)’,Int. J. Radiat. Biol. 32, 1.

Woodhead, D. S., Barker, C. J. and Rackham, B. D.: 1983, ‘The Effects of Chronicγ -Irradiationon Experimental Fish Populations: A Preliminary Account’, in:Biological Effects of Low-LevelRadiation, International Atomic Energy Agency. Vienna, pp. 646–648.

Woodwell, G. M.: 1962, ‘Effects of ionizing radiation on terrestrial ecosystems’,Science138, 572.Woodwell, G. M.: 1963, ‘The ecological effects of radiation’,Sci. Amer.208, 40.Yingping, X., Xianqian, L., Jingping, L. and Min, T.: 1994, ‘The effect of city air pollution on the

population ofEulecanium gigantea(Shinji) (Coccidae) in Taituan City, China, 7th Int. Symp.Scale Insect Studies, Bet Dagan, Israel.

Zach, R. and Mayoh, K. R.: 1985, ‘Gamma-radiation-induced spatial avoidance in birds’,RadiationResearch104, 66.

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Ecological and Toxicological Effects of Exposure to an Acidic, Radioactive Tailings Storage