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Journal of Environmental Radioactivity 123 (2013) 82e89

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Journal of Environmental Radioactivity

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Po-210 and Pb-210 in water and fish from Taboshar uranium miningPit Lake, Tajikistan

L. Skipperud a,*, A.G. Jørgensen a, L.S. Heier a, B. Salbu a, B.O. Rosseland b

aNorwegian University of Life Sciences, Isotope Laboratory, Department of Plant and Environmental Sciences, P.O. Box 5003, NO-1432 Aas, NorwaybNorwegian University of Life Sciences, Department of Ecology and Natural Resource Management, P.O. Box 5003, NO-1432 Aas, Norway

a r t i c l e i n f o

Article history:Received 23 November 2011Received in revised form1 March 2012Accepted 18 March 2012Available online 17 April 2012

Keywords:Po-210Pb-210FishAccumulationBiomagnificationCentral Asia

* Corresponding author. Tel.: þ47 64965546; fax: þE-mail address: lindis.skipperud@umb.no (L. Skipp

0265-931X/$ e see front matter � 2012 Elsevier Ltd.doi:10.1016/j.jenvrad.2012.03.013

a b s t r a c t

Polonium-210 in water and 210Pb and 210Po in different fish organs from 3 different fish species inTaboshar Pit Lake (n ¼ 13), located in the uranium mining area in Tajikistan, and in Kairakkum Reservoir(reference lake, n ¼ 3), have been determined as part of a Joint project between Norway, Kazakhstan,Kyrgyzstan and Tajikistan.

The average activity concentration of 210Pb and 210Po in liver, muscle and bone of Carassius auratus washigher than the concentration in similar tissues of C. carpio and Sander lucioperca from the reference site.The accumulation of 210Powas higher than for 210Pb, and the accumulation of 210Powas highest in the liverof C. auratus (3673 � 434 Bq kg�1 ww). Although the average activity concentration of 210Pb in liver andbones of C. auratus from Pit Lakewere fairly similar, a huge variation in the liver activity concentrations (25e327Bqkg�1ww)was found. The results confirmdirect uptake of unsupported 210Po into the liver, and thatthe distributions of 210Po and 210Pb in fish organs were different. The BCF (L/kg) for 210Po in bone, liver andmuscle clearly demonstrates high accumulation of 210Po in C. auratus, especially in the liver. The averageBCFs of liver, bone and muscle were >1.4 � 105, >2.5 � 104 and >1.4 � 104, respectively. All fish in thePit Lake were found to be in the same trophic level, however, a linear correlation between log 210Po inliver and d15N could indicate biomagnification of 210Po in liver of C. auratus.

In regards to the recommended Annual Limit of Intake (ALI) for 210Po, the concentration of 210Po inmuscle tissues of C. auratus is alarming, as there is a high probability for the local population at risk toexceed the recommended ALI through consumption of fish from Taboshar Pit Lake.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

The uraniummining industry in the USSR was established in thelate 1940seearly 1950s in the former Soviet Republics ofKazakhstan, Kyrgyzstan, Tajikistan and Uzbekistan as part of thenuclear weapon program. Furthermore, uranium-rich materialswere transported from several former East-European socialistcountries (e.g. East-Germany, Ukraine) to the Central Asian regionfor processing (Abraham et al., 2007).

In most countries, uranium mining is considered the mosthazardous step of nuclear materials production, both in terms ofradiation doses and in the number of people affected. Key problemshave been associated with the transport of uranium and itsdaughters in aquatic and terrestrial ecosystems, where radionu-clides are transferred from air, water, and soils into plants, fish/

47 64966007.erud).

All rights reserved.

animals and finally to man. Special attention is paid to the mosthazardous decay products of uranium; 210Pb and 210Po and 226Ra.

As identified during 2003e2004, a series of claims were putforward with respect to radioactive contamination, and to injuriesto man and the environment from radioactivity. However, thefactual base was poor in all countries involved. To meet the needsfor factual information from some key contaminated sites, theNATO RESCA project and the Joint NorwegianeKazakhstan,Kyrgyzstan and Tajikistan projects were initiated (Salbu et al.,2012).

The objective of the present work is to provide first handinformation on the concentration of the naturally occurringradioactive isotopes 210Pb and 210Po, based on speciation analysis ofwater and by analysis of different fish organs from an area of formeruranium mining activity in Tajikistan (Skipperud et al., 2012).

2. Materials and methods

Fieldwork was performed in the Republic of Tajikistan in August2008. The fieldwork focused on the site Taboshar, a mining and

Fig. 1. The Pit Lake in Taboshar, Tajikistan (Photo: L. Skipperud).

L. Skipperud et al. / Journal of Environmental Radioactivity 123 (2013) 82e89 83

tailing area, and in particular on samples of water and fish from thePit Lake, an artificial lake situated in the Taboshar mining area(Skipperud et al., 2012). The large freshwater reservoir Kairakkum,was used as reference (Table 1).

The main study site is an artificial lake within the Tabosharuranium mining site at the southern edge of the Kuramin Moun-tains close to the UzbekeTajik border (Stegnar et al., 2012). Thecompany Vostokredmet combine at Taboshar was established onthe basis of the former Leninabad Mining and Chemical Combine in1948. During the period of operation about 35 million m3 ofradioactive waste was generated. The waste was stored in 9 tailingsdumps (a total area of 1,741,000 m2) and in 21 dumps from oreswithin the mining and processing enterprises (Burykin, 2000). InTaboshar, U-rich ores was extracted and a pit lake was created inthe area (Fig. 1). The Taboshar Pit Lake is about 600 m long and200 mwide, and about 150 m deep. The 15 m upper part of the PitLake is oxic, while the deeper layers are anoxic, expected to bemoreor less the same throughout the year due to minor disturbance ofwater. A small creek is the only outlet from the lake, maintainingthe water level to about constant. Wild and domestic animals areusing the water for drinking, and the lake was stocked withCommon goldfish (Carassius auratus) which are exploited by thelocals.

Fish and water were sampled from study site and reference site(Kairakkum Lake) respectively. Additionally, water snails, watermoss, and rush were sampled from the area around the study site.All samples were stored cooled during the day of sampling and thenfrozen until returning to the Isotope Laboratory, NorwegianUniversity of Life Sciences (UMB) for analysis.

2.1. Water sampling

Sampling of water was performed by in situ fractionation,separating radionuclides in terms of size (molecular mass) andcharge (Salbu, 2007). Size fractionation was done by using a Milli-pore membrane filter (mixed cellulose esters) with cut-off at0.45 mm and a Micon Hollow fibre ultrafilter having a cut-off at10 kDa. Filter with a pore diameter of 0.45 mmandmembranes witha cut-off at 1e10 kDa ensured retention of particles (>0.45 mm) andcolloids (10 kDa < x < 0.45 mm), respectively. Charge fractionationwas done by ion exchange chromatography of the ultrafilteredsample. The cationic exchange resinwas Bio-Rad Chelex�100 resin(100e200 mesh). After fractionation, all water samples wereacidified to 1% with ultrapure hydrochloric acid (HCl) and storeduntil laboratory analysis were performed. TOC was determined byusing a Shimadzu TOC cpn Total organic analyzer and major anionswere determined by using Iachat IC5000 Ion Chromatograph.

2.2. Fish, snails, rush and moss sampling

Totally 13 fish (N ¼ 13) of Common goldfish from the TabosharPit Lake and Carassius carpio (N ¼ 2) and Sander lucioperca (N ¼ 1)from a reference site (Kairakkum Reservoir) were sampled. Fish inPit Lake were mainly obtained by local anglers using fishing lineand rod. The fish from the Kairakkum Reservoir were bought at

Table 1An overview of sampling locations in Tajikistan concerning their geographicalparameters.

Sample location Geographical coordinates Elevation(m.a.s.l)

Details

Pit Lake, Taboshar 40�58.798N, 069�66.769E 1260 Study siteKairakkum Reservoir 40�28.357N, 069�83.797E 1293 Reference site

*m.a.s.l. ¼ meter above sea level.

a local fish marked. Fish were killed by a blow to the head prior tomeasurement of length and weight. The dissection procedure fol-lowed the EMERGE protocol (Rosseland et al., 2001). Dissectedtissues were separately packed in aluminium foil and zipper bagsand stored at�20 �C prior to returning to the Norwegian Universityof Life Science (UMB), and kept at that temperature until analysis.Otholiths were used to determine the age of all fish species.

Additionally, water snails, rush and moss from the lake wereanalysed for stable carbon and nitrogen isotopes to gain informa-tion on a baseline trophic level of the study site.

2.3. Analytical measurements

Water quality variables as well as trace element concentrationsin water were analysed as described by Salbu et al. (2012).

Sample preparation prior to analyses of 210Pb, 210Po and stable13C/12C (d13C) and 15N/14N (d15N) isotope ratios (for identification offood sources and trophic levels of fish) using IRMS were performedin the Isotope Laboratory, UMB. The method for analysis of stableisotopes of carbon and nitrogen was performed according toChhatra et al. (2008, 2009) and Desta et al. (2006). The analysis ofstable isotopes of nitrogen and carbon were performed by com-busting the homogenized and freeze-dried samples in a FlashElemental Analyzer (EA) and separating the combustion gases (CO2and N2) with a Poraplot Q column and transferring them to a Fin-nigan DeltaPlus XP continuous-flow isotope ratiomass spectrometer(CF-IRMS).

Determination of 210Po and 210Pb in water samples was per-formed by combining the method of Chen et al. (2001) andSuriyanarayanan et al. (2008), while the analysis of fish organs wasperformed in accordance with the method described by Chen et al.(2001). Fish from study site (n ¼ 13) and reference site (n ¼ 3) wasanalysed simultaneously (n ¼ 16). The fish samples subjected to210Po and 210Pb analysis were bone (mainly spine), liver (total) andmuscle (part). All organs were analysed separately and related tothe individual fish. In addition, reagent blanks (n¼ 2) and analyticalblanks (n ¼ 3) were subjected to analysis.

All tissues were analysed separately and related to the indi-vidual fish. For total decomposition of tissue samples, aciddecomposition by UltraCLAVE high performance reactor was used.All samples, reagent blanks, and analytical blanks were weigheddirectly into their respective Teflon vessels. Reagent blanks andanalytical blanks were made by adding 5 ml of HNO3 into 5 Teflon

Table 2Some of the physical and chemical variables in water from the study site and the reference site, August 2008.

Site pH Conductivity (mS/cm) Temperature (�C) Ca (mg L�1) Fe (mg L�1) Mn (mg L�1) TOC (mg C L�1)

Study site 8.09 1251 24.5 126 17 13 2.2Ref. site 8.31 1494 29.5 n.m 730 n.m 1.24

n.m ¼ not measured.

L. Skipperud et al. / Journal of Environmental Radioactivity 123 (2013) 82e8984

vessels. Ultrapure nitric acid (68% HNO3) was added to ensure 1:10solid solution ratio during decomposition. Finally, 208Po tracersolution (0.1 ml) was added to all samples and the reagent blanksprior to decomposition.

Decomposed and dried samples were dissolved and radio-chemical separation of 210 Po done according to themethod of Chenet al. (2001).

The method for thermal plating of 210Po was performed inaccordance to the method of Chen et al. (2001) on nickel discs. The210Po in all samples was determined by alpha spectrometry. Theconcentration of 210Pb was analysed after 6-month of ingrowths of210Po where 210Po and 210Pb were considered at equilibrium. Thealpha spectrometry system used for this work consisted of 6 Can-berra models 7401 a-spectrometers linked to a Canberra ADCmodel 1520. The spectra were acquired using Canberra’s Genie PC2000 software. Samples were counted for 72 h or until the countingerror was below 10%. All 210Po and 210Pb activities from alphaspectrometry were decay corrected to the date of sampling (August27th 2008) by the Genie 2000 Software. Simultaneously, the Genie2000 Software corrected the yield to 100% using the added activityconcentration of the yield monitor 208Po. No significant countsabove instrumental background were detected in the blanks whencounting on alpha spectrometer, thus there was no indication of210Po and 210Pb contamination throughout the chemicalprocedures.

Statistical analysis was performed using Minitab 15. TheAnderson-Darling test was used to check the normality of the data,and data not normally distributed (activity concentration in organsand bioconcentration factors) were transformed using the soft-ware’s Johnson transformation. Equal variances were tested usingBartlett’s test. Differences between groups were tested usingANOVA (general linear model). Simple correlation analysis wasperformed using Pearson correlations coefficients and regressionwhere p < 0.05 was set as a criterion for significance.

3. Results and discussion

3.1. Water samples results

Some of the important physical and chemical variables in watercollected at the study site and reference site are given in Table 2.

Table 3The measured concentration of 210Po (mBq/L) in water samples from the Pit Lake,before and after size- (molecular mass) and charge fractionation and calculatedconcentrations in actual fractions.

Water sample Po-210 activityconcentration inwater samples(mBq/L)

Calculated concentrationin fractions (mBq/L)

Total 5.6 � 0.7 Particle 0.60.45 mm 5.0 � 0.5 Colloidal 3.410 kDa 1.6 � 0.4 LMM 1.6kDa and ion

exchange1.0 � 0.2 Cations 1.0

The Pit Lake and Kairakkum Reservoir are both alkalinefreshwater lakes, with a pH >8. The conductivity in both lakesare relatively high (>660 mS/cm) (Skjelkvåle et al., 2007), andcorrespond to 1 ppm seawater. The concentration of total organiccarbon (TOC) in the water of the study site was 2.2 mg C L�1

which is in the same range as oligotrophic lakes (Skjelkvåle et al.,2007).

The total activity concentration of 210Po in the Pit Lake was5.6 � 0.7 mBq/L (Table 3). According to World Health Organization(WHO, 2011), the guidance level (GL) of 210Po in drinking water isset at 0.1 Bq/L. In this respect, the activity of Po found in the studysite is well below the limit for drinking water.

The percentage distribution of 210Po, Mn and TOC species arepresented in Fig. 2. The main activity concentration of 210Po isrelated to species having nominal molecular mass >10 kDa witha distribution of particles and colloids being 11% and 60%, respec-tively. The low molecular mass fraction (LMM) of 210Po was 28%,with cations being the major LMM species (62%).

The relative distribution of Fe species >10 kDa was 76%. Frac-tionation of TOC in water revealed that 62% TOC were present asLMM species, while particles and colloids corresponded to 13% and23%, respectively. Generally, the literature states that polonium isa particle reactive element under alkaline conditions and that itbinds to most other compounds such as humic acids and variouselements (Kim et al., 2005; Matthews et al., 2006; Ohtsuka et al.,2000). Polonium is especially known to aggregate with Fe andMn and form colloids and it is to a great extend the solubility of thecompounds formed by complexation of polonium that is control-ling the mobility of this radionuclide (Kim et al., 2005; Matthewset al., 2006; Ohtsuka et al., 2000). Vaaramaa et al. (2003) deter-mined the soluble and particle-bound forms of naturally occurringradionuclides (234U, 238U, 226Ra and 210Po) in water from groundwater wells, using filters in the range 0.45 mme5 kDa. They foundthat the behaviour of 210Po varied with water composition, but that210Po was present in both soluble and particle-bound forms in allground waters. Further, they found that particle-bound 210Pocorrelated with the concentration of Fe, manganese and humicsubstances.

The speciation of 210Po observed in the study site, seen in rela-tion to the alkaline conditions and the presence of ligands, favoursthe assumption that 210Po was subjected to growth mechanisms inPit Lake, turning ionic species into colloid size. Based on generalknowledge in biogeochemistry of 210Po and the results from otherstudies, it is reasonable to assume that the explanation for theobserved speciation of 210Po was partly due to its association withTOC and Mn. However, the correlations between 210Po and TOC or210Po and Mn were not statistically significant. The distribution ofFe species was relatively similar to the speciation of 210Po. Both210Po and Fe were mainly present as species >10 kDa and theyshowed minor differences in the concentration of LMM species,which might indicate that 210Po was associated with Fe. However,due to problems differentiating between the particulate andcolloidal fraction of Fe we cannot conclude whether there isa relationship between 210Po and Fe in the particulate and HMMfraction. Consequently, further studies must be performed in thestudy site in order to decide which factors are contributing to thespeciation of 210Po in Pit Lake.

0

20

40

60

80

100

%

< 10 kDa anionic and neutral species< 10 kDa cationic species

0

20

40

60

80

x > 0.45 μm 0.45 μm > x >10 kDa x <10 kDa

%

Po-210

TOC

Mn

Fig. 2. The percentage distribution of 210Po, TOC, and Mn on different cut-off according to size in the Pit Lake; particulate (x > 0.45), colloidal HMM (10 kDa < x < 0.45) and LMM(<10 kDa) to the left (n ¼ 1). The distribution of LMM species of 210Po between cation and anionic/neutral species is given to the right.

L. Skipperud et al. / Journal of Environmental Radioactivity 123 (2013) 82e89 85

3.2. Radionuclides in fish

The data of C. auratus from the study site (n ¼ 13) and C. carpio(n ¼ 2) and S. lucioperca (n ¼ 1) from reference site are given inTable 4. Since the fish from the study site were mainly obtained bylocal anglers using fishing line and rods the results are not repre-sentative for a population with age/class structure. However, withage classes from 2 to 8 years, the data can be used to describe thegrowth pattern of the population and level of contaminants ofC. auratus from the study site (Rosseland et al., 2007).

The flesh colour of all individuals of C. auratus, C. carpio andS. lucioperca was white which is typical for these species (Kanguret al., 2007). The maturity stage of individuals of C. auratus wasIeII, representing an immature group of the population. The pop-ulation seemed to have a linear growth, with increasing lengthwithincreasing body size and no stagnation of growth occurred withinthis size range of C. auratus (Fig. 3). The age of the population, ofwhich >90% were females, represented age classes from 2 to 8years with an average age of 5.6 years. The population seemed tohave a linear growth up to age 8 (Fig. 4). The continuous growth offish depends on a series of factors, where of course the access andabundance of food are very important. This links directly to thepopulation size, as the growth in a low populated lake is muchbetter than if the lake is overpopulated or stunted population.However, the growth will not stop completely, but will come downto length increment which will not cause any growth zones. It istherefore important to always use otholiths for ageing, as they willcontinue to grow through the whole life of a fish. If the growth isstopped due to overpopulation, the weight will not increase either,it will be reduced, and wewill have a change in the condition factoras age increases. It is therefore a need to always use age, length andweight as three “dimensions” to the concentrations of pollutants infish organs. Age, being the most important as this gives the expo-sure timeframe. The life span of the common goldfish is not easy topredict for a certain location, as few data from populations in thewild exist (Tarkan et al., 2010). However, we know from goldfish incaptivity that they can become mature after 1e3 years, most

Table 4Population data of all fish species from Pit Lake (study site) and Kairakkum Reservoir (re

Species (n) Length (avg. cm) Range (cm) Weight (avg. g ww)

C. auratus (13) 15 10.4e18.5 49.5S. lucioperca (1) 46.5 e 800C. carpio (2) 35 33e37 730

a Age not determined due to poor quality of otholites and scales.b Not registered.

probably due to a rapid growth which typically leads to an earlymaturation inmost fish species. The life span of goldfish in captivitycan be more than 10 years. The specimens from the Pit Lake inTaboshar, however, were all immature, having ages between 2 and8 years, and with maximum sizes of 18.5 cm and 85 g.

Addressing the trophic level and the energy source of organismsby using stable isotopes is an important tool in ecology as itprovides important knowledge on ecosystem functioning. Addi-tionally, such knowledge can be used in ecotoxicology to explainintraspecific and interspecific variation in the concentration ofcontaminants in organisms (Cabana and Rasmussen, 1996; Cheungand Wang, 2008; Rognerud et al., 1996; Zhou and Wong, 2000).Fig. 5 shows the relationship between stable carbon isotopes (d13C)and nitrogen isotopes ratios (d15N) in individual fish, snail, rush andmoss from the Pit Lake.

The fractionation of d15N has previously been determined to3.4& per trophic level in temperate regions (Post, 2002; VanderZanden and Rasmussen, 2001). All the C. auratus collected in PitLake were found to be within the same trophic level (within 2&),Fig. 5. As the C. auratus was two tropic levels above the primaryproducers and snails, the main food was probably zooplankton (notanalysed). In the reference site, the d15N showed that S. luciopercarepresented a higher trophic position (d15N¼ 15.3) when comparedto C. carpio (d15N ¼ 10.9).

The d13C reflects from where the organism gain their carbon,where a more negative value represent sources of deeper in-lakeareas while less negative values reflect more littoral sources(Rosseland et al., 2007). In Fig. 5, the d13C in the individual fishshowed that there might be subgroups which were more frequentfeeding in different areas of the lake, but as a population “sharing”the whole lake area. A natural situation being the youngest year-classes seeking concealment in the rush closer to the littoral,which also seems to be the case in the Taboshar Pit Lake.

The activity concentrations of 210Pb and 210Po in liver, bone andmuscle from all species from the study site and reference site arepresented in Table 5. The average activity concentration of 210Pb inliver and bones of C. auratuswere similar (94 and 100 Bq kg�1 ww),

ference site), Taboshar, Tajikistan. Avg. ¼ average, ww ¼ wet weight, yr ¼ year.

Range (g ww) Age (avg. yr) Flesh (colour) Maturity (stage)

19e85 5.6 White IeIIe a White I700e760 a White b

y = 0.1122x + 9.5373

R2 = 0.8989

0

5

10

15

20

25

0 10 20 30 40 50 60 70 80 90

Weight (g)

Len

ght (

cm)

Fig. 3. The relationship between length (cm) and weight (g) of individuals of C. auratusfrom Pit Lake, Taboshar, Tajikistan.

L. Skipperud et al. / Journal of Environmental Radioactivity 123 (2013) 82e8986

but there was a huge variation in the liver activity concentrationsranging from 25 to 327 Bq kg�1 ww. The average activity concen-tration of 210Pb and 210Po in liver, muscle and bone of C. auratuswashigher than the activity concentration in similar tissues of C. Carpioand S. lucioperca from the reference site. The highest activityconcentration of 210Po was in liver (3700 � 430 Bq kg�1ww) ofC. auratus. In the reference site, the highest average activityconcentration of 210Po was found in liver of C. Carpio (180 Bq kg�1

ww). There were not possible to perform a test fish or do a moreextensive survey in the reference lake. The three controls thus serveonly as indicators of what was to expect of pollutant levels outsidethe mining and tailing areas, and we believe them to be better thannothing.

The activity concentration of 210Po in liver of C. auratus from thestudy site was generally much higher than the activity concentra-tions found of 210Po in bone and muscle. However, the lowestobservation of the activity concentration of 210Po in liver was lowerthan the lowest observation in bone andmuscle. This observation isconsidered an outlier as no other individual of C. auratus showedvalues <592 Bq kg�1 ww. Additionally, the majority of individualshad an activity concentration >3000 Bq kg�1 ww. The activityconcentration in liver, muscle and bone in C. auratus were allsignificant different from each other. There is a distinct difference inthe activity concentration of 210Po observed in the liver of C. carpiocompared to S. lucioperca from the reference site. In the referencesite, S. lucioperca showed relatively low activity concentrationcompared to C. carpio also in muscle. However, it is slightly higher

y = 7.1891x + 9.0918

R2 = 0.7347

0

10

20

30

40

50

60

70

80

90

0 2 4 6 8 10

Age (Yr)

Wei

ght (

g)

Fig. 4. The relationship between body weight (g) and age (

in bone. Based on liver andmuscle it seems as C. carpio had a higheractivity concentration of 210Po than S. lucioperca, despite havinga lower d15N signal. As we have no age data on these species, theexplanation may be that the two specimen of C. carpio were olderand thus had a higher bioaccumulation of 210Po than the singlespecimen of S. lucioperca.

The results confirm the highest uptake of unsupported 210Pointo the liver (Bellamy and Hunter, 1997), and that the distributionof 210Po and 210Pb in fish organs were different. A much higherfraction of 210Po was found in the liver, while 210Pb tends to bea “bone seeker”.

The activity concentration of 210Po found in muscle and liver ofC. auratus from study site and C. carpio and S. lucioperca fromreference site was compared to the activity concentration found inS. lucioperca from uranium mining and tailing sites in Kyrgyzstanand Kazakhstan. The average activity concentration of 210Po inmuscle tissue of C. auratus from Pit Lake in Taboshar, Tajikistan wasa factor of w250 and w500 higher compared to 210Po in muscle ofS. lucioperca from Kyrgyzstan and Kazakhstan, respectively. Further,the activity concentration of 210Po in C. auratus from Tajikistan wasa factor of w400 higher when compared to the activity concen-tration in liver of S. lucioperca from Kazakhstan.

3.3. Bioconcentration factors of 210Po

The bioconcentration factor (BCF ¼ Conc. in organ/conc. inwater) was calculated according to:

BCF ¼ Cons: organismðBq=kgðwwÞÞCons:waterðBq=LÞ

The BCF (L/kg) for 210Po in bone, liver and muscle clearlydemonstrate high accumulation of 210Po in C. auratus, especially inthe liver. The average BCFs of liver, bone and muscle were>1.4 � 105, >2.5 � 104 and >1.4 � 104, respectively. The bio-concentration factors are in agreement with other studies, showingbioconcentration factors in liver tissue ranging from 103 to 105

(Bellamy and Hunter, 1997). Considering the standard BCF valuespresented by IAEA (2009); (High potential BCF >1000; ModeratePotential 1000 > BCF > 250; Low potential 250 >BCF), the BCFvalues indicated high potential BCF of 210Po in all organs ofC. auratus. The bioconcentration factor (BCF) of 210Po in liver ofC. auratus was much higher and significantly different from theactivity in muscle (p < 0.001) and bone (p < 0.001). There are noavailable BCF for 210Pb from the fish species from the KairrakkumReservoir as no data was obtained on the concentration in waters.

y = 0.8283x + 10.434

R2 = 0.6969

0

5

10

15

20

25

0 2 4 6 8 10

Age (Yr)

Len

ght (

cm)

yr) of individuals of C. auratus from Pit Lake, Taboshar.

0

5

10

15

40 35 30 25 20 15

δ15 N

δ13C

C. auratusMossSnailRush

Fig. 5. The level of d13C (carbon source) and d15N (trophic level) in C. auratus, plantsand snail from the Pit Lake, Taboshar, Tajikistan.

L. Skipperud et al. / Journal of Environmental Radioactivity 123 (2013) 82e89 87

An important aspect is that by calculating the BCF based on thetotal concentration of a contaminant in water, an uncertaintyprevails in terms of which element species is the greatestcontributor to the concentration of a contaminant in organs oforganisms (Salbu, 2007; Salbu et al., 2004; Salbu and Skipperud,2007). The LMM fraction is known to be the most biologicallyreactive species (Rosseland et al., 2007; Salbu, 2000). By calculatingthe BCF from the LMM fraction of 210Po in the study site, it isapparent that the overall BCF of liver, bone and muscle increaseswith a factor of 17, 17 and 15, respectively.

200

150

3.4. Bioaccumulation of 210Po and 210Po

The results show accumulation 210Pb and 210Po, especially inliver and bones of C. auratus, and a higher uptake and accumulationof 210Po than of 210Pb. The concentrations of contaminants inorganisms often show interspecific and intraspecific variation. Suchvariation may be explained by several factors including the route ofuptake, age, size, feeding habits and trophic level (Rognerud et al.,2001; Walker et al., 2001). Additionally, various contaminants aredistributed differently throughout the tissues of organisms due todifferent mechanisms such as the biochemical characters of theelement and specific physiology of tissues (Walker et al., 2001). Thedistribution of 210Po observed in fish species in this study was in-line with observations in organisms and fish from other studiesperformed both in freshwater and marine waters. According toDurand et al. (1999) it is known that 210Po is accumulated and thatthe liver of fish may contain especially high concentrations.Shaheed et al. (1996) showed a general higher accumulative abilityof aquatic organisms (including fish) towards 210Po compared touptake of 210Pb and other radioactive nuclides. Durand et al. (2002)

Table 5The average (avg.) and median (med) concentration of 210Pb and 210Po (Bq kg�1)(ww) in liver (l), bone (b) and muscle (m) of C. auratus (n ¼ 13) from Pit Lake (studysite), and C. carpio (n ¼ 2) and S. lucioperca (n ¼ 1) from Kairakkum Reservoir(reference site), Tajikistan.

Species (tissue) Po-210 (Bq kg�1) Pb-210 (Bq kg�1)

Mean SD Median Range Mean SD Range

C. auratus (l) 3950 880 3400 593e9380 94 102 25e327C. auratus (b) 700 90 650 265e1390 100 54 22e185C. auratus (m) 410 92 290 128e1280 n.m e e

C. carpio (l) 183 e e 80e284 4.4 3.2 2.7e6.1C. carpio (b) 14 e e 4e23 0.85 0.06 0.81e0.89C. carpio (m) 7 e e 3e11 n.m e e

S. lucioperca (l) 11 e e e n.m e

S. lucioperca (b) 8 e e e n.m e

S. lucioperca (m) 2 e e e n.m e

l ¼ liver, b ¼ bone, m ¼ muscle, n.m ¼ not measured.

further strengthened the observation of 210Po and its strong affinityto bind to Fe containing proteins. They found that ferritin andhemocyanin were molecular traps in the liver tissues of fish.

3.5. Biomagnification properties of 210Po and 210Pb

The linear correlations between 210Pb and 210Po concentrationsin fish organs and the d15N indicate a trend of increasing activityconcentration as a function of the d15N level (Figs. 6 and 7).However, in order to establish whether there is a case of bio-magnification, the linear relationship between log 210Pb and log210Po activities and d15N has to be calculated. For mercury (Hg),which has biomagnification properties, a worldwide log THg tod15N relation lies between 0.11 and 0.35 (Sharma et al., 2008).Applying this to 210Po and 210Pb, a significant relationship (p< 0.05)between the activity concentration of 210Po in liver with d15N(linear regression: p ¼ 0.039) was found, giving the followingregression equation:

Log 210Po�Bq kg�1

�¼ �0:435þ 0:302 d15N (1)

This is an indication of a biomagnification rate of 0.30, but as allthe fish collected were found to be representative for the sametrophic level, more investigations are needed to confirm thepotential biomagnifications properties of 210Po in fish liver ofdifferent trophic levels. No potential biomagnifications were foundfor 210Po in muscle or bones. No significance could be attributed tobiomagnification of 210Pb into fish bones (p ¼ 0.403) or in fishmuscle and liver.

3.6. Risk assessment

Based on the obtained results, it is unlikely that annual effectiveradiation doses from gamma, water etc. to humans in Tabosharwould exceed the recommended annual threshold dose level of10 mSv, unless fish from the Pit Lake were used as dietary intake.The US Nuclear Regulatory Commission has set the Annual Limit ofIntake (ALI) of 210Po through ingestion to 5 kBq/year, or approxi-mately 15 Bq/day (NRC, 2011). The 210Po levels in fish muscles ofC. auratus in the Taboshar Pit Lake were very high. An average fishconsumption of 1.5 kg per month (50 g per day) with 210Poconcentration of 400 Bq/kg would exceed ALI and contribute about8 mSv to the annual effective dose.

13,513,012,512,011,5

10090807060

50

40

30

20

Log

Pb-2

10 (B

q/kg

)

Log210Pb (Bq kg-1) = -0.302 + 0.181 δ15N, p = 0.403

δ15N

Fig. 6. Scatterplot of the relationship between d15N and the log210Pb activityconcentration in bone of C. auratus from Pit Lake, Taboshar, Tajikistan.

13,513,012,512,011,5

10000

1000

100

Log

Po-2

10 (B

q/kg

)

Log210Po (Bq kg-1) = -0.435 + 0.302 δ15N, p = 0.039

δ15N

Fig. 7. Scatterplot of the relationship between d15N and log210Po activity concentrationin liver of C. auratus from Pit Lake, Taboshar, Tajikistan.

L. Skipperud et al. / Journal of Environmental Radioactivity 123 (2013) 82e8988

Groups at risk, such as pregnant women and children should notconsume fish from the Pit Lake in Taboshar and a high intake of fishfrom this lake is not recommended for the general population assuch. Water concentrations of 210Po and 210Pb were not taken intoconsideration for dose assessments due to very low concentrationsof both radionuclides in the water samples, and assumingly, theiradded dose contributions through drinking of water would be ofminor importance.

4. Conclusions

Within the Taboshar mining area, an open pit from whichuranium was extracted is filled with water due to ground waterinflow and precipitation, containing fish through stocking. The totalactivity concentration of 210Po in the Pit Lake is 5.6� 0.7mBq/L, andis well below the limit for drinking water.

The activity concentrations of 210Pb and 210Po in tissues ofC. auratus from Pit Lake (study site), Taboshar, were generallyhigher than in similar tissues of C. carpio and S. lucioperca from theKairakkum Reservoir (reference site). The activity concentration of210Po in liver of C. carpio from Kairakkum Reservoir was higher thanin S. lucioperca, although the d15N showed that S. lucioperca rep-resented a higher trophic position. This is attributed to the higher210Po load in the Pit Lake, but could also be a result of age differ-ences (which could not be determined). Generally, the highestaverage activity concentration of 210Po was observed in liver, andthe lowest in muscle for all species from both sites. The BCF valuesobserved in the tissues of C. auratus were significant higher in livercompared to bone and muscle tissues indicating that 210Po wasstrongly accumulated in the liver of C. auratus. The 210Pb showedsimilar concentration in liver and in bones, but with large variationin liver.

Correlation between log 210Pb and log 210Po concentrations infish organs relative to d15N showed statistically significant bio-magnification of 210Po in liver, but no significant biomagnificationfor 210Pb in bones.

In regards to the recommended ALI for 210Po, the concentrationof 210Po in muscle tissues of C. auratus is alarming, as there is a highprobability for the local population to exceed the recommended ALIthrough consumption of even small quantities of fish from Pit Lake.

Acknowledgements

The authors greatly acknowledge the funding and support of theUD project: Joint project between Norway, Kazakhstan, Kyrgyzstan

and Tajikistan: Environmental impact assessment of radionuclidecontamination of selected sites in Central Asia, no. 307046. Wethank Reidar Borgstrøm (UMB) for age determination of the fishand Gjermund Strømman for helping with d15N measurements.

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