Cadmium, lead, copper and zinc in blue mussels (Mytilus edulis)

sampled in the Hardangerfjord, Norway

Kare Julshamn,*a Eili Kristin Torpe,a,b Cathrine Børnes,a Leif J. Sæthreb and Amund Maagec

aInstitute of Nutrition, Directorate of Fisheries, P.O. Box 185, Sentrum, NO-5804 Bergen,Norway. E-mail: kare.julshamn@nutr.fiskeridir.no; Fax: z47 55 23 80 95; Tel: z47 55 2382 90

bDepartment of Chemistry, University of Bergen, NO-5007 Bergen, NorwaycAlex Stewart Environmental Services A/S, Tyssedalsveien 16, NO-5750 Odda, Norway

Received 4th April 2001, Accepted 29th May 2001First published as an Advance Article on the web 1st August 2001

Cadmium, lead, copper and zinc were determined in the soft tissues of blue mussels (Mytilus edulis) sampled

from four locations along the Hardangerfjord in western Norway. A source of pollution is located at the head

of the fjord and the sampling was performed at various distances from this source. The results obtained in this

study (1998) were compared with results from similar studies carried out in 1983 and 1992. The mean cadmium

concentrations in blue mussels sampled at Mage (13 km from the source of pollution) were approximately

18 mg kg21 fresh weight in 1983, 2.4 mg kg21 fresh weight in 1992 and 1.1 mg kg21 fresh weight in 1998. The

mean cadmium concentrations in blue mussels sampled at Varaldsøy (105 km from the source of pollution)

were approximately 5 mg kg21 fresh weight in 1983, 0.5 mg kg21 fresh weight in 1992 and 0.4 mg kg21 fresh

weight in 1998. The mean lead concentration in blue mussels sampled at Mage was 140 mg kg21 fresh weight in

1983. The mean lead concentrations in 1992 and 1998 had decreased to 6 and 3 mg kg21 fresh weight,

respectively. The mean lead concentrations in blue mussels from Gravdal were 15 mg kg21 fresh weight in

1982, 1 mg kg21 in 1992 and less than 1 mg kg21 fresh weight in 1998. The mean copper concentrations in blue

mussels were relatively constant over this period at all locations, with a variation between 0.6 and 1.2 mg kg21

fresh weight. The mean zinc concentration in blue mussels sampled at Mage decreased from 120 to 30 mg kg21

fresh weight in the period between 1983 and 1998.

Introduction

The Sørfjord is a north–south trending extension of theHardangerfjord, 1–2 km wide, 40 km long and 100–400 mdeep, lined with several factories, among them a zinc plant atOdda at the head of the fjord (Fig. 1). This plant is the onlyone in Scandinavia and industrial wastes have been dischargedfrom the inner part of the Sørfjord since 1915. The metalemissions to the fjord have varied through the years, both interms of the amounts of metals and the types of compounds. Asa consequence of environmental concern, a reduction of metalemissions to the fjord began in the middle of the 1970s, butthe discharges did not cease completely until 1986. Metalshave mainly been discharged as technical jarosite (compositeproduct of iron and alkali minerals), which was believed tobe almost insoluble in seawater. In the 1970s, the ranges ofdaily discharge loads were estimated to be 200–600 kg arsenic,2500–5000 kg zinc, 50–200 kg copper, 20–50 kg cadmium,100–200 kg lead and 1–3 kg mercury.1

The distributions of metals in various marine organismsfrom this fjord system have been intensively studied.2–5 All ofthese investigations revealed a water system heavily pollutedby metals.

Three surveys of heavy metals have been carried out in theperiod from 1983 to 1998. The first survey was carried outin late 1983 and early 1984 on behalf of the NorwegianDirectorate of Fisheries and the State Pollution ControlAuthority. In this study, fish (Gadus virens, Platichthys flesus)and blue mussels (Mytilus edulis) from 36 locations wereanalysed for As, Cu, Zn, Cd, Pb and Hg.5 The next survey wascarried out in 1992 on behalf of the Norwegian Directorate ofFisheries, and in this study only blue mussels were included.

Samples from 12 locations were analysed for As, Cu, Zn, Cdand Pb.6 The third survey was carried out in 1998, also onbehalf of the Norwegian Directorate of Fisheries, and againblue mussels were studied. The sampling locations chosen inthis study were more or less the same as those chosen in the

Fig. 1 Map of Hardangerfjord with sampling sites: 1, Mage; 2, Utne; 3,Nordheimsund; 4, Gravdal.

DOI: 10.1039/b103047g J. Environ. Monit., 2001, 3, 539–542 539

This journal is # The Royal Society of Chemistry 2001

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second survey. As in 1992, the study in 1998 focused on thecontent of cadmium, lead, copper and zinc in the soft part ofblue mussels in order to study the effects of the measures takenon the content of these heavy metals.

Methods

Field collection

Blue mussels were collected in the period from April to Junein 1992 and 1998 at four sites with a natural population. Themussels were collected about 0.5 m below mean low tide toavoid any effects of the deposition of airborne particles andsurface slicks. More than 75 specimens were sampled from eachsite. The length of the mussels varied between 3.0 and 4.0 cm,most specimens being about 4.0 cm.

Sample preparation and analysis

On arrival at the laboratory, the mussels were measured andthe soft part was removed from the shells. Approximately 25mussels were pooled. Pooling the specimens has the disadvan-tage of mixing the sexes. The advantage of pooling is to reducesome of the random variation from individual to individualand hence to obtain a close approximation to the populationmean of the variate in question.7 The pooled samples wereweighed to record a wet weight value, freeze dried and weighedagain to obtain a dry weight value before they were pulverized.Prior to elemental analyses, the samples were wet digested in aMilestone microwave laboratory system (Milestone, Sorisole,Italy) by the addition of 2 mL of nitric acid (65% m/v) and0.5 mL of hydrogen peroxide (30% m/v) (Ultrapure, Merck) tosamples of approximately 0.2 g dry matter. The concentrationsof copper and zinc were determined by flame atomic absorp-tion spectrometry on a Perkin-Elmer 3300 atomic absorptionspectrometer (Norwalk, CT, USA), equipped with a high-sensitivity nebulizer. Hollow cathode lamps for copper, zinc,cadmium and lead were employed following the manufac-turer’s recommendations for the respective atomic absorptionspectrometers. The calculations were made using standardcurve calibration. The concentrations of cadmium and leadwere analysed by electrothermal atomic absorption spectro-metry on a Zeeman atomic absorption spectrometer (Perkin-Elmer 4110 ZL, Norwalk, CT, USA) equipped with a THGAgraphite furnace and an AS 72 autosampler. Diammoniumhydrogen phosphate and magnesium nitrate were used as acombined matrix modifier for both elements. Quantificationwas made by means of peak height measurements and standardcurve calibration. The elemental analyses are all accreditedby the Norwegian Metrology and Accreditation Service. Thetrueness and precision of the analyses with each set of sampleswere controlled by analyses of standard reference materials(SRM). SRM of blue mussels was not available and thereforeBovine Liver 1577b from the National Institute of Standardsand Technology (NIST) was used for cadmium, copper andzinc, and TORT-2, lobster hepatopancreas, from the NationalResearch Council of Canada was used for lead. The SRMchosen had an element concentration quite similar to thatfound in blue mussels. The results for all sets of analysis areshown in Table 1. The elemental analyses used were found tobe satisfactory. The data are presented as the mean¡standarddeviation.

Results and discussion

The zinc plant in Odda ceased its release of jarosite in 1986 anda large project to cover up polluted sediments was performed in1990. In addition, several other minor measures have beentaken to minimize the release of heavy metals from the plant.

Cadmium

The results for cadmium in blue mussels sampled in 1998 aregiven in Table 2. The data show a correlation between thecadmium concentrations and the distance from the zinc plantresponsible for the discharge of heavy metals to the fjord untilthe mid-1980s. Since cadmium is partly soluble in seawater, theelement is transported with the water mass and diluted. Bluemussels sampled at Mage (13 km from the zinc plant) showeda mean cadmium concentration of 1 mg kg21 fresh weight.The mean cadmium concentration from Utne, 40 km fromthe zinc plant, was 0.57 mg kg21 fresh weight, whereas themean cadmium concentration from Gravdal, approximately105 km from the zinc plant, was 0.37 mg kg21 fresh weight.Table 2 also shows the mean cadmium concentrations inblue mussels sampled in 1983 and 1992 from Mage, Utne,Norheimsund and Gravdal.5,6 The data clearly show thatthe Hardangerfjord was very heavily cadmium polluted in1983. Reports on cadmium concentrations in blue musselsfrom the 1970s showed an increase in the concentration fromthat time until 1983.3,4 Julshamn4 reported a cadmium concen-tration in blue mussels from Mage of 50 mg kg21 dry weight,corresponding to approximately 9 mg kg21 fresh weight.Stenner and Nickless3 reported a cadmium concentration of140 mg kg21 dry weight (20 mg kg21 fresh weight) in bluemussels sampled 10 km from the zinc plant. In the period from1983 to 1992, the mean cadmium concentrations in bluemussels from Mage decreased from 18 mg kg21 fresh weight to2.4 mg kg21 fresh weight, which corresponds to a decrease of87%. The cadmium concentrations from Utne, Nordheimsundand Gravdal showed a relative decrease from 1983 to 1992 ofapproximately 90%. The mean cadmium concentrations in bluemussels further decreased in the period from 1992 to 1998(Table 2). The relative decrease in the period was from 40% to66%. The most substantial decrease was seen in the samplesfrom Mage and Utne. However, the improvement will beslower as the cadmium concentrations approach ‘the highbackground level’.8 The decrease in the mean cadmiumconcentrations from 1992 to 1998 can be attributed to theeffect of covering up the sediments at the discharge site withfibre cloths, and the slow replacement of polluted sedimentswith new sediments. Others9 have also reported on the positivedevelopment of the environment of Hardangerfjord. Unfortu-nately, uncontrolled discharge of heavy metals from the zincplant has happened from time to time during the last few

Table 1 Concentration of cadmium, lead, copper and zinc (mean¡s)in standard reference material (Bovine Liver 1577b, NIST, used forcadmium, copper and zinc; TORT-2, National Research Council ofCanada, used for lead). Analyses were carried out in the period fromSeptember 1998 to September 1999

Element naMean/mg kg21 s RSD (%)

Certified valuesb/mg kg21

Cadmium 35 0.50 0.02 4 0.50¡0.03Lead 30 0.39 0.04 10 0.35¡0.13Copper 34 167 2 1 160¡8Zinc 43 129 5 4 127¡16aNumber of analyses. bMean and 95% confidence interval.

Table 2 Means¡s (mg kg21 fresh weight) of cadmium in soft part ofpooled blue mussels (Mytilus edulis) from various sampling sites inHardangerfjord in the period from 1983 to 1998. The size of bluemussels was between 3.0 and 4.0 cm

Site 1983 1992 1998

Mage 18¡1 2.4¡0.6 1.0¡0.1Utne 12¡1 1.4¡0.4 0.57¡0.05Nordheimsund 8.1¡0.4 1.0¡0.1 0.48¡0.04Gravdal 4.7¡0.5 0.45¡0.05 0.37¡0.03

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years.10 Blue mussels sampled in unpolluted waters showcadmium concentrations between 0.05 and 0.2 mg kg21 freshweight.11,12 Thus, blue mussels sampled in Hardangerfjord arestill judged to be cadmium polluted, even though heavy metalloadings to the Hardangerfjord have improved substantiallyduring the last 20 years.

Lead

The mean lead concentrations in blue mussels sampled in 1998are shown in Table 3. The data show a decrease in the leadconcentrations throughout the fjord. Blue mussels sampled atMage showed a mean lead concentration of 1.5 mg kg21 freshweight, whereas the lead concentrations in mussels from Utne,Nordheimsund and Gravdal were 1.3, 0.52 and 0.70 mg kg21

fresh weight, respectively. The data given in Table 3 also showthe mean lead concentrations in blue mussels sampled in 1983and 1992.5,6 The mean lead concentrations clearly show thatthe Hardangerfjord was very polluted with lead at that time.Reports on lead concentrations in blue mussels from the 1970sshowed lower concentrations at that time compared withanalyses from 1983.3,4 Julshamn4 reported a lead concentrationin blue mussels from Mage of 530 mg kg21 dry weight,corresponding to 80 mg kg21 fresh weight (with a dry mattercontent of 150 g kg21 fresh weight). Stenner and Nickless3

reported a lead concentration of 3100 mg kg21 dry weight,corresponding to 465 mg kg21 fresh weight, in blue musselssampled 10 km from the zinc plant. If the lead analyses do notcontain systematic errors, this value for lead is the highest everreported in blue mussels. In the period from 1983 to 1992, themean lead concentrations in blue mussels from Mage decreasedfrom 120 to 6 mg kg21 fresh weight. This corresponds to arelative decrease in the lead concentration of 95%, whereas therelative decreases in lead concentration from Utne andNordheimsund were 97% and 98%, respectively. The differencebetween the relative decreases in the concentrations ofcadmium and lead in blue mussels may be due to the chemicalforms of the elements in the seawater. The reason for thedecrease in lead concentration in this period is the same asmentioned above for cadmium. Table 3 also shows that themean lead concentrations in blue mussels from Mage decreasedfrom 6 mg kg21 fresh weight in 1992 to 1.5 mg kg21 freshweight in 1998. The relative decrease was 75%. The decrease inthe mean lead concentrations at the other localities in theperiod was approximately 40%. However, the lead concentra-tions in blue mussels from the area studied showed mean valueshigher than ‘the high background level’ of 0.5 mg kg21 freshweight.8 Others9 have also reported the positive development ofthe environment of the Hardangerfjord regarding lead. Bluemussels sampled in unpolluted waters along the Norwegiancoast show lead concentrations between 0.05 and 0.3 mg kg21

fresh weight.13

Copper

The mean copper concentrations in blue mussels sampled in1998 varied from 0.9 mg kg21 fresh weight at Mage to0.7 mg kg21 fresh weight at Gravdal (Table 4). A similar

concentration range of copper was also found in musselssampled in 1992,6 whereas the concentration range for thesamples from 1983 was slightly higher, but still low.5 Thecopper concentration in blue mussels sampled at Mage inSeptember 1975 was 1.5 mg kg21 fresh weight.4 The copperdischarge to the fjord does not seem to have had any effect onthe copper concentrations in blue mussels from the localitiesstudied. The blue mussel is not regarded as a good surveillanceorganism for copper pollution because of its ability to regulatecopper levels in soft tissue even when exposed to high levels ofthe metal.14,15 The copper concentration found in blue musselsfrom the Hardangerfjord corresponds to the copper concen-tration found in blue mussels from unpolluted areas, and islow compared with the ‘high background level’ of 3 mg kg21

fresh weight.8 Copper concentrations in blue mussels fromthe Bergen Harbour area showed values between 1.0 and5.0 mg kg21 fresh weight,12 which indicated copper pollution inthis area. On the other hand, the cadmium concentrations inthese mussels were low. The copper concentration in oysters(Ostrea edulis), however, is approximately 20 times higher thanthat found in blue mussels sampled at the same locality.16

Zinc

Zinc is an essential trace element for humans and fish, but isalso regarded as a pollution problem in some areas. Comparedto copper, blue mussels provide a good indication of elevatedzinc concentrations in water. The mean zinc concentrationssampled in 1998 are shown in Table 5. The highest zincconcentrations were found in blue mussels sampled at Mage,with a mean concentration of 27 mg kg21 fresh weight, whereasthe mean zinc concentration decreased to 17 mg kg21 freshweight at Utne. At all sampling sites, the mean zinc con-centrations were lower than the ‘high background values’ inblue mussels from unpolluted areas.8 Table 5 also shows datafor the mean zinc concentrations in blue mussels sampled in1983 and 1992 from the same localities as in 1998. The meanzinc concentrations in blue mussels from 1983 varied from120 mg kg21 fresh weight at Mage to 80 mg kg21 fresh weightat Gravdal. The zinc concentration in blue mussels decreasedfrom 160 mg kg21 fresh weight in 1975 to 120 mg kg21 freshweight in 1983.4,17 This is in accordance with the reduction inmetal loadings from the end of the 1970s, as claimed byindustry. A relative decrease of 67–80% was found for zinc inblue mussels sampled between 1983 and 1992 (Table 5). Afurther decrease in the mean zinc concentrations took place in

Table 3 Means¡s (mg kg21 fresh weight) of lead in soft part of pooledblue mussels (Mytilus edulis) from various sampling sites in Hard-angerfjord in the period from 1983 to 1998. The size of blue mussels wasbetween 3.0 and 4.0 cm

Site 1983 1992 1998

Mage 120¡10 6¡2 1.5¡0.1Utne 65¡8 2.2¡0.1 1.3¡0.2Nordheimsund 40¡5 0.9¡0.1 0.52¡0.06Gravdal 10¡1 1.2¡0.2 0.7¡0.2

Table 4 Means¡s (mg kg21 fresh weight) of copper in soft part ofpooled blue mussels (Mytilus edulis) from various sampling sites inHardangerfjord in the period from 1983 to 1998. The size of bluemussels was between 3.0 and 4.0 cm

Site 1983 1992 1998

Mage 1.1¡0.2 0.9¡0.2 0.9¡0.3Utne 1.2¡0.2 0.9¡0.1 0.9¡0.2Nordheimsund 1.3¡0.4 0.9¡0.2 0.9¡0.1Gravdal 0.9¡0.3 0.7¡0.2 0.7¡0.2

Table 5 Means¡s (mg kg21 fresh weight) of zinc in soft part of pooledblue mussels (Mytilus edulis) from various sampling sites in Hard-angerfjord in the period from 1983 to 1998. The size of blue mussels wasbetween 3.0 and 4.0 cm

Site 1983 1992 1998

Mage 120¡15a 40¡10a 27¡3a

Utne 110¡15a 21¡3 17¡4Nordheimsund 89¡4b 21¡4 19¡2Gravdal 80¡4c 20¡4 13¡3abcMeans in the same row sharing a common superscript letter arenot significantly different (P¢0.05; one-way analysis of variance).

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the period from 1992 to 1998. The relative decrease rangedfrom 19% to 33%, with the greatest reduction at Mage. Thepresent data for zinc show no zinc pollution in the fjord fromUtne and outwards.12,18 Others10 have also reported on thepositive development of the environment with regard to zincconcentrations in blue mussels.

Conclusions

In conclusion, the levels of metals in blue mussels sampled fromthe Hardangerfjord water system show that the area is stillslightly contaminated with cadmium and lead. However, it isamazing that the fjord system has recovered to such an extentover the last 20 years. With regard to human consumption ofblue mussels from the Hardangerfjord, none of the elementsanalysed should give any cause for concern for consumers, asthe European Union is proposing an upper limit of heavymetals in seafood of 1.0 mg kg21 for cadmium and 1.0 mg kg21

for lead.

References

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3 R. D. Stenner and G. Nickless, Water, Air, Soil Pollut., 1974, 3,279.

4 K. Julshamn, Fisk. Dir. Skr. Ser. Ernæring, 1981, 1, 215.5 K. Julshamn and O. Grahl-Nielsen, Mar. Pollut. Bull., 1996, 32,

564.6 C. Børnes, Cand. Scient. Thesis, University of Bergen, 1994.7 N. J. MacKay, R. J. Williams, J. L. Kacprzac, H. N. Kazacos,

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13 K. Julshamn, unpublished work, 2001.14 C. Amirad-Triquet, B. Berhet, C. Metayer and J. C. Amirad, Mar.

Biol., 1986, 92, 7.15 D. J. H. Phillips, Mar. Biol., 1976, 38, 59.16 K. Julshamn, Fisk. Dir. Skr. Ser. Ernæring, 1981, 1, 267.17 K. Julshamn, K. E. Slinning, H. Haland, B. Bøe and L. Føyn,

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18 S. D. Berrow, Mar. Pollut. Bull., 1991, 22, 467.

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