the Science of the

-IbtalEnvIrolltnent
F
: TheScienceof the TotalEnvironmentZOl(1997)211-224

Heavy metal contamination in freshwater fish from the

border region between Norway and Russia

Per-Arne Amundsenat* , Frode J. Staldvik”, Anatolij A. Lukinb,

Nikolai A. Kashulinb, Olga A. Popova”, Yuri S. Reshetnikov”
“Norwegian College of Fishery Science, Universi~ of Troms& N-9037 Trams@, Norway
hlnstitute of North Ecological Industrial Problems, Kola Science Center, 14 Fersman Str., Apatity, Murmansk Region, Russia
‘A.N. Severtzov Institute of Ecology and Animal Morphology, Russian Academy of Sciences, Moscow, Russia

Received12February1997;accepted
8 April 1997

Abstract

The contentsof Cd, Cu, Cr, Hg, Ni and Zn in muscle,liver and gills were studiedin whitefish, perch, pike, brown
trout, burbot and vendace from three iake localities in a watercoursein the border region between Norway and
Russia,in the vicinity of mining activity and severalmetallurgic smelters.The contents of Cd and Ni in fish tissue
increasedwith increasingproximity to the smelters,whereasthe other elementsshowedsimilarconcentrationsat the
three localities. The recorded heavy metal concentrationsappearedto be within the rangesreported for fish from
other metal-contaminatedlakes,and higher than comparableobservationsfrom unpolluted systems.The heavy metal
concentrationswere usually lowest in muscleand highest in the liver or the gills. Significant differences in metal
concentration levels were found between different fish species,but Hg was the only metal where these species
differenceswere possiblyrelated to biomagnification.For the other elements,the concentrationsgenerally appeared
to be inversely related to the trophic level of the fish species. 0 1997Elsevier ScienceB.V.

Keywords: Heavy metals;Freshwaterfish; Pasvik River system;Norway; Russia

___

1. Introduction environmental pollution (Kelly, 1988). In aquatic

ecosystems, heavy metals have received consider-
Emission of heavy metals from mining activity, able attention due to their toxicity and accumula-
smelters and industry is the source of serious tion in biota (Mance, 1987; Mason, 1991). Some
of these elements are toxic to living organisms
even at quite low concentrations, whereas others
*Corresponding
author. are biologically essential and natural constituents

0048-9697/97/$17.00
0 1997ElsevierScienceB.V. All rightsreserved.
PI1 SOO48-9697(97>00125-3
212 P.-A. Amundsen et al. / The Science of the Total Environment
of the aquatic ecosystems and only become toxic
at very high concentrations. In fish, the toxic
effects of heavy metals may influence both physi-
ological functions, individual growth rates, repro-
duction and mortality (Mance, 1987; Sorensen,
1991; Woodward et al., 1994, 1995; Farag et al.,
1994, 1995). Heavy metals may enter fish bodies
in three possible ways: through the body surface,
the gills or the digestive tract (Dallinger et al.,
1987; Pourang, 1995). The gills are regarded as
the important site for direct uptake from the
water (Hughes and Flos, 1978; Thomas et al.,
1983; Dallinger et al., 19871, whereas the body
surface is generally assumed to play a minor role
in heavy metal uptake of fish (Varanasi and
Markey, 1978; Dallinger et al., 1987; Pourang,
1995). Food may also be an important source for
heavy metal accumulation (e.g. Aoyama et al.,
1978; Patric and Loutit, 1978; Dallinger and
Kautzky, 1985; Dallinger et al., 1987), potentially
leading to biomagnification, the increase of pollu-
tants up the food chain (Mason, 1991).
Major metallurgic industries are located in the
Murmansk Region in northwest Russia, with large
emissions of dust, heavy metals and sulphur diox-
ide. In the border region between Russia and
Norway, the main pollution sources are the
smelters of the Pechenganickel Company located
in the towns of Nikel and Zapolyarny. The Pasvik
River system, which is the main border river
between Russia and Norway, is located near the
smelters. The lower part of the Pasvik River
drains the Nikel smelters directly through Kuets-
jarvi, a lake which is situated in a sidebranch to
the main watercourse (Fig. 1). Pollutants may
enter the water system both via deposition of
atmospheric emissions and direct run-off from
slag piles. High contaminations of heavy metals
have been recorded in water and sediments in the
vicinity of the smelters (Traaen et al., 1991; Du-
valter, 1992, 1994; Moiseenko et al., 1995), pos-
sessing a potential threat to fish and other biota
in the water system. Increased levels of heavy
metals have also been observed in terrestrial
plants, birds and mammals in areas adjacent to
the smelters (Aamlid, 1992; KUs et al., 1995).
In the present work, the heavy metal concen-
trations in freshwater fish from the Pasvik River
201 (1997) 211-224
system were investigated. Three lake localities
with presumably different exposures to the pollu-
tant sources were studied; Kuetsjarvi close to the
smelters, Bjornevatn 13 km downstream and
Vaggatem 45 km upstream in the main water-
course (Fig. 1). The contents of cadmium, copper,
chromium, mercury, nickel and zinc were ana-
lyzed in muscle, liver and gills of the fish.
2. Study area and fish communities
The sub-arctic Pasvik River system runs along
the national border between Norway and Russia,
originating from Lake Inari in Finland (Fig. 1).
The Norwegian-Russian part of the river system
is 120 km long, has a total area of 142 km*, a
catchment area of 20.890 km2, and a mean water-
flow of about 175 m3/s. There are altogether
seven water impoundments in the Pasvik River
system. Previous rapids and waterfalls have disap-
peared, and the river system is dominated by
consecutive lakes and reservoirs. The water level
fluctuations are small, and usually less than 80
cm. The ice-free season in the lakes and reser-
voirs last from May/June to October/November.
Vaggatem (69” 14’ N, 29” 12’ E; 52 m above sea
level) is a lake situated in the upper part of the
main water course, Bjornevatn (69” 31’ N, 30” 7’
E; 22 m a.s.1.) in the lower part, and Kuetsjarvi
(69” 27.’ N, 30“ 11’ E; 23 m a.s.1.) in a tributary to
the main watercourse. The lakes are oligotrophic
with humic impacts (see Nest et al. (1991) and
Langeland (1993)). The geology in the region is
dominated by bedrock, mainly containing gneiss.
A birch- and pinewood landscape with stretches
of boggy land surrounds the watercourse. The
annual mean air temperature is low (-3‘0, and
the minimum and maximum monthly mean tem-
peratures are - 13.5”C and + 14.o”C, respectively.
The precipitation in the area is low, with an
annual mean of 358 mm.
The smelters in Nikel and Zapolyarny were
constructed for the processing of local ores, and
have been in operation since 1932 and 1955,
respectively. Since 1971, the smelters have
processed copper and nickel ores from Norilsk,
Central Siberia, which have a particularly high
sulphur content (Duvalter, 1994). In 1989, the
 P.-A. Amundsen et al. / The Science of the Total Environment 201 (1997) 211-224 213

Fig. 1. Map of the Pasvik River system.

annual emission of Ni and Cu to the atmosphere
from these smelters was estimated to be 504 and
300 metric tons, respectively (Sivertsen et al.,
1992).
Altogether 15 different fish species have been
recorded in the Pasvik River system, the most
commonly occurring species in the lakes are
whitefish (Coregonus lavaretus s.l.), perch (Perca
JzuviutiZis), pike (Esox lucks), burbot (Lotu lota)
and brown trout (Sulmo truttu). Vendace
(Coregonusalbula) h as recently invaded the Pasvik
River system, after being introduced to Lake Inari
in the 1960s. The whitefish consists of two differ-
ent morphs, differentiated by the morphology and
number of gill rakers, and referred to as densely
and sparsely rakered whitefish. The densely rak-
ered whitefish has numerous long and densely
spaced gill rakers (mean number 33.01, whereas
214 P.-A. Amundren et al. /The
the sparsely rakered form has fewer, shorter and
more widely spaced rakers (mean number 23.1).
According to Reshetnikov (1980), the two forms
may be referred to as C. lavaretus lavaretus
(densely rakered whitefish) and C. Zavaretzu pid-
schian (sparsely rakered), whereas Svfrdson (1957)
(1979) described these forms as two different
species; Coregonus lavaretus and C. nasus, respec-
tively.
3. Materials and methods
Fish were sampled both in 1991 and 1992 from
Kuetsjarvi, Bjarnevatn and Vaggatem. In 1991,
sampling was accomplished from July 14 to July
22, and from September 2 to September 15; and
in 1992, from June 22 to July 4, and from August
31 to September 16. Fish were sampled both in
the littoral, profundal and pelagic zones using
gillnets. The gillnets were 40 m long containing
eight sections of 5 m with different mesh sizes.
The mesh sizes used were 10, 12.5, 15, 18.5, 22,
26, 35 and 45 mm (knot to knot). In the littoral
and profundal zone, 1.5-m deep bottom nets were
used, whereas in the pelagic zone, 4-m deep
floating nets were employed. In addition, special
nets for pike were used, with mesh sizes 35, 45,
52. 63 and 74 mm. The fish samples included
densely and sparsely rakered whitefish, perch,
pike, brown trout, burbot and vendace. The fish
were weighed and fork length was measured. Sto-
machs were removed, conserved in 96% ethanol,
and the contents later analyzed. Samples of fish
tissue for heavy metal analysis were dissected
from muscle, liver and gills using stainless steel
implements, and frozen in sample tubes.
The heavy metal analyses were conducted at
the laboratory of The Norwegian Institute for
Nature Research, and included cadmium (Cd),
chromium (Cr), copper (CL& mercury (Hg), nickel
(Ni) and zinc (Zn). The samples were freeze-dried
for 24 h to a final pressure of 0.05 mbar at
-53°C. From each sample (standard 0.3-0.4 g
dry weight), the organic matter was extruded us-
ing concentrated nitric acid (HNO,), and the
content of heavy metals was determined by atomic
absorption spectroscopy (AAS) (Perkin Elmer
Science of the Total Environment 201 (1997) 211-224
Model 1100 B). Cd, Cu, Ni and Zn were analyzed
by flame AAS, Cr by using graphite-furnace HGA
700 with automatic sampler AS 70, and Hg by
using a hydride system (FIAS 200) with automatic
sampler AS 90. NaBH, was used as reducing
agent. The concentrations of heavy metals in fish
are expressed as pug/g dry weight of tissue. The
detection limits were 0.01 pg/g for Cd, 0.15
pg/g for Cr, 0.5 pg/g for Cu, 0.015 pg/g for Hg,
0.1 pg/g for Ni, and 0.5 pg/g for Zn. The
accuracy of the analytical procedures was checked
against the National Bureau of Standards (NBS)
for dogfish muscle DOLT-l. The accuracy of the
analytical procedures was satisfying for most met-
als, but for Cr, only 50-60% of the certified
values could be detected, and for Hg 85% (S.
Lierhagen, The Norwegian Institute for Nature
Research, personal communication).
The mean lengths of fish sampled for heavy
metal analysis are presented in Table 1. Brown
trout from Kuetsjarvi and burbot from Vaggatem
have been omitted in the presentation of the
results due to low observation numbers, whereas
vendace was not caught at all in Bjornevatn and
Kuetsjarvi. In Kuetsjarvi, no gill tissue samples
from perch were analyzed, whereas in fish from
Bjornevatn, the concentrations of Cr were not
analyzed in any tissue and Cd only in liver. Cu
concentrations were not analyzed in gills from
any species.
Distributions of heavy metal concentrations are
frequently skewed and non-normal (Giesy and
Wiener, 1977). Non-parametric statistics (Mann-
Whitney and Kruskal-Wallis tests) have therefore
been used in testing differences between samples.
Simple linear regression analysis has been used to
test for correlation between heavy metal concen-
trations and fish length.
4. Results
4.1. Tissue concentrations of hea y metals
With a few exceptions, there were rarely any
significant correlations between the tissue con-
centrations of heavy metals and the size of the
individual fish. For Zn, however, a significant
 P.-A. Amundsen et al. / The Science of the Total Environment 201 (1997) 211-224 215

Table 1
Mean length with range (in cm) and number (n) of fish analyzed for heavy metal contents in Vaggatem, Bjarnevatn and Kuetsjarvi

Vaggatem Bjamevatn Kuetsjarvi

Length Range n Length Range n Length Range n

Densely rakered whitefish 17.5 lo-29 12 19.2 lo-29 12 17.0 9-26 16

Sparsely rakered whitefish 25.2 12-36 16 26.1 lo-40 18 22.7 10-44 26
Perch 22.1 12-30 18 24.1 9-36 19 17.1 15-18 7
Pike 38.2 20-50 17 44.4 28-55 16 45.0 35-52 9
Brown trout 30.0 27-34 5 41.9 30-55 11 21.0 20-22 2
Burbot 1 29.3 18-47 7 54.6 53-57 4
Vendace 13.8 9-16 5 0 0

decrease in concentrations in muscle with increas-
ing fish length was found for both densely rakered
whitefish, sparsely rakered whitefish and perch. A
similar significant decrease in liver concentrations
of Zn was also found in densely and sparsely
rakered whitefish. For the other elements there
were rarely any significant differences with in-
creasing fish lengths, and in the further presenta-
tion of the results, the mean values of heavy
metal concentrations for each fish species have
been used, irrespective of the size of the fish.
The mean concentrations of heavy metals in
muscle, liver and gills from the different fish
species at the three different localities are pre-
sented in Fig. 2. Zinc made up the highest con-
centrations both in muscle, liver and gills of the
fish. Considering all fish species and localities, the
mean concentrations of heavy metals in muscle
varied from 0.01-0.81 pg/g Cd, 0.17-0.45 pg/g
Cr, 1.6-12.3 pg/g Cu, 0.16-0.89 pg/g Hg,
0.48-3.1 pg/g Ni, and 17-63 pg/g Zn. In the
liver, the concentrations varied from 0.40-4.3
pg/g Cd, 0.19-0.46 pg/g Cr, 11-180 pg/g Cu,
0.14-1.1 pg/g Hg, 0.58-9.0 pg/g Ni, and 98-614
pg/g Zn, and in the gills from 0.02-0.28 pg/g
Cd, 0.64-2.0 pg/g Cr, 0.03-0.10 pg/g Hg,
0.4-9.13 E*.g/g Ni, and 75-675 pg/g Zn (Fig. 2).
The maximum heavy metal concentrations
observed in the muscle of individual fish were
(name of species in brackets): 3.0 pg/g Cd
(densely rakered whitefish), 2.0 pg/g Cr (pike),
40.5 pg/g Cu (densely rakered whitefish), 2.0
pg/g Hg (perch), 8.0 pg/g Ni (densely rakered
whitefish), and 430 pg/g Zn (pike). In the liver,
the maximum recorded levels of individual fish
were 10 pg/g Cd (densely rakered whitefish), 1.0
pg/g Cr (densely rakered whitefish), 354 pg/g
Cu (brown trout), 2.0 pg/g Hg (brown trout), 18
pg/g Ni (sparsely rakered whitefish), and 891
pg/g Zn (sparsely rakered whitefish), whereas for
the gills, the highest observations were 0.69 pg/g
Cd (densely rakered whitefish), 3.0 pg/g Cr
(pike), 0.3 pg/g Hg (pike), 17.3 pg/g Ni (densely
rakered whitefish), and 1406 pg/g Zn (densely
rakered whitefish).
For most elements, the lowest concentrations
of heavy metals were found in the muscle (Table
2 and Fig. 2). For Cd, the highest concentrations
were always found in the liver, with levels many
times higher than in the muscle, although there
were large variations both between the different
fish species and the localities. The contents of Cr
in the liver were generally twice as high as in the
muscle, whereas the highest levels of Cr were
found in the gills. The Cu concentrations were
always higher in the liver than in the muscle, with
particularly high ratios in sparsely rakered white-
fish and brown trout. The recorded Hg concentra-
tions were always lowest in the gills, whereas the
liver contents of Hg generally were equal or
slightly higher than in the muscle. For Ni, the
levels in liver and gills generally were of similar
magnitude, and a few times higher than in the
muscle. The relative proportion of Ni in the gills
appeared to increase with decreasing distance
from the smelters. Zn had lowest concentrations
in the muscle, and, with the exception of perch,
the highest concentrations were found in the gills
(Table 2).
216 P.-A. Amundsen et al. / The Science of the Total Environment 201 (1997) 211-224

Vaggatcm Bjernevatn Kuetsjavri

3
l!iiiJm’ll1l.
15”
1.0

0.5

0.0

1.0
0.8
0.6
0.4
0.2
0.0
10

.W 8
6
z 4
2

*oi
600
400
200
0
1234567 1234567 1234567

Fish species
Fig. 2. Mean concentrations (fig/g dry weight) of Cd, Cr, Cu, Hg, Ni and Zn in muscle (black bars), liver (white bars) and gills
(hatched bars) in fish from three different lake localities in the Pasvik River system. The fish species are indicated by numbers: (1)
densely rakered whitefish, (2) sparsely rakered whitefish, (3) perch, (4) pike, (5) brown trout, (6) burbot, and (7) vendace.

4.2. Heay metal contamination in j&h from different
localities
For a few of the examined elements, the tissue
concentrations of heavy metals were significantly
different between the three investigated lake lo-
calities. In particular, the concentrations of Ni in
liver and gills decreased with increasing distances
from the smelters (Fig. 3). Similarly, the observed
concentrations of Cd in muscle and gills were
highest in Kuetsjarvi in the vicinity of the smelters,
and lowest in Vaggatem at the upper part of the
water course (Fig. 3). In the gills, the differences
between the localities in concentrations of both
Ni and Cd were most profound for densely and
sparsely rakered whitefish, whereas perch exhib-
ited the strongest difference in muscle contents of
Cd. For elements other than Ni and Cd, there
were generally no significant differences in con-
centration levels in fish tissue between the three
investigated lake localities.
4.3. Trophical statusand heay metal contamination
of different fish species
The most important habitat and prey choices of
lacustrine fish species in the Pasvik River system
are presented in Table 3. Adults of both pike,
 P.-A. Amundsen et al. / The Science of the Total Enviromnt 201 (1997) 211-224 217

Table 2
Ratios between muscle, liver and gills (M&G) in concentrations of heavy metals in different fish species at the three different
localities

Fish species Cd Cr cu Hg Ni Zn
and locality

Densely rakered whitefish

Vaggatem 1:3:3 1:2:8 1:2.5:- 3:7:1 1:4:1 1:7:15
Bjamevatn - - 1:2.5:- l:l:- 3:4:2 1:6:14
Kuetsjarvi 1.5:9:1 1:2:3 1:6.5:- 2:2:1 1:6:9 1:5:10
Sparsely rakered whitefish
Vaggatem 1:200:4 1:2:- 1:18:- 1:5:3 1:6:1 1:7:18
Bjamevatn - - 1:13:- 1:2:- 1:2:3 1:9:36
Kuetsjarvi 1:150:13 1:1.5:- 1:12:- 1:6:4 1:8:9 1:8:26
Perch
Vaggatem 1:200:6 l:l:- 1:12:- 1:1:0.1 1:1:2 1:6:4
Bjemevatn - - 1:1.7:- l:l:- I:22 1:5:4
Kuetsjarvi 1:5:- - 1:5:- l:l:- 1:5:- 1:8:-
Pike
Vaggatem 1:100:2 l:l:- 1:5:- 7:4:1 2:3:1 1:8:20
Bjtimevatn - - 1:3:- 1:1.5:1 l:l:- 1:13:24
Kuetsjarvi 1:4:0.5 1216 - 1.4:3:1 1:1.8:2.3 1:3:6
Brown trout
Vaggatem - - l:llo:- 1:1.6:- 1:1.4:- 1:7:-
Bjtimevatn - - 1:15:- 1:2:- 1:2:- 1:7:-
Burbot
Vaggatem - - - - 1:3:5
Bjemevatn - - - - - -

Vendace
Vaggatem - - 1:18:- 1:2:- - 1:17:-
-
- indicates insufficient or missing observations.

perch and brown trout were predominantly pisciv-
orous, and particularly pike and brown trout fed
heavily upon whitefish. Burbot, which most com-
monly was caught in the profundal zone, feed
both on zoobenthos and fish. The coregonids
(densely and sparsely rakered whitefish and ven-
date) were all restricted to invertebrate feeding.
The densely rakered whitefish occurred fre-
quently in all major habitats of the lakes in the
Pasvik river system, feeding both on zooplankton
and benthic prey. The sparsely rakered whitefish
were found to be restricted to the benthic habi-
tats feeding on zoobenthos, whereas vendace al-
most exclusively fed upon zooplankton in the
pelagic zone (Table 3).
Significant differences in heavy metal contents
between different fish species were found for Hg
and Zn in muscle, Hg, Zn, Cd, Ni, Cu and Cr in
liver, and Hg, Zn and Cd in gills (Table 4;
Kruskal-Wallis test, P < 0.05). For Hg, the muscle
concentrations were in general highest for the
piscivorous species, and lowest for the inverte-
brate feeders. Brown trout had the highest Hg
concentrations in the liver, whereas pike had the
highest Hg levels in the gills. Vendace and den-
sely rakered whitefish had the highest concentra-
tions of Zn in muscle and liver, and sparsely
rakered whitefish in the gills, whereas perch gen-
erally had the lowest Zn contents. The coregonid
species also had the highest levels of Cd both in
liver and gills, whereas the piscivorous species
had the lowest. Further, for both Ni and Cr, the
218 P.-A. Amunaken et al. / The Science of the Total Environment 201 (1997) 211-224

.I 0.8- Cd
s
,*R 0.6 -
::
”g 0.4
7 e---- Dr. w.firh
2%
g 0.2 - l - - S.r. w.fish
a--- Porch
n -. Pike
Kuotrj. Vnggotcm Knotrj. Vaggotsm
I I
Ni

e--- Dr. w.fish

l - - S.r. w.firh
a--- Perch
n- -- Pike

Fig. 3. Contaminations of Ni and Cd ( pg/g dry weight) in tissue of fish from Kuetsjati (close to the smelters), Bj0mevatn (13 km
downstream) and Vaggatem (45 km upstream).

Table 3
Predominant prey and habitat choices of lacustrine fish in the Pasvik River system

Fish species Dominant prey Dominant habitat

Densely rakered whitefish Zooplankton, benthic chydorids, dipteran pupae and larvae Pelagic, profundal and littoral
Sparsely rakered whitefish Dipteran pupae and larvae, molluscs, benthic chydorids Littoral, profundal
Perch Fish (9-sp. sticklebacks and whitefish), insect larvae Littoral
Pike Fish (whitefish, perch) Littoral
Brown trout Fish (whitefish) Littoral, pelagic
Burbot Insect larvae, fish Profundal, littoral
Vendace Zooplankton Pelagic

liver concentrations were highest in the corego-
nids and lowest in the piscivorous species, whereas
for Cu, the liver contents were highest for brown
trout, intermediate for the coregonid species and
lowest for pike and perch (Table 4).
5. Discussion
The six heavy metals studied in the present
investigation are all regarded as potential hazards
that can endanger both animal and human health
(Duffus, 1980; Mance, 1987). Knowledge of their
concentrations in fish is therefore important both
with respect to nature management and human
consumption of fish. The literature on metal up-
take and assimilation in fish may, however, be
both confusing and partly also conflicting (MC-
Farlane and Franzin, 1980). Chemical factors like
acidity, buffer capacity and the presence of Ca
and organic compounds, may, together with bio-
logical factors like habitat preferences, feeding
behaviour and growth rates, influence the
 P.-A. Amunaken et al. / The Science of the Total Environment 201 (1997) 211-224 219

Table 4
Ranking order of different fish species in the Pasvik River system according to their heavy metal contents. (Only species series with
significant differences are included; Kruskal-Wallis test, P < 0.05)

Hg
Muscle Burbot > Perch > B. trout = Pike > Vendace = D.r. whitefish = S.r. whitefish
Liver B. trout > Vendace > Perch > D.r. whitefish = S.r. whitefish > Pike
Gills Pike > Dr. whitefish > S.r. whitefish > Perch
Zn
Muscle D.r. whitefish > Vendace = Pike > Burbot > B. trout > Sr. whitefish = Perch
Liver Vendace > Pike = D.r. whitefish > Sr. whitefish = B. trout > Perch > Burbot
Gills S.r. whitefish > Pike = D.r. whitefish > Burbot > Perch
Cd
Liver Vendace > Dr. whitefish > S.r. whitefish > Perch > Pike > Burbot > B. trout
Gills S.r. whitefish = D.r. whitefish > Perch > Pike
Cr
Liver D.r. whitefish > S.r. whitefish > Perch > Pike
cu
Liver B. trout > Sr. whitefish > Vendace > Dr. whitefish > Pike > Perch
Ni
Liver Sr. whitefish > D.r. whitefish > Burbot > Perch > Pike > B.trout

bioavailability and accumulation of heavy metals
in fish (see e.g. McFarlane and Franzin, 1980;
Campbell and Stokes, 1985; Bradley and Morris,
1986; Dallinger et al., 1987; Sprenger et al., 1988;
Iivonen et al., 1992). Further, the predominant
pathways for heavy metal uptake appear to be
highly variable over the range of metals, contami-
nant levels and fish species studied (e.g. Williams
and Giesy, 1978; Dallinger et al., 1987). There
also seems to be large interspecific variation in
the assimilation of heavy metals from water and
food, as well as in the allocation of metals into
different organs and tissue. Additionally, the sen-
sitivity to heavy metals and the ability for
homeostatic control, detoxification and rejection
appear to be highly variable for different ele-
ments and fish species (e.g. Wiener and Giesy,
1979; Dallinger et al., 1987). Intraspecific differ-
ences related to e.g. age, size and physiological
status of the fish may also be of importance.
Moreover, numerous potential interactions
between different elements may influence both
the assimilation and toxicity of the metals (Soren-
sen, 1991). Thus, the heavy metal concentrations
in fish tissue may appear to be the result of a
complex interaction of many factors (Wiener and
Giesy, 1979; McFarlane and Franzin, 1980;
Dallinger et al., 19871, and Dallinger et al. also
emphasised the importance of taking the specific
ecological situation of a given environment into
consideration when investigating heavy metal pol-
lution in fish.
The studied fish species in the Pasvik River
system are important constituents of the limnetic
ecosystems in the lakes, and are also being ex-
ploited for human consumption. Coregonids,
perch, pike, brown trout and burbot have circum-
polar distributions, and although data on heavy
metal concentrations in Arctic and temperate fish
populations are limited, some comparable studies
exist. Allen-Gil and Martynov (1995) studied
heavy metal contents in muscle from fish in the
Pechora River, northern Russia. The muscle con-
tents of cadmium and copper found in the pre-
sent study were many times higher, and zinc con-
centrations slightly higher, than those found in
coregonids, perch and pike in the Pechora River.
Further, the concentrations of cadmium, copper
and zinc in muscle and liver of Pasvik fish were
generally higher than those found at two localities
220 P.-A. Amundren et al. / The Science of the Total Environment
in the Great Lakes (Brown and Chow, 1977),
whereas mercury levels were of similar magnitude
(conversions between dry and wet weight of fish
have been done by assuming 78% water contents).
Also, the concentrations of cadmium, copper and
zinc in liver of pike, perch, whitefish and brown
trout from the Pasvik River system were in gen-
eral higher than average concentrations found in
the same species from 14 unpolluted Finnish
lakes; although in these lakes, the mercury levels
in muscle were higher than in Pasvik (Iivonen et
al., 1992). Bradley and Morris (1986) studied heavy
metals in fish (including whitefish, perch and pike)
in a series of lakes near Sudbury, Ontario, where
large quantities of copper, nickel and other met-
als have been released into the environment from
several smelters. The levels of copper, nickel and
zinc in muscle and liver of fish from Pasvik were
similar or slightly higher than those found in
these metal-contaminated lakes. Pike from the
Pasvik River systems did, on the other hand, have
lower levels of cadmium and copper in the liver
compared to the maximum contaminations
recorded in pike from lakes near a base metal
smelter at Flin Flon, Manitoba, whereas the mer-
cury levels were of similar magnitude (McFarlane
and Franzin, 19801.
Concentrations of cadmium and nickel recorded
in fish tissue in the Pasvik River system, exhibited
significant increases with increasing proximity to
the smelters. For both metals, the lowest concen-
trations were found in Vaggatem and the highest
in Kuetsjarvi. The high levels of cadmium and
nickel in fish from Kuetsjarvi reflect the elevated
environmental levels of heavy metals that have
been found in the vicinity of the Pechenganikel
smelters (Duvalter, 1992, 1994; Moiseenko et al.,
1995). Both deposition of atmospheric emissions
from the smelters and direct run-off from slag
piles and mines may contribute to the metal con-
taminations in the Pasvik watercourse. Pollutants
may also be transported downstream by the water
Aow, although rapid sedimentation probably re-
strains this mode of heavy metal dispersal. The
cadmium contamination is likely to be most asso-
ciated with surface run-offs from the slag piles, as
elevated Cd concentrations in sediments have only
201 (1997) 211-224
been detected close to the Pechenganikel smelters
(Duvalter, 1994). For nickel, on the other hand,
the atmospheric emissions from the smelters are
large (Sivertsen et al., 1992), and apparently the
main pollution source for this element. Nickel
concentrations in sediments have been found to
be very high in Kuetsjarvi, intermediate in
Bjornevatn and small in Vaggatem (Rognerud et
al., 19931, and the declines in Ni levels in fish and
sediments with increasing distance from the
smelters, are probably related to rapid atmo-
spheric fallouts and deposition. The increasing
proportion of nickel in the gills with decreasing
distance from the smelters, may indicate that the
uptake over the gills becomes increasingly impor-
tant as the Ni contents in the water increases (see
also Sreedevi et al., 1992). For the other studied
metals, the lack of significant differences in fish
tissue concentrations with increasing distance
from the pollution source may suggest that the
exposures of these elements are similar through-
out the three localities. However, for most of
these metals, a decline in water and sediment
concentrations with increasing distance from the
smelters has been demonstrated (Duvalter, 1992,
1994; Moiseenko et al., 1995). The present find-
ings do, therefore, more likely reflect a poor
correlation in the concentrations of these ele-
ments between fish and environment. McFarlane
and Franzin (1980) emphasised that high Ca con-
centrations in lake waters may decrease metal
accumulation in fish. Due to large dust emissions
from the smelters, the Ca concentration in Kuets-
jarvi has been found to be very high (Traaen et
al., 1991; Nest et al., 19911, and this may have
moderated the metal accumulation of fish in the
lake. As a consequence, the heavy metal levels in
fish may not be a good indicator of the ambient
pollution levels (Wiener and Giesy, 1979; Bradley
and Morris, 1986). However, this also implies that
for an evaluation of the biological impacts of
heavy metal pollution, the actual metal concen-
trations in the fish, and not solely the metal levels
in water and sediments, should be taken into
consideration.
The Zn concentrations in fish tissue decreased
significantly with increasing length of the fish,
 P.-A. Amundsen et al. / The Science of the Total Environment 201 (1997) 21 l-224
which has also been demonstrated in several other
studies (e.g. Cross et al., 1973; Giesy and Wiener,
1977; Murphy et al., 1978; Wiener and Giesy,
1979). Patric and Loutit (1978) indicated that this
may partly be due to different adsorption rates
across the gut or more efficient excretion in older
fish. Zinc is an essential trace metal that is pre-
sumably homeostatically controlled (Frieden,
1972; Cross et al., 1973; Giesy and Wiener, 1977),
and negative correlations between metal concen-
trations and body size may also be a result of
homeostatic regulation (Wiener and Giesy, 1979).
These findings may, on the other hand, also be
related to the absorption rates of zinc across the
gills. Zinc was the only element that was found in
highest concentrations in the gills relative to the
muscle and liver contents. High concentrations of
a metal in the gills are indicative of a predomi-
nant uptake from water through the gills (Dal-
linger et al., 1987). The area of the gills relative to
body size decreases with increasing fish size
(Pauly, 1981>, and this may result in a larger
uptake of certain elements like zinc in the smaller
fish.
For all the elements studied, significant differ-
ences in concentration levels were found between
different fish species, demonstrating that the at-
tained concentration levels partly are species re-
lated. Generally, the two whitefish forms and
vendace seemed to have the highest concentra-
tions of zinc, cadmium, chromium and nickel,
whereas brown trout, burbot, perch and pike had
the highest concentrations of mercury. The sal-
monoid species had higher liver contents of cop-
per than pike and perch, which was also found by
Iivonen et al. (1992), and pike and perch seemed
in general to have lower accumulations of most
metals in the liver relative to the other species.
To a large extent the species differences in heavy
metal concentrations appeared to be related to
the trophic status of the fish species. Mercury
was, however, the only metal where these species
differences may be due to biomagnification. Par-
ticularly with respect to the muscle concentra-
tions, the mercury levels were highest in the pis-
civorous species and lowest in the invertebrate
feeders. Biomagnification of heavy metals in fish
221
is regarded as a controversial subject (Dallinger
et al., 1987), although biomagnification of mer-
cury along aquatic food chains has frequently
been reported (e.g. Jemlijv and Lann, 1971;
Sarkka et al., 1978; Mason, 1991). Biomagnifica-
tion of a pollutant may lead to toxic levels in
species high up in the trophic chain (Moriarity,
19841, and in freshwater systems, fish are usually
among the top consumers. In fish from the Pasvik
River system, the recorded levels of mercury were,
however, not high compared to other, comparable
fish studies (e.g. Haakanson et al., 1988; Iivonen
et al., 1992), and were well below the accepted
limits for human consumption (1 pg/g wet
weight). For the other elements, and especially
zinc and cadmium, the concentrations appeared
to be inversely related to the trophic status of the
fish.
Fish feeding on invertebrates have been found
to have higher concentrations of cadmium and
zinc than piscivorous species (Mathis and
Cummings, 1973; Windom et al., 1973; Murphy et
al., 1978). The results of the present study largely
supports these observations, as whitefish and ven-
date usually had the highest levels of these two
elements, and the piscivorous species the lowest.
In conclusion, the heavy metal concentrations
recorded in lacustrine fish from the Pasvik River
system appear to be within the ranges reported
for fish from metal-contaminated lakes, and
higher than comparable observations from unpol-
luted systems. The concentrations were lowest in
muscle, and the observed metal levels did not
exceed established quality standards for fish flesh.
The metal levels were usually several times higher
in the liver, which is known to be an important
detoxification centre in fish (McFarlane and
Franzin, 1980). Nickel and cadmium exhibited
significant increases in tissue concentrations with
decreasing distances from the smelters, and had
particularly high levels in Kuetsjarvi. Nickel may
be harmful to the survival and productivity of
freshwater fauna (Moore and Ramamoorthy,
19841, but studies of effects of Ni accumulation in
fish are scarce (Sreedevi et al., 1992). Cadmium is
a persistent material that may be toxic to aquatic
organisms at relatively low concentrations, but
222 P.-A. Amudsen et al. /The
Taylor (1983) considered the bioconcentration of
Cd in aquatic vertebrates to be so low that it was
likely of little significance. Dallinger et al. (19871,
on the other hand, pointed out that most heavy
metals are effective at very low concentrations, so
even low assimilation rates may be sufficient to
attain biologically significant or even harmful
concentrations in tissue. There are some indica-
tions that the fish populations in Kuetsjarvi may
suffer pollution stress from heavy metal accumu-
lations, since pathological anomalies such as
nephrocalcitosis and liver cirrhosis have been
shown frequently to occur (Langeland, 1993; Moi-
seenko et al., 1995; Lukin and Kashulin, unpub-
lished). There is also some evidence for recruit-
ment failure of the perch and pike populations in
the lake (unpublished data). Unfortunately, how-
ever, there is little empirical evidence about bio-
logically harmful concentrations of heavy metals
in fish, and it is, therefore, difficult to evaluate
the possible ecological effects of the metal levels
recorded in the present study. Adams et al. (1989)
advocated the use of bioindicators for assessing
the effects of pollutant stress in fish. For future
research it may be fruitful to integrate studies of
heavy metal concentrations in fish tissue with
investigations of bioindicators like fish pathology
and histology, as well as extensive ecological
surveillance both at the population and commu-
nity level.
Acknowledgements
Thanks are due to Syverin Lierhagen, The Nor-
wegian Institute for Nature Research, for help
with the heavy metal analyses, to Laina Dalsbpr,
Jan Evjen and Elleke Wartena, The Norwegian
College of Fishery Science, for assistance in field
and laboratory, and to Armand Kuris, University
of California, Santa Barbara, for correcting the
English. The study was part of a research pro-
gramme carried out under the Norwegian-Rus-
sian Environmental Protection Commission, and
had financial support from The Norwegian Min-
istry of Environment Protection and The Direc-
torate for Nature Management.
Science of the Total Enuironment 201 (1997) 211-224
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