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Mercury in Arctic char (Salvelinus alpinus) populations from Greenland
The Science of the Total Environment 245 Ž2000. 161᎐172
Mercury in Arctic char ž Sal¨elinus alpinus/ populations from Greenland F. RigetU , G. Asmund, P. Aastrup Ministry of En¨ ironment and Energy, National En¨ ironmental Research Institute, Department of Arctic En¨ ironment, Tagens¨ ej 135, 4 floor, DK-2200 Copenhagen N, Denmark Received 8 July 1999; accepted 11 July 1999
Abstract Mercury concentrations were determined in muscle tissue of lake resident and anadromous populations of Arctic char in Greenland. Mercury in lake sediment, and in soil and humus from the surrounding area were also determined in the main localities. Fish length and dry weight were shown to be important covariables, which have to be taken into account when comparing mercury levels between populations. Variations in fat content did not contribute further to the differing mercury concentrations. Mercury concentrations in lake sediments, humus from around the lakes and resident populations of Arctic char from west Greenland and south-west Greenland were higher than for populations from east Greenland and north-west Greenland. The mercury level in anadromous populations was found to be 10᎐15-fold lower than that found in lake resident populations, and similar to that found in marine fish species. Methyl mercury was determined in two of the populations investigated, and constituted 72᎐92% of the total mercury. 䊚 2000 Elsevier Science B.V. All rights reserved. Keywords: Sal¨ elinus alpinus; Methylmercury; Anadromous; Lake resident; Lake sediment; Soil; Humus
1. Introduction Mercury in Greenland ecosystems may be derived from both natural and anthropogenic sources, and the relative contributions are difficult to ascertain. In Arctic areas such as Green-
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Corresponding author.
land, natural sources due to erosion of soil and rocks may represent an important source of mercury. This has been observed in an indirect way by the temporally increased mercury levels in freshwater fish in new impoundments ŽCox et al., 1979.. The anthropogenic input is believed to be derived from atmospheric deposition of mercury transported from distant sources as industrial activities in Greenland are very limited. Atmo-
0048-9697r00r$ - see front matter 䊚 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 9 9 . 0 0 4 4 1 - 6
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F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
spheric transport of mercury to the Arctic areas may be an increasing problem due to the increased global energy consumption involving burning of coal and fossil fuels ŽNriagu and Pacyna, 1988., and mercury concentrations in the Northern Hemisphere have been reported to be increasing ŽFritzgerald, 1995.. Both natural and anthropogenic inputs can vary geographically, and observing these trends may aid the understanding of their relative importance. Once absorbed into the freshwater system, inorganic mercury passes from solution or suspension into the sediments. Microorganisms can transform inorganic mercury to organic mercury, which in turn can accumulate in animals, and biomagnifies in the food web. Mercury concentration in muscle of freshwater fish species increases
with size of the fish ŽScott and Armstrong, 1972; Akielaszek and Haines, 1981; Skurdal et al., 1985; Somers and Jackson, 1993.. It is therefore, necessary to adjust for size when comparing mercury concentrations in fish samples from different populations. Nothing is known about mercury in the freshwater system of Greenland, although bioaccumulation of mercury has been clearly demonstrated in the Greenland marine ecosystem ŽDietz et al., 1996., and Arctic char may be expected to have high concentrations of mercury as a top predator in Greenland lakes. Furthermore, elevated levels of mercury have been reported for freshwater fish in other Arctic areas ŽMuir et al., 1996.. Beside being a suitable species as a freshwater top predator for monitoring purposes such as
Fig. 1. Map showing the AMAP Greenland sampling areas.
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
geographical and time trends, Arctic char is also of some importance in relation to human consumption. In relation to human health, the concentrations of organic mercury are more relevant as it is more toxic than inorganic mercury. The aim of this study is to determine the mercury level in Arctic char Ž Sal¨ elinus alpinus. from lakes in Greenland, to detect possible geographical trends, to gain insight into the controlling factors for mercury in Arctic char, and to determine the most important covariable. Furthermore, this study is the first ‘point’ in a time trend study of mercury concentrations in Arctic char in
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Greenland. As an aid to explaining geographical variations in mercury concentrations in Arctic char, mercury has also been determined in lake sediments, and in soil and humus from the areas surrounding the lakes. Arctic char occur both as lake residents living their whole life in freshwater, and in an anadromous form migrating into marine waters during summer for eating. In one of the selected areas, mercury is determined in some anadromous populations in order to compare the mercury concentrations in the two forms. The fraction of organic mercury has been determined in one anadromous and one lake resident popula-
Fig. 2. Detailed map of the Qaqortoq area where sampling of Arctic char has been done.
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
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tion to establish the occurrence of these highly toxic compounds in relation to human health.
2. Materials and methods Four areas were selected to represent different parts of Greenland: Avanersuaq, north-west Greenland; Nuuk, west Greenland; Qaqortoq, south-west Greenland and Tasiilaq, east Greenland ŽFig. 1.. A small lake or a river without access from the sea inhabited by a resident Arctic char Ž Sal¨ elinus alpinus. population was selected from each of these areas. In Qaqortoq, additional sampling of Arctic char were taken from three other lake resident populations and from three anadromous populations in order to make comparisons between resident populations on a small geographically scale, and to compare mercury concentrations between lake resident and anadromous populations from the same area ŽFig. 2.. All lakes were situated close to the coastline, and at altitudes from near sea level to approximately 100 m above sea level. ŽTable 1.. The estimated surface area of lakes range between 0.5 km2 for Lake C and 1.25 km2 for the lake in Avanersuaq. pH and conductivity were measured using a portable pH meter with a glass electrode, and a portable conductivity meter with a platinum
conductivity cell, respectively. Surface and drainage areas were estimated from maps. The relatively low transparency of the lakes from Avanersuaq and the river from Tasiilaq was due to inflow of silt from glaciers of the inland ice. Sampling was carried out in autumn 1994 and autumn 1995. The fish were caught either in nets or by angling. Nets were emptied within 24 h. The length and weight of the fish were noted, and otoliths were taken for age determination. Muscle tissue from the axial part of the fish were sampled and stored frozen in polyethylene bags. Muscle tissues were lightly thawed before chemical analysis. The surface tissue was cut away to minimise potential contamination and to avoid the inclusion of dehydrated tissue. Special care was taken to avoid dehydrated tissue when cutting out the separate 2-g sample used for determination of dry weight by weighing before and after drying for 24 h at 105⬚C. Stainless steel scalpels, polyethylene gloves and polyethylene cutting boards were used. Lake sediment samples were taken from lakes in Avanersuaq, Nuuk, Tasiilaq and in Lake A in Qaqortoq using an Ekman bottom sampler deployed from a rubber boat. Only the upper portion Žapprox. 10 cm. of the sediment core was sampled. At each location, a composite sample was made up from four bottom samples taken at
Table 1 Localities and some physical charateristics of the study lakes and rivers Lakerriver
pH
Conductivity ŽSrcm.
Estimated surface Žarearkm2 .
Estimated drainage Žarea km2 .
Estimated water discharge Žm3 rs.
Altitude Žm.
Visibility Žm.
Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake
6.6 7.6 6.7 6.7
45 70 34 34
1.25 0.5᎐1 ᎐ 4᎐5
33 2.2 ᎐ 25᎐30
᎐ ᎐ 5᎐10 ᎐
100 50 ᎐ 168
2᎐3 8᎐9 ᎐ 4᎐5
Qaqortoq, Lake A, Lake B Lake C Lake D River I River II River III
6.2 5.8 7.2 5.9 5.8 6.3 6.1
18 18 19 14 12 11 11
0.5 0.8 0.1 1 ᎐ ᎐ ᎐
3.5 ? ? ? ᎐ ᎐ ᎐
᎐ ᎐ ᎐ ᎐ 2᎐4 15 5᎐10
25 10 20 100 ᎐ ᎐ ᎐
) 10 ) 10 ) 10 ) 10 ᎐ ᎐ ᎐
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
different sites in the deepest part of the lake. In all the lakes the sediment consisted of fine mud. Cubic soil samples Ž15 cm = 15 cm = 15 cm. were taken from the ground surface in the vicinity of the lakes in Avanersuaq, Nuuk, Tasiilaq and in Lake A in Qaqortoq. The plant cover was removed and the remaining material was divided. The upper layer, with a high content of organic material made up the humus sample, and the lower layer, consisting of mineral soil, the soil sample. Five samples were taken from each location except in Nuuk where only four and three soil and humus samples, respectively, were obtained. No lake sediment, soil and humus samples were taken in the additional lakes in the Qaqortoq area as the geology and environmental conditions were assumed to be very similar. During shipment from Greenland to Copenhagen all samples were stored at y20 o C. Total mercury was determined by cold flameless AAS after decomposition with nitric acid in teflon bombs. All mercury and dry weight analyses were run under an analytical quality protocol, involving the analysis of procedural blanks, and certified reference materials within each sample batch, intended to establish the performance of the methods under routine operation. Full details of the methods used and quality procedures used are given in Asmund and Cleemann, 2000, this issue. Organic mercury in fish from one anadromous and one resident population both in Qaqortoq was determined by extraction of blended fish muscle with toluene after addition of copper sulphate and sodium bromide, followed by back extraction with thiosulphate and then determination by cold flameless AAS. Organic mercury in fish is known to be primarily methylmercury. The quality of these analyses were controlled by analysing the Tort 1 and Tort 2 certified reference materials from the National Research Council of Canada. Also a laboratory intercomparison organised by IAEA showed good agreement between our method and those of other laboratories. Total lipids were determined in the resident char populations in lakes in Avanersuaq, Nuuk,
165
Tasiilaq and in Lake A in Qaqortoq by a modification of the method described by Bligh and Dyer Ž1959.. The amount of sample was scaled down from 100 g to approximately 1.5 g. Instead of homogenising with chloroform and methanol, the sample is homogenised prior to the addition of solvents. The sample is shaken with solvents in a closed system. In the statistical analyses, values below the detection limits have been treated as the reported values from the laboratory. The statistical analyses were performed with the SAS statistical software package ŽSAS Institute Inc., 1989.. Generally, Hg concentrations in fish did not differ from a normal distribution at the 5% significance level after logarithmic transformation Žbase e.. Correlation analysis was performed using Pearson’s correlation coefficient. The geographical variation in log e-Hg concentrations in soil and humus samples were examined by a one-way analysis of variance ŽANOVA. using the General Linear Model ŽGLM. procedure, and the significance of differences between localities was compared using the Tukey᎐Kramer multiple comparison option. The geographical variation in log e-Hg concentrations in Arctic char was tested by an analysis of covariance ŽANCOVA., with population as the classification factor, and fish length and dry weight percentage as covariables. The effect of the length covariable is allowed to differ among populations Žinteraction effect., whereas the effect of the dry weight covariable is assumed to be the same for all populations. If a first run of the ANCOVA show insignificant effects, these were removed and the ANCOVA was run again. Comparisons of log e-Hg levels between populations were done by pairwise testing for differences between the least square mean ŽLSMEAN. levels from the GLM analysis. LSMEAN are the estimated population means, with all covariates at their mean value.
3. Results Mercury concentrations in lake sediments, soil and humus from the four localities are shown in Table 2. The highest mercury level in lake sediments was found in the sediment samples from
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Table 2 Mercury concentrations in lake sediment, soil and humus Žgrg dry wt.. a Avanersuaq
Soil Humus Lake sediment L.o.I. a
N
GM
5 5 1
0.01 0.0367 0.023 3.7%
Nuuk
Qaqortoq
Tasiilaq
R.S.E.
N
GM
R.S.E.
N
GM
R.S.E.
N
GM
R.S.E.
᎐ 1.10 ᎐
4 3 1
0.02 0.117 0.052 12.9%
1.28 1.23 ᎐
5 5 1
0.03 0.0751 0.025 4.5%
1.14 1.28 ᎐
5 5 1
- 0.01 0.0199 0.018 1.4%
᎐ 1.13 ᎐
GM, geometric mean; R.S.E., relative standard error; N, number of samples; - value below detection limit.
the lake in Nuuk, where the level was a factor of 2 higher than in the lakes from Avanersuaq and Qaqortoq, and approximately a factor of 3 higher than in Tasiilaq. The sediment of the lake in Nuuk showed a considerably higher loss on ignition, than the sediments from other locations, indicating a higher content of organic matter in that lake. Mercury concentrations in soil from the surroundings of the lakes were below or just above the detection limit in all locations, indicating only small differences between localities. Mercury concentrations in humus from the surroundings of the lakes in Nuuk and Qaqortoq were found to be significantly higher than in humus lakes in Avan-
ersuaq and Tasiilaq Žone-way ANOVA, followed by Tukey᎐Kramer multiple test, P - 0.001.. Table 3 shows biological data from the Arctic char populations sampled. Mean lengths of the sampled fish differ significantly ŽANOVA, P0.001., ranging from a mean length of 23.5 cm for the river resident fish from Tasiilaq, to a mean length of 47.8 cm for the lake resident fish from the same area. The size variation was generally smaller in the samples of anadromous populations than in samples of resident populations. The mean age of the resident populations ranged from 10.6 years in Lake B in Qaqortoq, to 18.8 years in Tasiilaq. The anadromous char were generally younger than the resident char, with all
Table 3 Location, sample size, and univariate statistics for Arctic char populationsa Lakerriver
Fish length Žcm.
Fish age
Dry wt. Ž%.
Fat content Žgrkg.
Mean
S.D.
Mean
S.D.
29.4 25.3 24.6 49.0 16.2a
18.9 17.1 17.3 19.3 9.9
N
Mean
S.D.
Min
Max.
Mean
Min.
Max.
26 21 21 4 50 22 25 22
41.2 36.6 23.5 47.8 39.2 34.7 35.0 33.5
5.61 3.89 3.52 2.75 8.29 7.08 3.14 3.59
26 29 19 45 14.5 18 25.5 28.5
57 45 29 51 63 46.5 40 40.5
13.6 10.8 11.0 18.8 11.8 10.6 11.8 10.8
8 10 6 16 6 7 9 8
20 13 15 22 17 13 15 13
20.3 21.6 18.5 20.7 20.5 21.2 21.8 20.3
1.9 2.4 2.0 0.6 0.6 2.0 1.7 2.1
Anadromous populations River I 22 River II 25 River III 25
38.9 35.9 39.5
5.80 3.70 5.71
22 30 27
49.5 43 48
6.1 6.2 6.7
5 5 5
8 8 8
25.6 24.0 24.6
1.4 1.5 1.5
Resident populations Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake Qaqortoq, Lake A, Lake B Lake C Lake D
a
N s 25.
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
anadromous fish ranging from 5 to 8 years of age. The mean age ranged from 6.1 to 6.7 years. Fish length was found to be a better explanatory variable of the mercury concentrations than age, as the correlation coefficients between log-transformed mercury concentrations and length, in general, were higher than for correlations with age ŽTable 4.. Therefore, the mercury concentrations in the present paper are related to fish length. Fish length, dry weight, and fat content are possible covariables that may have an influence on mercury concentrations in muscle of Arctic char ŽFig. 3.. The correlation between these covariables showed a significant correlation between dry weight and fat content Ž P- 0.05., whereas there was no significant correlations found between either dry weight and fish length Ž Ps 0.96. or between fat content and fish length Ž Ps 0.27.. Table 4 shows the correlation coefficients between log e-Hg and length, dry weight and fat content. Log e-Hg is generally positively correlated with fish length and negatively correlated with dry weight and fat content. Because of the significant correlation between dry weight and fat content, the correlation between log e-Hg and dry
167
weight holding constant value of fat content, and the correlation between log e-Hg and fat content holding constant value of dry weight, have been calculated ŽTable 4.. The correlation between log e-Hg and dry weight was still clear, and in some cases even stronger; the correlation with fat content was weaker and significant only in one population. Based on these considerations, fish length and dry weight were determined to be the most important covariables. 3.1. Resident populations For the resident populations, the relationship between log e-Hg concentrations and length was significant Ž P- 0.001., however, this relationship did not differ significantly between populations ŽANCOVA, Ps 0.27.. An estimated common slope showed a doubling of Hg concentration with a 12-cm increase in length. The dry weight percent also had a highly significant influence Ž Ps 0.001.; the Hg concentration was halved with an increase in the dry weight of 7%. Table 5 shows the mercury concentrations normalised to a fish length of 34.8 cm and dry weight of 20% Žmean of all resident fish.. This may be a theoretical con-
Table 4 Pearson’s correlation coefficients between logarithmic transformed mercury concentration wlog e ŽHg.x and length of fish Žlgh., age of fish Žage., fat content Žfat. and tissue dry weight Ždry wt.. together with partial correlation coefficients N
lghr loge ŽHg.
Resident populations Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake Qaqortoq, Lake A Lake B Lake C Lake D
26 21 21 4 50a 22 25 22
0.63b 0.40 0.50b 0.76 0.85b 0.78b 0.54b 0.74b
0.48b 0.16 0.40 y0.23 0.52b 0.78b 0.33 0.20
Anadromous populations River I River II River III
22 25 25
0.05 0.59b 0.38
0.40 0.32 0.58b
a b
Ager loge ŽHg.
N s 25 when fat is one of variables in the correlation. Denotes P- 0.05.
Dry wt.r loge ŽHg.
Fatr loge ŽHg.
Dry wt.r loge ŽHg. partial fat
Fatr loge ŽHg. partial dry wt.
y0.71b y0.72b y0.55b y0.10 y0.60b y0.38 y0.30 y0.44b
y0.40b y0.55b y0.66b y0.87 y0.65b
y0.72b y0.75b 0.61b y0.34 y0.74b
y0.10 y0.27 y0.50b y0.88 y0.19
y0.36 y0.10 y0.13
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Fig. 3. Plots of mercury concentrations vs. fish length, dry wt. Ž%. and fat content Žgrkg. for resident Arctic char populations in Avanersuaq Ž`., Nuuk Ž=., Qaqortoq Žq. and Tasiilaq Ž ⌬ ..
centration in the river resident fish from Tasiilaq, where fish of that size were not sampled. The mercury levels in fish from the different lakes in the Qaqortoq area and the lake in Nuuk were similar ŽTable 6.. However, significant differences Žat the 5% level. were found between Lake D and the two lakes A and B in Qaqortoq. In the Avanersuaq population the mean mercury level was significantly lower than in all other populations, except the lake resident population in Tasiilaq. The lake and river populations from Tasiilaq have mercury levels in-between the Avanersuaq and the NuukrQaqortoq populations. The relative standard error for the lake population from Tasiilaq is high due to the low number of samples taken.
3.2. Anadromous populations For the anadromous populations, the relationship between size and log e-Hg concentrations was weaker than for the lake resident populations. The statistical analyses showed that regression slopes did not differ significantly among populations ŽANCOVA, Ps 0.07., and that the relationship was significant Ž Ps 0.007.. An estimated common slope showed a doubling of Hg concentration with a 40-cm increase in length. The influence of the dry weight percent on mercury concentration was not found to be significant Ž Ps 0.17.. Mercury concentrations normalised to a fish length of 38.1 cm Žmean of all anadromous fish. are shown in Table 5.
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Table 5 Arithmetic mean ŽAM., standard error ŽS.E.., minimum ŽMin.., maximum ŽMax.., geometric mean ŽGM. and relative standard error ŽR.S.E. of mercury concentrations in Arctic char populationsa N
AM
S.E.
Min
Max
GM
R.S.E.
Resident populations Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake Qaqortoq, Lake A Lake B Lake C Lake D
26 21 21 4 50 22 25 22
0.231 0.696 0.120 0.400 0.801 0.566 0.642 0.624
0.135 0.266 0.036 0.069 0.605 0.340 0.296 0.346
0.038 0.316 0.048 0.314 0.069 0.145 0.214 0.234
0.495 1.30 0.187 0.479 3.73 1.71 1.32 2.01
0.133 0.620 0.260 0.180 0.529 0.527 0.616 0.666
1.08 1.09 1.11 1.22 1.06 1.09 1.08 1.09
Anadromous populations River I River II River III
22 25 25
0.050 0.040 0.045
0.012 0.012 0.014
0.033 0.023 0.025
0.071 0.080 0.071
0.0478 0.0398 0.0423
1.06 1.06 1.05
Methyl Hgrtotal Hg "S.E.
0.915" 0.021
0.723" 0.020
a
The geometric mean concentrations are adjusted to a fish size of 34.8 cm and dry weight percent of 20. Anadromous populations are adjusted to a fish size of 38.1 cm
The mercury levels in the three anadromous populations from the Qaqortoq area are similar, although fish from River I have significantly higher mean concentrations of mercury than fish from River II at the 5% level ŽTable 6.. The mercury levels found in anadromous populations are a factor of 10᎐15 lower than in lake resident populations from the same area.
population and the anadromous population in River III, both in Qaqortoq area. The fraction of organic mercury, which ranged from 72% in the anadromous fish to 91% in the lake resident fish, differed significantly between the two populations Ž t-test; P- 0.001..
4. Discussion 3.3. Methylmercury In order to make geographical comparisons of mercury concentrations in muscle tissue of Arctic
Methylmercury was determined in the Lake B
Table 6 Results of pairwise test for difference in Hg levels between locations Resident populations Avanersuaq Tasiilaq, river Tasiilaq, lake Nuuk Lake A Lake B Lake C Anadromous populations River I River II U
Tasiilaq river
Tasiilaq lake
Nuuk
Lake A
Lake B
Lake C
Lake D
UU
᎐ ᎐
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
᎐
᎐ ᎐
᎐ ᎐ ᎐
River I
Denotes P- 0.05. Denotes P- 0.01 and ᎐ denotes P) 0.05.
UU
River II
U
River III ᎐ ᎐
᎐
U U
᎐
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char, it is necessary to allow for the correlated influence of other variables. Fish length, dry weight and fat content have in the present study been considered as possible covariables having influence on the mercury concentrations. It has been a normal procedure to adjust mercury concentrations for fish length ŽSomers and Jackson, 1993. and in case of lipophilic contaminants for fat content ŽHebert and Keenleyside, 1995.. Also, in studies of contaminants in tissue with highly variable fat content, such as cod liver, data have been normalised to fat content ŽNicholson et al., 1991; Grimas ˚ et al., 1995.. However, little or no attention has been given to the influence of dry weight of the tissue as a covariable. Fish length was chosen as a covariable instead of age, because the strongest correlations with mercury concentrations were obtained with fish length. This may be because assigning ages may be more problematic in older fish, or because the trophic level of individual fish is related more to their size than their age. Arctic char occur in different ecological forms Žsee later. with different growth rates, and so fish of the same length can be of very different age ŽSparholt, 1985; Riget et al., 1986.. The mercury concentrations in this study are negatively correlated with both dry weight and fat content of the muscle tissue Žno fat content determination had been made in anadromous fish.. When eliminating the influence of the variable with the strongest correlation, dry weight, the other, fat, becomes insignificant. It may not be surprising that fat content becomes insignificant, as methyl mercury, which constitutes approximately 90% of the total mercury Žsee later. in fish resides in protein rather than in fat tissue ŽBloom, 1992.. The correlation between mercury and dry weight cannot be a result of tissue dehydration prior to analysis, as that would yield a positive correlation. However, the reasons for the negative correlation between dry weight and mercury concentrations are unknown. One could argue that a fish with a low dry weight and therefore, low fat content, is a fish that is not thriving, which may be the reason for the high mercury concentration.
In lakes different ecological forms of resident Arctic char occur which may cause variability in the tissue mercury concentrations observed. It has been shown that position on the trophic scale is an important factor determining the degree of bioaccumulation of mercury ŽAkielaszek and Haines, 1981.. In general, the highest mercury concentrations are found in piscivorous fish species. In studies of lake trout, Sal¨ elinus namaycush ŽMacCrimmon et al., 1983., and brown trout, Salmo trutta ŽSkurdal et al., 1985., an increase in mercury accumulation was observed when trout changed their diet to fish. In Greenland lakes, three ecological forms of resident Arctic char have been found: a dwarf form feeding on benthos; a medium-sized pelagic form feeding on zooplankton; and a large cannibalistic form ŽSparholt, 1985; Riget et al., 1986.. The resident chars included in this study were all of a relatively large size, and may therefore all belong to the large-sized cannibalistic form. The only exception is the relatively small sized Arctic chars from the river resident population in Tasiilaq. Variability of mercury concentrations related to the occurrence of different resident forms of Arctic char may therefore be small. The mean mercury concentrations found in anadromous Arctic char were a factor of 10᎐15 lower than those found in lake resident char from the same area. Similar differences between the two forms have been documented in Arctic Canada ŽMuir et al., 1996.. The anadromous char migrates in spring to fjords or coastal areas for feeding, and when resident in lakes or rivers during winter time they probably do not eat. The mercury levels found in anadromous char were similar to those found in marine fish species in Greenland ŽRiget et al., 1997.. Mercury concentrations in humus from the surroundings of the lakes, in lake sediments, and in resident populations of Arctic char were found to be higher in west Greenland and south-west Greenland than from east Greenland and northwest Greenland. Mercury in the environment can originate from natural or anthropogenic sources. It is difficult to differentiate between these two sources, and this study adds a small piece of
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
information to the understanding of the importance of anthropogenic sources. The study areas are a long distance from anthropogenic sources of contamination. However, atmospheric concentrations of mercury have been increasing in the Northern Hemisphere, at least up until 1990 ŽFritzgerald, 1995.. There may therefore, be input of mercury which has been transported from sources remote from Greenland. Mason and Fitzgerald Ž1996. calculated the average wet deposition of mercury based on several references to the mercury concentration in rain, and average rainfall. They found that the mercury concentrations in rain north of 70⬚ are three times lower than south of 70⬚. This may be a partial explanation for the fact that the lowest level of mercury was found in the resident population in Avanersuaq, the most northern area. The accumulation of mercury in freshwater fish has been shown to be influenced by a variety of environmental factors. Only a few environmental parameters were determined in the present study, and so no detailed comments can be made. All the investigated lakes may be regarded as oligotrophic, however, the surroundings of the lakes in south-west and west Greenland are relatively vigorous with dwarf shrub heaths, whilst only fell fields with sparse vegetation surrounded the lakes in north-west Greenland and east Greenland. The bioproduction in the lakes from Avanersuaq and Tasiilaq is likely to be lower than in the other lakes because they both are influenced by water from glaciers, which decrease the transparency and probably also reduce primary productivity. In the case of Avanersuaq, reduced primary productivity may also be a consequence of the high latitude of the lake. This may be an indication of a relationship between productivity in the lakes and mercury concentrations in the Arctic char. The total mercury concentrations in lake resident Arctic char populations in Greenland ranged between 0.13 and 0.67 grg wet wt. This level seems to be in the same range as found in Arctic Canada Ž0.01᎐0.57. and somewhat higher than in Finnish Lapland Ž0.09᎐0.32., Iceland Ž0.02᎐0.03. Norway Ž0.03᎐0.25. Russia Ž0.01. and Sweden Ž0.10., figures given in grg wet wt. ŽNilsson, 1997..
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Mercury entering lakes can be transformed to bioavailable forms by microbial methylation, and can be bioaccumulated in the food chain. The average fraction of mercury present as methylmercury ranged from 72 to 92%, which is in the same order of magnitude as in freshwater fish in Canada ŽGrey et al., 1995 cited in Muir et al., 1996..
5. Conclusions Studies of mercury concentrations in muscle tissues in Arctic char belonging to seven different lake resident populations and three anadromous populations in Greenland showed a positive correlation with fish length and a negative correlation with dry weight. The fat content did not add further to the explanation of mercury concentrations. The length and dry weight-adjusted mean mercury concentrations in resident populations in the northernmost and the east coast localities were lower than in south-west and west Greenland. The explanation for this is not clear, but it could be the reported low concentration of mercury in rain at very high latitudes, or the general lower bioproductivity in the northern and eastern lakes. The mercury concentrations in lake resident populations were 10᎐15-fold higher than in anadromous populations, which were at the same level as found in marine fish species. Methyl mercury constitutes 72᎐92% of the total mercury.
Acknowledgements We gratefully acknowledge the financial funding by the Danish National Environmental Protection Agency. Lipid determinations were performed by Gudrun Beyer Paulsen, National Environmental Research Institute, Department of Environmental Chemistry. References Akielaszek JJ, Haines TA. Mercury in the muscle tissue of fish from three northern Maine Lakes. Bull Environ Contam Toxicol 1981;27:201᎐208.
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Asmund G, Cleemann M. Analytical methods, quality assurance and quality control used in the Greenland AMAP programme. Sci Total Environ 2000;245:203᎐219. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911᎐917. Bloom N. On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 1992;49: 1010᎐1017. Cox JA, Carnahan J, DiNunzio J, McCoy J, Meister J. Source of mercury in fish in new impoundments. Bull Environ Contam Toxicol 1979;23:779᎐783. Dietz R, Riget F, Johansen P. Lead, cadmium, mercury and selenium in Greenland marine animals. Sci Total Environ 1996;186:67᎐93. Fritzgerald WF. Is mercury increasing in the atmosphere? The need for an atmospheric network ŽAMNET.. Water, Air, Soil Pollut 1995;80:245᎐254. Grey BJ, Harbicht SM, Stephens GR. Mercury in fish from rivers and lakes in southwestern northwest territories. Yellowknife: Dept. of Indian and Northern Affairs Canada, 1995:61. Grimas A, Notter M, Olsson M, Reutergardh L. ˚ U, Gothberg ¨ ˚ Fat amount ᎏ a factor to consider in monitoring studies of heavy metals in cod liver. Ambio 1995;14:175᎐178. Hebert CE, Keenleyside KA. To normalize or not to normalize? Fat is the question. Environ Toxicol Chem 1995; 12:801᎐807. MacCrimmon HR, Christopher DW, Barra L. Mercury uptake by Lake Trout, Sal¨ elinus namaycush, relative to age, growth, and diet in Tadenac Lake with comparative data from other precambrian Shield Lakes. Can J Fish Aquat Sci 1983;40:114᎐120. Mason RP, Fitzgerald WF. Sources, sinks and biochemical cycling of mercury in the ocean. In: Baeyens W et al., editor. Global and regional mercury cycles: sources, fluxes and mass ballances. The Netherlands: Kluver Academic Publishers, 1996:249᎐272.
Muir D, Braune B, DeMarch B et al. Ecosystem uptake ands effects, chap 3. In: Jensen J, Adare K, Shearer R, editors. Canadian Arctic Contaminants Assessment Report. Ottawa: Indian and Northern Affairs Canada, 1996r1997. Nicholson MD, Green NW, Wilson SJ. Regression models for assessing trends in cadmium and PCBs in cod livers from the Oslofjord. Mar Pollut Bull 1991;22:77᎐81. Nilsson A. Arctic pollution issues: a state of the Arctic environment report. AMAP. Oslo: Arctic Monitoring and Assessment Programme, 1997:188. Nriagu JO, Pacyna JM. Quantitative assessment of worldwide contamination of air, water and soils with trace metals. Nature 1988;333:134᎐139. Riget F, Nygaard KN, Christensen B. Population structure, ecological segratation, and reproduction in a population of Arctic char Ž Sal¨ elinus alpinus. from Lake Tasersuaq, Greenland. Can J Fish Aquat Sci 1986;43:985᎐992. Riget F, Dietz R, Johansen P. Zinc, cadmium, mercury and selenium in Greenland fish. Medd Grønl Biosci 1997;48:29. SAS Institute Inc. SASrSTAT User’s Guide, version 6, 4th ed, vol. 2. Cary, NC: SAS Institute Inc, 1989:846. Scott DP, Armstrong FAJ. Mercury concentration in relation to size in several species of freshwater fishes from Manitoba and northwestern Ontario. Can J Fish Aquat Sci 1972;29:1685᎐1690. Skurdal JT, Qvenild OK, Skogheim . Mercury accumulation in five species of freshwater fish in Lake Tyrifjorden, southeast Norway, with emphasis on their suitability as test organisms. Environ Biol Fish 1985;14:233᎐238. Somers KM, Jackson DA. Adjusting mercury concentration for fish-size covariation: a multivariate alternative to bivariate regression. Can J Fish Aquat Sci 1993;50:2388᎐2396. Sparholt H. The population, survival, growth, reproduction and food of arctic charr, Sal¨ elinus alpinus, ŽL.., in four enexpoited lakes in Greenland. J Fish Biol 1985;26:313᎐330.
Mercury in Arctic char ž Sal¨elinus alpinus/ populations from Greenland F. RigetU , G. Asmund, P. Aastrup Ministry of En¨ ironment and Energy, National En¨ ironmental Research Institute, Department of Arctic En¨ ironment, Tagens¨ ej 135, 4 floor, DK-2200 Copenhagen N, Denmark Received 8 July 1999; accepted 11 July 1999
Abstract Mercury concentrations were determined in muscle tissue of lake resident and anadromous populations of Arctic char in Greenland. Mercury in lake sediment, and in soil and humus from the surrounding area were also determined in the main localities. Fish length and dry weight were shown to be important covariables, which have to be taken into account when comparing mercury levels between populations. Variations in fat content did not contribute further to the differing mercury concentrations. Mercury concentrations in lake sediments, humus from around the lakes and resident populations of Arctic char from west Greenland and south-west Greenland were higher than for populations from east Greenland and north-west Greenland. The mercury level in anadromous populations was found to be 10᎐15-fold lower than that found in lake resident populations, and similar to that found in marine fish species. Methyl mercury was determined in two of the populations investigated, and constituted 72᎐92% of the total mercury. 䊚 2000 Elsevier Science B.V. All rights reserved. Keywords: Sal¨ elinus alpinus; Methylmercury; Anadromous; Lake resident; Lake sediment; Soil; Humus
1. Introduction Mercury in Greenland ecosystems may be derived from both natural and anthropogenic sources, and the relative contributions are difficult to ascertain. In Arctic areas such as Green-
U
Corresponding author.
land, natural sources due to erosion of soil and rocks may represent an important source of mercury. This has been observed in an indirect way by the temporally increased mercury levels in freshwater fish in new impoundments ŽCox et al., 1979.. The anthropogenic input is believed to be derived from atmospheric deposition of mercury transported from distant sources as industrial activities in Greenland are very limited. Atmo-
0048-9697r00r$ - see front matter 䊚 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 9 9 . 0 0 4 4 1 - 6
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spheric transport of mercury to the Arctic areas may be an increasing problem due to the increased global energy consumption involving burning of coal and fossil fuels ŽNriagu and Pacyna, 1988., and mercury concentrations in the Northern Hemisphere have been reported to be increasing ŽFritzgerald, 1995.. Both natural and anthropogenic inputs can vary geographically, and observing these trends may aid the understanding of their relative importance. Once absorbed into the freshwater system, inorganic mercury passes from solution or suspension into the sediments. Microorganisms can transform inorganic mercury to organic mercury, which in turn can accumulate in animals, and biomagnifies in the food web. Mercury concentration in muscle of freshwater fish species increases
with size of the fish ŽScott and Armstrong, 1972; Akielaszek and Haines, 1981; Skurdal et al., 1985; Somers and Jackson, 1993.. It is therefore, necessary to adjust for size when comparing mercury concentrations in fish samples from different populations. Nothing is known about mercury in the freshwater system of Greenland, although bioaccumulation of mercury has been clearly demonstrated in the Greenland marine ecosystem ŽDietz et al., 1996., and Arctic char may be expected to have high concentrations of mercury as a top predator in Greenland lakes. Furthermore, elevated levels of mercury have been reported for freshwater fish in other Arctic areas ŽMuir et al., 1996.. Beside being a suitable species as a freshwater top predator for monitoring purposes such as
Fig. 1. Map showing the AMAP Greenland sampling areas.
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
geographical and time trends, Arctic char is also of some importance in relation to human consumption. In relation to human health, the concentrations of organic mercury are more relevant as it is more toxic than inorganic mercury. The aim of this study is to determine the mercury level in Arctic char Ž Sal¨ elinus alpinus. from lakes in Greenland, to detect possible geographical trends, to gain insight into the controlling factors for mercury in Arctic char, and to determine the most important covariable. Furthermore, this study is the first ‘point’ in a time trend study of mercury concentrations in Arctic char in
163
Greenland. As an aid to explaining geographical variations in mercury concentrations in Arctic char, mercury has also been determined in lake sediments, and in soil and humus from the areas surrounding the lakes. Arctic char occur both as lake residents living their whole life in freshwater, and in an anadromous form migrating into marine waters during summer for eating. In one of the selected areas, mercury is determined in some anadromous populations in order to compare the mercury concentrations in the two forms. The fraction of organic mercury has been determined in one anadromous and one lake resident popula-
Fig. 2. Detailed map of the Qaqortoq area where sampling of Arctic char has been done.
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
164
tion to establish the occurrence of these highly toxic compounds in relation to human health.
2. Materials and methods Four areas were selected to represent different parts of Greenland: Avanersuaq, north-west Greenland; Nuuk, west Greenland; Qaqortoq, south-west Greenland and Tasiilaq, east Greenland ŽFig. 1.. A small lake or a river without access from the sea inhabited by a resident Arctic char Ž Sal¨ elinus alpinus. population was selected from each of these areas. In Qaqortoq, additional sampling of Arctic char were taken from three other lake resident populations and from three anadromous populations in order to make comparisons between resident populations on a small geographically scale, and to compare mercury concentrations between lake resident and anadromous populations from the same area ŽFig. 2.. All lakes were situated close to the coastline, and at altitudes from near sea level to approximately 100 m above sea level. ŽTable 1.. The estimated surface area of lakes range between 0.5 km2 for Lake C and 1.25 km2 for the lake in Avanersuaq. pH and conductivity were measured using a portable pH meter with a glass electrode, and a portable conductivity meter with a platinum
conductivity cell, respectively. Surface and drainage areas were estimated from maps. The relatively low transparency of the lakes from Avanersuaq and the river from Tasiilaq was due to inflow of silt from glaciers of the inland ice. Sampling was carried out in autumn 1994 and autumn 1995. The fish were caught either in nets or by angling. Nets were emptied within 24 h. The length and weight of the fish were noted, and otoliths were taken for age determination. Muscle tissue from the axial part of the fish were sampled and stored frozen in polyethylene bags. Muscle tissues were lightly thawed before chemical analysis. The surface tissue was cut away to minimise potential contamination and to avoid the inclusion of dehydrated tissue. Special care was taken to avoid dehydrated tissue when cutting out the separate 2-g sample used for determination of dry weight by weighing before and after drying for 24 h at 105⬚C. Stainless steel scalpels, polyethylene gloves and polyethylene cutting boards were used. Lake sediment samples were taken from lakes in Avanersuaq, Nuuk, Tasiilaq and in Lake A in Qaqortoq using an Ekman bottom sampler deployed from a rubber boat. Only the upper portion Žapprox. 10 cm. of the sediment core was sampled. At each location, a composite sample was made up from four bottom samples taken at
Table 1 Localities and some physical charateristics of the study lakes and rivers Lakerriver
pH
Conductivity ŽSrcm.
Estimated surface Žarearkm2 .
Estimated drainage Žarea km2 .
Estimated water discharge Žm3 rs.
Altitude Žm.
Visibility Žm.
Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake
6.6 7.6 6.7 6.7
45 70 34 34
1.25 0.5᎐1 ᎐ 4᎐5
33 2.2 ᎐ 25᎐30
᎐ ᎐ 5᎐10 ᎐
100 50 ᎐ 168
2᎐3 8᎐9 ᎐ 4᎐5
Qaqortoq, Lake A, Lake B Lake C Lake D River I River II River III
6.2 5.8 7.2 5.9 5.8 6.3 6.1
18 18 19 14 12 11 11
0.5 0.8 0.1 1 ᎐ ᎐ ᎐
3.5 ? ? ? ᎐ ᎐ ᎐
᎐ ᎐ ᎐ ᎐ 2᎐4 15 5᎐10
25 10 20 100 ᎐ ᎐ ᎐
) 10 ) 10 ) 10 ) 10 ᎐ ᎐ ᎐
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
different sites in the deepest part of the lake. In all the lakes the sediment consisted of fine mud. Cubic soil samples Ž15 cm = 15 cm = 15 cm. were taken from the ground surface in the vicinity of the lakes in Avanersuaq, Nuuk, Tasiilaq and in Lake A in Qaqortoq. The plant cover was removed and the remaining material was divided. The upper layer, with a high content of organic material made up the humus sample, and the lower layer, consisting of mineral soil, the soil sample. Five samples were taken from each location except in Nuuk where only four and three soil and humus samples, respectively, were obtained. No lake sediment, soil and humus samples were taken in the additional lakes in the Qaqortoq area as the geology and environmental conditions were assumed to be very similar. During shipment from Greenland to Copenhagen all samples were stored at y20 o C. Total mercury was determined by cold flameless AAS after decomposition with nitric acid in teflon bombs. All mercury and dry weight analyses were run under an analytical quality protocol, involving the analysis of procedural blanks, and certified reference materials within each sample batch, intended to establish the performance of the methods under routine operation. Full details of the methods used and quality procedures used are given in Asmund and Cleemann, 2000, this issue. Organic mercury in fish from one anadromous and one resident population both in Qaqortoq was determined by extraction of blended fish muscle with toluene after addition of copper sulphate and sodium bromide, followed by back extraction with thiosulphate and then determination by cold flameless AAS. Organic mercury in fish is known to be primarily methylmercury. The quality of these analyses were controlled by analysing the Tort 1 and Tort 2 certified reference materials from the National Research Council of Canada. Also a laboratory intercomparison organised by IAEA showed good agreement between our method and those of other laboratories. Total lipids were determined in the resident char populations in lakes in Avanersuaq, Nuuk,
165
Tasiilaq and in Lake A in Qaqortoq by a modification of the method described by Bligh and Dyer Ž1959.. The amount of sample was scaled down from 100 g to approximately 1.5 g. Instead of homogenising with chloroform and methanol, the sample is homogenised prior to the addition of solvents. The sample is shaken with solvents in a closed system. In the statistical analyses, values below the detection limits have been treated as the reported values from the laboratory. The statistical analyses were performed with the SAS statistical software package ŽSAS Institute Inc., 1989.. Generally, Hg concentrations in fish did not differ from a normal distribution at the 5% significance level after logarithmic transformation Žbase e.. Correlation analysis was performed using Pearson’s correlation coefficient. The geographical variation in log e-Hg concentrations in soil and humus samples were examined by a one-way analysis of variance ŽANOVA. using the General Linear Model ŽGLM. procedure, and the significance of differences between localities was compared using the Tukey᎐Kramer multiple comparison option. The geographical variation in log e-Hg concentrations in Arctic char was tested by an analysis of covariance ŽANCOVA., with population as the classification factor, and fish length and dry weight percentage as covariables. The effect of the length covariable is allowed to differ among populations Žinteraction effect., whereas the effect of the dry weight covariable is assumed to be the same for all populations. If a first run of the ANCOVA show insignificant effects, these were removed and the ANCOVA was run again. Comparisons of log e-Hg levels between populations were done by pairwise testing for differences between the least square mean ŽLSMEAN. levels from the GLM analysis. LSMEAN are the estimated population means, with all covariates at their mean value.
3. Results Mercury concentrations in lake sediments, soil and humus from the four localities are shown in Table 2. The highest mercury level in lake sediments was found in the sediment samples from
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Table 2 Mercury concentrations in lake sediment, soil and humus Žgrg dry wt.. a Avanersuaq
Soil Humus Lake sediment L.o.I. a
N
GM
5 5 1
0.01 0.0367 0.023 3.7%
Nuuk
Qaqortoq
Tasiilaq
R.S.E.
N
GM
R.S.E.
N
GM
R.S.E.
N
GM
R.S.E.
᎐ 1.10 ᎐
4 3 1
0.02 0.117 0.052 12.9%
1.28 1.23 ᎐
5 5 1
0.03 0.0751 0.025 4.5%
1.14 1.28 ᎐
5 5 1
- 0.01 0.0199 0.018 1.4%
᎐ 1.13 ᎐
GM, geometric mean; R.S.E., relative standard error; N, number of samples; - value below detection limit.
the lake in Nuuk, where the level was a factor of 2 higher than in the lakes from Avanersuaq and Qaqortoq, and approximately a factor of 3 higher than in Tasiilaq. The sediment of the lake in Nuuk showed a considerably higher loss on ignition, than the sediments from other locations, indicating a higher content of organic matter in that lake. Mercury concentrations in soil from the surroundings of the lakes were below or just above the detection limit in all locations, indicating only small differences between localities. Mercury concentrations in humus from the surroundings of the lakes in Nuuk and Qaqortoq were found to be significantly higher than in humus lakes in Avan-
ersuaq and Tasiilaq Žone-way ANOVA, followed by Tukey᎐Kramer multiple test, P - 0.001.. Table 3 shows biological data from the Arctic char populations sampled. Mean lengths of the sampled fish differ significantly ŽANOVA, P0.001., ranging from a mean length of 23.5 cm for the river resident fish from Tasiilaq, to a mean length of 47.8 cm for the lake resident fish from the same area. The size variation was generally smaller in the samples of anadromous populations than in samples of resident populations. The mean age of the resident populations ranged from 10.6 years in Lake B in Qaqortoq, to 18.8 years in Tasiilaq. The anadromous char were generally younger than the resident char, with all
Table 3 Location, sample size, and univariate statistics for Arctic char populationsa Lakerriver
Fish length Žcm.
Fish age
Dry wt. Ž%.
Fat content Žgrkg.
Mean
S.D.
Mean
S.D.
29.4 25.3 24.6 49.0 16.2a
18.9 17.1 17.3 19.3 9.9
N
Mean
S.D.
Min
Max.
Mean
Min.
Max.
26 21 21 4 50 22 25 22
41.2 36.6 23.5 47.8 39.2 34.7 35.0 33.5
5.61 3.89 3.52 2.75 8.29 7.08 3.14 3.59
26 29 19 45 14.5 18 25.5 28.5
57 45 29 51 63 46.5 40 40.5
13.6 10.8 11.0 18.8 11.8 10.6 11.8 10.8
8 10 6 16 6 7 9 8
20 13 15 22 17 13 15 13
20.3 21.6 18.5 20.7 20.5 21.2 21.8 20.3
1.9 2.4 2.0 0.6 0.6 2.0 1.7 2.1
Anadromous populations River I 22 River II 25 River III 25
38.9 35.9 39.5
5.80 3.70 5.71
22 30 27
49.5 43 48
6.1 6.2 6.7
5 5 5
8 8 8
25.6 24.0 24.6
1.4 1.5 1.5
Resident populations Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake Qaqortoq, Lake A, Lake B Lake C Lake D
a
N s 25.
F. Riget et al. r The Science of the Total En¨ ironment 245 (2000) 161᎐172
anadromous fish ranging from 5 to 8 years of age. The mean age ranged from 6.1 to 6.7 years. Fish length was found to be a better explanatory variable of the mercury concentrations than age, as the correlation coefficients between log-transformed mercury concentrations and length, in general, were higher than for correlations with age ŽTable 4.. Therefore, the mercury concentrations in the present paper are related to fish length. Fish length, dry weight, and fat content are possible covariables that may have an influence on mercury concentrations in muscle of Arctic char ŽFig. 3.. The correlation between these covariables showed a significant correlation between dry weight and fat content Ž P- 0.05., whereas there was no significant correlations found between either dry weight and fish length Ž Ps 0.96. or between fat content and fish length Ž Ps 0.27.. Table 4 shows the correlation coefficients between log e-Hg and length, dry weight and fat content. Log e-Hg is generally positively correlated with fish length and negatively correlated with dry weight and fat content. Because of the significant correlation between dry weight and fat content, the correlation between log e-Hg and dry
167
weight holding constant value of fat content, and the correlation between log e-Hg and fat content holding constant value of dry weight, have been calculated ŽTable 4.. The correlation between log e-Hg and dry weight was still clear, and in some cases even stronger; the correlation with fat content was weaker and significant only in one population. Based on these considerations, fish length and dry weight were determined to be the most important covariables. 3.1. Resident populations For the resident populations, the relationship between log e-Hg concentrations and length was significant Ž P- 0.001., however, this relationship did not differ significantly between populations ŽANCOVA, Ps 0.27.. An estimated common slope showed a doubling of Hg concentration with a 12-cm increase in length. The dry weight percent also had a highly significant influence Ž Ps 0.001.; the Hg concentration was halved with an increase in the dry weight of 7%. Table 5 shows the mercury concentrations normalised to a fish length of 34.8 cm and dry weight of 20% Žmean of all resident fish.. This may be a theoretical con-
Table 4 Pearson’s correlation coefficients between logarithmic transformed mercury concentration wlog e ŽHg.x and length of fish Žlgh., age of fish Žage., fat content Žfat. and tissue dry weight Ždry wt.. together with partial correlation coefficients N
lghr loge ŽHg.
Resident populations Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake Qaqortoq, Lake A Lake B Lake C Lake D
26 21 21 4 50a 22 25 22
0.63b 0.40 0.50b 0.76 0.85b 0.78b 0.54b 0.74b
0.48b 0.16 0.40 y0.23 0.52b 0.78b 0.33 0.20
Anadromous populations River I River II River III
22 25 25
0.05 0.59b 0.38
0.40 0.32 0.58b
a b
Ager loge ŽHg.
N s 25 when fat is one of variables in the correlation. Denotes P- 0.05.
Dry wt.r loge ŽHg.
Fatr loge ŽHg.
Dry wt.r loge ŽHg. partial fat
Fatr loge ŽHg. partial dry wt.
y0.71b y0.72b y0.55b y0.10 y0.60b y0.38 y0.30 y0.44b
y0.40b y0.55b y0.66b y0.87 y0.65b
y0.72b y0.75b 0.61b y0.34 y0.74b
y0.10 y0.27 y0.50b y0.88 y0.19
y0.36 y0.10 y0.13
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Fig. 3. Plots of mercury concentrations vs. fish length, dry wt. Ž%. and fat content Žgrkg. for resident Arctic char populations in Avanersuaq Ž`., Nuuk Ž=., Qaqortoq Žq. and Tasiilaq Ž ⌬ ..
centration in the river resident fish from Tasiilaq, where fish of that size were not sampled. The mercury levels in fish from the different lakes in the Qaqortoq area and the lake in Nuuk were similar ŽTable 6.. However, significant differences Žat the 5% level. were found between Lake D and the two lakes A and B in Qaqortoq. In the Avanersuaq population the mean mercury level was significantly lower than in all other populations, except the lake resident population in Tasiilaq. The lake and river populations from Tasiilaq have mercury levels in-between the Avanersuaq and the NuukrQaqortoq populations. The relative standard error for the lake population from Tasiilaq is high due to the low number of samples taken.
3.2. Anadromous populations For the anadromous populations, the relationship between size and log e-Hg concentrations was weaker than for the lake resident populations. The statistical analyses showed that regression slopes did not differ significantly among populations ŽANCOVA, Ps 0.07., and that the relationship was significant Ž Ps 0.007.. An estimated common slope showed a doubling of Hg concentration with a 40-cm increase in length. The influence of the dry weight percent on mercury concentration was not found to be significant Ž Ps 0.17.. Mercury concentrations normalised to a fish length of 38.1 cm Žmean of all anadromous fish. are shown in Table 5.
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169
Table 5 Arithmetic mean ŽAM., standard error ŽS.E.., minimum ŽMin.., maximum ŽMax.., geometric mean ŽGM. and relative standard error ŽR.S.E. of mercury concentrations in Arctic char populationsa N
AM
S.E.
Min
Max
GM
R.S.E.
Resident populations Avanersuaq Nuuk Tasiilaq, river Tasiilaq, lake Qaqortoq, Lake A Lake B Lake C Lake D
26 21 21 4 50 22 25 22
0.231 0.696 0.120 0.400 0.801 0.566 0.642 0.624
0.135 0.266 0.036 0.069 0.605 0.340 0.296 0.346
0.038 0.316 0.048 0.314 0.069 0.145 0.214 0.234
0.495 1.30 0.187 0.479 3.73 1.71 1.32 2.01
0.133 0.620 0.260 0.180 0.529 0.527 0.616 0.666
1.08 1.09 1.11 1.22 1.06 1.09 1.08 1.09
Anadromous populations River I River II River III
22 25 25
0.050 0.040 0.045
0.012 0.012 0.014
0.033 0.023 0.025
0.071 0.080 0.071
0.0478 0.0398 0.0423
1.06 1.06 1.05
Methyl Hgrtotal Hg "S.E.
0.915" 0.021
0.723" 0.020
a
The geometric mean concentrations are adjusted to a fish size of 34.8 cm and dry weight percent of 20. Anadromous populations are adjusted to a fish size of 38.1 cm
The mercury levels in the three anadromous populations from the Qaqortoq area are similar, although fish from River I have significantly higher mean concentrations of mercury than fish from River II at the 5% level ŽTable 6.. The mercury levels found in anadromous populations are a factor of 10᎐15 lower than in lake resident populations from the same area.
population and the anadromous population in River III, both in Qaqortoq area. The fraction of organic mercury, which ranged from 72% in the anadromous fish to 91% in the lake resident fish, differed significantly between the two populations Ž t-test; P- 0.001..
4. Discussion 3.3. Methylmercury In order to make geographical comparisons of mercury concentrations in muscle tissue of Arctic
Methylmercury was determined in the Lake B
Table 6 Results of pairwise test for difference in Hg levels between locations Resident populations Avanersuaq Tasiilaq, river Tasiilaq, lake Nuuk Lake A Lake B Lake C Anadromous populations River I River II U
Tasiilaq river
Tasiilaq lake
Nuuk
Lake A
Lake B
Lake C
Lake D
UU
᎐ ᎐
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
UU
᎐
᎐ ᎐
᎐ ᎐ ᎐
River I
Denotes P- 0.05. Denotes P- 0.01 and ᎐ denotes P) 0.05.
UU
River II
U
River III ᎐ ᎐
᎐
U U
᎐
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char, it is necessary to allow for the correlated influence of other variables. Fish length, dry weight and fat content have in the present study been considered as possible covariables having influence on the mercury concentrations. It has been a normal procedure to adjust mercury concentrations for fish length ŽSomers and Jackson, 1993. and in case of lipophilic contaminants for fat content ŽHebert and Keenleyside, 1995.. Also, in studies of contaminants in tissue with highly variable fat content, such as cod liver, data have been normalised to fat content ŽNicholson et al., 1991; Grimas ˚ et al., 1995.. However, little or no attention has been given to the influence of dry weight of the tissue as a covariable. Fish length was chosen as a covariable instead of age, because the strongest correlations with mercury concentrations were obtained with fish length. This may be because assigning ages may be more problematic in older fish, or because the trophic level of individual fish is related more to their size than their age. Arctic char occur in different ecological forms Žsee later. with different growth rates, and so fish of the same length can be of very different age ŽSparholt, 1985; Riget et al., 1986.. The mercury concentrations in this study are negatively correlated with both dry weight and fat content of the muscle tissue Žno fat content determination had been made in anadromous fish.. When eliminating the influence of the variable with the strongest correlation, dry weight, the other, fat, becomes insignificant. It may not be surprising that fat content becomes insignificant, as methyl mercury, which constitutes approximately 90% of the total mercury Žsee later. in fish resides in protein rather than in fat tissue ŽBloom, 1992.. The correlation between mercury and dry weight cannot be a result of tissue dehydration prior to analysis, as that would yield a positive correlation. However, the reasons for the negative correlation between dry weight and mercury concentrations are unknown. One could argue that a fish with a low dry weight and therefore, low fat content, is a fish that is not thriving, which may be the reason for the high mercury concentration.
In lakes different ecological forms of resident Arctic char occur which may cause variability in the tissue mercury concentrations observed. It has been shown that position on the trophic scale is an important factor determining the degree of bioaccumulation of mercury ŽAkielaszek and Haines, 1981.. In general, the highest mercury concentrations are found in piscivorous fish species. In studies of lake trout, Sal¨ elinus namaycush ŽMacCrimmon et al., 1983., and brown trout, Salmo trutta ŽSkurdal et al., 1985., an increase in mercury accumulation was observed when trout changed their diet to fish. In Greenland lakes, three ecological forms of resident Arctic char have been found: a dwarf form feeding on benthos; a medium-sized pelagic form feeding on zooplankton; and a large cannibalistic form ŽSparholt, 1985; Riget et al., 1986.. The resident chars included in this study were all of a relatively large size, and may therefore all belong to the large-sized cannibalistic form. The only exception is the relatively small sized Arctic chars from the river resident population in Tasiilaq. Variability of mercury concentrations related to the occurrence of different resident forms of Arctic char may therefore be small. The mean mercury concentrations found in anadromous Arctic char were a factor of 10᎐15 lower than those found in lake resident char from the same area. Similar differences between the two forms have been documented in Arctic Canada ŽMuir et al., 1996.. The anadromous char migrates in spring to fjords or coastal areas for feeding, and when resident in lakes or rivers during winter time they probably do not eat. The mercury levels found in anadromous char were similar to those found in marine fish species in Greenland ŽRiget et al., 1997.. Mercury concentrations in humus from the surroundings of the lakes, in lake sediments, and in resident populations of Arctic char were found to be higher in west Greenland and south-west Greenland than from east Greenland and northwest Greenland. Mercury in the environment can originate from natural or anthropogenic sources. It is difficult to differentiate between these two sources, and this study adds a small piece of
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information to the understanding of the importance of anthropogenic sources. The study areas are a long distance from anthropogenic sources of contamination. However, atmospheric concentrations of mercury have been increasing in the Northern Hemisphere, at least up until 1990 ŽFritzgerald, 1995.. There may therefore, be input of mercury which has been transported from sources remote from Greenland. Mason and Fitzgerald Ž1996. calculated the average wet deposition of mercury based on several references to the mercury concentration in rain, and average rainfall. They found that the mercury concentrations in rain north of 70⬚ are three times lower than south of 70⬚. This may be a partial explanation for the fact that the lowest level of mercury was found in the resident population in Avanersuaq, the most northern area. The accumulation of mercury in freshwater fish has been shown to be influenced by a variety of environmental factors. Only a few environmental parameters were determined in the present study, and so no detailed comments can be made. All the investigated lakes may be regarded as oligotrophic, however, the surroundings of the lakes in south-west and west Greenland are relatively vigorous with dwarf shrub heaths, whilst only fell fields with sparse vegetation surrounded the lakes in north-west Greenland and east Greenland. The bioproduction in the lakes from Avanersuaq and Tasiilaq is likely to be lower than in the other lakes because they both are influenced by water from glaciers, which decrease the transparency and probably also reduce primary productivity. In the case of Avanersuaq, reduced primary productivity may also be a consequence of the high latitude of the lake. This may be an indication of a relationship between productivity in the lakes and mercury concentrations in the Arctic char. The total mercury concentrations in lake resident Arctic char populations in Greenland ranged between 0.13 and 0.67 grg wet wt. This level seems to be in the same range as found in Arctic Canada Ž0.01᎐0.57. and somewhat higher than in Finnish Lapland Ž0.09᎐0.32., Iceland Ž0.02᎐0.03. Norway Ž0.03᎐0.25. Russia Ž0.01. and Sweden Ž0.10., figures given in grg wet wt. ŽNilsson, 1997..
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Mercury entering lakes can be transformed to bioavailable forms by microbial methylation, and can be bioaccumulated in the food chain. The average fraction of mercury present as methylmercury ranged from 72 to 92%, which is in the same order of magnitude as in freshwater fish in Canada ŽGrey et al., 1995 cited in Muir et al., 1996..
5. Conclusions Studies of mercury concentrations in muscle tissues in Arctic char belonging to seven different lake resident populations and three anadromous populations in Greenland showed a positive correlation with fish length and a negative correlation with dry weight. The fat content did not add further to the explanation of mercury concentrations. The length and dry weight-adjusted mean mercury concentrations in resident populations in the northernmost and the east coast localities were lower than in south-west and west Greenland. The explanation for this is not clear, but it could be the reported low concentration of mercury in rain at very high latitudes, or the general lower bioproductivity in the northern and eastern lakes. The mercury concentrations in lake resident populations were 10᎐15-fold higher than in anadromous populations, which were at the same level as found in marine fish species. Methyl mercury constitutes 72᎐92% of the total mercury.
Acknowledgements We gratefully acknowledge the financial funding by the Danish National Environmental Protection Agency. Lipid determinations were performed by Gudrun Beyer Paulsen, National Environmental Research Institute, Department of Environmental Chemistry. References Akielaszek JJ, Haines TA. Mercury in the muscle tissue of fish from three northern Maine Lakes. Bull Environ Contam Toxicol 1981;27:201᎐208.
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Asmund G, Cleemann M. Analytical methods, quality assurance and quality control used in the Greenland AMAP programme. Sci Total Environ 2000;245:203᎐219. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911᎐917. Bloom N. On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 1992;49: 1010᎐1017. Cox JA, Carnahan J, DiNunzio J, McCoy J, Meister J. Source of mercury in fish in new impoundments. Bull Environ Contam Toxicol 1979;23:779᎐783. Dietz R, Riget F, Johansen P. Lead, cadmium, mercury and selenium in Greenland marine animals. Sci Total Environ 1996;186:67᎐93. Fritzgerald WF. Is mercury increasing in the atmosphere? The need for an atmospheric network ŽAMNET.. Water, Air, Soil Pollut 1995;80:245᎐254. Grey BJ, Harbicht SM, Stephens GR. Mercury in fish from rivers and lakes in southwestern northwest territories. Yellowknife: Dept. of Indian and Northern Affairs Canada, 1995:61. Grimas A, Notter M, Olsson M, Reutergardh L. ˚ U, Gothberg ¨ ˚ Fat amount ᎏ a factor to consider in monitoring studies of heavy metals in cod liver. Ambio 1995;14:175᎐178. Hebert CE, Keenleyside KA. To normalize or not to normalize? Fat is the question. Environ Toxicol Chem 1995; 12:801᎐807. MacCrimmon HR, Christopher DW, Barra L. Mercury uptake by Lake Trout, Sal¨ elinus namaycush, relative to age, growth, and diet in Tadenac Lake with comparative data from other precambrian Shield Lakes. Can J Fish Aquat Sci 1983;40:114᎐120. Mason RP, Fitzgerald WF. Sources, sinks and biochemical cycling of mercury in the ocean. In: Baeyens W et al., editor. Global and regional mercury cycles: sources, fluxes and mass ballances. The Netherlands: Kluver Academic Publishers, 1996:249᎐272.
Muir D, Braune B, DeMarch B et al. Ecosystem uptake ands effects, chap 3. In: Jensen J, Adare K, Shearer R, editors. Canadian Arctic Contaminants Assessment Report. Ottawa: Indian and Northern Affairs Canada, 1996r1997. Nicholson MD, Green NW, Wilson SJ. Regression models for assessing trends in cadmium and PCBs in cod livers from the Oslofjord. Mar Pollut Bull 1991;22:77᎐81. Nilsson A. Arctic pollution issues: a state of the Arctic environment report. AMAP. Oslo: Arctic Monitoring and Assessment Programme, 1997:188. Nriagu JO, Pacyna JM. Quantitative assessment of worldwide contamination of air, water and soils with trace metals. Nature 1988;333:134᎐139. Riget F, Nygaard KN, Christensen B. Population structure, ecological segratation, and reproduction in a population of Arctic char Ž Sal¨ elinus alpinus. from Lake Tasersuaq, Greenland. Can J Fish Aquat Sci 1986;43:985᎐992. Riget F, Dietz R, Johansen P. Zinc, cadmium, mercury and selenium in Greenland fish. Medd Grønl Biosci 1997;48:29. SAS Institute Inc. SASrSTAT User’s Guide, version 6, 4th ed, vol. 2. Cary, NC: SAS Institute Inc, 1989:846. Scott DP, Armstrong FAJ. Mercury concentration in relation to size in several species of freshwater fishes from Manitoba and northwestern Ontario. Can J Fish Aquat Sci 1972;29:1685᎐1690. Skurdal JT, Qvenild OK, Skogheim . Mercury accumulation in five species of freshwater fish in Lake Tyrifjorden, southeast Norway, with emphasis on their suitability as test organisms. Environ Biol Fish 1985;14:233᎐238. Somers KM, Jackson DA. Adjusting mercury concentration for fish-size covariation: a multivariate alternative to bivariate regression. Can J Fish Aquat Sci 1993;50:2388᎐2396. Sparholt H. The population, survival, growth, reproduction and food of arctic charr, Sal¨ elinus alpinus, ŽL.., in four enexpoited lakes in Greenland. J Fish Biol 1985;26:313᎐330.