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Organochlorine contaminants in a local marine food chain from Jarfjord, Northern Norway
Marine Environmental Research 48 (1999) 131±146 www.elsevier.com/locate/marenvrev
Organochlorine contaminants in a local marine food chain from Jarfjord, Northern Norway A. Ruus a,*, K.I. Ugland a, O. Espeland b,1, J.U. Skaare b,c a
University of Oslo, Biological Institute, Department of Marine Zoology and Marine Chemistry, PO Box 1064, Blindern, N-0316 Oslo, Norway b Norwegian School of Veterinary Science, Department of Pharmacology, Microbiology and Food Hygiene, Division of Pharmacology and Toxicology, PO Box 8146 dep., N-0033 Oslo, Norway c National Veterinary Institute, PO Box 8156 dep., N-0033 Oslo, Norway Received 14 January 1998; received in revised form 15 February 1999; accepted 22 February 1999
Abstract Polychlorinated biphenyls (PCBs; 17 congeners), DDT (p,p0 -DDT, p,p0 -DDD, p,p0 -DDE and o,p0 -DDD), chlordanes (oxychlordane and trans-nonachlor), hexachlorocyclohexanes (HCHs; a-, b- and g-isomers) and hexachlorobenzene (HCB) have been determined in a local marine food chain including the lesser sandeel (Ammodytes marinus), cod (Gadus morhua), harbour seal (Phoca vitulina) and grey seal (Halichoerus grypus), caught in Jarfjord, Northern Norway. The concentrations of the pollutants generally increased with trophic level. The highest biomagni®cation factor (36.9) was found for DDT from sandeel to harbour seal. The compositional patterns of accumulated organochlorines also diered between the species. The proportions of highly chlorinated biphenyls, p,p0 -DDE and oxychlordane increased with higher trophic level, while the proportions of mono-ortho substituted and meta±para unsubstituted PCB congeners, together with DDD decreased from ®sh to seal. The data suggest that the bioaccumulation mechanisms at lower trophic levels (®sh) depend primarily on physicochemical factors, such as the water solubility and lipophilicity of the pollutants. At higher trophic levels (seals), the bioaccumulation mechanisms are primarily aected by biochemical factors, such as the metabolic capacity of the organisms. Prey preference may also in¯uence the patterns of accumulated pollutants in the dierent species. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Organochlorines; Food chain; Biomagni®cation; Jarfjord; Harbour seal; Grey seal; Cod; Sandeel; PCB; DDT
* Corresponding author. 1 Current address: Telemark Central Hospital, Department of Occupational and Environmental Medicine, Ulefossveien, N-3710 Skien, Norway. 0141-1136/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S0141-1136(99)00037-9
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1. Introduction The marine environment has received considerable attention in relation to environmental pollution. Dierent contaminants have reached the marine environment from anthropogenic sources by direct discharge, or indirectly by rivers and runo. The world oceans comprise 71% of the earth's surface and are, therefore, also an enormous recipient of pollutants added to the atmosphere (Woodwell, Craig & Johnson, 1971). After emission to the atmosphere, many pollutants are dispersed by repeated deposition and evaporation. Long-range transport of these pollutants to relatively pristine areas, such as the Arctic and Antarctica, has been shown (Subramanian, Tanabe, Hidaka & Tatsukawa, 1983; Wania & Mackay, 1993). The extent to which pollutants enter food chains is highly dependent on the physical and chemical properties of the compounds. Persistence and high lipid solubility render the contaminants subject to bioaccumulation and biomagni®cation. Organochlorines (OCs) are known for these properties (Addison, 1982). The highest concentrations of these compounds are, therefore, found in top predators, such as sea birds, marine mammals and polar bears (Bernhoft, Wiig & Skaare, 1997; Espeland, Kleivane, Haugen & Skaare, 1997; Gabrielsen, Skaare, Polder & Bakken, 1995; Muir, Norstrom & Simon, 1988). In the present study, we have investigated the bioaccumulation of a selected number of OC compounds, such as the pesticides DDT (p,p0 -DDT, p,p0 -DDD, p,p0 -DDE and o,p0 -DDD), CHL (chlordanes; oxychlordane and trans-nonachlor) and hexachlorocyclohexanes (HCHs; a-, b- and g-isomers), as well as the industrial pollutants, hexachlorobenzene (HCB) and polychlorinated biphenyls (PCB-28, -99, -101, -105, -118, -128, -138 -141, -153, -156, -157, -170, -180, -187, -194, -206, -209, IUPAC numbering system; Ballschmiter & Zell, 1980), in a local marine food chain from Jarfjord, Northern Norway. This food chain consisted of the lesser sandeel (Ammodytes marinus), cod (Gadus morhua), harbour seal (Phoca vitulina) and grey seal (Halichoerus grypus). The objectives of the study were to compare the OC concentrations and patterns in the four species, determine the degree of biomagni®cation in the food chain, and discuss the in¯uence of dierent factors (the lipophilicity of the chemicals, and the metabolic capacity and prey preference of the organisms) on the accumulation of the pollutants. 2. Materials and methods The animals (Table 1) were caught in Jarfjord (69 480 N, 30 250 E) in 1989 and 1990. Jarfjord is a southern branch of Varangerfjord, located in Northern Norway close to the Russian border. Blubber (above sternum) of seals, liver of cod and homogenised individuals of sandeels were sampled. 2.1. Analytical procedures The cod liver samples were macerated on a Petri dish using a scalpel, while seal blubber samples and sandeels were homogenised in a glass tube using an Ika Ultra
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Table 1 Biological data for harbour seal, grey seal, cod and sandeel from Jarfjord, Northern Norway (1989±90)a Species Seals Harbour seal
Number (n)
Females
Males
Ageb mean (range) (years)
Weight mean (range) (g)
Length mean (range) (cm)
7 (1±17) 10 (0.2±26)
75.4103 (24.5103±137.5103) 134.3103 (34103±247103)
146 (93±180) 187 (125±242)
1182 (350±3200) 14 (5±31)
47 (32±66) 16 (12±20)
7
6
1
Grey seal
23
14
9
Fish Cod
54
33
21
±
Sandeel
14
7
7
±
a
Means are arithmetric. Determined by counting dentine growth layers in transverse canine sections after Bowen, Sergeant and éritsland (1983). b
Turrax2. The samples were then extracted twice with cyclohexane and acetone (3:2 proportion) using a Cole-Parmer ultrasonic homogeniser (4710 Series). After extraction, clean-up with sulphuric acid was done according to methods described by Brevik (1978), with some modi®cations by Bernhoft and Skaare (1994). Due to a time lag between the analysing of seal and ®sh samples, together with changes in laboratory equipment, two dierent gas chromatography (GC) procedures were used. All samples were injected automatically (Fisons AS 800 auto injector) on a Carlo Erba High Resolution Gas Chromatograph (5300 Mega Series) equipped with a 63Ni-electron capture detector (Carlo Erba) and a split/splitless injector. The split ratio was set to 1:30 of 2 ml for seal samples and 1:20 of 1 ml for ®sh samples. For the seals, helium was used as carrier gas (2 ml minÿ1) on a 25-m Ultra 1 capillary column (0.32 mm i.d., 0.17-mm ®lm; Hewlett-Packard Comp.), and N2 was used as make-up gas (60 ml minÿ1). The temperature program was as follows: start: 60 C (held for 3 min), 20 C minÿ1 to 150 C, 2 C minÿ1 to 230 C (held for 5±8 min). For the ®sh samples, H2 was used as carrier gas (2 ml minÿ1) on a 60-m SPB-5 capillary column (fused silica; 0.25 mm i.d., 0.25-mm ®lm; Supelco Inc.), and 5% CH4/95% Ar was used as make-up gas (30 ml minÿ1). The temperature program was as follows: start: 90 C (held for 2 min), 25 C minÿ1 to 180 C (held for 2 min), 1.5 C minÿ1 to 220 C (held for 2 min), 3 C minÿ1 to 275 C (held for 15 min). The GC was connected to an Olivetti M 290 PC equipped with the software program Maxima 820 version 3.02 (Millipore Waters) for integration purposes. The individual OCs were determined against corresponding components in standards obtained from Cambridge Isotope Laboratories, Promochem GmbH, and Supelco Inc. No speci®c co-elution was observed in the two GCcolumns used.
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2.2. Analytical quality assurance Quanti®cations were carried out within the linear range of the detector, which is routinely determined. Detection limits ranged from 0.003 to 10 ng gÿ1 (wet wt), dependent on which chemical and trophic level was examined. Non-detected components were assigned a value of zero. Percent recovery was calculated by adding a known amount of PCB and/or pesticide standards to two to four samples of clean material. The acceptable recovery was set within 80 to 110% of added standard amount. Reproducibility was continuously tested by analysing a control sample of seal blubber. Analytical standards are certi®ed by the participation in international intercalibration tests, including the four steps of the ICES/IOC/OSPARCOM (International Council for Exploration of the Sea/International Oceanographic Commission/Oslo±Paris Commission) on PCBs in marine material (Anon, 1995). The laboratory was accredited on 11 April 1996 by the Norwegian Accreditation as a testing laboratory according to the requirements of NS-EN45001 and ISO/IEC Guide 25. 2.3. Statistical methods Biomagni®cation factors (BMFs) are de®ned as the concentration ratio of the OCs in predator to prey (Muir et al., 1988). BMFs were only calculated where there were signi®cant dierences in OC concentrations between the trophic levels (Kruskal± Wallis multiple comparisons, p<0.05). The compositional patterns of accumulated PCB congeners were analysed with multivariate statistical methods using the program package PRIMER (Plymouth Routines In Multivariate Ecological Research; Clarke & Warwick, 1994). Individuals were classi®ed after Bray±Curtis similarity (Bray & Curtis, 1957), and a MDSordination (non-metric MultiDimensional Scaling) was deduced from the similarity matrix (Kruskal, 1964a, b; Shepard, 1962). The similarity matrix was based on the percentages of all PCB congeners in all individuals (of all four species). Goodnessof-®t in the MDS ordination plot was measured as stress with Kruskal's stress formula I (Kruskal & Wish, 1978). The PCB congeners with the highest contribution to the segregation of individuals in the MDS were recognised with the program SIMPER (Similarity Percentages). The signi®cance of the interspecies dierences in PCB congener patterns was calculated with the similarity analysis ANOSIM (Clarke & Green, 1988). Interspecies dierences in the proportions of the individual OC-isomers were evaluated using the non-parametric Kruskal±Wallis multiple comparisons test (p<0.05). Dierences in proportions of mono-ortho substituted congeners (congeners with only one Cl atom in ortho positions on the phenyl rings) and congeners unsubstituted in meta±para positions (congeners with viscinal H atoms in meta±para positions on at least one of the phenyl rings) in the four species were examined with Friedman's test (with multiple comparisons; p<0.05).
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3. Results The concentration means of OCs in the present food chain ranged from about 10 ng/g (HCB in harbour seal) to about 5600 ng/g (PCB in grey seal; Table 2). The biomagni®cation factors (Fig. 1) show that PCB, DDT and CHL demonstrate a sharp increase in concentrations with higher trophic level. Interspecies dierences in the patterns of accumulated OCs were observed. Multivariate statistical methods revealed signi®cantly dierent PCB congener patterns between all four species ( p<0.05, Rglobal=0.930; Fig. 2). In the MDS plot (Fig. 2) the dierent species are segregated in distinct groups. SIMPER pointed out the ®ve congeners PCB-101, -118, -138, -153 and -180 as the main factors for the segregation. In cod, higher chlorinated biphenyls (hexa-, hepta-, octa-, nona- and decachlorobiphenyls) constituted higher proportions of PCB than in sandeel (Fig. 2). These same congeners also constituted higher proportions in grey seal and harbour seal than in both cod and sandeel. In addition, PCB congeners with vicinal H-atoms in ortho±para positions substituted with only one Cl in ortho position (mono± \ortho), together with congeners unsubstituted in meta±para positions constituted lower proportions of PCB in grey seal than in both cod and sandeel, and lower proportions in harbour seal than in cod (Fig. 2). p,p0 -DDE was the major DDT-related compound in all species, but constituted signi®cantly higher percentages of DDT in the seals than in the ®sh (harbour seal: 70.7%, grey seal: 72.0%, cod: 53.0%, sandeel: 48.3%; Fig. 3). DDD (p,p0 - and o,p0 -) constituted higher percentages of DDT in the ®sh than in the seals (harbour seal: 3.2%, grey seal: 2.3%, cod: 36.4%, sandeel: 30.9%; Fig. 3). p,p0 -DDT constituted 20.8% of DDT in sandeel, as compared to 10.6% in cod (Fig. 3). trans-Nonachlor constituted signi®cantly higher percentages in ®sh than in seals (harbour seal:
Table 2 Concentrations (ng gÿ1 lipid weight) of organochlorines (OCs), and fat content in samples of harbour seal, grey seal, cod and sandeel from Jarfjord, Northern Norway (1989±90)a Species
PCB DDT CHL HCH HCB 17 congeners Four compounds Two compounds Three isomers
Seals Harbour seal 4876 (3320) (2246±11320) Grey seal 5609 (2420) (2972±10103) Fish Cod Sandeel a
559 (274) (245±1725) 174 (95) (80±397)
Fat content (%)
2065 (2429) (619±7752) 1982 (1339) (799±6039)
703 (624) (229±1974) 736 (805) (293±3223)
80 (58) (36±180) 28 (33) (5±97)
11 (33) (5±94) 43 (61) (10±207)
92 (2) (89±95) 93 (3) (88±97)
209 (96) (98±467) 56 (26) (28±126)
68 (37) (24±182) 21 (10) (13±53)
32 (5) (19±42) 39 (12) (24±61)
33 (14) (12±69) 16 (7) (8±28)
56 (6) (37±71) 4 (2) (2±8)
Data are geometric means followed by standard deviations with ranges given beneath. PCB, polychlorinated biphenyl; CHL, chlordane; HCH, hexachlorocyclohexane; HCB, hexachlorobenzene.
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Fig. 1. Biomagni®cation factors (BMFs) between levels in the studied food chain from Jarfjord, Northern Norway (1989±90).
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Fig. 2. (a) Proportions of individual polychlorinated biphenyl (PCB) congeners as percent of PCB in harbour seal, grey seal, cod and sandeel (error bars indicate SE). Mono-ortho substituted and meta±para unsubstituted congeners are shown (*, Cl-substitution). (b) MDS-ordination of the individuals (from all four species) based on the percentages of the congeners. H, harbour seal; G, grey seal; C, cod; S, sandeel.
66.6%, grey seal: 60.5%, cod: 90.6%, sandeel: 82.9%; Fig. 3). Of the HCHs, a-HCH was the major isomer in all species (harbour seal: 75.2%, grey seal: 88.1%, cod: 65.8%, sandeel: 45.2%; Fig. 3). b-HCH was not found in cod, but constituted signi®cantly higher percentages of HCH in sandeel (31.5%) than in seals (6.4 and 4.2% in harbour seal and grey seal, respectively; Fig. 3). Of all the ®ve groups of OCs (PCB, DDT, CHL, HCH and HCB), PCB and DDT constituted the highest proportions of total OCs in all species (PCB: 62.4, 66.0, 61.6 and 56.2% in harbour seal, grey seal, cod and sandeel, respectively;
Fig. 3. (a) Proportions of the dierent DDT compounds as percent of DDT; (b) proportions of the dierent chlordane (CHL) compounds as percent of CHL; (c) proportions of the dierent hexachlorocyclohexane (HCH) isomers as percent of HCH; and (d) proportions of the dierent organochlorine (OC) groups as percent of total OCs in harbour seal, grey seal, cod and sandeel (error bars indicate SE).
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DDT: 27.0, 23.6, 23.2 and 18.4% harbour seal, grey seal, cod and sandeel, respectively; Fig. 3). Furthermore, HCH and HCB constituted higher proportions in the ®sh than in the seals (HCH: 1.1, 0.5, 3.8 and 13.2% in harbour seal, grey seal, cod and sandeel, respectively; HCB: 0.3, 0.8, 3.8 and 5.4% harbour seal, grey seal, cod and sandeel, respectively; Fig. 3). HCH also constituted higher proportions of OC in sandeel than in cod (Fig. 3). 4. Discussion 4.1. Methods Ideally, BMFs should be developed by comparisons of whole body concentrations of OCs in predator and prey. However, in the present food chain this was not practical due to the great dierences in size between the species constituting the food chain. Therefore, selected single tissues or whole body concentrations were used depending on the size of the species. Although the BMFs were based on lipidnormalized concentrations, these may not be fully representative for the whole body concentrations, since intertissue dierences in OC levels and pro®les within a species may occur (Bernhoft & Skaare, 1994). Furthermore, the use of dierent GCcolumns with dierent separation eciency must be taken in consideration, and caution must be exercised in the interpretation of results. In addition, there are most likely more components present in the animals studied than the limited number our methods allowed us to analyse (Muir et al., 1988). For instance, we only analysed two chlordane compounds. Nevertheless, the proportions of these are interesting in regard to the metabolic capacity of each species. 4.2. Biomagni®cation The BMFs obtained in this study were not very dierent from corresponding factors reported earlier. Muir et al. (1988) found the following BMFs from arctic cod (Boreogadus saida) to (male) ringed seal (Phoca hispida) in a food chain of the Canadian arctic archipelago: BMFPCB=8.8, BMFDDT=20.2, BMFCHL=7.3, BMFHCH=1.5 and BMFCBz=0.2. Furthermore, Tanabe, Tanaka and Tatsukawa (1984) found dierences in tissue concentrations in the myctophid Diaphus suborbitalis and striped dolphin (Stenella coeruleoalba) equivalent to BMFPCB=18.7, BMFDDT=30.8 and BMFHCH=8.4. In a model proposed by Thomann (1989), low elimination rates apply to compounds with log Kow values (Kow is the octanol±water partition coecient) between 5 and 7, and thus, biomagni®cation will occur for these compounds. The individual PCBs determined in the present study have log Kow values between 5 and 8, with log Kow increasing with the degree of chlorination (Mackay, Shiu & Ma, 1992). Furthermore, the DDT and chlordane compounds have log Kow6 (Isnard & Lambert, 1988; Simpson, Wilcock, Smith, Wilkins & Langdon, 1995). For HCB log Kow 6, while the HCH isomers have log Kow4 (Isnard & Lambert, 1988). The low
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octanol±water partition coecients for the HCH isomers could, according to Thomann (1989), partly explain the low/absent biomagni®cation of these compounds in the food chain. In the present study no biomagni®cation was found for HCB from ®sh to harbour seal, due to the low concentrations of HCB in harbour seal. The lower concentrations of HCB in harbour seal, compared to grey seal, may be explained by dierent food preferences (Skeie, 1994). The low BMFs obtained for HCHs and HCB may re¯ect that ®sh bioconcentrate these compounds directly from the sea water, while seals have the capability to metabolise and eliminate them. Bioaccumulation of OCs in ®sh depends on the equilibrium partitioning between body lipids and the surrounding water, with the gill surface playing an important role in this partitioning (Bruggerman, Martron, Kooiman & Hutzinger, 1982). HCHs and HCB constitute the largest proportions of OC in sea water at high latitudes (Barrie et al., 1997). Seals have no respiratory surface in contact with water and, therefore, will not bioconcentrate OCs by this route. 4.3. Patterns of accumulated OCs The present interspecies dierences in patterns of accumulated OCs may be explained by dierent rates of accumulation from the water (bioconcentration) in the case of ®sh, and by the dietary route, especially in the case of seal (Knutzen, Klungsùyr, Oug & Nñs, 1992; Walker, 1990). The patterns also re¯ect dierences in metabolic capability among the species (Boon, Eijgenraam, Everaarts & Duinker, 1989). 4.3.1. PCBs The equilibrium partitioning of OCs between an aquatic organism and the surrounding water can be viewed as an approximate lipid±water partitioning, and can be estimated from the octanol±water partition coecient (Neely, Branson & Blau, 1974). Small individuals will probably reach equilibrium faster than larger individuals because the rate between the respiratory surface and the body volume is larger (Knutzen et al., 1992; Tarr, Barron & Hayton, 1990). Less lipophilic compounds will reach equilibrium ®rst (Hawker & Connell, 1985). Sandeels are smaller than cod (Table 1), and lower chlorinated biphenyls are less lipophilic than higher chlorinated biphenyls. This could explain some of the dierences in PCB congener patterns between sandeels and cod. The interspecies dierences in congener patterns (and segregation in the MDSplot) may also partly be explained by dierent prey preferences. Sandeels feed on planktonic crustaceans, while cod often prefer benthic animals. This may result in cod accumulating higher chlorinated biphenyls to a larger extent through the dietary route than sandeels. Subramanian et al. (1983) also found higher proportions of higher chlorinated biphenyls in bottom-dwelling ®sh than in pelagic zooplanktoneating ®sh. Dierent prey preferences (Skeie, 1994) may also explain some of the dierences in congener patterns found between the two seal species.
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Metabolism of lower chlorinated PCBs and biomagni®cation of highly chlorinated congeners most likely explain the major dierences in PCB patterns between ®sh and seals (Stegeman, 1993). Dierent PCB congeners are metabolised by biotransformation enzymes from dierent subfamilies in the cytochrome P450 system (Goksùyr & FoÈrlin, 1992; Stegeman, 1993). Enzymes of the CYP 1A subfamily biotransform coplanar PCB congeners with vicinal H-atoms in ortho±meta positions (Boon, Reijnders, Dols, Wensvoort & Hillebrand, 1987; Goksùyr & FoÈrlin, 1992; Stegeman, 1993). Mono-ortho substituted PCBs are partly coplanar, but congeners with two or more Cl-atoms in ortho-positions are sterically prevented from having this conformation. In mammals, enzymes of the CYP 2B subfamily catalyse the biotransformation of PCBs by epoxidation in meta±para position and are dependent on free H-atoms (no Cl-substitution) in these positions (Boon et al., 1987; Goksùyr & FoÈrlin, 1992; Stegeman, 1993). The CYP 2B proteins biotransform PCBs regardless of conformation (coplanar or globular). P450 proteins in the liver of several ®sh species may be classi®ed in the CYP 1A subfamily, while only a few have been found to have a close immunological relationship to the mammalian 2B proteins (Stegeman, 1993). Evidence of the presence of CYP 2B-type enzymes in seals is the discovery of methylsulfone metabolites of OCs in these animals (Haraguchi, Athanasiadou, Bergman, Hovander & Jensen, 1992; JanaÂk et al., 1998). The ®nding that mono-ortho substituted congeners (with vicinal H-atoms in ortho±meta positions) and congeners unsubstituted in the meta±para positions constituted lower proportions of PCB in grey seal than in both cod and sandeel, and lower proportions in harbour seal than in cod, is therefore most likely explained by seals having a higher metabolic capacity than ®sh. 4.3.2. DDTs Recording that p,p0 -DDE constituted higher percentages of DDT in the seals than in the ®sh, most likely resulted from higher metabolic capacity in the seals. p,p0 DDT is metabolised to p,p0 -DDE in both ®sh (Addison & Willis, 1978) and seals (Letcher, Norstrom & Muir, 1998). Increasing proportions of DDE, together with decreasing proportions of DDD from ®sh to marine mammals, have also been observed in other food chain studies (Tanabe et al., 1984). Dierences in the relative concentrations of the DDT compounds in sandeel and cod may re¯ect that the relative proportions of these compounds in the environment are changing (Larsson & Okla, 1989). Sandeels will probably respond faster than cod to a change in the relative concentrations of the DDT compounds in sea water due to their smaller size. Dierent prey preferences may also contribute to dierences in the relative proportions of accumulated DDT compounds in sandeel and cod. Sandeels feed on zooplankton, which appear to contain high proportions of p,p0 -DDT compared to p,p0 -DDE (Bildeman et al., 1989; Tanabe et al., 1984). 4.3.3. Chlordanes Higher oxychlordane:trans-nonachlor ratios in seals compared to ®sh are due to a higher capability of seals to metabolise chlordane compounds. Corresponding
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results have also been reported by others (Muir et al., 1988; Nakata, Tanabe, Tatsukawa, Amano, Miyazaki & Petrov, 1995). The most important components of technical chlordane (cis-chlordane, trans-chlordane and trans-nonachlor; Dearth & Hites, 1991) are known to be metabolised to oxychlordane in mammals (Street & Blau, 1972; Tashiro & Matsumura, 1978). 4.3.4. HCHs and HCB a-HCH was found to be the most abundant of the HCH-isomers in all the present species, and this is in accordance with other studies in northern areas (Nakata et al., 1995; Oehme, 1991). Oehme (1991) observed that the a-HCH:g-HCH ratio in ringed seal from the North Sea was approximately 2:1, while the same ratio was more than 20:1 in ringed seal from Svalbard. The annual transport of a- and g-HCH to the Arctic has been modelled by Cotham and Bidleman (1991). They concluded that the import of a-HCH was 7.5 times higher than the import of g-HCH. b-HCH constituted higher percentages of HCH in the seals than in cod, thus re¯ecting the high persistence of this isomer (Xu, Wu, Zhang, Staudacher, Kettrup & Steinberg, 1994), which gives it a high bioaccumulative potential (Baumann, Angerer, Heinrich & Lehnert, 1980). These ®ndings are also in accordance with other observations of HCHs in ®sh and sea mammals (Nakata et al., 1995; Tanabe et al., 1984). It is dicult to explain our ®nding that sandeels had accumulated remarkably larger percentages of b-HCH (34.5% of HCH) than all the other species. Highly developed capability to metabolise the other HCH-isomers is unlikely, but cannot be ruled out. Due to their relatively smaller size, sandeels may also have bioconcentrated b-HCH from the environment to a larger extent than cod. b-HCH has reached the environment from the usage of technical HCH (BHC), which contains 5±14% of this isomer (Li, McMillan & Scholtz, 1996). Technical HCH has been used to protect crops in the former Soviet Union (Li et al., 1996), and in Lake Baikal seals and ®sh have been found to contain elevated proportions of b-HCH (Nakata et al., 1995). HCH and HCB constituted higher proportions of the total OCs (OC) in ®sh, as compared to seals, and this probably results from continuous bioconcentration of these compounds from sea water through the gill epithelium in ®sh, while the seals to a larger extent metabolise and eliminate them. HCHs and HCB constitute the largest proportions of OC in arctic sea water (Barrie et al., 1997). HCH also constituted higher proportions of OC in sandeel than in cod, probably because sandeels have bioconcentrated HCHs to a larger extent, due to their relatively smaller size. It is also possible that sandeels have received more HCHs through their zooplankton diet, which contains elevated amounts of HCHs, relative to other OCs (Bidleman et al., 1989). 5. Conclusions The biomagni®cation factors calculated for the present food chain show that the concentrations of the OCs generally increase with trophic level. The highest BMF
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(36.9) was found for DDT from sandeel to harbour seal. HCH and HCB, however, are not biomagni®ed to a similar extent. The low BMFs obtained for HCH and HCB suggest that ®sh continuously bioconcentrate these compounds, while seals have a good capability to metabolise and eliminate them. HCH and HCB constituted higher proportions of OC in ®sh than in seals, probably for the same reasons. The compositional patterns of all the accumulated OCs diered among the species. Our observations suggest that the bioaccumulation mechanisms at lower trophic levels (®sh) depend primarily on physicochemical factors, such as the water solubility and lipophilicity of the pollutants. At higher trophic levels (seals), the bioaccumulation mechanisms are primarily aected by biochemical factors, such as the metabolic capacity of the organisms. In addition, prey preference may in¯uence the patterns of accumulated pollutants in all the species examined. Acknowledgements We thank the hunter Steinar Magnussen for help with collecting the material. Appreciation is also expressed to the following persons for help and enjoyable company during the work: Paul Eric Aspholm, Signe Haugen, Anuschka Polder, Vidar Berg, Erna Stai, Elisabeth Lie, Siri Fùreid, Lars Kleivane and Hñge Krogh. Thanks also to Jonathan Edward Colman and Jane Indrehus for proof-reading the manuscript. References Addison, R. F. (1982). Organochlorine compounds and marine lipids. Progress in Lipid Research, 21, 47±71. Addison, R. F., & Willis, D. E. (1978). The metabolism by rainbow trout (Salmo gairdnerii) of p,p0 [14C]DDT and some of its possible degradation products labeled with 14C. Toxicology and Applied Pharmacology, 43, 303±315. Anon. (1995). Report on the results of the ICES/IOC/OSPARCOM intercomparison programme on the analyses of chlorobiphenyls in marine media-step 2 (Cooperative Research Report No. 207). ICES, Copenhagen. Ballschmiter, K., & Zell, M. (1980). Analysis of polychlorinated biphenyls (PCB) by glass capillary gas chromatography. Composition of technical Aroclor± and Clophen±PCB mixtures. Fresenius' Zeitschrift fuÈr analytische Chemie, 302, 20±30. Barrie, L. Macdonald, R., Bidleman, T., Diamond, M., Gregor, D., Semkin, R., Strachan, W., Alaee, M., Backus, S., Bewers, M., Gobeil, C., Halsall, C., Ho, J., Li, A., Lockhart, L., Mackay, D., Muir, D., Pudykiewicz, J., Reimer, K., Smith, J., Stern, G. Schroeder, W., Wagemann R., Wania F., & Yunker, M. (1997). Sources, occurrence and pathways. In J. JensenK. AdareK. & R. Shearer, Canadian Arctic Contaminants Assessment Report (pp. 25±182). Ottawa: Indian and Northern Aairs Canada. Baumann, K., Angerer, J., Heinrich, R., & Lehnert, G. (1980). Occupational exposure to hexachlorocyclohexane. I. Body burden of HCH-isomers. International Archives of Occupational and Environmental Health, 47, 119±127. Bernhoft, A., & Skaare, J. U. (1994). Levels of selected individual polychlorinated biphenyls in dierent tissues of harbour seals (Phoca vitulina) from the southern coast of Norway. Environmental Pollution, 86, 99±107. Bernhoft, A., Wiig, é., & Skaare, J. U. (1997). Organochlorines in polar bears (Ursus maritimus) at Svalbard. Environmental Pollution, 95, 159±175.
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Kruskal, J. B. (1964b). Nonmetric multidimensional scaling: a numerical method. Psychometrika, 29, 115± 129. Kruskal, J. B., & Wish, M. (1978). Multidimensional scaling. Beverly Hills: Sage. Larsson, P., & Okla, L. (1989). Atmospheric transport of chlorinated hydrocarbons to Sweden in 1985 compared to 1973. Atmospheric Environment, 23, 1699±1711. Letcher, R. J., Norstrom, R. J., & Muir, D. C. G. (1998). Biotransformation versus bioaccumulation: sources of methyl sulfone PCB and 4,40 -DDE metabolites in the polar bear food chain. Environmental Science and Technology, 32, 1656±1661. Li, Y. F., McMillan, A., & Scholtz, M. T. (1996). Global HCH usage with 1 1 longitude/latitude resolution. Environmental Science and Technology, 30, 3525±3533. Mackay, D., Shiu, W. Y., & Ma, K. C. (1992). Illustrated handbook of physical±chemical properties and environmental fate for organic chemicals. Vol. 1. Monoaromatic hydrocarbons, chlorobenzenes, and PCBs. Boca Raton: Lewis. Muir, D. C. G., Norstrom, R. J., & Simon, M. (1988). Organochlorine contaminants in Arctic marine food chains: accumulation of speci®c polychlorinated biphenyls and chlordane-related compounds. Environmental Science and Technology, 22, 1071±1079. Nakata, H., Tanabe, S., Tatsukawa, R., Amano, M., Miyazaki, N., & Petrov, E. A. (1995). Persistent organochlorine residues and their accumulation kinetics in Baikal seal (Phoca sibirica) from Lake Baikal, Russia. Environmental Science and Technology, 29, 2877±2885. Neely, W. B., Branson, D. R., & Blau, G. E. (1974). Partition coecient to measure bioconcentration potential of organic chemicals in ®sh. Environmental Science and Technology, 8, 1113±1115. Oehme, M. (1991). Dispersion and transport paths of toxic persistent organochlorines to the ArcticÐ levels and consequences. The Science of the Total Environment, 106, 43±53. Shepard, R. N. (1962). The analysis of proximities: multidimensional scaling with an unknown distance function. II. Psychometrika, 27, 219±246. Simpson, C. D., Wilcock, R. J., Smith, T. J., Wilkins, A. L., & Langdon, A. G. (1995). Determination of octanol±water partition coecients for the major components of technical chlordane. Bulletin of Environmental Contamination and Toxicology, 55, 149±153. Skeie, K. (1994). Diet composition and niche partitioning between seal species in Jarfjord. Cand. Scient. thesis, University of Oslo. (In Norwegian.) Stegeman, J. J. (1993). The cytochromes P450 in ®sh. In Hochachka & Mommsen, Biochemistry and molecular biology of ®shes (Vol. 2, pp. 135±158). Amsterdam: Elsevier Science. Street, J. C., & Blau, S. E. (1972). Oxychlordane: accumulation in rat adipose tissue on feeding chlordane isomers or technical chlordane. Journal of Agricultural and Food Chemistry, 20, 395±397. Subramanian, B. R., Tanabe, S., Hidaka, H., & Tatsukawa, R. (1983). DDTs and PCB isomers and congeners in Antarctic ®sh. Archives of Environmental Contamination and Toxicology, 12, 621±626. Tanabe, S., Tanaka, H., & Tatsukawa, R. (1984). Polychlorobiphenyls, DDT, and hexachlorocyclohexane isomers in the western North Paci®c ecosystem. Archives of Environmental Contamination and Toxicology, 13, 731±738. Tarr, B. D., Barron, M. G., & Hayton, W. L. (1990). Eect of body size on the uptake and bioconcentration of di-2-ethylhexyl phthalate in rainbow trout. Environmental Toxicology and Chemistry, 9, 989± 995. Tashiro, S., & Matsumura, F. (1978). Metabolism of trans-nonachlor and related chlordane compounds in rat and man. Archives of Environmental Contamination and Toxicology, 7, 113±127. Thomann, R. V. (1989). Bioaccumulation model of organic chemical distribution in aquatic food chains. Environmental Science and Technology, 23, 699±707. Walker, C. H. (1990). Kinetic models to predict bioaccumulation of pollutants. Functional Ecology, 4, 295±301. Wania, F., & Mackay, D. (1993). Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions. Ambio, 22, 10±18. Woodwell, G. M., Craig, P. P., & Johnson, A. (1971). DDT in the biosphere: where does it go? Science, 174, 1101±1107.
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Organochlorine contaminants in a local marine food chain from Jarfjord, Northern Norway A. Ruus a,*, K.I. Ugland a, O. Espeland b,1, J.U. Skaare b,c a
University of Oslo, Biological Institute, Department of Marine Zoology and Marine Chemistry, PO Box 1064, Blindern, N-0316 Oslo, Norway b Norwegian School of Veterinary Science, Department of Pharmacology, Microbiology and Food Hygiene, Division of Pharmacology and Toxicology, PO Box 8146 dep., N-0033 Oslo, Norway c National Veterinary Institute, PO Box 8156 dep., N-0033 Oslo, Norway Received 14 January 1998; received in revised form 15 February 1999; accepted 22 February 1999
Abstract Polychlorinated biphenyls (PCBs; 17 congeners), DDT (p,p0 -DDT, p,p0 -DDD, p,p0 -DDE and o,p0 -DDD), chlordanes (oxychlordane and trans-nonachlor), hexachlorocyclohexanes (HCHs; a-, b- and g-isomers) and hexachlorobenzene (HCB) have been determined in a local marine food chain including the lesser sandeel (Ammodytes marinus), cod (Gadus morhua), harbour seal (Phoca vitulina) and grey seal (Halichoerus grypus), caught in Jarfjord, Northern Norway. The concentrations of the pollutants generally increased with trophic level. The highest biomagni®cation factor (36.9) was found for DDT from sandeel to harbour seal. The compositional patterns of accumulated organochlorines also diered between the species. The proportions of highly chlorinated biphenyls, p,p0 -DDE and oxychlordane increased with higher trophic level, while the proportions of mono-ortho substituted and meta±para unsubstituted PCB congeners, together with DDD decreased from ®sh to seal. The data suggest that the bioaccumulation mechanisms at lower trophic levels (®sh) depend primarily on physicochemical factors, such as the water solubility and lipophilicity of the pollutants. At higher trophic levels (seals), the bioaccumulation mechanisms are primarily aected by biochemical factors, such as the metabolic capacity of the organisms. Prey preference may also in¯uence the patterns of accumulated pollutants in the dierent species. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Organochlorines; Food chain; Biomagni®cation; Jarfjord; Harbour seal; Grey seal; Cod; Sandeel; PCB; DDT
* Corresponding author. 1 Current address: Telemark Central Hospital, Department of Occupational and Environmental Medicine, Ulefossveien, N-3710 Skien, Norway. 0141-1136/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S0141-1136(99)00037-9
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1. Introduction The marine environment has received considerable attention in relation to environmental pollution. Dierent contaminants have reached the marine environment from anthropogenic sources by direct discharge, or indirectly by rivers and runo. The world oceans comprise 71% of the earth's surface and are, therefore, also an enormous recipient of pollutants added to the atmosphere (Woodwell, Craig & Johnson, 1971). After emission to the atmosphere, many pollutants are dispersed by repeated deposition and evaporation. Long-range transport of these pollutants to relatively pristine areas, such as the Arctic and Antarctica, has been shown (Subramanian, Tanabe, Hidaka & Tatsukawa, 1983; Wania & Mackay, 1993). The extent to which pollutants enter food chains is highly dependent on the physical and chemical properties of the compounds. Persistence and high lipid solubility render the contaminants subject to bioaccumulation and biomagni®cation. Organochlorines (OCs) are known for these properties (Addison, 1982). The highest concentrations of these compounds are, therefore, found in top predators, such as sea birds, marine mammals and polar bears (Bernhoft, Wiig & Skaare, 1997; Espeland, Kleivane, Haugen & Skaare, 1997; Gabrielsen, Skaare, Polder & Bakken, 1995; Muir, Norstrom & Simon, 1988). In the present study, we have investigated the bioaccumulation of a selected number of OC compounds, such as the pesticides DDT (p,p0 -DDT, p,p0 -DDD, p,p0 -DDE and o,p0 -DDD), CHL (chlordanes; oxychlordane and trans-nonachlor) and hexachlorocyclohexanes (HCHs; a-, b- and g-isomers), as well as the industrial pollutants, hexachlorobenzene (HCB) and polychlorinated biphenyls (PCB-28, -99, -101, -105, -118, -128, -138 -141, -153, -156, -157, -170, -180, -187, -194, -206, -209, IUPAC numbering system; Ballschmiter & Zell, 1980), in a local marine food chain from Jarfjord, Northern Norway. This food chain consisted of the lesser sandeel (Ammodytes marinus), cod (Gadus morhua), harbour seal (Phoca vitulina) and grey seal (Halichoerus grypus). The objectives of the study were to compare the OC concentrations and patterns in the four species, determine the degree of biomagni®cation in the food chain, and discuss the in¯uence of dierent factors (the lipophilicity of the chemicals, and the metabolic capacity and prey preference of the organisms) on the accumulation of the pollutants. 2. Materials and methods The animals (Table 1) were caught in Jarfjord (69 480 N, 30 250 E) in 1989 and 1990. Jarfjord is a southern branch of Varangerfjord, located in Northern Norway close to the Russian border. Blubber (above sternum) of seals, liver of cod and homogenised individuals of sandeels were sampled. 2.1. Analytical procedures The cod liver samples were macerated on a Petri dish using a scalpel, while seal blubber samples and sandeels were homogenised in a glass tube using an Ika Ultra
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Table 1 Biological data for harbour seal, grey seal, cod and sandeel from Jarfjord, Northern Norway (1989±90)a Species Seals Harbour seal
Number (n)
Females
Males
Ageb mean (range) (years)
Weight mean (range) (g)
Length mean (range) (cm)
7 (1±17) 10 (0.2±26)
75.4103 (24.5103±137.5103) 134.3103 (34103±247103)
146 (93±180) 187 (125±242)
1182 (350±3200) 14 (5±31)
47 (32±66) 16 (12±20)
7
6
1
Grey seal
23
14
9
Fish Cod
54
33
21
±
Sandeel
14
7
7
±
a
Means are arithmetric. Determined by counting dentine growth layers in transverse canine sections after Bowen, Sergeant and éritsland (1983). b
Turrax2. The samples were then extracted twice with cyclohexane and acetone (3:2 proportion) using a Cole-Parmer ultrasonic homogeniser (4710 Series). After extraction, clean-up with sulphuric acid was done according to methods described by Brevik (1978), with some modi®cations by Bernhoft and Skaare (1994). Due to a time lag between the analysing of seal and ®sh samples, together with changes in laboratory equipment, two dierent gas chromatography (GC) procedures were used. All samples were injected automatically (Fisons AS 800 auto injector) on a Carlo Erba High Resolution Gas Chromatograph (5300 Mega Series) equipped with a 63Ni-electron capture detector (Carlo Erba) and a split/splitless injector. The split ratio was set to 1:30 of 2 ml for seal samples and 1:20 of 1 ml for ®sh samples. For the seals, helium was used as carrier gas (2 ml minÿ1) on a 25-m Ultra 1 capillary column (0.32 mm i.d., 0.17-mm ®lm; Hewlett-Packard Comp.), and N2 was used as make-up gas (60 ml minÿ1). The temperature program was as follows: start: 60 C (held for 3 min), 20 C minÿ1 to 150 C, 2 C minÿ1 to 230 C (held for 5±8 min). For the ®sh samples, H2 was used as carrier gas (2 ml minÿ1) on a 60-m SPB-5 capillary column (fused silica; 0.25 mm i.d., 0.25-mm ®lm; Supelco Inc.), and 5% CH4/95% Ar was used as make-up gas (30 ml minÿ1). The temperature program was as follows: start: 90 C (held for 2 min), 25 C minÿ1 to 180 C (held for 2 min), 1.5 C minÿ1 to 220 C (held for 2 min), 3 C minÿ1 to 275 C (held for 15 min). The GC was connected to an Olivetti M 290 PC equipped with the software program Maxima 820 version 3.02 (Millipore Waters) for integration purposes. The individual OCs were determined against corresponding components in standards obtained from Cambridge Isotope Laboratories, Promochem GmbH, and Supelco Inc. No speci®c co-elution was observed in the two GCcolumns used.
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2.2. Analytical quality assurance Quanti®cations were carried out within the linear range of the detector, which is routinely determined. Detection limits ranged from 0.003 to 10 ng gÿ1 (wet wt), dependent on which chemical and trophic level was examined. Non-detected components were assigned a value of zero. Percent recovery was calculated by adding a known amount of PCB and/or pesticide standards to two to four samples of clean material. The acceptable recovery was set within 80 to 110% of added standard amount. Reproducibility was continuously tested by analysing a control sample of seal blubber. Analytical standards are certi®ed by the participation in international intercalibration tests, including the four steps of the ICES/IOC/OSPARCOM (International Council for Exploration of the Sea/International Oceanographic Commission/Oslo±Paris Commission) on PCBs in marine material (Anon, 1995). The laboratory was accredited on 11 April 1996 by the Norwegian Accreditation as a testing laboratory according to the requirements of NS-EN45001 and ISO/IEC Guide 25. 2.3. Statistical methods Biomagni®cation factors (BMFs) are de®ned as the concentration ratio of the OCs in predator to prey (Muir et al., 1988). BMFs were only calculated where there were signi®cant dierences in OC concentrations between the trophic levels (Kruskal± Wallis multiple comparisons, p<0.05). The compositional patterns of accumulated PCB congeners were analysed with multivariate statistical methods using the program package PRIMER (Plymouth Routines In Multivariate Ecological Research; Clarke & Warwick, 1994). Individuals were classi®ed after Bray±Curtis similarity (Bray & Curtis, 1957), and a MDSordination (non-metric MultiDimensional Scaling) was deduced from the similarity matrix (Kruskal, 1964a, b; Shepard, 1962). The similarity matrix was based on the percentages of all PCB congeners in all individuals (of all four species). Goodnessof-®t in the MDS ordination plot was measured as stress with Kruskal's stress formula I (Kruskal & Wish, 1978). The PCB congeners with the highest contribution to the segregation of individuals in the MDS were recognised with the program SIMPER (Similarity Percentages). The signi®cance of the interspecies dierences in PCB congener patterns was calculated with the similarity analysis ANOSIM (Clarke & Green, 1988). Interspecies dierences in the proportions of the individual OC-isomers were evaluated using the non-parametric Kruskal±Wallis multiple comparisons test (p<0.05). Dierences in proportions of mono-ortho substituted congeners (congeners with only one Cl atom in ortho positions on the phenyl rings) and congeners unsubstituted in meta±para positions (congeners with viscinal H atoms in meta±para positions on at least one of the phenyl rings) in the four species were examined with Friedman's test (with multiple comparisons; p<0.05).
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3. Results The concentration means of OCs in the present food chain ranged from about 10 ng/g (HCB in harbour seal) to about 5600 ng/g (PCB in grey seal; Table 2). The biomagni®cation factors (Fig. 1) show that PCB, DDT and CHL demonstrate a sharp increase in concentrations with higher trophic level. Interspecies dierences in the patterns of accumulated OCs were observed. Multivariate statistical methods revealed signi®cantly dierent PCB congener patterns between all four species ( p<0.05, Rglobal=0.930; Fig. 2). In the MDS plot (Fig. 2) the dierent species are segregated in distinct groups. SIMPER pointed out the ®ve congeners PCB-101, -118, -138, -153 and -180 as the main factors for the segregation. In cod, higher chlorinated biphenyls (hexa-, hepta-, octa-, nona- and decachlorobiphenyls) constituted higher proportions of PCB than in sandeel (Fig. 2). These same congeners also constituted higher proportions in grey seal and harbour seal than in both cod and sandeel. In addition, PCB congeners with vicinal H-atoms in ortho±para positions substituted with only one Cl in ortho position (mono± \ortho), together with congeners unsubstituted in meta±para positions constituted lower proportions of PCB in grey seal than in both cod and sandeel, and lower proportions in harbour seal than in cod (Fig. 2). p,p0 -DDE was the major DDT-related compound in all species, but constituted signi®cantly higher percentages of DDT in the seals than in the ®sh (harbour seal: 70.7%, grey seal: 72.0%, cod: 53.0%, sandeel: 48.3%; Fig. 3). DDD (p,p0 - and o,p0 -) constituted higher percentages of DDT in the ®sh than in the seals (harbour seal: 3.2%, grey seal: 2.3%, cod: 36.4%, sandeel: 30.9%; Fig. 3). p,p0 -DDT constituted 20.8% of DDT in sandeel, as compared to 10.6% in cod (Fig. 3). trans-Nonachlor constituted signi®cantly higher percentages in ®sh than in seals (harbour seal:
Table 2 Concentrations (ng gÿ1 lipid weight) of organochlorines (OCs), and fat content in samples of harbour seal, grey seal, cod and sandeel from Jarfjord, Northern Norway (1989±90)a Species
PCB DDT CHL HCH HCB 17 congeners Four compounds Two compounds Three isomers
Seals Harbour seal 4876 (3320) (2246±11320) Grey seal 5609 (2420) (2972±10103) Fish Cod Sandeel a
559 (274) (245±1725) 174 (95) (80±397)
Fat content (%)
2065 (2429) (619±7752) 1982 (1339) (799±6039)
703 (624) (229±1974) 736 (805) (293±3223)
80 (58) (36±180) 28 (33) (5±97)
11 (33) (5±94) 43 (61) (10±207)
92 (2) (89±95) 93 (3) (88±97)
209 (96) (98±467) 56 (26) (28±126)
68 (37) (24±182) 21 (10) (13±53)
32 (5) (19±42) 39 (12) (24±61)
33 (14) (12±69) 16 (7) (8±28)
56 (6) (37±71) 4 (2) (2±8)
Data are geometric means followed by standard deviations with ranges given beneath. PCB, polychlorinated biphenyl; CHL, chlordane; HCH, hexachlorocyclohexane; HCB, hexachlorobenzene.
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Fig. 1. Biomagni®cation factors (BMFs) between levels in the studied food chain from Jarfjord, Northern Norway (1989±90).
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Fig. 2. (a) Proportions of individual polychlorinated biphenyl (PCB) congeners as percent of PCB in harbour seal, grey seal, cod and sandeel (error bars indicate SE). Mono-ortho substituted and meta±para unsubstituted congeners are shown (*, Cl-substitution). (b) MDS-ordination of the individuals (from all four species) based on the percentages of the congeners. H, harbour seal; G, grey seal; C, cod; S, sandeel.
66.6%, grey seal: 60.5%, cod: 90.6%, sandeel: 82.9%; Fig. 3). Of the HCHs, a-HCH was the major isomer in all species (harbour seal: 75.2%, grey seal: 88.1%, cod: 65.8%, sandeel: 45.2%; Fig. 3). b-HCH was not found in cod, but constituted signi®cantly higher percentages of HCH in sandeel (31.5%) than in seals (6.4 and 4.2% in harbour seal and grey seal, respectively; Fig. 3). Of all the ®ve groups of OCs (PCB, DDT, CHL, HCH and HCB), PCB and DDT constituted the highest proportions of total OCs in all species (PCB: 62.4, 66.0, 61.6 and 56.2% in harbour seal, grey seal, cod and sandeel, respectively;
Fig. 3. (a) Proportions of the dierent DDT compounds as percent of DDT; (b) proportions of the dierent chlordane (CHL) compounds as percent of CHL; (c) proportions of the dierent hexachlorocyclohexane (HCH) isomers as percent of HCH; and (d) proportions of the dierent organochlorine (OC) groups as percent of total OCs in harbour seal, grey seal, cod and sandeel (error bars indicate SE).
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DDT: 27.0, 23.6, 23.2 and 18.4% harbour seal, grey seal, cod and sandeel, respectively; Fig. 3). Furthermore, HCH and HCB constituted higher proportions in the ®sh than in the seals (HCH: 1.1, 0.5, 3.8 and 13.2% in harbour seal, grey seal, cod and sandeel, respectively; HCB: 0.3, 0.8, 3.8 and 5.4% harbour seal, grey seal, cod and sandeel, respectively; Fig. 3). HCH also constituted higher proportions of OC in sandeel than in cod (Fig. 3). 4. Discussion 4.1. Methods Ideally, BMFs should be developed by comparisons of whole body concentrations of OCs in predator and prey. However, in the present food chain this was not practical due to the great dierences in size between the species constituting the food chain. Therefore, selected single tissues or whole body concentrations were used depending on the size of the species. Although the BMFs were based on lipidnormalized concentrations, these may not be fully representative for the whole body concentrations, since intertissue dierences in OC levels and pro®les within a species may occur (Bernhoft & Skaare, 1994). Furthermore, the use of dierent GCcolumns with dierent separation eciency must be taken in consideration, and caution must be exercised in the interpretation of results. In addition, there are most likely more components present in the animals studied than the limited number our methods allowed us to analyse (Muir et al., 1988). For instance, we only analysed two chlordane compounds. Nevertheless, the proportions of these are interesting in regard to the metabolic capacity of each species. 4.2. Biomagni®cation The BMFs obtained in this study were not very dierent from corresponding factors reported earlier. Muir et al. (1988) found the following BMFs from arctic cod (Boreogadus saida) to (male) ringed seal (Phoca hispida) in a food chain of the Canadian arctic archipelago: BMFPCB=8.8, BMFDDT=20.2, BMFCHL=7.3, BMFHCH=1.5 and BMFCBz=0.2. Furthermore, Tanabe, Tanaka and Tatsukawa (1984) found dierences in tissue concentrations in the myctophid Diaphus suborbitalis and striped dolphin (Stenella coeruleoalba) equivalent to BMFPCB=18.7, BMFDDT=30.8 and BMFHCH=8.4. In a model proposed by Thomann (1989), low elimination rates apply to compounds with log Kow values (Kow is the octanol±water partition coecient) between 5 and 7, and thus, biomagni®cation will occur for these compounds. The individual PCBs determined in the present study have log Kow values between 5 and 8, with log Kow increasing with the degree of chlorination (Mackay, Shiu & Ma, 1992). Furthermore, the DDT and chlordane compounds have log Kow6 (Isnard & Lambert, 1988; Simpson, Wilcock, Smith, Wilkins & Langdon, 1995). For HCB log Kow 6, while the HCH isomers have log Kow4 (Isnard & Lambert, 1988). The low
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octanol±water partition coecients for the HCH isomers could, according to Thomann (1989), partly explain the low/absent biomagni®cation of these compounds in the food chain. In the present study no biomagni®cation was found for HCB from ®sh to harbour seal, due to the low concentrations of HCB in harbour seal. The lower concentrations of HCB in harbour seal, compared to grey seal, may be explained by dierent food preferences (Skeie, 1994). The low BMFs obtained for HCHs and HCB may re¯ect that ®sh bioconcentrate these compounds directly from the sea water, while seals have the capability to metabolise and eliminate them. Bioaccumulation of OCs in ®sh depends on the equilibrium partitioning between body lipids and the surrounding water, with the gill surface playing an important role in this partitioning (Bruggerman, Martron, Kooiman & Hutzinger, 1982). HCHs and HCB constitute the largest proportions of OC in sea water at high latitudes (Barrie et al., 1997). Seals have no respiratory surface in contact with water and, therefore, will not bioconcentrate OCs by this route. 4.3. Patterns of accumulated OCs The present interspecies dierences in patterns of accumulated OCs may be explained by dierent rates of accumulation from the water (bioconcentration) in the case of ®sh, and by the dietary route, especially in the case of seal (Knutzen, Klungsùyr, Oug & Nñs, 1992; Walker, 1990). The patterns also re¯ect dierences in metabolic capability among the species (Boon, Eijgenraam, Everaarts & Duinker, 1989). 4.3.1. PCBs The equilibrium partitioning of OCs between an aquatic organism and the surrounding water can be viewed as an approximate lipid±water partitioning, and can be estimated from the octanol±water partition coecient (Neely, Branson & Blau, 1974). Small individuals will probably reach equilibrium faster than larger individuals because the rate between the respiratory surface and the body volume is larger (Knutzen et al., 1992; Tarr, Barron & Hayton, 1990). Less lipophilic compounds will reach equilibrium ®rst (Hawker & Connell, 1985). Sandeels are smaller than cod (Table 1), and lower chlorinated biphenyls are less lipophilic than higher chlorinated biphenyls. This could explain some of the dierences in PCB congener patterns between sandeels and cod. The interspecies dierences in congener patterns (and segregation in the MDSplot) may also partly be explained by dierent prey preferences. Sandeels feed on planktonic crustaceans, while cod often prefer benthic animals. This may result in cod accumulating higher chlorinated biphenyls to a larger extent through the dietary route than sandeels. Subramanian et al. (1983) also found higher proportions of higher chlorinated biphenyls in bottom-dwelling ®sh than in pelagic zooplanktoneating ®sh. Dierent prey preferences (Skeie, 1994) may also explain some of the dierences in congener patterns found between the two seal species.
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Metabolism of lower chlorinated PCBs and biomagni®cation of highly chlorinated congeners most likely explain the major dierences in PCB patterns between ®sh and seals (Stegeman, 1993). Dierent PCB congeners are metabolised by biotransformation enzymes from dierent subfamilies in the cytochrome P450 system (Goksùyr & FoÈrlin, 1992; Stegeman, 1993). Enzymes of the CYP 1A subfamily biotransform coplanar PCB congeners with vicinal H-atoms in ortho±meta positions (Boon, Reijnders, Dols, Wensvoort & Hillebrand, 1987; Goksùyr & FoÈrlin, 1992; Stegeman, 1993). Mono-ortho substituted PCBs are partly coplanar, but congeners with two or more Cl-atoms in ortho-positions are sterically prevented from having this conformation. In mammals, enzymes of the CYP 2B subfamily catalyse the biotransformation of PCBs by epoxidation in meta±para position and are dependent on free H-atoms (no Cl-substitution) in these positions (Boon et al., 1987; Goksùyr & FoÈrlin, 1992; Stegeman, 1993). The CYP 2B proteins biotransform PCBs regardless of conformation (coplanar or globular). P450 proteins in the liver of several ®sh species may be classi®ed in the CYP 1A subfamily, while only a few have been found to have a close immunological relationship to the mammalian 2B proteins (Stegeman, 1993). Evidence of the presence of CYP 2B-type enzymes in seals is the discovery of methylsulfone metabolites of OCs in these animals (Haraguchi, Athanasiadou, Bergman, Hovander & Jensen, 1992; JanaÂk et al., 1998). The ®nding that mono-ortho substituted congeners (with vicinal H-atoms in ortho±meta positions) and congeners unsubstituted in the meta±para positions constituted lower proportions of PCB in grey seal than in both cod and sandeel, and lower proportions in harbour seal than in cod, is therefore most likely explained by seals having a higher metabolic capacity than ®sh. 4.3.2. DDTs Recording that p,p0 -DDE constituted higher percentages of DDT in the seals than in the ®sh, most likely resulted from higher metabolic capacity in the seals. p,p0 DDT is metabolised to p,p0 -DDE in both ®sh (Addison & Willis, 1978) and seals (Letcher, Norstrom & Muir, 1998). Increasing proportions of DDE, together with decreasing proportions of DDD from ®sh to marine mammals, have also been observed in other food chain studies (Tanabe et al., 1984). Dierences in the relative concentrations of the DDT compounds in sandeel and cod may re¯ect that the relative proportions of these compounds in the environment are changing (Larsson & Okla, 1989). Sandeels will probably respond faster than cod to a change in the relative concentrations of the DDT compounds in sea water due to their smaller size. Dierent prey preferences may also contribute to dierences in the relative proportions of accumulated DDT compounds in sandeel and cod. Sandeels feed on zooplankton, which appear to contain high proportions of p,p0 -DDT compared to p,p0 -DDE (Bildeman et al., 1989; Tanabe et al., 1984). 4.3.3. Chlordanes Higher oxychlordane:trans-nonachlor ratios in seals compared to ®sh are due to a higher capability of seals to metabolise chlordane compounds. Corresponding
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results have also been reported by others (Muir et al., 1988; Nakata, Tanabe, Tatsukawa, Amano, Miyazaki & Petrov, 1995). The most important components of technical chlordane (cis-chlordane, trans-chlordane and trans-nonachlor; Dearth & Hites, 1991) are known to be metabolised to oxychlordane in mammals (Street & Blau, 1972; Tashiro & Matsumura, 1978). 4.3.4. HCHs and HCB a-HCH was found to be the most abundant of the HCH-isomers in all the present species, and this is in accordance with other studies in northern areas (Nakata et al., 1995; Oehme, 1991). Oehme (1991) observed that the a-HCH:g-HCH ratio in ringed seal from the North Sea was approximately 2:1, while the same ratio was more than 20:1 in ringed seal from Svalbard. The annual transport of a- and g-HCH to the Arctic has been modelled by Cotham and Bidleman (1991). They concluded that the import of a-HCH was 7.5 times higher than the import of g-HCH. b-HCH constituted higher percentages of HCH in the seals than in cod, thus re¯ecting the high persistence of this isomer (Xu, Wu, Zhang, Staudacher, Kettrup & Steinberg, 1994), which gives it a high bioaccumulative potential (Baumann, Angerer, Heinrich & Lehnert, 1980). These ®ndings are also in accordance with other observations of HCHs in ®sh and sea mammals (Nakata et al., 1995; Tanabe et al., 1984). It is dicult to explain our ®nding that sandeels had accumulated remarkably larger percentages of b-HCH (34.5% of HCH) than all the other species. Highly developed capability to metabolise the other HCH-isomers is unlikely, but cannot be ruled out. Due to their relatively smaller size, sandeels may also have bioconcentrated b-HCH from the environment to a larger extent than cod. b-HCH has reached the environment from the usage of technical HCH (BHC), which contains 5±14% of this isomer (Li, McMillan & Scholtz, 1996). Technical HCH has been used to protect crops in the former Soviet Union (Li et al., 1996), and in Lake Baikal seals and ®sh have been found to contain elevated proportions of b-HCH (Nakata et al., 1995). HCH and HCB constituted higher proportions of the total OCs (OC) in ®sh, as compared to seals, and this probably results from continuous bioconcentration of these compounds from sea water through the gill epithelium in ®sh, while the seals to a larger extent metabolise and eliminate them. HCHs and HCB constitute the largest proportions of OC in arctic sea water (Barrie et al., 1997). HCH also constituted higher proportions of OC in sandeel than in cod, probably because sandeels have bioconcentrated HCHs to a larger extent, due to their relatively smaller size. It is also possible that sandeels have received more HCHs through their zooplankton diet, which contains elevated amounts of HCHs, relative to other OCs (Bidleman et al., 1989). 5. Conclusions The biomagni®cation factors calculated for the present food chain show that the concentrations of the OCs generally increase with trophic level. The highest BMF
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(36.9) was found for DDT from sandeel to harbour seal. HCH and HCB, however, are not biomagni®ed to a similar extent. The low BMFs obtained for HCH and HCB suggest that ®sh continuously bioconcentrate these compounds, while seals have a good capability to metabolise and eliminate them. HCH and HCB constituted higher proportions of OC in ®sh than in seals, probably for the same reasons. The compositional patterns of all the accumulated OCs diered among the species. Our observations suggest that the bioaccumulation mechanisms at lower trophic levels (®sh) depend primarily on physicochemical factors, such as the water solubility and lipophilicity of the pollutants. At higher trophic levels (seals), the bioaccumulation mechanisms are primarily aected by biochemical factors, such as the metabolic capacity of the organisms. In addition, prey preference may in¯uence the patterns of accumulated pollutants in all the species examined. Acknowledgements We thank the hunter Steinar Magnussen for help with collecting the material. Appreciation is also expressed to the following persons for help and enjoyable company during the work: Paul Eric Aspholm, Signe Haugen, Anuschka Polder, Vidar Berg, Erna Stai, Elisabeth Lie, Siri Fùreid, Lars Kleivane and Hñge Krogh. Thanks also to Jonathan Edward Colman and Jane Indrehus for proof-reading the manuscript. References Addison, R. F. (1982). Organochlorine compounds and marine lipids. Progress in Lipid Research, 21, 47±71. Addison, R. F., & Willis, D. E. (1978). The metabolism by rainbow trout (Salmo gairdnerii) of p,p0 [14C]DDT and some of its possible degradation products labeled with 14C. Toxicology and Applied Pharmacology, 43, 303±315. Anon. (1995). Report on the results of the ICES/IOC/OSPARCOM intercomparison programme on the analyses of chlorobiphenyls in marine media-step 2 (Cooperative Research Report No. 207). ICES, Copenhagen. Ballschmiter, K., & Zell, M. (1980). Analysis of polychlorinated biphenyls (PCB) by glass capillary gas chromatography. Composition of technical Aroclor± and Clophen±PCB mixtures. Fresenius' Zeitschrift fuÈr analytische Chemie, 302, 20±30. Barrie, L. Macdonald, R., Bidleman, T., Diamond, M., Gregor, D., Semkin, R., Strachan, W., Alaee, M., Backus, S., Bewers, M., Gobeil, C., Halsall, C., Ho, J., Li, A., Lockhart, L., Mackay, D., Muir, D., Pudykiewicz, J., Reimer, K., Smith, J., Stern, G. Schroeder, W., Wagemann R., Wania F., & Yunker, M. (1997). Sources, occurrence and pathways. In J. JensenK. AdareK. & R. Shearer, Canadian Arctic Contaminants Assessment Report (pp. 25±182). Ottawa: Indian and Northern Aairs Canada. Baumann, K., Angerer, J., Heinrich, R., & Lehnert, G. (1980). Occupational exposure to hexachlorocyclohexane. I. Body burden of HCH-isomers. International Archives of Occupational and Environmental Health, 47, 119±127. Bernhoft, A., & Skaare, J. U. (1994). Levels of selected individual polychlorinated biphenyls in dierent tissues of harbour seals (Phoca vitulina) from the southern coast of Norway. Environmental Pollution, 86, 99±107. Bernhoft, A., Wiig, é., & Skaare, J. U. (1997). Organochlorines in polar bears (Ursus maritimus) at Svalbard. Environmental Pollution, 95, 159±175.
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