Simonetta Corsolini,*, † Kurunthachalam Kannan, ‡ Takashi Imagawa, §, Silvano Focardi, †, and John P Giesy ‡
Dipartimento di Scienze Ambientali, Universita` di Siena, I-53100 Siena, Italy, National Food Safety and Toxicology Center, Michigan State University, East Lansing, Michigan 48824, and National Institute for Resources and Environment, 16-3 Onogawa, Tsukuba 305-8569, Japan
* Corresponding author phone: ++39 0577 232939; fax: ++39 0577 232806; e-mail: corsolini@unisi.it. Corresponding address: Dipartimento di Scienze Ambientali, Universita` degli Studi di Siena, Via delle Cerchia, 3-53100 Siena, Italy. † Universita` di Siena. ‡ Michigan State University. § National Institute for Resources and Environment.
Here we report accumulation patterns of polychlorinated naphthalenes (PCNs), polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), polychlorinated biphenyls (PCBs), and pesticides (HCB, p,p'DDE) in polar organisms (polar bear from Alaskan Arctic and krill, sharp-spined notothen, crocodile icefish, Antarctic silverfish, Adélie penguin, South polar skua, and Weddell seal from the Ross Sea, Antarctica). PCNs, found in most of the samples, ranged from 1.5 pg/g in krill to 2550 pg/g in South polar skua on a wet weight basis. Lower chlorinated PCNs were the predominant congeners in organisms except skua and polar bear that showed similar PCN homologue patterns. PCDD/F concentrations were <90 pg/g wet wt in polar organisms; PCDD congeners showed peculiar accumulation patterns in different organisms. Correlation existed between PCN and PCB concentrations. PCB, HCB, and p,p'DDE levels were the highest in skua liver (11150 ng/g wet wt, 345 ng/g wet wt, and 300 ng/g wet wt, respectively). Contribution of PCNs to 2,3,7,8- tetrachlorodibenzo-p-dioxin equivalents (TEQ) was negligible (<0.1%) because of the lack of most toxic congeners. The highest TEQ was found in South polar skua liver (45 pg/ g, wet weight). This is the first study to document the occurrence of PCNs in Antarctic organisms. High levels of dioxin-like chemicals in skua suggest the importance of intake via diet and migration habits, thus POP detection can be useful to trace migration behavior. Moreover, POP concentrations in penguin and skua eggs prove their transfer from the mother to eggs.
Introduction
Polar regions were considered to be pristine until the contamination by anthropogenic compounds was documented in the 1960s and 1970s (1, 2). Since then, there is a continuing concern about the potential effects of persistent organic pollutants (POPs) on polar environments. Arctic and Antarctic are both remote polar regions. While the former is a perennial frozen sea surrounded by continents, the latter is a snow covered continent surrounded by ocean. Apart from geographical features, several factors such as proximity to sources and physicochemical properties of POPs may determine their occurrence and deposition in those regions. Oceans are a major sink for persistent chemicals, which are transported from continental areas by atmospheric and oceanic currents (3-6). The Southern Ocean isolates Antarctica from the other oceans, therefore volatile contaminants can reach Antarctica only via the transport of air mass. Furthermore, the southern hemisphere is mainly occupied by oceans, and land is relatively less populated than the northern hemisphere. It is therefore expected that Arctic and Antarctic organisms show a different pattern of contamination by POPs. Global contamination and decreasing levels of polychlorinated biphenyls (PCBs) and organochlorine pesticides from the northern to the southern hemisphere are well documented (5-9). Global distillation or fractionation by condensation in cold polar environments has been proposed as a mechanism whereby the polar regions may become sinks for some POPs (7).Dueto the low temperatures and winter darkness, POP degradation is very slow in the polar regions. Ice can entrap POPs for a longer period and release them in the environment through ice melting (10) where they enter the trophic webs, bioaccumulate in the tissues of organisms, and biomagnify (9). Migratory animals (South Polar skua and other seabirds, whales) are another source of pollutants in polar regions with their excrements and carcasses.
Most volatile compounds are expected to travel from tropics and other source-areas to polar regions. POPs are industrial and agricultural chemicals that exhibit several common properties such as high lipophilicity and high environmental stability. Moreover, they elicit a variety of short and long-term toxic responses in organisms including humans (11-13). Among them, PCNs are a group of 75 compounds based on the naphthalene ring system (C10H8-nCln, n ) 1-8) where chlorine atoms may substitute one to eight hydrogens. Because of their good electrical properties, weather resistance, low flammability, high chemical, and thermal stability, they were produced and used since the 1930s. They are also byproducts of combustion and chlorinating processes (14). The release and distribution of PCNs in the environment and their global transport are still not well-known; apart from production and use of technical mixtures, chloralkali plants, magnesium refineries, and waste incinerators are other sources of PCNs (14, 15). As PCNs are microcontaminants in technical PCB mixtures (16), they are released into the environment through the use of PCBs and therefore likely to be transported together, having almost the same physical and chemical properties (14). PCNs bioaccumulate in organisms, and they have been detected in tissues from many areas of the world (i.e. refs 15, 17, and 18). Their bioconcentration factors (BCFs) are moderate to high depending on the chlorinating level and log BCF ranges up to 4.53 in several species of fish (17).
In this study, concentrations of polychlorinated naphthalenes (PCNs), polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), polychlorinated biphenyls (PCBs), and two pesticides, hexachlorobenzene (HCB) and p,p'DDE, were measured in tissues of polar bear from Alaskan Arctic and krill, sharp-spined notothen, crocodile icefish, Antarctic silverfish, Adélie penguin, South polar skua, and Weddell seal from the Ross Sea, Antarctica.
FIGURE 1. Sampling locations.
Materials and Methods
Sample Collection. Samples of polar bear (Ursus maritimus) livers were collected from the tissues archived by the U.S. Fish and Wildlife Service, Anchorage, AK. Krill (Euphausia superba), fish (Trematomus pennelli, Chionodraco hamatus, Pleuragramma antarcticum), Adélie penguin (Pigoscelys adeliae), South polar skua (Catharacta maccormicki), and Weddell seal (Leptonichotes weddelli) were collected from the Ross Sea (Antarctica) in Terra Nova Bay, during the X (1994/1995) and XI (1995/96) Italian Expeditions. Information on the sampling sites, methods, and biometric data are given (Figure 1 and Table 2; see Table 1, Supporting Information).
Chemical Analysis. PCNs, PCBs, and 2,3,7,8-substituted congeners of PCDDs and PCDFs were analyzed following the method described elsewhere (19). Tissues of polar bear, Weddell seal and skua, whole eggs of penguins, and whole body of krill and fishes were homogenized with sodium sulfate and Soxhlet extracted with methylene chloride and hexane (3:1, 400 mL) for 16 h. The extract was rotary evaporated at 40 °C, and an aliquot was used for the determination of fat content by gravimetry. The remaining extract was spiked with 13C-TCDD, 13C-TCDF, 13C-OCDD, and 13C-OCDF as internal standards and interferences removed by fractionation with multilayer silica gel column. The multilayer silica gel column was prepared by packing a glass column (20mm i.d.) with a series of layers of silica gel in the following order: 2 g of silica, 6 g of 40% acidic-silica, 2 g of silica, and a thin layer of sodium sulfate at the top. The column was cleaned with 150mLof hexane prior to the transfer of sample extracts. Samples were then eluted with 200 mL of hexane and rotary evaporated to 5 mL. A portion of the aliquot was taken for the analysis of PCB congeners other than non-ortho coplanar PCBs. The remaining samples were passed through a glass column (10mm i.d.) packed with1gof silica gel impregnated carbon (Wako Pure Chemical Industries, Tokyo, Japan) for the separation of ortho-substituted PCBs from PCNs and PCDD/DFs. The first fraction, which was eluted with 150 mL of hexane contained major PCB congeners, which interfere with the analysis of PCNs and PCDDs/DFs. The second fraction, which was eluted with 200 mL of toluene contained non-ortho substituted PCB congeners (77, 126, and 169), PCNs and PCDDs and PCDFs.
TABLE 2. Details of Samples Analyzed j
sample common name sampling method tissue sex/age body wt(g) length (mm) n
Weddell seal ba found dead blubber adult nd nd 1
Weddell seal l liver 1
krill b bioness wholebody 52% female 0.6 (av) 42 (av) pool c
crocodile icefish 3d gill net homogenate adult 299 nd 1
crocodile icefish 4 gill net homogenate adult 270 nd 1
sharp-spined notothen 1e gill net wholebody adult 81 nd 1
sharp-spined notothen 2 gill net wholebody adult 61 nd 1
silverfish 1f bioness muscle nd/adult 14.3 135 1
silverfish 4 bioness muscle nd/adult 13.4 132 1
silverfish 5 bioness muscle nd/adult 51 189 1
adélie penguin g found unhatched egg 5
south polar skua h found unhatched egg 5
south polar skua l found dead liver adult nd nd 1
south polar skua m muscle 1
polar bear 7,8,9,10,11i sacrified liver nd/adult nd nd 5
a Diet: fish, including D. mawsoni, Trematomus, P. antarcticum, cephalopods, krill, zooplankton, decapods.
b Diet: ice-attached phyto- and zooplanktons, invertebrate eggs, its own species.
c Pool of whole specimens, total wt ) 20, 22 g.
d Diet: fish, krill.
e Diet: benthic feeder (fish eggs, polychaetes, amphipods and molluscs).
f Diet: eggs and larvae of copepods and euphausiids, polychaetes, chaetognaths, larger items are ingested
with increase in size. g Diet: plankton, fish, krill.
h Diet: fish, krill, eggs and chicks of penguins, other small birds.
i Diet: seals, carcasses of cetaceans.
j nd=not detected, av=average, b=blubber, l=liver, m=muscle.
Identification and Quantification. PCB congeners were identified and quantified using a gas chromatograph (Perkin-Elmer series 600) equipped with 63Ni electron capture detector (GC-ECD), following a method described elsewhere (19). A fused silica capillary column coated with DB-5MS [(5%- phenyl)-methylpolysiloxane, 30 m × 0.25 mm i.d.; J&W Scientific, Folsom, CA, U.S.A.] having a film thickness of 0.25 µm was used. PCB congeners were identified against a standard mixture containing 100 congeners of known composition and content. Further details of PCB analysis are reported elsewhere (19, 20). Identification and quantification of individual PCN and PCDD/DF congeners were accomplished with a Hewlett-Packard 6890 series high resolution gas chromatograph (HRGC) coupled to a JEOL JMS-700 high-resolution mass spectrometer (HRMS). PCN congeners, hepta- and octa-chlorodibenzo-p-dioxins and furans, and non-ortho coplanar PCBs were separated by DB- 1701. Tetra- through hexachlorodibenzo-p-dioxinsandfurans were separated by a capillary column coated with SP-2331. The column oven temperature was programmed from 80 to 160 °C at a rate of 40 °C/min and then to 170 °Cat 10 °C/min, to 250 °C at 4 °C/min and then to 296 °C at 8 °C/min with a final hold time of 10 min. Injector and transfer line temperatures were held at 260 and 250 °C, respectively. Helium was used as the carrier gas. The mass spectrometer was operated at an electron impact (EI) energy of 70 eV. PCN and dioxin congeners were determined by selected ion monitoring (SIM) at the two most intensive ions of the molecular ion cluster. A mixture of Halowaxes 1001, 1014, and 1051 containing all the tri- through octachloronaphthalenes was used as a standard for the quantification of PCNs. PCDD and PCDF congeners were quantified by comparing individually resolved peak areas to the corresponding peak areas of the standards. Recoveries of 13Clabeled PCDDs/DFs, which elute in the second fraction containing PCNs and non-ortho coplanar PCBs, were 77- 95%. Reported concentrations were not corrected from the recoveries of internal standard. Recoveries of PCB, PCN, PCDD, and PCDF congeners through the analytical procedure were between 90 and 100%. Procedural blanks were analyzed through the whole analytical procedure to check for interferences. The detection limits of individual PCN and PCB congener varied depending on the sample mass, response factor, and interference. Generally, detection limit for individual congeners was 1-75 pg/g, on a wet weight basis. Detection limits of PCDD and PCDF congeners varied from 0.3 pg/g, wet weight to 25 pg/g, wet weight, depending on the samples. Quality control criteria for positive identification of target compounds include signal-to-noise ratio over three, isotope ratios of the two monitored ions for each compound within 15% of the theoretical chlorine values and the compound should elute at the same GC retention time as the standards. PCN and PCB congeners are represented by their IUPAC numbers throughout this manuscript.
Results and Discussion
Results are shown in Tables 3-5 and are given on a wet weight basis; lipid content of the tissues analyzed is reported in Table 3.
Polychlorinated Naphthalenes. PCNs were found in most of the samples analyzed (Table 3). Mean concentration in the livers of polar bear was 370 ( 390 pg/g wet weight. The highest PCN concentration of 2550 pg/g was found in the liver of South polar skua. PCNs were also detected in other Antarctic organisms including krill, which are at the lower trophic level in the food web. Concentrations (on a wet weight basis) of PCNs were 1.5 pg/g in krill, 1.3-2.8 pg/g in the sharp-spined notothens, 2.1-4.7 pg/g in icefishes, 86 pg/g in silverfish, and 77 pg/g and 44 pg/g in the Weddell seal blubber and liver, respectively (Table 3). Generally, concentrations of PCNs were greater in polar bear liver than in Weddell seal but less than that in skua. The concentrations tend to be great in predatory animals such as Weddell seal, skua, and polar bear, suggesting biomagnification in the polar food webs. Polar bear and skua show different feeding habits, the former is a specialized top predator feeding on marine mammals (21), while the latter is an opportunistic omnivorous species. The relationship between feeding habits and xenobiotic-metabolizing enzyme system activities has already been suggested (22). It may be responsible of the differences existing in the accumulation patterns both between them and the other Antarctic organisms.
TABLE 3. Concentration of PCNs, HCB, pp'DDE, and PCBsa
lipids(%) SPCNs HCB p,p'DDE SPCBs krill 1.5 1.5 0.2 <0.1 1.9 icefish 3 1.4 2.1 0.4 0.3 4.2 icefish 4 3.9 4.7 <0.1 <0.1 12.6 notothen 1 2.2 2.8 7.8 2.9 175 notothen 2 1.6 1.3 3.9 3.8 111 silverfish 9.4 86 4.4 0.3 138 seal blubber 100 77 0.8 17 395 seal liver 2.7 44 0.1 1.2 34 penguin eggs- average (min-max) 10.5(7.7-12.8) NA <0.1 <0.1 2.8(1.3-5.1) skua eggs- average (min-max) 9.1(4.5-13.9) NA <0.1 <0.1 155(88-222) skua liver 42 2550 345 300 11150 skua muscle 1.7 97 168 129 2630 polar bear - average (min-max) 11.4(7.8-14.9) 370(<0.1-945) 16(1.1-50) 13(2.9-28) 2110(523-5129) bear (SD) 2.6 390 20 9.6 1874 a Concentrations are expressed in ng/g wet weight for PCBs, p, p˘-DDE, and HCB, pg/g wet weight for PCNs; NA ) not analyzed; min-max ) minimum and maximum values; SD ) standard deviation.
TABLE 4. Concentration of the Coplanar PCB, PCN,a TCDD, and TCDF Congeners and TEQsb,c in Krill and Fish from the Ross Sead
krill icefish 3 icefish 4 notothen 1 notothen 2 silverfish 33˘44˘-TCB 4.4 3 1.1 4.1 1.8 4 33˘44˘5-PCB 3.3 1 1 1.4 Int 3 33˘44˘55˘-HCB <1 5 <1 <5 <2 <0.001 SNonortho PCBs 7.7 9 2.1 5.5 1.8 7 12357/12467-PCNs 0.446 <0.1 0.996 <0.1 <0.1 <0.1 12456-P5CN <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 12367-P5CN <0.1 <0.1 <0.1 <0.1 <0.1 2.33 12378-P5CN <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 123467/123567-H6CNs <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 123457/123568-H6CNs <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 123578-H6CN <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 123456-H6CN <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 123678-H6CN <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 1234567-H7CN <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 SPCNs 1.5 2.1 4.7 1.3 2.8 86 2378-T4CDD <0.1 <0.036 <0.041 <0.156 <0.065 0.242 12378-P5CDD <0.306 0.146 1.4 <0.156 <0.065 4.069 123478-H6CDD <0.043 <0.036 <0.041 <0.156 <0.065 <0.081 123678-H6CDD <0.043 <0.036 <0.041 <0.313 <0.065 <0.081 123789-H6CDD <0.043 <0.036 <0.041 <0.313 <0.065 <0.081 1234678-H7CDD 1.5 1.8 <0.204 <0.234 <0.100 <0.161 O8CDDs 0.919 <0.109 <0.041 2.057 <0.100 <0.081 SPCDD 2.9 2.2 1.8 3.4 0.5 4.8 2378-T4CDF <0.085 <0.073 <0.122 <0.156 <0.065 0.565 12378-P5CDF <0.043 <0.036 <0.122 <0.078 <0.065 <0.161 23478-P5CDF <0.043 <0.036 <0.122 <0.078 <0.065 <0.161 123478-H6CDF <0.085 <0.109 <0.881 <1.688 <0.065 <0.081 123678-H6CDF <0.085 <0.109 <0.881 <1.688 <0.065 <0.081 123789-H6CDF <0.085 <0.109 <0.881 <1.688 <0.065 <0.081 234678-H6CDF <0.085 <0.109 <0.881 <1.688 <0.065 <0.081 1234678-H7CDF 1.531 <0.182 <0.163 <0.313 <0.1 <0.969 1234789-H7CDF 1.531 0.292 <0.122 <0.234 <0.1 <0.969 O8CDF <0.001 <0.109 <0.122 <0.100 <0.1 2.018 SPCDFs 3.6 1.2 4.3 7.7 0.7 5.2 STEQs <2 average <4 average <5 <23 aPCN congener concentrations are reported only for those which elicit dioxin-like activity, while SPCNs includes all detected congeners. STEQs: sum of TEQ of the congener listed in the table. c Concentrations are expressed in pg/g wet weight; Int=severe interference. d For total PCDD summation, nondetectable congeners were assigned a value of detection limit.
TABLE 5. Concentration of the Coplanar PCB, PCN,a TCDD, and TCDF Congeners and TEQsb,c in Arctic and Antarctic Birds and Mammalsd
seal seal skua skua bear
blubber liver eggs penguin skua eggs liver muscle average (min-max)
33'44'-TCB 10.2 4.1 209 29 4(3-6)
33'44'5-PCB 29 3.1 565 78 10.3(4-22)
33'44'55'-HCB 12 3.8 678 91 89(9-403)
SNon-ortho PCBs 51 11 <0.001 <0.001 1453 198 104(16-431)
12357/12467-PCNs <0.1 <0.1 224 40 46(42-49)
12456-P5CN 19.8 <0.100 26 <0.1 36(23-50)
12367-P5CN <0.1 27 31 <0.1 82(9.2-213)
12378-P5CN <0.1 <0.1 n.d. <0.1 35(35-35)
123467/123567-H6CNs <0.1 <0.1 24 4.1 <0.1
123457/123568-H6CNs <0.1 <0.1 <0.1 <0.1 4.1(4.1-4.1)
123578-H6CN <0.1 <0.1 <0.1 <0.1 <0.1
123456-H6CN <0.1 <0.1 <0.1 <0.1 <0.1
123678-H6CN <0.1 <0.1 <0.1 <0.1 <0.1
1234567-H7CN <0.1 14 <0.1 7.6 <0.1
SPCNs 77 44 2550 97 370(<0.1-945)
2378-T4CDD 1.54 0.169 3.9 0.255 0.52(<0.1-1.2)
12378-P5CDD 0.306 27 3.9 1.8 0.463(<0.1-0.938)
123478-H6CDD 0.458 0.846 1.1 0.255 1.08(<0.1-3.7)
123678-H6CDD 0.458 0.846 1.3 0.255 1.05(<0.1-3.7)
123789-H6CDD 0.458 0.846 1.083 0.34 1.7(<0.1-3.7)
1234678-H7CDD 0.153 1.3 9.1 0.255 2.1(0.469-8.7)
O8CDDs 0.306 0.508 10.6 0.17 1.6(0.172-3.7)
SPCDD 3.7 31 0.4(0.1-0.9) 6.5(2.5-12.1) 31 3.4 8.5(4.1-22)
2378-T4CDF 12.1 6.1 19.8 3.1 0.303(<0.1-0.513)
12378-P5CDF 0.458 0.169 3.9 0.085 0.76(<0.1-1.7)
23478-P5CDF 0.611 0.169 27 1.96 1.2(<0.1-3.69)
123478-H6CDF 0.458 0.508 0.722 0.255 1.6(<0.1-3.7)
123678-H6CDF 0.458 0.508 24 0.255 1.6(<0.1-3.7)
123789-H6CDF 0.611 0.508 0.722 1.8 1.6(<0.1-3.7)
234678-H6CDF 0.917 0.508 0.722 1.8 1.6(<0.1-3.7)
1234678-H7CDF 0.458 1.2 0.181 0.595 2.8(0.344-8.7)
1234789-H7CDF 0.611 1.2 0.361 0.51 2.3(0.344-8.7)
O8CDF 0.458 1.01 9.1 4.23 3.5(<0.1-6.1)
SPCDFs 17 12 1.8(1.1-2.6) 13(6.5-31) 87 15 17(4-28)
STEQs 17 18 5 38 45 18 16(<0.1-21)
a PCN congener concentrations are reported only for those which elicit dioxin-like activity;
SPCNs includes all detected congeners.
b STEQs: sum of TEQ of the congener listed in the table.
c Concentrations are expressed in pg/g wet weight.
d For total PCDD summation, nondetectable congeners were assigned a value of detection limit.
Our results suggest widespread distribution of PCNs in remote marine environments and a contamination level slightly lower than in organism from other locations than Antarctica. In fact, concentrations of total PCNs in some species from different sites varied between few parts per billion (ppb) to hundreds ppb (Table 6, Supporting Information). For example, they were 13-320 ng/g, lipid weight, in tissues of fishes from the Baltic Sea (17) and in the ranges of 84-220 ng/g on a lipid weight basis in guillemot from Sweden (15). Double-crested cormorants and herring gulls from the Great Lakes (0.38-2.4 ng/g wet wt and 0.083-1.3 ng/g wet wt, respectively) contained greater chlorinated PCNs such as tetra-, penta-, and hexa-CNs (23). Isomer composition of PCNs in polar bears and in South polar skua tissues was predominated by higher chlorinated congeners: penta-CNs > tetra-CNs > hexa-CNs (Figure 2). It is interesting to note that the pattern of PCN homologues in polar bear and South polar skua was similar, which might be due to the exposure of skua to PCNs in its wintering grounds. South Polar skua, which nests in the Ross Sea are reported to migrate to the Northern Pacific Ocean to overwinter, making a clockwise loop migration around the Pacific Ocean--Japan, British Columbia, Washington, California (24-26). Adults tend to remain in more Southerly latitudes even at the edge of the Winter pack ice (27), while sightings of young birds are reported in the North Pacific regions and American coasts (26), where they can get exposed to contaminants. Polar bear shows a good capacity to eliminate persistent organochlorine compounds introduced by food (28), in particular hexa- and heptachlorobiphenyls and 2,5- or 2,5,6-chlorine substituted congeners (21). These findings are consistent with our results; polar bear of this study showed a higher concentration of penta-CBs compared to hexa- and hepta-CBs. PCNs show similar properties to PCBs thus they may behave similarly. Interestingly, the patterns of PCNs in polar bear and South polar skua were similar and were different with respect to the other Antarctic organisms. In other Antarctic organisms, PCN homologue pattern was dominated by tri-, tetra-, or penta-CNs (Figure 2). Lower chlorinated PCNs are more volatile and can reach polar regions by atmospheric transport. Moreover, PCNs are found in commercial PCB mixtures (16); therefore, it is likely that they are transported together by air masses; correlation existed between concentrations of PCBs and PCNs in the samples analyzed (r)0.98). The PCN profile observed in polar organisms is different from those observed in animals from point source areas such as the North American Great Lakes (19). Concentrations of PCNs in polar organisms is much less than in organisms from other parts of the world. The pattern of PCN profiles in technical mixtures vary (29) (Figure 2). The observed patterns in biota suggest transfer of low-chlorinated PCNs to Antarctica.
Other Dioxin-like Compounds. PCDD/F congener concentrations in lower trophic Antarctic organisms were less than the limits of detection; PCDD/F congeners with detectable concentrations were found in livers of skua and polar bear (Tables 4 and 5). SPCDDs/Fs were 31-87 pg/g, wet weight, in South polar skua liver, 8.5 and 17 pg/g wet weight (4-28 pg/g wet wt) in polar bear liver, respectively. PCDD/F congener traces were also found in skua and penguin eggs (Table 5). The higher concentration of SPCNs, SPCDDs/Fs, and coplanar PCBs in predator animals (seal, skua, and bear) with respect to krill and fish, that occupy a lower trophic level, may confirm the existence of biomagnification processes although all the analyzed animals do not belong to the same trophic web. Results were homogeneous in fish and krill, even if concentrations in the latter were quite high despite their low position in the trophic web, likely due to their high lipid content (9). PCNs showed an anomalous high value in silverfish, but species-specific differences might be due to different metabolism, lipid composition of tissues or feeding habits. Lipid composition may be responsible for the higher PCDD concentration in seal liver compared to the blubber as for the 1,2,3,7,8-P5CDD that was the highest in seal liver (27 pg/g wet wt). Its value was 3.9 pg/g wet wt in skua liver, while the opposite pattern was observed for the O8CDD (10.6 pg/g wet wt in skua liver and 0.508 pg/g wet wt in seal liver). Anyway the number of samples analyzed was low. Further studies are needed to better understand the POP accumulation in Antarctic species, even because, for example, the 1,2,3,7,8-P5CDD is considered as toxic as the most toxic 2,3,7,8-T4CDD. Levels in polar bear and skua are of the same order of magnitude as in double crested cormorants and herring gull from the polluted Great Lakes (23). Research bases in Antarctica may contribute to PCDD/F contamination through incineration activities (30), although atmospheric transport from other continents is thought to be the major source.
FIGURE 2. PCN isomers pattern in the polar organisms and in some PCN technical mixtures. The graph shows the percentage contribution of each class of isomers to the total PCN residue; the respective concentrations are given in the table (pg/g wet wt for organisms, Ěg/g for technical mixtures; data of technical mixtures are by Yamashita et al. ( 16)).
Tri-CN Tetra-CN Penta-CN Heaxa-CN Hepta-CN Octa-CN seal blubber 24 n.d. 53 n.d. n.d. n.d. seal liver 12 5.8 27 n.d. n.d. n.d. krill 0.8 0.2 0.45 n.d. n.d. n.d. icefish 3 n.d. n.d. 2.1 n.d. n.d. n.d. icefish 4 0.8 n.d. 3.9 n.d. n.d. n.d. polar bear n.d. 39 329 2.9 n.d. n.d. skua liver 2.2 211 2308 24 7.6 n.d. skua muscle n.d. 34 59 4.1 n.d. n.d. notothen 2 1.3 n.d. n.d. n.d. n.d. n.d. notothen 1 2.04 0.8 n.d. n.d. n.d. n.d. silverfish 43 23 6.5 n.d. 14 n.d. Aroclor1260 0.02 0.1 0.3 1.2 10 55 KC-300 0.3 9 17 4.5 1 0.4 Phenoclor 4 0.9 55 258 135 8.4 2.3
Mean PCB concentrations in polar bear livers were 2110 (range: 523-5129) ng/g wet weight (Table 3) and fall within the same ranges reported for the fat of Arctic polar bears from other locations including the Canadian Arctic (31). In the Antarctic organisms, the highest concentration of PCBs was found in South polar skua tissues, with a maximum of 11 150 ng/g and 2630 ng/g, wet weight, in liver and muscle, respectively. Among the other Antarctic organisms, PCBs concentrations decreased with trophic level of the food web. PCBs concentrations were 395 ng/g in the Weddell seal blubber, 138 ng/g in silverfish, 111-175 ng/g in sharp-spined notothen, 4.2-12.6 ng/g in crocodile icefish, and 1.9 ng/g in krill. PCB concentrations in penguin and South polar skua eggs were 2.8 and 155 ng/g wet weight, respectively. South polar skuas that nest on the coasts of the Ross Sea spend about 4 months in Antarctica and then migrate north to overwinter in the sub-Antarctic or North Pacific regions (24- 26), that are relatively more contaminated than Antarctic. Therefore, great concentrations of PCBs in migrating South polar skua might be due to high position in trophic webs and feeding habits and to exposure in wintering grounds. PCB concentration in Weddell seal blubber was slightly less than the previously reported value of 585 ng/g, wet weight (8). Nevertheless, PCB concentrations in South polar skua liver were much greater than those reported earlier (8). This suggests that Antarctic birds wintering in sub-Antarctic or North Pacific Islands carry heavy burdens of PCBs from their wintering grounds, and PCB exposures continue to be of concern despite the ban on production of PCBs in several developed countries in the northern hemisphere. POP concentrations in skua tissue might be a tool to obtain or confirm investigation on their migration habits; specimens that overwinter in sub-Antarctic regions can show lower POP levels compared to those that migrate to the polluted Northern hemisphere.
We also report here HCB and pp'DDE levels. Concentrations of HCB and pp'DDE in polar bear livers were 16 ng/g wet wt and 13 ng/g wet wt; highest levels were detected in skua liver, 345 ng/g wet wt and 300 ng/g wet wt. In the other Antarctic organisms HCB and pp'DDE were <0.1-7.8 ng/g wet wt and<0.1-17 ng/g wet wt, respectively (Table 3).HCB showed a higher concentration than pp'DDE in all the organisms except the seal and this trend is different from organisms from other locations (5, 6). DDE has a higher bioconcentration potential (log BCF ) 4.7 in fish) compared to the HCB (log BCF ) 3.1-4.5 in fish) but is more volatile and easily transported by air masses (HCB and pp'DDE vapor pressure are 1.8×10-6 and 1.7×10-8 atm, respectively) (32). Therefore fish-eating seabirds may accumulate a greater amount of HCB than pp'DDE, that might be lesser available to organisms in cold polar region. A similar phenomenon has already been described for HCHs; Lakaschus et al. (33) reported a strong latitudinal gradient of HCHs with higher concentration in the Northern hemisphere. Ice can be a trap for those chemicals such as HCHs and HCB and can release them during melting (33, 34) as well as PCBs (10).
Toxic Potential. The relative toxic potential of PCNs, PCDDs, PCDFs, and coplanar PCBs in polar organisms was calculated by using the Toxic Equivalency Factor (TEF) approach (11); H4IIE-assay specific relative potency values of PCNs and PCBs reported earlier (23, 35) were used. Contribution of SPCNs to TEQs was negligible in polar organisms (<0.1% in skua, 0.2% in polar bear, 0.0003% in seal, 0.3% in silverfish, 0.0004% in krill, 0% in notothen, and 0.0006% in icefish), because of the lack of toxic higher chlorinated congeners 123456, 123578, and 123678 (IUPAC nos. 63, 69, and 70) (Tables 4 and 5). The highest STEQ concentration was found in South polar skua liver and eggs (45 and 38 pg/g, wet weight), then in Weddell seal blubber (18 pg/g) and polar bear (16 pg/g). TEQ values in the other Antarctic organisms and in penguin eggs were less than 5 pg/g, wet weight (Table 4), except silverfish (23 pg/g wet wt). These TEQ values are 1-2 orders of magnitude lower than those considered to elicit toxicological effects in birds and marine mammals (36, 37). Organochlorine concentrations in polar animals indicate that top level predators in the food web such as polar bear and South polar skua are exposed to considerable levels of these compounds. Differences in POP levels and patterns suggest differences in metabolism, feeding habits, and trophic position. Interestingly, levels of different classes of POPs increase uniformly supporting the hypothesis that they reach Antarctica depending on their physicochemical properties (7) and from there on biomagnify (9, 38).
Our results confirm widespread global distribution of PCNs, PCBs, dioxins, and furans. High levels of dioxin-like chemicals in South polar skua suggest the importance of intake via diet and migration habits. POP levels in tissues of Antarctic seabirds and marine mammals can be useful to trace their migration behavior. Moreover, the detection of POPs in seabird eggs including penguin and South polar skua eggs prove their transfer from the mother to eggs, thereby exposing the future generations.
Acknowledgments
This research was funded by the Italian Antarctic Research Program (PNRA).
Supporting Information Available
Collection of samples (Table 1) and concentration of polychlorinated naphthalenes in organisms from different locations (Table 6). This material is available free of charge via the Internet at http://pubs.acs.org.
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Received for review January 8, 2002. Revised manuscript received May 29, 2002. Accepted June 4, 2002.
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