Environ. Sci. Technol. 2007, 41, 3829-3835
Residues of Persistent Organochlorine Contaminants in Southern Elephant Seals (Mirounga leonina) from Elephant Island, Antarctica KLEBER C. MIRANDA-FILHO,† TRACY L. METCALFE,‡ CHRIS D. METCALFE,‡ RICARDO B. ROBALDO,§ MO ˆ NICA M. C. MUELBERT,† ELTON P. COLARES,§ PABLO E. MARTINEZ,§ AND A D A L T O B I A N C H I N I * ,†,§ Programa de Po´s-Graduac¸ a˜o em Oceanografia Biolo´gica, Fundac¸ a˜o Universidade Federal do Rio Grande, Av. Ita´lia km 8, 96 201-900, Rio Grande-RS, Brazil, Water Quality Centre, Trent University, Peterborough, ON, Canada, and Departamento de Cieˆncias Fisiolo´gicas, Fundac¸ a˜o Universidade Federal do Rio Grande, Av. Ita´lia km 8, 96 201-900, Rio Grande-RS, Brazil
Contamination of blubber tissues by organochlorine pesticides (OC) and PCBs was assessed in female and male pups and juveniles, as well as in adult females and subdominant adult males of the Southern elephant seal, Mirounga leonina, from Elephant Island in the Antarctic Peninsula. All residues of persistent organochlorine contaminants analyzed were found in blubber samples, except for β-HCH, endosulfan II, endrin, heptachlor, and aldrin. The relative concentrations of the analytes detected were ΣDDT > ΣPCB > Σchlordane > mirex > dieldrin > HCB> Σendosulfan > methoxychlor > ΣHCHs > other OC pesticides. OC and PCBs concentrations were 1 or 2 orders of magnitude lower than those found in pinnipeds from northern hemisphere. The ratio ΣDDT/ΣPCB was higher in southern elephant seals. The relative importance of some OC residues indicates that pesticides used either currently or in the recent past in countries in the southern hemisphere are the sources of contamination in the Antarctic region. Data showed that concentrations of contaminants generally increased from pups < juveniles < adults and suggested that pups accumulated contaminants through transfer from the mother seals via transplacental and lactational routes.
Introduction The distribution of persistent organic pollutants (POPs) in the atmosphere, water resources, and biota of polar regions has been recognized as a research priority (1). The primary * Corresponding author phone: + 55 53 3233-6853; fax: + 55 53 3233-6848; e-mail:
[email protected]. † Programa de Po ´ s-Graduac¸ a˜o em Oceanografia Biolo´gica, Fundac¸ a˜o Universidade Federal do Rio Grande. ‡ Trent University. § Departamento de 177408n page, Fundac ¸ a˜o Universidade Federal do Rio Grande. 10.1021/es0621187 CCC: $37.00 Published on Web 04/27/2007
2007 American Chemical Society
source of these compounds at the poles is thought to be the global distillation phenomenon by which semivolatile compounds are transported from warmer temperate latitudes to the polar regions, where they condense on snow and ice and are deposited into the terrestrial and marine environments (2). Among the recognized classes of POPs, polychlorinated biphenyls (PCBs), and organochlorine pesticides are contaminants with high persistence, susceptibility to long-range transport, and potential for biomagnification through food chains. There is a great deal of information on the concentrations of POPs in the northern polar region (3), but there is much less information for Antarctica. However, the available contaminant data indicate that organochlorine contaminants are being deposited in the Antarctic continent (4). Some marine mammals have high lipid contents in their tissues, are relatively long-lived, and are generally high in the food chain. Therefore, they tend to have high POPs concentrations in their tissues relative to terrestrial mammals (5). The concentrations of organochlorine contaminants that have been reported for marine mammals from the southern hemisphere (6, 7) are generally lower than those observed in marine mammals from the northern hemisphere (3, 4). However, organochlorine pesticides that have been phased out in northern latitudes continue to be used in some developing countries in the southern hemisphere (8). These persistent pesticides may be a continuing source of contamination to the southern polar region. The Southern elephant seal Mirounga leonina has a circumpolar distribution with major concentrations for reproduction in the islands of the Antarctic Convergence (9) and Valde´s Peninsula, on the southern coast of Argentina (10). It is the biggest and the most sexually dimorphic seal among the 34 species. This seal spends more than 80% of its annual cycle in the sea feeding on prey inhabiting deep regions (>200 m). However, it needs to spend some time on land for reproduction and molting (11). Its life cycle includes two terrestrial periods, one for reproduction (SeptemberOctober) and another for molting (December-February), and two pelagic periods for feeding (postreproduction and postmolting) (10, 11). In general, elephant seals live and form breeding colonies in very remote locations. They are philopatric, returning to the same sites for reproduction and molting in the spring and summer, respectively. The mating period generally occurs in sub-Antarctic islands between September and November. Most of the large males are the first to arrive at the reproduction areas and stay there until all females had left the beaches. This behavior can ensure an opportunity to establish a high hierarchic position and a better chance to control a harem. Pregnant females arrive at the beach in October and November, deliver their pups, start the estrus cycle, copulate, and breast-feed their pups for 23 days (12). The pups suckle the lipid-rich milk for about the first 21 days of life. Lactational transfer of lipophilic contaminants is known to be a major route for the contamination of young in marine mammals (13). After the lactation period, seals go to the sea for the 2 month postreproduction feeding period and return to land for molting. After that, a long postmolting pelagic feeding period precedes the next reproductive season (10, 11). In the sea, the Southern elephant seal is able to perform long movements, reaching regions up to 5000 km far from their areas of reproduction and feeding (14). They are considered important predators in the food web (15). Their diet is composed of cephalopods (16), fish (17), and penguins VOL. 41, NO. 11, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Mean Concentrations (ng‚g-1 Lipid; ( Standard Error) of 25 PCB Congeners and ΣPCB in Blubber Samples of Southern Elephant Seals from Elephant Islanda PCBs
adult subdominant males
adult females
juveniles
pups
PCB-18 PCB-31 PCB-28 PCB-49 PCB-44 PCB-74 PCB-95 PCB-101 PCB-87 PCB-110 PCB-118 PCB-105 PCB-149 PCB-153 PCB-132 PCB-128 PCB-138 PCB-158 PCB-156 PCB-187 PCB-183 PCB-180 PCB-170 PCB-201 PCB-194 ΣPCB
3.16 ( 0.83 (9) 1.37 ( 0.30 (10) 1.34 ( 0.35 (9) 1.68 ( 0.22 (11) 1.13 ( 0.25 (6) 0.66 ( 0.09 (8) 2.05 ( 0.33 (8) 0.94 ( 0.15 (11) 0.85 ( 0.17 (9) 1.52 ( 0.28 (12) 4.21 ( 0.44 (15) 1.44 ( 0.26 (10) 1.96 ( 0.30 (10) 9.89 ( 0.90 (16) 1.52 ( 0.24 (10) 3.82 ( 0.53 (13) 6.96 ( 0.74 (16) 0.64 ( 0.15 (10) 0.86 ( 0.15 (14) 1.83 ( 0.18 (14) 2.48 ( 0.27 (10) 2.89 ( 0.25 (16) 1.31 ( 0.16 (14) 0.67 ( 0.06 (10) 0.43 ( 0.08 (7) 56.09
2.94 ( 0.48 (12) 1.21 ( 0.18 (12) 1.17 ( 0.24 (13) 1.45 ( 0.13 (18) 0.84 ( 0.12 (13) 0.63 ( 0.13 (6) 1.90 ( 0.26 (16) 0.80 ( 0.11 (16) 0.84 ( 0.11 (11) 1.11 ( 0.17 (19) 4.04 ( 0.45 (19) 1.06 ( 0.13 (17) 1.80 ( 0.23 (19) 9.69 ( 0.79 (19) 1.06 ( 0.13 (17) 2.96 ( 0.30 (19) 6.42 ( 0.58 (19) 0.51 ( 0.09 (14) 0.66 ( 0.07 (19) 1.69 ( 0.10 (19) 1.82 ( 0.15 (19) 2.73 ( 0.13 (19) 1.10 ( 0.06 (19) 0.63 ( 0.04 (19) 0.40 ( 0.06 (15) 49.92
2.82 ( 0.40 (17) 1.25 ( 0.09 (17) 0.98 ( 0.14 (22) 1.51 ( 0.09 (25) 0.82 ( 0.12 (14) 0.46 ( 0.06 (13) 1.59 ( 0.18 (17) 0.61 ( 0.07 (18) 0.58 ( 0.09 (16) 0.95 ( 0.09 (25) 3.11 ( 0.25 (31) 0.77 ( 0.08 (26) 1.34 ( 0.13 (20) 7.58 ( 0.49 (29) 0.87 ( 0.09 (18) 2.39 ( 0.20 (29) 5.14 ( 0.33 (27) 0.26 ( 0.05 (11) 0.45 ( 0.03 (23) 1.23 ( 0.11 (28) 1.37 ( 0.10 (22) 2.04 ( 0.12 (26) 0.74 ( 0.05 (28) 0.40 ( 0.03 (22) 0.21 ( 0.02 (12) 39.82
1.25 ( 0.11 (7) 0.78 ( 0.09 (16) 0.48 ( 0.04 (22) 0.94 ( 0.07 (21) 0.36 ( 0.03 (14) 0.34 ( 0.05 (12) 0.79 ( 0.08 (7) 0.39 ( 0.05 (14) 0.29 ( 0.04 (13) 0.51 ( 0.04 (27) 1.77 ( 0.17 (34) 0.39 ( 0.04 (22) 0.62 ( 0.06 (16) 3.47 ( 0.25 (32) 0.44 ( 0.04 (19) 1.02 ( 0.09 (25) 2.46 ( 0.20 (30) 0.22 ( 0.04 (7) 0.21 ( 0.02 (30) 0.46 ( 0.05 (24) 0.55 ( 0.05 (26) 0.74 ( 0.06 (22) 0.35 ( 0.03 (31) 0.15 ( 0.01 (20) 0.12 ( 0.02 (11) 19.32
a Mean values were calculated considering only samples with detectable levels. The number of samples with detectable levels is shown in parenthesis.
(18). However, elephant seals starve during their stay on land for reproduction and molting (11). These animals have large deposits of subcutaneous, lipid-rich blubber that functions as an energy reserve during periods of starvation and as insulation against low temperatures. According to McMahon et al. (19), the southern elephant seal underwent large decreases in population size throughout most of its breeding range in the Southern Ocean between the 1950s and 1990s. These authors pointed that current population estimates suggest a recent recovery, and the South Georgia population remained stable. Furthermore, they suggested that decreases in populations were likely caused by environmental change. According to them, human disturbance could be discounted as a possible cause. Despite that, poor survival and reproductive success in the southern elephant seal associated with contamination by POPs cannot be ruled out. In fact, Goerke et al. (20) recently reported increasing levels and biomagnification of POPs in Antarctic biota, including the southern elephant seal. Thus, our main objective was to assess the concentrations of PCBs and organochlorine compounds in female and male pups, juveniles and adults of M. leonina. Tissues were collected from animals that aggregated on Elephant Island in the Antarctic Peninsula during the austral summers from 1997 to 2000. These data will provide information on the concentrations of POPs in the southern hemisphere, and will contribute to an understanding of the influence of life history on the concentrations of these contaminants in marine mammals.
Experimental Section Collection of Samples and Morphometric Data. During three expeditions to Elephant Island (61°13′S-55°23′W), which are part of the Shetland Islands on the Antarctic Peninsula, blubber samples (n ) 129) were obtained from live and apparently healthy elephant seals that aggregated during the mating and molting periods on Shipwreck Beach and Great Beach in the austral summers of 1997/1998, 1998/1999, 3830
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and 1999/2000 (see Table 1 , Supporting Information). Pups (n ) 41), juveniles (n ) 53), and adults (n ) 35) of both sexes were anaesthetized with tiletamine/zolazepan (1:1) at an estimated dose of 1 mg‚kg-1 using a hypodermic dart, as described by Baker et al. (21). The darts consisted of 10 mL syringes propelled by a lighter-gas. The anaesthetized elephant seals were further restrained with a net. Morphometric data included girth, total length, and weight (see Table 2 , Supporting Information). Only subdominant adult males, which are younger and lighter, were sampled because of the limitation of the electronic scale employed (2000 kg). Samples of blubber weighing ∼3 g were removed by biopsy from the dorsal region of the seals, wrapped in aluminum foil, and maintained in liquid nitrogen. After the field work, the biological material was transported to the Laboratory of Zoophysiology in Brazil, where the samples were archived at -80 °C. In the fall of 2003, all samples were transported by air with cold packs to Trent University in Canada, where they were stored at -4 °C until they were prepared for contaminant analysis. Sample Preparation. Subsamples of blubber weighing approximately 0.2 g were ground with anhydrous sodium sulfate using a mortar and pestle. This material was packed into a 1 × 20 cm glass column to which was added 200 mL of 50:50 hexane:methylene chloride (DCM). The material remained in the solvent for at least 4 h in the glass column. Extracts were then drained into a 500 mL boiling flask and concentrated by rotary evaporation. The analytes were separated from lipids and other coextractives by gel permeation chromatography (GPC) with BioBeads S-X3 (Bio-Rad, Hercules, CA). Biobeads equivalent to 50 g dry wt. were packed into a 3 cm i.d. × 30 cm glass column fitted with a glass wool plug. The solvent used to elute the GPC column was 55:45 hexane:DCM. The sample extract was made up to 3 mL in the GPC solvent and loaded onto the column, followed by a rinsing. The column was then eluted with the solvent at a rate of 5-6 mL/min. The first 70 mL was discarded and the next 90 mL was collected
TABLE 2. Mean Concentrations (ng‚g-1 Lipid; ( Standard Error) of Organochlorine Pesticides and ΣDDT, ΣHCH, Σchlordane, and Σendosulfan in Blubber Samples of Southern Elephant Seals from Elephant Islanda organochlorines
adult subdominant males
adult females
juveniles
pups
p, p′-DDE p, p′-DDD p, p′-DDT o, p′-DDE o, p′-DDD o, p′-DDT ΣDDT P, p′-DDE/ΣDDT ΣDDT/ΣPCB HCB Mirex R-HCH γ-HCH β-HCH ΣHCH R-HCH/γ-HCH cis-chlordane trans-chlordane cis-nonachlor trans-nonachlor Σchlordane endosulfan endosulfan-sulfate endosulfan II Σendosulfan endrin endrin-ketone heptachlor heptachlor-epoxide methoxychlor aldrin dieldrin
178.52 ( 22.12 (11) 1.87 ( 0.89 (10) 6.63 ( 0.83 (10) 2.11 ( 0.36 (11) 2.20 ( 0.46 (8) 1.52 ( 0.72 (10) 192.85 (15) 0.93 3.44 11.20 ( 1.71 (16) 24.28 ( 1.57 (13) 0.51 ( 0.04 (10) 1.04 ( 0.39 (4) ND 2.20 (11) 0.49 1.76 ( 0.43 (8) 3.95 ( 0.5 (16) 10.23 ( 1.24 (12) 22.62 ( 2.09 (16) 38.56 (16) 1.07 ( 0.30 (3) 1.95 ( 0.23 (10) ND 3.02 (10) ND 0.53 ( 0.05 (3) ND 0.81 ( 0.12 (5) 2.89 ( 0.35 (13) ND 10.25 ( 1.15 (11)
170.94 ( 27.62 (18) 1.17 ( 0.22 (12) 5.21 ( 0.50 (18) 1.94 ( 0.37 (14) 1.90 ( 0.34 (9) 1.43 ( 0.17 (18) 182.59 (19) 0.94 3.66 8.58 ( 0.93 (19) 29.30 ( 1.40 (19) 0.47 ( 0.05 (19) 0.65 ( 0.07 (17) ND 1.61 (19) 0.72 1.24 ( 0.13 (14) 3.21 ( 0.28 (19) 9.12 ( 0.75 (19) 20.96 ( 2.13 (19) 34.53 (19) 0.97 ( 0.36 (5) 1.71 ( 0.12 (10) ND 2.68 (14) ND 0.51 ( 0.05 (5) ND 0.66 ( 0.31 (4) 2.70 ( 0.25 (16) ND 9.12 ( 1.07 (16)
115.45 ( 8.63 (28) 0.86 ( 0.09 (21) 3.94 ( 0.35 (26) 1.34 ( 0.17 (14) 0.80 ( 0.14 (11) 1.11 ( 0.09 (30) 123.50 (33) 0.93 3.10 8.89 ( 0.73 (28) 19.41 ( 1.34 (26) 0.43 ( 0.03 (22) 0.34 ( 0.05 (17) ND 1.24 (29) 1.26 0.70 ( 0.09 (23) 2.85 ( 0.25 (29) 7.39 ( 0.55 (27) 20.29 ( 1.89 (33) 31.20 (34) 0.42 ( 0.08 (12) 1.57 ( 0.20 (17) ND 1.99 (24) ND 0.33 ( 0.06 (21) ND 0.44 ( 0.12 (8) 2.20 ( 0.34 (12) ND 7.94 ( 0.58 (27)
77.13 ( 8.63 (31) 0.33 ( 0.05 (14) 1.13 ( 0.12 (18) 0.45 ( 0.03 (19) 0.35 ( 0.06 (11) 0.57 ( 0.05 (25) 79.95 (41) 0.96 4.14 4.60 ( 0.23 (22) 8.42 ( 0.77 (34) 0.28 ( 0.02 (37) 0.25 ( 0.02 (36) ND 0.81 (41) 1.12 0.42 ( 0.03 (31) 1.36 ( 0.13 (16) 4.01 ( 0.21 (33) 12.30 ( 0.91 (41) 18.09 (41) 0.29 ( 0.04 (10) 0.60 ( 0.06 (13) ND 0.90 (18) ND 0.19 ( 0.03 (21) ND 0.18 ( 0.05 (5) 1.30 ( 0.12 (17) ND 4.28 ( 0.29 (21)
a The ratios of p,p′-DDE/ΣDDT, ΣDDT/ΣPCB, and RHCH/γHCH are also shown. Mean values were calculated considering only samples with detectable levels. The number of samples with detectable levels is shown in brackets. ND indicates not detected in any of the samples.
for gravimetric determination of lipid content. The next 95 mL of eluent, which contained the analytes, was collected and rotary evaporated to 2 mL for further sample cleanup. Further fractionation was conducted by column chromatography with 5 g of activated 60-200 mesh silica gel (Sigma-Aldrich, Toronto, ON, Canada) packed into a 1 cm i.d. × 30 cm glass column fitted with a glass wool plug. Elution with 40 mL of hexane produced a fraction containing primarily PCB compounds and some pesticides (i.e., Fraction A), and further elution with 80 mL of 50:50 hexane:DCM produced a fraction containing the other organochlorine analytes (i.e., Fraction B). The extracts were rotary evaporated to ∼1 mL and transferred to conical centrifuge tubes with rinsings of hexane and iso-octane. These extracts were further evaporated in a vacuum centrifuge to a final volume of 100 µL, and they were placed in autosampler vials. Analysis. Samples were analyzed by high-resolution gas chromatography with an electron capture (63Ni) detector (HRGC-ECD) using a Varian model 3500 gas chromatograph equipped with a 60 m DB-5 (J&W) fused silica column (0.25 um ID, 0.25 µm film thickness) and splitless injection. The volume injected was 2 µL. For analysis of Fraction A, the temperature conditions were injector 250 °C, detector at 275 m, column starting temperature: 80 °C, increase at 4 degrees‚min-1 to 160 °C, then increase at 1.5 degrees‚min-1 to 220 °C, then increase at 7 degrees‚min-1 to 250 °C, 35 min hold. For analysis of Fraction B, the same detector and injector temperatures were used, but the column temperature program was starting temperature: 70 °C, increase at 15 degrees‚min-1 to 210 °C, hold for 9 min, increase at 2 degrees‚min-1 to 270 °C, hold for 5 min.
The analytes were identified by retention time. The PCB congeners analyzed included (in order of elution from the DB-5 column) IUPAC congener numbers 18, 31, 28, 49, 44, 74, 95, 101, 87, 110, 149, 118, 153, 132, 105, 138, 158, 183, 187, 128, 156, 180, 170, 194, and 201. In preliminary analyses of 35 PCB congeners in the blubber samples, these 25 congeners comprised over 96% of the total PCBs. Total PCBs were calculated as the sum of the concentrations of the 25 congeners. Quantification of the PCB congeners was done by comparison with standards obtained from the National Research Council, Halifax, N.S., Canada. Organochlorine analytes included, hexachlorobenzene (HCB), aldrin, dieldrin, mirex, methoxychlor, heptachlor, heptachlor-epoxide, endrin, endrin-ketone and (a) p,p′DDT, o,p′- DDT, p,p′- DDE, o,p′- DDE, and p,p′- DDD, o,p′DDD, and the sum of these compounds (total DDT); (b) cisand trans-nonachlor, cis-and trans-chlordane, and the sum of these compounds (total chlordane); (c) R-HCH, β-HCH, and γ-HCH, and the sum of these compounds (total HCH); (d) R-endosulfan, endosulfan II, endosulfan sulfate, and the sum of these compounds (total endosulfan). Quantification of the organochlorine compounds was done by comparison with standards obtained from the Wildlife Toxicology and Surveys Branch, Canadian Wildlife Service, Hull, QC, Canada. Concentrations of analytes were calculated on a lipidnormalized basis (ng/g lipid). The mean lipid content of all blubber samples was 66%, and the mean lipid content for blubber from the pups, juveniles and adults were 69.6, 57.3, and 68.4%, respectively. The Limits of Detection (LODs) were (on a lipid normalized basis) 0.1-0.3 ng‚g-1 for the PCB congeners, 0.2-0.3 ng‚g-1 for mirex, HCHs and chlordanes, and 0.3-0.5 ng‚g-1 for dieldrin and DDTs. Preliminary VOL. 41, NO. 11, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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analysis of the data for pups and juveniles showed no differences in the concentrations of analytes in the two sexes, and therefore, the data from male and female animals were pooled. For the adult animals, the data on analyte concentrations in females and subdominant males were kept separate. Quality Assurance. Procedural blanks were prepared to provide quality assurance for GC-ECD analysis. They were carried out after every 13 samples. No corrections were necessary. Cod liver oil reference material (SRM 1588) purchased from the U.S. National Institute of Standards and Technology (NIST) was analyzed for concentrations of PCBs and organochlorines pesticides, and concentrations of all analytes were within certified values. For PCBs, HCHs, DDTs, and chlordane compounds, the mean recovery ((standard deviation) was 74.2 ( 5.4%, 112.2 ( 5.6%, 114.4 ( 3.4%, and 117.4 ( 17.5%, respectively. Statistical Analysis. For all statistical comparisons, lipid normalized data were used to adjust for differences in the lipid content of the blubber. Data were previously tested for a possible influence of the year of collection on contaminant concentrations for the different life stages of the seals of both sexes. However, no significant differences were observed. Therefore, only one general mean was calculated for each developmental stage and sex. Data were previously logtransformed and compared using analysis of variance, with a posteriori analysis between paired groups using Tukey test. All statistical analyses were conducted at a level of significance of P < 0.05.
Results All PCB congeners and organochlorine pesticides analyzed were detected in the blubber samples from elephant seals, with the exception of β-HCH, endosulfan II, endrin, and aldrin. Their concentrations are shown in Tables 1 and 2, respectively. Among PCBs, the most abundant congeners were PCB 153, 138, 118, 128, 180, and 183, regardless of sex and developmental stage (Table 1). The dominant classes were the penta, hexa, and heptachlorobiphenyls, accounting, respectively, for 17.8% (six congeners), 51.2% (seven congeners), and 15.9% (four congeners) of the total PCBs present in all development phases of the elephant seals (see Figure 1, Supporting Information). There was a significant increase (P < 0.05) in the mean PCBs concentrations as the elephant seals developed from pups to juveniles to adults. Although there was a trend of higher PCB concentrations in subdominant male elephant seals, no significant difference (P > 0.05) between the mean PCB concentrations in the adult females and adult subdominant males was detected (Table 1). Among the DDT analytes, p,p′-DDE showed the highest mean concentration (>90% of the total DDT compounds). All other p,p′- and o,p′-isomers of DDT and its metabolites were also detected, but at much lower concentrations (Table 2, see also Figure 2, Supporting Information). Concentrations of p,p′-DDE and all other DDT compounds increased from pups to juveniles to adults. In adult females and adult subdominant males, no significant differences (P > 0.05) in the concentrations of DDT compounds were found, although a trend of lower concentrations was observed in females. The ΣDDT/ΣPCB proportion showed that ΣDDT concentrations were approximately 3-4 times higher than those of ΣPCB (Table 2). All other organochlorine compounds detected were present at mean concentrations between 0.18 and 29.3 ng.g-1 lipid. For all analytes, the mean organochlorines concentrations increased with developmental stage, with concentrations increasing from pups to juveniles to adults. However, no significant differences (P > 0.05) in the mean concentrations of organochlorine pesticide analytes were observed in adult female and adult subdominant males, although a trend 3832
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of lower concentrations was observed in females. One exception was the trend of a higher mean concentration of mirex in females, being not significantly different (P > 0.05) (Table 2). Data for several organochlorine pesticides warrant closer consideration. The average concentrations of mirex, HCB, trans-nonachlor, and dieldrin in different developmental stages, respectively, varied between 8.42, 4.60, 12.30, and 4.28 ng‚g-1 lipids in pups to 24.28, 11.2, 22.62, and 10.25 ng‚g-1 lipids in adult subdominant males, respectively. These mean concentrations exceeded the concentrations of most other organochlorine compounds, except for p, p′-DDE (Table 2). Regarding the individual chlordane compounds, isomers of HCH and endosulfan compounds, significantly higher (P < 0.05) relative proportions of trans-nonachlor and endosulfan were observed in pups, relative to the other developmental stages. Note for the HCH isomers that β-HCH was not detected and the proportions of R-HCH and γ-HCH isomers varied with the developmental stage, R-HCH being present in higher proportions in the pups and juveniles (Table 2, see also Figure 3, Supporting Information).
Discussion Our data contribute to the small body of literature on the concentrations of persistent organic contaminants in marine mammals from the Antarctic region. Results for ΣPCB, ΣDDT, ΣCHL, ΣHCH, HCB, dieldrin, and mirex are in complete agreement with those previously reported for southern elephant seal and other Antarctic pinnipeds (Table 3). They are also consistent with previous studies showing low contaminant levels in the blubber of marine mammals from the southern hemisphere, relative to marine mammals in the northern hemisphere (6, 7). The concentrations of DDT compounds and PCBs reported here were 1-2 orders of magnitude lower than those in blubber of pinnipeds from different regions in the northern hemisphere, which showed concentrations of ΣPCB approximately equivalent to or greater than concentrations of ΣDDT (22, 23), in comparison to a much higher proportion of DDT in the elephant seals from this study (Table 2). In fact, global contamination and decreasing levels of PCBs and OC pesticides from the northern to the southern hemisphere are widely reported (24). Despite that Antartica is a remote polar region, the fact that most of the OC compounds analyzed in the present study were detected, suggests that long-range transport of POPs from tropics and other source-areas to the southern polar region is occurring, mainly through the transport of air mass. Actually, data available clearly indicate that the longrange atmospheric transport and fate on global terms are involved in the Antarctic contamination by OCs such as HCHs, DDTs, CHLs, and PCBs (25, 26). 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 (2). There are evidence that the concentrations of several OC compounds are actually increasing in the southern hemisphere (7, 20). However, data compiled for pinnipeds from Antarctica are extremely variable among species (Table 3). Furthermore, no time series on OC levels in any Antarctic biota, except for minke whale (6), are available. Therefore, further studies are needed to allow us to make valid conclusions on the pattern and evolution of OC contamination in Antarctic pinnipeds. Once POPs reach the polar region, they are bioaccumulated in different levels of the food chain. In this context, the southern elephant seal, which shows seasonal movements that are not restricted to the areas close to their natal colonies (14), becomes susceptible to POPs contamination especially through diet. In fact, they are considered important predators in the food web, consuming high amounts of preys to ensure
TABLE 3. Maximum Concentration (ng‚g-1 Lipid) of Organochlorine Compounds in Blubber of Pinnipeds from Antarctica species location and year of collection, (reference) Lobodon carcinophagus Ross Island, 1964, (38) Leptonychotes weddellii McMurdo Sound, 1965/1967, (39) Leptonychotes weddellii Weddell Sea, 1980s, (40) Leptonychotes weddellii Syowa Station, 1980-1982, (34) Leptonychotes weddellii Syowa Station, 1981, (41)
Leptonychotes weddellii Syowa Station, 1981, (42) Leptonychotes weddellii Syowa Station, 1981, (25) Leptonychotes weddellii Weddell Sea, 1986-2000, (20)a Leptonychotes weddellii Ross Sea, 1994-1996, (24) Ommatophoca rossi Queen Maud Land, 1981-1982, (43) Hydrurga leptonyx Antarctica, 1970s, (44)a Mirounga leonina Elephant Island, 1996, (20)a Mirounga leonina Elephant Island, 1997-2000, (present study)
a
Values estimated from a graph.
b
stage/sex
ΣPCB
young male
ΣDDT
ΣCHL
ΣHCH
HCB
dieldrin
mirex
39 105 85
117
adult male adult male adult female male pup adult male adult female male pup Female pup -
0.7 69
38 33 5 12 8 0.6 2 38
186 101 24 52 29 4 4 170
62 36 16
25
108b
65
Adult
11
17b
Male Female
95 76 40
140 137 120
20
106b
33
56 50 40 19
193 183 124 80
39 35 31 18
adult male adult female juvenile pup
4
ΣPCB > Σchlordane > mirex > dieldrin > HCB > Σendosulfan > methoxychlor > ΣHCHs > other organochlorines. This pattern is in agreement with previous results showing higher ΣDDT than ΣPCB in several Antarctic pinnipeds (Table 3). However, it is generally opposed to that found in pinnipeds from the northern hemisphere, where similar or higher ΣPCB VOL. 41, NO. 11, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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than ΣDDT are observed, reflecting the importance of industrial sources of PCBs in developed countries (31). Based on the high ratios of p, p′-DDE/ΣDDT found in southern elephant seals, as well as high levels of p, p′-DDE in other Antartic species (Table 3), it appears that the residues of DDT compounds in pinnipeds from the southern hemisphere are due to recent past use of this pesticide. This compound comprised approximately 70% of total DDT in minke whales, Balaenoptera acutorostrata from the Antarctic Ocean (7). Higher proportions of p,p′-DDT relative to p,p′DDE were observed two decades ago in the cetacean, Pontoporia blainvillei from the Uruguayan coast, which reflects the heavy use of DDT in Brazil and Uruguay during the 1970s (32). More recently, Yogui et al. (10) observed ratios of ΣDDT to p,p′-DDE of approximately 0.8 in Brazilian dolphins (Sotalia fluviatilis) and attributed this ratio to inputs of DDT throughout the 1970s and early 1980s. While the p,p′-isomers of DDT compounds predominated in the blubber samples of Antarctic elephant seals, the concentrations of the o,p′-isomers are also notable because several of these compounds have been shown to have estrogenic or anti-estrogenic activity (33). Chlordane compounds are important contaminants in the elephant seals, levels being similar to those found in other Antarctic pinnipeds (Table 3). In elephant seals, transnonachlor is the dominant chlordane compound (>75%), followed by cis-nonachlor, R-chlordane, and γ-chlordane. This pattern is similar to those reported for Weddell seals (34). The relative importance of mirex as a contaminant in the elephant seals, as well as in other Antarctic pinnipeds (Table 3), is unusual in the context of the major organochlorines reported for species from the northern hemisphere where lower levels are observed (35). This finding associated with the significant concentrations of endosulfan compounds and methoxychlor in elephant seals suggest the predominance of pesticides that are currently used or were used historically for agriculture in the southern hemisphere (7, 36). The presence of methoxychlor and heptachlor epoxide residues in southern elephant reflects recent inputs of pesticides into the environment (37). The lack of detection of aldrin and endrin, as well as the presence of the metabolite endrinketone in the blubber of southern elephant seals, suggest that these pesticides are also easily metabolized by these pinnipeds. Aono et al. (6) observed HCB in the blubber of minke whales from Antarctica and attributed this to high rates of atmospheric transport and deposition in the cold polar region. The HCB observed in elephant seals from this study are similar to other Antarctic pinnipeds (Table 3), and almost certainly a consequence of transport within the southern hemisphere and deposition in the southern polar region. Aguilar et al. (31) observed a trend of increasing concentrations of HCH compounds in marine mammals from higher latitudes. Low concentrations of HCHs were detected in southern elephant seals. Nondetection of β-HCH was puzzling, as this isomer is a major constituent of technical-HCH. Higher concentrations of the γ-HCH isomer were observed in adults, while in juveniles and pups, the R-HCH isomer was the most important. The isomer patterns observed in the elephant seals may reflect the importance of lindane (i.e., γ-HCH) as a source of these residues, rather than technical-HCH. Aono et al. (6) also found that R-HCH (45%) and γ-HCH (30%) predominated in the blubber of minke whales from the Antarctic Ocean and suggested that high concentrations of γ-HCH are related to the continued major use of lindane as a pesticide in several countries in the southern hemisphere. In contrast, in California elephant seals (M. angustirostris), the mean concentrations of HCHs in blubber varied between 0.12 and 0.30 µg.g-1 lipid, and the 3834
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β-isomer was responsible for 87 to 95% of the total concentration (20). Therefore, the patterns of HCH-isomers in marine mammals from the northern hemisphere probably reflect contamination by both lindane and technical-HCH. In summary, data reported here show that DDT compounds and PCBs are the most accumulated POPs in the blubber of elephant seals from Elephant Island (Antarctic Peninsula). However, concentrations of these compounds are 1-2 orders of magnitude lower than those of pinnipeds from the northern hemisphere. The relative importance of other organochlorine pesticides in blubber tissue, such as mirex, methoxychlor, dieldrin, and γ-HCH, indicates that pesticides used either currently or in the recent past in countries in the southern hemisphere are the sources of contamination in the Antarctic region. Monitoring of marine mammals from Antarctica should continue to evaluate whether the concentrations of these compounds are increasing over time. A unique feature of this study was the observation that the pups and juveniles of elephant seals had accumulated significant quantities of persistent contaminants as a result of contaminant transfer from mother seals through transplacental and lactational routes. Early developmental stages of mammals are known to be susceptible to the impacts of exposure to persistent contaminants (23). However, to assess possible health effects, data are needed on the concentrations of persistent contaminants in target organs, such as the liver and brain, as well as critical information on key aspects of the health of the individuals sampled.
Acknowledgments This research was financially supported by the Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq), Secretaria da Comissa˜o Interministerial para os Recursos do Mar and Programa Anta´rtico Brasileiro of Brazil and the Natural Sciences and Engineering Research Council (NSERC) of Canada. We thank Shaun O’Toole for his assistance during the laboratory analyses. Adalto Bianchini is a research fellow from the Brazilian CNPq.
Supporting Information Available Tables with detailed description of the southern elephant seals sampled. Figures with the mean concentrations of PCB congeners in the blubber of adult subdominant male southern elephant seals and the proportions of HCH-isomers and DDT, chlordane, and endosulfan compounds in blubber of southern elephant seals from different developmental stages. This material is available free of charge via the Internet at http://pubs.acs.org.
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Received for review September 5, 2006. Revised manuscript received March 15, 2007. Accepted March 16, 2007. ES0621187
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