Environ. Sci. Technol. 2004, 38, 403-413
PCDDs, PCDFs, and Coplanar PCBs in Albatross from the North Pacific and Southern Oceans: Levels, Patterns, and Toxicological Implications S H I N S U K E T A N A B E , * ,† MAFUMI WATANABE,† TU BINH MINH,† TATSUYA KUNISUE,† SHIGEYUKI NAKANISHI,† HITOSHI ONO,‡ AND HIROYUKI TANAKA§ Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan, Branch Office in Ogasawara, Tokyo Metropolitan Government, Nishimachi, Chichijima, Ogasawara, Tokyo 100-2101, Japan, and National Research Institute for Fishery Environment of Inland Sea, Fishery Research Agency, Maruishi 2-17-5, Ohno-Cho, Hiroshima 739-0452, Japan
Concentrations of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and coplanar polychlorinated biphenyls (coplanar PCBs) were determined in five albatross species collected from the North Pacific and Southern Oceans to assess the northsouth differences in residue levels, accumulation patterns, and toxic potential. Black-footed and Laysan albatrosses from the North Pacific Ocean contained higher levels of PCDD/ Fs and coplanar PCBs than albatrosses from the Southern Ocean, indicating that emission sources of these contaminants were predominant in the northern hemisphere. Residue levels in albatrosses from the remote North Pacific Ocean far from the point source of pollution were comparable to or higher than those in terrestrial and coastal birds from contaminated areas in developed nations, suggesting the specific exposure and accumulation of PCDD/ Fs and coplanar PCBs in albatross. The long life span and ingestion of plastic resin pellets by albatrosses could be the plausible explanations for the elevated accumulation of persistent and lipophilic contaminants including PCDD/ Fs and coplanar PCBs in these birds. Relative proportions of PCDFs and coplanar PCBs in albatross were higher than those observed in birds inhabiting terrestrial and coastal areas, suggesting that these toxic chemicals may have higher transportability by air and water than PCDDs. Congener patterns of PCDD/Fs in albatross showed less variability as compared to those in terrestrial species, indicating that contamination patterns of PCDD/Fs were similar within the open ocean environment. Contributions of PCDD/Fs to total TEQs in albatrosses from the open ocean were generally lower than those in terrestrial birds, suggesting different toxic potency of PCDD/Fs and coplanar PCBs on animals inhabiting open ocean and terrestrial environment. * Corresponding author phone/fax: +81-89-927-8171; e-mail:
[email protected]. † Ehime University. ‡ Tokyo Metropolitan Government. § Fishery Research Agency. 10.1021/es034966x CCC: $27.50 Published on Web 12/10/2003
2004 American Chemical Society
Whereas albatrosses from southern oceans retained lower TEQ concentrations, possible adverse effects of PCDD/ Fs and coplanar PCBs to black-footed and Laysan albatrosses of the North Pacific Ocean may be suspected from TEQ levels.
Introduction Worldwide contamination by dioxin-related compounds, such as polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibezofurans (PCDFs), and coplanar polychlorinated biphenyls (coplanar PCBs), has been of great concern due to their persistency in the environment, highly bioaccumulative nature, and adverse effects on wildlife and humans (1). Many studies have been conducted to understand the contamination status and distribution and toxic effects of PCDD/Fs and coplanar PCBs in terrestrial and coastal wildlife from developed countries (e.g., refs 2-5). However, data on the levels, pattern,s and trends of dioxins and related compounds in wildlife from the remote open ocean, particularly in the Southern Ocean, are very limited. Albatrosses (Diomedeidae) are the biggest oceanic birds; they wander the open ocean during most of their lives. Most species are not intermingling between the northern and southern hemispheres. Previous studies have reported that albatrosses accumulated relatively higher concentrations of persistent organic pollutants (POPs) such as PCBs, organochlorine pesticides, and PCDD/Fs as compared to other sea birds (6-10). Laysan albatross from the central North Pacific Ocean carried elevated toxic equivalent (TEQ) concentrations that may be enough to cause a threat to its population (6). These observations indicate that albatrosses can be considered as a useful bioindicator for monitoring marine pollution and exploring clues for understanding possible toxic implications of POPs on wildlife in remote open oceans (11). In addition, despite some recent studies reported on dioxins and related compounds in birds from the open ocean of the North Pacific, very few investigations have examined the differences in residue levels and accumulation pattern in oceanic birds from the northern and southern oceans (6, 10). In the present study, concentrations of PCDDs, PCDFs, and coplanar PCBs were determined in muscles of five species of albatrosses collected from the North Pacific and Southern Oceans to understand the levels, patterns, and toxic potential. Extensive comparison with other avian species is made to provide insight into the north-south differences in accumulation patterns, crucial factors influencing these patterns, and source of contaminants in albatross. In addition, TEQ concentrations in muscle of albatross were estimated to evaluate the toxic potential of dioxin and dioxin-like compounds in these birds.
Materials and Methods Samples and Sampling Locations. Twenty-six specimens of albatrosses belonging to two species from the North Pacific Ocean and three species from the Southern Ocean were employed for the present study. The albatross species comprised black-footed albatross (BfA), Laysan albatross (LyA), black-browed albatross (BbA), grey-headed albatross (GhA), and light-mantled albatross (LmA). The details of sampling locations and biometric data of these birds are shown in Figure 1 and Table 1. Albatrosses were accidentally caught by various fishing gear. All of the samples were transported to the laboratory and stored at -20 °C until VOL. 38, NO. 2, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Map showing sampling locations of albatross from the North Pacific and Southern Oceans.
TABLE 1. Biometric Data of Albatross Collected from the Norh Pacific and Southern Oceans sample
year
life stage
body body length sex wt (kg) (cm)
location
North Pacific Ocean Black-Footed Albatross (BfA: Diomedea nigripes) BfA01 BfA02 BfA03 BfA04 BfA05 BfA06
1998 1998 1998 1999 1999 1999
LyA01 LyA02 LyA03 LyA04 LyA05
1998 1998 1998 1998 1998
immature mature mature mature mature mature
M F M M M M
3.10 3.65 3.90 4.00 4.10 4.20
61.1 78.6 83.3 83.7 82.1 83.5
24′ 49 N, 171′ 04 E 24′ 30 N, 169′ 37 E 24′ 32 N, 169′ 38 E off coast of Ogasawara, Japan
Laysan Albatross (LyA: D. immutabilis) mature mature mature mature mature
F M F F M
2.00 2.90 2.50 2.60 3.30
77.6 80.3 75.8 75.8 82.2
33′ 29 N, 142′ 06 E 24′ 04 N, 177′ 59 E 24′ 04 N, 177′ 59 E 24′ 35 N, 171′ 31 E 24′ 30 N, 169′ 37 E
Southern Ocean Black-Browed Albatross (BbA: D. melamophris) BbA01 BbA02 BbA03 BbA04 BbA05
1994 1995 1995 1994 1995
GhA01 GhA02 GhA03 GhA04 GhA05
1994 1996 1996 1996 1996
mature immature immature mature immature
M M F M M
4.40 3.75 3.05 4.45 3.85
89.3 85.3 83.2 89.6 86.4
39′ 04 S, 111′ 09 E 41′ 52 S, 9′ 37 E 43′ 01 S, 104′ 47 E 39′ 04 S, 111′ 09 E 42′ 08 S, 26′ 29 E
Grey-Headed Albatross (GhA: D. chrysostoma) immature immature immature immature immature
F M M M M
3.46 3.20 4.44 3.35 4.25
82 83 90.2 80.4 89.5
39′ 04 S, 111′ 09 E 37′ 00 S, 98′ 05 E 37′ 20 S, 99′ 13 E 37′ 20 S, 99′ 40 E 39′ 11 S, 97′ 38 E
Light-Mantled Albatross (LmA: Phoebetria palpebrata) LmA01 LmA02 LmA03 LmA04 LmA05
1995 1995 1996 1995 1995
mature mature mature mature mature
M F F M M
3.20 3.26 2.50 3.00 2.77
91.4 90.7 79.1 86.3 84.9
43′ 31 S, 11′ 27 E 37′ 32 S, 99′ 22 E 42′ 48 S, 100′ 48 E 38′ 18 S, 102′ 26 E 43′ 02 S, 25′ 35 E
analysis. After dissection, the breast muscle was used for chemical analysis. Chemical Analysis. The method for chemical analysis of PCDD/Fs and coplanar PCBs in the muscles of albatrosses was developed in this study. The breast muscle (10-25 g) was ground with anhydrous sodium sulfate and extracted in a Soxhlet apparatus for >8 h with dichloromethane (DCM). The extract was concentrated to 20 mL using a rotary evaporator, and a 2-mL aliquot of the extract was used for lipid determination by gravimetric method. 13C12-labeled PCDD/Fs and coplanar PCBs (2378-T4CDD/F, 12378-P5CDD/ 404
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F, 123678-H6CDD/F, 123789-H6CDF, 1234678-H7CDD/F, O8CDD/F, CB-77, CB-81, CB-118, CB-126, CB-156, CB-167, CB169, and CB-189) were spiked into the remaining extract as internal standards. Lipid and biogenic materials in this solution were removed by gel permeation chromatography (GPC) using a Bio-Bead S-X 3 packed glass column (50 cm × 2 cm i.d., Bio-Rad Laboratories, Hercules CA). A mixture of 50% hexane in DCM was used as mobile phase at a flow rate of 5 mL/min. The first 120 mL of eluted solvent was discarded, and 100 mL in the second fraction, which contained PCDD/Fs and coplanar PCBs, was collected, concentrated and passed through a 3-g activated silica gel packed glass column (Wako-gel S-1, Wako Pure Chemical Industries Ltd., Osaka, Japan). PCDD/Fs and coplanar PCBs were eluted with a 220 mL of hexane. After concentration to 3 mL, the cleaned up extract was spiked into a 10-g activated alumina packed glass column (aluminum oxide 90, Brockman activity I, 70-230 mesh; Merck, Darmstadt, Germany). The first fraction eluted with hexane contained PCB isomers including almost mono-ortho coplanar congeners, and the second fraction eluted with 50% of DCM in hexane contained the remaining mono-ortho coplanar PCBs, non-ortho coplanar PCBs, and PCDD/Fs. The second fraction eluted from the activated alumina column was then passed through a 1-g activated carbon-dispersed silica gel packed glass column (1 cm i.d., Kanto Chemical Co. Inc., Tokyo, Japan). The first fraction from the carbon-dispersed silica gel column was collected with 25% of DCM in hexane for mono-ortho coplanar PCBs and was combined with the first fraction from the alumina column. The second fraction from the carbondispersed silica gel column eluted with 220 mL of toluene contained non-ortho coplanar PCBs and PCDD/Fs. Both fractions were concentrated nearly to dryness. The 13C12labeled CB-105, CB-157, and CB-180 prepared in decane were then added in the combined first fraction, and 13C12-labeled 1234-T4CDD and 123789-H6CDD with decane were added in the second fraction. The identification and quantification of mono-ortho coplanar PCBs were performed using a gas chromatograph (GC) (Agilent 6890 series, Agilent Technology, Wilmington, DE) with an autoinjection system and a benchtop doublefocusing mass selective detector (JEOL GC-Mate II, JEOL Ltd., Tokyo, Japan) at a resolving power of >2000. The GC column used was a DB-1 fused silica capillary (60 m length, 0.25 mm i.d., 0.25-µm film thickness, J&W Scientific Inc., Folsom, CA) with deactivated fused silica guard columns on both ends. The identification and quantification of non-ortho coplanar PCBs and PCDD/Fs were performed using a GC (Agilent 6890
TABLE 2. Concentrations and TEQs of PCDD/Fs and Dioxin-like PCBs in Muscles of Albatrosses from the North Pacific and Southern Oceansa North Pacific Ocean species:
n: lipid (%): PCDD/DFs (pg/g of lipid wt) 2378-T4CDD 12378-P5CDD 123478-H6CDD 123678-H6CDD 123789-H6CDD 1234678-H7CDD O8CDD 2378-T4CDF 12378-P5CDF 23478-P5CDF 123478-H6CDF 123678-H6CDF 123789-H6CDF 234678-H6CDF 1234678-H7CDF 1234789-H7CDF O8CDF PCDDs PCDFs PCDD/Fs TEQs-PCDDs TEQs-PCDFs TEQ-PCDD/Fs coplanar PCBs (ng/g of lipid wt) CB-77 CB-81 CB-126 CB-169 CB-105 CB-114 CB-118 CB-123 CB-156 CB-157 CB-167 CB-189
Southern Ocean
black-footed albatross 6 4.4 2.8-6.1b
Laysan albatross 5 3.1 1.3-8.1
black-browed albatross 5 5.0 3.8-7.4
72 (70) 53-120 620 (600) 420-1000 120 (120) 87-180 600 (560) 400-1100 130 (120) 90-220 71 (68) 55-130 14 (12) 4.9-25 210 (200) 130-270 290 (290) 250-350 800 (780) 570-1100 270 (260) 180-410 360 (350) 240-600 14 (14) 8.5-24 430 (410) 260-650 24 (23) 16-33 8.7 (6.6)
