Evaluation of Noninvasive Approach for Monitoring PCB Pollution of

Jun 15, 2007 - ... in experimental drift nets and long-lines in the North Pacific Ocean. .... ILHA GRANDE BAY, RIO DE JANEIRO STATE, SOUTH-EASTERN ...
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Environ. Sci. Technol. 2007, 41, 4901-4906

Evaluation of Noninvasive Approach for Monitoring PCB Pollution of Seabirds Using Preen Gland Oil R E I Y A M A S H I T A , † H I D E S H I G E T A K A D A , * ,‡ MICHIO MURAKAMI,‡ MASA-AKI FUKUWAKA,§ AND YUTAKA WATANUKI† Faculty of Fisheries, Hokkaido University, Minato-cho 3-1-1, Hakodate, Hokkaido, 041-8611, Japan, Laboratory of Organic Geochemistry (LOG), Tokyo University of Agriculture and Technology, Saiwai-cho 3-5-8, Fuchu, Tokyo, 183-8509, and Japan, Hokkaido National Fisheries Research Institute, Fisheries Research Agency

Oil secreted from the preen gland (located at the base of the tail feathers) of seabirds can be collected from live birds. We determined PCB concentrations and profiles in the preen gland oil and corresponding abdominal adipose tissue collected from 30 seabirds (2 orders, 3 families, 10 genera, 13 species) to examine the utility of the oil as a monitoring medium. Samples were collected from seabirds that had died in traffic accidents or had become caught unintentionally in experimental drift nets and long-lines in the North Pacific Ocean. Significant concentrations of PCBs were detected in all oil samples, with a concentration range of 9-4834 ng/g-lipid and a geometric mean of 404 ng/ g-lipid. PCBs in the oil had more lower-chlorinated congeners than those in corresponding abdominal adipose, suggesting that they had less opportunity to undergo metabolism before they were secreted from the gland. We observed a weak but significant correlation between the PCB concentrations in the oil and abdominal adipose tissue (R2 ) 0.19, P < 0.05). Correcting for the metabolic loss of PCBs on the basis of congener profiles improved the correlation (R2 ) 0.48, P < 0.001), implying that congenerspecific determination of PCBs in the preen gland oil enables us to estimate PCB concentrations in the abdominal adipose within 1 order of magnitude difference. The differences in PCB concentrations among the 13 species are discussed in terms of dietary behavior, habitat, and migration.

Introduction Hydrophobic persistent organic pollutants (POPs), such as polychlorinated biphenyls (PCBs), are concentrated in biological tissue and biomagnified through the food web. POPs are highly accumulated in seabirds, because the birds are top predators in marine ecosystems. POPs in seabirds are monitored because their adverse effects are of concern (1, 2). Because of the biomagnification, the measurement of POPs in seabirds serves as a sentinel of POP contamination in marine ecosystems. * Corresponding author phone: +81-42-367-5825; fax: +81-42360-8264; e-mail: [email protected]. † Hokkaido University. ‡ Tokyo University of Agriculture and Technology. § Fisheries Research Agency. 10.1021/es0701863 CCC: $37.00 Published on Web 06/15/2007

 2007 American Chemical Society

Although there is a large diversity of seabird species distributed widely across the globe, only a small number of species from a limited area have been studied in regard to their accumulation of POPs. Most studies have been concentrated in freshwater areas and the continental coast of Europe and North America (1-5). However, few available data have been derived from pelagic species nesting on oceanic islands (6-9). This is largely due to the ethical, practical, and technical difficulties in obtaining samples, particularly from oceanic birds. Carcasses were sampled in most of previous studies for analysis for POPs (2, 3, 6-9). However, this is a passive approach, and systematic sampling is difficult to plan. Several methods have been proposed for taking samples from living birds, focusing on blood (10), droppings (11), feathers (12, 13), and preen gland oil (14, 15). Finkelstein et al. (10) measured PCBs in blood of seabirds sampled in Hawaii. Blood sampling, however, requires trained technical skill, without which the birds, especially small ones, suffer severe stress during sample collection. Penguin droppings were used to study pollution by organochlorine pesticides in Antarctica (11). Collection of droppings is noninvasive, but preservation and transport of the samples require cooling, which could be a problem in remote areas, especially in hot climates. Jaspers et al. (12, 13) evaluated the usefulness of feathers as a nondestructive biomonitoring tool. Feathers are easily carried and preserved. Another noninvasive biomonitoring tool, preen gland oil, has been proposed (14, 15). Oil secreted from the preen gland (located at the base of the tail feathers) of seabirds protects the body from water and parasites. Concentration ranges of PCBs in the preen gland oil were previously reported (14, 15). Relationships between PCB concentrations in the preen gland oil and the corresponding adipose tissue have been reported, but for only a single species. The method’s applicability to more diverse species of seabirds, therefore, has remained questionable. In the present study, we analyzed 30 seabirds (2 orders, 3 families, 10 genera, 13 species) for PCBs using preen gland oil and internal tissue and found a positive relationship between PCB concentrations in the oil and in the corresponding internal tissue. This has dramatically increased the applicability of this monitoring methodology to a diversity of seabirds. Thus, we propose a nondestructive method for global POP monitoring by utilizing oils secreted from the preen glands of seabirds.

Materials and Methods Preen gland oil and abdominal adipose samples were obtained from birds killed in traffic accidents or caught in experimental drift nets and long-lines from 1999 to 2006 in the North Pacific Ocean (Figure 1, Table 1). Preen gland oil (∼50 mg) was obtained by wiping the gland with a paper wipe (205 mm × 120 mm; Kimwipe S 200; Nippon Paper Crecia, Japan). Although glass tools have been proposed to collect preen gland oil (16,17), a paper wipe was used in the present study because the handling and transport is simple and safe in the field. Abdominal adipose was taken by dissection using a stainless steel knife. From two individuals out of 30, blood was collected using a solvent-rinsed glass syringe with stainless-steel needle. The details of the analytical procedure is available in the Supporting Information. Briefly, the oil with the paper wipe was extracted by pressurized solvent extraction, abdominal adipose tissue was macerated and extracted using a homogenizer, and the blood samples were liquid-liquid extracted. PCB concentrations in the VOL. 41, NO. 14, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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ducibility and recovery were confirmed through four replicate analyses of an abdominal adipose tissue sample with and without standard spiking. The relative standard deviations of concentrations of individual PCB congeners were less than 5.8%, and the recoveries were more than 96%. The lipid contents were determined gravimetrically after aliquots of the sample extracts were evaporated to complete dryness. For statistical analysis, SPSS 14.0 J software was used.

Results and Discussion

FIGURE 1. Locations of stations sampled for seabirds in 1999-2006. (O) sampling locations in the Bering Sea; (b) sampling locations in the North Pacific (excluding the Bering Sea). extracts were measured using a gas chromatograph equipped with electron capture detector (GC-ECD) following intensive cleanup using two-step column chromatography. Twenty PCB congeners (IUPAC numbers 8/5, 28, 52, 44, 90/101, 110/ 77, 118, 132/153, 138/160, 187, 128, 180, 170/190, and 206) were identified and quantified. Sum of the concentrations of the 20 PCB congeners are expressed as ∑20 PCB in the present study. Typical gas chromatograms are shown in the Supporting Information (Figure S1). A procedural blank including extraction of blank Kimwipe and whole purification procedure was run with every batch (normally seven samples). The limit of quantification (LOQ) was set at 2 times the detected amount in the procedural blank. Only values above the LOQ are listed in Table 1 and discussed. Repro-

PCBs were detected in all preen gland oil samples (Table 1). The ∑20 PCB (sum of the concentrations of the 20 congeners) ranged from 9 to 4834 ng/g-lipid, with geometric mean of 404 ng/g-lipid (Figure 2). This range encompasses PCB concentrations in preen gland oil previously reported (cape petrel, Daption capense: geometric mean 600 ng/g-fat, range 320-2170 ng/g-fat (14); southern fulmar, Fulmarus glacialoides: 80-1000 ng/g (18); Ade´lie penguin, Pygoscelis adeliae: 100-800 ng/g (18)). The PCB concentrations in the oil were significantly lower than those in the corresponding adipose (two-tailed paired t test based on logarithmic data, t ) 1.68, P < 0.05, Figure 2). We found a compositional difference in PCBs between the oil and the abdominal adipose. As shown in Figure 3, the preen gland oil was relatively richer in lower-chlorinated congeners than the adipose. The proportion of lowerchlorinated homologues (di-, tri-, and tetra-CB) was 14.2 ( 13.9% (n ) 30) in the oil, but only 4.3 ( 4.0% (n ) 30) in the abdominal adipose. Larsson and Lindegren (19) also recorded relative enrichment of lower-chlorinated congeners in preen gland oil. This difference can be explained by less metabolic transformation of PCBs in the preen gland oil owing to their shorter residence time in the body. Guruge et al. (7)

TABLE 1. Biometric Data and Total PCBs Concentration of Alcidae and Procellariiformes from the North Pacific Ocean sample no. Alcidae least auklet ancient murrelet ancient murrelet ancient murrelet thick-billed murre thick-billed murre thick-billed murre rhinoceros auklet rhinoceros auklet rhinoceros auklet tufted puffin tufted puffin tufted puffin horned puffin horned puffin horned puffin Procellariiformes Laysan albatross Laysan albatross Laysan albatross northern fulmar northern fulmar northern fulmar streaked shearwater streaked shearwater streaked shearwater mottled petrel Buller’s shearwater short-tailed shearwater short-tailed shearwater sooty shearwater

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

body weight no. (g)

∑20 PCBb in ∑20 PCBb preengland oil in adipose (ng/g-lipid) (ng/g-lipid)

species

sampling date

location latitude, longitude

Aethia pusilla Synthliboramphus antiquus Synthliboramphus antiquus Synthliboramphus antiquus Uria lomvia Uria lomvia Uria lomvia Cerorhinca monocerata Cerorhinca monocerata Cerorhinca monocerata Fratercula cirrhata Fratercula cirrhata Fratercula cirrhata Fratercula corniculata Fratercula corniculata Fratercula corniculata

30/12/2005 13/6/2002 2/11/1999 4/11/1999 2/7/2005 3/7/2005 10/7/2005 6/6/2005 6/6/2005 6/6/2005 1/7/2005 10/7/2005 20/6/2005 16/6/2005 1/7/2005 20/6/2005

44° 25′ N, 141° 20′ E 44° 00′ N, 155° 00′ E 42° 00′ N, 143° 40′ E 41° 53′ N, 144° 43′ E 56° 30′ N, 180° 00′ 57° 30′ N, 180° 00′ 57° 30′ N, 178° 00′ W 44° 25′ N, 141° 20′ E 44° 25′ N, 141° 20′ E 44° 50′ N, 141° 35′ E 55° 30′ N, 180° 00′ 57° 30′ N, 178° 00′ W 45° 00′ N, 180° 00′ 41° 00′ N, 180° 00′ 55° 30′ N, 180° 00′ 45° 00′ N, 180° 00′

B F D E Ma Ka La B B A Na La Q R Na Q

76 257 285 366 1092 1107 948 599 663 598 775 856 775 549 708 663

323 454 141 120 180 102 324 815 1289 1037 362 783 728 446 291 1317

908 641 342 82 290 615 837 4172 5383 1268 600 1677 1237 326 741 274

Diomedea immutabilis Diomedea immutabilis Diomedea immutabilis Fulmarus glacialis Fulmarus glacialis Fulmarus glacialis Calonectris leucomelas Calonectris leucomelas Calonectris leucomelas Pterodroma inexpectata Puffinus bulleri Puffinus tenuirostris Puffinus tenuirostris Puffinus griseus

22/6/2004 19/5/2005 16/5/2006 1/7/2005 26/6/2005 10/6/2005 6/10/2005 6/10/2005 6/10/2005 2/7/2004 1/7/2004 13/6/2002 3/7/2005 15/6/2002

47° 00′ N, 180° 00′ 38° 00′ N, 155° 00′ E 41° 00′ N, 155° 00′ E 55° 30′ N, 180° 00′ 55° 30′ N, 180° 00′ 51° 30′ N, 180° 00′ 34° 00′ N, 139° 00′ E 34° 00′ N, 139° 00′ E 34° 00′ N, 139° 00′ E 55° 30′ N, 180° 00′ 41° 00′ N, 165° 00′ E 44° 00′ N, 155° 00′ E 57° 30′ N, 180° 00′ 43° 30′ N, 155° 00′ E

P 2870 I 2430 H 3260 Na 769 a N 640 a O 592 C 553 C no data C 484 Na 269 J 474 F 555 Ka 639 G 836

523 165 412 2924 1137 1372 219 594 377 4834 219 34 985 9

10307 936 295 2061 1219 645 182 352 585 4711 504 1640 43 90.

a Sampling locations in the Bering Sea. No mark: sampling locations in the North Pacific (excluding the Bering Sea). of 20 PCB congeners (IUPAC nos. 8/5, 28, 52, 44, 90/101, 110 (77), 118, 132/153, 138/160, 187, 128, 180, 170/190, 206).

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b

Sum of concentrations

FIGURE 2. ∑20 PCB in preen gland oil (left) and abdominal adipose tissue (right) in the Alcidae and Procellariiformes.

documented that PCBs in adipose of seabirds are depleted in lower-chlorinated congeners through basic metabolism. We also found depletion of the lower-chlorinated congeners in the adipose, confirming the progression of PCB metabolism in the body of the seabirds. The higher proportion of lowerchlorinated (i.e., more metabolizable) congeners in preen gland oil than in adipose is probably a result of the PCBs in the oil having less opportunity to undergo chemical transformation before they were secreted from the gland. Our analytical results of PCBs in blood, which have shorter retention time in the body than those in adipose, from the same birds support this idea. The PCB compositions of the blood samples were similar to those in the preen gland oil (sample no. 28, short-tailed shearwater Puffinus tenuirostris, Pearson’s r ) 0.996, P < 0.0001; sample no. 30, sooty shearwater Puffinus griseus, Pearson’s r ) 0.890, P < 0.0001), and were relatively rich in lower-chlorinated congeners (Figure S2). To further assess the differences in the degrees of metabolism, we selected three independent congeners with different metabolic capacities, i.e., CB44, CB110, and CB180, and calculated their ratios. CB44 and CB110 have two types of connected, nonchlorine-substituted carbons, i.e., meta-para carbons (P area) and ortho-meta carbons (M area), and are susceptible to metabolism (20). PCB congeners with P and M areas, which enable the formation of epoxide, the initial reaction of PCB metabolism, are metabolized by phenobarbital (PB)- and 3-methylcholanthrene (MC)-induced microsomes, respectively. On the other hand, CB180 has no connected, nonchlorinesubstituted carbons, and is resistant to metabolism (20).

The concentration ratio of CB44 + CB110 to CB180 was higher in preen gland oil than in adipose of all birds examined (Figure 4) except one (no. 20). All the compositional parameters indicate that PCBs in the preen gland oil were less metabolized. Relative enrichment of lower-chlorinated congeners has also been reported in feces of chicken relative to internal tissues (breast, thigh, and adipose) (21). Furthermore, feathers of seabirds contained a greater contribution of lowerchlorinated congeners to their PCB profiles (12, 13), although this was attributed to external contamination of PCBs on the feather surface. However, spreading preen gland oil on feathers could explain the similar congener composition (i.e., relative abundance in lower-chlorinated congeners) in preen gland oil and feathers. Because preen gland oil samples are obtained directly from the preen gland and have little contact with ambient air and seawater, preen gland oil PCBs have little external contamination. We can conclude that preen gland oil accumulates PCBs that have had little opportunity to be metabolized, thus reflecting recent exposure to PCBs. We found a significant but weak correlation (R2 ) 0.19, P < 0.05) between the PCB concentrations in the preen gland oil and in the adipose tissue (Figure 5). Poor correlation is partly derived from the combination of different species with different capacities to metabolize PCBs, dietary behaviors, and migration habits. Van den Brink (14) found a good correlation (R2 ) 0.75, n ) 6) between preen gland oil and subcutaneous fat in a single species of seabird (cape petrel). When two groups (i.e., Alcidae and Procellariiformes) were separately examined, we obtained a better correlation for the Alcidae (i.e., R2 ) 0.39, P ) 0.01), but a weaker correlation for the Procellariiformes (R2 ) 0.14, P ) 0.19). Furthermore, excluding nos. 17-19 Laysan albatross, Diomedea immutabilis, and examination of the single family (i.e., Procellariidae) brought no improvement of the correlation (R2 ) 0.19, P ) 0.18). This weaker correlation may be attributable to the diversity in the migration habits of the Procellariiformes: some species migrate long distances, while others stay in a limited area. Combining all these species may have decreased the correlation for the Procellariiformes. The effect of migration is discussed further down. As shown in Figure 4, the ratio of (CB44 + CB110) to CB180 was highly variable among species and even among individuals in a single species. This indicates that the degree of metabolism of PCBs in individual birds was highly variable. These different metabolisms among individuals are an important factor in reducing the correlation. To correct for metabolic loss of congeners, we utilized these three congeners, which have different metabolic capacities, and conducted multiple regression analysis. Statistical analysis gave the following equation, which estimates PCB concentration in adipose based on concentrations of CB44, CB110, and CB180 in preen gland oil:

log

Σ20 PCB

ad

) 0.49 × logCB180pgo + 0.43 × logCB110pgo - 0.59 × logCB44pgo + 2.24

(R2 ) 0.48, P < 0.001, Figure 6) where ∑20 PCBad is the ∑20 PCB in adipose tissue; and CB180pgo, CB110pgo, and CB44pgo are the PCB concentrations in preen gland oil. The estimated PCB concentrations in the adipose tissue correlated strongly with the measured PCB concentrations in the adipose tissue. This correlation means that PCB concentrations in the internal adipose tissue can be estimated from a congener-specific analysis of PCBs in the preen gland oil within 1 order of magnitude difference. Again, much higher correlation was obtained for Alcidae VOL. 41, NO. 14, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 3. PCB congener compositions of preen gland oils (left) and abdominal adipose tissue (right) in the Alcidae (upper) and Procellariiformes (lower) (*may contain trace concentrations of CB77). when the two groups (Alcidae and Procellariiformes) were separately examined as below:

log

Σ20 PCB

ad ) 0.98 × logCB180pgo + 0.77 × logCB110pgo - 1.07 × logCB44pgo +

1.79 (R2 ) 0.83, P < 0.0001); for Alcidae log

Σ20 PCB

ad ) 0.45 × logCB180pgo + 0.33 × logCB110pgo - 0.55 × logCB44pgo +

2.25 (R2 ) 0.45, P ) 0.10); for Procellariiformes We found differences in PCB concentrations in preen gland 4904

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oil among species. As Figure 2 shows, the PCB concentrations in Procellariiformes oil were more variable than those in Alcidae (F test based on logarithmic data, F15,13 ) 0.41, P < 0.01). This may be explained by behavioral factors: Procellariiformes make long-range migrations between the northern and southern hemispheres and, therefore, are exposed to wider levels of PCBs, while the Alcidae remain in a limited area (northern North Pacific). PCB concentrations in subcutaneous fat from albatrosses (Procellariiformes) residing in the northern hemisphere (Laysan albatross, Diomedea immutabilis, 21 000 ng/g wet weight) were 1 order of magnitude higher than those in the southern hemisphere

FIGURE 4. Ratio of concentrations of CB44 + CB110 to CB180 in the preen gland oil of Alcidae and Procellariiformes.

FIGURE 5. ∑20 PCB in the preen gland oil of the Alcidae (b) and Procellariiformes (O) correlated with those in adipose tissue.

were comparable to or lower than those from the northern North Pacific (sample nos. 1-4, 8-10, 13, 14, 16; geometric mean 509 ng/g-lipid; two-tailed t test based on logarithmic data, t ) 2.16, P ) 0.15). However, preen gland oil PCB concentrations in Procellariiformes from the Bering Sea (sample nos. 20-22, 26, 29; geometric mean 1851 ng/g-lipid) were significantly higher than those from the northern North Pacific (sample nos. 17-19, 23-25, 27, 28, 30; geometric mean 170 ng/g-lipid; two-tailed t test based on logarithmic data, t ) 2.18, P ) 0.001). Species differences in both trophic levels and migration pattern might affect PCB concentrations. mottled petrel (Pterodroma inexpectata; sample no. 26: 4834 ng/g-lipid) and northern fulmar (Fulmarus glacialis; sample no. 20: 2924 ng/g-lipid; Table 1) collected from the Bering Sea had the highest PCB concentrations in their preen gland oil. Both species feed mainly on cephalopods (22), which greatly accumulate PCBs by biomagnification. Northern fulmars feed also on garbage (23) contaminated with PCBs. Many Procellariiformes species, including mottled petrel and short-tailed shearwater (Puffinus tenuirostris), migrate from the southern hemisphere to the North Pacific (22). During migration they suffer starvation, and lipids are depleted. As a result, persistent xenobiotics such as PCBs can be concentrated (8). Because of a complex combination of multiple factors, strategic collection of much larger numbers of samples and their analysis is necessary to make more concrete conclusions. The noninvasive methodology using preen gland oil, therefore, could enable strategic and systematic collection of samples. In previous studies, the monitoring of POPs in seabirds has been limited by the availability of carcasses. However, the noninvasive sampling of preen gland oil allows for the strategic global-scale monitoring of POPs. This approach can easily be combined with ecological investigations of seabirds. This could dramatically increase the availability of seabird samples, including repeated sampling on identical birds. Recently, electronic tracking tags have revolutionized our understanding of the large-scale movements and habitat use of mobile marine animals (10, 24). The combination of this technology in ecological research with POP analysis of preen gland oil will increase our knowledge of the global distribution and transport of POPs, their ecological impact, and the ecology and behaviors of seabirds.

Acknowledgments We thank the captains, officers, and crew onboard the R/V Wakatake-maru (Hokkaido prefecture) and T/S Oshoro-maru (Hokkaido University) for help with sample collection. This work was supported by the Promotion Program for International Resources Survey from the Fisheries Agency of Japan and Grant-in-Aid from the Ministry of Education of Japan (project no.19651003).

Supporting Information Available FIGURE 6. Relationship between predicted and measured adipose tissue concentrations of PCBs.(b) Alcidae; (O) Procellariiformes. (black-browed albatross, Diomedea melanophris, 1200 ng/g wet weight) (6)). This difference is ascribed to regional differences in ambient PCB concentrations (6), which may contribute to the large variability in PCB concentrations in the Procellariiformes. Higher concentrations of PCBs had been reported in tissues of seabirds that feed near industrialized areas (e.g., near North America) than in those that feed in remote areas (e.g., Bering Sea) (10). As shown in Figure 2, preen gland oil PCB concentrations in the Alcidae from the Bering Sea (sample nos. 5-7, 11, 12, 15; geometric mean 281 ng/g-lipid)

Details of analytical method, Figures S1 (gas chromatograms of PCBs in commercial standard, adipose, preen gland oil and procedural blank) and S2 (relative abundance of PCB congeners in preen gland oil, blood and adipose). This material is available free of charge via the Internet at http:// pubs.acs.org.

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Received for review January 24, 2007. Revised manuscript received May 12, 2007. Accepted May 14, 2007. ES0701863