Polychlorinated biphenyls and organochlorine pesticides in local waterbird eggs from Hong Kong: Risk assessment to local waterbirds

Chemosphere 83 (2011) 891–896

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Polychlorinated biphenyls and organochlorine pesticides in local waterbird eggs from Hong Kong: Risk assessment to local waterbirds Yuan Wang a,b, Margaret B. Murphy b, James C.W. Lam b, Liping Jiao c,d, Captain C.L. Wong e, Leo W.Y. Yeung b,1, Paul K.S. Lam b,⇑ a

Jiangsu Academy of Environmental Science, No. 241 Fenghuang West Road, Nanjing 210036, People’s Republic of China State Key Laboratory in Marine Pollution, Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong SAR, People’s Republic of China Third Institute of Oceanography, State Oceanic Administration, No. 174, Daxue Road, Xiamen 361005, People’s Republic of China d Key Laboratory of Global Change and Marine-Atmospheric Chemistry, State Oceanic Administration, 178 Daxue Road, Xiamen, Fijian, People’s Republic of China e Kadoorie Farm and Botanic Garden (KFBG), Lam Kam Road, Tai Po, New Territories, Hong Kong SAR, People’s Republic of China b c

a r t i c l e

i n f o

Article history: Received 8 October 2010 Received in revised form 25 February 2011 Accepted 27 February 2011

Keywords: PCBs Organochlorinated pesticides Waterbird egg DDT Risk assessment

a b s t r a c t The contamination status of the marine environment in Hong Kong was studied by measuring concentrations of organochlorine (OC) pollutants (i.e., hexachlorobenzene, aldrin, dieldrin, endrin, mirex, total heptachlor, total chlordane, total DDTs, total PCBs, and total toxaphenes) in the eggs of selected waterbird species from different locations around the city: Little Egret (Egretta garzetta) and Chinese Pond Heron (Ardeola bacchus) from Mai Po Village, Great Egret (Ardea alba) and Black-crowned Night Heron (Nycticorax nycticorax) from A Chau, and Chinese Pond Heron (A. bacchus) from Ho Sheung Heung. The mean concentrations of total PCBs and total DDTs ranged from 191–11 100 ng g1 lipid and 453–49 000 ng g1 lipid, respectively. Recent exposure of waterbirds to technical chlordane was found in Hong Kong. The risk characterization demonstrated potential risks to birds associated with exposure to DDE, which was found to cause a reduction in survival of young in Hong Kong Ardeids based on the endpoint in the risk assessment. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction The manufacture, use and subsequent release of persistent organic pollutants (POPs) pose a long-term threat to the environment all over the world because they are bioaccumulative, widely distributed and potentially toxic (Wania and MacKay 1996; Sabljic, 2001). These characteristics led to the implementation of the Stockholm Convention in 2001, aiming at the global restriction of the production or use of POPs so as to protect human health and the environment from these potentially harmful substances. Coastal waters in Hong Kong receive a large amount of wastewater resulting from the rapid economic development and human population expansion occurring in the Pearl River Delta (PRD) region (Fu et al., 2003). In the recent years, there is increasing evidence that the Mai Po Marshes Nature Reserve (MPMNR) and Inner Deep Bay, situated at the boundary of the northwestern part of Hong Kong, are under threat from a wide range of environmental contaminants. Sediments from the Mai Po Marshes have been found to have elevated concentrations of polybrominated diphenyl ⇑ Corresponding author. Tel.: +852 2788 7681; fax: +852 2788 7406. E-mail address: [email protected] (P.K.S. Lam). Present address: 80 St. George Street, University of Toronto, Toronto, Ontario, Canada M5S 3H6. 1

0045-6535/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2011.02.073

ethers (Shi et al., 2009), polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/Fs) (Muller et al., 2002; Zhang et al., 2009), and polycyclic aromatic hydrocarbons (PAHs) (Zheng et al., 2002; Choi et al., 2009). Organochlorine (OC) pesticides and polychlorinated biphenyls (PCBs) were detected in various environmental matrices such as air, water, sediment, and marine organisms in the PRD (Fu et al., 2003). Greater OC concentrations were measured in sediments from mudflats at MPMNR (7–96 ng g1 dry weight (d.w.)) than in those from A Chau (3.4– 5.7 ng g1 d.w.), a remote island in Starling Inlet which serves as a breeding ground for several waterbird species, however, lower concentrations of OCs (i.e., when compared with the relevant guideline values suggested by government agencies) were found in biota samples (i.e., fish, shrimp, polychaetes) from the mudflats (Wong et al., 2006). Although the production and usage of OC compounds has been forbidden in Hong Kong and China since the 1980s (Wong et al., 2005), the continual input of these compounds into the environment could arise from the usage of OC-containing products. Against such a background, it is conceivable that organisms at higher trophic levels, such as waterbirds, are exposed to relatively high concentrations of these environmental contaminants. Waterbirds are valuable for environmental monitoring because they are long-lived and highly mobile, and thus they integrate pollutants over a broad area (Furness, 1993). Since a large

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proportion of OC compounds are known to biomagnify in the eggyolk (Kleinow et al., 1999), contaminant levels in waterbird eggs serve as an important tool for monitoring changes in the environmental quality. In addition, collection of eggs is a relatively noninvasive technique that has minimal adverse effects on the bird community (Connell et al., 2003). Dong et al. (2004) measured residues of dichlorodiphenyltrichloroethane (DDT) and hexachlorocyclohexane (HCH) in eggs of waterbirds and their prey from Tai Lake in China, and a recent study detected several persistent halogenated compounds in muscles of several species of waterbirds from an e-waste recycling region from the Pearl River Delta (Luo et al., 2009). The results from both studies suggest that the residues levels among waterbird species were species-, habitat-, and dietspecific. In our earlier study, PCBs, dichlorodiphenyltrichloroethane (DDT), and chlordane were detected in waterbird eggs in Hong Kong (Connell et al., 2003). However, information on other OC contaminants such as toxaphene and PCDD/Fs found in the egg tissues is still very limited. In view of this, the objectives of the present study were to establish more complete baseline information on the ten OC contaminants listed under the Stockholm Convention in bird eggs, and to assess the risk of these contaminants to waterbirds based on the concentrations determined in the eggs of selected species in Hong Kong. 2. Materials and methods 2.1. Collection of eggs Fresh egg samples were collected from five resident egretries in Hong Kong following conditions stipulated by the Hong Kong Agriculture, Fisheries and Conservation Department (AFCD) over the period from March to April in 2006. These included 16 Great Egret (Egretta alba) eggs and 16 Night Heron (Nycticorax nycticorax) eggs from A Chau, 12 Chinese Pond Heron (Ardeola bacchus) eggs from Ho Sheung Heung, four Little Egret (Egretta garzetta) eggs from Mai Po Village, 5 Chinese Pond Heron eggs from Mai Po Lung Village and three Little Egret eggs from Pak Nai (Supplementary material Fig. S1). Three additional Little Egret eggs from Mai Po Village collected in 2000 were also analyzed for OC contaminants. Eggs collected were wrapped in aluminum foil, and individually labeled. The eggs were transferred to pre-cleaned glass jars and stored at 20 °C in the laboratory for subsequent analyses. 2.2. Chemical analysis Quantification of organochlorines (hexachlorobenzene (HCB), aldrin, dieldrin, endrin, mirex, total heptachlor, total chlordane, total DDT, total PCB, and total toxaphene) was accomplished by use of previously established methods (Hung et al., 2006; Lam et al., 2008), with modifications; details can be found in the Supplementary material. 2.3. Quality control and quality assurance A sequence table was established for each batch of samples, which comprised a standard mixture, five samples, one procedural blank and one solvent blank. With every batch, a mixture consisting of known concentrations of internal standards was injected into the GC before sample injection. Accuracy and precision of OC analysis were determined by use of spiked recoveries and fish certified reference materials (CRM: BCR598, cod liver oil, Institute for Reference Materials and Measurements) included with every 10 samples. Spiked standards and CRM recovery rates obtained by this procedure ranged from 95–108% and 89–112% for total PCBs and chlori-

nated pesticides, respectively. The recovery of toxaphene in the spiked recovery samples ranged from 77–95% for the heptahomologue, 80–92% for the octa-homologue, 75–80% for the nona-homologue, 94–95% for P26, 86–92% for P32, 77–89% for P50 and 85–95% for P62. 2.4. Statistical analysis Differences in the concentrations of PCB congeners and OC pesticides among egretries/locations were statistically analyzed, and the details can be found in the Supplementary material.

3. Results and discussion 3.1. Concentrations of OC contaminants Concentrations of OC contaminants in the eggs of Night Heron, Great Egret, Chinese Pond Heron and Little Egret from egretries in Hong Kong are summarized in Table 1. Since there were no significant differences between the concentrations found in the egg samples for Mai Po Village, Mai Po Lung Village and Pak Nai, the data for the egg samples collected from 2006 were pooled together for comparison under ‘‘Mai Po Village’’. No significant temporal variation was found in concentrations of the OC contaminants except for heptachlor, for which the mean concentration in egg samples from Mai Po Village collected during 2000 (75.3 ng g1 lipid weight (wt.)) was significantly greater than those samples collected in 2006 (12.7 ng g1 lipid wt.) (Mann– Whitney Rank Sum Test: p = 0.031) (Table 1). The greatest mean concentrations of total PCBs (4310 ng g1 lipid wt.), total toxaphene (295 ng g1 lipid wt.), endrin (31.3 ng g1 lipid wt.) and total chlordane (975 ng g1 lipid wt.) were detected in the eggs from Mai Po Village 2006, whereas those for total heptachlor (99.8 ng g1 lipid wt.) and aldrin (8.41 ng g1 lipid wt.) were measured in the eggs from Ho Sheung Heung. Night Heron eggs from A Chau contained the lowest concentrations of most of the contaminants including total PCBs, total chlordane, total heptachlor, total DDTs, dieldrin, endrin, aldrin, mirex and total toxaphenes. However, these egg samples contained the greatest mean concentration of HCB, which was significantly greater than that of the Great Egret eggs collected from the same location (Kruskal– Wallis Test: p < 0.05). Although the greatest mean concentration of total toxaphenes was quantified in the eggs from Mai Po Village, the greatest P26 (0.778 ng g1 lipid wt.) and P50 (0.849 ng g1 lipid wt.) concentrations were measured in Great Egret eggs from A Chau. These egg samples also contained the greatest mean concentration of total DDTs, which was statistically greater than the concentrations in Night Heron eggs from the same location and those collected from Mai Po Village and Ho Sheung Heung (Kruskal–Wallis Test: p < 0.05). No significant spatial variation in mirex concentrations were observed in the eggs collected from A Chau, Ho Sheung Heung and Mai Po Village (Kruskal–Wallis Test: p = 0.062). 3.2. Differences in OC concentrations among egretries This study revealed that the concentrations of total PCBs, toxaphenes, endrin and total chlordanes were significantly greater in eggs from Mai Po Village than eggs of Night Heron from A Chau (Mann–Whitney Rank Sum Test: p < 0.05) (Table 1). These results suggest spatial variation in the levels of trace organic pollution between the eastern and western areas of Hong Kong that are reflected in the different exposure levels of waterbird inhabiting these parts of the city.

Table 1 Concentrations (mean ± SD, ng g1 lipid wt.) of organochlorine contaminants in bird eggs from Hong Kong egretries. 2000

2006

Location

Mai Po Village

A Chau

Mai Po Village

Ho Sheung Heung

Bird species

Little Egret

Night Heron

Great Egret

Little Egret and Chinese Pond Heron

Chinese Pond Heron

Lipid (%) Total PCBs Cis-chlordane Trans-chlordane Cis-nonachlor Trans-nonachlor oxychlordane Total chlordane Heptachlor Heptachlor epoxide Total heptachlor p,p0 -DDT p,p0 -DDE p,p0 -DDD o,p0 -DDT o,p0 -DDE o,p0 -DDD Total DDTs Dieldrin Endrin Aldrin HCB Mirex P32 P26 P62 P50 Total toxaphenes

10.2 ± 3.05 (7.31–13.4) 4640 ± 2200 (2220–6510) 162 ± 124 (21.8–257) 24.6 ± 17.5 (7.92–42.8) 419 ± 273 (109–622) 922 ± 597 (247–1380) 643 ± 516 (89–1110) 2170 ± 1470 (475–3080) 4.23 ± 1.41 (2.61–5.19) 71.0 ± 51.3 (15.2–116) 75.3 ± 52.6 (17.8–121) 334 ± 182 (124–444) 3340 ± 1960 (1090–4590) 108 ± 73.6 (23.9–162) 3.48 ± 2.57 (0.539–5.31) 73.4 ± 46.3 (20.0–103) 25.0 ± 15.4 (10.6–41.2) 3890 ± 2270 (1270–5330) 111 ± 26.9 (80–130) 64.5 ± 39.5 (19.6–94.0) 13.9 ± 24.1 (<0.02–41.8) 128 ± 27.2 (97.4–150) 271 ± 202 (57.3–458) <0.2 1.36 ± 0.437 (0.859–1.63) <5.0 1.69 ± 0.0808 (1.64–1.78) 703 ± 413 (236–1020)

6.99 ± 0.888 (5.60–8.50) 881 ± 930 (191–3470) 4.57 ± 8.23 (0.435–34.2) 2.97 ± 6.21 (0.389–26.1) 38.8 ± 58.1 (2.03–206) 81.0 ± 117 (3.34–355) 31.1 ± 42.5 (0.762–135) 158 ± 225 (9.95–722) 1.09 ± 1.55 (0.101–6.06) 6.71 ± 9.99 (0.0364–34.7) 7.81 ± 11.1 (0.448–40.8) 94.3 ± 71.0 (16.3–238) 2340 ± 2160 (428–8940) 23.5 ± 29.2 (2.40–97.5) 1.46 ± 3.64 (0.0533–14.7) 17.2 ± 16.0 (3.70–66.4) 11.2 ± 14.3 (1.01–61.5) 2490 ± 2200 (453–9160) 8.36 ± 7.25 (0.370–25.4) 9.32 ± 18.8 (0.429–74.9) 0.492 ± 1.49 (0.0584–6.07) 241 ± 471 (37.3–1940) 84.2 ± 80.7 (15.5–295) <0.2 0.380 ± 0.477 (<0.2–1.93) <5.0 0.376 ± 0.553 (<0.200–1.89) 36.1 ± 72.6 (2.36–289)

6.54 ± 1.10 (4.98–8.59) 2040 ± 1160 (923–5220) 23.4 ± 5.75 (16.9–36.5) 3.18 ± 2.06 (<0.02–7.60) 54.6 ± 30.3 (32.7–140) 160 ± 110 (77.2–466) 108 ± 61.4 (27.8–254) 348 ± 193 (178–887) 0.649 ± 0.43 (0.180–1.73) 24.2 ± 11.8 (5.07–46.3) 24.8 ± 12.0 (5.46–48.0) 2390 ± 1670 (486–6000) 12 400 ± 3910 (7000–20 000) 1030 ± 329 (468–1510) 39.0 ± 11.4 (21.8–60.7) 244 ± 69.3 (147–358) 86.8 ± 41.0 (20.6–160) 16 100 ± 5690 (8970–28 000) 71.1 ± 30.4 (9.89–127) 17.5 ± 9.22 (4.97–32.3) 0.553 ± 0.454 (<0.02–1.45) 40.2 ± 19.9 (26.6–102) 107 ± 61.6 (55.6–312) <0.2 0.778 ± 0.325 (0.371–1.54) <5.0 0.849 ± 0.659 (<0.200–2.53) 212 ± 175 (67.9–791)

7.19 ± 1.44 (5.73–11.6) 4310 ± 4230 (451–11 100) 98.0 ± 161 (0.610–455) 11.8 ± 15.9 (<0.02–53.5) 237 ± 290 (8.79–779) 505 ± 628 (12.7–1670) 124 ± 92.5 (12.5–295) 975 ± 1140 (38.2–3160) 1.24 ± 1.09 (0.158–4.24) 11.5 ± 14.3 (0.034–46.2) 12.7 ± 14.6 (0.534–48.4) 816 ± 1360 (41.2–4420) 8070 ± 13 200 (551–44 400) 132 ± 256 (4.21–759) 23.2 ± 54.4 (<0.02–164) 128 ± 249 (0.985–851) 52.5 ± 104 (<0.02–289) 9220 ± 15 100 (601–49 000) 114 ± 209 (1.45–707) 31.3 ± 41.6 (1.73–139) 2.10 ± 3.76 (<0.02–12.3) 91.2 ± 79.9 (8.03–244) 255 ± 297 (31.3–905) <0.2 0.616 ± 1.33 (<0.200–4.49) <5.0 0.753 ± 1.31 (<0.200–3.87) 295 ± 372 (2.39–1080)

6.65 ± 0.562 (5.26–7.46) 1220 ± 690 (413–2590) 40.1 ± 46.9 (1.79–134) 6.46 ± 7.3 (0.67–27.7) 88.6 ± 76.0 (10.3–286) 233 ± 157 (14.1–529) 200 ± 168 (9.6–633) 567 ± 377 (36.5–1250) 0.487 ± 0.596 (<0.02–2.22) 99.4 ± 130 (0.717–465) 99.8 ± 130 (0.796–466) 230 ± 233 (35.3–793) 4320 ± 5790 (345–20 500) 96.0 ± 121 (3.40–354) 27.5 ± 70.5 (0.175–247) 68.0 ± 55.2 (2.27–214) 25.3 ± 35.6 (0.956–98.3) 4760 ± 6110 (400–21 800) 42.5 ± 36.7 (2.11–126) 9.71 ± 9.09 (1.4–34.4) 8.41 ± 13.7 (0.0849–48.5) 61.6 ± 44.0 (14.0–158) 126 ± 172 (6.54–641) <0.2 0.442 ± 0.540 (<0.200–1.46) <5.0 0.552 ± 1.17 (<0.200–4.01) 188 ± 256 (2.86–762)

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Sampling year

893

894

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The proximity of Mai Po Village to the Yuen Long Industrial Estate, as well as the industrial and agricultural activities across the border in the Shenzhen area, may have contributed to the higher levels of OC contaminants in eggs collected from that area. Although it is claimed that more than 98% of industrial wastewater is treated before discharge in Shenzhen, it should be noticed that there may be illegal discharges from small-scale industrial premises located outside the urban area of Shenzhen (Ho and Hui, 2001), thus adversely affecting the western part of the New Territories. It is anticipated that the OC contaminants that have persisted in the soils and sediments will continue to be an important source of contaminants in this part of south China. Indeed, greater quantities of PCBs were detected in sediments from Deep Bay than in those from Mirs Bay, which is located on the northeastern part of the New Territories (Connell et al., 1998). On the other hand, it should be noted that the concentration of total DDTs was significantly greater in Great Egret eggs from A Chau than in waterbird eggs from Mai Po Village 2006. This observation is in contrast to that of our previous study showing a significantly greater DDT concentration in the eggs from Mai Po Village as compared to A Chau in 2000 (Lam et al., 2001). However, contaminant concentrations were only monitored in Night Heron eggs in A Chau during 2000. Differences in feeding habits and foragingflight distances between Great Egrets and Night Herons may account for the variation in body burdens of contaminants. 3.3. Differences in OC concentrations between species The results of the present study revealed different bioaccumulation potentials among the bird species studied. The body burdens of OCs in Great Egret eggs were, in general, greater than those of Night Heron collected from A Chau egretry, probably due to species differences in feeding habits, foraging-flight distances and rates of pollutant metabolism in the birds. Indeed, interspecies variation in PCB concentrations in bird eggs have been reported previously (Hoshi et al., 1998) and were largely attributed to differences in parental dietary exposure (Hoshi et al., 1998) and their abilities to metabolize trace organic pollutants (Fossi et al., 1995). The foraging flight patterns of Great Egrets and Night Herons at A Chau have been investigated in Hong Kong (Wong et al., 1999). Great Egrets were shown to have longer foraging-flight distances than Night Herons. Furthermore, Great Egrets from A Chau fed on pelagic fish from a wider range of areas, while Night Herons mostly made use of mangrove and fishpond habitats for feeding (Wong et al., 1999). These variations may thus account for the greater body burdens of OCs in Great Egrets from A Chau. 3.4. Composition profiles of DDT and chlordane in bird egg samples The profiles of relative concentrations of total p,p0 -DDT and total o,p -DDT are shown in Supplementary material Fig. S1. Most of the total DDT concentrations in the eggs were contributed by total p,p0 DDT (p,p0 -DDT + p,p0 -DDD + p,p0 -DDE). Among these isomers, p,p0 DDE and o,p0 -DDE were the dominant chemicals among the total p,p0 -DDTs and o,p0 -DDTs (o,p0 -DDT + o,p0 -DDD + o,p0 -DDE), respectively, reflecting a decrease in the fresh input of DDT to the Hong Kong environment. The low DDT/(DDE + DDD) ratios in bird species further suggested that a great proportion of DDT could be attributed to historical agricultural and public health usage rather than recent discharges (Supplementary material Fig. S3 and S4). The composition pattern in eggs was similar to those found in other environmental matrices. DDE was also found to be the dominant contributor to total DDT in sediments, soil and biota in Hong Kong (Wong et al., 2006; Cheung et al., 2007). Significant amount of DDT detected in seawater samples from Mai Po Village and A Chau indicates the possible existence of fresh 0

input of DDT to the environment (Wong et al., 2006). Sources of DDT in the environment include the application of technical DDT and DDT-containing dicofol, which differ in their p,p0 -DDT and o,p0 -DDT contents. In the present study, p,p0 -DDT (3.8–14.8%) had a greater contribution than o,p0 -DDT (0.1–0.6%) to total DDTs in the bird eggs (Table 1) indicating that DDT pollution in Hong Kong is likely to be dominated by technical DDT. Nevertheless, the use of dicofol and DDT-containing antifouling paints may become an important source of DDT in the environment in the future (Qiu et al., 2005). The present results demonstrated that trans-nonachlor was the dominant contributor to total chlordanes (41.0–51.8%), followed by cis-nonachlor (15.6–24.5%) and oxychlordane (12.7–35.2%) in all of the egg samples (Supplementary material Fig. S5). Trans-chlordane (0.91–1.88%) contributed the least to total chlordane concentrations. Similar composition profiles were also observed in mussels, Indo Pacific hump-backed dolphin (Sousa chinensis) and finless porpoise (Neophocaena phocaenoides) in Hong Kong (Minh et al., 1999). In fact, trans-nonachlor is one of the major constituents in technical chlordane and thus its presence in the environment at relatively high concentrations likely indicates recent inputs of chlordane to the environment (Eisler, 1990). The higher transchlordane/total chlordane ratio (0.41–0.52) compared to the oxychlordane/total chlordane ratio (0.13–0.35) in all egg samples in the present study implies a recent exposure of birds to technical chlordane in Hong Kong. Other studies have suggested that different chlordane ratios might result from variations in diet and therefore food chain effects (Elliott et al., 2000), and different capacities to metabolize chlordane constituents (Yamashita et al., 1993). 3.5. Comparison of OC concentrations in waterbird eggs with other relevant studies elsewhere The OC concentrations quantified in bird egg samples in the present study were compared with those in the literature (Supplementary material Table S1). Concentrations of heptachlor, aldrin and endrin in bird eggs of Hong Kong were comparable to those of waterbirds from Lake Tai in China (Dong et al., 2004). Lake Tai is known for its pollution problems due to rapid economic growth and urbanization in the surrounding area. However, these contaminant concentrations were lower than those in eggs from Northern Italy (Fasola et al., 1998). HCB levels in Hong Kong waterbird eggs were generally low when compared to other studies. Concentrations of HCB in eggs of Black-legged kittiwakes (Rissa tridactyla), Northern fulmars (Fulmarus glacialis) and Thick-billed murres (Uria lomvia) from the Canadian Arctic were higher than those in the eggs from Hong Kong (Braune et al., 2001). Interestingly, the HCB levels in Hong Kong were comparable to those measured in eggs of Adelie penguin (Pygoscelis adeliae) in Antarctica although it is a remote continent (Corsolini et al., 2006). Generally, concentrations of total chlordanes in avian eggs were comparable between different countries except for the Adelie penguin in Antarctic which showed significantly lower levels (Corsolini et al., 2006). However, it should be noted that the highest chlordane levels (mean: 43 100 ng g1 lipid wt.) were found in eggs of Little Egrets in Hong Kong (Connell et al., 2003). Information on Mirex and toxaphene is lacking in the AsiaPacific region. Dieldrin and mirex in Hong Kong avian eggs showed similar levels when compared to other studies (Braune et al., 2001; Harris et al., 2003; Champoux et al., 2006), as did toxaphene, except that a much higher concentration was found in Blackfooted albatrosses (Phoebastria nigripes) from Midway Atoll in the Pacific Ocean (Muir et al., 2002). DDT levels in waterbird eggs in Hong Kong are comparable to other studies elsewhere, including Italy, Canada, China and Alaska.

Y. Wang et al. / Chemosphere 83 (2011) 891–896

Elliot et al. (1988) reported that much higher levels of p,p0 DDE were found in northern gannets (Sula bassanus) in Canada during the 1960s and 1970s. However, temporal declines in DDE levels are not consistent, as high tissue concentrations and eggshell thinning have been reported for some bird populations in recent decades; high levels of DDT and associated metabolites were found in American robin (Turdus migratorius) eggs from Canada during the 1990s (Harris et al., 2000), and elevated DDE levels have also been measured in osprey (Pandion haliaetus) eggs collected in the Pacific Northwest region of North America (Elliott et al., 2000), though a decreasing concentration trend for some osprey populations have also been reported (Henny et al., 2008). PCB concentrations in waterbird eggs in Hong Kong were comparatively higher than the levels in eggs of Adelie penguin from Antarctica (Corsolini et al., 2006), but lower than those in Red Kites and Buzzards from Doñana National Park in Spain (Gomara and Gonzalez, 2006). In fact, the levels of PCBs were comparable to those reported for other regions, including other studies in China, eastern Canada, the Canadian Arctic, Belgium and the Baltic Sea. Recent studies also shown that low levels of PCBs might not cause any adverse biological effects (Antoniadou et al., 2007); however, PCBs might still pose some risks to other receptors (e.g. Hung et al., 2006), and thus identification and elimination of pollution sources should be carried out. 3.6. Risk to Ardeid populations due to DDE exposure In this investigation, total DDTs refers to a mixture of all the isomers with DDE predominating. The available data on the relationship of the occurrence of DDE in Little Egret and Night Heron eggs with breeding success, measured as the percentage reduction in survival of young, have been assembled from Henny et al. (1984) and Findholt and Trost (1985), and were summarized in a previous study (Connell et al., 2003). In characterizing the risk of DDE exposure to Hong Kong’s Ardeid population, derived threshold values of 1000 and 2500 ng g1 wet weight from the literature were the most relevant and thus were chosen to represent lower- and upper-limit effect thresholds (Connell et al., 2003). It is important to note that these values were derived for only two of the four species sampled in the present study, and that there are currently no species-specific thresholds available for the Chinese Pond Heron or Great Egret. The threshold values derived by Connell et al. (2003) were also based on levels measured in birds living in temperate habitats in North America, and thus there may be some differences in DDE metabolism or effects between these populations and the subtropical populations sampled in the present study. The risk

y = 55.3x -71.3 R2 = 0.906 y = 162x-419 R2 = 0.918

Derived threshold levels, (i) 1000 ngg -1 (log value 3.0) (ii) 2500 ngg -1 (log value 3.4)

Log DDE concentration (ng g -1 wet wt.)

Fig. 1. Plot of the cumulative percent probability of the occurrence of a concentration of DDE in Ardeid eggs from the three sampling locations and A Chau great egret (ACGE). The derived thresholds are the values obtained from Connell et al. (2003) based on the percent reduction in the survival of young of the Ardeid population.

895

assessment of DDE can therefore be considered to be relatively robust for the Night Heron and Little Egret, and conservative for the Chinese Pond Heron and Great Egret. A probabilistic plot was constructed for DDE concentrations found in the egg samples (Fig. 1). As the levels of DDE between the three locations (i.e., Mai Po, Ho Sheung Heung and A Chau) were not statistically different in eggs, with the exception of Great Egret from A Chau, the data from three locations were plotted together to represent the range of values of occurrence of DDE in eggs from the three sampling sites, whilst the DDE data of Great Egret from A Chau were plotted as its own distribution. The derived threshold levels of 1000 and 2500 ng g1 wet weight in eggs causing a reduction in survival of young of the Ardeid population were entered onto the plot in Fig. 1 (Connell et al., 2003). This suggests that the concentrations of 1000 ng g1 wet weight of DDE in eggs could cause the reduction of survival of young in the Ardeid communities affecting approximately 6% and 30% of the population of the three sampling sites and Great Egret respectively, whereas the maximum threshold value (2500 ng g1 wet weight) as indicated in the graph is greater than the 99.9% cumulative probability (1260 and 1530 ng g1 wet weight for the three sampling sites and Great Egret respectively) of the two Ardeid populations. Alternatively, the Monte Carlo simulation technique was undertaken to integrate both the DDE exposure and dose-response data. The exposure was assumed to be a log-normal distribution of exposure data and a threshold range having a log-normal distribution with 1000 ng g1 as the mean and 2500 ng g1 wet weight as the upper 95% confidence interval to calculate the risk quotient (RQ). The simulations were run using Crystal Ball software with 1000 trials for the three sampling sites and Great Egret data. The results indicated a significant exceedance of the RQs of unity (9.5% and 37.5% for the three sampling sites and Great Egret, respectively) where adverse effects are initiated (Supplementary material Figs. S6 and S7). The overall outcome of the risk characterization demonstrated that there are potential risks to birds associated with exposure to DDE, which might be causing a reduction in survival of young in Hong Kong Ardeids. Acknowledgements The work described in this paper was partly supported by the Area of Excellence Scheme under the University Grants Committee of the Hong Kong Special Administration Region, China (Project No. AoE/P-04/2004) and a CityU Strategic Research Grant (7008035). We would like to thank the Agriculture, Fisheries and Conservation Department of the Hong Kong SAR Government for funding part of this work, and express our gratitude to the Hong Kong Birdwatching Society their invaluable advice on bird egg collection. We would like to thank Drs. Craig L.H. Hung and M.K. So (City University of Hong Kong) for their assistance in preparing the manuscript.

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