Risk to breeding success of waterbirds by contaminants in Hong Kong: evidence from trace elements in eggs

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Abstract

Concentrations of 17 trace elements (As, Se, Rb, Sr, Ag, Sb, Cs, Tl, Pb, V, Cr, Mn, Co, Cu, Zn, Cd, and Hg) were determined in eggs of little egrets (Egretta garzetta), black-crowned night herons (Nycticorax nycticorax) and bridled terns (Sterna anaethetus) from northwestern and northeastern coastal areas of Hong Kong. Results indicated significant differences among the three species. Eggs of little egrets and black-crowned night herons appeared to be good bioindicators for monitoring selected elements (As, Pb, Zn Cr, Cu, and V) due to consistent correlations between metal concentrations in eggs and those in coastal marine sediments. Based on limited toxicological information, the predicted no effect concentrations (PNECs) of Hg and Se in the bird eggs were estimated as 0.5 to 1.8 and 0.90 to 1.45 μg g−1, dry wt., respectively. Hazard quotients (HQs) indicated that Hg and Se might pose some risk to certain waterbirds in Hong Kong.

Introduction

The Pearl River Delta in southern China has experienced rapid development in the past two decades, and is now one of the fastest-growing industrial manufacturing areas in the world. Hong Kong, situated on the west side of the Pearl River Delta, is heavily influenced by the pollutant-laden discharge from the Pearl River and its many tributaries (Richardson et al., 2000). As a consequence, Hong Kong's western waters are generally exposed to greater concentrations of environmental contaminants as compared to its eastern waters (Connell et al., 2003). These contaminants include polycyclic aromatic hydrocarbons, petroleum hydrocarbons, organotins, organochlorines, and trace metals (Connell et al., 2003, Müller et al., 2002, Wong and Tanner, 1997, Zheng et al., 2000, Zheng et al., 2002). These contaminants have a negative impact on the integrity and sustainability of the marine ecosystems in southern China, including Hong Kong.

Trace metal concentrations in the coastal environment of Hong Kong have been reviewed by Wu, 1998, Phillips, 1989, and Blackmore, 1998a, Blackmore, 1998b. Previous studies on trace metals in Hong Kong marine waters have tended to focus on monitoring concentrations in sediments and certain marine organisms, mainly mussels [see review by Blackmore (1998b)]. Despite these efforts and the regular monitoring of pollutant concentrations in marine sediments by the Environmental Protection Department of Hong Kong, HKEPD (EPD, 2002), there is still a lack of baseline information regarding contaminant concentrations in protected wildlife of higher trophic levels, e.g. predatory waterbirds (Lam et al., 2004, Lam and Lam, 2004).

Apart from their conservation value, waterbirds are valuable for environmental monitoring because they are long-lived, top predators, and are able to integrate pollutant levels over an extensive area by bioaccumulation (Furness, 1993). A number of studies have shown that feathers are useful for monitoring metal contamination in birds as concentrations in feathers can reflect those in the blood during the production of feathers (Burger and Gochfeld, 1997, Goutner et al., 2001, Movalli, 2000). However, concentrations of trace elements measured in feathers can be strongly confounded by external contamination especially from atmospheric deposition (Dauwe et al., 2003, Furness and Camphuysen, 1997). Hence, it is instructive to complement the metal concentrations measured in feathers with other samples, e.g. eggs. Egg laying is recognized as a means of excreting environmental contaminants (e.g. metals) by oviparous females (Gochfeld and Burger, 1998, Burger, 1994, Lam et al., 2004), and thus contaminant concentrations in eggs can potentially be used as a surrogate for contaminant monitoring in egg-laying wildlife. Besides metals, bird eggs are also useful for evaluating lipophilic persistent organic pollutants (Connell et al., 2003).

Despite the small size and the pressing demand for land resources and development, Hong Kong has a wetland of international importance, the Mai Po and Inner Deep Bay Ramsar site, situated in the northwestern part of the territory. The Mai Po Marshes Nature Reserve (MPMNR), occupying an important area for biodiversity conservation within the Ramsar site, is an internationally acclaimed wetland for waterbirds. A Chau is another important habitat for waterbirds situated in the northeastern part of Hong Kong, and is relatively remote from the Pearl River Delta. Ardeids (herons and egrets) are common residents of MPMNR and A Chau (Lam and Lam, 2004). A recent study indicated that the concentrations of dichloro-diphenyl-dichloroethanes (DDEs) in eggs of little egret (Egretta garzetta) and black-crowned night heron (Nycticorax nycticorax) collected, respectively, from MPMNR and A Chau were sufficient to reduce reproductive success (Connell et al., 2003). In addition, an assessment of risks to ardeids due to trace metals, based on concentrations in the feathers, indicated that total mercury concentration in feathers of little egrets collected from a local egretry exceeded the threshold effect level for breeding success (Connell et al., 2002).

Apart from resident coastal waterbirds, certain seabirds, e.g. bridled terns (Sterna anaethetus), visit Hong Kong in the summer (May to August), and breed on an offshore island (Shek Ngau Chau) in Mirs Bay in the northeastern part of Hong Kong (Cheung and Yu, 2001). Monitoring contaminant concentrations in eggs of seabirds can reveal the exposure levels in the breeding grounds where the birds often spend up to many weeks before laying their eggs. However, the contaminant concentrations in the eggs can also be influenced by contaminants present in areas utilized by these birds outside the breeding seasons (Burger, 2002). Indeed, Monteiro et al. (1995) suggest that larids, such as terns, are excellent species to use as monitors of mercury in coastal environments. To date, no information is available on the exposure levels of contaminants to seabirds inhabiting offshore areas of Hong Kong and southern China. Monitoring contaminant concentrations in bridled terns will help to fill this information gap, and provide important information on the bioavailable contaminants in the open sea areas in and outside Hong Kong.

The objectives of this study are to (1) establish baseline information of trace element concentrations in eggs of little egret (E. garzetta), black-crowned night heron (N. nycticorax), and bridled tern (S. anaethetus); (2) examine the suitability and feasibility of using eggs of little egret, black-crowned night heron, and bridled tern as bioindicators for monitoring trace metal levels in the marine environments of Hong Kong; and (3) evaluate the potential risks to little egrets, black-crowned night herons, and bridled terns due to exposure to trace metals and metalloids. Further evaluations of the risk to breeding success of waterbirds from other contaminants are also underway.

Section snippets

Sample preparation

Eggs of little egrets, black-crowned night herons, and bridled terns were collected from MPMNR, A Chau and Shek Ngau Chau, respectively (Fig. 1). Details of the egretries at MPMNR and A Chau are given in Connell et al. (2003). Shek Ngau Chau is a rocky island in Mirs Bay, more remote from the Hong Kong mainland than A Chau. The egg sampling method, as stipulated by the Agriculture, Fisheries, and Conservation Department (AFCD) of the Hong Kong Government, is given in Connell et al., 2003, Lam

Results

Concentrations of the 17 trace elements in egg contents and eggshells of bridled terns from Shek Ngau Chau, Hong Kong, are summarized in Table 1, Table 2. Concentrations in the eggs of little egret and black-crowned night heron have been published in Lam et al. (2004), and the data are included in this paper (Table 1, Table 2) for completeness and comparative purposes. Some trace elements (Sb in the eggshells of all three species; Ag in the eggshells of bridled terns; Cs in the eggshells of

Interspecific comparison

There were significant variations in trace element concentrations in eggs of different waterbird species in Hong Kong (Table 1, Table 2). Significant variations in Cr, Se, V, Mn, and Cu concentrations in egg contents between coastal birds (little egrets and black-crowned night herons) and seabirds (bridled terns) were probably due to the differences in foraging areas and food types. Egrets and herons in Hong Kong typically feed in coastal wetlands, particularly fish ponds (Young, 1993), while

Acknowledgements

This project was funded by the Hong Kong Research Grants Council (CityU1112/02M), and the Area of Excellence Scheme under the University Grants Committee of the Hong Kong Special Administration Region, China (Project No. AoE/P-04/2004). This work was undertaken during tenure of a City University Postgraduate Studentship and a Fellowship under the “21st Century COE Program” from the Ministry of Education, Culture, Sports, Science and Technology of Japan to JCWL. We would like to thank the

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