Spatial and temporal trends of persistent organic pollutants and mercury in beluga whales (Delphinapterus leucas) from Alaska
Highlights
► We examined temporal and spatial differences in pollutants in Alaskan beluga whale. ► Mercury, PCBs, DDTs, and chlordanes were the predominant pollutants observed. ► Most POPs and Hg were higher in Chukchi Sea than Cook Inlet belugas, except BFRs. ► Most legacy POPs and Hg were stable, but PBDEs and α-HBCD were increasing. ► Maternal transfer of most POPs was indicated by sex differences & fetus:mother ratios.
Introduction
Although relatively isolated, the Arctic has been shown to be a sink for a variety of contaminants. Atmospheric transport is thought to be the predominant mode of delivery of volatile precursors (Wania and Mackay, 1993, Oehme et al., 1996). Nevertheless, oceanic transport, although somewhat patchy, has also been shown to contribute (Oehme, 1991, Barrie et al., 1992). As a result, the Arctic Monitoring and Assessment Programme (AMAP) was established in 1991 as an international effort to assess Arctic status with respect to target contaminants, including persistent organic pollutants (POPs) and heavy metals. AMAP's initial report (1997) documented the ubiquitous presence of POPs throughout the Arctic. Around the same timeframe, the Stockholm Convention on Persistent Organic Pollutants was signed in 2001 to initiate a global ban or restriction on production and use of a number of POPs (Rigét et al., 2010). The effectiveness of this treaty can only be realized by investigating temporal trends in levels of these compounds in the environment and associated biota. Since AMAP's and the Stockholm Convention's inceptions, extensive investigations of marine biota in Canadian and European Arctic regions have been conducted, whereas these have been somewhat lacking in the Alaskan Arctic region.
The beluga whale (Delphinapterus leucas) is a circumpolar Arctic cetacean that feeds high in the marine food web, with a diet consisting of various fishes, squid, octopus, and shrimp (Becker et al., 2000). Due to their estimated long life-span (> 60 yr) (Stewart et al., 2006), marine-based diet, and high lipid reserves, belugas have been shown to accumulate organic and inorganic contaminants, as do many other Arctic top predators, such as polar bears (Ursus maritimus), pinnipeds, and many species of cetaceans (Muir et al., 1992, Skaare, 1995, Kannan et al., 2005). While there have been numerous studies focusing on temporal and spatial trends of these contaminants in Canadian and eastern Arctic belugas (Muir et al., 1999, Braune et al., 2005, Stern et al., 2005, Lebeuf et al., 2007, Kelly et al., 2008), there is limited information on these trends in Alaskan Arctic beluga (Reiner et al., 2011).
Alaskan beluga whales can be divided into two genetically isolated populations: the Bering Sea and Cook Inlet. The Bering Sea population consists of four stocks; the eastern Chukchi Sea, Bristol Bay, the eastern Bering Sea, and the Beaufort Sea (Frost and Lowry, 1990, O'Corry-Crowe et al., 1997, Becker et al., 2000). Cook Inlet belugas (permanent residents of Cook Inlet and the area of the Gulf of Alaska immediately outside Cook Inlet) are geographically separated from the Bering Sea population by the Alaskan Peninsula, while the eastern Chukchi Sea belugas reside between the Russian and United States Arctic (Becker et al., 2000). As the Cook Inlet and eastern Chukchi Sea belugas represent two geographically and genetically isolated populations with tissue samples collected and banked from these two stocks over a span of almost two decades (1989 to 2006), their comparison provides an opportunity to investigate spatial as well as temporal trends in contamination in the Alaskan Arctic.
Beluga whales have been hunted by native Inuit peoples throughout the Arctic. Historical estimates of beluga populations in Cook Inlet and the eastern Chukchi Sea are approximately 1300 and 3700 individuals, respectively (Allen and Angliss, 2010). Although native subsistence hunting is not thought to affect the eastern Chukchi Sea population (Allen and Angliss, 2010), a severe decline in the Cook Inlet population number has led to a halt in this practice (Hobbs et al., 2000). In October 2008, the Cook Inlet belugas were placed on the Endangered Species List in an attempt to bolster dwindling numbers. The National Marine Fisheries Service's most recent survey estimates the population at 284, down approximately 20% from the prior year's estimate of 340 (Hobbs et al., 2011). Genetic isolation, potentially leading to inbreeding and infertility, could impede population growth. However, legacy POPs, as well as emerging contaminants (i.e., brominated flame retardants), have been associated with adverse health effects in marine mammals, including decreased reproduction and offspring survivorship (Schwacke et al., 2002, Wells et al., 2005, Hall et al., 2009) and could also be an impediment to population growth.
In this study, Cook Inlet and eastern Chukchi Sea beluga blubber samples previously collected between 1989 and 2006 as part of the Alaska Marine Mammal Tissue Archival Project (AMMTAP) (Becker et al., 1993) were analyzed for POPs [polychlorinated biphenyls (PCBs), dichlorodiphenyl-dichloroethane and related compounds (DDTs), chlordanes, hexachlorocyclohexanes (HCHs), chlorobenzenes, mirex, polybrominated diphenyl ethers (PBDEs), and semi-quantitatively for hexabromocyclododecanes (HBCDs)]. Blubber is the primary site of POP accumulation in cetaceans, comprising > 90% of the whole body burden (Isobe et al., 2009, Yordy et al., 2010a). Beluga liver samples that had been similarly collected were also used for the analysis of total mercury (Hg). The Cook Inlet belugas are thought to be exposed to more local anthropogenic sources coming from the surrounding urbanized area of Anchorage, while the eastern Chukchi Sea belugas, often migrating between the Russian and United States Arctic, should be more exposed to contaminant transported by atmospheric and oceanic mechanisms. There are few reported data sets on POPs in marine mammals from this region and having beluga samples from the Chukchi Sea is a unique opportunity to assess the influences of Asian and Russian production of legacy and emerging POPs to this area of the Arctic. In addition, this information will lead to a more comprehensive account of the Arctic's current and predicted environmental status. Therefore, the main objective of this paper is to provide information on the status and trends of POP and mercury (Hg) concentrations in belugas collected from Alaska.
Section snippets
Sample collection and preparation
As part of AMMTAP, full-depth blubber and liver tissues were collected from tide-stranded or free-ranging beluga whales during native subsistence hunts in Cook Inlet and the eastern Chukchi Sea, Alaska from 1989 to 2006 (Fig. 1; Supplemental information Table S1). Collection procedures followed standard AMMTAP protocols designed to preserve sample integrity and minimize sample contamination (Becker et al., 1991). Following collection, blubber and liver samples were shipped and stored according
Results and discussion
All POP classes and Hg were detected in 100% of the samples, except α-HBCD that was detected less frequently, in only 68% of the samples (Table 1). With both subpopulations and sexes combined, concentrations of ΣPOPs in blubber and Hg in liver concentrations ranged from 685 ng/g lipid to 24.9 μg/g lipid (median: 6503 ng/g lipid), and 0.337 to 158 μg/g wet mass (median: 5.51 μg/g wet mass), respectively. ΣPOP concentrations consisted of 37% ΣPCBs (medians shown in parentheses: 2360 ng/g lipid), 31%
Conclusions
This study demonstrates that even within a relatively small region of the Arctic, there exist significant spatial and temporal differences in potential exposure to various deleterious compounds. Although contaminant exposure sources can be speculated, it is not completely clear whether these differences are likely due to geographic variations in long-range atmospheric transport of contaminants, oceanic transport, localized releases, such as sewage treatment plants, feeding habits and nutrition,
Disclaimer
Certain commercial equipment, instruments, or materials are identified in this paper to specify adequately the experimental procedure. Such identification does not imply recommendation or endorsement by the National Institute of Standards and Technology, nor does it imply that the materials or equipment identified are necessarily the best available for the purpose.
Conflict of interest
None.
Acknowledgments
All specimens used in this study were collected and banked through the Alaska Marine Mammal Tissue Archival Project (AMMTAP) with funding support from the Minerals Management Service, U.S. Geological Survey Biological Resources Division (USGS BRD), National Marine Fisheries Service (NMFS) Office of Protected Resources (Teri Rowles), and the National Institute of Standards and Technology (NIST). The following individuals and organizations are acknowledged for their aid in the specimen
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