declining concentrations of persistent pcbs, pbdes, pcdes, and pcns in harbor seals (phoca vitulina)...

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    Article history:Available online 1 June 2013

    (PCDDs or dioxins) and polychlorinated dibenzofurans (PCDFs orfurans) (Bright et al., 1999; Hagen et al., 1997). Industrial activitieshave contaminated a number of sites, and contributed to heavypolychlorinated biphenyl (PCB) contamination in Puget Sound,

    e and toxic. KillerOcean have beenstent Organet al., 200

    et al., 2000a). While the salmon-eating resident killer whathought to reect in part a global POP signal (Cullon2009), harbor seals (Phoca vitulina) provide an indication of morelocalized food web contamination in the Salish Sea. Harbor sealsare relatively abundant, widely distributed, and have a limitedhome range (50 km2) (Cottrell, 1996; Olesiuk, 2009). Previouswork ascribed dioxins and furans in harbor seals to pulp and paperprocesses in the Strait of Georgia, PCBs to a history of industrial in-puts into Puget Sound, and a global contribution in seals from re-mote locations (Ross et al., 2004).

    Corresponding author. Tel.: +1 250 363 6806; fax: +1 250 363 6807.E-mail addresses: (P.S. Ross),

    (M. Nol), (D. Lambourn), (N. Dangereld), (J. Calambokidis),

    Progress in Oceanography 115 (2013) 160170

    Contents lists available at

    Progress in Oc (S. Jeffries).agricultural activities, municipal waste water and urban runoff,petrochemical facilities, and a variety of other industrial activities(Waldichuk, 1983). Pulp and paper mills have, in the past, releasedlarge quantities of by-produced polychlorinated dibenzo-p-dioxins

    icals considered to be persistent, bioaccumulativwhales (Orcinus orca) of the Northeast Pacicfound to be particularly contaminated with Persilutants (POPs), especially the legacy PCBs (Krahn0079-6611/$ - see front matter 2013 Elsevier Ltd. All rights reserved. Pol-7; Rossles areet al.,1. Introduction

    While boasting a rich diversity of aquatic species, the Salish Sea,comprising the Strait of Georgia, Juan de Fuca Strait and PugetSound on the Pacic coast of North America, has been at the receiv-ing end of household, agricultural and industrial contaminantsfrom both within and outside its watershed boundaries. Sourceswithin the watershed include major wood and paper industries,

    Washington, USA (West et al., 2008). In addition to local contami-nant inputs, global contaminants are delivered to the Salish Seathrough atmospheric transport (Nol et al., 2009) and biologicaldelivery to coastal food webs by migratory species, including sev-eral species of salmon (Christensen et al., 2005; Krummel et al.,2005).

    Situated atop coastal food webs, many marine mammals canprovide an integrated signal of food web contamination by chem-As high trophic level, non-migratory marine mammals, harbor seals (Phoca vitulina) inhabiting the Straitof Georgia, Juan de Fuca Strait and Puget Sound (collectively referred to as the Salish Sea) in northwesternNorth America provide an integrated measure of coastal food web contamination. We measured conge-ner-specic polychlorinated biphenyls (PCBs), polybrominated diphenylethers (PBDEs), polychlorinateddiphenylethers (PCDEs) and polychlorinated naphthalenes (PCNs) in blubber biopsies from free-rangingharbor seal pups inhabiting four sites in the Salish Sea in 2003. While legacy PCBs dominated the com-position of these contaminants in seals at all sites (PCBs > PBDEs > PCDEs > PCNs), PBDEs were notewor-thy in that they averaged as much as 59% of total PCB concentrations. We further evaluated temporaltrends in seals sampled at one of these sites (Puget Sound) for PCBs and PBDEs between 1984 and2009, and for PCDEs and PCNs between 1984 and 2003. PBDE concentrations doubled every 3.1 yearsbetween 1984 and 2003, but appeared to decline thereafter. Over the course of the 20 years between1984 and 2003, PCB concentrations had declined by 81%, PCDEs declined by 71%, and PCNs by 98%. Over-all, results suggest that regulations and source controls have noticeably reduced inputs of these contam-inants to the Salish Sea, consequently reducing the associated health risks to marine wildlife. Weestimate the total mass of these contaminants in the 53,000 harbor seals of the Salish Sea in 2009 tobe 2.6 kg PCBs and 1.0 kg PBDEs, compared to just trace amounts of the PCDEs and PCNs.

    2013 Elsevier Ltd. All rights reserved.a r t i c l e i n f o a b s t r a c tDeclining concentrations of persistent PCin harbor seals (Phoca vitulina) from the

    Peter S. Ross a,, Marie Nol a,b, Dyanna Lambourn c, Na Institute of Ocean Sciences, Fisheries & Oceans Canada, P.O. Box 6000, 9860 West SaanbUniversity of Victoria, P.O. Box 3055, Victoria, British Columbia, Canada V8W 3P6cWashington Department of Fish and Wildlife, 7801 Phillips Road SW, Lakewood, WA 9dCascadia Research, 218 West 4th, Olympia, WA 98501, USA

    journal homepage: www.s, PBDEs, PCDEs, and PCNslish Sea

    l Dangereld a, John Calambokidis d, Steven Jeffries c

    Road, Sidney, British Columbia, Canada V8L 4B2

    , USA

    SciVerse ScienceDirect


    evier .com/locate /pocean

  • The response of environmental compartments within the SalishSea to chemical regulations or source controls have been character-ized for a number of POPs, such as PCBs and polybrominated di-phenyl ethers (PBDEs) using sediment cores (Johannessen et al.,2008), dioxins and furans in Dungeness crab,Metacarcinus magister(Hagen et al., 1997), and PCBs and organochlorine pesticides in theeggs of double-crested cormorants, Phalacrocorax auritus (Harriset al., 2005). Despite such improvements, the regions killer whaleshave some of the highest PCB levels reported among the worldsmarine mammals, presenting troubling questions about the con-servation implications for POPs in marine food webs (Ross, 2006).

    PCBs have represented a major toxicological concern for manyhigh trophic level species; they were banned in 1976 and 1977in the USA and Canada, respectively. PCBs have been associatedwith reproductive impairment, tumors, immunotoxicity and endo-crine disruption in captive and free-ranging marine mammals (DeSwart et al., 1994; Mos et al., 2006; Reijnders, 1986; Ross et al.,1996; Ylitalo et al., 2005). PBDEs have been widely used as ameretardants in electronics, furniture and other products; two ofthe three commercial formulations (penta- and octa-) were with-drawn from the market in 2004, while the third product is facinga North American phase-out in 2013. Less is known about the tox-icity of PBDEs to marine mammals, but similarities in structureswould suggest similar toxic effects. Studies demonstrate thatPBDEs affect the function of white blood cells in harbor seals (Frou-in et al., 2010). Polychlorinated diphenyl ethers (PCDEs) have beenattributed to impurities in pentachlorophenol (PCP) used as awood preservative in the lumber industry, as well as in a varietyof pesticides and other products (Becker et al., 1991). Polychlori-

    Approximately 53,000 harbor seals are distributed over the17,000 km2 of the Salish Sea, feeding on Pacic hake (Merlucciusproductus), Pacic herring (Clupea pallasi), Pacic tomcod (Microga-dus proximus) and a variety of other pelagic and bottomsh species(Cullon et al., 2005; Lance et al., 2012; Olesiuk, 1993). They there-fore provide an integrated contaminant signal from the numeroussh and invertebrate prey species upon which they rely, and pro-vide insight into contamination hotspots and emerging contami-nants of concern (Cullon et al., 2005).

    In this study, we evaluated spatial variation in PCB, PBDE, PCDEand PCN concentrations and patterns in harbor seals inhabitingsites throughout the transboundary waters of the Salish Sea. Inaddition, we evaluated temporal trends in the concentrations ofPCBs and PBDEs in harbor seals from southern Puget Sound duringthe period 19842009, and for PCDEs and PCNs for the period19842003.

    2. Material and methods

    2.1. Live-capture and sampling of seals for spatial assessment

    We collected blubber biopsies from live-captured harbor sealpups from two locations in British Columbia, Canada (Hornby Is-land and the Fraser River estuary in Vancouver), and two locationsin Washington State, USA (Smith Island and Gertrude Island)(Fig. 1). Harbor seals were captured using one of two techniques.At the rocky Hornby Island site, individual seals were capturedby hand and using a sh landing net following a rapid yet careful

    P.S. Ross et al. / Progress in Oceanography 115 (2013) 160170 161nated naphthalenes (PCNs) were intentionally produced as ameretardants and wood preservatives, but have also been describedas impurities in PCBs and as by-products of combustion ofchlorine-containing products (Falandysz, 1998; Yamashita et al.,2000).Fig. 1. Harbor seals were live-captured at four sites in 2003, including Hornby Island andStrait, Washington State, USA) and Gertrude Island (Puget Sound, Washington State, USAtemporal trend analyses.approach by a 3.5 m aluminum outboard boat (Cottrell et al.,2002). At the three remaining sites, which consisted of sandyhaul-out areas, multiple seals were captured at one time using arapidly deployed beach seine net (Jeffries et al., 1993). In all cases,body weight, body length, girth, and sex were determined for eachVancouver (Strait of Georgia, British Columbia, Canada), Smith Island (Juan de Fuca). Harbor seals were sampled during the period 19842009 from Gertrude Island for

  • 2009 (n = 7). Samples from 1993, 1997 and 2009 were obtained

    conditions, and quality assurance/quality control criteria used for

    eanoPCBs by the Laboratory of Expertise for Aquatic Chemical Analysis(LEACA, Fisheries and Oceans Canada, Sidney BC


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