Article pubs.acs.org/est
Assimilation Efficiency of PBDE Congeners in Chinook Salmon Joseph P. Dietrich,*,† Stacy A. Strickland,‡,∥ Greg P. Hutchinson,‡,⊥ Ahna L. Van Gaest,‡,# Alex B. Krupkin,‡,○ Gina M. Ylitalo,§ and Mary R. Arkoosh† †
Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2032 SE OSU Drive, Newport, Oregon 97365, United States ‡ Frank Orth & Associates, 11411 NE 124th Street, Suite 230, Kirkland, Washington, 98034, United States § Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Boulevard, East Seattle, Washington 98112, United States S Supporting Information *
ABSTRACT: Polybrominated diphenyl ether (PBDE) flame retardants are environmental contaminants that can accumulate in biota. PBDE accumulation in an organism depends on exposure, assimilation efficiency, and elimination/metabolism. Net assimilation efficiency represents the fraction of the contaminant that is retained in the organism after exposure. In the present study, congener-specific estimates of net PBDE assimilation efficiencies were calculated from dietary exposures of juvenile Chinook salmon. The fish were exposed to one to eight PBDE congeners up to 1500 ng total PBDEs/g food. Mean assimilation efficiencies varied from 0.32 to 0.50 for BDE congeners 28, 47, 99, 100, 153, and 154. The assimilation efficiency of BDE49 was significantly greater than 100%, suggesting biotransformation from higher brominated congeners. Whole body concentrations of BDE49 significantly increased with both exposure to increasing concentrations of BDE99 and decreasing fish lipid levels, implying lipid-influenced debromination of BDE99 to BDE49. Excluding BDE49, PBDE assimilation efficiency was not significantly related to the numbers of congeners in the diets, or congener hydrophobicity, but was greater in foods with higher lipid levels. Estimates of PBDE assimilation efficiency can be used in bioaccumulation models to assess threats from PBDE exposure to Chinook salmon health and recovery efforts, as well as to their predators.
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INTRODUCTION Polybrominated biphenyl ethers (PBDEs) are a class of brominated flame-retardants that have been added to a number of household and commercial items including televisions, computers, electronic equipment, and furniture.1 PBDEs leach from these items into the environment and have been detected throughout the globe.2,3 Concerns with PBDEs arose due to their persistence, bioaccumulation, and their potential health effects to humans and wildlife. PBDE exposure can result in endocrine disruption, neurotoxic, and immunotoxic effects in numerous species, including the following: rats, fish, marine mammals, and humans.1,4−8 Concentrations of PBDEs detected in people and environmental samples increased exponentially from the 1970s to 2000s.1,2 Three different mixtures of PBDEs have been commercially mass-produced: penta-BDE, octa-BDE, and deca-BDE.9 Regulatory limits and phasing out the production and use of penta-BDE and octa-BDE mixtures in consumer items occurred in the US and European Union in the mid-2000s, followed by actions addressing deca-BDE.8,10 Recent monitoring results have found that PBDE levels are stabilizing and possibly decreasing.11−15 However, PBDEs in fish and marine mammals are still present,16 and inputs into the © 2015 American Chemical Society
base of the food web from sediments and plankton suggest that PBDE exposure and transfer to higher trophic level organisms will continue.17 Chinook salmon (Oncorhynchus tschawytscha) from the US Oregon coast and Canada’s British Columbia have the dubious distinction of having significantly higher PBDE loads than four other wild salmon species in a global monitoring survey.3 The effect of PBDE exposure on Chinook salmon (hereafter abbreviated to Chinook) has not been adequately characterized, despite this notoriety and the important and multifaceted role of this species. Chinook are a Pacific salmon species that includes populations that are actively reared in hatchery environments;18 prized as commercial and recreational fisheries;18,19 considered a threatened and endangered species;20 and the primary prey of threatened and endangered marine mammals.21,22 Received: Revised: Accepted: Published: 3878
November 21, 2014 February 13, 2015 February 18, 2015 February 18, 2015 DOI: 10.1021/es5057038 Environ. Sci. Technol. 2015, 49, 3878−3886
Article
Environmental Science & Technology Table 1. Description of the Dietary Exposures of PBDEs in Juvenile Chinook Salmon PBDE dietsa individual congener BDE47-III target congeners
a
range of total PBDE concentrations, ng/g food no. of treatments lipid content of food, % (±SD) duration of exposure no. of replicate feed tanks no. of fish per tank no. of samples analyzed for PBDEs per treatment sample format mean fish weight prior to exposure (SD), g mean fish weight after exposure (SD), g
BDE47-V
mixed congener
BDE99-III
BDE99-V
BDE47,99-V
BDEmixed-IIb
BDE47
BDE47
BDE99
BDE99
BDE47, BDE99
0.7−281
0.3−552
0.7−308
0.3−577
0.7−693
BDE47, BDE99, BDE100, BDE153, BDE154 280 and 1500
4 8.1 (0.2) 40 d 2 140 2
6 5.8 (0.4) 40 d 2 175 10
4 6.8 (0.1) 40 d 2 140 2
6 6.0 (0.4) 40 d 2 175 10
6 9.4 (0.2) 39 d 3 285 6
2 6.5 (0.4) 40 d 9 48 9
composite of 4 fish 10.8 (0.9)
individual fish 9.1 (1.6)
composite of 4 fish 10.8 (0.9)
individual fish 8.6 (0.5)
composite of 5 fish 5.4 (1.3)
individual fish
20.6 (2.4)
16.9 (3.4)
20.4 (4.5)
16.4 (4.1)
10.6 (1.4)
26.6 (17.4)
16.7 (7.5)
Diets are described as “Individual” or “Mixed” based on the number of PBDE congeners targeted per diet formulation. However, the analysis of food samples revealed nontarget congeners at low levels (Table 2). bThe BDEmixed-II diet and exposure has been previously described in Arkoosh et al.4
a
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METHODS PBDE Dietary Exposure. Three groups of juvenile Chinook, originating from hatcheries in Washington and Oregon USA, were reared and exposed to the PBDEs at the National Oceanographic and Atmospheric Administration’s in Newport, Oregon. The Chinook were all of the ocean-type life history19 and were exposed as subyearlings in flow-through seawater. They were fed a prescribed exposure concentration (treatment level) from one of the six PBDE-contaminated diets in replicate feeding tanks (Table 1) at approximately 2% of their body weight per day for 39 or 40 days. Forty-day exposure reflects the potential duration of juvenile salmon residence in urban watersheds.4 One of the PBDE diets, named “BDEmixedII”, and its exposure has been previously described in Arkoosh et al.4 The remaining five dietary exposures occurred similarly, with details specific to each exposure in Table 1. Rations were calculated based on numbers of fish per tank and an estimated fish mass and adjusted daily to reflect mortalities and estimated fish growth. After exposure, PBDE concentrations were determined in whole bodies of individual fish or composites samples (Table 1). Food Preparation. Salmon were fed six different PBDE diets that contained multiple treatment levels of PBDEs (Tables 1, 2). Four “Individual congener” diets targeted the most prominent PBDE congeners found in salmon (BDE47 and BDE99).3,34,35 In addition, two “Mixed congener” diets were targeted multiple congeners. The “BDEmixed-II” diet contained five PBDE congeners and was originally described in Arkoosh et al.4 The ‘BDE47,99-V’ targeted equivalent mixtures of BDE47 and BDE99. Each of the diets and treatment levels were prepared as per Arkoosh et al.4 Briefly, the congener diets were prepared from stock concentrations of PBDE congeners dissolved in methylene chloride (AccuStandard; New Haven, CT). The stock concentrations were further diluted in 3−4 L of methylene chloride for each treatment level and added to batches of dry food pellets (Rangen Inc.; Buhl, ID USA) in a 1:1 (mass:volume) ratio. Three lots of food pellets were used to prepare the six diets: BDEmixed-II from lot 1; BDE47-V and
Metabolism and rates of debromination of PBDEs have been identified in Chinook,23 and exposure has increased their susceptibility to disease.4 However, the efficiency that Chinook assimilate PBDEs from their prey is unknown. Assimilation efficiencies of PBDE congeners from hatchery feed or prey affects the congener profile and bioaccumulation within Chinook. Consequently, the assimilation efficiency of PBDEs in Chinook can be used to assess threats from PBDE exposure to their health and recovery efforts. In addition, the assimilation efficiency in Chinook can be used in modeling the exposure to and fate of PBDEs in Chinook predators. Bioaccumulation models use contaminant assimilation efficiencies that are based on laboratory-derived quantities or functions of the contaminant’s hydrophobicity.24 These models could help in the assessment of potential toxic threats to marine mammal populations, as well as the effectiveness of recovery plans that attempt to reduce these threats. Biologically relevant models require accurate descriptions of congener-specific concentrations, assimilation, and metabolism at multiple trophic levels.25 The assimilation efficiency of PBDEs has been estimated in other fish species: pike (Esox lucius),26 lake trout (Salvelinus namaycush),27 carp (Cyprinus carpio),28 sole (Solea solea L.),29 turbot (Psetta maxima),30 zebrafish (Danio rerio),31 and Atlantic salmon (Salmo salar L.),32,33 with varying values for the congeners, species, and exposure conditions studied. The observed variation and divergence in assimilation efficiencies and PBDE metabolism23 indicate that generalizing these values across species and congeners may be problematic. The objectives of the present study were to estimate the efficiency of PBDE assimilation in juvenile Chinook under various exposure conditions. Over 500 congener-specific estimates of assimilation efficiency were calculated from three different stocks of Chinook exposed to multiple combinations of PBDE congeners at concentrations spanning 3 orders of magnitude. The influence of the PBDE congener, lipids, and concentration on assimilation efficiency could be evaluated over the range of exposure conditions. 3879
DOI: 10.1021/es5057038 Environ. Sci. Technol. 2015, 49, 3878−3886
Article
Environmental Science & Technology Table 2. Concentration of PBDEs and Lipids in the Prepared Diets PBDE congener concentrations, ng PBDE/g food diet, level BDE47-III 0 1 2 3 BDE47-V 0 1 2 3 4 5 BDE99-III 0 1 2 3 BDE99-V 0 1 2 3 4 5 BDE47,99-V 0 1 2 3 4 5 BDEc mixed-II 0 1 2
lipid, % (±SD)
totala
BDE 28
BDE 47
BDE 49
BDE 66
BDE 85
BDE 99
BDE 100
BDE 153
BDE 154
