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Marine Environmental Research 99 (2014) 20e33

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Marine Environmental Research

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Mercury bioaccumulation in cartilaginous fishes from Southern NewEngland coastal waters: Contamination from a trophic ecology andhuman health perspective

David L. Taylor a, *, Nicholas J. Kutil a, Anna J. Malek b, Jeremy S. Collie b

a Roger Williams University, Department of Marine Biology, One Old Ferry Road, Bristol, RI 02809, USAb University of Rhode Island, Graduate School of Oceanography, South Ferry Road, Narragansett, RI 02882, USA

a r t i c l e i n f o

Article history:Received 20 February 2014Received in revised form26 April 2014Accepted 7 May 2014Available online 29 May 2014

Keywords:BioaccumulationDietDogfishFood webMercurySkateStable isotope

* Corresponding author. Tel.: þ1 401 254 3759; faxE-mail address: dtaylor@rwu.edu (D.L. Taylor).

http://dx.doi.org/10.1016/j.marenvres.2014.05.0090141-1136/© 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t

This study examined total mercury (Hg) concentrations in cartilaginous fishes from Southern New En-gland coastal waters, including smooth dogfish (Mustelus canis), spiny dogfish (Squalus acanthias), littleskate (Leucoraja erinacea), and winter skate (Leucoraja ocellata). Total Hg in dogfish and skates werepositively related to their respective body size and age, indicating Hg bioaccumulation in muscle tissue.There were also significant inter-species differences in Hg levels (mean ± 1 SD, mg Hg/kg dry weight,ppm): smooth dogfish (3.3 ± 2.1 ppm; n ¼ 54) > spiny dogfish (1.1 ± 0.7 ppm; n ¼ 124) > little skate(0.4 ± 0.3 ppm; n ¼ 173) ~ winter skate (0.3 ± 0.2 ppm; n ¼ 148). The increased Hg content of smoothdogfish was attributed to its upper trophic level status, determined by stable nitrogen (d15N) isotopeanalysis (mean d15N ¼ 13.2 ± 0.7‰), and the consumption of high Hg prey, most notably cancer crabs(0.10 ppm). Spiny dogfish had depleted d15N signatures (11.6 ± 0.8‰), yet demonstrated a moderate levelof contamination by foraging on pelagic prey with a range of Hg concentrations, e.g., in order of dietaryimportance, butterfish (Hg ¼ 0.06 ppm), longfin squid (0.17 ppm), and scup (0.11 ppm). Skates were lowtrophic level consumers (d15N ¼ 11.9e12.0‰) and fed mainly on amphipods, small decapods, andpolychaetes with low Hg concentrations (0.05e0.09 ppm). Intra-specific Hg concentrations were directlyrelated to d15N and carbon (d13C) isotope signatures, suggesting that Hg biomagnifies across successivetrophic levels and foraging in the benthic trophic pathway increases Hg exposure. From a human healthperspective, 87% of smooth dogfish, 32% of spiny dogfish, and <2% of skates had Hg concentrationsexceeding the US Environmental Protection Agency threshold level (0.3 ppm wet weight). These resultsindicate that frequent consumption of smooth dogfish and spiny dogfish may adversely affect humanhealth, whereas skates present minimal risk.

© 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Mercury (Hg) is a pervasive toxicant that is introduced into theenvironment mainly through anthropogenic activities (US EPA,1997). In the northeastern US, for example, Hg levels are elevatedin marine coastal environments due to local point sources anddistant non-point sources of contamination. The latter is domi-nated by the long-range transport of emissions from fossil-fuelcombustion, after which the Hg by-product enters a water bodythrough direct atmospheric deposition and watershed transport(Clarkson, 1992). Estuarine and coastal sediments are repositoriesfor Hg (Balcom et al., 2004), and are the principal location formethylation, a bacterial-mediated process that converts inorganic

: þ1 401 254 3310.

Hg to its more toxic organic form, methylmercury (MeHg) (Gilmouret al., 1992; Benoit et al., 2003). MeHg derived from surface sedi-ments may then be mobilized to the water column and transferredto biota through several physical and biological processes (Chenet al., 2008), including the bio-concentration of the contaminantin phytoplankton. This functional group, in turn, effectively trans-fers MeHg to both pelagic and benthic food webs (Mason et al.,1996; Moye et al., 2002), after which MeHg biomagnifies acrosssuccessive trophic levels, concentrating in the tissues of top-levelpredators, including fish and other consumers (Wiener et al., 2003).

Fish are exposed to MeHg mainly through diet (Hall et al., 1997),and MeHg exposure causes numerous health deficits in fish. Theseverity of these adverse effects depends on the interplay betweenintra-species life history traits and the concentration andduration ofMeHg exposure. Fish MeHg concentrations, for example, are posi-tively related to body size and age when dietary intake exceeds

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e33 21

depuration rates of the contaminant (Trudel and Rasmussen, 1997).Prey preferences and foraging ecology also impact MeHg dynamics,such that toxicant concentrations are elevated in fish feeding athigher trophic levels (Piraino and Taylor, 2009; Payne and Taylor,2010; Szczebak and Taylor, 2011). Accordingly, fish MeHg bio-accumulation rates need to be examined concurrentlywith species-specific characteristics, such as body size, age, and ontogenetic shiftsin diet and habitat use. Acute MeHg toxicity in fish (tissueMeHg ¼ 6.0 mg/kg wet weight) may lead to neurological disease,including reduced swimming activity and loss of equilibrium, andpossibly death (Armstrong,1979;Wiener and Spry,1996; Smith andWeis, 1997). Chronic, low-dose MeHg exposure in fish may alsocause more subtle end points of toxicity (tissue MeHg ¼ 0.1 mg/kgwet weight), with possible deleterious effects to both the individual(e.g., compromised metabolism, osmoregulation, oxygen exchange,reproduction, and growth) and population (e.g., reduced survivaland recruitment success) (Candelmo et al., 2010).

The majority of Hg-related research in marine ecosystems hasfocused on bony fishes (Division Teleostei) because of theirimportance as a human food resource (US EPA, 1997). Compara-tively, there is a paucity of information on Hg burdens in cartilag-inous fishes (Subclass Elasmobranchii), although a number of thesespecies support important commercial and recreational fisheries.Previous investigations on this topic have almost exclusively tar-geted sharks and have been limited geographically to coastal Pacificregions (Endo et al., 2009), tropical and sub-tropical waters (Heuteret al., 1995; de Pinho et al., 2002; Garcia-Hernandez et al., 2007;Maz-Courrau et al., 2012), and the pelagiceoceanic realm (Estradaet al., 2003; Branco et al., 2007; Suk et al., 2009). These priorstudies revealed that many sharks experience contaminant con-centrations above which adverse effects are realized, and further,may constitute a potential health risk for human consumers. Thereremains a lack of Hg research on a broad range of cartilaginousfishes from coastal regions of the Northwest Atlantic (e.g., sharksand skates), despite the ecological importance of these species innear-shore environments (Collette and Klein-MacPhee, 2002).Moreover, the broad distribution, high abundance, and upper tro-phic level status of cartilaginous fishes suggest that they stronglyinfluence the fate of Hg in coastal habitats.

The primary objective of this study was to examine Hg bio-accumulation rates in cartilaginous fishes from Southern New En-gland coastal waters, including the smooth dogfish, (Musteluscanis), spiny dogfish, (Squalus acanthias), little skate, (Leucorajaerinacea), and winter skate, (Leucoraja ocellata). Total Hg concen-trations were measured in these target species and results wereanalyzed relative to intra-specific life history traits, including bodysize, age, sex, habitat use, and feeding habits. For the latter, con-ventional stomach content analysis was coupled with stableisotope (nitrogen and carbon) measurements to assess the effect ofdiet history and trophic processes on Hg contamination (Shiffmanet al., 2012). Representative prey of each target fish was alsoanalyzed for Hg content to determine their effect on Hg exposure.Lastly, given the potential value of each target species as a humandietary resource (NEFSC, 1999, 2006; NMFS, 2010), Hg results wereevaluated relative to the US Environmental Protection Agency (USEPA) and US Food and Drug Administration (US FDA) criteria for thesafe consumption of fishery products.

2. Methods

2.1. Target fishes

Smooth dogfish (Family Triakidae) and spiny dogfish (FamilySqualidae) are the most numerically dominant shark species in thecoastal western Atlantic (Collette and Klein-MacPhee, 2002).

Smooth dogfish are a demersal species that occupy shallow near-shore waters (<18 me200 m) from the Bay of Fundy to Florida,with maximal abundances in the Mid-Atlantic region (Cape Hat-teras, North Carolina to New Jersey). Similarly, spiny dogfish areprincipally located from Nova Scotia southward to Cape Hatteras,but this species occupies a broader range of continental shelf wa-ters (shallows to 900 m) and utilizes both epibenthic and pelagichabitats (Stehlik, 2007). Both smooth and spiny dogfish undergopronounced latitudinal migrations in response to seasonal tem-perature changes, as well as onshoreeoffshore movements that aregoverned by prey availability and the onset of reproductive events,e.g., inshore pupping (Collette and Klein-MacPhee, 2002). Smoothand spiny dogfish also have varying life history strategies. Smoothdogfish are moderately sized [maximum size ~ 150 cm total length(TL)] and have relatively fast growth rates (15e20 cm TL/year) andshort life spans (10e15 years). Conversely, spiny dogfish are char-acterized by a smaller maximum body size (~100 and 125 cm TL formales and females, respectively), slower growth rate(1.5e3.5 cm TL/year), and extended longevity (35e40 to perhaps100 years) (Collette and Klein-MacPhee, 2002; Stehlik, 2007).Finally, smooth dogfish are mainly benthic foragers with decapodcrustaceans (crabs) representing the dominant prey, whereas theuse of pelagic waters by spiny dogfish is reflected in their diet, suchthat fish, squid, and ctenophores are the most important food re-sources (Smith and Link, 2010).

Little skates and winter skates are sympatric species (FamilyRajidae) with contrasting life history characteristics. Little skatesare relatively small-bodied [maximum size ~ 30 cm disk width(DW)] and short-lived (~12 years), whereas winter skates have alonger life span (~20 years) and achieve an appreciable larger bodysize (maximum size ~ 60 cm DW) (Packer et al., 2003a, 2003b). Thediet of both skates consist primarily of macro-invertebrates (e.g.,amphipods, polychaetes, and decapod crustaceans), with fishbecoming an increasingly important prey item for larger in-dividuals (Smith and Link, 2010). Little skates and, to a lesser extent,winter skates often numerically dominate the demersal fish com-munity in the Northwest Atlantic (Collette and Klein-MacPhee,2002). Their specific geographic ranges are comparable andencompass coastal waters from southeastern Newfoundland toCape Hatteras.

2.2. Sample collection and preparation

Dogfish, skates, and their prey were collected from Rhode Is-land/Block Island Sound and Narragansett Bay fromMay to October(2009e2012) using bottom trawls and hook & line (Fig. 1), andspecimens were identified by their time (year and day of collection)and location (latitudeelongitude) of capture. Prey were selected foranalysis based on their recognized dietary contribution to dogfishand skates (Smith and Link, 2010), and included scup (Stenotomuschrysops), butterfish (Peprilus triacanthus), longfin inshore squid(Doryteuthis pealeii), and cancer crabs (Cancer irroratus and Cancerborealis). Dogfish, skates, and prey collected in the field were eitherprocessed immediately after capture or put on ice for trans-portation and frozen at �20 �C in the laboratory for subsequentanalysis.

The processing of dogfish, skates, and prey in the field andlaboratory included assessing the sex of each shark and skate(presence/absence of claspers), measuring individual body size,excising muscle tissue samples, and extracting stomachs (trawl-collected dogfish and skates only). Size was measured as whole-body wet weight (g) and length or width (mm): dogfish, scup,and butterfish ¼ TL; skate ¼ DW; squid ¼ mantle length (ML); andcrab ¼ carapace width (CW). The age (years) of each dogfish andskate was also estimated from sex-specific ageelength

Fig. 1. Map of Rhode Island Sound, Block Island Sound, and Narragansett Bay (Rhode Island, USA) with points denoting collection sites of target fish (smooth dogfish, spiny dogfish,little skate, and winter skate) and prey (scup, butterfish, longfin squid, and cancer crabs).

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e3322

relationships reported in the literature (Soldat, 1982; Collette andKlein-MacPhee, 2002; Conrath et al., 2002; Sulikowski et al.,2003; Cicia et al., 2009). Muscle tissue samples (2e5 g wet weightwith skin removed) were excised from the dorsal axial musculatureof dogfish and scup, pectoral wings of skates, and mantle dorsalbody wall of squid using stainless-steel surgical blades, whereascrabs were processed as whole bodies. All muscle-tissue andwhole-body samples were freeze-dried for 48 h (Labconco Free-Zone 4.5-L Benchtop Freeze-Dry System), homogenized with cleanstainless-steel spatulas, and stored at room temperature in boro-silicate vials. The stomachs of dogfish and skates (~5 individuals/size class/species/trawl tow; assumed to have contents) wereextracted immediately after capture and preserved in Normalin®

following the procedures of Smith and Link (2010).

2.3. Mercury analysis

Total Hg concentrations in mg/kg dry weight (ppm) wasmeasured in homogenized muscle-tissue and whole-body samplesof dogfish, skates, and prey (~0.03 g dry weight) using automatedcombustion atomic absorption spectrometry (AC-AAS) (DMA-80Direct Hg Analyzer, Milestone, Inc., Shelton, Connecticut, USA),with a detection limit of 0.01 ng Hg (US EPA, 1998). The Hg analyzerwas calibrated using certified reference materials (CRMs) of knownHg concentrations, and included solid standards (TORT-1: lobsterhepatopancreas; DORM-2: dogfish muscle) and aqueous standards

prepared by the National Research Council Canada, Institute ofEnvironmental Chemistry (Ottawa, Canada) and the NationalInstitute of Standards and Technology (Gaithersburg, Maryland,USA), respectively. Calibration curves were highly linear (meanR2 ¼ 1.00; range R2 ¼ 0.99e1.00; p < 0.0001), and the recovery ofindependently analyzed samples of TORT-1, DORM-2, and PACS-2(marine sediment) CRMs ranged from 91.9% to 107.5%(mean ¼ 96.2%). All samples were analyzed as duplicates, and anacceptance criterion of 10% was implemented. Duplicate sampleswith <10% error were averaged for subsequent analysis (meanabsolute difference between duplicates¼ 3.8%). Samples with >10%error were reanalyzed to achieve the acceptance criterion or wereeliminated from further analysis. For additional quality control,blanks were analyzed every 10 samples to assess instrument ac-curacy and potential drift. Further, two previous studies deter-mined that AC-AAS used in this study produced statisticallyequivalent results to isotope dilution gas chromatography-inductively coupled plasma mass spectrometry, with R2 valuesranging from 0.902 to 0.946 between the twomethods (Piraino andTaylor, 2009; Payne and Taylor, 2010).

2.4. Diet and trophic ecology analysis

The contents of preserved dogfish and skate stomachs wereextracted in the laboratory and the total weight of these contentswas measured with analytical balances (mg wet weight). All

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e33 23

recovered prey items were identified to the lowest practical taxonwith the aid of stereomicroscopes, and when possible, the length orwidth of individual prey was measured as defined above. Thecontribution of each prey taxon to the overall diet of dogfish andskates was expressed as the frequency of occurrence (%F) andpercent weight (%W). Frequency of occurrence was calculated asthe number of stomachs containing a specific prey taxon divided bythe total number of stomachs with prey contents, whereas percentweight was calculated as theweight of a specific prey taxon dividedby the total weight of all prey types. The relative importance of eachprey taxon to the diet of dogfish and skates was also assessed usinga modified alimentary index (%IA):

%IA ¼ IAiPni¼1IAi

� 100 (1)

where, IA is calculated for each prey taxon i as the product of %Fi and%Wi, and n is the total number of prey taxa identified in the stomachcontents of dogfish and skates.

Stable isotope analysis was used to complement stomach con-tent data and assess the effect of trophic processes on dogfish andskate Hg concentrations (Shiffman et al., 2012). Specifically, stablenitrogen (15N/14N) isotope signatures were used to estimate time-integrated feeding history (Michener and Kaufman, 2007),whereas carbon (13C/12C) isotopes were used as indicators of theinitial carbon source to the marine food web, thus allowing forthe differentiation between pelagic and benthic trophic pathways(Fry and Sherr,1984). A sub-sample of dogfish and skates previouslyselected for stomach content analysis were used for stable isotopemeasurements (smooth dogfish: n ¼ 41; spiny dogfish: n ¼ 107;little skate: n ¼ 90; winter skate: n ¼ 82). Isotope measurements ofa sub-sample of muscle tissue (~1 mg dry weight) were performedby the Boston University Stable Isotope Laboratory (Boston, Mas-sachusetts) using automated continuous-flow isotope ratio massspectrometry (CF-IRMS). Previous studies on the stable isotopesignatures of cartilaginous fishes indicated that their muscle tissuehas isotopic turnover rates of 11e14 months (MacNeil et al., 2006;Logan and Lutcavage, 2010), and in this study, muscle samples werenot pre-treated for lipid extraction owing to the relatively low lipidcontent of this tissue (Hussey et al., 2010; Kim et al., 2011). Ratios of15N/14N and 13C/12C are described using the standard delta notation(d), expressed as the relative per mil (‰) difference between thesamples and international standards (atmospheric nitrogen, 15Nair,and Vienna Pee Dee Belemnite, 13CV-PDB, respectively), and calcu-lated using the following equation:

dX ¼�Rsample

.Rstandard � 1

�� 1000 ð‰Þ (2)

where, X is 15N or 13C and R is 15N/14N or 13C/12C. The recovery ofinternal reference materials (peptone and glycine) for the CF-IRMSmethod was 99.6% and 99.7% for nitrogen and carbon, respectively.The mean sample precision determined from duplicate analyseswas 98.6% (range ¼ 90.2e100.0%) and 99.5% (range ¼ 93.1e100.0%)for nitrogen and carbon, respectively.

2.5. Data analysis

Inter-species differences in mean total Hg concentrations andisotopic signatures (d15N and d13C) among dogfish and skates wereanalyzed with two-way analysis of variance (ANOVA) models usingspecies and sex as fixed factors, whereas differences in prey Hgcontent across taxa were examined with a one-way ANOVA model.The post hoc separation of mean differences in Hg and isotopevalues across 4 levels of target species and 4 levels of prey species

(Hg only) were contrasted with independentRyaneEinoteGabrieleWelsch (Ryan's Q) multiple comparisontests. Prior to these analyses, data were log10-transformed to meetassumptions of normality and homogeneity of variance. The effectsof body size, age, and isotopic values on the Hg concentration ofdogfish, skates, and prey (size only) were analyzed with least-squares exponential regressions (size and age) and linear re-gressions (d15N and d13C). Also for dogfish and skates, analysis ofcovariance (ANCOVA) models were used to assess the effect of sexand species on Hg bioaccumulation rates, with age as the covariateand sex or species as the discrete explanatory variable. Lastly,multiple linear regression analysis was used to assess the effects ofseveral biotic and abiotic variables on Hg concentrations and iso-topic signatures of dogfish and skates. Five regression models wereemployed that either examined: (1) the independent effects ofbody size, location of catch (latitude and longitude; decimal de-grees), and time of catch (year and day of collection) on theresponse variables, or (2) the cumulative effects of all predictorvariables, as determined from global and stepwise linear regressionmodels. Small-sample, bias-corrected Akaike's Information Crite-rion (AICc) and Akaike's weights (wi) were used to evaluate andselect the optimal regression model (Burnham and Anderson,2002):

AICc ¼ �2loghL�bq�iþ 2K þ 2KðK þ 1Þ

n� K � 1(3)

wi ¼ expð�0:5DiÞ,X5

k¼1

expð�0:5DkÞ (4)

where, L is the likelihood function of themodel parameters, n is thesample size, K is the number of regression parameters, and Di isequal to AICc,i � AICc,min. The model with the smallest AICc value(AICc,min) had the most support, and the wi value quantified theprobability that model i was the best among the candidate models.

3. Results and discussion

3.1. Mercury concentrations and bioaccumulation in cartilaginousfishes

Mean total Hg concentrations varied significantly among dog-fish and skate species, but not as a function of their sex (Tables 1and 2). Smooth dogfish had the highest mean Hg concentration(mean ± 1 SD ¼ 3.3 ± 2.1 ppm), followed by spiny dogfish(1.1 ± 0.7 ppm) and skates (little: 0.4 ± 0.3 ppm; winter:0.3 ± 0.2 ppm) (Fig. 2A). The Hg concentrations reported in thisstudy are consistent with literature values for conspecifics andcongeners from other geographic areas, including those collectedfrom European and Asian waters (Table 3). Conversely, there is alsoevidence of spatial and temporal variations in target fish Hg con-tent. In US coastal environments, for example, spiny dogfishcollected from the Pacific during the early to mid-1970s hadmarkedly higher Hg concentrations relative to Atlantic conspecifics(Table 3). In the northwestern Atlantic, the mean Hg content ofspiny dogfish has ostensibly declined ~35% over the last severaldecades. Winter skate Hg concentrations in this study were also~50% greater than levels measured in equally-sized conspecificsfrom New York commercial markets, where skates were collectedfrom a relatively broad geographic area (mid- to north Atlantic; U.S.US EPA, 2013). The observed spatio-temporal differences in fish Hgburdens are attributed to geographic variability and historicalchanges in contaminant inputs to coastal habitats (Benoit et al.,2003); the latter includes biota directly responding to recent

Table 1Comparison of total length, disk width, whole-body wet weight, and age among smooth dogfish, spiny dogfish, little skates, and winter skates. Sample sizes (n), means (±1 SD),and ranges are reported for males, females, and combined data sets. Size data are also reported for representative prey.

Species n Length/width (mm) Weight (kg) Age (year)

Mean ± SD Range Mean ± SD Range Mean ± SD Range

Smooth dogfishMale 30 800.9 ± 95.8 670e1080 2.73 ± 0.69 1.48e4.62 1.97 ± 1.34 0.78e7.59Female 24 829.3 ± 101.6 599e1090 4.03 ± 1.10 1.43e6.00 2.00 ± 1.04 0.33e5.38Combined 54 813.5 ± 98.5 e 3.31 ± 1.10 e 1.98 ± 1.20 e

Spiny dogfishMale 19 599.4 ± 31.2 500e645 1.60 ± 0.23 0.98e2.00 7.13 ± 0.81 4.74e8.46Female 105 685.1 ± 49.6 500e801 2.83 ± 0.74 1.04e5.78 8.91 ± 1.38 4.66e12.73Combined 124 672.1 ± 56.4 e 2.65 ± 0.82 e 8.64 ± 1.45 e

Little skateMale 114 267.3 ± 15.6 215e295 0.60 ± 0.10 0.34e0.83 6.61 ± 0.91 4.04e8.50Female 59 264.5 ± 18.4 220e295 0.60 ± 0.10 0.32e0.77 5.19 ± 0.88 3.32e6.97Combined 173 266.2 ± 16.6 e 0.60 ± 0.10 e 6.13 ± 1.12 e

Winter skateMale 80 326.6 ± 86.0 210e547 1.20 ± 1.07 0.23e5.17 6.31 ± 2.90 2.91e15.05Female 68 350.7 ± 70.2 205e505 1.40 ± 0.84 0.25e4.60 7.39 ± 2.21 3.17e12.82Combined 148 338.4 ± 79.7 e 1.31 ± 0.98 e 6.84 ± 2.65 e

PreyScup 126 203.3 ± 69.7 65e340 0.249 ± 0.201 0.006e0.872 e e

Butterfish 87 121.8 ± 33.8 40e195 0.045 ± 0.033 0.004e0.174 e e

Squid 84 90.6 ± 38.7 34e205 0.038 ± 0.033 0.002e0.154 e e

Cancer crab 41 65.4 ± 35.9 15e125 0.075 ± 0.083 0.001e0.269 e e

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e3324

reductions in point sources of Hg in the northeastern US(Sunderland et al., 2012). Moreover, geochemical, physicochemical,and ecological processes in marine coastal habitats vary overrelatively small spatial and temporal scales, thus affecting Hgmobilization and its eventual incorporation and transfer throughtrophic pathways (Chen et al., 2008).

Total Hg concentrations in dogfish and skates were directlyrelated to their body size and age (Table 4; Figs. 3 and 4), confirmingthe accumulation of Hg in muscle tissue. Multivariate regressionanalysis and estimates of the AICc andwi further revealed that bodysize was the most significant factor affecting the Hg content of allspecies (Table 5), although the level of influence varied betweendogfish (R2 ¼ 0.27e0.29) and skates (R2 ¼ 0.08e0.10). There werealso significant seasonal and annual variations in spiny dogfish andwinter skate Hg concentrations (Table 5), but these factorscontributed minimally to the cumulative R2-values for each model(day and year partial R2-values ¼ 0.03e0.04). Previous studiespurported Hg bioaccumulation in dogfish (Forrester et al., 1972;Hall et al., 1977; de Pinho et al., 2002; Endo et al., 2009, 2013),which is attributed to the disproportionate uptake of Hg relative toits low depuration rate (Maz-Courrau et al., 2012). In contrast,Storelli et al. (1998) found no correlation between the Hg content ofthree skate species (Raja spp.) and their respective body weight.

Total Hg concentrations varied significantly by sex in little skateswhen age was included as a covariate, such that females hadincreased contaminant levels at a given age relative to males(Table 6). Conversely, Hg concentrations did not differ between

Table 2Summary statistics for two-way analysis of variance (ANOVA) models used to examine t(d15N) and carbon (d13C) isotope signatures as a function of species and sex. Target fish i(Win). Also reported are the summary statistics for a one-way ANOVA model used to exasquid (Squ), and butterfish (But). Results of Ryan's Q multiple comparisons tests that con

Factor Species Sex

F (df) p F (df) p

Target fishHg 344.7 (3) <0.0001 1.88 (1) 0d15N 54.41 (3) <0.0001 7.65 (1) <0d13C 1506.0 (3) <0.0001 0.75 (1) 0

PreyHg 109.8 (3) <0.0001 e e

sexes in dogfish and winter skates (Table 6). The absence of gender-specific Hg burdens in dogfish is inconsistent with prior studies,and to the knowledge of the authors, has not been examined inskates. Endo et al. (2009, 2013) observed that male spiny dogfish(16e41 years) and star-spotted dogfish (Mustelus manazo) (4e8years) had higher Hg concentrations relative to females(S. acanthias: 18e61 years;M.manazo: 2e14 years), which is causedby the cessation of somatic growth in mature male dogfish. In thisstudy, the lack of gender effects on dogfish Hg concentrations werelikely due to the comparatively narrow age ranges examined intarget fishes (Table 1); noting that Endo et al. (2009, 2013) reportednegligible differences in sex-specific Hg concentrations at youngerage classes.

Hg bioaccumulation rates did not differ between smooth andspiny dogfish, and similarly, between little and winter skates(ANCOVA: Age � Species, p ¼ 0.06e0.16; Table 6). At a defined age,however, smooth dogfish and little skates had higher Hg concen-trations than spiny dogfish and winter skates, respectively (Table 6;Fig. 4). It is well documented that rapid somatic growth in bonyfishes reduces overall Hg burdens through growth dilution; aresponse caused by the disproportionate increase in fish size rela-tive to Hg dietary intake (Wang, 2012 and references therein). Re-sults from this study contradict growth dilution because of theincreased Hg content of faster growing species (Collette and Klein-MacPhee, 2002; Frisk and Miller, 2006). Endo et al. (2013) alsoobtained results that refuted Hg biodilution in cartilaginous fishes,such that the star-spotted dogfish had higher Hg concentrations

arget fish total mercury (Hg) concentrations (ppm dry weight) and stable nitrogennclude smooth dogfish (Smo), spiny dogfish (Spi), little skate (Lit), and winter skatemine prey Hg as a function of species, which include scup (Scu), cancer crabs (Can),trast Hg or isotope values across 4 levels of dogfish/skate and prey are reported.

Species � sex Ryan's Q test

F (df) p

.171 0.77 (3) 0.509 Smo > Spi > Lit ~ Win

.01 6.36 (3) <0.0005 Smo > Lit ~ Win > Spi

.389 0.60 (3) 0.614 Lit > Smo > Win > Spi

e e Scu > Can ~ Squ > But

Fig. 2. Total mercury (Hg) concentrations (ppm dry weight) of target fish (A) and prey (D), and stable nitrogen (B) and carbon (C) isotope signatures (d15N and d13C;‰) of target fish.Box plots illustrate the median, 1st and 3rd quartiles, and maximum and minimum values. Open squares and circles represent means for female and male target fish, respectively,and solid triangles represent means for prey. Target fish include smooth dogfish, spiny dogfish, little skate, and winter skate, and prey include scup, cancer crabs, longfin squid, andbutterfish.

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e33 25

compared to slower growing spiny dogfish. Differences in thegrowth rates between mustelid and squalid dogfish (M. canis:15e20 cm TL/year; S. acanthias: 1.5e3.5 cm TL/year; Collette andKlein-MacPhee, 2002; Stehlik, 2007) are also reflected in theirmetabolic expenditures (Mustelus norrisi: 161 mg O2/kg/hr at 26 �C;S. acanthias: 92 mg O2/kg/hr at 22 �C; Brett and Blackburn, 1978;Bushnell et al., 1989; Carlson and Parsons, 2001). To sustain theircomparatively high bioenergetic demands (i.e., growth and meta-bolism), mustelid dogfish have elevated feeding rates, expressed as% body weight consumed per day (Mustelus californicus: 1.3e1.6%;S. acanthias ¼ 0.4e1.3%; Holden, 1966; Jones and Green, 1977;San Filippo, 1996), thus concurrently increasing their dietary up-take and exposure to Hg. Further, differences in the food habits andHg content of preferred prey, as discussed in subsequent sections,likely obscure the Hg growth dilution response in dogfish andskates (Stafford and Haines, 2001).

3.2. Diet and trophic ecology of cartilaginous fishes

Direct visual analysis of smooth dogfish (n ¼ 34), spiny dogfish(n ¼ 57), little skate (n ¼ 125), and winter skate (n ¼ 92) stomachcontents revealed inter-species differences in feeding habits(Tables 7 and 8), and the results herein are consistent with previousdiet analyses of the target fishes (Smith and Link, 2010). The mean

standardized weight of stomach contents was greater in dogfishthan skates (stomach content weight/whole-body wet weight~2e3% and 0.3e0.4%, respectively), whereas skates generally hadmore distinct prey taxa in a single stomach compared to dogfish(4.2e4.5 and 2.0e3.5 unique prey/stomach, respectively). The re-sults also suggest that spiny dogfish have a more restricted overalldiet relative to smooth dogfish and skates (Tables 7 and 8); spinydogfish consumed a total of 13 different prey taxa, whereas 18e21novel prey taxa were identified in the stomachs of smooth dogfishand skates (excluding “unidentified” categories).

Spiny dogfish mostly consumed pelagic prey (bony fish andsquid), whereas smooth dogfish fed almost exclusively on benthicinvertebrates (crustaceans and polychaetes) (Table 7). The domi-nant prey of spiny dogfish, with respect to frequency of occurrence,were butterfish, scup, unidentified fish, longfin squid, and cancercrabs. Butterfish also accounted for the largest percentage byweight of spiny dogfish stomach contents, followed by longfinsquid, unidentified fish, scup, and silver hake. The order of impor-tance of prey to the diet of spiny dogfish, as expressed by thealimentary index (%IA), were butterfish, longfin squid, and un-identified fish, while the remaining prey groups had %IA less than3%. Cancer crabs, polychaetes, and unidentified animal tissue(including fish and crabs) were the most frequency encounteredprey in smooth dogfish stomachs, followed by algae/detritus, and

Table 3Literature review of dogfish and skate total mercury (Hg) concentrations (ppm dry weight). The following information is provided for each source document: fish species,location of sample, sample size (n), mean total length (TL; cm), and mean Hg concentrations reported in the “literature”. For comparative purposes, the total Hg content ofMustelus canis, Squalus acanthias, and Leucoraja ocellata (pre-defined size) were estimated from the exponential (Hg-size) regressionmodels presented in “this study” (Table 4).

Species Location n TL Total Hga Literature source

Literature This study

DogfishMustelus canis Southern coastal Brazil 79 89.2 1.6 1.7 de Pinho et al. (2002)Mustelus manazo Northern coastal Japan 61 94.0 3.6 e Endo et al. (2013)b

Mustelus mustelus Langebaan Lagoon, South Africa 12 112.5 8.4 e Bosch et al. (2013)b,c

Squalus acanthias Northwestern Atlantic, US 80 76.6 1.6 1.2 Greig et al. (1977)d

S. acanthias Northeastern Pacific, US 127 94.2 3.7 1.7 Hall et al. (1977)e

S. acanthias Northeastern Pacific, US 88 86.8 2.4 1.5 Childs and Gaffke (1973)c

S. acanthias Coastal Japan 75 86.9 1.4 1.5 Endo et al. (2009)b

S. acanthias Eastern Mediterranean Sea 47 58.0 8.3 0.84 Kousteni et al. (2006)c

SkateLeucoraja ocellata Commercial markets, New York, US 14 36.6 0.24 0.50 US EPA (2013)Raja asterias Adriatic Sea 120 44 2.9 e Storelli et al. (2003)Raja clavata Mouth of River Tyne, England 22 45.6 0.39 e Dixon and Jones (1994)R. clavata Bay of Biscay, France 11 93.5 2.0 e Chouvelon et al. (2012)Raja eglanteria Lower Delaware Bay, US 3 26 0.86 e Gerhart (1977)c,f

Raja kenojei Eastern China Sea 2 39 0.68 e Asante et al. (2008)Raja kwangtungensis Eastern China Sea 3 35 <0.2 e Asante et al. (2008)Raja microocellata Bay of Biscay, France 5 69.4 0.17 e Chouvelon et al. (2012)

a Literature Hg values expressed as wet weight were converted to dry weight assuming 75% water content (Bosch et al., 2013).b Literature values averaged across female and male dogfish.c Median length.d Samples collected from New York Bight to Gulf of Maine.e Female dogfish only.f Body size ¼ disk width (cm).

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e3326

other decapod crustaceans. According to other measures of dietaryimportance, cancer crabs and unidentified fish were the most uti-lized prey resource by smooth dogfish, while all remaining preywere of lesser importance (%IA < 1%).

Little skates and winter skates mostly consumed benthic prey(Table 8). Amphipods were the most frequently observed prey in

Table 4Summary statistics for univariate (non-linear) exponential and linear regressionmodels ulength (ML), and carapace width (CW)], age (years), and stable nitrogen (d15N) and carbweight).

Species/Relationship Regression model

Smooth dogfishHgeTL log(Hg) ¼ 1.47E�3 � TL�0.763HgeAge log(Hg) ¼ 0.115 � Age þ 0.200Hged15N Hg ¼ 0.516 � d15N�3.841Hged13C Hg ¼ 1.205 � d13C þ 23.32

Spiny dogfishHgeTL log(Hg) ¼ 1.99E�3 � TL�1.332HgeAge log(Hg) ¼ 0.081 � Age�0.696Hged15N Hg ¼ 0.555 � d15N�5.276Hged13C Hg ¼ 0.342 � d13C þ 8.654

Little skateHgeDW log(Hg) ¼ 4.56E�3 � DW�1.698HgeAge log(Hg) ¼ 0.050 � Age�0.792Hged15N Hg ¼ 0.153 � d15N�1.439Hged13C Hg ¼ 0.231 � d13C þ 4.203

Winter skateHgeDW log(Hg) ¼ 6.93E�4 � DW�0.849HgeAge log(Hg) ¼ 0.020 � Age�0.750Hged15N Hg ¼ 0.044 � d15N�0.238Hged13C Hg ¼ 3.48E�2 � d13C þ 0.893

ScupHgeTL log(Hg) ¼ 3.29E�3 � TL�1.283

ButterfishHgeTL log(Hg) ¼ 3.63E�3 � TL�1.636

SquidHgeML log(Hg) ¼ 2.86E�3 � ML�1.246

Cancer crabHgeCW log(Hg) ¼ 7.36E�3 � CW�1.399

skate stomachs, followed by polychaetes and other crustaceans,including sand shrimp, cancer crabs, and isopods. Amphipods andpolychaetes also accounted for a high percentage of the stomachweight in both skate species, while fish also contributed consider-ably to the stomach weight of larger winter skates (>350 mm DW),including sand lance and scup. The order of prey dietary

sed to examine the effect of body size [mm; total length (TL), disk width (DW), mantleon (d13C) isotope signatures on biota total mercury (Hg) concentrations (ppm dry

F (df) p R2

19.56 (1, 53) <0.0001 0.27317.74 (1, 53) <0.0001 0.2522.53 (1, 40) 0.120 0.0614.10 (1, 40) <0.05 0.095

49.14 (1, 123) <0.0001 0.28756.70 (1, 123) <0.0001 0.31772.16 (1, 105) <0.0001 0.41021.82 (1, 105) <0.0001 0.173

18.51 (1, 172) <0.0001 0.0989.66 (1, 172) <0.005 0.054

15.01 (1, 87) <0.0005 0.1498.93 (1, 87) <0.005 0.094

13.24 (1, 147) <0.0005 0.08311.95 (1, 147) <0.001 0.0764.41 (1, 79) <0.05 0.0540.58 (1, 79) 0.450 0.007

338.6 (1, 125) <0.0001 0.732

58.38 (1, 86) <0.0001 0.407

57.18 (1, 83) <0.0001 0.411

86.35 (1, 40) <0.0001 0.689

Fig. 3. Total mercury (Hg) concentrations (ppm dry weight) of target fish as a function of body size (total length or disk width; mm), and stable nitrogen and carbon isotopesignatures (d15N and d13C; ‰). Target fish include smooth dogfish (AeC), spiny dogfish (DeF), little skates (GeI), and winter skates (JeL). For significant relationships, exponentialand linear regression models were fit to size and isotope data, respectively.

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e33 27

importance for skates, expressed as %IA, were amphipods, poly-chaetes, sand shrimp, and cancer crabs, while the remainingidentifiable prey taxa had %IA less than 3%.

Stable nitrogen (d15N) isotope signatures were used to approx-imate the trophic status of dogfish and skates (Michener andKaufman, 2007), and mean d15N values varied significantlyamong target fish (Table 2). Smooth dogfish had a significantlyenriched d15N signature relative to spiny dogfish (13.2 ± 0.7 and11.6 ± 0.8‰, respectively), which corresponds to smooth dogfish

occupying a higher trophic position (Fig. 2B). The depleted d15Nsignature of spiny dogfish is attributed to the dietary contributionof low trophic level prey, including planktivorous forage fish (e.g.,butterfish; %IA ¼ 48.4%; Table 7) and possibly ctenophores (Smithand Link, 2010), although ctenophores were not detected in dog-fish stomachs due to their fragile tissues. Moreover, female spinydogfish (11.7 ± 0.7‰) had a significantly higher d15N value relativeto male conspecifics (10.8 ± 0.4‰), thus explaining the speciesesexinteraction effect in the two-way ANOVAmodel (Table 2). Little and

Fig. 4. Total mercury (Hg) concentrations (ppm dry weight) of dogfish (A) and skates(B) as a function of age. Smooth dogfish and little skates are denoted by solid circles,whereas spiny dogfish and winter skates are represented by open circles. Exponentialregression models were fit to species-specific data.

Table 5Summary statistics for small-sample, bias-corrected Akaike's Information Criterion (AICRegression analyses were used to predict dogfish and skate total mercury (Hg) concentratias function of several explanatory variables, including body size [mm; total length (TL) an[decimal degrees; latitude (Lat) and longitude (Long)]. Positive (þ) and negative (�) symbresponse variable, and “NS” is not significant.

Species/response variable Optimal model F (d

Smooth dogfishHg TL (þ) 19.5d15N Lat (þ) 5.7d13C Lat (þ)/Day (þ) 2.9

Spiny dogfishHg TL (þ)/Day (�)/Year (�) 19.5d15N TL (þ)/Long (�)/Day (þ) 21.5d13C Lat (NS) 0.7

Little skateHg DW (þ) 18.5d15N Day (þ)/Lat (þ)/Long (�)/DW (þ) 11.0d13C DW (þ)/Long (�) 5.5

Winter skateHg DW (þ)/Year (þ) 9.1d15N DW (þ)/Long (�)/Day (þ) 68.9d13C DW (�)/Year (þ)/Day (þ) 15.9

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e3328

winter skates had significantly lower d15N signatures than smoothdogfish, but the mean d15N values between skate species did notdiffer (little: 12.0 ± 0.7‰; winter: 11.9 ± 1.0‰; Fig. 2B), suggestingthat these species occupy the same, relatively low, trophic level.

Stable carbon (d13C) isotope signatures were used to differen-tiate among varying sources of primary production to the coastalfood web, and thus, distinguish between benthic and pelagic tro-phic linkages (Peterson and Howarth, 1987; France, 1995). Meand13C values ranged from �22.0 to �16.5‰ and varied significantlyamong dogfish and skates, but not as a function of their sex(Table 2; Fig. 2C). Moreover, two distinct isotopic groups wereevident that further corroborated this study's stomach contentanalysis. The depleted d13C value of spiny dogfish (~�22‰) indi-cated a phytoplankton-based (pelagic) food web, which is consis-tent with their preferred consumption of butterfish and squid.Conversely, the more enriched d13C signatures (~�17‰) of smoothdogfish and skates suggest benthic sources of primary production,which is presumably derived from their consumption of epibenthiccrustaceans and infaunal polychaetes.

Body size, location of catch (latitude and longitude), and time ofcatch (day of year and year) were the most significant factorsaffecting dogfish and skate isotopic signatures (Table 5). The esti-mated slope coefficients for the size-d15N relationship were posi-tive for spiny dogfish and skates, indicating that older individualsforage at higher trophic levels. There was also an inverse relation-ship between body size and d13C values in winter skates, which isattributed to larger skates (>350 mm DW) consuming pelagic prey,including butterfish, sand lance, and squid (Table 8). Dogfish andskate isotopic signatures also exhibited significant spatio-temporalvariations (Table 5). Specifically, d15N and d13C values increased in anortheasterly direction, in closer proximity to the mainland (“þ”

and “�” coefficient for latitude and longitude, respectively) (Fig. 1),as well as becoming more enriched as the sampling season pro-gressed (“þ” coefficient for day of year and year). It is unlikely thatdifferences in dogfish and skate foraging ecology accounted for theobserved spatio-temporal variations in isotopic values. It is moreprobable that these differences are the result of species-specificseasonal and annual migrations, and thus, spatio-temporal vari-ability in habitat use. This is especially relevant to dogfish becauseof their expansive coastal migrations (Collette and Klein-MacPhee,2002). Moreover, the added effect of site-specific environmentalconditions (e.g., spatially-explicit salinity profiles, terrestrially-

c) and Akaike’s weights (wi) used to select optimal multivariate regression models.ons (ppm dryweight) and stable nitrogen (d15N) and carbon (d13C) isotope signaturesd disk width (DW)], time of catch (year and day of collection), and location of catchols in parentheses after each explanatory variable denote their level of effect on each

f) p R2 AICc wi

6 (1, 53) <0.0001 0.273 �153.3 0.564 (2, 40) <0.01 0.232 �33.6 0.515 (2, 40) <0.01 0.243 �85.3 0.87

6 (3, 123) <0.0001 0.328 �432.5 0.746 (3, 105) <0.0001 0.388 �122.1 0.672 (1, 105) 0.398 0.007 �63.3 0.40

1 (1, 172) <0.0001 0.098 �504.8 0.979 (4, 87) <0.0001 0.348 �100.2 0.705 (2, 87) <0.01 0.116 �190.5 0.70

0 (2, 147) <0.0005 0.112 �498.1 0.815 (3, 79) <0.0001 0.731 �96.4 0.517 (1, 79) <0.0001 0.387 �149.8 0.82

Table 6Summary statistics for analysis of covariance (ANCOVA) models used to examine theeffect of sex and species on intra- and inter-specific total mercury bioaccumulationrates (ppm dry weight as function of age).

Factor Age � sex Age Sex

F (df) p F (df) p F (df) p

Smooth dogfish 1.63 (1) 0.208 17.25 (1) <0.0001 0.08 (1) 0.778Spiny dogfish 1.17 (1) 0.282 53.44 (1) <0.0001 1.65 (1) 0.202Little skate 0.38 (1) 0.539 17.75 (1) <0.0001 7.82 (1) <0.01Winter skate 0.59 (1) 0.443 10.43 (1) <0.005 0.52 (1) 0.473

Factor Age � species Age SpeciesF (df) p F (df) p F (df) p

Dogfishes 2.01 (1) 0.158 67.68 (1) <0.0001 168.02 (1) <0.0001Skates 3.53 (1) 0.061 17.09 (1) <0.0001 35.55 (1) <0.0001

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e33 29

derived and increased nutrient loading along the immediatecoastline) can have pronounced effects on the isotopic signatures ofthe target fishes (Pruell et al., 2006; Michener and Kaufman, 2007).

3.3. Trophic effects on cartilaginous fish mercury concentrations

Representative prey of dogfish and skates were measured fortotal Hg content to assess their potential effect on target fish Hglevels (Table 1). Mean prey Hg concentrations varied significantlyacross taxa (Table 2; Fig. 2D), such that scup had the highest Hg

Table 7Stomach contents of smooth dogfish and spiny dogfish. Values represent the percent frequmean (±1 SD) stomach content weight relative to whole-body wet weight and number ofand include total length (fish), carapace width (crab), carapace length (lobster) and man

Prey Smooth dogfish

Taxon %F %W %IA

Fish [32.3] [22.Butterfish (Peprilus triacanthus) 2.9 1.5 0.1Scup (Stenotomus chrysops) 5.9 6.0 0.6Silver hake (Merluccius bilinearis) 0 0 0American eel (Anguilla rostrata) 0 0 0Searobin (Prionotus sp.) 0 0 0Smallmouth flounder (Etropus microstomus) 0 0 0Sand lance (Ammodytes americanus) 0 0 0Herring (Alosa spp.) 0 0 0Skate (Rajidae) 5.9 4.1 0.4Spiny dogfish (Squalus acanthias) 2.9 0.8 0.04Unidentified fish 64.7 19.9 21.4

Crustaceans e [64.8] [76.Cancer crab (Cancer spp.) 82.4 54.7 74.6Lobster (Homarus americanus) 8.8 3.0 0.4Hermit crab (Pagurus spp.) 8.8 0.8 0.1Mud crab (Panopeus herbstii) 2.9 2.2 0.1Spider crab (Majidae) 2.9 0.8 0.4Isopod (Isopoda) 5.9 0.2 0.02Amphipod (Amphipoda) 2.9 <0.01 <0.0Mud shrimp (Thalassinoidea) 5.9 0.2 0.02Unidentified crabs 29.4 2.5 1.2Unidentified crustaceans 5.9 0.5 0.05

Molluscs e [0.4] [0.0Longfin squid (Doryteuthis pealeii) 5.9 0.3 0.03Shortfin squid (Illex sp.) 0 0 0Moon snail (Naticidae) 2.9 0.1 <0.0

Worms e [0.5] [0.2Polychaete (Polychaeta) 17.7 0.5 0.2Ribbon worm (Nemertea) 2.9 <0.01 <0.0

Cnidarians e Hydrozoa 2.9 0.02 <0.0Animal remains 26.5 1.9 0.8Eelgrass/Algae/Detritus 11.8 0.05 0.01Sediment 8.8 0.04 <0.0

Stomachs examined (n) 34Stomach content weight/whole-body weight (%) 1.70 ± 1.00Number of unique prey/stomach 3.47 ± 1.83

content (0.29 ± 0.18 ppm), followed by crabs (0.16 ± 0.11 ppm),squid (0.11 ± 0.04 ppm), and butterfish (0.07 ± 0.4 ppm). Prey Hgconcentrations were also positively related to body size (Table 4;Fig. 5), again indicating the bioaccumulation of the contaminant.Inter-species differences in dogfish and skate Hg concentrations areadequately explained by the Hg content of their preferred prey. Inthis study, smooth dogfish had the highest Hg concentration amongtarget fishes, and this species preferentially consumed cancer crabswith a mean body size of 55 mm CW, i.e., the mean size of crabsrecovered from smooth dogfish stomachs (Table 7). Crabs of thisrelatively large size have an estimated Hg content of 0.10 ppm, asdetermined from the Hg-size regression model (Table 4). It isimportant to reiterate that crabs in this study were processed aswhole bodies, whereas the Hg content of other prey was measuredin excised muscle tissue. This discrepancy in tissue-type likelyunderestimates the Hg concentration of cancer crabs. For example,the Hg content of blue crab (Callinectes sapidus) muscle tissue is~30% greater than the Hg burden of whole-body samples (Adamsand Engel, 2014). Spiny dogfish had a moderate level of Hgcontamination, and this species relied on prey that had both lowand high Hg concentrations; in order of dietary importance, but-terfish (Hg ¼ 0.06 ppm for 108 mm TL fish), longfin squid(Hg¼ 0.17 ppm for 168mmML squid), and scup (Hg¼ 0.11 ppm for94 mm TL fish) (Tables 4 and 7). Finally, little and winter skates hadthe lowest Hg concentrations observed in this study, and thesespecies fed upon amphipods, polychaetes, and small cancer crabs

ency of occurrence (%F), percentweight (%W), alimentary index (%IA; Eq. (1)), and theunique prey per stomach. The mean (±1 SD) of intact prey body size is also reported,tle length (squid). Squared brackets indicate major taxon sub-totals for %W and %IA.

Spiny dogfish

Size %F %W %IA Size

5] [64.7] [64.5]6.0 ± 0 42.3 42.0 48.4 10.8 ± 1.9e 17.3 3.9 1.9 9.4 ± 2.3e 5.8 3.7 0.6 22.0 ± 0e 1.9 1.8 0.1 40.6 ± 0e 1.9 0.7 0.03 e

e 1.9 0.2 0.01 e

e 1.9 0.1 0.01 10.2 ± 0e 1.9 0.04 <0.01 e

e 0 0 0 e

e 0 0 0 e

e 40.4 12.3 13.5 e

5] e e [5.3] [1.9] e

5.5 ± 2.6 13.5 5.2 1.9 7.6 ± 3.68.3 ± 3.9 0 0 0 e

2.3 ± 0 0 0 0 e

6.7 ± 0 0 0 0 e

4.6 ± 0 0 0 0 e

4.5 ± 0 0 0 0 e

1 e 3.9 <0.01 <0.01 e

e 0 0 0 e

e 0 0 0 e

e 3.9 0.01 <0.01 e

3] e e [27.3] [31.3] e

9.3 ± 5.7 42.3 27.2 31.3 16.8 ± 4.6e 1.9 0.1 <0.01 5.5 ± 0.0

1 e 0 0 0 e

] e e [0] [0] e

e 0 0 0 e

1 e 0 0 0 e

1 e 0 0 0 e

e 30.8 2.7 2.3 e

e 1.9 <0.01 <0.01 e

1 e 5.8 0.1 <0.01 e

572.76 ± 2.782.00 ± 1.12

Table 8Stomach contents of little skates and winter skates. Values represent the percent frequency of occurrence (%F), percent weight (%W), alimentary index (%IA; Eq. (1)), and themean (±1 SD) stomach content weight relative to whole-body wet weight and number of unique prey per stomach. The mean (±1 SD) of intact prey body size is also reported,and include total length (fish), carapace width (crab), carapace length (lobster) and mantle length (squid). Squared brackets indicate major taxon sub-totals for %W and %IA.

Prey Little skate Winter skate

Taxon %F %W %IA Size %F %W %IA Size

Fish e [3.8] [0.2] e e [35.1] [4.0] e

Butterfish (Peprilus triacanthus) 1.7 3.1 0.1 6.8 ± 0 2.2 4.6 0.4 12.1 ± 4.0Sand lance (Ammodytes americanus) 0 0 0 e 4.4 15.4 2.4 11.0 ± 1.4Scup (Stenotomus chrysops) 0 0 0 e 2.2 13.6 1.0 12.1 ± 4.7Herring (Alosa spp.) 0 0 0 e 1.1 0.5 0.02 e

Unidentified fish 9.2 0.7 0.1 e 5.6 1.1 0.2 e

Crustaceans e [64.4] [68.9] e e [35.5] [51.0] e

Amphipod (Amphipoda) 83.3 29.5 50.6 e 74.4 15.6 40.4 e

Isopod (Isopoda) 10.8 0.4 0.1 e 16.7 2.3 1.3 e

Sand shrimp (Crangon septemspinosa) 55.8 7.4 8.5 e 34.4 3.6 4.3 e

Pandalid shrimp (Pandalidae) 5.0 1.7 0.2 e 3.3 0.1 0.01 e

Hooded shrimp (Cumacea) 4.2 0.04 <0.01 e 6.7 0.03 0.01 e

Mud shrimp (Thalassinoidea) 3.3 2.3 0.2 e 2.2 1.7 0.1 e

Grass shrimp (Hippolytidae/Palaemonidae) 4.2 1.1 0.1 e 2.2 0.1 0.01 e

Cancer crab (Cancer spp.) 25.0 7.7 4.0 0.8 ± 0.4 13.3 6.3 2.9 1.8 ± 0.8Hermit crab (Pagurus spp.) 0.8 0.01 <0.01 e 0 0 0 e

Lobster (Homarus americanus) 1.7 0.9 0.03 2.7 ± 0 2.2 0.9 0.1 2.0 ± 0Unidentified shrimp 10.0 1.9 0.4 e 12.2 0.4 0.2 e

Unidentified crabs 22.5 7.0 3.2 e 10.0 3.1 1.1 e

Unidentified decapods 5.0 1.5 0.2 e 1.1 0.5 0.02 e

Unidentified crustaceans 25.0 3.2 1.6 e 20.0 1.1 0.7 e

Molluscs e [1.7] [0.05] e e [6.2] [1.0] e

Bivalves (Bivalvia) 7.5 0.1 0.02 e 11.1 0.2 0.1 e

Longfin squid (Doryteuthis pealeii) 0.8 1.2 0.02 12.8 ± 0 4.4 6.0 0.9 10.0 ± 4.4Shortfin squid (Illex sp.) 0.8 0.4 0.01 e 0 0 0 e

Worms e [16.8] [7.6] e e [10.8] [21.3] e

Polychaete (Polychaeta) 50.8 16.8 17.6 e 57.8 10.6 21.3 e

Ribbon worm (Nemertea) 0 0 0 e 1.1 0.1 <0.01 e

Peanut worm (Sipunculoidea) 0 0 0 e 1.1 0.1 <0.01 e

Round worm (Nematoda) 0.8 <0.01 <0.01 e 0 0 0 e

Porifera e Sponge 0.8 <0.01 <0.01 1.1 <0.01 <0.01Cnidarians e Hydrozoa 0 0 0 e 1.1 <0.01 <0.01 e

Animal remains 50.0 12.7 13.1 e 53.3 12.2 22.6 e

Eelgrass/Algae/Detritus 3.3 0.3 0.02 e 3.3 0.02 <0.01 e

Sediment 15.0 0.2 0.1 e 22.2 0.2 0.1 e

Stomachs examined (n) 125 92Stomach content weight/whole-body weight (%) 0.35 ± 0.30 0.37 ± 0.33Number of unique prey/stomach 4.58 ± 2.65 4.24 ± 2.80

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e3330

(<20mmCW). Payne and Taylor (2010)measured the Hg content ofamphipods and polychaetes collected from the Narragansett Bayestuary (Fig. 1), each with a mean Hg concentration of 0.09 ppm(converted fromwet weight). It is important to note that such preyspecies would likely have reduced Hg burdens in Rhode Island/Block Island Sound, as the environment is further removed fromanthropogenic influences (Taylor et al., 2012). Moreover, the esti-mated Hg content of cancer crabs consumed by skates was0.05 ppm (8e18 mm CW) (Tables 4 and 8). These collective resultsindicate that dogfish and skates are highly responsive to the Hgcontent of their preferred prey.

Stable isotope (d15N and d13C) analysis was coupled with totalHg data to provide insight into the effects of trophic processes onHg contamination in dogfish and skates. There were significantpositive relationships between Hg and d15N values measured forspiny dogfish and skates (Table 4; Fig. 3); hence verifying an in-crease in intra-specific Hg concentrations at higher trophic levels.These results are consistent with previous analyses of the trophiceffects on marine fish Hg concentrations, including several speciesof coastal and oceanic sharks (Adams et al., 2003; Cai et al., 2007;Suk et al., 2009; Maz-Courrau et al., 2012). Significant positive re-lationships were also observed between Hg and d13C valuesmeasured for dogfish and little skates (Table 4; Fig. 3). This resultsuggests that benthic associations may increase biotic Hg

concentrations via dietary intake or proximate contact with Hg-contaminated sediments, as reported elsewhere (Storelli et al.,1998; Hosseini et al., 2013). Other studies, however, indicate thatpelagic-feeding organisms (depleted d13C signatures) haveincreased Hg exposure (Chen et al., 2009; Kim et al., 2012). Ulti-mately, the fate of Hg through feeding pathways depends on thenumber of trophic steps and consumer's utilization of different preyassemblages (Kim et al., 2012), which likely vary across discreteaquatic ecosystems.

3.4. Cartilaginous fish mercury contamination from a human healthperspective

The Hg concentrations in some fish may be sufficiently high toadversely affect human health (McMichael and Butler, 2005;Willett, 2005), and human exposure to Hg occurs mainly throughdietary intake of contaminated fish (Hightower and Moore, 2003).Public health officials affiliated with federal and state agenciesrespond to the threat of fish Hg contamination by reporting criteriafor the safe consumption of fishery products, including the US FDAand US EPA threshold levels of 1.0 and 0.3 ppm Hg wet weight,respectively. Cartilaginous fishes are becoming increasingly utilizedas a human food source given the precipitous declines in traditionalfisheries (NEFSC, 1999, 2006; NMFS, 2010), thus underscoring the

Fig. 5. Total mercury (Hg) concentrations (ppm dry weight) of scup (A), butterfish (B), longfin squid (C), and cancer crabs (D) as a function of body size (total length, mantle length,or carapace width; mm). Exponential regression models were fit to the data.

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e33 31

importance of research focused on Hg contamination in thesespecies. For the purposes of comparing the results of this study tothe US FDA and US EPA action levels, Hg data originally expressed asdry weight were converted to wet weight assuming 75% watercontent of the muscle tissue (Bosch et al., 2013). Accordingly, 24.1%of smooth dogfish, 1.6% of spiny dogfish, and 0.0% of skates excee-ded the US FDA criterion of 1.0 ppm Hg wet weight. For the moreconservative US EPA threshold (0.3 ppm Hg), 87.0% of smoothdogfish, 32.0% of spiny dogfish, and <2% of skates were above thisvalue. The Hg-length exponential regression models also estimatedthat smooth and spiny dogfish obtain Hg concentrations of 0.3 ppmat relatively small body sizes (57.3 and 70.9 cm TL, respectively),whereas skates do not approach this threshold level even at theirmaximum body sizes (39.0 and 133.9 cm DW, respectively)(Table 4).

4. Conclusions

In this study, total Hg concentrations were measured in dogfishand skates, and results were evaluated relative to species-specificlife history traits. The total Hg content of dogfish and skate muscletissue was positively related to body size and age, indicating thebioaccumulation of the contaminant. Moreover, Hg concentrations

were significantly elevated in smooth dogfish, followed by spinydogfish and skates. The increased Hg content of smooth dogfishwas attributed to its upper trophic level status, consumption ofHg-enriched prey (e.g., large cancer crabs), and relatively highbioenergetic requirements. Comparatively, spiny dogfish had areduced trophic status owing to the dietary contribution of but-terfish, yet demonstrated a moderate level of Hg contaminationbecause this species also consumed high Hg prey (e.g., squid andscup). Little and winter skates were basal consumers and had thelowest Hg concentrations because they fed exclusively on Hg-depleted prey (e.g., amphipods, small decapods, and poly-chaetes). The collective results from the analysis of stable isotopesfurther indicated that Hg biomagnifies across successive trophiclevels and foraging in the benthic trophic pathway may increaseHg exposure. From a human health perspective, the consumptionof smooth dogfish and, to a lesser extent, spiny dogfish pose ahuman health risk, which therefore, justifies stringent consump-tion advisories for these species. Conversely, the consumption ofskates does not present a significant risk to human health. It is therecommendation of the authors that this information be effec-tively communicated to the general public so that citizens canmake informed decisions regarding the safe consumption offishery resources.

D.L. Taylor et al. / Marine Environmental Research 99 (2014) 20e3332

Acknowledgments

We are grateful to S. Olszewski (Rhode Island Division of FishandWildlife, Jamestown, RI), D. Palance, A. Hall, N. Kutil, G. LeBlanc,and B. Bourque (Roger Williams University, Bristol, RI) for assis-tance in sample collection and preparation. We also thank thecaptain and crew of the F/V Darana R and staff of the Northeast AreaMonitoring and Assessment Program survey for their able assis-tance in collecting the offshore samples. We thank R. Michener(Boston University Stable Isotope Laboratory, Boston, MA) for stableisotope analyses. The project described was supported by theRoger Williams University Foundation Fund Based Research Grant,the Rhode Island Ocean Special Area Management Plan(DE-EE00000293), the Commercial Fisheries Research Foundatione Southern New England Cooperative Research Initiative, and byAward P20RR016457 from the National Center for Research Re-sources (NA09NMF4720414). The content is solely the re-sponsibility of the authors and does not necessarily represent theofficial views of the National Center for Research Resources or theNational Institutes of Health.

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