Persistent organochlorines in 13 shark species from offshore and coastal waters of Korea: Species-specific accumulation and contributing factors

Ecotoxicology and Environmental Safety 115 (2015) 195–202

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Persistent organochlorines in 13 shark species from offshore and coastal waters of Korea: Species-specific accumulation and contributing factors Hyun-Kyung Lee a, Yunsun Jeong a, Sunggyu Lee a, Woochang Jeong a, Eun-Jung Choy b, Chang-Keun Kang c, Won-Chan Lee d, Sang-Jo Kim e, Hyo-Bang Moon a,n a

Department of Marine Sciences and Convergent Technology, College of Science and Technology, Hanyang University, Ansan 426-791, Republic of Korea Korea Polar Research Institute, Korea Institute of Ocean Science and Technology, Incheon 406-840, Republic of Korea School of Environmental Science and Engineering, Gwangju Institute of Science and Technology (GIST), Gwangju 500-712, Republic of Korea d National Fisheries Research and Development Institute (NFRDI), Busan 619-705, Republic of Korea e National Fisheries Products Quality Management Service, Goyang 410-315, Republic of Korea b c

art ic l e i nf o

a b s t r a c t

Article history: Received 7 January 2015 Received in revised form 9 February 2015 Accepted 10 February 2015

Data on persistent organochlorines (OCs) in sharks are scarce. Concentrations of OCs such as polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) were determined in the muscle tissue of 13 shark species (n ¼ 105) collected from offshore (Indian and Pacific Oceans) and coastal waters of Korea, to investigate species-specific accumulation of OCs and to assess the potential health risks associated with consumption of shark meat. Overall OC concentrations were highly variable not only among species but also within the same species of shark. The concentrations of PCBs, DDTs, chlordanes, hexachlorobenzene, and heptachlor in all shark species ranged from o LOQ (limit of quantification) to 184 (mean: 35.0), o LOQ to 1135 (58.2), oLOQ to 56.2 (4.31), o LOQ to 18.8 (1.64) and oLOQ to 77.5 (1.37) ng/g lipid weight, respectively. The determined concentrations of PCBs and DDTs in shark in our study were relatively lower than those reported in other studies. Aggressive shark species and species inhabiting the Indian Ocean had the highest levels of OCs. Inter-species differences in the concentrations and accumulation profiles of OCs among shark species could be explained by differences in feeding habit and sampling locations. Several confounding factors such as growth velocity, trophic position, and regional contamination status may affect the bioaccumulation of OCs in sharks. Hazard ratios of non-cancer risk for all the OCs were below one, whereas the hazard ratios of lifetime cancer risks of PCBs and DDTs exceeded one, implying potential carcinogenic effects in the general population in Korea. This is the first report to document the occurrence of OCs in sharks from Korea. & 2015 Elsevier Inc. All rights reserved.

Keywords: Organochlorines PCBs OCPs Inter-species difference Cancer risk

1. Introduction Organochlorines (OCs) such as polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) are ubiquitous contaminants on a global scale. Because of their persistent and bioaccumulative characters, OCs occur and accumulate in wildlife (Gelsleichter et al., 2005; Nakata et al., 2005; Moon et al., 2010) and humans (Bergonzi et al., 2009; Lee et al., 2013). PCBs and OCPs have adverse health effects such as developmental toxicity, cancer, and endocrine disruption (Beard, 2006; Foster et al., 2012). PCBs and OCPs are regulated by the Stockholm Convention as persistent organic pollutants (POPs) by the United Nations Environment n

Corresponding author. Fax: þ 82 31 408 6255. E-mail address: [email protected] (H.-B. Moon).

http://dx.doi.org/10.1016/j.ecoenv.2015.02.021 0147-6513/& 2015 Elsevier Inc. All rights reserved.

Programme (UNEP) since 2001 (Fielder et al., 2013). In Korea, approximately 4300 tons of PCBs and 3600 tons of OCPs were produced up till the 1990s (Breivik et al., 2002). Although the environmental levels of PCBs and OCPs have decreased considerably over the past three decades (Isobe et al., 2009; Sericano et al., 2014), these contaminants are still present in wildlife and human (Corsolini et al., 1995; Storelli and Marcotrigiano, 2001; Davis et al., 2002; Park et al., 2010; Lee et al., 2013). Sharks are cartilaginous fish and usually consume plankton, mollusks, crustaceans, and bony fishes (Parker, 2008). Some aggressive sharks (e.g. blue and white sharks) hunt large fishes, seabirds, marine mammals, and even other sharks (Parker, 2008). Due to their high trophic position, long life-span, and relatively low metabolic capacity, sharks contain high levels of POPs (Johnson-Restrepo et al., 2005). However, few studies are available on accumulation of OCs in sharks, with only one or few species and

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H.-K. Lee et al. / Ecotoxicology and Environmental Safety 115 (2015) 195–202

small sample sizes (Corsolini et al., 1995; Storelli and Marcotrigiano, 2001; Strid et al., 2007; Cascaes et al., 2014; Lu et al., 2014; Olin et al., 2014). In some countries, such as Australia, China, Japan, and Korea, sharks are consumed by the general population in form of fillets, fin soup, and nutritional supplements (e.g. liver oil). Previous studies have confirmed the human health risks associated with consumption of shark meat (Holtcamp, 2012; Man et al., 2014). In fact, the United States Environmental Protection Agency (US EPA) designated sharks as high mercury-containing fishes, which are hazardous to infants and pregnant women (US EPA, 1997). Although OCs ingested by humans via shark consumption are likely to pose health risks, little is known about residue levels and accumulation patterns of OCs in sharks (Zhou et al., 2013). In the present study, we determined the concentrations and accumulation features of OCs in 13 shark species collected from offshore and coastal waters of Korea, to investigate species-specific accumulation of these contaminants. The relationships between OC levels and certain biological factors (e.g. body length, body weight, lipid content, and trophic position) were investigated, to elucidate the contributing factors governing the bioaccumulation of OCs in a variety of sharks. Moreover, potential health risks to humans were assessed based on determining the daily intake of OCs due to consumption of shark meat by the general population of Korea.

2. Materials and methods 2.1. Sample collection Dorsal muscles were collected from 13 shark species (n ¼ 105) found entangled in the long lines of commercial fisheries or bycatch from offshore trawls of the Indian and Pacific Oceans and coastal waters of Korea during July to October in 2010. All shark species surveyed in this study are globally endangered; they are on the red list of the International Union for Conservation and Natural Resources (IUCN) (Parker, 2008). Biological information such as body length, body weight, feeding habits, and lipid content of each species are summarized in Table 1. However, the detailed information on the sampling locations of sharks collected from seawater zones (Indian and Pacific Oceans and coastal waters) are not available in our study. After dissection of the sharks on commercial ships, the collected dorsal tissues were transported to the National Fishery Products Quality Management Service, Korea, and kept frozen at 20 °C until analysis. 2.2. Experimental procedures Twenty two PCB congeners (CBs 8, 18, 28, 29, 44, 52, 87, 101, 105, 110, 118, 128, 138, 153, 170, 180, 183, 194, 195, 200, 205 and 206) composed of tri- to nona-CBs and 16 OCP compounds were measured in shark tissues. For OCPs, six dichlorodiphenyltrichloroethanes (DDTs; o,p′-DDE, p,p′-DDE, o,p′-DDD, p,p′-DDD, o,p

Table 1 Detailed information on the 13 shark species collected from offshore (Indian and Pacific Oceans) and coastal waters of Korea. Species (Scientific name)

na

Body length (cm)

Body weight (kg)

Lipid (%)

Habitatb

Feeding habit (Major prey)b,c

Blacktip reef shark (Carcharhinus melanopterus)

26 Pacific Ocean

90 716

217 11

4.2 7 1.3

17 Pacific Ocean

(63‒115) 81 78.2

(7.0‒42) 2.7 70.9

(1.6‒6.2) 187 3.6

Aggressive carnivore (cephalopods, crustaceans, bony fishes, and marine birds) Carnivore (squid, shrimp, crustaceans, fishes, and polychaetes)

(62‒93)

(1.5‒4.5)

(12‒23)

22 7 8.2 (12‒36) 40 7 29

3.5 7 1.5 (1.4‒5.2) 4.4 7 2.1

Coastal, continental shelf pelagic (20‒75 m) Coastal, continental slope lower bathyal (50‒ 150 m) Bathyal (150‒350 m)

Spiny dogfish (Squalus acanthias)

Sampling location

Blue shark (Prionace glauca)

15 Pacific Ocean

Pelagic thresher shark (Alopias pelagicus)

13 Pacific Ocean

112 720 (70‒144) 96 727

7 Pacific Ocean

(53‒143) 1187 9.8

(7.5‒108) 447 26

(1.4‒9.0) 4.3 7 1.4

Indian Ocean 5 Korean coast

(106‒133) 337 2.9

(19‒96) 0.8 71.0

(2.1‒5.9) 4.8 7 3.4

Oceanic whitetip shark (Carcharhinus longimanus)

4 Pacific Ocean

(30‒35) 85 725 (60‒119)

(0.2‒2.0) 177 16 (5.1‒40)

(1.7‒9.7) 4.17 1.4 (2.2‒5.4)

Shortnose spurdog (Squalus megalops) Milk shark (Rhizoprionodon acutus) Smooth hammerhead (Sphyrna zygaena)

4 Korean coast

87 72.9 (85‒91) 1087 9.6 (100‒120) 1057 17

4.2 70.7 (3.5‒5.1) 9.6 70.7 (9.0‒11) 177 12

3.4 7 2.1 (1.7‒6.2) 3.7 7 2.1 (1.7‒6.1) 4.5 7 0.3

(87‒120) 1117 40

(6.2‒30) 5.7 73.2

(4.2‒4.8) 4.6 7 1.0

(70‒150) 767 0.7 (75‒76) 60

(2.0‒8.0) 1.6 7 0.4 (1.3‒1.8) 1.6 7 0.8

(3.6‒5.6) 4.4 7 0.8 (3.9‒5.0) 6.0 7 1.0

(1.0‒2.2)

(5.3‒6.8)

Shortfin mako (Isurus oxyrinchus)

Cloudy dogfish (Scyliorhinu torazame)

4 Korean coast 3 Pacific Ocean Korean coast

Banded houndshark (Triakis scyllium)

3 Pacific Ocean

Crocodile shark (Pseudocarcharias kamoharai) Starspotted smooth-hound (Mustelus manazo)

2 Indian Ocean

a b c

Sample number analyzed. Parker, 2008. Stillwell and Kohler, 1982.

2 Korean coast

Upper bathyal ( 4150 m)

Aggressive carnivore (sardine, squid, marine birds, and marine mammals) Carnivore (squid and pelagic small fishes)

Coastal, bathyal ( 4500 m)

Aggressive carnivore (bony fishes, marine birds, marine mammal, and sharks)

Coastal, continental shelf, bathyal

Carnivore (squid, crustaceans, and small fishes)

Coastal, continental shelf ( 4150 m) Continental shelf, bathyal ( 450‒750 m) Continental shelf, bathyal (200 m) Continental shelf ( 4280 m)

Aggressive carnivore (pelagic cephalopods, bony fishes, marine birds, and marine mammals) Carnivore (squid, shrimp, crustaceans, and small fishes) Carnivore (squid, crustaceans, and fishes) Aggressive carnivore (squid, crustaceans, bony fishes, rays, and sharks)

Coastal, sandy, muddy water

Carnivore (squid, crustaceans, bony fishes, and benthic invertebrates)

Bathyal ( 4300 m)

Carnivore (squid, shrimp, and pelagic bony fishes) Carnivore (squid, shrimp, crustacean, shellfish, and small fishes)

Coastal, sandy, muddy waters (200‒360 m)

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′-DDT, and p,p′-DDT), three hexachlorocyclohexanes (HCHs; α-, βand γ-HCHs), five chlordanes (CHLs; cis-CHL, oxy-CHL, trans-CHL, trans-nonaCHL, and cis-nonaCHL), heptachlor, and hexachlorobenzene (HCB) were also analyzed in our study. Detailed experimental procedures to determine concentrations of OCs in the shark tissue have been described previously (Moon et al., 2009, 2010). In brief, approximately 2‒6 g of muscle tissues was homogenized with anhydrous Na2SO4 (Pesticide analysis grade, Wako Pure Chemicals, Tokyo, Japan) and extracted in a Soxhlet apparatus using 400 mL of 75% dichloromethane (DCM; ultra residue analysis, J.T. Baker, Phillipsburg, NJ, USA) in hexane (Ultra residue analysis, J.T. Baker) for 16 h. Before extraction, 100 ng of PCBs 103, 198, and 209 (AccuStandard, New Haven, CT, USA) were spiked as surrogate standards. The extract was concentrated to 11 mL and an aliquot (1 mL) was taken for gravimetric determination of lipid content. The remaining extract (10 mL) was subjected to gel permeation chromatography (GPC) using S-X3 Bio-beads (Bio-Rad Laboratories, Hercules, CA, USA) and a cartridge packed with 0.5 g of silica gel (neutral, 70‒230 mesh, GL Sciences, Tokyo, Japan) for removal of lipids. Before the clean-up procedure, the extract was spiked with mass-labeled PCBs (13C-PCBs, 10 ng; CBs 28, 52, 153, 180 and 209; EC9605-SS, Wellington Laboratories, Guelph, ON, Canada). Extracts were cleaned by passage through a multi-layer silica gel column with 150 mL of 15% DCM in hexane. Eluted fractions were concentrated, and were dissolved in 100 mL of nonane (Pesticide grade analysis, SigmaAldrich, St. Louis, MO, USA) for instrumental analysis.

197

isotope ratios of the sample and conventional standards (i.e., atmospheric air for nitrogen). Calibration was conducted using international standards as reference materials (IAEA-N1). 2.5. Calculation of daily intake of OCs The daily intake of OCs associated with shark consumption was calculated by multiplying the OC concentrations (ng/g fw) in sharks by the consumption rate of seafood (g/day) for the general population and for males and females separately. Data on seafood consumption and body weight were obtained from the Korean Exposure Factor Handbook (KEFH). The respective consumption rate of seafood and body weight used in this study were 89.4 g/day and 57.0 kg for males, and 70.5 g/day and 51.6 kg for females (KEFH, 2007). To estimate the human health risk due to consumption of sharks in Korea, the daily intake was compared with the benchmark concentration (BMC) for each OC compounds. The BMCs for carcinogenic effects were calculated with cancer slope factors of individual contaminants obtained from the Integrated Risk Information System (IRIS) with a cancer risk of 1:1,000,000 for lifetime exposure (US EPA, 2008). The BMCs for non-carcinogenic effects were based on the oral reference dose (RfD) from the IRIS. A hazard ratio (HR) of greater than one suggests a potential health risk. Detailed descriptions of BMCs and hazard ratios (HRs) are provided elsewhere (Moon et al., 2009). 2.6. Statistical analyses

2.3. Instrumental analysis and quality control Detailed descriptions of instrumental analyses of OCs have been reported elsewhere (Moon et al., 2009, 2010). OCs were analyzed using a gas chromatograph (Agilent 7890, Wilmington, DE, USA) coupled to a mass spectrometer (Agilent 5975C). The mass spectrometer (MS) was operated under positive electron impact (EI þ) and ions were monitored using selected ion monitoring (SIM) mode for OC analysis. A DB5-MS capillary column (30 m length, 0.25 mm inner diameter, 0.25 μm film thickness; J&W Scientific, Palo Alto, CA, USA) was used to separate individual OC compounds. Quantification of OCs was performed by the external standard method. Procedural blanks (n¼ 10) were processed for every set of 10 samples in the same manner as samples. Solvents injected before and after the injection of standards showed negligible carryover during instrumental analysis. The limit of quantification (LOQ) was calculated as 10 times the signal-to-noise ratio, which ranged from 0.003 to 0.006 ng/g fresh weight (fw) for PCBs and from 0.003 to 0.196 ng/g fw for OCPs. Recoveries of CBs 103, 198, and 209, spiked as surrogates, were 827 11% (average7standard deviation), 78 711%, and 85 714%, respectively. The recoveries of 13C-CBs 28, 52, 153, 180 and 209 were 72 727%, 103 721%, 89 719%, 897 19%, and 87720%, respectively. The concentrations of PCBs and OCPs reported in our study were not corrected for recoveries. 2.4. Stable isotope analysis Nitrogen stable isotope (δ15N) in shark samples was analyzed to identify their potential trophic position. Detailed descriptions of δ15N determination have been provided previously (Park et al., 2011). In brief, shark tissue was treated with 1 N HCl to remove carbonates and lipids, and then rinsed with distilled water. After drying, δ15N in homogenized samples was measured using a continuous flow isotope ratio mass spectrometer (CF-IRMS; Isoprime, GV Instruments, Manchester, UK) connected to an elemental analyzer (Eurovector 3000 Series, Milan, Italy). Data were expressed as delta (δ) notation of the relative difference between

Individual PCB (CBs 101, 118, 138, 153 and 180) and OCP (p, p′ -DDE, trans-nonaCHL) compounds detected in 450% of the samples were subjected to statistical analyses. Concentrations below the LOQ were treated as half the LOQ for each compound. Total concentrations of PCBs (ΣPCB; sum of 22 PCB congeners) and OCPs (ΣOCP; sum of 16 OCP compounds) were also used in statistical analyses. To calculate ΣPCB and ΣOCP, non-detected congeners/ compounds were treated as zero to avoid biased estimators and incorrect statistical analysis due to a low detection frequency. OC concentrations were log-transformed for all statistical analyses. Student's t-test was performed to investigate the significance of differences in the concentrations of OCs among shark species. Spearman's rank correlation analysis was performed to investigate the strength of relationships between the concentrations of OCs and biological attributes of the sharks. Statistical significance was set at po 0.05. All statistical analyses were performed using SPSS 18.0 for Windows (SPSS Inc., Chicago, IL, USA).

3. Results and discussion 3.1. Concentrations of OCs in sharks The concentrations of OCs in 13 shark species from offshore (Indian and Pacific Oceans) and coastal waters of Korea are summarized in Table 2. The detection rates of PCBs, DDTs, CHLs, HCB, and heptachlor for all shark species were 88%, 86%, 48%, 44%, and 8.6%, respectively. HCHs were not detected in any sharks. The concentrations of ΣPCB, ΣDDT, ΣCHL, HCB, and heptachlor ranged from oLOQ to 184 (mean: 34.1) ng/g lipid weight (lw), o LOQ to 1135 (58.9) ng/g lw, o LOQ to 62.5 (4.37) ng/g lw, oLOQ to 18.6 (1.48) ng/g lw, and oLOQ to 151 (5.60) ng/g lw, respectively. The major OC groups were PCBs and DDTs, because these contaminants are more persistent and lipophilic than the other OC groups (Zhou et al., 2013). Similar bioaccumulation patterns of OCs have been reported for fishes and marine mammals from Korean coastal waters (Moon et al., 2009, 2010; Park et al., 2010).

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Table 2 Concentrations of OCs (ng/g lipid weight) in 13 shark species from offshore (Indian and Pacific Oceans) and Korean coastal waters. Species

na

ΣPCB Mean 7 SD

ΣDDT Mean 7 SD

Range

Blacktip reef shark Spiny dogfish Blue shark

26 46.0 7 35.5 17 20.17 17.8 15 45.7 7 39.1

o LOQ‒184 87.17 165 o LOQ‒49.2 67.6 7 134 o LOQ‒125 88.5 7 290

Pelagic thresher shark Shortfin mako Cloudy dogfish Oceanic whitetip shark Shortnose spurdog Milk shark Smooth hammerhead Banded houndshark Crocodile shark Starspotted smoothhound

13 7 5 4 4 4 3 3 2 2

4.97‒76.6 o LOQ‒127 o LOQ‒63.9 o LOQ‒81.4 o LOQ‒45.2 o LOQ‒54.4 5.99‒33.5 o LOQ‒40.4 27.2‒67.5 6.84‒25.3

a

33.37 21.3 29.4 7 44.7 23.4 7 24.4 32.7 7 34.7 27.8 7 19.9 24.27 23.0 20.3 7 13.8 26.2 7 22.7 47.3 7 28.5 16.17 13.1

ΣCHL

10.4 7 9.23 1077 273 6.497 8.61 0.63 7 1.25 24.77 30.7 1.90 7 0.20 8.38 7 12.8 10.7 7 13.1 1817 238 1.59 7 2.25

HCB

Heptachlor

Range

Mean 7 SD

Range

Mean 7 SD

oLOQ‒788 oLOQ‒502 oLOQ‒ 1135 oLOQ‒26.3 oLOQ‒726 oLOQ‒21.5 oLOQ‒2.51 oLOQ‒66.2 1.66‒2.10 0.57‒23.2 oLOQ‒25.3 12.5‒349 oLOQ‒3.18

7.91 7 12.8 4.02 7 6.37 3.54 7 9.07

o LOQ‒39.7 2.32 7 3.46 o LOQ‒18.9 1.677 2.72 o LOQ‒34.3 1.76 74.91

0.30 7 0.43 o LOQ‒1.27 9.09 7 23.5 o LOQ‒62.5 0.46 7 0.81 o LOQ‒1.86 o LOQ o LOQ 2.357 3.96 o LOQ‒8.23 o LOQ o LOQ 0.36 7 0.62 o LOQ‒1.07 1.977 3.42 o LOQ‒5.92 22.4 7 30.5 0.77‒44.1 0.27 70.38 o LOQ‒0.54

Range

Mean 7SD

Range

oLOQ‒11.3 oLOQ‒7.32 oLOQ‒18.6

o LOQ o LOQ o LOQ

o LOQ o LOQ o LOQ

0.79 72.86 o LOQ 37.9 7 51.7 43.7 7 72.5 o LOQ o LOQ 25.0 743.3 4.177 7.23 o LOQ 62.7 788.7

o LOQ‒10.3 o LOQ o LOQ‒117 o LOQ‒151 o LOQ o LOQ o LOQ‒74.9 o LOQ‒12.5 o LOQ o LOQ‒125

0.157 0.33 oLOQ‒1.15 2.39 7 6.19 oLOQ‒16.4 0.177 0.26 oLOQ‒0.60 o LOQ oLOQ 1.447 2.19 oLOQ‒4.62 0.05 7 0.11 oLOQ‒0.22 0.36 7 0.47 oLOQ‒0.90 1.16 72.01 oLOQ‒3.49 4.88 7 6.69 0.15‒9.61 o LOQ oLOQ

Sample number analyzed.

Overall OC concentrations were highly variable not only among species, but also within the same species of sharks. In particular, the variability in the concentrations of OCPs such as DDTs, CHLs, and HCB was higher than that of PCBs among shark species. Shortfin mako (Isurus oxyrinchus) from the Indian Ocean had the highest concentrations of ΣPCB (127 ng/g lw) and ΣDDT (726 ng/g lw). Crocodile shark (Pseudocarcharias kamoharai) from the Indian Ocean also had concentrations of ΣDDT (mean: 181 ng/g lw), ΣCHL (22.4 ng/g lw), and HCB (4.88 ng/g lw), which were one or two orders of magnitude higher than those found in other shark species. Indian Ocean surrounds India and Africa. Previous studies reported the widespread usage of OCPs, including DDTs, in India and South Africa for agricultural and sanitary purposes until recent years (Sadasivaiah et al., 2007; Dash et al., 2008). This result

suggests that the accumulation of OCPs in sharks could be due to regional consumption of OCPs. Among the 13 shark species, aggressive sharks such as the blacktip reef shark (Carcharhinus melanopterus), blue shark (Prionace glauca), and shortfin mako (I. oxyrinchus) had significantly (p o0.05) higher concentrations of ΣPCB (mean: 43.5 ng/g lw) and ΣDDT (90.4 ng/g lw) than measured in non-aggressive shark species (ΣPCB, 26.1 ng/g lw and ΣDDT, 36.4 ng/g lw). This is likely related to be related to the feeding habits of the sharks. Predatory bony fishes are major prey of aggressive sharks, and these fishes contain high levels of persistent OCs (De Brito et al., 2002; Moon et al., 2009). Our findings indicate the importance of prey as a major exposure pathway of sharks to OCs. We compared the concentrations of PCBs and DDTs in various

Table 3 Global comparison of mean concentrations of PCBs and DDTs (ng/g lipid weight) in sharks measured in the present study with those reported for sharks in previous studies. Species

Sampling locations

Greenland shark (Sominiosus microcephalus) Greenland shark (Sominiosus microcephalus) Bull shark (Carcharhinus leucas) Bull shark (Carcharhinus leucas) Atlantic sharpnose shark (Rhizoprionodon terraenovae) Spiny dogfish (Squalus acanthias) Gulper shark (Centrophorus granulosus) Longnose spurdog (Squalus blainville) Various sharks Dog shark (Mustelus griseus) Bamboo shark (Hemiscylliidae) Leopard shark (Triakis semifasciata) Shortfin mako (Isurus oxyrinchus) Blacktip reef shark (Carcharhinus melanopterus) Spiny dogfish (Squalus acanthias) Blue shark (Prionace glauca) Pelagic thresher shark (Alopias pelagicus) Oceanic whitetip shark (Carcharhinus longimanus) Smooth hammerhead (Sphyrna zygaena) Smooth hammerhead (Sphyrna zygaena) Cloudy dogfish (Scyliorhinu torazame) Shortnose spurdog (Squalus megalops) Milk shark (Rhizoprionodon acutus) Banded houndshark (Triakis scyllium) Starspotted smooth-hound (Mustelus manazo) Crocodile shark (Pseudocarcharias kamoharai) Shortfin mako (Isurus oxyrinchus)

Atlantic Atlantic Atlantic Atlantic Atlantic

a b

Ocean Ocean Ocean Ocean Ocean

(Greenland) (Greenland) (Florida) (Florida) (Florida)

na 10 3 5 25 20

Sampling year PCBs 2001‒2005 2010 2002‒2004 1993‒1994 2004

Atlantic Ocean (Florida) 609 2004 Mediterranean Sea 7 1999 Mediterranean Sea 6 1999 Mediterranean Sea 5 1999 Pacific Ocean (China) 10 2011 Pacific Ocean (Hong Kong) 10 2003‒2004 Pacific Ocean (San Francisco) 8 1997 Pacific Ocean 6 2010 Pacific Ocean 26 2010 Pacific Ocean 17 2010 Pacific Ocean 15 2010 Pacific Ocean 13 2010 Pacific Ocean 4 2010 Pacific Ocean 2 2010 Pacific Ocean (Korean Coast) 1 2010 Pacific Ocean (Korean Coast) 5 2010 Pacific Ocean (Korean Coast) 4 2010 Pacific Ocean (Korean Coast) 4 2010 Pacific Ocean (Korean Coast) 3 2010 Pacific Ocean (Korean Coast) 2 2010 Indian Ocean 2 2010 Indian Ocean 1 2010

Sample number analyzed. Values in parentheses are concentrations based on ng/g fresh weight.

4100 (57800)b 71200 6440 5520 790 (28.3) (10.8) (6.63)

DDTs

(594)

(49.3) (16.8) (4.43) (16.5) (2.10) (2.45) (11.0) (5.30) 13.2 (0.69) 3.39 (0.16) 46.0 (1.63) 87.1 (2.74) 20.1 (3.70) 67.6 (14.0) 45.7 (1.25) 88.5 (3.56) 33.3 (1.18) 10.4 (0.37) 32.7 (1.65) 0.63 (0.01) 27.4 (1.21) 11.9 (0.54) 5.99 (0.29) 1.37 (0.07) 23.4 (1.27) 6.49 (0.21) 27.8 (1.13) 24.7 (0.79) 24.2 (0.61) 1.90 (0.07) 26.2 (1.20) 10.7 (0.43) 16.1 (0.90) 1.59 (0.08) 47.3 (2.21) 181 (8.95) 127 (2.69) 726 (15.4)

Reference Strid et al. (2007) Corsolini et al. (2014) Johnson-Restrepo et al. (2005) Johnson-Restrepo et al. (2005) Johnson-Restrepo et al. (2005) Johnson-Restrepo et al. (2005) Storelli and Marcotrigiano (2001) Storelli and Marcotrigiano (2001) Marcotrigiano and Storelli (2003) Zhou et al. (2013) Cornish et al. (2007) Davis et al. (2002) This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study

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shark species measured in the present study to those reported for sharks in other studies (Table 3). The overall concentrations of ΣPCB (mean: 34.1 ng/g lw; 1.70 ng/g ww) and ΣDDT (58.9 ng/g lw; 3.90 ng/g ww) in sharks in our study were similar to those measured in bamboo shark (Hemiscylliidae) and leopard shark (Triakis semifasciata) collected from the Pacific Ocean (Davis et al., 2002; Cornish et al., 2007). Concentrations of PCBs and DDTs in sharks from the Mediterranean Sea were 5–10 times higher than those measured in our study (Storelli and Marcotrigiano, 2001; Marcotrigiano and Storelli, 2003). Certain shark species from the Atlantic Ocean had the highest concentrations of PCBs and DDTs reported in sharks in previous studies (Johnson-Restrepo et al., 2005; Strid et al., 2007; Corsolini et al., 2014). In particular, the concentrations of PCBs and DDTs in Greenland shark (Somniosus microcephalus) and bull shark (Carcharhinus leucas) from the Atlantic Ocean were two to five orders of magnitude higher than those measured in our study (Strid et al., 2007; Corsolini et al., 2014). Elfes et al. (2010) reported that the concentrations of POPs in humpback whale (Megaptera novaeangliae) collected from the North Atlantic Ocean were significantly higher than those measured from whales caught in the North Pacific Ocean. Our global comparison confirmed that accumulation of OCs in sharks is dependent on ocean location e.g. Atlantic, Mediterranean, Pacific, and Indian Oceans. The relatively lower levels of OCs in sharks in our study may reflect a reduction in the POP levels in the aquatic environment and/or different sampling times compared with previous studies. 3.2. Accumulation features of OCs in sharks The accumulation profiles of PCBs and OCPs in individual shark species are presented in Figs. 1 and 2. Accumulation profiles of PCBs and OCPs differed among the various shark species, suggesting species-specific accumulation of these contaminants.

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Although shark species had different accumulation features of OCs, the predominant OC compounds were similar to those reported for predatory fishes and marine mammals from Korean coastal waters (Moon et al., 2009, 2010; Park et al., 2010). The predominant congener of PCBs was CB 153, which accounted for 41 728% of ΣPCB concentrations in most of shark species. However, the ΣPCB concentration in species such as the blacktip reef shark (C. melanopterus), milk shark (Rhizoprionodon acutus), smooth hammerhead (Sphyrna zygaena), and banded houndshark (Triakis scyllium) collected from Pacific Ocean was dominated by CB 180 (34 717%), implying species-specific differences in metabolic capacities for PCB congeners. The predominant OCP compound in most sharks was p,p’′-DDE, which accounted for 76 729% of the ΣOCP concentrations. However, heptachlor was the dominant OCP (mean: 65%) in some shark species such as the smooth hammerhead (S. zygaena), oceanic whitetip shark (Carcharhinus longimanus), cloudy dogfish (Scyliorhinu torazame), and starspotted smooth-hound (Mustelus manazo). DDTs are abiotically and biotically degraded to metabolites such as DDD or DDE (De La Cal et al., 2008). Thus, the proportion of DDT relative to DDE has been used for technical formulation of DDTs (e.g. dicofol) (Guo et al., 2012). In our study, DDT was not detected or contributed very little (o10%) to ΣOCP concentrations. However, in shortfin mako (I. oxyrinchus) and crocodile shark (P. kamoharai) collected from the Indian Ocean, DDT accounted for 4 20% of the ΣOCP concentrations. This result confirms that sharks inhabiting the Indian Ocean are being contaminated by technical formulations of DDTs from surrounding countries such as India and South Africa (Sadasivaiah et al., 2007; Dash et al., 2008). In our study, the same species collected from different sampling locations showed different accumulation profiles of OCs e.g. shortfin mako (Pacific vs. Indian Ocean; Figs. 1 and 2(e)) and

a

b

c

d

e

f

g

h

i

j

k

l

m

Fig. 1. Accumulation profiles of PCBs in 13 shark species. Data were normalized to the total concentrations of PCBs. Vertical lines represent standard deviations: (a) blacktip reef shark, (b) spiny shark, (c) blue shark, (d) pelagic thresher shark, (e) shortfin mako, (f) cloudy dogfish, (g) oceanic whitetip shark, (h) shortnose spurdog, (i) milk shark, (j) smooth hammerhead, (k) banded houndshark, (l) crocodile shark, and (m) starspotted smooth-hound.

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a

b

c

d

e

f

g

h

i

j

k

l

m

Fig. 2. Accumulation profiles of OCPs in 13 shark species. Data were normalized to the total concentrations of OCPs. Vertical lines represent standard deviations: (a) blacktip reef shark, (b) spiny shark, (c) blue shark, (d) pelagic thresher shark, (e) shortfin mako, (f) cloudy dogfish, (g) oceanic whitetip shark, (h) shortnose spurdog, (i) milk shark, (j) smooth hammerhead, (k) banded houndshark, (l) crocodile shark, and (m) starspotted smooth-hound.

smooth hammerhead (Pacific Ocean vs. Korean Coast; Figs. 1 and 2 (j)). These intra-species differences in the accumulation of OCs are likely due to local contamination differences in seawater zones. Lu et al. (2014) reported significant differences in chiral PCB congeners in Greenland shark (S. microcephalus) sampled from different locations. 3.3. Correlations between OC levels and biological factors Several studies have reported that accumulation of OCs in sharks is associated with contributing factors such as prey, habitat, trophic position, lipid content, sex, body length/weight, and metabolism (Strid et al., 2007; Van Ael et al., 2013). In this study, there were no significant correlations between OC levels and lipid content when all shark species were considered, nor were there correlations within each species. However, a significant correlation (r ¼0.503, p¼ 0.04) between lipid and ΣOCP was observed in spiny dogfish (Squalus acanthias) due to the wide range of lipid contents (12–23%) in this species compared to other species (1.4–9.7%). No significant correlations were found between OC levels and body length/weight when all shark species were considered or within each species, except for the blue shark. This is consistent with previous studies that reported no relationship between OC levels and body length in Greenland shark (S. microcephalus) or bonnethead shark (Sphyrna tiburo) (Fisk et al., 2002; Gelsleichter et al., 2005). In the case of the blue shark, body length and weight showed significant negative correlations for ΣPCB (r¼  0.795, p ¼0.001 for length and r ¼  0.781, p ¼0.001 for weight) and ΣDDT (r ¼  0.687, p ¼0.005 for length and r ¼  0.765, p¼ 0.001 for weight), reflecting bio-dilution of OCs with growth. Blue shark is one of the fastest-growing shark species (Parker, 2008; Stillwell

and Kohler, 1982). Although the blue shark had relatively higher concentrations of OCs than those measured in other sharks, the accumulation velocities of OCs for faster-growing species could be slower than those for slower-growing species. Our results imply that growth velocity could be a determinant of OC accumulation in sharks. In contrast, significant positive correlations (r ¼0.62–0.73, po 0.01) have been found between the OC levels and body length in marine mammals such as minke whales (Balaenoptera acutorostrata) and finless porpoises (Neophocaena phocaenoides) from Korean coastal waters (Moon et al., 2010; Park et al., 2010). This could be due to the differences in bioaccumulation behavior and metabolism of OCs between sharks and mammals. Limited information is available about the correlation between OC levels and nitrogen stable isotope (δ15N) values in sharks (Webster et al., 2014). The δ15N values of the 13 shark species investigated in this study ranged from 12.1% to 14.8% (mean: 13.3%), except for spiny dogfish (10.0%). In other studies, top predator fish such as Atlantic bluefin tuna (Thunnus thynnus) and white shark (Carcharodon carcharias) had δ15N values of 14.0% and 15.8%, respectively (Estrada et al., 2005; Jaime-Rivera et al., 2013), similar to levels measured in our study. δ15N values were significantly correlated with the concentrations of ΣPCB, CBs 101, 118, 138, and 180 (r ¼0.197‒0.283, po0.05), whereas δ15N values were not significantly correlated with the concentrations of OCPs, except for HCB (r ¼0.256, p ¼0.009). Our results indicate that trophic position (expressed as 15δN) could be one of the determinants governing the bioaccumulation of PCBs in sharks. 3.4. Exposure assessment of OCs via shark consumption Daily intake of OCs for the general population, males, and

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a

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of OCs and traditional consumption of shark meat in Korea, a comprehensive risk assessment of shark consumption should be performed taking into account the presence of other contaminants and sensitive populations such as pregnant woman.

4. Conclusions

b

The present study provides valuable information concerning the concentrations and accumulation features of OCs in various shark species. Wide ranges of OC concentrations were found in the muscle of various shark tissues. The determined concentrations of PCBs and DDTs in sharks in our study were relatively lower than those reported by other studies. Inter-species differences in the concentrations and accumulation profiles of OCs are likely due to differences in feeding habits and sampling locations. Growth velocity, trophic position, and regional contamination status are confounding factors associated with bioaccumulation of OCs in sharks. Hazard ratios of non-cancer risk of all OCs were below one, whereas the hazard ratios of lifetime cancer risks of PCBs and DDTs exceeded one, implying that consumption of shark by the general population of Korea has potential carcinogenic effects.

Acknowledgment This work was supported by the research fund of Hanyang University (HY-2012-000-0000-1399), Korea.

References

Fig. 3. Hazard ratios of (a) non-cancer and (b) cancer risk assessments for estimated daily intake of OCs due to shark consumption by the general population of Korea.

females in Korea was estimated to be 2.50, 2.67, 2.33 ng/kg body weight/day for ΣPCB, 5.73, 6.11, 5.32 ng/kg body weight/day for ΣDDT, 0.40, 0.43, 0.37 ng/kg body weight/day for ΣCHL, and 0.15, 0.16, 0.14 ng/kg body weight/day for HCB, respectively. The estimated daily intake (EDI) of OCs for males was higher than that determined in females, due to greater consumption of seafood by males (89.4 g/day) than females (70.5 g/day). This is consistent with our previous studies (Moon et al., 2009; Lee et al., 2013). The hazard ratios (HR) for non-cancer and cancer risk of OCs due to shark consumption by the general population of Korea are presented in Fig. 3. HRs of non-cancer risk for the general population were less than one for PCBs, DDTs, CHLs, and HCB, indicating that exposure to OCs via shark consumption has no adverse health effects in the Korean populations. Lifetime cancer risk assessment revealed that the HRs for PCBs ingested via shark consumption were greater than one for all shark species. For DDTs, consumption of five sharks, namely blacktip reef shark (C. melanopterus), spiny dogfish (S. acanthias), blue shark (P. glauca), shortfin mako (I. oxyrinchus), and crocodile shark (P. kamoharai) was associated with a HR of 1 in carcinogenic risk assessment, suggesting that consumption of these species should be restricted. HRs of CHLs and HCB were below one for consumption of all shark species, except spiny dogfish (S. acanthias) for HCB. Our results indicate that exposure to PCBs and DDTs due to shark consumption could have carcinogenic effects in the Korean population. Shark consumption also poses a potential health risk to humans due to high levels of other contaminants, such as methyl mercury. Based on adverse health risks, the US EPA and Health Canada recommend restricting consumption of sharks. Given the toxicological effects

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