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Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea
MPB-07331; No of Pages 6 Marine Pollution Bulletin xxx (2015) xxx–xxx
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Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea Sang-Jo Kim a, Hyun-Kyung Lee b, Abimbola C. Badejo b, Won-Chan Lee c, Hyo-Bang Moon b,⁎ a b c
National Fishery Products Quality Management Service (FiQ), Busan 606-705, Republic of Korea Department of Marine Sciences and Convergent Technology, College of Science and Technology, Hanyang University, Ansan 426-791, Republic of Korea Marine Environment Research Division, National Fisheries Research and Development Institute (NFRDI), Busan 619-705, Republic of Korea
a r t i c l e
i n f o
Article history: Received 16 September 2015 Received in revised form 9 November 2015 Accepted 16 November 2015 Available online xxxx Keywords: Mercury Methyl mercury Shark Feeding habit Trophic position Safety limit
a b s t r a c t Limited information is available on mercury (Hg) levels in various shark species consumed in Korea. The methylHg (Me-Hg) and total Hg concentrations in all shark species ranged from 0.08 to 4.5 (mean: 1.2) mg/kg wet weight and from 0.1 to 7.0 (mean: 1.4) mg/kg wet weight, respectively. Inter-species differences in Hg accumulation were found among the species; however, Hg accumulation was homogenous between dorsal and pectoral fins within species. The highest Hg levels were found in aggressive carnivore shark species. Trophic position was important in determining Hg accumulation for aggressive carnivore sharks. Approximately 80% of shark species exceeded the safety limits for Me-Hg established by domestic and international authorities. The mean estimated daily intake of Me-Hg (1.3 μg/kg body weight/day) for Korean populations consuming various sharks was higher than the guidelines proposed by international regulatory authorities, suggesting that excessive shark fin consumption may pose potential health risks for Koreans. © 2015 Published by Elsevier Ltd.
Mercury (Hg) is a global pollutant released into the atmosphere by a variety of anthropogenic activities such as industrial fossil fuel combustion and waste disposal (Pacyna et al., 2006; Swain et al., 2007). With global mercury emissions reaching an estimated 5000 to 8000 metric tons each year (UNEP, 2013), the presence of Hg in the atmosphere has become problematic as it is eventually deposited in the aquatic environments. Methyl mercury (Me-Hg), formed in sediment by microbial methylation of Hg, is extremely toxic and has raised human health concerns due to its bioaccumulation and biomagnification potential through the food web (Teffer et al., 2014; McMeans et al., 2015). Human exposure to Me-Hg is almost exclusively from consuming aquatic organisms, especially predatory fish (Moon et al., 2011; Karimi et al., 2014). Fish is a highly nutritious food with amazing human benefits, but the contamination of this important global commodity by MeHg has become a challenge to public health, as over 90% of Hg in fish is Me-Hg (Rimondi et al., 2012). Thus, Me-Hg exposure associated with consuming fish and shellfish poses health risks, such as immune deficiencies and toxicity to the central nervous system, especially in fetuses (Mergler et al., 2007; Choi et al., 2014). Sharks tend to accumulate high levels of toxic contaminants, such as persistent organic pollutants (POPs) and Hg, because they are top predators in the marine food web and have a long lifespan (Endo et al., 2008; Torres et al., 2014; Lee et al., 2015a,b). Sharks are commonly consumed ⁎ Corresponding author. E-mail address: [email protected] (H.-B. Moon).
in the form of shark fin soup, filets and liver oil in many countries such as Australia, China, Japan and Korea (Man et al., 2014; Nalluri et al., 2014). Shark liver oil is ingested as a nutritional source of omega-3 fatty acids, which lower the risk of heart disease, inflammatory disease and rheumatoid arthritis, among many other benefits (Maggie and Covington, 2004). The United States Environmental Protection Agency (US EPA) and Food and Drug Administration (US FDA) have designated sharks as high mercury-containing fishes to limit consumption by children and women of childbearing age (US EPA, 2001; US FDA, 2014). A nationwide survey of Hg in the Korean population suggested that blood Me-Hg levels are associated with fish consumption (You et al., 2012). In addition, some regions of Korea (e.g. Pohang and Daegu cities) traditionally consume shark as part of the local diets. However, Hg levels in marketed sharks and the potential health risks of Hg associated with shark consumption in Korea have not been documented. In this study, we determined Me-Hg and total mercury (T-Hg) concentrations in dorsal and pectoral fins in 13 shark species obtained offshore and in Korean coastal waters. We investigated the factors influencing Hg accumulation in various sharks. Furthermore, shark consumption limits were recommended based on the risk assessment of Me-Hg, using the reference dose (RfD) and tolerable daily intake (TDI) for Koreans. Muscle tissues from dorsal and pectoral fins were collected from 13 shark species (n = 103) found entangled in long lines of commercial fisheries or by-caught in trawl nets either offshore (Indian and Pacific Oceans) or in Korean coastal waters between July and October, 2010. All shark species surveyed in this study are globally endangered and
http://dx.doi.org/10.1016/j.marpolbul.2015.11.038 0025-326X/© 2015 Published by Elsevier Ltd.
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
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S.-J. Kim et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Table 1 Concentrations (mg/kg wet weight) of methyl (Me-Hg) and total mercury (T-Hg) in dorsal and pectoral fins from 13 shark species from offshore and Korean coastal waters. Species (scientific name)
Blacktip reef shark (Carcharhinus melanopterus) Spiny dogfish (Squlus acanthias)
na
Sampling locations
Feeding habitsb
26 Pacific Ocean Aggressive carnivore 17 Pacific Ocean Carnivore
BLc (m) (Mean
δ15Ne (‰) BWd (kg) (Mean ± SD) (Mean ±
± SD)
SD)
0.9 ±
21 ± 11
Dorsal fin
Pectoral fin
Mean ± SD (Min–Max)
%f
Mean ± SD (Min–Max)
T-Hg
12.8 ± 1.84
0.91 ± 0.63 (0.12–2.4)
1.1 ± 0.77 (0.13–3.2)
86 0.90 ± 0.67 (0.12–2.6)
1.0 ± 0.79 (0.15–3.4)
86
0.2
Me-Hg
%
Me-Hg
T-Hg
0.8 ±
2.7 ± 0.9 10.0 ± 0.92
0.80 ± 0.34 (0.36–1.7)
0.96 ± 0.38 (0.42–1.9)
84 0.98 ± 0.34 (0.39–1.6)
1.2 ± 0.41 (0.46–1.8)
82
0.1 1.1 ±
22 ± 8.2 13.8 ± 1.09
1.9 ± 0.94 (0.43–3.9)
2.3 ± 1.1 (0.55–4.8)
80 2.0 ± 1.1 (0.68–4.5)
2.5 ± 1.6 (0.88–7.0)
79
0.2 1.0 ±
40 ± 29
12.6 ± 2.38
1.3 ± 0.52 (0.24–2.1)
1.5 ± 0.51 (0.29–2.2)
86 1.4 ± 0.60 (0.20–2.7)
1.6 ± 0.66 (0.24–3.1)
84
0.3 1.2 ±
44 ± 26
14.5 ± 1.57
2.5 ± 0.31 (2.1–2.9)
3.0 ± 0.45 (2.5–3.5)
81 2.6 ± 0.57 (2.10–3.8)
3.3 ± 0.90 (2.2–5.0)
81
Carnivore
0.1 0.3
0.8 ± 1.0 12.5 ± 0.15
0.9
4.2 ± 0.7 14.4 ± 0.80
1.1 ± 0.43 (0.64–1.7) 0.53 ± 0.79 (0.12–1.7)
78 0.87 ± 0.30 (0.60–1.4) 82 0.37 ± 0.52 (0.09–1.2)
1.2 ± 0.29 (0.91–1.7) 0.53 ± 0.78 (0.13–1.7)
72
4 Pacific Ocean Carnivore
0.84 ± 0.40 (0.50–1.4) 0.41 ± 0.59 (0.08–1.3)
3 Korean coast
0.9 ±
17 ± 16
11.9 ± 1.65
0.11 ± 0.05 (0.08–0.17)
0.15 ± 0.04 (0.12–0.19)
73 0.12 ± 0.04 (0.08–0.16)
0.16 ± 0.06 (0.10–0.22)
74
0.3 1.1 ±
9.6 ± 0.7 13.6 ± 0.74
0.11 ± 0.02 (0.08–0.12)
0.16 ± 0.03 (0.14–0.19)
68 0.15 ± 0.02 (0.13–0.16)
0.21 ± 0.03 (0.17–0.24)
72
0.1 1.1 ±
17 ± 12
13.6 ± 1.90
1.4 ± 0.90 (0.42–2.2)
1.6 ± 0.90 (0.61–2.4)
83 1.4 ± 0.96 (0.33–2.0)
1.7 ± 1.0 (0.48–2.3)
81
Blue shark (Prionace glauca)
15 Pacific Ocean Aggressive carnivore
Pelagic thresher shark (Alopias pelagicus)
13 Pacific Ocean Aggressive carnivore
Shortfin mako (Isurus oxyrinchus)
7 Pacific Ocean Carnivore Indian Ocean
Cloudy dogfish (Scyliorhinus torazame) Shortnose spurdog (Carcharhinus longimanus) Oceanic whitetip shark (Squalus megalops)
5 Korean coast
Aggressive carnivore
Milk shark (Rhizoprionodon acutus)
3 Korean coast
Smooth hammerhead (Sphyrna zygaena)
3 Pacific Ocean Aggressive Korean coast carnivore
Banded hound shark (Triakis scyllium)
3 Pacific Ocean Carnivore
0.2 1.1 ±
5.7 ± 3.2 12.5 ± 1.00
0.77 ± 1.1 (0.12–2.0)
1.1 ± 1.4 (0.17–2.7)
69 0.58 ± 0.84 (0.09–1.6)
0.84 ± 1.20 (0.14–2.2)
69
Crocodile shark (Psedocarcharias kamoharai) Starspotted smooth-hound (Mustelus manazo)
2 Indian Ocean Carnivore
0.4 0.8
1.6 ± 0.4 14.8 ± 0.63
1.1 ± 0.26 (0.92–1.3)
1.5 ± 0.32 (1.3–1.7)
74 1.0 ± 0.30 (0.79–1.2)
1.4 ± 0.37 (1.1–1.6)
72
2 Korean coast
0.6
1.6 ± 0.8 13.1 ± 1.43
0.24 ± 0.07 (0.19–0.29)
0.32 ± 0.14 (0.23–0.42)
76 0.23 ± 0.06 (0.19–0.27)
0.32 ± 0.08 (0.26–0.38)
71
a b c d e f
Carnivore
75
Carnivore
n = sample number. Feeding habits were cited from Stillwell and Kohler (1982) and Parker (2008). BL = body length. BW = body weight. δ15N = delta nitrogen isotope ratio. % = ratio of methyl mercury to the total mercury.
part of the conservation inventory of the International Union for Conservation and Natural Resources (IUCN) Red List (Compagno et al., 2005). Biological information such as body length, body weight, feeding habits, and stable isotope ratios for each species are summarized in Table 1. Detailed information on habitats and major prey for each shark species were described in previous study (Lee et al., 2015a). After the sharks were dissected on commercial ships, the dorsal and pectoral fins were transported to the National Fishery Products Quality Management Service (FiQ) of Korea, and kept frozen at −20 °C until analysis. Me-Hg and T-Hg analyses have been described in detail elsewhere (Moon et al., 2011). In brief, T-Hg in the shark samples was determined using the gold amalgamation method, with a high-temperature combustion SP-3D analyzer (Nippon Instrument Co., Tokyo, Japan). Freeze-dried fins (approximately 100 mg) were placed on a layer of sodium carbonate and calcium hydroxide mixture (Additive M; Nippon Instrument Co.) in a ceramic boat. The sample was then covered with a layer of Additive M. A layer of aluminum oxide (Nippon Instrument Co.) was placed over the Additive M and then covered with another layer of Additive M. The boat was transferred into the mercury analyzer to determine T-Hg. A calibration curve with a correlation coefficient of at least 0.9 was drawn for every 20 samples. Analysis of duplicate samples yielded an average relative standard deviation (RSD) of less than 20%. To determine Me-Hg concentrations, freeze-dried muscles from fins (~2 g) were put into a 100-mL centrifuge tube, and 10 mL of 25% sodium chloride (NaCl; ultra residue analysis, Wako, Tokyo, Japan) was added. After shaking for 2 min, 15 mL of toluene (ultra residue analysis, J. T.
Baker, Phillipsburg, NJ, USA) and 4 mL of hydrochloric acid (HCl; hazardous metal analysis, Wako) were added and shaken for 2 min. The mixture was then centrifuged at 3000 rpm for 20 min, and the organic layer was put into a 125-mL separating funnel. The extract was washed with 10 mL of 25% NaCl. Five milliliters of L-cysteine solution (guaranteed reagent; Junsei, Tokyo, Japan) was added to the extract and shaken for 10 min. After standing for 10 min, the upper layer was put into a polypropylene tube; 4 mL of HCl solution (HCl: distilled water = 3:1) and 5 mL of toluene were added, and the mixture was shaken for 1 min and centrifuged at 2500 rpm for 5 min. The toluene layer was separated and dehydrated with anhydrous sodium sulfate (Na2SO4; ultra residue analysis, Merck, Darmstadt, Germany). The extracts were concentrated to 1 mL and analyzed by gas chromatography/electron capture detection (GC/ECD) (GC 6890 N; Agilent, Wilmington, DE, USA). The capillary column used was an Ulbon HR-Thermon Hg column (15m length, 0.53-mm inner diameter; Shimadzu, Kyoto, Japan). The inlet and detector temperatures were maintained at 170 °C. The carrier gas was nitrogen (N2) at a constant flow of 16 mL/min, and the makeup gas was N2 at 60 mL/min. The oven temperature was maintained at 160 °C for 10 min. To assess the quality of the analytical procedures and instrumental conditions for T-Hg, we analyzed standard mussel (Mytilus edulis) reference materials (ERM-CE278; IRMM, Geel, Belgium). The T-Hg values (n = 7) ranged from 80 to110% with a mean of 95% for the certified values. Matrix spike samples (100 ng of Me-Hg) were processed to assess the quality of Me-Hg determination. The Me-Hg recoveries ranged from 98 to 106% with a mean of 103%. The limits
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
S.-J. Kim et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
of detections (LODs) were designated as the lowest acceptable standards in the calibration curve for each chemical and were 5 ng/g for Me-Hg and 3 ng/g for T-Hg. The nitrogen stable isotope ratio (δ15N) in muscles from dorsal fins of the 13 shark species was analyzed to identify trophic position. The δ15N analysis method has been described in detail elsewhere (Park et al., 2011). In brief, wet samples were treated with 1 N HCl to remove carbonates, and rinsed with distilled water. Once dry, the samples were homogenized and weighed in a tin capsule. The samples were put into a CHN elemental analyzer (Euro Vector 3000 series, Milan, Italy) combined with a continuous-flow isotope ratio-mass spectrometer (IsoPrime, GV Instruments, UK) for oxidization at high temperature (1030 °C). δ15N was measured on 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 isotope ratios of the sample and conventional standards (i.e., atmospheric air for nitrogen), according to the following equation: δX (‰) = [(Rsample/Rstandard) − 1] × 103, where X is 15N and R is the 15N/14N ratio. Calibration was conducted using international standards as reference materials (IAEA-N1 for nitrogen). Daily intakes of Me-Hg and T-Hg were calculated by multiplying the seafood consumption rate (g/day) with the corresponding Hg concentrations (mg/kg). Average daily seafood consumption rates and body weight for general populations and sex groups in Korea were obtained from Korean Exposure Factor Handbook (KEFH). The seafood consumption rates used in this study were 79.6 g/day for the general population, 89.4 g/day for men and 70.6 g/day for women. The body weights were 54.1 kg for the general population, 57.0 g/day for men and 51.6 g/day for women (Jang et al., 2014). Kolmogorov–Smirnov and Shapiro–Wilk tests were performed to assess the normality of the Me-Hg and T-Hg concentrations. Me-Hg and T-Hg concentrations were not normally distributed in sharks, MeHg and T-Hg concentrations were log-transformed for all statistical analyses. Student's t-test was conducted to investigate significant differences in Me-Hg and T-Hg concentrations among shark species and feeding habits. Spearman's rank correlation analysis was performed to investigate the strength of relationships between Hg concentrations and factors contributing to accumulation in sharks. Statistical significance was set at p b 0.05. All statistical analyses were performed using SPSS 18.0 K for Windows (SPSS Inc., Chicago, IL, USA). Me-Hg and T-Hg concentrations in the dorsal and pectoral fins from 13 shark species found offshore and in Korean coastal waters are summarized in Table 1. The overall Me-Hg and T-Hg concentrations were highly variable among shark species. The Me-Hg and T-Hg concentrations in pectoral fins ranged from 0.08 to 4.5 (mean: 1.2) mg/kg wet weight (ww) and from 0.1 to 7.0 (mean: 1.5) mg/kg ww, respectively, for all samples. The Me-Hg and T-Hg concentrations in dorsal fins ranged from 0.08 to 3.9 (mean: 1.1) mg/kg ww and from 0.12 to 4.8 (mean: 1.4) mg/kg ww, respectively, for all samples. The T-Hg concentrations in various sharks in our study (0.1–7.0 mg/kg; mean 1.2 mg/kg ww) were similar to those measured in tiger sharks (Galeocerdo cuvier) from the Japanese coast (0.38–3.7 mg/kg ww; mean 0.78 mg/kg ww, Endo et al., 2008), common thresher shark (Alopias vulpinus) from the California coast (1.4 mg/kg ww, Lyons and Lowe, 2013), seven shark species from the Florida coast (0.19–4.5 mg/kg ww; mean 1.6 mg/kg ww, Rumbold et al., 2014), four exploited sharks from the Mexican coast (0.24–6.6 mg/kg ww; mean 1.8 mg/kg ww, Maz-Courrau et al., 2012), and thresher sharks (A. vulpinus) and shortfin mako (Isurus oxyrinchus) from the Atlantic Ocean (0.21–4.9 mg/kg ww; mean 1.8 mg/kg ww, Teffer et al., 2014). The Me-Hg and T-Hg concentrations were significantly correlated between dorsal and pectoral fins (r = 0.978 for dorsal; r = 0.969 for pectoral, p b 0.001) (Fig. 1), suggesting a homogeneous Hg distribution between fins. However, an earlier study reported differences in Hg accumulation among organs (muscle, kidney, liver and skin) from 15 shark
3
Fig. 1. Relationship between methyl (black circles) and total (white circles) mercury concentrations in dorsal and pectoral fin tissues in 13 shark species.
species (Pethybridge et al., 2010). In this study, the Me-Hg to T-Hg ratios in the pectoral fins of all shark species ranged from 62 to 99% (mean: 81%) and from 57 to 99% (mean: 82%) in the dorsal fins, similar to previous studies (Storelli et al., 2002; Forsyth et al., 2004). Dorsal and pectoral fins had similar Me-Hg/T-Hg ratios within species. Apex predator species, such as sharks, have high Me-Hg/T-Hg ratio due to Me-Hg biomagnification through the marine food web (Maz-Courrau et al., 2012; Teffer et al., 2014; McMeans et al., 2015). The highest Hg concentrations (dorsal fins: 2.5 ± 0.31 mg/kg for MeHg and 3.0 ± 0.45 mg/kg for T-Hg; pectoral fins: 2.6 ± 0.57 mg/kg for Me-Hg and 3.3 ± 0.90 mg/kg for T-Hg) were found in the shortfin mako (I. oxyrinchus). A previous study reported similar Hg levels (mean: 2.7 mg/kg ww) for the same species from the Atlantic Ocean (Teffer et al., 2014). In our study, shortfin mako (I. oxyrinchus) had the longest body length (1.2 ± 0.1 m; average ± standard deviation) and largest body weight (44 ± 26 kg) among all shark species. This result supports the importance of body length and weight in influencing Hg accumulation in sharks. Several studies have confirmed that body length and weight are important factors governing Hg accumulation in sharks (Endo et al., 2008; Rumbold et al., 2014; Teffer et al., 2014). Among shark species investigated, the starspotted smooth-hound shark (Mustelus manazo), oceanic whitetip shark (Squalus megalops), and milk shark (Rhizoprionodon acutus), which are characteristic inshore species, had lower Me-Hg and T-Hg concentrations than did offshore shark species, such as those from the Pacific Ocean. The difference could be due to greater biomagnification potentials of Hg (mostly Me-Hg) offshore than in coastal waters. In our study, five shark species, the blacktip reef shark (Carcharhinus melanopterus), blue shark (Picea glauca), shortfin mako (I. oxyrinchus), oceanic whitetip shark (S. megalops), and smooth hammerhead (Sphyrna zygaena), are aggressive species with carnivorous feeding habits (Compagno et al., 2005). The mean concentrations of Me-Hg (1.39 mg/kg ww) and T-Hg (1.69 mg/kg ww) in the five aggressive species were significantly (p b 0.01) higher than in non-aggressive species (0.89 mg/kg ww for Me-Hg and 1.09 mg/kg ww for T-Hg). This result suggests that feeding habits govern Hg accumulation in sharks, as supported by previous studies (Endo et al., 2013; McMeans et al., 2015). Similar results were found for POPs such as polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and polybrominated diphenyl ethers (PBDEs) in our earlier studies (Lee et al., 2015a,b). Previous studies have reported that Hg accumulation in sharks is influenced by several factors such as body length, age, sex, trophic levels, feeding habits, and local contamination (Pethybridge et al., 2010; Lyons and Lowe, 2013). In our study, Me-Hg levels were significantly
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
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S.-J. Kim et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 2. Correlations between methyl mercury concentrations and (a) body length and (b) body weight in 13 shark species. Abbreviations are as follows; BRS: blacktip reef shark, SD: spiny dogfish, BS: blue shark, PTS: pelagic thresher shark, SM: shortfin mako, CD: cloudy dogfish, SS: shortnose spurdog, OWS: oceanic whitetip shark, MS: milk shark, SH: smooth hammerhead, BHS: banded hound shark, CS: crocodile shark, and SSH: starspotted smooth-hound.
positively correlated with body length (r = 0.473, p b 0.001) and body weight (r = 0.474, p b 0.001) in all species (Fig. 2). These findings indicate that Me-Hg accumulation in sharks could be influenced by body length or weight, consistent with previous studies (Pethybridge et al., 2010; Endo et al., 2009). Of the four most-common shark species (n N 10 individuals), pelagic thresher sharks (Alopias pelagicus) had significant correlations between body length or weight and Me-Hg levels (r = 0.717 for length and r = 0.718 for weight; p b 0.001). A similar result was found for spiny dogfish (Squalus acanthias; r = 0.652, p b 0.001) and blue shark (P. glauca; r = 0.536, p b 0.01) with a significant correlations between body length and Me-Hg levels. However, blacktip reef sharks (C. melanopterus) showed no correlation between body length or weight and Me-Hg levels. The results imply that interspecies differences in Hg accumulation could be partly explained by growth rate. Our previous studies showed biodilution of PCBs, OCPs and PBDEs in blue shark (P. glauca), implying the different bioaccumulation behavior between both chemical groups (Lee et al., 2015a,b). Considering the limited information available on the specific diets of various shark species, evaluating the effects of feeding habits on Hg accumulation is difficult. A report measuring the levels of a nitrogen isotope tracer (δ15N) in stomach contents showed higher Hg levels in shortfin mako (I. oxyrinchus) than in thresher sharks (A. vulpinus) due to differences in diets between the species (Teffer et al., 2014). In this study, the δ15N levels in 13 shark species ranged from 8.1 to 16.6‰ (mean: 12.7‰). The spiny dogfish had the lowest δ15N levels (9.98 ± 0.92‰) while the mean δ15N level was 13.2‰ for the remaining 12 species. Me-Hg and T-Hg concentrations and δ15N ratios were not
significantly related in any of the shark species. The lack of relationship may be associated with diverse feeding patterns for the various shark species. Five shark species, blacktip reef shark (C. melanopterus), blue shark (P. glauca), shortfin mako (I. oxyrinchus), oceanic whitetip shark (S. megalops), and smooth hammerhead (S. zygaena) had significant positive correlations between Me-Hg (r2 = 0.96) or T-Hg (r2 = 0.94) levels and δ15N ratios (Fig. 3). These species could have diets comprising larger and more energetic animals containing more Hg. Previous studies have reported significant correlations between the Hg levels and δ15N ratios in sharks (Newman et al., 2011; Pethybridge et al., 2012). Our results imply the importance of trophic position in determining Hg accumulation in aggressive carnivorous sharks. A number of studies have reported that Me-Hg levels in human samples, such as blood and hair, are strongly correlated with fish and shellfish consumption (Mahaffey et al., 2009; You et al., 2012). Based on toxicity and potential health risks of Hg to humans, several countries and international authorities have suggested permissible residue levels and a reference dose (RfD) or tolerable daily intake (TDI) for Hg in seafood. The Korea Food and Drug Administration (KFDA) and Joint FAO/WHO Codex Alimentarius Commission established a safe limit of Me-Hg as 1 mg/kg wet weight for carnivorous or predatory fishes such as shark and tuna (FAO/WHO, 1991; KFDA, 2010). The Japanese Health Authority and the European Union (EU) have suggested seafood safety guidelines of 0.3 mg/kg for Me-Hg and 0.5 mg/kg for T-Hg (UNEP, 2008). In our study, 80% and 98% of all shark samples exceeded Me-Hg safety limits proposed by the KFDA and FAO/WHO (1 mg/kg ww) and the Japanese Health Authority (0.3 mg/kg ww) (Fig. 4). This result suggests that shark fins are not safe for consumption by Koreans. Among the shark species investigated, some inshore shark species, such as the starspotted smooth-hound shark (M. manazo), oceanic whitetip shark (S. megalops), and milk shark (R. acutus), were below the Me-Hg guidelines proposed by domestic and international health authorities. However, most shark species collected from offshore waters (e.g. Pacific Ocean) exceeded the Me-Hg guidelines proposed by the Japanese Health Authority. In particular, almost all aggressive shark species, such as the blacktip reef shark (C. melanopterus), blue shark (P. glauca), shortfin mako (I. oxyrinchus), oceanic whitetip shark (S. megalops), and smooth hammerhead (S. zygaena), exceeded the Me-Hg limits of the KFDA and FAO/WHO. To assess the potential health risks to Korean populations, estimated daily intakes (EDI) of Me-Hg from shark consumption were compared the RfD and TDI proposed by the US and international health authorities. The US EPA proposed the RfD of 0.1 μg/kg body weight (bw)/day for MeHg (US EPA, 2001) and the Joint FAO/WHO Expert Committee on Food
Fig. 3. Relationships between trophic levels and methyl and total mercury concentrations in five aggressive shark species. (a) black tip shark, (b) blue shark, (c) shortfin mako, (d) oceanic whitetip shark, and (e) smooth hammerhead. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
S.-J. Kim et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
5
Table 2 Maximum allowable shark consumption (g/day) for Me-Hg for Korean populations based on the reference dose (RfD) and provisional tolerable weekly intake (PTWI) suggested by the US EPA and JECFA. Shark species
US EPA (0.1 μg/kg bw/day)
JECFA (0.23 μg/kg bw/day)⁎
Male Female General Male population Blacktip reef shark Spiny dogfish Blue shark Pelagic thresher shark Shortfin mako Cloudy dogfish Shortnose spurdog Oceanic whitetip shark Milk shark Smooth hammerhead Banded hound shark Crocodile shark Starspotted smooth-hound
6.3 6.4 2.9 4.2 2.2 6.7 15 50 45 4.0 8.4 5.4 24
5.7 5.8 2.7 3.8 2.0 6.0 13 45 41 3.6 7.6 4.9 22
6.0 6.0 2.8 4.0 2.1 6.3 14 47 43 3.8 8.0 5.1 23
Female General population
14 13 15 13 6.7 6.1 9.7 8.8 5.1 4.6 15 14 33 30 113 103 103 93 9.2 8.3 19 17 12 11 55 50
14 14 6.4 9.2 4.9 15 32 108 98 8.7 18 12 53
⁎ Provisional tolerable weekly intake (PTWI) from JECFA was recalculated into daily basis.
13) g/day for the general population. Considering a fish meal size (~ 230 g; US EPA, 2001), our results suggest that most sharks should not be consumed at all. The US EPA and US FDA recommended limited shark consumption by children and women of childbearing age (US EPA, 2001; US FDA, 2014); however, there are no advisories for shark consumption associated with Hg exposure in Korea. The present study provides advisories for shark consumption related to Hg exposure to minimize potential health risks, especially pregnant women and toddlers in Korea. Because of the high consumption of seafood in Korea, a monitoring program for Hg (including Me-Hg) should be instituted for various shark species to protect human health. Acknowledgments This work was supported by the research fund of Hanyang University (HY-2012-000-0000-1399), Korea. References
Fig. 4. Cumulative distribution of methyl mercury concentrations in all shark species (a), distribution of Me-Hg concentrations for each shark species (b), and comparison with the Me-Hg guidelines proposed by the Korea Food and Drug Administration (KFDA, 2010), FAO/WHO (FAO/WHO, 1991) and Japanese Health Authority (UNEP, 2008).
Additives (JECFA) established a provisional tolerable weekly intake (PTWI) of 1.6 μg/kg bw/week (corresponding to 0.23 μg/kg bw/day) for Me-Hg (WHO, 2008). In our study, the EDIs of Me-Hg from consuming various sharks for the general populations, males and females in Korea were 0.2–3.7 (mean: 1.4) μg/kg bw/day, 0.2–4.0 (mean: 1.5) μg/kg bw/ day, and 0.2–3.5 (mean: 1.3) μg/kg bw/day, respectively. These EDIs exceeded regulatory guidelines for most shark species, indicating that excessive shark consumption may pose a potential health risk for Koreans due to Hg exposure. To make recommendations on shark consumption related to Me-Hg exposure for the Korean population, the maximum shark consumption was calculated by using regulatory guidelines from both the US EPA and JECFA (Table 2). Using the JECFA guideline, the allowable consumption for various sharks ranged from 4.9 to 108 (mean: 30) g/day for the general population. Using the more conservative guideline from the US EPA, the allowable consumption ranged from 2.1 to 47 (mean:
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Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
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Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea Sang-Jo Kim a, Hyun-Kyung Lee b, Abimbola C. Badejo b, Won-Chan Lee c, Hyo-Bang Moon b,⁎ a b c
National Fishery Products Quality Management Service (FiQ), Busan 606-705, Republic of Korea Department of Marine Sciences and Convergent Technology, College of Science and Technology, Hanyang University, Ansan 426-791, Republic of Korea Marine Environment Research Division, National Fisheries Research and Development Institute (NFRDI), Busan 619-705, Republic of Korea
a r t i c l e
i n f o
Article history: Received 16 September 2015 Received in revised form 9 November 2015 Accepted 16 November 2015 Available online xxxx Keywords: Mercury Methyl mercury Shark Feeding habit Trophic position Safety limit
a b s t r a c t Limited information is available on mercury (Hg) levels in various shark species consumed in Korea. The methylHg (Me-Hg) and total Hg concentrations in all shark species ranged from 0.08 to 4.5 (mean: 1.2) mg/kg wet weight and from 0.1 to 7.0 (mean: 1.4) mg/kg wet weight, respectively. Inter-species differences in Hg accumulation were found among the species; however, Hg accumulation was homogenous between dorsal and pectoral fins within species. The highest Hg levels were found in aggressive carnivore shark species. Trophic position was important in determining Hg accumulation for aggressive carnivore sharks. Approximately 80% of shark species exceeded the safety limits for Me-Hg established by domestic and international authorities. The mean estimated daily intake of Me-Hg (1.3 μg/kg body weight/day) for Korean populations consuming various sharks was higher than the guidelines proposed by international regulatory authorities, suggesting that excessive shark fin consumption may pose potential health risks for Koreans. © 2015 Published by Elsevier Ltd.
Mercury (Hg) is a global pollutant released into the atmosphere by a variety of anthropogenic activities such as industrial fossil fuel combustion and waste disposal (Pacyna et al., 2006; Swain et al., 2007). With global mercury emissions reaching an estimated 5000 to 8000 metric tons each year (UNEP, 2013), the presence of Hg in the atmosphere has become problematic as it is eventually deposited in the aquatic environments. Methyl mercury (Me-Hg), formed in sediment by microbial methylation of Hg, is extremely toxic and has raised human health concerns due to its bioaccumulation and biomagnification potential through the food web (Teffer et al., 2014; McMeans et al., 2015). Human exposure to Me-Hg is almost exclusively from consuming aquatic organisms, especially predatory fish (Moon et al., 2011; Karimi et al., 2014). Fish is a highly nutritious food with amazing human benefits, but the contamination of this important global commodity by MeHg has become a challenge to public health, as over 90% of Hg in fish is Me-Hg (Rimondi et al., 2012). Thus, Me-Hg exposure associated with consuming fish and shellfish poses health risks, such as immune deficiencies and toxicity to the central nervous system, especially in fetuses (Mergler et al., 2007; Choi et al., 2014). Sharks tend to accumulate high levels of toxic contaminants, such as persistent organic pollutants (POPs) and Hg, because they are top predators in the marine food web and have a long lifespan (Endo et al., 2008; Torres et al., 2014; Lee et al., 2015a,b). Sharks are commonly consumed ⁎ Corresponding author. E-mail address: [email protected] (H.-B. Moon).
in the form of shark fin soup, filets and liver oil in many countries such as Australia, China, Japan and Korea (Man et al., 2014; Nalluri et al., 2014). Shark liver oil is ingested as a nutritional source of omega-3 fatty acids, which lower the risk of heart disease, inflammatory disease and rheumatoid arthritis, among many other benefits (Maggie and Covington, 2004). The United States Environmental Protection Agency (US EPA) and Food and Drug Administration (US FDA) have designated sharks as high mercury-containing fishes to limit consumption by children and women of childbearing age (US EPA, 2001; US FDA, 2014). A nationwide survey of Hg in the Korean population suggested that blood Me-Hg levels are associated with fish consumption (You et al., 2012). In addition, some regions of Korea (e.g. Pohang and Daegu cities) traditionally consume shark as part of the local diets. However, Hg levels in marketed sharks and the potential health risks of Hg associated with shark consumption in Korea have not been documented. In this study, we determined Me-Hg and total mercury (T-Hg) concentrations in dorsal and pectoral fins in 13 shark species obtained offshore and in Korean coastal waters. We investigated the factors influencing Hg accumulation in various sharks. Furthermore, shark consumption limits were recommended based on the risk assessment of Me-Hg, using the reference dose (RfD) and tolerable daily intake (TDI) for Koreans. Muscle tissues from dorsal and pectoral fins were collected from 13 shark species (n = 103) found entangled in long lines of commercial fisheries or by-caught in trawl nets either offshore (Indian and Pacific Oceans) or in Korean coastal waters between July and October, 2010. All shark species surveyed in this study are globally endangered and
http://dx.doi.org/10.1016/j.marpolbul.2015.11.038 0025-326X/© 2015 Published by Elsevier Ltd.
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
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Table 1 Concentrations (mg/kg wet weight) of methyl (Me-Hg) and total mercury (T-Hg) in dorsal and pectoral fins from 13 shark species from offshore and Korean coastal waters. Species (scientific name)
Blacktip reef shark (Carcharhinus melanopterus) Spiny dogfish (Squlus acanthias)
na
Sampling locations
Feeding habitsb
26 Pacific Ocean Aggressive carnivore 17 Pacific Ocean Carnivore
BLc (m) (Mean
δ15Ne (‰) BWd (kg) (Mean ± SD) (Mean ±
± SD)
SD)
0.9 ±
21 ± 11
Dorsal fin
Pectoral fin
Mean ± SD (Min–Max)
%f
Mean ± SD (Min–Max)
T-Hg
12.8 ± 1.84
0.91 ± 0.63 (0.12–2.4)
1.1 ± 0.77 (0.13–3.2)
86 0.90 ± 0.67 (0.12–2.6)
1.0 ± 0.79 (0.15–3.4)
86
0.2
Me-Hg
%
Me-Hg
T-Hg
0.8 ±
2.7 ± 0.9 10.0 ± 0.92
0.80 ± 0.34 (0.36–1.7)
0.96 ± 0.38 (0.42–1.9)
84 0.98 ± 0.34 (0.39–1.6)
1.2 ± 0.41 (0.46–1.8)
82
0.1 1.1 ±
22 ± 8.2 13.8 ± 1.09
1.9 ± 0.94 (0.43–3.9)
2.3 ± 1.1 (0.55–4.8)
80 2.0 ± 1.1 (0.68–4.5)
2.5 ± 1.6 (0.88–7.0)
79
0.2 1.0 ±
40 ± 29
12.6 ± 2.38
1.3 ± 0.52 (0.24–2.1)
1.5 ± 0.51 (0.29–2.2)
86 1.4 ± 0.60 (0.20–2.7)
1.6 ± 0.66 (0.24–3.1)
84
0.3 1.2 ±
44 ± 26
14.5 ± 1.57
2.5 ± 0.31 (2.1–2.9)
3.0 ± 0.45 (2.5–3.5)
81 2.6 ± 0.57 (2.10–3.8)
3.3 ± 0.90 (2.2–5.0)
81
Carnivore
0.1 0.3
0.8 ± 1.0 12.5 ± 0.15
0.9
4.2 ± 0.7 14.4 ± 0.80
1.1 ± 0.43 (0.64–1.7) 0.53 ± 0.79 (0.12–1.7)
78 0.87 ± 0.30 (0.60–1.4) 82 0.37 ± 0.52 (0.09–1.2)
1.2 ± 0.29 (0.91–1.7) 0.53 ± 0.78 (0.13–1.7)
72
4 Pacific Ocean Carnivore
0.84 ± 0.40 (0.50–1.4) 0.41 ± 0.59 (0.08–1.3)
3 Korean coast
0.9 ±
17 ± 16
11.9 ± 1.65
0.11 ± 0.05 (0.08–0.17)
0.15 ± 0.04 (0.12–0.19)
73 0.12 ± 0.04 (0.08–0.16)
0.16 ± 0.06 (0.10–0.22)
74
0.3 1.1 ±
9.6 ± 0.7 13.6 ± 0.74
0.11 ± 0.02 (0.08–0.12)
0.16 ± 0.03 (0.14–0.19)
68 0.15 ± 0.02 (0.13–0.16)
0.21 ± 0.03 (0.17–0.24)
72
0.1 1.1 ±
17 ± 12
13.6 ± 1.90
1.4 ± 0.90 (0.42–2.2)
1.6 ± 0.90 (0.61–2.4)
83 1.4 ± 0.96 (0.33–2.0)
1.7 ± 1.0 (0.48–2.3)
81
Blue shark (Prionace glauca)
15 Pacific Ocean Aggressive carnivore
Pelagic thresher shark (Alopias pelagicus)
13 Pacific Ocean Aggressive carnivore
Shortfin mako (Isurus oxyrinchus)
7 Pacific Ocean Carnivore Indian Ocean
Cloudy dogfish (Scyliorhinus torazame) Shortnose spurdog (Carcharhinus longimanus) Oceanic whitetip shark (Squalus megalops)
5 Korean coast
Aggressive carnivore
Milk shark (Rhizoprionodon acutus)
3 Korean coast
Smooth hammerhead (Sphyrna zygaena)
3 Pacific Ocean Aggressive Korean coast carnivore
Banded hound shark (Triakis scyllium)
3 Pacific Ocean Carnivore
0.2 1.1 ±
5.7 ± 3.2 12.5 ± 1.00
0.77 ± 1.1 (0.12–2.0)
1.1 ± 1.4 (0.17–2.7)
69 0.58 ± 0.84 (0.09–1.6)
0.84 ± 1.20 (0.14–2.2)
69
Crocodile shark (Psedocarcharias kamoharai) Starspotted smooth-hound (Mustelus manazo)
2 Indian Ocean Carnivore
0.4 0.8
1.6 ± 0.4 14.8 ± 0.63
1.1 ± 0.26 (0.92–1.3)
1.5 ± 0.32 (1.3–1.7)
74 1.0 ± 0.30 (0.79–1.2)
1.4 ± 0.37 (1.1–1.6)
72
2 Korean coast
0.6
1.6 ± 0.8 13.1 ± 1.43
0.24 ± 0.07 (0.19–0.29)
0.32 ± 0.14 (0.23–0.42)
76 0.23 ± 0.06 (0.19–0.27)
0.32 ± 0.08 (0.26–0.38)
71
a b c d e f
Carnivore
75
Carnivore
n = sample number. Feeding habits were cited from Stillwell and Kohler (1982) and Parker (2008). BL = body length. BW = body weight. δ15N = delta nitrogen isotope ratio. % = ratio of methyl mercury to the total mercury.
part of the conservation inventory of the International Union for Conservation and Natural Resources (IUCN) Red List (Compagno et al., 2005). Biological information such as body length, body weight, feeding habits, and stable isotope ratios for each species are summarized in Table 1. Detailed information on habitats and major prey for each shark species were described in previous study (Lee et al., 2015a). After the sharks were dissected on commercial ships, the dorsal and pectoral fins were transported to the National Fishery Products Quality Management Service (FiQ) of Korea, and kept frozen at −20 °C until analysis. Me-Hg and T-Hg analyses have been described in detail elsewhere (Moon et al., 2011). In brief, T-Hg in the shark samples was determined using the gold amalgamation method, with a high-temperature combustion SP-3D analyzer (Nippon Instrument Co., Tokyo, Japan). Freeze-dried fins (approximately 100 mg) were placed on a layer of sodium carbonate and calcium hydroxide mixture (Additive M; Nippon Instrument Co.) in a ceramic boat. The sample was then covered with a layer of Additive M. A layer of aluminum oxide (Nippon Instrument Co.) was placed over the Additive M and then covered with another layer of Additive M. The boat was transferred into the mercury analyzer to determine T-Hg. A calibration curve with a correlation coefficient of at least 0.9 was drawn for every 20 samples. Analysis of duplicate samples yielded an average relative standard deviation (RSD) of less than 20%. To determine Me-Hg concentrations, freeze-dried muscles from fins (~2 g) were put into a 100-mL centrifuge tube, and 10 mL of 25% sodium chloride (NaCl; ultra residue analysis, Wako, Tokyo, Japan) was added. After shaking for 2 min, 15 mL of toluene (ultra residue analysis, J. T.
Baker, Phillipsburg, NJ, USA) and 4 mL of hydrochloric acid (HCl; hazardous metal analysis, Wako) were added and shaken for 2 min. The mixture was then centrifuged at 3000 rpm for 20 min, and the organic layer was put into a 125-mL separating funnel. The extract was washed with 10 mL of 25% NaCl. Five milliliters of L-cysteine solution (guaranteed reagent; Junsei, Tokyo, Japan) was added to the extract and shaken for 10 min. After standing for 10 min, the upper layer was put into a polypropylene tube; 4 mL of HCl solution (HCl: distilled water = 3:1) and 5 mL of toluene were added, and the mixture was shaken for 1 min and centrifuged at 2500 rpm for 5 min. The toluene layer was separated and dehydrated with anhydrous sodium sulfate (Na2SO4; ultra residue analysis, Merck, Darmstadt, Germany). The extracts were concentrated to 1 mL and analyzed by gas chromatography/electron capture detection (GC/ECD) (GC 6890 N; Agilent, Wilmington, DE, USA). The capillary column used was an Ulbon HR-Thermon Hg column (15m length, 0.53-mm inner diameter; Shimadzu, Kyoto, Japan). The inlet and detector temperatures were maintained at 170 °C. The carrier gas was nitrogen (N2) at a constant flow of 16 mL/min, and the makeup gas was N2 at 60 mL/min. The oven temperature was maintained at 160 °C for 10 min. To assess the quality of the analytical procedures and instrumental conditions for T-Hg, we analyzed standard mussel (Mytilus edulis) reference materials (ERM-CE278; IRMM, Geel, Belgium). The T-Hg values (n = 7) ranged from 80 to110% with a mean of 95% for the certified values. Matrix spike samples (100 ng of Me-Hg) were processed to assess the quality of Me-Hg determination. The Me-Hg recoveries ranged from 98 to 106% with a mean of 103%. The limits
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
S.-J. Kim et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
of detections (LODs) were designated as the lowest acceptable standards in the calibration curve for each chemical and were 5 ng/g for Me-Hg and 3 ng/g for T-Hg. The nitrogen stable isotope ratio (δ15N) in muscles from dorsal fins of the 13 shark species was analyzed to identify trophic position. The δ15N analysis method has been described in detail elsewhere (Park et al., 2011). In brief, wet samples were treated with 1 N HCl to remove carbonates, and rinsed with distilled water. Once dry, the samples were homogenized and weighed in a tin capsule. The samples were put into a CHN elemental analyzer (Euro Vector 3000 series, Milan, Italy) combined with a continuous-flow isotope ratio-mass spectrometer (IsoPrime, GV Instruments, UK) for oxidization at high temperature (1030 °C). δ15N was measured on 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 isotope ratios of the sample and conventional standards (i.e., atmospheric air for nitrogen), according to the following equation: δX (‰) = [(Rsample/Rstandard) − 1] × 103, where X is 15N and R is the 15N/14N ratio. Calibration was conducted using international standards as reference materials (IAEA-N1 for nitrogen). Daily intakes of Me-Hg and T-Hg were calculated by multiplying the seafood consumption rate (g/day) with the corresponding Hg concentrations (mg/kg). Average daily seafood consumption rates and body weight for general populations and sex groups in Korea were obtained from Korean Exposure Factor Handbook (KEFH). The seafood consumption rates used in this study were 79.6 g/day for the general population, 89.4 g/day for men and 70.6 g/day for women. The body weights were 54.1 kg for the general population, 57.0 g/day for men and 51.6 g/day for women (Jang et al., 2014). Kolmogorov–Smirnov and Shapiro–Wilk tests were performed to assess the normality of the Me-Hg and T-Hg concentrations. Me-Hg and T-Hg concentrations were not normally distributed in sharks, MeHg and T-Hg concentrations were log-transformed for all statistical analyses. Student's t-test was conducted to investigate significant differences in Me-Hg and T-Hg concentrations among shark species and feeding habits. Spearman's rank correlation analysis was performed to investigate the strength of relationships between Hg concentrations and factors contributing to accumulation in sharks. Statistical significance was set at p b 0.05. All statistical analyses were performed using SPSS 18.0 K for Windows (SPSS Inc., Chicago, IL, USA). Me-Hg and T-Hg concentrations in the dorsal and pectoral fins from 13 shark species found offshore and in Korean coastal waters are summarized in Table 1. The overall Me-Hg and T-Hg concentrations were highly variable among shark species. The Me-Hg and T-Hg concentrations in pectoral fins ranged from 0.08 to 4.5 (mean: 1.2) mg/kg wet weight (ww) and from 0.1 to 7.0 (mean: 1.5) mg/kg ww, respectively, for all samples. The Me-Hg and T-Hg concentrations in dorsal fins ranged from 0.08 to 3.9 (mean: 1.1) mg/kg ww and from 0.12 to 4.8 (mean: 1.4) mg/kg ww, respectively, for all samples. The T-Hg concentrations in various sharks in our study (0.1–7.0 mg/kg; mean 1.2 mg/kg ww) were similar to those measured in tiger sharks (Galeocerdo cuvier) from the Japanese coast (0.38–3.7 mg/kg ww; mean 0.78 mg/kg ww, Endo et al., 2008), common thresher shark (Alopias vulpinus) from the California coast (1.4 mg/kg ww, Lyons and Lowe, 2013), seven shark species from the Florida coast (0.19–4.5 mg/kg ww; mean 1.6 mg/kg ww, Rumbold et al., 2014), four exploited sharks from the Mexican coast (0.24–6.6 mg/kg ww; mean 1.8 mg/kg ww, Maz-Courrau et al., 2012), and thresher sharks (A. vulpinus) and shortfin mako (Isurus oxyrinchus) from the Atlantic Ocean (0.21–4.9 mg/kg ww; mean 1.8 mg/kg ww, Teffer et al., 2014). The Me-Hg and T-Hg concentrations were significantly correlated between dorsal and pectoral fins (r = 0.978 for dorsal; r = 0.969 for pectoral, p b 0.001) (Fig. 1), suggesting a homogeneous Hg distribution between fins. However, an earlier study reported differences in Hg accumulation among organs (muscle, kidney, liver and skin) from 15 shark
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Fig. 1. Relationship between methyl (black circles) and total (white circles) mercury concentrations in dorsal and pectoral fin tissues in 13 shark species.
species (Pethybridge et al., 2010). In this study, the Me-Hg to T-Hg ratios in the pectoral fins of all shark species ranged from 62 to 99% (mean: 81%) and from 57 to 99% (mean: 82%) in the dorsal fins, similar to previous studies (Storelli et al., 2002; Forsyth et al., 2004). Dorsal and pectoral fins had similar Me-Hg/T-Hg ratios within species. Apex predator species, such as sharks, have high Me-Hg/T-Hg ratio due to Me-Hg biomagnification through the marine food web (Maz-Courrau et al., 2012; Teffer et al., 2014; McMeans et al., 2015). The highest Hg concentrations (dorsal fins: 2.5 ± 0.31 mg/kg for MeHg and 3.0 ± 0.45 mg/kg for T-Hg; pectoral fins: 2.6 ± 0.57 mg/kg for Me-Hg and 3.3 ± 0.90 mg/kg for T-Hg) were found in the shortfin mako (I. oxyrinchus). A previous study reported similar Hg levels (mean: 2.7 mg/kg ww) for the same species from the Atlantic Ocean (Teffer et al., 2014). In our study, shortfin mako (I. oxyrinchus) had the longest body length (1.2 ± 0.1 m; average ± standard deviation) and largest body weight (44 ± 26 kg) among all shark species. This result supports the importance of body length and weight in influencing Hg accumulation in sharks. Several studies have confirmed that body length and weight are important factors governing Hg accumulation in sharks (Endo et al., 2008; Rumbold et al., 2014; Teffer et al., 2014). Among shark species investigated, the starspotted smooth-hound shark (Mustelus manazo), oceanic whitetip shark (Squalus megalops), and milk shark (Rhizoprionodon acutus), which are characteristic inshore species, had lower Me-Hg and T-Hg concentrations than did offshore shark species, such as those from the Pacific Ocean. The difference could be due to greater biomagnification potentials of Hg (mostly Me-Hg) offshore than in coastal waters. In our study, five shark species, the blacktip reef shark (Carcharhinus melanopterus), blue shark (Picea glauca), shortfin mako (I. oxyrinchus), oceanic whitetip shark (S. megalops), and smooth hammerhead (Sphyrna zygaena), are aggressive species with carnivorous feeding habits (Compagno et al., 2005). The mean concentrations of Me-Hg (1.39 mg/kg ww) and T-Hg (1.69 mg/kg ww) in the five aggressive species were significantly (p b 0.01) higher than in non-aggressive species (0.89 mg/kg ww for Me-Hg and 1.09 mg/kg ww for T-Hg). This result suggests that feeding habits govern Hg accumulation in sharks, as supported by previous studies (Endo et al., 2013; McMeans et al., 2015). Similar results were found for POPs such as polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and polybrominated diphenyl ethers (PBDEs) in our earlier studies (Lee et al., 2015a,b). Previous studies have reported that Hg accumulation in sharks is influenced by several factors such as body length, age, sex, trophic levels, feeding habits, and local contamination (Pethybridge et al., 2010; Lyons and Lowe, 2013). In our study, Me-Hg levels were significantly
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
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S.-J. Kim et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 2. Correlations between methyl mercury concentrations and (a) body length and (b) body weight in 13 shark species. Abbreviations are as follows; BRS: blacktip reef shark, SD: spiny dogfish, BS: blue shark, PTS: pelagic thresher shark, SM: shortfin mako, CD: cloudy dogfish, SS: shortnose spurdog, OWS: oceanic whitetip shark, MS: milk shark, SH: smooth hammerhead, BHS: banded hound shark, CS: crocodile shark, and SSH: starspotted smooth-hound.
positively correlated with body length (r = 0.473, p b 0.001) and body weight (r = 0.474, p b 0.001) in all species (Fig. 2). These findings indicate that Me-Hg accumulation in sharks could be influenced by body length or weight, consistent with previous studies (Pethybridge et al., 2010; Endo et al., 2009). Of the four most-common shark species (n N 10 individuals), pelagic thresher sharks (Alopias pelagicus) had significant correlations between body length or weight and Me-Hg levels (r = 0.717 for length and r = 0.718 for weight; p b 0.001). A similar result was found for spiny dogfish (Squalus acanthias; r = 0.652, p b 0.001) and blue shark (P. glauca; r = 0.536, p b 0.01) with a significant correlations between body length and Me-Hg levels. However, blacktip reef sharks (C. melanopterus) showed no correlation between body length or weight and Me-Hg levels. The results imply that interspecies differences in Hg accumulation could be partly explained by growth rate. Our previous studies showed biodilution of PCBs, OCPs and PBDEs in blue shark (P. glauca), implying the different bioaccumulation behavior between both chemical groups (Lee et al., 2015a,b). Considering the limited information available on the specific diets of various shark species, evaluating the effects of feeding habits on Hg accumulation is difficult. A report measuring the levels of a nitrogen isotope tracer (δ15N) in stomach contents showed higher Hg levels in shortfin mako (I. oxyrinchus) than in thresher sharks (A. vulpinus) due to differences in diets between the species (Teffer et al., 2014). In this study, the δ15N levels in 13 shark species ranged from 8.1 to 16.6‰ (mean: 12.7‰). The spiny dogfish had the lowest δ15N levels (9.98 ± 0.92‰) while the mean δ15N level was 13.2‰ for the remaining 12 species. Me-Hg and T-Hg concentrations and δ15N ratios were not
significantly related in any of the shark species. The lack of relationship may be associated with diverse feeding patterns for the various shark species. Five shark species, blacktip reef shark (C. melanopterus), blue shark (P. glauca), shortfin mako (I. oxyrinchus), oceanic whitetip shark (S. megalops), and smooth hammerhead (S. zygaena) had significant positive correlations between Me-Hg (r2 = 0.96) or T-Hg (r2 = 0.94) levels and δ15N ratios (Fig. 3). These species could have diets comprising larger and more energetic animals containing more Hg. Previous studies have reported significant correlations between the Hg levels and δ15N ratios in sharks (Newman et al., 2011; Pethybridge et al., 2012). Our results imply the importance of trophic position in determining Hg accumulation in aggressive carnivorous sharks. A number of studies have reported that Me-Hg levels in human samples, such as blood and hair, are strongly correlated with fish and shellfish consumption (Mahaffey et al., 2009; You et al., 2012). Based on toxicity and potential health risks of Hg to humans, several countries and international authorities have suggested permissible residue levels and a reference dose (RfD) or tolerable daily intake (TDI) for Hg in seafood. The Korea Food and Drug Administration (KFDA) and Joint FAO/WHO Codex Alimentarius Commission established a safe limit of Me-Hg as 1 mg/kg wet weight for carnivorous or predatory fishes such as shark and tuna (FAO/WHO, 1991; KFDA, 2010). The Japanese Health Authority and the European Union (EU) have suggested seafood safety guidelines of 0.3 mg/kg for Me-Hg and 0.5 mg/kg for T-Hg (UNEP, 2008). In our study, 80% and 98% of all shark samples exceeded Me-Hg safety limits proposed by the KFDA and FAO/WHO (1 mg/kg ww) and the Japanese Health Authority (0.3 mg/kg ww) (Fig. 4). This result suggests that shark fins are not safe for consumption by Koreans. Among the shark species investigated, some inshore shark species, such as the starspotted smooth-hound shark (M. manazo), oceanic whitetip shark (S. megalops), and milk shark (R. acutus), were below the Me-Hg guidelines proposed by domestic and international health authorities. However, most shark species collected from offshore waters (e.g. Pacific Ocean) exceeded the Me-Hg guidelines proposed by the Japanese Health Authority. In particular, almost all aggressive shark species, such as the blacktip reef shark (C. melanopterus), blue shark (P. glauca), shortfin mako (I. oxyrinchus), oceanic whitetip shark (S. megalops), and smooth hammerhead (S. zygaena), exceeded the Me-Hg limits of the KFDA and FAO/WHO. To assess the potential health risks to Korean populations, estimated daily intakes (EDI) of Me-Hg from shark consumption were compared the RfD and TDI proposed by the US and international health authorities. The US EPA proposed the RfD of 0.1 μg/kg body weight (bw)/day for MeHg (US EPA, 2001) and the Joint FAO/WHO Expert Committee on Food
Fig. 3. Relationships between trophic levels and methyl and total mercury concentrations in five aggressive shark species. (a) black tip shark, (b) blue shark, (c) shortfin mako, (d) oceanic whitetip shark, and (e) smooth hammerhead. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038
S.-J. Kim et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
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Table 2 Maximum allowable shark consumption (g/day) for Me-Hg for Korean populations based on the reference dose (RfD) and provisional tolerable weekly intake (PTWI) suggested by the US EPA and JECFA. Shark species
US EPA (0.1 μg/kg bw/day)
JECFA (0.23 μg/kg bw/day)⁎
Male Female General Male population Blacktip reef shark Spiny dogfish Blue shark Pelagic thresher shark Shortfin mako Cloudy dogfish Shortnose spurdog Oceanic whitetip shark Milk shark Smooth hammerhead Banded hound shark Crocodile shark Starspotted smooth-hound
6.3 6.4 2.9 4.2 2.2 6.7 15 50 45 4.0 8.4 5.4 24
5.7 5.8 2.7 3.8 2.0 6.0 13 45 41 3.6 7.6 4.9 22
6.0 6.0 2.8 4.0 2.1 6.3 14 47 43 3.8 8.0 5.1 23
Female General population
14 13 15 13 6.7 6.1 9.7 8.8 5.1 4.6 15 14 33 30 113 103 103 93 9.2 8.3 19 17 12 11 55 50
14 14 6.4 9.2 4.9 15 32 108 98 8.7 18 12 53
⁎ Provisional tolerable weekly intake (PTWI) from JECFA was recalculated into daily basis.
13) g/day for the general population. Considering a fish meal size (~ 230 g; US EPA, 2001), our results suggest that most sharks should not be consumed at all. The US EPA and US FDA recommended limited shark consumption by children and women of childbearing age (US EPA, 2001; US FDA, 2014); however, there are no advisories for shark consumption associated with Hg exposure in Korea. The present study provides advisories for shark consumption related to Hg exposure to minimize potential health risks, especially pregnant women and toddlers in Korea. Because of the high consumption of seafood in Korea, a monitoring program for Hg (including Me-Hg) should be instituted for various shark species to protect human health. Acknowledgments This work was supported by the research fund of Hanyang University (HY-2012-000-0000-1399), Korea. References
Fig. 4. Cumulative distribution of methyl mercury concentrations in all shark species (a), distribution of Me-Hg concentrations for each shark species (b), and comparison with the Me-Hg guidelines proposed by the Korea Food and Drug Administration (KFDA, 2010), FAO/WHO (FAO/WHO, 1991) and Japanese Health Authority (UNEP, 2008).
Additives (JECFA) established a provisional tolerable weekly intake (PTWI) of 1.6 μg/kg bw/week (corresponding to 0.23 μg/kg bw/day) for Me-Hg (WHO, 2008). In our study, the EDIs of Me-Hg from consuming various sharks for the general populations, males and females in Korea were 0.2–3.7 (mean: 1.4) μg/kg bw/day, 0.2–4.0 (mean: 1.5) μg/kg bw/ day, and 0.2–3.5 (mean: 1.3) μg/kg bw/day, respectively. These EDIs exceeded regulatory guidelines for most shark species, indicating that excessive shark consumption may pose a potential health risk for Koreans due to Hg exposure. To make recommendations on shark consumption related to Me-Hg exposure for the Korean population, the maximum shark consumption was calculated by using regulatory guidelines from both the US EPA and JECFA (Table 2). Using the JECFA guideline, the allowable consumption for various sharks ranged from 4.9 to 108 (mean: 30) g/day for the general population. Using the more conservative guideline from the US EPA, the allowable consumption ranged from 2.1 to 47 (mean:
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Please cite this article as: Kim, S.-J., et al., Species-specific accumulation of methyl and total mercury in sharks from offshore and coastal waters of Korea, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.11.038