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Methylmercury in dried shark fins and shark fin soup from American restaurants
STOTEN-16238; No of Pages 5 Science of the Total Environment xxx (2014) xxx–xxx
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Methylmercury in dried shark fins and shark fin soup from American restaurants Deepthi Nalluri a, Zofia Baumann b,⁎, Debra L. Abercrombie c, Demian D. Chapman c, Chad R. Hammerschmidt a, Nicholas S. Fisher c a b c
Department of Earth & Environmental Sciences, Wright State University, Dayton, OH 45435, United States Department of Marine Sciences, University of Connecticut, Avery Point, Groton, CT 06340, United States School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, United States
H I G H L I G H T S • Concentrations of monomethylmercury (MMHg) in fins and soup varied among shark species. • MMHg was highest in fins and soup from large, high trophic level sharks. • Estimated human exposures to MMHg from shark fin soup are relatively low.
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Article history: Received 13 February 2014 Received in revised form 24 April 2014 Accepted 25 April 2014 Available online xxxx Editor: Mae Sexauer Gustin Keywords: Shark fin soup Mercury Public health Food
a b s t r a c t Consumption of meat from large predatory sharks exposes human consumers to high levels of toxic monomethylmercury (MMHg). There also have been claims that shark fins, and hence the Asian delicacy shark fin soup, contain harmful levels of neurotoxic chemicals in combination with MMHg, although concentrations of MMHg in shark fins are unknown. We measured MMHg in dried, unprocessed fins (n = 50) of 13 shark species that occur in the international trade of dried shark fins as well as 50 samples of shark fin soup prepared by restaurants from around the United States. Concentrations of MMHg in fins ranged from 9 to 1720 ng/g dry wt. MMHg in shark fin soup ranged from b0.01 to 34 ng/mL, with MMHg averaging 62 ± 7% of total Hg. The highest concentrations of MMHg and total Hg were observed in both fins and soup from large, high trophic level sharks such as hammerheads (Sphyrna spp.). Consumption of a 240 mL bowl of shark fin soup containing the average concentration of MMHg (4.6 ng/mL) would result in a dose of 1.1 μg MMHg, which is 16% of the U.S. EPA's reference dose (0.1 μg MMHg per 1 kg per day in adults) of 7.4 μg per day for a 74 kg person. If consumed, the soup containing the highest measured MMHg concentration would exceed the reference dose by 17%. While shark fin soup represents a potentially important source of MMHg to human consumers, other seafood products, particularly the flesh of apex marine predators, contain much higher MMHg concentrations and can result in substantially greater exposures of this contaminant for people. © 2014 Published by Elsevier B.V.
1. Introduction Many marine apex predators contain high concentrations of mercury (Hg) and are potential sources of this contaminant for humans (Fitzgerald and Clarkson, 1991). Monomethylmercury (MMHg), as opposed to complexes of inorganic Hg, is the toxic form of Hg bioaccumulated by fish (Bloom, 1992). Shark muscle, for example, can contain concentrations of MMHg (~0.5–50 μg/g wet weight; Hornung et al., 1993; Storelli et al., 2003) that are far greater than the recommended human consumption advisory limit for MMHg in fish (0.3 μg/g; U.S. EPA, 2001). In addition to neurotoxicity, effects of MMHg may include increased risk of ⁎ Corresponding author. Tel.: +1 631 632 8697; fax: +1 631 632 3072. E-mail address: zofi[email protected] (Z. Baumann).
cardiovascular disease in adults who eat fish (Salonen et al., 1995; Karagas et al., 2012). Moreover, maternal transfer of MMHg to prenatal life stages can inhibit the neurological and cardiovascular development and growth of some children (Grandjean et al., 1997; Murata et al., 1999; Sorenson et al., 1999; Steuerwald et al., 2000; Karagas et al., 2012). Although it is well established that shark meat contains high values of Hg, less is known about concentrations in other shark body parts that are consumed by humans. Dried shark fins are among the most highly traded and consumed shark parts in the world. They are used to make the Asian delicacy - shark fin soup, a luxury dish that is often served as an appetizer. This expensive delicacy consists mostly of ceratotrichia (or “fin needles”; elastin and collagen fibers that resemble rice noodles when cooked) served with either chicken broth or another stock for flavor (Rose, 1996). Recent claims have been made that shark fin soup can
http://dx.doi.org/10.1016/j.scitotenv.2014.04.107 0048-9697/© 2014 Published by Elsevier B.V.
Please cite this article as: Nalluri D, et al, Methylmercury in dried shark fins and shark fin soup from American restaurants, Sci Total Environ (2014), http://dx.doi.org/10.1016/j.scitotenv.2014.04.107
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contain elevated levels of contaminants, potentially putting consumers at risk (Holtcamp, 2012; Mondo et al., 2012). To date, however, there are no published studies documenting Hg concentrations in either shark fins or shark fin soup. Our objective was to examine concentrations of total Hg and MMHg in dried unprocessed shark fins from wild captured animals, and shark fin soup, offered for retail sale in the United States, and evaluate potential health risk to human consumers. 2. Materials and methods 2.1. Samples All samples were collected using standard clean procedures for Hg analysis. Whole, dried unprocessed shark fins examined in this study were collected from wild-captured specimens taken from fisheries of the United States, Sri Lanka, Fiji, and South Africa as part of a separate study. All fins were sun-dried. Fins were stored at Stony Brook University in separate plastic bags at room temperature for 12 to 18 months prior to sampling. A small piece (~10 mm × 10 mm) of the distal portion of each fin was analyzed for Hg content. Fins originated from one of 13 shark species, all of which are known to occur in the international dried fin trade (Table 1). Bowls of shark fin soup were purchased for Hg analysis from 50 restaurants located throughout the United States by volunteers in March and April 2012 (Table S1). Either species or genus of origin of the fin used to make each bowl of soup was assessed using a mini-DNA barcode protocol on a single, randomly selected fin needle taken from each bowl (Fields et al., in review). Subsamples of soup for Hg speciation analysis were collected in 50-mL polypropylene centrifuge tubes that were cleaned with a rigorous technique suitable for trace-level Hg analysis (Hammerschmidt et al., 2011). 2.2. MMHg analysis Dried, unprocessed fin samples (0.05–0.3 g dry wt.) were freeze dried and broken into pieces by hand while inside zip-type plastic bags and weighed into 15-mL centrifuge tubes containing 7 mL of 4.57 M HNO3 (Hammerschmidt and Fitzgerald, 2006). Soup samples were shipped frozen to Wright State University, where soup was thawed and homogenized in a stainless steel blender cleaned with detergent and rinsed with reagent-grade water (resistivity ≥ 18 MΩ·cm). Separate aliquots of the homogenate were either freeze-dried for the analysis of carbon and nitrogen contents or digested with HNO3 (4.57 M final concentration) for MMHg determination. MMHg was measured by flow-injection gaschromatographic cold vapor atomic fluorescence spectrometry (CVAFS) after derivatization with sodium tetraethylborate (Bloom, 1989; Tseng et al., 2004). Quality assurance of MMHg determinations included analyses of procedural blanks and standards, procedural replicates, and certified
Fig. 1. MMHg is strongly related to total Hg in distal clips of dried shark fins: circle = blue shark (Prionace glauca), square = bull shark (Carcharhinus leucas), triangle up = copper shark (Carcharhinus brachyurus), triangle down = scalloped hammerhead (Sphyrna lewini), diamond = smooth hammerhead (Sphyrna zygaena), hexagon = shortfin mako (Isurus oxyrinchus).
reference materials from the National Research Council of Canada, lobster hepatopancreas (TORT-2) and fish protein (DORM-3). Standard solutions of MMHg were calibrated using a Hg(II) solution traceable to the U.S. National Institute of Standards and Technology (NIST). All measurements of MMHg in DORM-3 (n = 27 samples) and all but one measurement of TORT-2 (n = 30) were within the certified ranges. The mean (± 1SD) measured concentration of MMHg in DORM-3 was 329 ± 21 ng/g dry wt. (certified range = 299–411 ng/g) and that in TORT-2 was 150 ± 7 ng/g (certified range = 139–165 ng/g). Imprecision of MMHg analyses between procedural duplicates of soup averaged 7.7 relative percent difference (n = 7). The estimated detection limit for MMHg was ~ 0.01 ng/mL in soup and 0.02 ng/g for a 0.1-g sample of dried fin. 2.3. Total Hg analysis The 4.57 M HNO3 digestates of all soup samples and 18 of the fins also were used to quantify total Hg. Aliquots of the digestates were oxidized with BrCl for 12 h prior to the addition of NH2OH (Hammerschmidt and Fitzgerald, 2006). Sample Hg was reduced with SnCl2 and quantified by dual-Au amalgamation CVAFS (Fitzgerald and Gill, 1979; Bloom and Fitzgerald, 1988). Total Hg determinations were calibrated with aqueous Hg(II) solutions traceable to the U. S. NIST. All measurements of DORM-3 (n = 22) and TORT-2 (n = 28) were within the certified ranges: Total Hg in DORM-3 averaged 362 ± 12 ng/g (certified range = 322–442 ng/g) and that in TORT-2 averaged 271 ± 12 ng/g (certified range = 210–330 ng/g). Recovery of known Hg(II) additions averaged 101% (n = 7), and imprecision among procedural replicates
Table 1 Mean ±1SD concentration of monomethylmercury (MMHg) in distal fin clips of shark genera examined in this study. Ranges are given in parentheses. Scientific name
Common name
n
MMHg (ng/g dry wt.)
Carcharhinus plumbeus Alopias vulpinus Sphyrna zygaena Carcharhinus leucas Carcharhinus brevipinna Carcharhinus obscurus Carcharodon carcharias Prionace glauca Isurus oxyrinchus Carcharhinus longimanus Sphyrna mokarran Carcharhinus brachyurus Sphyrna lewini
Sandbar shark Common thresher Smooth hammerhead Bull shark Spinner shark Dusky shark Great white Blue shark Shortfin mako shark Oceanic whitetip Great hammerhead Copper shark Scalloped hammerhead
5 6 3 3 4 6 4 6 3 2 2 2 4
38 ± 16 (13–55) 87 ± 82 (9–239) 101 ± 52 (42–140) 111 ± 51 (74–170) 112 ± 72 (11–173) 158 ± 66 (39–230) 179 ± 146 (83–396) 247 ± 277 (19–763) 267 ± 97 (169–362) 299 (67–530) 337 (301–372) 432 (222–642) 869 ± 639 (214–1720)
Fig. 2. Relationship between MMHg and total Hg in shark fin soup.
Please cite this article as: Nalluri D, et al, Methylmercury in dried shark fins and shark fin soup from American restaurants, Sci Total Environ (2014), http://dx.doi.org/10.1016/j.scitotenv.2014.04.107
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Table 2 Genera of shark and summary statistics of monomethylmercury (MMHg) concentrations determined in samples of shark fin soup from 50 U.S. restaurants. Scientific name
Common name
n
MMHg (ng/mL) Mean
Prionace glauca Galeorhinus galeus Squalus acanthias Sphyrna zygaena Sphyrna lewini Carcharhinus leucas Carcharhinus sp. Carcharhinus brachyurus Isurus oxyrinchus Genetic testing inconclusive a
Blue shark School shark Spiny dogfish Smooth hammerhead Scalloped hammerhead Bull shark – Copper shark Shortfin mako sharka –
14 4 1 1 1 2 7 1 2 17
4.59 1.17 1.62 28.3 13.6 9.78 0.59 5.20 0.17 4.84
SD
Median
Range
6.40 1.35
2.15 0.77
0.15–24.0 0.04–3.12
12.06 0.69
9.78 0.29
1.25–18.3 0.02–1.69
8.33
2.04
0.01–33.9
Only one sample of the two that contained the DNA of shortfin mako shark was analyzed for MMHg.
averaged 3.4 relative percent difference (n = 5). The estimated detection limit for total Hg was approximately 0.03 ng/mL for soup and 1.5 ng/g for a 0.1-g sample of dried fin. 2.4. Soup physicochemistry As Hg binds to organic matter, most particularly protein in living organisms, soup samples were analyzed for nitrogen and carbon as proxies for the relative protein and organic contents, respectively. Water content was determined by the mass loss after freeze drying. Residual dried solids were homogenized by pulverization and analyzed for mass normalized C and N concentrations. For carbon and nitrogen determinations, ~5 mg of powder was placed inside tin capsules (5 × 9 mm), and analyzed with a CHN analyzer. Sulfanilamide was used for calibration standards. 2.5. Statistical analyses Statistical analyses, which are described in sections below, were performed with SigmaPlot 12.3 software. Nonparametric tests were used when the data were either not distributed normally or of equal variance. Statistical significance was assessed with an α value of 0.05. 3. Results and discussion 3.1. Hg speciation in dried, unprocessed shark fins MMHg concentrations were strongly correlated to those of total Hg in shark fins (Fig. 1). Concentrations of MMHg ranged over 2 orders of magnitude, from 9 to 1720 ng/g dry wt. (Table 1), and were significantly different among species of shark (Kruskal–Wallis test, p = 0.02), with fins from scalloped hammerheads (Sphyrna lewini) having greater MMHg levels than those of sandbar sharks (Carcharhinus plumbeus; Dunn's pairwise comparison, p b 0.05); pairwise tests between other
species were not significantly different. The mean (± SD) fraction of total Hg as MMHg in fin clips was 67 ± 22%, which is less than typically observed in shark muscle (~90%; Storelli et al., 2003; Branco et al., 2007). The wide range of MMHg concentrations among and within each shark species may reflect differences in individual age, size, population of origin, diet and trophic level that contribute to variable MMHg bioaccumulation (de Pinho et al., 2002). For example, the fins from the smooth hammerhead sharks (Sphyrna zygaena) came from individuals b120 cm total length and had low MMHg concentrations compared to larger scalloped hammerheads (S. lewini) sampled from the same location (Durban, South Africa). 3.2. Hg in shark fin soup MMHg concentrations in shark fin soup ranged from b0.01 to 34 ng/mL with a median value of 1.4 ng/mL (Table S1). In general, concentrations of MMHg were proportional to total Hg in soup (Fig. 2), although the fraction of total Hg as MMHg was highly variable among individual samples, ranging from 7 to 118%. The mean fraction of total Hg as MMHg was 62 ± 7%, a ratio similar to that found in dried fins (67 ± 22%). Of the soups containing shark identified to either species or genus level, the sample size was too small (e.g., n = 1 for spiny dogfish, smooth hammerhead, scalloped hammerhead or copper shark) for meaningful determination of differences in MMHg concentration between species (Fields et al., in review). Soup identified as being from smooth hammerhead, scalloped hammerhead, and bull sharks (Carcharhinus leucas) contained the highest MMHg concentrations, although only one or two samples were positively identified for each species (Table 2). Hammerhead and bull sharks tend to occupy high trophic levels, and previous studies have shown that hammerhead shark flesh, in particular, has high concentrations of Hg (Karimi et al., 2012). Dried fins from scalloped hammerheads contained the highest MMHg concentrations (869 ± 639 ng/g dry wt.; Table 1) of all sharks examined in this study.
Fig. 3. Spearman rank-order correlations of MMHg (A) and total Hg (B) concentrations with the nitrogen content of dried solids in shark fin soup.
Please cite this article as: Nalluri D, et al, Methylmercury in dried shark fins and shark fin soup from American restaurants, Sci Total Environ (2014), http://dx.doi.org/10.1016/j.scitotenv.2014.04.107
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Mercury content of shark fin soup was influenced by the chemical and physical compositions. MMHg and total Hg concentrations were positively correlated with the nitrogen content of dried soup (Fig. 3), but not with carbon content (p-values N 0.37). MMHg complexes with thiols in fish protein (Harris et al., 2003), the relative amount of which is indicated by nitrogen content. Accordingly, the positive relationships between both total Hg and MMHg with nitrogen suggest that both forms of Hg were derived from ceratotrichia that are composed of the proteins collagen and elastin. While the nitrogen content (1–12%) of soup is presumed to be largely a function of the amount of fin used to prepare it, the variability in these modest correlations may result from differences in the Hg/N ratios among fins used to prepare the soup, amount of fins, and other ingredients that can include chicken, chicken broth, vegetables (i.e. bamboo shoots, and mushrooms), soy sauce, and oil. Given that the N content of shark fins is relatively constant within and among species (~14%; Jayasinghe et al., 1998), high variability of Hg/N ratios in fish would be expected given the two orders of magnitude range in total Hg and MMHg concentrations that we observed among dried fins (Fig. 1). The fraction of total Hg as MMHg was inversely correlated with the fraction of dry solids among soup samples (Fig. 4), suggesting that non-protein solids contributed relatively more Hg(II) than MMHg to the soup (Fig. 4). While MMHg preferentially accumulates, as opposed to Hg(II) in shark protein (Storelli et al., 2003; Branco et al., 2007), including fins (Fig. 1), Hg(II) is the dominant Hg species in many nonfish food items, such as grains and vegetables (U.S. EPA, 1997). Therefore, the addition of ingredients other than fish to the soup (i.e., greater C/N ratio) may explain the observed decrease in the fraction of total Hg as MMHg because they contribute more Hg(II) than MMHg. 3.3. Potential human health risk from MMHg exposure We evaluated the potential for increased health risk emerging from human consumption of MMHg in shark fin soup. The greatest human concern with MMHg is neurotoxicity from maternal transfer to developing fetuses (Karagas et al., 2012). The U.S. Environmental Protection Agency (U.S. EPA) has established a reference dose (RfD) of 0.1 μg MMHg per kg of human body weight per day as an exposure limit intended to reduce the risk of potential deleterious effects during a lifetime (Rice et al., 2003). This equates to a dose of 7.4 μg of MMHg per day for a 74-kg human, the average weight of adult American females (McDowell et al., 2008). Given a standard serving volume of 240 mL (8 oz) of soup, we estimated a dose of 1.1 μg of MMHg from our mean measured concentration of MMHg in shark fin soup (4.6 ng/mL). Similarly, consumption of soup containing the greatest concentration (34 ng/mL) would result in a dose of 8.2 μg of MMHg. MMHg exposures from both the average and high concentration soups are either less than or comparable to the U.S. EPA RfD for the average American female.
Fig. 4. Fraction of total Hg as MMHg was correlated inversely with the solid content of shark fin soup.
However, shark fin soup is often consumed as an appetizer dish. Therefore, consumption of shark fin soup with additional fish products that contain MMHg may result in a dose that exceeds the RfD. For example, consumption of a 200 g (7 oz) steak of either blue shark or albacore tuna, containing from 180 to 1950 ng/g or 1060 ng/g wet wt., respectively, of organic Hg as MMHg (Branco et al., 2007; Storelli et al., 2002, 2003), results in a dose of 36–390 and 212 μg of MMHg, respectively. Accordingly, and while shark fin soup represents a potentially significant source of MMHg to human consumers, other seafood products contain much higher MMHg concentrations and can result in substantially greater exposures to the contaminant. 4. Conclusions We found that MMHg occurs at detectable levels in both dried, unprocessed shark fins and in commercially prepared shark fin soup. There was considerable variation of MMHg concentrations within and, in some cases, between the shark species we examined. Greater concentrations of MMHg were found in shark fin soup prepared with fins from sharks that are at higher trophic levels (e.g., bull shark and hammerheads). Conversely, MMHg concentrations were less in soups containing either a relatively small amount of shark fin or shark species occupying a relatively lower trophic level. Yet, estimated human exposures to MMHg from consumption of shark fin soup are less in comparison to those from eating the meat of apex marine fishes. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2014.04.107. Conflict of interest None of the authors have any conflicts of interest. Acknowledgments We thank D. Hirschberg, C.-S. Lee, M. Bond and J. Klaus for the laboratory assistance. We kindly thank M. Sexauer Gustin for helpful comments and suggestions. The Pew Charitable Trust provided shark fin soup samples. This research was supported by The Gelfond Fund for Mercury Research. References Bloom N. Determination of picogram levels of methylmercury by aqueous phase ethylation, followed by cryogenic gas chromatography with cold vapour atomic fluorescence detection. Can J Fish Aquat Sci 1989;46:1131–40. Bloom NS. On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 1992;49:1010–7. Bloom NS, Fitzgerald WF. Determination of volatile mercury species at the picogram level by low-temperature gas chromatography with cold-vapor atomic fluorescence detection. Anal Chim Acta 1988;208:151–61. Branco V, Vale C, Canário J, dos Santos MN. Mercury and selenium in blue shark (Prionace glauca, L. 1758) and swordfish (Xiphias gladius, L. 1758) from two areas of the Atlantic Ocean. Environ Pollut 2007;150:373–80. de Pinho AP, Guimarães JRD, Martins AS, Costa PAS, Olavo G, Valentin J. Total mercury in muscle tissue of five shark species from Brazilian offshore waters: effects of feeding habit, sex, and length. Environ Res 2002;89:250–8. Fields AT, Abercrombie DL, Eng R, Feldheim K, Chapman DD. A novel mini-DNA barcoding assay to identify processed fins from internationally protected shark species; 2014 [in review]. Fitzgerald WF, Clarkson TW. Mercury and monomethylmercury: present and future concerns. Environ Health Perspect 1991;96:159–66. Fitzgerald WF, Gill GA. Subnanogram determination of mercury by two-stage gold amalgamation applied to atmospheric analysis. Anal Chem 1979;51:1714–20. Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K, et al. Cognitive deficit in 7year-old children with prenatal exposure to methylmercury. Neurotoxicol Teratol 1997;19:417–28. Hammerschmidt CR, Bowman KL, Tabatchnick MD, Lamborg CH. Storage bottle material and cleaning for determination of total mercury in seawater. Limnol Oceanogr Methods 2011;9:426–31. Hammerschmidt CR, Fitzgerald WF. Bioaccumulation and trophic transfer of methylmercury in Long Island Sound. Arch Environ Contam Toxicol 2006;51:416–24. Harris HH, Pickering IJ, George GN. The chemical form of mercury in fish. Science 2003; 301:1203.
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Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Methylmercury in dried shark fins and shark fin soup from American restaurants Deepthi Nalluri a, Zofia Baumann b,⁎, Debra L. Abercrombie c, Demian D. Chapman c, Chad R. Hammerschmidt a, Nicholas S. Fisher c a b c
Department of Earth & Environmental Sciences, Wright State University, Dayton, OH 45435, United States Department of Marine Sciences, University of Connecticut, Avery Point, Groton, CT 06340, United States School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, United States
H I G H L I G H T S • Concentrations of monomethylmercury (MMHg) in fins and soup varied among shark species. • MMHg was highest in fins and soup from large, high trophic level sharks. • Estimated human exposures to MMHg from shark fin soup are relatively low.
a r t i c l e
i n f o
Article history: Received 13 February 2014 Received in revised form 24 April 2014 Accepted 25 April 2014 Available online xxxx Editor: Mae Sexauer Gustin Keywords: Shark fin soup Mercury Public health Food
a b s t r a c t Consumption of meat from large predatory sharks exposes human consumers to high levels of toxic monomethylmercury (MMHg). There also have been claims that shark fins, and hence the Asian delicacy shark fin soup, contain harmful levels of neurotoxic chemicals in combination with MMHg, although concentrations of MMHg in shark fins are unknown. We measured MMHg in dried, unprocessed fins (n = 50) of 13 shark species that occur in the international trade of dried shark fins as well as 50 samples of shark fin soup prepared by restaurants from around the United States. Concentrations of MMHg in fins ranged from 9 to 1720 ng/g dry wt. MMHg in shark fin soup ranged from b0.01 to 34 ng/mL, with MMHg averaging 62 ± 7% of total Hg. The highest concentrations of MMHg and total Hg were observed in both fins and soup from large, high trophic level sharks such as hammerheads (Sphyrna spp.). Consumption of a 240 mL bowl of shark fin soup containing the average concentration of MMHg (4.6 ng/mL) would result in a dose of 1.1 μg MMHg, which is 16% of the U.S. EPA's reference dose (0.1 μg MMHg per 1 kg per day in adults) of 7.4 μg per day for a 74 kg person. If consumed, the soup containing the highest measured MMHg concentration would exceed the reference dose by 17%. While shark fin soup represents a potentially important source of MMHg to human consumers, other seafood products, particularly the flesh of apex marine predators, contain much higher MMHg concentrations and can result in substantially greater exposures of this contaminant for people. © 2014 Published by Elsevier B.V.
1. Introduction Many marine apex predators contain high concentrations of mercury (Hg) and are potential sources of this contaminant for humans (Fitzgerald and Clarkson, 1991). Monomethylmercury (MMHg), as opposed to complexes of inorganic Hg, is the toxic form of Hg bioaccumulated by fish (Bloom, 1992). Shark muscle, for example, can contain concentrations of MMHg (~0.5–50 μg/g wet weight; Hornung et al., 1993; Storelli et al., 2003) that are far greater than the recommended human consumption advisory limit for MMHg in fish (0.3 μg/g; U.S. EPA, 2001). In addition to neurotoxicity, effects of MMHg may include increased risk of ⁎ Corresponding author. Tel.: +1 631 632 8697; fax: +1 631 632 3072. E-mail address: zofi[email protected] (Z. Baumann).
cardiovascular disease in adults who eat fish (Salonen et al., 1995; Karagas et al., 2012). Moreover, maternal transfer of MMHg to prenatal life stages can inhibit the neurological and cardiovascular development and growth of some children (Grandjean et al., 1997; Murata et al., 1999; Sorenson et al., 1999; Steuerwald et al., 2000; Karagas et al., 2012). Although it is well established that shark meat contains high values of Hg, less is known about concentrations in other shark body parts that are consumed by humans. Dried shark fins are among the most highly traded and consumed shark parts in the world. They are used to make the Asian delicacy - shark fin soup, a luxury dish that is often served as an appetizer. This expensive delicacy consists mostly of ceratotrichia (or “fin needles”; elastin and collagen fibers that resemble rice noodles when cooked) served with either chicken broth or another stock for flavor (Rose, 1996). Recent claims have been made that shark fin soup can
http://dx.doi.org/10.1016/j.scitotenv.2014.04.107 0048-9697/© 2014 Published by Elsevier B.V.
Please cite this article as: Nalluri D, et al, Methylmercury in dried shark fins and shark fin soup from American restaurants, Sci Total Environ (2014), http://dx.doi.org/10.1016/j.scitotenv.2014.04.107
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contain elevated levels of contaminants, potentially putting consumers at risk (Holtcamp, 2012; Mondo et al., 2012). To date, however, there are no published studies documenting Hg concentrations in either shark fins or shark fin soup. Our objective was to examine concentrations of total Hg and MMHg in dried unprocessed shark fins from wild captured animals, and shark fin soup, offered for retail sale in the United States, and evaluate potential health risk to human consumers. 2. Materials and methods 2.1. Samples All samples were collected using standard clean procedures for Hg analysis. Whole, dried unprocessed shark fins examined in this study were collected from wild-captured specimens taken from fisheries of the United States, Sri Lanka, Fiji, and South Africa as part of a separate study. All fins were sun-dried. Fins were stored at Stony Brook University in separate plastic bags at room temperature for 12 to 18 months prior to sampling. A small piece (~10 mm × 10 mm) of the distal portion of each fin was analyzed for Hg content. Fins originated from one of 13 shark species, all of which are known to occur in the international dried fin trade (Table 1). Bowls of shark fin soup were purchased for Hg analysis from 50 restaurants located throughout the United States by volunteers in March and April 2012 (Table S1). Either species or genus of origin of the fin used to make each bowl of soup was assessed using a mini-DNA barcode protocol on a single, randomly selected fin needle taken from each bowl (Fields et al., in review). Subsamples of soup for Hg speciation analysis were collected in 50-mL polypropylene centrifuge tubes that were cleaned with a rigorous technique suitable for trace-level Hg analysis (Hammerschmidt et al., 2011). 2.2. MMHg analysis Dried, unprocessed fin samples (0.05–0.3 g dry wt.) were freeze dried and broken into pieces by hand while inside zip-type plastic bags and weighed into 15-mL centrifuge tubes containing 7 mL of 4.57 M HNO3 (Hammerschmidt and Fitzgerald, 2006). Soup samples were shipped frozen to Wright State University, where soup was thawed and homogenized in a stainless steel blender cleaned with detergent and rinsed with reagent-grade water (resistivity ≥ 18 MΩ·cm). Separate aliquots of the homogenate were either freeze-dried for the analysis of carbon and nitrogen contents or digested with HNO3 (4.57 M final concentration) for MMHg determination. MMHg was measured by flow-injection gaschromatographic cold vapor atomic fluorescence spectrometry (CVAFS) after derivatization with sodium tetraethylborate (Bloom, 1989; Tseng et al., 2004). Quality assurance of MMHg determinations included analyses of procedural blanks and standards, procedural replicates, and certified
Fig. 1. MMHg is strongly related to total Hg in distal clips of dried shark fins: circle = blue shark (Prionace glauca), square = bull shark (Carcharhinus leucas), triangle up = copper shark (Carcharhinus brachyurus), triangle down = scalloped hammerhead (Sphyrna lewini), diamond = smooth hammerhead (Sphyrna zygaena), hexagon = shortfin mako (Isurus oxyrinchus).
reference materials from the National Research Council of Canada, lobster hepatopancreas (TORT-2) and fish protein (DORM-3). Standard solutions of MMHg were calibrated using a Hg(II) solution traceable to the U.S. National Institute of Standards and Technology (NIST). All measurements of MMHg in DORM-3 (n = 27 samples) and all but one measurement of TORT-2 (n = 30) were within the certified ranges. The mean (± 1SD) measured concentration of MMHg in DORM-3 was 329 ± 21 ng/g dry wt. (certified range = 299–411 ng/g) and that in TORT-2 was 150 ± 7 ng/g (certified range = 139–165 ng/g). Imprecision of MMHg analyses between procedural duplicates of soup averaged 7.7 relative percent difference (n = 7). The estimated detection limit for MMHg was ~ 0.01 ng/mL in soup and 0.02 ng/g for a 0.1-g sample of dried fin. 2.3. Total Hg analysis The 4.57 M HNO3 digestates of all soup samples and 18 of the fins also were used to quantify total Hg. Aliquots of the digestates were oxidized with BrCl for 12 h prior to the addition of NH2OH (Hammerschmidt and Fitzgerald, 2006). Sample Hg was reduced with SnCl2 and quantified by dual-Au amalgamation CVAFS (Fitzgerald and Gill, 1979; Bloom and Fitzgerald, 1988). Total Hg determinations were calibrated with aqueous Hg(II) solutions traceable to the U. S. NIST. All measurements of DORM-3 (n = 22) and TORT-2 (n = 28) were within the certified ranges: Total Hg in DORM-3 averaged 362 ± 12 ng/g (certified range = 322–442 ng/g) and that in TORT-2 averaged 271 ± 12 ng/g (certified range = 210–330 ng/g). Recovery of known Hg(II) additions averaged 101% (n = 7), and imprecision among procedural replicates
Table 1 Mean ±1SD concentration of monomethylmercury (MMHg) in distal fin clips of shark genera examined in this study. Ranges are given in parentheses. Scientific name
Common name
n
MMHg (ng/g dry wt.)
Carcharhinus plumbeus Alopias vulpinus Sphyrna zygaena Carcharhinus leucas Carcharhinus brevipinna Carcharhinus obscurus Carcharodon carcharias Prionace glauca Isurus oxyrinchus Carcharhinus longimanus Sphyrna mokarran Carcharhinus brachyurus Sphyrna lewini
Sandbar shark Common thresher Smooth hammerhead Bull shark Spinner shark Dusky shark Great white Blue shark Shortfin mako shark Oceanic whitetip Great hammerhead Copper shark Scalloped hammerhead
5 6 3 3 4 6 4 6 3 2 2 2 4
38 ± 16 (13–55) 87 ± 82 (9–239) 101 ± 52 (42–140) 111 ± 51 (74–170) 112 ± 72 (11–173) 158 ± 66 (39–230) 179 ± 146 (83–396) 247 ± 277 (19–763) 267 ± 97 (169–362) 299 (67–530) 337 (301–372) 432 (222–642) 869 ± 639 (214–1720)
Fig. 2. Relationship between MMHg and total Hg in shark fin soup.
Please cite this article as: Nalluri D, et al, Methylmercury in dried shark fins and shark fin soup from American restaurants, Sci Total Environ (2014), http://dx.doi.org/10.1016/j.scitotenv.2014.04.107
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Table 2 Genera of shark and summary statistics of monomethylmercury (MMHg) concentrations determined in samples of shark fin soup from 50 U.S. restaurants. Scientific name
Common name
n
MMHg (ng/mL) Mean
Prionace glauca Galeorhinus galeus Squalus acanthias Sphyrna zygaena Sphyrna lewini Carcharhinus leucas Carcharhinus sp. Carcharhinus brachyurus Isurus oxyrinchus Genetic testing inconclusive a
Blue shark School shark Spiny dogfish Smooth hammerhead Scalloped hammerhead Bull shark – Copper shark Shortfin mako sharka –
14 4 1 1 1 2 7 1 2 17
4.59 1.17 1.62 28.3 13.6 9.78 0.59 5.20 0.17 4.84
SD
Median
Range
6.40 1.35
2.15 0.77
0.15–24.0 0.04–3.12
12.06 0.69
9.78 0.29
1.25–18.3 0.02–1.69
8.33
2.04
0.01–33.9
Only one sample of the two that contained the DNA of shortfin mako shark was analyzed for MMHg.
averaged 3.4 relative percent difference (n = 5). The estimated detection limit for total Hg was approximately 0.03 ng/mL for soup and 1.5 ng/g for a 0.1-g sample of dried fin. 2.4. Soup physicochemistry As Hg binds to organic matter, most particularly protein in living organisms, soup samples were analyzed for nitrogen and carbon as proxies for the relative protein and organic contents, respectively. Water content was determined by the mass loss after freeze drying. Residual dried solids were homogenized by pulverization and analyzed for mass normalized C and N concentrations. For carbon and nitrogen determinations, ~5 mg of powder was placed inside tin capsules (5 × 9 mm), and analyzed with a CHN analyzer. Sulfanilamide was used for calibration standards. 2.5. Statistical analyses Statistical analyses, which are described in sections below, were performed with SigmaPlot 12.3 software. Nonparametric tests were used when the data were either not distributed normally or of equal variance. Statistical significance was assessed with an α value of 0.05. 3. Results and discussion 3.1. Hg speciation in dried, unprocessed shark fins MMHg concentrations were strongly correlated to those of total Hg in shark fins (Fig. 1). Concentrations of MMHg ranged over 2 orders of magnitude, from 9 to 1720 ng/g dry wt. (Table 1), and were significantly different among species of shark (Kruskal–Wallis test, p = 0.02), with fins from scalloped hammerheads (Sphyrna lewini) having greater MMHg levels than those of sandbar sharks (Carcharhinus plumbeus; Dunn's pairwise comparison, p b 0.05); pairwise tests between other
species were not significantly different. The mean (± SD) fraction of total Hg as MMHg in fin clips was 67 ± 22%, which is less than typically observed in shark muscle (~90%; Storelli et al., 2003; Branco et al., 2007). The wide range of MMHg concentrations among and within each shark species may reflect differences in individual age, size, population of origin, diet and trophic level that contribute to variable MMHg bioaccumulation (de Pinho et al., 2002). For example, the fins from the smooth hammerhead sharks (Sphyrna zygaena) came from individuals b120 cm total length and had low MMHg concentrations compared to larger scalloped hammerheads (S. lewini) sampled from the same location (Durban, South Africa). 3.2. Hg in shark fin soup MMHg concentrations in shark fin soup ranged from b0.01 to 34 ng/mL with a median value of 1.4 ng/mL (Table S1). In general, concentrations of MMHg were proportional to total Hg in soup (Fig. 2), although the fraction of total Hg as MMHg was highly variable among individual samples, ranging from 7 to 118%. The mean fraction of total Hg as MMHg was 62 ± 7%, a ratio similar to that found in dried fins (67 ± 22%). Of the soups containing shark identified to either species or genus level, the sample size was too small (e.g., n = 1 for spiny dogfish, smooth hammerhead, scalloped hammerhead or copper shark) for meaningful determination of differences in MMHg concentration between species (Fields et al., in review). Soup identified as being from smooth hammerhead, scalloped hammerhead, and bull sharks (Carcharhinus leucas) contained the highest MMHg concentrations, although only one or two samples were positively identified for each species (Table 2). Hammerhead and bull sharks tend to occupy high trophic levels, and previous studies have shown that hammerhead shark flesh, in particular, has high concentrations of Hg (Karimi et al., 2012). Dried fins from scalloped hammerheads contained the highest MMHg concentrations (869 ± 639 ng/g dry wt.; Table 1) of all sharks examined in this study.
Fig. 3. Spearman rank-order correlations of MMHg (A) and total Hg (B) concentrations with the nitrogen content of dried solids in shark fin soup.
Please cite this article as: Nalluri D, et al, Methylmercury in dried shark fins and shark fin soup from American restaurants, Sci Total Environ (2014), http://dx.doi.org/10.1016/j.scitotenv.2014.04.107
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Mercury content of shark fin soup was influenced by the chemical and physical compositions. MMHg and total Hg concentrations were positively correlated with the nitrogen content of dried soup (Fig. 3), but not with carbon content (p-values N 0.37). MMHg complexes with thiols in fish protein (Harris et al., 2003), the relative amount of which is indicated by nitrogen content. Accordingly, the positive relationships between both total Hg and MMHg with nitrogen suggest that both forms of Hg were derived from ceratotrichia that are composed of the proteins collagen and elastin. While the nitrogen content (1–12%) of soup is presumed to be largely a function of the amount of fin used to prepare it, the variability in these modest correlations may result from differences in the Hg/N ratios among fins used to prepare the soup, amount of fins, and other ingredients that can include chicken, chicken broth, vegetables (i.e. bamboo shoots, and mushrooms), soy sauce, and oil. Given that the N content of shark fins is relatively constant within and among species (~14%; Jayasinghe et al., 1998), high variability of Hg/N ratios in fish would be expected given the two orders of magnitude range in total Hg and MMHg concentrations that we observed among dried fins (Fig. 1). The fraction of total Hg as MMHg was inversely correlated with the fraction of dry solids among soup samples (Fig. 4), suggesting that non-protein solids contributed relatively more Hg(II) than MMHg to the soup (Fig. 4). While MMHg preferentially accumulates, as opposed to Hg(II) in shark protein (Storelli et al., 2003; Branco et al., 2007), including fins (Fig. 1), Hg(II) is the dominant Hg species in many nonfish food items, such as grains and vegetables (U.S. EPA, 1997). Therefore, the addition of ingredients other than fish to the soup (i.e., greater C/N ratio) may explain the observed decrease in the fraction of total Hg as MMHg because they contribute more Hg(II) than MMHg. 3.3. Potential human health risk from MMHg exposure We evaluated the potential for increased health risk emerging from human consumption of MMHg in shark fin soup. The greatest human concern with MMHg is neurotoxicity from maternal transfer to developing fetuses (Karagas et al., 2012). The U.S. Environmental Protection Agency (U.S. EPA) has established a reference dose (RfD) of 0.1 μg MMHg per kg of human body weight per day as an exposure limit intended to reduce the risk of potential deleterious effects during a lifetime (Rice et al., 2003). This equates to a dose of 7.4 μg of MMHg per day for a 74-kg human, the average weight of adult American females (McDowell et al., 2008). Given a standard serving volume of 240 mL (8 oz) of soup, we estimated a dose of 1.1 μg of MMHg from our mean measured concentration of MMHg in shark fin soup (4.6 ng/mL). Similarly, consumption of soup containing the greatest concentration (34 ng/mL) would result in a dose of 8.2 μg of MMHg. MMHg exposures from both the average and high concentration soups are either less than or comparable to the U.S. EPA RfD for the average American female.
Fig. 4. Fraction of total Hg as MMHg was correlated inversely with the solid content of shark fin soup.
However, shark fin soup is often consumed as an appetizer dish. Therefore, consumption of shark fin soup with additional fish products that contain MMHg may result in a dose that exceeds the RfD. For example, consumption of a 200 g (7 oz) steak of either blue shark or albacore tuna, containing from 180 to 1950 ng/g or 1060 ng/g wet wt., respectively, of organic Hg as MMHg (Branco et al., 2007; Storelli et al., 2002, 2003), results in a dose of 36–390 and 212 μg of MMHg, respectively. Accordingly, and while shark fin soup represents a potentially significant source of MMHg to human consumers, other seafood products contain much higher MMHg concentrations and can result in substantially greater exposures to the contaminant. 4. Conclusions We found that MMHg occurs at detectable levels in both dried, unprocessed shark fins and in commercially prepared shark fin soup. There was considerable variation of MMHg concentrations within and, in some cases, between the shark species we examined. Greater concentrations of MMHg were found in shark fin soup prepared with fins from sharks that are at higher trophic levels (e.g., bull shark and hammerheads). Conversely, MMHg concentrations were less in soups containing either a relatively small amount of shark fin or shark species occupying a relatively lower trophic level. Yet, estimated human exposures to MMHg from consumption of shark fin soup are less in comparison to those from eating the meat of apex marine fishes. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2014.04.107. Conflict of interest None of the authors have any conflicts of interest. Acknowledgments We thank D. Hirschberg, C.-S. Lee, M. Bond and J. Klaus for the laboratory assistance. We kindly thank M. Sexauer Gustin for helpful comments and suggestions. The Pew Charitable Trust provided shark fin soup samples. This research was supported by The Gelfond Fund for Mercury Research. References Bloom N. Determination of picogram levels of methylmercury by aqueous phase ethylation, followed by cryogenic gas chromatography with cold vapour atomic fluorescence detection. Can J Fish Aquat Sci 1989;46:1131–40. Bloom NS. On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 1992;49:1010–7. Bloom NS, Fitzgerald WF. Determination of volatile mercury species at the picogram level by low-temperature gas chromatography with cold-vapor atomic fluorescence detection. Anal Chim Acta 1988;208:151–61. Branco V, Vale C, Canário J, dos Santos MN. Mercury and selenium in blue shark (Prionace glauca, L. 1758) and swordfish (Xiphias gladius, L. 1758) from two areas of the Atlantic Ocean. Environ Pollut 2007;150:373–80. de Pinho AP, Guimarães JRD, Martins AS, Costa PAS, Olavo G, Valentin J. Total mercury in muscle tissue of five shark species from Brazilian offshore waters: effects of feeding habit, sex, and length. Environ Res 2002;89:250–8. Fields AT, Abercrombie DL, Eng R, Feldheim K, Chapman DD. A novel mini-DNA barcoding assay to identify processed fins from internationally protected shark species; 2014 [in review]. Fitzgerald WF, Clarkson TW. Mercury and monomethylmercury: present and future concerns. Environ Health Perspect 1991;96:159–66. Fitzgerald WF, Gill GA. Subnanogram determination of mercury by two-stage gold amalgamation applied to atmospheric analysis. Anal Chem 1979;51:1714–20. Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K, et al. Cognitive deficit in 7year-old children with prenatal exposure to methylmercury. Neurotoxicol Teratol 1997;19:417–28. Hammerschmidt CR, Bowman KL, Tabatchnick MD, Lamborg CH. Storage bottle material and cleaning for determination of total mercury in seawater. Limnol Oceanogr Methods 2011;9:426–31. Hammerschmidt CR, Fitzgerald WF. Bioaccumulation and trophic transfer of methylmercury in Long Island Sound. Arch Environ Contam Toxicol 2006;51:416–24. Harris HH, Pickering IJ, George GN. The chemical form of mercury in fish. Science 2003; 301:1203.
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