Marine Pollution Bulletin 102 (2016) 199–205
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Mercury concentrations in Northwest Atlantic winter-caught, male spiny dogfish (Squalus acanthias): A geographic mercury comparison and risk-reward framework for human consumption Adam T. St. Gelais ⁎, Barry A. Costa-Pierce Department of Marine Sciences, Marine Science Center, University of New England, Biddeford, ME 04005, USA
a r t i c l e
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Article history: Received 7 November 2015 Received in revised form 3 December 2015 Accepted 10 December 2015 Available online 21 December 2015 Keywords: Spiny dogfish Mercury Northwest Atlantic ocean Consumption Risk
a b s t r a c t Mercury (Hg) contamination testing was conducted on winter-caught male spiny dogfish (Squalus acanthias) in southern New England and results compared to available data on Hg concentrations for this species. A limited risk-reward assessment for EPA (eicosapentanoic acid) and DHA (docosahexanoic acid) lipid concentrations of spiny dogfish was completed in comparison with other commonly consumed marine fish. Mean Hg concentrations were 0.19 ppm (±0.30) wet weight. In comparison, mean Hg concentrations in S. acanthias varied geographically ranging from 0.05 ppm (Celtic Sea) to 2.07 ppm (Crete, Mediterranean Sea). A risk-reward assessment for Hg and DHA + EPA placed S. acanthias in both “low-risk, high-reward” and “high-risk, highreward” categories for consumption dependent on locations of the catch. Our results are limited and are not intended as consumption advisories but serve to illustrate the need for making more nuanced, geo-specific, consumption guidance for spiny dogfish that is inclusive of seafood traceability and nutritional benefits. © 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction Spiny dogfish (Squalus acanthias) are small, long-lived shark species found pan-globally in temperate coastal waters with a Northwest Atlantic distribution from Greenland to Florida. They have long been considered a benthic species with a “K” selected life history (i.e. slow growth, late maturity, lengthy gestation period). Females grow more rapidly and are larger than males and thus comprise a majority of fishery landings. From 1987 to 1996, landings of spiny dogfish in the USA increased nearly 10-fold as fishermen targeted larger female dogfish. The disproportionate removal of mature females led to a significant decline in the dogfish population, and its estimated spawning stock biomass (SSB) fell from about 234,000 MT in 1991 to 52,000 MT by 1999 (NEFSC, 1998, 2003; ASMFC, 2009; TRAC, 2010; MAFMC and NEFMC, 1999). A stock rebuilding plan with a 1814 MT annual quota and reduced possession limits for vessels fishing in US federal waters was established in 2000 with the aim to increase the SSB above 45,000 MT. Surprisingly large increases in SSB resulted; and the spiny dogfish stock was declared rebuilt in 2008. Catch limits were then raised in 2008 from 1814 MT to 18,506 MT in 2013 (ASMFC, 2008; MAFMC, 2012; Rago and Sosebee, 2012). There may be a much higher SSB in the NW Atlantic. In the USA, annual biomass estimates for spiny dogfish have been taken from multi⁎ Corresponding author. E-mail addresses:
[email protected] (A.T. St. Gelais),
[email protected] (B.A. Costa-Pierce).
species bottom trawl surveys (Carlson et al., 2014). However, Carlson et al. (2014) found that tag and bottom trawl data did not agree and suggested that spiny dogfish were present in large numbers not only as a benthic species but throughout the water column for at least some portion of the year. Thus, a large portion of the spiny dogfish population is most likely not sampled on an annual basis by bottom trawl surveys. Based upon these findings Sulikowski et al. (2010) estimated 230,000 MT of spawning dogfish – females of reproductive age – are in the Gulf of Maine. Carlson et al. (2014) found a 4:1 male to female ratio which means that the standing stock biomass of spiny dogfish in the Gulf of Maine may exceed 800,000 MT during the warmer times of year. This is compared with an estimated 10,000 MT of spawning stock biomass of Atlantic cod, a 23 to 1 imbalance. Recent research has shown that Georges Bank groundfish populations have shifted from predominantly gadids and flounders to mostly spiny dogfish, skates, and other small elasmobranchs (Fogarty and Murawski, 1998.) As spiny dogfish are apex predators this imbalance suggests that they could have a significant negative impact on New England groundfish species (NOAA, 2013). Studies have also reported dietary overlap (Fogarty and Murawski, 1998; Garrison and Link, 2000). Murawski and Idoine (1992) suggest that this diet overlap could hamper groundfish recovery as larger spiny dogfish ate more fish at a faster rate. Link et al. (2002) found a shift in spiny dogfish consumption from hake and sand lance in the 1970s and 1980s to herring in the 1990s. Recent ecosystem modeling has further illuminated the spiny dogfish's impacts (Smith and Link, 2010). Modeling has suggested that
http://dx.doi.org/10.1016/j.marpolbul.2015.12.009 0025-326X/© 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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the majority of groundfish species had decreased trophic levels between the 1990s and 2010s but the spiny dogfish's trophic level had increased. Model results indicate that the spiny dogfish have become a keystone species in New England with the highest prey overlap with Atlantic cod. Field investigations show that spiny dogfish eat substantial amounts of fish (Smith and Link, 2010). Stomach contents of adult female spiny dogfish indicate an index of relative importance of fish in the dogfish diet of over 80%. The main prey items were cod, sand lance, silver hake, and herring. Thus, spiny dogfish not only consume groundfish, they also competed with groundfish for prey. Given these findings the NW Atlantic spiny dogfish fishery may provide an outlet for contracting New England groundfish fleets and fishing communities and also help restore ecosystem balance. Fishery expansion would have important positive consequences for fishermen, fish processors, exporters, and consumers looking for a substitute for depleted groundfish. While spiny dogfish have been certified as sustainable by the Marine Stewardship Council (MSC), concerns over toxicants, principally mercury (Hg) contamination are constraining any an increase in landings of spiny dogfish and consumption. Taylor et al. (2014) reported that 32% of spiny dogfish exceeded the US EPA threshold level of 0.3 ppm (USEPA, 2000) wet weight and stated that “results indicate that frequent consumption of spiny dogfish may affect human health…”. Such findings have led to the rejection of spiny dogfish in domestic and international markets. Establishing consumer confidence and where needed contaminant consumption advisories are an extremely important issue for human health and wellness. However, there remain few comprehensive summaries and risk analyses of such mercury studies in this increasingly targeted species.
2. Why is Hg important? The biogeochemical cycle of Hg in the environment is well known. Hg enters the atmosphere as elemental mercury (Hg 0) is converted to mercuric-mercury (Hg2 +) then distributed via dry or wet deposition via dust and rain water (Clarkson and Magos, 2006). Sulfate-reducing bacteria in benthic sediments and water column microorganisms convert Hg2 + into Methlymercury, a neurotoxicant (Clarkson and Magos, 2006) which is biomagnified up aquatic food webs to predatory fish who thereby have the highest Methylmercury levels (Cladis et al., 2015). Regulatory agencies in the USA, Canada, and Europe have set guidelines for fish sold in commercial markets. Methylmercury is well recognized as a persistent inorganic pollutant whose concentrations have increased worldwide due to the acceleration of energy production (incineration of coal), the processing of metals, and waste combustion. Atmospheric deposition is the dominant source of Hg in most of the USA, especially in East Coast states that are “downwind” of the remaining coal-fired power stations in Midwestern states. As such, 40 states have issued advisories for Methylmercury, and 13 states have statewide advisories for some or all freshwater sportfish. Coastal areas in New England are also under advisories for Methylmercury for certain sport fish. In the USA, the Food and Drug Administration (FDA) regulates commercial seafood and has established an action level of 1 ppm total mercury for fish sold in commercial markets (USDA, 1994). However, some top trophic level species such as large swordfish contain upwards of 10 ppm of mercury and remain in commercial markets in the USA (Cladis et al., 2015). The US Environmental Protection Agency (US EPA), which does not regulate commercial seafood, has established a “reference dose” which is considered a safe limit of exposure to Hg of 0.1 μg/kg body weight/day. In Canada (Health Canada, 2012) and Europe (EC, 2005) the maximum Hg concentration for marketable seafood is 0.5 ppm. Concentrations of Hg in fish correlate strongly to species, age of fish, and location (Cladis et al., 2015).
3. Health characteristics There are very little data publicly available that identify the current health benefits and risks of NW Atlantic spiny dogfish. Seafood watch groups such as the Monterey Bay Seafood Watch and Blue Ocean Institute guides lack information about lesser known fisheries like dogfish. These groups bundle the testing of all sharks together and identify these groups as high risk to consumers. NOAA's FishWatch program and SeafoodSource.com provide some information, but it is unclear how and when this information was obtained. Neither provided a risk assessment that contains both positive (nutrients, lipids, minerals) and negative (toxins) aspects. The primary objective of this work was to conduct mercury testing of male spiny dogfish in one limited region of New England and compare results to other global data on S. acanthias, and to provide a limited risk assessment for Hg and lipid contents of these male spiny dogfish in comparison with other commonly consumed marine species. 4. Materials and methods A total of 57 mature male spiny dogfish were collected via a contracted commercial fishing vessel out of Point Judith, Rhode Island, USA. Fish were caught using a small mesh bottom trawl on a single tow within National Marine Fisheries Statistical Area 537 in Rhode Island Sound on 18 February 2015. Samples were kept whole, placed on ice, and stored for 24 h. After which they were transported to cold storage at the University of New England Marine Science Center in Biddeford, Maine, USA. Prior to processing, fish whole wet weight (g), total length (mm), gender, and maturity were recorded. Fish were then divided into discrete components: fillets (divided into proximal and distal portions), belly flaps, fins, and livers. Sample components were wrapped in foil, placed in sealed sample bags, catalogued, and stored frozen (−20 °C). For each fish collected a single filet sample from the left proximal portion of the fish was selected, thawed, and the skin was removed. Fish tissues were homogenized and samples were analyzed for total Hg and total solids within 24 h. Samples were analyzed at an EPA certified laboratory using EPA Method 245.6 (Lobring and Potter, 1991) for determination of Hg in tissues using cold vapor atomic absorption spectroscopy. Results were reported in both wet and dry weights. Total Hg was analyzed as this is the metric used for establishing consumption guidelines for fish and mercury in predator species is predominantly present in the form of Methylmercury. 5. Results and discussion Male spiny dogfish analyzed in this study were from 67.3 to 80.1 cm in size and contained a mean of 0.19 ppm wet weight of Hg (n = 57). These results are lower than reported by Taylor et al. (2014) (0.27 ppm) for the same region (Table 1). While the size ranges of fish analyzed here and by Taylor et al. (2014) were comparable, there were differences in the gender composition of fish analyzed. Our fish were 100% male, while the Taylor et al. (2014) fish were only 15% male. However, a previous study by Endo et al. (2009) found that there were no differences in Hg concentrations in same sized spiny dogfish by gender. Recent geospatial analyses of dogfish movements may explain these Hg differences, but they also complicate our fine-scale understanding of Hg in NW Atlantic S. acanthias. Telemetry studies suggest that spiny dogfish, which has been considered a homogeneous, panmictic NW Atlantic population, may be incorrect. Sulikowski et al. (2010) and Carlson et al. (2014) reported that spiny dogfish populations are comprised of distinct, highly mobile, and overlapping population segments consisting of a southern group with a mid-Atlantic residence, and northern group with its primary residence in the Gulf of Maine (GoM). The northern GoM group makes a southeast migration during the fall moving to the Georges Bank and Nantucket
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Table 1 Review of spiny dogfish (Squalus acanthias) total Hg concentrations by region. Regions
Length ranges
(n)
Genders
Hg (ppm) dry wt
Hg (ppm) wet wt
References
Atlantic, northeast (Celtic Sea) Atlantic, northwest (US, Narragansett) Atlantic, northwest (US, Narragansett) Atlantic, northwest (US, NY-ME) Mediterranean sea, eastern (Crete) Pacific, northeast (US, Oregon) Pacific, northeast (US, Puget Sound) Pacific, northwest (Japan) Southern Ocean (Southeast Australia)
60.0–66.0 67.3–80.1 50.0–80.1 66.0–99.0 43.0–72.0 65.0–108.6 60.0–117.0 50.5–131.1 77.0–85.0
6 57 124 25 47 88 141 75 10
Unknown Male Mixed Mixed Mixed Mixed Mixed Mixed Mixed
0.2 (±0.06) 0.71 (±0.60) 1.1 (±0.7) 1.8a 8.28a 2.408a 3.76a 1.4a 5.6a
0.05a 0.19 (±0.30) 0.275a 0.45b 2.07 (±1.17) 0.602 (±0.275) 0.94b 0.35b 1.4 (±0.4)
Domi et al., 2005 This study Taylor et al. (2014) Greig et al. (1977) Kousteni et al. (2006) Childs and Gaffke (1973) Hall et al. (1977) Endo et al. (2009) Pethybridge et al. (2010)
a b
Converted from reported wet or dry weight using 75% water content (Bosch et al. 2013). Calculated between multiple reported size ranges or pooled gender values reported separately for ease of comparison.
Shoals. Winter residence is split between the outer GoM and a portion overwintering south of the Nantucket Shoals continental shelf break in summer and autumn on Nantucket Shoals, southern Georges Bank, and Rhode Island Sound. Winter residence for this southern group shifts to the outer Albermarle Shelf Valley off the Chesapeake Bay and northern portions of the Outer Banks of North Carolina. The only period of temporal overlap between the two groups occurs in the fall. This may explain the lower mean total mercury reported for this study (0.19 ppm) than reported by Taylor et al. (2014) for the same region (0.27 ppm). The Taylor et al. (2014) spiny dogfish were collected between May and October, when the southern stock component was more likely to be in Rhode Island waters, while this study's samples were obtained in February, when our analyzed spiny dogfish were possibly derived from the GoM stock component in a potential region of overlap (Carlson et al., 2014). Hg exposure and accumulation in fish occurs via the diet (Hall et al., 1997), and the severity of bioaccumulation is directly linked to trophic status, prey preference, and habitat uses (Taylor et al., 2014). Hg in the marine environment and contamination within a species or species complex can be highly variable (Karimi et al., 2012). The prevalence of pathways by which Hg may enter the marine environment, and subsequently the food chain, varies by region, and the extent to which Hg biomagnifies through a food web or bioaccumulates in a given species is dependent on the abundance of and proximity to these pathways (Ullrich et al., 2001). Environmental Hg inputs are also not constant, and as emission regulations evolve they in many cases are in decline (Engstrom and Swain, 1997). Where environmental Hg declines have been documented, proportional declines in bioaccumulated Hg in fish tissues have also been observed (Cross et al., 2015). Furthermore, bioaccumulation and biomagnification are also impacted by localized trophic structure and trophic status of a given species (Taylor et al., 2014). These
are important considerations when assessing Hg exposure for human consumption of a given species, especially if sub-stocks utilize different regions and depths and have different prey preferences geographically and temporally, as may be occurring in NW Atlantic spiny dogfish (Carlson et al., 2014). Spiny dogfish are distributed globally; therefore, Hg concentrations are highly variable both geographically and temporally. Understanding fine scale patterns of contamination is important for this species as traceability and provenance of seafood sources become increasingly important to seafood markets both locally and globally. Available Hg data for spiny dogfish are shown in Table 1. These regionally specific Hg values were then compared to the widely cited “Mercury in Commercial Fish Species” database compiled by the US FDA (2014) to provide the region of origin for spiny dogfish and to compare values for Hg contamination in other commonly consumed fish species. The available literature showed that mean total Hg concentrations in filet tissues vary widely geographically by almost three orders of magnitude (Table 1). In general, spiny dogfish landed in US areas of the NW Atlantic (Taylor et al., 2014; Greig et al., 1977; this study) had lower total Hg concentrations than other areas. NW Atlantic spiny dogfish have historically shown lower levels of contamination than their Pacific counterparts (Hall et al., 1977; Childs and Gaffke, 1973; Greig et al., 1977). Taylor et al. (2014) corroborated these studies showing lower concentrations NW Atlantic spiny dogfish than Pacific spiny dogfish but also reported Hg values approaching or exceeding the EPA reference dose of 0.3 ppm in southern New England waters. Table 1 also suggests that there are geo-specific “hot spots” for Hg contamination where Hg concentrations exceeded both FDA (1 ppm) and EPA (0.3 ppm) thresholds. These areas are the waters around the island of Crete and certain areas off Southeast Australia (Table 1; Kousteni et al., 2006; Pethybridge et al., 2010). These results
Table 2 Risk categories for spiny dogfish accounting for Hg and fatty acid (FA) concentrations. Numbers in parentheses with “sp” are the number of species pooled from Cladis et al. (2014) that match species groupings in US FDA data. Low risk: low reward Hg b 0.3 ppm: FA N 500 mg/100 kg
Low risk: high reward Hg b 0.3 ppm: FA b 500 mg/100 kg
Elevated risk: high reward Hg b 0.3 ppm: FA N 500 mg/100 kg
Elevated risk: low reward Hg N 0.3 ppm: FA b 500 mg/100 kg
Catfish, Channel Tilapiaa Monkfish Tilefish (North) Haddock Flatfish (11sp)a Halibut (2sp) Hake, silver Cod (4sp) Snapper (3sp) Pollock (2 locations) Whiting, Pacific Perch FW (2sp) Mullet, striped Croaker, Atlantic
Bass, striped Perch, Pacific Ocean Shad, American Trout, freshwater (2 ps) Salmon, (5sp) Spiny dogfish (N. Atl)b Spiny dogfish N. Atlantic (This study ONLY)
Mackerel, Spanish Bluefish Swordfish Tuna, albacore SeaBass, Chilean Spiny dogfish, NE Pacific (US)b Spiny dogfish, Australia Spiny dogfish, Crete
Grouper, (4sp) Roughy, Orange Tilefish (Mexico) Tuna, Yellowfin Shark, Common Thresher Mackerel, King
a b
Indicated only Methylmercury was reported for the fish species. Indicates Hg data pooled across multiple studies in a region.
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highlight the important need to consider the geographic origin and the gender of the catch when considering species specific Hg advisories, and underscore the importance of transparency and traceability of spiny dogfish. Hg concentrations in spiny dogfish from many locations were ranked in comparison to Hg concentrations of other commonly consumed commercial fish species in the USA. Selected fish species and fish groupings from the US FDA “Mercury Levels in Commercial Fish and Shellfish” (USFDA, 2014) and the mean Hg values from Table 1
were collected in Fig. 1. The two identified “hot spots” for Hg are at the top of the list. Spiny dogfish with NW Atlantic origin have lower Hg concentrations, and have comparable mean Hg values to other commonly consumed, high value, fish species currently on seafood markets, or caught recreationally such as halibut, monkfish, and snapper. Spiny dogfish contain a wide variety of essential nutrients to human health, not only EPA and DHA. Mozaffarian and Rimm (2006) and Swanson et al. (2012) pointed out the numerous benefits of fish nutrients together with long chain fatty acids to human health. Cladis et al.
Fig. 1. Total Hg concentrations (ppm wet weight) of commonly consumed commercial fish species as represented by FDA data. Spiny dogfish data (outlined in black boxes) are sourced from primary literature represented in Table 1. Species annotated with “*” indicate results reported in only Methylmercury; “***” indicate spiny dogfish Hg data pooled across multiple studies to produce mean value for a region; numbers within parentheses with ^ following indicate number of species pooled.
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(2014) conducted a comprehensive analysis of fatty acid profiles of 76 commonly consumed fish species. We completed a simple risk assessment that contained both positive (EPA + DHA) and negative (Hg) attributes for spiny dogfish in comparison with other commonly consumed marine species as not all fish species contain high beneficial levels of EPA and DHA. EPA + DHA values of commonly consumed fish species from Cladis et al. (2014) were plotted to match species and species complexes listed by the US FDA “Hg Levels in Commercial Fish and Shellfish”. Fish species with the highest levels of EPA + DHA were assembled in ascending order (Fig. 2). Chilean sea bass and albacore tuna had the highest mean values, followed by spiny dogfish,
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salmon (pooled for 5 species), swordfish, bluefish, and freshwater trout (pooled for 2 species). While these species may impart the highest nutritional benefits due to their high EPA + DHA levels, species high in EPA + DHA may not necessarily also be low in Hg. A simple “risk-reward” assessment combining the datasets of EPA + DHA from Cladis et al. (2014), mean total Hg from US FDA (2000–2010), and the spiny dogfish data from Table 1 was made and presented in a scatterplot with risk-benefit boundaries (Fig. 3). These boundaries represent established guidelines for both Hg and EPA + DHA. For Hg a N 0.3 ppm reference dose was selected, representing the most conservative limit. For EPA + DHA, 500 mg was
Fig. 2. Select EPA + DHA values of commonly consumed fish species, adapted from Cladis et al. (2014). This list has been shortened and consolidated to match species and species complexes listed by the US FDA “Mercury Levels in Commercial Fish and Shellfish”. Numbers in parentheses with “sp” following indicate the number of species pooled from Cladis et al. (2014) to match species groupings in the FDA data. Spiny dogfish outlined in black box.
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Fig. 3. EPA + DHA levels (Cladis et al., 2014) vs mean total Hg values (ppm wet weight) as reported by US FDA with spiny dogfish values from Fig. 1. EPA + DHA levels are assumed to be consistent with Cladis et al. (2014) across time and space for all species. Risk-reward categories were created using the US EPA total Hg threshold of 0.3 ppm and for an EPA + DHA a daily intake of 500 mg as recommended by the American Heart Association, International Society for the Study of Fatty Acids, and the American Academy of Nutrition and Dietetics. Points within squares indicate commonly consumed fish species regarded as high in EPA + DHA; solid square = salmon (all species); dashed square = albacore Tuna. Points within ellipses represent spiny dogfish from various regions; solid ellipse = northwest Atlantic spiny dogfish; dashed ellipse = Pacific, Australian & Mediterranean (Crete) spiny dogfish.
selected as a threshold, the daily consumption recommended by the American Heart Association, the American Academy of Nutrition and Dietetics, and the International Society for the “Study of Fatty Acids and Lipids”. Results were grouped into four risk-reward categories: • Low risk–low reward: mean total Hg of ≤ 0.3 EPA + DHA ≤ 500 mg/100 g, • Low risk–high reward: mean total Hg of ≤ 0.3 EPA + DHA ≥ 500 mg/100 g, • Elevated risk–low reward: mean total Hg of ≥ 0.3 EPA + DHA ≤ 500 mg/100 g, • Elevated risk–high reward: mean total Hg of ≥ 0.3 EPA + DHA ≥ 500 mg/100 g.
ppm and ppm and ppm and ppm and
Fig. 3 highlights commonly consumed species as examples of low and elevated risk species with regard to Hg concentrations but high rewards due to their EPA + DHA contents; these are salmon (all 5 species) and albacore tuna. Table 2 specifies risk-reward categories for all species in the data sets analyzed. If EPA + DHA contents are assumed to be similar in a species throughout their range (acknowledging that this is likely not the case), spiny dogfish from various regions fall into both the low and elevated risks with high reward categories, depending on origin of catch. Both the pooled NW Atlantic spiny dogfish Hg values and mean Hg values from this study fall in the low risk–high reward category, while the pooled NE Pacific, Australian and Mediterranean (Crete) spiny dogfish fall in the elevated risk–high reward categories. When making public health recommendations regarding Hg concentrations and consumption of commercially harvested fish species, warnings are too often blanketed by species or species complex, and may not be based on the best available data. In this review, Hg concentrations in spiny dogfish varied by geography, season, fish size, and fish gender. Where limited data are available, such as in this study, and others such as Taylor et al. (2014), conservative health advisories are always advisable. However, whenever possible, and where regional data are available, more nuanced recommendations should be made (Shim et al., 2005); especially since risk analyses show that public health risk of fish containing Hg levels below US FDA the action level is outweighed by the potential health benefits of eating fish such as spiny dogfish with high levels of valuable fatty acids such as EPA + DHA (Mozaffarian and
Rimm, 2006; The Institute of Medicine, 2006; Environmental News Wire, 2005; Feig, 2006). Based upon the data reviewed here in this study, there is no reason why spiny dogfish from the NW Atlantic cannot be regarded as a safe choice for the general population with regards to Hg. Increased fish consumption is recommended for the general population with important exceptions for the highest risk groups, such as young children and women of child-bearing age (Oken et al., 2005). For these groups, public health professionals recommend specific limitations (International Food Information Council Foundation et al., 2004). According to one of the authors of this report (C. Santerre), the precautionary EPA reference dose is 0.1 μg/kg body weight/day. To get such a concentration limit for sensitive populations, Santerre has used a 60 kg body weight person and for fish with 0.186 to 0.377 ppm Hg, he recommends no more than 113 g (4 oz) per week be consumed. The US NW Atlantic spiny dogfish fishery has been independently certified by the Marine Stewardship Council (MSC) environmental standard as a sustainable fishery. In this limited analysis of male spiny dogfish from Rhode Island Sound taken in the winter, mean Hg concentrations were found to be below the US FDA action level of 1 ppm and below the EPA human health screening value of 0.3 ppm (USEPA, 2000). Hg concentrations from other regions were higher. It is obvious that additional Hg testing is needed for female spiny dogfish that comprise the bulk of the current fishery since evidence exists that female dogfish have higher Hg concentrations in some regions. A risk analysis for NW Atlantic male spiny dogfish combining Hg values and EPA + DHA concentrations from this study fall in the low risk–high reward category, while the pooled NE Pacific, Australian and Crete, Mediterranean Sea spiny dogfish fall in the elevated risk–high reward categories. A risk-reward framework can help provide more nuanced guidance to the consumption of other species based on this approach. However, this approach of determining optimal seafood intake based on multiple variables is not novel. Sirot et al. (2012) constructed more extensive, fine scale risk analysis model using a hierarchical cluster analysis based on EDP + DHA and environmental contaminants including Hg, cadmium, dioxins, and other trace metals. Future improvements to the Sirot et al. (2012) model need to be pursued to include regional and seasonal variabilities, fish sizes, and gender. Acknowledgments The authors wish to thank Professor Charles Santerre, Purdue University, and Jen Levin, Gulf of Maine Research Institute for their valuable comments on drafts of this paper. Funding for this research was provided by the US National Oceanographic and Atmospheric Agency Saltonstall Kennedy Research Program (Funding opportunity number: NOAA-NMFS-FHQ-2013-2003834). References Atlantic States Marine Fisheries Commission (ASMFC), 2008. Species profile: spiny dogfish stock rebuilding hinges on robust spawning stock. Excerpted from ASMFC Fisheries Focus 17:4, pp. 1–6. Atlantic States Marine Fisheries Commission (ASMFC), 2009. Interstate Fishery Management Plan for Spiny Dogfish. Bosch, A.C., Sigge, G.O., Kerwath, S.E., Cawthorn, D.M., Hoffman, L.C., 2013. The effects of gender, size and life-stage on the chemical composition of smoothound (Mustelus mustelus) meat. J. Sci. Food Agric. 93, 2384–2392. Carlson, A.E., Hoffmayer, E.R., Tribuzio, C.A., Sulikowski, J.A., 2014. The use of satellite tags to redefine movement patterns of spiny dogfish (Squalus acanthias) along the U.S. east coast: implications for fisheries management. PLoS One 9 (7), e103384. Childs, E.A., Gaffke, J.N., 1973. Mercury content of Oregon ground fish. Fish. Bull. 71.3. Cladis, D.P., Kleiner, A.C., Freiser, H.H., Santerre, C.R., 2014. Fatty acid profiles of commercially available finfish fillets in the United States. Lipids 49.10, 1005–1018. Cladis, E., Zhang, R., Tan, X., Craig, B., Santerre, C., 2015. Postharvest correlation between swordfish (Xiphius gladius) size and mercury concentration in edible tissues. J. Food Prot. 78 (2), 396–401. Clarkson, T.W., Magos, L., 2006. The toxicology of mercury and its chemical compounds. Crit. Rev. Toxicol. 36, 609–662.
A.T. St. Gelais, B.A. Costa-Pierce / Marine Pollution Bulletin 102 (2016) 199–205 Cross, F.A., Evans, D.W., Barber, R.T., 2015. Decadal declines of mercury in adult bluefish (1972–2011) from the mid-Atlantic coast of the U.S.A. Environ. Sci. Technol. 49, 9064–9072. Domi, N., Bouquegneau, J.-M., Das, K., 2005. Feeding ecology of five commercial shark species of the Celtic Sea through stable isotope and trace metal analysis. Mar. Environ. Res. 60 (5), 551–569. Endo, T., Hisamichi, Y., Kimura, O., Kotaki, Y., Ohta, C., Koga, N., Haraguchi, K., 2009. Contamination levels of mercury in the muscle of female and male spiny dogfishes (Squalus acanthias) caught off the coast of Japan. Chemosphere 77.10, 1333–1337. Engstrom, D.R., Swain, E.B., 1997. Recent declines in atmospheric mercury deposition in the upper Midwest. Environ. Sci. Technol. 31, 960–967. Environment News Wire, 2005. Seafood Health Benefits Outweigh Toxic Risks, Scientists Say (Dec. 7) . European Commission, 2005. Commission regulation (EC) no 78/2005 of 19 January 2005 amending regulation (EC) no 466/2001 as regards heavy metals. Off. J. Eur. Union L 16, 43–45. Feig, C., 2006. Seafood Benefits Outweigh Risks, Government Says. CNN (Nov. 2). (Available at http://www.cnn.com/2006/HEALTH/10/17/seafood.guidelines/). Fogarty, M.J., Murawski, S.A., 1998. Large-scale disturbance and the structure of marine systems: fishery impacts on Georges Bank. Ecol. Appl. 8.sp1, S6–S22. Garrison, L.P., Link, J.S., 2000. Dietary guild structure of the fish community in the northeast United States continental shelf ecosystem. Mar. Ecol. Prog. Ser. 202, 231–240. Greig, R.A., Wenzloff, D., Shelpuk, C., Adams, A., 1977. Mercury concentrations in three species of fish from north Atlantic offshore waters. Arch. Environ. Contam. Toxicol. 5 (1), 315–323. Hall, A.S., Teeny, F.M., Gauglitz Jr., E.J., 1977. Mercury in fish and shellfish of the northeast Pacific. III. Spiny dogfish, Squalus acanthias. Fish. Bull. 75.3 (United States). Hall, B.D., Bodaly, R.A., Fudge, R.J., Rudd, J.W., Rosenberg, D.M., 1997. Food as the dominant pathway of methylmercury uptake by fish. Water Air Soil Pollut. 100, 13–24. Health Canada, 2012. Canadian standards (maximum levels) for various chemical contaminants in foods Available at: http://www.hcsc.gc.ca/fn-an/securit/chem-chim/ contaminants-guidelines-directiveseng. php. Institute of Medicine, 2006. Seafood choices: balancing benefits and risks. Report Brief (Oct.). International Food Information Council Foundation, Cameron, G.T., Jeffery, E., MacDonald, R.S., Santerre, C.R., Weaver, C., 2004,. Guidelines for Communicating the Emerging Science of Dietary Components for Health. pp. 1–11 (0). Karimi, R., Fitzgerald, T.P., Fisher, N.S., 2012. A quantitative synthesis of mercury in commercial seafood and implications for exposure in the United States. Environ. Health Perspect. 120 (1), 1512–1519. Kousteni, V., Megalofonou, P., Dassenakis, M., Stathopoulou, E., 2006. Total mercury concentrations in edible tissues of two elasmobranch species from Crete (eastern Mediterranean Sea). Cybium 30 (4), 102–108. Link, J.S., Garrison, L.P., Almeida, F.P., 2002. Ecological interactions between elasmobranchs and groundfish species on the northeastern US continental shelf. I. Evaluating predation. N. Am. J. Fish Manag. 22 (2), 550–562. Lobring, L.B., Potter, B.B., 1991. EPA Method 245.6: Determination of Mercury in Tissues by Cold Vapor Atomic Absorption Spectrometry. U.S. Environmental Protection Agency. Mid-Atlantic Fishery Management Council (MAFMC), 2012. Amendment 2 to the Spiny Dogfish Fishery Management Plan. Mid-Atlantic Fishery Management Council (MAFMC), Northeast Fisheries Management Council (NEFMC), 1999s. Spiny dogfish fishery management plan. NOAA Award No. NA57FC002 (494 pp.).
205
Mozaffarian, D., Rimm, E.B., 2006. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA 296 (15), 1885–1899. Murawski, S.A., Idoine, J.S., 1992. Multispecies size composition: a conservative property of exploited fishery systems. J. Northwest Atl. Fish. Sci. 14, 79–85. NOAA, 2013. Fisheries service northeast fisheries science center. Apex Predators Program (Available at http://na.nefsc.noaa.gov/sharks/. Accessed Sept. 24, 2013). Northeast Fishery Science Center (NEFSC), 1998. 26th Northeast Regional Stock Assessment Workshop: Stock Assessment Review Committee (SARC) Consensus Summery of Assessments. NMFS, Woods Hole, MA, pp. 98–104 (NEFSC Ref.Doc). Northeast Fishery Science Center (NEFSC), 2003. 37th Northeast Regional Stock Assessment Workshop: Stock Assessment Review Committee (SARC). Oken, E., Wright, R.O., Kleinman, K.P., Bellinger, D., Amarasiriwardena, C.J., Hu, H., RichEdwards, J.W., Gillman, M.W., 2005. Maternal fish consumption, hair mercury, and infant cognition in a US cohort. Environ. Health Perspect. 1376–1380. Pethybridge, H., Cossa, D., Butler, E.C.V., 2010. Mercury in 16 demersal sharks from southeast Australia: biotic and abiotic sources of variation and consumer health implications. Mar. Environ. Res. 69.1, 18–26. Rago, P.J., Sosebee, K.A., 2012. Update on the Status of Spiny Dogfish in 2012 and Initial Evaluation of Harvest at the Fmsy Proxy. NOAA/NMFS Northeast Fisheries Science Center, Woods Hole, MA (44 pp.). Shim, S.M., Lasrado, J.A., Dorworth, L.E., Santerre, C.R., 2005. Mercury and omega-3 fatty acids in retail fish sandwiches. J. Food Prot. 68 (3), 633–635. Sirot, V., Leblanc, J.C., Margaritis, I., 2012. A “risk-benefit approach to seafood intake to determine optimal consumption.”. Br. J. Nutr. 106, 1812–1822. Smith, B.E., Link, J.S., 2010. The trophic dynamics of 50 finfish and 2 squid species on the northeast US continental shelf. NOAA Technical Memorandum NMFS-NE 216. Sulikowski, J.A., Galuardi, B., Bubley, W., Furey, N., Driggers, W.B., Ingram II, W., Tsang, P.C.W., 2010. Use of satellite tags to reveal the movements of spiny dogfish Squalus acanthias in the western north Atlantic ocean. Mar. Ecol. Prog. Ser. 418, 249–254. Swanson, D., Block, R., Mousa, S.A., 2012. Omega-3 fatty acids EPA and DHA: health benefits throughout life. Adv. Nutr. Int. Rev. J. 3 (1), 1–7. Taylor, D.L., Kutil, N.J., Malek, A.J., Collie, J.S., 2014. Mercury bioaccumulation in cartilaginous fishes from southern new England coastal waters: contamination from a trophic ecology and human health perspective. Mar. Environ. Res. 99, 20–33. TRAC (Transboundary Resources Assessment Committee), 2010. Northwest Atlantic spiny dogfish. TRAC Status Report 2010/02. U.S. Environmental Protection Agency (USEPA), 2000. Guidance for Assessing Chemical Contaminant Data for Use in Fish Advisories, Volume 2: Risk Assessment and Fish Consumption Limits. third ed. U.S. Environmental Protection Agency, Office of Science and Technology, Office of Water, Washington, D.C. (EPA-823-B-00-008. http://www. epa.gov/waterscience/fish/advice/volume2/index.html). U.S. Food and Drug Administration, 2014. Mercury levels in commercial fish and shellfish (1990–2010)Available at http://www.fda.gov/food/foodborneillnesscontaminants/ metals/ucm115644.htm (Accessed: 22 May 2015). U.S. Food and Drug Administration, 1994. Mercury levels in fish: cause for concern? Available at: http://www.fda.gov/OHRMS/DOCKETS/ac/02/briefing/3872_Advisory% 207.pdf (Accessed 10 December 2015) Ullrich, S.M., Tanton, T.W., Abdrashitova, S.A., 2001. Mercury in the aquatic environment: a review of factors affecting methylation. Crit. Rev. Environ. Sci. Technol. 31 (3), 241–293.