Marine Pollution Bulletin xxx (2013) xxx–xxx

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Total mercury concentrations in lionfish (Pterois volitans/miles) from the Florida Keys National Marine Sanctuary, USA Dane H. Huge a,b,⇑, Pamela J. Schofield a, Charles A. Jacoby c, Thomas K. Frazer b,d a

Southeast Ecological Science Center, United States Geological Survey, 7920 NW 71st Street, Gainesville, FL 32653, USA School of Natural Resources and Environment, University of Florida, 103 Black Hall, Gainesville, FL 32611, USA c Soil and Water Science Department, University of Florida, 7922 NW 71st Street, Gainesville, FL 32653, USA d Fisheries and Aquatic Sciences Program, School of Forest Resources and Conservation, University of Florida, 7922 NW 71st Street, Gainesville, FL 32653, USA b

a r t i c l e

i n f o

a b s t r a c t

Keywords: Lionfish Pterois volitans/miles Mercury South Florida Bioaccumulation Fish advisories

Strategies to control invasive lionfish in the western Atlantic and Caribbean are likely to include harvest and consumption. Until this report, total mercury concentrations had been documented only for lionfish from Jamaica, and changes in concentrations with increasing fish size had not been evaluated. In the Florida Keys, total mercury concentrations in dorsal muscle tissue from 107 lionfish ranged from 0.03 to 0.48 ppm, with all concentrations being less than the regulatory threshold for limited consumption. Mercury concentrations did not vary consistently with standard lengths or wet weights of lionfish. In 2010, lionfish from the upper Keys had mean concentrations that were 0.03–0.04 ppm higher than lionfish from the middle Keys, but mean concentrations did not differ consistently among years and locations. Overall, total mercury concentrations in lionfish were lower than those in several predatory fishes that support commercial and recreational fisheries in Florida. Published by Elsevier Ltd.

1. Introduction

(Phillips and Buhler, 1978; Lyle, 1986; Bernhoft, 2012) or are exposed prenatally (D’itri and D’itri, 1977; EPA, 2001a,b). In fact, consumption of seafood represents a primary source of mercury in human diets. Mercury toxicity is determined by a combination of the concentration of mercury in the fish or shellfish being consumed and the amount of the fish or shellfish consumed in a given period. In Florida, advisories regarding consumption of seafood are based on a total mercury concentration of 1.0 ppm, as recommended by the World Health Organization and the United States Food and Drug Administration. The categories for advisories are unlimited consumption when mercury concentrations in tissue are under 0.5 ppm, limited weekly consumption when concentrations are between 0.5 and 1.5 ppm (with young children and women of childbearing age advised to eat less fish per week), and no consumption when concentrations exceed 1.5 ppm. Mercury contamination of Florida’s fishes became a concern in 1982 when elevated levels of mercury were detected in numerous species of freshwater fishes (Lange et al., 1993; Adams et al., 2003). Additionally, sampling from 1989 through 2001 showed that gag grouper (Mycteroperca microlepis), greater amberjack (Seriola dumerili) and scamp (Mycteroperca phenax) from estuarine and coastal waters contained mercury at levels near or above the ‘‘limited consumption’’ category (0.5–1.0 ppm) and cobia (Rachycentron canadum) fell in the ‘‘no consumption’’ category (1.0–1.5 ppm) as determined by the Florida Department of Health (Adams et al., 2003).

Mercury discharged from natural and anthropogenic activities can affect the environment at local scales (e.g., industrial effluents, geothermal activity, and forest fires) and regional or global scales (e.g., atmospheric deposition from fossil fuel combustion, waste incineration, and metal refining; EPA, 2006). In both cases, environmental conditions influence bioavailability, uptake, and transfer through food webs. In estuarine and marine systems, for example, methylation of inorganic mercury is controlled primarily by sulfate:sulfide redox conditions (King, 1993), methylmercury (CH3Hg) is transferred through trophic webs efficiently (Coelho et al., 2013), and it generally accounts for 95% of mercury found in fishes (Bloom, 1992). In these systems, larger and older predatory fishes generally accumulate more mercury than smaller and younger herbivores or omnivores (Frederick et al., 1999; Snodgrass et al., 2000; Dang and Wang, 2012; Coelho et al., 2013). Bioaccumulation of mercury can cause adverse effects in fish and wildlife, including reproductive impairment, neurological damage, and detrimental changes in behavior (Scheuhammer, 1991; Suter, 1993; Beyer et al., 1997). Comparable effects have been observed in humans who consume contaminated seafood ⇑ Corresponding author at: Southeast Ecological Science Center, United States Geological Survey, 7920 NW 71st Street, Gainesville, FL 32653, USA. Tel.: +1 352 264 3540. E-mail addresses: [email protected] (D.H. Huge), pschofi[email protected] (P.J. Schofield), cajacoby@ufl.edu (C.A. Jacoby), frazer@ufl.edu (T.K. Frazer). 0025-326X/$ - see front matter Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.marpolbul.2013.11.019

Please cite this article in press as: Huge, D.H., et al. Total mercury concentrations in lionfish (Pterois volitans/miles) from the Florida Keys National Marine Sanctuary, USA. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.11.019

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D.H. Huge et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx

In the Florida Keys National Marine Sanctuary and elsewhere, consumption of harvested lionfish (Pterois volitans/miles), is being promoted as a management strategy that can limit the ecological impacts of this invasive species (Morris and Whitfield, 2009). Until now, information regarding concentrations of total mercury in lionfish was only available for Jamaica, where concentrations in 25 lionfish ranged from 0.02 to 0.06 ppm (mean ± standard deviation = 0.04 + 0.01) and accumulation was not evaluated (Hoo Fung et al., 2013). In the Florida Keys, lionfish could be expected to accumulate mercury because they are mid-sized predators that consume large quantities of smaller fishes and crustaceans (Morris and Akins, 2009; Layman and Allgeier, 2012) and they are living in areas where other predators have total mercury concentrations in their muscle that are near or above consumption limits (Adams et al., 2003). Thus, the objectives of this study were to quantify concentrations of total mercury in lionfish muscle, make a preliminary evaluation of spatiotemporal variation in these concentrations, and assess accumulation of mercury.

Department of Environmental Protection using cold vapor atomic absorption (DEP SOP: HG-006-3[based on EPA 245.6]/E31780). The working range for the direct mercury analyzer was 0.05– 600 ppt, and the minimum detection limit was 0.01 ppt. For cold vapor atomic absorption, the calibration range for tissue samples was 0.60–2.50 ppb. For 1 g of tissue, the minimum detection limit was 0.005 ppm and the practical quantitation limit was 0.02 ppm. In both sets of analyses, method blanks comprised deionized water, and certified commercial inorganic mercury standards were used to create laboratory control samples, matrix spikes and calibration standards. Duplicate measures of laboratory control samples and matrix spikes were made for each batch of 9–20 samples, and duplicate measures of calibration standards were made at the beginning and end of each batch, as well as after every set of 10 samples within each batch.

2. Methods and materials Lionfish were collected during five derbies held at Key Largo (upper Keys) in September 2010 and August 2011, Marathon (middle Keys) in October 2010 and May 2011, and Key West (lower Keys) in November 2010 (Fig. 1). During derbies, teams of recreational divers and snorkelers had approximately 10 h to spear or capture lionfish in various habitats and locations within the Florida Keys National Marine Sanctuary. When participants returned to a central collection area, lionfish were measured (standard length to the nearest mm), weighed (wet weight to the nearest g) and placed in uniquely labeled plastic bags that were sealed and stored on ice in coolers during transport. In the laboratory, fish were transferred to freezers and held at 20 °C. Fish were processed in the laboratory according to standard operating procedures that minimized the risk of cross contamination (EPA, 2000). A sample of muscle tissue (filet without skin) was taken posterior to the first dorsal fin. Between each sample, the stainless steel knives were rinsed sequentially in soapy water, tap water, ethyl alcohol, and acetone to remove organics. Samples were analyzed in two different ways due to a malfunctioning motor in one analyzer. Thirty-two samples were analyzed with a direct mercury analyzer according to the EPA (1998) method, and seventy-five samples were analyzed by the Florida

Fig. 1. Maps of the United States of America, with Florida in black, and Florida showing the centers of the three regions where derbies were held.

Fig. 2. Back-transformed mean (a) standard lengths, (b) wet weights and (c) concentrations of total mercury ± 95% confidence limits (CL). Letters indicate significantly different means according to Tukey’s multiple comparison tests, UK = Key Largo in the upper Keys, MK = Marathon in the middle Keys, LK = Key West in the lower Keys.

Please cite this article in press as: Huge, D.H., et al. Total mercury concentrations in lionfish (Pterois volitans/miles) from the Florida Keys National Marine Sanctuary, USA. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.11.019

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D.H. Huge et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx

Table 1 Results of analyses of covariance applied to log10-transformed concentrations of total mercury in lionfish, Pterois volitans/miles, from the Florida Keys National Marine Sanctuary. Source

df

SS

MS

F

p

Standard length Analytical method Standard length  Analytical method Error Standard length Analytical method Error Wet weight Analytical method Wet weight  Analytical method Error Wet weight Analytical method Error

1 1 1 102 1 1 103 1 1 1 102 1 1 103

0.00934 0.07994 0.05110 6.49618 0.00099 0.05918 6.54728 0.03261 0.13105 0.04795 6.46230 0.03802 0.08706 6.51025

0.00934 0.07994 0.05110 0.06369 0.00099 0.05918 0.06357 0.03261 0.13105 0.04795 0.06336 0.03802 0.08706 0.06321

0.15 1.26 0.80

0.703 0.265 0.373

0.02 0.93

0.901 0.337

0.51 2.07 0.76

0.475 0.153 0.386

0.60 1.38

0.440 0.243

Table 2 Standard lengths and total mercury concentrations in tissue of commonly harvested fishes from the Florida Keys National Marine Sanctuary (Adams et al., 2003; Adams and Onorato, 2005). Species

Black grouper (Mycteroperca bonaci) Redfish (Sciaenops ocellatus) Gag grouper (Mycteroperca microlepis) Red grouper (Epinephelus morio) White grunt (Haemulon plumieri) Gray snapper (Lutjanus griseus) Hogfish (Lachnolaimus maximus) Yellowtail snapper (Ocyurus chrysurus) Lionfish (Pterois volitans/miles)

Standard length (mm)

Concentration (ppm)

Range

Mean

Range

Mean

636–1000 230–628 428–605 405–470 138–213 152–396 200–341 235–386 50–226

772 454 511 438 177 246 289 301 123

0.83–1.60 0.11–2.70 0.24–0.82 0.16–0.33 0.09–0.51 0.03–0.62 0.08–0.35 0.04–0.28 0.03–0.48

1.16 0.50 0.46 0.27 0.23 0.21 0.16 0.15 0.13

The data supported ten statistical analyses. Three one-way analyses of variance (ANOVAs) tested for differences in standard lengths, wet weights and concentrations of total mercury among the five derbies. In addition, four analyses of covariance (ANCOVAs) examined differences between data from the two methods and relationships between total mercury concentrations and standard lengths or wet weights. One pair of ANCOVAs included interactions between the covariate (standard length or wet weight) and the method of analysis to test for differences in slopes. Prior to analyses, standard lengths and wet weights were square root transformed and concentrations were log10 transformed to improve normality as determined by Anderson–Darling tests and homoscedasticity as determined by Cochran’s tests.

significantly among derbies (F4,101 = 3.22, p = 0.02), but Tukey’s multiple comparison tests did not detect a consistent pattern (Fig. 2). The only significant difference detected by multiple comparisons was that concentrations in lionfish taken during the 2010 derby in the upper Keys were significantly higher than concentrations in lionfish taken in the middle Keys during the same year. Lionfish analyzed by the two methods had overlapping distributions of standard lengths and wet weights (direct analyzer: 79–226 mm and 11–423 g; atomic absorption: 50–198 mm and 3–319 g). The ANCOVAs, with standard length or wet weight as a covariate, indicated no significant difference in total mercury concentrations detected by the two methods and no significant relationship between concentration and fish size (Table 1).

3. Results 4. Discussion Quality assurance results indicated that estimates of total mercury concentrations in lionfish muscle were reliable, accurate, and precise. All method blanks yielded concentrations below the method detection limit. Duplicate measures of laboratory control samples, matrix spikes, and verification standards yielded mean percentage recovery rates ± standard deviations equal to or greater than 98.1 ± 5.6%, and percentage recovery rates between duplicates differed by no more than 1.6 ± 1.0% on average. In total, samples of muscle from 107 lionfish ranging from 50 to 226 mm standard length and 3–423 g wet weight were analyzed for total mercury concentrations, with significantly longer and heavier lionfish being taken during the 2011 derbies (Fig. 2; F4,101 = 23.41, p < 0.001 and F4,101 = 29.79, p < 0.001, respectively). Total mercury concentrations ranged from 0.03 to 0.48 ppm; therefore, all concentrations were less than the 0.50-ppm threshold for limited consumption. Total mercury concentrations varied

To our knowledge, the only total mercury concentrations published for lionfish apply to Jamaica, where values ranged from 0.02 ppm to 0.06 ppm (mean ± standard deviation = 0.04 ± 0.01 ppm) and the relationship between total mercury concentrations and fish size was not evaluated (Hoo Fung et al., 2013). On average, muscle from lionfish in the Florida Keys had higher concentrations (mean and standard deviation = 0.13 + 0.08 ppm), which may be expected given concerns about mercury in other fishes from the waters off Florida. Nevertheless, in comparison to commonly consumed predatory fishes collected from the Florida Keys and other waters around Florida, lionfish had the lowest mean total mercury concentrations (0.13 ppm), with yellowtail snapper (Ocyurus chrysurus, 0.15 ppm), and hogfish (Lachnolaimus maximus, 0.16 ppm) having the most similar concentrations (Table 2; Adams et al., 2003; Adams and Onorato, 2005). The relatively low

Please cite this article in press as: Huge, D.H., et al. Total mercury concentrations in lionfish (Pterois volitans/miles) from the Florida Keys National Marine Sanctuary, USA. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.11.019

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D.H. Huge et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx

concentrations in lionfish may be due to differences in mercury concentrations in their prey versus concentrations in the prey of other predators or differences in the physiological processing of mercury. In general, methylmercury is transferred efficiently from prey to predators, but elimination of mercury does vary among species and fish of different sizes (Wang and Wong, 2003; Amlund et al., 2007; Dang and Wang, 2012). Smaller and faster growing fish tend to have higher metabolic rates that can increase elimination of mercury, and concentrations in faster growing fish are affected by ‘‘growth dilution’’ (Dang and Wang, 2012). In comparison to most other predators that support commercial and recreational fisheries in the Florida Keys, lionfish are smaller and grow faster (Table 2; Morris and Akins, 2009), with significant growth detected between the two years of sampling conducted in this study. A test of the hypotheses that lionfish eliminate mercury more rapidly and experience more ‘‘growth dilution’’ than other predatory fishes in the Florida Keys would help to elucidate the mercury budget of lionfish. Typically, diets of marine fishes represent the primary influence on bioaccumulation of mercury in muscle tissue (Wang, 2002). Lionfish are considered generalist predators that consume prey according to their availability (Morris and Whitfield, 2009; Layman and Allgeier, 2012). For example, lionfish in the Bahamas consumed 21 families and 41 species of teleosts, at least four families of Crustacea and one family of Mollusca (Morris and Akins, 2009). In the Bahamas and off Little Cayman Island, larger lionfish preyed nearly exclusively on teleosts (Morris and Akins, 2009; Frazer et al., 2012). Studies of total mercury concentrations in common prey would elucidate uptake rates and provide additional insights into the mercury budget of invasive lionfish. There were no significant relationships between concentrations of total mercury in lionfish muscle and standard length or wet weight and no significant difference in concentrations between years. Nevertheless, such differences may develop as the lionfish population in the Florida Keys matures because older fish often accumulate methylmercury (Frederick et al., 1999; Snodgrass et al., 2000; Dang and Wang, 2012; Coelho et al., 2013). Fish examined in this study were likely to be no more than four years old because the first lionfish was observed in the upper Florida Keys in January 2009 (Schofield, 2010). In fact, measurable differences can develop over time and in space (Adams and McMichael, 2007; Dang and Wang, 2012), and the one significantly different concentration documented in this study provided some evidence that such differences could develop in the Florida Keys. Overall, our results show that muscle tissue from lionfish captured in the Florida Keys contained low concentrations of total mercury relative to native fishes and current regulatory thresholds. Additional samples from the Florida Keys and baseline samples from other locations will contribute to an understanding of the spatiotemporal dynamics of mercury bioaccumulation in lionfish and an improved ability to advise managers and participants in derbies or other harvesting activities about the benefits and risks associated with consuming these invasive predators (Petre et al., 2012). Acknowledgments This study was funded by the U.S. Geological Survey’s Invasive Species Program, the USGS Southeast Ecological Science Center, and the Institute of Food and Agricultural Sciences at the University of Florida. We thank the staff of the Florida Lab Support Section in the Florida Department of Environmental Protection for laboratory analysis of total mercury. Additionally, we thank Carla Weiser at USGS–SESC for laboratory technical support. Many thanks to Lad Akins and members of the Reef Environmental

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miles) from the Florida Keys National Marine Sanctuary, USA.

Strategies to control invasive lionfish in the western Atlantic and Caribbean are likely to include harvest and consumption. Until this report, total ...
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