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Article history: Blue crabs, Callinectes sapidus, from the Atlantic coast of Florida were analyzed for total mercury,
Received 2 October 2013 methylmercury, lead, and cadmium. Paired samples of two tissue types were analyzed for each crab,
Received in revised form (1) muscle tissue (cheliped and body muscles) and (2) whole-body tissue (all organs, muscle tissue and
13 November 2013
connective tissue), for evaluation of the concentration of metals available to human consumers as well as
Accepted 29 November 2013
estuarine predators. There were clear patterns of tissue-specific partitioning for each metal. Total
Available online 5 February 2014
mercury was significantly greater in muscle tissue (mean¼0.078 mg/g) than in whole-body tissue
Keywords: (mean¼ 0.055 mg/g). Conversely, whole-body concentrations of lead and cadmium (means ¼0.131 and
Contaminants 0.079 mg/g, respectively) were significantly greater than concentrations in muscle (means ¼0.02
Heavy metals
and 0.029 mg/g, respectively). There were no significant correlations between any metal contaminant
Mercury
and crab size. Cadmium levels were significantly greater in the muscle tissue of females, but, no other
Lead
Cadmium sex-related differences were seen for other metals or tissue types. Methylmercury composed 93–100% of
Blue crab (Callinectes sapidus) the total mercury in tissues. Compared to previous blue crab studies from different regions of the United
States, mean concentrations of mercury, lead, and cadmium were relatively low, although isolated groups
or individual blue crabs accumulated high metal concentrations.
& 2013 Elsevier Inc. All rights reserved.
0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ecoenv.2013.11.029
D.H. Adams, M.E. Engel / Ecotoxicology and Environmental Safety 102 (2014) 196–201 197
The Indian River Lagoon system (IRL) is a large estuarine Blue crabs were placed directly on ice after collection and returned to the
laboratory, where species was confirmed and carapace width (CW), total weight
ecosystem spanning approximately 251.1 km (156 miles) of the
(TW), and sex recorded. Whole crabs were packaged individually in clean plastic
Florida Atlantic coast. This estuarine system is characterized by bags and frozen at 20 1C. Frozen samples were shipped to the Food Safety
relatively constrained water circulation, limited freshwater inflow Laboratories at the Florida Department of Agriculture and Consumer Services
from inland sources, and restricted influence from the adjacent (Tallahassee, FL), where they were kept frozen until assayed.
Atlantic Ocean via five functional inlets. Coastal land uses along
the IRL system include diverse urban, suburban, industrial, and 2.2. Tissue preparation
agricultural development. Collectively, these characteristics make
the IRL and its fauna especially susceptible to pollution from local Each crab was laid on a clean surface dorsal side down with chelipeds pointing
and remote anthropogenic sources. Toxic metal contaminants in away, then split down the sagittal plane with a clean stainless-steel knife. For one
portions of the IRL system have been found to be elevated in half of each crab, solely muscle tissue was removed by picking and scraping with a
clean polypropylene transfer pipette. From the other half of the crab, all soft tissues
sediment, water and clams (Trefry et al., 2008) as well as in some (all muscle, organs, and connective tissue) were removed with a clean polypropy-
estuarine fish species (Adams et al., 2003; Adams and Paperno, lene transfer pipette. Each subsampled half of the crab was separately homo-
2012). genized in an acid-washed food processor (Robo Coupe, Ridgeland, MS, USA or One
Blue crabs are opportunistic omnivores and detritivores feeding Touch Food Chopper, Black and Decker, Towson, MD, USA). Homogenized tissue
was transferred to a 50-ml polypropylene centrifuge tube. Samples were frozen at
on a wide array of prey, including bivalves, fish, gastropods, and
20 1C until extraction (FDACS, 2010).
other crustaceans, as well as plant matter (Laughlin, 1982; Perkins-
Visser et al., 1996). In their range, blue crabs are a significant
2.3. Analysis of mercury, lead, and cadmium
contributor to the structure of estuarine benthic communities
(Virnstein, 1979; Clark et al., 1999; Douglass et al., 2011). Blue crabs
Total mercury, lead, and cadmium concentrations were determined in blue crab
are themselves prey for a large number of estuarine and marine
tissues following microwave digestion in 5 ml of Optima grade HNO3 (CEM MARSX,
predators (Van Den Avyle, 1984; Hines, 2007). The overall feeding Matthews, NC) by inductively-coupled plasma mass spectrometry (ICP-MS; Perki-
ecology, life history, and behavior of blue crabs places them in nElmer Sciex Elan 6100) (FDACS, 2010). All samples were analyzed in duplicate.
direct contact with metal contaminants in the environment via the Quality control samples included laboratory reagent blanks (after every 10 crab
samples), internal standards (recovery 60–125%), and analyses of standard reference
water column, sediments, and prey. Environmental contaminants
material (SRM 2976, NIST, Gaithersburg, MD). To verify mercury calibration (recovery
directly affect blue crab physiology; in studies comparing metal- 90–110%), standard reference material (SRM 1641d, NIST, Gaithersburg, MD) was
contaminated habitats with uncontaminated habitats, metals analyzed after each set of 10 samples and at the end of each analytical run. The
reduced a blue crab's ability to capture active prey (Reichmuth calibration verification standard for lead and cadmium was made from a second
et al., 2009). Mercury has been shown to reduce survival of early source (High Purity Standards, Charleston, SC). A rinse solution of 200 ng/ml gold, 1%
HCl and 5% HNO3 was used after each analysis to prevent carryover. The internal
life history stages and to inhibit hatching (Engel and Thayer, 1998).
standard for mercury and lead was lutetium, and the internal standard for cadmium
Depending on target tissues analyzed, results regarding metal was rhodium (FDACS, 2010). The ICP-MS analysis was run using the following
contamination in this species can be applied to multiple end- instrument conditions; nebulizer flow rate was 1.0 L/min, plasma gas flow rate was
points, including human health and consumption aspects, the 15 L/min, and the auxiliary gas flow rate was 0.2 L/min. The RF power was
health and fitness of blue crabs themselves, as well as trophody- maintained at 1100 W. The masses monitored were; Cd 111m/z and 113m/z, Pb
208m/z, and Hg 201m/z and 202m/z. The quantification masses were 111m/z for Cd
namic implications of blue crabs as both predator and prey in and 202m/z for mercury. The response for masses 206m/z, 207m/z and 208m/z were
coastal ecosystems. summed for Pb quantification.
The objectives of this study were to quantify and interpret total
mercury, methylmercury, lead, and cadmium in blue crabs from the
2.4. Tissue analysis of methylmercury
Atlantic coast of Florida, within the Indian River Lagoon system.
Specifically, we investigated the differences in levels of these metal Methylmercury was analyzed in duplicate by liquid chromatography induc-
contaminants in muscle (cheliped and body muscles) and whole- tively coupled mass spectrometry (LC–ICP-MS) (Waters 2695, Milford, MA, USA and
body tissues (all muscle, hepatopancreas, gill, brain, gonad, diges- Agilent 7500ce, Santa Clara, CA USA). Homogenates were extracted and analyzed
tive tract and all associated soft tissues) in relation to crab size and according to Hight and Cheng (2006), with the following modifications. Samples
were first screened using a liquid chromatography (LC) runtime of 20 min to
sex. This paired sampling design allowed us to assay the concentra-
determine whether propylmercury (retention time 16 min) was present. Because
tions of metals in the blue crab muscle tissues typically consumed no propylmercury was present in the samples the LC runtime was reduced to
by humans in picked crab meat. Whole-body-tissue assays were 5 min. A previously analyzed methylmercury proficiency sample was used as the
representative of the concentrations available to humans who quality control sample. The quantification standard was made fresh daily at
1 ng/ml. The LC–ICP-MS system was run under the following conditions; the
consume soft-shell crab, of which the entire body is eaten. These
high performance liquid chromatography (HPLC) mobile phase was 0.1%
whole-body concentrations are additionally helpful in understand- L-cysteine þ0.1% L-cysteinedHCldH2O. The HPLC flow rate was 1.0 ml/min and the
ing contaminant concentrations available to estuarine and marine injection volume was 50 ml. The HPLC column was a C-18 Phenomenex Synergi
predators that routinely consume blue crabs. 4 mm Hydro-RP80A (150 mm 4.6 mm). The running conditions for the Agilent
7500ce ICP-MS were; nebulizer gas flow rate was 1.2 L/min, plasma flow rate was
15 L/min and auxiliary gas flow rate was 0.9 L/min. The RF power was 1500 W. The
monitored and quantification mass was 202 m/z.
deviation
for lod and 10 baseline noise for loq. Zero was used for calculations when IHg
Mean Minimum Maximum Median Standard Mean Minimum Maximum Median Standard Mean Minimum Maximum Median Standard Mean Minimum Maximum Median Standard
results were below the detection level.
29.4
29.6
26.2
Linear regressions were used to describe relationships between crab size
(carapace width [mm] and total weight [g]) and metal concentrations (mg/g). When
appropriate, data were log-transformed to meet normality and homoscedasticity
requirements. A t-test or Mann–Whitney Rank Sum test was used, as appropriate,
122
127
110
to test for significant differences in metal concentration and sizes between males
and females and also between tissue types.
196
196
166
Carapace width (mm)
3. Results
130.7 80
113.0 75
Lagoon (IRL) on the central Atlantic coast of Florida. Of the blue
crabs examined, 35 were male and 16 were female. Four of the
females were mature and 12 were immature (based on abdomen
shape). Males were not examined internally for maturity stage, but
deviation
0.062
0.032
0.098
0.075
0.027
mature (Guillory and Hein, 1997; Guillory et al., 2001). All crabs
were at the intermolt stage. Carapace width (CW) ranged from
75 mm to 196 mm and total weight ranged from 23 g to 115 g
0.026
0.087
0.035
bloq
0.66
0.05
0.442
0.271
0.143
0.143
0.121
0.098 bloq
0.029 bdl
0.079 bdl
bdl
0.071 bdl
0.029
0.017
0.153
0.168
0.117
(Mann–Whitney rank sum test, P ¼0.004) (Fig. 1a). The blue crab
Total mercury, lead, and cadmium concentrations in blue crab, Callinectes sapidus, from the Atlantic coast of Florida.
0.054
0.061
0.017
0.011
0.011
0.381
0.139
0.139
Lead (µg/g wet weight)
0.55
0.55
males and females for either muscle tissue or whole body tissue
(P 40.05). No significant relationship was observed between
mercury concentration and carapace width (P 40.05) or total
0.019
bloq
bloq
0.019 bloq
weight (P 40.05).
bdl
0.021 bdl
0.131
0.141
0.02
0.11
Both the muscle and whole body tissues of four crabs (124–
0.048
0.065
0.046
0.053
0.072
0.065
0.046
0.061
0.06
0.05
for whole-body tissue and from 0.113 to 0.493 mg/g for muscle
Total mercury (µg/g wet weight)
0.295
0.227
0.416
0.416
(Table 2).
0.14
0.055 bloq
0.056 bloq
0.053 bloq
muscle 0.073 0.03
whole
whole
whole
body
body
body
(n ¼ 16)
Females
were all relatively small males (102 mm CW, 0.550 mg/g; 121 mm
duals
Males
Table 1
CW, 0.441 mg/g; 112 mm CW, 0.429 mg/g). All of these crabs were
all
collected during April 2010 from the same location in the southern
D.H. Adams, M.E. Engel / Ecotoxicology and Environmental Safety 102 (2014) 196–201 199
Table 2
Inorganic mercury (IHg), methylmercury (MeHg) and total mercury concentrations
and percentage methylmercury in blue crabs, Callinectes sapidus, from the Atlantic
coast of Florida.
4. Discussion
Mean cadmium concentrations (0.029 mg/g) in blue crab muscle in et al., 1981). Although metal concentrations were elevated in red
our study were generally lower than those observed in crabs from drum tissues compared with those in previous control samples of
Connecticut estuarine waters (0.05–0.40 mg/g) (Jop et al., 1997). this species, the exact causes of mortality were not determined.
Mean cadmium concentrations were also generally lower than (Cardeilhac et al., 1981).
those in composited muscle of blue crabs from Pensacola Metal transmission from blue crabs to predators is especially
( 0.07 mg/g), but these Gulf of Mexico results were classified as critical to those predators that consume large numbers of blue
bdl, with a detection limit of 0.16 mg/g (Karouna-Renier et al., crabs. One such predator is the bonnethead, Sphyrna tiburo, a small
2007). coastal species of hammerhead shark with a specialized feeding
Clear patterns of tissue-specific partitioning emerged for each ecology. This species principally consumes crabs, and blue crabs
metal contaminant type between muscle and whole-body tissue are a dominant prey item (Cortes et al., 1996; Adams and
groups. Mercury concentration was significantly higher in muscle McMichael, 1999). Bonnetheads occupy a lower trophic position
tissue than in whole body tissue. Conversely, lead and cadmium than many other shark species (Bethea et al., 2007; 2011) but in
concentrations were significantly higher in whole-body tissue Florida waters have been shown to bioaccumulate high total
than in muscle tissue. These findings are similar to those of mercury concentrations (to 1.6 mg/g in muscle) via their crab-
previous studies that found mercury concentrations in the hepa- dominated diet (Adams and McMichael, 1999; Adams et al., 2003).
topancreas of blue crabs were typically lower than in muscle tissue Because mercury accumulates in fish principally from dietary
and that lead and cadmium levels were frequently greater in the sources (Trudel and Rasmussen, 2001; Wang, 2002), blue crabs
hepatopancreas than in muscle tissue (Jop et al., 1997; Sastre et al., are an important source of mercury to this shark species.
1999; Reichmuth et al., 2010). Since the hepatopancreas is the Blue crabs are consumed by humans, and the subsequent
crab's largest organ and accounts for a significant portion of intake of mercury or other heavy metals from this species can
whole-body tissue, its overall lower mercury concentration may sometimes be significant in regard to human health (Lincoln et al.,
influence and reduce mercury in whole body tissue versus muscle 2011). Mercury in blue crab muscle can reach high concentrations,
and subsequently influence the increased lead and cadmium especially in contaminated areas such as Superfund sites and other
observed in whole body tissue versus muscle. Cadmium in the known hazardous waste sites (Reichmuth et al., 2010), but mean
water accumulates in the gills of blue crabs, and cadmium from concentrations in our study were comparatively low. Similarly,
dietary sources accumulates primarily in the hepatopancreas concentrations in whole-body tissues in our study were also
(Engel, 1983, Brouwer et al., 1995; Brouwer and Lee, 2007). typically low. These whole-body-tissue concentrations serve as
Cadmium in both the gill and hepatopancreas of blue crabs is the first results for blue crabs that are representative of contami-
bound to the metal-binding protein metallothionein (Brouwer and nant burdens that would be consumed by humans as soft-shell
Lee, 2007). This tissue-specific assimilation of cadmium may crab and by estuarine predators consuming whole crabs and can
explain why cadmium concentrations were greater in whole- be applied to multiple predator compartments within coastal
body tissues than in muscle tissue in blue crabs. systems.
Methylmercury is the most toxic form of mercury and bioac-
cumulates in many marine species (NRC, 2000). Methylmercury as
a percentage of total mercury in muscle tissue of blue crabs was Acknowledgments
initially reported to be 35% (Ward et al., 10979). A review by Evans
and Engel (1994) showed a median 63% of total mercury in blue We greatly appreciate the efforts of personnel from the FWC–
crab was methylmercury. Our results indicate that 98–100% of the FWRI Fisheries-Independent Monitoring Program in collecting
total mercury in the muscle of sampled blue crabs was methyl- blue crabs for this study. We appreciate helpful comments from
mercury; and of the total mercury in the whole-body tissue of blue B. Crowder, C. Crowley, K. Flaherty, R. Gandy, and R. Paperno that
crabs, 93–97% was methylmercury. These results are similar to improved this paper. This project was supported in part by funding
those (n¼ 3) for stone crabs, Menippe spp., from southwestern from the U.S. Department of the Interior, U.S. Fish and Wildlife
Florida waters, where approximately 92% of the total mercury was Service, Federal Aid for Sportfish Restoration Project Number F-43,
methylmercury (Thera, 2011). and by State of Florida saltwater recreational fishing license
Mercury, lead, and cadmium have no known biological function monies.
and can be toxic to marine biota. Laboratory exposure of blue crabs
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