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Heavy metals in red crabs, Chaceon quinquedens, from the Gulf of Mexico
Marine Pollution Bulletin 101 (2015) 845–851
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
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Heavy metals in red crabs, Chaceon quinquedens, from the Gulf of Mexico Harriet Perry a,⁎, Wayne Isphording b, Christine Trigg a, Ralf Riedel a a b
Gulf Coast Research Laboratory, University of Southern Mississippi, 703 East Beach Drive, Ocean Springs, MS 39564, United States University of South Alabama, 5506 Richmond Road, Mobile, AL 36608, United States
a r t i c l e
i n f o
Article history: Received 2 September 2015 Received in revised form 3 November 2015 Accepted 6 November 2015 Available online 14 November 2015 Keywords: Chaceon quinquedens Heavy metals Bioaccumulation Public health Sediment geochemistry Gulf of Mexico
a b s t r a c t The red crab, Chaceon quinquedens, is distributed in deep waters of the Gulf of Mexico (GOM) and is most abundant in an area associated with sediment deposition from the Mississippi River. Sediment geochemistry and biological and ecological traits of red crabs favor accumulation of contaminants. Red crabs, sediment, and bottom water samples were taken from three distinct geographic locations representing areas with differing exposure to contaminant laden effluents from the Mississippi River. Inductively coupled plasma spectrophotometry and atomic absorption spectrophotometry were employed to determine levels of heavy metals in red crab muscle tissue. Ion site partitioning was used to determine metal speciation in sediments. Red crabs showed evidence of heavy metal bioaccumulation in all sample areas with high variability in contaminant levels in individual crabs for some metals. Bioavailability of metals in sediment did not always result in accumulation in muscle tissue. © 2015 Elsevier Ltd. All rights reserved.
Deep water crabs of the family Geryonidae are widely distributed throughout the world's oceans (Manning and Holthuis, 1989). Crabs of the genus Chaceon (formerly Geryon) are fished for human consumption along both sides of the Atlantic Ocean including the coastal areas of southwest Africa, the eastern United States, and Bermuda (Beyers and Wilke, 1980; Lux et al., 1982; Manning and Holthuis, 1986; Erdman and Blake, 1988). Two species are known to occur in the Gulf of Mexico (GOM) and studies in the northeastern and north-central Gulf have shown a potential for limited commercial fisheries harvest (Lockhart et al., 1990; Waller et al., 1995). The red crab, Chaceon quinquedens, is widely distributed throughout the GOM (Lockhart et al., 1990; Waller et al., 1995) and is abundant off the mouth of the Mississippi River, an area impacted by freshwater run-off and its associated pollution from a major portion of the continental United States. Approximately 51% of the riverine discharge for the contiguous United States flows into the GOM with 73% of this discharge carried by the Mississippi River (Ward, 1980). The Mississippi River discharges 344 million tons of sediments into the GOM annually (Holt et al., 1982). Since its drainage encompasses areas of heavy industrialization and intense agriculture, it also carries pollutants that include heavy metals, trace elements, and organic compounds, much of which is particulate or sediment-hosted (Presley et al., 1980). More than 90% of the metal load in the Mississippi River is associated with particulate matter and the sediment has enriched levels of contaminants including Zn, Cd, and Pb (Presley et al., 1980). The River delta extends nearly 75 km across the continental shelf and the main river mouth is positioned near the shelf break. From satellite ⁎ Corresponding author. E-mail address: [email protected] (H. Perry).
http://dx.doi.org/10.1016/j.marpolbul.2015.11.020 0025-326X/© 2015 Elsevier Ltd. All rights reserved.
images, it is clear that the discharge and deposition extends beyond the shelf break, covering the upper continental slope where red crab populations exist. Heavy metal contaminants are known to concentrate in fine grain sediments (Buckley, 1972; Barnes and Rice, 1978) because these sediments have a larger particle surface area per total volume, compared to large particles, and are rich in organic matter. Both of these properties facilitate and promote greater metal adsorption. As bottom dwelling organisms, red crabs are constantly filtering fine sediment particles in the bottom mud and the water column immediately adjacent to the sediment-water interface. In addition, they are structurally adapted to dig through sediments to prey on benthic infauna. Red crabs grow slowly and are long-lived. Slow growth, a prolonged intermolt period, and their close association with the benthos (Van Heukelem et al., 1981; Lux et al., 1982; Whitlatch et al., 1990), afford this species the opportunity to assimilate heavy metals or other toxins present in sediments and in the water column. This study was initiated in response to interest in developing a commercial red crab fishery in the northern GOM. It was designed to provide information on heavy metal assimilation in Chaceon quinquedens, an organism whose biological activities were anticipated to reflect the benthic environment to which it is tied. Data were summarized in a report to the EPA upon completion of the project (Perry et al., 1998). The impetus for publication of these data was the 2010 Deep Water Horizon Oil disaster and the need for baseline information on the organisms and environment directly impacted by oil and dispersant. The data comprise a reference source against which future studies of heavy metals in the biotic and abiotic deep-sea environment can be compared and supplies information on metal/trace
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H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
element concentrations in an organism that periodically enters regional seafood markets in the GOM. The EPA Redbook (Procedures for Handling and Chemical Analysis of Sediment and Water Samples, 1981) procedures and methodologies were followed to: 1) standardize environmental sample collection, 2) secure sample integrity during collection, transport, storage, preparation, and chemical analyses, and 3) maintain data quality. Field collections, tissue dissection, and sample preparation were conducted by the Gulf Coast Research Laboratory (GCRL), University of Southern Mississippi. Microwave digestion of samples was conducted at the University of South Alabama (USA). Mercury analyses were conducted using atomic absorption (AA) spectrophotometry at the University of Southern Mississippi (USM). Full suite heavy metal analyses using inductively coupled plasma (ICP) spectrophotometry, ion site partitioning analyses (ISP), X-ray diffraction, mineralogy, and sediment size frequency distribution analyses were carried out in the Geochemistry Laboratory at the USA. Red crabs, sediment, and bottom water samples were taken from three distinct geographic locations representing areas with differing exposure to contaminant-laden effluents from the Mississippi River (Fig. 1). Rationale for site selection was based on distribution of red crabs (Lockhart et al., 1990) and prevailing patterns of water circulation and sediment deposition over the continental shelf. Area I, southeast of the mouth of the Mississippi River (28°50'N, 88°25'W), was located in a region where elevated levels of heavy metals in the sediments (composed of smectite group clays, largely montmorillonite) with enhanced ability to adsorb contaminants) would be expected (Isphording et al., 1985). Area III, located 437 km from Area I, was in the northeast GOM at 27°50'N, 85°25'W, a region characterized by kaolinitic clay sediments that are generally coarser in particle size and, typically, display a lesser ability to accumulate heavy metal contaminants. We anticipated that contaminants associated with Mississippi River flow would have minimal influence on sediment geochemistry in this Area. Area II (29°18'N, 87°32'W) was geographically intermediate between the regions of expected high and low contaminant levels.
During late August and early September 1995 collection cruises were conducted onboard the GCRL's research vessel the R/V Tommy Munro. Red crabs, sediment, and water were sampled at Area I (southeast of the Mississippi River Delta) and Area II (south of Mobile Bay, Alabama) in approximately 735 m of water. At Area III (west of Tampa Bay, Florida), red crabs were not found at this depth and a second trap line was set at 950 m. Twelve commercial plastic crab traps (Fathoms Plus®) were fished on 736 m of anchored ground tackle buoyed at a two to one scope. Soak time was approximately 18 h. Traps were baited with Atlantic croaker, Micropogonias undulatus. Upon retrieval of the trap line, the contents of each trap were removed and the crabs placed in refrigerated seawater systems containing approximately 1000 l of seawater maintained at 5 °C and 36‰ salinity. Crabs remained in the system until they were dissected. Carapace width (CW) and carapace length (CL) were recorded (±1 mm). Ten adult males and ten adult females from each of three areas (n = 60) in the eastern and northcentral GOM were individually analyzed. Mean carapace width of males was 134 ± 8 mm with a range of 119 to 150 mm compared to a mean of 116 ± 9 mm and range of 94 to 128 for female crabs. Corresponding values for carapace mean length were 113 ± 7 mm for males and 97 ± 9 mm for females (ranges = 99 to 125 mm and 78 to 111 mm for males and females, respectively). Crabs were dissected on a Teflon® dissection board. The exoskeleton was opened using high grade stainless steel scissors, and samples of gill, muscle, hepatopancreas, and gonads were removed using Teflon® and polyethylene dissection tools. The tissues were placed in 50 ml certified metal-free centrifuge tubes which were kept chilled in an ice water slurry during dissection and then frozen onboard at − 20 °C. The frozen tissues were returned to GCRL for processing. Only data for muscle tissue are reported in this paper. At each area, bottom sediments were collected with a 0.88 × 0.56 m Capetown Dredge lined with polyvinyl chloride. Approximately 1 kg of sediment was removed from the center of the dredged material. Sediment samples were placed in polyethylene sample bags, immediately purged with nitrogen in a portable glove box, and hermetically sealed
Fig. 1. Station locations for sediment, water and red crabs (Chaceon quinquedens) in the Gulf of Mexico.
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
to prevent any significant change from ambient conditions on the sea floor. Water samples were taken ~ 1 m off the bottom using a rosette sampler. Water samples were stored in 8 l Nalgene® carboys and were acidified with 5 ml of 16 N nitric acid (Baker Ultrex® II Ultrapure reagent). Sediment and water samples were kept under refrigeration at 4 °C. Frozen tissue samples were transferred to 300 ml flasks and wet weight was determined to the nearest 0.01 g using a Sartorius Model 1212 MP analytical balance. Tissues were lyophilized to constant dry weight at −42 °C and ≤33 × 10−3 millibars pressure with a Labconco Freeze Dry System/Freezone® (Model 4.5). Dried tissues were weighed, stored in sterile specimen bags, and kept in a low humidity environment at − 20 °C. Sediment and tissue samples were digested using a CEM MDS-2000 pressurized microwave digestive system. Following digestion, the tissue samples were split, and concentrations of the heavy metals were analyzed by AA or ICP spectrophotometry. Mercury levels in tissue (dry), water, and sediment (dry) were determined by AA spectrophotometry using a Varian SpectrAA Model 30 atomic absorption spectrophotometer and standard procedures. All other heavy metals/trace elements were measured by ICP spectrophotometry using a Perkin-Elmer Model 6500 Inductively Coupled Plasma Spectrophotometer. Ion site partitioning was carried out to determine the proportion of each metal bioavailable for uptake. Determination of the actual speciation (partitioning) of a metal is important, because depending upon how the metal is partitioned, it may or may not be in a form that allows its subsequent release back into the water column or its remobilization and absorption into the tissues of indigenous biota (Luoma and Bryan, 1978). Partitioning for chromium, lead, zinc, and arsenic occurring in sediment samples was carried out according to standard EPA methodology and one described by Engler et al. (1977). Selected metals were partitioned into (1) a pore water fraction, (2) an exchangeable phase, (3) an easily reducible phase, (4) a moderately reducible phase, (5) a chelated-organic and reducible sulfide phase, and (6) a structural phase. All phases except for the structural phase have the potential for uptake. Phases were analyzed by ICP spectrophotometry to determine the amount of each metal present. Extraction of the first three phases was performed with the sample in a glove box in a nitrogen atmosphere to prevent oxidation and change in the percentage of the metals in these phases. To obtain the pore water phase the sample was ultracentrifuged and the supernatant passed through a 0.45 μm filter. That portion passing through the filter was then analyzed as the pore water phase. The solid phase remaining after the original sample was centrifuged and treated by a sequential extraction technique. The exchangeable ion phase was extracted with 1 N ammonium acetate; the solid remaining treated with acidified 0.1 M hydroxylamine hydrochloride-0.01 M nitric acid solution to obtain the easily reducible phase. Following stripping of this phase, the remaining solid was treated with hydrogen peroxide and a buffered 1 N ammonium acetate solution. The filtrate was extracted to produce the organic phase. Following removal of the organic phase, the remaining solid was treated with sodium dithionate-sodium citrate solution and shaken for 17 h to extract the moderately reducible phase; any solid left after removal of this phase was treated with nitric and hydrofluoric acids to obtain the structural phase. Sediment particle size analyses were carried out using standard ASTM sieve and hydrometer methods. Measures of central tendency and dispersion were calculated for the particle size distribution and cumulative frequency plots of the size data generated. Mineral phases from sediments were identified using a SCINTAG, Model PAD2000 X-ray Diffraction System equipped with copper K-alpha radiation, a single crystal graphite monochrometer, and computerized search-match software. Bioconcentration data are provided for heavy metals and trace elements found in water, sediment, and dry tissue samples in Table 1. Twelve metals were selected for discussion based on their toxicity as defined by Wood (1974). Concentrations of cadmium, chromium, cobalt, lead, mercury, nickel, silver, zinc, vanadium, titanium, antimony, and
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the transition metal arsenic were determined for sediment and dry muscle tissue for male and female crabs by sampling area. Copper was not selected for analysis as it is part of the oxygen carrying blood protein (hemocyanin) in malacostracan crabs. Bioconcentration factors (BCF = tissue/sediment) were determined for each element using sediment and tissue dry weight values. Differences in tissue concentrations were analyzed using a two factor (area and gender) analysis of similarity (ANOSIM) with a Euclidean Distance Similarity Index (Clark, 1993). A similarity matrix was also generated for the sediment data using the same distance similarity index as above. This matrix was used to infer station separation as a function of metal concentration in the sediments. Because the USFDA uses concentration of metal in wet tissue to define levels of concern for human consumption, wet weight values were determined for muscle tissue for comparison with the USFDA guidelines (Zook et al., 1976; Hall et al., 1978). Concentrations of metals in bottom water samples were below 0.1 ppm (Table 1), with the exception of nickel in Area I. Levels of lead were 0.1 ppm in areas I, II, III; mercury was below detection limits in all areas. A strong similarity in sediment particle size was noted in Areas I and II. Using Shepard's (1954) classification, Areas I and II were characterized by silty-clay, with sediment median particle diameters of 1.505 and 1.202 μm, respectively. Both areas were rich in quartz (sand- and silt-sized material) and had similar clay mineral suites. The clay portion of the sediments in Areas I and II was dominated by the smectite group mineral montmorillonite. Montmorillonitic clays decreased from west to east. Sediments in Area III were primarily kaolinitic clays with a median particle diameter of 0.811 μm. The smaller particle size diameter of Area III sediments vs. those from Area I resulted from the fact that sediment samples from Area I contained a greater content of detrital quartz. Quartz particles are much larger than kaolinite and quartz was abundant in Area I and significantly lower in Area III. As a result, the median diameter for Area I (1.505 μm) was almost twice as large as that for Area III (0.811 μm). Differences in sediment size between Areas I and III can also be seen in the percentages of sand-siltclay. The sand and most of the silt-size component in Gulf of Mexico sediments is largely composed of quartz. Area I contained 29% sandsilt whereas Area III had only 12%. Ion site partitioning was conducted on zinc, chromium, lead, and arsenic from Area II. With the exception of arsenic, over 50% of the metals were in phases that could render them bioavailable; bioavailability of arsenic was slightly under 36% (Fig. 2). Concentration of mercury was below detection limits in sediment samples from Areas I and III and was 0.03 ppm in Area II (Table 1). Area III was well separated from Areas I and II, based on the similarity matrix for the sediment data. Euclidean distance values for the similarity matrix were 2.76, 6.06, and 5.26 between Areas I and II, I and III, and II and III, respectively. In Area 1, arsenic had the highest BCF in both male (40.15 ppm) and female (27.48 ppm) crabs. Mean levels of arsenic in tissue were high: 275 ppm in females and 402 ppm in males. Maximum levels in individual crabs were 379 ppm in females and 671 ppm in males. Zinc, silver, cadmium, and antimony showed evidence of accumulation in both sexes with BCFs less than 5.00 ppm. Lead, nickel, cobalt, titanium, and vanadium had concentration factors less than 1.0 ppm in male and female crabs. The BCF for chromium was above 1.0 in male crabs and below 1.0 in female crabs. Mercury levels in sediment were below detection limit and no concentration factors were determined. Mean mercury levels in tissue were below 1.0 ppm in both male and female tissue. As in Area I, arsenic in Area II had the highest BCF in both male (74.31 ppm) and female (58.25 ppm) crabs. Mean levels of arsenic in tissue were high: 291 ppm in females and 372 ppm in males. Maximum levels in individual crabs were 372 ppm in females and 530 ppm in males. Lead, nickel, cobalt, chromium, titanium, and vanadium had concentration factors less than 1.0 ppm in both sexes. Zinc, silver, cadmium, mercury, and antimony showed evidence of accumulation in both sexes: mean concentrations were below 4.5 ppm. Mercury levels were elevated with BCFs of 8.3 ppm in female crabs and 11.3 ppm in males.
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H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
Table 1 Metal concentrations (ppm) in water, dry red crab tissue, and sediment from the Gulf of Mexico determined by Inductively Coupled Plasma (ICP) Spectrophotometry. Mercury concentrations (ppm) determined by Atomic Absorption (AA) Spectrophotometry (Concentration factor (CF) = tissue/sediment).
Area I Water Sediment Female muscle Mean STD Min Max CF Male muscle Mean STD Min Max CF Area II Water Sediment Female muscle Mean STDS Min Max CF Male muscle Mean STD Min Max CF Area III Water Sediment Female muscle Mean STDS Min Max CF Male muscle Mean STD Min Max CF
Pb
Zn
Ag
Ni
Co
As
Cd
Sb
V
Cr
Ti
Hg
0.10 30.00
0.01 107
0.01 0.50
0.13 41.00
0.01 10.00
0.05 10.00
0.01 0.40
0.05 5.00
0.02 108
0.01 66.00
0.01 28.00
BDL BDL
11.24 0.58 10.32 12.22 0.37
226 21.96 198 261 2.11
1.12 0.06 1.03 1.22 2.25
5.78 4.71 1.12 13.53 0.14
1.12 0.06 1.03 1.22 0.11
275 58.39 210 379 27.48
1.12 0.06 1.03 1.22 2.81
6.81 2.95 5.16 14.73 1.36
1.12 0.06 1.03 1.22 0.01
6.53 8.25 1.02 22.86 0.10
1.12 0.06 1.03 1.22 0.04
0.56 0.12 0.43 0.77 –
12.54 3.85 9.90 22.89 0.42
240 36.11 206 326 2.24
1.57 0.73 1.02 3.34 3.14
26.58 34.32 0.96 108 0.65
4.42 2.49 1.06 10.26 0.44
402 129 234 671 40.15
1.14 0.12 0.99 1.35 2.85
5.80 0.64 4.95 6.76 1.16
1.14 0.12 0.99 1.35 0.01
88.69 106 12.98 296 1.34
1.14 0.12 0.99 1.35 0.04
0.36 0.11 0.23 0.51 –
0.10 23.00
0.01 90.00
0.01 0.50
0.01 43.00
0.01 9.00
0.05 5.00
0.01 0.40
0.05 5.00
0.01 89.00
0.01 58.00
0.01 24.00
BDL 0.03
17.37 9.35 10.21 33.84 0.76
214 20.40 196 253 2.38
1.29 0.42 1.02 2.10 2.58
10.50 7.56 1.02 19.05 0.24
1.50 0.53 1.02 2.19 0.17
291 56.68 215 372 58.25
1.41 0.54 1.02 2.23 3.53
5.84 0.56 5.10 6.74 1.17
1.30 0.46 1.02 2.18 0.01
6.85 5.32 2.16 20.31 0.12
2.16 0.11 2.04 2.41 0.09
0.25 0.22 0.04 0.70 8.33
12.13 3.70 10.27 22.52 0.53
206 26.38 161 238 2.28
1.21 0.37 1.03 2.25 2.43
8.10 4.77 0.96 14.74 0.19
1.98 0.47 1.12 2.42 0.22
372 81.56 258 530 74.31
1.63 0.53 1.03 2.24 4.07
5.94 1.04 5.14 8.35 1.19
1.10 0.06 1.03 1.20 0.01
5.44 4.94 1.86 16.55 0.09
2.20 0.13 2.05 2.41 0.09
0.34 0.21 0.16 0.85 11.33
0.10 8.00
0.01 47.00
0.01 0.50
0.08 35.00
0.01 4.00
0.05 5.00
0.01 0.40
0.07 5.00
0.01 33.00
0.01 23.00
BDL 8.00
BDL BDL
6.97 2.68 4.56 10.26 0.87
200 13.59 180 214 4.25
0.80 0.63 BDL 2.00 1.60
129 89.95 19.92 297 3.67
2.39 1.72 0.49 6.11 0.60
354 107 270 629 70.84
– – BDL 0.99 –
– – BDL 0.07 –
– – BDL 0.03 –
285 164 89.19 604 12.41
– – BDL BDL –
0.47 0.24 0.26 1.05 –
16.72 7.70 4.87 28.91 2.09
202 13.64 174 223 4.30
0.88 0.46 0.48 1.98 1.76
153 90.88 45.94 325 4.38
3.31 1.98 0.47 6.09 0.83
367 90.48 207 514 73.32
0.54 0.16 0.48 0.99 1.35
5.35 4.57 2.38 15.91 1.07
0.54 0.15 0.48 0.96 0.02
296 180 81.25 630 12.87
0.49 0.01 0.48 0.50 0.06
0.68 0.42 0.36 1.69 –
DL = below detection limits STD = standard deviation of the mean
Arsenic in Area III also had the highest BCF factor in both male (73.32 ppm) and female (70.84 ppm) crabs. Mean levels of arsenic in tissue were high: 354 ppm in females and 367 ppm in males. Maximum
Fig. 2. Ion site partitioning analysis of metals from Area II, northern Gulf of Mexico.
arsenic levels in individual crabs were 629 ppm in females and 514 ppm in males. Cobalt, titanium, and vanadium had concentration factors less than 1.0 ppm in both sexes; zinc, silver, and nickel, showed evidence of accumulation in both sexes with levels below 5 ppm. Chromium was elevated with a BCF of 12.41 ppm in female crabs and 12.87 in males. Lead, cadmium, and antimony had a BCF above 1.0 ppm in male crabs. Mercury levels in sediment were below detection limit. Mean mercury level in tissue was below 1.0 ppm in both male and female crabs. Areas I and II were generally similar with respect to bioconcentration factors in male and female crabs when comparing individual metals. Area II was the only site that showed mercury accumulation in tissue; however individual values for mercury were below 1.0 ppm in both male and female crabs. Arsenic was highly elevated in both sexes in all areas. Highest BCFs occurred in male crabs from Areas II and III (74.31 ppm and 73.32 ppm, respectively). Levels and bioavailability of metals in sediments were not predictors of bioaccumulation in tissue, as elevated levels of heavy metals in sediment did not always result in bioaccumulation. Although vanadium was elevated in sediment samples in all areas, particularly in Areas I and II, BCFs for male and female crabs were below 1.0 ppm. There was high variability in contaminant levels in
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
individual crabs for some metals (Table 1). Standard deviation of the mean was high for zinc in Areas I and II, nickel and chromium in Areas I and III, and arsenic in all areas. For some metals, large differences in contaminant levels were observed between male and female crabs. Results for the ANOSIM were highly significant (p b 0.01) for the two factors analyzed, indicating that gender and the three sample areas were well separated relative to the 12 metals analyzed in dry tissue (Figs. 3 and 4). Results of the ANOSIM also showed that Area III was separated from Areas I and II. Tables 2 and 3 list the U.S. Food and Drug Administration (USFDA) levels of concern (LOC) for age groups and red crab wet tissue data for GOM red crabs, respectively. The mean arsenic level in wet muscle tissue of crabs for each area was below the LOC for crustacean shellfish (86 ppm for children and 140 ppm for adult; Table 3). All areas, however, had individual crabs whose arsenic concentration exceeded the guideline for young children. Highest concentrations of arsenic occurred in individual females in Area III and males in Area I. Those levels exceeded the LOC for the 2 to 5 age group. Arsenic concentrations in individual males exceeded levels of concern for children 2 to 5 years in all areas. Mean concentrations of lead in both male and female crabs exceeded levels of concern for children ages 2 to 5 in all areas. Mean LOC for pregnant women was exceeded in female crabs in Area II and male crabs in Area III. Mean levels of chromium were elevated and exceeded the LOC in Area III in both male and female tissues. Mean levels of chromium in male crabs in Area I approached the level of concern and individual levels exceeded the LOC. Individual concentrations in some male and some female crabs greatly exceeded the LOC for children and adults. Nickel, cadmium, and mercury did not exceed the LOC in mean concentrations or in individual crabs. Particle size analyses and X-ray diffraction of sediments showed anticipated trends in clay mineralogy. Sediments in Areas I and II were composed of silty-clay, with median particle diameters of 1.505 and 1.202 μm, respectively. The clay portion of the sediment in Areas I and II was dominated by montmorillonite; sediments in Area III were primarily kaolinitic clays. Smectite-group clays (montmorillonite) have a small particle size (often b0.5 μm) and are characterized by high cation exchange capacity. Because of these properties, these clays have enhanced abilities to accumulate heavy metals and other contaminants. The predominance of such clays in the north-central Gulf was expected as a consequence of riverine input from the Mississippi River (the Mississippi carries a heavy load of smectite). There was strong similarity in sediment particle size in Areas I and II. Both areas were rich in quartz (sand- and silt-sized material) and had similar clay mineral suites. The differences seen for the particle size distributions and the mineralogy
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Fig. 4. Multidimensional Scaling plot indicating separation among sampling areas according to metal concentration in dry tissues from red crabs captured off Florida, eastern Gulf of Mexico.
seen on the X-ray diffractograms clearly reflect the provenance (source) areas for each region. Area III is composed of sediments deposited by off-shore (and longshore) currents that sweep northward along the Florida carbonate platform, while those from areas I and II are derived from weathering of source rocks in the Continental Interior and southern Appalachian Mountains and represent sediments that have been discharged into the Gulf by both the Mississippi River and the Mobile River systems. Seven of the 12 metals/trace elements listed in Table 1 were higher in sediment in Area I; lead, zinc, cobalt, arsenic, vanadium, chromium, and titanium. Two were more elevated in Area II (nickel and mercury) and there was no difference in levels of silver, cadmium and antimony among all areas. Patterns in metal concentrations in sediment were as expected based on sediment particle size distribution at the three sites. Area III was separated from Areas I and II, based on the similarity matrix for the sediment data; a separation driven by low zinc and vanadium concentrations in Area III relative to the other areas. Bioavailability of metals in sediment was not always related to bioaccumulation in muscle tissue. In Area II, sediment concentrations for lead and chromium were elevated, but tissue concentration factors were less than 1 ppm. Lead followed this pattern in Area I, nickel in Areas I and II and vanadium and titanium in all areas. The opposite pattern was also observed for some metals. Bioconcentration factors for arsenic were high although corresponding sediment concentrations were low. Sediment concentrations for silver and cadmium were below 0.6 ppm, but the metals were elevated in tissues. The availability of metals to bioaccumulate is dependent upon the concentration of the metal present in the sediment and how the metals are bound or partitioned in the sediment. Bioaccumulation is thus dependent upon the release potential associated with the metals that are partitioned in the aforementioned sites, under given conditions of Eh, pH, etc. (Isphording and Bundy, 1999) and the physiological and life history characteristics of the organism. For red crabs, age, stage in the molt cycle, and tissue type can affect levels of metals observed in the organism. Table 2 United States Food and Drug Administration guidance levels for metals in crustacean shellfish. Mean concentration levels of concern (ppm). Arsenic Cadmium Chromium Lead Nickel Mercury
Fig. 3. Multidimensional Scaling plot indicating separation among red crab gender according to metal concentration in dry tissues from red crabs captured off Florida, eastern Gulf of Mexico.
All Ages (2+ years) 2–5 years (20 kg) 18–44 years (males/females) Pregnant women Adults
140 86
6 –
22 –
– 1.2
– –
140 – –
6 – –
22 – –
8.3 2.8 –
– – 130
1
850
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
Table 3 Summary of metal concentrations (ppm) in Gulf of Mexico wet red crab tissue as determined by Inductively Coupled Plasma (ICP) Spectrophotometry. Mercury concentrations (ppm) as determined by Atomic Absorption (AA) Spectrophotometry. Pb Area I Female muscle Mean STDS Min Max Male muscle Mean STDS Min Max Area II Female muscle Mean STDS Min Max Male muscle Mean STDS Min Max Area III Female muscle Mean STDS Min Max Male muscle Mean STDS Min Max
Ni
As
Cd
Cr
Hg
2.00 0.23 1.54 2.31
1.00 0.80 0.20 2.11
48.99 12.70 37.49 72.93
0.20 0.02 0.15 0.23
1.11 1.41 0.19 4.16
0.10 0.02 0.08 0.15
2.30 0.76 1.75 4.36
4.76 6.01 0.17 18.51
73.43 24.43 43.94 124.97
0.21 0.02 0.17 0.25
15.91 18.94 2.29 50.96
0.07 0.02 0.04 0.10
3.21 1.73 1.75 6.31
1.96 1.44 0.19 3.63
53.87 10.88 38.74 68.84
0.26 0.11 0.17 0.43
1.27 1.00 0.42 3.79
0.05 0.04 0.01 0.13
2.24 0.77 1.75 4.35
1.48 0.87 0.19 2.86
67.95 13.37 48.19 90.58
0.30 0.10 0.17 0.43
1.02 0.95 0.31 3.11
0.06 0.04 0.03 0.16
1.41 0.59 0.91 2.28
25.76 17.99 3.67 59.67
70.79 20.82 52.57 118.85
– – BDL 0.23
57.09 32.87 16.43 121.46
0.09 0.05 0.05 0.19
3.33 1.55 0.96 5.73
30.53 17.87 8.89 62.25
72.87 18.72 42.16 103.38
0.11 0.03 0.09 0.19
58.95 35.37 15.73 120.83
0.14 0.09 0.07 0.35
BDL = Below Detection Limit
Chromium, lead, zinc, and arsenic were partitioned from sediment taken in Area II. With the exception of arsenic, over 50% of the metals were present in phases that could render them bioavailable; bioavailability of arsenic was slightly under 36%. Bioconcentration factors for
lead and chromium were less than one. Arsenic (BCF = 58.25♀, CF = 74.31♂) and zinc (BCF = 2.38♀, CF = 2.28♂) concentrations were elevated in both male and female crabs. Knowing how the metals were partitioned in the sediment was not a predictor of bioaccumulation, in that there were no consistent patterns between levels in sediment and tissue. While sediment concentrations for most metals were highest in Area I, red crab dry tissue concentrations did not follow a similar trend. We expected, but did not find, that crabs from Area III would show less evidence of bioaccumulation than crabs from Areas I and II. Eleven of the BCFs in Area I were above 1, twelve in Area II, and thirteen in Area III. Area III was distinct from the other two areas due primarily to extremely high tissue concentrations of chromium and nickel. Results for the ANOSIM were highly significant (p b 0.01), indicating that the three sample areas were well separated relative to the 12 metals analyzed in dry tissue. Gender also separated well, according to ANOSIM results. Most of the separation was due to the higher contamination found in males for some metals, especially arsenic, cobalt, and chromium. There are few studies on heavy metal/trace element levels in the red crab. Greig et al. (1976) provided data on heavy metals in red crab muscle tissue from a deepwater disposal site in the Middle Atlantic Bight. Mean concentrations of lead, nickel, arsenic, cadmium, chromium, mercury, zinc, and silver in wet tissue were determined (n = 7). Mean levels of cadmium and silver were similar to levels found in crabs from the GOM with concentrations of mercury and zinc lower in GOM samples. Higher levels of lead and extremely high levels of nickel, arsenic, and chromium were found in GOM crabs when compared to crabs from the Atlantic (Table 4). Bioaccumulation is a highly complex phenomenon that depends not only upon the species and their genetic adaptation to specific locations, but also involves climate, season, and the synergistic and antagonistic effects of other metals and organic compounds that may be present (Sager, 1989). A variety of defensive and resistance mechanisms have evolved to protect biota from toxic effects of heavy metals. These include complexation of metals to organic ligands, volatilization, alkylation, and a number of other adaptive physico-chemical mechanisms (Wood, 1974). Studies to date dealing with bioaccumulation of heavy metals in marine animals have dealt primarily with fish and mollusks. Fewer studies have been conducted with crustaceans. In 1993, the USFDA produced
Table 4 Comparison of metal concentrations (ppm) in sediment and muscle tissue (wet) in red crabs from the Gulf of Mexico (this study) and the Middle Atlantic Bight (Greig et al., 1976).
Gulf of Mexico Area I Sediment Female muscle Mean Male muscle Mean Area II Water Sediment Female muscle Mean Male muscle Mean Area III Sediment Female muscle Mean Male muscle Mean Middle Atlantic Bight Sediment Muscle Mean
Pb
Zn
Ag
Ni
As
30.00
107
0.50
41.00
10.00
Cd
Cr
Hg
0.40
66.00
BDL
2.0
39.92
0.20
1.00
48.99
0.20
1.11
0.10
2.30
44.00
0.29
4.76
73.43
0.21
15.91
0.07
0.10 23.00
0.01 90.00
0.01 0.50
0.01 43.00
0.05 5.00
0.01 0.40
0.01 58.00
BDL 0.03
3.21
39.56
0.24
1.96
53.87
0.26
1.27
0.05
2.24
37.85
0.22
1.48
67.95
0.30
1.02
0.06
8.00
47.00
0.50
35.00
5.00
0.40
23.00
BDL
1.41
39.96
0.16
25.76
70.79
–
57.09
0.09
3.33
40.16
0.17
30.53
72.87
0.11
58.95
0.14
7.5–15.0
19.5–47.8
ND
b7.4–33.1
ND
b1.25
6.0–16.7
ND
b1.00
69.00
b0.13
b0.48
1.60
b0.10
b0.51
0.23
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
guidelines for heavy metal concentrations of arsenic, cadmium, chromium, nickel, and lead in species of shellfish. These guidelines, based on the work of Zook et al. (1976) and Hall et al. (1978), established provisional tolerable total intake levels for various population groups. In Area III, chromium levels in muscle tissue were above the USFDA's level of concern (22 ppm). In all areas, lead was above the USFDA's level of concern for children 2–5 and for pregnant women in areas II and III. Lead level of concern for pregnant women was detected for females in Area II and males in Area III. Nickel, cadmium, and mercury levels were below the USFDA's level of concern for these metals. Levels of concern for other metals have not been established. High variability in levels of contaminants in individual crabs was noted for zinc, nickel, arsenic and chromium. If a fishery for red crabs were to develop in the GOM, it would be advisable to re-sample the population to more accurately characterize metal burdens and to periodically monitor the catch for those heavy metals known to bioaccumulate in muscle tissue.
Acknowledgments We would like to thank the United States Environmental Protection Agency/Gulf of Mexico Program for funding the original project (Project Identification Number MX 994731-95-0, 1995–1998) that led to the development of the current manuscript. Renee Bishop, Dick Waller, and Frank Frumar aided in field collections and we are grateful for their assistance. While the data in this study have been available in a completion report and circulated in the “gray” literature for many years, publishing the information makes it available to the larger scientific community. Additionally, acceptance of the data in a peer reviewed format places greater emphasis on the need for consideration of regulatory measures for the fishery in light of levels of chromium and lead above USFDA consumption guidelines in some tissues. These data also provide baseline information on heavy metals/trace elements in organisms whose habitat was directly impacted by oil and dispersant from the Deepwater Horizon Oil Spill.
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Engler, R., Brannon, J., Rose, J., Bigham, G., 1977. A practical selective extraction procedure for sediment characterization. In: Yen, T.F. (Ed.), Chemistry of Marine Sediments Ann Arbor Science, Michigan, pp. 163–180. Erdman, R., Blake, N., 1988. The golden crab (Geryon fenneri) fishery of southeast Florida. Proc. 12th Ann. Trop. Subtrop. Fish. Conf. Amer. FL Sea Grant College Report 92, pp. 95–106. Greig, R., Wenzloff, D., Pearce, J., 1976. Distribution and abundance of heavy metals in finfish, invertebrates and sediments collected at a deepwater disposal site. Mar. Pollut. Bull. 7 (10), 185–187. Hall, R., Zook, E., Meaburn, G., 1978. National marine fisheries service survey of trace elements in the fishery resource. NOAA Technical Report NMFS SSRF-721. USDC, NOAA, National Marine Fisheries Service. Holt, J., Bartz, M., Lehman, J., 1982. Draft Regional Environmental Impact Statement, Gulf of Mexico. Minerals Management Service, Gulf of Mexico OCS Region, Metairie, Louisiana (735 pp.). Isphording, W., Bundy, M., 1999. The dilemma of assessing heavy metal toxicity. Trans. Gulf Coast Assoc. Geol. Soc. 49, 282–291. Isphording, W., Stringfellow, J., Flowers, G., 1985. Sedimentary and geochemical systems in transitional marine sediments in the northeastern Gulf of Mexico. Trans. Gulf Coast Assoc. Geol. Soc. 35, 397–408. Lockhart, F., Lindberg, W., Blake, N., Erdman, R., Perry, H., Waller, R., 1990. Distributional differences and population similarities for two deep-sea crabs (family Geryonidae) in the northeastern Gulf of Mexico. Can. J. Fish. Aquat. Sci. 47 (11), 2112–2122. Luoma, S., Bryan, G., 1978. Factors controlling the availability of sediment-bound lead to the estuarine bivalve Scrobicularia plana. J. Mar. Biol. Assoc. U. K. 58, 793–802. Lux, F., Ganz, A., Rathjen, W., 1982. Marking studies of the red crab Geryon quinquedens Smith off southern New England. J. Shellfish Res. 2, 71–80. Manning, R., Holthuis, L., 1986. Notes on Geryon from Bermuda, with the description of Geryon inghami, new species (Crustacea: Decapoda: Geryonidae). Proc. Biol. Soc. Wash. 99 (2), 366–373. Manning, R., Holthuis, L., 1989. Two new genera and nine new species of geryonid crabs (Crustacea, Decapoda, Geryonidae). Proc. Biol. Soc. Wash. 102 (1), 50–77. Perry, H., Trigg, C., Waller, R., Isphording, W., Fawcett, N., 1998. Bioavailability of heavy metals to red crabs, Chaceon quinquedens. Final Report to the EPA, Project Number MX 994731-95-0. Presley, B., Trefry, J., Shokes, R., 1980. Heavy metal inputs to Mississippi Delta sediments. Water Air Soil Pollut. 13, 481–494. Sager, M., 1989. The speciation of heavy metals in river sediments found by sequential leaching methods. In: Vernet, J.P. (Ed.), Heavy Metals in the Environment, pp. 213–216. Shepard, F., 1954. Nomenclature based on sand-silt-clay ratios. J. Sediment. Petrol. 24, 151–158. Van Heukelem, W., Christman, M., Epifanio, C., Sulkin, S., 1981. Growth of Geryon quinquedens (Brachyura: Geryonidae) juveniles in the laboratory. Fish. Bull. 81 (4), 903–905. Waller, R., Perry, H., Trigg, C., McBee, J., Erdman, R., Blake, N., 1995. Estimates of harvest potential of the deep sea red crab, Chaceon quinquedens, in the North Central Gulf of Mexico. Gulf Res. Rep. 9 (2), 75–84. Ward, G., 1980. Hydrography and circulation processes of Gulf estuaries. In: Hamilton, P., MacDonald, K.B. (Eds.), Estuarine and Wetland Processes. Plenum Press, New York, pp. 183–215. Whitlatch, R., Grassle, J., Boyer, L., Zajac, R., 1990. Animal-sediment relationships involving red crabs (Chaceon quinquedens) on the southern New England upper continental slope. In: Lindberg, W., Wenner, E. (Eds.), Geryonid Crabs and Associated Continental Slope Fauna: A Research Workshop Report, SC Sea Grant Consortium Technical Paper 58, pp. 3–5. Wood, J., 1974. Biological cycles for toxic elements in the environment. Science 183, 1049–1052. Zook, E., Powell, J., Hackley, B., Emerson, J., Booker, J., Knoble Jr., G., 1976. National Marine Fisheries Service preliminary survey of selected seafoods for mercury, lead, cadmium, chromium, and arsenic content. J. Agric. Food Chem. 24 (1), 47–53.
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Baseline
Heavy metals in red crabs, Chaceon quinquedens, from the Gulf of Mexico Harriet Perry a,⁎, Wayne Isphording b, Christine Trigg a, Ralf Riedel a a b
Gulf Coast Research Laboratory, University of Southern Mississippi, 703 East Beach Drive, Ocean Springs, MS 39564, United States University of South Alabama, 5506 Richmond Road, Mobile, AL 36608, United States
a r t i c l e
i n f o
Article history: Received 2 September 2015 Received in revised form 3 November 2015 Accepted 6 November 2015 Available online 14 November 2015 Keywords: Chaceon quinquedens Heavy metals Bioaccumulation Public health Sediment geochemistry Gulf of Mexico
a b s t r a c t The red crab, Chaceon quinquedens, is distributed in deep waters of the Gulf of Mexico (GOM) and is most abundant in an area associated with sediment deposition from the Mississippi River. Sediment geochemistry and biological and ecological traits of red crabs favor accumulation of contaminants. Red crabs, sediment, and bottom water samples were taken from three distinct geographic locations representing areas with differing exposure to contaminant laden effluents from the Mississippi River. Inductively coupled plasma spectrophotometry and atomic absorption spectrophotometry were employed to determine levels of heavy metals in red crab muscle tissue. Ion site partitioning was used to determine metal speciation in sediments. Red crabs showed evidence of heavy metal bioaccumulation in all sample areas with high variability in contaminant levels in individual crabs for some metals. Bioavailability of metals in sediment did not always result in accumulation in muscle tissue. © 2015 Elsevier Ltd. All rights reserved.
Deep water crabs of the family Geryonidae are widely distributed throughout the world's oceans (Manning and Holthuis, 1989). Crabs of the genus Chaceon (formerly Geryon) are fished for human consumption along both sides of the Atlantic Ocean including the coastal areas of southwest Africa, the eastern United States, and Bermuda (Beyers and Wilke, 1980; Lux et al., 1982; Manning and Holthuis, 1986; Erdman and Blake, 1988). Two species are known to occur in the Gulf of Mexico (GOM) and studies in the northeastern and north-central Gulf have shown a potential for limited commercial fisheries harvest (Lockhart et al., 1990; Waller et al., 1995). The red crab, Chaceon quinquedens, is widely distributed throughout the GOM (Lockhart et al., 1990; Waller et al., 1995) and is abundant off the mouth of the Mississippi River, an area impacted by freshwater run-off and its associated pollution from a major portion of the continental United States. Approximately 51% of the riverine discharge for the contiguous United States flows into the GOM with 73% of this discharge carried by the Mississippi River (Ward, 1980). The Mississippi River discharges 344 million tons of sediments into the GOM annually (Holt et al., 1982). Since its drainage encompasses areas of heavy industrialization and intense agriculture, it also carries pollutants that include heavy metals, trace elements, and organic compounds, much of which is particulate or sediment-hosted (Presley et al., 1980). More than 90% of the metal load in the Mississippi River is associated with particulate matter and the sediment has enriched levels of contaminants including Zn, Cd, and Pb (Presley et al., 1980). The River delta extends nearly 75 km across the continental shelf and the main river mouth is positioned near the shelf break. From satellite ⁎ Corresponding author. E-mail address: [email protected] (H. Perry).
http://dx.doi.org/10.1016/j.marpolbul.2015.11.020 0025-326X/© 2015 Elsevier Ltd. All rights reserved.
images, it is clear that the discharge and deposition extends beyond the shelf break, covering the upper continental slope where red crab populations exist. Heavy metal contaminants are known to concentrate in fine grain sediments (Buckley, 1972; Barnes and Rice, 1978) because these sediments have a larger particle surface area per total volume, compared to large particles, and are rich in organic matter. Both of these properties facilitate and promote greater metal adsorption. As bottom dwelling organisms, red crabs are constantly filtering fine sediment particles in the bottom mud and the water column immediately adjacent to the sediment-water interface. In addition, they are structurally adapted to dig through sediments to prey on benthic infauna. Red crabs grow slowly and are long-lived. Slow growth, a prolonged intermolt period, and their close association with the benthos (Van Heukelem et al., 1981; Lux et al., 1982; Whitlatch et al., 1990), afford this species the opportunity to assimilate heavy metals or other toxins present in sediments and in the water column. This study was initiated in response to interest in developing a commercial red crab fishery in the northern GOM. It was designed to provide information on heavy metal assimilation in Chaceon quinquedens, an organism whose biological activities were anticipated to reflect the benthic environment to which it is tied. Data were summarized in a report to the EPA upon completion of the project (Perry et al., 1998). The impetus for publication of these data was the 2010 Deep Water Horizon Oil disaster and the need for baseline information on the organisms and environment directly impacted by oil and dispersant. The data comprise a reference source against which future studies of heavy metals in the biotic and abiotic deep-sea environment can be compared and supplies information on metal/trace
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element concentrations in an organism that periodically enters regional seafood markets in the GOM. The EPA Redbook (Procedures for Handling and Chemical Analysis of Sediment and Water Samples, 1981) procedures and methodologies were followed to: 1) standardize environmental sample collection, 2) secure sample integrity during collection, transport, storage, preparation, and chemical analyses, and 3) maintain data quality. Field collections, tissue dissection, and sample preparation were conducted by the Gulf Coast Research Laboratory (GCRL), University of Southern Mississippi. Microwave digestion of samples was conducted at the University of South Alabama (USA). Mercury analyses were conducted using atomic absorption (AA) spectrophotometry at the University of Southern Mississippi (USM). Full suite heavy metal analyses using inductively coupled plasma (ICP) spectrophotometry, ion site partitioning analyses (ISP), X-ray diffraction, mineralogy, and sediment size frequency distribution analyses were carried out in the Geochemistry Laboratory at the USA. Red crabs, sediment, and bottom water samples were taken from three distinct geographic locations representing areas with differing exposure to contaminant-laden effluents from the Mississippi River (Fig. 1). Rationale for site selection was based on distribution of red crabs (Lockhart et al., 1990) and prevailing patterns of water circulation and sediment deposition over the continental shelf. Area I, southeast of the mouth of the Mississippi River (28°50'N, 88°25'W), was located in a region where elevated levels of heavy metals in the sediments (composed of smectite group clays, largely montmorillonite) with enhanced ability to adsorb contaminants) would be expected (Isphording et al., 1985). Area III, located 437 km from Area I, was in the northeast GOM at 27°50'N, 85°25'W, a region characterized by kaolinitic clay sediments that are generally coarser in particle size and, typically, display a lesser ability to accumulate heavy metal contaminants. We anticipated that contaminants associated with Mississippi River flow would have minimal influence on sediment geochemistry in this Area. Area II (29°18'N, 87°32'W) was geographically intermediate between the regions of expected high and low contaminant levels.
During late August and early September 1995 collection cruises were conducted onboard the GCRL's research vessel the R/V Tommy Munro. Red crabs, sediment, and water were sampled at Area I (southeast of the Mississippi River Delta) and Area II (south of Mobile Bay, Alabama) in approximately 735 m of water. At Area III (west of Tampa Bay, Florida), red crabs were not found at this depth and a second trap line was set at 950 m. Twelve commercial plastic crab traps (Fathoms Plus®) were fished on 736 m of anchored ground tackle buoyed at a two to one scope. Soak time was approximately 18 h. Traps were baited with Atlantic croaker, Micropogonias undulatus. Upon retrieval of the trap line, the contents of each trap were removed and the crabs placed in refrigerated seawater systems containing approximately 1000 l of seawater maintained at 5 °C and 36‰ salinity. Crabs remained in the system until they were dissected. Carapace width (CW) and carapace length (CL) were recorded (±1 mm). Ten adult males and ten adult females from each of three areas (n = 60) in the eastern and northcentral GOM were individually analyzed. Mean carapace width of males was 134 ± 8 mm with a range of 119 to 150 mm compared to a mean of 116 ± 9 mm and range of 94 to 128 for female crabs. Corresponding values for carapace mean length were 113 ± 7 mm for males and 97 ± 9 mm for females (ranges = 99 to 125 mm and 78 to 111 mm for males and females, respectively). Crabs were dissected on a Teflon® dissection board. The exoskeleton was opened using high grade stainless steel scissors, and samples of gill, muscle, hepatopancreas, and gonads were removed using Teflon® and polyethylene dissection tools. The tissues were placed in 50 ml certified metal-free centrifuge tubes which were kept chilled in an ice water slurry during dissection and then frozen onboard at − 20 °C. The frozen tissues were returned to GCRL for processing. Only data for muscle tissue are reported in this paper. At each area, bottom sediments were collected with a 0.88 × 0.56 m Capetown Dredge lined with polyvinyl chloride. Approximately 1 kg of sediment was removed from the center of the dredged material. Sediment samples were placed in polyethylene sample bags, immediately purged with nitrogen in a portable glove box, and hermetically sealed
Fig. 1. Station locations for sediment, water and red crabs (Chaceon quinquedens) in the Gulf of Mexico.
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
to prevent any significant change from ambient conditions on the sea floor. Water samples were taken ~ 1 m off the bottom using a rosette sampler. Water samples were stored in 8 l Nalgene® carboys and were acidified with 5 ml of 16 N nitric acid (Baker Ultrex® II Ultrapure reagent). Sediment and water samples were kept under refrigeration at 4 °C. Frozen tissue samples were transferred to 300 ml flasks and wet weight was determined to the nearest 0.01 g using a Sartorius Model 1212 MP analytical balance. Tissues were lyophilized to constant dry weight at −42 °C and ≤33 × 10−3 millibars pressure with a Labconco Freeze Dry System/Freezone® (Model 4.5). Dried tissues were weighed, stored in sterile specimen bags, and kept in a low humidity environment at − 20 °C. Sediment and tissue samples were digested using a CEM MDS-2000 pressurized microwave digestive system. Following digestion, the tissue samples were split, and concentrations of the heavy metals were analyzed by AA or ICP spectrophotometry. Mercury levels in tissue (dry), water, and sediment (dry) were determined by AA spectrophotometry using a Varian SpectrAA Model 30 atomic absorption spectrophotometer and standard procedures. All other heavy metals/trace elements were measured by ICP spectrophotometry using a Perkin-Elmer Model 6500 Inductively Coupled Plasma Spectrophotometer. Ion site partitioning was carried out to determine the proportion of each metal bioavailable for uptake. Determination of the actual speciation (partitioning) of a metal is important, because depending upon how the metal is partitioned, it may or may not be in a form that allows its subsequent release back into the water column or its remobilization and absorption into the tissues of indigenous biota (Luoma and Bryan, 1978). Partitioning for chromium, lead, zinc, and arsenic occurring in sediment samples was carried out according to standard EPA methodology and one described by Engler et al. (1977). Selected metals were partitioned into (1) a pore water fraction, (2) an exchangeable phase, (3) an easily reducible phase, (4) a moderately reducible phase, (5) a chelated-organic and reducible sulfide phase, and (6) a structural phase. All phases except for the structural phase have the potential for uptake. Phases were analyzed by ICP spectrophotometry to determine the amount of each metal present. Extraction of the first three phases was performed with the sample in a glove box in a nitrogen atmosphere to prevent oxidation and change in the percentage of the metals in these phases. To obtain the pore water phase the sample was ultracentrifuged and the supernatant passed through a 0.45 μm filter. That portion passing through the filter was then analyzed as the pore water phase. The solid phase remaining after the original sample was centrifuged and treated by a sequential extraction technique. The exchangeable ion phase was extracted with 1 N ammonium acetate; the solid remaining treated with acidified 0.1 M hydroxylamine hydrochloride-0.01 M nitric acid solution to obtain the easily reducible phase. Following stripping of this phase, the remaining solid was treated with hydrogen peroxide and a buffered 1 N ammonium acetate solution. The filtrate was extracted to produce the organic phase. Following removal of the organic phase, the remaining solid was treated with sodium dithionate-sodium citrate solution and shaken for 17 h to extract the moderately reducible phase; any solid left after removal of this phase was treated with nitric and hydrofluoric acids to obtain the structural phase. Sediment particle size analyses were carried out using standard ASTM sieve and hydrometer methods. Measures of central tendency and dispersion were calculated for the particle size distribution and cumulative frequency plots of the size data generated. Mineral phases from sediments were identified using a SCINTAG, Model PAD2000 X-ray Diffraction System equipped with copper K-alpha radiation, a single crystal graphite monochrometer, and computerized search-match software. Bioconcentration data are provided for heavy metals and trace elements found in water, sediment, and dry tissue samples in Table 1. Twelve metals were selected for discussion based on their toxicity as defined by Wood (1974). Concentrations of cadmium, chromium, cobalt, lead, mercury, nickel, silver, zinc, vanadium, titanium, antimony, and
847
the transition metal arsenic were determined for sediment and dry muscle tissue for male and female crabs by sampling area. Copper was not selected for analysis as it is part of the oxygen carrying blood protein (hemocyanin) in malacostracan crabs. Bioconcentration factors (BCF = tissue/sediment) were determined for each element using sediment and tissue dry weight values. Differences in tissue concentrations were analyzed using a two factor (area and gender) analysis of similarity (ANOSIM) with a Euclidean Distance Similarity Index (Clark, 1993). A similarity matrix was also generated for the sediment data using the same distance similarity index as above. This matrix was used to infer station separation as a function of metal concentration in the sediments. Because the USFDA uses concentration of metal in wet tissue to define levels of concern for human consumption, wet weight values were determined for muscle tissue for comparison with the USFDA guidelines (Zook et al., 1976; Hall et al., 1978). Concentrations of metals in bottom water samples were below 0.1 ppm (Table 1), with the exception of nickel in Area I. Levels of lead were 0.1 ppm in areas I, II, III; mercury was below detection limits in all areas. A strong similarity in sediment particle size was noted in Areas I and II. Using Shepard's (1954) classification, Areas I and II were characterized by silty-clay, with sediment median particle diameters of 1.505 and 1.202 μm, respectively. Both areas were rich in quartz (sand- and silt-sized material) and had similar clay mineral suites. The clay portion of the sediments in Areas I and II was dominated by the smectite group mineral montmorillonite. Montmorillonitic clays decreased from west to east. Sediments in Area III were primarily kaolinitic clays with a median particle diameter of 0.811 μm. The smaller particle size diameter of Area III sediments vs. those from Area I resulted from the fact that sediment samples from Area I contained a greater content of detrital quartz. Quartz particles are much larger than kaolinite and quartz was abundant in Area I and significantly lower in Area III. As a result, the median diameter for Area I (1.505 μm) was almost twice as large as that for Area III (0.811 μm). Differences in sediment size between Areas I and III can also be seen in the percentages of sand-siltclay. The sand and most of the silt-size component in Gulf of Mexico sediments is largely composed of quartz. Area I contained 29% sandsilt whereas Area III had only 12%. Ion site partitioning was conducted on zinc, chromium, lead, and arsenic from Area II. With the exception of arsenic, over 50% of the metals were in phases that could render them bioavailable; bioavailability of arsenic was slightly under 36% (Fig. 2). Concentration of mercury was below detection limits in sediment samples from Areas I and III and was 0.03 ppm in Area II (Table 1). Area III was well separated from Areas I and II, based on the similarity matrix for the sediment data. Euclidean distance values for the similarity matrix were 2.76, 6.06, and 5.26 between Areas I and II, I and III, and II and III, respectively. In Area 1, arsenic had the highest BCF in both male (40.15 ppm) and female (27.48 ppm) crabs. Mean levels of arsenic in tissue were high: 275 ppm in females and 402 ppm in males. Maximum levels in individual crabs were 379 ppm in females and 671 ppm in males. Zinc, silver, cadmium, and antimony showed evidence of accumulation in both sexes with BCFs less than 5.00 ppm. Lead, nickel, cobalt, titanium, and vanadium had concentration factors less than 1.0 ppm in male and female crabs. The BCF for chromium was above 1.0 in male crabs and below 1.0 in female crabs. Mercury levels in sediment were below detection limit and no concentration factors were determined. Mean mercury levels in tissue were below 1.0 ppm in both male and female tissue. As in Area I, arsenic in Area II had the highest BCF in both male (74.31 ppm) and female (58.25 ppm) crabs. Mean levels of arsenic in tissue were high: 291 ppm in females and 372 ppm in males. Maximum levels in individual crabs were 372 ppm in females and 530 ppm in males. Lead, nickel, cobalt, chromium, titanium, and vanadium had concentration factors less than 1.0 ppm in both sexes. Zinc, silver, cadmium, mercury, and antimony showed evidence of accumulation in both sexes: mean concentrations were below 4.5 ppm. Mercury levels were elevated with BCFs of 8.3 ppm in female crabs and 11.3 ppm in males.
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Table 1 Metal concentrations (ppm) in water, dry red crab tissue, and sediment from the Gulf of Mexico determined by Inductively Coupled Plasma (ICP) Spectrophotometry. Mercury concentrations (ppm) determined by Atomic Absorption (AA) Spectrophotometry (Concentration factor (CF) = tissue/sediment).
Area I Water Sediment Female muscle Mean STD Min Max CF Male muscle Mean STD Min Max CF Area II Water Sediment Female muscle Mean STDS Min Max CF Male muscle Mean STD Min Max CF Area III Water Sediment Female muscle Mean STDS Min Max CF Male muscle Mean STD Min Max CF
Pb
Zn
Ag
Ni
Co
As
Cd
Sb
V
Cr
Ti
Hg
0.10 30.00
0.01 107
0.01 0.50
0.13 41.00
0.01 10.00
0.05 10.00
0.01 0.40
0.05 5.00
0.02 108
0.01 66.00
0.01 28.00
BDL BDL
11.24 0.58 10.32 12.22 0.37
226 21.96 198 261 2.11
1.12 0.06 1.03 1.22 2.25
5.78 4.71 1.12 13.53 0.14
1.12 0.06 1.03 1.22 0.11
275 58.39 210 379 27.48
1.12 0.06 1.03 1.22 2.81
6.81 2.95 5.16 14.73 1.36
1.12 0.06 1.03 1.22 0.01
6.53 8.25 1.02 22.86 0.10
1.12 0.06 1.03 1.22 0.04
0.56 0.12 0.43 0.77 –
12.54 3.85 9.90 22.89 0.42
240 36.11 206 326 2.24
1.57 0.73 1.02 3.34 3.14
26.58 34.32 0.96 108 0.65
4.42 2.49 1.06 10.26 0.44
402 129 234 671 40.15
1.14 0.12 0.99 1.35 2.85
5.80 0.64 4.95 6.76 1.16
1.14 0.12 0.99 1.35 0.01
88.69 106 12.98 296 1.34
1.14 0.12 0.99 1.35 0.04
0.36 0.11 0.23 0.51 –
0.10 23.00
0.01 90.00
0.01 0.50
0.01 43.00
0.01 9.00
0.05 5.00
0.01 0.40
0.05 5.00
0.01 89.00
0.01 58.00
0.01 24.00
BDL 0.03
17.37 9.35 10.21 33.84 0.76
214 20.40 196 253 2.38
1.29 0.42 1.02 2.10 2.58
10.50 7.56 1.02 19.05 0.24
1.50 0.53 1.02 2.19 0.17
291 56.68 215 372 58.25
1.41 0.54 1.02 2.23 3.53
5.84 0.56 5.10 6.74 1.17
1.30 0.46 1.02 2.18 0.01
6.85 5.32 2.16 20.31 0.12
2.16 0.11 2.04 2.41 0.09
0.25 0.22 0.04 0.70 8.33
12.13 3.70 10.27 22.52 0.53
206 26.38 161 238 2.28
1.21 0.37 1.03 2.25 2.43
8.10 4.77 0.96 14.74 0.19
1.98 0.47 1.12 2.42 0.22
372 81.56 258 530 74.31
1.63 0.53 1.03 2.24 4.07
5.94 1.04 5.14 8.35 1.19
1.10 0.06 1.03 1.20 0.01
5.44 4.94 1.86 16.55 0.09
2.20 0.13 2.05 2.41 0.09
0.34 0.21 0.16 0.85 11.33
0.10 8.00
0.01 47.00
0.01 0.50
0.08 35.00
0.01 4.00
0.05 5.00
0.01 0.40
0.07 5.00
0.01 33.00
0.01 23.00
BDL 8.00
BDL BDL
6.97 2.68 4.56 10.26 0.87
200 13.59 180 214 4.25
0.80 0.63 BDL 2.00 1.60
129 89.95 19.92 297 3.67
2.39 1.72 0.49 6.11 0.60
354 107 270 629 70.84
– – BDL 0.99 –
– – BDL 0.07 –
– – BDL 0.03 –
285 164 89.19 604 12.41
– – BDL BDL –
0.47 0.24 0.26 1.05 –
16.72 7.70 4.87 28.91 2.09
202 13.64 174 223 4.30
0.88 0.46 0.48 1.98 1.76
153 90.88 45.94 325 4.38
3.31 1.98 0.47 6.09 0.83
367 90.48 207 514 73.32
0.54 0.16 0.48 0.99 1.35
5.35 4.57 2.38 15.91 1.07
0.54 0.15 0.48 0.96 0.02
296 180 81.25 630 12.87
0.49 0.01 0.48 0.50 0.06
0.68 0.42 0.36 1.69 –
DL = below detection limits STD = standard deviation of the mean
Arsenic in Area III also had the highest BCF factor in both male (73.32 ppm) and female (70.84 ppm) crabs. Mean levels of arsenic in tissue were high: 354 ppm in females and 367 ppm in males. Maximum
Fig. 2. Ion site partitioning analysis of metals from Area II, northern Gulf of Mexico.
arsenic levels in individual crabs were 629 ppm in females and 514 ppm in males. Cobalt, titanium, and vanadium had concentration factors less than 1.0 ppm in both sexes; zinc, silver, and nickel, showed evidence of accumulation in both sexes with levels below 5 ppm. Chromium was elevated with a BCF of 12.41 ppm in female crabs and 12.87 in males. Lead, cadmium, and antimony had a BCF above 1.0 ppm in male crabs. Mercury levels in sediment were below detection limit. Mean mercury level in tissue was below 1.0 ppm in both male and female crabs. Areas I and II were generally similar with respect to bioconcentration factors in male and female crabs when comparing individual metals. Area II was the only site that showed mercury accumulation in tissue; however individual values for mercury were below 1.0 ppm in both male and female crabs. Arsenic was highly elevated in both sexes in all areas. Highest BCFs occurred in male crabs from Areas II and III (74.31 ppm and 73.32 ppm, respectively). Levels and bioavailability of metals in sediments were not predictors of bioaccumulation in tissue, as elevated levels of heavy metals in sediment did not always result in bioaccumulation. Although vanadium was elevated in sediment samples in all areas, particularly in Areas I and II, BCFs for male and female crabs were below 1.0 ppm. There was high variability in contaminant levels in
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
individual crabs for some metals (Table 1). Standard deviation of the mean was high for zinc in Areas I and II, nickel and chromium in Areas I and III, and arsenic in all areas. For some metals, large differences in contaminant levels were observed between male and female crabs. Results for the ANOSIM were highly significant (p b 0.01) for the two factors analyzed, indicating that gender and the three sample areas were well separated relative to the 12 metals analyzed in dry tissue (Figs. 3 and 4). Results of the ANOSIM also showed that Area III was separated from Areas I and II. Tables 2 and 3 list the U.S. Food and Drug Administration (USFDA) levels of concern (LOC) for age groups and red crab wet tissue data for GOM red crabs, respectively. The mean arsenic level in wet muscle tissue of crabs for each area was below the LOC for crustacean shellfish (86 ppm for children and 140 ppm for adult; Table 3). All areas, however, had individual crabs whose arsenic concentration exceeded the guideline for young children. Highest concentrations of arsenic occurred in individual females in Area III and males in Area I. Those levels exceeded the LOC for the 2 to 5 age group. Arsenic concentrations in individual males exceeded levels of concern for children 2 to 5 years in all areas. Mean concentrations of lead in both male and female crabs exceeded levels of concern for children ages 2 to 5 in all areas. Mean LOC for pregnant women was exceeded in female crabs in Area II and male crabs in Area III. Mean levels of chromium were elevated and exceeded the LOC in Area III in both male and female tissues. Mean levels of chromium in male crabs in Area I approached the level of concern and individual levels exceeded the LOC. Individual concentrations in some male and some female crabs greatly exceeded the LOC for children and adults. Nickel, cadmium, and mercury did not exceed the LOC in mean concentrations or in individual crabs. Particle size analyses and X-ray diffraction of sediments showed anticipated trends in clay mineralogy. Sediments in Areas I and II were composed of silty-clay, with median particle diameters of 1.505 and 1.202 μm, respectively. The clay portion of the sediment in Areas I and II was dominated by montmorillonite; sediments in Area III were primarily kaolinitic clays. Smectite-group clays (montmorillonite) have a small particle size (often b0.5 μm) and are characterized by high cation exchange capacity. Because of these properties, these clays have enhanced abilities to accumulate heavy metals and other contaminants. The predominance of such clays in the north-central Gulf was expected as a consequence of riverine input from the Mississippi River (the Mississippi carries a heavy load of smectite). There was strong similarity in sediment particle size in Areas I and II. Both areas were rich in quartz (sand- and silt-sized material) and had similar clay mineral suites. The differences seen for the particle size distributions and the mineralogy
849
Fig. 4. Multidimensional Scaling plot indicating separation among sampling areas according to metal concentration in dry tissues from red crabs captured off Florida, eastern Gulf of Mexico.
seen on the X-ray diffractograms clearly reflect the provenance (source) areas for each region. Area III is composed of sediments deposited by off-shore (and longshore) currents that sweep northward along the Florida carbonate platform, while those from areas I and II are derived from weathering of source rocks in the Continental Interior and southern Appalachian Mountains and represent sediments that have been discharged into the Gulf by both the Mississippi River and the Mobile River systems. Seven of the 12 metals/trace elements listed in Table 1 were higher in sediment in Area I; lead, zinc, cobalt, arsenic, vanadium, chromium, and titanium. Two were more elevated in Area II (nickel and mercury) and there was no difference in levels of silver, cadmium and antimony among all areas. Patterns in metal concentrations in sediment were as expected based on sediment particle size distribution at the three sites. Area III was separated from Areas I and II, based on the similarity matrix for the sediment data; a separation driven by low zinc and vanadium concentrations in Area III relative to the other areas. Bioavailability of metals in sediment was not always related to bioaccumulation in muscle tissue. In Area II, sediment concentrations for lead and chromium were elevated, but tissue concentration factors were less than 1 ppm. Lead followed this pattern in Area I, nickel in Areas I and II and vanadium and titanium in all areas. The opposite pattern was also observed for some metals. Bioconcentration factors for arsenic were high although corresponding sediment concentrations were low. Sediment concentrations for silver and cadmium were below 0.6 ppm, but the metals were elevated in tissues. The availability of metals to bioaccumulate is dependent upon the concentration of the metal present in the sediment and how the metals are bound or partitioned in the sediment. Bioaccumulation is thus dependent upon the release potential associated with the metals that are partitioned in the aforementioned sites, under given conditions of Eh, pH, etc. (Isphording and Bundy, 1999) and the physiological and life history characteristics of the organism. For red crabs, age, stage in the molt cycle, and tissue type can affect levels of metals observed in the organism. Table 2 United States Food and Drug Administration guidance levels for metals in crustacean shellfish. Mean concentration levels of concern (ppm). Arsenic Cadmium Chromium Lead Nickel Mercury
Fig. 3. Multidimensional Scaling plot indicating separation among red crab gender according to metal concentration in dry tissues from red crabs captured off Florida, eastern Gulf of Mexico.
All Ages (2+ years) 2–5 years (20 kg) 18–44 years (males/females) Pregnant women Adults
140 86
6 –
22 –
– 1.2
– –
140 – –
6 – –
22 – –
8.3 2.8 –
– – 130
1
850
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
Table 3 Summary of metal concentrations (ppm) in Gulf of Mexico wet red crab tissue as determined by Inductively Coupled Plasma (ICP) Spectrophotometry. Mercury concentrations (ppm) as determined by Atomic Absorption (AA) Spectrophotometry. Pb Area I Female muscle Mean STDS Min Max Male muscle Mean STDS Min Max Area II Female muscle Mean STDS Min Max Male muscle Mean STDS Min Max Area III Female muscle Mean STDS Min Max Male muscle Mean STDS Min Max
Ni
As
Cd
Cr
Hg
2.00 0.23 1.54 2.31
1.00 0.80 0.20 2.11
48.99 12.70 37.49 72.93
0.20 0.02 0.15 0.23
1.11 1.41 0.19 4.16
0.10 0.02 0.08 0.15
2.30 0.76 1.75 4.36
4.76 6.01 0.17 18.51
73.43 24.43 43.94 124.97
0.21 0.02 0.17 0.25
15.91 18.94 2.29 50.96
0.07 0.02 0.04 0.10
3.21 1.73 1.75 6.31
1.96 1.44 0.19 3.63
53.87 10.88 38.74 68.84
0.26 0.11 0.17 0.43
1.27 1.00 0.42 3.79
0.05 0.04 0.01 0.13
2.24 0.77 1.75 4.35
1.48 0.87 0.19 2.86
67.95 13.37 48.19 90.58
0.30 0.10 0.17 0.43
1.02 0.95 0.31 3.11
0.06 0.04 0.03 0.16
1.41 0.59 0.91 2.28
25.76 17.99 3.67 59.67
70.79 20.82 52.57 118.85
– – BDL 0.23
57.09 32.87 16.43 121.46
0.09 0.05 0.05 0.19
3.33 1.55 0.96 5.73
30.53 17.87 8.89 62.25
72.87 18.72 42.16 103.38
0.11 0.03 0.09 0.19
58.95 35.37 15.73 120.83
0.14 0.09 0.07 0.35
BDL = Below Detection Limit
Chromium, lead, zinc, and arsenic were partitioned from sediment taken in Area II. With the exception of arsenic, over 50% of the metals were present in phases that could render them bioavailable; bioavailability of arsenic was slightly under 36%. Bioconcentration factors for
lead and chromium were less than one. Arsenic (BCF = 58.25♀, CF = 74.31♂) and zinc (BCF = 2.38♀, CF = 2.28♂) concentrations were elevated in both male and female crabs. Knowing how the metals were partitioned in the sediment was not a predictor of bioaccumulation, in that there were no consistent patterns between levels in sediment and tissue. While sediment concentrations for most metals were highest in Area I, red crab dry tissue concentrations did not follow a similar trend. We expected, but did not find, that crabs from Area III would show less evidence of bioaccumulation than crabs from Areas I and II. Eleven of the BCFs in Area I were above 1, twelve in Area II, and thirteen in Area III. Area III was distinct from the other two areas due primarily to extremely high tissue concentrations of chromium and nickel. Results for the ANOSIM were highly significant (p b 0.01), indicating that the three sample areas were well separated relative to the 12 metals analyzed in dry tissue. Gender also separated well, according to ANOSIM results. Most of the separation was due to the higher contamination found in males for some metals, especially arsenic, cobalt, and chromium. There are few studies on heavy metal/trace element levels in the red crab. Greig et al. (1976) provided data on heavy metals in red crab muscle tissue from a deepwater disposal site in the Middle Atlantic Bight. Mean concentrations of lead, nickel, arsenic, cadmium, chromium, mercury, zinc, and silver in wet tissue were determined (n = 7). Mean levels of cadmium and silver were similar to levels found in crabs from the GOM with concentrations of mercury and zinc lower in GOM samples. Higher levels of lead and extremely high levels of nickel, arsenic, and chromium were found in GOM crabs when compared to crabs from the Atlantic (Table 4). Bioaccumulation is a highly complex phenomenon that depends not only upon the species and their genetic adaptation to specific locations, but also involves climate, season, and the synergistic and antagonistic effects of other metals and organic compounds that may be present (Sager, 1989). A variety of defensive and resistance mechanisms have evolved to protect biota from toxic effects of heavy metals. These include complexation of metals to organic ligands, volatilization, alkylation, and a number of other adaptive physico-chemical mechanisms (Wood, 1974). Studies to date dealing with bioaccumulation of heavy metals in marine animals have dealt primarily with fish and mollusks. Fewer studies have been conducted with crustaceans. In 1993, the USFDA produced
Table 4 Comparison of metal concentrations (ppm) in sediment and muscle tissue (wet) in red crabs from the Gulf of Mexico (this study) and the Middle Atlantic Bight (Greig et al., 1976).
Gulf of Mexico Area I Sediment Female muscle Mean Male muscle Mean Area II Water Sediment Female muscle Mean Male muscle Mean Area III Sediment Female muscle Mean Male muscle Mean Middle Atlantic Bight Sediment Muscle Mean
Pb
Zn
Ag
Ni
As
30.00
107
0.50
41.00
10.00
Cd
Cr
Hg
0.40
66.00
BDL
2.0
39.92
0.20
1.00
48.99
0.20
1.11
0.10
2.30
44.00
0.29
4.76
73.43
0.21
15.91
0.07
0.10 23.00
0.01 90.00
0.01 0.50
0.01 43.00
0.05 5.00
0.01 0.40
0.01 58.00
BDL 0.03
3.21
39.56
0.24
1.96
53.87
0.26
1.27
0.05
2.24
37.85
0.22
1.48
67.95
0.30
1.02
0.06
8.00
47.00
0.50
35.00
5.00
0.40
23.00
BDL
1.41
39.96
0.16
25.76
70.79
–
57.09
0.09
3.33
40.16
0.17
30.53
72.87
0.11
58.95
0.14
7.5–15.0
19.5–47.8
ND
b7.4–33.1
ND
b1.25
6.0–16.7
ND
b1.00
69.00
b0.13
b0.48
1.60
b0.10
b0.51
0.23
H. Perry et al. / Marine Pollution Bulletin 101 (2015) 845–851
guidelines for heavy metal concentrations of arsenic, cadmium, chromium, nickel, and lead in species of shellfish. These guidelines, based on the work of Zook et al. (1976) and Hall et al. (1978), established provisional tolerable total intake levels for various population groups. In Area III, chromium levels in muscle tissue were above the USFDA's level of concern (22 ppm). In all areas, lead was above the USFDA's level of concern for children 2–5 and for pregnant women in areas II and III. Lead level of concern for pregnant women was detected for females in Area II and males in Area III. Nickel, cadmium, and mercury levels were below the USFDA's level of concern for these metals. Levels of concern for other metals have not been established. High variability in levels of contaminants in individual crabs was noted for zinc, nickel, arsenic and chromium. If a fishery for red crabs were to develop in the GOM, it would be advisable to re-sample the population to more accurately characterize metal burdens and to periodically monitor the catch for those heavy metals known to bioaccumulate in muscle tissue.
Acknowledgments We would like to thank the United States Environmental Protection Agency/Gulf of Mexico Program for funding the original project (Project Identification Number MX 994731-95-0, 1995–1998) that led to the development of the current manuscript. Renee Bishop, Dick Waller, and Frank Frumar aided in field collections and we are grateful for their assistance. While the data in this study have been available in a completion report and circulated in the “gray” literature for many years, publishing the information makes it available to the larger scientific community. Additionally, acceptance of the data in a peer reviewed format places greater emphasis on the need for consideration of regulatory measures for the fishery in light of levels of chromium and lead above USFDA consumption guidelines in some tissues. These data also provide baseline information on heavy metals/trace elements in organisms whose habitat was directly impacted by oil and dispersant from the Deepwater Horizon Oil Spill.
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