METALS IN TISSUES OF DIAMONDBACK TERRAPIN FROM
NEW JERSEY
JOANNA BURGER
Division of Life Sciences, Institute of Marine and Coastal Sciences, Environmental and
Occupational Health Sciences Institute, Nelson Hall, Piscataway, New Jersey, U.S.A.
(e-mail: burger@biology.rutgers.edu)
(Received 30 January 2001; accepted 11 September 2001)
Abstract. Relatively little is known about contaminants in reptiles, particularly turtles. The dis-
tribution of metals in eggs, liver and muscle of diamondback terrapin (Malaclemys terrapin) was
examined from Barnegat Bay, New Jersey as part of an aquatic study to understand movement of
contaminants in the bay. Lead and cadmium were relatively low in all tissues. There were significant
differences among tissues for all metals, except lead. Where there were significant differences, levels
were highest in the liver, except for chromium. Levels of mercury were 6.6 times higher in the
liver than muscle, and manganese levels were 4 times as high. The levels of metals in muscle of
diamondback terrapin are below those that might cause effects in consumers, including humans who
eat them in stews. However, the level of mercury in liver is sufficiently high to be problematic for
consumers and scavengers that eat liver.
Keywords: Barnegat Bay, biomonitoring, consumers, metals, turtles
1. Introduction
Environmental and coastal managers are interested in assessing the health of mar-
ine and coastal environments, especially as more people concentrate along coasts,
and participate in a variety of activities in coastal waters. Overall, the majority
of people in the world live within 100 km of bays and estuaries (Norse, 1993;
NRC, 1995). Marine organisms are exposed to a variety of pollutants that enter
estuaries from surface runoff, airborne deposition, and natural geochemical cycles.
While anthropogenic contaminants from urban, industrial and agricultural runoff
are a major issue, levels are augmented by natural geological processes, and global
transport (Mailman, 1980; Fitzgerald, 1989).
Because of bioaccumulation and bioconcentration, organisms at intermediate
and higher trophic levels are exposed to higher concentrations of chemicals (Van
Straalen and Ernst, 1991; Burger et al., 1992; Burger, 1993). In marine systems,
most contaminants work concentrates on fish because of their importance in the
food chain, including human consumers. Relatively little attention is devoted to
other marine vertebrates, such as turtles.
In this article the levels of arsenic, cadmium, chromium, lead, manganese,
mercury and selenium in the eggs, liver, and muscle of diamondback terrapin
Environmental Monitoring and Assessment 77: 255–263, 2002.
© 2002 Kluwer Academic Publishers. Printed in the Netherlands.
256
J. BURGER
(Malaclemys terrapin) are reported from Barnegat Bay, at Tuckerton, New Jersey
to better understand movement of contaminants in the bay, and to provide baseline
data for trend analysis of metal levels. Of particular interest was whether terrapins
are accumulating mercury, as are some of the birds that forage on fish from these
same waters (Burger and Gochfeld, 1997). For example, the eggs of Forster’s tern
(Sterna fosterii) nesting nearby have some of the highest levels of mercury (mean
2.1 ppm, wet weight) of any birds in the bay, well above levels known to cause
adverse effects (Eisler, 1987). Further, with energy deregulation, mercury levels
in the bay may increase due to atmospheric deposition from coal-burning power
plants in the mid-west. Diamondback terrapins are still caught and eaten in New
Jersey and elsewhere along the Atlantic coast. Thus it is important to determine the
status of mercury levels in terrapins.
Diamondback terrapins live in estuarine waters from New England to Texas,
and would thus be useful for biomonitoring contaminants over a wide geographical
range. They are the only turtle to specialize in estuarine environments, with a diet
consisting of invertebrates (snails, crabs and worms), as well as some vegetation
(Palmer and Fowler, 1975, unpubl. data). In the waters from New Jersey to Florida
the terrapins are numerous, and nest in the hundreds on some nesting beaches.
2. Study Area and Methods
Under appropriate state collecting permits, 11 adult female diamondback terrapins
were collected along coastal New Jersey from the south end of Barnegat Bay at
Tuckerton (Figure 1). Terrapins had a mean carapace of length of 14.3±0.7 cm,
well within the range of adult breeding females for the region (Montevecchi and
Burger, 1975). New Jersey is a microcosm for examining coastal issues because it
is the most densely populated and one of the most highly industrialized states, and
yet it has important natural resources, including important fisheries (Burger, 1996;
MacKenzie, 1992).
Specimens were frozen immediately and transported to the Environmental and
Occupational Health Sciences Institute. Terrapin were dissected using standard
dissection tools except for heavy shears for the carapace. Tissues removed for
analysis included liver, leg muscle, and eggs (where they were present, N = 8).
Soft tissues (2 g wet weight) were digested in ultrex ultrapure nitric acid (2 mL) in
a microwave (MD 2000 CEM), using a digestion protocol of three stages of ten min
each under 50, 100 and 150 pounds per square inch (3.5, 7.0 and 10.6 kg cm−2) at
70X power. Digested samples were subsequently diluted with deionized water to a
final volume of 20 mL and a final acid matrix of 10%. Mercury was analyzed by
cold vapor atomic absorption spectroscopy, and all other metals were analyzed by
graphite furnace atomic absorption spectroscopy. All concentrations in tissues are
expressed in parts per billion (ng g−1 on wet weight).
METALS IN TISSUES OF DIAMONDBACK TERRAPIN
257
Figure 1. Map of NJ showing collection sites.
Detection limits were 0.02 ppb for cadmium, 0.08 ppb for chromium, 0.15 ppb
for lead, 0.09 ppb for manganese, 0.2 ppb for arsenic and mercury, and 0.7 ppb
for selenium. All specimens were run in batches of 35 that included blanks, spiked
samples, an initial calibration verification (NIST, bovine liver), and after each ten
samples there is a continuous calibration verification. The recoveries for spikes
ranged from 93% (mercury) to 101% (arsenic). The coefficient of variation (CV)
on replicate, samples ranged from 4–7%. Further quality control included periodic
blind analysis of samples for each metal (varied by less than ±8%). Duplicate
samples of each tissue were run and the means used for analysis.
Non-parametric Kruskal-Wallis One Way Analysis of Variance was used to
compare concentrations among tissues, followed by Duncan multiple range test
to examine differences among tissues (SAS, 1995). Tissues with a different letter
on Table I are significantly different from one another. Kendall tau correlations
were used to examine relationships among metals.
258
J. BURGER
TABLE I
Concentration of elements in diamond back terrapins (Tuckerton, NJ). Results are
expressed as mean and SE (wet weight) for each tissue. Geometric means are in-
dicated below arithmetic means. Means with the same letters are not significantly
different
Metal
Egg
Liver
Muscle
X2(P)a
Arsenic
12±6
562±168
728±190
6.44 (0.04)
15 (B)
370 (A)
551 (A)
Cadmium
0.26±0.24
66±19
18±7
11.29 (0.003)
0.07 (B)
52 (A)
12 (C)
Chromium
390±255
69±6
297±40
14.74 (0.0006)
254 (A)
67 (B)
267 (A)
Lead
40±30
90±21
62±13
1.70 (NS)
21 (A)
72 (A)
39 (A)
Manganese
248±141
2750±801
665±143
10.49 (0.005)
117 (B)
1982 (A)
524 (B)
Mercury
35±10
1139±473
172±38
8.23 (0.02)
32 (B)
271 (A)
123 (A,B)
Selenium
498±25
1621±260
507±116
12.12 (0.002)
497 (B)
1503 (A)
394 (B)
a X2(P): Analysis of variance test.
3. Results
There were significant differences among tissues for all metals except lead (Table I).
Both arithmetic and geometric means are given in Table I to facilitate comparisons
with other studies in the literature. For all tissues, cadmium and lead levels were
relatively low. Muscle to liver ratios were as follows: arsenic = 1:0.77, cadmium
= 1:3.8, chromium = 1:0.23, lead = 1:1.5, manganese = 1:4.1, mercury = 1:6.6,
selenium = 1:3.2. Thus the relative storage in the muscle varies, with a relatively
higher proportion of arsenic and chromium in the muscle than in the liver.
There were relatively few correlations among metals within muscle, although
there were significant correlations between cadmium and chromium (r = 0.62, P <
0.008), cadmium and lead (r = 0.56, P < 0.02), chromium and lead (r = 0.73, P <
0.002), chromium and manganese (r = 0.54, P < 0.02), and manganese and lead (r
= 0.59, P < 0.01). There were fewer significant correlations among metals in the
liver: cadmium and mercury (r = 0.64, P < 0.03), manganese and chromium (r =
0.57, P < 0.05), and manganese and lead (r = 0.57, P < 0.05).
METALS IN TISSUES OF DIAMONDBACK TERRAPIN
259
4. Discussion
4.1. TISSUE COMPARISONS
Very few studies with reptiles compare levels of metals in different tissues, but of-
ten they frequently examine whole body levels (see Campbell and Campbell, 2000,
2001). In the present study, levels were higher in the liver than muscle for most
metals, except chromium and arsenic, which were slightly higher in the muscle.
Thus, as with other vertebrates, the liver is the organ where metals concentrate,
with the exception of lead, which concentrates in bone (Ma, 1996).
One objective was to determine which metals are transferred from the female
to the egg, and to some extent, all metals were transferred (refer to Table I). Trans-
fer of metals to reptile eggs has been shown for a number of species, including
pine snakes (Pituophis melanoleucus, Burger, 1992) and slider turtles (Trachemys
scripta, Burger and Gibbons, 1998).
4.2. COMPARISONS WITH OTHER REPTILES
There is relatively little information on metal levels in liver and muscle of rep-
tiles, other than alligators, lizards, and snakes (Burger et al., 2000; Campbell and
Campbell, 2000, 2001). Lizards are useful because of their potential as bioindic-
ators because they are frequently common and widely-dispersed (Campbell and
Campbell, 2000). Despite the fact that in many regions people eat turtles, there is
little information on contaminant levels in muscle.
More data are available on metal contamination in eggs of reptiles. Mercury
levels for snapping turtle egg contents from the St. Lawrence River in Canada
ranged from 50 to 180 ppb for 6 pooled samples (Bonin et al., 1995). Mercury in
16 eggs of slider turtles from the Savannah River Site, near Aiken, South Carolina
averaged 40±15 (Burger and Gibbons, 1998). Metal levels in sea turtle (Caretta
caretta) eggs varied by nesting beaches, with average mercury levels ranging from
635 ppm to 1391 ppb (Stoneburner et al., 1980, Table II). Thus the mercury levels
in eggs of diamondback terrapin were relatively low.
Other than sampling on slider and sea turtles, there is relatively little information
on other metals in turtle eggs, and almost none on arsenic. In general, the levels of
metals in the eggs of diamondback terrapin were similar to or lower than those
reported for other turtles (Table II).
4.3. ECOSYSTEM CONSIDERATIONS AND HUMAN RISK
Increases in metal levels in higher trophic levels have been noted among many
different taxa (e.g. Hothem and Ohlendorf, 1980; Furness, 1996). Mercury and cad-
mium are key contaminants of concern in marine ecosystems because of their high
concentrations in seawater. Monteiro et al. (1998) demonstrated a clear relation-
ship between levels of mercury in prey organisms and mercury levels in seabirds,
260
J. BURGER
TABLE II
Comparison of metals in the eggs of turtles. Given are ranges (means) in ppb
Diamondback Terrapin
Sea Turtle
Slider Turtles
Source
This study
Stoneburner et al., 1980
Burger and Gibbons, 1980
Cadmium
0.01–0.74 (0.26)
26–195
3.0–444 (67)
Chromium
120.00–899 (390)
1043–1149
56.0–353 (139)
Lead
6.00–99.0 (40)
1134–2185
173.0–1852 (687)
Manganese
14.00–502
–
a
1903.0–8224 (4477)
Mercury
21.00–53 (35)
635–1391
0.4–240 (40)
Slenium
469.00–547 (498)
–
a
131.0–1041 (417)
a
= Not analyzed, ND = non detected.
and presumably this applies to other vertebrates and their prey. Kim et al. (1996)
recently suggested that some pelagic seabirds (albatrosses and petrels) are capable
of demethylating methylmercury in the liver, and storing it as an immobilizable
inorganic form, a chemical pathway which should be examined for estuarine and
marine turtles that have accumulated relatively high mercury levels. In diamond-
back terrapins mercury levels were relatively high in the liver (1139 ppb), but were
relatively low in the muscle (172 ppb), well below the limit allowed for interstate
commerce in fish muscle tissue (normally 0.5 or 1.0 ppm, FDA, 1987; Lange et al.,
1994). Further, risk from consumption is a function of both contaminant levels and
consumption rates, and diamondback terrapins are not a significant part of the diet
of people.
It is important to know whether the existing levels of metals are high enough
to cause a problem for terrapin populations or for predators and scavengers that
consume terrapins. Although humans are not apt to consume the liver of diamond-
back terrapins, other animals are, particularly scavengers. Arsenic residues of over
10 ppm (wet weight) in the liver or kidney of birds are indicative of poisoning
(Goede, 1985), and levels of 5 to 10 ppm in liver or kidney of domestic livestock
are indicative of poisoning (Vreman et al., 1986). Thus arsenic concentrations in
the livers of terrapin appear to be at non-toxic levels. Cadmium levels were also
sufficiently low in the terrapin to suggest no problems for consumers. Cadmium
damage is first noted in the kidney of mammals (Cooke and Johnson, 1996), sug-
gesting it might also be the organ of concern in terrapins. Sublethal toxic symptoms
have been noted at kidney levels of 30 ppm in mammals (wet weight, Chmielnicka
et al., 1989).
Hexavalent chromium is a mutagen, teratogen, embryotoxin, and carcinogen,
and tissue levels in excess of 12 ppm (wet weight) indicate chromium contamina-
tion in a wide range of vertebrates (Eisler, 1986; Domingo, 1994). The chromium
levels in terrapin were well below this.
METALS IN TISSUES OF DIAMONDBACK TERRAPIN
261
The lead levels in the terrapin were sufficiently low not to pose a problem.
Lead levels of 23 ppm in the liver, 32 ppm in the kidney, and 1.2 ppm in the brain
(wet weight) have been associated with acute lead poisoning in dogs (Forbes and
Sanderson, 1978), and 25 ppm is the critical kidney level for small mammals (Ma,
1989), but there are no comparable data for turtles.
While the levels of cadmium, chromium, lead and arsenic were relatively low in
all tissues, levels of manganese, mercury and selenium were higher, particularly in
the liver (which would be eaten by many consumers and scavengers). The dietary
threshold for selenium, where wildlife that consume them would be affected, is
1.6 ppm (wet weight) for fish skeletal muscle, and 3 ppm (wet weight) for fish liver
(Lemly, 1993), suggesting that the levels of selenium in muscle and liver of terrapin
are below a toxic level. There is information on the doses of manganese that are
toxic in mammals (Domingo, 1994), but there are no studies of the tissue levels
associated with toxicity in reptiles, although some effects similar to lead have been
found in birds (Burger and Gochfeld, 2000).
Mercury, however, could pose the biggest risk to consumers of terrapin. Tissue
concentrations of over 30 ppm (wet weight, liver and kidney) are lethal in some
animals, and levels of 1 ppm are associated with adverse effects in some mammals
(Eisler, 1987; Beyer et al., 1996). It is not unreasonable to assume that if consumers
or scavengers eat terrapin livers containing levels found in this study (1.1 ppm),
they might receive a sublethal toxic dose.
5. Conclusions
Levels of most metals were higher in the liver than in muscle, except for chromium
and arsenic, where the levels were similar. Selenium, chromium, and manganese
were sequestered in the eggs of diamondback terrapin at higher levels than were
other heavy metals. Overall, the levels of metals were not sufficient to cause prob-
lems for the terrapin or for consumers eating their muscle, although the levels of
mercury in liver may be sufficiently high to cause some sublethal effects.
Acknowledgements
I thank C. Dixon, J. Leonard, and T. Shukla for heavy metal and statistical analysis,
the Tuckerton Marine Laboratory for collecting the specimens, and the New Jersey
Department of Environmental Protection for permits to collect the terrapins. This
project was partially funded by NIEHS (ESO 5022) and DOE (DE-FG-26-OONT-
40938).
262
J. BURGER
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