Do Heavy Metal Concentrations Pose a Threat to Marine Turtles from the Mediterranean Sea?

Abstract

Concentrations of heavy metals (Hg, Cd and Pb) were determined in internal organs and nest contents of green turtles Chelonia mydas and loggerhead turtles Caretta caretta from northern Cyprus, eastern Mediterranean Sea. Concentrations of mercury in liver tissue were higher in loggerhead turtles (median 2.41 μg g−1 dry weight) than in green turtles (0.55 μg g−1 dry weight). Preliminary data suggest cadmium concentrations to be highest in kidney tissue of loggerhead turtles (median 30.50 μg g−1 dry weight) but in liver tissue of green turtles (median 5.89 μg g−1 dry weight). Concentrations of lead in internal tissues were often below analytical detection limits in both species, but when measurable, tended to be higher in loggerhead turtles. Concentrations of mercury and cadmium in nest contents from both species were low, often below analytical detection limits, while those of lead were relatively high in loggerhead turtle hatchlings (up to 10.56 μg g−1 dry weight). When measurable, concentrations of all three metals tended to be higher in loggerhead turtle nest contents than in green turtle nest contents. Results presented here are consistent with inter-specific differences in diet and trophic status. Heavy metal burdens in loggerhead turtles and green turtles from the Mediterranean are similar or lower than corresponding concentrations in turtles from Japan and Hawaii, but some lead concentrations in Mediterranean loggerhead hatchlings are at levels known to cause subclinical toxic effects in other vertebrates.

Full text

Do Heavy Metal Concentrations Pose a
Threat to Marine Turtles from the
Mediterranean Sea?
BRENDAN J. GODLEY*, DAVID R. THOMPSONৠand ROBERT W. FURNESSà
Marine Turtle Research Group, School of Biological Sciences, University of Wales, Swansea, SA2 8PP, UK
àDivision of Environmental and Evolutionary Biology, Graham Kerr Building, University of Glasgow, Glasgow, G12 8QQ,
UK
§National Institute of Water and Atmospheric Research, 301 Evans Bay Parade, Greta Point, P.O. Box 14-901, Kilbirnie,
Wellington, New Zealand
Concentrations of heavy metals (Hg, Cd and Pb) were
determined in internal organs and nest contents of green
turtles Chelonia mydas and loggerhead turtles Caretta
caretta from northern Cyprus, eastern Mediterranean
Sea. Concentrations of mercury in liver tissue were higher
in loggerhead turtles (median 2.41 lgg
ÿ1dry weight) than
in green turtles (0.55 lgg
ÿ1dry weight). Preliminary data
suggest cadmium concentrations to be highest in kidney
tissue of loggerhead turtles (median 30.50 lgg
ÿ1dry
weight) but in liver tissue of green turtles (median 5.89 lg
gÿ1dry weight). Concentrations of lead in internal tissues
were often below analytical detection limits in both spe-
cies, but when measurable, tended to be higher in log-
gerhead turtles. Concentrations of mercury and cadmium
in nest contents from both species were low, often below
analytical detection limits, while those of lead were rela-
tively high in loggerhead turtle hatchlings (up to 10.56 lg
gÿ1dry weight). When measurable, concentrations of all
three metals tended to be higher in loggerhead turtle nest
contents than in green turtle nest contents. Results pre-
sented here are consistent with inter-speci®c dierences in
diet and trophic status. Heavy metal burdens in logger-
head turtles and green turtles from the Mediterranean are
similar or lower than corresponding concentrations in
turtles from Japan and Hawaii, but some lead concen-
trations in Mediterranean loggerhead hatchlings are at
levels known to cause subclinical toxic eects in other
vertebrates. Ó1999 Elsevier Science Ltd. All rights re-
served
Keywords: marine turtles; Mediterranean; heavy metals;
Caretta caretta;Chelonia mydas; mercury; cadmium; lead.
Only three species of marine turtle occur regularly in the
Mediterranean Sea. These are loggerhead turtle Caretta
caretta, green turtle Chelonia mydas and leatherback
turtle Dermochelys coriacea (Groombridge, 1990). Of
these, loggerhead and green turtles breed within the re-
gion, whilst leatherback turtles are thought to be non-
breeding visitors. On a world-wide scale, marine turtle
populations are generally in decline (Eckert, 1995;
Limpus, 1995).Within the Mediterranean region, esti-
mated annual breeding populations are as few as 2000
female loggerhead turtles and 300±400 female green
turtles.
One of the potential threats to the survival of marine
turtles is pollution (Hutchinson and Simmonds, 1992;
Lutcavage et al., 1997). Of the major categories of po-
tential pollutants, the impacts upon marine turtles of
solid debris (Gramentz, 1988; Hobson et al., in press),
oil and tar (Gramentz, 1988) and organochlorine resi-
dues (McKenzie et al., in press) have been investigated
within the Mediterranean region. Kaska (1998) investi-
gated heavy metal contaminants in eggshells, yolk and
embryonic livers of loggerhead turtles from Turkey.
Because of the semi-closed nature of the Mediterra-
nean Sea and the relatively large centres of human
population that impinge upon its shores, levels of ma-
rine contaminants in this ecosystem are considered to be
relatively high (Bacci, 1989; Meadows, 1992; Kuetting,
1994; Borrell et al., 1997). Given the endangered status
of marine turtles and the potential for heavy metals to
have detrimental eects upon marine vertebrates (Bull
et al., 1983; Nicholson and Osborn, 1983; Rawson et al.,
1993; Work and Smith, 1996), there is a clear need to
augment the relatively small amount of data regarding
heavy metal burdens in marine turtles from the Medi-
terranean Sea.
In this paper, we present heavy metal concentrations
(mercury, cadmium and lead) in the organs and nest
contents of loggerhead and green turtles from northern
Cyprus, eastern Mediterranean. We assess to what ex-
tent marine turtles in this area exhibit potentially
harmful concentrations of heavy metals and we evaluate
the usefulness with which turtle nest contents may be
PII: S0025-326X(98)00184-2
Marine Pollution Bulletin Vol. 38, No. 6, pp. 497±502, 1999
Ó1999 Elsevier Science Ltd. All rights reserved
Printed in Great Britain
0025-326X/99 $ ± see front matter
*Corresponding author.
497

used to monitor heavy metal contamination in this
group.
Materials and Methods
Sample collection and preparation
Beaches were patrolled regularly as part of other
turtle studies in northern Cyprus. Within an investiga-
tion of stranded turtles washed ashore between 1994 and
1996, carcasses were collected for dissection. Curved
carapace length (CCL) was measured (using a ¯exible
tape-measure, to the nearest 0.5 cm), and liver, kidney
and muscle tissues were dissected from loggerhead tur-
tles (n7, mean CCL 63.5 cm, s.d. 14.2,
range 56.0±79.0 cm) and green turtles (n6, mean
CCL 49.5 cm, s.d. 16.6, range 27.5±56.0 cm)
within 24 h of stranding. Samples of the contents re-
maining in previously hatched nests of both species
(loggerhead turtles: n48; green turtles: n69) were
opportunistically sampled at Alagadi beach, northern
Cyprus, following an established protocol (Broderick
and Godley, 1996). Only one sample per nest (of a dead
hatchling, dead embryo or undeveloped egg) was in-
cluded in the study. All samples were stored frozen (at
ca.ÿ20°C) until further treatment. Prior to metal ana-
lyses, tissues were thawed at ambient room temperature
(ca. 20°C), then dried to constant mass in an oven at
50°C. Approximate water content, expressed as a per-
centage of fresh weight, was calculated. However, since
samples had been frozen, fresh weights are not pre-
sented.
Metal analyses
Total (organic and inorganic combined) mercury,
cadmium and lead concentrations were measured. Total
mercury concentrations were determined using a cold
vapour atomic absorption spectrophotometry technique
following an established methodology (Furness et al.,
1986; Thompson and Furness, 1989). Cadmium and
lead concentrations were measured using ¯ame atomic
absorption spectrophotometry according to the meth-
odology described in Stewart et al. (1994). All metal
concentrations are presented as lg gÿ1(ppm) of tissue
on a dry weight basis. Analytical limits of detection were
determined as 0.01 lg gÿ1dry weight.
Results
Concentrations of mercury, cadmium and lead in in-
ternal tissues of loggerhead and green turtles are pre-
sented in Table 1. Loggerhead turtles exhibited higher
metal concentrations than green turtles (Table 1).
Maximum concentrations in liver tissue of loggerheads
were 7.50, 12.97 and 4.90 lg gÿ1for mercury, cadmium
and lead, respectively, compared to 1.37, 10.73 and 1.84
lg gÿ1in that of green turtles (Table 1). Mercury con-
centrations were the highest in liver tissue >kid-
ney >muscle for both species, cadmium concentrations
in kidney tissue were as high or higher than those in liver
tissue, but lowest in muscle tissue, whilst lead concen-
trations were fairly similar in all three tissues (Table 1).
Mean water contents of liver, kidney and muscle tissues
were 78%, 72% and 79%, respectively.
Metal concentrations in nest contents of loggerhead
and green turtles are presented in Table 2. Mercury
concentrations were generally low, with maximum val-
ues of 0.24 lg gÿ1in green turtle hatchlings and 0.75 lg
gÿ1in loggerhead turtle hatchlings (Table 2). Maximum
cadmium concentrations were recorded in yolk and al-
bumen of green turtles (1.22 lg gÿ1; Table 2), and in
hatchling loggerhead turtles (1.45 lg gÿ1; Table 2). Lead
concentrations were higher, with maximum concentra-
tions in hatchlings of 10.56 and 3.86 lg gÿ1in logger-
head and green turtles, respectively. Metal
concentrations varied little among the three nest content
categories (Table 2). Water content in eggs, embryos
and hatchlings ranged from 70% to 75%.
Discussion
Data presented here, although based on relatively
small numbers of turtles, provide convincing evidence
that concentrations of heavy metals are likely to re¯ect
marked inter-speci®c dierences in diet. Green turtles
are thought to be generally herbivorous, whilst logger-
head turtles are carnivorous (Bjorndal, 1997). Although
TABLE 1
Mercury, cadmium and lead concentrations (lg gÿ1dry weight) in internal organs from loggerhead and green turtles found stranded in northern
Cyprus. Values are medians, sample size in parentheses and ranges. For analytical limits of detection, see Materials and Methods.
Species Tissue Mercury Cadmium Lead
Median (n) Range Median (n) Range Median (n) Range
Loggerhead turtle Liver 2.41 (5) 0.82±7.50 8.64 (4) 5.14±12.97 BDL (4) BDL±4.90
Kidney 0.47 (2) 0.13±0.80 30.50 (2) 18.80±42.20 2.45 (2) BDL±4.90
Muscle 0.48 (7) BDL±1.78 0.57 (4) 0.30±1.43 2.46 (4) BDL±5.53
Green turtle Liver 0.55 (6) 0.27±1.37 5.89 (6) 2.53±10.73 BDL (6) BDL±1.84
Kidney BDL (1) NA 3.46 (1) NA 1.81 (1) NA
Muscle 0.09 (5) BDL±0.37 0.37 (6) 0.12±0.78 BDL (6) BDL±2.45
BDL: Below detection limit; NA: Not applicable.
498
Marine Pollution Bulletin

TABLE 2
Mercury, cadmium and lead concentrations (lg gÿ1dry weight) in nest contents of loggerhead and green turtles from Alagadi beach, northern Cyprus. Values are medians, sample sizes in parentheses and
ranges. For analytical limits of detection, see Materials and Methods.
Species Sample type Mercury Cadmium Lead
Median (n) Range Median (n) Range Median (n) Range
Loggerhead turtle Hatchling 0.02 (16) BDL±0.75 0.34 (16) BDL±1.45 0.13 (16) BDL±10.56
Embryo 0.01 (27) BDL±0.22 0.21 (29) BDL±1.09 BDL BDL±6.48
Yolk and albumen 0.19 (3) 0.16±0.57 0.23 (3) 0.23±0.56 0.19 (3) BDL±3.93
Green turtle Hatchling BDL (24) BDL±0.24 0.23 (29) BDL±0.94 BDL (29) BDL±3.86
Embryo BDL (18) BDL±0.12 0.33 (16) BDL±0.93 0.66 (16) BDL±3.41
Yolk and albumen BDL (17) BDL±0.19 0.27 (24) 0.05±1.22 BDL (24) BDL±1.61
BDL: Below detection limit.
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Volume 38/Number 6/June 1999

there is a paucity of data regarding diet of these species
in the region, these broad dietary dierences, leading to
corresponding dierences in trophic status, were re-
cently con®rmed using stable isotope techniques (God-
ley et al., 1998a). The higher concentrations of metals in
loggerhead turtles compared to green turtles reported
here (Table 1) are entirely in keeping with these pro-
nounced trophic dierences. A similar pattern was also
found in a recent study of organochlorine contaminants
in tissues from turtles from the same populations
(McKenzie et al., in press). Within both species, patterns
of metal accumulation followed those described for
other marine vertebrates (see Thompson, 1990 for a
review), in that mercury concentrations tended to be
highest in liver tissue, cadmium concentrations tended
to be highest in kidney tissue and lead concentrations
tended to be higher in liver and kidney, than in muscle
(Table 1).
For comparative purposes, a summary of heavy metal
concentrations in internal tissues of marine turtles de-
termined by other studies is presented in Table 3. Data
from Aguirre et al. (1994) and from Sakai et al. (1995),
which were originally presented on a wet weight basis,
have been converted to approximate dry weight basis
using mean water content values determined in this
study of liver 78%, kidney 72% and muscle 78% (see
Results). Mercury concentrations in loggerhead turtles
from Japan (Sakai et al., 1995) were similar to those
reported here (Tables 1 and 3). In liver tissue, for ex-
ample, the median mercury concentration in loggerhead
turtles reported by Sakai et al. (1995) was ca. 1.73 lg gÿ1
(converted dry weight; Table 3), compared to 2.41 lg
gÿ1in this study (Table 1). In contrast, cadmium con-
centrations in both green turtles from Hawaii (median
kidney concentration ca. 56.79 lg gÿ1converted dry
weight; Table 3; Aguirre et al., 1994) and from logger-
head turtles from Japan (median kidney concentration
ca. 162.50 lg gÿ1converted dry weight; Table 3; Sakai
et al., 1995) were considerably higher than those reported
here (median kidney concentrations: green turtle 3.46 lg
gÿ1, loggerhead turtle 30.5 lg gÿ1; Table 1).
Dierences in heavy metal concentrations between
populations, may be explained by dierences in diet,
prevailing environmental contamination in their forag-
ing ranges, by age of individuals sampled, or by a
combination of these. Studies in Japan (Sakai et al.,
1995) and in Hawaii (Aguirre et al., 1994) incorporated
larger individual turtles than those sampled from the
Mediterranean here, and were likely, therefore, to have
been older. Since cadmium, for example, is known to
accumulate in marine vertebrates with age (Stewart
et al., 1994; Dietz et al., 1996), this may explain why
cadmium concentrations in both conspeci®c sample sets
(Table 3) were higher than those from the Mediterra-
nean (Table 1). Mercury levels were not determined in
green turtles from Hawaii (Aguirre et al., 1994), and
mercury concentrations in turtles from the Mediterra-
nean (Table 1) were comparable with those from Japan
(Sakai et al., 1995; Table 3). The fact that mercury
concentrations did not show the same spatial dierences
as for cadmium (see above) may be explained by the fact
that, in general, organisms from the Mediterranean
would be expected to have relatively high mercury levels
due to the presence of a natural mercury bed in the re-
gion (Bacci, 1989).
Concentrations of metals reported in leatherback
turtles from the north-east Atlantic (Davenport and
Wrench, 1990; Godley et al., 1998b; Table 3) were
generally similar to those recorded in green turtles in this
study (Table 1), but lower than those reported for log-
gerhead turtles from Japan (Sakai et al., 1995; Table 3)
and in this study (Table 1). Godley et al. (1998b) hy-
TABLE 3
Heavy metal concentrations (lg gÿ1dry weight) in internal tissues of marine turtles from other locations. Values are medians, samples sizes in
parentheses and ranges.
Species Location Tissue Mercury Cadmium Lead Reference
Median (n) Range Median (n) Range Median (n) Range
Loggerhead
turtle
Japan Liver 1.73 (7) 1.13±37.05 47.73 (7) 25.73±66.36 ND NA Sakai et al.
(1995)
Japan Kidney 1.00 (7) 0.43±1.57 162.50 (7) 64.64±201.79 ND NA Sakai et al.
(1995)
Japan Muscle 0.43 (7) 0.24±0.90 0.29 (7) 0.19±0.56 ND NA Sakai et al.
(1995)
Green turtle Hawaii Liver ND NA 23.82 (13) 1.77±118.18 ND NA Aguirre et al.
(1994)
Hawaii Kidney ND NA 56.79 (12) 16.86±250.71 ND NA Aguirre et al.
(1994)
Leatherback
turtle
UK Liver 0.61 (4) 0.29±1.20 8.50 (4) 0.22±88.00 0.08 (4) 0.02±14.00 Godley et al.
(1988b)
UK Muscle 0.12 (4) 0.04±0.29 2.10 (4) 0.06±7.50 0.08 (4) BDL±0.31 Godley et al.
(1988b)
BDL: Below detection limit; ND: Not determined; NA: Not applicable.
*
Also incorporated data from Davenport and Wrench (1990).
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Marine Pollution Bulletin

pothesised that the highly pelagic nature of this species
was likely to contribute to low contaminant burdens,
both due to avoidance of the contaminated neritic, and
through feeding at a level in the food web which is likely
to involve few trophic (and therefore bioaccumulative)
steps.
Heavy metal concentrations in nest contents of both
species in the present study were generally low, often
below quanti®able limits, but lower in green turtles than
in loggerhead turtles (Table 2). A preliminary analysis of
levels of organochlorines in eggs and hatchlings from
the same site showed similar patterns (McKenzie et al.,
in press). Whilst most egg content samples exhibited low
metal concentrations (Table 2), a small number of in-
dividual samples exhibited relatively high lead concen-
trations. Hatchling green turtles exhibited a maximum
lead concentration of 3.86 lg gÿ1and the corresponding
value for loggerhead turtle hatchlings was 10.56 lg gÿ1
(Table 2). No toxicological data have been published for
marine turtles describing threshold concentrations of
heavy metals above which detrimental eects would be
likely. Although not directly comparable, a recent re-
view of the toxicity of lead in birds (Franson, 1996)
suggested that liver concentrations of lead of as low as
ca. 2 lg gÿ1wet weight (approximately 10 lg gÿ1dry
weight) could cause subclinical toxic eects in some
species. Similarly, Ma (1996) concluded that in mam-
mals lead concentrations in excess of 10 lg gÿ1dry
weight in liver are consistent with acute poisoning. Lead
concentrations in loggerhead turtle hatchlings, in par-
ticular, and perhaps in green turtle hatchlings also
(Table 2), approach toxic levels reported in other ver-
tebrate groups, and would warrant further study.
Previous work by Stoneburner et al. (1980) deter-
mined a range of metals (including mercury, cadmium
and lead) in egg yolk from loggerhead turtles sampled at
four sites in the USA, and noted some relatively high
metal concentrations. The concentrations of metals
presented by Stoneburner et al. (1980) were up to two
orders of magnitude higher than those in nest contents
reported more recently (Aguirre et al., 1994; Sakai et al.,
1995; Kaska, 1998; this study). Such a wide discrepancy
between data sets may indeed be due to relatively high
levels of contamination in the USA neritic, or alterna-
tively, may re¯ect inaccuracies in earlier analytical
methods.
In conclusion, the preliminary data presented here
suggest that metal levels in both green and loggerhead
turtles are not likely to be high enough to aect the
health of these endangered species. The only exception
to this might be relatively high lead concentrations in
loggerhead turtle hatchlings, and perhaps also green
turtle hatchlings (Table 2). We suggest that for non-in-
vasive monitoring of the potential impact of metal pol-
lution on these species that undeveloped eggs, dead
embryos or dead hatchlings are equally useful moni-
toring units. That nest contents would constitute a non-
invasive and meaningful monitor of heavy metal bur-
dens in marine turtles is further supported by the ®nd-
ings of Sakai et al. (1995), who demonstrated that egg
concentrations correlated with those in the female from
which they were sampled. Additionally, whilst metal
concentrations tend to be generally low in eggs, given
the large number laid by reproductively active females
(Broderick and Godley, 1996), excretion of metals via
eggs may be a substantial elimination route in this
group. Sakai et al. (1995) suggested that this might not
be important (<0.5% of the cadmium burden and
<5% of the mercury burden per clutch), but appear to
have ignored the fact that turtles lay multiple clutches,
over many years. At the very least, further monitoring of
metal burdens in marine turtles in the Mediterranean
Sea region would seem prudent, especially from those
ranging into more intensively industrialised regions such
as Spain, Italy and Greece.
This work constituted part of a Ph.D. study by B.J.G. funded by a
University of Glasgow Post-Graduate Scholarship. Authors gratefully
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