Trace element levels in foetus–mother pairs of short-beaked common
dolphins (Delphinus delphis) stranded along the French coasts
V. Lahayea,1, P. Bustamantea, W. Dabinb, C. Churlaudc, F. Cauranta,⁎
aCentre de Recherche sur les Ecosystèmes Littoraux Anthropisés, UMR 6217 CNRS-IFREMER-Université de La Rochelle,
Université de La Rochelle, 22 Avenue Michel Crépeau, 17042 La Rochelle Cedex, France
bCentre de Recherche sur les Mammifères Marins, Institut du Littoral et de l'Environnement, Port des Minimes, Avenue du Lazaret, 17000 La Rochelle, France
cCentre Commun d'Analyses, Université de La Rochelle, 5 Perspectives de l'Océan, 17071 La Rochelle Cedex 9, France
Received 28 August 2006; accepted 30 May 2007
Available online 12 July 2007
Tissues of foetus–mother pairs of common dolphins (Delphinus delphis) stranded along the French coasts (Bay of Biscay and English
Channel) were analysed for their Cd, Cu, Hg, Se and Zn contents. In the kidneys, foetal Cd levels were extremely low, and strong relationships
between Cu and Zn suggested the involvement of metallothioneins since early foetal life. The results also indicated a limited maternal transfer of
Hg during pregnancy since levels in the tissues of foetuses were below 1 μg g−1w.wt. However, hepatic Hg levels in foetuses increased with body
length, and were also proportionate to maternal hepatic, renal and muscular Hg levels. Lastly, affinities between Hg and Se in tissues would
participate in Hg neutralisation in both mothers – through tiemannite granules – and fetuses – through reduced glutathione – counteracting the
toxic effects linked to the particularly high quantities of methyl–Hg to which marine mammals are naturally exposed.
© 2007 Elsevier Ltd. All rights reserved.
Keywords: Marine mammals; Mercury; Selenium; Pregnancy; North-Eastern Atlantic
During the last thirty years, a considerable body of data has
been built up on pollutants levels in marine mammals (e.g.
Wagemann and Muir, 1984; Law, 1996; Borrell and Reijnders,
1999). Indeed, due to their longevity and their elevated position
in marine food webs, these organisms are generally considered
as the integrators of the contamination of the environment
(Reijnders, 1988). Some concerns have already been raised
regarding adverse effects of pollutants, which include repro-
ductive failures (e.g. Reijnders, 1980, 1986). Among generally
focused contaminants, non essential heavy metals like cadmium
(Cd) and mercury (Hg) are widely dispersed in the environment,
since they are released from both natural and anthropogenic
sources (Nriagu, 1996). Food is the major route of uptake of
these elements for marine mammals, and consequently adult
dolphins often display high metal levels in their tissues (Aguilar
et al., 1999). Hence, the question of the importance of toxic
metal transfer from mother to offspring is raised. Indeed, metals
could be transferred from mothers to fetuses – via the placenta –
and to suckling calves – via the milk – affecting them during
their most sensitive periods of development. Generally,
important metal exposure of human offspring to methyl–Hg
can affect their normal neuronal development (WHO, 1990)
whereas high dose of Cd during the gestational period can
produce growth retardation in rat calves (Rohrer et al., 1979;
Baranski et al., 1982). Such an altered growth is known to be
induced by zinc (Zn) deficiency in foetuses, which may be
caused by elevated maternal Cd impregnation (Brzoska and
Numerous laboratory experiments and epidemiological
studies have enabled to better understand the modalities of
transfer of trace elements to offspring and their associated toxic
Environment International 33 (2007) 1021–1028
E-mail address: firstname.lastname@example.org (F. Caurant).
1Present address: School of Biological Sciences, University of Aberdeen,
Tillydrone Avenue, Aberdeen ABZ4 2TZ, United Kingdom.
0160-4120/$ - see front matter © 2007 Elsevier Ltd. All rights reserved.
effects in rodents and humans (see the reviews of Bell, 1984 and
of Chang, 1984). However, determining the impact of toxic
contaminants in wildlife marine mammal populations is more
levels and potential toxic effects are not evident to show in situ,
and 2) sampling is opportunistic. Sample accessibility easily
explains why little data is available on trace element bioaccu-
mulation in foetuses of cetaceans and is generally limited to few
individuals (Itano and Kawai, 1981; Honda and Tatsukawa,
1983; Fujise et al., 1988; Law et al., 1992; Caurant et al., 1993;
Yang et al., 2004).
originate from two basic sources, i.e. strandings and direct or
events. In the first case, the chemical levels may not reflect
sometimesthose ofhealthypopulations sincestranded individuals
poor nutritional status (e.g. Frank et al., 1992; Olsson et al., 1994;
Bennett et al., 2001; Das et al., 2004; Dehn et al., 2005). Such
biases are likely to be excluded when using animals from mass
living stranding events or accidental by-catches.
This study focussed at mother–foetus pairs of short-beaked
common dolphins (Delphinus delphis) from the North-Eastern
Atlantic. We used two sources of samples, for which metal
levels are likely to correctly reflect those of the healthy
population, i.e. 1) a mass living stranding event composed of
females and their calves, which got accidentally trapped during
the ebb tide in a shallow bay of the English Channel (Pleubian,
North coast of Brittany, February 2002) and 2) single stranding
events of accidentally by-caught dolphins along the Atlantic
French coastline (2002–2003). In these waters, common
dolphins typically feed on fish and cephalopods (Pierce et al.,
2004), which may expose them to a contamination risk by Hg
(Bloom, 1992; Bustamante et al., 2006) and Cd (Bustamante
et al., 1998, 2002). This cetacean species reach 20–30 years old,
and its gestation period is about 11 months (Collet, 1981;
Murphy, 2004). Such characteristics make the common dolphin
a suitable species to clarify the importance of trace element
gestational transfer in marine mammals. The investigated non
essential elements were Cd and Hg, plus essential elements
interacting in their detoxification processes. Firstly, we focussed
on copper (Cu) and zinc (Zn) measurements because they are
contained in metallothioneins (MTs), which play a key role in
Cd detoxification (see the review of Das et al., 2000a).
Secondly, selenium (Se) levels were examined because of its
well-known co-precipitation with Hg, which lead to accumu-
lation of non toxic granules of tiemannite (HgSe) in the liver
(e.g. synthesis of Law, 1996). The present objectives were 1) to
provide trace element levels in foetus–mother pairs of common
dolphins, and 2) to determine which factors are likely to
influence metal accumulation in foetuses.
2. Material and methods
This study is based on 17 foetus–mother pairs of common dolphins stranded
alongthe Frenchcoasts. Mostof the specimens(i.e. 10pairs) originatedfromthe
mass living stranding event composed of 47 females and their calves (Pleubian,
February 2002). The 7 other pairs were collected following single stranding
events along the Atlantic French coastline during January months of 2002 and
2003. Post-mortems were carried out by veterinarians or by trained biologists of
the Centre de Recherche sur les Mammifères Marins (CRMM) from the
University of La Rochelle, and results were included in the European program
BIOCETreports (Pierce et al., 2004). The nutritional condition of these animals,
established from visual assessment of dorsal muscles and blubber thickness, was
good in most cases (n=11) and medium in the other cases (n=6). No individuals
could be classified as showing a poor nutritional condition. Concerning single
stranding events, carcasses were fresh (intact pigmentation, cloudy eyes, tern
coloration of organs during dissection), except in the case of one individual,
which was slightly decomposed (skin peeling, moderate smell of decomposi-
tion). Moreover, some external observations (broken rostrum, amputated flukes)
have permitted to classify all these individuals as accidentally by-caught.
Note that before necropsy, total body length was measured (rostrum to fluke
notch) and values for foetuses ranged from 32 to 60 cm. In the North-Eastern
Atlantic, common dolphins have a length of 90–100 cm at birth (Collet, 1981;
Murphy, 2004). Thus, foetuses from this study would have been collected at
early to mid-pregnancy periods.
Various tissues and organs were sampled during necropsies. Teeth of
mothers were collected in order to determine age, following the recommenda-
tions of Perrin and Myrick (1980). One GLG (Growth Layer Group) is
consideredto represent oneyearin commondolphins(Gurevichetal., 1980)and
ages were recorded to the nearest 0.5 GLG. In addition, the kidneys and the liver
of foetuses and mothers were systematically sampled and stored in plastic bags
at −20 °C for trace element analyses. Muscle and blood samples were collected
from a subset of mothers and added to the sampling in order to investigate
modalities of Hgtransferto foetuses.Blood wasdirectly collectedfrompregnant
females (n=9) that died following the mass living stranding event and samples
were stored into sterile polypropylene tubes.
With the exception of blood, all fresh samples were freeze-dried and ground to
powder. The mean ratios between dry weight (d.wt.) and wet weight (w.wt.) were
the kidneys in foetuses and mothers, respectively. Each sample was then treated in
duplicate. For total Hg measurements, aliquots ranging from 0.5 to 3 mg of dried-
material, as well as thawed whole-blood from mothers, were analysed directly in an
Advanced Mercury Analyser spectrophotometer (Altec AMA 254). For the other
trace element analyses, 2 aliquots of approximately 200 mg of each homogenised
dry sample were digested with 3.5 mL of 65% HNO3at 60 °C for 3 days. The
digested contents were then diluted to 10 mL in milli-Q quality water. Then Cd, Cu
and Zn contents were assayed using a flame (Varian 250 Plus) Atomic Absorption
Spectrometer (AAS) with deuterium background correction whereas Se and some
low Cd contents were analysed with graphite furnace AAS (Hitachi Z-5000) with
Zeeman background correction. Quality controls were made using standard
reference materials from National Research Council of Canada (NRCC), i.e.
dogfish liver (DOLT-2 and DOLT-3), dogfish muscle (DORM-2), and lobster
hepatopancreas (TORT-2). These reference materials were treated and analysed
under the same conditions as the samples. Results were in good agreement with the
certified values (Table 1). In addition, the laboratory participates in intercalibration
exercises organised by the International Atomic Energy Agency (cf. Coquery et al.,
1999). During the last exercise, our laboratory was classified in group 1, indicating
the good quality of results for all analysed elements (Azemard et al., 2006).
Detection limits (μg g−1d.wt.) were 0.004 for Cd, 0.5 for Cu, 3 for Zn, 0.8 for
Se, and 0.005 for Hg. All concentrations below the detection limit were
replaced with “dummy values” that were half of the detection limit in order to
allow further statistical comparisons (Gibbons and Coleman, 2001). Metal
levels in dolphin tissues were expressed as μg g−1w.wt.
Spearman rank correlation coefficients were used 1) to determine
intermetallic relationships in the kidneys and the liver of foetuses, mothers,
and between the mother–foetus pairs, and 2) to establish correlations between
trace elements and length of foetuses or age of mothers. Particular attention was
paid to Hg, for which foetus–mother relationships were investigated using
maternal concentrations in blood, muscle, kidneys, and liver.
3. Results and discussion
Table 2 gathers mean trace element levels in the tissues and blood of
foetus and mother common dolphins stranded along the French coasts.
With the exception of Cd, all trace elements were present at higher
1022 V. Lahaye et al. / Environment International 33 (2007) 1021–1028
concentrations in the liver of both foetuses and mothers. Note that
foetuses from single stranding events were smaller than ones from the
massliving strandingevent. Inaddition, trace element levelsin theliver
et al., 1998; Zhou et al., 2001; Carvalho et al., 2002; Das et al., 2000b,
2003; Lahaye et al., 2005; Lahaye, 2006) and no significant differences
of non essential element levels were detected in females of various
reproductive status (Lahaye, 2006).
3.1. Cadmium, copper and zinc
All foetuses of common dolphins displayed renal and hepatic Cd
concentrations that were below the detection limit of AAS, as opposed
to the relatively high Cd concentrations found in the tissues of some
mothers (Table 2). Such low foetal Cd levels were previously reported
in other cetacean species from various areas (Table 3).
According to Webb (1979), metallothioneins (MTs) may act as
detoxifiers of Cd in animals which are able to accumulate this metal in
their tissues as common dolphin mothers do. Furthermore, pregnant
and lactating females have generally an increased induction of MTs to
accommodate increasing demand and storage of essential elements
(Solaiman et al., 2001). In pregnant females, Cd binding to MTs may
also prevent the transfer of Cd across the placenta (Hanlon et al., 1982).
From both human epidemiological studies and laboratory experiments
on animals, it effectively appears that the placenta may provide to the
foetus a certain degree of protection against Cd entrance (Bell, 1984).
In fact, placenta itself contains MTs and it may serve as a filter for Cd
by storing it (Itoh et al., 1996; Kuriwaki et al., 2005).
In adult marine mammals, Cd, Cu, and Zn are all contained in MTs
(see the review of Das et al., 2000a). Both Cu and Zn have the ability to
induce the biosynthesis of this protein (Kägi and Nordberg, 1979). The
chemical similarity between Cd and Zn (Tsalev and Zaprianov, 1983)
make Cd able to displace Zn ions from MTs (Mochizuki et al., 1985),
which may result in a further synthesis of these proteins (Simkiss et al.,
1982). The competition between Cd and Zn for the binding sites of
MTs might involve a co-accumulation of Cd and Zn in tissues (Toyama
et al., 1986; Wagemann et al., 1988), and especially in the kidneys
where Cd levels are the highest. Only a fraction of the total Cu and Zn
in tissues may also be bound to MTs, while practically all of the Cd in
Trace element levels (mean±SD; μg g−1d.wt.) in standard reference materials
Metals Standard reference materials (NRCC)
TORT-2 DORM-2DOLT-2 DOLT-3
Certified valueObserved valueCertified value Observed valueCertified valueObserved value Certified valueObserved value
Trace element levels (mean±SD; μg g−1w.wt.) in the tissues and blood of foetus–mother pairs of common dolphins
Sample characteristics Trace element levels (μg g−1w.wt.)
Sampling areaID Length (cm) or age⁎
Tissue CdCu HgSeZn
Bay of Biscay
(single stranding events; n=7)
(mass living stranding event; n=10
NB:⁎Length is used for foetuses whereas age stands for mothers; LD: limit of detection; nd: not determined.
1023 V. Lahaye et al. / Environment International 33 (2007) 1021–1028
chronically exposed animals may occur as MTs or MT-like proteins
(Wagemann and Hobden, 1986). Here, Cd and Zn were strongly and
positively correlated in the kidneys of mothers (RSpearman=0.932,
Pb0.001, Table 4). Hence, owing to the expected binding of Cd to MTs
in the kidneys of mothers, the transfer to offspring through the placenta
might be prevented.
In the liver, Cu levels varied greatly between foetuses and mothers.
The particular high Cu levels encountered in the liver of foetuses points
out an important transplacental transfer of this metal (e.g. Underwood,
1977; Law, 1996; Wagemann et al., 1988; Yang et al., 2004). Elevated
Cu levels in offspring could be due to either bioaccumulation of Cu
during pregnancy with low excretion rates in foetus or a specific
biochemical requirement for development (Wagemann et al., 1988). In
other words, foetuses could have only limited Cu excretion via bile or
elevated MTs in the liver to store essential elements for growth. Here,
hepatic Cu concentrations were significantly and positively correlated
to foetus length (RSpearman=0.655, Pb0.001, Table 4), which indicates
an effective bioaccumulation of Cu during pregnancy. Moreover, the
strong relationship between Cu and Zn in the kidneys of foetuses
(RSpearman=0.740, Pb0.001, Table 4) may reflect an involvement of
MTs in the sequestration of those essential elements during pregnancy,
as previously been reported in rats (Klaassen and Liu, 1997).
3.2. Mercury and selenium
Total Hg levels in foetuses were far lower than those of mothers
(Table 2). In addition, Hg levels in common dolphin foetuses from the
North Eastern Atlantic waters were comparable to those previously
reported in foetuses of other cetacean species, but they were, to some
extent, lower than those found in several species from the Pacific and
the Faroe Islands (Table 3).
Both the increase of Hg levels with body length in the liver of
foetuses (RSpearman=0.821, Pb0.001, Table 4) and their positive
correlations with hepatic, renal and muscular levels of mothers
(RSpearmanN0.6, Pb0.001, Table 5) strongly suggest a maternal transfer
of Hg during the prenatal life. However, this maternal Hg transfer
would be rather limited since Hg levels in the tissues of foetuses were
below 1 μg g−1w.wt. (Table 2).
Only methyl–Hg may be able to go through the placenta (Chang,
1984; WHO, 1990). Previous works suggested that limited transpla-
cental transfer of Hg in cetaceans is due to an efficient demethylation
process in the liver of mothers, with the formation of tiemannite
granules (HgSe), which in turn leads to low levels of methyl–Hg likely
to be transferred to foetuses (e.g. Caurant et al., 1993; Law, 1996). The
close relationship between Hg and Se in the liver of mothers
(RSpearman=0.961, Pb0.001, Table 4) strongly comforts this hypothesis
whereas the absence of such strong correlation in the liver of foetuses
(RSpearman=0.525, Pb0.05, Table 4) may indicate that this process is
not active at this life stage. This result, together with the far excess of
Trace element levels (mean±SD; μg g−1w.wt.) in the kidneys and the liver of cetacean foetuses (literature data)
Sample characteristics Trace element levels (μg g−1w.wt.) References
Species Sampling areaLength (cm) TissueN Cd CuHg Se Zn
Law et al. (1992)
Lahaye et al. (in press)
Fujise et al. (1988)
Yang et al. (2004)
Itano and Kawai (1981)
Pacific Ocean Honda and Tatsukawa (1981)
Honda and Tatsukawa (1983)
Caurant et al. (1993) Faroe Islands
na Liver5 0.83±0.402.43±1.43 54.7±36.0
NB: na, not available; LD, limit of detection.
Associations between trace elements, length of foetuses, age of mothers
(independent variables) and dependent variables at 0.90bP≤0.95 (not
underlined), 0.95bP≤0.99 (underlined) and Pb0.99 (double underlined)
The direction of the correlation coefficient of Spearman is indicated by algebraic
sign in front of the independent variable. NB:⁎Independent variables refer to
1024V. Lahaye et al. / Environment International 33 (2007) 1021–1028
Se compared to Hg amounts in foetus livers, also emphasizes the fact
that a threshold level of Hg is necessary to induce the formation of
tiemmanite (e.g. Palmisano et al., 1995).
The inability of foetuses to demethylate Hg could make them more
sensitive to methyl–Hg during their prenatal life. Maternal transfer of
methyl–Hg can be estimated through measurements of Hg in mother
blood. Total Hg levels found in blood of common dolphin mothers from
themassliving stranding eventranged from0.201to0.611 μgg−1w.wt.,
i.e. a mean of 0.426±0.120 μg g−1w.wt. (n=9; Table 2), corresponding
to a Hg level of 452±127 μg l−1in common dolphin blood. Higher Hg
concentrations were found in Pacific mature striped dolphins, with a
mean total Hg level of 1.4±0.4 μg g−1w.wt. (n=9), of which 70% was
methylated, i.e. mean methyl–Hg level of 0.95±0.45 μg g−1w.wt. (Itano
2000). According to the methyl–Hg proportion found in the blood of
Pacific striped dolphins, blood methyl–Hg mean concentration of our
studied pregnant common dolphins could be estimated around 300 μg l−1.
However, such result remains a rough estimate of maternal transfer of
only recent exposure to this metal, which may vary according to feeding
activity and/or age (Nielsen et al., 2000; Dehn et al., 2005). Thus, Hg is
taken up by all tissues from the bloodstream, and the initial phase of tissue
distribution takes about 1 to 2 days after a single dose (see review by
Clarkson, 1997). Moreover, the half time in blood has been evaluated to
body-that is less than 80 days (WHO, 2000). Further investigations on
factors influencing Hg concentrations in blood should have to be carried
In human adults, the signs or symptoms of methyl–Hg poisoning
become detectable at concentrations of about 200 μg l−1in blood
(Lauwerys, 1990). Although equivalent or even higher concentrations
are found in adult cetacean blood, no poisoning symptoms of Hg have
been observed to date (Itano and Kawai, 1981; Hyatt et al., 1999;
Nielsen et al., 2000). This clearly indicates that the adaptative
capacities of marine mammals to demethylate Hg in their liver might
modify the kinetic of Hg poisoning commonly described in other
organisms. In this study, Hg concentrations in blood seem to indicate
elevated short-time exposure of dolphins to methyl–Hg, which would
be readily neutralised in the liver of mothers.
Despite the high Hg levels measured in the blood of mature striped
dolphins (see above), Itano and Kawai (1981) observed relatively low
Hg concentrations in the blood of foetuses, i.e. 0.16±0.07 μg g−1w.wt
(n=4), but most of the metal was methyl–Hg (0.15±0.06 μg g−1w.wt,
i.e. 16±6 μg l−1). The authors suggested that, beside the already
mentioned methylated form (70% of total Hg), Hg in the maternal blood
may exist in a chemical form (i.e. combined with Se) that would be not
vary according to mother's diet, Hg concentrations in the blood of
human offspring under a chronic exposure to methyl–Hg during
pregnancy, i.e. 5.8 μg l−1methyl–Hg in cord blood (US NRC (United
an elevated methyl–Hg exposure to wild common dolphins remain
difficult to determine.
In addition, through their dietary consumption of seafood, marine
mammals may also benefit from important intakes of Se that protect
them against methyl–Hg. Experiments in rodents have shown that Se
could protect offspring against methyl–Hg toxic effects by preventing
it to go through the foetal blood–brain barrier via a methyl–Hg
trapping mechanism by glutathione (Fredriksson et al., 1993). In fact,
dietary supplementation of Se may increase activities of certain
enzymes like glutathione peroxydase and/or glutathione transferase,
leading to an increase of reduced glutathione in tissues and blood
(Schnell et al., 1988; Hassan et al., 1985), for which methyl–Hg has a
great affinity (Thomas and Smith, 1979; Naganuma and Imura, 1979).
Hence, total Hg concentrations in the blood of rodents fed with Se-
enriched diet were higher than those fed on standard diet, as a result of
Spearman rank correlation coefficients between Hg levels in foetuses (liver,
kidney) and mothers (liver, kidney, muscle, blood) at 0.90bP≤0.95 (not
underlined), 0.95bP≤0.99 (underlined) and Pb0.99 (double underlined)
NB: ns refers to not significant coefficients.
Fig. 1. Relationships between Hg and Se molar levels (nmol g−1w.wt.) in the liver of common dolphin foetuses. Foetuses from the mass living stranding event are
represented by black squares, and those from single stranding events by white squares.
1025V. Lahaye et al. / Environment International 33 (2007) 1021–1028
the methyl–Hg trapping mechanism by glutathione (Fredriksson et al.,
1993). Such processes might also occur in other mammals, like
In common dolphins, hepatic Hg and Se accumulate with length in
foetuses during gestation (RSpearman, Hg=0.821, Pb0.01; RSpearman
Se=0.552, Pb0.05) as well as with maternal hepatic Hg and Se levels
(Table 4). Thus, molar concentrations of Se increase with Hg in foetus
liver (Fig. 1). However, Hg:Se molar ratio is not correlated with foetus
body length since Se is far in excess compared to Hg (Fig. 2). This
excess may prevent the neurotoxic effects of methyl–Hg present in
large proportion in their blood. Regarding the relatively low Hg levels
encountered in the tissues of mother common dolphins (Table 2),
maternal transfer of Hg through the placenta is also unlikely to cause
severe effects to dolphin foetuses in European waters.
Trace element levels in common dolphin foetuses from the
North Eastern Atlantic waters were relatively low compared to
those encountered in several species from the Pacific and the
cross the placenta, the amounts that actually accumulated in the
tissues of the foetuses were relatively low (b1 μg g−1w.wt.),
regarding the levels of methyl–Hg to which they may con-
tinuously be in contact with (around 300 μg l−1in maternal
blood). Comparisons with epidemiological studies on humans
and laboratory experiments on rodents highlighted that marine
mammals may have developed efficient mechanisms to
counteract the very high levels of methyl–Hg to which they
are naturally exposed. Hence, affinities between Hg and Se may
participate in detoxification mechanisms in both mothers
through the formation of tiemannite granules, and foetuses
through the binding to reduced glutathione.
Sampling was carried out by the Réseau National
Echouages, co-ordinated by the Centre de Recherche sur les
Mammifères Marins (CRMM) of La Rochelle. This work was
funded by the European program BIOCET (EC: EVK3-CT-
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