Marine Pollution Bulletin 62 (2011) 1606–1615

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Marine Pollution Bulletin

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The occurrence of chemical elements and POPs in loggerhead turtles

(Caretta caretta): An overview
S. D’Ilio a,⇑, D. Mattei a, M.F. Blasi b, A. Alimonti a, S. Bogialli c
a
Italian National Institute for Health, Department of Primary Prevention, Viale Regina Elena 299, 00161 Rome, Italy
b
Filicudi WildLife Conservation, Stimpagnato Filicudi (Messina), 98050, Italy
c
University of Padova, Chemical Sciences Department, Via Marzolo 1, 35131 Padova, Italy

a r t i c l e i n f o a b s t r a c t

Keywords: Chemical elements and persistent organic pollutants (POPs) are globally present in aquatic systems and
Loggerhead turtles their potential transfer to loggerhead marine turtles (Caretta caretta) has become a serious threat for their
Chemical elements health status. The environmental fate of these xenobiotics may be traced by the analysis of turtles’ tissues
Persistent organic pollutants and blood. Generally, loggerhead turtles exhibited a higher metal load than other turtle species, this could
Environmental pollution
be explained by differences in diet habits being food the main source of exposure. Literature shows that
muscle, liver and kidney are most considered for the quantification of chemical elements, while, organic
compounds are typically investigated in liver and fat.
This paper is an overview of the international studies carried out on the quantification of chemical ele-
ments, polychlorinated biphenyls (PCBs), organochlorines (OCs) and perfluorinated compounds (PFCs), in
tissues, organs and fluids of C. caretta from the Mediterranean Sea, the Atlantic and the Pacific Oceans.
Ó 2011 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1607
2. Geographical distribution, habitat and biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1607
3. Major and trace elements in tissues, organs and fluids. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1607
3.1. Liver . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1608
3.2. Kidney . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1608
3.3. Lung . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1608
3.4. Muscle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1608
3.5. Adipose tissue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1608
3.6. Bone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1608
3.7. Heart and spleen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1610
3.8. Blood, gonads and spinal cord . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1610
3.9. Pancreas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1610
3.10. Brain and urinary bladder. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1610
3.11. Carapace. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1610
3.12. Eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1610
3.13. Minority studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1610
4. Persistent organic pollutants (POPs) in tissues and organs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1611
4.1. Polychlorinated biphenyls. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1611
4.2. Organochlorine compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612
4.3. Perfluorinated compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612
5. Analytical techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1612
6. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1613
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1613

⇑ Corresponding author. Address: Italian National Institute for Health, Department of Environment and Prevention, Viale Regina Elena 299, 00161 Rome, Italy. Tel.: +39
0649902252; fax: +39 0649902011.
E-mail address: sonia.dilio@iss.it (S. D’Ilio).

0025-326X/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2011.05.022
 S. D’Ilio et al. / Marine Pollution Bulletin 62 (2011) 1606–1615
1. Introduction
Inorganic contaminants and persistent organic pollutants
(POPs) are present in aquatic systems worldwide as a consequence
of their wide-spread usage and long-range transport. Coastal and
marine pollution is increasing throughout the world and a critical
threshold for many pollutants is almost unknown (Domingo and
Bocio, 2007; Hamann et al., 2010; Sobek et al., 2010). The bioaccu-
mulation of these toxic substances has become a matter of concern
for its possible transfer to food chain and impact on several wildlife
species of the marine environment, including loggerhead sea tur-
tles (Caretta caretta) (Marcotrigiano and Storelli, 2003; Keller
et al., 2005; Moon et al., 2010; Ogata et al., 2009; Roose and Brink-
man, 2005). Contamination of marine system is one of the key re-
search priorities highlighted by 35 sea turtle researchers from 13
nations working in fields related to turtle biology and/or conserva-
tion (Hamann et al., 2010).
Heavy metals in marine mammals (cetaceans, like dolphins and
beluga) may produce alterations in the immune function and in-
crease the incidence of infectious diseases (Cámara Pellissó et al.,
2008). Different authors assessed trace element body burden in
dolphins, all of them agreed on the need of establishing toxicolog-
ical consequence of this metal accumulation (Lavery et al., 2008;
Stavros et al., 2011) and spatial or temporal variations of stable
inorganic and organic pollutant levels (Holsbeek et al., 1998; Raach
et al., 2011; Yordy et al., 2010). Concentration of trace elements in
tissues of seals revealed difference in species accumulation provid-
ing possible basis for the evaluation of species susceptibility (Ikem-
oto et al., 2004).
Sea turtles are long-living vertebrates that may bioaccumulate
these contaminants from food, sediment and water. In this regard,
sea turtles are considered of increasing interest as potential bioin-
dicators for pollution in marine ecosystems (Andreani et al., 2008;
Godley et al., 1999; Keller et al., 2004b; Sakai et al., 2000). The con-
centrations of chlorobiphenyls (CBs) and organochlorine pesticides
(OCPs) in tissues of three marine turtle species from Mediterranean
and European Atlantic waters revealed that the level of these or-
ganic contaminants decreases in the order: logger-
head > green = leatherback. These differences may be related to
the diet habits of loggerhead turtle and its higher position in the
marine food chain. This may lead to a greater exposure to contam-
inants than the other two species (Mckenzie et al., 1999). Logger-
head sea turtles were tracked by satellite in combination with
the analysis of stable isotope in order to provide a means of linking
different phases of the migration cycle of these marine vertebrates.
The authors recommended the analysis of stable isotope and other
chemical markers as a standard procedure integrated with all stud-
ies of migratory vertebrates equipped with satellite transmitters.
This would open new perspectives in forensic tracking methodolo-
gies to increase proportionally the knowledge from a limited num-
ber of individuals to sample sizes that are more significant from a
population point of view (Zbinden et al., 2011). The loggerhead C.
caretta is the most abundant marine turtle species present in the
Mediterranean Sea and it can be also found in the Atlantic, the Pa-
cific and the Indian Oceans and other parts of the world (Day et al.,
2005; Nagelkerken et al., 2003; Caurant et al., 1999; Mingozzi
et al., 2007). Since 1975, C. caretta was included in Red List of
threatened species of the International Union for Conservation of
Nature (IUCN, 2009).
The present paper presents an overview on data of international
literature on the occurrence of trace elements and POPs in different
tissues, organs and fluids of loggerhead sea turtles (C. caretta) from
the Mediterranean Sea, the Atlantic and the Pacific Oceans, as a con-
tribution to the knowledge of the contamination levels of the species
and, more in general, of the marine environments.
1607
2. Geographical distribution, habitat and biology
Loggerhead sea turtles (C. caretta) are fairly widely distributed
across subtropical and temperate latitudes (Márquez, 1990). In
the Atlantic Ocean, the greatest concentration is along the South
eastern coast of North America and in the Gulf of Mexico (Spotila,
2004). Nesting extends as far North as Virginia, as far South as Bra-
zil, and as far East as the Cape Verde Islands. Along the African
coastline, loggerheads nest from Mozambique’s Bazaruto Archipel-
ago to South Africa’s St. Lucia estuary. Eastern Australia and Japan
are the major nesting areas. In the Mediterranean Sea, turtles nest
on eastern basin shores, mainly in Greece, Turkey and Cyprus
(Groombridge, 1994; Pritchard and Mortimer, 1999). C. caretta is
the most frequent chelonian in the Italian waters, with egg-laying
sites localized in southern Italy, Sardinia, Sicily and in its smaller
islands (Di Palma, 1978).
Migratory flux of loggerhead turtles near and through the Strait
of Gibraltar has been reported in both directions. Thanks to this
connection, Atlantic and Mediterranean loggerhead populations
share developmental habitats in western Mediterranean and in
North eastern Atlantic (Margaritoulis et al., 2003; Camiñas and
De La Serna, 1995). Loggerheads spend most of their life cycle in
marine environments, they are carnivorous, foraging primarily on
benthic invertebrates throughout their distribution range. The
great availability of food and warm shallow waters seem to be
ideal for foraging and as over-wintering environment.
Like other species, loggerhead sea turtles are migratory, and the
life cycle period influences the distance of their travel (Meylan,
1982; Meylan et al., 1983; Hughes, 1989; Limpus et al., 1992).
From nesting sites, hatchlings move to the open ocean foraging
on the surface, then they start a developmental migration towards
near-shore and continental shelf waters, foraging at the bottom in
the shallow fringes of the sea. Oceanic juveniles from this popula-
tion are distributed along the Mediterranean basin (Margaritoulis
et al., 2003). Juveniles and subadults feed in coastal areas, usually
far from their hatching ground (Carr, 1987; Bowen et al., 1993,
1995; Bolten et al., 1998). Sexually mature turtles move to specific
mating and nesting sites during the breeding season, they return
thereafter to the foraging and wintering areas where they spend
much of their life (Miller, 1997).
3. Major and trace elements in tissues, organs and fluids
Aluminum, As, Cd, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Sb, Se and Zn are the
elements most investigated in specimens of C. caretta. The collection
of papers has revealed that the 13 elements are analyzed according
to the following decreasing percentages: Cd (14.8), Cu (13.1), Pb
(12.5), Zn (12.1), total Hg (11.5), Fe (10.4), Ni (6.9), Mn (6.7), Al, As,
B, Ba, Cr, Mg, Sb and Se (<5). Chromium, Cu, Fe, Mn, Ni, Se and Zn play
an essential role in animal metabolism and growth (Alam and Brim,
2000), in particular, Cu and Fe have a crucial function in oxygen
transport, energy production and enzyme activity. Some essential
(Cu, Fe, Mn and Zn) and a limited number of toxic elements (As, Cd
and Pb) can be also transferred from the mother to turtle eggs (Kaska
et al., 2004). Cadmium is typically long-term accumulated in kidney,
this is principally due to its binding by metallothionein, while Cu and
Zn tend to accumulate in liver (Andreani et al., 2008). Mercury has
been recognized to induce toxic effects in fish, including neurotox-
icity, impaired growth and development, reduced reproductive suc-
cess, liver and kidney damage and immunomodulation. In the
aquatic systems, the inorganic Hg is microbially transformed to
the more toxic and bioavailable methylmercury (MeHg), a potent
neurotoxin with a strong tendency to biomagnify in aquatic food
webs (Day et al., 2005, 2007; Kampalath et al., 2006).
1608 S. D’Ilio et al. / Marine Pollution Bulletin 62 (2011) 1606–1615
Liver, muscle and kidney have been investigated in stranded
individuals of C. caretta because of the high level of accumulated
contaminants. Pancreas, spleen, bones and carapace were also con-
sidered, but it is generally difficult to comprehend the significance
of this data because of the lack of knowledge on the baseline levels
of those contaminants in marine turtles (Storelli et al., 1998b). If
we consider the number of samples analyzed (distributed as a per-
centage) per organ, tissue and fluid of C. caretta, the following trend
is highlighted: liver (20), muscle (19.6), kidney (15.8), lung (6.8),
blood (8.8), bone (6.3), fat (4.4), egg shell (3.5), carapace (3.4), albu-
men, bladder, brain, eggs, egg yolk, gonads, heart, pancreas, spinal
cord and spleen (62).
The international studies collected on C. caretta were carefully
selected in order to avoid repetition of data. Organs, tissues and
fluids are singularly discussed in this text and a comprehensive
summary of mean value concentration ranges is provided in
Table 1.
3.1. Liver
In the Mediterranean Sea, the analysis revealed a wide range of
concentration for Cd, while, lower values were found in French
coast of the Atlantic Ocean and the Baja California peninsula (Mex-
ico). A Japanese research found 9.74 ± 3.37 lg g1 (w.w.) in six
samples of female sea turtles living in their coastal waters of the
Pacific Ocean. Five groups of researchers studied Cu reporting sim-
ilar values in loggerhead turtles from Mediterranean coasts of Italy
(South and East), Spain, Turkey and Atlantic coasts of France, while,
higher values from Japan, Canary Islands, Italy (West), and Baja
California peninsula (Mexico). However, a different expression of
results, in terms of moisture content, may lead to higher concen-
tration in the same area (Andreani et al., 2008; Maffucci et al.,
2005). Iron was almost always at very high level in this organ com-
pared to other elements. This is probably due to the high degree of
vascularization of liver tissue (Storelli et al., 2005). Mediterranean
and Atlantic (coasts of USA) turtles had moderately low concentra-
tions of total Hg, these levels are also consistent with those of Gulf
of California (Mexico). On the contrary, Pacific coasts of Japan
exhibited rather higher values (Sakai et al., 2000). For Mn, the re-
sults of two investigations from Mediterranean were in good
agreement, while, species living in different environments, like
Japanese and Mexican coasts of the Pacific Ocean, showed lower
values (Sakai et al., 2000; Gardner et al., 2006).
Toxic and carcinogenic effects of Ni compounds may be associ-
ated to nickel-mediated oxidative damage to DNA and inhibition
of cellular antioxidant defenses, but there is no evidence to support
these effects in turtles of Italian and Spanish coasts of the Mediterra-
nean Sea (Franzellitti et al., 2004; Torrent et al., 2004). In addition,
the chemical form of Ni ingested by turtles from fish and marine
invertebrates is still unclear. A narrow range of concentration of Pb
was quantified in turtles from the Mediterranean Sea and the pacific
Ocean. Similarly to Fe, in this organ Se was at the highest concentra-
tion in respect of other tissues. The accumulation of Zn is primarily
due to the binding of metals by metallothionein (Andreani et al.,
2008), its levels in turtles from the Mediterranean Sea, the Pacific
and the Atlantic Oceans were quite homogenous.
3.2. Kidney
It is well known that Cd is preferentially accumulated in kidney
at relatively high levels. Loggerhead turtles from the Mediterra-
nean Sea, the Atlantic Ocean from Japanese and Mexican coasts
of the Pacific Ocean seem to confirm this tendency. Copper can
be found at physiological level in kidney and is considered to be
the element with the lowest concentration. As previously men-
tioned, Fe tends to accumulate in liver rather than kidney. Low
concentrations of Hg seem to be very common for turtles from
Mediterranean Sea, Atlantic Ocean and Mexican coasts, except for
a Japanese study that presented high data (Sakai et al., 2000). As re-
gards Mn, liver and kidney exhibit very similar concentrations.
Three studies presented high values of Pb (Kaska et al., 2004; Tor-
rent et al., 2004; Godley et al., 1999), while for the rest only a min-
or variation is highlighted and in one case Pb was not measurable
(Andreani et al., 2008). For Se only studies from Mediterranean
were available (Kaska et al., 2004; Storelli et al., 1998b). Finally,
concentrations of Zn of no concern were detected from the Medi-
terranean Sea, the Atlantic and the Pacific Oceans.
3.3. Lung
Cadmium, Cu, Fe, Hg, Mn, Ni, Pb, Se and Zn were the elements of
most interest for lung in the international literature. From these re-
sults no particular concern has arisen for these elements. The rela-
tively high concentrations of Fe are probably due to the degree of
vascularization of this organ. As for Hg, only a Japanese study
found a high level (Sakai et al., 2000) comparing with two Italian
studies. Manganese is an essential cofactor for some enzymes,
but it is also toxic for mammals at high doses. Lung was found to
be the main site of accumulation of Mn in a study from the Medi-
terranean Sea (Franzellitti et al., 2004).
3.4. Muscle
Generally, the concentration of elements tends to be low in this
tissue (Godley et al., 1999; Sakai et al., 2000; Andreani et al., 2008;
Caurant et al., 1999; Storelli et al., 2005, 1998b; Kaska et al., 2004;
Torrent et al., 2004; Maffucci et al., 2005; Franzellitti et al., 2004;
García-Fernández et al., 2009; Gardner et al., 2006). In particular,
Hg was found to be at very low levels in loggerhead turtles from
different parts of the world (the Mediterranean Sea, the Pacific
and the Atlantic Oceans), except for a Japanese study reporting a
value of one order of magnitude higher (Sakai et al., 2000). Copper,
Fe, Mn, Ni, Pb and Se were also quantified at very low levels. On the
other hand, Zn shows the highest average value in this tissue (And-
reani et al., 2008; Maffucci et al., 2005; Franzellitti et al., 2004; Gar-
cía-Fernández et al., 2009).
3.5. Adipose tissue
Nickel seems to accumulate in adipose tissue of loggerhead tur-
tles living in the Adriatic Sea (18.77 ± 4.40 lg g1 w.w.) (Fran-
zellitti et al., 2004), but the authors could not establish the
reason for such elevated levels. While, others studies reported sig-
nificantly lower levels (0.17 lg g1 d.w. and <0.03 lg g1 w.w.)
(Gardner et al., 2006; Sakai et al., 2000). Zinc seems to be accumu-
lated in this tissue, but this phenomenon was not clearly explained
(96.1 ± 18.8, 64.7 ± 22.47 and 68.2 ± 34.7 lg g1 w.w.), since sea
turtles have a quite stable diet, it is difficult to find an association
to specific feeding habits (Sakai et al., 2000; Storelli et al., 2005;
Franzellitti et al., 2004). Another hypothesis associates the content
of Zn with pigment proteins responsible for the particular colora-
tion, slight green, of lipid layer of these animals (Storelli et al.,
2005). Cadmium, Cu, Fe, Hg, Mn, Pb and Se were quantified at lev-
els of no major interest.
3.6. Bone
Two studies out of three (from the Mediterranean Sea and the
Pacific Ocean) recorded high values of Zn in bone (197 ± 26.5 and
51.28 ± 5.76 lg g1 w.w.) (Sakai et al., 2000; Torrent et al., 2004;
García-Fernández et al., 2009). Lead is usually high in hard tissues,
as bone and carapace, its concentrations ranged from 0.99 to
 S. D’Ilio et al. / Marine Pollution Bulletin 62 (2011) 1606–1615 1609

Table 1
Range of mean values for elements in liver, kidney, lung and muscle (from literature).

Element lg g1 Liver Kidney Lung Muscle Reference

M A P M A P M A P M A P
Al w.w. 2.2 – – 0.7 – – – – – 1.5 – – Torrent et al. (2004)
As d.w. 14.2–22 – – 19–30 – – 8.7–24 – – 20.8–69 – – Kaska et al. (2004), Storelli and
Marcotrigiano (2000b)
w.w. 6.7–17.1 – – 13.8 – – – – – 15.5 – – Storelli et al. (1998b), Torrent et al.
(2004)
Cd d.w. 2.4–23 – 1.8b 5.8–57 – 73.1b 1.4–5.7 – – 0.2–3.6 – 0.1b Andreani et al. (2008), Gardner et al.
(2006), García-Fernández et al.
(2009), Godley et al. (1999), Kaska
et al. (2004), Storelli and
Marcotrigiano (2000b), Maffucci
et al. (2005)
w.w. 2.5–5.9 2.6 9.7 5.0–10.5 13.3 45.5 0.2–0.5 – 0.4 0.07–1.1 0.08 0.06 Caurant et al. (1999), Franzellitti
et al. (2004), García-Fernández et al.
(2009), Sakai et al. (2000), Storelli
et al. (2005), Torrent et al. (2004)
Cr d.w. 1.1–2.8 – – 1.6–2.1 – – 2.3–2.5 – – 1.4 – – Storelli and Marcotrigiano (2000b),
Kaska et al. (2004)
b b
Cu d.w. 3.0–37.3 – 33.9 2.1–5.6 – 4.4 2.8–3.8 – – 1.5–5.0 – 0.4b Andreani et al. (2008), Gardner et al.
(2006), García-Fernández et al.
(2009), Kaska et al. (2004), Maffucci
et al. (2005), Torrent et al. (2004)
w.w. 5.4–7.7 8.3 19.4 1.2–4.6 2.2 1.3 0.8–1.8 – 0.6 0.6–2.9 0.7 0.95 Caurant et al. (1999), Franzellitti
et al. (2004), García-Fernández et al.
(2009), Sakai et al. (2000), Storelli
et al. (2005), Torrent et al. (2004)
Fe d.w. 15.7–1232 – – 15.3–764 – 237b 15.6–184 – – 20.6–85.4 - 77.4b Andreani et al. (2008), Gardner et al.
(2006), Kaska et al. (2004)
w.w. 342–456 – 917 38.0–48.2 – 30.0 107–184 – 134 1.0–60.9 – 22.2 Franzellitti et al. (2004), García-
Fernández et al. (2009), Sakai et al.
(2000), Storelli et al. (1998b), Storelli
et al. (2005), Torrent et al. (2004)
Total d.w. 1.1–2.4a – 1790 0.47a–0.9 – 1080 0.45 - - 0.4–0.69 – 410 Godley et al. (1999), Kampalath et al.
Hg (2006), Maffucci et al. (2005),
Storelli and Marcotrigiano (2000b)
w.w. 0.04–0.4 0.59 8150 0.04–0.16 0.21 304 0.06 – 127 0.18–0.21 0.16 189 Day et al. (2007), Sakai et al. (2000),
Storelli and Marcotrigiano (2000b),
Storelli et al. (2005), Torrent et al.
(2004)
Mn d.w. 7.5 – 1.3b 7.0 – 6.0b 1.2 – – 1.4 ± 0.24 - 0.84b Andreani et al. (2008), Gardner et al.
(2006)
w.w. 6.2 – 2.2 - – 2.0 5.3 – 0.25 – – 0.43 Franzellitti et al. (2004), Sakai et al.
(2000)
Ni d.w. 11.6 – 0.35b 9.6 – 0.04b 10.1 – – 10.0 – 0.01 Franzellitti et al. (2004), Gardner
et al. (2006), Kaska et al. (2004)
w.w. 2.9–4.4 – <0.03 5.8 v 0.22 1.8 – <0.03 2.8 – 0.08 Franzellitti et al. (2004), Kaska et al.
(2004), Sakai et al. (2000), Torrent
et al. (2004)
Pb d.w. 0.1–3.6 – – 0.5–4.0 – 0.03b 0.6–4.0 – – 0.5–2.5a – 0.01b Andreani et al. (2008), García-
Fernández et al. (2009), Godley et al.
(1999), Kaska et al. (2004), Storelli
and Marcotrigiano (2000b)
w.w. 0.16–3.0 – 0.21 0.12–2.4 – 0.16 0.03 – <0.03 0.04–2.3 – 0.02 García-Fernández et al. (2009), Sakai
et al. (2000), Storelli et al. (2005),
Torrent et al. (2004)
Sb d.w. - – – 2.35 – – 3.06 – – 2.51 – – Kaska et al. (2004)
Se d.w. 9.8–15.9 – – 7.8–15.5 – – 7.4–10.8 – – 2.5–11.2 – – Kaska et al. (2004), Maffucci et al.
(2005), Storelli and Marcotrigiano
(2000b)
w.w. 3.5–46.5 – – 2.2 – – 1.2 – – 1.7 – - Storelli and Marcotrigiano (2000b),
Storelli et al. (2005)
Zn d.w. 66.0–107 – 69.1b 27.9–119 – 32.5b 75.0 – – 7.1–107 – 31.1b Andreani et al. (2008), Gardner et al.
(2006), García-Fernández et al.
(2009), Kaska et al. (2004), Maffucci
et al. (2005)
w.w. 13.5–29.3 25.0 28.1 9.1–23.1 23.6 28.4 17.0– – 16.7 6.7–30.9 19.6 25.0 Caurant et al. (1999), Franzellitti
22.5 et al. (2004), García-Fernández et al.
(2009), Sakai et al. (2000), Storelli
et al. (2005), Torrent et al. (2004)

M = Mediterranean Sea; A = Atlantic Ocean; P = Pacific Ocean.

a
Median.
b
Geometric mean.
1610 S. D’Ilio et al. / Marine Pollution Bulletin 62 (2011) 1606–1615
3.53 lg g1 w.w. (Sakai et al., 2000; Torrent et al., 2004; García-
Fernández et al., 2009). In general, the concentrations of Cd, Cu,
Fe, Mn and Ni were very low, but the number of samples analyzed
is generally limited.
3.7. Heart and spleen
Cadmium was detected at similar concentration with a maxi-
mum value of 2.2 lg g1 d.w. in heart (Andreani et al., 2008) and
1.19 lg g1 w.w. in spleen (Sakai et al., 2000). Iron is generally
present at relatively elevated levels in highly vascularized organs
like heart and spleen (Storelli et al., 2005). In heart, the concentra-
tion ranged from 47.4 lg g1 w.w. to 314 lg g1 d.w. (Sakai et al.,
2000; Andreani et al., 2008; Storelli et al., 2005), whereas in spleen
varied from 44.8 to 221 lg g1 w.w. (Sakai et al., 2000; Storelli
et al., 2005). A single study measured Se in both organs
(1.40 ± 0.36 and 1.45 ± 0.81 lg g1 w.w.), being this element rarely
quantified (Storelli et al., 2005). Cadmium, Mn, Ni and Pb showed
low levels equally distributed in the two matrices, whereas, quite
inhomogeneous values were reported for Cu, Hg and Zn.
3.8. Blood, gonads and spinal cord
Blood is the primary means of transportation of Hg throughout
the body and target organs (Day et al., 2010), in fact, blood was
proved to be an effective predictor of total Hg stored in muscle
and spinal cord (Day et al., 2005). Only one study determined Cd,
Cu, Fe, Mn, Pb and Zn in gonads of three individuals from Italian
coasts (Andreani et al., 2008).
3.9. Pancreas
A Japanese study found an accumulation of Cd (39.2 ± 16.1
lg g1 w.w.) and Mn (26.4 ± 20.2 lg g1 w.w.) (Sakai et al., 2000)
in comparison to the Italian lower results for Cd (2.6 ± 1.9 lg g1
d.w.) and Mn (1.34 ± 0.65 lg g1 d.w.) (Andreani et al., 2008). While,
both investigations reported comparable values for Zn and very
low levels of Ni and Pb. The same two papers also discussed Cu, Hg
and Fe.
3.10. Brain and urinary bladder
The level of Cd, Cu, Fe, Hg, Mn, Ni, Pb and Zn in brain is generally
low (Sakai et al., 2000; García-Fernández et al., 2009). One study
presented relatively high concentrations of Cd (11.16 ± 4.61 lg
g1 d.w.), Ni (7.99 ± 1.94 lg g1 d.w.) and Pb (3.96 ± 2.16 lg g1
d.w.) in urinary bladder of turtles stranded along the Turkish
beaches (Kaska et al., 2004). A different research quantified Cu,
Fe, Mn, Se and Zn at concentrations of no risk for turtles’ health, ex-
cept for a high value of Hg (37.0 ± 15.5 lg g1 w.w.) (Sakai et al.,
2000).
3.11. Carapace
Low values of Hg were quantified in carapace of live and
stranded individuals of the Atlantic coasts (0.461 ± 0.009 and
0.941 ± 0.299 lg g1 w.w.) (Day et al., 2005). Many other elements
were also analyzed in carapace (Cd, Cu, Fe, Mn, Ni, Pb, Zn) obtain-
ing for Hg different concentrations (Sakai et al., 2000).
3.12. Eggs
The content of elements in whole eggs is typically lower than in
liver and kidney. This is particularly highlighted in a Japanese
study that quantified Cd at concentration 10- or 20-fold less in eggs
(Sakai et al., 2000). Low levels of Cu, Fe, Mn, Ni and Zn were also
shown in two papers (Sakai et al., 2000; Alam and Brim, 2000).
Selenium is seldom analyzed, it was determined in one research
on turtles from the Atlantic coasts (Alam and Brim, 2000). A
marked difference was observed for Hg between high data from
the Pacific Ocean (Sakai et al., 2000) and the low levels obtained
from the Mediterranean Sea and the Atlantic Ocean (Godley
et al., 1999; Alam and Brim, 2000). In eggs collected in nests from
six beaches of the Northwest Florida, Al shows a geometric mean of
25.54 lg g1 (d.w.) (Alam and Brim, 2000).
One author analyzed albumen in six individuals with the fol-
lowing results: Cd 0.49 ± 0.24, Cu 0.129 ± 0.083, Fe 0.870 ± 0.377,
Hg 0.012 ± 0.0034, Mn 0.17 ± 0.30, Ni < 0.03, Pb < 0.03 and Zn
0.59 ± 0.58 lg g1 (w.w.) (Sakai et al., 2000).
Eggshell of turtles from Pacific (<0.01 lg g1 w.w.) (Sakai et al.,
2000) and Turkish coasts of the Mediterranean Sea (0.649 ±
0.131 lg g1 d.w.) (Kaska and Furness, 2001) revealed a slightly
different but low content of Cd. On the other hand, consistent val-
ues were found for Cu (5.57 ± 0.767 lg g1 w.w. and 5.29 ± 0.48
lg g1 d.w.), Fe (10.6 ± 2.20 lg g1 w.w. and 17.75 ± 7.00 lg g1
d.w.) and Zn (2.17 ± 0.59 lg g1 w.w. and 5.00 ± 2.20 lg g1 d.w.)
(Sakai et al., 2000; Kaska and Furness, 2001) for both investigations.
Mercury was below the limit of detection (LoD) in eggshell from
Turkey (Kaska and Furness, 2001) and a value of 4.05 ± 1.31 lg g1
(w.w.) from Japan (Sakai et al., 2000). Manganese and Ni were also
very low at concentrations of 0.68 ± 0.48 and <0.03 lg g1 (w.w.)
(Sakai et al., 2000), and Pb from <0.03 to 0.633 ± 0.162 lg g1
(d.w.) (Sakai et al., 2000; Kaska and Furness, 2001).
Two papers reported values of no concern in yolk for Cd, Fe, Hg,
Pb and Zn (Sakai et al., 2000; Kaska and Furness, 2001). Nickel was
below 0.03 and Mn at 0.91 ± 0.42 lg g1 w.w. (Sakai et al., 2000).
Finally, data for Cu was in agreement with previous results in
whole eggs (Sakai et al., 2000; Kaska and Furness, 2001).
3.13. Minority studies
Although metals are preferably accumulated in liver, higher
levels of total As were reported in muscle tissue (interval of
2.64–31.21 lg g1 w.w.) of marine turtles beached along the Ital-
ian coast (the South Adriatic sea) (Storelli and Marcotrigiano,
2000b). This elevated concentration of As in muscle tissue was also
confirmed in other studies on turtles from Turkish and Italian
coasts in the Mediterranean sea (at level of 20.80 ± 9.97 and
68.94 lg g1 d.w.) (Kaska et al., 2004; Storelli et al., 1998b). This
was probably due to the fact that most of the As is present in the
organometallic form, such as, arsenocoline and arsenobetaine,
which are very stable and complexes physiologically inactive.
Loggerhead turtles feeding on algae and mollusks are therefore ex-
pected to accumulate high concentrations of this element (Storelli
et al., 1998b; Saeki et al., 2000; Torrent et al., 2004).
Aluminum in liver, kidney, muscle and bone of loggerhead
turtles stranded in the Canary Islands (Spain) was discovered at
mean values of 2.21 ± 0.53, 0.72 ± 0.16, 1.49 ± 0.26 and 30.49 ±
5.77 lg g1 (w.w.), respectively. Since bone is the tissue where Al
is preferably stored, this considerably high level of Al finds its jus-
tification (Torrent et al., 2004).
Comparable mean concentrations of Cr were present in liver
(1.05 ± 0.58 and 2.77 ± 0.93 lg g1 d.w.) (Kaska et al., 2004; 42),
kidney (1.57 ± 2.05 and 2.06 ± 0.59 lg g1 d.w.) (Kaska et al.,
2004; Storelli and Marcotrigiano, 2000b), lung (2.29 ± 1.73 and
2.54 ± 0.83 lg g1 d.w.) (Kaska et al., 2004; Storelli and Marcotrigi-
ano, 2000b), bladder (1.96 ± 0.62 lg g1 d.w.) (Kaska et al., 2004),
eggs (geometric mean, 1.2 lg g1 d.w.) (Alam and Brim, 2000)
and muscle of turtles beached along the Mediterranean Sea
(1.43 ± 0.87 lg g1 d.w.) (Storelli and Marcotrigiano, 2000b).
Methylmercury in liver varies from 0.24 to 0.33 lg g1 (w.w.)
and from 0.16 to 0.41 lg g1 (w.w.) in muscle tissue of C. caretta
 S. D’Ilio et al. / Marine Pollution Bulletin 62 (2011) 1606–1615 1611

found stranded along the coasts of the South Adriatic sea (Italy)
(Storelli et al., 1998a). In muscle tissue Hg is mainly present in
the methylated form while in liver in lower percentage. This low
content of MeHg in liver may be explained with a detoxification
process that takes place in this organ that involves demethylation
of MeHg. The assumption of a demethylation process occurring in
liver tissue seems to be confirmed by a study that analyzed MeHg
in adipose, muscle, liver and kidney tissue of sea turtles (Kampa-
lath et al., 2006; Storelli et al., 1998a). Muscle tissue of marine
organisms contains Hg for the most part as MeHg, whereas, in liver
the inorganic form is dominant, a similar trend can be observed in
turtles (Storelli and Marcotrigiano, 2003).
A number of minor elements (B, Ba, Be, Mg, Mo and V) were
analyzed in unhatched eggs from Northwest Florida, but only Ba
and Mg were present at detectable concentrations (geometric
mean of six beaches 2.80 and 1822 lg g1 d.w.) (Alam and Brim,
2000). One study focused on the determination of Sb in muscle
(2.51 ± 0.82 lg g1 d.w.), lung (3.06 ± 1.53 lg g1 d.w.), kidney
(2.35 ± 0.69 lg g1 d.w.), bladder (0.96 ± 0.52 lg g1d.w.) and liver
(below the detection limit) (Kaska et al., 2004).
4. Persistent organic pollutants (POPs) in tissues and organs
Persistent organic pollutants are unique chemicals because they
possess the following characteristics, they are: (i) persistent in the
environment even for decades; (ii) capable of concentrating in fatty
tissues, transferring to food chain and traveling to long distances
(generally moving from tropical and temperate regions to northern
latitudes); (iii) linked with serious health effects in humans and
other living organisms (even for exposure to low level). For these
reasons, POPs represent a concern for the environment at
compounds (PFCs) are the most studied persistent organic pollu-
tants. Among OCs, organochlorinated pesticides and hexachloro-
benzene (HCB) are the two most important classes investigated
by different authors. Their characteristics and environmental fate
make them similar to other POPs. Table 2 summarized the ranges
of single values for PCBs, pesticide and its metabolites and PFCs
in organs, tissues and fluids from literature.
4.1. Polychlorinated biphenyls
Polychlorinated biphenyls have been reported having effects on
the immune, endocrine and reproductive system of different ani-
mal species (Fox, 2001). These compounds are able to bioaccumu-
late and their catabolic process generally occurs in liver and/or
intestine of vertebrates. For this reason, the analysis of PCBs are
mainly conducted on lipophilic organs involved in detoxification
activities. Unfortunately, no threshold level of toxicity exists for
sea turtles and each congener exhibits a different toxicity.
The level of PCBs in C. caretta was deeply investigated by several
researchers (Keller et al., 2004b; Storelli and Marcotrigiano, 2000a;
Corsolini et al., 2000; Cobb and Wood, 1997; Storelli et al., 2007;
Alava et al., 2006; Orós et al., 2009; Richardson et al., 2010). The
maximum mean value (expressed as a sum of eight congeners)
was experimented in specimens of stranded turtles from the Atlan-
tic Ocean (Canary Island) during a surveillance program over the
year 2001–2005 (Orós et al., 2009) and the East Adriatic Sea (Lazar
et al., 2011). The cachexia observed in these turtles may indicate a
previous remobilization of fat and pollutants as well as the high
concentration of PCBs observed in liver (Orós et al., 2009). The
P
mean concentrations of PCB in liver of 30 samples was
1980 ± 5320 ng g (w.w) and in adipose tissue 450 ± 1700 ng g1
1

international level. Unfortunately, almost all living organisms on
Earth contain measurable levels of these substances in their tissues
(Joint FAO/WHO document, 1993).
For the preservation of sea turtles, polychlorinated biphenyls
(PCBs), organochlorine compounds (OCs) and perfluorinated
(w.w.), with a remarkable contribute of the deca-congener PCB
209 (1200 ± 3120 ng g1 w.w) in liver and the hepta-congener
PCB 180 (217 ± 907 ng g1 w.w.) in adipose tissue. Slightly higher
P
values of PCB (474 ± 547 ng g1 w.w.) were registered in adipose
tissue of 27 turtles in a recently study (Lazar et al., 2011) with a

Table 2
Ranges of singles results for three classes of organic contaminants in organs, tissues and fluids (from literature).

Matrix ng g1 RPCBs RDDT RPFCs Reference

M A P M A P M A P
Eggs d.w. – – – – 753–800 – – – – Alam and Brim (2000)
l.w. – 10,100 ± 5466 – – – – – – – Cobb and Wood (1997)
w.w. – 144–3720 50.2 ± 92a – – – – Alam and Brim (2000), Alava et al. (2006)
Liver l.w. 210–6540 – – 250–1810 – – – – – Storelli and Marcotrigiano (2000a)
w.w. 6.9–298 <LoD-34,900 19.3 ± 5.8 2.3–73.6 <LoD-811 – – – – Storelli et al. (2007), Corsolini et al. (2000),
Richardson et al. (2010), Monagas et al.
(2008), Orós et al. (2009)
Kidney l.w. 240–5070 – – 90–1590 – – – – – Storelli and Marcotrigiano (2000a)
w.w. 0.9–113 – – 0.4–29 – – – – – Storelli et al. (2007)
Lung l.w. 120–4010 – – 100–780 – – – – – Storelli and Marcotrigiano (2000a)
w.w. 0.54–116 – – 0.12–33.1 – – – – – Storelli et al. (2007)
Heart l.w. 110–4820 – – 80–1550 – – – – – Storelli and Marcotrigiano (2000a)
Muscle l.w. 100–3110 – – 100–770 – – – – – Storelli and Marcotrigiano (2000a)
w.w. 0.6–23.5 – – 0.3–4.9 – – – – – Storelli et al. (2007), Corsolini et al. (2000)
Fat w.w. 136–2934 8.0–9800 – 39.3–449 <LoD-449 – – – – Keller et al. (2004b), Lazar et al. (2011),
Corsolini et al. (2000), Monagas et al.
(2008), Orós et al. (2009)
Plasma w.w. – – – – – – – 11.2 ± 17.3a (PFSs) – Keller et al. (2005)
15.8 ± 19.1a(PFCas)
w.w. – 1.5–13.7 – – 0.24–1.0 – – – – Keller et al. (2004a)
Blood w.w. - 0.12–23.9 – – 0.19–3.8 – – – – Keller et al. (2004a,b)
P
PCBs = sum of polychlorinated biphenyls.
P
DDT = sum of DDT pesticide and its metabolites.
P
PFCs = sum of perfluorinated compounds.
d.w. = dry weight; l.w. = lipid weight; w.w. = wet weight.
M = Mediterranean Sea; A = Atlantic Ocean; P = Pacific Ocean.
PFSs = perfluoroalkylsulfonates compounds; PFCas = perfluorocarboxylate compounds.
a
Mean ± standard deviation.
1612 S. D’Ilio et al. / Marine Pollution Bulletin 62 (2011) 1606–1615
PCB profile dominated by hexa- and hepta-chlorinated congeners.
The congeners most analyzed in both matrices were PCB 180,
PCB 153, PCB 28 and 31, hexa- and tri-congeners, respectively.
However, no histological lesions entirely ascribable to the acute ef-
fects of PCBs were described. The levels in liver are 10 times higher
than those occurred in stranded specimens from Mediterranean
Sea (Corsolini et al., 2000) (119 ± 60 ng g1 w.w.) and even 100
times higher than those registered from Pacific coast of Mexico
(19.3 ± 5.80 ng g1 w.w.) (Richardson et al., 2010).
P
Average levels of PCB of 4.65 ± 5.58 ng g1 (w.w.) in muscle
tissues and 52.32 ± 74.99 ng g1 (w.w.) in liver were measured in
19 sea turtles sampled in Eastern Mediterranean (Cobb and Wood,
1997). While values of 0.16 ± 0.06 lg g1 in muscle tissues and
5.01 ± 1.22 lg g1 in liver (both expressed as lipid weight) were re-
ported from the same sites (Storelli and Marcotrigiano, 2000a).
When blood and adipose tissue are analyzed in pair, blood concen-
P
trations of PCB and RTCDD-like PCBs are 5.56 ± 5.28 and
0.395 ± 0.426 ng g1 respectively, about 50–100 times lower than
the corresponding concentrations in adipose tissue (Keller et al.,
2004b). Eggs were analyzed for PCBs in three cases (Cobb and
Wood, 1997; Alam and Brim, 2000; Alava et al., 2006) with the
aim of selecting a non invasive tool of analysis. The mean concen-
tration of PCB in 22 samples from southern Florida was
144 ± 280 ng g1 (w.w.) (Alava et al., 2006), while an order of mag-
nitude higher was found in eggs collected from the East cost of USA
(Alam and Brim, 2000; Cobb and Wood, 1997). One paper has
simultaneously investigated PCB levels in eggs and chorioallantoic
membranes and it turned out to be that for membranes values
were ten times higher than eggs (Cobb and Wood, 1997). Wherever
the distribution of PCB congeners was discussed, PCB 138 and PCB
153, the hexa-congeners shown the highest concentration, fol-
lowed by PCB 180 and PCB 101, the penta-congener. A different
distribution was revealed in a surveillance program of the Canary
Islands (Orós et al., 2009) that identified the deca-congener PCB
209 as the main contributor (about 60%) of sum of PCB compounds.
4.2. Organochlorine compounds
Organochlorine compounds are well known to bioaccumulate
in animal tissues inducing hepatotoxicity, wasting, immunotoxic-
ity, developmental abnormalities and reproductive toxicity along
with endocrine disruption, neurobehavioral effects and population
declines (Fox, 2001).
Several studies were carried out on levels of organochlorinated
pesticide in sea turtles from different areas of the world (Pugh and
Becker, 2001). A contamination was reported in C. caretta from the
Atlantic Ocean West coast (Keller et al., 2004a,b), the Canary Is-
lands (Monagas et al., 2008) and from the Mediterranean Sea (Kel-
ler et al., 2004b; Storelli and Marcotrigiano, 2000a; Cobb and
Wood, 1997; Lazar et al., 2011). The pesticides more often investi-
gated are DDT, chlordane congeners, and dieldrin. Since DDT pos-
sesses lipophilic property, the highest average concentration of
this pesticide (expressed as a sum of congeners) was found in adi-
pose tissue of 44 live specimens from North Carolina (Keller et al.,
2004a) and in liver of 22 samples stranded in Canary Island (Keller
et al., 2004a).
The distribution through the organism was carried out by
studying the concentration in liver, kidney, lung and muscle tissues
of turtles living in the Mediterranean Sea (Cobb and Wood, 1997),
while adipose tissue was not analyzed. In this research, the levels
of organochlorine ranged from 18.27 ± 18.40 to 1.45 ± 1.10 ng g1
(w.w.) according to the order liver > kidney > lung > muscular tis-
sue; they were also found to be positively correlated with the tis-
sues lipid content. A similar trend was observed for the same
matrices in 13 turtles beached in the Adriatic Sea (Storelli and Mar-
cotrigiano, 2000a). In this case the heart was sampled showing
higher concentrations than muscle and lungs tissues. This survey
also reported concentration levels of HCB (0.02–0.04 lg g1, lipid
weight), but they did not seem to depend on the matrices analyzed
(Storelli and Marcotrigiano, 2000a).
Organochlorine contaminants were monitored in non-invasive
matrices like whole blood (Keller et al., 2004a; Pugh and Becker,
2001), plasma and red blood cells (Pugh and Becker, 2001) and
similarly to other mammalians, plasma contained the highest con-
centrations, followed by blood and red blood cells. These findings
suggested that plasma may be the best blood component to be
used in monitoring OCs in sea turtles. However, adipose tissue re-
tains a level of OCs more than 100 times higher than blood (Keller
et al., 2004a).
Unhatched eggs collected in Florida were analyzed for the con-
tent of DDT, chlordane, dieldrin, mirex, PCB and HCH (Alam and
Brim, 2000; Alava et al., 2006). In the Southern coast, DDT and
its congeners were found at mean concentration level of
50.2 ± 92.4 ng g1 (w.w.) with a significant amount of chlordane;
P
while dieldrin, mirex and HCH were 20–200 times lower than
P
DDT (Alava et al., 2006). On the other hand, only p,p0 -DDD was
tested at about 800 ng g1 d.w. in the Northwest coast (Alam and
Brim, 2000).
4.3. Perfluorinated compounds
Perfluorinated compounds are a broad class of chemicals that
have their main applications as polymerization adjuvant, flame-
retardants and in electronic and plastic industries (Hekster et al.,
2003). PFCs were recognized as emerging environmental contami-
nants widespread in the Earth and identified in wildlife tissues. The
strength of the carbon–fluorine bond makes these substances very
persistent. Toxic effects like tumor promotion, liver damage and
alterations in hormones levels were registered in laboratory on
animals exposed to PFCs (Olsen et al., 2003). The perfluorooctane-
sulfonate (PFOS) and perfluorooctanoic acid (PFOA), bearing to
sub-classes of PFCs, namely perfluoroalkylsulfonates and perflu-
orocarboxylates, are commonly measured in environmental sam-
ples and particular attention was paid to their suspected role as
Endocrine Disruptors (Lau et al., 2007). Only one group reported
the analysis of PFCs in plasma (Keller et al., 2005; O’Connell
et al., 2010) and serum (O’Connell et al., 2010) of specimens of C.
caretta coming from different sites of Atlantic West coast. PFCs,
PFOS and PFOA are the predominant compounds detected with
mean concentrations of 11.0 ng g1 and 3.20 ng g1, respectively,
while the concentrations of short-chain perfluorocarboxylates
were negligible. Some statistical considerations indicated that bio-
accumulation of PFCs in plasma depends on age and site of cap-
tures. A similar consideration was accounted in a study (Keller
et al., 2005) that considered 163 samples of serum and plasma of
juvenile sea turtles from USA Atlantic coast. Juvenile specimens
were selected in order to avoid biases from reproductive offloading
and limit the contributes due to bioaccumulation and migration.
PFOS was found to be the dominant compound (from 0.31 to
39.0 ng g1). Its concentration was interestingly correlated to the
human population together with perfluoroundecanoate (PFUnA),
since the release of this compound can be attributed to the con-
sumers rather than the manufacturing production. Since 2004,
the industrially use of these substances began to be limited and
current trend indicates a substantial decrease of the presence of
PFCs in the environment.
5. Analytical techniques
Six analytical techniques were employed for the quantification
of elements in organs, tissues and fluids of loggerhead turtles
 S. D’Ilio et al. / Marine Pollution Bulletin 62 (2011) 1606–1615
(C. caretta). Atomic Absorption Spectrometry (AAS) was mostly
adopted in the analysis of As, Cd, Cu, Fe, Pb, Zn, and in all studies
in the case of Mn, Sb and Se. Analysis of Al was solely carried out
by Inductively Coupled Plasma Atomic Emission Spectrometry
(ICP-AES) and AAS. As for Cold Vapor AAS there is a percentage
of use of 46% (Hg), maximum of 91% (Fe) for AAS, from 6% (Cd)
to 21% (As) for ICP-AES, finally, an interval between 2% (Fe) and
13% (Cr) is reported for Anodic Stripping Voltammetry (ASV). Mer-
cury was determined in different percentages by Automatic Mer-
cury Analyzer (AMA, 30%), Isotopic Dilution Cold Vapor
Inductively Coupled Plasma Mass Spectrometry (ID-CV-ICP-MS,
16%) and Cold Vapor Atomic Fluorescence Spectrometry (CV-AFS,
8%).
As regards organic contaminants, they are almost invariably
analyzed by using gas chromatographic (GC) separation coupled
with Electron Capture Detectors (ECDs) or Mass Spectrometric
Detectors (MS). This can be addressed to the hydrophobic, ther-
mo-stable and volatile nature of the pollutants considered, bearing
to the POPs chemicals. Moreover, the majority of these substances
are halogenated, therefore they required robust, cheap and sensi-
tive ECD detectors. The unequivocal identification of the target
compounds is assured if the most selective MS detector is em-
ployed. Perfluorinated compounds were analyzed using Liquid
Chromatography (LC)-tandem MS equipments. This class of ther-
molabile and medium-strong acids organic compounds could be
conveniently separated by LC and determined in the high selective
negative ionization mode.
6. Conclusions
International literature on trace elements in tissues and organs of
loggerhead turtles (C. caretta) shows that muscle, liver and kidney
are the matrices most considered by different authors. Al usually
stores in bone, even if it is also accumulated in brain (Torrent et al.,
2004). The highest levels of Cd are found in kidney according to
the trend observed in other marine mammals, followed by liver, lung
and muscle. The distinctive accumulation of Hg in liver is reported by
many researchers for other marine organisms like dolphins, seals
and porpoises (Storelli et al., 1998b). The total concentration of Hg
measured in organs of individuals tends to vary as follows:
liver > kidney > muscle > adipose (Kampalath et al., 2006). Copper
and Se exhibit the highest levels in liver (Caurant et al., 1999; Storelli
et al., 2005; Maffucci et al., 2005). Iron show the highest concentra-
tion in all tissues examined, commonly in this decreasing order:
liver > kidney > gonads > heart > pancreas > lung > muscle > adi-
pose tissue (Andreani et al., 2008). However, the high concentration
of Fe in liver, heart and lung are in relation to the high degree of vas-
cularization of these tissues (Storelli et al., 2005). Rather homoge-
neous concentrations of Ni can be found in liver, lung and muscle,
while in some cases the highest accumulation is observed in adipose
tissue (Franzellitti et al., 2004). Among the internal tissues and or-
gans, significant amounts of Mn, Pb and Zn are accumulated in hard
tissue like bone and carapace (Sakai et al., 2000; Torrent et al., 2004;
García-Fernández et al., 2009).
Generally, loggerhead turtles exhibit a higher metal load than
other turtle species (for instance green turtles) (Sakai et al.,
2000). Differences in diet habits may explain this contamination
in the population under study of C. caretta, in fact, loggerhead
turtles are carnivorous and in this respect, several studies high-
lighted that food is the main source of exposure to chemical ele-
ments. These observations could be extended to organic
compounds by taking into account the impact on adipose tissue.
In fact, animals with abundant deposits of fat are able to tolerate
relatively high concentrations of toxic lipophilic chemicals,
because of a lower availability to target organs, such as liver. On
1613
the contrary, low-fat animals which mobilized their lipid, they
may be more vulnerable to toxic substances (Bernhoft and Skaare,
1994).
Liver and fat are the matrices of choice for the investigation of
organic compounds, because they reflect the chemico-physical
properties of the target analyte. Differences in the geographical
contamination might be evaluated by the levels of PCBs and OCs
in liver and adipose tissue. Data available show that, in liver of tur-
tles from the Atlantic Ocean, the level of organic contaminants is at
least 10 times higher than that found in the Mediterranean Sea,
while, values from the Pacific Ocean are still scarce for a compara-
tive estimation. Minor variations seem to be for the content of PCBs
P
and DDT in adipose tissues of the Atlantic Ocean and the Medi-
terranean Sea, nevertheless, additional information about age, sex
and dietary behavior is strongly recommended in order to make
hypothesis about this phenomenon. Eggs, plasma and blood have
been analyzed only in specimens collected in the Atlantic Ocean.
The level of contamination in plasma and blood is relatively low,
if compared to other organs and tissues. Very few studies have
been conducted on eggs, these non-invasive matrices are useful
samples for future evaluation of spatial and temporal trends of or-
ganic contamination of C. caretta. At present, a correlation between
organic contamination and health status of sea turtles is difficult to
propose because of limited numbers of data available.
Sampling of blood is the least considered to assess trace ele-
ments exposure in loggerhead turtles, in spite of this, its use should
be encouraged. In fact, blood can be non-lethally collected and al-
most all of total Hg present in blood is MeHg, this can help in
avoiding an expensive and time-consuming speciation analysis
(Day et al., 2007). Furthermore, blood may be used to assess and
monitor a potential contamination of turtle’s environment over
the time, also thanks to recaptured individuals in the recovery cen-
ters. Monitoring of POPs by using blood and eggs may be also a
useful tool in large-scale projects for the conservation of C. caretta.
The amount of data available on chemical contamination of sea
turtles and the effects on their health is still relatively limited, the
implementation of monitoring programs and investigations may
help to protect and control the health status of the entire popula-
tion of C. caretta.
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