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Science of the Total Environment 373 (2007) 94 – 102
www.elsevier.com/locate/scitotenv

Metal profiles used as environmental markers of Green Turtle

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(Chelonia mydas) foraging resources
Ana Talavera-Saenz a,b , Susan C. Gardner a,⁎,

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Rafael Riosmena Rodriquez b , Baudilio Acosta Vargas a
a
Centro de Investigaciones Biológicas del Noroeste, S.C. (CIBNOR) Mar Bermejo #195, Col. Playa Palo de Santa Rita. A.P. 128,
23090, La Paz, Baja California Sur, Mexico
b
Programa de Investigación en Botánica Marina, Departamento de Biología Marina, Universidad Autónoma de Baja California Sur. La Paz,
Baja California Sur 23080 Mexico

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Received 12 June 2006; received in revised form 8 October 2006; accepted 9 October 2006
Available online 22 December 2006
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Abstract
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The Baja California Peninsula, Mexico serves an important role for feeding and developing sea turtles. High concentrations of
metals detected in green turtles (Chelonia mydas) from Magdalena Bay prompted an investigation into the sources of metals in the
region. We compared metal concentrations in sea turtle tissues with plant species found in their stomach contents, and with the
same species of plants collected inside a sea turtle refuge area known as Estero Banderitas. Differences in the metal concentrations
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between marine plant species were minimal. Principal components analysis of the percent contribution of individual metals to the
overall metal signature of each plant or tissue sample generated three principal components that explained 80.7% of the total
variance in the data. The plant samples collected within Estero Banderitas formed a separate grouping from the green turtle tissue
samples and the plants from the stomach contents. The plants in the stomach contents contained greater percent contributions of Cd
and Zn than the plants collected inside the bay, while Pb and Mn contributed more to the metal profiles in the bay samples. The
metal profiles in the sea turtle tissues more closely resembled the stomach contents than the same species of plants collected within
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Estero Banderitas, and suggest that sea turtles collected inside Magdalena Bay use foraging resources outside of the Estero
Banderitas region. This work supports the suggestion that metal profiles can be used as “environmentally acquired markers” to
improve our understanding of the extent of sea turtle foraging areas.
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© 2006 Elsevier B.V. All rights reserved.

Keywords: Green turtle; Chelonia mydas; Foraging; Metals; Macroalgae; Sea grass; Cadmium
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1. Introduction green turtles (Chelonia mydas) have been found to have


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exceptionally high kidney cadmium concentrations.


High concentrations of heavy metals have been Elevated Cd levels have been measured in green turtles
found in sea turtles from many regions of the world from around the world including Japan (Sakai et al.,
(Storelli and Marcotrigiano, 2003). Although metal 2000; Anan et al., 2001), China (Lam et al., 2004),
concentrations vary greatly by region and tissue type, Europe (Caurant et al., 1999), Australia (Gordon et al.,
1998) and the Arabian Sea (Bicho et al., 2006). Gordon
⁎ Corresponding author. Tel.: +52 2026476867. et al. (1998) found that Cd concentrations in green
E-mail address: gardnerscm@yahoo.com (S.C. Gardner). turtles from Australia were up to three times higher than
0048-9697/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2006.10.012
A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102 95

the levels reported in commercial seafood products. areas as previously suggested by other authors (Fran-
Recent studies of green turtles from Magdalena Bay on zellitti et al., 2004).
the Pacific coast of the Baja California Peninsula, Mex-
ico measured the highest concentration of Cd in kidney 2. Materials and methods
ever reported in any sea turtle (Gardner et al., 2006).
The Baja California Peninsula serves an important role 2.1. Study area
as foraging grounds for five of the world's seven sea turtle
species (Gardner and Nichols, 2001). Although much of Magdalena Bay is located on the Pacific coast of the

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the peninsula is considered pristine, exploitation of Baja California Peninsula, Mexico between 24° 15′ N
mineral deposits has occurred since the 19th Century and 25° 20′ N, and 111° 30′ W and 112° 15′ W. It is a
and concentrations of Cd, Zn, Cu and Pb in sediment and shallow lagoon protected from the Pacific by barrier

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marine fauna have been observed above those in more islands, with high productivity resulting from seasonal
industrialized regions (Gutiérrez-Galindo et al., 1999; marine upwelling along the coast. Diverse marine ha-
Shumilin et al., 2000). In the mid 1970's, Martin and bitats within the bay include sandy bottoms and rocky
Broenkow (1975) reported that concentrations of Cd along margins, extensive beds of the seagrass Zostera marina
the coast of the Baja California Peninsula were remarkably and a diverse assemblage of macroalgae. A sea turtle
elevated as compared to other regions of the eastern refuge area known as Estero Banderitas is located within

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Pacific. Sources of heavy metals in Baja California have the mangrove channels in the northwest region of the
been generally attributed to natural factors related to Bay where green turtles reside year-round (Fig. 1). Be-
upwelling and the biogeochemistry of the region, however, cause of the perceived importance of this area for green
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the potential contribution from anthropogenic sources (e.g. turtle foraging, its protection has been identified as a
mining and urbanization) cannot be entirely dismissed priority for conservation efforts (Arriaga et al., 1998;
(Martin and Broenkow, 1975; Sañudo-Wihelmy and Nichols et al., 2000).
Flegal, 1996; Méndez-Rodríguez et al., 1998; Gutiérrez-
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Galindo et al., 1999; Shumilin et al., 2001). 2.2. Marine plant collection
The processes controlling the concentration and
distribution of metals in coastal environments are poorly Three separate sampling trips were made in Estero
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understood. It is generally assumed that diet is the main Banderitas (November 2004, February, 2005 and April,
source of metals to sea turtles (Caurant et al., 1999; Anan 2005) in order to collect marine plants available during
et al., 2001), but little is known of the process of metal different seasons. Algae and seagrass samples were
accumulation in these species because data on metal collected along the length of the mangrove channel using
residues in most components of sea turtles' diet has been 16 transects of 30 m length. Every 6 m along the tran-
lacking. As adults, green turtles forage largely on marine sects, plants were manually collected within a 25 cm2 to
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algae and seagrasses with variation in the diet due to the 1 m2 area, depending on the density of the flora at that
relative availability of food types over geographic and location, for a total of 80 samples per trip. The samples
temporal scales (Garnett et al., 1985; Brand-Gardner were stored in labeled plastic bags and contents were
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et al., 1999; Seminoff et al., 2002). In Magdalena Bay, separated by species using taxonomic keys (Riosmena-
like other regions of the Baja California Peninsula Rodríguez, 1999). Samples were sun-dried in the field
(Seminoff et al., 2002), juvenile and adult green turtles and then pressed to further remove moisture.
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preferentially consume soft red algae, especially species


of Gracilaria (López-Mendilaharsu et al., 2005). Studies 2.3. Sea turtle tissue collection
in Baja California have demonstrated that these same
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species of red algae tend to have higher enrichment Liver and kidney tissues were collected from 8 dead
factors of metals than other groups of seaweeds green turtles that incidentally drowned in commercial
(Sánchez-Rodríguez et al., 2001), which could account fishing nets set in Magdalena Bay between February 2002
for the high accumulation of metals in foraging green and April 2003. The straight carapace length of the turtles
turtles in this region. The objective of this study was to ranged from 47–77 cm, which is representative of the size
assess the levels of metals in the diet of green turtles in range of green turtles in the region (Gardner and Nichols,
Magdalena Bay in order to better understand the sources 2001). The samples were collected within 24 h after the
of metals to turtles in this region. In addition, we explore time of death from carcasses with minimal decomposi-
how tissue metal profiles can be used as “environmen- tion. Tissue samples were stored in plastic bags and placed
tally acquired markers” to determine sea turtle feeding on ice for transport to the laboratory where they were
96 A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102

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Fig. 1. Map of Estero Banderitas located in Magdalena Bay, Baja California Sur, Mexico.
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frozen at − 80°C until analyzed. From five turtles, intact yzed were over 95%. Detection limits were: Zn = 0.0008,
stomachs were also collected. Cd = 0.0009, Mn = 0.002, Cu = 0.0025, Ni = 0.004,
Fe = 0.005, Pb = 0.006 μg/g.
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2.4. Stomach content analyses


2.6. Quantitative analyses
All stomach contents were collected and identified to
the lowest possible taxonomic level based on published Reported statistics are medians (n N 2) and ranges in μg/
keys (Abbott and Hollenberg, 1976; Riosmena-Rodrí- g on a dry weight basis. The Mann–Whitney test was used
guez, 1999). Entire sample volume and the relative sample
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volume of each plant species were calculated by the


procedure of water displacement in a graduated cylinder.
Voucher material was housed in Herbario Ficológico of
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Table 1
the Universidad Autónoma de Baja California Sur Percent volume of macroalgae and sea grasses in the stomach contents
(UABCS), La Paz, Mexico. of five green turtles (Chelonia mydas) collected in Estero Banderitas,
Magdalena Bay, Mexico
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2.5. Laboratory analyses Stomach contents


Species 1 2 3 4 5 Total
Tissue and plant samples (0.5 g) were dried in an oven
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Codium 69.1% 13.8%


at 70 °C until a dry weight was obtained. Dried samples amplivesiculatum
were digested in acid-washed Teflon tubes with concen- Gracilaria textorii 30.9% 51.6% 16.5%
trated nitric acid in a microwave oven (CEM model Mars Gracilaria 48.4% 33.6% 100% 36.4%
5X, Matthews, NC). Samples were analyzed by atomic vermiculophylla
Neoagarddhiella 36.2% 7.2%
absorption (GBC Scientific equipment, model AVANTA,
baileyi
Dandenong, Australia) using an air-acetylene flame. The Pterocladiella 20.5% 4.1%
certified standard reference material, TORT-2 (National capillacea
Research Council of Canada, Ottawa) was used to verify Ruppia maritima 43.3% 8.7%
accuracy, and that the analytical values were within the Ulva lactuca 31.8% 6.4%
Zostera marina 34.5% 6.9%
range of certified values. All recoveries of metals anal-
A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102 97

for conducting two-tailed sample comparisons of tissues 3. Results


for each metal separately and for comparing metals in
marine plants collected in Magdalena Bay with those found 3.1. Stomach contents
in the stomach contents. The Kruskal–Wallis test was used
to compare the median metal concentration across all plant Eight species of marine flora were identified within
species. The null hypothesis was rejected if p ≤ 0.05. the green turtle stomach contents (Table 1). These same
The influence of concentration differences among species were also collected from the mangrove channel of
samples was removed by converting data to the percent Estero Banderitas with the exception of Neoagarddhiella

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contribution of each metal to the total metal signature of baileyi, Pterocladiella capillacea and Ulva lactuca.
the individual sample. Fe was removed from these anal- Hypnea johnstonii, which has been previously reported
yses because of its high concentration and dominance of as a major food item in green turtle diet (López-

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the metal signature profile. Principal Components Anal- Mendilaharsu et al., 2005), was available in the bay but
ysis (PCA) of the percent contribution of the metals in not found in the stomachs of the turtles. Gracilaria
plants and tissues was conducted using the Statgraphics vermiculophylla was present in 60% of the turtle stomachs
Plus software program (Version 5, Rockville, MD). analyzed and made up the greatest total percent volume

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Table 2
Metal concentrations in plants and tissues of green turtles (Chelonia mydas) collected in Magdalena Bay, Mexico
Metal
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Cd Pb Ni Mn Fe Zn Cu
Bay
Codium amplivesiculatum 0.01 0.80 7.29 20.40 350 8.75 0.98
(n = 7) (nd–1.94) (nd–2.29) (6.02–9.98) (12.05–63.54) (189–523) (2.17–18.20) (nd–7.31)
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Gracilaria textorii 3.65 0.83 4.94 46.92 401 12.31 1.34


(n = 8) (nd–4.80) (nd–1.95) (3.01–7.59) (37.63–54.84) (81.8–1231) (6.04–58.77) (0.41–4.77)
Gracilaria vermiculophylla 1.40 0.84 4.26 19.33 236 9.59 0.99
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(n = 9) (0.54–2.88) (nd–3.34) (1.13–5.54) (14.35–23.87) (139–771) (5.68–11.71) (0.33–1.62)


Hypnea johnstonii 0.38 1.11 6.66 26.73 568 4.13 1.82
(n = 5) nd–2.74) (nd–8.54) (1.76–11.34) (20.64–283) (227.84–1424) (2.01–17.19) (nd–4.36)
Ruppia maritima 4.52 2.12 2.29 30.60 1230 16.93 0.45
(n = 2) (2.09–6.95) (0.46–3.79) (1.70–2.88) (28.56–32.63) (1017–1443) (8.93–24.93) (0.00–0.91)
Zostera marina 1.09 1.23 2.94 56.25 341 15.04 0.98
(n = 2) (nd–2.18) (0.02–2.45) (2.75–3.13) (33.91–78.59) (51.06–630) (13.53–16.54) (0.36–1.61)
Stomach contents
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Codium amplivesiculatum 2.49 0.01 0.90 12.73 173 8.82 0.79


(n = 1)
Gracilaria textorii 6.31 nd 2.66 11.89 49.43 11.19 0.69
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(n = 2) (5.09–7.52) (2.64–2.68) (10.69–13.08) (42.08–56.78) (10.10–12.27) (0.02–1.36)


Gracilaria vermiculophylla 5.79 0.00 2.77 6.25 40.54 13.80 1.11
(n = 3) (2.22–6.29) (nd–0.02) (1.68–7.09) (4.02–11.78) (31.81–107) (9.46–21.45) (1.01–1.21)
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Neoagarddhiella baileyi 10.19 0.04 4.71 7.16 317 23.11 4.67


(n = 1)
Pterocladiella capillacea 6.93 0.11 9.44 5.74 131 19.72 1.02
(n = 1)
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Ruppia maritima 11.11 0.12 9.67 10.55 209 60.96 5.70


(n = 1)
Ulva lactuca 4.42 0.07 6.93 5.43 93.37 41.32 2.12
(n = 1)
Zostera marina 4.69 0.07 3.03 7.92 97.80 38.67 0.49
(n = 1)
Green turtle tissues
Kidney 110 0.05 3.19 1.51 93.16 189 5.83
(n = 8) (65.08–653) (nd–1.74) (1.19–25.13) (nd–7.73) (nd–547) (102–281) (1.98–11.6)
Liver 16.92 0.00 0.00 0.24 350 90.95 76.52
(n = 8) (nd–72.57) (nd–0.07) (nd–30.88) (nd–5.31) (nd–671) (41.81–109) (6.79–128)
Data are expressed as medians (μg/g dry weight) with ranges given in parenthesis. nd signifies not detected.
98 A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102

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Fig. 2. Percent contribution of metals in species of marine flora collected in Magdalena Bay and in green turtle stomach contents. a) G.
vermiculophylla, b) G. textorii, c) C. amplivesiculatum, d) R. maritima y e) Z. marina.

(36%). Gracilaria textorii was present in the second cantly different from the stomach contents. Sea turtle
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greatest percent volume (16.5%). kidney Cd concentration was significantly higher than
liver ( p = 0.002), while Zn was the same in both tissues.
3.2. Comparison of metals in plant species
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In comparisons of the metal concentrations between


plant species, the only significant differences were detected
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for Cd ( p = 0.009). Cd concentration in Ruppia maritima


was higher than all other species. Gracilaria textorii had
higher Cd concentrations than Codium amplivesiculatum
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(Table 2).

3.3. Metals in sea turtle tissues, stomach contents, and


plants from the bay

Concentrations of Cd and Zn in flora from the sea


turtle stomach contents were greater than the same
species of marine plants collected in the bay ( p b 0.001
and p = 0.003, respectively) (Table 2). For both metals, Fig. 3. Percent contribution of metals in tissues and stomach contents
the concentrations in sea turtle liver were not signifi- of green turtles from Magdalena Bay, Mexico.
A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102 99

Pb, Mn and Fe in flora from the stomach contents significantly different in Fe. There were no differences
were significantly lower than in flora collected from the in the concentrations of these metals in liver and kidney.
bay ( p b 0.001 for each) (Table 2). The stomach contents Ni and Cu concentrations did not differ in plants from
had higher Pb and Mn concentrations than liver the two sources. Ni concentration in liver was similar to
( p = 0.04 and p b 0.001, respectively) but were not kidney concentrations, but significantly lower than the
stomach contents ( p = 0.005). Cu was higher in liver than
stomach contents ( p b 0.001) and higher than kidney
( p b 0.001).

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These same trends persisted when the data were
transformed to the percent contribution of the metals in
each plant species in the stomach contents as compared

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to the bay samples (Fig. 2). For each of the five plant
species, the percent contribution of Mn and Pb was
greater in the bay-collected plants, while Cd and Zn
consistently contributed more to the total metal profile
in plants from the stomach contents. Fig. 3 shows the
percent contribution of each metal in paired samples of

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liver, kidney and stomach contents (all flora combined)
from the same turtles. Cd and Zn contributed most
to the overall metal profile in the kidney, while Cu
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contributed more in liver. The percent contribution of
Mn and Ni were greatest in the plants from the stomach
contents.
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3.4. Principle components analysis

Principal components analysis (PCA) of the percent


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contribution of individual metals to the overall metal


signature of each plant or tissue sample generated three
principal components (PC) that explained 80.7% of the
total variance in the data (50.1%, 17.6%, and 13.1%,
respectively) (Fig. 4). Plots of the sample scores on the
first and second principal components produced four
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groupings. Bay and stomach plant samples were separated


by their scores on PC(1), while kidney and liver samples
were separated by their scores on PC(2) (Fig. 4A). All but
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one of the bay plant samples obtained negative scores on


PC(1), whereas plants from the stomach contents gen-
erally scored greater than 0. The loadings plot, which
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illustrates the influence of each metal on sample scores,


indicated that the bay and stomach samples separated on
PC(1) based on the dominance of the stomach samples'
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metal signatures by Zn and Cd. The separation of liver and


kidney samples appeared to be influenced by the greater
contribution of Cd to the metal profile in kidney, and the
dominance of Cu in liver samples which scored higher on
PC(2) (Fig. 4B).

4. Discussion
Fig. 4. A) Plot of sample scores of a Principle Component Analysis of
the percent contribution of individual metals to the overall signature of
marine flora from Magdalena Bay, and kidney, liver and stomach Much of the literature on sea turtles has worked with
content samples from green turtles. B) Loadings plot. absolute concentrations of metals, which is appropriate
100 A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102

for comparisons of very similar sample types such as the overall diet (8.7%) in this study, and was absent
different sea turtle tissues or the same tissue in different from the diet of 24 green turtles analyzed in previous
sea turtle species. In the present paper we used absolute work (López-Mendilaharsu et al., 2005). Gracilaria
concentrations to compare metals in tissues (kidney vs. textorii made up a larger proportion of the turtles'
liver) and to compare metal concentrations in different stomach contents (16.5%), but was similar in Cd con-
plant species. However in order to better understand the centration to most other plant species ingested by the
sources of metals to turtles in this region, the profile of all green turtles. The results of the PCA also support
metals combined was used as an environmentally ac- this conclusion since the bay-collected plant samples

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quired marker. For this objective, we removed the grouped separately from the samples in the stomach
influence of concentration differences among samples contents despite that both groups consisted of the same
by converting the data to percent contribution of each five plant species.

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metal to the total metal signature of the individual sample.
This approach enabled the comparison of metal profiles 4.2. Sea turtle tissue comparisons
across greatly different samples and was more appropriate
than comparisons of absolute concentrations alone. For Pb, Cu and Mn concentrations in tissue from this
example, a single plant species located in two different study were within the range of those reported for sea
areas will accumulate metals using the same physiological turtles in other parts of the world (Lam et al., 2004;

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mechanisms. Therefore, a difference in metal profiles of Storelli and Marcotrigiano, 2003). However, the average
the plant species from two different locations is an indi- concentrations of Cd, Zn and Ni in kidney of green
cation of differences in the availability of the metals from turtles from Magdalena Bay were high compared to
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the environment. However, differences in the absolute previously reports for sea turtle tissues (Sakai et al.,
concentrations of metals in plants would not necessarily 1995, 2000; Storelli and Marcotrigiano, 2003). Studies
indicate environmental difference because other factors of loggerhead turtles (Maffucci et al., 2005) suggest that
might also be at play (e.g. age of the plant). sea turtles can regulate Cu and Zn concentrations
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through homeostatic processes but that Cd uptake is not


4.1. Comparison of metals in marine plant species controlled by active process and thus tissue concentra-
tions of this metal reflect exposure. In agreement with
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Metal concentrations in marine flora are controlled these findings, we observed that Cd concentrations in
by both the bioavailability of metals in the surrounding green turtle liver were similar to their food and that the
water and the uptake capacity of the particular plant Cu concentration in sea turtle liver was greater than in
species. Marine algae have the capacity to accumulate the stomach content. Similar relationships have been
trace metals several thousand times higher than the observed in green turtles from Japan (Anan et al., 2001).
concentration in seawater (Bryan and Langston, 1992; However, contrary to the findings of Maffucci et al.
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Sánchez-Rodríguez et al., 2001). Red algae, such as (2005), Zn concentrations in the livers and kidneys of
Gracilaria sp tend to reflect the environmental avail- green turtles in our study were not significantly different
ability of metals but have higher bioaccumulation of Cd, from their stomach contents.
or

Cu and Zn than other macroalgal groups (Sánchez- The distribution of metals among organs is influenced
Rodríguez et al., 2001; Roncarati, 2003). These same by both duration and concentration of exposure. Liver is
species are a major component of the green turtle diet a major site of short-term Cd storage, whereas during
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along the Baja California Peninsula (Seminoff et al., long-term exposure, Cd is redistributed from the liver to
2002; López-Mendilaharsu et al., 2005), and we the kidney where it is absorbed and concentrated
proposed previously (Gardner et al., 2006) that their (Thomas et al., 1994; Linder and Grillitsch, 2000; Rie
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foraging habits could account for the high metal con- et al., 2001). Therefore a significantly greater concen-
centrations found in this population. However, compar- tration of Cd in green turtle kidney than liver is often
isons across plant species in the present study suggest observed (Storelli and Marcotrigiano, 2003; Maffucci
that species differences in metal concentrations are et al., 2005; Gardner et al., 2006) and likely results from
minimal. The only significant difference detected be- years of accumulation in this long-lived species. While
tween plant species was that Cd was higher in Ruppia kidney Cd concentration may serve as a good indicator
maritima than all other species, and higher in Gracilaria for assessments of sea turtle health, liver more closely
textorii than Codium amplivesiculatum. R. maritima reflects the concentration of this metal in the food and so
was encountered in only one of the sea turtle stomachs analyses of liver may provide a better indication of recent
analyzed, contributing a relatively small percentage of environmental exposure. Accordingly, Cd concentrations
A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102 101

in the livers analyzed in the present study were not ronment. Surface water metal concentrations have been
different from the food in the sea turtles' stomachs. strongly correlated with upwelling events and natural
Concentrations of Fe and Zn in liver were also similar to components of regional biogeochemistry (Daesslé et al.,
the stomach contents. Whereas, Pb, Ni and Mn 2000; Lares et al., 2002). Similar to the distribution of
concentrations in liver were similar to kidney, but were nutrients in the water column, metals such as Cd and Zn
lower than in the stomach contents, which may indicate are depleted in the surface and enriched in deeper water.
metabolic processing of these metals. Alternatively, Cu Upwelling processes are an important mechanism that
concentration was higher in liver than in the turtles' food brings elevated concentrations of both nutrients and

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and appeared to be preferentially accumulated in liver metals to the surface and thus available for marine floral
over kidney. accumulation. Therefore it is highly probable that the sea
turtles collected within Magdalena Bay are utilizing

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4.3. Metals in sea turtle stomach contents and marine foraging areas in an upwelling-rich coastal region outside
plants from the bay of the Bay.
Coastal lagoons of the Baja California Peninsula
Two principle components, PC(1) and PC(2), explained such as Magdalena Bay have been identified as priority
68% of the total variance in the data. When plotted relative areas for sea turtle conservation programs (Nichols
to PC(1) and PC(2), the plant samples collected in the bay et al., 2000). Long-term sea turtle monitoring studies

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formed a grouping at the left side of the plot while the have demonstrated high site fidelity to Estero Banderitas
green turtle tissue samples and the plants from the stomach over time, and low emigration of sea turtles from Mag-
contents plotted higher on PC(1) (Fig. 4A). Examination of dalena Bay to other coastal lagoons along the Baja
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the loadings plot for each of the metals confirmed that California Peninsula (Grupo Tortuguero, unpublished
samples scoring high on PC1 had signatures dominated by data). Efforts to protect areas within Magdalena Bay
Cd and Zn (stomach contents and kidney) or Cu (liver) have focused on the creation of a refuge in the mangrove
(Fig. 4B). This agrees with the observation that the plants channels of Estero Banderitas, in part, because of the
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in the stomach contents contained greater percent perceived importance of this habitat for sea turtle
contributions of Cd and Zn than the samples collected in foraging (Nichols and Arcas, 2001). However, data
the bay, while Pb and Mn contributed more to the metal generated by our work suggest that sea turtles residing in
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profiles in the bay samples as shown in Fig. 2; a tendency Estero Banderitas are feeding in areas outside of the bay,
that was consistent in all five plant species. most likely in coastal regions with high upwelling.
The metal profiles in the sea turtle tissues more These findings support those of López-Mendilaharsu
closely resembled the plants in the stomach contents et al. (2005) and indicate that green turtles utilize
than the same species of plants collected within Estero spatially distinct feeding habitats within coastal areas.
Banderitas. The fact that the concentrations of Cd, Fe Therefore, we recommend that sea turtle protected
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and Zn in green turtle liver were the same as the stomach areas be designed with an appreciation of regional rather
contents but different from the plants collected in the than local scales in order to protect broader foraging
bay suggests that sea turtles collected inside of Mag- areas.
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dalena Bay use foraging resources outside of the Estero


Banderitas region. Further support of this conclusion is Acknowledgements
provided by the fact that three algal species (N. baileyi,
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P. capillacea and U. lactuca) in the stomach contents Funding for this project was provided by a grant to
were not found in Estero Banderitas. SC Gardner from the Consejo Nacional de Ciencia y
Franzellitti et al. (2004) proposed that tissue metal Tecnología (Conacyt, SEP-2004-CO1-45749) and the
Au

profiles can be used as “environmentally acquired mark- Centro de Investigaciones Biológicas del Noroeste, S.C.
ers” to determine sea turtle feeding areas. Similarly, prin- (CIBNOR). The authors express their appreciation to
ciple component analyses have been applied previously to Dr. Wallace J. Nichols, Rodrigo Rangel and the Grupo
determine sources of metals in aquatic environments Tortuguero for their assistance in this project. We also
(Ruiz-Fernández et al., 2001). Comparison of the metal appreciate the expertise of Dr. Samuel Chávez Rosales
signature profiles in plants from the bay and the sea turtle and Griselda Peña Armenta for their help with the
stomach contents indicate that the plant species contained quantitative analyses. This research was conducted in
inside the sea turtle stomachs originated from a location accordance with Mexican laws and regulations, under
outside of Estero Banderitas, in an area where Cd and Zn permits provided by the Secretaria de Medio Ambiente
concentrations dominate the metal profiles in the envi- y Recursos Naturales (SGPA/DGVS/002-2895).
102 A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94–102

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