Talavera et al 2007

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p yMetal profiles used as environmental markers of Green Turtle

(Chelonia mydas ) foraging resources

Ana Talavera-Saenz a,b , Susan C. Gardner a, ,Rafael Riosmena Rodriquez b , Baudilio Acosta Vargas a

a Centro de Investigaciones Biolgicas 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 Investigacin en Botnica Marina, Departamento de Biologa Marina, Universidad Autnoma de Baja California Sur. La Paz, Baja California Sur 23080 Mexico

Received 12 June 2006; received in revised form 8 October 2006; accepted 9 October 2006Available online 22 December 2006

Abstract

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 theregion. 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 between marine plant species were minimal. Principal components analysis of the percent contribution of individual metals to theoverall metal signature of each plant or tissue sample generated three principal components that explained 80.7% of the totalvariance in the data. The plant samples collected within Estero Banderitas formed a separate grouping from the green turtle tissuesamples and the plants from the stomach contents. The plants in the stomach contents contained greater percent contributions of Cdand Zn than the plants collected inside the bay, while Pb and Mn contributed more to the metal profiles in the bay samples. Themetal profiles in the sea turtle tissues more closely resembled the stomach contents than the same species of plants collected withinEstero Banderitas, and suggest that sea turtles collected inside Magdalena Bay use foraging resources outside of the EsteroBanderitas region. This work supports the suggestion that metal profiles can be used as environmentally acquired markers toimprove our understanding of the extent of sea turtle foraging areas. 2006 Elsevier B.V. All rights reserved.

Keywords: Green turtle; Chelonia mydas ; Foraging; Metals; Macroalgae; Sea grass; Cadmium

1. Introduction

High concentrations of heavy metals have beenfound in sea turtles from many regions of the world(Storelli and Marcotrigiano, 2003 ). Although metalconcentrations vary greatly by region and tissue type,

green turtles ( Chelonia mydas ) have been found to haveexceptionally high kidney cadmium concentrations.Elevated Cd levels have been measured in green turtlesfrom around the world including Japan ( Sakai et al.,2000; Anan et al., 2001 ), China (Lam et al., 2004 ),Europe ( Caurant et al., 1999 ), Australia ( Gordon et al.,1998 ) and the Arabian Sea ( Bicho et al., 2006 ). Gordonet al. (1998) found that Cd concentrations in greenturtles from Australia were up to three times higher than

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

Corresponding author. Tel.: +52 2026476867. E-mail address: [email protected] (S.C. Gardner).

0048-9697/$ - see front matter 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.scitotenv.2006.10.012


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the levels reported in commercial seafood products.Recent studies of green turtles from Magdalena Bay onthe Pacific coast of the Baja California Peninsula, Mex-ico measured the highest concentration of Cd in kidneyever reported in any sea turtle ( Gardner et al., 2006 ).

The Baja California Peninsula serves an important roleas foraging grounds for five of the world's seven sea turtlespecies (Gardner and Nichols, 2001 ). Although much of the peninsula is considered pristine, exploitation of mineral deposits has occurred since the 19th Centuryand concentrations of Cd, Zn, Cu and Pb in sediment andmarine fauna have been observed above those in moreindustrialized regions ( Gutirrez-Galindo et al., 1999;Shumilin et al., 2000 ). In the mid 1970's, Martin andBroenkow (1975) reported that concentrationsof Cd along

thecoast of theBaja CaliforniaPeninsula were remarkablyelevated as compared to other regions of the easternPacific. Sources of heavy metals in Baja California have been generally attributed to natural factors related toupwelling and the biogeochemistry of the region,however,the potential contribution fromanthropogenic sources( e.g.mining and urbanization) cannot be entirely dismissed(Martin and Broenkow, 1975; Saudo-Wihelmy andFlegal, 1996; Mndez-Rodrguez et al., 1998; Gutirrez-Galindo et al., 1999; Shumilin et al., 2001 ).

The processes controlling the concentration anddistribution of metals in coastal environments are poorlyunderstood. It is generally assumed that diet is the mainsource of metals to sea turtles ( Caurant et al., 1999; Ananet al., 2001 ), but little is known of the process of metalaccumulation in these species because data on metalresidues in most components of sea turtles' diet has beenlacking. As adults, green turtles forage largely on marinealgae and seagrasses with variation in the diet due to therelative availability of food types over geographic andtemporal scales ( Garnett et al., 1985; Brand-Gardner et al., 1999; Seminoff et al., 2002 ). In Magdalena Bay,like other regions of the Baja California Peninsula

(Seminoff et al., 2002 ), juvenile and adult green turtles preferentially consume soft red algae, especially speciesof Gracilaria (Lpez-Mendilaharsu et al., 2005 ). Studiesin Baja California have demonstrated that these samespecies of red algae tend to have higher enrichment factors of metals than other groups of seaweeds(Snchez-Rodrguez et al., 2001 ), which could account for the high accumulation of metals in foraging greenturtles in this region. The objective of this study was toassess the levels of metals in the diet of green turtles inMagdalena Bay in order to better understand the sources

of metals to turtles in this region. In addition, we explorehow tissue metal profiles can be used as environmen-tally acquired markers to determine sea turtle feeding

areas as previously suggested by other authors ( Fran-zellitti et al., 2004 ).

2. Materials and methods

2.1. Study area

Magdalena Bay is located on the Pacific coast of theBaja California Peninsula, Mexico between 24 15 Nand 25 20 N, and 111 30 W and 112 15 W. It is ashallow lagoon protected from the Pacific by barrier islands, with high productivity resulting from seasonalmarine upwelling along the coast. Diverse marine habitats within the bay include sandy bottoms and rockymargins, extensive beds of the seagrass Zostera marina

and a diverse assemblage of macroalgae. A sea turtlerefuge area known as Estero Banderitas is located withinthe mangrove channels in the northwest region of theBay where green turtles reside year-round ( Fig. 1). Be-cause of the perceived importance of this area for greenturtle foraging, its protection has been identified as a priority for conservation efforts ( Arriaga et al., 1998; Nichols et al., 2000 ).

2.2. Marine plant collection

Three separate sampling trips were made in EsteroBanderitas (November 2004, February, 2005 and April,2005) in order to collect marine plants available duringdifferent seasons. Algae and seagrass samples werecollected along the length of the mangrove channel using16 transects of 30 m length. Every 6 m along the tran-sects, plants were manually collected within a 25 cm 2 to1 m2 area, depending on the density of the flora at that location, for a total of 80 samples per trip. The sampleswere stored in labeled plastic bags and contents wereseparated by species using taxonomic keys ( Riosmena-Rodrguez, 1999 ). Samples were sun-dried in the field

and then pressed to further remove moisture.

2.3. Sea turtle tissue collection

Liver and kidney tissues were collected from 8 deadgreen turtles that incidentally drowned in commercialfishing nets set in Magdalena Bay between February 2002and April 2003. The straight carapace length of the turtlesranged from 47 77 cm, which is representative of the sizerange of green turtles in the region ( Gardner and Nichols,2001). The samples were collected within 24 h after the

time of death from carcasses with minimal decomposi-tion. Tissue samples were storedin plastic bags andplacedon ice for transport to the laboratory where they were

95 A. Talavera-Saenz et al. / Science of the Total Environment 373 (2007) 94 102


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frozen at 80C until analyzed. From five turtles, intact stomachs were also collected.

2.4. Stomach content analyses

All stomach contents were collected and identified tothe lowest possible taxonomic level based on publishedkeys (Abbott and Hollenberg, 1976; Riosmena-Rodr-guez, 1999 ). Entire sample volume and the relativesamplevolume of each plant species were calculated by the procedure of water displacement in a graduated cylinder.Voucher material was housed in Herbario Ficolgico of the Universidad Autnoma de Baja California Sur (UABCS), La Paz, Mexico.

2.5. Laboratory analyses

Tissue and plant samples (0.5 g) were dried in an ovenat 70 C until a dry weight was obtained. Dried sampleswere digested in acid-washed Teflon tubes with concen-trated nitric acid in a microwave oven (CEM model Mars5X, Matthews, NC). Samples were analyzed by atomicabsorption (GBC Scientific equipment, model AVANTA,Dandenong, Australia) using an air-acetylene flame. Thecertified standard reference material, TORT-2 (National

Research Council of Canada, Ottawa) was used to verifyaccuracy, and that the analytical values were within therange of certified values. All recoveries of metals anal-

yzed were over 95%. Detection limits were: Zn=0.0008,Cd= 0.0009, Mn= 0.002, Cu= 0.0025, Ni= 0.004,Fe=0.005, Pb=0.006 g/g.

2.6. Quantitative analyses

Reported statistics are medians ( n N 2) and ranges in g/ g on a dry weight basis. The Mann Whitney test was used

Fig. 1. Map of Estero Banderitas located in Magdalena Bay, Baja California Sur, Mexico.

Table 1Percent volume of macroalgae and sea grasses in the stomach contentsof five green turtles ( Chelonia mydas ) collected in Estero Banderitas,

Magdalena Bay, MexicoStomach contents

Species 1 2 3 4 5 Total

Codiumamplivesiculatum

69.1% 13.8%

Gracilaria textorii 30.9% 51.6% 16.5%Gracilaria

vermiculophylla48.4% 33.6% 100% 36.4%

Neoagarddhiellabaileyi

36.2% 7.2%

Pterocladiellacapillacea

20.5% 4.1%

Ruppia maritima 43.3% 8.7%Ulva lactuca 31.8% 6.4% Zostera marina 34.5% 6.9%



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for conducting two-tailed sample comparisons of tissuesfor each metal separately and for comparing metals inmarine plantscollected in MagdalenaBaywith those foundin the stomach contents. The Kruskal Wallis test was usedto compare the median metal concentration across all plant species. The null hypothesis was rejected if p 0.05.

The influence of concentration differences amongsamples was removed by converting data to the percent contribution of each metal to the total metal signature of the individual sample. Fe was removed from these anal-yses because of its high concentration and dominance of the metal signature profile. Principal Components Anal-ysis (PCA) of the percent contribution of the metals in plants and tissues was conducted using the StatgraphicsPlus software program (Version 5, Rockville, MD).

3. Results

3.1. Stomach contents

Eight species of marine flora were identified withinthe green turtle stomach contents ( Table 1 ). These samespecies were also collected from the mangrove channel of Estero Banderitas with the exception of Neoagarddhiellabaileyi , Pterocladiella capillacea and Ulva lactuca . Hypnea johnstonii , which has been previously reportedas a major food item in green turtle diet ( Lpez-Mendilaharsu et al., 2005 ), was available in the bay but not found in the stomachs of the turtles. Gracilariavermiculophylla waspresent in 60%of the turtle stomachsanalyzed and made up the greatest total percent volume

Table 2Metal concentrations in plants and tissues of green turtles ( Chelonia mydas ) collected in Magdalena Bay, Mexico

Metal

Cd Pb Ni Mn Fe Zn Cu

BayCodium 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)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

(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 contentsCodium 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(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) 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) 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 tissuesKidney 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 ( g/g dry weight) with ranges given in parenthesis. nd signifies not detected.



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(36%). Gracilaria textorii was present in the secondgreatest percent volume (16.5%).

3.2. Comparison of metals in plant species

In comparisons of the metal concentrations between

plant species, theonlysignificant differences were detectedfor Cd ( p=0.009). Cd concentration in Ruppia maritimawas higher than all other species. Gracilaria textorii hadhigher Cd concentrations than Codium amplivesiculatum(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 seaturtle stomach contents were greater than the same

species of marine plants collected in the bay ( pb

0.001and p =0.003, respectively) ( Table 2 ). For both metals,the concentrations in sea turtle liver were not signifi-

cantly different from the stomach contents. Sea turtlekidney Cd concentration was significantly higher thanliver ( p = 0.002), while Zn was the same in both tissues.

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 .

Fig. 3. Percent contribution of metals in tissues and stomach contentsof green turtles from Magdalena Bay, Mexico.



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Pb, Mn and Fe in flora from the stomach contentswere significantly lower than in flora collected from the bay ( p b 0.001 for each) ( Table 2 ). The stomach contentshad higher Pb and Mn concentrations than liver ( p = 0.04 and p b 0.001, respectively) but were not

significantly different in Fe. There were no differencesin the concentrations of these metals in liver and kidney.

Ni and Cu concentrations did not differ in plants fromthe two sources. Ni concentration in liver was similar tokidney concentrations, but significantly lower than thestomach contents ( p = 0.005). Cu was higher in liver thanstomach contents ( p b 0.001) and higher than kidney( p b 0.001).

These same trends persisted when the data weretransformed to the percent contribution of the metals ineach plant species in the stomach contents as comparedto the bay samples ( Fig. 2). For each of the five plant species, the percent contribution of Mn and Pb wasgreater in the bay-collected plants, while Cd and Znconsistently 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 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 Cucontributed more in liver. The percent contribution of Mn and Ni were greatest in the plants from the stomachcontents.

3.4. Principle components analysis

Principal components analysis (PCA) of the percent contribution of individual metals to the overall metalsignature of each plant or tissue sample generated three principal components (PC) that explained 80.7% of thetotal variance in the data (50.1%, 17.6%, and 13.1%,respectively) ( Fig. 4). Plots of the sample scores on thefirst and second principal components produced four groupings. Bay andstomach plant samples were separated by their scores on PC(1), while kidney and liver sampleswere separated by their scores on PC(2) ( Fig. 4A). All but one of the bay plant samples obtained negative scores onPC(1), whereas plants from the stomach contents gen-

erally scored greater than 0. The loadings plot, whichillustrates the influence of each metal on sample scores,indicated that the bay and stomach samples separated onPC(1) based on the dominance of the stomach samples'metal signatures by Zn and Cd. The separation of liver andkidney samples appeared to be influenced by the greater contribution of Cd to the metal profile in kidney, and thedominance of Cu in liver samples which scored higher onPC(2) (Fig. 4B).

4. Discussion

Much of the literature on sea turtles has worked withabsolute concentrations of metals, which is appropriate

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 stomachcontent samples from green turtles. B) Loadings plot.



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for comparisons of very similar sample types such asdifferent sea turtle tissues or the same tissue in different sea turtle species. In the present paper we used absoluteconcentrations to compare metals in tissues (kidney vs.liver) and to compare metal concentrations in different plant species. However in order to better understand thesources of metals to turtles in this region, the profile of allmetals combined was used as an environmentally ac-quired marker. For this objective, we removed theinfluence of concentration differences among samples by converting the data to percent contribution of eachmetal to the total metal signature of the individual sample.This approach enabled the comparison of metal profilesacrossgreatly different samples and was more appropriatethan comparisons of absolute concentrations alone. For

example, a single plant species located in two different areaswill accumulate metals using thesame physiologicalmechanisms. Therefore, a difference in metal profiles of the plant species from two different locations is an indi-cation of differences in the availability of the metals fromthe environment. However, differences in the absoluteconcentrations of metals in plants would not necessarilyindicate environmental difference because other factorsmight also be at play (e.g. age of the plant).

4.1. Comparison of metals in marine plant species

Metal concentrations in marine flora are controlled by both the bioavailability of metals in the surroundingwater and the uptake capacity of the particular plant species. Marine algae have the capacity to accumulatetrace metals several thousand times higher than theconcentration in seawater ( Bryan and Langston, 1992;Snchez-Rodrguez et al., 2001 ). Red algae, such asGracilaria sp tend to reflect the environmental avail-ability of metals but have higher bioaccumulation of Cd,Cu and Zn than other macroalgal groups ( Snchez-Rodrguez et al., 2001; Roncarati, 2003 ). These same

species are a major component of the green turtle diet along the Baja California Peninsula ( Seminoff et al.,2002; Lpez-Mendilaharsu et al., 2005 ), and we proposed previously ( Gardner et al., 2006 ) that their foraging habits could account for the high metal con-centrations found in this population. However, compar-isons across plant species in the present study suggest that species differences in metal concentrations areminimal. The only significant difference detected be-tween plant species was that Cd was higher in Ruppiamaritima than all other species, and higher in Gracilaria

textorii than Codium amplivesiculatum . R. maritimawas encountered in only one of the sea turtle stomachsanalyzed, contributing a relatively small percentage of

the overall diet (8.7%) in this study, and was absent from the diet of 24 green turtles analyzed in previouswork (Lpez-Mendilaharsu et al., 2005 ). Gracilariatextorii made up a larger proportion of the turtles'stomach contents (16.5%), but was similar in Cd con-centration to most other plant species ingested by thegreen turtles. The results of the PCA also support this conclusion since the bay-collected plant samplesgrouped separately from the samples in the stomachcontents despite that both groups consisted of the samefive plant species.

4.2. Sea turtle tissue comparisons

Pb, Cu and Mn concentrations in tissue from this

study were within the range of those reported for seaturtles in other parts of the world ( Lam et al., 2004;Storelli and Marcotrigiano, 2003 ). However, the averageconcentrations of Cd, Zn and Ni in kidney of greenturtles from Magdalena Bay were high compared to previously reports for sea turtle tissues ( Sakai et al.,1995, 2000; Storelli and Marcotrigiano, 2003 ). Studiesof loggerhead turtles ( Maffucci et al., 2005 ) suggest that sea turtles can regulate Cu and Zn concentrationsthrough homeostatic processes but that Cd uptake is not controlled by active process and thus tissue concentra-tions of this metal reflect exposure. In agreement withthese findings, we observed that Cd concentrations ingreen turtle liver were similar to their food and that theCu concentration in sea turtle liver was greater than inthe stomach content. Similar relationships have beenobserved in green turtles from Japan ( Anan et al., 2001 ).However, contrary to the findings of Maffucci et al.(2005) , Zn concentrations in the livers and kidneys of green turtles in our study were not significantly different from their stomach contents.

The distribution of metals among organs is influenced by both duration and concentration of exposure. Liver is

a major site of short-term Cd storage, whereas duringlong-term exposure, Cd is redistributed from the liver tothe kidney where it is absorbed and concentrated(Thomas et al., 1994; Linder and Grillitsch, 2000; Rieet al., 2001 ). Therefore a significantly greater concen-tration of Cd in green turtle kidney than liver is oftenobserved ( Storelli and Marcotrigiano, 2003; Maffucciet al., 2005; Gardner et al., 2006 ) and likely results fromyears of accumulation in this long-lived species. Whilekidney Cd concentration may serve as a good indicator for assessments of sea turtle health, liver more closely

reflects the concentration of this metal in the food and soanalyses of liver may provide a better indication of recent environmental exposure. Accordingly, Cd concentrations



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in the livers analyzed in the present study were not different from the food in the sea turtles' stomachs.Concentrations of Fe and Zn in liver were also similar tothe stomach contents. Whereas, Pb, Ni and Mnconcentrations in liver were similar to kidney, but werelower than in the stomach contents, which may indicatemetabolic processing of these metals. Alternatively, Cuconcentration was higher in liver than in the turtles' foodand appeared to be preferentially accumulated in liver over kidney.

4.3. Metals in sea turtle stomach contents and marine plants from the bay

Two principle components, PC(1) andPC(2), explained

68% of the total variance in thedata. When plotted relativeto PC(1) and PC(2), the plant samples collected in the bayformed a grouping at the left side of the plot while thegreen turtle tissue samples and the plants from the stomachcontents plotted higher on PC(1) ( Fig.4A).Examination of the loadings plot for each of the metals confirmed that samplesscoring high on PC1 had signatures dominated byCd and Zn (stomach contents and kidney) or Cu (liver)(Fig. 4B). This agrees with the observation that the plantsin the stomach contents contained greater percent contributions of Cd and Zn than the samples collected inthe bay, while Pb and Mn contributed more to the metal profiles in the bay samples as shown in Fig. 2; a tendencythat was consistent in all five plant species.

The metal profiles in the sea turtle tissues moreclosely resembled the plants in the stomach contentsthan the same species of plants collected within EsteroBanderitas. The fact that the concentrations of Cd, Feand Zn in green turtle liver were the same as the stomachcontents but different from the plants collected in the bay suggests that sea turtles collected inside of Mag-dalena Bay use foraging resources outside of the EsteroBanderitas region. Further support of this conclusion is

provided by the fact that three algal species ( N. baileyi, P. capillacea and U. lactuca ) in the stomach contentswere not found in Estero Banderitas.

Franzellitti et al. (2004) proposed that tissue metal profiles can be used as environmentally acquired mark-ers to determine sea turtle feeding areas. Similarly, prin-ciple component analyses have been applied previously todetermine sources of metals in aquatic environments(Ruiz-Fernndez et al., 2001 ). Comparison of the metalsignature profiles in plants from the bay and the sea turtlestomach contents indicate that the plant species contained

inside the sea turtle stomachs originated from a locationoutside of Estero Banderitas, in an area where Cd and Znconcentrations dominate the metal profiles in the envi-

ronment. Surface water metal concentrations have beenstrongly correlated with upwelling events and naturalcomponents of regional biogeochemistry ( Daessl et al.,2000; Lares et al., 2002 ). Similar to the distribution of nutrients in the water column, metals such as Cd and Znare depleted in the surface and enriched in deeper water.Upwelling processes are an important mechanism that brings elevated concentrations of both nutrients andmetals to the surface and thus available for marine floralaccumulation. Therefore it is highly probable that the seaturtles collected within Magdalena Bay are utilizingforaging areas in an upwelling-rich coastal region outsideof the Bay.

Coastal lagoons of the Baja California Peninsulasuch as Magdalena Bay have been identified as priority

areas for sea turtle conservation programs ( Nicholset al., 2000 ). Long-term sea turtle monitoring studieshave demonstrated high site fidelity to Estero Banderitasover time, and low emigration of sea turtles from Mag-dalena Bay to other coastal lagoons along the BajaCalifornia Peninsula (Grupo Tortuguero, unpublisheddata). Efforts to protect areas within Magdalena Bayhave focused on the creation of a refuge in the mangrovechannels of Estero Banderitas, in part, because of the perceived importance of this habitat for sea turtleforaging ( Nichols and Arcas, 2001 ). However, datagenerated by our work suggest that sea turtles residing inEstero Banderitas are feeding in areas outside of the bay,most likely in coastal regions with high upwelling.These findings support those of Lpez-Mendilaharsuet al. (2005) and indicate that green turtles utilizespatially distinct feeding habitats within coastal areas.Therefore, we recommend that sea turtle protectedareas be designed with an appreciation of regional rather than local scales in order to protect broader foragingareas.

Acknowledgements

Funding for this project was provided by a grant toSC Gardner from the Consejo Nacional de Ciencia yTecnologa (Conacyt, SEP-2004-CO1-45749) and theCentro de Investigaciones Biolgicas del Noroeste, S.C.(CIBNOR). The authors express their appreciation toDr. Wallace J. Nichols, Rodrigo Rangel and the GrupoTortuguero for their assistance in this project. We alsoappreciate the expertise of Dr. Samuel Chvez Rosalesand Griselda Pea Armenta for their help with thequantitative analyses. This research was conducted in

accordance with Mexican laws and regulations, under permits provided by the Secretaria de Medio Ambientey Recursos Naturales (SGPA/DGVS/002-2895).



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References

Abbott IA, Hollenberg GJ. Marine algae of California. U.S.A.:Standford University Press; 1976. 827 pp.

Anan Y, Kunito T, Watanabe I, Sakai H, Tanabe S. Trace element accumulation in hawksbill turtles ( Eretomochelys imbricata ) andgreen turtles ( Chelonia mydas ) from Yaeyama Islands, Japan.Environ Toxicol Chem 2001;20:2802 14.

Arriaga CL, Vzquez-Domnguez E, Gonzlez-Cano J, Jimnez-Rosenberg R, Muoz-Lpez E, Aguilar-Sierra V. Regionesmarinas prioritarias de Mxico. Mxico: Comisin Nacional parael Conocimiento y uso de la Biodiversidad; 1998. 198 pp.

Bicho R, Joaquim N, Mendonca V, Al Kiyumi A, Mahmoud IY, Al KindiA. Levels of heavy metals and antioxidant enzymes in green turtle(Chelonia mydas ) in the Arabian Sea, Sultanate of Oman. Twentysixth annual symposium on sea turtle biology and conservation.Athens, Greece: International Sea Turtle Society; 2006.

Brand-Gardner SJ, Lanyon JM, Limpus CJ. Diet selection byimmature green turtles, Chelonia mydas , in subtropical MoretonBay, South-east Queensland. Aust J Zool 1999;47:181 91.

Bryan GW, Langston WJ. Bioavailability, accumulation and effects of heavy metals in sediments with special reference to UnitedKingdom estuaries: a review. Environ Pollut 1992;76:89-131.

Caurant F, Bustamante P, Bordes M, Miramand P. Bioaccumulation of cadmium, copper and zinc in some tissues of three species of marine turtles stranded along the French Altantic coasts. Mar Pollut Bull 1999;38:1085 91.

Daessl LW, Carriquiry JD, Navarro R, Villaescusa-Celaya JA.Geochemistry of surficial sediments from Sebastian VizcainoBay, Baja California. J Coast Res 2000;16:1133 45.

Franzellitti S, Locatelli C, Gerosa G, Vallini C, Fabbri E. Heavy metals in

tissues of loggerhead turtles ( Caretta caretta ) from the northwesternAdriatic Sea. Comp Biochem Physiol C 2004;138:187 94.

Gardner SC, Nichols WJ. Assessment of sea turtle mortality rates inthe Baha Magdalena region, Baja California Sur, Mxico.Chelonian Conserv Biol 2001;4:197 9.

Gardner SC, Fitzgerald SL, Acosta-Vargas B, Mndez-Rodrguez L.Heavy metal accumulation in four species of sea turtles from theBaja California Peninsula, Mexico. BioMetals 2006;19:91 9.

Garnett ST, Pirce IR, Scott FJ. The diet of the green turtle, Cheloniamydas (L.), in Torres Strait. Aust Wildl Res 1985;12:103 12.

Gordon AN, Pople AR, Ng J. Trace metal concentrations in livers andkidneys of sea turtles from south-eastern Queensland, Australia.Mar Freshw Res 1998;49:409 14.

Gutirrez-Galindo EA, Villaescusa-Celaya JA, Arrelola-Chimal A.Bioaccumulation of metals in mussels from tour sites of the coastalregion of Baja California. Cienc Mar 1999;25:557 77.

Lam JCW, Tanabe S, Chan SKF, Yuen EKW, Lam MHW, Lam PKS.Trace element residues in tissues of green turtles ( Chelonia mydas )from South China waters. Mar Pollut Bull 2004;48:164 92.

Lares ML, Flores-Muoz G, Lara-Lara R. Temporal variability of bioavailable Cd, Hg, Zn, Mn and Al in an upwelling regime.Environ Pollut 2002;120:595 608.

Linder G, Grillitsch B. Ecotoxicology of Metals. In: Sparling DW,Linder G, Bishop CA, editors. Ecotoxicology of amphibians andreptiles. Society of Environmental Toxicology and ChemistrySETAC press; 2000. p. 325 459.

Lpez-Mendilaharsu M, Gardner SC, Riosmena-Rodriguez R, Semin-

off JA. Identifying critical foraging habitats of the green turtle(Chelonia mydas ) along the Pacific Coast of the Baja CaliforniaPeninsula, Mxico. Aquat Conserv 2005;15:259 69.

Martin JH, Broenkow WW. Cadmium in plankton: elevatedconcentrations off Baja California. Science 1975;190:884 5.

Maffucci F, Caurant F, Bustamante P, Bentivegna F. Trace element (Cd, Cu, Hg, Se, Zn) accumulation and tissue distribution inloggerhead turtles ( Caretta caretta ) from the Western Mediterra-nean Sea (southern Italy). Chemosphere 2005;58:535 42.

Mndez-Rodrguez L, Acosta-Vargas B, Alvarez-Castaeda ST,Lechuga-Devze CH. Trace metal distribution along the southerncoast of Bahia de La Paz (Gulf of California), Mexico. BullEnviron Contam Toxicol 1998;61:616 22.

Nichols WJ, Arcas F. Third Annual Meeting of the Sea TurtleConservation Network of the Californias (Grupo Tortuguero de lasCalifornias). Mar Turt Newsl 2001;93:30 1.

Nichols WJ, Bird KE, Garcia S. Community-based research and itsapplication to sea turtle conservation in Bahia Magdalena, BCS,Mexico. Mar Turt Newsl 2000;89:4 7.

Rie MT, Lendas KA, Callard IP. Cadmium: tissue distribution and binding protein induction in the painted turtle, Chrysemys picta .Comp Biochem Physiol C 2001;130:41 51.

Riosmena-Rodrguez R. Vegetacin subacutica. In: Ongay E, editor.Informe Final de Actividades del Proyecto Salitrales de SanIgnacio. UABCS-ESSA; 1999. 523 pp.

Roncarati F. Utilizzo di macrofite marine come indicatori di stressambientali. Thesis in Environmental Sciences. University of Bologna, Campus Ravenna, Italy, 2003.

Ruiz-Fernndez AC, Pez-Osuna F, Hillaire-Marcel C, Soto-JimnezM, Gheleb B. Principle component analysis applied to theassessment of metal pollution from urban wastes in the Culiacnriver estuary. Bull Environ Contam Toxicol 2001;67:741 8.

Sakai H, Ichihashi H, Suganuma H, Tatsukawa R. Heavy metalmonitoring in seaturtles using eggs. MarPollut Bull 1995;30:347 53.

Sakai H, Saeki K, Ichihashi H, Suganuma H, Tanabe S, Tatsukawa R.

Species-specific distribution of heavy metals in tissues andorgans of loggerhead turtle ( Caretta caretta ) and green turtle(Chelonia mydas ) from Japanese coastal waters. Mar Pollut Bull2000;40:701 9.

Snchez-Rodrguez I, Huerta-Daz MA, Choumiline E, Holguin-Quinones O, Zertuche-Gonzlez JA. Elemental concentrations indifferent species of seaweeds from Loreto Bay, Baja CaliforniaSur, Mexico: implications for the geochemical control of metals inalgal tissues. Environ Pollut 2001;114:145 60.

Saudo-Wihelmy SA, Flegal AR. Trace metal concentrations in thesurf zone and in coastal waters off Baja California, Mexico.Environ Sci Technol 1996;30:1575 80.

Seminoff JA, Resendiz A, Nichols WJ. Diet of the East Pacific greenturtle, Chelonia mydas , in the central Gulf of California, Mexico.J Herpetol 2002;36:447 53.

Shumilin EN, Rodriguez-Figueroa G, Bermea OM, Baturina EL,Hernandez E, Rodrguez-Meza GD. Anomalous Trace Element Composition of Coastal Sediments near the Copper MiningDistrict of Santa Rosalia, Peninsula of Baja California, Mexico.Bull Environ Contam Toxicol 2000;65:261 8.

Shumilin E, Paez-Osuna F, Green-Ruiz C, Sapozhnikov D, Rodriguez-Meza GD, Godinez-Orta L. Arsenic, antimony, selenium and other trace elements in sediments of the La Paz lagoon, Peninsula of BajaCalifornia, Mexico. Mar Pollut Bull 2001;42:174 8.

Storelli MM, Marcotrigiano GO. Heavy metal residues in tissues of marine turtles. Mar Pollut Bull 2003;46:367 400.

Thomas P, Baer KN, White RB. Isolation and partial characterization

of metallothionein in the liver of the red-eared turtle ( Trachemys scripta ) following intraperitoneal administration of cadmium.Comp Biochem Physiol C 1994;107:221 6.


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Talavera et al 2007