**3. Results**

480 Health Management – Different Approaches and Solutions

Three separate sampling trips were made in Estero Banderitas (November 2004, February, 2005 and April, 2005) in order to collect marine plants available during different seasons. Algae and seagrass samples were collected along the length of the mangrove channel using 16 transects of 30 m length. Every 6 m along the transects, plants were manually collected within a 25 cm2 to 1 m2 area, depending on the density of the flora at that location, for a total of 80 samples per trip. The samples were stored in labeled plastic bags and contents were separated by species using taxonomic keys (Riosmena Rodríguez, 1999). Samples were

Liver and kidney tissues were collected from 8 dead green turtles that incidentally drowned in commercial fishing nets set in Magdalena Bay between February 2002 and April 2003. The straight carapace length of the turtles ranged from 47–77 cm, which is representative of the size range 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 decomposition. Tissue samples were stored in plastic bags and placed on ice for transport to the laboratory where they were

All stomach contents were collected and identified to the lowest possible taxonomic level based on published keys (Abbott and Hollenberg, 1976; Riosmena-Rodríguez, 1999). Entire sample volume and the relative sample 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 the Universidad Autónoma de Baja California Sur (UABCS), La Paz,

Tissue and plant samples (0.5 g) were dried in an oven at 70 °C until a dry weight was obtained. Dried samples were digested in acid-washed Teflon tubes with concentrated nitric acid in a microwave oven (CEM modelMars 5X, Matthews, NC). Samples were analyzed by atomic absorption (GBC Scientific equipment, model AVANTA, Dandenong, Australia) using an air-acetylene flame. The certified standard reference material, TORT-2 (National Research Council of Canada, Ottawa) was used to verify accuracy, and that the analytical values were within the range of certified values. All recoveries of metals analyzed were over 95%. Detection limits were: Zinc=0.0008, Cadmium = 0.0009, Mn= 0.002, Cu= 0.0025, Ni =

We analyzed the data based on taxonomic group (red algae, green algae, and seagrass), season, spatial area, and dominant species. Reported statistics are medians (nN2) and ranges in μg/g on a dry weight basis. The Mann–Whitney test was used for conducting two-tailed sample comparisons of tissues for each metal separately and for comparing metals in marine plants collected in Magdalena Bay with those found in the stomach contents. The Kruskal– Wallis test was used to compare the median metal concentration across all plant species. The null hypothesis was rejected if p≤0.05. The influence of concentration differences among samples was removed by converting data to the percent contribution of each metal to the

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

sun-dried in the field and then pressed to further remove moisture.

**2.2 Marine plant collection** 

**2.3 Sea turtle tissue collection** 

**2.4 Stomach content analyses** 

**2.5 Laboratory analyses** 

0.004, Fe=0.005, Pb=0.006 μg/g.

**2.6 Quantitative analyses** 

México.

#### **3.1 Temporal and spatial variation of metal concentration in plant species**

Based on our analysis, we found temporal and spatial variations in the concentration in several of heavy metals in seaweeds and seagrasses. In comparisons between the profiles of heavy metals in major plant groups, we found that Nickel differed significantly between the major groups (P=0.01), wherein seagrasses had lower concentrations (Tables 1 and 2). Analyzing all of the species (all sites combined), we found significant seasonal differences in the heavy metal concentrations with the exception of Zinc (P=0.53). Samples collected in April had a higher concentration of Cadmium (P<0.001) and Iron (P=0.002) and a lower concentration of Plumb (P<0.001) and Nickel (P=0.002) than the other months. Manganese was highest in November (P=0.049) and Copper was higher in November compared to February (P=0.01). In comparisons of the metal concentrations between plant species, the only significant differences were detected for Cadmium (p=0.009) in *Ruppia maritima* than all other species. In the case of the analysis of green algae alone, using all species combined, we found temporal significant differences of Cadmium in April (P=0.01).

In the case of other metals, we found significantly temporal differences in Plumb (Pb) concentration in *G. vermiculophylla* (P=0.02) in November but this species also had the highest concentration of Ni (P=0.03) in relation to the other species. Also, there were significant differences in the concentrations of Cadmium (P=0.001), Iron (P=0.01), and Nickel (P=0.002), while Plumb (P<0.001) and Copper (P=0.03) were significantly different than the same metals in November. In the same month, highest Nickel concentrations were recorded in *Codium amplivesiculatum*, while in April, *C. amplivesiculatum*, *Codium cuneatum*, and *Caulerpa sertularioides* from the middle region had the highest concentrations of Copper (7.3μg g−1 dw), Ni (11μg g−1 dw), and Mn (61.4μg g−1 dw), respectively. In February, like November, we had the highest Iron concentration and several species were responsible for this difference (in *H. johnstonii*; 567.5μg g−1 dw) and Zinc concentration (in *G. textorii*; 46.8μg g−1 dw). However, the lower zone had the highest concentrations of Cadmium (in *G. textorii*; 4.4μg g−1 dw) and Ni (*L. pacifica* and *Chondria nidifica*; 13.3 and 13.3μg g−1 dw). Copper (in *L. pacifica*; 2.9μg g−1 dw) and Plumb concentrations were highest in *G. andersonii*  from the middle zone (3.8μg g−1 dw).

The Foragining Ecology of the Green Turtle in the Baja California Peninsula: Health Issues 483

**Site Species Cadmium Plumb Nickel Manganese Iron Copper Head** *Codium amplivesiculatum\** nd 2.3 6.6 20.4 522.7 0.8

*Chondria nidifica\** nd 1.5 5.1 14.4 88.8 0.2

*Gracilaria textorii* 1.3 1 4.5 50.1 853.7 3

*Gracilaria vermiculophylla* 1.1 0.7 5 22.4 236.2 0.8

*Gracilariopsis andersonii\** 0.5 2 5.7 28.5 195.2 2.5

*Hypnea johnstonii* 0.7 4.3 9.1 151.6 995.8 2.2

*Ruppia maritima\** 6.9 3.8 2.9 32.6 1017.4 nd

*Codium cuneatum* 0.9 1 8.4 20.1 334.4 1.1

*Chondria nidifica\** 1 1.6 9.3 20.9 557.8 1.4

*Gracilaria textorii* 3.9 1 4.8 45.4 325 0.7

*Gracilaria vermiculophylla* 1.4 0.9 3.5 18.1 302.7 1.4

*Gracilariopsis andersonii\** 1.6 3.8 4.5 23.5 160.4 2.1

*Hypnea johnstonii\** 0.3 1.1 6.7 26.7 263.9 1

*Ruppia maritima\** 2.1 0.5 1.7 28.6 1443 0.9

*Codium cuneatum\** 2.2 0.1 3.2 10.5 141.5 0.5

*Caulerpa sertularoides\** 1.8 nd 1.8 7.3 223.9 1.1

*Chondria nidifica\** 1.7 1.6 13.3 15.6 291.5 1.3

*Gracilaria crispata\** 4.6 nd 3.9 40.3 576.8 1.6

*Gracilaria textorii* 4.3 0.7 5.1 48.5 100.9 1.5

*Gracilaria vermiculophylla* 1.6 0.8 4.3 14.7 186 0.9

*Gracilariopsis andersonii\** 3.8 0.1 2.3 25.5 322.3 1.5

*Hypnea johnstonii* 1.6 1.2 3.9 32.8 501.1 1.9

*Laurencia pacifica* 3.8 0.8 7.6 24 346.7 2.3

*Zostera marina\** 2.2 nd 2.8 33.9 630.3 1.6

Table 2. Heavy metal concentrations (µg.g-1 dry weight) in seaweeds and seagrasses

collected in the three sites. Values are expressed as medians and ranges given in parenthesis.

\* The values are refered to 1 specimen. nd signifies not detected.

*Sarcodiotheca gaudichaudii\** 0.9 1 5.4 17.2 121.8 0.1

**Mouth** *Codium amplivesiculatim* nd 0.8 6.2 15.3 298.1 1

*Caulerpa sertularioides\** 2.3 0.4 3.4 61.4 524.1 2.5

**Medium** *Coduim amplivesiculatum* 0.5 0.7 7.9 22.1 349.8 1.2



(nd - 2.7) (nd - 2) (3 - 6) (45.3 - 54.8) (476.3 - 1231.2) (1.2 - 4.8)

(0.6 - 2.9) (0.2 - 3.3) (1.1 - 5.1) (19.5 - 23.6) (206.2 - 372.2) (0.3 - 1.6)


(nd - 1.5) (0 - 8.5) (6.9 - 11.4) (20.6 - 282.5) (567.5 - 1424.1) (nd - 4.4)


(nd - 1.2) (nd - 1.3) (7.3 - 10) (12.1 - 63.5) (190.2 - 500.4) (nd - 7.3)

(nd - 2.3) (0.5 - 1.6) (5.9 - 11) (17.2 - 22.9) (241.7 - 427.1) (0.4 - 1.8)



(3.4 - 4.8) (0.6 - 1.4) (4.5 - 7.6) (43.5 - 51.2) (139.9 - 580.6) (0.4 - 1.8)

(1.1 - 1.6) (0.6 - 1) (2.9 - 5.5) (13 - 19.3) (269.9 - 771.5) (1 - 1.6)





(nd - 1.9) (0.4 - 2.3) (6 - 7.6) (12.6 - 42.2) (189.5 - 374.7) (0.7 - 1.3)





(1.5 - 4.4) (0.1 - 1.9) (3 - 6.2) (37.6 - 49.1) (81.8 - 578.4) (0.5 - 1.6)

(0.5 - 2.9) (0 - 2.7) (2.9 - 5.3) (14.4 - 23.9) (139.4 - 214.4) (0.6 - 1.3)


(0.4 - 2.7) (0.6 - 1.8) (1.8 - 6) (23.7 - 41.9) (227.8 - 774.5) (1.8 - 2.1)

(3 - 4.6) (nd - 1.7) (1.9 - 13.3) (22.9 - 25.2) (195.8 - 497.6) (1.8 - 2.6)



\* The values are referred to 1 specimen. nd signifies not detected.

Table 1. Temporal variation of heavy metal concentrations µg.g-1 dry weight in seaweeds and seagrasses collected at the Estero Banderitas. Values are expressed as medians and ranges given in parenthesis.


**Season Species Cadmium Plumb Nickel Manganese** Iron **Copper November** *Codium amplivesiculatum* 0.2 1.8 8 52.9 362.2 0.9

**February** *Codium amplivesiculatum* nd 0.8 6.6 12.6 190.2 0.8

\* The values are referred to 1 specimen. nd signifies not detected.

ranges given in parenthesis.

*Gracilaria textorii* 1.5 1.4 4.8 48.5 325 1.6

*Gracilaria vermiculophylla* 0.6 2.7 5.3 22.4 302.7 1.3

*Gracilariopsis andersonii\** 0.5 2 5.7 28.5 195.2 2.5

*Hypnea johnstonii* 0.4 1.8 6.7 26.7 263.9 1.8

*Codium cuneatum\** nd 1.6 5.9 17.2 241.7 0.4

*Chondria nidifica* 1 1.6 9.3 15.6 291.5 1.3

*Gracilaria textorii* 3.4 1 6 49.1 139.9 0.5

*Gracilaria vermiculophylla* 1.1 0.8 4.3 19.3 206.2 0.6

*Gracilariopsis andersonii\** 1.6 3.8 4.5 23.5 160.4 2.1

*Hypnea johnstonii\** nd nd 11.3 20.6 567.5 nd

*Laurencia pacifica\** 3 1.7 13.3 25.2 195.8 2.9

*Zostera marina\** nd 2.5 3.1 78.6 51.1 0.4

*Codium cuneatum* 2.1 0.3 7.1 16.7 284.3 1.2

*Caulerpa sertularioides* 2.1 0.2 2.6 34.3 374 1.8

*Gracilaria crispata\** 4.6 nd 3.9 40.3 576.8 1.6

*Gracilaria textorii* 4.5 0.4 5.3 41.5 579.5 1.7

*Gracilaria vermiculophylla* 2.9 0.2 2.9 18.1 236.2 0.9

*Gracilariopsis andersonii\** 3.8 0.1 2.3 25.5 322.3 1.5

*Hypnea johnstonii\** 2.7 0.6 1.8 41.9 774.5 2.1

*Laurencia pacifica\** 4.6 nd 1.9 22.9 497.6 1.8

*Ruppia maritima* 4.5 2.1 2.3 30.6 1230.2 0.5

*Zostera marina\** 2.2 nd 2.8 33.9 630.3 1.6

Table 1. Temporal variation of heavy metal concentrations µg.g-1 dry weight in seaweeds and seagrasses collected at the Estero Banderitas. Values are expressed as medians and

*Sarcodiotheca gaudichaudii\** 0.9 1 5.4 17.2 121.8 0.1

**April** *Codium amplivesiculatum* 1.6 0.5 7.8 18.7 399.2 4.1

(nd - 0.5) (1.3 - 2.3) (6 - 9.9) (42.2 - 63.5) (349.8 - 374.7) (0.7 - 1.2)

(nd - 3.9) (nd - 1.9) (3 - 5.1) (45.3 - 51.1) (100.9 - 1231.2) (0.7 - 4.8)

(0.5 - 1.4) (1 - 3.3) (4.9 - 5.5) (13 - 23.9) (185.9 - 372.2) (1 - 1.6)


(0.3 - 1.5) (1.1 - 8.5) (6 - 6.9) (23.7 - 282.5) (227.8 - 1424.1) (0.9 - 4.4)


(nd - 1.7) (1.5 - 1.6) (5.1 - 13.3) (14.40- 21) (88.8 - 557.8) (0.2 - 1.4)

(2.7 - 4.4) (0.7 - 2) (4.5 - 6.2) (43.5 - 54.8) (81.8 - 476.3) (0.4 - 1.2)

(1.1 - 1.6) (0.7 - 0.9) (3.6 - 5.1) (14.4 - 19.5) (139.4 - 269.9) (0.3 - 1.6)






(1.2 - 1.9) (0.4 - 0.7) (7.6 - 7.9) (15.3 - 22.1) (298.1 - 500.4) (1 - 7.3)

(1.9 - 2.2) (0.1 - 0.5) (3.2 - 11) (10.5 - 23) (141.5 - 427.1) (0.5 - 1.8)

(1.8 - 2.3) (nd - 0.4) (1.8 - 3.4) (7.3 - 61.4) (223.9 - 524.1) (1.1 - 2.6)


(4.3 - 4.8) (0.1 - 0.6) (3 - 7.6) (37.6 - 45.4) (578.4 - 580.6) (1.5 - 1.8)

(2.7 - 2.9) (nd - 0.6) (1.1 - 2.9) (14.7 - 23.6) (214.4 - 771.5) (0.9 - 1.6)




(2.1 - 7) (0.5 - 3.8) (1.7 - 2.9) (28.6 - 32. 6) (1017.4 - 1443) (nd - 0.9)


(0 - 2.3) (6.2 - 7.3) (12.1 - 20.4) (189.5 - 522.7) (nd - 1.3)



\* The values are refered to 1 specimen. nd signifies not detected.

Table 2. Heavy metal concentrations (µg.g-1 dry weight) in seaweeds and seagrasses collected in the three sites. Values are expressed as medians and ranges given in parenthesis.

The Foragining Ecology of the Green Turtle in the Baja California Peninsula: Health Issues 485

Fig. 3. Multivariate analysis of the spatial concentration of heavy metal in green algae.

Fig. 4. Multivariate analysis of the spatial concentration of heavy metal in red algae.

metals with low concentration (Fig. 5).

Multivariate analyses show the same path in red algae (Figs. 4 and 5) with the clump of areas within metals and a group of metals with high concentration (Fig. 4) in relation to

Spatial differences in metal concentrations were dependent on the major taxa. In the case of seagrasses, we found a high concentration of Iron (Table 2) who was significant different from Manganese (in *Z. marina*; 78.6 μg g−1 dw) concentrations were highest in the upper zone (P=0.01) because their uneven distribution in the area. Consistent with the above analysis were the multifactorial analysis (Fig. 2) wherein the extreme values are represented by Iron and Manganese with no association among seasons or areas. In the green algae (Table 2), we were able to find many metals in the entire area, but the significant difference was found in Cadmium in April (P=0.01), when all species combined, because the low value in relation to other metals are highly concentrated. There is no consistent pattern in relation to the area of the highest concentration of any metal; they tend to present a group lower in relation to higher concentration in different areas or times (Tables 1 and 2).

Fig. 2. Multivariate analysis of heavy metals contents in seagrasses.

This is well supported by the multivariate analysis (Fig.3) wherein most of the observed metals show a combination among them and the areas of sampling. We found an extremely high variability in the median content in the red algae (Table 2) but there were no significant differences between sites, with the exception of Zinc which was significantly higher in the upper zone (P=0.02). The highest concentration of any metal was Iron in *Hypnea johnstonii* from the upper zone (1,424.1μg g−1 dw). The highest concentration of Manganese (282.5μg g−1 dw) and Plumb (8.5) μg g−1 dw) were also detected in *H. johnstonii* from the upper zone. Similarly, Zinc (58.8μg g−1 dw) and Copper (4.8μg g−1 dw) concentrations were highest in *G. textorii* in the same zone. The highest Cadmium concentrations were measured in *G. textorii* (4.8μg g−1 dw).

Spatial differences in metal concentrations were dependent on the major taxa. In the case of seagrasses, we found a high concentration of Iron (Table 2) who was significant different from Manganese (in *Z. marina*; 78.6 μg g−1 dw) concentrations were highest in the upper zone (P=0.01) because their uneven distribution in the area. Consistent with the above analysis were the multifactorial analysis (Fig. 2) wherein the extreme values are represented by Iron and Manganese with no association among seasons or areas. In the green algae (Table 2), we were able to find many metals in the entire area, but the significant difference was found in Cadmium in April (P=0.01), when all species combined, because the low value in relation to other metals are highly concentrated. There is no consistent pattern in relation to the area of the highest concentration of any metal; they tend to present a group lower in relation to higher concentration in different

areas or times (Tables 1 and 2).

in *G. textorii* (4.8μg g−1 dw).

Fig. 2. Multivariate analysis of heavy metals contents in seagrasses.

This is well supported by the multivariate analysis (Fig.3) wherein most of the observed metals show a combination among them and the areas of sampling. We found an extremely high variability in the median content in the red algae (Table 2) but there were no significant differences between sites, with the exception of Zinc which was significantly higher in the upper zone (P=0.02). The highest concentration of any metal was Iron in *Hypnea johnstonii* from the upper zone (1,424.1μg g−1 dw). The highest concentration of Manganese (282.5μg g−1 dw) and Plumb (8.5) μg g−1 dw) were also detected in *H. johnstonii* from the upper zone. Similarly, Zinc (58.8μg g−1 dw) and Copper (4.8μg g−1 dw) concentrations were highest in *G. textorii* in the same zone. The highest Cadmium concentrations were measured

Fig. 3. Multivariate analysis of the spatial concentration of heavy metal in green algae.

Multivariate analyses show the same path in red algae (Figs. 4 and 5) with the clump of areas within metals and a group of metals with high concentration (Fig. 4) in relation to metals with low concentration (Fig. 5).

Fig. 4. Multivariate analysis of the spatial concentration of heavy metal in red algae.

The Foragining Ecology of the Green Turtle in the Baja California Peninsula: Health Issues 487

Fig. 6. Percent contribution of metals in species of marine flora collected in the Magdalena Bay and in green turtle (*Chelonia mydas*) stomach contents. A) *G. vermiculophylla*, B) *G.* 

Eight species of marine flora were identified within the green turtle stomach contents (Table 3). These same species were also collected from the mangrove channel of Estero Banderitas with the exception of *Neoagarddhiella baileyi, Pterocladiella capillacea* and *Ulva lactuca*. *Hypnea johnstonii*, which has been previously reported as a major food item in green turtle diet (López-Mendilaharsu et al., 2005), was available in the bay but not found in the stomachs of the turtles. *Gracilaria vermiculophylla* was present in 60%of the turtle stomachs analyzed and made up the greatest total percent volume (36%). Gracilaria textorii was present in the

*textorii*, C) *C. amplivesiculatum*, D) *R. maritima* and E) *Z. marina*.

second greatest percent volume (16.5%).

Fig. 5. Multivariate analysis of the spatial concentration of heavy metal in red algae.

#### **3.2 Metals in sea turtle tissues, stomach contents, and plants from the bay**

Concentrations of Cadmium and Zinc in flora from the sea turtle stomach contents were greater than the same species of marine plants collected in the bay (p<0.001 and p=0.003, respectively) (Figure 6). For both metals, the concentrations in sea turtle liver were not significantly different from the stomach contents. Sea turtle kidney Cadmium concentration was significantly higher than liver ( p=0.002), while Zinc was the same in both tissues. Plumb, Manganese and Fe in flora from the stomach contents were significantly lower than in flora collected from the bay (p<0.001 for each) (Figure 6). The stomach contents had higher Plumb and Manganese concentrations than liver (p=0.04 and p<0.001, respectively) but were not significantly different in Fe. There were no differences in the concentrations of these metals in liver and kidney. Nickel and Copper concentrations did not differ in plants from the two sources. Nickel concentration in liver was similar to kidney concentrations, but significantly lower than the stomach contents (p=0.005). Copper was higher in liver than stomach contents (p<0.001) and higher than kidney (p<0.001). 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 to the bay samples (Fig. 6). For each of the five plant species, the percent contribution of Manganese and Plumb was greater in the baycollected plants, while Cadmium and Zinc consistently contributed more to the total metal profile in plants from the stomach contents. Fig. 7 shows the percent contribution of each metal in paired samples of liver, kidney and stomach contents (all flora combined) from the same turtles. Cadmium and Zinc contributed most to the overall metal profile in the kidney, while Copper contributed more in liver. The percent contribution of Manganese and Nickel were greatest in the plants from the stomach contents.

Fig. 5. Multivariate analysis of the spatial concentration of heavy metal in red algae.

Concentrations of Cadmium and Zinc in flora from the sea turtle stomach contents were greater than the same species of marine plants collected in the bay (p<0.001 and p=0.003, respectively) (Figure 6). For both metals, the concentrations in sea turtle liver were not significantly different from the stomach contents. Sea turtle kidney Cadmium concentration was significantly higher than liver ( p=0.002), while Zinc was the same in both tissues. Plumb, Manganese and Fe in flora from the stomach contents were significantly lower than in flora collected from the bay (p<0.001 for each) (Figure 6). The stomach contents had higher Plumb and Manganese concentrations than liver (p=0.04 and p<0.001, respectively) but were not significantly different in Fe. There were no differences in the concentrations of these metals in liver and kidney. Nickel and Copper concentrations did not differ in plants from the two sources. Nickel concentration in liver was similar to kidney concentrations, but significantly lower than the stomach contents (p=0.005). Copper was higher in liver than stomach contents (p<0.001) and higher than kidney (p<0.001). 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 to the bay samples (Fig. 6). For each of the five plant species, the percent contribution of Manganese and Plumb was greater in the baycollected plants, while Cadmium and Zinc consistently contributed more to the total metal profile in plants from the stomach contents. Fig. 7 shows the percent contribution of each metal in paired samples of liver, kidney and stomach contents (all flora combined) from the same turtles. Cadmium and Zinc contributed most to the overall metal profile in the kidney, while Copper contributed more in liver. The percent contribution of Manganese and Nickel

**3.2 Metals in sea turtle tissues, stomach contents, and plants from the bay** 

were greatest in the plants from the stomach contents.

Fig. 6. Percent contribution of metals in species of marine flora collected in the Magdalena Bay and in green turtle (*Chelonia mydas*) stomach contents. A) *G. vermiculophylla*, B) *G. textorii*, C) *C. amplivesiculatum*, D) *R. maritima* and E) *Z. marina*.

Eight species of marine flora were identified within the green turtle stomach contents (Table 3). These same species were also collected from the mangrove channel of Estero Banderitas with the exception of *Neoagarddhiella baileyi, Pterocladiella capillacea* and *Ulva lactuca*. *Hypnea johnstonii*, which has been previously reported as a major food item in green turtle diet (López-Mendilaharsu et al., 2005), was available in the bay but not found in the stomachs of the turtles. *Gracilaria vermiculophylla* was present in 60%of the turtle stomachs analyzed and made up the greatest total percent volume (36%). Gracilaria textorii was present in the second greatest percent volume (16.5%).

The Foragining Ecology of the Green Turtle in the Baja California Peninsula: Health Issues 489

contribution of individual metals to the overall signature of marine flora from Magdalena Bay, kidney, liver and stomach contents samples from green turtles (*Chelonia mydas*). B)

In our study we found less of 1% of the animals with some fibropapiloms but at least 20% with epibionts. This is consistent with the data from Caribbean populations in where 2% had tumors present. The main observed difference was the degree of development between the populations in Bahía Magdalena (Fig. 9a) with very few in the carapace, frontal fins and head. In Caribbean populations bibber tumors (Fig. 9b) were observed and more

Fig. 9. A) Population in Bahía Magdalena (Fig. 9a) with very few in the carapace, frontal fins and head. B) Caribbean population's bibber tumors were observed and more concentrated

Fig. 8. A) Plot of sample scores of a Principle Component Analysis of the percent

Loadings plot

**3.4 Prescence of fibropapiloms and epibionts** 

concentrated in the head or in the frontal fins.

in the head or in the frontal fins.

Fig. 7. Percent contribution of metals in tissues and the stomach contents of green turtles (*Chelonia mydas*) from Magdalena Bay, Mexico.


Table 3. Percent volume of macroalgae and sea grasses in the stomach contents of five green turtles (*Chelonia mydas*) collected in Estero Banderitas, Magdalena Bay, Mexico.

#### **3.3 Principal components analysis**

Principal components analysis (PCA) of the percent 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. 8). Plots of the sample scores on the first and second principal components produced four 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. 8A). All but one of the bay plant samples obtained negative scores on PC(1), whereas plants from the stomach contents generally scored greater than 0. The loadings plot, which 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' metal signatures by Zinc and Cadmium. The separation of liver and kidney samples appeared to be influenced by the greater contribution of Cadmium to the metal profile in kidney, and the dominance of Cu in liver samples which scored higher on PC(2) (Fig. 8B).

Fig. 8. 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, kidney, liver and stomach contents samples from green turtles (*Chelonia mydas*). B) Loadings plot

#### **3.4 Prescence of fibropapiloms and epibionts**

488 Health Management – Different Approaches and Solutions

Fig. 7. Percent contribution of metals in tissues and the stomach contents of green turtles

**Species** 1 2 3 4 5 TOTAL *Codium amplivesiculatum* 69.1% 13.8% *Gracilaria textorii* 30.9% 51.6% 16.5% *Gracilaria vermiculophylla* 48.4% 33.6% 100% 36.4% *Neoagarddhiella baileyi* 36.2% 7.2% *Pterocladiella capillacea* 20.5% 4.1% *Rupia maritima* 43.3% 8.7% *Ulva lactuca* 31.8% 6.4% *Zostera marina* 34.5% 6.9%

Table 3. Percent volume of macroalgae and sea grasses in the stomach contents of five green

Principal components analysis (PCA) of the percent 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. 8). Plots of the sample scores on the first and second principal components produced four 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. 8A). All but one of the bay plant samples obtained negative scores on PC(1), whereas plants from the stomach contents generally scored greater than 0. The loadings plot, which 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' metal signatures by Zinc and Cadmium. The separation of liver and kidney samples appeared to be influenced by the greater contribution of Cadmium to the metal profile in kidney, and the dominance of Cu in liver samples which scored higher on PC(2) (Fig. 8B).

turtles (*Chelonia mydas*) collected in Estero Banderitas, Magdalena Bay, Mexico.

(*Chelonia mydas*) from Magdalena Bay, Mexico.

**Stomach Contents** 

**3.3 Principal components analysis** 

In our study we found less of 1% of the animals with some fibropapiloms but at least 20% with epibionts. This is consistent with the data from Caribbean populations in where 2% had tumors present. The main observed difference was the degree of development between the populations in Bahía Magdalena (Fig. 9a) with very few in the carapace, frontal fins and head. In Caribbean populations bibber tumors (Fig. 9b) were observed and more concentrated in the head or in the frontal fins.

Fig. 9. A) Population in Bahía Magdalena (Fig. 9a) with very few in the carapace, frontal fins and head. B) Caribbean population's bibber tumors were observed and more concentrated in the head or in the frontal fins.

The Foragining Ecology of the Green Turtle in the Baja California Peninsula: Health Issues 491

cases, in the levels of toxicity. Temporal variations in metal concentrations, such as high concentrations in Cadmium and other metals observed in April, may be related to local upwelling events. Surface water Cadmium concentrations have been strongly correlated with upwelling (Lares et al. 2002) which occurs during spring and early summer off the coast of Magdalena Bay (Zaytsev et al., 2003). These levels of Cadmium in seaweeds has not been observed in the Gulf of California studied populations but strong species and spatial variations where observed (Páez-Osuna et al., 2000; Sánchez-Rodríguez et al. 2001; Rodriguez-Castañeda et al., 2006). The differences in heavy metal concentrations that we found in the seaweeds did not generally correspond with patterns of those elements previously observed in the sediment from the same region or seaweed species (Rodríguez-Meza et al., 2008), contrary to the studied sites in the Gulf of California near a mine (Rodriguez-Castañeda et al., 2006) or near industrial ports (Páez-Osuna et al., 2000; Sánchez-Rodríguez et al., 2001; Rodriguez-Castañeda et al., 2006). This finding, together with the observed species differences, suggests that the metabolic condition and life cycle stage of the individual species might influence metal uptake and accumulation (Lobban and Wynne 1981). Similarly, Riget et al., (1995) found differences between seaweed species *Ascophyllum nodosum, Fucus vesiculosus*, and *Fucus distichus*. We found lower levels of Ni and Zinc in *H. johnstonii* than in the environment as reported by Rodríguez-Meza et al., (2008). Based on our data, there are similarities between the composition and concentration of heavy metals between the plant species reviewed and the sediment; except in the case of Cu, Fe, and Mn (Rodríguez-Meza et al., 2008). All those elements are considered critical in the photosynthetic metabolism (Lobban and Wynne, 1981). We might assume that those elements are more easily assimilated by the plants because of their use in photosynthesis. The role of seaweeds and seagrasses in coastal lagoons (like Banderitas or any other along the Baja California Peninsula) are relevant because they are feeding grounds for black turtles (*C. mydas*), loggerhead turtles (*Caretta caretta*), olive Ridley turtles (*Lepidochelys olivacea*), and hawksbill turtles (*Eretmochelys imbricata*) and migratory birds like Brant geese (*Branta bernicla*; Seminoff, 2000; Herzog and Sedinger, 2004). All of the species are included in the Mexican endangered species list (NOM ECOL 059) and on the red list in the UICN endangered species (www. uicnredlist.org). They are high productivity areas for fishing all kind of products (CONABIO, 2000; Carta Nacional, 2005). The fact that we found more significant variation in the spatial than temporal heavy metal concentrations in most of the species show that they might be constantly incorporated in the diet of many herbivorous animals (Gardner et al., 2006) with severe consequences in their health. Management

strategies for these species should consider monitoring the levels of metals.

Pb, Cu and Mn concentrations in tissue from this study were within the range of those reported for sea turtles in other parts of the world (Lam et al., 2004; Storelli and Marcotrigiano, 2003). However, the average concentrations of Cadmium, Zinc and Ni in kidney of green turtles from Magdalena Bay were high compared to previously reports for sea turtle tissues (Sakai et al., 1995, 2000; Storelli and Marcotrigiano, 2003). Studies of loggerhead turtles (Maffucci et al., 2005) suggest that sea turtles can regulate Copper and Zinc concentrations through homeostatic processes but that Cadmium uptake is not controlled by active process and thus tissue concentrations of this metal reflect exposure. In agreement with these findings, we observed that Cadmium concentrations in green turtle liver were similar to their food and that the Cu concentration in sea turtle liver was greater

**4.2 Sea turtle tissue comparisons** 
