Contamination by Persistent Organochlorines in Cetaceans ...

Arch. Environ. Contam. Toxicol. 46, 124 –134 (2004) DOI: 10.1007/s00244-003-2239-y

A R C H I V E S O F

Environmental Contamination a n d Toxicology © 2004 Springer-Verlag New York Inc.

Contamination by Persistent Organochlorines in Cetaceans Incidentally Caught Along Brazilian Coastal Waters N. Kajiwara,1 S. Matsuoka,1 H. Iwata,1 S. Tanabe,1 F. C. W. Rosas,2 G. Fillmann,3 J. W. Readman4 1 2 3 4

Center for Marine Environmental Studies, Ehime University, 3-5-7 Tarumi, Matsuyama 790-8566, Japan Instituto Nacional de Pesquisas da Amazoˆnia, C.P. 478, Manaus, AM, 69011-970, Brazil Fundaçaõ Universidade Federal do Rio Grande, C.P. 474, Rio Grande, RS, 96201-900, Brazil Plymouth Marine Laboratory, Prospect Place, The Hoe Plymouth, PL1 3DH UK

Received: 28 October 2002 /Accepted: 16 March 2003

Abstract. Wide ranges of organochlorine residues were determined in the blubber of franciscana (Pontoporia blainvillei), estuarine dolphin (Sotalia guianensis), Atlantic spotted dolphin (Stenella frontalis), and long-beaked common dolphin (Delphinus capensis) incidentally caught along Brazilian coastal waters. Concentrations of DDTs and PCBs were the highest, followed by CHLs, TCPMOH, dieldrin, TCPMe, heptachlor epoxide, HCB, and HCHs. Unexpectedly, significant pollution of PCBs, DDTs, TCPMe, and TCPMOH were observed in cetaceans from Brazil, implying the occurrence of local sources in the Southern Hemisphere comparable to those in the Northern Hemisphere, probably by high industrialization in Brazil. On the other hand, CHLs, HCB, HCHs, heptachlor epoxide, and dieldrin residue levels in Brazilian dolphins were much lower than those in other species from the Northern Hemisphere. Significant correlations of TCPMe and TCPMOH were found along with PCBs and DDTs, indicating the highly bioaccumulative nature of all these compounds and/or possible similar pollution sources.

The worldwide contamination by persistent organochlorines (OCs) such as PCBs and DDTs has been documented and poses a great concern by their endocrine disrupting effects on human and wildlife. Because of the chemically stable and lipophilic nature of these OCs, their contamination and extensive biomagnification have been noted in aquatic mammals, the top predators of the ecosystem (Tanabe et al. 1984). Since 1968, several abnormalities such as reproductive failure, immune impairment, tumors, and virus infection have been observed in aquatic mammals over the world, and declines in population and mass mortality have also been reported (e.g., Colborn and Smolen 1996). Since a linkage between these abnormalities and high concentrations of OCs was suspected, we conducted

Correspondence to: Shinsuke Tanabe; e-mail: [email protected]

studies focused on OC contaminants in various aquatic mammals (e.g., Subramanian et al. 1987a; Tanabe et al. 1994a; Nakata et al. 1995; Kajiwara et al. 2002a). In accordance with the massive usage of chemicals in several developed countries, notable OC pollution in the Northern Hemisphere became obvious by our studies. Although OCs levels in the Southern Hemisphere have been thought to be low, little information is available for elucidating the contamination status there. Only limited studies are available for addressing the differences of OCs pollution between the two hemispheres using offshore species such as minke whale (Balaenoptera acutorostrata) (Aono et al. 1997) and albatross (Guruge et al. 2001). However, only very few studies have been conducted regarding the OCs pollution of terrestrial and coastal areas in the Southern Hemisphere (e.g., Sericano et al. 1995). The present study is aimed at understanding the contamination of OCs in cetaceans incidentally caught along Brazilian coastal waters during 1997 and 1999. The two newly identified microcontaminants, tris(4-chlorophenyl)methane [TCPMe] and tris(4-chlorophenyl)methanol [TCPMOH] were also examined to understand their global distribution and behavior.

Materials and Methods Samples Twenty-six estuarine dolphins (Sotalia guianensis), 26 franciscanas (Pontoporia blainvillei), 2 Atlantic spotted dolphins (Stenella frontalis), and a long-beaked common dolphin (Delphinus capensis) were incidentally caught along the coasts of Sao˜ Paulo and Parana´ states in Brazil during 1997 and 1999 (Figure 1). Both the estuarine dolphin and the franciscana are endemic odontoceti species distributed in southwestern Atlantic waters. They inhabit mainly shallow waters without any wide range migration and feed on fish, cephalopods, and crustaceans (Da Silva and Best 1994; Danilewicz et al. 2002). For comparison, two Blainville’s beaked whales (Mesoplodon densirostris) found stranded on the coast of Mauritius in September 2000 were also included in this study. The limited information available for Blainville’s beaked whale shows that these whales generally feed on squid and possibly some fish at the seabed in deep waters. Biological data on

Contamination by Organochlorines in Cetaceans

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Fig. 1. Map showing the location of cetaceans incidentally caught in Brazilian coastal waters.

the animals analyzed in the present study are given in Table 1. Blubber samples were excised from dead animals, wrapped in aluminum foil, and kept in a deep freezer at ⫺20°C until analysis.

Chemical Analysis PCBs and other organochlorines (DDTs, HCHs, CHLs, HCB, heptachlor epoxide, dieldrin, TCPMe, and TCPMOH) were analyzed following the method reported by Tanabe et al. (1994b) and Watanabe et al. (1999) with slight modification. Briefly, approximately 2–3 g of blubber sample was ground with anhydrous sodium sulfate and extracted in a Soxhlet apparatus with a mixture of diethyl ether and hexane for 7– 8 h. After concentration, an aliquot of the extract was added to a gel permeation chromatography column (GPC; Bio-Beads S-X3, Bio-Rad Laboratories, CA; 2-cm i.d. and 50-cm length) for lipid removal. Equivalent mixture of dichloromethane in hexane was used as mobile phase with a flow rate of 5 ml/min. The first 120-ml fraction was discarded. The second 100-ml fraction containing organochlorine compounds was collected, concentrated, and passed through an activated Florisil column for fractionation. The first fraction eluted with

hexane contained PCBs, p,p⬘-DDE, trans-nonachlor, and HCB, and the second fraction eluted with 20% dichloromethane in hexane contained chlordane compounds (oxychlordane, cis-chlordane, transchlordane, cis-nonachlor, trans-nonachlor), DDTs (p,p⬘-DDE, p,p⬘DDD, p,p⬘-DDT), HCHs (␣-, ␤-, ␥-isomers), and TCPMe. The third fraction eluted with 50% dichloromethane in hexane contained heptachlor epoxide, dieldrin, and TCPMOH. Quantification of PCBs and organochlorine pesticides was performed using a GC (Hewlett Packard 6890 series) equipped with an ECD (electron capture detector) and an autoinjection system. The GC column used was a fused silica capillary (DB-1; J&W Scientific; 0.25-␮m film thickness, 0.25-mm i.d., 30-m length). Identification and quantification of TCPMe and TCPMOH were performed using a GC-MS (HP6890 and HP5973) in selective ion monitoring mode (SIM) equipped with an autoinjection system (HP6893) and a fused silica capillary (DB-1; J&W Scientific; 0.25-␮m film thickness, 0.25-mm i.d., 30-m length). The concentration of individual organochlorines was quantified from the peak area on the sample to that of the corresponding external standard. The PCB standard used for quantification was an equivalent mixture of Kanechlor preparations (KC-300, KC-400, KC-500, and KC-600) with known PCB composition and

a

BL (cm)

4 15

NA

NA NA

1 213

1 340 1 400

2 (0–4) 12 (8–16) 2 (0–4) 6 (5–7)

1 (0–3) 16 (11–27) 1 (0–5) 14 (7–29)

Age (yr)

1 157 1 198

8 100 (75–114) 2 126 (124–127) 11 99 (66–112) 5 113 (110–119)

4 133 (96–165) 5 181 (173–186) 9 141 (89–160) 8 187 (180–198)

n

83 81

57

19 18

87 (79–95) 79 (72–85) 87 (82–99) 80 (73–86)

81 (77–84) 55 (5.4–72) 76 (65–82) 72 (58–79)

Lipid (%)

1,300 1,500

17,000

58,000 60,000

2,200 (970–5,000) 2,300 (1,500–3,000) 2,100 (320–4,900) 5,300 (1,800–12,000)

12,000 (6,000–20,000) 11,000 (1,300–49,000) 9,700 (2,800–22,000) 34,000 (10,000–79,000)

PCBs

BL, body length; HP epox., heptachlor epoxide; NA, no data available.

Atlantic spotted dolphin (Stenella frontalis) Immature male Mature male Long-beaked common dolphin (Delphinus capensis) Mature male Mauritius Blainville’s beaked whale (Mesoplodon densirostris) Immature male Mature male

Mature male

Immature male

Mature female

Franciscana (Pontoporia blainvillei) Immature female

Mature male

Immature male

Mature female

Brazil Estuarine dolphin (Sotalia guianensis) Immature female

Species

2,700 2,700

11,000

25,000 48,000

2,800 (670–3,200) 1,200 (950–1,400) 1,700 (580–3,600) 9,900 (1,800–35,000)

14,000 (1,400–25,000) 7,600 (1,000–29,000) 22,000 (3,900–64,000) 52,000 (12,000–150,000)

DDTs

55 69

200

660 690

38 (17–74) 39 (31–47) 40 (4.7–94) 64 (38–110)

180 (6.3–310) 150 (15–680) 150 (50–500) 420 (150–1100)

CHLs

21 15

200

390 160

18 (0.58–43) 21 (15–26) 28 (11–61) 29 (17–42)

42 (0.59–70) 8.8 (5.1–13) 120 (18–340) 170 (93–340)

Dieldrin

76 85

32

71 84

10 (5.6–18) 9.2 (6.4–12) 11 (1.4–21) 11 (9.4–13)

25 (1.6–57) 19 (2.1–79) 16 (4.5–28) 68 (6.9–400)

HCB

2.0 1.5

77

130 84

6.2 (2.4–12) 4.4 (4.0–4.7) 7.0 (3.1–14) 7.8 (4.6–12)

39 (14–88) 2.8 (1.6–4.2) 56 (17–140) 98 (38–180)

4.1 3.1

24

50 27

2.6 (1.5–4.6) 4.6 (2.3–6.8) 2.5 (⬍1–4.3) 3.8 (3.4–5.3)

12 (⬍1–14) 2.3 (⬍1–2.5) 15 (4.5–61) 19 (7.7–38)

HP epox. HCHs

Table 1. Biological data and organochlorine concentrations (mean and range, ng/g lipid weight) in the blubber of cetaceans from Brazil and Mauritiusa

2.9 2.7

82

180 550

6.8 (1.8–18) 5.4 (4.0–6.7) 3.9 (0.66–7.5) 23 (5.7–72)

34 (24–51) 63 (7.4–240) 30 (12–54) 160 (36–460)

TCPMe

5.3 6.2

97

210 110

18 (6.3–47) 12 (7.9–16) 16 (6.0–38) 40 (14–120)

77 (56–100) 12 (8.0–17) 140 (36–380) 140 (60–290)

TCPMOH

126 N. Kajiwara et al.


content (Tanabe et al. 1987a). Concentrations of individually resolved peaks of PCBs isomers and congeners were summed to obtain total PCB concentrations. Procedural blanks were analyzed simultaneously with samples to check for interferences or contamination from solvents and glassware. The concentration of OCs was expressed on a lipid weight basis unless otherwise specified. For quality assurance and control, our laboratory participated in the Intercomparison Exercise for Persistent Organochlorine Contaminants in Marine Mammals Blubber, organized by the National Institute of Standards and Technology (Gaithersburg, MD) and the Marine Mammal Health and Stranding Response Program of the National Oceanic and Atmospheric Administration’s National Marine Fisheries Service (Silver Spring, MD). Standard reference material (SRM 1945) was analyzed for selected PCB congeners and persistent OCs. Data from our laboratory were in good agreement with those for reference materials. The average percentage deviation from the certified values was 13% (range: 0.5–20%) for organochlorine pesticides and 28% (range: 1.3–57%) for PCB congeners. Probability values less than 0.05 were considered statistically significant using Mann–Whitney U test and Spearman rank correlation.

Results and Discussion Contamination Status OC contaminants were detected in all the blubber samples of estuarine dolphin, franciscana, Atlantic spotted dolphin, and long-beaked common dolphin from the Brazilian coastal waters and Blainville’s beaked whales from Mauritius (Table 1). In the Brazilian dolphins, DDTs and PCBs were the predominant contaminants, with 150 and 79 ␮g/g lipid wt as the maximum concentrations in the blubber sample of estuarine dolphin and 35 and 12 ␮g/g lipid wt in franciscana, respectively. On the other hand, CHLs, HCB, HCHs, TCPMe, TCPMOH, heptachlor epoxide, and dieldrin were detected at levels two to three orders of magnitude lower than those of PCBs and DDTs. HCH accumulation was the lowest among all the OCs analyzed and ␣- and ␥-HCH were below the detection limit (⬍1 ng/g lipid wt) in all the Brazilian samples. TCPMe and TCPMOH in some samples were not quantified due to interference. Elevated concentrations of PCBs and DDTs suggest serious pollution by these chemicals on the southern Brazilian coast. In Brazil, although the agricultural use of DDT and other persistent OC pesticides was forbidden in 1985, they are still being used for public health purposes (Paumgartten et al. 2000). In the Mauritius samples, DDT was the predominant contaminant, followed by PCBs ⬎ HCB ⬎ CHLs ⬎ dieldrin ⬎ TCPMOH ⬎ HCHs ⬎ TCPMe ⬎ heptachlor epoxide (Table 1). Except for HCB, OC residue levels found in the blubber of Blainville’s beaked whales from Mauritius were generally lower than in Brazilian samples and the order of contaminants levels was slightly different between the cetaceans from these two regions. TCPMe and TCPMOH were detected in most of the samples analyzed, ranging from 0.66 to 550 ng/g lipid wt and from 5.3 to 380 ng/g lipid wt, respectively, indicating widespread contamination by these compounds in the coastal ecosystem of Brazil and Mauritius. To our knowledge, this is the first comprehensive study showing the accumulation of TCPMe with TCPMOH in animals from the Southern Hemisphere.

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OC residue levels detected in estuarine dolphin were significantly higher than those in franciscana for all the compounds analyzed (p ⬍ 0.001 except HCB, with p ⬍ 0.05; Table 1). This can be explained by their ecology since the estuarine dolphin lives closer to coastal area and catches bigger prey than franciscana. In contrast to male animals that showed an agedependent accumulation of OCs, mature females generally contained lower levels (Figures 2 and 3) A similar trend has also been recorded in many species of aquatic mammals (e.g., Subramanian et al. 1987b; Tanabe et al. 1987b; Nakata et al. 1995; Kajiwara et al. 2002b). The lactational transfer of these compounds to their calves can explain the lower concentrations of OC residues in mature females. In this study, extremely high OC residues were detected in one of the mature female estuarine dolphin (Figure 2). Since this specimen was so lean and the lipid content was only 5.4%, poor nutritive condition might be stated as one of the causes for its death. The OCs might have been concentrated in the remaining portions of the lipid leading to the extremely high concentration. Additionally, it is assumed that this animal was in the senescence stage and had already started accumulating OCs as observed in males. Although senescence is not very common in marine mammals, Rosas and Monteiro-Filho (2002) have proved that occurs in estuarine dolphins. To understand the accumulation characteristics, percentage compositions of OCs were considered. Figure 4 shows the compositions of DDT and CHL compounds in the blubber of estuarine dolphin, franciscana, Atlantic spotted dolphin, and long-beaked common dolphin from Brazil and Blainville’s beaked whale from Mauritius. Among DDTs, p,p⬘-DDE dominated, indicating its higher persistency in all the cetacean species analyzed. The p,p⬘-DDT in commercial DDT formulations once discharged into the environment degrades to p,p⬘DDE and p,p⬘-DDD, which are stable DDT metabolites. Therefore compositions of DDT compounds are useful to estimate the novel environmental input/recent usage of DDT (Aguilar 1984). In this study, the percentage of p,p⬘-DDT in Blainville’s beaked whales was higher than those in Brazilian dolphins, implying recent usage of technical DDT around Mauritius. Moreover, differences of diet preferences and metabolic capacity are able to affect OC residue patterns in animal bodies. Among CHLs, trans-nonachlor was prominent in all the blubber samples of cetaceans from Brazil and Mauritius. Nakata et al. (1995) compiled the percentage composition of CHLs residues in various biotas and showed that the higher trophic organisms retained a higher percentage of transnonachlor with some exceptions, like Baikal seals (Phoca sibirica), which had a higher proportion of oxychlordane. The elevated percentage of oxychlordane observed in franciscana in this study indicates its higher metabolic capacity to decompose or transform chlordane compounds, higher than that of other species. It is well known that cetaceans generally have a lower ability to metabolize persistent OCs compared with other mammals due to the specific mode of the cytochrome P450 enzyme system (Tanabe et al. 1988, 1994a). Considering these facts, it can be stated that the differences in metabolic capacity among different aquatic mammals should be evaluated to establish adequate risk assessment of OCs to each species.

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Fig. 2. Organochlorine residue levels with age in male (F) and female (E) estuarine dolphins from Brazilian coastal waters.

Fig. 3. Organochlorine residue levels with age in male (F) and female (E) franciscana from Brazilian coastal waters.

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Fig. 4. Percentage compositions of DDT and CHL compounds in the blubber of estuarine dolphin, franciscana, Atlantic spotted dolphin, and long-beaked common dolphin from Brazil and Blainville’s beaked whale from Mauritius. c-CA, cis-chlordane; t-nona, trans-nonachlor; c-nona, cis-nonachlor; Oxy, oxychlordane.

Fig. 5. Comparison of mean concentrations of PCBs and DDTs in the blubber of small cetaceans (mature males) from various regions. [1] This study, [2] dusky dolphin (de Kock et al. 1994), [3] beluga (Muir et al. 1996), [4] bottlenose dolphin (Corsolini et al. 1995), [5] harbor porpoise (Kuiken et al. 1993), [6] harbor porpoise (Karlson et al. 2000), [7] harbor porpoise (Tanabe et al. 1997), [8] humpback dolphin (Prudente et al. 1997), [9] finless porpoise (Minh et al. 1999), [10] finless porpoise (Japan Environmental Agency 1999), and [11] harbor porpoise (Tanabe et al. 1997).

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Fig. 6. Comparison of mean concentrations of CHLs, HCB, and HCHs in the blubber of small cetaceans (mature males) from various regions. [1] This study, [2] dusky dolphin (de Kock et al. 1994), [3] beluga (Muir et al. 1996), [4] harbor porpoise (Kuiken et al. 1993), [5] harbor porpoise (Tanabe et al. 1997), [6] humpback dolphin (Prudente et al. 1997), [7] finless porpoise (Minh et al. 1999), [8] finless porpoise (Japan Environmental Agency 1999), and [9] harbor porpoise (Tanabe et al. 1997). (#) No data available.

Southern Hemisphere vs. Northern Hemisphere Since the sample sizes of franciscana and estuarine dolphins were large enough, the OC residue levels found in mature males of these two species were compared with those reported in coastal odontoceti species from other parts of the world. Unexpectedly, contamination by PCBs and DDTs in estuarine dolphins was comparable to that in animals from most locations except highly industrialized areas such as the Mediterranean Sea (Corsolini et al. 1995), the Atlantic coast of Canada (Muir et al. 1996), and Japanese coastal waters (Japan Environmental Agency 1999) (Figure 5). In comparison to industrialized countries, Paumgartten et al. (2000) observed lower levels of PCBs and HCB in a pooled sample of human breast milk collected from 40 mothers living in the urban area of Rio de Janeiro (Brazil) in 1992. However, results on the Brazilian dolphins in this study indicate a contrasting picture, possibly due to the existence of highly polluted areas in the Southern Hemisphere comparable to the northern developed countries. On the other hand, contamination levels of CHLs, HCB, HCHs, dieldrin, and heptachlor epoxide in the Brazilian dolphins were generally lower than in the Northern Hemisphere species (Figures 6 and 7), suggesting less contamination by these OCs in the Brazilian coastal waters. Contrary to our present observation, the residue level of HCHs in a pooled sample of human breast milk

collected in Brazil was higher than that of PCBs (Paumgartten et al. 2000). Since data on the environmental occurrence of TCPMe and TCPMOH are limited, comparison of pollution status was difficult. However, TCPMe and TCPMOH residue levels in Brazilian cetaceans were almost comparable to those in some species from the Northern Hemisphere (Figure 8), indicating widespread contamination by these compounds in the marine ecosystem including both the hemispheres. Contamination of OCs in the Southern Hemisphere has been considered to be lesser than in the Northern Hemisphere because of higher usage of OCs in the north. For example, according to the estimates by Breivik et al. (2002), almost 97% of the global historical usage of PCBs occurred in the Northern Hemisphere. Studies examining minke whale and albatross showed a clear difference of OCs residue levels between the Northern and the Southern Hemisphere (Aono et al. 1997; Guruge et al. 2001). Even based on a small sample size, OCs residues found in Blainville’s beaked whales in this study were also apparently lower than those in the animal stranded in the United Kingdom, one of the most industrialized countries in the Northern Hemisphere (Law et al. 1997). However, the present study revealed the existence of highly polluted areas by certain OC contaminants in the Southern Hemisphere, such as southern Brazilian coastal regions, comparable to the northern industrialized areas. High OC contamination in mussels from the coastal waters of Brazil and Argentina (Sericano et al. 1995) may


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Fig. 7. Comparison of mean concentrations of heptachlor epoxide and dieldrin in the blubber of small cetaceans (mature males) from various regions. [1] This study, [2] harbor porpoise (Jarman et al. 1996)*, [3] bottlenose dolphin (Kuehl et al. 1991), [4] beluga (Muir et al. 1996), [5] harbor porpoise (Kleivane et al. 1995), [6] harbor porpoise (Kuiken et al. 1993), [7] bottlenose dolphin (Cockcroft et al. 1989)**, [8] Ganges river dolphin (Kannan et al. 1993)*, and [9] finless porpoise (Japan Environmental Agency 1999). (#) No data available. *Including immature males; **wet wt basis.

partly support the specific accumulation of OCs in Brazilian dolphins. Furthermore, Guruge et al. (2001) reported relatively high OC concentrations in royal albatrosses (Diomedea epomophora), which mainly inhabit Australian/New Zealand waters. Time-related trends of OC residues in minke whale from both hemispheres suggest that OC levels were declining in the Northern Hemisphere, but those in the Southern Hemisphere were slightly increasing (Aono et al. 1997). Considering all these facts, it is suggested that further investigations should be conducted, particularly on the analysis of highly toxic OCs such as coplanar PCBs, polychlorinated dibenzo-p-dioxins (PCDDs), and dibenzofurans (PCDFs) as well as polybrominated flame retardants and organotins accumulated in Brazilian species to elucidate the contamination status in the Southern Hemisphere.

Specific Accumulation of TCPMe and TCPMOH Although pollution sources of TCPMe and TCPMOH are still unclear, they have been considered as the impurities in technical

pesticide preparations such as DDT (Buser 1995) and dicofol (de Boer 1997), as well as synthetic high polymer and dye products (Jarman et al. 1992). Regarding the toxicity of these compounds, recent in vivo and in vitro studies have shown their endocrine disrupting effects (Foster et al. 1999; Lascombe et al. 2000). In the present study, significant correlations of TCPMe and TCPMOH with PCBs and DDTs were found in cetaceans from Brazilian coastal waters (Fig. 9). These results indicate the highly bioaccumulative nature of TCPMe and TCPMOH, which were comparable to PCBs and DDTs. Watanabe et al. (1999) reported the comparable biomagnification factors (BMFs) of TCPMe (logBMF ⫽ 2.3), TCPMOH (logBMF ⫽ 2.4), and DDTs (logBMF ⫽ 2.4) by calculating from their results on the levels of these compounds in Caspian seals (Phoca caspica) from Russia and largha seals (Phoca largha) from northwestern Japan. Furthermore, the significant correlations between DDT and TCPMe/TCPMOH concentrations found in this study may suggest that technical DDT is the possible source for these compounds, although it might not be the only one.

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Fig. 8. Comparison of mean concentrations of TCPMe and TCPMOH in the blubber of small cetaceans (mature males) from various regions. [1] This study, [2] beluga (Lebeuf et al. 2001), [3] harbor porpoise (de Boer et al. 1996), [4] harbor porpoise (Falandysz et al. 1999)*, [5] spinner dolphin (Minh et al. 2000), [6] finless porpoise (Minh et al. 2000), [7] spinner dolphin (Minh et al. 2000), [8] killer whale (Watanabe et al. 1999), and [9] harbor porpoise (Minh et al. 2000). (#) No data available. *Including female samples.

Fig. 9. Relationship between concentrations of TCPMe and DDTs in the blubber of estuarine dolphin and franciscana.

Acknowledgments. The authors wish to express their gratitude to Ms. K. R. Moothien Pillay (Albion Fisheries Research Centre, Mauritius) and Dr. Hiroaki Terashima (JICA, c/o Albion Fisheries Research

Centre, Mauritius) for collecting Blainville’s beaked whale samples in Mauritius. This study was supported by a fund from “UK–Japan Research Cooperation on Endocrine Disrupting Chemicals,” Japanese


Ministry of the Environment, and partly by a Grant-in-Aid for Scientific Research (A) (Project No. 12308030) and (B) (Project No. 13480170) from the Japan Society for the Promotion of Science and for Scientific Research on Priority Areas (A) (Project No. 13027101) and the “21st Century COE Program” from the Japanese Ministry of Education, Culture, Sports, Science and Technology.

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