e n v i r o n m e n t a l t o x i c o l o g y a n d p h a r m a c o l o g y 3 8 ( 2 0 1 4 ) 469–479

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevier.com/locate/etap

Organochlorine contaminants in tissues of common bottlenose dolphins Tursiops truncatus from the northeastern part of the Adriatic Sea S. Herceg Romani´c a , D. Holcer b,c , B. Lazar d,e,f , D. Klinˇci´c a,∗ , P. Mackelworth c , C.M. Fortuna c,g a

Biochemistry and Organic Analytical Chemistry Unit, Institute for Medical Research and Occupational Health, Ksaverska cesta 2, HR-10001 Zagreb, Croatia b Department of Zoology, Croatian Natural History Museum, Demetrova 1, HR-10000 Zagreb, Croatia c Blue World Institute of Marine Research and Conservation, Kaˇstel 24, HR-51551 Veli Loˇsinj, Croatia d Department of Biodiversity, Faculty of Mathematics, Natural Sciences and Information Technologies, University of Primorska, Glagoljaska 8, SI-6000 Koper, Slovenia e Institute for Biodiversity Studies, Science and Research Center, University of Primorska, Garibaldijeva 1, SI-6000 Koper, Slovenia f Marine Sciences Program, University of Pula, Zagrebaˇcka 30, HR-52100 Pula, Croatia g Italian National Institute for Environmental Protection and Research, via di Casalotti 300, 00166 Roma, Italy

a r t i c l e

i n f o

a b s t r a c t

Article history:

Levels of 24 organochlorine compounds, including toxic mono-ortho PCB congeners, were

Received 25 February 2014

determined in the organs and tissues (blubber, kidney, lung, muscle, liver, heart) of 13 com-

Received in revised form

mon bottlenose dolphins (Tursiops truncatus) stranded between 2000 and 2005 in the northern

24 July 2014

part of the Croatian territorial waters of the Adriatic Sea. Polychlorinated biphenyls (PCBs)

Accepted 25 July 2014

were found at higher concentrations in comparison with organochlorine pesticides (OCPs)

Available online 4 August 2014

in all of the analyzed tissues. Sums of six indicator congeners (6PCB) constituted around 50% of the total PCB amount, while PCB-153 and PCB-138 were found to have the high-

Keywords:

est concentrations. Among the seven investigated OCPs, p,p -DDE was found at the highest

Common bottlenose dolphin

concentrations.

Marine mammals

In blubber, mean values of 22,048 and 11,310 ng g−1 wet weight were determined for PCB

Organochlorine pollutants

and DDT, respectively. Much lower concentrations were found in muscle samples, followed

Adriatic Sea

by similar concentrations in kidneys, liver and heart, while the lowest levels of organochlo-

Mediterranean Sea

rine contaminants were found in lungs. The results indicate that p,p -DDT is still being introduced in the Mediterranean region. PCB concentrations are among the highest found in this region and toxicological assessments indicate that the health of this specie is at high risk. © 2014 Elsevier B.V. All rights reserved.



Corresponding author. Tel.: +385 1 4682 554. ˇ c). ´ E-mail addresses: [email protected], [email protected] (D. Klinci

http://dx.doi.org/10.1016/j.etap.2014.07.017 1382-6689/© 2014 Elsevier B.V. All rights reserved.

470

1.

e n v i r o n m e n t a l t o x i c o l o g y a n d p h a r m a c o l o g y 3 8 ( 2 0 1 4 ) 469–479

Introduction

Polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) are synthetic organochlorine compounds (OCs) extensively used for industrial, agriculture, and public health purposes. Their production and usage began after World War II, but due to concerns about their high persistency and toxicity for humans and wildlife, many developed countries prohibited their further production and usage during the 1970s and 1980s. Their properties, which include lipophility, chemical stability, and strong bioaccumulative nature enable them to bioaccumulate and biomagnify in the marine food chain. Therefore marine mammals, top predators in the marine environment, can have extremely high levels of organochlorines, and are most vulnerable to their toxic effects. In addition, dolphins have a long lifespan, as well as a low capacity to decompose these toxicants (Tanabe, 2002), which makes them accumulate organochlorines in large amounts, particularly in their hypodermic fatty tissue – blubber. Organochlorine compounds have a number of adverse effects on the marine mammal population, such as reproductive impairment and suppression of the immune system (Aguilar et al., 2002), which can have long-term consequences for population viability. The toxic equivalent (TEQ) approach was developed to simplify the toxicity assessment of compounds that show properties similar to 2,3,7,8-tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD). The toxic equivalent factor (TEF) was assigned to coplanar PCBs: non- and mono-ortho PCB congeners. Probably due to the semi-enclosed nature of the Mediterranean Sea and its surroundings comprising countries with intense industrial and agricultural activity, Aguilar et al., 2002 found high levels of organochlorines in Mediterranean cetaceans. Furthermore, it has been suggested that high PCB concentrations found in the tissues of dead Mediterranean striped dolphins enhanced their mortality rates which skyrocketed during the last decades due to morbillivirus infections (Aguilar and Borrell, 1994; Kannan et al., 1993). Several studies published the levels of OC contaminants in cetaceans stranded along the western part of the Adriatic Sea (Storelli and Marcotrigiano, 2000a, 2003; Storelli et al., 2007; Marsili and Focardi, 1997), while the data for the eastern Adriatic coast are scarce and refer to the levels of OC contamination in tissues of one short-beaked common dolphin (Lazar et al., 2012). Because of the lack of scientific data that present PCB and organochlorine pesticide levels in dolphins stranded along the northeastern Adriatic Sea coast, in the territorial waters of Croatia, the aim of this study was to investigate organochlorine levels in different tissues of common bottlenose dolphins (Tursiops truncatus). Furthermore, congener specific analysis of toxic mono-ortho PCB congeners allowed for a toxicological risk assessment. This paper presents the first detailed analysis of organochlorines in common bottlenose dolphins in the Adriatic Sea and provides an insight into new data on the exposure of Mediterranean cetaceans to organochlorine contamination. The comparison of OC levels measured in this study with those previously reported allowed us to draw conclusions on the specific organochlorine accumulation in the dolphins analyzed.

2.

Materials and methods

2.1.

Study area and sampling

Common bottlenose dolphins (T. truncatus) were found stranded at different locations in the northeast of the Adriatic Sea (Fig. 1) between 2000 and 2005. The animals were in different states of decomposition from fresh to poor, which should be considered when discussing the actual OC burden and particularly the ratio between certain compounds (Borrell and Aguilar, 1990). A total of 13 individual dolphin specimens were collected. The animals were dissected, and organ and tissue samples (blubber, muscle, kidney, lung, heart, and liver) were wrapped in aluminum foil and kept at -20 ◦ C pending chemical analysis. Biometric data of the specimens analyzed are given in Table 1.

2.2.

Chemical analysis

Tissue samples were analyzed using a procedure similar to Storelli et al. (2012). Samples (about 1 g) were grinded with 2 g of sodium sulfate in a glass mortar. Mixture was extracted with 40 mL of n-hexane as an extraction agent and mixed until homogenous according to procedure in Storelli et al. (2012) and Erney (1983). The mixture was quantitatively passed through filter paper (Whatman No. 1). The extracts were concentrated under a gentle stream of nitrogen. Tissue lipid content was determined gravimetrically. The lipid extracts were dissolved in 5 mL of n-hexane and cleaned up with 4 mL of 96% sulfuric acid. The clean-up was repeated two more times. The solvent was evaporated to residues under a gentle stream of nitrogen. Before gas chromatography, the residues were dissolved in 1.0 mL of n-hexane. The following compounds were analyzed: 17 PCB congeners (numbered according to IUPAC): PCB-28, PCB-52, PCB-101, PCB-138, PCB-153, and PCB-180 (six indicator PCB congeners), PCB-105, PCB-114, PCB-118, PCB-123, PCB-156, PCB-157, PCB-167, and PCB-189 (eight toxic mono-ortho PCB congeners), and PCB-60, PCB-74, and PCB-170; and OCPs hexachlorobenzene (HCB), ␣-, ␤, ␥-hexachlorocyclohexanes (␣-HCH, ␤-HCH, ␥-HCH), (p,p -DDE), 1,1-dichloro-2,2-di(4-chlorophenyl)ethylene  1,1-dichloro-2,2-di(4-chlorophenyl)ethane (p,p -DDD), and 1,1,1-trichloro-2,2-di(4-chlorophenyl)ethane (p,p -DDT). For high resolution gas chromatography with electron capture detector(s) (HRGC/ECD), we used “ATI UNICAM” 610 SERIES chromatographs with 63 Ni detectors. The compounds were analyzed simultaneously on two capillary columns (“Supelco”, Bellefonte, USA): (1) 60 m × 0.25 mm, SPB-5 film thickness 0.25 ␮m, temperature program 100 ◦ C, then 4 ◦ C min−1 up to 240 ◦ C, 50 min isothermally; and (2) 30 m × 0.25 mm, SPB-1701 film thickness 0.25 ␮m, temperature program 110 ◦ C, then 4 ◦ C min−1 up to 240 ◦ C, 50 min isothermally. The carrier gas was nitrogen. The injector and detector temperature were 250 ◦ C and 270 ◦ C, respectively, and the volume of the injected sample was 5 ␮L. Only compounds identified on both columns were evaluated. Qualitative and quantitative analyses were done by comparison with the external standard.

e n v i r o n m e n t a l t o x i c o l o g y a n d p h a r m a c o l o g y 3 8 ( 2 0 1 4 ) 469–479

471

Fig. 1 – Sampling area in the northern part of the Adriatic Sea (bold square).

Method recovery and reproducibility were determined by adding a known amount of all of the analyzed compounds (at levels between 2.4 and 22.2 ng g−1 wet weight (ww) for OCPs; at levels between 14 and 20.2 ng g−1 ww for PCBs) to five aliquots of homogenized samples before extraction (method of additions). The recoveries of PCBs and OCPs were

calculated after subtracting the mean levels of two nonfortified subsamples from the fortified ones. The recoveries for the PCBs ranged from 79% to 91%, with a relative standard deviation from 9% to 15%. OCP recoveries ranged from 73% to 86%, with a relative standard deviation from 13% to 19%.

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Table 1 – Biometric data of the analyzed bottlenose dolphins. Sample no.

Sex

Length (cm)

Growth stage

Decomposition state

Sampling year

Tissues analyzed

1 2 3 4 5 6 7 8 9 10 11a 12 13

– F – F M M F M M M F F M

– 176 100 270 187 305 240 210 258 305 – 285 260

Adult Calf New-born Adult Calf Adult Adult Juvenile Adult Adult – Adult Adult

Poor Poor Poor Medium Fresh Medium Good Poor Fresh Medium – Fresh Fresh

2000 2001 2003 2003 2005 2005 2004 2004 2004 2005 2001 2001 2004

M, B B M, B, H, Li M, B M, B, H, Li, Lu, K M, B, H, Li, Lu, K M, B, H, Li, Lu, K M, B, H, Li, K M, B, H, Li, Lu, K M, B, H, Li, Lu, K M, B, Li M, B, Li, Lu M, B, H, Li, Lu, K

M – muscle, B – blubber, H – heart, Li – liver, Lu – lung, K – kidney. – unknown. a Not considered for statistics.

The detection limits (LOD) for PCBs and OCPs were 0.3 ng g−1 and 0.1 ng g−1 ww, respectively, and were calculated as the average of all determinations based on signal-to-noise ratio and recovery of compounds. A blank reagent was used to show laboratory contamination, and the concentration of analytes was below the detection limit. The results were recalculated by recovery.

2.3.

Statistics

We tested the distribution of data with the Kolmogorov–Smirnov test. As the OC concentrations were not normally distributed (all p < 0.05), only nonparametric statistics were applied. However, we also summarized our data as arithmetic mean ± standard deviation (SD) so that we could compare our results with the relevant literature. We separately summarized the concentrations of six indicator PCB congeners (6PCB = PCB-28 + PCB-52 + PCB-101 + PCB138 + PCB-153 + PCB-180) based on their dominant presence in the environment and tissues. For the total number of PCBs (PCB), we considered the sum of all 17 PCB congeners analyzed; total HCHs (HCH) comprised the sum of ␣-, ␤-, and ␥-HCH, while total DDTs (DDT) included the sum of concentrations of p,p -DDE, p,p -DDD and p,p -DDT. In cases where OC levels were below LOD we conservatively used zero concentration values (0.00) in statistical analyses in order to minimize the possible overestimation of OC burdens. Relations between tissue lipid contents and OC levels were tested by Spearman correlation. The differences in OC levels between sexes were tested using the Mann–Whitney test. In order to test for differences in OC levels between sampled tissues and the existence of growth-related changes in OC accumulation we used the Kruskal–Wallis test with post hoc Bonferroni correction applied where appropriate. Due to the small sample size, for the latter we pooled animals only in two life-stage groups: immature dolphins (new-born, calves and juvenile, N = 4) and adults (N = 8). All statistical tests were performed on the basis of wet weight, using the SPSS 17.0 for Windows software (SPSS Inc., Chicago, IL, USA).

3.

Results and discussion

3.1.

PCBs and OCPs

All of the investigated compounds were found in all samples, except for ␣-HCH and ␥-HCH, which were not found in one blubber sample. In one muscle sample, ␣-HCH could not be determined due to sample contamination. In general, the organochlorine compound distribution in all of the tissues followed this order: PCB » DDT > HCH » HCB, with only a few exceptions such as: HCH > DDT (Table 2). This profile led to a PCB/DDT ratio higher than 1 in all of the samples (range 1.1–9.7) indicating that PCBs are still present in this region at higher concentrations than p,p DDT and its metabolites. This indicates that, although PCBs and p,p -DDT use was banned approximately at the same time, PCBs are more stable and decompose at a much slower rate than DDTs. PCB/DDT ratios ranged from 1.3 in blubber to 5.9 in muscles in adult male short-beaked common dolphin (Delphinus delphis), found also in the northern part of the Adriatic Sea (Lazar et al., 2012). Borrell and Aguilar (2007) showed a decrease of DDT levels in the western Mediterranean coast by a factor of 23.7 during a 25-year period, while PCBs only decreased by a factor of 6.1. Wafo et al. (2005) found an extremely high PCB/DDT ratio (17.5) in dolphins from the Mediterranean littoral environment of France.

3.2.

Levels and profiles of OCPs

Among organochlorine pesticides, the lowest concentrations were most frequently recorded for ␣-HCH and HCB, while ␤HCH and p,p -DDE were found at the highest concentrations (Table 2). In the DDT group, compounds are distributed as follows: p,p -DDE > p,p -DDT > p,p -DDD, with a few exceptions: p,p -DDT concentrations exceed or are similar to p,p -DDE concentrations. p,p -DDE is the main p,p -DDT metabolite and is very persistent. The p,p -DDE percentage, a common indicator of p,p -DDT degradation and therefore of the contaminant

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Table 2 – Organochlorine contaminant concentrations (ng g−1 wet weight) in tissues of bottlenose dolphins from the northern part of the Adriatic Sea. Compound

Blubber (n = 13)

Liver (n = 10)

Kidney (n = 7)

Mean ± SD

Median

Min–max

Mean ± SD

33 ± 20

43

1.8–56

3±6

Polychlorinated biphenyls 90 ± 87 48 PCB-28 260 ± 251 PCB-52 236 PCB-101 667 ± 655 456 4013 ± 4751 2762 PCB-138 9331 ± 11,188 5645 PCB-153 971 ± 1096 552 PCB-180 637 ± 727 553 PCB-60 154 ± 185 73 PCB-74 637 ± 730 467 PCB-105 228 ± 303 169 PCB-114 791 ± 786 542 PCB-118 1550 ± 2109 1258 PCB-123 249 ± 270 215 PCB-156 127 ± 130 87 PCB-157 456 ± 433 323 PCB-167 1136 ± 1219 905 PCB-170 752 ± 2220 PCB-189 101  15,331 ± 17,68810,899 6PCB 22,048 ± 24,33916,904 PCBa PCB 97 ± 133 49

19–316 15–839 30–1940 85–14,935 187–33,407 15–3244 34–2647 12–706 24–2393 5–1130 56–2517 38–8098 10–1001 12–470 20–1530 41–3750 13–8129 391–51,619 704–71,913 2–494

18 ± 7 30 ± 18 20 ± 20 110 ± 121 267 ± 307 38 ± 49 41 ± 50 18 ± 7 24 ± 23 10 ± 5 33 ± 43 44 ± 45 18 ± 22 14 ± 7 29 ± 25 60 ± 61 18 ± 9 484 ± 505 791 ± 783 155 ± 207

17 31 11 46 119 16 18 17 17 9 18 23 11 11 25 39 16 271 480 74

Organochlorine pesticides 79 ± 87 57 HCB ␣-HCH 23 ± 21 16 ␤-HCH 552 ± 1301 152 46 ± 47 24 ␥-HCH  HCH 620 ± 1287 201 p,p -DDE 8400 ± 14,382 2509 p,p -DDD 692 790 ± 757 2121 ± 2564 1061 p,p -DDT  11,310 ± 15,956 6179 DDTa DDT 47 ± 75 23

4–306 0.0–78 23–4859 0.0–156 33–4859 67–44,473 31–2399 90–9232 187–51,058 0.4–279

9 ± 14 6 ± 3.8 48 ± 34 15 ± 9 70 ± 36 107 ± 106 31 ± 48 46 ± 48 183 ± 185 29 ± 35

5 5 41 14 72 51 14 27 92 19

% Lipid

Compound

Lung (n = 7) Mean ± SD

% Lipid

0.4 ± 0.2

Polychlorinated biphenyls 22 ± 27 PCB-28 43 ± 58 PCB-52 12 ± 6 PCB-101 51 ± 37 PCB-138 120 ± 91 PCB-153 13 ± 9 PCB-180 20 ± 11 PCB-60 15 ± 12 PCB-74 14 ± 5 PCB-105 9±4 PCB-114 14 ± 5 PCB-118 22 ± 11 PCB-123 12 ± 4 PCB-156 14 ± 5 PCB-157 20 ± 6 PCB-167 26 ± 10 PCB-170 15 ± 4 PCB-189  6PCB 262 ± 216  442 ± 267 PCBa PCB 286 ± 488

Median 1.0

Min–max

Mean ± SD

0.1–19

0.5 ± 0.5

9–28 9–60 6–67 11–345 16–922 4–152 5–134 9–30 7–83 4–21 5–149 5–133 6–78 5–26 8–91 10–176 5–41 63–1544 167–2504 4–676

19 ± 14 33 ± 20 15 ± 15 98 ± 157 246 ± 403 29 ± 50 34 ± 50 14 ± 11 17 ± 17 10 ± 6 15 ± 13 41 ± 56 11 ± 9 14 ± 13 38 ± 42 47 ± 66 15 ± 8 440 ± 640 696 ± 890 666 ± 1361

1.5–48 2.8–14 15–118 3.2–31 21–141 8–266 8–164 9–167 27–595 1–118

3.5 ± 2.1 4.6 ± 2.7 57 ± 46 9.5 ± 4.7 71 ± 51 146 ± 293 16 ± 16 35 ± 24 197 ± 328 216 ± 492

Muscle (n = 12) Median 0.5

13 20 13 56 130 14 17 10 14 9 14 23 10 13 18 23 16 232 391 92

Min–max

Mean ± SD

0.0–0.7

2.6 ± 6.6

3.5–81 8–168 5–21 9–120 17–282 4–24 7–38 5–36 7–21 4–15 8–23 9–39 6–17 5–19 12–28 14–43 9–19 57–688 193–964 37–1383

17 ± 15 27 ± 23 38 ± 77 211 ± 505 479 ± 1186 35 ± 67 53 ± 130 13 ± 11 34 ± 63 9±7 60 ± 132 72 ± 158 24 ± 51 13 ± 14 40 ± 80 31 ± 32 16 ± 14 806 ± 1851 1171 ± 2513 179 ± 185

Median 0.1

19 35 8 24 59 10 10 11 12 10 12 20 9 13 15 23 15 204 365 209

Min–max 0.0–1.1

0.6–44 1.1–59 2.6–43 9–437 18–1122 2.4–141 6–137 0.7–30 1.2–52 0.3–18 3.0–41 3.2–162 0.7–28 0.5–40 1.9–117 3.5–193 0.7–26 41–1825 63–2621 29–3744

3.7 5.4 49 11 64 19 9.2 28 72 39

0.6–6 0.5–9 3.0–121 1.4–15 4.8–137 10–804 2.1–51 5–76 17–931 8–1330

Median

Min–max

Heart (n = 8)

Median 0.3

14 23 9 47 97 10 10 12 14 8 13 24 6 9 15 21 13 240 413 122

Min–max

Mean ± SD

0.0–23

0.5 ± 0.6

0.9–63 0.7–87 2.0–274 2.5–1797 6–4211 1.4–237 1.5–462 0.4–40 1.0–227 1.6–30 2.9–467 4–568 0.7–185 0.3–52 1.2–288 2.9–122 0.3–56 22–6621 42–9031 20–557

22 ± 26 27 ± 21 13 ± 14 95 ± 161 207 ± 352 25 ± 40 38 ± 50 12 ± 10 17 ± 19 9±7 16 ± 18 31 ± 43 12 ± 12 14 ± 10 20 ± 22 43 ± 59 45 ± 85 389 ± 600 645 ± 833 578 ± 873

0.1

14 22 5 14 34 4 10 9 9 6 7 10 7 12 12 15 17 78 253 305

0.0–1.5

1.4–82 1.8–54 3.3–38 4.8–424 10–950 1.7–95 4.2–135 2.2–32 3.5–56 2.4–21 4.7–52 5.1–106 2.5–37 3.5–31 3.4–56 7–140 4.1–254 58–1634 110–2303 9–2661

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Table 2 – (Continued). Compound

Lung (n = 7) Mean ± SD

Organochlorine pesticides 3.5 ± 1.1 HCB 5.4 ± 3.7 ␣-HCH 50 ± 29 ␤-HCH 12 ± 9 ␥-HCH  HCH 68 ± 28 p,p -DDE 57 ± 69 13 ± 7 p,p -DDD 19 ± 9 p,p -DDT  89 ± 78 DDTa DDT 54 ± 93 a

Muscle (n = 12) Median 3.5 4.1 48 7 75 41 10 20 79 17

Min–max

Mean ± SD

2.0–5.0 1.0–13 18–95 3.8–28 26–102 7–207 7–26 6–32 20–254 6–262

8 ± 13 6.1 ± 3.3 42 ± 37 10 ± 10 58 ± 40 275 ± 765 51 ± 99 69 ± 125 395 ± 981 38 ± 36

Heart (n = 8)

Median 2.9 5.9 27 7 45 42 11 28 82 31

Min–max

Mean ± SD

0.2–46 0.1–12 0.8–143 0.5–33 1.3–150 3.1–2696 1.9–342 2.5–445 10–3483 4–137

4.0 ± 4.0 5.5 ± 4.7 52 ± 61 6.5 ± 4.6 64 ± 69 136 ± 283 14 ± 16 27 ± 29 177 ± 319 113 ± 172

Median 1.9 3.1 28 5.2 34 13 5.9 13 35 51

Min–max 0.7–11 0.9–13 5.7–165 1.4–14 8–192 6–816 3.5–41 5.3–72 15–929 1–517

mg kg−1 lipid weight.

“age”, increased in the western Mediterranean from about 65% in 1987 to 82% in 2002 (Aguilar and Borrell, 2005). p,p DDE/DDT ratios reported in the literature range from 0.7 (Marsili and Focardi, 1997; Wafo et al., 2005) to 0.9 (ShohamFrider et al., 2009). In the present study p,p -DDE/DDT ratios ranged from 0.2 to 0.9 (median 0.5). The median value for p,p -DDE/DDT ratios was lower than any reported value in recent years and was below 0.6, which is regarded as the critical threshold (Aguilar, 1984). In a recent paper on a common dolphin from the northern Adriatic, the calculated DDE/DDT ratios in various tissues were also close to the threshold value; between 0.5 and 0.7 (Lazar et al., 2012). We can assume that further p,p -DDT contamination in the Adriatic region is possible considering that UNEP reported (UNEP, 2002) that p,p -DDT is still in use in some Mediterranean countries and is also an intermediate in the production of dicofol. Borrell and Aguilar (1990) found a significant increase in DDE/DDT ratios with time in the blubber of a fresh dolphin carcass left in outdoor conditions for 55 days. Although direct comparison was not possible due to different age of the dolphins analyzed in our work, the mean DDE/DDT ratio found in the blubber of four fresh dolphin carcasses was higher (0.63) than the ratio found in the blubber of dolphins in a state of poor decomposition (0.44). A probable reason for this discrepancy is that, out of the four animals found in a poor stage of decomposition, only one was adult, while among the carcasses found in fresh state, three were adults (assumed to contain larger amounts of OC contaminants). The ␣-HCH/␥-HCH ratio is often used as an indicator of a fresh lindane input (99% ␥-HCH) or a technical mixture of HCHs (64% ␣-, 10% ␤-, 13% ␥-, 9% ␦-, and 1% ␧-HCH) in the environment. ␣-HCH/␥-HCH ratios (range 0.12–2.3) in this study were below 1 in 84% of all analyzed samples, which points to a recent lindane input. Only two recent papers have reported specific HCHs isomer concentrations in dolphin blubber. Stockin et al. (2007) reported very low levels; in only three samples, levels of both ␣-HCH and ␥-HCH were above the quantification limit and the ␣-HCH/␥-HCH ratios were lower than 1. Contradictory results were reported by Weisbrod et al. (2001) in the blubber of dolphins from the northwestern part of the Atlantic. They detected ␣-HCH, ␤-HCH, and ␥-HCH at concentrations of 162, 29.7, and 30.2 ng g−1 fresh weight. These

results show a greater contribution of technical mixtures to HCH contamination. Our work reports much higher ␤-HCH concentrations, but also considerably lower ␣-HCH levels in blubber.

3.3. levels

Polychlorinated biphenyl congener profile and

Fig. 2 illustrates the distribution of PCB congeners in different tissues based on the number of chlorine atoms bound on two phenyl rings. It is evident that the distribution follows this scheme in all of the tissues: hexachloro-  pentachloro> heptachloro- > tetrachloro- > trichlorobiphenyls. An identical domination of higher chlorinated homologues in the PCB profile was found in dolphins from other parts of the Mediterranean (Marsili and Focardi, 1997; Storelli and Marcotrigiano, 2003; Storelli et al., 2007, 2012; Wafo et al., 2005), indicating that the Mediterranean region is exposed mostly to highly chlorinated PCB formulations. In all of the tissues, the sums of six indicator congeners (6PCB) constituted around 50% of the total PCB amount. The 6PCB/PCB ratio averages were between 0.49 (heart, lung) and 0.65 (blubber). The PCB profile in all of the tissues was dominated by two indicator congeners which are also hexachlorobiphenyls: PCB153 and PCB-138 (Fig. 3 shows the PCB congener distribution in blubber samples). These two PCB congeners are particularly resistant to metabolization by marine mammals (Marsili and Focardi, 1997) and are regularly found at the highest levels among dolphin PCB congeners, most frequently followed by PCB-180 (Marsili and Focardi, 1997; Shoham-Frider et al., 2009; Storelli and Marcotrigiano, 2003; Storelli et al., 2007; Wafo et al., 2005). The same PCB profile was also found in loggerhead sea turtles, Caretta caretta, large marine vertebrates with long lifespans sampled in the Adriatic Sea (Lazar et al., 2011; Storelli and Marcotrigiano, 2000b). Taking only into account indicator PCB congeners, our results reveal a PCB-153 > PCB-138 > PCB-180 profile in blubber and liver. In the lungs, the third most abundant indicator PCB is PCB-52, while PCB-52 and PCB-180 have similar concentrations in the remaining tissues and are both ranked third. In the study of Lailson-Brito et al. (2012), contribution of low-chlorinated PCBs (such as PCB-28 and PCB-52) in Fraser’s

475

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100.0

80.0 3 Cl 60.0

%

4 Cl 5 Cl

40.0

6 Cl 7 Cl

20.0

0.0 blubber

muscle

liver

heart

kidney

lung

Fig. 2 – Percentage of total concentration of each PCB isomer class in the tissues of bottlenose dolphins.

dolphin showed the highest percentage. They found that summed concentrations of di-, tri- and tetra-chlorobiphenyls  PCBs ranged between 17.2% for Fraser’s dolphin and 7.2% to for long-beaked dolphin. Their explanation is a more efficient influence of long range transport of low chlorinated biphenyls from the atmosphere, in association with water column. This could also be the explanation for our findings of PCB-28 and PCB-52 presence in lungs. However, when considering all of the analyzed PCBs (see Table 2), high levels of PCB-123 and PCB-170 can be observed in all of the tissues. While PCB-123 is a toxic mono-ortho PCB, PCB-170 is a di-ortho PCB congener, as are PCB-138, PCB153, and PCB-180, and they do not entail dioxin-like toxicity. According to the available literature, PCB-170 is usually not often analyzed, but the studies of Santos-Neto et al. (2014) and Lailson-Brito et al. (2012) showed their relatively high presence in different delphinids. High levels of this congener and its obvious persistency may represent good grounds for its inclusion in common PCB analyses. Furthermore, considerably high levels of this congener were also found in bluefin ˇ c´ D and tuna (Thunnus thynnus) from the Adriatic Sea (Klinci Herceg Romanic´ S, unpublished data). A comparison of the results presented in Table 2 with data from the literature summarized in Tables 3 and 4 reveals that total PCB concentrations measured in tissue samples in this

study are higher than most recently measured PCB levels in dolphins. Comparable levels were found in adult male common bottlenose dolphins from the US (Yordy et al., 2010) and Italian coastal areas (Marsili and Focardi, 1997) in the species sampled between 1987 and 1993. While Storelli et al. (2007) reported significantly lower total PCB levels in different tissues of common bottlenose dolphins from the coastal waters of the Adriatic and Ionian seas, Storelli et al. (2012) found levels similar to the levels reported in this study in the blubber, kidney, heart, and lung of striped dolphins from south-eastern Mediterranean.

3.3.1.

Toxic PCBs

We analyzed eight mono-ortho substituted PCB congeners that have assigned TEF values and are toxic to animals and humans. They are present at levels of at least one order of magnitude higher than non-ortho congeners (also toxic but not analyzed in this study) and are therefore easier to accurately quantify. According to Ross et al., 2000 mono-ortho PCB congeners in male killer whales attributed to the total sum of toxic PCB congeners (the sum included non- and monoortho PCB congeners) with 94%. Furthermore, all of the toxic PCB congeners contributed to the total TEQ (along with PCBs congeners of polychlorinated-p-dioxins and polychlorinated dibenzofurans) with 97%. In short, TEQ values calculated on

80.0

Contribution to Σ PCB / %

70.0 60.0 50.0 40.0 30.0 20.0 10.0 0.0

Fig. 3 – PCB congener contamination pattern (mean values and standard deviation, on a wet weight basis) in the blubber of bottlenose dolphins.

476

e n v i r o n m e n t a l t o x i c o l o g y a n d p h a r m a c o l o g y 3 8 ( 2 0 1 4 ) 469–479

Table 3 – Sums (mg kg−1 lipid weight) of PCB congener and DDT compound concentrations in dolphin blubber. Location and year of sampling

Specie

N

PCB

DDT

Reference

Israeli Mediterranean coast, 2004–2006 Western Mediterranean 1978–1989 1990–1999 2000–2002 Eastern Italian coast, 1999–2000 Gran Canaria, Spain Sarasota Bay, Florida, 2000–2005

T.t.

5

6.3 ± 2.3a

34.8 ± 59.5a

Shoham-Frider et al., 2009

T.t.

9 18 9

578.6 ± 362.4 209.0 ± 170.9 149.9 ± 77.0

246.9 ± 153.1 91.2 ± 100.8 60.3 ± 55.9

Borrell and Aguilar, 2007

T.t. T.t. T.t.

9 1 16 31

Taiwan coastal waters, 2000–2001 Coastal Georgia, USA, 2004

T.t. T.t.

6 7 6

Italian coasts, 1987–1993 Mediterranean littoral environment (France), 2000–2003 Western Mediterranean, 2002 Southeastern Mediterranean Sea, 1999–2004 SW Mediterranean, 1992–1994

T.t. S.c. and T.t.

8 3

32.7 ± 16.9 11.0a 98.6 ± 159 (adult male) 4.7 ± 5.4 (adult female) 5.4 ± 3.6a 78.6 ± 32.4 (contaminated location) 5.0 ± 6.1 21.7b 70.0 ± 35.5

S.c. S.c.

5 17

S.c. D.d. Delphinus sp. S.g. S.f. D.c.

27 26

L.a.

6

New Zealand, 1999–2005 Brazil, 1997–1999

Northwest Atlantic, 1994–1996

8 1 1

15.6a 51.5 ± 123 1.3 ± 3.1

Storelli and Marcotrigiano, 2003 Jaber et al., 2005 Yordy et al., 2010

Chou et al., 2004 Pulster et al., 2009

6.0b 4.0 ± 2.2

Marsili and Focardi, 1997 Wafo et al., 2005

75.9 ± 16.8 22.0 ± 20.3a

55.1 ± 15.3

Aguilar and Borrell, 2005 Storelli et al., 2012

68 ± 39 30 ± 28 0.6± 0.5a (N = 19) 34 (mature male) 60 (mature male) 17 (mature male) 13.0 ± 7.1a

79 ± 47 31 ± 39 1.3 ± 1.3a (N = 17) 52 48 11

Borrell and Aguilar, 2005

14.0 ± 9.6a

Weisbrod et al., 2001

Stockin et al., 2007 Kajiwara et al., 2004

T.t. – Tursiops truncates, S.c. – Stenella coeruleoalba, D.d. – Delphinus delphis, S.g. – Sotalia guianensis, S.f. – Stenella frontalis, D.c. – Delphinus capensis L.a. – Lagenorhynchus acutus. a Wet weight. b Conversion on wet weight basis was applied based on moisture content in each tissue.

literature. Our mean TEQ value was 267 ng g−1 ww and, an approximately two-fold lower value than that reported by Storelli and Marcotrigiano, 2003 (493 ng g−1 ww). The mean blubber TEQ value on the lipid basis was 1220 pg g−1 lipid weight (lw). This value greatly exceeds the value of 103 pg g−1

800 700

TEQ / pg g-1 wet weight

the basis of mono-ortho PCB congeners present more than 90% of the total toxicity of the mixture of polychlorinated organic contaminants in these cetaceans. Our study reported PCB-156, PCB-123, PCB-114, and PCB-118 as dominant mono-ortho congeners in blubber, while PCB-167 always exhibited the lowest concentration. Toxic equivalents were calculated on the basis of TEF values determined by van den Berg et al. (1998) and are here presented in Fig. 4. Blubber samples had the highest mean TEQ value of 680 pg g−1 ww while other tissues had similar TEQ values ranging from 24 to 41 pg g−1 ww. TEQ values in specific tissues positively correlated with the lipid content in tissue (p < 0.05). In the available studies on dolphins, only three or five mono-ortho congeners have been analyzed in blubber samples: PCB-105, PCB-118, and PCB-156 (Storelli and Marcotrigiano, 2003; Storelli et al., 2007; Storelli et al., 2012), PCB-157 and PCB189 along with the previously mentioned ones (Chou et al., 2004). We calculated TEQ values on the basis of only three monoortho PCB concentrations (105, 118, and 156) in blubber, which allowed for a comparison with the available data in the

680

600 500 400 300 200 100

41

33

28

27

24

heart

kidney

lung

0 blubber

muscle

liver

Fig. 4 – Mean TEQ values in the tissues.

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Table 4 – Sums (mg kg−1 ) of PCB congener and DDT compound concentrations in different dolphin tissues (N; number of samples). Liver

Muscle

Kidney

PCB w.w.

0.053 (N = 1)

0.079 (N = 1)

0.5 ± 0.4 (N = 3)

DDT w.w.

2.8 ± 3.6 (N = 5) 44.7 ± 33.6

0.526 (N = 1)

7.1 (N = 1)

19.9 ± 19.0

39.4 ± 36.5

10.6 (N = 13)

8.2 (N = 12)

1.1 (N = 3)

2.4 (N = 13) 13.6 ± 13.7 (N = 6)

1.5 (N = 12) 11.1 ± 15.7 (N = 4)

0.2 (N = 3) 5.5 ± 4.2 (N = 7)

3.1 ± 1.3 (N = 6)

2.8 (N = 4) 8.8 ± 7.3 (N = 3)

0.8 ± 0.6 (N = 6) 3.6 ± 4.5

0.3 ± 0.3 (N = 4) 0.2 ± 0.5

0.5 ± 0.2 (N = 7) 0.7 ± 0.9

0.3 ± 0.3 (N = 6) 0.6 ± 0.6

0.9 ± 0.7 (N = 3) 0.5 ± 0.5

1.6 (N = 2)

0.5 (N = 2)

1.5 (N = 2)

0.4 (N = 2)

696 ± 890 197 ± 328 666 ± 1361 216 ± 492

442 ± 267 89 ± 78 286 ± 488 54 ± 93

PCB l.w. (N = 12) PCB d.w. DDT d.w. PCB d.w.

DDT d.w. PCB w.w. (N = 17) PCB w.w. DDT w.w. PCB w.w. DDT w.w. PCB l.w. DDT l.w.

0.4 ± 0.3 (N = 6) 0.3 ± 0.3 (N = 6) 791 ± 783 183 ± 185 155 ± 207 29 ± 35

1171 ± 2513 395 ± 981 179 ± 185 38 ± 36

Lung

Heart

16.1 ± 25.7

8.9 (N = 4)

645 ± 833 177 ± 319 578 ± 873 113 ± 172

Location and year of sampling

Specie

Reference

Israeli Mediterranean coast, 2004–2006

T.t.

ShohamFrider et al., 2009

Coastal areas of the Adriatic and Ionian Sea, 2001–2002 Italian coasts, 1987–1993

T.t.

Storelli et al., 2007

T.t.

Marsili and Focardi, 1997

Mediterranean littoral environment (France), 2000–2003

S.c. and T.t.

Wafo et al., 2005

Southeastern Mediterranean, 1999–2004 Northwest Atlantic, 1994–1996

S.c.

Storelli et al., 2012

L.a.

Weisbrod et al., 2001

T.t.

This study

T.t. – Tursiops truncates, S.c. – Stenella coeruleoalba, L.a.– Lagenorhynchus acutus. w.w. – wet weight; l.w. – lipid weight; d.w. – dry weight.

lw reported by Chou et al. (2004) for dolphins from Taiwan coastal waters. The most indicative value of toxic PCB burden in the analyzed dolphins is the mean TEQ in blubber samples (based on all eight mono-ortho substituted PCBs): 2940 pg g−1 lw (range 88–15,184 pg g−1 lw). This value significantly exceeds the toxic threshold value of 255 pg g−1 lipid total TEQ recommended by Ross et al. (2000) based on an immunotoxicological study of pinnipeds and adjustments made on the basis of data for killer whales. The only blubber sample that did not exceed this value was the one from a new-born dolphin. These alarming results indicate serious PCB contamination in dolphins from the investigated area and a possibly grave impact on the health of dolphins.

3.4. PCBs and organochlorine pesticides distribution in dolphin tissues PCB and DDT distribute similarly among tissues. Their levels on wet weight basis decrease in the following order: blubber  muscle > kidney ∼ liver ∼ heart > lung. In the case of HCH and HCB, their distributions between tissues are somewhat different and follow the following order: blubber  muscle > heart > liver ∼ kidney > lung for HCH and blubber  liver ∼ muscle > heart > kidney > lung for HCB. Literature data on organochlorine compound distributions in dolphin tissues from the Mediterranean reveal various patterns, but in general, blubber stands out as the dominant

tissue for organochlorine accumulation, while the lungs are the least affected by OC concentrations. The most obvious difference found in our study was the high level of OC contaminants in muscle tissues. It has been established that the pattern of contaminants is related to the lipid content of various compartments, as well as to the lipid composition of tissues and the polarity of lipid components, which have different selective affinities for these compounds and bind them differently (Marsili and Focardi, 1997). Our study found a positive correlation (p < 0.05) of PCBs and DDTs with the lipid content of specific tissues. The lipid content of blubber was higher than for any other tissue (all p ≤ 0.001), and in comparison with other organs, blubber  accumulated significantly higher concentrations of PCB and  DDT, including the majority of individual PCB congeners (PCB-138, PCB-153, PCB-180, PCB-118, PCB-60, PCB-74, PCB-101, PCB-105, PCB-123, PCB-156, PCB-170) and organochlorine pesticides (HCB, p,p -DDE, p,p -DDD, p,p -DDT) (Kruskal–Wallis, all p < 0.05). Levels of individual organochlorine compounds were positively correlated with tissue lipid contents only in muscles for all compounds except for PCB-28, PCB-52, HCB, ␣-HCH, and ␥-HCH (rs range: 0.715–0.942, all p < 0.05). Significant growthdependent changes in organochlorine accumulation were found only for PCB-28, ␣- and ␥-HCH in blubber and PCB-28 in muscles. Blubber burdens of PCB-28, ␣- and ␥-HCH in immature common bottlenose dolphins (median values: 23.9, 4.9 and 7.3 ng g−1 ww, respectively; N = 4) were significantly lower

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than in adults (median values: 102.4, 25.8 and 42.7 ng g−1 ww, respectively; N = 8, all p < 0.05). The muscle tissue of immature dolphins contained higher levels of PCB-28 (median: 18.6, N = 4) than adults (median: 12.0, N = 8; all p < 0.05). Other OCs showed no differences in accumulation between immature individuals and adults for any of the tissues analyzed. Similarly, no differences were found in the accumulation pattern between sexes for any of the OCs in any of the tissues, regardless of life stage (all p > 0.05). Considering biological factors such as sex or age, organochlorine concentration in cetaceans generally differ. Bioaccumulation starts in fetal life, levels increase in juveniles and decrease in adult females due to lactation whereas in males they increase with age (Storelli et al., 2012). However, some studies present absence of significant differences. Leonel et al. (2010) did not find statistically significant differences in levels between males and females of franciscana dolphin. Among different adults, juveniles and calves, significant differences were only found between adult males and juveniles and calves for PCBs, and between adult females and juveniles for HCB. This discrepancy could be related to contaminant properties and feeding grounds.

4.

Conclusions

Overall, this study revealed a much higher PCB than OCP contamination in the investigated dolphins. While DDT levels did not stand out in comparison with published data, our results show that there is a probable continuation in p,p -DDT input in the Mediterranean region. On the other hand, PCB levels are higher than levels in most published data. According to estimations, concentrations exceeding 50 ␮g g−1 ww of total PCBs in the blubber might present a health risk to cetaceans (Kannan et al., 1993; Storelli and Marcotrigiano, 2003). Total PCB concentrations exceeded this value in only two blubber samples. But, the calculated TEQ values indicate that the health of dolphins from the northeastern Adriatic Sea might be at risk. Furthermore, our reported OC values probably underestimate the values at the time of death, because the bodies of some of the animals studied in this work were found in various stages of decomposition, which undoubtedly lead to a decrease in DDT and PCB concentrations (Borrell and Aguilar, 1990). However, the dolphins with the highest DDT, p,p -DDE and PCB levels in blubber were one adult and one calf found in medium decomposed and fresh state, respectively. The data reported in this work reveal the necessity of serious protective measures for the entire Mediterranean marine ecosystem.

Conflict of interest The authors declare that there are no conflicts of interest.

Transparency document The Transparency document associated with this article can be found in the online version.

Acknowledgements We wish to thank Mrs. Mirjana Kralj for exquisite techniˇ cal assistance during our experimental work, Mrs. Zeljana Pavlakovic´ for language advice, the Blue World Institute team for the assistance in collecting the samples, and the persons who reported the stranded animals.

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Organochlorine contaminants in tissues of common bottlenose dolphins Tursiops truncatus from the northeastern part of the Adriatic Sea.

Levels of 24 organochlorine compounds, including toxic mono-ortho PCB congeners, were determined in the organs and tissues (blubber, kidney, lung, mus...
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