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Persistent organic pollutants in blubber of fin whales (Balaenoptera physalus) from the Southern Ocean
Marine Pollution Bulletin 145 (2019) 148–152
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Baseline
Persistent organic pollutants in blubber of fin whales (Balaenoptera physalus) from the Southern Ocean
T
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Satie Taniguchia, , Fernanda I. Colabuonoa, Luciano Dalla Rosab, Eduardo R. Secchib, Josilene da Silvaa, Daniela A. Maiaa, Rosalinda C. Montonea a b
Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, São Paulo, SP 05508-120, Brazil Instituto de Oceanografia, Universidade Federal do Rio Grande – FURG, Rio Grande, RS 96203-000, Brazil
A R T I C LE I N FO
A B S T R A C T
Keywords: Antartica Fin whale Balaenoptera physalus POPs Organochlorine pesticides Southern Ocean
Persistent organic pollutants (POPs) were analyzed in eighteen blubber samples biopsied from fin whales (Balaenoptera physalus) during the feeding season near the Antarctic Peninsula in the summer of 2013. POP content (in ng g−1 lipid weight) ranged from 46.4 to 708 for polychlorinated biphenyls (∑PCBs), 6.77 to 123 for hexachlorobenzene (HCB), 10.1 to 489 for dichlorodiphenyltrichloroethane and derivatives (∑DDTs), 5.38 to 52.8 for hexachlorocyclohexanes (∑HCH) and < 0.40 to 2.54 for polybrominated diphenyl ethers (∑PBDEs). The presence of those compounds in Southern Ocean fin whales is related to long-range transport and their diet based mainly on euphausiids (krill). Their contents were much lower compared to the same species in other locations, especially in the Northern Hemisphere, presumably due to differences in trophic position and the proximity of POP sources and contamination of prey items.
The fin whale (Balaenoptera physalus) is a pelagic cetacean that inhabits all major oceans and some limited areas, such as the Gulf of California, East China Sea and Mediterranean Sea, but its overall range and distribution is not well known (Jefferson et al., 2008). This whale was once an important target species, with approximately 750,000 individuals killed in the Southern Hemisphere during the whaling period in the 20th century (Clapham and Baker, 2001). In relatively recent decades, several authors have described its presence on the coasts of Chile and Brazil (Pantoja et al., 1984; Zerbini et al., 1997; Pérez et al., 2006). In the Southern Ocean, fin whales have been sighted associated with euphausiids (krill), which are the main prey items of the species (Širović et al., 2004; Santora et al., 2010; Herr et al., 2016). Like any organism in the marine environment, whales are subject to contamination by anthropogenic compounds, such as persistent organic pollutants (POPs), which include organochlorine pesticides (OCP) and polychlorinated biphenyls (PCBs). POPs have been reported in several whale species in Antarctica, such as the humpback whale [Megaptera novaeangliae (Dorneles et al., 2015; Das et al., 2017)], Antarctic minke whale [Balaenoptera bonaerensis (Yasunaga et al., 2015)] and common minke whale [Balaenoptera acutorostrata (Aono et al., 1997)]. However, to our knowledge there are just a few published reports of contaminant levels in fin whales in the Southern Hemisphere (e.g. Yasunaga and Fujise, 2014; Pantoja et al., 1984, 1985).
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To assess POP contents in this species, 18 blubber samples were collected during the feeding season in Bransfield Strait (n = 5 in 2013 and n = 4 in 2015), northern Antarctic Peninsula, and near the Powell Basin (n = 9 in 2013), northwestern Weddell Sea (Fig. 1). Blubber and skin samples were collected from live fin whales by firing a biopsy dart with a crossbow into the dorsal region of the individuals, as previously described by Gauthier et al. (1997). The analytical procedure followed that described by MacLeod et al. (1986) with minor modifications. Briefly, about 0.1 g of the wet tissue was dried with anhydrous sodium sulphate and extracted in Soxhlet apparatus for 8 h using 80 ml of n-hexane and methylene chloride (1:1, v:v). Before extraction, 2,2′,4,5′,6-pentachlorobiphenyl (PCB 103) and 2,2′,3,3′,4,5,5′,6-octachlorobiphenyl (PCB 198) were added to all samples, blanks and reference material as surrogates for OCPs and PCBs. After the determination of extractable lipids by gravimetric analysis in one aliquot, the extracts were cleaned up using column chromatography with 8 g of silica and 16 g of alumina, both 5% waterdeactivated and eluted with 80 ml of n-hexane and methylene chloride (1:1, v:v). To remove excess lipids, the fraction was further purified by high-performance liquid chromatography (HPLC) with two size exclusion columns (300 × 21.2 mm), using methylene chloride as the eluent, with a flow of 5 ml min−1. The internal standard 2,4,5,6-tetrachlorometaxylene (TCMX) was added before gas chromatographic
Corresponding author. E-mail address: [email protected] (S. Taniguchi).
https://doi.org/10.1016/j.marpolbul.2019.05.045 Received 22 March 2019; Received in revised form 9 May 2019; Accepted 20 May 2019 Available online 24 May 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Study area with sampling locations (red dots) of fin whales along the northern Antarctic Peninsula and northwestern Weddell Sea. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
investigated, including the following IUPAC numbers: 8, 18, 28, 31, 33, 44, 49, 52, 56, 60, 66, 70, 74, 77, 81, 87, 95, 97, 99, 101, 105, 110, 114, 118, 123, 126, 128, 132, 138, 141, 149, 151, 153, 156, 157, 158, 167, 169, 170, 174, 177, 180, 183, 187, 189, 194, 195, 199, 203, 206 and 209. The target PBDE congeners included IUPAC numbers 28, 47, 99, 100, 153, 154 and 183. The POP profile found (Table 1) in fin whale blubber (PCBs > HCB > DDTs > HCHs > PBDEs) was very similar to that found in humpbacks whales and fin whales that fed near the Antarctic Peninsula (Dorneles et al., 2015; Yasunaga and Fujise, 2014, respectively), but slightly different from humpbacks feeding in the Indian Ocean sector of Antarctica, in which higher concentrations of HCB (HCB > DDT > PCB > PBDE) have been reported (Das et al., 2017). No marked differences were found between male and female whales collected in Bransfield Strait (Fin 1–9) and Weddell Sea (Fin 10–18). Although the prey items of fin and humpback whales can differ, both feed mainly on krill (Pérez et al., 2006). Santora et al. (2010) found that fin whales were associated with large (> 45 mm) mature krill located offshore, whereas humpback whales were associated with juvenile krill (< 35 mm) in Bransfield Strait. In an aerial survey of Bransfield Strait and the Drake Passage, Herr et al. (2016) found that fin whales fed in an area dominated by Thysanoessa macrura in the Drake Passage, whereas humpback whales were found mostly in areas with a greater biomass of Euphausia superba, in the Bransfield Strait. Some of our samples (Fin 1–9) were obtained in the Bransfield Strait, just south of King George Island and POP contents were similar to that found in specimens collected in Weddell Sea (Fin 10–18). Nemoto (1970) analyzed the stomach contents of 35139 Antarctic fin whales caught from 1961 to 1965 and found mainly euphausiids, which form dense swarms in the sea, unlike the same whale species in the North Pacific, which fed
analysis. A procedural blank was run for every set of ten samples. OCP, PCB and PBDE were quantitatively analyzed in an Agilent Technologies 7890B gas chromatograph with a 7010B triple quadrupole mass spectrometer (GC/MS/MS) using a 30 m × 0.25 mm i.d. capillary column coated with a 5% phenyl-substituted dimethylpolysiloxane phase (film thickness: 0.25 μm). The injected volume was 1 μl in automatic pulsed splitless mode. Helium was used as the carrier gas (constant flow of 1.1 ml min−1). The interface, source and quadrupole temperatures were 300 °C, 300 °C and 150 °C, respectively. The oven temperature was programmed as follows: 75 °C for 3 min, raised at 15 °C min−1 to 150 °C, then raised at 2.0 °C min−1 to 260 °C and at 20 °C min−1 to 300 °C, with a final hold of 10 min. For quality assurance/quality control (QA/QC), the analytical method was validated using a standard reference (SRM 1945 – organics in whale blubber) purchased from the National Institute of Standards and Technology (NIST), USA, which was analyzed in duplicate. The average recovery of analytes (68–114%) was within the range reported (50–120%) in Intergovernamental Oceanographic Commission (IOC) technical series by Wade and Cantillo (1994). The recovery of analytes in spiked blanks (76–109%) and matrices (85–116%) produced satisfactory results. Compounds in laboratory blanks were subtracted from the samples. The limit of quantification (LOQ) for PCBs, POCs and PBDEs was 0.4, 1.0 and 0.1 ng g−1 lipid weight (lw), respectively. The quantification of analytes was based on a nine-level analytical curve and followed the internal standard procedure. Surrogate recoveries were acceptable, with mean ± standard deviation of 87 ± 7. The OCPs analyzed in this study were dichlorodiphenyltrichloroethane and derivatives (o,p′-DDT, p,p′-DDT, o,p′-DDD, p,p′-DDD, o,p′-DDE and p,p′-DDE), hexachlorocyclohexanes (α, β-, δ- and γ-HCH) and hexachlorobenzene (HCB). A suite of 51 PCBs was also 149
Marine Pollution Bulletin 145 (2019) 148–152
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Table 1 Persistent organic pollutant content in fin whale blubber in ng g−1 lipid weight (ng g−1 wet weight). POP
Gender
Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin
F F M F M M – M F M M M M M M M F F
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
ΣPCBs
HCB
ΣDDTs
ΣHCHs
ΣPBDEs
86.1 (42.4) 241 (54.8) 66.1 (25.8) 202 (54.4) 46.4 (19.2) 321 (78.2) 386 (166) 266 (116) 211 (52) 110 (41.3) 89.2 (26.0) 708 (139) 186 (114) 78.7 (42.3) 162 (49.9) 339 (79.1) 560 (274) 222 (31.4)
13.5 (6,62) 123 (28.0) 58.2 (22.7) 39.6 (10.7) 52.2 (21.5) 69.5 (16.9) 58.4 (25.1) 45.4 (19.7) 56.2 (13.9) 29.5 (11.1) 6.77 (1.97) 55.3 (10.9) 35.2 (21.6) 25.5 (13.7) 48.0 (14.8) 51.9 (12.1) 11.6 (5.65) 16.9 (2.38)
15.1 (7.42) 60.8 (13.8) 17.5 (6.83) 10.1 (2.72) 24.8 (10.2) 336 (81.9) 439 (189) 422 (183) 489 (121) 29.1 (10.9) 10.4 (3.04) 85.2 (16.7) 27.0 (16.5) 78.4 (42.2) 21.3 (6.54) 49.5 (11.6) 15.0 (7.34) 20.5 (2.89)
17.1 52.8 11.7 46.1 8.31 13.0 7.80 11.8 13.0 10.7 5.38 39.6 23.7 6.24 10.8 31.9 47.2 21.3
0.64 (0.15) 1.08 (0.53) < 0.40 (< 0.10) 0.41 (0.11) 0.33 (0.14) < 0.40 (< 0.10) < 0.40 (< 0.10) 1.57 (0.65) 1.30 (0.54) 1.26 (0.47) < 0.40 (< 0.10) 2.54 (0.50) 0.95 (0.58) < 0.40 (< 0.10) 0.36 (0.11) 0.80 (0.19) 0.61 (0.30) 0.99 (0.14)
(8.39) (12.0) (4.58) (12.4) (3.43) (3.16) (3.35) (5.14) (3.21) (4.01) (1.57) (7.78) (14.5) (3.36) (3.31) (7.44) (23.1) (3.00)
% lipid 22.7 49.2 39.0 26.9 41.3 24.3 42.9 43.5 24.7 37.6 29.1 19.7 61.2 53.8 30.7 23.3 48.9 14.1
archived blubber samples from fin whales collected in 1971–72 compared to samples collected in 1991 in eastern Canada. Tetrachlorobiphenyls, such as PCB-44, 49 and 52, were predominant in the older samples, whereas the penta-, hexa- and heptachlorobiphenyls, such as PCB-101, 153 and 180, had relatively higher contents in the newer samples. Predominance of heavier compounds can be attributed to the accumulation by biomagnification or because of POP content in the environment and in prey species of the whales. Other chlorinated compounds, such as HCB, DDTs and HCHs, are frequently reported in different organisms in Antarctica, such as penguins (Montone et al., 2016), which also feed mainly on krill. HCB was initially used as a fungicide for seed treatment of grain crops, but later became mainly a by-product in the production of a large number of lower chlorinated compounds (UNEP, 2002a). Taniguchi et al. (2009) and Colabuono et al. (2014) reported that the amounts of HCB in
on similar quantities of euphausiids, large copepods and gregarious fish. Table 2 presents the contents of POPs reported in fin whales blubber sampled worldwide. Marsili and Focardi (1996) and Fossi et al. (2006) reported variable amounts of PCBs in Mediterranean fin whales, which also feed on large amounts of euphausiid species, mainly northern krill (Meganyctiphanes norvegica), among other marine organisms, but the proximity to the sources are likely the main reason for the differences in PCB contents. The predominance of tri-, tetra- and pentachlorinated biphenyls in the present study indicate PCBs coming from long-range transport, unlike that found for the same species in the Mediterranean Sea, in which higher contents of PCBs have been found, with a predominance of heavier congeners, such as hexa- (PCB 138, 149 and 153) and heptachlorinated biphenyls (170, 180 and 187), as described by Fossi et al. (2014). Hobbs et al. (2001) described experiments with
Table 2 Published contents of polychlorinated biphenyls, polybrominated diphenyl ether, organochlorine pesticide in fin whales blubber [ng g−1 lipid (lw) or wet weight (ww)]. Lipid % a
Antarctica North Atlanticb Northern hemisphere Chilean Coastb Chilean Coastb North-western Spain and Icelanda Eastern North Atlantica Eastern North Atlantica Icelanda Durban, South Africanb Mediterranean Sea Italyc Gulf of St Lawrence, Canadaa Eastern Canada - Newfoundlanda Eastern Canada - Nova Scotiaa Eastern Canada - Gulf of St Lawrencea Mediterranean Seab Mediterranean Seaa Mediterranean Sea and Mexicoc Arctic and North Atlantic regionsa Antarcticaa Mediterranean Sea (Italy)a Mediterranean Sea Mediterranean Seaa Sea of Cortez, Mexicoa a b c
14.1–61.2 30
HCB
ΣDDT < 10.1–489
ΣPCB
ΣHCH 5.38 to 52.8 – – – 1.7 – –
< 0.40 to 2.54 – – – – – –
– – – 215 ± 92134–426 121–238 84.7–376 – – – – 0.65 – – – –
– – – – – – – – 806 82–305.06 5–12 (1986/89) 20–31 (2006/09) – – – – –
– – – 77.5 10.8–85.6 – – 4.1–87 4.1–87 – – – – –
6.77–123 – – – – – – – – – – 96 ± 82 114–619 136–334 10–318 39.5 – – –
2.83 54.4 – 1145 483–1981 500–1490 610–850 30–330 3000–6800 3812 ± 3908 1410–8110 5750–32,700 651–13,100 4400 – – –
46.4 to 708 12–185 3.6 – – – 561–2026 770–1820 940–1260 n.d. (Aroclor 1254) 2600–3800 2674 ± 2850 673–2930 1470–10,800 229–10,200 3800 – – –
– – – –
39 129.13–286.26 – 29.9 ± 12 38.5 ± 33.6
13 6580.67–26,833.64 6643 ± 5549 10,477.3 ± 7477.3 3109.9 ± 2245.9
6.5 9117.09–42,778.45 5721 ± 5180 13,327.3 ± 8548.3 8753.8 ± 6542.6
Lipid weight. Wet weight. Dry weight. 150
ΣPBDE
Reference This study Saschenbrecker (1973) Holden (1975) Pantoja et al. (1984) Pantoja et al. (1985) Borrell and Aguilar (1987) Aguilar and Borrell (1988) Aguilar and Borrell (1991) Borrell (1993) Henry and Best (1983) Marsili and Focardi (1996) Gauthier et al. (1997) Hobbs et al. (2001) Hobbs et al. (2001) Hobbs et al. (2001) Fossi et al. (2003) Pettersson et al. (2004) Fossi et al. (2010) Rotander et al. (2012) Yasunaga and Fujise (2014) Fossi et al. (2014) Pinzone et al. (2015) Fossi et al. (2016) Fossi et al. (2016)
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helped collecting samples and data, especially Alexandre Azevedo, Artur Andriolo and Jorge Acevedo. This study was conducted by Projeto Baleias/Brazilian Antarctic Program (CNPq grants 557064/2009-0 and 408096/2013-6), with additional support by INCT-APA (National Institute of Science and Technology on Antarctic Environmental Research). CNPq provided research fellowships to L.D.R. (PQ309258/ 2016-2) and to E.R.S. (PQ 307846/2014-8). The authors are also grateful to Márcia Caruso Bícego and the Brazilian fostering agency FAPESP (Process number: 2015/18348-1) for the use of gas chromatograph with triple quadrupole mass spectrometer (GC/MS/MS).
Antarctic seabirds were comparable to those found in migratory animals, such as the polar skua, and non-migratory birds, such as penguins. This is related to the high volatility of HCB in warmer regions associated with moderate partition coefficients compared to other POPs (Barber et al., 2005). That movement in multiple hops, which is known as the “grasshopper effect” (Wania and MacKay, 1996), leads to the condensation at high latitudes, such as Antarctica. HCB was found on the same order of magnitude as that of fin whales from other locations (Table 2), such as the Mediterranean Sea (Fossi et al., 2003, 2016) and Canada (Gauthier et al., 1997). DDT content, however, was higher (by a factor of about 15 to 380) compared to specimens from the Northern Hemisphere. The predominance of p,p′-DDE in the adipose tissue of fin whales among total DDTs ranged from 57 to 100% (78 ± 23%), which may be related to old sources of DDT in Antarctica, as reported by Fossi et al. (2003) in Mediterranean fin whales. However, this finding differs from the mean of 34.42% reported by Borrell and Aguilar (1987) in fin whales landed in north-western Spain, which was attributed to new sources of these compounds more than one decade earlier. Although the use of some organochlorine pesticides was restricted in a number of countries before the 1980s, DDT remained in use in some Mediterranean countries as a precursor of dicofol in the 1990s and even for agriculture purposes (UNEP, 2002b). Hobbs et al. (2001) found that samples from fin whales collected in 1971–72 had similar p,p′-DDT content, whereas samples collected in 1991 had about seven times higher p,p′-DDE content compared to its precursor. Saschenbrecker (1973) also found higher amounts of p,p′-DDT than p,p′-DDE in fin whales in the North Atlantic, which may be related to the use of this compound at the time, since its current use is severely restricted in North America (UNEP, 2002c). The HCH content was about one order of magnitude lower in comparison to fin whales in the Northern Hemisphere. Only γ–HCH was found in the blubber samples and may be related to the use of this compound, known as Lindane, in the Southern Hemisphere (Tanabe et al., 1983), since there is no local source of HCH in Antarctica. Concentrations in marine biota from Antarctica are similar in several species of the trophic web, which may be related to the higher solubility of this compound in water compared to other POPs, such as PCBs and DDTs (UNEP, 2002a). The PBDE content in Antarctic fin whale blubber was similar to that reported by Rotander et al. (2012) in samples from the same species collected in the Arctic and North Atlantic in 1986. In the same study, values one order of magnitude higher were found in samples from 2006 to 2009, which the authors attributed to the increase in the global production of technical PBDE mixtures in the 1990s. Higher contents of these compounds were found in fin whales from the Mediterranean Sea and Gulf of California in Mexico, where use was heavier, as reported by Pettersson et al. (2004) and Fossi et al. (2010). The presence of PBDEs in Arctic and Antarctic organisms may be related to long-range transport, as occurs with PCBs. All these studies found a predominance of the congeners 47 and 99, which may come from the commercial mixture penta-BDE or the debromination of heavier PBDEs, as suggested by Dorneles et al. (2015). These authors also found similar content (0.97 to 5.77 ng g−1 lw) and the predominance of the same congeners in humpback whales from Antarctica. Comparison between fin whales from Southern Ocean and other places should be carefully performed. The low POP content in Antarctic fin whales is related to the lower trophic position of the species given its diet differs from those found in some areas of Northern Hemisphere. The relative proximity of local POP sources is also an important consideration since they reach the polar region mainly through long-range transport.
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Acknowledgments The authors are grateful to all crew members of the Polar Vessel Almirante Maximiano of the Brazilian Navy and the investigators who 151
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back whales. Can. J. Comp. Med. 37, 203–206. Širović, A., Hildebrand, J.A., Wiggins, S.M., McDonald, M.A., Moore, S.E., Thiele, D., 2004. Seasonality of blue and fin whale calls and the influence of sea ice in the Western Antarctic Peninsula. Deep-Sea Res. 51, 2327–2344. Tanabe, S., Hidaka, H., Tatsukawa, R., 1983. PCBs and chlorinated hydrocarbon pesticides in Antarctic atmosphere and hydrosphere. Chemosphere 12, 277–288. Taniguchi, S., Montone, R.C., Bícego, M.C., Colabuono, F.I., Weber, R.R., Sericano, J.L., 2009. Chlorinated pesticides, polychlorinated biphenyls and polycyclic aromatic hydrocarbons in the fat tissue of seabirds from King George Island, Antarctica. Mar. Pollut. Bull. 58, 129–133. UNEP (United Nations Environment Programme), 2002a. Regionally Based Assessment of Persistent Toxic Substances – Antarctica Regional Report. UNEP (United Nations Environment Programme), 2002b. Regionally Based Assessment of Persistent Toxic Substances – Mediterranean Regional Report. UNEP (United Nations Environment Programme), 2002c. Regionally Based Assessment of Persistent Toxic Substances – North America Regional Report. Wade, T.L., Cantillo, A.Y., 1994. Use of Standards and Reference Materials in the Measurement of Chlorinated Hydrocarbons Residues. National Status and Trend Program for Marine Environmental Quality, NOAA, Silver Spring, pp. 68. Wania, F., MacKay, D., 1996. Peer reviewed: tracking the distribution of persistent organic pollutants. Environ. Sci. Technol. 30 (9), 390–396. Yasunaga, G., Fujise, Y., 2014. A note on mercury and organochlorine accumulation in the Antarctic fin whale based on JARPAII data. In: Paper SC/F14/J25 Presented to the IWC Sponsored Meeting to Review Data and Results from the Japanese Whale Research Program under Special Permit in the Antarctic Phase II (JARPAII) (JARPAII Review Meeting), February 2014. Yasunaga, G., Fujise, Y., Zenitani, R., Tanabe, S., Kato, H., 2015. Spatial and temporal variation of PCBs and organochlorine pesticides in the Antarctic minke whales, Balaenoptera bonaerensis, in the period 1987-2005. Chemosphere 126, 11–17. Zerbini, A.N., Secchi, E.R., Siciliano, S., Simões-Lopes, P.C., 1997. A review of the occurence and distribution of whales of the genus Balaenoptera along the Brazilian Coast. Rep. Int. Whal. Commn. 47, 407–417.
Compounds. US Department of Commerce, NOAA Technical Memorandum NMFS F/ NWC-92. Marsili, L., Focardi, S., 1996. Organochlorine levels in subcutaneous blubber biopsies of fin whales (Balaenoptera physalus) and striped dolphins (Stenella coeruleoalba) from the Mediterranean Sea. Environ. Pollut. 91, 1–9. Montone, R.C., Taniguchi, S., Colabuono, F.I., Martins, C.C., Cipro, C.V.Z., Barroso, H.S., da Silva, J., Bícego, M.C., Weber, R.R., 2016. Persistent Organic Pollutants and Polycyclic Aromatic Hydrocarbons in Penguins of the Genus Pygoscelis in Admiralty Bay — An Antarctic Specially Managed Area. Nemoto, T., 1970. Feeding pattern of baleen whales in the oceans. In: Steele, J.H. (Ed.), Marine Food Chains. University of California Press, Berkeley, CA, pp. 241–252. Pantoja, S., Pastene, L., Becerra, J., Silva, M., Gallardo, V.A., 1984. DDTs in Balaenopterids (Cetacea) from the Chilean coast. Mar. Pollut. Bull. 15, 451. Pantoja, S., Pastene, L., Becerra, J., Silva, M., Gallardo, V.A., 1985. Lindane, Aldrin and Dieldrin in some Chilean Cetacea. Mar. Pollut. Bull. 16, 255. Pérez, M.J., Thomas, F., Uribe, F., Sepúlveda, M., Flores, M., Moraga, R., 2006. Fin whales (Balaenoptera physalus) feeding on Euphausia mucronata in nearshore waters off northcentral Chile. Aquat. Mamm. 32, 109–113. Pettersson, A., van Bavel, B., Engwall, M., Jimenez, B., 2004. Polybrominated diphenylethers and methoxylated tetrabromodiphenylethers in cetaceans from the Mediterranean Sea. Arch. Environ. Contam. Toxicol. 47, 542–550. Pinzone, M., Budzinski, H., Tasciotti, A., Ody, D., Lepoint, G., Schnitzler, J., Scholl, G., Thomé, J.-P., Tapie, N., Eppe, G., Das, K., 2015. POPs in free-ranging pilot whales, sperm whales and fin whales from the Mediterranean Sea: influence of biological and ecological factors. Environ. Res. 142, 185–196. Rotander, A., van Bavel, B., Polder, A., Rigét, F., Auðunsson, G.A., Gabrielsen, G.W., Víkingsson, G., Bloch, D., Dam, M., 2012. Polybrominateddiphenyl ethers (PBDEs) in marine mammals from Arctic and North Atlantic regions, 1986–2009. Environ. Intern. 40, 102–109. Santora, J.A., Reiss, C.S., Loeb, V.J., Veit, R.R., 2010. Spatial association between hotspots of baleen whales and demographic patterns of Antarctic krill Euphausia superbasuggests size-dependent predation. Mar. Ecol. Prog. Ser. 405, 255–269. Saschenbrecker, P.W., 1973. Levels of DDT and PCB compounds in North Atlantic fin-
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Baseline
Persistent organic pollutants in blubber of fin whales (Balaenoptera physalus) from the Southern Ocean
T
⁎
Satie Taniguchia, , Fernanda I. Colabuonoa, Luciano Dalla Rosab, Eduardo R. Secchib, Josilene da Silvaa, Daniela A. Maiaa, Rosalinda C. Montonea a b
Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, São Paulo, SP 05508-120, Brazil Instituto de Oceanografia, Universidade Federal do Rio Grande – FURG, Rio Grande, RS 96203-000, Brazil
A R T I C LE I N FO
A B S T R A C T
Keywords: Antartica Fin whale Balaenoptera physalus POPs Organochlorine pesticides Southern Ocean
Persistent organic pollutants (POPs) were analyzed in eighteen blubber samples biopsied from fin whales (Balaenoptera physalus) during the feeding season near the Antarctic Peninsula in the summer of 2013. POP content (in ng g−1 lipid weight) ranged from 46.4 to 708 for polychlorinated biphenyls (∑PCBs), 6.77 to 123 for hexachlorobenzene (HCB), 10.1 to 489 for dichlorodiphenyltrichloroethane and derivatives (∑DDTs), 5.38 to 52.8 for hexachlorocyclohexanes (∑HCH) and < 0.40 to 2.54 for polybrominated diphenyl ethers (∑PBDEs). The presence of those compounds in Southern Ocean fin whales is related to long-range transport and their diet based mainly on euphausiids (krill). Their contents were much lower compared to the same species in other locations, especially in the Northern Hemisphere, presumably due to differences in trophic position and the proximity of POP sources and contamination of prey items.
The fin whale (Balaenoptera physalus) is a pelagic cetacean that inhabits all major oceans and some limited areas, such as the Gulf of California, East China Sea and Mediterranean Sea, but its overall range and distribution is not well known (Jefferson et al., 2008). This whale was once an important target species, with approximately 750,000 individuals killed in the Southern Hemisphere during the whaling period in the 20th century (Clapham and Baker, 2001). In relatively recent decades, several authors have described its presence on the coasts of Chile and Brazil (Pantoja et al., 1984; Zerbini et al., 1997; Pérez et al., 2006). In the Southern Ocean, fin whales have been sighted associated with euphausiids (krill), which are the main prey items of the species (Širović et al., 2004; Santora et al., 2010; Herr et al., 2016). Like any organism in the marine environment, whales are subject to contamination by anthropogenic compounds, such as persistent organic pollutants (POPs), which include organochlorine pesticides (OCP) and polychlorinated biphenyls (PCBs). POPs have been reported in several whale species in Antarctica, such as the humpback whale [Megaptera novaeangliae (Dorneles et al., 2015; Das et al., 2017)], Antarctic minke whale [Balaenoptera bonaerensis (Yasunaga et al., 2015)] and common minke whale [Balaenoptera acutorostrata (Aono et al., 1997)]. However, to our knowledge there are just a few published reports of contaminant levels in fin whales in the Southern Hemisphere (e.g. Yasunaga and Fujise, 2014; Pantoja et al., 1984, 1985).
⁎
To assess POP contents in this species, 18 blubber samples were collected during the feeding season in Bransfield Strait (n = 5 in 2013 and n = 4 in 2015), northern Antarctic Peninsula, and near the Powell Basin (n = 9 in 2013), northwestern Weddell Sea (Fig. 1). Blubber and skin samples were collected from live fin whales by firing a biopsy dart with a crossbow into the dorsal region of the individuals, as previously described by Gauthier et al. (1997). The analytical procedure followed that described by MacLeod et al. (1986) with minor modifications. Briefly, about 0.1 g of the wet tissue was dried with anhydrous sodium sulphate and extracted in Soxhlet apparatus for 8 h using 80 ml of n-hexane and methylene chloride (1:1, v:v). Before extraction, 2,2′,4,5′,6-pentachlorobiphenyl (PCB 103) and 2,2′,3,3′,4,5,5′,6-octachlorobiphenyl (PCB 198) were added to all samples, blanks and reference material as surrogates for OCPs and PCBs. After the determination of extractable lipids by gravimetric analysis in one aliquot, the extracts were cleaned up using column chromatography with 8 g of silica and 16 g of alumina, both 5% waterdeactivated and eluted with 80 ml of n-hexane and methylene chloride (1:1, v:v). To remove excess lipids, the fraction was further purified by high-performance liquid chromatography (HPLC) with two size exclusion columns (300 × 21.2 mm), using methylene chloride as the eluent, with a flow of 5 ml min−1. The internal standard 2,4,5,6-tetrachlorometaxylene (TCMX) was added before gas chromatographic
Corresponding author. E-mail address: [email protected] (S. Taniguchi).
https://doi.org/10.1016/j.marpolbul.2019.05.045 Received 22 March 2019; Received in revised form 9 May 2019; Accepted 20 May 2019 Available online 24 May 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Study area with sampling locations (red dots) of fin whales along the northern Antarctic Peninsula and northwestern Weddell Sea. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
investigated, including the following IUPAC numbers: 8, 18, 28, 31, 33, 44, 49, 52, 56, 60, 66, 70, 74, 77, 81, 87, 95, 97, 99, 101, 105, 110, 114, 118, 123, 126, 128, 132, 138, 141, 149, 151, 153, 156, 157, 158, 167, 169, 170, 174, 177, 180, 183, 187, 189, 194, 195, 199, 203, 206 and 209. The target PBDE congeners included IUPAC numbers 28, 47, 99, 100, 153, 154 and 183. The POP profile found (Table 1) in fin whale blubber (PCBs > HCB > DDTs > HCHs > PBDEs) was very similar to that found in humpbacks whales and fin whales that fed near the Antarctic Peninsula (Dorneles et al., 2015; Yasunaga and Fujise, 2014, respectively), but slightly different from humpbacks feeding in the Indian Ocean sector of Antarctica, in which higher concentrations of HCB (HCB > DDT > PCB > PBDE) have been reported (Das et al., 2017). No marked differences were found between male and female whales collected in Bransfield Strait (Fin 1–9) and Weddell Sea (Fin 10–18). Although the prey items of fin and humpback whales can differ, both feed mainly on krill (Pérez et al., 2006). Santora et al. (2010) found that fin whales were associated with large (> 45 mm) mature krill located offshore, whereas humpback whales were associated with juvenile krill (< 35 mm) in Bransfield Strait. In an aerial survey of Bransfield Strait and the Drake Passage, Herr et al. (2016) found that fin whales fed in an area dominated by Thysanoessa macrura in the Drake Passage, whereas humpback whales were found mostly in areas with a greater biomass of Euphausia superba, in the Bransfield Strait. Some of our samples (Fin 1–9) were obtained in the Bransfield Strait, just south of King George Island and POP contents were similar to that found in specimens collected in Weddell Sea (Fin 10–18). Nemoto (1970) analyzed the stomach contents of 35139 Antarctic fin whales caught from 1961 to 1965 and found mainly euphausiids, which form dense swarms in the sea, unlike the same whale species in the North Pacific, which fed
analysis. A procedural blank was run for every set of ten samples. OCP, PCB and PBDE were quantitatively analyzed in an Agilent Technologies 7890B gas chromatograph with a 7010B triple quadrupole mass spectrometer (GC/MS/MS) using a 30 m × 0.25 mm i.d. capillary column coated with a 5% phenyl-substituted dimethylpolysiloxane phase (film thickness: 0.25 μm). The injected volume was 1 μl in automatic pulsed splitless mode. Helium was used as the carrier gas (constant flow of 1.1 ml min−1). The interface, source and quadrupole temperatures were 300 °C, 300 °C and 150 °C, respectively. The oven temperature was programmed as follows: 75 °C for 3 min, raised at 15 °C min−1 to 150 °C, then raised at 2.0 °C min−1 to 260 °C and at 20 °C min−1 to 300 °C, with a final hold of 10 min. For quality assurance/quality control (QA/QC), the analytical method was validated using a standard reference (SRM 1945 – organics in whale blubber) purchased from the National Institute of Standards and Technology (NIST), USA, which was analyzed in duplicate. The average recovery of analytes (68–114%) was within the range reported (50–120%) in Intergovernamental Oceanographic Commission (IOC) technical series by Wade and Cantillo (1994). The recovery of analytes in spiked blanks (76–109%) and matrices (85–116%) produced satisfactory results. Compounds in laboratory blanks were subtracted from the samples. The limit of quantification (LOQ) for PCBs, POCs and PBDEs was 0.4, 1.0 and 0.1 ng g−1 lipid weight (lw), respectively. The quantification of analytes was based on a nine-level analytical curve and followed the internal standard procedure. Surrogate recoveries were acceptable, with mean ± standard deviation of 87 ± 7. The OCPs analyzed in this study were dichlorodiphenyltrichloroethane and derivatives (o,p′-DDT, p,p′-DDT, o,p′-DDD, p,p′-DDD, o,p′-DDE and p,p′-DDE), hexachlorocyclohexanes (α, β-, δ- and γ-HCH) and hexachlorobenzene (HCB). A suite of 51 PCBs was also 149
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Table 1 Persistent organic pollutant content in fin whale blubber in ng g−1 lipid weight (ng g−1 wet weight). POP
Gender
Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin Fin
F F M F M M – M F M M M M M M M F F
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
ΣPCBs
HCB
ΣDDTs
ΣHCHs
ΣPBDEs
86.1 (42.4) 241 (54.8) 66.1 (25.8) 202 (54.4) 46.4 (19.2) 321 (78.2) 386 (166) 266 (116) 211 (52) 110 (41.3) 89.2 (26.0) 708 (139) 186 (114) 78.7 (42.3) 162 (49.9) 339 (79.1) 560 (274) 222 (31.4)
13.5 (6,62) 123 (28.0) 58.2 (22.7) 39.6 (10.7) 52.2 (21.5) 69.5 (16.9) 58.4 (25.1) 45.4 (19.7) 56.2 (13.9) 29.5 (11.1) 6.77 (1.97) 55.3 (10.9) 35.2 (21.6) 25.5 (13.7) 48.0 (14.8) 51.9 (12.1) 11.6 (5.65) 16.9 (2.38)
15.1 (7.42) 60.8 (13.8) 17.5 (6.83) 10.1 (2.72) 24.8 (10.2) 336 (81.9) 439 (189) 422 (183) 489 (121) 29.1 (10.9) 10.4 (3.04) 85.2 (16.7) 27.0 (16.5) 78.4 (42.2) 21.3 (6.54) 49.5 (11.6) 15.0 (7.34) 20.5 (2.89)
17.1 52.8 11.7 46.1 8.31 13.0 7.80 11.8 13.0 10.7 5.38 39.6 23.7 6.24 10.8 31.9 47.2 21.3
0.64 (0.15) 1.08 (0.53) < 0.40 (< 0.10) 0.41 (0.11) 0.33 (0.14) < 0.40 (< 0.10) < 0.40 (< 0.10) 1.57 (0.65) 1.30 (0.54) 1.26 (0.47) < 0.40 (< 0.10) 2.54 (0.50) 0.95 (0.58) < 0.40 (< 0.10) 0.36 (0.11) 0.80 (0.19) 0.61 (0.30) 0.99 (0.14)
(8.39) (12.0) (4.58) (12.4) (3.43) (3.16) (3.35) (5.14) (3.21) (4.01) (1.57) (7.78) (14.5) (3.36) (3.31) (7.44) (23.1) (3.00)
% lipid 22.7 49.2 39.0 26.9 41.3 24.3 42.9 43.5 24.7 37.6 29.1 19.7 61.2 53.8 30.7 23.3 48.9 14.1
archived blubber samples from fin whales collected in 1971–72 compared to samples collected in 1991 in eastern Canada. Tetrachlorobiphenyls, such as PCB-44, 49 and 52, were predominant in the older samples, whereas the penta-, hexa- and heptachlorobiphenyls, such as PCB-101, 153 and 180, had relatively higher contents in the newer samples. Predominance of heavier compounds can be attributed to the accumulation by biomagnification or because of POP content in the environment and in prey species of the whales. Other chlorinated compounds, such as HCB, DDTs and HCHs, are frequently reported in different organisms in Antarctica, such as penguins (Montone et al., 2016), which also feed mainly on krill. HCB was initially used as a fungicide for seed treatment of grain crops, but later became mainly a by-product in the production of a large number of lower chlorinated compounds (UNEP, 2002a). Taniguchi et al. (2009) and Colabuono et al. (2014) reported that the amounts of HCB in
on similar quantities of euphausiids, large copepods and gregarious fish. Table 2 presents the contents of POPs reported in fin whales blubber sampled worldwide. Marsili and Focardi (1996) and Fossi et al. (2006) reported variable amounts of PCBs in Mediterranean fin whales, which also feed on large amounts of euphausiid species, mainly northern krill (Meganyctiphanes norvegica), among other marine organisms, but the proximity to the sources are likely the main reason for the differences in PCB contents. The predominance of tri-, tetra- and pentachlorinated biphenyls in the present study indicate PCBs coming from long-range transport, unlike that found for the same species in the Mediterranean Sea, in which higher contents of PCBs have been found, with a predominance of heavier congeners, such as hexa- (PCB 138, 149 and 153) and heptachlorinated biphenyls (170, 180 and 187), as described by Fossi et al. (2014). Hobbs et al. (2001) described experiments with
Table 2 Published contents of polychlorinated biphenyls, polybrominated diphenyl ether, organochlorine pesticide in fin whales blubber [ng g−1 lipid (lw) or wet weight (ww)]. Lipid % a
Antarctica North Atlanticb Northern hemisphere Chilean Coastb Chilean Coastb North-western Spain and Icelanda Eastern North Atlantica Eastern North Atlantica Icelanda Durban, South Africanb Mediterranean Sea Italyc Gulf of St Lawrence, Canadaa Eastern Canada - Newfoundlanda Eastern Canada - Nova Scotiaa Eastern Canada - Gulf of St Lawrencea Mediterranean Seab Mediterranean Seaa Mediterranean Sea and Mexicoc Arctic and North Atlantic regionsa Antarcticaa Mediterranean Sea (Italy)a Mediterranean Sea Mediterranean Seaa Sea of Cortez, Mexicoa a b c
14.1–61.2 30
HCB
ΣDDT < 10.1–489
ΣPCB
ΣHCH 5.38 to 52.8 – – – 1.7 – –
< 0.40 to 2.54 – – – – – –
– – – 215 ± 92134–426 121–238 84.7–376 – – – – 0.65 – – – –
– – – – – – – – 806 82–305.06 5–12 (1986/89) 20–31 (2006/09) – – – – –
– – – 77.5 10.8–85.6 – – 4.1–87 4.1–87 – – – – –
6.77–123 – – – – – – – – – – 96 ± 82 114–619 136–334 10–318 39.5 – – –
2.83 54.4 – 1145 483–1981 500–1490 610–850 30–330 3000–6800 3812 ± 3908 1410–8110 5750–32,700 651–13,100 4400 – – –
46.4 to 708 12–185 3.6 – – – 561–2026 770–1820 940–1260 n.d. (Aroclor 1254) 2600–3800 2674 ± 2850 673–2930 1470–10,800 229–10,200 3800 – – –
– – – –
39 129.13–286.26 – 29.9 ± 12 38.5 ± 33.6
13 6580.67–26,833.64 6643 ± 5549 10,477.3 ± 7477.3 3109.9 ± 2245.9
6.5 9117.09–42,778.45 5721 ± 5180 13,327.3 ± 8548.3 8753.8 ± 6542.6
Lipid weight. Wet weight. Dry weight. 150
ΣPBDE
Reference This study Saschenbrecker (1973) Holden (1975) Pantoja et al. (1984) Pantoja et al. (1985) Borrell and Aguilar (1987) Aguilar and Borrell (1988) Aguilar and Borrell (1991) Borrell (1993) Henry and Best (1983) Marsili and Focardi (1996) Gauthier et al. (1997) Hobbs et al. (2001) Hobbs et al. (2001) Hobbs et al. (2001) Fossi et al. (2003) Pettersson et al. (2004) Fossi et al. (2010) Rotander et al. (2012) Yasunaga and Fujise (2014) Fossi et al. (2014) Pinzone et al. (2015) Fossi et al. (2016) Fossi et al. (2016)
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helped collecting samples and data, especially Alexandre Azevedo, Artur Andriolo and Jorge Acevedo. This study was conducted by Projeto Baleias/Brazilian Antarctic Program (CNPq grants 557064/2009-0 and 408096/2013-6), with additional support by INCT-APA (National Institute of Science and Technology on Antarctic Environmental Research). CNPq provided research fellowships to L.D.R. (PQ309258/ 2016-2) and to E.R.S. (PQ 307846/2014-8). The authors are also grateful to Márcia Caruso Bícego and the Brazilian fostering agency FAPESP (Process number: 2015/18348-1) for the use of gas chromatograph with triple quadrupole mass spectrometer (GC/MS/MS).
Antarctic seabirds were comparable to those found in migratory animals, such as the polar skua, and non-migratory birds, such as penguins. This is related to the high volatility of HCB in warmer regions associated with moderate partition coefficients compared to other POPs (Barber et al., 2005). That movement in multiple hops, which is known as the “grasshopper effect” (Wania and MacKay, 1996), leads to the condensation at high latitudes, such as Antarctica. HCB was found on the same order of magnitude as that of fin whales from other locations (Table 2), such as the Mediterranean Sea (Fossi et al., 2003, 2016) and Canada (Gauthier et al., 1997). DDT content, however, was higher (by a factor of about 15 to 380) compared to specimens from the Northern Hemisphere. The predominance of p,p′-DDE in the adipose tissue of fin whales among total DDTs ranged from 57 to 100% (78 ± 23%), which may be related to old sources of DDT in Antarctica, as reported by Fossi et al. (2003) in Mediterranean fin whales. However, this finding differs from the mean of 34.42% reported by Borrell and Aguilar (1987) in fin whales landed in north-western Spain, which was attributed to new sources of these compounds more than one decade earlier. Although the use of some organochlorine pesticides was restricted in a number of countries before the 1980s, DDT remained in use in some Mediterranean countries as a precursor of dicofol in the 1990s and even for agriculture purposes (UNEP, 2002b). Hobbs et al. (2001) found that samples from fin whales collected in 1971–72 had similar p,p′-DDT content, whereas samples collected in 1991 had about seven times higher p,p′-DDE content compared to its precursor. Saschenbrecker (1973) also found higher amounts of p,p′-DDT than p,p′-DDE in fin whales in the North Atlantic, which may be related to the use of this compound at the time, since its current use is severely restricted in North America (UNEP, 2002c). The HCH content was about one order of magnitude lower in comparison to fin whales in the Northern Hemisphere. Only γ–HCH was found in the blubber samples and may be related to the use of this compound, known as Lindane, in the Southern Hemisphere (Tanabe et al., 1983), since there is no local source of HCH in Antarctica. Concentrations in marine biota from Antarctica are similar in several species of the trophic web, which may be related to the higher solubility of this compound in water compared to other POPs, such as PCBs and DDTs (UNEP, 2002a). The PBDE content in Antarctic fin whale blubber was similar to that reported by Rotander et al. (2012) in samples from the same species collected in the Arctic and North Atlantic in 1986. In the same study, values one order of magnitude higher were found in samples from 2006 to 2009, which the authors attributed to the increase in the global production of technical PBDE mixtures in the 1990s. Higher contents of these compounds were found in fin whales from the Mediterranean Sea and Gulf of California in Mexico, where use was heavier, as reported by Pettersson et al. (2004) and Fossi et al. (2010). The presence of PBDEs in Arctic and Antarctic organisms may be related to long-range transport, as occurs with PCBs. All these studies found a predominance of the congeners 47 and 99, which may come from the commercial mixture penta-BDE or the debromination of heavier PBDEs, as suggested by Dorneles et al. (2015). These authors also found similar content (0.97 to 5.77 ng g−1 lw) and the predominance of the same congeners in humpback whales from Antarctica. Comparison between fin whales from Southern Ocean and other places should be carefully performed. The low POP content in Antarctic fin whales is related to the lower trophic position of the species given its diet differs from those found in some areas of Northern Hemisphere. The relative proximity of local POP sources is also an important consideration since they reach the polar region mainly through long-range transport.
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Acknowledgments The authors are grateful to all crew members of the Polar Vessel Almirante Maximiano of the Brazilian Navy and the investigators who 151
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