Science of the Total Environment 481 (2014) 619–634

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Anthropogenic (PBDE) and naturally-produced (MeO-PBDE) brominatedcompounds in cetaceans — A review

Mariana B. Alonso a,b,c,⁎, Alexandre Azevedo b, João Paulo M. Torres a, Paulo R. Dorneles a, Ethel Eljarrat d,Damià Barceló d,e, José Lailson-Brito Jr. b, Olaf Malm a

a Radioisotopes Laboratory, Biophysics Institute, Federal University of Rio de Janeiro (UFRJ), Brazilb Aquatic Mammal and Bioindicator Laboratory (MAQUA), School of Oceanography, Rio de Janeiro State University (UERJ), Brazilc Projeto BioPesca, Praia Grande, SP, Brazild Department of Environmental Chemistry, IDAEA, CSIC, Jordi Girona 18-26, 08034 Barcelona, Spaine Catalan Institute for Water Research (ICRA), Parc Científic i Tecnològic de la Universitat de Girona, Pic de Peguera 15, 17003 Girona, Spain

H I G H L I G H T S

• PBDE contamination is higher in cetaceans from Northern than Southern hemisphere.• The opposite occurs in relation to MeO-BDEs contamination.• Only in UK the PBDE concentrations in cetaceans decreased in the last decades.• Studies presented PBDE levels higher than the threshold to potential health effects in marine mammals.

⁎ Corresponding author at: Universidade Federal do RiBiofísica Carlos Chagas Filho (IBCCF), Laboratório deFranca (LREPF), Av. Carlos Chagas Filho, 373 — CCSUniversitária, 21941-902, Rio de Janeiro, RJ, Brazil. Tel.: +22808193.

E-mail addresses: alonso.mb@gmail.com, mary_alonsoazevedo.alex@uerj.br (A. Azevedo), jptorres@biof.ufrj.br (dorneles@biof.ufrj.br (P.R. Dorneles), eeeqam@iiqab.csic.edbcqam@cid.csic.es (D. Barceló), lailson@uerj.br (J. Lailson(O. Malm).

http://dx.doi.org/10.1016/j.scitotenv.2014.02.0220048-9697/© 2014 Elsevier B.V. All rights reserved.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 7 June 2013Received in revised form 15 January 2014Accepted 7 February 2014Available online xxxx

Keywords:PBDEsMeO-PBDEsEndocrine disruptorsCetaceansMarine mammalsTime trends

This paper reviews the available data on brominated flame retardants, the polybrominated diphenyl ethers(PBDEs), as well as on the naturally-produced methoxylated polybrominated diphenyl ethers (MeO-PBDEs) incetacean tissues around the world. Levels and possible sources of both compound classes are discussed.Odontocete cetaceans accumulate higher PBDE concentrations than mysticete species. PBDE contaminationwas higher in cetaceans from the Northern hemisphere, whereas MeO-PBDE levels were higher in animalsfrom the Southern hemisphere. Southern resident killer whales from NE Pacific presented the highest levelsreported in biota, followed by bottlenose dolphins from North Atlantic (U.K. and U.S. coast). Many species pre-sented PBDE concentrations above threshold levels for health effects in odontocetes. Time trend studies indicatethat PBDE concentrations in odontocetes from Japan, China, U.S. and Canada coastal zones have increased signif-icantly over the past 30 years. Studies from U.K. waters and NE Atlantic showed a decrease and/or stability ofPBDE levels in cetacean tissues in recent decades. The highest MeO-PBDE concentrationswere found in dolphinsfrom Tanzania (Indian Ocean), bottlenose dolphins from Queensland, Australia (SW Pacific), and odontocetesfrom coastal and continental shelf waters off southeastern Brazil (SW Atlantic). The upwelling phenomenonand the presence of coral reef complexes in these tropical oceans may explain the large amounts of thenaturally-produced organobromines. Considering that these bioaccumulative chemicals have properties thatcould cause many deleterious effects in those animals, future studies are required to evaluate the potentialecotoxicological risks.

© 2014 Elsevier B.V. All rights reserved.

o de Janeiro (UFRJ), Instituto deRadioisótopos Eduardo Penna— Bl. G — subsolo, Cidade55 21 25615339; fax: +55 21

@biof.ufrj.br (M.B. Alonso),J.P.M. Torres),s (E. Eljarrat),-Brito), olaf@biof.ufrj.br

1. Introduction

Brominated flame retardants (BFRs) constitute a chemically diverseclass of compounds that are either aromatic, aliphatic or cycloaliphaticwith different contents of bromine, and are used in a variety of commer-cial applications (plastics, wood, paper, textiles, electronic circuitry andother materials) to prevent fires. The estimated global consumption ofBFRs shows that their usage increased from 1990 to 2000, a period inwhich such usage was more than doubled, from 145 to 310 kilotons

620 M.B. Alonso et al. / Science of the Total Environment 481 (2014) 619–634

approximately (Arias, 2001). Themost used BFRs are the polybrominateddiphenyl ethers (PBDEs). Due to their persistence in the environment,biomagnification in the food web and toxicity, these contaminants havebeen extensively studied during the past three decades (DeCarlo, 1979;Kuehl et al., 1991; Law et al., 2003; Rotander et al., 2012). Themarine en-vironment is particularly vulnerable to halogenated compounds and con-sequently contains a large portion of these pollutants (Tanabe et al.,1988).

World-wide, 50,000 metric tons of PBDEs are produced annually. Itis estimated that 40% of this amount is used in North America (Arias,2001). PBDEs are produced at three degrees of bromination and theircommercial mixtures are classified as Deca-, Octa- and Penta-BDE(ATSDR, 2004). In 1999, the worldwide market demand was up to54,800, 3825 and 8500 tons of these formulations, respectively (Alaeeet al., 2003).

Structural similarity to other environmental chemicals with knowntoxic effects (polychlorinated biphenyls— PCBs, polybrominated biphe-nyls — PBBs and dioxins), suggests that exposure to PBDEs may posehealth risks. A variety of biological effects have been reported forPBDEs in mammals, as an influence on the homeostasis of steroidaland thyroidal hormones (Darnerud, 2003; Zhou et al., 2001) andimmunotoxicity (Fowles et al., 1994) as well as reproductive andother neurological endpoints (Betts, 2002; Siddiqi et al., 2003).

In May 2009, the Stockholm Convention on Persistent OrganicPollutants (POPs) listed commercial Penta-BDE and Octa-BDE as POPs(UNEP, 2009). Since 2004, the E.U. and U.S. phased out the productionand use of these mixtures (Directive EEC, 2003; Renner, 2004). Insome U.S. states, Deca-BDE was banned last year (USEPA, 2012). InEurope their use was prohibited in electronic applications in 2008 andconsequently by REACH (European Regulation for the Registration,Evaluation, Authorization and Restriction of Chemical substances) legis-lation in 2010 (European Court of Justice, 2008; UNEP, 2009). Despitethis, PBDEs continue to be used and commercialized as flame retardantsthroughout the rest of the world.

Organohalogenated compounds from natural origin have recentlybeen detected in marine food chains in different regions. These include1,1′-dimethyl-2, 2′-bipyrroles (HDBPs), hexachlorinated 1′-methyl-1,2′-bipyrrole (C17-MBP), methoxylated polybrominated diphenylethers (MeO-PBDEs), dimethoxy tetrabromodiphenyls (diMeO-BB),polybrominated hexahydroxanthene derivatives (PBHDs), amongothers (Haraguchi et al., 2009; Vetter, 2001).

MeO-PBDEs have been detected in algae, mollusks, marine sponges,fish, birds and mammals (Kelly et al., 2008; Malmvärn et al., 2005;Weijs et al., 2013a,b). It is proposed that methoxylated-PBDEs are syn-thesized by some algae, such as red algae (Ceramium tenuicone,Plocamium cartilagineum, Polysiphonia sphaerocarpa, Polysiphoniafucoides, Jania sp.; Malmvärn et al., 2005, 2008; Asplund et al., 2001;Haraguchi et al., 2010), green algae (Cladophhora fasciculatis), brownalgae (Pilayella littoralis, Sargassum sp.; Haraguchi et al., 2010), and alsoby marine sponges (e.g. Dysidea herbacea, D. fragilis, Phyllospongiafoliascen and Ephydatia fluviatilis; Bowden et al., 2000; Fu et al., 1995;Handayani et al., 1997) and their associated cyanobacteria (Oscillatoriaspongeliae, Aphanizomenon flos-aquae, Nodularia sprumigena; Malmvärnet al., 2008; Unson et al., 1994). Another synthesis pathway of MeO-PBDEs can be via biotransformation of hydroxylated PBDEs (Wan et al.,2010b). The biotransformation pathways have been partly elucidatedby recent studies (Wan et al., 2010a,b; Wang et al., 2012). MeO-PBDEsmay be generated by microbial O-methylation products of hydroxylatedPBDEs, as observed for the related phenols (Allard et al., 1987; Georgeand Haggblom, 2008).

MeO-PBDEs can biomagnify through the trophic web just as thecorresponding anthropogenic PBDEs, and were found in considerableconcentrations in top predator marine birds and mammals (Losadaet al., 2009; Weijs et al., 2009b). These compounds are proposed tohave a natural origin and have been present in themarine environmentfor centuries (Teuten et al., 2005; Teuten and Reddy, 2007; Vetter,

2006). Teuten et al. (2005) confirmed that MeO-PBDEs have a naturalorigin through the detection of these compounds in oil samples of thetrue beaked whale (Mesoplodon mirus) from the1920s (Teuten andReddy, 2007).

The two predominant MeO-PBDE congeners in marine top predatortissues are 2′-MeO-BDE-68 and 6-MeO-BDE-47. Vetter (2006) hypoth-esized that congener 2′-MeO-BDE-68 is synthesized mainly by spongesor associated organisms, whereas 6-MeO-BDE-47 is produced by algaeor associated organisms. Based on this hypothesis, the author pointsout that 2′-MeO-BDE-68/6-MeO-BDE-47 ratios greater than 1.0 in ani-mal tissues imply that these species would be receivingMeO-PBDE pre-dominantly from sponges or associated organisms, while ratios lowerthan 1.0 suggest that these animals would be receiving MeO-PBDEspredominantly from algae. However, a recent study by Haraguchiet al. (2010) found evidence that both congeners can be synthesizedby tropical algae.

Cetacean species are a good biomonitor of the presence of several or-ganic contaminants in the environment. These animals occupy high tro-phic levels and have a large reserve of energy in the blubber, the fattissue that is able to accumulate high concentrations of lipophilic con-taminants. They have a long life span, estimated up to 97 years (Krahnet al., 2009). Furthermore, they can be a tool that may help to elucidatethe human exposure to these compounds through ingestion of fish andsea food (Aguilar, 1987).

The objective of this review is to summarize published data on PBDEandMeO-PBDE levels in different species of marine cetaceans distribut-ed throughout the globe, and describe the current state of knowledge onthese anthropogenic and naturally-produced organobrominatedcompounds.

2. PBDEs in cetaceans

A total of 62 studies were found in the literature reporting PBDEs inblubber and liver of cetaceans around theworld, published from1991 to2013. All the data discussed here were reported inmean concentrationsand expressed on a lipid basis. In order to turn it possible to compareconcentrations, data reported in blubber tissue in wet weight (ww)were re-calculated to lipid weight (lw) applying a mean of 70% oflipid content, as suggested by Tanabe et al. (1994).

2.1. Blubber and liver concentrations

Blubber and liver are the two tissues selected in this review due tothe great amount of published data in cetaceans. In total, 54 and 15 pub-lications were found for blubber and liver, respectively. Other organswere also analyzed to evaluate PBDE contamination in cetaceans, suchas blood (Nomiyama et al., 2011; Weijs et al., 2009a), central nervoussystem (Montie et al., 2009; Weijs et al., 2010a), kidney (Kannanet al., 2005; Ramu et al., 2005; Weijs et al., 2010b), muscle (Isobeet al., 2009; Ramu et al., 2005) and milk (Yordy et al., 2010), but thesestudies were not discussed in this review. Tables 1 and 2 show PBDElevels in blubber samples from odontocete and mysticete cetaceans, re-spectively. Table 3 presents mean PBDE levels in livers of cetaceanaround the world.

Odontocete cetaceans accumulate higher PBDE levels thanmysticetein fatty tissues (Moon et al., 2010). This fact occurs due to a higher tro-phic position in the food web for odontocetes compared to mysticetes.Normally mysticetes belong to shorter trophic chains than odontocetesince they may feed on zooplankton and small fish (Dehn et al., 2006).Odontocetes are usually at the top of their food webs (or near the top,such as small dolphins which are only predated by sharks and otherodontocete) and eat larger and more contaminated preys, resulting inhigher concentrations of persistent bioaccumulative toxicants in com-parison to mysticetes (Johnson-Restrepo et al., 2005; Law et al., 2005;Moon et al., 2010).

Table 1Mean PBDE and MeO-PBDE concentrations (ng/g lw) in blubber of odontocete cetaceans around the world.

Species Area Locality Year n Sex/age classa PBDEs MeO-PBDEs Ref.e

Bottlenose dolphin(Tursiops truncatus)

NW Atlantic Texas and Alabama, U.S. 1990 8 AM 3110 1Texas, U.S. 1990–01 5 AF 190

1990 5 Ju 19001990 5 NB 313

Virginia, U.S. 1987 3 AF 200 2Florida, U.S. 1991–01 14 M, F 817 3Indian River, FL, U.S. 2001–04 6 M, F 1130

2003–04 25 AM 1690 414 AF 69611 Ju 979

Charleston, SC, U.S. 2003–05 31 AM 68309 AF 115313 Ju 7055

Indian River, FL, U.S. 2003–05 31 AM 1490 515 AF 58123 Ju 1101

Charleston, SC, U.S. 2003–05 35 AM 591711 AF 97720 Ju 4400

Cape May, U.S. 2000–07 3 M 6560 6Beaufort, U.S. 2000–07 2 M 1460Holden Beach, U.S. 2000–07 3 M 3650Charleston, U.S. 2000–07 20 M 5060Sapelo, U.S. 2000–07 30 M 3980Brunswick, U.S. 2000–07 19 M 3610N Biscayne Bay, U.S. 2000–07 15 M 2360S Biscayne Bay, U.S. 2000–07 15 M 870Sarasota Bay, U.S. 2000–07 33 M 1910Tampa Bay, U.S. 2000–07 5 M 1430Apalachicola Bay, U.S. 2000–07 20 M 690St. Joseph Bay, U.S. 2000–07 38 M 1470Mississipi Sound, U.S. 2000–07 55 M 3780Bermuda, U.S. 2000–07 3 M 1660Sarasota Bay, FL, U.S. 2000–05 19 JM 1390 7

22 JF 150016 AM 175031 AF 151

Florida, U.S. 2002–04 31 AM, Ju 563 82002–04 6 AF 30

Brunswick, U.S. 2006–09 24 M 3850 910 F 630

Brunswick and Sapelo, U.S. 2006–09 18 M 51204 F 380

Sapelo, U.S. 2006–09 32 M 248014 F 1270

NE Atlantic U.K. 1995–2001 6 M 7040 103 F 8880

SW Pacific Australia 1995 1 80 111996 1 209

Queensland, Australia 1 13,145 12Queensland, Australia 4 2095 13

SW Atlantic Sao Paulo, Brazil 1996–03 1 M 64.2 14Indo-Pacific bottlenose dolphin(Tursiops aduncus)

Indian Tanzania 2000–02 4 AF 22,500 154 JF 70,0004 AM 151,2505 JM 28,220

Harbor porpoise(Phocoena phocoena)

NE Atlantic North Sea 1999–04 8 AM 1540 16, 175 AF 85012 JM 17309 JF 700

1990–98 1 NB 132b 20b 184 Ca 2586b 149b

1 Ju 4771b 118b

1 Ad 1900b 156b

2000–08 2 NB 462b 97b

12 Ca 552b 138b

5 Ju 494b 224b

2 Ad 1194b 80b

1992–98 30 AM 1340 1925 AF 103063 Ju 1620

North and Baltic Sea 1997–01 M, F 170 20Iceland 1997–01 M, F 38

(continued on next page)

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Table 1 (continued)

Species Area Locality Year n Sex/age classa PBDEs MeO-PBDEs Ref.e

Baltic Sea 6 M 170 217 F 660

Norway 4 M 42012 F 560

England and Wales 1996–99 18 M 2800 2234 F 2200

Iceland 1992 5 M 94c 231997 5 M 75c

Norway 2000 5 M 161c

Scotland (U.K.) 2001–03 AF 1363 24Irish 2001–03 AF 656North Sea 2001–03 AF 1056France 2001–03 AF 1398Spain 2001–03 AF 284

Black Sea 1998 11 AM 65.6b 46.6b 259 JM 57.0b 52.9b

NE Pacific British Columbia, Canada 1991–93 5 M 868 26NW Pacific Japan 1999 3 AM 73 27

Dall's porpoise(Phocoenoides dalli)

Truei-type NW Pacific Off Sanriku, Japan 2000 5 AM 57Dalli-type Off Hokkaido, Japan 2000 5 AM 530

Killer whale(Orcinus orca)

NE Pacific Alaska, U.S. 1993–94 13 N resident, M 203 281993 8 N resident, F 415

Washington, U.S. 1993–95 5 S resident, M 942Washington and Alaska, U.S. 1993–96 6 transient, M 1014

7 transient, F 885Alaska, U.S. 2003–04 40 N resident, AM 76 29

4 Offshore, AM 3300California and Alaska, U.S. 2003–04 16 transient, AM 6695Puget Sound, WA, U.S. 2006 1 S resident, JM 15,000 30

2 S resident, AM 6550Canada 2004 5 S resident, AM 2820

1 S resident, AF 7500Puget Sound to Georgia Basin 1993–94 15 N resident, AM 230 28

3 N resident, JM 1307 N resident, AF 351 N resident, JF 1400

Puget Sound to Georgia Basin 1993–97 6 transient, AM 3905 transient, AF 3402 transient, JM 190

Puget Sound to Georgia Basin 1995 5 S resident, AM 450Puget Sound to BritishColumbia

2004 3 S resident, AM 2967 312 S resident, JM 12,0006 S resident, AF 30101 S resident, JF 15,000

NW Pacific Japan 2005 1 N resident, AM 216 183 325 N resident, AF 313 4183 N resident, C 585 690

Rausu, Japan 2005 1 AM 270 331 CM 4705 AF 2602 CF 520

NE Atlantic U.K. 1994–01 2 M 2526 102 F 12,642

Norway 2002 8 AM 475 34False killer whale(Pseudorca crassidens)

NE Pacific Hawaii 2008 1 JF 2400 351 JM 29002 AM 12005 AF 420

Finless porpoise(Neophocaena phocaenoides)

NW Pacific Hong Kong 2000–01 5 M 566 361 F 470

South China Sea 1990 7 AM 113 37Hong Kong 2000–01 5 AM 714Seto Inland, Japan 1998–2000 5 AM 730 27Pacific Coast, Japan 1999 2 AM 620HongKong 2000–01 6 AM 600Korea 2003 15 JM 890 38

20 JF 8707 AM 87010 AF 510

Hong Kong 2003–08 33 1113 39South China Sea 1990 7 M 110 33

2000–01 5 M 710Melon-headed whale(Peponocephala electra)

NW Pacific Japan 1982 5 AM 26 401982 5 M 26 27, 332001 5 AM 320

4 AM 24 402 AF 16

Harbor porpoise(Phocoena phocoena)

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Table 1 (continued)

Species Area Locality Year n Sex/age classa PBDEs MeO-PBDEs Ref.e

2001–02 6 AM 32020 AF 648 JM 3006 JF 190

2006 5 AM 300SW Pacific Australia 1996 1 AM 230 11

Queensland, Australia 1 2005 12Queensland, Australia 1 2020 13

Long-finned pilot whale(Globicephala melas)

NE Atlantic Faroe Islands 1996 8 AM 1600d 4113 JM 3160d

19 AF 1047d

4 JF 3038d

1994 9 AF 843d

Faroe Islands 1996 19 AF 1048d 428 AM 1610d

Faroe Islands 1986 3–5 M 51d 231997 3–5 M 613d

2006–07 3–5 M 1041d

SW Pacific Tasmania, Australia 2008 6 JF 25 843 559 JF 16 5539 AF 8 2378 AF 6 1576 JM 17 62810 JM 13 3895 AM 10 3536 JF 31 85616 AF 17 3596 AF 6 1445 AF 10 2423 JM 19 33211 AM 10 272

2011 3 JM 32 4712011 4 AM 26 355

Franciscana dolphin(Pontoporia blainvillei)

SW Atlantic Sao Paulo, Brazil 1996–03 4 M 101 144 F 19.6

Beluga(Delphinapterus leucas)

NW Atlantic St. Lawrence, Canada 1999–00 7 M 536 118 F 535

1997–99 15 AM 430 4314 AF 540

Frobisher Bay, Canadian Arctic 1996 5 M 11.5 44E Hudson Bay, Canadian Arctic 1999–03 9/5 Ca 27 310 45

14/6 F 16 6221/6 M 34 300

NE Atlantic Svalbard, Norway 1996–01 5 AM 93.7 461 AF 1206 Ju 85.1

NE Pacific Cook Inlet, Alaska 1989–06 15 M 13.8b 4712 F 14.6b

Eastern Chukchi Sea, Alaska 1989–06 26 M 12.8b

14 F 5.05b

Indo-Pacific humpback dolphin(Sousa chinensis)

NW Pacific Hong Kong 1995–01 8 M 1378 372 F 1135

1997–01 7 AM 1900 272002–07 17 3590 39

SW Pacific Queensland, Australia 1 2795 12Indian India 1992 2 AM 11 27

Irrawaddy dolphin(Orcaella brevirostris)

Indian Chilika Lake, BengalBay, India

2000–01 1 JM 1.2 483 AF 4.81 AM 18

Guiana dolphin(Sotalia guianensis)

SW Atlantic Sao Paulo, Brazil 1996–03 5 M 59.5 144 F 73.2

Striped dolphin(Stenella coeruleoalba)

NW Atlantic FL, U.S. 1994 1 AF 660 3NW Pacific Ehime, Japan 2003 6 AM 632 49

1 AF 84Taiji, Japan 1972–82 15 AM 272

NW Pacific Japan 1999 1 50.8 52 50Spinner dolphin(Stenella longirostris)

Indian India 1990–92 3 AM 6.8 28Tanzania 2000–02 4 AF 45,500 15

3 JF 46,00010 AM 101,6001 JM 52,000

NW Pacific Phillipines 1996 3 AM 36 27Atlantic spotted dolphin(Stenella frontalis)

SW Atlantic Sao Paulo, Brazil 1996–03 2 M 770 14SP and PR, Brazil 2004–07 1 AM 677 51

1 JM 4141 CM 1327

(continued on next page)

Melon-headed whale(Peponocephala electra)

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Table 1 (continued)

Species Area Locality Year n Sex/age classa PBDEs MeO-PBDEs Ref.e

2 AF 2352 JF 3571 CF 727

Atlantic white-sided dolphin(Lagenorhynchus acutus)

NW Atlantic Massachusetts, U.S. 1997 15 AM 1820 529 AF 61023 Ju 2400

NE Atlantic Faroe Islands 1997 3–5 M 230c 232001–02 3–5 M 673c

2006 3–5 M 279c

North Sea 1995 1 7777 53Pacific white-sided dolphin(Lagenorhynchus obliquidens)

NW Pacific Japan 1999 5 AM 690 27

Short-beaked common dolphin(Delphinus delphis)

NE Atlantic Irish 2001–03 5 AF 758 24France 2001–03 6 AF 612Spain 2001–03 8 AF 422

SW Pacific Queensland, Australia 1 5435 12Queensland, Australia 1 1960 13

Long-beaked common dolphin(Delphinus capensis)

NW Pacific Korea 2006 12 AM 1700 5410 AF 1600

Risso's dolphin(Grampus griseus)

NE Atlantic U.K. 2000 1 JF 850 10

Rough-toothed dolphin(Steno bredanensis)

NW Atlantic Massachusetts, U.S. 1997 6 AF 510 527 Ju 1360

SW Atlantic Sao Paulo, Brazil 1996–03 2 M 475 14Sowerby beaked-whale(Mesoplodon bidens)

NE Atlantic U.K. 1992–02 3 AM 659 106 AF 232

Stejneger's beaked whale(Mesoplodon stejnegeri)

NW Pacific Sea of Japan, Japan 2000–01 5 AM 530 27

Cuvier's beaked whale(Ziphius cavirostris)

NE Atlantic U.K. 2002 1 AM 355 10

Northern bottlenose whale(Hyperoodon ampullatus)

NE Atlantic U.K. 2001 1 JF 492 10

Pygmy sperm whale(Kogia breviceps)

NE Atlantic U.K. 1999 1 – 42 102002 1 AF 47

SW Pacific Queensland, Australia 1 2888 12Queensland, Australia 1 1470 13

Sperm whale(Physeter macrocephalus)

NE Atlantic North Sea 1995 3 AM 261 53

Narwhal(Monodon monoceros)

NW Atlantic Broughton Is., Canadian Arctic 2000 5 M 18.9 44

a M = male, F = female, Ju = juvenile, Ca = calf, NB = newborn, AM = adult male, AF = adult female, JM = juvenile male, JF = juvenile female, Ad = adult, CM = calfmale, CF = calf female, S resident = Southern resident, N resident = Northern Resident (see study).

b Median.c Median and pooled multiple samples.d Pooled multiple samples.e 1. Kuehl and Haebler (1995). 2. Kuehl et al. (1991). 3. Johnson-Restrepo et al. (2005). 4. Fair et al. (2007). 5. Fair et al. (2010). 6. Kucklick et al. (2011). 7. Yordy et al. (2010).

8. Litz et al. (2007). 9. Balmer et al. (2011). 10. Law et al. (2005). 11. Law et al. (2003). 12. Melcher et al. (2005). 13. Vetter et al. (2002). 14. Yogui et al. (2011). 15. Mwevura et al.(2010). 16. Weijs et al. (2009a). 17. Weijs et al. (2009b), 18. Weijs et al. (2010a). 19. Law et al. (2010). 20. Law et al. (2006). 21. Beineke et al. (2005). 22. Law et al. (2002).23. Rotander et al. (2012). 24. Pierce et al. (2008). 25. Weijs et al. (2010b). 26. Ikonomou et al. (2002). 27. Kajiwara et al. (2006a). 28. Rayne et al. (2004). 29. Krahn et al.(2007a). 30. Krahn et al. (2007b). 31. Krahn et al. (2009). 32. Haraguchi et al. (2009). 33. Kajiwara et al. (2006b). 34. Wolkers et al. (2007). 35. Ylitalo et al. (2009). 36. Ramuet al. (2005). 37. Ramu et al. (2006). 38. Park et al. (2010). 39. Lam et al. (2009). 40. Kajiwara et al. (2008). 41. Lindstrom et al. (1999). 42. Bloch et al. (2003). 43. Lebeufet al. (2004). 44. Tomy et al. (2008). 45. Kelly et al. (2008). 46. Villanger et al. (2011). 47. Hoguet et al. (2013). 48. Kannan et al. (2005). 49. Isobe et al. (2009). 50. Marshet al. (2005). 51. Leonel et al. (2012). 52. Tuerk et al. (2005). 53. deBoer et al. (1998). 54. Moon et al. (2010). 55. Weijs et al. (2013a,b).

Atlantic spotted dolphin(Stenella frontalis)

624 M.B. Alonso et al. / Science of the Total Environment 481 (2014) 619–634

2.1.1. Mysticete cetaceansPBDE concentrations were determined in four different mysticete

species: fin whales (Balaenopthera physalus), humpback whales(Megaptera novaeangliae), common minke whales (Balaenopteraacutorostrata) and sei whales (Balaenoptera borealis) from Northernhemisphere. For the Southern hemisphere, only the study on humpbackwhales from Antarctic waters was found (Dorneles et al., 2011).

Fig. 1 shows that male humpback whales from the Gulf of Maine,NW Atlantic collected in 2000s (Elfes et al., 2010) are the mysticetesthat have the highest PBDE concentrations in their blubber. They arefollowed by minke whales (of unknown gender) from the North Sea,sampled in the 1990s (deBoer et al., 1998) and by male minke whalesfrom Korean waters, collected in the 2000s (Moon et al., 2010). Maleminke whales from U.K. (Law et al., 2005) and male humpback whalesfrom California (Elfes et al., 2010) also presented high PBDE levels.

In general, humpback whales have higher PBDE concentrations thanminke Humpback whales feed intensely during the summer period inthe polar regions (Hogan and Cleveland, 2011). On the other hand,minke whales also feed on high latitudes in summer near estuaries, in-lets and inshorewaters. Therefore, attention is neededwhen comparingsuch species given that they have: 1) different feeding grounds, 2) dif-ferent migration patterns, 3) different life history traits, 4) differentmetabolic capacities and 5) potentially different PBDE congeners in-cluded in the sum of PBDEs in the different studies.

Humpback whales from North Atlantic have 95% of their diet basedon small fish from the Clupeidae, Gadidae and Ammodytidae families,while humpback whales from North Pacific feed primarily on pacificsaura (Cololabis saira), atka mackerel (Pleurogrammus azonus) and eu-phausiids (krill) (Hogan and Cleveland, 2011). The trophic level of thepreys directly influences the input of the contaminants in the predator

Table 2Mean PBDE and MeO-PBDE concentrations (ng/g lw) in blubber of mysticete cetaceans around the world.

Species Area Locality Year n Sex/age classa PBDEs MeO-PBDEs Ref.c

Fin whale(Balaenoptheraphysalus)

Mediterranean Pelagos Sanctuary, Italy 2008 6 M 15 16 F 210

NW Atlantic Gulf of Mexico 2008 3 M 302 F 15

NE Atlantic Iceland 1986–89 3 M, F 8.4b 22006–09 5 M, F 22b

U.K. 2000 1 JF 8.54 3Humpback whale(Megapteranovaeangliae)

NW Atlantic SW Gulf of Maine, U.S. 2005–06 10 M 870 4NE Gulf of Maine, U.S. 2005–06 10 M 900

NE Atlantic U.K. 2001 1 JM 14.5 3NE Pacific S California, U.S. 2004 5 M 180 4

N California, U.S. 2004 5 M 55Washington, U.S. 2004 10 M 100SE Alaska, U.S. 2003–04 10 M 22N Gulf of Alaska, U.S. 2004 8 M bLOQW Gulf of Alaska, U.S. 2004 9 M 8E Aleutian Is., U.S. 2004 10 M bLOQBering Sea, U.S. 2004 10 M bLOQ

Minke whale(Balaenopteraacutorostrata)

NE Atlantic Norway 1993 5–6 M 126b 21999 5–6 M 105b

Greenland 1998 4 F 71b

Iceland 2003–06 5 M 99b

U.K. 2000 1 JM 194 3North Sea 1995 1 871 5

NW Pacific Korea 2006 11 AM 270 67 JM 709 JF 100

Japan 1999 1 47 48 7Sei whale(Balaenopteraborealis)

NE Atlantic U.K. 2000 1 nd 3

LOQ= limit of quantification, nd = not detected.a M= male, F = female, AM= adult male, JM = juvenile male, JF = juvenile female.b Median and pooled multiple samples.c 1. Fossi et al. (2010). 2. Rotander et al. (2012). 3. Law et al. (2005). 4. Elfes et al. (2010). 5. deBoer et al. (1998). 6. Moon et al. (2010). 7. Marsh et al. (2005).

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organism. The current data seem to demonstrate higher trophic levels inthe prey of humpback whales from the North Atlantic, as suggested byElfes et al. (2010) or may reflect dissimilarities in the past use ofPBDEs in the countries of the North Atlantic and Pacific in the past.Therefore, more detailed studies are necessary to explain differencesin PBDE concentrations between North Atlantic and North Pacifichumpback whales.

Only two species of baleen whales have been analyzed for investi-gating PBDE concentrations in livers. The study of minke whales fromKorea was the only one that determined PBDE concentrations in bothblubber and liver of the same individuals. The results showed thatPBDE levels were higher in blubber than in liver (Moon et al., 2010).The same pattern was observed in common dolphins from Koreancoastal waters, since hepatic PBDE concentrations were several timeslower than the levels found in subcutaneous adipose tissue (Moonet al., 2010).

2.1.2. Odontocete cetaceansA total of thirty different odontocetes species have been analyzed to

determine PBDE levels in their blubber tissues (Table 1) and twentyspecies had their livers analyzed for the same purpose (Table 3). Sincemost of the studies focused on three species (bottlenose dolphin,Tursiops truncatus; harbor porpoise, Phocoena phocoena; and killerwhale, Orcinus orca), these cetaceans were used for comparing PBDElevels from different geographical areas.

There are threeNortheastern Pacific killerwhale ecotypes: residents,transients and offshores, which differ from each other fundamentallybecause of their diet and migration patterns. The residents belong to a“fish-eating” ecotype; the transients are “mammal-eating” individuals;and the offshore killer whales are the “fish and squid-eating” ecotype.They also differ in their genetics, acoustic behavior, morphology and

feeding ecology (Krahn et al., 2007a,b, 2009). Regarding the residents,there are the “Southern Resident” populations, which inhabit the regionbetween the Puget Sound, Washington State, and the Strait of Georgia,British Columbia, as well as the “Northern Resident” population,which inhabits an area that extends from the Strait of Georgia toVancouver Island, British Columbia (Rayne et al., 2004). Killer whalesfrom the Japanese coast could also belong to theNorthernResident pop-ulation, as their PBDE profile is very similar to the one found in commu-nities from the Northern Pacific and Norway (Haraguchi et al., 2009).

Southern Resident killer whales from the K-pod had the highestPBDE levels (up to 15,000 ng/g lw) among North Pacific ecotypes(Krahn et al., 2007a). As the authors suggested, this population probablyfeeds on the coast of California, a disturbed and industrialized area onthe US coastline. Evidences include several sightings of the SouthernResident K-pod individuals off the coast of California and a typical“Californian signature” from POPs, which can be exemplified by a rela-tively high DDTs/PCBs ratio, a pattern that is similar to the one foundin Chinook salmon from this area (Krahn et al., 2007a, 2009) (Fig. 2).

The Southern residents also presented the highest PBDE con-centrations reported in any environmental sample analyzed so far(15,000 ng/g lw in a juvenile male), showing that these killer whalesare highly contaminated and at risk of adverse health effects (Krahnet al., 2007a). To the authors' knowledge, only one study reported healtheffects related to PBDE levels in marine mammals. Hall et al. (2003) re-ported alterations in thyroid hormone levels when PBDE concentrationsin the blubber of gray seals (Halichoerus grypus) ranged between 61 and1500 ng/g lw. Although phocids and odontocetes have differentmetabolization capabilities, seals are the closest marine mammal forwhich data on the health impact of PBDE exposure are available. The dif-ference inmetabolic biotransformation capacity of organic contaminantsbetween pinnipeds and cetaceans was investigated by some studies

Table 3Mean PBDE and MeO-PBDE concentrations (ng/g lw) in liver of cetaceans around the world.

Species Area Locality Year n Sex/age classa PBDEs MeO-PBDEs Ref.d

Harbor porpoise(Phocoena phocoena)

NE Atlantic North Sea 1990–98 3 Ca 485b 43b 11 Ad 1552b 100b

2000–08 8 Ca 337b 70b

3 Ju 318b 120b

2 Ad 426b 43b

Belgian North Sea 1997–00 21 229 2Black Sea 1998 10 AM 45a 18b 3

8 JM 44 22Finless porpoise(Neophocaena phocaenoides)

NW Pacific Hong Kong 2000–01 2 M 270 41 F 380

Franciscana dolphin(Pontoporia blainvillei)

SW Atlantic Espirito Santo, SE Brazil 1994–09 2 AM 103 1726 54 JM 201 55372 CM 89 28462 AF 293 2168

Rio de Janeiro, Brazil 1994–09 3 JF 33 839Sao Paulo, SE Brazil 1994–09 1 – 37 280

4 AM 130 2162 JM 74 1933 AF 22 742 JF 389 2861 CF 46 131

Paraná, S Brazil 1994–09 1 AF 22 1412 CF 82 378

Santa Catarina, S Brazil 1994–09 4 JM 718 8553 CM 514 5113 AF 62 424

Rio Grande do Sul, S Brazil 1994–09 4 AM 36 3633 JM 42 3444 JF 39 223

Guiana dolphin(Sotalia guianensis)

SW Atlantic Rio de Janeiro, Brazil 1994–06 13 M 670 150 66 F 160 751 NB 242 3310 M, F 259 7

Indo-Pacific humpback dolphin(Sousa chinensis)

NW Pacific Hong Kong 1995–01 2 M 520 41 F 340

Atlantic Spotted dolphin(Stenella frontalis)

SW Atlantic Rio de Janeiro, Brazil 1994–06 6 M 1150 19,200 6

Spotted dolphin(Stenella attenuata)

SW Atlantic Rio de Janeiro, Brazil 1994–06 1 M 1215 88,200 6

Striped dolphin(Stenella coeruleoalba)

Mediterranean Italy 1990–92 3 M 5532 123 82 F 764 124

SW Atlantic Rio de Janeiro, Brazil 1994–06 1 – 210 6900 6NW Pacific Japan 1999 1 233c 540c 9

Rough-toothed dolphin(Steno bredanensis)

SW Atlantic Rio de Janeiro, Brazil 1994–06 1 M 360 3900 62 F 1150 15,200

Short-beaked common dolphin(Delphinus delphis)

SW Atlantic Rio de Janeiro, Brazil 1994–06 1 M 240 3700 61 F 125 2900

Long-beaked common dolphin(Delphinus capensis)

NW Pacific Korea 2006 12 AM 170 1010 AF 200

Bottlenose dolphin(Tursiops truncatus)

Mediterranean Italy 1990–92 3 M 294 52 81 F 85 97

SW Atlantic Rio de Janeiro, Brazil 1994–06 3 M 960 19,900 6Fraser's dolphin(Lagenodelphis hosei)

SW Atlantic Rio de Janeiro, Brazil 1994–06 2 M 22 2310 67 F 7 1000

Atlantic white-sided dolphin(Lagenorhynchus acutus)

NE Atlantic North Sea 1995 1 114 11

Irrawaddy dolphin(Orcaella brevirostris)

Indian Chilika Lake, Bengal Bay, India 2000–01 1 AF 0.71 121 JM 1.3

Beluga(Delphinapterus leucas)

NW Atlantic St. Lawrence, Canada 2000–03 6/2 M, F 2210 25 13W Hudson Bay, Canadian Arctic 2002–03 11/2 M, F 53 43E Hudson Bay, Canadian Arctic 17/14 M 18 310 14St. Lawrence, Canada 1993–07 33 M 404 15

32 F 489Sperm whale(Physeter macrocephalus)

NE Atlantic North Sea 1995 1 AM 18 11

Long-finned pilot whale(Globicephala melas)

Mediterranean Italy 1990–92 1 M 483 81 8

Risso's dolphin(Grampus griseus)

Mediterranean Italy 1990–92 2 M 2388 164 81 F 2917 795

False killer whale(Pseudorca crassidens)

SW Atlantic Rio de Janeiro, Brazil 1994–06 2 NB 3600 148,700 6

Fin whale(Balaenopthera physalus)

Mediterranean Italy 1990–92 1 F 886 127 8

Minke whale(Balaenoptera acutorostrata)

NW Pacific Korea 2006 11 AM 40 107 JM 8.19 JF 20

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2008

2008

2005-06

1986-89

2001

1998

2000

1999

2008

2008

2005-06

2006-09

2003-06

2006

2004

1999

2006

2004

1993

2006

2004

2000

2004

1995

2004

0 100 200 300 400 500 600 700 800 900

Fin

Fin

Humpback

Fin

Humpback

Minke

Sei

Minke

Humpback

Med

iter

rane

anN

W A

tlant

icN

E A

tlant

icN

WP

acifi

cN

EP

acifi

c Male

Female

No sex defined

Male and Female

(ng/g

Fig. 1. PBDE mean concentrations (ng/g lw) in the blubber of mysticete species according to sex, year and locations in the published literature. References in the text.

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(Weijs et al., 2009b; Pangallo and Reddy, 2010). As suggested byPangallo and Reddy (2010), the contaminants in the blubber of pinni-pedsmaybemore available formetabolism, beingmore readily removedfrom the body. Other facts that support this hypothesis are that the bodyburden of organic contaminants was lower in seals than in their prey(Pangallo and Reddy, 2010). In addition, comparing sympatric seal andporpoise populations with similar feeding habits, the cetaceans showedhigher contaminant levels than the pinnipeds (Weijs et al., 2009b).

If we use the levels associated with endocrine disruption in grayseals in order to have a comparison ground for killer whale populationsfrom NE Pacific, PBDEmean concentrations are above the upper limit ofthreshold (1500 ng/g lw; Hall et al., 2003; Fig. 2). This suggests that at-tention should be given to these populations of large marine predatorsfrom the NE Pacific with alarming levels of PBDEs.

The bottlenose dolphin (Tursiops truncatus) is a cosmopolitan apexpredator that inhabits estuarine and near-shore waters. This dolphinhas been extensively used as indicator of the trophic flow of POPs incoastal ecosystems (Fair et al., 2010; Kucklick et al., 2011; Balmeret al., 2011). The U.S. Atlantic coast was broadly sampled using blubberof bottlenose dolphins to evaluate PBDE contamination. The first studywas conducted with animals sampled in 1987 (Kuehl et al., 1991).Since then, many other studies have been performed using remote bi-opsies from live animals or samples from stranded or bycaughtbottlenose dolphins (Kuehl and Haebler, 1995; Johnson-Restrepoet al., 2005; Litz et al., 2007; Fair et al., 2007, 2010; Yordy et al., 2010;Kucklick et al., 2011; Balmer et al., 2011). The highest PBDE concentra-tionswere found in dolphins fromCapeMay, Charleston, Sapelo,Missis-sippi Sound and Brunswick; from U.S. coast, and according to theauthors the results suggested a broader scale contamination possiblyfrom atmospheric deposition (Kucklick et al., 2011). In bottlenose

Notes to Table 3:a M = male, F = female, Ju = juvenile, Ca = calf, NB = newborn, AM = adult male, AF

CF = calf female.b Median.c Cooked liver.d 1.Weijs et al. (2010a). 2. Covaci et al. (2002). 3.Weijs et al. (2010b). 4. Ramu et al. (2005).

(2004). 9. Marsh et al. (2005). 10. Moon et al. (2010). 11. deBoer et al. (1998). 12. Kannan et a

dolphins from Charleston harbor estuary, PBDE levels exceeded thosefound in resident adult male killer whales from NW Pacific (Krahnet al., 2007a,b). In addition, those bottlenose dolphins provided PBDElevels that were 6-fold higher than those found in killer whales fromNE Pacific (Rayne et al., 2004). A possible explanation for this lies inthe fact that Charleston is a highly urbanized area, thereby contributingto a large input of PBDE in these dolphins (Fair et al., 2010). The concen-trations in Charleston dolphins constituted some of the highest PBDElevels measured in cetaceans (up to 7055 ng/g lw). As suggested bythe authors, these extremely high concentrationswarrant further inves-tigation on the potential deleterious effects of these bioaccumulativetoxicants (Fair et al., 2007, Fig. 3).

Other marine waters, such as the NE and SW Atlantic, as well as theSW Pacific, were investigated by few studies. The PBDE concentrationsin bottlenose dolphins fromU.K. had alarming levels, similar to dolphinsfrom South Carolina (levels ranged from 7040 to 8880 ng/g lw; Lawet al., 2005). Comparing hemispheres, in general, cetaceans from thesouth half of the planet had significantly lower PBDE levels (p =0.025) than those from Northern hemisphere (Fig. 4). These compari-sons can be clearly observed when it is taken into account thatbottlenose dolphins from Australia and Brazil presented PBDE levelstwo orders of magnitude lower than those from North Atlantic (Lawet al., 2003; Yogui et al., 2011, Table 2).

There are several studies with harbor porpoises in NE Atlantic coastand the populations from North Sea (Pierce et al., 2008; Weijs et al.,2009a, 2010a), U.K., England, Wales (Law et al., 2002, 2010; Pierceet al., 2008) and France (Pierce et al., 2008) presented the highestPBDE concentrations, reflecting the use of these endocrine disruptorscompounds in these countries and their surrounding waters, as sug-gested by the authors. Weijs et al. (2010a) analyzed harbor porpoises

= adult female, JM = juvenile male, JF = juvenile female, Ad = adult, CM = calf male,

5. Alonso et al. (2012). 6. Dorneles et al. (2010). 7. Quinete et al. (2011). 8. Pettersson et al.l. (2005). 13. Mckinney et al. (2006). 14. Kelly et al. (2008). 15. Raach et al. (2011).

Fig. 2. PBDEmean concentrations (ng/g lw) in the blubber of killer whale ecotypes (Northern and Southern residents, offshores and transients) from NW and NE Pacific Ocean. The traceline indicates the upper level of threshold that presented health effects in gray seals (Hall et al., 2003). For reference see the manuscript text.

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(neonates, calves, juveniles and adults) from European North Sea andconcluded that the youngest animals from that population, the calves,are probably the most vulnerable individuals because they do nothave a well developed mechanism for metabolic biotransformation ofcontaminants.

The false killer whales (Pseudorca crassidens) from the HawaiianIslands belong to a resident population and high PBDE levels (up to

Fig. 3. PBDEmean concentrations (ng/g lw) in the blubber of bottlenose dolphins (Tursiops trunthat presented health effects in gray seals (Hall et al., 2003). References in the text.

2900 ng/g lw) were found in “healthy” free-ranging whales. Thisstudy showed that subadults had major concentrations than adults,and possibly the PBDE source may be the effluents from wastewatertreatment plants in Hawaiian coastal areas (Ylitalo et al., 2009).

The Faroe Islands have a resident population of long-finned pilotwhale (Globicephala melas) in their waters, which has presented highPBDE concentrations in the blubber, with means ranging from 77 to

catus) fromAtlantic and Pacific Oceans. The trace line indicates the upper level of threshold

1 10 100 1000 10000

South

North

PBDEs (ng/g lw)

Hem

isp

her

e *

*

1 10 100 1000 10000 100000

South

North

MeO-PBDEs (ng/g lw)

Hem

isp

her

e *

*

Fig. 4. Log PBDE andMeO-PBDEmean concentrations (ng/g lw) in cetacean blubbers fromNorthern andSouthernhemisphere according to thepublished data. *Statistically different(p b 0.05).

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3160 ng/g lw. The authors suggested that these endocrine disruptorscan probably be transported from industrialized countries in temperateregions by atmospheric currents reaching the polar regions as PCBs(Rotander et al., 2012).

Asian countries were responsible for 40% of PBDE consumption inthe global market in 2001 (BSEF, 2004). Due to China that is the world'slargest manufacturing industry of electronics and electrical productsand the growing Chinese economy in the last decades, PBDE residuelevels in their environment have been increased (Ramu et al., 2006).This fact is reflected in the tissues of marine top predators from Asia,such as finless porpoise (Neophocaena phocaenoides) and Indo-Pacifichumpback dolphins (Sousa chinensis), which reached PBDE concentra-tions ranging around 3000 ng/g lw (Lam et al., 2009). The highest levelswere found in dolphins from Hong Kong followed by Japan and Korea(Ramu et al., 2005, 2006; Kajiwara et al., 2006a; Park et al., 2010). Con-sidering these facts and as suggested by Kajiwara et al. (2006b), PBDEsshould be considered as an increasing pollution problem in the Asia-Pacific region.

Considering that these bioaccumulative chemicals have propertiesthat could cause many deleterious effects in immune, reproductiveand nervous systems of mammals, continuous studies are required toaccurately evaluate the potential risks to cetacean species around theoceans from exposure to these contaminants.

2.2. Time trends

PBDEs were first detected in the environment at the end of 1970s(DeCarlo, 1979), but the first report with PBDEs in cetaceans tissueswas published almost ten years after when these compounds were an-alyzed in bottlenose dolphins fromVirginia, U.S. (Kuehl et al., 1991). Thementioned study is the only one that analyzed odontocete samples from1980s and in the following decades many studies have been conducted,thus enabling temporal comparisons.

The historical records of legacy POPs (PCBs and DDTs) showed a de-creasing trend in the environment and in mammals, due to the

prohibition of its manufacture and use in many countries (Kajiwaraet al., 2008). In contrast, PBDE concentrations showed an exponentialgrowth over the past decades (Lebeuf et al., 2004; Rayne et al., 2004;Tanabe et al., 2008; Kajiwara et al., 2008).

Few studies reported the temporal trends of PBDEs in cetacean sam-ples. According to Kajiwara et al. (2006a) and Ramu et al. (2006), whostudied PBDE residue levels in finless porpoises collected in SouthChina Sea coast from 1990 to 2000/01, the PBDE values increasedabout five times during the past decade. Tanabe (2008) showed apeak of the PBDE usage in Japan in the 1990s followed by a levelingoff and an increase in the proportion of higher brominated BDEs in re-cent years in environment samples as well as in cetaceans, probablydue to prohibitions of Penta- and Octa-BDE commercial mixtures.Kajiwara et al. (2008) found PBDE levels in melon-headed whales(Peponocephala electra) collected from the coast of Japan in 2001–02significantly higher than in 1982 (p b 0.01), showing a tenfold increasein the last decade in this Asian country.

Concentrations of PBDEs in beluga whale (Delphinapterus leucas)from the resident population in St. Lawrence Estuary, Canada, a highlypopulated and industrialized urban area, showed an exponential in-crease throughout 1988–1999, and the concentrations increased 200%over those last five years in the blubber of the whales (Lebeuf et al.,2004). This beluga population is widely studied and presented highlevels of PBDEs and the classical POPs, with concentrations up to 30fold higher in blubber and liver tissues, compared to those from Canadi-an Arctic and Alaskan population (McKinney et al., 2006; Tomy et al.,2008; Kelly et al., 2008; Hoguet et al., 2013). Another study with thesame beluga population from St. Lawrence Estuary showed thatmean PBDE ratios in blubber of males increased 12.7 ± 2.4% yearly(p b 0.05) between 1993 and 2007 (Raach et al., 2011). Until the1990s PBDEs had not been regulated in Canada, which resulted inhigh concentrations in the whale tissues from this estuary. The Bromi-nated Science and Environmental Forum (BSEF) member companiesin U.S. voluntarily phased out the production and use of the Penta-and Octa-BDE in 2004, and of Deca-BDE in 2012 in cooperation withU.S. EPA (BSEF, 2013). In Canada, a global program to reduce emissionsof brominated flame retardants from manufacturing facilities is incourse tomonitor and reduce emissions of these chemicals in industrialsettings to provide basis for an Environmental Performance Agreement(EPA) with Environment Canada (BSEF, 2013).

Alaskan beluga populations were also studied in relation to timetrends of these contaminants from 1989 to 2006 and again significanttemporal increases in concentrations of PBDEs were observed (Hoguetet al., 2013). Some investigations believed that the growth rate of thispopulation could have been limited by the presence of elevated POPlevels in their tissues (Lebeuf et al., 2004). The toxicological implicationsof these bioaccumulative contaminants in beluga whales are stillunknown and the potential impact on cetacean and human healthstill exists and should be considered, as indicated by Hoguet et al.(2013).

Law et al. (2010) analyzed levels and trends of PBDEs in harbor por-poises from the U.K. from the 1990s until the late 2000, and suggestedthat median concentrations peaked around 1998 and decreased from50 to 70% until 2008. However, this downward trend has not been ob-served in temporal trend studies with cetaceans from North Americaand Asia. In these cases, the tendency was to increase exponentiallyeach decade since the 1980s until nowadays, as observed by Shaw andKannan (2009) in an extensive review about PBDEs in marine ecosys-tems from America.

Rotander et al. (2012) analyzed PBDE concentrations in marinemammal tissues from Arctic and North Atlantic in order to understandthe dynamic of these compounds from 1986 until 2009. The conclusionwas that the highest concentrations were from the late 1990s or begin-ning of 2000 and these levels may possibly be reflecting the increasingtrade and global usage of PBDEs in the 1990s. The higher brominatedcongeners, such as BDE-153 and -154 were found in increased levels

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relative to total PBDE in samples from recent years, suggesting an in-crease in exposure to these chemicals until 2000, probably reflecting adecrease in use of penta and octa-BDEmixtures banned in the countriesof North Atlantic. Meanwhile, deca-BDE increases continuously in theU.S. (Arias, 2001).

These time trend studies indicated that PBDE concentrations in ceta-ceans from Japan, China, U.S. and Canada coastal zone have increasedsignificantly over the past 30 years. Temporal variations in the concen-trations of these contaminants were consistent with their historicalconsumption in these countries. These observations are in agreementwith other studies that showed increased PBDE concentrations inmany regions during the last decades (Hites, 2004; Ramu et al., 2006).The studies that showed a decrease and/or stability of PBDE levels incetacean tissues in recent decades in relation to 1990s were from U.K.waters (Law et al., 2010) and NE Atlantic (Rotander et al., 2012),reflecting the prohibition of these toxic compounds in Europe in thelast years.

3. MeO-PBDEs in cetaceans

The majority of the studies that analyzed naturally-producedorganobrominated compounds in cetacean tissues focus mainly ontwo congeners, 6-MeO-BDE-47 and 2′-MeO-BDE-68. In order to com-pare the published data, Tables 1 to 3 showed the mean concentrationsof ΣMeO-PBDEs (as the sum of these 2 congeners). All the datadiscussed here were expressed in lipid weight (lw). For the studies inwhich MeO-PBDEs data were reported in wet weight, concentrationswere re-calculated in lw applying a mean of 70% of lipid content inthe blubber of cetaceans, as suggested by Tanabe et al. (1994).

3.1. Blubber and liver concentrations

Similar to PBDEs, themajor part of the data found in the literature forMeO-PBDE compounds in cetaceans were analyzed in the blubber andliver samples. A total of 12 studies in these two organs from cetaceansaround the world were found in published papers or available via jour-nal websites, from October 2002 to April 2013. Only three studies ana-lyzed other tissues, such as kidney, brain and liver of harbor porpoisesfrom Black and North Sea (Weijs et al., 2010a,b) and blood from ceta-ceans along Japanese waters (Nomiyama et al., 2011). Tables 1 and 2presented the data of MeO-PBDEs in cetacean blubber samples andTable 3 showed the data of these natural compounds in cetacean liversamples.

The higher MeO-PBDE concentrations in the blubber of cetaceanswere found in Indo-Pacific bottlenose dolphin (T. aduncus) and spinnerdolphins (Stenella longirostris), from Tanzania, Indian Ocean, with adultmales reaching concentrations up to 151,250 and 101,600 ng/g lw, re-spectively (Mwevura et al., 2010). These biogenic brominated organiccompounds were found at high levels, up to two orders of magnitudehigher than the most contaminated cetaceans by anthropogenicpolybrominated diphenyl ethers (PBDEs), the Southern resident Killerwhales from Puget Sound (Krahn et al., 2007b, 2009).

Similarly as it occurs to other organohalogenated compounds, themature male dolphins presented higher levels of the naturally bromi-nated compounds compared with adult females, as a result of maternaltransfer (Alonso et al., 2012; Dorneles et al., 2010; Mwevura et al.,2010). Newborns and calves are exposed to comparable or higher con-centrations of these compounds than adults, receiving high loadsthrough their mothers at critical stages of development, potentiallyplacing them at a disproportionate risk for the effects on their healthand on the population as a whole (Haraguchi et al., 2009; Weijs et al.,2010a).

In cetaceans from Queensland, NE Australia (SW Pacific) MeO-PBDElevels ranged between 1470 and 5435 ng/g lw in the blubber ofbottlenose dolphins, melon-headed whales (Peponocephala electra),Indo-Pacific humpback dolphins (Sousa chinensis), short-beaked

common dolphins (Delphinus delphis) and pygmy sperm whales(Kogia breviceps) (Vetter et al., 2002; Melcher et al., 2005). This dataneed to be analyzed carefully due to the small sample size. The authorsfound similar MeO-PBDE profile in marine sponges Dysidea sp.,cyanobacteria, nudibranchs andmollusks located in the area. Themech-anism of howMeO-PBDE reaches the top predators has been elucidated,and evidence points absorption from food, such as it occurswith the an-thropogenic PBDEs (Kelly et al., 2008). Comparisons ofMeO-PBDE levelsin cetaceans and herbivores, as dugongs and green turtles, have shownthat the latter group possessed 1 to 10% lower concentrations in theirtissues (Vetter et al., 2002).

The MeO-PBDE concentrations in liver samples in cetaceans thatinhabit the continental shelf and oceanic environments near to Rio deJaneiro, Southeastern off Brazil (SWAtlantic) are among the highest de-tected to date (up to 250,000 ng/g lw). The continental shelf odontoceteanalyzedwere false killer whale newborn (148,700 ng/g lw), bottlenose(19,900 ng/g lw), Atlantic-spotted S. frontalis (19,200 ng/g lw) andrough-toothed dolphins (Steno bredanensis) (15,200 ng/g lw). Also theoffshore dolphin species such as spotted S. attenuata (88,200 ng/g lw)and spinner S. longirostris (38,000 ng/g lw) presented very high levelsof MeO-PBDEs in their livers (Dorneles et al., 2010).

Also in southeastern Brazil on the coast of Espírito Santo, the littledolphin franciscana had mean levels of MeO-PBDE ranging 1839–5737 ng/g lw, and in juveniles there were concentrations up to14,000 ng/g lw (Alonso et al., 2012). The hypothesis linking the toothedcetaceans from Brazilian tropical zone (between Rio de Janeiro andEspírito Santo waters), and very high levels of methoxylated-PBDEs isan oceanographic phenomenon and a biological feature. The southeast-ern coast of Brazil is the stage of an important upwelling phenomenon(RJ coast) and shelters the largest coral reef complex in WesternSouth Atlantic. It also has a big rhodolith area (ES coast) that is consid-ered one of the largest rhodolith beds in the world (Costa andFernandes, 1993; Foster, 2001; Leão et al., 2003).

These characteristics might be contributing to the significantamount of naturally-produced organobrominated compounds in thistropical area of the South Atlantic. Advection by upwelling is an impor-tant key in redistribution of organic compounds, in particular fornektonic organisms. And coral reefs are a refuge for many marineorganohalogenated synthesizers, such as Dysidea sp. and other spongesand red algae, as well as many mollusks and nudibranchs. The factsdescribed above render the methoxylated-PBDEs bioavailable to ma-rine food chain, biomagnifying until it reaches the cetaceans, as sug-gested by Kelly et al. (2008), Weijs et al. (2009b) and Losada et al.(2009).

Analyzing all the data of MeO-PBDE concentrations in cetaceans, it isclear that the highest levels were found in samples of tropical–equato-rial waters from the Southern hemisphere (Fig. 4), as SW Pacific (NEAustralia, 19°S) (Vetter et al., 2002; Melcher et al., 2005), SW Atlantic(SE Brazil, 19°S–22°S) (Alonso et al., 2012; Dorneles et al., 2010) andW Indian (Tanzania, 06°S) (Mwevura et al., 2010). All samples fromthe studies mentioned above are located near reef areas (Great Barrierin Australia; Abrolhos Bank, Brazil and Tanzania's reef) and are subjectto the upwelling phenomenon (Fig. 5). This fact suggests a possiblemore intense biosynthesis of MeO-PBDEs and/or bioavailability ofthese compounds in those regions possessing these characteristics, aspointed by Dorneles et al. (2010) and Alonso et al. (2012).

Mean concentrations of MeO-PBDE in Southern hemisphereodontocetes were significantly different than in the Northern hemi-sphere (p b 0.02, Fig. 4). The data of cetaceans from Northernhemisphere were collected only in temperate and polar waters, like inEurope (Mediterranean, North Sea and Black Sea), North Asia (NorthernJapan), North America (Canada) and the Arctic. It would be interestingif the cetaceans that inhabit waters near coral reef areas from North-ern hemisphere were contemplated in future work, in order to com-pare the data with the cetaceans of these areas from Southernhemisphere.

Fig. 5.Map showing (A) PBDE and (B) MeO-PBDE studies reporting concentration levels in blubber and liver tissues of cetaceans along the oceans and seas over the world.

631M.B. Alonso et al. / Science of the Total Environment 481 (2014) 619–634

Among the baleen whales, only two papers analyzed MeO-PBDElevels, one Mediterranean female fin whale that liver was analyzed(127 ng/g lw) (Pettersson et al., 2004) and aminkewhale (Balaenopteraborealis) from Japan that blubber was analyzed (48 ng/g lw) (Marshet al., 2005). The levels of MeO-PBDEs in baleen whales were in thesame order of magnitude compared with those obtained in toothedwhales of the same regions, thus indicating the presence of suchchemicals in the marine environment at different trophic levels(Pettersson et al., 2004).

Finally, it should be pointed out that only few studies exist in whichother methoxylated-PBDE congeners were analyzed in cetacean blub-ber and liver. Two studies described the presence of additional peakscorresponding to MeO-PBDE congeners, but without a specific identifi-cation of each one (Dorneles et al., 2010; Pettersson et al., 2004) andtwo works identified other MeO-PBDE congeners in cetaceans fromtropical waters, two tetrabrominated congeners (5-MeO-BDE 47 and4′-MeO-BDE 49) and four pentabrominated (5′-MeO-BDE 100, 4′-MeO-BDE-103, 5′-MeO-BDE 99, 4′-MeO-BDE 101) from SE Braziliancoast (Alonso et al., 2012) and five tribrominated congeners (2-MeO-BDE 39, 2′-MeO-BDE 28, 6-MeO-BDE 28, 6′-MeO-BDE 17, 6-MeO-BDE17) from NE Australian coast (Melcher et al., 2005).

The data showed that cetaceans accumulate natural brominatedphenoxyanisoles at surprising levels; therefore it is interesting to deter-mine whether this bioaccumulation represents potential health risks tothese animals or if they are adapted to chronic exposure to these natural

compounds, aswell as Vetter et al. (2002) commented in hiswork. Afterall, the two mainly MeO-PBDEs congeners (2′-MeO-BDE-68 and6-MeO-BDE-47) demonstrated to cause multiple endocrine-disruptingeffects in tests with mammals in a recent report (Hu et al., 2011).More studies focused on methoxylated naturally-produced brominatedcompounds are necessary to understand their mechanisms and effectsin marine mammals' health such as in humans.

4. Conclusions

Numerous published studies indicated that PBDE levels in cetaceanswere higher in the Northern hemisphere while the naturally-producedbrominated MeO-PBDE levels were significantly higher in Southernhemisphere cetaceans. PBDEs were broadly produced and used in thepast in highly industrialized regions, but nowadays they are still usedin some areas of the world where the ban is not yet effective or notoccurred. It is expected that the continued use of these pollutants willbe reflected in the concentration levels in marine top predators withina certain period of time.

It is very important to continue the monitoring programs on PBDElevels in cetaceans, in order to determine a potential concentrationlevel decline in those geographical areas in which PBDEs have been al-ready banned. And in turn, to assess whether there is an increase ofthe levels in other areas where pollutants are still produced and usedwithout restrictions.

632 M.B. Alonso et al. / Science of the Total Environment 481 (2014) 619–634

Themonitoring of the PBDEs in cetaceans around theworld needs tocontinue to understand the time trends, the most affected species andareas, and effects that these contaminants could have in cetacean me-tabolism. Potential health risks from exposures to PBDEs in mammalsinclude a variety of biological effects (e.g., thyroid disruption, neurobio-logical development and fetal toxicity/teratogenicity) and many of thestudies listed in the present review found concentrations of PBDEshigher than the upper threshold level related to alterations in thyroidhormone in marine mammals.

More information is required for the naturally occurring MeO-PBDEs. These compounds should be included in monitoring programs,as well as toxicological studies on their possible effects, since publisheddata have demonstrated high levels in cetaceans from some areas, oftenhigher than PBDE levels. MeO-PBDEs presented the higher concentra-tion in cetaceans from southern hemisphere that inhabits waters nearcoral reefs and banks. More studies are needed to understand thedynamics of these naturally-produced brominated compounds in themarine ecosystem.

Acknowledgments

This work was supported by the Ministry of Education of Brazil —CAPES (fellowship to M.B. Alonso “Sandwich Programme” — PDEE),Brazilian Research Council — CNPq (grant #304826/2008-1), Rio deJaneiro State Government Research Agency — FAPERJ (Jovem Cientistado Nosso Estado #101.449/2010), Mount Sinai School of Medicine(NY/USA), and Fogarty International Center NIH/USA (grant1D43TW0640). AFA and JL-B have research grant from CNPq (PQ-2)and FAPERJ (JCNE). The authors are thankful to the anonymous re-viewers of the manuscript.

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