Science of the Total Environment 472 (2014) 194–203

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Organochlorine concentrations (PCBs, DDTs, HCHs, HCB and MIREX) indelphinids stranded at the northeastern Brazil

Elitieri B. Santos-Neto a,b,⁎, Claudio Eduardo Azevedo-Silva a, Tatiana L. Bisi a, Jessica Santos a,Ana Carolina O. Meirelles c, Vitor L. Carvalho c, Alexandre F. Azevedo a,José Eugênio Guimarães b,d, José Lailson-Brito a

a Laboratório de Mamíferos Aquáticos e Bioindicadores Professora Izabel Gurgel (MAQUA), Faculdade de Oceanografia, Universidade do Estado do Rio de Janeiro, Brazilb Programa de Pós-graduação em Saúde Animal nos Trópicos, Escola de Medicina Veterinária e Zootecnia, Universidade Federal da Bahia, Brazilc Associação de Pesquisa e Preservação de Ecossistemas Aquáticos (AQUASIS), Caucaia, Ceará, Brazild Departamento de Anatomia, Patologia e Clínicas/DEAPAC, Universidade Federal da Bahia, Brazil

H I G H L I G H T S

• The highest OCs levels were found in Guiana dolphins from the Metropolitan region.• Guiana and spinner dolphins showed predominantly ∑PCB, followed by ∑DDT and Mirex.• ∑DDT was the main compound found in Fraser's, Atlantic spotted and striped dolphins.• PCB congeners with high chlorination levels dominated every species.• Discriminant analysis showed distinct organochlorine accumulation pattern among delphinids.

⁎ Corresponding author at: Laboratório de Mamíferos AqIzabel Gurgel” (MAQUA), Faculdade de Oceanografia, UnJaneiro, 20530-013, Rio de Janeiro, RJ, Brazil. Tel.:+55 21 23

E-mail addresses: neto.vet@gmail.com (E.B. Santos-Ne(C.E. Azevedo-Silva), tbisi@yahoo.com (T.L. Bisi), jessicasicameirelles@yahoo.com.br (A.C.O. Meirelles), vitorluz@yaazevedo.alex@uerj.br (A.F. Azevedo), jeugenio@ufba.br (J.(J. Lailson-Brito).

0048-9697/$ – see front matter © 2013 Elsevier B.V. All rihttp://dx.doi.org/10.1016/j.scitotenv.2013.10.117

a b s t r a c t

a r t i c l e i n f o

Article history:Received 21 August 2013Received in revised form 16 October 2013Accepted 29 October 2013Available online xxxx

Keywords:Guiana dolphinBioaccumulationCetaceansOrganochlorinesDiscriminant analysis

Organochlorine compounds are highly persistent in the environment, causing bioaccumulation and bio-magnification through the marine food chain. To verify the bioaccumulation pattern of DDT and its metabolites,as well as PCBs, Mirex, HCHs and HCB, samples of subcutaneous adipose tissue from 25 Guiana dolphins (Sotaliaguianensis), two Fraser's dolphins (Lagenodelphis hosei), two spinner dolphins (Stenella longirostris), one spotteddolphin (Stenella frontalis), and one striped dolphin (Stenella coeruleoalba) were analyzed. The collected speci-mens were found stranded in northeastern Brazil between 2005 and 2011. The concentrations were reportedin μg·g−1 lip, varying from 0.02 to 17.3 for ΣPCB, from 0.003 to 5.19 for ΣDDT, from 0.005 to 0.16 for ΣHCH,from 0.002 to 0.16 for HCB, and from 0.02 to 2.38 for Mirex. The PCBs dominated the bioaccumulation patternfor both the Guiana and spinner dolphins; for the other species, DDT was the major compound. A discriminantfunction analysis revealed the differences in the organochlorine accumulation patterns between the Guiana dol-phin (S. guianensis) and the continental shelf/oceanic dolphins (S. frontalis and S. longirostris). The results alsoshow that the concentrations of organochlorine compounds found in the delphinids in northeastern Brazilwere lower than the delphinids found in other regions of Brazil, aswell as other locationsworldwidewith intenseagroindustrial development and/or a larger population.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

Organochlorines are stable, lipophilic compounds with numerousindustrial and agricultural uses in recent decades (O'Shea, 1999). The

uáticos e Bioindicadores “Profa.iversidade do Estado do Rio de340065; fax:+552123340621.to), azevedo.silva@gmail.comlvauerj@gmail.com (J. Santos),hoo.com.br (V.L. Carvalho),E. Guimarães), lailson@uerj.br

ghts reserved.

oceans are the final destination for many of these compounds (Weber,1992). These compounds integrate with organic matter and aresubsequently absorbed by plankton, leading to bioaccumulation andbiomagnification throughout the marine food chain (Gray, 2002). Be-cause they occupy the top of the marine food chain, marine mammalsabsorb high levels of organochlorine compounds, exposing them toneurological, endocrine, immunological and neoplastic effects (Gregoryand Cyr, 2000; Reijnders, 2000).

In the Southwestern Atlantic, the measurement of organochlorinecompounds in cetaceans is currently limited to the southeastern andsouthern areas of Brazil, Uruguay and Argentina (O'Shea et al., 1980;Colombo et al., 1990; Corcuera et al., 1995; Lailson-Brito et al., 2010,

195E.B. Santos-Neto et al. / Science of the Total Environment 472 (2014) 194–203

2012). Few studies have examined organochlorine compounds in thecontext of the aquatic biota in northeastern Brazil; the existing studiesutilized birds (Weber, 1983; Cunha et al., 2012), mollusks (Tavareset al., 1988; Sericano et al., 1995) and fish (Azevedo e Silva et al.,2007, 2009).

Recently, a few studies about organochlorine compounds contami-nation with continental shelf and oceanic delphinids have been pub-lished (Leonel et al., 2012; Lailson-Brito et al., 2012), but most of thestudies carried out in Brazil involve coastal dolphin species, such asthe Guiana dolphin (Sotalia guianensis) (Yogui et al., 2003; Kajiwaraet al., 2004; Alonso et al., 2010; Lailson-Brito et al., 2010) and theFranciscana dolphin (Pontoporia blainvillei) (Lailson-Brito et al., 2011).Some authors found concentrations of contaminants similar to thehigh levels reported in the industrialized areas in the Northern Hemi-sphere (Lailson-Brito et al., 2010, 2012). Guiana dolphins are distributedalong the South and Central American eastern coast, from SantaCatarina (27°35′S/48°35′W) to Honduras (15°58′N/79°54′W) (Floresand Da Silva, 2009). The Guiana dolphin inhabits mostly bays, estuariesand other sheltered areas, although there have been sightings in theopen waters of the Abrolhos Archipelago, Bahia, Brazil (Borobia et al.,1991; Rossi-Santos et al., 2006). This species also demonstrates highresidence and site fidelities in several populations along the Braziliancoast (Azevedo et al., 2007; Flach et al., 2008; Rossi-Santos et al., 2007).

Because they inhabit shallow waters along the coast, Guiana dol-phins are constantly exposed to anthropogenic risk factors: fishing netentanglements, habitat loss, ingestion of plastic and both acoustic andchemical pollution (Reeves et al., 2003; Azevedo et al., 2008; Meirelleset al., 2010; Lailson-Brito et al., 2010). Despite the numerous studiesconducted in the last decade and the great anthropogenic pressure onits habitat, the Guiana dolphins remain classified as “data deficient”(DD) by the International Union Conservation of Nature (IUCN, 2011).

The present study also focuses on delphinid species residingalong the continental shelf and in oceanic environments: the Atlanticspotted (Stenella frontalis), spinner (Stenella longirostris), striped (Stenellacoeruleoalba) and Fraser's dolphins (Lagenodelphis hosei). The Atlanticspotted dolphin is mainly distributed along the continental shelf,but there are some reports of this species in oceanic environments(Moreno et al., 2005). The other delphinids are oceanic species thatfeed mainly on fish and cephalopods in the mesopelagic zone (Dolaret al., 2003; Moreno et al., 2003; Rosas et al., 2002; Spitz et al., 2006).

Because the lack of scientific studies that have evaluated the organ-ochlorine concentrations in cetaceans of northeastern Brazil, as wellas the known persistence and harmful effects of organochlorineson those mammals, the bioaccumulation pattern was verified forpolychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane(DDT) and its metabolites, hexachlorocyclohexanes (HCHs), hexachlo-robenzene (HCB) and Mirex in the subcutaneous adipose tissue ofthe following delphinid species found stranded along the Ceará Statecoast in Brazil: Guiana, Fraser's, spinner, Atlantic spotted and stripeddolphins.

2. Methodology

2.1. Study area

The delphinid species were collected along the Ceará State coast inBrazil. This State has a 573 km coastal extension, representing 20% ofthe northeastern coast of Brazil. This area is mainly composed ofsandy beaches, dunes, estuaries withmangrove forests, coastal lagoons,cliffs and low plateaus. Like other areas of the Brazilian coast, the regionis densely populated, totaling 178.13 hab./km2 (Campos and Polette,2003). The studied area is very large compared to the size of the homeranges described in the literature for the Guiana dolphin in other re-gions of the Brazilian coast (Rossi-Santos et al., 2007). Therefore, thearea was divided in three regions (C1, Metropolitan and C2) in accor-dance with the level of industrial development and population density

(Fig. 1). The Metropolitan region is the third largest industrial centerin northeastern Brazil and is more densely populated (598 hab./km2)than the C1 (70 hab./km2) and C2 regions (44 hab./km2). The most im-portant economic activities in C1 and C2 are agriculture, fishing andtourism (IPCE, 2010; Campos and Polette, 2003).

2.2. Sampling

Subcutaneous adipose tissue (blubber) samples were collected toidentify the presence of organochlorines in 25 Guiana dolphins, twoFraser's dolphins, two spinner dolphins, one Atlantic spotted dolphinand one striped dolphin. The samples were collected from strandedspecimens found on the Ceará coast between 2005 and 2011 duringbeachmonitoring carried out by the Associação de Pesquisa e Preservaçãode Ecossistemas Aquáticos, (AQUASIS). Necropsies followed the proce-dures suggested by Geraci and Lounsbury (2005). Once collected, thesamples were wrapped in aluminum foil and stored at −20 °C untilthe analyses could be conducted.

Sexual maturity was estimated according to the total length ofeach species: spinner dolphins (Male = 180 cm/Female = 176 cm),striped dolphin (Male/Female = 180–190 cm), Fraser's dolphins(Male = 220–230 cm/Female = 210–220 cm) (Jefferson et al., 2008)and Guiana dolphins (Male = 170–175 cm/Female = 164–169 cm)(Rosas and Monteiro-Filho, 2002). The status of the dolphin carcasseswas evaluated according to the classifications suggested by Geraci andLounsbury (2005).

2.3. Analytical procedure

The analytical procedurewas an adaptation of themethod suggestedby Lailson-Brito et al. (2010). Briefly, approximately 1.0 g of an entirevertical cross-section of blubber was homogenized with anhydrous so-dium sulfate (Na2SO4) (1:6), and the internal surrogate standard PCB103 and PCB 198 (100 ng·mL−1) was added. The extraction procedureswere performed using a continuous Soxhlet extraction with 100 mLhexane:dichloromethane (1:1) for 8 h. After the lipid determination(performed gravimetrically on an aliquot of the extract), the extractwas treated with sulfuric acid. After centrifugation and phase separa-tion, an internal standard (2,3,5,6-tetrachloro-m-xyleno/TCMX) wasadded.

The analyses were performed on an Agilent Technologies 7890 chro-matographwith a 63Ni electron capture detector (CG-DCE) and an auto-matic injector (Agilent Technologies 7683B). The detector was kept at320 °C, and 2 μL of sample was added by the injector at 280 °C operat-ing over 30 s in splitless mode. Hydrogen (99.999% pure) was used asthe carrier gas at 13 psi. Nitrogen was used as an auxiliary gas (makeup). The column temperature was programmed as follows: started at70 °C, held for 1 min, and increased by 40 °C/min up to 170 °C. Thetemperature was then first raised to 240 °C at 1.5 °C/min, and then in-creased to 300 °C at 15 °C/min before being held for 11 min. The totalchromatographic run took 65 min. For the analyses, a fused silica DB-5capillary column (Agilent Technologies, 30 m × 0.25 i.d. mm and filmthickness 1 μm) was used. The acquisition, integration, and calculationof the data were performed with the Ezchrom 3.2.1 Software System.

In the present study, 25 PCB congeners (28, 44, 49, 97, 101, 105, 118,132, 138, 141, 151, 153, 158, 170, 174, 177, 180, 183, 187, 194, 195, 199,203, 206 and 209), 3 DDT isomers (p,p′-DDT, p,p′-DDE and p,p′-DDD), 4HCH isomers (α-HCH, β-HCH, γ-HCH and δ-HCH), HCB andMirexwereanalyzed. The standard solutions were the PCB Congener Mix for WestCoast Fish Studies and the WHO/NIST/NOAA Congener List for PCBsand Pesticide Mix for pesticides. All standards were acquired from theAccuStandard® laboratory. In this study, the recoveries for the internalsurrogate standards (PCB 103 and PCB 198) ranged from 88 to 129%.

The analytical method was validated using a certified standard(Cod Liver Oil – SRM-1588 and Whale Adipose Tissue – SRM 1945,from the National Institute of Standards and Technology – NIST). The

Fig. 1. Study area by region (C1, Metropolitan and C2) on the Ceará coast.

196 E.B. Santos-Neto et al. / Science of the Total Environment 472 (2014) 194–203

validation criteria were based on those of Wade and Cantillo (1994),accepting concentrations between 65 and 135%. The method detectionlimits ranged from 2.06 to 2.96 ng·g−1 for PCBs and from 2 to2.64 ng·g−1 for pesticides. In addition to the abovementioned qualitycontrol measures, regular analyses of procedural blanks were per-formed (relative standard deviation—RSD b 20% for nine replicates).

2.4. Statistical analysis

The organochlorine concentrations were expressed as μg·g−1 andcalculated based on the lipid content (μg·g−1 lip). Descriptive statisticswere employed tomeasure the central tendencies of each sample repli-cate as well as to determine the standard deviation. Shapiro–Wilk's testwas used to test the normality of the data. This test revealed that thedata did not present a normal distribution, and non-parametric statisti-cal tests were performed. The significant differences among the sam-pling regions were verified using the Kruskal–Wallis test, followed bya post hoc multiple comparison test. A discriminant function analysiswas used to investigate any possible differences in the organochlorineaccumulation patterns between the Guiana dolphins and the continen-tal shelf/oceanic delphinids. The data were transformed to natural loga-rithms before the discriminant function analysis. Of the 34 compounds(PCBs, DDTs, HCHs and HCB), 17 were used in the test because theymet the tolerance limit requirements (0.01) of themodel (discriminantfunction analysis). To remove any possible influence of sexual maturity,the mature females were excluded from the discriminant analysis. Allanalyses were performed using the STATISTIC 7.0 Software System.

3. Results and discussion

3.1. Guiana dolphin

The biological information and organochlorine compound concen-trations of the Guiana dolphins are presented in Table 1. For all regions,∑PCB were the predominant compound, followed by ∑DDT, Mirex,∑HCH and HCB. This pattern was previously reported in other studiesinvolving cetaceans from southern and southeastern Brazil (Alonsoet al., 2010; Lailson-Brito et al., 2010, 2012; Leonel et al., 2012). Thesefindings are most likely related to the higher utilization and persistenceof PCBs and DDTs in the environment.

The highest mean values for ∑PCB (7.35 μg·g−1 lip), ∑DDT(1.11 μg·g−1 lip), ∑HCH (0.04 μg·g−1 lip) and Mirex (0.09 μg·g−1

lip) were found in the specimens from the Metropolitan region, whilethe highest mean value of HCB (0.02 μg·g−1 lip) was measured inGuiana dolphins from the C1 region (Table 1). The lowest valueswere found in the C2 region. The mean concentrations of ∑DDT and∑PCB varied significantly between the regions (Kruskal–Wallis test;p = 0.02 and p = 0.014, respectively). The Guiana dolphins from theMetropolitan region contained higher ∑DDT and ∑PCB levels thanthose from the C2 region (multiple comparison test, p = 0.02 andp = 0.01, respectively). However, there was no difference in the organ-ochlorine concentrations between the C1 and C2 regions (multiplecomparison test, p N 0.17). The Metropolitan region has the highestpopulation density in Ceará State; it is the third most important indus-trial center in northeastern Brazil (Campos and Polette, 2003; IPCE,

Table 1Total organochlorine compounds (∑PCB,∑DDT,∑HCH, HCB and Mirex,) in Guiana dolphins (Sotalia guianensis) from three different regions of the Ceará coast. Mean ± standard de-viation (mean ± SD), median andminimum andmaximum (min–max) values are presented. Information on year of sampling, sex, total length (TL, cm) and lipid content (%) of the sub-cutaneous adipose tissue are also shown. Organochlorine concentrations were expressed as μg·g−1, calculated on a lipid basis (μg·g−1 lip).

Specimen Sampling year Sex TL (cm) Lipids (%) COD ∑PCB ∑ DDT ∑HCH HCB Mirex ∑DDT/∑PCB

C1 regionSg #01 2009 FM 178 29 3 3.85 0.43 bDL 0.01 0.11 0.11Sg #02 2009 InI 153 26 4 1.67 0.26 0.12 0.04 0.12 0.15Sg #03 2010 FM 180 54 3 0.02 0.006 bDL bDL 0.02 0.2Sg #04 2011 MM 190 48 3 3.37 0.63 bDL 0.003 0.08 0.18Mean ± SD 2.23 ± 1.74 0.33 ± 0.26 – 0.02 ± 0.02 0.08 ± 0.04Median 2.52 0.34 – 0.01 0.09Min–max 0.02–3.85 0.006–0.63 – 0.003–0.04 0.02–0.12 0.16

Metropolitan regionSg #05 2007 MM 173 41 2 7.32 1.48 0.05 0.01 0.09 0.20Sg #06 2008 MM 188 73 4 3.93 0.88 bDL 0.003 0.15 0.22Sg #07 2010 FI 143 35 3 0.04 0.06 bDL bDL 0.04 1.44Sg #08 2010 FM 178 73 3 2.63 0.55 bDL 0.002 0.08 0.21Sg #09 2010 MI 122 66 2 17.3 1.91 0.04 0.01 0.08 0.11Sg #10 2010 MM 180 44 4 16.2 1.87 bDL 0.007 0.08 0.12Sg #11 2010 FI 117 23 3 7.05 1.45 bDL 0.009 0.10 0.21Sg #12 2011 FM 181 73 3 4.30 0.69 0.04 0.005 0.06 0.16Mean ± SD 7.35 ± 6.27 1.11 ± 0.66 0.04 ± 0.01 0.007 ± 0.004 0.09 ± 0.03 0.33Median 5.68 1.17 0.04 0.007 0.08Min–max 0.04–17.3 0.06–1.91 0.04–0.05 0.002–0.01 0.04 0.15

C3 regionSg #13 2009 MM 183 39 4 0.49 0.26 0.08 0.007 0.05 0.53Sg #14 2009 MI 157 39 4 3.00 0.61 bDL bDL 0.09 0.20Sg #15 2009 MI 155 24 4 0.37 0.35 bDL bDL 0.14 0.94Sg #16 2009 MI 89 75 3 0.04 0.08 bDL 0.004 0.03 2.12Sg #17 2009 FM 176 29 4 bDL 0.003 0.01 bDL 0.02 –

Sg #18 2009 FI 158 74 3 3.08 0.82 bDL 0.006 0.16 0.27Sg #19 2010 MM 180 65 3 0.94 0.53 bDL bDL 0.09 0.56Sg #20 2010 MM 174 60 3 0.85 0.14 bDL bDL 0.07 0.16Sg #21 2011 FM 204 38 3 0.03 0.10 0.03 bDL bDL 3.32Sg #22 2011 MI 159 68 4 3.64 0.78 0.05 0.006 0.07 0.21Sg #23 2011 FI 100 89 3 0.08 0.09 0.03 0.003 0.02 1.12Sg #24 2011 FM 180 71 3 0.81 0.15 0.005 bDL 0.04 0.18Sg #25 2011 FI 102 77 2 0.15 0.06 0.02 0.008 0.03 0.40Mean ± SD 1.12 ± 1.32 0.30 ± 0.28 0.03 ± 0.03 0.006 ± 0.002 0.07 ± 0.05 0.77Median 0.65 0.15 28 0.006 0.06Min–max 0.03–3.64 0.003–0.82 0.005–0.08 0.003–0.008 0.02–0.16

DL = Detection Limit; F = Female; M = Male; In = Indeterminate; I = Immature; M = Mature.

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2008, 2010), and the industrial park houses the textiles, footwear andfood industries (Araújo, 2007). Several studies have reported high levelsof PCBs in the marine biota from industrialized areas and regions withhigh population densities (e.g.: Tanabe, 2002; Pulster and Maruya,2008; Lailson-Brito et al., 2010). Consequently, the ∑PCB concentra-tions in the Guiana dolphins from the Metropolitan region are attribut-ed to their proximity to a more plentiful source of these compoundsthan the individuals from the C1 and C2 regions.

The ∑DDT concentration was also higher in specimens from theMetropolitan region than in those individuals from the other twostudy areas due to the agricultural activities in the area; these agricul-tural areas drain into the Metropolitan river basin (IPCE, 2008). More-over, the extensive use of DDTs in the vector control programs thatprevent diseases in Ceará State, such as malaria, yellow fever, and den-gue fever (Lima et al., 2009) might also introduce these compounds tothe marine environment.

Compared to the organochlorine concentrations in the Guiana dol-phins in southern (Kajiwara et al., 2004; Lailson-Brito et al., 2010) andsoutheastern Brazil (Yogui et al., 2003; Kajiwara et al., 2004; Alonsoet al., 2010; Lailson-Brito et al., 2010), our results yielded lower∑PCB, ∑DDT, ∑HCH and HCB concentrations in the specimensfromCeará State (Table 2), excepting the∑PCB and∑HCH levelsmea-sured in the specimens from the Metropolitan region; these exceptionsare higher than the values reported for Guiana dolphins from Cananéia(SP; Yogui et al., 2003) and Paranaguá Bay (PR; Lailson-Brito et al.,2010). Most of the areas in southern and southeastern Brazil sampledin previous studies (Table 2) contained regions with a strong industrial

presence and highly populated areas, such as Guanabara Bay, SepetibaBay and Santos region complex (Kjerfve et al., 1997; IFIAS, 1998;Lamparelli et al., 2001), while the northeastern region typically presentsfewer agroindustrial developments and a lower population density(IBGE, 2011).

The organochlorine concentrations found in the present study werealso lower than those values reported for other delphinid species in thenorthern hemisphere, such as the bottlenose (Tursiops truncatus) andstriped dolphins from the Mediterranean Sea (Fossi et al., 2004;Storelli et al., 2012), the Atlantic white-sided dolphin (Lagenorhynchusacutus) from the Gulf of Maine, USA (Weisbrod et al., 2001), thebottlenose dolphin from Georgia and Gulf of Mexico, USA (Balmeret al., 2011;Wilson et al., 2012) and the Indo-Pacific humpback dolphin(Sousa chinensis) from Hong Kong, China (Minh et al., 1999; Table 2).These findings highlight the lower degree of industrialization in north-eastern Brazil. However, although the organochlorine levels in Guianadolphin in the study area were lower than the levels in the highlycontaminated areas in Brazil and the northern hemisphere, the risk ofdeleterious effects caused by these compounds cannot be ignored. Stud-ies have reported the adverse effects associated with the accumulationof organochlorine compounds in marine mammals (e.g.: Reijnders,1980; O'Shea, 1999; Villanger et al., 2011), including immune systemdepression (e.g.: Aguilar and Borrell, 1994; Ross et al., 1995; De Guiseet al., 1998; Pierce et al., 2008). In the present study, two Guiana dol-phins from the Metropolitan region (Sg #09 and Sg #10) showed∑PCB concentrations close to the threshold level (17 μg·g−1 lip) asso-ciatedwith health effects onmarinemammals (Kannan et al., 2000; Law

Table 2Comparison of the minimum and maximum (min–max) and means ± standard deviations (mean ± SD) values of the organochlorine compounds (∑PCB, ∑DDT, ∑HCH, HCB andMirex,) in odontocetes from different regions around the world and in the present study. The organochlorine concentrations were expressed as μg·g−1.

Locality Species References N ∑PCB ∑DDT ∑HCH HCB Mirex

C1 region Sotalia guianensis Present studya 4 0.02–3.852.23 ± 1.74

0.006–0.630.33 ± 0.26

– 0.003–0.040.02 ± 0.02

0.02–0.120.08 ± 0.04

Metropolitan region Sotalia guianensis Present studya 8 0.04–17.37.35 ± 6.27

0.06–1.911.11 ± 0.66

0.04–0.050.04 ± 0.01

0.002–0.010.007 ± 0.004

0.04–0.150.09 ± 0.03

C2 region Sotalia guianensis Present studya 13 0.03–3.641.12 ± 1.32

0.003–0.820.30 ± 0.28

0.005–0.080.03 ± 0.03

0.003–0.0080.006 ± 0.002

0.02–0.160.07 ± 0.05

Cananéia estuary, Brazil Sotalia guianensis Yogui et al. (2003)a 9 0.2–9.224.61 ± 3.31

0.54–12535.9 ± 46.8

b0.003–0.030.02 ± 0.02

b0.003–0.020.02 ± 0.009

0.01–0.310.15 ± 0.09

Paraná and São Paulo, Brazil Sotalia guianensis Kajiwara et al. (2004)a 26 1.30–79 1–150 b1–0.061 0.002–0.4 –

Guanabara bay, Brazil Sotalia guianensis Lailson-Brito et al. (2010)a 12 6.66–99.234.8 ± 26.3

2.07–21.57.95 ± 6.91

– b0.004–0.110.05 ± 0.04

–

Sepetiba/Ilha grande bays, Brazil Sotalia guianensis Lailson-Brito et al. (2010)a 5 1.74–25.512.3 ± 11.7

0.65–103.86 ± 3.89

– 0.01–0.080.03 ± 0.03

–

Paranaguá bay, Brazil Sotalia guianensis Lailson-Brito et al. (2010)a 15 0.77–14.34.56 ± 3.97

0.98–23.65.76 ± 5.84

– b0.004–0.160.04 ± 0.04

–

Ubatuba, Brazil Sotalia guianensis Alonso et al. (2010)a 3 25.9–66.047.8

16.9–48.034.0

0.06–0.070.07

0.08–0.140.11

0.57–0.191.26

Complex of Santos, Brazil Sotalia guianensis Alonso et al. (2010)a 3 27.9–61.339.7

24.6–55.936.9

0.03–0.210.09

0.07–0.170.12

0.24–1.040.76

Mediterranean Sea Stenella coeruleoalba Fossi et al. (2004)b 9 13.2 10.0 – 0.07 –

Mediterranean Sea Stenella coeruleoalba Storelli et al. (2012)b 17 22 ± 20.31 – – – –

Georgia, EUA Tursiops truncatus Balmer et al. (2011)a 102 20.7–703 0.23–88.1 – 0–0.07 0.12–3.78Gulf of Maine, EUA Lagenorhynchus acutus Weisbrod et al. (2001)b 6 12.97 14.05 0.22 0.18 0.05Gulf of Mexico, EUA Tursiops truncatus Wilson et al. (2012)b 77 0.32–42.1 0.10–33.1Hong Kong/China Sousa chinensis Minh et al. (1999)b 11 24 46 0.8 0.07 –

a Values expressed on a lipid basis.b Values expressed on wet weight.

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et al., 2012). Furthermore, the specimens in the metropolitan regionpresented skin lesions from the “tattoo skin disease” caused by a poxvi-rus (Associação de Pesquisa e Preservação de Ecossistemas Aquáticos,unpublished data). This disease has been associated with impaired im-mune systems (Van Bressem and VanWaerebeek, 1996; Moller, 2003).

Every region containedmostly PCB congenerswith high chlorinationlevels (hexa-, hepta- and octa-chlorobiphenyls) (Fig. 2), but there weremore octachlorinated congeners contributed by the C1 and C2 regionsthan the Metropolitan region. The predominant congener was PCB153 for the Guiana dolphins in every region, agreeing with the patternreported for the marine mammals from other regions in Brazil (Alonsoet al., 2010; Lailson-Brito et al., 2010, 2011, 2012) and around theworld (Marsili and Focardi, 1996; Corsolini et al., 2003; Wafo et al.,2005). The predominance of those compounds may be related to theirgreater persistence in the environment because their bioaccumulationpotential increases with the degree of chlorine substitution and theirmolecular weights (Marsili and Focardi, 1996; Aguilar et al., 1999).

The commercial mixtures of PCBs congeners sold in Brazil wereimported mainly from the United States and Germany. The most com-mon mixture was the Aroclor® series (1221, 1232, 1016, 1242, 1248,1254 and 1260) that contains 18.8 to 68.8% chlorine (Penteado andVaz, 2001). There is no information regarding where each mixturewas used within the different Brazilian regions, precluding any correla-tion between the contamination profiles of the Guiana dolphin and aspecific Aroclor® mixture.

Regarding∑DDT, p,p′DDE was the dominant species in the Guianadolphin from every region (Fig. 3), and the ratio of p,p′DDE/∑DDTwascalculated for individual to determine the chronology of the introduc-tion of DDT to the systems (Aguilar, 1987). Differences were observedin the DDT accumulation between the different areas; theMetropolitanregion presented the lowest average value (0.56), followed by the C3(0.63) and C1 (0.69) regions. Aguilar (1984) suggests that ratios above0.6 may indicate an old DDT source. Therefore, the data for the Metro-politan region reveals the more recent DDT use in this area throughthe significant contribution of p,p′DDT (33%) to∑DDT, which is almostthree times larger than the value reported for the C1 region (11%). DDTshave been used recently in the vector control programs for diseases inCeará State (Lima et al., 2009). Additionally, the ratios found in the

Guiana dolphins from the three areas were lower than those reportedfor the cetaceans from Rio de Janeiro State (ratios N 0.7; Lailson-Britoet al., 2010, 2012) and from São Paulo State (ratios N 0.8; Yogui et al.,2003; Kajiwara et al., 2004; Alonso et al., 2010).

Lastly, the∑DDT/∑PCB ratio is used to assesswhether the agricul-tural/vector control or the industrial/dense population contribute themostmarine contamination. In the present study, the∑DDT/∑PCB ra-tios for theMetropolitan and C1 regionswere 0.33 and 0.16, respective-ly (Table 1), revealing a stronger influence of industrial pollution andhigh-density population on the organochlorine accumulation on theCeará coast. Even in the C2 region, which has a smaller population den-sity and fewer industrial activities, the ratio (0.77) (Table 1)was smallerthan the values reported by Yogui et al. (2003) (6.5), Kajiwara et al.(2004) (1.53) and Lailson-Brito et al. (2010) (1.33) for traditional agri-cultural areas in southern and southeastern Brazil.

3.2. Continental shelf and oceanic dolphins

The organochlorine compound concentrations and ∑DDT/∑PCBratios found in the delphinids from the continental shelf and oceanicregions are shown in Table 3. Only the spinner dolphins showedpredominantly ∑PCB, followed by ∑DDT and Mirex. The highest∑PCB concentrations were observed in this species, followed by theAtlantic spotted, Fraser's and, lastly, striped dolphins. ∑DDT was thepredominant compound in Fraser's, Atlantic spotted and striped dol-phins; the concentrations decrease in the following order (not statisti-cally significant): Fraser's dolphin N Atlantic spotted dolphin N stripeddolphin N spinner dolphin. As observed for theGuianadolphin, in general,the organochlorine concentrations from northeastern Brazil were lowerthan those reported in the delphinid species from southeastern Brazil(Leonel et al., 2012; Lailson-Brito et al., 2012) due to the higher agro-industrial development observed in southeastern Brazil (IBGE, 2011).

Although the primary source of organochlorine compounds fordelphinids is dietary (Aguilar, 1987), other aspects may be influencingthe differences in organochlorine concentrations among the delphinidspecies. The Atlantic spotted dolphins feed on prey at a higher trophiclevel (Melo et al., 2010) than the striped, spinner and Fraser's dolphins(Bisi et al., in press; Dolar et al., 2003; Rosas et al., 2002; Spitz et al.,

Fig. 2.Relative contributions of the PCB congeners grouped by thenumber of chlorine atoms in themolecule for theΣPCB in the blubber fromGuianadolphins (Sotalia guianensis) strandedat the Ceará coast.

Fig. 3. Percentages of p,p′-DDE, p,p′-DDT and p,p′-DDD in the blubber from Guiana dolphins (Sotalia guianensis) stranded at the Ceará coast.

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Table 3Concentrations of organochlorine compounds (∑PCB,∑DDT,∑HCH, HCB andMirex,) and the∑DDT/∑PCB ratio in delphinids (n = 6) on the Ceará coast in the context of the year ofsampling, sex, total length (TL, cm) and lipid percentage of the subcutaneous adipose tissue. The organochlorine concentrationswere expressed as μg·g−1 lip and calculated based on thelipid content (μg·g−1 lip).

Species Sampling year Sex TL (cm) Lipids (%) COD ∑PCB ∑DDT ∑HCH HCB Mirex ∑DDT/∑PCB

Stenella frontalis (Sf #01) 2006 MIn 176 3 2 1.89 2.88 0.11 0.06 2.38 1.89Stenella coeruleoalba (Sc #01) 2007 FM 217 74 2 0.96 1.07 0.06 0.1 0.10 1.11Stenella longirostris (Sl #01) 2008 MI 168 42 2 7.16 0.69 bDL 0.03 0.25 0.1Stenella longirostris (Sl #02) 2010 FI 172 23 2 4.91 0.68 0.15 0.02 0.38 0.13Lagenodelphis hosei (Lh #01) 2009 FM 217 51 2 1.66 3.38 0.13 0.07 0.12 2.03Lagenodelphis hosei (Lh #02) 2010 FM 234 5 3 1.89 5.19 0.16 0.09 0.41 2.75

DL = Detection Limit; F = Female; M = Male; I = Immature; M = Mature; In = Indeterminate.

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2006). However, the ∑PCB levels in Atlantic spotted dolphin werelower than in the spinner dolphins and similar to the values inFraser's dolphins, while the highest ∑DDT concentrations occurredin Fraser's dolphins (Table 3). The contamination levels found in thedelphinids stranded along the Ceará coast are most likely due to the

Fig. 4.Relative contributions of the PCB congeners for theΣPCB in the blubber of Fraser's (Lagenodolphins (Stenella coeruleoalba) stranded at the Ceará coast.

great mobility of this species; individuals can forage in large areas.Consequently, these species can experience contamination beyondthe Ceará State coast.

PCB congeners with high chlorination levels (hexa- and hepta-chlorobiphenyls) dominated every species (Fig. 4), similar to theGuiana

delphis hosei), spinner (Stenella longirostris), Atlantic spotted (Stenella frontalis) and striped

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dolphins in the present study (Fig. 2). The Atlantic spotted dolphinswere the only species that did not exhibit a PCB contribution with alower chlorination level (tri-, tetra- and penta-chloro) in the contami-nation profile. The low lipid content (3%) of the subcutaneous adiposetissue in the Atlantic spotted dolphins may influence the results andwould not be reflected the pattern for this species in this region. Otherstudies identified lower chlorination PCB congeners in the contamina-tion profiles of Atlantic spotted dolphins (Leonel et al., 2012) andother delphinid species with coastal habitats (continental shelf)(Lailson-Brito et al., 2012) in southeastern Brazil.

The subcutaneous adipose tissue (blubber) found in cetaceans iscritical both for thermoregulation and as an energy source (Rommeland Lowenstine, 2001). However, lipids are mobilized more quicklythan the lipophilic contaminants; moreover, the mobilization patternsof the various organochlorine compounds are different. Some studiesshowed that individuals utilizing mobilized lipids from blubber as anenergy source had higher organochlorine levels (Aguilar and Borrell,1994; Aguilar et al., 1999). Animals in poor health state may not feednormally and therefore must mobilize lipids, influencing the organo-chlorine concentrations. Two specimens contained low lipid levels(Lh #01 and Sf #01). The carcasses were at an early stage of decompo-sition and therefore were in good condition (code 2; Geraci andLounsbury, 2005); however, during necropsy, the poor health of thesespecimens became apparent. The Lh #01 had septicemia, while the Sf#01 was in a cachectic state with chronic pneumonia (Associação dePesquisa e Preservação de Ecossistemas Aquáticos, unpublished data).Consequently, the organochlorine concentrations and patterns inthese individuals should be viewed with caution because they maynot be representative of the species. However, it is important to high-light that these compounds are incorporated in the continental shelfand oceanic biota of northeastern Brazil.

Regarding the ∑DDT/∑PCB ratio, the values varied between thedelphinid species (from 0.1 to 2.75; Table 3). Only the spinner dolphinsshowed a higher influence of industrial pollution on the accumulation oforganochlorines within their forage area, similar to the data for theGuiana dolphins from the present study and that for the oceanic and

Fig. 5. Graphic showing the canonical variables for the Guiana dolphin (C1, Metropolitan and Ccircles represent means for each area.

coastal delphinids from southeastern Brazil (Lailson-Brito et al., 2012).For the Fraser's, Atlantic spotted and striped dolphins, a higheragricultural contribution in the contamination pattern was found. The∑DDT/∑PCB ratios for these species were similar to those reportedfor the Guiana dolphins in the agricultural regions of southern andsoutheastern Brazil (Kajiwara et al., 2004; Lailson-Brito et al., 2010).The differences in the contamination patterns indicate that thedelphinids forage in distinct areas beyond the waters influenced bytheCeará State coast; thedifferent contamination patternsmay be relat-ed to differences in their feeding grounds (Ross et al., 2000; Hansenet al., 2004).

3.3. Guiana dolphins versus continental shelf and oceanic dolphins

A discriminant function analysis was performed to investigate anypossible differences in the organochlorine contamination profiles be-tween the delphinid species and among the Guiana dolphin specimensfrom the three different regions. This analysis revealed the significantdifferences in the delphinid organochlorine accumulation patterns(Wilks' Lambda: 0.0000; F (51.3) = 6.7606; p b 0.037). The delphinidswere separated into three distinct groups (C1 andMetropolitan regions,C2 region and continental shelf/oceanic dolphins), and the first two ca-nonical variables are graphically represented in Fig. 5.

The smallest Mahalanobis distance (D2) was observed between theGuiana dolphins from the C1 and Metropolitan regions (p = 0.87).The largest distance (D2) was found between the C1 and Metropolitanregions and the C2 region, but the D2 was insignificant (p = 0.08 andp = 0.05, respectively). These data revealed the differences betweenthe accumulation patterns of the Guiana dolphins from the Ceará coast.Differences were also found between the continental shelf/oceanicdolphins and the Guiana dolphins from all three regions, but withouta significant difference in D2 (p N 0.013) (Table 4). The most im-portant compounds separated from canonical axis 1 were PCB 28, PCB105, α-HCH, and γ-HCH, while those for axis 2 were PCB 28, α-HCH,β-HCH and γ-HCH. The percentage correctly classified was 100%.

2 regions) and for the continental shelf/oceanic dolphins stranded at the Ceará coast. The

Table 4The F value (lower-left) and Mahalanobis distance (D2—upper-right) between thedelphinids from northeastern Brazil coast obtained from the discriminant analysis.C1—Guiana dolphins from the C1 region, Metropolitan—Guiana dolphins from theMetropolitan region, C2—Guiana dolphin from the C2 region and CS/Oc—delphinidsfrom the continental shelf and oceanic environment.

C1 Metropolitan C2 CS/OC

C1 74.26 15742.68 5129.69Metropolitan 0.38 15652.70 5033.21C2 90.79 203.11 3190.53CS/OC 21.30 34.83 25.47

Non-significant values.

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In the discriminant function analysis, the distance between thegroups may be related to the differences in their diet and/or feedinggrounds. The bioaccumulation of organochlorine compounds in ceta-ceans is mainly related to their dietary intake (Aguilar, 1987; Rosset al., 2000; Hansen et al., 2004). However, information regarding thefeeding ecology of delphinids from the study area remains absent, pre-cluding further discussion. According to the stomach contents analyzedin other areas, the spinner dolphins feed mainly on mesopelagic fishfrom the Myctophidae family (Dolar et al., 2003), while the Atlanticspotted dolphins consume coastal and oceanic prey, including fish andcephalopods (Melo et al., 2010). The Guiana dolphins prey mainly onteleost fish, but the species or importance of each diet vary within thepopulations (e.g.: Daura-Jorge et al., 2011;Di Beneditto et al., 2001; San-tos et al., 2002). Moreover, Bisi et al. (in press) observed differences inthe preferred habitat and feeding ecology among three populations ofGuiana dolphins, as well as the continental shelf and oceanic speciesfrom southeastern Brazil.

According to Aguilar (1987) and Lailson-Brito et al. (2010), the dif-ferences in the bioaccumulation patterns between species and individ-uals of the same species can be used to distinguish populations whiledeveloping conservation measures.

4. Conclusions

The present study is the first to report the presence of organochlo-rine compounds in delphinid tissues fromnortheastern Brazil. Industrialcompounds were more prevalent in the bioaccumulation patterns forthe Guiana and spinner dolphins, while agricultural compounds domi-nated the values for the Fraser's, Atlantic spotted and striped dolphins.By using a discriminant function analysis, the distinct accumulation pat-terns among the Guiana dolphins from the C2, Metropolitan and C1 re-gions, as well as those in the continental shelf/oceanic dolphins andGuiana dolphins from all three coastal regions of Ceará coast, were re-vealed. However, due to the low sample number, these results shouldbe viewed with caution; further studies should be conducted in the fu-ture to understand the accumulation patterns for organochlorine com-pounds in the delphinid species in northeastern Brazil. Finally, theorganochlorine concentrations found in the present study and thehigh incidence of animals stranded due to interactions with the fishingindustry (Meirelles et al., 2010) demonstrate that the Guiana dolphinsare under high anthropogenic pressure in the Metropolitan region ofCeará State.

Acknowledgments

This research was funded by the Brazilian Research Council—CNPQNo. 480701/2009-1, under the supervision of Prof. Dr. José LailsonBrito Junior. Researcher fellowship was provided by the Research Sup-port Foundation of the State of Bahia (FAPESB). We gratefully acknowl-edge the Laboratório de Mamíferos Aquáticos e BioindicadoresProfessora Izabel Gurgel (MAQUA) and the Associação de Pesquisa ePreservação de Ecossistemas Aquáticos (AQUASIS) for all their supportduring the research. We thank LANDOSIG/UFBA for the maps and

Luciana Leite for the English version of this study. We also express ourimmense gratitude to CNPq and FAPESB for their financial support.J Lailson-Brito and AF Azevedo have research grants from CNPq (PQ-2),FAPERJ (JCNE) and UERJ (“Prociência” Program). The collection of speci-mens was carried out under the authorization of Instituto ChicoMendesde Conservação da Biodiversidade SISBIO # 14104-5. AQUASIS is part ofthe Brazilian Aquatic Mammal Stranding Network. Programa PetrobrasAmbiental provided important financial support.

Appendix A. Supplementary data

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.scitotenv.2013.10.117.

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