Organochlorine Residues in the Blubber andLiver of Bottlenose Dolphins (Tursiops truncatus)Stranded in the Canary Islands, North AtlanticOcean

Matilde Carballo,1 Manuel Arbelo,2 Fernado Esperon,1 Marina Mendez,2 Ana de la Torre,1

Maria Jesus Munoz1

1Animal Health Research Centre-INIA, Division of Environmental Health, 28130 Valdeolmos,Madrid, Spain

2Unit Histology and Pathology, Institute of Animal Health, Veterinary School,University of Las Palmas, 35001 Arucas, Las Palmas de Gran Canaria, Spain

Received 22 March 2007; revised 13 July 2007; accepted 24 July 2007

ABSTRACT: Polychlorinated biphenyls (PCBs) and chlorinated pesticides: dichlorodiphenyltrichloro-ethane and its metabolites (DDTs), chlordanes (CHLs), dieldrin, and hexaclorobenzene (HCB) weredetected in the blubber and liver of 11 bottlenose dolphins (Tursiops truncatus) from the Canary Islands(North Atlantic Ocean). Samples were obtained from stranded dolphins over the period 1997–2005.Among the organochlorines analyzed, PCBs and DDTs were predominant in the two tissues, followed indecreasing order by chlordane, trans-nonachlor[cis-nonachlor[dieldrin and HCB. The sum 11 PCBs inthe blubber ranged between 301 and 33,212 ng g21 ww (990 and 136,679 ng g21 lw). Highly chlorinatedPCBs such us CB153, CB180, and CB138 were the prominent congeners, accounting for 51% of the totalPCBs. The sum DDT concentration in the blubber ranged between 147 and 21,050 ng g21 ww. (490–105,250 ng g21 lw) The main DDT metabolite was p,p0-DDE, representing 83% of DDTs in the blubber. Ingeneral, the levels of PCBs and DDTs detected were similar to those found in bottlenose dolphins in theNorth of Europe. The 2,3,7,8-TCDD toxic equivalent (TEQ) in blubber and liver was calculated for the tox-icity assessment of mono-ortho substituted PCBs congeners (CB105, CB118, CB156). It is important tomention that TEQ values and p,p0-DDE concentration in adult male specimens are approaching the levelsassociated with adverse effects found in marine mammals. The information provided represents the firsttissue loads of organochlorine compounds in small cetaceans from this area. # 2008 Wiley Periodicals, Inc.

Environ Toxicol 23: 200–210, 2008.

Keywords: bottlenose dolphins; organochlorine; tissue analysis; Canary Islands

INTRODUCTION

The Canary Islands (Spain) are located in the North Atlan-

tic Ocean near Europe and North Africa, in the subtropical

zone between 138 and 188 W longitude and 27.58 and 298N latitude. Together with the Azores, Madeira, and the CapVerde Islands, they form the Macaronesian biogeographicregion. The oceanographic characteristics of these volcanicislands make possible the presence in large numbers of avariety of cetaceans. More than 30 species have been iden-tified along the coast of the Canary Islands, some of themmigratory, others with sedentary local populations(SECAC, 2003; Culik, 2004). Some of these animals, suchas bottlenose dolphins, are within Annex II of the Habitats

Correspondence to:M. Carballo; e-mail: carballo@inia.es

Contract grant sponsor: National Researching Plan.

Contract grant number: REN 2002-04162-CO2-02.

Published online 23 January 2008 in Wiley InterScience (www.

interscience.wiley.com). DOI 10.1002/tox.20322

�C 2008 Wiley Periodicals, Inc.

200

Directives (Directive 92/43/CEE) and need specialprotection.

The bottlenose dolphin (Tursiops truncatus) is a small

odontocete cetacean widely distributed in temperate seas

worldwide. In the Canary Islands, some groups of sub pop-

ulations of bottlenose dolphins are considered as resident

(SECAC, 2003). This dolphin species has a number of bio-

logical traits that make it prone to accumulating organo-

chlorinated compounds and it is a useful sentinel for moni-

toring levels of fat-soluble contaminants in the coastal

waters (O’Shea and Tanabe, 2003; Wells et al., 2004;

Houde et al., 2005). These characteristics stem from their

high trophic level, their high lipid content, their longevity,

and the fact that they are a near-shore species feeding in

coastal waters and with a relatively high metabolic rate

(Borrell and Aguilar, 2005). This places them among the

marine mammals with the largest amounts of persistent

organochlorines accumulated. Organochlorine contami-

nants (OCs), such as polychlorinated biphenyls (PCBs) and

chlorinated pesticides, are persistent, lipophilic, with bioac-

cumulative capacity and can biomagnify via the food chain

(Borrell et al., 1995; Colborn and Smolen, 2003; O’Shea

and Tanabe, 2003). They are also suspected of producing

serious pathological disorders in marine mammals, such as

reproductive (Schwacke et al., 2002) and endocrine

(Tanabe, 2002) impairment, depression of the immune

function (De Guise et al., 2003), and carcinogenic effects

(Ylitalo et al., 2005). These not only affect the health of

individual specimens but also could have long-term detri-

mental effect on the population as a whole.

There is a substantial body of published references on

organochlorine tissue levels in the Atlantic bottlenose dol-

phin (Kuehl et al., 1991; Berrow et al., 2002; Hansen et al.,

2004) However, this information is not useful in evaluating

the organochlorine levels in these species in the Canary ar-

chipelago. Agriculture, trade, tourism and small-scale

industries dominate the economy of these islands. Shipping

is another important economic factor in this area. These

activities are a potential source for a variety of man-made

compounds. The proximity of the Moroccan coast (100

km), where DDT and their derivatives are still being used

(UNEP, 2003), should also be taken into consideration.

This study presents concentrations of organochlorine

compounds found in the blubber and liver of bottlenose dol-

phins stranded during the last 10 years in the Canary

Islands. The analyzed compound were 11 PCB congeners,

DDT and its metabolites and 14 non-DDTs pesticides:

chlordane, cis-nonachlor, trans-nonachlor, heptachlor, hep-tachlor-epoxide, dieldrin, endosulfan I and II, endrin, hexa-

chlorohexanes (HCHs), hexachlorobenzene (HCB), and lin-

dane. The levels found were compared with similar studies

in other geographic regions. Their toxicological impact is

also discussed. This article presents the first information

about persistent organochlorine compounds in this small

cetacean from the Canary Islands.

MATERIALS AND METHODS

Sample Collection

Samples of blubber and liver tissues from 12 bottlenose

dolphins (Tursiops truncatus) were obtained from the ma-

rine mammals’ tissue bank of the Histology and Pathology

Unit at the Veterinary School of the University of Las

Palmas (Gran Canaria). The samples were collected from

animals stranded along the coast of the Canary Islands

(Fig. 1) from 1997 to 2005. They were stored in a frozen

state at 2208C. The tissue sampling and state of decompo-

sition of stranded specimens were determined following the

Kuiken and Garcia-Hartmann (1991) methodology. The

samples used for this study were fresh samples as recom-

mended by Borrell and Aguilar (1990) for this type of

study. Three nutritive status (good, poor, and very poor) of

stranded animals were established based on morphological

characteristics like development of the dorsal muscle and

bone prominence. The animals analyzed in this study con-

sisted of seven males and four females. The body length

and maturity of the sexual organs were used to classify the

animals into juveniles and adults. The ages were only esti-

mated in six individuals from dental analysis (Slooten,

1991). Biological information obtained from the tissue

bank was gathered for each specimen in Table I.

Analytical Methods

Extraction and quantification of the chlordanes (CHLs)

(chlordane cis1trans, cis-nonachlor, trans-nonachlor, hep-tachlor, heptachlor-epoxide), DDTs (p,p0-DDT, o,p0-DDT,p,p0-DDD, o,p0-DDD, p,p0-DDE, and o,p0-DDE), dieldrin,endosulfan, endrin, hexachlorohexanes (HCHs) (a-HCH, b-HCH, c-HCH), hexachlorobenzene (HCB), lindane, and

PCBs congeners [IUPAC (28, 52, 101, 105, 118, 138, 149,

153, 156, 180, and 187)] were conducted according to the

methods reported in UNEP/IOC/IAEA (1986/1988). The

quality control was managed according to guidelines given

in Quality Assurance for Marine Environmental Measure-

ments (Quasimeme). Briefly, the defrosted samples were

ground with anhydrous sodium sulfate and the lipid phase

extracted in a Soxhlet with a mixture of dichloromethane

and n-hexane (residue-free quality) for 8 h. The extract

obtained was concentrated and a portion of it was used to

determined quantity of extractable fat per gram of blubber.

The rest after purification with Jensen treatment two ali-

quots were separated. A portion of this extract was mixed

with sulfuric acid for the clean-up and used to determine

the PCBs concentration. A further amount was passed

through a mix column and the n-hexane recovered for anal-

ysis for organochlorine pesticides. The sample extracts

were injected into a gas chromatograph (Hewlett-Packard

5890) equipped with an electron capture detector (ECD) at

3008C. The analyses were made using two capillary

201ORGANOCHLORINE RESIDUES IN BLUBBER AND LIVER OF BOTTLENOSE DOLPHINS

Environmental Toxicology DOI 10.1002/tox

chromatographic columns : HP-5; 60 m length, 0.25 mm

i.d. with 1.0 lm film thickness with 5% phenylmethylsilox-

ane and HP-50 of 60 m length, 0.53 mm i.d. with 1.0 lmfilm thickness with 50% phenylmethylsilicone. The column

temperature program was started at 608C, held for 5 min

and then increased to 2808C in 25 min. The carrier gas was

helium at a linear flow of 50 cm3/min. The injector port

temperature was 2908C. The concentration of individual

organochlorine was quantified on the basis of peak areas

and comparison with a calibration curve obtained from the

corresponding standards. The standards were those avail-

able from Dr. Ehrenstorfer (Dr. Ehrenstorfer, Germany),

Riedel de Haen (Sigma-Aldrich, Laborchemikalien, Ger-

many) and AccuStandard (CT, USA), all with 97% purity.

Procedural blanks were analyzed simultaneously with sam-

ples to check for interference or contamination from sol-

vents and glassware. The detection limit of all analyses was

2.3 ng g21 of tissue wet weight and the recovery efficiency

varied between 80 and 90% for spiked samples.

The ratio p,p0-DDE/DDTs was estimated as an indica-

tion of recent exposition to DDT. The ratio DDTs/PCBs

indicating predominantly agrarian or industrial compounds

was also calculated. The blubber to liver concentration ratio

of OCs was estimated. The 2,3,7,8-TCDD toxic equivalents

(TEQs) approach in blubber and liver, using toxic equiva-

lent factors (TEF) reported by Ahlborg et al. (1994), was

adopted for the toxicity assessment of mono-ortho substi-

tuted PCBs congeners (CB105, CB118, CB156).

RESULTS AND DISCUSSION

The presence of cetacean in the Canary Archipelago has

lead to the Canary Islands being designated, since 2003, as

a Particularly Sensitive Sea Area for the International Mari-

time Organization (IMO). It is now considered a protected

marine area. To manage such a site it is essential to know

what threats could affect the cetaceans and their habitat,

including the levels of organochlorine contaminants and to

assess their impact on the health of these animals. The exis-

tence of a marine mammal tissue bank has made possible

the study of samples of T. truncatus, a coastal top predator

species, that can accumulate relatively high loads of

contaminants.

Levels of organochlorine compounds in the blubber and

liver of bottlenose dolphins are given in Tables II and III,

respectively. All concentrations are expressed in ng g21

wet weight (ww), concentration in lipid weight (lw) for

total PCBs and total DDTs in the blubber were also

included. The relative contribution of the different com-

pounds analyzed in the two tissues was shown in Figure 2.

No statistical analysis was made for the small sample size.

PCBs were found in greatest concentrations in the two tis-

sues analyzed. The sum of 11 PCBs in the blubber ranged

from 301 to 33,212 ng g21 ww (990 to 136,679 ng g21 lw)

and in the liver between 373 and 52,374 ng g21 ww. In

males, the average SPCBs concentration in the blubber was

12,736 ng g21 ww (range: 1972–33,212 ng g21 ww) and in

females 2899 ng g21 ww (range: 301–7810 ng g21 ww). It

can be observed that the tissue concentrations in adult

females are lower than in adult males and juveniles. It is

known that females offload a large portion of their chlori-

nated compounds through transfer to offspring during preg-

nancy and lactation (Borrell et al., 1995; Ridgway and

Reddy, 1995; Borrell and Aguilar, 2005). The magnitude of

the reproductive transference is extremely variable, ranging

from 7 to 100% depending on the species and the com-

pound (Houde et al., 2005). In male and juveniles, the OC

loads tend to increase with the age because the uptake of

contaminants usually exceeds metabolization and excretion.

In adult males this pattern continues throughout their life-

span and OC residues in fat tissues may reach very high

levels (Borrell et al., 1995; Wells et al., 2005).

A wide range in the concentrations of PCBs was also

detected in the liver. In females, SPCB concentration in the

liver ranged from 833 to 1035 ng g21 ww and in males

TABLE I. Details of the bottlenose dolphins (Tursiops truncatus) stranded in Canary Islands

Ref No. Sex

Sexual

Condition

Length

(cm) Age Animal

Nutritive

Status Year Location

Cet 43 F immature 220 dead poor 1997 Tenerife

Cet 50 F mature 285 21 alive poor 1998 Gran Canaria

Cet 78 M mature 294 31 alive poor 1999 Gran Canaria

Cet 93 M immature 257 4 dead poor – Tenerife

Cet 94 M immature 260 5 dead good – Tenerife

Cet 124 M mature 305 20 dead poor 2001 Tenerife

Cet 144 M immature 167 alive good 2001 Gran Canaria

Cet 145 F mature 280 16 alive good 2001 Gran Canaria

Cet 168 M immature 217 alive good 2002 Tenerife

Cet 171 F immature 238 4 alive good 2002 Tenerife

Cet 311 M immature 265 dead poor 2005 Fuerteventura

M, Male; F, Female.

202 CARBALLO ET AL.

Environmental Toxicology DOI 10.1002/tox

from 373 to 52,374 ng g21 ww. The mean of the blubber/

liver PCB ratio was 7.2 (Table III). In general, we found

that the PCB levels in the liver were lower than those

found in the blubber. However, the comparison of OC

concentrations in these two tissues should be based on

total lipid weight (Tilbury et al., 1999). Differences

between tissues was largely accounted for by the differ-

ence in total lipid content (Stein et al., 2003), lipid-nor-

malized concentration is measured, the OC concentration

can be very similar (Tilbury et al., 1999). It should be

emphasize that in one adult male (Cet 78), the ratio blub-

ber/liver was inverted and the PCB concentrations in the

liver were high. The poor nutritive status and low lipid

composition of the blubber of this specimen may reflect

mobilization of PCBs from the blubber. However, other

should not be discarded. The profile of OCs in the liver

and blubber of dolphins stranded in the Canary Islands are

very similar, as was found in stranded dolphins on the US

Atlantic coast (Stein et al., 2003).

In this study, only juvenile and adult male samples were

used to compare the magnitude of contamination with other

studies. Because no data on OCs levels in odontocetes spe-

cies from Canary Island waters are available, our results

were compared with small cetaceans from other geographi-

cal regions (Table V). PCB concentrations in the blubber of

adult males from the Canary Islands presented ranges

between those observed in T. truncatus on the Irish coasts

(Berrow et al., 2002) and levels obtained in the US Atlantic

coast (Hansen et al., 2004). Higher concentration are found

in Mediterranean bottlenose dolphins, well known for their

extremely high OCs burden (Aguilar et al., 2002; Borrell

and Aguilar, 2005, 2007).

TABLE II. Organochlorine compounds (ng g21 on ww) in blubber of Tursiops truncatus

Reference No.

Cet 50

(30.4)

Cet 78

(10.2)

Cet 94

(50.4)

Cet 124

(24.3)

Cet 144

(56.1)

Cet 145

(54.7)

Cet 168

(57.4)

Cet 171

(55.7)

Cet 311

(35.0)

Organochlorine pesticides

Chlordane 2 112 32 585 282 57 2,940 3,040 140

Trans-nonachlor 6 753 135 1,046 149 13 497 288 125

Cis-nonachlor 2 42 22 411 133 14 86 55 44

Dieldrin 2 36 21 51 89 9 183 80 –

Hexaclorobencene 2 11 4 33 98 5 70 19 –

o,p0-DDE 2 11 4 80 15 nd 91 32 nd

p,p0-DDE 106 12,500 725 18,550 2,324 141 4,570 3,070 344

o,p0-DDD 2 133 14 166 59 6 389 113 4

p,p0-DDD 6 308 40 257 175 21 340 169 7

o,p0-DDT 3 480 35 333 70 7 310 136 6

p,p0-DDT 31 2,160 132 1,664 704 48 1,130 687 103

SDDTs 147 15,592 950 21,050 3,347 222 6,830 4,207 464

SDDTs lw 483 152,862 1,885 86,625 5,977 406 11,899 7,553 1,326

PCB congeners

CB 28 nd nd nd nd nd nd 6 3 nd

CB 52 nd 18 14 80 21 nd 38 28 29

CB 101 9 87 66 577 308 12 360 184 181

CB 105 nd 27 14 122 34 nd 33 29 41

CB 118 8 115 66 876 288 16 377 248 113

CB 138 44 1,650 333 6,350 1,460 52 1,170 1,160 2,575

CB 149 19 693 146 2,390 652 25 612 512 152

CB 153 76 2,890 589 10,500 2,930 133 2,200 2,320 4,870

CB 156 7 250 38 517 210 12 33 39 213

CB 180 84 3,100 436 7,010 2,550 172 1,240 1,850 3,475

CB 187 54 2,140 270 4,790 1,680 163 1,200 1,440 1,215

ICES 7 PCBa 221 7,860 1,504 25,393 7,557 385 5,391 5,793 11,247

SPCB 301 10,970 1,972 33,212 10,133 585 7,269 7,810 12,859

SPCB lw 990 107,549 3,912 136,679 18,062 1,069 12,664 14,021 36,740

Ratios

p,p0DDE/SDDT 0.72 0.80 0.76 0.88 0.69 0.63 0.67 0.73 0.74

SDDT/PCB 0.48 1.4 0.48 0.63 0.33 0.37 0.93 0.53 0.03

SDDTs and SPCBs were also expressed on lipid weight (lw). The values within parentheses are lipidic %.a ICES 7 PCB 5 S28 1 52 1 1011 1181 1381 1531 180; nd, not detectable. No sample in Cet 43 and Cet 93.

203ORGANOCHLORINE RESIDUES IN BLUBBER AND LIVER OF BOTTLENOSE DOLPHINS

Environmental Toxicology DOI 10.1002/tox

Similar PCB congener compositions were observed in

the two tissues, apparently with a relatively high contribu-

tion of hexa and hepta-chlorobiphenyls. PCB congener 153

contributed most to the SPCB, with a mean percent contri-

bution of 29% in male blubber and liver (Fig. 3). This con-

gener is abundant in higher chlorinated PCB formulations

and is known to be very persistent. Hexa and hepta-PCBs

are congeners with higher chlorine content and usually

more difficult to metabolize (Watanabe et al., 2000; Col-

born and Smolen, 2003) and their biomagnification poten-

tial through the food chain is high (Weisbrod et al., 2001).

These compounds are predominant in top cetacean preda-

tors (Colborn and Smolen, 2003).

To know the toxicological significance of PCBs concen-

trations in this limited sample group of dolphins, the signifi-

cance of the total PCBs were first considered. The concen-

trations of PCBs in the dolphins of this study are quite far

from the high concentrations detected in the blubber of dol-

phins in mass stranding episodes. Thus, mean concentra-

tions of SPCB 65,100 ng g21 ww were detected in male

bottlenose dolphins in the Gulf of Texas (Kuehl and Hae-

bler, 1995) and up to twice that level was detected in the

blubber in victims of large-scale deaths of dolphins in the

Mediterranean Sea (Corsolini et al., 1995). Wagemann and

Muir (1984) considered that PCB concentrations [50,000

ng g21 in blubber may put the health of cetaceans at risk.

Kannan et al. (2000) and Jepson et al. (2005) estimated a

threshold level for observed effects on reproduction and im-

munity in marine mammals’ blubber close to 12,000 ng

g21 PCB. Levels in adult males in this study were higher

than these and, on the basis of this criterion, PCBs could

present a health risk. It is important to note that in male

adult Cet 78, where the highest SPCBs levels were detectedin the liver, a lymphoma was also identified (Jaber et al.,

2005). The induction of carcinoma by PCBs in other marine

mammals has been confirmed by Ylitalo et al. (2005). In

TABLE III. Organochlorine compounds (ng g21 on ww) in liver of Tursiops truncatus

Reference No.

Cet 43 Cet 50 Cet 78 Cet 93 Cet 94 Cet 124 Cet 168

Organochlorine pesticides (OCPs)

Chlordane 6 9.7 58.8 130 49.1 43 502

Cis-nonachlor nd 3.4 21.5 24.4 13.4 35.8 7

Trans-nonachlor 24.1 11.9 138 166 59.5 58.7 nd

Dieldrin 10.6 4.3 nd 23.3 27.4 13.2 10

Hexaclorobencene 12.9 2.4 2.2 9.4 7.4 3.3 9

O,p0-DDE 1.1 1.4 2.6 11.2 3.4 6 5

P,p0-DDE 372 184 2,320 2,820 590 1,050 196

O,p0-DDD 7.3 3.8 31.9 91.5 16.1 15.7 19

P,p0-DDD 23.4 8.3 45.6 100 27 18.7 21

O,p0-DDT nd nd nd nd nd 12.7 5

P,p0-DDT 56.7 24.3 129 148 69.3 86.8 19

SDDTs 460 220 2,529 3,171 706 1,190 265

PCB congeners

CB 28 nd nd nd nd nd nd nd

CB 52 6 6 45 15 13 9 4

CB 101 33 25 546 103 66 37 16

CB 105 6 6 79 22 14 12 nd

CB 118 28 21 764 95 55 52 18

CB 138 150 111 8,910 1,070 328 453 58

CB 149 64 59 3,730 506 162 185 29

CB 153 274 222 15,400 1,920 575 775 107

CB 156 24 17 1,100 137 42 50 2

CB 180 279 217 13,400 1,620 450 580 79

PCB 187 169 147 8,400 1,150 323 444 59

ICES 7 PCBa 770 602 39,065 4,823 1,517 1,906 282

SPCB 1,035 833 52,374 6,638 2,028 2,597 373

Ratios

p,p0DDE/ SDDT 0.80 0.83 0.91 0.88 0.83 0.89 0.74

SDDT/PCB 0.4 0.26 0,05 0.47 0.3 0.45 0.7

PCBs blubber/liver – 3 0.2 – 1 13 19

a ICES 7 PCB 5 S28 1 52 1 1011 1181 1381 1531 180; nd, not detectable.

No sample in Cet 144, Cet 145, and Cet 311.

204 CARBALLO ET AL.

Environmental Toxicology DOI 10.1002/tox

addition, it is known that individual PCB congeners differ

greatly in their toxic potency. When the toxicity of PCB-

dioxin like, particularly of the mono-ortho-coplanar conge-ners (CB105, CB118, and CB156) was assessed in the blub-

ber and liver of dolphins stranded in the Canary Islands,

using the 2,3,7,8-TCDD equivalents (TEQs) concept (Ahl-

borg et al., 1994), mean values of 104 pg g21 ww were esti-

mated (Table IV). Although the total TEQ could be higher,

in the absence of any evaluation of other dioxin-like PCB

congeners such as the highly toxic non-ortho coplanar con-

geners, the level was 100 times lower than that reported to

cause immunological suppression and mortality in dolphins

(Kannan et al., 1993; Corsolini et al., 1995). The estimated

values would probably be close to those of healthy popula-

tions of marine mammals, i.e., in the range of 100–5000 pg

g21 ww (Corsolini et al., 1995). However, it is reasonable

to assume that the damage of planar TEQs may elicit

weight loss, and reproductive, immunological and hepato-

toxic effects through their interaction with the aryl hydro-

carbon receptor (Carvan et al., 2003). So in the males Cet

78, Cet 124, Cet 144 of bottlenose dolphins from the Ca-

nary Islands the TEQ values were greater than the threshold

concentration for seals immunosuppression, estimated at

209 pg g21 (Ross et al., 1995) and also higher than the 50%

effective concentration (EC50) for mink reproduction, esti-

mated at 169 pg g21 (Leonards et al., 1998). Although it is

not possible to extrapolate the effects on seals to those in

dolphins, these may provide an approximate estimation of

the potential effects of PCB contamination on these

dolphins.

Within the organochlorine pesticide compounds, the

DDT groups were present in the highest concentrations.

The concentration of DDTs in the blubber ranged from 147

to 21,050 ng g21 ww (483–86,625 ng g21 lw) (Table II)

and in the liver from 220 to 3171 ng g21 ww (Table III). In

males, the average SDDT concentration in the blubber was

9553 ng g21 ww (range: 950–21,050 ng g21 ww) and in the

liver 1572 ng g21 ww (range: 265–3171 ng g21 ww) In

females, the average SDDT concentration in the blubber

was 1525 ng g21 ww (range: 147–4207 ng g21 ww) and in

the liver range from 220 to 566 ng g21 ww. The male

Fig. 1. Geographical situation. [Color figure can be viewed in the online issue, which isavailable at www.interscience.wiley.com.]

Fig. 2. Percentage compositions of organochlorinatedcompounds (OCs) in Tursiops truncatus blubber and liver tis-sues. PCs*, pesticide chlorinated non-DDTs; CHL, chlor-dane; t-nona, trans-nonaclor; c-nona, cis-nonachlor; dield,dieldrin; OCs, organochlorine compounds. [Color figure canbe viewed in the online issue, which is available at www.interscience.wiley.com.]

205ORGANOCHLORINE RESIDUES IN BLUBBER AND LIVER OF BOTTLENOSE DOLPHINS

Environmental Toxicology DOI 10.1002/tox

bottlenose dolphins presented average concentrations of

SDDT higher than those previously reported in the north of

Europe and much lower than those found in the Mediterra-

nean dolphins (Table V).

p,p0-DDE was the DDT group compound present at the

highest concentration in the two tissues, contributing 73%

(63–88%) to SDDT in the blubber and 83% (74–91%) in

the liver (Fig. 2). It was followed in the blubber by p,p0-DDT (17%), p,p0-DDD (4%), and o,p0-DDT (3%). Most

studies of organochlorinated pesticides in dolphins and

other cetacean species have reported that p,p0-DDE contrib-

uted the most to SDDT (O’Shea and Tanabe, 2003), which

is consistent with the present results. The relatively high

fraction of p,p0-DDE indicates the metabolic capacity for

conversion of DDTs to DDE and the absence of metabolic

enzymes to detoxify p,p0-DDE, as has been shown in ceta-

ceans in general (Colborn and Smolen, 2003). The isomeric

composition of DDTs in the bottlenose dolphin of the Ca-

nary Islands is similar to that of other dolphins with a simi-

lar diet based mostly on fish, cephalopods, and shrimp

(Karuppiah et al., 2005).

Normally the p,p0-DDE/DDT ratio in environmental

media is used to evaluate the chronology of the usage of

DDT compounds. DDT residue levels were found to be

maximum in the 70–80 s and then decreased (Aguilar et al.,

2002; Aguilar and Borrell, 2005). Although DDT levels

have decreased since its use has been severely restricted

worldwide, an increase has been noted in the concentration

of its main metabolite, p,p0-DDE (Aguilar and Borrell,

2005). When the ratio p,p0-DDE/DDTs in marine mammals

is 0.7, it can be assumed that the exposure to this pesticide

is not recent. The p,p0-DDE/DDTs ratios in the blubber of

bottlenose dolphins from the Canary Islands were between

0.63 and 0.88 (Table II). Similar ratios were found during

the 1990s in Mediterranean dolphins (Marsili and Focardi,

1997), but lower than those found in the same area 10 years

later (Aguilar and Borrell, 2005). This could well indicate

more recent inputs in the Canary Islands than on the Medi-

terranean coast.

The mean DDTs/PCBs ratio in this area of 0.63 (Table

II) indicates a predominance of industrial inputs over those

associated with agriculture, and is similar to the pattern

observed in areas of the North Atlantic and Mediterranean,

which are mostly industrial (Aguilar et al., 2002).

As for the toxic effects of DDTs, Wagemann and Muir

(1984) suggest that the threshold of DDT concentrations

usually associated with reproductive failure and pathologi-

cal alterations in cetaceans was upward of 50,000 ng g21 in

the blubber. However, much lower concentrations have

been associated in cetaceans with neurological disorders,

immunosupression, and endocrinal pathologies (Lahvis

et al., 1995; Tanabe, 2002; De Guise et al., 2003). The con-

centrations of p,p0-DDE in some adult males analyzed in

this study are possibly hazardous. The concentration of

p,p0-DDE bioaccumulated in bottlenose dolphin liver (Cet

78, Cet 93, Cet 124) is more than twice the effective dose

that inhibits androgen binding to androgen receptor in rat

liver cells and is related to delayed puberty in male rats

(Kelce et al., 1995). Also, these concentrations of p,p0-DDEin the liver are close to levels that could, in male Dall’s por-

poise, lead to a reduction of testosterone levels in the blood

(Tanabe et al., 1994).

Following DDTs in the organochlorinated pesticides

detected at the highest concentrations were the chlordane

compounds. The sum of chlordanes (SCHL), that includesonly chlordane, cis-nonachlor, and trans-nonachlor, in the

blubber presented an average of 1159 ng g21 in females

and 1419 ng g21 in males (Table II). Lower SCHL concen-

Fig. 3. Percentage compositions of PCBs congeners in Tur-siops truncatus blubber and liver tissues.

TABLE IV. Mean and range concentrations of mono-ortho coplanar PCBs and their 2,3,7,8-TCDD toxic equivalents(TEQs) in Tursiops truncatus blubber and liver tissue

PCBs TEFa

Blubber Liver

Concentration

(ng/g ww)

TEQs

(pg/g ww)

Concentration

(ng/g ww)

TEQs

(pg/g ww)

105 0.0001 50 (14–122)b 5 (14–12) 20 (nd–79) 2 (nd–8)

118 0.0001 293 (8–876) 29 (0.8–88) 138 (18–764) 14 (2–76)

156 0.0005 140 (7–517) 70 (3–258) 176 (3–1,100) 88 (1.5–550)

aToxic equivalents factor values were obtained from Ahlborg et al. (1994).bValues in parentheses indicate the range.

206 CARBALLO ET AL.

Environmental Toxicology DOI 10.1002/tox

TABLEV.

Levels

oforganochlorinecompounds(ng/g

ww)in

blubberofmalesofTursiopstruncatusfrom

AtlanticOceancoast

Location

Year

Sam

ple

Number

PCBs

DDTs

CHLs

HCB

Reference

NorthAmerican

AtlanticCoast

Massachusetts

1992

Sn5

4a

1,1006

640

3,3006

3,100

1806

120

166

6Stein

etal.,2003

NorthCarolina

1995–2000

BB

n5

5,n5

29b

13,245c,7,624c

15,571c,8,164c

2,106c,1,106c

Hansen

etal.,2004

South

Carolina

1999–2001

BB

n5

4,n5

2b

11,314c,5,622c

10,923c,5,511c

4,401c,2,066c

IndianRiver

Lagoon,

Florida

2002

BB

n5

95,777c

5,058c

2,378c

GulfofMexicocoast

GulfofMexico

1994

BB

n5

220,4476

560

115,8326

55,877

4,6646

1,402

1646

0.2

Reddyetal.,1998

MatagordaBay,Texas

1992

BB

n5

763,0346

37,520c

Schwacke

etal.,2002

SarasotaBay,Florida

1997–1999

BB

n5

649,1476

5,544c

2000–2001

BB

n5

16

54,0316

36,936c

Welletal.,2004

Texas

toFloridacoast

1990–1993

Sn5

64a

24,2816

17,584

25,4446

10,071

5,4506

3,447

3736

226

Stein

etal.,2003

EuropeanAtlanticcoast

ShannonEstuary,Ireland

2000

BB

n5

65,0106

6,017

3,1706

4,216d

5526

500

406

35

Berrowetal.,2002

CanaryIslands

1993–2001

Sn5

712,7366

9,788

12,7366

9,788

1,2556

1,182

436

30

Ourstudy

MediterraneanSea

Coast

Mediterraneancoast

ofSpain

1990–2002

Sn5

9126,3306

78,658c

52,6956

26,102c

9386

1090c

Borrelland

Aguilar,2007

AdriaticcoastofItaly

1992

Sn5

5562,0006

316,000

187,6006

196,610

Corsolinietal.,1995

1999–2000

Sn5

517,5466

4,516

Storelliand

Marcotrigiano,2003

African

Atlanticcoast

WestcoastofSouth

Africa

1980s

Sn5

62,9106

2,665

4,5446

4,105

226

9DeKock

etal.,1994

Dataofstranded

anim

als(S)andin

blubber

biopsies

offree-ranginganim

als(BB)since

1990wereconsidered.

aMale1

Fem

ale.

bJuvenile.

cOriginaldatein

lipid

weightwhichistransform

edto

wetweightbytheequation:[lipid

wt.]3

100/lipids%

5[w

etwt.].When

noavailabledataexistsonthelipidiccontent,an

averagevalueof70%

isused(A

guilar

etal.,2002).

dp,p0DDE.

207ORGANOCHLORINE RESIDUES IN BLUBBER AND LIVER OF BOTTLENOSE DOLPHINS

Environmental Toxicology DOI 10.1002/tox

trations were detected in liver than in blubber, the mean

concentration in female liver being 27 ng g21 ww and

159.6 ng g21 ww in males (Table III). The predominance

of CHLs within non-DDT chlorinated pesticides has also

been reported in bottlenose dolphins of the US Atlantic

coast (Stein et al., 2003; Hansen et al., 2004), yet the same

does not occur in Atlantic white-sided dolphins on the Scot-

tish or Irish coasts (McKenzie et al., 1997). It has been sug-

gested that the distribution patterns for these compounds

are very much influenced by various local factors such as

point source usage and influx into the ecosystems via leach-

ing and drainage (Hansen et al., 2004). In this study, the

concentration of CHLs was 100 times lower than PCBs,

and similar differences have been described in other studies

(Table V). This could be explained by their lower inputs,

and the fact that they are more degradable and less persis-

tent than other organochlorine compounds. In this group we

found that trans-nonachlor and chlordane are the most

abundant compounds. Trans-nonachlor, containing nine

chlorine atoms, appears to be more resistant to metabolism

than other chlordanes, it seems that cetaceans have a rela-

tively low capacity to metabolize trans-nonachlor (Smyth

et al., 2000).

Dieldrin and hexachlorobenzene (HCB) are organo-

chlorinated pesticides, which were found in the animals an-

alyzed, but in very low concentrations. Dieldrin was

detected in all dolphin samples analyzed. Dieldrin concen-

trations in female dolphin samples had a mean of 30 ng g21

ww in the blubber and 7.5 ng g21 ww in the liver (Tables II

and III). Males had a mean dieldrin concentration of 76 ng

g21 ww in the blubber and 18 ng g21 ww in the liver

(Tables II and III). HCB concentration in female dolphins

was 8.5 ng g21 ww in the blubber and 7.6 ng g21 ww in the

liver (Tables II and III). Males had a mean HCB concentra-

tion of 43.2 ng g21 in the blubber and 6.2 ng g21 in the

liver (Tables II and III). Residues of these compounds have

been generally detected in very low concentrations in other

areas although concentrations of dieldrin higher than in this

study have been detected in adult male bottlenose dolphins

in the US North Atlantic coast and also in the Gulf of Mex-

ico (Table V). As for the concentrations of HCB, the high-

est levels for this compound have been found in dolphins in

the Sea of Japan (Tanabe, 2002). It has been suggested that

HCB distribution is heavily dependent on the temperature,

with HCB migrating mainly to cold areas or higher lati-

tudes (Struntz et al., 2004).

This study, conducted with small number of dolphins, is

the first one to record the range of concentration of some

OCs in marine mammals in the Canary Islands. The results

are consistent with those reported in other areas for this

species. In toxicological terms, the levels for some PCB

congeners and p,p0-DDE found in the blubber and liver of

adult males could present a certain risk to the health of

these animals since they are close to the concentrations that

could produce immunosupression and antiandrogenic

effects in other marine mammals. It must also be noted that

the impact of these compounds on the health of the animals

studied should be tackled from the point of view of their

combined effects. So far, little is known about the cumula-

tive impact of the complex mixtures of organochlorine on

dolphin health (Struntz et al., 2004). In-depth studies of this

situation are called for in order to protect the health of ma-

rine mammals which present a substantial capacity to accu-

mulate lipophilic pollutants.

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