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: [email protected]
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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