Organochlorine pesticides and polychlorinated biphenyls in fin whales (Balaenoptera physalus) from the Gulf of California.

Abstract

The present study reports unique data on concentrations of several classes of organochlorine pesticides and polychlorinated biphenyls in blubber biopsies from healthy living fin whales (Balaenoptera physalus) from the Gulf of California, Mexico, one of the most isolated and unstudied population in the world. OC levels in this population were generally lower than levels reported in fin whales from other regions. The rank order of OCs were SigmaDDTs (range from 300 to 2400 ng g(-1) lw) > SigmaPCBs (range from 40 to 290 ng g(-1) lw) > SigmaHCHs (range from <LOQ to 92 ng g(-1) lw) > or = SigmaCHLORs (from < LOQ to 100 ng g(-1) lw). The most abundant OC pesticide measured was the DDT metabolite, p,p'-DDE. The PCBs 138, 153, and 180 were the most abundant PCBs congeners found in the fin whales samples. Males had significant higher concentrations of SigmaOC, SigmaDDTs and SigmaPCBs than females (P < 0.05), although the p,p'-DDE/SigmaDDTs ratios were similar between the sexes. Although the OC concentrations found in this population were generally below the levels that would be expected to cause deleterious health effects, the maximum values observed (2700 ng g(-1) lw) in some animals were higher than those associated with reproductive effects in whales. Given the small population size and highly isolated characteristics of Gulf of California fin whales, health effects in individuals could readily translate into population-level effects. Future research on this topic will be necessary to better understand the role that these compounds may have on the health of this population.

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Organochlorine Pesticides and Polychlorinated
Biphenyls in Fin Whales (Balaenoptera physalus)
from the Gulf of California
Carlos Alberto Nin ˜o-Torres,1,3Tania Zenteno-Savı ´n,2Susan C. Gardner,2
Jorge Urba ´n R.3
1Postgraduate Program in Marine Sciences and Limnology, National Autonomous University of
Mexico, Postal Box 70-305, Ciudad Universitaria, Me ´xico 04510, D.F. Mexico
2The Northwestern Center of Biological Research, Mar Bermejo 195, Playa Palo Santa Rita,
La Paz, Baja California Sur, Me ´xico 23090
3Marine Mammal Laboratory, Autonomous University of Baja California Sur, Ap. Post. 12-B,
La Paz, Baja California Sur, Me ´xico 23081
Received 30 October 2008; revised 7 April 2009; accepted 7 April 2009
ABSTRACT: The present study reports unique data on concentrations of several classes of organochlor-
ine pesticides and polychlorinated biphenyls in blubber biopsies from healthy living fin whales (Balaenop-
tera physalus) from the Gulf of California, Mexico, one of the most isolated and unstudied population in
the world. OC levels in this population were generally lower than levels reported in fin whales from other
regions. The rank order of OCs werePDDTs (range from 300 to 2400 ng g21lw) [PPCBs (range from
g21lw). The most abundant OC pesticide measured was the DDT metabolite, p,p0-DDE. The PCBs 138,
153, and 180 were the most abundant PCBs congeners found in the fin whales samples. Males had signif-
icant higher concentrations ofPOC,PDDTs andPPCBs than females (P \ 0.05), although the p,p0-
tion were generally below the levels that would be expected to cause deleterious health effects, the
maximum values observed (2700 ng g21lw) in some animals were higher than those associated with
reproductive effects in whales. Given the small population size and highly isolated characteristics of Gulf
of California fin whales, health effects in individuals could readily translate into population-level effects.
Future research on this topic will be necessary to better understand the role that these compounds may
have on the health of this population.#2009 Wiley Periodicals, Inc. Environ Toxicol 00: 000–000, 2009.
Keywords: fin whale; Gulf of California; organochlorine; pesticides; PCBs; Balaenoptera physalus
40 to 290 ng g21lw)[PHCHs (range from\LOQ to 92 ng g21lw) ?PCHLORs (from\LOQ to 100 ng
DDE/PDDTs ratios were similar between the sexes. Although the OC concentrations found in this popula-
INTRODUCTION
Fin whales (Balaenoptera physalus, Linnaeus, 1758) from
the Gulf of California are year-round permanent residents
in the gulf with the same name, and are considered one of
the most isolated populations of this species (Be ´rube ´ et al.,
1998, 2002). With ?600 (estimates range from 400 to 800)
animals (Urba ´n-Ramı ´rez et al., 2005; Dı ´az-Guzma ´n, 2006),
this population constitutes a unique and separate unit of
conservation, which is vulnerable to anthropogenic and nat-
ural effects (Be ´rube ´ et al., 2002).
Exposure to persistent organic pollutants such as organo-
chlorine pesticides and polychlorinated biphenyls (PCBs)
in marine mammals has been associated with a number of
Correspondence to: C. A. Nin ˜o-Torres; e-mail: carlosalni@gmail.com
Contract grant sponsor: SEMARNAT-CONACYT
Contract grant numbers: SEMARNAT-2002-C01-0078, SEMARNAT-
2002-C01-1415
Published online in Wiley InterScience (www.interscience.wiley.com).
DOI 10.1002/tox.20508
?
C 2009 Wiley Periodicals, Inc.
1

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toxic effects (e.g., immune suppression, reproductive dys-
function, increased cancer incidence) (Reijnders, 1986;
Ross et al., 2000; Le Boeuf et al., 2002; Jepson et al., 2005;
Ylitalo et al., 2005). Organochlorine compounds (OCs) are
man made compounds that, due to their chemical and phys-
ical characteristics (high lipid affinity, high chemical stabil-
ity and low volatility), accumulate and biomagnify easily in
marine food webs (O’shea, 1999). Organisms containing
high lipids reserves, such as cetaceans, accumulate high
concentrations of OCs in their tissues. However, cetaceans
have a poor detoxifying potential for OCs (Fossi et al.,
2003), making them susceptible to deleterious effects
(Marsili and Focardi, 1996; Gauthier et al., 1997a). Marine
mammals encounter OC compounds initially during devel-
opment stages (e.g., gestational and lactation process)
through the transfer of fat-soluble contaminants from
mother to calf (Aguilar and Borrell, 1994), and later,
through the consumption of contaminated prey (Borrell
et al., 1995; Connolly and Glaser, 2002).
Despite decades of research assessing bioaccumulation
of OCs in marine mammals, we know relatively little about
contaminant exposure and accumulation in baleen whales.
In fin whales there have only been a few studies assessing
pollutant concentrations (Aguilar and Borrell, 1994; Marsili
and Focardi, 1996; Herna ´ndez et al., 2000; Fossi et al.,
2003), and most of these studies were based on samples
collected from the North Atlantic and Mediterranean Sea.
The aim of the present work is to provide unique data on
OC concentrations in healthy living fin whales from the
Gulf of California, on the west coast of Mexico. Contami-
nant levels in this population have not been previously
assessed and are compared to levels reported in fin whales
from other regions.
MATERIALS AND METHODS
Field Work
Subcutaneous blubber biopsies were obtained from 21
wild-ranging adult fin whales from the Gulf of California
during July 2004 and January 2005 (Fig. 1, Table I).
Whales were approached on board of a 25 foot boat
equipped with a 110HP outboard engine. All animals were
photographed and their features were identified to avoid
sampling the same individual two times. Biopsies bolts, a
regular crossbow aluminum bolt modified with a stainless
steel collecting tip (cylinder of 40 3 8 mm with three inter-
nal prongs to retain the tissue), stopper and floater, were
fired with a 65 Kg power-shot crossbow. Shots were made
at a distance of ?20 m from the body whale and biopsies
were taken dorsal-laterally near the dorsal fin base. Before
each shot, cleaned bolt tips were rinsed with ethanol (which
was allowed to evaporate) to avoid contamination.
Samples were divided in two portions; skin for genetic
sex determination, and blubber for OCs analysis. Skin sam-
ples were immersing in ethanol (biology molecular grade)
Fig. 1. Study area in the Gulf of California, Mexico. The
circle represents the area where fin whale biopsies were
collected.
TABLE I. General data of each fin whale sampled.
Female (F), and Male (M)
Individual CodeSex% Liplds Sampling year
Bp-270105-34
Bp270105-2
Bp270105-17
Bp-270105-05
Bp-270105-16
Bp-270105-55
Bp-270105-45
Bp-150604-16
Bp-050704-62
Bp-070704-71
Bp-070704-72
Bp-100704-88
Bp-270105-30
Bp270105-50
Bp270105-10
Bp-050704-66
Bp-040704-59
Bp-010704-50
Bp-160604-19
Bp-050704-67
Bp-050704-68
F
F
F
F
F
F
F
F
F
F
F
F
M
M
M
M
M
M
M
M
M
49
67
61
80
51
65
36
63
58
38
62
39
41
68
42
58
75
34
79
83
61
2005
2005
2005
2005
2005
2005
2005
2004
2004
2004
2004
2004
2005
2005
2005
2004
2004
2004
2004
2004
2004
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in plastic vials and blubber was wrapped in precleaned (ac-
etone) aluminum foil and stored in a plastic vial. Both por-
tions were transported at 248C to the laboratory where all
samples were stored at 2208C until chemical analyses
were performed.
Chemicals and Reagents
All solvents and reagents (HPLC grade) used in the current
study were purchased from the source indicated: pentane,
hexane and methylene chloride from Across Organics (Pis-
cataway, NJ); isooctane from Fisher Scientific Company;
Florisil (60–100 mesh), sodium sulfate and pesticide mix
(CLP) from Supelco (Belefonte, PA). Individual PCB con-
geners (PCB101, PCB105, PCB114, PCB128, PCB153,
PCB138, PCB156, PCB157, PCB170, PCB180, PCB189,
PCB190, PCB198, PCB200, and PCB209) were purchased
from Ultra Scientific (North Kingstown, RI). The surrogate
(1,2,3,4-tetrachlorodibenzo-p-dioxin) and internal standard
(standard [1,7,8-triclorodibenzo-p-dioxin]) were obtained
from Accustandard (New Haven, CT).
Laboratory Work
OCs and lipids were extracted at the Environmental and
Toxicological Laboratory at Centro de Investigaciones Bio-
lo ´gicas del Noroeste in La Paz, Mexico, using procedures
described previously (Nin ˜o-Torres et al., 2009). Briefly,
?0.3 mg of blubber sample, 40 mL of hexane/pentane (1:1
v/v), sodium sulfate (5 g) (Supelco, Belefonte, PA), and
250 ng of surrogate standard (1,2,3,4-tetrachlorodibenzo-p-
dioxin) were homogenized with a Polytron 3100 probe at
15000 rpm. Centrifugation (1509 3 g for 5 min) was used
to separate solids and lipid extracts from the homogenized
mixture. ?1 mL of extract was separated and used to deter-
mine the lipid content in the blubber by measuring the total
nonvolatile extract (expressed as percent total lipids)
according to standardized procedures (Sloan et al., 2004;
Gardner et al., 2007; Nin ˜o-Torres et al., 2009). The sample
extract was reduced to (1 mL at 308C in a Centrivap Con-
centrator System (Labconco; Kansas City, MO). In order to
separate OCs from interfering compounds (e.g., lipids) the
(1 mL sample extract was passed through a preconditioned
[20 mL of methylene chloride/hexane (1:1 v/v)] gravimet-
ric-flow-column packed with 10 g of Florisil (60–100
mesh; Fired to 7008C overnight, and stored at 1308C) and
eluted with 20 mL of methylene chloride/hexane (1:1 v/v)
(Bernal et al., 1992).
Selected OCs pesticides, including DDTs (o,p-DDE, o,p-
DDT, p,p0-DDE, o,p-DDD, p,p0-DDD and p,p0-DDT),
HCHs (a-HCH, b-HCH, c-HCH, and d-HCH), CHLORs (b-
chlordane, c-chlordane, heptachlor and heptachlor epoxy),
and PCBs (PCB-77, PCB-101, PCB-105, PCB-114, PCB-
126, PCB-128, PCB 153, PCB-138, PCB-156, PCB-157,
PCB 180, PCBs170 1 190, PCB-189, PCB-198, PCB-200,
and PCB-209)] were analyzed by gas chromatography mass
spectrometry (GC/MS). GC/MS analyses were performed
using an Agilent 6890N gas chromatograph equipped with
an Agilent 5973N mass spectrometer. A HP5MS capillary
column (30 m 3 0.25 mm 3 0.25 lm, 5% phenylmethyl
silicone) was used for compound separation. Two lL of the
clean extract were injected with an auto sampler injector
system (Agilent 7386). A splitless injection mode was used.
GC/MS was operated in the selective ion monitoring mode
for chemical identification and quantification. PCBs and
OC pesticides were determined separately using two differ-
ent GCMS programs. Data were acquired by an Agilent
GC/MSD ChemStation software. OCs concentrations were
calculated from the peak area of the sample relative to the
internal standard (1,7,8-TriCDD). The relative recovery of
the surrogate standard (1,2,3,4-TCDD) was employed to
correct for losses during the process.
Quality Assurance
Calibration curves for each compound analyzed were made
employing multilevel calibration solutions. All solutions
were prepared in house using isooctane as solvent. The GC
calibration standards and the internal standard solutions
were prepared such that the concentrations of the internal
standards in final sample extracts analyzed, were approxi-
mately equal to the concentrations of the internal standards
in the GC calibration standards. Two different calibration
standards solutions for OC pesticides [o,p-DDE, o,p-DDT,
p,p0-DDE, o,p-DDD, p,p0-DDD and p,p0-DDT, a-HCH, b-
HCH, c-HCH, d-HCH, CHLORs, b-chlordane, c-chlordane,
heptachlor, and heptachlor epoxy), and PCBs (PCB-101,
PCB-105, PCB-114, PCB-128, PCB 153, PCB-138, PCB-
156, PCB-157, PCB 180, PCBs170 1 190, PCB-189, PCB-
198, PCB-200, and PCB-209) were prepared at the follow-
ing concentrations: Level 1 at 0.002 ng lL21each com-
pound, level 2 at 0.004 ng lL21each compound, level 3 at
0.01 ng lL21each compound, level 4 at 0.05 ng lL21each
compound, level 5 at 0.1 ng lL21each compound, level 6
at 0.5 ng lL21each compound, level 7 at 1 ng lL21each
compound, level 8 at 4 ng lL21each compound, level 9 at
5 ng lL21each compound, level 10 at 10 ng lL21each
compound, level 10 at 20 ng lL21each compound.
The stability of GC/MS system was regularly tested
employing calibration standards; the system was considered
stable if the area of an analyte was within 615% of the
average of repetitions. To measure the accuracy of the
method, each sample set of 10 samples was analyzed with a
National Institute of Standards and Technology (NIST)
blubber Standard Reference Material (SRM 1945) and a
method blank to determine background interference. Upper
and lower control limits were used according to previously
established methods (Sloan et al., 2004). SRM results were
3
ORGANOCHLORINE PESTICIDES AND POLYCHLORINATED BIPHENYLS IN FIN WHALES
Environmental Toxicology DOI 10.1002/tox

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consider acceptable if the determined concentration for
more than 70% of analytes having NIST certified concen-
trations fell within the upper and lower control limits. This
criterion was not applied to analytes that do not have certi-
fied concentrations. Spiked samples were used to check
extraction efficiency and recoveries from extraction and
Florisil cleanup. Recoveries of the surrogate standard
ranged from 80 to 103%. The limits of quantification
(LOQ) for OCs ranged from 5 to 10 ng g21lipid.
Concentrations of OCs were lipid normalized and
reported as nanograms per gram lipid (ng g21lw), however,
for comparison purposes nonlipid corrected concentrations
[expressed on a wet weight basis (ng g21ww)] were
included in Table II. The concentration of total DDTs
(SDDT) was calculated by the sum of o,p-DDE, o,p-DDT,
p,p0-DDE, o,p-DDD, p,p0-DDD and p,p0-DDT. The total
hexaclorocyclohexanes (SHCHs) were calculated as the
sum of four isomers when those were detected; total chlor-
danes (SCHLORs) are reported as the sum of concentration
of b-chlordane, c-chlordane and heptachlor and heptachlor
epoxide when those were detected, and total PCBs concen-
tration (SPCBs) were calculated as the sum of congeners
PCB-101, PCB-105, PCB-114, PCB-128, PCB 153, PCB-
138, PCB-156, PCB-157, PCB 180, PCBs170 1 190, PCB-
189, PCB-198, PCB-200, and PCB-209, when these were
detected. Total organochlorine concentration (SOCs) was
determined as the sum of PCB congeners and OC pesticides
detected. Pollutants that were not detected in any sample
were removed from statistical treatment.
Limits of Quantitation (LOQ) were determinate accord-
ing protocols described by Sloan et al. (2004). The lower
limit of quantition for a given analyte in a given sample
was the concentration that would be calculated if the ana-
lyte had a GC/MS response area equivalent to its area in the
lowest level calibration standard used in the calibration.
When an analyte was not detected in a sample or had an
area that was smaller than its area in the lowest level cali-
bration standard used, the concentration of the analyte in
that sample was reported to be less than the value of its
lower limit of quantitation.
Statistical Analyses
Analytes that were not detected in any sample or had an
area that was smaller than the analyte area in the lowest
level in the GC calibration curve level used, were reported
as less than the lowest limit of quantification (\LOQ). For
calculation of the mean,\LOQ values were replaced with
a random number between LOQ and one half LOQ.
Kolmogoroff-Smirnoff-Lillifors test was used to evalu-
ate normality, and the Kruskall-Wallis test was employed
to identify differences between sexes. The null hypothesis
was rejected if the P value was\0.05. All statistical analy-
ses were conducted using STATISTICA 6.0 (StatSoft). Val-
ues represent mean 6 standard error unless otherwise
noted.
Sex Determination
Sex determination was conduced by M. Be ´rube ´ at the Eco-
system Sciences Division of the University of California
Berkeley, according to previously described methods
(Be ´rube ´ and Palsbøll, 1996a,b). Briefly, cell lyses (from the
skin biopsy) was performed by the addition of sodium
dodecyllauryl sulfate, and proteinase K. DNA extraction
was made with phenol/chloroform/isoamyl alcohol mixture,
followed by a precipitation with ethanol. Oligonucleotide
primers ZFY and ZFX were used for amplification. Differ-
ences in the size amplified products (of both sexes) were
distinguished by gel electrophoresis (at 200 V) through 2%
NuSieveTM(cointaining 0.05 lg mL21ethildiumbromide).
RESULTS
Mean, standard error (SE) and range of concentrations for
SDDT, SPCB, SCHLORs, and SHCHs found in 12 female
and 9 male fin whales’ blubber biopsies are reported in Ta-
ble II. The mean concentration of SOCs found in this study
ranged from 360 to 2700 ng g21lw. The dominant pollutant
group was DDTs, followed by PCBs [ HCHs ? CHLORs
TABLE II. Concentration [mean 6 standard error SE] of SOCs, SDDTs, SPCBs, SHCHs, and SCHLORs measured in
blubber of fin whales from the Gulf of California, Mexico
n % Liplds
SHCHs
SCHLORs
SDDTs
SPCBs
SOCs
Females
(mean 6 SE)
12 56 6 4
36–80
ng g21ww
min–max
ng g21lw
min–max
ng g21ww
min–max
ng g21lw
min–max
13 6 6
\LOQa–62
23 6 11
\LOQa–92
15 6 7
\LOQa–61
25 6 5
\LOQa–77
6 6 3500 6 100
200–1200
950 6 200
300–2300
850 6 200
400–1900
1400 6 220
500–2400
70 6 15
15–190
130 6 25
40–270
120 6 30
40–240
200 6 30
120–290
610 6 130
170–1360
1100 6 230
360–2700
1000 6 240
300–2200
1700 6 270
500–2500
\LOQa–34
11 6 5
\LOQa–50
24 6 11
\LOQa–82
34 6 14
\LOQa–100
Males
(mean 6 SE)
9 60 6 6
34–83
a\LOQ 5 Less than the limit of quantification.
ng g21ww, ng g21wet weight; ng g21lw, ng g21lipid weight; min, minimum; max, maximum.
4
NIN˜O-TORRES ET AL.
Environmental Toxicology DOI 10.1002/tox

Page 5

(Fig. 2). Five OC pesticides (c-HCH, d-HCH, HCB, hepta-
chlor epoxide and methoxychlor) and four PCB congeners
(PCBs 114, 189, 198, 209) were\LOQ in all samples ana-
lyzed. Heptachlor and the PCB congeners 101, 156, 157,
and 170 1 190 were found in less than 15% of the analyzed
samples (Fig. 2). The mean SOCs in males (1700 ng g21
lw) was significantly greater than those in females (1100 ng
g21lw) (K-W h 5 3.9 P\0.046).
The mean concentration of total DDTs present in fin
whale blubber was 1200 6 150 ng g21lw, with concentra-
tions ranging from 300 ng g21lw (in a female) to 2400 ng
g21lw (in a male) (Table II). SDDTs contributed more
than 70% of the total OCs (Fig. 2). The most abundant
DDT metabolite was p,p0-DDE (representing ?60% of total
DDTs (Fig. 2), and more than 50% of the total OCs) fol-
lowed by o,p0-DDD[p,p0-DDD[o,p0-DDT[o,p0-DDE,
[p,p0-DDT. Male fin whales (1400 ng g21lw) had signifi-
cant higher DDTs values than females (950 ng g21lw) (K-
W h 5 4.2, P 5 0.039). The p,p0-DDE/SDDTs mean ratios
were 0.71 6 0.04 in females (ranging from 0.61 to 0.93);
and 0.63 6 0.03 in males (ranging from 0.54 to 0.78).
PCBs had the second highest concentration in fin whales
biopsies. The mean concentration in blubber samples was
160 6 20 ng g21lw, ranging from 40 (in a female) to 290
ng g21lw (in a male) (Table II). The congener with the
highest concentration was PCB 153, contributing more than
10% of the total OCs and more than 20% of SPCBs, fol-
lowed by PCB138 and PCB180 (Fig. 2). SPCBs concentra-
tions were higher in males (200 ng g21lw) than females
(130 ng g21lw) (K-W h 5 3.6, P 5 0.042).
SHCHs and SCHLORs were also measured in fin whales
biopsies, but their concentrations were considerably lower
than those of SDDTs and SPCBs. SHCHs for all fin whales
sampled ranged from\LOQ to 92 ng g21lw, with a mean
of 24 6 7 ng g21lw. a-HCH and b-HCH were the dominant
HCH isomers, present in 33% of the samples. SHCHs repre-
sented less than 3% of total OCs. SCHLORs ranged from\
LOQ to 100 ng g21lw, with a mean of 21 6 7 ng g21lw. c-
Chlordane and b-chlordane were the principal CHLOR
compounds, and were detected in 43% of the fin whale blub-
ber samples, however, these compounds represented less
than 3% of SOCs (Fig. 2). The mean SHCHs and
SCHLORs concentrations measured in male and female
blubber were not statistically different (SHCHs: K-W h 5
0.01, P 5 0.90; SCHLORs: K-W h 5 0.95, P 5 0.32).
DISCUSSION
This work contributes valuable data on OC concentrations
in an isolated population of fin whales that has not been
Fig. 2. Percent contribution (mean % 6 SE) of each compound analyzed to the total OCs
in fin whales (A) females, and (B) males. Dots represent the number of samples in which
each analyte was detected.
5
ORGANOCHLORINE PESTICIDES AND POLYCHLORINATED BIPHENYLS IN FIN WHALES
Environmental Toxicology DOI 10.1002/tox

Page 6

assessed in previous pollution studies. The results of our
study indicate that this population is generally clean com-
pared to other marine mammal species or other fin whale
populations in other regions. Although the resolution of our
analytical methods was not as sensitive as that of some pre-
vious studies that measured these compounds by high reso-
lution GC/MS, our detection limits were sufficiently low to
detect biologically relevant OC concentrations. The mean
concentrations of OCs found in fin whale blubber biopsies
in the present study are lower (2–70 times for PCBs; 2–90
times for DDTs; 7–50 times for CHLORs; and 5–17 times
for HCHs) than those reported in fin whales from the North-
western Atlantic during 1970s (Hobbs et al., 2001) and
1990s (Gauthier et al., 1997b; Hobbs et al., 2001); and from
the Mediterranean Sea (Marsili and Focardi, 1996, 1997;
Marsili et al., 1998; Herna ´ndez et al., 2000) (Table III). The
lipid content (%) found in our fin whale blubber samples
were consistent with the findings of previous studies of fin
whales from other geographic regions (34 to 88% of lipid)
(Aguilar and Borrell, 1988, 1990; Hobbs et al., 2001). The
relatively low lipid values found in the present study
(ranging from 34 to 83%) could be due to multiple factors,
such as the animal’s age [it is known that marine mammal
blubber lipid content increases with age] (Struntz et al.,
2004), as well lactating and resting processes in females
(Aguilar and Borrell, 1990).
OCs in Marine Mammals from
the Gulf of California
Although many of the fin whale populations around the
world make long migrations, the Gulf of California popula-
tion is a permanent year-round resident of the Gulf, repre-
senting one of the most isolated populations of this species
(Vidal et al., 1993; Rice, 1998; Be ´rube ´ et al., 2002; Urba ´n-
Ramı ´rez et al., 2005). While pollutant sources such as
atmospheric and marine current transport from the U.S.
State of California to the Gulf of California can contribute
to the pollutant concentrations in the Gulf, many local stud-
ies have shown that the major sources of contamination in
this area are, and historically have been, the agriculture
activities in this region (Enrı ´quez-Andrade et al., 2005;
Garcı ´a-Herna ´ndez et al., 2001, 2006; Lluch-Cota et al.,
2007; Nin ˜o-Torres et al., 2009). Currently, the states sur-
rounding the Gulf of California, especially Sonora and
Sinaloa, are considered a principal Mexican agricultural
zone supporting more than 40% of the national production
(Enrı ´quez-Andrade et al., 2005). Therefore, it is likely that
the OCs found in fin whales in this study were derived pri-
marily from the contamination produced in the Mexican
territory rather than as a result of long-range transport.
Historically the Gulf of California has exhibited lower
concentrations of OCs, compared with other marine regions
(e.g., west coast of USA, Mediterranean Sea). Concentra-
tions of OCs in marine mammals from the Gulf of Califor-
nia have been reported in blue whales (Balaenoptera mus-
culus), California sea lions (Zalophus californianus), and
vaquita (Phocoena sinus). In these species, the OC profiles
were made up of DDT [ PCBs [ HCHs, similar to the
tendency we observed in fin whales. Concentrations of
DDTs in fin whales were intermediate between those
reported in blue whales [ranging from 100 to 500 ng g21
lw; (Valdez-Marquez et al., 2004)], California sea lions
[ranging from 500 to 7700 ng g21lw; (Nin ˜o-Torres et al.,
2009)] and vaquita [from 530 to 9100 ng g21lw; (Calam-
bokidis, 1988)]. SPCBs in fin whales in our study were
similar to the mean concentrations reported in blue whales
[?140 ng g21lw; (Valdez-Marquez et al., 2004)], and
vaquita [from \ LOQ to 200 ng g21lw; (Calambokidis,
1988)] but lower than the concentrations observed in Cali-
fornia sea lions (420 to 2800 ng g21lw; (Nin ˜o-Torres et al.,
2009). HCHs concentrations in fin whales were similar to
those reported in blue whales and California sea lions from
the Gulf of California (ranging from\LOQ to 200 ng g21
lw). The differences in OC concentrations between species
TABLE 3. Concentrations (mean and range, ng g21lipid weight) of DDTs, PCBs, HCHs, and CHLORs in some
published studies on Balaenoptera physalus
Location DDTsPCBs HCHsCHLORs Author
Northwestern Atlanticmean
range
mean
range
mean
range
mean
range
mean
range
3800 2700210 570 Gauthier et al., 1997
650–13,086
26,900
3400–37,700
5700A
4200–9500A
1770A
459–9900A
1200
300–2400
230–10,200
10,900
3340–21,100
6500A
5500–7100A
5000A
4200–9500A
160
40–290
160–370
165
120–420
NA
NA
NA
NA
24
\LOQa- 92
170–1020
1500
970–2600
NA
NA
NA
NA
21
\LOQa- 100
Northwestern Atlantic Hobss et al., 2001
Mediterranean Sea
Marsili and Focardi, 1997
Mediterranean Sea
Marsili et al., 1998
Gulf of California Present study
NA, Data not available.
Ang g21dry weight;\LOQa, Less than the limit of quantification.
6
NIN˜O-TORRES ET AL.
Environmental Toxicology DOI 10.1002/tox

Page 7

could be influenced by the differences between metabolic
capacities, feeding ecology, and the distribution pattern of
the species. For example, fin whales from the Gulf of Cali-
fornia feed on both zooplankton and fish (Guerrero-Ruiz
et al., 2006), whereas blue whales feed predominantly on
euphausids (Gendron and Sears, 1993), and California sea
lions prey especially on fish (Aurioles-Gamboa et al., 2003;
Mellink and Romero-Saavedra, 2005).
Pesticides
Concentrations of DDT in the Gulf of California can still
be found (especially as DDE isomer) as vestiges of their
past use. In Mexico during 1970s, the use of technical DDT
as a pesticide was banned (Garcı ´a-Herna ´ndez et al., 2001,
2006) and its production was practically eliminated
(Castro-Dı ´az and Dı ´az-Arias, 2004). However, today DDT
is still used by the Mexican health authorities in the fight
against of the principal vector (mosquito Anopheles spp.) in
malaria transmission (Castro-Dı ´az and Dı ´az-Arias, 2004).
DDTs are commonly found as the principal pollutant class
in samples from the Gulf of California. The DDT metabo-
lite, p,p0-DDE, has been observed as the main OC pesticide
present in sediments (Garcı ´a-Herna ´ndez et al., 2001), mus-
sels (Gutierrez-Galindo and Mun ˜oz, 1992), birds (Jime ´nez
et al., 2005; Garcı ´a-Herna ´ndez et al., 2006), and California
sea lions (Nin ˜o-Torres et al., 2009) from the Gulf of Cali-
fornia. Because p,p0-DDE is the main degradation product
of DDT, the p,p0-DDE/SDDTs ratio is indicative of the
time since the technical DDT was released into the environ-
ment (Aguilar, 1984; Aguilar and Borrell, 1988; Borrell
et al., 1995). The p,p0-DDE/SDDTs ratios found in fin
whales in the present study (ratio 5 0.70) suggest that
recent inputs of technical DDT into the Gulf of California
has been low, and is consistent with the findings reported in
blue whales (ratio 5 0.87) (Valdez-Marquez et al., 2004),
and California sea lions (ratios between 0.88 and 0.96)
(Nin ˜o-Torres et al., 2009) from the same area.
The concentrations of HCHs in the present study are
consistent with previous data from the Gulf of California in
which a and b-HCH isomers dominated the HCHs profiles
in California sea lions (Nin ˜o-Torres et al., 2009), blue
whales (Valdez-Marquez et al., 2004; Robledo-Marenco
et al., 2006) and shrimp (Robledo-Marenco et al., 2006). In
other marine regions, such as the North Pacific and Califor-
nia, the b-HCH has been the dominant HCH isomer found
in whales, dolphins (Prudente et al., 1997) and sea lions
(Del Toro et al., 2006), whereas in the northwestern Atlan-
tic, a-HCH was the dominant isomer in Balenopterid spe-
cies (Gauthier et al., 1997a).
The major components of technical grade chlordane and
those that are usually found in the environment are a-chlor-
dane and c-chlordane (EPA, 1997). This agrees with our
findings in which c-chlordane was the predominant
CHLORs isomer. Similar CHLORs profiles have been
reported in California sea lions from the Pacific coast of
Baja California, the U.S. State of California (Del Toro
et al., 2006), and the Gulf of California (Nin ˜o-Torres et al.,
2009).
Polychlorinated Biphenyls
The predominant PCBs congeners found in the present
study were those with di-ortho Cl substitution, such as, the
PCBs 153, 138, and 180. These same congeners were also
reported as dominant in the PCBs profile in other species
from the Gulf of California, such as, California sea lions
(Nin ˜o-Torres et al., 2009) and birds (Jime ´nez et al., 2005).
Similarly, those compounds were dominant in California
sea lions from the Pacific coast of Baja California (Del
Toro et al., 2006), and killer whales from the North Pacific
(Ross et al., 2000). It has been hypothesized that presence
of di-ortho Cl substituted PCB congeners in balaenopterids
and other marine mammals are associated with an inability
to metabolize ortho-meta unsubstituted congeners with
more than one chlorine atom in the ortho position (Gauthier
et al., 1997a).
Males and Females
Our findings of differences in the concentrations of total
OCs, DDTs and PCBs between sexes agree with previous
studies on cetaceans in which adult males generally have
higher concentrations of pollutants compared with adult
females (Aguilar and Borrell, 1994; Ross et al., 2000). This
difference is attributable to that the capacity of females to
depurate lipophilic contaminants from their tissues through
the transfer from mother to calf during gestational and lac-
tational processes (Aguilar and Borrell, 1994; Krahn et al.,
1994). On the other hand, males only have the capacity to
eliminate these substances through metabolic processes,
and tend to increase their pollutant load with age, reaching
a plateau in tissue concentrations in fully grown animals
(Aguilar and Borrell, 1994). The lack of differences found
in the concentrations of SHCHs and SCHLORs between
males and females in this study could be due to the low
concentrations present in both contaminant classes because
pollutant mobilization is directly influenced by the OC
loads in the animal tissue (Aguilar and Borrell, 1994).
Despite the fact that SDDT concentrations were higher
in males than females in the fin whales we studied, the p,p0-
DDE/SDDTs ratios were similar between the sexes. It is
possible that differences existed but were not detected due
to the small sample size and large variation. Aguilar and
Borrell (1988) observed similar ratios between sexes in
‘‘young’’ mature North Atlantic fin whales, but not in older
animals. Because the age of the whales biopsied in our
7
ORGANOCHLORINE PESTICIDES AND POLYCHLORINATED BIPHENYLS IN FIN WHALES
Environmental Toxicology DOI 10.1002/tox

Page 8

study is unknown, we are unable to make a similar compar-
ison. This remains an area for further study.
Toxicological Effects
Previous studies of marine mammals have described OCs
compounds as having endocrine disruptor (Marsili et al.,
1998) and immuno suppressor effects (Kannan et al.,
2000). These endocrine disrupting chemicals cause effects
by mimicking sexual hormones (Fossi et al., 1992; Ankley
et al., 1998; Fossi et al., 2007). Studies describing hormonal
disorders in marine mammals caused by OC exposure have
focused principally on odontocetii, and pinnipeds because
they accumulate high amounts of OC in their tissues (Fossi
et al., 1999; Spinsanti et al., 2006; Hickie et al., 2007). Evi-
dence of contaminant induced endocrine disruption in mys-
ticetii species is relatively limited, however, these chemi-
cals have been associated with transformation of epididy-
mal and testicular tissue in North Pacific minke whales (B.
acutorostrata) (Fujise et al., 1998; Fossi et al., 2003), pseu-
dohermaphroditism in bowhead whales (Balaena mystice-
tus) from Alaska [440 ng g21lw (n 5 71) of SDDT]
(Tarpley et al., 1995; Hoekstra et al., 2002) and fin whales
from the Mediterranean Sea [mean SDDT 5 5000 ng g21
lw (n 5 27)] (Fossi et al., 2003).
Overall, the levels of OCs detected in the Gulf of Cali-
fornia fin whale population from our study were very low,
and are among the lowest reported for any marine mammal
worldwide, even among other fin whale populations. Ba-
leen whales commonly exhibit contaminant levels that are
an order of magnitude below those of pinnipeds (seals and
sea lions) and odontocetes (toothed whales) (Reijnders,
1986; Schwacke et al., 2002; Fossi et al., 2003) because
mysticetes are mid -trophic level organisms feeding on
crustaceans and small pelagic fishes. The findings from our
study support the generally held concept that concerns for
the health effects of POPs are more relevant for odontocetes
and pinnipeds than mysticetes. However, the effects of ex-
posure to OC insecticides and PCBs on endocrine function
and reproduction in baleen whales have been documented
and indicate that OC compounds can interfere with the
reproduction of mysticetes (Tarpley et al., 1995; Hoekstra
et al., 2002; Fossi et al., 2003). DDTs and PCBs among
others OCs have the potential for both estrogenic- antian-
drogenic and antiestrogenic-androgenic properties in fin
whales (Marsili et al., 1998; Fossi et al., 2003).
Considering that maximum OCs values found in the
present study (2700 ng g21lw) were higher than those
found in baleen whales characterized with endocrine disor-
ders (1400 ng g21lw) (Tarpley et al., 1995; Hoekstra et al.,
2002), the potential for these chemicals to present a health
effect in the individuals with the highest concentrations
should not be dismissed. Because of the low calf production
[females give birth to a single calf every 2 years] (Aguilar,
2001), the grade of isolation (Be ´rube ´ et al., 1998, 2002),
and the small population size (600 animals) of the Gulf of
California fin whales (Urba ´n-Ramı ´rez et al., 2005; Dı ´az-
Guzma ´n, 2006), even slight impairment of reproduction
effectiveness in a small number of individuals could affect
the status this population (Be ´rube ´ et al., 1998, 2002; Urba ´n-
Ramı ´rez et al., 2005). Future research on this topic will be
necessary to understand the role that these compounds may
have on the health of these population.
In conclusion, concentrations of OC pesticides and poly-
chlorinated biphenyls found in living fin whales from the
Gulf of California were lower than those in fin whales from
other regions (such as the North Atlantic and Mediterranean
Sea). However, the maximum values observed (2700 ng
g21lw) in some individuals, were two times higher than
those reported to be associated with reproductive problems
in bow head whales (Tarpley et al., 1995; Hoekstra et al.,
2002), suggesting that the potential for these chemicals to
present health effects deserve consideration. Health effects
in a small number of individuals could have population-
level effects given the small population size and highly iso-
lated characteristics of Gulf of California fin whales. Effects
of OCs on baleen whales are largely unknown and warrant
further study, in addition to research in other fields includ-
ing social structure, ecology and identifying other possible
threats which will contribute valuable information for the
development of conservation plans for this population.
The authors thank UNAM that provided a fellowship to CANT
to conduct this study as part of his PhD dissertation. They thank
the people from the Marine Mammal Laboratory (UABCS) for
their help collecting samples, and to the people at the Ecology and
Toxicology Laboratory (CIBNOR) for their help during process-
ing of the samples. The authors appreciate M. Be ´rube ´ by her valu-
able collaboration in the sample sex determination. They also
deeply appreciate the collaboration of the NWFSC Environmental
Conservation Division for providing training to CANT on the OC
analysis and their input into the project. All the sampling activities
were conducted in compliance with Mexican laws and regulations,
SEMARNAT permit No SGPA/DGVS/00668/07.
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Environmental Toxicology DOI 10.1002/tox