TISSUE-SPECIFIC DISTRIBUTION AND WHOLE-BODY BURDEN ESTIMATES OF PERSISTENT
ORGANIC POLLUTANTS IN THE BOTTLENOSE DOLPHIN (TURSIOPS TRUNCATUS)
JENNIFER E. YORDY,*yz D. ANN PABST,§ WILLIAM A. MCLELLAN,§ RANDALL S. WELLS,k
TERI K. ROWLES,# and JOHN R. KUCKLICKz
yMarine Biomedicine and Environmental Sciences Center, Medical University of South Carolina, 221 Fort Johnson Rd., Charleston,
South Carolina 29412, USA
zNational Institute of Standards and Technology, Hollings Marine Laboratory, Charleston, South Carolina 29412, USA
§Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, North Carolina 28403, USA
kChicago Zoological Society c/o Mote Marine Laboratory, Sarasota, Florida 34236, USA
#Office of Protected Resources, National Marine Fisheries Service, Silver Spring, Maryland 20910, USA
(Submitted 19 October 2009; Returned for Revision 30 November 2009; Accepted 17 January 2010)
Abstract—Most exposure assessments for free-ranging cetaceans focus on contaminant concentrations measured in blubber, and few
data are available for other tissues or the factors governing contaminant distribution among tissues. The goal of this study was to provide
a detailed description of the distribution of persistent organic pollutants (POPs) within the common bottlenose dolphin (Tursiops
truncatus) bodyand assess therole oflipiddynamics inmediating contaminant distribution. Thirteen tissues (brain, blubber, heart,liver,
lung, kidney, mammary gland, melon, skeletal muscle, spleen, thyroid, thymus, and testis/uterus) were sampled during necropsy from
bottlenose dolphins (n¼4) and analyzed for lipid and 85 POPs, including polychlorinated biphenyls, organochlorine pesticides, and
polybrominated diphenyl ethers. Significant correlations between tissue POP concentrations and lipid suggest that distribution of POPs
is generally related to tissue lipid content. However, blubber:tissue partition coefficients ranged widely from 0.753 to 6.25, suggesting
that contaminant distribution is not entirely lipid-dependent. Tissue-specific and whole-body contaminant burdens confirmed that
blubber, theprimary siteof metaboliclipid storage, isalso the primarysite for POP accumulation, contributing >90% tothe whole-body
burdens. Observations also suggest that as lipid mobilizes from blubber, contaminants may redistribute, leading to elevated tissue
concentrations. These results suggest that individuals with reduced blubber lipid may be at increased risk for exposure-related health
effects. However, this study also provides evidence that the melon, a metabolically inert lipid-rich structure, may serve as an alternate
depot for POPs, thus preventing the bulk of blubber contaminants from being directly available to other tissues. This unique
physiological adaptation should be taken into consideration when assessing contaminant-related health effects in wild cetacean
populations. Environ. Toxicol. Chem.# 2010 SETAC
Keywords—Persistent organic pollutantsTissue distributionBody burden Bottlenose dolphin
Odontocetes (toothed whales, dolphins, and porpoises) are
fore are predisposed to the accumulation of lipophilic and
bioaccumulative contaminants, such as persistent organic pol-
lutants (POPs) . Legacy POPs, including polychlorinated
biphenyls (PCBs) and organochlorine pesticides, as well as
compounds of emerging concern, such as polybrominated
diphenyl ethers (PBDEs), have been associated with effects
on marine mammal reproduction and immune function [2–4],
reduced offspring survivorship [5–7], and depressed population
growth rates , and therefore remain a significant concern for
odontocete health and population sustainability. Studies on
cetaceans, however, are few, because they are federally pro-
tected within U.S. waters and the direct collection of tissues for
assessment of POP exposure in free-ranging populations is
logistically difficult. The collection of tissues to assess con-
taminant exposure is limited to those that can be sampled
nonlethally. Because blubber can be collected nonlethally via
surgical biopsies, or from a distance using projectile darts, most
biomonitoring efforts rely on blubber to assess contaminant
exposure in wild cetacean populations .
Blubber is a lipid-rich hypodermis, unique to marine mam-
mals, that consists primarily of adipocytes interwoven by
structural collagen and elastin fibers [9,10]. As a modified form
energy storage in cetaceans and also functions in streamlining,
thermoregulation, locomotion, protection from predation, and
buoyancy control . Because of its high lipid content and
primary site of accumulation for lipophilic contaminants, con-
tributing >90% to the whole-body contaminant burden in
cetacean species . Blubber composition is dynamic, with
lipid deposition occurring when dietary intake exceeds ener-
getic needs, and mobilization of lipid from blubber occurring
when energy is needed to meet the demands associated with
thermoregulation, reproduction, lactation, disease, or starva-
tion. For example, female fin whale (Balaenoptera physalus)
blubber thickens 25 to 45% during pregnancy and is subse-
quently depleted as lipids are used during lactation .
Environmental Toxicology and Chemistry
# 2010 SETAC
Printed in the USA
All Supplemental Data may be found in the online version of this article.
* To whom correspondence may be addressed
Published online 19 February 2010 in Wiley InterScience
Furthermore, both blubber thickness and volume are reduced in
starved harbor porpoises (Phocoena phocoena) in comparison
with porpoises in robust body condition . Given the multi-
functional nature of blubber, it is not surprising that variations
in blubber thickness, lipid content, as well as adipocyte size and
number occur in accordance with ontogeny, reproductive state,
and with seasonal and regional differences in water temperature
In addition to blubber, cetaceans possess a unique lipid-rich
structure that serves as another site for the accumulation of
lipophilic contaminants; the melon is a specialized fatty
structure within the cetacean forehead that functions in the
transmission of echolocation signals [21–24]. The melon
cannot be sampled nonlethally and therefore is not routinely
collected for contaminant analysis. However, in several instan-
ces POPs have been measured in the melon at high concen-
trations similar to those detected in blubber, suggesting this
tissue may serve as another depot for contaminant accumu-
lation [25–27]. Although both blubber and the melon consist
predominantly of neutral lipids such as triacylglycerols, the
fatty acid composition of the melon is unique, consisting of
short- and medium-chain (C5–C12), branched, saturated fatty
acids specialized for sound transmission [21,24,28]. A major
constituent of melon fatty acids, isovaleric acid, has been
associated with toxic effects—vomiting, convulsions, coma,
death—when introduced into circulation of other mammalian
species [29,30]. Thus, it is probable that melon lipids are
synthesized in situ and are not mobilized into circulation in
response to energetic demands, as are blubber lipids [21,31].
For example, whereas blubber thickness and volume are
reduced in starved harbor porpoises, the lipid content and
lipid composition of melons from starved individuals are no
different from those of robust individuals, suggesting the
melon is not used as a metabolic energy depot [15,31]. The
conservative nature of this fat depot is consistent with its
crucial function for sound transmission.
Persistent organic pollutants strongly associate with lipid.
Therefore, it is likely that changes in the volume and distribu-
tion of lipids affect the movement of contaminants throughout
the cetacean body, with lipid-rich tissues, such as blubber and
melon, playing integral roles in contaminant storage and bio-
melon, as mobile and nonmobile lipid stores, respectively, may
influence their relative importance as sinks or sources of con-
taminants within the body. However, to date little is known
regarding the toxicokinetics of POPs in cetaceans. Data from
other marine mammal species, such as the harbor seal (Phoca
vitulina), support a kinetic model whereby blood acts as a
between POPs from external inputs, such as diet, and those
stored in tissues . In the case of lipophilic contaminants,
lipid movement between body compartments is assumed to
facilitate the distribution of contaminants among blood and
tissues. As previously observed in bottlenose dolphins, the
proportion of contaminants within blood may increase with
decreasing blubber lipid content, indicating that as blubber lipid
is used, POPs redistribute into blood . It may therefore be
anticipated that changes in blubber lipid also affect POP con-
centrations in other organs that are the direct targets of POP-
mediated toxicity. It is currently unknown whether the burden
of contaminants contained within melon is also subject to
mobilization or remains sequestered because melon lipids do
not appear to be used during periods of metabolic stress. An
understanding of the role of this unique cetacean adaptation is
important for deriving species-specific toxicokinetic models
and risk assessments.
taminants in cetaceans clearly has important implications for
biomonitoring and animal health. Knowledge regarding the
relationship of blubber concentrations to those in other
tissues and to whole-body burdens is needed for accurate
exposure assessments. The redistribution of POPs from lipid
stores into blood and other organs may increase contaminant
bioavailability and thus the risk of exposure-related health
effects. A redistribution of contaminants may also affect blub-
ber contaminant levels and thus its relevance for estimating
exposure in wild populations. Therefore, a better understanding
of the relationship between lipid dynamics and tissue distribu-
tion is needed to accurately assess exposure and risks to
The goal of this study was to describe the distribution of
POPs in tissues of a well-studied odontocete, the common
bottlenose dolphin (Tursiops truncatus). Our objectives were
to determine whether POPs distributed among tissues non-
contribution of individual tissues to whole-body contaminant
burden. To our knowledge, whole-body contaminant burdens
for cetaceans have been described in detail in only one other
study, in which tissues were collected from just one animal, a
pelagic striped dolphin (Stenella coeruleoalba) . Thus, the
expansion of this dataset to include multiple animals of a single
dolphin species will allow us to assess the relevance of blubber
concentration data to whole-body burden, an important con-
sideration for risk assessments. Furthermore, the inclusion of
animals with varying blubber lipid content and body condition
should provide insights into the influence of lipid dynamics on
the toxicokinetics of POPs in cetaceans.
MATERIALS AND METHODS
Blubber and other tissue samples were collected from four
bottlenose dolphins that had been stranded or had been
incidentally killed in North Carolina, Virginia, or Florida,
USA (Table 1). Contaminant concentrations in stranded ceta-
ceans may change with tissue decomposition in the time
following death ; therefore, individuals in this study were
sampled only when the time of death could be determined and
tissues collected within 12h postmortem. Two adult female
dolphins, WAM 559 and WAM 631, exhibited evidence of
cardiac pathologies: dolphin WAM 559 presented with con-
siderable heart valve problems, while WAM 631 died of a
cardiac infarct and was found with multiple system lesions.
The mammary glands of WAM 559 did not appear active,
whereas milk was present in the mammary glands of WAM
631. An immature male, VMSM20001049, was incidentally
killed and was found to have no other concurrent health
issues. An adult male, FB 192, was in poor body condition
and presented with evidence of infection, severe emaciation,
and reduced pulmonary function.
Environ. Toxicol. Chem. 29, 2010 J.E. Yordy et al.
Dolphins WAM 559 and VMSM20001049 exhibited a
convex epaxial muscle profile and lack of a depression caudal
to the blowhole, indicating they were robust in body condition.
Dolphins FB 192 and WAM 631 were characterized as thin
animals based on evidence of reduced blubber stores (ribs
evident from external examination). In addition, FB192’s blub-
ber thickness at a standard diagnostic location below the dorsal
fin was only 10mm, 62.5% of what had been measured for this
same animal during a health assessment in June 1999 and well
below the 18-mm average for Sarasota Bay, Florida, dolphins in
Whole carcasses were weighed to the nearest kilogram to
obtain total mass and were subsequently necropsied according
to a mass dissection protocol previously described for harbor
porpoises . Briefly, blubber, muscle, and whole organs
were systematically dissected from each carcass and weights
recorded to the nearest gram prior to sampling for histopa-
thology and contaminant analysis. Blubber was flensed from
the length of body bridging the nuchal crest of the skull and
the insertion of flukes with care taken not to remove under-
lying subdermal connective tissue and muscle. Appendages,
including the dorsal fin, pectoral flippers, and flukes, were not
included in the blubber mass measurement. A subsample of
blubber from a dorsal, midthoracic site was retained for
contaminant analysis. Skeletal muscles, including the pectoral,
ventral cervical, axial, thoracic, and abdominal muscles, were
dissected from skeletal elements and weighed individually. All
other organs were dissected cleanly from the carcass and
weighed whole. In total, 13 tissues were sampled from each
animal for analysis: brain (cerebrum), heart, liver, lung,
kidney, melon, skeletal muscle, spleen, thyroid, thymus, blub-
ber, testis from male dolphins, and uterus and mammary gland
tissue from females. Tissues were chosen for analysis because
of a substantial contribution to total body mass and/or for their
likelihood of contaminant accumulation or potential as a target
for toxicity. Bone and appendages, although contributing
significantly to overall body mass, were not included in this
study, because Tanabe et al.  concluded that bone did not
contribute significantly to the overall contaminant body bur-
den. Melon was not included in the calculation of whole-body
burden because the mass for this structure was not specifically
determined. Subsamples of each tissue designated for con-
taminant analysis were wrapped in solvent-rinsed aluminum
foil or placed in Teflon jars/bags and stored at ?808C until
Extraction and cleanup
Tissue samples were extracted as described previously for
blubber.Briefly,asubsample ofeach tissue (1.0–5.0g)was
weighed and minced using solvent-rinsed instruments. Samples
were mixed with sodium sulfate and transferred to pressurized
fluid extraction (PFE) cells, at which point an internal standard
solution containing 28 isotopically labeled compounds was
added. Samples were extracted with dichloromethane using
PFE. Tissue extracts contained residual water (?0.5ml), which
was removed by pipette. Extracts were then reduced in volume
under a stream of purified nitrogen and centrifuged at 2750
RPM for 5min to sediment out insoluble material. Additional
Table 1. Persistent organic pollutant (POP) concentrations (mg/g wet mass) and lipid (%) in tissues of four bottlenose dolphins
North Topsail Island, NC
Wrightsville Beach, NC
aPPCBs¼sum of 69 polychlorinated biphenyls,PPBDEs¼sum of 10 polybrominated diphenyl ethers,PDDTs¼sum of six dichlorodiphenyltrichloroethanes.
Tissue distribution and body burden of POPs in dolphins
Environ. Toxicol. Chem. 29, 20103
cleanup steps, including size exclusion chromatography and
solid phase extraction with 5% deactivated alumina, were used
to remove lipid and high molecular weight interferences from
the extracts. Prior to clean-up steps, lipid content was deter-
mined gravimetrically from 10% of the extract. Tissue lipid
content is expressed as the ratio of lipid to wet mass of the
Persistent organic pollutants were quantified using a gas
chromatograph-mass spectrometer (GC/MS; Agilent 6890/
5973) with electron impact ionization operated in the
selected ion monitoring mode. Compounds were separated
on a 60m?0.25mm i.d.?0.25mm film thickness DB-5ms
capillary column (Agilent Technologies). Analyte concentra-
tions were calculated from the slope and y intercept gen-
erated by at least a three-point calibration curve. The limit of
detection was defined as the greater of the mass of the
analyte in the lowest detectable calibration solution divided
by the sample mass or the mean analyte concentration plus
three times the standard deviation calculated in four blank
The concentrations of 85 compounds were determined: 69
PCB congeners (IUPAC numbers 18, 29, 28/31, 44, 49, 52, 56,
112, 128, 130, 137, 146, 149, 153/132, 151, 154, 156, 157, 163/
138/158, 165, 166, 167, 170,172, 174, 175, 176, 177, 178, 180/
193, 183, 185, 187, 188, 189, 194, 195, 196/203, 197, 199, 200,
201, 202, 205, 206, 207, 208, 209); 10 PBDE congeners (47, 49,
66, 71, 75, 99, 100, 153, 154, 155), and six DDTs (2,40and 4,40-
DDD, -DDT, -DDE).
Tissue samples were analyzed in batches of 15 to 25
samples. Each batch was extracted alongside a minimum of
three blanks and a five-point calibration curve ranging from
500 to 0.15ng of each analyte. The calibration curve was
extended up to 10mg for select analytes. Limits of detection
averaged 0.3ng/g wet mass for PCB congeners, 0.8ng/g wet
mass for PBDE congeners, and 0.8ng/g wet mass for the
Replicates of National Institute of Standards and Technol-
ogy (NIST) SRM 1945 Organics in Whale Blubber were
analyzed alongside samples as an analytical control material.
On average, the values obtained for each control material
differed from the certified values by 14.2%.
Statistics and calculations
Wet-mass normalized contaminant concentrations were
used in all calculations and statistics except for the calcu-
lation of tissue partition coefficients, which used lipid-nor-
malized POP concentrations. The relationship between tissue
PPCB concentrations and lipid content within each individ-
partition coefficients were calculated as the ratio of lipid-
normalized contaminant concentrations in blubber to that in
ual was assessed using linear regression. Blubber/tissue
blubber=tissue partition coefficient ¼
POPblubberðmg=g lipidÞ=POPtissueðmg=g lipidÞ:
Tissue contaminant burdens were calculated as the product
of the tissue mass and tissue POP concentration:
POP burdentissueðmgÞ ¼
masstissueðgÞ ? POPtissueðmg=g wet massÞ:
Whole-body contaminant burdens were calculated as the
sum of all tissue burdens within an animal:
The contribution of a tissue to total body mass is the ratio of
tissue mass to the whole-body mass recorded prior to necropsy:
The contribution of tissue POP burden to whole-body POP
burden is the ratio of tissue contaminant burden to whole-body
POP burdenbodyðmgÞ ¼
%body mass ¼ masstissueðgÞ=massbodyðgÞ
%POP body burden ¼
POP burdentissueðmgÞ=POP burdenbodyðmgÞ
RESULTS AND DISCUSSION
POP tissue distribution: relationship with lipid
Within individual dolphins, lipid content was highest in the
melon > blubber > mammary gland (in females) > brain > all
other tissues (Table 1). Although the lipid content of melon was
higher than that of blubber, the lipid content of melon did not
vary dramatically (mean and SD, 86.3?2.3%) among individ-
uals as it did for blubber, which ranged widely from 19.3 to
67.4% (Table 1). This observation is consistent with the gen-
erally accepted functional differences of lipids within these two
tissues. The short- and medium-chain saturated, branched fatty
acids of the melon are thought to be specialized for sound
transmission and are likely not used as an energetic source.
Koopman et al.  observed that the lipid content and lipid
composition of melons from starved harbor porpoises were no
different from those of robust individuals, suggesting melon
composition does not vary in accordance with body condition.
The authors proposed that the melon does not serve as an
energetic reserve because short-chain fatty acids are not sig-
nificant sources of metabolic energy and melon lipids are of
critical importance in maintaining acoustic function, and there-
fore should be preserved at all cost . Mobilization of melon
acid, a fatty acid that has proven toxic when introduced into the
blubber lipids typically consist of longer-chain, unsaturated,
straight fatty acids [36,37]. Blubber is considered to be the
primary site of metabolic energy storage within the body, but
also supports a number of other physiological functions (i.e.,
streamlining, thermoregulation, locomotion, buoyancy) for
cetaceans . Therefore, it is not surprising that variables
such as nutritional status, reproductive status, ontogeny, and
environmental temperature changes have been observed to
affect blubber composition (i.e., blubber depth, percent lipid
content, adipocyte number, adipocyte size, fatty acid compo-
sition) [15–20,38]. These variables likely contributed to the
Environ. Toxicol. Chem. 29, 2010J.E. Yordy et al.
variation in lipid content observed among individuals in the
Contaminant concentrations followed a similar tissue dis-
tribution pattern to that of lipid. Persistent organic pollutant
concentrations were higher in the melon, blubber, and mam-
and a significant positive relationship was detected between
tissue lipid content andPPCB (Fig. 1),PDDT, andPPBDE
ute among most tissues in accordance with lipid content. Brain
tissue, however, tended to deviate from this relationship, and
contained lower than expected POP concentrations (Fig. 1).
This finding has been observed previously [13,39–41] and may
be attributed to the unique lipid composition of brain matter or
the presence of the blood–brain barrier, a series of tightly joined
endothelial cells at the brain:circulatory interface that impede
the passage of polar solutes from blood into the brain. The lipid
profile of brain tissue is dominated by phospholipids, which are
more polar in comparison to the triacylglycerols composing
blubber and melon . Thus, it has been proposed that
distribution of nonpolar chemicals, such as POPs, is related
not only to lipid quantity, but also to the lipid composition of
marine mammal tissues [26,42,43]. It has also been suggested
that movement of POPs into the central nervous system may be
restricted by the blood–brain barrier [40,44].
concentrations (data not shown), suggesting that POPs distrib-
With the exception of brain tissue, the overall relationship
between tissue lipid content and contaminant concentrations
suggests that contaminants generally distribute throughout the
body in accordance with lipid. However, it should be noted that
the strength of this relationship is likely driven by the high
concentrations in the blubber and melon (Fig. 1), and therefore
may not necessarily hold true for tissues with lower lipid
Tissue-specific partition coefficients
Tissue partition coefficients were calculated for the major
contaminant classes (PPCBs,PPBDEs, andPDDTs) using
tition equally among lipid compartments of blubber and other
tissue, and also to provide a basis for estimating internal
contaminant concentrations from blubber (Table 2). Coeffi-
cients equal to 1 are indicative of an equal distribution between
blubber and the other tissue; coefficients >1 indicate a selective
accumulation in blubber over the other tissue. Contaminant
distribution is likely related to a number of overlapping factors,
including tissue-specific differences, physiochemical differen-
ces between compounds, as well as individual specific differ-
ences in life history and physiological state; therefore, anumber
of comparisons can be made from the data in Table 2.
lipid-normalized concentrations to examine whether POPs par-
Fig. 1. RelationshipoflipidandPPCB(polychlorinatedbiphenyl)concentrationswithintissuesofbottlenosedolphins.Squareindicatesareaofblown-upinset.
p<0.000005.(C) VMSM: r2¼0.990, p<0.000001. (D) FB 192: r2¼0.998, p<0.000001. For reference, dolphins WAM 559 and VMSM were in robust body
condition and WAM 631 and FB192 were considered thin.
Log-transformed data were used to evaluate significance and fit of linear regression. (A) WAM 631: r2¼0.989, p<0.000001. (B) WAM 559: r2¼0.944,
Tissue distribution and body burden of POPs in dolphins
Environ. Toxicol. Chem. 29, 20105
One obvious source of variation was the difference in the
tissue partition coefficients of male and female dolphins
(Table 2). Males tended to exhibit higher partition coefficients
females¼1.81), suggesting POPs concentrate to a greater
extent within the blubber of male dolphins. In contrast, the
low partition coefficients observed in females indicate POPs
are distributed more equally between blubber/blood and tissue.
Although the reason for this sex-related difference is not
specifically known for these individuals, given that both
females in the study were sexually mature this disparity
could be attributed to the mobilization of blubber lipid and
contaminants that occurs during lactation. Previous studies in
other physiological conditions where lipids are mobilized from
fat stores (i.e., starvation), blood contaminant concentrations
increase [33,45,46]. Therefore, it is possible that the movement
of contaminants from blubber to blood during lactation would
lower blubber contaminant concentrations and/or increase other
tissue concentrations, resulting in lower blubber/tissue partition
coefficients. However, if this phenomenon was specifically
related to mobilization of contaminants concurrent with lipid
use, FB192, a thin male, would have been expected to exhibit
lower tissue partition coefficients than VMSM20001049, a
robust male. Because this is not the case, it suggests that the
lower partition coefficients observed in females are likely more
related to the effects of reproduction and lactation rather than
simply mobilization from contaminant stores from blubber to
tissue. This generalization, however, cannot be confirmed with-
out tissue contaminant data from preparturient females.
Contaminant distribution also varied by tissue type. Overall,
the majority of blubber/tissue partition coefficients were greater
than 1, indicating that POPs are more concentrated in blubber
than in other tissues (Table 2). However, mean tissue partition
coefficients also varied widely between tissues, suggesting that
contaminant distribution is selective, tissue-specific, and not
entirely relatedtotissue lipidconcentrations (Table2).Partition
coefficients were highest for brain tissue, reflecting the pre-
viously noted impedance to POP transfer or accumulation in
this organ. Among other tissues, partition coefficients ranged
widely from 0.753 to 6.25, suggesting contaminants concen-
For example, in male dolphins mean blubber/tissue partition
coefficients for heart, kidney, liver, lung, muscle, spleen, and
testis ranged from 2.12 to 6.25, indicating contaminant con-
centrations (lipid wt) in blubber exceeded those in tissues by a
factor of 2 to 6. In comparison, mean partition coefficients
forthemelon, thymus,andthyroid werecloser to1 (range 1.03–
1.57), indicating contaminants distributed approximately
equally between the lipid compartments of blubber and these
The reason for differential partitioning is unclear but could
be attributed to variations in tissue lipid composition. In the
striped dolphin, Kawai et al.  observed that POP levels were
highest in tissues with a high proportion of triacylglycerols,
whereas tissues dominated by phospholipids and cholesterol
exhibited lower POP concentrations. Furthermore, Guitart et al.
 detected correlations between contaminant concentrations
and fatty acid composition of striped dolphin tissues. Tissue
lipid composition, in addition to lipid content, may therefore
play a role in determining the level of tissue-specific contam-
It is not surprising that tissue distribution also appeared to
vary among the three compound classes given their distinct
differences in physiochemical properties such as size and lipid
solubility (molecular weight and log octanol water coefficients
(log KOW), in order of rank, PCBs3–6chlorines?DDTs<
PCBs7–10chlorines?PBDEs). Tissue-partition coefficients were
generally lowest for PCBs < DDTs < PBDEs (Table 2),
indicating that the DDTs and PBDEs have a greater propensity
Table 2. Blubber/tissue partition coefficients for persistent organic pollutants (POPs) in male and female bottlenose dolphins
Blubber/tissue partition coefficientsa
VMSM192 VMSM192 VMSM192Male 559631559 631 559 631Female
aPartition coefficients¼POPblubber(mg/g lipid)/POPtissue(mg/g lipid).PPCBs is sum of 69 polychlorinated biphenyls,PPBDEs is sum of 10 polybrominated
bFor brevity, animal IDs are abbreviated as follows: VMSM20001049 (VMSM), FB 192 (192), WAM 559 (559), WAM 631 (631).
diphenyl ethers,PDDTs is sum of six dichlorodiphenyltrichloroethanes.
Environ. Toxicol. Chem. 29, 2010J.E. Yordy et al.
to accumulate in blubber, or a lesser ability to accumulate in
other tissues, as compared to PCBs.
Lipid solubility (log KOW) increases in relation to molecular
weight for most of the measured compounds; therefore, it is
difficult to attribute these class-specific differences in partition-
ing solely to one of these two physiochemical properties. Size
has been proposed to hinder the diffusion of large compounds
(i.e., higher-brominated PBDEs) across biological membranes
; therefore, it remains possible that size may influence the
isalso verylikelythatcompoundlipidsolubility,at leastin part,
mediates the distribution of contaminants between blubber and
tissue. It was previously observed that blubber of pilot whales
contained greater proportions of the most lipophilic PCB con-
dominated by the least lipophilic congeners (log KOW<6.5)
. Our observations generally agree with this pattern of
distribution, in that the largest and most lipophilic compounds
(DDTs and PBDEs) have higher blubber tissue partition coef-
ficients, indicating their selective accumulation in blubber
relative to other tissues. It is surprising, however, that the
partition coefficients of PCBs were low, despite the larger size
and high log KOWvalues of the highly chlorinated PCBs7–
10chlorines.Additional examination of the data indicated that the
lower-chlorinated PCBs3–6chlorineswere more prevalent in each
animal (50–80% ofPPCB concentrations). As a result, the
reflect the tissue partitioning properties of the smallest and least
lipophilic congeners (PCBs3–6chlorines). This observation could
therefore explain the lower than expected partition coefficients
contaminant classes, congener-specific differences in tissue
partitioning were also examined. Tissue contaminant profiles
and partition-coefficients for the major PCB, PBDE, and DDT
tissue partition coefficients calculated forPPCBs most likely
In light of the differences observed among the three major
congeners are given in the Supplemental Data. In contrast to the
differences observed between the three contaminant classes,
congener-specific differences in partitioning were generally not
consistent across individuals or tissues. Such variation is likely
to be expected, given that the four individual animals are of
varying age, sex, body condition, reproductive status, and
quality of health. Thus, more detailed conclusions could not
be reached with this limited sample size.
The large size and protected status of cetaceans makes the
determination of whole-body contaminant burdens impractical;
consequently, the majority of assessments rely on the collection
of blubber samples for information regarding contaminant
exposure in wild populations . Blubber contaminant concen-
trations, however, can vary throughout time, because contam-
inants may be diluted by increases in body mass , or may be
redistributed to other tissues as blubber lipid is used .
Therefore, contaminant concentrations in this tissue may not
be the most accurate indicator of individual exposure levels and
age-related accumulation patterns. By accounting for the mass
and contaminant concentrations of all tissues, the estimation of
whole-body burdens circumvents these uncertainties and may
lend insight into the relevance of blubber concentrations to
whole-body contaminant exposure.
Tissue-specific and whole-body contaminant burdens for the
four dolphins are presented in Table 3 and the percent con-
tribution of each tissue to whole-body contaminant burden for
each individual is displayed in Table 4. For all individuals,
skeletal muscle and blubber were the largest contributors to
total body mass, with muscle contributing more to overall mass
(26.9–41.9%) than blubber (11.5–24.2%) (Table 4). Despite its
lower contributionto total bodymass, blubber contained 92.5 to
98.1% of the contaminant body burden for each animal; com-
paratively, skeletal muscle contributed only 0.69 to 5.2% to
Table 3. Tissue-specific and whole-body masses and persistent organic pollutant (POP) burdens in four bottlenose dolphinsa
ID WAM 631 WAM 559 VMSM20001049FB 192
Mass (g) Burden (mg)b
Mass (g) Burden (mg)b
Mass (g) burden (mg)b
mass (g) burden (mg)b
SPCB SPBDE SDDT Tissue
aMelon omitted from analyses because mass not taken.
bTissue POP burden¼tissue mass (g)?tissue POP concentration (mg/g wet mass).PPCBs¼sum of 69 polychlorinated biphenyls,PPBDEs¼sum of 10 polybrominated diphenyl
eSkeletal muscle mass includes pectoral, epaxial, rectus abdominal, hypaxial, scalene, sternomastoid, sternohyoid and sternothyroid muscles.
fTotal is sum of all measured tissues.
ethers,PDDTs¼sum of six dichlorodiphenyltrichloroethanes.
Tissue distribution and body burden of POPs in dolphins
Environ. Toxicol. Chem. 29, 20107
whole-body contaminant burden (Table 4). These results are in
good agreement with values reported by Tanabe et al.  for
the contribution of blubber (95%) and muscle (4.5%) to the
PPCB body burden of a striped dolphin. Compared with
body mass (<10%) and contaminant body burden (0.31–4.2%)
The large burden of contaminants contained in the blubber is
a consequence of its high lipid content and substantial contri-
bution to total body mass. Because blubber mass changes with
growth [12,16], body burden provides a different measure
of exposure than tissue concentrations. This effect is most
apparent in the comparison of two animals, WAM 559 and
VMSM20001049, which exhibited similar blubber PCB con-
centrations (?30mg/g; Table 1) but dramatically different
PCB body burdens (2,000mg and 675mg, respectively;
Table 3) at least in part because the blubber mass of WAM
599 was twice as high. By accounting for the accumulation of
POPs with growth (i.e., increases in body mass), body burden
may provide a more accurate and meaningful measure of
exposure than tissue concentrations and, therefore, should be
taken into consideration for future risk assessments evaluating
Blubber appears to hold consistently >90% of the whole-
body contaminant burden; thus, it is reasonable to conclude that
blubber concentrations may be useful for estimating body
burden in cetaceans, provided that information regarding
total body and blubber mass is known. In cases of stranded
individuals or animals sampled during capture and release
health assessments, mass data can be readily collected; how-
ever, for free-ranging cetaceans, and especially large whales,
this information is difficult to collect. Because body length
may be the easiest parameter to estimate for free-swimming
cetaceans, morphological data relating length and body mass
and blubber and body mass in cetaceans would provide a useful
resource for estimating body burden in wild populations.
blubber and muscle, other tissues contributed much less to total
Blubber and melon lipids and POP distribution
Two of the dolphins in the present study, WAM 631 and
FB192, were characterized as thin animals during necropsy
and additionally exhibited low blubber lipid content and low
blubber mass (relative to whole body) in comparison with
the other dolphins, WAM 559 and VMSM20001049, which
were considered to be robust in body condition (Tables 1, 4).
The inclusion of animals with varying body condition in this
study provides an opportunity to examine contaminant tissue
distribution in relation to blubber composition. For simplicity,
comparisons focus primarily onPPCBs, althoughobservations
PDDTs as well.
animals in comparison with robust individuals (Tables 1, 4).
Consequently, blubber accounted for a lower proportion of the
PPCB burden in thin animals (92.5–93.6%) as compared to
burden of muscle and other tissues was higher in thin animals
(6.3–7.5%) than in robust animals (2.4–3.2%).
It is unlikely that the higherPPCB burdens observed in the
lipid or organ masses, because these parameters did not appear
to differ between thin and robust animals (Tables 1, 4). There-
contaminants redistribute among the lipid components of the
body, elevating other tissuePPCB burdens.
relationship between blubber and other tissuePPCB concen-
concentrations were proportionately higher in blubber than in
other tissues (i.e., reproductive tissue, liver). However,
in animals with reduced blubber lipid the ratio between
blubber/tissue shifts, as
tissues increase and blubber concentrations are reduced.
for this compound class were consistent forPPBDEs and
Both blubber lipid content and mass were reduced in thin
robust animals (96.8–97.6%; Table 4); accordingly, thePPCB
other tissues of thin animals correspond to increases in tissue
Although limited by the small sample size, an inverse
trations was observed (Fig. 2). In robust animals,
PPCB concentrations in other
Table 4. Percent contribution of tissues to whole-body mass and persistent organic pollutant (POP) contaminant burdens in four bottlenose dolphinsa,b,c
ID WAM 631 WAM 559 VMSM20001049 FB 192
SPCB SPBDE SDDT Mass
SPCB SPBDE SDDTMass
SPCB SPBDE SDDT Mass
SPCB SPBDE SDDT
Mammary gland 0.496
aMelon omitted from analyses because mass was not taken.
b% Body mass¼masstissue(g)/massbody(g)?100%, where massbodyis the body mass recorded prior to necropsy.
c% POP body burden¼POP burdentissue (mg)/POP burdenbody (mg)?100%.
polybrominated diphenyl ethers,PDDTs¼sum of 6 dichlorodiphenyltrichloroethanes.
fSkeletal muscle mass includes pectoral, epaxial, rectus abdominal, hypaxial, scalene, sternomastoid, sternohyoid and sternothyroid muscles.
PPCBs¼sum of 69 polychlorinated biphenyls,
PPBDEs¼sum of 10
Environ. Toxicol. Chem. 29, 2010J.E. Yordy et al.
Mobilization of lipid from blubber may thus increase the
bioavailability of contaminants within other tissues and, there-
fore, the risk of exposure-related toxicity.
It should be noted that the relative increase in other tissue
exposure is small compared to the increase observed in the
melon. For example, in robust animalsPPCB concentrations
equal to 0.2% of those in blubber, whereas in thin animals
PPCB concentrations were approximately equal to 1.4% of
mass) in the liver, a metabolically active tissue, were approx-
imately equal to 1.0% of those in blubber in robust animals and
approximately equal to 7.0% of those in the blubber of a thin
individual. Although this change represents a 7-fold difference
in exposure between the two body conditions, tissuePPCB
7.0%) of those detected in blubber (Fig. 2). This small differ-
ence in the magnitude of exposure noted for reproductive
tissues and liver is in marked contrast to the large difference
inPPCB concentrations observed in the melon (Fig. 2, Table
blubberand melonwereapproximately equal(˜100%);however,
in thin animals the melon contained up to four times (˜400%) the
concentrations measured in blubber. Although this represents
only a fourfold difference inPPCB levels, it indicates PCB
any other tissue of thin animals.
At least three explanations exist for this observation. First,
the depletion of blubber lipid results in the mobilization of
blubber contaminants; the redistribution, metabolism, and/or
excretion of mobilized blubber contaminants lowers blubber
contaminant concentrations, while contaminants in the melon
remain sequestered and concentrations are unchanged. Second,
the depletion of blubber lipid results in a redistribution of
(ng/g wet mass) in reproductive tissues were approximately
those in blubber. Similarly,PPCB concentrations (mg/g wet
concentrations in thin animals were still only a fraction (1.4–
1). In robust animals,PPCB concentrations (mg/g wet mass) in
concentrations were higher in the melon than in the blubber or
blubber contaminants to other tissues, while contaminants in
the melon are labile, but respond at a slower rate than con-
taminants in blubber. Lastly, the depletion of blubber lipid
results in a redistribution of contaminants to other tissues, but
predominantly to the melon.
The first explanation, that the melon is a nonlabile sink for
lipophilic contaminants, is unlikely. Although melon lipids are
stable and metabolically inert, it is probable that the melon
contaminant burden is mobile and subject to change. Functional
images of the bottlenose dolphin cranial anatomy confirmed
that the melon is highly vascularized and receives extensive
blood flow , making it conceivable that POPs could dis-
tribute to this tissue despite its lack of metabolic activity.
Organochlorine contaminants have been measured in the melon
of fetal harbor porpoises indicating that these compounds are
deposited in melon during gestation . Furthermore, Marsili
and Focardi  observed that organochlorine contaminant
levels in the melon of striped dolphins increased with body
length in males, and decreased with body length in females,
similar to the age-related patterns observed in blubber. An age-
related increase in melon contaminants suggests contaminants
are deposited within the melon as they are accrued. Conversely,
the age-related decrease in female blubber contaminants is
typically associated with the mobilization and off-loading of
contaminants from blubber into milk; therefore, the simulta-
neous decrease in melon contaminant levels suggests that
contaminants within the melon are also subject to lactation-
associated mobilization despite a lack of lipid use from this
tissue. Cumulatively, these data support a model whereby
contaminants are capable of moving in and out of the melon
lipids, making it unlikely that melon contaminant levels would
be unaffected by changes in blubber lipid and tissue contam-
The other two options are plausible explanations for our
observation. The second explanation, that contaminants in
the melon respond to physiological changes at a slower
rate than blubber, cannot be discounted without a controlled
toxicokinetic study of POPs in cetaceans undergoing lipid
use. The last possibility—that contaminants redistribute from
blubber and predominantly to the melon—is also conceivable.
Because persistent organic pollutants strongly associate with
lipid, distribution among tissues is generally related to
tissue lipid content (Fig. 1). It is therefore imaginable that as
blubber lipid is reduced and blubber contaminants are mobi-
lized into blood that contaminants will redistribute to tissues in
accordance with their lipid content and/or composition. The
melon, the most lipid-rich tissue within the cetacean body
(Table 1) and an apparently nonmobile pool of lipid, represents
a likely alternate depot for contaminants mobilized from blub-
ber. In this scenario, the existence of the melon would have
significant implications for the bioavailability of POPs in
cetaceans. If contaminants are primarily redistributed to the
melon during periods of blubber lipid use, the presence of this
specialized structure may prevent the bulk of contaminants
from being directly available to the blood and other tissues
one of several possible explanations for the relationships
observed herein, the suggestion that this unique structure
may influence the bioavailability of POPs in cetaceans serves
as a reminder that the unique physiological traits of specific
Fig. 2. Partitioning of polychlorinated biphenyls (PCBs) between blubber
and selected tissues in relation to blubber lipid content. Relationship of
blubber lipid content (%) with ratio ofPPCBs (mg/g wet mass) in tissue
four bottlenose dolphins. Measurements were not available for liver sample
of WAM 559.
Tissue distribution and body burden of POPs in dolphins
Environ. Toxicol. Chem. 29, 20109
wildlife are important to consider when evaluating the risks of
contaminant exposure in wild populations.
Toxicokinetic data are difficult to obtain for free-ranging
cetacean species as a result of their large size, challenging
environment, and protected status. The present study is the first
to provide a detailed description of the tissue distribution of
contaminants in relation to lipid and body condition in an
odontocete cetacean. Our data suggest that, in general, distri-
bution of POPs among body compartments is related to lipid
dynamics. However, observations of tissue-specific differences
suggest that a toxicokinetic model based solely on lipid dis-
Our results confirm that blubber, the primary site of lipid
storage, is also the primary storage depot for POPs, contri-
buting substantially (>90%) to whole-body contaminant bur-
dens. Thus, with knowledge of body mass and morphometrics,
blubber may be used to estimate whole-body burdens, a more
accurate measure of cetacean exposure than tissue contami-
nant concentrations. Our observations suggest that as lipid is
mobilized from blubber, contaminants may redistribute among
body lipids, leading to increased concentrations within other
tissues. Therefore, individuals with reduced blubber-lipid
stores may be at an increased risk for exposure-related health
effects as other organs face increased exposure from the
contaminants recently mobilized from blubber. However, it
remains possible that the melon, a metabolically inert lipid-
rich structure, may serve as an alternate depot for at least some
POPs, thus preventing the bulk of blubber contaminants from
being directly available to other tissues. This unique physio-
logical adaptation should be taken into consideration when
assessing contaminant-related health effects in wild cetacean
populations. Future efforts should be directed toward the
collection of tissue-specific morphometrics and contaminant
data from stranded individuals to facilitate the estimation of
whole-body contaminant burdens and the development of
toxicokinetic models specific to odontocetes.
Figure S1. Contaminant profiles in female dolphins, WAM
631 and WAM 559.
Figure S2. Contaminant profiles in male dolphins,
VMSM20001049 and FB 192.
Table S1. Congener- and isomer-specific blubber/tissue
partition coefficients for POPs in dolphin WAM 631.
Table S2. Congener- and isomer-specific blubber/tissue
partition coefficients for POPs in dolphin WAM 559.
Table S3. Congener- and isomer-specific blubber/tissue
partition coefficients for POPs in dolphin FB 192.
Table S4. Congener- and isomer-specific blubber/tissue
partition coefficients for POPs in dolphin VMSM20001049.
(173 KB PDF).
Acknowledgement—Funding for this project was provided by the National
Marine Fisheries Service, NOAA Prescott Stranding grants and NIST.
We thank Sue Barco, Mark Swingle and the Virginia Aquarium & Marine
Science Center and Stranding Program, Ne ´lio Barros and the Mote Marine
Laboratory Stranding Investigations Program, members of the VABLAB,
especially D.J. Struntz, and the NIST Charleston laboratory for support and
Standards and Technology, nor does it imply that the equipment or
instruments are the best available for the purpose.
1. Houde M, Hoekstra PF, Solomon KR, Muir DC. 2005. Organohalogen
contaminants in delphinoid cetaceans. Rev Environ Contam Toxicol
2. Reijnders PJH. 1986. Reproductive failure in common seals feeding on
fish from polluted coastal waters. Nature 324:456–457.
Osterhaus AD. 1995. Impaired cellular immune response in harbour
Clin Exp Immunol 101:480–486.
4. Lahvis GP, Wells RS, Kuehl DW, Stewart JL, Rhinehart HL, Via CS.
1995. Decreased lymphocyte responses in free-ranging bottlenose
dolphins (Tursiops truncatus) are associated with increased concen-
103 Suppl 4: 67–72.
5. Hall AJ, Thomas GO, McConnell BJ. 2009. Exposure to persistent
organic pollutants and first-year survival probability in gray seal pups.
Environ Sci Technol 43:6364–6369.
Fair PA. 2002. Probabilistic risk assessment of reproductive effects of
polychlorinated biphenyls on bottlenose dolphins (Tursiops truncatus)
7. Wells RS, Tornero V, Borrell A, Aguilar A, Rowles TK, Rhinehart
HL, Hofmann S, Jarman WM, Hohn AA, Sweeney JC. 2005.
Integrating life-history and reproductive success data to examine
potential relationships with organochlorine compounds for bottlenose
dolphins (Tursiops truncatus) in Sarasota Bay, FL. Sci Total Environ
Reijnders PJH, Wells RS. 2006. Individual-based model framework to
bottlenose dolphins. Environ Health Perspect 114:60–64.
9. Parry DA. 1949. The structure of whale blubber and a discussion of its
thermal properties. Q J Microsc Sci 90:13–25.
10. Hamilton JL, Dillaman RM, McLellan WA, Pabst DA. 2004. Structural
fiber reinforcement of keel blubber in harbor porpoise (Phocoena
phocoena). J Morphol 261:105–117.
11. Pabst DA, Rommel SA, McLellan WA. 1999. The functional
morphology of marine mammals. In Reynolds JE III, Rommel SA,
DC, USA, pp 15–72.
12. McLellan WA, Koopman HN, Rommel SA, Read AJ, Potter CW,
Nicholas JR, Westgate AJ, Pabst DA. 2002. Ontogenetic allometry and
body composition of harbour porpoises (Phocoena phocoena, L.) from
the western North Atlantic. J Zool (Lond) 257:457–471.
T. 1981. Distribution and total burdens of chlorinated hydrocarbons in
bodies of striped dolphins (Stenella coeruleoalba). Agric Biol Chem
and sei whales. Can J Zool 63:2323–2338.
Changes in blubber distribution and morphology associated with
starvation in the harbor porpoise (Phocoena phocoena): Evidence for
regional differences in blubber structure and function. Physiol Biochem
16. Struntz DJ, McLellan WA, Dillaman RM, Blum JE, Kucklick JR, Pabst
DA. 2004. Blubber development in bottlenose dolphins (Tursiops
truncatus). J Morphol 259:7–20.
17. Dunkin RC, McLellan WA, Blum J, Pabst DA. 2005. Ontogenetic
changes in the thermal properties of Atlantic bottlenose dolphin
(Tursiops truncatus) blubber. J Exp Biol 208:1469–1480.
18. Meagher EM, McLellan WA, Westgate AJ, Wells RS, Blum JE, Pabst
DA. 2008. Seasonal patterns of heat loss in wild bottlenose dolphins
(Tursiops truncatus). J Comp Physiol B 178:529–543.
Environ. Toxicol. Chem. 29, 2010J.E. Yordy et al.
19. NorenSR,WellsRS.2009.Blubberdepositionduringontogenyinfree- Download full-text
locomotion. J Mammal 90:629–637.
bottlenose dolphins (Tursiops truncatus) from the southeastern United
States: Influence of geographic location, age class, and reproductive
state. J Morphol 269:496–511.
21. Cranford TW, Amundin M, Norris KS. 1996. Functional morphology
and homology in the odontocete nasal complex: Implications for sound
generation. J Morphol 228:223–285.
22. Harper CJ, McLellan WA, Rommel SA, Gay DM, Dillaman RM, Pabst
facial muscles in bottlenose dolphins (Tursiops truncatus). J Morphol
23. Mead JG. 1975. Anatomy of the external nasal passages and facial
complex in the Delphinidae (Mammalia:Cetacea). Smithson Contrib
24. Varanasi U, Malins DC. 1971. Unique lipids of the porpoise (Tursiops
gilli): Differences in triacyl glycerols and wax esters of acoustic
organochlorine concentrations in porpoise melon and blubber. Mar
Mamm Sci 23:434–444.
26. Kawai S, Fukushima M, Miyazaki N, Tatsukawa R. 1988. Relationship
between lipid composition and organochlorine levels in the tissues of
striped dolphin. Mar Pollut Bull 19:129–133.
27. Marsili L, Focardi S. 1997. Chlorinated hydrocarbon (HCB, DDTs and
Environ Monit Assess 45:129–180.
28. Malins DC, Varanasi U. 1975. Cetacean biosonar: Part 2. The
biochemistry of lipids in acoustic tissues. In Malins DC, Sargent JR,
eds, Biochemical and Biophysical Perspectives in Marine Biology.
Academic, New York, NY, USA, pp 237–287.
29. Wretlind A. 1957. The toxicity of low-molecular triglycerides. Physiol
30. Tanaka K, Budd MA, Efron ML, Isselbacher KJ. 1966. Isovaleric
acidemia: A new genetic defect of leucine metabolism. Proc Nat Acad
Sci U S A 56:236–242.
31. Koopman HN, Iverson SJ, Read AJ. 2003. High concentrations of
isovaleric acid in the fats of odontocetes: Variation and patterns of
accumulation in blubber vs. stability in the melon. J Comp Physiol B
the bioaccumulation of chlorobiphenyl congeners in marine mammals.
Eur J Pharmacol 270:237–251.
33. Yordy J. 2009. Persistent organic pollutant (POP) mixtures in wild
bottlenose dolphins: The influences of life history, dietary exposure,
physiology and their potential for endocrine disruption. PhD thesis.
Medical University of South Carolina, Charleston, SC, USA.
34. Borrell A, Aguilar A. 1990. Loss of organochlorine compounds in the
35. Litz JA, Garrison LP, Fieber LA, MartinezA, Contillo JP, KucklickJR.
2007. Fine-scale spatial variation of persistent organic pollutants in
bottlenose dolphins (Tursiops truncatus) in Biscayne Bay, FL. Environ
Sci Technol 41:7222–7228.
and melon oils of the beluga whale (Delphinapterus leucas). Lipids
37. Lok CM, Folkersma B. 1979. Composition of wax esters and
triacylglycerols in the melon and blubber fats of a young Sowerby’s
whale Mesoplodon bidens. Lipids 14:872–875.
bottlenose dolphin (Tursiops truncatus) blubber as a function of body
site, season and reproductive state. Can J Zool 82:1933–1942.
39. Guitart R, Guerrero X, Silvestre AM, Gutierrez JM, Mateo R. 1996.
Organochlorine residues in tissues of striped dolphins affected by the
1990 Mediterranean epizootic: Relationships with the fatty acid
composition. Arch Environ Contam Toxicol 30:79–83.
40. Tilbury KL, Stein JE, Meador JP, Krone CA, Chan SL. 1997. Chemical
contaminants in harbor porpoise (Phocoena phocoena) from the north
Atlantic coast: Tissue concentrations and intra- and inter-organ
distribution. Chemosphere 34:2159–2181.
41. Duinker JC, Hillebrand TJ, Zeinstra T, Boon JP. 1989. Individual
chlorinatedbiphenylsand pesticides intissuesofsomecetaceanspecies
from the North Sea and the Atlantic Ocean: Tissue distribution and
biotransformation. Aquat Mamm 15.3:95–124.
estuary. Environ Pollut 97:205–211.
43. Jenssen BM, Skaare JU, Ekker M, Vongraven D, Lorensten S-H. 1996.
Organochlorine compounds in blubber, liver and brain in neonatal grey
seal pups. Chemosphere 32:2115–2125.
44. Frank R, Ronald K, Braun HE. 1973. Organochlorine residues in harp
seals (Pagophilus groenlandicus) caught in eastern Canadian waters. J
Fish Res Board Can 30:1053–1063.
45. Keller JM, Kucklick JR, Harms CA, McClellan-Green PD. 2004.
blood and fat. Environ Toxicol Chem 23:726–738.
2006. Mobilization of PCBs from blubber to blood in northern elephant
seals (Mirounga angustirostris) during the post-weaning fast. Aquat
47. Opperhuizen A, van der Velde EW, Gobas FAPC, Liem DAK, van der
Steen JMD, Hutzinger O. 1985. Relationship between bioconcentration
in fish and steric factors of hydrophobic chemicals. Chemosphere
patterns of polychlorinated biphenyls and chlorinated pesticides in
northwest Atlantic pilot whales. Environ Toxicol Chem 19:667–677.
for hydrophobic contaminants in marine mammals. Environ Toxicol
R, Ridgway S. 2004. Structural and functional imaging of bottlenose
Tissue distribution and body burden of POPs in dolphins
Environ. Toxicol. Chem. 29, 201011