Lipids (2007) 42:659669

DOI 10.1007/s11745-007-3061-5

ORIGINAL ARTICLE

Uniform Fatty Acid Mobilization from Anatomically Distinct

Fat Depots in the Sable (Martes zibellina)
Petteri Nieminen Anne-Mari Mustonen

Received: 27 March 2007 / Accepted: 30 March 2007 / Published online: 2 June 2007

AOCS 2007

Abstract The mobilization of fatty acids (FA) is a BMI Body mass index
selective process in humans, rodents and the few previ- DBI Double bond index
ously studied carnivores. The FA composition of and D9-DI D9-Desaturation index
mobilization from different fat depots reflect the functions EDTA Ethylenediaminetetraacetic acid
of adipose tissues, e.g. in energy storage or insulation. FA Fatty acid
Sixteen farm-raised sables (Martes zibellina), a terrestrial FAME Fatty acid methyl ester
mustelid, were assigned into a fed control group or fasted FFA Free fatty acid
for 4 days. The FA composition of the sable was relatively FID Flame ionization detector
similar to other previously studied mustelids. The masses iab Intraabdominal
of the different fat depots decreased by 2855% during mes Mesenteric
fasting. The subcutaneous (sc) and intraabdominal (iab) MUFA Monounsaturated fatty acid
fats had a uniform FA composition and the sable could om Omental
mobilize both sc and iab FA. 18:3n-3, 18:4n-3 and 16:1n-7 PG Prostaglandin
were effectively mobilized, while long-chain saturated PUFA Polyunsaturated fatty acid
(SFA) and monounsaturated FA (MUFA) increased in RM Relative mobilization
proportion. Relative mobilization (RM) correlated in- rp Retroperitoneal
versely with the FA chain length and D9-desaturation in- sc Subcutaneous
creased RM of several MUFA compared to SFA. The SFA Saturated fatty acid
results reinforce the hypothesis that the terrestrial sable can TACL Total average chain length
utilize sc and iab fat depots as energy reserves during UFA Unsaturated fatty acid
nutritional scarcity. The natural history of the species is an VLCFA Very-long-chain fatty acid
important determinant of the FA composition and RM WAT White adipose tissue
between anatomically different fat depots.

Keywords Fasting
Fatty acids
Martes zibellina

Sable
White adipose tissue
Introduction
Abbreviations
ANOVA Analysis of variance White adipose tissue (WAT) is presently considered to be
BM Body mass an active organ and not just an inert energy store. WAT is
endocrinologically active [12], it regulates the immune
response [3] and reflects the long-term nutritional history
P. Nieminen (&)
A.-M. Mustonen
of the individual [4]. In laboratory rats (Rattus norvegicus)
Faculty of Biosciences, University of Joensuu,
P.O. Box 111, 80101 Joensuu, Finland the release of fatty acids (FA) from WAT reserves is
e-mail: pniemine@cc.joensuu.fi selective and influenced by the carbon chain length and the

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660 Lipids (2007) 42:659669

degree of unsaturation [5]. FA are mobilized more effec- Experimental Procedures

tively if they have short carbon chains, are unsaturated and
if their double bonds are located close to the terminal For these experiments 16 male sables born in spring 2004
methyl group of the chain. In rats [6], American minks were randomly divided into two experimental groups. The
(Mustela vison) [7], raccoon dogs (Nyctereutes procyono- animals were housed singly in standard cages
ides) [8] and emperor penguins (Aptenodytes forsteri) [9], (85 30 46 cm) with wooden nest boxes (24 32
longer-chain saturated (SFA) and monounsaturated FA 35 cm) suspended above ground in an unheated shed at a
(MUFA) have relatively low mobilization rates. Also in the commercial fur farm in Himanka, Finland (649N,
American marten (Martes americana), 20:0, 20:1n-11, 2342E). Before the experiment the animals were fed for
20:1n-9 and 22:1n-11 are poorly mobilized [10]. The dif- several months with a standard fur animal feed (200220 g
ferences in mobilization efficiency are independent of re- or 1,5001,600 kJ animal1 day1; slaughterhouse offal
cent FA intake and probably caused by the structure of FA 35%, Baltic herring 24%, barley 14%, cooked cereal 5%,
[11]. protein concentrate 4%, fox fat 4%, meat and feather flour
Many mammals inhabiting the boreal climate experi- 3%, mashed potatoes 2%; metabolizable energy
ence autumnal fattening followed by wintertime food 7,400 kJ kg fresh weight1; protein 13.6%, fat 9.8%, car-
scarcity and energy catabolism (for the sable M. zibel- bohydrates 13.9%; Himangan kala ja minkki Oy, Himan-
lina, see [12]). This type of seasonal body mass (BM) ka). The FA composition of the diet is depicted in Table 1.
fluctuation is considered nonpathological, while the hu- The fasting experiment was conducted between October
man weight cycling caused by repeated dieting and 29November 1, 2004. Half of the animals were put to a
weight gain is a health risk due to an increased incidence total 4-day fast, while the other half was fed using the diet
of e.g. cardiovascular diseases [13]. The sable is a ter- and procedure described above. The duration of the fast
restrial mustelid inhabiting Palearctic coniferous forests was determined to be safe for mustelids of this body size
[14]. It is mostly carnivorous but feeds also on seeds and [7, 10, 1821], yet long enough to detect the specific
berries [15, 16]. At temperatures below 30 C, the sable effects of fasting on the various FA in diverse WAT depots.
can stay in the den for several days [17]. As a conse-
quence, the species probably experiences short-term food
deprivation in its natural habitat. During a 4-day fasting Table 1 The proportions of the most abundant fatty acids (1 mol%)
in the diet of the sables (mean SE; n = 5)
period the farmed sable uses both subcutaneous (sc) and
intraabdominal (iab) fat depots as metabolic energy [18]. Fatty acid mol% in diet
Of these fat tissues, the relative loss of mass is the 14:0 1.9 0.1
highest for retroperitoneal (rp) fat. In addition, the spe- 16:0 21.0 0.8
cies utilizes body proteins during fasting indicated by
18:0 6.8 0.3
e.g. increased plasma levels of urea and essential amino
S:SFA 31.2 0.9
acids. It also experiences hepatic dysfunction evidenced
16:1n-7 5.0 0.2
by elevated plasma transaminase activities and liver tri-
18:1n-9 30.4 1.0
acylglycerol content. It can be hypothesized that the
18:1n-7 2.5 0.1
sable would exhibit active mobilization of diverse FA
20:1n-9 1.0 0.1
during fasting and there also exists the possibility of
S:MUFA 41.8 1.2
specialized roles of anatomically distinct WAT in the use
18:2n-6 16.4 2.1
of FA.
20:2n-6 1.6 0.8
The specific aims of this study were (1) to determine
18:3n-3 2.0 0.2
the FA composition of sable plasma, liver and regional
18:4n-1 1.6 0.9
WAT depots after a balanced long-term feeding of the
same diet, (2) to study the effects of food deprivation on 22:6n-3 1.7 0.1
the FA profiles of these tissues, (3) to determine the S:PUFA 27.1 1.7
possible selectivity in mobilization of different FA and n-6 PUFA 18.9 1.6
WAT depots during food deprivation and (4) to inves- n-3 PUFA 6.3 0.3
tigate the structural basis of this selectivity. Previous n-3/n-6 PUFA ratio 0.3 <0.1
data on the physiology of the sable are scarce and basic UFA/SFA ratio 2.2 <0.1
information on the fat metabolism of the species can be Also minor fatty acids not listed in the table are included in the sums
useful not only in comparative physiology but also due SFA saturated fatty acid, MUFA monounsaturated fatty acid, PUFA
to the status of the sable as a fur-producing species. polyunsaturated fatty acid, UFA unsaturated fatty acid

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Lipids (2007) 42:659669
The fed group was fasted overnight before the sampling to
avoid e.g. lipemic plasma caused by the eating of food
remnants. The overnight fast was considered relatively
short to allow sampling from the fed group during phase I
of fasting. Water was available for both experimental
groups ad lib. The experiment was approved by the Animal
Care and Use Committee of the University of Joensuu and
complied with current EU laws.
Body mass were recorded on the first day of the
experiment and at sampling. Body lengths from the tip of
the nose to the anus were also determined at sampling.
Body mass indices (BMI) indicating body adiposity of the
sable [18] were calculated with the formula BMI = BM
(kg) [body length3 (m)]1. The animals were anaesthetized
with intramuscular ketamine (5 mg kg1) and xylazine
(2 mg kg1). Blood samples were obtained sterilely by
cardiac punctures and the animals were euthanized with an
intracardial injection of a mixture of embutramide
(60 mg kg1), mebezonium (15 mg kg1) and tetracaine
hydrochloride (1.5 mg kg1). Blood samples were placed
into test tubes containing EDTA to prevent clotting, cen-
trifuged for 15 min at 4,000g, after which the plasma was
removed. The livers were dissected and the WAT samples
collected as follows: sc scapular, sc rump, sc ventral, iab
omental (om), iab mesenteric (mes) and iab rp. The sc
samples were collected from the middle of each anatomical
region and the mass of the sc depots was determined as a
whole. The iab depots were dissected and weighed sepa-
rately. The rp depot represents all WAT at the dorsal side
of the abdominal cavity around the kidneys and the great
blood vessels, while om fat and mes fat represent the whole
of the omentum and mesentery, respectively. All samples
were frozen immediately in Eppendorf vials with liquid
nitrogen and stored at 80C. The carcasses were frozen at
20 C, thawed later and the remaining WAT were dis-
sected and weighed.
The plasma free FA (FFA) concentrations were mea-
sured with the NEFA Non Esterified Fatty Acids reagents
(Randox Laboratories Ltd, Crumlin, UK) using the Tech-
nicon RA-XTTM analyzer (Swords, Ireland). For the FA
analyses, subsamples of WAT, liver and plasma were
transmethylated according to Christie [22] by heating with
1% methanolic H2SO4 under nitrogen atmosphere. The
formed FA methyl esters (FAME) were extracted with
hexane. The dried and concentrated FAME were analyzed
by a gasliquid chromatograph equipped with two injectors
and flame ionization and mass detectors (GC-FID and GC-
MS, 6890N network GC system with autosampler, FID
detector and 5973 mass selective detector, Agilent Tech-
nologies Inc, Palo Alto, CA, USA). The GC-FID and GC-
MS lines were both equipped with a DB-wax capillary
column (30 m, ID 0.25 mm, film 0.25 lm, J&W Scientific,
Folsom, CA, USA). The injection volume was 2 ll, and the
661
split ratio 1:20. The injectors were set at 250 C, and the
FID and mass interphases were at 250 and 200 C. Helium
was used as a carrier gas (1.8 and 1.0 ml min1 for FID and
mass detecting lines). The initial oven temperature of
180 C was held for 8 min, and then programmed to rise by
3 C min1 to a final temperature of 210 C, which was
maintained for 25 min. The peaks were reintegrated man-
ually and the mass spectra extracted using the Agilent
ChemStation software (Agilent Technologies Inc). The
FAME were identified based on the retention time, mass
spectrum and comparisons with authentic (Sigma, St.
Louis, MO, USA) and natural standards of a known com-
position and published reference spectra (WW Christie
http://www.lipidlibrary.co.uk/masspec.html). Quantifica-
tions were based on FID responses. The peak areas of the
FID chromatograms were converted to mol% by using the
theoretical response factors [23] and calibrations with
quantitative authentic standards. The FA were marked by
using the abbreviations: [carbon number]:[number of
double bonds] n-[position of the first double bond calcu-
lated from the methyl end]. If not stated otherwise, poly-
unsaturated FA (PUFA) were methylene-interrupted.
The double bond index (DBI) and the total average
chain length (TACL) indicating the mean number of dou-
ble bonds or carbon atoms per molecule were calculated
according to standard formulae [24]. D9-Desaturation in-
dex (D9-DI), the ratio of the most important potentially
endogenous D9-MUFA to the corresponding SFA, was
calculated as [(mol% 14:1n-5) + (mol% 16:1n-7) + (mol%
16:1n-9) + (mol% 18:1n-9) + (mol% 18:1n-7)]:[(mol%
14:0) + (mol% 16:0) + (mol% 18:0)]. The very-long-chain
FA (VLCFA) were calculated as the sum of all FA with a
chain length 24 carbons (i.e. 24:0 + 24:1n-9; ref. 25).
Relative mobilization (RM) was calculated by the formula:
[mol% in the fed animalsmol% in the fasted ani-
mals]:[mol% in the fed animals] [10]. The FA composition
and RM were also determined for the total pooled sc
(scapular, rump and ventral combined) and total pooled iab
(om, mes and rp combined) fat depots.
Multiple comparisons were performed with the one-way
analysis of variance (ANOVA) followed by the Duncans
post hoc test. The normality of distribution and the
homogeneity of variances were determined with the Kol-
mogorovSmirnov test and the Levene test. Comparisons
between the two study groups were performed with the
Students t test for independent samples. In case of non-
parametric data (normality of distribution and homogeneity
of variances not attained after standard transformations),
the MannWhitney U test was used. Significant differences
in the time series (BM) were analyzed with the t-test for
related samples. Correlations were calculated using the
Spearman correlation coefficient (rs). The P value less than
0.05 was considered to be statistically significant. The re-
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662
sults are presented as the mean SE. FA with proportions
> 0.1% are presented in the tables, but also FA with trace
amounts were included in the sums and used in the cal-
culation of indices.
Results
The initial BM of the fed (1.20 0.04 kg) and the fasted
sables (1.17 0.05 kg) did not differ between the experi-
mental groups, while the BM of the fasted animals was
lower after the 4-day food deprivation period (1.14 0.03
vs. 0.98 0.03 kg). Decreases in the absolute and relative
masses of the specific fat depots due to fasting were as
follows: total sc fat: fed 59.0 7.1 vs. fasted 27.6 6.6 g;
difference 53%; P < 0.05; om fat: 9.2 1.0 vs.
6.3 1.6 g; 32%; NS; mes fat: 8.5 0.8 vs. 6.1 1.4 g;
28%; NS; rp fat: 13.8 2.4 vs. 6.2 1.4 g; 55%; P < 0.05
and total iab fat: 33.5 4.2 vs. 19.6 4.6 g; 41%;
P < 0.05. The body fat% was significantly higher in the fed
animals than in the fasted group (8.0 0.8 vs. 4.7 1.0%).
The concentrations of plasma FFA were higher in the
fasted animals (0.6 0.18 vs. 2.6 0.57 mmol l1,
P < 0.05). The most abundant FA (proportion > 1%) in
sable plasma were 16:0, 18:0, 18:1n-9, 18:1n-7, 18:2n-6,
20:4n-6, 20:5n-3, 22:5n-3 and 22:6n-3 (Table 2). Fasting
caused decreases in the proportions of 15:0, 17:0, 18:0,
16:1n-9, 18:2n-6, total dienes and trienes, n-6 PUFA and
total PUFA in plasma, while the proportions of 14:0, 16:0,
total SFA, 14:1n-9, 20:1n-11, 20:1n-9, 22:1n-11, total
MUFA and total n-3 PUFA as well as the n-3/n-6 PUFA
ratios increased. The ratio of unsaturated FA (UFA) to SFA
decreased in plasma. In liver, the most obvious decreases
induced by fasting were in 17:0, 18:0, 22:0, 24:0, 20:4n-6,
22:4n-6, total n-6 PUFA and total PUFA, while the pro-
portions of 12:0, 14:0, 14:1n-5, 18:1n-9, 20:1n-11, 20:1n-9
and total MUFA increased. The DBI and TACL decreased
in liver due to food deprivation. In plasma and liver the
proportions of 16:0, 18:0, 20:4n-6, 20:5n-3 and 22:6n-3
were higher than in the WAT, while the proportions of
several MUFA, especially 16:1n-7 and 18:1n-9, were
lower. The most abundant FA with decreased proportions
in WAT due to fasting were 16:1n-7, 18:3n-3 and 18:4n-3,
while the percentages of 14:0, 20:0, 22:0, 24:0, 20:1n-11,
20:1n-9, 22:1n-11 and 24:1n-9 increased (Tables 2, 3, 4).
The n-3/n-6 PUFA ratio decreased in the pooled sc and iab
fat depots as well as in the mes and rp fats. The sum of
VLCFA increased in the pooled sc and iab fat depots.
Most FA increased in proportion in the WAT during
fasting (Fig. 1). 20:0, 22:1n-11, 20:1n-11, 20:1n-9 and
22:5n-3 were mostly preserved, while 18:3n-3, 18:4n-3,
16:1n-7, 17:1n-8, 15:0 and 16:0 had high RM values. There
were no differences in RM of FA between the different
123
Lipids (2007) 42:659669
WAT. RM of SFA correlated negatively with the chain
length when all trunk WAT were analyzed as a whole
(rs = 0.127, P < 0.01; Fig. 2a). The same was observed in
n-5 (rs = 0.191, P < 0.01), n-7 (rs = 0.285, P < 0.01)
and n-9 MUFA (rs = 0.366, P < 0.01; Fig. 2b). The
influence of chain length on RM of PUFA was tested by
comparing PUFA with the same degree of unsaturation and
position of the first double bond but a different chain
length. The difference was significant in five out of eight
pairs in the way that the PUFA with the longer chain length
had a lower RM value (Fig. 2c). When SFA and corre-
sponding MUFA were compared, RM increased signifi-
cantly with D9-desaturation in three out of seven pairs
(Fig. 2d). The influence of unsaturation on RM of PUFA
was studied by comparing PUFA with the same chain
length and position of the first double bond but with a
different double bond number. The difference was signifi-
cant in one out of eight pairs in the way that the PUFA with
the higher number of double bonds had a higher RM rate.
The influence of positional isomerism on RM of MUFA
was tested by comparing MUFA of the same chain length
but different position of the double bond. The difference
was statistically significant in 4 out of 11 pairs in the way
that the MUFA with the double bond closer to the methyl
end of the molecule had a lower (three cases) or a higher
RM value (one case). When comparing PUFA with the
same chain length and unsaturation but with a different
position of the first double bond, the difference was sta-
tistically significant in one out of seven pairs in the way
that the PUFA with the first double bond closer to the
methyl end had a lower RM rate.
Discussion
The FA composition of the tissues of the farmed sable was
quite similar to another mustelid, the farmed American
mink [7, 2627] with 16:0, 18:0, 18:1n-9 and 18:2n-6 as
the most abundant FA. The sc and iab WAT depots of the
sable contained less total MUFA (46 vs. 5255%) but
higher proportions of total PUFA (20 vs. 10%) compared to
the mink due to e.g. the high percentage of 18:2n-6 (16 vs.
78%). The FA profile of the sable was also very similar to
the closely related farmed American marten [10], which
had slightly more SFA, especially 14:0 and 20:0 in its fat
tissues, while the percentages of MUFA, especially 18:1n-
9, were higher in the sable. As the FA composition of the
diets probably varied between the studies, the observed
differences between the species could have been caused by
different FA intake. The most abundant FA in the WAT of
the farmed sable were also mostly the same as recorded
previously for the wild raccoon dog, European brown bear
(Ursus arctos arctos) and gray wolf (Canis lupus; 28).
Lipids (2007) 42:659669 663

Table 2 Effects of fasting on the composition of the most abundant fatty acids (mol%) in total sc and iab fat tissues, plasma and livers of the
sables (mean SE)
Fatty acid Total sc fat Total iab fat Plasma Liver
Fed Fasted Fed Fasted Fed Fasted Fed Fasted

12:0 0.7 <0.1a 0.8 <0.1*b 0.7 <0.1a 0.7 <0.1a 0.3 0.1 0.3 0.1 0.9 0.2 3.1 0.5*
a b a
14:0 5.1 0.2 6.1 0.3* 5.0 0.3 5.3 0.4a 0.6 0.1 0.9 0.1* 1.3 0.2 3.4 0.7*
16:0 20.5 0.2 19.6 0.5 20.8 0.3 19.7 0.7 22.9 0.4 27.0 0.6* 25.6 0.5 27.0 0.6
17:0 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.4 <0.1 0.3 <0.1* 0.4 <0.1 0.3 <0.1*
18:0 6.3 0.2 6.5 0.2 6.7 0.2 7.8 0.4* 12.7 0.3 11.0 0.2* 14.3 0.9 8.6 1.6*
S:0 33.9 0.3 33.3 1.4 34.5 0.4 35.1 0.6 38.3 0.4 40.9 0.6* 43.8 0.6 43.6 0.5
14:1n-5 0.2 <0.1 0.3 <0.1 0.2 <0.1 0.2 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.2 <0.1*
16:1n-9 0.6 <0.1 0.6 <0.1* 0.6 <0.1 0.6 <0.1 0.3 <0.1 0.2 <0.1* 0.4 <0.1 0.5 <0.1
16:1n-7 4.4 0.3b 3.8 0.2ab 3.9 0.2b 3.1 0.3*a 0.9 0.1 1.0 0.1 1.6 0.2 2.7 0.5
18:1n-9 35.9 0.3 35.4 0.2 35.6 0.3 34.6 1.0 13.8 0.3 15.2 0.6 12.2 0.6 16.1 1.6*
18:1n-7 2.6 <0.1 2.6 <0.1 2.6 <0.1 2.7 0.1 1.8 <0.1 1.9 0.1 2.3 0.1 2.4 0.1
24:1n-9 0.1 <0.1 0.1 <0.1* 0.1 <0.1 0.2 <0.1* 0.5 <0.1 0.6 <0.1 0.3 <0.1 0.2 <0.1
S:1 46.1 0.4 43.8 1.8 45.6 0.3 44.4 1.1 18.2 0.4 20.1 0.7* 17.7 0.6 23.4 2.2*
D9-DI 1.4 <0.1 1.3 <0.1 1.3 <0.1 1.3 <0.1 0.5 <0.1 0.5 <0.1 0.4 <0.1 0.6 0.1*
18:2n-6 15.8 0.2 15.8 0.1 16.0 0.2 16.2 0.4 22.5 1.0 15.3 0.5* 15.4 0.4 16.5 0.5
20:2n-6 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.1 <0.1 0.2 <0.1 0.3 <0.1 0.2 <0.1
18:3n-6 0.1 <0.1 0.1 <0.1* 0.1 <0.1 0.1 <0.1* 0.6 <0.1 0.2 <0.1* 0.5 <0.1 0.3 <0.1*
18:3n-3 1.2 <0.1c 1.0 <0.1*b 1.2 <0.1c 0.9 0.1*a 0.5 <0.1 0.4 <0.1 0.6 0.1 0.8 0.1
18:4n-3 0.1 <0.1 0.1 <0.1* 0.1 <0.1 0.1 <0.1* 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.2 <0.1
20:3n-6 0.1 <0.1 0.2 <0.1 0.1 <0.1 0.2 <0.1 0.9 0.1 0.4 <0.1* 0.8 0.1 0.3 <0.1*
20:4n-6 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.6 0.3 7.4 0.4 8.1 0.2 6.1 0.5 3.4 0.7*
22:4n-6 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.1 <0.1*
20:5n-3 0.2 <0.1 0.1 <0.1* 0.2 <0.1 0.2 <0.1 2.3 0.1 2.2 0.2 1.5 0.1 1.1 0.1*
22:5n-3 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.3 0.1 1.2 0.1 1.2 0.1 1.3 0.1 0.9 0.1
22:6n-3 0.9 <0.1 0.9 0.1 0.8 <0.1 0.8 0.2 7.1 0.4 10.0 0.7* 10.8 0.4 8.6 1.5
S:PUFA 20.0 0.2 20.3 0.7 19.9 0.3 20.5 0.9 43.5 0.6 39.1 0.7* 38.5 1.0 33.0 1.8*
S:n-6 PUFA 16.8 0.2 18.0 1.3 16.9 0.2 17.7 0.7 32.0 1.0 24.8 0.6* 23.7 0.5 21.0 0.4*
S:n-3 PUFA 3.0 0.1 3.4 0.7 2.7 0.1 2.6 0.3 11.4 0.5 14.1 0.7* 14.6 0.5 11.8 1.5
n-3/n-6 PUFA 0.2 <0.1c 0.2 <0.1*b 0.2 <0.1bc 0.1 0.1*a 0.4 <0.1 0.6 <0.1* 0.6 <0.1 0.6 <0.1
S:VLCFA 0.1 <0.1 0.2 <0.1* 0.1 <0.1 0.2 <0.1* 0.7 <0.1 0.7 <0.1 0.4 <0.1 0.3 0.1
UFA/SFA 2.0 <0.1 2.5 0.6 1.9 <0.1 1.9 <0.1 1.6 <0.1 1.5 <0.1* 1.3 <0.1 1.3 <0.1
DBI 0.9 <0.1 0.9 <0.1 0.9 <0.1 0.9 <0.1 1.6 <0.1 1.7 <0.1 1.6 <0.1 1.4 <0.1*
TACL 17.3 <0.1 17.3 <0.1 17.3 <0.1 17.4 0.1 17.9 <0.1 18.0 <0.1 18.0 0.1 17.4 0.2*
sc subcutaneous, iab intraabdominal, D9-DI D9-desaturation index, PUFA polyunsaturated fatty acid, VLCFA very-long-chain fatty acid (chain
length 24 C), UFA unsaturated fatty acid, SFA saturated fatty acid, DBI double bond index, TACL total average chain length. Also minor fatty
acids not listed in the table are included in the sums
* Significant difference between the fed and the fasted animals (t test, MannWhitney U test, P < 0.05), means with no common letter indicate
that the values of sc and iab fats differ at P < 0.05 (one-way ANOVA)

The FA composition of the trunk WAT was very uni-
form in the sable and no clear differences could be detected
in the FA proportions between the sc and iab fats. This is
quite different from the related American mink, which has
significantly lower proportions of total SFA but higher
percentages of total MUFA in its sc fats compared to the
iab depots [7]. In addition, the DBI and D9-DI are higher in
the sc depots of the mink, which results from the high
proportions of longer-chain SFA in the iab fats. These FA
have high melting points and could thus be at risk of
solidification during swimming if they were concentrated
in the sc depots of the mink. As a terrestrial species with
good insulation against cold air, the sable does not seem to
require similar FA gradients as a thermal adaptation. While
it has been established that an unsaturation gradient exists
also between the trunk fats and the body appendages in the

123
 664

123
Table 3 Effects of fasting on the composition of the most abundant saturated and monounsaturated fatty acids (mol%) in adipose tissues of the sables (mean SE)
Fatty acid Scapular sc fat Rump sc fat Ventral sc fat Mesenteric fat Omental fat Retroperitoneal fat
Fed Fasted Fed Fasted Fed Fasted Fed Fasted Fed Fasted Fed Fasted

12:0 0.7 0.1 0.7 0.1 0.6 <0.1 0.8 0.1 0.7 <0.1 0.8 <0.1* 0.6 <0.1 0.6 0.1 0.8 0.1 0.8 <0.1 0.6 <0.1 0.6 <0.1
14:0 5.4 0.6 5.8 0.5 4.8 0.2 5.8 0.5 5.0 0.4 6.7 0.6* 4.3 0.2 4.4 0.7 6.4 0.4 6.8 0.4 4.1 0.1 4.8 0.4
16:0 20.8 0.3 19.6 0.9 20.3 0.3 19.2 1.0 20.5 0.4 20.2 0.7 20.2 0.5 19.6 1.2 22.3 0.4 21.4 1.3 20.0 0.4 18.1 1.1
18:0 6.1 0.5 6.8 0.3 6.3 0.3 6.6 0.5 6.4 0.3 6.3 0.2 7.2 0.3 8.6 0.8 5.7 0.3 6.3 0.4 7.3 0.2 8.4 0.6
S:0 34.3 0.4 34.4 0.8 33.3 0.4 33.9 0.8 34.0 0.6 31.5 4.2 33.7 0.5 34.9 1.2 36.6 0.5 36.7 1.0 33.4 0.3 33.7 0.7
14:1n-5 0.3 0.1 0.2 <0.1 0.2 <0.1 0.3 <0.1 0.2 <0.1 0.3 <0.1* 0.2 <0.1 0.2 <0.1 0.3 <0.1 0.3 <0.1 0.2 <0.1 0.2 <0.1
16:1n-9 0.6 <0.1 0.6 <0.1 0.6 <0.1 0.7 <0.1 0.6 <0.1 0.6 <0.1 0.6 <0.1 0.6 0.1 0.6 <0.1 0.6 <0.1 0.6 <0.1 0.7 <0.1
16:1n-7 4.6 0.6 3.4 0.3 4.4 0.4 3.9 0.4 4.1 0.3 4.1 0.3 3.5 0.3 2.6 0.4 4.8 0.4 4.2 0.5 3.5 0.2 2.5 0.4
18:1n-9 35.4 0.5 35.7 0.4 36.2 0.4 35.7 0.5 36.0 0.5 34.9 0.4 36.2 0.4 33.7 2.8 34.2 0.5 34.3 0.5 36.4 0.3 35.7 0.8
18:1n-7 2.5 0.1 2.6 0.1 2.6 <0.1 2.6 0.2 2.6 <0.1 2.6 0.1 2.6 0.1 2.8 0.1 2.5 0.1 2.5 0.1 2.6 <0.1 2.8 0.1
20:1n-11 0.2 <0.1 0.3 <0.1* 0.3 <0.1 0.3 <0.1* 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.4 0.1 0.2 <0.1 0.3 0.1 0.3 <0.1 0.4 0.1
20:1n-9 1.0 0.1 1.4 0.1* 1.1 0.1 1.4 0.2 1.1 0.1 1.2 0.1 1.2 0.1 1.2 0.2 0.9 0.1 1.2 0.2 1.2 0.1 1.7 0.3
24:1n-9 0.1 <0.1 0.1 <0.1* 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.2 <0.1* 0.1 <0.1 0.1 <0.1* 0.1 <0.1 0.2 <0.1*
S:1 45.8 0.5 45.6 0.4 46.6 0.7 46.2 0.6 46.0 0.7 39.7 5.4 45.9 0.5 43.0 3.2 44.8 0.5 44.7 0.4 46.0 0.4 45.5 0.8
D9-DI 1.4 <0.1 1.3 <0.1 1.4 <0.1 1.4 <0.1 1.4 <0.1 1.3 <0.1 1.4 <0.1 1.3 0.1 1.2 <0.1 1.2 <0.1 1.4 <0.1 1.3 <0.1
sc subcutaneous, D9-DI D9-desaturation index. Also minor fatty acids not listed in the table are included in the sums
* Significant difference between the fed and the fasted animals (t test, MannWhitney U test, P < 0.05)
Lipids (2007) 42:659669
 Table 4 Effects of fasting on the composition of the most abundant polyunsaturated fatty acids (mol%) in adipose tissues of the sables (mean SE)
Fatty acid Scapular sc fat Rump sc fat Ventral sc fat Mesenteric fat Omental fat Retroperitoneal fat
Lipids (2007) 42:659669

Fed Fasted Fed Fasted Fed Fasted Fed Fasted Fed Fasted Fed Fasted

18:2n-6 15.7 0.4 16.0 0.2 15.9 0.3 15.9 0.3 15.9 0.2 15.5 0.3 16.5 0.2 17.4 0.9 14.9 0.3 15.1 0.4 16.7 0.2 16.3 0.4
18:3n-3 1.2 0.1 1.0 0.1* 1.2 0.1 1.0 0.1* 1.2 0.1 1.0 0.1* 1.2 0.1 0.8 0.1* 1.2 0.1 1.0 0.1 1.2 0.1 0.8 0.1*
18:4n-3 0.1 <0.1 0.1 <0.1 0.2 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1* 0.2 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1*
20:4n-6 0.2 <0.1 0.2 <0.1 0.3 <0.1 0.3 0.1 0.2 <0.1 0.2 <0.1 0.2 <0.1 1.1 0.9 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.6 0.4
22:4n-6 0.1 <0.1 0.2 <0.1 0.1 <0.1 0.2 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.2 <0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.2 <0.1
20:5n-3 0.2 <0.1 0.1 <0.1* 0.1 <0.1 0.1 <0.1 0.2 <0.1 0.1 <0.1 0.1 <0.1 0.3 0.3 0.2 <0.1 0.1 <0.1* 0.1 <0.1 0.1 0.1
22:5n-3 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.3 0.1 0.3 <0.1 0.3 <0.1 0.3 <0.1 0.3 0.1 0.2 <0.1 0.3 <0.1 0.3 <0.1 0.5 0.2
22:6n-3 0.9 0.1 0.9 0.1 0.9 0.1 0.9 0.1 0.9 0.1 0.8 0.1 0.8 0.1 0.8 0.2 0.7 0.1 0.7 0.1 0.8 0.1 1.0 0.4
S:PUFA 19.9 0.5 20.0 0.4 20.1 0.4 19.9 0.1 20.0 0.3 21.2 1.9 20.4 0.3 22.1 2.3 18.6 0.4 18.5 0.6 20.6 0.3 20.8 1.1
S:n-6 PUFA 16.7 0.4 17.0 0.3 16.9 0.3 16.9 0.4 16.9 0.2 20.2 3.8 17.5 0.2 19.3 1.9 15.7 0.3 15.9 0.5 17.6 0.2 17.9 0.5
S:n-3 PUFA 3.0 0.1 2.8 0.2 3.0 0.2 2.7 0.2 3.0 0.1 4.8 2.1 2.8 0.1 2.6 0.5 2.7 0.1 2.4 0.1 2.7 0.1 2.8 0.6
n-3/n-6 PUFA 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.1 <0.1* 0.2 <0.1 0.2 <0.1 0.2 <0.1 0.1 <0.1*
S:VLCFA 0.1 <0.1 0.2 <0.1 0.1 <0.1 0.2 <0.1 0.1 0.1 0.1 <0.1 0.1 <0.1 0.3 0.1 0.1 <0.1 0.1 <0.1 0.1 <0.1 0.2 0.1
UFA/SFA 1.9 <0.1 1.9 0.1 2.0 <0.1 2.0 0.1 2.0 0.1 3.7 1.9 2.0 <0.1 1.9 0.1 1.7 <0.1 1.7 0.1 2.0 <0.1 2.0 0.1
DBI 0.9 <0.1 0.9 <0.1 1.0 <0.1 0.9 <0.1 0.9 <0.1 0.9 <0.1 0.9 <0.1 1.0 0.1 0.9 <0.1 0.9 <0.1 0.9 <0.1 1.0 0.1
TACL 17.3 0.1 17.3 <0.1 17.3 <0.1 17.3 0.1 17.3 <0.1 17.2 <0.1 17.4 <0.1 17.4 0.1 17.2 <0.1 17.2 0.1 17.4 <0.1 17.5 0.1
sc subcutaneous, PUFA polyunsaturated fatty acid, VLCFA very-long-chain fatty acid (chain length 24 C), UFA unsaturated fatty acid, SFA saturated fatty acid, DBI double bond index,
TACL total average chain length. Also minor fatty acids not listed in the table are included in the sums
* Significant difference between the fed and the fasted animals (t test, MannWhitney U test, P < 0.05)

123
665
666 Lipids (2007) 42:659669

Fig. 1 In vivo relative

mobilization of the most
abundant fatty acids in the white
adipose tissues of the sables
fasted for 4 days, all trunk
adipose tissues analyzed as a
whole (mean + SE). Positive
values indicate that the
proportion of a fatty acid has
decreased in the fasted animals
compared to the fed control
group, negative values signify
that the proportion of a fatty
acid has increased compared to
the fed group. The asterisk
indicates that the proportion
(mol%) of a fatty acid in the
fasted group is significantly
different from the
corresponding value of the fed
animals

Fig. 2 Effects of fatty acid structure on relative mobilization in the
sables after 4 days of fasting, all trunk adipose tissues analyzed as a
whole. Positive values indicate that the proportion of a fatty acid has
decreased in the fasted animals compared to the fed control group,
negative values signify that the proportion of a fatty acid has
increased compared to the fed group. a Relative mobilization of
saturated fatty acids (SFA) of different carbon chain lengths
(mean + SE). b Correlation between relative mobilization and fatty
acid chain length of monounsaturated fatty acids (MUFA), cir-
cles = n-5 MUFA, triangles = n-7 MUFA, squares = n-9 MUFA
(mean SE). c Effect of fatty acid chain length on relative
mobilization of selected polyunsaturated fatty acids (PUFA), *sig-
nificant difference in relative mobilization between PUFA with the
same degree of unsaturation but different chain length (t test,
P < 0.05; mean + SE). d The influence of D9-desaturation on relative
mobilization of selected fatty acids, *significant difference in relative
mobilization between SFA and corresponding MUFA (t test,
P < 0.05; mean + SE)

123
Lipids (2007) 42:659669
sable [29], it is more modest than in the American mink
[7]. The terrestrial American marten also exhibits an
indistinct FA gradient with a lower percentage of 18:0 and
a higher proportion of 16:1n-7 in the sc fat compared to the
iab depots but no differences in the total SFA, MUFA or
fluidity indices, thus bearing close similarity to the sable
[10].
Several changes in the relative proportions of minor FA
were recorded in the fasted sables. Many of these statisti-
cally significant effects can be physiologically quite irrel-
evant by themselves, while the sum of these effects, e.g.
changes in the n-3/n-6 PUFA balance can be important.
Preferential hydrolysis of particular PUFA can have sig-
nificant health effects (discussed later) or reveal details
about the structural basis of FA mobilization, which has
previously been shown to be selective in e.g. rats [6],
American marten and mink [7, 10] and raccoon dogs [8].
According to Raclot et al. [11], the site of fat depot has no
major influence on the mobilization of FA in rats and the
same was established also for the American marten [10]
and the sable. In contrast, the semiaquatic American mink
mobilizes FA more efficiently from its iab depots com-
pared to the sc fats probably as an adaptation to preserve
fluidity in the sc depots for aquatic predation [7].
The shorter and more unsaturated FA of triacylglycerol
molecules are supposedly distributed more peripherally in
the lipid droplet at the water-lipid interface [30]. As a re-
sult, they could be more easily accessible to hormone-
sensitive lipases and hydrolyzed during food deprivation
leading to an increase in the relative amount of less polar
FA in the WAT depots. This was observed also in the
sables as chain length correlated negatively with RM in
SFA, most MUFA and several PUFA. This seems to be a
general feature of FA mobilization in mammals, as the
same has been observed in rats [6], American marten and
mink [7, 10] and raccoon dogs [8]. In these species,
especially 20:0, 20:1n-11, 20:1n-9, 22:1n-11 and 24:1n-9
are poorly mobilized and similar phenomena were ob-
served in the WAT of the fasted sables. Only the ventral sc
fat diverged slightly from this by the relative preservation
of especially 12:0, 14:0 and 14:1n-5. In addition, the pro-
portion of 12:0 in liver increased over three-fold after 4 d
of fasting. The increase in the percentages of 12:0 and 14:0
could have been caused e.g. by chain-shortening of longer
FA. These mechanisms would decrease the undesirable
fasting-induced changes in the fluidity by preserving those
SFA that have relatively low melting points, especially in
the ventral sc depot, which would be in the closest contact
with snow in winter. In rats, for FA of the same carbon
chain length, mobilization usually increases with the
number of double bonds [6]. Similar results could be ob-
tained from the sables, as the RM of MUFA was higher
than that of the corresponding SFA in several cases. In
667
PUFA, there were no significant changes in RM with
increasing unsaturation. These data were also quite similar
to previous studies on the American marten [10].
The principle of competitive inhibition in the metabo-
lism of PUFA in mammals suggests that n-3 PUFA are
preferred over n-6 PUFA in the rate-limiting steps of de-
saturation reactions [31]. The more intensive RM of n-3
PUFA from the fat depots of the sable could be observed in
the decrease of the n-3/n-6 PUFA ratio in the sc and iab
fats. Opposite to this, the n-3/n-6 PUFA ratio and the
proportion of n-3 PUFA increased in plasma as n-3 PUFA
were released into the circulation to be utilized for meta-
bolic energy. An exception was the unchanged WAT pro-
portion of 22:6n-3, which is very important for biological
membranes [32]. In fact, some of the observed decreases in
the proportions of various n-3 PUFA could be due to their
metabolic conversion into 22:6n-3. As a result, the relative
abundance of circulating 22:6n-3 increased to be distrib-
uted to various tissues. Similar effects of fasting on n-3 and
n-6 PUFA have been previously detected in the rat [30] and
several carnivores [78, 10]. The fasted sables also had
decreased proportions of 18:2n-6 in plasma, while in the
other studied tissues the percentages of this important
precursor of longer-chain n-6 PUFA were stable. The ob-
served decrease could be due to altered lipoprotein profile
in plasma due to fasting. It is also possible that 18:2n-6
could have been transferred into various tissues to be used
in biosynthesis pathways causing the relative decrease in
the plasma percentages.
It has been previously established that the lymphocyte
count of the sable decreases during fasting indicating
immunosuppression [18]. Important molecular regulators
of the immune function derive from particular long-chain
PUFA. 18:2n-6 is first metabolized into 18:3n-6, which is
further converted into long-chain n-6 PUFA [31]. Of these,
20:3n-6 is the precursor of 1-series prostaglandins (PG),
while 20:4n-6 and 22:4n-6 are transformed into 2- and 4-
series PG. 18:3n-3 is converted via 18:4n-3 and 20:4n-3
into 20:5n-3, which is the precursor of 3-series PG, espe-
cially PGE3 and leukotrienes. The decreases in 18:3n-3 and
18:4n-3 observed in the sc and iab fats of this study can be
due to the conversion of these PUFA into 20:5n-3 to be
used in PG synthesis. Yet also the percentages of longer-
chain PUFA eventually decreased, as the 20:5n-3 propor-
tion of WAT and the 20:4n-6 and 22:4n-6 percentages of
liver decreased during fasting. This could indicate trans-
formation of these PUFA into PGE3 and 2- and 4-series
PG. PGE3 is especially important as it has beneficial health
effects in humans, such as inhibition of lung cancer cell
proliferation [33]. Increased proportions of n-6 PUFA
predispose to cardiac diseases [34], while the proportions
very-long-chain n-3 PUFA correlate inversely with the
incidence of myocardial infarction [35]. These phenomena
123
668
could be among the causes of adverse health effects ob-
served during prolonged food deprivation in various
mammalian species experiencing preferential hydrolysis of
n-3 PUFA.
The FA composition showed a high similarity between
the sc and iab WAT in the terrestrial sable. The species was
able to mobilize all its major sc and iab fat depots while
preserving particular PUFA, such as 20:4n-6 and 22:6n-3,
required for e.g. eicosanoid production and membrane
stability. This was similar to another terrestrial mustelid,
the American marten [10] but different from the semi-
aquatic American mink, which displays a clear FA gradient
of unsaturation between its sc and iab trunk fats and
mobilizes FA from its iab depots more efficiently as an
adaptation to aquatic predation [7]. The mechanisms of
selective FA mobilization in the sable are most probably
dictated by the structure of FA molecules. FA chain length
and D9-desaturation seem to exert the strongest influence
on the RM in the species.
Acknowledgments This study was financially supported by the
Academy of Finland, by the Otto A. Malms Donation Fund and by
the Helve Foundation. We sincerely thank Tommi Paakkonen for
assistance and Eero Joensuu and his personnel for providing us with
the experimental animals.
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