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First published online December 14, 2007
Journal of Experimental Biology 211, 29-34 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.009340
Selective mobilization of fatty acids from adipose tissue in migratory birds
1 Division of Biological Sciences, University of Montana, Missoula, MT 59812,
USA
2 Faculty of Biosciences, University of Helsinki, Helsinki 00014, Finland
Author for correspondence (e-mail:
eprice3{at}uwo.ca)
Accepted 15 October 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: migration, relative mobilization, unsaturated fatty acids, linoleic acid, hormone-sensitive lipase, Zonotrichia, Philomachus
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Hollenberg and Angel, 1963;
Raclot and Groscolas, 1993;
Soppela and Nieminen, 2002).
This fatty acid selectivity has been demonstrated in both in vivo
(Herzberg and Skinner, 1997;
Nieminen et al., 2006;
Soppela and Nieminen, 2002)
and in vitro (Raclot and
Groscolas, 1993; Raclot et
al., 1995) studies and has led to adaptive explanations regarding
the functions of the specific fatty acids that are selectively retained or
mobilized (Falkenstein et al.,
2001; Florant et al.,
1990; Nieminen et al.,
2006; Soppela and Nieminen,
2002). However, in a recent review, Raclot concluded that
differential mobilization of fatty acids occurs primarily due to the molecular
structure of each fatty acid species; fatty acids that are shorter, more
unsaturated and have their double bonds closer to the methyl end are more
polar and are preferentially mobilized
(Raclot, 2003). This may occur
due to a combination of enzyme specificity, access of HSL to polar lipids at
the lipid/aqueous interface, and other lipid transport processes within the
adipocyte (Raclot, 2003;
Raclot et al., 2001).
During migratory flights, birds engage in endurance (often >8 h)
exercise, achieving maximal rates of oxygen consumption that are more than
double those achieved by similarly sized mammals, all while fasting
(Butler and Woakes, 1990).
Stored adipose TRIG serves as the primary fuel source during these flights
(McWilliams et al., 2004;
Odum et al., 1964;
Ramenofsky, 1990), and birds
undergo seasonal changes in physiology that allow them to utilize fat at high
rates (Guglielmo et al.,
2002a; Jenni-Eiermann and
Jenni, 1992; Pelsers et al.,
1999). The mobilization of lipids from adipocytes is an important
step in this process (Johnston,
1973). The selective mobilization of particular fatty acids may
also be important given that the fatty acid composition of adipose stores can
affect migratory performance (Johnston,
1973; Pierce et al.,
2005). Nonetheless, the phenomenon of selective fatty acid
mobilization at the adipose tissue has not been studied in birds except in
fasting penguins (Groscolas,
1990; Johnson and West,
1973). Moreover, to our knowledge, selective fatty acid
mobilization has not been investigated in vitro in any animal during
its different life history stages and periods of energy demand. The goals of
this study, therefore, were to characterize the selective mobilization of
fatty acids in vitro for two migratory bird species and to
investigate any changes in selective fatty acid mobilization associated with
the migratory period in one of the species. Specifically, we were interested
in whether migratory state would result in an increase in mobilization of
18:2n6 (Soppela and Nieminen,
2002) or a selective retention of 18:2n6, perhaps to conserve this
fatty acid for use during breeding
(Florant et al., 1990;
Mostafa et al., 1994).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Twelve white-crowned sparrows (Zonotrichia leucophrys gambelii
Nuttall) were captured during fall migration in Missoula, MT, USA in September
2004. Another five sparrows were captured in fall 2003 at Sunnyside, WA, USA
and used for other diet experiments until April 2004
(Cerasale and Guglielmo, 2006),
after which they were kept in an outdoor aviary in Missoula until our
experiment. All sparrows were thus exposed to natural light conditions for an
extended period before experiments and had completed feather molt and autumn
migration before entering the short-day photoperiod conditioning. Sparrows
were individually housed indoors in 38 cmx43 cmx 41 cm cages at
22°C for the duration of the study. Sparrows were weighed in the morning
before feeding every 2–3 days throughout the experiment. Ten sparrows
were aged as `hatch year' and the rest as `after hatch year' according to Pyle
(Pyle, 1997). Sex was
determined after the experiment by inspection of the gonads. Sparrows were fed
a diet of black oil sunflower seeds, and water was provided ad
libitum, with supplemental grit and vitamins offered weekly. This limited
diet ensured that sparrows on both treatments would have similar adipose
stores so that relative mobilization rates would be more easily comparable. A
nightlight (<1 lux) was provided to encourage nightly migratory behavior.
Experimental protocols were approved by the University of Montana
Institutional Animal Care and Use Committee and appropriate permits for
collection, export/import and possession were obtained from the US Fish and
Wildlife Service, Canadian Wildlife Service, and Montana State Department of
Fish Wildlife and Parks.
Photoperiod manipulation
All sparrows were initially kept on a short day light cycle (8 h:16 h L:D)
for 58 days to break photorefractoriness and simulate winter. Sparrows were
then randomly assigned to treatment groups of long days (migrant=MIG;
N=10; 16 h:8 h L:D) and short days (winter=WIN; N=7; 8 h:16
h L:D). All sparrows were then maintained for another 22–26 days before
experiments were initiated. This manipulation of the light cycle in MIG
sparrows induced zugunruhe, a captive analog of the migratory condition in
which birds undergo nightly hopping and wing fluttering
(Breuner et al., 1999;
King and Farner, 1963). As
evidence of this, nightly hopping activity, as measured by counters attached
to the perches, was significantly elevated in the MIG sparrows compared to WIN
sparrows (P<0.05).
Adipocyte incubation and fatty acid analysis
The protocol for determining relative mobilization from adipocytes
generally followed that described by Raclot and Groscolas
(Raclot and Groscolas, 1993).
Birds were euthanized between 10.00 h and 14.30 h (2–6.5 h after lights
on) by pentabarbitol overdose. Approximately 400 mg adipose tissue was removed
immediately from the claviculo-corocoid depot and placed in Krebs Ringer
buffer (made with 15 mmol l–1 NaHCO3, 3.32 mmol
l–1 CaCl2 and 4% fatty-acid-free bovine serum
albumen; Sigma, St Louis MO, USA) (KRBA/BSA). Tissue was minced with scissors
and washed with KRBA/BSA three times. Washed tissue was then transferred to a
polypropylene flask containing 4 ml fresh KRBA/BSA warmed to 37°C. We
added epinephrine (Sigma) to a final concentration of 100 µmol
l–1, and the flask was flushed with 95%/5%
O2/CO2 and capped. The flask was incubated for 90 min at
37°C in a shaking water bath. The contents were then filtered under vacuum
with a glass microfiber filter (cat # 28297-978; VWR, West Chester, PA, USA).
A sample of this filtrate was taken for glycerol analysis (described below).
We added heptadecanoic acid (17:0; 200 µl 1.107 mmol l–1
hexane) as an internal standard. Three 1 ml aliquots of the incubation medium
were each added to vials containing 15 ml chloroform:methanol (1:1 v/v) and
shaken vigorously. For analysis of adipose lipids, 5–10 mg of
subcutaneous adipose tissue was removed from the claviculo-corocoid depot,
added to 15 ml chloroform:methanol (1:1 v/v) and homogenized at high speed for
3x10 s with a 1 cm generator (Polytron). Total lipid extracts from
incubation medium and from adipocytes were then centrifuged for 15 min at 2056
g and filtered (Whatman no. 1), adding 10 ml of
chloroform:methanol (2:1 v/v) to rinse. We added 6 ml 0.25% KCl to partition
and remove aqueous solutes. The aqueous layer was vacuum pipetted off and the
organic solvent was evaporated (Rotovapor, Buchi, Flawil, Switzerland). Lipids
were resuspended in 100 µl chloroform for loading onto Supelclean
solid-phase extraction tubes (LC-NH2; 100 mg; Supelco, Bellefonte, PA, USA).
Neutral lipids (NL, primarily TRIG) were eluted with 1.8 ml
chloroform:isopropanol (2:1 v/v). Non-esterified fatty acids (NEFA) were then
eluted with 1.6 ml isopropyl ether:acetic acid (49:1 v/v). Columns were washed
between samples with hexane and methanol. We added the internal standard
(17:0; 200 µl 1.107 mmol l–1 hexane) to the adipocyte NL
fraction and then evaporated each lipid fraction to dryness under
N2. NEFA were methylated at room temperature for 30 min following
addition of 100 µl methanol, 1 ml dimethoxypropane and 40 µl
concentrated HCl. The sample was dried under N2 and resuspended in
40 µl isooctane before injection in the gas chromatograph (GC) column. The
NL fraction was transesterified with 2 ml acetyl chloride in methanol (1 mol
l–1), heated for 2 h at 90°C. The solvent was evaporated
under N2, and fatty acid esters were resuspended in 60 µl
isooctane for injection onto the GC column.
Fatty acids were separated on a Hewlett Packard HP 6890 (Hewlett Packard, Palo Alto, CA, USA) with a J&W scientific high-resolution gas chromatography column (DB-225 ms; Agilent Technologies, Palo Alto, CA, USA) and flame ionization detector. The carrier gas was N2. The temperature program was 2 min at 120°C, then increase at 5°C per min for 16 min, hold at 200°C for 5 min, increase at 5°C per min for 4 min, then hold at 220°C for 13 min. Fatty acids with fewer than 16 carbons were excluded from statistical analysis because precautions to minimize volatization were not taken. Only fatty acids constituting more than 0.25% of the total neutral lipids in adipose tissue were considered in the analysis. The identities of fatty acids were determined by comparison of retention times to those of standard mixtures of fatty acid methyl esters (Supelco 37 component mix, Supelco PUFA No. 3; Sigma).
Glycerol concentration was measured in the medium after adipose incubation as a measure of overall lipolysis rate. Glycerol was assayed on a microplate spectrophotometer (BioTek Powerwave X340; Winooski, VT, USA) in 400 µl flat-bottomed microplates with an endpoint assay (Sigma; Trinder reagent A, 5 µl medium, 300 µl reagent). Glycerol is reported as (concentration in medium)/(mass of adipose incubated).
Statistical analysis
For each bird, relative mobilization for each fatty acid was calculated as
(mass % in NEFA from the incubation)/(mass % in NL from adipose). Only fatty
acids that were detected in both NL and NEFA were included in the analysis
(infinite and zero relative mobilizations were excluded). The 18:1n9 and
18:2n6 chromatograph peaks were inseparable in one WIN sparrow's adipose NL.
These fatty acids were removed from analysis for this animal.
In comparing the relative mobilization rates of different fatty acid species, normal statistical approaches are inappropriate due to the non-independence of data. For our analyses, we used a permutation approach aided by scripts written in S-Plus (Insightful Corp., Seattle, WA, USA). To test for a general effect of chain length, we measured a least-squares regression `observed slope' of relative mobilization vs chain length on the relative mobilizations of all fatty acids for all individuals. We then performed a random permutation of the relative mobilizations within an individual and within a degree of unsaturation (i.e. the relative mobilizations for 16:0 and 18:0 were permuted for each animal, the relative mobilizations for 16:1, 18:1 and 20:1 were permuted for each animal, etc.). A new slope was determined for all the permuted data. This process was repeated 1000 times to obtain a distribution of slopes. We considered chain length to have a significant effect if the observed slope was as or more extreme than the most extreme 5% (two-sided) of the slopes in the permuted distribution. A similar process was conducted for analyzing the effect of degree of unsaturation (# of double bonds), permuting within individual and within a given chain length. While we recognize that the effects of these factors may not be linear and that these slopes may not have biological meaning, these tests give a general indication of the effects of chain length and unsaturation on relative mobilization.
To compare mobilization rates of two different fatty acids, we performed a standard permutation test. To evaluate the effects of sex, age and photoperiod on the relative mobilization of a particular fatty acid and glycerol we used Mann–Whitney tests. Results are presented as means ± s.e.m.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Treatment did not have a significant effect on glycerol concentration (P=0.070) although there was a trend towards higher glycerol in migrant birds (Fig. 4). Neither age (P=0.536) nor sex (P=0.601) had significant effects on glycerol concentration. The ratio of moles fatty acids released to moles glycerol was 2.28:1.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), as well as
in vivo measurements from fasting penguins
(Groscolas, 1990). Although we
have not studied subcellular processes such as hydrolysis of TRIG by HSL, this
agreement generally suggests that the biochemical processes that result in
selective mobilization of fatty acids are similar between mammals and birds.
These mechanisms may include specificity of HSL for certain TRIG-bound fatty
acids as well as access of HSL to more polar fatty acids at the lipid droplet
interface (Hazel and Sidell,
2004; Raclot,
2003).
We used a photoperiodic manipulation to investigate the effects of
migratory state on relative mobilization rates in sparrows. Our results
indicate that the patterns of mobilization rates of individual fatty acids
relative to the overall mobilization rate do not vary with migratory state.
While we did not find a significant effect of migratory state on overall
lipolysis rates, the trend we observed can fuel further hypotheses.
Specifically, it appears that migratory state may alter adipose tissue such
that it responds more strongly to stimulation by epinephrine. Similar results
were found in Junco hyemalis
(Savard et al., 1991). This
could occur by an increase in receptor density
(Breuner et al., 2003;
Landys et al., 2004a).
Additional findings include the observation that 18:2n6 was not selectively
retained in the birds, contrary to the predictions of Mostafa et al. based on
work in a congeneric species (Mostafa et
al., 1994). Interestingly, young sparrows mobilized 18:0 at higher
relative rates than their older counterparts, although the importance of this
finding is unknown.
Traditional use of photoperiod-manipulated captive birds as models for
migration in endocrinology and orientation studies have relied on zugunruhe as
evidence for migratory condition (Able and
Cherry, 1986; Landys et al.,
2004b). Data on bird zugunruhe indicate that the MIG sparrows did
respond to the photoperiodic treatment by increasing nightly activity. This
treatment may not, however, perfectly mimic the biochemical changes that occur
in adipocytes during true migration. Using a captive protocol, however,
provides the opportunity to study birds with very similar adipose stores by
controlling diet. Additionally, it is possible that no change in relative
mobilization was observed with migration due to the limited number of fatty
acids available in abundance for this experiment, although this limited fatty
acid composition may be typical for wild passerines
(Blem, 1976;
Conway et al., 1994). Further
experiments could evaluate relative mobilization rates in free-living migrants
across seasons, particularly in shorebirds that eat a varied diet and whose
adipose depots would be expected to have a variable fatty acid
composition.
Selective mobilization and seasonal changes in energetic demand
Several investigators have studied changes in adipose tissue fatty acid
composition under conditions of fasting, nutritional stress and/or hibernation
(Falkenstein et al., 2001;
Florant et al., 1990;
Groscolas, 1990;
Nieminen et al., 2006;
Soppela and Nieminen, 2002).
When selective mobilization of fatty acids has been observed, it has often
been interpreted as adaptive (for example to maintain metabolism and functions
of essential PUFA or to maintain fluidity of fat reserves)
(Falkenstein et al., 2001;
Nieminen et al., 2006;
Soppela and Nieminen, 2002).
Given the apparent ubiquity and consistency in the pattern of selective
mobilization of fatty acids (Groscolas,
1990; Groscolas and Herzberg,
1997; Hazel and Sidell,
2004; Raclot,
2003; Raclot et al.,
1995) (present study), we recommend that such interpretations
should be made in light of `background' selective mobilization. For example,
Soppela and Nieminen (Soppela and
Nieminen, 2002) infer functional importance from the observation
that 18:2n6 was highly mobilized from malnourished reindeer, but high
mobilization should not be unexpected because, in general, 18:2n6 is
preferentially mobilized relative to the other fatty acids that make up
reindeer TRIG. On the other hand, the selective retention of 18:2n6 in
hibernating marmots (Florant et al.,
1990) and hibernating echidnas
(Falkenstein et al., 2001) is
notable as it demonstrates an exception to the general pattern. Valuable
information about lipid metabolism might be gained from these and other
species by comparing in vitro selective mobilization from adipocytes
excised at different stages of the animals' life histories.
Importance of selective mobilization to migratory birds
Because birds use extramuscular lipids as their primary fuel during
migratory flights (McWilliams et al.,
2004), the composition of stored fats has long been of interest to
physiologists. A particular focus has been on the amount of unsaturated fats
stored (Conway et al., 1994;
Egeler and Williams, 2000;
Johnston, 1973;
Yom-Tov and Tietz, 1978).
Although unsaturated fats are less energy dense than saturates, this energetic
difference is relatively small (Bower and
Helms, 1968), and whole-organism oxidation rates of unsaturates
are higher than those of saturated fats in fed rats
(Leyton et al., 1987). Thus,
it might be advantageous for birds to store unsaturated fats because they are
more easily transported from adipose stores to the muscle during energetically
demanding flights. Johnston observed that migratory species tend to have more
unsaturated fatty acids in adipose stores than non-migratory birds
(Johnston, 1973), although
Blem found no trend in saturation for migratory and non-migratory birds
(Blem, 1976;
Blem, 1980). Additionally, some
researchers have noted a change in fatty acid composition leading up to
migration, although this observation has not been consistent
(Egeler and Williams, 2000;
Hicks, 1967;
McGreal and Farner, 1956) and
does not seem to be the direct result of selective metabolism
(Pierce and McWilliams, 2005).
Many authors have noted that adipose fatty acid composition tends to reflect
dietary composition, and changes in bird diets leading up to migration can
alter adipose stores (Bower and Helms,
1968; Conway et al.,
1994; Egeler and Williams,
2000; Morton and Liebman,
1974; Pierce and McWilliams,
2005; West and Meng,
1968). Experiments with sandpipers have indicated that diet is not
solely responsible for changes to increased adipose unsaturation leading up to
migration but that endogenous modification, preferential deposition and de
novo synthesis can increase adipose unsaturation prior to and during
migration (Egeler and Williams,
2000; Egeler et al.,
2000; Egeler et al.,
2003).
During a migratory flight, the utilization rate for fatty acids will depend
on four processes: the rates of (1) mobilization from adipocyte, (2) transport
through the blood, (3) uptake at the muscles and (4) intracellular oxidation
(Egeler and Williams, 2000).
Despite the importance of fat utilization to avian flight, none of these
processes has previously been studied in migratory birds with respect to fatty
acid composition. Leyton et al. have often been cited as reporting that
oxidation rates of unsaturated fatty acids are high
(Leyton et al., 1987).
However, their study reported rates of whole-organism oxidation from fed rats
and therefore their results could be due to preferential deposition of
saturated dietary fatty acids rather than selective transport, uptake and
oxidation of unsaturates. As such, their results may not be easily comparable
to the process of fat utilization in fasting, migrating birds. Our results
indicate that mobilization of fatty acids from adipocytes is generally more
rapid for more highly unsaturated fatty acids (as well as for shorter fatty
acids). This could have adaptive significance for the preferential storage of
unsaturated fatty acids, but only if adipose mobilization is limiting [which
does not appear to be the case (McWilliams
et al., 2004)] or may be limiting under certain conditions [e.g.
increased energetic demands due to adverse weather
(Conway et al., 1994)]. Other
processes may limit the supply of fats to fuel migratory flight, although it
seems likely that unsaturated fatty acids would also be transported and
utilized more quickly in these processes, due to their greater solubility in
water. Additionally, the preferential mobilization of unsaturated fatty acids
compared to saturates may not indicate substantially increased rates of
overall lipolysis. Our results indicate a trend towards increased lipolysis in
migratory-stage birds without a change in the pattern of selective
mobilization of fatty acids.
Although many researchers have speculated that the higher mobility of
unsaturated fatty acids is beneficial to migratory performance, Pierce et al.
found that very high concentrations of dietary and adipose 18:1 and total
unsaturates resulted in poorer exercise performance in captive vireos
(Pierce et al., 2005).
Conversely, vireos with higher dietary 18:2n6 had improved performance. This
finding has been replicated in rats (Ayre
and Hulbert, 1997) and fish
(McKenzie et al., 1998) and
may be due to diet-influenced changes in phospholipid fatty acid composition
(Ayre and Hulbert, 1997;
Guglielmo et al., 2002b).
Thus, the composition of adipose stores may not be the only mechanism by which
dietary lipids can affect performance. The relative importance of dietary,
adipose and phospholipid fatty acid composition to performance in migratory
birds deserves further study.
LIST OF ABBREVIATIONS
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Acknowledgments |
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Footnotes |
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