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APPETITE, OBESITY AND METABOLISM
Centre d'Ecologie et Physiologie Energétiques, Centre National de la Recherche Scientifique, 67087 Strasbourg, France
Submitted 26 February 2003 ; accepted in final form 1 May 2003
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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-hydroxybutyrate (-OHB). In
SB, glucose infusion induced an 
2.5-fold decrease in lipolytic fluxes and
a large decrease in FA oxidation, as reflected by a 64% decrease in the plasma
concentration of -OHB. There were also a 35% decrease in plasma TAG, a
6.5- and 2.8-fold decrease in plasma glucagon and corticosterone,
respectively, and a threefold increase in insulinemia. These data show that in
fasting king penguins, glucose regulates lipid metabolism (inhibition of
lipolysis and/or of FA oxidation) and affects hormonal status differently in
stressed vs. nonstressed individuals. The results also suggest that in birds,
as in humans, the availability of glucose, not of FA, is an important
determinant of the substrate mix (glucose vs. FA) that is oxidized for energy
production. lipolytic fluxes; fatty acid oxidation; stress; isotopic tracers; seabirds
Almost all our knowledge on in vivo glucose-FA interactions comes from studies in humans. How the substrate metabolism is controlled and what the importance of glucose availability is in this control in other vertebrates, especially birds, is poorly understood. Moreover, no study has examined the metabolic interactions between glucose and FA during prolonged fasting when the metabolic rate is sustained mainly by FA oxidation. Under these circumstances, chances of observing an effect of glucose on FA metabolism are maximized and the interindividual variability of carbohydrate and protein metabolism is minimized. Such a physiological situation can be mimicked using restricted-carbohydrate, high-fat diets or lipid emulsions (24). However, this condition is encountered naturally in wild birds and mammals that spontaneously fast during their annual cycle. Among them are penguins (Spheniciforms), seabirds living in the antarctic and subantarctic regions. Penguins feed exclusively at sea and must fast on land for a period of up to 4 mo during breeding (16). Their fasting physiology is well-defined and is representative of that of other birds (10) and to some extent of mammals (9). Penguins adjust to prolonged fasting by mobilizing their fat stores, with about 90–96% of energy production coming from lipid oxidation while body proteins are spared (phase II of fasting) (10, 16). Thanks to their large body size and their tameness, penguins offer the opportunity of conducting in vivo metabolic studies in wild animals. For example, the king penguin (Aptenodytes patagonicus) is the only bird on which lipolytic fluxes have been measured in vivo under field conditions in different fasting situations (2, 3). Recently, we have suggested that in this bird, including during phase III of fasting, hormonal adjustments are oriented toward maintenance of glycemia rather than FA delivery (5). This could suggest that in penguins glucose has a central place in fuel utilization.
Here we examine whether glucose is an important regulator of lipid metabolism in spontaneously fasting king penguins. The in vivo lipolytic, metabolic, and hormonal responses to infusion of glucose were investigated under field conditions during phase II of fasting. Lipolytic fluxes [rate of appearance (Ra) of nonesterified FA (NEFA) and of glycerol] were measured using tracer methodology before, during, and after a 2-h glucose infusion. Due to an unusual and unpredictable human activity in their vicinity, half of the birds were exposed to noise and were stressed at the time of the infusion experiment (see RESULTS and DISCUSSION). This gave us the opportunity of comparing the effect of glucose on lipid metabolism in two fasting situations where birds had the same energy reserves but different hormonal and metabolic statuses.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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25-day breeding
fast and after having been fasting ashore for 1–3 days. Their average
body mass (BM) at capture was 12.81 ± 0.15 kg. One bird was caught
every other day and then kept in an outdoor fenced area (3 x 3 m) next
to the colony under natural climatic conditions and within its thermoneutral
range. They were habituated to captivity for 6 days, a time period known to be
sufficient to suppress the confinement stress in penguins
(19). Given that infusion
experiments were also performed every other day and begun 6 days after
penning, throughout most of the study three birds were simultaneously present
in the habituation pen. Because at capture birds had been fasting ashore for
1–3 days, the fasting duration at the time of the infusion experiment
was 8 days, which is more than the 2- to 3-day duration of the transition
from the fed state to phase II reported for this species
(11). BM at the infusion
experiment (11.5 kg, see RESULTS) was similar to that of
free-living male king penguins at the onset of the first incubation shift,
i.e., after about 8–10 days of fasting
(31). It was also 2.0 kg
higher than the 9.5- to 10-kg BM measured at the phase II-phase III transition
in breeding-fasting king penguins
(8,
11). Thus penguins at the time
of the infusion experiment were in the phase II fasting status, which is
characterized by a high contribution of lipids to energy production and body
protein sparing (16). Over the 3-wk period of infusion experiments, the climatic conditions remained unchanged (air temperature 10–15°C, limited rainfalls, no storms). However, due to an unusual and unpredictable human activity in the vicinity of the fenced area on some days and throughout the whole study, it randomly occurred that 5 of the 10 animals were infused under noisy conditions (engines working at a 20-m distance, from 1–2 h before the beginning of the infusion experiment until its end). Other birds were infused under very quiet conditions. Although there was no direct human perturbation, not even visual contact, and although infused penguins behaved similarly in the two conditions, the measurement of basal plasma levels of hormone and metabolites (see RESULTS) showed that birds exposed to noise were stressed. Thus penguins in this study were separated into two groups (n = 5 per group): nonstressed birds (NSB, quiet environment) and stressed birds (SB, noisy environment).
Catheterization and experimental setup. The infusion experiment on a bird lasted a total of 8 h and was separated into basal condition (3 h of tracer infusion without glucose), glucose infusion (2 h of tracer plus glucose infusion), and postglucose period (3 h of tracer infusion without glucose). On the day before the infusion experiment, the unanesthetized bird was cannulated with a polyethylene catheter (50-mm long; 1.1-mm OD) inserted percutaneously into the marginal vein of each flipper and extended with a 2-m-long section of tubing. Catheters were kept patent by infusion of saline (12 ml/day) using a small peristaltic pump. Catheterization of an artery for blood sampling for lipolytic flux measurements could not be adequately performed in field conditions. We assumed that any particular metabolism of the flipper (essentially feathers, bones, and tendons) is low and that the flipper venous blood reflects whole body metabolism. After catheterization, the birds were allowed to habituate to the experimental setup for 24 h. This setup was installed in a fenced area adjoining the habituation one and consisted of a small wooden pen (70 x 70 cm) with one wall high enough to prevent us from being seen by the bird. Catheter extensions were placed into a balance lever system to avoid damage to the extensions or removal of catheters. It also allowed the bird to move freely (a few steps) inside the pen and even to lay on its belly or sleep with the bill under the shoulder, as was regularly observed during tracer infusion. The free ends of catheter extensions were brought outside the pen to allow intravenous infusion of isotopic tracers and glucose into one flipper and blood sampling from the other one, from a distance, without disturbing the animal. Once the animal was in the experimental setup, particular care was taken to avoid any further intervention. On the day after the infusion experiment, the equipment was removed, and the penguins were weighed, marked on the chest with nyanzol dye to allow resighting, and released in the colony next to the beach. All the birds used in the study were resighted the following weeks, caught, and weighed. All had restored their BM, which indicates that they had been successfully feeding at sea and that the experiments had no impact on their health.
Infusion protocol and preparation of the infusates. At 0900, a
primed constant-rate infusion of labeled glycerol and palmitate was started
using a calibrated syringe pump and continued for 8 h (see above). The tracer
infusate was prepared daily as described by Wolfe
(48) and Turcotte et al.
(44) using
[2-3H]glycerol (Amersham, 40.7 GBq/mmol) and
[1-14C]palmitate (Amersham, 2.04 GBq/mmol). Delipidated bovine
serum albumin (catalog no. A-3803, Sigma) was used as the palmitate carrier.
Maybe penguin plasma would have been a more suitable carrier, but under our
field conditions we were not confident in preparing plasma with the required
sterility. Palmitate is one of the most commonly used FA for measuring NEFA
kinetics in mammals: it is the second most abundant NEFA and shows low
interindividual variability in its percent contribution to NEFA. The same was
observed here for king penguins, and we have determined previously that using
palmitate to measure NEFA kinetics in penguins gives realistic estimates of
Ra NEFA (2). Even if
the absolute Ra values obtained with the methodology used cannot be
fully ascertained, it is likely that the relative changes of Ra on
which this study was partly based were correctly determined. Infusion rates of
[2-3H]glycerol and [1-14C]palmitate were 215,000
± 4,000 and 116,000 ± 4,000
dpm·kg-1·min-1,
respectively (n = 10), which corresponded to trace amounts of
<0.002% of basal Ra glycerol and <0.03% of basal
Ra palmitate. Glucose dissolved in sterile saline was infused at 5
mg·kg-1·min-1 using
a calibrated syringe pump and the same catheter as for tracers. This dose was
determined from preliminary trials as inducing an 2-fold increase in
plasma glucose, the maximum glycemia reached (24 mmol/l) being close to
the highest glycemia (28 mmol/l) measured in fasting penguins
(19). Dead volume of the
infusion catheter (2.3 ml) and the infusion rate were taken into account to
determine the exact time at which glucose infusion actually begun and
ended.
Based on data from a previous study (2), a delay of 135 min separated the beginning of the tracer infusion and the first blood sampling to ensure that a steady state had been reached. Blood samples were taken every 15 min (basal period) and then every 30 min, except during the two last hours when blood was obtained on an hourly basis. Five milliliters of blood was collected at each sampling time, with EDTA used as an anticoagulant. After blood sampling the catheter was flushed with a volume of saline equal to sample volume plus dead volume of the catheter. Saline remaining in the catheter was withdrawn at the onset of the next sampling. Immediately after sampling, the blood was centrifuged and the plasma separated and stored at -20°C until analysis.
Determination of glycerol and palmitate specific activities. Plasma glycerol and NEFA specific activities were determined as previously described (3, 4). A 1-ml aliquot of plasma was mixed with chloroform-methanol (2:1, vol/vol). After extraction and evaporation, an aqueous and an organic extract were obtained and resuspended in ethanol-water (1:1, vol/vol) and hexane-isopropanol (3:2, vol/vol), respectively. A volume of aqueous extract equivalent to 300 µl of plasma was used to determine the glycerol concentration. It was dried under nitrogen and resuspended in hydrazine buffer. Glycerol concentration was measured enzymatically. Total tritium activity was counted on another aliquot of aqueous extract equivalent to 150 µl of plasma using scintillation fluid (Ecoscint A, National Diagnostics) and a Wallac 1409 counter. At this step of analysis, tritium activity is found only in glycerol and glucose. The percent activity in glycerol was obtained by separating glycerol from glucose using thin-layer chromatography with chloroform-methanol (40:24, vol/vol) as the developing solvent. The glycerol and glucose fractions were resuspended in scintillation fluid for counting. The specific activity of glycerol was calculated as total tritium activity times the fraction of activity in glycerol divided by glycerol concentration.
Total NEFA concentration was measured on 10 µl of plasma with an analytic test kit (NEFA C, Wako Chemicals). Palmitate concentration was obtained by multiplying NEFA concentration by the fractional contribution of palmitate to total NEFA, as determined by gas-liquid chromatography. Briefly, an aliquot of the lipid extract was separated by thin-layer chromatography using hexane-diethyl ether-acetic acid (70:30:1, vol/vol/vol) as the developing solvent. The NEFA fraction was isolated and converted to methyl esters using 14% boron trifluoride in methanol. FA methyl esters were separated and quantified using a gas chromatograph (Chrompack CP 9001) equipped with a capillary column (AT-WAX) and a flame ionization detector. The total 14C activity was counted on an aliquot of the organic extract, and its distribution in plasma lipids [triacylglycerols (TAG), diacylglycerols, NEFA, and phospholipids] was determined after separation of lipids by thin-layer chromatography as described above. Each fraction was resuspended in ethanol-water (1:1, vol/vol) and counted in scintillation fluid (Ecoscint A). Because no 14C is incorporated in FA other than palmitate, palmitate activity was calculated by multiplying total 14C activity found in the lipid extract by the fraction of activity in NEFA. Palmitate activity divided by palmitate concentration yielded palmitate specific activity.
Other metabolites and hormones. Plasma glucose and
-hydroxybutyrate (-OHB) levels were determined on deproteinized
plasma by enzymatic methods (Test-Combination, Boehringer-Mannheim). TAG
levels were estimated by enzymatic colorimetric methods using a commercial kit
(Peridochrom triglycerides GPO-PAP, Boehringer-Mannheim). Radioimmunoassay was
used to measure plasma glucagon (GL-32K kit, Linco), insulin (insulin-CT kit,
CIS bio international), and corticosterone (DA 200T kit, ICN). All
measurements were made in the same run, and the intra-assay coefficient of
variation was 5–8%, depending on the hormone. Hormones were measured at
the end of each infusion period (basal, glucose, postglucose).
Calculations and statistics. During the basal period, physiological and isotopic steady states were maintained. Glycerol and palmitate Ra were therefore calculated with the steady-state equation of Steele (40): Ra = tracer infusion rate (dpm/min)/specific activity (dpm/mmol). After glucose infusion, the isotopic steady state was not significantly disrupted, but significant changes in plasma glycerol and palmitate concentrations were observed. In this case, the Ra and the rate of disappearance (Rd) of glycerol and palmitate were calculated using the non-steady-state equations of Steele (40). Because the distribution volume of glycerol and palmitate is unknown in penguins, calculations were made using the various values reported for mammals. Irrespective of the distribution volume (150–325 ml/kg for glycerol, 40–50 ml/kg for palmitate), at all times of the infusion experiment Ra and Rd were not significantly different from each other or from flux rate values (Rt) calculated using the steady-state equation (P < 0.05). Consequently, all fluxes are presented as Ra calculated with the steady-state equation and expressed per unit BM. Ra NEFA was determined by dividing Ra palmitate by the fractional contribution of palmitate to total NEFA. This contribution did not change significantly during the infusion experiment (P < 0.49) and averaged 20.5 ± 0.7%. Ra and Rd were compared with the Wilcoxon signed rank test. The identity of Ra and Rt was determined by verifying that the slope of the linear regression between them was not statistically different from unity, as according to Tomassone et al. (41). Statistical differences of means between the two groups were assessed using the unpaired Student's t-test. Statistical significance of changes induced by glucose infusion was assessed using two-way ANOVA with time and penguins as the main factors. When populations were not normal or homoscedastic, the Mann-Whitney ranked-sum test or Kruskal-Wallis ANOVA on ranks were used. When significant changes were detected with ANOVA, the Student-Newman-Keuls method was used to determine which means were different from basal values. Values are means ± SE. The criterion of significance was P < 0.05.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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-OHB (see
Fig. 4A), TAG (see
Fig. 4B), and insulin
(Table 1) levels were not
significantly different between the two groups.
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Response to glucose infusion. In the two groups, glucose infusion
resulted in a comparable 2-fold progressive increase in plasma glucose
(P < 0.001) followed by a partial and significant (P <
0.05) return toward basal levels postglucose
(Fig. 1). During and after
glucose infusion, glycemia was not significantly different between the two
groups (P < 0.09). In NSB, the plasma concentration and
Ra of glycerol and NEFA were not affected by glucose infusion
(P < 0.16; Figs. 2
and 3). Throughout the infusion
experiment, they averaged 0.06 ± 0.01 and 0.62 ± 0.02 mmol/l for
the concentration of glycerol and NEFA, respectively, and 6.85 ± 0.58
and 15.24 ± 0.45
µmol·kg-1·min-1
for the Ra of glycerol and NEFA, respectively. In SB, glucose
infusion decreased plasma concentration and Ra of glycerol and NEFA
by 2.5-fold (P < 0.001). This effect was significant and
maximum as soon as 30 min after the beginning of glucose infusion, when the
plasma glucose level (14.67 ± 0.65 mmol/l) was only slightly higher
than basal glycemia in NSB (P = 0.046). A tendency for a return
toward basal values was observed postglucose, although changes were not
significant. During glucose infusion and postglucose, the concentrations and
Ra of glycerol and NEFA were not significantly different between SB
and NSB (P < 0.07).
Glucose infusion induced a 25 and 64% decrease in plasma -OHB level
in NSB and SB, respectively (P < 0.001;
Fig. 4A). In both
groups, the lowest concentrations of -OHB were observed at the end of
glucose infusion when glycemia was at the highest, and postglucose.
Postglucose, the -OHB level was twice lower in SB than in NSB
(P < 0.001). The plasma TAG level was not affected by glucose
infusion in NSB (P < 0.05; Fig.
4B) but decreased by 35% in SB (P < 0.01),
reaching postglucose values 1.5 times lower than in NSB (P <
0.001).
In NSB, plasma corticosterone and insulin remained unchanged during glucose
infusion, the twofold decrease in plasma glucagon being nonsignificant
(P = 0.44), possibly due to the high variability in the basal state
(Table 1). In SB, glucose
infusion induced 2.8- and 6.5-fold decreases in plasma corticosterone and
glucagon, respectively, and an 3-fold increase in insulinemia (P
< 0.05). No further changes were observed postglucose (P <
0.05). At the end of the glucose infusion and postglucose, the plasma levels
of glucagon and insulin were similar in SB and NSB (P < 0.05),
that of corticosterone remaining higher in SB.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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Lipolytic response to glucose. In humans, glucose ingestion or intravenous infusion induces a drop in both lipolysis (Ra glycerol) and in the release of FA from adipose tissue (Ra NEFA). This antilipolytic effect was observed under basal physiological conditions (49), after an 84-h fast (23), under euinsulinemic clamp (6), and during exercise (12). Our results show that the lipolytic response to glucose in the king penguin depends on the metabolic and/or hormonal status of the animal. Glucose infused at 5 mg·kg-1·min-1 for 2 h had no antilipolytic effect under normal fasting conditions (NSB), whereas it decreased the plasma concentrations and Ra of glycerol and NEFA by more than 2 in SB. These parameters reached minimum values as soon as 30 min after the start of glucose infusion and tended to increase as glycemia decreased postglucose. This result supports the view that the decrease in lipolytic fluxes and plasma concentrations of glycerol and NEFA in SB was not due to a progressive attenuation of stress but to an antilipolytic effect of glucose. To date, lipolytic fluxes had never been measured in birds during glucose infusion. However, in agreement with our results in NSB penguins, glucose intravenous injection or an oral load was shown to have no effect on plasma NEFA in the domestic fowl (21) or the garden warbler (43) under various fasting situations. A decrease in plasma NEFA was observed by Totzke et al. (42) in fasted garden warbler, but the authors did not report if the animals were stressed or not.
In SB, glucose infusion resulted in a significant fall in Ra
glycerol, which reflects an inhibition of lipolysis. The fact that
Ra NEFA did not fall more than Ra glycerol indicates
that primary reesterification (the process where part of the NEFA released by
TAG hydrolysis is reesterified back to TAG before entering the circulation)
was not stimulated. Thus the decrease in NEFA availability in SB was only
related to a reduction of lipolysis. In contrast, in humans, glucose was shown
to decrease the mobilization of fat stores by both inhibiting lipolysis and
stimulating primary reesterification, this stimulation depending on the rate
of glucose infusion (49). It
is possible that larger doses of glucose would have stimulated primary
reesterification in stressed fasting king penguins. Because glucose had no
antilipolytic effect in NSB, the possibility that it inhibited lipolysis in SB
by acting directly on adipose tissue can be excluded. Instead, glucose action
may have been indirect through induction of hormonal or metabolic changes. In
humans, the lipolytic response to glucose infusion is predominantly mediated
by insulin (47). In birds,
insulin has no antilipolytic effect
(20) so that the decrease in
lipolytic fluxes observed in SB cannot be related to the 3 times increase
in plasma insulin level. Rather, the large decrease in plasma glucagon, and
perhaps also of corticosterone, that accompanied glucose infusion might
explain this antilipolytic effect. Indeed, glucagon is the main lipolytic
hormone in birds, including penguins
(17,
20). Its secretion was shown
to be inhibited by supplying exogenous glucose in chickens
(20). Corticosterone
stimulates lipid fuel mobilization in mammals
(34), but its role in the
regulation of lipid metabolism in birds in unclear
(38). The idea that the
antilipolytic effect of glucose observed in SB is mediated by the decrease in
plasma glucagon and corticosterone is supported by the observation that
glucose infusion does not affect either lipolytic fluxes or plasma levels of
these hormones in NSB penguins.
Effect of glucose on FA oxidation. Glucose infusion resulted in an
inhibition of ketogenesis and hepatic FA oxidation, as reflected by the 1.4-
and 2.5-fold decreases in plasma -OHB in NSB and SB, respectively. As
the plasma -OHB level is considered to be an index of FA oxidation in
fasting penguins (30), we
suggest that an increase of glucose availability inhibits (total) FA oxidation
in these birds. In NSB, this inhibition occurred whereas lipolysis and NEFA
availability remained at basal levels. In accordance with this finding, an
increase in the availability of glucose was shown to inhibit FA oxidation in
humans, despite the maintenance of FA availability by infusion of lipid and
heparin (37). Our results in
fasting king penguins thus support the idea that the availability of glucose,
not FAs, is a prime determinant of the substrate mix (glucose vs. fat) that is
oxidized for energy production
(37).
The finding that glucose inhibits FA oxidation, without significant changes
in the plasma levels of glucagon, corticosterone, and insulin, suggests that
it could act directly on FA oxidation in NSB. Accordingly, in humans, glucose
is thought to inhibit FA oxidation by restricting entrance of long-chain FA
into the mitochondria (33,
45). The larger decrease in
plasma -OHB in SB suggests that FA oxidation was inhibited to a larger
extent in these birds than in NSB. The metabolic and hormonal changes observed
in SB secondary to glucose infusion may have contributed to this greater
inhibition. Glucose infusion resulted in a threefold increase in plasma
insulin concentration. In mammals, this hormone is proposed to inhibit FA
oxidation throughout enzymatic cascades, leading either to a decreased rate of
entry of FA into mitochondria
(33) or to the inhibition of
enzymes of -oxidation
(35). The glucose-induced
decrease of the plasma glucagon also probably contributed to lower FA
oxidation in SB. In birds, glucagon stimulates FA oxidation and energy
expenditure, as illustrated by the finding that glucagon infusion caused a
1.5-fold increase in plasma -OHB level in long-term fasting king
penguins (5) and induced a 47%
rise in the metabolic rate of king penguin chicks
(1). FA oxidation and/or the
metabolic rate of SB birds may thus have decreased in response to the lowering
of the glucagon level induced by glucose. The observation in SB that the
plasma TAG level, which reflects hepatic reesterification, decreased in
parallel with plasma -OHB suggests that the decrease in hepatic FA
oxidation was related to a reduced supply of FA rather than to a reorientation
of NEFA toward reesterification. Thus the inhibition of lipolysis, mediated by
glucose-induced lowering of glucagon and corticosterone (see above), certainly
contributed to reduce FA oxidation in SB by decreasing NEFA availability
(Ra NEFA) for oxidative tissues. To sum up, in SB a decrease in
total fat oxidation during glucose infusion could be due to concerted
reductions in lipolysis, NEFA availability, and FA oxidation by tissues, this
response to glucose being direct or mediated by hormonal changes.
Glucose-lipid interactions in stress and fasting. A major finding of this study is that the regulation of metabolic fuel utilization by glucose is affected by stress. While in NSB glucose infusion induced only a moderate reduction in FA oxidation, in SB it induced an important decrease in lipolytic rate, FA oxidation, plasma TAG, glucagon, and corticosterone levels, and an increase in plasma insulin. Therefore it appears necessary to carefully consider whether animals are stressed or not in further field studies on fuel metabolism. It is well-known that the metabolic and hormonal changes observed during stress are directed at provisioning the body with metabolic fuels at a higher rate to face increased energy expenditure (34, 39). Since in phase II fasting birds and mammals, FAs derived from the hydrolysis of TAG stored in adipose tissue are the main fuel, it is likely that the increased lipolytic rate observed in SB during the basal period was aimed at fueling this high-energy need. Within 30 min after the onset of glucose infusion in SB, the lipolytic rate was markedly depressed, and this infusion induced a decrease in glucagon and corticosterone secretion. These observations demonstrate that during phase II of fasting the stress-induced metabolic and hormonal adjustments can be rapidly reversed by the supply of an alternative fuel.
In birds as in mammals, when a fast is prolonged until a lower threshold in fat stores is reached, animals enter a new fasting state (phase III) corresponding to a simultaneous acceleration in the catabolism of protein and a decrease in the contribution of lipid to energy production (15, 25, 32). In the king penguin, this shift is associated with an increase in lipolytic rate (2) and in the plasma levels of glucagon (2, 11) and corticosterone (11), as presently in the basal state of SB, while the resting metabolic rate expressed per kilogram of BM (10, 13) and plasma glucose (11) remain unchanged. These observations lead to the suggestion that the increase in lipolytic rate at the entrance into phase III could contribute to maintaining glycemia by providing glycerol (a gluconeogenic precursor) from TAG hydrolysis rather than supplying the body with more lipid fuels, as likely occurs in phase II fasting SB. Reaching the critical depletion of fat stores characterizing the entrance into phase III is a stressful (emergency) situation that has been observed in animals spontaneously fasting at certain stages of their annual cycle (7, 18, 30). Other stressful situations such as food shortage, bad weather conditions, predation, and anthropic disturbances can be encountered by wild animals (46). Present data for phase II fasting king penguins and previous findings for phase III suggest that the metabolic and hormonal way animals adjust to stress would depend on the type and/or amount of endogenous and/or exogenous fuel substrates available.
Perspectives
Using the king penguin as an animal model, this study shows that glucose is a factor regulating lipid metabolism in birds. Depending on the metabolic and hormonal status of the animals, glucose seems to control lipid metabolism through concerted variations of lipolysis, NEFA availability, and FA oxidation. These changes in lipid metabolism could be due to a direct action of glucose on FA oxidation or could be mediated by alterations of the levels of glucagon, corticosterone, and insulin, the main hormones regulating lipid and/or carbohydrate metabolism in birds. This study also suggests that, as in mammals, the availability of glucose, not of FAs, controls substrate metabolism in birds. This notion could help to explain the metabolic and hormonal changes related to stress, prolonged fasting, or other physiological situations in birds (migration, molt). Further support for this notion should arise from the determination of the relative importance of glucose and FA in energy metabolism under these diverse physiological situations. This requires the development of devices and methodologies that allow the measurement of substrate oxidation in field conditions in birds and more generally in wild animals.
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DISCLOSURES |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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, NSB; 
, SB. Values are means
± SE (n = 5 in each group). bSignificantly
different from basal values in SB, P < 0.05.
