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Am J Physiol Regul Integr Comp Physiol 279: R2104-R2112, 2000;
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Vol. 279, Issue 6, R2104-R2112, December 2000

Refeeding signal in fasting-incubating king penguins: changes in behavior and egg temperature

R. Groscolas, F. Decrock, M.-A. Thil, C. Fayolle, C. Boissery, and J.-P. Robin

Centre d'Ecologie et Physiologie Energétiques, Centre National de la Recherche Scientifique, 67087 Strasbourg Cedex, France


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

This study is directed toward understanding the process of feeding stimulation ("refeeding signal") that has been suggested to operate below a body mass threshold or critical metabolic status in spontaneously fasting birds. Behavior and egg temperature (Tegg) were continuously monitored by video monitoring and biotelemetry, respectively, in fasting-incubating king penguins kept in a pen to prevent relief by the partner until spontaneous egg abandonment. Penned birds fasted 10 days more and lost 1.2 kg more than birds relieved normally by their partner, abandoning the egg about 1 wk after reaching a critical body mass. Definitive egg abandonment was preceded by transitory abandonments of progressively increasing duration during which time the birds went further and further away from their egg. There were marked interindividual differences but on average transitory abandonments began 36 ± 5 h before the definitive abandonment and were paralleled by resumption of display songs signaling the readiness of the bird to depart for feeding. Tegg was maintained at around 35.7°C during normal incubation but significantly decreased the last 2 days before egg abandonment. These changes are interpreted as reflecting a stimulation to refeed at a threshold body mass corresponding to a critical fat store depletion. Thus the fasting-incubating king penguin appears to be an interesting animal model for understanding the long-term metabolic control of feeding behavior in relation to energy status.

feeding behavior; spontaneous fasting; incubation; fat stores; body mass threshold; birds


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

ENERGY EXPENDITURE AND ENERGY intake are the two components of the long-term regulation of body mass and principally of body fat. There is evidence that this regulation occurs mainly through the control of energy (food) intake (18, 30, 36). The control of food intake is at least partly based on metabolic signals for control of eating behavior (5, 7, 14, 16, 32). Indeed, for changes in energy stores to affect energy intake there must be a mechanism that translates alterations in energy metabolism into this behavior (14). The control of feeding behavior has been investigated mainly in laboratory mammals, which mostly furnishes information on the short-term control, for example meal onset and termination (19, 23, 25). Thus whereas a clear picture of this short-term control is progressively emerging, the long-term metabolic control of feeding behavior is still obscure (21).

A better understanding may come from consideration of the behavioral ecology of wild animals, including their reproductive (4) and feeding strategies. Notably, relevant information can be obtained from wild mammals and birds that show prolonged periods of spontaneous hyperphagia and fasting throughout their annual cycle (24). Recent findings suggest that some seabirds breeding in the antarctic and subantarctic regions, e.g., penguins and petrels, can be valuable animal models for studies in this field (9, 17, 22, 28). Because egg incubation on land competes with feeding at sea, these birds fast ashore for prolonged periods of up to 1 mo or more, relying on large fat stores as the main energy source (17). Parents alternate in incubating and depart to sea for refeeding after relief by the partner. However, the latter can be delayed, forcing the incubating bird to prolong its fast until eventually it abandons its egg and goes to sea for feeding (2, 9). This finding is in agreement with the previous observation that spontaneously fasting seabirds do not fast to death, which has led to the suggestion that a refeeding signal might trigger egg desertion and departure to sea to refeed (17, 22).

Recently, the concept of a refeeding signal has found support in behavioral and metabolic data that show a spontaneous increase in locomotor activity of captive fasting but nonincubating emperor penguins (Aptenodytes forsteri) below a body mass threshold corresponding to an increase in body protein catabolism (28). This was interpreted as reflecting an increase in the drive to refeed and has led to the hypothesis that a shift from the preferential use of body lipid to that of body protein would be the metabolic signal that triggers refeeding. However, whether this applies to incubating birds, where the drive to incubate may overcome that for refeeding, is unknown. It is conceivable that the behavioral changes that reflect the drive to refeed are not the same if the bird has to care for an egg or that even the triggering to refeed or its effects may be delayed to improve egg survival. This triggering of feeding during incubation has not been studied to date.

Behavioral changes are the visible manifestation of the endogenous metabolic and endocrine changes that trigger refeeding. Studying behavioral changes may therefore help to understand the mechanism(s) that control feeding. For example, a different mechanism might be expected if egg abandonment is the conclusion of progressive behavioral changes spread over a long period of time or whether it occurs suddenly. To improve our knowledge of the metabolic control of feeding behavior in an ecological context, the present study has therefore analyzed in detail the behavioral changes that could reflect the conflicting drives to refeed and to incubate below a threshold body mass in a fasting-incubating seabird, the king penguin (Aptenodytes patagonicus). This bird fasts for periods of up to 1 mo during breeding, and its reproduction behavior (8) and fasting physiology (11) are well documented. It is known that a significant proportion of breeders spontaneously abandon their egg because they have reached a low body mass (Gauthier-Clerc M, Le Maho Y, Gender J-P, Durant J, and Handrich Y, unpublished data). In the present work changes in behavior were examined in penned birds incubating under natural conditions by video monitoring and by continuous biotelemetry recording of egg temperature (Tegg), an index of egg attendance.


    MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

The study was conducted in the breeding colony of the Baie du Marin, Possession Island, Crozet Archipelago (46° 26' S, 51° 52' E, Indian Ocean) from November 1997 to March 1999. This colony close to the Alfred Faure Station contains about 30,000 pairs of king penguins.

Animals

King penguins are about 12-kg seabirds that breed in dense colonies. They lay only one egg (average mass 300 g, average size 105 × 75 mm) that males and females incubate alternately on their feet under the brood patch while fasting. Because of delayed relief by the partner (26) or premature energy reserve exhaustion, spontaneous egg abandonment is not a rare phenomenon. It affects up to 5% of breeders in years of reduced food availability (Gauthier-Clerc et al., unpublished data). However, because there is no nest and because incubating birds stand very close together, with more than one bird per square meter (8), the corresponding changes in incubation behavior cannot be conveniently monitored on a large sample of free-living birds. Thus this was done on incubating birds kept in a pen. A preliminary experiment demonstrated that incubating birds from the colony transported to a nearby pen with their egg continue to incubate. Interestingly, penned birds adopted the same behavior as in the wild. They stood close together, leaving most of the pen area free, and spent time battling and pecking to defend their small territory. They also displayed the same behavioral repertoire as free-living birds, with comfort activities (shaking, stretching, cleaning, preening, and egg shifting), sleeping with the bill under the flipper, and resting with the beak pointed forward (8). Besides allowing continuous behavior monitoring, penning prevented the relief of incubating birds, forcing them to extend their fast until spontaneous egg abandonment. A total of 25 birds were penned in small groups of five to eight birds to facilitate individual watching. To avoid possible difference in behavior between sexes and between the different incubation shifts within a sex only males during the first incubation shift were used in this study. The first incubation shift begins within hours after laying, when the female leaves her egg to her partner and goes to sea for refeeding.

Birds were penned under natural climatic conditions and photoperiod after having been freely incubating for 4 days, a duration indicating that they were experienced breeders and ensuring that they were strongly motivated to incubate. The pen (3 × 3 m width, 1.7 m height) was situated approximately 10 meters from the colony and made of wood so that the captive birds could not see other birds outside. The pen was covered with a net to prevent egg predation by skuas (Catharacta skua l.) and sheatbills (Chionis minor). At penning, birds were rapidly paint-marked on the chest to allow easy identification during video recording. The 10 birds used for Tegg records were also weighed to the nearest 20 g on a platform balance. The whole capture, transport, weighing, and marking procedure lasted about 3 min, the head of the bird being covered with a linen mask to reduce stress and agitation. Thereafter, birds were left undisturbed, and their behavior was continuously recorded by video monitoring. When a bird was observed to have abandoned its egg for 2 h, we assumed that the abandonment was definitive (see RESULTS) and the door of the pen was opened remotedly until the bird went outside spontaneously. It was caught for weighing to the nearest 20 g and released. Birds departed to sea for refeeding within the following 24 h and all came back in good health within the following weeks.

Analysis of Behavior

The behavior of captive, incubating birds was recorded day and night by using a video camera fixed on a pole 2.5 m above the pen and protected against bad weather. An automatically switched-on infrared light allowed nighttime recording. The camera was linked to a time-lapse videorecorder located in a nearby shelter, which registered one frame per second. A total of 530 days of video recording were obtained of the 25 birds studied. A review of the records showed that definitive egg abandonments were preceded by transitory abandonments. The time course of egg abandonment and the corresponding behavioral events were therefore determined and quantified using the following criteria: the time of the beginning of the egg abandonment sequence was taken as the time of the first transitory abandonment. The time and duration of other transitory abandons were determined, the transitory abandonments being classified into three categories according to the maximum distance between the bird and its egg: 1) category 1, egg very close to the feet; 2) category 2, egg 20 cm-1 m from the bird; and 3) category 3, egg more than 1 m from the bird. The underlying assumption is that the greater the time and distance from the egg, the lower the drive to incubate. The times when the birds sang or tried to escape were also noted. Birds were considered as wanting to escape when, having left the egg, they moved along the pen wall, sometimes pushing at it or trying to look outside. The time of definitive egg abandonment was taken as the end of the last incubation episode. The difference between the time of the first transitory abandonment and definitive abandonment yielded the total duration of egg abandonment. The total number and duration of transitory egg abandonments, the maximum duration of a transitory abandonment, and the total number of songs during egg abandonment were registered.

Tegg

Video recording allowed one to determine whether the egg was kept on the foot (incubated) or not. It did not indicate whether the egg was well warmed and thus well attended. To determine more precisely the changes in egg attendance and to obtain information on the normal pattern of egg incubation throughout the incubation shift, Tegg was continuously monitored for 10 of the 25 birds of the study. An Aktiv 500 telemetry system (Gesellschaft für Telemetriesysteme) that enables monitoring ten temperatures simultaneously (13) was used as previously described (2). Temperature transmitters (3-4 g), calibrated in a water bath before and after deployment, yielded pulses with a time interval inversely proportional to temperature, i.e., from 4.4 s to 1.1 s for a 0.0 to 42.5°C temperature range. Each egg was monitored for 30 s every 5 min to give one temperature value every 5 min calculated from about 15 pulses to 0.1°C. A total of 220 days of Tegg recording at this sampling frequency was obtained from the 10 birds studied. The transmitters were embedded in plaster dummy eggs with the same size, shape, mass, and color as king penguin eggs.

Two preliminary experiments were performed to determine the position of the transmitter in the dummy egg that allowed the best detection of changes of Tegg in relation to changes in egg attendance. The king penguin egg is not spherical but piriform and therefore could be nonhomogeneously warmed. In one experiment, a dummy egg was equipped simultaneously with five transmitters at five positions and exchanged with a true egg in two freely incubating birds. The five temperatures were recorded for 5 days for each bird, roughly during the middle part of an incubation shift. As illustrated in Fig. 1, temperature significantly differed (P < 0.0001) among the five positions, being higher and the more steady at the broad pole (36.5 ± 0.1°C) and the lower and more changing at the narrow pole (29.4 ± 0.8°C). In another experiment, we checked whether a transmitter at the broad pole could detect a change in Tegg induced by a short exposure to the outside, given that the telemetry system as applied in the field recorded only a single Tegg every 5 min. A 1-min exposure to 12°C (the average air temperature during the study) followed by rewarming at 37°C induced an immediate 1.7 ± 0.2°C fall in Tegg, with a slightly lower minimum value being reached 3.0 ± 0.8 min after the onset of cold exposure and being maintained for several minutes. Consequently, the transmitter was positioned peripherally at the broad pole throughout all the study because it 1) gave realistic Tegg (around 35-37°C), 2) was sensitive to a short absence from the egg, but 3) changed the least during normal incubation (low "background noise").


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  		Fig. 1.   Typical data of the 24-h changes in temperature at 5 positions inside a dummy egg incubated by a free-living king penguin. Transmitters were inserted peripherally at the broad and narrow poles of the egg, peripherally at opposite sides at the level of the larger diameter, and centrally.

Fasting Duration and Body Mass at Relief in Freely Incubating Birds

For comparison with penned birds forced to fast until egg abandonment, the duration of the first incubation shift and the body mass at relief were determined in 20 freely incubating males. They were marked on the first day of incubation, observed daily, caught, and weighed to the nearest 20 g within 1 h following relief.

Calculations and Statistics

The number and the time course of transitory egg abandonments differed markedly among individuals (see RESULTS). Consequently, the changes in the average duration of transitory egg abandonments and the average distance between birds and eggs throughout the egg abandonment process cannot be calculated meaningfully on a time basis. Instead, for each bird the total number of transitory abandonments was divided into quintiles in chronological order of occurrence, each quintile containing the same number of abandonments (see Fig. 3 legend).

Values are given as means ± SE. After normality of distribution and homogeneity of variance were checked, data for the duration of transitory abandonments and for the bird-egg distance during transitory abandonments were analyzed using one-way ANOVA with repeated measurements for the factor individual. Post hoc multiple comparisons were done with Tukey's test. Changes in Tegg with time were analyzed using one- (individuals) or two-way (time × individual, mean for the ten individuals) ANOVA followed by Dunnett's post hoc test to compare daily means to the plateau value. Least-squares linear regression analysis with the F test were performed for relationships between the various behavioral parameters and between these parameters and Tegg. Student's t-test was used for comparison of two means. In all cases the criterion of significance was P < 0.05.

Ethical Considerations

The penning of incubating king penguins until egg abandonment induced the loss of their eggs. Whereas the mortality due to our study was low compared with the thousands of eggs or chicks that die naturally every year in the colony (34), we nevertheless reduced the impact of the experiment by using only birds breeding in an unfavorable location where natural mortality is known to be close to 100% (e.g., area submitted to frequent flooding). The study was approved by the Ethical Committee of the "Institut Français pour la Recherche et la Technologie Polaires" and conformed to the "Agreed Measures for the Conservation of Antarctic and Subantarctic Fauna."


    RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

Duration of the Incubation Shift and Body Mass at the End of Fasting

In free-living birds, the duration of the incubation shift and the body mass at relief were 15.9 ± 0.3 days (12-21 days) and 10.02 ± 0.19 kg (9.65-11.28 kg), respectively (n = 20). In birds penned until egg abandonment, the duration of the incubation shift and the body mass at abandonment were, respectively, 10 days more (25.8 ± 1.5 days, 14-42 days) and 1.24 kg less (8.78 ± 0.16 kg, 7.44-10.51 kg) than for relieved birds (P < 0. 0001, n = 25). Body mass at penning ranged from 9.3 to 12.7 kg.

Behavior of Egg Abandonment

Normal incubation behavior was characterized by the birds' continuously keeping the egg on the feet, even if sometimes it was not entirely covered by the brood patch. This happened occasionally, for example, when a bird was making comfort movements (cleaning, stretching) or when it was specifically caring for the egg. Visual observations suggested that the cleaning, stretching, and moving activities tended to increase a few days before egg abandonment in some birds, but these observations were not consistent or confidently measurable. Leaving the egg transitorily unincubated on the ground very close to the feet and usually for only a few seconds was the first consistent behavioral sign indicating a decline in the drive to incubate. It was observed in all birds. Consequently, the analysis of abandonment behavior focused mainly on transitory egg abandonments. Songs and escape attempts were other major behavioral features characterizing egg abandonment.

Transitory egg abandonments. Although there were large interindividual differences in the timing and the number of transitory egg abandonments, a general pattern emerged, as illustrated in Fig. 2. Ninety percent (427/475) of transitory egg abandonments were diurnal events and 100% of definitive abandonments occurred during daytime. On average, each bird transitorily abandoned its egg 20.1 ± 2.6 times (range 2-76 times, n = 25) before definitive abandonment.


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  		Fig. 2.   Histogram showing the major behavioral features of egg abandonment and their timing in a typical king penguin. Time 0 corresponds to the first transitory abandonment. Each entry along the x-axis indicates an egg abandonment. The height of a spike indicates the maximum distance reached between the bird and its egg as scored into three categories (close to the feet, score 1; 20 cm-1 m, score 2; and >1 m, score 3). The width of a spike indicates the duration of the abandonment. Solid arrows show times of songs and the open arrow shows the time of the first attempt to escape. The upper horizontal black and white bars indicate nighttime and daytime, respectively. DEA, definitive egg abandonment.

The total duration of transitory abandonments and the maximum duration of one transitory abandonment were 60.2 ± 7.8 min (range 1-150 min, n = 25) and 15.3 ± 2.0 min (range 1-34 min, n = 25), respectively. The total duration of the egg abandonment process (from the first transitory to the definitive egg abandonment) averaged 36.0 ± 5.1 h (range 3.8-108 h, n = 25). Birds remained close to the egg during most (72%) of the transitory abandonments. However, as illustrated in Figs. 2 and 3, they tended to move farther away for longer durations as the successive abandonments continued. From the first to the last quintile of transitory abandonments (see Calculations and Statistics), the average duration of transitory abandonments progressively and significantly (P < 0.0001) increased by 10-fold (Fig. 3A). Similarly, the distance score by categories between the bird and the egg progressively and significantly (P < 0.0002) increased (Fig. 3B). A 20-cm to 1-m and >1-m distance was reached for the first time 19.4 ± 3.5 h (range 2.5-50.6 h) and 29.4 ± 4.9 h (range 3.2-95.4 h), respectively, after the first transitory abandonment.


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  		Fig. 3.   Changes in the duration of transitory abandonments (A) and in the distance reached between the bird and its egg (B) throughout successive transitory egg abandonments. Values (means ± SE, n = 10) not sharing the same superscript letter are significantly different, P < 0.05. Quintiles 1, 2, etc... represent the 1st, 2nd, etc... 5th of total transitory abandonments considered in their chronological order (see Calculations and Statistics). Only data from birds showing at least 15 transitory egg abandonments were used for these calculations. The individual value for each quintile is the mean of at least 3 measurements. Distance scores, see Fig. 2 and MATERIALS AND METHODS.

Songs. Almost all birds (n = 23) sang during the last days of incubation, on average 10.8 ± 2.0 times (1-40 times, see Fig. 2). One-half the birds (n = 13) sang for the first time before the first transitory egg abandonment (from 68.8 to 0.2 h before, average 21.2 ± 5.1 h), the others singing for the first time either during the abandonment process (n = 7) or after definitive abandonment (n = 3). On average, the first song occurred 2.0 ± 7.5 h (n = 23) before the first transitory abandonment.

Escape attempts. Almost all birds (n = 23) attempted to escape from the pen, 22 and 78% of the attempts being observed shortly before (6 h at the maximum) or after definitive egg abandonment, respectively (see Fig. 2). On average, escape attempts occurred for the first time 0.2 ± 0.6 h (n = 23) after definitive egg abandonment, all attempts being diurnal.

There were no significant relationships between the various parameters characterizing the behavior of egg abandonment (number, total and maximum duration of transitory abandonments, total duration of the abandonment process, number of songs and timing of the first song) on one hand and the body mass of birds at penning, the body mass at definitive egg abandonment, and the duration of the incubation shift on the other hand (0.07 < P < 0.83). The number and the timing of the songs also were unrelated to the number, total and maximum duration of transitory egg abandonments, and to the total duration of the abandonment process (0.08 < P < 0.87, n = 25).

Tegg During Normal Incubation and Abandonment

During the first days of incubation in the pen, Tegg showed pronounced fluctuations and tended overall to increase (not shown). Thereafter, it was maintained around a plateau level, individual changes as well as interindividual differences being blunted, as illustrated by the decrease in SE of Tegg (P < 0.01, n = 10; Fig. 4A). This was considered as characterizing the period of "normal" incubation behavior, the egg being continuously kept on the feet during this period. Tegg at plateau averaged 35.7 ± 0.4°C (n = 10) and was not significantly different during the day (35.7 ± 0.4°C) and night (35.5 ± 0.5°C) (Fig. 4B). Nevertheless, large interindividual differences in the pattern of Tegg were sometimes observed during normal incubation (Fig. 5). If Tegg remained high and steady for some birds most of the time (Fig. 5A), for others it showed random and brusque transitory falls of several degrees (Fig. 5B) or frequent slow and prolonged 4-5°C decreases (Fig. 5C). As a consequence, during normal incubation individual mean Tegg ranged from 33.0 ± 0.2 to 37.0 ± 0.0°C.


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  		Fig. 4.   Changes in the mean daily (A) and diurnal and nocturnal (B) egg temperature (Tegg) throughout the course of incubation. Values are means ± SE for 10 individuals with usually 288, 198, and 90 temperature readings per individual for the daily, diurnal, and nocturnal Tegg curves, respectively. Because of large individual differences in the duration of incubation shifts, only the last 15 days were considered. *Significantly different from the plateau value, P < 0.05.



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  		Fig. 5.   Changes in Tegg during the 15 days preceding egg abandonment in three king penguins. A: bird showing relatively steady Tegg. B: bird showing similar constancy in Tegg but with a few transitory drops. C: bird showing an unsteady Tegg. The upper horizontal black and white bars indicate nighttime and daytime, respectively. Arrows show the first transitory abandonment.

As illustrated in Fig. 6 for a representative bird the process of egg abandonment was characterized by frequent and large drops in Tegg. Most of the drops were diurnal and corresponded to periods of transitory egg abandonment, with a few others corresponding to periods of incomplete covering of the egg by the brood patch, especially during stretching and cleaning. Falls in Tegg tended to be greater and longer as the abandonment process advanced. Because transitory decreases in Tegg also occurred during normal incubation, it was usually impossible to determine which one represented the first decrease in egg attendance not related to a transitory abandonment. We attempted to determine this with three birds where Tegg remained remarkably steady for at least 5 days before the first transitory abandonment. The first decrease in Tegg and the first transitory egg abandonment occurred 47.4 ± 6.6 and 27.7 ± 5.5 h (n = 3) before definitive egg abandonment, respectively. This result suggests that a decrease in egg attendance in some birds can be detected from acute changes in Tegg about 1 day before the first transitory abandonment.


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  		Fig. 6.   Changes in Tegg during the days preceding definitive egg abandonment in a typical king penguin. Solid and open arrows show periods of transitory egg abandonment and defective egg covering, respectively, as determined by video recording. The horizontal black and white bars indicate nighttime and daytime, respectively.

A final progressive and significant decline in mean daily Tegg below the plateau level occurred with all birds, from 0 to 5 days before the day of definitive egg abandonment, and from 1 day before to 1 day after the beginning of transitory abandonments, depending on the individual. On average, the decline was significant (P < 0.05, n = 10) 1.7 days before the day of definitive egg abandonment for daily and diurnal Tegg and only on the day of definitive abandonment for nocturnal Tegg (Fig. 4). Mean diurnal Tegg decreased for 3 consecutive days, respectively, by 0.4, 1.5, and 10.0°C. During the last 5 days of incubation, the mean diurnal Tegg (y) was directly related to the daily total duration of transitory abandonments (x) according to y = 35.4°C - 0.19x (n = 50, r = 0.46, P < 0.001). There were no significant relationships between Tegg maintained at plateau and the various behavioral parameters characterizing egg abandonment (P > 0.40, n = 10).


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

Progressive Behavioral Changes Reflect the Stimulation of Feeding Behavior

This study shows that preventing relief by the partner of fasting-incubating king penguins leads to an increase in the fasting duration until the egg is spontaneously abandoned. This abandonment is not sudden and definitive but is preceded by behavioral changes such as songs and decreased egg attendance by transitory abandonments. The duration of transitory abandonment and the distance between the bird and the briefly abandoned egg progressively increase during the abandonment process. As summarized in Table 1, the duration of this process, as estimated from various criteria, averages 1.5 days but can be as long as 5 days.

                              
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  		Table 1.   Average and extreme durations of the decrease in the drive to incubate according to various behavioral and physiological criteria

Because our data were obtained on penned birds, the question arises as to how these results represent the behavior of egg abandonment under free-living conditions. The observation that penned penguins defended a small territory and displayed the same behavioral repertoire as in the wild suggests that penning did not affect normal incubation behavior. The finding that definitive egg abandonment and escape attempts were exclusively diurnal events agrees with the observation that in the wild 80% of the departures to sea for feeding occur during daytime (8). This suggests that the timing of the departure to refeed, as reflected by definitive egg abandonment and escape attempts, is not affected by captivity. Finally, the fact that penned penguins repeatedly sang before abandoning the egg also argues for the lack of any penning effect. Singing is the normal way used by mates to recognize each other at relief (31), and it is likely that singing penned birds were calling to their partner for egg exchange, thus signaling their readiness to depart to refeed. Nevertheless, the captivity conditions may have affected certain aspects of egg abandonment. We observed that because only a few birds were kept in the pen they were not prevented by their neighbors to take their egg again after transitory abandonment, the latter being moreover protected from predation. In contrast, we observed in the wild that a bird that transitorily abandons and moves even a small distance away has great difficulty retrieving its egg because the bird is violently aggressed by its neighbors defending their territory, which favors egg predation. Thus it seems that for free-living birds the number of transitory abandonments, their durations, and the total duration of the egg abandonment process would be lower than found in this study, because birds in the wild could be forced to prematurely leave their egg even if their drive to incubate was not fully abolished. In contrast, what we observed in penned birds is probably the full and endogenously driven sequence of behavioral events that reflect the stimulation to refeed independently of interactions with conspecifics. Thus captive king penguins incubating under normal environmental conditions should constitute a convenient and valid animal model to study on the long-term (several days) how the incubation behavior is redirected toward the search for food.

The progressive behavioral changes observed in the incubating king penguin before definitive egg abandonment are reminiscent of those observed in another large-sized long-term fasting penguin, the emperor. When fasting, but not incubating, this bird markedly and progressively increases its spontaneous locomotor activity below a threshold body mass (28). In the absence of an egg, the increase in locomotor activity can only be stimulated by an increase in the refeeding drive unrelated to changes in the drive to incubate. The progressively increasing distance walked by king penguins over their successive transitory abandonments also corresponds to increasing spontaneous locomotor activity. The similarities between nonincubating emperors and incubating king penguins reinforces the idea that the decrease in the drive to incubate observed in the present study is the direct consequence of a stimulation of the refeeding drive. This also is consistent with the previous finding that the amount of recess time taken by incubating Canadian geese for feeding increases dramatically once a lower critical body mass is reached (1).

The first clear indication of a decrease in the drive to incubate was the transitory abandonment of the egg, which was associated with sharp transitory fall in Tegg. The significant correlation between diurnal Tegg and total duration of transitory abandonments supports the view that on average there was no clear decrease in egg attendance before the first transitory abandonment. However, there were behavioral (song, increase in cleaning, stretching, and moving activity) and biotelemetry (decrease in Tegg 1 day before the first transitory abandonment) indications that in several birds a decrease in the drive to incubate is detectable about 1-2 days before the first transitory abandonment. A high rate of comfort activities is commonly seen in relieved birds before they depart to sea. As mentioned previously, singing before the beginning of transitory abandonments probably corresponds to an alarm reflecting the attainment of a high refeeding drive. Thus the average duration of the various behavioral changes preceding definitive egg abandonment should be set instead at 2-3 days for most birds. This seems to be the average duration needed for penguins to redirect their activity from one of a normal life history stage (incubation) to one of survival (egg abandonment and departure to refeed). Such a shift in behavior fits well with the "emergency response" concept proposed by Wingfield et al. (35) and differs from the stress response that develops within a few seconds. Our results extend the time scale of the former concept by showing that in certain situations in large birds the emergency response may take a much longer time to develop than usually considered, i.e., days instead of minutes or hours.

Behavioral Changes are Triggered on Reaching a Lower Body Mass Threshold and Differ Considerably Among Individuals

The duration of the fast at egg abandonment in penned birds was 60% longer than that in birds relieved normally by their partner. The body mass at egg abandonment (8.8 kg) was not only lower than for relieved birds (10.0 kg) but also lower than the 9.6-10 kg critical body mass reported for breeding-fasting male king penguins (10, 11). This critical, or threshold, body mass corresponds to a critical but not total exhaustion of fat stores and to a transition from lipids to proteins as the main energy fuel, the so-called "phase III" of fasting (11, 17). In nonincubating penguins, entrance into phase III is reflected by a progressive increase in daily body mass loss and by an elevation in plasma uric acid, due to the increased protein breakdown (11, 29), and in circulatory corticosterone (11). In the emperor penguin, the increase in the refeeding drive is concomitant with an increase in daily body mass loss, plasma uric acid, and corticosterone, and by a decrease in circulating beta -hydroxybutyrate (28). Plasma uric acid and corticosterone at egg abandonment were not measured here, but in another experiment where penned birds abandoned at a similar body mass, the values were increased (Groscolas R, Fayolle C, Decrok F, Thil MA, Mikowski E, and Robin J-P, unpublished data). The behavioral changes observed in incubating king penguins were progressive as were the metabolic and endocrine changes observed in nonincubating penguins. Overall, this finding strongly suggests that in incubating king penguins and as has been proposed in nonincubating emperors (28), a metabolic shift induced by a critical exhaustion of energy stores acts as a signal to stimulate feeding behavior to ensure survival. Furthermore, the observation that body mass at egg abandonment was about 1 kg lower than the critical value suggests that egg abandonment does not occur as soon as the threshold body mass is reached but several days later. From previously reported data on daily body mass loss during phase III (11), it can be calculated that definitive egg abandonment occurs about 1 wk after the critical body mass is reached. Accordingly, the first transitory abandonment occurs, on average, when the birds have been fasting into phase III for 5-6 days, which would be the time required for the refeeding drive to outweigh the motivation to incubate. More subtle signs of stimulated feeding behavior could be observed 4-5 days after the threshold body mass was reached. It therefore appears that the refeeding signal needs to operate for several days or that its intensity needs to reach a given level before triggering behavioral changes. The observation that definitive egg abandonments occurred only during daytime suggests that even when at its maximum intensity, the signal may be overriden temporarily by other factors. It is indeed likely that some birds were ready to depart in the evening but waited overnight before leaving early in the morning, possibly to have better light conditions for orientation. Thus it seems that critically energy-depleted penguins still have a safety margin, which allows some flexibility in the timing of refeeding.

Although all birds showed the same characteristic behavioral features (transitory egg abandonments, songs, escape attempts), there was no evidence that they formed a concerted behavioral pattern. No relationship was found between the number and the timing of these different features. Moreover, there were marked interindividual differences in the pattern and timing of the various behaviors and more strikingly in the overall duration of the egg abandonment process. The number of transitory abandonments and songs and the maximum duration of a transitory abandonment differed by 30- to 40-fold, whereas the total duration of transitory abandonment covered a 150-fold range. Taking into account the first evidence for a decrease in the drive to incubate, the total duration of the egg abandonment process ranged from 20 h to 5 days, i.e., a factor of six. These behavioral differences could reflect interindividual differences in the sensitivity to the refeeding signal and/or in the rate at which the signal is generated by the metabolic shift. The latter possibility finds support in the observation that below the threshold body mass the slope of the increase in body mass loss, plasma uric acid, and corticosterone with time in fasting penguins varies greatly among individuals (11, 28, 29). On the other hand, the lack of relationships between the pattern or timing of behavioral changes and the initial body mass or the total duration of fasting does not argue for an effect of initial adiposity or absolute fat store depletion on the refeeding signal. Perhaps previous breeding experience is important, notably for the time a bird can go on incubating after reaching a lower threshold in energy reserves. Experienced breeders would be more resistant to fasting, tolerate greater energy depletion, and have a higher drive to incubate than inexperienced ones, thus better resisting an intense stimulation to refeed. This would meet with the suggestion that experienced birds can compensate for lower body reserves by being more proficient foragers (26). Interindividual differences in incubation experience and efficiency are suggested by the differences observed in the Tegg patterns during normal incubation (e.g., Fig. 5) and in the average temperature at which eggs were incubated (33-37°C). However, the lack of relationships between Tegg during normal incubation and any of the various behavioral parameters characterizing egg abandonment, notably its total duration, does not support the above hypothesis. The possibility that some birds could have received cues from the developing chick, which would have influenced the timing of definitive egg abandonment, cannot be considered to explain interindividual variability because all the birds incubated a dummy egg. Moreover, in a preliminary experiment we observed that the abandonment pattern of a newly hatched chick (4 days of age) was similar to that of an egg (15 transitory abandonments, duration from the first transitory abandonment to definitive abandonment = 33 h, body mass at abandonment = 9.55 kg). Prolactin has a major role in the stimulation of incubation behavior in birds (6), whereas in contrast corticosterone stimulates food searching (3). Thus the measurement of the plasma level of these hormones at the onset and end of the incubation shift might help in understanding individual differences in the triggering of feeding behavior and, more generally, the mechanism of the refeeding signal. Because leptin has been shown to inhibit food intake in mammals (33) and birds (27), its plasma level reflecting fat mass (12), a decrease in plasma leptin below the threshold body mass also could be a major component of this signal.

Perspectives

This study shows that captive incubating king penguins constitute a promising tool for understanding the mechanism(s) by which energy and metabolic status control feeding behavior for the long term. It should be feasible to follow continuously the metabolic and endocrine status of birds in relation to those of behavior for several days and thus to better understand how refeeding is triggered. Given the important role of leptin in interrelating energy metabolism, fat stores, and food intake in mammals it would be of great interest to determine whether this hormone has a similar action in birds, especially during natural fasting. Among possible mechanisms of the refeeding signal, a decrease below a body (fat) mass threshold in the production rate of fatty acids by adipose tissue and thus in the contribution of this fuel to energy production can be suggested. Indeed, it has been shown that an experimental blockade of fatty acid oxidation stimulates food intake in rats fed a high-fat diet (15, 20). This hypothesis could be tested by measuring fatty acid production in vivo at different stages of fasting using tracers and by studying the effects of pharmacological manipulation of fatty acid production and/or utilization on behavior. The king penguin model also could be appropriate to determine how the redirection of behavior toward the search for food below a body mass threshold is efficient for survival to prolonged fasting.


    ACKNOWLEDGEMENTS

This study was supported by grants from Institut Français pour la Recherche et la Technologie Polaires (Program 119) and received logistical support from Terres Australes et Antarctiques Françaises.


    FOOTNOTES

Address for reprint requests and other correspondence: R. Groscolas, Centre d'Ecologie et Physiologie Energétiques, CNRS, 23 rue Becquerel, 67087 Strasbourg, France (E-mail: rene.groscolas{at}c-strasbourg.fr).

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.

Received 22 February 2000; accepted in final form 17 July 2000.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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Am J Physiol Regul Integr Comp Physiol 279(6):R2104-R2112
0363-6119/00 $5.00 Copyright © 2000 the American Physiological Society


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