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Keywords:

  • Body mass increase;
  • intra-individual variation;
  • Luscinia luscinia;
  • stopover ecology;
  • Thrush Nightingale

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1. We studied the changes in body mass, metabolizable energy intake rate (ME) and basal metabolic rate (BMR) of a Thrush Nightingale, Luscinia luscinia, following repeated 12-h migratory flights in a wind tunnel. In total the bird flew for 176 h corresponding to 6300 km. This is the first study where the fuelling phase has been investigated in a bird migrating in captivity.

2. ME was very high, supporting earlier findings that migrating birds have among the highest intake rates known among homeotherms. ME was significantly higher the second day of fuelling, indicating a build-up of the capacity of the digestive tract during the first day of fuelling.

3. Further indications of an increase in size or activity level of metabolically active structures during fuelling come from the short-term variation in BMR, which increased over the 2-day fuelling period with more than 20%, and in almost direct proportion to body mass. However, mass-specific BMR decreased over the season.

4. The patterns of mass change, ME and BMR of our focal bird following two occasions of 12-h fasts were the same as after flights, indicating that fast and flight may involve similar physiological processes.

5. The relatively low ME the first day following a flight may be a contributing factor to the well-known pattern that migrating birds during stopover normally lose mass the first day of fuelling.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

During migration a bird regularly alternates between two main activities: flight and fuelling. These activities to a large extent put different, and sometimes opposing, demands on the behaviour and physiology of the migrant (Jehl 1997; Piersma & Lindström 1997). During flight the bird should be an efficient flying-machine, with flight muscles well proportioned to efficient flight (Pennycuick 1975; Marsh 1984). It should preferably carry only energy-rich fuel, that is, fat, and it should minimize the mass of structures that do not contribute to the flying-machine (Jehl 1997; Piersma & Gill 1998). On the other hand, during fuelling, the bird should be an efficient eating-machine with a high ability to find and process food. A high fuelling rate is important for a bird that wants to maximize migration speed (Alerstam & Lindström 1990; Lindström 1991).

Birds, like many other vertebrates, have the ability to change their morphology and physiology drastically over periods as short as days (‘phenotypic flexibility’sensuPiersma & Lindström 1997). Given that muscles and body organs are energetically and behaviourally costly to sustain and carry, this optimization of organ size may be regarded as ‘a way for animals to cope successfully with a much wider range of conditions occurring during various life-cycle events than fixed metabolic machinery would allow’ (Piersma & Lindström 1997).

The migratory journey, with its repeated, predictable and rapid switches between activities with drastically different demands on the bird, is an event where natural selection may well have favoured such a phenotypic flexibility and, indeed, such a flexibility has been demonstrated in several studies (Jehl 1997; Piersma & Lindström 1997). Physiological changes may take place during both flight and fuelling, but in this paper we focus on the potential physiological changes taking place during the fuelling (stopover) phase.

Some aspects of the stopover ecology of migrating birds are preferably studied in captivity, for example when it is necessary to study in detail the same individual over longer periods, or when advanced technical equipment is needed. Many such studies have been carried out, shedding new light on various aspects of the fuelling phase of migration (e.g. King 1963; Bairlein 1985; Biebach 1985; Klaassen & Biebach 1994; Lindström & Kvist 1995; Hume & Biebach 1996; Klaassen, Lindström & Zijlstra 1997). However, so far nobody has been able to study the important interplay between flight and fuelling in captivity, simply because it has not been possible to have birds flying for extended periods. Instead, flight has been simulated by fasting the birds over a period long enough to entail a mass loss equivalent to a migratory flight (Biebach 1985; Klaassen & Biebach 1994; Hume & Biebach 1996; Klaassen et al. 1997). It is not known, however, how well fasting mirrors flight, which lends some uncertainty to conclusions drawn from migration experiments involving fasting phases.

In this paper we present data on the fuelling phase of a Thrush Nightingale Luscinia luscinia L., a long-distance passerine migrant, that carried out a full autumn migration in captivity, including many long flight sessions in a wind tunnel (M. Klaassen, A. Kvist & Å. Lindström, unpublished data). Our results on energy intake rates and changes in basal metabolic rate (BMR) give indirect support to earlier findings of a rapid and significant physiological flexibility during fuelling.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Our focal bird was one in a clutch of five Thrush Nightingales that was taken from the nest in the Revinge area (55°40′N, 13°25′E), 20 km east of Lund in summer 1995 (under licence from the Swedish Environmental Protection Board). The nestlings were raised in captivity by their biological parents. All the juveniles became very tame. After independence all young went through a typical partial moult (body feathers and some wing coverts) in July and August. One of the juveniles (named Blue) was subsequently selected for training and experiments. Some data are also presented for another Thrush Nightingale studied in 1994.

HOUSING CONDITIONS AND FOOD

Prior to and between experimental trials, Blue was kept in an aviary measuring 1·5 m × 1·5 m × 2·2 m, situated within the wind-tunnel building at Lund University, Sweden. Up to 20 September the light regime was the same as the local light regime of Lund. After 20 September, Blue had a light regime of 12L:12D, starting at 09·00 local time. Ambient temperature in the building was between + 17 and + 23 °C. Blue always had access to water, and was fed either mealworms (Tenebrio larvae) or a food mix consisting of boiled eggs (including shell), boiled ‘sour’ milk, bread-crumbs, commercial dried insect mix, minced meat, vitamins and calcium.

EXPERIMENTAL DESIGN

Between 18 September and 7 November Blue carried out seven 12-h flights in the wind tunnel. These flights will be described in detail elsewhere. Blue made one flight per week, always on Mondays, between 09·00 and 21·00. Although Thrush Nightingales normally migrate at night, Blue preferred to fly under daylight condition. Food was removed in the early afternoon of the day preceding the flight session. After each flight Blue was placed in a metabolic chamber in which oxygen consumption was measured during the following night and two additional full days (Fig. 1). Although it had been desirable, oxygen consumption was not measured the night prior to the flight, since experience from the beginning of our study (but outside the trials reported here) indicated that this made Blue less inclined to fly. During the daylight hours of this postflight recovery period in the metabolic chamber, Blue had ad libitum access to mealworms and regained the mass it had lost during flight. Between the trials, Blue was given food mix on Thursday and Friday (to make the diet more varied), and mealworms on Saturday and Sunday (as preparation for the subsequent fuelling period in the respirometer, when only mealworms were available).

image

Figure 1. . A schematic view of the experimental protocol. The bottom bar shows the light:dark cycle (12:12) and the daytime activity (flight or food) over the 3 experimental days. A typical pattern of body mass change is shown in the middle section, with filled circles marking actual weighing occasions and open circles indicating estimates of evening body masses (when the bird was not weighed). When oxygen consumption was measured is also indicated.

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Starting 13 and 27 November, Blue went through two similar 3-day trials, but the flight session of the first day was exchanged for a fasting period. Blue was then without food and water for 12 h (as it was during flight) while kept at + 20 °C.

During 2–12 December 1994 another Thrush Nightingale (named Niels) went through an experimental protocol very similar to the one used for Blue. However, instead of repeated 3-day trials Niels went through one continuous 10-day trial. The major difference was that Niels never flew for long enough periods to allow the type of analyses made for Blue. Trial days of Niels included either feeding or fasting. On seven of the days Niels flew for periods lasting between 5 min and 4 h in late afternoon and evening. The three longest flights lasted 4 h (4 Dec), 2 h (2 Dec) and 2 h (11 Dec), respectively. Here we present data on the daily variation in BMR of Niels. One important reason for this is to be able to separate the possible effects on BMR of mass loss due to flight, and the effect of the flight in itself (as an exercise).

METABOLIC MEASUREMENTS

Oxygen consumption of Blue was measured in a 22-l metabolic chamber, containing a perch, a water tube and a food container. Measurements started around 21·30 in the evening, directly after the 12 h flight. The first night the bird had access to water only. The next morning at 09·00 the bird was taken out and weighed, given 10-min access to a bowl of water and then weighed again. During this 10-min period the bird never bathed and normally drank very little water (less than 0·2 g). Thereafter followed a 24-h period in the metabolic chamber when the bird had access to water and a known amount of food for the first 12 h. At lights off, the food container was shut and the bird had no longer access to food. In a few cases mealworms were then lying on the floor, but these were never eaten during the dark period. The next morning the same procedure was repeated as on the previous morning. In addition, the remaining food was weighed to yield gross food intake over the first postflight recovery day. After another 24-h period, the experiments ended and the bird was brought back to its aviary (Fig. 1).

The oxygen consumption of Blue was measured in an open-circuit system. The metabolic chamber was placed in a temperature-controlled cabinet (BK600, Heraeus, Hanau, Germany) which was set to give the bird an ambient temperature of + 26·5 °C. Air was sucked through the metabolic chamber at a controlled rate of 20·0 l dry air (at ± 0 °C and 1 atm) h–1 (flow controllers 5850E, Brooks, Veenendaal, the Netherlands). Silica gel was used to dry the effluent air. Every 90 min, reference air was measured for 15 min and air from the bird for 75 min. Oxygen concentration of the air was measured to the nearest 0·01% (1100 A, Servomex, Crowborough, East Sussex, UK). Oxygen consumption was corrected for the difference in volume of inlet and outlet air (Klaassen et al. 1997), assuming a respiratory quotient, the ratio of CO2 produced to O2 consumed, of 0·72.

The basal metabolic rate (BMR) is the energy expenditure rate of a normothermic, postabsorptive, non-productive (no reproduction, moult, etc.) and inactive animal, measured under thermoneutral conditions during the natural resting phase of the day (e.g. Aschoff & Pohl 1970). Assuming that it takes 3 h to acquire a postabsorptive state (Klaassen & Biebach 1994), Blue probably satisfied all the BMR criteria between 00·00 and 09·00. As an estimate of BMR in Blue the lowest 10-min average of oxygen consumption was used, which always occurred between 00·00 and 06·00. The oxygen consumption of the mealworms present in the chamber during nights 2 and 3 were corrected for when estimating BMR. The night-time metabolic rate of mealworms at + 26·5 °C was determined in a separate trial to 0·0057 ml O2 min–1 g–1.

A relatively large metabolic chamber was used to provide reasonable comfort to the bird and to reduce the risk of damaging the plumage. A large chamber in relation to flow and size of the bird typically leads to an overestimate of BMR for a bird that is partially active. However, Blue was hand-tame and very quiet in the chamber. We are therefore confident that our BMR estimates reflect true steady rates of minimum oxygen consumption.

Two batches of mealworms (nos 1 and 2) were used over the autumn, with the first batch used until 1 November and the second batch from 1 November and onwards. Mealworms were stored at + 8 °C. Their energy densities were 10·06 (no. 1, SD = 0·15, n = 3) and 11·35 (no. 2, SD = 0·16, n = 5) kJ g–1 wet mass, as determined by bomb calorimetry (IKA C400 adiabatic calorimeter, Staufen, Germany). The difference in energy content of mealworms from the different batches was statistically significant (t-test, t6 = 11·3, P < 0·001). After collection the excreta produced during day 2 and day 3 were dried for 48 h at + 70° and stored at – 20 °C. The energy content was later determined in a bomb calorimeter to 14·68 (after eating mealworms of no. 1, SD = 0·16, n = 9) and 15·65 (after eating mealworms of no. 2, SD = 0·36, n = 7) kJ g–1 dry mass. The difference in energy content of excreta produced from the different batches of mealworms was statistically significant (t-test, t14 = 7·3, P < 0·001).

The daily apparent efficiency of energy utilization (cf. Hume & Biebach 1996) was calculated as the difference between daily energy intake (gross intake of mealworms times the average energy density of a given batch of mealworms) and daily excreta energy output (dry mass of excreta times the average energy density of excreta originating from a given batch of mealworms), divided by daily energy intake. Since we lacked data on energy contents of excreta for two of the experimental days the average value of excreta energy density was used, instead of the actual value from each day. Since the variation was very small, the difference between our estimates of daily apparent efficiency of utilization and the actual values for separate days were less than 1% (cf. Klaassen et al. 1997). The metabolizable energy intake (ME) over a given day was calculated as the gross intake of mealworms times the energy content estimated for that batch of mealworms times the average apparent efficiency of utilization.

Statistics were performed using the Analysis Tools package of Microsoft Excel 7·0. Tests on proportions were done after angular transformation of data, but real values are reported.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The variation in body mass, BMR and metabolizable energy intake of Blue during the nine different experimental sessions (seven flights and two fasts) are presented in Table 1.

Table 1.  . Variation in body mass, basal metabolic rate (BMR) and metabolizable energy intake (ME) of a juvenile Thrush Nightingale during seven test sessions starting with a 12-h flight, and two test session starting with a 12-h fast. A schematic view of the test protocol is given in Fig. 1Thumbnail image of

BODY MASS CHANGES

During the 2-day fuelling phase, body mass increased with on average 23% following the flights, and 29% following the fasts. After the flights, body mass increase was significantly higher over day 3 than over day 2 (paired t-test, t6 = 3·15, P = 0·02). The average body mass increases over day 2 and day 3 for all nine sessions were 2·55 g and 3·24 g, respectively, which are equal to 11·6% and 14·7% of lean body mass day–1 (assuming a lean body mass of 22 g).

METABOLIZABLE ENERGY INTAKE

The apparent efficiency of utilization for the two batches of mealworms was similar (0·792 ± SD 0·009 for no. 1 and 0·790 ± SD 0·009 for no. 2; t-test, t16 = 0·55, P = 0·59). The difference in apparent efficiency of utilization between day 2 (0·793 ± SD 0·006) and day 3 (0·790 ± SD 0·011) was not statistically significant (paired t-test, t8 = 0·84, P = 0·43).

ME varied between 70·4 and 180·7 kJ day–1 and was on average 58% higher during day 3 than during day 2 (paired t-test, t8 = 11·0, P < 0·001, Table 1, Fig. 2). Since body mass was always higher on day 3 than on day 2, it follows that ME to some degree correlates with body mass. However, to exclude the possibility that this correlation is only an effect of the amount of time spent on fuelling, it was tested whether ME correlated with body mass for day 2 days and day 3 days separately. ME was significantly positively correlated to body mass on day 3 days only (day 2, log ME (kJ day–1) = – 0·31 + 1·64 log body mass (g), r2 = 0·30, P = 0·126, n = 9, day 3, log ME (kJ day–1) = – 0·74 + 2·03 log body mass (g), r2 = 0·74, P = 0·003, n = 9).

image

Figure 2. . Daily metabolizable energy intake of a juvenile Thrush Nightingale (‘Blue’) on the first (day 2, open bars) and second (day 3, black bars) day following a 12-h flight (session 1–7) and a 12-h fast (session 8–9).

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BASAL METABOLIC RATE

The BMR of Blue was positively correlated to body mass within sessions (Fig. 3). For each 3-day session we calculated the relationship between BMR and body mass (m) using the equation: log BMR=log a+b log m. The slope, b, was on average 0·92 (SD = 0·38, range 0·22–1·51, n = 9). Thus, on average, BMR increased almost directly in proportion to body mass. BMR increased from night 1 to night 3 with on average 22·7% (the average mass increase was 24·3%). The overall intra-individual slope combining all nine trials was 0·75 (r2 = 0·72, P < 0·001, n = 27).

image

Figure 3. . Basal metabolic rate (BMR) in relation to body mass of a fuelling Thrush Nightingale (‘Blue’) during 3 successive nights following a 12-h flight (filled circles, seven sessions), and a 12-h daytime fast (open circles, two session). Data from the same fuelling period are connected with lines. The scales of the axes are non-logarithmic, but regressions were calculated using logarithmic values (see text).

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For each three-day session the BMR was estimated at 26 g from the session-specific regression of BMR on body mass. The BMR values at this standard mass show that the mass-specific BMR decreased as the season progressed (Fig. 4). It was this seasonal decrease that caused the between-session slope of BMR on body mass (0·75) to be shallower than the average within-session slope (0·92).

image

Figure 4. . Seasonal change in basal metabolic rate (BMR) of a juvenile Thrush Nightingale (‘Blue’) at a body mass of 26 g. Each value was estimated from each of the slopes of log BMR on log body mass (Fig. 3) following a 12-h flight in a wind tunnel (filled circles, n = 7), and a 12-h day-time fast (open circles, n = 2). Least square regression line is BMR = – 0·0017 date + 61·032, r2 = 0·63, P = 0·011, n = 9.

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The BMR of Niels varied significantly with body mass over the 10-day study period, with a slope of 1·48 (Fig. 5).

image

Figure 5. . Basal metabolic rate in relation to body mass of a second juvenile Thrush Nightingale (‘Niels’) over a period of 10 consecutive days. Body mass varied between days due to fuelling, fasting or flight. Open circles denote BMR values from the nights following the three longest flights (2–4 h). The scales of the axes are non-logarithmic, but the regression was made using logarithmic values. The line is the least-square regression line (log BMR (ml O2 min–1) = – 2·22 + 1·48 log body mass (g), r2 = 0·76, P < 0·001, n = 10).

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

During autumn and early winter of 1995 our juvenile Thrush Nightingale flew a corresponding distance of 6300 km in the wind tunnel (M. Klaassen et al., unpublished data). This equals a full autumn migration from southern Sweden to the species’ winter quarters in SE Africa (Cramp 1985). In addition the bird normally flew in flights lasting 12 h, which ought to reflect the length of flights in the wild for this night migrant. In between the flights the bird was allowed to fuel-up, within the range of body masses normally found in the wild (Cramp 1985). Hence, for the first time it was possible to study the energetic details of fuelling of an individual migrant actually migrating in captivity.

METABOLIZABLE ENERGY INTAKE AND BODY MASS INCREASE

The energy intake rate of Blue during fuelling was high. Kirkwood (1983) suggested an absolute ceiling to maximum daily metabolizable energy intake in homeotherms at 2200 kJ kg0·72. The highest daily metabolizable energy intake of our bird was 180·7 kJ, at a mass of 29·7 g, which in Kirkwood’s terms is equal to 2273 kJ kg0·72. This fits the finding of Lindström & Kvist (1995) that intake rates of passerine birds during migration are very high compared with other homeotherms. In their study of 22 species of captive passerine migrants during autumn (not including Thrush Nightingale), 12 had a daily metabolizable energy intake higher than the maximum suggested by Kirkwood (1983), the highest being 2699 kJ kg0·72 in the Sedge Warbler, Acrocephalus schoenobaenus L.

Concomitant with this high level of metabolizable energy intake rate of Blue was a high body mass increase rate, with an average of 14·7% of lean body mass day–1 during day 3 (assuming a lean body mass of 22 g). Lindström (1991) predicted maximum rates of body mass increase for birds of different body mass, using Kirkwood’s (1983) equation of maximum daily metabolizable energy intake, and estimates of minimum levels of energy expenditures of free-living birds. For a passerine with a lean body mass of 22 g, the predicted maximum mass increase rate was 6·2% day–1. The highest values reported in the literature for similar-sized free-living individual passerine birds were 7·7–12·4% day–1 (Lindström 1991). In conclusion, the fuelling performance of Blue was exceptionally high.

ENERGY INTAKE RATE AND PHYSIOLOGICAL FLEXIBILITY

It has become increasingly clear that migrating birds possess a great deal of short-term phenotypic flexibility (for example, McLandress & Raveling 1981; Piersma 1990; Lindström & Piersma 1993; Jehl 1997; Piersma & Lindström 1997), involving body components important for energy intake (for example, the digestive tract and the liver) and locomotion (flight muscles). Unfortunately we have no information about potential changes in the size of flight muscles of Blue. A preliminary try-out with Blue and other Thrush Nightingales using ultra-sound did not give any useful information, probably owing to a combination of inexperience with the technique and the very small structures studied (Å. Lindström, M. Klaassen and A. Kvist, unpublished data). However, it is likely that our data from Blue relate to a physiological flexibility in the digestive organs.

The energy intake rate of Blue was significantly lower the first day of fuelling than the second. This pattern has been found in other studies of captive long-distance migrant birds (Klaassen & Biebach 1994; Hume & Biebach 1996; Klaassen et al. 1997). In fuelling Garden Warblers, Sylvia borin (Bodd.), the increase in energy intake rate was paralleled by an increase in the dry mass of the digestive tract (Hume & Biebach 1996). Although direct evidence is lacking, it is likely that the same process took place in Blue.

Metabolizable energy intake rate as such would be a good indication of intake capacity if it was certain that birds in migratory disposition always fed at their maximum rate. There are good reasons to believe this. In a study of Thrush Nightingales, fuelling at three different ambient temperatures (– 7, 7 and 22 °C), Klaassen et al. (1997) found that intake rate was largely independent of temperature, despite the fact that body mass increase was lower or absent at the lower temperatures. Thus, despite the risk of a negative energy balance the birds at lower temperatures did not eat more, indicating that they had reached their maximum capacity.

BASAL METABOLIC RATE AND PHYSIOLOGICAL FLEXIBILITY

Further indirect evidence of physiological changes during fuelling comes from the short-term variation in BMR. The metabolic activity of organs such as gut, intestines, liver and skeletal muscles contribute significantly to BMR (Field, Belding & Martin 1939; Martin & Fuhrman 1955; Oikawa & Itazawa 1984; Itazawa & Oikawa 1986; Scott & Evans 1992; Weber & Piersma 1996). Stored fat, however, probably has little impact on BMR (Martin & Fuhrman 1955; Scott & Evans 1992). The BMR of Blue increased with on average 23% over 2 days, and the BMR had a mass exponent of 0·92. The corresponding exponent for Niels was 1·48. Given that an increase in fat alone should not influence BMR to any significant extent, there are strong reasons to believe that the increase in body mass was at least partly due to an increase in metabolically active body organs. Indeed, separate analyses of the energy and nitrogen budget of Blue and other Thrush Nightingales, showed that a considerable part of the mass increase during fuelling was due to deposition of protein (Klaassen et al. 1997; unpublished data).

BMR of Blue was always lowest the night following a flight. The low BMR could potentially be an effect of the flight and not of mass loss. If so, the increase in BMR over the fuelling period would be a sign of recuperation from an endurance exercise and not related to changes in organ size. If this was the case we would expect no changes in BMR in fuelling birds following starvation. However, this was not the case for Blue. Also, in starved Garden Warblers, BMR increased in parallel to body mass during fuelling (Klaassen & Biebach 1994). In addition, data from Niels indicate that a flight will not lower BMR the following night, since the three BMR values from the nights following flights of 2–4 h were all above the regression line of BMR against body mass (Fig. 5).

SCALING AND SEASONALITY OF BASAL METABOLIC RATE

In the few studies of birds where intra-individual variation in BMR has been measured, the log BMR vs log body mass slopes were all above 1: 1·67 in the European Kestrel, Falco tinnunculus L. (Daan et al. 1989), 1·38 in the Knot, Calidris canutus L. (Piersma, Cadée & Daan 1995), and 1·26 in the Redshank, Tringa totanus L. (Scott, Mitchell & Evans 1996). Clearly, the BMR of a given individual may vary substantially over short periods and caution is needed when discussing BMR as a fixed value for an individual or a species. Also, the within-individual slope of log BMR against log body mass is steeper (0·9–1·7) than the log BMR vs log body mass slopes of about 0·6–0·8 found among species, populations and individuals of one species (Daan et al. 1989). Hence, the scaling of BMR against body mass is highly dependent on the level of comparison (Bennet & Harvey 1987; Daan et al. 1989).

There was a seasonal decline in the mass-specific BMR of Blue. This could be a captivity effect (cf. Piersma et al. 1996). Alternatively, it may reflect a seasonal change in metabolic activity level, as has been suggested for waders moving between Arctic breeding grounds and tropical winter quarters (Klaassen, Kersten & Ens 1990; Piersma et al. 1995, 1996; Lindström 1997).

WHEN ARE BUILT-UP STRUCTURES BROKEN DOWN AGAIN?

In migrants going through repeated cycles of flight and fuelling, a build-up of the digestive tract during the early phase of fuelling must be balanced by a break-down of the same structures during another phase of the migratory cycle. In grebes and waders it seems as if the size of the digestive tract is reduced prior to the migratory flight (Jehl 1997; Piersma & Gill 1998). This makes sense, since the digestive tract is purely a ballast during flight (cf. Piersma & Gill 1998). For small migrants such as the Thrush Nightingale, no equivalent information is available. A reduction in size of digestive organs may also take place during the migratory flight. In a separate analysis we found that some protein was indeed catabolized by Blue during flight, although the origin of this protein is unknown (M. Klaassen et al., unpublished data). Also, Hume & Biebach (1996) found a significant decrease in the size of the digestive tract during a 2-day fast, aimed at simulating a migratory flight.

Fasting has repeatedly been used as a substitute for migratory flights (Biebach 1985; Klaassen & Biebach 1994; Hume & Biebach 1996; Klaassen et al. 1997). Indeed, the pattern of energy intake, mass increase and BMR during the fuelling phase of Blue was similar after flights and starvation, respectively, and similar to the patterns found in the above-mentioned fasting studies. This supports the view of Piersma (1990), that long-distance migration may be considered as a very rapid starvation process.

COMPARISON WITH BIRDS ON STOPOVER IN NATURE

The relatively low food intake of Blue on the first day compared with the second day of fuelling coincided with a lower mass increase during that day. Numerous stopover studies have shown that the first day after ringing (assumed to be the time of arrival, but see Lindström 1995) is the day with the lowest mass increase and that most birds actually lose mass the first day (for example, Mascher 1966; Hansson & Pettersson 1989). Our data on Blue support the suggestion that one important factor contributing to this pattern is the change in physiological state from a ‘flight-state’ to a state of hyperphagia (Langslow 1976; Klaassen & Biebach 1994).

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The wind tunnel set-up was financed by grants from Knut and Alice Wallenberg Foundation (to Thomas Alerstam), the Swedish Council for Planning and Coordination of Research (to T.A. and Å.L.) and the Swedish Natural Science Research Council (to T.A. and Å.L.). M.K. was supported by a grant from the Swedish Institute. This is publication 2454 of the Netherlands Institute of Ecology, Centre for Limnology.

Footnotes
  1. Present address: Netherlands Institute of Ecology, Center for Limnology, Rijksstraatweg 6, NL-3631 AC Nieuwersluis, the Netherlands.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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