(Sylvia borin Boddaert) ... weight at night and gain weight during the day- time, thus .... Mean period n. Seasonal length. (birds) body weight. (days)". Diet .c 20-.
J Comp Physiol B (1986) 156:859-865
Journal of Comparative Systemic, ~om,.,, and EnvironPhysiology
Physiology B m..,.,
9 Springer-Verlag 1986
Spontaneous, approximately semimonthly rhythmic variations of body weight in the migratory garden warbler (Sylvia borin Boddaert) Franz Bairlein Physiological Ecology Section, Department of Zoology, University of K61n, Weyertal 119, D-5000 K61n, Federal Republic of Germany Accepted June 21, 1986
Summary. 1. Two groups of garden warblers, a western Palaearctic long-distance migratory passerine bird species, were kept under controlled laboratory conditions and their weights were recorded almost daily for up to 18 and 30 months, respectively. 2. All specimens exhibited spontaneous, regular body weight fluctuations with an average periodicity of about 18 days and an amplitude of up to 32% of the corresponding initial body weight. The period length of the cycle was influenced by the seasonal level of body weight due to migratory fattening as well as by the nutritional composition of the diet. 3. This is the first time that such spontaneous cyclic, body weight fluctuations with almost a semimonthly period are described for a bird species. 4. Since no obvious external zeitgeber seems to exist for these rhythms in body weight they appear to be endogenously controlled. 5. It is suggested that the observed infradian cycle in body weight may be an expression of an internal metabolic regulatory process in order to set up to species-specific fixed body weight. 6. The adaptive value of such infradian body weight variations is discussed in relation to the bird's migratory behavior.
Introduction Body weights of birds are relevant to many aspects of avian biology, either taxonomy, physiology or ecology, and a great amount of data is found scattered throughout the literature (for reviews see Nice 1938; Baldwin and Kendeigh 1938 ; Amadon
1943; Blake 1956; and more recently, Clark 1979; for a recent survey of body weights of birds see Brough 1983). Besides the more stochastic variations in the body weights of birds depending on such variables as sex, age, year, climate, food availability, geography or climate, at least three cyclic types of weight fluctuations are known in birds: They run parallel to the daily light-dark cycle, to the seasons and to the two migration periods in migrant species. It is well known that birds feeding diurnally lose weight at night and gain weight during the daytime, thus exhibiting a regular daily body weight cycle with minimum levels at dawn and maximum levels in the afternoon (weight increase about 10% of initial body weight; Baldwin and Kendeigh 1983). It has also long been known that many resident birds have higher body weights during winter and lower body weight during the summer months (Clark 1979). The most obvious variations in body weight in birds are found in migratory species. Particularly long-distance migrants deposit large amounts of lipids prior to and during migration both in autumn and spring (Berthold 1975; Blem 1980). Thus migrant species show some of the greatest regular body weight changes with weight gains of 50-100% (for instance garden warblers 80%) above nonmigratory levels. This body weight cycle is related to the birds' migratory habits and is influenced by an endogenous annual rhythm which is, in the field, controlled by the photoperiod cycle of the year (Gwinner 1977, 1981). The deposition of fat is seen as an energetic adjustment to ]migration and the extent of weight increase is related to the distance traveled during migration (Berthold 1973, 1975). Furthermore, the seasonal premigratory fattening is in parallel with a seasonal increase in food intake together with an increase in the efficiency of food and nutrient utilization (Bairlein
860
F. Bairlein: Semimonthly rhythm of body weight in the garden warbler
1985b). During an analysis of nutritional adaptations in the premigratory fattening period in the garden warbler, a long-distance migrant which breeds in the western Palaearctic and winters in Africa south of the Sahara (Zink 1973), birds were weighed daily. In doing so over several months a new type of cyclic variation in the body weights of the birds was detected. Its period was about 2 to 3 weeks. These characteristic, about semimonthly, fluctuations have been analysed in more detail. They may offer a new approach to the analysis of species-specific body weight regulations, at least in migratory bird species. Materials and methods Two groups of birds were used. The first one was a group of 16 garden warblers either handraised as nestlings or caught as juveniles from a natural population near K61n (Western Germany) in July 1982. The birds were maintained individually under controlled laboratory conditions (LD 12 :12; 20 +_ 1 ~ 50-60% R.H. ; constant nocturnal dim light of 0.01 lux). Until the end of April 1983, food consumption was measured in these birds during premigratory fattening (Bairlein 1985b). In May 1983 they were divided into a control group and two experimental groups to test influences of different diets on the birds' seasonal body weight cycles (Bairlein, in preparation). The birds' body weights were recorded daily. In order to exclude the possibility that the observed variations in body weight were due to the fact that the birds had been kept under laboratory conditions for about one year, a second group of 19 nestlings was handraised in June 1984. The birds were maintained under the same laboratory conditions as described for the above groups from mid July 1984 onwards. All birds were fed ad libitum on a diet prepared from dried insects, casein, saccharose, starch, vegetable oil, minerals, vitamins and cellulose, containing 14% (by wet weight) crude protein, 10% crude fat and 5% digestible carbohydrates (for a more detailed description see Bairlein 1986). The control birds received this standard food mixture continuously; the experimental groups received nutrient (protein, fat, carbohydrate) reduced diets temporarily. Water was also available ad libitum. The birds were weighed daily (except weekends) at the onset of light. In order to determine the influences of not weighing the birds on the weekends, all birds were additionally weighed daily including the weekends, during two six week periods. During the first year food intake and fecal production for the previous 24 h period were recorded for the first group of birds at least once every two weeks as previously described (Bairlein 1985b). Furthermore, food intake and fecal production were recorded daily in twelve birds of the second group over a period of 18 days. With these data the daily food intake and the efficiency of food utilization ((food intake - fecal loss)/food intake)) were calculated. Moreover, the nocturnal activity (migratory restlessness; Berthold et al. 1972 a) of each bird was continuously recorded by using cages with electromechanical perches and a microcomputer unit. Once a week the moult stage of each bird was checked. From February 1985 to November 1985 five birds were kept under an artificial moon light cycle. Within a period of 30 days the intensity of the illumination changed from 0.01 lux (simulated new moon conditions) to 0.3 lux (simulated full moon conditions; see Fig. 4). Furthermore, the daily moonlight
period (moonrise and moonset, respectively) was shifted according to the natural run of the moon (Neumann 1981, and personal communication). During the new moon phase the same constant dim light of 0.01 lux was maintained as in the other experiments. Without such a dim light the natural behavior of the garden warbler, the nocturnal activity (migratory restlessness) is suppressed even if the birds are optimally disposed for migration (Czeschlik 1977). The data were analysed by using SPSS- ( N i e e t al. 1975) and BMDP- (Dixon et al. 1981) statistical computer software and particularly by using the methods of time series analysis (univariate spectral analysis; e.g. Bloomfield 1976; Koopmans 1974; Leiner 1978). The most prominent cycle of each time interval tested was obtained by calculating periodograms using fast Fourier transform procedures as well as autocorrelation functions. Since spectral analysis is dependent on the time intervals used for calculation, all period lengths shown in this paper were calculated using the same lengths of intervals. Furthermore, period lengths obtained by the spectral analysis procedure were examined by means of peak to peak intervals for each individual bird.
Results
As seen in Figs. 1 and 2, garden warblers maintained under controlled laboratory conditions for 30 and 18 months, respectively, showed regular fluctuations in body weight in the range of a few weeks only. These regular changes were expressed independent of the seasonal, premigratory body weight increase. Such periods of high body weights in migrant bird species are associated with the birds' migratory behavior and are known both from the laboratory and the field as characteristic of the circannual rhythm (Berthold et al. 1972a; Bairlein 1985b). But at least in warblers main-
20-
~
Z 20-
0
120
2 0
3 0 time
;80
600
720
8L~O
(days)
Fig. 1. Body weight recordings for three individual garden warblers housed under controlled laboratory conditions and fed the standard diet for 30 months (group 1 ; see text). Day 0 refers to July 20, 1983
F, Bairlein: Semimonthly rhythm of body weight in the garden warbler
861
Table 1. Relationship between the mean period length of the body weight cycles and the seasonal level in body weight, and diet consumed (for statistics see text) 20-
/
J .c 2 0 -
|
J
/ /
I
>, o 20-
i 120
240 time
360 [do
480
Mean period length (days)"
n (birds)
Seasonal body weight
Diet
16.7 __ 1.6 (14.019.0)
12
high
standard
21.6 __+2.2 (15.9-24.9)
12
low
standard
19.3 _ 4.3 (14.1-25.6)
6
high
reduced lipid
22.5 • 6.4 (16.0-34.0)
6
low
reduced lipid
14.6 _ 2.6 (10.7-16.0)
5
17.5_+ 3.6 (12.3-26.0)
11
reduced carbohydrates reduced protein
ys)
Mean, standard deviation and range
Fig. 2. Body weight recordings of three other garden warblers kept under controlled laboratory conditions and fed the standard diet for 18 months (group 2; see text), D a y 0 refers to July 9, 1984
tained under constant laboratory conditions for a long time, the seasonal course of migratory fattening (onset, duration, end) became less obvious with time although it was still weakly present after three years (Berthold et al. 1972 a). In addition, the body weight increase in laboratory birds is much more pronounced during periods related to autumn migration than to spring migration (Berthold et al. 1972a; Bairlein 1985b; Gwinner, personal communication). In correspondence with these observations the seasonal weight increases were less obvious particularly in the birds of group 1 (Fig. 1). However, the second group of birds showed two periods with well established seasonal body weight increases, one during the first autumn migration period and a second one about one year later during the birds' second autumn (Fig. 2). During such premigratory weight gain periods garden warblers normally reach weights of up to 80% above the nonmigratory levels. The about semimonthly weight fluctuations were more pronounced during the periods of high seasonal body weight (amplitudes of the fluctuations of up to 32% of the corresponding initial weight) than during the periods of low body weight (amplitudes only up to 19%). To analyse these complex long-term weight recordings univariate spectral analysis methods were used. By these statistical methods it could be tested first, if there was any significant regular variation and second, the domain frequency of the underly-
o
301 20 |
~E
9 0o
10 l
n=47
r =-0,221(ns) 00 9 9
9 90
99 9
,9 ~ 1 4 9 1 7 6 1 97 6 1 4 9
9
9 9
9 9 oe
9
o9
time Cnurnber ofcycteJ Fig. 3. An example for the relationship between the Iength of consecutive weight cycles of one bird and the experimental time (number of cycle). For further explanations see text
ing cycle and the length of the period could be evaluated. All of the 35 birds tested showed a significant regular variation in body weight. For birds always feeding on the standard diet the lengths of cycle periods ranged from 14.0 to 24.9 days with a mean period of 18.3_+2.2 days irrespective of the different seasonal levels in body weight (mean_+ SD; Table 1). From the graphical expression of the weight recordings (Figs. I and 2) one could suppose that the semimonthly weight variations became less pronounced and less regular as the experiment progressed. Therefore, the period lengths of consecutive cycles were calculated for each bird and plotted against cycle number (for an example see Fig. 3). No significant linear trends either in the length of the cycle periods or in the variation of
862
F. Bairlein: Semimonthly rhythm of body weight in the garden warbler
the period values were found; the periods were stable with time during the run of the experiment. As further seen from Table 1, the mean domain period depended on the absolute seasonal level of body weight and was influenced by the nutritional composition of the diet. At high body weight levels, due to migratory fattening, the mean length of the cycle was significantly shorter than during the lower body weight phases (U-test; P
