Endogenous Rhythms of Seasonal Migratory Body ...

Endogenous Rhythms of Seasonal Migratory Body Mass Changes and Nocturnal Restlessness in Different Populations of Northern Wheatear Oenanthe oenanthe Ivan Maggini1 and Franz Bairlein Institute of Avian Research “Vogelwarte Helgoland,” Wilhelmshaven, Germany Abstract The Northern Wheatear (Oenanthe oenanthe) is a migratory bird species that shows different strategies of migration between populations, adapted to cope with different ecological barriers. This raises the question whether and to which extent these adaptations are endogenously determined. We studied seasonal patterns of body mass change and nocturnal restlessness in wheatears from Iceland, which face an initial sea crossing of at least 800 km; from Norway, which fly a similar distance as Icelandic birds but without a long sea crossing; and from Morocco, which fly a shorter distance to reach their wintering grounds. To isolate the endogenous component of the regulation of these migratory traits, we kept the wheatears in a “common garden,” all 3 populations experiencing the same environmental conditions and a constant photoperiod during their first year of life. Icelandic birds showed a greater increase of their body mass in autumn than the other 2 populations, indicating preparation for the initial barrier crossing. The autumnal timing of nocturnal restlessness and the total activity during autumn were related to the distance to be covered, although the differences between populations were smaller than expected. In all 3 populations, body mass increased to a greater extent in autumn than in spring, whereas nocturnal activity was higher in spring than in autumn. This suggests that the endogenous program responds to specific seasonal needs, with more time invested in storing fuel for a safe journey in autumn and more time invested in flying to reach the breeding grounds early in spring. Contrary to expectations, the timing of onset of body mass increase and nocturnal restlessness in spring did not differ between populations. This might be explained by the lack of external cues, most likely photoperiod, which are responsible for the fine tuning of the expression of migratory behavior. Key words Oenanthe oenanthe, bird migration, seasonal rhythms, body mass changes, nocturnal restlessness, endogenous program

The Northern Wheatear (Oenanthe oenanthe) is a long-distance migratory passerine bird distributed over a wide breeding range across the Holarctic region

(Collar, 2005). All its populations overwinter in Sub-Saharan Africa (Keith et al., 1996), resulting in a highly diverse migration system within the species.

1. To whom all correspondence should be addressed: Ivan Maggini, Institute of Avian Research “Vogelwarte Helgoland,” An der Vogelwarte 21, D-26386 Wilhelmshaven, Germany; e-mail: [email protected]. JOURNAL OF BIOLOGICAL RHYTHMS, Vol. 25 No. 4, August 2010 268-276 DOI: 10.1177/0748730410373442 © 2010 SAGE Publications

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Maggini, Bairlein / SEASONAL RHYTHMS IN NORTHERN WHEATEARS 269

Different populations encounter distinct ecological barriers on the way, for example, deserts or seas, and cover different migratory distances ranging from relatively short desert crossings (spp. seebohmi) (Browne, 1982; Förschler et al., 2008) to extremely long journeys of many thousands of kilometers, which fall within the longest among passerines (e.g., birds of Alaska that cross the Asian continent to overwinter in eastern Africa) (Cramp, 1988). Because of this high variability and the fact that it is comparatively easy to observe this species in the field and to keep it in captivity as well, the Northern Wheatear has become a useful model species to investigate migratory strategies in birds (Bairlein, 2008). Field observations have shown differences in stopover behavior between wheatears facing different migratory routes (Dierschke and Delingat, 2001) and have enabled the formulation of hypotheses relating to optimal migratory strategies in this species (Delingat et al., 2006, 2008). Migrating wheatears take account of environmental cues during migration, such as weather, predation risk, and food availability (Schmaljohann and Dierschke, 2005), but the question remains if and to what extent their migratory behavior is based on endogenous mechanisms as well. An endogenous control of migratory traits was first described from studies of Willow Warblers (Phylloscopus trochilus), which showed seasonal rhythms of body mass change, nocturnal restlessness, and moult even under constant conditions (Gwinner, 1968). The occurrence of such traits repeated itself in cycles of approximately 1 year for many years, hence, the definition as a circannual rhythm. Circannual rhythms have since been demonstrated to exist in many species of birds and other organisms (Gwinner, 1986; Gwinner and Dittami, 1990; Guyomarc’h and Guyomarc’h, 1995; Holberton and Able, 1992; Cadée et al., 1996; Berthold et al., 2001; Piersma, 2002). In birds, migratory species as well as tropical residents have been found to show rhythmicity in reproduction and moult (e.g., Gwinner and Dittami, 1990; Hartley and Hustler, 1993; Helm and Gwinner, 1999; Styrsky et al., 2004). The observed seasonality implies an endogenous control because it occurs even in the absence of environmental cues (Gwinner, 1996a, 1996b, 2003). At least 3 important features relating to migration have been shown to underlie endogenous circannual rhythmicity: 1) migratory fattening, the increase of body mass through accumulation of fat as an energy reserve for migratory flight (Berthold, 1976; Bairlein

and Gwinner, 1994); 2) nocturnal restlessness (Zugunruhe), an indication of the disposition to perform migratory flight when the bird is caged (Berthold et al., 1972; Berthold and Querner, 1981; Gwinner, 1987; Berthold, 1988); and 3) migratory orientation and directional changes, reflecting the changes that occur during actual migration (Gwinner and Wiltschko, 1978, 1980; Helbig et al., 1989; Wiltschko and Wiltschko, 2003). These features have been shown to occur irrespective of environmental cues in some species (e.g., European warblers; see Gwinner, 1996a, 1996b) but may need some additional cues in other species, as shown by studies in which birds required a simulation of the magnetic field over the migratory route (Beck and Wiltschko, 1988; Fransson et al., 2001; Kullberg et al., 2003). The only external stimulus that has been shown capable of modulating the time course of nocturnal restlessness, as well as most other seasonally occurring behavior (moult, testis size, body weight), is photoperiod (Gwinner, 1996a, 1996b, 2003; Dawson et al., 2001; Gwinner and Helm, 2003). Previous studies have shown that the amount of fuel stored and of nocturnal restlessness were linked to the migratory distances to be covered in different species of European warblers (Berthold, 1974, 1988; Gwinner, 1990). The same was found between different populations of the same species (Berthold and Querner, 1981). Furthermore, different conspecific populations have been shown to exhibit different photosensitivity, reacting in a specific way to manipulations of the photoperiod (Gwinner, 1996a, 2003; Gwinner and Helm, 2003; Helm and Gwinner, 2005). In order to understand the mechanism controlling the different migratory strategies in the Northern Wheatear, we needed to study whether they possess an endogenous control. Additionally, we wanted to determine whether different populations show innate adaptations to the various ecological barriers and different distances to be covered. We examined 3 populations with different migratory routes, namely birds from Iceland (spp. leucorhoa), from southern Norway, and from southern Morocco. While the Icelandic birds have to cross the northern Atlantic for at least 800 to 900 km in order to reach their first autumn stopover sites in the British Isles (Timmermann, 1949), birds from the Norwegian population have a shorter crossing over the North Sea of 600 km at most, with the possibility of detouring over Denmark. For birds of both populations, the rest of the southbound migration to their Sub-Saharan African wintering grounds is rather similar, mainly over land, except crossing the

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270 JOURNAL OF BIOLOGICAL RHYTHMS / August 2010

western Mediterranean Sea. The birds from Morocco (spp. seebohmi) have to fly a much shorter distance and all over land (Browne, 1982; Thévenot et al., 2003; Förschler et al., 2008). It has been proposed that Icelandic wheatears may even be able to reach their African wintering quarters in a single nonstop flight over the entire northern Atlantic (Alerstam, 1996; Thorup et al., 2006), but this is still debated (Delingat et al., 2008). We used a common garden approach keeping hand-raised birds under the same controlled conditions during their first year of life and measuring their seasonal changes in body mass and nocturnal restlessness and posed the following 2 questions: 1) Does the migratory behavior of Northern Wheatears have an endogenous basis? If so, they should exhibit seasonal variation in nocturnal activity, reflecting their nocturnal migration behavior in the wild, even under constant conditions without environmental cues. 2) Is the different migratory behavior of populations based on population-specific variation in the endogenous basis of migratory behavior? If so, the 3 populations should show differences in the extent of nocturnal migratory activity and body mass change.

and a standardized food containing dried insects and other additives (Bairlein, 1986). Measurements The activity of the wheatears was automatically recorded by highly motion-sensitive microphones attached to the cage walls. Each time the bird moved, an impulse was transmitted to a converting device (developed by R. Nagel, Wilhelmshaven, Germany). To avoid the recording of occasional nonmigratory activity, we set a threshold of 3 impulses per second before it was recorded as an activity count. Another device (developed by S. F. Becker, Bremen, Germany) created a CSV file summarizing the activity counts over 15-minute intervals. Nocturnal restlessness was recorded in 16 birds from Iceland, 15 birds from Norway, and 9 birds from Morocco. All birds were weighed to the nearest 0.1 g twice a week during the whole period of the experiments. Weighing was always done in the morning, just after the lights in the rooms went on. The measurements were stopped around mid-May the following spring. Nocturnal Restlessness

MATERIALS AND METHODS Study Birds We took under license 27 nestling Northern Wheatears from Norway (13 in 2005 and 14 in 2006), 17 from Iceland (9 in 2005 and 8 in 2006), and 10 from Morocco (all in 2008) when they were 5 to 10 days old. At this age, their eyes are still closed, and they sit in nests located inside cavities where almost no light enters from outside. Within 2 to 3 days, the nestlings were transported to the Institute of Avian Research in Wilhelmshaven (Germany), where they were hand raised indoors in controlled conditions and subsequently kept in individual cages of 50 × 40 × 40 cm in rooms with no windows and a constant temperature of 20 °C ± 2 °C. For the first 60 days of life, they experienced a daily light-dark cycle of 14L:10D, after which it was switched to 12L:12D and kept constant throughout the following 9 to 10 months. In this paper, we have taken the day of photoperiodic switch as the beginning of the experimental period (day 0). After being taken from their nests, the birds were fed by hand with mealworms until they were able to feed independently. At this point, their diet constituted a mix of live mealworms

For every night, we calculated the total nocturnal activity as the number of 15-minute intervals with activity. An interval was counted if it included more than 5 activity counts. The first and the last hour of the night were not taken into account in order to avoid including nonmigratory activity around dusk and dawn, respectively. To estimate the date of onset and end of nocturnal restlessness in autumn and spring, we first divided the season in 2 parts: the autumnal phase being from the beginning of the measurements on the day of photoperiodic switch from 14L:10D to 12L:12D (day 0, at an age of approximately 60 days) until 31 December, and the spring phase beginning the following year on 1 February and lasting until the end of the measurements in early May. For every bird, we then calculated 5-day running means of nocturnal activity in order to smooth the curve. Onset and end of nocturnal activity were identified in the first 5-day periods when the mean activity went over (respectively under) a threshold of 4 intervals per night (which corresponds to 10% of one night). The exact day of onset and end was then determined as the first (respectively last) day with an activity over (respectively under) the threshold within the previously defined 5-day period. In some cases



(7 birds in autumn and 4 birds in spring; 18% and 10%, respectively), the mean 5-day activity was not constantly over the threshold throughout the season. For these cases, we applied a more complex method for estimating onset and end of activity (see Supplementary Material online). In cases where the threshold was not exceeded for more than five 5-day periods within the whole season (autumn or spring), we excluded the birds from the analysis (3 birds in autumn and 6 birds in spring; 7.5% and 15%, respectively). In total, we could determine the onset of activity in autumn in 53% (21 of 40 birds), the end in autumn in 70% (n = 28), and the onset in spring in 80% (n = 32) of the birds. The low percentage of birds for which we could determine the onset of activity in autumn is explained by technical problems in 2005, which did not allow a timely beginning of recordings. These started when almost all birds had already begun their autumnal restlessness. The intensity of nocturnal restlessness in autumn was calculated as the mean activity of all nights between the estimated date of onset and end of activity for the 16 birds in which both dates were determined. In cases where only the date of onset (5 birds) was available, the mean was calculated between this date and the end of the season. In cases where only the date of end was available (16 birds), the mean was calculated between the beginning of the season and this date. The intensity of nocturnal restlessness in spring was calculated as the mean activity of all nights between the estimated date of onset and the end of the measurements. No bird had terminated his spring nocturnal restlessness by the end of measurements (Gwinner and Czeschlik, 1978). In total, mean intensity of activity was calculated in 37 of 40 birds (93%) in autumn and in 34 of 40 birds (85%) in spring. Body Mass In order to estimate the extent of body mass gain, often called fuel load, we first estimated the lean body mass for every bird by taking its lowest body mass over the whole season. We then calculated fuel load by using the formula (BM – LBM)/LBM, where BM is the actual body mass, and LBM is the lean body mass. To determine the onset of the increase in body mass in both autumn and spring, we first calculated mean fuel load for every bird over 5-day periods. As soon as there was a continuous increase of fuel load for at least 3 consecutive 5-day periods, we took the third day of the first period of this series as the autumnal onset of the increase in body mass. For the estimate of the onset in spring, we used the same method by

taking the first 3 consecutive increasing 5-day means in fuel load after 1 January. In total, we were able to estimate onset of body mass gain in 53 of 54 birds (98%) in autumn and in 46 of 54 birds (85%) in spring. Population-specific extent of fuel load was calculated as the mean fuel load during a “plateau” phase (for definition of the “plateau” phase, see Suppl. Material), when body mass was almost constant at maximum values. “Plateau” phases and thus fuel loads were determined separately for autumn and spring, respectively. Data Analysis We estimated onset, end, and intensity of nocturnal restlessness in autumn, onset and intensity in spring, and onset and intensity of body mass gain in autumn and spring. For all 9 variables, we ran a linear model with population, sex, and year of sampling as covariates. The model was simplified by stepwise eliminating nonsignificant terms until reaching a best-fit model according to the lowest Akaike information criterion (AIC). Statistical testing was performed using the software R 2.8.0 (R Development Core Team, 2008), and the models were checked for heteroscedasticity, nonnormality of errors, and influence of outliers by plotting residuals as described in Crawley (2007). We found no reason to reject the outcome of the models. In cases where there were significant effects of population, we compared the populations pairwise with Wilcoxon rank-sum tests. RESULTS Spontaneous Seasonal Changes in Nocturnal Restlessness All 3 populations revealed spontaneous seasonal patterns of nocturnal restlessness (Fig. 1). The estimated dates of onset and end, as well as the intensity of nocturnal restlessness in autumn and spring, are summarized in Table 1. Linear models (LMs) showed no effects of sex and year of sampling on date of onset and end and intensity of nocturnal restlessness in autumn, respectively. In spring, sex had a significant effect on onset of restlessness (Maggini and Bairlein, in preparation), but this effect was similar in all 3 populations. No significant effect of year of sampling on the onset and intensity of nocturnal restlessness in spring, nor of sex on the intensity in spring, was revealed by the LM. The outcomes of the LM are presented in the online Supplementary



between Icelandic and Moroccan birds (Wilcoxon rank-sum test: W = 2, p = 0.008) and between Norwegian and Moroccan birds (Wilcoxon rank-sum test: W = 0, p = 0.022) but not so between Icelandic and Norwegian birds (Wilcoxon rank-sum test: W = 12, p = 0.513). The onset of autumnal nocturnal restlessness in Moroccan birds was later than in both other populations (Table 1). The end (LM: p = 0.753, adj. r2 = 0.594) and the intensity (LM: p = 0.831, adj. r2 = 0.128) of nocturnal restlessness in autumn as well as the onset (LM: p = 0.119, adj. r2 = 0.404) and the intensity (LM: p = 0.836, adj. r2 = –0.224) of nocturnal restlessness in spring did not differ significantly between populations. Figure 1. Seasonal patterns of nocturnal restlessness in 3 populations of Northern Wheatears Within all 3 populations, kept in captivity. Ten-day mean activities are plotted. Period 1 is the period beginning on the day the intensity of nocturnal of photoperiodic switch from 14L:10D to 12L:12D (day 0). The means refer to the number of restlessness was higher in 15-minute intervals with activity in one night (the maximum would be 40 intervals per night, referring to the 10 hours per night considered; see Materials and Methods). Error bars show stanspring than in autumn dard errors of the mean, and the numbers above each point indicate the Ns. (Table 1). This difference was significant in Icelandic birds (Wilcoxon signed-rank test: Table 1. Date of onset and end and intensity of nocturnal restV = 7.5, p = 0.015) but not in Norwegian (Wilcoxon lessness in autumn and spring, respectively, in 3 populations of signed-rank test: V = 26, p = 0.191) or Moroccan birds Northern Wheatears in captivity. (Wilcoxon signed-rank test: V = 8, p = 0.688). Iceland Norway Morocco In order to obtain a proxy for the innate basis of the migration distance of the different populations N Mean ± SD N Mean ± SD N Mean ± SD (cf. Gwinner, 1986), we multiplied the mean intensity Autumn of nocturnal restlessness by the mean duration of Onset (d)a 6 8.8 ± 3.6 3 6.3 ± 0.6 7 27.3 ± 8.2 End (d)a 7 97.7 ± 22.1 11 92.8 ± 27.4 9 93.6 ± 14.9 migratory activity (difference in onset and end of Intensityb 12 12.00 ± 5.16 15 12.36 ± 4.44 9 14.04 ± 4.40 activity) in autumn. While Icelandic and Norwegian Spring birds were very similar in their total migratory activOnset (d)a 14 212.9 ± 24.0 13 227.6 ± 34.2 5 235.0 ± 25.6 ity (1067 fifteen-minute intervals and 1069 intervals, Intensityb 15 15.32 ± 6.40 13 15.04 ± 5.92 6 17.00 ± 6.76 respectively), the Moroccan birds showed a lower a. Days are counted from the day of photoperiodic switch from total (931 intervals). 14L:10D to 12L:12D (day 0). b. Mean number of intervals with activity in one night between date of onset and date of end of activity.

Material. However, onset of autumnal nocturnal migratory activity differed between populations (LM: p = 0.001, adj. r2 = 0.873). The difference was significant

Spontaneous Seasonal Changes in Body Mass The seasonal pattern of fuel load of the 3 populations is shown in Figure 2. The dates of onset of body mass increase, as well as the extent of maximum fuel load in autumn and in spring, are summarized in



onset of fueling in spring (Maggini and Bairlein, in preparation). However, as this was similar in all 3 populations, it did not affect the comparison of the 3 populations. LM analysis (for details, see online Supplementary Material) revealed significant differences between populations in both the date of onset of fueling (LM: p < 0.001, adj. r2 = 0.263) and extent of fuel load in autumn (LM: p < 0.001, adj. r2 = 0.300). The difference in onset of fueling was significant between Icelandic and Norwegian birds (Wilcoxon rank-sum test: W = 101, p = 0.007) and between Icelandic and Moroccan birds (Wilcoxon rank-sum test: W = 13.5, p < 0.001), respectively, but slightly nonsignificant Figure 2. Seasonal patterns of changes in fuel load, calculated as (BM – LBM)/LBM in 3 populabetween Norwegian and tions of Northern Wheatears kept in captivity under constant photoperiod. Ten-day means are Moroccan birds (Wilcoxon plotted. Period 1 is the period beginning on the day of photoperiodic switch from 14L:10D to rank-sum test: W = 82, p = 12L:12D (day 0). Error bars show standard errors of the mean, and the numbers above each point indicate the Ns. 0.061). Icelandic birds began increasing their body mass first, followed by Norwegian Table 2. Date of onset and extent of body mass gain in and then Moroccan birds (Table 2). The extent of fuel autumn and spring in 3 populations of Northern Wheatears in load was significantly different between Icelandic captivity. and Norwegian birds (Wilcoxon rank-sum test: W = Iceland Norway Morocco 369, p < 0.001) and between Icelandic and Moroccan birds (Wilcoxon rank-sum test: W = 125, p = 0.017) but N Mean ± SD N Mean ± SD N Mean ± SD not so between Norwegian and Moroccan birds Autumn a (Wilcoxon rank-sum test: W = 84, p = 0.084). Icelandic Onset (d) 15 –4.9 ± 8.4 27 2.7 ± 7.4 10 7.0 ± 3.2 Max. fuel 16 0.602 ± 0.173 28 0.417 ± 0.107 10 0.476 ± 0.072 birds showed the highest mean autumnal maximum loadb fuel load (Table 2). The onset of body mass gain Spring (LM: p = 0.100, adj. r2 = 0.390) as well as the extent Onset (d)a 15 197.3 ± 25.7 22 184.2 ± 26.8 9 199.4 ± 30.3 of maximum fuel load (LM: p = 0.101, adj. r2 = 0.217) Max. fuel 14 0.436 ± 0.275 21 0.300 ± 0.092 9 0.385 ± 0.254 in spring did not differ significantly between loadb populations. a. Days are counted from the day of photoperiodic switch from Maximum fuel load was higher in autumn than in 14L:10D to 12L:12D (day 0). b. Fuel load calculated as (BM – LBM)/LBM, extent of maximum spring in all populations but significantly so only in fuel load calculated as the mean fuel load over the “plateau” phase Icelandic (Wilcoxon signed-rank test: V = 93, p = 0.009) (see text). and Norwegian birds (Wilcoxon signed-rank test: V = 216, p < 0.001), while the difference was nonsignificant Table 2. LM showed no significant effects of sex and in Moroccan birds (Wilcoxon signed-rank test: V = 28, year of sampling in onset of fueling and extent of fuel p = 0.570). load in autumn but a significant effect of sex in the Downloaded from jbr.sagepub.com at IBIT-INFORMATIONS-,BIBLIOTHEK on August 28, 2010


DISCUSSION The expression of spontaneous seasonal variations in nocturnal restlessness and body mass in the Northern Wheatear despite the lack of environmental cues confirms that these traits are under an endogenous regulation. This is in line with expectations because in all migratory species studied to date, it could be shown that they exhibit changes in nocturnal activity and body mass even when lacking environmental cues (Gwinner, 1996a). Knowledge of the endogenous component of migratory behavior helps us to understand the mechanisms underlying the behavior observed in the field (e.g., Delingat et al., 2006, 2008). Furthermore, our data show that these endogenous traits are population specific, reflecting the different migratory behavior of populations coping with crossing different ecological barriers and different overall migration distances. Northern Wheatears showed nocturnal migratory restlessness twice across the experiment, corresponding in the main to autumn and spring migration in free-living conspecifics. The expression of this behavior varied between populations: Icelandic and Norwegian birds started their autumnal nocturnal restlessness earlier in the season than Moroccan birds. The intensity and the end of nocturnal restlessness, however, did not vary significantly between populations, resulting in different total amounts of activity over the season. While it has been shown in warblers (Berthold, 1974, 1988; Berthold and Querner, 1981; Gwinner, 1990) that the total amount of nocturnal activity in caged birds is closely correlated to the overall flight distance of free-living conspecifics, the expected flight distance and the observed total activity in the Northern Wheatear were not that closely related to each other. In particular, we expected that Moroccan birds should have shown a much smaller amount of total migratory activity as compared to the 2 other populations because the migration distance of Moroccan birds in the wild is just about one third of that of the 2 other populations. Likely, external cues are involved in the timing of migratory activity as well. It has been shown that fine tuning of the timing of nocturnal activity is regulated by photoperiod (Gwinner, 1996a, 1996b, 2003; Dawson et al., 2001; Gwinner and Helm, 2003) and that the response to photoperiodic cues is population specific (e.g., Coppack et al., 2003; Helm and Gwinner, 2005). The mean intensity of nocturnal restlessness in spring was higher than in autumn. Considering the mean intensity as a proxy for average flying effort

and thus flying distance in one night, this difference may indicate that the wheatears are endogenously predisposed to fly longer bouts in spring than in autumn. There is evidence that overall migration speed in long-distance migratory birds is higher in spring than in autumn (Fransson, 1995; Yohannes et al., 2009). Icelandic birds showed higher maximum fuel load in autumn than the 2 other populations. This reflects the energetic needs of the Icelandic birds to prepare for a longer barrier crossing as compared to the 2 other populations (Dierschke et al., 2005; Delingat et al., 2008). It has been demonstrated that during spring migration, wheatears fly mostly in short bouts with daily stopovers (Delingat et al., 2006), and this may apply to autumn migration as well. In this regard, wheatears differ from other long-distance migrating species that carry higher amounts of fat during migration (e.g., Moreau and Dolp, 1970; Schaub and Jenni, 2000). Such species, however, are probably more constrained by the availability of suitable habitats for refueling, whereas wheatears are likely to find refueling opportunities almost everywhere along their migration route, even under conditions as harsh as in the desert (personal observation). The timing of onset of body mass gain in autumn differed significantly between populations. Icelandic wheatears began first, followed by Norwegian and Moroccan birds. Given that Icelandic and Norwegian wheatears did not differ in the date of onset of nocturnal activity, it follows that the time lag between onset of body mass gain and onset of activity was around 10 days longer in Icelandic birds. This may be explained by the observation that Icelandic wheatears accumulate more reserves than Norwegian birds in autumn and therefore need to invest more time in fuel deposition. In all populations studied, the seasonal maximal fuel load in the captive birds was higher in autumn than in spring. Combined with the higher rates of nocturnal activity, this is explained by an adaptation to the seasonal need to reach the breeding quarters earlier in spring. Because accumulating fuel requires time, reducing this time results in accelerated overall migration speed (Hedenström and Alerstam, 1997). Field observations revealed that during spring migration, wheatears carry only moderate fuel loads (Delingat et al., 2006) and that they rarely stop over for more than 1 day en route, except at coastal sites where they have to prepare for sea crossing (Delingat et al., 2008). Our results demonstrate that the Northern Wheatear disposes of an endogenous basis for the control of



timing and intensity of traits linked to migration and that different populations with different migratory habits differ in their endogenously predisposed behavior. However, wheatears do not rely exclusively on the endogenous program but need external cues for fine regulation of migration. This guarantees the behavioral flexibility that is necessary to cope with unpredictable changes in the environment. However, an innate internal clock provides the basic implementation of the major events related to migration. The way this internal clock works is still largely unknown (Wikelski et al., 2008), and future research will have to concentrate on this aspect in order to understand how the endogenous program interacts with environmental cues to shape the migratory behavior of different bird species and populations.

ACKNOWLEDGMENTS The authors thank Rolf Nagel, Simon Fabian Becker, and Ulrike Strauss for their contribution to the study, Nigel Richards and three anonymous reviewers for comments on an earlier version of the paper. The project was funded by the Deutsche Forschungsgemeinschaft (DFG). NOTE Supplementary online material for this article is available on the journal’s Web site: http://jbr.sagepub .com/supplemental. REFERENCES Alerstam T (1996) The geographical scale factor in orientation of migrating birds. J Exp Biol 199:9-19. Bairlein F (1986) Ein standardisiertes futter für ernährungsuntersuchungen an omnivoren kleinvögeln. J Ornithol 127:338-340. Bairlein F (2008) The mysteries of bird migration: still much to be learnt. Brit Birds 101:68-81. Bairlein F and Gwinner E (1994) Nutritional mechanisms and temporal control of migratory energy accumulation in birds. Annu Rev Nutr 14:187-215. Beck W and Wiltschko W (1988) Magnetic factors control the migratory direction of pied flycatchers (Ficedula hypoleuca Pallas). Proc Int Congr Ornithol 19:1955-1962. Berthold P (1974) Circannuale periodik bei grasmücken (Sylvia). III: periodik der mauser, der nachtunruhe und des körpergewichtes bei mediterranen arten mit unterschiedlichem zugverhalten. J Ornithol 115:251-272.

Berthold P (1976) Über den einfluß der fettdeposition auf die zugunruhe bei der gartengrasmücke (Sylvia borin). Vogelwarte 28:263-266. Berthold P (1988) The control of migration in European warblers. Proc Int Congr Ornithol 19:215-249. Berthold P and Querner U (1981) Genetic basis of migratory behaviour in European warblers. Science 212:77-79. Berthold P, Gwinner E, and Klein H (1972) Circannuale periodik bei grasmücken. I: periodik des körpergewichtes, der mauser und der nachtunruhe bei Sylvia atricapilla und S. borin unter verschiedenen konstanten bedingungen. J Ornithol 113:407-417. Berthold P, Iovchenko NP, Mohr G, Querner U, and Fertikova KP (2001) Circannual rhythms in the whitethroat, Sylvia communis. Zool Zhurnal 80:1387-1394. Browne PWP (1982) Palaearctic birds wintering in southwest Mauritania: species, distributions and population estimates. Malimbus 4:69-92. Cadée N, Piersma T, and Daan S (1996) Endogenous circannual rhythmicity in a non-passerine migrant, the knot Calidris canutus. Ardea 84:75-84. Collar NJ (2005) Turdidae (thrushes). In Handbook of the Birds of the World, Vol. 10: Cuckoo-shrikes to Thrushes, del Hoyo J, Elliott A, and Christie DA, eds, pp 514-807. Barcelona: Lynx Edicions. Coppack T, Pulido F, Czisch M, Auer DP, and Berthold P (2003) Photoperiodic response may facilitate adaptation to climatic change in long-distance migratory birds. Proc R Soc Lond B 270(Suppl):S43-S46. Cramp S, ed (1988) The Birds of the Western Palaearctic. Vol. 5. Oxford: Oxford University Press. Crawley MJ (2007) The R Book. Chichester (UK): Wiley & Sons Ltd. Dawson A, King VM, Bentley GE, and Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365-380. Delingat J, Dierschke V, Schmaljohann H, Mendel B, and Bairlein F (2006) Daily stopovers as optimal migration strategy in a long-distance migrating passerine: the northern wheatear Oenanthe oenanthe. Ardea 94:593-605. Delingat J, Bairlein F, and Hedenström A (2008) Obligatory barrier crossing and adaptive fuel management in migratory birds: the case of the Atlantic crossing in northern wheatears (Oenanthe oenanthe). Behav Ecol Sociobiol 62:1069-1078. Dierschke V and Delingat J (2001) Stopover behaviour and departure decision of Northern Wheatears, Oenanthe oenanthe, facing different onward non-stop flight distances. Behav Ecol Sociobiol 50:535-545. Dierschke V, Mendel B, and Schmaljohann H (2005) Differential timing of spring migration in northern wheatears Oenanthe oenanthe: hurried males or weak females? Behav Ecol Sociobiol 57:470-480. Förschler M, Metzger B, Maggini I, Neumann R, and Bairlein F (2008) Seebohm’s wheatear Oenanthe oenanthe seebohmi in West Africa. Bull Afr Bird Club 15:242-244. Fransson T (1995) Timing and speed of migration in North and West European populations of Sylvia warblers. J Avian Biol 26:39-48.


276 JOURNAL OF BIOLOGICAL RHYTHMS / August 2010 Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J, and Vallin A (2001) Bird migration: magnetic cues trigger extensive refuelling. Nature 414:35-36. Guyomarc’h C and Guyomarc’h JC (1995) Moulting cycles in European quail (Coturnix coturnix coturnix) under constant photoperiodic conditions. Biol Rhythm Res 26:292-305. Gwinner E (1968) Circannuale periodik als grundlage des jahreszeitlichen funktionswandels bei zugvögeln: untersuchungen am fitis (Phylloscopus trochilus) und am waldlaubsänger (Phylloscopus sibilatrix). J Ornithol 109:70-95. Gwinner E (1986) Circannual Clocks. Berlin: Springer Verlag. Gwinner E (1987) Annual rhythms of gonadal size, migratory disposition and moult in garden warblers (Sylvia borin) exposed in winter to an equatorial or a southern hemisphere photoperiod. Ornis Scand 18:251-256. Gwinner E (1990) Bird Migration: Physiology and Ecophysiology. Berlin: Springer Verlag. Gwinner E (1996a) Circannual clocks in avian reproduction and migration. Ibis 138:47-63. Gwinner E (1996b) Circadian and circannual programmes in avian migration. J Exp Biol 199:39-48. Gwinner E (2003) Circannual rhythms in birds. Curr Op Neurobiol 13:770-778. Gwinner E and Czeschlik D (1978) On the significance of spring migratory restlessness in caged birds. Oikos 30:364-372. Gwinner E and Dittami J (1990) Endogenous reproductive rhythms in a tropical bird. Science 249:906-908. Gwinner E and Helm B (2003) Circannual and circadian contributions to the timing of avian migration. In Avian Migration, Berthold P, Gwinner E, and Sonnenschein E, eds, pp 81-95. Berlin: Springer Verlag. Gwinner E and Wiltschko W (1978) Endogenously controlled changes in migratory direction of the garden warbler, Sylvia borin. J Comp Physiol 125:267-273. Gwinner E and Wiltschko W (1980) Circannual changes in migratory orientation of the garden warbler, Sylvia borin. Behav Ecol 7:73-78. Hartley R and Hustler K (1993) A less-than-annual breeding cycle in a pair of African bat hawks Machaeramphus alcinus. Ibis 135:456-458. Hedenström A and Alerstam T (1997) Optimal fuel loads in migratory birds: distinguishing between time and energy minimization. J Theor Biol 189:227-234. Helbig A, Berthold P, and Wiltschko W (1989) Migratory orientation of blackcaps (Sylvia atricapilla): population-specific shifts of direction during the autumn. Ethology 82:307-315. Helm B and Gwinner E (1999) Timing of postjuvenal molt in African (Saxicola torquata axillaris) and European

(Saxicola torquata rubicola) stonechats: effects of genetic and environmental factors. Avian Sci 1:31-42. Helm B and Gwinner E (2005) Carry-over effects of day length during spring migration. J Ornithol 146:348-354. Holberton RL and Able KP (1992) Persistence of circannual cycles in a migratory bird held in constant dim light. J Comp Physiol A 171:477-481. Keith S, Urban EK, and Fry CH (1996) Birds of Africa. Vol. 4. London: Academic Press. Kullberg C, Lind J, Fransson T, Jakobsson S, and Vallin A (2003) Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia). Proc R Soc Lond B 270:373-378. Moreau RE and Dolp RM (1970) Fat, water, weights and wing-lengths of autumn migrants in transit on the north-west coast of Egypt. Ibis 112:209-228. Piersma T (2002) Shorebird cycles: when it takes 18 months to make a year complete. Naturwissenschaften 89:278-279. R Development Core Team (2008) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Schaub M and Jenni L (2000) Body mass of six long-distance migrant passerine species along the autumn migration route. J Ornithol 141:441-460. Schmaljohann H and Dierschke V (2005) Optimal bird migration and predation risk: a field experiment with northern wheatears Oenanthe oenanthe. J Anim Ecol 74:131-138. Styrsky JD, Berthold P, and Robinson WD (2004) Endogenous control of migration and calendar effects in an intratropical migrant, the yellow-green vireo. Anim Behav 67:1141-1149. Thévenot M, Vernon R, and Bergier P (2003) The Birds of Morocco. Tring (UK): British Ornithologists’ Union. Thorup K, Ortvad TE, and Rabøl J (2006) Do Nearctic northern wheatears (Oenanthe oenanthe leucorhoa) migrate nonstop to Africa? Condor 108:446-451. Timmermann G (1949) Die Vögel Islands. Reykjavik: Leiftur. Wikelski M, Martin LB, Scheuerlein A, Robinson MT, Robinson ND, Helm B, Hau M, and Gwinner E (2008) Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control. Phil Trans R Soc B 363:411-423. Wiltschko R and Wiltschko W (2003) Mechanisms of orientation and navigation in migratory birds. In Avian Migration, Berthold P, Gwinner E, and Sonnenschein E, eds, pp 433-456. Berlin: Springer Verlag. Yohannes E, Biebach H, Nikolaus G, and Pearson DJ (2009) Migration speeds among eleven species of long-distance migrating passerines across Europe, the desert and eastern Africa. J Avian Biol 40:126-134.
