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Keywords:

  • behavioural plasticity;
  • departure direction;
  • departure time;
  • ecological barrier;
  • migration;
  • migratory direction;
  • radiotracking;
  • songbird

Summary

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

1. An innate migration strategy guides birds through space and time. Environmental variation further modulates individual behaviour within a genetically determined frame. In particular, ecological barriers could influence departure direction and its timing. A shift in the migratory direction in response to an ecological barrier could reveal how birds adjust their individual trajectories to environmental cues and body condition.

2. Northern wheatears of the Greenland/Iceland subspecies Oenanthe oenanthe leucorhoa arrive in Western Europe en route from their West African winter range. They then undergo an endogenously controlled shift in migratory direction from north to north-west to cross a large ecological barrier, the North Atlantic. We radiotracked these songbirds departing from Helgoland, a small island in the North Sea, over an unprecedented range of their journey.

3. Here, we show that both birds’ body condition and the wind conditions that they encountered influenced the departure direction significantly. Jointly high fuel loads and favourable wind conditions enabled migrants to cross large stretches of sea. Birds in good condition departed early in the night heading to the sea towards their breeding areas, while birds with low fuel loads and/or flying in poor weather conditions departed in directions leading towards nearby mainland areas during the entire night. These areas could be reached even after setting off late at night.

4. Behavioural adjustment of migratory patterns is a critical adaptation for crossing ecological barriers. The observed variation in departure direction and time in relation to fuel load and wind revealed that these birds have an innate ability to respond by jointly incorporating internal information (body condition) and external information (wind support).


Introduction

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

Naive birds rely on endogenously controlled migration strategies to reach their migratory destinations. These strategies include among others a general spatiotemporal pattern of migration (Berthold 2001), whereby the onset of migration and the general trajectory are genetically determined (Gwinner & Wiltschko 1978; Berthold & Helbig 1992; Gwinner 1996; Conklin et al. 2010).

In many bird species, whose breeding and wintering grounds are separated by large ecological barriers, i.e. mountains, deserts and sea, specific migration strategies evolved that minimize the constraints of such a demanding journey. Genetically determined shifts in the migratory direction allow birds to cross an ecological barrier along a route avoiding the most risky parts (Gwinner & Wiltschko 1978; Hake, Kjellén & Alerstam 2001). Despite this genetically determined general spatiotemporal organization, migrants respond to environmental cues on the ground (Erni et al. 2002; Jenni & Schaub 2003) as well as aloft (Liechti 2006; Schmaljohann, Bruderer & Liechti 2008; Schmaljohann, Liechti & Bruderer 2009) and to their current body condition (e.g. Bairlein 1988; Dierschke, Mendel & Schmaljohann 2005). Physically fit migrants are less likely to detour from the principal migratory direction, if a barrier is ahead, whereas lean birds orient away from the barrier (Alerstam 1978; Sandberg 1994; Sandberg & Moore 1996; Sandberg 2003; Deutschlander & Muheim 2009). There are, however, no studies testing the separate and combined effect of wind condition and fuel load in free-flying birds. In migrants, in which a shift in the migratory direction is linked with the crossing of an ecological barrier, the timing of departure in relation to environmental conditions and body condition is particularly important. Ignoring one crucial factor may lead to failure, because wind alone cannot carry a bird and high fuel loads are useless when flying in strong headwind (Liechti 2006). Migrants need to consider both wind conditions and fuel load, because both factors determine a bird’s potential flight range. Additionally, they have to select among alternative directions to set off, if there are cues on the extent of the barrier in different directions. In summary, migrants cannot rely solely on the endogenously controlled spatiotemporal migration strategy to reach their migratory goals, but need complex adaptations for short-term decisions on barrier crossing and detour migration (Gwinner 1996; Thorup & Rabøl 2001; Alerstam 2001; Henningsson & Alerstam 2005). Following the Lagrangian approach by considering the inner state of a migrant (body condition) and the current dynamic environment (wind) allows to study the phenotypic response in relation to the general spatiotemporal pattern of the migration system (Nathan et al. 2008; Shamoun-Baranes et al. 2010).

The northern wheatear’s (Oenanthe oenanthe L.) subspecies leucorhoa exhibits such a migration pattern with a shift in the migratory direction and an ecological barrier to be crossed. When en route from wintering areas in West Africa (Cramp 1988), the birds first fly north towards Western Europe. They eventually shift their migratory direction towards the north-west to cross via a long flight the North Atlantic and finally reach their breeding grounds (Fig. 1). On Helgoland, a small island in the North Sea, large numbers of leucorhoa northern wheatears (leucorhoa wheatear hereafter) rest during spring migration (Dierschke & Delingat 2001). Birds have no visual cues on potential stopover sites in the open sea towards north-west, but they may collect information on the dimension of the sea barrier in any other direction (Fig. 1). Hence, birds departing from Helgoland have two options. They may head directly towards their breeding areas in a north-westerly direction and cross several hundred kilometres of sea. Alternatively, they may depart in any other direction. If they do so, their next stopover opportunities are relatively near (about 50–100 km or 1–3 h of flight, Fig. 1). Departing to the north-west enables fast migration but is otherwise risky (i.e. no cues on potential stopover sites). It is to the advantage of lean birds and birds facing unfavourable weather conditions to circumvent the barrier initially and to follow the longer but safer pathway over land (Fig. 1). The latter birds would then head towards their breeding areas after refuelling and a wait for favourable wind conditions from a new stopover site. We hypothesize that the genetically determined general strategy for shifting the general migration direction from north to north-west to cross the sea barrier is adjusted jointly by body condition and wind conditions through their influence on the birds’ potential flight range. Thus, we expect that fuel load, wind conditions and visual cues will significantly influence the direction in which leucorhoa wheatears depart from Helgoland.

image

Figure 1.  Location of Helgoland in the North Sea. The bold black arrow pointing towards north-west (315°) indicates the ‘fast and risky’ direct flyway towards the breeding areas on Greenland and Iceland. The other arrows indicate the alternative and safe routes to the nearby coast. Birds departing in these directions would find stopover sites after a 1–3 h flight.

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The timing of departure is also crucial in relation to the birds’ decision about their subsequent migration stage. Birds that choose to depart directly towards the north-west and that anticipate crossing the sea are expected to depart early after sunset to fly all night, as they are nocturnal migrants. Birds leaving in other directions may depart at any time in the night because their next stopover sites can be reached by a short flight. We thus hypothesize that body condition and wind conditions at departure influence the timing of nocturnal departure.

To test these hypotheses, we radio tagged leucorhoa wheatears on Helgoland during spring migration. In contrast to cage experiments (Nievergelt & Liechti 2000), radio tagged birds interact freely with their environment and allow determining the exact departure time and tracking the departure direction for the first 12–15 km of birds’ migration off Helgoland. The tracking range was, therefore, about three times that of tracking radar (cf. Schmaljohann et al. 2008).

Materials and methods

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

Data were collected on the German island of Helgoland (1 km2; 54°11′N, 07°55′E). The distance to the nearest coast in eastern to southern directions is c. 50 km, while birds heading to the north-west face about 750 km of sea (Fig. 1). We trapped northern wheatears during spring 2008 and spring 2009 from the beginning of April to the end of May, the main spring migration period (Dierschke & Delingat 2001). Birds were ringed, aged, sexed and measured according to Svensson (1992) and weighed to the nearest 0·2 g. Fat stores and size of the breast muscle were scored according to Kaiser (1993) and Bairlein (1994). Wing length was used to identify the subspecies: males and females with wing lengths exceeding 102 and 97 mm, respectively, were treated as belonging to the leucorhoa subspecies (Svensson 1992). Ten in 2008 and 21 in 2009 of the overall 278 birds trapped were radio tagged. Leucorhoa wheatears were caught, ringed and radio tagged under licence of the Ministry for Agriculture, the Environment and Rural Areas, Schleswig-Holstein, Germany.

Radiotransmitters were constructed by the Swiss Ornithological Institute in cooperation with the University of Applied Sciences Bern, Switzerland (Naef-Daenzer et al. 2005). Radiotransmitters, including battery and harness, weighed 0·8 g. The transmitters were attached to the leucorhoa wheatears using a Rappole-type harness made from 0·5-mm elastic cord (Rappole & Tipton 1990). Length of leg-loops was adjusted individually to birds (Naef-Daenzer 2007). Because the lowest body mass of the leucorhoa wheatears involved was 21·3 g (mean 29·7 g, SD 5·1 g, n = 31), the mass of the radiotransmitter represents <3·8% (mean: 2·7%) of the bird’s body mass. The relative load was therefore below the recommended 5% limit (Cochran 1980; Caccamise & Hedin 1985). Potential adverse effects on the birds’ behaviour are insubstantial (e.g. Naef-Daenzer, Widmer & Nuber 2001; Rae et al. 2010), and the increase in flight costs is small (Irvine, Leckie & Redpath 2007); though, drag (Bowlin et al. 2010) as well as energy expenditure (Barron, Brawn & Weatherhead 2010) increases. Transmitter life was about 30 days.

Using Yagi 3EL2 hand-held antennas (Vårgårda, Sweden) in combination with YAESU FT-290RII receivers, the detection range was c. 12–15 km. The detection range was determined by using a radiotransmitter on a ferry leaving the island and locating its position every few seconds by means of a GPS device. As birds likely fly at an altitude exceeding that of the test transmitter, this represents a minimum tracking distance. The detection range of the radios is affected by the orientation of the transmitter antenna, if pointing towards the receiver the detection range was 8 km, if oriented perpendicularly towards Helgoland 15 km. We tracked departing birds for on average 18 min (SD 7·5 min, = 26). As a northern wheatear’s airspeed is about 47 km h−1 (Bruderer & Boldt 2001), the duration of tracking also indicated a mean detection range of 14 km (SD 6 km), which coincided well with the detection range obtained by the ferry experiment. We tracked birds every night continuously from sunset till early morning or until departure. The locations of the birds on the island were estimated by triangulation mostly from two to three mobile observers or by a single mobile observer localizing the bird from different positions on the island. During each departure event, birds were radiotracked from the ‘Oberland’ cliff (c. 50 m above sea level and highest area of the island) mostly by one mobile observer. For departing birds, we recorded directions until loss of signal. According to the bearings, birds departed in a straight line from the island. We used last recorded direction before loss of signal as the departure direction. The bearing accuracy was determined by blindfolded tests with fixed radiotransmitters. The average bearing error was 3° (SD 5°, = 49); see also Schmaljohann et al. (2011). Flight altitude cannot be determined with the radiotelemetry settings used in this study. As the island is very small, a potential parallax error in direction estimates is small compared to the bearing accuracy of hand-held antennas (Kenward 2001). Set-off distance between bird and observer was far <500 m (see above); the parallax error in respect to a tracking distance of 15 km would be <2°.

We compared fuel loads rather than body masses because leucorhoa wheatears differ substantially in size (range of wing lengths in this study 97·5–109 mm). We estimated lean body mass from wing length using a linear regression based on 220 ‘lean’ northern wheatears with fat score <2 and muscle score <2 caught on Helgoland in the years 1998–2002 and 2008:

  • image(eqn 1)

(linear regression: = 220, F1,218 = 95·07, adj-R2 = 0·30, <0·0001).

Departure fuel load was calculated for each individual as:

  • image(eqn 2)

We used body mass at capture as departure body mass for ten birds that departed on the night of their capture day. We estimated departure body mass for the other 21 leucorhoa wheatears by remote weighing or by modelling. Our method of remote weighing was to place bowls supplied with mealworms ad libitum on electric balances so that the body mass of individually ringed leucorhoa wheatears could be read repeatedly over time (Schmaljohann & Dierschke 2005). We defined a bird’s departure body mass as its body mass on the evening of departure (after 7 pm). This procedure succeeded for four birds. Departure body mass and fuel deposition rate, as the relative body mass increase over time (Schmaljohann & Dierschke 2005), of the other 17 had to be modelled. Mean minimum stopover duration of these 17 birds was 2·6 days (SD 2·3 days). From intensive research with northern wheatears on Helgoland (Dierschke & Delingat 2001; Dierschke, Mendel & Schmaljohann 2005; Schmaljohann & Dierschke 2005; Delingat et al. 2009; Schmaljohann et al. 2011), we know that the average fuel deposition rate is about 0·09 day−1 proportionally to bird’s lean body mass (see Appendix S1 in Supporting Information).

To estimate the effect of wind on departure decision, we used wind data from the National Oceanic and Atmospheric Administration (NOAA, Boulder, CO, USA; available http://www.cdc.noaa.gov/cdc/data.ncep.reanalysis.derived.html; Kalnay et al. 1996). These data included four different pressure levels (1000, 925, 850, and 700 mbar) representing roughly four altitude intervals (ground level – 445, 445–1145, 1145–2375 and 2375–4000 m). Midnight wind direction and wind speed correlated significantly between adjacent altitudes during the main study period (April – May 2009: Rc–c > 0·84 and RS > 0·76, all < 0·0001). We included midnight wind data for our analyses, because departure time in every case was closest to the 0 a.m. wind data. The individual wind profit was calculated at the four different altitudinal intervals on departure night following Liechit, Hedenström & Alerstam (1994) and Erni et al. (2002) as:

  • image(eqn 3)

Leucorhoa wheatear’s air speed was set to 13 m s−1 (Bruderer & Boldt 2001), and its overall migratory goal was denoted to 315° (direction towards Iceland, Fig. 1). Because flapping and bounding flyers migrate at the altitude with best wind support (Liechti 2006; Schmaljohann, Bruderer & Liechti 2008; Schmaljohann, Liechti & Bruderer 2009), we selected the strongest wind profit per night to describe the potential support each individual might have experienced on its departure.

To assess the effect of the wind profit on the flight range of each bird, we first estimated the bird’s potential nocturnal flight duration. This quantity is a function of departure fuel load:

  • image(eqn 4)

following Delingat, Bairlein & Hedenström (2008). Bird’s flight duration was, however, restricted to the time remaining between departure and sunrise and not until fuel load was depleted, because northern wheatears are nocturnal migrants (Schmaljohann et al. 2011). This nocturnal flight duration was then multiplied by species air speed (13 m s−1 = 47 km h−1; Bruderer & Boldt 2001), which is the flight range in still air restricted for the period between departure and sunrise (restricted flight rangei). To account for the wind profit experienced, we added the nocturnal flight durationi times the wind profiti to the restricted flight rangei in still air:

  • image(eqn 5)

To consider potential long nonstop flights across the Atlantic (cf. Thorup, Ortvad & Rabøl 2006), we estimated birds’ maximum flight ranges based on the assumption that they would experience the same wind condition along their route as they did during their departure, whereby total flight duration was defined as birds’ flight duration until fuel loads were depleted, see eqn 4:

  • image(eqn 6)

We used sun’s elevation at departure rather than time elapsed after sunset to describe departure at night because sun elevation is a physical trait that has important effects on orientation cues (Muheim, Moore & Phillips 2006) and because the time associated with a particular elevation changes over the season.

Statistics were calculated using the statistical software package R (R Development Core Team 2010). Uniformity of directions was tested with the Rayleigh test of uniformity (Batschelet 1981; Jammalamadaka & SenGupta 2001). Circular–linear correlations were calculated following the methods described by Jammalamadaka & SenGupta (2001). The P-value for a circular–linear correlation was approximated by a randomization test. For each circular and linear variable, random samples with replacement were drawn, and the circular–linear correlation coefficient of these values was estimated. We used 10 000 random replications in each case. The number of such replicates that have correlation coefficient larger than that associated with the original data set, divided by the total number of replications, provides a robust estimate of the corresponding P-value (Crawley 2005). Values of sun’s elevation were log-transformed in all linear regression models so that residual analyses did not show any serious deviation from normal distribution. All appropriate statistical analyses remained significant when the time after sunset instead of the sun’s elevation was used as a predictor.

Results

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

Departure Direction

Leucorhoa wheatears did not depart from Helgoland in a uniform direction (Rayleigh test of uniformity: = 30, = 0·09, = 0·77; Fig. 2). Julian day did not have a significant influence on departure direction (circular–linear correlation: = 30, F2,30–3 = 0·79, Rc–l = 0·03, = 0·67). Minimum stopover duration was on average 1·6 days [SD 2·1 days, range: (1, 7), = 31]. Variation in minimum stopover duration did not influence birds’ departure direction (circular–linear correlation: = 30, F2,30–3 = 5·50, Rc–l = 0·17, = 0·08).

image

Figure 2.  Departure directions of Greenland/Iceland northern wheatears (Oenanthe oenanthe leucorhoa) from Helgoland (Rayleigh test of uniformity: = 30, = 0·09, = 0·77). The shaded area indicates the ‘fast and risky’ direct way across the North Sea.

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Departure direction correlated significantly with departure fuel load (circular–linear correlation: = 30, F2,30–3 = 10·00, Rc–l = 0·27, = 0·013, Fig. 3). This result remained significant even if the assumed fuel deposition rate was allowed to vary from 0·01 to 0·15 day−1 for the 17 birds whose departure fuel load had to be modelled (see Fig. S1 in Appendix S1). All subsequent analyses assumed a fuel deposition rate of 0·09 day−1. Departure directions of leucorhoa wheatears correlated significantly with best wind profit at departure (circular–linear correlation: = 30, F2,30–3 = 6·28, Rc–l = 0·19, = 0·047) but not with wind direction at any of the altitudinal levels (circular–circular correlation: > 0·27). To estimate the combined effect on departure direction of the potential flight range (departure fuel load) and of the wind profit experienced, we calculated two flight ranges, each of which incorporated both variables. The first flight range was restricted temporally to the time birds had available from departure until sunrise (nocturnal flight rangei, eqn 5). The second flight range was based on depletion of fuel load to simulate a maximum flight range (eqn 6). We considered the best available wind profit at departure for both flight ranges (see methods for further explanations; circular–linear correlation: one nocturnal flight bout: = 30, F2,30–3 = 6·61, Rc–l = 0·20, = 0·036; maximum flight range: = 30, F2,30–3 = 7·88, Rc–l = 0·23, = 0·030; Fig. 4).

image

Figure 3.  Departure directions in relation to departure fuel load of Greenland/Iceland northern wheatears (Oenanthe oenanthe leucorhoa) from Helgoland (circular–linear correlation: = 30, F2,30–3 = 9·69, Rc–l = 0·26, = 0·0186). The shaded area indicates the ‘fast and risky’ direct way across the North Sea.

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image

Figure 4.  Departure directions over the maximum flight range of Greenland/Iceland northern wheatears (Oenanthe oenanthe leucorhoa), as estimated by fuel load and wind profit (circular–linear correlation: = 30, F2,30–3 = 7·88, Rc–l = 0·23, = 0·030, see Materials and Methods). The shaded area indicates the ‘fast and risky’ direct way across the North Sea. Dashed line indicates the farthest distance across the North Sea towards Great Britain (800 km) and dotted line the distance towards the nearest breeding areas on Greenland (2500 km).

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Birds that depart from Helgoland in different directions must cross different sized sea barriers (Fig. 1). For each 15° interval around Helgoland, we measured sea barrier ranges, defined as the distance from the island to the nearest land within the given interval. These barrier ranges correlated significantly with direction (circular–linear correlation: = 24, F2,24–3 = 39·42, Rc–l = 0·65, < 0·0001). We assigned the appropriate barrier range per 15° interval to each bird according to its departure direction. Departure fuel load and maximum flight range correlated both positively and significantly with the barrier range that had to be crossed (Spearman rank correlation: = 30, = 2720, RS = 0·20, = 0·0308; maximum flight range: = 30, = 2687, RS = 0·40, = 0·0275). Hence, the higher the departure fuel loads and maximum flight ranges of individuals were, the wider were the barriers they headed for.

Timing of Departure

All leucorhoa wheatears departed well after the end of civil twilight, when the sun was at least 6° under the horizon; mean sun’s elevation at departure was −14·2° (SD 5·6°, median = −12°, range: [−6·2°,−24·7°], = 31).

Departure fuel load explained 18% of the variation in the timing of departure. Leucorhoa wheatears with high fuel loads initiated their departure earlier (at higher sun elevation) than did leaner birds (linear regression: = 31, F1,29 = 6·422, R2 = 0·18, = 0·0169, Fig. 5). This result remained significant, even if the assumed fuel deposition rate varied from 0·01 to 0·15 day−1 for the 17 birds for which departure fuel load was modelled (see Fig. S2 in Appendix S1). We divided the leucorhoa wheatears into two groups relative to the median overall departure fuel load (0·39). Birds with high fuel load departed at significantly higher sun elevations (on average −11·8°, SD 5·2°) than birds with low fuel load (on average −16·1°, SD 5·1°; Wilcoxon rank sum test, one-sided: nhigh fuel load = 15, nlow fuel load = 16, = 183, = 0·007). We found no significant correlation between the sun’s elevation at departure and best wind profit and maximum flight range (Spearman rank correlations: all > 0·06).

image

Figure 5.  Timing of departure (sun elevation) of northern wheatear’s (Oenanthe oenanthe leucorhoa) in relation to their departure fuel load (linear regression: = 31, F1,29 = 6·422, R2 = 0·18, = 0·0169).

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The sun’s elevation at departure correlated significantly with departure direction (linear–circular correlation: = 30, F2,30–3 = 7·36, Rc–l = 0·21, = 0·040). To test whether the departure direction could in part explain the values recorded for the sun’s elevation at departure, we included departure direction in a linear model by using the corresponding sine and cosine values instead of the angular values. The sine of the departure direction did not influence sun’s elevation at departure (multiple linear model: sine of departure direction: = 0·27, cosine of departure direction: = 0·043; = 30, F1,28 = 3·68, R2 = 0·21, = 0·039). However, the cosine of departure direction alone was responsible for 18% of the variation in sun elevations at departure (linear model: = 30, F1,28 = 6·0, R2 = 0·18, = 0·021). This result indicates that a stronger northward component in departure directions was associated with higher sun elevations at departure. Thus, birds heading to the breeding grounds departed at higher sun elevations (c. earlier in the night) than did birds setting off to east or south.

Discussion

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

Our results suggest that leucorhoa wheatears take body condition together with weather conditions into account to adjust their migration trajectory for the sea barrier ahead. Birds having high fuel loads and experiencing favourable wind conditions were likely to depart for a long nonstop flight across the sea (Fig. 1). This choice represents a risky but direct and, hence, fast migratory route towards the breeding area. Similarly, birds departing in the seasonally appropriate direction started relatively soon after sunset and were able to use the whole night for flying. In contrast, birds having decided to set off under unfavourable conditions – low fuel load and bad weather – chose a safe route towards the nearby mainland within a 50–100 km range and left Helgoland throughout the night. The correlation of the minimum sea barrier to be crossed and birds’ physical condition suggests that, in addition to fuel load and wind, also visual cues were used in the decision on departure directions.

Departure Direction

Our results agree with the outcome of orientation cage experiments and with a study that used light-sticks to track departure directions (detection range about 1 km; Sandberg 1994; Sandberg & Moore 1996; Sandberg 2003; Deutschlander & Muheim 2009). Here, we show now for free-flying birds over an unprecedented range that leucorhoa wheatears departed towards the open sea only if they had large fuel loads (Figs 1 and 3). Additionally, the wind profit correlated significantly with departure direction; though, trajectory analyses have to show whether birds encountered favourable winds along the entire route (Shamoun-Baranes et al. 2010; Shamoun-Baranes & van Gasteren in press). Wind support is crucial, if migrants are to cross barriers successfully (Liechti 2006; Schmaljohann, Liechti & Bruderer 2009) or to perform long nonstop flights (Shamoun-Baranes et al. 2010), but wind support alone is not sufficient because a minimum fuel load is required for flying. The combination of both departure fuel load and wind profit resulted in the strongest correlation with departure direction. Therefore, departing leucorhoa wheatears respond to these factors jointly. If the overall potential flight range is reduced, birds avoid the north-west direction towards the sea barrier.

Migrants setting off from Helgoland face ecological barriers whose size varies with the birds’ departure direction (Fig. 1). Many leucorhoa wheatears had high fuel loads allowing flight ranges much larger than the minimum barrier distance, see e.g. Bairlein (1988) and Dierschke, Mendel & Schmaljohann (2005). We suggest leucorhoa wheatears behaved with a considerable physiological safety margin when making departure decisions (Moore & Kerlinger 1992). Klaassen (1996) hypothesized that an individual bird’s physiological safety margin may be related to its navigational skills. The most parsimonious interpretation is that leucorhoa wheatears do not know the exact dimension of the ecological barrier towards north-west, but that they can estimate alternative directions, in which the sea barrier is limited and where stopover sites are nearby. Ascending during their departure or on ‘exploratory flights’ (Schmaljohann et al. 2011), birds can test the wind conditions aloft and easily make out land on the horizon from north-east to south-west, which can be reached in 1–3 h (distance <100 km). Between south-west and north, no land can be seen, indicating that a long nonstop flight would therefore be required (Fig. 1). Leucorhoa wheatears setting off from Helgoland with an insufficient physiological safety margin for a flight to the north-west have reliable information, in which directions land can be reached by a short flight.

Adaptive behavioural adjustments of migratory direction are critical for crossing ecological barriers (Alerstam 2001; Henningsson & Alerstam 2005). The observed variation of departure direction in relation to fuel load and wind conditions reveals the ability for such behavioural responses. Our radiotracking measurements of the departure direction of free-flying leucorhoa wheatears for the first 12–15 km of their outbound flight indicated that the relevant phenotypic trait was a behavioural response to internal information (body condition) and external information (wind support). This finding also suggests that birds incorporate a physiological safety margin when selecting a route for the next migration stage. In general, birds crossing ecological barriers under unfavourable circumstances, including environmental conditions and the internal state, will have a lower survival rate than birds prepared for such a crossing (‘differential survival’). Such a selection process will likely fine-tuned the spatiotemporal migration pattern in relation to environmental cues and individual fuel load and hence minimize the fitness costs of such crossings.

Timing of Departure

Leucorhoa wheatears did not depart within a fixed time window, as songbirds in other studies (reviewed in Bolshakov et al. 2007; Schmaljohann et al. 2011). Wind, clouds, season, stopover duration and fuel load may influence the nocturnal departure decision, but these factors lack consistent effects across different studies (cf. Åkesson et al. 2001; Bolshakov et al. 2007; Schmaljohann et al. 2011). Possibly atmospheric conditions in relation to air turbulences might play a rule for the departure decision within the night (Kerlinger & Moore 1989). Migrants heading towards their migratory goal with a long potential flight vector are supposed to use the entire night for flying. Lean birds – having decided to leave the island based on general conditions (Dierschke & Delingat 2001; Erni et al. 2002; Goymann et al. 2010) – could depart either early or late at night to aim for nearby stopover sites with likely more favourable conditions. Possibly, lean birds decide several times during the night whether departure conditions are sufficient to leave the stopover site, whereas birds with long potential flight vectors may have a shorter time window during the first half of the night for their departure decision. Although nocturnal departure occurs within a genetically predetermined time window (Cochran 1987; Coppack, Becker & Becker 2008), environmental factors, birds’ body condition and the choice between continuing migration towards the seasonally appropriate direction and seeking a nearby stopover site will modulate the exact timing (Åkesson et al. 2001; Bulyuk & Tsvey 2006).

Acknowledgements

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

We are very grateful to Franz Bairlein who supported this project in various ways. The field work could not have been carried out without the effort of the radiotracking team: Philipp J.J. Becker, Margarita Berg, Celia Grande, Benedikt Holtmann, Hakan Karaardic and Sven Stadtmann braved many cold, wet and uncomfortable hours during the nights. Furthermore, we thank Ommo Hüppop, Freimut Schramm and several volunteers of the Institute of Avian Research ‘Vogelwarte Helgoland’ for their important support during the field studies. Meteorological data were kindly supplied by Deutscher Wetterdienst and the NOAA-CIRES Climate Diagnostics Center, Boulder, Colorado, from their Web site at http://www.cdc.noaa.gov/. The authors are very grateful to Ulric Lund for his advice on circular statistics. Franz Bairlein, Lukas Jenni, Judy Shamoun-Baranes and one anonymous referee kindly provided very helpful comments on the manuscript.

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  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
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Supporting Information

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

Appendix S1. Sensitivity analysis of modelled fuel deposition rate.

Fig. S1. Influence of modelled departure fuel load on departure direction.

Fig. S2. Influence of modelled departure fuel load on sun elevations at departure.

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