J Ornithol DOI 10.1007/s10336-013-0987-7

ORIGINAL ARTICLE

Food availability and fuel loss predict Zugunruhe Cas Eikenaar • Franz Bairlein

Received: 5 May 2013 / Revised: 11 June 2013 / Accepted: 16 June 2013 Ó Dt. Ornithologen-Gesellschaft e.V. 2013

Abstract Migrating birds spend most of their time at stopover sites where they replenish the fuel used during flight, termed refueling. The overall time of migration thus largely depends on the duration of stopovers, and factors shaping stopover duration therefore are of interest. A handful of field studies have shown that the likelihood of departure from stopover sites increases with poor feeding conditions. However, food availability and stopover duration are generally difficult to quantify accurately in the field. Results of fasting-refueling experiments on captive birds using migratory restlessness (Zugunruhe) as a proxy for departure likelihood are mixed. Although Zugunruhe usually decreased with refueling, fasting often failed to increase Zugunruhe. In addition, some experiments lacked randomization. In a fasting-refueling experiment on Northern Wheatears (Oenanthe oenanthe), using birds as their own control in a randomized fashion, we found that fasting increased Zugunruhe, whereas refueling decreased Zugunruhe. These results show that the motivation to migrate, quantified by Zugunruhe, is affected by changes in food availability. Furthermore, Zugunruhe during refueling did not depend on fuel reserves left after fasting, but tended to decrease with the amount of fuel lost during fasting. We discuss why extent of fuel loss may be a better predictor of stopover duration than fuel reserves.

Communicated by L. Fusani. C. Eikenaar (&)
F. Bairlein Institute of Avian Research, An der Vogelwarte 21, 26386 Wilhelmshaven, Germany e-mail: [email protected] F. Bairlein e-mail: [email protected]

Keywords Northern Wheatear
Oenanthe oenanthe
Migratory restlessness
Fasting
Fueling
Stopover
Zugunruhe Zusammenfassung Nahrungsverfu¨gbarkeit und Ko¨rpermassenverlust bedingen Zugunruhe Zugvo¨gel verbringen in Rastgebieten wa¨hrend des Zuges die meiste Zeit damit, im Flug vorher verbrauchte Energiereserven wieder aufzufu¨llen (,,aufzutanken‘‘). Deshalb ha¨ngt die Zuggeschwindigkeit insbesondere von der Dauer der Rastaufenhalte ab, weshalb Faktoren, die diese bestimmen, von großem Interesse sind. Eine Handvoll von Arbeiten hat gezeigt, dass die Wahrscheinlichkeit, ein Rastgebiet wieder zu verlassen, ansteigt, wenn die Nahrungsbedingungen schlecht sind. Allerdings ist die Erfassung von Nahrungsverfu¨gbarkeit und Rastdauer im Freiland ganz allgemein schwierig zu quantifizieren. Sog. ,,Fasten-Auftanken‘‘-Experimente (,,fasting-refuelling‘‘) an geka¨figten Vo¨geln, die Zugunruhe als Merkmal fu¨r Abflugwahrscheinlichkeit nutzen, ergaben unterschiedliche Ergebnisse. Auch wenn die Zugunruhe u¨blicherweise abnahm, sobald die Vo¨gel nach Fasten wieder Futter bekamen, erho¨hte das Fasten selbst die Zugunruhe meist nicht. Zudem mangelt es manchen dieser Studien an fehlender Randomisierung. In einem ,,fasting-refuelling‘‘Experiment mit Steinschma¨tzern (Oenanthe oenanthe), in dem wir den einzelnen Vogel randomisiert als seine eigene Kontrolle nutzten, fanden wir, dass wa¨hrend des Fasten die Zugunruhe zunahm, wa¨hrend sie bei erneuter Massenzunahme (,,refuelling‘‘) abnahm. Dies zeigt, dass die Motivation zu ziehen, ausgedru¨ckt u¨ber die gemessene Zugunruhe, von der Nahrungsverfu¨gbarkeit bestimmt ist.

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Weiterhin war die Zugunruhe wa¨hrend des ,,refuelling‘‘nicht von der nach dem Fasten noch restlichen Energiemenge abha¨ngig. Vielmehr nahm sie mit dem Ausmaß des Energieverlustes wa¨hrend des Fastens ab. In der Diskussion ero¨rtern wir, warum der Verlust an ,,Treibstoff‘‘eine bessere Vorhersage der Rastdauer erlaubt als der Energievorrat selbst.

Introduction Optimal migration theory commonly assumes that birds minimize the overall time of migration (Alerstam and Lindstro¨m 1990; Hedenstro¨m and Alerstam 1997; Hedenstro¨m 2008; Alerstam 2011). During migration, birds spend most of their time at stopover sites (e.g., Hedenstro¨m and Alerstam 1997; Green et al. 2002) where they replenish the fuel (fat) used during flight. Therefore, the rate at which fuel reserves are replenished may be the most important determinant of the overall time of migration. Although an increased assimilation efficiency of food or seasonal shifts in diet may also contribute to fueling (Bairlein 2002), hyperphagia (over-eating) is the main driver of fuel deposition (Lindstro¨m 2003). Food availability at a stopover site is thus expected to directly affect a bird’s decision to stay or to depart. In accordance with this idea, field studies on species foraging on quantifiable food items, such as berries or aphids, have shown that birds are more likely to move on when food is scarce than when food is plentiful (Bibby and Green 1981; Ottich and Dierschke 2003). Likewise, the likelihood of departure can be decreased by supplemental feeding at stopover sites (Dierschke et al. 2005). The results of food manipulation experiments on captive birds are in line with the field studies, however, not invariably so. In such experiments, captive birds are typically fasted for some days and subsequently re-fed. Nocturnal migratory restlessness (Zugunruhe) is then used as a proxy for the motivation of a bird to depart (from a stopover site). Although in comparison to field data, experiments on captive birds may seem artificial, early studies have been able to show that Zugunruhe was higher when birds were fasted, and lower when birds were refueling, as compared to periods of ad libitum access to food (Biebach 1985; Gwinner et al. 1985, 1988). These results are consistent with the idea that food availability affects a bird’s motivation to depart from a stopover site, because when feeding conditions are poor a bird should leave, whereas abundant food should make a bird stay (Gwinner et al. 1985, 1988). A potential issue, however, with the early studies of Biebach (1985) and Gwinner et al. (1985, 1988) is that the control and experimental periods were not randomized; Zugunruhe during fasting was compared to that in the

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preceding nights, and Zugunruhe during refueling was compared to that in the following nights. Also, other studies did not match these results. While Zugunruhe did decrease during refueling in one study (Fusani and Gwinner 2004), fasting failed to increase Zugunruhe in other studies (Berthold 1976; Fusani and Gwinner 2004; Bauchinger et al. 2008; Ramenofsky et al. 2008). Next to the availability of food, current fuel reserves may be an important determinant of the decision to stay or depart from a stopover site. Indeed, in wild birds captured after having crossed an ecological barrier, Zugunruhe was higher in fat birds than in lean birds (Yong and Moore 1993; Fusani et al. 2009). However, the results of studies measuring stopover duration are mixed; some found that fat birds were more likely to depart than lean conspecifics (e.g., Bairlein 1985; Biebach et al. 1986; Goymann et al. 2010), whereas in other studies, stopover duration was unrelated with fuel reserves at capture (e.g., Kuenzi et al. 1991; Salewski and Schaub 2007; Tsvey et al. 2007; Schaub et al. 2008). Because a main purpose of stopovers is to replenish fuel used during flight, the motivation to refuel during stopover may not only depend on fuel reserves left, but likely is also driven by the amount of fuel lost during the preceding flight. Perhaps, therefore, the extent of fuel loss prior to stopover may be a good predictor of stopover duration. In a fasting-re-feeding experiment on Northern Wheatears (Oenanthe oenanthe), we investigated the relationship between food availability and Zugunruhe, using birds as their own control in a randomized fashion. Furthermore, we determined whether fuel reserves after fasting and the extent of fuel loss predicted Zugunruhe during refueling. Northern Wheatears are nocturnal long-distance migrants and have previously been shown to adjust departure decisions to food availability at stopover; an artificial increase in food availability increased the likelihood of individuals prolonging their stopover (Dierschke et al. 2005).

Methods From August 2012 onwards, 15 adult Northern Wheatears, born in captivity, were housed in individual cages of 40 9 40 9 50 cm in a single room with ad libitum access to food and water. To promote migratory fueling, on 3 September the photo-period in the room was changed from long days (14L:10D) to short days (12L:12D). After the birds had reached a stable high body mass, each bird was subjected to two 6-day trials during which Zugunruhe was measured (Fig. 1). Birds were thus used as their own control. In the ‘experimental trial’, during three consecutive days, the daily amount of food birds received was

J Ornithol Fig. 1 Schematic illustration of the experimental and control trials. Days 1–3 represent the fasting period and its respective control, and days 4–6 represent the refueling period and its respective control

reduced from ad libitum access to food to 2 g (hereafter termed ‘fasting’). Two grams of food is approximately 20 % of the amount eaten on a regular day once birds have reached a stable body mass in autumn (CE, personal observation). Each bird always fully consumed these 2 g of food. Immediately following the days of reduced food, birds were given ad libitum access to food for three days (hereafter termed ‘refueling’). In the ‘control trial’ the birds had continuous ad libitum access to food. The order of the trials was randomized, and experimental and control trials were separated by three weeks to allow birds to recover from fasting. This was effective in that all birds subjected to the experimental trial first, recovered their prefast body mass and fuel reserves at least 1 week before the start of the control trial. The composition of the food in the experiment was the same as in the pre-experimental period. The temperature in the room was held constant at 20 °C, and water was provided ad libitum throughout the experiment. To calculate fuel (fat) reserves after fasting and fuel loss, birds were weighed the day immediately before and the day immediately after fasting, directly after lights on in the morning. Additionally, the amount of subcutaneous fat was scored on a scale of 0–8 (Kaiser 1993). Fuel reserves were calculated as: (body mass on day 4 - lean body mass)/lean body mass. Lean body mass was calculated after Schmaljohann and Naef-Daenzer (2011). Fuel loss was calculated as (body mass before fasting - body mass after fasting)/lean body mass. Zugunruhe was recorded automatically with motion-sensitive microphones, one of which was attached to the right wall of each cage. Each time a 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 three impulses per second before it was recorded as an activity count. Another device (developed by SF Becker, Bremen, Germany) created a CSV file summarizing the activity counts over 15-min intervals. Zugunruhe was then expressed as the number of 15 min intervals in a night during which a bird showed at least five activity counts (Maggini and Bairlein 2010, 2012). In captive birds, Zugunruhe can change dramatically from one night to the next (Berthold 1978; CE and FB, personal observation). Therefore, to determine the

effects of fasting and refueling on Zugunruhe, we totalled the Zugunruhe recorded during the three nights for the fasting, refueling and respective control periods. All variables and residuals were normally distributed (Kolmogorov–Smirnov test, all P [ 0.5).

Results Figure 2 shows Zugunruhe during the nights in the experimental and control trials. Fasting resulted in increased Zugunruhe; during the three nights in the fasting period total Zugunruhe was higher than during the first three nights of the control trial (paired T test: T = 4.23, P = 0.001, N = 15, Fig. 3). When, after fasting, birds again had ad libitum access to food, Zugunruhe dropped precipitously (Fig. 2). Refueling with ad libitum access to food resulted in decreased Zugunruhe; during the three nights in the refueling period total Zugunruhe was lower than during the last three nights of the control trial (paired T test: T = -2.82, P = 0.01, N = 15, Fig. 4). Fasting resulted in a mean and SD fuel loss of 0.17 ± 0.03 (N = 15), meaning that on average birds lost

Fig. 2 Mean and SEM Zugunruhe during the nights in the experimental (closed circles) and control (open circles) trials. In the experimental trial, nights 1–3 were those that followed days of fasting, and nights 4–6 were those that followed days of refueling (N = 15)

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Fig. 3 Total Zugunruhe during the fasting and respective control periods in 15 Northern Wheatears

Fig. 5 The relationship between fuel loss and total Zugunruhe during the refueling period. Fuel loss is expressed as the proportion of a bird’s lean body mass lost during fasting (N = 15)

refueling tended to decrease with increasing fuel loss (Pearson’s r = -0.46, P = 0.116, N = 13).

Discussion

Fig. 4 Total Zugunruhe during the refueling and respective control periods in 15 Northern Wheatears

an amount of fuel equivalent to 17 % of their lean body mass. Fat scores were significantly lower after fasting than before fasting (paired T test: T = 8.29, P \ 0.001, N = 15), showing that fuel loss reflected subcutaneous fat loss. There was a negative trend between the extent of fuel loss and total Zugunruhe during refueling (Pearson’s r = -0.44, P = 0.105, N = 15, Fig. 5). Fuel reserves after fasting (on day 4) was not correlated with total Zugunruhe during refueling (Pearson’s r = -0.06, P = 0.84, N = 15), nor with the extent of fuel loss (Pearson’s r = -0.02, P = 0.93, N = 15). Two birds showed little Zugunruhe throughout the experiment as compared to the other 13 birds (in Figs. 3 and 4, these are the lowest two points in the control period). Excluding these two birds from the analyses did not change the results in any significant way; fasting increased Zugunruhe (paired T test: T = 4.17, P = 0.001, N = 13), while refueling decreased Zugunruhe (paired T test: T = -3.31, P = 0.006, N = 13). Zugunruhe during

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Using an improved control, to our best knowledge, our study is the first to confirm the observation made by Biebach (1985) and Gwinner et al. (1985, 1988) that fasting increases Zugunruhe. This result is in line with observational field studies showing that migrants are more likely to depart from a stopover site when food is scarce than when food is plentiful (Bibby and Green 1981; Ottich and Dierschke 2003). More interestingly, it also matches the finding of Dierschke et al. (2005) that in wild Northern Wheatears stopover duration can be extended by supplemental feeding. We also found that refueling decreased Zugunruhe, again confirming earlier findings (Biebach 1985; Gwinner et al. 1985; Fusani and Gwinner 2004). This makes sense in that, when replenishing fuel reserves, the motivation to depart from a stopover site has to be inhibited until sufficient fuel has been accumulated for the next flight (Biebach 1985; Yong and Moore 1993). This inhibition likely is stronger when more fuel has to be replenished; an idea that finds support in the observation that after crossing an ecological barrier, Zugunruhe is lower in lean than fat birds (Yong and Moore 1993; Fusani et al. 2009). Our experiment provides additional support with the observation that birds that lost much fuel (corrected for body mass) during fasting tended to have lower Zugunruhe during subsequent refueling than birds that lost little fuel. In contrast to fuel loss, fuel reserves after fasting did not predict Zugunruhe. Perhaps, therefore, the extent of fuel loss prior to stopover is a better predictor of stopover

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duration than current fuel reserves. This is not unlikely because the amount of fuel used to travel the same stretch of the migratory route will differ among individuals of the same species for several reasons. First, physical and physiological traits important for migration, such as flight apparatus and fat metabolism, vary among individuals. Indeed, our observation that, despite being subjected to the same fasting regime, individuals differed considerably in how much fuel they lost (Fig. 5) indicates variation in fat metabolism. Second, environmental factors influencing flight performance, such as wind direction and wind speed change throughout the migration season. Think of the following scenario. Two birds travel between the same two stopover sites, but bird A migrates a few weeks earlier than bird B. Although bird A has more fuel reserves at departure than bird B, they are caught at the second stopover site with the same fuel reserves, because bird A faced a mild head wind while bird B experienced a tail wind. Bird A, thus, used more fuel than bird B to travel the same stretch. Consequently, despite arriving with the same fuel reserves, they differ in their motivation to refuel, which probably results in different stopover durations. Unfortunately, when catching birds at stopover sites, there is no way of determining the amount of fuel a bird has used during the preceding flight. Nonetheless, it may help to explain why in many species, stopover duration was found to be independent of fuel reserves at arrival (e.g., DeWolfe et al. 1973; Safriel and Lavee 1988; Kuenzi et al. 1991; Ellegren 1991; Lyons and Haig 1995; Morris et al. 1996; Salewski and Schaub 2007; Tsvey et al. 2007; Schaub et al. 2008). In summary, our study shows that changes in both food availability as well as fuel reserves affect the motivation to migrate, quantified in captive birds by Zugunruhe. How Zugunruhe translates into departure decisions in wild birds at stopover remains to be determined. Acknowledgments We thank Ulrich Meyer and Adolf Vo¨lk for their assistance in the experiment, Marc Bulte for help with the Zugunruhe equipment, and two anonymous reviewers for their constructive comments.

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