J. Ornithol. 144, 33-44 (2003) Deutsche Ornithologen-Gesellschaft/Blackwell Verlag, Berlin ISSN 0021-8375

Time allocation in migrating Northern Wheatears (Oenanthe oenanthe) during stopover: is refuelling limited by food availability or metabolically?

Volker Dierschke*, Julia Delingat and Heiko Schmaljohann

Institut fiar Vogelforschung ,,Vogelwarte Helgoland", Inselstation Helgoland, Postfach 1220, D-27494 Helgoland, Germany (*corresponding author: Email: volker-ifv@t-online.de)

Summary

According to full-day observations (scan sampling), Northern Wheatears (Oenanthe oenanthe) stopping over on the island of Helgoland (SE North Sea) during spring and au- tumn migration spent 51-67 % of the daylight period foraging. Large parts of the day were used for resting or being vigilant, whereas flying, preening and aggressive behaviour were of minor importance. The density of Wheatears did not influence the time devoted to for- aging and aggressive behaviour, and the time spent resting/vigilant was not correlated to predation risk (measured as the rate of raptor flying over). Several observations showed that refuelling on the beach, which presented the most favourable feeding conditions and allowed high rates of body mass gain, was metabolically limited. The total time devoted to foraging was independent of day length, and additional food (mealworms) offered in bowls was completely ignored, an indication that reduced foraging effort would not improve net energy gain within the physiological capacity. In contrast, Wheatears responded strongly to additional food supplied in the poorer grassland habitat. Although this strongly suggests that refuelling is limited by the amount of food available and the costs of obtaining it, for- aging times were the same as on the beach. In grassland, the behaviour pattern of birds refuelling was probably distorted by a high proportion of transient and exploring individu- als. Therefore, knowledge about foraging ecology and the response to additional food im- proves the value of the foraging time parameter in considerations of refuelling limitations.

Keywords: stopover ecology, time allocation, refuelling, Northern Wheatear, Oenanthe oenan- the.

Zusammenfassung

Zeitbudgets ziehender Steinschm~itzer (Oenanthe oenanthe) wiihrend der Rast: Ist die N~ihrstoffdeposition durch Nahrungsverfiigbarkeit oder Stoffwechsel limitiert?

Ganztagsbeobachtungen an auf Helgoland wfihrend des Heim- und Wegzugs rastenden Steinschm~itzern ergaben, dass 51-67 % der Tageslichtperiode ftir die Nahrungssuche ge- nutzt werden. Groge Zeitanteile entfielen auf Ruhen und Wachsamkeit, wahrend Fliegen, Putzen und Revierverteidigung von geringerer zeitlicher Bedeutung waren. Die ftir Nah- rungssuche und Revierverteidigung anfgewendeten Zeitanteile waren unabh~ingig von der Individuendichte rastender Steinschm~itzer, und der Zeitanteil ftir Ruhen/Wachsamkeit war nicht mit dem Pr~idationsrisiko, das als Rate von Greifvogel-Oberfltigen gemessen wurde, korreliert. Verschiedene Beobachtungen zeigten, dass die Nahrstoffdeposition am Strand, wo sehr gtinstige Ern~ihrungsbedingungen herrschten, durch den Stoffwechsel be-

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34 Journal ftir Ornithologie 144, 2003

grenzt wurde. Einerseits war die Dauer der Nahrungssuche unabhtingig von der Tagesl~in- ge, andererseits wurde in Schalen angebotenes Zusatzfutter (Mehlwtirmer) vollsttindig ignoriert. Innerhalb der physiologischen Grenzen hfitte ein verringerter Aufwand bei der Nahrungssuche offenbar die Nettoenergieaufnahme nicht weiter steigern k6nnen. Im Ge- gensatz dazu nutzten Steinschm~itzer das zus~itzliche Futter im nahrungs~irmeren Grtinland sehr intensiv. Obwohl dieses Verhalten stark auf eine Limitierung der N~ihrstoffdeposition durch das verftigbare Nahrungsangebot und die Kosten, dieses zu nutzen, hinweist, unter- schied sich die Dauer der Nahrungssuche nicht von jener am Strand. Wahrscheinlich wur- de im Grtinland das Verhalten von tats~ichlich dolt rastenden Individuen von solchen V6geln tiberlagelt, die dort nur durchwandelten bzw. auf der Suche nach geeigneten Rasthabitaten explorierten. Ffir die Frage, ob die N~hrstoffdeposition durch Nahrungsver- ffigbarkeit oder physiologisch limitiert ist, sind deshalb Kenntnisse fiber die Ern~ihmngs- 6kologie und die Reaktion auf Zusatzfutter als wichtige Ergtinzung zu Zeitbudgets anzusehen.

Introduction

During stopovers, migrating birds usually de- vote their time to foraging, because fuel has to be stored in order to allow onward migration. At least in spring, but probably also in autumn, when early arrival in the breeding or wintering area favours establishment of high quality territories (M¢ller 1994, Currie etal. 2000, Morris & Glasgow 2001), high refuelling rates are required to allow a high maximum speed of migration (Alerstam & Lindstr6m 1990). Very high refuelling rates as observed in labo- ratory studies (Klaassen et al. 1997) are some- times found (Lindstr6m 2002), but are often not possible in the field because energy intake can be limited by food supply and foraging conditions (habitat suitability, competition, in- terference, predation risk, weather: Bibby & Green 1981, Bairlein 1988, Simons & Bairlein 1990, Moore & Yong 1991, Morris etal. 1996, Schaub & Jenni 2000, 2001). Influenced by this set of environmental and behavioural vari- ables, the time available for foraging can limit the daily food intake and thus the fuel deposi- tion rate (FDR, Lindstr6m 2002). For experi- mental birds the daily FDR, i. e. the amount of fuel stored within 24 hours, was shown to de- pend largely on the length of the period during which food is available (Kvist & Lindstr6m 2000). In addition to foraging time, migrants

can be limited by the combined effects of the amount of food available and the costs in- volved in getting it, but may try to increase the instantaneous rate of food intake in order to improve FDR (Lindstr6m 1991, A. Lindstr6m pers. comm.). On the other hand, digestive bot- tlenecks and absorption capacities can restrict the FDR of migrating birds to a certain ceiling (Kirkwood 1983, Zwarts & Dirksen 1990, Klaassen etal. 1997). Although time-limita- tion also applies to those birds, they are unable to increase instantaneous intake rates for phys- iological reasons and are therefore metabol- ically limited in their FDR. Whether the FDR of migrants is limited by food availability or metabolically is discussed by Lindstr6m (1991, 2002) with respect to time budgets, but so far very few field studies present estimates of time allocation in migrants. Time budgets during migration are best studied in shorebirds and geese, but these birds often stay long in wetlands to which they return annually (e. g. Pienkowski 1976, Prokosch 1984, Rehfisch et al. 1996) and with which they are familiar in respect of foraging conditions. Passerine mi- grants are usually less faithful to stopover sites (Moreau 1961, Merom etal. 2000, Dierschke 2002) and seem to imterrupt migratory flights at random parts of the country, where they probably explore for suitable habitats (Hutto 1985, Bruderer & Jenni 1988, Aborn & Moore

v. Dierschke et al. • Migrating Northern Wheatears 35

1997, Jenni-Eiermann & Jenni 1999) and often stay for only one or a few days (e. g. Rappole & Warner 1976, Bairlein 1985, Berthold et al. 1991, Akesson etal. 1995). Passerines thus present a better opportunity to study short-term effects of a given environment on time alloca- tion. In order to identify thctors which influ- ence time budgets and thus possibly limit the refuelling of passerine migrants we studied the time allocation of Northern Wheatears (Oenanthe oenanthe; hereafter Wheatears) stopping over on Helgoland, a small island out in the North Sea.

In contrast to many other abundant passerine migrants, Wheatears live in open habitats and are thus an ideal study species for observing stopover behaviour in the field. On Helgoland they occur in two types of habitat which differ in food supply and cause different patterns of stopover (Delingat & Dierschke 2000). In one habitat, wrack beds on the beach, very high rates of body mass increase (on average 8.5 % and 6.0 % of lean mass per day in spring and autumn, respectively; Dierschke & Delingat 2001 and unpubl.) suggest that the birds ap- proach their theoretical metabolic ceiling, which would be of 6.4 % for a passerine weighing 20 g for a medium day length (Lind- str6m 1991) and somewhat higher during the longest days (17 hours) in this study. It seems that the refuelling of Wheatears stopping over in the rich beach habitat is limited metabol- ically. Therefore, we expected a relatively low proportion of daylight hours spent foraging on the beach, because foraging time cannot be ex- ceeded for physiological reasons. In the poorer grassland habitat, Wheatears might be ex- pected to spend longer periods foraging in or- der to compensate as much as possible for the probably lower food intake rate caused by an inferior food supply (Delingat & Dierschke 2000). As opposed to the situation on the beach, the refuelling of birds on grassland was expected to be limited by the food available.

In addition to the amount of time allocated to foraging, the reaction to additional food has been established as an indicator of food-avail-

ability versus metabolic limitation of refuel- ling (Lindstr6m 1991 and pers. comm.). Whereas metabolically limited birds should in theory neglect an increased food supply (be- cause they are unable to increase instantaneous intake rates for physiological reasons), food- availability limited migrants should exploit ad- ditional food in order to improve their refuel- ling rate (Lindstr6m 1991). Therefore, addi- tional food offered in a field experiment was expected to be ignored by the Wheatears on the beach, but included in the diet of Wheat- ears on grassland.

Apart from energetic considerations, which apply to the question of minimizing time or energy costs during migration, safety from predators is another possible factor determin- ing the stopover behaviour of migrating birds (Alerstam & Lindstr6m 1990, Lindstr6m 1990, Cimprich & Moore 1999). Therefore, if Wheatears respond to the presence of preda- tors, the amount of time spent scanning for predators and kept unexposed or motionless (freezing) would be related to the number of predator attacks at the expense of foraging time. In this study, decreased foraging time was expected with more raptor flights occur- ring as a possible threat for Wheatears.

Methods

The study was conducted on the small island of Helgoland (1.5 kma), which is situated c. 50 km off the German Wadden Sea coast in the North Sea (54 ° 11' N, 07 ° 55" E). Wheatears were studied in two different habitats: 30-50 m wide sandy beaches (partly covered with rotting brown algae) and grass- land habitats with interspersed open patches and boulders. These two types of habitat differ signifi- cantly in the food supply available for Wheatears. On the beach, kelp flies (Coelopidae) and their lar- vae present the only but very abundant food supply, while various ground-dwelling arthropods can be found in grassland habitats. For further details of these habitats see Delingat & Dierschke (2000).

Stopover behaviour of Wheatears was sampled by scanning birds present for their instantaneous ac- tion in 14 full-day periods (from 30 rain before sun-

36 Journal fiir Omithologie 144, 2003

Table 1. Days and sample sizes of full-day observations of Northern Wheatear behaviour on Helgoland. Note that very low numbers of birds per scan were mostly due to first birds becoming visible in early morn- ing. Also given are estimates of Wheatear density (average number of birds per scan) and predation risk (raptor flights per hour). Time is given as Central European Time. Tab. 1. Ganztagsbeobachtungen zum Rastverhalten des Steinschmfitzers auf Helgoland. Zu beachten ist, dass sehr geringe Anzahlen von V6geln je Zfihldurchgang vor allem auf die allerersten V6gel am friihen Morgen zurtickzuftihren sind. Angegeben sind auch Schfitzungen der Steinschmatzer-Dichte (durchschnit- tliche Anzahl von V6geln pro Z~ihldurchgang) und des Pr~idationsrisikos (Greifvogel-Lrberfltige pro Stunde). Zeitangaben in MEZ.

Date habitat

sunrise sunset day length n n mean (range raptors birds

-30 rain +30 min (min) scans birds birds/scan per scan) per hour

spring migration

03May 2000 grassland 0415 2030

05May 2000 grassland 0411 2034

04May 1999 beach 0413 2032

09May 2000 beach 0403 2041

l l M a y 1999 beach 0400 2045

23May 2000 beach 0341 2104

autumn migration

22Aug 2000 grassland 0446 2009

04 Sep2000 grassland 0509 1938

28Aug 1999 beach 0457 1955

01Sep 1999 beach 0504 1945

12 Sep 2000 beach 0523 1918

15 Sep 2000 beach 0529 1911

22 Sep 2000 beach 0541 1853

28 Sep 2000 beach 0552 1839

975 93 676 7.3 (1-27) 0.06

983 85 327 3.8 (1-15) 0.29

979 92 741 8.0 (1-18) 0.51

998 99 1239 12.5 (2-38) 0.57

1005 101 584 5.8 (2-13) 0.25

1043 100 247 2.5 (1-7) 0.06

923 90 833 9.3 (1-24) 0.27

869 84 887 10.6 (1-38) 0.41

898 87 490 5.6 (1-10) 0.00

881 84 2995 35.7 (5-68) 0.75

835 80 384 4.8 (1-14) 0.22

822 76 661 8.7 (2-20) 0.48

792 78 984 12.6 (5-24) 0.85

767 73 1172 16.1 (3-35) 0.75

rise until 30 min after sunset), six of which relate to spring migration and eight to autumn migration (Ta- ble 1). The scans were started every 10 rain from a standard observation point. The action of birds was assigned to five categories: foraging, rest/vigilance, aggression, preening and flying. Foraging included birds hopping on the ground in search of prey items or fly catching in the air. In the latter behaviour, birds often remained on a perch motionless and scanned the sky for flying insects. In such situations the observer waited for about 10 s after which a bird was considered as a resting/vigilant bird. Rest and vigilance was lumped together into one category be- cause the aim of sitting motionless was not clear in many situations. Vigilance often coincided with freezing behaviour as a reaction to flying raptors. A bird was classified as being aggressive when attack-

ing other birds (in most cases conspecifics) by short flights in the direction of the victim or even physical conflict. Flying was assigned to flights not aimed at attacking neighbours or catching prey, but usually to change location. Preening also included bathing.

The proportion of birds engaged in a given activ- ity was assumed to be equivalent to the proportion of time spent in that activity by an average individu- al (Altmann 1974). The percentage of birds falling into each of the five behavioural categories was cal- culated for each scan. An average percentage for each category was calculated for each hour of the day (e. g. 1300 to 1359) and multiplied by 60 min to obtain the time devoted to that action in the respec- tive hour. This procedure made it possible to sum up the minutes spent for each category over the whole

Vo Dierschke et al.. Migrating Northern Wheatears 37

daylight period from 30 min before sunrise until 30 min after sunset. Owing to seasonal variation in day length the diurnal activity pattern is shown for a standard day, which consists of twelve equal sec- tions of the time from 30 min before sunrise until 30 min after sunset. Average percentages of behav- ioural categories were calculated for these sections and not for hours in this case.

The results of scan sampling were examined with respect to two biological factors which possibly in- fluence the behaviour of Wheatears. First, the den- sity of Wheatears on Helgoland was measured as the average number of individuals contained in the scans for each day. Second, the number of raptor flights per hour through and over the study site was taken as an index for predation risk. Only raptors constituting a threat for small passerines were con- sidered (Sparrowhawk Accipiter nisus, European Kestrel Falco tinnunculus, European Hobby F. sub- buteo, Merlin E columbarius, Peregrine F. peregri- r l t l S ) .

In a field experiment with Wheatears, mealworms were supplied ad libitum in six bowls placed in a grassland habitat from 19 August to 3 October 2001. At this study site 218 Wheatears were captured with spring traps and marked with individual combina- tions of colour-rings. During the whole daylight pe- riod, in any visit of a colour-ringed bird at a bowl, the number of mealworms taken was counted and later assigned to one of twelve sections of a standard day (see above). Because on the day of colour-mark- ing a Wheatear could not be observed all day long (e. g. because of arrival later than in the morning), only individuals present after the day of ringing were considered. Aggressive encounters between colour-ringed Wheatears and other birds (conspe- cifics and other species) were monitored and ana- lysed similarly. From 5-9 October 2001, the same type of experiment was conducted on the beach.

beach (spnng) beach (autumn)

80 t~

°~ ~ 40

o

o 2 N 20

0

>~ 8 0 , ~ m 80 ,_ _>

4o N 20

o time (30 mln before sunrise to 30 rain after sunset)

grass land (spr ing) g rass land (autumn)

m 8 0 -g 60 .~ 60

20

S

lOO 1oo

~ ~ ~Oo °i i'° i 60 "-> 60

40 ~ 40 o~ 20 ~ 20

- - 0 - -

time (30 rain before sunnSe to 30 rain after sunset)

R e s u l t s

Diurnal pat tern of t ime al locat ion

Foraging was the main activity shown by

Wheatears during stopovers on Helgoland and

occurred throughout the dayl ight per iod

(Fig. 1). Al though the t ime spent foraging in-

creased during the first ha l f of the day on the beach in spring and on grassland in autumn, no

clear pat tern with distinct peaks or troughs was

Fig. 1. Diurnal pattern of foraging, rest/vigilance and aggressive behaviour in Wheatears during standard days. Data were lumped for full-day obser- vations from beach and grassland for spring and au- tumn migration, respectively. For sample sizes see Table 1. Abb. 1. Tageszeitliches Muster von Nahrungs- suche, Ruhen/Wachsamkeit und Revierverteidigung von Steinschm~itzern an Relativtagen. Die Daten sind zusammengefasst f'tir Ganztagsbeobachtungen yon Strand und Grtinland bzw. ftir Heim- und Weg- zug. Stichprobenumfiinge sind in Tab. 1 angegeben.

38 Journal far Omithologie 144, 2003

Table 2. Results of scan sampling: absolute time and percentage of daylight period spent in five behaviou- ral categories by Northern Wheatears. For sample sizes see Table 1. Tab. 2. Ergebnisse der Verhaltensbeobachtungen: Absolute Zeit und Anteil an der Tageslichtperiode ftir ftinf Verhaltenskategorien (Nahmngssuche, Ruhen/Wachsamkeit, Revierverteidigung, Putzen, Fliegen). Stichprobenumffinge sind in Tab. 1 angegeben.

day foraging rest/vigilance aggression preening flight length

date habitat (min) min (%) min (%) min (%) min (%) rain (%)

spring migration

03May2000 grassland 975 622 (63.8) 208 (21.4) 2 (0.2) 29 (3.0) 113 (11.6)

05May2000 grassland 983 513 (52.1) 350 (35.6) 0 (0.0) 30 (3.0) 91 (9.21)

04May1999 beach 979 570 (58.2) 242 (24.7) 80 (8.2) 16 (1.7) 71 (7.3)

09May2000 beach 998 554 (55.5) 270 (27.1) 70 (7.1) 13 (1.3) 90 (9.0)

l lMay1999 beach 1005 540 (53.8) 271 (26.9) 80 (8.0) 24 (2.4) 90 (8.9)

23May2000 beach 1043 565 (54.2) 250 (24.0) 25 (2.4) 28 (2.7) 175 (16.8)

autumn migrati- on

22Aug2000 grassland 923 502 (54.4) 300 (32.5) 5 (0.5) 19 (2.1) 97 (10.5)

04Sep2000 grassland 869 411 (47.4) 388 (44.6) 0 (0.0) 18 (2.1) 52 (5.9)

28Aug1999 beach 898 661 (73.6) 151 (16.8) 18 (2.0) 3 (0.4) 65 (7.3)

01Sep1999 beach 881 629 (71.4) 192 (21.8) 3 (0.3) 3 (0.3) 54 (6.1)

12Sep2000 beach 835 456 (54.6) 138 (16.5) 96 (11.6) 11 (1.3) 133 (16.0)

15Sep2000 beach 822 489 (59.5) 140 (17.0) 39 (4.7) 6 (0.7) 149 (18.1)

22Sep2000 beach 792 542 (68.4) 126 (15.9) 30 (3.8) 7 (0.9) 87 (11.0)

28Sep2000 beach 767 547 (71.3) 117 (15.2) 31 (4.0) 9 (t.2) 63 (8.2) mean

spring grassland 567 (58.0) 279 (28.5) 1 (0.1) 30 (3.0) 102 (10.4)

spring beach 557 (55.4) 258 (25.7) 64 (6.4) 20 (2.0) 107 (10.5.)

autumn grassland 457 (50.9) 344 (38.6) 2 (0.3) 19 (2.1) 74 (8.2)

autumn beach 554 (66.5) 144 (17.2) 36 (4.4) 7 (0.8) 92 (11.1)

observed. The same holds true for resting/vigi- lant behaviour, which was the mirror image of foraging activity (Fig. 1). Aggressive behav- iour occurred on the beach throughout the day, but was almost completely lacking on grass- land (Fig. 1). In harmony with the results of scan sampling, Wheatears in the field experi- ment consistently foraged throughout the day- light period as expressed by the number of mealworms taken from the bowls. Only the very first part of the day typically showed a lower amount of food intake (Fig. 2). Aggres- sive encounters in the experiment were lacking

in early morning, peaked in the first half of the day, but were less frequent later on (Fig. 2).

Proportions of daylight period and total time devoted to activities

In all full-day observations, foraging made up the largest proportion of activities shown by Wheatears with percentages of daylight spent foraging ranging between 47.4 % and 73.6 % (Table 2). Most of the remaining time was used for rest and vigilance (15.2-44.6 %), whereas flying (5.9-18.1%), aggressive behaviour

V. Dierschke et al. . Migrating Northern Wheatears 39

(0 .0-11 .6%) and preening (0 .3 -3 .0%) ab- 20 sorbed less of the time budget. The total ~- amount of time devoted to the five activities "

~ 1 5 fluctuated greatly (Table 2). Total foraging o~ time was not correlated to the length of day- E light period (rs = 0.279, n = 14, P = 0.334), ~ 1 0

even if only observations from the beach are considered (rs = 0.321, n = 10, P -- 0.365), but c° 5 time spent resting/vigilant and preening in- creased when days were longer (rs = 0.675, n -- 0 14, P = 0.008 and rs = 0.657, n = 14, P = 0.011,

E 2 0 respectively). Mean values of foraging time

were quite similar for Wheatears in spring c

(both habitats) and autumn (beach), but much ~ 15 o

less time was used for foraging on grassland in ~- I1)

autumn (Table 2). As already mentioned, terri- >o 10 torial behaviour made up 0.5-1.5 hours on ~ most days on the beach, but was close to ab- sent in grassland (0-5 minutes per day, Ta- ~ 5 ble 2). Although not measured explicitly, for- aging time was very low for birds in the field o~ 0 experiment. Most or all of their daily energy intake occurred during a couple of short visits

to the bowls, where up to 21 mealworms were taken in a single visit. Fig. 2.

Time allocation and Wheatear density

Absolute foraging time was not related to the density of Wheatears (rs = 0.055, n = 14, P = 0.852). The same holds for aggressive behav- iour, which did not show a connection to

Wheatear density (total time aggressive: rs = -0.055, n = 14, P = 0.852). This result re- mained unchanged if only full-day observa- tions from the beach were considered (total foraging time: rs = 0.115, n = 10, P = 0.751; total t ime aggressive: rs = -0.304, n = 10, P = 0.393).

Time allocation and predation risk

Wheatear behaviour was not correlated with the rate of raptor flights across the study sites (total foraging time: rs = -0.075, n = 14, P = 0.799; total t ime resting/vigilant: rs = -0.260, n = 14, P = 0.370). From the analysis of single events of raptor flights, only a slight influence

time (30 min before sunrise to 30 min after sunset)

Diurnal pattern of foraging (percentages of mealworms taken from bowls, n = 7397) and ag- gressive behaviour (percentages of encounters ob- served, n = 1001) during standard days in the field experiment (lumped for 46 full-day periods, autumn migration). Abb.2. Tageszeitliches Muster der Nahrungs- suche (Anteile aller aus Schalen entnommenen Mehlwfirmer, n = 7397) und der Revierverteidigung (Anteile aller beobachteten Interaktionen, n = 1001/ an Relativtagen im Freilandexperiment (zusammen- gefasst far 46 Ganztagsperioden auf dem Wegzug).

on the percentage of resting/vigilant birds emerged. After the majority of raptor flights, this proportion remained more or less constant, whereas an increase of rest/vigilance was noted after 26 %, but a decrease after only 4 %

of raptor flights (Table 3).

Response to additional food

Bowls with mealworms strongly attracted Wheatears in the grassland habitat. Ninety-

40 Journal fiir Omithologie 144. 2003

Table 3. Changes of percentage of Northern Wheatears resting/vigilant from scans before to scans after single raptor flight events. In the case of more than one raptor flight between two scans only the last raptor species occurring was considered. Tab. 3. Ver~ndenmgen im Anteil ruhender/wachsamer Steinschmatzer von Z~ihlungen vor zu Z/ihlungen nach einzelnen Oberfliigen von Greifv6geln. Falls zwischen zwei Z~ihlungen mehr als ein Greifvogel er- schien, so wurde nur der letzte berticksichtigt.

percentage of birds resting/vigilant

decrease d e c r e a s e unchanged increase increase

-100to-60% -60to-20% -20to+20% +20to+60% +60to+100%

Sparrowhawk Accipiter nisus

European Kestrel Falco tinnunculus

European Hobby Falco subbuteo

Merlin Falco columbarius

Peregrine Falco peregrinus

total (incl. 2 unidentified raptors)

1 13 4 2

1 1 2 3 -

- 3 1 -

- - 5 - -

- 2 1 -

2 35 10 3

nine out of the total of 218 individually colour- ringed birds were seen to take mealworms after capture and ringing. As others may have taken mealworms before capture and did not return to the study site after release, this re- sponse to additional food is a conservative es- timate. The attractive feeding conditions are further endorsed by the high proportion of Wheatears staying beyond the day of arrival (38.1%, n = 218) compared to only 8.6% on grassland without additional food (Delingat & Dierschke 2000). Although 8-13 Wheatears were present on the beach when mealworms were offered in early October, the additional food was completely ignored. Instead, Wheat- ears fed intensively on kelp fly imagines, which were very abundant owing to large amounts of brown algae washed ashore during that time, and to lesser extend on kelp fly lar- vae.

D i s c u s s i o n

Diurnal pattern of time allocation

Since refuelling is the major task during mi- gratory stopovers, foraging was expected to occur during most of the daytime. The results of scan sampling generally confirmed the pre- ponderance of foraging, and diurnal variation among the activities studied was almost lack- ing. Nevertheless, on the beach in spring and on grassland in autumn, foraging activity was low in the morning and increased within the first half of the daylight period. It is possible that resting/vigilance behaviour refers to birds which had just arrived and recovered from the migratory flight (Schwilch et al. 2002), which could have been as long as several hundred ki- lometres or even more. Perhaps they also had to familiarise themselves with an unknown en- vironment, i. e. to explore for feeding opportu- nities and to check the situation regarding pre- dation risk. The reluctance to forage after arrival may also be due to neophobia (re- viewed by Woodrey 2000), Wheatears landing

V. Dierschke et al. • Migrating Northern Wheatears 41

on Helgoland having probably never before encountered the food types available on this is- land. Furthermore, after being partly metabol- ised during a long flight, the digestive tract of newly arrived birds may have to be restored in order to allow efficient foraging and thus re- fuelling (Hume & Biebach 1996, Lindstr6m etal. 1999, Gannes 2002). An early morning low in foraging activity was also found in the field experiment, in which only birds on days subsequent to arrival day are considered. The offer of ad libitum food rules out any effect of prey availability on the diurnal pattern of for- aging.

It seems that a minimum of about 20-30 % of time was needed as non-foraging time. A full digestive tract most probably was respon- sible for breaks in foraging, especially after the intake of tens or hundreds of kelp fly larvae within a few minutes. Such a pattern of mas- sive food intake in short feeding bouts and sub- sequent breaks of various duration was also shown by Wheatears in our field experiment, much similar to the food intake of Thrush Nightingales Luscinia luscinia in cage experi- ments (Kvist & Lindstrrm 2000). On the other hand, periods of low foraging activity also oc- curred in grassland habitat, where food intake is probably much lower (Dierschke in prep.). Safety interest seemed to have little impact on the time budget of Wheatears, because the amount of rest/vigilance did not correlate with predation risk. The dominance of foraging over safety behaviour has already been shown in other species during migration (Metcalfe & Furness 1984, Moore 1994).

Food-availability or metabolically limited refuelling?

Several observations from this study suggest that Wheatears stopping over on Helgoland beaches are metabolically limited in their re- fuelling rate. A strong indicator for this is the ignoring of an additional food supply, i. e, a re- duced searching and handling time would not further improve the relation between energy intake and energy expenditure within the phys-

iological capacity (Lindstr0m 1991). Further- more, longer daylight periods were not used to increase foraging times, i.e. longer foraging was perhaps not possible because the maxi- mum metabolisable energy intake had already been attained. Another sign of metabolic limi- tation is the relatively low proportion of day- light used for foraging compared to other bird species during stopover, generally leaving much time for other activities. The average foraging proportions of 51-67 % of daylight period were longer than those in two examples assigned to metabolically limited migrants by Lindstrrm (1991; 25 % in Rufous Humming- birds Selasphorus rufus, Hixon et al. 1983, and 34 % in Bramblings Fringilla montifringilla, Lindstrrm 1990), but shorter than values ob- tained for a number of shorebirds and geese (usually 60-80%; Drent 1980, Kiis 1984, Madsen 1985, Melter 1995, Stock & Hofeditz 1996, Dierschke 1997) as well as for three sylviid Warblers (78-82 %; Ilyina & Grachova 1990). The much time available for aggressive behaviour directed against conspecifics may also serve as evidence of unlimited foraging time on the beach.

In contrast to the beach situation, Wheatears strongly responded to additional food in grass- land habitat. This suggests that refuelling in this habitat, where the natural food supply de- clines sharply from August to October (Delin- gat & Dierschke 2000), is food-availability limited (Lindstrrm 1991). Nevertheless, total foraging time was also low in this habitat, es- pecially during autumn migration. The reason in this case is probably not the approach of a metabolic ceiling, but the general difference of habitat use. Compared to Wheatears on the beach, those in grassland are more transient with short stopover lengths and the tendency to explore the island for a suitable habitat (De- lingat & Dierschke 2000). Perhaps the birds recognized that a high refuelling rate cannot be obtained in that habitat, abandoned the attempt and prepared for onward migration, as is pre- dicted by optimal migration theory (Alerstam & Lindstr6m 1990) and shown for migrants

42 Journal ffir Omithologie 144, 2003

departing from unsuitable stopover sites else- where (Bruderer & Jenni 1988, Moore & Si- mons 1992, Jenni 1996, Spina & Pilastro 1999). Thus, the pattern of habitat use com- bined with the successive occurrence of differ- ent individuals probably superimposed the time budgets of single individuals actually re- fuelling in the grassland habitat. As a conse- quence, care has to be taken when birds are

observed in a poor habitat because low propor- tions of foraging in the time budget may be misinterpreted as being caused by a metabolic limitation. In situations where migrants are not settled but explore the area for the most suit-

able habitat, turnover of individuals restricts the reliability of scan sampling as a method for investigating the time budget of an average bird. As an indicator of which type of limita- tion in refuelling occurs, scan sampling should be accompanied by studies of foraging behav- iour, energy intake or experimental manipula- tion of feeding conditions.

The example of Wheatears, which were found to be metabolically limited in one habi- tat and food-availability limited in another, makes it clear that a given species is not gener- ally confined to one type of refuelling rate lim- itation. Flexibility in the use of a diversity of stopover site is an important feature for mi-

grating birds, which cannot expect to find their most favourable habitat everywhere along their migratory route (Bairlein 1981, Moore etal. 1990, Schaub & Jenni 2001). Regarding refuelling conditions such flexibility seems to

be less apparent in the time budgets of mi- grants, but is more obvious in the decision of skipping or using a stopover site (Moore et al. 1990, Jenni 1996, Morris et al. 1996). This was shown in Wheatears where the proportion and the duration of stopover is much higher in the

favourable beach habitat compared to the poorer grassland habitat (Delingat & Dier- schke 2000).

Acknowledgements Continuous field work throughout daylight periods was fundamental for the results of this study, which would have

been impossible without the help of volunteers during the full-day observations (Sophia Engel. Sophie Jaquier, Betti- na Mendel) as well as in the experiment (Sophie Jaquier, Maren Rebke. Annegret Walter). Considerable financial support was given by the "Freunde und F6rderer der Insel- station der Vogelwarte Helgoland e. V.'. Technical support was obtained from Ommo Htippop and Rolf Nagel. We are grateful to Franz BaMein for encouraging the study of stop- over ecology on Helgoland and for critically commenting on the manuscript, which was also much improved by Ake Lindstr6m. Further comments were kindly made by Ommo Htippop and an anonymous referee.

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Accepted: 17 September 2002