How do migratory songbirds cross the Sahara?

f&ny European songbirds winter in Africa south of the Sahara. Along their migratory routes they must fly over the huge desert belt of the Sahara twice u year. For decades ornithologists have igssumed that most migrants cross this ecological barrier’ in one lotig nour-stop /fight of thousands of kilometres. Results of recent research, however, suggest that /Wang of the song6irds that migrate across ihe Sahara follow an intermittent mi<‘ratory strategy with regular stopovers iti the desert.

Each year, millions of migrants that breed in Europe and winter in cub-Saharan Africa have to cross the Sahara desert belt twice fin autumn and spring), during their long-distance migratory flightsr-3. The Sahara (Fig. I) is generally thought of as an extremely inhospitable land with huge sandy regions, stony or rocky deserts, and tew oases - and therefore, practically no suitable stopover sites for birds’. Thus, it has usually been assumed that Palearctic passerine migrants flying over the Sahara I awards tropical Africa have to cross the Sahara in one long non-stop f ight, for which the birds depart even from north of the Mediterranean”. Based on this assumption, such migrants would fave to cover a distance of at least 2200-2400 km, which would require at least 40-60 hours of continuous flight. How do migrating songbirds cope with crossing the Sahara? Do tley really fly over the Sahara during their autumn migration in one long non-stop flight or do they stop Feriodically at suitable sites as t:ley do during migration over areas north of the Mediterranean?

HowDoMigratorySongbirdsCross the Sahara? Franz Bairlein periodic and temperature conditions exhibit spontaneous nocturnal activity only during those periods when freeliving specimens migrate, thus corresponding to the typically night migrating behaviour. This migratory restlessness, the socalled zugunruhe, in migratory warblers peaks at times when birds in the wild could be assumed to be crossing northern Africa. Furthermore, species-specific as well as population-specific levels of this nocturnal zugunruhe in captive birds during autumn migration are positively correlated with the distance travelled by the birds in the wild5,7-9. The degree of zugunruhe is genetically determinedlo. The body mass of many of these long-distance passerine migrants increases spontaneously prior to and during migration with mass gains of up to 100% above nonmigratory levels, both in the laboratory and in the wildr’~t2. This tremendous mass increase is mainly attributable to the deposition of large amounts of fat (Fig. 2). As lipids are the main source of energy for migratory flights’r,r3, this pronounced migratory fat deposition of long-distance migrants must be interpreted as an energetic adaptation for flights across ecological barriers such as water or des-

erts’ l,14. Migrants without a minimum amount of such fuel might not be able to migrate successfully. If no food is consumed during flight the amount of available fat determines the potential duration of non-stop flights. For a typical transSahara passerine migrant,, the garden warbler (Sylvia borin), this relationship is shown in Fig. 3: the more fuel on board, the wider is the theoretical flight range. Considering, for example, the Iminimum flight distance for a garden warbler crossing northern Africa nonstop, a large amount of fuel is needed to match the journey; there could be, however, some advantage of favourable tail-winds, at least in autumn4. Migratory songbirds, especially the inexperienced young, are equipped with an innate migratory programme that determines the temporal events for their migration as well as seasonal changes in migratory directionr6,17. IHowever, neither such endogenous timing mechanisms nor the deposition of large amounts of fuel constitute support for the non-stop crossing hypothesis to the exclusion of other ideas. Field data on Sahara crossing Recently, there has

been

40’

an

SO’

The endogenous control of migration Laboratory data on migratory behaviour in songbirds, in particuLlr from Old world Sylvia and Phyl/oscopus warblers, clearly reveal that their migration is largely contr,olled by internal, mostly innate nlechanisms5,“,7. For instance, migratory warblers kept individually if) cages at controlled photo-

FranzBairlein is at the Physiological Ecology Sectitan, Department of Zoology, University of Koeln, Weyertaf 119, D-5000 Koeln 41, Federal Republicof C zrmany

20.

0’

20.

Fig. I. The Sahara desert belt in N. Africa. The stippled by less than 100 mm annual rainfall.

40’ area shows the extent

60’

of the Sahara as defined

TREE vol. 3, no. 8, August

Fig. 2. Long-distancemigratory songbirds deposit large amounts of fat for their subcutaneous by F. Bairlein

depot is clearly visible on parting the breast feathers. lal a lean bird;

fbl

journeys This a fat one. Photos

over sites, to catch grounded migrants and to check their body mass and the visible subcutaneous deposits of fat. In addition, repeated trappings of individuals provide information on the duration of rest periods, on weight changes and thus on the refuelling conditions during stopover. Surprisingly, some of the results of recent fieldwork on migrants in the Sahara indicated that many more passerines, both in terms of species and numbers, were recorded at the various study sites than previously suggested on the basis of the non-stop hypothesis. For example, specimens of almost all of those species which are known to pass over the Sahara’,’ were recorded - mainly warblers, yellow wagtails, swallows, flycatchers and redstarts. The daily turnover of longdistance migrants at oases, as determined by multiple daily census 4000 7.5 mlsec g of migrants along a fixed transect, is 5 m/set .$ high, indicating very short resting & periods and a rapid passage2’. This conclusion is also supported by reE still-air & captures of individuals. The time f: 5 2000 L 1 between their first and last trapI ‘minimum stopover ping, the 5 mlsec % .s g 1000 period’, was very short (in most 3 ,m cases only 1-2 days). g 30000 & Most birds that were found 15 20 25 30 grounded in autumn were in very Body weight (g) good physiological condition, i.e. their body mass and fat levels were Fig. 3. Relationship between theoretical flight range high (Fig. 4). The proportion of lean (calculated according to Tucker”) and body mass in birds without visible subcutaneous garden warblers in relation to wind conditions. Still-air condition is considered to be an average for natural fat was surprisingly low. Most birds migration. A body mass of I5 g is assumed to be an carried fat, and were not exhausted. approximation to a fat-free body The dotted lines Among those birds caught in larger indicate minimum flight distance from S. Spain to well-established oases, the proporsub-Sahara and the corresponding body mass. From Ref IS. tion of lean birds was higher than increasing number of field studies of desert crossings by migrant birdslC20. The main problem facing investigators, however, is one of how to gather appropriate information. If migrants cross the desert according to the non-stop crossing hypothesis, largely controlled by innate mechanisms, then not only would the number of individual birds found grounded in potential stopover sites in the desert (e.g. oases) be relatively small, but such birds would have to be regarded as ‘fallouts’ that had been forced to break their endogenous migratory programme (probably because their fuel and/or water reserves were exhausted and would not permit them to migrate further south). One way to tackle this problem is to gather data on the occurrence of migrants in potential desert stop-

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among those caught at an artificial trapping site within the desert” or in a very small oasis with only a few bushes (Fig. 41; this indicates that the decision of where to land seems to be related to the fuel reserves of the individual migrant19. Because some of the birds trapped for the first time were later retrapped at the same site, one can ask whether there are physiological differences between such retraps and single traps, comparing both at their first trapping. In one species trapped at an Egyptian oasis (Fig, 51, the frequency distributions of body mass and fat score of individuals differed significantly between the two groups: there was a much higher proportion of initially light and lean birds in retraps. Thus, lean birds in particular used the oasis as a staging area. Figure 6 shows that the food available at this oasis enabled birds with less reserves to refuel. The individuals gained weight and the proportion of birds with more extensive fat depots increased. Thus, long-distance migrants grounded with less fuel can in fact replenish their fat reserves within Saharan oases - a conclusion that is supported by the analyses of stomach content and faeces and by observational data on feeding behaviour’8,1? Birds with no visible fat at their first trapping were retaught more often than birds with initially higher fat scores, and the minimum length of stopover depended on the initial fat score: lean birds rested for longer than fatter birds. Although the results presented on the physiological state of captured birds suggest that migrant songbirds found grounded in the Sahara in the autumn should be able to continue their southward migration (albeit sometimes after refuellingl, it is difficult to know whether they do in fact fly further. Experiments with garden warblers caged after their first trapping provided an answer. The activities of the birds, recorded electromechanically in cages with two perches, depended on body mass and fat score. Lean birds with no visible fat were active only during the daylight period, and they fed on food offered in the cages. Fat birds with significant reserves, however, were

i’REE vol. 3, no. 8, August

1988 80 (a)

inactive during the daylight hours, and they did not feed despite food being offered. At night, these fat birds showed nocturnal restlessness, corresponding to their mig*atory activity’“. This relationship between fat reserves, food availa 3ility and nocturnal restlessness has also been demonstrated controlled laboratory u lder conditions”,‘3. Slopover in northern Algeria As shown above, at least some species of migrant songbirds seem tc.1cross the Sahara in autumn in short stages with some rest at deselt stopover sites. This being the cclse, then it might be expected ttat these species should also make landfall in stopover sites along the coastal region of northern Alrica, after crossing the Mediterranean Sea and prior to setting off on the first stage of their trans-Saharan journey. In fact, a large number of migratory birds were caught in a some kilometres resting area inland from the coast in north west Algeria during autumn migration (Ref. 15 and F. Bairlein, unpubIi? hedl. Most of the captured songbirds showed low to moderate deposits of fat at their first trapping. They gained mass and deposited fan stores very rapidly, taking aclvantage of the plentiful supplies of insects and fruits (e.g. figs, 01 ves) which are known to provide in- portant food during migratory fat dt*position”.24. Thus, they replenished their fat deposits in prepar&ion for their further exhausting journey across the desert. Therefo!.e, resting areas in northern Africa rn,ay be much more important for passerine migrants than previously supposed. These areas are of great sip:nificance for the successful conservation of migrating songbird pcpulations, which are declining almost everywhere in Europe25.26. Strategies for crossing the desert We are now able to reconsider previous ideas and to add a further idea regarding migration of songbil,ds across the Sahara, at least in the autumn. Following a night of mEgration towards the Sahara desert a songbird needs to have enough fuel to be independent of feeding areas during subsequent migration. Therefore, fuel is replenished at least just north of the

desert. From dawn onwards, the bird tries to find a resting place similar to those in areas away from the desert. However, the decision where to land seems to be related to the fat reserves of the individual. For birds grounded with high fat stores, refuelling is not necessary. Thus, they rest, inactive, in the shade throughout the day and then continue their migratory journey the following night; they cross the desert very quickly. For these fat birds, it is sufficient for them to find a place that offers enough shade to meet the thermoregulatory needs (particularly water balance) of a rest. Therefore, mountain ridges as well as oases could be appropriate stopover sites; migrants can indeed be found here in holes up to depths of 0.5 m (Ref. 191. Shaded places are really quite common in the desert, especially in the far west region along the Atlantic coast, in the central parts from the High Atlas mountains southeast to the Ahaggar and the Air mountains and in the eastern Sahara along the Nile valleylJ’. Because of their diurnal inactivity fat birds are difficult to observe, which may be why so few migrants could be observed by bird watchers in desert habitats during autumn migration’. The use of mist-nets has now indicated the presence of birds which had hitherto been overlooked and has also showed some species to be much more common than previously suspetted. Birds grounded with very low amounts of fat depend on locally available food; they must refuel to resume successful migration. If food sources do not exist the birds might have made a fatal ‘mistake’. However, if they land at places rich in vegetation and food (especially insects and fleshy fruits in oases) they forage actively during the day and are therefore more easily observed. If the amount of energy refuelled during the day is sufficient for a further flight, the bird will resume its migration the following night. However, a bird may have to spend several days in the staging area until it has accumulated enough fat for a further flight. As the proportion of really lean exhausted birds is relatively low, however, compared to all individuals migrating across the Sahara (see Fig. 3), no conspicuous mass influx of

30~

Marroket / Nebka (74)

80 40

t W

e I

30

1

70

Hadjar (49)

50 30

Yi,,,,,&,’ 10

20

30

10 0

Body weight (g)

0123 Fat score

Fig. 4. Body mass and fat score (scaled from 0: no visible fat, to 3: a lot of visible fatlHl of garden warblers caught in two oases in central Algeria during fall migration. la) a large oasis, lb1 a very small oasis. From Ref 15.

migrants in desert oases would normally be expected: although they are present, they are almost inactive. Recent papers on trans-Sahara songbird migration are in agreement that stopovers seem to be a well-developed strategy in the Sahara, and that many European long-distance passerine migrants apparently cross the Sahara (at least in autumn) in stages rather than in one long hop. At the moment, most of the available data are concentrated on species like warblers, flycatchers, redstarts and yellow wagtails for which intermittent crossing of the desert seems to be an adequate strategy. For more aerial species, in particular the hirundines, data from desert habitats are scarce; grounded individuals seem to have a relatively low body mass, suggesting a nonstop crossing strategy. However, we should remember that both of the strategies mentioned are the extremes in a gradient of possible

Fig. 5. Frequency distribution of body mass of yellow wagtails lhfotacilla flaval caught only once (open columns; n = I 179) and at first capture of retraps (stippled columns ; n = 321 in an Egyptian oasis during fall migration. Data from Ref 19.

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TREE vol. 3, no. 8, August

0

4

minimum

6

12

stopover

16 period

20

24

( days )

Fig. 6. Changes in body mass of individual retrapped yellow wagtails in an Egyptian oasis. The changes in body mass are plotted relative to the body mass at the first capture fn = 321. Redrawn from Ref. 19.

tactics to cope with trans-Sahara migration. At the moment, however, the data are too scarce to evaluate the various tactics at the level of particular species. Hitherto, I have focused on transSahara migration during autumn together with the need for energy fuelling north of the desert. During return migration to the breeding grounds in spring the strategy of trans-Sahara migration appears to be similar, with a pronounced deposition of fat in the northern Guinea savanna prior to the northward journey27-29. The spring migratory programme seems to be dominated much more by time constraints because of a greater urgency to reach the breeding grounds; this results in a more rapid migration than in autumn20. In addition, after the winter cooling period, dehydration could be less of a problem. Therefore, a non-stop crossing of the desert seems to have some advantage. However, the weather conditions in spring

are different, with more unfavourable winds4. Moreover, vegetation and food (insects) are less scant in spring than in autumn, thus favouring crossing of the desert in stages. The idea that at least some species cross the Sahara by an intermittent migratory strategy is based on some clear evidence. This strategy also seems to be adopted by migrants in middle Asian deserts, both in the autumn and in the The idea has recently spring30,j’. received some further support from a re-evaluation of data on water balance during long flights; flight duration, and thus flight range, appear to be strongly limited by an increasing degree of dehydration of the birds’ body with increasing ambient temperaturejl. For long flights across deserts, it is evident that water loss must be reduced to a minimum, probably by flying at night and resting in the shade throughout the hot hours of the day or by flying at higher altitudes in cooler ai+? At present however, there is no detailed information either on the altitude of flight or on the local meteorological conditions over the desert, although G. Schaefer fin Ref. I ) has reported migrants in autumn moving at heights as high as 3 km. Therefore, radar studies of bird migration over the Sahara will be needed, together with weather data and further studies on the ground. These radar data will also indicate the proportion of desert migrants that use staging posts whilst undertaking the Sahara crossing’, and provide information on the question of broad-front migration across northern Africa versus migration along ‘flyways2r

1988

Acknowledgements I wish to thank Prof. Dr Neumann and Dr Biebach for critically reading the manuscript and Martin Brett for improving the English text In addition, many thanks to the referees for their helpful comments.

References

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