A mimicked bacterial infection prolongs stopover duration in songbirds-but more pronounced in short- than long-distance migrants.

Migration usually consists of intermittent travel and stopovers, the latter being crucially important for individuals to recover and refuel to successfully complete migration. Quantifying how sickness behaviours influence stopovers is crucial for our understanding of migration ecology and how diseases spread. However, little is known about infections in songbirds, which constitute the majority of avian migrants. We experimentally immune-challenged autumn migrating passerines (both short- and long-distance migrating species) with a simulated bacterial infection. Using an automated radiotelemetry system in the stopover area, we subsequently quantified stopover duration, "bush-level" activity patterns (0.1-30 m) and landscape movements (30-6,000 m). We show that compared to controls, immune-challenged birds prolonged their stopover duration by on average 1.2 days in long-distance and 2.9 days in short-distance migrants, respectively (100%-126% longer than controls, respectively). During the prolonged stopover, the immune-challenged birds kept a high "bush-level" activity (which was unexpected) but reduced their local movements, independent of migration strategy. Baseline immune function, but not blood parasite infections prior to the immune challenge, had a prolonging effect on stopover duration, particularly in long-distance migrants. We conclude that a mimicked bacterial infection does not cause lethargy, per se, but restricts landscape movements and prolongs stopover duration, and that this behavioural response also depends on the status of baseline immune function and migration strategy. This adds a new level to the understanding of how acute inflammation affect migration behaviour and hence the ecology and evolution of migration. Accounting for these effects of bacterial infections will also enable us to fine-tune and apply optimal migration theory. Finally, it will help us predicting how migrating animals may respond to increased pathogen pressure caused by global change.

Immune function and blood parasite infections impact stopover ecology in passerine birds.

Stopovers play a crucial role for the success of migrating animals and are key to optimal migration theory. Variation in refuelling rates, stopover duration and departure decisions among individuals has been related to several external factors. The physiological mechanisms shaping stopover ecology are, however, less well understood. Here, we explore how immune function and blood parasite infections relate to several aspects of stopover behaviour in autumn migrating short- and long-distance migrating songbirds. We blood sampled individuals of six species and used an automated radio-telemetry system in the stopover area to subsequently quantify stopover duration, 'bush-level' activity patterns (~ 0.1-30 m), landscape movements (~ 30-6000 m), departure direction and departure time. We show that complement activity, the acute phase protein haptoglobin and blood parasite infections were related to prolonged stopover duration. Complement activity (i.e., lysis) and total immunoglobulins were negatively correlated with bush-level activity patterns. The differences partly depended on whether birds were long-distance or short-distance migrants. Birds infected with avian malaria-like parasites showed longer landscape movements during the stopover than uninfected individuals, and birds with double blood parasite infections departed more than 2.5 h later after sunset/sunrise suggesting shorter flight bouts. We conclude that variation in baseline immune function and blood parasite infection status affects stopover ecology and helps explain individual variation in stopover behaviour. These differences affect overall migration speed, and thus can have significant impact on migration success and induce carry-over effects on other annual-cycle stages. Immune function and blood parasites should, therefore, be considered as important factors when applying optimal migration theory.

Actogram analysis of free-flying migratory birds: new perspectives based on acceleration logging.

The use of accelerometers has become an important part of biologging techniques for large-sized birds with accelerometer data providing information about flight mode, wing-beat pattern, behaviour and energy expenditure. Such data show that birds using much energy-saving soaring/gliding flight like frigatebirds and swifts can stay airborne without landing for several months. Successful accelerometer studies have recently been conducted also for free-flying small songbirds during their entire annual cycle. Here we review the principles and possibilities for accelerometer studies in bird migration. We use the first annual actograms (for red-backed shrike Lanius collurio) to explore new analyses and insights that become possible with accelerometer data. Actogram data allow precise estimates of numbers of flights, flight durations as well as departure/landing times during the annual cycle. Annual and diurnal rhythms of migratory flights, as well as prolonged nocturnal flights across desert barriers are illustrated. The shifting balance between flight, rest and different intensities of activity throughout the year as revealed by actogram data can be used to analyse exertion levels during different phases of the life cycle. Accelerometer recording of the annual activity patterns of individual birds will open up a new dimension in bird migration research.

Adaptive strategies in nocturnally migrating insects and songbirds: contrasting responses to wind.

Animals that use flight as their mode of transportation must cope with the fact that their migration and orientation performance is strongly affected by the flow of the medium they are moving in, that is by the winds. Different strategies can be used to mitigate the negative effects and benefit from the positive effects of a moving flow. The strategies an animal can use will be constrained by the relationship between the speed of the flow and the speed of the animal's own propulsion in relation to the surrounding air. Here we analyse entomological and ornithological radar data from north-western Europe to investigate how two different nocturnal migrant taxa, the noctuid moth Autographa gamma and songbirds, deal with wind by analysing variation in resulting flight directions in relation to the wind-dependent angle between the animal's heading and track direction. Our results, from fixed locations along the migratory journey, reveal different global strategies used by moths and songbirds during their migratory journeys. As expected, nocturnally migrating moths experienced a greater degree of wind drift than nocturnally migrating songbirds, but both groups were more affected by wind in autumn than in spring. The songbirds' strategies involve elements of both drift and compensation, providing some benefits from wind in combination with destination and time control. In contrast, moths expose themselves to a significantly higher degree of drift in order to obtain strong wind assistance, surpassing the songbirds in mean ground speed, at the cost of a comparatively lower spatiotemporal migratory precision. Moths and songbirds show contrasting but adaptive responses to migrating through a moving flow, which are fine-tuned to the respective flight capabilities of each group in relation to the wind currents they travel within.

When and where does mortality occur in migratory birds? Direct evidence from long-term satellite tracking of raptors.

Information about when and where animals die is important to understand population regulation. In migratory animals, mortality might occur not only during the stationary periods (e.g. breeding and wintering) but also during the migration seasons. However, the relative importance of population limiting factors during different periods of the year remains poorly understood, and previous studies mainly relied on indirect evidence. Here, we provide direct evidence about when and where migrants die by identifying cases of confirmed and probable deaths in three species of long-distance migratory raptors tracked by satellite telemetry. We show that mortality rate was about six times higher during migration seasons than during stationary periods. However, total mortality was surprisingly similar between periods, which can be explained by the fact that risky migration periods are shorter than safer stationary periods. Nevertheless, more than half of the annual mortality occurred during migration. We also found spatiotemporal patterns in mortality: spring mortality occurred mainly in Africa in association with the crossing of the Sahara desert, while most mortality during autumn took place in Europe. Our results strongly suggest that events during the migration seasons have an important impact on the population dynamics of long-distance migrants. We speculate that mortality during spring migration may account for short-term annual variation in survival and population sizes, while mortality during autumn migration may be more important for long-term population regulation (through density-dependent effects).

Differences in speed and duration of bird migration between spring and autumn.

It has been suggested that birds migrate faster in spring than in autumn because of competition for arrival order at breeding grounds and environmental factors such as increased daylight. Investigating spring and autumn migration performances is important for understanding ecological and evolutionary constraints in the timing and speed of migration. We compiled measurements from tracking studies and found a consistent predominance of cases showing higher speeds and shorter durations during spring compared to autumn, in terms of flight speeds (airspeed, ground speed, daily travel speed), stopover duration, and total speed and duration of migration. Seasonal differences in flight speeds were generally smaller than those in stopover durations and total speed/duration of migration, indicating that rates of foraging and fuel deposition were more important than flight speed in accounting for differences in overall migration performance. Still, the seasonal differences in flight speeds provide important support for time selection in spring migration.

Solar heating may explain extreme diel flight altitude changes in migrating birds.

Great reed warblers, Acrocephalus arundinaceus,1 and great snipes, Gallinago media,2 exhibit a diel cycle in flight altitudes-flying much higher during the day than the night-when performing migratory flights covering both night and day. One hypothesis proposed to explain this behavior is that the birds face additional heating by solar radiation during daytime and hence must climb to very high, and thus also very cold, altitudes to avoid overheating during daytime flights.1,2 Yet, solar heat gain in birds has been shown to drastically decrease with wind speed,3,4 and the quantitative heating effect by solar radiation on a bird flying with an airspeed of 10 m/s or more is unknown. We analyzed temperature data from multisensor data loggers (MDLs)5,6 placed without direct exposure to solar radiation on great reed warblers (the logger covered by feathers on the back) and great snipes (the logger on the leg, covered from the sun by the tail). We found that logger temperatures were significantly higher (5.9°C-8.8°C in great reed warblers and 4.8°C-5.4°C in great snipes) during the day than during the night in birds flying at the same altitudes (and thus also the same expected ambient air temperatures). These results strongly indicate that the heat balance of the flying birds is indeed affected by solar radiation, which is in accordance with the hypothesis that solar radiation is a key factor causing the remarkable diel cycles in flight altitude observed in these two long-distance migrant bird species.1,2.

The annual cycle of a trans-equatorial Eurasian-African passerine migrant: different spatio-temporal strategies for autumn and spring migration.

The small size of the billions of migrating songbirds commuting between temperate breeding sites and the tropics has long prevented the study of the largest part of their annual cycle outside the breeding grounds. Using light-level loggers (geolocators), we recorded the entire annual migratory cycle of the red-backed shrike Lanius collurio, a trans-equatorial Eurasian-African passerine migrant. We tested differences between autumn and spring migration for nine individuals. Duration of migration between breeding and winter sites was significantly longer in autumn (average 96 days) when compared with spring (63 days). This difference was explained by much longer staging periods during autumn (71 days) than spring (9 days). Between staging periods, the birds travelled faster during autumn (356 km d(-1)) than during spring (233 km d(-1)). All birds made a protracted stop (53 days) in Sahelian sub-Sahara on southbound migration. The birds performed a distinct loop migration (22 000 km) where spring distance, including a detour across the Arabian Peninsula, exceeded the autumn distance by 22 per cent. Geographical scatter between routes was particularly narrow in spring, with navigational convergence towards the crossing point from Africa to the Arabian Peninsula. Temporal variation between individuals was relatively constant, while different individuals tended to be consistently early or late at different departure/arrival occasions during the annual cycle. These results demonstrate the existence of fundamentally different spatio-temporal migration strategies used by the birds during autumn and spring migration, and that songbirds may rely on distinct staging areas for completion of their annual cycle, suggesting more sophisticated endogenous control mechanisms than merely clock-and-compass guidance among terrestrial solitary migrants. After a century with metal-ringing, year-round tracking of long-distance migratory songbirds promises further insights into bird migration.

Activity patterns throughout the annual cycle in a long-distance migratory songbird, the red-backed shrike Lanius collurio.

BACKGROUND: Long-distance migratory birds undergo complex annual cycles during which they must adjust their behaviour according to the needs and conditions encountered throughout the year. Yet, variation in activity throughout the entire annual cycle has rarely been studied in wild migratory birds. METHODS: We used multisensor data loggers to evaluate the patterns of activity throughout the complete annual cycle of a long-distance migratory bird, the red-backed shrike Lanius collurio. Accelerometer data was used to identify life-history stages and to estimate levels of activity during various phases of the annual cycle. In this study, we analysed the variation in daytime activity along the annual cycle and between migratory and non-migratory days. RESULTS: The birds' daytime activity varied throughout the annual cycle while night-time activity was almost exclusively restricted to migratory flights. The highest daytime activity levels were observed during the breeding season, while it remained low during autumn migration and the winter period. Daytime activity differed between sexes during the breeding period, when the males showed the highest level in activity. During migratory periods, both sexes exhibited a higher daytime activity in spring compared to autumn migration, being particularly high in the final migratory leg towards the breeding ground. The birds showed a lower daytime activity on migratory days (days when a migratory flight took place during the succeeding night) than on non-migratory days during both migratory seasons. CONCLUSIONS: Activity measured during daytime results from a combination of several behaviours, and a high daytime activity during spring migration and the breeding period is possibly reflecting particularly energy-demanding periods in the annual cycle of migratory birds. The use of multisensor data loggers to track annual activity provides us with a full annual perspective on variation in activity in long-distance migratory species, an essential approach for understanding possible critical life-history stages and migration ecology.

Geographical and temporal flexibility in the response to crosswinds by migrating raptors.

Wind and ocean currents may potentially have important effects on travelling animals, as an animal which does not respond to lateral flow will be drifted from its intended direction of movement. By analysing daily movements of migrating ospreys Pandion haliaetus and marsh harriers Circus aeruginosus, as recorded by satellite telemetry, in relation to global wind data, we showed that these raptors allow on average 47 per cent drift. Furthermore, our analyses revealed significant geographical and temporal variation in the response to crosswinds. During some parts of the migration, the birds drifted and in other parts they compensated or even overcompensated. In some regions, the response of marsh harriers depended on the wind direction. They drifted when the wind came from one side and (over)compensated when the wind came from the opposite side, and this flexible response was different in different geographical regions. These results suggest that migrating raptors modulate their response to crosswinds at different places and times during their travels and show that individual birds use a much more varied repertoire of behavioural responses to wind than hitherto assumed. Our results may also explain why contrasting and variable results have been obtained in previous studies of the effect of wind on bird migration.

Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds.

Vast numbers of insects and passerines achieve long-distance migrations between summer and winter locations by undertaking high-altitude nocturnal flights. Insects such as noctuid moths fly relatively slowly in relation to the surrounding air, with airspeeds approximately one-third of that of passerines. Thus, it has been widely assumed that windborne insect migrants will have comparatively little control over their migration speed and direction compared with migrant birds. We used radar to carry out the first comparative analyses of the flight behaviour and migratory strategies of insects and birds under nearly equivalent natural conditions. Contrary to expectations, noctuid moths attained almost identical ground speeds and travel directions compared with passerines, despite their very different flight powers and sensory capacities. Moths achieved fast travel speeds in seasonally appropriate migration directions by exploiting favourably directed winds and selecting flight altitudes that coincided with the fastest air streams. By contrast, passerines were less selective of wind conditions, relying on self-powered flight in their seasonally preferred direction, often with little or no tailwind assistance. Our results demonstrate that noctuid moths and passerines show contrasting risk-prone and risk-averse migratory strategies in relation to wind. Comparative studies of the flight behaviours of distantly related taxa are critically important for understanding the evolution of animal migration strategies.

Individuality in bird migration: routes and timing.

The exploration of animal migration has entered a new era with individual-based tracking during multiple years. Here, we investigated repeated migratory journeys of a long-distance migrating bird, the marsh harrier Circus aeruginosus, in order to analyse the variation within and between individuals with respect to routes and timing. We found that there was a stronger individual repeatability in time than in space. Thus, the annual timing of migration varied much less between repeated journeys of the same individual than between different individuals, while there was considerable variation in the routes of the same individual on repeated journeys. The overall contrast in repeatability between time and space was unexpected and may be owing to strong endogenous control of timing, while short-term variation in environmental conditions (weather and habitat) might promote route flexibility. The individual variation in migration routes indicates that the birds navigate mainly by other means than detailed route recapitulation based on landmark recognition.

Great flights by great snipes: long and fast non-stop migration over benign habitats.

Migratory land birds perform extreme endurance flights when crossing ecological barriers, such as deserts, oceans and ice-caps. When travelling over benign areas, birds are expected to migrate by shorter flight steps, since carrying the heavy fuel loads needed for long non-stop flights comes at considerable cost. Here, we show that great snipes Gallinago media made long and fast non-stop flights (4300-6800 km in 48-96 h), not only over deserts and seas but also over wide areas of suitable habitats, which represents a previously unknown migration strategy among land birds. Furthermore, the great snipes achieved very high ground speeds (15-27 m s(-1)), which was not an effect of strong tailwind support, and we know of no other animal that travels this rapidly over such a long distance. Our results demonstrate that some migratory birds are prepared to accept extreme costs of strenuous exercise and large fuel loads, even when stopover sites are available along the route and there is little tailwind assistance. A strategy of storing a lot of energy before departure, even if migration is over benign habitats, may be advantageous owing to differential conditions of fuel deposition, predation or infection risk along the migration route.

Extreme altitudes during diurnal flights in a nocturnal songbird migrant.

Billions of nocturnally migrating songbirds fly across oceans and deserts on their annual journeys. Using multisensor data loggers, we show that great reed warblers (Acrocephalus arundinaceus) regularly prolong their otherwise strictly nocturnal flights into daytime when crossing the Mediterranean Sea and the Sahara Desert. Unexpectedly, when prolonging their flights, they climbed steeply at dawn, from a mean of 2394 meters above sea level to reach extreme cruising altitudes (mean 5367 and maximum 6267 meters above sea level) during daytime flights. This previously unknown behavior of using exceedingly high flight altitudes when migrating during daytime could be caused by diel variation in ambient temperature, winds, predation, vision range, and solar radiation. Our finding of this notable behavior provides new perspectives on constraints in bird flight and might help to explain the evolution of nocturnal migration.

Extreme altitude changes between night and day during marathon flights of great snipes.

Several factors affect the flight altitude of migratory birds, such as topography, ambient temperature, wind conditions, air humidity, predation avoidance, landmark orientation, and avoiding over-heating from direct sunlight.1-6 Recent tracking of migratory birds over long distances has shown that migrants change flight altitude more commonly and dramatically than previously thought.4-8 The reasons behind these altitude changes are not well understood. In their seasonal migrations between Sweden and sub-Saharan Africa, great snipes Gallinago media make non-stop flights of 4,000-7,000 km, lasting 60-90 h.9,10 Activity and air pressure data from multisensor dataloggers showed that great snipes repeatedly changed altitudes around dawn and dusk, between average cruising heights about 2,000 m (above sea level) at night and around 4,000 m during daytime. Frequency and autocorrelation analyses corroborated a conspicuous diel cycle in flight altitude. Most birds regularly flew at 6,000 m and one bird reached 8,700 m, possibly the highest altitude ever recorded for an identified migrating bird. The diel altitude changes took place independently of climate zone, topography, and habitat overflown. Ambient temperature, wind condition, and humidity have no important diel variation at the high altitudes chosen by great snipes. Instead, improved view for orientation by landmarks, predator avoidance, and not least, seeking cold altitudes at day to counteract heating from direct sunlight are the most plausible explanations for the diel altitude cycle. Together with similar recent findings for a small songbird,6 the great snipes' altitudinal performance sheds new light on the complexity and challenges of migratory flights.

Flight speeds among bird species: allometric and phylogenetic effects.

Flight speed is expected to increase with mass and wing loading among flying animals and aircraft for fundamental aerodynamic reasons. Assuming geometrical and dynamical similarity, cruising flight speed is predicted to vary as (body mass)(1/6) and (wing loading)(1/2) among bird species. To test these scaling rules and the general importance of mass and wing loading for bird flight speeds, we used tracking radar to measure flapping flight speeds of individuals or flocks of migrating birds visually identified to species as well as their altitude and winds at the altitudes where the birds were flying. Equivalent airspeeds (airspeeds corrected to sea level air density, Ue) of 138 species, ranging 0.01-10 kg in mass, were analysed in relation to biometry and phylogeny. Scaling exponents in relation to mass and wing loading were significantly smaller than predicted (about 0.12 and 0.32, respectively, with similar results for analyses based on species and independent phylogenetic contrasts). These low scaling exponents may be the result of evolutionary restrictions on bird flight-speed range, counteracting too slow flight speeds among species with low wing loading and too fast speeds among species with high wing loading. This compression of speed range is partly attained through geometric differences, with aspect ratio showing a positive relationship with body mass and wing loading, but additional factors are required to fully explain the small scaling exponent of Ue in relation to wing loading. Furthermore, mass and wing loading accounted for only a limited proportion of the variation in Ue. Phylogeny was a powerful factor, in combination with wing loading, to account for the variation in Ue. These results demonstrate that functional flight adaptations and constraints associated with different evolutionary lineages have an important influence on cruising flapping flight speed that goes beyond the general aerodynamic scaling effects of mass and wing loading.

How hazardous is the Sahara Desert crossing for migratory birds? Indications from satellite tracking of raptors.

We investigated the risk associated with crossing the Sahara Desert for migrating birds by evaluating more than 90 journeys across this desert by four species of raptors (osprey Pandion haliaetus, honey buzzard Pernis apivorus, marsh harrier Circus aeruginosus and Eurasian hobby Falco subbuteo) recorded by satellite telemetry. Forty per cent of the crossings included events of aberrant behaviours, such as abrupt course changes, slow travel speeds, interruptions, aborted crossings followed by retreats from the desert and failed crossings due to death, indicating difficulties for the migrants. The mortality during the Sahara crossing was 31 per cent per crossing attempt for juveniles (first autumn migration), compared with only 2 per cent for adults (autumn and spring combined). Mortality associated with the Sahara passage made up a substantial fraction (up to about half for juveniles) of the total annual mortality, demonstrating that this passage has a profound influence on survival and fitness of migrants. Aberrant behaviours resulted in late arrival at the breeding grounds and an increased probability of breeding failure (carry-over effects). This study also demonstrates that satellite tracking can be a powerful method to reveal when and where birds are exposed to enhanced risk and mortality during their annual cycles.

Migratory and resident blue tits Cyanistes caeruleus differ in their reaction to a novel object.

Individuals differ consistently in their behavioural reactions towards novel objects and new situations. Reaction to novelty is one part of a suit of individually consistent behaviours called coping strategies or personalities and is often summarised as bold or shy behaviour. Coping strategies could be particularly important for migrating birds exposed to novel environments on their journeys. We compared the average approach latencies to a novel object among migrants and residents in partially migratory blue tits Cyanistes caeruleus. In this test, we found migrating blue tits to have shorter approach latencies than had resident ones. Behavioural reactions to novelty can affect the readiness to migrate and short approach latency may have an adaptive value during migration. Individual behaviour towards novelty might be incorporated among the factors associated with migratory or resident behaviour in a partially migratory population.

Converging migration routes of Eurasian hobbies Falco subbuteo crossing the African equatorial rain forest.

Autumn migration of adult Eurasian hobbies Falco subbuteo from Europe to southern Africa was recorded by satellite telemetry and observed routes were compared with randomly simulated routes. Two non-random features of observed routes were revealed: (i) shifts to more westerly longitudes than straight paths to destinations and (ii) strong route convergence towards a restricted area close to the equator (1 degree S, 15 degrees E). The birds migrated south or southwest to approximately 10 degrees N, where they changed to south-easterly courses. The maximal spread between routes at 10 degrees N (2134 km) rapidly decreased to a minimum (67 km) close to the equator. We found a striking relationship between the route convergence and the distribution of continuous rainforest, suggesting that hobbies minimize flight distance across the forest, concentrating in a corridor where habitat may be more suitable for travelling and foraging. With rainforest forming a possible ecological barrier, many migrants may cross the equator either at 15 degrees E, similar to the hobbies, or at 30-40 degrees E, east of the rainforest where large-scale migration is well documented. Much remains to be understood about the role of the rainforest for the evolution and future of the trans-equatorial Palaearctic-African bird migration systems.

Flight by night or day? Optimal daily timing of bird migration.

Many migratory bird species fly mainly during the night (nocturnal migrants), others during daytime (diurnal migrants) and still others during both night and day. Need to forage during the day, atmospheric structure, predator avoidance and orientation conditions have been proposed as explanations for the widespread occurrence of nocturnal migration. However, the general principles that determine the basic nocturnal-diurnal variation in flight habits are poorly known. In the present study optimal timing of migratory flights, giving the minimum total duration of the migratory journey, is evaluated in a schematic way in relation to ecological conditions for energy gain in foraging and for energy costs in flight. There exists a strong and fundamental advantage of flying by night because foraging time is maximized and energy deposition can take place on days immediately after and prior to the nocturnal flights. The increase in migration speed by nocturnal compared with diurnal migration will be largest for birds with low flight costs and high energy deposition rates. Diurnal migration will be optimal if it is associated with efficient energy gain immediately after a migratory flight because suitable stopover/foraging places have been located during the flight or if energy losses during flight are substantially reduced by thermal soaring and/or by fly-and-forage migration. A strategy of combined diurnal and nocturnal migration may be optimal when birds migrate across regions with relatively poor conditions for energy deposition (not only severe but also soft barriers). Predictions about variable timing of migratory flights depending on changing foraging and environmental conditions along the migration route may be tested for individual birds by analysing satellite tracking results with respect to daily travel routines in different regions. Documenting and understanding the adaptive variability in daily travel schedules among migrating animals constitute a fascinating challenge for future research.