Seasonal patterns and processes of migration in a long-distance migratory bird: energy or time minimization?

Optimal migration theory prescribes adaptive strategies of energy, time or mortality minimization. To test alternative hypotheses of energy- and time-minimization migration we used multisensory data loggers that record time-resolved flight activity and light for positioning by geolocation in a long-distance migratory shorebird, the little ringed plover, Charadrius dubius. We could reject the hypothesis of energy minimization based on a relationship between stopover duration and subsequent flight time as predicted for a time minimizer. We found seasonally diverging slopes between stopover and flight durations in relation to the progress (time) of migration, which follows a time-minimizing policy if resource gradients along the migration route increase in autumn and decrease in spring. Total flight duration did not differ significantly between autumn and spring migration, although spring migration was 6% shorter. Overall duration of autumn migration was longer than that in spring, mainly owing to a mid-migration stop in most birds, when they likely initiated moult. Overall migration speed was significantly different between autumn and spring. Migratory flights often occurred as runs of two to seven nocturnal flights on adjacent days, which may be countering a time-minimization strategy. Other factors may influence a preference for nocturnal migration, such as avoiding flight in turbulent conditions, heat stress and diurnal predators.

Extremely low daylight sea-crossing flights of a nocturnal migrant.

Understanding the trade-off between energy expenditure of carrying large fuel loads and the risk of fuel depletion is imperative to understand the evolution of flight strategies during long-distance animal migration. Global flyways regularly involve sea crossings that may impose flight prolongations on migrating land-birds and thereby reduce their energy reserves and survival prospects. We studied route choice, flight behavior, and fuel store dynamics of nocturnally migrating European nightjars (Caprimulgus europaeus) crossing water barriers. We show that barrier size and groundspeed of the birds influence the prospects of extended daylight flights, but also that waters possible to cross within a night regularly result in diurnal flight events. The nightjars systematically responded to daylight flights by descending to about a wingspan's altitude above the sea surface while switching to an energy-efficient flap-glide flight style. By operating within the surface-air boundary layer, the nightjars could fly in ground effect, exploit local updraft and pressure variations, and thereby substantially reduce flight costs as indicated by their increased proportion of cheap glides. We propose that surface-skimming flights, as illustrated in the nightjar, provide an energy-efficient transport mode and that this novel finding asks for a reconsideration of our understanding of flight strategies when land-birds migrate across seas.

Consequences of migratory distance, habitat distribution and season on the migratory process in a short distance migratory shorebird population.

BACKGROUND: The migratory process in birds consists of alternating periods of flight and fueling. Individuals of some populations make few flights and long stopovers, while others make multiple flights between short stopovers. Shorebirds are known for executing marathon flights (jumps), but most populations studied are long distance migrants, often crossing major barriers and thus forced to make long-haul flights. The sub-division of migration in short/medium distance migratory populations, where the total migration distance is shorter than documented non-stop flight capacity and where routes offer more homogenous stopover landscape, is little explored. METHODS: Here we combine data based on conventional light level geolocators and miniaturized multi sensor loggers, comprising acceleration and light sensors, to characterize the migratory routes and migration process for a short/medium distance (~ 1300 to 3000 km) migratory population of common ringed plover (Charadrius hiaticula) breeding in southern Sweden. We were specifically interested in the variation in number and duration (total and individual) of flights/stopovers between seasons and in relation to migration distance. RESULTS: Most stopovers were located along the European Atlantic coast. On average 4.5 flights were made during autumn migration irrespective of migration distance, but in spring the number of flights increased with distance. The equal number of flights in autumn was explained by that most individuals migrating farther performed one longer flight (all but one lasting > 20 h), likely including crossing of the Bay of Biscay. Median duration of single flights was 8.7 h in autumn and 5.5 h in spring, and median stopover duration was ~ 1 day in both seasons. There was a positive relationship between total flight duration and migration distance, but total flight duration was 36% lower in spring compared to autumn. CONCLUSIONS: Our results suggest that when suitable stopovers are abundant common ringed plovers prefer making shorter flights even if longer flights are within the capacity of the species. This behaviour is predicted under both time and energy minimizing strategies, although the variable flight distances suggest a policy of time selected migration. Even if populations using several stopovers seem to be more resilient for environmental change along the route, these results are informative for conservation efforts and for predicting responses to future environmental change.

Conversion efficiency of flight power is low, but increases with flight speed in the migratory bat Pipistrellus nathusii.

The efficiency with which flying animals convert metabolic power to mechanical power dictates an individual's flight behaviour and energy requirements. Despite the significance of this parameter, we lack empirical data on conversion efficiency for most species as in vivo measurements are notoriously difficult to obtain. Furthermore, conversion efficiency is often assumed to be constant across flight speeds, even though the components driving flight power are speed-dependent. We show, through direct measurements of metabolic and aerodynamic power, that conversion efficiency in the migratory bat (Pipistrellus nathusii) increases from 7.0 to 10.4% with flight speed. Our findings suggest that peak conversion efficiency in this species occurs near maximum range speed, where the cost of transport is minimized. A meta-analysis of 16 bird and 8 bat species revealed a positive scaling relationship between estimated conversion efficiency and body mass, with no discernible differences between bats and birds. This has profound consequences for modelling flight behaviour as estimates assuming 23% efficiency underestimate metabolic costs for P. nathusii by almost 50% on average (36-62%). Our findings suggest that conversion efficiency may vary around an ecologically relevant optimum speed and provide a crucial baseline for investigating whether this drives variation in conversion efficiency between species.

Effects of wing damage and moult gaps on vertebrate flight performance.

Vertebrates capable of powered flight rely on wings, muscles that drive their flapping and sensory inputs to the brain allowing for control of the motor output. In birds, the wings are formed of arrangements of adjacent flight feathers (remiges), whereas the wings of bats consist of double-layered skin membrane stretched out between the forelimb skeleton, body and legs. Bird feathers become worn from use and brittle from UV exposure, which leads to loss of function; to compensate, they are renewed (moulted) at regular intervals. Bird feathers and the wings of bats can be damaged by accident. Wing damage and loss of wing surface due to moult almost invariably cause reduced flight performance in measures such as take-off angle and speed. During moult in birds, this is partially counteracted by concurrent mass loss and enlarged flight muscles. Bats have sensory hairs covering their wing surface that provide feedback information about flow; thus, wing damage affects flight speed and turning ability. Bats also have thin, thread-like muscles, distributed within the wing membrane and, if these are damaged, the control of wing camber is lost. Here, I review the effects of wing damage and moult on flight performance in birds, and the consequences of wing damage in bats. I also discuss studies of life-history trade-offs that make use of experimental trimming of flight feathers as a way to handicap parent birds feeding their young.

The role of wingbeat frequency and amplitude in flight power.

Body-mounted accelerometers provide a new prospect for estimating power use in flying birds, as the signal varies with the two major kinematic determinants of aerodynamic power: wingbeat frequency and amplitude. Yet wingbeat frequency is sometimes used as a proxy for power output in isolation. There is, therefore, a need to understand which kinematic parameter birds vary and whether this is predicted by flight mode (e.g. accelerating, ascending/descending flight), speed or morphology. We investigate this using high-frequency acceleration data from (i) 14 species flying in the wild, (ii) two species flying in controlled conditions in a wind tunnel and (iii) a review of experimental and field studies. While wingbeat frequency and amplitude were positively correlated, R2 values were generally low, supporting the idea that parameters can vary independently. Indeed, birds were more likely to modulate wingbeat amplitude for more energy-demanding flight modes, including climbing and take-off. Nonetheless, the striking variability, even within species and flight types, highlights the complexity of describing the kinematic relationships, which appear sensitive to both the biological and physical context. Notwithstanding this, acceleration metrics that incorporate both kinematic parameters should be more robust proxies for power than wingbeat frequency alone.

Moonlight drives nocturnal vertical flight dynamics in black swifts.

Many animals have evolved a migratory lifestyle as an adaptation to seasonality,1,2 ranging from insects3 to fish,4 terrestrial and marine mammals,5-7 and birds.8 Old World swifts have evolved an extraordinary aerial non-breeding life phase lasting for 6-10 months.9-11 Swifts exploit the aerosphere in search of insects to meet the high energy demands of flight.12 During this period they roost and likely also sleep in the open airspace. Nocturnal insectivores with restricted foraging time may use moonlight to increase energy intake.13 Using multisensor data loggers that record light for geolocation, acceleration for flight activity, and pressure for flight altitude, we investigated if Northern black swifts, Cypseloides niger borealis, breeding in North America, also lead an aerial lifestyle similar to their Old World relatives. Individual flight activity showed they are airborne >99% of the time, with only occasional landings during their 8-month non-breeding period. Unexpectedly, during periods around the full moon, they conducted regular nocturnal ascents to altitudes up to >4,000 m (mean 2,000 m). A lunar eclipse triggered a synchronized descent, showing a direct effect of moonlight on flight altitude. This previously unknown behavior of nocturnal ascents during moonlight nights could be either a response to predator avoidance or that moonlight provides a foraging opportunity. Observed elevated nocturnal flight activity during periods of moonlight compared to dark nights suggests swifts were hawking for prey. Our finding of this novel behavior provides new perspectives on nocturnal flight behavior during periods surrounding the full moon.

Flight altitude dynamics of migrating European nightjars across regions and seasons.

Avian migrants may fly at a range of altitudes, but usually concentrate near strata where a combination of flight conditions is favourable. The aerial environment can have a large impact on the performance of the migrant and is usually highly dynamic, making it beneficial for a bird to regularly check the flight conditions at alternative altitudes. We recorded the migrations between northern Europe and sub-Saharan Africa of European nightjars Caprimulgus europaeus to explore their altitudinal space use during spring and autumn flights and to test whether their climbs and descents were performed according to predictions from flight mechanical theory. Spring migration across all regions was associated with more exploratory vertical flights involving major climbs, a higher degree of vertical displacement within flights, and less time spent in level flight, although flight altitude per se was only higher during the Sahara crossing. The nightjars commonly operated at ascent rates below the theoretical maximum, and periods of descent were commonly undertaken by active flight, and rarely by gliding flight, which has been assumed to be a cheaper locomotion mode during descents. The surprisingly frequent shifts in flight altitude further suggest that nightjars can perform vertical displacements at a relatively low cost, which is expected if the birds can allocate potential energy gained during climbs to thrust forward movement during descents. The results should inspire future studies on the potential costs associated with frequent altitude changes and their trade-offs against anticipated flight condition improvements for aerial migrants.

Hovering flight in hummingbird hawkmoths: kinematics, wake dynamics and aerodynamic power.

Hovering insects are divided into two categories: 'normal' hoverers that move the wing symmetrically in a horizontal stroke plane, and those with an inclined stroke plane. Normal hoverers have been suggested to support their weight during both downstroke and upstroke, shedding vortex rings each half-stroke. Insects with an inclined stroke plane should, according to theory, produce flight forces only during downstroke, and only generate one set of vortices. The type of hovering is thus linked to the power required to hover. Previous efforts to characterize the wake of hovering insects have used low-resolution experimental techniques or simulated the flow using computational fluid dynamics, and so it remains to be determined whether insect wakes can be represented by any of the suggested models. Here, we used tomographic particle image velocimetry, with a horizontal measurement volume placed below the animals, to show that the wake shed by hovering hawkmoths is best described as a series of bilateral, stacked vortex 'rings'. While the upstroke is aerodynamically active, despite an inclined stroke plane, it produces weaker vortices than the downstroke. In addition, compared with the near wake, the far wake lacks structure and is less concentrated. Both near and far wakes are clearly affected by vortex interactions, suggesting caution is required when interpreting wake topologies. We also estimated induced power (Pind) from downwash velocities in the wake. Standard models predicted a Pind more than double that from our wake measurements. Our results thus question some model assumptions and we propose a reevaluation of the model parameters.

Fine-scale changes in speed and altitude suggest protean movements in homing pigeon flights.

The power curve provides a basis for predicting adjustments that animals make in flight speed, for example in relation to wind, distance, habitat foraging quality and objective. However, relatively few studies have examined how animals respond to the landscape below them, which could affect speed and power allocation through modifications in climb rate and perceived predation risk. We equipped homing pigeons (Columba livia) with high-frequency loggers to examine how flight speed, and hence effort, varies in relation to topography and land cover. Pigeons showed mixed evidence for an energy-saving strategy, as they minimized climb rates by starting their ascent ahead of hills, but selected rapid speeds in their ascents. Birds did not modify their speed substantially in relation to land cover, but used higher speeds during descending flight, highlighting the importance of considering the rate of change in altitude before estimating power use from speed. Finally, we document an unexpected variability in speed and altitude over fine scales; a source of substantial energetic inefficiency. We suggest this may be a form of protean behaviour adopted to reduce predation risk when flocking is not an option, and that such a strategy could be widespread.

Evolution of chain migration in an aerial insectivorous bird, the common swift Apus apus.

Spectacular long-distance migration has evolved repeatedly in animals enabling exploration of resources separated in time and space. In birds, these patterns are largely driven by seasonality, cost of migration, and asymmetries in competition leading most often to leapfrog migration, where northern breeding populations winter furthest to the south. Here, we show that the highly aerial common swift Apus apus, spending the nonbreeding period on the wing, instead exhibits a rarely found chain migration pattern, where the most southern breeding populations in Europe migrate to wintering areas furthest to the south in Africa, whereas the northern populations winter to the north. The swifts concentrated in three major areas in sub-Saharan Africa during the nonbreeding period, with substantial overlap of nearby breeding populations. We found that the southern breeding swifts were larger, raised more young, and arrived to the wintering areas with higher seasonal variation in greenness (Normalized Difference Vegetation Index) earlier than the northern breeding swifts. This unusual chain migration pattern in common swifts is largely driven by differential annual timing and we suggest it evolves by prior occupancy and dominance by size in the breeding quarters and by prior occupancy combined with diffuse competition in the winter.

Measuring power input, power output and energy conversion efficiency in un-instrumented flying birds.

Cost of flight at various speeds is a crucial determinant of flight behaviour in birds. Aerodynamic models, predicting that mechanical power (Pmech) varies with flight speed in a U-shaped manner, have been used together with an energy conversion factor (efficiency) to estimate metabolic power (Pmet). Despite few empirical studies, efficiency has been assumed constant across flight speeds at 23%. Ideally, efficiency should be estimated from measurements of both Pmech and Pmet in un-instrumented flight. Until recently, progress has been hampered by methodological constraints. The main aim of this study was to evaluate recently developed techniques and estimate flight efficiency across flight speeds. We used the 13C-labelled sodium bicarbonate method (NaBi) and particle image velocimetry (PIV) to measure Pmet and Pmech in blackcaps flying in a wind tunnel. We also cross-validated measurements made by NaBi with quantitative magnetic resonance (QMR) body composition analysis in yellow-rumped warblers. We found that Pmet estimated by NaBi was ∼12% lower than corresponding values estimated by QMR. Pmet varied in a U-shaped manner across flight speeds in blackcaps, but the pattern was not statistically significant. Pmech could only be reliably measured for two intermediate speeds and estimated efficiency ranged between 14% and 22% (combining the two speeds for raw and weight/lift-specific power, with and without correction for the ∼12% difference between NaBi and QMR), which were close to the currently used default value. We conclude that NaBi and PIV are viable techniques, allowing researchers to address some of the outstanding questions regarding bird flight energetics.

Lunar synchronization of daily activity patterns in a crepuscular avian insectivore.

Biological rhythms of nearly all animals on earth are synchronized with natural light and are aligned to day-and-night transitions. Here, we test the hypothesis that the lunar cycle affects the nocturnal flight activity of European Nightjars (Caprimulgus europaeus). We describe daily activity patterns of individuals from three different countries across a wide geographic area, during two discrete periods in the annual cycle. Although the sample size for two of our study sites is small, the results are clear in that on average individual flight activity was strongly correlated with both local variation in day length and with the lunar cycle. We highlight the species' sensitivity to changes in ambient light and its flexibility to respond to such changes in different parts of the world.

The migration pattern of a monogamous shorebird challenges existing hypotheses explaining the evolution of differential migration.

Differential migration by sex, where one sex migrates further than the other, occurs in many bird species. How this pattern evolves is however little understood. The first aim of this study was to investigate the extent of differential migration in the common ringed plover Charadrius hiaticula, breeding in southeast Sweden, and test three main hypotheses (the social dominance, body size and arrival time hypothesis) regarding the evolution of differential migration. Geolocators were used to derive spatiotemporal data and morphometrics were collected from the studied population. Males migrated 800 km farther compared to females, were marginally larger and there was no statistical difference in spring arrival between the sexes. In contrast to other studies none of the previously proposed hypotheses could account for the observed pattern. An additional finding was that both sexes arrive up to 1.5 months before egg laying, but males initiate territorial behavior upon arrival. Based on these observations we suggest that males have a higher energetic demand, and challenges to meet those, early in the breeding season. Therefore we hypothesize that males arrive to the breeding site with residual fuel reserves accumulated at the wintering site to cover at least parts of these demands. Based on this hypothesis we present a simple model to explain the longer migration by males. The model is contingent on a trade-off between site specific fueling rates (which we assume to increase with decreasing latitude), cost of the extra migration distance and predation risk during fueling. This framework may be applicable to other cases of differential migration, especially in temperate breeding species which exhibit long pre-egg laying periods.

Wind-associated detours promote seasonal migratory connectivity in a flapping flying long-distance avian migrant.

It is essential to gain knowledge about the causes and extent of migratory connectivity between stationary periods of migrants to further the understanding of processes affecting populations, and to allow efficient implementation of conservation efforts throughout the annual cycle. Avian migrants likely use optimal routes with respect to mode of locomotion, orientation and migration strategy, influenced by external factors such as wind and topography. In self-powered flapping flying birds, any increases in fuel loads are associated with added flight costs. Energy-minimizing migrants are therefore predicted to trade-off extended detours against reduced travel across ecological barriers with no or limited foraging opportunities. Here, we quantify the extent of detours taken by different populations of European nightjars Caprimulgus europaeus, to test our predictions that they used routes beneficial according to energetic principles and evaluate the effect of route shape on seasonal migratory connectivity. We combined data on birds tracked from breeding sites along a longitudinal gradient from England to Sweden. We analysed the migratory connectivity between breeding and main non-breeding sites, and en route stopover sites just south of the Sahara desert. We quantified each track's route extension relative to the direct route between breeding and wintering sites, respectively, and contrasted it to the potential detour derived from the barrier reduction along the track while accounting for potential wind effects. Nightjars extended their tracks from the direct route between breeding and main non-breeding sites as they crossed the Mediterranean Sea-Sahara desert, the major ecological barrier in the Palaearctic-African migration system. These clockwise detours were small for birds from eastern sites but increased from east to west breeding longitude. Routes of the tracked birds were associated with partial reduction in the barrier crossing resulting in a trade-off between route extension and barrier reduction, as expected in an energy-minimizing migrant. This study demonstrates how the costs of barrier crossings in prevailing winds can disrupt migratory routes towards slightly different goals, and thereby promote migratory connectivity. This is an important link between individual migration strategies in association with an ecological barrier, and both spatially and demographic population patterns.

The lunar cycle drives migration of a nocturnal bird.

Every year, billions of seasonal migrants connect continents by transporting nutrients, energy, and pathogens between distant communities and ecosystems. For animals that power their movements by endogenous energy stores, the daily energy intake rates strongly influence the speed of migration. If access to food resources varies cyclically over the season, migrants sensitive to changes in daily energy intake rates may adjust timing of migration accordingly. As an effect, individuals adjusting to a common temporal cycle are expected to approach synchrony in foraging and movement. A large-scale periodic pattern, such as the dark-light cycle of the moon, could thus synchronize migrations across animal populations. However, such cyclic effects on the temporal regulation of migration has not been considered. Here, we show the temporal influence of the lunar cycle on the movement activity and migration tactics in a visual hunting nocturnal insectivore and long-distance migrant, the European nightjar, Caprimulgus europeaus. We found that the daily foraging activity more than doubled during moonlit nights, likely driven by an increase in light-dependent fuelling opportunities. This resulted in a clear cyclicity also in the intensity of migratory movements, with occasionally up to 100% of the birds migrating simultaneously following periods of full moon. We conclude that cyclic influences on migrants can act as an important regulator of the progression of individuals and synchronize pulses of migratory populations, with possible downstream effects on associated communities and ecosystems.

Optic flow cues help explain altitude control over sea in freely flying gulls.

For studies of how birds control their altitude, seabirds are of particular interest because they forage offshore where the visual environment can be simply modelled by a flat world textured by waves then generating only ventral visual cues. This study suggests that optic flow, i.e. the rate at which the sea moves across the eye's retina, can explain gulls' altitude control over seas. In particular, a new flight model that includes both energy and optical invariants helps explain the gulls' trajectories during offshore takeoff and cruising flight. A linear mixed model applied to 352 flights from 16 individual lesser black backed gulls (Larus fuscus) revealed a statistically significant optic flow set-point of ca 25° s-1. Thereafter, an optic flow-based flight model was applied to 18 offshore takeoff flights from nine individual gulls. By introducing an upper limit in climb rate on the elevation dynamics, coupled with an optic flow set-point, the predicted altitude gives an optimized fit factor value of 63% on average (30-83% in range) with respect to the GPS data. We conclude that the optic flow regulation principle helps gulls to adjust their altitude over sea without having to directly measure their current altitude.

An Implantable, Low-Power Instrumentation for the Long Term Monitoring of the Sleep of Animals under Natural Conditions.

Sleep is a universal and complex state and it is widely agreed that this state is present in every animal species. However, the evolutionary origins of sleep remain ignored or misunderstood, which has led researchers to study, in various species, this common behaviour of all living organisms. Sleep is commonly studied at various levels under laboratory conditions, using tethered devices which record electroencephalographic or electromyographic readings. These artificial settings tend to induce stress, reduce animal freedom and prevent the use of sleeping shelters. In this paper, we present a novel, implantable instrumentation for a complete characterization of sleep under natural conditions suitable for a wide range of animal species, even for animals as small as pigeons or mice. Several configurations of this system are possible to enable the measurement of up to 16 electrophysiology channels, 3 temperature channels as well as 3-axes accelerometry. With an embedded flash memory card for the storage of data collected, the system can be used as a datalogger for the recording of signals in the field.

The Ornithodolite as a tool to quantify animal space use and habitat selection: a case study with birds diving in tidal waters.

Animal-attached technologies can be powerful means to quantify space use and behavior; however, there are also ethical implications associated with capturing and instrumenting animals. Furthermore, tagging approaches are not necessarily well-suited for examining the movements of multiple individuals within specific, local areas of interest. Here, we assess a method of quantifying animal space use based on a modified theodolite with an inbuilt laser rangefinder. Using a database of >4200 tracks of migrating birds, we show that detection distance increases with bird body mass (range 5 g to >10 kg). The maximum distance recorded to a bird was 5500 m and measurement error was ≤5 m for targets within this distance range: a level comparable to methods such as GPS tagging. We go on to present a case study where this method was used to assess habitat selection in seabirds operating in dynamic coastal waters close to a tidal turbine. Combining positional data with outputs from a hydrographic model revealed that great cormorants (Phalacrocorax carbo) appeared to be highly selective of current characteristics in space and time, exploiting areas where mean current speeds were <0.8 m·s-1 and diving at times when turbulent energy levels were low. These birds also oriented into tidal currents during dives. Taken together, this suggests that collision risks are low for cormorants at this site, as the 2 conditions avoided by cormorants (high mean current speeds and turbulence levels) are associated with operational tidal turbines. Overall, we suggest that this modified theodolite system is well-suited to the quantification of movement in small areas associated with particular development strategies, including sustainable energy devices.