The importance of time of day for magnetic body alignment in songbirds.

Spontaneous magnetic alignment is the simplest known directional response to the geomagnetic field that animals perform. Magnetic alignment is not a goal directed response and its relevance in the context of orientation and navigation has received little attention. Migratory songbirds, long-standing model organisms for studying magnetosensation, have recently been reported to align their body with the geomagnetic field. To explore whether the magnetic alignment behaviour in songbirds is involved in the underlying mechanism for compass calibration, which have been suggested to occur near to sunset, we studied juvenile Eurasian reed warblers (Acrocephalus scirpaceus) captured at stopover during their first autumn migration. We kept one group of birds in local daylight conditions and an experimental group under a 2 h delayed sunset. We used an ad hoc machine learning algorithm to track the birds' body alignment over a 2-week period. Our results show that magnetic body alignment occurs prior to sunset, but shifts to a more northeast-southwest alignment afterwards. Our findings support the hypothesis that body alignment could be associated with how directional celestial and magnetic cues are integrated in the compass of migratory birds.

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.

Enhancing monitoring and transboundary collaboration for conserving migratory species under global change: The priority case of the red kite.

Calls for urgent action to conserve biodiversity under global change are increasing, and conservation of migratory species in this context poses special challenges. In the last two decades the Convention on the Conservation of Migratory Species of Wild Animals (CMS) has provided a framework for several subsidiary instruments including action plans for migratory bird species, but the effectiveness and transferability of these plans remain unclear. Such laws and policies have been credited with positive outcomes for the conservation of migratory species, but the lack of international coordination and on-ground implementation pose major challenges. While research on migratory populations has received growing attention, considerably less emphasis has been given to integrating ecological information throughout the annual cycle for examining strategies to conserve migratory species at multiple scales in the face of global change. We fill this gap through a case study examining the ecological status and conservation of a migratory raptor and facultative scavenger, the red kite (Milvus milvus), whose current breeding range is limited to Europe and is associated with agricultural landscapes and restricted to the temperate zone. Based on our review, conservation actions have been successful at recovering red kite populations within certain regions. Populations however remain depleted along the southern-most edge of the geographic range where many migratory red kites from northern strongholds overwinter. This led us to a forward-looking and integrated strategy that emphasizes international coordination involving researchers and conservation practitioners to enhance the science-policy-action interface. We identify and explore key issues for conserving the red kite under global change, including enhancing conservation actions within and outside protected areas, recovering depleted populations, accounting for climate change, and transboundary coordination in adaptive conservation and management actions. The integrated conservation strategy is sufficiently general such that it can be adapted to inform conservation of other highly mobile species subject to global change.

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.

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 importance of migratory connectivity for global ocean policy.

The distributions of migratory species in the ocean span local, national and international jurisdictions. Across these ecologically interconnected regions, migratory marine species interact with anthropogenic stressors throughout their lives. Migratory connectivity, the geographical linking of individuals and populations throughout their migratory cycles, influences how spatial and temporal dynamics of stressors affect migratory animals and scale up to influence population abundance, distribution and species persistence. Population declines of many migratory marine species have led to calls for connectivity knowledge, especially insights from animal tracking studies, to be more systematically and synthetically incorporated into decision-making. Inclusion of migratory connectivity in the design of conservation and management measures is critical to ensure they are appropriate for the level of risk associated with various degrees of connectivity. Three mechanisms exist to incorporate migratory connectivity into international marine policy which guides conservation implementation: site-selection criteria, network design criteria and policy recommendations. Here, we review the concept of migratory connectivity and its use in international policy, and describe the Migratory Connectivity in the Ocean system, a migratory connectivity evidence-base for the ocean. We propose that without such collaboration focused on migratory connectivity, efforts to effectively conserve these critical species across jurisdictions will have limited effect.

Magnetic body alignment in migratory songbirds: a computer vision approach.

Several invertebrate and vertebrate species have been shown to align their body relative to the geomagnetic field. Many hypotheses have been proposed to explain the adaptive significance of magnetic body alignment outside the context of navigation. However, experimental evidence to investigate alternative hypotheses is still limited. We present a new setup to track the preferential body alignment relative to the geomagnetic field in captive animals using computer vision. We tested our method on three species of migratory songbirds and provide evidence that they align their body with the geomagnetic field. We suggest that this behaviour is involved in the underlying mechanism for compass orientation and calibration, which may occur near to sunrise and sunset periods. Our method could easily be extended to other species and used to test a large set of hypotheses to explain the mechanisms behind the magnetic body alignment and the magnetic sense in general.

Magnetic storms disrupt nocturnal migratory activity in songbirds.

Birds possess a magnetic sense and rely on the Earth's magnetic field for orientation during migration. However, the geomagnetic field can be altered by solar activity at relative unpredictable intervals. How birds cope with the temporal geomagnetic variations caused by solar storms during migration is still unclear. We addressed this question by reproducing the effect of a solar storm on the geomagnetic field and monitoring the activity of three songbird species during autumn migration. We found that only the European robin reduced nocturnal migratory restlessness in response to simulated solar storms. At the same time, robins increased activity during early morning. We suggest that robins reduced activity at night when the perception of magnetic information would be strongly disrupted by temporal variations of the magnetic field, to extend their migration during daytime when several visual cues become available for orientation. The other two species, chiffchaff and dunnock, showing low or no nocturnal migratory activity, did not respond to the solar storm by changing activity.

Route simulations, compass mechanisms and long-distance migration flights in birds.

Bird migration has fascinated humans for centuries and routes crossing the globe are now starting to be revealed by advanced tracking technology. A central question is what compass mechanism, celestial or geomagnetic, is activated during these long flights. Different approaches based on the geometry of flight routes across the globe and route simulations based on predictions from compass mechanisms with or without including the effect of winds have been used to try to answer this question with varying results. A major focus has been use of orthodromic (great circle) and loxodromic (rhumbline) routes using celestial information, while geomagnetic information has been proposed for both a magnetic loxodromic route and a magnetoclinic route. Here, we review previous results and evaluate if one or several alternative compass mechanisms can explain migration routes in birds. We found that most cases could be explained by magnetoclinic routes (up to 73% of the cases), while the sun compas s could explain only 50%. Both magnetic and geographic loxodromes could explain <25% of the routes. The magnetoclinic route functioned across latitudes (1°S-74°N), while the sun compass only worked in the high Arctic (61-69°N). We discuss the results with respect to orientation challenges and availability of orientation cues.

Flying with the winds: differential migration strategies in relation to winds in moth and songbirds.

The gamma Y moth selects to migrate in stronger winds compared to songbirds, enabling fast transport to distant breeding sites, but a lower precision in orientation as the moth allows itself to be drifted by the winds. Photo: Ian Woiwod. In Focus: Chapman, J.R., Nilsson, C., Lim, K.S., Bäckman, J., Reynolds, D.R. & Alerstam, T. (2015) Adaptive strategies in nocturnally migrating insects and songbirds: contrasting responses to winds. Journal of Animal Ecology, In press Insects and songbirds regularly migrate long distances across continents and seas. During these nocturnal migrations, they are exposed to a fluid medium, the air, in which they transport themselves by flight at similar speeds as the winds may carry them. It is crucial for an animal to select the most favourable flight conditions relative to winds to minimize the distance flown on a given amount of fuel and to avoid hazardous situations. Chapman et al. (2015a) showed contrasting strategies in how moths initiate migration predominantly under tailwind conditions, allowing themselves to drift to a larger extent and gain ground speed as compared to nocturnal songbird migrants. The songbirds use more variable flight strategies in relation to winds, where they sometimes allow themselves to drift, and at other occasions compensate for wind drift. This study shows how insects and birds have differentially adapted to migration in relation to winds, which is strongly dependent on their own flight capability, with higher flexibility enabling fine-tuned responses to keep a time programme and reach a goal in songbirds compared to in insects.

No evidence for assortative mating within a willow warbler migratory divide.

INTRODUCTION: In contact zones, genetic mixing of two taxa can be restricted by prezygotic (e.g. assortative mating) or postzygotic (lower fitness of hybrid offspring) barriers, or a combination of the two. A hybrid zone between two willow warbler subspecies (Phylloscopus trochilus trochilus, P. t. acredula) with distinctive migratory strategies occurs in central Sweden. These subspecies exhibit differences in migratory direction and distance, resulting in geographically distinct wintering areas in Africa. The subspecies may have diverged from a common refuge after the last ice age, and neutral genetic markers are homogeneous across their range. By contrast, several phenotypic traits and genetic markers of two chromosomal regions previously identified show steep clines across the divide. The evolutionary forces that maintain this migratory divide remain unknown. Here we use plumage colour, morphology, genetic markers and feather stable nitrogen-isotopes (δ (15)N) to assess if assortative mating between migratory phenotypes could be acting as a possible mechanism for keeping the two forms genetically separate and maintaining the migratory divide. We colour-ringed a willow warbler breeding population in the central part of the hybrid zone and observed the breeding population to assess phenotypic and genotypic traits of social pairs. RESULTS: Our data suggest that wintering area and genetic ancestry had an effect on male arrival time to the breeding grounds which could contribute to assortment. However, evidence for assortative mating could not be detected based on a comparison of plumage colour, morphology and δ (15)N between social mates. CONCLUSION: This finding was strengthened by analyses of subspecies-specific genetic markers, which allowed us to identify the presence of a large proportion of potential hybrids and backcrosses at the study site. Our results supported the hypothesis that pre-mating isolation in willow warblers is weak, resulting in extensive hybridisation across the migratory divide.

Continental-scale patterns in diel flight timing of high-altitude migratory insects.

Many insects depend on high-altitude, migratory movements during part of their life cycle. The daily timing of these migratory movements is not random, e.g. many insect species show peak migratory flight activity at dawn, noon or dusk. These insects provide essential ecosystem services such as pollination but also contribute to crop damage. Quantifying the diel timing of their migratory flight and its geographical and seasonal variation, are hence key towards effective conservation and pest management. Vertical-looking radars provide continuous and automated measurements of insect migration, but large-scale application has not been possible because of limited availability of suitable devices. Here, we quantify patterns in diel flight periodicity of migratory insects between 50 and 500 m above ground level during March-October 2021 using a network of 17 vertical-looking radars across Europe. Independent of the overall daily migratory movements and location, peak migratory movements occur around noon, during crepuscular evening and occasionally the morning. Relative daily proportions of insect migration intensity and traffic during the diel phases of crepuscular-morning, day, crepuscular-evening and night remain largely equal throughout May-September and across Europe. These findings highlight, extend, and generalize previous regional-scale findings on diel migratory insect movement patterns to the whole of temperate Europe. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Animal migration in the Anthropocene: threats and mitigation options.

Animal migration has fascinated scientists and the public alike for centuries, yet migratory animals are facing diverse threats that could lead to their demise. The Anthropocene is characterised by the reality that humans are the dominant force on Earth, having manifold negative effects on biodiversity and ecosystem function. Considerable research focus has been given to assessing anthropogenic impacts on the numerical abundance of species/populations, whereas relatively less attention has been devoted to animal migration. However, there are clear linkages, for example, where human-driven impacts on migration behaviour can lead to population/species declines or even extinction. Here, we explore anthropogenic threats to migratory animals (in all domains - aquatic, terrestrial, and aerial) using International Union for the Conservation of Nature (IUCN) Threat Taxonomy classifications. We reveal the diverse threats (e.g. human development, disease, invasive species, climate change, exploitation, pollution) that impact migratory wildlife in varied ways spanning taxa, life stages and type of impact (e.g. from direct mortality to changes in behaviour, health, and physiology). Notably, these threats often interact in complex and unpredictable ways to the detriment of wildlife, further complicating management. Fortunately, we are beginning to identify strategies for conserving and managing migratory animals in the Anthropocene. We provide a set of strategies that, if embraced, have the potential to ensure that migratory animals, and the important ecological functions sustained by migration, persist.

Characterisation of a transcriptome to find sequence differences between two differentially migrating subspecies of the willow warbler Phylloscopus trochilus.

BACKGROUND: Animal migration requires adaptations in morphological, physiological and behavioural traits. Several of these traits have been shown to possess a strong heritable component in birds, but little is known about their genetic architecture. Here we used 454 sequencing of brain-derived transcriptomes from two differentially migrating subspecies of the willow warbler Phylloscopus trochilus to detect genes potentially underlying traits associated with migration. RESULTS: The transcriptome sequencing resulted in 1.8 million reads following filtering steps. Most of the reads (84%) were successfully mapped to the genome of the zebra finch Taeniopygia gutatta. The mapped reads were situated within at least 12,101 predicted zebra finch genes, with the greatest sequencing depth in exons. Reads that were mapped to intergenic regions were generally located close to predicted genes and possibly located in uncharacterized untranslated regions (UTRs). Out of 85,000 single nucleotide polymorphisms (SNPs) with a minimum sequencing depth of eight reads from each of two subspecies-specific pools, only 55 showed high differentiation, confirming previous studies showing that most of the genetic variation is shared between the subspecies. Validation of a subset of the most highly differentiated SNPs using Sanger sequencing demonstrated that several of them also were differentiated between an independent set of individuals of each subspecies. These SNPs were clustered in two chromosome regions that are likely to be influenced by divergent selection between the subspecies and that could potentially be associated with adaptations to their different migratory strategies. CONCLUSIONS: Our study represents the first large-scale sequencing analysis aiming at detecting genes underlying migratory phenotypes in birds and provides new candidates for genes potentially involved in migration.

A new approach to evaluate multimodal orientation behaviour of migratory passerine birds recorded in circular orientation cages.

Circular orientation cages have been used for several decades to record the migratory orientation of passerine migrants, and have been central to the investigation of the functional characteristics of the biological compasses used for orientation. The use of these cages offers unique possibilities to study the migratory behaviour of songbirds, but suffers from statistical limitations in evaluating the directions of the activity recorded in the cages. The migratory activity has been reported to vary, including complex multimodal orientation of migratory passerines tested in orientation cages irrespective of species studied. The currently applied circular statistical methods fail to describe orientation responses differing from unimodal and axial distributions. We propose for the first time a modelling procedure enabling the analysis of multimodal distributions at either an individual or a group level. In this paper we compare the results of conventional methods and the recommended modelling approach. Migratory routes may be more complex than a simple migratory direction, and multimodal behaviour in migratory species at the individual and population levels can be advantageous. Individuals may select the expected migratory direction, but may also return to safer sites en route, i.e. sites already known, which provide food and/or shelter in reverse directions. In individual birds, several directions may be expressed in the same test hour. At the species level, multimodal orientation may give an opportunity to expand the range or may refer to differential migration route preferences in different populations of birds. A conflicting experimental situation may also result in a different preferential orientation. In this paper we suggest a statistical solution to deal with these types of variations in orientation preference.

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.

Autumn fueling behavior in passerines in relation to migratory distance and daylength.

Songbirds have evolved diverse strategies to cope with seasonality, including long-, medium-, and short-distance migration. There is some evidence that birds with a longer migration distance deposit fuel faster. However, most studies focus on long-distance migrants. Comparisons between species with different migration distances are necessary to broaden our understanding of fueling capacity in migratory birds. We present maximum fuel deposition rates of five songbird species migrating along the southeast coast of Sweden in autumn with migration distances ranging from long (neotropical migrant) to short (partial/irruptive migrant) (Willow Warbler Phylloscopus trochilus, Lesser Whitethroat Curruca curruca, Common Chiffchaff P. collybita, European Robin Erithacus rubecula, and Blue Tit Cyanistes caeruleus). The birds were fed ad libitum in captivity and were exposed to either extended or natural daylength. All species ceased to increase in mass when they reached a certain fuel load, generally corresponding to migration distance, despite unlimited access to food and ample time for foraging. Blue Tits, Willow Warblers, and Lesser Whitethroats had the highest fuel deposition rates with extended daylength (19%, 20%, and 20%, respectively), and about 13% with natural daylength, which is comparable to the highest rates found in migratory songbirds in nature. European Robins and Common Chiffchaffs that winter in the temperate Mediterranean had the lowest fuel deposition rates (12% and 12% with extended daylength, respectively). Our results suggest that the long- and short-distance migrants in this study have developed an extreme capacity for rapid refueling for different reasons; speedy migration to distant wintering grounds or winter survival in Scandinavia. This study contributes to our current knowledge of maximum fuel deposition rates in different species and the limitations posed by daylength. We highlight the need for future studies of species with different migration strategies in order to draw broad conclusions about fueling strategies of migratory birds.

Migration direction in a songbird explained by two loci.

Migratory routes and remote wintering quarters in birds are often species and even population specific. It has been known for decades that songbirds mainly migrate solitarily, and that the migration direction is genetically controlled. Yet, the underlying genetic mechanisms remain unknown. To investigate the genetic basis of migration direction, we track genotyped willow warblers Phylloscopus trochilus from a migratory divide in Sweden, where South-West migrating, and South-East migrating subspecies form a hybrid swarm. We find evidence that migration direction follows a dominant inheritance pattern with epistatic interaction between two loci explaining 74% of variation. Consequently, most hybrids migrate similarly to one of the parental subspecies, and therefore do not suffer from the cost of following an inferior, intermediate route. This has significant implications for understanding the selection processes that maintain narrow migratory divides.

Spatial monitoring of flying insects over a Swedish lake using a continuous-wave lidar system.

We have used a continuous-wave bi-static lidar system based on the Scheimpflug principle in measurements on flying insects above, and in the vicinity of, a small lake located in a forested area in Southern Sweden. The system, which operates on triangulation principles, has a high spatial resolution at close distance, followed by a subsequent decline in resolution further from the sensor, related to the compact system design with a separation of transmitter and receiver by only 0.81 m. Our study showed a strong increase in insect abundance especially at dusk, but also at dawn. Insect numbers decreased over water compared to over land, and larger insects were over-represented over water. Further, the average size of the insects increased at night compared to day time.

Diurnal migration patterns in willow warblers differ between the western and eastern flyways.

It is a long-standing view that the main mechanism maintaining narrow migratory divides in passerines is the selection against intermediate and suboptimal migratory direction, but empirical proof of this is still lacking. We present novel results from a willow warbler migratory divide in central Sweden from where birds take the typical SW and SE as well as intermediate routes to winter quarters in Africa. We hypothesized that individuals that take the intermediate route are forced to migrate in daytime more often when crossing wide ecological barriers than birds that follow the typical western or eastern flyways. Analyses of geolocator tracks of willow warblers breeding across the entire Sweden, including the migratory divide, provided no support for our hypothesis. Instead, birds that migrated along the western flyway were the most likely to undertake full day flights. The probability of migrating for a full day when crossing major barriers declined linearly from west to east. We speculate that this difference is possibly caused by more challenging conditions in the western part of the Sahara Desert, such as the lack of suitable day-time roost sites. However, it may equally likely be that willow warblers benefit from migrating in daytime if favorable tailwinds offer assistance.