Experience reduces route selection for conspecifics by the collectively migrating white stork.

Migration can be an energetically costly behavior with strong fitness consequences in terms of mortality and reproduction.1,2,3,4,5,6,7,8,9,10,11 Migrants should select migratory routes to minimize their costs, but both costs and benefits may change with experience.12,13,14 This raises the question of whether experience changes how individuals select their migratory routes. Here, we investigate the effect of age on route selection criteria in a collectively migrating soaring bird, the white stork (Ciconia ciconia). We perform step-selection analysis on a longitudinal dataset tracking 158 white storks over up to 9 years to quantify how they select their routes based on the social and atmospheric environments and to examine how this selection changes with age. We find clear ontogenetic shifts in route selection criteria. Juveniles choose routes that have good atmospheric conditions and high conspecific densities. Yet, as they gain experience, storks' selection on the availability of social information reduces-after their fifth migration, experienced birds also choose routes with low conspecific densities. Thus, our results suggest that as individuals age, they gradually replace information gleaned from other individuals with information gained from experience, allowing them to shift their migration timing and increasing the timescale at which they select their routes.

Learning shapes the development of migratory behavior.

How animals refine migratory behavior over their lifetime (i.e., the ontogeny of migration) is an enduring question with important implications for predicting the adaptive capacity of migrants in a changing world. Yet, our inability to monitor the movements of individuals from early life onward has limited our understanding of the ontogeny of migration. The exploration-refinement hypothesis posits that learning shapes the ontogeny of migration in long-lived species, resulting in greater exploratory behavior early in life followed by more rapid and direct movement during later life. We test the exploration-refinement hypothesis by examining how white storks (Ciconia ciconia) balance energy, time, and information as they develop and refine migratory behavior during the first years of life. Here, we show that young birds reduce energy expenditure during flight while also increasing information gain by exploring new places during migration. As the birds age and gain more experience, older individuals stop exploring new places and instead move more quickly and directly, resulting in greater energy expenditure during migratory flight. During spring migration, individuals innovated novel shortcuts during the transition from early life into adulthood, suggesting a reliance on spatial memory acquired through learning. These incremental refinements in migratory behavior provide support for the importance of individual learning within a lifetime in the ontogeny of long-distance migration.

The price of being late: short- and long-term consequences of a delayed migration timing.

Choosing the right migration timing is critical for migrants because conditions encountered en route influence movement costs, survival, and, in social migrants, the availability of social information. Depending on lifetime stages, individuals may migrate at different times due to diverging constraints, affecting the composition of migration groups. To examine the consequences of a delayed migration timing, we artificially delayed the migration of juvenile white storks (Ciconia ciconia) and thereby altered their physical and social environment. Using nearly continuous 1 Hz GPS trajectories, we examined their migration behaviour, ranging from sub-second level performance to global long-distance movement, in relation to two control groups. We found that delayed storks experienced suboptimal soaring conditions, but better wind support and thereby achieved higher flight speeds than control storks. Delayed storks had a lower mortality rate than the control storks and wintered closer to the breeding area. In fact, none of the delayed storks reached the traditional African wintering areas. Thus, our results show that juvenile storks can survive migrating at the 'wrong' time. However, this had long-term consequences on migration decisions. We suggest that, when timing their migration, storks balance not just energy and time, but also the availability of social information.

White stork movements reveal the ecological connectivity between landfills and different habitats.

BACKGROUND: Connections between habitats are key to a full understanding of anthropic impacts on ecosystems. Freshwater habitats are especially biodiverse, yet depend on exchange with terrestrial habitats. White storks (Ciconia ciconia) are widespread opportunists that often forage in landfills and then visit wetlands, among other habitats. It is well known that white storks ingest contaminants at landfills (such as plastics and antibiotic resistant bacteria), which can be then deposited in other habitats through their faeces and regurgitated pellets. METHODS: We characterized the role of white storks in habitat connectivity by analyzing GPS data from populations breeding in Germany and wintering from Spain to Morocco. We overlaid GPS tracks on a land-use surface to construct a spatially-explicit network in which nodes were sites, and links were direct flights. We then calculated centrality metrics, identified spatial modules, and quantified overall connections between habitat types. For regional networks in southern Spain and northern Morocco, we built Exponential Random Graph Models (ERGMs) to explain network topologies as a response to node habitat. RESULTS: For Spain and Morocco combined, we built a directed spatial network with 114 nodes and 370 valued links. Landfills were the habitat type most connected to others, as measured by direct flights. The relevance of landfills was confirmed in both ERGMs, with significant positive effects of this habitat as a source of flights. In the ERGM for southern Spain, we found significant positive effects of rice fields and salines (solar saltworks) as sinks for flights. By contrast, in the ERGM for northern Morocco, we found a significant positive effect of marshes as a sink for flights. CONCLUSIONS: These results illustrate how white storks connect landfills with terrestrial and aquatic habitats, some of which are managed for food production. We identified specific interconnected habitat patches across Spain and Morocco that could be used for further studies on biovectoring of pollutants, pathogens and other propagules.

New frontiers in bird migration research.

Bird migrations are impressive behavioral phenomena, representing complex spatiotemporal strategies to balance costs of living while maximizing fitness. The field of bird migration research has made great strides over the past decades, yet fundamental gaps remain. Technologies have sparked a transformation in the study of bird migration research by revealing remarkable insights into the underlying behavioral, cognitive, physiological and evolutionary mechanisms of these diverse journeys. Here, we aim to encourage broad discussions and promote future studies by highlighting research fields that are characterized by major knowledge gaps or conflicting evidence, namely the fields of navigation, social learning, individual development, energetics and conservation. We approach each topic by summarizing the current state of knowledge and provide a future outlook of ideas and state-of-the-art methods to further advance the field. Integrating knowledge across these disciplines will allow us to understand the adaptive abilities of different species and to develop effective conservation strategies in a rapidly changing world.

Viewing animal migration through a social lens.

Evidence of social learning is growing across the animal kingdom. Researchers have long hypothesized that social interactions play a key role in many animal migrations, but strong empirical support is scarce except in a few unique systems and species. In this review, we aim to catalyze advances in the study of social migrations by synthesizing research across disciplines and providing a framework for understanding when, how, and why social influences shape the decisions animals make during migration. Integrating research across the fields of social learning and migration ecology will advance our understanding of the complex behavioral phenomena of animal migration and help to inform conservation of animal migrations in a changing world.

Smell of green leaf volatiles attracts white storks to freshly cut meadows.

Finding food is perhaps the most important task for all animals. Birds often show up unexpectedly at novel food sources such as freshly tilled fields or mown meadows. Here we test whether wild European white storks primarily use visual, social, auditory or olfactory information to find freshly cut farm pastures where insects and rodents abound. Aerial observations of an entire local stork population documented that birds could not have become aware of a mown field through auditory, visual or social information. Only birds within a 75° downwind cone over 0.4-16.6 km approached any mown field. Placing freshly cut grass from elsewhere on selected unmown fields elicited similarly immediate stork approaches. Furthermore, uncut fields that were sprayed with a green leaf volatile organic compound mix ((Z)-3-hexenal, (Z)-3-hexenol, hexenyl acetate), the smell of freshly cut grass, immediately attracted storks. The use of long-distance olfactory information for finding food may be common in birds, contrary to current perception.

Longer days enable higher diurnal activity for migratory birds.

Seasonal geophysical cycles strongly influence the activity of life on Earth because they affect environmental conditions like temperature, precipitation and day length. An increase in daylight availability during summer is especially enhanced when animals migrate along a latitudinal gradient. Yet, the question of how day length (i.e. daylight availability) influences the activity patterns of long-distance, latitudinal migrants is still unclear. Here, we ask whether migration provides benefits to long-distance migrants by enabling them to increase their diurnal movement activities due to an increase in daylight availability. To answer this question, we tested whether four vastly different species of long-distance migratory birds-two arctic migrants and two mid-latitude migrants-can capitalise on day length changes by adjusting their daily activity. We quantified the relationship between daily activity (measured using accelerometer data) and day length, and estimated each species' daily activity patterns. In addition, we evaluated the role of day length as an ultimate driver of bird migration. All four species exhibited longer activity periods during days with more daylight hours, showing a strong positive relationship between total daily activity and day length. The slope of this relationship varied between the different species, with activity increasing 1.5-fold on average when migrating from wintering to breeding grounds. Underlying mechanisms of these relationships reveal two distinct patterns of daily activity. Flying foragers showed increasing activity patterns, that is, their daytime activities rose uniformly up to solar noon and decreased until dusk, thereby exhibiting a season-specific activity slope. In contrast, ground foragers showed a constant activity pattern, whereby they immediately increased their activity to a certain level and maintained this level throughout the day. Our study reveals that long days allow birds to prolong their activity and increase their total daily activity. These findings highlight that daylight availability could be an additional ultimate cause of bird migration and act as a selective agent for the evolution of migration.

Los ciclos geofísicos estacionales influyen fuertemente la actividad de la vida en la Tierra ya que afectan diversas condiciones ambientales como la temperatura, la precipitación y la duración del día. El aumento de la disponibilidad de luz solar durante el verano favorece especialmente a las especies que migran a lo largo de un gradiente latitudinal. Sin embargo, el efecto de la duración del día (es decir, la disponibilidad de luz solar) en los patrones de actividad de las especies que migran latitudinalmente largas distancias, aún no es claro. Aquí nos preguntamos si un aumento de la disponibilidad de luz solar representa un beneficio para los animales que migran largas distancias, al prolongar el periodo de actividad diurna. Para responder a esta pregunta, investigamos si cuatro especies diferentes de aves migratorias de larga distancia, dos migrantes árticos y dos migrantes de latitudes medias, pueden ajustar su actividad diaria y aprovechar los cambios en la duración del día. Cuantificamos la relación entre la actividad diaria (medida con datos de acelerómetro) y la duración del día, y estimamos los patrones de actividad de cada especie. Además, evaluamos el papel de la duración del día como mecanismo último subyacente a la migración de las aves. Las cuatro especies mostraron períodos de actividad más largos durante los días con más horas de luz, mostrando una fuerte relación positiva entre la actividad diaria total y la duración del día. Esta relación varió entre las especies evaluadas. La actividad aumentó en promedio 1.5 veces durante la migración desde las áreas de invernada a las áreas de reproducción. Los mecanismos subyacentes a estas relaciones revelan dos patrones de actividad diaria. Las especies que forrajean en vuelo mostraron un aumento en su patrón de actividad. En este caso, la actividad diurna aumentó uniformemente hasta el mediodía y disminuyó hasta el atardecer, mostrando una pendiente de actividad específica para la estación. De otro lado, las especies que forrajean en tierra mostraron un patrón de actividad constante. Según este patrón, la actividad diurna aumenta hasta un determinado nivel, a partir del cual se mantiene durante el resto del día. Nuestro estudio revela que el aumento en la longitud del día le permite a las aves prolongar su actividad e incrementar su actividad diaria total. Estos resultados señalan que la disponibilidad de luz diurna podría ser otro mecanismo último subyacente a la migración de las aves y puede actuar como un factor de selección en la evolución de la migración.

Overland and oversea migration of white storks through the water barriers of the straits of Gibraltar.

Soaring landbirds typically exploit atmospheric uplift as they fly overland, displaying a highly effective energy-saving locomotion. However, large water bodies lack thermal updrafts, potentially becoming ecological barriers that hamper migration. Here we assessed the effects of a sea surface on the migratory performance of GPS-tagged white storks (Ciconia ciconia) before, during and after they crossed the straits of Gibraltar. Oversea movements involved only flapping and gliding and were faster, traversed in straighter, descending trajectories and resulted in higher movement-related energy expenditure levels than overland, supporting the water barrier hypothesis. Overland movements at both sides of the sea straits resulted in tortuous routes and ascending trajectories with pre-crossing flights showing higher elevations and more tortuous routes than post-crossing, thus supporting the barrier negotiation hypothesis. Individual positions at both ends of the sea narrow were predicted by zonal winds and storks´ location at entry in the European hinterland, and birds did not show compensational movements overland in anticipation to subsequent wind displacements oversea. The length of the water narrow at departure shore, the elevation therein and the winds on route affected major components of sea crossing performance (such as distances and times overwater, minimum elevations, climb angles, speeds and energy expenditure), supporting the departure position and oversea winds hypotheses. In summary, our study provides a prime example at high temporal resolution of how birds adjust their behavior and physiology as they interact with the changing conditions of the travelling medium, reallocating resources and modifying their movement to overcome an ecological barrier.

Birds advancing lay dates with warming springs face greater risk of chick mortality.

In response to a warming planet with earlier springs, migratory animals are adjusting the timing of essential life stages. Although these adjustments may be essential for keeping pace with resource phenology, they may prove insufficient, as evidenced by population declines in many species. However, even when species can match the tempo of climate change, other consequences may emerge when exposed to novel conditions earlier in the year. Here, using three long-term datasets on bird reproduction, daily insect availability, and weather, we investigated the complex mechanisms affecting reproductive success in an aerial insectivore, the tree swallow (Tachycineta bicolor). By examining breeding records over nearly half a century, we discovered that tree swallows have continuously advanced their egg laying by ∼3 d per decade. However, earlier-hatching offspring are now exposed to inclement weather events twice as often as they were in the 1970s. Our long-term daily insect biomass dataset shows no long-term trends over 25 y but precipitous drops in flying insect numbers on days with low ambient temperatures. Insect availability has a considerable impact on chick survival: Even a single inclement weather event can reduce offspring survival by >50%. Our results highlight the multifaceted threats that climate change poses on migrating species. The decoupling between cold snap occurrence and generally warming spring temperatures can affect reproductive success and threaten long-term persistence of populations. Understanding the exact mechanisms that endanger aerial insectivores is especially timely because this guild is experiencing the steepest and most widespread declines across North America and Europe.

Synergistic Benefits of Group Search in Rats.

Locating unpredictable but essential resources is a task that all mobile animals have to perform in order to survive and reproduce. Research on search strategies has focused largely on independent individuals [1-3], but many organisms display collective behaviors, including during group search and foraging [4-6]. One classical experimental search task, informing studies of navigation, memory, and learning, is the location of a reward in a confined, complex maze setting [7, 8]. Rats (Rattus norvegicus) have been paradigmatic in psychological and biological studies [9, 10], but despite rats being highly social [11, 12], their group search behavior has not been investigated. Here, we explore the decision making of rats searching individually, or in groups, for a reward in a complex maze environment. Using automated video tracking, we find that rats exhibit-even when alone-a partially systematic search, leading to a continuous increase in their chance of finding the reward because of increased attraction to unexplored regions. When searching together, however, synergistic group advantages arise through integration of individual exploratory and social behavior. The superior search performances result from a strategy that represents a hierarchy of influential preferences in response to social and asocial cues. Furthermore, we present a computational model to compare the essential factors that influence how collective search operates and to validate that the collective search strategy increases the search efficiency of individuals in groups. This strategy can serve as direct inspiration for designing computational search algorithms and systems, such as autonomous robot groups, to explore areas inaccessible to humans. VIDEO ABSTRACT.

Daily energy expenditure in white storks is lower after fledging than in the nest.

Many juvenile birds turn into long-distance migrants within weeks of fledging. This transition involves upheavals in their energy management as major changes in growth and activity occur. Understanding such ontogenetic transitions in energy allocation has been difficult because collecting continuous data on energy costs in wild developing birds was previously largely impossible. Here, we continuously measured heart rate and fine-scale movements of 20 free-living juvenile white storks (Ciconia ciconia) using on-board bio-loggers to explore individual and environmental factors relating to daily mean heart rate. In addition, we explored which specific energy management strategy storks use during these crucial early life stages. We found that daily mean heart rate increased with overall movement activity, and increasing body temperature, but that it decreased with age. Further, we found that during the nestling period, when growth costs are high, activity costs are low, and post-fledging that activity costs are increased while maintenance costs are low, indicating a constraint on overall energy use in both phases. Our observations are consistent with the hypothesis that individuals invested more energy per unit time while still in the nest than after fledging despite the high costs of flight.

"Closer-to-home" strategy benefits juvenile survival in a long-distance migratory bird.

Human-induced changes in the climate and environment that occur at an unprecedented speed are challenging the existence of migratory species. Faced with these new challenges, species with diverse and flexible migratory behaviors may suffer less from population decline, as they may be better at responding to these changes by altering their migratory behavior. At the individual level, variations in migratory behavior may lead to differences in fitness and subsequently influence the population's demographic dynamics. Using lifetime GPS bio-logging data from 169 white storks (Ciconia ciconia), we explore whether the recently shortened migration distance of storks affects their survival during different stages of their juvenile life. We also explore how other variations in migratory decisions (i.e., time, destination), movement activity (measured using overall body dynamic acceleration), and early life conditions influence juvenile survival. We observed that their first autumn migration was the riskiest period for juvenile white storks. Individuals that migrated shorter distances and fledged earlier experienced lower mortality risks. In addition, higher movement activity and overwintering "closer-to-home" (with 84.21% of the tracked individuals stayed Europe or North Africa) were associated with higher survival. Our study shows how avian migrants can change life history decisions over only a few decades, and thus it helps us to understand and predict how migrants respond to the rapidly changing world.

Fly with the flock: immersive solutions for animal movement visualization and analytics.

Understanding the movement of animals is important for a wide range of scientific interests including migration, disease spread, collective movement behaviour and analysing motion in relation to dynamic changes of the environment such as wind and thermal lifts. Particularly, the three-dimensional (3D) spatial-temporal nature of bird movement data, which is widely available with high temporal and spatial resolution at large volumes, presents a natural option to explore the potential of immersive analytics (IA). We investigate the requirements and benefits of a wide range of immersive environments for explorative visualization and analytics of 3D movement data, in particular regarding design considerations for such 3D immersive environments, and present prototypes for IA solutions. Tailored to biologists studying bird movement data, the immersive solutions enable geo-locational time-series data to be investigated interactively, thus enabling experts to visually explore interesting angles of a flock and its behaviour in the context of the environment. The 3D virtual world presents the audience with engaging and interactive content, allowing users to 'fly with the flock', with the potential to ascertain an intuitive overview of often complex datasets, and to provide the opportunity thereby to formulate and at least qualitatively assess hypotheses. This work also contributes to ongoing research efforts to promote better understanding of bird migration and the associated environmental factors at the global scale, thereby providing a visual vehicle for driving public awareness of environmental issues and bird migration patterns.

Static landscape features predict uplift locations for soaring birds across Europe.

Soaring flight is a remarkable adaptation to reduce movement costs by taking advantage of atmospheric uplifts. The movement pattern of soaring birds is shaped by the spatial and temporal availability and intensity of uplifts, which result from an interaction of local weather conditions with the underlying landscape structure. We used soaring flight locations and vertical speeds of an obligate soaring species, the white stork (Ciconia ciconia), as proxies for uplift availability and intensity. We then tested if static landscape features such as topography and land cover, instead of the commonly used weather information, could predict and map the occurrence and intensity of uplifts across Europe. We found that storks encountering fewer uplifts along their routes, as determined by static landscape features, suffered higher energy expenditures, approximated by their overall body dynamic acceleration. This result validates the use of static features as uplift predictors and suggests the existence of a direct link between energy expenditure and static landscape structure, thus far largely unquantified for flying animals. Our uplift availability map represents a computationally efficient proxy of the distribution of movement costs for soaring birds across the world's landscapes. It thus provides a base to explore the effects of changes in the landscape structure on the energy expenditure of soaring birds, identify low-cost movement corridors and ultimately inform the planning of anthropogenic developments.

From local collective behavior to global migratory patterns in white storks.

Soaring migrant birds exploit columns of rising air (thermals) to cover large distances with minimal energy. Using social information while locating thermals may benefit such birds, but examining collective movements in wild migrants has been a major challenge for researchers. We investigated the group movements of a flock of 27 naturally migrating juvenile white storks by using high-resolution GPS and accelerometers. Analyzing individual and group movements on multiple scales revealed that a small number of leaders navigated to and explored thermals, whereas followers benefited from their movements. Despite this benefit, followers often left thermals earlier and at lower height, and consequently they had to flap considerably more. Followers also migrated less far annually than did leaders. We provide insights into the interactions between freely flying social migrants and the costs and benefits of collective movement in natural populations.

Collective animal navigation and migratory culture: from theoretical models to empirical evidence.

Animals often travel in groups, and their navigational decisions can be influenced by social interactions. Both theory and empirical observations suggest that such collective navigation can result in individuals improving their ability to find their way and could be one of the key benefits of sociality for these species. Here, we provide an overview of the potential mechanisms underlying collective navigation, review the known, and supposed, empirical evidence for such behaviour and highlight interesting directions for future research. We further explore how both social and collective learning during group navigation could lead to the accumulation of knowledge at the population level, resulting in the emergence of migratory culture.This article is part of the theme issue 'Collective movement ecology'.

Synchronization, coordination and collective sensing during thermalling flight of freely migrating white storks.

Exploring how flocks of soaring migrants manage to achieve and maintain coordination while exploiting thermal updrafts is important for understanding how collective movements can enhance the sensing of the surrounding environment. Here we examined the structural organization of a group of circling white storks (Ciconia ciconia) throughout their migratory journey from Germany to Spain. We analysed individual high-resolution GPS trajectories of storks during circling events, and evaluated each bird's flight behaviour in relation to its flock members. Within the flock, we identified subgroups that synchronize their movements and coordinate switches in their circling direction within thermals. These switches in direction can be initiated by any individual of the subgroup, irrespective of how advanced its relative vertical position is, and occur at specific horizontal locations within the thermal allowing the storks to remain within the thermal. Using the motion of all flock members, we were able to examine the dynamic variation of airflow within the thermals and to determine the specific environmental conditions surrounding the flock. With an increasing amount of high-resolution GPS tracking, we may soon be able to use these animals as distributed sensors providing us with a new means to obtain a detailed knowledge of our environment.This article is part of the theme issue 'Collective movement ecology'.

Wind estimation based on thermal soaring of birds.

The flight performance of birds is strongly affected by the dynamic state of the atmosphere at the birds' locations. Studies of flight and its impact on the movement ecology of birds must consider the wind to help us understand aerodynamics and bird flight strategies. Here, we introduce a systematic approach to evaluate wind speed and direction from the high-frequency GPS recordings from bird-borne tags during thermalling flight. Our method assumes that a fixed horizontal mean wind speed during a short (18 seconds, 19 GPS fixes) flight segment with a constant turn angle along a closed loop, characteristic of thermalling flight, will generate a fixed drift for each consequent location. We use a maximum-likelihood approach to estimate that drift and to determine the wind and airspeeds at the birds' flight locations. We also provide error estimates for these GPS-derived wind speed estimates. We validate our approach by comparing its wind estimates with the mid-resolution weather reanalysis data from ECMWF, and by examining independent wind estimates from pairs of birds in a large dataset of GPS-tagged migrating storks that were flying in close proximity. Our approach provides accurate and unbiased observations of wind speed and additional detailed information on vertical winds and uplift structure. These precise measurements are otherwise rare and hard to obtain and will broaden our understanding of atmospheric conditions, flight aerodynamics, and bird flight strategies. With an increasing number of GPS-tracked animals, we may soon be able to use birds to inform us about the atmosphere they are flying through and thus improve future ecological and environmental studies.

The challenges of the first migration: movement and behaviour of juvenile vs. adult white storks with insights regarding juvenile mortality.

Migration conveys an immense challenge, especially for juvenile birds coping with enduring and risky journeys shortly after fledging. Accordingly, juveniles exhibit considerably lower survival rates compared to adults, particularly during migration. Juvenile white storks (Ciconia ciconia), which are known to rely on adults during their first fall migration presumably for navigational purposes, also display much lower annual survival than adults. Using detailed GPS and body acceleration data, we examined the patterns and potential causes of age-related differences in fall migration properties of white storks by comparing first-year juveniles and adults. We compared juvenile and adult parameters of movement, behaviour and energy expenditure (estimated from overall dynamic body acceleration) and placed this in the context of the juveniles' lower survival rate. Juveniles used flapping flight vs. soaring flight 23% more than adults and were estimated to expend 14% more energy during flight. Juveniles did not compensate for their higher flight costs by increased refuelling or resting during migration. When juveniles and adults migrated together in the same flock, the juvenile flew mostly behind the adult and was left behind when they separated. Juveniles showed greater improvement in flight efficiency throughout migration compared to adults which appears crucial because juveniles exhibiting higher flight costs suffered increased mortality. Our findings demonstrate the conflict between the juveniles' inferior flight skills and their urge to keep up with mixed adult-juvenile flocks. We suggest that increased flight costs are an important proximate cause of juvenile mortality in white storks and likely in other soaring migrants and that natural selection is operating on juvenile variation in flight efficiency.