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Many species travel in highly organized groups. The most quoted function of these configurations is to reduce energy expenditure and enhance locomotor performance of individuals in the assemblage. The distinctive V formation of bird flocks has long intrigued researchers and continues to attract both scientific and popular attention. The well-held belief is that such aggregations give an energetic benefit for those birds that are flying behind and to one side of another bird through using the regions of upwash generated by the wings of the preceding bird, although a definitive account of the aerodynamic implications of these formations has remained elusive. Here we show that individuals of northern bald ibises (Geronticus eremita) flying in a V flock position themselves in aerodynamically optimum positions, in that they agree with theoretical aerodynamic predictions. Furthermore, we demonstrate that birds show wingtip path coherence when flying in V positions, flapping spatially in phase and thus enabling upwash capture to be maximized throughout the entire flap cycle. In contrast, when birds fly immediately behind another bird—in a streamwise position—there is no wingtip path coherence; the wing-beats are in spatial anti-phase. This could potentially reduce the adverse effects of downwash for the following bird. These aerodynamic accomplishments were previously not thought possible for birds because of the complex flight dynamics and sensory feedback that would be required to perform such a feat. We conclude that the intricate mechanisms involved in V formation flight indicate awareness of the spatial wake structures of nearby flock-mates, and remarkable ability either to sense or predict it. We suggest that birds in V formation have phasing strategies to cope with the dynamic wakes produced by flapping wings.
We trace the history of the endangered Northern Bald Ibis through different epochs to the present. A particular focus is placed on its life in and disappearance from ancient Egypt, where the bird attained great cultural and religious significance, and on the modern endeavour to re-wild the species. Due to the characteristic appearance, behaviour and habitat of the species as well as its need for open foraging areas, a close mutualistic relationship between humans and the birds was formed in ancient Egypt, as in other cultures. A clear benefit for the Northern Bald Ibis was the availability of feeding habitats, which were cleared by humans for farming or grazing. The benefit to people was rather cultural because the bird attracted religious veneration or symbolic meanings from ancient Egypt to medieval Europe. The proximity to humans, however, carried a high risk as well. We discuss various types of impact (including human impacts as well as climate change) as triggers for the extinction of the species. The evidence for a triple disappearance of the Northern Bald Ibis (around 2000 BCE, around 1600 CE and in modern time) represents a unique basis for studying both the bird’s habitat preferences and its vulnerability. This is because different, mainly anthropogenic, causes stood behind these three historical disappearances, although the disappearances in all three epochs occurred during a period of climate change.
The impact of biologging devices on the aerodynamics or hydrodynamics of animals is still poorly understood. This stands in marked contrast to the ever more extensive use of such technologies in wild-living animals. Recently, increasing concerns have been raised about the impairing effects of these devices on the animals concerned. In the early days of biotelemetry, attention was focused solely on reducing weight, but now aerodynamic effects are also increasingly being considered. To investigate these effects, we trained Northern Bald Ibises to fly in a wind tunnel in which we measured heart rate and dynamic body acceleration (VeDBA) as proxies for energy expenditure in relation to different logger shapes and wind flow directions.
Our results show that detrimental effects can be reduced with relatively little effort, in particular through a strictly aerodynamic design of the housing and increased consideration of aerodynamics when attaching the device to the body. In birds, the attachment of biologging devices via leg loops to the lower back is clearly preferable to the common attachment via wing loops on the upper back, even if this affects the efficiency of the solar panels. Nevertheless, the importance of drag reduction may vary between systems, as the benefits of having a biologging devices close to the center of gravity may outweigh the increase in drag that this involves. Overall, more research is required in this field. This is both in the interest of animal welfare and of avoiding biasing the quality of the collected data.
The northern bald ibis Geronticus eremita disappeared from Europe in the Middle Ages. Since 2003 a migratory population has been reintroduced in Central Europe. We conducted demographic analyses of the survival and reproduction of 384 northern bald ibises over a period of 12 years (2008–2019). These data also formed the basis for a Population Viability Analysis simulating the possible future development of the northern bald ibis population under different scenarios. We analysed life stage-specific survival rates, rearing protocols and colonies, and the influence of stochastic catastrophic events and reinforcement translocations on population growth. Life stage-specific survival probabilities were 0.64–0.78. Forty-five per cent of the mature females reproduced, with a mean fecundity of 2.15 fledglings per nest. The complementary population viability analysis indicated that the Waldrappteam population is close to self-sustainability, with an estimated population growth rate of 0.95 and a 24% extinction probability within 50 years. Of the 326 future scenarios tested, 94% reached the criteria of <5% extinction probabilities and population growth rates >1. Stochastic catastrophic events had only a limited effect. Despite comparatively high survival and fecundity rates the population viability analysis indicated that to achieve self-sustainability the Waldrappteam population needs further translocations to support population growth and the implementation of effective measures against major mortality threats: illegal hunting in Italy and electrocution on unsecured power poles. The findings of this study are to be implemented as part of a second European LIFE project.
The Northern Bald Ibis is an endangered migratory species, which went extinct in Europe in the 17th century. Currently, a translocation project in the frame of the European LIFE program is carried out, to reintroduce a migratory population with breeding colonies in the northern and southern Alpine foothills and a common wintering area in southern Tuscany. The population meanwhile consists of about 200 individuals, with about 90% of them carrying a GPS device on their back. We used biologging data from 2021 to model the habitat suitability for the species in the northern Alpine foothills. To set up a species distribution model, indices describing environmental conditions were calculated from satellite images of Landsat-8, and in addition to the well-proven use of optical remote sensing data, we also included Sentinel-1 actively sensed observation data, as well as climate and urbanization data. A random forest model was fitted on NBI GPS positions, which we used to identify regions with high predicted foraging suitability within the northern Alpine foothills. The model resulted in 84.5% overall accuracy. Elevation and slope had the highest predictive power, followed by grass cover and VV intensity of Sentinel-1 radar data. The map resulting from the model predicts the highest foraging suitability for valley floors, especially of Inn, Rhine, and Salzach-Valley as well as flatlands, like the Swiss Plateau and the agricultural areas surrounding Lake Constance. Areas with a high suitability index largely overlap with known historic breeding sites. This is particularly noteworthy because the model only refers to foraging habitats without considering the availability of suitable breeding cliffs. Detailed analyses identify the transition zone from extensive grassland management to intensive arable farming as the northern range limit. The modeling outcome allows for defining suitable areas for further translocation and management measures in the frame of the European NBI reintroduction program. Although required in the international IUCN translocation guidelines, the use of models in the context of translocation projects is still not common and in the case of the Northern Bald Ibis not considered in the present Single Species Action Plan of the African-Eurasian Migratory Water bird Agreement. Our species distribution model represents a contemporary snapshot, but sustainability is essential for conservation planning, especially in times of climate change. In this regard, a further model could be optimized by investigating sustainable land use, temporal dynamics, and climate change scenarios.
One conspicuous feature of several larger bird species is their annual migration in V-shaped or echelon formation. When birds are flying in these formations, energy savings can be achieved by using the aerodynamic up-wash produced by the preceding bird. As the leading bird in a formation cannot profit from this up-wash, a social dilemma arises around the question of who is going to fly in front? To investigate how this dilemma is solved, we studied the flight behavior of a flock of juvenile Northern bald ibis (Geronticus eremita) during a human-guided autumn migration. We could show that the amount of time a bird is leading a formation is strongly correlated with the time it can itself profit from flying in the wake of another bird. On the dyadic level, birds match the time they spend in the wake of each other by frequent pairwise switches of the leading position. Taken together, these results suggest that bald ibis cooperate by directly taking turns in leading a formation. On the proximate level, we propose that it is mainly the high number of iterations and the immediacy of reciprocation opportunities that favor direct reciprocation. Finally, we found evidence that the animals’ propensity to reciprocate in leading has a substantial influence on the size and cohesion of the flight formations.
A considerable proportion of the world’s bird species undertake seasonal long-distance migrations. These journeys are energetically demanding. Two major behavioural means to reduce energy expenditure have been suggested: the use of thermal uplifts for a soaring-gliding migration style and travelling in echelon or V-shaped formation. Both strategies have immediate consequences for the social organization of the birds as they either cause large aggregations or require travelling in small and stable groups. Here, we first discuss those consequences, and second present an analysis of formation flight in a flock of northern bald ibis on their first southbound migration. We observe clear correlations between leading and trailing on the dyadic level but only a weak correlation on the individual level during independent flight and no convincing correlation during the human guided part of the migration. This pattern is suggestive of direct reciprocation as a means for establishing cooperation during formation flight. In general, we conclude that behavioural adaptations for dealing with physiological constraints on long-distance migrations either necessitate or ultimately foster formation of social groups with different characteristics. Patterns and social organization of birds travelling in groups have been elusive to study; however, new tracking technology—foremost lightweight GPS units—will provide more insights in the near future.
Birds face exceptionally high energy demands during their flight. One visible feature of some species is alternating between flapping and gliding, which should allow them to save energy. To date, there is no empirical evidence of an energetic benefit to this. To understand the physiology behind the strategy, we equipped hand-raised Northern Bald Ibises (Geronticus eremita) with data loggers during human-guided migration. We monitored the position of the birds, wingbeats, overall dynamic body acceleration (ODBA), and heart rates as a proxy for energy expenditure. The energy expenditure was significantly affected by the length of flapping and gliding bouts. A pronounced decrease in heart rate was measured after already 1 s of gliding. Additionally, the heart rate at flapping bouts up to 30 s increased steadily but stabilized thereafter. The gliding proportion during intermittent flight affected the energy saving compared to continuous flapping. At a gliding proportion of about 20%, we measured a maximum of 11% saving based on heart rate measurement. At higher gliding proportions, the additional energy saving was negligible. Furthermore, as during flight, not all energy is used for mechanical work, we found a greater decrease rate of ODBA at different gliding proportions compared to heart rate. Nevertheless, the combination of the two methods is essential to determine birds’ movement and energy expenditure. This study provides empirical evidence that intermittent flight is energetically beneficial and can reduce the high costs of flights.
Migratory journeys represent an energetic challenge for many long-distance migrants. The choice of flight times, migration route, altitude, travelling speed, wingbeat patterns, soaring as well as formation flight can all affect the energy expenditure for the journey. We monitored the flight patterns of two Northern Bald Ibises (Geronticus eremita) equipped with data loggers while crossing the Alps during a human-led migration from southern Germany to Tuscany. We observed that the birds used an intermittent flapping pattern, where phases of active flapping flight were regularly interrupted by short gliding phases. As a result of intermittent flight, the effective wing beat frequency was 13–20% lower than the observed wing beat frequency of 4.0 s−1. When local conditions allowed, the birds gained altitude through circling in thermal updrafts. During those circling bouts, gliding on the outstretched wing was predominant, though active wing flapping was still observed. Overall, the two birds spent 19 and 22% of the time soaring on the outstretched wing, accruing during that time 26 and 28% of the altitude gain required for the crossing of a major mountain range. This shows that, apart from formation flight, northern bald ibis use at least two more strategies—thermal soaring and intermittent flap-gliding—for improving energy economy during migratory flights.
Many migrating birds undertake extraordinary long flights. How birds are able to perform such endurance flights of over 100-hour durations is still poorly understood. We examined energy expenditure and physiological changes in Northern Bald Ibis Geronticus eremite during natural flights using birds trained to follow an ultra-light aircraft. Because these birds were tame, with foster parents, we were able to bleed them immediately prior to and after each flight. Flight duration was experimentally designed ranging between one and almost four hours continuous flights. Energy expenditure during flight was estimated using doubly-labelled-water while physiological properties were assessed through blood chemistry including plasma metabolites, enzymes, electrolytes, blood gases, and reactive oxygen compounds. Instantaneous energy expenditure decreased with flight duration, and the birds appeared to balance aerobic and anaerobic metabolism, using fat, carbohydrate and protein as fuel. This made flight both economic and tolerable. The observed effects resemble classical exercise adaptations that can limit duration of exercise while reducing energetic output. There were also in-flight benefits that enable power output variation from cruising to manoeuvring. These adaptations share characteristics with physiological processes that have facilitated other athletic feats in nature and might enable the extraordinary long flights of migratory birds as well.
In this paper, we present evidence that biologging is strongly correlated with eye irritation, with sometimes severely impairing effects. A migratory population of the Northern Bald Ibis (Geronticus eremita, NBI) is reintroduced in Europe, in course of a LIFE + project. Since 2014, all individuals have been equipped with GPS-devices. Remote monitoring allows the implementation of focussed measures against major mortality causes.
Initially all birds carried battery-powered devices, fixed on the lower back of the birds. Since 2016 an increasing amount of birds has been equipped with solar-powered devices, fixed on the upper back, the more sun-exposed position. In 2016, we observed opacity in the cornea of one eye (unilateral corneal opacity; UCO) during a regular health monitoring for the first time.
By 2018, a total of 25 birds were affected by UCO, with varying intensity up to blindness. Clinical examination of the birds revealed no clear cause for the symptoms. However, only birds carrying a device on the upper back were affected (2017 up to 70% of this group). In contrast, none of the birds carrying devices on the lower back ever showed UCO symptoms. This unexpected relationship between tagging and UCO was discovered in 2017. After we took countermeasures by removing the device or repositioning it on the lower back, we observed an immediate reduction of the incidence rate without any new cases reported since January 2019. NBI roost with their head on the back, one eye closely placed to the device if it was positioned on the upper back. Thus, we conclude that the most parsimonious explanation for the symptomatology is either a repetitive slight temperature rise in the corneal tissue due to electromagnetic radiation by the GSM module of the device or a repetitive slight mechanical irritation of the corneal surface. Concrete evidence is missing so far. Meanwhile, cases of UCO were found in another NBI population.
Our observations indicate that further research in the fast-growing field of biologging is urgently needed. The findings question the positioning of devices on the upper back in birds roosting with the head on the back.
A blower-type wind tunnel for physiological bird flight experiments has been developed, constructed and evaluated. Since the birds to be investigated are rather big (Northern Bald Ibis, Geronticus eremita), the cross-sectional area of the test section measures 2.5 m × 1.5 m. The maximum achievable flow speed is approximately 16 ms−1. The wind tunnel exhibits a flexible outlet nozzle to provide up- and downdraft to allow for gliding and climbing flights. The current paper describes in detail the layout, design and construction of the wind tunnel including its control. Numerical simulations of the flow and measurements of the velocity distribution in the test section are presented. Apart from a non-homogeneous flow region in the mixing layer at the boundaries of the free jet, the test section exhibits a very even velocity distribution; the local speed deviates by less than two percent from the mean velocity. The turbulence intensity inside the test section was measured to be between 1 and 2%. As a constraint, a limited budget was available for the project. Four northern bald ibises were hand-raised and trained to fly in the wind tunnel.
Many threatened species are bred in captivity for conservation purposes and some of these programmes aim at future reintroduction. The Northern Bald Ibis, Geronticus eremita, is a Critically Endangered bird species, with recently only one population remaining in the wild (Morocco, Souss Massa region). During the last two decades, two breeding programs for reintroduction have been started (in Austria and Spain). As the genetic constitution of the founding population can have strong effects on reintroduction success, we studied the genetic diversity of the two source populations for reintroduction (‘Waldrappteam’ and ‘Proyecto eremita’) as well as the European zoo population (all individuals held ex situ) by genotyping 642 individuals at 15 microsatellite loci. To test the hypothesis that the wild population in Morocco and the extinct wild population in the Middle East belong to different evolutionary significant units, we sequenced two mitochondrial DNA fragments. Our results show that the European zoo population is genetically highly structured, reflecting separate breeding lines. Genetic diversity was highest in the historic samples from the wild eastern population. DNA sequencing revealed only a single substitution distinguishing the wild eastern and wild western population. Contrary to that, the microsatellite analysis showed a clear differentiation between them. This suggests that genetic differentiation between the two populations is recent and does not confirm the existence of two evolutionary significant units. The European zoo population appears to be vital and suitable for reintroduction, but the management of the European zoo population and the two source populations for reintroductions can be optimized to reach a higher level of admixture.
The Northern Bald Ibis is one of the rarest bird species, extinct in Europe for 400 years and critically endangered worldwide. The European Union-co-financed LIFE+ project “Reason for Hope – Reintroduction of the Northern Bald Ibis in Europe” aims to reintroduce the species in Europe (Germany, Austria, Italy). In order to obtain information on the genetic diversity within zoo colonies and the reintroduced population, 15 polymorphic microsatellite markers, specific for the Northern Bald Ibis, Geronticus eremita (Linnaeus, 1785), have been isolated from next-generation sequencing (Illumina MiSeq) and are described here. The microsatellite primers were tested in 30 individuals and measures of genetic variability were calculated. Values for the observed heterozygosity ranged from 0.393 to 0.867, while expected heterozygosity ranged from 0.573 to 0.718. Ten out of 15 loci were in Hardy–Weinberg equilibrium and only one showed indication for the presence of null alleles. The newly developed PCR primers can be used to examine population genetic parameters, e.g. for future conservation genetic studies of this critically endangered bird species.
The critically endangered Northern Bald Ibis (Geronticus eremita) is a migratory bird that became extinct in Europe centuries ago. Since 2014, the Northern bald ibis is subject to an intensive rehabilitation and conservation regime aiming to reintroduce the bird in its original distribution range in Central Europe and concurrently to maintain bird health and increase population size. Hitherto, virtually nothing is known about the microbial communities associated with the ibis species; an information pivotal for the veterinary management of these birds. Hence, the present study was conducted to provide a baseline description of the cultivable microbiota residing in the Northern bald ibis. Samples derived from the choana, trachea, crop and cloaca were examined employing a culturomic approach in order to identify microbes at each sampling site and to compare their frequency among age classes, seasonal appearances and rearing types. In total, 94 microbial species including 14 potentially new bacterial taxa were cultivated from the Northern bald ibis with 36, 58 and 59 bacterial species isolated from the choana, crop and cloaca, respectively. The microbiota of the Northern bald ibis was dominated by members of the phylum Firmicutes, followed by Proteobacteria, Actinobacteria, Bacteroidetes and Fusobacteria, altogether phylotypes commonly observed within avian gut environments. Differences in relative abundances of various microbial taxa were evident among sample types indicating mucosa-specific colonisation properties and tissue tropism. Besides, results of the present study indicate that the composition of microbiota was also affected by age, season (environment) and rearing type. While the prevalence of traditional pathogenic microbial species was extremely low, several opportunists including Clostridium perfringens toxotype A were frequently present in samples indicating that the Northern bald ibis may represent an important animal reservoir for these pathogens. In summary, the presented study provides a first inventory of the cultivable microbiota residing in the critically endangered Northern bald ibis and represents a first step in a wider investigation of the ibis microbiome with the ultimate goal to contribute to the management and survival of this critically endangered bird.
From the perspective of zoological institutions reintroduction projects offer many possibilities to link conservation and research programmes. An example of the multi-layered and diverse contributions that zoological institutions in general and, specifically, Vienna Zoo, Austria, can make is the reintroduction of the Northern bald ibis Geronticus eremita in central Europe. The involvement of zoological institutions ranges from the provision of eggs or birds for release trials, to financial and advocacy support, including with government agencies and non-governmental organizations. Through involvement at a steering level at the coordinative association ‘Förderverein Waldrappteam’ and as a partner in the EU LIFE+ reintroduction project, Vienna Zoo directly contributes to the shape of the reintroduction project for this Critically Endangered species, and provides much more than technical and infrastructural support. The reintroduction of the Northern bald ibis is broadly in line with the reintroduction guidelines of the International Union for Conservation of Nature. This project provides added benefits not only through its work to prevent the illegal hunting of migratory birds but also the production and dissemination of scientific research.
Under the project of “Human-Led Migration,” the authors had the unique opportunity to accompany hand-raised northern bald Iibises (NBIs; Geronticus eremita) during migration, which occurred in stages from Bavaria, Germany, to southern Tuscany, Italy. The aim of this study was to investigate the immediate effects of flight, with respect to flight duration, and the more delayed recovery effects on hematologic variables. A total of 31 birds were sampled. Blood samples were taken immediately before take-off, after landing, and 1 day after the flight. Hematocrit was determined and blood smears were prepared to estimate the total white blood count with leukocyte concentrations and differential blood cell count. Postflight, significant decreases in hematocrit, tWBC, lymphocytes (abs., %), heterophils (abs.), eosinophils (abs., %), and monocytes (abs.) were observed. In contrast, heterophils (%), basophils (%), and the heterophil/lymphocyte (H/L) ratio increased significantly. With increasing flight duration, the H/L ratio increased further. One day postflight, there were still significant decreases in tWBC, lymphocytes (abs.), and eosinophils (abs., %) and significant increases in heterophils (%) and the H/L ratio. The hematocrit dropped even further. These data show that the decrease of tWBC is mainly caused by the lymphocyte fraction and that NBIs need more than 1 day to reverse the postflight changes in some hematologic values. Hematocrit changes postflight and on the recovery day are most likely to be explained by hemodynamics and the metabolic and hormonal changes caused by flight. The hematologic changes postflight in NBIs were largely consistent with those of other birds, but they differed from humans and mammals postexercise mainly in the levels of tWBC, heterophils (matching neutrophils in mammals), and lymphocytes.
With this project we want to investigate the physiology of bird migration in free flight using the example of the northern bald ibis. A hand-reared group is to be guided on their autumn migration to northern Italy. The northern bald ibis is a globally endangered bird species that became extinct in Europe at the end of the Middle Ages. Establishing migratory behavior using a guided train is an essential part of an international action plan for the conservation of this species. The aim of the application is to carry out physiological investigations during migration in order to gain a better understanding of the physiology and energetics of the flight of migrating birds. The close contact between the birds and their foster parents allows for data collection with minimal disruption to the birds. The analysis of the individual flight behavior plays a special role. The flight behavior is compared with blood-physiological parameters that are suitable for the energetic conditions, the use of endogenous fat and protein as energy sources and the
to characterize endurance performance. With the help of the “double marked water” method, the individual energy consumption during the flights is to be examined. The non-invasive analysis of corticosterone in fecal samples will complement the blood-physiological and energetic data. The recording of the body mass and the non-invasive assessment of the visible subcutaneous fat reserves serve as a measure of the use of the body’s own energy sources. The flight plan is designed in such a way that long (>100 km) and short (<50 km) daily flight stages alternate in the first year of the study, so that the relationship between flight duration and physiological parameters can be examined at extremely different loads. In the second year, the flight routes are determined by the birds themselves. This makes it possible to document the naturally occurring target values with regard to the regulation of migration behavior and physiology. The planned study is the first to integratively investigate diagnostic blood parameters, endocrine data and energetic measurements in a free-flying migratory bird.
It has long been believed that the primary function of formation flying is to conserve energy by using the thermal lift generated by the bird flying ahead. This assumption is often presented in the literature as a proven fact, although it has so far only been supported primarily by theoretical models and simulations, while empirical data is largely lacking due to a lack of adequate technical possibilities. The Austrian Northern Bald Ibis team has been researching formation flight in Northern Bald Ibises (Geronticus eremita) in cooperation with various partners for many years. The unique possibility of human-led migration is used to release this endangered migratory bird species. On these flights, hand-reared young birds are led over a distance of around 800 km to Tuscany using ultralight aircraft. In a study (Portugal et al. 2014; NATURE), the team was able to show that northern bald ibises coordinate themselves very precisely in formation flight, which largely corresponded to the assumptions of theoretical models. However, there was still no direct evidence from measuring the energy expenditure. Quantitative measurements during the migration flights were therefore a key objective of the research project financed by the FWF. In addition, it should be investigated which mechanisms ensure stable cooperation during formation flight. We equipped all 30 birds in the formation with specially developed, aerodynamically shaped data loggers. In addition to motion sensors, these also included high-frequency GNSS loggers, which made it possible to determine the position with a deviation of a few centimetres. In addition, five birds were equipped with a non-invasive ECG for continuous heart rate measurement. The approximately 1.2 million position and 45,000 heart rate measurements collected in this way are the first approach to empirical data acquisition in migratory birds during migration. We found that during the flights, the birds mostly positioned themselves in a narrow area laterally offset behind a conspecific. These results are essentially in agreement with current theories. However, the birds flying sideways behind each other overlapped by almost half a wingspan, while most models assume only a few percent wingtip overlap. A plausible explanation for this is that these simplified models only focused on the lift-generating wings and do not sufficiently consider the influence of the aerodynamics of the bird’s body. Our data also provide quantitative results for the first time on energy savings through formation flight. The heart rate measurements combined with total body dynamic acceleration (ODBA) show that the birds’ heart rates decrease significantly when flying in formation. Surprisingly, the number of short, intermediate gliding sequences also increased when the birds flew in formation. This suggests that part of the energy savings during formation flight is due to an increased proportion of slip joints. This is a new and surprising finding that significantly affects our understanding of formation flight.