Matching times of leading and following suggest cooperation through direct reciprocity during V-formation flight in ibis
- Proceedings of the National Academy of Sciences of the United States of America
- Published over 5 years ago
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.
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.
The reproductive season is energetically costly as revealed by elevated glucocorticoid concentrations, constrained immune functions and an increased risk of infections. Social allies and affiliative interactions may buffer physiological stress responses and thereby alleviate associated effects. In the present study, we investigated the seasonal differences of immune reactive corticosterone metabolite concentrations, endoparasite burden (nematode eggs and coccidian oocysts) and affiliative interactions in northern bald ibis (Geronticus eremita), a critically endangered bird. In total, 43 individually marked focal animals from a free-ranging colony were investigated. The analyses included a description of initiated and received affiliative interactions, pair bond status as well as seasonal patterns of hormone and endoparasite levels. During the reproductive season, droppings contained parasite eggs more often and corticosterone metabolite levels were higher as compared to the period after reproduction. The excretion rate of endoparasite products was lower in paired individuals than in unpaired ones, but paired animals exhibited higher corticosterone metabolite concentrations than unpaired individuals. Furthermore, paired individuals initiated affiliative behaviour more frequently than unpaired ones. This suggests that the reproductive season influences the excretion patterns of endoparasite products and corticosterone metabolites and that affiliative interactions between pair partners may positively affect endoparasite burden during periods of elevated glucocorticoid levels. Being embedded in a pair bond may have a positive impact on individual immune system and parasite resistance.
Dark pigments provide animals with several adaptive benefits such as protection against ultraviolet (UV) radiation and mechanical abrasion, but may also impose several constraints like a high absorbance of solar radiation. Endotherms, with relatively constant and high body temperatures, may be especially prone to thermoregulatory limitations if dark coloured and inhabiting hot environments. It is therefore expected that adaptations have specifically evolved because of these limitations. Bare, highly vascularised head skin may have evolved in birds with dark plumage from hot geographical regions because of favouring heat dissipation. Using the Northern bald ibis (Geronticus eremita) as a model species, we measured the surface temperature (Tsurf) of the head, the bill and the black feathered body of 11 birds along ambient temperatures (Ta) ranging from 21 to 42.5 °C employing thermal imaging.
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.
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, fifteen polymorphic microsatellite markers, specific for the Northern Bald Ibis, Geronticus eremita (LINNAEUS, 1785), have been isolated from next-generation sequencing (Illumina MiSeq) and are here described. 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 fifteen 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.
Relation between travel strategy and social organization of migrating birds with special consideration of formation flight in the northern bald ibis
- Philosophical transactions of the Royal Society of London. Series B, Biological sciences
- Published about 3 years ago
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.This article is part of the themed issue ‘Physiological determinants of social behaviour in animals’.
The parasitic quill mites of the family Syringophilidae (Acariformes: Prostigmata) are recorded on ibises and spoonbills (Pelecaniformes: Threskiornithidae) for the first time. Four new species of the genus Stibarokris Kethley, 1970 are described: 1) S. theristicus Skoracki, Zmudzinski & Unsoeld sp. nov. ex Theristicus caudatus (Boddaert, 1783) from Brazil, 2) S. geronticus Skoracki, Zmudzinski & Unsoeld sp. nov. ex Geronticus calvus (Boddaert, 1783) from South Africa, 3) S. brevisetosus Skoracki & Zmudzinski sp. nov. ex Plegadis falcinellus (L., 1766) from Turkey, and 4) S. plataleus Skoracki & Zmudzinski sp. nov. ex Platalea leucorodia L., 1758 from Austria. Additionally, a key to all described species in the genus is presented, and hypothesis of the Gondwanan origin of syringophilids associated with ibises and spoonbills is briefly discussed.
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.
Ambient temperature and air pressure are relevant stimuli that can elicit hormonal responses in alignment with adjusting individuals' physiology and behaviour. This study investigated possible changes in corticosterone © and testosterone (T) and contingencies with behaviour in response to ambient temperature and air pressure, and it evaluated the temporal response dynamics of these hormones in 12 individual Greylag geese (Anser anser) over 26 and 12 individual Northern bald ibis (Geronticus eremita) over 27 days, during late winter. Immunoreactive metabolites of C and T were analysed non-invasively from 626 fecal samples by means of group-specific antibodies and correlated to behaviour and weather factors. In both species, high C levels correlated with low temperatures 24hours before sampling, but low C levels correlated with high air pressure 6 to 12hours before sampling. In both species, C levels and behavioural activity were negatively correlated. In addition, temperature had a positive influence on T levels in both species 12 to 24hours before sampling. The fact that weather conditions influenced changes in levels of C, while social interactions did not, is indicative of a general mechanism of graduated physiological adjustment to environmental variations affecting metabolism, stress responses and behaviour.