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 almost 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.
Species distribution models (SDM) link species occurrence with a suite of environmental predictors and provide an estimate of habitat quality when the variable set captures the biological requirements of the species. SDMs are inherently more complex when they include components of a species' ecology such as conspecific attraction and behavioral flexibility to exploit resources that vary across time and space. Wading birds are highly mobile, demonstrate flexible habitat selection, and respond quickly to changes in habitat quality; thus serving as important indicator species for wetland systems. We developed a spatio-temporal, multi-SDM framework using Great Egret (Ardea alba), White Ibis (Eudocimus albus), and Wood Stork (Mycteria Americana) distributions over a decadal gradient of environmental conditions to predict species-specific abundance across space and locations used on the landscape over time. In models of temporal dynamics, species demonstrated conditional preferences for resources based on resource levels linked to differing temporal scales. Wading bird abundance was highest when prey production from optimal periods of inundation was concentrated in shallow depths. Similar responses were observed in models predicting locations used over time, accounting for spatial autocorrelation. Species clustered in response to differing habitat conditions, indicating that social attraction can co-vary with foraging strategy, water-level changes, and habitat quality. This modeling framework can be applied to evaluate the multi-annual resource pulses occurring in real-time, climate change scenarios, or restorative hydrological regimes by tracking changing seasonal and annual distribution and abundance of high quality foraging patches.
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.
Worldwide, Salmonella spp. is a significant cause of disease for both humans and wildlife, with wild birds adapted to urban environments having different opportunities for pathogen exposure, infection, and transmission compared to their natural conspecifics. Food provisioning by people may influence these factors, especially when high-density mixed species flocks aggregate. White Ibises (Eudocimus albus), an iconic Everglades species in decline in Florida, are becoming increasingly common in urbanized areas of south Florida where most are hand-fed. We examined the prevalence of Salmonella shedding by ibises to determine the role of landscape characteristics where ibis forage and their behavior, on shedding rates. We also compared Salmonella isolated from ibises to human isolates to better understand non-foodborne human salmonellosis. From 2010-2013, 13% (n = 261) adult/subadult ibises and 35% (n = 72) nestlings sampled were shedding Salmonella. The prevalence of Salmonella shedding by ibises significantly decreased as the percent of Palustrine emergent wetlands and herbaceous grasslands increased, and increased as the proportion of open-developed land types (e.g. parks, lawns, golf courses) increased, suggesting that natural ecosystem land cover types supported birds with a lower prevalence of infection. A high diversity of Salmonella serotypes (n = 24) and strain types (43 PFGE types) were shed by ibises, of which 33% of the serotypes ranked in the top 20 of high significance for people in the years of the study. Importantly, 44% of the Salmonella Pulsed-Field Gel Electrophoresis patterns for ibis isolates (n = 43) matched profiles in the CDC PulseNet USA database. Of these, 20% came from Florida in the same three years we sampled ibis. Importantly, there was a negative relationship between the amount of Palustrine emergent wetland and the number of Salmonella isolates from ibises that matched human cases in the PulseNet database (p = 0.056). Together, our results indicate that ibises are good indicators of salmonellae strains circulating in their environment and they have both the potential and opportunity to transmit salmonellae to people. Finally, they may act as salmonellae carriers to natural environments where other more highly-susceptible groups (nestlings) may be detrimentally affected.
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 over 2 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’.
A new quill mite species of the family Syringophilidae (Acariformes: Prostigmata: Cheyletoidea) is described from Phimosus infuscatus (Lichtenstein) (Pelecaniformes: Threskiornithidae) in Argentina. Selenonycha insperata n. sp. differs from other species of the genus Selenonycha Kethley, 1970 by the presence of wing-like cuticular projections of coxal fields III-IV situated in front of trochanters (vs absence). An unexpected finding of this species on a bird of the family Threskiornithidae (Pelecaniformes) is discussed as an example of host shift. Additionally, a key to the species of the genus is provided.