Flight Style Research Articles

Insights into Argentavis magnificens (Aves, Teratornithidae) lifestyle based on neuroanatomy.

Teratornithidae is an extinct bird family, likely related to Cathartidae, known exclusively from the Americas. They were once thought to be scavengers, but recent theories suggest they were opportunistic or piscivorous birds capable of swallowing prey whole. The most notable species, Argentavis magnificens, had a wingspan of 6 to 8 m and weighed 70 to 80 kg. In order to infer paleobiological aspects of this bird, its endocast (as a proxy for brain morphology), reconstructed from computed tomography scans of the holotype skull, is here described and compared to that of other bird species of zoophagous feeding habits with different flight styles. The brain of Argentavis presents a general appearance similar to that of Cathartidae, being dorsoventrally flattened and anteroposteriorly elongated, with small optic lobes in relation to the total encephalic surface. The estimated volume of the bulbi olfactorii is very similar to that of the Andean Condor Vultur gryphus. The main difference observed with Cathartidae is the marked development of the eminentiae sagittales present in Argentavis (structures closely related to the perception of visual information), which are more similar to those of the Accipitriformes and Falconiformes analyzed. The results obtained here suggest that Argentavis was a scavenger or even maybe a kleptoparasitic bird, relying more on vision than on smell (similar to that observed in the Andean Condor). Furthermore, the inner ear and flocculi exhibit characteristics similar to birds without acrobatic flight, indicating that Argentavis had a soaring flight and inhabited open areas without much vegetation.

Oxidative state is associated with migration distance, but not traits linked to flight energetics

Flight can be highly energy demanding, but its efficiency depends largely on flight style, wing shape and wing loading, and a range of morphological and lifestyle adaptations that can modify the cost of sustained flight. Such behavioural and morphological adaptations can also influence the physiological costs associated with migration. For instance, during intense flight and catabolism of reserves, lipid damage induced by pro‐oxidants increases, and to keep oxidative physiological homeostasis under control, the antioxidant machinery can be upregulated. Studies on the oxidative physiology of endurance flight have produced contradictory results, making generalization difficult, especially because multispecies studies are missing. Therefore, to explore the oxidative cost of flight and migration, we used samples collected during the breeding season from 113 European bird species and explored the associations of measures of antioxidant capacity (total antioxidant status, uric acid and glutathione concentration) and oxidative damage of lipids (malondialdehyde) with variables reflecting flight energetics (year‐round or specifically during migration) using a phylogenetic framework. We found that none of the traits predicting year‐round flight energy expenditure (flight style, wing morphology and flight muscle morphology) explained any measures of oxidative state. Our results suggest that birds endure their everyday flight exercise without or with low oxidative cost. However, oxidative damage to lipids and one component of the endogenous antioxidant system (uric acid), measured after the end of spring migration on breeding adult birds, increased with migration distance. Our results suggest that migration could have oxidative consequences that might be carried over to subsequent life‐history stages (breeding).

A secondary endochondral ossification centre in the furcula of extant birds and its significance for the evolution of the neornithine acrocoracoclavicular joint

ABSTRACT The processus acrocoracoideus claviculae on the furcular epicleidium of some extant birds has been hypothesised to have developed independently from the main body of furcula, potentially representing a secondary ossification centre within avian furcula. However, the developmental pattern of the processus acrocoracoideus claviculae remains unclear, impeding our understanding of its homology and evolution. Here, we analysed the morphology, articulation and developmental pattern of the avian furcular epicleidium through X-ray computed tomography scanning and histochemical staining in several bird exemplars. The results show that the processus acrocoracoideus claviculae is a secondary endochondral ossification in the furcula, distinct from the intramembranously ossified main furcula and separated by connective tissue. The processus acrocoracoideus claviculae fuses with the furcula during postnatal development and forms the articular surface of the acrocoracoclavicular joint. The developmental pattern suggests that the left and right processus acrocoracoideus claviculae may be formed by the fusion of a sesamoid with the respective furcular ramus and evolved convergently among different neornithine lineages. This unique structure of furcula not only increases the morphological diversity of the acrocoracoclavicular joint in neornithine birds but also lays the foundation for their complex and diverse flight styles.

The respiratory system influences flight mechanics in soaring birds.

The subpectoral diverticulum (SPD) is an extension of the respiratory system in birds that is located between the primary muscles responsible for flapping the wing1,2. Here we survey the pulmonary apparatus in 68 avian species, and show that the SPD was present in virtually all of the soaring taxa investigated but absent in non-soarers. We find that this structure evolvedindependently with soaring flight at least seven times, which indicates that the diverticulum might have a functional and adaptive relationship with this flight style. Using the soaring hawks Buteo jamaicensis and Buteo swainsoni as models, we show that the SPD is not integral for ventilation, that an inflated SPD can increase the moment arm of cranial parts of the pectoralis, and that pectoralis muscle fascicles are significantly shorter in soaring hawks than in non-soaring birds. This coupling of an SPD-mediated increase in pectoralis leverage with force-specialized muscle architecture produces a pneumatic system that is adapted for the isometric contractile conditions expected in soaring flight. The discovery of a mechanical role for the respiratory system in avian locomotion underscores the functional complexity and heterogeneity of this organ system, and suggests that pulmonary diverticula are likely to have other undiscovered secondary functions. These data provide a mechanistic explanation for the repeated appearance of the SPD in soaring lineages and show that the respiratory system can be co-opted to provide biomechanical solutions to the challenges of flight and thereby influence the evolution of avian volancy.

Albatrosses employ orientation and routing strategies similar to yacht racers

The way goal-oriented birds adjust their travel direction and route in response to wind significantly affects their travel costs. This is expected to be particularly pronounced in pelagic seabirds, which utilize a wind-dependent flight style called dynamic soaring. Dynamic soaring seabirds in situations without a definite goal, e.g. searching for prey, are known to preferentially fly with crosswinds or quartering-tailwinds to increase the speed and search area, and reduce travel costs. However, little is known about their reaction to wind when heading to a definite goal, such as homing. Homing tracks of wandering albatrosses (Diomedea exulans) vary from beelines to zigzags, which are similar to those of sailboats. Here, given that both albatrosses and sailboats travel slower in headwinds and tailwinds, we tested whether the time-minimizing strategies used by yacht racers can be compared to the locomotion patterns of wandering albatrosses. We predicted that when the goal is located upwind or downwind, albatrosses should deviate their travel directions from the goal on the mesoscale and increase the number of turns on the macroscale. Both hypotheses were supported by track data from albatrosses and racing yachts in the Southern Ocean confirming that albatrosses qualitatively employ the same strategy as yacht racers. Nevertheless, albatrosses did not strictly minimize their travel time, likely making their flight robust against wind fluctuations to reduce flight costs. Our study provides empirical evidence of tacking in albatrosses and demonstrates that man-made movement strategies provide a new perspective on the laws underlying wildlife movement.

What makes the diverse flight of birds possible? Phylogenetic comparative analysis of avian alula morphology

Abstract Studies on the evolution of avian flight have failed to clarify why wing shape is weakly correlated with flight styles and phylogenetically constrained. Birds seem to have achieved their diverse flight styles owing to changes in the shapes of localized parts of the wing, despite a highly conserved wing outline. The alula, which stems from the first digit of the wing, is a part of the wing that might have enabled various flight styles to develop. To test this hypothesis, we measured alula length and width using museum specimens of 187 species from 21 orders of birds and used a phylogenetic comparative method to investigate the relationship between alula morphology and flight style, body mass, habitat and migratory distance. We found that: (1) phylogenetic signals were weak for the alula width and aspect ratio but moderate for length; (2) alula morphology exhibited an allometric relationship with body mass; and (3) fewer flapping birds had large alulae. Alula morphology might have evolved in response to changes in body mass and flight styles. Variations in the shape of localized wing parts, such as the alula, which modifies airflow around a wing, might be key to the evolution of the diverse flight styles of birds.

Extremely low daylight sea-crossing flights of a nocturnal migrant.

Understanding the trade-off between energy expenditure of carrying large fuel loads and the risk of fuel depletion is imperative to understand the evolution of flight strategies during long-distance animal migration. Global flyways regularly involve sea crossings that may impose flight prolongations on migrating land-birds and thereby reduce their energy reserves and survival prospects. We studied route choice, flight behavior, and fuel store dynamics of nocturnally migrating European nightjars (Caprimulgus europaeus) crossing water barriers. We show that barrier size and groundspeed of the birds influence the prospects of extended daylight flights, but also that waters possible to cross within a night regularly result in diurnal flight events. The nightjars systematically responded to daylight flights by descending to about a wingspan's altitude above the sea surface while switching to an energy-efficient flap-glide flight style. By operating within the surface-air boundary layer, the nightjars could fly in ground effect, exploit local updraft and pressure variations, and thereby substantially reduce flight costs as indicated by their increased proportion of cheap glides. We propose that surface-skimming flights, as illustrated in the nightjar, provide an energy-efficient transport mode and that this novel finding asks for a reconsideration of our understanding of flight strategies when land-birds migrate across seas.

Reconstructing locomotor ecology of extinct avialans: a case study of Ichthyornis comparing sternum morphology and skeletal proportions.

Avian skeletal morphology is associated with locomotor function, including flight style, swimming and terrestrial locomotion, and permits informed inferences on locomotion in extinct taxa. The fossil taxon Ichthyornis (Avialae: Ornithurae) has long been regarded as highly aerial, with flight similar to terns or gulls (Laridae), and skeletal features resembling foot-propelled diving adaptations. However, rigorous testing of locomotor hypotheses has yet to be performed on Ichthyornis, despite its notable phylogenetic position as one of the most crownward stem birds. We analysed separate datasets of three-dimensional sternal shape (geometric morphometrics) and skeletal proportions (linear measurements across the skeleton), to examine how well these data types predict locomotor traits in Neornithes. We then used this information to infer locomotor capabilities of Ichthyornis. We find strong support for both soaring and foot-propelled swimming capabilities in Ichthyornis. Further, sternal shape and skeletal proportions provide complementary information on avian locomotion: skeletal proportions allow better predictions of the capacity for flight, whereas sternal shape predicts variation in more specific locomotor abilities such as soaring, foot-propelled swimming and escape burst flight. These results have important implications for future studies of extinct avialan ecology and underscore the importance of closely considering sternum morphology in investigations of fossil bird locomotion.

Allometry of the pectoral flight muscles in birds: Flight style is related to variability in the mass of the supracoracoideus muscle

AbstractAvian flight is powered by a downstroke force generated by the pectoralis (P) muscle and an upstroke force generated by the supracoracoideus (SC) muscle. Some taxa, notably penguins and hummingbirds, have very low P:SC ratios associated with larger masses of the supracoracoideus. Allometric relationships of these muscles are not reported relative to body mass and presumably the two muscles will exhibit isometry in volant birds. This study collated muscle masses for over 600 species representing 28 orders of birds and used phylogenetically controlled analysis of covariance to test for the effects of taxonomic grouping on the allometry of the flight muscles in birds. The P:SC ratio and the standardized residuals for the allometric relationships, were calculated for different orders. The pectoralis scaled isometrically with body mass but the supracoracoideus muscle exhibited a slight but significant negative allometry. Both muscles showed significant effects of taxonomic group but this effect was magnified for the supracoracoideus. Wing‐propelled divers and hovering hummingbirds had disproportionately high proportions of supracoracoideus muscles but tinamous, gamebirds and pigeons, which exhibit burst flight, also had low P:SC ratios. Many taxonomic groups had a ratio around 10:1 but values of 20:1, recorded for birds of prey and owls, were associated with relatively small masses of the supracoracoideus muscle. The P:SC ratio seems to reflect differing flight styles with the greater variability being more associated with the size of the supracoracoideus, the significance of which has not necessarily been fully appreciated in the morphology and flight action of birds.

Kütle ve Kanat Alanı Grafiğinden Kanat Formlarının İncelenmesi

The wing loading parameter depending on the wing area and weight and the aspect ratio parameter, which is the wing shape factor, are the main parameters that determine the fixed-wing flight mechanics. In this study, the relationship between wing forms and flight style of 195 bird species was evaluated using wing area and mass scatter plot. The slope of the mass and wing area chart is proportional to the 1/wing loading. The results showed that birds with more wing area per unit mass tended to perform unpowered flight styles such as soaring and gliding; and birds with less wing area per unit mass tended to have powered flight styles, such as flapping and hovering. In general, it has been found that the slope of the trendline curve is more inclined tended to expend more energy in flight. Unlike the fixed-wing flight mechanics, hand-wings and arm-wings should also be examined to understand the flight mechanics of flapping wings as different effects occur during flapping flight in terms of the lift and thrust forces. In addition, scythe-shaped wings differ from high-speed wings in terms of the ratio of hand wing length/arm wing length according to their wing structure.

Do Seabirds Control Wind Drift during Their Migration across the Strait of Gibraltar? A Study Using Remote Tracking by Radar

This study presents data on the directional flying behaviour of the five most abundant seabird species migrating across the Strait of Gibraltar in relation to the wind, as observed from the north coast, based on radar tracking, and identified to species level by visual observations. A total of 318 seabird trajectories were analysed, illustrating the expected east–west or west–east movements in spring and autumn. We hypothesised that the seabirds that cross the Strait channel during their migrations would behave differently with respect to compensation for wind direction, depending on their flight styles, the migratory period, and the prevailing winds. In this regard, our results showed that flapping birds (Razorbill, Puffin, Northern Gannet, and Balearic shearwater) compensated for wind drift independently of the season and the predominant wind direction. This agrees with the theory that suggests that under moderate winds and whenever visual contact with the coastline is present (as in the case of our study), migrants should compensate for wind drift to avoid being drifted towards the coast, off their main direction of flight. However, Cory’s shearwater, an active gliding seabird with long, slender wings, showed an adaptive directional response to wind, allowing it to be drifted in spring when westerly tailwinds were prevalent, but compensated for wind in autumn, when both easterly and westerly winds were similarly frequent. This adaptive flight behaviour allows it to take advantage of the prevailing tailwinds in spring, gaining ground speed and saving energy during its passage through the Strait, while in autumn, more frequent headwind conditions and a more directional migration to the south may favour compensating for wind drift. Our results support the usefulness of bird radar as a remote tool for describing the pattern of animal movements in the marine environment, as well as their behavioural response to atmospheric conditions. These studies are particularly relevant in the current framework of climate change.

Geometric morphometric analysis of the humerus in New and Old World vultures.

The vulture guild is composed of two distinct groups, Old and New World, which provide a unique insight into how morphology varies among convergent species. All vultures are considered to be large birds of prey that utilize a style of flight called thermal soaring to search and feed primarily on carrion. Even though this flight style is exhibited among all 23 species, slight variations in their skeletal morphology may relate to their differences in ecology. We hypothesized that vulture humeral morphology varies in relation to these organisms' habitat, average body mass, courtship displays, and migratory behavior. To address this hypothesis, we used three-dimensional geometric morphometrics to measure the overall shape differences of vulture humeri. Humeral morphology was found to vary most by habitat association and migratory tendency. The humeri of vultures that inhabit forested areas exhibit features that suggest increased flapping flight compared to those in open and mountainous regions. Migratory species were found to possess more robust features near the glenohumeral joint. We found these (and other features) have some utility for predicting ecology and behavior, but we suggest that further investigation into skeletal and muscular wing elements may reveal greater understanding of the habits of extinct vulture species.

Novel flight style and light wings boost flight performance of tiny beetles

Flight speed is positively correlated with body size in animals1. However, miniature featherwing beetles can fly at speeds and accelerations of insects three times their size2. Here we show that this performance results from a reduced wing mass and a previously unknown type of wing-motion cycle. Our experiment combines three-dimensional reconstructions of morphology and kinematics in one of the smallest insects, the beetle Paratuposa placentis (body length 395 μm). The flapping bristled wings follow a pronounced figure-of-eight loop that consists of subperpendicular up and down strokes followed by claps at stroke reversals above and below the body. The elytra act as inertial brakes that prevent excessive body oscillation. Computational analyses suggest functional decomposition of the wingbeat cycle into two power half strokes, which produce a large upward force, and two down-dragging recovery half strokes. In contrast to heavier membranous wings, the motion of bristled wings of the same size requires little inertial power. Muscle mechanical power requirements thus remain positive throughout the wingbeat cycle, making elastic energy storage obsolete. These adaptations help to explain how extremely small insects have preserved good aerial performance during miniaturization, one of the factors of their evolutionary success.

Relative forelimb–hindlimb investment is associated with flight style, foraging strategy, and nestling period, but not nest type

AbstractWe investigated Dial’s 2003 hypothesis that birds that rely more heavily on flight as their primary mode of locomotion and thus invest more in their forelimbs than hindlimbs will experience selection for smaller body sizes, greater altriciality, and more complex nests. To test this hypothesis, we examined the skeletons of over 2,000 individuals from 313 species representing the majority of avian families and all major branches of the avian tree. We used the lengths of the sternal keel and long bones of the wing relative to the lengths of the leg long bones as an index of relative locomotor investment. We found that locomotor investment was predicted by flight style, foraging method, and length of nestling period, supporting Dial’s hypothesis. Soaring birds and birds with more acrobatic flight styles, birds whose foraging methods were heavily reliant upon flight, and birds whose young spent more time in the nest tended to invest more in their forelimbs relative to hindlimbs. Nest type and body size were not significant predictors of relative forelimb–hindlimb investment, however, suggesting that the relationships among flight style, locomotor investment, and life history are not as tightly intertwined as Dial originally hypothesized.

Book Review

Book Review

(Invited) Humeral Bone Strength and Flight in Eumaniraptoran Dinosaurs

The strength of the humerus bone is evaluated for 17 species of extant birds with varying mass and flight styles by measuring its section modulus. The least massive bird is Regulus calendula (0.0058 kg) while the most massive is Cygnus olor (8.959 kg), a range in mass spanning more than three orders of magnitude. The humeral section modulus is found to be approximately proportional to the mass of the bird. This relationship is used to evaluate the possible flight abilities of 19 extinct dinosaurs from Avialae, Dromaeosauridae, and Troodontidae. Though all the avialans could fly, only four dromaeosaurids (Microraptor gui, Graciliraptor lujiahunensis, Buitreraptor gonzalezorum, and Changyuraptor yangi) and one troodontid (Jianianhualong tengi) are found to have had humeri that were strong enough for bird-like flight. The humeri of the remaining dromaeosaurids and troodontids were too weak.

Allometric analysis sheds light on the systematics and ontogeny of anurognathid pterosaurs

ABSTRACT Anurognathids are a clade of non-pterodactyloid pterosaurs with generally conservative morphology, but specializations as insectivores. They are represented by a disparate collection of adult and juvenile specimens that range in wingspan from ∼0.24–1 m. There have been concerns about the extent to which ontogenetic variation might affect phylogenetic inference, and indeed how aspects of their ontogeny might relate to the distinctive anurognathid adult morphology. Here we perform allometric analysis on 23 key skeletal dimensions in 13 anurognathid specimens. Our results show that all anurognathids share a common growth trajectory in most dimensions, and that ontogeny affects variation in a minority of characters commonly used in phylogenetic analysis. Excluding these ontogeny-related characters, a new taxon, Cascocauda rong gen. et sp. nov., is established. Based on the ontogenetically corrected dataset, our phylogenetic analysis supports Anurognathidae as the sister-group of Breviquartossa and reveals a general trend of tail reduction in the clade. Allometric growth suggests the anurognathid lifestyle remained consistent throughout ontogeny, maintaining a highly maneuverable flight style by near-isometric development in the wing, small prey (i.e., insects), by strong negative allometry in the skull, and an arboreal habit by strong positive allometry in the claws. This specialized lifestyle suggests retention of plesiomorphic juvenile traits into later ontogeny and facilitated morphological stasis by stabilizing selection during over 40 million years of evolution in the group.

Cartilage on the furculae of living birds and the extinct bird Confuciusornis: a preliminary analysis and implications for flight style inferences in Mesozoic birds

Cartilage on the furculae of living birds and the extinct bird Confuciusornis: a preliminary analysis and implications for flight style inferences in Mesozoic birds

Furcula Diversity Within the Avian Flight Apparatus

A major unknown in avian biology is the morphological basis of flight style diversity. While certain aspects of avian pectoral anatomy, such as an enlarged sternum and hypertrophied pectoral muscles, clearly relate to aerial locomotion in general, the finer details of form-function correspondence are less apparent. Nevertheless, furcula shape has been used to infer flight style in extinct avians because the furcula is the cranial origin of the largest flight muscle, m. pectoralis, in most extant birds. However, previous studies, which examined the furcula in isolation, indicate only a modest correlation between furcula shape and flight style. We hypothesized that the relationship of the furcula to flight style may be heavily mediated by other aspects of pectoral anatomy, particularly furcula orientation and flight muscle morphology. We used computed tomography and digital dissection techniques to collect in situ morphological data on a large (n=108) and diverse (21 orders) sample of formalin-fixed specimens. While some specimens required the addition of Lugol's iodine to visualize soft tissue, most specimens did not require contrast enhancement to permit bone and muscle reconstruction. We found moderate correspondence between flight style and furcula shape consistent with previous studies (e.g., soaring birds have flatter, more V-shaped furculae), however the magnitude of shape differences between flight style and taxonomic categories was smaller, perhaps due to different measurement techniques. Novel measures of furcular orientation in the pectoral girdle revealed that larger, slower-flapping birds tend to have more cranially-positioned furculae, which may relate to a greater need for wing protraction via m. pectoralis. Further, the centers-of-mass of the main pectoral muscles tend to be more cranial in large birds with more laterally-bowed furculae. In most measures, hummingbirds did not group with birds of similar mass or furcula shape, likely owing to their kinematically-unique flight style. Overall, our findings recommend caution in inferring flight style from furcula shape alone. Rather, furcula shape may be better viewed as part of a larger functional unit including the sternum, coracoids, and major flight muscles.

Osteohistology of the Scapulocoracoid of Confuciusornis and Preliminary Analysis of the Shoulder Joint in Aves

As key components of the tetrapod pectoral girdle, the scapula and coracoid have played a significant role in the evolution of forelimb locomotion among terrestrial vertebrates. The transition from a rigid fused scapulocoracoid in ancestral non-avian theropods to a presumably more flexible separated scapula-coracoid in early birds is considered to be one of the key morphological transitions related to the rapid refinement of flight. In most Mesozoic birds (e.g., Enantiornithes and Ornithuromorpha) and crown birds the scapula and coracoid are separate (unfused), with few exceptions (e.g., flightless paleognaths). In contrast, in Confuciusornis, a basal pygostylian from the Early Cretaceous Jehol Biota known from thousands of specimens, the scapula and coracoid remain plesiomorphically fused. This raises questions regarding the influence of shoulder girdle architecture on the early evolution and refinement of avian flight. The paravian scapula-coracoid joint has never previously been investigated using histology, and thus joint morphology has only been inferred superficially. In order to better understand the evolution of this joint in Mesozoic birds, we make the first histological study of the scapulocoracoid glenoid joint in Confuciusornis. The results demonstrate that the scapula and coracoid both consist of cancellous and compact bone, with both fibrolamellar and parallel-fibered structure. A thin layer of calcified cartilage is present on the glenoid fossa surface, representing remnants of the articular surface for the humerus. Both histology and computed tomography reveal that the scapulocoracoid of Confuciusornis is fully fused, forming a synostosis. Humeral histology suggests the studied individual was nearing completion of its first year of growth, suggesting the Confuciusornis scapulocoracoid fused before skeletal maturity was achieved, as in flightless paleognaths, whereas in the plesiomorphic condition fusion occurs late in ontogeny. We hypothesize the fused scapulocoracoid of Confuciusornis is secondarily evolved and suggest the primary factor responsible for this morphology may have been a decrease in mechanical stimulation at the glenoid of Confuciusornis relative to other volant birds, linked to the unique flight style of this taxon. Further investigation into the histology of the glenoid joint in other Mesozoic paravians and extant birds will help to clarify the morphological transition of the scapula-coracoid joint in early avian evolution.