Cross sectional geometry of the forelimb skeleton and flight mode in pelecaniform birds

Avian wing elements have been shown to experience both dorsoventral bending and torsional loads during flapping flight. However, not all birds use continuous flapping as a primary flight strategy. The pelecaniforms exhibit extraordinary diversity in flight mode, utilizing flapping, flap‐gliding, and soaring. Here we (1) characterize the cross‐sectional geometry of the three main wing bone (humerus, ulna, carpometacarpus), (2) use elements of beam theory to estimate resistance to loading, and (3) examine patterns of variation in hypothesized loading resistance relative to flight and diving mode in 16 species of pelecaniform birds. Patterns emerge that are common to all species, as well as some characteristics that are flight‐ and diving‐mode specific. In all birds examined, the distal most wing segment (carpometacarpus) is the most elliptical (relatively high I_max/I_min) at mid‐shaft, suggesting a shape optimized to resist bending loads in a dorsoventral direction. As primary flight feathers attach at an oblique angle relative to the long axis of the carpometacarpus, they are likely responsible for inducing bending of this element during flight. Moreover, among flight modes examined the flapping group (cormorants) exhibits more elliptical humeri and carpometacarpi than other flight modes, perhaps pertaining to the higher frequency of bending loads in these elements. The soaring birds (pelicans and gannets) exhibit wing elements with near‐circular cross‐sections and higher polar moments of area than in the flap and flap‐gliding birds, suggesting shapes optimized to offer increased resistance to torsional loads. This analysis of cross‐sectional geometry has enhanced our interpretation of how the wing elements are being loaded and ultimately how they are being used during normal activities. J. Morphol., 2011. © 2011 Wiley‐Liss,Inc.     

Sexual dimorphism in wing beat frequency in relation to eye span in stalk‐eyed flies (Diopsidae)

Although male ornaments may provide benefits to individuals bearing them, such structures may also entail fitness costs. Selection should favour aspects of the phenotype that act to reduce such costs, yet such compensatory traits are often ignored in studies of sexual selection. If a male ornament increases predation risk via reduced locomotor performance, then there may be selection for changes in morphological traits to compensate for behavioural or biomechanical changes in how individuals use their morphology (or both). We took a comparative approach aiming to test whether changes in wing beat frequency are evolutionarily correlated with increases in male ornamentation across stalk‐eyed fly species. Previous studies have shown that increased male eye span is evolutionarily correlated with increased wing size; thus, we tested whether there is additional compensation via increases in size‐adjusted wing beat frequency. The results obtained revealed that relative wing beat frequency is negatively related to relative eye span in males, and sexual dimorphism in wing beat frequency is negatively related to dimorphism in eye span. These findings, in addition to our finding that eye span dimorphism is positively related to aspect ratio dimorphism, suggest that male stalk‐eyed flies compensate primarily by increasing wing size and shape, which may then have resulted in the subsequent evolutionary reduction in wing beat frequency. Thus, exaggerated ornaments can result in evolutionary modifications in wing morphology, which in turn lead to adjustments in flapping kinematics, illustrating the tight envelope of trade‐offs when compensating for exaggerated ornaments. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 670–679.     

Phylogenetic clustering of wingbeat frequency and flight‐associated morphometrics across insect orders

Wingbeat frequency in insects is an important variable in aerodynamic and energetic analyses of insect flight and often is studied on a family‐ or species‐level basis. Meta‐analyses of these studies report order‐level patterns suggesting that flight strategy is moderately well conserved phylogenetically. Studies incorporated into these meta‐analyses, however, use variable methodologies across different temperatures, which may confound results and phylogenetic patterns. In the present study, a high‐speed camera is used to measure wingbeat frequency in a wide variety of species (n = 102) under controlled conditions aiming (i) to determine the validity of previous meta‐analyses showing phylogenetic clustering of flight strategy and (ii) to identify new evolutionary patterns between wingbeat frequency, body mass, wing area, wing length and wing loading at the order level. All flight‐associated morphometrics significantly affect wingbeat frequency. Linear models show that wing area explains the most amount of variation in wingbeat frequency (r² = 0.59, P ≤ 0.001), whereas body mass explains the least (r² = 0.09, P ≤ 0.01). A multiple regression model incorporating both body mass and wing area is the best overall predictor of wingbeat frequency (r² = 0.84, P ≤ 0.001). Order‐level phylogenetic patterns across relationships are consistent with previous studies. Thus, the present study provides experimental validation of previous meta‐analyses and provides new insights into phylogenetically conserved flight strategies across insect orders.     

Flight mode affects allometry of migration range in birds

Billions of birds migrate to exploit seasonally available resources. The ranges of migration vary greatly among species, but the underlying mechanisms are poorly understood. I hypothesise that flight mode (flapping or soaring) and body mass affect migration range through their influence on flight energetics. Here, I compiled the tracks of migratory birds (196 species, weighing 12–10 350 g) recorded by electronic tags in the last few decades. In flapping birds, migration ranges decreased with body mass, as predicted from rapidly increasing flight cost with increasing body mass. The species with higher aspect ratio and lower wing loading had larger migration ranges. In soaring birds, migration ranges were mass‐independent and larger than those of flapping birds, reflecting their low flight costs irrespective of body mass. This study demonstrates that many animal‐tracking studies are now available to explore the general patterns and the underlying mechanisms of animal migration.     

Morphological and kinematic basis of the hummingbird flight stroke: scaling of flight muscle transmission ratio

Hummingbirds (Trochilidae) are widely known for their insect-like flight strokes characterized by high wing beat frequency, small muscle strains and a highly supinated wing orientation during upstroke that allows for lift production in both halves of the stroke cycle. Here, we show that hummingbirds achieve these functional traits within the limits imposed by a vertebrate endoskeleton and muscle physiology by accentuating a wing inversion mechanism found in other birds and using long-axis rotational movement of the humerus. In hummingbirds, long-axis rotation of the humerus creates additional wing translational movement, supplementing that produced by the humeral elevation and depression movements of a typical avian flight stroke. This adaptation increases the wing-to-muscle-transmission ratio, and is emblematic of a widespread scaling trend among flying animals whereby wing-to-muscle-transmission ratio varies inversely with mass, allowing animals of vastly different sizes to accommodate aerodynamic, biomechanical and physiological constraints on muscle-powered flapping flight.     

Exploring the relationship between flapping behaviour and accelerometer signal during ascending flight,and a new approach to calibration

We understand little about the energetic costs of flight in free-ranging birds, in part because current techniques for estimating flight energetics in the wild are limited. Accelerometry is known to estimate energy expenditure through body movement in terrestrial animals, once calibrated using a treadmill with chamber respirometry. The flight equivalent, a wind tunnel with mask respirometry, is particularly difficult to instigate, and has not been applied to calibrate accelerometry. We take the first steps in exploring a novel method for calibrating accelerometers with flight energy expenditure. We collected accelerometry data for Harris's Hawks Parabuteo unicinctus flying to varying heights up to 4.1 m over a small horizontal distance; the mechanical energy expended to gain height can be estimated from physical first principles. The relationship between accelerometry and mechanical energy expenditure was strong, and while a simple wing flapping model confirmed that accelerometry is sensitive to both changes in wing beat amplitude and frequency, the relationship was explained predominately by changes in wing beat frequency, and less so by changes in amplitude. Our study provides initial, positive evidence that accelerometry can be calibrated with body power using climbing flights, potentially providing a basis for estimating flapping flight metabolic rate at least in situations of altitude gain.     

Skipping flights in Ypthima butterflies (Lepidoptera: Nymphalidae)

The skipping flight patterns of three species of Ypthima (Lepidoptera: Nymphalidae) were analyzed using high‐speed video recordings to clarify how wings move and how driving forces are produced. All three species showed a flight pattern that includes a pause that accounts for about 50% of a flap cycle when their wings completely close after each upstroke. The observed pause causes the “skipping” flight trajectory based on the clap–fling mechanism. Pause duration was correlated with upstroke wing motion, suggesting the contribution of the latter to a long pause duration. This is also supported by the temporal relationship between the wing and body motions. The aerodynamic power necessary for the pause flight was calculated for the three species.     

Precocial development of locomotor performance in a ground-dwelling bird (Alectoris chukar): negotiating a three-dimensional terrestrial environment

Developing animals are particularly vulnerable to predation. Hence, precocial young of many taxa develop predator escape performance that rivals that of adults. Ontogenetically unique among vertebrates, birds transition from hind limb to forelimb dependence for escape behaviours, so developmental investment for immediate gains in running performance may impair flight performance later. Here, in a three-dimensional kinematic study of developing birds performing pre-flight flapping locomotor behaviours, wing-assisted incline running (WAIR) and a newly described behaviour, controlled flapping descent (CFD), we define three stages of locomotor ontogeny in a model gallinaceous bird (Alectoris chukar). In stage I (1–7 days post-hatching (dph)) birds crawl quadrupedally during ascents, and their flapping fails to reduce their acceleration during aerial descents. Stage II (8–19 dph) birds use symmetric wing beats during WAIR, and in CFD significantly reduce acceleration while controlling body pitch to land on their feet. In stage III (20 dph to adults), birds are capable of vertical WAIR and level-powered flight. In contrast to altricial species, which first fly when nearly at adult mass, we show that in a precocial bird the major requirements for flight (i.e. high power output, wing control and wing size) convene by around 8 dph (at ca 5% of adult mass) and yield significant gains in escape performance: immature chukars can fly by 20 dph, at only about 12 per cent of adult mass.     

Locust flight initiation: a comparison of normal and artificial release

Flight initiation was analysed in the migratory locust, Locusta migratoria L. using conventional and high‐speed video systems. Flight was initiated by three methods: normal jump, free fall and controlled catapult. Parameters evaluated were time from release to wing‐opening, body angle, speed, height gain, wing‐opening, initial wing‐beat frequency. Fastest wing‐opening occurred following a normal jump. A catapult device allowed manipulation of the launching parameters: speed and angles at launching. It appeared that in an artificially catapulted start there was a minimum speed (v > 0.75 m/s) required to initiate flight. However, under free‐fall conditions a mean speed of v = 0.6 m/s at wing‐opening was observed. When the different parameters of the controlled catapult start were equal to those for normal jump then the time to wing‐opening was found to be extended for the catapult launch. However, other parameters were not affected, occasionally even a ‘kick in air’ was observed. The catapult launches indicated that within about three wing‐beat cycles the animals showed active flight, with positive lift and constant or increasing speed, compared to a ballistic trajectory. Our results indicate that a controlled catapult device will prove useful to the study of sensory and central processes underlying free flight initiation.     

PRIZES FOR ESSAYS

Mendelsohn, J. M., Kemp, A. C, Biggs, H. C, Biggs, R. &; Brown, C.J. 1989. Wing areas, wing loadings and wing spans of 66 species of African raptors. Ostrich 60:35-42.

The paper provides data on the wing areas of 855 birds of 66 species and wing spans of 918 individuals of 58 species of African raptors. Two measures of wing loading were calculated for those individuals that were weighed. Wing, secondary and ulnar lengths are used to derive an index of wing area which explains 98,8% of the variation in the mean wing areas of 46 species. A regression, derived from this relationship, can be used to estimate wing areas from the three linear measurements, all of which can be taken on museum specimens. Similarly, an index, using the sum of wing and ulnar lengths accounts for 99,5% of the variation in the mean wing spans of 36 species. The wing dimensions of males and females, and adults and juveniles are compared in several species. For those species with adequate samples of measurements of wing area, body mass and wing span, the cost of flapping flight can be estimated with confidence.     

Avoidance of headwinds or exploitation of ground effect—why do birds fly low?

ABSTRACT Birds often fly close to the ground or water. Wind shear theory predicts that wind speeds decline with proximity to the substratum, so birds might be expected to fly lower when flying upwind than when flying downwind. We tested this prediction and found that the wind shear equation is valid at heights below 4 m, with wind speed over a smooth surface ～40% lower at a height of 0.08 m than at 4 m. Birds that fly close enough to smooth substrata can also benefit energetically from ground effect, where vortices generated by their flight interact with the ground or water. This suggests that birds should use ground effect more when flying upwind than when flying downwind. We determined the percent time spent flying in ground effect by 21 species of passerine and non‐passerine birds flying in sheltered coastal aquatic and nearby terrestrial areas of County Cork, Ireland. We found that use of ground effect was uncommon for passerines, but common for a variety of non‐passerine waterbirds. However, phylogenetic analysis indicates no linkage between phylogeny and incidence of ground effect use and it is probable that incidence of use is determined by ecology rather than phylogeny. Great Cormorants (Phalacrocorax carbo) used ground effect most frequently over water (59.4% of time in flight). Over land, Barn Swallows (Hirundo rustica) used ground effect most often (19.8% of time). Phylogenetic contrasts regression analysis showed no significant relationship between use of ground effect and either wing aspect ratio or wing loading for 18 of our focal species, though simple linear regression analysis indicated that birds with greater wing loading used ground effect slightly (but significantly) more often. We found that 95% of Great Cormorants flying upwind used ground effect whereas only 35% did so when flying downwind. Few Black‐headed Gulls (Chroicocephalus ridibundus) used ground effect (probably because they fly high to locate prey), but still showed greater use when flying upwind (25%) than downwind (2.5%). When flying upwind in ground effect at the wind speeds encountered in our study, the velocity for minimum power (V_mp) for Great Cormorants was exceeded, suggesting theoretical benefits of about 14.3%. Our study indicates that several species exploit both wind shear and ground effect to minimize energy expenditure during commuting and foraging, but that others do not, because of either complexity of habitat morphology or the demands of their foraging ecology.     

Metabolic costs of avian flight in relation to flight velocity: a study in Rose Coloured Starlings (Sturnus roseus, Linnaeus)

The metabolic costs of flight at a natural range of speeds were investigated in Rose Coloured Starlings (Sturnus roseus, Linnaeus) using doubly labelled water. Eight birds flew repeatedly and unrestrained for bouts of 6 h at speeds from 9 to 14 m s⁻¹ in a low-turbulence wind tunnel, corresponding to travel distances between 200 and 300 km, respectively. This represents the widest speed range where we could obtain voluntarily sustained flights. From a subset of these flights, data on the wing beat frequency (WBF) and intermittent flight behaviour were obtained. Over the range of speeds that were tested, flight costs did not change with velocity and were on an average 8.17±0.64 W or 114 W kg⁻¹. Body mass was the only parameter with a significant (positive) effect on flight costs, which can be described as EE_f=0.741 M ^0.554. WBF changed slightly with speed, but correlated better with body mass. Birds showed both types of intermittent flight, undulating and bounding, but their frequencies did not systematically change with flight speed.     

Seasonal differences in energy requirements of Garden Warblers Sylvia borin migrating across the Sahara desert

The Sahara desert acts as an ecological barrier for billions of passerine birds on their way to and from their African wintering areas. The Garden Warbler Sylvia borin is one of the most common migrants involved. We used body mass of this species from Greece in autumn and spring to simulate the desert crossing and to assess how body mass relates to fuel requirement. The flight range estimates were adjusted to the seasonal extent of the desert, 2200 km in autumn and about 2800 km in spring. In autumn, with an average fuel load of about 100% of body mass without fuel, birds were not able to cross the desert in still air, but northerly winds prevail during September and with the average wind assistance only one in 14 was predicted to fail to make the crossing. Body mass data from spring, after the desert crossing, was used to estimate departure body mass from south of the desert. The average wind assistance in spring is close to zero and departure body mass of the average bird arriving at Antikythira, a small Greek island, under such conditions was estimated to be 34.6 g, which corresponded to a fuel load of 116%. Calculations based on 1% body mass loss per hour of flight showed slightly larger body mass loss than that calculated from flight range estimates. The results suggest that passerine birds about to cross the eastern part of the Sahara desert need to attain a larger fuel load in spring than in autumn.     

Flight modes in migrating European bee-eaters: heart rate may indicate low metabolic rate during soaring and gliding

Background

Many avian species soar and glide over land. Evidence from large birds (m _b>0.9 kg) suggests that soaring-gliding is considerably cheaper in terms of energy than flapping flight, and costs about two to three times the basal metabolic rate (BMR). Yet, soaring-gliding is considered unfavorable for small birds because migration speed in small birds during soaring-gliding is believed to be lower than that of flapping flight. Nevertheless, several small bird species routinely soar and glide.

Methodology/Principal Findings

To estimate the energetic cost of soaring-gliding flight in small birds, we measured heart beat frequencies of free-ranging migrating European bee-eaters (Merops apiaster, m _b∼55 g) using radio telemetry, and established the relationship between heart beat frequency and metabolic rate (by indirect calorimetry) in the laboratory. Heart beat frequency during sustained soaring-gliding was 2.2 to 2.5 times lower than during flapping flight, but similar to, and not significantly different from, that measured in resting birds. We estimated that soaring-gliding metabolic rate of European bee-eaters is about twice their basal metabolic rate (BMR), which is similar to the value estimated in the black-browed albatross Thalassarche (previously Diomedea) melanophrys, m _b∼4 kg). We found that soaring-gliding migration speed is not significantly different from flapping migration speed.

Conclusions/Significance

We found no evidence that soaring-gliding speed is slower than flapping flight in bee-eaters, contradicting earlier estimates that implied a migration speed penalty for using soaring-gliding rather than flapping flight. Moreover, we suggest that small birds soar and glide during migration, breeding, dispersal, and other stages in their annual cycle because it may entail a low energy cost of transport. We propose that the energy cost of soaring-gliding may be proportional to BMR regardless of bird size, as theoretically deduced by earlier studies.     

Greater energy stores enable flightless moulting geese to increase resting behaviour

Many species of waterfowl undergo a post‐breeding simultaneous flight feather moult (wing moult) which renders them flightless and vulnerable to predation for up to 4 weeks. Here we present an analysis of the correlations between individual time‐budgets and body mass states in 13 captive Barnacle Geese Branta leucopsis throughout an entire wing moult. The daily percentage of time spent resting was positively correlated with initial body mass at the start of wing moult. Behaviour of individual birds during wing moult is dependent on initial physiological state, which may in turn be dependent on foraging ability; the storage of energy before the start of wing moult will help birds to reduce exposure to the dangers of predation.     

The gliding speed of migrating birds: slow and safe or fast and risky?

Aerodynamic theory postulates that gliding airspeed, a major flight performance component for soaring avian migrants, scales with bird size and wing morphology. We tested this prediction, and the role of gliding altitude and soaring conditions, using atmospheric simulations and radar tracks of 1346 birds from 12 species. Gliding airspeed did not scale with bird size and wing morphology, and unexpectedly converged to a narrow range. To explain this discrepancy, we propose that soaring‐gliding birds adjust their gliding airspeed according to the risk of grounding or switching to costly flapping flight. Introducing the Risk Aversion Flight Index (RAFI, the ratio of actual to theoretical risk‐averse gliding airspeed), we found that inter‐ and intraspecific variation in RAFI positively correlated with wing loading, and negatively correlated with convective thermal conditions and gliding altitude, respectively. We propose that risk‐sensitive behaviour modulates the evolution (morphology) and ecology (response to environmental conditions) of bird soaring flight.     

Wing size but not wing shape is related to migratory behavior in a soaring bird

Both wing size and wing shape affect the flight abilities of birds. Intra and inter‐specific studies have revealed a pattern where high aspect ratio and low wing loading favour migratory behaviour. This, however, have not been studied in soaring migrants. We assessed the relationship between the wing size and shape and the characteristics of the migratory habits of the turkey vulture Cathartes aura, an obligate soaring migrant. We compared wing size and shape with migration strategy among three fully migratory, one partially migratory and one non‐migratory (resident) population distributed across the American continent. We calculated the aspect ratio and wing loading using wing tracings to characterize the wing morphology. We used satellite‐tracking data from the migratory populations to calculate distance, duration, speed and altitude during migration. Wing loading, but not aspect ratio, differed among the populations, segregating the resident population from the completely migratory ones. Unlike what has been reported in species using flapping flight during migration, the migratory flight parameters of turkey vultures were not related to the aspect ratio. By contrast, wing loading was related to most flight parameters. Birds with lower wing loading flew farther, faster, and higher during their longer journeys. Our results suggest that wing morphology in this soaring species enables lower‐cost flight, through low wing‐loading, and that differences in the relative sizes of wings may increase extra savings during migration. The possibility that wing shape is influenced by foraging as well as migratory flight is discussed. We conclude that flight efficiency may be improved through different morphological adaptations in birds with different flight mechanisms.     

Aerodynamic Interactions Between Wing and Body of a Model Insect in Forward Flight and Maneuvers

The aerodynamic interactions between the body and the wings of a model insect in forward flight and maneuvers are studied using the method of numerically solving the Navier-Stokes equations over moving overset grids. Three cases are considered, including a complete insect, wing pair only and body only. By comparing the results of these cases, the interaction effect between the body and the wing pair can be identified. The changes in the force and moment coefficients of the wing pair due to the presence of the body are less than 4.5% of the mean vertical force coefficient of the model insect; the changes in the aerodynamic force coefficients of the body due to the presence of the wings are less than 5.0% of the mean vertical force coefficient of the model insect. The results of this paper indicate that in studying the aerodynamics and flight dynamics of a flapping insect in forward flight or maneuver, separately computing (or measuring) the aerodynamic forces and moments on the wing pair and on the body could be a good approximation.     

Wing shape,wing size,and sexual dimorphism in eye‐span in stalk‐eyed flies (Diopsidae)

The eyes of stalk‐eyed flies (Diopsidae) are positioned at the end of rigid peduncles (‘stalks’) protruding laterally from the head. Eye‐stalk length varies within the family and, in some species, varies between males and females. Larger eye‐stalks in males result from sexual selection for longer stalks, a trait that increases male reproductive success. In the present study, we examined whether an increase in eye‐stalk length results in an adjustment of wing size and shape to deal with the burden of bearing an exaggerated ‘ornament’. We compared wing morphology among ten species of stalk‐eyed flies that differ in eye‐span and the degree of sexual dimorphism. Mass‐specific wing length differed between males and females in seven out of the ten species. Nondimensional wing shape parameters differed between the species (P < 0.001), but mostly did not differ between males and females of the same species. Dimorphism in eye‐span closely correlated with dimorphism in wing length (r = 0.89, P < 0.001) and the correlation remained significant (r = 0.81, P = 0.006) after correcting for phylogenetic relationships. Once corrected for phylogenetic relatedness, the mass‐specific wing length of males (but not females) was weakly correlated with mass‐specific eye‐span (r = 0.66, P = 0.042). We propose that the observed proportional increase in wing length associated with increased eye‐span can facilitate aerial manoeuverability, which would otherwise be handicapped by the elevated moment of inertia imposed by the wider head. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 860–871.     

Flight initiation distance and escape behavior in the black redstart (Phoenicurus ochruros)

There are many anti‐predatory escape strategies in animals. A well‐established method to assess escape behavior is the flight initiation distance (FID), which is the distance between prey and predator at which an animal flees. Previous studies in various species throughout the animal kingdom have shown that group size, urbanization, and distance to refuge and body mass affect FID. In most species, FID increases if body mass, group size or distance to refuge decreases. However, how age and sexual dimorphism affect FID is rather unknown. Here, we assess the escape behavior and FID of the black redstart (Phoenicurus ochruros), a small turdid passerine. When approached by a human, males initiated flights later, that is allowing a closer approach than females. Males of this species are more conspicuous, and therefore, may exhibit aposematism to deter potential predators or are less fearful than females. Additionally, juveniles fled at shorter distances and fled to lower heights than adults. Lastly, concerning escape strategy, black redstarts, unless other passerine birds, fled less often into cover, but rather onto open or elevated spots. Black redstarts are especially prone to predation by ambushing predators that might hide in cover. Hence, this species most likely has a higher chance of escaping by fleeing to an open spot rather than to a potentially risky cover.