Small deviations in kinematics and body form dictate muscle performances in the finely tuned avian downstroke.

Avian takeoff requires peak pectoralis muscle power to generate sufficient aerodynamic force during the downstroke. Subsequently, the much smaller supracoracoideus recovers the wing during the upstroke. How the pectoralis work loop is tuned to power flight is unclear. We integrate wingbeat-resolved muscle, kinematic, and aerodynamic recordings in vivo with a new mathematical model to disentangle how the pectoralis muscle overcomes wing inertia and generates aerodynamic force during takeoff in doves. Doves reduce the angle of attack of their wing mid-downstroke to efficiently generate aerodynamic force, resulting in an aerodynamic power dip, that allows transferring excess pectoralis power into tensioning the supracoracoideus tendon to assist the upstroke-improving the pectoralis work loop efficiency simultaneously. Integrating extant bird data, our model shows how the pectoralis of birds with faster wingtip speed need to generate proportionally more power. Finally, birds with disproportionally larger wing inertia need to activate the pectoralis earlier to tune their downstroke.

A wing-assisted incline running exercise regime during rearing increases initial flight velocity during descent in adult white- and brown-feathered laying hens.

Domestic laying hens rely primarily on their hindlimbs for terrestrial locomotion. Although they perform flapping flight, they appear to use maximal power during descent and thus may lack control for maneuvering and avoiding injuries on landing. This in turn may result in injury in open rearing systems. Wing-assisted incline running (WAIR) requires a bird to use its wings to assist the hindlimbs during climbing of an incline, and training in WAIR may therefore provide a useful method to increase a hen's power reserve and control for flight. We subjected hens to an exercise regimen involving inclines to induce WAIR for 16 wk during rearing. We then measured wing and body kinematics during aerial descent from a 155 cm platform. We hypothesized that birds reared with exercise would be better able to modulate their wing and body kinematics for making slower, more-controlled descent and landing. Brown-feathered birds exhibited greater wing beat frequencies than white-feathered birds, which is consistent with the higher wing loading of brown-feathered birds and WAIR-trained birds exhibited greater initial flight velocities compared to control birds. This may indicate that WAIR training provided an improved capacity to modulate flight velocity and strengthen the leg muscles. Providing incline exercises during rearing may therefore improve welfare for adult laying hens as greater initial flight velocity should reduce the power required for supporting body weight in the air and allow a hen to direct her excess power toward maneuvering.

Reduction of wing area affects estimated stress in the primary flight muscles of chickens.

In flying birds, the pectoralis (PECT) and supracoracoideus (SUPRA) generate most of the power required for flight, while the wing feathers create the aerodynamic forces. However, in domestic laying hens, little is known about the architectural properties of these muscles and the forces the wings produce. As housing space increases for commercial laying hens, understanding these properties is important for assuring safe locomotion. We tested the effects of wing area loss on mass, physiological cross-sectional area (PCSA), and estimated muscle stress (EMS) of the PECT and SUPRA in white-feathered laying hens. Treatments included Unclipped (N = 18), Half-Clipped with primaries removed (N = 18) and Fully-Clipped with the primaries and secondaries removed (N = 18). The mass and PCSA of the PECT and SUPRA did not vary significantly with treatment. Thus, laying hen muscle anatomy may be relatively resistant to changes in external wing morphology. We observed significant differences in EMS among treatments, as Unclipped birds exhibited the greatest EMS. This suggests that intact wings provide the greatest stimulus of external force for the primary flight muscles.

Hummingbirds use wing inertial effects to improve manoeuvrability.

Hummingbirds outperform other birds in terms of aerial agility at low flight speeds. To reveal the key mechanisms that enable such unparalleled agility, we reconstructed body and wing motion of hummingbird escape manoeuvres from high-speed videos; then, we performed computational fluid dynamics modelling and flight mechanics analysis, in which the time-dependent forces within each wingbeat were resolved. We found that the birds may use the inertia of their wings to achieve peak body rotational acceleration around wing reversal when the aerodynamic forces were small. The aerodynamic forces instead counteracted the reversed inertial forces at a different wingbeat phase, thereby stabilizing the body from inertial oscillations, or they could become dominant and provide additional rotational acceleration. Our results suggest such an inertial steering mechanism was present for all four hummingbird species considered, and it was used by the birds for both pitch-up and roll accelerations. The combined inertial steering and aerodynamic mechanisms made it possible for the hummingbirds to generate instantaneous body acceleration at any phase of a wingbeat, and this feature is probably the key to understanding the unique dexterity distinguishing hummingbirds from other small-size flyers that solely rely on aerodynamics for manoeuvering.

Thermal acclimation in a non-migratory songbird occurs via changes to thermogenic capacity, but not conductance.

Thermoregulatory performance can be modified through changes in various subordinate traits, but the rate and magnitude of change in these traits is poorly understood. We investigated flexibility in traits that affect thermal balance between black-capped chickadees (Poecile atricapillus) acclimated for 6 weeks to cold (-5°C) or control (23°C) environments (n=7 per treatment). We made repeated measurements of basal and summit metabolic rates via flow-through respirometry and of body composition using quantitative magnetic resonance of live birds. At the end of the acclimation period, we measured thermal conductance of the combined feathers and skins. Cold-acclimated birds had a higher summit metabolic rate, reflecting a greater capacity for endogenous heat generation, and an increased lean mass. However, birds did not alter their thermal conductance. These results suggest that chickadees respond to cold stress by increasing their capacity for heat production rather than increasing heat retention, an energetically expensive strategy.

Active wing-pitching mechanism in hummingbird escape maneuvers.

Previous studies suggested that wing pitching, i.e. the wing rotation around its long axis, of insects and hummingbirds is primarily driven by an inertial effect associated with stroke deceleration and acceleration of the wings and is thus passive. Here we considered the rapid escape maneuver of hummingbirds who were initially hovering but then startled by the frontal approach of a looming object. During the maneuver, the hummingbirds substantially changed their wingbeat frequency, wing trajectory, and other kinematic parameters. Using wing kinematics reconstructed from high-speed videos and computational fluid dynamics modeling, we found that although the same inertial effect drove the wing flipping at stroke reversal as in hovering, significant power input was required to pitch up the wings during downstroke to enhance aerodynamic force production; furthermore, the net power input could be positive for wing pitching in a complete wingbeat cycle. Therefore, our study suggests that an active mechanism was present during the maneuver to drive wing pitching. In addition to the powered pitching, wing deviation during upstroke required twice as much power as hovering to move the wings caudally when the birds redirected the aerodynamic force vector for escaping. These findings were consistent with our hypothesis that enhanced muscle recruitment is essential for hummingbirds' escape maneuvers.

The evolution of nest site use and nest architecture in modern birds and their ancestors.

The evolution of nest site use and nest architecture in the non-avian ancestors of birds remains poorly understood because nest structures do not preserve well as fossils. Nevertheless, the evidence suggests that the earliest dinosaurs probably buried eggs below ground and covered them with soil so that heat from the substrate fuelled embryo development, while some later dinosaurs laid partially exposed clutches where adults incubated them and protected them from predators and parasites. The nests of euornithine birds-the precursors to modern birds-were probably partially open and the neornithine birds-or modern birds-were probably the first to build fully exposed nests. The shift towards smaller, open cup nests has been accompanied by shifts in reproductive traits, with female birds having one functioning ovary in contrast to the two ovaries of crocodilians and many non-avian dinosaurs. The evolutionary trend among extant birds and their ancestors has been toward the evolution of greater cognitive abilities to construct in a wider diversity of sites and providing more care for significantly fewer, increasingly altricial, offspring. The highly derived passerines reflect this pattern with many species building small, architecturally complex nests in open sites and investing significant care into altricial young. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Born without a Silver Spoon: A Review of the Causes and Consequences of Adversity during Early Life.

A huge amount of research attention has focused on the evolution of life histories, but most research focuses on dominant individuals that acquire a disproportionate level of reproductive success, while the life histories and reproductive tactics of subordinate individuals have received less attention. Here, we review the links between early life adversity and performance during adulthood in birds, and highlight instances in which subordinate individuals outperform dominant conspecifics. Subordinate individuals are those from broods raised under high risk of predation, with low availability of food, and/or with many parasites. Meanwhile, the broods of many species hatch or are born asynchronously and mitigation of the asynchrony is generally lacking from variation in maternal effects such as egg size and hormone deposition or genetic effects such as offspring sex or parentage. Subordinate individuals employ patterns of differential growth to attempt to mitigate the adversity they experience during early life, yet they overwhelmingly fail to overcome their initial handicap. In terms of surviving through to adulthood, subordinate individuals employ other "suboptimal" tactics, such as adaptively timing foraging behaviors to avoid dominant individuals. During adulthood, meanwhile, subordinate individuals rely on "suboptimal" tactics, such as adaptive dispersal behaviors and competing for partners at optimal times, because they represent the best options available to them to acquire copulations whenever possible. We conclude that there is a gap in knowledge for direct links between early life adversity and subordination during adulthood, meaning that further research should test for links. There are instances, however, where subordinate individuals employ "suboptimal" tactics that allow them to outperform dominant conspecifics during adulthood.

Biomechanics of landing in injured and uninjured chickens and the role of meloxicam.

Birds use their legs and wings when transitioning from aerial to ground locomotion during landing. To improve our understanding of the effects of footpad dermatitis (FPD) and keel bone fracture (KBF) upon landing biomechanics in laying hens, we measured ground-reaction forces generated by hens (n = 37) as they landed on force plates (Bertec Corporation, Columbus, OH) from a 30 cm drop or 170 cm jump in a single-blinded placebo-controlled trial using a cross-over design where birds received an anti-inflammatory (meloxicam, 5 mg/kg body mass) or placebo treatment beforehand. We used generalized linear mixed models to test for effects of health status, treatment and their interaction on landing velocity (m/s), maximum resultant force (N), and impulse (force integrated with respect to time [N s]). Birds with FPD and KBF tended to show divergent alterations to their landing biomechanics when landing from a 30 cm drop, with a higher landing velocity and maximum force in KBF compared to FPD birds, potentially indicative of efforts to either reduce the use of their wings or impacts on inflamed footpads. In contrast, at 170 cm jumps fewer differences between birds of different health statuses were observed likely due to laying hens being poor flyers already at their maximum power output. Our results indicate that orthopedic injuries, apart from being welfare issues on their own, may have subtle influences on bird mobility through altered landing biomechanics that should be considered.

Free-living Allen's hummingbirds (Selasphorus sasin) rarely use torpor while nesting.

For reproducing animals, maintaining energy balance despite thermoregulatory challenges is important for surviving and successfully raising offspring. This is especially apparent in small endotherms that exhibit high mass-specific metabolic rates and live in unpredictable environments. Many of these animals use torpor, substantially reducing their metabolic rate and often body temperature to cope with high energetic demands during non-foraging periods. In birds, when the incubating parent uses torpor, the lowered temperatures that thermally sensitive offspring experience could delay development or increase mortality risk. We used thermal imaging to noninvasively explore how nesting female hummingbirds sustain their own energy balance while effectively incubating their eggs and brooding their chicks. We located 67 active Allen's hummingbird (Selasphorus sasin) nests in Los Angeles, California and recorded nightly time-lapse thermal images at 14 of these nests for 108 nights using thermal cameras. We found that nesting females usually avoided entering torpor, with one bird entering deep torpor on two nights (2% of nights), and two other birds possibly using shallow torpor on three nights (3% of nights). We also modeled nightly energetic requirements of a bird experiencing nest temperatures vs. ambient temperature and using torpor or remaining normothermic, using data from similarly-sized broad-billed hummingbirds. Overall, we suggest that the warm environment of the nest, and possibly shallow torpor, help brooding female hummingbirds reduce their own energy requirements while prioritizing the energetic demands of their offspring.

Does wing use and disuse cause behavioural and musculoskeletal changes in domestic fowl (Gallus gallus domesticus)?

Domestic chickens may live in environments which restrict wing muscle usage. Notably, reduced wing activity and accompanying muscle weakness are hypothesized risk factors for keel bone fractures and deviations. We used radio-frequency identification (RFID) to measure duration spent at elevated resources (feeders, nest-boxes), ultrasonography to measure muscle thickness (breast and lower leg) changes, radiography and palpation to determine fractures and deviations, respectively, following no, partial (one-sided wing sling) and full (cage) immobilization in white- and brown-feathered birds. We hypothesized partially immobilized hens would reduce elevated resource usage and that both immobilization groups would show decreased pectoralis thickness (disuse) and increased prevalence of fractures and deviations. Elevated nest-box usage was 42% lower following five weeks of partial immobilization for brown-feathered hens but no change in resource usage in white-feathered birds was observed. Fully immobilized, white-feathered hens showed a 17% reduction in pectoralis thickness, while the brown-feathered counterparts showed no change. Lastly, fractures and deviations were not affected in either strain or form of wing immobilization; however, overall low numbers of birds presented with these issues. Altogether, this study shows a profound difference between white- and brown-feathered hens in response to wing immobilization and associated muscle physiology.

Musculoskeletal wing-actuation model of hummingbirds predicts diverse effects of primary flight muscles in hovering flight.

Hummingbirds have evolved to hover and manoeuvre with exceptional flight control. This is enabled by their musculoskeletal system that successfully exploits the agile motion of flapping wings. Here, we synthesize existing empirical and modelling data to generate novel hypotheses for principles of hummingbird wing actuation. These may help guide future experimental work and provide insights into the evolution and robotic emulation of hummingbird flight. We develop a functional model of the hummingbird musculoskeletal system, which predicts instantaneous, three-dimensional torque produced by primary (pectoralis and supracoracoideus) and combined secondary muscles. The model also predicts primary muscle contractile behaviour, including stress, strain, elasticity and work. Results suggest that the primary muscles (i.e. the flight 'engine') function as diverse effectors, as they do not simply power the stroke, but also actively deviate and pitch the wing with comparable actuation torque. The results also suggest that the secondary muscles produce controlled-tightening effects by acting against primary muscles in deviation and pitching. The diverse effects of the pectoralis are associated with the evolution of a comparatively enormous bicipital crest on the humerus.

Aerodynamics of avian flight.

Much of the awe that humans have for the flight of birds derives from our earthbound habits and our bias toward emphasizing visual cues for interpreting processes in the world. Although we move through it and breathe it, air is vastly less dense than our bodies, so it is fanciful to imagine moving our limbs in a manner that would enable us to support our weight in the air. Moreover, air is invisible to us unless we use special tools to reveal its flow patterns. As evidence of our visual bias, contemplate a strong wind. You probably form a mental image of leaves moving on tree branches, or dust swirling about in a tornado, in both cases, solids moving in response to the force of the wind rather than the essence of the wind itself.

Wing Kinematics and Unsteady Aerodynamics of a Hummingbird Pure Yawing Maneuver.

As one of few animals with the capability to execute agile yawing maneuvers, it is quite desirable to take inspiration from hummingbird flight aerodynamics. To understand the wing and body kinematics and associated aerodynamics of a hummingbird performing a free yawing maneuver, a crucial step in mimicking the biological motion in robotic systems, we paired accurate digital reconstruction techniques with high-fidelity computational fluid dynamics (CFD) simulations. Results of the body and wing kinematics reveal that to achieve the pure yaw maneuver, the hummingbird utilizes very little body pitching, rolling, vertical, or horizontal motion. Wing angle of incidence, stroke, and twist angles are found to be higher for the inner wing (IW) than the outer wing (OW). Unsteady aerodynamic calculations reveal that drag-based asymmetric force generation during the downstroke (DS) and upstroke (US) serves to control the speed of the turn, a characteristic that allows for great maneuvering precision. A dual-loop vortex formation during each half-stroke is found to contribute to asymmetric drag production. Wake analysis revealed that asymmetric wing kinematics led to leading-edge vortex strength differences of around 59% between the IW and OW. Finally, analysis of the role of wing flexibility revealed that flexibility is essential for generating the large torque necessary for completing the turn as well as producing sufficient lift for weight support.

High Wing-Loading Correlates with Dive Performance in Birds, Suggesting a Strategy to Reduce Buoyancy.

Diving birds are regarded as a classic example of morphological convergence. Divers tend to have small wings extending from rotund bodies, requiring many volant species to fly with rapid wingbeats, and rendering others flightless. The high wing-loading of diving birds is frequently associated with the challenge of using forelimbs adapted for flight for locomotion in a "draggier" fluid, but this does not explain why species that rely exclusively on their feet to dive should have relatively small wings, as well. Therefore, others have hypothesized that ecological factors shared by wing-propelled and foot-propelled diving birds drive the evolution of high wing-loading. Following a reexamination of the aquatic habits of birds, we tested between hypotheses seeking to explain high wing-loading in divers using new comparative data and phylogenetically informed analyses. We found little evidence that wing-propelled diving selects for small wings, as wing-propelled and foot-propelled species share similar wing-loadings. Instead, our results suggest that selection to reduce buoyancy has driven high wing-loading in divers, offering insights for the development of bird-like aquatic robots.

Wing-feather loss in white-feathered laying hens decreases pectoralis thickness but does not increase risk of keel bone fracture.

Feather loss in domestic chickens can occur due to wear and tear, disease or bird-to-bird pecking. Flight feather loss may decrease wing use, cause pectoral muscle loss and adversely impact the keel bone to which these muscles anchor. Feather loss and muscle weakness are hypothesized risk factors for keel bone fractures that are reported in up to 98% of chickens. We used ultrasound to measure changes in pectoral muscle thickness and X-rays to assess keel bone fracture prevalence following symmetric clipping of primary and secondary feathers in white- and brown-feathered birds. Four and six weeks after flight feather clipping, pectoralis thickness decreased by approximately 5%, while lower leg thickness increased by approximately 5% in white-feathered birds. This pectoralis thickness decrease may reflect wing disuse followed by muscle atrophy, while the increased leg thickness may reflect increased bipedal locomotion. The lack of effect on muscle thickness in brown-feathered hens was probably due to their decreased tendency for aerial locomotion. Finally, pectoralis thickness was not associated with keel bone fractures in either white- or brown-feathered birds. This suggests that the white-feathered strain was more sensitive to feather loss. Future prevention strategies should focus on birds most susceptible to muscle loss associated with flight feather damage.

Effects of clipping of flight feathers on resource use in Gallus gallus domesticus.

Ground-dwelling species of birds, such as domestic chickens (Gallus gallus domesticus), experience difficulties sustaining flight due to high wing loading. This limited flight ability may be exacerbated by loss of flight feathers that is prevalent among egg-laying chickens. Despite this, chickens housed in aviary style systems need to use flight to access essential resources stacked in vertical tiers. To understand the impact of flight feather loss on chickens' ability to access elevated resources, we clipped primary and secondary flight feathers for two hen strains (brown-feathered and white-feathered, n = 120), and recorded the time hens spent at elevated resources (feeders, nest-boxes). Results showed that flight feather clipping significantly reduced the percentage of time that hens spent at elevated resources compared to ground resources. When clipping both primary and secondary flight feathers, all hens exhibited greater than or equal to 38% reduction in time spent at elevated resources. When clipping only primary flight feathers, brown-feathered hens saw a greater than 50% reduction in time spent at elevated nest-boxes. Additionally, brown-feathered hens scarcely used the elevated feeder regardless of treatment. Clipping of flight feathers altered the amount of time hens spent at elevated resources, highlighting that distribution and accessibility of resources is an important consideration in commercial housing.

Multi-modal locomotor costs favor smaller males in a sexually dimorphic leaf-mimicking insect.

BACKGROUND: In most arthropods, adult females are larger than males, and male competition is a race to quickly locate and mate with scattered females (scramble competition polygyny). Variation in body size among males may confer advantages that depend on context. Smaller males may be favored due to more efficient locomotion leading to higher mobility during mate searching. Alternatively, larger males may benefit from increased speed and higher survivorship. While the relationship between male body size and mobility has been investigated in several systems, how different aspects of male body morphology specifically affect their locomotor performance in different contexts is often unclear. RESULTS: Using a combination of empirical measures of flight performance and modelling of body aerodynamics, we show that large body size impairs flight performance in male leaf insects (Phyllium philippinicum), a species where relatively small and skinny males fly through the canopy in search of large sedentary females. Smaller males were more agile in the air and ascended more rapidly during flight. Our models further predicted that variation in body shape would affect body lift and drag but suggested that flight costs may not explain the evolution of strong sexual dimorphism in body shape in this species. Finally, empirical measurements of substrate adhesion and subsequent modelling of landing impact forces suggested that smaller males had a lower risk of detaching from the substrates on which they walk and land. CONCLUSIONS: By showing that male body size impairs their flight and substrate adhesion performance, we provide support to the hypothesis that smaller scrambling males benefit from an increased locomotor performance and shed light on the evolution of sexual dimorphism in scramble competition mating systems.

Domestic egg-laying hens, Gallus gallus domesticus, do not modulate flapping flight performance in response to wing condition.

Wild birds modulate wing and whole-body kinematics to adjust their flight patterns and trajectories when wing loading increases flight power requirements. Domestic chickens (Gallus gallus domesticus) in backyards and farms exhibit feather loss, naturally high wing loading, and limited flight capabilities. Yet, housing chickens in aviaries requires birds to navigate three-dimensional spaces to access resources. To understand the impact of feather loss on laying hens' flight capabilities, we symmetrically clipped the primary and secondary feathers before measuring wing and whole-body kinematics during descent from a 1.5 m platform. We expected birds to compensate for increased wing loading by increasing wingbeat frequency, amplitude and angular velocity. Otherwise, we expected to observe an increase in descent velocity and angle and an increase in vertical acceleration. Feather clipping had a significant effect on descent velocity, descent angle and horizontal acceleration. Half-clipped hens had lower descent velocity and angle than full-clipped hens, and unclipped hens had the highest horizontal acceleration. All hens landed with a velocity two to three times greater than in bird species that are adept fliers. Our results suggest that intact laying hens operate at the maximal power output supported by their anatomy and are at the limit of their ability to control flight trajectory.

Physiology and behavior under food limitation support an escape, not preparative, response in the nomadic pine siskin (Spinus pinus).

Migration allows animals to use resources that are variable in time and/or space, with different migratory strategies depending on the predictability of resource variation. When food varies seasonally, obligate migrants anticipate and prepare for migration. In contrast, facultative migrants, whose movements are unpredictable in timing and destination, may prepare for either migration or escape when resources are depleted. We propose and test two alternative hypotheses regarding the behavioral and physiological responses of facultative migrants to declining food availability. (1) The prepare hypothesis predicts that facultative migrants prepare for departure by increasing fuel stores in response to declining food availability, and elevations of baseline corticosterone (CORT) facilitate increased activity. (2) The escape hypothesis predicts that facultative migrants do not prepare for departure, body condition declines as food availability declines, and stress-induced levels of CORT induce escape behavior when both energetic condition and food resources are low. We conducted a 16-day experiment, measuring body composition (using quantitative magnetic resonance), activity (using force perches) and baseline CORT in pine siskins (Spinus pinus) given ad libitum food or a slow decline, fast decline or randomly changing amount of food. Our results support the escape hypothesis: body condition declined as food declined, decreases in body and fat mass were associated with increases in baseline CORT, and activity increased only when food availability was low. This work suggests that facultative migration in autumn allows birds to escape low-resource areas and that the underlying physiological mechanisms differ from those driving both seasonal, obligate migrations and spring nomadic movements.