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.

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.

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.

A heterothermic spectrum in hummingbirds.

Many endotherms use torpor, saving energy by a controlled reduction of their body temperature and metabolic rate. Some species (e.g. arctic ground squirrels, hummingbirds) enter deep torpor, dropping their body temperature by 23-37°C, while others can only enter shallow torpor (e.g. pigeons, 3-10°C reduction). However, deep torpor in mammals can increase predation risk (unless animals are in burrows or caves), inhibit immune function and result in sleep deprivation, so even for species that can enter deep torpor, facultative shallow torpor might help balance energy savings with these potential costs. Deep torpor occurs in three avian orders, but the trade-offs of deep torpor in birds are unknown. Although the literature hints that some bird species (mousebirds and perhaps hummingbirds) can use both shallow and deep torpor, little empirical evidence of such an avian heterothermy spectrum within species exists. We infrared imaged three hummingbird species that are known to use deep torpor, under natural temperature and light cycles, to test whether they were also capable of shallow torpor. All three species used both deep and shallow torpor, often on the same night. Depending on the species, they used shallow torpor for 5-35% of the night. The presence of a heterothermic spectrum in these bird species indicates a capacity for fine-scale physiological and genetic regulation of avian torpid metabolism.

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.

Sex-specific energy management strategies in response to training for increased foraging effort prior to reproduction in captive zebra finches.

Free-living animals often engage in behaviour that involves high rates of workload and results in high daily energy expenditure (DEE), such as reproduction. However, the evidence for elevated DEE accompanying reproduction remains equivocal. In fact, many studies have found no difference in DEE between reproducing and non-reproducing females. One of the hypotheses explaining the lack of difference is the concept of an 'energetic ceiling'. However, it is unclear whether the lack of increase in energy expenditure is due to the existence of an energetic ceiling and/or compensation by males during parental care. To investigate whether an energetic ceiling exists, we experimentally manipulated foraging effort in captive zebra finches, Taeniopygia guttata, creating two groups with high and low foraging efforts followed by both groups breeding in the low foraging effort common garden condition. DEE was measured in both sexes throughout the experiment. We show sex-specific energy management strategies in response to training for increased foraging effort prior to reproduction. Specifically, males and females responded differently to the high foraging effort treatment and subsequently to chick rearing in terms of energy expenditure. Our results also suggest that there is an energetic ceiling in females and that energetic costs incurred prior to reproduction can be carried over into subsequent stages of reproduction in a sex-specific manner.

Physiological adjustments to high foraging effort negatively affect fecundity but not final reproductive output in captive zebra finches.

Foraging at elevated rates to provision offspring is thought to be an energetically costly activity and it has been suggested that there are physiological costs associated with the high workload involved. However, for the most part, evidence for costs of increased foraging and/or reproductive effort is weak. Furthermore, despite some experimental evidence demonstrating negative effects of increased foraging and parental effort, the physiological mechanisms underlying costs associated with high workload remain poorly understood. To examine how high workload affects haematology, oxidative stress and reproductive output, we experimentally manipulated foraging effort in captive zebra finches, Taeniopygia guttata, using a previously described technique, and allowed individuals to breed first in low foraging effort conditions and then in high foraging effort conditions. We found that birds upregulated haematocrit and haemoglobin concentration in response to training. Birds subjected to increased workload during reproduction had lower fecundity, although final reproductive output was not significantly different than that of controls. Offspring of parents subjected to high workload during reproduction also had higher oxidative stress when they were 90 days of age. Total antioxidant capacity and reactive oxygen metabolites of birds responded differently in the two breeding attempts, but we did detect an overall increase in oxidative stress in response to training in either attempt, which could explain the lower fecundity observed in birds subjected to increased workload during reproduction.

The allometry of daily energy expenditure in hummingbirds: An energy budget approach.

Within-clade allometric relationships represent standard laws of scaling between energy and size, and their outliers provide new avenues for physiological and ecological research. According to the metabolic-level boundaries hypothesis, metabolic rates as a function of mass are expected to scale closer to 0.67 when driven by surface-related processes (e.g. heat or water flux), while volume-related processes (e.g. activity) generate slopes closer to one. In birds, daily energy expenditure (DEE) scales with body mass (M) in the relationship logDEE=2.35+0.68×logM , consistent with surface-level processes driving the relationship. However, taxon-specific patterns differ from the scaling slope of all birds. Hummingbirds have the highest mass-specific metabolic rates among all vertebrates. Previous studies on a few hummingbird species, without accounting for the phylogeny, estimated that the DEE-body mass relationship for hummingbirds was logDEE=1.72+1.21×logM . In Contrast to the theoretical expectations, this slope >1 indicates that larger hummingbirds are less metabolically efficient than smaller hummingbirds. We collected DEE and mass data for 12 hummingbird species, which, combined with published data, represented 17 hummingbird species in eight of nine hummingbird clades over a sixfold size range of body size (2.7-17.5 g). After accounting for phylogenetic relatedness, we found DEE scales with body mass as logDEE=2.04+0.95×logM . This slope of 0.95 is lower than previously estimated for hummingbirds, but much higher than the slope for all birds (0.68). The high slopes of torpor, hovering and flight potentially explain the high interspecific DEE slope for hummingbirds compared to other endotherms.

Integrating morphology and kinematics in the scaling of hummingbird hovering metabolic rate and efficiency.

Wing kinematics and morphology are influential upon the aerodynamics of flight. However, there is a lack of studies linking these variables to metabolic costs, particularly in the context of morphological adaptation to body size. Furthermore, the conversion efficiency from chemical energy into movement by the muscles (mechanochemical efficiency) scales with mass in terrestrial quadrupeds, but this scaling relationship has not been demonstrated within flying vertebrates. Positive scaling of efficiency with body size may reduce the metabolic costs of flight for relatively larger species. Here, we assembled a dataset of morphological, kinematic, and metabolic data on hovering hummingbirds to explore the influence of wing morphology, efficiency, and mass on hovering metabolic rate (HMR). We hypothesize that HMR would decline with increasing wing size, after accounting for mass. Furthermore, we hypothesize that efficiency will increase with mass, similarly to other forms of locomotion. We do not find a relationship between relative wing size and HMR, and instead find that the cost of each wingbeat increases hyperallometrically while wingbeat frequency declines with increasing mass. This suggests that increasing wing size is metabolically favourable over cycle frequency with increasing mass. Further benefits are offered to larger hummingbirds owing to the positive scaling of efficiency.

Hovering in the heat: effects of environmental temperature on heat regulation in foraging hummingbirds.

At high temperature (greater than 40°C) endotherms experience reduced passive heat dissipation (radiation, conduction and convection) and increased reliance on evaporative heat loss. High temperatures challenge flying birds due to heat produced by wing muscles. Hummingbirds depend on flight for foraging, yet inhabit hot regions. We used infrared thermography to explore how lower passive heat dissipation during flight impacts body-heat management in broad-billed (Cynanthus latirostris, 3.0 g), black-chinned (Archilochus alexandri, 3.0 g), Rivoli's (Eugenes fulgens, 7.5 g) and blue-throated (Lampornis clemenciae, 8.0 g) hummingbirds in southeastern Arizona and calliope hummingbirds (Selasphorus calliope, 2.6 g) in Montana. Thermal gradients driving passive heat dissipation through eye, shoulder and feet dissipation areas are eliminated between 36 and 40°C. Thermal gradients persisted at higher temperatures in smaller species, possibly allowing them to inhabit warmer sites. All species experienced extended daytime periods lacking thermal gradients. Broad-billed hummingbirds lacking thermal gradients regulated the mean total-body surface temperature at approximately 38°C, suggesting behavioural thermoregulation. Blue-throated hummingbirds were inactive when lacking passive heat dissipation and hence might have the lowest temperature tolerance of the four species. Use of thermal refugia permitted hummingbirds to tolerate higher temperatures, but climate change could eliminate refugia, forcing distributional shifts in hummingbird populations.

Flight mechanics and control of escape manoeuvres in hummingbirds. II. Aerodynamic force production, flight control and performance limitations.

The superior manoeuvrability of hummingbirds emerges from complex interactions of specialized neural and physiological processes with the unique flight dynamics of flapping wings. Escape manoeuvring is an ecologically relevant, natural behaviour of hummingbirds, from which we can gain understanding into the functional limits of vertebrate locomotor capacity. Here, we extend our kinematic analysis of escape manoeuvres from a companion paper to assess two potential limiting factors of the manoeuvring performance of hummingbirds: (1) muscle mechanical power output and (2) delays in the neural sensing and control system. We focused on the magnificent hummingbird (Eugenes fulgens, 7.8 g) and the black-chinned hummingbird (Archilochus alexandri, 3.1 g), which represent large and small species, respectively. We first estimated the aerodynamic forces, moments and the mechanical power of escape manoeuvres using measured wing kinematics. Comparing active-manoeuvring and passive-damping aerodynamic moments, we found that pitch dynamics were lightly damped and dominated by the effect of inertia, while roll dynamics were highly damped. To achieve observed closed-loop performance, pitch manoeuvres required faster sensorimotor transduction, as hummingbirds can only tolerate half the delay allowed in roll manoeuvres. Accordingly, our results suggested that pitch control may require a more sophisticated control strategy, such as those based on prediction. For the magnificent hummingbird, we estimated that escape manoeuvres required muscle mass-specific power 4.5 times that during hovering. Therefore, in addition to the limitation imposed by sensorimotor delays, muscle power could also limit the performance of escape manoeuvres.

Flight mechanics and control of escape manoeuvres in hummingbirds. I. Flight kinematics.

Hummingbirds are nature's masters of aerobatic manoeuvres. Previous research shows that hummingbirds and insects converged evolutionarily upon similar aerodynamic mechanisms and kinematics in hovering. Herein, we use three-dimensional kinematic data to begin to test for similar convergence of kinematics used for escape flight and to explore the effects of body size upon manoeuvring. We studied four hummingbird species in North America including two large species (magnificent hummingbird, Eugenes fulgens, 7.8 g, and blue-throated hummingbird, Lampornis clemenciae, 8.0 g) and two smaller species (broad-billed hummingbird, Cynanthus latirostris, 3.4 g, and black-chinned hummingbirds Archilochus alexandri, 3.1 g). Starting from a steady hover, hummingbirds consistently manoeuvred away from perceived threats using a drastic escape response that featured body pitch and roll rotations coupled with a large linear acceleration. Hummingbirds changed their flapping frequency and wing trajectory in all three degrees of freedom on a stroke-by-stroke basis, likely causing rapid and significant alteration of the magnitude and direction of aerodynamic forces. Thus it appears that the flight control of hummingbirds does not obey the 'helicopter model' that is valid for similar escape manoeuvres in fruit flies. Except for broad-billed hummingbirds, the hummingbirds had faster reaction times than those reported for visual feedback control in insects. The two larger hummingbird species performed pitch rotations and global-yaw turns with considerably larger magnitude than the smaller species, but roll rates and cumulative roll angles were similar among the four species.

Three-dimensional simulation for fast forward flight of a calliope hummingbird.

We present a computational study of flapping-wing aerodynamics of a calliope hummingbird (Selasphorus calliope) during fast forward flight. Three-dimensional wing kinematics were incorporated into the model by extracting time-dependent wing position from high-speed videos of the bird flying in a wind tunnel at 8.3 m s(-1). The advance ratio, i.e. the ratio between flight speed and average wingtip speed, is around one. An immersed-boundary method was used to simulate flow around the wings and bird body. The result shows that both downstroke and upstroke in a wingbeat cycle produce significant thrust for the bird to overcome drag on the body, and such thrust production comes at price of negative lift induced during upstroke. This feature might be shared with bats, while being distinct from insects and other birds, including closely related swifts.

Size dependence in non-sperm ejaculate production is reflected in daily energy expenditure and resting metabolic rate.

The non-sperm components of an ejaculate, such as copulatory plugs, can be essential to male reproductive success. But the costs of these ejaculate components are often considered trivial. In polyandrous species, males are predicted to increase energy allocation to the production of non-sperm components, but this allocation is often condition dependent and the energetic costs of their production have never been quantified. Red-sided garter snakes (Thamnophis sirtalis parietalis) are an excellent model with which to quantify the energetic costs of non-sperm components of the ejaculate as they exhibit a dissociated reproductive pattern in which sperm production is temporally disjunct from copulatory plug production, mating and plug deposition. We estimated the daily energy expenditure and resting metabolic rate of males after courtship and mating, and used bomb calorimetry to estimate the energy content of copulatory plugs. We found that both daily energy expenditure and resting metabolic rate were significantly higher in small mating males than in courting males, and a single copulatory plug without sperm constitutes 5-18% of daily energy expenditure. To our knowledge, this is the first study to quantify the energetic expense of size-dependent ejaculate strategies in any species.

Heat dissipation during hovering and forward flight in hummingbirds.

Flying animals generate large amounts of heat, which must be dissipated to avoid overheating. In birds, heat dissipation is complicated by feathers, which cover most body surfaces and retard heat loss. To understand how birds manage heat budgets during flight, it is critical to know how heat moves from the skin to the external environment. Hummingbirds are instructive because they fly at speeds from 0 to more than 12 m s(-1), during which they transit from radiative to convective heat loss. We used infrared thermography and particle image velocimetry to test the effects of flight speed on heat loss from specific body regions in flying calliope hummingbirds (Selasphorus calliope). We measured heat flux in a carcass with and without plumage to test the effectiveness of the insulation layer. In flying hummingbirds, the highest thermal gradients occurred in key heat dissipation areas (HDAs) around the eyes, axial region and feet. Eye and axial surface temperatures were 8°C or more above air temperature, and remained relatively constant across speeds suggesting physiological regulation of skin surface temperature. During hovering, birds dangled their feet, which enhanced radiative heat loss. In addition, during hovering, near-body induced airflows from the wings were low except around the feet (approx. 2.5 m s(-1)), which probably enhanced convective heat loss. Axial HDA and maximum surface temperature exhibited a shallow U-shaped pattern across speeds, revealing a localized relationship with power production in flight in the HDA closest to the primary flight muscles. We conclude that hummingbirds actively alter routes of heat dissipation as a function of flight speed.

Respiratory evaporative water loss during hovering and forward flight in hummingbirds.

Hummingbirds represent an end point for small body size and water flux in vertebrates. We explored the role evaporative water loss (EWL) plays in management of their large water pool and its use in dissipating metabolic heat. We measured respiratory evaporative water loss (REWL) in hovering hummingbirds in the field (6 species) and over a range of speeds in a wind tunnel (1 species) using an open-circuit mask respirometry system. Hovering REWL during the active period was positively correlated with operative temperature (T(e)) likely due to some combination of an increase in the vapor-pressure deficit, increase in lung ventilation rate, and reduced importance of dry heat transfer at higher T(e). In rufous hummingbirds (Selasphorus rufus; 3.3g) REWL during forward flight at 6 and 10 m/s was less than half the value for hovering. The proportion of total dissipated heat (TDH) accounted for by REWL during hovering at T(e)> 40°C was <40% in most species. During forward flight in S. rufus the proportion of TDH accounted for by REWL was ~35% less than for hovering. REWL in hummingbirds is a relatively small component of the water budget compared with other bird species (<20%) so cutaneous evaporative water loss and dry heat transfer must contribute significantly to thermal balance in hummingbirds.