Effects of wing damage and moult gaps on vertebrate flight performance.

Vertebrates capable of powered flight rely on wings, muscles that drive their flapping and sensory inputs to the brain allowing for control of the motor output. In birds, the wings are formed of arrangements of adjacent flight feathers (remiges), whereas the wings of bats consist of double-layered skin membrane stretched out between the forelimb skeleton, body and legs. Bird feathers become worn from use and brittle from UV exposure, which leads to loss of function; to compensate, they are renewed (moulted) at regular intervals. Bird feathers and the wings of bats can be damaged by accident. Wing damage and loss of wing surface due to moult almost invariably cause reduced flight performance in measures such as take-off angle and speed. During moult in birds, this is partially counteracted by concurrent mass loss and enlarged flight muscles. Bats have sensory hairs covering their wing surface that provide feedback information about flow; thus, wing damage affects flight speed and turning ability. Bats also have thin, thread-like muscles, distributed within the wing membrane and, if these are damaged, the control of wing camber is lost. Here, I review the effects of wing damage and moult on flight performance in birds, and the consequences of wing damage in bats. I also discuss studies of life-history trade-offs that make use of experimental trimming of flight feathers as a way to handicap parent birds feeding their young.

Reconstruction of Flight Parameters of a Bat for Flapping Robots.

The flight of bats is comparatively less documented and understood than birds and insects and may provide novel inspiration for the design of flapping flight robots. This study captured the natural flight of short-nosed fruit bats (Cynopterus sphinx) by an optical motion capture system, "OptiTrack", with pasted markers on the wings and body to reconstruct the flight parameters. Due to the self-occlusion at some moments, points on the membrane wings cannot be captured by any cameras. To draw a smooth trajectory, it is desired to reconstruct all missing data. Therefore, an algorithm is proposed by using numerical techniques, accompanied by modern mathematical and computational tools, to envisage the missing data from the captured flight. The least-square fitted polynomial engendered the parameter equations for x-, y-, and z-coordinates of marked points which were used to reconstruct the trajectory of the flight. The parameter equations of position coordinates were also used to compute the morphological and aerodynamic characteristics of the flight. The most outstanding contribution of the work is that not only the trajectory, velocity, and velocity field but also the morphing areas of the membrane wings were recreated using the reconstructed data. These data and reconstructed curves of trajectory and velocity field will be used for the further aerodynamic analysis and mechanism design of the flapping robot. This method can also be generalized to reconstruct the performance parameters of any other animals for bionic design.

Direct Measurements of the Wing Kinematics of a Bat in Straight Flight.

Bat is the only mammal in the nature that can fly. Compared with birds and insects, bats are quite special in that their wings are formed by an elastic membrane, which renders that the airfoil deforms greatly during downstroke and upstroke. Due to the compliant skin of a bat, the movements of its wings are three-dimensionally complex during diverse flight behaviors. To understand the maneuverability and flight performance, three-dimensional reconstruction of the flight kinematics is essential. This study focuses on the reconstruction of the wing kinematics of the bat and identifies the primary relationship of parameters of aerodynamics in straight flight. With markers pasted on the wings and body of a bat, the motions of these points are recorded by a computerized optical motion capture system. The kinematic analysis shows that the motion of wings is very intricate. The digits of the wing display the sign of coupled motion. A novel approach was developed to measure the angle of attack and flapping angle of the wing. The angle of attack of leading edge differs with the overall angle of attack of the wing. The kinematics of the bat's wing is helpful to interpret the secret of the bat's flight.

Specialized landing maneuvers in Spix's disk-winged bats (Thyroptera tricolor) reveal linkage between roosting ecology and landing biomechanics.

Disk-winged bats (Thyroptera spp.) are the only mammals that use suction to cling to smooth surfaces, having evolved suction cups at the bases of the thumbs and feet that facilitate attachment to specialized roosts: the protective funnels of ephemeral furled leaves. We predicted that this combination of specialized morphology and roosting ecology is coupled with concomitantly specialized landing maneuvers. We tested this by investigating landings in Thyroptera tricolor using high-speed videography and a force-measuring landing pad disguised within a furled leaf analogue. We found that their landing maneuvers are distinct among all bats observed to date. Landings comprised three phases: (1) approach, (2) ballistic descent and (3) adhesion. During approach, bats adjusted trajectory until centered in front of and above the landing site, typically the leaf's protruding apex. Bats initiated ballistic descent by arresting the wingbeat cycle and tucking their wings to descend toward the leaf, simultaneously extending the thumb disks cranially. Adhesion commenced when the thumb disks contacted the landing site. Significant body reorientation occurred only during adhesion, and only after contact, when the thumb disks acted as fulcra about which the bats pitched 75.02±26.17 deg (mean±s.d.) to swing the foot disks into contact. Landings imposed 6.98±1.89 bodyweights of peak impact force. These landing mechanics are likely to be influenced by the orientation, spatial constraints and compliance of furled leaf roosts. Roosting ecology influences critical aspects of bat biology, and taken as a case study, this work suggests that roosting habits and landing mechanics could be functionally linked across bats.

Warm bodies, cool wings: regional heterothermy in flying bats.

Many endothermic animals experience variable limb temperatures, even as they tightly regulate core temperature. The limbs are often cooler than the core at rest, but because the large locomotor muscles of the limbs produce heat during exercise, they are thought to operate at or above core temperature during activity. Bats, small-bodied flying mammals with greatly elongated forelimbs, possess wings with large surfaces lacking any insulating fur. We hypothesized that during flight the relatively small muscles that move the elbow and wrist operate below core body temperature because of elevated heat loss. We measured muscle temperature continuously in the small fruit bat Carollia perspicillata before and during wind tunnel flights, and discretely in diverse bats at rest in Belize. We found that bats maintained high rectal temperatures, but that there was a steep proximal-to-distal gradient in wing muscle temperature. Forearm muscles were 4-6°C cooler than rectal temperature at rest and approximately 12°C cooler during flights at an air temperature of 22°C. These findings invite further study into how bats and other endotherms maintain locomotor performance in variable environments, when some muscles may be operating at low temperatures that are expected to slow contractile properties.

Bat flight: aerodynamics, kinematics and flight morphology.

Bats evolved the ability of powered flight more than 50 million years ago. The modern bat is an efficient flyer and recent research on bat flight has revealed many intriguing facts. By using particle image velocimetry to visualize wake vortices, both the magnitude and time-history of aerodynamic forces can be estimated. At most speeds the downstroke generates both lift and thrust, whereas the function of the upstroke changes with forward flight speed. At hovering and slow speed bats use a leading edge vortex to enhance the lift beyond that allowed by steady aerodynamics and an inverted wing during the upstroke to further aid weight support. The bat wing and its skeleton exhibit many features and control mechanisms that are presumed to improve flight performance. Whereas bats appear aerodynamically less efficient than birds when it comes to cruising flight, they have the edge over birds when it comes to manoeuvring. There is a direct relationship between kinematics and the aerodynamic performance, but there is still a lack of knowledge about how (and if) the bat controls the movements and shape (planform and camber) of the wing. Considering the relatively few bat species whose aerodynamic tracks have been characterized, there is scope for new discoveries and a need to study species representing more extreme positions in the bat morphospace.

Rapid flapping and fibre-reinforced membrane wings are key to high-performance bat flight.

Bats fly using significantly different wing motions from other fliers, stemming from the complex interplay of their membrane wings' motion and structural properties. Biological studies show that many bats fly at Strouhal numbers, the ratio of flapping to flight speed, 50-150% above the range typically associated with optimal locomotion. We use high-resolution fluid-structure interaction simulations of a bat wing to independently study the role of kinematics and material/structural properties in aerodynamic performance and show that peak propulsive and lift efficiencies for a bat-like wing motion require flapping 66% faster than for a symmetric motion, agreeing with the increased flapping frequency observed in zoological studies. In addition, we find that reduced membrane stiffness is associated with improved propulsive efficiency until the membrane flutters, but that incorporating microstructural anisotropy arising from biological fibre reinforcement enables a tenfold reduction of the flutter energy while maintaining high aerodynamic efficiency. Our results indicate that animals with specialized flapping motions may have correspondingly specialized flapping speeds, in contrast to arguments for a universally efficient Strouhal range. Additionally, our study demonstrates the significant role that the microstructural constitutive properties of the membrane wing of a bat can have in its propulsive performance.

Thermal Stability of Contractile Proteins in Bat Wing Muscles Explains Differences in Temperature Dependence of Whole-Muscle Shortening Velocity.

AbstractMuscle contractile properties are dependent on temperature: cooler temperatures generally slow contractile rates. Contraction and relaxation are driven by underlying biochemical systems, which are inherently sensitive to temperature. Carollia perspicillata, a small Neotropical bat, experiences large temperature differentials among body regions, resulting in a steep gradient in temperature along the wing. Although the bats maintain high core body temperatures during flight, the wing muscles may operate at more than 10°C below body temperature. Partially compensating for these colder operating temperatures, distal wing muscles have lower temperature sensitivities in their contractile properties, including shortening velocity, relative to the proximal pectoralis. Shortening velocity is correlated with the activity of myosin ATPase, an enzyme that drives the cross-bridge cycle. We hypothesized that the thermal properties of myofibrillar ATPase from the pectoralis and forearm muscles of the bat wing would correlate with the temperature sensitivity of those muscles. Using myofibrillar ATPases from the proximal and distal muscles, we measured enzyme activity across a range of temperatures and enzyme thermal stability after heat incubation across a range of time points. We found that forearm muscle myofibrillar ATPase was significantly less thermally stable than pectoralis myofibrillar ATPase but that there was no significant difference in the acute temperature dependence of enzyme activity between the two muscles.

Turning-ascending flight of a Hipposideros pratti bat.

Bats exhibit a high degree of agility and provide an excellent model system for bioinspired flight. The current study investigates an ascending right turn of a Hipposideros pratti bat and elucidates on the kinematic features and aerodynamic mechanisms used to effectuate the manoeuvre. The wing kinematics captured by a three-dimensional motion capture system is used as the boundary condition for the aerodynamic simulations featuring immersed boundary method. Results indicate that the bat uses roll and yaw rotations of the body to different extents synergistically to generate the centripetal force to initiate and sustain the turn. The turning moments are generated by drawing the wing inside the turn closer to the body, by introducing phase lags in force generation between the wings and redirecting force production to the outer part of the wing outside of the turn. Deceleration in flight speed, an increase in flapping frequency, shortening of the upstroke and thrust generation at the end of the upstroke were observed during the ascending manoeuvre. The bat consumes about 0.67 W power to execute the turning-ascending manoeuvre, which is approximately two times the power consumed by similar bats during level flight. Upon comparison with a similar manoeuvre by a Hipposideros armiger bat (Windes et al. 2020 Bioinspir. Biomim. 16, abb78d. (doi:10.1088/1748-3190/abb78d)), some commonalities, as well as differences, were observed in the detailed wing kinematics and aerodynamics.

Power requirements for bat-inspired flapping flight with heavy, highly articulated and cambered wings.

Bats fly with highly articulated and heavy wings. To understand their power requirements, we develop a three-dimensional reduced-order model, and apply it to flights of Cynopterus brachyotis, the lesser dog-faced fruit bat. Using previously measured wing kinematics, the model computes aerodynamic forces using blade element momentum theory, and incorporates inertial forces of the flapping wing using the measured mass distribution of the membrane wing and body. The two are combined into a Lagrangian equation of motion, and we performed Monte Carlo simulations to address uncertainties in measurement errors and modelling assumptions. We find that the camber of the armwing decreases with flight speed whereas the handwing camber is more independent of speed. Wing camber disproportionately impacts energetics, mainly during the downstroke, and increases the power requirement from 8% to 22% over flight speed U = 3.2-7.4 m s-1. We separate total power into aerodynamic and inertial components, and aerodynamic power into parasitic, profile and induced power, and find strong agreement with previous theoretical and experimental studies. We find that inertia of wings help to balance aerodynamic forces, alleviating the muscle power required for weight support and thrust generation. Furthermore, the model suggests aerodynamic forces assist in lifting the heavy wing during upstroke.

Wake structure and kinematics in two insectivorous bats.

We compare kinematics and wake structure over a range of flight speeds (4.0-8.2 m s(-1)) for two bats that pursue insect prey aerially, Tadarida brasiliensis and Myotis velifer Body mass and wingspan are similar in these species, but M. velifer has broader wings and lower wing loading. By using high-speed videography and particle image velocimetry of steady flight in a wind tunnel, we show that three-dimensional kinematics and wake structure are similar in the two species at the higher speeds studied, but differ at lower speeds. At lower speeds, the two species show significant differences in mean angle of attack, body-wingtip distance and sweep angle. The distinct body vortex seen at low speed in T. brasiliensis and other bats studied to date is considerably weaker or absent in M. velifer We suggest that this could be influenced by morphology: (i) the narrower thorax in this species probably reduces the body-induced discontinuity in circulation between the two wings and (ii) the wing loading is lower, hence the lift coefficient required for weight support is lower. As a result, in M. velifer, there may be a decreased disruption in the lift generation between the body and the wing, and the strength of the characteristic root vortex is greatly diminished, both suggesting increased flight efficiency.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'.

Lift enhancement by bats' dynamically changing wingspan.

This paper elucidates the aerodynamic role of the dynamically changing wingspan in bat flight. Based on direct numerical simulations of the flow over a slow-flying bat, it is found that the dynamically changing wingspan can significantly enhance the lift. Further, an analysis of flow structures and lift decomposition reveal that the elevated vortex lift associated with the leading-edge vortices intensified by the dynamically changing wingspan considerably contributed to enhancement of the time-averaged lift. The nonlinear interaction between the dynamically changing wing and the vortical structures plays an important role in the lift enhancement of a flying bat in addition to the geometrical effect of changing the lifting-surface area in a flapping cycle. In addition, the dynamically changing wingspan leads to the higher efficiency in terms of generating lift for a given amount of the mechanical energy consumed in flight.