Application of a novel deep learning-based 3D videography workflow to bat flight.

Studying the detailed biomechanics of flying animals requires accurate three-dimensional coordinates for key anatomical landmarks. Traditionally, this relies on manually digitizing animal videos, a labor-intensive task that scales poorly with increasing framerates and numbers of cameras. Here, we present a workflow that combines deep learning-powered automatic digitization with filtering and correction of mislabeled points using quality metrics from deep learning and 3D reconstruction. We tested our workflow using a particularly challenging scenario: bat flight. First, we documented four bats flying steadily in a 2 m3 wind tunnel test section. Wing kinematic parameters resulting from manually digitizing bats with markers applied to anatomical landmarks were not significantly different from those resulting from applying our workflow to the same bats without markers for five out of six parameters. Second, we compared coordinates from manual digitization against those yielded via our workflow for bats flying freely in a 344 m3 enclosure. Average distance between coordinates from our workflow and those from manual digitization was less than a millimeter larger than the average human-to-human coordinate distance. The improved efficiency of our workflow has the potential to increase the scalability of studies on animal flight biomechanics.

Strategic predatory pursuit of the stealthy, highly manoeuvrable, slow flying bat Corynorhinus townsendii.

A predator's capacity to catch prey depends on its ability to navigate its environment in response to prey movements or escape behaviour. In predator-prey interactions that involve an active chase, pursuit behaviour can be studied as the collection of rules that dictate how a predator should steer to capture prey. It remains unclear how variable this behaviour is within and across species since most studies have detailed the pursuit behaviour of high-speed, open-area foragers. In this study, we analyse the pursuit behaviour in 44 successful captures by Corynorhinus townsendii, Townsend's big-eared bat (n = 4). This species forages close to vegetation using slow and highly manoeuvrable flight, which contrasts with the locomotor capabilities and feeding ecologies of other taxa studied to date. Our results indicate that this species relies on an initial stealthy approach, which is generally sufficient to capture prey (32 out of 44 trials). In cases where the initial approach is not sufficient to perform a capture attempt (12 out of 44 trials), C. townsendii continues its pursuit by reacting to prey movements in a manner best modelled with a combination of pure pursuit, or following prey directly, and proportional navigation, or moving to an interception point.

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.

By a whisker: the sensory role of vibrissae in hovering flight in nectarivorous bats.

Whiskers are important tactile structures widely used across mammals for a variety of sensory functions, but it is not known how bats-representing about a fifth of all extant mammal species-use them. Nectar-eating bats typically have long vibrissae (long, stiff hairs) arranged in a forward-facing brush-like formation that is not present in most non-nectarivorous bats. They also commonly use a unique flight strategy to access their food-hovering flight. Here we investigated whether these species use their vibrissae to optimize their feeding by assisting fine flight control. We used behavioural experiments to test if bats' flight trajectory into the flower changed after vibrissa removal, and phylogenetic comparative methods to test whether vibrissa length is related to nectarivory. We found that bat flight trajectory was altered after vibrissae removal and that nectarivorous bats possess longer vibrissae than non-nectivorous species, providing evidence of an additional source of information in bats' diverse sensory toolkit.

Hair, there and everywhere: A comparison of bat wing sensory hair distribution.

Bat wing membranes are composed of specialized skin that is covered with small sensory hairs which are likely mechanosensory and have been suggested to help bats sense airflow during flight. These sensory hairs have to date been studied in only a few of the more than 1,400 bat species around the world. Little is known about the diversity of the sensory hair network across the bat phylogeny. In this study, we use high-resolution photomicrographs of preserved bat wings from 17 species in 12 families to characterize the distribution of sensory hairs along the wing and among species. We identify general patterns of sensory hair distribution across species, including the apparent relationships of sensory hairs to intramembranous wing muscles, the network of connective tissues in the wing membrane, and the bones of the forelimb. We also describe distinctive clustering of these sensory structures in some species. We also quantified sensory hair density in several regions of interest in the propatagium, plagiopatagium, and dactylopagatia, finding that sensory hair density was higher proximally than distally. This examination of the anatomical organization of the sensory hair network in a comparative context provides a framework for existing research on sensory hair function and highlights avenues for further research.

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.

Bats actively modulate membrane compliance to control camber and reduce drag.

Bat wing skin is exceptionally compliant and cambers significantly during flight. Plagiopatagiales proprii, arrays of small muscles embedded in the armwing membrane, are activated during flight and are hypothesized to modulate membrane tension. We examined the function of these muscles using Jamaican fruit bats, Artibeus jamaicensis. When these muscles were paralyzed using botulinum toxin, the bats preferred flight speed decreased and they were unable to fly at very low speeds. Paralysis of the plagiopatagiales also resulted in increased armwing camber consistent with a hypothesized role of modulating aeroelastic interactions. Other compensatory kinematics included increased downstroke angle and increased wingbeat amplitude. These results are consistent with the bats experiencing increased drag and flight power costs associated with the loss of wing-membrane control. Our results indicate that A. jamaicensis likely always employ their wing membrane muscles during sustained flight to control camber and to enhance flight efficiency over a wide flight envelope.

A comparison of thermal sensitivities of wing muscle contractile properties from a temperate and tropical bat species.

Endotherms experience temperature variation among body regions, or regional heterothermy, despite maintaining high core body temperatures. Bat forelimbs are elongated to function as wings, which makes them vulnerable to heat loss and exaggerates regional heterothermy. A tropical bat species, Carollia perspicillata, flies with distal wing muscles that are substantially (>10°C) cooler than proximal wing muscles and significantly less temperature sensitive. We hypothesized that the difference between proximal and distal wing muscles would be even more extreme in a temperate bat species that is capable of flight at variable environmental temperatures. We measured the contractile properties of the proximal pectoralis muscle and distal extensor carpi radialis muscle at a range of temperatures in the big brown bat, Eptesicus fuscus, and compared their thermal dependence with that of the same muscles in C. perspicillata. We found that, overall, temperature sensitivities between species were remarkably similar. The sole exception was the shortening velocity of the pectoralis muscle in E. fuscus, which was less temperature sensitive than in C. perspicillata. This decreased temperature sensitivity in a proximal muscle runs counter to our prediction. We suggest that the relative lability of body temperature in E. fuscus may make better pectoralis function at low temperatures advantageous.

A proximal-distal difference in bat wing muscle thermal sensitivity parallels a difference in operating temperatures along the wing.

Flight is a demanding form of locomotion, requiring fast activation and relaxation in wing muscles to produce the necessary wingbeat frequencies. Bats maintain high body temperatures during flight, but their wing muscles cool under typical environmental conditions. Because distal wing muscles are colder during flight than proximal muscles, we hypothesized that they would be less temperature sensitive to compensate for temperature effects, resulting in proximal-distal differences in temperature sensitivity that match differences in muscle operating temperature. We measured contractile rates across temperatures in the proximal pectoralis muscle and an interosseous in the handwing of Carollia perspicillata, a small neotropical fruit bat, and compared their thermal dependence with that of a forearm muscle measured in a previous study. We found that the contractile properties of the pectoralis were significantly more temperature sensitive than those of the distal muscles. This suggests that cooling of the distal wing muscles imposes a selective pressure on muscle contractile function which has led to shifts in temperature sensitivity. This study is the first to demonstrate differences in temperature sensitivity along the length of a single limb in an endotherm and suggests that temperature variation may be underappreciated as a determinant of locomotor performance in endotherms generally.

Bats use topography and nocturnal updrafts to fly high and fast.

During the day, flying animals exploit the environmental energy landscape by seeking out thermal or orographic uplift, or extracting energy from wind gradients.1-6 However, most of these energy sources are not thought to be available at night because of the lower thermal potential in the nocturnal atmosphere, as well as the difficulty of locating features that generate uplift. Despite this, several bat species have been observed hundreds to thousands of meters above the ground.7-9 Individuals make repeated, energetically costly high-altitude ascents,10-13 and others fly at some of the fastest speeds observed for powered vertebrate flight.14 We hypothesized that bats use orographic uplift to reach high altitudes,9,15-17 and that both this uplift and bat high-altitude ascents would be highly predictable.18 By superimposing detailed three-dimensional GPS tracking of European free-tailed bats (Tadarida teniotis) on high-resolution regional wind data, we show that bats do indeed use the energy of orographic uplift to climb to over 1,600 m, and also that they reach maximum sustained self-powered airspeeds of 135 km h-1. We show that wind and topography can predict areas of the landscape able to support high-altitude ascents, and that bats use these locations to reach high altitudes while reducing airspeeds. Bats then integrate wind conditions to guide high-altitude ascents, deftly exploiting vertical wind energy in the nocturnal landscape.

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.

Wings as inertial appendages: how bats recover from aerial stumbles.

For many animals, movement through complex natural environments necessitates the evolution of mechanisms that enable recovery from unexpected perturbations. Knowledge of how flying animals contend with disruptive forces is limited, however, and is nearly nonexistent for bats, the only mammals capable of powered flight. We investigated perturbation recovery in Carollia perspicillata by administering a well-defined jet of compressed air, equal to 2.5 times bodyweight, which induced two types of disturbances, termed aerial stumbles: pitch-inducing body perturbations and roll-inducing wing perturbations. In both cases, bats responded primarily by adjusting extension of wing joints, and recovered pre-disturbance body orientation and left-right symmetry of wing motions over the course of only one wingbeat cycle. Bats recovered from body perturbations by symmetrically extending their wings cranially and dorsally during upstroke, and from wing perturbations by asymmetrically extending their wings throughout the recovery wingbeat. We used a simplified dynamical model to test the hypothesis that wing extension asymmetry during recovery from roll-inducing perturbations can generate inertial torques that alone are sufficient to produce the observed body reorientation. Results supported the hypothesis, and also suggested that subsequent restoration of symmetrical wing extension help to decelerate recovery rotation via passive aerodynamic mechanisms. During recovery, humeral elevation/depression remained largely unchanged while bats adjusted wing extension at the elbow and wrist, suggesting a proximo-distal gradient in the neuromechanical control of the wing.

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.

The dynamics of hovering flight in hummingbirds, insects and bats with implications for aerial robotics.

We analyze the effects of morphology and wing kinematics on the performance of hovering flight. We present a simplified dynamical model with body translational and rotational degrees of freedom that incorporates the flapping, long-axis wing rotation and folding of the wing. To validate our simulation, we compare our results with direct measurements from hovering insects, hummingbirds and bats. Results show that long-axis wing rotation angle (a proxy for pronation) has a significant effect on energy efficiency. For a given wing rotation amplitude, the hovering system has a power-optimal flapping frequency for each stroke-plane orientation, and that frequency closely corresponds to the wingbeat frequencies observed in a diverse range of hummingbird species. We find that larger animals (with larger total mass and wing size), such as bats, require more power to maintain a stable hovering orbit and that hovering with a constant wingspan becomes increasingly impractical with increasing body size. We show, as an exemplar, that for a system of the size of a hovering bat, e.g. Glossophaga soricina, hovering with constant wingspan is dynamically possible, but is implausible and inefficient. For these conditions, hovering with varying wingspan, retracting the wing on the upstroke, is a more realistic hovering modality.

Low thermal dependence of the contractile properties of a wing muscle in the bat Carollia perspicillata.

Temperature affects contractile rate properties in muscle, which may affect locomotor performance. Endotherms are known to maintain high core body temperatures, but temperatures in the periphery of the body can fluctuate. Such a phenomenon occurs in bats, whose wing musculature is relatively poorly insulated, resulting in substantially depressed temperatures in the distal wing. We examined a wing muscle in the small-bodied tropical bat Carollia perspicillata and a hindlimb muscle in the laboratory mouse at 5°C intervals from 22 to 42°C to determine the thermal dependence of the contractile properties of both muscles. We found that the bat extensor carpi radialis longus had low thermal dependence from near body temperature to 10°C lower, with Q10 values of less than 1.5 for relaxation from contraction and shortening velocities in that interval, and with no significant difference in some rate properties in the interval between 32 and 37°C. In contrast, for all temperature intervals below 37°C, Q10 values for the mouse extensor digitorum longus were 1.5 or higher, and rate properties differed significantly across successive temperature intervals from 37 to 22°C. An ANCOVA analysis found that the thermal dependencies of all measured isometric and isotonic rate processes were significantly different between the bat and mouse muscles. The relatively low thermal dependence of the bat muscle likely represents a downward shift of its optimal temperature and may be functionally significant in light of the variable operating temperatures of bat wing muscles.

The influence of aspect ratio and stroke pattern on force generation of a bat-inspired membrane wing.

Aspect ratio (AR) is one parameter used to predict the flight performance of a bat species based on wing shape. Bats with high AR wings are thought to have superior lift-to-drag ratios and are therefore predicted to be able to fly faster or to sustain longer flights. By contrast, bats with lower AR wings are usually thought to exhibit higher manoeuvrability. However, the half-span ARs of most bat wings fall into a narrow range of about 2.5-4.5. Furthermore, these predictions do not take into account the wide variation in flapping motion observed in bats. To examine the influence of different stroke patterns, we measured lift and drag of highly compliant membrane wings with different bat-relevant ARs. A two degrees of freedom shoulder joint allowed for independent control of flapping amplitude and wing sweep. We tested five models with the same variations of stroke patterns, flapping frequencies and wind speed velocities. Our results suggest that within the relatively small AR range of bat wings, AR has no clear effect on force generation. Instead, the generation of lift by our simple model mostly depends on wingbeat frequency, flapping amplitude and freestream velocity; drag is mostly affected by the flapping amplitude.

Speed-dependent modulation of wing muscle recruitment intensity and kinematics in two bat species.

Animals respond to changes in power requirements during locomotion by modulating the intensity of recruitment of their propulsive musculature, but many questions concerning how muscle recruitment varies with speed across modes of locomotion remain unanswered. We measured normalized average burst EMG (aEMG) for pectoralis major and biceps brachii at different flight speeds in two relatively distantly related bat species: the aerial insectivore Eptesicus fuscus, and the primarily fruit-eating Carollia perspicillata These ecologically distinct species employ different flight behaviors but possess similar wing aspect ratio, wing loading and body mass. Because propulsive requirements usually correlate with body size, and aEMG likely reflects force, we hypothesized that these species would deploy similar speed-dependent aEMG modulation. Instead, we found that aEMG was speed independent in E. fuscus and modulated in a U-shaped or linearly increasing relationship with speed in C. perspicillata This interspecific difference may be related to differences in muscle fiber type composition and/or overall patterns of recruitment of the large ensemble of muscles that participate in actuating the highly articulated bat wing. We also found interspecific differences in the speed dependence of 3D wing kinematics: E. fuscus modulates wing flexion during upstroke significantly more than C. perspicillata Overall, we observed two different strategies to increase flight speed: C. perspicillata tends to modulate aEMG, and E. fuscus tends to modulate wing kinematics. These strategies may reflect different requirements for avoiding negative lift and overcoming drag during slow and fast flight, respectively, a subject we suggest merits further study.

Diversity in the organization of elastin bundles and intramembranous muscles in bat wings.

Unlike birds and insects, bats fly with wings composed of thin skin that envelops the bones of the forelimb and spans the area between the limbs, digits, and sometimes the tail. This skin is complex and unusual; it is thinner than typical mammalian skin and contains organized bundles of elastin and embedded skeletal muscles. These elements are likely responsible for controlling the shape of the wing during flight and contributing to the aerodynamic capabilities of bats. We examined the arrangement of two macroscopic architectural elements in bat wings, elastin bundles and wing membrane muscles, to assess the diversity in bat wing skin morphology. We characterized the plagiopatagium and dactylopatagium of 130 species from 17 families of bats using cross-polarized light imaging. This method revealed structures with distinctive relative birefringence, heterogeneity of birefringence, variation in size, and degree of branching. We used previously published anatomical studies and tissue histology to identify birefringent structures, and we analyzed their architecture across taxa. Elastin bundles, muscles, neurovasculature, and collagenous fibers are present in all species. Elastin bundles are oriented in a predominantly spanwise or proximodistal direction, and there are five characteristic muscle arrays that occur within the plagiopatagium, far more muscle than typically recognized. These results inform recent functional studies of wing membrane architecture, support the functional hypothesis that elastin bundles aid wing folding and unfolding, and further suggest that all bats may use these architectural elements for flight. All species also possess numerous muscles within the wing membrane, but the architecture of muscle arrays within the plagiopatagium varies among families. To facilitate present and future discussion of these muscle arrays, we refine wing membrane muscle nomenclature in a manner that reflects this morphological diversity. The architecture of the constituents of the skin of the wing likely plays a key role in shaping wings during flight.

PRINCIPLES AND PATTERNS OF BAT MOVEMENTS: FROM AERODYNAMICS TO ECOLOGY.

Movement ecology as an integrative discipline has advanced associated fields because it presents not only a conceptual framework for understanding movement principles but also helps formulate predictions about the consequences of movements for animals and their environments. Here, we synthesize recent studies on principles and patterns of bat movements in context of the movement ecology paradigm. The motion capacity of bats is defined by their highly articulated, flexible wings. Power production during flight follows a U-shaped curve in relation to speed in bats yet, in contrast to birds, bats use mostly exogenous nutrients for sustained flight. The navigation capacity of most bats is dominated by the echolocation system, yet other sensory modalities, including an iron-based magnetic sense, may contribute to navigation depending on a bat's familiarity with the terrain. Patterns derived from these capacities relate to antagonistic and mutualistic interactions with food items. The navigation capacity of bats may influence their sociality, in particular, the extent of group foraging based on eavesdropping on conspecifics' echolocation calls. We infer that understanding the movement ecology of bats within the framework of the movement ecology paradigm provides new insights into ecological processes mediated by bats, from ecosystem services to diseases.

Airplane tracking documents the fastest flight speeds recorded for bats.

The performance capabilities of flying animals reflect the interplay of biomechanical and physiological constraints and evolutionary innovation. Of the two extant groups of vertebrates that are capable of powered flight, birds are thought to fly more efficiently and faster than bats. However, fast-flying bat species that are adapted for flight in open airspace are similar in wing shape and appear to be similar in flight dynamics to fast-flying birds that exploit the same aerial niche. Here, we investigate flight behaviour in seven free-flying Brazilian free-tailed bats (Tadarida brasiliensis) and report that the maximum ground speeds achieved exceed speeds previously documented for any bat. Regional wind modelling indicates that bats adjusted flight speeds in response to winds by flying more slowly as wind support increased and flying faster when confronted with crosswinds, as demonstrated for insects, birds and other bats. Increased frequency of pauses in wing beats at faster speeds suggests that flap-gliding assists the bats' rapid flight. Our results suggest that flight performance in bats has been underappreciated and that functional differences in the flight abilities of birds and bats require re-evaluation.