The crouching of the shrew: Mechanical consequences of limb posture in small mammals.

An important trend in the early evolution of mammals was the shift from a sprawling stance, whereby the legs are held in a more abducted position, to a parasagittal one, in which the legs extend more downward. After that transition, many mammals shifted from a crouching stance to a more upright one. It is hypothesized that one consequence of these transitions was a decrease in the total mechanical power required for locomotion, because side-to-side accelerations of the body have become smaller, and thus less costly with changes in limb orientation. To test this hypothesis we compared the kinetics of locomotion in two mammals of body size close to those of early mammals (< 40 g), both with parasagittally oriented limbs: a crouching shrew (Blarina brevicauda; 5 animals, 17 trials) and a more upright vole (Microtus pennsylvanicus; 4 animals, 22 trials). As predicted, voles used less mechanical power per unit body mass to perform steady locomotion than shrews did (P = 0.03). However, while lateral forces were indeed smaller in voles (15.6 ± 2.0% body weight) than in shrews (26.4 ± 10.9%; P = 0.046), the power used to move the body from side-to-side was negligible, making up less than 5% of total power in both shrews and voles. The most power consumed for both species was that used to accelerate the body in the direction of travel, and this was much larger for shrews than for voles (P = 0.01). We conclude that side-to-side accelerations are negligible for small mammals-whether crouching or more upright-compared to their sprawling ancestors, and that a more upright posture further decreases the cost of locomotion compared to crouching by helping to maintain the body's momentum in the direction of travel.

Falling with Style: Bats Perform Complex Aerial Rotations by Adjusting Wing Inertia.

The remarkable maneuverability of flying animals results from precise movements of their highly specialized wings. Bats have evolved an impressive capacity to control their flight, in large part due to their ability to modulate wing shape, area, and angle of attack through many independently controlled joints. Bat wings, however, also contain many bones and relatively large muscles, and thus the ratio of bats' wing mass to their body mass is larger than it is for all other extant flyers. Although the inertia in bat wings would typically be associated with decreased aerial maneuverability, we show that bat maneuvers challenge this notion. We use a model-based tracking algorithm to measure the wing and body kinematics of bats performing complex aerial rotations. Using a minimal model of a bat with only six degrees of kinematic freedom, we show that bats can perform body rolls by selectively retracting one wing during the flapping cycle. We also show that this maneuver does not rely on aerodynamic forces, and furthermore that a fruit fly, with nearly massless wings, would not exhibit this effect. Similar results are shown for a pitching maneuver. Finally, we combine high-resolution kinematics of wing and body movements during landing and falling maneuvers with a 52-degree-of-freedom dynamical model of a bat to show that modulation of wing inertia plays the dominant role in reorienting the bat during landing and falling maneuvers, with minimal contribution from aerodynamic forces. Bats can, therefore, use their wings as multifunctional organs, capable of sophisticated aerodynamic and inertial dynamics not previously observed in other flying animals. This may also have implications for the control of aerial robotic vehicles.

Hindlimb motion during steady flight of the lesser dog-faced fruit bat, Cynopterus brachyotis.

In bats, the wing membrane is anchored not only to the body and forelimb, but also to the hindlimb. This attachment configuration gives bats the potential to modulate wing shape by moving the hindlimb, such as by joint movement at the hip or knee. Such movements could modulate lift, drag, or the pitching moment. In this study we address: 1) how the ankle translates through space during the wingbeat cycle; 2) whether amplitude of ankle motion is dependent upon flight speed; 3) how tension in the wing membrane pulls the ankle; and 4) whether wing membrane tension is responsible for driving ankle motion. We flew five individuals of the lesser dog-faced fruit bat, Cynopterus brachyotis (Family: Pteropodidae), in a wind tunnel and documented kinematics of the forelimb, hip, ankle, and trailing edge of the wing membrane. Based on kinematic analysis of hindlimb and forelimb movements, we found that: 1) during downstroke, the ankle moved ventrally and during upstroke the ankle moved dorsally; 2) there was considerable variation in amplitude of ankle motion, but amplitude did not correlate significantly with flight speed; 3) during downstroke, tension generated by the wing membrane acted to pull the ankle dorsally, and during upstroke, the wing membrane pulled laterally when taut and dorsally when relatively slack; and 4) wing membrane tension generally opposed dorsoventral ankle motion. We conclude that during forward flight in C. brachyotis, wing membrane tension does not power hindlimb motion; instead, we propose that hindlimb movements arise from muscle activity and/or inertial effects.

Glide performance and aerodynamics of non-equilibrium glides in northern flying squirrels (Glaucomys sabrinus).

Gliding is an efficient form of travel found in every major group of terrestrial vertebrates. Gliding is often modelled in equilibrium, where aerodynamic forces exactly balance body weight resulting in constant velocity. Although the equilibrium model is relevant for long-distance gliding, such as soaring by birds, it may not be realistic for shorter distances between trees. To understand the aerodynamics of inter-tree gliding, we used direct observation and mathematical modelling. We used videography (60-125 fps) to track and reconstruct the three-dimensional trajectories of northern flying squirrels (Glaucomys sabrinus) in nature. From their trajectories, we calculated velocities, aerodynamic forces and force coefficients. We determined that flying squirrels do not glide at equilibrium, and instead demonstrate continuously changing velocities, forces and force coefficients, and generate more lift than needed to balance body weight. We compared observed glide performance with mathematical simulations that use constant force coefficients, a characteristic of equilibrium glides. Simulations with varying force coefficients, such as those of live squirrels, demonstrated better whole-glide performance compared with the theoretical equilibrium state. Using results from both the observed glides and the simulation, we describe the mechanics and execution of inter-tree glides, and then discuss how gliding behaviour may relate to the evolution of flapping flight.

Kinematic plasticity during flight in fruit bats: individual variability in response to loading.

All bats experience daily and seasonal fluctuation in body mass. An increase in mass requires changes in flight kinematics to produce the extra lift necessary to compensate for increased weight. How bats modify their kinematics to increase lift, however, is not well understood. In this study, we investigated the effect of a 20% increase in mass on flight kinematics for Cynopterus brachyotis, the lesser dog-faced fruit bat. We reconstructed the 3D wing kinematics and how they changed with the additional mass. Bats showed a marked change in wing kinematics in response to loading, but changes varied among individuals. Each bat adjusted a different combination of kinematic parameters to increase lift, indicating that aerodynamic force generation can be modulated in multiple ways. Two main kinematic strategies were distinguished: bats either changed the motion of the wings by primarily increasing wingbeat frequency, or changed the configuration of the wings by increasing wing area and camber. The complex, individual-dependent response to increased loading in our bats points to an underappreciated aspect of locomotor control, in which the inherent complexity of the biomechanical system allows for kinematic plasticity. The kinematic plasticity and functional redundancy observed in bat flight can have evolutionary consequences, such as an increase potential for morphological and kinematic diversification due to weakened locomotor trade-offs.

Upstroke wing flexion and the inertial cost of bat flight.

Flying vertebrates change the shapes of their wings during the upstroke, thereby decreasing wing surface area and bringing the wings closer to the body than during downstroke. These, and other wing deformations, might reduce the inertial cost of the upstroke compared with what it would be if the wings remained fully extended. However, wing deformations themselves entail energetic costs that could exceed any inertial energy savings. Using a model that incorporates detailed three-dimensional wing kinematics, we estimated the inertial cost of flapping flight for six bat species spanning a 40-fold range of body masses. We estimate that folding and unfolding comprises roughly 44 per cent of the inertial cost, but that the total inertial cost is only approximately 65 per cent of what it would be if the wing remained extended and rigid throughout the wingbeat cycle. Folding and unfolding occurred mostly during the upstroke; hence, our model suggests inertial cost of the upstroke is not less than that of downstroke. The cost of accelerating the metacarpals and phalanges accounted for around 44 per cent of inertial costs, although those elements constitute only 12 per cent of wing weight. This highlights the energetic benefit afforded to bats by the decreased mineralization of the distal wing bones.

Whole-body kinematics of a fruit bat reveal the influence of wing inertia on body accelerations.

The center of mass (COM) of a flying animal accelerates through space because of aerodynamic and gravitational forces. For vertebrates, changes in the position of a landmark on the body have been widely used to estimate net aerodynamic forces. The flapping of relatively massive wings, however, might induce inertial forces that cause markers on the body to move independently of the COM, thus making them unreliable indicators of aerodynamic force. We used high-speed three-dimensional kinematics from wind tunnel flights of four lesser dog-faced fruit bats, Cynopterus brachyotis, at speeds ranging from 2.4 to 7.8 m s(-1) to construct a time-varying model of the mass distribution of the bats and to estimate changes in the position of their COM through time. We compared accelerations calculated by markers on the trunk with accelerations calculated from the estimated COM and we found significant inertial effects on both horizontal and vertical accelerations. We discuss the effect of these inertial accelerations on the long-held idea that, during slow flights, bats accelerate their COM forward during 'tip-reversal upstrokes', whereby the distal portion of the wing moves upward and backward with respect to still air. This idea has been supported by the observation that markers placed on the body accelerate forward during tip-reversal upstrokes. As in previously published studies, we observed that markers on the trunk accelerated forward during the tip-reversal upstrokes. When removing inertial effects, however, we found that the COM accelerated forward primarily during the downstroke. These results highlight the crucial importance of the incorporation of inertial effects of wing motion in the analysis of flapping flight.

Climbing flight performance and load carrying in lesser dog-faced fruit bats (Cynopterus brachyotis).

The metabolic cost of flight increases with mass, so animals that fly tend to exhibit morphological traits that reduce body weight. However, all flying animals must sometimes fly while carrying loads. Load carrying is especially relevant for bats, which experience nightly and seasonal fluctuations in body mass of 40% or more. In this study, we examined how the climbing flight performance of fruit bats (Cynopterus brachyotis; N=4) was affected by added loads. The body weights of animals were experimentally increased by 0, 7, 14 or 21% by means of intra-peritoneal injections of saline solution, and flights were recorded as animals flew upwards in a small enclosure. Using a model based on actuator disk theory, we estimated the mechanical power expended by the bats as they flew and separated that cost into different components, including the estimated costs of hovering, climbing and increasing kinetic energy. We found that even our most heavily loaded bats were capable of upward flight, but as the magnitude of the load increased, flight performance diminished. Although the cost of flight increased with loading, bats did not vary total induced power across loading treatment. This resulted in a diminished vertical velocity and thus shallower climbing angle with increased loads. Among trials there was considerable variation in power production, and those with greater power production tended to exhibit higher wingbeat frequencies and lower wing stroke amplitudes than trials with lower power production. Changes in stroke plane angle, downstroke wingtip velocity and wing extension did not correlate significantly with changes in power output. We thus observed the manner in which bats modulated power output through changes in kinematics and conclude that the bats in our study did not respond to increases in loading with increased power output because their typical kinematics already resulted in sufficient aerodynamic power to accommodate even a 21% increase in body weight.

The effect of body size on the wing movements of pteropodid bats, with insights into thrust and lift production.

In this study we compared the wing kinematics of 27 bats representing six pteropodid species ranging more than 40 times in body mass (M(b)=0.0278-1.152 kg), to determine whether wing posture and overall wing kinematics scaled as predicted according to theory. The smallest species flew in a wind tunnel and the other five species in a flight corridor. Seventeen kinematic markers on the midline and left side of the body were tracked in three dimensions. We used phylogenetically informed reduced major axis regression to test for allometry. We found that maximum wingspan (b(max)) and maximum wing area (S(max)) scaled with more positive allometry, and wing loading (Q(s)) with more negative allometry (b(max)∝M(b)(0.423); S(max)∝M(b)(0.768); Q(s)∝M(b)(0.233)) than has been reported in previous studies that were based on measurements from specimens stretched out flat on a horizontal surface. Our results suggest that larger bats open their wings more fully than small bats do in flight, and that for bats, body measurements alone cannot be used to predict the conformation of the wings in flight. Several kinematic variables, including downstroke ratio, wing stroke amplitude, stroke plane angle, wing camber and Strouhal number, did not change significantly with body size, demonstrating that many aspects of wing kinematics are similar across this range of body sizes. Whereas aerodynamic theory suggests that preferred flight speed should increase with mass, we did not observe an increase in preferred flight speed with mass. Instead, larger bats had higher lift coefficients (C(L)) than did small bats (C(L)∝M(b)(0.170)). Also, the slope of the wingbeat period (T) to body mass regression was significantly more shallow than expected under isometry (T∝M(b)(0.180)), and angle of attack (α) increased significantly with body mass [α∝log(M(b))7.738]. None of the bats in our study flew at constant speed, so we used multiple regression to isolate the changes in wing kinematics that correlated with changes in flight speed, horizontal acceleration and vertical acceleration. We uncovered several significant trends that were consistent among species. Our results demonstrate that for medium- to large-sized bats, the ways that bats modulate their wing kinematics to produce thrust and lift over the course of a wingbeat cycle are independent of body size.

Wake structure and wing kinematics: the flight of the lesser dog-faced fruit bat, Cynopterus brachyotis.

We investigated the detailed kinematics and wake structure of lesser dog-faced fruit bats (Cynopterus brachyotis) flying in a wind tunnel. High speed recordings of the kinematics were conducted to obtain three-dimensional reconstructions of wing movements. Simultaneously, the flow structure in the spanwise plane perpendicular to the flow stream was visualized using time-resolved particle image velocimetry. The flight of four individuals was investigated to reveal patterns in kinematics and wake structure typical for lower and higher speeds. The wake structure identified as typical for both speed categories was a closed-loop ring vortex consisting of the tip vortex and the limited appearance of a counter-rotating vortex near the body, as well as a small distally located vortex system at the end of the upstroke that generated negative lift. We also investigated the degree of consistency within trials and looked at individual variation in flight parameters, and found distinct differences between individuals as well as within individuals.

Echolocation call production during aerial and terrestrial locomotion by New Zealand's enigmatic lesser short-tailed bat, Mystacina tuberculata.

Linkage of echolocation call production with contraction of flight muscles has been suggested to reduce the energetic cost of flight with echolocation, such that the overall cost is approximately equal to that of flight alone. However, the pattern of call production with limb movement in terrestrially agile bats has never been investigated. We used synchronised high-speed video and audio recordings to determine patterns of association between echolocation call production and limb motion by Mystacina tuberculata Gray 1843 as individuals walked and flew, respectively. Results showed that there was no apparent linkage between call production and limb motion when bats walked. When in flight, two calls were produced per wingbeat, late in the downstroke and early in the upstroke. When bats walked, calls were produced at a higher rate, but at a slightly lower intensity, compared with bats in flight. These results suggest that M. tuberculata do not attempt to reduce the cost of terrestrial locomotion and call production through biomechanical linkage. They also suggest that the pattern of linkage seen when bats are in flight is not universal and that energetic savings cannot necessarily be explained by contraction of muscles associated with the downstroke alone.

Bats go head-under-heels: the biomechanics of landing on a ceiling.

Bats typically roost head-under-heels but they cannot hover in this position, thus, landing on a ceiling presents a biomechanical challenge. To land, a bat must perform an acrobatic flip that brings the claws of the toes in contact with the ceiling and do so gently enough as to avoid injury to its slender hindlimbs. In the present study, we sought to determine how bats land, to seek a link between landing kinematics and ceiling impact forces, and to determine whether landing strategies vary among bat species. To do this, we measured the kinematics and kinetics of landing behaviour in three species of bats as they landed on a force-measuring platform (Cynopterus brachyotis, N=3; Carollia perspicillata, N=5; Glossophaga soricina, N=5). Kinematics were similar for all bats within a species but differed among species. C. brachyotis performed four-point landings, during which body pitch increased until the ventral surface of the body faced the ceiling and the thumbs and hindlimbs simultaneously grasped the surface. Bats of the other two species performed two-point landings, whereby only the hindlimbs made contact with the ceiling. During these two-point landings, the hindlimbs were drawn up the side of the body to come in contact with the ceiling, causing simultaneous changes in body pitch, roll and yaw over the course of the landing sequence. Right-handed and left-handed forms of the two-point landing were observed, with individuals often switching back and forth between them among landing events. The four-point landing of C. brachyotis resulted in larger peak forces (3.7+/-2.4 body weights; median +/- interquartile range) than the two-point landings of C. perspicillata (0.8+/-0.6 body weights) or G. soricina (0.8+/-0.2 body weights). Our results demonstrate that the kinematics and kinetics of landing vary among bat species and that there is a correlation between the way a bat moves its body when it lands and the magnitude of peak impact force it experiences during that landing. We postulate that these interspecific differences in impact force could result because of stronger selective pressure for gentle landing in cave-roosting (C. perspicillata, G. soricina) versus foliage-roosting (C. brachyotis) species.

Quantifying the complexity of bat wing kinematics.

Body motions (kinematics) of animals can be dimensionally complex, especially when flexible parts of the body interact with a surrounding fluid. In these systems, tracking motion completely can be difficult, and result in a large number of correlated measurements, with unclear contributions of each parameter to performance. Workers typically get around this by deciding a priori which variables are important (wing camber, stroke amplitude, etc.), and focusing only on those variables, but this constrains the ability of a study to uncover variables of influence. Here, we describe an application of proper orthogonal decomposition (POD) for assigning importances to kinematic variables, using dimensional complexity as a metric. We apply this method to bat flight kinematics, addressing three questions: (1) Does dimensional complexity of motion change with speed? (2) What body markers are optimal for capturing dimensional complexity? (3) What variables should a simplified reconstruction of bat flight include in order to maximally reconstruct actual dimensional complexity? We measured the motions of 17 kinematic markers (20 joint angles) on a bat (Cynopterus brachyotis) flying in a wind tunnel at nine speeds. Dimensional complexity did not change with flight speed, despite changes in the kinematics themselves, suggesting that the relative efficacy of a given number of dimensions for reconstructing kinematics is conserved across speeds. By looking at subsets of the full 17-marker set, we found that using more markers improved resolution of kinematic dimensional complexity, but that the benefit of adding markers diminished as the total number of markers increased. Dimensional complexity was highest when the hindlimb and several points along digits III and IV were tracked. Also, we uncovered three groups of joints that move together during flight by using POD to quantify correlations of motion. These groups describe 14/20 joint angles, and provide a framework for models of bat flight for experimental and modeling purposes.

Ultrasonic sound as an indicator of acute pain in laboratory mice.

In response to pain, mice may vocalize at frequencies above the range of human hearing (greater than 20 kHz). To determine whether an ultrasonic recording system is a reliable tool for assessing acute pain, we measured audible and ultrasonic vocalization in mice subjected to either nonpainful or potentially painful procedures performed routinely in animal facilities. Data were collected from 109 weanling mice (Mus musculus; B6, 129S6-Stab 5b) scheduled for 2 potentially painful procedures: DNA testing by tail snip and identification by ear notching. The mice each were assigned randomly to 1 of 4 groups: 1) actual tail snip, 2) sham tail snip, 3) actual ear notch, or 4) sham ear notch. Vocalizations during the treatments were recorded with an ultrasonic recorder. Most mice (65%; n = 55) demonstrated no vocal response to the potentially painful procedures. More mice that received actual tail snips produced audible sounds (11 of 29 mice) than did those that underwent sham tail snips (0 of 30 mice). In addition, audible vocalizations occurred more frequently during ear notch procedures (8 of 26 mice) than during sham ear-notch manipulations (2 of 24 mice). For all 20 of the mice that produced ultrasonic vocalizations, these calls were accompanied by simultaneous audible components. We conclude that ultrasonic vocalizations do not provide any more information than do audible vocalizations for assessing responses to potentially painful procedures. In addition, because many mice made no sound at all after a potentially painful stimulus, vocalizations generally are not good metrics of acute pain in laboratory mice. Alternatively, the lack of vocalizations in many of the mice may suggest that tail snipping and ear notching are not particularly painful procedures for most of these mice.

Terrestrial locomotion of the New Zealand short-tailed bat Mystacina tuberculata and the common vampire bat Desmodus rotundus.

Bats (Chiroptera) are generally awkward crawlers, but the common vampire bat (Desmodus rotundus) and the New Zealand short-tailed bat (Mystacina tuberculata) have independently evolved the ability to manoeuvre well on the ground. In this study we describe the kinematics of locomotion in both species, and the kinetics of locomotion in M. tuberculata. We sought to determine whether these bats move terrestrially the way other quadrupeds do, or whether they possess altogether different patterns of movement on the ground than are observed in quadrupeds that do not fly. Using high-speed video analyses of bats moving on a treadmill, we observed that both species possess symmetrical lateral-sequence gaits similar to the kinematically defined walks of a broad range of tetrapods. At high speeds, D. rotundus use an asymmetrical bounding gait that appears to converge on the bounding gaits of small terrestrial mammals, but with the roles of the forelimbs and hindlimbs reversed. This gait was not performed by M. tuberculata. Many animals that possess a single kinematic gait shift with increasing speed from a kinetic walk (where kinetic and potential energy of the centre of mass oscillate out of phase from each other) to a kinetic run (where they oscillate in phase). To determine whether the single kinematic gait of M. tuberculata meets the kinetic definition of a walk, a run, or a gait that functions as a walk at low speed and a run at high speed, we used force plates and high-speed video recordings to characterize the energetics of the centre of mass in that species. Although oscillations in kinetic and potential energy were of similar magnitudes, M. tuberculata did not use pendulum-like exchanges of energy between them to the extent that many other quadrupedal animals do, and did not transition from a kinetic walk to kinetic run with increasing speed. The gait of M. tuberculata is kinematically a walk, but kinetically run-like at all speeds.

Testing the hindlimb-strength hypothesis: non-aerial locomotion by Chiroptera is not constrained by the dimensions of the femur or tibia.

In the evolution of flight bats appear to have suffered a trade-off; they have become poor crawlers relative to terrestrial mammals. Capable walking does occur in a few disparate taxa, including the vampire bats, but the vast majority of bats are able only to shuffle awkwardly along the ground, and the morphological bases of differences in crawling ability are not currently understood. One widely cited hypothesis suggests that the femora of most bats are too weak to withstand the compressive forces that occur during terrestrial locomotion, and that the vampire bats can walk because they possess more robust hindlimb skeletons. We tested a prediction of the hindlimb-strength hypothesis: that during locomotion, the forces produced by the hindlimbs of vampire bats should be larger than those produced by the legs of poorly crawling bats. Using force plates we compared the hindlimb forces produced by two species of vampire bats that walk well, Desmodus rotundus (N=8) and Diaemus youngi (N=2), to the hindlimb forces produced during over-ground shuffling by a similarly sized bat that is a poor walker (Pteronotus parnellii; N=6). Peak hindlimb forces produced by P. parnellii were larger (ANOVA; P<0.05; N=65) and more variable (93.5+/-36.6% body weight, mean +/- s.d.) than those of D. rotundus (69.3+/-8.1%) or D. youngi (75.0+/-6.2%). Interestingly, the vertical components of peak force were equivalent among species (P>0.6), indicating similar roles for support of body weight by the hindlimbs in the three species. We also used a simple engineering model of bending stress to evaluate the support capabilities of the hindlimb skeleton from the dimensions of 113 museum specimens in 50 species. We found that the hindlimb bones of vampires are not built to withstand larger forces than those of species that crawl poorly. Our results show that the legs of poorly crawling bats should be able to withstand the forces produced during coordinated crawling of the type used by the agile vampires, and this indicates that some mechanism other than hindlimb bone thickness, such as myology of the pectoral girdle, limits the ability of most bats to crawl.

Biomechanics: independent evolution of running in vampire bats.

Most tetrapods have retained terrestrial locomotion since it evolved in the Palaeozoic era, but bats have become so specialized for flight that they have almost lost the ability to manoeuvre on land at all. Vampire bats, which sneak up on their prey along the ground, are an important exception. Here we show that common vampire bats can also run by using a unique bounding gait, in which the forelimbs instead of the hindlimbs are recruited for force production as the wings are much more powerful than the legs. This ability to run seems to have evolved independently within the bat lineage.