Gliding flight in Chrysopelea: turning a snake into a wing

Although many cylindrical animals swim through water, flying snakes of the genus Chrysopelea are the only limbless animals that glide through air. Despite a lack of limbs, these snakes can actively launch by jumping, maintain a stable glide path without obvious control surfaces, maneuver, and safely land without injury. Jumping takeoffs employ vertically looped kinematics that seem to be different than any other behavior in limbless vertebrates, and their presence in a closely related genus suggests that gap-crossing may have been a behavioral precursor to the evolution of gliding in snakes. Change in shape of the body by dorsoventral flattening and high-amplitude aerial undulation comprise two key features of snakes' gliding behavior. As the snake becomes airborne, the body flattens sequentially from head to vent, forming a cross-sectional shape that is roughly triangular, with a flat surface and lateral "lips" that protrude ventrally on each side of the body; these may diminish toward the vent. This shape likely provides the snake with lift coefficients that peak at high angles of attack and gentle stall characteristics. A glide trajectory is initiated with the snake falling at a steep angle. As the snake rotates in the pitch axis, it forms a wide "S" shape and begins undulating in a complex three-dimensional pattern, with the body angled upward relative to the glide path. The head moves side-to-side, sending traveling waves posteriorly toward the tail, while the body (most prominently, the posterior end) oscillates in the vertical axis. These active movements while gliding are substantially different and more dynamic than those used by any other animal glider. As the snake gains forward speed, the glide path becomes less steep, reaching minimally recorded glide angles of 13°. In general, smaller snakes appear to be more proficient gliders. Chrysopelea paradisi can also maneuver and land either on the ground or on vegetation, but these locomotor behaviors have not been studied in detail. Future work aims to understand the mechanisms of production and control of force in takeoff, gliding, and landing, and to identify the musculoskeletal adaptations that enable this unique form of locomotion.     

Animal aloft: the origins of aerial behavior and flight

Diverse taxa of animals exhibit remarkable aerial capacities, including jumping, mid-air righting, parachuting, gliding, landing, controlled maneuvers, and flapping flight. The origin of flapping wings in hexapods and in 3 separate lineages of vertebrates (pterosaurs, bats, and birds) greatly facilitated subsequent diversification of lineages, but both the paleobiological context and the possible selective pressures for the evolution of wings remain contentious. Larvae of various arboreal hemimetabolous insects, as well as many adult canopy ants, demonstrate the capacity for directed aerial descent in the absence of wings. Aerial control in the ancestrally wingless archaeognathans suggests that flight behavior preceded the origins of wings in hexapods. In evolutionary terms, the use of winglets and partial wings to effect aerial righting and maneuvers could select for enhanced appendicular motions, and ultimately lead to powered flight. Flight behaviors that involve neither flapping nor wings are likely to be much more widespread than is currently recognized. Further characterization of the sensory and biomechanical mechanisms used by these aerially capable taxa can potentially assist in reconstruction of ancestral winged morphologies and facilitate our understanding of the origins of flight.     

Introductory remarks on this issue. On the role of the ampulla in disturbances of vestibular function.

The article reports on the use of pigeons as models in the study of vestibular dysfunction. In the experiment reported, the cupula was loosened by raising the endolymph pressure on one side of the ampulla. The pigeon eyes showed a nystagmus. One day later, the pigeons were able to stand upright, but with head tilted toward the side of operation. The pigeons were able to fly within 15 days. Vestibular defects added in some experimental birds resulted in an inability to regain flying capacity.     

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.     

The biology of gliding in flying lizards (genus Draco) and their fossil and extant analogs

The flying lizards of the genus Draco are among the most remarkable and successful clades of gliding vertebrates. Here, we evaluate the evolution of gliding in Draco and other lizards, describe the suite of morphological innovations that characterize Draco, discuss the ecological context of gliding in this genus, describe functions of their patagial membranes that are not related to gliding, and summarize the interspecific allometry of the Draco gliding apparatus, as well as the corresponding consequences for their now empirically quantified gliding performance. Several fossil reptilian lineages had morphologies similar to that of modern Draco, with patagial membranes supported by elongated ribs or rib-like dermal structures. Using Draco's snout-vent length/mass relationships, we provide improved estimates of wing loading for three of these fossil gliders (Icarosaurus seifkeri, Kuehneosaurus sp., Coelurosauravus elivensis) and then estimate absolute gliding performance for each taxon by extrapolating from Draco's wing loading/glide performance relationship. We find that I. seifkeri likely represented the best nonflapping terrestrial vertebrate glider yet described, whereas the larger Kuehneosaurus and Coelurosauravus probably required high descent velocities to achieve sufficient lift for gliding, with commensurately greater height loss with each glide.     

Evolution of skull and body shape in Triturus newts reconstructed from three‐dimensional morphometric data and phylogeny

To explore the relationship between morphological change and species diversification, we reconstructed the evolutionary changes in skull size, skull shape, and body elongation in a monophyletic group of eight species that make up salamander genus Triturus. Their well‐studied phylogenetic relationships and the marked difference in ecological preferences among five species groups makes this genus an excellent model system for the study of morphological evolution. The study involved three‐dimensional imagery of the skull and the number of trunk vertebrae, in material that represents the morphological, spatial, and molecular diversity of the genus. Morphological change largely followed the pattern of descent. The reconstruction of ancestral skull shape indicated that morphological change was mostly confined to two episodes, corresponding to the ancestral lineage that all crested newts have in common and the Triturus dobrogicus lineage. When corrected for common descent, evolution of skull shape was correlated to change in skull size. Also, skull size and shape, as well as body shape, as inferred from the number of trunk vertebrae, were correlated, indicating a marked impact of species' ecological preferences on morphological evolution, accompanied by a series of niche shifts, with the most pronounced one in the T. dobrogicus lineage. The presence of phylogenetic signal and correlated evolutionary changes in skull and body shape suggested complex interplay of niche shifts, natural selection, and constraints by a common developmental system. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 243–255.     

Dragondrop: a novel passive mechanism for aerial righting in the dragonfly

Dragonflies perform dramatic aerial manoeuvres when chasing targets but glide for periods during cruising flights. This makes dragonflies a great system to explore the role of passive stabilizing mechanisms that do not compromise manoeuvrability. We challenged dragonflies by dropping them from selected inverted attitudes and collected 6-degrees-of-freedom aerial recovery kinematics via custom motion capture techniques. From these kinematic data, we performed rigid-body inverse dynamics to reconstruct the forces and torques involved in righting behaviour. We found that inverted dragonflies typically recover themselves with the shortest rotation from the initial body inclination. Additionally, they exhibited a strong tendency to pitch-up with their head leading out of the manoeuvre, despite the lower moment of inertia in the roll axis. Surprisingly, anaesthetized dragonflies could also complete aerial righting reliably. Such passive righting disappeared in recently dead dragonflies but could be partially recovered by waxing their wings to the anaesthetised posture. Our kinematics data, inverse dynamics model and wind-tunnel experiments suggest that the dragonfly''s long abdomen and wing posture generate a rotational tendency and passive attitude recovery mechanism during falling. This work demonstrates an aerodynamically stable body configuration in a flying insect and raises new questions in sensorimotor control for small flying systems.     

Aerodynamic Characteristics of a Feathered Dinosaur Measured Using Physical Models. Effects of Form on Static Stability and Control Effectiveness

We report the effects of posture and morphology on the static aerodynamic stability and control effectiveness of physical models based on the feathered dinosaur, Microraptor gui, from the Cretaceous of China. Postures had similar lift and drag coefficients and were broadly similar when simplified metrics of gliding were considered, but they exhibited different stability characteristics depending on the position of the legs and the presence of feathers on the legs and the tail. Both stability and the function of appendages in generating maneuvering forces and torques changed as the glide angle or angle of attack were changed. These are significant because they represent an aerial environment that may have shifted during the evolution of directed aerial descent and other aerial behaviors. Certain movements were particularly effective (symmetric movements of the wings and tail in pitch, asymmetric wing movements, some tail movements). Other appendages altered their function from creating yaws at high angle of attack to rolls at low angle of attack, or reversed their function entirely. While M. gui lived after Archaeopteryx and likely represents a side experiment with feathered morphology, the general patterns of stability and control effectiveness suggested from the manipulations of forelimb, hindlimb and tail morphology here may help understand the evolution of flight control aerodynamics in vertebrates. Though these results rest on a single specimen, as further fossils with different morphologies are tested, the findings here could be applied in a phylogenetic context to reveal biomechanical constraints on extinct flyers arising from the need to maneuver.     

Mechanisms and implications of animal flight maneuverability

Accelerations and directional changes of flying animals derivefrom interactions between aerodynamic force production and theinertial resistance of the body to translation and rotation.Anatomical and allometric features of body design thus mediatethe rapidity of aerial maneuvers. Both translational and rotationalresponsiveness of the body to applied force decrease with increasedtotal mass. For flying vertebrates, contributions of the relativelyheavy wings to whole-body rotational inertia are substantial,whereas the relatively light wings of many insect taxa suggestthat rotational inertia is dominated by the contributions ofbody segments. In some circumstances, inertial features of wingdesign may be as significant as are their aerodynamic propertiesin influencing the rapidity of body rotations. Stability inflight requires force and moment balances that are usually attainedvia bilateral symmetry in wingbeat kinematics, whereas bodyroll and yaw derive from bilaterally asymmetric movements ofboth axial and appendicular structures. In many flying vertebrates,use of the tail facilitates the generation of aerodynamic torquesand substantially enhances quickness of body rotation. Geometricalconstraints on wingbeat kinematics may limit total force productionand thus accelerational capacity in certain behavioral circumstances.Unitary limits to animal flight performance and maneuverabilityare unlikely, however, given varied and context-specific interactionsamong anatomical, biomechanical, and energetic features of design.     

A novel resource-service mutualism between bats and pitcher plants

Mutualistic relationships between vertebrates and plants apart from the pollen and seed-dispersal syndromes are rare. At first view, carnivorous pitcher plants of the genus Nepenthes seem to be highly unlikely candidates for mutualistic interactions with animals, as they form dimorphic terrestrial and aerial pitchers that trap arthropods and small vertebrates. Surprisingly, however, the aerial pitchers of Nepenthes rafflesiana variety elongata are poor insect traps, with low amounts of insect-attractive volatile compounds and low amounts of digestive fluid. Here, we show that N. rafflesiana elongata gains an estimated 33.8 per cent of the total foliar nitrogen from the faeces of Hardwicke's woolly bats (Kerivoula hardwickii hardwickii) that exclusively roost in its aerial pitchers. This is the first case in which the faeces-trapping syndrome has been documented in a pitcher plant that attracts bats and only the second case of a mutualistic association between a carnivorous plant and a mammal to date.     

Moving in a moving medium: new perspectives on flight

One of the defining features of the aerial environment is its variability; air is almost never still. This has profound consequences for flying animals, affecting their flight stability, speed selection, energy expenditure and choice of flight path. All these factors have important implications for the ecology of flying animals, and the ecosystems they interact with, as well as providing bio-inspiration for the development of unmanned aerial vehicles. In this introduction, we touch on the factors that drive the variability in airflows, the scales of variability and the degree to which given airflows may be predictable. We then summarize how papers in this volume advance our understanding of the sensory, biomechanical, physiological and behavioural responses of animals to air flows. Overall, this provides insight into how flying animals can be so successful in this most fickle of environments.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

The descended larynx is not uniquely human

Morphological modifications of vocal anatomy are widespread among vertebrates, and the investigation of the physiological mechanisms and adaptive functions of such variants is an important focus of research into the evolution of communication. The "descended larynx" of adult humans has traditionally been considered unique to our species, representing an adaptation for articulate speech, and debate concerning the position of the larynx in extinct hominids assumes that a lowered larynx is diagnostic of speech and language. Here, we use bioacoustic analyses of vocalizing animals, together with anatomical analyses of functional morphology, to document descended larynges in red and fallow deer. The resting position of the larynx in males of these species is similar to that in humans, and, during roaring, red-deer stags lower the larynx even further, to the sternum. These findings indicate that laryngeal descent is not uniquely human and has evolved at least twice in independent lineages. We suggest that laryngeal descent serves to elongate the vocal tract, allowing callers to exaggerate their perceived body size by decreasing vocal-tract resonant frequencies. Vocal-tract elongation is common in birds and is probably present in additional mammals. Size exaggeration provides a non-linguistic alternative hypothesis for the descent of the larynx in human evolution.     

Phylogeny and cryptic diversification in Southeast Asian flying geckos

The closed-canopy forests of Southeast Asia are home to an impressive number of vertebrates that have independently evolved morphologies that enhance directed aerial descent (gliding, parachuting). These assemblages include numerous mammal, frog, snake, and lizard clades. Several genera of gekkonid lizards, in particular, have evolved specialized structures such as cutaneous expansions, flaps, and midbody patagia, that enhance lift generation in the context of unique gliding and parachuting locomotion. The genus Ptychozoon represents arguably the most morphologically extreme, highly specialized clade of gliding geckos. Despite their notoriety and celebrated locomotor ability, members of the genus Ptychozoon have never been the subject of a species-level molecular phylogenetic analysis. In this paper, we utilize molecular sequence data from mitochondrial and nuclear gene fragments to estimate the evolutionary relationships of this unique group of flying geckos. Capitalizing on the recent availability of genetic samples for even the rarest of known species, we include the majority of known taxa and use model-based phylogenetic methods to reconstruct their evolutionary history. Because one species, P. kuhli, exhibits an unusually wide distribution coupled with an impressive range of morphological variation, we additionally use intensive phylogeographic/population genetic sampling, phylogenetic network analyses, and Bayesian species delimitation procedures to evaluate this taxon for the possible presence of cryptic evolutionary lineages. Our results suggest that P. kuhli may consist of between five and nine unrecognized, distinct species. Although we do not elevate these lineages to species status here, our findings suggest that lineage diversity in Ptychozoon is likely dramatically underestimated.     

Morphometric investigations of sensory vestibular structures in tadpoles (Xenopus laevis) after a spaceflight: implications for microgravity-induced alterations of the vestibuloocular reflex

In lower vertebrates, gravity deprivation by orbital flights modifies the vestibuloocular reflex. Using the amphibian Xenopus laevis, the experiments should clarify to which extent macular structures of the labyrinth are responsible for these modifications. In particular, the shape of otoconia and number and size of sensory macular cells expressing CalBindin were considered. CalBindin is common in mature sensory cells including vestibular hair cells and is probably involved in otoconia formation. Two developmental stages were used for this study: stage 26/27 embryos, which were unable to perform the roll-induced vestibuloocular reflex (rVOR) at onset of microgravity, and stage 45 tadpoles, which had already developed the reflex. The main observations were that the developmental progress of the animals was not affected by microgravity; that in the young tadpole group with normal body shape the rVOR was not modified by microgravity, while in the older group with microgravity experience, the rVOR was augmented; and that significant effects on the shape of otoconia and on the number and size of CalBindin-expressing cells of the labyrinthine maculae cells were absent. In addition, behavioural data were never significantly correlated with morphological features of macular structures such as size and number of CalBindin-expressing cells. It is postulated that mechanisms of vestibular adaptation to microgravity during early development are probably based on mechanisms located in central structures of the vestibular system.     

Evolution of the Role of RA and FGF Signals in the Control of Somitogenesis in Chordates

During vertebrate development, the paraxial mesoderm becomes segmented, forming somites that will give rise to dermis, axial skeleton and skeletal muscles. Although recently challenged, the "clock and wavefront" model for somitogenesis explains how interactions between several cell-cell communication pathways, including the FGF, RA, Wnt and Notch signals, control the formation of these bilateral symmetric blocks. In the cephalochordate amphioxus, which belongs to the chordate phylum together with tunicates and vertebrates, the dorsal paraxial mesendoderm also periodically forms somites, although this process is asymmetric and extends along the whole body. It has been previously shown that the formation of the most anterior somites in amphioxus is dependent upon FGF signalling. However, the signals controlling somitogenesis during posterior elongation in amphioxus are still unknown. Here we show that, contrary to vertebrates, RA and FGF signals act independently during posterior elongation and that they are not mandatory for posterior somites to form. Moreover, we show that RA is not able to buffer the left/right asymmetry machinery that is controlled through the asymmetric expression of Nodal pathway actors. Our results give new insights into the evolution of the somitogenesis process in chordates. They suggest that RA and FGF pathways have acquired specific functions in the control of somitogenesis in vertebrates. We propose that the "clock and wavefront" system was selected specifically in vertebrates in parallel to the development of more complex somite-derived structures but that it was not required for somitogenesis in the ancestor of chordates.     

Evidence for repeated acquisition and loss of complex body-form characters in an insular clade of Southeast Asian semi-fossorial skinks

Evolutionary simplification, or loss of complex characters, is a major theme in studies of body-form evolution. The apparently infrequent evolutionary reacquisition of complex characters has led to the assertion (Dollo's Law) that once lost, complex characters may be impossible to re-evolve, at least via the exact same evolutionary process. Here, we provide one of the most comprehensive, fine-scale analyses of squamate body-form evolution to date, introducing a new model system of closely related, morphologically variable, lizards. Our phylogenetic results support independent instances of complete limb loss as well as multiple instances of digit and external ear opening loss and re-acquisition. Even more striking, we find strong statistical support for the re-acquisition of a pentadactyl body form from a digit-reduced ancestor. Our study reveals that species of the genus Brachymeles exemplify regions of morphospace (body plans) previously undocumented in squamates. Our findings have broad, general implications for body-form evolution in burrowing vertebrates: whatever constraints have shaped trends in morphological evolution among other squamate groups (excluding Bipes) have been lost in this one exemplary clade. The results of our study join a nascent body of literature showing strong statistical support for character loss, followed by evolutionary re-acquisition of complex structures associated with a generalized pentadactyl body form.     

Animal flight dynamics I. Stability in gliding flight

Stability is as essential to flying as lift itself, but previous discussions of how flying animals maintain stability have been limited in both number and scope. By developing the pitching moment equations for gliding animals and by discussing potential sources of roll and yaw stability, we consider the various sources of static stability used by gliding animals. We find that gliding animals differ markedly from aircraft in how they maintain stability. In particular, the pendulum stability provided when the centre of gravity lies below the wings is a much more important source of stability in flying animals than in most conventional aircraft. Drag-based stability also appears to be important for many gliding animals, whereas in aircraft, drag is usually kept to a minimum. One unexpected consequence of these differences is that the golden measure of static pitching stability in aircraft--the static margin--can only strictly be applied to flying animals if the equilibrium angle of attack is specified. We also derive several rules of thumb by which stable fliers can be identified. Stable fliers are expected to exhibit one or more of the following features: (1) Wings that are swept forward in slow flight. (2) Wings that are twisted down at the tips when swept back (wash-out) and twisted up at the tips when swept forwards (wash-in). (3) Additional lifting surfaces (canard, hindwings or a tail) inclined nose-up to the main wing if they lie forward of it, and nose-down if they lie behind it (longitudinal dihedral). Each of these predictions is directional--the opposite is expected to apply in unstable animals. In addition, animals with reduced stability are expected to display direct flight patterns in turbulent conditions, in contrast to the erratic flight patterns predicted for stable animals, in which large restoring forces are generated. Using these predictions, we find that flying animals possess a far higher degree of inherent stability than has generally been recognized. This conclusion is reinforced by measurements of the relative positions of the centres of gravity and lift in birds, which suggest that the wings alone may be sufficient to provide longitudinal static stability. Birds may therefore resemble tailless aircraft more closely than conventional aircraft with a tailplane.     

Optimization of the mechanical performance of a two-duct semicircular duct system--part 3: the positioning of the ducts in the head

In the majority of vertebrates, the horizontal duct of the vestibular system lies approximately in the yawing plane of the head. The positioning of the vertical ducts, however, is not in the pitch- and roll planes but the vertical ducts generally lie under an angle of about 30-45 degrees relative to the medial plane. Using the equations for a hydrodynamically interconnected two-duct system, optimal positions of the vertical and horizontal ducts in different vertebrate groups can be derived. It was stated that the mean response of the vertical ducts should be optimized. This leads to a symmetrical positioning of the vertical ducts with respect to the medial plane. In all observed vertebrate groups, a solution of mu =(pi-alpha)/2 is found (mu is the angle of the vertical ducts relative to the medial plane, alpha is the angle between the vertical duct planes). For alpha=90 degrees, this provides an equal sensitivity for pitch- and roll- movements. For alpha>90 degrees, a larger sensitivity for pitch movements is obtained, at the expense of a lower sensitivity for roll movements. It is argued that the angle alpha between the vertical ducts may vary from 90 to 120 degrees. In most vertebrates, the centre of mass is stabilized by e.g. fins, tri- or quadrupedal stability, a crawling body or upside-down resting positions (e.g. bats). Birds are generally biped, so in walking they are also rather sensitive to roll. These features are related to labyrinth positioning in the head.     

The erroneous courtship hypothesis: do insects really engage in aerial wars of attrition?

Males of various flying insects perform conspicuous aerial interactions around their mating stations. The broadly accepted interpretation of their aerial interaction is a war of attrition, where two contestants perform costly displays, and the one that reaches its cost threshold earlier gives up. The implicit but important requirement in this model is that some forces that match the intensity of display of the two contestants are necessary, and failure to enforce matching allows foul contestants that delay or stop their display to avoid paying contest costs. In addition, wars of attrition require flying insects to distinguish the sex of flying conspecifics because their aerial interactions begin when intruders fly into the territory. We investigated past research on the behaviour of odonates and butterflies aiming to clarify whether the two prerequisites of wars of attrition are fulfilled: (1) contestants can inflict substantial costs on nondisplaying opponents and (2) contestants can discriminate the sex of flying conspecifics. In odonates, we found an abundance of evidence suggesting that contests involve physical attack and that the ability of sexual discrimination is sufficient. Therefore, wars of attrition may occur in territorial odonates. In butterflies, however, we could not find any evidence that the two prerequisites are filled. The aerial interactions of butterflies are better interpreted as courtship between sexually active males (the erroneous courtship hypothesis). Based on these results, we discuss future directions of research on the aerial contests of flying insects.