Cranial kinesis facilitates quick retraction of stuck woodpecker beaks.

Much like nails that are hammered into wood, the beaks of woodpeckers regularly get stuck upon impact. A kinematic video analysis of pecking by black woodpeckers shows how they manage to quickly withdraw their beaks, revealing a two-phase pattern: first a few degrees of beak-tip-down rotation about the nasofrontal hinge causes the tip of the upper beak to be retruded while its proximal end is lifted. Next, the head is lifted, causing beak-tip-up rotation about the nasofrontal hinge while the lower beak starts retruding and initiates the final freeing. We hypothesise that these consecutive actions, taking place in about 0.05 s, facilitate beak retraction by exploiting the presumably low frictional resistance between the upper and lower beak keratin surfaces, allowing them to slide past each other. It also demonstrates the counter-intuitive value of maintaining cranial kinesis in a species adapted to deliver forceful impacts.

A biaxial tensional model for early vertebrate morphogenesis.

We propose a simple biaxial tensional model which is able to reproduce at a qualitative level several aspects of early stages of vertebrate morphogenesis. The model is based on subsequent excitable contractions of an orthoradial and periclinal (radial) set of contracting lines, which generate first the basic embryonic pattern (a motile tube), and second the lateral orifices such as ears, eyes, mouth, gills, etc. An important aspect of the model is the self-arresting character of the process, akin to wound healing. At later stages, the biaxial lines may also work in extension, and this generates a developmental feedback which is quadratic with respect to curvature.

Modeling intervertebral articulation: The rotule à doigt mechanical joint (RAD) in birds and mammals.

The vertebrate skeleton is composed of articulated bones. Most of the articulations are classically described using mechanical joints, except the intervertebral joint. The aim of this study was to identify a joint model with the same mechanical features as the cervical joints. On the neck vertebrae, six articular surfaces participate in the joint: the cranial part of the centrum and the facets of the two prezygapophyses of a vertebra articulate on the caudal part of the centrum and the two articular facets of the postzygapophyses of the previous vertebra. We used the intervertebral joints of the birds neck to identify the mechanical joint representing intervertebral linkage. This link was described in the literature as a joint allowing two or three rotations and no translation. These features correspond to the rotule à doigt (RAD) joint, a ball and socket joint with a pin. We compared the RAD joint to the postaxial intervertebral joints of the avian neck and found it a suitable model to determine the geometrical features involved in the joint mobility. The difference in the angles of virtual axes linking the geometrical center of the centrum to the zygapophysis surfaces determines the mean dorsoventral flexion of the joint. It also helps to limit longitudinal rotation. The orientation of the zygapophysis surfaces determines the range of motion in both dorsoventral and lateral flexion. The overall system prevents dislocation. The model was validated on 13 joints of a vulture neck and 11 joints of a swallow neck and on one joint (C6-C7) in each of three mammal species: the wolf (Canis lupus), mole (Talpa europaea), and human (Homo sapiens). The RAD mechanical joint was found in all vertebral articulations. This validation of the model on different species shows that the RAD intervertebral joint model makes it possible to extract the parameters that guide and limit the mobility of the cervical spine from the complex shape of the vertebrae and to compare them in interspecific studies.

Gulper, ripper and scrapper: anatomy of the neck in three species of vultures.

The head-neck system of birds is a highly complex structure that performs a variety of demanding and competing tasks. Morphofunctional adaptations to feeding specializations have previously been identified in the head and neck, but performance is also influenced by other factors such as its phylogenetic history. In order to minimize the effects of this factor, we here analyzed the anatomy of three closely related vultures that distinctly differ in feeding strategy. Vultures, as obligate scavengers, have occupied a special ecological niche by exclusively feeding on carrion. However, competition among sympatric vultures led to ecological differences such as preference of certain types of food from a carcass. Via comparative dissections we systematically described the craniocervical anatomy in the Griffon vulture (Gyps fulvus), the Cinereous vulture (Aegypius monachus) and the Hooded vulture (Necrosyrtes monachus) that exploit the same food resources in different ways. Our results revealed differences in the number of cervical vertebrae, in the morphology of the atlas-axis complex as well as in the neck musculature despite overall similarities in the musculoskeletal system. Gulpers, rippers and scrappers adopt specific postures while feeding from a carcass, but the cervical vertebral column is indispensable to position the head during all kinds of behavior. The great range of demands may explain the conservation of the overall muscle topography of the neck across the studied taxa.

Extensive chondroid bone in juvenile duck limbs hints at accelerated growth mechanism in avian skeletogenesis.

Modern altricial birds are the fastest growing vertebrates, whereas various degrees of precocity (functional maturity) result in slower growth. Diaphyseal osteohistology, the best proxy for inferring relative growth rates in fossils, suggests that in the earliest birds, posthatching growth rates were more variable than in modern representatives, with some showing considerably slow growth that was attributed to their assumed precocial flight abilities. For finding clues how precocial or altricial skeletogenesis and related growth acceleration could be traced in avian evolution, as a case study we investigated the growing limb diaphyseal histology in an ontogenetic series of ducks which, among several other avian taxa, show a combination of altricial wing and precocial leg development. Here we report the unexpected discovery that chondroid bone, a skeletal tissue family intermediate between cartilage and bone, extensively contributes to the development of limb bone shaft in ducks up to at least 30 days posthatching age. To our knowledge, chondroid bone has never been reported in such quantities and with an ontogenetically extended deposition period in post-embryonic, non-pathological periosteal bone formation of any tetrapod limb. It shows transitional cellular/lacunar morphologies and matrix staining properties between cartilage and woven bone and takes a significant part in the diametric growth of the limb bone shaft. Its amount and distribution through duckling ontogeny seems to be associated with the disparate functional and growth trajectories of the altricial wings vs. precocial legs characteristic of duck limb development. The presence of isogenous cell groups in the periosteal chondroid bone implies that cartilage-like interstitial growth took place before matrix mineralization complementing appositional bone growth. Based on these characteristics and on its fast formation rate in all previously reported normal as well as pathological cases, we suggest that chondroid bone in ducks significantly accelerates diametric limb bone growth. Related to this growth acceleration, we hypothesize that chondroid bone may be generally present in the growing limb bones of modern birds and hence may have key skeletogenic importance in achieving extreme avian growth rates and placing birds among the fastest growing vertebrates. Thus, we encourage future studies to test this hypothesis by investigating the occurrence of chondroid bone in a variety of precocial and altricial bird species, and to explore the presence of similar tissues in the growing limbs of other extant and extinct tetrapods in order to understand the evolutionary significance of chondroid bone in accelerated appendicular skeletogenesis.

How to walk carrying a huge egg? Trade-offs between locomotion and reproduction explain the special pelvis and leg anatomy in kiwi (Aves; Apteryx spp.).

Kiwi (Aves; genus Apteryx) are famous for laying an enormous egg in comparison with their relatively small body size. Considering the peculiar gait of this flightless bird, we suspected the existence of morpho-functional trade-offs between reproduction and locomotion. To understand how structural constraints, imposed by a large egg size, might influence the terrestrial locomotion of Apteryx, we analysed the anatomy of the limb osteomuscular system in two species of kiwi (Apteryx mantelli and Apteryx owenii). We performed detailed dissections and brought to light specific anatomical features of kiwi, in comparison with other ratites and neognathous birds. Our osteological study revealed a strongly curved pelvis, a rigid tail, and enlarged ribs. Our myology study showed an unusual location of the caudofemoralis muscle origin and insertion. The insertion of the pars pelvica along the entire caudal face of the femur, contrasts with the proximal insertion usually seen in other birds. Additionally, the pars caudalis originates along the entire tail, whereas it only inserts on the uropygium in the other birds. To interpret these specificities from a functional point of view, we built three-dimensional osteomuscular models based on computed tomography scans, radiographies and our dissections. We chose three postures associated with reproductive constraints: the standing position of a gravid compared with a non-gravid bird, as well as the brooding position. The 3D model of the brooding position suggested that the enlarged ribs could support the bodyweight when leaning on the huge egg in both males and females. Moreover, we found that in gravid females, the unusual shape of the pelvis and tail allowed the huge egg to sit ventrally below the pelvis, whereas it is held closer to the rachis in other birds. The specific conformation of the limb and the insertions of the two parses of the caudofemoralis help to maintain the tail flexed, and to keep the legs adducted when carrying the egg. The caudal location of the hip and its flexed position explains the long stance phase during the strange gait of kiwi, revealing the functional trade-off between reproduction and locomotion in this emblematic New Zealand bird.

Whole-body 3D kinematics of bird take-off: key role of the legs to propel the trunk.

Previous studies showed that birds primarily use their hindlimbs to propel themselves into the air in order to take-off. Yet, it remains unclear how the different parts of their musculoskeletal system move to produce the necessary acceleration. To quantify the relative motions of the bones during the terrestrial phase of take-off, we used biplanar fluoroscopy in two species of birds, diamond dove (Geopelia cuneata) and zebra finch (Taeniopygia guttata). We obtained a detailed 3D kinematics analysis of the head, the trunk and the three long bones of the left leg. We found that the entire body assisted the production of the needed forces to take-off, during two distinct but complementary phases. The first one, a relatively slow preparatory phase, started with a movement of the head and an alignment of the different groups of bones with the future take-off direction. It was associated with a pitch down of the trunk and a flexion of the ankle, of the hip and, to a lesser extent, of the knee. This crouching movement could contribute to the loading of the leg muscles and store elastic energy that could be released in the propulsive phase of take-off, during the extension of the leg joints. Combined with the fact that the head, together with the trunk, produced a forward momentum, the entire body assisted the production of the needed forces to take-off. The second phase was faster with mostly horizontal forward and vertical upward translation motions, synchronous to an extension of the entire lower articulated musculoskeletal system. It led to the propulsion of the bird in the air with a fundamental role of the hip and ankle joints to move the trunk upward and forward. Take-off kinematics were similar in both studied species, with a more pronounced crouching movement in diamond dove, which can be related to a large body mass compared to zebra finch.

Foot shape in arboreal birds: two morphological patterns for the same pincer-like tool.

The feet are the only contact between the body and the substrate in limbed animals and as such they provide a crucial interface between the animal and its environment. This is especially true for bipedal and arboreal species living in a complex three-dimensional environment that likely induces strong selection on foot morphology. In birds, foot morphology is highly variable, with different orientations of the toes, making it a good model for the study of the role of functional, developmental, and phylogenetic constraints in the evolution of phenotypic diversity. Our data on the proportions of the phalanges analyzed in a phylogenetic context show that two different morphological patterns exist that depend mainly on habitat and toe orientation. In the anisodactyl foot, the hallux is the only backward-oriented toe and is enlarged in climbing species and reduced in terrestrial ones. Moreover, a proximo-distal gradient in phalanx size is observed depending on the degree of terrestriality. In the two other cases (heterodactyl and zygodactyl) that have two toes that point backward, the hallux is rather small in contrast to the other backward-pointing toe, which is enlarged. The first pattern is convergent and common among tetrapods and follows rules of skeletal development. The second pattern is unique for the clade and under muscle-morphogenetic control. In all cases, the functional result is the same tool, a pincer-like foot.

Transition from wing to leg forces during landing in birds.

Transitions to and from the air are critical for aerial locomotion and likely shaped the evolution of flying animals. Research on take-off demonstrates that legs generate greater body accelerations compared with wings, and thereby contribute more to initial flight velocity. Here, we explored coordination between wings and legs in two species with different wingbeat styles, and quantified force production of these modules during the final phase of landing. We used the same birds that we had previously studied during take-off: zebra finch (Taeniopygia guttata, N=4) and diamond dove (Geopelia cuneata, N=3). We measured kinematics using high-speed video, aerodynamics using particle image velocimetry, and ground-reaction forces using a perch mounted on a force plate. In contrast with the first three wingbeats of take-off, the final four wingbeats during landing featured ~2 times greater force production. Thus, wings contribute proportionally more to changes in velocity during the last phase of landing compared with the initial phase of take-off. The two species touched down at the same velocity (~1 m s(-1)), but they exhibited significant differences in the timing of their final wingbeat relative to touchdown. The ratio of average wing force to peak leg force was greater in diamond doves than in zebra finches. Peak ground reaction forces during landing were ~50% of those during take-off, consistent with the birds being motivated to control landing. Likewise, estimations of mechanical energy flux for both species indicate that wings produce 3-10 times more mechanical work within the final wingbeats of flight compared with the kinetic energy of the body absorbed by legs during ground contact.

Gait transitions and modular organization of mammal locomotion.

Quadrupedal locomotion is the result of complex interactions between biomechanical and neural systems. During steady gaits, both systems are in stable states. When the animal changes its speed, transitions between gaits can occur in which the different coordination parameters are dissociated. Consequently, transitions are the periods where it is possible to detect and identify those parameters involved in the mechanical or neural control of locomotion. We studied interlimb coordination using a sequential method (antero-posterior sequence) to measure the footfall patterns of dogs when accelerating and decelerating from 1.5 m s(-1) to more than 6 m s(-1) and back. We obtained 383 transitions between all the symmetrical and asymmetrical gaits used by the dogs. Analysis of the interlimb coordination modifications and of each foot parameter showed that mechanics drive the stance phase whereas coordination is controlled during the swing phase. Furthermore, comparison of the transition patterns between all gaits reveals the modular organization of locomotion: a pectoral module coordinates the two forelimbs, a pelvic module coordinates the two hindlimbs and an axial module coordinates the two pairs of limbs and the trunk motion. The three modules cooperate to give rise to a template of stable interlimb coordination pattern, such as walk, trot or gallop.

An upright life, the postural stability of birds: a tensegrity system.

Birds are so stable that they can rest and even sleep standing up. We propose that stable static balance is achieved by tensegrity. The rigid bones can be held together by tension in the tendons, allowing the system to stabilize under the action of gravity. We used the proportions of the bird's osteomuscular system to create a mathematical model. First, the extensor muscles and tendons of the leg are replaced by a single cable that follows the leg and is guided by joint pulleys. Analysis of the model shows that it can achieve balance. However, it does not match the biomechanical characteristics of the bird's body and is not stable. We then replaced the single cable with four cables, roughly corresponding to the extensor groups, and added a ligament loop at the knee. The model is then able to reach a stable equilibrium and the biomechanical characteristics are satisfied. Some of the anatomical features used in our model correspond to innovations unique to the avian lineage. We propose that tensegrity, which allows light and stable mechanical systems, is fundamental to the evolution of the avian body plan. It can also be used as an alternative model for bipedal robots.

Transition from leg to wing forces during take-off in birds.

Take-off mechanics are fundamental to the ecology and evolution of flying animals. Recent research has revealed that initial take-off velocity in birds is driven mostly by hindlimb forces. However, the contribution of the wings during the transition to air is unknown. To investigate this transition, we integrated measurements of both leg and wing forces during take-off and the first three wingbeats in zebra finch (Taeniopygia guttata, body mass 15 g, N=7) and diamond dove (Geopelia cuneata, body mass 50 g, N=3). We measured ground reaction forces produced by the hindlimbs using a perch mounted on a force plate, whole-body and wing kinematics using high-speed video, and aerodynamic forces using particle image velocimetry (PIV). Take-off performance was generally similar between species. When birds were perched, an acceleration peak produced by the legs contributed to 85±1% of the whole-body resultant acceleration in finch and 77±6% in dove. At lift-off, coincident with the start of the first downstroke, the percentage of hindlimb contribution to initial flight velocity was 93.6±0.6% in finch and 95.2±0.4% in dove. In finch, the first wingbeat produced 57.9±3.4% of the lift created during subsequent wingbeats compared with 62.5±2.2% in dove. Advance ratios were <0.5 in both species, even when taking self-convection of shed vortices into account, so it was likely that wing-wake interactions dominated aerodynamics during wingbeats 2 and 3. These results underscore the relatively low contribution of the wings to initial take-off, and reveal a novel transitional role for the first wingbeat in terms of force production.

Second-order division in sectors as a prepattern for sensory organs in vertebrate development.

We present in vivo observations of chicken embryo development which show that the early chicken embryo presents a principal structure made out of concentric rings and a secondary structure composed of radial sectors. During development, physical forces deform the main rings into axially directed, antero-posterior tubes, while the sectors roll up to form cylinders that are perpendicular to the antero-posterior axis. As a consequence, the basic structure of the chicken embryo is a series of encased antero-posterior tubes (gut, neural tube, body envelope, amnion, chorion) decorated with smaller orifices (ear duct, eye stalk, nasal duct, gills, mouth) forming at right angles to the main body axis. We argue that the second-order divisions reflect the early pattern of cell cleavage, and that the transformation of radial and orthoradial lines into a body with sensory organs is a generic biophysical mechanism more general than the chicken embryo.

Woodpeckers minimize cranial absorption of shocks.

The skull of a woodpecker is hypothesized to serve as a shock absorber that minimizes the harmful deceleration of its brain upon impact into trees1-11 and has inspired the engineering of shock-absorbing materials12-15 and tools, such as helmets.16 However, this hypothesis remains paradoxical since any absorption or dissipation of the head's kinetic energy by the skull would likely impair the bird's hammering performance4 and is therefore unlikely to have evolved by natural selection. In vivo quantification of impact decelerations during pecking in three woodpecker species and biomechanical models now show that their cranial skeleton is used as a stiff hammer to enhance pecking performance, and not as a shock-absorbing system to protect the brain. Numerical simulations of the effect of braincase size and shape on intracranial pressure indicate that the woodpeckers' brains are still safe below the threshold of concussions known for primate brains. These results contradict the currently prevailing conception of the adaptive evolution of cranial function in one of nature's most spectacular behaviors. VIDEO ABSTRACT.

Radial porosity profiles: a new bone histological method for comparative developmental analysis of diametric limb bone growth.

In fossil tetrapods, limb bone histology is considered the most reliable tool not only for inferring skeletal maturity-a crucial assessment in palaeobiological and evolutionary studies-but also for evaluating the growth dynamics within the ontogenetic window represented by the primary bone cortex. Due to its complex relationship with bone growth and functional maturation, primary cortical vascularity is an indispensable osteohistological character for reconstructing growth dynamics, especially in the context of various developmental strategies along the precocial-altricial spectrum. Using this concept as our working hypothesis, we developed a new quantitative osteohistological parameter, radial porosity profile (RPP), that captures relative cortical porosity changes in limb bones as trajectories. We built a proof-of-concept RPP dataset on extant birds, then added fossil paravian dinosaurs and performed a set of trajectory-grouping analyses to identify potential RPP categories and evaluate them in the context of our ontogeny-developmental strategy working hypothesis. We found that RPPs, indeed, reflect important developmental features within and across elements, specimens and taxa, supporting their analytical power. Our RPPs also revealed unexpected potential osteohistological correlates of growth and functional development of limb bones. The diverse potential applications of RPPs open up new research directions in the evolution of locomotor ontogeny.

Estimating motion between avian vertebrae by contact modeling of joint surfaces.

Estimating the motion between two bones is crucial for understanding their biomechanical function. The vertebral column is particularly challenging because the vertebrae articulate at more than one surface. This paper proposes a method to estimate 3D motion between two avian vertebrae, by bones surface reconstruction and contact modeling. The neck of birds was selected as a case study because it is a functionally highly versatile structure combining dexterity and strength. As such, it has great potential to serve as a source for bioinspired design, for robotic manipulators for instance. First, 3D models of the vertebrae are obtained by computed tomography (CT). Next, joint surfaces of contact are approximated with polynomial surfaces, and a system of equations derived from contact modeling between surfaces is established. A constrained optimization problem is defined in order to find the best position of the vertebrae for a set of given orientations in space. As a result, the possible intervertebral range of motion is estimated.

The end of the fat dodo? A new mass estimate for Raphus cucullatus.

A new mass estimate for the dodo (Raphus cucullatus), based on the lengths of the femur, tibiotarsus and tarsometatarsus, is attempted. The obtained mean mass is 10.2 kg, which is less than previous estimates based on other methods, which ranged from 10.6 to 21.1 kg, and much lower than the 50 lbs reported by a seventeenth-century eyewitness. The new estimated mass, which is similar to that of a large wild turkey, seems more realistic than previous ones and supports the hypothesis that contemporary illustrations of extremely fat dodos were either exaggerations, or based on overfed specimens. Pictures of "fat" dodos may also have been based on individuals exhibiting a display behaviour with puffed out feathers.

The skin of birds' feet: Morphological adaptations of the plantar surface.

The skin of the foot provides the interface between the bird and the substrate. The foot morphology involves the bone shape and the integument that is in contact with the substrate. The podotheca is a layer of keratinized epidermis forming scales that extends from the tarsometatarsus to the toe extremities. It varies in size, shape, amount of overlap and interacts with the degree of fusion of the toes (syndactyly). A study of toe shape and the podotheca provides insights on the adaptations of perching birds. Our analysis is based on micro-CT scans and scanning electron microscopy images of 21 species from 17 families, and includes examples with different orientations of the toes: zygodactyl (toes II and III forward), anisodactyl (toes II, III, and IV forward), and heterodactyl (toes III and IV forward). We show that in these three groups, the skin forms part of a perching adaptation that involves syndactyly to different degrees. However, syndactyly does not occur in Psittacidae that use their toes also for food manipulation. The syndactyly increases the sole surface and may reinforce adherence with the substrate. Scale shape and toe orientation are involved in functional adaptations to perch. Thus, both bone and skin features combine to form a pincer-like foot.

Does bone preparation impact its shape: consequences for comparative analyses of bone shape.

Vertebrate osteological collections provide comparative material for morphological analysis. Before being stored in the collection and studied by researchers, specimens are treated by preparators or curators and are cleaned. The preparation protocol employed ideally should not damage the material. Here, we explore the potential deformation of bones due to preparation using geometric morphometric methods. We focus both on intraspecific and interspecific variability. Our data on the scapular girdle of birds show that, at an intraspecific level, the effect of preparation on bone shape cannot be neglected. Paired and unpaired bones did not respond to the preparation process in the same way, possibly due to differences in function and their anatomical characteristics. Moreover, deformations due to preparation can be estimated by looking at the texture of the bone. At the interspecific level, we found no significant differences as the deformations induced by preparation are relatively small compared to differences among species. This study highlights the importance of carefully selecting preparation methods in order to avoid physical damage that could impact the shape of bones, especially for studies at the intraspecific level.