Avian Neck Research Articles

The neck as a keystone structure in avian macroevolution and mosaicism

BackgroundThe origin of birds from non-avian theropod dinosaur ancestors required a comprehensive restructuring of the body plan to enable the evolution of powered flight. One of the proposed key mechanisms that allowed birds to acquire flight and modify the associated anatomical structures into diverse forms is mosaic evolution, which describes the parcelization of phenotypic traits into separate modules that evolve with heterogeneous tempo and mode. Avian mosaicism has been investigated with a focus on the cranial and appendicular skeleton, and as such, we do not understand the role of the axial column in avian macroevolution. The long, flexible neck of extant birds lies between the cranial and pectoral modules and represents an opportunity to study the contribution of the axial skeleton to avian mosaicism.ResultsHere, we use 3D geometric morphometrics in tandem with phylogenetic comparative methods to provide, to our knowledge, the first integrative analysis of avian neck evolution in context with the head and wing and to interrogate how the interactions between these anatomical systems have influenced macroevolutionary trends across a broad sample of extant birds. We find that the neck is integrated with both the head and the forelimb. These patterns of integration are variable across clades, and only specific ecological groups exhibit either head-neck or neck-forelimb integration. Finally, we find that ecological groups that display head-neck and neck-forelimb integration tend to display significant shifts in the rate of neck morphological evolution.ConclusionsCombined, these results suggest that the interaction between trophic ecology and head-neck-forelimb mosaicism influences the evolutionary variance of the avian neck. By linking together the biomechanical functions of these distinct anatomical systems, the cervical vertebral column serves as a keystone structure in avian mosaicism and macroevolution.

A surrogate forelimb: Evolution, function and development of the avian cervical spine.

The neck is a critical portion of the avian spine, one that works in tandem with the beak to act as a surrogate forelimb and allows birds to manipulate their surroundings despite the lack of a grasping capable hand. Birds display an incredible amount of diversity in neck morphology across multiple anatomical scales-from varying cervical counts down to intricate adaptations of individual vertebrae. Despite this morphofunctional disparity, little is known about the drivers of this enormous variation, nor how neck evolution has shaped avian macroevolution. To promote interest in this system, I review the development, function and evolution of the avian cervical spine. The musculoskeletal anatomy, basic kinematics and development of the avian neck are all documented, but focus primarily upon commercially available taxa. In addition, recent work has quantified the drivers of extant morphological variation across the avian neck, as well as patterns of integration between the neck and other skeletal elements. However, the evolutionary history of the avian cervical spine, and its contribution to the diversification and success of modern birds is currently unknown. Future work should aim to broaden our understanding of the cervical anatomy, development and kinematics to include a more diverse selection of extant birds, while also considering the macroevolutionary drivers and consequences of this important section of the avian spine.

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.

Evolutionary versatility of the avian neck.

Bird necks display unparalleled levels of morphological diversity compared to other vertebrates, yet it is unclear what factors have structured this variation. Using three-dimensional geometric morphometrics and multivariate statistics, we show that the avian cervical column is a hierarchical morpho-functional appendage, with varying magnitudes of ecologically driven osteological variation at different scales of organization. Contrary to expectations given the widely varying ecological functions of necks in different species, we find that regional modularity of the avian neck is highly conserved, with an overall structural blueprint that is significantly altered only by the most mechanically demanding ecological functions. Nevertheless, the morphologies of vertebrae within subregions of the neck show more prominent signals of adaptation to ecological pressures. We also find that both neck length allometry and the nature of neck elongation in birds are different from other vertebrates. In contrast with mammals, neck length scales isometrically with head mass and, contrary to previous work, we show that neck elongation in birds is achieved predominantly by increasing vertebral lengths rather than counts. Birds therefore possess a cervical spine that may be unique in its versatility among extant vertebrates, one that, since the origin of flight, has adapted to function as a surrogate forelimb in varied ecological niches.

A novel dynamic stabilization and vibration isolation structure inspired by the role of avian neck

A novel multi-layer structure with functions for dynamic stabilization and vibration isolation, bio-inspired by the role of an avian neck, is proposed in this paper. Inspired by the fact that an avian neck can stabilize the head from body flapping, we expect that the proposed structure can achieve dynamic stabilization effectiveness under external excitation with a low frequency, large amplitude, and displacement mutations. First, for different configurations of the bio-inspired structure, the key characteristics, such as the elastic deformation energy, restoring force and equivalent dynamic properties are determined by mechanical modeling. It discovers that the proposed bio-inspired structure could achieve the designed loading capacity and dynamic zero stiffness simultaneously. Then according to the analysis of the dynamic behaviors under impact excitation and harmonic excitation by the perturbation method, the optimum criteria for the structural configuration and parameters are carried out. Thus, the effective isolation band begins at zero frequency, and the dynamic behavior could be quickly stabilized. Finally, the constructed multi-layer structure could achieve the stabilization functions of the avian neck. For different strengths of gusts, the amplitude of the top layer is less than a fifth of the excitation from the body. Due to the multiple functions in dynamic stabilization and control, the proposed structure can solve the bottleneck techniques in nonlinear isolation structural design, and it has remarkable potential applications in the fields of mechanical arms, sensors in satellites, etc.

Correlated evolution of neck length and leg length in birds.

Despite a diversity of about 10 000 extant species, the sophisticated avian ‘body plan’ has not much changed once it was achieved around 160 Ma after the origin of powered flight. All birds are bipedal having wings, a rigid trunk, a short and ossified tail, a three-segmented leg and digitigrade feet. The avian neck, however, has always been regarded as a classic example of high variability ranging from short necks in songbirds to extremely long, serpentine necks in herons. Yet, the wide array of small to very large species makes it difficult to evaluate the actual neck length. Here, we investigate the evolution of the vertebral formulae in the neck of birds and the scaling relationships between skeletal dimensions and body size. Cervical count in birds is strongly related to phylogeny, with only some specialists having an exceptional number of vertebrae in the neck. In contrast with mammals, the length of the cervical vertebral column increases as body size increases and, thus, body size does not constrain neck length in birds. Indeed, neck length scales isometrically with total leg length suggesting a correlated evolution between both modules. The strong integration between the cervical and pelvic module in birds is in contrast with the decoupling of the fore- and hindlimb module and may be the result of the loss of a functionally versatile forelimb due to the evolution of powered flight.

Experimental determination of three-dimensional cervical joint mobility in the avian neck

BackgroundBirds have highly mobile necks, but neither the details of how they realize complex poses nor the evolution of this complex musculoskeletal system is well-understood. Most previous work on avian neck function has focused on dorsoventral flexion, with few studies quantifying lateroflexion or axial rotation. Such data are critical for understanding joint function, as musculoskeletal movements incorporate motion around multiple degrees of freedom simultaneously. Here we use biplanar X-rays on wild turkeys to quantify three-dimensional cervical joint range of motion in an avian neck to determine patterns of mobility along the cranial-caudal axis.ResultsRange of motion can be generalized to a three-region model: cranial joints are ventroflexed with high axial and lateral mobility, caudal joints are dorsiflexed with little axial rotation but high lateroflexion, and middle joints show varying amounts axial rotation and a low degree of lateroflexion. Nonetheless, variation within and between regions is high. To attain complex poses, substantial axial rotation can occur at joints caudal to the atlas/axis complex and zygapophyseal joints can reduce their overlap almost to osteological disarticulation. Degrees of freedom interact at cervical joints; maximum lateroflexion occurs at different dorsoventral flexion angles at different joints, and axial rotation and lateroflexion are strongly coupled. Further, patterns of joint mobility are strongly predicted by cervical morphology.ConclusionBirds attain complex neck poses through a combination of mobile intervertebral joints, coupled rotations, and highly flexible zygapophyseal joints. Cranial-caudal patterns of joint mobility are tightly linked to cervical morphology, such that function can be predicted by form. The technique employed here provides a repeatable protocol for studying neck function in a broad array of taxa that will be directly comparable. It also serves as a foundation for future work on the evolution of neck mobility along the line from non-avian theropod dinosaurs to birds.

The role of passive avian head stabilization in flapping flight.

Birds improve vision by stabilizing head position relative to their surroundings, while their body is forced up and down during flapping flight. Stabilization is facilitated by compensatory motion of the sophisticated avian head-neck system. While relative head motion has been studied in stationary and walking birds, little is known about how birds accomplish head stabilization during flapping flight. To unravel this, we approximate the avian neck with a linear mass-spring-damper system for vertical displacements, analogous to proven head stabilization models for walking humans. We corroborate the model's dimensionless natural frequency and damping ratios from high-speed video recordings of whooper swans (Cygnus cygnus) flying over a lake. The data show that flap-induced body oscillations can be passively attenuated through the neck. We find that the passive model robustly attenuates large body oscillations, even in response to head mass and gust perturbations. Our proof of principle shows that bird-inspired drones with flapping wings could record better images with a swan-inspired passive camera suspension.

The Paired Cervico‐Cephalic Air Sacs and their Role in the Vocalizations of Songbirds

The avian neck contains a coelomic cavity within which the esophagus and trachea are anchored by mesenteries (Cozic et al. 2014). In order to evaluate the role of the neck in the resonance (filtering) of sounds generated by the syrinx, we created a 3D animated model of the shoulder, neck, and head of a Northern Cardinal (Cardinalis cardinalis) based on x-ray fluoroscopy and x-ray CT data and supplemented with data from micro-dissections. Our model revealed a space in the upper neck between the trachea and vertebral column, which increases in volume when the tongue is protracted during low-frequency sounds and decreases in volume when the tongue is retracted during high-frequency sounds. Our micro-dissections revealed paired cervico-cephalic air sacs within the upper cervical coelomic cavity of a Cardinal and a House Sparrow (Passer domesticus) where the fluctuating space is shown in the 3D model. These air sacs, which are not connected to the pulmonary system, were already described by Fanny Bignon (1889) in a variety of birds, but their functioning and role have been poorly understood. We infer that in songbirds these air sacs are passively inflated when the tongue and trachea are protracted and, thereby, fill the increasing space between the trachea and vertebral column, and are compressed and deflated when the tongue and trachea are retracted. Supported by NIH grant NINDS R01 NS029467 and LSU Foundation account “Functional Morphology of Birds”

Control of the Cranio-Cervical System During Feeding in Birds1

The avian neck is a complex, kinematically redundant system, which plays a role during inter alia food prehension and manipulation. Kinematical analysis shows that chickens (Gallus domesticus) move their vertebrae according to a geometric principle that maximizes angular rotation efficiency. The movement pattern shows simultaneous rotations in some joints, while not in the others. Anseriformes show a pattern of successive, rather than simultaneous rotations in the rostral part of the neck. A kinematical model indicates that the geometric principle produces an anseriform-like pattern only if a constraint on the movement of the caudal vertebrae is introduced. The strength of this constraint, required for a realistic simulation, is related to the amount of stretch in the long dorsal neck muscles (M. biventer and M. longus colli dorsalis), which have a different configuration in Anseriformes compared to the chicken. To investigate whether the difference in movement pattern is a result of differences in anatomy only, or also of differences in neuromotor patterns, the EMG-patterns of the neck muscles of the mallard and chicken during drinking and pecking were studied. Considerable overlap in the activity of antagonists is found in mallards, but not in chickens. Muscles in the rostral part of the neck are activated successively in mallards, but simultaneously in chickens. We conclude that the difference in movement patterning between chickens and Anseriformes, results from both a difference in the control system of the neck, and a difference in the anatomy. The anseriform pattern is found in water as well as on land, which suggests that neck movement in both environments is controlled by the same neuromotor patterns. The modifications in motor control system and anatomy of the Anseriformes may have evolved as an adaptation to aquatic feeding, since the anseriform pattern is energetically more beneficial in an aquatic environment than on land.

Evolutionary Morphology of the Neck System in Ratites, Fowl and Waterfowl

The avian neck is a complex, kinematically redundant system that controls the position and orientation of the head. The kinematic redundancy is resolved by movement principles, which result in characteristic movement patterns. General neck movement patterns are compared between Ratites, Fowl and Waterfowl in order to find a relationship with anatomical differences and to identify the biological role(s) to which neck movement is adapted. Kinematic analyses show that Fowl move their vertebrae according to a minimal rotation principle that maximizes rotation efficiency. The resulting movement pattern shows rotations in some joints, while keeping the other vertebrae as straight bars. Waterfowl show a pattern of successive, rather than simultaneous rotations of vertebrae, limited to the rostral part of the neck. A third movement pattern is found in Ratites, which show successive rotations of the vertebrae in the middle region of the neck. The ratite-pattern is related to large vertical head trajectories, and is occasionaly also found in the Chicken. However, due to large body movements in the Chicken, head trajectories are relatively much shorter than in the Rhea. A kinematic neck model based on the minimal rotation principle only produces the Waterfowl pattern if a constraint on the movement of the caudal vertebrae is introduced. We conclude that a fundamental change occurred in the movement pattern of the Waterfowl neck, which is energetically advantageous and an adaptation to aquatic feeding.

Postures of the avian craniocervical column.

The avian cervical column comprises a large number of vertebrae and has far more degrees of freedom than necessary to position and orient the head. The large number of joints makes the avian neck a very suitable model for the study of coordination and movement strategies in kinematically redundant chains. A static optimization model that finds a solution for the configuration of cervical vertebrae is proposed and tested in a series of neck postures of a chicken. As inputs, the model uses length of the vertebrae, orientation of the articulation facies, and the position and orientation of the head with respect to the body. The model demonstrates that an even distribution of rotation over the whole chain is sufficient to explain all the essential characteristics of neck postures. It is shown that the model not only predicts static postures but also minimizes the change in angle needed to go through a series of successive postures. J Morphol 231:287-295, 1997. © 1997 Wiley-Liss, Inc.

Postures of the avian craniocervical column

The avian cervical column comprises a large number of vertebrae and has far more degrees of freedom than necessary to position and orient the head. The large number of joints makes the avian neck a very suitable model for the study of coordination and movement strategies in kinematically redundant chains. A static optimization model that finds a solution for the configuration of cervical vertebrae is proposed and tested in a series of neck postures of a chicken. As inputs, the model uses length of the vertebrae, orientation of the articulation facies, and the position and orientation of the head with respect to the body. The model demonstrates that an even distribution of rotation over the whole chain is sufficient to explain all the essential characteristics of neck postures. It is shown that the model not only predicts static postures but also minimizes the change in angle needed to go through a series of successive postures. J Morphol 231:287–295, 1997. © 1997 Wiley-Liss, Inc.