Control of the Cranio-Cervical System During Feeding in Birds1

Abstract

SYNOPSIS. 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 versatility of the avian neck

“…Only mechanically demanding ecological behaviours appear to be associated with statistically significant modifications to this universal structural and morphological blueprint ( figure 2 c – g ). Our results also reveal, contrary to previous expectations [ 5 , 6 , 54 , 55 ], that lengthening of vertebrae rather than cervicalization (the addition of vertebrae to the neck) drives neck elongation in birds, and that neck length scales isometrically with both body and head size (figure S4) with little ecological signal (electronic supplementary material, figure S2 and table S4). In spite of this overall conservation of neck architecture, our analyses of intra-regional osteological variation indicate that intrinsic and particularly extrinsic factors do exert significant adaptive morphological changes (electronic supplementary material, figure S2 and table S3), representing finer-scale modifications to the generalized avian cervical system.…”

“…Results from the PTA ( figure 2 ) lend credence to this hypothesis as patterns of morphological variation across the entire cervical spine as a whole are conserved across the majority of species studied, suggesting that these patterns may be adapted for providing the neck with generalized kinematics. Birds share patterns of cervical kinematics for many activities and the conservative nature of regionalization and inter-regional variation found herein provides the morphological evidence the avian neck, generally, may be adapted to the ‘economics of continuous movement’ than to any specific ecology or behaviour [ 4 , 6 , 54 , 55 ]. Alternatively, the retainment of consistent overall morphological blueprint across most ecological groups may represent constraints imposed a conserved pattern of Hox gene expression, although that modifications have evolved in response to mechanically demanding neck functions ( figure 2 ) suggests it is most likely a product of both genetic and functional influences.…”

“…Cervicalization (increases to the number of cervical vertebrae) was previously thought to be responsible for neck elongation in birds [ 5 , 6 , 54 , 55 ]. However, our data provide no evidence in support of this hypothesis and instead suggest that vertebral elongation is the primary mechanism by which neck elongation occurs.…”

The role of many-to-one mapping of vertebral form to function in Psittaciform tripedal locomotion

“…A key difference between the skull and neck of parrots is that dietary preference accounts for more morphological variation in the neck of parrots (up to 15% vs 2.4%, Supplementary Table 4). We had expected to observe the opposite pattern as the skull directly manipulates and processes food, not the neck (7,22,49,50). Diet is still a minor (∼15%) component of neck morphological variation however, and the differences observed here may be due to discrepancies in dietary classification schemes between the two studies (22).…”

“RobOstrich” Manipulator: A Novel Mechanical Design and Control based on the Anatomy and Behavior of an Ostrich Neck

“…In chickens the length of the dorsal long muscle hardly changes from its initial length during the rolling pattern [21]. In addition, not only the dorsal long muscle, but also the ventral muscle increases its electromyography potential [22]. In addition, as can be seen from the crosssectional view of the ostrich neck shown in Fig.…”