Barn owls maximize head rotations by a combination of yawing and rolling in functionally diverse regions of the neck

Abstract

Owls are known for their outstanding neck mobility: these birds can rotate their heads more than 270°. The anatomical basis of this extraordinary neck rotation ability is not well understood. We used X-ray fluoroscopy of living owls as well as forced neck rotations in dead specimens and computer tomographic (CT) reconstructions to study how the individual cervical joints contribute to head rotation in barn owls (Tyto furcata pratincola). The X-ray data showed the natural posture of the neck, and the reconstructions of the CT-scans provided the shapes of the individual vertebrae. Joint mobility was analyzed in a spherical coordinate system. The rotational capability was described as rotation about the yaw and roll axes. The analyses suggest a functional division of the cervical spine into several regions. Most importantly, an upper region shows high rolling and yawing capabilities. The mobility of the lower, more horizontally oriented joints of the cervical spine is restricted mainly to the roll axis. These rolling movements lead to lateral bending, effectively resulting in a side shift of the head compared with the trunk during large rotations. The joints in the middle of the cervical spine proved to contribute less to head rotation. The analysis of joint mobility demonstrated how owls might maximize horizontal head rotation by a specific and variable combination of yawing and rolling in functionally diverse regions of the neck.

Modularity of the Neck in Birds (Aves)

“…In conclusion, our results are consistent with those of previous studies on the regionalization of the neck in birds (e.g., Virchow 1910;Boas 1929;Zweers et al 1987;van der Leeuw et al 2001;Tambussi et al 2012;Cobley et al 2013;Krings et al 2017;Kambic et al 2017). However, they indicate that the pattern of modularity is more complex than expected, including subdivisions of the traditional functional regions and module redundancy.…”

“…These subdivisions consist only of redundant modules and therefore share similar (even if not identical) postural properties but present varied shapes. This finding is in line with those of Krings et al (2014Krings et al ( , 2017, who identified three to seven modules along the neck of owls based on morphological and functional studies.…”

“…The cranial portion is characterized by prevalent ventral flexion, the intermediate region is prevalently flexible in the dorsal direction, and the caudal portion allows movements in both directions. Several studies have supported this regionalization of the avian neck (e.g., Zweers et al 1987;Heidweiller et al 1992;Bout 1997;van der Leeuw et al 2001;Tambussi et al 2012;Cobley et al 2013;Krings et al 2017; but see also Kambic et al (2017), who challenged this three-region model).…”

Vertebral pneumaticity is correlated with serial variation in vertebral shape in storks

“…To the extent that diminished range of motion limits load variability, safe development of more pneumatic bones could be brought about by serial decreases in flexibility in the caudal cervical vertebrae. Range of motion, at least in some axes, has been shown to decrease toward the base of the neck in some birds (Van der Leeuw et al, 2001; Dzemski & Christian, 2007; Cobley et al, 2013; Krings et al, 2017), though patterns of mobility are complex (Kambic et al, 2017). Caudal cervical vertebrae also likely benefit from the stabilizing and load‐sharing effects of relatively large intervertebral ligaments and the envelopment of the base of the neck by large masses of muscle (Dzemski & Christian, 2007; Cobley et al, 2013), perhaps further enabling increased pneumaticity in these elements.…”

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

“…A few studies have quantified lateroflexion in addition to, and independently of, dorsoventral flexion [ 26 , 33 ]. Only three studies have attempted to reconstruct bird neck movements in three dimensions (specifically in owls [ 35 , 39 , 40 ]), with the potential to quantify all three rotational degrees of freedom simultaneously, including axial rotation. Such data are critical for understanding joint function, as musculoskeletal movements incorporate motion around multiple degrees of freedom simultaneously (e.g.…”