Myological variability in a decoupled skeletal system: Batoid cranial anatomy

Abstract

Chondrichthyans (sharks, batoids, and chimaeras) have simple feeding mechanisms owing to their relatively few cranial skeletal elements. However, the indirect association of the jaws to the cranium (euhyostylic jaw suspension) has resulted in myriad cranial muscle rearrangements of both the hyoid and mandibular elements. We examined the cranial musculature of an abbreviated phylogenetic representation of batoid fishes, including skates, guitarfishes and with a particular focus on stingrays. We identified homologous muscle groups across these taxa and describe changes in gross morphology across developmental and functional muscle groups, with the goal of exploring how decoupling of the jaws from the skull has effected muscular arrangement. In particular, we focus on the cranial anatomy of durophagous and nondurophagous batoids, as the former display marked differences in morphology compared to the latter. Durophagous stingrays are characterized by hypertrophied jaw adductors, reliance on pennate versus fusiform muscle fiber architecture, tendinous rather than aponeurotic muscle insertions, and an overall reduction in mandibular kinesis. Nondurophagous stingrays have muscles that rely on aponeurotic insertions onto the skeletal structure, and display musculoskeletal specialization for jaw protrusion and independent lower jaw kinesis, relative to durophagous stingrays. We find that among extant chondrichthyans, considerable variation exists in the hyoid and mandibular muscles, slightly less so in hypaxial muscles, whereas branchial muscles are overwhelmingly conserved. As chondrichthyans occupy a position sister to all other living gnathostomes, our understanding of the structure and function of early vertebrate feeding systems rests heavily on understanding chondrichthyan cranial anatomy. Our findings highlight the incredible variation in muscular complexity across chondrichthyans in general and batoids in particular.

Morphology does not predict performance: jaw curvature and prey crushing in durophagous stingrays

“…There are many differences in the feeding apparatus of durophagous rays, including the size, shape, insertion, and pennation of muscles, and the arrangement of connective tissue (Kolmann et al, 2014), but we cannot ascribe any performance difference to one of the most obvious differences in morphology -the shape of the jaws. With minor exceptions, the shape of myliobatid jaws had little effect on the crushing performance of hard prey, regardless of prey type.…”

“…Compared with non-durophagous stingrays, myliobatids have reduced cranial mobility (e.g. caused by jaw symphyseal fusion), several instances of duplicated or reoriented muscles, and increased skeletal reinforcement, all features convergent with other durophagous vertebrates (Summers, 2000;Kolmann et al, 2014;Mulvany and Motta, 2014). Durophagous stingrays also feature robust teeth, interlocking at their bases to form shallow-domed tooth plate arrays ( Fig.…”

Feeding biomechanics of the cownose ray, Rhinoptera bonasus, over ontogeny

“…The morphology of this muscle division is markedly different between durophagous rays and non‐durophagous rays, with the AMMa in the former wrapping around the lower jaw like a sling (Kolmann et al. ). This arrangement maximizes use of cranial space in a system that is constrained laterally by the pectoral propterygia.…”

“…The nomenclature and relative insertion and origin points of these muscles follow Kolmann et al. (; Fig. ), which draws from Miyake et al.…”

“…; Ajemian & Powers, ), and possess characteristics such as: grinding tooth plates, trabecular‐reinforced jaw skeletons, fused jaw symphyses and massive pennate‐fibered jaw adductors with fibrocartilaginous pads that wrap around the corners of the jaw (Summers, ; Aschliman, ; Kolmann et al. ). These stingrays have a euhyostylic jaw suspension in which the jaws are disarticulated from the cranium and the paired hyomandibulae provide indirect attachment (Dean et al.…”