Functional morphology of the Alligator mississippiensis larynx with implications for vocal production

Abstract

Sauropsid vocalization is mediated by the syrinx in birds and the larynx in extant reptiles; but whereas avian vocal production has received much attention, the vocal mechanism of basal reptilians is poorly understood. The American alligator (Alligator mississippiensis) displays a large vocal repertoire during mating and in parent-offspring interactions. Although vocal outputs of these behaviors have received some attention, the underlying mechanism of sound production remains speculative. Here, we investigate the laryngeal anatomy of juvenile and adult animals by macroscopic and histological methods. Observations of the cartilaginous framework and associated muscles largely corroborate earlier findings, but one muscle, the cricoarytenoideus, exhibits a heretofore unknown extrinsic insertion that has important implications for effective regulation of vocal fold length and tension. Histological investigation of the larynx revealed a layered vocal fold morphology. The thick lamina propria consists of non-homogenous extracellular matrix containing collagen fibers that are tightly packed below the epithelium but loosely organized deep inside the vocal fold. We found few elastic fibers but comparatively high proportions of hyaluronan. Similar organizational complexity is also seen in mammalian vocal folds and the labia of the avian syrinx: convergent morphologies that suggest analogous mechanisms for sound production. In tensile tests, alligator vocal folds demonstrated a linear stress-strain behavior in the low strain region and nonlinear stress responses at strains larger than 15%, which is similar to mammalian vocal fold tissue. We have integrated morphological and physiological data in a two-mass vocal fold model, providing a systematic description of the possible acoustic space that could be available to an alligator larynx. Mapping actual call production onto possible acoustic space validates the model's predictions.

Keywords: Extracellular matrix; Hyaluronan; Larynx; Sauropsida; Syrinx; Vocal control; Vocal production.