Surface morphology and distribution of oropharyngeal taste papillae in sharks and rays (Elasmobranchii, Chondrichthyes): Implications for gustatory sensitivity

Abstract

Gustation or taste in elasmobranch fishes (sharks, skates, and rays) is an important sensory modality that dictates the palatability and ultimately the final decision regarding the ingestion of food. However, the surface morphology, size, abundance, and distribution of taste papillae in this group of apex predators has received little attention. This comparative study uses scanning electron microscopy, histology, and quantitative topographic analyses to assess the surface ultrastructure and density of taste papillae within the oropharyngeal cavity of six batoid species from three families and five selachian species from three families, all from a range of habitats and with a variety of diets. Within the batoids, mean taste papilla diameter ranges from 56 to 220 μm (with 0.7–1.6% of the papilla surface covered with sensory microvilli), while papilla diameter ranges from 152 to 360 μm in selachians (with 0.4–1.0% of the papilla surface covered with sensory microvilli). Both batoids and selachians possess two distinct size classes of papillae within the oropharyngeal cavity, where up to five small papillae (56–62 μm in diameter) often surround a large papilla (159–192 μm in diameter). There are significant differences in the total number of taste papillae within the oropharyngeal cavity in both superorders of elasmobranchs with a range of 2,119–20,317 in batoids (papillae occupying up to 3.1% of the oropharyngeal cavity with 0.05% of the cavity occupied by sensory microvilli) and a range of 1,354–11,890 in selachians (papillae occupying up to 1.7% of the oropharyngeal cavity with 0.02% of the cavity occupied by sensory microvilli) with taste papillae generally concentrated in areas used for food mastication. In batoids, papillae concentrate on ridges within the oropharyngeal cavities and in some species also on the oral valves (47–175 cm⁻¹ in the dorsal cavity, 33–160 cm⁻¹ in the ventral cavity). In selachians, the highest concentrations of taste papillae are on the oral valves and anterior regions of the oral cavity (4–215 cm⁻¹ in the dorsal cavity; 5–159 cm⁻¹ in the ventral cavity), which permits taste assessment during biting and manipulation of potential food items. This study is the first to investigate the abundance and distribution of taste papillae in the oropharyngeal cavity of a range of species of elasmobranchs, thereby improving our understanding of the importance of gustation, implications for oral food manipulation, and interpretations of both gustatory resolution and sensitivity.