Abstract

ABSTRACTGustation in sharks is not well understood, especially within species that ingest food items using suction. This study examines the morphological and immunohistochemical characterisation of taste papillae and oral denticles in the oropharynx of the brown-banded bamboo shark Chiloscyllium punctatum and compares their distribution during development. Taste papillae of C. punctatum are located throughout the oropharyngeal region and are most concentrated on the oral valves (2125-3483 per cm2 in embryos; 89-111 per cm2 in mature adults) close to the tooth territories. Papillae appearance is comparable at all stages of development, with the exception of the embryos (unhatched specimens), where no microvilli are present. Oral valve papillae are comparable in structure to Type I taste buds of teleost fishes, whereas those of the rest of the oropharyngeal region are comparable to Type II. Both types of papillae show immunofluorescence for a number of markers of taste buds, including β-Catenin and Sox2. Taste papillae densities are highest in embryos with 420-941 per cm2 compared to 8-29 per cm2 in mature adults. The total number of papillae remains around 1900 for all stages of development. However, the papillae increase in diameter from 72±1 μm (mean±s.e.m.) in embryos to 310±7 μm in mature individuals. Microvilli protrude in multiple patches at the apical tip of the papilla covering ∼0.5% of the papillar surface area. We further document the relationship between taste papillae and the closely associated oral denticles within the shark orophayngeal cavity. Oral denticles first break through the epithelium in the antero-central region of the dorsal oral cavity, shortly after the emergence of teeth, around time of hatching. Denticles are located throughout the oropharyngeal epithelium of both immature and mature stages, with the highest concentrations in the antero-dorsal oral cavity and the central regions of the pharynx. These denticle-rich areas of the mouth and pharynx are therefore thought to protect the epithelium, and importantly the taste papillae, from abrasion since they correlate with regions where potential food items are processed or masticated for consumption. Taste papillae and denticles are more dense in anterior oropharyngeal regions in close association with the oral jaws and teeth, and in the juvenile or hatchling shark taste units are functional, and innervated, allowing the shark to seek out food in utero, at birth or on emergence from the egg case.

Highlights

  • Taste buds are secondary sense organs of the gustatory chemosensory system involved in the evaluation of food quality

  • Our findings reveal that taste papillae appear early in development, closely linked with the timing of tooth development (Rasch et al 2016) and we show that these taste buds are functional during later stages of embryo development before hatching

  • This is in stark contrast to mammals, where taste buds are distinctly localised to specific pockets of epithelia mainly on the tongue

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Summary

Introduction

Taste buds are secondary sense organs of the gustatory chemosensory system involved in the evaluation of food quality. Taste buds in teleost fish are more numerous than in any other animal (Kasumyan and Døving, 2003), yet they are poorly understood Within teleost fishes, they are present on the surface of the skin, lips, fins and barbels as well as within the epithelia of the oral cavity, pharynx, oesophagus and gills (Jakubowski and Whitear, 1990; Reutter et al, 2000). They are present on the surface of the skin, lips, fins and barbels as well as within the epithelia of the oral cavity, pharynx, oesophagus and gills (Jakubowski and Whitear, 1990; Reutter et al, 2000) Their broad distribution distinguishes teleosts from other gnathostomes, which only contain taste buds within the oral cavity. Taste buds are comprised of receptor cells, support cells and sometimes basal cells and are innervated by branches of the VII (facial), IX (glossopharyngeal) and X (vagal) cranial nerves (Reutter, 1992)

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