The Gustatory System of Elasmobranchs: morphology, distribution and development of oral papillae and oral denticles

Carla Atkinson (2011). The Gustatory System of Elasmobranchs: morphology, distribution and development of oral papillae and oral denticles PhD Thesis, School of Biomedical Sciences, The University of Queensland.

       
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Author Carla Atkinson
Thesis Title The Gustatory System of Elasmobranchs: morphology, distribution and development of oral papillae and oral denticles
School, Centre or Institute School of Biomedical Sciences
Institution The University of Queensland
Publication date 2011-03
Thesis type PhD Thesis
Supervisor Prof Shaun Collin
Dr Ian Tibbetts
Total pages 164
Total colour pages 6
Total black and white pages 158
Language eng
Subjects 11 Medical and Health Sciences
Abstract/Summary Abstract The gustatory system in cartilaginous fishes has received almost no attention despite the importance of this sense in this vertebrate group of apex predators. Gustation determines the palatability of food prior to ingestion. For the first time, the morphology and distribution of taste buds and denticles in a range of elasmobranchs (selachians and batoids) is examined both during development and in adults. Representatives of the two major orders are analysed including two species from the family Rhinobatidae; Aptychotrema rostrata (Shaw, 1794), Trygonorrhina fasciata (Müller & Henle, 1841), three species from the family Dasyatidae; Dasyatis fluviorum (Ogilby, 1908), Neotrygon kuhlii (Müller & Henle, 1841), Taeniura lymma (Forsskål, 1755), and one species from the family Gymnuridae; Gymnura australis (Ramsay & Ogilby, 1886), which form the batoid clade. Included in the selachians are two species from the family Orectolobidae; Orectolobus maculatus (Bonnaterre, 1778), and Orectolobus ornatus (De Vis, 1883), two species from the family Hemiscylliidae; Chiloscyllium punctatum (Müller & Henle, 1838), Hemiscyllium ocellatum (Bonnaterre, 1788), and two species from the family Carcharhinidae; Carcharhinus melanopterus (Quoy & Gaimard, 1824), and Negaprion acutidens (Rüppell, 1837). Papillae of putative taste buds are located throughout the oropharyngeal epithelium of the six batoid species from three families and the six selachian species from three families. There appears to be two types of taste buds in the selachian oropharyngeal cavity. Those that are located on the oral valves protrude a greater distance above the surrounding epithelium and are comparable in structure and distribution to Type I taste buds of teleost fishes, whereas those papillae located in the oral cavity and pharynx protrude a lesser distance and are comparable to Type II taste buds of teleost fishes. The presence of Type III taste buds (previously identified in teleosts), found within epithelial pores, cannot be unequivocally confirmed although similar structures were identified in G. australis and C. melanopterus. D. fluviorum and N. kuhlii have two distinct size classes of papillae within the oropharyngeal cavity where up to five small papillae (56-62μm in diameter) often surround large papillae (159-192μm in diameter). Microvilli protruding from papillae in the batoid species resemble solitary chemosensory cells, occur in small groups all over the papilla surface and cover 0.7-1.6% of the papilla surface area. Microvilli of the selachian papillae also protrude in multiple groups but from a more localised area on the apical tip of the papilla and cover 0.4-1.6% of the papilla surface area. Papillae diameters range from approximately 150μm in N. acutidens (TL 1,209mm) to 360μm in O. maculatus (TL 1,172mm). Papillae size does not correlate with the total length of the animal i.e. larger specimens do not necessarily have larger papillae. Ontogenetic studies with C. punctatum, however, revealed that taste papillae increase in diameter as the animal grows, i.e. 72 ± 1μm in embryos to 310 ± 7μm in mature individuals. Putative taste papillae appear to concentrate in areas of food mastication. In selachians the highest concentrations are on the oral valves and anterior regions of the oral cavity, which suggests the biting and manipulation of prey with the jaws is also important for taste assessment. In batoids, papillae are concentrated on ridges within the oropharyngeal cavities and, in some species, also occur on the oral valves. Elasmobranchs appear to have relatively low densities of taste buds when compared with teleost fishes, which may have 800+ taste buds per cm2. The lowest density recorded in this study was 4 taste buds per cm2 in the oral cavity of O. maculatus, whereas the greatest density recorded was 159 taste buds per cm2 in the pharynx of T. fasciata. It is suggested that the low densities recorded may be a result of the large size many of these species attain, as ontogenetic studies with C. punctatum revealed papillae densities are highest in embryos, with 420-941 taste buds per cm2, compared to mature adults, with 8-29 taste buds per cm2. Total numbers of papillae range from ~1,350-2,000 in benthic selachians to as high as ~9,250-11,900 in pelagic species. Ontogenetic studies on C. punctatum identified that the number or papillae remains constant throughout all stages of development, with ~1,900 papillae present in embryos, hatchlings, immature and mature adults. Possessing more papillae, however, does not necessarily equate to a greater gustatory sensitivity as the percentage area of the oropharyngeal cavity covered by the papillae was lowest in N. acutidens (0.900%), which has the highest total number of papillae (11,890 papillae). Previous studies on the denticles (placoid scales) in the external epidermis of elasmobranchs is abundant and their form has been used as a technical model to prevent hydrodynamic drag, which has been implemented in various ways including athletic swimwear (Speedo Fastskin®). The function of denticles within the oropharyngeal cavity of elasmobranchs, however, is still being debated. Of the batoids analysed, no denticles are found in the Gymnuridae or Dasyatidae families, however they are present in the Rhinobatidae. Oral denticles are present in all the selachians analysed, except in the Orectolobidae. In C. punctatum, they appear to first break through the epithelium in the anterior central region of the dorsal oral cavity around the time of hatching. The denticles of the carcharhinids have a grooved surface and a central spine, which is angled towards the posterior of the mouth. This structure is beneficial to reduce hydrodynamic drag which would be advantageous to these free swimming species that use ram ventilation. T. fasciata also has denticles with a ridged crown. Sometimes these ridges form circles around taste papillae and may therefore direct water flow over these organs as the animal swims, possibly helping to locate a food source. Alternatively, H. ocellatum and C. punctatum have broad bulbous denticles that often overlap. These denticles would provide a hard surface to protect the epithelium from abrasion during the consumption of hard bodied prey items. The number and distribution of oral denticles appears to compromise that of the taste papillae. For example, A. rostrata has no denticles over the gill arches, where there are numerous taste papillae. This thesis contains the first comparative analyses of elasmobranch taste bud morphology in which there seem to be many consistencies among species, at least externally. Some morphological features described suggest that elasmobranch taste buds may be an intermediate form between Schneider organs and teleost taste buds. The gustatory system is not easy to research, however elasmobranchs form the earliest group of jawed fishes and can help us to understand the evolution of this important sensory system. Research into the electrophysiology of elasmobranch taste, taste preferences would also help us to understand these apex predators and their behaviour and this knowledge could be further utilised when producing shark repellents to not only protect humans but also to protect fishing gear and other industrial apparatus within the oceans. There is still much to learn about the elasmobranch gustatory system. Unfortunately, difficulties may arise due to the apparent scarcity of these organs. The discovery of a genetic probe or immunohistochemical label for taste cells could help elucidate this inconsistency and clarify whether the taste cells are apoptotic or rare.
Keyword Chemoreception
gustation
Taste
taste bud
elasmobranch
oral denticle
sensory biology
ecology
brown-banded bamboo shark
solitary chemosensory cell

 
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