The form and function of the digestive and respiratory systems of the marine pulmonate, Siphonaria zelandica
The marine pulmonate limpet Siphonaria Zelandica is commonly found in the mid-eulittoral zone in shallow pans or rock pools with dense algal growth. Though it resembles a true limpet externally, it is active when emersed during the ebbing of the tide browsing on small succulent algae, rather than grazing the surface film. The structure and function of the digestive and respiratory systems of Siphonaria were studied, particularly in relation to its adaptations to the intertidal mode of life.
The digestive system is relatively simple consisting of a large buccal mass with paired salivary glands, a spacious esophageal crop, a slightly muscular stomach with two digestive diverticula and a simple intestine-rectum.
The arrangement of the 28 muscles of the buccal mass and the odontophore is typical of patelliform pulmonates. The radula is a broad sheet with 144 ± 31 rows of teeth, each row having a tooth formula of (18±4) + (18±3) + (1) + (18±3) + (18±4). The radular teeth are continuously produced at a rate of 4.9 rows per day similar to those of active feeding herbivorous gastropods. The characteristics of the teeth and the movement of the mouth and the feeding traces showed that the feeding processes do not involve rasping of a hard substratum but browsing and scooping of soft lush algal growth.
The whole alimentary tract is lined by ciliated columnar cells of a basic form but with slight structural variations in different region. Those in the oesophagus and stomach contain apical vesicles and lysosome-like bodies indicating involvement in intracellular digestion, while those in the intestine contain various amounts of lipid and glycogen, functioning in active absorption and storage. The ciliated cells of the post-intestine, having a much folded basal plasma membrane are apparently involved in osmoregulation. The proteinaceous secretory cells in the crop and mid-intestine and the glycoprotein cells in the pro-intestine are either producing enzymes for extracellular digestion or secreting the faecal-binding sheath. Mucous cells interspersed among the ciliated cells of the oesophagus intestine and rectum produce mucoid material for lubrication and transport of food particles. The cuticular strip in the anterior chamber of the stomach, probably a vestigial gastric shield consists of tall non-ciliated cells with thick microvilli embedded in a dense fibrous matrix.
The salivary gland contains six cell types: grain cells, duct mucocytes, mucocytes I and mucocytes II, duct ciliated cells and undifferentiated cells. The first four are secretory, the grain cell being serous secretory and the other three muciparous, with varying amounts of mucopolysaccharides.
The tubules of the digestive gland are made up of five cell types, acinous digestive cells, neck digestive cells, crypt cells, vacuolated cells and undifferentiated cells. Both types of digestive cells participate in absorption and digestion. The high lipofuscin content in the neck digestive cell suggests its possible role in lipid digestion. The crypt cell with elaborate GER whorls and proteinaceous globules is apparently secretory, producing enzymes for extracellular digestion. Apocrinal secretion of the globules from the crypt cells was observed for the first time. The vacuolated cells appear to be degenerated crypt cells with an excretory function. The digestive gland tubule was found to undergo cyclic changes, correlated with the feeding activity which is related with the tides.
Enzyme assays showed the presence of various carbohydrases, proteolytic and lipolytic enzymes in the different region of the digestive system. The digestive gland is the main site of enzyme production. The pH optima of amylase, laminarinase and sucrase from various regions of the digestive tract were found to be within the pH range of the alimentary tract. The activities of various enzymes in the salivary gland and the oesophagus but not digestive gland were synchronous and correlated with feeding.
When emersed, Siphonaria respires atmospherically with the pneumostome wide open, and the mantle cavity functioning as a lung without any active ventilatory movements. When submerged, the mantle cavity is filled with water, a strong water current through the gill being created by the ciliated dorsal and ventral raphe behind the gill. The available respiratory surfaces include the sides of the foot, the anterior mantle roof and the single plicate gill. All these are lined by a thin epidermis with large blood spaces beneath it the non-ciliated epidermal cells in different regions carry different lengths of microvilli, apparently related to the degree of their protective role.
The respiratory physiology of Siphonaria was also studied. No tidal or diurnal rhythm in oxygen consumption was revealed. In unagitated conditions the aerial respiratory rate was much higher than the aquatic rate but with agitation, the aquatic rate increased to near the aerial rate. Cutaneous respiration constituted about 25% of the total. The respiratory rate varied with body weight, the coefficient b being temperature-independent (0.791 ± 0.122). Both aerial and aquatic respiratory rates increased with temperature. The highest temperature-sensitive range was 10-25°C in winter and 15-30°C in summer which coincided with the normal environmental temperature. No seasonal temperature acclimation was found within the normal thermal range.
Respiratory pigments haemocyanin and myoglobin were detected in the blood and buccal mass respectively. Their characteristics were studied and their role in oxygen transfer system was postulated. The reverse Bohr shift of the haemocyanin may facilitate oxygen uptake in the lung during burses of activity at low tide. A high oxygen-combining capacity of the buccal mass myoglobin (21.2 vol%) indicated a role of oxygen storage during bursts of feeding activity. The distribution of carbonic anhydrase in various tissues was consistent with a transfer system facilitating the release of metabolic CO2 from the buccal mass.
Finally the phylogenetic relationships of Siphonariidae with other groups of marine pulmonates were discussed. The unspecialised digestive system, the advanced form of nervous system and the possession of a secondary gill suggest that Siphonariidae, as a family, may not be an advanced derivative of any of the more primitive living basommatophoran groups, but could represent, along with the Gadiniidae, a specialized group which has originated directly from a primitive pulmonate stock and are adapted to life on exposed rock shores.
Advisor:Professor J.E. Morton; Dr R.M.G. Wells
School:The University of Auckland / Te Whare Wananga o Tamaki Makaurau
School Location:New Zealand
Source Type:Master's Thesis
Keywords:fields of research 270000 biological sciences 270700 ecology and evolution 270702 marine estuarine incl ichthyology
Date of Publication:01/01/1980