Variations in ampullary organ morphology and electroreception due to environmental characteristics in members of Siluriformes and Charcharhinidae

Whitehead, Darryl L. (2002). Variations in ampullary organ morphology and electroreception due to environmental characteristics in members of Siluriformes and Charcharhinidae PhD Thesis, Centre for Marine Studies, The University of Queensland.

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Author Whitehead, Darryl L.
Thesis Title Variations in ampullary organ morphology and electroreception due to environmental characteristics in members of Siluriformes and Charcharhinidae
School, Centre or Institute Centre for Marine Studies
Institution The University of Queensland
Publication date 2002
Thesis type PhD Thesis
Supervisor Ian Tibbetts
Total pages 143
Collection year 2002
Language eng
Subjects L
270603 Animal Physiology - Systems
770302 Living resources (incl. impacts of fishing on non-target species)
Formatted abstract
In this study, I examined the histological structure of ampullary organs of Arius graeffei native to freshwater systems. Two types of ampullary organs, Types II and III hereafter, are described from the freshwater specimens that both differ from the ampullary organs studied from estuarine members of the species. Type I. Both freshwater types of ampullary organs consist of a short canal (0.2-0.5 mm) that is oriented perpendicular to the basement membrane and ending in an ampulla. The ampullary canals contain an acidic mucopolysaccharide gel, which is uniform in its staining properties along the canals.

Type II ampullary organs consist of a canal, lined with cuboidal epithelial cells, which opens into an ampulla containing 50-60 receptor cells. Electron microscopy revealed that the pear-shaped receptor cells bear microvilli on their luminal surface and lie adjacent to an unmyelinated neuron. Type III ampullary organs differ from Type II in that the canal wall consists of cells that possess a protein-rich sac at the luminal apex and have a polymorphic nucleus. The canals of Type III ampullary organs open to an ampulla with 8-30 receptor cells that are similar in both staining properties and structure to those of the Type II organ. In both types of ampullary organs, supportive cells surround each receptor cell except at the apex of the receptor cell.

The resulting data provided cogent reasons to investigate the effects of differing levels of salinity on the histology of ampullary organs in juvenile A. graeffei. In this area of the study, variations were noted to occur in the average number of ampullary organs per square centimetre from areas of the head. In specimens held in estuarine waters (20-24 ppt) for 90 days ampullary density (45 ampullae/cm) changed only marginally from specimens studied on the day of capture (44 ampullae/cm). The average calculated from specimens held in freshwater for the same period of 90 days showed a change (27 ampullae/cm).

Skin samples from animals held in estuarine waters had ampullary organs that resemble Type I and Type II morphology. In this experiment, the animals in the freshwater treatment resembled those held in estuarine water up to and including Day 30 samples. Day 60 and Day 90 freshwater specimens revealed evidence of ampullary de- and regeneration, supportive of plastic changes in their histological structure. Degenerated ampullae were defined by the absence of neural terminals within the ampullae. Regenerating ampullary organs had neural terminals; low numbers of receptor cells, uncharacteristic bi-layers of supportive cells and had atypical canals opening to the skin surface.

Additionally, I examined the histology of ampullary organs in two members of the Plotosidae, Plotosus tandanus and Euristhmus lepturus, each being native to different levels of environmental salinity. In Plotosus tandanus, the ampullary pores give rise to a short canal (50-60 pim) produced by columnar epithelial cells bound together by tight junctions and desmosomes. At the junction of the canal and the ampulla, cuboidal epithelial cells make up the wall. The ampulla consists of layers of collagen fibers that surround flattened squamous epithelial cells in the lateral regions. At the base of the ampulla, these flattened cells give rise to supportive cells that encase a small number of receptor cells (10-15). The ovoid receptor cells possess microvilli along the luminar apical area. An unmyelinated neuron adjoins with each receptor cell opposite multiple presynaptic bodies. This form of micro-ampulla has not been previously described within the Plotosidae.

Euristhmus lepturus, an estuarine plotosid, possesses electroreceptors in the form of ampullae of Lorenzini. They are covered with linearly arranged ampullary pores that reach highest density upon the head of the fishes. The majority of these pores are connected to ampullae lying in the mid dorso-cranial region slightly anterior of the eyes. Along the trunk of the body lie four linear tracks of ampullary pores. These pores (125- 130 ^im, diameter) connect with canals that terminate in a single ampulla. The ampullary canal is composed of one to two layers of flattened epithelial cells, the basement membrane, and a complex collagen sheath. The internal cells lining the canal are adjoined via tight junctions and desmosomes. The ampulla contains receptor cells and thin supportive cells separated from the receptor cells by intercellular spaces of various sizes. The two cell types are joined only in their apico-lateral regions. Each receptor cell possesses microvilli on the apical surface that is exposed to the lumen of the ampulla, whereas supportive cells are smooth with small ridges along their surfaces. The receptor cells are attached to numerous neural terminals in the intercellular spaces, possessing several pre-synaptic bodies within the cell and lying opposite to this site of innervation. The supportive cells are elongate and narrow structures that pass from the basement membrane to the lumen of the ampulla.

Ampullae of Lorenzini were examined from Carcharhinus leucas captured in the freshwater reaches of the Brisbane River. Ampullary pores (140 - 205 \im, diameter) are distributed across the head area of the shark. The total counts of ampullary pores in the two specimens studied were 2681 and 2913. The ampullary canals consist of squamous epithelial cells possessing vacuoles that contain a darkly staining material. There are two general forms of the canal epithelial cells, flattened squamous and ridged cells that contain a high density of vacuoles and appear to release material into the lumen of the canal.

The ampullae of Carcharhinus leucas contain numerous receptor and supportive cells bound by tight junctions and desmosomes. The pear-shaped receptor cells possess a single kinocilium that extends into the ampullary lumen. Along the basal surface of the receptor cells are junctions with unmyelinated neural terminals. Apically nucleated supportive cells produce a rigid ampullary wall and possess a low number of microvilli. These two cells types produce sensory alveoli that are surrounded by squamous epithelial cells that together produce a marginal zone. A central centrum cap consisting of a luminal layer of cuboidal epithelial cells overlying squamous epithelial cells lies in the centre of the basal ampullary region. This overlies the primary incoming afferent nerve, which radiates from this central area to divide and connect with all receptor cells.

The results reported here represent the first detailed analysis of the morphology of the ampullary organs of siluriforms and a carcharhinid that inhabit environments of varying salinities. This work confirms previous conjecture that variation in salinity, and thereby conductivity, result in the reported histological variations that exist between freshwater and marine electroreceptive fishes. The study also provides an elemental test of the direct effects of changes in habitat salinity on ampullary organ morphology.
Keyword Catfishes.
Additional Notes

Variant title : Ampullary organ morphology

Note: Thesis does not contain a Title Page

Document type: Thesis
Collection: UQ Theses (RHD) - UQ staff and students only
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Created: Fri, 24 Aug 2007, 17:51:29 EST