Morphology of the teleost ampullary organs in marine salmontail catfish Neoarius graeffei (Pisces: Ariidae) with comparative analysis to freshwater and estuarine conspecifics

Abstract

We hypothesized that due to the relative conductivity of the environment, and to maintain sensory function, ampullary organs of marine Neoarius graeffei would differ morphologically from those described previously for estuarine and freshwater conspecifics. Unlike the ampullary systems of N. graeffei from freshwater and estuarine habitats, the ampullary pores of marine specimens occur in two distinct patterns; numerous pores seemingly randomly scattered on the head and ventro-lateral regions of the body, and pores arranged in distinctive vertical lines above the lateral line on the dorso-lateral body of the fish. Light and electron microscopy revealed that the ampullary organs also differed morphologically from estuarine and freshwater specimens in the presence of longer ampullary canals, a hitherto unreported canal wall composition, and in the collagen sheath surrounding both the canal and the ampulla proper within dermal connective tissues. Ampullary pores were wider in marine individuals and opened to the longest ampullary canals reported for this species. The canal wall was lined by cuboidal and squamous epithelial cells. Each ampullary canal opened into a single ampulla proper containing significantly more receptor cells than estuarine and freshwater conspecifics. The distribution of ampullary pores as well as the microstructure of the ampullary organs indicates that the electrosensory system of marine N. graeffei differs from those of estuarine and freshwater specimens in ways that would be expected to maintain the functionality of the system in a highly conductive, fully marine environment, and reveals the remarkable plasticity of this species' ampullary system in response to habitat conductivity.

Variations in electrosensory system morphology in teleost and elasmobranch fishes

“…argyropleuron were of a completely different type, being similar to the micro-ampullae found in freshwater silurids in shape, length, and quantity of receptor cells (Whitehead et al, 2015b). Specimens of Neoarius graeffei living in the estuarine reaches of the Brisbane River have ampullary canals that are longer than their freshwater counterparts, at up to 1.9 mm long, and possess more receptor cells (Whitehead et al, 1999;Gauthier et al, 2015).…”

“…Each ampulla proper is composed of 250 to 750 receptor cells (Friedrich-Freksa, 1930;Lekander, 1949;Bauer & Denizot, 1972;Obara, 1976). Marine Neoarius graeffei possess significantly longer ampullary organs then those found in freshwater and estuarine specimens, with more numerous receptor cells reaching a length of 600 µm with more than a 100 receptor cells per ampulla (Gauthier et al, 2015).…”

“…This pore leads to an ampullary canal filled with a highly conductive mucopolysaccharide gel (Doyle, 1967;Murray, 1974;Josberger et al, 2016). The wall of the ampullary canal is composed of epithelial cells that can be squamous, cuboidal or columnar depending on the species and environment (Herrick, 1901;Mullinger, 1964;Wachtel & Szamier, 1969;Obara & Sugawara, 1984;Whitehead et al, 1999;Gauthier et al, 2015). Tight junctions are present between canal wall cells to maximize electrical passage through the mucopolysaccharide gel, while underlying desmosomes bind adjacent cells (Waltman, 1966;Obara & Sugawara, 1984;Kramer, 1996;Whitehead et al, 1999;2002a;2002b;2015a;Gauthier et al, 2015).…”

“…The receptor cells are pear-shaped or elongate and their apices are exposed to the ampullary lumen. The exposed apex contains multiple microvilli (Herrick, 1901;Mullinger, 1964;Wachtel & Szamier, 1969;Kramer, 1996;Whitehead et al, 1999;2015b;Raschi & Gerry, 2003;Gauthier et al, 2015). In Chondrichthyes, there are several types of ampullae: simple, assembled, lobular, finger-shaped, and alveolar, many of which are composed of several sensory chambers, and are aggregated in ampullary clusters (Jørgensen, 2005).…”

“…Environmental factors thus affect the morphology of the ampullary organs of both elasmobranchs and teleosts (Whitehead, 2002a;Jørgensen, 2005;Kempster et al, 2012;Gauthier et al, 2015). To better understand the variations in the morphology of ampullary organ displayed in elasmobranchs and teleosts as well as their possible causes, thorough research of known modulations is needed.…”