Olfactory metamorphosis in the Coastal Giant Salamander (Dicamptodon tenebrosus)

Abstract

This study examined the gross morphology and ultrastructure of the olfactory organ of larvae, neotenic adults, and terrestrial adults of the Coastal Giant Salamander (Dicamptodon tenebrosus). The olfactory organ of all aquatic animals (larvae and neotenes) is similar in structure, forming a tube extending from the external naris to the choana. A nonsensory vestibule leads into the main olfactory cavity. The epithelium of the main olfactory cavity is thrown into a series of transverse valleys and ridges, with at least six dorsal and nine ventral valleys lined with olfactory epithelium, and separated by ridges of respiratory epithelium. The ridges enlarge with growth, forming large flaps extending into the lumen in neotenes. The vomeronasal organ is a diverticulum off the ventrolateral side of the main olfactory cavity. In terrestrial animals, by contrast, the vestibule has been lost. The main olfactory cavity has become much broader and dorsoventrally compressed. The prominent transverse ridges are lost, although small diagonal ridges of respiratory epithelium are found in the lateral region of the ventral olfactory epithelium. The posterior and posteromedial wall of the main olfactory cavity is composed of respiratory epithelium, in contrast to the olfactory epithelium found here in aquatic forms. The vomeronasal organ remains similar to that in large larvae, but is now connected to the mouth by a groove that extends back through the choana onto the palate. Bowman's glands are present in the main olfactory cavity at all stages, but are most abundant and best developed in terrestrial adults. They are lacking in the lateral olfactory epithelium of the main olfactory cavity. At the ultrastructural level, in aquatic animals receptor cells of the main olfactory cavity can have cilia, short microvilli, a mix of the two, or long microvilli. Supporting cells are of two types: secretory supporting cells with small, electron-dense secretory granules, and ciliated supporting cells. Receptor cells of the vomeronasal organ are exclusively microvillar, but supporting cells are secretory or ciliated, as in the main olfactory cavity. After metamorphosis two distinct types of sensory epithelium occur in the main olfactory cavity. The predominant epithelium, covering most of the roof and the medial part of the floor, is characterized by supporting cells with large, electron-lucent vesicles. The epithelium on the lateral floor of the main olfactory cavity, by contrast, resembles that of aquatic animals. Both types have both microvillar and ciliated receptor cells. No important changes are noted in cell types of the vomeronasal organ after metamorphosis. A literature survey suggests that some features of the metamorphic changes described here are characteristic of all salamanders, while others appear unique to D. tenebrosus.

Larval development and metamorphosis of the olfactory and vomeronasal organs in the toad Rhinella (Bufo) arenarum (Hensel, 1867)

“…It would be exciting to explore whether different populations of olfactory receptor neurons are present in the adult larval-type sensory epithelium described here. Interestingly, a larval-type sensory epithelium has been described in the terrestrial coastal giant salamander Dicamptodon tenebrosus (Steulpnagel and Reiss 2005), and in the aquatic adult of the caecilian Typhlonectes compressicauda (Saint Girons and Zylberberg 1992). Surprisingly, somewhat resembling the situation in R. arenarum, the larval-type sensory epithelium of these amphibians is anteroventrally situated in the nasal region, and lacks associated Bowman's glands.…”

“…This change in lifestyle dramatically affects the anatomy, physiology and ecology of amphibians, mainly of anurans (Duellman and Trueb 1986). The olfactory and vomeronasal system of amphibians have been studied in caecilians (Badenhorst 1978;Billo and Wake 1987), caudates (Dawley and Bass 1988;Eisthen et al 1994;Dawley and Crowder 1995;Eisthen 1997Eisthen , 2000Steulpnagel and Reiss 2005), and anurans (Born 1876;Hinsberg 1901;Watanabe 1936;Rowedder 1937;Cooper 1943;Tsui 1946;Yvroud 1966;Northcutt and Royce 1974;Scalia 1976;Khalil 1978a,b;Taniguchi et al 1996a,b;Reiss and Burd 1997;Hansen et al 1998;Jermakowicz et al 2004;Wang et al 2008). The VNO appears early during development in most anuran amphibians, around the time of operculum development, and long before hindlimb development (Cooper 1943;Nieuwkoop and Faber 1956;Taniguchi et al 1996a,b;Tsui 1946;Wang et al 2008).…”

Chemosensory reception, behavioral expression, and ecological interactions at multiple trophic levels

“…As a consequence of life-history stage, profound changes occur in salamander olfactory epithelial morphology (Getchell et al, 1984;Stuelpnagel and Reiss, 2005) and electrophysiological responses to applied chemical stimuli (Arzt et al, 1986). Moreover, behavioral tests on California newt larvae and adults in response to arginine analogs suggest distinct chemosensory receptor populations in each life-history stage.…”

The role of olfaction throughout juvenile development: Functional adaptations in elasmobranchs

“…Significant size modifications could indicate a change in the importance of the olfactory system with increasing age of the individual. The sensory development in elasmobranchs after birth is difficult to compare to the development in teleosts and amphibians after hatching, as these often undergo metamorphosis, a period during which the olfactory system as well as other sensory modalities undergo significant changes (Appelbaum et al, 1983;Hara and Zielinski, 1989;Hansen and Zeiske, 1993;Stuelpnagel and Reiss, 2005).…”