2005Journal of MorphologyRequires access

Olfactory metamorphosis in the Coastal Giant Salamander (Dicamptodon tenebrosus)

Jeremy T. Stuelpnagel, J. Reiß

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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.

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What this paper is about

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.

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Available 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.

Key concepts: Biology, Metamorphosis, Salamander, Zoology, Ecology, Evolutionary biology, Larva

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