Olfactory responses of aquatic and terrestrial tiger salamanders to airborne and waterborne stimuli

Arzt, Adam H.; Silver, Wayne L.; Mason, J M; Clark, Larry

doi:10.1007/bf00603794

Cited by 18 publications

(18 citation statements)

References 14 publications

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“…Also the marine hermit crab Clibanarius vittatus has been shown to react to volatile compounds, where seawater containing volatiles from conspecific haemolymph stimulate shell investigation behaviour [24]. Olfactory responses that were conserved during the switch from an aquatic to a terrestrial lifestyle have been shown in the tiger salamander Ambystoma tigrinum , where airborne volatiles, volatile solution and amino acid solutions activated the olfactory epithelium in both aquatic larvae and terrestrial adults [25]. …”

Section: Discussionmentioning

confidence: 99%

Transition from sea to land: olfactory function and constraints in the terrestrial hermit crabCoenobita clypeatus

et al. 2012

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The ability to identify chemical cues in the environment is essential to most animals. Apart from marine larval stages, anomuran land hermit crabs (Coenobita) have evolved different degrees of terrestriality, and thus represent an excellent opportunity to investigate adaptations of the olfactory system needed for a successful transition from aquatic to terrestrial life. Although superb processing capacities of the central olfactory system have been indicated in Coenobita and their olfactory system evidently is functional on land, virtually nothing was known about what type of odourants are detected. Here, we used electroantennogram (EAG) recordings in Coenobita clypeatus and established the olfactory response spectrum. Interestingly, different chemical groups elicited EAG responses of opposite polarity, which also appeared for Coenobita compressus and the closely related marine hermit crab Pagurus bernhardus. Furthermore, in a two-choice bioassay with C. clypeatus, we found that water vapour was critical for natural and synthetic odourants to induce attraction or repulsion. Strikingly, also the physiological response was found much greater at higher humidity in C. clypeatus, whereas no such effect appeared in the terrestrial vinegar fly Drosophila melanogaster. In conclusion, our results reveal that the Coenobita olfactory system is restricted to a limited number of water-soluble odourants, and that high humidity is most critical for its function.

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Section: Discussionmentioning

confidence: 99%

Transition from sea to land: olfactory function and constraints in the terrestrial hermit crabCoenobita clypeatus

et al. 2012

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“…This is likely necessary not only to protect the epithelium from desiccation, but also to secrete odorant-binding proteins to aid in transporting volatile molecules across the layer of mucus. Interestingly, although no obvious morphological changes occur in the receptor cells at metamorphosis, physiological studies of Tiger Salamanders (Arzt et al, 1986) have shown that the larval epithelium responds more effectively to amino acids in solution, the adult epithelium to volatile compounds in air. This difference may be mediated by changes in the chemistry of the mucus (e.g., a change in odorant-binding protein expression).…”

Section: Implications For Functionmentioning

confidence: 98%

Olfactory metamorphosis in the Coastal Giant Salamander (Dicamptodon tenebrosus)

Stuelpnagel

Reiss

2005

Journal of Morphology

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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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“…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.…”

Section: The Ontogenetic Basis For Shifts In Chemosensory Receptionmentioning

confidence: 99%

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

Ferrer

Zimmer

2007

Journal of Experimental Biology

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SUMMARY Chemoreception may function throughout an entire animal lifetime, with independent, stage-specific selection pressures leading to changes in physiological properties, behavioral expression, and hence, trophic interactions. When the California newt (Taricha torosa) metamorphoses from an entirely aquatic larva to a semi-terrestrial juvenile/adult form, its chemosensory organs undergo dramatic reorganization. The relationship between newt life-history stage and chemosensory-mediated behavior was established by comparing responses of adults (as determined here) to those of conspecific larvae (as studied previously). Bioassays were performed in mountain streams,testing responses of free-ranging adults to 13 individual l-amino acids. Relative to stream water (controls), adults turned immediately upcurrent and moved to the source of arginine, glycine or alanine release. These responses were indicative of predatory search. Arginine was the strongest attractant tested, with a response threshold (median effective dose)of 8.3×10–7 mol l–1 (uncorrected for dilution associated with chemical release and delivery). In contrast to adult behavior, arginine suppressed cannibal-avoidance and failed to evoke search reactions in larvae. For a common set of arginine analogs, the magnitudes of adult attraction and larval suppression were not positively correlated. Suppression of cannibal-avoidance behavior in larvae was unaffected by most structural modifications of the arginine molecule. Adult behavior, on the other hand, was strongly influenced by even subtle alterations in the parent compound. Reactions to arginine in both adults and larvae were eliminated by blocking the external openings of the nasal cavity. Stimulating adult predatory search in one case and inhibiting larval cannibal avoidance in the other, arginine is a chemical signal with opposing behavioral effects and varying ecological consequences. Significant differences between responses of adults and larvae to changes in arginine structure suggest alternative, chemosensory receptor targets. Although arginine reception functions throughout an entire newt lifetime, an ontogenetic shift in larval and adult chemoreceptive ability changes behavioral expression, and thus, reflects the unique selection pressures that act at each life-history stage.

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Olfactory responses of aquatic and terrestrial tiger salamanders to airborne and waterborne stimuli

Cited by 18 publications

References 14 publications

Transition from sea to land: olfactory function and constraints in the terrestrial hermit crabCoenobita clypeatus

Transition from sea to land: olfactory function and constraints in the terrestrial hermit crabCoenobita clypeatus

Olfactory metamorphosis in the Coastal Giant Salamander (Dicamptodon tenebrosus)

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

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