Odours detected by rhinophores mediate orientation to flow in the nudibranch mollusc,Tritonia diomedea

Abstract

SUMMARY Tritonia diomedea is a useful neuroethological model system that can contribute to our understanding of the neural control of navigation. Prior work on both sensory and locomotory systems is complemented by recent field experiments, which concluded that these animals primarily use a combination of odours and water flow as guidance cues. We corroborate these field results by showing similar navigation behaviours in a flow tank. Slugs crawled upstream towards both prey and conspecifics, and turned downstream after crawling into a section of the flow tank downstream of a predator. Controls without upstream odour sources crawled apparently randomly. We then tested whether these behaviours depend on odours detected by the rhinophores. Outflow from a header tank was used to generate prey, predator and unscented control odour plumes in the flow tank. Slugs with rhinophores crawled upstream towards a prey odour plume source, turned downstream in a predator odour plume, and showed no reaction to a control plume. Slugs without rhinophores behaved similarly to controls, regardless of odour plume type. Finally, we used extracellular recordings from the rhinophore nerve to demonstrate that isolated rhinophores are chemosensitive. Afferent activity increased significantly more after application of all three odour types than after unscented control applications. Responses were odour specific. We conclude that rhinophores mediate orientation to flow, and suggest that future work should focus on the integration of mechanosensation and chemosensation during navigation in T. diomedea.

Functional neuroanatomy of the rhinophore of Archidoris pseudoargus

“…The lack of any obvious olfactory glomeruli in Archidoris may indicate that the rhinophore may not serve in the Wrst line as an olfactory organ for long distance reception of odorants and may be a primarily tactile or rheotaxic organ. In favour of the rhinophores as an olfactory organ Wyeth and Willows (2006) showed the importance of predator or prey odour plumes for navigational response in Tritonia. Receptor neurons within the rhinophore epithelium of Archidoris may not be very sensitive to stimulation with amino acids.…”

Chemical Defenses: From Compounds to Communities

“…The specialist nudibranch Tritonia diomedea used watersoluble cues in flow to move toward its prey and toward conspecifics in laboratory experiments (Wyeth and Willows, 2006b). In Y-maze experiments, T. diomedea consistently moved toward chemical cues, but the chemotaxis response was eliminated with the removal of rhinophores, the major olfactory organ in opisthobranchs (Chase, 2002).…”

“…In Y-maze experiments, T. diomedea consistently moved toward chemical cues, but the chemotaxis response was eliminated with the removal of rhinophores, the major olfactory organ in opisthobranchs (Chase, 2002). Using an en passant suction electrode to measure action potentials from neurons in rhinophores isolated from T. diomedea, Wyeth and Willows (2006b) detected significant increases in the number and frequency of action potentials associated with waterborne cues from prey, predator, and conspecific individuals. These experiments also indicated that physical properties such as flow affect the ability of T. diomedea to use olfaction to detect prey and conspecifics in the laboratory (Wyeth and Willows, 2006b), and video analysis demonstrated that water flow affects chemotaxis similarly in the field (Wyeth and Willows, 2006a).…”

“…Using an en passant suction electrode to measure action potentials from neurons in rhinophores isolated from T. diomedea, Wyeth and Willows (2006b) detected significant increases in the number and frequency of action potentials associated with waterborne cues from prey, predator, and conspecific individuals. These experiments also indicated that physical properties such as flow affect the ability of T. diomedea to use olfaction to detect prey and conspecifics in the laboratory (Wyeth and Willows, 2006b), and video analysis demonstrated that water flow affects chemotaxis similarly in the field (Wyeth and Willows, 2006a). An important component of understanding this specialist behavioral response will be the structural elucidation of compounds that interact with the neurological receptors in T. diomedea.…”

One rhinophore likely provides sufficient sensory input for odour-based navigation by the nudibranch mollusc,Tritonia diomedea

“…By contrast, aquatic gastropods also often have a primary reliance on odour-based navigation (Croll, 1983;Cummins and Wyeth, 2014), yet have more narrowly spaced sensory structures and a lower typical speed of locomotion that might lead to differences in navigation adaptations when compared with the faster taxa. Our objective then was to build on recent efforts (Ferner and Weissburg, 2005;Wilson and Weissburg, 2012;Wyeth and Willows, 2006b;Wyeth et al, 2006) to explore the navigational strategies used by gastropods in turbulent odour plumes. A parallel motivation was to isolate the sensory structures that contribute to odour-based navigation in the nudibranch Tritonia diomedea (Bergh 1894) (synonymous with Tritonia tetraquetra; Martynov, 2006).…”