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First published online March 30, 2006
Journal of Experimental Biology 209, 1441-1453 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02164

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

Russell C. Wyeth^* and A. O. Dennis Willows

Department of Biology, University of Washington, Seattle, WA 98195-1800, USA and Friday Harbor Laboratories, 620 University Road, Friday Harbor, WA 98250, USA

View larger version (14K): [in a new window]   Fig. 1. Flow tank schematic. Seawater was first piped into a tilted inflow tank (95 cm wide, not shown), passing over or under four barriers, before spilling into the flow tank across its full width (black arrows). Flow continued through a 0.75 cm thick Plexiglas baffle (bf) drilled with 0.75 cm holes, two upstream grilles (ug1 and ug2; 1 cm square mesh, 0.75 cm thick), a behavioural arena (ba), and a downstream grille (dg) to prevent slugs being swept out of the tank, before spilling over the downstream end wall (cut 2 cm lower than the other tank walls). Plexiglas walls spanning the gap between the upstream grilles created an odour stimulus chamber (osc). This design created unidirectional flow through the behavioural arena with enough turbulence to spread fluorescein dye plumes (grey approximates the average plume shape) similarly to plumes in the field (Wyeth and Willows, in press). Odor plumes will be similar to these dye plumes since flow dominates chemical transport under such conditions (Vogel, 1994). The 2nd upstream grille also served to obscure any downstream flow patterns characteristic of the odour sources (Vogel, 1994). Flow tank width, 1 m.

View larger version (40K): [in a new window]   Fig. 2. Tritonia diomedea detect and locate upstream prey odour sources in the flow tank. T. diomedea tracks with (solid lines) and without (dotted lines) their prey in an upstream odour stimulus chamber (osc). With upstream prey, eight of nine slugs crawled upstream to make direct contact with the upstream grille, and seven of nine found the osc (x marks point of first contact with upstream grille). In controls, only one slug crawled directly upstream, three eventually reached the upstream grille crawling after contact with the sidewalls, and none found the empty osc (o marks point of first contact with upstream grille). Tracks are projected onto a scaled and simplified flow tank diagram. Flow tank width, 1 m.

View larger version (55K): [in a new window]   Fig. 3. Tritonia diomedea often detect and locate upstream conspecific odour sources in the flow tank. T. diomedea tracks with (solid lines) and without (dotted lines) conspecifics in an upstream odour stimulus chamber (one slug in osc, two slugs in osc*). With upstream conspecifics, 12 of 20 slugs crawled upstream to make direct contact with the upstream grille and seven found the osc (x marks point of first contact with upstream grille). Only two slugs in controls crawled upstream to make contact with the upstream grille without first contacting the side walls of the tank, and none found the empty osc (o marks point of first contact with upstream grille). Tracks are projected onto a scaled and simplified flow tank diagram. Flow tank width, 1 m. See Fig. 3 movie in supplementary material for an example movie.

View larger version (29K): [in a new window]   Fig. 4. Tritonia diomedea detects and turns away downstream from upstream predators in the flow tank. T. diomedea tracks with a predator (solid lines) and controls (dotted lines) with similarly shaped latex tubing in the odour stimulus chambers (osc). With an upstream predator, those slugs that crawled into a plume zone downstream of the predator had a greater tendency to turn downstream. The inset shows the downstream turn magnitude (P=predator; C=control) measured by comparing mean crawling headings for the 2 min on either side of the estimated plume zone entry points (+). Slugs in four experimental trials (x) and two control trials (o) crawled upstream and contacted the second upstream grille without entering the plume zone. A further three animals (2 controls, 1 experimental) reached neither the plume zone nor the upstream grille. Tracks are projected onto a scaled and simplified flow tank diagram. Flow tank width, 1 m.

View larger version (91K): [in a new window]   Fig. 5. Tritonia diomedea without rhinophores do not show navigational responses to prey and predator odour plumes. Each image is a mean projection of a motion enhanced video recording of a slug (s) crawling in the flow tank, showing slug movement (direction shown by arrowheads) and the dyed odour plume (`o', odour plume source; flow is from left to right). With rhinophores, slugs crawling cross-stream responded with upstream crawling when encountering a prey odour plume (A) or a downstream turn away from predator odour (B). Without rhinophores, slugs showed no response to odour plumes (C,D). Elapsed time (min) is shown in A–D. Scale bar, 25 cm. See Fig. 5 movies in supplementary material for the videos corresponding to A–D in this figure.

View larger version (31K): [in a new window]   Fig. 6. A greater response in the rhinophore nerve to prey odour than to control. (A) Extracellular activity was greatest in response to perfusion of prey odour through the sensory tuft, with a lesser increase over baseline in response to control seawater. Bar indicates odour stimulus duration. Scale: 10 µV between < and marks. (B) Raster plots of extracellular spikes surpassing +10 but not +20 µV (< and , respectively, in A) for all five trials on this rhinophore (+,x,o indicate the raster plots for the recordings in A). (C) Mean spike counts with standard error bars from all five trials, grouped into ten intervals. This rhinophore responded more strongly, on average, to seawater with prey odours than control seawater. Time for B and C is measured relative to the perfusion stream switch for prey and control applications, and an arbitrary time between trials for baseline. Broken lines show the time window used for spike count analysis.

View larger version (24K): [in a new window]   Fig. 7. A greater response in the rhinophore nerve to conspecific odour than to control. (A) Extracellular activity was greatest in response to perfusion of conspecific (consp.) odour through the sensory tuft, with a lesser increase over baseline in response to control seawater. Bar indicates odour stimulus duration. Scale: 8 µV between < and marks. (B) Raster plots of extracellular spikes surpassing +9 µV but not +17 µV (< and , respectively, in A) for all five trials on this rhinophore (+,x,o indicate the raster plots for the recordings in A). (C) Mean spike counts with standard error bars from all five trials grouped into ten intervals. This rhinophore responded more strongly on average, to seawater with conspecific odours than control seawater. Time for B and C is measured relative to the perfusion stream switch for conspecific and control applications, and an arbitrary time between trials for baseline. Broken lines show time window used for spike count analysis.

View larger version (12K): [in a new window]   Fig. 8. Rhinophores are responsive to prey (A), predator (B) and conspecific odours (C). Mean normalized spike counts are shown with standard error bars, for seven rhinophores tested for responses to prey odour, seven for predator odour, and ten for conspecific odour. Responses to all three odour types are significantly greater than controls (Table 4). Controls were consistently greater than baseline for prey and conspecific odours, although significant in only 2 of 6 tests (Table 4).

View larger version (45K): [in a new window]   Fig. 9. Extracellular spike waveforms are responsive to predator odour. (A,B) Spikes during perfusion of control seawater (white) and seawater with predator odour (black) are overlaid. Control waveforms are drawn after predator odour waveforms and waveform transparency is scaled to the total number of waveforms displayed. Consequently, any distinct dark areas indicate waveforms with higher relative frequency during perfusion of predator odour. The number of waveforms displayed is given for each treatment type (controls, white; predator odour, black). (Ai–vii) All large amplitude spikes in the analysis window (the voltage level defining `large' is consistent for each rhinophore). (Bi–vii) Only waveforms that matched a template using Spike2 software. For each rhinophore tested (i–vii), amongst the various large magnitude waveforms recorded (A), a single group of dark waveforms with distinct shape can be seen, and can be sorted using templates (B). This waveform occurred either not at all, or at much lower frequency during perfusion of control seawater. In rhinophore vii, spontaneous unresponsive activity was too great to visualize the responsive waveform, and therefore waveforms matching the six most frequent templates are not drawn in A to avoid obscuring rarer waveforms. Scale bars (20 µV) apply to A and B for each rhinophore.

View larger version (43K): [in a new window]   Fig. 10. Tritonia diomedea are inconsistent in their ability to stimulate rhinophore responses. Eight rhinophores were established as responsive to seawater with conspecific odour isolated from multiple slugs. Responses were then recorded to odours from a pair of non-mating slugs and a pair of mating slugs. Shown are the mean normalized spike counts with standard errors, for each rhinophore for applications of control seawater, non-mating pair seawater, and mating pair seawater. Lines link non-significant pairwise comparisons between treatments within each rhinophore (ANOVA, followed by Tukey's pairwise mean comparisons, P=0.05); *means significantly different from both other treatments. Conspecific responsive units in the rhinophores did not respond equally to odours isolated from specific pairs of T. diomedea, suggesting that the odours are only intermittently released.

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