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Selective ablation of antennular sensilla on the Caribbean spiny lobster Panulirus argus suggests that dual antennular chemosensory pathways mediate odorant activation of searching and localization of food

Pascal Steullet^*, Omar Dudar, Tanya Flavus, Min Zhou and Charles D. Derby

Department of Biology and Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30303, USA

View larger version (119K): [in a new window]   Fig. 1. An antennule and its setae of the Caribbean spiny lobster Panulirus argus. (A) Drawing of the spiny lobster showing the antennules with their lateral and medial flagella. The aesthetasc tuft, which contains aesthetasc sensilla and other associated setae, is located on the ventral side of the distal half of the lateral flagellum. Chemosensory neurons that innervate the setae, other than aesthetascs on the lateral and medial flagella, are collectively called ‘non-aesthetasc chemosensory neurons’. (B) Scanning electron micrograph showing part of the aesthetasc tuft of the lateral antennular flagellum, with aesthetasc sensilla (a), asymmetric setae (as), guard setae (gs) and companion setae (cs). Scale bar, 100 µm. (C) Scanning electron micrograph showing the non-tuft region of the lateral flagellum. Like the medial flagellum, this region has numerous non-aesthetasc setae, including plumose (ps) and setuled setae (ss) as well as chemosensilla such as hooded sensilla (hs) and simple sensilla (ms) of three lengths (short, medium and long) (Cate and Derby, 2000, 2001). Scale bar, 200 µm. (D) High-magnification scanning electron micrograph of three medium-length simple sensilla (ms), one short setuled seta (ss) and one plumose seta (ps). Scale bar, 50 µm. (E) High-magnification scanning electron micrograph of two hooded sensilla (hs) and one plumose seta (ps). Scale bar, 50 µm.

View larger version (186K): [in a new window]   Fig. 2. Scanning electron micrograph showing part of the aesthetasc tuft on the lateral antennular flagellum of group 4 animals; i.e. after only the aesthetascs (a) and asymmetric setae (as) had been ablated by shaving, without affecting the guard setae (gs) or any other setae. Pieces of the shafts of cut aesthetascs and other debris are indicated by arrows. Scale bar, 150 µm.

View larger version (18K): [in a new window]   Fig. 3. Success in finding food (the percentage of lobsters that successfully found a piece of squid) for sham control animals (group C) and eight groups of animals (groups 1–8) with specific sensory ablations of the antennules (see Table 1 for a description of the groups). An asterisk indicates that the success of a group of ablated lobsters is significantly different from that of the group of sham control lobsters (G-test; P lower than the critical value for a 5 % experiment-wise error rate as determined by a sequential test using the Dunn–idák method for eight planned comparisons) (Sokal and Rohlf, 1997). The number of trials was 20 (two trials for each of 10 lobsters) for all groups except group C (22 trials, 11 lobsters) and group 3 (18 trials, 10 lobsters).

View larger version (13K): [in a new window]   Fig. 4. Activation times (the latency for initiating searching) for sham control animals (group C) and eight groups of animals with specific sensory ablations of the antennules (groups 1–8). The groups are defined in Table 1 and are the same as in Fig. 3. An asterisk indicates that the activation time for a group of ablated lobsters is significantly different from that for the sham control lobsters (two-sample randomization test for median difference as the statistic; P lower than the critical value for a 5 % experiment-wise error rate as determined by a sequential test using the Dunn–idák method for eight planned comparisons) (Sokal and Rohlf, 1997). The horizontal dashed line indicates the maximum time (10 min) allowed for each lobster to become activated. For each group of lobsters, the median () and upper and lower quartiles are shown. Each group of ablated lobsters represents 10 animals, and the group of sham control lobsters contains 11 animals. This graph was prepared using the mean activation time from the two trials for each animal.

View larger version (15K): [in a new window]   Fig. 5. Search duration (the time to find squid following activation) for sham control animals (group C) and eight groups of animals with specific sensory ablations of the antennules (groups 1–8). The groups are defined in Table 1 and are the same as in Fig. 3. An asterisk indicates that the search duration of the group of ablated lobsters is significantly different from that of the group of sham control lobsters (two-sample randomization test for median difference as the statistic; P lower than the critical value for a 5 % experiment-wise error rate as determined by a sequential test using the Dunn–idák method for eight planned comparisons) (Sokal and Rohlf, 1997). An asterisk in parentheses indicates that the search duration of the group of ablated lobsters is close to being significantly different from that of the group of sham control lobsters (two-sample randomization test for median difference as the statistic; P values for group 8 and group 3 correspond respectively to 5.5 % and 7.6 % experiment-wise error rate as determined by a sequential test using the Dunn–idák method for eight planned comparisons) (Sokal and Rohlf, 1997). The horizontal dashed line indicates the maximum time (10 min) given to each activated lobster to find squid. For each group of lobsters, the median () and upper and lower quartiles are shown. The number of activated lobsters in groups C and 1–8 is 10, 3, 9, 8, 10, 7, 10, 10 and 9, respectively. The mean search durations were calculated only from those trials for which animals were activated to search.

View larger version (14K): [in a new window]   Fig. 6. Search mode (the proportion of time spent walking during searching) for sham control animals (group C) and eight groups of animals with specific sensory ablations of the antennules (groups 1–8). The groups are defined in Table 1 and are the same as in Fig. 3. For each group of lobsters, the median () and upper and lower quartiles are shown. The numbers of activated lobsters in groups C and 1–8 are the same as in Fig. 5. The values were calculated only from those trials for which animals were activated to search.

View larger version (13K): [in a new window]   Fig. 7. Effects of the removal of aesthetascs and asymmetric setae on the search responses (the time spent walking) over 3 min following stimulation of the antennules with a series of concentrations of artificial oyster odor. The responses before (filled squares) and after (open circles) shaving the aesthetascs and asymmetric setae are not significantly different (one-way MANOVA, P>0.05). Values are means ± S.E.M. from seven animals (three trials per animal).