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Mar Drugs
2023 Mar 16;213:. doi: 10.3390/md21030184.
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A Distinct Saponin Profile Drives an Olfactory-Mediated Aggregation in the Aquacultivated Sea Cucumber Holothuria scabra.
Claereboudt EJS
,
Claereboudt MR
,
Savarino P
,
Caulier G
,
Gaumez L
,
Deleu M
,
Gerbaux P
,
Eeckhaut I
.
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Intraspecific chemical communication between echinoderms has often been limited to prespawning aggregation. However, sea cucumber farmers have long observed year-round adult aggregation as a potential source of disease propagation and the suboptimal use of available sea pen acreage and food resources. In this study, through spatial distribution statistics, we demonstrated the significant aggregation of the aquacultivated sea cucumber Holothuria scabra both as adults in large sea-based pens and as juveniles in laboratory-based aquaria, proving that aggregation in these animals is not only observed during spawning. The role of chemical communication in aggregation was investigated using olfactory experimental assays. Our study established that the sediment that H. scabra feeds on as well as the water preconditioned by conspecifics induced positive chemotaxis in juvenile individuals. More specifically, through comparative mass spectrometry, a distinct triterpenoid saponin profile/mixture was identified to be a pheromone allowing sea cucumber intraspecific recognition and aggregation. This "attractive" profile was characterized as containing disaccharide saponins. This "attractive" aggregation-inducing saponin profile was, however, not conserved in starved individuals that were no longer attractive to other conspecifics. In summary, this study sheds new light on the pheromones in echinoderms. It highlights the complexity of the chemical signals detected by sea cucumbers and suggests a role of saponins well beyond that of a simple toxin.
Figure 7. Sea pens used for large-scale spatial distribution analyses of H. scabra adults. (A) Map of the position of the sea pens analyzed and located in the bay of Sarodrano near Toliara in Southwest Madagascar. (B) An example of a sea pen at low tide. (C) Example of the regular distribution of the 4 m2 quadrats (black squares) used to count the surface and buried adult H. scabra sea cucumbers in a sea pen (represented as grey rectangles G01–G08).
Figure 1. Histogram of sea cucumber density (ind. m−2) in considered quadrats. The percentage that each bar represents is indicated above each bar, and the average density is indicated with a dotted line.
Figure 2. Heat maps of the evolution of sea cucumber density over 12 h. A total of 40 juvenile H. scabra sea cucumbers were placed in a circular aquarium (radius of 60 cm) and were photographed hourly over 12 h. p-values of the MAD tests are displayed around each experimental circle. Significance (p < 0.05) is highlighted with a red border around the experiment. The density heat map is on a scale of 0 to 0.06 individuals per cm2.
Figure 3. Heat maps of the densities of juvenile sea cucumbers in each overnight experiment. Different numbers of sea cucumbers (n = 25, 20, and 10) were photographed in circular aquaria after a 12 h overnight period. The randomness of the spatial distribution of individuals was then analyzed through a maximum absolute deviation test. p-values of the tests are displayed under each experiment, and significance (p < 0.05) is highlighted with a red border around the experiment. The density heat map is on a scale 0 to 0.05 individuals/cm2.
Figure 4. Summary of the response of H. scabra juveniles to various types of stimuli tested in a Y-tube olfactometer. Dark grey portions of bars represent the percentage of n H. scabra juveniles that moved along the tube during each 10 min experiment. Light grey parts of the bars represent the proportion of individuals that did not move. The number of experiments (n) is annotated on the left of the chart for each stimulus. p-value of Fisher’s exact test of significance is annotated on the right of the bar graph with an asterisk (*) to indicate significance of movement compared to the control experiments. The proportion of moving and stationary individuals in control experiments in the absence of stimuli is indicated with a vertical dashed line.
Figure 5. MALDI ToF analysis of different Holothuria scabra extracts. Saponin ions (m/z +Na+) are indicated by a circle above their respective peaks. Saponins are named and described in Table 2. Disaccharide saponins are highlighted with a green circle, and stimuli that were attractive during behavioral assays are highlighted with a green tick mark.
Figure 6. Saponin structures of the disaccharide saponins that were unique to extracts that were attractive to H. scabra juveniles during olfactory behavioral assays.
Figure 8. Raw data collection from circular tank aggregation experiments. (A) Example of raw data collection from photographs of a circular aquarium containing 20 H. scabra juveniles. Using the software Fiji [44], the diameter of the tank was set to 60 cm, and the X and Y coordinates of the position of each cucumber were measured. (B) Example of how sea cucumber positions were projected onto the circumference of the tanks. The coordinates and angles shown in the two photos were the basis of further statistical tests.
Figure 9. Scheme of the experimental setup of olfactory behavioral assays. Thanks to the elevated stimulus tanks and the adjustment of the three taps (one on each stimulus tank, and one on the terminal tank), a laminar flow through the Y-tube was obtained. The stimulus flow in the olfactometer is represented by grey color.
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