The triterpene glycosides of Holothuria forskali: usefulness and efficiency as a chemical defense mechanism against predatory fish

Abstract

SUMMARYMore than 100 triterpene glycosides (saponins) have been characterized in holothuroids in the past several decades. In particular, Holothuria forskali contains 26 saponins in its Cuvierian tubules and 12 in its body wall. This high diversity could be linked to a chemical defense mechanism, the most commonly accepted biological role for these secondary metabolites. We performed an integrated study of the body-wall saponins of H. forskali. The saponins are mainly localized in the epidermis and in the mesothelium of the body wall and appear to be released when the holothuroid is stressed. Among the saponins present in the epidermis, one (holothurinoside G) was detected in the seawater surrounding non-stressed holothuroids and three others (holohurinosides C and F, and desholothurin A) were secreted when the animals were stressed. In addition, two new congeners (detected at m/z 1301 and 1317) were also present in the immediate surroundings of stressed holothuroids. These new saponins do not originate from the epidermis and could come from an internal organ. Quantities of secreted saponins were very low compared with the body wall and Cuvierian tubules concentrations. At natural concentrations, saponins do not represent a threat to the health of predatory fish. The deterrent effect of saponins seems therefore to act as an aposematic signal, warning potential predators of the unpalatability of the holothuroid tissues.

Discovery of Novel Saponins from the Viscera of the Sea Cucumber Holothuria lessoni

“…The presence of Holothurinosides C/C 1 (isomers), Holothurinosides A/A 1 (isomers), Desholothurin A (synonymous with Nobiliside 2A), Desholothurin A 1 and Holothurinosides E/E1 were also described in H . forskali by several groups [65,69,88]. We were not able to identify all the saponin congeners detected in the semi-pure extract in the HPCPC-fractionated samples.…”

“…While only a few studies have compared the saponin contents of the body wall with that of the cuvierian tubules in other species [50,60,61,62], to our knowledge, no study has investigated the contribution of saponins of the body wall or the viscera of Holothuria lessoni . Sea cucumbers expel their internal organs as a defense mechanism called evisceration, a reaction that includes release of the respiratory tree, intestine, cuvierian tubules and gonads through the anal opening [50,58,61,63,64,65,66,67,68]. We hypothesize that the reason for this ingenious form of defense is because these organs contain high levels of compounds that repel predators [60,61,69,70].…”

Effects of Holothuroid Ichtyotoxic Saponins on the Gills of Free-Living Fishes and Symbiotic Pearlfishes

“…The high toxicity showed by Cuvierian tubules does not, therefore, seem to be explained by the qualitative nature of the molecules in the cocktails. Rather, it may be due to the higher concentration of saponins present in the Cuvierian tubules, as shown by Van Dyck et al (2011). Parmentier and Vandewalle (2005) were the first to test carapid resistance to the presence of Cuvierian tubules.…”

“…In situ, predatory fishes that approach holothuroids are surrounded by saponins, which are constantly secreted (VanDyck et al, 2011). If these predators disturb the holothuroids, the latter emit higher concentrations and specific saponin congeners into the water (Van Dyck et al, 2011). Moreover, several species also expel some of their Cuvierian tubules through the cloacum, increasing the concentration of saponins in the surrounding water.…”

“…The final saponin concentration used in the 1-liter aerated aquaria was 200 g/ml, quantification being obtained through the weighing of the dried extract. The chosen concentration corresponds to the range of saponin concentration previously measured in the water conditioned by H. forskali (290 g/l; Van Dyck et al, 2011) and by Bohadschia vitiensis (250 g/l; Eeckhaut, unpubl. data).…”