Packaging and delivery of chemical weapons: a defensive trojan horse stratagem in chromodorid nudibranchs

• Published in: PloS one 2013-04, Vol.8 (4), p.e62075-e62075
• Main Authors: Carbone, Marianna, Gavagnin, Margherita, Haber, Markus, Guo, Yue-Wei, Fontana, Angelo, Manzo, Emiliano, Genta-Jouve, Gregory, Tsoukatou, Maria, Rudman, William B, Cimino, Guido, Ghiselin, Michael T, Mollo, Ernesto
• Format: Article
• Language: English
• Subjects: Adaptiveness; Animal Structures - anatomy & histology; Animal Structures - metabolism; Animals; Biological Factors - chemistry; Biological Factors - metabolism; Biology; Breakage; Chemical attack; Chemical weapons; Chemicals; Chemistry; Chemoreception; Chromatography; Chromodorididae; Decapoda; Earth Sciences; Evolution; Exudation; Feeding; Feeding Behavior; Gastropoda; Gastropoda - anatomy & histology; Gastropoda - metabolism; Glossodoris; Hardness; Histology; Malware; Marine mollusks; Metabolites; Mollusca; Mollusks; NMR; Nuclear magnetic resonance; Nudibranchia; Opisthobranchia; Organs; Packaging; Plant metabolites; Predators; Secondary metabolites; Shellfish; Skin; Studies; Weapons; Zoology
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0062075

Storage of secondary metabolites with a putative defensive role occurs in the so-called mantle dermal formations (MDFs) that are located in the more exposed parts of the body of most and very likely all members of an entire family of marine mollusks, the chromodorid nudibranchs (Gastropoda: Opisthobranchia). Given that these structures usually lack a duct system, the mechanism for exudation of their contents remains unclear, as does their adaptive significance. One possible explanation could be that they are adapted so as to be preferentially attacked by predators. The nudibranchs might offer packages containing highly repugnant chemicals along with parts of their bodies to the predators, as a defensive variant of the strategic theme of the Trojan horse. We detected, by quantitative (1)H-NMR, extremely high local concentrations of secondary metabolites in the MDFs of six species belonging to five chromodorid genera. The compounds were purified by chromatographic methods and subsequently evaluated for their feeding deterrent properties, obtaining dose-response curves. We found that only distasteful compounds are accumulated in the reservoirs at concentrations that far exceed the values corresponding to maximum deterrent activity in the feeding assays. Other basic evidence, both field and experimental, has been acquired to elucidate the kind of damage that the predators can produce on both the nudibranchs' mantles and the MDFs. As a result of a long evolutionary process that has progressively led to the accumulation of defensive chemical weapons in localized anatomical structures, the extant chromodorid nudibranchs remain in place when molested, retracting respiratory and chemosensory organs, but offering readily accessible parts of their body to predators. When these parts are masticated or wounded by predators, breakage of the MDFs results in the release of distasteful compounds at extremely high concentration in a way that maximizes their repugnant impact.