Distribution of Defensive Metabolites in Nudibranch Molluscs
Many plants and animals store toxic or unpalatable compounds in tissues that are easily encountered by predators during attack. Defensive compounds can be produced de novo, or obtained from dietary sources and stored directly without selection or modification, or can be selectively sequestered or biotransformed. Storage strategies should be optimized to produce effective defence mechanisms but also prevent autotoxicity of the host. Nudibranch molluscs utilize a diverse range of chemical defences, and we investigated the accumulation and distribution of defensive secondary metabolites in body tissues of 19 species of Chromodorididae nudibranchs. We report different patterns of distribution across tissues, where: 1) the mantle had more or different (but structurally related) compounds than the viscera; 2) all compounds in the mantle were also in the viscera; and 3) the mantle had fewer compounds than the viscera. We found no further examples of species that selectively store a single compound, previously reported in Chromodoris species. Consistent with other studies, we found high concentrations of metabolites in mantle rim tissues compared to the viscera. Using bioassays, compounds in the mantle were more toxic than compounds found in the viscera for Glossodoris vespa Rudman, 1990 and Ceratosoma brevicaudatum Abraham, 1876. In G. vespa, compounds in the mantle were also more unpalatable to palaemonid shrimp than compounds found in the viscera. This indicates that these species may modify compounds to increase bioactivity for defensive purposes and/or selectively store more toxic compounds. We highlight clear differences in the storage of sequestered chemical defences, which may have important implications for species to employ effective defences against a range of predators.
KeywordsTerpenes Chemical defences Sequestration, marine molluscs Aposematism Natural products Bioactivity
We would like to thank Talia Pettigrew and Gloria Miller for help with chemical extractions and Sean Young for help running assays. This work was funded by the Australian Pacific Science Foundation (APSF) (awarded to KLC and MJG) and The University of Queensland Promoting Women Fellowship (awarded to KLC). Anne Winters was supported by an Endeavour Postgraduate Scholarship.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
- Angas GF (1864) Description d’especes nouvelles appurtenant a plusiers genres de Mollusques Nudibranches des environs de Port-Jackson (Nouvelle-Galles du Sud), accompagnee de dessins faits d’apres nature (GFA & H Crosse). J Conchyliol 12:43–70 pls. 4–6Google Scholar
- Avila C (1995) Natural products of opisthobranch molluscs: a biological review. Ocean Mar Biol 33:487–559Google Scholar
- Carbone M, Gavagnin M, Haber M, Guo YW, Fontana A, Manzo E, Genta-Jouve G, Tsoukatou M, Rudman WB, Cimino G, Ghiselin MT, Mollo E (2013) Packaging and delivery of chemical weapons: a defensive Trojan horse stratagem in chromodorid nudibranchs. PLoS One 8:e62075CrossRefPubMedPubMedCentralGoogle Scholar
- Cheney KL, White A, Mudianta IW, Winters AE, Quezada M, Capon RJ, Mollo E, Garson MJ (2016) Choose your weaponry: selective storage of a single toxic compound, latrunculin A, by closely related nudibranch molluscs. PLoS One 11:e0145134. https://doi.org/10.1371/journal.pone.0145134 CrossRefPubMedPubMedCentralGoogle Scholar
- Dumdei EJ, Flowers AE, Garson MJ, Moore CJ (1997) The biosynthesis of sesquiterpene isocyanides and isothiocyanates in the marine sponge Acanthella cavernosa (Dendy); evidence for dietary transfer to the dorid nudibranch Phyllidiella pustulosa. Comp Biochem Physiol A Physiol 118:1385–1392CrossRefGoogle Scholar
- Fahey SJ, Garson MJ (2002) Geographic variation of natural products of tropical nudibranch Asteronotus cespitosus. J Chem Ecol 28 (9):1773–1785. https://doi.org/10.1023/A:1020509117545
- Garrett A (1873) Descriptions of new species of marine shells inhabiting the South Sea islands. Proc Acad Nat Sci Phila 1873:209–231Google Scholar
- Giordano G, Carbone M, Ciavatta ML, Silvano E, Gavagnin M, Garson MJ, Cheney KL, Mudianta IW, Russo GF, Villani G, Magliozzi L, Polese G, Zidorn C, Cutignano A, Fontana A, Ghiselin MT, Mollo E (2017) Volatile secondary metabolites as olfactory signals and defensive weapons in aquatic environments. Proc Natl Acad Sci 114:3451–3456CrossRefPubMedPubMedCentralGoogle Scholar
- Heller C (1862). Neue Crustaceen, gesammelt während der Weltumseglung der k.k. Fregatte Novara. Zweiter vorläufiger Bericht. Verh Zool-Bot Ges Wien 12:519–528Google Scholar
- Karuso P (1987) Chemical ecology of the nudibranchs. In: Scheuer PJ (eds) Bioorganic marine chemistry. vol 1. Springer, Berlin, HeidelbergGoogle Scholar
- Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
- Keyzers RA, Northcote PT, Davies-Coleman MT (2006) Spongian diterpenoids from marine sponges. Nat Prod Rep 23:321−334Google Scholar
- Rogers SD, Paul, VJ (1991) Chemical defenses of three Glossodoris nudibranchs and their dietary Hyrtios sponges. Mar Ecol Prog Ser 77:221–232Google Scholar
- Rudman WB, Bergquist PR (2007) A review of feeding specificity in the sponge-feeding Chromodorididae (Nudibranchis: Mollusca). Molluscan Res 27:60–88Google Scholar
- Turner LM, Wilson NG (2008) Polyphyly across oceans: a molecular phylogeny of Chromodorididae (Mollusca, Nudibranchia). Zool Scr 37:23–42Google Scholar