Skip to main content
SpringerLink
Log in

Defense in the Aeolidoidean Genus Phyllodesmium (Gastropoda)

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The genus Phyllodesmium (Aeolidoidea, Gastropoda) comprises shell-less marine snails, whose defense strategies are not well investigated yet. Here we report results of the first chemical investigation of P. briareum, as well as a re-investigation of P. longicirrum and P. magnum. Briarane diterpenes were isolated from P. briareum, and their origin could be traced to its prey organism Briareum sp. (Octocorallia). Considerable enrichment of the soft coral secondary metabolites in the slug was shown. Re-investigation of P. magnum led to isolation of cembrane diterpenes, 2-phenylethylamide, and furano sesquiterpenes. Sequestration of chemicals seems to have influenced speciation and evolution of Phyllodesmium species. Structural similarity or dissimilarity of particular slug metabolites suggests a closer, or more distant relationship of the respective Phyllodesmium taxa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Affeld S, Kehraus S, Wägele H, König GM (2009) Dietary derived sesquiterpenes from Phyllodesmium lizardensis. J Nat Prod 72:298–300

    Article  CAS  PubMed  Google Scholar 

  • Bernstein J, Shmeuli U, Zadock E, Kashman Y, Néeman I (1974) Sarcophine, a new epoxy cembranolide from marine origin. Tetrahedron 30:2817–2824

    Article  CAS  Google Scholar 

  • Berrue F, Kerr RG (2009) Diterpenes from gorgonian corals. Nat Prod Rep 26:681–710

    Article  CAS  PubMed  Google Scholar 

  • Bishara A, Yeffet D, Sisso M, Shmul G, Scheyer M, Benayahu Y, Rudi A, Kashman Y (2008) Nardosinanols A-I and lemnafricanol, sesquiterpenes from several soft corals, Lemnalia sp., Paralemnalia clavata, Lemnalia africana, and Rhytisma fulvum fulvum. J Nat Prod 71:375–380

    Article  CAS  PubMed  Google Scholar 

  • Borges RM, Bessiere JM, Ranganathan Y (2013) Diet variation in fig volatiles across syconium development: making sense of scents. J Chem Ecol 39:630–642

    Article  CAS  PubMed  Google Scholar 

  • Bowden BF, Coll JC, de Silva ED, de Costa MSL, Djura PJ, Mahendran M, Tapiolas DM (1983) Studies of australian soft corals – XXXI. Novel furanosesquiterpenes from several sinularian soft corals (Coelenterata, Octocorallia, Alcyonacea). Aust J Chem 36:371–376

    Article  CAS  Google Scholar 

  • Breitmaier E (2005) Terpene. WILEY-VCH, Weinheim, p 23

    Book  Google Scholar 

  • Burghardt I, Evertsen JM, Johnsen G, Wägele H (2005) Solar powered seaslugs – mutualistic symbiosis of aeolid Nudibranchia (Mollusca, Gastropoda, Opisthobranchia) with Symbiodinium. Symbiosis 38:227–250

    Google Scholar 

  • Burghardt I, Gosliner TM (2006) Phyllodesmium rudmani (Mollusca: Nudibranchia: Aeolidoidea), a new solar powered species from the Indo-West Pacific with data on its symbiosis with zooxanthellae. Zootaxa 1308:31–47

  • Burghardt I, Schrödl M, Wägele H (2008a) Three new solar-powerd species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidoidea) from the tropical Indo-Pacific, with analysis of their photosynthetic activity and notes on biology. J Molluscan Stud 74:277–292

    Article  Google Scholar 

  • Burghardt I, Stemmer K, Wägele H (2008b) Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca: Gastropoda), with analysis of long-term retention. Org Divers Evol 8:66–76

    Article  Google Scholar 

  • Burghardt I, Wägele H (2004) A new solar powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidoidea) from Indonesia with analysis of its photosynthetic activity and notes on biology. Zootaxa 596:1–18

    Google Scholar 

  • Cardellina JH, James TR, Chen MHM, Clardy J (1984) Structure of Brianthein W, from the soft coral Briareum polyanthes. J Org Chem 49:3398–3399

    Article  CAS  Google Scholar 

  • Cattaneo-Vietti R, Angelini S, Bavestrello G (1993) Skin and gut spicules in Discodoris atromaculata (Bergh, 1880) (Mollusca: Nudibranchia). B Malacol 29:173–180

    Google Scholar 

  • Coll JC (1992) The chemistry and chemical ecology of Octocorals (Coelenterata, Anthozoa, Octocorallia). Chem Rev 92:613–631

    Article  CAS  Google Scholar 

  • Coll JC, Bowden BF, Tapiolas DM, Willis RH, Djura P, Streamer M, Trott L (1985) Studies on australian soft corals – XXXV; The terpenoid chemistry of soft corals and its implications. Tetrahedron 41:1065–1085

    Article  Google Scholar 

  • Duda TF, Kohn AJ (2005) Species-level phylogeography and evolutionary history of the hyperdiverse marine gastropod genus Conus. Mol Phylogenet Evol 34:257–272

    Article  PubMed  Google Scholar 

  • Edmunds MJ (1968) Eolid mollusca from Ghana, with further details of west atlantic species. Bull Mar Sci 18:203–219

    Google Scholar 

  • Edmunds MJ (1987) Color in Opisthobranchs. Am Malacol Bull 5:185–196

    Google Scholar 

  • Epifanio R de A, da Gama BAP, Pereira RC (2006) 11β,12β-Epoxypukalide as the antifouling agent from the Brazilian endemic sea fan Phyllogorgia dilatata Esper (Octocorallia, Gorgoniidae). Biochem Syst Ecol 34:446–448

  • Epifanio R de A, Martins DL, Villaca R, Gabriel R (1999) Chemical defenses against fish predation in three Brazilian octocorals: 11β,12β-epoxypukalide as a feeding deterrent in Phyllogorgia dilatata. J Chem Ecol 25:2255–2265

  • Grace KJS, Zavortink D, Jacobs RS (1994) Inactivation of bee venom phospholipase A2 by a sesquiterpene furanoic acid marine natural product. Biochem Pharmacol 47:1427–1434

    Article  CAS  PubMed  Google Scholar 

  • Greenwood PJ (2009) Acquisition and use of nematocysts by cnidarian predators. Toxicon 54:1065–1070

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grode SH, James TR, Cardellina JH, Onan KD (1983) Molecular structures of the Briantheins, new insecticidal diterpenes from Briareum polyanthes. J Org Chem 48:5203–5207

    Article  CAS  Google Scholar 

  • Guerriero A, Dambrosio M, Pietra F (1990) Isolation of the cembranoid preverecynarmin alongside some briaranes, the verecynarmins, from both the nudibranch mollusk Armina maculata and the octocoral Veretillum cynomorium of the east pyrenean mediterranean-sea. Helv Chim Acta 73:277–283

    Article  CAS  Google Scholar 

  • Hamm S, Bleton J, Connan J, Tchapla A (2005) A chemical investigation by headspace SPME and GC-MS of volatile and semi-volatile terpenes in various olibanum samples. Phytochemistry 66:1499–1514

    Article  CAS  PubMed  Google Scholar 

  • Hsieh PW, Chang FR, McPhail AT, Lee KH, Wu YC (2003) New cembranolide analogues from the formosan soft coral Sinularia flexibilis and their cytotoxicity. Nat Prod Res 17:409–418

    Article  CAS  PubMed  Google Scholar 

  • Iguchi K, Mori K, Suzuki M, Takahashi H, Ymada Y (1986) New marine furanosesquiterpenoids, Tubipofuran and 15-Acetoxytubipofuran from the Stolonifer Tubipora musica Linnaeus. Chem Lett 10:1789–1792

    Article  Google Scholar 

  • Izac RR, Fenical W, Tagle B, Clardy J (1981) Neolemnane and eremophilane sesquiterpenoids from the pacific soft coral Lemnalia africana. Tetrahedron 37:2569–2573

    Article  CAS  Google Scholar 

  • Jurek J, Scheuer PJ (1993) Sesquiterpenoids and norsesquiterpenoids from the soft coral Lemnalia africana. J Nat Prod 56:508–513

    Article  CAS  PubMed  Google Scholar 

  • Kamel HN, Slattery M (2005) Terpenoids of Sinularia: chemistry and biomedical applications. Pharm Biol 43:253–269

    Article  CAS  Google Scholar 

  • Kazlauskas R, Marwood JF, Wells RJ (1980) 2-Phenylethylamides of a novel lipid acid atrial stimulants from the soft coral Sinularia flexibilis. Aust J Chem 33:1799–1803

    Article  CAS  Google Scholar 

  • Kimland B, Norin T (1968) Thunbergol, a new macrocyclic diterpene alcohol. Acta Chem Scand 22:943–948

    Article  CAS  Google Scholar 

  • Kitagawa I, Kobayashi M, Cui Z, Kiyota Y, Ohnishi M (1986) Marine natural products. XV. Chemical constituents of an okinawan soft coral of Xenia sp. (Xeniidae). Chem Pharm Bull 34:4590–4596

    Article  CAS  Google Scholar 

  • Kobayashi M, Hirase T (1990) Marine terpenes and terpenoids. XI. Structures of new dihydrofuranocembranoids isolated from a Sarcophyton sp. soft coral of Okinawa. Himal Chem Pharm Bull 38:2442–2445

    Article  CAS  Google Scholar 

  • Kobayashi M, Nakagawa T, Mitsuhashi H (1979) Marine terpenes and terpenoids. I. Structures of four cembrane-type diterpenes; Sarcophytol-A, Sarcophytol-A Acetate, Sarcophytol-B, and Sarcophytonin-A from the soft coral Sarcophyton glaucum. Chem Pharm Bull 27:2382–2387

    Article  CAS  Google Scholar 

  • Ksebati MB, Ciereszko LS, Schmitz FJ (1984) 11β,12β-Epoxypukalide - a furanocembranolide from the Gorgonian Loeptogorgia setacea. J Nat Prod 47:1009–1012

    Article  CAS  PubMed  Google Scholar 

  • Li C, La MP, Tang H, Pan WH, Sun P, Krohn K, Yi YH, Li L, Zhang W (2012) Bioactive briarane diterpenoids from the South China Sea gorgonian Dichotella gemmacea. Bioorg Med Chem Lett 22:4368–4372

    Article  CAS  PubMed  Google Scholar 

  • Mao SC, Gavagnin M, Mollo E, Guo YW (2011) A new rare asteriscane sesquiterpene and other related derivatives from the Hainan aeolid nudibranch Phyllodesmium magnum. Biochem Syst Ecol 39:408–411

    Article  CAS  Google Scholar 

  • McFadden CS, France SC, Sanchez JA, Alderslade P (2006) A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol Phylogenet Evol 41:513–527

    Article  CAS  PubMed  Google Scholar 

  • Moore E, Gosliner TM (2009) Three new species of Phyllodesmium Ehrenberg (Gastropoda: Nudibranchia: Aeolidoidea), and a revised phylogenetic analysis. Zootaxa 2201:30–48

    Google Scholar 

  • Moore E, Gosliner TM (2011) Molecular phylogeny and evolution of symbiosis in a clade of Indopacific nudibranchs. Mol Phylogenet Evol 58:116–123

    Article  PubMed  Google Scholar 

  • Putz A, König GM, Wägele H (2009) Defensive Strategies of Cladobranchia (Gastropoda, Opisthobranchia). Nat Prod Rep 27:1386–1402

    Article  Google Scholar 

  • Qi SH, Zhang S, Qian PY, Xu HH (2009) Antifeedant and antifouling briaranes from the south china sea gorgonian Junceella juncea. Chem Nat Compd 45:49–54

    Article  CAS  Google Scholar 

  • Rudman WB (1991) Further studies on the taxonomy and biology of the octocoral-feeding genus Phyllodesmium Ehrenberg, 1831 (Nudibranchia: Aeolidoidea). J Molluscan Stud 57:167–203

    Article  Google Scholar 

  • Rudman WB (2002) Phyllodesmium sp., 5 [In] Sea Slug Forum. Australian Museum, Sydney, Available from http://www.seaslugforum.net/find/phyllodsp5

    Google Scholar 

  • Sheu JH, Sung PJ, Cheng MC, Liu HY, Fang LS, Duh CY, Chiang MY (1998) Novel cytotoxic diterpenes, Excavatolides A-E, isolated from the Formosan gorgonian Briareum excavatum. J Nat Prod 61:602–608

    Article  CAS  PubMed  Google Scholar 

  • Sheu JH, Sung PJ, Huang LH, Lee SF, Wu T, Chang BY, Duh CY, Fang LS, Soong K, Lee TJ (1996) New cytotoxic briaran diterpenes from the Formosan gorgonian Briareum sp. J Nat Prod 59:935–938

    Article  CAS  PubMed  Google Scholar 

  • Slattery M, Avila C, Starmer J, Paul VJ (1998) A sequestered soft coral diterpene in the aeolid nudibranch Phyllodesmium guamensis. J Exp Mar Biol Ecol 226:33–49

    Article  CAS  Google Scholar 

  • Slattery M, Starmer J, Paul VJ (2001) Temporal and spatial variation in defensive metabolites of the tropical Pacific soft corals Sinularia maxima and S. polydactyla. Mar Biol 138:1183–1193

    Article  CAS  Google Scholar 

  • Steinebrunner F, Twele R, Francke W, Leuchtmann A, Schiestl FP (2008) Role of odour compounds in the attraction of gamete vectors in endophytic Epichloë fungi. New Phytol 178:401–411

    Article  CAS  PubMed  Google Scholar 

  • Stemmer K, Burghardt I, Mayer C, Reinicke GB, Wägele H, Tollrian R, Leese F (2013) Morphological and genetic analysis of xeniid soft coral diversity (Octocorallia; Alcyonacea). Org Divers Evol 13:135–150

    Article  Google Scholar 

  • Sung PJ, Sheu JH, Xu JP (2002) Survey of briarane-type diterpenoids of marine origin. Heterocycles 57:535–579

    Article  CAS  Google Scholar 

  • Tursch B, Braekman JC, Daloze D, Fritz P, Kelecom A, Karlsson R, Losman D (1974) Chemical studies of marine invertebrates. VIII. Africanol, an unusual sesquiterpene from Lemnalia africana (Coelenterata, Octocorallia, Alcyonacea). Tetrahedron Lett 9:747–750

    Article  Google Scholar 

  • Uchio Y, Nitta M, Nakayama M, Iwagawa T, Hase T (1983) Ketoemblide and sarcophytolide, two new cembranolides with ε-lactone function from the soft coral Sarcophyta elegans. Chem Lett 4:613–616

    Article  Google Scholar 

  • Wägele H (2004) Potential key characters in Opisthobranchia (Gastropoda, Mollusca) enhancing adaptive radiation. Org Div Evol 4:175–188

    Article  Google Scholar 

  • Wägele H, Ballesteros M, Avila C (2006) Defensive glandular structures in opisthobranch molluscs – from histology to ecology. Oceanogr Mar Biol 44:197–276

    Google Scholar 

  • Wägele H, Klussmann-Kolb A (2005) Opisthobranchia (Mollusca, Gastropoda) - more than just slimy slugs. Shell reduction and its implications on defence and foraging. Front Zool 2:1–18

    Article  Google Scholar 

  • Wägele H, Raupach MJ, Burghardt I, Grzymbowski Y, Händeler K (2010) Solar powered seaslugs (Opisthobranchia, Gastropoda, Mollusca): incorporation of photosynthetic units: a key character enhancing radiation? In: Glaubrecht M (ed) Evolution in action. Springer, Berlin-Heidelberg, pp 263–282

    Chapter  Google Scholar 

  • Weinheimer AJ, Chang CWJ, Matson JA (1979) Naturally Occuring Cembranes. In: Herz W, Grisenbach H, Kirby GW (eds) Progress in the chemistry of organic natural products, vol 36, Springer-Verlag, Wien., pp 285–387

    Google Scholar 

  • Wessels M, König GM, Wright AD (2000) New natural product isolation and comparison of the secondary metabolite content of three distinct samples of the sea hare Aplysia dactyomela from Tenerife. J Nat Prod 63:920–928

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank Dana Obermann, who detected the single specimen of Phyllodesmium magnum in the aquaristic shop in Bonn and brought it to us for further analysis. We thank the German Science Foundation for support to two authors: HW (Wa618/10-1) and GK (Ko 902/8-1).

Author information

Authors and Affiliations

  1. Institute for Pharmaceutical Biology, University of Bonn, Nussallee 6, 53115, Bonn, Germany

    Alexander Bogdanov, Stefan Kehraus & Gabriele M. König

  2. Faculty of Mathematics and Natural Sciences, University of Wuppertal, Gaußstraße 20, 42097, Wuppertal, Germany

    Sabrina Bleidissel & Gela Preisfeld

  3. Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany

    Dorothee Schillo & Heike Wägele

  4. Institute of Microbiology, Eidgenoessische Technische Hochschule (ETH) Zurich, Wolfgang-Pauli-Straße 10, 8083, Zurich, Switzerland

    Jörn Piel & Alexander O. Brachmann

Authors
  1. Alexander Bogdanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Kehraus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sabrina Bleidissel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gela Preisfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dorothee Schillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jörn Piel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alexander O. Brachmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Heike Wägele
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gabriele M. König
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriele M. König.

Electronic supplementary material

Supporting Information Available. Spectroscopic data and other relevant information are included for compounds 1–8.

ESM 1

(DOC 4836 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bogdanov, A., Kehraus, S., Bleidissel, S. et al. Defense in the Aeolidoidean Genus Phyllodesmium (Gastropoda). J Chem Ecol 40, 1013–1024 (2014). https://doi.org/10.1007/s10886-014-0496-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-014-0496-z

Keywords

Search

Navigation