Skip to main content
SpringerLink
Log in

Secondary metabolites of the cyanobacterium Microcoleus lyngbyaceus and the sea hare Stylocheilus longicauda: palatability and toxicity

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The cyanobacterium Microcoleus lyngbyaceus (Kütz.) Crouan (Lyngbya majuscula Gomont) produces a variety of nitrogen-containing secondary metabolites. M. lyngbyaceus is eaten by the specialist sea hare Stylocheilus longicauda, which sequesters secondary metabolites from its diet and transforms some sequestered metabolites into related compounds. We examined the palatability and toxicity of the metabolites malyngamide A, malyngamide B, and a mixture of majusculamides A and B (from M. lyngbyaceus), and malyngamide B acetate (from S. longicauda, derived from malyngamide B), in order to explore a series of hypotheses about why M. lyngbyaceus produces secondary metabolites and why S. longicauda sequesters and transforms them. All three M. lyngbyaceus metabolites significantly reduced feeding by omnivorous pufferfish (Canthigaster solandri) and crabs (Leptodius spp.). Direct comparisons indicated that neither malyngamide A nor the majusculamide mixture differed significantly in palatability from malyngamide B. The S. longicauda metabolite malyngamide B acetate did not significantly deter feeding by either consumer. Direct comparisons indicated that pufferfish found malyngamide B acetate more palatable than malyngamide B, and that crabs showed a non-significant trend in this direction. Palatability of the metabolites did not correlate with toxicity. Although no significant differences were observed among the M. lyngbyaceus metabolites in their palatability, two toxicity assays consistently ranked malyngamide A more toxic than malyngamide B, which was more toxic than the majusculamide mixture. The majusculamide mixture did not significantly differ in toxicity from malyngamide B acetate, even though the two differed strongly in palatability.

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

Similar content being viewed by others

References

  • Arakaki Y, Uehara T (1991) Physiological adaptations and reproduction of the four types of Echinometra mathaei (Blainville). In: Janagisawa T, Yasumasu I, Oguro C, Suzuki N, Motokawa T (eds) Biology of Echinodermata. A.A. Balkema, Rotterdam, pp 105–112

    Google Scholar 

  • Avila C (1995) Natural products from opisthobranch molluscs: a biological review. Oceanogr mar Biol A Rev 33: 487–559

    Google Scholar 

  • Cardellina II JH, Marner F-J, Moore RE (1979a) Seaweed dermatitis: structure of lyngbyatoxin A. Science, NY 204: 193–195

    Google Scholar 

  • Cardellina II JH, Marner F-J, Moore RE (1979b) Malyngamide A, a novel chlorinated metabolite of the marine cyanophyte Lyngbya majuscula. J Am chem Soc 101: 240–241

    Google Scholar 

  • Carefoot TH (1987) Aplysia: its biology and ecology. Oceanogr mar Biol A Rev 25: 167–241

    Google Scholar 

  • Faulkner DJ (1992) Chemical defenses of marine molluscs. In: Paul VJ (ed) Ecological roles of marine natural products. Comstock, Ithaca, pp 119–163

    Google Scholar 

  • Faulkner DJ, Ghiselin MT (1983) Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Mar Ecol Prog Ser 13: 295–301

    Google Scholar 

  • Gerwick WH, Proteau PJ, Nagle DG, Hamel E, Blokhin A, Slate DL (1994) Structure of curacin A, a novel antimitotic, antiproliferative, and brine shrimp toxic natural product from the marine cyanobacterium Lyngbya majuscula. J org Chem 59: 1243–1245

    Google Scholar 

  • Hay ME, Fenical W, Gustafson K (1987) Chemical defense against diverse coral-reef herbivores. Ecology 68: 1581–1591

    Google Scholar 

  • Humm HJ, Wicks SR (1980) Introduction and guide to the marine bluegreen algae. John Wiley & Sons, New York

    Google Scholar 

  • Ireland C, Stallard MO, Faulkner DJ, Finer J, Clardy J (1976) Some chemical constituents of the digestive gland of the sea hare Aplysia californica. J org Chem 41: 2461–2465

    Google Scholar 

  • Kato Y, Scheuer PJ (1974) Aplysiatoxin and debromoaplysiatoxin, constituents of the marine mollusk Stylocheilus longicauda (Quoy and Gaimard, 1824). J Am chem Soc 96: 2245–2246

    Google Scholar 

  • Kato Y, Scheuer PJ (1975) The aplysiatoxins. Pure appl Chem 41: 1–14

    Google Scholar 

  • Koehn FE, Longley RE, Reed JK (1992) Microcolins A and B, new immunosuppressive peptides from the blue-green alga Lyngbya majuscula. J nat Products 56: 613–619

    Google Scholar 

  • La Barre SC, Coll JC, Sammarco PW (1986) Defensive strategies of soft corals (Coelenterata: Octocorallia) of the Great Barrier Reef. II. The relationship between toxicity and feeding deterrence. Biol Bull mar biol Lab, Woods Hole 171: 565–576

    Google Scholar 

  • Marner FJ, Moore RE, Hirotsu K, Clardy J (1977) Majusculamides A and B, two epimeric lipodipeptides from Lyngbya majuscula Gomont. J org Chem 42: 2815–2819

    Google Scholar 

  • Moore RE (1981) Constituents of blue-green algae. In: Scheuer PJ (ed) Marine natural products. Vol. 4. Academic Press, New York, pp 1–52

    Google Scholar 

  • Moore RE, Blackman AJ, Cheuk CE, Mynderse JS, Matsumoto GK, Clardy J, Woodard RW, Craig JC (1984) Absolute stereochemistries of the aplysiatoxins and oscillatoxin A. J org Chem 49: 2484–2489

    Google Scholar 

  • Myers RF (1989) Micronesian reef fishes. Coral Graphics, Guam

    Google Scholar 

  • Mynderse JS, Moore RE, Kashgawi M, Norton TR (1977) Antileukemia activity in the Oscillatoriaceae: isolation of debromoaplysiatoxin from Lyngbya. Science, NY 196: 538–539

    Google Scholar 

  • Nys R de, Steinberg PD, Rogers CN, Charlton TS, Duncan MW (1996) Quantitative variation of secondary metabolites in the sea hare Aplysia parvula and its host plant, Delisea pulchra. Mar Ecol Prog Ser 130: 135–146

    Google Scholar 

  • Paul VJ (1992) Ecological roles of marine natural products. Comstock Publishing Associates, Ithaca

    Google Scholar 

  • Paul VJ, Meyer KD, Nelson SG, Sanger HR (1993) Deterrent effects of seaweed extracts and secondary metabolites on feeding by the rabbitfish Siganus spinus. Proc 7th int coral Reef Symp 2: 867–874 [Richmond RH (ed) University of Guam, Mangilao, Guam]

    Google Scholar 

  • Paul VJ, Nelson SG, Sanger HR (1990) Feeding preferences of adult and juvenile rabbitfish Siganus argenteus in relation to chemical defenses of tropical seaweeds. Mar Ecol Prog Ser 60: 23–34

    Google Scholar 

  • Paul VJ, Pennings SC (1991) Diet-derived chemical defenses in the sea hare Stylocheilus longicauda (Quoy et Gaimard 1824). J exp mar Biol Ecol 151: 227–243

    Google Scholar 

  • Paul VJ, Wylie CR, Sanger HR (1989) Effects of algal chemical defenses toward different coral-reef herbivorous fishes. Proc 6th int coral Reef Symp 3: 73–78 [Choat JH et al. (eds) Sixth International Coral Reef Symposium Executive Committee, Townsville]

  • Pawlik J (1993) Marine invertebrate chemical defenses. Chem Rev 93: 1911–1922

    Google Scholar 

  • Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar Ecol Prog Ser 127: 183–194

    Google Scholar 

  • Pennings SC (1990) Multiple factors promoting narrow host range in the sea hare, Aplysia calfornica. Oecologia 82: 192–200

    Google Scholar 

  • Pennings SC (1994) Interspecific variation in chemical defenses in the sea hares (Opithobranchia: Anaspidea). J exp mar Biol Ecol 180: 203–219

    Google Scholar 

  • Pennings SC, Carefoot TH (1995) Post-ingestive consequences of consuming secondary metabolites in sea hares (Gastropoda: Opisthobranchia). Comp Biochem Physiol 111C: 249–256

    Google Scholar 

  • Pennings SC, Paul VJ (1993a) Secondary chemistry does not limit the dietary range of the specialist sea hare Stylocheilus longicauda (Quoy et Gaimard, 1824). J exp mar Biol Ecol 174: 97–113

    Google Scholar 

  • Pennings SC, Paul VJ (1993b) Sequestration of dietary secondary metabolites by three species of sea hares: location, specificity and dynamics. Mar Biol 117: 535–546

    Google Scholar 

  • Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80: 82–86

    Google Scholar 

  • Pettit GR, Herald CL, Allen MS, VonDreele RB, Vanelle LD, Kao JPY, Blake W (1977) The isolation and structure of aplysistatin. J Am chem Soc 99: 262–263

    Google Scholar 

  • Rogers CN, Steinberg PD, de Nys R (1995) Factors associated with oligophagy in two species of sea hares (Mollusca: Anaspidea). J exp mar Biol Ecol 192: 47–73

    Google Scholar 

  • Sammarco PW, Coll JC (1992) Chemical adaptations in the Octocorallia: evolutionary considerations. Mar Ecol Prog Ser 88: 93–104

    Google Scholar 

  • Schmitt TM, Hay ME, Lindquist N (1995) Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76: 107–123

    Google Scholar 

  • Schulte BA, Bakus GJ (1992) Predation deterrence in marine sponges: laboratory versus field studies. Bull mar Sci 50: 205–211

    Google Scholar 

  • Stallard MO, Faulkner DJ (1974a) Chemical constituents of the digestive gland of the sea hare Aphysia californica. I. Importance of diets. Comp Biochem Physiol 49B: 25–35

    Google Scholar 

  • Stallard MO, Faulkner DJ (1974b) Chemical constituents of the digestive gland of the sea hare Aplysia californica. II. Chemical transformations. Comp Biochem Physiol 49B: 37–41

    Google Scholar 

  • Todd JS, Gerwick WH (1996) Malyngamide I from the tropical marine cyanobacterium Lyngbya majuscula and the probable structure revision of stylocheilamide. Tetrahedron Lett (in press)

  • Wylie CR, Paul VJ (1988) Feeding preferences of the surgeonfish Zebrasoma flavescens in relation to chemical defenses of tropical algae. Mar Ecol Prog Ser 45: 23–32

    Google Scholar 

Download references

Author information

Author notes

  1. S. C. Pennings

    Present address: Marine Institute, University of Georgia, Sapelo Island, 31327, Georgia, USA

  2. A. M. Weiss

    Present address: , 377 Nautilus Street, 92037, La Jolla, California, USA

Authors and Affiliations

  1. Marine Laboratory, University of Guam, 96923, Mangilao, Guam, USA

    S. C. Pennings, A. M. Weiss & V. J. Paul

Authors
  1. S. C. Pennings
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. M. Weiss
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. J. Paul
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by N. H. Marcus, Tallahassee

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pennings, S.C., Weiss, A.M. & Paul, V.J. Secondary metabolites of the cyanobacterium Microcoleus lyngbyaceus and the sea hare Stylocheilus longicauda: palatability and toxicity. Marine Biology 126, 735–743 (1996). https://doi.org/10.1007/BF00351340

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00351340

Keywords

Search

Navigation