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The Fate of Lyngbya majuscula Toxins in Three Potential Consumers

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Abstract

Blooms of Lyngbya majuscula have been reported with increasing frequency and severity in the last decade in Moreton Bay, Australia. A number of grazers have been observed feeding upon this toxic cyanobacterium. Differences in sequestration of toxic compounds from L. majuscula were investigated in two anaspideans, Stylocheilus striatus, Bursatella leachii, and the cephalaspidean Diniatys dentifer. Species fed a monospecific diet of L. majuscula had different toxin distribution in their tissues and excretions. A high concentration of lyngbyatoxin-a was observed in the body of S. striatus (3.94 mg/kg−1) compared to bodily secretions (ink 0.12 mg/kg−1; fecal matter 0.56 mg/kg−1; eggs 0.05 mg/kg−1). In contrast, B. leachii secreted greaterconcentrations of lyngbyatoxin-a (ink 5.41 mg/kg−1; fecal matter 6.71 mg/kg−1) than that stored in the body (2.24 mg/kg−1). The major internal repository of lyngbyatoxin-a and debromoaplysiatoxin was the digestive gland for both S. striatus (6.31 ± 0.31 mg/kg−1) and B. leachii (156.39 ± 46.92 mg/kg−1). D. dentifer showed high variability in the distribution of sequestered compounds. Lyngbyatoxin-a was detected in the digestive gland (3.56 ± 3.56 mg/kg−1) but not in the head and foot, while debromoaplysiatoxin was detected in the head and foot (133.73 ± 129.82 mg/kg−1) but not in the digestive gland. The concentrations of sequestered secondary metabolites in these animals did not correspond to the concentrations found in L. majuscula used as food for these experiments, suggesting it may have been from previous dietary exposure. Trophic transfer of debromoaplysiatoxin from L.majuscula into S. striatus is well established; however, a lack of knowledge exists for other grazers. The high levels of secondary metabolites observed in both the anaspidean and the cephalapsidean species suggest that these toxins may bioaccumulate through marine food chains.

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References

  • E. G. Abal W. C. Dennison P. F. Greenfield (2001) ArticleTitleManaging the Brisbane River and Moreton Bay: an integrated research/management program to reduce the impacts on an Australian estuary Water Sci. Technol. 43 57–70 Occurrence Handle1:CAS:528:DC%2BD3MXltFGktrs%3D

    CAS  Google Scholar 

  • C. Avila (1995) ArticleTitleNatural products of opisthobranch molluscs: A biological review Oceanogr. Mar. Biol. Ann. Rev. 33 487–559

    Google Scholar 

  • E. Cruz-Rivera V. J. Paul (2002) Coral reef benthic cyanobacteria as food and refuge: Diversity, chemistry and complex interactions Proceedings of the 9th International Coral Reef Symposium Bali Indonesia 515–520

    Google Scholar 

  • D. J. Faulkner (1984) ArticleTitleMarine natural products: Metabolites of marine algae and herbivorous marine molluscs Nat. Prod. Rep. 1 251–280 Occurrence Handle1:CAS:528:DyaL2cXmtVOhsLk%3D

    CAS  Google Scholar 

  • W. A. Gallimore D. L. Galario C. Lacy Y. Zhu P. J. Scheuer (2000) ArticleTitleTwo complex proline esters from the sea hare Stylocheilus longicauda J. Nat. Prod. 63 1022–1026 Occurrence Handle1:CAS:528:DC%2BD3cXjt1Git74%3D Occurrence Handle10924193

    CAS  PubMed  Google Scholar 

  • P. M. Johnson A. O. D. Willows (1999) ArticleTitleDefense in sea hares (Gastropoda, Opisthobranchia, Anaspidea): Multiple layers of protection from egg to adult Mar. Fresh. Behav. Physiol. 32 147–180

    Google Scholar 

  • Y. Kato P. J. Scheuer (1975) ArticleTitleAplysiatoxin and debromoaplysiatoxin, constituents of the marine mollusk Stylocheilus longicauda (Quoy and Gaimard, 1824) J. Am. Chem. Soc. 96 2245–2246

    Google Scholar 

  • Y. Kato P. J. Scheuer (1976) ArticleTitleThe aplysiatoxins. Reactions with acid and oxidants Pure Appl. Chem. 48 29–33 Occurrence Handle1:CAS:528:DyaE2sXhvV2kt74%3D

    CAS  Google Scholar 

  • E. F. Lowe R. L. Turner (1976) ArticleTitleAggregation and trail-following in juvenile Bursatella leachii pleii The Veliger 19 153–155

    Google Scholar 

  • D. G. Nagle V. J. Paul (1999) ArticleTitleProduction of secondary metabolites by filamentous tropical marine cyanobacteria: Ecological functions of the compounds J. Phycol. 35 1412–1421 Occurrence Handle1:CAS:528:DC%2BD3cXmvFynsQ%3D%3D

    CAS  Google Scholar 

  • D. G. Nagle F. T. Camacho V. J. Paul (1998) ArticleTitleDietary preferences of the opisthobranch mollusc Stylocheilus longicauda for secondary metabolites produced by the tropical cyanobacterium Lyngbya majuscula Mar. Biol. 132 267–273

    Google Scholar 

  • J. A. Paige (1988) ArticleTitleBiology, metamophosis and postlarval development of Bursatella leachii plei Rang (Gastropoda: Opistobranchia) Bull. Mar. Sci. 42 65–75

    Google Scholar 

  • V. J. Paul S. C. Pennings (1991) ArticleTitleDiet-derived chemical defenses in the sea hare Stylocheilus longicauda (Quoy et Gaimard 1824) J. Exp. Mar. Biol. Ecol. 151 227–243

    Google Scholar 

  • S. C. Pennings V. J. Paul (1993a) ArticleTitleSequestration of dietary secondary metabolites by three species of sea hares: Location, specificity and dynamics Mar. Biol. 117 535–546 Occurrence Handle1:CAS:528:DyaK2cXhtVamtro%3D

    CAS  Google Scholar 

  • S. C. Pennings V. J. Paul (1993b) ArticleTitleSecondary chemistry does not limit dietary range of the specialist sea hare Stylocheilus longicauda (Quoy et Gaimard 1824) J. Exp. Mar. Biol. Ecol. 174 97–113

    Google Scholar 

  • S. C. Pennings A. M. Weiss V. J. Paul (1996) ArticleTitleSecondary metabolites of the cyanobacterium Microcoleus lyngbyaceus and the sea hare Stylocheilus longicauda: Palatability and toxicity Mar. Biol. 126 735–743

    Google Scholar 

  • S. C. Pennings V. J. Paul D. C. Dunbar M. T. Hamann W. A. Lumbang B. Novack R. S. Jacobs (1999) ArticleTitleUnpalatable compounds in the marine gastropod Dolabella auricularia: Distribution and effect of diet J. Chem. Ecol. 25 735–755 Occurrence Handle1:CAS:528:DyaK1MXjtVOitL8%3D

    CAS  Google Scholar 

  • S. C. Pennings S. Nastisch V. J. Paul (2001) ArticleTitleVulnerability of sea hares to fish predators: Importance of diet and fish species Coral Reefs 20 320–324

    Google Scholar 

  • L. J. Ramos J. L. L. Rocafort M. W. Miller (1995) ArticleTitleBehavior patterns of the Aplysiid gastropod Bursatella leachii in its natural habitat and in the laboratory Neurobiol. Learn. Mem. 63 246–259 Occurrence Handle1:STN:280:ByqH3c%2FntFU%3D Occurrence Handle7670838

    CAS  PubMed  Google Scholar 

  • C. N. Rogers R. De Nys T. S. Charlton P. D. Steinberg (2000) ArticleTitleDynamics of algal secondary metabolites in two species of sea hare J. Chem. Ecol. 26 721–744 Occurrence Handle1:CAS:528:DC%2BD3cXit1Klu7g%3D

    CAS  Google Scholar 

  • Rudman, W. B. 1999. Stylocheilus longicauda and Stylocheilus citrina. Nomenclature discussion, [in] Sea Slug Forum. http://www.seaslugforum.net/factsheet.cfm?base=stylnome date accessed 23 May 2005.

  • M. Switzer-Dunlap M. G. Hadfield (1977) ArticleTitleObservations on developmental, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia) in laboratory culture J. Exp. Mar. Biol. Ecol. 29 245–261

    Google Scholar 

  • M. Watson M. D. Rayner (1973) ArticleTitleMidgut gland toxins of Hawaiian sea hares: II. A preliminary pharmacological study Toxicon 11 269–276 Occurrence Handle1:CAS:528:DyaE3sXktVWisbY%3D Occurrence Handle4721927

    CAS  PubMed  Google Scholar 

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Acknowledgments

This project has been supported by Centre for Marine Studies Morteon Bay Research Station Scholarship; South East Queensland Regional Water Quality Management Strategy (SEQRWQMS), Brisbane, Australia; and Graduate Research Student Travel Award, University of Queensland. The authors thank the following people for their help: Dr. Wayne Knibb and Daniel Willett for supply of Lyngbya-naïve S. striatus from Bribie Island Aquaculture Research Centre (BIARC); Dr. Clay Carlson for assistance in identification of D. dentifer; Mr. Geoff Eaglesham and Mr. Nick Osborne for help with toxicology work at National Research Centre for Environmental Toxicology (EnTox); Dr. Nazim Khan (University of Queensland) for help and guidance with statistics; Prof. Valerie Paul and Mr. Raphael Ritson-Williams for feedback and critique of the manuscript.

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Correspondence to Angela Capper.

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Capper, A., Tibbetts, I.R., O’Neil, J.M. et al. The Fate of Lyngbya majuscula Toxins in Three Potential Consumers. J Chem Ecol 31, 1595–1606 (2005). https://doi.org/10.1007/s10886-005-5800-5

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