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Journal of Chemical Ecology

, Volume 33, Issue 3, pp 643–654 | Cite as

The Role of Vanadium in the Chemical Defense of the Solitary Tunicate, Phallusia nigra

  • Shobu Odate
  • Joseph R. Pawlik
Article

Abstract

Ascidians (sea squirts) may defend themselves from predators, biofouling competitors, and bacterial infection by producing secondary metabolites or sequestering acid, but many species also accumulate heavy metals, most notably vanadium. The defensive functions of heavy metals in ascidians remain unclear, and to this end, the solitary Caribbean tunicate, Phallusia nigra, was studied to localize vanadium in its tissues and to assess the defensive properties of vanadium-containing compounds. As determined by flame atomic absorption spectroscopy, the internal tissues and blood contained the highest vanadium concentrations (mean values of 2,280 and 1,886 ppm dry mass, respectively), followed by the tunic surface (871 ppm dry mass). Results of laboratory feeding assays with the bluehead wrasse, Thalassoma bifasciatum, confirmed outcomes of past studies that demonstrated that vanadyl sulfate (VOSO4·6H2O) and sodium vanadate (Na3VO4) were unpalatable to fish, although these salts do not accurately reflect the chelation environment or oxidation state of vanadium in living tunicates. Fresh preparations of whole tunic, internal tissues, and blood were unpalatable to fish, but freezing and thawing of internal tissues and blood rendered them palatable. Crude organic extracts of whole tunic and internal tissues contained vanadium metabolites (225 and 750 ppm dry mass, respectively) and were palatable to T. bifasciatum; crude extracts also exhibited no antimicrobial effects against a panel of four marine bacteria known to be pathogens of marine invertebrates (Vibrio parahaemolyticus, Vibrio harveyi, Leucothrix mucor, and Deleya marina). Nonacidic vanadium (+3) complexes neither deterred predation nor inhibited microbial growth, whereas acidic aqua vanadium (+3 and +4) complexes were unpalatable to T. bifasciatum and exhibited antimicrobial activity. Difficulties in decoupling low pH from oxidation state and chelation environment of vanadium prevent definitive conclusions about the importance of some vanadium metabolites, but low pH appears to be the principal agent of chemical defense for P. nigra.

Keywords

Tunicate Ascidian Predation Chemical defense Heavy metals pH Vanadium Acid 

Notes

Acknowledgments

This research was funded by grants from the NOAA/NURC Program (NOAA-NA96RU-0260), from the National Science Foundation Biological Oceanography Program (OCE-0095724, 0550468), and by a GlaxoWellcome Ocean and Human Health Fellowship. We thank Robert D. Hancock, Richard M. Dillaman, Richard D. Lancaster, Stephen A. Skrabal, and S. Bart Jones for advice and technical support.

References

  1. Brand, S. G., Hawkins, C. J., Marshall, A. T., Nette, G. W., and Parry, D. L. 1989. Vanadium chemistry of ascidians. Comp. Biochem. Physiol. 93B(2):425–436.Google Scholar
  2. Bruening, R. C., Oltz, E. M., Furukawa, J., and Nakanishi, K. 1985. Isolation of tunichrome B-1, a reducing blood pigment of the sea squirt, Ascidia nigra. J. Nat. Prod. 49(2):193–204.CrossRefGoogle Scholar
  3. Ciereszko, L. S., Ciereszko, E. M., Harris, E. R., and Lane, C. A. 1963. Vanadium content of some tunicates. Comp. Biochem. Physiol. 8:137–140.CrossRefGoogle Scholar
  4. Cooper, S. R., Koh, Y. B., and Raymond, K. N. 1982. Synthetic, structural, and physical studies of bis(triethylammonium) tris(catecholato) vanadate(IV), potassium bis(catecholato) oxovanadate(IV), and potassium tris(catecholato) vanadate(III). J. Am. Chem. Soc. 104:5092–5102.CrossRefGoogle Scholar
  5. Davis, A. R. and Wright, A. E. 1989. Interspecific differences in fouling of two congeneric ascidians (Eudistoma olivaceum and E. capsulatum): is surface acidity an effective defense? Mar. Biol. 102:491–497.CrossRefGoogle Scholar
  6. Dingley, A. L., Kustin, K., Macara, I. G., McLeod, G. C., and Roberts, M. F. 1982. Vanadium-containing tunicate blood cells are not highly acidic. Biochim. Biophys. Acta 720:384–389.PubMedCrossRefGoogle Scholar
  7. Dworjanyn, S. A., De Nys, R., and Steinberg, P. D. 1999. Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra. Mar. Biol. 102:491–497.Google Scholar
  8. Frank, P., Carlson, R. M. K., Carlson, E. J., and Hodgson, K. O. 2003. Medium-dependence of vanadium K-edge X-ray absorption spectra with application to blood cells from phlebobranch tunicates. Coord. Chem. Rev. 237(1–2):31–39.CrossRefGoogle Scholar
  9. Goodbody, I. 1962. A biology of Ascidia nigra (Savigny). I. Survival and mortality in an adult population. Biol. Bull. 122:40–51.CrossRefGoogle Scholar
  10. Hernández-Zanuy, A. C. and Carballo, J. L. 2001. Distribution and abundance of ascidian assemblages in Caribbean reef zones of the Golfo de Batabanó (Cuba). Coral Reefs 20:159–162.CrossRefGoogle Scholar
  11. Hirose, E. 1999. Pigmentation and acid storage in the tunic: protective functions of the tunic cells in the tropical ascidian Phallusia nigra. Invertebr. Biol. 118(4):414–422.CrossRefGoogle Scholar
  12. Hirose, E., Yamashiro, H., and Mori, Y. 2001. Properties of tunic acid in the ascidian Phallusia nigra (Ascidiidae, Phlebobranchia). Zool. Sci. 18:309–314.CrossRefGoogle Scholar
  13. Kelly, S. R., Jensen, P. R., Henkel, T. P., Fenical, W., and Pawlik, J. R. 2003. Effects of Caribbean sponge extracts on bacterial attachment. Aquat. Microb. Ecol. 31:175–182.Google Scholar
  14. Kustin, K., Levine, D. S., McLeod, G. C., and Curby, W. A. 1976. The blood of Ascidia nigra: blood cell frequency distribution, morphology, and the distribution and valence of vanadium in living blood cells. Biol. Bull. 150:426–441.CrossRefGoogle Scholar
  15. Lambert, G. and Lambert, C. C. 1987. Spicule formation in the solitary ascidian, Herdmania momus. J. Morph. 192:145–159.CrossRefGoogle Scholar
  16. López-Legentil, S., Turon, X., and Schupp, P. 2006. Chemical and physical defenses against predators in Cystodytes (Ascidiacea). J. Exp. Mar. Biol. Ecol. 332(1):27–36.CrossRefGoogle Scholar
  17. Lindquist, N., Hay, M. E., and Fenical, W. 1992. Defense of ascidians and their conspicuous larvae: adult vs. larval chemical defenses. Ecol. Monogr. 62(4):547–568.CrossRefGoogle Scholar
  18. Michibata, H., Yamaguchi, N., Uyama, T., and Ueki, T. 2003. Molecular approaches to the accumulation and reduction of vanadium by ascidians. Coord. Chem. Rev. 237:41–51.CrossRefGoogle Scholar
  19. Newbold, R. W., Jensen, P. R., Fenical, W., and Pawlik, J. R. 1999. Antimicrobial activity of Caribbean sponge extracts. Aquat. Microb. Ecol. 19:279–284.Google Scholar
  20. Parry, D. L. 1984. Chemical properties of the test of ascidians in relation to predation. Mar. Ecol. Prog. Ser. 17:279–282.Google Scholar
  21. Pawlik, J. R. 1993. Marine invertebrate chemical defenses. Chem. Rev. 93:1911–1922.CrossRefGoogle Scholar
  22. Pawlik, J. R., Chanas, B., Toonen, R. J., and Fenical, W. 1995. Defenses of Caribbean sponges against predatory reef fish: I. Chemical deterrency. Mar. Ecol. Prog. Ser. 127:183–194.Google Scholar
  23. Pisut, D. P. and Pawlik, J. R. 2002. Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids? J. Exp. Mar. Biol. Ecol. 207:203–214.CrossRefGoogle Scholar
  24. Rehder, D. 1999. The coordination chemistry of vanadium as related to its biological functions. Coord. Chem. Rev. 182:297–322.CrossRefGoogle Scholar
  25. Selbin, J. 1966. Oxovanadium(IV) complexes. Coord. Chem. Rev. 1(3):293–314.CrossRefGoogle Scholar
  26. Sahade, R., Tatian, M., Kowalke, J., Kuehne, S., and Esnal, G. B. 1998. Benthic faunal association of soft substrates at Potter Cove, King George Island, Antarctica. Polar Biol. 19(2):85–91.CrossRefGoogle Scholar
  27. Stoecker, D. 1978. Resistance of a tunicate to fouling. Biol. Bull. 155:615–626.CrossRefGoogle Scholar
  28. Stoecker, D. 1980a. Relationships between chemical defense and ecology in benthic ascidians. Mar. Ecol. Prog. Ser. 3:257–265.Google Scholar
  29. Stoecker, D. 1980b. Chemical defenses of ascidians against predators. Ecology 61(6):1327–1334.CrossRefGoogle Scholar
  30. Swinehart, J. H., Biggs, W. R., Halko, D. J., and Schroeder, N. C. 1974. The vanadium and selected metal contents of some ascidians. Biol. Bull. 146:302–312.PubMedCrossRefGoogle Scholar
  31. Tarjuelo, I., López-Legentil, S., Codina, M., and Turon, X. 2002. Defence mechanisms of adults and larvae of marine invertebrates: patterns of toxicity and palatability in colonial ascidians. Mar. Ecol. Prog. Ser. 235:103–115.Google Scholar
  32. Thompson, T. E. 1960. Defensive acid-secretion in marine gastropods. J. Mar. Biol. Assoc. U.K. 39:499–517.Google Scholar
  33. Van Alstyne, K. L., McCarthy, J. J., Hustead, C. L., and Kearns, L. J. 1999. Phlorotannin allocation among tissues of Northeastern Pacific kelps and rockweeds. J. Phycol. 35:483–492.CrossRefGoogle Scholar
  34. Wahl, M., Jensen, P. R., and Fenical, W. 1994. Chemical control of bacterial epibiosis on ascidians. Mar. Ecol. Prog. Ser. 110:45–57.Google Scholar
  35. Webb, D. A. 1939. Observations on the blood of certain ascidians, with special reference to the biochemistry of vanadium. J. Exp. Biol. 16:499–523.Google Scholar
  36. Zangerl, A. R. and Rutledge, C. E. 1996. The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. Am. Nat. 147:599–607.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of Biology and Marine Biology Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA

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