Journal of Chemical Ecology

, Volume 32, Issue 5, pp 993–1004

UV-Induced Mortality in Encapsulated Intertidal Embryos: Are Mycosporine-Like Amino Acids an Effective Sunscreen?



Mycosporine-like amino acids (MAAs) are believed to protect a variety of marine organisms against the negative effects of ultraviolet radiation (UVR). However, their role in protecting developing intertidal encapsulated embryos remains untested. In the present study, we focused on the UV protective role of natural concentrations of MAAs for two intertidal gastropod species, Bembicium nanum and Siphonaria denticulata, which lay egg masses in habitats exposed to direct sunlight. We predicted that in both species, a higher concentration of MAAs within the egg mass would increase the likelihood of embryonic survivorship in the presence of UVR. Egg masses from both species were collected along the rocky shores of southeastern New South Wales, and a portion from each was subjected to one of three separate spectral treatments: full spectrum, UV-B block, and UV block. Proportions of surviving embryos were recorded following 72 hr exposure to spectral treatment. In addition, MAAs in each egg mass were quantified. Levels of variation in MAA concentration were striking, with S. denticulata egg masses showing more intraspecific variation than those of B. nanum. Surprisingly, survivorship under all spectral treatments was extremely high for both species, irrespective of MAA concentration. Under full spectrum treatments, B. nanum survivorship and total MAA concentration were significantly and positively correlated; however, MAA accounted for just 23.6% (R = 0.486) of the variation in survivorship. In contrast, survivorship in S. denticulata was not correlated with MAA concentration under full spectrum light. We conclude that the dependence on MAAs as photoprotection may be species-specific; however, it is likely that both species possess alternative mechanisms that minimize the negative effects of UVR.

Key words

Mycosporine-like amino acids UV-B Ultraviolet radiation Egg mass Gastropod Embryonic survivorship Intertidal MAAs 


  1. Adams, N. L. and Shick, J. M. 1996. Myscosporine-like amino acids provide protection against ultraviolet radiation in eggs of the green sea urchin Strongylocentrotus droebachiensis. Photochem. Photobiol. 64:149–158.CrossRefGoogle Scholar
  2. Adams, N. L. and Shick, J. M. 2001. Mycosporine-like amino acids prevent UVB-induced abnormalities during early development of the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 138:267–280.CrossRefGoogle Scholar
  3. Adams, N. L., Shick, J. M., and Dunlap, W. C. 2001. Selective accumulation of mycosporine-like amino acids in ovaries of the green sea urchin Strongylocentrotus droebachiensis is not affected by ultraviolet radiation. Mar. Biol. 138:281–294.CrossRefGoogle Scholar
  4. Baker, K. S., Smith, R. C., and Green, E. S. 1980. Middle ultraviolet reaching the ocean surface. Photochem. Photobiol. 32:367–374.CrossRefGoogle Scholar
  5. Belden, L. K. and Blaustein, A. 2002. Population differences in sensitivity to UV-B radiation for larval long-toed salamanders. Ecology 83:1586–1590.CrossRefGoogle Scholar
  6. Benkendorff, K. and Davis, A. R. 2004. Gastropod egg mass deposition on a temperate, wave-exposed coastline in New South Wales, Australia: Implications for intertidal conservation. Aquat. Conserv. 14:263–280.CrossRefGoogle Scholar
  7. Bentley, R. 1990. The shikimate pathway: A metabolic tree with many branches. Crit. Rev. Biochem. Mol. Biol. 25:307–384.PubMedCrossRefGoogle Scholar
  8. Biermann, C., Schinner, G., and Strathmann, R. 1992. Influence of solar radiation, microalgal fouling, and current on deposition site and survival of embryos of a dorid nudibranch gastropod. Mar. Ecol., Prog. Ser. 86:205–215.CrossRefGoogle Scholar
  9. Bjorn, L. O. 1999. Ultraviolet radiation, the ozone layer and ozone depletion, pp. 21–37, in J. Rozema (ed.). Stratospheric Ozone Depletion: The Effects of Enhanced UV-B Radiation on Terrestrial Ecosystems. Backhuys, Leiden.Google Scholar
  10. Booth, C. R. and Morrow, J. J. 1997. The penetration of UV into natural waters. Photochem. Photobiol. 65:254–275.CrossRefGoogle Scholar
  11. Carlini, D. B. and Regan, J. D. 1995. Photolyase activities of Elysia tuca, Bursatella leachii, and Haminaea antillarum (Mollusca: Opisthobranchia). J. Exp. Mar. Biol. Ecol. 189:219–232.CrossRefGoogle Scholar
  12. Chatterjee, S. and Price, B. 1977. Regression Analysis by Example. Wiley, New York.Google Scholar
  13. Cockell, C. S. and Knowland, J. 1999. Ultraviolet radiation screening compounds. Biol. Rev. 74:311–345.CrossRefPubMedGoogle Scholar
  14. Dunlap, W. C. and Chalker, B. E. 1986. Identification and quantitation of near-UV absorbing compounds (S-320) in a hermatypic scleractinian. Coral Reefs 5:155–159.CrossRefGoogle Scholar
  15. Dunlap, W. C. and Yamamoto, Y. 1995. Small-molecule antioxidants in marine organisms: Antioxidant activity of mycosporine–glycine. Comp. Biochem. Physiol., Part B Biochem. Mol. Biol. 112:105–114.CrossRefGoogle Scholar
  16. Franklin, L., Yakovleva, I., Karsten, U., and Luning, K. 1999. Synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae) and the consequences for sensitivity to ultraviolet B radiation. J. Phycol. 35:682–693.CrossRefGoogle Scholar
  17. Garcia-Pichel, F. and Castenholz, R. W. 1993. Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolated and an estimate of their screening capacity. Appl. Environ. Microbiol. 59:163–169.PubMedGoogle Scholar
  18. Gleason, D. F. and Wellington, G. M. 1995. Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Mar. Biol. 123:693–703.CrossRefGoogle Scholar
  19. Haeder, D. P., Kumar, H. D., Smith, R. C., and Worrest, R. C. 1998. Effects on aquatic ecosystems. J. Photochem. Photobiol. 46:53–68.CrossRefGoogle Scholar
  20. Helbling, E. W., Menchi, C. F., and Villafane, V. 2002. Bioaccumulation and role of UV-absorbing compounds in two marine crustacean species from Patagonia, Argentina. Photochem. Photobiol. Sci. 1:820–825.CrossRefPubMedGoogle Scholar
  21. Jeffrey, S. W., Mactavish, H. S., Dunlap, W. C., Vesk, M., and Groenewoud, K. 1999. Occurrence of UVA- and UVB-absorbing compounds in 152 species (206 strains) of marine macroalgae. Mar. Ecol., Prog. Ser. 189:35–51.CrossRefGoogle Scholar
  22. Karentz, D. 2001. Chemical defenses of marine organisms against solar radiation exposure: UV-absorbing mycosporine-like amino acids and scytonemin, pp. 481–520, in J. McClintock and B. Baker (eds.). Marine Chemical Ecology. CRC Press, Boca Raton, FL.Google Scholar
  23. Karentz, D., Mceuen, F. S., Land, M. C., and Dunlap, W. C. 1991. Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: Potential protection from ultraviolet exposure. Mar. Biol. 108:157–166.CrossRefGoogle Scholar
  24. Karsten, U., Sawall, T., and Wiencke, C. 1998. A survey of the distribution of UV-absorbing substances in tropical macroalgae. Phycol. Res. 46:271–279.CrossRefGoogle Scholar
  25. Macfadyen, E. J., Williamson, C. E., Grad, G., Lowery, M., Jeffrey, W. H., and Mitchell, D. L. 2004. Molecular response to climate change: Temperature dependence of UV-induced DNA damage and repair in the freshwater crustacean Daphnia pulicaria. Glob. Chang. Biol. 10:408–416.CrossRefGoogle Scholar
  26. Paul, N. D. and Gwynn-Jones, D. 2003. Ecological roles of solar UV radiation: Towards an integrated approach. Trends Ecol. Evol. 18:48–55.CrossRefGoogle Scholar
  27. Platt, U. 2000. Reactive halogen species in the mid-latitude troposphere: Recent discoveries. Water, Air, and Soil 123:229–244.CrossRefGoogle Scholar
  28. Prota, G. 1988. Progress in the chemistry of melanins and related metabolites. Med. Res. Rev. 8:525–556.PubMedCrossRefGoogle Scholar
  29. Przeslawski, R. 2004. A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses. Molluscan Res. 24:43–63.CrossRefGoogle Scholar
  30. Przeslawski, R. 2005. Combined effects of solar radiation and desication on the mortality and development of encapsulated embryos of rocky shore gastropods. Mar. Ecol., Prog. Ser. 298:169–177.CrossRefGoogle Scholar
  31. Przeslawski, R., Davis, A. R., and Benkendorff, K. 2004. Effects of ultraviolet radiation and visible light on the development of encapsulated molluscan embryos. Mar. Ecol., Prog. Ser. 268:151–160.CrossRefGoogle Scholar
  32. Przeslawski, R., Benkendorff, K., and Davis, A. R. 2005a. A quantitative survey of mycosporine-like amino acids (MAAs) in intertidal egg masses from temperate rocky shores. J. Chem. Ecol. 31:2417–2438.CrossRefPubMedGoogle Scholar
  33. Przeslawski, R., Davis, A. R., and Benkendorff, K. 2005b. Synergies, climate change and the development of rocky shore invertebrates. Glob. Chang. Biol. 11:515–522.CrossRefGoogle Scholar
  34. Rawlings, T. A. 1996. Shields against ultraviolet radiation: An additional protective role for the egg capsules of benthic marine gastropods. Mar. Ecol., Prog. Ser. 136:81–95.CrossRefGoogle Scholar
  35. Rose, R. A. 1986. Direct development in Rostanga arbutus (Angas) (Mollusca: Nudibranchia) and the effects of temperature and salinity on embryos reared in the laboratory. J. Malacol. Soc. Australas. 7:141–154.Google Scholar
  36. Shick, J. M. and Dunlap, W. C. 2002. Mycosporine-like amino acids and related gadusols: Biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 64:223–262.CrossRefPubMedGoogle Scholar
  37. Shick, J. M., Dunlap, W. C., Chalker, B. E., Banaszak, A. T., and Rosenzweig, T. K. 1992. Survey of ultraviolet radiation-absorbing mycosporine-like amino acids in organs of coral reef holothuroids. Mar. Ecol., Prog. Ser. 90:139–148.CrossRefGoogle Scholar
  38. Shick, J. M., Romaine-Lioud, S., Ferrier-Pages, C., and Gattuso, J. 1999. Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol. Oceanogr. 44:1667–1682.CrossRefGoogle Scholar
  39. Shick, J. M., Dunlap, W. C., Pearse, J. S., and Pearse, V. B. 2002. Mycosporine-like amino acid content in four species of sea anemones in the genus anthopleura reflects phylogenetic but not environmental or symbiotic relationships. Biol. Bull. 203:315–330.PubMedCrossRefGoogle Scholar
  40. Sommaruga, R. and Garcia-Pichel, F. 1999. UV-absorbing mycosporine-like compounds in planktonic and benthic organisms from a high-mountain lake. Arch. Hydrobiol. 144:255–269.Google Scholar
  41. Teai, T., Drollet, J. H., Bianchini, J.-P., Cambon, A., and Martin, P. M. V. 1997. Widespread occurrence of mycosporine-like amino acid compounds in scleractinians from French Polynesia. Coral Reefs 16:169–176.CrossRefGoogle Scholar
  42. Zar, J. H. 1998. Biostatistical Analysis. Prentice-Hall, Upper Saddle River.Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of WollongongWollongongAustralia

Personalised recommendations