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Marine Biology

, Volume 144, Issue 6, pp 1057–1064 | Cite as

Effects of diet, ultraviolet exposure, and gender on the ultraviolet absorbance of fish mucus and ocular structures

  • J. P. ZamzowEmail author
Research Article

Abstract

Ultraviolet (UV) radiation can be damaging to fish skin and ocular components. Coral reef fishes are regularly exposed to potentially harmful radiation. It was recently discovered that tropical marine fishes possess UV-absorbing compounds in their mucus. This experiment demonstrates significant effects of both diet and ultraviolet exposure on the UV-absorbing compounds in the mucus of a tropical wrasse, Thalassoma duperrey. Fish that are exposed to UV radiation increase the UV absorbance of their mucus only if UV-absorbing compounds are provided in their diet. Fish that are protected from UV radiation decrease the UV absorbance of their mucus regardless of diet. Mucus from female T. duperrey absorbed less UV and females had higher rates of skin damage than males. Females sequester UV-absorbing compounds in their pelagic eggs as well as their epithelial mucus, whereas males do not sequester these compounds in the testes. Spectral transmission through the whole eye was not affected by diet or UV manipulations, but corneal tissue transmission decreased significantly in the UV-exposed individuals. These results demonstrate that coral reef fish can adapt to UV exposure, so long as UV-absorbing compounds are available in the diet.

Keywords

High Performance Liquid Chromatography Fish Length Damage Score Mucus Sample Epithelial Mucus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

G. Losey, A. Taylor, T. Tricas, P. Nachtigall, D. Jameson, P. Nelson, and D. Copson provided valuable discussions and helpful comments that greatly improved the final manuscript. K. Del Carmen, S. Shimoda, E.G. Grau, E. Conklin, and M. Okihiro are appreciated for their help with the experimental diet formulation. P. Jokiel graciously allowed the use of his tanks. A. May, S. Christensen, and R. Bidigare facilitated the HPLC analyses. This work was funded by NSF-OCE9810387 and is contribution 1171 of the Hawaii Institute of Marine Biology. These experiments were conducted under IACUC Protocol # 95-012 and comply with the current laws of the United States.

References

  1. Adams NL (2001) UV radiation evokes negative phototaxis and covering behavior in the sea urchin Strongylocentrotus droebachiensis. Mar Ecol Prog Ser 213:87–95Google Scholar
  2. Adams NL, Shick JM, Dunlap WC (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 138:267–280CrossRefGoogle Scholar
  3. Ahmed FE, Setlow RB (1993) Ultraviolet radiation-induced DNA damage and its photorepair in the skin of the platyfish Xiphophorus. Cancer Res 53:2249–2255PubMedGoogle Scholar
  4. Banaszak AT, Lesser MP (1995) Survey of mycosporine-like amino acids in macrophytes in Kane’ohe Bay. In: Gulko D, Jokiel PL (eds) Ultraviolet radiation and coral reefs (Vol UNIHI-Seagrant-CR-95-03) Sea Grant Publication, Honolulu, Hawaii, pp 171–179Google Scholar
  5. Banaszak AT, Lesser MP, Kuffner IB, Ondrusek M (1998) Relationship between ultraviolet (UV) radiation and mycosporine-like amino acids (MAAs) in marine organisms. Bull Mar Sci 63:617–628Google Scholar
  6. Bandaranayake WM, Des Rocher A (1999) Role of secondary metabolites and pigments in the epidermal tissues, ripe ovaries, viscera, gut contents and diet of the sea cucumber Holothuria atra. Mar Biol 133:163–169Google Scholar
  7. Bullock AM, Roberts RJ, Waddington P (1983) Sunburn lesions in koi carp. Vet Rec 112:551PubMedGoogle Scholar
  8. Buma AGJ, de Boer MK, Boelen P (2001) Depth distributions of DNA damage in Antarctic marine phyto- and bacterioplankton exposed to summertime UV radiation. J Phycol 37:200–208CrossRefGoogle Scholar
  9. Carefoot TH, Harris M, Taylor BE, Donovan D, Karentz D (1998) Mycosporine-like amino acids: possible UV protection in eggs of the sea hare Aplysia dactylomela. Mar Biol 130:389–396Google Scholar
  10. Carefoot TH, Karentz D, Pennings SC, Young CL (2000) Distribution of mycosporine-like amino acids in the sea hare Aplysia dactylomela: effect of diet on amounts and types sequestered over time in tissues and spawn. Comp Biochem Physiol C Toxicol Pharmacol 126:91–104CrossRefPubMedGoogle Scholar
  11. Carreto JI, Carignan MO, Daleo G, DeMarco SG (1990) Occurrence of mycosporine-like amino acids in the red-tide dinoflagellate Alexandrium excavatum: UV-photoprotective compounds? J Plankton Res 12:909–921Google Scholar
  12. Carroll AK, Shick JM (1996) Dietary accumulation of UV-absorbing mycosporine-like amino acids (MAAs) by the green sea urchin (Strongylocentrotus droebachiensis). Mar Biol 124:561–569Google Scholar
  13. Chioccara F, Della Galla A, De Rosa M, Novellino E, Prota G (1980) Mycosporine aminoacids and related compounds from the eggs of fishes. Bull Soc Chim Belg 89:1101–1106Google Scholar
  14. Cockell CS, Knowland J (1999) Ultraviolet radiation screening compounds. Biol Rev 74:311–345Google Scholar
  15. Cullen AP, Monteith-McMaster CA (1993) Damage to the rainbow trout (Oncorhynchus mykiss) lens following an acute dose of UVB. Curr Eye Res 12: 97–106Google Scholar
  16. Cullen AP, Monteith-McMaster CA, Sivak JG (1994) Lenticular changes in rainbow trout following chronic exposure to UV radiation. Curr Eye Res 13:731–737PubMedGoogle Scholar
  17. DeKoven DL, Nunez JM, Lester SM, Conklin DE, Marty GD, Parker LM, Hinton DE (1992) A purified diet for Medaka (Oryzias latipes): refining a fish model for toxicological research. Lab Anim Sci 42:180–189PubMedGoogle Scholar
  18. Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34:418–430CrossRefGoogle Scholar
  19. Dunlap WC, Chalker BE, Oliver JK (1986) Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia III. UV-B absorbing compounds. J Exp Mar Biol Ecol 104:239–248CrossRefGoogle Scholar
  20. Dunlap WC, Williams DM, Chalker BE, Banaszak AT (1989) Biochemical photoadaptation in vision: U.V.-absorbing pigments in fish eye tissues. Comp Biochem Physiol B Biochem Mol Biol 93:601–607CrossRefGoogle Scholar
  21. Dunlap WC, Shick JM, Yamamoto Y (2000) UV protection in marine organisms I. Sunscreens, oxidative stress and antioxidants. In: Yoshikawa T, Toyokuni S, Yamamoto Y, Naito Y (eds) Free radicals in chemistry, biology, and medicine. OICA International, London, pp 200–214Google Scholar
  22. Fabacher DL, Little EE (1995) Skin component may protect fishes from ultraviolet-B radiation. Environ Sci Pollut Res Int 2:30–32Google Scholar
  23. Grant PT, Middleton C, Plack PA, Thomson RH (1985) The isolation of four aminocyclohexenimines (mycosporines) and a structurally related derivative of cyclohexane-1:3-dione (gadusol) from the brine shrimp, Artemia. Comp Biochem Physiol B Biochem Mol Biol 80:755–759CrossRefGoogle Scholar
  24. Helbling EW, Chalker BE, Dunlap WC, Holm-Hansen O, Villafane VE (1996) Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation. J Exp Mar Biol Ecol 204:85–101CrossRefGoogle Scholar
  25. Hobson ES (1974) Feeding relationships of teleostean fishes on coral reefs in Kona, Hawaii. Fish Bull 72:915–1031Google Scholar
  26. Hogan MJ, Alvarado JA, Weddell JE (1971) Histology of the human eye. Saunders, PhiladelphiaGoogle Scholar
  27. Jokiel PL (1980) Solar ultraviolet radiation and coral reef epifauna. Science 207:1069–1071Google Scholar
  28. Karentz D, Lutze LH (1990) Evaluation of biologically harmful ultraviolet radiation in Antarctica with a biological dosimeter designed for aquatic environments. Limnol Oceanogr 35:549–561Google Scholar
  29. Lesser MP, Farrell JH, Walker CW (2001) Oxidative stress, DNA damage and p53 expression in the larvae of Atlantic cod (Gadus morhua) exposed to ultraviolet (290–400 nm) radiation. J Exp Biol 204:157–164PubMedGoogle Scholar
  30. Losey GS, Nelson PA, Zamzow JP (2000) Ontogeny of spectral transmission in the eye of the tropical damselfish, Dascyllus albisella (Pomacentridae), and possible effects on UV vision. Environ Biol Fish 59:21–28CrossRefGoogle Scholar
  31. Lowe C, Goodman-Lowe G (1996) Suntanning in hammerhead sharks. Nature 383:677PubMedGoogle Scholar
  32. Lyons MM, Aas P, Pakulski JD, Waasbergen L van, Miller RV, Mitchell DL, Jeffrey WH (1998) DNA damage induced by ultraviolet radiation in coral-reef microbial communities. Mar Biol 130:537–543CrossRefGoogle Scholar
  33. Madronich S, McKenzie RL, Bjorn LO, Caldwell MM (1998) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. J Photochem Photobiol B Biol 46:5–19CrossRefGoogle Scholar
  34. Mason DS, Schafer F, Shick JM, Dunlap WC (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids (MAAS) are acquired from their diet by medaka fish (Oryzias latipes) but not by SKH-1 hairless mice. Comp Bioch Physiol A Mol Integr Physiol 120:587–598CrossRefGoogle Scholar
  35. Nelson PA, Zamzow JP, Erdmann SW, Losey GS (2003) Ontogenetic changes and environmental effects on ocular transmission in four species of coral reef fishes. J Comp Physiol [A] 189:391–399Google Scholar
  36. Newman SJ, Dunlap WC, Nicol S, Ritz D (2000) Antarctic krill (Euphausia superba) acquire a UV-absorbing mycosporine-like amino acid from dietary algae. J Exp Mar Biol Ecol 255:93–110PubMedGoogle Scholar
  37. Orlov OY, Gamburtzeva AG (1976) Changeable coloration of cornea in the fish Hexagrammos octogrammus. Nature 263:405–407PubMedGoogle Scholar
  38. Plack PA, Fraser NW, Grant PT, Middleton C, Mitchell AI, Thomson RH (1981) Gadusol, an enolic derivative of cyclohexane-1,3-dione present in the roes of cod and other marine fish. Biochem J 199:741–747PubMedGoogle Scholar
  39. Ramos KT, Fries LT, Berkhouse CS, Fries JN (1994) Apparent sunburn of juvenile paddlefish. Prog Fish-Culturist 56:214–216Google Scholar
  40. Roberts RJ (1989) Miscellaneous non-infectious diseases. In: Roberts RJ (ed) Fish pathology. Balliere Tindall, London, pp 363–373Google Scholar
  41. Ross RM, Losey GS (1983) Annual, semilunar, and diel reproductive rhythms in the Hawaiian labrid Thalassoma duperrey. Mar Biol 72:311–318Google Scholar
  42. Shand J, Foster RG (1999) The extraretinal photoreceptors of non-mammalian vertebrates. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive mechanisms in the ecology of vision. Kluwer Academic, Dordrecht, pp 197–222Google Scholar
  43. Shephard KL (1994) Functions for fish mucus. Rev Fish Biol Fish 4:401–429Google Scholar
  44. Shick JM, Lesser MP, Stochaj WR (1991) Ultraviolet radiation and photooxidative stress in zooxanthellate Anthozoa: the sea anemone Phyllodiscus semoni and the octocoral Clavularia sp. Symbiosis 10:145–173Google Scholar
  45. Shick JM, Lesser MP, Dunlap WC, Stochaj WR, Chalker BE, Wu Won J (1995) Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar Biol 122:41–51Google Scholar
  46. Shick JM, Dunlap WC, Buettner GR (2000) Ultraviolet (UV) protection in marine organisms II. Biosynthesis, accumulation, and sunscreening function of mycosporine-like amino acids. In: Yoshikawa T, Toyokuni S, Yamamoto Y, Naito Y (eds) Free radicals in chemistry, biology, and medicine. OICA International, London, pp 215–228Google Scholar
  47. Siebeck UE, Marshall NJ (2000) Transmission of ocular media in labrid fishes. Philos Trans R Soc Lond 355:1257–1261Google Scholar
  48. Siebeck UE, Marshall NJ (2001) Ocular media transmission of coral reef fish—can coral reef fish see ultraviolet light? Vis Res 41:133–149CrossRefPubMedGoogle Scholar
  49. Smith EJ, Partridge JC, Parsons KN, White EM, Cuthill IC, Bennett ATD, Church SC (2002) Ultraviolet vision and mate choice in the guppy (Poecilia reticulata). Behav Ecol 13:11–19CrossRefGoogle Scholar
  50. Stimson J, Larned ST, Conklin E (2001) Effects of herbivory, nutrient levels, and introduced algae on the distribution and abundance of the invasive macroalga Dictyosphaeria cavernosa in Kaneohe Bay, Hawaii. Coral Reefs 19:343–357Google Scholar
  51. Stolarski R, Bojkov R, Bishop L, Zerefos C, Staehelin J, Zawodny J (1992) Measured trends in stratospheric ozone. Science 256:342–349Google Scholar
  52. Thorpe A, Douglas RH (1993) Spectral transmission and short-wave absorbing pigments in the fish lens—II. Effects of age. Vis Res 33:301–307CrossRefPubMedGoogle Scholar
  53. Thorpe A, Douglas RH, Truscott RJW (1993) Spectral transmission and short-wave absorbing pigments in the fish lens—I. Phylogenetic distribution and identity. Vis Res 33:289–300CrossRefPubMedGoogle Scholar
  54. Vetter RD, Kurtzman A, Mori T (1999) Diel cycles of DNA damage and repair in eggs and larvae of northern anchovy, Engraulis mordax, exposed to solar ultraviolet radiation. Photochem Photobiol 69:27–33Google Scholar
  55. Whitehead K, Karentz D, Hedges JI (2001) Mycosporine-like amino acids (MAAs) in phytoplankton, a herbivorous pteropod (Limacina helicina), and its pteropod predator (Clione antarctica) in McMurdo Bay, Antarctica. Mar Biol 139:1013–1019CrossRefGoogle Scholar
  56. Zagarese H, Williamson CE (2001) The implications of solar UV radiation exposure for fish and fisheries. Fish Fisheries 2:250–260CrossRefGoogle Scholar
  57. Zamzow JP, Losey GS (2002) Ultraviolet radiation absorbance by coral reef fish mucus: photo-protection and visual communication. Environ Biol Fish 63:41–47CrossRefGoogle Scholar
  58. Zigman S (1995) Environmental near-UV radiation and cataracts. Optom Vis Sci 72:899–901PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Zoology Department and Hawaii Institute of Marine BiologyUniversity of Hawaii at ManoaKaneoheUSA

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