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Coral Reefs

, Volume 31, Issue 4, pp 1077–1091 | Cite as

Effects of UV radiation on the growth, photosynthetic and photoprotective components, and reproduction of the Caribbean shallow-water coral Porites furcata

  • J. L. Torres-PérezEmail author
  • R. A. Armstrong
Report

Abstract

Shallow reef corals can frequently be subjected to high doses of ultraviolet radiation [280–400 nm (UVR)] and have developed mechanisms to cope with this. Nevertheless, slight changes in this stressor may impact their physiology and ultimately their survival. Here, we present results on the effects of artificially enhanced UVR on the growth, reproduction, production of photosynthetic pigments and photoprotective compounds of the Caribbean shallow-water branching coral Porites furcata. Corals were randomly located in one of the three different treatments: normal photosynthetically active radiation (PAR) + UVR; normal PAR+ enhanced UVR; normal PAR+ depleted UVR. Growth rates were measured using the Alizarin red staining method, photosynthetic pigments as well as mycosporine-like amino acids (MAAs) were quantified through high-performance liquid chromatography, and fecundity was estimated after histological analyses. Growth and photosynthetic pigment concentration were negatively correlated with increased UVR, compared to controls exposed to normal UVR. A significant increase in MAAs was also found in colonies under enhanced UVR. Based on their respective concentrations, the primary mycosporine-glycine (λmax = 310 nm) and shinorine (λmax = 333 nm) are the main contributors to UVR absorption in this species, while the levels of the secondary MAA palythine (λmax = 320 nm) tripled toward the end of the 128 days of the experimental period. While several physical factors may influence reef coral physiology, the results suggest that slight increases in UVR can debilitate the skeletal constitution and severely reduce the fecundity of corals living in shallow waters.

Keywords

Ultraviolet radiation Coral growth Mycosporine-like amino acids Coral reproduction Porites furcata 

Notes

Acknowledgments

We would like to acknowledge the help and support from the Department of Marine Sciences, University of Puerto Rico. This research was supported by fellowships from the Alliance for Graduate Education Professoriate (AGEP) and from the National Science Foundation’s Puerto Rico Graduate Teaching Fellows in K-12 Education to the corresponding author, and a NASA grant (NCCW-0088) to RAA. We are grateful to the Puerto Rico Department of Natural and Environmental Resources particularly the Marine Fisheries Laboratory for facilitating their histology laboratory. This manuscript was greatly improved by the comments of two anonymous reviewers.

References

  1. Ayoub L, Hallock P, Coble P (2009) Colored dissolved organic material increases resiliency of coral reefs by controlling exposure to UVR. Proc 11th Int Coral Reef Symp 572–576Google Scholar
  2. Baker AC (1995) Solar UV-A inhibition of planula larvae in the reef-building coral Pocillopora damicornis. In: Gulko D, Jokiel PL (eds) Ultraviolet radiation and coral reefs. HIMB Tech. Report #41. UNIHI-Sea Grant-CR-95-03, pp 149–163Google Scholar
  3. Banaszak AT, Lesser MP (2009) Effects of solar ultraviolet radiation on coral reef organisms. Photochem Photobiol Sci 8:1276–1294PubMedCrossRefGoogle Scholar
  4. Banaszak AT, Trench RK (1995) Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses. II. The synthesis of mycosporine-like amino acids in response to exposure to UV in Anthopleura elegantissima and Cassiopeia xamachana. J Exp Mar Biol Ecol 194:233–250CrossRefGoogle Scholar
  5. Banaszak AT, Barba Santos MG, LaJeunesse TC, Lesser MP (2006) The distribution of mycosporine-like amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean. J Exp Mar Biol Ecol 337:131–146CrossRefGoogle Scholar
  6. Bidigare RR (1991) Analysis of algal chlorophylls and carotenoids. In: Hurd DC, Spencer DW (eds) Marine particles: analysis and characterization. Geophysical Monograph 63. American Geophysical Union, pp 119–123Google Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of Protein-Dye Binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  8. Chalker BE, Dunlap WC (1981) Extraction and quantitation of endosymbiotic algal pigments from reef-building corals. Proc 4th Int Coral Reef Symp 2:45–50Google Scholar
  9. Chornesky EA, Peters EC (1987) Sexual reproduction and colony growth in the scleractinian coral Porites astreoides. Biol Bull 172:161–177CrossRefGoogle Scholar
  10. Corredor JE, Bruckner AW, Muszynski FZ, Armstrong RA, García R, Morell JM (2000) UV-absorbing compounds in three species of Caribbean zooxanthellate corals: depth distribution and spectral response. Bull Mar Sci 67:821–830Google Scholar
  11. Davies PS (1991) Effects of daylight variations on the energy budget of shallow water corals. Mar Biol 108:137–144CrossRefGoogle Scholar
  12. Drohan AF, Thoney DA, Baker AC (2005) Synergistic effect of high temperature and ultraviolet-B radiation on the gorgonian Eunicea tuorneforti (Octocorallia: Alcyonacea: Plexauridae). Bull Mar Sci 77:257–266Google Scholar
  13. Drollet JH, Teai T, Faucon M, Martin PMV (1997) Field study of compensatory changes in UV-absorbing compounds in the mucus of the solitary coral Fungia repanda (Scleractinia: Fungiidae) in relation to solar UV radiation, sea-water temperature, and other coincident physico-chemical parameters. Mar Freshw Res 48:329–333CrossRefGoogle Scholar
  14. Dunlap WC, Chalker BE (1986) Identification and quantification of near-UV absorbing compounds (S-320) in a hermatypic scleractinian. Coral Reefs 5:155–159CrossRefGoogle Scholar
  15. Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol B 112:105–114CrossRefGoogle Scholar
  16. Dunlap WC, Chalker BE, Bandaranayake WM (1988) Ultraviolet light absorbing agents derived from tropical marine organisms of the Great Barrier Reef, Australia. Proc 6th Int Coral Reef Symp 3:89–93Google Scholar
  17. Ferrier-Pagès C, Richard C, Forcioli D, Allemand D, Pichon M, Shick JM (2007) Effects of temperature and UV radiation increases on the photosynthetic efficiency in four Scleractinian coral species. Biol Bull 213:76–87PubMedCrossRefGoogle Scholar
  18. Gladfelter EH (1984) Skeletal development in Acropora cervicornis: III. A comparison of monthly rates of linear extension and calcium carbonate accretion measured over a year. Coral Reefs 3:51–57CrossRefGoogle Scholar
  19. Gleason DF (1993) Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coral Porites astreoides. Limnol Oceanogr 38:1452–1463CrossRefGoogle Scholar
  20. Gleason DF, Wellington GM (1993) Ultraviolet radiation and coral bleaching. Nature 365:836–838CrossRefGoogle Scholar
  21. Gleason DF, Wellington GM (1995) Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Mar Biol 123:693–703CrossRefGoogle Scholar
  22. Häder DP, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285PubMedCrossRefGoogle Scholar
  23. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  24. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  25. Ito S, Hirata Y (1977) Isolation and structure of a mycosporine from the zoanthid Palythoa tuberculosa. Tetrahedron Lett 28:2429–2430CrossRefGoogle Scholar
  26. Jeffrey SW, Mantoura RFC, Wright SW (1997) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO PublishingGoogle Scholar
  27. Jeffrey SW, Wright SW, Zapata M (2011) Microalgal classes and their signature pigments. In: Roy S, Llewellyn CA, Egeland ES, Johnsen G (eds) Phytoplankton pigments: Characterization, chemotaxonomy and applications in oceanography. Cambridge University Press, Cambridge, pp 3–77CrossRefGoogle Scholar
  28. Jerlov NG (1950) Ultraviolet radiation in the sea. Nature 166:111–112PubMedCrossRefGoogle Scholar
  29. Jokiel PL, York RH Jr (1982) Solar ultraviolet photobiology of the reef coral Pocillopora damicornis and symbiotic zooxanthellae. Bull Mar Sci 32:301–315Google Scholar
  30. Jokiel PL, Leser MP, Ondrusek ME (1997) UV-absorbing compounds in the coral Pocillopora damicornis: interactive effects of UV radiation, photosynthetically active radiation, and water flow. Limnol Oceanogr 42:1468–1473CrossRefGoogle Scholar
  31. Jones RJ (1997) Changes in zooxanthellar densities and chlorophyll concentrations: in corals during and after a bleaching event. Mar Ecol Prog Ser 158:51–59CrossRefGoogle Scholar
  32. Kinzie RA III (1993) Effects of ambient levels of solar ultraviolet radiation on zooxanthellae and photosynthesis of the reef coral Montipora verrucosa. Mar Biol 116:319–327CrossRefGoogle Scholar
  33. Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120PubMedCrossRefGoogle Scholar
  34. Krupp DA, Blanck J (1995) Preliminary report on the occurrence of mycosporine-like amino acids in the eggs of the Hawaiian scleractinian corals Montipora verrucosa and Fungia scutaria. In: Gulko D, Jokiel PL (eds) Ultraviolet radiation and coral reefs. HIMB Tech. Report #41. UNIHI-Sea Grant-CR-95-03, pp 129–134Google Scholar
  35. Kuffner IB (2001a) Effects of ultraviolet radiation and water motion on the reef coral Porites compressa Dana: a flume experiment. Mar Biol 138:467–476CrossRefGoogle Scholar
  36. Kuffner IB (2001b) Effects of ultraviolet (UV) radiation on larval settlement of the reef coral Pocillopora damicornis. Mar Ecol Prog Ser 217:251–261CrossRefGoogle Scholar
  37. Kuwahara VS, Nakajima R, Othman BHR, Kushairi MRM, Toda T (2010) Spatial variability of UVR attenuation and bio-optical factors in shallow coral-reef waters of Malaysia. Coral Reefs 29:693–704CrossRefGoogle Scholar
  38. Leavitt PR, Cumming BF, Smol JP, Reasoner M, Pienitz R, Hodgson DA (2003) Climatic control of ultraviolet radiation effects on lakes. Limnol Oceanogr 48:2062–2069CrossRefGoogle Scholar
  39. Lesser MP (2012) Oxidative stress in tropical marine ecosystems. In: Abele D, Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative stress in aquatic ecosystems. Blackwell Publishing Ltd, pp 9–19Google Scholar
  40. Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377CrossRefGoogle Scholar
  41. Lesser MP, Lewis S (1996) Action spectrum for the effects of UV radiation on photosynthesis in the hermatypic coral Pocillopora damicornis. Mar Ecol Prog Ser 134:171–177CrossRefGoogle Scholar
  42. Lewis S (1995) Response of a Pacific stony coral to short-term exposure of ultraviolet and visible light. In: Gulko D, Jokiel PL (eds) Ultraviolet radiation and coral reefs. HIMB Tech. Report #41. UNIHI-Sea Grant-CR-95-03, pp 89–106Google Scholar
  43. Madronich S, McKenzie RL, Björn LO, Caldwell MM (1995) Changes in ultraviolet radiation reaching the Earth’s surface. Ambio 24:143–152Google Scholar
  44. Marsh JA (1970) Primary productivity of reef building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  45. Masiri I, Nuñez M, Weller E (2008) A 10-year climatology of solar radiation for the Great Barrier Reef: implications for recent mass coral bleaching events. Int J Remote Sens 29:4443–4462CrossRefGoogle Scholar
  46. Masuda K, Goto M, Maruyama T, Miyachi S (1993) Adaptation of solitary corals and their zooxanthellae to low light and UV radiation. Mar Biol 117:685–691CrossRefGoogle Scholar
  47. McKenzie RL, Aucamp PJ, Bais AF, Björn LO, Ilyas M (2007) Changes in biologically-active ultraviolet radiation reaching the Earth’s surface. Photochem Photobiol Sci 6:218–231PubMedCrossRefGoogle Scholar
  48. McKenzie RL, Aucamp PJ, Bais AF, Björn LO, Ilyas M, Madronich S (2011) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 10:182–198PubMedCrossRefGoogle Scholar
  49. Miller RL, Belz M, Del Castillo C, Trzaska R (2002) Determining CDOM absorption spectra in diverse coastal environments using a multiple pathlength, liquid core waveguide system. Cont Shelf Res 22:1301–1310CrossRefGoogle Scholar
  50. Muszynski FZ, Bruckner A, Armstrong RA, Morell JM, Corredor JE (1998) Within-colony variations of UV absorption in a reef building coral. Bull Mar Sci 63:589–594Google Scholar
  51. Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10PubMedCrossRefGoogle Scholar
  52. Ott RL, Longnecker M (2001) An introduction to statistical methods and data analysis. Duxbury Press, CaliforniaGoogle Scholar
  53. Pelejero C, Calvo E, McCulloch MT, Marshall JF, Gagan MK, Lough JM, Opdyke BN (2005) Preindustrial to modern interdecadal variability in coral reef pH. Science 309:2204–2207PubMedCrossRefGoogle Scholar
  54. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci USA 105:13674–13678PubMedCrossRefGoogle Scholar
  55. Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417CrossRefGoogle Scholar
  56. Shick JM (2004) The continuity and intensity of ultraviolet irradiation affect the kinetics of biosynthesis, accumulation, and conversion of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Limnol Oceanogr 49:442–458CrossRefGoogle Scholar
  57. Shick JM, Romaine-Lioud S, Ferrier-Pagès C, Gattuso J-P (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 44:1667–1682CrossRefGoogle Scholar
  58. Shick JM, Ferrier-Pagès C, Grover R, Allemand D (2005) Effects of starvation, ammonium concentration, and photosynthesis on the UV-dependent accumulation of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Mar Ecol Prog Ser 295:135–156CrossRefGoogle Scholar
  59. Siebeck O (1981) Photoreactivation and depth-dependent U.V. tolerance in reef coral in the Great Barrier Reef/Australia. Naturwissenschaften 67:426–427CrossRefGoogle Scholar
  60. Singh SP, Kumari S, Rastogi RP, Singh KL, Sinha RP (2008) Mycosporine-like amino acids (MAAs): Chemical structure, biosynthesis and significance as UV-absorbing/screening compounds. Indian J Exp Biol 46:7–17PubMedGoogle Scholar
  61. Smith RC, Baker KS (1979) Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem Photobiol 29:311–323CrossRefGoogle Scholar
  62. Soong K (1991) Sexual reproductive patterns of shallow-water reef corals in Panama. Bull Mar Sci 49:832–846Google Scholar
  63. Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54CrossRefGoogle Scholar
  64. Szmant AM, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastraea annularis. Coral Reefs 8:217–224CrossRefGoogle Scholar
  65. Szmant-Froelich AM, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum (Esper): Lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892Google Scholar
  66. Takano S, Uemura D, Hirata Y (1978a) Isolation and structure of a new amino acid, palythine, from the zoanthid Palythoa tuberculosa. Tetrahedron Lett 26:2299–2300CrossRefGoogle Scholar
  67. Takano S, Uemura D, Hirata Y (1978b) Isolation and structure of two new amino acids, palythinol and palythene, from the zoanthid Palythoa tuberculosa. Tetrahedron Lett 49:4909–4912CrossRefGoogle Scholar
  68. Takano S, Nakanishi A, Uemura D, Hirata Y (1979) Isolation and structure of a 334 nm UV-absorbing substance, porphyra-334 from the red alga Porphyra tenera Kjellman. Chem Lett 25:419–420CrossRefGoogle Scholar
  69. Tedetti M, Sempéré R (2006) Penetration of ultraviolet radiation in the marine environment: A review. Photochem Photobiol 82:389–397PubMedCrossRefGoogle Scholar
  70. Tomasick T, Sanders F (1985) Effects of eutrophication on reef-building corals: growth rate of the reef-building coral Montastrea annularis. Mar Biol 87:143–155CrossRefGoogle Scholar
  71. Torres JL, Morelock J (2002) Effects of terrigenous sediments influx on the coral cover and linear extension rates of three Caribbean massive coral species. Caribb J Sci 38:222–229Google Scholar
  72. Torres JL, Amstrong RA, Corredor JE, Gilbes F (2007) Physiological responses of Acropora cervicornis to increased solar irradiance. Photochem Photobiol 83:839–851PubMedCrossRefGoogle Scholar
  73. Torres JL, Armstrong RA, Weil E (2008) Enhanced ultraviolet radiation can terminate sexual reproduction in a Caribbean broadcasting species. J Exp Mar Biol Ecol 358:39–45CrossRefGoogle Scholar
  74. Tsujino I, Yabe K, Sekikawa I (1980) Isolation and structure of a new amino acid, shinorine from the red alga, Chondrus yendoi Yamada et Mikami. Bot Mar 23:65–68Google Scholar
  75. Venn AA, Wilson MA, Trapido-Rosenthal HG, Keely BJ, Douglas AE (2006) The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium. Plant Cell Environ 29:2133–2142PubMedCrossRefGoogle Scholar
  76. Warner ME, Berry-Lowe S (2006) Differential xanthophyll cycling and photochemical activity in symbiotic dinoflagellates in multiple locations of three species of Caribbean coral. J Exp Mar Ecol Biol 339:86–95CrossRefGoogle Scholar
  77. Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Mar Biol 141:31–38Google Scholar
  78. Weatherhead EC, Andersen SB (2006) The search for signs of recovery of the ozone layer. Nature 441:39–45PubMedCrossRefGoogle Scholar
  79. Wilkerson FP, Kobayashi D, Muscatine L (1988) Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7:29–36CrossRefGoogle Scholar
  80. Williamson CE, Zagarese HE (2003) UVR effects on aquatic ecosystems: a changing climate perspective. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems. Royal Society of Chemistry, Cambridge, pp 547–567CrossRefGoogle Scholar
  81. Winters G, Loya Y, Röttgers R, Beer S (2003) Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ. Limnol Oceanogr 48:1388–1393CrossRefGoogle Scholar
  82. Worrest RC, Van Dyke H, Thomson BE (1978) Impact of enhanced simulated solar ultraviolet radiation upon a marine community. Photochem Photobiol 27:471–478CrossRefGoogle Scholar
  83. Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjørnland T, Repeta D, Welschmeyer N (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 77:183–196CrossRefGoogle Scholar
  84. Yakovleva I, Bhangooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol B 139:721–730PubMedCrossRefGoogle Scholar
  85. Zepp RG, Shank CG, Stabenau E, Patterson KW, Cyterski M, Fisher W, Bartels E, Anderson SL (2008) Spatial and temporal variability of solar ultraviolet exposure of coral assemblages in the Florida Keys: Importance of colored dissolved organic matter. Limnol Oceanogr 53:1901–1922CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of Puerto RicoMayagüezUSA
  2. 2.NASA-AMES Research CenterMoffet FieldUSA

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