- Published:
The influence of UV radiation on number and ultrastructure of the endosymbiotic dinoflagellates in the sea anemoneCereus pedunculatus (Anthozoa: Actiniaria)
Helgoländer Meeresuntersuchungen volume 51, pages 487–502 (1998)
Abstract
The sea anemoneCereus pedunculatus was artificially UV-irradiated to test the effect of UV-light on the number of endosymbiotic dinoflagellates in its gastrodermis and on their ultrastructure. Anemones were kept in the laboratory in a light: dark cycle (LD 12∶12; 13 W m−2) at 18 °C and briefly (2, 5 and 9 d) exposed to UV radiation at quasisolar intensities, 0.5 or 1 W m−2. Their tentacles were then examined in the electron microscope for qualitative and quantitative changes in the zooxanthellae. There was an intensity-dependent decrease in the number of symbionts, which in some cases were lost altogether (bleaching). Irradiated anemones contained a larger proportion of symbionts with ultrastructural abnormalities, namely diminished starch, some mitochondria with altered matrix and, in particular, characteristic changes in the chloroplasts; instead of being densely stacked, the thylakoids were spread apart and swollen at the ends of their membranes to form vesicle-like structures. Relatively large vesicles also appeared in the cytoplasm. The resulting enlargement of the whole dinoflagellate cell was documented morphometrically. Another intensity-dependent effect was a significant decrease in mitosis rate, established by counting dividing symbiont cells in TEM micrographs. *** DIRECT SUPPORT *** A03B6037 00006
Literature Cited
Achituv, Y. & Dubinsky, Z., 1990. The adaptation of symbiotic associations between zooxanthellae and corals at different light levels. In: Microbiology in poecilotherms. Ed. by R. Lesel. Elsevier Science Publisher, Amsterdam, p. 43–46.
Banaszak, A. T. & Trench, R. K., 1995. Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbiosis. The synthesis of mycosporine-like maino acids in response to exposure to UV inAnthopleura elegantissima andCassiopeia xamachana.—J. exp. mar. Biol. Ecol.194, 233–250.
Banaszak, A. T., Iglesias-Prieto, R. & Trench, R. K., 1993.Scrippsiella velellae sp. nov. (Peridinia andGloeodinium viscum sp. nov. (Phytodiniales), dinoflagellate symbionts of two hydrozoans (Cnidaria).—J. Phycol.29, 517–528.
Benson-Rodenbough, B. & Ellington, W. R., 1982. Responses of the sea anemoneBunodosoma cavernata (Bosc.) (Anthozoa, Actiniaria, Actiniidae) to osmotic stress.—Comp. Biochem. Physiol.72, 731–735.
Brown, B. E. & Suharsono, 1990. Damage and recovery of coral reefs affected by El Niño-related seawater warming in the Thousand Islands, Indonesia.—Coral Reefs8, 163–170.
Brown, B. E. & Ogden, J. E., 1993. Coral bleaching.—Scient. Am.268, 44–50.
Brown, B. E., Dunne, R. P., Scoffin, T. P. & Letissier, M. D. A., 1994. Solar damage in intertidal corals.—Mar. Ecol. Prog. Ser.112, 312.
Buma, A. G. J., Zemmelink, H. J., Sjollema, K. & Gieskes, W. W. C., 1996. UV-B radiation modifies protein and photosynthetic pigment content, volume and ultrastructure of marine diatoms.— Mar. Ecol. Prog. Ser.142, 47–54.
Calkins, J. (Ed.) 1982. The role of solar ultraviolet radiation in marine ecosystems. Plenum Press, New York, 724 pp.
Coles, S. L. & Jokiel, P. L., 1977. Effects of temperature on photosynthesis and respiration in hermatypic corals.—Mar. Biol.43, 209–216.
Cook, C. B., 1983. Metabolic interchange in algae-invertebrate symbiosis.—Int. Rev. Cytol. (Suppl)14, 177–210.
Cook, C. B., Logan, A., Ward, J., Luckhurst, B. & Berg, C. J., 1990. Elevated temperatures and bleaching on a high latitude coral reef, the 1988 Bermuda event.—Coral Reefs9, 45–49.
Dodge, J. D., 1968. The fine structure of chloroplasts and pyrenoids in some marine dinoflagellates. —J. Cell Sci.3, 41–48.
Douglas, A. E., McAuley, P. J. & Davies, P. S., 1993. Algal symbiosis in Cnidaria.—J. Zool.231, 175–178.
Drollet, J. H., Glazion, P. & Martin, P. M. V., 1993. A study of mucus from a solitary coralFungia fungites (Scleractinia, Fungiidae) in relation to photobiological UV-adaptation.—Mar. Biol.115, 263–266.
Drollet, J. H., Faucon, M. & Martin, P. M. V., 1995. Elevated sea-water temperature and solar UV-B flux associated with two successive coral mass bleaching events in Tahiti.—Mar. Freshwat. Res.46, 1153–1157.
Fisk, D. A. & Done, T. J., 1985. Taxonomic and bathymetric patterns of bleaching corals, Myrmidon Reef, Queensland. In: Proceedings of the 5th International Coral Reef Congress. Ed. by C. Gabriel, J. Toffart & B. Salvat. 149–154.
Fitt, W. K. & Warner, M. E., 1995. Bleaching patterns of four species of Carribean reef corals.—Biol. Bull. mar. biol. Lab., Woods Hole189, 298–307.
Fleischmann, E. M., 1989. The measurement and penetration of ultraviolet radiation into tropical marine water.—Limnol. Oceanogr.34, 1623–1629.
Gates, R. D., 1990. Seawater temperature and sublethal coral bleaching in Jamaica.—Coral Reefs8, 193–198.
Gates, R. D., Baghdasarian, G. & Muscatine, C., 1992. Temperature stress causes host cell detachment in symbiotic cnidarians: Implications for coral bleaching.—Biol. Bull. mar. biol. Lab., Woods Hole182, 324–332.
Gieskes, W. W. C. & Kraay, 1990. Transmission of ultraviolet light in the Weddell Sea. Report on the first measurement made in Antarctic.—Biomass Newsl.12, 12–14.
Gleason, D. F., 1993. Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coralPorites asteroides.—Limnol. Oceanogr.38, 1452–1463.
Gleason, D. F. & Wellington, G. M., 1993. Ultraviolet radiation and coral bleaching.—Nature, Lond.365, 836–838.
gleason, D. F., Bhartia, P. K., Herman, J. R., McPeters, R., Newman, P., Stolarski, R. S., Flynn, L., Labow, G., Larko, D., Seftor, C., Wellemeyer, C., Komhyr, W. D., Miller, A. J. & Planet, W., 1993. Record low global ozone in 1992.—Science, N. Y.260, 523–526.
Glynn, P. W., 1991. Coral reef bleaching in the 1980s and possible connections with global warming. —Trends Ecol. Evol.6, 175–179.
Glynn, P. W., 1993. Coral reef bleaching: Ecological perspectives.—Coral Reefs12, 1–17.
Glynn, P. W., 1996. Coral reef bleaching: facts, hypotheses and implications.—Global Change Biol.2, 495–509.
Grigg, R. W. & Dollar, S. J., 1990. Effects of natural and anthropogenic disturbance on coral reefs. In: Coral reefs. Ed. by Z. Dubinsky. Elsevier, New York, 439–452.
Häberlein, A. & Häder, D. P., 1992. UV effects on photosynthetic oxygen production and chromoprotein composition in the freshwater flagellateCryptomonas S2.—Acta protozool.31, 85–92.
Häder, D. P., 1996. Effects of enhanced solar UV-B radiation on phytoplankton.—Scientia mar.60 (Suppl. 1), 59–63.
Häder, D. P. & Brodhun, B., 1991. Effects of ultraviolet radiation on the photoreceptor proteins and pigments in the paraflagellar body of the flagellate,Euglena gracilis.—J. Pl. Physiol.132, 641–646.
Häder, D. P. & Liu, S. M., 1990. Effects of artificial and solar UV-B radiation on the gravitactic orientation of the dinoflagellate,Peridinium gaternense.—FEMS Microbiol. Ecol.73, 331–338.
Häder, D. P. & Worrest, R. C., 1991. Effects of enhanced solar ultraviolet radiation on aquatic ecosystems.—Photochem. Photobiol.50, 459–468.
Harland, A. D. & Davies, P. S., 1994. Time-course of photoadaptation in the sea anemoneAnemonia viridis.—Mar. Biol.119, 45–51.
Harland, A. D., Fixter, L. M., Davies, P. S., Spencer, D. & Anderson, R. A., 1992. Effect of light on the total lipid content and storage lipeds of the symbiotic sea anemoneAnemonia viridis.—Mar. Biol.112, 253–258.
Hayes, R. L. & Bush, P. G., 1990. Microscopic observation of recovery in the reef-building scleractinian coral,Montastrea annularis after bleaching on a Cayman reef.—Coral Reefs8, 203–209.
Høegh-Guldberg, O & Smith, G. J., 1989. The effect of sudden changes in temperature, light, and salinity on population density and export of zooxanthellae from the reef coralSeriatopora pistillata andStylophora hystrix.—J. exp. mar. Biol. Ecol.129, 279–303.
Høegh-Guldberg, O., McClosky, L. R. & Muscatine, L., 1987. Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea.—Coral Reefs5, 201–204.
Jaap, W. C., 1985. An epidemic zooxanthellae expulsion during 1983 in the lower Florida Keys coral reefs: Hyperthermic ecology. In: Proceedings of the 5th International Coral Reef Congress. Ed. by C. Gabriel, J. Toffart & B. Salvat. 143–148.
Janssen, H. H. & Möller, H., 1981. Effects of various feeding conditions onAnemonia sulcata.—Zool. Anz.206, 161–170.
Jokiel, P. L. & Coles, S. L., 1974. Effects of heated effluent on hermatypic corals at Kahe Point, Oahu.—Pacif. Sci.28, 1–18.
Jokiel, P. L. & Coles, S. L., 1977. Effects of temperature on the mortality and growth of Hawaiian reef corals.—Mar. Biol.43, 201–208.
Jokiel, P. L. & Coles, S. L., 1990. Responses of Hawaiian and the Indo-Pacific reef corals elevated temperature.—Coral Reefs8, 155–162.
Jokiel, P. L. & York, R. H., 1982. Importance of ultraviolet radiation in photoinhibition of microalgal growth.—Limnol. Oceanogr.26, 192–199.
Jokiel, P. L. & York, R. H., 1984. Solar ultraviolet photobiology of the reef coralPocillopora damicornis and symbiotic zooxanthellae.—Bull. mar. Sci.32, 301–315.
Kevin, M. J., Hall, W. T., McLaughlin, J. J. A. & Zahl, P. A., 1969.Symbiodinium microadriaticum Freudenthal, a revised taxonomic description, ultrastructure.—J. Phycol.5, 341–350.
Khalilov, R. I., Khomutov, G. V. & Tikhonov, H. N., 1993. Effect of ultraviolet radiation on structural-functional characteristics of the thylakoid membrane.—Russ. Pl. Physiol.40, 338–342.
Kinzie, R. A., 1993. Effects of ambient levels of solar ultraviolet radiation on zooxanthellae and photosynthesis of reef coralMontipora verrucosa.—mar. Biol.116, 319–327.
Kushmaro, A., Loya, Y., Fine, M. & Rosenberg, E., 1996. Bacterial infection and coral bleaching.—Nature, Lond.380, 396.
Lasker, H. R., Peters, E. C. & Coffroth, M. A., 1984. Bleaching of reef coelenterates in the San Blas Islands, Panama.—Coral Reefs3, 183–190.
Lesser, M. P. & Shick, J. M., 1989. Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae ofAiptasia pallida: primary production, photoinhibition, and enzymatic defenses against oxygen toxicity.—Mar. Biol.102, 243–256.
Lesser, M. P., Stochaij, W. J., Tapley, D. W. & Shick, J. M., 1990. Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen.—Coral Reefs8, 225–232.
Masuda, K., Goto, M., Marayuma, T. & Miyachi, S., 1993. Adaptation of solitary corals and their zooxanthellae to low light and UV-radiation.—Mar. Biol.117, 685–691.
McLaughlin, J. J. A., Zahl, P. A. & Nowak, A., 1964. In vitro analysis, nutritional requirements and population dynamics of some free-living phytoplanktons and symbiotic algae (Zooxanthellae). In: 10th Intern. Botan. Congr., Edinburgh, 518 pp.
Muscatine, L., 1973. Nutrition of corals. In: Biology of coral reefs. Ed. by R. Endean. Acad. Press, New York, 2, 77–115.
Muscatine, L., 1980. Productivity of zooxanthellae. In: Primary productivity in the sea. Ed. by P. G. Falkowski. Plenum Press, New York, 381–402.
Muscatine, L., Falkowski, P., Dubinsky, Z., Cook, P. A. & McCloskey, L. R., 1989. The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral.—Proc. R. Soc. London (Ser. B)236, 311–324.
Pierce, S. K. & Minasian, L. C. Jr., 1974. Water balance of a euryhaline sea anemone,Diadumene leucolena.—Comp. Biochem. Physiol.49, 159–167.
Renger, G., Völker, M., Eckert, H.-J., Fromme, R., Hohm-Veit, S. & Gräber, P., 1989. On the mechanisms of photosystem II deterioration by UV-B irradiation.—Photochem. Photobiol.49, 97–105.
Schäfer, J., Sebastian, C. & Häder, D. P., 1993. Effects of solar radiation on motility, orientation, pigmentation and photosynthesis in a green dinoflagellateGymnodinium.—Acta protozool.33, 59–65.
Schmidt, H., 1972. Prodromus zu einer Monographie der mediterranen Aktinien.—Zoologica, Stuttgart,121, 1–146.
Shibata, K., 1969. Pigments and a UV-absorbing substance in corals and bluegreen algae living in the Great Barrier Reef.—Plant Cell Phys. Tokyo10, 325–335.
Shick, J. M., Lesser, M. P. & Jokiel, P. L., 1996. Effects of ultraviolet radiation on corals and other coral reef organisms.—Global Change Biol.2, 527–545.
Smith, R. C. & Baker, K. S., 1979. Penetration of UV-B and biologically effective dose rate in natural water.—Photochem. Photobiol.29, 311–323.
Smith, R. C. & Baker, K. S., 1984. The analysis of ocean optical data. Proceedings of the SPIE.—Ocean Optics489, 119–126.
Smith, R. C. & Tyler, J. E., 1976. Transmission of solar radiation into natural waters. In: Photochem. Photobiol. Rev.1, 117–155.
Steele, R. D., 1976. Light intensity as a factor in the regulation of the density of symbiotic zooxanthellae inAiptasia tagetes (Coelenterata, Anthozoa).—J. Zool.179, 387–405.
Suharsono & Brown, B. E., 1992. Comparative measurements of mitotic index in zooxanthellae from a symbiontic cnidarian subject to temperature increase.—J. exp. mar. Biol. Ecol.158, 179–188.
Taylor, D. L., 1968. In situ studies on the cytochemistry and ultrastructure of a symbiotic marine dinoflagellate.—J. mar. biol. Ass. U.K.48, 349–366.
Taylor, D. L., 1973. The cellular interactions of algal-invertebrate symbiosis.—Adv. mar. Biol.11, 1–55.
Tevini, M. (Ed.), 1993. UV-B radiation and ozone depletion. Effects on humans, animals, plants, microorganisms, and materials. Lewis Publishers, Boca Raton, 248 pp.
Tirlapur, U., Scheuerlein, R. & Häder, D.-P., 1993. Motility and orientiation of a dinoflagellate,Gymnodinium, impaired by solar and ultraviolet radiation.—FEMS Microbiol. Ecol.102, 167–174.
Trench, R. K. & Blank, R. J., 1987.Symbiodinium microadriaticum Freudenthal,S. goreaui, sp. nov.,S. kawaguti, sp. nov., andS. pilosum, sp. nov.: gymnodinoid dinoflagellate symbionts of marine invertebrates.—J. Phycol.23, 469–481.
Vernet, M. & Whitehead, K., 1996. Release of ultraviolet-absorbing compounds by the red-tide dinoflagellateLingulodinium polyedra.—Mar. Biol.127, 35–44.
Williams, E., Goenaga, C. & Vicente, V., 1987. Mass bleaching on the Atlantic coral reefs.— Science, N.Y.238, 877–878.
Zündorf, I. & Häder, D. P., 1991. Biochemical and spectroscopic analysis of UV effects in the marine flagellateCryptomonas maculata.—Archs Microbiol.156, 405–411.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hannack, K., Kestler, P., Sicken, O. et al. The influence of UV radiation on number and ultrastructure of the endosymbiotic dinoflagellates in the sea anemoneCereus pedunculatus (Anthozoa: Actiniaria). Helgoländer Meeresunters. 51, 487–502 (1998). https://doi.org/10.1007/BF02908729
Issue Date:
DOI: https://doi.org/10.1007/BF02908729