[en] Studying the morphological changes of zooxanthellae in the host gastroderm is essential to understand the mechanisms of bleaching. Transmission electron microscopy was used to observe samples from four coral species-three collected from a barrier reef in Madagascar (Acropora digitifera (Dana, 1846), Echinopora hirsutissima Milne-Edwards & Haime, 1849 and Porites (Synaraea) rus Forskal, 1775)) and one cut from an aquarium-grown coral (Pocillopora damicornis (Linnaeus, 1758)-and from the hermatypic (zooxanthellae-containing) sea anemone Aiptasia pulchella (Carlgren, 1943). Zooxanthellae from bleached animals showed different stages of degradation or disorganization. Some were free, detached from the host gastroderm, associated or not with host-cell remains. Others were vacuolated, with abundant reserve material globules and angular holes probably created by the loss of crystalline material during cutting. Experimentally heat-shocked P. damicornis harboured, moreover, a greater number of dividing algae. Bleached individuals were found to vary as regards their response to stress, and zooxanthellae expelled from heat-shocked anemones showed a greater mitotic index and a higher survival rate than algae extracted or naturally externalized from healthy individuals. We propose a combination of morphological criteria for use in diagnosing the health state of algae-cnidarian symbiosis, so vulnerable in the case of bleaching.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Ladrière, Ophélie ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Ecologie animale et écotoxicologie
Compère, Philippe ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Département des sciences et gestion de l'environnement
Decloux, Nicole ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Département des sciences et gestion de l'environnement
Vandewalle, Pierre ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Morphologie fonctionnelle et évolutive
Poulicek, Mathieu ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Ecologie animale et écotoxicologie
Language :
English
Title :
Morphological alterations of zooxanthellae in bleached cnidarian hosts
Alternative titles :
[fr] Altérations morphologiques de zooxanthelles d'hôtes cnidaires atteints de blanchissement
Publication date :
2008
Journal title :
Cahiers de Biologie Marine
ISSN :
0007-9723
Publisher :
CNRS - Cahiers de Biologie Marine, Roscoff, France
Volume :
49
Issue :
3
Pages :
215-227
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Baghdasarian G. & Muscatine L. 2000. Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. The Biological Bulletin, 199: 278-286.
Banaszak A.T. & Trench R.K. 1995. Effects of ultraviolets; (UV) radiation on marine microalgal-invertebrate symbioses. I. Response of the algal symbionts in culture and in hospite. Journal of Experimental Marine Biology and Ecology, 194: 213-232.
Banin E., Ben-Haim Y., Israely T., Loya Y. & Rosenberg E. 2000. Effect of the environment on the bacterial bleaching of corals. Water, Air and Soil Pollution, 123: 337-352.
Brown B.E., Le Tissier M.D.A. & Bythell J.C. 1995. Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Marine Biology, 122: 655-663.
Buddemeier R. W. & Fautin D. G. 1993. Coral Bleaching as an Adaptive Mechanism: a Testable Hypothesis. Bioscience, 43: 320-326.
Drew E.A. 1972. The biology and physiology of alga-invertebrate symbioses. II. The density of symbiotic algal cells in a number of hermatypic hard corals and alcyonarians from various depths. Journal of Experimental Marine Biology and Ecology, 9: 71-75.
Dunn S.R., Bythell J.C., Le Tissier M.D.A., Burnett W.J. & Thomason J.C. 2002. Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. Journal of Experimental Marine Biology and Ecology, 272: 29-53.
Fagoonee I., Wilson H.B., Hassel M. & Turner J. 1999. The dynamics of zooxanthellae populations: a long-term study in the field. Science, 283: 843-845.
Falkowski P.G., Dubinsky Z., Muscatine L. & McCloskey L. 1993. Population control in symbiotic corals. Ammonium ions and organic materials maintain the density of zooxanthellae. Bioscience, 43: 606-611.
Fang L.H., Wang J.T. & Lin K.L. 1998. The subcellular mechanism of the release of zooxanthellae during coral bleaching. Proceedings of the National Science Council, 22: 150-158.
Fitt W.K., McFarland F.K., Warner M.E. & Chilcoat G.C. 2000. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef coral and relation to coral bleaching. Limnology and Oceanography, 45: 677-685.
Freshney R. 1987. Culture of animal cells: a manual of basic technique (A.R. Liss ed), pp. 117, Inc., New York.
Gates R. D., Baghdasarian G. & Muscatine L. 1992. Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. The Biological Bulletin, 182: 324-332.
Glynn P.W., Imai R., Sakai K., Nakano Y. & Vamazato K. 1993. Environmental responses of Okinawan (Ryuku Islands, Japan) reef corals to high sea temperature and UV radiation. In: Proceedings of the 7th International Coral Reef Symposium 1: 27-37.
Goreau T.F. 1964. Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora. Science, 145: 383-386.
Hoegh-Guldberg O. & Smith G.J. 1989. The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Daria. Journal of Experimental Marine Biology and Ecology, 129: 279-303.
Hoegh-Guldberg O. & Salvat B. 1995. Periodic mass bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia. Marine Ecology Progress Series, 121: 181-190.
Hoegh-Guldberg O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research, 50: 839-866.
Hoegh-Guldberg O. & Fine M. 2004. Low temperatures cause coral bleaching. Coral Reefs, 23: 444.
Jokiel P.L. 2004. Temperature stress and coral bleaching. In: Coral health and disease (E. Rosenberg & Y. Loya eds), Springer: Berlin. 488 pp.
Jones R.J. 1997. Changes in zooxanthellae densities and chlorophyll concentrations in corals during and after a bleaching event. Marine Ecology Progress Series, 158: 51-59.
Jones R.J. & Steven A.L. 1997. Effects of cyanide on corals in relation to cyanide fishing on reefs. Marine and Freshwater Research, 48: 517-522.
Kleppel G.S., Dodge R.E. & Reese C.J. 1989. Changes in Pigmentation Associated with the Bleaching of Stony Corals. Linmology and Oceanography, 34: 1331-1335.
Kuffner I.B. 2005. Temporal variation in photosynthetic pigments and UV-absorbing compounds in shallow populations of two Hawaiian reef corals. Pacific Sciences, 59: 561-580.
Kushmaro A., Loya Y., Fine M. & Rosenberg E. 1996. Bacterial infection and coral bleaching. Nature, 380: 396.
Ladrière O. 2006. Le blanchiment des coraux: Implications microbiennes et nouvelle voie d'investigation. Master Thesis in Oceanography, University of Liège, 69 pp.
LaJeunesse T.C. 2001. Investigating the biodiversity, ecology, and phylogeny of endosymblotic dinoflagellates in the genus Symbiodinium using the internal transcribed spacer region: in search of a "species" level marker. Journal of Phycology, 37: 866-880.
Meehan W.J. & Ostrander G.K. 1997. Coral bleaching: a potential biomarker of environmental stress. Journal of Toxicology and Environmental Health, 50: 529-552.
McClanahan T.R., Muthiga N.A. & Mangi S. 2001. Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs. Coral Reefs, 19: 380-391.
Mise T. & Hidaka M. 2003. Degradation of zooxanthellae in the coral Acropora nasuta during bleaching. Galaxea, 5: 33-40.
Muscatine L. & Porter J.W. 1977. Reef Corals: Mutualistic symbioses adapted to nutrient-poor environments. BioScience, 27: 454-460.
Nakano Y., Yamazato K., Masubara H. & Ito S. 1997. Responses of Okinawan reef-building corals to artificial high salinity. Galaxea, 13: 181-195.
Pillay R.M., Willis B. & Terashima H. 2005. Trends in the density of zooxanthellae in Acropora millepora (Ehrenberg, 1834) at the Palm Island Group, Great Barrier Reef, Australia. Symbiosis, 38: 209-226.
Ralf P.J., Gademann R. & Larkum A.W.D. 2001. Zooxanthellae expelled from bleached corals at 33°C are photosynthetically competent. Marine Ecology Progress Series, 220: 163-168.
Rosenberg E. & Loya Y. 1999. Vibrio shiloi is the etiological (causative) agent of Oculina patagonica bleaching: General implications. Reef Encounter, 25: 8-10.
Rowan R. 2004. Thermal adaptation in reef coral symbionts. Nature, 430: 742.
Rowan R., Knowlton N., Baker A.C. & Jara J. 1997. Landscape ecology of algal symbiont communities explains variation in episodes of coral bleaching. Nature, 388: 265-269.
Salih A., Hoegh-Guldberg O. & Cox G. 1997. Bleaching responses of symbiotic dinoflagellates in corals: the effects of light and elevated temperature on their morphology and physiology. In: Proceedings of the Australian Coral Reef Society - 75th Anniversary Conference, Heron Island.
Searle J., Kerr J.F.R. & Bishop C.J. 1982. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathology Annual, 17: 229-259.
Stimson J. 1997. The annual cycle of density of zooxanthellae in the tissues of field and laboratoryheld Pocillopora damicornis (Linnaeus). Journal of Experimental Marine Biology and Ecology, 214: 35-48.
Warner M.E., Fitt W.K. & Schmidt G.W. 1996. The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant, Cell and Environment, 19: 291-299.
Wilkerson F.P., Muller Parker G. & Muscatine L. 1983. Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnology and Oceanography, 28: 1009-1014.
Wilkerson F.P., Kobayashi D. & Muscatine L. 1988. Mitotic Index of symbiotic algae in Carribean reef corals. Coral Reefs, 7: 29-36.
