Hostname: page-component-848d4c4894-nr4z6 Total loading time: 0 Render date: 2024-05-12T03:55:32.632Z Has data issue: false hasContentIssue false

Photosymbiosis: The Driving Force for Reef Success and Failure

Published online by Cambridge University Press:  21 July 2017

George D. Stanley Jr.
Affiliation:
Department of Geosciences, The University of Montana, Missoula 59812
Jere H. Lipps
Affiliation:
Department of Geology, University of Georgia, Athens 30602
Get access

Abstract

Photosymbiosis has been an important process in the evolution of ancient reef systems and in reef success today. Modern reefs and many of those in the geologic past inhabited nutrient-depleted settings. The complete collapse of some ancient reef ecosystems may be attributed to the breakdown of the ecologic and physiologic relationships between symbiont and host. Many algal groups developed symbioses with calcifying metazoans and protists and live with them, but the most common of these today are dinoflagellates in the genus Symbiodinium, sometimes called zooxanthellae. This photosymbiotic relationship conferred important metabolic advantages to both partners, allowing exploitation of tropical, shallow-water oligotrophic settings. In addition to improved metabolism, a by-product was rapid calcification which increased the growth of reefs and provided advantages to the hosts through larger and stronger skeletal support. Strong evolutionary pressures exerted by the symbiont-host relationship created bonds and favored longevity and adaptive novelty. Photosynthesis accounts for the remarkable reef growth and carbonate sedimentation in the tropics. Photosymbiosis gave reef organisms an adaptive edge to develop new life strategies that could not be developed by organisms which did not foster this relationship. Many living calcified organisms harbor many different photosymbionts and likely a variety of ancient calcified organisms did too (foraminifera, calcified sponges, corals, brachiopods and bivalve mollusks). Symbiodinium now a dominant symbiont apparently appeared in the Eocene and so was probably not utilized by earlier reef organisms, although the fossil record of dinoflagellates most closely related to Symbiodinium extends back to the Triassic. Today Symbiodinium inhabits a wide variety of unrelated host organisms from protists to mollusks. While the identity of more ancient photosymbionts is unclear, indirect evidence suggests photosymbiotic ecosystems existed as far back as the Proterozoic and possibly even earlier.

Assessment of photosymbiosis in ancient reef ecosystems requires recognition of specific characteristics possessed by the calcifying reef organisms. Since the symbionts do not fossilize, the presence of photosymbiosis in fossils is a working hypothesis based on modern symbioses and best confirmed by a set of specific morphologic adaptations and isotopic analyses. Important among these is the thin tissue syndrome—the modification to achieve the “solar panel” effect. Large size and unusual or complex morphology also may indicate photosymbiosis. In the case of colonial organisms such as corals, high levels of corallite integration, where corallites are modified for increasing cooperation, may assist because most colonial photosymbiotic organisms today, such as corals, are exclusively photosymbiotic.

Analysis of organisms and reefs through geologic time permits assessment of the strength of photosymbiosis as a driving force. Reef ecosystems revealing the strongest assessment for photosymbiosis are those of the mid-Paleozoic (Late Ordovician to Devonian), late Paleozoic, early Mesozoic and Neogene. The Early Cambrian archaeocyathan (sponge) reefs indicate photosymbiosis but perhaps with different ancient symbionts such as cyanobacteria, also contained in some modern sponges. Reef ecosystems of the late Paleozoic and early part of the Jurassic indicate the presence of some photosymbiosis. The extinction of many photosymbiotic reef ecosystems during critical intervals of mass extinctions may have been driven by the failure of the symbiosis or demise of the symbionts. Reef gaps in the geologic record reflect the absence of photosymbiosis. The present-day reef crisis involves disturbance of photosymbiosis, and study of future reef declines will benefit by application of data from the fossil record.

Type
Research Article
Copyright
Copyright © 2011 by The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allwood, A. C., Waiter, M.R., Kamber, B.S., Marshall, C.P. and Burch, I.W. 2006. Stromatolite reef from the Early Archaean era of Australia. Nature, 441:714718.CrossRefGoogle ScholarPubMed
Baker, A.C. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology and biogeography of Symbiodinium . Annual Review of Ecology Evolution and Systematics, 34:661689.Google Scholar
Baron-Szabo, R. 2008. Corals of the K/T-boundary: scleractinians corals of the suborders Dendrophylliina, Caryophylliina, Fungiina, Microsolenina, and Stylinina. Zootaxa, 1952, 1244.Google Scholar
Benton, M. J. 2003. When Life Nearly Died: the greatest mass extinction of all time. Thames & Hudson, London, 335 p.Google Scholar
Berner, R.A., and Kothavala, Z. 2001. Geocarb III: a revised model of atmospheric CO2 over Phanerozoic time. American Journal of Science, 301:182204.Google Scholar
Blank, R. J., and Trench, R. K. 1985b. Symbiodinium microadriaticum: a single species? Proceedings of the Fifth International Coral Reef Congress, Tahiti, 6:113117.Google Scholar
Budd, A. F. 2000. Diversity and extinction in the Cenozoic history of Caribbean reefs. Coral Reefs, 19:2535.Google Scholar
Butterfield, N. J. and Rainbird, R. H. 1998. Diverse organic-walled fossils including ‘possible dinoflagellates’ from the early Neoproterozoic of arctic Canada. Geology, 26:963966.Google Scholar
Cairns, S. D. 1999. Species richness of recent Scleractinia. Atoll Research Bulletin, 459:146.CrossRefGoogle Scholar
Cairns, S. D. 2007. Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bulletin of Marine Science, 31:311322.Google Scholar
Carlon, D. B., Goreau, T.J., Goreau, N.I., Trench, R. K., Hayes, R. L., and Marshall, A.T. 1996. Calcification Rates in Corals. Science, 274:117118.CrossRefGoogle ScholarPubMed
Carpenter, K., Abrar, M., Aeby, G., et al. 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science, v. 321, p. 560563 Google Scholar
Coates, A. G., and Jackson, J. B. C. 1987. Clonal growth, algal symbiosis, and reef formation by corals. Paleobiology, 13:363378.Google Scholar
Coates, A. G., and Oliver, W. A. Jr. 1973. Coloniality in zoantharian corals, p. 325 In Boardman, R. S., Cheetham, A. H., and Oliver, W. A. Jr. (eds.), Animal Colonies: Development and Function Through Time. Dowden, Hutchinson, and Ross, Stroudsburg, PA.Google Scholar
Copper, P. 1989. Enigmas in Phanerozoic reef development. Memoirs of the Association of Australasian Paleontology, 8:371385.Google Scholar
Copper, P. 1994. Ancient reef ecosystem expansion and collapse. Coral Reefs, 13:311.Google Scholar
Copper, P. 2001. Evolution, radiations, and extinctions in Proterozoic to Mid-Paleozoic reefs, p. 89119 In Stanley, G. D. Jr. (ed.), The History and Sedimentology of Ancient Reef Systems. Kluwer Academic/Plenum Publishers, New York.Google Scholar
Copper, P. 2002a. Reef development at the Frasnian/Famennian mass extinction boudary. Palaeogeography, Palaeoclimatology, Palaeoecology, 181:2765.Google Scholar
Copper, P. 2002b. Silurian and Devonian reefs: 80 million years of global greenhouse between two ice ages, p. 181238 In Kiessling, W., Flügel, E., and Golonka, J. (eds.), Phanerozoic Reef Patterns. Volume 72. SEPM (Society for Sedimentary Geology), Tulsa.CrossRefGoogle Scholar
Copper, P., and Scotese, C. R. 2003. Megareefs in Middle Devonian supergreenhouse climates. Geological Society of America, Special Paper, 370:209230.Google Scholar
Cowen, R. 1983. Algal symbiosis and its recognition in the fossil record, p. 431478 In Tevesz, M. J. S. and McCall, P. L. (eds.), Biotic Interactions in Recent and Fossil Benthic Communities. Plenum Press, New York.Google Scholar
Cowen, R. 1988. The role of algal symbiosis in reefs through time. Palaios, 3:221227.Google Scholar
Dodge, R. E., and Vaišnys, J. R. 1980. Skeletal growth chronologies of Recent and fossil corals, p. 493517 In Rhoads, D. C. and Lutz, R. A. (eds.), Skeletal Growth of Aquatic Organisms: Biological Records of Environmental Change. Plenum Press, New York.Google Scholar
Erwin, D. H. 2006. Extinction: How Life On Earth Nearly Ended 250 Million Years Ago. Princeton University Press, Princeton, 296 p.Google Scholar
Ezaki, Y., and Kato, M. 1989. Growth bands in a Permian coral, in Proceedings, Fifth International Symposium of Fossil Cnidaria including Archaeocyatha and Spongiomorpha: Brisbane, Association of Australasian Palaeontologists, 5:8390.Google Scholar
Fagerstrom, J. A. 1987. The Evolution of Reef Communities. John Wiley and Sons, New York, 600 p.Google Scholar
Fagerstrom, J. A. 1996. Paleozoic brachiopod symbioses: Testing the limits of modern analogues in paleoecology. Geological Society of America Bulletin, 108:13931403.Google Scholar
Farmer, M. A., Fitt, W. K., and Trench, R. K. 2001. Morphology of the Symbiosis Between Corculum cardissa (Mollusca: Bivalvia) and Symbiodinium corculorum (Dinophyceae). Biological Bulletin, 200:336343.Google Scholar
Fautin, B. G., and Buddemeer, R. W. Adantive bleaching a general phenomenon. Hydrobiologia, 530/531:459467.Google Scholar
Fay, S., Weber, M., and Lipps, J.H. 2009. The distribution of Symbiodinium diversity within individual host foraminifera. Coral Reefs, 28:717726.Google Scholar
Fine, M., and Tchernov, D. 2007. Scleractinian coral species survive and recover from decalcification. Science, 315:1811.Google Scholar
Flügel, E. 2002. Triassic reef patterns. p. 391463 In Kiessling, W., Flügel, E., and Golonka, J. (eds.), Phanerozoic Reef Patterns. SEPM Special Publication 72, Tulsa.Google Scholar
Flügel, E., and Senowbari-Daryan, B. 2001. Triassic reefs of the Tethys, p. 217249 In Stanley, G. D. Jr. (ed.), The History and Sedimentology of Ancient Reef Systems. Kluwer Academic/Plenum Publishers, New York.CrossRefGoogle Scholar
Flügel, E., and Stanley, G. D. Jr. 1984. Reorganization development and evolution of post-Permian reefs and reef organisims. Palaeontographica Americana, 54:177186.Google Scholar
Fraser, N. M., Bottjer, D. J., and Fischer, A. G. 2004. Dissecting “Lithiotis” Bivalves: implications for the Early Jurassic reef eclipse. Palaios, 19:5167.Google Scholar
Freudenthal, H. D. 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. Journal of Protozoology 9:4552.Google Scholar
Furla, P., Allemand, D., Shick, J.M., Ferrier-Pages, C., and Richier, S. 2005. The symbiotic anthozoan: a physiological chimera between alga and animal. Integrative and Comparative Biology, 45:595604.Google Scholar
Gao, J. G., and Copper, P., 1997. Growth rates of Middle Paleozoic corals and sponges: Early Silurian of Eastern Canada, in Proceedings, 8th International Coral Reef Symposium: Panama City, Panama, 2:16511656.Google Scholar
Gattuso, J.-P., Allemand, D., and Frankignoulle, M. 1999. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: A review on interactions and control by carbonate chemistry. American Zoologist, 39:160183.CrossRefGoogle Scholar
Gili, E., Masse, J.-P., and Skelton, P. W. 1994. Rudists as gregarious sediment-dwellers, not reef-builders, on Cretaceous carbonate platforms. Palaeogeography, Palaeoclimatolgy, Palaeoecology, 118:245267.CrossRefGoogle Scholar
Goreau, T. F., and Goreau, N. I. 1959. The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biological Bulletin, 117:127167.Google Scholar
Goreau, T. J., Goreau, N.I., Trench, R.K., and Hayes, R.L. 1996. Calcification rates in corals. Science, 274:117.CrossRefGoogle ScholarPubMed
Grant, R. E. 1972. The lophophore and feeding mechanism of the Productidina (Brachiopoda). Journal of Paleontology, 46:213249.Google Scholar
Grotzinger, J. P. 1990. Geochemical model for Proterozoic stromatolite decline. American Journal of Science, 290A:80103.Google Scholar
Grotzinger, J.P. 1994. Trends in Precambrian carbonate sediments and their implication for the understanding of the evolution of life, p. 254258 In Bengton, S., (ed.), Early Life on Earth. Columbia University Press, New York.Google Scholar
Grotzinger, J. P., and Knoll, A.H. 1995. Anomalous Carbonate Precipitates: Is the Precambrian the Key to the Permian? Palaios, 10(6):578596.Google Scholar
Grotzinger, J. P., Watters, W. A., and Knoll, A. H. 2000. Calcified metazoans in thrombolite-stromatolite reefs of the terminal Proterozoic Nama Group, Namibia. Paleobiology 26:334359.Google Scholar
Hallock, P. 1997. Reefs and reef limestones in Earth history, p. 1342 In Birkeland, C. (ed.), Life and Death of Coral Reefs. Chapman and Hall, New York.Google Scholar
Hallock, P. 2001. Coral reefs, carbonate sediments, nutrients, and global change, p. 388427 In Stanley, G. D. Jr. (ed.), The History and Sedimentology of Ancient Reef Systems. Kluwer Academic/Plenum Publishers, New York.Google Scholar
Hallock, P., and Schlager, W. 1986. Nutrient excess and the demise of coral reefs and carbonate platforms. Palaios, 1:389398.Google Scholar
Hill, M., Allenby, A., Ramsby, B., Schönberg, C., and Hill, A. 2011. Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: Evidence of heteroplasmy and putative host-specific symbiont lineages. Molecular Phylogenetic Evolution, 59:81–8.Google Scholar
Hopley, D., Smithers, S. G., and Parnell, K. E. 2007. The geomorphology of the Great Barrier Reef: development, diversity, and change. Cambridge, Cambridge University Press, 532 pp.Google Scholar
Insalaco, E., Hallam, A., and Rosen, B. 2008. Oxfordian (Upper Jurassic) coral reefs in Western Europe: reef types and conceptual depositional model. Sedimentology, 44:707734.Google Scholar
Isozaki, Y., and Aljinović, D. 2009. End-Guadalupian extinction of the Permian gigantic bivalve Alatoconchidae: end of gigantism in tropical seas by cooling. Palaeogeography, Palaeoctimatology, Palaeoecology, 284:111.Google Scholar
Johnson, C. C. 2002. The rise and fall of Rudist reefs. American Scientist, 90:148153.Google Scholar
Johnson, C. C. and Kauffman, E. G. 2001. Cretaceous evolution of reef ecosystems: a regional synthesis of the Caribbean tropics, p. 311349 In Stanley, G. D. Jr. (ed.), The History and Sedimentology of Ancient Reef Systems. Kluwer Academic/ Plenum Publishers, New York.CrossRefGoogle Scholar
Johnson, K. G., Jackson, B.C., and Budd, A.F. 2008. Caribbean Reef Development Was Independent of Coral Diversity over 28 Million Years. Science, 319:15211523.Google Scholar
Jones, D.S., and Jacobs, D.K. 1992. Photosymbiosis in cardium nuttalli: Implications for tests of photosymbiosis in fossil molluscs: Palaios, 7:8695.Google Scholar
Kauffman, E. G., and Johnson, C. C. 1988. The morphological and ecological evolution of Middle and Upper Cretaceous reef-building rudistids. Palaios, 3:194216.Google Scholar
Kiessling, W. 2009. Geologic and biologic controls on the evolution of reefs. Annual Reviews of Ecology, Evolution and Systematics, 40:173192.Google Scholar
Kiessling, W. 2010. Reef expansion during the Triassic: Spread of photosymbiosis balancing climatic cooling. Palaeogeography, Palaeoclimatology, Palaeoecology, 290:1119.Google Scholar
Kiessling, W. 2011. On the potential for ocean acidification to be a general cause of ancient reef crises. Global Change Biology, 17:5667.Google Scholar
Kiessling, W., and Baron-Szabo, R.C. 2004. Extinction and recovery patterns of scleractinian corals at the Cretaceous-Tertiary boundary. Palaeogeography, Palaeoclimatology, Palaeoecology, 214:195223.CrossRefGoogle Scholar
Kleypas, J. A., Buddemeier, R. W., Archer, D., Gattuso, J. P., Langdon, C., and Opdyke, B. N. 1999. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science, 284:118120.Google Scholar
Knowlton, N, and Rohwer, F. 2003. Multispecies microbial mutualisms on coral reefs: the host as a habitat. American Naturalist 162 (4 Suppl):S5162.Google Scholar
Lajeunesse, T. C., Pettay, D. T., Sampayo, E. M., Phongsuwan, N., Brown, B., Obura, D. O., Hoegh-Guldberg, O., and Fitt, W. K. 2010. Long-standing environmental conditions, geographic isolation and host—symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium . Journal of Biogeography, 37:785800.Google Scholar
Langer, M. R. 2008. Assessing the contribution of foraminiferan protists to global ocean carbonate production. Journal of Eukaryotic Microbiology, 55:163169.Google Scholar
Langer, M. R., Silk, M. T., and Lipps, J. H. 1997. Global ocean carbonate and carbon dioxide production: The role of reef foraminifera. Journal of Foraminiferal Research, 27: 271277.CrossRefGoogle Scholar
Lee, J. J. 2006. Algal symbiosis in larger foraminifera. Symbiosis, 42(2):6375.Google Scholar
Lee, J. J. 2011. Fueled by symbiosis, Foraminifera have evolved to be giant complex protists. In Seckbach, J. and Dubinski, Z. (eds.), All Flesh Is Grass: Plant-Animal Interrelationships (Cellular Origin, Life in Extreme Habitats and Astrobiology), 16:427452.Google Scholar
Leingelder, R. R. 2001. Jurassic reef ecosystems, p. 251309 In Stanley, G. D. Jr. (ed.), The History and Sedimentology of Ancient Reef Systems. Kluwer Academic/Plenum Publishers, New York.Google Scholar
Lipps, J. H. 1986. Extinction dynamics in pelagic ecosystems, in: Elliott, D. K. (ed.), Dynamics of Extinction. J. Wiley & Sons, Inc., New York, p. 87104 Google Scholar
Little, A. F., Van Oppen, J. H., and Willis, B. L. 2004. Flexibility in algal endosymbioses shapes growth in reef corals. Science, 304:14921494.Google Scholar
Marshall, A. T. 1996. Calcification in Hermatypic and Ahermatypic Corals. Science, 271:637639.Google Scholar
Medina, M., Collins, A. G., Takaoka, T. L., Kuehl, J., and Boore, J. L. 2006. Naked Corals: Skeleton loss in Scleratinia. PNAS, 103:90969100.Google Scholar
Moldowan, J. M., Dahl, J., Jacobson, S.R., Huizinga, B.J., Fago, F.J., Shetty, R., Watt, D.S., and Peters, K.E. 1996. Chemostratigraphic reconstruction of biofacies: molecular evidence linking cyst-forming dinoflagellates with pre-Triassic ancestors. Geology, 24:159162.Google Scholar
Muscatine, L. 1990. The role of symbiotic algae in carbon and energy flux in reef corals. In Dubinsky, Z. (ed.), Ecosystems of the World: Coral Reefs. Elsevier, Amsterdam, pp. 7587 Google Scholar
Muscatine, L., Goiran, C., Land, L., Jaubert, J., Cuff, J.-P., and Allemand, D. 2005. Stable isotopes (-13C and -15N) of organic matrix from coral skeleton. PNAS, 102:15251530.Google Scholar
Nestor, H., Copper, P., and Stock, C.W. 2010. Late Ordovician and Early Silurian stromatoporoid sponges from Anticosti Island, eastern Canada: crossing the O/S mass extinction boundary. NRC Research Press, Ottawa, 163 pp., 28 text-figs., 28 pls. Google Scholar
Oliver, W. A. Jr. 1996. Origins and relationships of Paleozoic coral groups and the origin of the Scleractinia, p. 107134 In Stanley, G. D. Jr. (ed.), Paleobiology and Biology of Corals. Volume 1. Paleontological Society, Pittsburgh.Google Scholar
Pandolfi, J.M., Jackson, J.B.C., Baron, N., Bradbury, R.H., Guzman, H.M., Hughes, T.P., Kappel, C.V., Micheli, F., Ogden, J.C., Possingham, H.P., and Sala, E. 2005. Are US coral reefs on the slippery slope to slime? Science, 307(5716):17251726.Google Scholar
Pelejero, C., Calvo, E., McCulloch, M. T., Marshall, J. F., Gagan, M. K., Lough, J. M., and Opdyke, B. N. 2007. Preindustrial to modern interdecadal variability in coral reef pH. Science, 309:22042207.Google Scholar
Perrin, C. 2002. Tertiary: the emergence of modern reef ecosystems, p. 587621 In Kiessling, W., Flugel, E., and Golonka, J. (eds.), Phanerozoic Reef Patterns. SEPM Special Publication 72, Tulsa.Google Scholar
Piller, W. E. 1981. The Steinplatte reef complex, part of an Upper Triassic carbonate platform near Salzburg, Austria. Society of Economic Paleontologists and Mineralogists (SEPM). Special Publications, 30:261290.Google Scholar
Pochon, X., Montoya-Burgos, J. I., Stadelmann, B., and Powlowski, B.J.P. 2006. Molecular Phylogenetics and Evolution, 38:2030.Google Scholar
Pruss, S.B., and Bottjer, D. J. 2005. The reorganization of reef communities following the end-Permian mass extinction. Computes Rendus Palevol, 4:553568.Google Scholar
Riding, R. 1992. Temporal variation in calcification in marine cyanbacteria. Journal of the Geological Society of London, 149:979989.Google Scholar
Romano, S. L., and Palumbi, S. R. 1996. Evolution of scleractinian corals inferred from molecular systematics. Science, 271:640642.Google Scholar
Rosen, B. R. 2000. Algal symbiosis, and the collapse and recovery of reef communities: Lazarus corals across the K-T boundary. p. 164180 In Culver, S. J. and Rawson, P. A. (eds.), Biotic Response to Global Change: The Last 145 Million Years. Cambridge University Press, Cambridge.Google Scholar
Rosen, B. R., and Turnšek, D. 1989. Extinction patterns and biogeography of scleractinian corals across the Cretaceous/Tertiary boundary, p. 355370 In Jell, P. A. and Pickett, J. W. (eds.), Fossil Cnidaria 5. Association of Australasian Paleontology Memoir Nr. 8, Brisbane.Google Scholar
Rowland, S. M. 2001. Archaeocyaths—A history of phylogenetic interpretation. Journal of Paleontology, 75 (6):1065–107.Google Scholar
Rowland, S. M., and Gangloff, R. A. 1988. Structure and paleoecology of Lower Cambrian reefs. Palaios, 3:111135.Google Scholar
Rowland, S.M. and Shapiro, S.H. 2002. Reef patterns and environmental influences in the Cambrian and earliest Ordovician, p. 95128 In Kiessling, W., Flugel, E., and Golonka, J. (eds.), Phanerozoic Reef Patterns. SEPM Special Publication 72, Tulsa.Google Scholar
Royer, D.L., Berner, R.A., Montañez, I.P., Tabor, N.J., and Beerling, D.J. 2004. CO2 as a primary driver of Phanerozoic climate. GSA Today, 4:49.Google Scholar
Schopf, J.W. 1992. Paleobiology of the Archean, p. 2540 In Schopf, J.W., and Klein, C. (eds.), The Proterozoic Biosphere. Cambridge University Press, Cambridge.Google Scholar
Scott, R. W. 1988. Evolution of Late Jurassic and Early Cretaceous reef biotas. Palaios, 3:184193.Google Scholar
Scott, R. W., Fernández-Mendiola, P. A., Gili, E., and Simó, A. 1990. Persistence of coral-rudist reefs into the Late Cretaceous. Palaios, 5:98110.Google Scholar
Senowbari-Daryan, B., and Stanley, G.D. Jr. 2009. Taxonomic affinities and paleogeography of Stromatomorpha californica Smith, a distinctive Upper Triassic reef-adapted demosponge. Journal of Paleontology, 83(5):783793.Google Scholar
Siano, R., Montresor, M., Probert, I., Not, F., and de Vargas, C. 2010. Pelagodinium gen. nov. and P. beii comb nov., a dinoflagellate symbiont of planktonic foraminifera. Protist, 161:385399.Google Scholar
Stanley, G. D. Jr. 1981. Early history of scleractinian corals and its geological consequences. Geology, 9:507511.Google Scholar
Stanley, G. D. Jr. 1988. The history of early Mesozoic reef communities: A three-step process. Palaios, 3:170183.Google Scholar
Stanley, G. D. Jr. 2001. Introduction to reef ecosystems and their evolution. p. 139 In Stanley, G. D. Jr. (ed.), The History and Sedimentology of Ancient Reef Systems. New York, Kluwer Academic/Plenum Publishers.CrossRefGoogle Scholar
Stanley, G. D. Jr. 2003. The evolution of modern corals and their early history. Earth-Science Reviews, 60:195225.Google Scholar
Stanley, G. D. Jr. 2005. Coral microatolls from the Triassic of Nevada: oldest scleractinian examples. Coral Reefs, 24:247.CrossRefGoogle Scholar
Stanley, G. D. Jr. 2006. Photosymbiosis and the evolution of modern coral reefs. Science, 312, p. 857860 Google Scholar
Stanley, G. D. Jr. 2010. Recovery of coral reefs after the End-Permian and the “Naked Coral” Lazarus effect. Journal of Earth Science, 21, Special Issue: 161164.Google Scholar
Stanley, G.D. Jr., and Helmle, K.P. 2010. Middle Triassic coral growth bands and their implication for photosymbiosis. Palaios, 25:754763.Google Scholar
Stanley, G. D. Jr., and Fautin, D.F. 2001. The origins of modern corals. Science, 291:19131914.Google Scholar
Stanley, G. D. Jr., and Swart, P.K. 1995. Evolution of the coral-zooxanthellae symbiosis during the Triassic: a geochemical approach. Paleobiology, 21:179199.Google Scholar
Stanley, G. D. Jr. and Van de Schootbrugge, B. 2009. The evolution of the coral- algal symbiosis. In van Oppen, M.J.H. and Lough, J. M. (eds.), Coral Bleaching: Patterns, Processes, Causes and Consequences. Ecological Studies Series, 205:719.Google Scholar
Stanley, S. M., and Hardie, L. A. 1998. Secular oscillations in the carbonate mineralogy of reef-building and sediment-producing organisms driven by tectonically forced shifts in seawater chemistry. Palaeogeography, Palaeoclimatology, Palaeoecology, 144:319.Google Scholar
Stanton, R. J., and Flügel, E. 1987. Paleoecology of Upper Triassic reefs in the Northern Calcareous Alps: reef communities. Facies, 16:157186.Google Scholar
Steuber, T. 2000. Skeletal growth rates of Upper Cretaceous rudist bivalves: implications for carbonate production and organism-environment feedbacks. p. 2132 In Insalaco, E., Skeleton, P.W., and Palmer, T.J. (eds.), Carbonate Platform Systems: Components and Interactions Geological Society, London, Special Publications, 178, London.Google Scholar
Surge, D.M., Savarese, M., Dodd, J.R., and Lohmann, K.C. 1997. Carbon isotopic evidence for photosymbiosis in Early Cambrian oceans. Geology, 25:503506.Google Scholar
Tager, D., Webster, J. M., Potts, D. C., Renema, W., Braga, J. C., and Pandolfi, J. M. 2010. Community dynamics of Pleistocene coral reefs during alternative climatic regimes. Ecology, 91:191200.Google Scholar
Talent, J. A. 1988. Organic reef-building: episodes of extinction and symbiosis? Senckenbergiana Lethaea, 69:315368.Google Scholar
Talge, H. K., and Hallock, P. 2003. Ultrastructural responses in field-bleached and experimentally stressed Amphistegina gibbosa (Class Foraminifera). Journal of Eukaryotic Microbiology, 50: 324333.Google Scholar
Turner, E.C., Nargonne, G.M., and James, N.P. 1993. Neoproterozoic reef microstructure from the Little Dal Group, northwestern Canada. Geology, 21:259262.Google Scholar
Van Oppen, M. J. H., and Lough, J. M. 2009. Coral Bleaching: Patterns, Processes, Causes, and Consequences. Springer-Verlag, Berlin Heidelberg, 178 p.Google Scholar
Veron, J.E.N. 2000. Corals of the World. Australian Institute of Marine Sciences, Townsville, 1350 p.Google Scholar
Vernon, J.E.N. 2008. Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs, 27:459472.Google Scholar
Vogel, K. 1975. Endosymbiotic algae in rudists. Palaeogeography, Palaeoclimatology, Palaeoecology, 17:327332.Google Scholar
Walter, M. R. 1983. Archean stromatolites: evidence of the Earth's earliest benthos, p. 187213 In Schopf, J.W. (ed.), Earth's Earliest Biosphere, Princeton University Press, Princeton.Google Scholar
Watson, M. E., and Signor, P. W. 1986. How a clam builds windows: shell microstructure in Corculum (Bivalvia: Cardiidae). The Veliger, 28:348355.Google Scholar
Webby, B.D. 2002. Patterns of Ordovician reef development. p. 129179 In Kiessling, W., Flugel, E., and Golonka, J. (eds.), Phanerozoic Reef Patterns. SEPM Special Publication 72, Tulsa.Google Scholar
Weidlich, O. 2002. Middle and Late Permian reefs—distributional patterns and reservoir potential, p. 339390 In Kiessling, W., Flugel, E., and Golonka, J. (eds.), Phanerozoic Reef Patterns. SEPM Special Publication 72, Tulsa.Google Scholar
Wignall, P.B. and Twitchett, R. J. 1996. Oceanic Anoxia and the End Permian Mass Extinction. Science, 272:11551158.Google Scholar
West, R. R. 1988. Temporal changes in Carboniferous reef mound communities. Palaios, 3:152169.Google Scholar
Wood, R. 1993. Nutrients, predation and the history of reef-building. Palaios, 8:526543.Google Scholar
Wood, R. 1999. Reef Evolution. Oxford University Press, Oxford, 414 p.Google Scholar
Yancey, T. E. and Stanley, G. D. Jr. 1999. Giant alatoform bivalves in the Upper Triassic of western North America. Paleontology, 42:123.Google Scholar
Young, G. A., and Kershaw, S. 2005. Classification and controls of internal banding in Paleozoic stromatoporoids and colonial corals: Palaeontology, 48:623651.Google Scholar
Zhuravlev, A.Y. 2001. Paleoecology of Cambrian Reef ecosystems. p. 121157 In Stanley, G. D. Jr. (ed.), The History and Sedimentology of Ancient Reef Systems. New York, Kluwer Academic/Plenum Publishers.Google Scholar