Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-19T01:34:49.978Z Has data issue: false hasContentIssue false
  • English
  • Français

Biodiversity dynamics and environmental occupancy of fossil azooxanthellate and zooxanthellate scleractinian corals

Published online by Cambridge University Press:  22 April 2015

Wolfgang Kiessling  and
Ádám T. Kocsis
Wolfgang Kiessling
Affiliation:
GeoZentrum Nordbayern, Department of Geography and Geosciences, Universität Erlangen-Nürnberg, Loewenichstraße 28, D-91054 Erlangen, Germany. E-mail: [email protected]
Ádám T. Kocsis
Affiliation:
MTA-MTM-ELTE Research Group for Paleontology and Department of Physical and Applied Geology, Eötvös University, Pázmány Péter sétány 1/C, H-1117 Budapest, Hungary
Get access Rights & Permissions [Opens in a new window]

Abstract

Scleractinian corals have two fundamentally different life strategies, which can be inferred from morphological criteria in fossil material. In the non-photosymbiotic group nutrition comes exclusively from heterotrophic feeding, whereas the photosymbiotic group achieves a good part of its nutrition from algae hosted in the coral’s tissue. These ecologic differences arose early in the evolutionary history of corals but with repeated evolutionary losses and presumably also gains of symbiosis since then. We assessed the biodiversity dynamics and environmental occupancy of both ecologic groups to identify times when the evolutionary losses of symbiosis as inferred from molecular analyses might have occurred and if these can be linked to environmental change. Two episodes are likely: The first was in the mid-Cretaceous when non-symbiotic corals experienced an origination pulse and started to become more common in deeper, non-reef habitats and on siliciclastic substrates initiating a long-term offshore trend in occupancy. The second was around the Cretaceous/Paleogene boundary with another origination pulse and increased occupancy of deep-water settings in the non-symbiotic group. Environmental factors such as rapid global warming associated with mid-Cretaceous anoxic events and increased nutrient concentrations in Late Cretaceous–Cenozoic deeper waters are plausible mechanisms for the shift. Turnover rates and durations are not significantly different between the two ecologic groups when compared over the entire history of scleractinians. However, the deep-water shift of non-symbiotic corals was accompanied by reduced extinction rates, supporting the view that environmental occupancy is a prominent driver of evolutionary rates.

Type
Articles
Information
Paleobiology , Volume 41 , Supplement 3 , June 2015 , pp. 402 - 414
Copyright
Copyright © 2015 The Paleontological Society. All rights reserved. 

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

Literature Cited

Alroy, J. 2010. The shifting balance of diversity among major marine animal groups. Science 329:1191–1194.CrossRefGoogle ScholarPubMed
Alroy, J. 2014. Accurate and precise estimates of origination and extinction rates. Paleobiology 40:374–397.CrossRefGoogle Scholar
Ando, A., Kaiho, K., Kawahata, H., and Kakegawa, T. 2008. Timing and magnitude of early Aptian extreme warming: unraveling primary delta O-18 variation in indurated pelagic carbonates at Deep Sea Drilling Project Site 463, central Pacific Ocean. Palaeogeography, Palaeoclimatology, Palaeoecology 260:463–476.CrossRefGoogle Scholar
Barbeitos, M. S., Romano, S. L., and Lasker, H. R. 2010. Repeated loss of coloniality and symbiosis in scleractinian corals. Proceedings of the National Academy of Sciences USA 107:11877–11882.CrossRefGoogle ScholarPubMed
Benayahu, Y., and Loya, Y. 1981. Competition for space among coral-reef sessile organisms at Eilat, Red Sea. Bulletin of Marine Science 31:514–522.Google Scholar
Bernecker, M., and Weidlich, O. 2005. Azooxanthellate corals in the Late Maastrichtian–Early Paleocene of the Danish basin: bryozoan and coral mounds in a boreal shelf setting. Pp. 3–25in A. Freiwald, and J. M. Roberts, eds. Cold-water corals and ecosystems. Springer, Berlin.CrossRefGoogle Scholar
Best, M. B. 2001. Some notes on the terms “deep-sea ahermatypic” and “azooxanthellate,” illustrated by the coral genus Madracis. Pp. 19–29in J. H. M. Willison, J. Hall, S. Gass, E. L. R. Kenchington, M. Butler, and P. Doherty, eds. Proceedings of the first international symposium on deep-sea corals. Ecology Action Centre and Nova Scotia Museum, Halifax.Google Scholar
Bottjer, D. J., and Jablonski, D. 1988. Paleoenvironmental patterns in the evolution of post-Paleozoic benthic marine invertebrates. Palaios 3:540–560.CrossRefGoogle Scholar
Bralower, T. J., and Thierstein, H. R. 1984. Low productivity and slow deep-water circulation in mid-Cretaceous oceans. Geology 12:614–618.2.0.CO;2>CrossRefGoogle Scholar
Cairns, S. D. 1999. Species richness of recent Scleractinia. Atoll Research Bulletin 459:1–46.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 81:311–322.Google Scholar
Caroselli, E., Mattioli, G., Levy, O., Falini, G., Dubinsky, Z., and Goffredo, S. 2012. Inferred calcification rate of a Mediterranean azooxanthellate coral is uncoupled with sea surface temperature along an 8 degrees latitudinal gradient. Frontiers in Zoology 9:32.CrossRefGoogle Scholar
Caruthers, A. H., Smith, P. L., and Grocke, D. R. 2013. The Pliensbachian-Toarcian (Early Jurassic) extinction, a global multi-phased event. Palaeogeography, Palaeoclimatology, Palaeoecology 386:104–118.CrossRefGoogle Scholar
Coates, A. C., and Jackson, J. B. C. 1987. Clonal growth, algal symbiosis, and reef formation by corals. Paleobiology 13:363–378.CrossRefGoogle Scholar
Creed, J. 2006. Two invasive alien azooxanthellate corals, Tubastraea coccinea and Tubastraea tagusensis, dominate the native zooxanthellate Mussismilia hispida in Brazil. Coral Reefs 25:350–350.CrossRefGoogle Scholar
Davies, P. S. 1984. The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2:181–186.CrossRefGoogle Scholar
de Paula, A. F., Pires, D. D., and Creed, J. C. 2014. Reproductive strategies of two invasive sun corals (Tubastraea spp.) in the southwestern Atlantic. Journal of the Marine Biological Association of the United Kingdom 94:481–492.CrossRefGoogle Scholar
Edmunds, P. J., and Davies, P. S. 1986. An energy budget for Porites porites (Scleractinia). Marine Biology 92:339–348.CrossRefGoogle Scholar
Erba, E., Bottini, C., Weissert, H. J., and Keller, C. E. 2010. Calcareous nannoplankton response to surface-water acidification around Oceanic Anoxic Event 1a. Science 329:428–432.CrossRefGoogle ScholarPubMed
Falkowski, P. G., Dubinsky, Z., Muscatine, L., and Porter, J. W. 1984. Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709.CrossRefGoogle Scholar
Foote, M. 2000. Origination and extinction components of taxonomic diversity: general problems. In D. H. Erwin, and S. L. Wing, eds. Deep time: Paleobiology’s perspective (Paleobiology 26(Suppl. to No. 4), 74–102.Google Scholar
Foote, M., and Miller, A. I. 2007. Principles of paleontology. W. H. Freeman, New York.Google Scholar
Foote, M., and Raup, D. M. 1996. Fossil preservation and the stratigraphic ranges of taxa. Paleobiology 22:121–140.CrossRefGoogle ScholarPubMed
Forster, A., Schouten, S., Baas, M., and Damste, J. S. S. 2007a. Mid-Cretaceous (Albian-Santonian) sea surface temperature record of the tropical Atlantic Ocean. Geology 35:919–922.CrossRefGoogle Scholar
Forster, A., Schouten, S., Moriya, K., Wilson, P. A., and Damste, J. S. S. 2007b. Tropical warming and intermittent cooling during the Cenomanian/Turonian oceanic anoxic event 2: Sea surface temperature records from the equatorial Atlantic. Paleoceanography 22–1:1–14.Google Scholar
Gill, G. A., Santantonio, M., and Lathuiliere, B. 2004. The depth of pelagic deposits in the Tethyan Jurassic and the use of corals: an example from the Apennines. Sedimentary Geology 166:311–334.CrossRefGoogle Scholar
Gradstein, F. M., Ogg, J. G., Schmitz, M. D., and Ogg, G. M., eds. 2012. The geologic time scale 2012. Elsevier, Amsterdam.Google Scholar
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., Knowlton, N., Eakin, C. M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R. H., Dubi, A., and Hatziolos, M. E. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742.CrossRefGoogle ScholarPubMed
Hopkins, M. J., Simpson, C., and Kiessling, W. 2014. Differential niche dynamics among major marine invertebrate clades. Ecology Letters 17:314–323.CrossRefGoogle ScholarPubMed
Houlbrèque, F., and Ferrier-Pagès, C. 2009. Heterotrophy in tropical scleractinian corals. Biological Reviews 84:1–17.CrossRefGoogle ScholarPubMed
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J. B. C., Kleypas, J., Lough, J. M., Marshall, P., Nystrom, M., Palumbi, S. R., Pandolfi, J. M., Rosen, B., and Roughgarden, J. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933.CrossRefGoogle ScholarPubMed
Insalaco, E. 1996. Upper Jurassic microsolenid biostromes of northern and central Europe: facies and depositional environment. Palaeogeography, Palaeoclimatology, Palaeoecology 121:169–194.CrossRefGoogle Scholar
Jablonski, D. 2005. Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution. Journal of Experimental Zoology B 304:504–519.CrossRefGoogle ScholarPubMed
Jablonski, D., and Bottjer, D. J. 1990. Onshore-offshore trends in marine invertebrate evolution. Pp. 21–75in R. M. Ross and W. D. Allmon, eds. Causes of evolution: a paleontological perspective. University of Chicago Press, Chicago.Google Scholar
Jablonski, D., Sepkoski, J. J. Jr., Bottjer, D. J., and Sheehan, P. M. 1983. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222:1123–1125.CrossRefGoogle ScholarPubMed
Jackson, J. B. C., and Buss, L. 1975. Alleopathy and spatial competition among coral reef invertebrates. Proceedings of the National Academy of Sciences USA 72:5160–5163.CrossRefGoogle ScholarPubMed
Jacobs, D. K., and Lindberg, D. R. 1998. Oxygen and evolutionary patterns in the sea: Onshore/offshore trends and recent recruitment of deep-sea faunas. Proceedings of the National Academy of Sciences USA 95:9396–9401.CrossRefGoogle ScholarPubMed
Jenkyns, H. C. 2010. Geochemistry of oceanic anoxic events. Geochemistry Geophysics Geosystems 11. doi: 10.1029/2009GC002788.CrossRefGoogle Scholar
Kiessling, W. 2010. Reef expansion during the Triassic: spread of photosymbiosis balancing climatic cooling. Palaeogeography, Palaeoclimatology, Palaeoecology 290:11–19.CrossRefGoogle Scholar
Kiessling, W., and Aberhan, M. 2007. Environmental determinants of marine benthic biodiversity dynamics through Triassic-Jurassic times. Paleobiology 33:414–434.CrossRefGoogle Scholar
Kiessling, W., and Baron-Szabo, R. 2004. Extinction and recovery patterns of scleractinian corals at the Cretaceous-Tertiary boundary. Palaeogeography, Palaeoclimatology, Palaeoecology 214:195–223.CrossRefGoogle Scholar
Kiessling, W., and Simpson, C. 2011. On the potential for ocean acidification to be a general cause of ancient reef crises. Global Change Biology 17:56–67.CrossRefGoogle Scholar
Kiessling, W., Aragón, E., Scasso, R., Aberhan, M., Kriwet, J., Medina, F., and Fracchia, D. 2005. Massive corals in Paleocene siliciclastic sediments of Chubut (Patagonia, Argentina). Facies 51:233–241.CrossRefGoogle Scholar
Kiessling, W., Aberhan, M., Brenneis, B., and Wagner, P. J. 2007. Extinction trajectories of benthic organisms across the Triassic-Jurassic boundary. Palaeogeography, Palaeoclimatology, Palaeoecology 244:201–222.CrossRefGoogle Scholar
Kiessling, W., Simpson, C., and Foote, M. 2010. Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic. Science 327:196–198.CrossRefGoogle ScholarPubMed
Killick, R., and Eckley, I. A. 2014. changepoint: an R package for changepoint analysis. Journal of Statistical Software 58–3:1–19.Google Scholar
Kitahara, M. V., Cairns, S. D., Stolarski, J., Blair, D., and Miller, D. J. 2010. A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PLoS ONE 5:e11490.CrossRefGoogle ScholarPubMed
Klaus, J. S., Murray, S. T., Swart, P. K., and McNeill, D. F. 2013. Resource partitioning and paleoecology of Neogene free-living corals as determined from skeletal stable isotope composition. Bulletin of Marine Science 89:937–954.CrossRefGoogle Scholar
Kocsis, Á. T., Kiessling, W., and Pálfy, J. 2014. Radiolarian biodiversity dynamics through the Triassic and Jurassic: implications for proximate causes of the end-Triassic mass extinction. Paleobiology 40:625–639.CrossRefGoogle Scholar
Koh, E. G. L., and Sweatman, H. 2000. Chemical warfare among scleractinians: bioactive natural products from Tubastraea faulkneri Wells kill larvae of potential competitors. Journal of Experimental Marine Biology and Ecology 251:141–160.CrossRefGoogle ScholarPubMed
Liow, L. H. 2007. Does versatility as measured by geographic range, bathymetric range and morphological variability contribute to taxon longevity? Global Ecology and Biogeography 16:117–128.Google Scholar
McKinney, M. L., and Oyen, C. W. 1989. Causation and nonrandomness in biological and geological time series: temperature as a proximal control of extinction and diversity. Palaios 4:3–15.CrossRefGoogle Scholar
Muscatine, L., and Porter, J. W. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environment. Bioscience 27:454–460.CrossRefGoogle Scholar
Muscatine, L., Goiran, C., Land, L., Jaubert, J., Cuif, J.-P., and Allemand, D. 2005. Stable isotopes (δ13C and δ15N) of organic matrix from coral skeleton. Proceedings of the National Academy of Sciences USA 102:1525–1530.CrossRefGoogle ScholarPubMed
Pandolfi, J. M., and Kiessling, W. 2014. Gaining insights from past reefs to inform understanding of coral reef response to global climate change. Current Opinion in Environmental Sustainability 7:52–58.CrossRefGoogle Scholar
Peters, S. E., and Loss, D. P. 2012. Storm and fair-weather wave base: a relevant distinction? Geology 40:511–514.CrossRefGoogle Scholar
R Development Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.Google Scholar
Raup, D. M. 1979. Biases in the fossil record of species and genera. Bulletin of the Carnagie Museum of Natural History 13:85–91.Google Scholar
Rex, M. A., Etter, R. J., Morris, J. S., Crouse, J., McClain, C. R., Johnson, N. A., Stuart, C. T., Deming, J. W., Thies, R., and Avery, R. 2006. Global bathymetric patterns of standing stock and body size in the deep-sea benthos. Marine Ecology Progress Series 317:1–8.CrossRefGoogle Scholar
Roberts, J. M., Wheeler, A. J., and Freiwald, A. 2006. Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547.CrossRefGoogle ScholarPubMed
Roder, C., Berumen, M. L., Bouwmeester, J., Papathanassiou, E., Al-Suwailem, A., and Voolstra, C. R. 2013. First biological measurements of deep-sea corals from the Red Sea. Scientific Reports 3:2802. doi:10.1038/srep02802.CrossRefGoogle ScholarPubMed
Rosen, B. R. 2000. Algal symbiosis, and the collapse and recovery of reef communities: Lazarus corals across the K-T boundary. Pp. 164–180in S. J. Culver and P. F. Rawson, eds. Biotic response to global change: the last 145 million years. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Rosen, B. R., Aillud, G.S, Bosellini, F. R., Clarke, N. J., Insalaco, E., Valldeperas, F. X., and Wilson, M. E. J. 2000. Platy coral assemblages: 200 million years of functional stability in response to the limiting effects of light and turbidity. Proceedings of the Ninth International Coral Reef Symposium 1:255–264.Google Scholar
Sepkoski, J. J. Jr. 1991. A model of onshore-offshore change in faunal diversity. Paleobiology 17:58–77.CrossRefGoogle Scholar
Simpson, C. 2013. Species selection and the macroevolution of coral coloniality and photosymbiosis. Evolution 67:1607–1621.CrossRefGoogle ScholarPubMed
Smith, A. B., and Stockley, B. 2005. The geological history of deep-sea colonization by echinoids: roles of surface productivity and deep-water ventilation. Proceedings of the Royal Society of London B 272:865–869.Google ScholarPubMed
Stanley, G. D. Jr. 1981. Early history of scleractinian corals and its geological consequences. Geology 9:507–511.2.0.CO;2>CrossRefGoogle Scholar
Stanley, G. D. Jr., and Cairns, S. D. 1988. Constructional azooxanthellate coral communities; an overview with implications for the fossil records. Palaios 3:233–242.Google Scholar
Stanley, G. D. Jr., and Helmle, K. P. 2010. Middle Triassic coral growth bands and their implication for photosymbiosis. Palaios 25:754–763.CrossRefGoogle Scholar
Stanley, G. D. Jr., and Swart, P. K. 1995. Evolution of the coral-zooxanthellae symbiosis during the Triassic: a geochemical approach. Paleobiology 21:179–199.CrossRefGoogle Scholar
Stolarski, J., Kitahara, M., Miller, D., Cairns, S., Mazur, M., and Meibom, A. 2011. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC. Evolutionary Biology 11:316. doi:10.1186/1471-2148-11-316.Google Scholar
Veron, J. E. N. 1995. Corals in space and time. Cornell University Press, Ithaca, N.Y.Google Scholar
Wellington, G. M., and Trench, R. K. 1985. Persistence and coexistence of a nonsymbiotic coral in open reef environments. Proceedings of the National Academy of Sciences USA 82:2432–2436.CrossRefGoogle ScholarPubMed
Wilson, P. A., and Norris, R. D. 2001. Warm tropical ocean surface and global anoxia during the mid-Cretaceous period. Nature 412:425–429.CrossRefGoogle ScholarPubMed
Wulff, J. 1985. Clonal organisms and the evolution of mutualism. Pp. 437–466in J. B. C. Jackson, L. W. Buss, and R. E. Cook, eds. Population biology and evolution of clonal organisms. Yale University Press, New Haven, Conn.Google Scholar