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Recognition and Macroevolutionary Significance of Photosymbiosis in Molluscs, Corals, and Foraminifera

Published online by Cambridge University Press:  21 July 2017

Richard D. Norris
Richard D. Norris*
Affiliation:
MS-23, Woods Hole Oceanographic Institution, Woods Hole, MA 02543-1541, USA
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Extract

Symbiotic relationships are common between algae and diverse lineages of corals, planktic foraminifera, benthic foraminifera, and bivalves as well as in many other groups that do not leave an extensive fossil record. Ancient photosymbioses can be inferred using various lines of inference including the morphology of the host, its habitat, rates of calcification, (which tend to be high in many photosymbiotic taxa), and the geochemistry of the host's shell. This survey shows that stable isotopes are reliable means of identification of photosymbioses in corals and planktic foraminifera, but are far less reliable in benthic foraminifera and bivalves. Organisms that increase their symbiont density proportionate to their own growth display a steep rise in shell δ13C, while organisms whose own growth exceeds that of their symbiont population display a far smaller effect on shell δ13C.

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Research Article
Information
The Paleontological Society Papers , Volume 4: Isotope Paleobiology and Paleoecology , October 1998 , pp. 68 - 100
Copyright
Copyright © 1998 by The Paleontological Society 

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References

Berger, W.H., Killingly, J.S., and Vincent, E. 1978. Stable isotopes in deep sea carbonates: box core ERDC-92, west equatorial Pacific. Oceanologica Acta 1:203–216.Google Scholar
Berggren, W.A., and Norris, R.D. 1997. Biostratigraphy, phylogeny and systematics of Paleocene trochospiral planktic foraminifera. Micropaleontology, Supplement 43 (1):1–166.Google Scholar
Bermudes, D., and Back, R.C. 1991. Symbiosis inferred from the fossil record. p. 72–94 in Margulis, L. and Fester, R., (eds.), Symbiosis as a Source of Evolutionary Innovation. MIT Press, Cambridge, Mass. Google Scholar
Bermudes, D., and Margulis, L. 1987. Symbiont acquisition as neoseme: origin of species and higher taxa. Symbiosis 4:185–198.Google Scholar
Buchardt, B., and Hansen, H. J. 1977. Oxygen isotope fractionation and algal symbiosis in benthic foraminifera from the Gulf of Elat, Israel. Bulletin of the Geological Society of Denmark 26:185–194.Google Scholar
Caron, D., and Swanberg, N. 1990. The ecology of planktonic sarcodines. Aquatic Sciences 3:147–180.Google Scholar
Coates, A. G., and Jackson, J. B. C. 1987. Clonal growth, algal symbiosis, and reef formation by corals. Paleobiology 13 (4):363–378.Google Scholar
Cohen, A. L., and Hart, S. R. 1997. The effect of colony topography on climate signals in coral skeleton. Geochimica et Cosmochimica Acta 61 (18):3905–3912.Google Scholar
Cowen, R. 1983. Algal symbiosis and its recognition in the fossil record. p. 431–478 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 (2):221–227.Google Scholar
D'Hondt, S., and Donaghay, P. 1995. Carbon isotopic recovery from mass extinctions: no strangelove oceans on geologic timescales? Geological Society of America Abstracts with Programs 27 (6):A-164.Google Scholar
D'Hondt, S., and Zachos, J. C. 1993. On stable isotopic variation and earliest Paleocene planktonic foraminifera. Paleoceanography 8:527–547.Google Scholar
D'Hondt, S., and Zachos, J. C. 1995. 75 million years of photosymbiosis in planktic foraminifera. Geological Society of America Abstracts with Programs 27 (6):A-244.Google Scholar
D'Hondt, S., Zachos, J. C., and Schultz, G. 1994. Stable Isotopic signals and photosymbiosis in Late Paleocene planktic foraminifera. Paleobiology 20 (3):391–406.Google Scholar
Erez, J. 1978. Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273:199–102.Google Scholar
Fairbanks, R. G., and Dodge, R. E. 1979. Annual periodicity of the 18O/16O and 13C/12C ratios in the coral Montastrea annularis . Geochimica et Cosmochimica Acta 43:1009–1020.Google Scholar
Gagan, M. K., Chivas, A. R., and Isdale, P. J. 1996. Timing coral-based climatic histories using 13C enrichments driven by synchronized spawning. Geology 24 (11):1009–1012.2.3.CO;2>CrossRefGoogle Scholar
Gasperi, J. T., and Kennett, J. P. 1992. Isotopic evidence for depth stratification and paleoecology of Miocene planktonic foraminifera: western equatorial Pacific DSDP Site 289. Pp. 117–150 in Tsuchi, R. and Ingle, J. C. Jr., (eds.), Pacific Neogene environment, evolution and events. University of Tokyo Press, Tokyo.Google Scholar
Gast, R. J., and Caron, D. A. 1996. Molecular phylogeny of symbiotic dinoflagellates from planktonic foraminifera and radiolaria. Molecular Biology and Evolution 13 (9): 1192–1197.Google Scholar
Hallock, P. 1985. Why are larger Foraminifera large? Paleobiology 11 (2): 195–208.Google Scholar
Hemleben, C., Spindler, M., and Anderson, O.R. 1989. Modern Planktonic Foraminifera. Springer-Verlag, New York.Google Scholar
Houston, R. M., and Huber, B. T. (in press). Evidence of photosymbiosis in fossil taxa? Ontogenetic stable isotope trends in some late Cretaceous planktonic foraminifera. Marine Micropaleontology: 1–18.Google Scholar
Houston, R. M., Huber, B. T., and Spero, H. J. 1997. Evidence of photosymbiosis in fossil taxa? Ontogenetic stable isotope analysis of late Cretaceous planktonic foraminifera. Geological Society of America Abstracts with Programs 29 (6):A-160.Google Scholar
Huber, B. T., Bijma, J., and Darling, K. 1997. Cryptic speciation in the living planktonic foraminifer Globigerinoides siphonifera (d'Orbigny). Paleobiology 23 (1):33–62.Google Scholar
Jones, D. S., and Jacobs, D. K. 1992. Photosymbiosis in Clinocardium nuttalli: implications for tests of photosymbiosis in fossil molluscs. Palaios 7 (1):86–95.Google Scholar
Jones, D. S., Williams, D. F., and Romanek, C. S. 1986. Life History of symbiont-bearing giant clams from stable isotope profiles. Science 231:46–48.Google Scholar
Kelly, D. C., Arnold, A. J., and Parker, W. C. 1996. Paedomorphosis and the origin of the Paleogene planktonic foraminiferal genus Morozovella . Paleobiology 22 (2):266–281.Google Scholar
Kendrick, B. 1991. Fungal symbioses and evolutionary innovations. p. 249–261 in Margulis, L. and Fester, R., (eds.), Symbiosis as a Source of Evolutionary Innovation. MIT Press, Cambridge, Mass. Google Scholar
Krantz, D. E., Williams, D. F., and Jones, D. S. 1987. Ecological and paleoenvironmental information using stable isotope profiles from living and fossil molluscs. Palaeogeography, Palaeoclimatology, Palaeoecology 58:249–266.Google Scholar
Land, L. S., Lang, J. C., and Smith, B. N. 1975. Preliminary observations on the carbon isotopic composition of some reef coral tissues and symbiotic zooxanthellae. Limnology and Oceanography 20:283–287.Google Scholar
Langer, M. R. 1995. Oxygen and carbon isotopic composition of Recent larger and smaller foraminifera from the Madang Lagoon (Papua New Guinea). Marine Micropaleontology 26:215–221.Google Scholar
Leder, J. J., et al. 1996. The origin of variations in the isotopic record of scleractinian corals: I. oxygen. Geochimica et Cosmochimica Acta 60 (15):2857–2870.Google Scholar
Lee, J. J., and Anderson, O. R. 1991. Symbiosis in foraminifera. p. 157–220 in Lee, J. J. and Anderson, O. R., (eds.), Biology of Foraminifera. Academic Press, San Diego, CA.Google Scholar
Lee, J. J., and Hallock, P. 1987. Algal symbiosis as a driving force in the evolution of larger foraminifera. Annals of the New York Academy of Sciences 503:330–347.Google Scholar
Lohmann, G.P. 1995. A model for variation in the chemistry of planktonic foraminifera due to secondary calcification and selective dissolution. Paleoceanography 10 (3):445–457.Google Scholar
Margulis, L. 1976. Genetic and evolutionary consequences of symbiosis. Experimental Parasitology 39:277–349.Google Scholar
Margulis, L., and Fester, R., (eds.). 1991. Symbiosis as a Source of Evolutionary Innovation. The MIT Press, Cambridge, Mass. Google Scholar
McConnaughey, T. 1989a. 13C and 18O isotopic disequilibrium in biological carbonates: I. Patterns. Geochimica et Cosmochimica Acta 53:151–162.Google Scholar
McConnaughey, T. 1989b. 13C and 18O isotopic disequilibrium in biological carbonates: II. In vitro simulation of kinetic isotopic effects. Geochimica et Cosmochimica Acta 53:163–171.Google Scholar
Norris, R. D. 1996a. Macroevolutionary origins of photosymbiosis in planktic foraminifera. Geological Society of America Abstracts with Programs 28 (7):A-484.Google Scholar
Norris, R. D. 1996b. Symbiosis as an evolutionary innovation in the radiation of Paleocene planktic foraminifera. Paleobiology 22 (4):461–480.Google Scholar
Norris, R. D. 1996c. Symbiosis as an evolutionary innovation in the radiation of planktic foraminifera. Paleontological Society Special Publication 8:291.Google Scholar
Norris, R. D. in press. Miocene-Pliocene surface water hydrography of the eastern equatorial Atlantic. Reports of the Ocean Drilling Program, Scientific Results 159.Google Scholar
Norris, R.D., Corfield, R.M., and Cartlidge, J.E. 1996. What is gradualism? Cryptic speciation in gradually-evolving globorotaliid planktic foraminifera. Paleobiology 22 (3):386–405.Google Scholar
Norris, R. D., and Wilson, P. A. (in press). Low-latitude sea-surface temperatures for the mid-Cretaceous and the evolution of planktic foraminifera. Geology.Google Scholar
Ortiz, J. D., et al. 1996. Deep-dwelling planktonic foraminifera of the northeastern Pacific Ocean reveal environmental control of oxygen and carbon isotopic disequilibria. Geochimica et Cosmochimica Acta 60 (22):4509–4523.Google Scholar
Pearson, P.N., Shackleton, N.J., and Hall, M. 1993. Stable isotope paleoecology of middle Eocene planktonic foraminifera and multispecies isotope stratigraphy, DSDP Site 523, South Atlantic. Journal of Foraminiferal Research 23:123–140.CrossRefGoogle Scholar
Ravelo, A., and Fairbanks, R. G. 1992. Oxygen isotopic composition of multiple species of planktonic foraminifera: recorders of the modern photic zone temperature gradient. Paleoceanography 7:815–831.Google Scholar
Ravelo, A.C., and Fairbanks, R.G. 1995. Carbon isotopic fractionation in multiple species of planktonic foraminifera from core-tops in the tropical Atlantic. Journal of Foraminiferal Research 25 (1):53–74.Google Scholar
Romanek, C. S., and Grossman, E. L. 1989. Stable isotope profiles of Tridacna maxima as environmental indicators. Palaios 4 (5):402–413.Google Scholar
Schweitzer, P.N., and Lohmann, G.P. 1991. Ontogeny and habitat of modern menardiiform planktonic foraminifera. Journal of Foraminiferal Research 21:332–346.Google Scholar
Shackleton, N. J., Corfield, R.M., and Hall, M.A. 1985. Stable isotope data and the ontogeny of Paleocene planktonic foraminifera. Journal of Foraminiferal Research 15:321–336.Google Scholar
Smith, D.C., and Douglas, A.E. 1987. The Biology of Symbiosis. Edward Arnold, London.Google Scholar
Spero, H.J. 1992. Do planktonic foraminifera accurately record shifts in the carbon isotopic composition of seawater δ13C∑CO2? Marine Micropaleontology 19:275–285.Google Scholar
Spero, H.J., and DeNiro, M.J. 1987. The influence of symbiont photosynthesis on the δ18O and δ13C values of planktonic foraminiferal shell calcite. Symbiosis 4:213–228.Google Scholar
Spero, H., and Lea, D. 1993. Does the carbon isotopic composition of planktonic foraminifera prey affect shell δ13C values? EOS, Transactions of the American Geophysical Union 74:183.Google Scholar
Spero, H. J., and Lea, D. W. 1995. Experimental determination of stable isotope variability in Globigerina bulloides: implications for paleoceanographic reconstructions. Marine Micropaleontology 28:231–246.Google Scholar
Spero, H.J., Lerche, I., and Williams, D.F. 1991. Opening the carbon isotope “vital effect” black box, 2 quantitative model for interpreting foraminiferal carbon isotope data. Paleoceanography 6:639–655.Google Scholar
Spero, H.J., and Parker, S.L. 1985. Photosymbiosis in the symbiotic planktonic foraminifer Orbulina universa, and its potential contribution to oceanic primary productivity. Journal of Foraminiferal Research 15:273–281.Google Scholar
Stanley, G. D., and Swart, P. K. 1995. Evolution of the coral-zooxanthellae symbiosis during the Triassic: a geochemical approach. Paleobiology 21 (2): 179–199.Google Scholar
Steuber, T. 1996. Stable isotope sclerochonology of rudist bivalves: growth rates and late Cretaceous seasonality. Geology 24 (4):315–318.Google Scholar
Swart, P. K. 1983. Carbon and oxygen isotope fractionation in scleractinian corals: a review. Earth-Science Reviews 19:51–80.Google Scholar
Swart, P. K., Dodge, R. E., and Hudson, H. J. 1996a. A 240-year stable oxygen and carbon isotopic record in a coral from South Florida: implications for the prediction of precipitation in southern Florida. Palaios 1 (4):362–375.Google Scholar
Swart, P. K., Dodge, R. E., and Hudson, H. J. 1996b. A 240-year stable oxygen and carbon isotopic record in a coral from South Florida: implications for the prediction of precipitation in southern Florida. Palaios 11 (4):362–375.Google Scholar
Swart, P. K., et al. 1996c. The origin of variations in the isotopic record of scleractinian corals: II. Carbon. Geochimica et Cosmochimica Acta 60 (15):2871–2885.Google Scholar
ter Kuile, B. 1991. Mechanisms for calcification and carbon cycling in algal symbiont-bearing foraminifera. p. 73–89 in Lee, J. J. and Anderson, O. R., (eds.), Biology of Foraminifera. Academic Press, London.Google Scholar
ter Kuile, B., and Erez, J. 1987. Uptake of inorganic carbon and internal carbon cycling in benthonic symbiont-bearing foraminifera. Marine Biology 94:499–510.Google Scholar
Vinot-Berthouille, A.-C, and Duplessy, J. C. 1973. Individual isotopic fractionation of carbon and oxygen in benthic foraminifera. Earth and Planetary Science Letters 18:247–252.Google Scholar
Vogel, K. 1975. Endosymbiotic algae in rudists? Palaeogeography, Palaoeclimatology, Palaeoecology 17:327–332.Google Scholar
Watson, M. E., and Signor, P. W. 1986. How a clam builds windows: shell microstructure in Corculum (Bivalvia: Cardiidae). Veliger 28:348–355.Google Scholar
Wefer, G., and Berger, W. H. 1980. Stable isotopes in benthic foraminifera: seasonal variation in large tropical species. Science 209:803–805.Google Scholar
Wefer, G., and Berger, W. H. 1991. Isotope paleontology: growth and composition of extant calcareous species. Marine Geology 100:207–248.Google Scholar
Wefer, G., Killingley, J. S., and Lutze, G. F. 1981. Stable isotopes in recent larger Foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology 33:253–270.Google Scholar