Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T02:46:44.377Z Has data issue: false hasContentIssue false
  • English
  • Français

Symbiosis as an evolutionary innovation in the radiation of Paleocene planktic foraminifera

Published online by Cambridge University Press:  08 April 2016

Richard D. Norris
Richard D. Norris*
Affiliation:
MS-23, Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543-1541
Get access Rights & Permissions [Opens in a new window]

Abstract

Symbioses are often regarded as an important means for the creation of evolutionary novelty as well as a trigger for the abrupt appearance of higher taxa. The fossil record of foraminifer-algal symbiosis suggests that the appearance of this ecological association contributed to the radiation of Paleogene planktic foraminifera. Isotopic evidence shows that photosymbiosis evolved in synchrony with a major diversification of trochospiral planktic foraminifera about 3.5 m.y. after the end-Cretaceous extinction. In modern planktic foraminifera, photosymbiotic species tend to have more cosmopolitan distributions than asymbiotic foraminifera and a greater ability to withstand periods of nutrient stress. The simultaneous taxonomic radiation and acquisition of photosymbiosis are evidence that the ecological strategy permitted Paleocene foraminifera to expand their niche in pelagic environments by diversifying into low-nutrient surface waters.

A comparison of the species longevities of Neogene and Paleogene symbiotic clades suggests that photosymbiosis does not regulate the characteristic rate of taxonomic turnover in clades after they appear. Species longevities are much shorter in Paleocene and Eocene photosymbiotic morphospecies than they are among photosymbiotic Neogene clades; apparently photosymbiosis does not exert a significant control over long-term evolutionary rates. In addition, the absence of a characteristic morphology associated with photosymbiosis in Cenozoic planktic foraminifera suggests that morphology, as with rate of evolutionary turnover, is linked to symbiosis only because of common inheritance instead of a functional relationship. Although the coincidence between the acquisition of photosymbiosis and generic diversification does suggest a linkage between this ecology and the appearance of foraminiferal higher taxa, there is little indication at the present that symbioses control long-term morphological or ecological patterns within these groups after their appearance. Photosymbiosis, and other evolutionary innovations, may be more a catalyst for the differentiation of major groups than a predictable governor on evolutionary rates.

Type
Articles
Information
Paleobiology , Volume 22 , Issue 4 , Fall 1996 , pp. 461 - 480
Copyright
Copyright © 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

Literature Cited

Ahmadjian, V., and Paracer, S. 1986. Symbiosis: an introduction to biological associations. University Press of New England, Hanover, N.H.Google Scholar
Bé, A. W. H. 1982. Biology of planktonic foraminifera. pp. 51–89In Buzas, M. A., Sen Gupta, B. K., and Broadhead, T. W., eds. Foraminifera—notes for a short course. University of Tennessee, Knoxville.Google Scholar
Bé, A. W. H., Spero, H. J., and Anderson, O. R. 1982. Effects of symbiont elimination and reinfection on the life processes of the planktonic foraminifer Globigerinoides sacculifer. Marine Biology 70:73–86.Google Scholar
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. In press. Phylogeny and taxonomy of Paleocene trochospiral planktic foraminifera. Micropaleontology Special Publication. American Museum of Natural History, New York.Google Scholar
Berggren, W. A., et al. 1994. A Paleocene magnetic, biochronologic and isotopic reference section at DSDP Site 384. EOS 75(16):52.Google Scholar
Berggren, W. A., et al. 1995. A revised Cenozoic geochronology and chronostratigraphy. pp. 129–212In Berggren, W. A., Kent, D. V., Aubry, M.-P., and Hardenbol, J., eds. Geochronology, time scales and global stratigraphic correlations: a unified temporal framework for an historical geology. SEPM, Tulsa, Okla.Google Scholar
Bermudes, D., and Back, R. C. 1991. Symbiosis inferred from the fossil record. pp. 72–94in Margulis and Fester 1991.Google Scholar
Bermudes, D., and Margulis, L. 1987. Symbiont acquisition as neoseme: origin of species and higher taxa. Symbiosis 4:185–198.Google Scholar
Bijma, J. 1991. On the biology of tropical spinose Globigerinidae (Sarcodina, foraminiferida) and its implications for paleoecology. Ph.D. dissertation. Rijksuniversiteit, Groningen, Netherlands.Google Scholar
Boersma, A., and Premoli Silva, I. 1983. Paleocene planktonic foraminiferal biogeography and paleoceanography of the Atlantic Ocean. Micropaleontology 29:355–381.CrossRefGoogle Scholar
Boersma, A., et al. 1979. Carbon and oxygen isotope variations at DSDP Site 384 (North Atlantic) and some paleotemperatures and carbon isotope variations in the Atlantic Ocean. Initial Reports of the Deep Sea Drilling Project 43:695–717.Google Scholar
Bralower, T. J., Zachos, J. C., Thomas, E., Parrow, M., Paull, C. K., Kelly, D. C., Premoli Silva, I., Sliter, W. V., and Lohmann, K. C. 1995. Late Paleocene to Eocene paleoceanography of the equatorial Pacific Ocean: stable isotopes recorded at Ocean Drilling Program Site 865, Allison Guyot. Paleoceanography 10:841–865.CrossRefGoogle Scholar
Brooks, D. R., and McLennan, D. A. 1991. Phylogeny, ecology and behavior. University of Chicago Press, Chicago.Google Scholar
Caron, D., and Swanberg, N. 1990. The ecology of planktonic sarcodines. Aquatic Sciences 3:147–180.Google Scholar
Caron, D. A., Bé, A. W. H., and Anderson, O. R. 1981. Effects of variations in light intensity on life processes of the planktonic foraminifer Globigerinoides sacculifer in laboratory culture. Journal of the Marine Biological Association of the United Kingdom 62:435–451.Google Scholar
Coddington, J. A. 1988. Cladistic tests of adaptational hypotheses. Cladistics 4:3–22.CrossRefGoogle ScholarPubMed
Corfield, R. M., and Cartlidge, J. E. 1991. Isotopic evidence for the depth stratification of fossil and Recent Globigerinina: a review. Historical Biology 5:37–63.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: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 20:391–406.Google Scholar
Douglas, R. G., and Savin, S. M. 1978. Oxygen isotope evidence for the depth stratification of Tertiary and Cretaceous planktic foraminifera. Marine Micropaleontology 3:175–196.Google Scholar
Erez, J., and Honjo, S. 1981. Comparison of isotopic composition of planktonic foraminifera in plankton tows, sediment traps and sediments. Palaeogeography, Palaeoclimatology, Palaeoecology 33:129–156.Google Scholar
Hallock, P., et al. 1991. Hypotheses on form and function in foraminifera. pp. 41–72In Lee, J. J. and Anderson, O. R., eds. Biology of foraminifera. Academic Press, San Diego.Google Scholar
Hemleben, C., Spindler, M., and Anderson, O. R. 1989. Modern planktonic foraminifera. Springer, New York.Google Scholar
Hemleben, C., et al. 1991. Surface texture and the first occurrence of spines in planktonic foraminifera from the early Tertiary. Geologische Jahrbuch A128:117–146.Google Scholar
J⊘ergensen, B. B., et al. 1985. Symbiotic photosynthesis in a planktonic foraminiferan, Globigerinoides sacculifer (Brady), studied with microelectrodes. Limnology and Oceanography 30:1253–1267.CrossRefGoogle Scholar
Kelly, D. C., et al. 1996. Paedomorphosis and the origin of the Paleogene planktonic foraminiferal genus Morozavella. Paleobiology 22:266–281.CrossRefGoogle Scholar
Kendrick, B. 1991. Fungal symbioses and evolutionary innovations. pp. 249–261in Margulis and Fester 1991.Google Scholar
Lauder, G. 1981. Form and function: structural analysis in evolutionary morphology. Paleobiology 7:430–442.Google Scholar
Lee, J. J., and Anderson, O. R. 1991. Symbiosis in foraminifera. pp. 157–220In Lee, J. J. and Anderson, O. R., eds. Biology of foraminifera. Academic Press, San Diego.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
Lewis, D. H. 1991. Mutualistic symbioses in the origin and evolution of land plants. pp. 288–300in Margulis and Fester 1991.Google Scholar
Lohmann, G. P. 1995. A model for variation in the chemistry of planktonic foraminifera due to secondary calcification and selective dissolution. Paleoceanography 10:445–457.CrossRefGoogle Scholar
Margulis, L., and Fester, R. 1991. Symbiosis as a source of evolutionary innovation. MIT Press, Cambridge.Google Scholar
McConnaughy, T. 1989. 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. 1991. Biased extinction and evolutionary trends. Paleobiology 17:388–399.CrossRefGoogle Scholar
Norris, R. D. 1992. Extinction selectivity and ecology in planktonic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology 95:1–17.CrossRefGoogle Scholar
Oppo, D. W., and Fairbanks, R. G. 1989. Carbon isotope composition of tropical surface water during the past 22,000 years. Paleoceanography 4:333–351.CrossRefGoogle Scholar
Pearson, P. N. 1993. A lineage phylogeny for the Paleogene planktonic foraminifera. Micropaleontology 39:193–232.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.Google Scholar
Ravelo, A., and Fairbanks, R. 1992. Oxygen isotopic composition of multiple species of planktonic foraminifera: recorders of the modern photic zone temperature gradient. Paleoceanography 7:815–831.CrossRefGoogle Scholar
Ravelo, A., and Fairbanks, R. 1995. Carbon isotopic fractionation in multiple species of planktonic foraminifera from core-tops in the tropical Atlantic. Journal of Foraminiferal Research 25:53–74.Google Scholar
Schweitzer, P. N. 1990. Inference of eoclogy from the ontogeny of microfossils. Ph.D. dissertation. Geology and Geophysics, MIT-WHOI Joint Program, Boston.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 σ 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. J., and Lea, D. W. 1993. Intraspecific stable isotope variability in the planktonic foraminifer Globigerinoides sacculifer: results for laboratory experiments. Marine Micropaleontology 22:193–232.Google Scholar
Spero, H. J., and Parker, S. L. 1985. Photosymbiosis in the symbiotic planktonic foraminifer Orbulina universa, and its potential ontribution to oceanic primary productivity. Journal of Foraminiferal Research 15:273–281.CrossRefGoogle 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
Swofford, D., and Begle, D. 1993. PAUP—Phylogenetic Analysis Using Parsimony 3.1. Center for Biodiversity, Illinois Natural History Survey, Champaign.Google Scholar
Tourmarkine, M., and Luterbacher, H. 1985. Palocene and Eocene planktic foraminifera. pp. 87–154In Bolli, H. M., Saunders, J. B., and Perch-Nielsen, K., eds. Plankton stratigraphy. Cambridge University Press, Cambridge.Google Scholar
Turner, J. V. 1982. Kinetic fractionation of 13C during calcium carbonate precipitation. Geochimica et Cosmochimica Acta 46:1183–1191.Google Scholar
van Eijden, A. J. M. 1995. Morphology and relative frequency of planktic foraminiferal species in relation to oxygen isotopically inferred depth habitats. Palaeogeography, Palaeoclimatology, Palaeoecology 113:267–301.Google Scholar