Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-03T00:46:27.295Z Has data issue: false hasContentIssue false

Morphological optimization in the largest living foraminifera: implications from finite element analysis

Published online by Cambridge University Press:  08 February 2016

Yan Song
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720
R. Gary Black
Affiliation:
Department of Architecture, University of California, Berkeley, California 94720
Jere H. Lipps
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720

Abstract

Benthic foraminifera have attained gigantic sizes many times throughout geologic history. To understand the selective processes underlying foraminiferal gigantism, we used a computer-based, three-dimension, solid finite element model to analyze the mechanical strength of different discoid forms, including two of the largest living foraminifera—Cycloclypeus carpenteri Brady and Marginopora vertebralis Quoy and Gaimard. These two species enlarge by cyclic, planar growth, resulting in slightly biconvex (C. carpenteri) and slightly biconcave (M. vertebralis) forms. As the tests enlarge, the maximum stresses induced by a standard bending moment decrease in both species. Such stress-reducing growth plans apparently allow growth to extraordinarily large sizes and allow volume to increase with minimal lowering of the surface-to-volume ratio, a critical functional factor in ensuring increased surface area for photosynthesis by endosymbionts contained within the tests and for chemical exchange by the foraminifera with the external environment. Of the two species, M. vertebralis has a stronger construction and a lower surface-to-volume ratio. These features indicate optimal constructional solutions to environmental constraints (degree of turbulence and light availability) in their disparate natural habitats: M. vertebralis in the mechanically rigorous inter- to subtidal, and C. carpenteri on the light-minimal and hydraulically quieter, deeper sea beds. We conclude that morphological design in larger foraminifera is constrained by a biomechanical factor, and that gigantism and biomechanical optimization are demonstrably related.

Type
Research Article
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

, A. W. H. 1965. The influence of depth on shell growth in Globigerinoides sacculifer (Brady). Micropaleontology 11:8197.CrossRefGoogle Scholar
, A. W. H. 1980. Gametogenic calcification in a spinose planktonic foraminifer, Globerigerinoides sacculifer (Brady). Marine Micropaleontology 5:283310.CrossRefGoogle Scholar
, A. W. H., and Hemleben, C. 1970. Calcification in a living planktonic foraminifera, Globigerina sacculifer (Brady). Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 134:221234.Google Scholar
, A. W. H., Hemleben, C., Anderson, O. R., and Spindler, M. 1979. Chamber formation in planktonic foraminifera. Micropaleontology 25:294307.CrossRefGoogle Scholar
Brasier, M. 1982. Architecture and evolution of the foraminiferid test—a theoretical approach. Pp. 141in Banner, F. and Lord, A., eds. Aspects of micropalaeontology. Allen and Unwin, London.Google Scholar
Brasier, M. 1986a. Form, function, and evolution in benthic and planktic foraminiferid test architecture. Systematics Association Special Publication 30:252268.Google Scholar
Brasier, M. 1986b. Why do lower plants and animals biomineralize? Paleobiology 12:241250.CrossRefGoogle Scholar
Conger, S., Green, H. W. II, and Lipps, J. H. 1977. Test ultrastructure of some calcareous foraminifera. Journal of Foraminiferal Research 7:278296.CrossRefGoogle Scholar
Drooger, C. W. 1974. The P-Q model combining improved radial growth and size increase as interdependent evolutionary trends in larger foraminifera. Journal of Foraminiferal Research 4:1628.CrossRefGoogle Scholar
Hallock, P. 1979. Trends in test shape with depth in large, symbiont-bearing foraminifera. Journal of Foraminiferal Research 9:6169.CrossRefGoogle Scholar
Hallock, P. 1981. Light dependence in Amphistegina. Journal of Foraminiferal Research 11:4248.CrossRefGoogle Scholar
Hallock, P. 1982. Evolution and extinction in larger foraminifera. Proceedings of the Third North American Paleontological Convention 1:221225.Google Scholar
Hallock, P. 1984. Distribution of selected species of living algal symbiont-bearing foraminifera on two Pacific coral reefs. Journal of Foraminiferal Research 14:250261.CrossRefGoogle Scholar
Hallock, P. 1985. Why are larger foraminifera large? Paleobiology 11:195208.CrossRefGoogle Scholar
Hallock, P. 1988a. Diversification in algal symbiont-bearing foraminifera: a response to oligotrophy? Revue de Paléobiologie, Special Vol. 2, Benthos 86:789797.Google Scholar
Hallock, P. 1988b. Interoceanic differences in foraminifera with symbiotic algae: a result of nutrient supplies? Proceedings of the Sixth International Coral Reef Symposium, Australia, 1988. 3:251255.Google Scholar
Hallock, P., and Glenn, E. C. 1986. Larger foraminifera: a tool for paleoenvironmental analysis of Cenozoic carbonate depositional facies. Palaios 1:5564.CrossRefGoogle Scholar
Hallock, P., and Hansen, H. J. 1979. Depth adaptation in Amphistergina: change in lamellar thickness. Bulletin of the Geological Society of Denmark 27:99104.CrossRefGoogle Scholar
Hallock, P., Forward, L. B., and Hansen, H. J. 1986. Influence of environment on the test shape of Amphistegina. Journal of Foraminiferal Research 16:207215.CrossRefGoogle Scholar
Hallock, P., Röttger, R., and Wetmore, K. 1991. Hypotheses on form and function in foraminifera. Pp. 4172in Lee, J. J. and Anderson, O. R., eds. Biology of the foraminifera. Academic Press, London.Google Scholar
Hansen, H. J. 1970. Electron-microscopical studies on the ultrastructures of some perforate calcitic radiate and granulate foraminifera. Biologiske Meddelelser, Danske Videnskabernes Selskab 17:116.Google Scholar
Hansen, H. J. 1979. Test structure and evolution in the foraminifera. Lethaia 12:173182.CrossRefGoogle Scholar
Hansen, H. J., and Reiss, Z. 1972. Scanning electron microscopy of wall structures in some benthonic and planktonic foraminifera. Revista Española Micropaleontología 4:169179.Google Scholar
Haynes, J. R. 1965. Symbiosis, wall structure and habitat in foraminifera: Contributions from the Cushman Foundation for Foraminiferal Research 16:4043.Google Scholar
Haynes, J. R. 1981. Foraminifera. Wiley, New York.CrossRefGoogle Scholar
Hottinger, L. 1978. Comparative anatomy of elementary shell structures in selected larger Foraminifera. Pp. 203266in Hedley, R. H. and Adams, C. G., eds. Foraminifera, Vol. 3. Academic Press, London.Google Scholar
Hottinger, L. 1981. Fonctions de la disposition alternante des loges chez leσ foraminifères et la structure D'omphalocyclus. Cahiers de Micropaleontologie 4:4555.Google Scholar
Hottinger, L. 1982. Larger foraminifera, giant cells with a historical background. Naturwissenschaften 69:361371.CrossRefGoogle Scholar
Hottinger, L. 1983. Processes determining the distribution of larger foraminifera in space and time. Utrecht Micropaleontological Bulletins 30:239254.Google Scholar
Hottinger, L. 1984. Foraminifères de grand taille: signification des structures complexes de la coquille. Pp. 309315in Oertli, H. J., ed. Benthos '83, Second International Symposium on Benthic Foraminifera. Elf Aquitaine, Esso REP and Total CFP, Pau and Bordeaux.Google Scholar
Hottinger, L. 1986. Construction, structure, and function of foraminifera shells. Pp. 219235in Leadbeater, B. S. C. and Riding, R., eds. Biomineralization in lower plants and animals. Systematics Association Special Publication no. 30, Clarendon Press, New York.Google Scholar
Hottinger, L. 1990. Significance of diversity in shallow benthic foraminifera. Atti del Quarto Simposio di Ecologia e Paleoecologia delle Comunità Bentoniche, Sorrento, Museo Regionale di Scienze Naturali, Torino, p. 3551.Google Scholar
Larsen, A. R. 1976. Studies of Recent Amphistegina: taxonomy and some ecological aspects. Israel Journal of Earth Science 25:126.Google Scholar
Larsen, A. R., and Drooger, C. W. 1977. Relative thickness of the test in Amphistegina species of the Gulf of Elat. Utrecht Micropaleontological Bulletins 15:225239.Google Scholar
Lee, J. J., McEnery, M. E., Kahn, E. G., and Schuster, F. L. 1979. Symbiosis and the evolution of larger foraminifera. Micropaleontology 25:118140.CrossRefGoogle Scholar
Leutenegger, S. 1984. Symbiosis in benthic foraminifera: specificity and host adaptations. Journal of Foraminiferal Research 14:1635.CrossRefGoogle Scholar
Lipps, J. H. 1973. Test structure in foraminifera. Annual Review of Microbiology 27:471488.CrossRefGoogle ScholarPubMed
Loeblich, A. R. Jr., and Tappan, H. 1987. Foraminiferal genera and their classification. Van Nostrand Reinhold, New York.Google Scholar
MacGillavry, H. J. 1978. Foraminifera and parallel evolution: how or why? Geologie en Mijnbouw 57:385394.Google Scholar
Popov, E. P. 1985. Mechanics of materials. Prentice-Hall, Englewood Cliffs, New Jersey.Google Scholar
Reiss, Z., and Hottinger, L. 1984. The Gulf of Aqaba: ecological micropaleontology. Springer, New York.CrossRefGoogle Scholar
Reiss, Z., Leutenegger, S., Hottinger, L., Fermont, W. J. J., Meulenkamp, J. E., Thomas, E., Hansen, H. J., Buchardt, B., Larsen, A. R., and Drooger, C. W. 1977. Depth-relations of Recent larger foraminifera in the Gulf of Aqaba-Elat. Utrecht Micropaleontological Bulletins 15:1244.Google Scholar
Ross, C. A. 1972. Biology and ecology of Marginopora vertebralis (Foraminiferida), Great Barrier Reef. Journal of Protozoology 19:181192.CrossRefGoogle Scholar
Ross, C. A. 1974. Evolutionary and ecological significance of large, calcareous Foraminiferida (Protozoa), Great Barrier Reef. Proceedings of the Second International Coral Reef Symposium 1:327333.Google Scholar
Ross, C. A. 1977. Calcium carbonate fixation by large reef-dwelling foraminifera. American Association of Petroleum Geologists, Studies in Geology 4:219230.Google Scholar
Ross, C. 1979. Ecology of large, shallow-water, tropical foraminifera. Pp. 5459in Lipps, J. H., Berger, W. H., Buzas, M. A., Douglas, R. G., and Ross, C. A.Foraminiferal ecology and paleoecology. Society of Economic Paleontologists and Mineralogists Short Course no. 6, Tulsa, Oklahoma.CrossRefGoogle Scholar
Röttger, R., and Hallock, P. 1982. Shape trends in Heterostegina depressa (Protozoa, Foraminiferida). Journal of Foraminiferal Research 12:197204.CrossRefGoogle Scholar
Seilacher, A. 1979. Constructional morphology of sand dollars. Paleobiology 5:191221.CrossRefGoogle Scholar
Severin, K. 1987. Spatial and temporal variation of Marginopora vertebralis on seagrass in Papua New Guinea during a six week period. Micropaleontology 33:368377.CrossRefGoogle Scholar
Tappan, H., and Loeblich, A. R. Jr. 1988. Foraminiferal evolution, diversification, and extinction. Journal of Paleontology 62:695714.Google Scholar
Tudhope, A. W., and Scoffin, T. P. 1988. The relative importance of benthic foraminiferans in the production of carbonate sediment on the central Queensland shelf. Proceedings of the Sixth International Coral Reef Symposium, Australia 2:583588.Google Scholar
Wainwright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M. 1976. Mechanical design in organisms. Princeton University Press, Princeton.Google Scholar
Wetmore, K. L. 1987. Correlation between test strength, morphology and habitat in some benthic foraminifera from the coast of Washington. Journal of Foraminiferal Research 17:113.CrossRefGoogle Scholar
Wetmore, K. L., and Plotnick, R. E. 1992. Correlations between test morphology, crushing strength, and habitat in Amphistegina gibbosa, Archaias angulatus, and Laevipeneroplis proteus from Bermuda. Journal of Foraminiferal Research 22:112.CrossRefGoogle Scholar
Wilson, E., and Habibullah, A. 1991. SAP, a series of computer programs for the finite element analysis of structures. Computers and Structures Inc., Berkeley.Google Scholar