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Ecological, taxonomic, and taphonomic components of the post-Paleozoic increase in sample-level species diversity of marine benthos

  • Michał Kowalewski (a1), Susan L. Barbour Wood (a1), Wolfgang Kiessling (a2), Martin Aberhan (a2), Franz T. Fürsich (a3), Daniele Scarponi (a4) and Alan P. Hoffmeister (a5)...


Biological veracity of the sharp diversity increase observed in many analyses of the post-Paleozoic marine fossil record has been debated vigorously in recent years. To assess this question for sample-level (“alpha”) diversity, we used bulk samples of shelly invertebrates, representing three major fossil groups (brachiopods, bivalves, and gastropods), to compare the Jurassic and late Cenozoic sample-level diversity of marine benthos. After restricting the data set to single-bed, whole-fauna, bulk samples (n ≥ 30 specimens) from comparable open marine siliciclastic facies, we were able to retain 427 samples (255 Jurassic and 172 late Cenozoic), with most of those samples originating from our own empirical work.

Regardless of the diversity metric applied, the initial results suggest that standardized sample-level species (or genus) diversity, driven by evenness and/or richness of the most common taxa, increased between the Jurassic and late Cenozoic by at least a factor of 1.6. When the data are partitioned into the three dominant higher taxa, it becomes clear that (1) the bivalves, which dominated the samples for both time intervals, increased in sample-level diversity between the Jurassic and the late Cenozoic by a much smaller factor than the total fauna; (2) the removal of brachiopods, which were a noticeable component of the Jurassic samples, did not significantly affect standardized sample-level diversity estimates; and (3) the gastropods, which were rare in the Jurassic but common in many late Cenozoic samples, contributed notably to the increase in sample-level diversity observed between the two time intervals. Parallel to these changes, the samples revealed secular trends in ecological structure, including Jurassic to late Cenozoic increases in proportion of (1) infauna, (2) mobile forms, and (3) non-suspension-feeding organisms. These trends mostly persist when data are restricted to bivalves.

Supplementary analyses indicate that these patterns cannot be attributed to sampling heterogeneities in paleolatitudinal range, lithology, or paleoenvironment of deposition. Likewise, when data are restricted to samples dominated by species with originally aragonitic shells, the observed temporal changes persist at a comparable magnitude, suggesting that the pervasive loss of aragonite in the older fossil record is unlikely to have been the primary cause of the observed patterns. The comparable ratio of identified to unidentified species and genera, observed when comparing the Jurassic and late Cenozoic samples, indicates that the relatively poorer (mold/cast) preservation of Jurassic aragonite species also is unlikely to have been responsible for the observed patterns. However, the diagenesis-related taphonomic and methodological artifacts cannot be ruled out as an at least partial contributor to the observed post-Paleozoic changes in diversity, taxonomic composition, and ecology (the outcomes of the three tests of the diagenetic bias available to us are incongruent).

The study demonstrates that the post-Paleozoic trends in the sample-level diversity, ecology, and taxonomic structure of common taxa can be replicated across multiple studies. However, the diversity increase estimated here is much less prominent than suggested by many previous analyses. The results also narrow the list of causative explanations down to two testable hypotheses. The first is diagenetic bias—a spurious trend driven by either (a) increasing taphonomic loss of small specimens in the older fossil record or (b) a shift in sampling procedures between predominantly lithified rocks of the Mesozoic and predominately unlithified, and therefore sievable, sediments of the late Cenozoic. The second hypothesis is genuine biological changes—macroevolutionary trends in the structure of marine benthic associations through time, consistent with predictions of several related models such as evolutionary escalation, increased ecospace utilization, and the Mesozoic marine revolution. Future studies should focus on testing these two rival models, a key remaining challenge for identifying the primary causative mechanism for the long-term changes in sample-level diversity, ecology, and taxonomic structure observed in the Phanerozoic marine fossil record.



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Aberhan, M. 1993. Benthic macroinvertebrate associations on a carbonate-clastic ramp in segments of the Early Jurassic backarc basin of northern Chile (26–29°S). Revista Geológica de Chile 20:105136.
Aberhan, M. 1994. Guild-structure and evolution of Mesozoic benthic shelf communities. Palaios 9:516545.
Aberhan, M. 1998. Early Jurassic Bivalvia of western Canada. Part I. Subclasses Palaeotaxodonta, Pteriomorphia, and Isofilibranchia. Beringeria 21:57150.
Aberhan, M., and Fürsich, F. T. 1991. Paleoecology and paleoenvironments of the Pleistocene deposits of Bahía la Choya (Gulf of California, Sonora, Mexico). Zitteliana 18:135163.
Aberhan, M., Kiessling, W., and Fürsich, F. T. 2006. Testing the role of biological interactions for the evolution in mid-Mesozoic marine benthic ecosystems. Paleobiology 32:259277.
Alroy, J., and Hendy, A. J. W. 2005. Did alpha diversity triple between the Paleozoic and Cenozoic? Geological Society of America Abstracts with Programs 37(7):117.
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fürsich, F. T., Hansen, T. A., Holland, S. M., Ivany, L. C., Jablonski, D., Jacobs, D. K., Jones, D. C., Kosnik, M. A., Lidgard, S., Low, S., Miller, A. I., Novack-Gottshall, P. M., Olszewski, T. D., Patzkowsky, M. E., Raup, D. M., Roy, K., Sepkoski, J. J., Sommers, M. G., Wagner, P. J., and Webber, A. 2001. Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proceedings of the National Academy of Sciences USA 98:62616266.
Ausich, W. I., and Bottjer, D. J. 1982. Tiering in suspension-feeding communities on soft substrata throughout the Phanerozoic. Science 216:173174.
Bambach, R. K. 1977. Species richness in marine benthic habitats through the Phanerozoic. Paleobiology 3:152167.
Bambach, R. K. 1983. Ecospace utilization and guilds in marine communities through the Phanerozoic. Pp. 719746 (Chapter 15) in Tevesz, M. and McCall, P., eds. Biotic interactions in recent and fossil benthic communities. Plenum, New York.
Bambach, R. K. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiology 19:372397.
Bambach, R. K. 1999. Energetics in the global marine fauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios 32:131144.
Bambach, R. K., Knoll, A. H., and Wang, S. C. 2004. Origination, extinction, and mass depletions of marine diversity. Paleobiology 30:522542.
Benton, M. J. 1995. Diversification and extinction in the history of life. Science 268:5258.
Bush, A. M., and Bambach, R. K. 2004. Did alpha diversity increase during the Phanerozoic? Lifting the veil of taphonomic, latitudinal, and environmental biases in the study of paleocommunities. Journal of Geology 112:625642.
Bush, A. M., Markey, M. J., and Marshall, C. R. 2004. Alpha, beta, gamma: the effects of spatially organized biodiversity on sampling-standardization. Paleobiology 30:666686.
Cherns, L., and Wright, V. P. 2000. Missing molluscs as evidence of large-scale, early skeletal aragonite dissolution in a Silurian sea. Geology 28:791794.
Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 199:13021310.
Cooper, R. A., Maxwell, P. A., Crampton, J. S., Beu, A. G., Jones, C. M., and Marshall, B. A. 2006. Completeness of the fossil record: estimating losses due to small body size. Geology 34:241244.
Efron, B. 1981. Nonparametric standard errors and confidence intervals. Canadian Journal of Statistics 9:139172.
Finnegan, S., and Droser, M. L. 2005. Relative and absolute abundance of trilobites and rhynchonelliform brachiopods across the Lower/Middle Ordovician boundary, eastern Basin and Range. Paleobiology 31:480502.
Fürsich, F. T. 1977. Corallian (Upper Jurassic) marine benthic associations from England and Normandy. Palaeontology 20:337385.
Fürsich, F. T., and Wendt, J. 1977. Biostratinomy and palaeoecology of the Cassian Formation (Triassic) of the Southern Alps. Palaeogeography, Palaeoclimatology, Palaeoecology 22:257323.
Gradstein, F. M., Ogg, J. G., Smith, A. G., Bleeker, W., and Lourens, L. J. 2004. A new geologic time scale, with special reference to Precambrian and Neogene. Episodes 27:83100.
Hall, P. 1992. Efficient bootstrap simulations. Pp. 127143 in Lepage, R. and Billard, L. L., eds. Exploring the limits of bootstrap. Wiley, New York.
Hendy, A. J. W. 2005. Lithification and the measurement of biodiversity—is missing alpha stuck between a rock and a hard place? Geological Society of America Abstracts with Programs 37(7):117.
Hoffmeister, A. P., and Kowalewski, M. 2001. Spatial and environmental variation in the fossil record of drilling predation: a case study from the Miocene of Central Europe. Palaios 16:566579.
Hubalek, Z. 2000. Measures of species diversity in ecology: an evaluation. Folia Zoologica 49:241260.
Jablonski, D. J., Roy, K., Valentine, J. W., Price, R. M., and Anderson, P. S. 2003. The impact of the Pull of the Recent on the history of marine diversity. Science 300:11331135.
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 95:93969401.
Kidwell, S. M. 2001. Preservation of species abundance in marine death assemblages. Science 294:10911094.
Kidwell, S. M. 2005. Shell composition has no net impact on large-scale evolutionary patterns in molluscs. Science 307:914917.
Kidwell, S. M., and Brenchley, P. J. 2004. Patterns in bioclastic accumulations through the Phanerozoic: changes in input or in destruction? Geology 22:11391143.
Kiessling, W. 2002. Radiolarian diversity patterns in the latest Jurassic-earliest Cretaceous. Palaeogeography, Palaeoclimatology, Palaeoecology 187:179206.
Kiessling, W. 2005. Long-term relationships between ecological stability and biodiversity in Phanerozoic reefs. Nature 433:410413.
Kittl, E. 1891. Die Gastropoden der Schichten von St. Cassian der südalpinen Trias. Annalen des Kaiserlich-Königlichen Naturhistorischen Hofmuseums 6:166262.
Kosnik, M. A. 2005. Changes in Late Cretaceous–early Tertiary benthic marine assemblages: analyses from the North American coastal plain shallow shelf. Paleobiology 31:459479.
Kowalewski, M., and Bambach, R. K. 2003. The limits of paleontological resolution. In Harries, P. J., ed. High-resolution approaches in stratigraphic paleontology. Topics in Geobiology 21:148. Plenum/Kluwer Academic, New York.
Kowalewski, M., and Hoffmeister, A. P. 2003. Sieves and fossils: effects of mesh size on paleontological patterns. Palaios 18:460469.
Kowalewski, M., Goodfriend, G. A., and Flessa, K. W. 1998. The high-resolution estimates of temporal mixing in shell beds: the evils and virtues of time-averaging. Paleobiology 24:287304.
Kowalewski, M., Gürs, K., Nebelsick, J. H., Oschmann, W., Piller, W. E., and Hoffmeister, A. P. 2002. Multivariate hierarchical analyses of Miocene mollusk assemblages of Europe: paleogeographic, paleoecological, and biostratigraphic implications. Geological Society of America Bulletin 114:239256.
Kowalewski, M., Hoffmeister, A. P., Baumiller, T. K., and Bambach, R. K. 2005. Secondary evolutionary escalation between brachiopods and enemies of other prey. Science 308:17741777.
Krebs, C. J. 1999. Ecological methodology. Addison-Wesley, Menlo Park, Calif.
Magurran, A. E. 1998. Ecological diversity and its measurement. Princeton University Press, Princeton, NJ.
Magurran, A. E. 2004. Measuring biological diversity. Blackwell, London.
May, R. M. 1976. Patterns of species abundance and diversity. Pp. 81120 in Cody, M. L. and Diamond, J. M., eds. Ecology and evolution of communities. Harvard University Press, Cambridge.
Newell, N. D. 1959. Adequacy of the fossil record. Journal of Paleontology 33:488499.
Olszewski, T. D. 2004. A unified mathematical framework for the measurement of richness and evenness within and among multiple communities. Oikos 104:377387.
Peters, S. E. 2004. Evenness in Cambrian–Ordovician benthic marine communities in North America. Paleobiology 30:325346.
Peters, S. E., and Foote, M. 2001. Biodiversity in the Phanerozoic: a reinterpretation. Paleobiology 27:583601.
Powell, M. G., and Kowalewski, M. 2002. Increase in evenness and sampled alpha diversity through the Phanerozoic: comparison of early Paleozoic and Cenozoic marine fossil assemblages. Geology 30:331334.
Raup, D. M. 1972. Taxonomic diversity during the Phanerozoic. Science 177:10651071.
Raup, D. M. 1976. Species diversity in the Phanerozoic: an interpretation. Paleobiology 2:289297.
Sageman, B. B., and Bina, C. R. 1997. Diversity and species abundance patterns in Late Cenomanian Black Shales Biofacies, Western Interior, USA. Palaios 12:449466.
Scarponi, D., and Kowalewski, M. 2004. Stratigraphic paleoecology: bathymetric signatures and sequence overprint of mollusk associations from the upper Quaternary sequences of the Po Plain, Italy. Geology 32:989992.
Scarponi, D., and Kowalewski, M. In press. Sequence stratigraphic anatomy of diversity patterns: late Quaternary benthic mollusks of Po Plain, Italy. Palaios.
Scherer, M. 1977. Preservation, alteration and multiple cementation of aragonitic skeletons from the Cassian Beds (U. Triassic, southern Alps): petrographic and geochemical evidence. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 154:213262.
Sepkoski, J. J. Jr. 1981. A factor analytic description of the Phanerozoic marine fossil record. Paleobiology 7:3653.
Sepkoski, J. J. Jr., Bambach, R. K., Raup, D. M., and Valentine, J. W. 1981. Phanerozoic marine diversity: a strong signal from the fossil record. Nature 293:435437.
Smith, B., and Wilson, J. B. 1996. A consumer's guide to evenness indices. Oikos 76:7082.
Sohl, N. F. 1987. Cretaceous gastropods: contrasts between Tethys and the temperate provinces. Journal of Paleontology 61:10851111.
Stanley, S. M. 1968. Post-Paleozoic adaptive radiation of infaunal bivalve molluscs; a consequence of mantle fusion and siphon formation. Journal of Paleontology 42:214229.
Stanley, S. M. 1977. Trends, rates, and patterns of evolution in the Bivalvia. Pp. 209250 in Hallam, A., ed. Patterns of evolution as illustrated by the fossil record. Elsevier, New York.
Taylor, J. D., Morris, N. J., and Taylor, C. N. 1980. Food specialization and the evolution of predatory prosobranch gastropods. Palaeontology 23:375409.
Thayer, C. W. 1983. Sediment-mediated biological disturbance and the evolution of marine benthos. Pp. 479625 in Tevesz, M. J. S. and McCall, P. L., eds. Biotic interactions in Recent and fossil benthic communities. Plenum, New York.
Tilman, D., Polasky, S., and Lehman, C. 2005. Diversity, productivity and temporal stability in the economies of humans and nature. Journal of Environmental Economics and Management 49:405426.
Valentine, J. W. 1969. Patterns of taxonomic and ecological structure of the shelf benthos during Phanerozoic time. Palaeontology 12:684709.
Vermeij, G. J. 1977. The Mesozoic marine revolution: the evidence from snails, predators, and grazers. Paleobiology 3:245258.
Vermeij, G. J. 1987. Evolution and escalation; an ecological history of life. Princeton University Press, Princeton, NJ.
Vermeij, G. J. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21:125152.
Washington, H. G. 1984. Diversity, biotic and similarity indices: a review with special relevance to aquatic ecosystems. Water Resources 18:653694.
Wright, P., Cherns, L., and Hodges, P. 2003. Missing molluscs: field testing taphonomic loss in the Mesozoic through early large-scale aragonite dissolution. Geology 31:211214.

Ecological, taxonomic, and taphonomic components of the post-Paleozoic increase in sample-level species diversity of marine benthos

  • Michał Kowalewski (a1), Susan L. Barbour Wood (a1), Wolfgang Kiessling (a2), Martin Aberhan (a2), Franz T. Fürsich (a3), Daniele Scarponi (a4) and Alan P. Hoffmeister (a5)...


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