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

Published online by Cambridge University Press:  08 April 2016

Michał Kowalewski
Affiliation:
Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061. E-mail: [email protected]
Susan L. Barbour Wood
Affiliation:
Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061. E-mail: [email protected]
Wolfgang Kiessling
Affiliation:
Museum für Naturkunde, Humboldt-Universität Berlin, Invalidenstrasse 43, Berlin D-10115, Germany
Martin Aberhan
Affiliation:
Museum für Naturkunde, Humboldt-Universität Berlin, Invalidenstrasse 43, Berlin D-10115, Germany
Franz T. Fürsich
Affiliation:
Institut für Paläontologie, Universität Würzburg, Pleicherwall 1, Würzburg, 97070, Germany
Daniele Scarponi
Affiliation:
Department of Earth Sciences, University of Bologna, via Zamboni 67, Bologna 40126, Italy
Alan P. Hoffmeister
Affiliation:
Department of Earth Science, SUNY Oswego, 7060 Route 104, Oswego, New York 13126

Abstract

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.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

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.Google Scholar
Aberhan, M. 1994. Guild-structure and evolution of Mesozoic benthic shelf communities. Palaios 9:516545.CrossRefGoogle Scholar
Aberhan, M. 1998. Early Jurassic Bivalvia of western Canada. Part I. Subclasses Palaeotaxodonta, Pteriomorphia, and Isofilibranchia. Beringeria 21:57150.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Ausich, W. I., and Bottjer, D. J. 1982. Tiering in suspension-feeding communities on soft substrata throughout the Phanerozoic. Science 216:173174.CrossRefGoogle ScholarPubMed
Bambach, R. K. 1977. Species richness in marine benthic habitats through the Phanerozoic. Paleobiology 3:152167.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Bambach, R. K. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiology 19:372397.CrossRefGoogle Scholar
Bambach, R. K. 1999. Energetics in the global marine fauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios 32:131144.CrossRefGoogle Scholar
Bambach, R. K., Knoll, A. H., and Wang, S. C. 2004. Origination, extinction, and mass depletions of marine diversity. Paleobiology 30:522542.2.0.CO;2>CrossRefGoogle Scholar
Benton, M. J. 1995. Diversification and extinction in the history of life. Science 268:5258.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Bush, A. M., Markey, M. J., and Marshall, C. R. 2004. Alpha, beta, gamma: the effects of spatially organized biodiversity on sampling-standardization. Paleobiology 30:666686.2.0.CO;2>CrossRefGoogle Scholar
Cherns, L., and Wright, V. P. 2000. Missing molluscs as evidence of large-scale, early skeletal aragonite dissolution in a Silurian sea. Geology 28:791794.2.0.CO;2>CrossRefGoogle Scholar
Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 199:13021310.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Efron, B. 1981. Nonparametric standard errors and confidence intervals. Canadian Journal of Statistics 9:139172.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Fürsich, F. T. 1977. Corallian (Upper Jurassic) marine benthic associations from England and Normandy. Palaeontology 20:337385.Google Scholar
Fürsich, F. T., and Wendt, J. 1977. Biostratinomy and palaeoecology of the Cassian Formation (Triassic) of the Southern Alps. Palaeogeography, Palaeoclimatology, Palaeoecology 22:257323.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Hall, P. 1992. Efficient bootstrap simulations. Pp. 127143 in Lepage, R. and Billard, L. L., eds. Exploring the limits of bootstrap. Wiley, New York.Google Scholar
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.Google Scholar
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 16:566579.2.0.CO;2>CrossRefGoogle Scholar
Hubalek, Z. 2000. Measures of species diversity in ecology: an evaluation. Folia Zoologica 49:241260.Google Scholar
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.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 95:93969401.CrossRefGoogle ScholarPubMed
Kidwell, S. M. 2001. Preservation of species abundance in marine death assemblages. Science 294:10911094.CrossRefGoogle ScholarPubMed
Kidwell, S. M. 2005. Shell composition has no net impact on large-scale evolutionary patterns in molluscs. Science 307:914917.CrossRefGoogle Scholar
Kidwell, S. M., and Brenchley, P. J. 2004. Patterns in bioclastic accumulations through the Phanerozoic: changes in input or in destruction? Geology 22:11391143.2.3.CO;2>CrossRefGoogle Scholar
Kiessling, W. 2002. Radiolarian diversity patterns in the latest Jurassic-earliest Cretaceous. Palaeogeography, Palaeoclimatology, Palaeoecology 187:179206.CrossRefGoogle Scholar
Kiessling, W. 2005. Long-term relationships between ecological stability and biodiversity in Phanerozoic reefs. Nature 433:410413.CrossRefGoogle ScholarPubMed
Kittl, E. 1891. Die Gastropoden der Schichten von St. Cassian der südalpinen Trias. Annalen des Kaiserlich-Königlichen Naturhistorischen Hofmuseums 6:166262.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
Kowalewski, M., and Hoffmeister, A. P. 2003. Sieves and fossils: effects of mesh size on paleontological patterns. Palaios 18:460469.2.0.CO;2>CrossRefGoogle Scholar
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.Google Scholar
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 114:239256.2.0.CO;2>CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Krebs, C. J. 1999. Ecological methodology. Addison-Wesley, Menlo Park, Calif.Google Scholar
Magurran, A. E. 1998. Ecological diversity and its measurement. Princeton University Press, Princeton, NJ. Google Scholar
Magurran, A. E. 2004. Measuring biological diversity. Blackwell, London.Google Scholar
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.Google Scholar
Newell, N. D. 1959. Adequacy of the fossil record. Journal of Paleontology 33:488499.Google Scholar
Olszewski, T. D. 2004. A unified mathematical framework for the measurement of richness and evenness within and among multiple communities. Oikos 104:377387.CrossRefGoogle Scholar
Peters, S. E. 2004. Evenness in Cambrian–Ordovician benthic marine communities in North America. Paleobiology 30:325346.2.0.CO;2>CrossRefGoogle Scholar
Peters, S. E., and Foote, M. 2001. Biodiversity in the Phanerozoic: a reinterpretation. Paleobiology 27:583601.2.0.CO;2>CrossRefGoogle Scholar
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 30:331334.2.0.CO;2>CrossRefGoogle Scholar
Raup, D. M. 1972. Taxonomic diversity during the Phanerozoic. Science 177:10651071.CrossRefGoogle ScholarPubMed
Raup, D. M. 1976. Species diversity in the Phanerozoic: an interpretation. Paleobiology 2:289297.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Scarponi, D., and Kowalewski, M. In press. Sequence stratigraphic anatomy of diversity patterns: late Quaternary benthic mollusks of Po Plain, Italy. Palaios.Google Scholar
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.Google Scholar
Sepkoski, J. J. Jr. 1981. A factor analytic description of the Phanerozoic marine fossil record. Paleobiology 7:3653.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Smith, B., and Wilson, J. B. 1996. A consumer's guide to evenness indices. Oikos 76:7082.CrossRefGoogle Scholar
Sohl, N. F. 1987. Cretaceous gastropods: contrasts between Tethys and the temperate provinces. Journal of Paleontology 61:10851111.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
Taylor, J. D., Morris, N. J., and Taylor, C. N. 1980. Food specialization and the evolution of predatory prosobranch gastropods. Palaeontology 23:375409.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Valentine, J. W. 1969. Patterns of taxonomic and ecological structure of the shelf benthos during Phanerozoic time. Palaeontology 12:684709.Google Scholar
Vermeij, G. J. 1977. The Mesozoic marine revolution: the evidence from snails, predators, and grazers. Paleobiology 3:245258.CrossRefGoogle Scholar
Vermeij, G. J. 1987. Evolution and escalation; an ecological history of life. Princeton University Press, Princeton, NJ. CrossRefGoogle Scholar
Vermeij, G. J. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21:125152.CrossRefGoogle Scholar
Washington, H. G. 1984. Diversity, biotic and similarity indices: a review with special relevance to aquatic ecosystems. Water Resources 18:653694.Google Scholar
Wright, P., Cherns, L., and Hodges, P. 2003. Missing molluscs: field testing taphonomic loss in the Mesozoic through early large-scale aragonite dissolution. Geology 31:211214.2.0.CO;2>CrossRefGoogle Scholar