Decoupled Temporal Patterns of Evolution and Ecology in Two Post-Paleozoic Clades

Frank K. McKinney, * Scott Lidgard, J. John Sepkoski Jr., Paul D. Taylor

Science 1998; 281: 807-809.

Counts of taxonomic diversity are the prevailing standards for documenting large-scale patterns of evolution in the fossil record. However, the secular pattern of relative ecological importance between the bryozoan clades Cyclostomata and Cheilostomata is not reflected fully in compilations of generic diversity or within-fauna species richness, and the delayed ecological recovery of the Cheilostomata after the mass extinction at the Cretaceous-Tertiary boundary is missed entirely. These observations demonstrate that evolutionary success and ecological dominance can be decoupled and profoundly different, even over tens of millions of years.

F. K. McKinney, Department of Geology, Appalachian State University, Boone, NC 28608-2067, USA. S. Lidgard, Department of Geology, Field Museum, Roosevelt Road at Lake Shore Drive, Chicago, IL 60605, USA. J. J. Sepkoski Jr., Department of the Geophysical Sciences, University of Chicago, Chicago, IL 60637, USA. P. D. Taylor, Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK.
*   To whom correspondence should be addressed. E-mail: mckinneyfk@appstate.edu

Taxonomic diversity, or richness (1, 2), is the current paradigm used to describe how Earth's biota has changed over time. An alternative approach examines patterns in biological activity or habitat structure (3, 4), but this has rarely been associated with taxonomic diversity. Here, we describe a different approach. We compiled data on skeletal mass of two coexisting marine bryozoan clades (Cyclostomata and Cheilostomata) to measure one aspect of relative local ecological dominance over geological time (5). Dominance is usually measured by the abundance of a group of organisms relative to co-occurring groups, or less often by the relative effect of a group on energy flow within a community (6). Species are not equally abundant or important energetically, so lists of species alone may not reflect dominance. Moreover, despite calls for recognizing the importance of abundance in large-scale evolutionary patterns (7), there have been few applications (4, 8).

We compared bryozoan abundance data spanning the past 150 million years with two measures of taxonomic diversity to assess the degree of correspondence between the evolutionary success and ecological importance, or dominance, of the two clades on continental shelves, where they have similar ecological distributions (9). During the past 150 million years, cheilostome bryozoans radiated to an extent comparable with the euteleost fishes, neogastropods, and echinoids (2), whereas diversification of cyclostome bryozoans was arrested.

Cyclostome bryozoans survived the severe crises at the end-Permian and Triassic mass extinctions that removed the other stenolaemate bryozoan clades that had much higher Paleozoic diversities (10). Cyclostome genera increased from four in the Early Jurassic [Hettangian; 206 to 202 million years ago (Ma)] to a maximum of 176 in the latest Cretaceous (Maastrichtian; 71 to 65 Ma). Cheilostomes did not appear until the Late Jurassic and increased from four genera in the mid-Cretaceous (Aptian; 121 to 112 Ma) to a maximum of 178 in the Maastrichtian. The Cretaceous-Tertiary (K-T) extinction resulted in a decrease to 111 genera of cheilostomes and to 83 of cyclostomes by the late Paleocene (Thanetian; 61 to 55 Ma). Cheilostome diversity recovered during the Eocene, and the number of genera exceeded that of the Maastrichtian by mid-Eocene (Lutetian; 49 to 41 Ma). Cyclostome generic diversity, on the other hand, never rebounded after the Paleocene. On the basis of global generic diversity, the later originating cheilostomes had become as species rich as cyclostomes by the Maastrichtian, and through the Cenozoic the proportion of cheilostome species continued to increase (Figs. 1 and 2).

Fig. 1. Early Cretaceous to Quaternary global generic diversity of the bryozoan clades Cyclostomata and Cheilostomata.

Fig. 2. The proportion of global bryozoan generic diversity constituted by cyclostomes from Early Cretaceous to Quaternary.

To assess the ecological consequences of changing diversity, we determined the skeletal mass of cyclostome and cheilostome bryozoans for samples from 70 Jurassic-to-Holocene marine continental shelf deposits (11). The sampled faunas were mostly from Europe and eastern North America and have about the same geographic concentration as the taxonomic databases (12, 13). Despite the noise potentially introduced by taphonomic bias (11), a distinct temporal pattern in relative skeletal mass of cyclostomes and cheilostomes emerges that cannot be attributed to local taphonomic effects.

The within-fauna skeletal mass of cyclostomes declined steeply relative to the skeletal mass of cheilostomes from the mid- through Late Cretaceous (Fig. 3) so that cyclostomes constituted an average of only 28% of total bryozoan skeletal mass by the Maastrichtian. However, relative mass abundance reversed abruptly to 72% cyclostomes immediately above the K-T boundary, and in terms of skeletal mass the cyclostomes dominated to the end of the Danian (65 to 61 Ma) (14). Thanetian through Ypresian (Early Eocene; 55 to 49 Ma) faunas are underrepresented in our data. Therefore, we cannot distinguish adequately whether the Danian cyclostome peak (i) is a relatively short-lived spike of abundance (about 4 million years), similar to but of greater duration than abundance spikes seen in ferns and some foraminifers in the recovery biota (15), or whether (ii) the ecological replacement of cyclostomes by cheilostomes was reset such that tens of millions of years were required for cheilostomes to regain their Late Cretaceous ecological dominance over cyclostomes. Regardless, the long-term pattern in relative skeletal mass of cheilostomes and cyclostomes departs substantially from the generic diversity pattern (Fig. 2) and from patterns at higher taxonomic levels (13).

Fig. 3. Cretaceous and Cenozoic (Tertiary-Quaternary) within-fauna relative skeletal mass of the bryozoan clades Cyclostomata and Cheilostomata, plotted as percent cyclostomes. The moving average curves were fitted by a distance-weighted least squares method (19).

Mean within-fauna species richness of both cheilostomes and cyclostomes declined from the Late Cretaceous into the Paleocene (13). The decline in species richness of cyclostomes appears to have begun in the Cenomanian (99 to 93 Ma), whereas cheilostomes reached maximum species richness in the Maastrichtian and then declined at the K-T boundary. When the cheilostomes began to diversify in the mid-Cretaceous, the ratio of cyclostome to cheilostome species in local communities began a long-term decline that lasted across the K-T boundary through to the early Oligocene (Fig. 4).

Fig. 4. Cretaceous and Cenozoic (Tertiary-Quaternary) curves for within-fauna relative species richness of cyclostomes and cheilostomes, plotted as percent cyclostomes. The moving average curves were fitted by a distance-weighted least squares method (19).

The two measures of taxonomic diversity summarized above differ in detail but both imply that the cheilostomes were more resilient than the cyclostomes during the end-Cretaceous crisis. Among total calcified bryozoans the global proportion of cyclostome genera declined slightly from the Maastrichtian (~50%) to the Danian (~46%), and the proportion of within-fauna cyclostome species richness declined from ~37% in the Maastrichtian to ~30% in the Danian. The abrupt Danian increase in relative skeletal mass of cyclostomes contrasts sharply with these trends in global generic and within-fauna species diversities. This Danian spike could not have been determined from taxonomic databases, and it demonstrates that macroecological and macroevolutionary patterns can be decoupled even within a well-delimited suite of ecologies, such as the overlapping ecological range occupied by both cyclostome and cheilostome bryozoans on marine shelves. This is not unlike some patterns of global morphological disparity relative to taxonomic diversity (16).

The overall Mesozoic and Cenozoic histories of relative within-fauna species richness and skeletal mass of cyclostomes and cheilostomes also demonstrate that macroevolutionary and macroecological patterns can correspond qualitatively but differ quantitatively. As shown in Figs. 3 and 4, the relative skeletal mass of cyclostomes declined much more precipitously than did relative species richness through the Late Cretaceous and again during the post-Paleocene after the Danian spike in cyclostome skeletal mass. The lack of quantitative correspondence of the within-fauna species richness and skeletal mass curves through geologic time indicates that, in the absence of major perturbations, there is a long-term trend for the average cheilostome species to generate a progressively greater skeletal mass than the average cyclostome species. This could result from a gradual trend toward relatively larger colony sizes within cheilostomes (17), a greater number of colonies per cheilostome species, or both.

These data suggest that multiple measures of biotic change through time are necessary for a rich understanding of biospheric evolution. As in contemporary biotic communities, taxonomic diversity captures only limited aspects of the complexity of the biota (18). Multiple measures of biotic systems provide greater insight into history and processes and a better basis for predicting future biodiversity.

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  20. Supported by the NSF (DEB 9306729 to S.L.; EAR 9117289 to F.K.M.), U.S.-U.K. Fulbright program (F.K.M.), National Geographic Society (F.K.M.), Petroleum Research Fund of American Chemical Society (F.K.M.), NASA (NAGW-1963 to J.J.S.J.), and Global Change and the Biosphere Programme of the National History Museum/University College London (P.D.T.). We thank S. Hageman, R. Lupia, and two anonymous reviewers for evaluating the manuscript and numerous colleagues who served as guides to field localities.

16 April 1998; accepted 26 June 1998