Andrew M. Bush

Did Alpha Diversity Increase during the Phanerozoic? Lifting the Veils of Taphonomic, Latitudinal, and Environmental Biases

We estimate the effects of three biases on the observed alpha diversity of paleocommunities from the Middle Paleozoic and Late Cenozoic. The first bias results from the preferential dissolution of aragonite relative to calcite; this bias can lower the relative abundance and preserved diversity of aragonitic taxa, potentially lowering the rarefied diversity of an entire fossil assemblage. We model the effects of this bias by analytically reinserting aragonitic specimens and taxa into Paleozoic assemblages that have been described in the literature. The aragonitic specimens are inserted using a wide range of reasonable assumptions about the original local paleocommunity composition. Although the dissolution bias is probably not as severe as has been argued by some, our analytical modeling indicates that the average Paleozoic assemblage may have lost up to 29% of its total diversity. The second bias results from the higher diversity of the tropics relative to temperate latitudes, but the Late Cenozoic collections we analyzed from the literature represent temperate assemblages whereas the Paleozoic collections were tropical in origin (the northward drift of North America and Europe through time caused this difference). On the basis of latitudinal diversity gradients in the Late Cenozoic, the diversity of the temperate Late Cenozoic samples should be at least doubled for an accurate comparison to the tropical Paleozoic samples. The third bias is environmental: our Late Cenozoic samples tend to come from more onshore, stressed habitats than the Paleozoic samples. In our study, this factor should reduce the apparent diversity of Late Cenozoic paleocommunities by about 9%. After correcting for these biases, standardized alpha diversity appears to increase by a factor of 3.0–3.7 from the Middle Paleozoic to the Late Cenozoic. Previous studies that did not correct for these biases suggested that alpha diversity increased by a factor of 2.5 times; the earlier studies produced approximately correct results because (by chance) the effects of the biases largely cancel out. In the “consensus” article on marine diversity history, an observed increase in alpha diversity was taken as powerful support for an increase in global diversity from the Paleozoic to the Cenozoic. Although we do not test all conflating factors, this study provides new rigor to this longstanding view on alpha diversity change in the Phanerozoic.

Changes in theoretical ecospace utilization in marine fossil assemblages between the mid-Paleozoic and late Cenozoic

Abstract We present a new three-dimensional theoretical ecospace for the ecological classification of marine animals based on vertical tiering, motility level, and feeding mechanism. In this context, analyses of a database of level-bottom fossil assemblages with abundance counts demonstrate fundamental changes in marine animal ecosystems between the mid-Paleozoic (461–359 Ma) and late Cenozoic (23–0.01 Ma). The average local relative abundance of infaunal burrowers, facultatively motile animals, and predators increased, whereas surface dwellers and completely non-motile animals decreased in abundance. Considering tiering, motility, and feeding together, more modes of life had high to moderate average relative abundance in the Cenozoic than in the Paleozoic. These results are robust to the biasing effects of aragonite dissolution in Paleozoic sediments and to heterogeneities in the latitudinal and environmental distributions of collections. Theoretical ecospace provides a unified system for future analyses of the utilization of ecologic opportunities by marine metazoa.

Removing bias from diversity curves: the effects of spatially organized biodiversity on sampling-standardization

Abstract The study of ancient biodiversity trends is confounded by biases of the paleontologic record, but standardizing sampling intensity among time intervals can ameliorate sample-size biases. We show that several existing standardization methods are intimately linked to the spatial components of diversity (alpha, the within-assemblage diversity; and beta, the between-assemblage diversity). The subsampling curves generated by these methods can also be generated by various manipulations of alpha and beta, so that one can predict the responses of the methods to specific changes in alpha or beta diversity. The responses of the subsampling methods to changes in total diversity depend on whether measured alpha or measured beta diversity changed. Like biodiversity, sampling consists of a within-sample component (the number of specimens collected per locality) and a between-sample component (the number of localities). Several subsampling methods (rarefaction, OW, O2W) attempt to standardize sampling effort at both levels, although they use no direct information on the former. Instead, they alter sampling intensity at the beta level to compensate for perceived biases at the alpha level. We show that alpha and beta diversity are not so easily interchangeable and that the accuracy of the subsampling methods depends critically on the spatial characteristics of diversity in a data set. Current methods are calibrated only to the abundance-richness characteristics of individual collections, but the amount of beta diversity and the degree to which the rareness/commonness of taxa correlates among samples also strongly affect the accuracy of the subsampling methods. We offer new calibrations based on empirical data sets that account for these factors. Our findings do not support Alroy et al.s (2001) tentative claim that the taxonomic radiation in the Cenozoic marine realm is an artifact of biased sampling intensity. Their diversity curves that most strongly contradict Sepkoskis traditional Phanerozoic curve are based on a method that overcorrects for local sample-size biases, whereas the remaining curves are either consistent with the traditional curve or ambiguous because of the limited temporal and taxonomic coverage of the analysis. Other factors may bias Sepkoskis curve, but there is insufficient evidence to claim that variations in sampling intensity are the major determinant of its long-term trajectory.

Time-averaging, evolution, and morphologic variation

Abstract Many fossil assemblages are time-averaged, with multiple generations of organisms mixed into a single stratigraphic horizon. A time-averaged sample of a taxon should be more variable than a single-generation sample if enough morphologic change occurred during the interval of time-averaging. Time-averaging may also alter correlations between morphologic variables and obscure allometric relationships in an evolving population. To investigate these issues, we estimated the variability of six modern, single-generation samples of the bivalve Mercenaria campechiensis using Procrustes analysis and compared them with several time-averaged Pleistocene samples of M. campechiensis and M. permagna. Both the modern and the fossil samples ranged in variability, but these ranges were virtually identical. Morphology was quite stable over the hundreds to many thousands of years that passed as the assemblages accumulated, and the variabilities of the fossil samples could be used to estimate single-generation variability. At one fossil locality, the environment and paleocommunity changed partway through the collection interval; the morphology of Mercenaria appears stable above and below the transition but changes across it. This change is similar in magnitude to the differences between geographically separated modern populations, whereas temporal variation within single environmental settings is distinctly less than geographic variation. Analytical time-averaging (the mixing of fossils from different horizons) between paleocommunities increased variability slightly (but not significantly) above that found in living populations. While its constituent populations appear stable on millennial timescales, M. campechiensis has been evolutionarily static since at least the early to middle Pleistocene.

Multiple paleoecological controls on the composition of marine fossil assemblages from the Frasnian (Late Devonian) of Virginia, with a comparison of ordination methods

Abstract Ecological ordination can reveal gradients in the species composition of fossil assemblages that can be correlated with paleoenvironmental gradients. Ordinations of simulated data sets suggest that nonmetric multidimensional scaling (NMDS) generally produces less distorted results than detrended correspondence analysis (DCA). We ordinated 113 brachiopod-dominated samples from the Frasnian (Late Devonian) Brallier, Scherr, and lower Foreknobs Formations of southwest Virginia, which represent a range of siliciclastic marine paleoenvironments. A clear environmental signal in the ordination results was obscured by (apparently) opportunistic species that occurred at high abundance in multiple environments; samples dominated by these species aggregated in ordination space regardless of paleoenvironmental provenance. After the opportunist-dominated samples were removed, NMDS revealed a gradient in species composition that was highly correlated with substrate (grain size); a second, orthogonal gradient likely reflects variation in disturbance intensity or frequency within grain-size regimes. Additional environmental or ecological factors, such as oxygenation, may also be related to the gradients. These two gradients, plus the environmental factors that controlled the occurrence of opportunistic species, explain much of the variation in assemblage composition in the fauna. In general, the composition of fossil assemblages is probably influenced by multiple paleoecological and paleoenvironmental factors, but many of these can be decomposed and analyzed.

Ecological selectivity of the emerging mass extinction in the oceans

To better predict the ecological and evolutionary effects of the emerging biodiversity crisis in the modern oceans, we compared the association between extinction threat and ecological traits in modern marine animals to associations observed during past extinction events using a database of 2497 marine vertebrate and mollusc genera. We find that extinction threat in the modern oceans is strongly associated with large body size, whereas past extinction events were either nonselective or preferentially removed smaller-bodied taxa. Pelagic animals were victimized more than benthic animals during previous mass extinctions but are not preferentially threatened in the modern ocean. The differential importance of large-bodied animals to ecosystem function portends greater future ecological disruption than that caused by similar levels of taxonomic loss in past mass extinction events.

Adjusting global extinction rates to account for taxonomic susceptibility

Abstract Studies of extinction in the fossil record commonly involve comparisons of taxonomic extinction rates, often expressed as the percentage of taxa (e.g., families or genera) going extinct in a time interval. Such extinction rates may be influenced by factors that do not reflect the intrinsic severity of an extinction trigger. Two identical triggering events (e.g., bolide impacts, sea level changes, volcanic eruptions) could lead to different taxonomic extinction rates depending on factors specific to the time interval in which they occur, such as the susceptibility of the fauna or flora to extinction, the stability of food webs, the positions of the continents, and so on. Thus, it is possible for an extinction event with a higher taxonomic extinction rate to be caused by an intrinsically less severe trigger, compared to an event with a lower taxonomic extinction rate. Here, we isolate the effects of taxonomic susceptibility on extinction rates. Specifically, we quantify the extent to which the taxonomic extinction rate in a substage is elevated or depressed by the vulnerability to extinction of classes extant in that substage. Using a logistic regression model, we estimate that the taxonomic susceptibility of marine fauna to extinction has generally declined through the Phanerozoic, and we adjust the observed extinction rate in each substage to estimate the intrinsic extinction severity more accurately. We find that mass extinctions do not generally occur during intervals of unusually high susceptibility, although susceptibility sometimes increases in post-extinction recovery intervals. Furthermore, the susceptibility of specific animal classes to extinction is generally similar in times of background and mass extinction, providing no evidence for differing regimes of extinction selectivity. Finally, we find an inverse correlation between extinction rate within substages and the evenness of diversity of major taxonomic groups, but further analyses indicate that low evenness itself does not cause high rates of extinction.

POTENTIAL PALEOECOLOGIC BIASES FROM SIZE-FILTERING OF FOSSILS: STRATEGIES FOR SIEVING

Abstract The methods by which fossils are extracted from sediments can alter their observed size-frequency distributions, which can in turn alter observed paleoecologic patterns. Building on previous work, this study uses virtual sieving (i.e., replicated via subsampling on a computer) to test the effects of size filtering on the apparent ecologic composition of a database of Miocene mollusks in which the size of every specimen was measured. When simulated mesh sizes varied by nearly an order of magnitude (2–10 mm), the apparent relative abundances of tiering, motility, and feeding categories varied substantially in some individual bulk samples. Not surprisingly, the extent to which variations in mesh size affected the ecologic proportions of a sample depended in part on its size-frequency distribution. If the goal is to characterize the ecology of adult assemblages, the chosen mesh size should not be so small that juveniles dominate the results or so large that a majority of specimens are excluded. For many molluscan assemblages, 2–4 mm should often be appropriate. For preexisting data sets composed of heterogeneously collected data, there is a positive result: averaging samples together to produce a mean view of ecologic composition tends to remove the more egregious effects of the size-filtering bias. Thus, comparisons of the ecologic composition of single samples may be sensitive to mesh-size effects, but comparisons of regional or global faunas are likely more robust, and variations in size filtering may not be an obstacle to large-scale, secular comparisons of ecospace use. Measuring ecologic importance using biomass instead of abundance also reduced the effects of the mesh-size bias by reducing the influence of small-bodied individuals on ecologic proportions.

Contrasting the ecological and taxonomic consequences of extinction

Abstract Extinction in the fossil record is most often measured by the percentage of taxa (species, genera, families, etc.) that go extinct in a certain time interval. This is a measure of taxonomic loss, but previous work has indicated that taxonomic loss may be decoupled from the ecological effects of an extinction. To understand the role extinction plays in ecological change, extinction should also be measured in terms of loss of functional diversity. This study tests whether ecological changes increase correspondingly with taxonomic changes during the Late Ordovician M4/M5 extinction, the Ordovician/Silurian mass extinction, and the Late Devonian mass extinction. All three extinctions are evaluated with regional data sets from the eastern United States. Ecological effects are measured by classifying organisms into ecological lifestyles, which are groups based on ecological function rather than evolutionary history. The taxonomic and ecological effects of each extinction are evaluated with additive diversity partitioning, detrended correspondence analysis, and relative abundance distributions. Although the largest taxonomic changes occur in the Ordovician/Silurian extinction, the largest ecological changes occur in the Late Devonian extinction. These results suggest that the ecological consequences of extinction need to be considered in addition to the taxonomic effects of extinction.

Sustained Mesozoic–Cenozoic diversification of marine Metazoa: A consistent signal from the fossil record

Paleobiological data provide a key historical record of global biodiversity dynamics, but their interpretation is controversial due to geological and sampling biases. Raw data suggest that marine metazoans diversified dramatically during the late Mesozoic and Cenozoic, whereas bias-corrected analyses based on occurrence-level data in the Paleobiology Database (PBDB) have indicated much less Cenozoic diversification. These standardized analyses are cited as evidence that biases strongly conceal underlying patterns in the global fossil record. However, we show that marine diversity did increase substantially and continuously from the Jurassic to the Neogene, even after correcting for biases in PBDB data. Previous standardized analyses did not capture this diversification in full because they were based on incomplete data. In the Cenozoic, observed richness rose to twice the Paleozoic average, which is within the range of values seen in analyses of raw data, suggesting that even the raw global marine fossil record preserves first-order signals of diversity history.