Spatial Bias in the Marine Fossil Record

Inference of past and present global biodiversity requires enough global data to distinguish biological pattern from sampling artifact. Pertinently, many studies have exposed correlated relationships between richness and sampling in the fossil record, and methods to circumvent these biases have been proposed. Yet, these studies often ignore paleobiogeography, which is undeniably a critical component of ancient global diversity. Alarmingly, our global analysis of 481,613 marine fossils spread throughout the Phanerozoic reveals that where localities are and how intensively they have been sampled almost completely determines empirical spatial patterns of richness, suggesting no separation of biological pattern from sampling pattern. To overcome this, we analyze diversity using occurrence records drawn from two discrete paleolatitudinal bands which cover the bulk of the fossil data. After correcting the data for sampling bias, we find that these two bands have similar patterns of richness despite markedly different spatial coverage. Our findings suggest that i) long-term diversity trends result from large-scale tectonic evolution of the planet, ii) short-term diversity trends are region-specific, and iii) paleodiversity studies must constrain their analyses to well-sampled regions to uncover patterns not driven by sampling.     

Biodiversity curves for the Ordovician of Baltoscandia

Biodiversity curves for the Ordovician of Baltoscandia show a substantial increase in taxonomical diversity through the period, as seen also in global data sets. A database of 10,340 records of first and last appearances of species at different localities in the region has been analysed using simple species counts, and partly validated with resampling methods. While the biodiversity curve for all fossil groups combined is probably reasonably accurate except for an unknown scaling constant, taxonomical or geographical subsets may not be sufficiently well sampled to allow precise measurement of their species counts through time. The analysis shows a major diversification event commencing in the middle Arenig (Ibex-Whiterock boundary), and more limited diversification events in the Llanvirn, Caradoc and Ashgill. The Scandinavian (Norwegian and Swedish) biodiversity curves are broadly correlated with major changes in sea level, with low biodiversity at highstands and high biodiversity at lowstands, although this pattern is not clear for all fossil groups. In the Arenig, graptolites and trilobites appear to have higher diversities at high sea levels, while the brachiopods and ostracodes show higher diversities at low sea level. As a consequence, the Arenig diversification is delayed for the latter two groups until the upper end of the interval.     

Did hard substrate taxa diversify prior to the Great Ordovician Biodiversification Event?

The Great Ordovician Biodiversification Event (GOBE) refers to one of the greatest increases in biodiversity during the Phanerozoic. Recent studies have shown that this taxonomic increase can be attributed to elevated origination rates around the Dapingian–Darriwilian boundary in the Middle Ordovician, while extinction rates stayed relatively constant throughout the Ordovician. Even though this global pattern of origination and extinction appears similar across diverse groups and geographical areas, earlier studies suggested that hard substrate taxa may have diversified prior to the GOBE, during the Early Ordovician. Here, we quantify Ordovician diversification dynamics of hard substrate taxa while simultaneously accounting for temporally varying sampling probabilities. Diversification rates of hard substrate taxa, both as a whole and when analysed as separate groups, appear to be very similar to those of free-living benthic taxa. The observation that the diversification dynamics of many different taxonomic and ecological groups show the same temporal pattern, suggests a common cause of Ordovician diversification dynamics.     

New crinoids from the Baltic region (Estonia): fossil tip‐dating phylogenetics constrains the origin and Ordovician–Silurian diversification of the Flexibilia (Echinodermata)

This study documents previously unknown taxonomic and morphological diversity among early Palaeozoic crinoids. Based on highly complete, well preserved crown material, we describe two new genera from the Ordovician and Silurian of the Baltic region (Estonia) that provide insight into two major features of the geological history of crinoids: the early evolution of the flexible clade during the Great Ordovician Biodiversification Event (GOBE), and their diversification history surrounding the end‐Ordovician mass extinction. The unexpected occurrence of a highly derived sagenocrinid, Tintinnabulicrinus estoniensis gen. et. sp. nov., from Upper Ordovician (lower Katian) rocks of the Baltic palaeocontinent provides high‐resolution temporal, taxonomic and palaeobiogeographical constraints on the origin and early evolution of the Flexibilia. The Silurian (lower Rhuddanian, Llandovery) Paerticrinus arvosus gen. et sp. nov. is the oldest known Silurian crinoid from Baltica and thus provides the earliest Baltic record of crinoids following the aftermath of the end‐Ordovician mass extinction. A Bayesian ‘fossil tip‐dating’ analysis implementing the fossilized birth–death process and a relaxed morphological clock model suggests that flexibles evolved c. 3 million years prior to their oldest fossil record, potentially involving an ancestor–descendant relationship (via ‘budding’ cladogenesis or anagenesis) with the paraphyletic cladid Cupulocrinus. The sagenocrinid subclade rapidly diverged from ‘taxocrinid’ grade crinoids during the final stages of the GOBE, culminating in maximal diversity among Ordovician crinoid faunas on a global scale. Remarkably, diversification patterns indicate little taxonomic turnover among flexibles across the Late Ordovician mass extinction. However, the elimination of closely related clades may have helped pave the way for their subsequent Silurian diversification and increased ecological role in post‐Ordovician Palaeozoic marine communities. This study highlights the significance of studies reporting faunas from undersampled palaeogeographical regions for clade‐based phylogenetic studies and improving estimates of global biodiversity through geological time.     

HOW DO GEOLOGICAL SAMPLING BIASES AFFECT STUDIES OF MORPHOLOGICAL EVOLUTION IN DEEP TIME? A CASE STUDY OF PTEROSAUR (REPTILIA: ARCHOSAURIA) DISPARITY

A fundamental contribution of paleobiology to macroevolutionary theory has been the illumination of deep time patterns of diversification. However, recent work has suggested that taxonomic diversity counts taken from the fossil record may be strongly biased by uneven spatiotemporal sampling. Although morphological diversity (disparity) is also frequently used to examine evolutionary radiations, no empirical work has yet addressed how disparity might be affected by uneven fossil record sampling. Here, we use pterosaurs (Mesozoic flying reptiles) as an exemplar group to address this problem. We calculate multiple disparity metrics based upon a comprehensive anatomical dataset including a novel phylogenetic correction for missing data, statistically compare these metrics to four geological sampling proxies, and use multiple regression modeling to assess the importance of uneven sampling and exceptional fossil deposits (Lagerstätten). We find that range‐based disparity metrics are strongly affected by uneven fossil record sampling, and should therefore be interpreted cautiously. The robustness of variance‐based metrics to sample size and geological sampling suggests that they can be more confidently interpreted as reflecting true biological signals. In addition, our results highlight the problem of high levels of missing data for disparity analyses, indicating a pressing need for more theoretical and empirical work.     

Conodontophorid biodiversification during the Ordovician in South China

Wu, R., Stouge, S. & Wang, Z. 2012: Conodontophorid biodiversification during the Ordovician in South China. Lethaia, Vol. 45, pp. 432–442. Analysis of the Ordovician conodontophorid diversity pattern for South China using normalized and total diversity measures reveals that diversity peaks occurred in the mid‐Tremadocian, mid‐late Floian, early Dapingian and mid‐Darriwilian periods. The conodontophorids radiated during the Floian, maintaining relatively high diversity into the early part of the Middle Ordovician until a significant diversity decrease occurred in the late Dapingian. A relatively low diversity level prevailed in the Late Ordovician. Three diversification intervals based on origination, extinction and turnover rates have been identified i.e. (1) Tremadocian to mid‐late Floian, (2) early Dapingian and (3) late Dapingian to early Darriwilian. Diversity curves for conodontophorids, brachiopods, graptolites, acritarchs and trilobites from South China are comparable during the Early Ordovician, although differences are apparent in the Middle and Late Ordovician. In South China, conodontophorid diversity reacted primarily to sea‐level changes during the Early and Middle Ordovician, when the peak of this biodiversification generally coincided with a transgression. Climate changes – especially the global cooling that occurred during the Late Ordovician glaciation – and sea‐water chemistry were also important controlling factors. □Biodiversification, conodonts, Ordovician, South China.     

Modeling bivalve diversification: the effect of interaction on a macroevolutionary system

The global diversification of the class Bivalvia has historically received two conflicting interpretations. One is that a major upturn in diversification was associated with, and a consequence of, the Lake Permian mass extinction. The other is that mass extinctions have had little influence and that bivalves have experienced slow but nearly steady exponential diversification through most of their history, unaffected by interactions with other clades. We find that the most likely explanation lies between these two interpretations. Through most of the Phanerozoic, the diversity of bivalves did indeed exhibit slow growth, which was not substantially altered by mass extinctions. However, the presence of "hyperexponential bursts" in diversification during the initial Ordovician radiation and following the Late Permian and Late Cretaceous mass extinctions suggests a more complex history in which a higher characteristic diversification rate was dampened through most of the Phanerozoic. The observed pattern can be accounted for with a two-phase coupled (i.e., interactive) logistic model, where one phase is treated as the "bivalves" and the other phase is treated as a hypothetical group of clades with which the "bivalves" might have interacted. Results of this analysis suggest that interactions with other taxa have substantially affected bivalve global diversity through the Phanerozoic.     

Sea level,dinosaur diversity and sampling biases: investigating the ‘common cause’ hypothesis in the terrestrial realm

The fossil record is our primary window onto the diversification of ancient life, but there are widespread concerns that sampling biases may distort observed palaeodiversity counts. Such concerns have been reinforced by numerous studies that found correlations between measures of sampling intensity and observed diversity. However, correlation does not necessarily mean that sampling controls observed diversity: an alternative view is that both sampling and diversity may be driven by some common factor (e.g. variation in continental flooding driven by sea level). The latter is known as the ‘common cause’ hypothesis. Here, we present quantitative analyses of the relationships between dinosaur diversity, sampling of the dinosaur fossil record, and changes in continental flooding and sea level, providing new insights into terrestrial common cause. Although raw data show significant correlations between continental flooding/sea level and both observed diversity and sampling, these correlations do not survive detrending or removal of short-term autocorrelation. By contrast, the strong correlation between diversity and sampling is robust to various data transformations. Correlations between continental flooding/sea level and taxic diversity/sampling result from a shared upward trend in all data series, and short-term changes in continental flooding/sea level and diversity/sampling do not correlate. The hypothesis that global dinosaur diversity is tied to sea-level fluctuations is poorly supported, and terrestrial common cause is unsubstantiated as currently conceived. Instead, we consider variation in sampling to be the preferred null hypothesis for short-term diversity variation in the Mesozoic terrestrial realm.     

Did the evolution of the phytoplankton fuel the diversification of the marine biosphere?

We discuss the possible links between the fossil record of marine biodiversity, nutrient availability and primary productivity. The parallelism of the fossil records of marine phytoplankton and faunal biodiversity implicates the quantity (primary productivity) and quality (stoichiometry) of phytoplankton as being critical to the diversification of the marine biosphere through the Phanerozoic. The relatively subdued marine biodiversity of the Palaeozoic corresponds to a time of relatively low macronutrient availability and poor food quality of the phytoplankton as opposed to the diversification of the Modern Fauna through the Mesozoic–Cenozoic. Increasing nutrient runoff to the oceans through the Phanerozoic resulted from orogeny, the emplacement of Large Igneous Provinces (LIPs), the evolution of deep-rooting forests and the appearance of more easily decomposable terrestrial organic matter that enhanced weathering. Positive feedback by bioturbation of an expanding benthos played a critical role in evolving biogeochemical cycles by linking the oxidation of dead organic matter and the recycling of nutrients back to the water column where they could be re-utilized. We assess our conclusions against a recently published biogeochemical model for geological time-scales. Major peaks of marine diversity often occur near rising or peak fluxes of silica, phosphorus and dissolved reactive oceanic phosphorus; either major or minor ⁸⁷Sr/⁸⁶Sr peaks; and frequently in the vicinity of major (Circum-Atlantic Magmatic Province) and minor volcanic events, some of which are associated with Oceanic Anoxic Events. These processes appear to be scale-dependent in that they lie on a continuum between biodiversification on macroevolutionary scales of geological time and mass extinction.     

Geographical,environmental and intrinsic biotic controls on Phanerozoic marine diversification

Abstract: The Paleobiology Database now includes enough data on fossil collections to produce useful time series of geographical and environmental variables in addition to a robust global Phanerozoic marine diversity curve. The curve is produced by a new ‘shareholder quorum’ method of sampling standardization that removes biases but avoids overcompensating for them by imposing entirely uniform data quotas. It involves drawing fossil collections until the taxa that have been sampled at least once (the ‘shareholders’) have a summed total of frequencies (i.e. coverage) that meets a target (the ‘quorum’). Coverage of each interval’s entire data set is estimated prior to subsampling using a variant of a standard index, Good’s u. This variant employs counts of occurrences of taxa described in only one publication instead of taxa found in only one collection. Each taxon’s frequency within an interval is multiplied by the interval’s index value, which limits the maximum possible sampling level and thereby creates the need for subsampling. Analyses focus on a global diversity curve and curves for northern, southern and ‘tropical’ (30°N to 30°S) palaeolatitudinal belts. Tropical genus richness is remarkably static, so most large shifts in the curve reflect trends at higher latitudes. Changes in diversity are analysed as a function of standing diversity; the number, spacing and palaeolatitudinal position of sampled geographical cells; the mean onshore–offshore position of cells; and proportions of cells from carbonate, onshore and reefal environments. Redundancy among the variables is eliminated by performing a principal components analysis of each data set and using the axis scores in multiple regressions. The key factors are standing diversity and the dominance of onshore environments such as reefs. These factors combine to produce logistic growth patterns with slowly changing equilibrium values. There is no evidence of unregulated exponential growth across any long stretch of the Phanerozoic, and in particular there was no large Cenozoic radiation beyond the Eocene. The end‐Ordovician, Permo–Triassic and Cretaceous–Palaeogene mass extinctions had relatively short‐term albeit severe effects. However, reef collapse was involved in these events and also may have caused large, longer term global diversity decreases in the mid‐Devonian and across the Triassic/Jurassic boundary. Conversely, the expansion of reef ecosystems may explain newly recognized major radiations in the mid‐Permian and mid‐Jurassic. Reef ecosystems are particularly vulnerable to current environmental disturbances such as ocean acidification, and their decimation might prolong the recovery from today’s mass extinction by millions or even tens of millions of years.     

Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form

We examine terminal addition, the process of addition of serial elements in a posterior subterminal growth zone during animal development, across modern taxa and fossil material. We argue that terminal addition was the basal condition in Bilateria, and that modification of terminal addition was an important component of the rapid Cambrian evolution of novel bilaterian morphology. We categorize the often-convergent modifications of terminal addition from the presumed ancestral condition. Our focus on terminal addition and its modification highlights trends in the history of animal evolution evident in the fossil record. These trends appear to be the product of departure from the initial terminal addition state, as is evident in evolutionary patterns within-fossil groups such as trilobites, but is also more generally related to shifts in types of morphologic change through the early Phanerozoic. Our argument is contingent on dates of metazoan divergence that are roughly convergent with the first appearance of metazoan fossils in the latest Proterozoic and Cambrian, as well as on an inference of homology of terminal addition across bilaterian Metazoa.     

Mollusks in Phanerozoic marine communities: Implications from the analysis of global paleontological databases

Evolutionary history of three mollusk classes (Bivalvia, Gastropoda, and Cephalopoda), regarded as components of the Phanerozoic marine biota, is discussed based on the comparison of dynamics of quantitative parameters obtained from the analysis of the global paleontological databases. The main trends in the evolution of the role of mollusks in Phanerozoic marine ecosystems and relationships between the diversification of this group and biodiversity of paleocommunities are considered. Certain parameters show similarity between the diversity dynamics of mollusks and the whole marine biota, including the paleolatitudinal distribution of diversity. At the same time, mollusk classes differ considerably in certain aspects. The evolutionary history of Bivalvia, Gastropoda, and Cephalopoda was different and determined presumably by deep ecological divergence which occurred as early as the Early Paleozoic adaptive radiation. Bivalves and gastropods followed the trend of a gradual and constant increase in their role in marine communities; they are characterized by high and constantly growing duration of genera, high (and also growing) frequency in paleontological collections. Cephalopods show more chaotic macroevolutionary dynamics, relatively low mean duration of genera and low relative frequency.     

El Ordovícico Medio del Anti-Atlas marroquí: paleobiodiversidad, actualización bioestratigráfica y correlación

Middle Ordovician formations of the Anti-Atlas ranges of southern Morocco provided a diverse record of trilobites, molluscs, echinoderms, brachiopods, graptolites and micro- and ichnofossils from about 180 fossil localities. These were mainly found during the national geological mapping to the 1:200.000 scale, and most of them remained unreferenced until now. The lithostratigraphic position of all fossil localities is briefly studied showing, in some cases, noteworthy discrepances with previous works. Besides this stratigraphical reappraisal, a review of the fossil record for each formation and locality is done, together with a taxonomical update. From a chronostratigraphical point of view, the whole sucession constituted by the Tachilla Formation and First Bani Group formations are here referred to the Mediterranean regional scale. The Oretanian-Dobrotivian and Dobrotivian-Berounian boundaries are located respectively in the Bou-Zeroual Formation and at the top of the Izegguirene Formation. The transition between the lower and upper Oretanian is provisionally established in the upper third of the Tachilla Formation, and those between the lower and upper Dobrotivian at the base or in the lower part of the Ouine-Inirne Formation. A general correlation with the global standard and British regional scales is also suggested for the Middle Ordovician of the Moroccan Anti-Atlas. The basal limit of the Upper Ordovician series probably lies within the lower part of the Izegguirene Formation. Paleobiogeographical data confirm the interest of this area as an important diversification center for many Mediterranean faunas that underwent remarkable dispersal in northern Gondwanan shelves.     

THE EFFECTS OF SAMPLING BIAS ON PALAEOZOIC FAUNAS AND IMPLICATIONS FOR MACROEVOLUTIONARY STUDIES

Abstract:  Trilobites, a dominant component of marine faunas during the Cambrian and Ordovician and which survived until the end of the Permian (542–251 Ma) have been used in many macroevolutionary analyses. Here, we use a discovery curve to document the sampling history of trilobites, which we consider a proxy for Palaeozoic faunas in general. At higher taxonomic ranks, orders, suborders and superfamilies, the fossil record has been completely sampled, while the family rank also shows a high level of sampling completeness, having reached an asymptote in 1970. Importantly, this levelling-off occurred even though worker effort continued to increase. However, at genus level the sampling record is incomplete, indicating that families should not be used as a proxy for genera. There is little variation among the different subsets of generic data, with the sampling history of different stratigraphic periods and among different orders being very similar. However, there is noticeable variation among geographical regions, caused by variations in worker effort, and this could cause problems when comparing speciation and diversity patterns across faunal provinces. The role of synonyms on sampling history has had little effect.     

Phanerozoic marine biodiversity follows a hyperbolic trend

Changes in marine biodiversity through the Phanerozoic correlate much better with hyperbolic model (widely used in demography and macrosociology) than with exponential and logistic models (traditionally used in population biology and extensively applied to fossil biodiversity as well). The latter models imply that changes in diversity are guided by a first-order positive feedback (more ancestors, more descendants) and/or a negative feedback arising from resource limitation. Hyperbolic model implies a second-order positive feedback. The hyperbolic pattern of the world population growth arises from a second-order positive feedback between the population size and the rate of technological growth. The hyperbolic character of biodiversity growth can be similarly accounted for by a feedback between the diversity and community structure complexity. The similarity between the curves of biodiversity and human population probably comes from the fact that both are derived from the interference of the hyperbolic trend with cyclical and stochastic dynamics.     

Diversity and Evolution of Body Size in Fishes

The diversity of body sizes observed among species of a clade is a combined result of microevolutionary processes (i.e. natural selection and genetic drift) that cause size changes within phylogenetic lineages, and macroevolutionary processes (i.e. speciation and extinction) that affect net rates of diversification among lineages. Here we assess trends of size diversity and evolution in fishes (non-tetrapod craniates), employing paleontological, macroecological, and phylogenetic information. Fishes are well suited to studies of size diversity and evolution, as they are highly diverse, representing more than 50% of all living vertebrate species, and many fish taxa are well represented in the fossil record from throughout the Phanerozoic. Further, the frequency distributions of sizes among fish lineages resemble those of most other animal taxa, in being right-skewed, even on a log scale. Using an approach that measures rates of size evolution (in darwins) within a formal phylogenetic framework, we interpret the shape of size distributions as a balance between the competing forces of diversification, pushing taxa away from ancestral values, and of conservation, drawing taxa closer to a central tendency. Within this context we show how non-directional mechanisms of evolution (i.e. passive diffusion processes) can produce an hitherto unperceived bias to larger size, when size is measured on the conventional log scale. These results demonstrate how the interpretation of macroecological datasets can be enriched from an historical perspective, and document the ways in which macroevolutionary and microevolutionary processes may be decoupled in the production of size diversity.     

On formation‐based sampling proxies and why they should not be used to correct the fossil record

The fossil record is a unique resource on the history of life, but it is well known to be incomplete. In a series of high‐profile papers, a residual modelling technique has been applied to correct the raw palaeodiversity signal for this bias and incompleteness, and the claim is made that the processed time series are more accurate than the raw data. We apply empirical and simulation approaches to test for correlation and directionality of any relationships between rock and fossil data. The empirical data comprise samples of the global fossil record through the Phanerozoic, and we use simulations to assess whether randomly sampled subsets of modelled data can be improved by application of the residual modelling technique. Our results show that using formation counts as a sampling proxy to correct the fossil record via residual modelling is ill founded. The supposedly independent model of sampling is information‐redundant with respect to the raw palaeodiversity data it seeks to correct, and so the outputs are generally likely to be further from the truth than the raw data. We recommend that students of palaeodiversity cease to use residual modelling estimates based on formation counts, and suggest that results from a substantial number of papers published in the past ten years require re‐evaluation.     

Biodiversity patterns of Early–Middle Ordovician marine microphytoplankton in South China

Based on new materials from six sections and all available literature data, new diversity curves are presented for the phytoplankton (acritarchs) from South China, covering the Early–Middle Ordovician interval, when the Great Ordovician Biodiversification Event took place. The total diversity curve and the origination data imply that a major radiation of the phytoplankton occurred during the analysed interval. A peak of the total acritarch diversity curve appears in the A. suecicus graptolite biozone. The diversity changes vary in the different parts of the investigated area, most probably depending on the position of the analysed sections on the carbonate shelf or the slope, reflecting diversity differences due to the position on an inshore–offshore transect.The Early–Middle Ordovician diversity pattern of the phytoplankton is compared with those of several marine invertebrate groups. Compared with the diversity curve peak of the acritarchs, the conodonts and brachiopods reached their highest diversities before the acritarchs, while the highest diversity of the chitinozoans appears slightly later. The graptolites show two peaks during the Early–Middle Ordovician, while the trilobites diversity curve shows a peak only in the Sandbian. The different fossil groups, such as chitinozoans, conodonts, graptolites, brachiopods and trilobites show therefore different evolutionary patterns to that of the acritarchs, that are not yet fully understood, and correlations are so far difficult.The acritarch diversity changes can partly be compared to the local sea-level changes from four sections in South China. At a larger scale, the acritarch radiation coincides with a general transgression. At a regional or local scale, correlations are not straightforward, pointing out that more detailed data, based on both acritarch studies and more precise sea-level investigations, are necessary.     

Do new reconstructions clarify the relationships between the Phanerozoic diversity dynamics of marine invertebrates and long-term eustatic trends?

A relationship between global sea levels and the diversity of marine invertebrates throughout the Phanerozoic remains an urgent matter for debates. Its recognition depends on a proper selection of diversity and eustatic curves. A comparison of changes in the revised sample-standardized generic diversity and long-term global sea-level changes provides a weaker evidence for a direct covarying relationship than established earlier, although the eustatic control on diversity dynamics of marine invertebrates was important during ∼74% of the Phanerozoic. Multiple causation of biodiversity changes, data bias, erroneous reconstructions, and conceptual misinterpretations are likely explanations of observed difference between the new biodiversity and eustatic curves.