Memoir 4: An Analysis of the History of Marine Animal Diversity

There are essentially three major crinoid faunas of the Paleozoic: 1) the lower Paleozoic (Ordovician) fauna dominated by disparids and diplobathrid camerates; 2) the middle Paleozoic (Silurian-middle Mississippian) fauna dominated by monobathrid camerates, cladids, and flexibles; and 3) the upper Paleozoic (middle Mississippian-Permian) fauna dominated by cladids. Change from the middle Paleozoic fauna to the late Paleozoic fauna, at or near the Osagean-Meramecian boundary, was characterized by Laudon (1948) as “one of the most remarkable faunal breaks in the entire Paleozoic era”. The monobathrids that had reached their zenith in the Osagean (Tournaisian-Visean) became a very minor component of late Paleozoic faunas. Conventional thinking has implied that a mass extinction of crinoids occurred at the Osagean-Meramecian boundary.We have biostratigraphically subdivided the late Osagean and early Meramecian into four zones (times A-D, oldest to youngest, all within the Gnathodustexanus zone) in order to study the origination and extinction of all crinoid species during the changeover from the middle to upper Paleozoic faunas. Rather than a mass extinction, a monotonic turnover of species fits a pattern of gradual extinction as extinctions outpaced originations. Data are based on 216 species (taxonomically updated) from 69 localities and are as follows:The pattern of originations and extinctions for monobathrids is very similar to the pattern for all crinoid species.The above data have maximum diversity during Time B of the late Osagean followed by declining diversity in times C and D into the early Meramecian. Late Meramecian crinoid faunas (after time D) were less diverse with a maximum of about 45 species. The gradual decline of crinoids across the Osagean-Meramecian boundary cannot be explained as sampling bias (Signor-Lipps effect), because ranges of crinoids thought to be extinct at the boundary are extended into the early Meramecian as well as disappearing at various tinles prior to the boundary.The decline in diversity and the monotonic turnover of species are hypothesized to be the result of habitat reduction as the Eastern Interior Basin of North America was gradually infilled with clastic sediments at the end of the Acadian Orogeny. Most notable in this regard was the smothering of the Keokuk Limestone carbonate bank. Changes in sea level also contributed to habitat reduction. Lowering of sea level at the end of the Osagean caused restriction of open marine environments. A transgression in the early Meramecian was followed by shoaling and restriction during deposition of the late Meramecian Salem and St. Louis limestones.

Comments on: Periodicity in the extinction rate and possible astronomical causes – comment on mass extinctions over the last 500 myr: an astronomical cause? (Erlykin <i>et al</i>.)

The kinetic model of taxonomic diversity predicts that the long-term diversification of taxa within any large and essentially closed ecological system should approximate a logistic process controlled by changes in origination and extinction rates with changing numbers of taxa. This model is tested with a new compilation of numbers of metazoan families known from Paleozoic stages (including stage-level subdivisions of the Cambrian). These data indicate the occurrence of two intervals of logistic diversification within the Paleozoic. The first interval, spanning the Vendian and Cambrian, includes an approximately exponential increase in families across the Precambrian-Cambrian Boundary and a “pseudo-equilibrium” through the Middle and Late Cambrian, caused by diversity-dependent decrease in origination rate and increase in extinction rate. The second interval begins with a rapid re-diversification in the Ordovician, which leads to a tripling of familial diversity during a span of 50 Myr; by the end of the Ordovician diversity attains a new dynamic equilibrium that is maintained, except for several extinction events, for nearly 200 Myr until near the end of the Paleozoic. A “two-phase” kinetic model is constructed to describe this heterogeneous pattern of early Phanerozoic diversification. The model adequately describes the “multiple equilibria,” the asymmetrical history of the “Cambrian fauna,” the extremely slow initial diversification of the later “Paleozoic fauna,” and the combined patterns of origination and extinction in both faunas. It is suggested that this entire pattern of diversification reflects the early success of ecologically generalized taxa and their later replacement by more specialized taxa.

Data on numbers of marine families within 91 metazoan classes known from the Phanerozoic fossil record are analyzed. The distribution of the 2800 fossil families among the classes is very uneven, with most belonging to a small minority of classes. Similarly, the stratigraphic distribution of the classes is very uneven, with most first appearing early in the Paleozoic and with many of the smaller classes becoming extinct before the end of that era. However, despite this unevenness, a Q -mode factor analysis indicates that the structure of these data is rather simple. Only three factors are needed to account for more than 90% of the data. These factors are interpreted as reflecting the three great “evolutionary faunas” of the Phanerozoic marine record: a trilobite-dominated Cambrian fauna, a brachiopod-dominated later Paleozoic fauna, and a mollusc-dominated Mesozoic-Cenozoic, or “modern,” fauna. Lesser factors relate to slow taxonomic turnover within the major faunas through time and to unique aspects of particular taxa and times. Each of the three major faunas seems to have its own characteristic diversity so that its expansion or contraction appears as being intimately associated with a particular phase in the history of total marine diversity. The Cambrian fauna expands rapidly during the Early Cambrian radiations and maintains dominance during the Middle to Late Cambrian “equilibrium.” The Paleozoic fauna then ascends to dominance during the Ordovician radiations, which increase diversity dramatically; this new fauna then maintains dominance throughout the long interval of apparent equilibrium that lasts until the end of the Paleozoic Era. The modern fauna, which slowly increases in importance during the Paleozoic Era, quickly rises to dominance with the Late Permian extinctions and maintains that status during the general rise in diversity to the apparent maximum in the Neogene. The increase in diversity associated with the expansion of each new fauna appears to coincide with an approximately exponential decline of the previously dominant fauna, suggesting possible displacement of each evolutionary fauna by its successor.

Approximate periodicity for peak rates of global extinction during the past 250 m.y. may have resulted from delayed recovery following major extinction events. Two components can be envisioned for such delays: persistence of inimical environmental conditions for some time after the onset of the crisis, and slow restoration of vulnerable taxa. This general hypothesis is consistent with statistical evidence of linkage between measured rates of extinction of marine invertebrate genera for contiguous stages and substages of the geologic column. The nine broad valleys between the “periodic” peak rates for the past 250 m.y. exhibit only three trivial secondary peaks, indicating that, if the pattern is not artifactual, trends in global rates of extinction have not readily been abruptly reversed. Moreover, the smooth observed trends reflect the fact that regional crises tend to remove many species but few genera. To some degree, high rates of extinction that precede peak rates must represent bias of the incomplete fossil record (the Signor-Lipps effect). High rates that immediately follow peak rates also may, to a degree, reflect biological legacy: (1) final extinction of weakened genera or (2) extinction of new genera that contain few species or represent failed evolutionary “experiments.” Nonetheless, there is evidence that protracted intervals of stressful environmental conditions contributed to high rates of extinction preceding or following certain peak intervals, including the Scythian, Cenomanian, Early Paleocene, and Early Oligocene. The reef-building rudists, for example, suffered heavy extinction during both Cenomanian and Turonian time and then failed to recover quickly. The late Neogene record of bivalve molluscs in the Western Atlantic offers a more detailed picture of delayed recovery. Here early intervals of glacial expansion caused heavy extinction, leaving an impoverished, eurythermal fauna that was virtually unaffected by late Pleistocene glacial episodes. The episode of heavy extinction in Late Eocene time exhibits a similar phenomenon on a worldwide scale. Among the planktonic foraminifera, warm-adapted stenothermal species died out, and eurythermal forms predominated throughout Oligocene time; restoration of vulnerable, stenothermal species proceeded gradually during the Miocene Epoch. This example of delayed recovery and others like it following earlier global crises may have prevented such crises from following one another in rapid succession, yielding an appearance of periodicity.

The fossil record of non-marine tetrapods (amphibians, reptiles, birds and mammals) has been described by numerous authors1–3, and major ecological replacements, mass extinctions and adaptive radiations have been identified. However, most of these features of the large-scale evolution of tetrapods have been noted without numerical data of the kind assembled for marine invertebrates4–10, marine vertebrates7–10 and vascular land plants11. Much has been learnt from the record of marine invertebrates, particularly about the overall patterns of diversification with time, the performance of different major taxonomic groups at different times, and the magnitude and timing of mass extinctions. The present study tests some of the general conclusions on the basis of a new compilation of data on the fossil record of terrestrial tetrapods. I show that family diversity rose with time, and in particular from the Cretaceous to the present day. There were several mass extinction events, but none of these was associated with a statistically high extinction rate. The extinction events, including the famous terminal Cretaceous extinction, were the result of a slightly elevated extinction rate combined with a depressed origination rate, and the present evidence does not support the view that mass extinctions are statistically distinguishable from background extinctions. Further, the record of non-marine tetrapods shows an increasing total extinction rate and an only marginally decreasing probability of extinction (per-taxon rate) from the late Devonian to the present, the opposite of the findings from the record of marine animals.

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.

The discipline-wide effort to database the fossil record at the occurrence level has made it possible to estimate marine invertebrate extinction and origination rates with much greater accuracy. The new data show that two biotic mechanisms have hastened recoveries from mass extinctions and confined diversity to a relatively narrow range over the past 500 million years (Myr). First, a drop in diversity of any size correlates with low extinction rates immediately afterward, so much so that extinction would almost come to a halt if diversity dropped by 90%. Second, very high extinction rates are followed by equally high origination rates. The two relationships predict that the rebound from the current mass extinction will take at least 10 Myr, and perhaps 40 Myr if it rivals the Permo-Triassic catastrophe. Regardless, any large event will result in a dramatic ecological and taxonomic restructuring of the biosphere. The data also confirm that extinction and origination rates both declined through the Phanerozoic and that several extinctions in addition to the Permo-Triassic event were particularly severe. However, the trend may be driven by taxonomic biases and the rates vary in accord with a simple log normal distribution, so there is no sharp distinction between background and mass extinctions. Furthermore, the lack of any significant autocorrelation in the data is inconsistent with macroevolutionary theories of periodicity or self-organized criticality.

Brachiopods are a key group in Phanerozoic marine diversity analyses for their excellent fossil record and distinctive evolutionary history. A genus-level survey of raw diversity trajectories allows the identification of the Brachiopod Big Five, episodes of major genus losses in the phylum which are compared with the established Big Five mass extinctions of Phanerozoic marine invertebrates. The two lists differ in that the end-Cretaceous extinction appears subdued for brachiopods, whereas the mid-Carboniferous is recognized as an event with significant loss of brachiopod genera. At a higher taxonomic level, a review of temporal ranges of rhynchonelliform orders reveals episodes of synchronous termination of multiple orders, here termed clade extinctions. The end-Ordovician, Late Devonian and end-Permian events are registered as both mass extinctions and clade extinctions. The Late Cambrian and the Early Jurassic are identified as the other two clade extinction events. Coincident with the Early Toarcian oceanic anoxic event, the last clade extinction of brachiopods is defined by the disappearance of the last two spire-bearing orders, Athyridida and Spiriferinida. Their diversity trajectory through the recovery after the end-Permian crisis parallels that of the extant terebratulides and rhynchonellides until a Late Triassic peak but diverge afterwards. The end-Triassic diversity decline and Toarcian vanishing of spire-bearers correspond with contraction in their spatial distribution. The observed patterns and extinction selectivity may be explained both ecologically and physiologically. The specialized adaptation of morphologically diverse spire-bearers, as well as their fixed lophophore and passive feeding put them at a disadvantage at times of environmental crises, manifest in their end-Triassic near-extinction and Toarcian demise. Similar analyses of other clade extinctions may further improve our understanding of drivers and processes of extinction.

Abstract: Mass extinctions in the past have been characterized by abnormally high species extinction rates within almost all taxa. Attempts to estimate relative rates of extinction and threat among modern taxa, such as insects, plants, and vertebrates, are impeded by differences in the quality of information about each group. Insects and marine groups, for example, have much smaller percentages of known threatened species but also have many more undescribed species than do plants or vertebrates. I tested the possibility that all major groups have equally high rates of extinction and threat. The first test was a model assuming that differences in apparent global extinction and threat rate are caused by two sampling biases that produce artificially low rates in understudied taxa: (1) a common‐species bias in which taxonomists tend to record common (more extinction‐resistant) species first and (2) evaluative neglect, which is a tendency to spend relatively less effort evaluating the extinction and threat status of recorded species in understudied taxa. Global extinction and threat data from a number of groups generally follow the pattern predicted by this model. The second test shows that in direct measurements of extinction and threat between taxa in well‐studied regions, such as the United States and United Kingdom, the apparent global disparity among taxa is greatly reduced. Indeed, many globally understudied taxa, such as insects and other invertebrates, have higher rates of threat than many other taxa, including mammals, in these well‐studied areas. These two tests provide quantitative support for previous suggestions that the wide disparity in rates of species extinction and threat among groups represents an artifactual distortion of the actual rates. Specific suggestions for improved estimates of actual threat include (in order of increasing accuracy): use of well‐studied proxy taxa such as mammals; comparison of threat data among taxa only in well‐studied regions; and, especially important, increased efforts to evaluate the threat status of recorded species of understudied taxa.

According to when they attained high diversity, major taxa of marine animals have been clustered into three groups, the Cambrian, Paleozoic, and Modern Faunas. Because the Cambrian Fauna was a relatively minor component of the total fauna after mid-Ordovician time, the Phanerozoic history of marine animal diversity is largely a matter of the fates of the Paleozoic and Modern Faunas. The fact that most late Cenozoic genera belong to taxa that have been radiating for tens of millions of years indicates that the post-Paleozoic increase in diversity indicated by fossil data is real, rather than an artifact of improvement of the fossil record toward the present. Assuming that ecological crowding produced the so-called Paleozoic plateau for family diversity, various workers have used the logistic equation of ecology to model marine animal diversification as damped exponential increase. Several lines of evidence indicate that this procedure is inappropriate. A plot of the diversity of marine animal gene...

Documented extinctions of marine and anadromous species are rare, but extinction of species and extirpation of major populations have occurred – there are cases of near extinction – and there may be undocumented extinctions. Factors associated with known extinctions and near extinctions include specific life-history characteristics (e.g. low fecundity, high age at maturity, low mobility), habitat degradation, high value and high susceptibility to harvesting, ecological specialization. Harvesting mortality, targeted or incidental, is implicated in some known extinctions or near extinctions, and may act synergistically with other threats. Criteria to make assessments of risk of extinction more consistent have been developed, but given the limited experience to date with extinctions in the marine environment there have been questions about applying these to some marine species. The wide range of life history characteristics in marine species suggests that a range of approaches to assessing extinction risk will be needed. Protocols for defining significant population units are also required since protection of populations is part of protecting endangered species. Keeping species and populations well away from endangered status should be the main goal of conservation programmes. Implementation of precautionary conservation frameworks for exploited species could be a sound approach to preventing “endangerment”.

Biotic recovery after the end-Triassic extinction event: Evidence from marine bivalves of the Neuquén Basin, Argentina

Mass extinction events (MEEs), defined as significant losses of species diversity in significantly short time periods, have attracted the attention of biologists because of their link to major environmental change. MEEs have traditionally been studied through the fossil record, but the development of birth‐death models has made it possible to detect their signature based on extant‐taxa phylogenies. Most birth‐death models consider MEEs as instantaneous events where a high proportion of species are simultaneously removed from the tree (“single pulse” approach), in contrast to the paleontological record, where MEEs have a time duration. Here, we explore the power of a Bayesian Birth‐Death Skyline (BDSKY) model to detect the signature of MEEs through changes in extinction rates under a “time‐slice” approach. In this approach, MEEs are time intervals where the extinction rate is greater than the speciation rate. Results showed BDSKY can detect and locate MEEs but that precision and accuracy depend on the phylogeny's size and MEE intensity. Comparisons of BDSKY with the single‐pulse Bayesian model, CoMET, showed a similar frequency of Type II error and neither model exhibited Type I error. However, while CoMET performed better in detecting and locating MEEs for smaller phylogenies, BDSKY showed higher accuracy in estimating extinction and speciation rates.

Over 40years ago, Raup and Sepkoski identified five episodes of elevated extinction in the marine fossil record that were thought to be statistically distinct, thus warranting the term the "Big Five" mass extinctions. Since then, the term has become part of standard vocabulary, especially with the naming of the current biodiversity crisis as the "sixth mass extinction." However, there is no general agreement on which time intervals should be viewed as mass extinctions, in part because the Big Five turn out not to be statistically distinct from background rates of extinction, and in part, because other intervals of time have even higher extinction rates, in the Cambrian and early Ordovician. Nonetheless, the Big Five represent the five largest events since the early Ordovician, including in analyses that attempt to compensate for the incompleteness of the fossil and rock records. In the last 40years, we have learned a great deal about the causes of many of the major and minor extinction events and are beginning to unravel the mechanisms that translated the initial environmental disturbances into extinction. However, for many of the events, further understanding will require going back to the outcrop, where the patchy distribution of environments and pervasive temporal gaps in the rock record challenge our ability to establish true extinction patterns. As for the current biodiversity crisis, there is no doubt that the rate of extinction is among the highest ever experienced by the biosphere, perhaps the second highest after the end-Cretaceous bolide impact. However (and fortunately), the absolute number of extinctions is still relatively small - there is still time to prevent this becoming a genuine mass extinction. Given the arbitrariness of calling out the Big Five, perhaps the current crisis should be called the "incipient Anthropocene mass extinction" rather than the "sixth mass extinction."