Decreasing Phanerozoic extinction intensity as a consequence of Earth surface oxygenation and metazoan ecophysiology.

The decline in background extinction rates of marine animals through geologic time is an established but unexplained feature of the Phanerozoic fossil record. There is also growing consensus that the ocean and atmosphere did not become oxygenated to near-modern levels until the mid-Paleozoic, coinciding with the onset of generally lower extinction rates. Physiological theory provides us with a possible causal link between these two observations-predicting that the synergistic impacts of oxygen and temperature on aerobic respiration would have made marine animals more vulnerable to ocean warming events during periods of limited surface oxygenation. Here, we evaluate the hypothesis that changes in surface oxygenation exerted a first-order control on extinction rates through the Phanerozoic using a combined Earth system and ecophysiological modeling approach. We find that although continental configuration, the efficiency of the biological carbon pump in the ocean, and initial climate state all impact the magnitude of modeled biodiversity loss across simulated warming events, atmospheric oxygen is the dominant predictor of extinction vulnerability, with metabolic habitat viability and global ecophysiotype extinction exhibiting inflection points around 40% of present atmospheric oxygen. Given this is the broad upper limit for estimates of early Paleozoic oxygen levels, our results are consistent with the relative frequency of high-magnitude extinction events (particularly those not included in the canonical big five mass extinctions) early in the Phanerozoic being a direct consequence of limited early Paleozoic oxygenation and temperature-dependent hypoxia responses.

A high-resolution record of early Paleozoic climate.

The spatial coverage and temporal resolution of the Early Paleozoic paleoclimate record are limited, primarily due to the paucity of well-preserved skeletal material commonly used for oxygen-isotope paleothermometry. Bulk-rock [Formula: see text] datasets can provide broader coverage and higher resolution, but are prone to burial alteration. We assess the diagenetic character of two thick Cambro-Ordovician carbonate platforms with minimal to moderate burial by pairing clumped and bulk isotope analyses of micritic carbonates. Despite resetting of the clumped-isotope thermometer at both sites, our samples indicate relatively little change to their bulk [Formula: see text] due to low fluid exchange. Consequently, both sequences preserve temporal trends in [Formula: see text] Motivated by this result, we compile a global suite of bulk rock [Formula: see text] data, stacking overlapping regional records to minimize diagenetic influences on overall trends. We find good agreement of bulk rock [Formula: see text] with brachiopod and conodont [Formula: see text] trends through time. Given evidence that the [Formula: see text] value of seawater has not evolved substantially through the Phanerozoic, we interpret this record as primarily reflecting changes in tropical, nearshore seawater temperatures and only moderately modified by diagenesis. Focusing on the samples with the most enriched, and thus likely least-altered, [Formula: see text] values, we reconstruct Late Cambrian warming, Early Ordovician extreme warmth, and cooling around the Early-Middle Ordovician boundary. Our record is consistent with models linking the Great Ordovician Biodiversification Event to cooling of previously very warm tropical oceans. In addition, our high-temporal-resolution record suggests previously unresolved transient warming and climate instability potentially associated with Late Ordovician tectonic events.

Isotopes from fossil coronulid barnacle shells record evidence of migration in multiple Pleistocene whale populations.

Migration is an integral feature of modern mysticete whale ecology, and the demands of migration may have played a key role in shaping mysticete evolutionary history. Constraining when migration became established and assessing how it has changed through time may yield valuable insight into the evolution of mysticete whales and the oceans in which they lived. However, there are currently few data which directly assess prehistoric mysticete migrations. Here we show that calcite δ18O profiles of two species of modern whale barnacles (coronulids) accurately reflect the known migration routes of their host whales. We then analyze well-preserved fossil coronulids from three different locations along the eastern Pacific coast, finding that δ18O profiles from these fossils exhibit trends and ranges similar to modern specimens. Our results demonstrate that migration is an ancient behavior within the humpback and gray whale lineages and that multiple Pleistocene populations were undertaking migrations of an extent similar to those of the present day.

A signature of transience in bedrock river incision rates over timescales of 10(4)-10(7) years.

Measured rates of river incision into bedrock are commonly interpreted as proxies for rates of rock uplift (see refs 1 and 2, for example) and indices of the strength of climatic forcing of erosion over time (see refs 3 and 4, for example). This approach implicitly assumes that river incision rates are in equilibrium with external forcings over a wide range of timescales. Here we directly test this assumption by examining the temporal scaling of bedrock river incision from 155 independent measurements of river incision compiled from 14 sites. Of these sites, 11 exhibit a negative power-law dependence of bedrock river incision rate on measurement interval, a relationship that is apparent over timescales of 10(4)-10(7) years and is independent of tectonic and geomorphic setting. Thus, like rates of sediment accumulation, rates of river incision into bedrock exhibit non-steady-state behaviour even over very long measurement intervals. Non-steady-state behaviour can be explained by episodic hiatuses in river incision triggered by alluvial deposition, if such hiatuses have a heavy-tailed length distribution. Regardless of its cause, the dependence of incision rate on measurement interval complicates efforts to infer tectonic or climatic forcing from changes in rates of river incision over time or from comparison of rates computed over different timescales.

Plate tectonic regulation of global marine animal diversity.

Valentine and Moores [Valentine JW, Moores EM (1970) Nature 228:657-659] hypothesized that plate tectonics regulates global biodiversity by changing the geographic arrangement of continental crust, but the data required to fully test the hypothesis were not available. Here, we use a global database of marine animal fossil occurrences and a paleogeographic reconstruction model to test the hypothesis that temporal patterns of continental fragmentation have impacted global Phanerozoic biodiversity. We find a positive correlation between global marine invertebrate genus richness and an independently derived quantitative index describing the fragmentation of continental crust during supercontinental coalescence-breakup cycles. The observed positive correlation between global biodiversity and continental fragmentation is not readily attributable to commonly cited vagaries of the fossil record, including changing quantities of marine rock or time-variable sampling effort. Because many different environmental and biotic factors may covary with changes in the geographic arrangement of continental crust, it is difficult to identify a specific causal mechanism. However, cross-correlation indicates that the state of continental fragmentation at a given time is positively correlated with the state of global biodiversity for tens of millions of years afterward. There is also evidence to suggest that continental fragmentation promotes increasing marine richness, but that coalescence alone has only a small negative or stabilizing effect. Together, these results suggest that continental fragmentation, particularly during the Mesozoic breakup of the supercontinent Pangaea, has exerted a first-order control on the long-term trajectory of Phanerozoic marine animal diversity.

Hierarchical complexity and the size limits of life.

Over the past 3.8 billion years, the maximum size of life has increased by approximately 18 orders of magnitude. Much of this increase is associated with two major evolutionary innovations: the evolution of eukaryotes from prokaryotic cells approximately 1.9 billion years ago (Ga), and multicellular life diversifying from unicellular ancestors approximately 0.6 Ga. However, the quantitative relationship between organismal size and structural complexity remains poorly documented. We assessed this relationship using a comprehensive dataset that includes organismal size and level of biological complexity for 11 172 extant genera. We find that the distributions of sizes within complexity levels are unimodal, whereas the aggregate distribution is multimodal. Moreover, both the mean size and the range of size occupied increases with each additional level of complexity. Increases in size range are non-symmetric: the maximum organismal size increases more than the minimum. The majority of the observed increase in organismal size over the history of life on the Earth is accounted for by two discrete jumps in complexity rather than evolutionary trends within levels of complexity. Our results provide quantitative support for an evolutionary expansion away from a minimal size constraint and suggest a fundamental rescaling of the constraints on minimal and maximal size as biological complexity increases.

Identifying the most surprising victims of mass extinction events: an example using Late Ordovician brachiopods.

Mass extinction events are recognized by increases in extinction rate and magnitude and, often, by changes in the selectivity of extinction. When considering the selective fingerprint of a particular event, not all taxon extinctions are equally informative: some would be expected even under a 'background' selectivity regime, whereas others would not and thus require special explanation. When evaluating possible drivers for the extinction event, the latter group is of particular interest. Here, we introduce a simple method for identifying these most surprising victims of extinction events by training models on background extinction intervals and using these models to make per-taxon assessments of 'expected' risk during the extinction interval. As an example, we examine brachiopod genus extinctions during the Late Ordovician Mass Extinction and show that extinction of genera in the deep-water 'Foliomena fauna' was particularly unexpected given preceding Late Ordovician extinction patterns.

Biogeographic and bathymetric determinants of brachiopod extinction and survival during the Late Ordovician mass extinction.

The Late Ordovician mass extinction (LOME) coincided with dramatic climate changes, but there are numerous ways in which these changes could have driven marine extinctions. We use a palaeobiogeographic database of rhynchonelliform brachiopods to examine the selectivity of Late Ordovician-Early Silurian genus extinctions and evaluate which extinction drivers are best supported by the data. The first (latest Katian) pulse of the LOME preferentially affected genera restricted to deeper waters or to relatively narrow (less than 35°) palaeolatitudinal ranges. This pattern is only observed in the latest Katian, suggesting that it reflects drivers unique to this interval. Extinction of exclusively deeper-water genera implies that changes in water mass properties such as dissolved oxygen content played an important role. Extinction of genera with narrow latitudinal ranges suggests that interactions between shifting climate zones and palaeobiogeography may also have been important. We test the latter hypothesis by estimating whether each genus would have been able to track habitats within its thermal tolerance range during the greenhouse-icehouse climate transition. Models including these estimates are favoured over alternative models. We argue that the LOME, long regarded as non-selective, is highly selective along biogeographic and bathymetric axes that are not closely correlated with taxonomic identity.

Marine extinction risk shaped by trait-environment interactions over 500 million years.

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait-based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta-analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait-based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life-habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow-ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3-3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.

Climate change and the selective signature of the Late Ordovician mass extinction.

Selectivity patterns provide insights into the causes of ancient extinction events. The Late Ordovician mass extinction was related to Gondwanan glaciation; however, it is still unclear whether elevated extinction rates were attributable to record failure, habitat loss, or climatic cooling. We examined Middle Ordovician-Early Silurian North American fossil occurrences within a spatiotemporally explicit stratigraphic framework that allowed us to quantify rock record effects on a per-taxon basis and assay the interplay of macrostratigraphic and macroecological variables in determining extinction risk. Genera that had large proportions of their observed geographic ranges affected by stratigraphic truncation or environmental shifts at the end of the Katian stage were particularly hard hit. The duration of the subsequent sampling gaps had little effect on extinction risk, suggesting that this extinction pulse cannot be entirely attributed to rock record failure; rather, it was caused, in part, by habitat loss. Extinction risk at this time was also strongly influenced by the maximum paleolatitude at which a genus had previously been sampled, a macroecological trait linked to thermal tolerance. A model trained on the relationship between 16 explanatory variables and extinction patterns during the early Katian interval substantially underestimates the extinction of exclusively tropical taxa during the late Katian interval. These results indicate that glacioeustatic sea-level fall and tropical ocean cooling played important roles in the first pulse of the Late Ordovician mass extinction in Laurentia.

Using the Fossil Record to Understand Extinction Risk and Inform Marine Conservation in a Changing World.

Understanding the long-term effects of ongoing global environmental change on marine ecosystems requires a cross-disciplinary approach. Deep-time and recent fossil records can contribute by identifying traits and environmental conditions associated with elevated extinction risk during analogous events in the geologic past and by providing baseline data that can be used to assess historical change and set management and restoration targets and benchmarks. Here, we review the ecological and environmental information available in the marine fossil record and discuss how these archives can be used to inform current extinction risk assessments as well as marine conservation strategies and decision-making at global to local scales. As we consider future research directions in deep-time and conservationpaleobiology, we emphasize the need for coproduced research that unites researchers, conservation practitioners, and policymakers with the communities for whom the impacts of climate and global change are most imminent.

An 800-year record of benthic foraminifer images and 2D morphometrics from the Santa Barbara Basin.

The Santa Barbara Basin is an extraordinary archive of environmental and ecological change, where varved sediments preserve microfossils that provide an annual to decadal record of the dynamics of surrounding ecosystems. Of the microfossils preserved in these sediments, benthic foraminifera are the most abundant seafloor-dwelling organisms. While they have been extensively utilized for geochemical and paleoceanographic work, studies of their morphology are lacking. Here we use a high-throughput imaging method (AutoMorph) designed to extract 2D data from photographic images of fossils to produce a large image and 2D shape dataset of recent benthic foraminifera from two core records sampled from the center of the Santa Barbara Basin that span an ~800-year-long interval during the Common Era (1249-2008 CE). Information on more than 36,000 objects is included, of which more than 22,000 are complete or partially-damaged benthic foraminifera. The dataset also includes other biogenic microfossils including ostracods, pteropods, diatoms, radiolarians, fish teeth, and shark dermal denticles. We describe our sample preparation, imaging, and identification techniques, and outline potential data uses.

Was the Late Ordovician mass extinction truly exceptional?

The Late Ordovician mass extinction event is the oldest of the five great extinction events in the fossil record. It has long been regarded as an outlier among mass extinctions, primarily due to its association with a cooling climate. However, recent temporally better resolved fossil biodiversity estimates complicate this view, providing growing evidence for a prolonged but punctuated biodiversity decline modulated by changes in atmospheric composition, ocean chemistry, and viable habitat area. This evolving view invokes extinction drivers similar to those that occurred during other major extinctions; some are even factors in the current human-induced biodiversity crisis. Even this very ancient and, at first glance, exceptional event conveys important lessons about the intensifying 'sixth mass extinction'.

Why the Early Paleozoic was intrinsically prone to marine extinction.

The geological record of marine animal biodiversity reflects the interplay between changing rates of speciation versus extinction. Compared to mass extinctions, background extinctions have received little attention. To disentangle the different contributions of global climate state, continental configuration, and atmospheric oxygen concentration (pO2) to variations in background extinction rates, we drive an animal physiological model with the environmental outputs from an Earth system model across intervals spanning the past 541 million years. We find that climate and continental configuration combined to make extinction susceptibility an order of magnitude higher during the Early Paleozoic than during the rest of the Phanerozoic, consistent with extinction rates derived from paleontological databases. The high extinction susceptibility arises in the model from the limited geographical range of marine organisms. It stands even when assuming present-day pO2, suggesting that increasing oxygenation through the Paleozoic is not necessary to explain why extinction rates apparently declined with time.

Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity.

The maximum size of organisms has increased enormously since the initial appearance of life >3.5 billion years ago (Gya), but the pattern and timing of this size increase is poorly known. Consequently, controls underlying the size spectrum of the global biota have been difficult to evaluate. Our period-level compilation of the largest known fossil organisms demonstrates that maximum size increased by 16 orders of magnitude since life first appeared in the fossil record. The great majority of the increase is accounted for by 2 discrete steps of approximately equal magnitude: the first in the middle of the Paleoproterozoic Era (approximately 1.9 Gya) and the second during the late Neoproterozoic and early Paleozoic eras (0.6-0.45 Gya). Each size step required a major innovation in organismal complexity--first the eukaryotic cell and later eukaryotic multicellularity. These size steps coincide with, or slightly postdate, increases in the concentration of atmospheric oxygen, suggesting latent evolutionary potential was realized soon after environmental limitations were removed.

The evolutionary consequences of oxygenic photosynthesis: a body size perspective.

The high concentration of molecular oxygen in Earth's atmosphere is arguably the most conspicuous and geologically important signature of life. Earth's early atmosphere lacked oxygen; accumulation began after the evolution of oxygenic photosynthesis in cyanobacteria around 3.0-2.5 billion years ago (Gya). Concentrations of oxygen have since varied, first reaching near-modern values ~600 million years ago (Mya). These fluctuations have been hypothesized to constrain many biological patterns, among them the evolution of body size. Here, we review the state of knowledge relating oxygen availability to body size. Laboratory studies increasingly illuminate the mechanisms by which organisms can adapt physiologically to the variation in oxygen availability, but the extent to which these findings can be extrapolated to evolutionary timescales remains poorly understood. Experiments confirm that animal size is limited by experimental hypoxia, but show that plant vegetative growth is enhanced due to reduced photorespiration at lower O(2):CO(2). Field studies of size distributions across extant higher taxa and individual species in the modern provide qualitative support for a correlation between animal and protist size and oxygen availability, but few allow prediction of maximum or mean size from oxygen concentrations in unstudied regions. There is qualitative support for a link between oxygen availability and body size from the fossil record of protists and animals, but there have been few quantitative analyses confirming or refuting this impression. As oxygen transport limits the thickness or volume-to-surface area ratio-rather than mass or volume-predictions of maximum possible size cannot be constructed simply from metabolic rate and oxygen availability. Thus, it remains difficult to confirm that the largest representatives of fossil or living taxa are limited by oxygen transport rather than other factors. Despite the challenges of integrating findings from experiments on model organisms, comparative observations across living species, and fossil specimens spanning millions to billions of years, numerous tractable avenues of research could greatly improve quantitative constraints on the role of oxygen in the macroevolutionary history of organismal size.

How predictable is extinction? Forecasting species survival at million-year timescales.

A tenet of conservation palaeobiology is that knowledge of past extinction patterns can help us to better predict future extinctions. Although the future is unobservable, we can test the strength of this proposition by asking how well models conditioned on past observations would have predicted subsequent extinction events at different points in the geological past. To answer this question, we analyse the well-sampled fossil record of Cenozoic planktonic microfossil taxa (Foramanifera, Radiolaria, diatoms and calcareous nanoplankton). We examine how extinction probability varies over time as a function of species age, time of observation, current geographical range, change in geographical range, climate state and change in climate state. Our models have a 70-80% probability of correctly forecasting the rank order of extinction risk for a random out-of-sample species pair, implying that determinants of extinction risk have varied only modestly through time. We find that models which include either historical covariates or account for variation in covariate effects over time yield equivalent forecasts, but a model including both is overfit and yields biased forecasts. An important caveat is that human impacts may substantially disrupt range-risk dynamics so that the future will be less predictable than it has been in the past. This article is part of a discussion meeting issue 'The past is a foreign country: how much can the fossil record actually inform conservation?'

Twelve thousand recent patellogastropods from a northeastern Pacific latitudinal gradient.

Body size distributions can vary widely among communities, with important implications for ecological dynamics, energetics, and evolutionary history. Here we present a dataset of body size and shape for 12,035 extant Patellogastropoda (true limpet) specimens from the collections of the University of California Museum of Paleontology, compiled using a novel high-throughput morphometric imaging method. These specimens were collected over the past 150 years at 355 localities along a latitudinal gradient ranging from Alaska to Baja California, Mexico and are presented here with individual images, 2D outline coordinates, and 2D measurements of body size and shape. This dataset provides a resource for assemblage-scale macroecological questions and documents the size and diversity of recent patellogastropods in the northeastern Pacific.

Increase in predator-prey size ratios throughout the Phanerozoic history of marine ecosystems.

The escalation hypothesis posits that predation by increasingly powerful and metabolically active carnivores has been a major driver of metazoan evolution. We test a key tenet of this hypothesis by analyzing predatory drill holes in fossil marine shells, which provide a ~500-million-year record of individual predator-prey interactions. We show that drill-hole size is a robust predictor of body size among modern drilling predators and that drill-hole size (and thus inferred predator size and power) rose substantially from the Ordovician to the Quaternary period, whereas the size of drilled prey remained stable. Together, these trends indicate a directional increase in predator-prey size ratios. We hypothesize that increasing predator-prey size ratios reflect increases in prey abundance, prey nutrient content, and predation among predators.

Formation of the Isthmus of Panama.

The formation of the Isthmus of Panama stands as one of the greatest natural events of the Cenozoic, driving profound biotic transformations on land and in the oceans. Some recent studies suggest that the Isthmus formed many millions of years earlier than the widely recognized age of approximately 3 million years ago (Ma), a result that if true would revolutionize our understanding of environmental, ecological, and evolutionary change across the Americas. To bring clarity to the question of when the Isthmus of Panama formed, we provide an exhaustive review and reanalysis of geological, paleontological, and molecular records. These independent lines of evidence converge upon a cohesive narrative of gradually emerging land and constricting seaways, with formation of the Isthmus of Panama sensu stricto around 2.8 Ma. The evidence used to support an older isthmus is inconclusive, and we caution against the uncritical acceptance of an isthmus before the Pliocene.