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.

Shifts in sexual dimorphism across a mass extinction in ostracods: implications for sexual selection as a factor in extinction risk.

Sexual selection often favours investment in expensive sexual traits that help individuals compete for mates. In a rapidly changing environment, however, allocation of resources to traits related to reproduction at the expense of those related to survival may elevate extinction risk. Empirical testing of this hypothesis in the fossil record, where extinction can be directly documented, is largely lacking. The rich fossil record of cytheroid ostracods offers a unique study system in this context: the male shell is systematically more elongate than that of females, and thus the sexes can be distinguished, even in fossils. Using mixture models to identify sex clusters from size and shape variables derived from the digitized valve outlines of adult ostracods, we estimated sexual dimorphism in ostracod species before and after the Cretaceous/Palaeogene mass extinction in the United States Coastal Plain. Across this boundary, we document a substantial shift in sexual dimorphism, driven largely by a pronounced decline in the taxa with dimorphism indicating both very high and very low male investment. The shift away from high male investment, which arises largely from evolutionary changes within genera that persist through the extinction, parallels extinction selectivity previously documented during the Late Cretaceous under a background extinction regime. Our results suggest that sexual selection and the allocation of resources towards survival versus reproduction may be an important factor for species extinction during both background and mass extinctions.

A conservation palaeobiological perspective on Chesapeake Bay oysters.

The eastern oyster plays a vital role in estuarine habitats, acting as an ecosystem engineer and improving water quality. Populations of Chesapeake Bay oysters have declined precipitously in recent decades. The fossil record, which preserves 500 000 years of once-thriving reefs, provides a unique opportunity to study pristine reefs to establish a possible baseline for mitigation. For this study, over 900 fossil oysters were examined from three Pleistocene localities in the Chesapeake region. Data on oyster shell lengths, lifespans and population density were assessed. Comparisons to modern Crassostrea virginica, sampled from monitoring surveys of similar environments, reveal that fossil oysters were significantly larger, longer-lived and more abundant than modern oysters from polyhaline salinity zones. This pattern results from the preferential harvesting of larger, reproductively more active females from the modern population. These fossil data, combined with modern estimates of age-based fecundity and mortality, make it possible to estimate ecosystem services in these long-dead reefs, including filtering capacity, which was an order of magnitude greater in the past than today. Conservation palaeobiology can provide us with a picture of not just what the Chesapeake Bay looked like, but how it functioned, before humans. This article is part of a discussion meeting issue 'The past is a foreign country: how much can the fossil record actually inform conservation?'

Little lasting impact of the Paleocene-Eocene Thermal Maximum on shallow marine molluscan faunas.

Global warming, acidification, and oxygen stress at the Paleocene-Eocene Thermal Maximum (PETM) are associated with severe extinction in the deep sea and major biogeographic and ecologic changes in planktonic and terrestrial ecosystems, yet impacts on shallow marine macrofaunas are obscured by the incompleteness of shelf sections. We analyze mollusk assemblages bracketing (but not including) the PETM and find few notable lasting impacts on diversity, turnover, functional ecology, body size, or life history of important clades. Infaunal and chemosymbiotic taxa become more common, and body size and abundance drop in one clade, consistent with hypoxia-driven selection, but within-clade changes are not generalizable across taxa. While an unrecorded transient response is still possible, the long-term evolutionary impact is minimal. Adaptation to already-warm conditions and slow release of CO2 relative to the time scale of ocean mixing likely buffered the impact of PETM climate change on shelf faunas.

High male sexual investment as a driver of extinction in fossil ostracods.

Sexual selection favours traits that confer advantages in the competition for mates. In many cases, such traits are costly to produce and maintain, because the costs help to enforce the honesty of these signals and cues 1 . Some evolutionary models predict that sexual selection also produces costs at the population level, which could limit the ability of populations to adapt to changing conditions and thus increase the risk of extinction2-4. Other models, however, suggest that sexual selection should increase rates of adaptation and enhance the removal of deleterious mutations, thus protecting populations against extinction3, 5, 6. Resolving the conflict between these models is not only important for explaining the history of biodiversity, but also relevant to understanding the mechanisms of the current biodiversity crisis. Previous attempts to test the conflicting predictions produced by these models have been limited to extant species and have thus relied on indirect proxies for species extinction. Here we use the informative fossil record of cytheroid ostracods-small, bivalved crustaceans with sexually dimorphic carapaces-to test how sexual selection relates to actual species extinction. We show that species with more pronounced sexual dimorphism, indicating the highest levels of male investment in reproduction, had estimated extinction rates that were ten times higher than those of the species with the lowest investment. These results indicate that sexual selection can be a substantial risk factor for extinction.

Correlation between investment in sexual traits and valve sexual dimorphism in Cyprideis species (Ostracoda).

Assessing the long-term macroevolutionary consequences of sexual selection has been hampered by the difficulty of studying this process in the fossil record. Cytheroid ostracodes offer an excellent system to explore sexual selection in the fossil record because their readily fossilized carapaces are sexually dimorphic. Specifically, males are relatively more elongate than females in this superfamily. This sexual shape difference is thought to arise so that males carapaces can accommodate their very large copulatory apparatus, which can account for up to one-third of body volume. Here we test this widely held explanation for sexual dimorphism in cytheroid ostracodes by correlating investment in male genitalia, a trait in which sexual selection is seen as the main evolutionary driver, with sexual dimorphism of carapace in the genus Cyprideis. We analyzed specimens collected in the field (C. salebrosa, USA; C. torosa, UK) and from collections of the National Museum of Natural History, Washington, DC (C. mexicana). We digitized valve outlines in lateral view to obtain measures of size (valve area) and shape (elongation, measured as length to height ratio), and obtained several dimensions from two components of the hemipenis: the muscular basal capsule, which functions as a sperm pump, and the section that includes the intromittent organ (terminal extension). In addition to the assessment of this primary sexual trait, we also quantified two dimensions of the male secondary sexual trait-where the transformed right walking leg functions as a clasping organ during mating. We also measured linear dimensions from four limbs as indicators of overall (soft-part) body size, and assessed allometry of the soft anatomy. We observed significant correlations in males between valve size, but not elongation, and distinct structural parts of the hemipenis, even after accounting for their shared correlation with overall body size. We also found weak but significant positive correlation between valve elongation and the degree of sexual dimorphism of the walking leg, but only in C. torosa. The correlation between the hemipenis parts, especially basal capsule size and male valve size dimorphism suggests that sexual selection on sperm size, quantity, and/or efficiency of transfer may drive sexual size dimorphism in these species, although we cannot exclude other aspects of sexual and natural selection.

Millennial-scale sustainability of the Chesapeake Bay Native American oyster fishery.

Estuaries around the world are in a state of decline following decades or more of overfishing, pollution, and climate change. Oysters (Ostreidae), ecosystem engineers in many estuaries, influence water quality, construct habitat, and provide food for humans and wildlife. In North America's Chesapeake Bay, once-thriving eastern oyster (Crassostrea virginica) populations have declined dramatically, making their restoration and conservation extremely challenging. Here we present data on oyster size and human harvest from Chesapeake Bay archaeological sites spanning ∼3,500 y of Native American, colonial, and historical occupation. We compare oysters from archaeological sites with Pleistocene oyster reefs that existed before human harvest, modern oyster reefs, and other records of human oyster harvest from around the world. Native American fisheries were focused on nearshore oysters and were likely harvested at a rate that was sustainable over centuries to millennia, despite changing Holocene climatic conditions and sea-level rise. These data document resilience in oyster populations under long-term Native American harvest, sea-level rise, and climate change; provide context for managing modern oyster fisheries in the Chesapeake Bay and elsewhere around the world; and demonstrate an interdisciplinary approach that can be applied broadly to other fisheries.

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.

Extinctions. Paleontological baselines for evaluating extinction risk in the modern oceans.

Marine taxa are threatened by anthropogenic impacts, but knowledge of their extinction vulnerabilities is limited. The fossil record provides rich information on past extinctions that can help predict biotic responses. We show that over 23 million years, taxonomic membership and geographic range size consistently explain a large proportion of extinction risk variation in six major taxonomic groups. We assess intrinsic risk-extinction risk predicted by paleontologically calibrated models-for modern genera in these groups. Mapping the geographic distribution of these genera identifies coastal biogeographic provinces where fauna with high intrinsic risk are strongly affected by human activity or climate change. Such regions are disproportionately in the tropics, raising the possibility that these ecosystems may be particularly vulnerable to future extinctions. Intrinsic risk provides a prehuman baseline for considering current threats to marine biodiversity.

Integrating paleobiology, archeology, and history to inform biological conservation.

The search for novel approaches to establishing ecological baselines (reference conditions) is constrained by the fact that most ecological studies span the past few decades, at most, and investigate ecosystems that have been substantially altered by human activities for decades, centuries, or more. Paleobiology, archeology, and history provide historical ecological context for biological conservation, remediation, and restoration. We argue that linking historical ecology explicitly with conservation can help unify related disciplines of conservation paleobiology, conservation archeobiology, and environmental history. Differences in the spatial and temporal resolution and extent (scale) of prehistoric, historic, and modern ecological data remain obstacles to integrating historical ecology and conservation biology, but the prolonged temporal extents of historical ecological data can help establish more complete baselines for restoration, document a historical range of ecological variability, and assist in determining desired future conditions. We used the eastern oyster (Crassostrea virginica) fishery of the Chesapeake Bay (U.S.A.) to demonstrate the utility of historical ecological data for elucidating oyster conservation and the need for an approach to conservation that transcends disciplinary boundaries. Historical ecological studies from the Chesapeake have documented dramatic declines (as much as 99%) in oyster abundance since the early to mid-1800 s, changes in oyster size in response to different nutrient levels from the sixteenth to nineteenth centuries, and substantial reductions in oyster accretion rates (from 10 mm/year to effectively 0 mm/year) from the Late Holocene to modern times. Better integration of different historical ecological data sets and increased collaboration between paleobiologists, geologists, archeologists, environmental historians, and ecologists to create standardized research designs and methodologies will help unify prehistoric, historic, and modern time perspectives on biological conservation.

Extinctions in ancient and modern seas.

In the coming century, life in the ocean will be confronted with a suite of environmental conditions that have no analog in human history. Thus, there is an urgent need to determine which marine species will adapt and which will go extinct. Here, we review the growing literature on marine extinctions and extinction risk in the fossil, historical, and modern records to compare the patterns, drivers, and biological correlates of marine extinctions at different times in the past. Characterized by markedly different environmental states, some past periods share common features with predicted future scenarios. We highlight how the different records can be integrated to better understand and predict the impact of current and projected future environmental changes on extinction risk in the ocean.

Abundance not linked to survival across the end-Cretaceous mass extinction: patterns in North American bivalves.

Ecological studies suggest that rare taxa are more likely to go extinct than abundant ones, but the influence of abundance on survivorship in the fossil record has received little attention. An analysis of Late Maastrichtian bivalve subgenera from the North American Coastal Plain found no evidence that survivorship is tied to abundance across the end-Cretaceous mass extinction (65 million years ago), regardless of abundance metric or spatial scale examined. The fact that abundance does not promote survivorship in end-Cretaceous bivalves suggests that the factors influencing survivorship during mass extinctions in the fossil record may differ from those operating during intervals of background extinction.