Pincelli M. Hull

Marine Ecosystem Responses to Cenozoic Global Change

The future impacts of anthropogenic global change on marine ecosystems are highly uncertain, but insights can be gained from past intervals of high atmospheric carbon dioxide partial pressure. The long-term geological record reveals an early Cenozoic warm climate that supported smaller polar ecosystems, few coral-algal reefs, expanded shallow-water platforms, longer food chains with less energy for top predators, and a less oxygenated ocean than today. The closest analogs for our likely future are climate transients, 10,000 to 200,000 years in duration, that occurred during the long early Cenozoic interval of elevated warmth. Although the future ocean will begin to resemble the past greenhouse world, it will retain elements of the present “icehouse” world long into the future. Changing temperatures and ocean acidification, together with rising sea level and shifts in ocean productivity, will keep marine ecosystems in a state of continuous change for 100,000 years.

The temporal dimension of marine speciation

Speciation is a process that occurs over time and, as such, can only be fully understood in an explicitly temporal context. Here we discuss three major consequences of speciation’s extended duration. First, the dynamism of environmental change indicates that nascent species may experience repeated changes in population size, genetic diversity, and geographic distribution during their evolution. The present characteristics of species therefore represents a static snapshot of a single time point in a species’ highly dynamic history, and impedes inferences about the strength of selection or the geography of speciation. Second, the process of speciation is open ended—ecological divergence may evolve in the space of a few generations while the fixation of genetic differences and traits that limit outcrossing may require thousands to millions of years to occur. As a result, speciation is only fully recognized long after it occurs, and short-lived species are difficult to discern. Third, the extinction of species or of clades provides a simple, under-appreciated, mechanism for the genetic, biogeographic, and behavioral ‘gaps’ between extant species. Extinction also leads to the systematic underestimation of the frequency of speciation and the overestimation of the duration of species formation. Hence, it is no surprise that a full understanding of speciation has been difficult to achieve. The modern synthesis—which united genetics, development, ecology, biogeography, and paleontology—greatly advanced the study of evolution. Here we argue that a similarly synthetic approach must be taken to further our understanding of the origin of species.

Rarity in mass extinctions and the future of ecosystems.

The fossil record provides striking case studies of biodiversity loss and global ecosystem upheaval. Because of this, many studies have sought to assess the magnitude of the current biodiversity crisis relative to past crises—a task greatly complicated by the need to extrapolate extinction rates. Here we challenge this approach by showing that the rarity of previously abundant taxa may be more important than extinction in the cascade of events leading to global changes in the biosphere. Mass rarity may provide the most robust measure of our current biodiversity crisis relative to those past, and new insights into the dynamics of mass extinction.

Evidence for abrupt speciation in a classic case of gradual evolution

In contrast with speciation in terrestrial organisms, marine plankton frequently display gradual morphological change without lineage division (e.g., phyletic gradualism or gradual evolution), which has raised the possibility that a different mode of evolution dominates within pelagic environments. Here, we reexamine a classic case of putative gradual evolution within the Globorotalia plesiotumida–G. tumida lineage of planktonic foraminifera, and find both compelling evidence for the existence of a third cryptic species during the speciation event and the abrupt evolution of the descendant G. tumida. The third morphotype, not recognized in previous analyses, differs in shape and coiling direction from its ancestor, G. plesiotumida. This species dominates the globorotaliid population for 414,000 years just before the appearance of G. tumida. The first population of the descendant, G. tumida, evolves abruptly within a 44,000-year interval. A combination of morphological data and biostratigraphic evidence suggests that G. tumida evolved by cladogenesis. Our findings provide an unexpected twist on one of the best-documented cases of within-lineage phyletic gradualism and, in doing so, revisit the limitations and promise of the study of speciation in the fossil record.

Environmental and biological controls on size‐specific δ13C and δ18O in recent planktonic foraminifera

As living organisms, planktonic foraminifera are not passive tracers of the environment. Their test geochemistry—arguably the single most important resource for paleoceanographic research—reflects the combined signal of environmental, biological, and preservational processes. For most species, comparisons of test stable isotopic composition within and among taxa provide the primary means for disentangling the relative influences of these different processes. Here we test the foundations of our paleoceanographic interpretations with the first quantitative comparison of the determinants of carbon and oxygen isotopic variation across multiple ocean basins, studies, and species by re-analyzing size-specific data collated from the literature. We find clear evidence of species-specific biological effects (i.e., vital effects), as the intercepts of size-specific carbon and oxygen isotopic compositions differ significantly among species. Trends in body size and isotopic composition, particularly in dinoflagellate bearing taxa, suggest that much of the size-dependent isotopic variation observed in death assemblages (i.e., core tops and sediments) relates to factors influencing the maximum size obtained by adults rather than ontogeny. The presence and type of photosymbiont hosted (dinoflagellate, chrysophyte, or none) were a major factor affecting species- and size-specific ?18O values. In contrast, size-related trends in ?13C values were driven by depth habitat (mixed layer, thermocline, subthermocline), symbiont ecology and whether the assemblage was alive or dead when sampled. On this broad geographic and oceanographic scale, ocean basin and biome had a significant effect on ?18O and ?13C values . Our analysis and its model-averaged predictions provide a quantitative basis for interpreting size-specific isotopic variation in 22 species of modern macroperforate planktonic foraminifera. We conclude by highlighting existing data gaps and outstanding questions of the relative influence of environmental, preservational, and biological processes on variation in the test geochemistry of planktonic foraminifera.

Life in the Aftermath of Mass Extinctions

The vast majority of species that have ever lived went extinct sometime other than during one of the great mass extinction events. In spite of this, mass extinctions are thought to have outsized effects on the evolutionary history of life. While part of this effect is certainly due to the extinction itself, I here consider how the aftermaths of mass extinctions might contribute to the evolutionary importance of such events. Following the mass loss of taxa from the fossil record are prolonged intervals of ecological upheaval that create a selective regime unique to those times. The pacing and duration of ecosystem change during extinction aftermaths suggests strong ties between the biosphere and geosphere, and a previously undescribed macroevolutionary driver - earth system succession. Earth system succession occurs when global environmental or biotic change, as occurs across extinction boundaries, pushes the biosphere and geosphere out of equilibrium. As species and ecosystems re-evolve in the aftermath, they change global biogeochemical cycles - and in turn, species and ecosystems - over timescales typical of the geosphere, often many thousands to millions of years. Earth system succession provides a general explanation for the pattern and timing of ecological and evolutionary change in the fossil record. Importantly, it also suggests that a speed limit might exist for the pace of global biotic change after massive disturbance - a limit set by geosphere-biosphere interactions. For mass extinctions, earth system succession may drive the ever-changing ecological stage on which species evolve, restructuring ecosystems and setting long-term evolutionary trajectories as they do.

Biogeochemical significance of pelagic ecosystem function: an end-Cretaceous case study.

Pelagic ecosystem function is integral to global biogeochemical cycling, and plays a major role in modulating atmospheric CO2 concentrations (pCO2). Uncertainty as to the effects of human activities on marine ecosystem function hinders projection of future atmospheric pCO2. To this end, events in the geological past can provide informative case studies in the response of ecosystem function to environmental and ecological changes. Around the Cretaceous–Palaeogene (K–Pg) boundary, two such events occurred: Deccan large igneous province (LIP) eruptions and massive bolide impact at the Yucatan Peninsula. Both perturbed the environment, but only the impact coincided with marine mass extinction. As such, we use these events to directly contrast the response of marine biogeochemical cycling to environmental perturbation with and without changes in global species richness. We measure this biogeochemical response using records of deep-sea carbonate preservation. We find that Late Cretaceous Deccan volcanism prompted transient deep-sea carbonate dissolution of a larger magnitude and timescale than predicted by geochemical models. Even so, the effect of volcanism on carbonate preservation was slight compared with bolide impact. Empirical records and geochemical models support a pronounced increase in carbonate saturation state for more than 500 000 years following the mass extinction of pelagic carbonate producers at the K–Pg boundary. These examples highlight the importance of pelagic ecosystems in moderating climate and ocean chemistry.

Chromium isotopic composition of core-top planktonic foraminifera

The chromium isotope system (53 Cr/52 Cr expressed as δ53 Cr relative to NIST SRM 979) is potentially a powerful proxy for the redox state of the ocean-atmosphere system, but a lack of temporally continuous, well-calibrated archives has limited its application to date. Marine carbonates could potentially serve as a common and continuous Cr isotope archive. Here, we present the first evaluation of planktonic foraminiferal calcite as an archive of seawater δ53 Cr. We show that single foraminiferal species from globally distributed core tops yielded variable δ53 Cr, ranging from 0.1‰ to 2.5‰. These values do not match with the existing measurements of seawater δ53 Cr. Further, within a single core-top, species with similar water column distributions (i.e., depth habitats) yielded variable δ53 Cr values. In addition, mixed layer and thermocline species do not consistently exhibit decreasing trends in δ53 Cr as expected based on current understanding of Cr cycling in the ocean. These observations suggest that either seawater δ53 Cr is more heterogeneous than previously thought or that there is significant and species-dependent Cr isotope fractionation during foraminiferal calcification. Given that the δ53 Cr variability is comparable to that observed in geological samples throughout Earths history, interpreting planktonic foraminiferal δ53 Cr without calibrating modern foraminifera further, and without additional seawater measurements, would lead to erroneous conclusions. Our core-top survey clearly indicates that planktonic foraminifera are not a straightforward δ53 Cr archive and should not be used to study marine redox evolution without additional study. It likewise cautions against the use of δ53 Cr in bulk carbonate or other biogenic archives pending further work on vital effects and the geographic heterogeneity of the Cr isotope composition of seawater.

Towards a morphological metric of assemblage dynamics in the fossil record: a test case using planktonic foraminifera.

With a glance, even the novice naturalist can tell you something about the ecology of a given ecosystem. This is because the morphology of individuals reflects their evolutionary history and ecology, and imparts a distinct ‘look’ to communities—making it possible to immediately discern between deserts and forests, or coral reefs and abyssal plains. Once quantified, morphology can provide a common metric for characterizing communities across space and time and, if measured rapidly, serve as a powerful tool for quantifying biotic dynamics. Here, we present and test a new high-throughput approach for analysing community shape in the fossil record using semi-three-dimensional (3D) morphometrics from vertically stacked images (light microscopic or photogrammetric). We assess the potential informativeness of community morphology in a first analysis of the relationship between 3D morphology, ecology and phylogeny in 16 extant species of planktonic foraminifera—an abundant group in the marine fossil record—and in a preliminary comparison of four assemblages from the North Atlantic. In the species examined, phylogenetic relatedness was most closely correlated with ecology, with all three ecological traits examined (depth habitat, symbiont ecology and biogeography) showing significant phylogenetic signal. By contrast, morphological trees (based on 3D shape similarity) were relatively distantly related to both ecology and phylogeny. Although improvements are needed to realize the full utility of community morphometrics, our approach already provides robust volumetric measurements of assemblage size, a key ecological characteristic.

A probabilistic assessment of the rapidity of PETM onset

Knowledge of the onset duration of the Paleocene-Eocene Thermal Maximum—the largest known greenhouse-gas-driven global warming event of the Cenozoic—is central to drawing inferences for future climate change. Single-foraminifera measurements of the associated carbon isotope excursion from Maud Rise (South Atlantic Ocean) are controversial, as they seem to indicate geologically instantaneous carbon release and anomalously long ocean mixing. Here, we fundamentally reinterpret this record and extract the likely PETM onset duration. First, we employ an Earth system model to illustrate how the response of ocean circulation to warming does not support the interpretation of instantaneous carbon release. Instead, we use a novel sediment-mixing model to show how changes in the relative population sizes of calcareous plankton, combined with sediment mixing, can explain the observations. Furthermore, for any plausible PETM onset duration and sampling methodology, we place a probability on not sampling an intermediate, syn-excursion isotopic value. Assuming mixed-layer carbonate production continued at Maud Rise, we deduce the PETM onset was likely <5 kyr.Single-foraminifera measurements of the PETM carbon isotope excursion from Maud Rise have been interpreted as indicating geologically instantaneous carbon release. Here, the authors explain these records using an Earth system model and a sediment-mixing model and extract the likely PETM onset duration.