Palaeoecology of the Hiraiso Formation (Miyagi Prefecture, Japan) and implications for the recovery following the end-Permian mass extinction.

The Hiraiso Formation of northeast Japan represents an important and under-explored archive of Early Triassic marine ecosystems. Here, we present a palaeoecological analysis of its benthic faunas in order to explore the temporal and spatial variations of diversity, ecological structure and taxonomic composition. In addition, we utilise redox proxies to make inferences about the redox state of the depositional environments. We then use this data to explore the pace of recovery in the Early Triassic, and the habitable zone hypothesis, where wave aerated marine environments are thought to represent an oxygenated refuge. The age of the Hiraiso Formation is equivocal due to the lack of key biostratigraphical index fossils, but new ammonoid finds in this study support an early Spathian age. The ichnofossils from the Hiraiso Formation show an onshore-offshore trend with high diversity and relatively large faunas in offshore transition settings and a low diversity of small ichnofossils in basinal settings. The body fossils do not, however, record either spatial or temporal changes, because the shell beds represent allochthonous assemblages due to wave reworking. The dominance of small burrow sizes, presence of key taxa including Thalassinoides, Rhizocorallium and Holocrinus, presence of complex trace fossils, and both erect and deep infaunal tiering organisms suggests that the benthic fauna represents an advanced stage of ecological recovery for the Early Triassic, but not full recovery. The ecological state suggests a similar level of ecological complexity to late Griesbachian and Spathian communities elsewhere, with the Spathian marking a globally important stage of recovery following the mass extinction. The onshore-offshore distribution of the benthic faunas supports the habitable zone hypothesis. This gradient is, however, also consistent with onshore-offshore ecological gradients known to be controlled by oxygen gradients in modern tropical and subtropical settings. This suggests that the habitable zone is not an oxygenated refuge that is only restricted to anoxic events. The lack of observed full recovery is likely a consequence of a persistent oxygen-limitation (dysoxic conditions), hot Early Triassic temperatures and the lack of a steep temperature/water-depth gradient within the habitable zone.

Global record of "ghost" nannofossils reveals plankton resilience to high CO2 and warming.

Predictions of how marine calcifying organisms will respond to climate change rely heavily on the fossil record of nannoplankton. Declines in calcium carbonate (CaCO3) and nannofossil abundance through several past global warming events have been interpreted as biocalcification crises caused by ocean acidification and related factors. We present a global record of imprint-or "ghost"-nannofossils that contradicts this view, revealing exquisitely preserved nannoplankton throughout an inferred Jurassic biocalcification crisis. Imprints from two further Cretaceous warming events confirm that the fossil records of these intervals have been strongly distorted by CaCO3 dissolution. Although the rapidity of present-day climate change exceeds the temporal resolution of most fossil records, complicating direct comparison with past warming events, our findings demonstrate that nannoplankton were more resilient to past events than traditional fossil evidence suggests.

Marine Metazoan Modern Mass Extinction: Improving Predictions by Integrating Fossil, Modern, and Physiological Data.

Evolution, extinction, and dispersion are fundamental processes affecting marine biodiversity. Until recently, studies of extant marine systems focused mainly on evolution and dispersion, with extinction receiving less attention. Past extinction events have, however, helped shape the evolutionary history of marine ecosystems, with ecological and evolutionary legacies still evident in modern seas. Current anthropogenic global changes increase extinction risk and pose a significant threat to marine ecosystems, which are critical for human use and sustenance. The evaluation of these threats and the likely responses of marine ecosystems requires a better understanding of evolutionary processes that affect marine ecosystems under global change. Here, we discuss how knowledge of ( a) changes in biodiversity of ancient marine ecosystems to past extinctions events, ( b) the patterns of sensitivity and biodiversity loss in modern marine taxa, and ( c) the physiological mechanisms underpinning species' sensitivity to global change can be exploited and integrated to advance our critical thinking in this area.

Modelling determinants of extinction across two Mesozoic hyperthermal events.

The Late Triassic and Early Toarcian extinction events are both associated with greenhouse warming events triggered by massive volcanism. These Mesozoic hyperthermals were responsible for the mass extinction of marine organisms and resulted in significant ecological upheaval. It has, however, been suggested that these events merely involved intensification of background extinction rates rather than significant shifts in the macroevolutionary regime and extinction selectivity. Here, we apply a multivariate modelling approach to a vast global database of marine organisms to test whether extinction selectivity varied through the Late Triassic and Early Jurassic. We show that these hyperthermals do represent shifts in the macroevolutionary regime and record different extinction selectivity compared to background intervals of the Late Triassic and Early Jurassic. The Late Triassic mass extinction represents a more profound change in selectivity than the Early Toarcian extinction but both events show a common pattern of selecting against pelagic predators and benthic photosymbiotic and suspension-feeding organisms, suggesting that these groups of organisms may be particularly vulnerable during episodes of global warming. In particular, the Late Triassic extinction represents a macroevolutionary regime change that is characterized by (i) the change in extinction selectivity between Triassic background intervals and the extinction event itself; and (ii) the differences in extinction selectivity between the Late Triassic and Early Jurassic as a whole.

Ecological impact of the end-Cretaceous extinction on lamniform sharks.

Lamniform sharks are apex marine predators undergoing dramatic local and regional decline worldwide, with consequences for marine ecosystems that are difficult to predict. Through their long history, lamniform sharks have faced widespread extinction, and understanding those 'natural experiments' may help constrain predictions, placing the current crisis in evolutionary context. Here we show, using novel morphometric analyses of fossil shark teeth, that the end-Cretaceous extinction of many sharks had major ecological consequences. Post-extinction ecosystems supported lower diversity and disparity of lamniforms, and were dominated by significantly smaller sharks with slimmer, smoother and less robust teeth. Tooth shape is intimately associated with ecology, feeding and prey type, and by integrating data from extant sharks we show that latest Cretaceous sharks occupied similar niches to modern lamniforms, implying similar ecosystem structure and function. By comparison, species in the depauperate post-extinction community occupied niches most similar to those of juvenile sand tigers (Carcharias taurus). Our data show that quantitative tooth morphometrics can distinguish lamniform sharks due to dietary differences, providing critical insights into ecological consequences of past extinction episodes.

Subsequent biotic crises delayed marine recovery following the late Permian mass extinction event in northern Italy.

The late Permian mass extinction event was the largest biotic crisis of the Phanerozoic and has the longest recovery interval of any extinction event. It has been hypothesised that subsequent carbon isotope perturbations during the Early Triassic are associated with biotic crises that impeded benthic recovery. We test this hypothesis by undertaking the highest-resolution study yet made of the rock and fossil records of the entire Werfen Formation, Italy. Here, we show that elevated extinction rates were recorded not only in the Dienerian, as previously recognised, but also around the Smithian/Spathian boundary. Functional richness increases across the Smithian/Spathian boundary associated with elevated origination rates in the lower Spathian. The taxonomic and functional composition of benthic faunas only recorded two significant changes: (1) reduced heterogeneity in the Dienerian, and (2) and a faunal turnover across the Smithian/Spathian boundary. The elevated extinctions and compositional shifts in the Dienerian and across the Smithian/Spathian boundary are associated with a negative and positive isotope excursion, respectively, which supports the hypothesis that subsequent biotic crises are associated with carbon isotope shifts. The Spathian fauna represents a more advanced ecological state, not recognised in the previous members of the Werfen Formation, with increased habitat differentiation, a shift in the dominant modes of life, appearance of stenohaline taxa and the occupation of the erect and infaunal tiers. In addition to subsequent biotic crises delaying the recovery, therefore, persistent environmental stress limited the ecological complexity of benthic recovery prior to the Spathian.

The oldest post-Palaeozoic Crinoid and Permian-Triassic origins of the Articulata (Echinodermata).

The Crinoidea are the most primitive class of living echinoderms, and suffered a severe crisis during the Late Permian mass extinction event. All post-Palaeozoic crinoids, including living species, belong to the Articulata, and morphological and recent molecular studies demonstrate that they form a monophyletic clade. The Articulata originated from Palaeozoic cladid crinoids, but the nature and timing of their origination remains obscure. Problems with understanding the origin and early evolution of the Articulata have arisen because the Permian-Triassic crinoid fossil record is particularly poor. We report on a new genus and species from the earliest Triassic, which is the oldest known post-Palaeozoic articulate crinoid and fundamentally alters our understanding of the early evolution of the Articulata. Prior to this study, the most primitive post-Palaeozoic articulate was thought to be Holocrinus of the order Isocrinida. Unexpectedly, the new taxon belongs to the order Encrinida, which reveals a previously hidden diversity of crinoids in the earliest Triassic. Its discovery implies either a dramatic radiation of crinoids in the immediate post-extinction aftermath, when environmental conditions were at their most severe, or a pre-extinction origin of the crown group articulates and survival of multiple lineages.

Ecological succession of a Jurassic shallow-water ichthyosaur fall.

After the discovery of whale fall communities in modern oceans, it has been hypothesized that during the Mesozoic the carcasses of marine reptiles created similar habitats supporting long-lived and specialized animal communities. Here, we report a fully documented ichthyosaur fall community, from a Late Jurassic shelf setting, and reconstruct the ecological succession of its micro- and macrofauna. The early 'mobile-scavenger' and 'enrichment-opportunist' stages were not succeeded by a 'sulphophilic stage' characterized by chemosynthetic molluscs, but instead the bones were colonized by microbial mats that attracted echinoids and other mat-grazing invertebrates. Abundant cemented suspension feeders indicate a well-developed 'reef stage' with prolonged exposure and colonization of the bones prior to final burial, unlike in modern whale falls where organisms such as the ubiquitous bone-eating worm Osedax rapidly destroy the skeleton. Shallow-water ichthyosaur falls thus fulfilled similar ecological roles to shallow whale falls, and did not support specialized chemosynthetic communities.

Hierarchical random walks in trace fossils and the origin of optimal search behavior.

Efficient searching is crucial for timely location of food and other resources. Recent studies show that diverse living animals use a theoretically optimal scale-free random search for sparse resources known as a Lévy walk, but little is known of the origins and evolution of foraging behavior and the search strategies of extinct organisms. Here, using simulations of self-avoiding trace fossil trails, we show that randomly introduced strophotaxis (U-turns)--initiated by obstructions such as self-trail avoidance or innate cueing--leads to random looping patterns with clustering across increasing scales that is consistent with the presence of Lévy walks. This predicts that optimal Lévy searches may emerge from simple behaviors observed in fossil trails. We then analyzed fossilized trails of benthic marine organisms by using a novel path analysis technique and find the first evidence, to our knowledge, of Lévy-like search strategies in extinct animals. Our results show that simple search behaviors of extinct animals in heterogeneous environments give rise to hierarchically nested Brownian walk clusters that converge to optimal Lévy patterns. Primary productivity collapse and large-scale food scarcity characterizing mass extinctions evident in the fossil record may have triggered adaptation of optimal Lévy-like searches. The findings suggest that Lévy-like behavior has been used by foragers since at least the Eocene but may have a more ancient origin, which might explain recent widespread observations of such patterns among modern taxa.

Isotopic evidence for long term warmth in the Mesozoic.

Atmospheric CO2 concentrations appear to have been considerably higher than modern levels during much of the Phanerozoic and it has hence been proposed that surface temperatures were also higher. Some studies have, however, suggested that Earth's temperature (estimated from the isotopic composition of fossil shells) may have been independent of variations in atmospheric CO2 (e.g. in the Jurassic and Cretaceous). If large changes in atmospheric CO2 did not produce the expected climate responses in the past, predictions of future climate and the case for reducing current fossil-fuel emissions are potentially undermined. Here we evaluate the dataset upon which the Jurassic and Cretaceous assertions are based and present new temperature data, derived from the isotopic composition of fossil brachiopods. Our results are consistent with a warm climate mode for the Jurassic and Cretaceous and hence support the view that changes in atmospheric CO2 concentrations are linked with changes in global temperatures.

The impact of global warming and anoxia on marine benthic community dynamics: an example from the Toarcian (Early Jurassic).

The Pliensbachian-Toarcian (Early Jurassic) fossil record is an archive of natural data of benthic community response to global warming and marine long-term hypoxia and anoxia. In the early Toarcian mean temperatures increased by the same order of magnitude as that predicted for the near future; laminated, organic-rich, black shales were deposited in many shallow water epicontinental basins; and a biotic crisis occurred in the marine realm, with the extinction of approximately 5% of families and 26% of genera. High-resolution quantitative abundance data of benthic invertebrates were collected from the Cleveland Basin (North Yorkshire, UK), and analysed with multivariate statistical methods to detect how the fauna responded to environmental changes during the early Toarcian. Twelve biofacies were identified. Their changes through time closely resemble the pattern of faunal degradation and recovery observed in modern habitats affected by anoxia. All four successional stages of community structure recorded in modern studies are recognised in the fossil data (i.e. Stage III: climax; II: transitional; I: pioneer; 0: highly disturbed). Two main faunal turnover events occurred: (i) at the onset of anoxia, with the extinction of most benthic species and the survival of a few adapted to thrive in low-oxygen conditions (Stages I to 0) and (ii) in the recovery, when newly evolved species colonized the re-oxygenated soft sediments and the path of recovery did not retrace of pattern of ecological degradation (Stages I to II). The ordination of samples coupled with sedimentological and palaeotemperature proxy data indicate that the onset of anoxia and the extinction horizon coincide with both a rise in temperature and sea level. Our study of how faunal associations co-vary with long and short term sea level and temperature changes has implications for predicting the long-term effects of "dead zones" in modern oceans.

Photic zone euxinia during the Permian-triassic superanoxic event.

Carbon and sulfur isotopic data, together with biomarker and iron speciation analyses of the Hovea-3 core that was drilled in the Perth Basin, Western Australia, indicate that euxinic conditions prevailed in the paleowater column during the Permian-Triassic superanoxic event. Biomarkers diagnostic for anoxygenic photosynthesis by Chlorobiaceae are particularly abundant at the boundary and into the Early Triassic. Similar conditions prevailed in the contemporaneous seas off South China. Our evidence for widespread photiczone euxinic conditions suggests that sulfide toxicity was a driver of the extinction and a factor in the protracted recovery.