How predictable are mass extinction events?

Many modern extinction drivers are shared with past mass extinction events, such as rapid climate warming, habitat loss, pollution and invasive species. This commonality presents a key question: can the extinction risk of species during past mass extinction events inform our predictions for a modern biodiversity crisis? To investigate if it is possible to establish which species were more likely to go extinct during mass extinctions, we applied a functional trait-based model of extinction risk using a machine learning algorithm to datasets of marine fossils for the end-Permian, end-Triassic and end-Cretaceous mass extinctions. Extinction selectivity was inferred across each individual mass extinction event, before testing whether the selectivity patterns obtained could be used to 'predict' the extinction selectivity exhibited during the other mass extinctions. Our analyses show that, despite some similarities in extinction selectivity patterns between ancient crises, the selectivity of mass extinction events is inconsistent, which leads to a poor predictive performance. This lack of predictability is attributed to evolution in marine ecosystems, particularly during the Mesozoic Marine Revolution, associated with shifts in community structure alongside coincident Earth system changes. Our results suggest that past extinctions are unlikely to be informative for predicting extinction risk during a projected mass extinction.

Early evolution of beetles regulated by the end-Permian deforestation.

The end-Permian mass extinction (EPME) led to a severe terrestrial ecosystem collapse. However, the ecological response of insects-the most diverse group of organisms on Earth-to the EPME remains poorly understood. Here, we analyse beetle evolutionary history based on taxonomic diversity, morphological disparity, phylogeny, and ecological shifts from the Early Permian to Middle Triassic, using a comprehensive new dataset. Permian beetles were dominated by xylophagous stem groups with high diversity and disparity, which probably played an underappreciated role in the Permian carbon cycle. Our suite of analyses shows that Permian xylophagous beetles suffered a severe extinction during the EPME largely due to the collapse of forest ecosystems, resulting in an Early Triassic gap of xylophagous beetles. New xylophagous beetles appeared widely in the early Middle Triassic, which is consistent with the restoration of forest ecosystems. Our results highlight the ecological significance of insects in deep-time terrestrial ecosystems.

A Cretaceous peak in family-level insect diversity estimated with mark-recapture methodology.

The history of insects' taxonomic diversity is poorly understood. The two most common methods for estimating taxonomic diversity in deep time yield conflicting results: the 'range through' method suggests a steady, nearly monotonic increase in family-level diversity, whereas 'shareholder quorum subsampling' suggests a highly volatile taxonomic history with family-level mass extinctions occurring repeatedly, even at the midpoints of geological periods. The only feature shared by these two diversity curves is a steep increase in standing diversity during the Early Cretaceous. This apparent diversification event occurs primarily during the Aptian, the pre-Cenozoic interval with the most described insect occurrences, raising the possibility that this feature of the diversity curves reflects preservation and sampling biases rather than insect evolution and extinction. Here, the capture-mark-recapture (CMR) approach is used to estimate insects' family-level diversity. This method accounts for the incompleteness of the insect fossil record as well as uneven sampling among time intervals. The CMR diversity curve shows extinctions at the Permian/Triassic and Cretaceous/Palaeogene boundaries but does not contain any mass extinctions within geological periods. This curve also includes a steep increase in diversity during the Aptian, which appears not to be an artefact of sampling or preservation bias because this increase still appears when time bins are standardized by the number of occurrences they contain rather than by the amount of time that they span. The Early Cretaceous increase in family-level diversity predates the rise of angiosperms by many millions of years and can be better attributed to the diversification of parasitic and especially parasitoid insect lineages.

Conservation evidence from climate-related stressors in the deep-time marine fossil record.

Conservation of marine species requires the ability to predict the effects of climate-related stressors in an uncertain future. Experiments and observations in modern settings provide crucial information, but lack temporal scale and cannot anticipate emergent effects during ongoing global change. By contrast, the deep-time fossil record contains the long-term perspective at multiple global change events that can be used, at a broad scale, to test hypothesized effects of climate-related stressors. For example, geologically rapid carbon cycle disruption has often caused crises in reef ecosystems, and selective extinctions support the hypothesis that greater activity levels promote survival. Geographical patterns of extinction and extirpation were more variable than predicted from modern physiology, with tropical and temperate extinction peaks observed at different ancient events. Like any data source, the deep-time record has limitations but also provides opportunities that complement the limitations of modern and historical data. In particular, the deep-time record is the best source of information on actual outcomes of climate-related stressors in natural settings and over evolutionary timescales. Closer integration of modern and deep-time evidence can expand the types of hypotheses testable with the fossil record, yielding better predictions of extinction risk as climate-related stressors continue to intensify in future oceans. This article is part of a discussion meeting issue 'The past is a foreign country: how much can the fossil record actually inform conservation?'

Arthropods in modern resins reveal if amber accurately recorded forest arthropod communities.

Amber is an organic multicompound derivative from the polymerization of resin of diverse higher plants. Compared with other modes of fossil preservation, amber records the anatomy of and ecological interactions between ancient soft-bodied organisms with exceptional fidelity. However, it is currently suggested that ambers do not accurately record the composition of arthropod forest paleocommunities, due to crucial taphonomic biases. We evaluated the effects of taphonomic processes on arthropod entrapment by resin from the plant Hymenaea, one of the most important resin-producing trees and a producer of tropical Cenozoic ambers and Anthropocene (or subfossil) resins. We statistically compared natural entrapment by Hymenaea verrucosa tree resin with the ensemble of arthropods trapped by standardized entomological traps around the same tree species. Our results demonstrate that assemblages in resin are more similar to those from sticky traps than from malaise traps, providing an accurate representation of the arthropod fauna living in or near the resiniferous tree, but not of entire arthropod forest communities. Particularly, arthropod groups such as Lepidoptera, Collembola, and some Diptera are underrepresented in resins. However, resin assemblages differed slightly from sticky traps, perhaps because chemical compounds in the resins attract or repel specific insect groups. Ground-dwelling or flying arthropods that use the tree-trunk habitat for feeding or reproduction are also well represented in the resin assemblages, implying that fossil inclusions in amber can reveal fundamental information about biology of the past. These biases have implications for the paleoecological interpretation of the fossil record, principally of Cenozoic amber with angiosperm origin.

Multiple episodes of extensive marine anoxia linked to global warming and continental weathering following the latest Permian mass extinction.

Explaining the ~5-million-year delay in marine biotic recovery following the latest Permian mass extinction, the largest biotic crisis of the Phanerozoic, is a fundamental challenge for both geological and biological sciences. Ocean redox perturbations may have played a critical role in this delayed recovery. However, the lack of quantitative constraints on the details of Early Triassic oceanic anoxia (for example, time, duration, and extent) leaves the links between oceanic conditions and the delayed biotic recovery ambiguous. We report high-resolution U-isotope (δ238U) data from carbonates of the uppermost Permian to lowermost Middle Triassic Zal section (Iran) to characterize the timing and global extent of ocean redox variation during the Early Triassic. Our δ238U record reveals multiple negative shifts during the Early Triassic. Isotope mass-balance modeling suggests that the global area of anoxic seafloor expanded substantially in the Early Triassic, peaking during the latest Permian to mid-Griesbachian, the late Griesbachian to mid-Dienerian, the Smithian-Spathian transition, and the Early/Middle Triassic transition. Comparisons of the U-, C-, and Sr-isotope records with a modeled seawater PO43- concentration curve for the Early Triassic suggest that elevated marine productivity and enhanced oceanic stratification were likely the immediate causes of expanded oceanic anoxia. The patterns of redox variation documented by the U-isotope record show a good first-order correspondence to peaks in ammonoid extinctions during the Early Triassic. Our results indicate that multiple oscillations in oceanic anoxia modulated the recovery of marine ecosystems following the latest Permian mass extinction.

Organism activity levels predict marine invertebrate survival during ancient global change extinctions.

Multistressor global change, the combined influence of ocean warming, acidification, and deoxygenation, poses a serious threat to marine organisms. Experimental studies imply that organisms with higher levels of activity should be more resilient, but testing this prediction and understanding organism vulnerability at a global scale, over evolutionary timescales, and in natural ecosystems remain challenging. The fossil record, which contains multiple extinctions triggered by multistressor global change, is ideally suited for testing hypotheses at broad geographic, taxonomic, and temporal scales. Here, I assess the importance of activity level for survival of well-skeletonized benthic marine invertebrates over a 100-million-year-long interval (Permian to Jurassic periods) containing four global change extinctions, including the end-Permian and end-Triassic mass extinctions. More active organisms, based on a semiquantitative score incorporating feeding and motility, were significantly more likely to survive during three of the four extinction events (Guadalupian, end-Permian, and end-Triassic). In contrast, activity was not an important control on survival during nonextinction intervals. Both the end-Permian and end-Triassic mass extinctions also triggered abrupt shifts to increased dominance by more active organisms. Although mean activity gradually returned toward pre-extinction values, the net result was a permanent ratcheting of ecosystem-wide activity to higher levels. Selectivity patterns during ancient global change extinctions confirm the hypothesis that higher activity, a proxy for respiratory physiology, is a fundamental control on survival, although the roles of specific physiological traits (such as extracellular pCO2 or aerobic scope) cannot be distinguished. Modern marine ecosystems are dominated by more active organisms, in part because of selectivity ratcheting during these ancient extinctions, so on average may be less vulnerable to global change stressors than ancient counterparts. However, ancient extinctions demonstrate that even active organisms can suffer major extinction when the intensity of environmental disruption is intense.

Ancient origin of high taxonomic richness among insects.

Insects are a hyper-diverse group, comprising nearly three-quarters of all named animal species on the Earth, but the environmental drivers of their richness and the roles of ecological interactions and evolutionary innovations remain unclear. Previous studies have argued that family-level insect richness increased continuously over the evolutionary history of the group, but inclusion of extant family records artificially inflated the relative richness of younger time intervals. Here we apply sampling-standardization methods to a species-level database of fossil insect occurrences, removing biases present in previous richness curves. We show that insect family-richness peaked 125 Ma and that Recent values are only 1.5-3 times as high as the Late Palaeozoic. Rarefied species-richness data also tentatively suggest little or no net increase in richness over the past 125 Myr. The Cretaceous peak in family richness was coincident with major radiations within extant groups but occurred prior to extinctions within more basal groups. Those extinctions may in part be linked to mid-Cretaceous floral turnover following the evolution of flowering plants. Negligible net richness change over the past 125 Myr implies that major radiations within extant groups were offset by reduced richness within groups that are now relict or extinct.

Global patterns of insect diversification: towards a reconciliation of fossil and molecular evidence?

Macroevolutionary studies of insects at diverse taxonomic scales often reveal dynamic evolutionary patterns, with multiple inferred diversification rate shifts. Responses to major past environmental changes, such as the Cretaceous Terrestrial Revolution, or the development of major key innovations, such as wings or complete metamorphosis are usually invoked as potential evolutionary triggers. However this view is partially contradicted by studies on the family-level fossil record showing that insect diversification was relatively constant through time. In an attempt to reconcile both views, we investigate large-scale insect diversification dynamics at family level using two distinct types of diversification analyses on a molecular timetree representing ca. 82% of the extant families, and reassess the insect fossil diversity using up-to-date records. Analyses focusing on the fossil record recovered an early burst of diversification, declining to low and steady rates through time, interrupted by extinction events. Phylogenetic analyses showed that major shifts of diversification rates only occurred in the four richest holometabolous orders. Both suggest that neither the development of flight or complete metamorphosis nor the Cretaceous Terrestrial Revolution environmental changes induced immediate changes in diversification regimes; instead clade-specific innovations likely promoted the diversification of major insect orders.

Canopy flow analysis reveals the advantage of size in the oldest communities of multicellular eukaryotes.

VIDEO ABSTRACT: At Mistaken Point, Newfoundland, Canada, rangeomorph "fronds" dominate the earliest (579-565 million years ago) fossil communities of large (0.1 to 2 m height) multicellular benthic eukaryotes. They lived in low-flow environments, fueled by uptake [1-3] of dissolved reactants (osmotrophy). However, prokaryotes are effective osmotrophs, and the advantage of taller eukaryotic osmotrophs in this deep-water community context has not been addressed. We reconstructed flow-velocity profiles and vertical mixing using canopy flow models appropriate to the densities of the observed communities. Further modeling of processes at organismal surfaces documents increasing uptake with height in the community as a function of thinning of the diffusive boundary layer with increased velocity. The velocity profile, produced by canopy flow in the community, generates this advantage of upward growth. Alternative models of upward growth advantage based on redox/resource gradients fail, given the efficiency of vertical mixing. In benthic communities of osmotrophs of sufficient density, access to flow in low-flow settings provides an advantage to taller architecture, providing a selectional driver for communities of tall eukaryotes in contexts where phototropism cannot contribute to upward growth. These Ediacaran deep-sea fossils were preserved during the increasing oxygenation prior to the Cambrian radiation of animals and likely represent an important phase in the ecological and evolutionary transition to more complex eukaryotic forms.

Environmental and biotic controls on the evolutionary history of insect body size.

Giant insects, with wingspans as large as 70 cm, ruled the Carboniferous and Permian skies. Gigantism has been linked to hyperoxic conditions because oxygen concentration is a key physiological control on body size, particularly in groups like flying insects that have high metabolic oxygen demands. Here we show, using a dataset of more than 10,500 fossil insect wing lengths, that size tracked atmospheric oxygen concentrations only for the first 150 Myr of insect evolution. The data are best explained by a model relating maximum size to atmospheric environmental oxygen concentration (pO(2)) until the end of the Jurassic, and then at constant sizes, independent of oxygen fluctuations, during the Cretaceous and, at a smaller size, the Cenozoic. Maximum insect size decreased even as atmospheric pO(2) rose in the Early Cretaceous following the evolution and radiation of early birds, particularly as birds acquired adaptations that allowed more agile flight. A further decrease in maximum size during the Cenozoic may relate to the evolution of bats, the Cretaceous mass extinction, or further specialization of flying birds. The decoupling of insect size and atmospheric pO(2) coincident with the radiation of birds suggests that biotic interactions, such as predation and competition, superseded oxygen as the most important constraint on maximum body size of the largest insects.

Phanerozoic trends in the global diversity of marine invertebrates.

It has previously been thought that there was a steep Cretaceous and Cenozoic radiation of marine invertebrates. This pattern can be replicated with a new data set of fossil occurrences representing 3.5 million specimens, but only when older analytical protocols are used. Moreover, analyses that employ sampling standardization and more robust counting methods show a modest rise in diversity with no clear trend after the mid-Cretaceous. Globally, locally, and at both high and low latitudes, diversity was less than twice as high in the Neogene as in the mid-Paleozoic. The ratio of global to local richness has changed little, and a latitudinal diversity gradient was present in the early Paleozoic.

Prolonged Permian Triassic ecological crisis recorded by molluscan dominance in Late Permian offshore assemblages.

The end-Permian mass extinction was the largest biotic crisis in the history of animal life, eliminating as many as 95% of all species and dramatically altering the ecological structure of marine communities. Although the causes of this pronounced ecosystem shift have been widely debated, the broad consensus based on inferences from global taxonomic diversity patterns suggests that the shift from abundant brachiopods to dominant molluscs was abrupt and largely driven by the catastrophic effects of the end-Permian mass extinction. Here we analyze relative abundance counts of >33,000 fossil individuals from 24 silicified Middle and Late Permian paleocommunities, documenting a substantial ecological shift to numerical dominance by molluscs in the Late Permian, before the major taxonomic shift at the end-Permian mass extinction. This ecological change was coincident with the development of fluctuating anoxic conditions in deep marine basins, suggesting that numerical dominance by more tolerant molluscs may have been driven by variably stressful environmental conditions. Recognition of substantial ecological deterioration in the Late Permian also implies that the end-Permian extinction was the climax of a protracted environmental crisis. Although the Late Permian shift to molluscan dominance was a pronounced ecological change, quantitative counts of 847 Carboniferous-Cretaceous collections from the Paleobiology Database indicate that it was only the first stage in a stepwise transition that culminated with the final shift to molluscan dominance in the Late Jurassic. Therefore, the ecological transition from brachiopods to bivalves was more protracted and complex than their simple Permian-Triassic switch in diversity.