Early onset of secondary extinctions in ecological communities following the loss of top predators

The large vulnerability of top predators to human-induced disturbances on ecosystems is a matter of growing concern. Because top predators often exert strong influence on their prey populations their extinction can have far-reaching consequences for the structure and functioning of ecosystems. It has, for example, been observed that the local loss of a predator can trigger a cascade of secondary extinctions. However, the time lags involved in such secondary extinctions remain unexplored. Here we show that the loss of a top predator leads to a significantly earlier onset of secondary extinctions in model communities than does the loss of a species from other trophic levels. Moreover, in most cases time to secondary extinction increases with increasing species richness. If local secondary extinctions occur early they are less likely to be balanced by immigration of species from local communities nearby. The implications of these results for community persistence and conservation priorities are discussed.     

Species loss leads to community closure

Global extinction of a species is sadly irreversible. At a local scale, however, extinctions may be followed by re-invasion. We here show that this is not necessarily the case and that an ecological community may close its doors for re-invasion of species lost from it. Previous studies of how communities are assembled have shown that there may be rules for that process and that limitations are set to the order by which species are introduced and put together. Instead of focusing on the assembly process we randomly generated simple competitive model communities that were stable and allowed for two to 10 coexisting species. When a randomly selected single species was removed from the community, the cascading species loss was recorded and frequently the resulting community was more than halved. Cascading extinctions have previously been recorded, but we here show that the relative magnitude of the cascade is dependent on community size (and not only trophic structure) and that the reintroduction of the original species lost often is impossible. Hence, species loss does not simply leave a void potentially refilled, but permanently alters the entire community structure and consequently the adaptive landscape for potential re-invaders.     

Decoupling of morphological disparity and taxic diversity during the adaptive radiation of anomodont therapsids

Adaptive radiations are central to macroevolutionary theory. Whether triggered by acquisition of new traits or ecological opportunities arising from mass extinctions, it is debated whether adaptive radiations are marked by initial expansion of taxic diversity or of morphological disparity (the range of anatomical form). If a group rediversifies following a mass extinction, it is said to have passed through a macroevolutionary bottleneck, and the loss of taxic or phylogenetic diversity may limit the amount of morphological novelty that it can subsequently generate. Anomodont therapsids, a diverse clade of Permian and Triassic herbivorous tetrapods, passed through a bottleneck during the end-Permian mass extinction. Their taxic diversity increased during the Permian, declined significantly at the Permo–Triassic boundary and rebounded during the Middle Triassic before the clade''s final extinction at the end of the Triassic. By sharp contrast, disparity declined steadily during most of anomodont history. Our results highlight three main aspects of adaptive radiations: (i) diversity and disparity are generally decoupled; (ii) models of radiations following mass extinctions may differ from those triggered by other causes (e.g. trait acquisition); and (iii) the bottleneck caused by a mass extinction means that a clade can emerge lacking its original potential for generating morphological variety.     

Body length of bony fishes was not a selective factor during the biggest mass extinction of all time

The Permo‐Triassic mass extinction devastated life on land and in the sea, but it is not clear why some species survived and others went extinct. One explanation is that lineage loss during mass extinctions is a random process in which luck determines which species survive. Alternatively, a phylogenetic signal in extinction may indicate a selection process operating on phenotypic traits. Large body size has often emerged as an extinction risk factor in studies of modern extinction risk, but this is not so commonly the case for mass extinctions in deep time. Here, we explore the evolution of non‐teleostean Actinopterygii (bony fishes) from the Devonian to the present day, and we concentrate on the Permo‐Triassic mass extinction. We apply a variety of time‐scaling metrics to date the phylogeny, and show that diversity peaked in the latest Permian and declined severely during the Early Triassic. In line with previous evidence, we find the phylogenetic signal of extinction increases across the mass extinction boundary: extinction of species in the earliest Triassic is more clustered across phylogeny compared to the more randomly distributed extinction signal in the late Permian. However, body length plays no role in differential survival or extinction of taxa across the boundary. In the case of fishes, size did not determine which species survived and which went extinct, but phylogenetic signal indicates that the mass extinction was not a random field of bullets.     

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.     

Permian–Triassic Osteichthyes (bony fishes): diversity dynamics and body size evolution

The Permian and Triassic were key time intervals in the history of life on Earth. Both periods are marked by a series of biotic crises including the most catastrophic of such events, the end‐Permian mass extinction, which eventually led to a major turnover from typical Palaeozoic faunas and floras to those that are emblematic for the Mesozoic and Cenozoic. Here we review patterns in Permian–Triassic bony fishes, a group whose evolutionary dynamics are understudied. Based on data from primary literature, we analyse changes in their taxonomic diversity and body size (as a proxy for trophic position) and explore their response to Permian–Triassic events. Diversity and body size are investigated separately for different groups of Osteichthyes (Dipnoi, Actinistia, ‘Palaeopterygii’, ‘Subholostei’, Holostei, Teleosteomorpha), within the marine and freshwater realms and on a global scale (total diversity) as well as across palaeolatitudinal belts. Diversity is also measured for different palaeogeographical provinces. Our results suggest a general trend from low osteichthyan diversity in the Permian to higher levels in the Triassic. Diversity dynamics in the Permian are marked by a decline in freshwater taxa during the Cisuralian. An extinction event during the end‐Guadalupian crisis is not evident from our data, but ‘palaeopterygians’ experienced a significant body size increase across the Guadalupian–Lopingian boundary and these fishes upheld their position as large, top predators from the Late Permian to the Late Triassic. Elevated turnover rates are documented at the Permian–Triassic boundary, and two distinct diversification events are noted in the wake of this biotic crisis, a first one during the Early Triassic (dipnoans, actinistians, ‘palaeopterygians’, ‘subholosteans’) and a second one during the Middle Triassic (‘subholosteans’, neopterygians). The origination of new, small taxa predominantly among these groups during the Middle Triassic event caused a significant reduction in osteichthyan body size. Neopterygii, the clade that encompasses the vast majority of extant fishes, underwent another diversification phase in the Late Triassic. The Triassic radiation of Osteichthyes, predominantly of Actinopterygii, which only occurred after severe extinctions among Chondrichthyes during the Middle–Late Permian, resulted in a profound change within global fish communities, from chondrichthyan‐rich faunas of the Permo‐Carboniferous to typical Mesozoic and Cenozoic associations dominated by actinopterygians. This turnover was not sudden but followed a stepwise pattern, with leaps during extinction events.     

Impact of the Late Triassic mass extinction on functional diversity and composition of marine ecosystems

Mass extinctions have profoundly influenced the history of life, not only through the death of species but also through changes in ecosystem function and structure. Importantly, these events allow us the opportunity to study ecological dynamics under levels of environmental stress for which there are no recent analogues. Here, we examine the impact and selectivity of the Late Triassic mass extinction event on the functional diversity and functional composition of the global marine ecosystem, and test whether post‐extinction communities in the Early Jurassic represent a regime shift away from pre‐extinction communities in the Late Triassic. Our analyses show that, despite severe taxonomic losses, there is no unequivocal loss of global functional diversity associated with the extinction. Even though no functional groups were lost, the extinction event was, however, highly selective against some modes of life, in particular sessile suspension feeders. Although taxa with heavily calcified skeletons suffered higher extinction than other taxa, lightly calcified taxa also appear to have been selected against. The extinction appears to have invigorated the already ongoing faunal turnover associated with the Mesozoic Marine Revolution. The ecological effects of the Late Triassic mass extinction were preferentially felt in the tropical latitudes, especially amongst reefs, and it took until the Middle Jurassic for reef ecosystems to fully recover to pre‐extinction levels.     

Changhsingian brachiopod communities along a marine depth gradient in South China and their ecological significance in the end-Permian mass extinction

Diversity indices (dominance and evenness) and ecological spatial structure (lifestyles and relative abundances) are important features of Changhsingian brachiopod communities prior to the end-Permian mass extinction (EPME) and could predict temporal and spatial extinction patterns during the EPME. In South China, Changhsingian brachiopod communities show higher diversity than other contemporaneous brachiopod communities in the world and have been reported from a variety of sedimentary environments. In this paper, brachiopods from 18 sections in South China were selected to divide communities and compare their ecological structure. Based on the results of network analysis, cluster analysis and quantitative data from the selected sections, we show that Changhsingian brachiopod communities in South China can be categorized into three assemblages along a marine depth gradient: the Neochonetes–Fusichonetes–Paryphella Assemblage from the shallow-water clastic-rock facies, Spinomarginifera–Peltichia–Oldhamina Assemblage from the shallow-water carbonate platform facies and Fusichonetes–Crurithyris Assemblage from the deep-water siliciclastic intracontinental basin facies. Compared with communities from carbonate platform facies, the communities from siliciclastic facies were characterized by high dominance, low evenness and low lifestyle diversity, which might be important biotic factors leading to earlier extinctions. After the extinction began in all environments, the whole earliest Triassic brachiopod community was first dominated by Fusichonetes and then by Crurithyris. These patterns of domination and replacement could be explained by morphological and ecological advantages. The domination of these two genera, which were already adapted to the oxygen and food-limited deep-water habitat, indicates that the cooler deep-water environment might have been a relatively less stressed habitat after the beginning of the EPME. This suggests that global warming might be the main trigger among the previously proposed synergistic environmental stresses, while anoxia might not, at least for the beginning of EPME.     

Keystone species and vulnerable species in ecological communities: strong or weak interactors?

The loss of a species from an ecological community can trigger a cascade of secondary extinctions. The probability of secondary extinction to take place and the number of secondary extinctions are likely to depend on the characteristics of the species that is lost--the strength of its interactions with other species--as well as on the distribution of interaction strengths in the whole community. Analysing the effects of species loss in model communities we found that removal of the following species categories triggered, on average, the largest number of secondary extinctions: (a) rare species interacting strongly with many consumers, (b) abundant basal species interacting weakly with their consumers and (c) abundant intermediate species interacting strongly with many resources. We also found that the keystone status of a species with given characteristics was context dependent, that is, dependent on the structure of the community where it was embedded. Species vulnerable to secondary extinctions were mainly species interacting weakly with their resources and species interacting strongly with their consumers.     

Evolution of the Permian and Triassic tetrapod communities of Eastern Europe

The Permo-Triassic terrestrial and freshwater tetrapod communities of Eastern Europe are reconstructed as food-webs. The Late Permian theriodont-dinocephalian community (Ocher, Mezen, Isheyevo) changes to a latest Permian theriodont-pareiasaur community (North Dvina, Vyazniki). After a major extinction, the Triassic thecodontian-dicynodont communities appear, a lystrosaurid one in the Early Triassic (Lower and ?Upper Vetluga), and a kannemeyerid one in the later Early Triassic (?Yarenga) and the Mid Triassic (Donguz, Bukobay). Similar stages are represented in the evolution of aquatic communities: the Late Permian temnospondyl community (Ocher, Isheyevo), the latest Permian chroniosuchian one (North Dvina, Vyazniki), the Lower and Middle Triassic new temnospondyl one (from Vetluga to Bukobay). The faunal changes in Eastern Europe are mirrored in other parts of the world, although there are some endemic Russian forms.     

Species loss and secondary extinctions in simple and complex model communities

1. The loss of a species from an ecological community can trigger a cascade of secondary extinctions. Here we investigate how the complexity (connectance) of model communities affects their response to species loss. Using dynamic analysis based on a global criterion of persistence (permanence) and topological analysis we investigate the extent of secondary extinctions following the loss of different kinds of species. 2. We show that complex communities are, on average, more resistant to species loss than simple communities: the number of secondary extinctions decreases with increasing connectance. However, complex communities are more vulnerable to loss of top predators than simple communities. 3. The loss of highly connected species (species with many links to other species) and species at low trophic levels triggers, on average, the largest number of secondary extinctions. The effect of the connectivity of a species is strongest in webs with low connectance. 4. Most secondary extinctions are due to direct bottom-up effects: consumers go extinct when their resources are lost. Secondary extinctions due to trophic cascades and disruption of predator-mediated coexistence also occur. Secondary extinctions due to disruption of predator-mediated coexistence are more common in complex communities than in simple communities, while bottom-up and top-down extinction cascades are more common in simple communities. 5. Topological analysis of the response of communities to species loss always predicts a lower number of secondary extinctions than dynamic analysis, especially in food webs with high connectance.     

Why was there a delayed radiation after the end‐Palaeozoic extinctions?

Data from widespread dysaerobic facies, carbon/sulphur ratios and cerium anomalies suggest that the early Triassic was a time when anoxic conditions spread widely over epicontinental seas. These conditions, associated with marine transgression following the latest Permian regression, are likely to be a prime cause of the mass extinction of Palaeozoic marine faunas. The occurrence of many Lazarus taxa in the Middle and Upper Triassic indicates, however, that the extinctions at the end of the Permian were less severe than has been widely assumed, and that the turnover from Palaeozoic to Mesozoic faunas was considerably extended in time, being finally accomplished only after the end‐Triassic mass extinction event.     

EXTINCTION SPACE—A METHOD FOR THE QUANTIFICATION AND CLASSIFICATION OF CHANGES IN MORPHOSPACE ACROSS EXTINCTION BOUNDARIES

Three main modes of extinction are responsible for reductions in morphological disparity: (1) random (caused by a nonselective extinction event); (2) marginal (a symmetric, selective extinction event trimming the margin of morphospace); and (3) lateral (an asymmetric, selective extinction event eliminating one side of the morphospace). These three types of extinction event can be distinguished from one another by comparing changes in three measures of morphospace occupation: (1) the sum of range along the main axes; (2) the sum of variance; and (3) the position of the centroid. Computer simulations of various extinction events demonstrate that the pre‐extinction distribution of taxa (random or normal) in the morphospace has little influence on the quantification of disparity changes, whereas the modes of the extinction events play the major role. Together, the three disparity metrics define an “extinction‐space” in which different extinction events can be directly compared with one another. Application of this method to selected extinction events (Frasnian‐Famennian, Devonian‐Carboniferous, and Permian‐Triassic) of the Ammonoidea demonstrate the similarity of the Devonian events (selective extinctions) but the striking difference from the end‐Permian event (nonselective extinction). These events differ in their mode of extinction despite decreases in taxonomic diversity of similar magnitude.     

Amniotes through major biological crises: faunal turnover among Parareptiles and the end‐Permian mass extinction

Abstract: The Parareptilia are a small but ecologically and morphologically diverse clade of Permian and Triassic crown amniotes generally considered to be phylogenetically more proximal to eureptiles (diapsids and their kin) than to synapsids (mammals and their kin). A recent supertree provides impetus for an analysis of parareptile diversity through time and for examining the influence of the end‐Permian mass extinction on the clade’s origination and extinction rates. Phylogeny‐corrected measures of diversity have a significant impact on both rates and the distribution of origination and extinction intensities. Time calibration generally results in a closer correspondence between origination and extinction rate values than in the case of no time correction. Near the end‐Permian event, extinction levels are not significantly higher than origination levels, particularly when time calibration is introduced. Finally, regardless of time calibration and/or phylogenetic correction, the distribution of rates does not differ significantly from unimodal. The curves of rate values are discussed in the light of the numbers and distributions of both range extensions and ghost lineages. The disjoint time distributions of major parareptile clades (e.g. procolophonoids and nycteroleterids‐pareiasaurs) are mostly responsible for the occurrence of long‐range extensions throughout the Permian. Available data are not consistent with a model of sudden decline at the end‐Permian but rather suggest a rapid alternation of originations and extinctions in a number of parareptile groups, both before and after the Permian/Triassic boundary.     

Vyazniki biotic assemblage of the terminal Permian

A new unique and diverse biotic assemblage of the terminal Permian has recently been discovered in the town of Vyazniki (Central Russia). The Vyazniki terrestrial community is transitional between Permian and Triassic ones and represents the last, so far unknown stage of the global ecological crisis of the continental biota at the Permian-Triassic boundary. The successive development of land biotic crisis in the Late Permian, which was followed by mass extinction at the Permian-Triassic boundary, and long, successive postcrisis development and specialization of new Triassic groups as well as rearrangement and diversification of the biotic assemblage composition and community structure suggest predominance of intrinsic, biotic causes of this crisis, realized in destabilization, alteration, and new stabilization of continental communities and ecosystems.     

Archosauromorph extinction selectivity during the Triassic–Jurassic mass extinction

Many traits have been linked to extinction risk among modern vertebrates, including mode of life and body size. However, previous work has indicated there is little evidence that body size, or any other trait, was selective during past mass extinctions. Here, we investigate the impact of the Triassic–Jurassic mass extinction on early Archosauromorpha (basal dinosaurs, crocodylomorphs and their relatives) by focusing on body size and other life history traits. We built several new archosauromorph maximum‐likelihood supertrees, incorporating uncertainty in phylogenetic relationships. These supertrees were then employed as a framework to test whether extinction had a phylogenetic signal during the Triassic–Jurassic mass extinction, and whether species with certain traits were more or less likely to go extinct. We find evidence for phylogenetic signal in extinction, in that taxa were more likely to become extinct if a close relative also did. However, there is no correlation between extinction and body size, or any other tested trait. These conclusions add to previous findings that body size, and other traits, were not subject to selection during mass extinctions in closely‐related clades, although the phylogenetic signal in extinction indicates that selection may have acted on traits not investigated here.     

Predator–prey interactions amongst Permo‐Triassic terrestrial vertebrates as a deterministic factor influencing faunal collapse and turnover

Unlike modern mammalian communities, terrestrial Paleozoic and Mesozoic vertebrate systems were characterized by carnivore faunas that were as diverse as their herbivore faunas. The comparatively narrow food base available to carnivores in these paleosystems raises the possibility that predator–prey interactions contributed to unstable ecosystems by driving populations to extinction. Here, we develop a model of predator–prey interactions based on diversity, abundance and body size patterns observed in the Permo‐Triassic vertebrate fossil record of the Karoo Basin, South Africa. Our simulations reflect empirical evidence that despite relatively high carnivore: herbivore species ratios, herbivore abundances were sufficient for carnivores to maintain required intake levels through most of the Karoo sequence. However, high mortality rates amongst herbivore populations, even accounting for birth rates of different‐sized species, are predicted for assemblages immediately preceding the end‐Guadalupian and end‐Permian mass extinctions, as well as in the Middle Triassic when archosaurs replaced therapsids as the dominant terrestrial fauna. These results suggest that high rates of herbivore mortality could have played an important role in biodiversity declines leading up to each of these turnover events. Such declines would have made the systems especially vulnerable to subsequent stochastic events and environmental perturbations, culminating in large‐scale extinctions.     

Pleistocene megafaunal interaction networks became more vulnerable after human arrival

The end of the Pleistocene was marked by the extinction of almost all large land mammals worldwide except in Africa. Although the debate on Pleistocene extinctions has focused on the roles of climate change and humans, the impact of perturbations depends on properties of ecological communities, such as species composition and the organization of ecological interactions. Here, we combined palaeoecological and ecological data, food-web models and community stability analysis to investigate if differences between Pleistocene and modern mammalian assemblages help us understand why the megafauna died out in the Americas while persisting in Africa. We show Pleistocene and modern assemblages share similar network topology, but differences in richness and body size distributions made Pleistocene communities significantly more vulnerable to the effects of human arrival. The structural changes promoted by humans in Pleistocene networks would have increased the likelihood of unstable dynamics, which may favour extinction cascades in communities facing extrinsic perturbations. Our findings suggest that the basic aspects of the organization of ecological communities may have played an important role in major extinction events in the past. Knowledge of community-level properties and their consequences to dynamics may be critical to understand past and future extinctions.     

Permian and early Triassic isotopic records of carbon and strontium in Australia and a scenario of events about the Permian‐Triassic boundary

The negative shift in δ¹³C values of carbonate carbon at the Permian/Triassic boundary is one of the better documented geochemical signatures of a mass extinction event. The similar negative shift in δ¹³C values in organic carbon from Permian/Triassic boundary marine sediments in Austria and Canada is shown to occur also in marine and non‐marine sediments from Australian sedimentary basins. This negative shift in δ¹³C values is used to calibrate Australian sections lacking diagnostic faunal elements identifying the Permian/Triassic boundary. The minimum in the carbonate ⁸⁷Sr/⁸⁶Sr seawater curve from carbonates across the Guadalupian/Ochoan Stage boundary, mainly from North America, is shown to occur also in brachiopod calcite mainly from the Bowen Basin of eastern Australia, hence providing a second calibration point in the Australian sedimentary record. These two geochemical events support a model of a runaway greenhouse developing about the Permian/Triassic boundary; this is inferred to have contributed to the end‐Permian mass extinction.     

Diversity partitioning in Permian and Early Triassic benthic ecosystems of the Western USA: a comparison

This paper compares the relative contributions of within-habitat diversity [alpha-diversity] and between-habitat-diversity [beta-diversity] to regional diversity [gamma-diversity] in marine benthic communities of the western US before and after the end-Permian mass extinction. We found that presumably cool-water faunas from the Permian Gerster Limestone and the Park City Formation had low alpha- and beta-diversities, comparable to those of low diverse faunas of the Early Triassic. In contrast, tropical Permian faunas had much higher alpha-diversities and a variable pattern of beta-diversity: Whereas faunas of space-limited bioherms show a positive correlation between beta-diversity and gamma-diversity, beta-diversity in level-bottom faunas is elevated only when gamma-diversity is very high (>250 species). This contrasting pattern probably reflects differential effects of interspecific competition on habitat partitioning. In low-competitive level-bottom faunas, species are able to coexist until competition forces species into their ecological optima, thereby increasing beta-diversity. This effect occurs at much lower gamma-diversities in more competitive reef-bound faunas, causing the observed positive correlation between beta- and gamma-diversity. We suggest that differences in the level of interspecific competition and hence diversity partitioning between Permian and Triassic benthic communities result from the higher average metabolic rates in the Mesozoic mollusc-dominated benthos in contrast to their Permian counterparts.