Global warming generates predictable extinctions of warm- and cold-water marine benthic invertebrates via thermal habitat loss.

Anthropogenic global warming is redistributing marine life and may threaten tropical benthic invertebrates with several potential extinction mechanisms. The net impact of climate change on geographical extinction risk nevertheless remains uncertain. Evidence of widespread climate-driven extinctions and of potentially unidentified mechanisms exists in the fossil record. We quantify organism extinction risk across thermal habitats, estimated by paleoclimate reconstructions, over the past 300 million years. Extinction patterns at seven known events of rapid global warming (hyperthermals) differ significantly from typical patterns, resembling those driven by global geometry under simulated global warming. As isotherms move poleward with warming, the interaction between the geometry of the globe and the temperature-latitude relationship causes an uneven loss of thermal habitat and a bimodal latitudinal distribution of extinctions. Genera with thermal optima warmer than ~21°C show raised extinction odds, while extinction odds continually increase for genera with optima below ~11°C. Genera preferring intermediate temperatures generally have no additional extinction risk during hyperthermals, except under extreme conditions as the end-Permian mass extinction. Widespread present-day climate-driven range shifts indicate that occupancy loss is already underway. Given the most-likely projections of modern warming, our model, validated by seven past hyperthermal events, indicates that sustained warming has the potential to annihilate cold-water habitat and its endemic species completely within centuries.

Diversity partitioning in Phanerozoic benthic marine communities.

Biotic interactions such as competition, predation, and niche construction are fundamental drivers of biodiversity at the local scale, yet their long-term effect during earth history remains controversial. To test their role and explore potential limits to biodiversity, we determine within-habitat (alpha), between-habitat (beta), and overall (gamma) diversity of benthic marine invertebrates for Phanerozoic geological formations. We show that an increase in gamma diversity is consistently generated by an increase in alpha diversity throughout the Phanerozoic. Beta diversity drives gamma diversity only at early stages of diversification but remains stationary once a certain gamma level is reached. This mode is prevalent during early- to mid-Paleozoic periods, whereas coupling of beta and gamma diversity becomes increasingly weak toward the recent. Generally, increases in overall biodiversity were accomplished by adding more species to local habitats, and apparently this process never reached saturation during the Phanerozoic. Our results provide general support for an ecological model in which diversification occurs in successive phases of progressing levels of biotic interactions.

Victims of ancient hyperthermal events herald the fates of marine clades and traits under global warming.

Organismic groups vary non-randomly in their vulnerability to extinction. However, it is unclear whether the same groups are consistently vulnerable, regardless of the dominant extinction drivers, or whether certain drivers have their own distinctive and predictable victims. Given the challenges presented by anthropogenic global warming, we focus on changes in extinction selectivity trends during ancient hyperthermal events: geologically rapid episodes of global warming. Focusing on the fossil record of the last 300 million years, we identify clades and traits of marine ectotherms that were more prone to extinction under the onset of six hyperthermal events than during other times. Hyperthermals enhanced the vulnerability of marine fauna that host photosymbionts, particularly zooxanthellate corals, the reef environments they provide, and genera with actively burrowing or swimming adult life-stages. The extinction risk of larger sized fauna also increased relative to non-hyperthermal times, while genera with a poorly buffered internal physiology did not become more vulnerable on average during hyperthermals. Hyperthermal-vulnerable clades include rhynchonelliform brachiopods and bony fish, whereas resistant clades include cartilaginous fish, and ostreid and venerid bivalves. These extinction responses in the geological past mirror modern responses of these groups to warming, including range-shift magnitudes, population losses, and experimental performance under climate-related stressors. Accordingly, extinction mechanisms distinctive to rapid global warming may be indicated, including sensitivity to warming-induced seawater deoxygenation. In anticipation of modern warming-driven marine extinctions, the trends illustrated in the fossil record offer an expedient preview.

Persistent ecological shifts in marine molluscan assemblages across the end-Cretaceous mass extinction.

Contemporary biodiversity loss and population declines threaten to push the biosphere toward a tipping point with irreversible effects on ecosystem composition and function. As a potential example of a global-scale regime shift in the geological past, we assessed ecological changes across the end-Cretaceous mass extinction based on molluscan assemblages at four well-studied sites. By contrasting preextinction and postextinction rank abundance and numerical abundance in 19 molluscan modes of life--each defined as a unique combination of mobility level, feeding mode, and position relative to the substrate--we find distinct shifts in ecospace utilization, which significantly exceed predictions from null models. The magnitude of change in functional traits relative to normal temporal fluctuations at far-flung sites indicates that molluscan assemblages shifted to differently structured systems and faunal response was global. The strengths of temporal ecological shifts, however, are mostly within the range of preextinction site-to-site variability, demonstrating that local ecological turnover was similar to geographic variation over a broad latitudinal range. In conjunction with varied site-specific temporal patterns of individual modes of life, these spatial and temporal heterogeneities argue against a concerted phase shift of molluscan assemblages from one well-defined regime to another. At a broader ecological level, by contrast, congruent tendencies emerge and suggest deterministic processes. These patterns comprise the well-known increase of deposit-feeding mollusks in postextinction assemblages and increases in predators and predator-resistant modes of life, i.e., those characterized by elevated mobility and infaunal life habits.

Ocean warming affected faunal dynamics of benthic invertebrate assemblages across the Toarcian Oceanic Anoxic Event in the Iberian Basin (Spain).

The Toarcian Oceanic Anoxic Event (TOAE; Early Jurassic, ca. 182 Ma ago) represents one of the major environmental disturbances of the Mesozoic and is associated with global warming, widespread anoxia, and a severe perturbation of the global carbon cycle. Warming-related dysoxia-anoxia has long been considered the main cause of elevated marine extinction rates, although extinctions have been recorded also in environments without evidence for deoxygenation. We addressed the role of warming and disturbance of the carbon cycle in an oxygenated habitat in the Iberian Basin, Spain, by correlating high resolution quantitative faunal occurrences of early Toarcian benthic marine invertebrates with geochemical proxy data (δ18O and δ13C). We find that temperature, as derived from the δ18O record of shells, is significantly correlated with taxonomic and functional diversity and ecological composition, whereas we find no evidence to link carbon cycle variations to the faunal patterns. The local faunal assemblages before and after the TOAE are taxonomically and ecologically distinct. Most ecological change occurred at the onset of the TOAE, synchronous with an increase in water temperatures, and involved declines in multiple diversity metrics, abundance, and biomass. The TOAE interval experienced a complete turnover of brachiopods and a predominance of opportunistic species, which underscores the generality of this pattern recorded elsewhere in the western Tethys Ocean. Ecological instability during the TOAE is indicated by distinct fluctuations in diversity and in the relative abundance of individual modes of life. Local recovery to ecologically stable and diverse post-TOAE faunal assemblages occurred rapidly at the end of the TOAE, synchronous with decreasing water temperatures. Because oxygen-depleted conditions prevailed in many other regions during the TOAE, this study demonstrates that multiple mechanisms can be operating simultaneously with different relative contributions in different parts of the ocean.

Temperature-related body size change of marine benthic macroinvertebrates across the Early Toarcian Anoxic Event.

The Toarcian Oceanic Anoxic Event (TOAE, Early Jurassic, ~182 Ma ago) was characterised by severe environmental perturbations which led to habitat degradation and extinction of marine species. Warming-induced anoxia is usually identified as main driver, but because marine life was also affected in oxygenated environments the role of raised temperature and its effects on marine life need to be addressed. Body size is a fundamental characteristic of organisms and is expected to decrease as a response to heat stress. We present quantitative size data of bivalves and brachiopods across the TOAE from oxygenated habitats in the Iberian Basin, integrated with geochemical proxy data (δ13C and δ18O), to investigate the relationship between changes in temperature and body size. We find a strong negative correlation between the mean shell size of bivalve communities and isotope-derived temperature estimates, suggesting heat stress as a main cause of body size reduction. While within-species size changes were minor, we identify changes in the abundance of differently sized species as the dominant mechanism of reduced community shell size during the TOAE. Brachiopods experienced a wholesale turnover across the early warming phase and were replaced by a virtually monotypic assemblage of a smaller-sized, opportunistic species.

Marine Biodiversity and Geographic Distributions Are Independent on Large Scales.

Fundamental ecological and evolutionary theories, such as community saturation and diversity-dependent diversification, assume that biotic competition restricts resource use, and thus limits realized niche breadth and geographic range size [1-3]. This principle is called competitive exclusion. The corollary (ecological release) posits that, after competitors disappear from a region, species that were previously excluded will invade. Hundreds of field experiments have demonstrated ecological release in living populations. However, few of these studies were conducted in marine environments, and almost no work extended beyond 10 years and 1,000 km2 [4, 5]. In limited investigation of marine taxa at larger spatiotemporal scales, macroecologists and paleobiologists have observed little evidence of competitive exclusion [6-9]. Here, we quantified spatial trends in the rich and densely sampled fossil history of brachiopods and bivalves, while accounting for inconsistent sampling coverage through time using a new method of spatial standardization. The number of potential competitors in a region did not explain the geographic distribution of constituent species or genera. Furthermore, although ecological release predicts species to expand after extinction events, survivors of intervals with net species loss expanded as rarely as species in other intervals. Regression model estimates indicated different spatial responses of brachiopods and bivalves, and of habitat specialists and generalists, but no effect from changes in number of potential competitors. Biotic competition may control the distribution of populations, but, on larger spatiotemporal scales, non-competitive factors may have driven biogeographic patterns of brachiopods and bivalves.

Resilience of marine invertebrate communities during the early Cenozoic hyperthermals.

The hyperthermal events of the Cenozoic, including the Paleocene-Eocene Thermal Maximum, provide an opportunity to investigate the potential effects of climate warming on marine ecosystems. Here, we examine the shallow benthic marine communities preserved in the late Cretaceous to Eocene strata on the Gulf Coastal Plain (United States). In stark contrast to the ecological shifts following the end-Cretaceous mass extinction, our data show that the early Cenozoic hyperthermals did not have a long-term impact on the generic diversity nor composition of the Gulf Coastal Plain molluscan communities. We propose that these communities were resilient to climate change because molluscs are better adapted to high temperatures than other taxa, as demonstrated by their physiology and evolutionary history. In terms of resilience, these communities differ from other shallow-water carbonate ecosystems, such as reef communities, which record significant changes during the early Cenozoic hyperthermals. These data highlight the strikingly different responses of community types, i.e., the almost imperceptible response of molluscs versus the marked turnover of foraminifera and reef faunas. The impact on molluscan communities may have been low because detrimental conditions did not devastate the entire Gulf Coastal Plain, allowing molluscs to rapidly recolonise vacated areas once harsh environmental conditions ameliorated.

The effects of taxonomic standardization on sampling-standardized estimates of historical diversity.

Occurrence-based databases such as the Palaeobiology database (PBDB) provide means of accommodating the heterogeneities of the fossil record when evaluating historical diversity patterns. Although palaeontologists have given ample attention to the effects of taxonomic practice on diversity patterns derived from synoptic databases (those using first and last appearances of taxa), workers have not examined the effects of taxonomic error on occurrence-based diversity studies. Here, we contrast diversity patterns and diversity dynamics between raw data and taxonomically vetted data in the PBDB to evaluate the effects of taxonomic errors. We examine three groups: Palaeozoic gastropods, Jurassic bivalves and Cenozoic bivalves. We contrast genus-level diversity patterns based on: (i) all occurrences assigned to a genus (i.e. both species records and records identifying only the genus), (ii) only occurrences for which a species is identified, and (iii) only occurrences for which a species is identified, but after vetting the genus to which the species is assigned. Extensive generic reassignments elevate origination and extinction rates within Palaeozoic gastropods and origination rates within Cenozoic bivalves. However, vetting increases generic richness markedly only for Cenozoic bivalves, and even then the increase is less than 10%. Moreover, the patterns of standing generic richness are highly similar under all three data treatments. Unless our results are unusual, taxonomic standardization can elevate diversity dynamics in some cases, but it will not greatly change inferred richness over time.

Detecting hybridization between sister species of Terebratulina (Brachiopoda, Cancellothyridoidea) in the North Atlantic: morphology versus molecules.

Investigating samples of the cancellothyridid brachiopod Terebratulina collected during the IceAGE (Me85/3) expedition of RV METEOR at the continental shelf around Iceland with both morphometrical and molecular methods, we were for the first time able to detect a hybridization event between brachiopod sister species, which are thought to have separated 60 MYA. Terebratulina retusa and T. septentrionalis can clearly be distinguished on the basis of consistent species-specific molecular signatures in both mitochondrial and nuclear markers, whereas morphometrical analyses proved to be less reliable for species determination than previously thought. Two out of 28 specimens were identified as offspring of a one-way hybridization event between T. retusa eggs and T. septentrionalis sperm. Whereas the fossil record of Terebratulina in the North Atlantic region is too fragmentary to reconstruct the history of the hybridization event, the different life history traits of the two species and current oceanographic conditions around Iceland offer plausible explanations for the occurrence of crossbreeds in this common brachiopod genus.

Interdependence of specialization and biodiversity in Phanerozoic marine invertebrates.

Studies of the dynamics of biodiversity often suggest that diversity has upper limits, but the complex interplay between ecological and evolutionary processes and the relative role of biotic and abiotic factors that set upper limits to diversity are poorly understood. Here we statistically assess the relationship between global biodiversity and the degree of habitat specialization of benthic marine invertebrates over the Phanerozoic eon. We show that variation in habitat specialization correlates positively with changes in global diversity, that is, times of high diversity coincide with more specialized faunas. We identify the diversity dynamics of specialists but not generalists, and origination rates but not extinction rates, as the main drivers of this ecological interdependence. Abiotic factors fail to show any significant relationship with specialization. Our findings suggest that the overall level of specialization and its fluctuations over evolutionary timescales are controlled by diversity-dependent processes--driven by interactions between organisms competing for finite resources.

Rebuilding biodiversity of Patagonian marine molluscs after the end-Cretaceous mass extinction.

We analysed field-collected quantitative data of benthic marine molluscs across the Cretaceous-Palaeogene boundary in Patagonia to identify patterns and processes of biodiversity reconstruction after the end-Cretaceous mass extinction. We contrast diversity dynamics from nearshore environments with those from offshore environments. In both settings, Early Palaeogene (Danian) assemblages are strongly dominated by surviving lineages, many of which changed their relative abundance from being rare before the extinction event to becoming the new dominant forms. Only a few of the species in the Danian assemblages were newly evolved. In offshore environments, however, two newly evolved Danian bivalve species attained ecological dominance by replacing two ecologically equivalent species that disappeared at the end of the Cretaceous. In both settings, the total number of Danian genera at a locality remained below the total number of late Cretaceous (Maastrichtian) genera at that locality. We suggest that biotic interactions, in particular incumbency effects, suppressed post-extinction diversity and prevented the compensation of diversity loss by originating and invading taxa. Contrary to the total number of genera at localities, diversity at the level of individual fossiliferous horizons before and after the boundary is indistinguishable in offshore environments. This indicates an evolutionary rapid rebound to pre-extinction values within less than ca 0.5 million years. In nearshore environments, by contrast, diversity of fossiliferous horizons was reduced in the Danian, and this lowered diversity lasted for the entire studied post-extinction interval. In this heterogeneous environment, low connectivity among populations may have retarded the recolonisation of nearshore habitats by survivors.

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.

Statistical independence of escalatory ecological trends in Phanerozoic marine invertebrates.

Ecological interactions, such as predation and bioturbation, are thought to be fundamental determinants of macroevolutionary trends. A data set containing global occurrences of Phanerozoic fossils of benthic marine invertebrates shows escalatory trends in the relative frequency of ecological groups, such as carnivores and noncarnivorous infaunal or mobile organisms. Associations between these trends are either statistically insignificant or interpretable as preservational effects. Thus, there is no evidence that escalation drives macroecological trends at global and million-year time scales. We also find that taxonomic richness and occurrence data are cross-correlated, which justifies the traditional use of one as a proxy of the other.