Abundance-diversity relationship as a unique signature of temporal scaling in the fossil record.

Species diversity increases with the temporal grain of samples according to the species-time relationship (STR), impacting palaeoecological analyses because the temporal grain (time averaging) of fossil assemblages varies by several orders of magnitude. We predict a positive relation between total abundance and sample size-independent diversity (ADR) in fossil assemblages because an increase in time averaging, determined by a decreasing sediment accumulation, should increase abundance and depress species dominance. We demonstrate that, in contrast to negative ADR of non-averaged living assemblages, the ADR of Holocene fossil assemblages is positive, unconditionally or when conditioned on the energy availability gradient. However, the positive fossil ADR disappears when conditioned on sediment accumulation, demonstrating that ADR is a signature of diversity scaling induced by variable time averaging. Conditioning ADR on sediment accumulation can identify and remove the scaling effect caused by time averaging, providing an avenue for unbiased biodiversity comparisons across space and time.

Fossil evidence for vampire squid inhabiting oxygen-depleted ocean zones since at least the Oligocene.

A marked 120 My gap in the fossil record of vampire squids separates the only extant species (Vampyroteuthis infernalis) from its Early Cretaceous, morphologically-similar ancestors. While the extant species possesses unique physiological adaptations to bathyal environments with low oxygen concentrations, Mesozoic vampyromorphs inhabited epicontinental shelves. However, the timing of their retreat towards bathyal and oxygen-depleted habitats is poorly documented. Here, we document a first record of a post-Mesozoic vampire squid from the Oligocene of the Central Paratethys represented by a vampyromorph gladius. We assign Necroteuthis hungarica to the family Vampyroteuthidae that links Mesozoic loligosepiids with Recent Vampyroteuthis. Micropalaeontological, palaeoecological, and geochemical analyses demonstrate that Necroteuthis hungarica inhabited bathyal environments with bottom-water anoxia and high primary productivity in salinity-stratified Central Paratethys basins. Vampire squids were thus adapted to bathyal, oxygen-depleted habitats at least since the Oligocene. We suggest that the Cretaceous and the early Cenozoic OMZs triggered their deep-sea specialization.

Ecological regime shift preserved in the Anthropocene stratigraphic record.

Palaeoecological data are unique historical archives that extend back far beyond the last several decades of ecological observations. However, the fossil record of continental shelves has been perceived as too coarse (with centennial-millennial resolution) and incomplete to detect processes occurring at yearly or decadal scales relevant to ecology and conservation. Here, we show that the youngest (Anthropocene) fossil record on the northern Adriatic continental shelf provides decadal-scale resolution that accurately documents an abrupt ecological change affecting benthic communities during the twentieth century. The magnitude and the duration of the twentieth century shift in body size of the bivalve Corbula gibba is unprecedented given that regional populations of this species were dominated by small-size classes throughout the Holocene. The shift coincided with compositional changes in benthic assemblages, driven by an increase from approximately 25% to approximately 70% in median per-assemblage abundance of C. gibba. This regime shift increase occurred preferentially at sites that experienced at least one hypoxic event per decade in the twentieth century. Larger size and higher abundance of C. gibba probably reflect ecological release as it coincides with an increase in the frequency of seasonal hypoxia that triggered mass mortality of competitors and predators. Higher frequency of hypoxic events is coupled with a decline in the depth of intense sediment mixing by burrowing benthic organisms from several decimetres to less than 20 cm, significantly improving the stratigraphic resolution of the Anthropocene fossil record and making it possible to detect sub-centennial ecological changes on continental shelves.

A decline in molluscan carbonate production driven by the loss of vegetated habitats encoded in the Holocene sedimentary record of the Gulf of Trieste.

Carbonate sediments in non-vegetated habitats on the north-east Adriatic shelf are dominated by shells of molluscs. However, the rate of carbonate molluscan production prior to the 20th century eutrophication and overfishing on this and other shelves remains unknown because: (i) monitoring of ecosystems prior to the 20th century was scarce; and (ii) ecosystem history inferred from cores is masked by condensation and mixing. Here, based on geochronological dating of four bivalve species, carbonate production during the Holocene is assessed in the Gulf of Trieste, where algal and seagrass habitats underwent a major decline during the 20th century. Assemblages of sand-dwelling Gouldia minima and opportunistic Corbula gibba are time-averaged to >1000 years and Corbula gibba shells are older by >2000 years than shells of co-occurring Gouldia minima. This age difference is driven by temporally disjunct production of two species coupled with decimetre-scale mixing. Stratigraphic unmixing shows that Corbula gibba declined in abundance during the highstand phase and increased again during the 20th century. In contrast, one of the major contributors to carbonate sands - Gouldia minima - increased in abundance during the highstand phase, but declined to almost zero abundance over the past two centuries. Gouldia minima and herbivorous gastropods associated with macroalgae or seagrasses are abundant in the top-core increments but are rarely alive. Although Gouldia minima is not limited to vegetated habitats, it is abundant in such habitats elsewhere in the Mediterranean Sea. This live-dead mismatch reflects the difference between highstand baseline communities (with soft-bottom vegetated zones and hard-bottom Arca beds) and present-day oligophotic communities with organic-loving species. Therefore, the decline in light penetration and the loss of vegetated habitats with high molluscan production traces back to the 19th century. More than 50% of the shells on the sea floor in the Gulf of Trieste reflect inactive production that was sourced by heterozoan carbonate factory in algal or seagrass habitats.

Deep-water cirripedes colonizing dead shells of the cephalopod Nautilus macromphalus from New Caledonian waters.

Fossil cephalopods are frequently encrusted by epibionts; however, determining whether encrustation occurred prior to or post-mortem to the host, and whether the final environment of deposition corresponds to the habitat of encrustation is complex. The present paper describes cirripede epibionts, their calcareous bases and their attachment scars on 6 post-mortem shells of Nautilus macromphalus, collected from deep water off New Caledonia. The cirripedes have left both cemented calcareous bases of Hexelasma and scars associated with bioerosion and discoloration produced by verrucomorph barnacles. Live cirripedes included a Metaverruca recta, with articulated opercular plates and organic tissue (on a shell that had been exposed on the sea floor for at least 150 years), and specimens of Hexelasma velutinum, one of which was partly attached to an internal surface of a shell. The disposition of verrucomorphs indicates that most Nautilus shells were colonized post-mortem rather than during a floating stage. However, as cirripedes are known to have colonized living Nautilus, some Hexelasma, preserved only as calcareous eroded bases, may represent specimens that settled on a living Nautilus. The degree of bioerosion and discoloration induced by verrucomorph barnacles varies according to the surface preservation of Nautilus shells, with deeper and discolored traces preserved on old and degraded shells. Traces made by verrucomorphs described here are ellipsoidal and a new ichnotaxon, Anellusichnus ellipticus, is proposed to accommodate them. Importantly, verrucomorphs and other cirripede taxa with membranous bases that were attached to pristine shells may not leave any substantial scars, and, thus, will be difficult to detect in the fossil record.

Molluscan benthic communities at Brijuni Islands (northern Adriatic Sea) shaped by Holocene sea-level rise and recent human eutrophication and pollution.

The effects of and the interplay between natural and anthropogenic influences on the composition of benthic communities over long time spans are poorly understood. Based on a 160-cm-long sediment core collected at 44 m water depth in the NE Adriatic Sea (Brijuni Islands, Croatia), we document changes in molluscan communities since the Holocene transgression ~11,000 years ago and assess how they were shaped by environmental changes. We find that (1) a transgressive lag deposit with a mixture of terrestrial and marine species contains abundant seagrass-associated gastropods and epifaunal suspension-feeding bivalves, (2) the maximum-flooding phase captures the establishment of epifaunal bivalve-dominated biostromes in the photic zone, and (3) the highstand phase is characterized by increasing infaunal suspension feeders and declining seagrass-dwellers in bryozoan-molluscan muddy sands. Changes in the community composition between the transgressive and the highstand phase can be explained by rising sea level, reduced light penetration, and increase in turbidity, as documented by the gradual up-core shift from coarse molluscan skeletal gravel with seagrass-associated molluscs to bryozoan sandy muds. In the uppermost 20 cm (median age <200 years), however, epifaunal and grazing species decline and deposit-feeding and chemosymbiotic species increase in abundance. These changes concur with rising concentrations of nitrogen and organic pollutants due to the impact of eutrophication, pollution, and trawling in the 20th century. The late highstand benthic assemblages with abundant bryozoans, high molluscan diversity, and abundance of soft-bottom epi- and infaunal filter feeders and herbivores represent the circalittoral baseline community largely unaffected by anthropogenic impacts.

20th century increase in body size of a hypoxia-tolerant bivalve documented by sediment cores from the northern Adriatic Sea (Gulf of Trieste).

An increase in the frequency of hypoxia, mucilages, and sediment pollution occurred in the 20th century in the Adriatic Sea. To assess the effects of these impacts on bivalves, we evaluate temporal changes in size structure of the opportunistic bivalve Corbula gibba in four sediment cores that cover the past ~500 years in the northern, eutrophic part and ~10,000 years in the southern, mesotrophic part of the Gulf of Trieste. Assemblages exhibit a stable size structure during the highstand phase but shift to bimodal distributions and show a significant increase in the 95th percentile size during the 20th century. This increase in size by 2-3 mm is larger than the northward size increase associated with the transition from mesotrophic to eutrophic habitats. It coincides with increasing concentrations of total organic carbon and nitrogen, and can be related to enhanced food supply and by the tolerance of C. gibba to hypoxia.

Historical ecology of a biological invasion: the interplay of eutrophication and pollution determines time lags in establishment and detection.

Human disturbance modifies selection regimes, depressing native species fitness and enabling the establishment of non-indigenous species with suitable traits. A major impediment to test the effect of disturbance on invasion success is the lack of long-term data on the history of invasions. Here, we overcome this problem and reconstruct the effect of disturbance on the invasion of the bivalve Anadara transversa from sediment cores in the Adriatic Sea. We show that (1) the onset of major eutrophication in the 1970s shifted communities towards species tolerating hypoxia, and (2) A. transversa was introduced in the 1970s but failed to reach reproductive size until the late 1990s because of metal contamination, resulting in an establishment and detection lag of ~25 years. Subfossil assemblages enabled us to (1) disentangle the distinct stages of invasion, (2) quantify time-lags and (3) finely reconstruct the interaction between environmental factors and the invasion process, showing that while disturbance does promote invasions, a synergism of multiple disturbances can shift selection regimes beyond tolerance limits and induce significant time lags in establishment. The quantification of these time lags enabled us to reject the hypothesis that aquaculture was an initial vector of introduction, making shipping the most probable source.

Holocene ecosystem shifts and human-induced loss of Arca and Ostrea shell beds in the north-eastern Adriatic Sea.

The molluscan assemblages in a sediment core from the north-eastern Adriatic show significant compositional changes over the past 10,000yrs related to (1) natural deepening driven by the post-glacial sea-level rise, (2) increasing abundance of skeletal sand and gravel, and (3) anthropogenic impacts. The transgressive phase (10,000-6000 BP) is characterized by strongly time-averaged communities dominated by infaunal bivalves. During the early highstand (6000-4000 BP), the abundance of epifaunal filter feeders and grazers increases, and gastropods become more important. Epifaunal dominance culminates during the late highstand (4000-2000 BP) with the development of extensive shell beds formed by large-sized Arca noae and Ostrea sp. bivalves. This community persists until the early 20th century, when it falls victim to multiple anthropogenic impacts, mainly bottom trawling, and is substituted by an infauna-dominated community indicative of instability, disturbance and organic enrichment. The re-establishment of this unique shell-bed ecosystem can be a goal for restoration efforts.

Assessing kinetic fractionation in brachiopod calcite using clumped isotopes.

Brachiopod shells are the most widely used geological archive for the reconstruction of the temperature and the oxygen isotope composition of Phanerozoic seawater. However, it is not conclusive whether brachiopods precipitate their shells in thermodynamic equilibrium. In this study, we investigated the potential impact of kinetic controls on the isotope composition of modern brachiopods by measuring the oxygen and clumped isotope compositions of their shells. Our results show that clumped and oxygen isotope compositions depart from thermodynamic equilibrium due to growth rate-induced kinetic effects. These departures are in line with incomplete hydration and hydroxylation of dissolved CO2. These findings imply that the determination of taxon-specific growth rates alongside clumped and bulk oxygen isotope analyses is essential to ensure accurate estimates of past ocean temperatures and seawater oxygen isotope compositions from brachiopods.

Responses of molluscan communities to centuries of human impact in the northern Adriatic Sea.

In sediment cores spanning ~500 years of history in the Gulf of Trieste, down-core changes in molluscan community structure are characterized by marked shifts in species and functional composition. Between the 16th and 19th century, a strong heavy metal contamination of the sediments, most notably by Hg, together with the effects of natural climatic oscillations (increased sedimentation and organic enrichment) drive community changes. Since the early 20th century up to 2013, the combined impacts of cultural eutrophication, frequent hypoxic events and intensifying bottom trawling replace heavy metal contamination and climatic factors as the main drivers. The pollution-tolerant and opportunistic bivalve Corbula gibba and the scavenging gastropod Nassarius pygmaeus significantly increase in abundance during the 20th century, while species more sensitive to disturbances and hypoxia such as Turritella communis and Kurtiella bidentata become rare or absent. An infaunal life habit and scavenging emerge as the dominant life strategies during the late 20th century. Down-core shifts in the proportional abundances of molluscan species and functional groups represent a sensitive proxy for past ecological changes and reveal a century-long anthropogenic impact as the main driver behind these processes in the northern Adriatic Sea, offering also a unique perspective for other shallow marine ecosystems worldwide.

Nineteenth-century collapse of a benthic marine ecosystem on the open continental shelf.

The soft-sediment seafloor of the open continental shelf is among the least-known biomes on Earth, despite its high diversity and importance to fisheries and biogeochemical cycling. Abundant dead shells of epifaunal suspension-feeding terebratulid brachiopods (Laqueus) and scallops on the now-muddy mainland continental shelf of southern California reveal the recent, previously unsuspected extirpation of an extensive offshore shell-gravel ecosystem, evidently driven by anthropogenic siltation. Living populations of attached epifauna, which formerly existed in a middle- and outer-shelf mosaic with patches of trophically diverse muds, are restricted today to rocky seafloor along the shelf edge and to the sandier shelves of offshore islands. Geological age-dating of 190 dead brachiopod shells shows that (i) no shells have been produced on the mainland shelf within the last 100 years, (ii) their shell production declined steeply during the nineteenth century, and (iii) they had formerly been present continuously for at least 4 kyr. This loss, sufficiently rapid (less than or equal to 100 years) and thorough to represent an ecosystem collapse, coincides with intensification of alluvial-plain land use in the nineteenth century, particularly livestock grazing. Extirpation was complete by the start of twentieth-century urbanization, warming, bottom fishing and scientific surveys. The loss of this filter-feeding fauna and the new spatial homogeneity and dominance of deposit- and detritus-feeders would have altered ecosystem functioning by reducing habitat heterogeneity and seawater filtering. This discovery, attesting to the power of this geological approach to recent ecological transitions, also strongly increases the spatial scope attributable to the negative effects of siltation, and suggests that it has been under-recognized on continental shelves elsewhere as a legacy of coastal land use.

Detecting, sourcing, and age-dating dredged sediments on the open shelf, southern California, using dead mollusk shells.

Molluscan shell debris is an under-exploited means of detecting, sourcing, and age-dating dredged sediments in open-shelf settings. Backscatter features on the Southern California shelf are suggestive of dredged sediment hauled from San Diego Bay but deposited significantly inshore of the EPA-designated ocean disposal site. We find that 36% of all identifiable bivalve shells >2mm (44% of shells >4mm) in sediment samples from this 'short dump' area are from species known to live exclusively in the Bay; such shells are absent at reference sites of comparable water depth, indicating that their presence in the short-dump area signals non-compliant disposal rather than natural offshore transport or sea level rise. These sediments lack the shells of species that invaded California bays in the 1970s, suggesting that disposal preceded federal regulations. This inexpensive, low-tech method, with its protocol for rejecting alternative hypotheses, will be easy to adapt in other settings.

Unifying latitudinal gradients in range size and richness across marine and terrestrial systems.

Many marine and terrestrial clades show similar latitudinal gradients in species richness, but opposite gradients in range size-on land, ranges are the smallest in the tropics, whereas in the sea, ranges are the largest in the tropics. Therefore, richness gradients in marine and terrestrial systems do not arise from a shared latitudinal arrangement of species range sizes. Comparing terrestrial birds and marine bivalves, we find that gradients in range size are concordant at the level of genera. Here, both groups show a nested pattern in which narrow-ranging genera are confined to the tropics and broad-ranging genera extend across much of the gradient. We find that (i) genus range size and its variation with latitude is closely associated with per-genus species richness and (ii) broad-ranging genera contain more species both within and outside of the tropics when compared with tropical- or temperate-only genera. Within-genus species diversification thus promotes genus expansion to novel latitudes. Despite underlying differences in the species range-size gradients, species-rich genera are more likely to produce a descendant that extends its range relative to the ancestor's range. These results unify species richness gradients with those of genera, implying that birds and bivalves share similar latitudinal dynamics in net species diversification.

Onshore-offshore gradient in metacommunity turnover emerges only over macroevolutionary time-scales.

Invertebrate lineages tend to originate and become extinct at a higher rate in onshore than in offshore habitats over long temporal durations (more than 10 Myr), but it remains unclear whether this pattern scales down to durations of stages (less than 5 Myr) or even sequences (less than 0.5 Myr). We assess whether onshore-offshore gradients in long-term turnover between the tropical Eocene and the warm-temperate Plio-Pleistocene can be extrapolated from gradients in short-term turnover, using abundances of molluscan species from bulk samples in the northeast Atlantic Province. We find that temporal turnover of metacommunities does not significantly decline with depth over short durations (less than 5 Myr), but significantly declines with depth between the Eocene and Plio-Pleistocene (approx. 50 Myr). This decline is determined by a higher onshore extinction of Eocene genera and families, by a higher onshore variability in abundances of genera and families, and by an onshore expansion of genera and families that were frequent offshore in the Eocene. Onshore-offshore decline in turnover thus emerges only over long temporal durations. We suggest that this emergence is triggered by abrupt and spatially extensive climatic or oceanographic perturbations that occurred between the Eocene and Plio-Pleistocene. Plio-Pleistocene metacommunities show a high proportion of bathymetric generalists, in contrast to Eocene metacommunities. Accordingly, the net cooling and weaker thermal gradients may have allowed offshore specialists to expand into onshore habitats and maintain their presence in offshore habitats.

Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient.

Latitudinal diversity gradients are underlain by complex combinations of origination, extinction, and shifts in geographic distribution and therefore are best analyzed by integrating paleontological and neontological data. The fossil record of marine bivalves shows, in three successive late Cenozoic time slices, that most clades (operationally here, genera) tend to originate in the tropics and then expand out of the tropics (OTT) to higher latitudes while retaining their tropical presence. This OTT pattern is robust both to assumptions on the preservation potential of taxa and to taxonomic revisions of extant and fossil species. Range expansion of clades may occur via "bridge species," which violate climate-niche conservatism to bridge the tropical-temperate boundary in most OTT genera. Substantial time lags (∼5 Myr) between the origins of tropical clades and their entry into the temperate zone suggest that OTT events are rare on a per-clade basis. Clades with higher diversification rates within the tropics are the most likely to expand OTT and the most likely to produce multiple bridge species, suggesting that high speciation rates promote the OTT dynamic. Although expansion of thermal tolerances is key to the OTT dynamic, most latitudinally widespread species instead achieve their broad ranges by tracking widespread, spatially-uniform temperatures within the tropics (yielding, via the nonlinear relation between temperature and latitude, a pattern opposite to Rapoport's rule). This decoupling of range size and temperature tolerance may also explain the differing roles of species and clade ranges in buffering species from background and mass extinctions.

The effects of temporal resolution on species turnover and on testing metacommunity models.

Patterns of low temporal turnover in species composition found within paleoecological time series contrast with the high turnover predicted by neutral metacommunity models and thus have been used to support nonneutral models. However, these predictions assume temporal resolution on the scale of a season or year, whereas individual fossil assemblages are typically time averaged to decadal or centennial timescales. We simulate the effects of time averaging by building time-averaged assemblages from local dispersal-limited, nonaveraged assemblages and compare the predicted turnover with observed patterns in mollusk and ostracod fossil records. Time averaging substantially reduces temporal turnover such that neutral predictions converge with those of trade-off and density-dependent models, and it tends to decrease species dominance and increase the proportion of rare species. Observed turnover rates are comparable to an appropriately scaled neutral model: patterns of high community stability can be produced or reinforced by time averaging alone. The community attributes of local time-averaged assemblages approach those of the metacommunity. Time-averaged assemblages are thus unlikely to capture attributes arising from processes operating at small spatial scales, but they should do well at capturing the turnover and diversity of metacommunities and thus will be a valuable basis for analyzing the large-scale processes that determine metacommunity evolution.

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.