The quality of the fossil record across higher taxa: compositional fidelity of phyla and classes in benthic marine associations.

Although the fossil record preserves a wealth of historical data about past ecosystems, the current paradigm, which postulates that fossils provide faithful archives of ecological information, stems from research primarily focused on a single group of organisms known for their high fossilization potential: molluscs. Here, we quantify the fidelity of higher taxa (six phyla and 11 classes) by comparing live communities and sympatric dead remains (death assemblages) using comprehensive surveys of benthic marine invertebrates from coastal habitats in North Carolina (U.S.A). We found that although community composition differed between the two assemblages across phyla and classes, these differences were predictable with an overabundance of robust and more preservable groups. In addition, dead molluscs appear to be an excellent proxy for all taxa when tracking spatio-temporal patterns and shifts in community structure using a variety of ecological metrics, including measures of α, γ, and ß diversity/evenness. This suggests that despite filters imposed by differential preservation of taxa and time-averaging, the fossil record is likely to be reliable with respect to relative comparisons of composition and diversity in shallow benthic marine paleocommunities. This is consistent with previous work indicating that shallow marine death assemblages can yield robust ecological estimates adequate for assessing the variability of ecosystems that existed under natural, pre-anthropogenic conditions.

Spatial distribution, diversity, and taphonomy of clypeasteroid and spatangoid echinoids of the central Florida Keys.

Background: Irregular echinoids are ecosystem engineers with diverse functional services. Documenting present-day distribution of those widespread organisms is important for understanding their ecological significance and enhancing our ability to interpret their rich fossil record. Methods: This study summarizes SCUBA surveys of clypeasteroid and spatangoid echinoids conducted in 2020 and 2021 along the central part of the Florida Keys. The survey included observations on both live and dead specimens, their distribution, habitat preferences, abundance, and live-dead comparison. Results: Echinoids were found at 17 out of 27 examined sites (63%) and occurred across a wide range of habitats including coastal seagrass meadows, subtidal sand and seagrass settings of the Hawk Channel, backreef sands, and fine muddy sands of deeper forereef habitats. The encountered species, both dead and alive, included Clypeaster rosaceus (four sites), Clypeaster subdepressus (five sites), Encope michelini (three sites), Leodia sexiesperforata (eight sites), Meoma ventricosa (nine sites), and Plagiobrissus grandis (four sites). All sites were dominated by one species, but some sites included up to five echinoid species. Live-dead fidelity was high, including a good agreement in species composition of living and dead assemblages, congruence in species rank abundance, and overlapping spatial distribution patterns. This high fidelity may either reflect long-term persistence of local echinoid populations or fragility of echinoid tests that could prevent post-mortem transport and the formation of time-averaged death assemblages. Regardless of causative factors, the live-dead comparisons suggest that irregular echinoid assemblages, from settings that are comparable to the study area, may provide a fossil record with a high spatial and compositional fidelity. The survey of live fauna is consistent with past regional surveys in terms of identity of observed species, their rank abundance, and their spatial distribution patterns. The results suggest that despite increasingly frequent hurricanes, active seasonal fisheries, massive tourism, and urban development, irregular echinoids continue to thrive across a wide range of habitats where they provide diverse ecosystem services by oxygenating sediments, recycling organic matter, supporting commensal organisms, and providing food to predators. Results reported here document the present-day status of local echinoid populations and should serve as a useful reference point for assessing future regional changes in echinoid distribution and abundance.

Hexagonal Voronoi pattern detected in the microstructural design of the echinoid skeleton.

Repeated polygonal patterns are pervasive in natural forms and structures. These patterns provide inherent structural stability while optimizing strength-per-weight and minimizing construction costs. In echinoids (sea urchins), a visible regularity can be found in the endoskeleton, consisting of a lightweight and resistant micro-trabecular meshwork (stereom). This foam-like structure follows an intrinsic geometrical pattern that has never been investigated. This study aims to analyse and describe it by focusing on the boss of tubercles-spine attachment sites subject to strong mechanical stresses-in the common sea urchin Paracentrotus lividus. The boss microstructure was identified as a Voronoi construction characterized by 82% concordance to the computed Voronoi models, a prevalence of hexagonal polygons, and a regularly organized seed distribution. This pattern is interpreted as an evolutionary solution for the construction of the echinoid skeleton using a lightweight microstructural design that optimizes the trabecular arrangement, maximizes the structural strength and minimizes the metabolic costs of secreting calcitic stereom. Hence, this identification is particularly valuable to improve the understanding of the mechanical function of the stereom as well as to effectively model and reconstruct similar structures in view of future applications in biomimetic technologies and designs.

Resilient biotic response to long-term climate change in the Adriatic Sea.

Preserving adaptive capacities of coastal ecosystems, which are currently facing the ongoing climate warming and a multitude of other anthropogenic impacts, requires an understanding of long-term biotic dynamics in the context of major environmental shifts prior to human disturbances. We quantified responses of nearshore mollusk assemblages to long-term climate and sea-level changes using 223 samples (~71,300 specimens) retrieved from latest Quaternary sediment cores of the Adriatic coastal systems. These cores provide a rare chance to study coastal systems that existed during glacial lowstands. The fossil mollusk record indicates that nearshore assemblages of the penultimate interglacial (Late Pleistocene) shifted in their faunal composition during the subsequent ice age, and then reassembled again with the return of interglacial climate in the Holocene. These shifts point to a climate-driven habitat filtering modulated by dispersal processes. The resilient, rather than persistent or stochastic, response of the mollusk assemblages to long-term environmental changes over at least 125 thousand years highlights the historically unprecedented nature of the ongoing anthropogenic stressors (e.g., pollution, eutrophication, bottom trawling, and invasive species) that are currently shifting coastal regions into novel system states far outside the range of natural variability archived in the fossil record.

A multiscale view of the Phanerozoic fossil record reveals the three major biotic transitions.

The hypothesis of the Great Evolutionary Faunas is a foundational concept of macroevolutionary research postulating that three global mega-assemblages have dominated Phanerozoic oceans following abrupt biotic transitions. Empirical estimates of this large-scale pattern depend on several methodological decisions and are based on approaches unable to capture multiscale dynamics of the underlying Earth-Life System. Combining a multilayer network representation of fossil data with a multilevel clustering that eliminates the subjectivity inherent to distance-based approaches, we demonstrate that Phanerozoic oceans sequentially harbored four global benthic mega-assemblages. Shifts in dominance patterns among these global marine mega-assemblages were abrupt (end-Cambrian 494 Ma; end-Permian 252 Ma) or protracted (mid-Cretaceous 129 Ma), and represent the three major biotic transitions in Earth's history. Our findings suggest that gradual ecological changes associated with the Mesozoic Marine Revolution triggered a protracted biotic transition comparable in magnitude to the end-Permian transition initiated by the most severe biotic crisis of the past 500 million years. Overall, our study supports the notion that both long-term ecological changes and major geological events have played crucial roles in shaping the mega-assemblages that dominated Phanerozoic oceans.

An asynchronous Mesozoic marine revolution: the Cenozoic intensification of predation on echinoids.

Predation traces found on fossilized prey remains can be used to quantify the evolutionary history of biotic interactions. Fossil mollusc shells bearing these types of traces provided key evidence for the rise of predation during the Mesozoic marine revolution (MMR), an event thought to have reorganized global marine ecosystems. However, predation pressure on prey groups other than molluscs has not been explored adequately. Consequently, the ubiquity, tempo and synchronicity of the MMR cannot be thoroughly assessed. Here, we expand the evolutionary record of biotic interactions by compiling and analysing a new comprehensively collected database on drilling predation in Meso-Cenozoic echinoids. Trends in drilling frequency reveal an Eocene rise in drilling predation that postdated echinoid infaunalization and the rise in mollusc-targeted drilling (an iconic MMR event) by approximately 100 Myr. The temporal lag between echinoid infaunalization and the rise in drilling frequencies suggests that the Eocene upsurge in predation did not elicit a coevolutionary or escalatory response. This is consistent with rarity of fossil samples that record high frequency of drilling predation and scarcity of fossil prey recording failed predation events. These results suggest that predation intensification associated with the MMR was asynchronous across marine invertebrate taxa and represented a long and complex process that consisted of multiple uncoordinated steps probably with variable coevolutionary responses.

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.

Seasonal oyster harvesting recorded in a Late Archaic period shell ring.

The function of Late Archaic period (5000-3000 B.P.) shell rings has been a focus of debate among archaeologists for decades. These rings have been variously interpreted as a product of seasonal feasting/ceremonial gatherings, quotidian food refuse generated by permanent dwellers, or a combination of seasonal and perennial activities. Seasonality of shell rings can be assessed by reconstructing the harvest time of oysters (Crassostrea virginica), the primary faunal component of shell rings. We estimated the timing of oyster harvest at St. Catherines Shell Ring (Georgia, USA) by statistical modeling of size frequency distributions of the impressed odostome (Boonea impressa), a parasitic snail inadvertently gathered by Archaic peoples with its oyster host. The odostome samples from three archaeological excavation units were evaluated against resampling models based on monthly demographic data obtained for present-day populations of Boonea impressa. For all samples, the harvest was unlikely to start earlier than late fall and end later than late spring, indicating that shell deposits at St. Catherines Shell Ring formed seasonally with substantial harvesting activities restricted to non-summer months. For all samples, the resampling models indicated that harvesting activities likely occurred during multiple months. However, these analytical outcomes would also be expected in the case of extensively time-averaged records of short-term, non-summer harvest events. Regardless of the exact harvest duration, the results point to seasonal harvesting and suggest that Archaic populations may have opted out of consuming summer oysters to focus on other resources, avoid unpalatable food, decrease pathogen risks, or ensure sustainable harvesting.

Long-term persistence of structured habitats: seagrass meadows as enduring hotspots of biodiversity and faunal stability.

Ecological studies indicate that structurally complex habitats support elevated biodiversity, stability and resilience. The long-term persistence of structured habitats and their importance in maintaining biodiverse hotspots remain underexplored. We combined geohistorical data (dead mollusc assemblages, 'DA') and contemporary surveys (live mollusc assemblages, 'LA') to assess the persistence of local seagrass habitats over multi-centennial timescales and to evaluate whether they acted as long-term drivers of biodiversity, stability and resilience of associated fauna. We sampled structured seagrass meadows and open sandy bottoms along Florida's Gulf Coast. Results indicated that: (i) LA composition differed significantly between the two habitat types, (ii) LA from seagrass sites were characterized by significantly elevated local biodiversity and significantly higher spatial stability, (iii) DA composition differed significantly between the two habitat types, and (iv) fidelity between LA and DA was significantly greater for seagrass habitats. Contemporary results support the hypotheses that local biodiversity and spatial stability of marine benthos are both elevated in structured seagrass habitats. Geohistorical results suggest that structured habitats persist as local hotspots of elevated biodiversity and faunal stability over centennial-to-millennial timescales; indicating that habitat degradation and concomitant loss within structurally complex marine systems is a key driver of declining biodiversity and resilience.

Stratigraphic signatures of mass extinctions: ecological and sedimentary determinants.

Stratigraphic patterns of last occurrences (LOs) of fossil taxa potentially fingerprint mass extinctions and delineate rates and geometries of those events. Although empirical studies of mass extinctions recognize that random sampling causes LOs to occur earlier than the time of extinction (Signor-Lipps effect), sequence stratigraphic controls on the position of LOs are rarely considered. By tracing stratigraphic ranges of extant mollusc species preserved in the Holocene succession of the Po coastal plain (Italy), we demonstrated that, if mass extinction took place today, complex but entirely false extinction patterns would be recorded regionally due to shifts in local community composition and non-random variation in the abundance of skeletal remains, both controlled by relative sea-level changes. Consequently, rather than following an apparent gradual pattern expected from the Signor-Lipps effect, LOs concentrated within intervals of stratigraphic condensation and strong facies shifts mimicking sudden extinction pulses. Methods assuming uniform recovery potential of fossils falsely supported stepwise extinction patterns among studied species and systematically underestimated their stratigraphic ranges. Such effects of stratigraphic architecture, co-produced by ecological, sedimentary and taphonomic processes, can easily confound interpretations of the timing, duration and selectivity of mass extinction events. Our results highlight the necessity of accounting for palaeoenvironmental and sequence stratigraphic context when inferring extinction dynamics from the fossil record.

Regional surveys of macrobenthic shelf invertebrate communities in Onslow Bay, North Carolina, U.S.A.

Despite its importance for quantifying ecosystem responses to environmental and anthropogenic drivers, our understanding of spatial heterogeneity in marine communities remains inadequate. Studies in coastal marine benthic habitats are sparse, and predominantly target single higher taxonomic groups. Here we describe macrobenthic marine invertebrate community surveys from 52 localities in Onslow Bay (Beaufort, North Carolina, U.S.A.), over an extensive geographic area (~200 km2). The data consist of 11,467 individuals, 175 species, and 7 phyla. The data include species abundance data for each sample at all localities, and corresponding species lists and locality information. The metadata describe the sampling protocols and localities. The data provided here will facilitate examination of assemblage heterogeneity with regards to spatial and temporal patterns, and depth gradient analyses.

Surges in trematode prevalence linked to centennial-scale flooding events in the Adriatic.

The forecasts of increasing global temperature and sea level rise have led to concern about the response of parasites to anthropogenic climate change. Whereas ecological studies of parasite response to environmental shifts are necessarily limited to short time scales, the fossil record can potentially provide a quantitative archive of long-term ecological responses to past climate transitions. Here, we document multi-centennial scale changes in prevalence of trematodes infesting the bivalve host Abra segmentum through multiple sea-level fluctuations preserved in brackish Holocene deposits of the Po Plain, Italy. Prevalence values were significantly elevated (p < 0.01) in samples associated with flooding surfaces, yet the temporal trends of parasite prevalence and host shell length, cannot be explained by Waltherian facies change, host availability, salinity, diversity, turnover, or community structure. The observed surges in parasite prevalence during past flooding events indicate that the ongoing global warming and sea-level rise will lead to significant intensification of trematode parasitism, suppressed fecundity of common benthic organisms, and negative impacts on marine ecosystems, ecosystem services, and, eventually, to human well-being.

Increase in predator-prey size ratios throughout the Phanerozoic history of marine ecosystems.

The escalation hypothesis posits that predation by increasingly powerful and metabolically active carnivores has been a major driver of metazoan evolution. We test a key tenet of this hypothesis by analyzing predatory drill holes in fossil marine shells, which provide a ~500-million-year record of individual predator-prey interactions. We show that drill-hole size is a robust predictor of body size among modern drilling predators and that drill-hole size (and thus inferred predator size and power) rose substantially from the Ordovician to the Quaternary period, whereas the size of drilled prey remained stable. Together, these trends indicate a directional increase in predator-prey size ratios. We hypothesize that increasing predator-prey size ratios reflect increases in prey abundance, prey nutrient content, and predation among predators.

Hierarchical complexity and the size limits of life.

Over the past 3.8 billion years, the maximum size of life has increased by approximately 18 orders of magnitude. Much of this increase is associated with two major evolutionary innovations: the evolution of eukaryotes from prokaryotic cells approximately 1.9 billion years ago (Ga), and multicellular life diversifying from unicellular ancestors approximately 0.6 Ga. However, the quantitative relationship between organismal size and structural complexity remains poorly documented. We assessed this relationship using a comprehensive dataset that includes organismal size and level of biological complexity for 11 172 extant genera. We find that the distributions of sizes within complexity levels are unimodal, whereas the aggregate distribution is multimodal. Moreover, both the mean size and the range of size occupied increases with each additional level of complexity. Increases in size range are non-symmetric: the maximum organismal size increases more than the minimum. The majority of the observed increase in organismal size over the history of life on the Earth is accounted for by two discrete jumps in complexity rather than evolutionary trends within levels of complexity. Our results provide quantitative support for an evolutionary expansion away from a minimal size constraint and suggest a fundamental rescaling of the constraints on minimal and maximal size as biological complexity increases.

Surrogate taxa and fossils as reliable proxies of spatial biodiversity patterns in marine benthic communities.

Rigorous documentation of spatial heterogeneity (ß-diversity) in present-day and preindustrial ecosystems is required to assess how marine communities respond to environmental and anthropogenic drivers. However, the overwhelming majority of contemporary and palaeontological assessments have centred on single higher taxa. To evaluate the validity of single taxa as community surrogates and palaeontological proxies, we compared macrobenthic communities and sympatric death assemblages at 52 localities in Onslow Bay (NC, USA). Compositional heterogeneity did not differ significantly across datasets based on live molluscs, live non-molluscs, and all live organisms. Death assemblages were less heterogeneous spatially, likely reflecting homogenization by time-averaging. Nevertheless, live and dead datasets were greater than 80% congruent in pairwise comparisons to the literature estimates of ß-diversity in other marine ecosystems, yielded concordant bathymetric gradients, and produced nearly identical ordinations consistently delineating habitats. Congruent estimates from molluscs and non-molluscs suggest that single groups can serve as reliable community proxies. High spatial fidelity of death assemblages supports the emerging paradigm of Conservation Palaeobiology. Integrated analyses of ecological and palaeontological data based on surrogate taxa can quantify anthropogenic changes in marine ecosystems and advance our understanding of spatial and temporal aspects of biodiversity.

Understanding modern extinctions in marine ecosystems: the role of palaeoecological data.

Because anthropogenic impacts on ecological systems pre-date the oldest scientific observations, historical documents and archaeological records, understanding modern extinctions requires additional data sources that extend further back in time. Palaeoecological records, which provide quantitative proxy records of ecosystems prior to human impact, are essential for understanding recent extinctions and future extinction risks. Here we critically review the value of the most recent fossil record in contributing to our understanding of modern extinctions and illustrate through case studies how naturally occurring death assemblages and Holocene sedimentary records provide context to the plight of marine ecosystems. While palaeoecological data are inherently restricted censuses of past communities (manipulative experiments are not possible), they yield quantitative records over temporal scales that are beyond the reach of ecology. Only by including palaeoecological data is it possible to fully assess the role of long-term anthropogenic processes in driving modern extinction risk.

Environmental and scale-dependent evolutionary trends in the body size of crustaceans.

The ecological and physiological significance of body size is well recognized. However, key macroevolutionary questions regarding the dependency of body size trends on the taxonomic scale of analysis and the role of environment in controlling long-term evolution of body size are largely unknown. Here, we evaluate these issues for decapod crustaceans, a group that diversified in the Mesozoic. A compilation of body size data for 792 brachyuran crab and lobster species reveals that their maximum, mean and median body size increased, but no increase in minimum size was observed. This increase is not expressed within lineages, but is rather a product of the appearance and/or diversification of new clades of larger, primarily burrowing to shelter-seeking decapods. This argues against directional selective pressures within lineages. Rather, the trend is a macroevolutionary consequence of species sorting: preferential origination of new decapod clades with intrinsically larger body sizes. Furthermore, body size evolution appears to have been habitat-controlled. In the Cretaceous, reef-associated crabs became markedly smaller than those in other habitats, a pattern that persists today. The long-term increase in body size of crabs and lobsters, coupled with their increased diversity and abundance, suggests that their ecological impact may have increased over evolutionary time.

Differential responses of marine communities to natural and anthropogenic changes.

Responses of ecosystems to environmental changes vary greatly across habitats, organisms and observational scales. The Quaternary fossil record of the Po Basin demonstrates that marine communities of the northern Adriatic re-emerged unchanged following the most recent glaciation, which lasted approximately 100,000 years. The Late Pleistocene and Holocene interglacial ecosystems were both dominated by the same species, species turnover rates approximated predictions of resampling models of a homogeneous system, and comparable bathymetric gradients in species composition, sample-level diversity, dominance and specimen abundance were observed in both time intervals. The interglacial Adriatic ecosystems appear to have been impervious to natural climate change either owing to their persistence during those long-term perturbations or their resilient recovery during interglacial phases of climate oscillations. By contrast, present-day communities of the northern Adriatic differ notably from their Holocene counterparts. The recent ecosystem shift stands in contrast to the long-term endurance of interglacial communities in face of climate-driven environmental changes.

Growth, inter- and intraspecific variation, palaeobiogeography, taphonomy and systematics of the Cenozoic ghost shrimp Glypturus.

Studies in systematic palaeontology are greatly aided when numerous, well-preserved specimens are available so that quantitative methods can be used to substantiate qualitative observations. This is often not the case for fossil decapod crustaceans due to their relatively low preservation potential. Here, we examined primarily two large collections of the well-preserved ghost shrimp Glypturus from the Holo-Pleistocene of Panama and the late Miocene of Florida. Using descriptive, bivariate, multivariate and geometric morphometric methods, two new species are described based on appendage material: Glypturus panamacanalensis sp. nov. and G. sikesi sp. nov. New characters are identified, and size-related and intraspecific variation are assessed for these taxa and modern G. acanthochirus. Taxonomic placement of single specimens from other localities was confirmed by multivariate methods. Furthermore, Glypturus is revised, especially with regard to Western Atlantic species that inhabited both carbonate and siliciclastic environments. Callianassa anguillensis, C. latidigata, and Neocallichirus? quisquellanus are referred to as Glypturus sp. until more material is available to determine the validity of these species. Diversity within Glypturus may thus be underestimated, thereby also impacting the assessment of phylogenetic relationships. Minor propodi appear under-represented relative to major propodi, suggesting a taphonomic bias. Single specimens of interest include a specimen of G. panamacanalensis sp. nov. exhibiting a peculiar swelling in the fixed finger and another showing damage on the propodal upper margin, suggesting failed predation or antagonistic behaviour. Glypturus is first found in the Oligocene in the Western Atlantic and may have expanded its palaeobiogeographical range since the Miocene. The genus was still present on the Pacific side of the Isthmus of Panama in the Holo-Pleistocene, but is only known from the Western Atlantic today, suggesting a relatively recent extinction on the Pacific side.

Utility of marine benthic associations as a multivariate proxy of paleobathymetry: a direct test from recent coastal ecosystems of North Carolina.

Benthic marine fossil associations have been used in paleontological studies as multivariate environmental proxies, with particular focus on their utility as water depth estimators. To test this approach directly, we evaluated modern marine invertebrate communities along an onshore-offshore gradient to determine the relationship between community composition and bathymetry, compare the performance of various ordination techniques, and assess whether restricting community datasets to preservable taxa (a proxy for paleontological data) and finer spatial scales diminishes the applicability of multivariate community data as an environmental proxy. Different indirect (unconstrained) ordination techniques (PCoA, CA, DCA, and NMDS) yielded consistent outcomes: locality Axis 1 scores correlated with actual locality depths, and taxon Axis 1 scores correlated with actual preferred taxon depths, indicating that changes in faunal associations primarily reflect bathymetry, or its environmental correlatives. For datasets restricted to taxa with preservable hard parts, heavily biomineralized mollusks, open ocean habitats, and a single onshore-offshore gradient, the significant correlation between water depth and Axis 1 was still observed. However, for these restricted datasets, the correlation between Axis 1 and bathymetry was reduced and, in most cases, notably weaker than estimates produced by subsampling models. Consistent with multiple paleontological studies, the direct tests carried out here for a modern habitat using known bathymetry suggests that multivariate proxies derived from marine benthic associations may serve as a viable proxy of water depth. The general applicability of multivariate paleocommunity data as an indirect proxy of bathymetry is dependent on habitat type, intrinsic ecological characteristics of dominant faunas, taxonomic scope, and spatial and temporal scales of analysis, highlighting the need for continued testing in present-day depositional settings.