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.

Human-driven breakdown of predator-prey interactions in the northern Adriatic Sea.

Long-term baseline data that allow tracking how predator-prey interactions have responded to intensifying human impacts are often lacking. Here, we assess temporal changes in benthic community composition and interactions between drilling predatory gastropods and their molluscan prey using the Holocene fossil record of the shallow northern Adriatic Sea, which is characterized by a long history of human transformation. Molluscan assemblages differ between the Isonzo and Po prodelta, but both show consistent temporal trends in the abundance of dominant species. Samples of mollusc prey collected at high stratigraphic resolution indicate that drilling frequencies have drastically declined in the Po prodelta since the mid-twentieth century, while a weaker trend in the more condensed sediments of the Isonzo prodelta is not statistically significant. The decrease in drilling predation intensity and the community turnover are linked to the loss of predatory gastropods and the increased relative abundance of less-preferred prey during the most recent decades. Our results align with data showing the substantial depletion of marine resources at higher trophic levels in the region and indicate that the strong simplification of the food web initiated in the late nineteenth century accelerated further since the mid-twentieth century.

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.

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.

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.

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.

Parasitism and host behavior in the context of a changing environment: The Holocene record of the commercially important bivalve Chamelea gallina, northern Italy.

Rapid warming and sea-level rise are predicted to be major driving forces in shaping coastal ecosystems and their services in the next century. Though forecasts of the multiple and complex effects of temperature and sea-level rise on ecological interactions suggest negative impacts on parasite diversity, the effect of long term climate change on parasite dynamics is complex and unresolved. Digenean trematodes are complex life cycle parasites that can induce characteristic traces on their bivalve hosts and hold potential to infer parasite host-dynamics through time and space. Previous work has demonstrated a consistent association between sea level rise and increasing prevalence of trematode traces, but a number of fundamental questions remain unanswered about this paleoecological proxy. Here we examine the relationships of host size, shape, and functional morphology with parasite prevalence and abundance, how parasites are distributed across hosts, and how all of these relationships vary through time, using the bivalve Chamelea gallina from a Holocene shallow marine succession in the Po coastal plain. Trematode prevalence increased and decreased in association with the transition from a wave-influenced estuarine system to a wave-dominated deltaic setting. Prevalence and abundance of trematode pits are associated with large host body size, reflecting ontogenetic accumulation of parasites, but temporal trends in median host size do not explain prevalence trends. Ongoing work will test the roles of temperature, salinity, and nutrient availability on trematode parasitism. Parasitized bivalves in one sample were shallower burrowers than their non-parasitized counterparts, suggesting that hosts of trematodes can be more susceptible to their predators, though the effect is ephemeral. Like in living parasite-host systems, trematode-induced malformations are strongly aggregated among hosts, wherein most host individuals harbor very few parasites while a few hosts have many. We interpret trace aggregation to support the assumption that traces are a reliable proxy for trematode parasitism in the fossil record.

Phanerozoic parasitism and marine metazoan diversity: dilution versus amplification.

Growing evidence suggests that biodiversity mediates parasite prevalence. We have compiled the first global database on occurrences and prevalence of marine parasitism throughout the Phanerozoic and assess the relationship with biodiversity to test if there is support for amplification or dilution of parasitism at the macroevolutionary scale. Median prevalence values by era are 5% for the Paleozoic, 4% for the Mesozoic, and a significant increase to 10% for the Cenozoic. We calculated period-level shareholder quorum sub-sampled (SQS) estimates of mean sampled diversity, three-timer (3T) origination rates, and 3T extinction rates for the most abundant host clades in the Paleobiology Database to compare to both occurrences of parasitism and the more informative parasite prevalence values. Generalized linear models (GLMs) of parasite occurrences and SQS diversity measures support both the amplification (all taxa pooled, crinoids and blastoids, and molluscs) and dilution hypotheses (arthropods, cnidarians, and bivalves). GLMs of prevalence and SQS diversity measures support the amplification hypothesis (all taxa pooled and molluscs). Though likely scale-dependent, parasitism has increased through the Phanerozoic and clear patterns primarily support the amplification of parasitism with biodiversity in the history of life. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Climate variation during the Holocene influenced the skeletal properties of Chamelea gallina shells in the North Adriatic Sea (Italy).

Understanding how marine taxa will respond to near-future climate changes is one of the main challenges for management of coastal ecosystem services. Ecological studies that investigate relationships between the environment and shell properties of commercially important marine species are commonly restricted to latitudinal gradients or small-scale laboratory experiments. This paper aimed to explore the variations in shell features and growth of the edible bivalve Chamelea gallina from the Holocene sedimentary succession to present-day thanatocoenosis of the Po Plain-Adriatic Sea system (Italy). Comparing the Holocene sub-fossil record to modern thanatocoenoses allowed obtaining an insight of shell variations dynamics on a millennial temporal scale. Five shoreface-related assemblages rich in C. gallina were considered: two from the Middle Holocene, when regional sea surface temperatures were higher than today, representing a possible analogue for the near-future global warming, one from the Late Holocene and two from the present-day. We investigated shell biometry and skeletal properties in relation to the valve length of C. gallina. Juveniles were found to be more porous than adults in all horizons. This suggested that C. gallina promoted an accelerated shell accretion with a higher porosity and lower density at the expense of mechanically fragile shells. A positive correlation between sea surface temperature and both micro-density and bulk density were found, with modern specimens being less dense, likely due to lower aragonite saturation state at lower temperature, which could ultimately increase the energetic costs of shell formation. Since no variation was observed in shell CaCO3 polymorphism (100% aragonite) or in compositional parameters among the analyzed horizons, the observed dynamics in skeletal parameters are likely not driven by a diagenetic recrystallization of the shell mineral phase. This study contributes to understand the response of C. gallina to climate-driven environmental shifts and offers insights for assessing anthropogenic impacts on this economic relevant species.

Unveiling an odd fate after death: The isolated Eneolithic cranium discovered in the Marcel Loubens Cave (Bologna, Northern Italy).

An isolated human cranium, dated to the early Eneolithic period, was discovered in 2015 at the top of a vertical shaft in the natural Marcel Loubens gypsum Cave (Bologna area, northern Italy). No other anthropological or archaeological remains were found inside the cave. In other caves of the same area anthropic and funerary use are attested from prehistory to more recent periods. We focused on investigating the circumstances surrounding the death of this individual, since the cranium shows signs of some lesions that appear to be the results of a perimortem manipulation probably carried out to remove soft tissues. Anthropological analyses revealed that the cranium belonged to a young woman. We analysed the taphonomic features and geological context to understand how and why the cranium ended up (accidentally or intentionally) in the cave. The analyses of both the sediments accumulated inside the cranium and the incrustations and pigmentation covering its outer surface suggested that it fell into the cave, drawn by a flow of water and mud, likely from the edges of a doline. The accidental nature of the event is also seemingly confirmed by some post-mortem lesions on the cranium. The comparison with other Eneolithic archaeological sites in northern Italy made it possible to interpret the find as likely being from a funerary or ritual context, in which corpse dismemberment (in particular the displacement of crania) was practiced.

Environmental influence on calcification of the bivalve Chamelea gallina along a latitudinal gradient in the Adriatic Sea.

Environmental factors are encoded in shells of marine bivalves in the form of geochemical properties, shell microstructure and shell growth rate. Few studies have investigated how shell growth is affected by habitat conditions in natural populations of the commercial clam Chamelea gallina. Here, skeletal parameters (micro-density and apparent porosity) and growth parameters (bulk density, linear extension and net calcification rates) were investigated in relation to shell sizes and environmental parameters along a latitudinal gradient in the Adriatic Sea (400 km). Net calcification rates increased with increasing solar radiation, sea surface temperature and salinity and decreasing Chlorophyll concentration in immature and mature shells. In immature shells, which are generally more porous than mature shells, enhanced calcification was due to an increase in bulk density, while in mature shells was due to an increase in linear extension rates. The presence of the Po river in the Northern Adriatic Sea was likely the main driver of the fluctuations observed in environmental parameters, especially salinity and Chlorophyll concentration, and seemed to negatively affect the growth of C. gallina.

Early-Middle Pleistocene benthic turnover and oxygen isotope stratigraphy from the Central Mediterranean (Valle di Manche, Crotone Basin, Italy): Data and trends.

Ostracod faunal turnover and oxygen isotope data (foraminifera) along the Valle di Manche (VdM) section are herein compiled. Specifically, the material reported in this work includes quantitative palaeoecological data and patterns of ostracod fauna framed within a high-resolution oxygen isotope stratigraphy (δ18O) from Uvigerina peregrina. In addition, the multivariate ostracod faunal stratigraphic trend (nMDS axis-1 sample score) is calibrated using bathymetric distributions of extant molluscs sampled from the same stratigraphic intervals along the VdM section. Data and analyses support the research article "Dynamics of benthic marine communities across the Early-Middle Pleistocene boundary in the Mediterranean region (Valle di Manche, Southern Italy): biotic and stratigraphic implications" Rossi et al. [1].

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.