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.

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.

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.

An innovative piston corer for large-volume sediment samples.

Coring is one of several standard procedures to extract sediments and their faunas from open marine, estuarine, and limnic environments. Achieving sufficiently deep penetration, obtaining large sediment volumes in single deployments, and avoiding sediment loss upon retrieval remain problematic. We developed a piston corer with a diameter of 16 cm that enables penetration down to 1.5 m in a broad range of soft bottom types, yields sufficient material for multiple analyses, and prevents sediment loss due to a specially designed hydraulic core catcher. A novel extrusion system enables very precise slicing and preserves the original sediment stratification by keeping the liners upright. The corer has moderate purchase costs and a robust and simple design that allows for a deployment from relatively small vessels as available at most marine science institutions. It can easily be operated by two to three researchers rather than by specially trained technicians. In the northern Adriatic Sea, the corer successfully extracted more than 50 cores from a range of fine mud to coarse sand, at water depths from three to 45 m. The initial evaluation of the cores demonstrated their usefulness for fauna sequences along with heavy metal, nutrient and pollutant analyses. Their length is particularly suited for historical ecological work requiring sedimentary and faunal sequences to reconstruct benthic communities over the last millennia.