TRACING ORIGIN AND COLLAPSE OF HOLOCENE BENTHIC BASELINE COMMUNITIES IN THE NORTHERN ADRIATIC SEA

The shallow northern Adriatic Sea has a long history of anthropogenic impacts that reaches back many centuries. While the effects of eutrophication, overfishing, pollution, and trawling over recent decades have been extensively studied, the major ecological turnovers during the Holocene as a whole remain poorly explored. In this study, we reconstruct ecological baselines defining benthic ecosystem composition prior to major anthropogenic changes at four stations characterized by low sedimentation and millennial-scale time averaging of molluscan assemblages. We discriminate between natural and anthropogenic drivers based on (1) stratigraphic changes in the composition of molluscan communities observed in sediment cores and (2) changes in concentrations of heavy metals, pollutants, and organic enrichment. The four 1.5-m long sediment cores reach back to the Pleistocene–Holocene boundary, allowing for a stratigraphic distinction of the major sea-level phases of the Holocene. During the transgressive phase and maximum flooding, sea-level and establishment of the modern circulation pattern determined the development of benthic communities in shallow-water, vegetated habitats with epifaunal biostromes and, in deeper waters, with bryozoan meadows. After sea-level stabilization, the composition of these baseline communities remained relatively uniform and started to change markedly only with the intensification of human impacts in the late highstand, leading to a dominance of infauna and a decline of epifauna at all sites. This profound ecological change reduced species richness, increased the abundance of infaunal suspension feeders, and led to a decline of grazers and deposit feeders. We suggest that modern soft-bottom benthic communities in the northern Adriatic Sea today do not show the high geographic heterogeneity in composition characteristic of benthos prior to anthropogenic influences

Supplement Table 3-Corbula age data

Amino acid racemization data and calibrated estimates of postmortem age of Corbula gibba and Piran 2

Supplement Table 2-Gouldia age data

Amino acid racemization data and calibrated estimates of postmortem age of Gouldia minima collected from the shell bed at Piran 1 and Piran 2

Data from: 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 NE 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 (1) monitoring of ecosystems prior to the 20th century was scarce and (2) 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 > 1,000 years and C. gibba shells are older by >2,000 years than shells of co-occurring G. minima. This age difference is driven by temporally disjunct production of two species coupled with decimeter-scale mixing. Stratigraphic unmixing shows that Corbula gibba declined in abundance during the highstand phase and increased again in 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. G. minima and herbivorous gastropods associated with macroalgae or seagrasses are abundant in the top-core increments but are rare alive. Although G. 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 seafloor in the Gulf of Trieste reflect inactive production that was sourced by heterozoan carbonate factory in algal or seagrass habitats

Supplementary Table 2

Supplementary Table 2 – Amino acid racemization and calibrated age data of Corbula gibba from two Po stations (analyzed in this paper), from the Bay of Panzano (Tomasovych et al. 2017, Geology, and analyzed this paper), and from Piran (Mautner et al. 2018, Marine Pollution Bulletin)

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

<div><p>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 16^th and 19^th 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 20^th 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 <i>Corbula gibba</i> and the scavenging gastropod <i>Nassarius pygmaeus</i> significantly increase in abundance during the 20^th century, while species more sensitive to disturbances and hypoxia such as <i>Turritella communis</i> and <i>Kurtiella bidentata</i> become rare or absent. An infaunal life habit and scavenging emerge as the dominant life strategies during the late 20^th 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.</p></div

Data from: Tracing the effects of eutrophication on molluscan communities in sediment cores: outbreaks of an opportunistic species coincide with reduced bioturbation and high frequency of hypoxia in the Adriatic Sea

Estimating the effects and timing of anthropogenic impacts on the composition of macrobenthic communities is challenging because early 20th century surveys are sparse and the corresponding intervals in sedimentary sequences are mixed by bioturbation. Here, to assess the effects of eutrophication on macrobenthic communities in the northern Adriatic Sea, we account for mixing with dating of the bivalve Corbula gibba at two stations with high sediment accumulation (Po prodelta) and one station with moderate accumulation (Isonzo prodelta). We find that, first, pervasively bioturbated muds typical of highstand conditions deposited in the early 20th century were replaced by muds with relicts of flood layers and high content of total organic carbon (TOC) deposited in the late 20th century at the Po prodelta. The 20th century shelly muds at the Isonzo prodelta are amalgamated but also show an upward increase in TOC. Second, dating of C. gibba shells shows that the shift from the early to the late 20th century is characterized by a decrease in stratigraphic disorder and by an increase in temporal resolution of death assemblages from ~25-50 years to ~10-20 years in both regions. This shift reflects a decline in the depth of the fully-mixed layer from more than 20 cm to few centimeters. Third, the increase in abundance of the opportunistic species C. gibba and the loss of formerly abundant, hypoxia-sensitive species coincided with the decline in bioturbation, higher preservation of organic matter, and higher frequency of seasonal hypoxia in both regions. This depositional and ecosystem regime shift occurred in ~1950 AD. Therefore, the effects of enhanced food supply on macrobenthic communities were overwhelmed by oxygen depletion even when hypoxic conditions are limited to few weeks per year in the northern Adriatic Sea. Preservation of trends in molluscan abundance and flood events in sedimentary sequences was enhanced by eutrophication that reduced bioturbational mixing

Supplement Table 1-core data

Absolute abundances of molluscs in two cores at Piran 1 and Piran 2, including two surface living assemblages collected by Van Veen grabs at the same sites in 2014 (1 mm mesh size). Complete valves or fragments with umbo preserved were selected from the >1 mm sieve fraction of each increment, identified to species level, and counted. For each species, the higher number of single valves (either right or left) was added to the number of double-valved specimens to get the final count in each increment

Redundancy analysis for down-core community changes in relation to environmental variables.

<p>Total nitrogen separates the topmost core intervals from the rest of the core and explains a significant amount of variation in relative abundance of species (A), feeding guilds (B), organism-substrate relations (C), and host associations (D). The second axis represent the first principal component in A-C because the stepwise selection selected one environmental variable only.</p

Supplementary code

R language source code for age unmixing procedure and for reproduction of some plots and analyses underlying the manuscript.The excel file "Supplementary Table 2" should be saved as tab-delimited txt file. This file is uploaded by the script