The FORCIS database: A global census of planktonic Foraminifera from ocean waters.

Planktonic Foraminifera are unique paleo-environmental indicators through their excellent fossil record in ocean sediments. Their distribution and diversity are affected by different environmental factors including anthropogenically forced ocean and climate change. Until now, historical changes in their distribution have not been fully assessed at the global scale. Here we present the FORCIS (Foraminifera Response to Climatic Stress) database on foraminiferal species diversity and distribution in the global ocean from 1910 until 2018 including published and unpublished data. The FORCIS database includes data collected using plankton tows, continuous plankton recorder, sediment traps and plankton pump, and contains ~22,000, ~157,000, ~9,000, ~400 subsamples, respectively (one single plankton aliquot collected within a depth range, time interval, size fraction range, at a single location) from each category. Our database provides a perspective of the distribution patterns of planktonic Foraminifera in the global ocean on large spatial (regional to basin scale, and at the vertical scale), and temporal (seasonal to interdecadal) scales over the past century.

The combined effects of rising temperature and salinity may halt the future proliferation of symbiont-bearing foraminifera as ecosystem engineers.

Rising sea surface temperatures and extreme heat waves are affecting symbiont-bearing tropical calcifiers such as corals and Large Benthic Foraminifera (LBF). In many ecosystems, parallel to warming, global change unleashes a host of additional changes to the marine environment, and the combined effect of such multiple stressors may be far greater than those of temperature alone. One such additional stressor, positively correlated to temperature in evaporation-dominated shallow-water settings is rising salinity. Here we used laboratory culture experiments to evaluate the combined thermohaline tolerance of one of the most common LBF species and carbonate producer, Amphistegina lobifera. The experiments were done under ambient (39 psu) and modified (30, 45, 50 psu) salinities and at optimum (25 °C) and warm temperatures (32 °C). Calcification of the A. lobifera holobiont was evaluated by measuring alkalinity loss in the culturing seawater, as an indication of carbonate ion uptake. The vitality of the symbionts was determined by monitoring pigment loss of the holobiont and their photosynthetic performances by measuring dissolved oxygen. We further evaluated the growth of Peneroplis (P. pertusus and P. planatus), a Rhodophyta bearing LBF, which is known to tolerate high temperatures, under elevated salinities. The results show that the A. lobifera holobiont exhibits optimal performance at 39 psu and 25 °C, and its growth is significantly reduced upon exposure to 30, 45, 50 psu and under all 32 °C treatments. Salinity and temperature exhibit a significant interaction, with synergic effects observed in most treatments. Our results confirm that Peneroplis has a higher tolerance to elevated temperature and salinity compared to A. lobifera, implying that a further increase of salinity and temperatures may result in a regime shift from Amphistegina- to Peneroplis-dominated assemblages.

Relative abundances of benthic foraminifera in response to total organic carbon in sediments: Data from European intertidal areas and transitional waters.

We gathered total organic carbon (%) and relative abundances of benthic foraminifera in intertidal areas and transitional waters from the English Channel/European Atlantic Coast (587 samples) and the Mediterranean Sea (301 samples) regions from published and unpublished datasets. This database allowed to calculate total organic carbon optimum and tolerance range of benthic foraminifera in order to assign them to ecological groups of sensitivity. Optima and tolerance range were obtained by mean of the weighted-averaging method. The data are related to the research article titled "Indicative value of benthic foraminifera for biomonitoring: assignment to ecological groups of sensitivity to total organic carbon of species from European intertidal areas and transitional waters" [1].

Indicative value of benthic foraminifera for biomonitoring: Assignment to ecological groups of sensitivity to total organic carbon of species from European intertidal areas and transitional waters.

This work contributes to the ongoing work aiming at confirming benthic foraminifera as a biological quality element. In this study, benthic foraminifera from intertidal and transitional waters from the English Channel/European Atlantic coast and the Mediterranean Sea were assigned to five ecological groups using the weighted-averaging optimum with respect to TOC of each species. It was however not possible to assign typical salt marsh species due to the presence of labile and refractory organic matter that hampers TOC characterization. Tests of this study species' lists with Foram-AMBI on two independent datasets showed a significant correlation between Foram-AMBI and TOC, confirming the strong relation between foraminifera and TOC. For one of the validation datasets, associated macrofaunal data were available and a significant correlation was found between the foraminiferal Foram-AMBI and the macrofaunal AMBI. The here proposed lists should be further tested with sensitivity-based indices in different European regional settings.

Epiphytic benthic foraminiferal preferences for macroalgal habitats: Implications for coastal warming.

Considering the thermal limits of coastal macroalgae habitats in the South-Eastern Mediterranean, it is important to study the response of the associated meiofauna to better understand the expected feedback of ecosystems to future warming. In this study, we compared benthic foraminiferal assemblages from two common macroalgal habitats, Turf and Coralline algae, based on ecological monitoring of a thermally polluted station representing near future warming, and an undisturbed environment. None of the common local species is confined to a specific algal habitat. This implies that their existence is not threatened by the disappearance of the Coralline algae. However, most likely their community structure will be impacted with coastal warming. Species that are more affiliated with Coralline algae are highly thermally tolerant, thus their proliferation might be reduced with warming. Specifically, the negative response of Coralline algae to warming may limit the contribution of invasive species such as Pararotalia calcariformata.

Thermal tolerance and range expansion of invasive foraminifera under climate changes.

The Eastern Mediterranean is experiencing a large-scale invasion of alien tropical species from the Red Sea. This "Lessepsian invasion" began with the opening of the Suez Canal and is promoted by the ongoing oceanic warming. The environmental differences between the Red Sea and the Mediterranean act as a buffer allowing the invasion of certain species. This provides an opportunity to study the differences in temperature sensitivity between two sibling species of the cosmopolitian foraminifera Amphistegina. Both species are very common in the Red Sea. Whilest, only one is a successful invader and the other is absent in the Eastern Mediterranean. Here we show that the two species are different in their temperature sensitivity, which explains their selective invasion into the Mediterranean. These differences demonstrate that in respect to climate change resilient marine species can be distinguished by their ability to compensate for temperature changes by adjusting their physiological performance and by having tolerance to a wider temperature range. Moreover, we demonstrate that selective filtering mechanisms during invasion can prefer species that are more resilient to colder rather than expected warmer temperatures.

Evidence for a humid interval at ∼56-44 ka in the Levant and its potential link to modern humans dispersal out of Africa.

This study provides a detailed reconstruction of the paleoenvironmental conditions that prevailed during one of the periods of modern human migration out of Africa and their occupation of the Eastern Mediterranean-Levant during the Late Middle Paleolithic-Early Upper Paleolithic. Tracing the past vegetation and climate within the Eastern Mediterranean-Levant region is largely based on a south-eastern Mediterranean marine pollen record covering the last 90 kyr (core MD-9509). The various palynomorphs were linked to distinct vegetation zones that were correlated to the two climate systems affecting the study area: the low-latitude monsoon system and the North Atlantic-Mediterranean climate system. The bioprovince palynological markers show that during the period between ∼56 and 44 ka, which covers the early part of Marine Isotope Stage 3 (MIS 3), there was an increase in transportation of pollen from Nilotic origin and a rise in dinoflagellate cyst ratios. These changes coincided with maximum insolation values at 65°N, which led to an enhancement in Nile River discharge into the Eastern Mediterranean following the intensification of the African monsoonal system. At the same time, the rise in Mediterranean arboreal pollen values (broadleaved, coniferous and deciduous temperate trees) is most likely driven by increased precipitation related to the intensification of the North Atlantic-Mediterranean climate system. The ∼56-44 ka wet event coincides with Dansgaard-Oeschger interstadials 14 and 12 and with a warming phase in the Levant, as evidenced by the melting of permafrost along the higher elevations of Mount Hermon. We suggest that African modern humans were able to cross the harsher arid areas due to the intensification of the monsoonal system during the first part of MIS 3, and inhabit the Eastern Mediterranean-Levant region where climatic conditions were favorable (wetter and warmer), even in the currently semiarid/steppe regions.

Author Correction: Depth related adaptations in symbiont bearing benthic foraminifera: New insights from a field experiment on Operculina ammonoides.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Depth related adaptations in symbiont bearing benthic foraminifera: New insights from a field experiment on Operculina ammonoides.

Large benthic foraminifera (LBF) are marine calcifying protists that commonly harbor algae as symbionts. These organisms are major calcium carbonate producers and important contributors to primary production in the photic zones. Light is one of the main known factors limiting their distribution, and species of this group developed specific mechanisms that allow them to occupy different habitats across the light gradient. Operculina ammonoides (Gronovius, 1781) is a planispiral LBF that has two main shell morphotypes, thick involute and flat evolute. Earlier studies suggested morphologic changes with variation in water depth and presumably light. In this study, specimens of the two morphotypes were placed in the laboratory under artificial low light and near the sea floor at depths of 15 m, 30 m, and 45 m in the Gulf of Aqaba-Eilat for 23 days. Differences in growth and symbionts content were evaluated using weight, size, and chlorophyll a. Our results show that O. ammonoides exhibit morphological plasticity when constructing thinner chambers after relocation to low light conditions, and adding more weight per area after relocation to high light conditions. In addition, O. ammonoides exhibited chlorophyll content adaptation to a certain range of light conditions, and evolute specimens that were acclimatized to very low light did not survive relocation to a high light environment, possibly due to photo-oxidative stress.

Foraminiferal single chamber analyses of heavy metals as a tool for monitoring permanent and short term anthropogenic footprints.

In order to establish environmentally sustainable industries there is a need for high-resolution temporal and spatial monitoring of heavy metal pollutants even at low concentrations before they become hazardous for local ecosystems. Here we present single chamber records of Cu, Zn and Pb in shells of two benthic foraminifera species with different shell types from two shallow coastal stations in Israel: An area adjacent to an electrical power plant and desalination factory (Hadera) and an industrially free nature reserve (Nachsholim). Records of both foraminifera species show elevated metal concentrations in Hadera clearly identifying the footprint of the local industrial facilities. Moreover, short-term events of elevated Cu and Pb concentrations were detected by single chamber analyses. This study demonstrates the potential of using heavy metals anomalies in foraminiferal single chambers as a tool for detecting the industrial footprint of coastal facilities as well as short term events of elevated heavy metals.

Geochemical signatures of benthic foraminiferal shells from a heat-polluted shallow marine environment provide field evidence for growth and calcification under extreme warmth.

Shallow marine calcifiers play an important role as marine ecosystem engineers and in the global carbon cycle. Understanding their response to warming is essential to evaluate the fate of marine ecosystems under global change scenarios. A rare opportunity to test the effect of warming acting on natural ecosystems is by investigation of heat-polluted areas. Here, we study growth and calcification in benthic foraminifera that inhabit a thermally polluted coastal area in Israel, where they are exposed to elevated temperatures reaching up to ~42°C in summer. Live specimens of two known heat-tolerant species Lachlanella sp. 1 and Pararotalia calcariformata were collected over a period of 1 year from two stations, representing thermally polluted and undisturbed (control) shallow hard bottom habitats. Single-chamber element ratios of these specimens were obtained using laser ablation, and the Mg/Ca of the most recently grown final chambers were used to calculate their calcification temperatures. Our results provide the first direct field evidence that these foraminifera species not only persist at extreme warm temperatures but continue to calcify and grow. Species-specific Mg/Ca thermometry indicates that P. calcariformata precipitate their shells at temperatures as high as 40°C and Lachlanella sp. 1 at least up to 36°C, but both species show a threshold for calcification at cold temperatures: calcification in P. calcariformata only occurred above 22°C and in Lachlanella sp. 1 above 15°C. Our observations from the heat-polluted area indicate that under future warming scenarios, calcification in heat-tolerant foraminifera species will not be inhibited during summer, but instead the temperature window for their calcification will be expanded throughout much of the year. The observed inhibition of calcification at low temperatures indicates that the role of heat-tolerant foraminifera in carbonate production will most likely increase in future decades.

Temporal trends in live foraminiferal assemblages near a pollution outfall on the Levant shelf.

Long and short term effects of activated sewage sludge input on live benthic foraminiferal assemblages of the shallow shelf off Palmachim, Israel were examined at three stations along the eutrophic gradient. Over ten years from 2003 to 2012, foraminiferal abundance decreased dramatically by >50% in all stations. In 2012, new species were found near the discharge point, relative abundance of the dominant species decreased and in-sediment depth increased. In the remote stations the dominant species failed to bloom seasonally. Each year, dispersion of sludge was accompanied by intense current activity, aeration, and periodic local sediment transport, reintroducing species from nearby. Storm frequency was notably high in 2012. The decrease in numbers over time despite seasonal amelioration indicates that the constant OM input is a permanent source of environmental stress. Aside from this stress, natural variability, changes in Nile input, or a hidden impact of long-term climate change may play a role.

Selective responses of benthic foraminifera to thermal pollution.

Persistent thermohaline pollution at a site along the northern coast of Israel, due to power and desalination plants, is used as a natural laboratory to evaluate the effects of rising temperature and salinity levels on benthic foraminifera living in shallow hard-bottom habitats. Biomonitoring of the disturbed area and a control station shows that elevated temperature is a more significant stressor compared to salinity, thus causing a decrease in abundance and richness. Critical temperature thresholds were observed at 30 and 35°C, the latter representing the most thermally tolerant species in the studied area Pararotalia calcariformata, which is the only symbiont-bearing species observed within the core of the heated area. Common species of the shallow hard-bottom habitats including several Lessepsian invaders are almost absent in the most exposed site indicating that excess warming will likely impede the survival of these species that currently benefit from the ongoing warming of the Eastern Mediterranean.

Molecular Phylogeny and Ecology of Textularia agglutinans d'Orbigny from the Mediterranean Coast of Israel: A Case of a Successful New Incumbent.

Textularia agglutinans d'Orbigny is a non-symbiont bearing and comparatively large benthic foraminiferal species with a widespread distribution across all oceans. In recent years, its populations have considerably expanded along the Israeli Mediterranean coast of the eastern Levantine basin. Despite its exceptionally widespread occurrence, no molecular data have yet been obtained. This study provides the first ribosomal DNA sequences of T. agglutinans complemented with morphological and ecological characterization, which are based on material collected during environmental monitoring of the hard bottom habitats along the Israeli Mediterranean coast, and from the Gulf of Elat (northern Red Sea). Our phylogenetic analyses reveal that all specimens from both provinces belong to the same genetic population, regardless their morphological variability. These results indicate that modern population of T. agglutinans found on the Mediterranean coast of Israel is probably Lessepsian. Our study also reveals that T. agglutinans has an epiphytic life mode, which probably enabled its successful colonization of the hard bottom habitats, at the Mediterranean coast of Israel, which consist of a diverse community of macroalgae. Our study further indicates that the species does not tolerate high SST (> 35°C), which will probably prevent its future expansion in the easternmost Mediterranean in light of the expected rise in temperatures.

Recent Invasion of the Symbiont-Bearing Foraminifera Pararotalia into the Eastern Mediterranean Facilitated by the Ongoing Warming Trend.

The eastern Mediterranean is a hotspot of biological invasions. Numerous species of Indo-pacific origin have colonized the Mediterranean in recent times, including tropical symbiont-bearing foraminifera. Among these is the species Pararotalia calcariformata. Unlike other invasive foraminifera, this species was discovered only two decades ago and is restricted to the eastern Mediterranean coast. Combining ecological, genetic and physiological observations, we attempt to explain the recent invasion of this species in the Mediterranean Sea. Using morphological and genetic data, we confirm the species attribution to P. calcariformata McCulloch 1977 and identify its symbionts as a consortium of diatom species dominated by Minutocellus polymorphus. We document photosynthetic activity of its endosymbionts using Pulse Amplitude Modulated Fluorometry and test the effects of elevated temperatures on growth rates of asexual offspring. The culturing of asexual offspring for 120 days shows a 30-day period of rapid growth followed by a period of slower growth. A subsequent 48-day temperature sensitivity experiment indicates a similar developmental pathway and high growth rate at 28°C, whereas an almost complete inhibition of growth was observed at 20°C and 35°C. This indicates that the offspring of this species may have lower tolerance to cold temperatures than what would be expected for species native to the Mediterranean. We expand this hypothesis by applying a Species Distribution Model (SDM) based on modern occurrences in the Mediterranean using three environmental variables: irradiance, turbidity and yearly minimum temperature. The model reproduces the observed restricted distribution and indicates that the range of the species will drastically expand westwards under future global change scenarios. We conclude that P. calcariformata established a population in the Levant because of the recent warming in the region. In line with observations from other groups of organisms, our results indicate that continued warming of the eastern Mediterranean will facilitate the invasion of more tropical marine taxa into the Mediterranean, disturbing local biodiversity and ecosystem structure.

Geochemical evidence for the link between sulfate reduction, sulfide oxidation and phosphate accumulation in a Late Cretaceous upwelling system.

BACKGROUND: On Late Cretaceous Tethyan upwelling sediments from the Mishash/Ghareb Formation (Negev, Israel), bulk geochemical and biomarker analyses were performed to explain the high proportion of phosphates in the lower part and of organic matter (OM) preserved in upper parts of the studied section. The profile is composed of three facies types; the underlying Phosphate Member (PM), the Oil Shale Member (OSM) and the overlying Marl Member (MM). RESULTS: Total organic carbon (TOC) contents are highly variable over the whole profile reaching from 0.6% in the MM, to 24.5% in the OSM. Total iron (TFe) varies from 0.1% in the PM to 3.3% in the OSM. Total sulfur (TS) ranges between 0.1% in the MM and 3.4% in the OSM, resulting in a high C/S ratio of 6.5 in the OSM section. A mean proportion of 11.5% total phosphorus (TP) in the PM changed abruptly with the facies to a mean value of only 0.9% in the OSM and the MM. The TOC/TOCOR ratios argue for a high bacterial sulfate reduction activity and in addition, results from fatty acid analyses indicate that the activity of sulfide-oxidizing activity of bacteria was high during deposition of the PM, while decreasing during the deposition of the OSM. CONCLUSIONS: The upwelling conditions effected a high primary productivity and consequently the presence of abundant OM. This, in combination with high sulfate availability in the sediments of the PM resulted in a higher sulfide production due to the activity of sulfate-reducing bacteria. Iron availability was a limiting factor during the deposition of the whole section, affecting the incorporation of S into OM. This resulted in the preservation of a substantial part of OM against microbial degradation due to naturally-occurring sulfurization processes expressed by the high C/S ratio of 6.5 in the OSM. Further, the abundant sulfide in the pore water supported the growth of sulfide-oxidizing bacteria promoting the deposition of P, which amounted to as much as 15% in the PM. These conditions changed drastically from the PM to the OSM, resulting in a significant reduction of the apatite precipitation and a high concentration of reactive S species reacting with the OM.

Molecular evidence for Lessepsian invasion of soritids (larger symbiont bearing benthic foraminifera).

The Mediterranean Sea is considered as one of the hotspots of marine bioinvasions, largely due to the influx of tropical species migrating through the Suez Canal, so-called Lessepsian migrants. Several cases of Lessepsian migration have been documented recently, however, little is known about the ecological characteristics of the migrating species and their aptitude to colonize the new areas. This study focused on Red Sea soritids, larger symbiont-bearing benthic foraminifera (LBF) that are indicative of tropical and subtropical environments and were recently found in the Israeli coast of the Eastern Mediterranean. We combined molecular phylogenetic analyses of soritids and their algal symbionts as well as network analysis of Sorites orbiculus Forskål to compare populations from the Gulf of Elat (northern Red Sea) and from a known hotspot in Shikmona (northern Israel) that consists of a single population of S. orbiculus. Our phylogenetic analyses show that all specimens found in Shikmona are genetically identical to a population of S. orbiculus living on a similar shallow water pebbles habitat in the Gulf of Elat. Our analyses also show that the symbionts found in Shikmona and Elat soritids belong to the Symbiodinium clade F5, which is common in the Red Sea and also present in the Indian Ocean and Caribbean Sea. Our study therefore provides the first genetic and ecological evidences that indicate that modern population of soritids found on the Mediterranean coast of Israel is probably Lessepsian, and is less likely the descendant of a native ancient Mediterranean species.

The effect of thermal pollution on benthic foraminiferal assemblages in the Mediterranean shoreface adjacent to Hadera power plant (Israel).

The thermal pollution patch of Hadera power plant was used as a natural laboratory to evaluate the potential long-term effects of rise in Eastern Mediterranean SST on living benthic foraminifera. Their sensitivity to environmental changes makes foraminifera ideal for this study. Ten monthly sampling campaigns were performed in four stations located along a temperature gradient up to 10 °C from the discharge site of heated seawater to a control station. The SST along this transect varied between 25/18 °C in winter and 36/31 °C in summer. A significant negative correlation was found between SST in all stations and benthic foraminiferal abundance, species richness and diversity. The total foraminiferal abundance and species richness was particularly low at the thermally polluted stations especially during summer when SST exceeded 30 °C, but also throughout the entire year. This indicates that thermal pollution has a detrimental effect on benthic foraminifera, irrelevant to the natural seasonal changes in SST.

The paleoclimate of the Eastern Mediterranean during the transition from early to mid Pleistocene (900 to 700 ka) based on marine and non-marine records: An integrated overview.

Climate change is frequently considered an important driver of hominin evolution and dispersal patterns. The role of climate change in the last phase (900-700 ka) of the Middle Pleistocene Transition (MPT) in the Levant and northeast Africa was examined, using marine and non-marine records. During the MPT the global climate system shifted from a linear 41 k.yr. into a highly non-linear 100 k.yr. system, considerably changing its global modulation. Northeast Africa aridity further intensified around 950ka, as indicated by a sharp increase in dust flux, and a jump to overall higher levels thereafter, coinciding with a lack of sapropels in the deep eastern Mediterranean (930-690ka). The increased dust flux centering at ∼800ka corresponds to the minima in 400 k.yr. eccentricity, a minima in 65 °N solar forcing and in the weakest African monsoon precession periodicity. This resulted in expansion of hyper-arid conditions across North Africa, the lowest lake levels in eastern Africa and the lowest rainfall in the Nile River headwaters. In the eastern Mediterranean an increasing continental signature is seen in glacial stages 22 (∼880ka) and 20 (∼800ka). Lower arboreal pollen values also indicate arid conditions during these glacial stages. The southern and eastern parts of the Negev Desert, unlike its northern part, were hyper-arid during the MPT, making them highly unsustainable. The fluctuations in the stands of Lake Amora follow global climate variability but were more moderate than those of its last glacial Lake Lisan successor. In the northern Jordan-Valley Hula Lake, frequent fluctuations in lake level coincide with both global climate changes and minor changes in water salinity varying from fresh to oligohaline. It appears therefore that the most pronounced and widespread deterioration in climate occurred in northeast Africa from 900 to 700ka, whereas in the Levant the corresponding climatic changes were more moderate.

Tracing natural and anthropogenic Pb in sediments along the Mediterranean Coast of Israel using Pb isotopes.

The natural and anthropogenic sources of Pb in surface sediments offshore the Israeli Mediterranean coast were studied using the isotopic composition of Pb in diluted acid sediment extracts. Surface sediments were collected at the lower reaches of coastal streams, along a south-north offshore transect and at selected monitoring stations of the Dan Region Wastewater Plant (DRWP) outfall pipe. The background values of the Pb isotopic composition were determined from the deepest part of two representative cores collected offshore and were found to have a narrow range dominated mainly by clays derived from both inland soils and the Nilotic cell and to a lesser extent from the Saharan dust. The impact of the DRWP activated sludge can be traced to a distance of ca. 2 km from the outfall pipe. Enrichment factors of Zn, Cu, and Pb were up to 25 and are strongly correlated with each other and with the Pb isotopic composition, thus demonstrating the sludge to be their common source. The isotopic compositions of Pb in stream sediments have the widest range of values and indicate a strong anthropogenic contribution, probably from both post-1992 aerosols and point sources. However the impact of stream sediments on marine sediments could not be clearly detected.