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.

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.

The effect of long-term brine discharge from desalination plants on benthic foraminifera.

Desalination plants along the Mediterranean Israeli coastline currently provide ~587 million m3 drinking water/year, and their production is planned to increase gradually. Production of drinking water is accompanied by a nearly equivalent volume of brine discharge with a salinity of ~80 that is twice the normal, which can potentially impact marine ecosystems. The goal of this study was to examine whether benthic foraminifera, a known sensitive marine bio-indicator, are affected by this brine-discharge. For that, we investigated the seasonal and cumulative effect of brine discharges of three operating desalination facilities along the Israeli coast. Those facilities are located in Ashkelon, Hadera, and Sorek. The brine-discharge in the first two desalination plants is associated with thermal pollution, while the Sorek facility entails increased salinity but no thermal pollution. In four seasonal cruises during one year, we collected surface sediment samples in triplicates by grabs from the outfall (near the discharge site), and from a non-impacted control station adjacent to each study site. Our results highlight that the most robust responses were observed at two out of three desalination shallow sites (Ashkelon and Hadera), where the brine was discharged directly from a coastal outfall and was accompanied with thermal pollution from the nearby power plants. The total foraminiferal abundance and diversity were, generally, lower near the outfalls, and increased towards the control stations. Moreover, changes in the relative abundances of selected species indicate their sensitivity to the brine discharge. The most noticeable response to exclusively elevated salinity was detected at Sorek discharge site, where we observed a sharp decline in organic-cemented agglutinated benthic foraminifera, suggesting that these are particularly sensitive to elevated salinity. The herein study contribute new insights into the effect of brine discharge from desalination plants, on benthic foraminifera, and propose a scientifically-based ecological monitoring tool that can help stakeholders.

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.

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.

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.

Natural oligotrophy vs. pollution-induced eutrophy on the SE Mediterranean shallow shelf (Israel): environmental parameters and benthic foraminifera.

The eastern Mediterranean is naturally highly oligotrophic, but urbanization along the Levant coast has led to raised organic and nutrient loads. This study tracks living foraminiferal assemblages at two sites near an activated sewage sludge outfall from 11/2003 to 5/2004. Oligotrophic site PL29 shows seasonal variations in O(2), chlorophyll a, and organic carbon, and has an abundant, diverse benthic foraminiferal assemblage living at various in-sediment depths. At eutrophic site PL3, approximately 16 years of sludge injection favor a depleted assemblage primarily of opportunist foraminifera. This site shows less seasonality, is subjected to organic matter overload, O(2)-stress, and periodic anoxia, foraminifera are less abundant and diverse, and live at shallower depths. The assemblages at both sites represent a common pool of species, with Ammonia tepida highly dominant. Benthic foraminifera were therefore found to be sensitive to trophic trajectories, respond on sub-seasonal time-scales, and track injection and dispersal of organic loads on the shelf.