Nanoparticle-Biological Interactions in a Marine Benthic Foraminifer.

The adverse effects of engineered nanomaterials (ENM) in marine environments have recently attracted great attention although their effects on marine benthic organisms such as foraminifera are still largely overlooked. Here we document the effects of three negatively charged ENM, different in size and composition, titanium dioxide (TiO2), polystyrene (PS) and silicon dioxide (SiO2), on a microbial eukaryote (the benthic foraminifera Ammonia parkinsoniana) using multiple approaches. This research clearly shows the presence, within the foraminiferal cytoplasm, of metallic (Ti) and organic (PS) ENM that promote physiological stress. Specifically, marked increases in the accumulation of neutral lipids and enhanced reactive oxygen species production occurred in ENM-treated specimens regardless of ENM type. This study indicates that ENM represent ecotoxicological risks for this microbial eukaryote and presents a new model for the neglected marine benthos by which to assess natural exposure scenarios.

Impacts of ocean acidification on intertidal benthic foraminiferal growth and calcification.

Foraminifera are expected to be particularly susceptible to future changes in ocean carbonate chemistry as a function of increased atmospheric CO2. Studies in an experimental recirculating seawater system were performed with a dominant benthic foraminiferal species collected from intertidal mudflats. We investigated the experimental impacts of ocean acidification on survival, growth/calcification, morphology and the biometric features of a calcareous species Elphidium williamsoni. Foraminifera were exposed for 6 weeks to four different pH treatments that replicated future scenarios of a high CO2 atmosphere resulting in lower seawater pH. Results revealed that declining seawater pH caused a decline in foraminiferal survival rate and growth/calcification (mainly through test weight reduction). Scanning electron microscopy image analysis of live specimens at the end of the experimental period show changes in foraminiferal morphology with clear signs of corrosion and cracking on the test surface, septal bridges, sutures and feeding structures of specimens exposed to the lowest pH conditions. These findings suggest that the morphological changes observed in shell feeding structures may serve to alter: (1) foraminiferal feeding efficiency and their long-term ecological competitiveness, (2) the energy transferred within the benthic food web with a subsequent shift in benthic community structures and (3) carbon cycling and total CaCO3 production, both highly significant processes in coastal waters. These experimental results open-up the possibility of modelling future impacts of ocean acidification on both calcification and dissolution in benthic foraminifera within mid-latitude intertidal environments, with potential implications for understanding the changing marine carbon cycle.

The response of cultured meiofaunal and benthic foraminiferal communities to lead exposure: Results from mesocosm experiments.

Lead (Pb) is regarded as a highly toxic element that poses a serious threat to biota. A mesocosm experiment was performed to assess the influence of Pb on meiofaunal (metazoans within 45-500 µm) and benthic foraminiferal (protozoan) communities. To this end, sediments bearing such communities were incubated in mesocosms, exposed to different levels of Pb in seawater, and monitored for up to 8 wk. Concentrations of Pb <1 ppm in water did not promote a significant increase of this metal in sediments. Relatively high concentrations of Pb seemed to affect meiofaunal and benthic foraminiferal communities by reducing their richness or diversity, and the abundance of the most sensitive taxa. The mesocosm approach can be considered an effective method to document the responses of meiofaunal and benthic foraminiferal communities to various kinds and concentrations of pollutants over time. This approach allows the evaluation of dose-response relationships, validates the outcomes of field studies, and possibly confirms the sediment quality guidelines and thresholds. Environ Toxicol Chem 2018;37:2439-2447. © 2018 SETAC.

Morphological deformities of benthic foraminifera in response to nearshore pollution of the Red Sea, Egypt.

The Red Sea encompasses a wide range of tropical marine habitats that are stressed due to anthropogenic activities. The main anthropogenic activities are hydrocarbon exploration and important trading harbors. This work aims to assess the influence of the Red Sea coastal heavy metal contamination on the marine meiofauna along three sites (Ras Gharib, Safaga, and Quseir). Eight heavy metal (Cu, Cd, Zn, Pb, Cr, Co, Ni, and Mn) contents are considered in four benthic foraminiferal species (Elphidium striatopunctatum, Amphistegina lobifera, Amphisorus hemprichii, and Ammonia beccarii). Quseir Harbor showed the highest level of pollution followed by Safaga and Ras Gharib sites. The analyzed benthic foraminiferal tests displayed noteworthy high concentrations of Cd, Zn, and Pb in Quseir Harbor which could be attributed to the anthropogenic activities in the nearshore areas. Some foraminiferal tests exhibited abnormalities in their apertures, coiling, and shape of chambers. A comparison between normal and deformed foraminiferal tests revealed that the deformed ones are highly contaminated with elevated heavy metal contents such as Fe, Mn, Ni, and Cd. Statistics in addition to geo-accumulation and pollution load indices reveal a whistling alarm for the Quseir harbor. The present data are necessary to improve conservation and management of the Red Sea ecosystem in the near future.

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.

Environmental impact of the largest petroleum terminal in SE Brazil: A multiproxy analysis based on sediment geochemistry and living benthic foraminifera.

The Dutos e Terminais do Centro Sul (DTCS) is one of the largest petroleum terminals of the South America located in the São Sebastião Channel (SSC) on the southeastern Brazilian coast. The aims of this study were to compare the sediment quality near the DTCS with that of several sites in the SSC region including the Araçá (AR) domestic sewage outfall and to assess the efficiency of the DTCS wastewater treatment plant. To achieve these goals, textural, geochemical, and living benthic foraminifera results were analyzed for the DTCS, AR, and SSC regions. Sediments in the DTCS area were silty with high concentrations of total organic carbon (1.7-2.4%), total nitrogen (0.2-0.3%), total sulfur (0.4-0.6%), and total (0.12-0.18%) and inorganic phosphorous (0.07-0.11%). These values were higher than those in sediments collected in the SSC and Araçá regions. The sediments' concentrations of As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn in the SSC and AR regions were lower than their corresponding probable effect levels (PELs). However, sediments near the DTCS were enriched with As, Cu, and Ni, whose concentrations exceeded their corresponding threshold effect levels (TELs). Around the DTCS outfall diffusers, living foraminiferal densities and diversities were lower than those for the other areas studied. In the DTCS area, it was necessary to search 50 to 190 cm3 of sediment to find 100 live specimens. In the SSC and Araçá areas, a maximum of 40 cm3 of sediment was enough to locate 100 live specimens. The lower density and diversity of living foraminifera around the DTCS than around the other areas illustrates the impact of the environmental stress caused by the presence of pollutants. These results indicate that the wastewater treatment plant efficiency is low and its discharge of pollutants from petrochemical waste liquids affects the benthic fauna around the DTCS in a potentially harmful manner.

Identifying past petroleum exploration related drill cutting releases and influences on the marine environment and benthic foraminiferal communities, Goliat Field, SW Barents Sea, Norway.

The present multiproxy investigation of marine sediment cores aims at: 1) Identifying dispersion of petroleum exploration related drill cutting releases within the Goliat Field, Barents Sea in 2006/07 and 2) Assessing past and present influence of drill cuttings on the marine environment. The cores were recovered 5, 30, 60, 125 and 250m from the drill site in the eastward downstream direction. Downstream dispersion of drill cuttings is evaluated by examining sediment grain size distribution and barium (Ba), heavy metal, total organic carbon and sulphur concentrations. Dispersion of drill cuttings was limited to <125m east from the drill site. Influence of drill cutting releases on the marine environment is assessed via microfaunal analysis of primarily calcareous benthic foraminifera. The findings suggest contemporaneous physical smothering at ≤30m from the drill site, with a natural fauna reestablishing after drilling cessation indicating no long-term effect of drill cutting releases.

Assessing the effect of mercury pollution on cultured benthic foraminifera community using morphological and eDNA metabarcoding approaches.

Mercury (Hg) is a highly toxic element for living organisms and is known to bioaccumulate and biomagnify. Here, we analyze the response of benthic foraminifera communities cultured in mesocosm and exposed to different concentrations of Hg. Standard morphological analyses and environmental DNA metabarcoding show evidence that Hg pollution has detrimental effects on benthic foraminifera. The molecular analysis provides a more complete view of foraminiferal communities including the soft-walled single-chambered monothalamiids and small-sized hard-shelled rotaliids and textulariids than the morphological one. Among these taxa that are typically overlooked in morphological studies we found potential bioindicators of Hg pollution. The mesocosm approach proves to be an effective method to study benthic foraminiferal responses to various types and concentrations of pollutants over time. This study further supports foraminiferal metabarcoding as a complementary and/or alternative method to standard biomonitoring program based on the morphological identification of species communities.

Benthic foraminifera as bio-indicators of chemical and physical stressors in Hammerfest harbor (Northern Norway).

We investigated benthic foraminiferal assemblages in contaminated sediments in a subarctic harbor of Northern Norway to assess their utility as indicators of anthropogenic impacts. Sediments in the harbor are repositories for POPs and heavy metals supplied through discharges from industry and shipping activities. Sediment contaminant concentrations are at moderate to poor ecological quality status (EcoQS) levels. The EcoQS based on benthic foraminiferal diversity reflects a similar trend to the EcoQS based on contaminant concentrations. Foraminiferal density and diversity is low throughout the harbor with distinct assemblages reflecting influence of physical disturbances or chemical stressors. Assemblages impacted by physical disturbance are dominated by L. lobatula and E. excavatum, while assemblages impacted by chemical stressors are dominated by opportunistic species S. fusiformis, S. biformis, B. spathulata and E. excavatum. The foraminiferal assemblage from an un-impacted nearby fjord consists mainly of agglutinated taxa. These assemblages provides a valuable baseline of the ecological impacts of industrialization in northern coastal communities.

Heavy metal accumulation in surface sediments at the port of Cagliari (Sardinia, western Mediterranean): Environmental assessment using sequential extractions and benthic foraminifera.

Superficial sediments were taken at the port of Cagliari (Sardinia, Italy), which includes the oil terminal of one of the largest oil refineries in the Mediterranean. Significant trace metal concentrations were found in the whole port area. Sequential extraction of metals from the different sediment fractions (BCR method) showed a higher risk of remobilisation for Cd, which is mostly bound to the exchangeable fraction. Foraminiferal density and richness of species were variable across the study area. The living assemblages were characterized by low diversity in samples collected close to the port areas. Ammonia tepida and bolivinids, which were positively correlated with concentrations of heavy metals and organic matter content, appeared to show tolerance to the environmental disturbance. The sampling sites characterized by the highest values of biotic indices were located far from the port areas and present an epiphytic and epifaunal biocoenosis.

Effects of hypoxia caused by mussel farming on benthic foraminifera in semi-closed Gamak Bay, South Korea.

Seawater monitoring and geochemical and benthic foraminiferal analysis of sediments were conducted to identify the effects of hypoxia created by a mussel farm on benthic foraminifera in a semi-closed bay. Extremely polluted reductive conditions with a high content of organic matter (OM) at >12.0% and oxygen minimum zones (OMZs) with dissolved oxygen (DO) <0.4mg∙L(-1) were formed below the mussel farm in the northwest area of Gamak Bay, and gradually diffused toward the south. Highly similar patterns of variation were observed in species diversity, abundance frequency, and benthic foraminiferal assemblage distributed from Elphidium subarcticum-Ammonia beccarii in the northwest area through E. subarcticum-A. beccarii-Trochammina hadai, E. subarcticum-A. beccarii-Elphidiumclavatum, and E. clavatum-Ammonia ketienziensis in the southern area. These phenomena were caused by hydrodynamics in the current water mass. It was thought that E. subarcticum is a bioindicator of organic pollution caused by the mussel farm.

Influence of local habitat on the physiological responses of large benthic foraminifera to temperature and nutrient stress.

Large benthic foraminifera (LBF) are important for reef sediment formation, but sensitive to elevated temperature and nutrients. However, it is possible that conspecific foraminifera living in different reef sites present divergent response to environmental shifts. We investigated how populations of Amphistegina lobifera from reef sites located along a temperature and nutrient gradient of the northern Great Barrier Reef respond and acclimate to elevated temperature and nitrate under lab-controlled conditions. Generalized linear mixed models showed that interaction between reef sites and temperature or nitrate conditions had a significant effect on survivorship, bleaching frequency and growth rates of A. lobifera. Further physiological analyses of antioxidant capacity and Ca-ATPase activity showed that populations collected from the inner-shelf sites (highest nutrient levels, largest temperature variation) were consistently able to acclimate to both parameters after 30 days. In contrast, foraminifera collected from the reef sites located in the mid- and outer-shelfs were significantly more sensitive to elevated temperatures and nitrate. Our results highlight the importance of local habitat in shaping the tolerance of LBF to changing environmental conditions; populations that live in stable environments are more sensitive to elevated temperature and nitrate, even within their fundamental tolerance range, than those that experience fluctuating conditions.

Evolution of the anthropogenic impact in the Augusta Harbor (Eastern Sicily, Italy) in the last decades: benthic foraminifera as indicators of environmental status.

The study of benthic foraminifera in sediment cores provides the opportunity to recognize environmental changes, including those due to the anthropogenic impact. The integration of these data with chemical-physical parameters provides a comprehensive quality assessment. This research was applied to a sediment core collected in the Augusta bay, where a very large commercial and military harbor and one of the largest petrochemical poles in Europe are present. Inside the petrochemical area also operated, from 1958 to 2003, a chlor-alkali plant with mercury cell technology which caused anthropic contamination of surrounding land and marine areas. The sediment core was collected in front of this plant and characterized for grain size and pollutants directly associated to chlor-alkali activity, such as mercury (Hg), barium (Ba), polychlorobiphenyls (PCBs), and polycyclic aromatic hydrocarbons (PAHs). Composition of foraminiferal assemblages and faunal parameters such as specific diversity, faunal density, abundance of abnormal specimens, and foraminiferal size were investigated as potential indicators of environmental status. Statistical analysis indicated a main common origin for Hg, Ba, and PCBs and the influence of pollutants on species distribution and faunal diversity and density. Exceptionally high Hg concentrations (63-680 mg/kg d.w.) were recorded in the whole core, where the geochronological study attributed the most contaminated levels to the period of maximum activity of the chlor-alkali plant, while a decrease of contamination was recorded after the stop of the activity. Distinct foraminiferal assemblages identified different ecozones along the core, which suggested decreasing anthropogenic impact from the bottom to the top.

Assessment of the impacts of trace metals on benthic foraminifera in surface sediments from the northwestern Taiwan Strait.

The distribution patterns of foraminiferal assemblages in relation to trace metals, sediment grain size, and calcium carbonate were studied in 232 surface sediments collected from the northwestern Taiwan Strait. Multivariate analyses of biotic and abiotic data revealed a separation of near-shore, coastal, and deep-water zones. The modified degree of contamination suggested that the overall contamination was very low to low. Trace metals were enriched in the near-shore and outside bays. Their distribution was likely determined by sediment transport pathways and hydrodynamic conditions. High metal concentrations co-occurred with a low density and diversity of foraminiferal assemblages. Pb, Ba, organic carbon, Ga, Zn, Cu, and Co had a positive correlation with near-shore assemblage, whereas Cr and Ni positively related to the deep-water assemblages. Some calcareous foraminifera were favored by CaCO3, Sr, and sand. This study highlights species' responses that are specific to environmental variables.

Effects of lead pollution on Ammonia parkinsoniana (foraminifera): ultrastructural and microanalytical approaches.

The responses of Ammonia parkinsoniana (Foraminifera) exposed to different concentrations of lead (Pb) were evaluated at the cytological level. Foraminifera-bearing sediments were placed in mesocosms that were housed in aquaria each with seawater of a different lead concentration. On the basis of transmission electron microscopy and environmental scanning electron microscopy coupled with energy dispersive spectrometer analyses, it was possible to recognize numerous morphological differences between untreated (i.e., control) and treated (i.e., lead enrichment) specimens. In particular, higher concentrations of this pollutant led to numerical increase of lipid droplets characterized by a more electron-dense core, proliferation of residual bodies, a thickening of the organic lining, mitochondrial degeneration, autophagosome proliferation and the development of inorganic aggregates.  All these cytological modifications might be related to the pollutant-induced stress and some of them such as the thickening of organic lining might suggest a potential mechanism of protection adopted by foraminifera.

A decline in benthic foraminifera following the deepwater horizon event in the northeastern Gulf of Mexico.

Sediment cores were collected from three sites (1000-1200 m water depth) in the northeastern Gulf of Mexico from December 2010 to June 2011 to assess changes in benthic foraminiferal density related to the Deepwater Horizon (DWH) event (April-July 2010, 1500 m water depth). Short-lived radioisotope geochronologies (²¹°Pb, ²³4Th), organic geochemical assessments, and redox metal concentrations were determined to relate changes in sediment accumulation rate, contamination, and redox conditions with benthic foraminiferal density. Cores collected in December 2010 indicated a decline in density (80-93%). This decline was characterized by a decrease in benthic foraminiferal density and benthic foraminiferal accumulation rate (BFAR) in the surface 10 mm relative to the down-core mean in all benthic foraminifera, including the dominant genera (Bulimina spp., Uvigerina spp., and Cibicidoides spp.). Cores collected in February 2011 documented a site-specific response. There was evidence of a recovery in the benthic foraminiferal density and BFAR at the site closest to the wellhead (45 NM, NE). However, the site farther afield (60 NM, NE) recorded a continued decline in benthic foraminiferal density and BFAR down to near-zero values. This decline in benthic foraminiferal density occurred simultaneously with abrupt increases in sedimentary accumulation rates, polycyclic aromatic hydrocarbon (PAH) concentrations, and changes in redox conditions. Persistent reducing conditions (as many as 10 months after the event) in the surface of these core records were a possible cause of the decline. Another possible cause was the increase (2-3 times background) in PAH's, which are known to cause benthic foraminifera mortality and inhibit reproduction. Records of benthic foraminiferal density coupled with short-lived radionuclide geochronology and organic geochemistry were effective in quantifying the benthic response and will continue to be a valuable tool in determining the long-term effects of the DWH event on a larger spatial scale.

Basin-scale estimates of pelagic and coral reef calcification in the Red Sea and Western Indian Ocean.

Basin-scale calcification rates are highly important in assessments of the global oceanic carbon cycle. Traditionally, such estimates were based on rates of sedimentation measured with sediment traps or in deep sea cores. Here we estimated CaCO3 precipitation rates in the surface water of the Red Sea from total alkalinity depletion along their axial flow using the water flux in the straits of Bab el Mandeb. The relative contribution of coral reefs and open sea plankton were calculated by fitting a Rayleigh distillation model to the increase in the strontium to calcium ratio. We estimate the net amount of CaCO3 precipitated in the Red Sea to be 7.3 ± 0.4·10(10) kg·y(-1) of which 80 ± 5% is by pelagic calcareous plankton and 20 ± 5% is by the flourishing coastal coral reefs. This estimate for pelagic calcification rate is up to 40% higher than published sedimentary CaCO3 accumulation rates for the region. The calcification rate of the Gulf of Aden was estimated by the Rayleigh model to be ∼1/2 of the Red Sea, and in the northwestern Indian Ocean, it was smaller than our detection limit. The results of this study suggest that variations of major ions on a basin scale may potentially help in assessing long-term effects of ocean acidification on carbonate deposition by marine organisms.

Decalcification of benthic foraminifera due to "Hebei Spirit" oil spill, Korea.

In order to determine the effects on foraminifera due to spilled crude oil in the "Herbei Spirit" incident, a study of benthic foraminiferal assemblages was carried out on sediment samples collected from the Sogeunri tidal flat, Taean Peninsula, Korea. Breakages of the chambers in the Ammonia beccarii and Elphidium subincertum species of the Sogeunri tidal flat with a low pH (6.98 on average) were marked. These chamber breakages occurred in 71.6% of A. beccarii and are thought to be caused by decalcification due to the fall in pH resulting from the "Hebei Spirit" oil spill. The factors that affect breakage of the chamber in benthic foraminifera under low pH condition may be not only deto decalcification but also to exposure duration of substrata in the tidal flat spilled crude oil.

The impact of ocean acidification on the functional morphology of foraminifera.

Culturing experiments were performed on sediment samples from the Ythan Estuary, N. E. Scotland, to assess the impacts of ocean acidification on test surface ornamentation in the benthic foraminifer Haynesina germanica. Specimens were cultured for 36 weeks at either 380, 750 or 1000 ppm atmospheric CO2. Analysis of the test surface using SEM imaging reveals sensitivity of functionally important ornamentation associated with feeding to changing seawater CO2 levels. Specimens incubated at high CO2 levels displayed evidence of shell dissolution, a significant reduction and deformation of ornamentation. It is clear that these calcifying organisms are likely to be vulnerable to ocean acidification. A reduction in functionally important ornamentation could lead to a reduction in feeding efficiency with consequent impacts on this organism's survival and fitness.

Deep-sea foraminifera from the Cassidaigne Canyon (NW Mediterranean): assessing the environmental impact of bauxite red mud disposal.

Benthic foraminiferal assemblages were investigated from two sites along the axis of the Cassidaigne Canyon (NW Mediterranean Sea). Both areas are contaminated by bauxite red mud enriched in iron, titanium, vanadium and chromium. These elemental enrichments are related to bauxite-derived minerals and various amorphous phases. At the shallowest station located very close to the pipe outlet, the benthic living foraminiferal community is characterised by a very low diversity and by an unusual dominance of Gyroidina umbonata and Bulimina marginata. The mechanical stress related to downslope transport of red mud is a likely source of hydro-sedimentary pollution precluding the settlement of diverse fauna. The living and dead foraminiferal faunas from the deepest site are typical of oligo-mesotrophic conditions prevailing in natural environments. There, bauxite residues have obviously no environmental impact on foraminiferal faunas. The bioavailability of trace metals is likely low as elemental enrichments were not observed in foraminiferal test chemistry.