Assessment of the ecological quality status of the Sepetiba Bay (SE Brazil): When metabarcoding meets morphology on foraminifera.

In recent years, the region surrounding Sepetiba Bay (SB; SE Brazil) has become a hub of intense urban expansion and economic exploitation in response to ore transport and industrial and port activities. As a result, contaminants have been introduced into the bay, leading to an overall worsening of the environmental quality. The present work applies for the first time a foraminiferal morphology-based approach (M) and eDNA-based metabarcoding sequencing (G), along with geochemical data to assess the ecological quality status (EcoQS) in the SB. Principal component analysis shows that the eDNA and morphospecies diversity as well as most of the taxa relative abundance decline in response to the environmental stress (ES) gradient related to total organic carbon (TOC) and metal pollution. Based on ecological indices, Exp(H'bc) (G), Exp(H'bc) (M), foraminifera ATZI marine biotic index (Foram-AMBI), Foram Stress Index (FSI), and geochemical indices (TOC and Potential Ecological Risk Index), the lowest values of EcoQS (i.e., bad to moderate) are inferred in the innermost part of the SB. Despite minor discrepancies among the six EcoQS indices, an agreement has been found for 63% of the stations. To improve the agreement between the ecological indices, it is necessary to fill the gap in species ecology; information on the ecology of many species is still unknown. This work reinforces the importance of molecular analysis and morphological methods in environmental impact studies and confirms the reliability of foraminiferal metabarcoding in EcoQS assessment. This is the first study evaluating the EcoQS in the South Atlantic by using combined foraminiferal eDNA metabarcoding with morphological data.

Inferring the ecological quality status based on living benthic foraminiferal indices in transitional areas of the Guanabara bay (SE Brazil).

Using benthic foraminifera, we evaluate the ecological quality status (EcoQS) of transitional waters of the Guanabara Bay (SE Brazil) by applying the diversity-based index exp (H'bc) and the sensitivity-based Foram-AMBI for the first time in South America. The Guanabara Bay was selected for this study as it is one of the largest transitional ecosystems in the State of Rio de Janeiro and has been severely impacted by anthropogenic activities. Concentrations of potentially toxic elements (PTEs) were assessed by sequential chemical extraction in three phases (i.e., dissolved in water, adsorbed on organic matter, and Mn oxy-hydroxides). Total organic carbon, total nitrogen, and stable isotope (δ13C and δ15N) signatures of organic matter were analyzed to trace environmental stress. The Ammonia/Elphidium ratio suggests hypoxic conditions at most of the sampled sites. Principal component analysis identifies the first component as environmental stress underlying organic matter and PTE enrichment (in all three phases), which is positively related to Foram-AMBI and negatively to exp (H'bc). The exp (H'bc) and Foram-AMBI indices reveal that stations near the Governador Island and Niterói margin have the worst EcoQS, showing medium to extreme pollution. Additionally, Foram-AMBI and exp (H'bc) provide a congruent EcoQS classification for ∼64% of the sites. Although these results are promising, they suggest that a significant effort should be made to obtain better knowledge of foraminiferal ecological requirements to employ benthic foraminifera as a biomonitoring and management method.

Trace metals enrichment and potential ecological risk in sediments of the Sepetiba Bay (Rio de Janeiro, SE Brazil).

The Sepetiba Bay (SB; SE Brazil) has been severely affected by growing of urbanization and industrial activity. This work aims to analyze the evolution of contamination by metals of sediments in SB. The results show a marked increasing trend in the concentrations of potentially toxic elements (PTEs), which is consistent with the rapid populational and industrial growth, mostly since 1970 CE. The remobilization and redistribution of sediments by currents have contributed to the dispersion of metals from the main source of pollutants to relatively distant regions. "Moderately to strongly polluted" sediments are also recorded in some sites in deeper sedimentary layers (namely in preindustrial periods), probably due to lithologic sources of the sediments. The concentrations of PTEs in SB are relatively high when compared with those found globally and in other Brazilian water bodies. Samples of high-resolution sediment cores confirmed that potential ecological risk to the coastal system is influenced not only through human actions but also by natural causes.

Ecological quality status of the NE sector of the Guanabara Bay (Brazil): A case of living benthic foraminiferal resilience.

The ecological quality status of the NE region of the Guanabara Bay (SE Brazil), one of the most important Brazilian embayments, is evaluated. For this purpose, sediment samples from in the inner of the Guanabara Bay (GB) were collected and analyzed (grain-size, mineralogy, geochemistry and living foraminifera). In this study, it is hypothesized that the potentially toxic elements (PTEs) concentrations, in solution and associated with organic matter (OMPTEs, potential nutrient source), may represent two potential pathways to impact benthic foraminifers. A multiproxy approach applied to complex statistical analyses and ecological indexes shows that the study area is, in general, eutrophic (with high organic matter and low oxygen content), polluted by PTEs and oil. As a consequence, foraminifera are not abundant and their assemblages are poorly diversified and dominated by some stress-tolerant species (i.e., Ammonia tepida, Quinqueloculina seminula, Cribroelphidium excavatum). The results allow us to identify a set of species sensitive to eutrophication and OMPTEs. Factors such as the increase of organic matter contents and OMPTEs and, in particular of Zn, Cd and Pb, the oxygen depletion and the presence of oil, altogether contribute to a marked reduction in the abundance and diversity of foraminifera. Ammonia-Elphidium Index and the Foram Stress Index confirm that the NE zone of GB is, in general, "heavily polluted", with "poor ecological quality status" and experiences suboxic to anoxic conditions. In light of it, special attention from public authorities and policymakers is required in order to take immediate actions to enable its environmental recovery.

Benthic foraminiferal and organic matter compounds as proxies of environmental quality in a tropical coastal lagoon: The Itaipu lagoon (Brazil).

Lagoons in the southeast coast of Brazil have experienced eutrophication due to the exponential increase of human population and sewage discharges. Living benthic foraminifera have demonstrated to be good bioindicators of such impacts. This study aims to evaluate the organic matter accumulation effects on the foraminiferal distribution in the Itaipu lagoon (Brazil). On the basis of the biotic and abiotic analyses, three sectors are identified. The Sector I, an inner area, is characterized by high dissolved oxygen values and foraminiferal species with preference for marine conditions, demonstrating the sea influence. The Sector II, in the mangrove margins, is associated to sandy sediment and biopolymers and mainly represented by euryhaline species. The Sector III is marked by low density or absence of living foraminifera and corresponds to a low quality organic matter enriched area (North, Southwest and Centre).

Assessment of the trophic state of a hypersaline-carbonatic environment: Vermelha Lagoon (Brazil).

Vermelha Lagoon is a hypersaline shallow transitional ecosystem in the state of Rio de Janeiro (Brazil). This lagoon is located in the protected area of Massambaba, between the cities of Araruama and Saquarema (Brazil), and displays two quite uncommon particularities: it exhibits carbonate sedimentation and displays the development of Holocene stromatolites. Due to both particularities, the salt industry and property speculation have been, increasingly, generating anthropic pressures on this ecosystem. This study aims to apply a multiproxy approach to evaluate the trophic state of Vermelha Lagoon based on physicochemical parameters and geochemical data for the quantification and qualification of organic matter (OM), namely total organic carbon (TOC), total sulfur (TS), total phosphorus (TP) and biopolymeric carbon (BPC), including carbohydrates (CHO), lipids (LIP) and proteins (PTN). The CHO/TOC ratio values suggest that OM supplied to the sediment is of autochthonous origin and results, essentially, from microbial activity. The cluster analyses allowed the identification of four regions in Vermelha Lagoon. The Region I included stations located in shallow areas of the eastern sector of Vermelha lagoon affected by the impact of the artificial channel of connection with Araruama Lagoon. The Region II, under the influence of salt pans, is characterized by the highest values of BPC, namely CHO promoted by microbiological activity. The Region III include stations spread through the lagoon with high values of dissolved oxygen and lower values of TP. Stromatolites and microbial mattes growth was observed in some stations of this sector. Region IV, where the highest values of TOC and TS were found, represents depocenters of organic matter, located in general in depressed areas. Results of this work evidences that the Vermelha Lagoon is an eutrophic but alkaline and well oxygenated environment (at both water column and surface sediment) where the autotrophic activity is greater than heterotrophic one. These particular conditions make this a special and rare ecosystem.

Environmental Quality Assessment of Bizerte Lagoon (Tunisia) Using Living Foraminifera Assemblages and a Multiproxy Approach.

This study investigated the environmental quality of the Bizerte Lagoon (Tunisia) through an integrated approach that combined environmental, biogeochemical, and living benthic foraminiferal analyses. Specifically, we analyzed the physicochemical parameters of the water and sediment. The textural, mineralogical, and geochemical characteristics of the sediment, including total organic carbon, total nitrogen, simultaneously extracted metals (SEM), acid volatile sulfides (AVS), chlorophyll a, CaCO3, and changes in bacterial populations and carbon isotopes were measured. The SEM/AVS values indicated the presence of relatively high concentrations of toxic metals in only some areas. Foraminiferal assemblages were dominated by species such as A. parkinsoniana (20-91%), Bolivina striatula (<40%), Hopkinsina atlantica (<17%), and Bolivina ordinaria (<15%) that cannot be considered typical of impacted coastal lagoons both in Mediterranean and northeast Atlantic regions. The results of this work suggest that Bizerte Lagoon is a unique setting. This lagoon is populated by typical marine species that invaded this ecosystem, attracted not only by the prevailing favorable environmental conditions but also by the abundance and quality of food. The results indicate that the metal pollution found in some areas have a negative impact on the assemblages of foraminifera. At present, however, this negative impact is not highly alarming.

Characterization of bottom hydrodynamic conditions on the central western Portuguese continental shelf based on benthic foraminifera and sedimentary parameters.

Dead benthic foraminiferal assemblages from the central western Portuguese continental shelf have been studied to identify the prevalent oceanographic processes in the study area. Sediment samples collected at 46 stations along transepts perpendicular to the coastal line, between the latitudes of 38-40 °N and 17-190 m water depth, in April/May 2008, were analysed for selected physicochemical parameters (temperature, redox potential), grain size, organic matter content, and benthic foraminifera. Statistical analysis identified two main groups of stations, the Inshore/Offshore groups, which are not only defined by their geographical positions, but easily distinguishable by different hydrodynamic conditions. The Offshore Group is mainly represented by deeper stations characterized by a higher percentage of fines and TOM, negative values of redox potential and by the higher foraminiferal density and species diversity than the Inshore one. Foraminiferal assemblages of the Offshore Group are dominated/represented by species (such as Cassidulina laevigata/Cassidulina carinata, Bolivina spathulata, Bolivina ordinaria, Globocassidulina minuta, Bulimina elongata/Bulimina gibba and Bulimina marginata) common in areas with significant concentrations of organic matter. The benthic foraminiferal assemblages of the Inshore Group are instead characterized by epifaunal species such as Lobatula lobatula, Cibicides ungerianus, Planorbulina mediterranensis, Gavelinopsis praegeri and Quinqueloculina seminula. Both the sedimentary and foraminiferal results suggest that this group of stations is subjected to stronger bottom hydrodynamic conditions, caused by waves and swell activity and coastal currents, than the Offshore Group. Bray-Curtis similarity comparison between the stations of both groups reveals that the Offshore Group has a higher internal similarity than the Inshore Group. These differences seem to stem from topographic forcing, from the presence of rocky outcrops, from canyons and capes, from the distribution of rivers and from the magnitude of their discharges, which determine specific hydrodynamic features and differences in the sedimentary deposits and biological productivity. The influence of the Tagus river (supply of fresh water, detritus and organic matter from continental sources), the presence of canyons and capes, which leave the most important imprint on the study area, are marked by changes in the foraminiferal assemblages both in the Inshore and Offshore groups.

Early diagenesis and clay mineral adsorption as driving factors of metal pollution in sediments: the case of Aveiro Lagoon (Portugal).

This work aims to define the factors driving the accumulation of metals in the sediment of the lagoon of Aveiro (Portugal). The role of initial diagenetic processes in controlling trace metal retention in surface sediment is traced by mineralogy, magnetic susceptibility and geochemical analyses. Although several studies have focused on the metal distribution in this polihaline and anthropized coastal lagoon, most of them have been solely focused on the total metal concentrations. This study instead represents the first attempt to evaluate in a vast area of the Aveiro Lagoon the role of biogeochemical processes in metal availability and distribution in three extracted phases: exchangeable cations adsorbed by clay and elements co-precipitated with carbonates (S1), organic matter (S2) and amorphous Mn hydroxides (S3). According to the sediment guideline values, the sediment is polluted by, for instance, As and Hg in the inner area of the Murtosa Channel, Pb in the Espinheiro Channel, Aveiro City canals and Aveiro Harbour, and Zn in the northern area of the Ovar Channel. These sites are located near the source areas of pollutants and have the highest total available concentrations in each extracted phase. The total available concentrations of all toxic metals are however associated, firstly, with the production of amorphous Mn hydroxides in most of the areas and, secondly, with adsorption by organic compounds. The interplay of the different processes implies that not all of the sites near pollution sources have polluted surface sediment. The accumulation of metals depends on not only the pollution source but also the changing in the redox state of the sediments that may cause alterations in the sediment retention or releasing of redox-sensitive metals. Results of this work suggest that the biogeochemical processes may play a significant role in the increase of the pollutants in the sediment of the Aveiro Lagoon.

Response of benthic foraminifera to organic matter quantity and quality and bioavailable concentrations of metals in Aveiro Lagoon (Portugal).

This work analyses the distribution of living benthic foraminiferal assemblages of surface sediments in different intertidal areas of Ria de Aveiro (Portugal), a polihaline and anthropized coastal lagoon. The relationships among foraminiferal assemblages in association with environmental parameters (temperature, salinity, Eh and pH), grain size, the quantity and quality of organic matter (enrichment in carbohydrates, proteins and lipids), pollution caused by metals, and mineralogical data are studied in an attempt to identify indicators of adaptability to environmental stress. In particular, concentrations of selected metals in the surficial sediment are investigated to assess environmental pollution levels that are further synthetically parameterised by the Pollution Load Index (PLI). The PLI variations allowed the identification of five main polluted areas. Concentrations of metals were also analysed in three extracted phases to evaluate their possible mobility, bioavailability and toxicity in the surficial sediment. Polluted sediment in the form of both organic matter and metals can be found in the most confined zones. Whereas enrichment in organic matter and related biopolymers causes an increase in foraminifera density, pollution by metals leads to a decline in foraminiferal abundance and diversity in those zones. The first situation may be justified by the existence of opportunistic species (with high reproduction rate) that can live in low oxic conditions. The second is explained by the sensitivity of some species to pressure caused by metals. The quality of the organic matter found in these places and the option of a different food source should also explain the tolerance of several species to pollution caused by metals, despite their low reproductive rate in the most polluted areas. In this study, species that are sensitive and tolerant to organic matter and metal enrichment are identified, as is the differential sensitivity/tolerance of some species to metals enrichment.

Foraminiferal biotopes and their distribution control in Ria de Aveiro (Portugal): a multiproxy approach.

Ria de Aveiro, which is located in the centre of Portugal (40° 38' N, 8° 45' W), is a well-mixed and complex coastal lagoon that is separated from the sea by a sandy barrier and connects with the Atlantic through an artificial inlet. Tidal currents are the main factor controlling the lagoon's hydrodynamics and, to a great extent, the sedimentary dynamic. The inner lagoonal zones receive input from several rivers and experience the pressure caused by the accumulation of organic matter and pollutants (namely, trace metals) from diverse anthropic activities. This paper is the first piece of work aiming to recognize, characterize and explain the main benthic foraminiferal biotopes in Ria de Aveiro. To provide a broad overview of this kind of setting, our results are compared to those of previous published studies conducted in similar transitional environments. The research is based on an investigation of 225 sites spread throughout this ecosystem. Utilizing a statistical approach, this study analyses the details of dead benthic foraminiferal assemblages composed of 260 taxa, the texture and composition (mineralogical and geochemical) of the sediment and physicochemical data. On the basis of the results of R-mode and Q-mode cluster analyses, several different biotopes can be defined as marsh biotope/near-marsh biotope; marginal urban/marginal urban mixing biotope; inner-outer lagoon biotope or enclosed lagoon; outer lagoon biotope, mixed sub-biotope; and outer lagoon, marine sub-biotope. These biotopes are related to foraminifera assemblages and substrate type and are influenced by local currents, water depth, chemical and physicochemical conditions, river or oceanic proximity, and anthropogenic impact, as evidenced by the mapping of the six factor loadings of the principal component analysis conducted herein. Based on a similar methodology of analysis as that applied in previous studies in the Lagoon of Venice, comparable biotypes were identified in Lagoon of Aveiro.

Assessment of the health quality of Ria de Aveiro (Portugal): heavy metals and benthic foraminifera.

This work analyses the distribution of heavy metals in the sediments of Ria de Aveiro (Portugal) assessed by total digestion and sequential chemical extraction of the sediments. The influence of environmental parameters on the living benthic foraminiferal assemblages was studied. The most polluted parts in the Ria de Aveiro are areas where the residence time is high and cohesive sediments are deposited. Organic matter, which is an excellent scavenger for a number of metals, is in general more abundant in the finer deposits of this lagoon, which act as sinks of anthropogenic pollutants. This condition is observed in Aveiro canals and Murtosa channel where sediments with the highest concentrations of Zn, Pb, Cu, and Cr are found. The sediments of Murtosa channel are also enriched in As, Co and Hg. In Aveiro canals the enrichment of heavy metals is mostly related to the past industrial production at their margins (ceramic and metallurgy), whereas in Murtosa channel with effluent discharges of the Chemical Complex of Estarreja. Foraminiferal density and diversity reach higher values near the lagoon mouth under higher marine influence and decline in general under very low-oxygen conditions. Some species seems to be indifferent to the increasing of TOC (e.g. Haynesina germanica and Ammonia tepida) and some have an opportunistic behaviour in areas with very depressed levels of oxygen (e.g. A. tepida and Quinqueloculina seminulum) whereas other species can better tolerate sulphide/reducing conditions (e.g. H. germanica, Bolivina ordinaria, Buliminella elegantissima, Bulimina elongata/gibba and Nonionella stella) a widespread condition in this lagoon. Foraminiferal density and some species are negatively correlated with concentrations of heavy metals. A most sensitive group of species to higher concentrations of heavy metals is identified (such as B. ordinaria, B. pseudoplicata and B. elongata/gibba) and another one of more tolerant species (such as H. germanica A. tepida and Q. seminulum). Foraminifera are more tolerate higher available concentrations (AC) of Zn in any phase than higher AC of Cu adsorbed do clay minerals (F1) and associated with Fe and Mn oxides (F2) and of Pb in F2; the phase F2, probably the most mobile phase, and even phase F1 seems to be more toxic than the increasing of metals in organic matter (F3).