Foraminifera and plastic pollution: Knowledge gaps and research opportunities.

Plastic has become one of the most ubiquitous and environmentally threatening sources of pollution in the Anthropocene. Beyond the conspicuous visual impact and physical damages, plastics both carry and release a cocktail of harmful chemicals, such as monomers, additives and persistent organic pollutants. Here we show through a review of the scientific literature dealing with both plastic pollution and benthic foraminifera (Rhizaria), that despite their critical roles in the structure and function of benthic ecosystems, only 0.4% of studies have investigated the effects of micro- and nano-plastics on this group. Consequently, we urge to consider benthic foraminifera in plastic pollution studies via a tentative roadmap that includes (i) the use of their biological, physiological and behavioral responses that may unveil the effects of microplastics and nanoplastics and (ii) the evaluation of the indicative value of foraminiferal species to serve as proxies for the degree of pollution. This appears particularly timely in the context of the development of management strategies to restore coastal ecosystems.

Sediment reworking of intertidal sediments by the benthic foraminifera Haynesina germanica: the importance of motion behaviour and densities.

This study aimed to describe for the first time the vertical motion behaviour of the intertidal foraminifera Haynesina germanica and its contribution to bioturbation. Its infaunal behaviour leads to the creation of a one-end tube within the first centimetre of sediment. In addition, a vertical trail following behaviour was described for the first time in foraminifera, which may be linked to the sustainability of the biogenic sedimentary structures. As a consequence, H. germanica produces a vertical transport of both mud and fine sediment fractions similarly to the sediment reworking mode reported for gallery-diffusor benthic species. This finding allows us to refine the bioturbating mode of H. germanica, previously classified as surficial biodiffusor. Furthermore, sediment reworking intensity appeared to be dependent on the foraminiferal density. H. germanica would adapt its motion behaviour to deal with the intra-specific competition for food and space that may occur when density increases. Consequently, this behavioural modification would affect both the species and the individual contribution to sediment reworking processes. In fine, sediment reworking in H. germanica may further contribute to the bioirrigation of intertidal sediments, which has implications for oxygen availability in sediments and on aerobic microbial processes involved in carbon and nutrient cycling at the sediment-water interface.

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.

A whale of a plastic tale: A plea for interdisciplinary studies to tackle micro- and nanoplastic pollution in the marine realm.

Plastic is one of the most ubiquitous sources of both contamination and pollution of the Anthropocene, and accumulates virtually everywhere on the planet. As such, plastic threatens the environment, the economy and human well-being globally. The related potential threats have been identified as a major global conservation issue and a key research priority. As a consequence, plastic pollution has become one of the most prolific fields of research in research areas including chemistry, physics, oceanography, biology, ecology, ecotoxicology, molecular biology, sociology, economy, conservation, management, and even politics. In this context, one may legitimately expect plastic pollution research to be highly interdisciplinary. However, using the emerging topic of microplastic and nanoplastic leachate (i.e., the desorption of molecules that are adsorbed onto the surface of a polymer and/or absorbed into the polymer matrix in the absence of plastic ingestion) in the ocean as a case study, we argue that this is still far from being the case. Instead, we highlight that plastic pollution research rather seems to remain structured in mostly isolated monodisciplinary studies. A plethora of analytical methods are now available to qualify and quantify plastic monomers, polymers and the related additives. We nevertheless show though a survey of the literature that most studies addressing the effects of leachates on marine organisms essentially still lack of a quantitative assessment of the chemical nature and content of both plastic items and their leachates. In the context of the ever-increasing research effort devoted to assess the biological and ecological effects of plastic waste, we subsequently argue that the lack of a true interdisciplinary approach is likely to hamper the development of this research field. We finally introduce a roadmap for future research which has to evolve through the development of a sound and systematic ability to chemically define what we biologically compare.

Plastic leachates: Bridging the gap between a conspicuous pollution and its pernicious effects on marine life.

With 4 to 12 million tons of plastic entering the marine environment each year, plastic pollution has become one of the most ubiquitous sources of pollution of the Anthropocene threatening the marine environment. Beyond the conspicuous physical damages, plastics may release a cocktail of harmful chemicals, i.e. monomers, additives and persistent organic pollutants. Although known to be highly toxic, plastic leachates seemingly appear, however, as the "somewhat sickly child" of the plastic pollution literature. We reviewed the only 26 studies investigating the impact of plastic leachates on marine microbes and invertebrates, and concluded that the observed effects essentially depend on the species, polymer type, plastic composition, accumulated contaminants and weathering processes. We identified several gaps that we believe may hamper progress in this emerging area of research and discussed how they could be bridged to further our understanding of the effects of the compounds released by plastic items on marine organisms. We first stress the lack of a consensus on the use of the term 'leachate', and subsequently introduce the concepts of primary and secondary leachates, based on the intrinisic or extrinsic origin of the products released in bulk seawater. We discuss how methodological inconsistencies and the discrepancy between the polymers used in experiments and their abundance in the environment respectively limit comparison between studies and a comprehensive assessment of the effects leachate may actually have in the ocean. We also discuss how the imbalanced in the variety of both organisms and polymers considered, the mostly unrealistic concentrations used in laboratory experiments, and the lack of investigation on key ecosystem engineers may considerably narrow the spectrum of our understanding of the plastic leachates' effects. We finally discuss how increasing multi-disciplinarity through collaborations between different research fields may benefit to an area of research which is still in its early infancy.

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].

Effects of temperature on the behaviour and metabolism of an intertidal foraminifera and consequences for benthic ecosystem functioning.

Heatwaves have increased in intensity, duration and frequency over the last decades due to climate change. Intertidal species, living in a highly variable environment, are likely to be exposed to such heatwaves since they can be emerged for more than 6 h during a tidal cycle. Little is known, however, on how temperature affects species traits (e.g. locomotion and behaviour) of slow-moving organisms such as benthic foraminifera (single-celled protists), which abound in marine sediments. Here, we examine how temperature influences motion-behaviour and metabolic traits of the dominant temperate foraminifera Haynesina germanica by exposing individuals to usual (6, 12, 18, 24, 30 °C) and extreme (high; i.e. 32, 34, 36 °C) temperature regimes. Our results show that individuals reduced their activity by up to 80% under high temperature regimes whereas they remained active under the temperatures they usually experience in the field. When exposed to a hyper-thermic stress (i.e. 36 °C), all individuals remained burrowed and the photosynthetic activity of their sequestered chloroplasts significantly decreased. Recovery experiments subsequently revealed that individuals initially exposed to a high thermal regime partially recovered when the hyper-thermic stress ceased. H. germanica contribution to surface sediment reworking substantially diminished from 10 mm3 indiv-1 day-1 (usual temperature) to 0 mm3 indiv-1 day-1 when individuals were exposed to high temperature regimes (i.e. above 32 °C). Given their role in sediment reworking and organic matter remineralisation, our results suggest that heatwaves may have profound long-lasting effects on the functioning of intertidal muddy ecosystems and some key biogeochemical cycles.

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.

Reconstruction of the palaeo-ecological quality status in an impacted estuary using benthic foraminifera: The Santos Estuary (São Paulo state, SE Brazil).

The Santos Estuary (SE Brazil) is a coastal ecosystem with a high ecological importance and has been strongly impacted by human activities over the last century. A multiproxy analysis of sediment core dated by 137Cs, 210Pb and 226Ra activities and based on sediment geochemistry and benthic foraminifera is here used to reconstruct the environmental changes and the variations of the Palaeo-Ecological Quality Status (Palaeo-EcoQS) during the last ~120 years. The Palaeo-EcoQS was reconstructed by applying the diversity index Exp(H'bc) based on the benthic foraminiferal fauna. Specifically, the Ecological Quality Ratio (EQR) allowed to assess the Palaeo-EcoQS during the last ~120 years using local reference conditions. Based on our data, the pre-industrial period (~1883-1902) represents the reference conditions with "Good" Palaeo-EcoQS. The ~1902-1972 period coincides with the beginning of industrial operations and intensification of coastal urbanization leading to a deterioration of the environmental quality and Palaeo-EcoQS shifting to "Moderate" conditions. Dredging operations in 1972 led to increase the influences of adjacent sea that ultimately resulted in a "Good" Palaeo-EcoQS persisting up to the 1990s. Despite the preservation actions and recovery programs, the 1993-2012 period was characterized by an overall deterioration of the environmental conditions. Indeed, the reconstructed "Poor" to "Bad" Palaeo-EcoQS suggest the ineffectiveness of the remediation actions. This work confirmed that benthic foraminifera are reliable to evaluate EcoQS and Palaeo-EcoQS in estuarine ecosystems. Based on the present findings and previous studies showing the potential of fossil foraminifera to define in situ reference conditions, we recommend the inclusion of foraminifera in the list of biological quality elements within legislations concerning transitional and marine habitats.

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.

Can benthic foraminifera serve as proxies for changes in benthic macrofaunal community structure? Implications for the definition of reference conditions.

Benthic macrofauna is one of the most widely used biological groups to assess the ecological status of marine systems. Lately, attention has been paid to similar use of benthic foraminifera. In this study, distribution patterns of benthic foraminiferal and macrofaunal species were investigated simultaneously in 11 fjords in southeastern Norway in order to assess correlations and responses to environmental conditions. Selected fjords allowed to investigate contrasted environmental conditions from low total organic carbon (TOC) content (sediment TOC < 2.7%) in normoxia (bottom-water [O2] > 2 mL O2.L-1) up to high TOC content (> 3.4%) in severe hypoxia (< 0.5 mL O2.L-1). Environmental parameters comprised bottom-water dissolved oxygen, grain size, total organic carbon, total nitrogen (TN), pigments and depth below threshold (DBT). Foraminiferal and macrofaunal community data were significantly correlated (Procrustes analysis m2 = 0.66, p = 0.001). Hence, benthic foraminiferal distribution patterns mirror those of benthic macrofauna. However, as opposed to the foraminifera, macrofauna was not recorded at the most oxygen-depleted stations and, hence, was more sensitive to severe oxygen depletion. With regard to assigning species to ecological groups for ecological quality status assessment, the results suggest that species, e.g. Spiroplectammina biformis (foraminifera), Scalibregma inflatum (macrofauna), may exhibit different ecological requirements depending on their habitat. Considering the observed congruent patterns of benthic foraminifera and macrofauna, palaeo-communities of benthic foraminifera could be used as indicators of reference conditions for benthic macrofaunal community structure. This would however need further developments of algorithms to perform such a translation.

Influence of oyster culture practices and environmental conditions on the ecological status of intertidal mudflats in the Pertuis Charentais (SW France): a multi-index approach.

The ecological quality status (EcoQ) of intertidal mudflats constrained by Pacific oyster farming was assessed by single (H', AMBI, BENTIX and BOPA) and multimetric (M-AMBI and average score) index approaches in the Pertuis Charentais (SW France). Fifteen sampling stations were monitored seasonally for sedimentological features and macrozoobenthos in 2004. Sediments affected by oyster biodeposits showed organic matter enrichment, and sediments from off-bottom culture sites had higher organic matter contents and lower redox potentials than sediments from on-bottom culture sites. Biotic indices consistently registered responses of macrozoobenthos to organic enrichment but there was only partial agreement between single index-derived EcoQs. The average score was better than M-AMBI and single indices for determining EcoQs. Accordingly, oyster farming alters intertidal macrozoobenthic assemblages moderately, and off-bottom cultures cause more disturbance than on-bottom cultures. Hydrodynamics and seasons may interact with culture practices in smothering/strengthening biodeposition-mediated effects through dispersal/accumulation of biodeposits.

Effects of short-term environmental disturbances on living benthic foraminifera during the Pacific oyster summer mortality in the Marennes-Oléron Bay (France).

Sediment cores were collected from April to August 2004 on tidal mudflats of the macrotidal Marennes-Oléron Bay (SW France), famous for the cultivation of Pacific oysters (Crassostrea gigas). The response of living (stained) benthic foraminifera to short-term biogeochemical disturbances in the sediment and overlying water, which may be involved in oyster summer mortality, was monitored. Short-term hypoxia occurred in early June, in conjunction with a sudden rise in temperature. In mid-June, the ammonia content of sediment porewater increased, leading to potentially maximal flux towards overlying waters. Foraminiferal assemblages, particularly in the topmost layer, were altered. Ammonia tepida was the most tolerant to temperature increase and hypoxic conditions whereas Brizalina variabilis and Haynesina germanica were sensitive to organic degradation and hypoxia. Cribroelphidium gunteri was the most opportunistic during recolonisation. Benthic foraminifera showed that short-term biochemical changes in the sediment are toxic and may be involved in the summer mortality of Pacific oysters.