Benthic Foraminifera as Useful Bioindicators of Heavy Metal and Organic Enrichment in Northern Temperate Coastal Zones: A Comprehensive Review Free

Most of the world’s coastal regions are heavily affected by human pressures (Williams et al., 2022). Coastal ecosystems are experiencing rapid physicochemical alterations due to enhanced anthropogenic activities such as unregulated and improper disposal of sewage and solid waste (including heavy metals) (Yang et al., 2007), overuse of fertilizers (Bailey et al., 2020), and emission of toxic and nontoxic gases into the atmosphere (Allegra et al., 2018). These activities contribute to the deterioration of coastal ecosystem health and the loss of marine life, especially in areas where human settlements are dense and widespread. Urbanization, increased land use, and industrialization can lead to severe alteration of the physical and chemical properties of marine environments (Tanaka, Minggat, and Roseli, 2021), thus impacting the persistence of benthic organisms, especially calcifiers like corals and foraminifera (Ciais et al., 2014; Doney et al., 2012; Hoegh-Guldberg et al., 2007; Orr et al., 2005).

Layers of coastal sediments act as a repository for contaminants entering coastal marine systems and can preserve a reliable record of contamination sources (Sawe, Shilla, and Machiwa 2022). This contamination is not always directly evident but can make the sediments toxic for the benthic and epibenthic organisms that spend a large part of their life cycle in or on the sediment. It can lead to toxicity, bioaccumulation, and biological disruptions within the benthic and epibenthic communities (Billah et al., 2022). These effects can manifest as reduced biodiversity, altered community structure, impaired reproduction and development, and even population decline (Billah et al., 2022). Several studies have attempted to evaluate the anthropogenic contribution towards the degradation of the health of the coastal benthic environment through various techniques, by documenting (1) geochemical proxies (e.g., isotopic studies) (Barik et al., 2022; Dasgupta et al., 2018), (2) geophysical properties (e.g., magnetic susceptibility and saturation isothermal remanent magnetization) (Yang et al., 2007), and (3) biomarkers (Vilela et al., 2004). Benthic foraminifera are one such group of organisms that rapidly and faithfully record variations in their surroundings and, as such, can be considered useful bioindicators of anthropogenically induced environmental change. For example, traces of anthropogenic CO₂ and heavy metal concentrations in seawater and sediment can be integrated and preserved in their mineralized tests (Weber and Casazza, 2006). They are useful for monitoring environmental changes, including contamination, biodiversity, climate, and various physicochemical parameters that directly or indirectly affect the state of the marine ecosystem (Boltovskoy, Scott, and Medioli, 1991).

Foraminifera are marine protists that are abundant worldwide (Frontalini and Coccioni, 2011). They have survived multiple mass extinction events since emerging during the Cambrian explosion, around 500 Ma (Culver and Buzas, 1995). Extant species are estimated to number around 10,000 (Pawlowski, Holzmann, and Tyszka, 2013; Vickerman, 1992). They are classified into four subclasses based on the composition of their tests: (1) allogromid (test made of organic materials) (Pawlowski et al., 2002), (2) agglutinated (particles from the surrounding environment agglutinate to form the test) (Bender et al., 1995), (3) siliceous (test composed of silica) (Gupta, 1999), and (4) calcareous (calcium carbonate test) (Gupta, 1999). Calcareous foraminifera are further subdivided into hyaline (porous CaCO₃ test with interlocking microcrystals) and porcelaneous (nonporous CaCO₃ test with randomly arranged rods) forms. According to the World Modern Foraminifera Database (Hayward et al., 2024), the Foraminifera Phylum contains four extant classes: Globothalamea, Monothalamea, Nodosariata, and Tubothalamea.

Foraminiferal tests can be well preserved in sedimentary archives for millions of years (Holbourn et al., 2013) and thus provide an archive that can be used to reconstruct past environmental changes at different timescales. For the recent past, they can be useful to assess the impact of anthropogenic activities, like the emergence of industries on estuarine environments (Cearreta et al., 2000, 2002; Ruiz et al., 2004). They were used for the first time as proxies for contamination in the early 1960s (Alve and Murray, 1995; Boltovskoy, Scott, and Medioli, 1991), and since then, publications focusing on foraminifera as a tool for monitoring coastal contamination have increased substantially (Scott et al., 2005; Yanko, Arnold, and Parker, 1999). Different environmental settings have been the focus of the response of benthic foraminifera to various forms of contamination (Alve, 1995; Culver and Buzas, 1995; Martin, 2000; Murray, 2006; Murray and Alve, 2002; Scott, Medioli, and Schafer, 2007; Yanko, Ahmad, and Kaminski, 1998; Yanko, Kronfeld and Flexer, 1994). These include sewage outfalls (Schafer, 1973), oil spills (Lee et al., 2014), heavy metal inputs (Youssef, 2015), inputs related to paper and pulp mills (Nagy and Alve, 1987), and thermal activities where water is used for cooling purposes in industries or power plants, where the water absorbs heat and is then released back into the environment at a higher temperature (Arieli et al., 2011). This can disrupt the aquatic ecosystem in several ways, such as by reducing oxygen solubility and increasing the incidence of algal blooms (Schafer, 1970, 1973; Xu et al., 2021).

Many characteristics of foraminifera make them powerful environmental bioindicators: a short lifespan and rapid growth, rich diversity and specific autecological preferences, and a small size (∼0.1 mm to 20 mm). They also often have high population density, allowing for statistically significant sample sizes that can be collected quickly and inexpensively for either assemblage assessments or experimental studies, with minimal environmental impact (Desrosiers et al., 2013). In unfavorable environmental conditions or in the context of a disturbance, foraminifera protect themselves through a biological defense mechanism that causes morphological changes, which translate as detectable evidence of stress (Ben-Eliahu et al., 2020; Bergamin et al., 2019; Frontalini and Coccioni, 2008). Living populations and surface sediment assemblages can therefore be used to assess the current state of the benthic ecosystem, while the foraminiferal content of stratified sedimentary accumulations can serve as archives of past environmental conditions. In the paleoenvironmental context, the study of benthic foraminifera morphology, such as pore patterns, test thickness, and proloculus size, offers critical insights into past environmental stressors and bottom water conditions. Recent findings, such as those by Ni et al. (2024), highlight how species like Elphidium clavatum adapted to varying salinity and oxygen levels during the Last Interglacial period. These adaptations, including increased porosity and reduced test thickness under stressful conditions, underscore the utility of foraminiferal morphological features as reliable proxies for reconstructing past environmental changes in brackish and hypoxic marine settings. Such studies enhance our understanding of foraminiferal responses to ecological shifts and contribute to broader paleoclimatic reconstructions.

The objective of this study was to analyze the scientific literature to assess the usefulness of benthic foraminifera as bioindicators of recent anthropogenic heavy metal and organic enrichment in coastal environments of the Northern Hemisphere. To do this, data available from the literature relating to human impacts were reviewed, and a list was compiled of potentially useful indicator species of these types of contamination in various regions that could help to track coastal change.

A literature search was carried out to compile all peer-reviewed journal articles and literature reviews that investigated the role of foraminifera as bioindicators for assessing anthropogenic impacts in northern temperate coastal zones. Two databases were used: Web of Science and Google Scholar, and a time constraint of 1980 to the present was applied with the following keywords: foraminifera, foraminifera as bioindicator, and anthropogenic impact on foraminifera. Three criteria were applied to assess the response of foraminifera to metal and organic enrichment: Studies were considered in which (1) only benthic foraminifera were studied; (2) benthic foraminifera species and either metal or organic contaminants, or both, were studied; and (3) benthic foraminifera showed some visual changes in their morphology or community structure. In total, 106 papers satisfied the above criteria and were included in the analysis. In addition, 33 more articles were included in the study as supporting documents (Figure 1).

Previous review articles were also used to build on the established knowledge base, demonstrating continuity and progression in the research. Additionally, they helped to identify gaps in the existing literature that this work addresses and contextualize the advancements this review brings to the field.

The selected articles were grouped into two categories: (1) heavy metal contamination (containing information about foraminifera responses toward heavy metal contamination, such as habitat, shell size, shell abnormality, and test deformation), and (2) organic contaminants (containing qualitative information about foraminifera responses toward organic contamination such as change in species density, diversity, and morphology). The taxa present in each study, their abundances, and information on morphological changes were compiled.

Data from the selected literature were extracted from the text, with particular attention paid to contaminant types and their effects, which were noted from each article to identify general trends. This information was visualized using a pie chart. To analyze research trends, articles published between 1970 and 2024 were grouped into 10 year intervals and displayed using a bar graph. The locations of the study sites were recorded in an Excel sheet and plotted onto a world map using Adobe Photoshop.

Based on the reviewed literature, this section presents the publication trends, geographical distribution of studies, and the impacts of various contaminants—both metallic and organic—on foraminifera.

Figure 2 illustrates trends in publications within this study subject, focusing on “benthic foraminifera as bioindicators of anthropogenic contamination.” Despite the fact that the impacts of global industrialization on coastal environments started to attract attention in the 1960s (Bandy, Ingle, and Resig, 1964), the selection of 1970 as the base year was strategic, as it allowed easier access to most published material on the subject from that time onwards.

The trend in the number of studies on the topic shows clear growth over the past four decades. Initially, there was a relatively smaller number of studies conducted before 1980 and during the 1980–90 period. However, there was a notable increase in the number of studies and citations between 1990 and 2000. This growth continued, reaching a peak in the period from 2001 to 2010, which had, in this analysis, the highest number of studies. Following this peak, the number of studies saw a slight decrease from 2011 to 2020. The number of citations followed an increasing trend. In the most recent period of 2021 to 2024, the rise is notable, considering it spans only four years and almost equals the numbers from the past decadal interval. Overall, the data suggest a strong and increasing interest in the field since the beginning of the 21st century.

The geographical distribution of the study sites in the papers retained for this analysis is presented in Figure 3. The sites are mostly concentrated around the Mediterranean Sea (including the Adriatic and Black Seas) and the Red Sea. The eastern coast of North America and the East China Sea are also relatively well studied, along with western Europe (especially France and Norway) and northern Baja California. However, wide gaps occur in the geographical coverage of this type of study, especially the west coast of North America and the Far East.

In the article database, studies focusing on metal contamination consistently showed test deformations in foraminifera, highlighting the impact of metal concentrations on their test morphology. In contrast, articles addressing organic and inorganic enrichment emphasized changes in community structure, abundance, and diversity of foraminifera (Figure 4). Notably, only four articles in this latter category (El Hassi and Muftah, 2024; Lei et al., 2015; Melis and Covelli, 2013; Morvan et al., 2004) highlighted test deformations arising from organic contamination.

The following subsections detail the effects of metals commonly found in coastal systems (iron, manganese, copper, zinc, lead, cadmium) on benthic foraminifera, as described in the literature included in the article database.

Iron (Fe) is common in geochemical environments because it is readily available in the continental crust (2–3 wt%) (Gao et al., 1998). Being a major Earth element, it is also essential in the functioning of the marine ecosystem. Aggregates of iron sulfide were found in the species Ammonia tepida from Santa Gilla Lagoon in Sardinia. Distorted tests from the region showed multiple deformities like abnormal chambers and some Siamese twins within the species A. tepida and Haynesina germanica (Frontalini and Coccioni, 2011). In the Naples (Italy) region, Fe enrichment was found in a compositional study on the deformed crystalline reticulum in Miliolinella subrotunda, which led to the suggestion that the species is a useful bioindicator for Fe contamination, as the major pollutants in this region are Fe, Cu, and most importantly Pb. However, the species contained only Fe ions in the crystalline reticulum associated with the development of abnormal specimens (Romano et al., 2008). A study from the Red Sea coast (Youssef, 2015) highlighted that the tests of Sorites marginalis had measured concentrations as high as 10,065 ppm, and Peneroplis planatus had concentrations of 7221 to 8537 ppm Fe. Deformations were observed in both species, such as abnormal and blackened tests in S. marginalis and abnormal growth of the last chamber and protuberances in P. planatus.

Manganese (Mn) mostly coexists with Fe and is transported along with it (Ruiz et al., 2012). In a study of major contaminants in the Nador and El Melah lagoons of North Africa, measured concentrations of Mn in the sediment reached up to ∼5141 ppm and ∼296 ppm, respectively, making them the highest among any metal contaminant in these regions. The species Nonion depressulum and H. germanica were dominant in these regions, indicating that these species are stress tolerant towards Mn (Ruiz et al., 2012). According to Bergin et al. (2006), N. depressulum and A. tepida are bioindicator species of metal contamination in salt lakes of Turkey. They show a positive correlation in abundance with heavy metals, specifically Mn contents, in the Gulf of Izmir. In a study in the south Jeddah area (Saudi Arabia), foraminifera tests of the genera Sorites and Peneroplis were found to be dominant but enriched in Mn (Youssef et al., 2021). These genera therefore are tolerant of high Mn as well as to high Fe concentrations in the Red Sea region.

Copper (Cu) can reach the marine coastal environment through diverse sources such as smelting, mining, industrial activities, algicides, and antifouling paints applied to boat hulls (Frontalini and Coccioni, 2012). In limited amounts, Cu helps in the growth of marine organisms but becomes toxic if it exceeds a threshold value of 120 ppm (Frontalini and Coccioni, 2012). A study by Frontalini and Coccioni (2012) stated that increased concentrations of Cu (higher than 120 µg/L) lead to a decrease in foraminiferal density and diversity and an increased occurrence of test abnormalities. Using inductively coupled plasma mass spectrometry (ICP-MS), Sharifi, Croudace, and Austin in (1991) found that deformed specimens of foraminifera contained a higher concentration of metals, particularly Cu and Zn, than nondeformed specimens from sites in the United Kingdom. Test deformations were mostly due to heavy Cu contamination from oil refineries in Southampton, where they also observed a replacement of Ammonia beccarii by Elphidium excavatum that was correlated with a rise in Cu concentrations. This was further followed by a culture experiment, in which A. beccarii specimens displayed the formation of anomalous chambers during a 12 week incubation period in a culture medium that was enriched with Cu at concentrations ranging from 0.01 to 0.02 ppm (Sharifi, Croudace, and Austin, 1991). Another cultured experiment by Le Cadre and Debenay (2006) highlighted that species of A. beccarii and A. tepida were sensitive to concentrations as low as <10 µg/L but also survived up to the lethal value of concentrations >200 µg/L, although there was detectable evidence of stress (dwarfism, no reproduction, and deformities in the shell) with increasing concentration. A study by Dabbous and Scott (2012) from Halifax, Canada, found that before enhanced treatment, the inner harbor and North West Arm, which were highly polluted, had low abundance and diversity of foraminifera. Noncalcareous species like Eggerella advena, Reophax scottii, Cribrostomoides crassimargo, and Spiroplectammina biformis showed high shell deformities, including dwarfism and aberrant chambers. In contrast, the outer harbor, where waste material was carried to the ocean, had high diversity and abundance, with few deformities, and calcareous species like E. excavatum and Haynesina orbiculara. During treatment, the inner harbor's foraminifera resembled the outer harbor's, showing significant improvement. After treatment stopped, conditions reverted. Pollutants included high concentrations of copper (10,700 kg/y), zinc (36,000 kg/y), lead (34,600 kg/y), and mercury (185 kg/y). In Lake Burullus, Egypt, researchers found that industrial and agricultural waste led to deformities in A. tepida and Cribroelphidium excavatum. Major contaminants in this study included manganese (Mn), copper (Cu), and mercury (Hg), with higher concentrations in deformed specimens, indicating significant contamination effects (El Baz, 2015). Another study by Hoff et al. (2024) on the biogeochemical impact of historical submarine mine tailings in the Repparfjord (northern Norway) provided detailed insights into the changes in benthic foraminiferal communities due to mining activities through the analysis of foraminifer assemblages in a sediment core. Before the disposal of mine tailings, the benthic foraminiferal community included species such as Adercotryma glomeratum, Buccella spp., Lobatula lobatula, and C. excavatum. Following the disposal period, the original community nearly disappeared, and a new community emerged, dominated by stress-tolerant and opportunistic species like Bulimina marginata, Spiroplectammina biformis, Cassidulina jeffreysii, Astronion hamadaense, and Globobulimina turgida. Metal contaminants associated with the mine tailings included copper (Cu), nickel (Ni), zinc (Zn), and lead (Pb). In the western Baltic Sea, elevated concentrations of metals such as copper (Cu), zinc (Zn), tin (Sn), and lead (Pb) have been associated with significant morphological abnormalities in benthic foraminifera (Polovodova and Schönfeld, 2008). Despite the high contamination levels, A. beccarii showed increased abundance yet exhibited signs of stress, including reduced chamber size and excessive chamber development. In contrast, Ammotium cassis was absent from contaminated areas, suggesting that metal pollution created conditions unsuitable for its survival (Polovodova and Schönfeld, 2008). A study on foraminifera test chemistry from two distinct locations in the Red Sea, Egypt (El-Esh and Quseir Harbor), found lower concentrations of Cu in A. beccarii (0.32 ppm, El-Esh) than in Operculinella cumingii (∼86.7 ppm, Quseir Harbor) (Mansour, Nawar, and Madkour, 2005). Cu content measured in foraminiferal tests from Abu-Shaar (Red Sea coast, Egypt) varied between 9.6 and 36.4 ppm in species of the genera Sorites and Spiroloculina (Madkour and Ali, 2009). This shows that the bioaccumulation of Cu can differ between genera from the same location, highlighting variable tolerances. A study undertaken in Nador Lagoon (Morocco) reported Cu content >400 mg/kg, along with zinc (>1000 mg/kg) and lead (>400 mg/kg), in sediments collected near an old iron mine that had an assemblage dominated by Nonion depressulum, suggesting that this species is a bioindicator of heavy metal contamination (Ruiz et al., 2012).

Zinc (Zn) is an essential trace element in all living systems (Merian and Clarkson, 1991). It is coprecipitated with calcium carbonate and substitutes calcium (Ca) to form isomorphous zinc carbonate (Merian and Clarkson, 1991). The major anthropogenic sources of zinc in coastal environments are from agricultural wastes, pesticides, antifouling paints, zinc sulfate (from pesticides), air conditioning ducts, garbage cans, galvanized pipes, batteries, and automobile tires (Merian and Clarkson, 1991). In experimental studies by Kubisch et al. (2017), A. beccarii, E. excavatum, and H. germanica showed increased deformities and reduced density at lead (Pb) concentrations of 20–100 µg/g, cadmium (Cd) levels of 0.3–3 µg/g, and zinc (Zn) concentrations of 50–200 µg/g. In Baltimore Harbor, Maryland (USA), increased Zn concentrations (200–250 μg/g) resulted in the disappearance of Ammobaculites crassus, which was previously flourishing (Ellison, Broome, and Ogilvie, 1986). In Sapelo Island, Georgia (USA), exposure to Cd, Pb, and Zn decreased foraminiferal abundance, species richness, and evenness. Haynesina germanica and A. tepida showed significant abnormalities under Zn exposure, with A. tepida displaying enlarged apertures and aberrant calcification (Smith and Goldstein, 2021). A study from Ria de Aveiro, Portugal, highlighted the finding that A. tepida, E. excavatum, and Spiroloculina lobata tolerated high levels of heavy metals like zinc, copper, and mercury. Conversely, Quinqueloculina seminula and Bolivina ordinaria showed reduced abundances in contaminated areas, highlighting their sensitivity to these metals (Martins et al., 2015). In Boulogne-sur-Mer (France), high Zn enrichment factor (EF_Zn = 7) and Pb (EF_Pb = 5) concentrations resulted in deformities and reduced species diversity in foraminifera like C. excavatum and H. germanica, while opportunistic species like Cribroelphidium gunteri were flourishing (Francescangeli et al., 2016). In Goro Lagoon (Italy), Zn, along with chromium, nickel, and lead, caused deformities in Ammonia perlucida and Q. seminula, while Cribroelphidium translucens was found to be zinc tolerant (Coccioni, 2000). In Santa Gilla Lagoon (Italy), a negative correlation was observed between Rosalina globularis abundance and Cd, Pb, Zn, and Cr concentrations, indicating sensitivity to metals (Frontalini et al., 2009). In Venice Lagoon, significant trace metal contamination, including Zn (35.0–463.7 mg/kg), Pb (0.18–4.28 mg/kg), and Hg (0.2–2.3 mg/kg), led to deformities in A. beccarii and H. germanica (Frontalini et al., 2009). In the Gulf of Milazzo (Sicily), contamination from Zn (12.56–167.35 mg/kg) and Pb (4.79–49.19 mg/kg) impacted Ammonia spp. and Nonion spp., causing test deformities and disappearance of miliolids (an order of foraminifera with calcareous, porcelaneous tests that are imperforate and commonly have a pseudochitinous lining) in highly polluted areas (Cosentino et al., 2013). A study by Dimiza et al. (2022) from Saronikos Gulf (Greece) highlighted that A. tepida faced significant stress from Cu (20–100 µg/g), resulting in reduced density and increased deformities. Pb (50–150 µg/g) caused high mortality rates and abnormalities in Bulimina elongata and B. marginata. Zn (100–300 µg/g) decreased Nonionella turgida abundance and increased deformities. Yümün and Önce-Nişancioğlu (2023) found that in the Sea of Marmara, significant deformities in foraminifera like Ammonia compacta and Anomalinoides rubiginosus were caused by heavy metals, particularly Pb, Zn, Cu, As, and Mn. Pb levels often exceeded safe limits, and Zn ranged from 68 to 78 ppm. In Quseir, Safaga, and Hurghada Harbors (Egypt), Zn concentrations in foraminiferal tests were higher than in molluscan shells, suggesting greater sensitivity in foraminifera (Mansour, Nawar, and Madkour, 2005). In Norway, faunal shifts due to Zn and Pb contamination were observed, with Verneuilina media dominant in moderately polluted environments and Eggerelloides scabrous dominant in extremely polluted layers (Alve, 1991a). An experimental study on Heterostegina depressa revealed negative impacts of sunscreen containing ZnO on their growth (Lintner et al., 2022).

The high lead (Pb) concentrations in the coastal environment are attributable to several sources such as boat exhaust systems, oil spills, other petroleum compounds, and sewage effluent discharge into the water (Laxen, 1983). Some species of foraminifera, including H. germanica, M. subrotunda, and Q. parvula, have been observed to be tolerant to high Pb concentrations (Bergamin et al., 2003). An experimental study by Schmidt et al. (2022) investigated the incorporation of heavy metals into the calcite tests of A. aomoriensis, Ammonia batava, and E. excavatum, and it revealed strong positive correlations between these species and Pb. Another experimental study highlighted that Astrammina rara experienced significant shell deformations when exposed to Pb, resulting in fragile, “moth-eaten” shells, indicating more pronounced detrimental effects of Pb compared to cadmium (Cd) (Andreas and Bowser, 2023). In a study by Kubisch et al. (2017), species such as A. beccarii, E. excavatum, and H. germanica were analyzed. The research found that A. beccarii showed increased deformities and reduced density at Pb concentrations of 20–100 µg/g. In Naples (Italy), the strong statistical correlation between E. advena deformations and Pb concentrations indicates that deformation represents the response of this species to high Pb contamination (255 mg/kg). This deformation seems to be caused by a temporal perturbation that involves the construction of one single chamber, and no foreign elements are included in the crystalline framework contamination (Romano et al., 2008). A study from the central Adriatic Sea coast of Italy reported that species like Ammonia parkinsoniana, A. tepida, Aubignyna perlucida, Eggerella scabra, and No. turgida showed increased deformities and reduced population densities in response to Pb contamination, with concentrations between 40 and 100 µg/g (Frontalini and Coccioni, 2008). In the Gulf of Palermo (Italy), A. parkinsoniana and Asterigerinata mamilla were noted as sensitive species against Pb contamination as their abundance decreased with increasing Pb concentration. Moreover, morphological abnormalities, including twin specimens and abnormal chambers, were also noted in species such as L. lobatula, Gavelinopsis praegeri, and Quinqueloculina limbata, with Pb concentrations ranging from 11.6 to 60.2 mg/kg (Di Leonardo et al., 2009). Madkour and Ali (2009) compared Pb concentrations in foraminifera and mollusks in Egypt's Quseir, Safaga, Hurghada, and El-Esh regions. They found that foraminifera showed a greater affinity for Pb, either binding or absorbing it more readily than other elements, making them better indicators of Pb contamination than mollusks in these areas. In Abu-Qir Bay, Alexandria (Egypt), A. beccarii displayed significant test deformities and reduced population density in areas with high concentrations of Pb and Cd, and Bolivina striatula experienced high mortality rates and severe morphological changes in response to increased Pb contamination (Elshanawany et al., 2011). A study in the western Baltic Sea by Polovodova and Schönfeld (2008) revealed that A. beccarii exhibited the highest frequency of abnormalities, including aberrant chamber shapes and additional chambers, which were strongly correlated with high concentrations of Pb, An, Cu, and Sn, particularly in industrial areas with Pb levels up to 2169 mg/kg. A study in Liaodong Bay, China, highlighted the significant impact of heavy metals on benthic foraminiferal communities, with Elphidium subincertum and Rotalinoides compressiuscula showing a negative correlation with lead (Pb), indicating lower species diversity and richness in areas with elevated Pb concentrations (Guo et al., 2020). In Yangpu Bay, Hainan Island, China, benthic foraminifera, particularly A. beccarii and E. excavatum, exhibited several types of morphological deformities due to high Pb concentrations ranging from 2 to 100 mg/kg. These deformities included abnormal chamber shapes, reduced test size, and irregular growth patterns (Zhang et al., 2023).

Cadmium (Cd) abundances in the marine environment range from 0.1 to 0.3 ppm (Kabata and Pendias, 1984). The anthropogenic sources of this metal in the marine ecosystem may include the discharge of refining wastes and untreated sewage effluents. The U.S. Environmental Protection Agency (EPA) lists Cd as one of 129 priority pollutants and lists it among the 25 hazardous substances (Kabata and Pendias, 1984). Cd is incorporated into the foraminiferal test as a substitute for Ca (Marchitto, Curry, and Oppo, 2000). In a comparative study between the Seine Estuary and the Authie Estuary in France, industrial contamination, particularly from heavy metals such as Cd, significantly affected foraminiferal communities. The polluted areas in the Seine Estuary showed a higher proportion of A. tepida and a lower overall density and species richness compared to the relatively unpolluted Authie Estuary, indicating the sensitivity of the foraminiferal communities to Cd contamination (du Châtelet and Debenay, 2010). In Naples Harbor (Italy), the tests of A. tepida were extremely enriched in Cd (up to 150.00 ppm) due to anthropogenic inputs and showed a positive correlation of deformations with Cd concentrations (Rumolo et al., 2009). In the Bay of Koper, NE Adriatic Sea, the impact of heavy metals, including Cd, on benthic foraminifera was investigated by Žvab Rožič et al. (2022). Key affected species included A. parkinsoniana, A. tepida, Haynesina depressula, and Elphidium sp. The study found reduced species diversity and richness in areas with higher concentrations of Cd, highlighting the utility of benthic foraminifera as bioindicators for monitoring heavy metal contamination and assessing ecological health in marine environments. In the Black Sea, key species studied included A. beccarii, E. excavatum, and B. marginata. Heavy metal contaminants like Cd (up to 50 µg/g) caused deformities, such as abnormal chamber shapes, reduced test sizes, and irregular growth patterns, leading to increased mortality (Yanko, 2022). In the Gulf of Aqaba (Red Sea), the highest concentration of Cd (1.2 ppm) was found in the tests of the species P. planatus, but no test deformations were reported to co-occur with this concentration (Youssef et al., 2021). In the Oujiang Estuary (China), Zhao et al. (2024) examined the impact of heavy metals on benthic foraminiferal communities. Key findings showed that genera such as Alveolinella, Nummulites, Parasorites, Globorotalia, and Calcarina exhibited a significantly negative correlation with Cd, indicating their sensitivity to this contaminant. Table 1 provides a comprehensive summary of the effects of various metals on foraminifera, highlighting both detrimental and, in some cases, neutral or positive impacts.

Morphological variations are a common phenomenon seen in foraminiferal tests, arising due to environmental stressors, including natural and anthropogenic metal enrichment (Culver and Buzas, 1995), physical (pH, temperature, salinity) (Bergin et al., 2006) and chemical (ion flux) parameters (Frontalini and Coccioni, 2012), and competition for resources and nutrition (Bergin et al., 2006; Ruiz et al., 2012). In 1991, Boltovskoy, Scott, and Medioli observed that the connection between contamination and foraminifera is complicated, not just due to the diverse nature of pollutants but also because their impacts on different species vary significantly (Boltovskoy, Scott, and Medioli, 1991). Yanko, Ahmad, and Kaminski (1998) observed that abnormal specimens contained higher concentrations of Cu and Zn than nondeformed specimens. This result pointed to heavy metal content as a more probable cause of deformity than other causes. The species A. beccarii, P. planatus, Sorites variabilis, and Adelosina pulchella showed abnormalities due to Zn contamination in two bays in Egypt, and it was also observed that tests with twisted or abnormal growth were exposed to higher heavy metal contamination than those showing protuberances (Samir and El-Din, 2001). In another study at south Jeddah, Youssef et al. (2021) found specimens of P. planatus with abnormal growth of the last chamber, protuberances, and the last chamber divided into branches. The abnormalities in foraminiferal tests at sites on the Red Sea coast included abnormal growth of the last formed chamber, protuberances, branched last chamber, and abnormal test shape. Some species displayed a double aperture, a sign of pathological morphogenesis (Youssef, 2015). In addition to morphological deformation, results from the Ghannouch-Gabes area also demonstrated a relationship between low density and diversity towards increasing pollutant concentrations (Ayadi et al., 2016). According to Sharifi, Croudace, and Austin (1991), there are four modes of abnormalities: (1) Siamese twins (Stouff, Debenay, and Lesourd, 1999), (2) reduced chamber size (Alve, 1995; Jayaraju, Sundara Raja Reddy, and Reddy, 2008; Wade and Olsson, 2009), (3) aberrant chambers (Hallock et al., 1995), and (4) distorted chamber arrangement or change in coiling (Ernst et al., 2006).

El-Kahawy et al. (2018) found that deformed specimens, such as those with reduced chamber size, contained an elevated concentration of heavy metals. Their study illustrated that signs of environmental contamination may be well maintained in the foraminiferal tests of some species. It was concluded in the study that Amphisorus hemprichii displayed a high affinity to iron incorporation in its test structure. The Pb concentration in the deformed foraminiferal tests was exceedingly high compared to the normal tests of the same species, whereas deformed Amphistegina lobifera had a high concentration of Mg in their tests. In another study, Samir and El-Din (2001) pointed out that tests with twisted, compressed, and abnormal growth were characterized by higher values of heavy metals than forms with protuberances. In Table 2, we highlight some common abnormalities found in foraminifera tests due to anthropogenic contamination (Martinez-Colon, Hallock, and Green-Ruiz, 2009). Figure 5 shows examples of normal and deformed foraminifera observed in the surface sediments from the Bay of Sept-Îles (Québec, Canada), a high-use deep-water mineral port. Deformities include Siamese twinning in Eggerella sp., protuberances in Elphidium sp., and a deformed outer shell in Cornuspira sp.

The responses of benthic foraminifera assemblages to organic contamination have been assessed through several ways, such as long-term monitoring of species assemblages, and the study of sediment cores, sediment flux, and changes in abundance and diversity of foraminifera. Based on this study of the existing literature, it appears that organic contamination is not associated with test deformities in foraminifera, but rather it is associated with changes in assemblage structure and abundance.

Recent studies showed that the visible effects of pH in seawater are species-specific, with hyaline and porcelaneous foraminifera showing higher abundances at higher pH values. In contrast, agglutinated taxa are more abundant at lower pH values, whereas calcareous forms are the first to show test deformities under lower pH (<7.5). These relationships could be used to infer seawater pH changes in ecological investigations (Dong et al., 2020). Another study highlighted that a change in pH can cause deformities as the tests begin to dissolve when pH is below 7.8 (Alve and Nagy, 1990) and begin to regenerate when the pH returns to normal, which appear as deformities (Le Cadre, Debenay, and Lesourd, 2003). This potential reaction to pH in foraminifera is particularly relevant in the current context of ocean acidification due to its absorbance of excess atmospheric CO₂. Foraminifera could therefore be used as bioindicators of acidification in various regions.

In Louisiana (USA), a study by Brunner et al. (2013) focused on marsh foraminifera, particularly Balticammina pseudomacrescens and Ammobaculites spp., revealing various deformities like reversals in coiling and misshapen chambers. These deformities were linked to oil contamination from the 2010 Macondo blowout, with Total Polycyclic Aromatic Hydrocarbons (TPAH) concentrations between 5000 and 18,000 mg/g in heavily oiled sites. Deformed, dead foraminifera were found exclusively in heavily oiled cores, suggesting lethality. Lightly oiled sites showed population booms, indicating ecological disturbances. Another study from coastal California (USA) reached a similar conclusion, finding that benthic foraminiferal species replaced those that were present ∼30 years before in the sewage outfall shelf of Los Angeles. A heap of agglutinated shells was dominant in the death assemblage below the sewage field, whereas the living population of today is dominated by calcareous forms (Bandy, Ingle, and Resig, 1964; Scott et al., 1996). Increased nutrient flux from the 1960s to 1990s in south Florida resulted in a shift in foraminifera growth cycles from long-lived algal symbiont-bearing to small, fast-growing heterotrophic taxa (Cockey, Hallock, and Lidz, 1996). A relationship between a switch in foraminifera assemblage composition and input of agricultural and urban waste was observed in the Bay of Biscayne (near Miami, Florida, USA), where the population of symbiont-bearing taxa declined, whereas some species of Ammonia flourished (Carnahan et al., 2009).

In Canada, in a seminal work by Clark (1971), an intriguing phenomenon came to light: the elevated prevalence of Eg. advena in the eastern sector of Clam Bay, Nova Scotia, as opposed to its western counterpart. The low nutrient levels in the western part of the bay may have accounted for the low population size of this species in that area. The swift change in the overall sample percentage could indicate that Eg. advena is a species with high nutrient demands. Clark’s study suggests that the localized nutrient enrichment resulting from the aquaculture operations was a key driving force behind the observed variations in species abundance between the two regions of the bay. Schafer (1973) highlighted that the Elphidium clavatum group took prominence within the living fauna found near sewage outfalls in Chaleur Bay, eastern Canada. The group thus displayed an impressive capacity to establish and sustain its presence in nearshore sediment substrates in acidic pH conditions (where levels were reduced to 6.4).

A study by Ernst et al. (2006) focused on species such as A. beccarii, Bo. ordinaria, and B. marginata. The addition of organic matter initially increased foraminiferal density due to more food availability but then led to declines as oxygen levels dropped. Oxygen depletion caused high mortality in Bolivina ordinaria and reduced reproduction in A. beccarii. Metal contamination (Pb and Cd) worsened these effects, causing further declines and morphological abnormalities like abnormal chamber shapes and reduced shell size. Bouchet et al. (2023) reviewed the impact of different types of plastics on benthic foraminifera and found significant adverse effects. Polystyrene nanoparticles at a concentration of 1 mg/L induced oxidative stress in A. parkinsoniana, promoting the accumulation of neutral lipids and enhancing the production of reactive oxygen species. Exposure to polyethylene microparticles at a concentration of 1 particle/mL altered the feeding strategies of Amphistegina gibbosa, causing it to rely more on autotrophy. Additionally, Rosalina bradyi, Textularia bocki, and L. lobatula were found to colonize polyethylene plastic bags, leading to the accumulation of protein beta-sheets in these species, which is indicative of oxidative stress. These findings highlight the detrimental effects of plastic contamination on the physiology and behavior of benthic foraminifera, underscoring the need for more research in this area.

To comprehend the impact of the Erika fuel spill, the oil spill incident involving the sinking of the oil tanker Erika off the coast of France in 1999, which spilled 31,000 tons of fuel, controlled laboratory cultures of foraminifera were carried out by Morvan et al. (2004), where 5.5 mg per 100 mL of oil revealed morphological anomalies, cellular alterations, and a reduced reproduction rate in A. tepida. The field study conducted in the affected region of Vendée showed poor development and lower faunal densities. Another experimental study carried out on oil contamination for the same affected area revealed increased mortality of H. germanica, whereas 4 weeks after the spill, there was a rise in the population of Ammonia and Textularia spp., concluding that there was a dual response by the foraminiferal species (Ernst et al., 2006).

An experimental study on nicotine’s effect on foraminifera species revealed that nicotine contamination in foraminifera causes shell decalcification. Accumulated nicotine adversely affects foraminifera shell development, causing structural abnormalities and shell weakening (Sabbatini et al., 2023). This result could be relevant in certain coastal areas in the context where there is runoff affected by cigarette manufacturing or where tobacco is cultivated (WHO, 2017).

Oron et al. (2021) conducted geochemical analysis on the shells of benthic foraminifera, specifically, at a former fish farm site. The analysis revealed that the concentrations of copper (Cu), zinc (Zn), and phosphorus (P) were significantly high in the 3 years following the removal of fish cages, with a notable reduction over time. However, even 10 years post removal, the Cu/Ca levels were still more than four times higher than the background levels. This study highlights that benthic foraminifera can serve as effective monitors of bioavailable contaminants in seawater and underscores the need for long-term heavy metal monitoring around marine aquaculture facilities due to the prolonged environmental impact observed.

In France, Bouchet et al. (2020) observed significant impacts on sensitive species of benthic foraminifera due to the salmon farming activities in the Rade de Cherbourg. Sensitive species such as Discorbis vilardeboanus, Cribroelphidium magellanicum, and Bolivina pseudoplicata showed a marked decrease in abundance under the salmon cages compared to areas outside the farm. The primary pollutant, organic matter from salmon farming, led to anoxic conditions in the sediments, adversely affecting these sensitive species. In contrast, tolerant species like B. variabilis and Quinqueloculina stelligera became more dominant under the cages. This shift indicates that the increased organic matter from fish farming activities has a detrimental effect on sensitive foraminiferal species, leading to a reduction in ecological quality in the impacted areas. Debenay et al. (2000) examined the impact of various pollutants on benthic foraminifera in the Adour Estuary (France). This estuary is significantly influenced by freshwater input and contamination from marina activities, a fish farm, and a slaughterhouse. The research highlighted that the species Miliammina fusca, along with other foraminifera exhibiting abnormal tests, were predominantly found in polluted areas. Additionally, larger foraminifera were observed near outfalls from the fish farm and slaughterhouse, likely due to the higher availability of organic matter. That study underscores the sensitivity of foraminiferal assemblages to contamination and their potential as bioindicators in estuarine environments. Another study focused on the impact of boat activities, cleaning, painting, oil, motor-fuel oil, and motor fuel outfall on benthic foraminifera in Port Joinville Harbor, Yeu Island (France), found that C. excavatum and H. germanica were significantly affected by these contaminants. Cribroelphidium excavatum showed increased abundances in polluted areas, indicating its tolerance to oil and motor-fuel outfall, and suggesting its resilience to hydrocarbon contamination (Debenay et al., 2001). Similarly, H. germanica was also found in higher densities in areas affected by boat activities and associated pollutants, reflecting its tolerance to contamination from cleaning and painting activities, oil, and motor-fuel outfall. These findings highlight the potential of these species as effective bioindicators for assessing the ecological impact of boat-related activities and hydrocarbon contamination in coastal environments. The study by Debenay et al. (1997) found that bolivinids and Cribroelphidium excavatum were significantly impacted by marina and fishing dock activities in La Turballe, Loire Atlantique (France). Both species showed increased abundance in polluted areas, indicating their tolerance to contaminants from these activities. This highlights their potential use as bioindicators for monitoring environmental impact in coastal regions.

Sediment cores from Drammens and Frier Fjords (Norway) revealed long-term accumulation of organic waste (e.g., paper pulp, domestic sewage) that caused a shift from an oxic to an anoxic benthic environment. This change was accompanied by a change from a diverse assemblage of calcareous species to agglutinated species, and finally to afaunal conditions in the top 3 cm of the core (Alve, 1991b), corresponding to the current anoxic conditions.

In Libya, a study conducted on the Susa coast in northeast Libya revealed significant environmental implications due to pollutants such as sewage, desalination plant wastewater discharge, and oil accumulation in which the most affected benthic foraminiferal species included Amphistegina lessonii, Textularia bocki, and Peneroplis pertusus, which exhibited various abnormalities. These abnormalities included double apertures, reduced chamber sizes, extra chambers, complex forms, enlarged and deformed apertures, aberrant chamber shapes, twinned forms, loose miliolid coiling, wrong coiling, twisted tests, and corroded tests. The findings also indicated low to moderate species density, low species diversity, and frequent occurrences of abnormal specimens, reflecting the adverse effects of contamination on the coastal ecosystem (El Hassi and Muftah, 2024). Similarly, excessive organic carbon in the surface sediments of Elefsis Bay (Greece) created a challenging habitat for benthic foraminifera. The stressed environment is suggested by low-diversity faunas, featuring stress-tolerant species such as A. tepida, B. elongata, B. marginata, and No. turgida (Dimiza et al., 2022). Discharges of asphalt and natural gases in Zakynthos Island (Greece) were monitored at six submarine stations (1040 m deep), and it was observed that calcareous benthic foraminifera (e.g., Elphidium, Cibicides, Quinqueloculina, and Ammonia) were abundant at all sites, whereas agglutinated forms were completely absent. This suggests that the agglutinated tests were either dissolved, or they could not live at all in the contaminated environment. However, it is uncertain whether agglutinated taxa exist in unpolluted shallow waters near Zakynthos Island because they were not mentioned in the earlier article by Dermitzakis and Alafousou (1987).

A study conducted in the coastal regions of Israel concluded that benthic foraminifera (e.g., A. tepida) are sensitive to organic matter overload, oxygen stress, and anoxia, and they were only present at shallower depths (Hyams-Kaphzan et al., 2009). In the coastal region near the Hadera power plant in Israel, thermal contamination is the primary concern, with discharged seawater raising local temperatures by up to 10°C. This significantly impacts benthic foraminiferal communities, reducing species richness and diversity. Sensitive species like Textularia agglutinans, Tretomphalus bulloides, and Rosalina globularis showed marked declines, while tolerant species such as Lachlanella sp. 1, Lachlanella sp. 2, and Pararotalia spinigera persisted. Morphological abnormalities, especially in species like L. lobatula and Planorbulina mediterranensis, were also observed near the discharge site, highlighting the adverse effects of elevated sea temperatures and trace element contamination (Arieli et al., 2011). The study focused on the effects of brine discharge from desalination plants on benthic foraminifera along the Mediterranean coast of Israel, particularly in Ashkelon, Hadera, and Sorek. These facilities discharge brine with a salinity of about 80, which is twice the normal seawater level. In Ashkelon and Hadera, the discharge is associated with thermal contamination from nearby power plants, raising local sea temperatures by 0.5–5°C and 1–2°C, respectively. Elevated concentrations of trace elements such as chromium (Cr) and manganese (Mn) were also observed, particularly at the Sorek outfall. The brine discharge significantly impacted benthic foraminiferal communities, with sensitive species like Spiroplectammina sp. and Eggerelloides advenus showing a sharp decline, especially at the Sorek discharge site. Tolerant species such as A. parkinsoniana, A. beccarii, and A. tepida exhibited higher relative abundances near the outfalls at Ashkelon and Hadera. Overall, species richness and abundance were generally lower near the outfalls and increased towards the control stations, with the lowest numerical abundance and species richness found at Ashkelon and higher values at the deeper Sorek site. This study highlights the need for careful monitoring and management of desalination brine discharge to mitigate its adverse effects on marine ecosystems (Kenigsberg, Abramovich, and Hyams-Kaphzan, 2020). In the Persian Gulf, Parsaian, Shokri, and Pazooki, (2018) examined benthic foraminifera in two northern Persian Gulf reefs, revealing contrasting impacts of aquaculture and industrial sewage on the foraminifera assemblages. The reef subjected to industrial sewage featured a low-diversity assemblage dominated by the stress-tolerant species Quinqueloculina sp. and larger symbiont-bearing Amphistegina sp. In contrast, the reef subjected to aquaculture sewage displayed common occurrences of opportunistic species Ammonia sp. and Elphidium sp. In Kuwait, rapid urbanization and industrialization have degraded water and sediment quality in Kuwait Bay. Geochemical and statistical analyses pinpoint the Sulaibikhat Bay and Ras Kazmah areas as the most impacted. Environmental stress, including organic, metal, and hydrocarbon contaminations, is linked to significant changes in morphological and molecular data sets. In Kuwait Bay, Ammonia spp. largely dominate the rotaliids, reflecting the opportunistic behavior of this genus common in coastal environments (Al-Enezi et al., 2022). Table 3 highlights the impact of organic contaminants, such as Agricultural and domestic effluent, pisciculture, sewage, etc, on foraminifera.

This review highlights the responses of benthic foraminifera to metal and organic contamination in northern temperate coastal zones, focusing on using them as a proxy to infer ecosystem disturbance. By analyzing the literature, this study determined that metal contamination induces higher chances of deformations in foraminiferal tests, whereas organic contamination mostly affects abundance and species assemblages of foraminiferal communities. Very limited studies included in this review show that organic contamination (eutrophication and oil spills) can lead to abnormal test growths, moreover, no metal concentration was studied in conjunction with the organic contamination in these studies, which leaves the possibility that the deformations could be the result of undetected metal concentrations. There appears to have been a rise in the number of published morphological studies of foraminifera in the past few years, which could have been influenced by advances in technology, particularly in the fields of cytology and genetics (Ishitani et al., 2023; Lattanzi et al., 2024), which directed researchers to explore new methodologies and tools for studying foraminifera. These methods might contribute to better and more detailed insights into the biological and genetic aspects of these organisms. However, studies that include various approaches should be favored whenever possible to maximize insights into the variations in morphology and assemblage structure. This review supports the statement that foraminifera constitute a useful tool to improve current understanding of the effects of metal and organic contamination on the benthic coastal environment.

In the Northern Hemisphere, studies on the effects of heavy metals on foraminifera in the Mediterranean regions and Red Sea are the most abundant followed by the eastern coast of North America. Reasons for this could include the following:

The Red Sea coast and Mediterranean are almost enclosed by land, resulting in limited tidal interactions with the open oceans. This characteristic can contribute to the preservation of coastal change evidence in their mostly undisturbed sediments, making them attractive study areas.

Scientific research is often driven by specific research questions and priorities. Foraminiferal research efforts tend to focus on areas with perceived needs or significant environmental and ecological concerns. The ecological significance and unique environmental conditions in the Red Sea coast and Mediterranean may have led to greater attention in these regions.

Limited availability of comprehensive data sets can pose challenges to research. Incomplete or scarce databases can impede research efforts. The lack of available data may discourage researchers from directing their studies to these areas.

This distribution highlights the necessity for a more balanced global research approach to address the diverse and interconnected issues affecting marine environments worldwide. Future studies should aim to fill the existing gaps, particularly in underrepresented regions like the North American West Coast, to provide a more holistic understanding of marine ecological health and resilience. A few reports on water and sediment quality and industrialization have highlighted contamination in the eastern Canadian Maritimes (Bernatchez and Dubois, 2004; Comité ZIP Côte-Nord du Golfe, 2013); however, no major studies on foraminifera in the eastern coast region have been conducted in the last decade.

Concerns arise from the enrichment of zinc, cadmium, lead, and iron in marine and coastal environments within the Northern Hemisphere, posing substantial threats to ecosystem health. Remarkably, certain foraminiferal species, including S. marginalis, A. tepida, and M. subrotunda, exhibit a remarkable ability to thrive in iron-contaminated environments, suggesting their potential as stress indicators for iron contamination. Highlighting the specificity of foraminiferal responses to particular metal pollutants, species like A. beccarii and E. excavatum emerge as reliable indicators for copper contamination. In environments with escalating copper contamination, the survival of A. beccarii diminishes, gradually replaced by E. excavatum. This species-specific responsiveness underscores the significance of foraminifera in evaluating and monitoring metal contamination levels. An inverse relationship has been inferred to exist between sediment heavy metal concentrations and foraminiferal abundance and diversity, while a direct correlation is observed between the prevalence of deformed tests and heavy metal levels (Sen Gupta et al., 2003).

The responses of benthic foraminifera assemblages to organic contamination, as reviewed across multiple studies, indicate that organic contamination primarily impacts the species structure and abundance of these assemblages rather than causing test deformities. Studies have shown that the presence of organic pollutants often leads to a decrease in species diversity and shifts in dominant species, favoring those that can tolerate higher levels of contamination. For example, species such as Eg. advena and A. tepida have been observed to thrive in nutrient-rich and contaminated environments, while more sensitive species decline. This shift in assemblage composition is often accompanied by changes in population dynamics, such as population booms in lightly polluted areas and high mortality rates in heavily contaminated sites. Furthermore, the impact of specific types of organic contaminants, such as those from oil spills, agricultural runoff, and aquaculture operations, has been documented to cause significant ecological disturbances. For instance, oil contamination from the Macondo blowout led to deformities and lethality in foraminifera in Louisiana marshes, while increased organic matter from salmon farming in France caused anoxic conditions detrimental to sensitive species. Studies also highlight the role of foraminifera as bioindicators of environmental health, with their responses to contaminants providing valuable insights into the ecological impacts of pollution. The findings underscore the need for continued monitoring and management of organic contamination to mitigate its adverse effects on marine ecosystems.

This review focused on the morphological characteristics of benthic foraminiferal assemblages to assess their responses to environmental stressors. Although foraminifera are known to be sensitive to changes in their environment and various contaminants, their specific reactions to different stress factors are not fully understood. Many studies utilize proxies like water and sediment chemistry to evaluate the impact of pollutants on foraminiferal communities and morphology. However, such correlations alone may not reliably identify the precise causes behind observed morphological changes, nor do they confirm whether these abnormalities are harmful to the organisms. While morphology-based taxonomy remains a preferred method for studying foraminiferal composition and diversity, alternative approaches, like metabarcoding, are emerging. These newer techniques have been effectively applied to understand the influence of human activities on benthic foraminiferal communities, including the impacts of fish farms (He et al., 2019; Pawlowski et al., 2014) and industrial pollutants (Al-Enezi et al., 2022). Laboratory experiments using controlled environments, such as micro- and mesocosms, have further investigated the ecotoxicological effects of pollutants like heavy metals, persistent organic pollutants, and oil (Ernst et al., 2006). These experiments could provide insights into the consequences of test deformities on reproduction or feeding in foraminifera, addressing questions such as whether such abnormalities affect their survival or functionality. As these effects continue to be explored, standardized protocols, such as those developed by the FOBIMO (Foraminiferal BIo-Monitoring) initiative (Schönfeld et al., 2012) and Foram-AMBI (Foraminiferal AZTI Marine Biotic Index) (Alve et al., 2016), could enhance research consistency and comparability. Incorporating both morphology-centered approaches and emerging molecular techniques could ultimately offer a more holistic understanding of foraminiferal responses to environmental stressors, facilitating the development of effective sediment quality guidelines.

This review highlights the physiological responses in foraminifera to contaminants and their promise as reliable early indicators of environmental stress caused by heavy metal and organic contamination in temperate coastal environments. To improve the usefulness of foraminifera as bioindicators of anthropogenic pressure in these environments, it is essential to increase quantitative physiological measurements and establish better-defined standard exposure protocols. By expanding research efforts, data collection, and collaboration, a more comprehensive understanding of foraminiferal responses to contamination and their ecological implications in benthic nearshore zones can be achieved. These efforts will contribute to a more comprehensive understanding of the role of benthic foraminifera as bioindicators of metal and organic concentrations and their potential use for assessing environmental health.

Grateful acknowledgment is extended to Bibliothèque Université Laval for providing access to otherwise inaccessible manuscripts and books. N.J. expresses appreciation to Étienne Masson and other lab mates for their unwavering support throughout this research journey. N.J. was supported by a scholarship from the EcoZone Research Chair, a partnership between Université Laval, Institut nordique de recherche en environnement et en santé au travail (INREST), and the Port of Sept-Îles.

An executive summary of this research was originally published in Joshi, Arya, and Saulnier-Talbot (2024).