Morphological deformities in benthic foraminiferal assemblages from shallow marine and lagoonal environments of the western Arabian Gulf

To assess the impact of environmental stressors on ecosystems, selecting the organisms to target is a crucial step (Holt & Miller, 2011). Given the ever-increasing threat of climate change to marine environments, a careful choice of marine communities becomes important from a multidisciplinary standpoint (Kaiho, 2022; Pinsky et al., 2022). Foraminifera serve as valuable environmental monitoring tools due to their ability to secrete shells that are preserved in the fossil record, and their relatively rapid responses to various stressors (Frontalini & Coccioni, 2011; Sabbatini et al., 2014; Martins et al., 2019). Originally employed as index fossils for dating sedimentary rocks (Grzybowski, 1898; Cushman, 1928), modern and fossil foraminiferal assemblages are versatile, providing insight not only into ambient environmental conditions (Sen Gupta, 2003; Murray, 2006), but also acting as proxies for paleotemperature, paleoproductivity, oxygenation, and sea level fluctuations (Herguera & Berger, 1991; Kaiho, 1994; Kaminski, 2012; Groeneveld & Filipsson, 2013; Jennings, 2015; Kaminski et al., 2018; Lane et al., 2023). Moreover, they hold promise for future projections, enabling predictions of their geographical range expansion in response to environmental changes (Langer et al., 2013; Merkado et al., 2013; Weinmann et al., 2013; Kenigsberg et al., 2019; Briguglio & Kaminski, 2023) and their ability to endure extreme conditions that are predicted for future decades (Titelboim et al., 2016, 2019; Pinko et al., 2020).

Benthic foraminiferal assemblages, in particular, possess diverse strategies to respond to intraspecific stressors. These organisms can respond to both natural and anthropogenic stressors through community-level structural and compositional modifications (Murray, 2006; Jones, 2014). Responses include changes in diversity patterns (Hess et al., 2001), proliferation of opportunistic species (Hart et al., 2022), gradual responses to mass mortality events (Hess et al., 2001; Hikmahtiar et al., 2022), and the display of varying degrees of test abnormalities (Yanko et al., 1998; Geslin, 2000). For the last aspect particularly, understanding the dominant triggering factors and controls of test-structure alteration in foraminifera poses a significant challenge. Even in relatively natural or undisturbed environments, these organisms can exhibit certain morphological anomalies (Boltovskoy et al., 1991; Martins et al., 2019; Geslin et al., 2000, 2002), for example associated with breakage and repair (e.g., Röttger & Hallock, 1982; Geslin et al., 2000; Souder et al., 2010). Moreover, under extreme hypersaline conditions, the occurrence of morphological deformities in foraminifera is more frequent and varied (Geslin et al., 2002; Consorti et al., 2020; Fiorini & Lokier, 2020).

A number of studies have investigated the impact of environmental perturbations on living organisms, particularly foraminifera, through controlled experiments using culture-based specimens exposed to natural and anthropogenic stressors. While various experiments have been conducted, foraminifera have mainly been subjected to chemical pollutants such as trace elements and organic matter (Saraswat et al., 2004; Barras et al., 2018; Frontalini et al., 2018; Price et al., 2019). Other studies have explored the effects of natural stressors, particularly salinity-induced conditions, on foraminiferal morphology test deformation. For instance, Stouff et al. (1999) observed that hyaline-test species of Ammonia tepida raised under high salinity conditions exhibited morphological deformities in later stages at a rate of 50%, compared to only 1% in individuals under normal conditions. Similarly, when Charrieau et al. (2018) reduced salinity to levels lower than normal sea water (hyposaline), decalcification and aberrant test specimens of Ammonia and Elphidium crispum were observed. These findings provided valuable insight into how environmental stressors can impact the morphology of foraminifera, demonstrating their sensitivity and response to changes in their surroundings.

In the Arabian Gulf, a wide range of environmental conditions, including both naturally undisturbed areas and highly polluted regions, coexist and significantly influence the benthic communities, particularly foraminifera (Sheppard et al., 1992; Price et al., 1993; Sheppard et al., 2010). Despite characterization of the Gulf as five zones based on the benthic foraminiferal assemblages by Amao et al. (2022), the western side remains insufficiently studied in terms of foraminiferal populations and their adaptations to extreme environments characterized by high temperature and salinity. Future climate projections suggest a further increase in temperature, and the expansion of desalinization plants along the coastline will lead to even more hypersaline conditions by the middle of the 21^st century (Pal & Eltahir, 2016; Paparella et al., 2022; Safieddine et al., 2022), particularly in intertidal and shallow waters and lagoonal areas. Therefore, this study aims to explore the diversity of foraminifera as well as the extent of morphological deformities that may arise in response to hypersalinity at locations with different salinity conditions, in these supposedly natural (unpolluted) environments.

Eight locations were initially selected to represent areas with different ranges of hypersalinity. These prospective locations included six subtidal and lagoonal areas in Eastern Saudi Arabia and two subtidal areas in Bahrain. The selection criteria were based on the relatively pristine state, as those areas were situated far from anthropogenic activity and previous studies supported this characterization (Arslan et al., 2016a, 2017). To make comparisons, we included another pristine locality in Saudi Arabia with similar conditions, but with a lack of previous research on foraminifera. Sediment samples were collected at a water depth of approximately 1 m, about 50–100 m offshore from the low-tide mark, in the early winter period of late December 2022. The choice of sampling localities was also influenced by additional remarks by Amao et al. (2022), which highlighted the need for further exploration in these regions. As the final consideration, we selected six of these localities as the main sampling targets for this study (Fig. 1). Sampling was conducted at fore-shore localities in eastern Bahrain (EBH-FS), in Half Moon Bay (HMB-FS), and at Al-Uqayr Beach (AUQ-FS) in Saudi Arabia, and in the three ponds comprising the lagoonal system at Al-Uqayr (AUQ-P1, AUQ-P2, and AUQ-P3).

Surficial sediments, comprising the top 1 cm of the sea floor and representing recently accumulated materials, were sampled directly using glass sample jars with dimensions of 5 cm in diameter and 10 cm in height. For each sample, we used a 30:70 ratio of sediment to water in the jars. Two sets of sediment samples were collected to serve different purposes: unstained samples were gathered to estimate relative diversity and occurrence of deformities in larger benthic foraminifera (LBF), while a second set of samples was collected from each locality and stained to assess total and living benthic foraminiferal diversity. Samples were stained with rose Bengal in a 70% ethanol mixture and left to stain for two weeks, without duplicate or triplicate samples due to the sampling limitation in the region. Additional untreated (unstained) sediment samples and water samples were also collected for grain size, trace element, and organic-carbon analyses. Subsequently, the samples were transferred to the Micropaleontology Laboratory of King Fahd University of Petroleum & Minerals for further analysis and investigation.

To determine the ecological status of our sampling locations, we conducted both field and laboratory measurements of the physical and chemical characteristics of water and sediment. Using a multiparameter probe (Hanna HI98194), we measured pH, salinity (in PSU and/or mS/cm), and temperature (in °C) in the field at the time of sampling.

Using freshly collected sediment samples, we performed trace-element and organic-carbon analyses to assess the natural conditions. A weight of 0.25 grams of the sediment sample was initially dried at 30°C for 24 hours, followed by digestion in 10 ml of nitric acid and dilution with deionized water to 100 ml as per the EPA 3050 method (Amao et al., 2018). We assessed trace-element concentrations including manganese (Mn), chromium (Cr), copper (Cu), nickel (Ni), arsenic (As), lead (Pb), cadmium (Cd), zinc (Zn), and mercury (Hg) using Thermo Fisher iCAP RQ ICP-MS (Inductively Coupled Plasma Mass Spectrometer).

We also quantified total organic carbon (TOC) content using the Elementar soli TOC cube TOC ANALYZER and followed modified versions of DIN19539 protocols for the analysis. Approximately 25 mg of dried sediments were analyzed in porcelain cups, with two replicates for each sample to account for possible errors. As a quality control measure, we also analyzed similar amounts of calcium carbonate (CaCO₃) and glucose to establish baseline values. The organic carbon constituents were obtained by subjecting the materials to elevated temperatures with a 200°C difference.

Additionally, we analyzed grain-size distributions using the HELOS Particle Size Analysis. One mg of unwashed wet material was poured into the apparatus, and various datasets, such as cumulative distribution and distribution density, were obtained to characterize our samples.

As noted above, sediment samples for analyses of foraminiferal assemblages were processed in two ways, unstained samples for total LBF and stained samples for all taxa collected, including those collected live (stained). For LBF, sediments were washed with flowing water through a 63-μm sieve to remove fine particles. After air-drying for a day, approximately 50 grams of dried sediment were weighed from each sample. To ensure unbiased representation, the sediment material was split into aliquots using a Micropress Europe microsplitter, and dry-sieved on a 125-μm screen to remove juveniles. Approximately 300 specimens of only LBF were then picked from sufficient sediment materials within the smallest possible split. From this set of samples, we calculated the bulk abundance of LBF for each gram of sand-sized sediment (>125 μm), as well as the percentage of LBF exhibiting deformities from each locality.

For the stained samples, similar washing and preparation methods were followed, but for a longer duration to ensure sufficient removal of the rose Bengal stain. Similarly, around 300 specimens were picked from subsamples after aliquot partitioning, but in this case, all benthic foraminifera (larger and smaller benthic foraminifera/SBF) were picked from the materials. From this sample set, we utilized the foraminiferal data to compare between live and dead assemblages, normal-appearing and deformed specimens, as well as to calculate diversity indices.

From both sets of picked foraminiferal materials, stained and unstained specimens were taxonomically identified. References used included the monograph of Loeblich & Tappan (1994), digital library (Horton et al., 2017), and previously published materials from neighboring areas (Murray, 1970; Cherif et al., 1997; Amao, 2016; Amao et al., 2016, 2018; Arslan et al., 2016a,b; Kaminski et al., 2020; Hayward et al., 2021). The specimens were categorized as normal or deformed-test specimens, and living and dead assemblages were distinguished from the stained materials, considering the ratio between live-dead assemblages and possible lethality induced by deformities. For species identification, representative specimens were selected for scanning electron microscopy imaging using a GEOL 7000 Desktop SEM. The utilized materials are currently housed in the Micropaleontology Laboratory at KFUPM. Illustrated specimens will be permanently archived at the European Micropalaeontological Reference Centre in Kraków. Poland.

We evaluated the foraminiferal assemblages based on abundances and various indices. These indices encompassed relative abundance for each taxon, species richness (S), dominance (D), the Shannon-Wiener index (H’), evenness e^H/S, and Fisher-alpha calculated using the software PAST v4.03 (Hammer et al., 2001).

The field data acquired from six localities indicated hypersaline environments and relatively normal pH levels. In open marine areas like EBH-FS, salinity was above that of normal seawater (40 PSU) but below that of other localities (<50 PSU) such as in the HMB-FS at 60.1 PSU and AUQ-P3 at 68.5 PSU. The pH levels across the sampling sites remained consistently >8, ranging from 8.2–8.5. The temperature dataset reflected relatively cool winter conditions, ranging from 22–25°C across the sampling localities.

Physical and chemical parameters from each locality are summarized in Table 1. Trace-element results show very low to undetectable levels or below detected limit (BDL) at certain locations. The concentrations of listed elements did not exceed the limits set by international standards (Pazi, 2011; Sharifuzzaman et al., 2016; Onjefu et al., 2020). For instance, lead (Pb) in marine sediments has an acceptable limit of 40 ppm, while all our samples contain <2 ppm. Only two samples showed slightly higher levels for the nickel (Ni) and arsenic (As) constituents, but not for all trace elements. Organic constituents (TOC) were also found to be low, with values ranging from 0.16–1.79%. Grain-size analysis indicated predominantly fine to medium sand-size range (3–1 Φ; >63 µm based on Wentworth, 1922), representing sand-sized particles for 90% to 95% of the total composition.

From six unstained samples focusing on LBF, three of the six contained sufficient material (at least 300 specimens within the smallest possible split from the collected sediment sample) for further analysis: HMB-FS, EBH-FS, and AUQ-P1. The remaining samples contained too few LBF, even from the entire sample. Peneroplis and Monalysidium were present in most samples, with sporadic occurrences of Coscinospira and Sorites. Six LBF species were identified based on SEM observation: Peneroplis pertusus, P. planatus, P. arietinus, Coscinospira hemprichii, Monalysidium aciculare, and Sorites orbiculus (Table 2). Abundance varied, with 200 specimens/gram in HMB-FS, 100 specimens/gram in AUQ-P1, and 663 specimens/gram in EBH-FS. Relative abundances by genus are presented in Table 3 and SEM images of the species are provided in Figure 2. Broken and intact carapaces of ostracods and mollusks were also observed, notably bivalve and gastropods characteristic of hypersaline environments such as the mud creeper (Pirenella) and a salinity-tolerant ostracod (Cyprideis), but their investigation is beyond the scope of this study.

From the six stained samples, both LBF and SBF specimens were identified, with members of three orders present: Miliolida, Rotaliida, and Textulariida. More than 30 species were identified at each locality based on morphological distinctions, with some taxonomic assignments limited to the genus level. The EBH-FS locality exhibited the highest species richness, with 74 species, while AUQ-P2 had the lowest with 32 species. EBH-FS had the highest number of specimens (773 specimens/g), and AUQ-P2 had the lowest (32 specimens/g). AUQ-P1 had the highest dominance (D), EBH-FS had the highest Shannon Index (H’), HMB-FS had the highest evenness (e^H/S), and EBH-FS had the highest Fisher α Index (Table 4). Species listed in Table 5 represent all benthic foraminiferal species from each location, in raw quantity or counts and percentage. Scanning electron microscope images of representative species are presented in Figures 3 and 4.

Based on the rose Bengal-stained samples, the living fauna at each locality comprised more than a quarter of the total picked specimens. The ranked living abundances at the genus level, from highest to lowest, were as follows: Peneroplis, Triloculina, Quinqueloculina, Ammonia, Miliolinella, Elphidium, Monalysidium, and Coscinospira. Comparing living and dead assemblages found that proportions overall were quite similar, with only the Peneroplis “living” mean notably lower than the mean for the dead specimens counted. Coscinospira was not found in samples from AUQ-P2, AUQ-P3, and HMB-FS ( Appendix 1).

For the morphological deformity occurrences, overall LBF exhibited a higher proportion of morphological deformities (>40%) compared to SBF across the salinity gradient (Table 6 for summary, Appendices 2–3 for raw counts). Peneroplis accounted for most of the deformed percentage among LBF specimens (Appendices 2–3), followed by Coscinospira and Monalysidium (Figs. 5, 6). For SBF (Figs. 7, 8), Ammonia exhibited the greatest number of morphological deformities, followed by Elphidium, both comprising from 25% and up to above 75% of the total genus-level assemblages. Fewer morphological deformities were observed in the Miliolidea (Quinqueloculina, Triloculina, Spiroloculina, Agglutinella, Pseudotriloculina, Miliolinella), comprising ∼25 − 30% of the total individuals in their genera at lower hypersaline conditions, then gradually increasing to >50% at higher salinity >60 PSU ( Appendix 3). The percentage of morphological deformities in the assemblages significantly increased with salinity at the sample sites (Fig. 9).

We found multiple types of morphological deformities, varying from mild to severe. Typical mild deformities (i.e., deformities that do not totally alter specimen appearance) such as multiple changes in chamber size, apertural modifications, and the presence of attached epibionts. Severe deformities include bizarre developments that make it difficult to determine the species. Such deformities include twinning, constrictions, coiling-plane modifications, a highly trochospiral appearance in the genus Ammonia, bifurcation, and multiple morphological deformities within a single specimen. Around 50% of deformed specimens were found in adult forms, especially for the LBF that developed abnormalities at later stages such as in flaring stages in Peneroplis and uncoiling stages in Coscinospira and Monalysidium. Fewer than 10% of juvenile stages displayed abnormalities and most of those deformities were mild. Among SBF specimens such as Ammonia, Elphidium, Quinqueloculina, Triloculina, Pseudotriloculina, and Miliolinella; the occurrences of deformities were mostly considered to be mild, were mostly observed on the final chamber, and were rarely found in the early stages of test development.

The western Arabian Gulf, particularly the eastern side of Saudi Arabia and Bahrain, experiences extreme fluctuations in temperature and salinity, especially during the summer (Kaminski et al., 2021, 2023; Amao et al., 2022). During our winter sampling session in December 2022, temperatures <25°C were recorded, while salinity values as high as 68.5 PSU were observed at one locality, indicating highly hypersaline conditions. Additionally, in-situ temperature monitoring over the last three years from summer 2020 to winter 2023 by Kaminski et al. (2023) revealed sea-surface temperatures exceeding 35°C in the offshore, with field measurements indicating substrate temperatures above 50°C in the intertidal zone. Inhabitants of such environments, especially foraminifera, may respond to extreme conditions in several possible ways, including tolerating the high temperatures (Schmidt et al., 2016; Prazeres et al., 2017), increasing reproduction to cope with the challenges (Schönfeld & Numberger, 2007; Amao et al., 2018), or possibly entering dormancy phases (Ross & Hallock, 2016).

In a previous study of foraminifera from the hypersaline Gulf of Salwa, Amao et al. (2018) suggested that increased salinity might be the primary trigger for deformities, given the limited influence of other anthropogenic factors such as trace elements and petroleum hydrocarbons. However, the sampling site had fairly uniform salinity values. In contrast, our study includes several localities in close proximity to one another but with quite different salinity conditions.

Most studies of morphological deformities in foraminifera have focused on the potential effect of anthropogenic pollution, although natural factors like salinity changes (rapid or seasonal) and hydrodynamic (high energy and rapid sedimentation environment) influences may also contribute to deformities, albeit to a lesser extent (Hallock et al., 1995; Toler & Hallock, 1998; Yanko et al., 1998; Geslin et al., 2000, 2002; Sen Gupta et al., 2003; Frontalini & Coccioni, 2011). Furthermore, morphological deformities are not a recent or modern issue, as fossil records of foraminifera also exhibit deformities in the absence of human or anthropogenic influence (Coccioni & Luciani, 2006; Ferràndez-Cañadell et al., 2014; Antonarakou et al., 2018), which makes understanding how morphological deformities occur in natural or naturally stressed environments an intriguing research pursuit.

The sampling sites in the western Arabian Gulf, including Half Moon Bay and Al-Uqayr in Saudi Arabia, and East Bahrain Foreshore, lie in foreshore or shallow-water lagoonal settings with a maximum depth of no more than 10 m (Amao et al., 2022). These sites are considered relatively pristine locations with low human influence, as defined by Murray (2006). This region is naturally stressed by high salinities and temperatures especially during the summer, and some areas have been identified by Kaminski et al. (2021, 2023) as a potential “kill zones,” particularly in intertidal areas and ephemeral lagoons. Additionally, several studies also consider the seasonal north wind (the Shammal Wind) that can generate strong waves and disrupt the bottom sediment (Aboobacker et al., 2021; Langodan et al., 2023), adding additional stress on the environment for benthic animals living in the shallow waters of the Arabian Gulf.

The sediment composition at the sampling sites consists mainly of sand-sized particles, comprising the dominant fraction (95–99%). This composition suggests that the sediment is locally transported from nearby sources, such as sand dunes or aeolian deposits, which are predominantly siliciclastic materials (Arslan et al., 2016a). Amao et al. (2018) previously reported that western Arabian Gulf localities are mostly characterized by sand-sized materials, with hard grounds formed from lithified bioclastic materials due to seasonal exposure to high temperature and oversaturated saline water (Weijermars, 1999). Unlike what Amao et al. (2018) reported in the Gulf of Salwa, fragments of other calcifying invertebrates, such as mollusks (bivalves and gastropods) and ostracod carapaces that are found in the hypersaline benthic communities, also contribute to the sediment composition based on our sampled sediments and the composition of bioclastic hardgrounds.

Based on the analysis of trace elements and organic constituents, very low to undetectable levels of contaminants were found at all the sampled localities, which is consistent with the findings of Arslan et al. (2017) and Amao et al. (2018), indicating minimal human influence. Another possible explanation for the low occurrence of anthropogenic constituents is the dominance of sandy sediment, as most of the aforementioned constituents are normally adsorbed into finer sediment like mud (Rao et al., 2008; Martins et al., 2011).

The three sites sampled for LBF are dominated by one genus of Peneroplis, with smaller proportions of Monalysidium, Coscinospira, and Sorites. These taxa vary in proportion as salinity increases and in semi-restricted environments (Murray, 1970; Clarke & Keij, 1973; Amao et al., 2018; Fiorini & Lokier, 2020). These genera, characterized by porcelaneous tests, thrive in hypersaline waters, while LBF with hyaline tests prefer normal salinity conditions (Murray, 2006). The LBF were abundant at three localities that have a direct connection to the Arabian Gulf, with the exception of the AUQ-FS site. Similarly, LBF were more abundant at sites that are in direct proximity of the Arabian Gulf (e.g., EBH-FS), compared to more restricted areas like sites AUQ-P2 and AUQ-P3, in addition to HMB-FS and AUQ-P1.

In the total assemblages, comprising both SBF and LBF, miliolids dominated, reflecting their ecological adaptations to high salinity, such as that found in the Arabian Gulf (Murray, 2006; Amao et al., 2022). No significant relationship was observed between the relative abundances of benthic foraminifera with organic and inorganic pollution from the nearby sampling sites in the western Arabian Gulf (Arslan et al., 2017). Abundances of LBF were higher in more open marine areas (samples with the FS = foreshore code), and gradually declined with distance from open-marine influx, for example, in the AUQ P2 and P3 samples from the lagoons at Al-Uqayr, except in the AUQ-P1. Similar findings from the fossil record of hypersaline environments from the Miocene Dam Formation (Chan et al., 2017) represent an ancient analogue of the modern Arabian Gulf.

Regarding the morphological deformities, these mostly appear in the adult forms of LBF (in the uncoiled parts of Coscinospira and Monalysidium, flared portion in Peneroplis) compared with the juvenile forms (planispiral part). This observation aligns with the findings of Clarke & Keij (1973) and Fiorini & Lokier (2020), which indicated that most of the adult stages show aberrant tests with severe cases, suggesting that these morphological abnormalities may result from external stressors later in life. Some of our juvenile LBF specimens exhibited slight deformities, but not as substantial or complex as in adult specimens (Figs. 5, 6). Additionally, some deformed specimens were found in our stained samples, indicating that the deformities are not lethal. Similar cases have been observed in environments with high levels of pollution or other stressors where aberrant tests occur but are not lethal (e.g., Yanko et al., 1994, 1998; Toler & Hallock, 1998; Geslin et al., 2002; Pati & Patra, 2012; Amao et al., 2018). Experimental studies involving culture specimens subjected to trace elements have also shown that morphological deformities do not prove to be lethal (Stouff et al., 1999; Nigam et al., 2009; de Nooijer et al., 2007; Saraswat et al., 2015; Price et al., 2019). Based on our findings indicating low levels of anthropogenic stressors, the most likely cause of abnormalities is related to the elevated hypersaline conditions observed in the restricted water bodies of the Gulf.

Salinity plays a crucial role in calcification and elemental incorporation, such as magnesium and calcium, for building foraminiferal tests (Dissard et al., 2010; Charrieau et al., 2018; Geerken et al., 2018). A related factor in the development of aberrant tests is the seasonal change in salinity. During the normal summer season, the western Arabian Gulf can experience salinity levels in excess of 60 PSU, which then decreases during the winter period to around 50–55 PSU (a difference of 5–10 PSU) at some sites, particularly in restricted lagoons (Joydas et al., 2015, 2023). Benthic foraminifera prefer more stable or normal conditions for reproduction, with preferable temperatures and salinity, or they will remain in adult form while growing in size, as captured in fossil records during environmentally stressed conditions with unusual temperatures in the late Paleocene and early to mid-Eocene, or during the Late Paleocene Thermal Maximum (Boudagher-Fadel, 2008; Speijer et al., 2012; Schmidt et al., 2018; Hallock & Seddighi, 2022). Nevertheless, the benthic foraminifera are capable of reproducing under stressed conditions such as during a thermal stress experiment (Titelboim et al., 2021), albeit in a reduced capacity. The occurrence of deformed tests mainly in the adult form and rarely in the juvenile form suggests that these specimens were produced during environmentally favorable conditions, and subsequent salinity changes caused abnormalities in their growth, which is in agreement with the culture experiment by Stouff et al. (1999) on Ammonia.

In addition to the potential salinity-based factor that induces morphological deformities, the shallow-water and intertidal environments in our study area also possesses another potential deformity inducer. Apart from the high sand fraction composition revealed by our grain size analysis and the siliciclastic nature of the substrate observed by Arslan et al. (2016a), amplified by strong winter winds that disrupt sediment settlement in the shallow waters of the Gulf (Langodan et al., 2023); the weak shell configuration of miliolids, which dominate the assemblages in our study area, means that mechanical abrasion can easily damage them or break them apart (Briguglio & Hohenegger, 2011). Although post-mortem abrasion or damage to the outer shell of benthic foraminifera due to hydrodynamic action (Kotler et al., 1992; Walker & Goldstein, 1999; Hohenegger, 2009) is more obvious compared to damage induced by dissolution due to ocean acidification (Haynert et al., 2014; Prazeres et al., 2015), benthic foraminifera can survive such high-energy environments after encountering breakage and continue to grow. However, their newly developed chambers or shell portions start from the damaged part. Therefore, abnormal development, distinct from the previously developed chamber arrangement, is quite obvious (Wetmore, 1987; Hallock et al., 1995; Toler & Hallock, 1998). Several potential examples from among our foraminiferal specimens exhibiting such deformities are shown for Monalysidium aciculare (Fig. 5, specimen 9) and Peneroplis planatus (Fig. 5, specimen 20), as well as for Peneroplis pertusus (Fig. 6, specimen 4) and Coscinospira hemprichii (Fig. 6, specimen 11).

Regarding both possibilities on whether our observed morphological deformities are induced by salinity constraints or hydrodynamic conditions, there is currently no clear evidence to conclusively prove either argument, or both can certainly play a role. On the one hand, there are few consistent records that measure the seasonality of salinity throughout the year, with sporadic reports indicating increasing salinity levels in the Arabian Gulf since the late 20^th century, possibly due to the increasing volume of brine discharge from desalination plants (Campos et al., 2020; Paparella et al., 2022), and how this affects the meiofaunal ecology in the system. On the other hand, while several studies have mentioned the extensive impact of waves on benthic communities in the Arabian Gulf (Barth & Khan, 2008; Riegl & Purkis, 2012), there are no reports explaining whether the hydrodynamic conditions specifically disrupt the living conditions of the benthic foraminifera. Therefore, further experimental work with culture-based specimens under controlled laboratory conditions is required to adequately test these hypotheses.

In this study, we assessed benthic foraminiferal assemblages at six western Arabian Gulf localities considered to represent pristine but naturally stressed environments, including quantifying the occurrences of morphological deformities in the foraminifera. Our sample sites covered a range of salinity levels above normal for the region (>40 PSU), and exhibited little or no human disturbance, as shown by low levels of pollutants. The species diversity at the selected localities was relatively high, with an average species richness of ∼49 and diversity indices ∼3. Both living and dead assemblages were dominated by Miliolida, notably the genera Peneroplis, Coscinospira, and Monalysidium that host algal endosymbionts. The smaller Miliolida genera Quinqueloculina and Triloculina were especially common in the foreshore and less restricted areas, while Rotaliida genera such as Ammonia and Elphidium, along with smaller miliolids, were more common in restricted environments. Morphological abnormalities were frequently observed in the LBF specimens (as high >40%) and rarely found in juveniles, with less complexity in abnormalities observed among the SBF. The low levels of anthropogenic pollutants (trace elements and organic content) suggest there is no causal relationship with abnormalities in foraminiferal tests, which demonstrate that deformities occur naturally at the unpolluted localities in the western Arabian Gulf. Therefore, we conclude that abnormally high salinity, either in terms of absolute values or seasonally dependent changes, are major factors in the development of morphological deformities. An additional factor that cannot be ignored in the shallow-water and intertidal environment affected by hydrodynamic processes is wave action, which can potentially induce breakage and repair deformities in the benthic foraminifera living in the sandy substrate. Further sampling across the study area, as well as future experimental studies based on cultured specimens from the area, will be necessary to confirm these observations and the roles of the assumed morphological deformity inducers.

We are grateful to the Deanship of Scientific Research, King Fahd University of Petroleum and Minerals, for funding the current research through Project DF191042. We thank Dr. Abduljamiu O. Amao for reading an early draft of the paper. We appreciate the constructive feedback and comments from the Editor-in-Chief of the journal, Dr. Marci Robinson, the Associate Editor, Prof. Pamela Hallock, and the reviewers of this study, Prof. Antonino Briguglio, and anonymous reviewers. The Appendices can be found linked to the online version of this article.

Appendix 1. Live (stained) specimens from the stained samples from each locality (both LBF and SBF) in raw counts and % of living specimens of each species.

Appendix 2. Total assemblages for each locality in the current studies for unstained samples (LBF only) in raw count and % for morphological deformity case.

Appendix 3. Morphological deformities (raw count and %) found in total assemblages for each locality in the current studies for stained samples (all forms, LBF and SBF).