Morphological Deformities in Benthic Foraminiferal Assemblages from Shallow Marine and Lagoonal Environments of the Western Arabian Gulf

(1)

MORPHOLOGICAL DEFORMITIES IN BENTHIC FORAMINIFERAL ASSEMBLAGES FROM SHALLOW MARINE AND LAGOONAL ENVIRONMENTS

OF THE WESTERN ARABIAN GULF

S

INATRYA

D. P

RAYUDI

, B

ASSAM

S. T

AWABINI

, A

SMAA

K

ORIN

,

AND

M

ICHAEL

A. K

AMINSKI

*

Geoscience Department, College of Petroleum Engineering and Geoscience, King Fahd University of Petroleum and Minerals, PO Box 5070, Dhahran, 31261, Saudi Arabia

ABSTRACT

This study examines larger and smaller benthic forami- niferal assemblages at six localities from western Arabian Gulf, documenting their diversity, abundance, and mor- phological deformities across a salinity gradient. Both unstained and stained samples were used to quantify spe- cies diversity, percent of deformities, and bulk quantity at each site. These samples revealed that 109 species were present and approximately one-quarter of specimens were alive during the sampling period. We observed different morphological deformities with various degrees of severity and an increasing overall percentage of deformities across a salinity gradient from 40 to 68.5 PSU (averaging . 40%).

Environmental analysis of marine sediment revealed no dangerous levels of anthropogenic stressors, such as trace metals or organic pollutants. Therefore, morphological deformities in the benthic foraminifera are likely salinity- induced (owing to a salinity gradient or seasonal change), as deformities are primarily observed in the adult specimens.

INTRODUCTION

To assess the impact of environmental stressors on ecosys- tems, 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 (Fron- talini & Coccioni, 2011; Sabbatini et al., 2014; Martins et al., 2019). Originally employed as index fossils for dating sedi- mentary 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 pale- otemperature, paleoproductivity, oxygenation, and sea level ﬂ uctuations (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 intraspeci fi c stressors. These organisms can respond to both natural and anthropogenic stressors through community-level structural and composi- tional modi fi cations (Murray, 2006; Jones, 2014). Responses include changes in diversity patterns (Hess et al., 2001), prolif- eration of opportunistic species (Hart et al., 2022), gradual responses to mass mortality events (Hess et al., 2001; Hikmah- tiar 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 signi fi cant 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; Bar- ras 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 Char- rieau et al. (2018) reduced salinity to levels lower than normal sea water (hyposaline), decalci ﬁ cation and aberrant test specimens of Ammonia and Elphidium crispum were observed.

These ﬁ ndings provided valuable insight into how environ- mental 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 signi fi cantly in fl uence the benthic communities, particularly foraminifera (Sheppard et al., 1992; Price et al., 1993; Sheppard et al., 2010). Despite characterization of the Gulf as fi ve zones based on the benthic foraminiferal assemblages by Amao et al. (2022), the western

* Correspondence author. E-mail:[email protected]

(2)

side remains insuf ﬁ ciently 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 desali- nization 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; Sa ﬁ eddine et al., 2022), partic- ularly in intertidal and shallow waters and lagoonal areas. There- fore, 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 condi- tions, in these supposedly natural (unpolluted) environments.

MATERIALS AND METHODS L

OCALITY

S

ELECTION

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 crite- ria 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 in ﬂ uenced by additional remarks by Amao et al.

(2022), which highlighted the need for further exploration in these regions. As the ﬁ nal 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).

S

EDIMENT

S

AMPLING

Sur ﬁ cial sediments, comprising the top 1 cm of the sea ﬂ oor and representing recently accumulated materials, were sam- pled 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 sedi- ment 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.

P

HYSIO

-

CHEMICAL

A

NALYSIS

To determine the ecological status of our sampling loca- tions, we conducted both ﬁ eld and laboratory measurements of the physical and chemical characteristics of water and sedi- ment. Using a multiparameter probe (Hanna HI98194), we measured pH, salinity (in PSU and/or mS/cm), and tempera- ture (in °C) in the ﬁ eld 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 quanti ﬁ ed total organic carbon (TOC) content using the Elementar soli TOC cube TOC ANALYZER and followed modi ﬁ ed 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 (CaCO

3

) 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.

F

ORAMINIFERA

S

AMPLE

P

REPARATION

, S

UBSAMPLING AND

I

DENTIFICATION

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 fl owing water through a 63- l m sieve to remove fi ne 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- l m screen to remove juveniles. Approximately 300 specimens of only LBF were then picked from suf fi cient 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 l m), 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

suf ﬁ cient removal of the rose Bengal stain. Similarly, around

300 specimens were picked from subsamples after aliquot par-

titioning, but in this case, all benthic foraminifera (larger and

smaller benthic foraminifera/SBF) were picked from the mate-

rials. From this sample set, we utilized the foraminiferal data

(3)

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 identi ﬁ ed. References used included the monograph of Loeblich & Tappan (1994), digital library (Horton et al., 2017), and previously published materials from neighbor- ing 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 deformi- ties. For species identi ﬁ cation, 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 Refer- ence Centre in Kraków. Poland.

FIGURE1. Location of the study area and sampling sites.

(4)

D

ATA

A

NALYSIS

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).

RESULTS

E

NVIRONMENTAL

Q

UALITY

A

SSESSMENT OF

S

AMPLED

L

OCALITIES

The ﬁ eld 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 data- set re ﬂ ected 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; Sharifuzza- man 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 ﬁ ne to medium sand-size range (3 – 1 U ; . 63 m m based on Wentworth, 1922), representing sand-sized particles for 90% to 95% of the total composition.

B

^ENTHIC

F

ORAMINIFERAL

D

IVERSITY

From six unstained samples focusing on LBF, three of the six contained suf ﬁ cient 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 identi ﬁ ed 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-toler- ant ostracod (Cyprideis), but their investigation is beyond the scope of this study.

From the six stained samples, both LBF and SBF specimens were identi ﬁ ed, with members of three orders present: Milio- lida, Rotaliida, and Textulariida. More than 30 species were identi ﬁ ed at each locality based on morphological distinctions,

TABLE1. Physical and chemical parameters from each locality based onﬁeld and laboratory analysis. Trace element limits based on several global references such as EPA and WHO and regional references, summarized by Pazi (2011), Sharifuzzaman et al. (2016) and Onjefu et al. (2020). BDL5Below Detection Limit.

Parameters Unit Limit HMB-FS EBH-FS AUQ-FS AUQ-P1 AUQ-P2 AUQ-P3

Temperature (seawater) °C - 22.50 22.10 21.70 20.80 20.50 20.10

Salinity (seawater) PSU - 60.01 44.50 53.50 58.44 64.48 67.11

pH (seawater) - - 8.12 8.32 8.28 8.26 8.25 8.23

TOC (sediments) % - 1.79 0.91 1.64 0.36 0.16 0.23

Mn (sediments) ppm 300 30.61 26.77 44.96 35.72 47.02 41.82

Cr (sediments) ppm 25 9.99 18.33 16.34 12.00 23.05 16.15

Cu (sediments) ppm 25 1.82 3.12 2.55 2.24 2.65 2.29

Ni (sediments) ppm 20 18.09 14.42 21.97 17.14 25.24 17.71

As (sediments) ppm 3 3.64 1.02 3.50 2.27 1.47 1.25

Pb (sediments) ppm 40 1.07 1.42 1.32 1.54 1.42 1.08

Cd (sediments) ppm 6 1.89 0.61 BDL BDL BDL BDL

Zn (sediments) ppm 90 16.84 11.45 13.50 12.66 15.68 7.64

Hg (sediments) ppm - 0.70 1.00 0.13 0.37 3.19 0.18

TABLE2. Total assemblages of LBF from unstained materials in each locality which contain sufﬁcient materials within (around 300 specimens).

Species

HMB–FS EBH–FS AUQ–P1

Count % Count % Count %

Coscinospira hemprichii(Ehrenberg, 1839) 0 0.00 108 41.70 49 15.65

Monalysidium aciculare(Batsch, 1791) 25 7.79 9 3.47 46 14.70

Peneroplis arietinus(Batsch, 1791) 1 0.31 1 0.39 2 0.64

Peneroplis pertusus(Forsskål in Niebuhr, 1775) 235 73.21 134 51.74 207 66.13

Peneroplis planatus(Fichtel & Moll, 1798) 60 18.69 6 2.32 9 2.88

Sorites orbiculus(Forsskål in Niebuhr, 1775) 0 0.00 1 0.39 0 0.00

TOTAL 321 100 259 100 313 100

(5)

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 a Index (Table 4). Species listed in Table 5 represent all benthic foraminiferal species from each location, in raw quantity or counts and

TABLE3. Relative abundances and bulk quantity of LBF genera from the three selected localities.

Genus/Aspects HMB-FS EBH-FS AUQ-P1

Individuals 317 259 313

Peneroplis_% 92.1 54.8 69.7

Coscinospira_% 0.00 41.7 15.7

Monalysidium_% 7.90 3.5 14.7

Sorites_% 0.00 0.01 0.00

Total specimens/g 200 663 100

FIGURE2. LBF specimens from the order Miliolida found in this study.1–3Monalysidium aciculare(Batsch, 1791).4–6Peneroplis planatus(Fichtel

& Moll, 1798).7–9Peneroplis pertusus(Forsskål in Niebuhr, 1775).10–12Coscinospira hemprichiiEhrenberg, 1839.13Sorites orbiculus(Forsskål in Niebuhr, 1775). In this plate,“a”shows apertural view while“b–c”shows side views, except forSorites. Specimen number 1, 4, 7, and 10 represent an early stage of development while remaining specimens are in a later stage of development (uncoiled and/orﬂaring). All line scales are representing 100mm.

(6)

percentage. Scanning electron microscope images of represen- tative species are presented in Figures 3 and 4.

L

IVE

-D

EAD

C

OMPARISON AND

N

ORMAL

-D

EFORMED

M

ORPHOLOGY

O

CCURRENCES

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, Elphi- dium, 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. Cosci- nospira 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 morpho- logical deformities were observed in the Miliolidea (Quinquelocu- lina, 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 signi ﬁ cantly 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 modi fi cations, and the presence of attached epibionts. Severe deformities include bizarre developments that make it dif fi cult to determine the species. Such deformities include twinning, constrictions, coiling-plane modi fi cations, 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 fl aring 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 ﬁ nal chamber, and were rarely found in the early stages of test development.

DISCUSSION

The western Arabian Gulf, particularly the eastern side of Saudi Arabia and Bahrain, experiences extreme ﬂ uctuations in temperature and salinity, especially during the summer (Kamin- ski 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 condi- tions. 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 ﬁ eld 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 tolerat- ing 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 in ﬂ uence 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 sedimenta- tion environment) in ﬂ uences 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 in ﬂ uence (Coccioni &

Luciani, 2006; Ferràndez-Cañadell et al., 2014; Antonarakou et al., 2018), which makes understanding how morphological

TABLE4. Diversity indices results from each sampling site and total bulk of benthic foraminifera (SBF and LBF) per gram sediments.

Parameter/Species

Sampling Stations

HMB-FS EBH-FS AUQ-FS AUQ-P1 AUQ-P2 AUQ-P3

Number of taxa 58 74 59 37 32 35

Individuals identiﬁed 263 303 266 211 200 217

Dominance D 0.04 0.10 0.05 0.13 0.09 0.06

Shannon H’ 3.49 3.21 3.34 2.63 2.79 3.07

Evenness e^H/S 0.57 0.33 0.48 0.38 0.51 0.62

Fishera 23.02 31.21 23.49 13.00 10.76 11.81

Specimens per gram 337 773 170 270 32 69

(7)

TABLE5. Total assemblages (living and dead) for each locality in the current studies for stained samples in raw count and % for all specimens.

Species

HMB–FS EBH–FS AUQ–FS AUQ–P1 AUQ–P2 AUQ–P3

Count % Count % Count % Count % Count % Count %

Agglutinella kaminskiiGarrison, 2019 1 0.38 3 0.99 0 0.00 1 0.48 0 0.00 1 0.46

Agglutinella robustaEl–Nakhal, 1983 3 1.14 3 0.99 0 0.00 0 0.00 0 0.00 1 0.46

Agglutinella soriformisEl–Nakhal, 1983 1 0.38 2 0.66 0 0.00 0 0.00 0 0.00 0 0.00

Ammonia aberdoveyensisHaynes, 1973 6 2.28 5 1.65 1 0.37 0 0.00 4 2.00 0 0.00

Ammonia abramovichaeHayward & Holzmann, 2021 in Hayward et al., 2021

2 0.76 5 1.65 6 2.25 0 0.00 4 2.00 9 4.15

Ammonia arabicaKaushik, 2021 in Hayward et al., 2021 11 4.18 2 0.66 4 1.50 0 0.00 0 0.00 6 2.76

Ammonia beccarii(Linnaeus, 1758) 0 0.00 2 0.66 4 1.50 1 0.48 0 0.00 5 2.30

Ammonia goldsteinaeHayward & Holzmann, 2021 in Hayward et al., 2021

3 1.14 0 0.00 0 0.00 0 0.00 2 1.00 4 1.84

Ammoniasp. 6 2.28 0 0.00 1 0.37 0 0.00 0 0.00 0 0.00

Ammoniasp. of Amao (2016) 3 1.14 1 0.33 5 1.87 4 1.91 6 3.00 0 0.00

Ammoniasp. 01 4 1.52 1 0.33 0 0.00 0 0.00 0 0.00 3 1.38

Ammoniasp. 01 of Amao (2016) 0 0.00 1 0.33 0 0.00 2 0.96 0 0.00 0 0.00

Ammoniasp. 02 0 0.00 3 0.99 0 0.00 0 0.00 0 0.00 0 0.00

Ammoniasp. 02 of Amao (2016) 2 0.76 1 0.33 0 0.00 0 0.00 3 1.50 0 0.00

Ammoniasp. 03 0 0.00 2 0.66 1 0.37 1 0.48 0 0.00 7 3.23

Ammonia tepida(Cushman, 1926) 0 0.00 2 0.66 9 3.37 0 0.00 3 1.50 0 0.00

Ammonia veneta(Schultze, 1854) 1 0.38 3 0.99 1 0.37 0 0.00 0 0.00 10 4.61

Clavulina angularisd'Orbigny, 1826 0 0.00 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Coscinospira hemprichiiEhrenberg, 1839 0 0.00 24 7.92 3 1.12 10 4.78 0 0.00 0 0.00

Cycloforina quinquecarinata(Collins, 1958) 0 0.00 0 0.00 2 0.75 0 0.00 0 0.00 0 0.00

Elphidium advena(Cushman, 1922) 1 0.38 2 0.66 0 0.00 0 0.00 2 1.00 5 2.30

Elphidium excavatum(Terquem, 1875) 3 1.14 2 0.66 0 0.00 2 0.96 0 0.00 0 0.00

Elphidiumﬁchtelianum(d'Orbigny, 1846) 0 0.00 5 1.65 0 0.00 0 0.00 0 0.00 0 0.00

Elphidium gerthivan Voorthuysen, 1957 1 0.38 0 0.00 1 0.37 0 0.00 0 0.00 0 0.00

Elphidium hawkesburyense(Albani, 1974) 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 1 0.46

Elphidium hispidulumCushman, 1936 2 0.76 0 0.00 8 3.00 0 0.00 0 0.00 0 0.00

Elphidium indicumCushman, 1936 0 0.00 0 0.00 0 0.00 2 0.96 0 0.00 4 1.84

Elphidium macellum(Fichtel & Moll, 1798) 0 0.00 4 1.32 1 0.37 2 0.96 5 2.50 6 2.76

Elphidium maoriumHayward, 1997 2 0.76 6 1.98 5 1.87 0 0.00 3 1.50 0 0.00

Elphidiumsp. 0 0.00 0 0.00 2 0.75 2 0.96 4 2.00 1 0.46

Elphidiumsp. 01 5 1.90 0 0.00 3 1.12 1 0.48 2 1.00 1 0.46

Elphidiumsp. 02 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 4 1.84

Elphidium tongaense(Cushman, 1931) 2 0.76 6 1.98 0 0.00 2 0.96 5 2.50 9 4.15

Flintinasp. of Amao (2016) 0 0.00 1 0.33 1 0.37 1 0.48 0 0.00 0 0.00

Glabratellinasp. 10 3.80 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Glabratellinasp. 01 5 1.90 0 0.00 0 0.00 1 0.48 0 0.00 0 0.00

Glabratellinasp. 02 3 1.14 0 0.00 0 0.00 1 0.48 0 0.00 0 0.00

Miliolinella chukchiensisLoeblich & Tappan, 1953 0 0.00 5 1.65 15 5.62 1 0.48 0 0.00 0 0.00

Miliolinella circularis(Bornemann, 1855) 0 0.00 2 0.66 3 1.12 0 0.00 0 0.00 5 2.30

Miliolinellaﬁchteliana(d'Orbigny, 1839) 15 5.70 7 2.31 31 11.61 8 3.83 24 12.00 31 14.29

Miliolinella hybrida(Terquem, 1878) 2 0.76 2 0.66 2 0.75 5 2.39 4 2.00 2 0.92

Milionellasp. 0 0.00 1 0.33 1 0.37 0 0.00 0 0.00 0 0.00

Miliolinellasp. 01 1 0.38 2 0.66 0 0.00 0 0.00 1 0.50 0 0.00

Miliolinellasp. 01 of Amao (2016) 1 0.38 4 1.32 1 0.37 0 0.00 0 0.00 0 0.00

Mililionellasp. 02 1 0.38 2 0.66 0 0.00 0 0.00 1 0.50 0 0.00

Miliolinellasp. 03 0 0.00 0 0.00 1 0.37 0 0.00 0 0.00 0 0.00

Miliolinella valvularis(Reuss, 1851) 0 0.00 0 0.00 1 0.37 0 0.00 0 0.00 0 0.00

Monalysidium aciculare(Batsch, 1791) 20 7.60 31 10.23 10 3.75 22 10.53 0 0.00 0 0.00

Peneroplis arietinus(Batsch, 1791) 0 0.00 1 0.33 1 0.37 2 0.96 0 0.00 0 0.00

Peneroplis pertusus(Forsskål in Niebuhr, 1775) 26 9.89 83 27.39 13 4.87 66 31.58 46 23.00 9 4.15

Peneroplis planatus(Fichtel & Moll, 1798) 2 0.76 2 0.66 1 0.37 2 0.96 0 0.00 0 0.00

Pseudolachlanella eburnea(d'Orbigny, 1839) 0 0.00 2 0.66 1 0.37 1 0.48 0 0.00 0 0.00

Pseudotriloculina hottingeriAmao & Kaminski, 2017 6 2.28 10 3.30 20 7.49 16 7.66 25 12.50 32 14.75

Pseudotriloculinasp. 0 0.00 0 0.00 2 0.75 1 0.48 8 4.00 0 0.00

Pseudotriloculinasp. 01 2 0.76 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Pseudotriloculina subgranulata(Cushman, 1918) 2 0.76 2 0.66 0 0.00 1 0.48 0 0.00 0 0.00

Quinqueloculina agglutinansd'Orbigny, 1839 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00

Quinqueloculina aknerianad'Orbigny, 1846 14 5.32 4 1.32 0 0.00 9 4.31 0 0.00 5 2.30

Quinqueloculina bidentatad'Orbigny, 1839 0 0.00 2 0.66 0 0.00 0 0.00 0 0.00 0 0.00

(8)

deformities occur in natural or naturally stressed environ- ments an intriguing research pursuit.

E

NVIRONMENTAL

D

ATA

I

NTERPRETATION

The sampling sites in the western Arabian Gulf, including Half Moon Bay and Al-Uqayr in Saudi Arabia, and East Bah- rain Foreshore, lie in foreshore or shallow-water lagoonal set- tings with a maximum depth of no more than 10 m (Amao et al., 2022). These sites are considered relatively pristine locations with low human in ﬂ uence, as de ﬁ ned by Murray

(2006). This region is naturally stressed by high salinities and temperatures especially during the summer, and some areas have been identi ﬁ ed 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.

TABLE5. Continued.

Species

HMB–FS EBH–FS AUQ–FS AUQ–P1 AUQ–P2 AUQ–P3

Count % Count % Count % Count % Count % Count %

Quinqueloculina bubnanensisMcCulloch, 1977 1 0.38 0 0.00 1 0.37 2 0.96 1 0.50 0 0.00

Quinqueloculina carinatastriata(Wiesner, 1923) 5 1.90 2 0.66 3 1.12 14 6.70 10 5.00 4 1.84

Quinqueloculina myagmarsurenParker, 2009 2 0.76 2 0.66 0 0.00 0 0.00 0 0.00 3 1.38

Quinqueloculina poeyanad'Orbigny, 1839 2 0.76 0 0.00 5 1.87 0 0.00 0 0.00 0 0.00

Quinqueloculina seminulum(Linnaeus, 1758) 2 0.76 2 0.66 4 1.50 0 0.00 0 0.00 0 0.00

Quinqueloculinasp. 2 0.76 2 0.66 0 0.00 0 0.00 0 0.00 4 1.84

Quinqueloculinasp. of Amao (2016) 0 0.00 2 0.66 0 0.00 0 0.00 0 0.00 0 0.00

Quinqueloculinasp. 01 0 0.00 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Quinqueloculinasp. 09 of Amao (2016) 3 1.14 1 0.33 1 0.37 0 0.00 0 0.00 0 0.00

Rosalinasp. 1 0.38 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Rosalinasp. 01 0 0.00 0 0.00 1 0.37 0 0.00 0 0.00 0 0.00

Sigmoilina canisdementisKaminski, Garisson &

Waskowska, 2020

20 7.60 3 0.99 0 0.00 0 0.00 0 0.00 0 0.00

Sorites orbiculus(Forsskål in Niebuhr, 1775) 0 0.00 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Spiroloculinasp. 1 0.38 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00

Spiroloculinasp. 01 0 0.00 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Spiroloculinasp. 02 0 0.00 1 0.33 1 0.37 0 0.00 0 0.00 0 0.00

Triloculina schreiberianad'Orbigny, 1839 4 1.52 2 0.66 24 8.99 1 0.48 0 0.00 0 0.00

Triloculinasp. 8 3.04 2 0.66 1 0.37 0 0.00 0 0.00 0 0.00

Triloculinasp. 01 0 0.00 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Triloculinasp. 02 0 0.00 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

Triloculinasp. 03 0 0.00 0 0.00 2 0.75 0 0.00 0 0.00 0 0.00

Triloculinasp. 04 0 0.00 0 0.00 2 0.75 7 3.35 0 0.00 0 0.00

Triloculinasp. 05 0 0.00 1 0.33 3 1.12 0 0.00 0 0.00 0 0.00

Triloculinasp. 05 of Amao (2016) 2 0.76 1 0.33 20 7.49 3 1.44 2 1.00 10 4.61

Triloculinasp. 06 0 0.00 0 0.00 4 1.50 0 0.00 0 0.00 0 0.00

Triloculinasp. 07 3 1.14 0 0.00 2 0.75 0 0.00 2 1.00 0 0.00

Triloculinasp. 08 7 2.66 2 0.66 3 1.12 8 3.83 4 2.00 3 1.38

Triloculina vespertilioZheng, 1988 8 3.04 5 1.65 14 5.24 2 0.96 3 1.50 2 0.92

Vertebralina striatad'Orbigny, 1826 0 0.00 1 0.33 0 0.00 0 0.00 0 0.00 0 0.00

TOTAL 263 100 303 100 267 100 209 100 200 100 217 100

(9)

FIGURE3. SBF specimens from the orders Rotaliida, Textulariida and Miliolida found in this study.1Ammonia abramovichaeHayward & Holzmann, 2021 in Hayward et al., 2021.2Ammonia beccarii (Linnaeus, 1758).3Ammoniasp.4Ammoniasp. of Amao, 2016.5Ammonia aberdoveyensisHaynes, 1973.6 Ammonia goldsteinaeHayward & Holzmann, 2021 in Hayward et al., 2021.7Ammoniasp. 1.8Elphidium excavatum(Terquem, 1875).9Elphidium hispidulum Cushman, 1936. 10Elphidium advena(Cushman, 1922).11Elphidium macellum (Fichtel & Moll, 1798).12Elphidium gerthi van Voorthuysen, 1957.13 Elphidium indicumCushman, 1936.14Elphidium tongaense(Cushman, 1931).15Elphidium maoriumHayward, 1997.16Elphidiumsp.17Rosalinasp.18 Glabratellinasp.19Glabratellinasp. 1.20Clavulina angularisd'Orbigny, 1826.21Vertebralina striatad'Orbigny, 1826.ForElphidiumandVertebralina:“a” shows the apertural view and“b–c”show side views (except number 15). ForAmmonia,Rosalina, andGlabratellina:“a”shows side view,“b”shows spiral view, and“c”shows umbilical view (except numbers 3, 5, 6, and 7). ForClavulina:“a”and“b”shows side view. All line scales are representing 100mm.

(10)

FIGURE4. SBF specimens from the order Miliolida found in this study.1Agglutinella kaminskiiGarrison, 2019.2Agglutinella soriformisEl-Nakhal, 1983.3– 4Pseudotriloculina hottingeri Amao & Kaminski, 2017. 5Miliolinella chukchiensisLoeblich & Tappan, 1953. 6 Miliolinella hybrida(Terquem, 1878). 7 Miliolinellasp.8Quinqueloculina carinatastriata(Wiesner, 1923).9Quinqueloculina sp. 18 of Amao, 2016.10Quinqueloculinasp. 27 of Amao, 2016.11 Quinqueloculina poeyanad'Orbigny, 1839.12Quinqueloculina bubnanensisMcCulloch, 1977.13Quinqueloculinasp. 33 of Amao, 2016.14Quinqueloculinasp.

15Quinqueloculina sp. 1. 16Quinqueloculina sp. 2. 17Quinqueloculina akneriana d'Orbigny, 1846. 18 Sigmoilina canisdementis Kaminski, Garrison &

Waskowska, 2020.19Spiroloculinasp.20Miliolinellaﬁchteliana(d'Orbigny, 1839).21Triloculina vespertilioZheng, 1988.22Triloculina sp.23Triloculinasp.

1.24Triloculinasp. 5 of Amao, 2016. In this plate,“a”shows the apertural view and“b–c”shows side views. All line scales are representing 100mm.

(11)

The sediment composition at the sampling sites consists mainly of sand-sized particles, comprising the dominant frac- tion (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 lithi ﬁ ed bioclastic materials due to seasonal exposure to high tempera- ture and oversaturated saline water (Weijermars, 1999). Unlike what Amao et al. (2018) reported in the Gulf of Salwa, frag- ments 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 fi ndings of Arslan et al. (2017) and Amao et al. (2018), indicating mini- mal human in fl uence. 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 fi ner sediment like mud (Rao et al., 2008;

Martins et al., 2011).

B

^ENTHIC

F

ORAMINIFERA

A

^SSEMBLAGES

: D

EFORMITIES AND

T

^HEIR

P

OSSIBLE

O

RIGINS

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 & Lok- ier, 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 Ara- bian 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, re fl ecting their ecological adaptations to high salinity, such as that found in the Arabian Gulf (Murray, 2006; Amao et al., 2022). No signi fi cant 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 5 foreshore code), and gradually declined with distance from open-marine in fl ux, for example, in the AUQ P2 and P3 samples from the lagoons at Al-Uqayr, except in the AUQ-P1. Similar fi ndings from the fossil record of hypersaline environments from the Miocene Dam Forma- tion (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, ﬂ ared portion in Peneroplis) compared with the juvenile forms (planispiral part). This observation aligns with the ﬁ ndings of Clarke & Keij (1973) and Fiorini & Lokier (2020), which indicated that most of the

TABLE6. Summary of representative benthic foraminifera from the sampling sites for the stained samples, outlining the major species contributors and counts for each species grouping, including total specimen quantity, living specimen, and deformed specimen in record.

Species/Grouping Counts

Sampling Sites

HMB-FS EBH-FS AUQ-FS AUQ-P1 AUQ-P2 AUQ-P3

Peneroplisspp. Total 28 86 15 70 46 9

Live 8 22 8 15 3 1

Deformed 17 17 7 21 27 9

Coscinospira hemprichii Total 0 24 3 10 0 0

Live 0 12 1 4 0 0

Deformed 0 11 1 4 0 0

Monalysidium aciculare Total 20 31 10 22 0 0

Live 8 15 4 4 0 0

Deformed 10 5 5 9 0 0

Miliolinella spp. Total 20 25 55 14 30 38

Live 3 8 11 4 4 7

Deformed 11 7 12 4 5 9

Quinqueloculinaspp. Total 51 35 27 30 37 46

Live 11 9 3 4 1 2

Deformed 4 3 1 2 5 11

Triloculinaspp. Total 32 15 75 21 11 15

Live 10 3 6 2 2 3

Deformed 3 0 4 4 1 5

Ammoniaspp. Total 38 28 32 8 22 44

Live 16 11 9 2 7 10

Deformed 14 3 9 2 5 11

Elphidiumspp. Total 16 25 20 11 21 31

Live 7 9 7 3 7 5

Deformed 8 7 6 6 7 17

(12)

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; Saras- wat et al., 2015; Price et al., 2019). Based on our ﬁ ndings indicating low levels of anthropogenic stressors, the most likely

FIGURE5. LBF specimens fromMonalysidium aciculare(1–9) andPeneroplis planatus(10–21) showing various type of morphological deformities: dis- tortedﬁnal chambers (1, 6, 12, 17, 18), dented chambers (2, 4, 10, 11, 16), changing of coiling plane (5, 6), enlargement or shrinkage of certain chambers (5, 6, 9), twinning (7, 9, 15), aberrant aperture (3, 6, 8, 17, 18), splitting aperture (13, 14), branching twin (20), bifurcation (19, 21), and multiple deformities in one specimen (4–9, 12, 16–21). Within this plate, a shows apertural view while b–c shows side views. All line scales are representing 100mm.

(13)

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 calci ﬁ cation 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 experi- ence 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), ampli ﬁ ed by strong winter winds that disrupt sedi- ment settlement in the shallow waters of the Gulf (Langodan et al., 2023); the weak shell con ﬁ guration of miliolids, which dominate the assemblages in our study area, means that

FIGURE6. LBF specimens fromPeneroplis pertusus(1–8),Coscinospira hemprichii(9–14), andSorites orbiculus(15) showing various type of morphological deformities: twinning (1, 5), changing of coiling plane (2, 6, 8–11, 14, 15), splitting aperture (3), bifurcation (13), apertural development in both side (4), branching twin (7), distortedﬁnal chamber (8), dented chamber (3, 5, 7, 8, 13), aberrant aperture (4, 5, 12), and multiple deformities in one specimen (4, 8, 12). Within this plate, a shows apertural view while b–c shows side views (except number15). All line scales are representing 100mm.

(14)

mechanical abrasion can easily damage them or break them apart (Briguglio & Hohenegger, 2011). Although post-mor- tem 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 acidi ﬁ cation (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 & Hal- lock, 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 mor- phological 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

FIGURE7. SBF specimen from the order Rotaliida fromAmmonia(1–5) andElphidium(6–10) showing various types of morphological deformities: distorted or brokenfinal chamber (1–4), dented chamber (2, 4, 7), become highly trochospiral (2–4), distorted umbilical side (4),flattened on the umbilical side (5), protuberance growth (6), sunkenfinal chamber (8), obliterated apertural face (8–10), and multiple deformities in one specimen (2, 4, 10). For Ammonia: a shows side view, b shows spiral view, and c shows umbilical views. ForElphidium: a shows apertural view, and b–c shows side views. All line scales are representing 100mm.

(15)

speci ﬁ cally 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.

CONCLUSIONS

In this study, we assessed benthic foraminiferal assemblages at six western Arabian Gulf localities considered to represent pristine but naturally stressed environments, including quanti- fying the occurrences of morphological deformities in the foraminifera. Our sample sites covered a range of salinity lev- els above normal for the region ( . 40 PSU), and exhibited lit- tle 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, Cosci- nospira, and Monalysidium that host algal endosymbionts.

FIGURE 8. SBF specimens from the order Miliolida from Miliolinella (1–4), Pseudotriloculina (5), Spiroloculina (6), Triloculina (7), and Quinqueloculina(8–12) showing various types of morphological deformities: distorted or aberrant aperture (1–4), eroded or dented chamber (5, 8), change in coiling plane development (6, 10, 12), attached epibiont in side part (9), and multiple deformities in one specimen (3, 4, 9). A shows apertural view while b–c shows side views (except number 4 and 9d for zoomed version of attached epibiont). All line scales are representing 100mm.

FIGURE9. Relationship between the salinity values and the percentage of morphological deformities observed in this study.

(16)

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 con ﬁ rm these observations and the roles of the assumed morphological deformity inducers.

ACKNOWLEDGMENTS

We are grateful to the Deanship of Scienti ﬁ c 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.

REFERENCES

Aboobacker, V. M., Samiksha, S. V., Veerasingam, S., Al-Ansari, E. M., and Vethamony, P., 2021, Role of Shamal and easterly winds on the wave characteristics off Qatar, central Arabian Gulf: Ocean Engineer- ing, v. 236, p. 1–11.

Amao, A. O., 2016, Benthic foraminiferal taxonomy, distribution and ecology in the Arabian Gulf: Unpublished Ph.D. dissertation, King Fahd University of Petroleum & Minerals, 364 p.

Amao, A. O., Kaminski, M. A., and Setoyama, E., 2016, Diversity of foraminifera in a shallow restricted lagoon in Bahrain: Micropaleontology, v. 62, p. 197–211.

Amao, A. O., Kaminski, M. A., and Babalola, L., 2018, Benthic foraminifera in hypersaline Salwa Bay (Saudi Arabia): An insight into future climate change in the gulf region?: Journal of Foraminiferal Research, v.

48, p. 29–40.

Amao, A. O., Kaminski, M. A., Bucci, C., Hallock, P., Al-Enezi, E., Zaky, A. S., and Frontalini, F., 2022, Benthic foraminifera in the Arabian Gulf: Biodiversity and geographical trends: Marine Micropaleontol- ogy, v. 176, p. 1–14.

Antonarakou, A., Kontakiotis, G., Zarkogiannis, S., Mortyn, P. G., Drinia, H., Koskeridou, E., and Anastasakis, G., 2018, Planktonic foraminiferal abnormalities in coastal and open marine eastern Mediterranean environments: A natural stress monitoring approach in recent and early Holocene marine systems: Journal of Marine Systems, v. 181, p. 63–78.

Arslan, M., Kaminski, M. A., Tawabini, B. S., Ilyas, M., and Frontalini, F., 2016a, Benthic foraminifera in sandy (siliciclastic) coastal sediments of the Arabian Gulf (Saudi Arabia): A technical report: Arabian Jour- nal of Geosciences, v. 9, p. 1–7.

Arslan, M., Kaminski, M. A., Tawabini, B. S., Ilyas, M., Babalola, L. O., and Frontalini, F., 2016b, Seasonal variations, environmental parameters, and standing crop assessment of benthic foraminifera in eastern Bahrain, Arabian Gulf: Geological Quarterly, v. 60, p. 26–37.

Arslan, M., Kaminski, M. A., Khalil, A., Ilyas, M., and Tawabini, B. S., 2017, Benthic Foraminifera in Eastern Bahrain: Relationships with local pollution sources: Polish Journal of Environmental Studies, v. 26, p. 969–984.

Barras, C., Mouret, A., Nardelli, M. P., Metzger, E., Petersen, J., La, C., Filipsson, H. L., and Jorissen, F., 2018, Experimental calibration of manganese incorporation in foraminiferal calcite: Geochimica et Cos- mochimica Acta, v. 237, p. 49–64.

Barth, H. J., and Khan, N. Y., 2008, Biogeophysical setting of the Gulf,in Abuzinada, A. H., et al. (eds.), Protecting the Gulf’s Marine Ecosys- tems from Pollution: Birkhäuser, Basel, p. 1–21.

Boltovskoy, E., Scott, D. B., and Medioli, F. S., 1991, Morphological variations of benthic foraminiferal tests in response to changes in ecological parameters: A review: Journal of Paleontology, v. 65, p. 175–185.

BouDagher-Fadel, M. K., 2008, Biology and evolutionary history of larger benthic foraminifera: Developments in Palaeontology and Stratigra- phy, v. 21, p. 1–37.

Briguglio, A., and Hohenegger, J., 2011, How to react to shallow water hydrodynamics: the larger benthic foraminifera solution: Marine Micropaleontology, v. 81, p. 63–76.

Briguglio, A., and Kaminski, M. A., 2023, Advances in the biostratigraphy of Paleogene larger benthic foraminifera: Micropaleontology, v. 69, p.

361–362.

Campos, E. J., Vieira, F., Cavalcante, G., Kjerfve, B., Abouleish, M., Shahriar, S., Mohamed, R., and Gordon, A. L., 2020, Impacts of brine disposal from water desalination plants on the physical environment in the Persian/

Arabian Gulf: Environmental Research Communications, v. 2, p. 1–12.

Chan, S. A., Kaminski, M. A., Al-Ramadan, K., and Babalola, L. O., 2017, Foraminiferal biofacies and depositional environments of the Burdigalian mixed carbonate and siliciclastic Dam Formation, Al- Lidam area, Eastern Province of Saudi Arabia: Palaeogeography, Palaeoclimatology, Palaeoecology, v. 469, p. 122–137.

Charrieau, L. M., Filipsson, H. L., Nagai, Y., Kawada, S., Ljung, K., Kritzberg, E., and Toyofuku, T., 2018, Decalciﬁcation and survival of benthic foraminifera under the combined impacts of varying pH and salinity: Marine Environmental Research, v. 138, p. 36–45.

Cherif, O. H., Al-Ghadban, A. N., and Al-Rifaiy, I. A., 1997, Distribution of foraminifera in the Arabian Gulf: Micropaleontology, v. 43, p. 253–280.

Clarke, M. H., and Keij, A. J., 1973, Organisms as producers of carbonate sediment and indicators of environment in the southern Persian Gulf, inPurser, B. H. (ed.), The Persian Gulf: Holocene Carbonate Sedimen- tation and Diagenesis in a Shallow Epicontinental Sea: Springer, Ber- lin, p. 33–56.

Coccioni, R., and Luciani, V., 2006,Guembelitria irregularisbloom at the KT boundary: Morphological abnormalities induced by impact-related extreme environmental stress?,inCockell, C., et al. (eds.), Biological Pro- cesses Associated with Impact Events: Springer, Berlin, p. 179–196.

Consorti, L., Kavazos, C. R. J., Ford, C., Smith, M., and Haig, D. W., 2020, High productivity ofPeneroplis(Foraminifera) including aberrant morphotypes, in an inland thalassic salt pond at Lake Macleod, Western Australia: Marine Micropaleontology, v. 160, p. 1–18.

Cushman, J. A., 1928, Foraminifera: Their classiﬁcation and economic use: Cushman Laboratory for Foraminiferal Research Special Publica- tion, v. 1, p. 1–401.

de Nooijer, L. J., Reichart, G. J., Dueñas-Bohórquez, A., Wolthers, M., Ernst, S. R., Mason, P. R. D., and Van der Zwaan, G. J., 2007, Copper incorporation in foraminiferal calcite: Results from culturing experiments: Biogeosciences, v. 4, p. 493–504.

Dissard, D., Nehrke, G., Reichart, G. J., and Bijma, J., 2010, Impact of seawater pCO2on calciﬁcation and Mg/Ca and Sr/Ca ratios in benthic foraminifera calcite: Results from culturing experiments withAmmo- nia tepida: Biogeosciences, v. 7, p. 81–93.

Ferràndez-Cañadell, C., Briguglio, A., Hohenegger, J., and Wöger, J., 2014, Test fusion in adult foraminifera: A review with new observations of an Early EoceneNummulitesspecimen: Journal of Foraminif- eral Research, v. 44, p. 316–324.

(17)

Fiorini, F., and Lokier, S. W., 2020, Abnormal test growth in larger benthic foraminiferal from hypersaline coastal ponds of the United Arab Emir- ates: Micropaleontology, v. 66, p. 151–156.

Frontalini, F., and Coccioni, R., 2011, Benthic foraminifera as bioindicators of pollution: A review of Italian research over the last three decades: Revue de Micropaléontologie, v. 54, p. 115–127.

Frontalini, F., Greco, M., Di Bella, L., Lejzerowicz, F., Reo, E., Caruso, A., Cosentino, C., Maccotta, A., Scopelliti, G., Nardelli, M. P., and Losada, M. T., 2018, Assessing the effect of mercury pollution on cultured benthic foraminifera community using morphological and eDNA metabar- coding approaches: Marine Pollution Bulletin, v. 129, p. 512–524.

Geerken, E., de Nooijer, L. J., van Dijk, I., and Reichart, G. J., 2018, Impact of salinity on element incorporation in two benthic foraminiferal species with contrasting magnesium contents: Biogeosciences, v.

15, p. 2205–2218.

Geslin, E., Stouff, V., Debenay, J. P., and Lesourd, M., 2000, Environmen- tal variation and foraminiferal test abnormalities,inMartin, R. E. (ed.), Environmental Micropaleontology: The Application of Microfossils to Environmental Geology: Springer, Boston, p. 191–215.

Geslin, E., Debenay, J. P., Duleba, W., and Bonetti, C., 2002, Morphologi- cal abnormalities of foraminiferal tests in Brazilian environments:

Comparison between polluted and non-polluted areas: Marine Micro- paleontology, v. 45, p. 151–168.

Groeneveld, J., and Filipsson, H. L., 2013, Mg/Ca and Mn/Ca ratios in benthic foraminifera: The potential to reconstruct past variations in temperature and hypoxia in shelf regions: Biogeosciences, v. 10, p.

5125–5138.

Grzybowski, J., 1898, Otwornice pokładów naftonosnych okolicy Krosna.

Rozprawy Akademii Umieje˛tnosci w Krakowie, Wydział Matema- tyczno-Przyrodniczy: Kraków, ser. 2, v. 33, p. 257–305.

Hallock, P., and Seddighi, M., 2022, Why did some larger benthic foraminifera become so large andﬂat?: Sedimentology, v. 69, p. 74–87.

Hallock, P., Talge, H. K., Cockey, E. M., and Muller, R. G., 1995, A new disease in reef-dwelling foraminifera: Implications for coastal sedi- mentation: Journal of Foraminiferal Research, v. 25, p. 280–286.

Hammer, O., Harper, D., and Ryan, P., 2001, PAST: Paleontological Statis- tics Software Package for education and data analysis: Palaeontologia Electronica, v. 4, p. 1–9.

Hart, M. B., Fisher, J. K., Smart, C. W., Speers, R., and Wall-Palmer, D., 2022, Re-colonization of hostile environments by benthic foraminifera:

An example from Montserrat, Lesser Antilles Volcanic Arc: Micropa- leontology, v. 68, p. 1–27.

Haynert, K., Schönfeld, J., Schiebel, R., Wilson, B., and Thomsen, J., 2014, Response of benthic foraminifera to ocean acidiﬁcation in their natural sediment environment: A long-term culturing experiment: Bio- geosciences, v. 11, p. 1581–1597.

Hayward, B. W., Holzmann, M., Pawlowski, J., Parker, J. H., Kausik, T., Toyofuku, M. S., and Tsuchiya, M., 2021, Molecular and morphological taxonomy of livingAmmoniaand related taxa (Foraminifera) and their biogeography: Micropaleontology, v. 67, p. 109–313.

Herguera, J. C., and Berger, W. H., 1991, Paleoproductivity from benthic foraminifera abundance: Glacial to postglacial change in the west- equatorial Paciﬁc: Geology, v. 19, p. 1173–1176.

Hess, S., Kuhnt, W., Hill, S., Kaminski, M. A., Holbourn, A. E., and de Leon, M., 2001, Monitoring the recolonization of the Mt. Pinatubo 1991 ash layer by benthic foraminifera: Marine Micropaleontology, v.

43, p. 119–142.

Hikmahtiar, S., Kaminski, M. A., and Cetean, C. G., 2022, Lower Paleo- cene deep-water agglutinated foraminifera from the Contessa Highway Section (Umbria-Marche Basin, Italy): Taxonomy, stratigraphic distribution and assemblage turnover across the Cretaceous/Paleogene Boundary: Rivista Italiana de Paleontologia e Stratigraﬁa, v. 128, p.

719–744.

Hohenegger, J., 2009, Functional shell geometry of symbiont-bearing benthic foraminifera: Galaxea, Journal of Coral Reef Studies, v. 11, p. 81– 89.

Holt, E. A., and Miller, S. W., 2011, Bioindicators: Using organisms to measure environmental impacts: Nature Education Knowledge, v. 2, p. 8–13.

Horton, T., Kroh, A., Bailly, N., Boury-Esnault, N., Brandão, S. N., Costello, M. J., Gofas, S., Hernandez, F., Mees, J., Paulay, G., Poore,

G., Rosenberg, G., Stöhr, S., Decock, W., and others, 2017, World Register of Marine Species (WoRMS): WoRMS Editorial Board.

http://www.marinespecies.org/.

Jennings, D., 2015, Culturing benthic foraminifera to understand the effects of changing seawater chemistry and temperature on foraminiferal shell chemistry: Doctoral dissertation, Iowa State University, 102 p.

Jones, R. W., 2014, Foraminifera and Their Applications: Cambridge Uni- versity Press, Cambridge, 391 p.

Joydas, T. V., Qurban, M. A., Manikandan, K. P., Ashraf, T. T. M., Ali, S. M., Al-Abdulkader, K., Qasem, A., and Krishnakumar, P. K., 2015, Status of microbenthic communities in the hypersaline waters of the Gulf of Salwa, Arabian Gulf: Journal of Sea Research, v. 99, p. 34–46.

Joydas, T. V., Qurban, M. A., Borja, A., Manokaran, S., Manikandan, K. P., Rabaoui, L. J., Garmendia, J. M., Asharaf, T. T. M., Ayranci, K., Shemsi, A. M., and Mohammed, S., 2023, Ecological status of microbenthic communities in the Saudi waters of the western Arabian Gulf: Regional Studies in Marine Science, v. 57, p. 1–15.

Kaiho, K., 1994, Benthic foraminiferal dissolved oxygen index and dissolved oxygen levels in the modern ocean: Geology, v. 22, p. 719–722.

Kaiho, K., 2022, Relationship between extinction magnitude and climate change during major marine and terrestrial animal crises: Biogeoscien- ces, v. 19, p. 3369–3380.

Kaminski, M. A., 2012, Calibration of the benthic foraminiferal oxygen index in the Marmara Sea: Geological Quarterly, v. 56, p. 757–764.

Kaminski, M. A., Chan, S. A., Balc, R., Gull, H. M., Amao, A. O., and Babalola, L. O., 2018, Middle Jurassic Planktonic Foraminifera in Saudi Arabia–a new biostratigraphical marker for the J30 maximum ﬂooding surface in the Middle East: Stratigraphy, v. 15, p. 37–46.

Kaminski, M. A., Amao, A. O., Garrison, T. F., Fiorini, F., Magliveras, S., and Waskowska, A., 2020. AnEntzia-dominated marsh-type agglutinated foraminiferal assemblage from a salt marsh in Tubli Bay, Bah- rain: Geology, Geophysics and Environment, v. 46, p. 189–204.

Kaminski, M. A., Amao, A. O., Babalola, L., Khamsin, A. B., Fiorini, F., Garrison, A. M., Gull, H. M., Johnson, R. L., Tawabini, B. S., Frontalini, F., and Garrison, T. F., 2021, Substrate temperature as a primary control on meiofaunal populations in the intertidal zone: A dead zone attributed to elevated summer temperatures in eastern Bahrain:

Regional Studies in Marine Science, v. 42, p. 1–6.

Kaminski, M., Prayudi, S. D., Korin, A., and Tawabini, B. S., 2023, Inter- tidal lagoons in the western Arabian Gulf are summer dead zones:

Geophysical Research Abstracts, v. 23 (No. EGU23-7210), Copernicus Meetings.

Kenigsberg, C., Abramovich, S., and Hyams-Kaphzan, O., 2020, The effect of long-term brine discharge from desalination plants on benthic foraminifera: PloS ONE, v. 15, p. 1–20.

Kotler, E., Martin, R. E. and Liddell, W. D., 1992, Experimental analysis of abrasion and dissolution resistance of modern reef-dwelling foraminifera: Implications for the preservation of biogenic carbonate: Palaios, v. 7, p. 244–276.

Lane, M. K., Fehrenbacher, J. S., Fisher, J. L., Fewings, M. R., Crump, B. C., Risien, C. M., Meyer, G. M., and Schell, F., 2023, Planktonic foraminiferal assemblages reﬂect warming during two recent mid-lati- tude marine heatwaves: Frontiers in Marine Science, v. 10, p. 1–13.

Langer, M. R., Weinmann, A. E., Lötters, S., Bernhard, J. M., and Rödder, D., 2013, Climate-driven range extension ofAmphistegina(protista, foraminiferida): Models of current and predicted future ranges: PloS One, v. 8, p. 1–10.

Langodan, S., Cavaleri, L., Benetazzo, A., Bertotti, L., Dasari, H. P., and Hoteit, I., 2023, The peculiar wind and wave climatology of the Ara- bian Gulf: Ocean Engineering, v. 290, p. 1–13.

Loeblich A. R. Jr., , and Tappan, H., 1994, Foraminifera of the Sahul Shelf and Timor Sea: Cushman Foundation for Foraminiferal Research Spe- cial Publication, v. 30, 661 p.

Martins, V., Yamashita, C., Sousa, S. H. D. M., Martins, P., Laut, L. L. M., Figueira, R. C., Mahiques, M. M. D., Ferreira da Silva, E., Dias, J. M., and Rocha, F., 2011, The response of benthic foraminifera to pollution and environmental stress in Ria de Aveiro (N Portugal): Journal of Ibe- rian Geology, v. 37, p. 231–246.

Martins, M. V. A., Yamashita, C., de Sousa, S. H. D. M., Koutsoukos, E. A. M., Disaró, S. T., Debenay, J. P., and Duleba, W., 2019, Response

(18)

of benthic foraminifera to environmental variability: Importance of benthic foraminifera in monitoring studies, in Fouzia, H. B. (ed.), Monitoring of Marine Pollution: IntechOpen, p. 1–26.

Merkado, G., Holzmann, M., Apothéloz-Perret-Gentil, L., Pawlowski, J., Abdu, U., Almogi-Labin, A., Hyams-Kaphzan, O., Bakhrat, A., and Abramovich, S., 2013, Molecular evidence for Lessepsian invasion of Soritids (larger symbiont bearing benthic foraminifera): PloS One, v.

8, p. 1–12.

Murray, J. W., 1970, The foraminifera of the hypersaline Abu Dhabi lagoon, Persian Gulf: Lethaia, v. 3, p. 51–68.

Murray, J. W., 2006, Ecology and Applications of Benthic Foraminifera:

Cambridge University Press, Cambridge, 426 p.

Nigam, R., Linshy, V. N., Kurtarkar, S. R., and Saraswat, R., 2009, Effects of sudden stress due to heavy metal mercury on benthic foraminifer Rosalina leei: Laboratory culture experiment: Marine Pollution Bulle- tin, v. 59, p. 362–368.

Onjefu, S. A., Shaningwa, F., Lusilao, J., Abah, J., Hess, E., and Kwaambwa, H. M., 2020, Assessment of heavy metals pollution in sediment at the Omaruru River basin in Erongo region, Namibia: Envi- ronmental Pollutants and Bioavailability, v. 32, p. 187–193.

Pal, J. S., and Eltahir, E. A., 2016, Future temperature in southwest Asia projected to exceed a threshold for human adaptability: Nature Climate Change, v. 6, p. 197–200.

Paparella, F., D’Agostino, D. and Burt, J. A., 2022, Long-term, basin-scale salinity impacts from desalination in the Arabian/Persian Gulf: Scien- tiﬁc Reports, v. 12, p. 1–12.

Pati, P., and Patra, P. K., 2012, Benthic foraminiferal responses to coastal pollution: A review: International Journal of Geology, Earth and Envi- ronmental Sciences, v. 2, p. 2277–2081.

Pazi, I., 2011, Assessment of heavy metal contamination in Candarli Gulf sediment, Eastern Aegean Sea: Environmental Monitoring and Assess- ment, v. 174, p. 199–208.

Pinko, D., Abramovich, S., and Titelboim, D., 2020, Foraminiferal holo- biont thermal tolerance under future warming–roommate problems or successful collaboration?: Biogeosciences, v. 17, p. 2341–2348.

Pinsky, M. L., Comte, L., and Sax, D. F., 2022, Unifying climate change biology across realms and taxa: Trends in Ecology & Evolution, v. 37, p. 672–682.

Prazeres, M., Uthicke, S., and Pandolfi, J. M., 2015, Ocean acidification induces biochemical and morphological changes in the calcification process of large benthic foraminifera: Proceedings of the Royal Soci- ety B: Biological Sciences, v. 282, p. 1–10.

Prazeres, M., Roberts, T. E., and Pandolﬁ, J. M., 2017, Variation in sensitivity of large benthic Foraminifera to the combined effects of ocean warming and local impacts: Scientiﬁc Reports, v. 7, p. 1–11.

Price, A. R. G., Sheppard, C. R. C., and Roberts, C. M., 1993, The Gulf:

Its biological setting: Marine Pollution Bulletin, v. 27, p. 9–15.

Price, E. B., Kabengi, N., and Goldstein, S. T., 2019, Effects of heavy- metal contaminants (Cd, Pb, Zn) on benthic foraminiferal assemblages grown from propagules, Sapelo Island, Georgia (USA): Marine Micro- paleontology, v. 147, p. 1–11.

Rao, C. R. M., Sahuquillo, A., and Lopez Sanchez, J. F., 2008, A review of the different methods applied in environmental geochemistry for single and sequential extraction of trace elements in soils and related materials: Water, Air, and Soil Pollution, v. 189, p. 291–333.

Riegl, B. M., and Purkis, S. J., 2012, Environmental constraints for reef building in the Gulf,inRiegl, B. M., and Purkis, S. J. (eds.), Coral reefs of the Gulf: Adaptation to climatic extremes: Springer, Dor- drecht, p. 5–32.

Ross, B. J., and Hallock, P., 2016, Dormancy in the foraminifera: A review: Journal of Foraminiferal Research, v. 46, p. 358–368.

Röttger, R., and Hallock, P., 1982. Shape trends inHeterostegina: Journal of Foraminiferal Research, v. 12, p. 197–204.

Sabbatini, A., Morigi, C., Nardelli, M. P., and Negri, A., 2014, Foraminif- er