An Entzia-dominated marsh-type agglutinated foraminiferal assemblage from a salt marsh in Tubli Bay, Bahrain

A salt-marsh assemblage of agglutinated foraminifera was recovered from a salt marsh on the east side of Tubli Bay in eastern Bahrain. This locality is one of the last remaining patches of salt marsh on the east coast of Tubli Bay. The salt marsh is covered by a single marsh plant species, Arthrocnemum macrostachyum. Samples were collected from beneath the Arthrocnemum canopy in two transects beginning at the maximum landward extent of halophytic plants in the high marsh and extending to a tidal channel at the seaward side of the low marsh. A distinct elevation-related zonation in foraminifera is observed from the high marsh to the low marsh. The trochamminids Entzia macrescens and Trochammina inflata are characteristic of the high marsh, whereas Ammonia, Elphidium, Peneroplis and smaller miliolids become common in the middle part of the marsh transect. The tidal channel at the lower limit of the marsh contains an assemblage dominated by Ammonia, Elphidium, adult specimens of Peneroplis, and smaller miliolids, with Clavulina and Agglutinella as the only agglutinated taxa. Living specimens of Entzia and Trochammina were observed during the winter 2019–2020 sampling season, whereas samples collected in Autumn 2019 contained only dead specimens. One new species, ?Sigmoilina canisdementis sp. nov., is described herein. This is the first report of a live Entzia-dominated salt marsh assemblage in the Arabian Gulf region.


INTRODUCTION
For more than half a century, salt-marsh foraminifera have been widely accepted as useful bioindicators for past sea level change and reconstructing the Holocene. Beginning with the work of Bartenstein & Brand (1938), Cushman & Brönnimann (1948), Andersen (1951), Saunders (1957) and Pfleger (1960Pfleger ( , 1970, it became apparent that salt marshes contain unique assemblages of agglutinated foraminifera consisting mainly of a diverse range of trochamminids. Because saltmarsh foraminifera (and their presumed carriers, the migratory shore birds) have wide geographical distribution and distinct vertical ranges, the use of agglutinated foraminifera as bioindicators has increasing importance in different parts of the world in understanding the rate of relative sea level change especially with the current scenario of global warming and predicted global sea level rise.
The pioneering studies of Scott & Medioli (1978, 1980 have shown that the spatial distribution of agglutinated foraminifera in temperate salt marshes may be closely related to the tide level. For example, a salt-marsh foraminiferal species, Entzia macrescens (Brady), was recorded by Scott & Medioli (1980) just below the level of higher high water (HHW), above which the living foraminifera rapidly disappear. Other marsh foraminifera (i.e., Tiphotrocha, Trochammina, Miliammina, and calcareous benthic species) occur at lower elevations with respect to HHW, and consequently the occurrence of such foraminifera in sediment cores can be used as indicators of past sea-level changes (see Horton & Edwards 2006). Later studies by Scott et al. (1990) have shown that E. macrescens are widely distributed along the Atlantic coastline of North and South America. Furthermore, E. macrescens has been found across the globe in the salt marshes of NW Europe (Bartenstein & Brand 1938), North America (Scott & Medioli 1980), the Caspian Sea (Shmal'gauzen 1950) and the Bay of Bengal (Kumar et al. 2014). Two distinct phylotypes of E. macrescens have already been reported in Europe (Holzmann & Pawlowski 2017), and considering the large distances between populations of Entzia from Europe, North and South America and the Indian coast one can expect to find additional cryptic species (M. Holzmann 2020, personal communication). The species has even colonized saline springs found near the salt mines of central Transylvania (Daday 1884, Filipescu & Kaminski 2011. The E. macrescens population in Transylvania is genetically identical to the population from South Wales, and specimens have likely been transported by birds during seasonal migrations (Holzmann & Pawlowski 2017).
Along the shores of the western Arabian Gulf, the last remaining salt marshes are currently under threat from coastal development and land reclamation. In this study, we are reporting a survey of foraminifera found in one of the extant salt marshes that has not been developed. Although studies of benthic foraminifera have been conducted from the intertidal zone in Bahrain (Basson & Murray 1995, Amao et al. 2016, Garrison 2019, until now, there have been no reported surveys of salt-marsh foraminifera found in vegetated marshes.

STUDY AREA
The study site was a 100 m by 300 m patch of vegetated salt marsh and mangal located adjacent to an automotive dealership on the Shaikh Jaber Al-Subah Highway in Sitra, Bahrain. The site is located on the eastern side of Tubli Bay (Fig. 1). Tubli Bay is a shallow wedge-shaped inlet (average depth 5 m) with a surface area of 10 km 2 located in northeastern Bahrain (Seedo et al. 2017). It is home to large numbers of pink flamingos, egrets, and other wading birds, but its intertidal zone has now been largely reclaimed, particularly on the eastern side in Sitra. The patch of salt marsh and mangroves next to the automotive dealership is the only remaining undisturbed marsh habitat on the eastern side of the bay. The intertidal zone at the studied site (from HHW to the bay) consists of six habitats: (1) a vegetated high marsh covered by a monospecific canopy of the perennial halophyte Arthrocnemum macrostachyum (Mericand), (2) a tidal creek leading to a tidal pool, (3) the highest occurrence of sparse grey mangrove bushes (Avicenna marina), grading into (4) a thick canopy of mature mangrove trees, and on the seaward side, (5) an intertidal mud flat with patches of algal mat cut by tidal channels extending to the low tide mark, and finally (6) the open waters of Tubli Bay (Fig. 1).
This study focuses on the foraminiferal assemblages found within the A. macrostachyum salt marsh, along an elevational transect extending from the highest occurrence of the A. macrostachyum canopy on the landward side to the tidal channel separating the salt marsh from the mangroves on the seaward side (Fig. 2). At the landward edge of the salt marsh, some additional halophytic plants were noted, including Halocnemem strobilaceum (Pallas), Tetraena qatarensis (Hadid), and Cistanche tubulosa (Schenk). Above HHW the upland is sparsely covered by tufts of grass until it meets the highway.

MATERIAL AND METHODS
Samples were collected from beneath the Arthrocnemum canopy in two transects beginning at the tidal channel at the seaward side of the low marsh and extending to the maximum extent of halophytic plants in the high marsh. The marsh was first sampled for taxonomic purposes on December 7, 2019 (samples VW0-VW5) along the line of transect 1. Transect 1 was sampled again at the end of January, 2020, and transect 2 was sampled two weeks later on February 13, 2020. On the day transect 2 was collected, air and sediment temperatures were 17°C. Samples were collected by inserting the mouth of a 125 ml glass sample jar into the sediment underneath an Arthrocnemum plant to a depth of 1 cm, thereby collecting a plug of surficial sediment 4 cm in diameter and 1 cm thick. Samples were brought back to the lab within a few hours and soaked in a rose Bengal solution (80% ethanol with 5 g rose Bengal powder per litre), for a minimum of two weeks. Samples were gently washed over a 63 mm sieve, dried in an oven at 60°C, and split into manageable fractions using a brass microsplitter (Micropress Europe, Poland). Each split sample yielded approximately 300 specimens (typically 1/16 of the original sample), which were drysieved over a 125 mm sieve, and the foraminifera (both stained and unstained) were picked from the ≥125 mm fraction into cardboard microscope slides. Selected specimens were photographed using a FEI QUANTA 200 FEG SEM at the Laboratory of Critical Elements, Faculty of Geology, Geophysics and Environmental Protection, AGH University of Science & Technology, Kraków, Poland. The foraminiferal reference slides will be deposited in the collections of the European Micropaleontological Reference Centre in Kraków, Poland.

RESULTS
Benthic Foraminifera were recovered from all samples in both transects. The sampled transects begin beneath the highest Arthrocnemum plant at the landward edge of the marsh. The total assemblage is tabulated in Tables 1 and 2, with stained and unstained specimens counted separately. In all samples the proportion of stained specimens is small, less than 5% of the total assemblage.
A distinct elevation-related zonation in both rose-Bengal stained and unstained benthic foraminifera is observed from the high marsh to the low marsh. The results are discussed separately.

Live assemblage
Samples collected on December 7, 2019 did not yield any living (rose Bengal stained) foraminifera Living specimens of benthic foraminifera were recovered during the winter 2019-2020 (January-February, 2020) sampling season. The highest occurrence of living foraminifera is found at the landward edge of the Arthrocnemum canopy at HHW. The highest samples are dominated by Entzia macrescens, a slender fusiform smaller miliolid, here named Sigmoilina canisdementis sp. nov. and an occasional specimen of Reophax sp. At higher elevations on the landward side of the marsh Entzia macrescens is dominant, whereas in the middle part of the marsh Trochammina inflata becomes dominant, while Ammonia tepida, Trichohyalus, Elphidium, and miliolids increase in abundance in the seaward direction. The sample from edge of the tidal channel at the lower limit of the marsh (T2, sample 10) contains an assemblage of calcareous benthic foraminifera dominated by the rotaliids Ammonia, Elphidium, and the miliolid Peneroplis.

Dead assemblage
The dead assemblage is more diverse compared with the live assemblage and is enriched in various miliolid species, including the larger miliolid genera Peneroplis and Coscinospira. At the landward edge of the marsh the trochamminids dominate the dead assemblage (Figs. 3, 4). The trochamminds are generally well-preserved, and therefore the recovered specimens must have been alive recently. Their relative abundances mirror that of the live assemblage. At the landward end of the transects, Entzia is the dominant genus, then Trochammina becomes dominant in the mid-to lower marsh. The larger specimens of Trochammina at the studied locality sometimes display deformities of the chambers (Plate 1). The proportion of calcareous benthic foraminifera (rotaliids and miliolids) increases in the seaward direction (Figs. 3, 4). In the high marsh, only juvenile specimens of Peneroplis are observed, while in the middle and low marsh adult specimens were found in association with juvenile specimens of Coscinospira. In the mid-to low marsh calcareous forms dominate the dead assemblages, mostly Ammonia, Elphidium, a diverse assemblage of smaller miliolids (mostly Quinqueloculina with rare specimens of Agglutinella, Articulina, Hauerina, Spiroloculina, Sigmoilina, and Triloculina), and Coscinospira 0/1 0/2 0/7 0/2 0/12 0/9 0/4 0/2 0/3 0/9 0/10 S. canisdementis rare specimens of Clavulina, Haynesina, Sorites, and Trichohyalus. Large specimens of Peneroplis are particularly common in sample T2-10 (the edge of the tidal channel at the lower end of the marsh). The genus Sorites is found only in the proximity of the tidal channel in the low marsh.

DISCUSSION
Temperate salt marshes in North America and northwest Europe are characterized by a benthic foraminiferal fauna dominated by agglutinated foraminifera, predominantly trochamminids (Scott & Medioli 1980, Scott et al. 1990, Horton & Edwards 2006). In the British marshes, the species Entzia macrescens occurs near HHW, whereas Trochammina inflata is dominant at in the middle marsh, and Miliammina fusca and various calcareous species characterize the lower marsh elevations and the mud flats (Horton & Edwards 2006).
Miliammina fusca is often also found in tidal channels. North American salt marshes contain more diverse trochamminids, including the genera Arenoparella, Balticammina, Siphotrochammina, and Tiphotrocha, as well as accompanying non-trochammind agglutinated foraminifera such as Reophax, Haplophragmoides and Polysaccammina (Edwards et al. 2004). In Bahrain, the diversity of agglutinated foraminifera is lower that of the North American salt marshes, consisting of only five genera. The composition of the marsh assemblage in Bahrain is more similar to that of the British marshes, with Entzia (= Jadammina in older publications) dominating at the fringe of the high marsh, Trochammina and Reophax extending to the middle marsh, and the agglutinated miliolid genus Agglutinella substituting for Miliammina in the low marsh and muddy tidal flat. Interestingly, the species Agglutinella kaminskii Garrison has the same fusiform shape and probably occupies a similar habitat as Miliammina fusca, but differs in its wall composition (see Garrison 2019). Additionally, Clavulina is found in association with Agglutinella in the low marsh, although at the time of our sampling only dead specimens of these genera were found. The largest adult specimens of Clavulina were observed at the lower edge of the marsh. The species Entzia macrescens has a worldwide distribution and is likely dispersed by birds along their migration pathways (Holzmann & Pawlowski 2017). The island of Bahrain sits squarely within the East Africa -West Asia flyway (Kube et al. 1998: fig. 24, Leblebicioglu et al. 2014: fig. 2). Much of the ornithological research shows migratory flyways via the Gulf and Bahrain heading north and eastward to central Asia and China (Sun et al. 2008, Si et al. 2009, de Fouw et al. 2017. However, there is evidence of flyways heading north and westward from Bahrain (Kube et al. 1998, Leblebicioglu et al. 2014). This bird migration flyway is from East Africa, Yemen, northward to Oman, Bahrain, Kuwait, Iraq, Turkey, Romania, and to other parts of Eastern Europe (Kube et al. 1998: fig. 24, Leblebicioglu et al. 2014: fig. 2). Entzia macrescens probably arrived with birds in Romanian salt ponds but to assume that it is the same cryptic species everywhere along migratory bird routes would necessitate a molecular investigation.
Tubli Bay is a well-known stopover point for migratory shore birds, and we have observed flamingos, egrets, and smaller shore birds at our sample locality. Trochammina inflata also has a worldwide distribution in salt marshes (Scott et al. 1990), although it has not been observed at the Entzia locality in landlocked Transylvania (Kaminski & Filipescu 2011, Telespan et al. 2017. The species has been found in a mangrove-dominated environment in the U.A.E. (Fiorini et al. 2019), but our finding in Tubli Bay in Bahrain is the first report of the species in a salt-marsh environment in the western Arabian Gulf region. Based on the known migration pathway of the oystercatchers, Haematopus ostralegus iongipe, reported by Kube et al. (1998) and the great reed warbler, Acrocephalus arunddinaceus, reported by Leblebicioglu et al. (2014), we might expect to find trochamminids at other salt marshes in the western Gulf region, but this remains to be verified by an expanded survey. At our sampled locality larger specimens often display curious morphological deformities, such as irregular coiling or deformities of the chambers. A few specimens were found that display an abnormally lobate periphery, with radially elongated chambers (Plate 1, Figs. D1, D2). Deformities in peneroplids commonly observed in the Gulf region have been ascribed to extremes in temperature and salinity (Amao et al. 2018, Fiorini & Lokier 2020), but it is not yet clear whether the occurrence of deformities in this population of T. inflata has an underlying environmental cause.

Remarks:
This species had often been reported as "Discorinopsis" aguayoi, even though it clearly has a hyaline calcareous test, and Bermúdez (1935) had originally placed it in the calcareous (rotaliid) genus Discorbis. The genus Discorinopsis is an agglutinated taxon from the Eocene of Florida (Cole 1941). We have recovered several live specimens from our sampled locality. Bermúdez & Seiglie (1963) reported it as abundant in mangrove lagoons in Trinidad and in the Gulf of Cariaco, Venezuela. It is found in marine mangrove ponds in Bermuda (Javaux & Scott 2003) and Brazil (Semensatto 2020). Avnaim-Katav et al. (2017) reported it from a salt marsh in the Tijuana River estuary in southern California.  Förderer & Langer, 2018, p. 132, pl. 49, figs. 1-3. Remarks: Juvenile specimens were living on the salt marsh at the time the samples were collected. Our specimens are plano-convex and are more like the "type 1" variety of Förderer & Langer (2018). Holzmann (2000) and Hayward et al. (2004), have shown that the genus Ammonia contains different phylotypes that may constitute distinct species. Small morphotypes of Ammonia with no distinct ornamentation are called Ammonia tepida by many authors, but according to molecular results they belong to different species (M. Holzmann 2020, personal communication).