Subsurface and Infaunal Foraminifera of Kemaman- Mangrove Swamps, East Coast Peninsular

Malaysia RESEARCH PAPER

ROKIAH SURIADI WAN NURZALIA WAN SAELAN BEHARA SATYANARAYANA SUHAIMI SURATMAN HASRIZAL SHAARI

*Author affiliations can be found in the back matter of this article

ABSTRACT CORRESPONDING AUTHOR: This study analysed the distribution and abundance of dead and live (Rose Bengal Wan Nurzalia Wan Saelan stained) infaunal foraminifera from three short cores taken at three locations in the Faculty of Science and mangrove swamps of Kemaman-Chukai, , . Eighteen agglutinated Marine Environment, taxa were recorded in assemblages dominated by Arenoparrella mexicana, Universiti Malaysia Haplophragmoides wilberti and Miliammina fusca; and of these, only two taxa were Terengganu, MY recorded as live. The distribution of subsurface and infaunal foraminifera varied from [email protected] core to core, as did their depth of occurrence. Core 1 (seaward core) was dominated by sandy deposits, relatively high salinity (32 ppt), and extensive crab mounds, displayed KEYWORDS: very low numbers of dead foraminifera inconsistently throughout the core, while no sediment; bioturbation; infaunal foraminifera were observed, indicating intense bioturbation by mangrove taphonomy; agglutinated; crabs. In Core 2 (middle core), even though the numbers of live foraminifera decreased down-core; palaeo sea-level down-core, the number of dead or subsurface foraminifera were inconsistent, indicating taphonomic loss of the tests. Core 3 (landward core) however, displayed TO CITE THIS ARTICLE: ideal foraminiferal distribution patterns required in the palaeo sea-level reconstruction Suriadi, R, Saelan, WNW, Satyanarayana, B, Suratman, (with less taphonomic loss and decreasing number of infaunal foraminifera down- S, Shaari, H. 2021. Subsurface core). Because of the similarity displayed in the foraminiferal assemblages in the 0–1 and Infaunal Foraminifera of cm and 10–11 cm intervals, the surface sample (0–1 cm) should be an acceptable Kemaman-Chukai Mangrove basis for down-core reconstructions in this study. Live (Rose Bengal stained) infaunal Swamps, East Coast Peninsular foraminifera, though observed at 40–41 cm depth, are not considered abundant enough Malaysia. Open Quaternary, 7: to influence the dead assemblage in the subsurface sediment and its applicability for 5, pp. 1–14. DOI: https://doi. org/10.5334/oq.95 palaeoenvironmental and sea-level reconstructions. Therefore, it is possible for palaeo sea-level to be reconstructed based on foraminiferal assemblages preserved in the Kemaman-Chukai mangrove swamps. Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 2

INTRODUCTION study sites, the mangrove sediments are muddy and soft and therefore, the term infaunal (shallow and deep) is Salt marsh foraminifera have been utilized by used to represent our foraminiferal mode of living. many authors as an excellent biological proxy for Abundance and distribution patterns of infaunal palaeoenvironmental studies, including precise foraminifera vary considerably from site to site, due Holocene sea-level indicators (e.g., Scott & Medioli to local environmental conditions and bioturbation 1978; Gehrels 1994; Scott, Medioli & Schafer 2004). (Culver & Horton 2005). In temperate regions, infaunal The understanding of former sea-levels based on the foraminifera have been reported at a depth of 60 cm in interpretation of foraminiferal assemblages requires Delaware salt marshes (Hippensteel et al. 2000) and at a that their relationship to tidal elevation is known (Scott depth of 50 cm in New England salt marshes (Saffert & & Medioli 1978; Horton, Edwards & Llyod 1999; Horton Thomas 1998). At a site that was located around ~150 & Edwards 2006), and it differs among sites and regions km north from this present study, Culver et al. (2013) (Kemp et al. 2013). Recently, a transfer function has reported the first infaunal foraminiferal occurrences in been developed based on the statistically significant Malaysia and the deepest in this region; 78–80 cm in Setiu relationship between foraminiferal assemblages estuary and lagoon. In comparison with salt marshes in (modern data sets) and elevation with respect to the temperate regions, mangrove foraminifera from tropical tidal frame (e.g., Gehrels 2000; Horton, Edwards & environment received less attention even though Llyod 1999; Horton & Edwards 2006; Leorri, Horton & intertidal zonation was proven to be established (Haslett, Cearreta 2008; Kemp et al. 2013), which can be used 2001; Horton et al. 2005). This study therefore, aimed to to infer the former heights of fossil salt marsh deposits document the dead and living infaunal populations of (Berkeley et al. 2007). An ideal modern foraminiferal foraminifera from a tropical mangrove environment and assemblage to be used in sea-level studies must be their taphonomic inferences. shown to correspond to environmental gradients, to be autochthonous and must remain compositionally similar with their subsurface (dead) assemblages throughout REGIONAL SETTING the core (Horton & Edwards 2006; Berkeley et al. 2007; Edwards & Wright 2015). In the of Terengganu, east coast Dead subsurface assemblages that accurately reflect Peninsular Malaysia, mangrove swamps are highly the dead surface assemblage indicate low taphonomic distributed in estuaries and along tidal segments of rivers processes (Horton & Edwards 2006) and suitability to be in Chukai, Kertih, Kemaman and (Figure 1). Due to used in palaeoenvironmental studies. However, other higher wave energy from the South China Sea, mangrove studies reported that occurrences of infaunal foraminifera swamps are less extensive along the east coast than could influence the composition of dead assemblages the west coast of Peninsular Malaysia (Husain & Yaakob in subsurface sediments and lead to erroneous 1995; Husain & Sulong 2001; Sulong et al. 2002). The conclusions regarding their original composition (e.g., relatively pristine mangrove swamps have been gazetted Goldstein & Harben 1993; Goldstein, Watkins & Kuhn as a mangrove forest reserve by the Terengganu Forestry 1995; Saffert & Thomas 1998; Culver & Horton 2005; Department. The dominant mangrove species includes Horton & Edwards 2006; Culver et al. 2013), which Rhizophora, Avicennia and Xylocarpus spp. (Sulong et al. resulted in biased interpretation of palaeo sea-level and 2002; Kamaruzzaman & Ong 2008; Shaari et al. 2020). palaeoenvironmental studies. In this context, subsurface The wet equatorial climate of the study area is dead assemblages should therefore be evaluated characterized by high temperatures and seasonally heavy to optimize the accuracy of palaeoenvironmental rainfall, especially during the annual northeast monsoon interpretations (Goldstein & Harben 1993). from November to January. The mean maximum and Goldstein et al (1995) characterized the mode of living minimum annual temperatures are 32.7°C and 24.2°C of salt marsh foraminifera into three; 1) predominantly respectively, and in Peninsular Malaysia, the total rainfall epifaunal (allogromiinans, most monothalamous recorded is between 1800 mm to 3900 mm (Malaysian agglutinated taxa, and miliolids); 2) shallow to Meteorological Service 2019). Tides are asymmetric but intermediate infaunal (0–5 cm or 9–11 cm) (e.g., predominantly diurnal with a mean tidal range of 1.8 m. Ammonia beccarii, Miliammina fusca, Pseudothurammina During the highest astronomical tides, tidal range can limnetis, Ammotium salsum, Ammobaculites dilatatus, exceed 2 m. Tidal intrusion into the rivers can reach up Reophax nana, Textularia palustris, Siphotrochammina to 20 km (Kamaruzzaman 1994). Sedimentation rates lobata, Trochammina inflata, and T. macrescens); and 3) within the Kemaman-Chukai mangroves range from 0.9 deep infaunal (deeper than 10 cm) (e.g., Arenoparrella to 1.1 cm year–1 (Kamaruzzaman & Ong 2008). Sediment mexicana, Haplophragmoides wilberti). However, the characteristics are influenced by monsoon season, distinction between epifaunal and shallow infaunal may where sand content is higher during dry season and finer be negligible if the sediment is soft (Murray, 2003). In our sediment is dominant during wet season (Ong et al. 2012). Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 3

Figure 1 Location of the study area: A) showing some of the mangrove swamp areas in Peninsular Malaysia (Larut Matang and Kapar in the west coast of Peninsular, Setiu and Kemaman-Chukai in the east coast of Peninsular). Arrow indicates the location of Kemaman-Chukai; B and C) showing the location of the three sites selected in the present study; Core 1, Core 2, Core 3.

MATERIAL AND METHODS running tap water within 36 hours of collection SAMPLE COLLECTION AND ANALYSES (usually much less). Caution must be exercised, as the Field sampling in the Kemaman Forest Reserve was agglutinants are known to be very fragile and to avoid conducted in July 2009. Three sites were selected loss of foraminifera during the procedure. After washing (Table 1 and Figure 1); Core 1 (seaward core) was located over 600 and 63 µm sieves to remove coarse material and on the northern part of Che Wan Dagang Island near the mud, the sample fractions retained on the small sieve confluence of the Kemaman and Chukai rivers (Figure 1). were preserved in 10% formalin and 0.1% Rose Bengal Core 2 (middle core) and Core 3 (landward core) were (Walton 1952) mixture for preservation and staining located about 2 km and 4 km, respectively, up the Chukai of live foraminifera for about two to three weeks. The River (Figure 1). Rose Bengal method remains the most practical way to Cores were collected using a D-section (Russian) corer quantify living foraminiferal fauna (Martin 2000) and can (50 cm) during low tide and from muddy substrates for lead to 96% correct identifications (Lutze & Altenbach easy penetration of the corer (Figure 2). Coring sites were 1991). Live specimens were identified by the presence also established far from root systems and crab mounds of Rose Bengal stained protoplasm in their test (Wang et whenever possible. Due to the lithological homogeneity al. 2016). Only specimens with >50% stained test were of the sediment throughout the core, the cores were considered as living. sectioned at every 10 cm (e.g., 0–10 cm), and each section were divided into two parts (vertically) for foraminiferal LABORATORY ANALYSIS FOR FORAMINIFERA and environmental analyses purposes. For foraminiferal Before picking procedure started, samples were washed analysis, 10 g of sediment were subsampled from the again in tap water to remove the formalin. Preserved top 1 cm of each section, wrapped in polythene sample foraminiferal samples were poured onto a petri dish bags, and labelled (e.g., C1S1 = Core 1, subsample 0–1 and the foraminifera were picked in a wet medium, cm). sorted and identified. Living and dead specimens were To avoid bacterial oxidation and destruction of the counted separately to provide information on living organic wall of the foraminiferal test, all foraminiferal microfauna (Debenay, Guiral & Parra 2002). Due to the sediment samples were gently washed under slow- very low foraminiferal density, less than 300 individuals Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 4 0/0 0.9/0 0.9/0 0.9/0 0/0 0.8/0 0.7/0 0.6/0 0.8/0 0.6/0.7 0.5/1.0 0.5/0 0.7/1.0 0.7/0 1.0/0 LIVE) (DEAD/ (DEAD/ J’ 0/0 0.6/0 0/0 1.6/0 1.5/0 1.7/0 1.8/0 1.7/0 1.4/0 1.8/0 1.5/0.5 1.2/0.7 1.4/0 1.6/0.7 1.8/0 H’ LIVE) (DEAD/ (DEAD/ 0/0 0.9/0 0/0 4.6/0 4/0 10.9/0 3.5/0 3.2/0 3.4/0 3.1/0.6 3.1/0 3.2/1.2 3.8/0 2.6/0 2.4/0.7 (DEAD/ (DEAD/ LIVE) α 6/0 6/0 9/1 9/0 5/0 1/0 1/0 10/1 12/1 13/2 10/2 12/0 12/0 14/0 2/0 LIVE) S (DEAD/ (DEAD/ 0 0 0 0 0 0 0 0 47.4 50 Total: 0 Total: 100 Total: 100 Total: 16.7 13.2 10.5 33.3 28.9 DOWN-CORE DOWN-CORE SPECIMENS % OF LIVE % OF LIVE 0 0 0 0 0 0 0 0 4 5 Total: 0 Total: 6 Total: 38 Total: 1 18 11 3 2 NO. LIVE NO. LIVE SPECIMENS 45.7 5.7 Total: 100 Total: 100 Total: 100 Total: 15.9 18.9 19.3 17.9 18.9 2.9 20.0 25.7 24.6 27.2 2.9 29.3 25.0 DOWN-CORE DOWN-CORE SPECIMENS SPECIMENS % OF DEAD % OF DEAD 8 81 68 9 44 Total: 35 Total: 276 Total: 777 Total: 1 16 194 147 150 139 147 2 7 75 NO. DEAD NO. DEAD SPECIMENS Nypa Rhizophora Rhizophora fruticans Xylocarpus apiculata apiculata granatum, DOMINANT DOMINANT VEGETATION 4.9 5.4 5.7 5.1 5.9 5.6 5.9 5.4 5.4 5.1 5.9 5.7 5.7 5.8 5.7 (%) TOC Muddy sand Muddy sand Mud Muddy sand Mud Muddy sand Sand Sandy mud Sandy mud Sandy mud Sandy mud Sandy mud Sandy mud Sandy mud Sandy mud SEDIMENT SEDIMENT CLASSIFICATION 1.7 1.2 2 ELEVATION ELEVATION MSL (M) 32 28 28 SALINITY SALINITY (PPT) 0–1 0–1 0–1 40–41 40–41 40–41 10–11 10–11 10–11 30–31 30–31 30–31 20–21 20–21 20–21 19’”N, 103°25’26”’E) DEPTH DEPTH SUBSAMPLE SUBSAMPLE INTERVAL INTERVAL (CM) ’ Location, depth interval, salinity, elevation level relative to mean sea-level (MSL), sediment types, total organic carbon, dominant vegetation, number of dead and live foraminifera and diversity and diversity foraminifera number of dead and live vegetation, dominant carbon, organic types, total (MSL), sediment to mean sea-level relative level salinity, elevation depth interval, Location, Core 1 (04°14’39’’N, 103°25’53’’E) Core C1S1 C1S2 C1S3 C1S4 C1S5 2 (04°15 Core C2S1 C2S2 C2S3 C2S4 C2S5 3 (04°15’6”’N, 103°25’2”’E) Core C3S1 C3S2 C3S3 C3S4 C3S5 indices of 15 sediment subsamples taken from three cores in the Kemaman-Chukai mangrove swamp. swamp. mangrove in the Kemaman-Chukai cores three from subsamples taken indices of 15 sediment Table 1 Table Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 5

Figure 2 Root systems of Rhizophora apiculata (A) and Xylocarpus granatum (B) at the sampling sites. Subset C showing a huge (±1 m height) crab mound found at the seaward site (Core 1) of Kemaman-Chukai mangrove. Yellow arrow in subset D showing soft and muddy sediment were sampled using a D-section (Russian) corer during low tide. were picked in each sample. Foraminifera were identified DATA ANALYSES to the species level following Loeblich & Tappan 1964; Shannon-Wiener Information Function (H’) and Fisher’s Whittaker & Hodgkinson 1979; Oki 1989; Hottinger, alpha index (α) were used to measure the species Halicz & Reiss 1993; and Culver et al. 2013. diversity indices. Pielou’s evenness index (J’) was used to describe how individuals were divided among ENVIRONMENTAL PARAMETERS species; the greater the dominance of one species, the Pore water salinity data were obtained by collecting lower the value of evenness. Values of H’, α, and J’ were water from crab holes and small ditches at every calculated using PRIMER version 6.1.12 (Clarke & Gorley coring site and measured using a handheld salinity 2006). refractometer. The land elevation in relation to mean sea-level (MSL) was determined using a TOPCON® (AT-G7 N, Japan) dumpy level surveying equipment. The grain RESULTS size analysis was carried out through laser diffraction method (Malvern Particle Size Analyser) and then The 15 sediment core subsamples collected from followed the Folk’s (1954) classification. However, in the Kemaman-Chukai mangrove swamps contained 18 case of seaward samples with a high sand fraction, the agglutinated taxa, while no presence of calcareous dry sieving method using British Standard sieves (63 µm) hyaline and calcareous porcelaneous were recorded was employed. The oxidation dichromate acid technique (Table 2). The number of dead and live foraminifera (Holme & McIntyre 1971) was used for total organic recovered varied from core to core, as did their depth of carbon (TOC) analysis. occurrence. Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 6 D/L 0/0 0/0 0/0 0/0 66/0 6/0 40–41 5/0 5/0 1/0 1/0 147/4 3/0 3/0 2/0 2/0 23/0 2/0 21/4 7/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 8/0 65/2 1/0 11/3 139/5 30–31 34/0 3/0 2/0 2/0 2/0 2/0 2/0 7/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 87/0 9/0 5/0 1/0 1/0 1/0 1/0 1/0 1/0 150/0 3/0 33/0 20–21 7/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 CORE 3 98/5 4/0 4/0 10–11 18/0 11/6 1/0 147/11 3/0 3/0 3/0 2/0 D/L 0–1 0/0 0/0 0/0 0/0 0/0 6/0 108/3 19/0 1/0 1/0 194/18 3/0 3/0 3/0 3/0 34/15 3/0 3/0 7/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 40–41 4/0 44/0 5/0 1/0 19/0 1/0 3/0 2/0 2/0 7/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 81/1 43/1 4/0 1/0 1/0 1/0 13/0 15/0 1/0 30–31 2/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 CORE 2 8/0 1/0 1/0 1/0 1/0 20–21 2/0 2/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 6/0 10–11 1/0 1/0 1/0 13/0 1/0 10/2 3/0 32/0 3/0 2/0 2/0 75/2 D/L 0–1 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 68/3 9/3 5/0 1/0 1/0 1/0 31/0 3/0 3/0 7/0 7/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 40–41 2/0 2/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 9/0 1/0 1/0 30–31 3/0 2/0 2/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 CORE 1 CORE 1 5/0 20–21 2/0 7/0 D/L 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 6/0 10–11 1/0 16/0 3/0 3/0 2/0 D/L 0/0 0–1 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 1/0 1/0 . sp sp. sp. A sp. B → sp. sp. ↓ Foraminiferal census data for dead and live specimens in 15 sediment subsamples taken from three cores in the Kemaman-Chukai mangrove swamp. D = dead, L live. swamp. mangrove in the Kemaman-Chukai cores three from subsamples taken specimens in 15 sediment dead and live for census data Foraminiferal Bruneica clypea Bruneica Entzia manilaensis Haplophragmoides wilberti Haplophragmoides Paratrochammina Miliammina obliqua Miliammina fusca Depth (cm) Caronia exilis Caronia Acupeina triperforata salsa Ammoastuta Ammotium pseudocassis Ammotium salsum Ammotium mexicana Arenoparrella Siphotrochammina Siphotrochammina Taxa specimen/10 g Total Trochammina inflata Trochammina Trochammina Trochammina Table 2 Table Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 7

CORE 1 (SEAWARD CORE) Throughout the core, dead specimens were more Sandy sediment characterized the top 30 cm of Core 1 abundant (98%) than live foraminifera (2%) (Figure 3). and below 30 cm downwards, the sediment changed to The number of dead foraminifera was the highest in sandy mud (Table 1). Salinity at coring site was 32 ppt and the 30–31 cm interval (81 specimens/10 g of sediment), elevation level was 1.7 m (MSL). Mangrove vegetation at while the lowest was in the 20–21 cm interval (8 the core site was dense and dominated by Rhizophora specimens/10 g of sediment) (Table 1). A very low apiculata. Total organic carbon (TOC) ranged from 4.9– number of live/infaunal foraminifera was recorded in the 5.9 (Table 1). Intense crab mounds were observed in the 0–1 cm, 10–11 cm and 30–31 cm interval (3, 2 and 1 vicinity of the coring site. specimen/10 g of sediment respectively). S values varied No live (Rose Bengal stained) or infaunal foraminifera from 6–12 in dead foraminifera and 2 in live foraminifera; were recorded throughout the core. The number of dead α values ranged from 2.6–10.9 in dead foraminifera and foraminifera was the highest in the 10–11 cm interval 0 in live foraminifera; H’ values recorded from 1.4–1.8 in (16 specimens/10 g of sediment), while the lowest was dead foraminifera and 0 in live foraminifera; J’ values recorded in the 0–1 cm and 40–41 cm interval (1 and ranged from 0.6–1 in dead foraminifera and 0 in live 2 specimen/10 g of sediment respectively) (Table 1). foraminifera (Table 1). Seventeen taxa were recorded, Below the 10–11 cm interval, the number of foraminifera mainly dominated by Arenoparrella mexicana and decreased with increasing depth (except in 30–31 cm followed by Miliammina fusca (Table 2). Live Miliammina interval). Species richness (S) varied from 1–6, Fisher’s fusca occurred in the upper part of the core down to the Alpha value ranged from 0.9–4.6, Shannon-Wiener 10–11 cm interval (Figure 4). Live Arenoparrella mexicana diversity index (H’) values recorded from 0.6–1.6, and the however, was found living relatively deeper in the core Evenness (J’) value in Core 1 was 0.9 (Table 1). Eight taxa (30–31 cm interval) in a very low abundance (Figure 4). were found in low abundance and mainly dominated by Only these two taxa were recorded as live foraminifera Arenoparrella mexicana (Table 2). in Core 2.

CORE 2 (MIDDLE CORE) CORE 3 (LANDWARD CORE) Core 2 was characterized by muddy sediment, except in Muddy sediment was observed throughout the core but the 20–41 cm interval (Table 1). Salinity was 28 ppt and sandier in the 30–31 cm interval (Table 1). Salinity was elevation level was 2.0 m (MSL). Rhizophora apiculata 28 ppt and elevation level was 1.2 m (MSL). Mangrove dominated the vegetation in Core 2 and TOC ranged from vegetation was dominated by Xylocarpus granatum and 5.1–5.9. Fewer crab mounds were observed in this coring Nypa fruticans. TOC ranged between 5.7–5.9 and no crab site when compared to Core 1. mounds were observed in this coring site.

Figure 3 Relative abundance of dead and live foraminiferal assemblages in all cores taken at three locations in the Kemaman-Chukai mangrove swamp. Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 8

Figure 4 A and B showing number of live specimens/10 g of sediment throughout the cores.

In comparison, the number of dead and live thus resulting in a very low abundance of common foraminifera in Core 3 were higher than recorded in Core mangrove taxa throughout the core (e.g., Arenoparrella 1 and 2 (Figure 3). Number of dead specimens/10 g of mexicana and Miliammina fusca). Even though Core 1 is sediment were much higher (95%) than numbers of live located at a site closer to the sea with high salinity, there foraminifera (5%) (Figure 3). The highest number of dead were no calcareous taxa recorded either. foraminifera was recorded in the 0–1 cm interval (194 The transition between the front (Core 1) and middle specimens/10 g of sediment) and decreased down-core. and high mangrove (Core 2 and 3) corresponds to an A notable increase in the number of live foraminifera increase in the relative abundance of the most dominant was observed in Core 3 and they were found down to taxa; Arenoparrella mexicana, Haplophragmoides wilberti the 40–41 cm interval (Figure 3). Peak concentrations and Miliammina fusca. In Core 2 and 3, Arenoparrella of living foraminiferal populations occurred in upper mexicana consistently dominated the assemblages 1 cm sediment (18 specimens/10 g of sediment) and (relative abundance >40% at all intervals, except in Core later decreased down-core (Figure 3). Similar to Core 2, at 20–21 cm interval). In Core 3, the agglutinated 2, only Arenoparrella mexicana and Miliammina fusca species were represented by a more diverse assemblage were found living infaunally in the sediment (Figure 4). S compared to Core 2 despite having similar salinity range values varied from 10–14 in dead foraminifera and 2 in and sediment characteristics (but lower elevation was live foraminifera; α values ranged from 2.4–3.8 in dead observed in Core 3; 1.2 m MSL and 2.0 m MSL in Core foraminifera and 0.6–1.2 in live foraminifera; H’ values 2). Acupeina triperforata, Ammotium pseudocassis, recorded from 1.2–1.8 in dead foraminifera and 0.5–0.7 Ammoastuta salsa and Trochammina spp. were among in live foraminifera; J’ values ranged from 0.5–0.7 in taxa with higher number of specimens recorded in Core dead foraminifera and 0.7–1 in live foraminifera (Table 1). 3 but low in Core 2. Seventeen taxa were recorded, mainly dominated by Generally, the distributions of intertidal foraminifera Arenoparrella mexicana, followed by Haplophragmoides can be divided into two zonations, 1) calcareous wilberti and Miliammina fusca (Table 2). Scanning Electron assemblage that dominates the mudflats and sandflats Microscope (SEM) images of some dominant taxa are of the intertidal zone and 2) agglutinated assemblage illustrated in Figure 5. that is distributed in the vegetated marsh (Horton et al. 2005). These zonations were formed as direct function of elevation, with the duration and frequency of intertidal DISCUSSION exposure as the most crucial environmental factors SPATIAL AND VERTICAL DISTRIBUTION (Horton et al. 2005). Arenoparrella mexicana, Miliammina PATTERNS OF FORAMINIFERA fusca, Trochammina inflata, Ammobaculites exiguus, Total population of foraminifera (dead and live) were Haplophragmoides wilberti, Caronia exilis and Bruneica low in the seaward core (Core 1) and higher at the clypea were among agglutinated taxa observed in the two cores (Cores 2 and 3) from the more inland sites landward margins of salt marsh and mangrove swamps (Tables 1, 2; Figure 3). Core 1 located closer to the high worldwide (Horton et al. 2005; Murray, 2006; Berkeley wave energy of the South China Sea and with relatively et al. 2008; Culver et al. 2013). Assemblages dominated high salinity (32 ppt), was dominated by sandy deposits. by Caronia exilis, Siphotrochammina lobata, Ammotium Intense environmental stress at this site may destroy directum, and Ammobaculites exiguus, were recorded by most tests and reduce the number of living individuals Culver et al. (2013) in the high swamp of Setiu estuary especially in the 0–1 cm sample. This environment was and lagoon, Malaysia. Horton et al. (2005) identified not favourable for agglutinated foraminifera to flourish, high abundances of Arenoparrella mexicana, Miliammina Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 9

Figure 5 Scanning Electron Microscope images of some foraminiferal species identified from Kemaman-Chukai mangroves. Scale bars = 100 μm. 1 = Arenoparrella mexicana (Kornfeld, 1931) a) ventral b) side; 2 = Haplophragmoides wilberti (Andersen, 1953) a) dorsal b) side; 3 = Miliammina fusca (Brady, 1870); 4 = Acupeina triperforata (Millett, 1899) a) side b) aperture; 5 = Bruneica clypea (Brönnimann, Keij and Zaninetti, 1983) a) dorsal b) ventral; 6 = Paratrochammina sp. (Brönnimann, 1979, emended Brönnimann and Whittaker, 1986); 7 = Ammotium pseudocassis (Cushman and Brönnimann, 1948).

fusca, Miliammina obliqua and Trochammina inflata at the between cores and contributed only slightly (relative landward edge of the mangroves of Kadelupa, Indonesia. abundance) to the total assemblage; 0% in Core 1; 2% in Core 2; and 5% in Core 3. Only two out of eighteen INFAUNAL FORAMINIFERA AND taxa were observed living in the infaunal habitat MICROHABITATS IN THE KEMAMAN-CHUKAI (Arenoparrella mexicana and Miliammina fusca) with very MANGROVE low abundances (Figure 4). The number of infaunal foraminifera in this study varied Diversity values (number of specimens and species according to depth in the cores analysed, as well as richness) were much lower compared to the adjacent Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 10 mangrove of Setiu estuary and lagoon. Culver et al. Even though the abundance of infaunal foraminifera in (2013) reported nine taxa with >20 live specimens; the study area decreased with increasing depth, they were Ammobaculites exiguus (95 specimens), Bruneica clypea found to live deeper at the upper/landward mangrove (92), Siphotrochammina lobata (51), Arenoparrella site (Core 3) and shallower in the site closer to the sea mexicana (46), Caronia exilis (35), Trochammina inflata (Core 2) (Figures 3 and 4). These microhabitat preferences (29), Miliammina petila (25), Ammotium directum (23) correspond well with those found in the tropical intertidal and Haplophragmoides wilberti (22). In this study, only environment of Cocoa Creek, Queensland, Australia Miliammina fusca showed the highest number of live (Berkeley et al. 2008) where species observed living in the specimens; 33 specimens (Figure 4). This discrepancy distal mangrove area had deeper living habits than those may be resulted from different sample interval (2 found in the proximal mangrove and mudflat sediments. cm in Culver et al. 2013 and 10 cm in the present More than 50% of the total population of infaunal study). Culver et al. (2013) also reported the deepest foraminifera in Core 2 and 3 were found in the upper 11 infaunal occurrence in Malaysia so far (78–80 cm depth cm of the core (Figures 3 and 4). Thus, foraminifera living interval, 11 specimens/20 cm3 of sediment) and was in the 0–11 cm interval are considered to be shallow characterized by Bruneica clypea, Trochammina inflata infaunal and those dwelling deeper than 11 cm are and Siphotrochammina lobata. considered to be deep infaunal. This classification was Throughout the cores (Core 2 and 3), the abundance based upon Culver & Horton (2005); and Leorri & Martin of infaunal foraminifera decreased with increasing depth (2009). In the Setiu estuary and lagoon (Culver et al. (Table 2, Figure 3). The highest abundance of infaunal 2013), shallow infaunal foraminifera were described as foraminifera was found in the upper 11 cm of Core 3, those living in the 0–16 cm interval, slightly deeper than where they contributed 71.7% of the total infaunal this present study. population in this core. Even though the maximum depth where they were found alive (Rose Bengal stained) was BIOTURBATION AND TAPHONOMIC at 40–41 cm (Core 3), their relative abundance in this INFERENCES interval constituted only 12.3% of the total infaunal Foraminifera represent an important potential food source population. for many organisms, including flatworms, polychaetes, Infaunal foraminifera were found at sites with muddy gastropods, bivalves and crustaceans because they are (Core 2 and 3) rather than sandy sediments (Core commonly present in great abundance in the water 1) (Table 1). However, contrary to our results, Horton column, on the sea floor (Culver & Lipps 2003) and in the & Edwards (2006) reported a greater percentage of sediment (including mangrove-fringed estuary) (Stoner infaunal foraminifera in the sandier substrates of the and Zimmerman, 1988). Predatory activities by these tidal flat environment of Rusheen Bay, Ireland, with no organisms undoubtedly causes taphonomic changes in occurrence of infaunal foraminifera were recorded in the foraminiferal assemblages as they fossilize and it varies high, middle and low marsh environments which was from environment to environment (Culver & Lipps 2003). dominated by silty sediment. Berkeley et al. (2008) listed Core 1 displayed significant evidence of bioturbation three important factors that contribute to the depths at processes. Intense crab mounds at this site defined active which foraminifera can live: 1) sediment oxygenation predation by mangrove/fiddler crabs and increased the – coarser substrates are associated with deeper possibility of reworked sediment (by crabs burrowing oxygenated layer and therefore, favours the down-core deep into the sediment). In Core 2, the abundance of distribution of infaunal foraminifera (Goldstein & Harben foraminifera at 20–21 cm depth was surprisingly low 1993); 2) bioturbation – by falling into tubes or burrows compared to super- and sub-jacent horizons (Figure 3). (Green, Aller & Aller 1993) or by deep burrowing activity This could be a result of taphonomic removal of many of foraminifera to avoid predation e.g., crustaceans, of the foraminifera originally dwelling at that site at gastropods, polychaetes (Lipps 1983); and 3) organic the time of sediment accumulation. It could also result matter flux – food source for foraminifera. In this regard, from increased sedimentation rate possibly related to a the presence of infaunal foraminifera in Core 3 (with major runoff event or storm surge. Thus, further study muddy sediment and less crab mounds observed) may is suggested to understand the possible reasons behind be a response to organic matter availability rather than the taphonomic loss of foraminifera in this study area, sediment oxygenation and bioturbation. On the other especially from this specific depth interval. hand, no live/infaunal foraminifera occurrences in Core Comparison between distribution of live population 1 may be resulted from bioturbation process by fiddler/ and dead assemblages of foraminifera provides insights mangrove crabs as observed from intense crab mounds in into the taphonomic loss of foraminiferal specimens the surrounding area. Similar results have been observed (Culver et al. 2013). In landward core (Core 3), numbers in Bombay Hook marshes, USA where low abundances of live specimens/10 g of sediment decreased down- of infaunal foraminifera were observed in areas with core (Table 1 and Figure 4), but the numbers of dead extensive crab mounds (Leorri, Horton & Cearreta 2008). specimens were high throughout the core length (despite Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 11 the down-core percentage of dead specimens was Our results derived from Core 3 resemble those from reduced by 6% in the 10–11 cm interval) (Table 1). Below the mangrove of Setiu estuary and lagoon (Culver et al. 11 cm, the relative abundance of dead assemblages 2013). Based on a comparison with the Setiu estuary and remained consistent (97–100%) (Figure 3). Similar taxa lagoon data, the dead assemblage in this present study (Arenoparrella mexicana, Haplophragmoides wilberti was formed in the 0–11 cm interval, slightly shallower and Miliammina fusca) characterized the upper 1 cm than the two Setiu high-swamp cores. This interval was and subsurface assemblages. This pattern, suggesting thin enough to produce multi-decadal to centennial-scale less taphonomic loss down core compared to seaward temporal resolution reconstructions (which equivalent (Core 1) and middle core (Core 2). Although the number to C-14 age resolution), based on the Pb-210 derived of Miliammina fusca (specimens/10 g of sediment) sedimentation rate of ~0.3 cm yr–1 (Culver et al. 2013). was irregular down core (Table 2), this patchiness was Because of the similarity displayed in the foraminiferal compensated by increased number of specimens of assemblages in the 0–1 cm and 10–11 cm intervals, Haplophragmoides wilberti. This pattern was believed to surface sample (0–1 cm) should be an acceptable basis be an environmentally driven assemblage change rather (Culver et al. 2013) for down core reconstructions in this than taphonomic activity (Culver et al. 2013). present study. The preservation potential of Miliammina fusca in the core of this present study was in contrast to the Setiu estuary and lagoon, Malaysia (Culver et al. 2013). CONCLUSION Generally, Miliammina fusca was listed as one of the taxa that are less likely to be preserved. The non-mineralized, Agglutinated taxa dominated our samples with no organic cement of the test of Miliammina fusca make records of calcareous foraminifera. In general, species them susceptible to degradation (Lipps 1971). In Setiu found in this present study were common and similar estuary and lagoon samples (e.g., SET10 SET1), two dead with mangrove foraminifera worldwide. Bioturbation specimens of Miliammina fusca/20 cm3 of sediment was and taphonomic loss were intense in seaward (Core 1) recorded from 38–40 cm interval but our result showed and middle core (Core 2). High-mangrove-swamp core better preservation (21 specimens/10 g of sediment in (Core 3) was proven to be the optimum site for sea-level the 40–41 cm interval) (Figure 3). or palaeoenvironmental research in this region and is in agreement with other infaunal foraminiferal study from IMPLICATIONS FOR SEA-LEVEL Malaysian mangrove swamps. RECONSTRUCTIONS Foraminifera have been an excellent biological proxy in evaluating the significance of recent changes in ADDITIONAL FILE relative sea-level, since they are capable of bridging the gap between short instrumental records (e.g., tide The additional file for this article can be found as follows: gauges) and longer term geological data (Shennan et al. 2015; Edwards & Wright 2015). Spatial variability • Lay Summary. Mangrove foraminifera as a key to the in the composition, elevation and vertical range of past sea-level. DOI: https://doi.org/10.5334/oq.95.s1 foraminiferal zonation provides fundamental constraints on the application of an assemblage zone approach to the reconstruction of former relative sea-level (Horton & ACKNOWLEDGEMENTS Edwards 2006). In this study, distribution patterns of subsurface and We thank the Institute of Oceanography and Environment infaunal foraminifera in the Kemaman-Chukai mangrove (INOS) staff for providing technical support, Kemaman swamps differ from core to core. In seaward core Forestry Department, and postgraduate comrades for (Core 1 with extensive crab mounds), numbers of dead their help in the field. We also thank Prof. Dr. Stephen foraminifera were very low and inconsistent throughout Culver from East Carolina University who kindly assisted the core, with no infaunal foraminifera were observed, us with foraminiferal identification and manuscript indicating intense bioturbation by mangrove crabs. In revision. Core 2 (middle core), even though the numbers of live foraminifera decreased down core, the number of dead specimens were inconsistent especially in the 20–21 FUNDING INFORMATION cm interval, indicating taphonomic loss of specimens. Core 3 (landward core) however, displayed an ideal This project was funded by the Higher Institute Centre foraminiferal distribution patterns required in the palaeo of Excellence (HICoE) Grant (Vote No. 66928) awarded sea-level reconstruction (with less taphonomic loss and to Institute of Oceanography and Environment (INOS), decreasing number of infaunal foraminifera down core). Universiti Malaysia Terengganu and Fundamental Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 12

Research Grant Scheme (FRGS/1/2018/WAB09/ York: Kluwer Academic/Plenum Publishers. DOI: https://doi. UMT/02/3) provided by Ministry of Higher Education org/10.1007/978-1-4615-0161-9_2 Malaysia. Debenay, J–P, Guiral, D and Parra, M. 2002. Ecological factors acting on the microfauna in mangrove swamps. The case of foraminiferal assemblages in French Guiana. Estuarine, COMPETING INTERESTS Coastal and Shelf Science, 55: 509–533. DOI: https://doi. org/10.1006/ecss.2001.0906 The authors have no competing interests to declare. Edwards, R and Wright, A. 2015. Foraminifera. In Shennan, I, Long, AJ and Horton, BP (eds.) Handbook of sea level research. John Wiley and Sons, UK. 191–217. DOI: https:// AUTHOR AFFILIATIONS doi.org/10.1002/9781118452547.ch13 Rokiah Suriadi orcid.org/0000-0001-9075-2094 Folk, RL. 1954. The distinction between grain size and mineral Institute of Oceanography and Environment, Universiti Malaysia composition in sedimentary rocks. Journal of Geology, 62: Terengganu, MY 344–359. DOI: https://doi.org/10.1086/626171 Wan Nurzalia Wan Saelan orcid.org/0000-0002-5876-9571 Gehrels, WR. 1994. Determining relative sea-level change from Faculty of Science and Marine Environment, Universiti Malaysia salt marsh foraminifera and plant zones on the coast of Terengganu, MY Maine, U.S.A. Journal of Coastal Research, 10(4): 990–1009. Behara Satyanarayana orcid.org/0000-0003-4191-2607 Gehrels, WR. 2000. Using foraminiferal transfer functions to Institute of Oceanography and Environment, Universiti Malaysia produce high-resolution sea-level records from salt-marsh Terengganu, MY deposits, Maine, USA. Holocene, 10: 367–376. DOI: https:// Suhaimi Suratman orcid.org/0000-0002-1115-5361 doi.org/10.1191/095968300670746884 Institute of Oceanography and Environment, Universiti Malaysia Terengganu, MY Goldstein, ST and Harben, EB. 1993. Taphofacies implications of infaunal foraminiferal assemblages in a Georgia salt Hasrizal Shaari orcid.org/0000-0002-7738-3885 Faculty of Science and Marine Environment, Universiti Malaysia marsh, Sapelo Island. Microplaeontology, 39(1): 53–62. DOI: Terengganu, MY https://doi.org/10.2307/1485974 Goldstein, ST, Watkins, GT and Kuhn, RM. 1995. Microhabitats of salt marsh foraminifera: St. Catherines Island, Georgia, REFERENCES USA. Marine Micropaleontology, 26: 17–29. DOI: https://doi. org/10.1016/0377-8398(95)00006-2 Berkeley, A, Perry, CT, Smithers, SG and Horton, BP. Green, MA, Aller, RC and Aller, JY. 1993. Carbonate 2008. The spatial and vertical distribution of living dissolution and temporal abundances of foraminifera (stained) benthic foraminifera from a tropical, intertidal in Long Island Sound sediments. Limnology and environment, north Queensland, Australia. Marine Oceanography, 38: 331–345. DOI: https://doi.org/10.4319/ Micropaleontology, 69: 240–261. DOI: https://doi. lo.1993.38.2.0331 org/10.1016/j.marmicro.2008.08.002 Haslett, SK. 2001. The palaeoenvironmental implications of the Berkeley, A, Perry, CT, Smithers, SG, Horton, BP and distribution of intertidal foraminifera in a tropical Australian Taylor, KG. 2007. A review of the ecological and estuary: a reconnaissance study. Australian Geographical taphonomic controls on foraminiferal assemblage Studies, 39(1): 67–74. DOI: https://doi.org/10.1111/1467- development in intertidal environments. Earth-Science 8470.00130 Reviews, 83: 205–230. DOI: https://doi.org/10.1016/j. Hippensteel, SP, Martin, RE, Nikitina, D and Pizzuto, JE. earscirev.2007.04.003 2000. The formation of Holocene marsh foraminiferal Clarke, KR and Gorley, RN. 2006. Primer V6: User manual – assemblages, middle Atlantic Coast, USA: implications Tutorial. Plymouth, U.K.: Plymouth Marine Laboratory. for the Holocene sea-level change. Journal of Culver, SJ and Horton, BP. 2005. Infaunal marsh foraminifera Foraminiferal Research, 30: 272–293. DOI: https://doi. from the outer banks, North Carolina, USA. Journal of org/10.2113/0300272 Foraminiferal Research, 35: 148–170. DOI: https://doi. Holme, NA and McIntyre, AD. 1971. Methods of the study org/10.2113/35.2.148 of marine benthos. IBP Handbook No, 16. Oxford and Culver, SJ, Leorri, E, Corbett, DR, Mallinson, DJ, Shazili, Edinburgh: Blackwell Science Publication. NAM, Mohammad, NM, Parham, PR and Yaacob, R. 2013. Horton, BP and Edwards, RJ. 2006. Quantifying Holocene sea Infaunal mangrove swamp foraminifera in the Setiu level change using intertidal foraminifera: lessons from the Wetland, Terengganu, Malaysia. Journal of Foraminiferal British Isles. Cushman Foundation for Foraminiferal Research Research, 43(3): 262–279. DOI: https://doi.org/10.2113/ Special Publication, 40: 97. gsjfr.43.3.262 Horton, BP, Edwards, RJ and Llyod, JM. 1999. UK Intertidal Culver, SJ and Lipps, JH. 2003. Predation on and by foraminiferal distributions: implications for sea-level foraminifera. In Kelley, PH, Kowalewski, M and Hansen, TA. studies. Marine Micropaleontology, 36: 205–223. DOI: (eds.) Predator-prey interactions in the fossil record. New https://doi.org/10.1016/S0377-8398(99)00003-1 Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 13

Horton, BP, Gibbard, PL, Milne, GM, Morley, RJ, Application of Microfossils to Environmental Geology. New Purintavaragul, C and Stargardt, JM. 2005. Holocene sea York: Springer Science. DOI: https://doi.org/10.1007/978-1- levels and palaeoenvironments, Malay-Thai Peninsula, 4615-4167-7 southeast Asia. The Holocene, 15(8): 1199–1213. DOI: Murray, JW. 2003. An illustrated guide to the benthic https://doi.org/10.1191/0959683605hl891rp foraminifera of the Hebridean Shelf, west of Scotland, with Hottinger, L, Halicz, E and Reiss, Z. 1993. Recent foraminiferida notes on their mode of life. Palaeontologia Electronica, 5(1): from the Gulf of Aqaba, Red Sea. Ljubljana: Slovenian 31. Academy of Sciences. Murray, JW. 2006. Ecology and Applications of Benthic Husain, ML and Sulong, I. 2001. Mangroves of Terengganu. Foraminifera. Cambridge: Cambridge University Press. DOI: Malaysia: Kolej Universiti Sains and Teknologi Malaysia and https://doi.org/10.1017/CBO9780511535529 Forestry Department of Peninsular Malaysia. Oki, K. 1989. Ecological analysis of benthonic foraminifera in Husain, ML and Yaakob, R. 1995. Beach erosion variability Kagoshima Bay, South Kyushu, Japan. South Pacific Studies, during a northeast monsoon: The Kuala Setiu coastline, 10: 1–191. Terengganu, Malaysia. Pertanika J. Sci. Tech, 3(2): 337–348. Ong, MC, Kamaruzzaman, BY and Noor Azhar, MS. 2012. Kamaruzzaman, BY. 1994. A Study of some Physico-Chemical Sediment characteristic studies in the surface sediment Parameters in the Estuarine System of Chukai-Kemaman from Kemaman mangrove forest, Terengganu, Malaysia. Rivers, Terengganu. Unpublished thesis (MSc), Universiti Oriental Journal of Chemistry, 28(4): 1639–1644. DOI: Putra Malaysia. https://doi.org/10.13005/ojc/280413 Kamaruzzaman, BY and Ong, MC. 2008. Recent sedimentation Saffert, H and Thomas, E. 1998. Living foraminifera and rate and sediment ages determination of Kemaman- total populations in salt marsh peat cores: Kelsey mars Chukai mangrove forest, Terengganu, Malaysia. American (Clinton, CT) and the Great Marshes (Barnstable, MA). Journal of Agricultural and Biological Sciences, 3(3): 522– Marine Micropaleontology, 33: 175–202. DOI: https://doi. 525. DOI: https://doi.org/10.3844/ajabssp.2008.522.525 org/10.1016/S0377-8398(97)00035-2 Kemp, AC, Telford, RJ, Horton, BP, Anisfeld, SC and Scott, DB and Medioli, FS. 1978. Vertical zonations of Sommerfield, CK. 2013. Reconstructing Holocene sea marsh foraminifera as accurate indicators of former level using salt-marsh foraminifera and transfer functions: sea-levels. Nature, 272: 528–531. DOI: https://doi. lessons from New Jersey, USA. Journal of Quaternary org/10.1038/272528a0 Science, 28(6): 617–629. DOI: https://doi.org/10.1002/ Scott, DB, Medioli, FS and Schafer, CT. 2004. Monitoring of jqs.2657 Coastal environments using foraminifera and thecamoebian Leorri, E, Horton, BP and Cearreta, A. 2008. Development indicators. Cambridge: Cambridge University Press. of a foraminifera-based transfer function in the Basque Shaari, H, Nasir, QM, Pan, HJ, Mohamed, CAR, Yusoff, AH, Khalik, marshes, N. Spain: Implications for sea-level studies in the WMAWM, Naim, E, Setiawan, RY and Anthony, EJ. 2020. Bay of Biscay. Marine Geology, 251: 60–74. DOI: https://doi. Sedimentation and sediment geochemistry in a tropical org/10.1016/j.margeo.2008.02.005 mangrove channel meander, Sungai , Peninsular Leorri, E and Martin, RE. 2009. The input of foraminiferal Malaysia. Progress in Earth and Planetary Science, 7(46): 1–11. infaunal populations to sub-fossil assemblages along an DOI: https://doi.org/10.1186/s40645-020-00362-y elevational gradient in a salt marsh: application to sea- Shennan, I, Long, AJ and Horton, BP. 2015. Handbook of sea level studies in the mid-Atlantic coast of North America. level research. UK: John Wiley and Sons. DOI: https://doi. Hydrobiologia, 625: 69–81. DOI: https://doi.org/10.1007/ org/10.1002/9781118452547 s10750-008-9697-1 Stoner, AW and Zimmerman, RJ. 1988. Food pathways Lipps, JH. 1971. Siliceous cement in agglutinated foraminifera. associated with penaeid shrimps in a mangrove-fringed Journal of Protozoology, 18(Supplement): 30. estuary. In Dizon, AE (ed.) Fishery Bulletin. Washington, Lipps, JH. 1983. Biotic interactions in benthic foraminifera. Scientific Publications Office, National Marine Fisheries In Tevesz, MJS and McCall, PL (eds.), Biotic interactions in Service, NOAA. recent and fossil benthic communities. New York: Plenum Sulong, I, Mohd-Lokman, H, Mohd-Tarmizi, K and Press. DOI: https://doi.org/10.1007/978-1-4757-0740- Ismail, A. 2002. Mangrove mapping using landsat 3_8 imagery and aerial photograph: Kemaman district, Loeblich, AR and Tappan, H. 1964. Treatise on Invertebrate Terengganu, Malaysia. Environment, Development, Paleontology (Vol. 1 and 2). New York: The University of and Sustainability, 4: 135–152. DOI: https://doi. Kansas Press and The Geological Society of America. org/10.1023/A:1020844620215 Lutze, GF and Altenbach, A. 1991. Technik und signifikanz der Walton, W. 1952. Techniques for recognition of living lebendfarbung benthischer foraminiferen mit Bengalrot. foraminifera. Contributions from the Cushman Foundation Geologisches Jahrbuch A, 128: 251–265. for Foraminiferal Research, 3: 56–60. Malaysian Meteorological Service. 2019. Annual report. Kuala Wang, F, Gao, M, Liu, J, Pei, S, Li, C, Mei, X and Yang, S. Lumpur: Jabatan Meteorology Malaysia. 2016. Distribution and environmental significance Martin, RE. 2000. Environmental Micropaleontology the of live and dead benthic foraminiferal assemblages Suriadi et al. Open Quaternary DOI: 10.5334/oq.95 14

in surface sediments of Laizhou Bay, Bohai Sea. Whittaker, JE and Hodgkinson, RL. 1979. Foraminifera of the Marine Micropaleontology, 123: 1–14. DOI: https://doi. Togopi Formation, Eastern , Malaysia. Bulletin of the org/10.1016/j.marmicro.2015.12.006 British Museum, 31: 1–120.

TO CITE THIS ARTICLE: Suriadi, R, Saelan, WNW, Satyanarayana, B, Suratman, S, Shaari, H. 2021. Subsurface and Infaunal Foraminifera of Kemaman-Chukai Mangrove Swamps, East Coast Peninsular Malaysia. Open Quaternary, 7: 5, pp.1–14. DOI: https://doi.org/10.5334/oq.95

Submitted: 30 December 2020 Accepted: 05 May 2021 Published: 19 August 2021

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