Reef Foraminifera As Bioindicator Of Coral Reef Health in Pulau Tioman, Pahang, Malaysia


 Pulau Tioman is one of the famous tourism islands in Peninsular Malaysia due to the beautiful terrestrial and coral reefs ecosystem. This study aims to assess and monitor the health of coral reef sites surrounding Pulau Tioman based on the application of Foraminifera in Reef Assessment and Monitoring (FORAM) Index. A total of ten selected sampling sites from west and east side of Pulau Tioman were setup in front of the major beach areas around Pulau Tioman. At each site, 100 m transect was laid out from shore towards the reef slope and surface sediment samples were collected at 50 m intervals. Eight orders, 41 families, 80 genera and 161 species of benthic foraminifera were identified around Pulau Tioman. Amphistegina lessonii found to be the most dominant species and the least dominant species (< 4%) are Bolivina vadescens, Elphidium neosimplex, Heterolepa dutemplei, Heterolepa subhaidingerii, Mikrobelodontos bradyi, Milliolinella suborbicularis, Operculina discoidalis, Parahourinoides fragillissimus, Quinqueloculina incisa, Quinqueloculina sulcate, Triloculinella bertheliniana and Triloculinella parisa. The highest and lowest numbers of species was recorded at station J3 and station F3. The agglutinated type of foraminifera contributed between 2–8% of the total assemblages. Meanwhile, calcareous hyaline and porcelaneous group represent 79% and 19% of total assemblages respectively. Based on the functional groups, symbiont-bearing taxa were the most common foraminiferal found in most of the stations. The present study indicates that majority of sampling sites around Pulau Tioman are conducive for coral reef growth and could recover from any future bleaching events or temporary damage in the ecosystem. However, several areas with higher coastal development and tourism activities has reduced water quality (FI < 4) and chances of better reef recovery. Thus, the number of visitors and tourists should be revised in order to produce a better condition for coral reefs to grow. This assumption is based on the established results of the FORAM index. Thus, we suppose that FORAM index could be used together with coral reef health index in other reef ecosystems around Malaysia to determine the condition and status of coral reef area.


Introduction
Coral reef ecosystem is among the most biologically diverse ecosystem in the world which play a vital role in shaping the ecosystems over the past 200 million years (Hoegh-Guldberg, 1999). Coral reef provides goods and services to marine tropical and subtropical regions (Moberg and Folke, 1999). Globally, coral reef ecosystem has been threatened and many have already been lost due to climate change and human intervention (Shahbudin et al., 2017).
On a larger scale, elevated sea temperature and ocean acidi cation due to climate change has challenged the natural resilient of tropical reef (Anthony et al., 2015). Meanwhile the local stressors which ranged from human activities such as coastal development and pollution, reef predatory and diseases usually reduce the potential of reef recovery to climate change (Bruno and Selig, 2007;Anthony et al., 2015;Cowburn et al., 2018). Since coral reef ecosystems provide various natural environmental services, their ability to survive the global climate anomaly is very important. Consequently, understanding the health status of local individual reefs is important in order to make sure the coral reef survive and recover from any next mass mortality event in near future (Anthony et al., 2015).
Pulau Tioman which is situated in the Southern South China Sea (SSCS) is surrounded by extensive coral covers that host various marine species (Harborne et al., 2000). Recognizing the importance of coral ecosystem, part of Pulau Tioman has been gazetted as National Marine Park by Malaysian government (Department of Marine Park, 2012). Concurrently the beauty of the island has attracted and promote tourisms activities since 1990 (Chia et al., 2018).
Tourisms, recreational diving activities and coastal development may post local threat to the surrounding reef ecosystem by reducing their resilience to climate change (Cowburn et al., 2018). Therefore, the most viable management approach in facing climate change is to reduce and monitor local stressors such as coastal pollution (Game et al., 2014;Anthony et al., 2015). Benthic foraminifera have been proven to be an excellent indicator for sediment quality, heavy metal pollution, organic pollution and water quality (Alve, 1995;Hallock et al., 2003;Sen Gupta, 2003;Carnahan, 2005). This single cell organism is abundant in reef ecosystems with several taxa that possess similar ecological requirements as reef building corals (Hallock et al., 2003). Several studies have successfully monitor the potential recovery of reef environment using benthic foraminifera as indicator (Schueth and Frank, 2008;Uthicke et al., 2010;Natsir and Subkhan, 2012). The development of Foraminifera in Reef Assessment and Monitoring (FORAM) index by Hallock et al. (2003) has allow continuous monitoring of reef health condition. In order to safeguard the coral ecosystems and maintain their ecological importance in Pulau Tioman, monitoring the environmental health surrounding the reef is very important to park management. This study aim to assess and monitor the health of reef environment surrounding the Pulau Tioman based on the application of Foraminifera in Reef Assessment and Monitoring (FORAM) Index.

Study site
The study was carried out at Pulau Tioman, Pahang, Malaysia (Fig. 1). Pulau Tioman lies off the southeast coast of Peninsular Malaysia in SCS region. The island is located in tropical region under the in uence of two type of monsoon; the northeast monsoon and southwest monsoon (Akhir et al., 2014). The maximum wave height during the northeast monsoon that occur through November to March is ~ 4 m while during southwest monsoon (April to August), the maximum wave height is < 1 m (Chu et al., 2004;Marghany, 2001). Pulau Tioman is surrounded by numerous coral reefs area with approximately 57-59 genera of hard coral distributed around the island (Shahbudin et al., 2016). Accropora, Montipora and Porites are among the most common coral genera reported from Pulau Tioman (Toda et al., 2007;Shahbudin et al., 2017). The sheltered west coast of Pulau Tioman (Fig. 1) made such area suitable for snorkeling and diving activities compared to the west side of the island. Therefore, the east coast of Pulau Tioman receives more tourist visits and much more developed with numerous resorts and housing area that are distributed along the coast (Shahbudin et al., 2017).

Samples Collection
In order to assess the marine environmental health of Pulau Tioman, samples were collected from coastal water of both west and east side of the island. A total of 10 sampling sites were selected based on the intensity of human activities and development along the coastal environment around Pulau Tioman. A transect of three sampling points were setup at each sampling site, giving a total of 30 sampling points around Pulau Tioman. At each sampling site, three samples were collected along the 100 m transect laid perpendicular from the shore towards the reef slope. On each transect, the samples were collected at every 50 m intervals. Bulk sediment samples were collected by SCUBA divers using scoop and kept in labelled plastic bags. The in-situ parameters (i.e., water salinity, temperature and pH) and water depth (m) were obtained at each sampling station using Hydrolab Quanta Multiparameter from a small vessel. All samples collected at eld were brought back to the marine park station to be sorted. Sediment samples that have been collected were divided into two components for future analysis, i.e., foraminiferal and sedimentological analyses. Approximately 30 cm 3 sediments were subsampled from the bulk samples for foraminiferal analysis and were xed with 4% buffered formalin (Murray, 2006). The remaining sediment samples were kept in zip-lock plastic bags, labelled and brought back to the laboratory for sediment grain size analysis.

Laboratory analysis
In the laboratory, the sediment samples for foraminiferal analysis were gently washed under running tap water over a 63 µm mesh sieve (Hallock et al., 2003).
The residue on the 63 µm sieve was carefully transferred into pre-labelled weighing boat before being dried in the oven at 40-50 ºC overnight. The dried samples were later kept in plastic bags for analysis. Foraminiferal specimens were handpicked using a ne brush under a stereomicroscope. Approximately 300 optimally preserved foraminifera test were picked from every station (Culver et al., 2012). If the samples have less than 300 foraminifera, all specimens were picked (Culver et al., 2012). Afterward, the specimens were sorted and mounted on micropalaeontological cardboard slides. The identi cation of foraminifera was carried out based on (Loeblich & Tappan, 1988) and other regional taxonomic manuscript (e.g. Szarek The grain size analysis was carried out based on dry sieving method by Folk (1980). Approximately 100 g of dried sediment samples were sieved onto 4000 µm, 2000 µm, 1000 µm, 500 µm, 250 µm, 125 µm and 63 µm sieves size. After that, the percentage of each sediment fraction was determined.
Meanwhile the organic matter composition in sediment was determined by the loss on ignition (LOI) method (Dean, 1974). Prior to heating, 5 g of each sediment samples were weighed. The samples were gradually heated until they reached the temperature of 500-550˚C and afterwards ignited for 4 hours.
After the samples have cool to room temperature, the nal weight was recorded. The percentages of organic matter were calculated based on Heiri et al.

Data analysis and statistical analysis
To avoid working on reworked samples, only foraminifera species with relative abundance of more than 2% were maintained for further statistical analysis.
Diversity indices such as diversity index (Fisher's alpha, α), species diversity (Shannon-Wiener, H'), and evenness (Pielou, J') were analysed using PAST (PAleontological STatistics) software version 3. Meanwhile, cluster analysis was performed to simplify the large data sets for easy recognition (Romesburg, 2004). In order to investigate the foraminifera species environment relationship, ordination techniques of Canonical Correspondence Analysis (CCA) was carried out (Milker et al., 2009).

FORAM Index
The application of FORAM Index was carried out in order to determine the health status of reef in Pulau Tioman. Foraminifera species collected and identi ed around Pulau Tioman were grouped into functional groups ( Table 2) Table 3.  Table 2 Functional Groups assigned to benthic foraminifera used in coral reef assessment (Hallock et al., 2003). *Full range of opportunistic genera under local conditions is not well known.    Based on the functional groups, on average, symbiont-bearing taxa (63%) were the most common foraminiferal found in almost all stations (  (Fig. 3). Meanwhile the average abundant of stress-tolerant genera (12%) includes Ammonia, Bolivina, Cellanthus, Elphidium, Pararotalia and Rotalia (Fig. 4) and other small heterotrophic taxa (25%). Extremely high dominance of symbiont-bearing group was recorded at station B2 (Kampung Mukut) at water depth 10.4 m. The stress-tolerant taxa on the other hand was dominant at station F1which is situated close to the Marine Park Centre and jetty.
The FORAM index (FI) values from this study varies between 2.8 to 9.2 with most sites around Pulau Tioman representing conducive environment for reef growth and recovery (FI > 5) (Table 3). However, three stations namely F1, E3, and G1 that have FORAM Index value of 2.8, 3.0, and 3.6 respectively indicate marginal environment for reef growth and unsuitable for reef recovery.

Sediment characteristic of Pulau Tioman
Most of the sediments in the study area can be classi ed as sandy with coarse to medium sand dominating the grain size percentages ( was dominated by ner sediment composition. The average percentage of organic matter was 3.35 ± 0.08% with range between 1.31 and 5.89% (Table 6). The highest organic matter content was recorded at E3 in the vicinity of Teluk Tekek, a famous tourist site for snorkelling and diving. Meanwhile the lowest organic matter content was documented in Tanjung Geleber (C1), a sheltered headland that received less tourist visits. Statistical analysis on benthic foraminiferal assemblages Cluster analysis was carried out to determine of similarities between all sampling sites based on the numbers of foraminifera species found around Pulau Tioman. The Q-mode analysis revealed four major groups of benthic foraminiferal assemblages; Group A, Group B, Group C and Group D (Fig. 5). The rst cluster group, Group A consist of two stations (Station F3 and G3). The foraminiferal assemblages of this group are characterized by relatively high average abundance of Nummulites venosus (31%) and Assilina ammonoides (22%). While Group B made up of four stations which are Station E3, F2, G1 and F1. The species that dominated the assemblages in this group is Ammonia tepida with average relative abundance of 17%. Group C consist of three stations (Station D1, H2 and H3) which is dominated by Calcarina gaudichaudii (34%) and Amphistegina lessoni (23%). Group D consist of the other 21 remaining stations (Station A1, A2, A3, B1, B2, B3, C1, C2, C3, D2, D3, E1, E2, G2, H1, I1, I2, I3,

FORAM INDEX ecological interpretation
The increase in construction and land reclamation activities around the east coast region has exposed many coral reef areas to high rates of sedimentation consequently reducing the diversity of live corals including those in Pulau Tioman (Shahbudin et al., 2017). To make matters worse, the active tourism related activities such as trampling action by divers or snorkelers and resuspension of sediment by boats has increased the mortality rate of corals (Zakai and To understand the similarity of foraminifera assemblages around Pulau Tioman, Q-mode cluster analysis has been carried out. The results indicated that benthic foraminifera assemblages can be classi ed into four major groups (i.e., Group A, Group B, Group C and Group D). Three of these groups (Group A, Group B and Group C) represent foraminifera assemblages found on the west side of the island. Group A represent deeper water environment that is dominated by Numulites venosus and Operculina ammonoides. Both symbiont bearing species which belong to Numulitiidae family have been reported to have better growth rate at low light area (Ovon et al., 2018). Hence explaining their increase in abundance at deeper reef slope area (> 18 m water depth) on the west coast of Pulau Tioman. The calculated FORAM index for Group A (FI > 6) shows that the water quality conditions within these stations (F3 and G3) could be classi ed as oligotrophic which optimum for reef recovery (Hallock et al., 2003;Prazeres et al., 2020). Hence, despite the intensity of diving activity in Mesoh and Panuba Bay, the increased distance from shoreline has both reduced the anthropogenic impacts on coral and support healthy coral growth and recovery (Oliver et al., 2018). Meanwhile, Group B recorded signi cant increase in porcelaneous foraminifera group with relatively higher abundance of stress tolerant taxa such as Ammonia tepida. Distributed on the west side of the Pulau Tioman, the relatively higher average composition of organic matter (3.81%) recorded in the sediment provide food sources for heterotrophic taxa and increase the number of stress tolerant species such as Ammonia. The FI values for this group varied between 2.7-4.0 with the lowest values recorded in the vicinity of Mesoh where comparatively high snorkelling and diving activities took place every day. The sheltered beach in Mesoh is among the most popular sites for local and tourist to enjoy swimming and snorkelling. Based on the observation during eld sampling, the water in F1(Mesoh) is more turbid with higher number of coral fragments discovered close to the shoreline. Group C represent foraminifera assemblages that are distributed in shallow waters (6-7m water depth) on the west of Pulau Tioman. This group has relatively lower stress tolerant taxa (< 5%) but relatively higher heterotrophic species such as Eponoides, Discorbinella and Textularia. The presence of plenty food sources may have promoted the increase number of heterotrophic taxa but limit the dominance by stress tolerant taxa (Hallock et

Conclusion
The present study indicates that majority of sampling sites around Pulau Tioman are conducive for coral reef growth and could recover from any future bleaching events or temporary damage in the ecosystem. However, several areas with higher coastal development and tourism activities has reduced water quality (FI < 4) and chances of better reef recovery. The carrying capacity of visitors and tourists at Tioman Marine Park however should be reviewed in order to produce an optimum condition for corals to grow. This assumption is based on the established results of the FORAM index. This nding also implied that FORAM index could be used together with coral reef health index to determine the condition and status of coral reef area. Hence, this index coupled with reef health index could be applied at other reef ecosystems around Malaysia in order to determine their health.