Pulau Tioman foraminiferal assemblages
Similar to the worldwide reef foraminifera distributions (i.e., Uthicke & Nobes; Renema, 2018; Förderer & Langer, 2019), the foraminifera assemblages in Pulau Tioman is dominated by Rotaliid group (i.e., Amphistegina, Calcarina, Operculina and Peneroplis) with most species have symbiotic relationship with diatom or algae (Table 3). The foraminifera diversity around Pulau Tioman is slightly higher (H’= 1.8-3.0) than those reported from fringing reef environment in Brazil (Echler and de Morray, 2020). Amphistegina lessoni and Calcarina gaudichaudii, which are among the most widespread species found in the Indo-Pacific waters (Renema, 2018), are very abundant and common in Pulau Tioman. Amphistegina lessoni for instance occurred at all stations around Pulau Tioman except in F3 (Mesoh) where deeper water (> 18 m) occurred, increase algae distribution and turbid water may have restrict their presence (Renema, 2010). Meanwhile, despite having relatively lower abundances (4–55%) compared to study in northern atoll of South China Sea (Chen & Lin, 2017), the calcareous porcelaneous group (Triloculina, Quinqueloculina and Lachlanella) contributed to > 50% of total foraminifera assemblage in Pulau Tioman. In Mesoh especially, where water depth was > 15 m and slightly murky, there was a significant increase of porcelaneous representatives such as Lachlanella compressiostoma (35%), Triloculina tricarinata (23%) and Triloculinella chiastocytis (21%). This finding supports the observation by Uthicke et al. (2010) in the Great Barrier Reef where relatively high abundance of miliolids was also recorded in turbid waters. Triloculina was common in Dongsha Atoll, northern South China Sea but their abundance was recorded to be < 20% (Chen & Lin, 2017).
The Amphistegina and Calcarina are common in reef environment worldwide (Hallock, 1988; Weinmann et al., 2013) especially in Southeast Asia(Szarek, 2001; Natsir and Subkhan, 2012; Culver et at., 2012). Most living Amphistegina can be found attached to reef substrates and less in sediment and usually occurred in high abundance at coral reef environments (Natsir and Subkhan, 2012). Due to their ecological requirement and distribution, foraminifera assemblages are among the best candidate to monitor reef health. Meanwhile opportunistic taxa especially Ammonia, Elphidium and Bolivina are among those that are tolerant of environmental variability (Hallock et al., 2003; Carnahan et al., 2009). Hence typical polluted marine conditions with the enrichment of organic matter and reduction of dissolved oxygen allowed these group to opportunistically increase in relative abundance (Dimiza et al., 2016).
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 Chadwick-Furman, 2002; Toda et al., 2007). The FORAM index was developed by Hallock et al. (2003) as low-cost monitoring tool which could indicate if the water quality surrounding reef ecosystem can support reef growth. This index which was first applied in Westen Atlantic reef (Hallock et al., 2003) has also been applied to other regions including the Great Barrier Reef in Australia (Schueth and Frank, 2008; Uthicke et al., 2010), reefs in Brazil waters (Barbosa et al, 2009) and Saronikos Gulf, Greece (Dimiza et al., 2016). The reliability, simplicity and cost affective of the FORAM index has made it a suitable proxy in coral reef monitoring program.
Majority of the FI values obtained around Pulau Tioman waters are greater than 4 which indicate that general water quality is favorable for reef growth and recovery (Uthicke et al., 2010, Barbosa et al., 2009). Additionally, the FI values observed on the east of Pulau Tioman is relatively higher > 5 than those observed on the west of the island. This study therefore indicates that the reefs on the east of Pulau Tioman are more likely to survive and recover future bleaching events compare to those on the west of the island. Incredibly, our finding is comparable to the study by Shahbudin et al. (2017) which reported that the east of Pulau Tioman have better live coral covers whereas the west side of the island recorded higher percentage of dead corals. The degraded reef condition on the west coast of Pulau Tioman has been associated with rapid coastal development (Unsworth et al., 2010), active tourisms (Praveena et al., 2012) and boating activities (Shahbudin et al., 2017).
Concurrent with previous studies on reef condition (e.g. Shahbudin et al., 2017; Akmal et al., 2019), three stations (i.e., E3, F1 and G1) that recorded lower FI values (FI < 4) in this study are recognized as a famous diving and snorkeling sites among the tourists. These three stations are located near to the Pulau Tioman Marine Park jetty which also serve as route for boat and attraction spots among tourists for snorkelling and SCUBA diving activities. The relatively higher anthropogenic activities lead to the increase of organic matter and nutrient concentrations which in turn create a less favorable environment to symbiont-bearing foraminifera and allowed stress tolerant taxa to dominate (Hallock et al., 2003; Uthicke et al., 2010).
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 classified 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 classified 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 significant 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 field 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 al., 2003; Carnahan et al., 2009). Finally, group D are majorly made up of stations located on the east of Pulau Tioman with FI = 6–9 indicating a very good water condition for reef growth and recovery. The reduced coastal development activities observed on the east coast of Pulau Tioman may have reduced the impact of sedimentation and allowed greater diversity of live corals to thrive (Shahbudin et al., 2017).