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

doi:10.21203/rs.3.rs-51033/v1

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.

Oceanography

Foraminifera

Coral Reef

FORAM Index

Coastal development

Reef recovery

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 acidification 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 influence 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 field 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 cm³ sediments were subsampled from the bulk samples for foraminiferal analysis and were fixed 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 fine 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 identification of foraminifera was carried out based on (Loeblich & Tappan, 1988) and other regional taxonomic manuscript (e.g. Szarek, 2006; Culver et al., 2012; Martin et al., 2018).

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 final weight was recorded. The percentages of organic matter were calculated based on Heiri et al. (2001).

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 identified around Pulau Tioman were grouped into functional groups (Table 2) as suggested by Hallock et al. (2003) and Carnahan et al. (2009). The calculation of FORAM Index was based on the equation proposed by Hallock et al. (2003) and values obtained from the calculation were interpreted based on Table 3.

Table 1

Coordinate and location of all 30 sampling stations around the coastal waters of Pulau Tioman.
Station	Description of location	Coordinate
Station	Description of location	LONGITUDE	LATITUDE
A1	Benuang • Low number of snorkelling and SCUBA diving activity.	2˚44'27.4" N	104˚13'01.3" E
A2		2˚42'27.7" N	104˚13'04.9" E
A3		2˚42'28.9" N	104˚13'06.3" E
B1	Kampung Mukut • Fisherman village, not a snorkelling and SCUBA diving site	2˚43'37.4" N	104˚13'00.3" E
B2		2˚43'36.2" N	104˚13'01.9" E
B3		2˚43'35.2" N	104˚13'03.5" E
C1	Gelaber • Not a snorkelling and SCUBA diving site	2˚45'11.6" N	104˚07'09.7" E
C2		2˚45'15.5" N	104˚07'07.1" E
C3		2˚45'17.7" N	104˚07'05.2" E
D1	Pulau Renggis • High number of snorkelling and SCUBA diving activities at this site	2˚48'37.4" N	104˚08'09.6" E
D2		2˚48'39.0" N	104˚08'08.8" E
D3		2˚48'41.6" N	104˚08'08.3" E
E1	Teluk Tekek • Snorkelling and SCUBA diving site, boating route, Jetty	2˚49'04.4" N	104˚09'13.2" E
E2		2˚49'08.2" N	104˚09'10.4" E
E3		2˚49'11.5" N	104˚09'08.2" E
F1	Mesoh • Marine Park Centre, Jetty, snorkelling and SCUBA diving site	2˚49'57.9" N	104˚09'42.4" E
F2		2˚49'57.4" N	104˚09'40.7" E
F3		2˚49'57.1" N	104˚09'38.7" E
G1	Teluk Panuba • Snorkelling and SCUBA diving site, boating route	2˚51'01.9" N	104˚09'11.4" E
G2		2˚51'00.8" N	104˚09'09.4" E
G3		2˚50'59.6" N	104˚09'07.5" E
H1	Teluk Salang • Not a snorkelling and SCUBA diving site	2˚52'30.4" N	104˚09'02.6" E
H2		2˚52'31.9" N	104˚09'02.5" E
H3		2˚52'33.5" N	104˚09'02.7" E
11	Teluk Dalam • Not a snorkelling and SCUBA diving site	2˚51'38.8" N	104˚11'14.5" E
I2		2˚51'38.9" N	104˚11'16.8" E
I3		2˚51'39.5" N	104˚11'18.2" E
J1	Batu Mambang • Not a snorkelling and SCUBA diving site	2˚48'18.1" N	104˚12'26.2" E
J2		2˚48'18.1" N	104˚12'28.3" E
J3		2˚48'19.1" N	104˚12'30.1" E

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.
Functional Group	Order	Family	Genus	Distribution
Symbiont-bearing	Rotaliida	Amphisteginidae	Amphistegina	Circumtropical
		Calcarinidae	5 genera	Indo-Pacific
		Nummulitidae	Heterostegina	Circumtropical
		Nummulitidae	3 other genera	Indo-Pacific
	Miliolida	Miliolida	Alveolinella	Indo-Pacific
		Miliolida	Borelis	Circumtropical
		Peneroplidae	several genera	Circumtropical
		Soritidae	Sorites	Circumtropical
			Amphisorus	Circumtropical
			3 genera	Caribbean
			Marginopora	Indo-Pacific
Opportunistic*	Trochamminida	Trochamminidae	Several genera	Cosmopolitan
	Textulariida	Lituolidae	Several genera	Cosmopolitan
	Buliminida	Bolivinidae	Several genera	Cosmopolitan
	Buliminida	Buliminidae	Several genera	Cosmopolitan
	Rotaliida	Rotaliidae	Ammonia	Cosmopolitan
	Rotaliida	Elphidiidae	Elphidium	Cosmopolitan
Other Small Taxa	Miliolida	Most except larger taxa noted above		Cosmopolitan
	Rotaliida	Most except those noted above		Cosmopolitan
	Textulariida	Most		Cosmopolitan
	Other	Most		Cosmopolitan

Table 3

The values and interpretation of FORAM index (FI) (Hallock et al., 2003)
FI Value	Interpretation
> 4	Environment conducive to reef growth
2–4	Environment marginal for reef growth and unsuitable for recovery
< 2	Stressed condition and unsuitable for reef growth

Foraminiferal Assemblages, Functional Groups and FORAM Index

A total of 8 orders, 41 families, 80 genera and 161 species of benthic foraminifera identified around Pulau Tioman. The most dominant species is Amphistegina lessonii 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. Overall, the agglutinated foraminifera contributed between 2–8% of the total foraminifera assemblages in Pulau Tioman. Meanwhile calcareous hyaline and calcareous porcelaneous group represent on average 79% and 19% of total assemblages respectively (Table 4). Majority of species that made up calcareous hyaline group belong to the larger benthic foraminifera from family Amphisteginidae, Calcarinidae and Nummulitidae. As for the porcelaneous species, the most common family recorded belong to the Miliolidae. The highest number of species was recorded at station J3 (S = 25) while the minimum number of species (S = 12) at station F3. The Shannon-Wiener (H’) diversity index around Pulau Tioman ranged between 1.8 and 3.0. Meanwhile species evenness (J’) values ranged between 0.37 and 0.79

Table 4

Benthic foraminifera distribution in Pulau Tioman presented in type of test wall (agglutinated, calcareous hyaline and calcareous porcelaneous), diversity indices (number of species (S), the number specimen collected (N), Pielou’s eveness (J’), Fisher’s alpha (α) and Shannon-wiener (H’) indices), functional groups and calculated FORAM index value.
Station		Type of test wall			Diversity indices				Functional Group			FORAM Index
Station	Water depth (m)	Agglutinated (%)	Calcareous hyaline (%)	Calcareous porcelaneous (%)	No. of Species (S)	Shannon-Wiener (H’)	Pielou’s Evenness (J’)	Fisher’s alpha (α)	Symbiont-Bearing (%)	Stress Tolerant (%)	Others Heterothrophic Taxa(%)	FORAM Index
A1	7	1	90	9	17	2.36	0.63	6.43	69	10	21	7.5
A2	12	5	84	11	23	2.72	0.66	11.21	62	8	30	6.9
A3	13	1	93	7	19	2.27	0.51	7.23	77	9	14	8.1
B1	5	0	95	5	11	1.74	0.52	3.26	64	1	5	9.3
B2	10	4	94	2	14	2.03	0.54	4.60	94	1	9	9.2
B3	15	0	91	9	12	2.03	0.63	3.67	86	1	11	9.0
C1	5	0	93	7	18	2.36	0.59	6.58	59	13	26	6.7
C2	14	0	92	7	15	1.91	0.45	5.06	55	18	30	6.1
C3	14	3	84	12	15	2.26	0.64	5.20	50	20	34	5.6
D1	6	8	83	10	16	2.08	0.50	6.06	43	4	46	5.7
D2	11	2	89	9	17	2.33	0.61	6.17	62	13	21	7.1
D3	15	3	90	7	16	2.14	0.53	5.43	83	3	17	8.4
E1	5	1	89	10	20	2.34	0.52	7.82	84	4	16	8.4
E2	11	0	90	10	20	2.62	0.68	7.92	71	5	21	7.8
E3	18	2	71	27	24	2.95	0.79	11.13	14	22	58	3.0
F1	5	1	74	25	17	2.10	0.48	6.24	17	51	37	2.8
F2	16	2	63	35	20	2.54	0.63	8.19	29	24	47	4.1
F3	18	2	90	8	12	2.00	0.62	3.65	57	21	18	6.6
G1	5	8	69	23	23	2.69	0.64	9.91	24	27	52	3.6
G2	11	8	72	20	19	2.21	0.48	7.23	47	20	30	5.7
G3	18	0	89	11	14	1.90	0.48	4.51	84	5	13	8.5
H1	5	3	82	15	23	2.56	0.56	10.71	57	10	32	6.5
H2	7	1	93	6	17	1.83	0.37	6.03	91	1	14	8.8
H3	7	1	95	4	15	1.83	0.41	5.06	73	3	11	8.7
I1	6	2	85	13	22	2.63	0.63	9.28	71	7	21	7.6
I2	8	0	84	16	21	2.60	0.64	8.79	65	11	32	6.7
I3	10	1	94	5	19	2.52	0.65	7.14	73	13	13	7.8
J1	5	0	89	10	18	2.26	0.53	7.03	69	10	26	7.2
J2	9	0	97	3	15	1.83	0.42	5.06	85	6	14	8.4
J3	13	0	89	11	25	2.64	0.56	10.98	71	11	21	7.4

Based on the functional groups, on average, symbiont-bearing taxa (63%) were the most common foraminiferal found in almost all stations (Table 4). These symbiont-bearing taxa identified includes Amphistegina, Assilina, Calcarina, Coscinospira, Dendritina, Euthymonaca, Heterostegina, Nummulites, Operculina, Pararotalia, Parasorites, Peneroplis, Sorites and Spirolina (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 classified as sandy with coarse to medium sand dominating the grain size percentages (Table 5). Study area near Kampung Mukut (B1-B3), where the fishermen village is located shows relatively coarser sediment type. Meanwhile study site in Batu Mumbang (J1-J3) was dominated by finer 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.

Table 5

The composition of sediment grain size and organic matter around Pulau Tioman.
Stations	Grain size (%)					Organic Matter (%)
Stations	Coarse Sand (500 µm)	Medium Sand (250 µm)	Fine Sand (125 µm)	Very Fine Sand (63 µm)	Mud (< 63 µm)	Organic Matter (%)
A1	6.36	56.57	34.28	2.35	0.43	2.96
A2	18.97	46.00	31.35	3.34	0.34	3.21
A3	12.57	46.64	37.12	3.29	0.39	3.06
B1	98.81	0.93	0.13	0.09	0.04	3.45
B2	69.48	23.53	4.95	1.62	0.43	3.74
B3	98.95	0.71	0.19	0.12	0.03	3.22
C1	44.89	42.47	10.73	1.61	0.30	1.31
C2	73.51	16.30	9.72	0.15	0.32	1.82
C3	28.12	47.69	21.60	2.08	0.51	2.14
D1	93.21	5.55	0.94	0.21	0.09	3.26
D2	57.75	23.45	16.50	1.72	0.59	3.52
D3	85.26	12.33	2.11	0.20	0.10	3.45
E1	82.66	13.70	2.76	0.55	0.33	3.35
E2	39.10	20.34	24.54	11.91	4.12	3.75
E3	77.80	10.00	6.30	5.43	0.47	5.89
F1	87.05	3.61	3.37	5.84	0.13	2.19
F2	7.05	10.35	44.63	28.70	9.27	3.58
F3	32.14	21.48	36.02	5.91	4.46	4.13
G1	90.02	9.30	0.58	0.09	0.01	3.58
G2	87.30	9.22	1.29	0.18	2.01	3.51
G3	33.76	34.48	29.31	2.19	0.26	3.28
H1	51.91	20.20	20.17	6.74	0.97	3.70
H2	68.99	16.47	10.15	3.42	0.96	3.50
H3	90.04	7.60	1.70	0.42	0.24	3.75
I1	36.67	9.09	50.23	0.02	3.99	3.80
I2	23.76	4.85	62.46	0.18	8.75	3.29
I3	1.52	17.79	68.07	12.56	0.07	2.97
J1	3.50	42.23	49.68	4.55	0.03	3.75
J2	49.52	46.91	3.26	0.27	0.04	3.48
J3	5.63	28.25	47.97	18.09	0.06	3.91

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 first 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, J1, J2 and J3). The common species that have been identified for Group D area is Amphistegina lessoni (27%) and Amphistegina papillosa (8%).

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).

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 finding 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.

i) Relative abundance of total benthic foraminifera in Pulau Tioman (After Screening)

Species	A1	A2	A3	B1	B2	B3	C1	C2	C3	D1	D2	D3	E1	E2	E3	F1	F2	F3	G1	G2	G3	H1	H2	H3	I1	I2	I3	J1	J2	J3
Ammonia convexa	0	0	0	0	0	0	1	2	5	0	0	0	0	0	2	0	0	0	9	3	2	0	0	0	0	1	0	0	0	0
Ammonia supera	0	0	1	0	0	0	3	2	0	0	0	0	0	0	0	0	2	0	0	0	0	3	0	0	0	0	4	0	0	0
Ammonia tepida	0	0	0	0	0	0	3	2	7	1	0	0	0	0	5	39	11	5	14	15	1	0	0	0	1	5	0	2	1	5
Amphistegina lessoni	18	14	29	41	19	19	25	39	27	16	26	40	33	19	2	2	2	0	11	36	18	21	25	29	14	20	19	28	48	27
Amphistegina papillosa	18	9	16	4	10	12	8	2	2	1	14	7	4	4	0	1	0	1	1	1	2	3	2	3	7	9	11	12	10	13
Amphistegina radiata	10	9	12	13	10	19	6	0	0	1	6	6	6	13	0	0	0	0	1	2	3	3	3	3	5	6	13	9	6	5
Assilina ammonoides	5	9	6	2	3	11	0	0	3	0	2	6	1	6	10	2	18	23	0	1	21	1	0	2	8	11	10	6	4	6
Bolivina vadescens	0	9	0	0	0	0	0	0	0	1	0	0	0	0	3	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Calcarina gaudichaudii	0	9	0	2	16	1	0	0	0	26	4	0	11	10	0	0	0	0	1	2	0	15	41	36	1	0	0	0	1	4
Calcarina hispida	2	9	1	17	24	18	3	2	1	0	0	0	3	2	0	0	0	0	0	0	0	1	1	3	6	1	3	0	0	2
Calcarina mayori	0	9	1	3	3	0	0	0	0	0	0	0	5	5	0	0	0	0	0	0	0	1	6	5	0	0	0	0	2	0
Cavarotalia annectens	3	9	0	0	0	0	18	19	9	0	0	0	1	0	0	0	0	0	12	0	0	0	0	0	0	0	0	0	6	1
Cellanthus craticulatus	0	9	0	0	0	1	0	0	3	1	11	2	3	5	4	0	2	12	1	2	2	0	1	2	0	0	2	0	2	1
Discorbinella bertheloti	0	9	0	0	0	0	0	0	0	11	0	0	0	0	4	0	0	0	0	0	0	0	0	0	0	1	1	0	0	0
Dendritina ambigua	0	9	0	0	0	0	0	0	0	0	0	0	0	0	1	1	2	4	0	0	0	0	1	0	0	0	0	0	0	0
Dendritina striata	0	9	0	0	0	0	0	0	0	0	0	0	0	0	1	0	2	4	0	0	0	0	0	0	0	0	0	0	0	0
Elphidium advenum	4	9	1	0	0	0	2	2	0	0	0	0	0	0	1	0	0	0	0	0	0	0	0	0	0	0	1	2	0	1
Elphidium crispum	0	9	5	0	1	0	3	9	4	1	2	2	1	0	6	8	7	4	2	0	0	4	0	0	5	3	6	5	2	3
Elphidium neosimplex	3	9	2	0	0	0	0	0	0	0	0	0	0	0	0	0	1	0	0	0	0	0	0	0	0	0	0	0	0	0
Eponides cribrorepandus	2	9	1	0	0	0	0	0	0	4	2	0	0	3	0	0	0	0	0	0	0	0	1	2	1	0	0	0	1	0
Eponides repandus	1	9	3	0	0	0	1	0	0	3	5	1	0	2	0	0	0	0	0	0	0	1	3	1	0	1	1	4	0	2
Fijella simplex	1	9	0	0	0	0	0	0	0	0	0	0	0	1	4	0	0	0	0	0	0	0	0	1	0	0	0	0	0	0
Hesterostegina depressa	0	9	1	4	1	5	0	0	0	0	3	3	5	5	0	0	0	0	1	0	0	1	1	0	1	0	0	0	1	0
Heterolepa dutemplei	0	9	0	0	0	0	0	0	1	0	0	0	0	0	0	0	0	0	0	0	0	0	0	2	1	3	0	0	0	0
Heterolepa subhaidingerii	0	9	0	0	0	0	0	0	0	0	0	0	0	0	1	3	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Lachlanella compressiostoma	1	9	1	0	0	2	1	1	0	0	1	0	2	1	4	0	12	1	7	3	0	0	1	0	1	0	0	1	0	2
Mikrobelodontos bradyi	0	9	0	0	0	0	0	0	0	0	0	0	1	1	0	0	1	0	3	1	0	2	0	0	0	0	1	0	0	1
Millettiana milletti	0	9	0	0	0	0	0	0	0	1	0	0	0	0	5	0	0	0	1	0	0	0	0	0	1	0	0	0	0	0
Milliolinella suborbicularis	0	9	0	0	0	0	0	0	0	1	0	0	1	3	0	3	0	0	2	2	0	0	0	0	0	0	0	0	0	1
Nonionoides grateloupii	0	9	0	0	0	0	0	0	0	0	0	0	0	0	4	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
Nummulites venosus	4	9	2	3	1	3	1	1	0	0	2	2	0	0	0	0	3	28	0	0	34	1	0	0	9	4	8	1	4	7
Operculina discoidalis	0	9	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	3	0	0	0	0	0	0	0	0	0
Parahourinoides fragillissimus	0	9	0	0	0	0	0	0	0	0	0	3	0	0	0	0	0	0	0	0	0	0	0	0	0	1	0	0	0	0
Pararotalia calcariformata	0	9	0	0	0	0	0	0	0	0	0	0	0	0	0	4	0	0	1	0	0	0	0	0	4	0	0	0	0	0
Pararotalia domantayi	8	9	6	2	0	0	10	0	11	0	0	0	8	2	0	0	1	0	1	0	0	2	4	1	15	3	3	6	4	2
Parrelina hispidulla	0	9	0	0	0	0	0	0	0	0	0	0	0	1	6	1	2	6	1	0	0	0	0	0	0	1	1	1	1	1
Peneroplis pertusus	1	9	2	0	1	1	5	7	3	0	7	10	4	4	1	5	0	1	6	4	1	7	2	2	1	5	6	2	0	3
Peneroplis planatus	2	9	0	0	0	0	1	1	0	0	1	8	1	3	0	0	1	0	0	2	0	1	0	0	0	0	0	0	0	1
Pseudorotalia indopacifica	0	9	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	4	0	0	0	0	2	0	0	0
Quinqueloculina cuvieriana	0	9	0	0	0	0	1	0	0	1	1	1	1	0	3	8	0	0	0	1	0	1	1	1	5	3	2	1	0	1
Quinqueloculina incisa	0	9	0	0	0	0	0	0	0	0	0	0	0	0	0	2	1	0	0	0	0	3	1	0	0	0	0	1	0	0
Quinqueloculina parvaggluta	1	9	1	0	0	0	0	0	0	0	0	0	0	0	1	0	0	0	0	4	5	0	0	0	1	6	0	0	0	0
Quinqueloculina philippinensis	0	9	0	0	0	0	0	0	0	0	0	0	0	0	3	0	2	5	0	0	1	0	0	0	1	0	0	0	0	2
Quinqueloculina sulcata	0	9	0	1	0	0	0	0	0	0	0	0	1	1	0	0	0	0	0	0	0	3	1	0	0	0	0	0	0	0
Quinqueloculina vandiemeniensis	0	9	0	0	0	0	0	0	0	0	0	0	0	0	10	2	0	0	1	1	0	0	0	0	0	0	0	0	0	0
Rosalina globularis	0	9	0	0	0	0	0	0	0	4	0	0	0	0	0	1	1	0	0	0	0	0	0	0	0	1	0	1	0	0
Textularia agglutinans	0	9	0	0	1	0	0	0	1	0	1	1	0	0	0	0	0	0	4	0	0	0	0	0	0	0	0	0	0	0
Textularia lateralis	0	9	0	0	1	0	0	0	2	6	0	2	0	0	0	0	0	0	0	6	0	1	0	0	1	0	0	0	0	0
Triloculina marshallana	0	9	2	0	0	1	0	1	0	0	0	0	0	0	0	0	0	0	1	6	2	0	0	0	0	1	1	1	0	3
Triloculina tricarinata	0	9	0	0	0	0	0	3	9	0	3	4	1	0	1	6	8	0	7	0	0	0	0	0	0	1	0	1	0	1
Triloculinella bertheliniana	0	9	0	0	1	0	3	0	0	0	0	0	0	0	0	0	0	0	0	0	1	0	0	0	1	0	0	0	0	0
Triloculinella parisa	0	9	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0	3	0	0	1	0	0	0	0	0	0	0	1
Triloculinella chiastocytis	0	9	0	0	0	0	0	0	0	0	0	0	0	0	3	1	7	0	0	1	0	1	0	0	0	0	0	0	0	0

AVAILABILITY OF DATA AND MATERIALS

All data and materials for this manuscript will be shared upon request. Please contact for data requests.

FUNDING

This project was funded by the grant research from Department of Fisheries Malaysia (DOF), Joseph A. Cushman Award for Student Research (2019), Higher Institute Centre of Excellence (HICoE) research grant (Vote No. 66928) awarded to Institute of Oceanography and Environment (INOS), Universiti Malaysia Terengganu and Fundamental Research Grant Scheme (FRGS/1/2018/WAB09/UMT/02/3) provided by Ministry of Education Malaysia.

COMPETING INTERESTS

We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us.

We confirm that we have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. In so doing we confirm that we have followed the regulations of our institutions concerning intellectual property.

We understand that the Corresponding Author is the sole contact for the Editorial process (including Editorial Manager and direct communications with the office). He is responsible for communicating with the other authors about progress, submissions of revisions and final approval of proofs. We confirm that we have provided a current, correct email address which is accessible by the Corresponding Author and which has been configured to accept email from [email protected]

AUTHOR CONTRIBUTIONS FORM

ANAA has carried out the foraminifera analysis, statistical analysis and perform the calculation for FORAM index. Has also contributed in writing the manuscript.

FIM has proposed this study, contributed in major revision of the manuscript including statistical interpretation and writing the discussion.

HJP has contributed in critical revision of the manuscript with input on language and the flow of the manuscript.

HS and WNWS have contributed their research funding for field and laboratory works.

NA and OARAM has involved in field samples collection and laboratory analysis of sediment and organic matter content.

MNI has assisted and involved in the field sampling and data collections.

ACKNOWLEDGEMENTS

Authors would like to extend their gratitude to En. Syed Ahmad Rizal Tuan Nik and Syed Shahrul Afzan Syed Bidin for their help in surface sediment samples collection.

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

Status:

Version 1

Abstract

Figures

Introduction

Methods/experimental

Study site

Samples Collection

Laboratory analysis

Data analysis and statistical analysis

FORAM Index

Results

Foraminiferal Assemblages, Functional Groups and FORAM Index

Sediment characteristic of Pulau Tioman

Statistical analysis on benthic foraminiferal assemblages

Discussion

Conclusion

Appendix

Declarations

References

Status:

Version 1