Foraminifera assemblages in Pulau Redang: Uncovering Discrepancies and the Importance of FoRAM Index Calibration for Precise Reef Monitoring

Foraminifera assemblages in Pulau Redang: Uncovering Discrepancies and the Importance of FoRAM Index Calibration for Precise Reef Monitoring | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Foraminifera assemblages in Pulau Redang: Uncovering Discrepancies and the Importance of FoRAM Index Calibration for Precise Reef Monitoring FATIN IZZATI MINHAT, Che Din Mohd Safuan, Sabrina Alia Mohd Emran, and 4 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3784490/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract To mitigate the adverse effects of ocean warming on coral reef degradation, resource managers increasingly explore the management and regulation of local stressors to bolster coral resilience and recovery. Comprehensive assessments and monitoring efforts offer a holistic understanding of reef dynamic ecosystems. Using the Foraminifera-based Reef Assessment (FoRAM) index, we documented the distribution of benthic foraminiferal assemblages surrounding Pulau Redang, Malaysia, and assessed their potential for monitoring coral reef health. Undeveloped (R1–R3) and developed (R4–R6) reef sites revealed distinct differences in reef conditions. The significant presence of dead corals in R4–R6 is linked to Tropical Storm Pabuk. Foraminiferal distribution showed Amphistegina lessonii (14–34%) as the dominant species, followed by Calcarina hispida (21%) and Calcarina mayori (19%). Surprisingly, FoRAM consistently yielded high values across the study area despite varying coral reef conditions, probably due to the prevalence of Calcarina mayori in mesotrophic reefs (R4, R5, and R6), potentially skewing FoRAM values and providing a misleading indicator of reef conditions. We recommend calibrating the FoRAM Index, particularly in mesotrophic reefs where calcarinids dominate foraminiferal assemblages, to enhance its precision and reliability for coral reef health monitoring and assessment within the region. Earth and environmental sciences/Ecology Earth and environmental sciences/Environmental sciences/Environmental impact Earth and environmental sciences/Ocean sciences/Marine biology Figures Figure 1 Figure 2 Figure 3 INTRODUCTION Coral reefs in the tropics face diverse challenges arising from global and local stressors. Globally, rising ocean temperatures, driven by climate change, pose a significant threat, resulting in coral bleaching events and widespread coral mortality 1 . During coral bleaching events, enhancing water quality is considered crucial for the resilience and recovery rates of reef-building corals 2 , 3 . At the local level, coastal development and sewage discharge into marine environments have spurred the proliferation of macroalgae and the destruction of coral reefs 3 . Given the challenge of mitigating the adverse effects of ocean warming on coral reef degradation, resource managers are increasingly focusing on managing and regulating local stressors as an alternative approach to bolster coral resilience and recovery. Given the unique nature of each reef environment, assessments and monitoring efforts that use integrated data (i.e., coral distributions and bioindicators) may provide a comprehensive understanding of these dynamic ecosystems. Foraminifera are single-cell microscopic protists that inhibit various marine ecosystems, including coral reefs. In warm tropical coral reef environments, most foraminiferal assemblages consist of large and small benthic foraminiferal groups 4 – 6 . Larger benthic foraminifera (LBF) refers to a group of foraminiferal species that are relatively larger in size and engage in symbiotic relationships with various photosymbionts such as diatoms, cyanobacteria, dinoflagellates and rhodophytes 7 , 8 . LBF play a crucial role in the construction and maintenance of tropical carbonate platforms and are important components of reef ecosystems 9 , 10 . Meanwhile, smaller benthic groups constitute heterotrophic, smaller, and fast-growing species of foraminifera that do not have symbiotic relationships 11 , 12 . Within tropical coral reef environments, both LBF and smaller benthic taxa coexist, and their respective compositions demonstrate dynamic responses to the quantity of organic material 11 , water quality 8 , and characteristics of the surrounding substrate 13 . Notably, LBF, owing to their similar environmental requirements as corals, frequently exhibit early indicators of environmental health degradation within the area 12 – 14 . This unique trait positions LBF as valuable indicator species for assessing the ecological well-being of coral reef ecosystems 4 , 12 . Since the early 2000s, the Foraminifera-based Reef Assessment (FoRAM) index has gained global recognition as a pivotal monitoring tool for coral reefs and marginal sea areas 14 – 18 . Its notable success in reef monitoring efforts resonates across numerous regions, notably in the Atlantic Ocean 19 , 20 , extending to locales such as Tioman Island in Malaysia 6 . Notwithstanding these achievements, several studies have highlighted the potential limitations of this index in the Indo-Pacific region, emphasising the need for species-specific calibration and refinement to ensure its applicability and accuracy. The present study aimed to document the distribution of benthic foraminifera assemblages around Pulau Redang, Malaysia, and to assess their potential as an effective tool in monitoring coral reef health. RESULTS Biotic and Abiotic components in coral reef areas The percentage coverage of biotic and abiotic components in the coral reefs area, Pulau Redang, was reported previously 21 . multi-dimensional scaling (MDS) analysis (Fig. 1 ) clearly showed degradation of the coral reef located close to the development area largely affected by anthropogenic activities. This is shown by the high dead coral cover in R5 and R6 21 . Meanwhile, a high cover of algae and other invertebrates (mainly zoanthids – data not shown) was found in R4, indicating a potential nutrient enrichment and zoanthid-dominated reef, which causes low live coral cover in the area (Fig. 1 : R4). Sediment grain size analysis indicated that all study sites were covered with coarse sandy sediment types (Table 1 ). The organic matter composition ranged between 2.6–5.4%, with the highest concentration recorded in R6. Table 1 The water depth and sediment grain size composition in all six study sites around Pulau Redang. Station Water Depth (m) Organic matter Gravel > 1 mm Coarse sand 500 µm medium sand 250 µm Fine sand 125 µm Mud < 63 R1 6 2.6 54.3 34.7 11.0 0.0 0.0 R2 6 2.7 69.8 27.3 2.8 0.0 0.0 R3 6 2.8 57.5 18.6 23.5 0.4 0.0 R4 6 3.9 46.0 35.1 18.5 0.3 0.0 R5 6 3.1 20.5 25.3 53.5 0.7 0.0 R6 13 5.4 40.5 35.6 21.4 2.2 0.3 Foraminifera assemblage and distribution A total of 32 species of benthic foraminifera were identified in the coral reef of Pulau Redang. Among these, 22 species fell under the category of LBF. The foraminiferal assemblage was dominated by the hyaline group (92%), followed by the porcelaneous (6%) and agglutinated groups (2%) (Table 2 ). Overall, Amphistegenids ( Amphistegina lessonii , 22%, and Amphistegina lobifera , 9%) and calcarinids ( Calcarina mayori , 19%, and Calcarina hispida , 21%) co-dominated the reef foraminifera assemblage in Pulau Redang. In sites R1–R5, where the water depth ranged between 5–7 m, A. lessonii exhibited a relative abundance of > 15%. In R6, with water depths between 10–15 m, the most dominant LBF species was C. hispida (43%). Additionally, C. mayori (> 20% relative abundance) was more dominant on the west side of the island. The Fisher’s alpha (α) diversity index indicated that foraminifera assemblages in R1–R3 were relatively more diverse (α > 5) than those in R4–R6 (α = 2.77–3.97). Similarly, the values of the Shannon-Wiener diversity index were higher in R1–R3 (H’= 2.16–2.39) compared to R4–R6 (H’= 1.64–2.01). The FoRAM Index (FI) calculated for all study areas was notably high (FI = 8–9). These values indicate that all areas are conducive to coral reef growth with good recoverability from future stress to the ecosystem. Table 2 The percentage of foraminifera species according to test types, the Foraminifera for Reef Monitoring (FoRAM) Index values, and diversity indices for all study sites around Pulau Redang. Station Calcareous % Porcelaneous % Agglutinated % FoRAM Index (FI) Shannon-Wienner (H’) Pielou’s Evenness (J’) Fisher’s alpha (α) R1 89 9 2 8 2.39 0.55 7.56 R2 97 2 0 9 2.16 0.54 5.35 R3 84 15 1 8 2.21 0.57 5.43 R4 97 1 2 9 1.91 0.56 3.59 R5 90 8 2 9 2.01 0.58 3.97 R6 94 3 3 9 1.64 0.51 2.77 Based on Q-mode cluster analysis, the distribution of foraminiferal assemblages in Pulau Redang can be divided into two groups: Group A, comprising three stations on the west side of the island (R1–R3), and Group B, comprising three stations on the east side of the island (R4–R6) (Table 3 ). Table 3 The cluster groups defined by Q-mode cluster analysis at Pulau Redang. The Anthropogenic Pressure* was based on the classification made by Lachs et al. 3 . The water depth, live coral cover, organic matter composition, Fisher’s alpha diversity values, and abundance data are shown as maximum and minimum values. Cluster group Group A Group B Samples ID R1, R2, R3 R4, R5, R6 Locations Western Pulau Redang Eastern Pulau Redang Anthropogenic Pressure* Low High Water depth (m) 5–7 m 5–15 m Live coral cover (%) 30–39% 8–20% Organic matter (%) 2.6–2.8% 3.1–5.4% Fisher's alpha values (α) 5.35–7.56 2.77–3.97 Symbiont-bearing group (%) 82 90 Heterotrophic group (%) 5 2 Stress tolerant group (%) 13 8 Average taxa > 10% A. lessonii (15–34%) C. mayori (23–37%) C. hispida (6–32%) C. hispida (10–43%) A. lobifera (5–18%) A. lessonii (14–24%) Canonical correspondence analysis (CCA) was employed to determine the correlation between foraminiferal species and environmental spatial distribution. The results indicate that the composition of organic matter and substrate type (i.e., live and dead coral cover) affect the distribution of benthic foraminiferal assemblages in Pulau Redang (Fig. 2 ). The abundances of C. mayori and Amphistegina radiata could be correlated with higher organic matter composition, increased water depth, higher fine sand content, and algae and dead coral cover. DISCUSSION Over the years, ongoing monitoring by the Reef Check Association around Pulau Redang has documented a decline in live coral cover, decreasing from over 50% in 2011 to 28% in 2019. The primary driver behind this decrease was believed to be the substantial increase in crown-of-thorns starfish (COT) observed between 2016 and 2018 22 . Additionally, the substantial reduction in live coral cover in 2019 was linked to the impact of Tropical Storm Pabuk, which struck early in that year 21 . However, a remarkable turnaround was observed in the reefs surrounding Pulau Redang in 2020 23 , possibly attributed to the restrictions imposed on tourism during the COVID-19 (SARS-CoV-2 virus) pandemic. Despite this, the reef recovery from the Pabuk event around Pulau Redang falls short, as records in 2022 show the reef condition to be ‘Fair’ compared to ‘Excellent’ in 2020 22 . In this study, three (R4–R6) of the six stations belonged to the area subjected to the annual Reef Check Association monitoring. The observations by Razak et al. 21 underscored the persistent ‘poor’ coral conditions in these reef areas, pointing to a threat posed by anthropogenic activities to the reefs near coastal development 3 . This region has a low live coral cover, predominantly featuring dead coral, with some sites exhibiting a considerably high algal cover, along with other invertebrates such as zoanthids 3 , 21 . Additionally, the nutrient influx from improper drainage systems may have driven the domination of macroalgae that compete with corals for space, thereby compromising the resilience of coral reef ecosystems 3 , 24 . This effect is consistent with the areas with poor reef cover, such as R4, situated in areas with high anthropogenic pressure, where improper waste discharge may promote algal colonisation 21 . In reef ecosystems, benthic foraminifera offer advantages as bioindicators due to their short life spans (a few weeks to ~ 2 years) and quicker response to changes in nutrient flux compared to reef-building corals with potential multi-year responses 12 , 25 . Therefore, changes in water quality, not immediately detectable in adult reef-building corals, may lead to rapid increases in populations of shorter-lived, purely heterotrophic species of benthic foraminifera, causing a reduction in the proportions of LBF 26 . Nevertheless, unlike corals, foraminifera remain resilient against coral-specific diseases, and their communities demonstrate remarkable resistance to perturbations from cyclone events or COT outbreaks 27 . The Indo-Pacific region hosts over 60 LBF morphospecies, a number continually expanding with ongoing research efforts 8 , 28 . A total of 22 LBF species were successfully identified from Pulau Redang, with 11 species exhibiting a relative abundance of > 2%. In the Philippines, Heterostegina depressa , Calcarina mayori , and Amphistegina lessonii are among the most widespread, particularly in the reef slope environments 28 . In Pulau Redang, A. lessonii (14–34%) is one of the most prevalent species distributed in the reef-flat environment, followed by Calcarina hispida (21%) and C. mayori (19%). These findings echo research on Tioman Island, where a comparable study recorded an average relative abundance of A. lessonii of 21% 28 . A. lessonii demonstrates remarkable adaptability to water depths, reaching up to approximately 100 m 29 , and exhibits considerable abundance across various locations in the Indo-Pacific region 28 , 30 . The most prevalent calcarinids in Pulau Redang are C. hispida (6–43%) and C. mayori (2–37%). Both species have been reported to have different habitat preferences in the Spermonde Archipelago. C. hispida thrives in reef-flat areas with water depths ranging between 1–6 m, while C. mayori is typically found in reef slope areas with depths reaching up to 24 m 13 . In this study, both species were observed in reef-flat areas along the east and west coasts of Pulau Redang. The CCA results revealed a substantial influence of substrate type and organic matter composition on the distribution of benthic foraminifera in the reef environments of Pulau Redang. The influence of substrate type on the local distribution of benthic foraminifera in reef environments is a significant yet complex environmental factor 8 , 31 , 32 . Within Pulau Redang, the Q-mode cluster analysis classified the foraminiferal assemblages into two groups (Table 3 ). Group A represented samples collected from the western coast of Pulau Redang. Here (R1–R3), the coral reef ecosystems received minimal anthropogenic pressure and were classified as pristine sites 3 . With more than 30% live coral and low algal cover, the foraminiferal assemblage was characterised by a high abundance of amphisteginids (> 40%) and dominated by A. lessonii (26%), C. hispida (19%), and A. lobifera (10%). Here, foraminiferal assemblages exhibited higher diversity (α > 5) compared to Group B. In contrast, Group B included areas facing high anthropogenic pressure, mainly from tourism, sewage nutrient enrichment, and coastal development 3 , 33 . The area along Pasir Panjang (R4–R5) exhibits relatively high dead coral cover, with coral rubble dominating the substrate. The foraminiferal assemblage here is dominated by calcarinids, with an average relative abundance of > 50%. The presence of dead coral rubble and an alga-dominated environment is conducive to the high abundance of Calcarina mayori (37%), particularly in R4. Interestingly, Calcarina mayori in Pulau Redang showed increased abundance in areas with higher algal cover. These observations are consistent with those of studies on the Indo-Pacific reef, associating calcarinids with the presence of algae and seagrass communities in areas characterised by coarse sandy substrates 34 , 35 . Overall, the FI indicated high values (FI = 8–9) across all reef sites and areas within Pulau Redang despite notable variations in observed coral reef conditions. Notably, both the western and eastern coral reef areas of Pulau Redang exhibited a remarkably high prevalence of symbiont-bearing species, exceeding 80% in relative abundance. It is worth noting that high FI values suggest strong potential for reef recovery within the Pulau Redang reef area, even in R4-R6, where “poor” coral conditions have been observed 21 . The FI has proven its effectiveness as a reliable proxy for assessing reef conditions, particularly in the western Atlantic and Caribbean regions 12 . Notably, this index exhibits a strong correlation with the water quality in the Great Barrier Reef of the Pacific Ocean 27 , 36 . The application of the FI to Tioman Island accurately reflects the true state of the local reef environment 6 . However, despite the strong resemblance between FI values and reef recovery records, previous studies have highlighted that the persistence of high FI values in mesotrophic reefs is often attributed to dense populations of calcarinids, a symbiont-bearing group 12 , 37 . In our investigation of Pulau Redang, on average, calcarinids constituted approximately 34% of the relative abundance within Group A (R1–R3), an area characterised by minimal anthropogenic influence. In contrast, within the mesotrophic reef zone of Group B (R4–R6), calcarinids represented an average of 55% of the total foraminiferal assemblages. This is attributed to the epiphytic proliferation of certain Calcarinidae family species on a range of macrophytic algae. Interestingly, the high algal coverage (8%) in R4 correlated well with the increase in calcarinids (relative abundance of 58%). Studies indicate that in highly stressed reef environments with available sunlight, calcarinid densities tend to rise with increased algal cover 12 , 37 . Therefore, suggestions for calibrating the FI for the Indo-west Pacific region, where Calcarinidae occur 12 , are particularly relevant, especially where algal cover visually surpasses coral cover. The dataset from Pulau Redang primarily focused on sediment quality and coral cover. However, due to the unavailability of water quality records, we were unable to establish a direct correlation between the FI and water quality near the reef. Nevertheless, our observations revealed an increase in calcarinid prevalence within areas of Pulau Redang dominated by algae. This phenomenon persisted despite suboptimal coral conditions and relatively low live coral cover. Intriguingly, the FI consistently indicated high FI values, suggesting favourable conditions for coral recovery. Hence, we believe that a tailored calibration of the FI is imperative, especially within mesotrophic reefs where calcarinids dominate. Coral reefs worldwide face threats from natural and anthropogenic factors, emphasising the urgent need for preservation amid global warming. Our observations in Pulau Redang revealed vulnerable reefs near coastal development, which remain at risk from human activities. Recent tropical storms have dramatically altered the structural landscape of these reefs, resulting in extensive damage, particularly to the shallow-water branching and tabulating coral species. The storm's aftermath appears to be a contributing factor to the poor coral conditions, particularly on the eastern side of the island. Foraminifera are effective monitoring tools for assessing coral reef health. The FI, designed as a straightforward indicator, assesses whether water quality supports calcifying organisms that host algal endosymbionts, reflecting the potential for reef recovery. In Pulau Redang, the foraminiferal species distribution conformed to the typical assemblage of tropical reefs, with symbiont-bearing taxa dominating the community. Surprisingly, the FI consistently recorded high values throughout the study area despite notable variations in observed coral reef conditions. While the FI has been successfully applied to Tioman Island, its application to Pulau Redang presents different challenges. We believe that a customised calibration of the FI is imperative, especially in mesotrophic reefs where calcarinids dominate foraminiferal assemblages. Such calibration is essential for enhancing the accuracy and reliability of the index as a valuable tool for monitoring and assessing coral reef health in the region. METHODS Study area This study was conducted in Pulau Redang (5°46'38.30"N, 103° 0'40.06"E), a gazetted marine park. The island is situated in Terengganu waters along the shallow, tropical shelf on the east coast of Peninsular Malaysia (Fig. 3 ). The primary economic activities of the island's inhabitants are closely tied to tourism. The central region of Pulau Redang is intensively developed with a small airport, hotels, resorts, and residential areas (Fig. 3 ). Another extensively developed area is along the sandy beaches, which are situated on the east coast of the island (Fig. 3 ). Pulau Redang experiences two monsoonal systems: the northeast (October-March) and the southwest monsoon (April-August) 38 . The sea conditions along the east coast of Peninsular Malaysia are relatively calmer during the southwest monsoon (dry season) compared to the period during the northeast monsoon (wet season), which brings heavy rain and strong winds 39 . Depending on the season, the near-bottom temperature recorded in the study area ranged between 26–30°C 40 . Additionally, more frequent intense tropical storm events during the northeast season have been observed along the east coast of Peninsular Malaysia in recent years 41 . The magnificent coral reef area has contributed to Pulau Redang's flourishing as a tourist destination. Based on a dataset by Akmal et al. 42 and a report by Reef Check Malaysia in 2020 43 , coral reefs in the marine parks can be categorised from ‘poor’ to ‘good’ coral condition following the criteria of coral health status by Chou et al. 44 . As indicated by Akmal et al. 42 , less affected reef zones by coastal development and human activities have established good coral conditions and higher coral genera diversity. This was further proven by Lachs et al. 3 , which highlighted the effect of tourism development in some parts of the island that caused ‘poor’ reef conditions. Apart from that, coral reefs in Pulau Redang also experienced coral bleaching in 2010, as reported by Tan and Heron 45 , showing that natural disturbances also affect the health status of the reef. In-situ data and sediment collections Coral reef assessment was carried out using standard protocol video sampling in July 2022 46 . Method for Coral Video Transect (CVT) has been published in Razak et al. 21 . As for foraminifera and the sediment collections, two sediment samples were collected along each transect. The sediments were collected by the diver by scooping the surface sediment into plastic bags and centrifuge tubes. The permission for sample collection in this study has been approved by the Department of Fisheries Malaysia. For foraminifera analysis, approximately 30 cm 3 of sediment was placed into the centrifuge tube. On board, the sediments were fixed with buffered ethanol (> 90%) 12,47 . All sediment samples were brought back to the laboratory for analysis. Foraminifera analysis In the laboratory, the preserved samples underwent a gentle washing process under running tap water, using a 63 µm sieve to eliminate extraneous silt and clay 47 . The resulting residues were carefully transferred into a pre-labelled weighing boat. The samples were then dried in an oven at a temperature range of 40–50°C for 24 h 48 . After drying, the samples were divided into manageable aliquots, and approximately 300 foraminiferal specimens were handpicked at random from each sample using a fine brush (000) with the aid of a 40× light microscope 17 . The specimens were then sorted and mounted on a micropalaeontological slide coated with non-toxic, water-soluble glue to ensure immobility 49 . Benthic foraminifera were identified based on the criteria established by Loeblich and Tappan 50 , as well as insights from regional literature sources 8 , 48 , 51 , 52 . To avoid reworking the specimens during the picking process, foraminiferal tests displaying any discoloration, breakage, or poor preservation 53 were excluded. Sediment and organic matter analysis In this study, dry sieving methods 54 were used to determine the sediment grain size. For sediment grain size analysis, all samples underwent pretreatment with HCl (10%) to dissolve chunky carbonate fragments. Next, the samples were rinsed and oven-dried at 50°C for 36 h. Once dried, approximately 100 g samples were sieved using a set of sieves with sizes 4000, 2000, 1000, 500, 250, 125, and 63 µm, and the percentage of each sediment size fraction was determined. The organic matter content of the sediments was assessed using the loss on ignition (LOI) method 55 , 56 . Prior to heating, 5 g of each sediment sample was weighed. The samples were combusted at 550°C for 4 h and then left to cool to room temperature (30°C) before the final weight was recorded. The percentage of organic matter was calculated using the formula described previously 56 . Data analysis Coral data analysis The coral cover around Pulau Redang was reported by Razak et al. 21 as a percentage cover. The percentage cover includes live coral (C), algae (ALG), other invertebrates (OT), dead coral (DC), and sand, silt, or rock (SR). A MDS analysis was performed in this study to understand the correlation between coral cover distribution and anthropogenic pressures (developed and non-developed areas). Foraminiferal data analysis To avoid reworked specimens, only foraminiferal species with a relative abundance greater than 2% were retained for subsequent statistical analysis. For comparison with A’ziz et al. 6 , we calculated diversity indices such as Fisher’s alpha diversity index (α), Shannon-Wiener species diversity (H′), and species evenness of Pielou (J′) using PAST (Palaeontological STatistics) software version 3. Relative abundance data were derived from the mean average of foraminiferal species across replicates. Q-mode cluster analysis, based on the Euclidean distance similarity measure, was used to identify the similarity of fauna assemblages between the study sites 6 , 57 . CCA was used to test the correlation between sediment characteristics, organic matter content, coral reef cover, and foraminiferal assemblages. To evaluate the applicability of the FI in Pulau Redang, the identified foraminiferal species were classified into three functional groups, following the classifications of Hallock et al. 4 and Carnahan et al. 11 (Supplementary 1). The FI was calculated for each site using the equation proposed by Hallock et al. 4 . Declarations ACKNOWLEDGEMENTS This study is funded by the Fundamental Research Grant Scheme (FRGS /1/2022/WAB07/UMT/02/1). AUTHOR CONTRIBUTIONS Fatin I. Minhat: Contributed to conceptualization, investigation, writing and major revision of the manuscript, Supervision, and funding acquisition. Che Din Mohd Safuan: Contributed to conceptualization, methodology on coral analysis, writing – review, and editing. Sabrina A. M. Emran: performed foraminifera analysis, statistical analysis, and the original writing of the manuscript. Aida F. M. Hasnizul: performed foraminifera analysis, sediment and organic matter analysis, and original writing of the manuscript. Aminudin Muhammad Afiq-Firdaus: performed field sample collections, data analysis, and statistical analysis on coral cover and distributions. Zainudin Bachok: contributed to conceptualization, review, and editing of the manuscript. Wan I. A.W. Talaat: contributed to the conceptualization, review, and editing of the manuscript. DATA AVAILABILITY STATEMENT All data generated or analysed during this study are included in this article (and its Supplementary Information files) COMPETING INTERESTS STATEMENT The authors declare no competing interests. References Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543 , 373–377 (2017). (DOI 10.1038/nature21707) MacNeil, M. A. et al. Water quality mediates resilience on the Great Barrier Reef. Nat. Ecol. Evol. 3 , 620–627 (2019). (DOI 10.1038/s41559-019-0832-3) Lachs, L. et al. 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Adopting Marine Spatial Planning (MSP) using coral health assessment as indicator: A case study in Pulau Redang Marine Park, Malaysia. Ocean & Coastal Management. 248 , 106943 (2024). (DOI 10.1016/j.ocecoaman.2023.106943) Reef Check. Malaysia Annual Survey Report (Kuala Lumpur: Reef Check Malaysia, 2022). Reef Check. Malaysia Annual Survey Report (Kuala Lumpur: Reef Check Malaysia, 2021). Heery, E. C. et al. Urban coral reefs: degradation and resilience of hard coral assemblages in coastal cities of East and Southeast Asia. Mar. Pollut. Bull. 135 , 654–681 (2018). (DOI 10.1016/j.marpolbul.2018.07.041) Crevison, H. L., McRae, G & Hallock, P. Sediment cores from the Florida Keys (USA): is resolution sufficient for environmental applications?. Journal of Environmental Micropaleontology, Microbiology, and Meiobenthology. 3 ,61 (2006). Kelmo, F. & Hallock, P. Responses of foraminiferal assemblages to ENSO climate patterns on bank reefs of northern Bahia, Brazil: A 17-year record. Ecological Indicators. 30, 148-157 (2013). (DOI 10.1016/j.ecolind.2013.02.009) Uthicke, S., Thompson, A. & Schaffelke, B. Effectiveness of benthic foraminiferal and coral assemblages as water quality indicators on inshore reefs of the Great Barrier Reef, Australia. Coral Reefs 29 , 209–225 (2010). (DOI 10.1007/s00338-009-0574-9) Förderer, M. & Langer, M. R. Exceptionally species-rich assemblages of modern larger benthic foraminifera from nearshore reefs in northern Palawan (Philippines). Rev. Micropaleontol. 65 , 100387 (2019). (DOI 10.1016/j.revmic.2019.100387) Hohenegger, J. Depth coenoclines and environmental considerations of western Pacific larger foraminifera. J. Foram. Res. 34 , 9–33 (2004). (DOI 10.2113/0340009) Renema, W. Larger foraminfera as marine environmental indicators. Scr. Geol. 124 , 1–260 (2002). Hohenegger, J. Distribution of living larger foraminifera NW of Sesoko‐Jima, Okinawa, Japan. Mar. Ecol. 15 , 291–334 (1994). (DOI 10.1111/j.1439-0485.1994.tb00059.x) Renema, W. Habitat variables determining the occurrence of large benthic foraminifera in the Berau area (east Kalimantan, Indonesia). Coral Reefs 25 , 351–359 (2006). (DOI 10.1007/s00338-006-0119-4) Praveena et al. , 2010 Renema, W. & Troelstra, S. R. Larger foraminifera distribution on a mesotrophic carbonate shelf in SW Sulawesi (Indonesia). Palaeogeogr. Palaeoclimatol. Palaeoecol. 175 , 125–146 (2001). (DOI 10.1016/S0031-0182(01)00389-3) Meng, M., Yu, K., Hallock, P. & Qin, G. Distribution of recent Foraminifera as depositional indicators in Yongle Atoll, Xisha Islands, South China Sea. Mar. Micropaleontol. 158 , 101880 (2020). (DOI 10.1016/j.marmicro.2020.101880) Fabricius, K. E. et al. A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar. Pollut. Bull. 65 , 320–332 (2012). (DOI 10.1016/j.marpolbul.2011.09.004) (Pubmed:21978685) Renema, W. Is increased calcarinid (foraminifera) abundance indicating a larger role for macro-algae in Indonesian Plio-Pleistocene coral reefs? Coral Reefs 29 , 165–173 (2010). (DOI 10.1007/s00338-009-0568-7) Akhir, M., Fadzil, M., Zakaria, N. Z. & Tangang, F. Intermonsoon variation of physical characteristics and current circulation along the east coast of Peninsular Malaysia. Int. J. Oceanogr. , 1–9 (2014). (DOI 10.1155/2014/527587) Roseli, N. H. M. & Akhir, M. F. Variations of southern South China Sea characteristics near Pahang. Sains Malays. 43 , 1389–1396 (2014). Roseli, N. H. & Akhir, M. F. Temperature variability caused by internal tides in the coastal waters of east coast of Peninsular Malaysia. Acta Oceanol. Sin. 38 , 22–31 (2019). (DOI 10.1007/s13131-019-1367-9) Santos, C. F. D. et al. Marine spatial planning in World Seas: an Environmental Evaluation . III : Ecological Issues and Environmental Impacts (2nd ed., pp. 571–592) (Elsevier, 2019). (DOI 10.1016/b978-0-12-805052-1.00033-4) Akmal, K. F., Shahbudin, S., Faiz, M. H. M. & Hamizan, Y. M. Diversity and abundance of scleractinian corals in the East Coast of peninsular Malaysia: A case study of redang and Tioman Islands. Ocean Sci. J. 54 , 435–456 (2019). (DOI 10.1007/s12601-019-0018-6) Reef Check. Malaysia Annual Survey Report (Kuala Lumpur: Reef Check Malaysia, 2020). Chou, L. M. et al. Status of coral reefs in the ASEAN region in (eds Wilkinson, C. R., Chou, L. M. & Sudara, S.). Proceedings of the Third Asean-Australia Symposium on Living Coastal Resources (Bangkok, Thailand: Chulalongkorn University, 1995). 16–20 May 1994. Tan, C. H. & Heron, S. F. First observed severe mass bleaching in Malaysia, Greater Coral Triangle. J. Coral Reef Stud. 13 , 27–28 (2011). (DOI 10.3755/galaxea.13.27) Safuan, M., Boo, W. H., Siang, H. Y., Chark, L. H. & Bachok, Z. Optimization of coral video transect technique for coral reef survey: comparison with intercept transect technique. Open J. Mar. Sci. 05 , 379–397 (2015). (DOI 10.4236/ojms.2015.54031) Schönfeld, J. et al. The FOBIMO (FOraminiferal BIo-MOnitoring) initiative: towards a standardised protocol for soft-bottom benthic foraminiferal monitoring studies. Mar. Micropaleontol. , 94.e95, 1e13 (2012). (DOI 10.1016/j.marmicro.2012.06.001) A’ziz, A. N. A. et al. Reef foraminifera as bioindicators of coral reef health in southern South China Sea. Sci. Rep. 11 , 8890 (2021). (DOI 10.1038/s41598-021-88404-3) Scott, D. B., Medioli, F. S. & Schafer, C. T. Monitoring in Coastal Environments Using Foraminifera and Thecamoebian Indicators ; 177pp (Cambridge University Press, 2001). (DOI 10.1017/CBO9780511546020) Loeblich, A. R. & Tappan, H. Foraminiferal Genera and Their Classification (Van Nostrand Reinhold, 1987). Martin, S. Q. et al. Distribution and taxonomy of modern benthic Foraminifera of the Western Sunda Shelf (South China Sea) off peninsular Malaysia. Cushman. Spec. Publ. Cushman Found. Foram. Res. 47 (2018). Azmi, N. et al. Distribution of benthic foraminifera off Kelantan, Peninsular Malaysia, South China Sea. J. Foram. Res. 50 , 89–96 (2020). (DOI 10.2113/gsjfr.50.1.89) Yordanova, E. K. & Hohenegger, J. Taphonomy of larger foraminifera: relationships between living individuals and empty tests on flat reef slopes (Sesoko Island, Japan). Facies 46 , 169–203 (2002). (DOI 10.1007/BF02668080) Folk, R. L. Petrology of Sedimentary Rocks 182 (Austin, TX: Hemphill Publishing Company, 1980). Dean, W. E. Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition; comparison with other methods. J. Sediment. Res. 44 , 242–248 (1974). Heiri, O., Lotter, A. F. & Lemcke, G. Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J. Paleolimnol. 25 , 101–110 (2001). (DOI 10.1023/A:1008119611481) Culver, S. J. et al. Distribution of foraminifera of the Poverty continental margin, New Zealand: implications for sediment transport. J. Foram. Res. 42 , 305–326 (2012). (DOI 10.2113/gsjfr.42.4.305) Additional Declarations No competing interests reported. Supplementary Files Supplementarymaterial.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3784490","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":264579022,"identity":"55e50908-6602-4089-9835-28e6ffc33460","order_by":0,"name":"FATIN IZZATI MINHAT","email":"","orcid":"","institution":"University Malaysia Terengganu","correspondingAuthor":false,"prefix":"","firstName":"FATIN","middleName":"IZZATI","lastName":"MINHAT","suffix":""},{"id":264579023,"identity":"debec1ac-d6ea-4aa9-947c-c598a194dc74","order_by":1,"name":"Che Din Mohd Safuan","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABE0lEQVRIiWNgGAWjYDACCSBKANIGDECyAsjgh4gzE6nlDJAh2cDA2EBQCwOyFoMDBLTwz24+eOPhjm1y5uzpDz8cbLPLM76Rnf6AocI6sUHsjAFWS+4cS7ZIPHPb2LLnjbHEwbbkYrMbuRsbGM6kJzZI52DVYiCRYyaR2HY7ccONHAbpj23MidtAWhjbDuPRkv8NqiX98Y+DbfWJm2eAtPzDpyWHDaolwQzosMOJGyRAWhpwa5G4kWZsAdRibHDmjZnFgXPHE2ecebtxRsKxdOM26bQCrCE2I/nhzZ9tt+UMjqc/vnGgrDqxvz13w4cPNday/dLJG7CGMnaQAMRsDBxYHYYXsD8gWcsoGAWjYBQMRwAACNtxBzDq+70AAAAASUVORK5CYII=","orcid":"","institution":"University Malaysia Terengganu","correspondingAuthor":true,"prefix":"","firstName":"Che","middleName":"Din Mohd","lastName":"Safuan","suffix":""},{"id":264579024,"identity":"0a9310c5-ed98-4e67-af3c-a21d061d8e71","order_by":2,"name":"Sabrina Alia Mohd Emran","email":"","orcid":"","institution":"University Malaysia Terengganu","correspondingAuthor":false,"prefix":"","firstName":"Sabrina","middleName":"Alia Mohd","lastName":"Emran","suffix":""},{"id":264579025,"identity":"dfc5eadb-7383-4deb-ab9a-8092f8457b38","order_by":3,"name":"Aida Farisah Mohd Hasnizul","email":"","orcid":"","institution":"University Malaysia Terengganu","correspondingAuthor":false,"prefix":"","firstName":"Aida","middleName":"Farisah Mohd","lastName":"Hasnizul","suffix":""},{"id":264579026,"identity":"35fa4196-7740-4dce-a4f1-50cd9ac31890","order_by":4,"name":"Aminudin Muhammad Afiq-Firdaus","email":"","orcid":"","institution":"Universiti Malaysia Terengganu","correspondingAuthor":false,"prefix":"","firstName":"Aminudin","middleName":"Muhammad","lastName":"Afiq-Firdaus","suffix":""},{"id":264579027,"identity":"c6eb3290-f5ac-4ea3-99b9-5bd99c5f04e7","order_by":5,"name":"Zainudin Bachok","email":"","orcid":"","institution":"Universiti Malaysia Terengganu","correspondingAuthor":false,"prefix":"","firstName":"Zainudin","middleName":"","lastName":"Bachok","suffix":""},{"id":264579028,"identity":"687087a9-0c77-48c1-a522-2fb309836457","order_by":6,"name":"Wan Izzatul Asma Wan Talaat","email":"","orcid":"","institution":"Universiti Malaysia Terengganu","correspondingAuthor":false,"prefix":"","firstName":"Wan","middleName":"Izzatul Asma Wan","lastName":"Talaat","suffix":""}],"badges":[],"createdAt":"2023-12-21 03:14:03","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3784490/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3784490/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":49018016,"identity":"d58f2fbc-21c5-462d-b935-3878920243da","added_by":"auto","created_at":"2024-01-01 06:17:12","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":324757,"visible":true,"origin":"","legend":"\u003cp\u003eRelative percentage cover (a) and multi-dimensional scaling (MDS) of biotic (C, ALG, and OT) and abiotic (DC, SR) components in coral reef areas between different sites (n = 4 per site) and areas (n = 12 per area)\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-3784490/v1/0759bc4e6026994bbad6d73a.png"},{"id":49018088,"identity":"445ce42d-fbe6-4d81-b7a0-bd528235ad54","added_by":"auto","created_at":"2024-01-01 06:25:12","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":63079,"visible":true,"origin":"","legend":"\u003cp\u003eThe Canonical Correspondence Analysis triplot between environmental variables and foraminifera species and samples (R1-R6) from Pulau Redang. The variance of data along axis-1 is 42.05%, while the variance of data along axis-2 is 27.11%. (Other inv = Other invertebrates, \u003cem\u003eA. bici\u003c/em\u003e= \u003cem\u003eA. bicirculata, Q. \u003c/em\u003esp = \u003cem\u003eQuinqueloculina\u003c/em\u003e sp., \u003cem\u003eOper. amm \u003c/em\u003e= \u003cem\u003eOperculina ammonoides\u003c/em\u003e, \u003cem\u003eC. brad\u003c/em\u003e = \u003cem\u003eCymbaloporetta bradyi, S. glob = Sphaerogypsina globula\u003c/em\u003e)\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-3784490/v1/3a0882ed6d4de2b456564869.png"},{"id":49018018,"identity":"861c8b0b-69d3-46e4-b490-5c026f633ba7","added_by":"auto","created_at":"2024-01-01 06:17:12","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":261417,"visible":true,"origin":"","legend":"\u003cp\u003eThe study area shows the map of A- Peninsular Malaysia, with a box marking Pulau Redang and B- the distribution of sampling sites and land use at Pulau Redang.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-3784490/v1/24efa2c5c9d9ab15dcbe44f5.png"},{"id":54670574,"identity":"bb22b7ba-44e2-452f-abeb-7ef6fb7fe31a","added_by":"auto","created_at":"2024-04-15 04:54:28","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1057495,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3784490/v1/33f9adba-7a0f-461a-a597-6838748ace35.pdf"},{"id":49018019,"identity":"396e8e06-2702-4340-9db5-6095cc66bc4f","added_by":"auto","created_at":"2024-01-01 06:17:12","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":16052,"visible":true,"origin":"","legend":"","description":"","filename":"Supplementarymaterial.docx","url":"https://assets-eu.researchsquare.com/files/rs-3784490/v1/ad5257d730ecdddface04213.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Foraminifera assemblages in Pulau Redang: Uncovering Discrepancies and the Importance of FoRAM Index Calibration for Precise Reef Monitoring","fulltext":[{"header":"INTRODUCTION","content":"\u003cp\u003eCoral reefs in the tropics face diverse challenges arising from global and local stressors. Globally, rising ocean temperatures, driven by climate change, pose a significant threat, resulting in coral bleaching events and widespread coral mortality\u003csup\u003e\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u003c/sup\u003e. During coral bleaching events, enhancing water quality is considered crucial for the resilience and recovery rates of reef-building corals\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e,\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. At the local level, coastal development and sewage discharge into marine environments have spurred the proliferation of macroalgae and the destruction of coral reefs\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. Given the challenge of mitigating the adverse effects of ocean warming on coral reef degradation, resource managers are increasingly focusing on managing and regulating local stressors as an alternative approach to bolster coral resilience and recovery. Given the unique nature of each reef environment, assessments and monitoring efforts that use integrated data (i.e., coral distributions and bioindicators) may provide a comprehensive understanding of these dynamic ecosystems.\u003c/p\u003e \u003cp\u003eForaminifera are single-cell microscopic protists that inhibit various marine ecosystems, including coral reefs. In warm tropical coral reef environments, most foraminiferal assemblages consist of large and small benthic foraminiferal groups\u003csup\u003e\u003cspan additionalcitationids=\"CR5\" citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e. Larger benthic foraminifera (LBF) refers to a group of foraminiferal species that are relatively larger in size and engage in symbiotic relationships with various photosymbionts such as diatoms, cyanobacteria, dinoflagellates and rhodophytes\u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e,\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e\u003c/sup\u003e. LBF play a crucial role in the construction and maintenance of tropical carbonate platforms and are important components of reef ecosystems\u003csup\u003e\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e,\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e\u003c/sup\u003e. Meanwhile, smaller benthic groups constitute heterotrophic, smaller, and fast-growing species of foraminifera that do not have symbiotic relationships\u003csup\u003e\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e,\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u003c/sup\u003e. Within tropical coral reef environments, both LBF and smaller benthic taxa coexist, and their respective compositions demonstrate dynamic responses to the quantity of organic material\u003csup\u003e\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e\u003c/sup\u003e, water quality\u003csup\u003e\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e\u003c/sup\u003e, and characteristics of the surrounding substrate\u003csup\u003e\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e\u003c/sup\u003e. Notably, LBF, owing to their similar environmental requirements as corals, frequently exhibit early indicators of environmental health degradation within the area\u003csup\u003e\u003cspan additionalcitationids=\"CR13\" citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e\u003c/sup\u003e. This unique trait positions LBF as valuable indicator species for assessing the ecological well-being of coral reef ecosystems\u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e,\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eSince the early 2000s, the Foraminifera-based Reef Assessment (FoRAM) index has gained global recognition as a pivotal monitoring tool for coral reefs and marginal sea areas\u003csup\u003e\u003cspan additionalcitationids=\"CR15 CR16 CR17\" citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e\u003c/sup\u003e. Its notable success in reef monitoring efforts resonates across numerous regions, notably in the Atlantic Ocean\u003csup\u003e\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e,\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e\u003c/sup\u003e, extending to locales such as Tioman Island in Malaysia\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e. Notwithstanding these achievements, several studies have highlighted the potential limitations of this index in the Indo-Pacific region, emphasising the need for species-specific calibration and refinement to ensure its applicability and accuracy.\u003c/p\u003e \u003cp\u003eThe present study aimed to document the distribution of benthic foraminifera assemblages around Pulau Redang, Malaysia, and to assess their potential as an effective tool in monitoring coral reef health.\u003c/p\u003e"},{"header":"RESULTS","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eBiotic and Abiotic components in coral reef areas\u003c/h2\u003e \u003cp\u003eThe percentage coverage of biotic and abiotic components in the coral reefs area, Pulau Redang, was reported previously\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e. multi-dimensional scaling (MDS) analysis (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e) clearly showed degradation of the coral reef located close to the development area largely affected by anthropogenic activities. This is shown by the high dead coral cover in R5 and R6\u003csup\u003e21\u003c/sup\u003e. Meanwhile, a high cover of algae and other invertebrates (mainly zoanthids \u0026ndash; data not shown) was found in R4, indicating a potential nutrient enrichment and zoanthid-dominated reef, which causes low live coral cover in the area (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e: R4).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eSediment grain size analysis indicated that all study sites were covered with coarse sandy sediment types (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The organic matter composition ranged between 2.6\u0026ndash;5.4%, with the highest concentration recorded in R6.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eThe water depth and sediment grain size composition in all six study sites around Pulau Redang.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"8\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eStation\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eWater Depth (m)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eOrganic matter\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eGravel\u0026thinsp;\u0026gt;\u0026thinsp;1 mm\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eCoarse sand 500 \u0026micro;m\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003emedium sand 250 \u0026micro;m\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003eFine sand 125 \u0026micro;m\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c8\"\u003e \u003cp\u003eMud\u0026thinsp;\u0026lt;\u0026thinsp;63\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e2.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e54.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e34.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e11.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0.0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e2.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e69.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e27.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0.0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e2.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e57.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e18.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e23.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0.0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e3.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e46.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e35.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e18.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0.0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e3.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e20.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e25.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e53.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0.0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e5.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e40.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e35.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e21.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e2.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0.3\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eForaminifera assemblage and distribution\u003c/h2\u003e \u003cp\u003eA total of 32 species of benthic foraminifera were identified in the coral reef of Pulau Redang. Among these, 22 species fell under the category of LBF. The foraminiferal assemblage was dominated by the hyaline group (92%), followed by the porcelaneous (6%) and agglutinated groups (2%) (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Overall, Amphistegenids (\u003cem\u003eAmphistegina lessonii\u003c/em\u003e, 22%, and \u003cem\u003eAmphistegina lobifera\u003c/em\u003e, 9%) and calcarinids (\u003cem\u003eCalcarina mayori\u003c/em\u003e, 19%, and \u003cem\u003eCalcarina hispida\u003c/em\u003e, 21%) co-dominated the reef foraminifera assemblage in Pulau Redang. In sites R1\u0026ndash;R5, where the water depth ranged between 5\u0026ndash;7 m, \u003cem\u003eA. lessonii\u003c/em\u003e exhibited a relative abundance of \u0026gt;\u0026thinsp;15%. In R6, with water depths between 10\u0026ndash;15 m, the most dominant LBF species was \u003cem\u003eC. hispida\u003c/em\u003e (43%). Additionally, \u003cem\u003eC. mayori\u003c/em\u003e (\u0026gt;\u0026thinsp;20% relative abundance) was more dominant on the west side of the island. The Fisher\u0026rsquo;s alpha (α) diversity index indicated that foraminifera assemblages in R1\u0026ndash;R3 were relatively more diverse (α\u0026thinsp;\u0026gt;\u0026thinsp;5) than those in R4\u0026ndash;R6 (α\u0026thinsp;=\u0026thinsp;2.77\u0026ndash;3.97). Similarly, the values of the Shannon-Wiener diversity index were higher in R1\u0026ndash;R3 (H\u0026rsquo;= 2.16\u0026ndash;2.39) compared to R4\u0026ndash;R6 (H\u0026rsquo;= 1.64\u0026ndash;2.01). The FoRAM Index (FI) calculated for all study areas was notably high (FI\u0026thinsp;=\u0026thinsp;8\u0026ndash;9). These values indicate that all areas are conducive to coral reef growth with good recoverability from future stress to the ecosystem.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eThe percentage of foraminifera species according to test types, the Foraminifera for Reef Monitoring (FoRAM) Index values, and diversity indices for all study sites around Pulau Redang.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"8\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eStation\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eCalcareous %\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePorcelaneous %\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eAgglutinated %\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eFoRAM Index (FI)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eShannon-Wienner (H\u0026rsquo;)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003ePielou\u0026rsquo;s\u003c/p\u003e \u003cp\u003eEvenness\u003c/p\u003e \u003cp\u003e(J\u0026rsquo;)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c8\"\u003e \u003cp\u003eFisher\u0026rsquo;s alpha (α)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e89\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.55\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e7.56\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e97\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.54\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e5.35\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e84\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.21\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.57\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e5.43\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e97\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e1.91\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.56\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3.59\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e90\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.01\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.58\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3.97\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eR6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e1.64\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e0.51\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e2.77\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eBased on Q-mode cluster analysis, the distribution of foraminiferal assemblages in Pulau Redang can be divided into two groups: Group A, comprising three stations on the west side of the island (R1\u0026ndash;R3), and Group B, comprising three stations on the east side of the island (R4\u0026ndash;R6) (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eThe cluster groups defined by Q-mode cluster analysis at Pulau Redang. The Anthropogenic Pressure* was based on the classification made by Lachs \u003cem\u003eet al.\u003c/em\u003e\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. The water depth, live coral cover, organic matter composition, Fisher\u0026rsquo;s alpha diversity values, and abundance data are shown as maximum and minimum values.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCluster group\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eGroup A\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eGroup B\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSamples ID\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eR1, R2, R3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eR4, R5, R6\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLocations\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eWestern Pulau Redang\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eEastern Pulau Redang\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAnthropogenic Pressure*\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLow\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eHigh\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eWater depth (m)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5\u0026ndash;7 m\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e5\u0026ndash;15 m\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLive coral cover (%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e30\u0026ndash;39%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8\u0026ndash;20%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOrganic matter (%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2.6\u0026ndash;2.8%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3.1\u0026ndash;5.4%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFisher's alpha values (α)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5.35\u0026ndash;7.56\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2.77\u0026ndash;3.97\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSymbiont-bearing group (%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e82\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e90\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHeterotrophic group (%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eStress tolerant group (%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAverage taxa\u0026thinsp;\u0026gt;\u0026thinsp;10%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cem\u003eA. lessonii\u003c/em\u003e (15\u0026ndash;34%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cem\u003eC. mayori\u003c/em\u003e (23\u0026ndash;37%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cem\u003eC. hispida\u003c/em\u003e (6\u0026ndash;32%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cem\u003eC. hispida\u003c/em\u003e (10\u0026ndash;43%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cem\u003eA. lobifera\u003c/em\u003e (5\u0026ndash;18%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cem\u003eA. lessonii\u003c/em\u003e (14\u0026ndash;24%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eCanonical correspondence analysis (CCA) was employed to determine the correlation between foraminiferal species and environmental spatial distribution. The results indicate that the composition of organic matter and substrate type (i.e., live and dead coral cover) affect the distribution of benthic foraminiferal assemblages in Pulau Redang (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The abundances of \u003cem\u003eC. mayori\u003c/em\u003e and \u003cem\u003eAmphistegina radiata\u003c/em\u003e could be correlated with higher organic matter composition, increased water depth, higher fine sand content, and algae and dead coral cover.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"DISCUSSION","content":"\u003cp\u003eOver the years, ongoing monitoring by the Reef Check Association around Pulau Redang has documented a decline in live coral cover, decreasing from over 50% in 2011 to 28% in 2019. The primary driver behind this decrease was believed to be the substantial increase in crown-of-thorns starfish (COT) observed between 2016 and 2018\u003csup\u003e22\u003c/sup\u003e. Additionally, the substantial reduction in live coral cover in 2019 was linked to the impact of Tropical Storm Pabuk, which struck early in that year\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e. However, a remarkable turnaround was observed in the reefs surrounding Pulau Redang in 2020\u003csup\u003e23\u003c/sup\u003e, possibly attributed to the restrictions imposed on tourism during the COVID-19 (SARS-CoV-2 virus) pandemic. Despite this, the reef recovery from the Pabuk event around Pulau Redang falls short, as records in 2022 show the reef condition to be \u0026lsquo;Fair\u0026rsquo; compared to \u0026lsquo;Excellent\u0026rsquo; in 2020\u003csup\u003e22\u003c/sup\u003e. In this study, three (R4\u0026ndash;R6) of the six stations belonged to the area subjected to the annual Reef Check Association monitoring. The observations by Razak \u003cem\u003eet al.\u003c/em\u003e\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e underscored the persistent \u0026lsquo;poor\u0026rsquo; coral conditions in these reef areas, pointing to a threat posed by anthropogenic activities to the reefs near coastal development\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. This region has a low live coral cover, predominantly featuring dead coral, with some sites exhibiting a considerably high algal cover, along with other invertebrates such as zoanthids\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e, \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e. Additionally, the nutrient influx from improper drainage systems may have driven the domination of macroalgae that compete with corals for space, thereby compromising the resilience of coral reef ecosystems\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e,\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e\u003c/sup\u003e. This effect is consistent with the areas with poor reef cover, such as R4, situated in areas with high anthropogenic pressure, where improper waste discharge may promote algal colonisation\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eIn reef ecosystems, benthic foraminifera offer advantages as bioindicators due to their short life spans (a few weeks to ~\u0026thinsp;2 years) and quicker response to changes in nutrient flux compared to reef-building corals with potential multi-year responses\u003csup\u003e\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e,\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e\u003c/sup\u003e. Therefore, changes in water quality, not immediately detectable in adult reef-building corals, may lead to rapid increases in populations of shorter-lived, purely heterotrophic species of benthic foraminifera, causing a reduction in the proportions of LBF\u003csup\u003e\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e\u003c/sup\u003e. Nevertheless, unlike corals, foraminifera remain resilient against coral-specific diseases, and their communities demonstrate remarkable resistance to perturbations from cyclone events or COT outbreaks\u003csup\u003e\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe Indo-Pacific region hosts over 60 LBF morphospecies, a number continually expanding with ongoing research efforts\u003csup\u003e\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e,\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e\u003c/sup\u003e. A total of 22 LBF species were successfully identified from Pulau Redang, with 11 species exhibiting a relative abundance of \u0026gt;\u0026thinsp;2%. In the Philippines, \u003cem\u003eHeterostegina depressa\u003c/em\u003e, \u003cem\u003eCalcarina mayori\u003c/em\u003e, and \u003cem\u003eAmphistegina lessonii\u003c/em\u003e are among the most widespread, particularly in the reef slope environments\u003csup\u003e\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e\u003c/sup\u003e. In Pulau Redang, A. \u003cem\u003elessonii\u003c/em\u003e (14\u0026ndash;34%) is one of the most prevalent species distributed in the reef-flat environment, followed by \u003cem\u003eCalcarina hispida\u003c/em\u003e (21%) and \u003cem\u003eC. mayori\u003c/em\u003e (19%). These findings echo research on Tioman Island, where a comparable study recorded an average relative abundance of \u003cem\u003eA. lessonii\u003c/em\u003e of 21%\u003csup\u003e28\u003c/sup\u003e. \u003cem\u003eA. lessonii\u003c/em\u003e demonstrates remarkable adaptability to water depths, reaching up to approximately 100 m\u003csup\u003e\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e\u003c/sup\u003e, and exhibits considerable abundance across various locations in the Indo-Pacific region\u003csup\u003e\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e,\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e\u003c/sup\u003e. The most prevalent calcarinids in Pulau Redang are \u003cem\u003eC. hispida\u003c/em\u003e (6\u0026ndash;43%) and \u003cem\u003eC. mayori\u003c/em\u003e (2\u0026ndash;37%). Both species have been reported to have different habitat preferences in the Spermonde Archipelago. \u003cem\u003eC. hispida\u003c/em\u003e thrives in reef-flat areas with water depths ranging between 1\u0026ndash;6 m, while \u003cem\u003eC. mayori\u003c/em\u003e is typically found in reef slope areas with depths reaching up to 24 m\u003csup\u003e\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e\u003c/sup\u003e. In this study, both species were observed in reef-flat areas along the east and west coasts of Pulau Redang.\u003c/p\u003e \u003cp\u003eThe CCA results revealed a substantial influence of substrate type and organic matter composition on the distribution of benthic foraminifera in the reef environments of Pulau Redang. The influence of substrate type on the local distribution of benthic foraminifera in reef environments is a significant yet complex environmental factor\u003csup\u003e\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e,\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e,\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e\u003c/sup\u003e. Within Pulau Redang, the Q-mode cluster analysis classified the foraminiferal assemblages into two groups (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). Group A represented samples collected from the western coast of Pulau Redang. Here (R1\u0026ndash;R3), the coral reef ecosystems received minimal anthropogenic pressure and were classified as pristine sites\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. With more than 30% live coral and low algal cover, the foraminiferal assemblage was characterised by a high abundance of amphisteginids (\u0026gt;\u0026thinsp;40%) and dominated by \u003cem\u003eA. lessonii\u003c/em\u003e (26%), \u003cem\u003eC. hispida\u003c/em\u003e (19%), and \u003cem\u003eA. lobifera\u003c/em\u003e (10%). Here, foraminiferal assemblages exhibited higher diversity (α\u0026thinsp;\u0026gt;\u0026thinsp;5) compared to Group B. In contrast, Group B included areas facing high anthropogenic pressure, mainly from tourism, sewage nutrient enrichment, and coastal development\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e,\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e\u003c/sup\u003e. The area along Pasir Panjang (R4\u0026ndash;R5) exhibits relatively high dead coral cover, with coral rubble dominating the substrate. The foraminiferal assemblage here is dominated by calcarinids, with an average relative abundance of \u0026gt;\u0026thinsp;50%. The presence of dead coral rubble and an alga-dominated environment is conducive to the high abundance of \u003cem\u003eCalcarina mayori\u003c/em\u003e (37%), particularly in R4. Interestingly, \u003cem\u003eCalcarina mayori\u003c/em\u003e in Pulau Redang showed increased abundance in areas with higher algal cover. These observations are consistent with those of studies on the Indo-Pacific reef, associating calcarinids with the presence of algae and seagrass communities in areas characterised by coarse sandy substrates\u003csup\u003e\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e,\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eOverall, the FI indicated high values (FI\u0026thinsp;=\u0026thinsp;8\u0026ndash;9) across all reef sites and areas within Pulau Redang despite notable variations in observed coral reef conditions. Notably, both the western and eastern coral reef areas of Pulau Redang exhibited a remarkably high prevalence of symbiont-bearing species, exceeding 80% in relative abundance.\u003c/p\u003e \u003cp\u003eIt is worth noting that high FI values suggest strong potential for reef recovery within the Pulau Redang reef area, even in R4-R6, where \u0026ldquo;poor\u0026rdquo; coral conditions have been observed\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e. The FI has proven its effectiveness as a reliable proxy for assessing reef conditions, particularly in the western Atlantic and Caribbean regions\u003csup\u003e\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u003c/sup\u003e. Notably, this index exhibits a strong correlation with the water quality in the Great Barrier Reef of the Pacific Ocean\u003csup\u003e\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e,\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e\u003c/sup\u003e. The application of the FI to Tioman Island accurately reflects the true state of the local reef environment\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eHowever, despite the strong resemblance between FI values and reef recovery records, previous studies have highlighted that the persistence of high FI values in mesotrophic reefs is often attributed to dense populations of calcarinids, a symbiont-bearing group\u003csup\u003e\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e,\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e\u003c/sup\u003e. In our investigation of Pulau Redang, on average, calcarinids constituted approximately 34% of the relative abundance within Group A (R1\u0026ndash;R3), an area characterised by minimal anthropogenic influence. In contrast, within the mesotrophic reef zone of Group B (R4\u0026ndash;R6), calcarinids represented an average of 55% of the total foraminiferal assemblages. This is attributed to the epiphytic proliferation of certain Calcarinidae family species on a range of macrophytic algae. Interestingly, the high algal coverage (8%) in R4 correlated well with the increase in calcarinids (relative abundance of 58%).\u003c/p\u003e \u003cp\u003eStudies indicate that in highly stressed reef environments with available sunlight, calcarinid densities tend to rise with increased algal cover\u003csup\u003e\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e,\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e\u003c/sup\u003e. Therefore, suggestions for calibrating the FI for the Indo-west Pacific region, where Calcarinidae occur\u003csup\u003e\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u003c/sup\u003e, are particularly relevant, especially where algal cover visually surpasses coral cover. The dataset from Pulau Redang primarily focused on sediment quality and coral cover. However, due to the unavailability of water quality records, we were unable to establish a direct correlation between the FI and water quality near the reef. Nevertheless, our observations revealed an increase in calcarinid prevalence within areas of Pulau Redang dominated by algae. This phenomenon persisted despite suboptimal coral conditions and relatively low live coral cover. Intriguingly, the FI consistently indicated high FI values, suggesting favourable conditions for coral recovery. Hence, we believe that a tailored calibration of the FI is imperative, especially within mesotrophic reefs where calcarinids dominate.\u003c/p\u003e \u003cp\u003eCoral reefs worldwide face threats from natural and anthropogenic factors, emphasising the urgent need for preservation amid global warming. Our observations in Pulau Redang revealed vulnerable reefs near coastal development, which remain at risk from human activities. Recent tropical storms have dramatically altered the structural landscape of these reefs, resulting in extensive damage, particularly to the shallow-water branching and tabulating coral species. The storm's aftermath appears to be a contributing factor to the poor coral conditions, particularly on the eastern side of the island.\u003c/p\u003e \u003cp\u003eForaminifera are effective monitoring tools for assessing coral reef health. The FI, designed as a straightforward indicator, assesses whether water quality supports calcifying organisms that host algal endosymbionts, reflecting the potential for reef recovery. In Pulau Redang, the foraminiferal species distribution conformed to the typical assemblage of tropical reefs, with symbiont-bearing taxa dominating the community. Surprisingly, the FI consistently recorded high values throughout the study area despite notable variations in observed coral reef conditions.\u003c/p\u003e \u003cp\u003eWhile the FI has been successfully applied to Tioman Island, its application to Pulau Redang presents different challenges. We believe that a customised calibration of the FI is imperative, especially in mesotrophic reefs where calcarinids dominate foraminiferal assemblages. Such calibration is essential for enhancing the accuracy and reliability of the index as a valuable tool for monitoring and assessing coral reef health in the region.\u003c/p\u003e"},{"header":"METHODS","content":"\u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eStudy area\u003c/h2\u003e \u003cp\u003eThis study was conducted in Pulau Redang (5\u0026deg;46'38.30\"N, 103\u0026deg; 0'40.06\"E), a gazetted marine park. The island is situated in Terengganu waters along the shallow, tropical shelf on the east coast of Peninsular Malaysia (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). The primary economic activities of the island's inhabitants are closely tied to tourism. The central region of Pulau Redang is intensively developed with a small airport, hotels, resorts, and residential areas (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). Another extensively developed area is along the sandy beaches, which are situated on the east coast of the island (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003ePulau Redang experiences two monsoonal systems: the northeast (October-March) and the southwest monsoon (April-August)\u003csup\u003e\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e\u003c/sup\u003e. The sea conditions along the east coast of Peninsular Malaysia are relatively calmer during the southwest monsoon (dry season) compared to the period during the northeast monsoon (wet season), which brings heavy rain and strong winds\u003csup\u003e\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e\u003c/sup\u003e. Depending on the season, the near-bottom temperature recorded in the study area ranged between 26\u0026ndash;30\u0026deg;C\u003csup\u003e\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e\u003c/sup\u003e. Additionally, more frequent intense tropical storm events during the northeast season have been observed along the east coast of Peninsular Malaysia in recent years\u003csup\u003e\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe magnificent coral reef area has contributed to Pulau Redang's flourishing as a tourist destination. Based on a dataset by Akmal et al.\u003csup\u003e\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e\u003c/sup\u003e and a report by Reef Check Malaysia in 2020\u003csup\u003e43\u003c/sup\u003e, coral reefs in the marine parks can be categorised from \u0026lsquo;poor\u0026rsquo; to \u0026lsquo;good\u0026rsquo; coral condition following the criteria of coral health status by Chou et al.\u003csup\u003e\u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e44\u003c/span\u003e\u003c/sup\u003e. As indicated by Akmal \u003cem\u003eet al.\u003c/em\u003e\u003csup\u003e\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e\u003c/sup\u003e, less affected reef zones by coastal development and human activities have established good coral conditions and higher coral genera diversity. This was further proven by Lachs et al.\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e, which highlighted the effect of tourism development in some parts of the island that caused \u0026lsquo;poor\u0026rsquo; reef conditions. Apart from that, coral reefs in Pulau Redang also experienced coral bleaching in 2010, as reported by Tan and Heron\u003csup\u003e\u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e45\u003c/span\u003e\u003c/sup\u003e, showing that natural disturbances also affect the health status of the reef.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eIn-situ data and sediment collections\u003c/h2\u003e \u003cp\u003eCoral reef assessment was carried out using standard protocol video sampling in July 2022\u003csup\u003e46\u003c/sup\u003e. Method for Coral Video Transect (CVT) has been published in Razak \u003cem\u003eet al.\u003c/em\u003e\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eAs for foraminifera and the sediment collections, two sediment samples were collected along each transect. The sediments were collected by the diver by scooping the surface sediment into plastic bags and centrifuge tubes. The permission for sample collection in this study has been approved by the Department of Fisheries Malaysia. For foraminifera analysis, approximately 30 cm\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e of sediment was placed into the centrifuge tube. On board, the sediments were fixed with buffered ethanol (\u0026gt;\u0026thinsp;90%)\u003csup\u003e12,47\u003c/sup\u003e. All sediment samples were brought back to the laboratory for analysis.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eForaminifera analysis\u003c/h2\u003e \u003cp\u003eIn the laboratory, the preserved samples underwent a gentle washing process under running tap water, using a 63 \u0026micro;m sieve to eliminate extraneous silt and clay\u003csup\u003e\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e\u003c/sup\u003e. The resulting residues were carefully transferred into a pre-labelled weighing boat. The samples were then dried in an oven at a temperature range of 40\u0026ndash;50\u0026deg;C for 24 h\u003csup\u003e\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e\u003c/sup\u003e. After drying, the samples were divided into manageable aliquots, and approximately 300 foraminiferal specimens were handpicked at random from each sample using a fine brush (000) with the aid of a 40\u0026times; light microscope\u003csup\u003e\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e\u003c/sup\u003e. The specimens were then sorted and mounted on a micropalaeontological slide coated with non-toxic, water-soluble glue to ensure immobility\u003csup\u003e\u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e49\u003c/span\u003e\u003c/sup\u003e. Benthic foraminifera were identified based on the criteria established by Loeblich and Tappan\u003csup\u003e\u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e\u003c/sup\u003e, as well as insights from regional literature sources\u003csup\u003e\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e,\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e,\u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e51\u003c/span\u003e,\u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e52\u003c/span\u003e\u003c/sup\u003e. To avoid reworking the specimens during the picking process, foraminiferal tests displaying any discoloration, breakage, or poor preservation\u003csup\u003e\u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e53\u003c/span\u003e\u003c/sup\u003e were excluded.\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eSediment and organic matter analysis\u003c/h3\u003e\n\u003cp\u003eIn this study, dry sieving methods\u003csup\u003e\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e\u003c/sup\u003e were used to determine the sediment grain size. For sediment grain size analysis, all samples underwent pretreatment with HCl (10%) to dissolve chunky carbonate fragments. Next, the samples were rinsed and oven-dried at 50\u0026deg;C for 36 h. Once dried, approximately 100 g samples were sieved using a set of sieves with sizes 4000, 2000, 1000, 500, 250, 125, and 63 \u0026micro;m, and the percentage of each sediment size fraction was determined. The organic matter content of the sediments was assessed using the loss on ignition (LOI) method\u003csup\u003e\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e,\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e. Prior to heating, 5 g of each sediment sample was weighed. The samples were combusted at 550\u0026deg;C for 4 h and then left to cool to room temperature (30\u0026deg;C) before the final weight was recorded. The percentage of organic matter was calculated using the formula described previously\u003csup\u003e\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cdiv id=\"Sec12\" class=\"Section3\"\u003e \u003ch2\u003eCoral data analysis\u003c/h2\u003e \u003cp\u003eThe coral cover around Pulau Redang was reported by Razak et al.\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e as a percentage cover. The percentage cover includes live coral (C), algae (ALG), other invertebrates (OT), dead coral (DC), and sand, silt, or rock (SR). A MDS analysis was performed in this study to understand the correlation between coral cover distribution and anthropogenic pressures (developed and non-developed areas).\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003eForaminiferal data analysis\u003c/h2\u003e \u003cp\u003eTo avoid reworked specimens, only foraminiferal species with a relative abundance greater than 2% were retained for subsequent statistical analysis. For comparison with A\u0026rsquo;ziz et al.\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e, we calculated diversity indices such as Fisher\u0026rsquo;s alpha diversity index (α), Shannon-Wiener species diversity (H\u0026prime;), and species evenness of Pielou (J\u0026prime;) using PAST (Palaeontological STatistics) software version 3. Relative abundance data were derived from the mean average of foraminiferal species across replicates. Q-mode cluster analysis, based on the Euclidean distance similarity measure, was used to identify the similarity of fauna assemblages between the study sites\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e,\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e\u003c/sup\u003e. CCA was used to test the correlation between sediment characteristics, organic matter content, coral reef cover, and foraminiferal assemblages. To evaluate the applicability of the FI in Pulau Redang, the identified foraminiferal species were classified into three functional groups, following the classifications of Hallock et al.\u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u003c/sup\u003e and Carnahan \u003cem\u003eet al.\u003c/em\u003e\u003csup\u003e\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e\u003c/sup\u003e (Supplementary 1). The FI was calculated for each site using the equation proposed by Hallock et al.\u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eACKNOWLEDGEMENTS\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis study is funded by the Fundamental Research Grant Scheme (FRGS /1/2022/WAB07/UMT/02/1).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAUTHOR CONTRIBUTIONS\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eFatin I. Minhat: Contributed to conceptualization, investigation, writing and major revision of the manuscript, Supervision, and funding acquisition. Che Din Mohd Safuan: Contributed to conceptualization, methodology on coral analysis, writing – review, and editing. Sabrina A. M. Emran: performed foraminifera analysis, statistical analysis, and the original writing of the manuscript. Aida F. M. Hasnizul: performed foraminifera analysis, sediment and organic matter analysis, and original writing of the manuscript. Aminudin Muhammad Afiq-Firdaus: performed field sample collections, data analysis, and statistical analysis on coral cover and distributions. Zainudin Bachok: contributed to conceptualization, review, and editing of the manuscript. Wan I. A.W. Talaat: contributed to the conceptualization, review, and editing of the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eDATA AVAILABILITY STATEMENT\u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll data generated or analysed during this study are included in this article (and its Supplementary Information files)\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCOMPETING INTERESTS STATEMENT\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no competing interests.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003eHughes, T. P. \u003cem\u003eet al.\u003c/em\u003e Global warming and recurrent mass bleaching of corals. \u003cem\u003eNature\u003c/em\u003e \u003cstrong\u003e543\u003c/strong\u003e, 373\u0026ndash;377 (2017). 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(DOI 10.2113/gsjfr.42.4.305)\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-3784490/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3784490/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eTo mitigate the adverse effects of ocean warming on coral reef degradation, resource managers increasingly explore the management and regulation of local stressors to bolster coral resilience and recovery. Comprehensive assessments and monitoring efforts offer a holistic understanding of reef dynamic ecosystems. Using the Foraminifera-based Reef Assessment (FoRAM) index, we documented the distribution of benthic foraminiferal assemblages surrounding Pulau Redang, Malaysia, and assessed their potential for monitoring coral reef health. Undeveloped (R1\u0026ndash;R3) and developed (R4\u0026ndash;R6) reef sites revealed distinct differences in reef conditions. The significant presence of dead corals in R4\u0026ndash;R6 is linked to Tropical Storm Pabuk. Foraminiferal distribution showed \u003cem\u003eAmphistegina lessonii\u003c/em\u003e (14\u0026ndash;34%) as the dominant species, followed by \u003cem\u003eCalcarina hispida\u003c/em\u003e (21%) and \u003cem\u003eCalcarina mayori\u003c/em\u003e (19%). Surprisingly, FoRAM consistently yielded high values across the study area despite varying coral reef conditions, probably due to the prevalence of \u003cem\u003eCalcarina mayori\u003c/em\u003e in mesotrophic reefs (R4, R5, and R6), potentially skewing FoRAM values and providing a misleading indicator of reef conditions. We recommend calibrating the FoRAM Index, particularly in mesotrophic reefs where calcarinids dominate foraminiferal assemblages, to enhance its precision and reliability for coral reef health monitoring and assessment within the region.\u003c/p\u003e","manuscriptTitle":"Foraminifera assemblages in Pulau Redang: Uncovering Discrepancies and the Importance of FoRAM Index Calibration for Precise Reef Monitoring","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-01 06:17:07","doi":"10.21203/rs.3.rs-3784490/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"7e81e5ae-f51c-4d62-9268-5e1b4fc34669","owner":[],"postedDate":"January 1st, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":27880971,"name":"Earth and environmental sciences/Ecology"},{"id":27880972,"name":"Earth and environmental sciences/Environmental sciences/Environmental impact"},{"id":27880973,"name":"Earth and environmental sciences/Ocean sciences/Marine biology"}],"tags":[],"updatedAt":"2024-04-15T04:46:21+00:00","versionOfRecord":[],"versionCreatedAt":"2024-01-01 06:17:07","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3784490","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3784490","identity":"rs-3784490","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}