Middle-East Journal of Scientific Research 24 (6): 2145-2151, 2016 ISSN 1990-9233 © IDOSI Publications, 2016 DOI: 10.5829/idosi.mejsr.2016.24.06.23657

Ecology of Bivalves in the Area of Setiu Wetlands, ,

11Nurulafifah Yahya, Nurul Zalizahana Zakaria, 1 Zakirah Mohd Taufeq, 12Noor Shahida Rosli and Zainudin Bachok

1Institute of Oceanography and Environment (INOS), Universiti Malaysia Terengganu, 21030, Kuala Terengganu, Malaysia 2School of Marine and Environmental Sciences, Universiti Malaysia Terengganu, 21030, Kuala Terengganu, Malaysia

Abstract: Study on ecology of bivalves in the lagoon area of Setiu Wetlands, Terengganu, South China was conducted on two months interval for a year (July, September, November 2011 and January, March, May 2012). Bivalve samples and environmental parameters (in situ parameters and sediments) were collected from 11 stations within 50 m transect line along the lagoon. A total of 10, 845 individual of bivalves were collected and classified into 11 families, 21 genera and 34 species with mean total density of 33±17 individuals/m2 . There was no significant temporal changes in abundance of bivalves and environmental parameter (p>0.05). The density of bivalves, in situ parameters (salinity and pH) and sediment analysis (total organic matter and sediment size) had significant difference among stations (p<0.05). However, density of bivalves had no significant relationship with all environmental parameters studied (p>0.05). Density of bivalves was higher in the brackish subtidal area compared to freshwater subtidal and intertidal area. The abundance of bivalve’s species in the lagoon area of Setiu Wetlands is relatively high to the area covered. Salinity was the only parameter that strongly correlated with the diversity of bivalves in the lagoon area of Setiu Wetlands.

Key words: Bivalve Distribution Environmental parameter Setiu Wetlands South China Sea

INTRODUCTION habitats that are part of the most productive ecosystems in the world which are mangrove forest Bivalves are molluscs consisted of two calcified and beds that served high biodiversity of flora valves joined by elastic ligament. Bivalves can be found and fauna [10]. Setiu Wetlands had divided into nine worldwide in marine, brackish and freshwater areas. inter-connected ecosystems which are the sea, beach, The distribution patterns of bivalves are significantly , lagoon, , islands, , mangrove forest correlated with physical environmental parameters such and coastal forest from Kg. Penarik to Kg. Beting Lintang as temperature, salinity, food availability, sediment [11]. composition, current pattern and organic matter [1, 2, 3, 4]. Despite being exploited by local communities in Setiu Bivalves are important as indicators for aquatic Wetlands, lack of studies had been done on the environment, substrate stabiliser, decreasing erosion distribution of bivalves in the lagoon area of Setiu and create beneficial habitat complexity [5, 6, 7]. South Wetlands which the data collected will be crucial for China Sea waters recorded about 802 species of molluscs biodiversity conservation and sustainable management [8]. In Malaysia, there were 37 families with 206 species of purposes. The various ecosystems provide high diversity bivalves have been recorded [9]. of flora and fauna, hence, created the need to study the Setiu Wetlands is located at the Northeast of abundance and diversity of bivalves at Setiu Wetlands. Peninsular Malaysia in the state of Terengganu and Therefore, this study was done to determine the ecology has been listed as one of the most important of bivalve in the lagoon area of Setiu Wetlands, wetlands in Malaysia since it consists of a few Terengganu.

Corresponding Author: Zainudin Bachok, School of Marine and Environmental Sciences, Universiti Malaysia Terengganu, 21030, Kuala Terengganu, Malaysia. Tel: +6096683211. 2145 Middle-East J. Sci. Res., 24 (6): 2145-2151, 2016

Fig. 1: Study area of sample collection in the lagoon area of Setiu Wetlands, Terengganu

MATERIALS AND METHODS parameters recorded include salinity (psu), temperature (°C), dissolved oxygen (mg/L) and pH. Sediment samples Study Area: Setiu Wetlands covered about 14 km of for grain size analysis and total organic matter (TOM) shallow, elongated stretch of water body and dune analysis were collected using scoop or Ponar Grab Wildco system that with parallel to rise ridges of Setiu lagoon Instruments. Samples for grain size analysis were placed from Kg. Beting Lintang to Kg. Penarik. The lagoon is in plastic bags whereas sediment samples TOM analysis located along the coast facing the South China Sea and were put in aluminium foil and stored in the ice-chest. received water discharged from Setiu River. 11 stations The samples were brought back to the INOS laboratory were selected which were divided into brackish subtidal for further analysis. TOM was analysed using loss-on- (St. 1, St. 2, St. 3, St. 4, St. 5 and St. 7), freshwater subtidal ignition (LOI) method was [23]. Grain size analysis was (St. 9, St. 10 and St. 11) and mangrove intertidal (St. 6 and analysed by wet-sieved [24] and dry-sieved method St. 8) (Fig. 1). [25, 26, 27].

Samples Collection and Preparation: The sampling was Data Analysis: The abundance of bivalves was express in conducted on two months interval for a year which was in density as a total number of individual(s) per meter square July, September, November 2011 and January, March, (no. of individuals/m2 ). The diversity of bivalve May 2012. A 50 m transect had been set up at each communities was described by the diversity index of sampling station which was then divided into four points Shannon-Weiner, H’ [28], whereas the evenness of a (10 m distance from each point) perpendicular to the bivalve community was represented by Pielou's evenness coastline [12, 13]. Bivalve samples were handpicked in the index, J’ [29]. For the multivariate analysis, the data were area of 0.25 m2 quadrate to the depth of 0.2 m [14, 15]. analysed using PRIMER. The density data from each The number of individuals was counted before they were station were entered into a new MS EXCEL format and preserved in 70 % ethanol [16]. The identification was were input into the PRIMER 6 V 6.1.6 programmer [30] for based on the shell morphology by looking at the shape, subsequent data analysis. A multivariate technique was colour, size, thickness and design on the shells [17] and performed on the data matrix. The species composition also through the comparison with the bivalves illustrated and abundance matrix were based on hierarchical, in references [18, 19, 20, 21, 22]. The samples were agglomerative classification employing group averaging deposited at the South China Sea Repository and sorting on the Bray-Curtis similarity coefficient Reference Centre of INOS. implemented in PRIMER [31, 32]. The cluster analysis of The in situ parameters at each station were recorded abundance of organisms is displayed in the form of a using Hydrolab Quanta (Multiprob System). The dendrogram.

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For sediment data, the relative importance of gravel, Community Structure and Similarities: Species number, sand (very coarse sand, coarse sand, moderately coarse diversity and evenness of bivalves had no significant sand, fine sand and very fine sand) and silt and clay difference among stations (p>0.05). The highest species fractions were expressed in percentages of dry weight. number and diversity were concentrated at the brackish The grain size distribution of sediments was analyzed for subtidal area, whereas the lowest species number and median, sorting and skewness according to graphical diversity were concentrated at the freshwater subtidal measures [33]. area (Fig. 3a, Fig. 3b). The lowest diversity was mostly All the results obtained was analysed using one-way occurred in brackish subtidal (St. 2) and freshwater analysis of variance (ANOVA) to determine whether there subtidal (St. 9, St. 10 and St. 11). was any significant difference between the mean of Four clusters were examined in this study that clearly biological parameters and environmental parameter among showed that the sampling sites were divided into their stations. If the ANOVA showed significant differences, a similar ecosystems. However, the percentage of the post hoc test of Least Significant Difference (LSD) was similarity was quite low. St. 10 and St. 11 located at the conducted for a pair wise comparison. The correlation and freshwater subtidal areas were group together at 2 % regression were done between density, diversity and similarity. At 16 % similarity, St. 4, St. 5 and St. 7 which evenness with in situ parameters (salinity, pH, DO and were located at brackish subtidal areas and also St. 9 temperature), sediment characteristics and TOM using which was located at the freshwater subtidal can be MS EXCEL. grouped together in similar cluster. St. 1, St. 2 and St. 3 can be grouped together at 20 % similarity with all of the RESULTS stations were located in the brackish subtidal areas. St. 6 and St. 8 were grouped together at 32 % in which both Bivalves Composition: A total of 10, 845 individuals of stations were located in the mangrove intertidal areas. bivalve were collected along the study with mean density of 33±17 individuals/m2 . There were 11 families in the Environmental Parameters: Fig. 5a showed physical lagoon area of Setiu Wetlands, Terengganu (Fig. 2a) parameters recorded in the lagoon area of Setiu Wetlands, which consisted of 21 genera and 34 species. The Terengganu. Salinity and pH had significant difference distribution of bivalves had significant difference among throughout sampling (p<0.05). The water temperature and stations in the lagoon area of Setiu Wetlands (p<0.05). DO had no significant difference throughout the stations Mean density of bivalves at St. 1 (261±154 individuals/m2 ) (p>0.05). St. 8 had the highest percentage of TOM and was significantly higher (p<0.05) compared to other this might be due to the location of the station, which is stations (Fig. 2b). in the mangrove forest area (Fig. 5b).

Fig. 2: Bivalves composition a) percentage abundance of bivalves family and b) density of bivalves in the lagoon area of Setiu Wetlands, Terengganu

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Fig. 3: Community structure of bivalves a) species number and b) diversity and evenness index in the lagoon area of Setiu Wetlands, Terengganu

Fig. 4: Similarity of bivalves in the lagoon area of Setiu Wetlands, Terengganu

Fig. 5: Environmental parameters recorded a) in situ parameters and b) total organic matter (%) in the lagoon area of Setiu Wetlands, Terengganu (n = 6, mean±SD)

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Table 1: Percentage of sediment textures and grain size distribution at each station in the lagoon area of Setiu Wetlands, Terengganu (n = 6; mean±SD) Area Station Granule (%) Sand (%) Silt + Clay (%) Mean (phi) Sorting (phi) Skewness (phi) Brackish subtidal St. 1 0.01±0.02 97.44±1.02 2.55±1.03 1.47±0.04 0.97±0.07 -0.17±0.22 Brackish subtidal St. 2 0.01±0.01 91.71±3.46 8.36±3.41 1.96±0.13 0.93±0.09 -0.29±0.10 Brackish subtidal St. 3 0.00±0.01 96.32±2.04 3.68±2.04 1.63±0.09 0.87±0.05 -0.03±0.24 Brackish subtidal St. 4 0.01±0.01 97.61±1.33 2.38±1.33 1.44±0.06 0.95±0.05 -0.20±0.11 Brackish subtidal St. 5 0.22±0.18 82.78±6.84 17.00±6.81 1.83±0.36 1.26±0.08 -0.43±0.30 Mangrove intertidal St. 6 0.43±0.28 90.68±2.39 8.90±2.20 1.33±0.36 1.19±0.10 -0.07±0.18 Brackish subtidal St. 7 0.26±0.21 98.23±1.67 1.51±1.60 1.17±0.22 0.99±0.02 -0.31±0.04 Mangrove intertidal St. 8 0.31±0.31 87.33±3.96 12.36±3.99 1.38±0.32 1.51±0.37 0.06±0.14 Freshwater subtidal St. 9 0.01±0.02 89.94±3.55 10.06±3.56 1.82±0.18 1.03±0.08 -0.12±0.19 Freshwater subtidal St. 10 0.48±0.70 98.27±2.24 1.26±1.64 1.00±0.13 0.97±0.07 -0.11±0.09 Freshwater subtidal St. 11 0.41±0.64 90.29±6.99 9.36±7.34 1.39±0.52 0.96±0.11 -0.13±0.24

Table 1 showed percentage of sediment textures and on bivalves taxonomist in Malaysia and limited studies distribution at each station in the lagoon area of Setiu was conducted at the east coast of Peninsular Malaysia. Wetlands. Sediment textures (%) were divided into three The diverse ecosystems in Malaysia are still not well types which were granule, sand and silt and clay with the studied and explored by researchers. Furthermore, some sizes of 2.0-4.0 mm, 63 µm-2.0 mm and <63 µm respectively. studies that had been done in Malaysia are not well The sediment textures had significant difference among documented or published making it difficult for the people stations (p<0.05). The distribution of the grain size in the to know the actual number of bivalve species recorded in sampling areas was affected by the current velocity. The Malaysian waters. freshwater subtidal area faced high velocity of water The highest diversity of bivalves in the brackish inflow from Setiu River and Chalok River that might have subtidal area occurred at seagrass and estuary transported the fine sand and deposited the heavier sand. ecosystems bordered by mangrove forest which are Since Setiu Wetland consisted of a few small islands, so highly productive ecosystems. St. 2 had less diversity this can be a factor can reduce the water current, hence that might be due to the unfavourable conditions as a affected the sediment deposition. habitat for bivalves. The freshwater subtidal had low diversity probably because of the velocity of river flow. DISCUSSION The highest and the lowest evenness of bivalves were at the freshwater subtidal area. Biodiversity of Bivalves: Mean density of bivalves at St. 1 was significantly higher (p<0.05) compared to other Bivalves–Environmental Parameters Relationship: stations (Fig. 2b) because of the presence of Environmental parameters such as salinity, temperature, Potamocorbula fasciata as this species has the ability to pH, dissolved oxygen and sediment distribution were tolerate environmental changes such as fluctuations in factors that affected the distribution of bivalves [4, 34]. salinity and anoxia [20] that reflected the abundance up However, only salinity had significant correlation with to thousands per m2 . This species contributed 77 % diversity and evenness of bivalves (p<0.01). Generally, from the total abundance of bivalves collected in the areas that had high salinity had high density and high lagoon area of Setiu Wetlands. This species was not diversity index, but had low evenness index. However, St. listed in the previous studies in Malaysia. St. 10 and St. 11 1 and St. 2 that had high salinity had low diversity and (<1 individuals/m2 ) that were located in the freshwater evenness index. This might be due to the biology of the subtidal area had the lowest density of bivalves might be bivalve species there that were present in high abundance due to the high current velocity as the stations were and dominated the areas. The abundance of bivalve influenced by the river flow from Chalok River and Setiu species increased with salinity [34]. Even though a study River. The high current velocity might affect the bivalves’ by [35] stressed that the density of bivalves increased larvae settlement as they might be washed away. with increasing sand, silt and organic matter of the Out of 34 species collected in this study, only 9 sediment, but in this study, all the sediment textures and species were similar with 206 species of bivalves listed in organic matter had low correlation with the density, Malaysia [9] while the other 24 species were not listed in diversity and evenness of bivalves. The diversity and the recent collection. This might be due to less expertise abundance of bivalves were controlled by sediment type

2149 Middle-East J. Sci. Res., 24 (6): 2145-2151, 2016 and organic matter [36, 37]. However, in this study, the 6. Kreeger, D., J. Adkins, P. Cole, R. Najjar, D. Velinsky, relationships were not clearly shown. This might be due P. Conolly and J. Kraeuter, 2010. Climate Change and to fact that the bivalve species in the Setiu Wetlands were the Delaware Estuary: Three Case Studies in well distributed into different types of sediment and level Vulnerability Assessment and Adaptation Planning. of TOM. Partnership for the Delaware Estuary, PDE, 10(01): 1-117. CONCLUSION 7. Dewiyanti, I. and S. Karina, 2012. Diversity of gastropods and bivalves in mangrove ecosystem The density and diversity of bivalves were higher in rehabilitation areas in Aceh Besar and Banda Aceh the brackish subtidal area compared to freshwater subtidal districts, Indonesia. , Aquarium, and mangrove intertidal area. The mean density of Conservation & Legislation, International Journal of bivalves was significantly higher at St. 1 since the station the Bioflux Society, 5(2): 55-59. was dominated by Potamocorbula fasciata, a species 8. Liu, J.Y., 2013. Status of Marine Biodiversity of the with high environment toleration. However, high diversity China . PLoS ONE, 8(1): 1-24. of bivalves was recorded at the stations that had diverse 9. Wong, N.L.W.S. and A. Arshad, 2011. A brief review ecosystems, such as mangrove forest and seagrass bed. of marine shelled mollusca (gastropod and ) Only salinity had strong correlation with diversity record in Malaysia. Journal of Fisheries and Aquatic whereas other parameters had low correlations. The Science, 6(7): 669-699. species of bivalve collected in the lagoon area of Setiu 10. Salam, M.N.A., 1997. Coastal and estuarine land use Wetland were about 15 % from the number of bivalve management around some major river systems in species recorded in Malaysia. Despite relatively small area Peninsular Malaysia. Case study III: Sg. Setiu, that was covered during sampling activities, the lagoon of Terengganu. Project MYS 304/94. WWF Malaysia, Setiu Wetlands could be categorised as high biodiversity Petaling Jaya: 8-21. of bivalve’s species in the east coast of Peninsular 11. Nakisah, M.A. and A.H. Fauziah, 2003. Setiu Malaysia. Wetland: Tranquility Amidst Plenty, 1st Edition. Kolej Universiti Sains dan Teknologi Malaysia REFERENCES (KUSTEM). 12. Ashton, E.C., D.J. Macintosh and P.J. Hogarth, 2003. 1. Sreeramamoorthy, R. and D.V. Rama Sarma, 1986. A baseline study of the diversity and community Distribution and abundance of benthic macrofauna in ecology of crab and molluscan macrofauna in the the Gosthani and Champavathi River of Sematan mangrove forest, Sarawak, Malaysia. Andhra Pradesh, India. In Biology of Benthic Marine Journal of Tropical Ecology, 19: 127-142. Organisms: Techniques and Methods as Applied to 13. Delgado, J.G., Y.M. Reverol, A.R. Godoy and the Indian Ocean. Balkema / Rotterdam AA (1987) Indian Edition Series 12, India. H.J. Severeyn, 2006. Distribution and seasonal 2. Gosling, E., 2003. Bivalve molluscs: biology, ecology variation of intertidal bivalves on a sandy beach at and culture. Fishing New Books, a division of Caimare Chico, Venezuela. Boletín Del Centro De Blackwell Publishing, UK. Investigaciones Biológicas, 40(3): 257-27. 3. Cardoso, J.F.M.F., J.I. Witte and H.W. Van Der Veer, 14. Urban, H.J. and B. Campos, 1994. Population 2009. Differential reproductive strategies of two dynamics of the bivalves Garisolida, Semele bivalves in the Dutch Wadden Sea. Estuarine, solida and Protothaca thaca from a small bay in Coastal and Shelf Science, 84: 37-44. Chile at 36°S*. Marine Ecology Progress Series, 4. Dame, R.F., 2012. Ecology of marine bivalves: An 115: 93-102. ecosystem approach, 2nd edition, pp: 11-78. CRC 15. Sasekumar, A. and V.C. Chong, 1998. Faunal Press Taylor & Francis Group. diversity in Malaysian . Global Ecology 5. Yusof, A.M., N.F. Yanta and A.K.H. Wood, 2004. and Biogeograph Letters, 7: 57-60. The used of bivalves as bio-indicator in the 16. Sturm, C.F., T.A. Pearce and A. Valdes, 2006. The assessment of marine pollution along a coastal area. mollusks: A guide to their study collection and Journal of Radio analytical and Nuclear Chemistry, preservation. American Malacological Society, 259(1): 119-127. pp: 344-345.

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