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GASTROPOD AND BIVALVE MOLLUSCS ASSOCIATED WITH THE SEAGRASS BED AT MERAMBONG SHOAL, JOHOR STRAITS,

Gastropod and Bivalve Molluscs Associated with the Seagrass Bed at Merambong Shoal, Johor Straits, Malaysia

Zaidi Che Cob1, Aziz Arshad2, Wan-Lotfi Wan Muda1 & Mazlan Abd. Ghaffar1

1 Marine Ecosystem Research Center (EKOMAR), School of Environmental and Natural Resource Science, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 Bangi, Selangor, Malaysia 2Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia

ABSTRACT

Seagrass beds are important marine ecosystems that have high productivity and support a large number of marine . Surveys on mollusc fauna were conducted from November 2005 to January 2006, using both transect and quadrat methods. The seagrass bed ecosystem of the Merambong Shoal supports a high density of bivalves and gastropod molluscs. A total of 119 bivalves and 131 gastropods were sampled, with combined densities ranging from 0.49 – 1.39 ind/m2. Among the bivalves, the pen shell (Pinnidae) and the venus clams (Veneridae) were the most abundant and important groups. Within the gastropods, snails () were the most important, contributing more than 50% of all gastropods sampled. The Shannon-Weiner diversity indices were high, ranging from 2.17 to 2.75 for bivalves and from 1.77 to 2.52 for gastropods. The evenness index ranged from 0.75 to 0.87 for bivalves and from 0.57 to 0.64 for gastropods, while the richness index ranged from 3.21 to 4.87 for bivalves and from 2.57 to 4.59 for gastropods. The differences in seagrass biodiversity and coverage could contribute to the differences in gastropod and bivalve composition and abundance between stations. The shoal supports large numbers of economically important such as the conch (Strombidae), venus clam (Veneridae), mussels (Mytilidae) and cockles (Arcidae), which the local communities within the coastal areas have traditionally been utilized for food.

Keywords: Diversity; benthos; invertebrate; Sungai Pulai Estuary; ecological index.

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Introduction

The seagrass is an ecologically important habitat that forms the basis of many complex marine ecosystems of the sea. The seagrass sheltering effects and abundance of adequate food make it the preferred breeding sites, nursery grounds and temporary shelter for fishes and crustaceans (Den Hartog, 1970). Dense vegetation of seagrasses produces a great quantity of organic material, and offers a good substrate for epiphytic small algae, microflora, and sessile invertebrates. The grass plant itself and its mats of rhizome creates unique microhabitats for invertebrates and other small animals. The invertebrates are very important communities in seagrass beds as the ecosystem thrives on the detrital food chain (Howard et al., 1989). Contrary to most ecosystems, in which higher trophic levels feed on living plant materials, seagrass systems are generally detrital in nature; i.e., energy transfer and foods are provided through dead plant material and associated microflora and fauna. Most invertebrates are secondary producers, which transfer energy to higher trophic levels thus maintaining the delicate food chains from collapsing (Heck et al., 1995). Some invertebrate fauna may have very close association with the seagrass meadows and form different biotic components of seagrass ecosystems. The seagrass ecosystem thus, contains a high diversity of invertebrate organisms, but inventories are lacking and monitoring for management purposes is almost non-existent. Seagrass meadows only grow in shallow waters close to the shore and are therefore very susceptible to pollution from human activities. It has been suggested that 20 – 50% of seagrass areas in Malaysia has already been damaged. Studies on the invertebrate fauna diversity, distribution and their ecology in the seagrass beds are, therefore, important for a better understanding and better management of this significant ecosystem.

Materials and Method

Study Site Merambong Shoal is located within the Sungai Pulai estuary, western Johor Straits, between 1o 19’ to 1o 21’ North and 103o 34’ to 103o 37’ East (Figure 1). Enhalus acoroides and the Halophila ovalis complex dominate the seagrass meadow. Surveys were conducted during periods of extreme low tide as the shoal was submerged most of the time. Field samplings were conducted from November 2005 to January 2006.

Field Sampling Molluscs diversity and abundance were determined using both transect and quadrat (box corer) methods. A transect belt of 50 m x 2 m was laid perpendicularly to the water edge and all mollusc present were sampled. A box corer of 0.25 m x 0.25 m was then deployed randomly to sample the molluscs that live on the sediment. The sediment within the core area was dug out using a scoop, up to ca 10 cm depth, sieved using 1 mm mesh-sized sieve, after which all molluscs were collected. A total of 5 core samples were taken along the transect line. All specimens were then preserved in 10% formalin in seawater

90 GASTROPOD AND BIVALVE MOLLUSCS ASSOCIATED WITH THE SEAGRASS BED AT MERAMBONG SHOAL, JOHOR STRAITS, MALAYSIA

FIGURE 1: The Study Location at Merambong Shoal, Johor Straits, Malaysia for further identification and analysis. Identification of gastropods and molluscs were based on Dharma (1992), Abbott (1960, 1991) and Poutiers (1998a, b).

Ecological Indices Number of taxa (S), total number of individuals (N), and various diversity indices were calculated and analysed. Discussions of these and other diversity indices can be found in Magurran (1988), Krebs (1989) etc. Among the important indexes used for this study were Shannon-Weiner diversity index (H’), dominance index (D) and Margalef’s richness index (Dmg). Macrophyte Parameters Estimation of cover adapted from Saito & Atobe (1970), as outlined in English et al. (1994). A 0.5 x 0.5 m quadrat, which was subdivided into 25 (0.1 x 0.1 m) sectors, was placed on the substratum. The dominance of each macrophyte species in each of the 25 sectors was recorded, using the classes defined in Table 1. Three replicates were sampled at each station.

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TABLE 1: Classes of Dominance Used to Record Cover (From Saito & Atobe 1970)

Class Amount of substratum % substratum Mid point % (M) covered covered 5 ½ to all 50 – 100 75 4 ¼ to ½ 25 – 50 37.5 3 1/8 to ¼ 12.5 – 25 18.75 2 1/16 to 1/8 6.25 – 12.5 9.38 1 < 1/16 < 6.25 3.13 0 absent 0 0

The coverage (C) of each species in each 0.5 x 0.5 m quadrat was calculated using the equation:

∑ (M i xf i ) C = ∑ f where: Mi is the mid point percentage of Class-i; and f is the frequency i.e. number of sectors with the same class of dominance. The process was repeated for each species present within the quadrat.

Sediment Parameters Two replicate cores of sediment (5 cm depth) were collected within each quadrat. One subsample of ~ 100 g wet weight was dried in a muffle furnace at 80oC to constant weight and incinerated at 550oC for 4 h to determine sediment organic content (percentage difference between dry weight and ash-free dry weight) (mass loss on ignition, LOI). Another subsample of ~ 50 g was used to determine grain size frequency distribution. After washing to remove salts and to extract silt-clay fraction, sand-sized particles were analysed using standard dry sieved fractionation procedures (Folk, 1966). Product moment statistics were used to calculate mean grain size and sorting coefficients (McBride, 1971).

Results

The location of each transect is presented in Table 2. In general, the habitat was comprised of sandy calcareous mud bottom type of sediment. There was no significant difference in the mean grain size (oneway-ANOVA, F = 1.09, d.f. = 8, p = 0.39), sorting coefficient (oneway-ANOVA, F = 0.82, d.f. = 8, p = 0.48), nor the sediment organic content (oneway- ANOVA, F = 4.02, d.f. = 8, p = 0.08), among the three stations. The macrophyte composition and percentage covers are presented in Table 3. Station 3 had significantly higher E. acoroides coverage compared with station 1 and 2 (oneway- ANOVA, F = 181.88, d.f. = 8, p < 0.001). Conversely, station 3 showed significantly

92 GASTROPOD AND BIVALVE MOLLUSCS ASSOCIATED WITH THE SEAGRASS BED AT MERAMBONG SHOAL, JOHOR STRAITS, MALAYSIA

TABLE 2: GPS Locations and Physical Characteristics of the Sampling Stations

Station 1 Station 2 Station 3

GPS of 1o 20.299 N 1o 20.148 N 1o 19.859 N transect 103o 36.057 E 103o 36.017 E 103o 35.953 E Grain size 1.58 2.00 1.75 1.91 1.61 2.22 1.77 2.24 2.30 Sorting 2.27 2.09 2.19 2.56 2.14 1.35 2.37 1.51 1.05 % LOI 1.05 1.17 1.12 1.33 0.96 1.43 1.30 2.38 1.90 Texture Sand loamy sand sand loamy sand sand sand sand sand sand

TABLE 3: Species Composition and Percent Cover of Macrophytes in Three Stations at Merambong Shoal. Different Abbreviations Denotes Significant Difference when Compared Between Stations, at α = 0.05

Station 1 Station 2 Station 3 Enhalus acoroides 4.17 ± 1.42a 0.46 ± 0.11a 68.25 ± 4.68b Thalassia hemprichii 0.54 ± 0.54 0.17 ± 0.11 0.63 ± 0.45 Halophila spp. 63.50 ± 8.67a 73.00 ± 1.32a 0.00b Ulva sp. 4.42 ± 1.22 0.92 ± 0.50 12.79 ± 11.50 Halodule pinnifolia 0.00 0.50 ± 0.00 0.00 Total cover 72.63 ± 9.89 75.04 ± 1.84 81.67 ± 13.17 No. macrophyte species 3.33 ± 0.33a 4.67 ± 0.33ab 2.33 ± 0.33b lower (zero) Halophila spp. coverage compared with station 1 and 2 (oneway-ANOVA, F = 61.37, d.f. = 8, p < 0.001). Station 3 had significantly lower number of macrophytes compared with station 1, but was not significantly different from station 2 (oneway- ANOVA, F = 12.33, d.f. = 8, p < 0.01). Halophila Pinnifolia was present only in station 2. There was no significant difference in T. hemprichii coverage, and Ulva coverage (oneway-ANOVA, p > 0.05) between stations. The similarity index between the various stations, based on seagrass coverage, is presented in Figure 2. Station 1 and 2 are more similar to each other compared with station 3. The composition of bivalves and gastropods sampled throughout the sampling period presented in Table 4 and Table 5, respectively. The seagrass bed ecosystem was in good condition as shown by the diverse groups of bivalves and gastropods that thrived within the seagrass meadow. A total of 119 bivalves and 131 gastropods were successfully sampled. The dominance index ranged between 0.08 to 0.13 for bivalve sub-population, and from 0.12 to 0.26 for gastropod sub-population. The Shannon diversity index ranged from 2.17 to 2.75 for bivalves, and from 1.77 to 2.52 for gastropods. The evenness index

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FIGURE 2: Bray-Curtis Similarity of the Sampling Stations ranged from 0.75 to 0.87 for bivalves and from 0.57 to 0.64 for gastropods. Finally, the richness index ranged from 3.21 to 4.87 for bivalves and from 2.57 to 4.59 for gastropods.

There was no significant difference in terms of abundance (Table 6), and the ecological indices (Table 7) of bivalve and gastropod populations sampled from the study area (p > 0.05). However, bivalves were more evenly distributed among species when compared to gastropods (oneway-ANOVA, F = 23.50, d.f. = 5, p < 0.01). In summation, the high diversity, high evenness, and low dominant values indicated that both the bivalve and gastropod mollusc populations were still in good conditions, characteristic of an undisturbed environment. Among the bivalves, the pen shell (Pinnidae) and the venus clam (Veneridae) were the most abundant and important groups. Other important bivalves included the mussels (Mytilidae) and cockles (Arcidae). Within the gastropods, conch snail (Strombidae) was the most important group of mollusc, contributing more than 50% of all gastropods sampled. Other important gastropods included the dove shells (Columbellidae), mostly epiphytic on seagrass blade, and the mud snail (Nassaridae), an important group of scavenger in seagrass habitat.

94 GASTROPOD AND BIVALVE MOLLUSCS ASSOCIATED WITH THE SEAGRASS BED AT MERAMBONG SHOAL, JOHOR STRAITS, MALAYSIA

TABLE 4: Bivalve Molluscs Sampled from Merambong Shoal, Johor Straits, Malaysia

Station 1 Station 2 Station 3 Total ARCIDAE Scapharca cornea (Reeve, 1844) 33 Trisidos tortuosa (Linnaeus, 1758) 44 Scapharca inaequivalvis (Bruguiere, 1789) 12 3 Barbatia foliata (Forsskal, 1775) 22 CARDIDAE Trachycardium sp. 1113 MALLEIDAE Malleus albus Lamarck, 1819 3216 MYTILIDAE Modiolus aratus (Dunker, 1857) 246 Modiolus philippinarum (Hanley, 1843) 3115 Perna viridis (Linnaeus, 1758) 123 PINNIDAE Atrina pectinata (Linnaeus, 1767) 47 11 Atrina vexillum (Born, 1778) 66 Pinna bicolor Gmelin, 1791 39 12 Pinna deltodes (Menke, 1843) 213 Pinna incurva (Gmelin, 1791) 11 Pinna muricata Linnaeus, 1758 123 PLACUNIDAE Placuna ephippium (Philipson, 1788) 2114 PTERIIDAE radiata (Leach, 1814) 213 SOLENIDAE Solen lamarkii Deshayes, 1839 67 13 Pharella acutidens (Broderip & Sowerby, 1828) 11 Pharella javanica (Lamarck, 1818) 11 VENERIDAE Meretrix lyrata (Sowerby, 1851) 75 12 Placamen tiara (Dillwyn, 1817) 44210 Clausinella chlorotica 31 4 TOTAL 426116119

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TABLE 5: Gastropod Molluscs Sampled from Merambong Shoal, Johor Straits, Malaysia

Station 1 Station 2 Station 3 Total COLUMBELLIDAE Euplica scripta 37 414 Pyrene versicolor (Sowerby, 1832) 10 8 15 33 CYPRAEDAE Cyprae annulus Linnaeus, 1758 21 3 Cyprae ovum 11 Cyprae onyx Linnaeus, 1758) 11 Cyprae sp. 11 Pugilina ternatana (Gmelin, 1791) 24 17 Pugilina cochlidium (Linnaeus, 1758) 22 MURICIDAE Murex martinianus Reeve, 1845 33 Thais gradata 11 NASSARIDAE Nassarius spp. 51 28 Nassarius albescens 24 17 Nassarius venustus 31 15 NATICIDAE Polinices didyma (Roding, 1798) 11 Polinices melanostomus (Gmelin, 1791) 11 Natica tigrina (Roding, 1798) 53 19 APLYSIIDAE Syphonata geographica 12 3 STROMBIDAE Strombus canarium Linnaeus, 1758 30 18 2 50 Strombus urceus Linnaeus, 1758 12 8 0 20 Strombus marginatus var. robustus 33 Strombus marginatus var. succinctus 22 Strombus vittatus vittatus 21 3 TROCHIDAE Trochus maculatus Linnaeus, 1758 358 TURRITELLIDAE Turritella sp. 11 2 melo (Lightfoot, 1786) 22 nobilis 34 7 SCAPHOPODA Dentalium sp. 22 TOTAL 97 69 33 131

96 GASTROPOD AND BIVALVE MOLLUSCS ASSOCIATED WITH THE SEAGRASS BED AT MERAMBONG SHOAL, JOHOR STRAITS, MALAYSIA

TABLE 6: Abundance and Density of Molluscan Fauna from Merambong Shoal, Johor Straits, Malaysia

Bivalvia Total N Density N Density N Density

T1 42 0.42 97 0.97 139 1.39 T2 61 0.61 69 0.69 130 1.3 T3 16 0.16 33 0.33 49 0.49

Mean 39.67 0.40 66.33 0.66 106.00 1.06 S.E. 13.04 0.13 18.52 0.19 28.62 0.29

TABLE 7: Ecological Indices Calculated for Molluscs at Merambong Shoal, Johor Straits, Malaysia

Bivalvia Gastropoda Mean ± S.E. Range Mean ± S.E. Range

No. of Species 14.67 ± 3.28 10.00 – 21.00 16.67 ± 3.53 10.00 – 22.00 No. of Individuals 39.67 ± 13.04 16.00 – 61.00 66.33 ± 18.52 33.00 – 97.00 Dominance (D) 0.10 ± 0.02 0.08 – 0.13 0.17 ± 0.04 0.12 – 0.26 Shannon (H’) 2.44 ± 0.17 2.17 – 2.75 2.25 ± 0.24 1.77 – 2.52 Simpson (1-D) 0.90 ± 0.02 0.87 – 0.92 0.83 ± 0.04 0.74 – 0.88 Evenness (J) 0.83 ± 0.04 0.75 – 0.87 0.60 ± 0.02 0.57 – 0.64

Margalef (Dmg) 3.77 ± 0.55 3.21 – 4.87 3.73 ± 0.60 2.57 – 4.59

Discussion

Seagrass beds are important and highly productive marine ecosystems that support large number of marine animals (Odum, 1975; Den Hartog, 1970). In estuarine and shallow water environments, seagrasses are important primary producers yielding food for a number of invertebrates (Mayer et al., 1975), producing raw materials for fertilisers (McRoy & Helffreich, 1980), as sediment stabilisers (Thorhaug, 1986), and most importantly forming suitable habitat for various organisms (Kikuchi & Peres, 1977). This study showed that the seagrass bed of Merambong Shoal supported high density of bivalves and gastropod molluscs. The Shannon-Weiner diversity indices were considered high, which ranged from 2.17 to 2.75 for bivalves and from 1.77 to 2.52 for gastropods. These values were higher compared with a similar study by Omar et al., (2001), on gastropods in the seagrass at Barang Lompo Island, Indonesia. In their study, diversity index (H’) values ranged from 0.96 to 1.34, and evenness index (J) values from 0.71 to 0.80.

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The differences in seagrass biodiversity and coverage could contribute to the differences in observed gastropod and bivalve molluscs composition and abundance between stations. According to Heck & Orth (1980), the diversity and abundance of fishes and invertebrates were related to seagrass morphology, or seagrass surface area, and species richness and abundance of animals should increase with increasing seagrass density. Omar et al. (2001) found gastropod diversity and abundance in areas with higher seagrass density. The Merambong shoal supports large numbers of economically important species such as the conchs (Strombidae), venus clams (Veneridae), mussels (Mytilidae) and cockles (Arcidae). Local communities within the coastal areas has traditionally been utilising the shoal as collecting and gleaning sites for gastropods and molluscs (Japar et al., 2006). The most important species is S. canarium, which is abundant during peak collecting season, from November till end of March, when hundreds of people come to the shoal to harvest this species during this period.

Acknowledgements

The authors would like to thank the Deanery and staff of the School of the Environmental and Natural Resource Sciences, Universiti Kebangsaan Malaysia (UKM), for technical support and laboratory facilities provided. The first author would also like to thank the Faculty of Science, UKM for the research grant (ST-020-2005), which made this study possible.

References

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