1 Marine Science Centre, Office of Deputy Vice Chancellor (Research & Innovation),

Universiti Putra

Malaysia, Batu 7, Teluk Kemang, 71050 Port Dickson, Negeri Sembilan, Malaysia.

* Coressponding author e-mail: nurleena@upm.edu.my

2 Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia.

3 Faculty of Agriculture and Food Sciences, Universiti Putra Malaysia Kampus Bintulu.

4 School of Environmental & Natural Resource Sciences, Faculty of Science &

Technology, UniversitiKebangsaan Malaysia.

Malayan Nature Journal 2014, 66(1 and 2), 42-51

The Epifaunal Marine Bivalves and Macrophytes in

Merambong Shoal, Pulai River Estuary, Straits of Malacca

WONG N. L. W. S.1*, A. ARSHAD

2, F. M. YUSOFF

2, B. JAPAR

SIDIK3 and A. G. MAZLAN

4

Abstract : The study was carried out to investigate the diversity of

epifaunal bivalves in Merambong seagrass bed, Pulai River Estuary. The

sample collection field trips started from May 2008 to July 2009, 18

transects (from six stations) have been laid perpendicularly along the

elongated shoal during lowest low spring tide. A total of 15 species from

10 bivalve families were recorded throughout the study period. Young

Anadara gubernaculum attached to Enhalus ecoroides showed the

highest abundance throughout the seagrass bed. Veneridae is the most

diverse family with four species recorded during the study followed by 2

species each for Mytilidae and Pinnidae. Negative correlation was

observed between Circe scripta abundance and Ulva spp. coverage (r2= -

0.829, P= 0.042). Station 4 (H’=1.2137; 1-D=0.5807; S=10) and Station

6 (H’=1.5279; 1-D=0.6696; S=13) have higher bivalve diversity and

species richness, and are more heterogeneous compared to other stations.

However, bivalve density was relatively lower in both stations 4 and 6

than the rest of the stations. The result of this study revealed that the

coverage of macrophytes plays an important role in determining the

density and distribution of epifaunal bivalves.

Keywords : Epifaunal bivalve; marine macrophytes; seagrass

INTRODUCTION

Merambong Shoal (1o

19.55’ N, 103o 35.57’ E) seagrass bed is a unique

ecosystem in Pulai River Estuary (Figure 1), southwest of Johor Straits.

It is surrounded by rivers, mangrove, stilts villages, industrial zone and

even small patches of reef around the nearby island.

42

It is a 30 ha sandy-mud subtidal shoals where from nine species

out of a total of 12 seagrass species recorded in Malaysia could be found

here (Japar Sidik et al. 2006). Over the years Merambong Shoal has been

providing food for the local fishing communities in terms of marine

fishes, crabs, and edible molluscs such as bivalves and gastropods. This

valuable ecosystem has major market and non-market economic values

in fisheries, raw materials research, shoreline protection, carbon

sequestration and as an important contributor in biodiversity (MPP-EAS

1999).

However, due to rapid and heavy development activities in the

surrounding area, and with the increasing number of people utilizing the

coast and adjacent waters, this ecosystem is currently under serious

threats (Japar Sidik et al. 2006). Epifaunal invertebrates which include

benthic bivalves and gastropods are organisms which rely on the

aboveground part of seagrass as major habitat throughout their life span

(Nakaoka 2005). Hence they are expected to be more sensitive to

changes in flora abundance and structures compared to the epifaunal

species. However, from previous studies Nakaoka (2005) found that

epifaunal species on different species of seagrasses overlap broadly

within each locality. While a species of epifaunal bivalve might not

completely rely on a single species of macrophyte as their habitat, it is

important to find out the relationship between epifaunal bivalves and the

macrophytes coverage as a whole to determine the influence of

macrophytes coverage on the distribution of epifaunal bivalves or vice

versa.

Therefore, in this study the abundance of epifaunal bivalves and

coverage of marine macrophytes will be estimated. The relationship

between these two groups of organisms will be explored. Epifaunal

bivalve richness and diversity for each station along the shoal will be

determined, while the coverage and species composition of seagrass and

macroalga, Ulva spp., will be taken into account. Ulva spp. is normally

found loose among seagrasses (Japar Sidik et al. 2001). Ulva is a genus

of thin-leaf green macroalgae which is also known as sea lettuce. Unlike

the seagrasses which have root system that would limits the seagrasses

movement to its leaves, Ulva spp. often hang loose between seagrasses

blades and could cover a wide area with its flexible sheet-like thallus. It

might play an important role in affecting the abundance of epifaunal

bivalve by providing protection against predations.

MATERIALS AND METHODS

Monthly field trips for sample collection were conducted during low

spring tides between May 2008 and July 2009. Due to the highly turbid

water in this area (which exposed to muddy mangrove soils in the north

43

and Singapore industrial zone in the east), research activities were

limited to low tides when tide is lower than 0.2 m and the shoal is

exposed during receded tide. Sampling trip was ceased from September

2008 to April 2009 because of unsuitable tides and resumed by May

2009. Eighteen transect belts (three transects per station) with 50m in

length and 5m in width were laid perpendicular to the length of

Merambong Shoal in Pulai River Estuary. For each transect belt, five

0.5m x 0.5m quadrats were placed along the belt for macrophytes

coverage estimation using the phytosociological technique of Saito and

Atobe (1970) as described in English et al. (1994). All epifaunal found

aboveground by visual and touch among macrophytes were collected and

preserved in 5% buffered formalin before transported back to the

laboratory in Institute of Bioscience, Universiti Putra Malaysia.

Bivalve specimens were identified based on the references of

Poutiers (1998), Lamprell and Healy (1998) and Okutani (2000) while

macrophytes were identified with the aid of Seagrass-Watch (McKenzie

et al. 2009). The relationship between bivalves and macrophytes were

explored using Spearman’s Rank correlation coefficient (r2) in SPSS

statistical analysis programme while bivalves diversity were determined

with the Shannon-Wiener diversity index in PRIMER 5.

RESULTS

There are 15 species from 10 families of epifaunal bivalves found in the

seagrass ecosystem in this study (Table 1). Family Veneridae is the most

diverse group with four species found within transects followed by

families Mytilidae and Pinnidae with two species each. Anadara

gubernaculum is widely distributed and could be found in almost all

transects with total number of specimens collected up to 647 (216±35

ind./transect) in Station 3 (Table 1). However, low abundance were

observed in Stations 4 and 6 with only 94 individuals (31±16

ind./transect) and 14 individuals (5±5 ind./transect) sampled.

Though lower in epifaunal bivalves abundance, Station 4 (21

ind./100m2) and Station 6 (25 ind./100m

2) have higher species richness

compared to the other stations (Table 2). Shannon-Wiener diversity

indices for both Station 4 (H’= 1.2137; J=0.5271; 1-D=0.5807) and

Station 6 (H’=1.5279; J=0.5957; 1-D=0.6696) revealed higher epifaunal

bivalve diversity and the species were more heterogeneous and evenly

distributed in comparison to other stations (Table 2).

Meanwhile, a total of eight species of macrophytes were identified in

this study. These are Enhalus acoroides, Ulva spp., Halophila ovalis,

Halophila minor, Halophila spinulosa, Halodule pinifolia, Cymodocea

serrulata and Thalassia hemprichii. Among these macrophytes, E.

acoroides, Ulva spp. and H. minor were found in all stations (Table 3).

44

The highest number of macrophytes present were observed in Stations 5

and 6, whereas the lowest number of species presence where found in

both Stations 1 and 3 with five species in total (Table 3).

Among the eight species of macrophytes, Ulva spp. was found to be

the most dominant. In fact it was found to dominate in all the stations,

taking up more than 50% of the total macrophytes populations in Stations

1 and 3, 41.8% in Station 4 and more than 33% in Stations 5 and 6

(Figure 2). Whereas, Halodule pinifolia was found to be the least

dominant species with the highest percentage contribution of 2.37% in

Station 4. Likewise Halodule pinifolia was present only in three stations

(Stations 4, 5 and 6).

Overall, Spearman’s Rank correlation coefficient (r2) between the

abundance of epifaunal bivalves and macrophytes coverage are weak and

not significant (Table 4). However, significant negative correlations

between the abundance of C. scripta and Ulva spp. coverage (r2= -0.829,

P=0.042) was observed (Table 4).

DISCUSSION

Seagrasses habitat generally formed along the mainland coastal areas

between mangroves and corals from low tide level to coral reef fringe

(Japar Sidik et al. 2006). Merambong Shoal seagrass bed creates a unique

ecosystem unlike any other seagrass beds in Malaysia. Surrounded by

various ecosystems and influenced by heavy human impacts, it is under

greater threat than any other seagrass ecosystem along the coastal area.

The complexity of the environment might contribute to the lack of

uniformity in biodiversity throughout the shoal.

Anadara gubernaculum was found in distinctively high density in

most stations compared to other epifaunal species. Interestingly, this

species is a burrowing infaunal in later stage of their life and only their

youngs could be found attach to macrophytes with byssus. Most of the

specimens collected were found attached on blades of E. acoroides or

thallus of Ulva spp. Though there is no significant correlation between A.

gubernaculum and coverage of macrophytes E. acoroides and Ulva spp.,

it is interesting to note that there exist a negative correlations between

this bivalve species and coverage of two seagrass species, H. minor and

H. ovalis (Table 4.). Most A. gubernaculum specimens found have length

ranging from 10 to 23 mm. Perhaps, the size and mass of A.

gubernaculum may be too much for the fragile stem and leaf of these two

relatively small seagrass species. Hence, contributed to the negative

relationship.

In contrary, negative correlations were found between Modiolus

philippinacum and macrophytes E. acoroides and Ulva spp. (Table 4).

Again, although the relationship was not statistically significant, M.

45

philippinacum apparently present in area with less shed and better

exposure. This was further proven during other trips where M.

philippinacum was collected for other research purposes. Most

specimens of this species were found among small seagrass species such

as H. ovalis and H. minor. Enhalus acoroides and Ulva spp. were found

throughout the shoal (Table 3) with the long blades of E. acoroides

providing calmer water columns for the free-floating Ulva spp. Ulva spp.

is a group of well-known macroalgae which are effective biofilter for

treatment of effluents from aquaculture farm (Vandermeulen and Gordin

1990; Cohen and Neori 1991; Neori et al. 1991, 2003; Jimenez et al.

1996; Msuya and Neori 2002; Msuya et al. 2006). This group of green

algae has been tested for their ability to control harmful algal bloom and

Ulva lactuca was successfully tested for successfully reducing the cell

density of common harmful algal bloom species via allelopathy (Tang

and Gobler 2011).

The increase in abundance of Ulva spp. might be closely related to

other environmental factors. Sousa-Dias and Melo (2008) found that the

coverage of Ulva spp. shows a significant positive correlation with

temperature and concluded that algae such as Ulva spp. are excellent

environmental indicators. Increase in air and sea surface temperature

could provide a positive influence in flourishing of Ulva spp. and

therefore, as suggested by Sousa-Dias and Melo (2008), the current

global warming scenarios might increase the dominance of Ulva spp.

Using microcosm experiment, Bartoli et al. (2003) has proved that the

presense of clam increases the growth rate and production of Ulva spp.

thallus segments. However, thick macroalgae mats could create

unfavourable environment for the clams. Thick Ulva spp. mats on the

surface of sediment could reduce the dissolved oxygen level under the

macroalgal mats (Marsden and Bressington, 2009) and causing the clams

to move away from this harsh living condition. This could explain the

negative correlations between the highly abundant Ulva spp. and

epifaunal bivalves, C. scripta, P. sella and M. philippinacum (Table 4).

Local fishermen have commented on the decrease of seagrass

density and the appearance of patchiness on the shoal over the last tenth

of years. With the rapid development on the coastal area along Johor

Straits, heavy silt carried by the turbid river outflow may have caused

sedimentation on the northern shoal over years and threaten the survival

of smaller seagrasses species (Figure 2).

In a study conducted by Peterson and Heck Jr. (2001), seagrass

assemblages significantly affect the survival of suspension feeding

bivalve and shows a strong mutualistic relationship between Modiolus

americanus and Thalassia testudinum. The study also suggests that

seagrass meadows may exist as a nutrient and productivity ‘hot spots’

with the presence of suspension feeding organisms to provide essential

46

Figure 1. Arrows show the location of Merambong Shoal seagrass bed

between Peninsular Malaysia and Singapore. (Lower inserted image

shows sampling stations along the shoal.)

Table 1. Total number of epifaunal bivalves collected from each station

(750m2) on Merambong Shoal, Johor.

Family Species St.1 St.2 St.3 St.4 St.5 St.6

Arcidae Anadara gubernaculum

(Reeve, 1844) 281 537 647 94 506 14

Veneridae Circe scripta Linnaeus,

1758 1 16 13 44 23 101

Placamen isabellina

(Philippi, 1849) 0 0 0 3 4 6

Anomalocardia squamosa

Linnaeus, 1758 0 1 0 5 1 0

Gafrarium divaricatum

(Gmelin, 1791) 0 1 0 1 0 2

Placunidae Placuna sella

(Philipsson, 1788) 0 5 5 7 1 15

Mytilidae Modiolus philippinarum

Hanley, 1844 0 0 0 2 0 37

Perna viridis

(Linnaeus, 1758) 0 0 1 0 0 1

Pinnidae Pinna bicolor Chemnitz in 0 3 3 0 0 2

47

Gmelin, 1790

Atrina vexillum Born, 1778 0 0 0 0 0 4

Mactridae Mactra mera (Reeve, 1853) 0 0 3 2 1 1

Pteridae Pinctada fucata

(Gould, 1850) 0 0 0 2 0 4

Solenidae Solen sp. 0 0 0 1 0 0

Pectinidae Chlamys sp. 0 0 0 0 0 1

Placutilidae Plicatula sp. 0 0 0 0 0 1

Total: 10 15 282 563 672 161 536 189

Table 2. Ecological indices calculated for epifaunal bivalve from each

station at Merambong Shoal, Johor.

St.1 St.2 St.3 St.4 St.5 St.6

Shannon (H') 0.0235 0.2386 0.2073 1.2137 0.2612 1.5660

Species Richness

(S) 2 6 6 10 6 13

Evenness (J’) 0.0340 0.1332 0.1157 0.5271 0.1458 0.6105

Table 3. Marine macrophytes recorded from each sampling station in

Merambong Shoal, Johor.

Species\Site St.1 St.2 St.3 St.4 St.5 St.6

Enhalus acoroides (L.f.) Royle + + + + + +

Ulva spp. + + + + + +

Halophila ovalis (R.Br.) Hook. f. + +

+ + +

Halophila minor (Zoll.) den Hartog + + + + + +

Halophila spinulosa Aschers.

+

+ +

Halodule pinifolia (Miki) den Hartog

+ + +

Cymodocea serrulata (R. Br.) Aschers.

and Magnus

+ + + +

Thalassia hemprichii (Ehrenb.)

Aschers.

+ + + + +

Total: 5 6 5 6 8 8

48

Table 4. Spearman’s Rank correlation coefficient (r2) of four most

abundance bivalve and macrophytes species in Merambong Shoal

seagrass ecosystem.

nutrients for floral productivity. There are numerous possibilities when

exploring the truth behind the decreasing of epifaunal molluscs

population which are collected by the local fishermen as food product.

Some might suggest that the decline in seagrass density might be the

reason of the falling mollusc population. If the theory of Peterson and

Heck Jr. (2001) is taken into account, one might need to explore the

condition in an opposite direction which suggest that the decline in

suspension-feeding mollusc could be the reason for the lost of seagrasses.

Further studies are necessary to pinpoint the threats behind the decrease

of certain bivalve population.

Bivalve abundance

(total number per

transect)

Coverage (%)

Enhalus

acoroides Ulva spp.

Halophil

a minor

Halophila

ovalis

Anadara

gubernaculum

r2 0.371 0.429 -0.486 -0.543

P 0.468 0.397 0.329 0.266

Circe scripta r2 0.029 -0.829* 0.657 -0.029

P 0.957 0.042 0.156 0.957

Placuna sella r2 0.174 -0.522 0.551 -0.319

P 0.742 0.288 0.257 0.538

Modiolus

philippinacum

r2 -0.068 -0.541 0.541 0.101

P 0.899 0.268 0.268 0.848

*Correlation is significant at the 0.05 level.

49

Figure 2. Species composition of macrophytes in each station in

Merambong Shoal, Straits of Malacca.

50

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