CHECKLIST OF MANGROVE SNAILS (MOLLUSCA: GASTROPODA) IN
SETIU WETLANDS
            Nursalwa Baharuddin1*, Melissa Beata Martin1, Thilahgavani Nagappan1, and
                                       Hafiz Borkhanuddin1
          1School   of Marine and Environmental Sciences, Universiti Malaysia Terengganu,
                           21030 Kuala Terengganu, Terengganu, Malaysia
                                        *
[email protected]Keywords: gastropods, mangrove forest, species checklist, distribution
INTRODUCTION
Gastropods (Gastropoda) belongs to the phylum Mollusca and are the second most diverse
animal class (behind Insecta), especially in terms of described species in the tropical forests
(Schilthuizen and Rutjes 2001; Schilthuizen et al. 2002). Gastropods are algal feeders,
detritivores or deposit feeders that feed on living and decaying algae, organic detritus and plant
materials and consequently are important in the food webs (Houbrick 1984; 1991; Plaziat 1984;
Kelaher et al. 2007; Nagelkerken et al. 2008). Gastropods are rich in protein and are a delicacy
in some parts of Malaysia, such as Sarawak (Hamli et al. 2013). In Brunei, Thailand and
Indonesia, gastropods are included in the diet of coastal communities (Nursalwa 2016; Sri-
aroon et al. 2004; Burgos 2016).
         Gastropods can be categorized as either epifauna which live on solid surfaces or
arboreal which live on vegetation. Gastropods are unique from an ecological perspective
because they inhabiting extremely contrasting habitats (Marshall et al. 2015) such as marine,
freshwater and terrestrial environments [although they are predominantly marine] compared
to other larger metazoans (Dayrat et al. 2011; Webb 2012). Cantera et al. (1983) reported 277
species of gastropods are associated with mangrove forests globally.
         Mangrove forests span shorelines and are considered the most productive ecosystem
in the world (Berger et al. 2008). Mangrove forests are crucial to gastropods providing breeding
and nursery grounds, food sources and shelter from predators (Vermeij 1973; Plaziat 1984;
Reid 1986; Plaziat et al. 2001; Lozouet and Plaziat 2008; Reid et al. 2008; Reid et al. 2010).
In tropical countries, the total land area covered by mangrove forest has decreased from
170,000 km2 in 2001 to 150,000 km2 in 2008 (Valiela et al. 2001; Alongi 2008).
         In the east coast of Peninsular Malaysia lies Setiu Wetlands which is the largest
wetland system in Malaysia (Sathiamurthy 2015). Setiu Wetlands includes 10 different
habitats: estuaries, deltas, intertidal mudflats, sand flats, mangroves forest, coastal brackish,
lagoons, marshes, freshwater swamp forest and lowland dry forest (Nakisah and Fauziah
2003). These large systems are under pressure due to conversion of land for aquaculture
(such as pen and oyster cultures), supporting the rapidly growing economic activities in the
area (Li 2016; Suratman et al. 2014). Consequently, it is crucial to understand the species
richness and relative abundance of gastropods in shallow marine environments (particularly
mangrove forest) considering gastropods diversity is declining vastly worldwide (Nützel and
Hausmann 2016; Lydeard et al. 2004).
         This study aims to provide a checklist of species and distribution information of
gastropods in the mangrove forests of Setiu Wetlands.
MATERIALS AND METHODS
Study area
Mangrove forests of Setiu wetlands are located in the Setiu district of north Terengganu that
covers a 14 km stretch of lagoon by the South China Sea coastline. Nine different sampling
stations were selected for this study (Figure 1). The descriptions of the sampling stations are
provided in Table 1.
                                                                                                1
                                          South China Sea
Figure 1: Map of sampling stations in mangrove forests of Setiu Wetlands. The locations are
1: Pulau Semut; 2: Pulau Che Him; 3: Pulau Besar; 4: Pulau Tok Haji; 5: Pulau Gemia I; 6:
Pulau Gemia II; 7: Pulau Gemia III; 8: Pulau Kerengga I; and 9: Pulau Kerengga II. Source:
Google Earth.
Gastropods were collected from the 21st to the 23rd of April 2016 during the WWF-Setiu
Wetlands Scientific Expedition. Live gastropods were randomly collected from mangrove roots,
branches, leaves, trees or on mud and sandy substratum at each station (Table 1). Gastropods
were handpicked and preserved in 70% ethanol. All specimens were identified based on
Nursalwa and Marshall (2014) and nomenclature was verified via World Register of Marine
Species (WoRMS, www.marinespecies.org). Specimens were photographed and deposited at
the School of Marine and Environmental Sciences, Universiti Malaysia Terengganu.
                                                                                          2
Table 1: GPS coordinates for each sampling location, sediment type and vegetation of
mangrove forests, Setiu Wetlands.
 Station
 No.       Station name          Coordinates           Sediment type        Vegetation
                                                                            Nypa fruticans,
    1      Pulau Semut           05°40'31.7"N;         Mud + Clay           Rhizophora apiculata,
                                 102°43'05.3"E                              Avicennia sp.
    2      Pulau Che Him         05°40'15.9"N;         Sand                 Nypa fruticans,
                                 102°43'25.8"E                              Rhizophora apiculata
    3      Pulau Besar           05°39'27.7"N;         Mud + Sand           Nypa fruticans,
                                 102°44'23.2"E                              Rhizophora apiculata,
                                                                            seagrass
    4      Pulau Tok Haji        05°39'15.6"N;         Mud + Sand           Nypa fruticans
                                 102°44'37.5"E
    5      Pulau Gemia I         05°39'05.9"N;         Mud                  Nypa fruticans,
                                 102°44'59.6"E                              Rhizophora apiculata
    6      Pulau Gemia II        05°38'47.7"N;         Mud                  Nypa fruticans
                                 102°45'08.9"E
                                 05°38'33.2"N;         Mud                  Avicennia sp.,
    7      Pulau Gemia III       102°45'45.6"E                              Rhizophora apiculata
                                 05°37'26.8"N;
    8      Pulau Kerengga I      102°47'14.9"E         Soft mud + Silt      Nypa fruticans
    9      Pulau Kerengga II     05°37'25.1"N;         Mud                  Nypa fruticans
                                 102°47'16.8"E
RESULTS AND DISCUSSION
A total of 17 species comprising 6 families and 3 subclasses of gastropods were collected
(Figure 2, Table 2). The species richness was highest in Pulau Semut, Pulau Che Him and
Pulau Gemia III, with 8-9 species consisting of species from 3 families - Littorinidae,
Potamididae and Neritidae. In contrast, the lowest species richness was found at Pulau Gemia
II with only a single species recorded: Cerithidea quoyii (Figure 2, Table 2).
         Of the 17 species of gastropods collected at Setiu Wetlands, 5 species of gastropods
(Assiminea brevicula, Littoraria pallescens, Cerithidea sp., Batillaria zonalis, and Cassidula
nucleus) were only found at Pulau Semut, Pulau Che Him and Pulau Gemia I but not at other
stations. The most widely distributed species were Littoraria articulata, Littoraria carinifera,
Littoraria lutea, Pirenella alata and Cerithidea quoyii (found at almost all stations). Other
common gastropods that were distributed irregularly included Littoraria melanostoma,
Littoraria strigata, Pirenella cingulata, Clithon faba, Clithon oualaniense, Neripteron violaceum
and Neripteron sp. (Table 2, Figure 3).
                                                                                               3
                                   10
                                    9
                                    8
               Number of species    7
                                    6
                                    5
                                    4
                                    3
                                    2
                                    1
                                    0
                                        1   2   3   4      5    6   7   8   9
                                                        Station
Figure 2: Comparison of species richness across nine sampling stations of mangrove forests,
Setiu Wetlands.
In this study, species richness of gastropods inhabits mangrove forest in Setiu wetlands
consists of 17 species from 6 families. These findings were similar to the findings of Hamli et
al. (2013) in Sarawak (Kuching, Sibu, Mukah, Bintulu, Miri, Limbang and Lawas) who reported
21 species from 11 families; Ashton et al. (2003) who reported 37 species from 8 families in
Sematan mangrove forest, Sarawak; Rahmawati et al. (2015) that reported 17 species from 7
families in Aceh Besar mangrove forest, Indonesia; and Piamklad et al. (2014) who reported
28 species from 12 families in mangrove forest at Pak Nam Pran, Thailand. However, the
species richness reported at this forests in Southeast Asia (including the present study) were
considerably lower than the species richness reported from mangrove forests of Uttara
Karnataka, India at 133 species (Boominathan et al. 2012). Our study covered nine stations
from Pulau Semut to Pulau Kerengga (almost half of total 14 km lagoon) but was limited to a
three day sampling period.
        We found the highest species richness of gastropods from collections on vegetation
such as on Nypa fruticans, Rhizophora apiculata, and Avicennia sp. leaves, stem, branches
and roots. In this study, family Littorinidae was the highest in terms of species richness with 6
species that were found at almost all stations. Littoraria feed on young mangrove trees (Reid
1986) and species such as Littoraria articulata, Littoraria delicatula and Littoraria melanostoma
graze on hairs of Avicennia leaves (Bouillon et al. 2002). Studies by Reid (1986) and Blanco
and Cantera (1999) also found that Littoraria may graze on surface layers of trunks and roots
where micro-ephipytes are available. Moreover, Littoraria are tree-dwelling snails and have
been categorized as tree climbers, climbing up and down trees following tidal cycles (Tee
1982).
        The second most common gastropod families (in terms of species richness) -
Potamididae, Batillariidae, and Neritidae. Potamididae - were found on clay, mud or sand.
Species such as Pirenella cingulata, Pirenella alata and Cerithidea sp. were found in high
abundance in at least in four stations. High abundances of these families was also recorded in
eastern Thailand (Sri-aroon et al. 2004) and in the United Arab Emirates lagoon (Feulner and
Hornby 2006). Gastropods in the family Potamididae are known as mud creepers or horn shells
and can be found on solid surfaces of the mangrove substratum. Species of the genus
Pirenella (previously known as Cerithidea; WoRMS 2016) were dominant at mangrove forests
of Pondicherry, India (Satheeshkumar and Khan 2012) and reportedly favour places with
sandy and firm substrates overgrown by algae (Feulner and Hornby 2006).
                                                                                               4
Table 2: Species distribution and habitats of gastropods from nine sampling stations of Setiu
Wetlands, mangrove forests.
 Subclass /      Species                                               Stations                                  Habitats
 Family
                                       1       2       3       4         5       6       7       8       9
 Caenogastropoda
 Assimineidae Assiminea                    -       -       -       -      √          -       -       -       -   Solid surface,
              brevicula                                                                                          under shaded
                                                                                                                 mangrove trees
 Littorinidae    Littoraria            √       √       √       √             -       -   √           -       -   Mangrove
                 articulata                                                                                      leaves, stem,
                                                                                                                 branches
                 Littoraria            √       √       √       √             -       -   √       √       √       Mangrove
                 carinifera                                                                                      leaves, stem,
                                                                                                                 branches
                 Littoraria lutea      √       √       √       √             -       -   √           -   √       Mangrove
                                                                                                                 leaves,
                                                                                                                 branches
                 Littoraria                -       -   √           -         -       -   √           -       -   Mangrove
                 melanostoma                                                                                     leaves,
                                                                                                                 branches
                 Littoraria                -   √           -       -         -       -       -       -       -   Mangrove
                 pallescens                                                                                      leaves,
                                                                                                                 branches
                 Littoraria strigata       -   √           -       -         -       -   √           -       -   Mangrove
                                                                                                                 leaves,
                                                                                                                 branches
 Potamididae     Pirenella alata       √       √           -       -      √          -   √           -       -   Solid surface
                                                                                                                 (clay, mud or
                                                                                                                 sand)
                 Pirenella             √       √           -       -      √          -       -       -       -   Solid surface
                 cingulata                                                                                       (clay, mud or
                                                                                                                 sand)
                 Cerithidea quoyii     √           -       -   √             -    √          -   √       √       Mangrove stem,
                                                                                                                 roots
                 Cerithidea sp.        √           -       -       -         -       -       -       -       -   Solid surface
                                                                                                                 (clay or sand)
 Batillariidae   Batillaria zonalis        -   √           -       -         -       -       -       -       -   Solid surface
                                                                                                                 (clay, mud or
                                                                                                                 sand)
 Neritimorpha
 Neritidae       Clithon faba              -       -       -       -         -       -   √           -   √       Mangrove stem
                                                                                                                 and roots
                 Clithon               √       √       √           -         -       -       -       -       -   Solid surface
                 oualaniense                                                                                     (clay, mud or
                                                                                                                 sand)
                 Neripteron            √           -       -   √             -       -       -   √       √       Mangrove stem
                 violaceum
                 Neripteron sp.            -       -       -   √             -       -   √           -       -   Mangrove stem
 Heterobranchia
 Ellobiidae     Cassidula                  -       -       -       -      √          -       -       -       -   Mangrove stem,
                nucleus                                                                                          roots, solid
                                                                                                                 surface (clay,
                                                                                                                 mud)
                                                                                                                                  5
Figure 3: Gastropods collected at mangrove forests, Setiu Wetlands. A: Assiminea brevicula; B:
Littoraria articulata; C: Littoraria carinifera; D: Littoraria lutea; E: Littoraria melanostoma; F:
Littoraria pallescens; G: Littoraria strigata; H: Pirenella alata; I: Pirenella cingulata; J: Cerithidea
quoyii; K: Cerithidea sp.; L: Batillaria zonalis: M: Clithon faba; N: Clithon oualaniense;
O: Neripteron violaceum; P: Cassidula nucleus; and Q: Neripteron sp.
                                                                                                           6
CONCLUSION
This study revealed that species richness and distribution varied with habitat characteristics
and vegetation. We found 17 species representing 6 families and 3 subclasses of gastropods
in the mangrove forests of Setiu Wetlands. It is recommended that sampling periods to be
extended so that mangrove forests along the 14 km lagoon are covered and contribute towards
a more comprehensive. The present findings provide information on gastropods that would be
a useful reference for scientists and community members that work in the wetland. This will
ensure decision and policy makers are well-informed and take into account sustainability
before converting this wetland for development activities in the future.
ACKNOWLEDGEMENTS
We would like to thank the WWF organising committee in providing accommodation, meals
and transportation during the expedition. Special gratitude to Mr. Adnan Abd Ghani (UMT) and
Mr. Mohd Fadli Seman (UMT) for their awesome navigation through shallow and narrow waters
through the lagoon; Mr. Tye Andrew Jeffrey (Museum of Tropical Queensland, Australia) for
his support and sampling expertise; and Dr. Izwandy Idris (UMT) in providing his high
resolution DSLR Nikon camera for photography.
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