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Article

Assessing the Fauna Diversity of Marudu Bay Mangrove Forest, Sabah, Malaysia, for Future Conservation

by
Mohamed Zakaria
1,* and
Muhammad Nawaz Rajpar
2
1
Faculty of Forestry, Universiti Putra Malaysia, UPM International, Serdang 43400, Selangor Darul Ehsan, Malaysia
2
Sindh Wildlife Department, Opposite PIA Reservation Office, Moulana Din Muhammad Road, Saddar, Karachi 77550, Pakistan
*
Author to whom correspondence should be addressed.
Diversity 2015, 7(2), 137-148; https://doi.org/10.3390/d7020137
Submission received: 24 February 2015 / Revised: 20 April 2015 / Accepted: 21 April 2015 / Published: 30 April 2015
(This article belongs to the Special Issue Mangrove Conservation)

Abstract

:
Mangrove is an evergreen, salt tolerant plant community, which grows in inter-tidal coastal zones of tropical and subtropical regions of the world. They are ecologically important for many fauna species and are rich in food resources and consist of many different vegetation structures. They serve as ideal foraging and nursery grounds for a wide array of species such as birds, mammals, reptiles, fishes and aquatic invertebrates. In spite of their crucial role, around 50% of mangrove habitats have been lost and degraded in the past two decades. The fauna diversity of mangrove habitat at Marudu Bay, Sabah, East Malaysia was examined using various methods: i.e. aquatic invertebrates by swap nets, fish by angling rods and cast nets, reptiles, birds, and mammals through direct sighting. The result showed that Marudu Bay mangrove habitats harbored a diversity of fauna species including 22 aquatic invertebrate species (encompassing 11 crustacean species, six mollusk species and four worm species), 36 fish species, 74 bird species, four reptile species, and four mammal species. The wide array of fauna species could be due to the availability of complex vegetation structures, sheltered beaches and tidal mudflats, which are rich in food resources and also offer safe foraging and breeding grounds for them. These heterogeneous habitats must be protected in a sustainable way in order to ensure the continued presence of aquatic and terrestrial fauna species for future generations.

1. Introduction

Mangrove is a salt tolerant plant that occurs within inter-tidal zones where a river enters into the sea, especially in the coastal belt [1,2]. They are a highly productive, tropical coastal ecosystem encompassing estuaries, creeks, lagoons, backwaters, mud-flats, salt-pans and islands which has both great aquatic and terrestrial biodiversity [3] and plays an integral role in coastal ecosystem functions at the interface between terrestrial, freshwater and marine systems [4]. Mangrove fauna are animal communities that inhabit or utilize mangrove habitats, such as coastal inter-tidal zones, estuaries and riverine areas where rivers drain into the sea, to fulfill their need for survival and reproduction [5,6]. The vegetation structure and composition of mangrove areas may vary depending upon soil texture and structure, rainfall pattern, and inflow of freshwater from rivers to the sea [7,2].
Mangrove forests are considered as a highly productive ecosystem, i.e., they provide important ecological and economic services [8,9]. They play a crucial role in providing suitable habitats for fauna, safe breeding and chick rearing grounds, nurseries for a diversity of fishes and shellfishes, as well as ideal foraging grounds for animals such as fishes, birds and aquatic invertebrates and refuge from predators [10]. Mangrove habitats are consistently undervalued, degraded and are being lost at an alarming rate due to human intervention, i.e., coastal development, deforestation, tin mining, urbanization, salt production, conversion into paddy fields and aquaculture ponds, over-harvesting of timber and fuel-wood, pollution, i.e., dumping of domestic sewage and crude oil exploration [2,11,12,13,14].
It has been stated that around 50% of mangrove habitats has been lost and degraded in the past two decades due to human interventions [15,10]. The mangrove habitat loss and degradation have posed major threats to a wide array of fauna [16,17] bringing them among the ranks of endangered and extinct species [2,18,19,20].
Recently, considerable attention has been paid to mangrove fauna diversity and habitat due to their importance and functions [21]. There has been no detailed study undertaken to examine the fauna diversity in Marudu Bay mangrove forest, Sabah, Malaysia. Thus, there was an urgent need to examine the fauna diversity inhabiting mangrove habitats in order to understand the impact of disturbance for future conservation and management.
This current study was aimed at examining the fauna diversity (such as birds, mammals, reptiles, fishes and aquatic invertebrates) inhabiting or utilizing the downstream to upstream mangrove and river tributaries of Marudu Bay. The scientific baseline data obtained from the study would provide an in depth understanding of the current fauna diversity status for better future conservation and management initiatives.

2. Materials and Methods

2.1. Study Site

Marudu Bay mangrove forest is located between latitude 6°15′′ to 6°45′′ N and a longitude of 116° to 117° E, 113 km from Kota Kinabalu Sabah, Malaysia (Figure 1). The forest is still in pristine condition, i.e., >90% intact, spread over several creeks and lagoons and covers an area of 9550 ha. This mangrove forest is managed, in accordance with the principles of conservation and sustainable use, by the Sabah Forest Department, Malaysia. The mangrove forest consists of 16 tree species of 12 genera and nine families, such as Rhizopora apiculata, R. mucronata, Bruguiera parviflora, B. gymnorrhiza and Ceriops decandra. Marudu Bay mangrove forest is rich in fauna diversity, i.e., aquatic invertebrates, fishes, birds, reptiles and mammals. This mangrove forest provides a wide range of ecosystem services such as timber, fuel-wood, fisheries, eco-tourism and nursery habitat for different animals. Marudu Bay mangrove forest is an important source of livelihood for local communities.
Figure 1. Location of the Marudu Bay Mangrove forest Sabah, Malaysia.
Figure 1. Location of the Marudu Bay Mangrove forest Sabah, Malaysia.
Diversity 07 00137 g001

2.2. Fauna Surveys

The presence of birds, mammals, and reptiles was determined by boat using direct observation using 10 × 50 binoculars from 23 March to 3 April 2009, 21–27 May 2009 and 2–8 February 2010. A total of 60 point stations along the three rivers and mudflats was established randomly to cover different habitat types, i.e. from downstream to upstream Marudu Bay mangrove forest. The location of each point station was at intervals of 250 m apart. The main reason for locating point stations 250 m apart was to avoid double counting the same species at more than one station. This was based on the recommendation by [22] who stated this approach was suitable: (i) for dense habitats, such as forest and shrubs; (ii) to survey cryptic, shy, and skulking species; (iii) for the populations that are of higher density and are more species rich; (iv) for situations where access is restricted; and (v) particularly for bird-habitat studies. The survey was conducted by boat along selected streams as it was the easiest way to observe the birds in the mangrove forests early in the morning (between 6:30 a.m. and 7:00 a.m. depending on weather) and to be completed before 12:00 p.m. The methodology followed was developed by [23,24].
The fish fauna were caught through angling rods and cast nets while aquatic invertebrate were collected through swap nets.

3. Results

3.1. Aquatic Invertebrate Fauna

Marudu Bay mangrove habitats were rich in aquatic invertebrate fauna (i.e., 22 species), which comprised crustaceans (crabs, prawns and shrimps), mollusks (snails, clams, periwinkle, murex and oysters) and worms (lug worms, tube worms, eunicid worms and polychaete worms; Table 1).
Table 1. List of aquatic invertebrate species detected in Marudu Bay mangrove habitat.
Table 1. List of aquatic invertebrate species detected in Marudu Bay mangrove habitat.
Family NameCommon NameScientific Name
Crustacean Species
AlpheidaeMangrove Snapping PrawnsAlpheus sp.
GrapsidaeMangrove Root CrabGoniopsis cruentata
LimulidaeHorseshoe Mangrove CrabTachypleus gigas
OcypodidaeOrange-clawed Fiddler CrabUca coarctata
Orange Fiddler CrabUca vocans
Rosy Fiddler CrabUca rosea
PenaeidaeGreasy-back ShrimpMetapenaeus ensis
Banana PrawnPenaeus merguiensis
PortunidaeGiant Mud CrabScylla serrata
SesarmidaeMangrove Tree CrabAratus pisonii
SquillidaeSilver Mantis ShrimpHarpiosquilla harpax
Mollusks Species
CerithiidaeCerith SnailCerithium sp.
CyrenidaeMud ClamPolymesoda erosa
EllobiidaeMangrove Helmet SnailCassidula sp.
LithorinidaeMangrove PeriwinkleLittorina angulifera
MuricidaeMangrove MurexChicoreus capuncinus
OnchidiidaeGrey-footed Mangrove Onch SlugPlatyvindex sp.
OstreidaeMangrove Tree OysterCrassostrea sp.
Worm Species
ArenicolidaeLugwormsArenicola cristata
ChaetopteridaeParchment Tube WormChaetopterus sp.
EunicidaeEunicid WormLysidice sp.
OnuphidaePolychaete wormsDiopatra sp.

3.2. Fish Fauna

Angling rods and cast nets caught a total of 36 fish species belonging to 22 families from mangrove and river tributaries of the Marudu Bay habitats. The findings highlighted that Leiognathidae, Lutjanidae and Sciaenidae were three most abundant fish families based on the number of captured species (i.e., each three fish species) in the study area. In contrast, 12 fish families were recorded as the rarest in the study area, i.e., only one fish species was captured for each family (Table 2).
Table 2. List of fish species captured in Marudu Bay mangrove and river tributaries.
Table 2. List of fish species captured in Marudu Bay mangrove and river tributaries.
Family NameCommon NameScientific Name
AmbassidaeBuru Glass PerchletAmbassis buruensis
Naked-head Glassy PerchletAmbassis gymnocephalus
ApogonidaeHookfin CardinalfishApogon griffini
BelonidaeSpottail Needle FishStrongylura strongylura
Carangidae Hardtail ScadMegalaspis cordyla
Talang QueenfishScomberoides commersonnianus
ChirocentridaeWhitefin Wolf herringChirocentrus nudus
DrepaneidaeConcertina FishDrepane longimana
EleotridaeFlatheaded SleeperOphiocara porocephala
TenpounderElops machnata
EngraulidaeAnchovy FishAnchovia spp.
GerreidaeWhipfin Silver-biddyGerres filamentosus
Silver BiddyGerres erythrourus
GobiidaeMangrove GobyAcentrogobius caninus
Tank GobyGlossogobius giuris
HaemulidaeSaddle GruntPomadasys maculatus
Javelin GruntPomadasys kaakan
HemiramphidaeHalfbeak or GarfishHemiramphus spp.
Leiognathidae Whipfin PonyfishEquulites leuciscus
Spotnape PonyfishNuchequula nuchalis
Shortnose PonyfishLeiognathus brevirostris
LutjanidaeBlack SnapperApsilus dentatus
One Spot SnapperLutjanus monostigma
Mangrove Red SnapperLutjanus argentimaculatus
MegalopidaeIndo-Pacific TarponMegalops cyprinoides
Mugilidae Greenback MulletLiza subviridis
Square-tail MulletLiza vaigiensis
PlotosidaeWhite-lipped Eel CatfishParaplotosus albilabris
ScatophagidaeSpotted ScatScatophagus argus
SciaenidaeGoatee CroakerDendrophysa russelii
Orange Spotted Grouper Epinephelus coioides
Cloudy Grouper FishEpinephelus erythrurus
SiganidaeStreaked Spinefoot FishSiganus javus
Goldlined SpinefootSiganus guttatus
TerapontidaeJarbua TeraponTerapon jarbua
TrichiuridaeLarge-head HairtailTrichiurus lepturus
Very few reptile species were detected during the study. The reptile fauna comprised of crocodiles, monitor lizards and skinks (Table 3).
Table 3. List of reptile species detected at Marudu Bay mangrove river tributaries.
Table 3. List of reptile species detected at Marudu Bay mangrove river tributaries.
Family NameCommon NameScientific Name
CrocodylidaeCrocodileCrocodylus palustris
VaranidaeMangrove Monitor LizardVaranus indicus
Malaysian Water Monitor LizardVaranus salvator
ScincidaeMangrove SkinkEmoia atrocostata

3.3. Bird Fauna

Bird fauna of downstream to upstream mangrove and river tributaries included 74 species representing 33 families. The results showed that Ardeidae (nine bird species), Scolopacidae (six species), Cuculidae and Picidae (each five species) were the four most dominant families in Marudu Bay mangrove habitats. On the contrary, 17 families, i.e., Anhingidae, Apodidae, Artamidae, Campephagidae, Chloropseidae, Ciconiidae, Coraciidae, Dicaeidae, Hemiprocnidae, Hirundinidae, Muscicapidae, Pachycephalidae, Psittacidae, Rhipiduridae, Sittidae, Timaliidae, and Sternidae were the rarest in the study area (i.e., only one species detected for each family. Out of all bird species, six species were endangered, one rare and one nearly threatened (Table 4).
Table 4. List of bird species detected in Marudu Bay Mangrove habitat.
Table 4. List of bird species detected in Marudu Bay Mangrove habitat.
Family NameCommon NameScientific Name
AccipitridaeBrahminy KiteHaliastur indus
White-bellied Fish-EagleHaliaeetus leucogaster
OspreyPandion haliaetus
AlcedinidaeStork-billed KingfisherPelargopsis capensis
Common KingfisherAlcedo atthis
Collared KingfisherHalcyon chloris
White-throated KingfisherHalcyon smymensis
AnhingidaeOriental Darter (E)Anhinga melanogaster
ApodidaeWhite-bellied SwiftletCollocalia esculenta
ArdeidaeLittle EgretEgretta garzetta
Little HeronButorides striatus
Great EgretCasmerodius albus
Intermediate EgretEgretta intermedia
Chinese Egret (E)Egretta eulophotes
Cattle EgretBubulcus ibis
Schrenck's BitternIxobrychus eurhythmus
Yellow BitternIxobrychus sinensis
Rufous Night-HeronNycticorax caledonicus
ArtamidaeWhite-breasted Wood-SwallowArtamus leucorhynchus
CampephagidaePied ThrillerLalage nigra
CharadriidaePacific Golden-PloverPluvialis fulva
Little Ringed PloverCharadrius dubius
Common Ringed PloverCharadrius hiaticula
ChloropseidaeCommon IoraAegithina tiphia
CiconiidaeLesser Adjutant (E)Leptoptilos javanicus
ColumbidaePink-necked Green PigeonTreron vernans
Little Green-PigeonTreron olax
Jambu Fruit-DovePtilinopus jambu
CoraciidaeDollar BirdEurystomus orientalis
CuculidaeBlack-bellied Malkoha (E)Phaenicophaeus diardi
Chestnut-bellied Malkoha (E)Phaenicophaeus sumatranus
Greater CoucalCentropus sinensis
Malayan Bronze CuckooChrysococcyx minutillus
Lesser CoucalCentropus bengalensis
DicaeidaeScarlet-backed FlowerpeckerDicaeum curentatum
EstrilidaeDusky MuniaLonchura fuscans
Black-headed MuniaLonchura articapilla
HemiprocnidaeWhiskered TreeswiftHemiprocne comata
HirundinidaePacific SwallowHirundo tahitica
LaniidaeBar-winged Flycatcher-ShrikeHemipus picatus
Black-winged Flycatcher-ShrikeHemipus hirundinaceus
MeropidaeBlue-tailed Bee-eaterMerops philippinus
Blue-throated Bee-eaterMerops viridus
MuscicapidaeMangrove Blue-FlycatcherCyornis rufigastra
NectariniidaeOlive-backed SunbirdNectarinia jugularis
Plain SunbirdAnthreptes simplex
Brown-throated SunbirdAnthreptes malacensis
Purple-throated SunbirdNectarinia sperata
PachycephalidaeMangrove WhistlerPachycephala grisola
PhalacrocoracidaeGreat Cormorant (R/A)Phalacrocorax carbo
Little CormorantPhalacrocorax niger
PicidaeCommon FlamebackDinopium javanense
Brown-capped WoodpeckerPicoides moluccensis
Speckled PiculetPicumnus innominatus
White-bellied WoodpeckerDryocopus javensis
Maroon WoodpeckerBlythipicus rubiginosus
PsittacidaeBlue-crowned Hanging ParrotLoriculus galgulus
RhipiduridaePied FantailRhipidura javanica
ScolopacidaeCommon RedshankTringa totanus
Nordmann’s Greenshank (E)Tringa guttifer
Grey–tailed Tattler (NT)Tringa brevipes
Common SandpiperTringa hypoleucos
Terek SandpiperXenus cinereus
WhimbrelNumenius phaeopus
SittidaeVelvet-fronted NuthatchSitta frontalis
SturnidaePhilippine Glossy StarlingAplonis panayensis
Hill MynaGracula religiosa
SylviidaeAshy TailorbirdOrthotomus ruficeps
Common TailobirdOrthotomus sutorius
Rufous-tailed TailorbirdOrthotomus sericeus
TimaliidaeStriped Tit-BabblerMacronus gularis
TurdidaeMagpie RobinCopsychus saularis
White-rumped ShamaCopsychus malabaricus
SternidaeWhiskered TernChildonias hybrida
NT = Nearly Threatened; R/A = Rare/Accidental; E = Endangered.

3.4. Mammal Fauna

Only three mammal species belonging to three families were detected during the study period, which include monkeys, pigs and squirrels (Table 5).
Table 5. List of mammal species detected at Marudu Bay mangrove river tributaries.
Table 5. List of mammal species detected at Marudu Bay mangrove river tributaries.
Family NameCommon NameScientific Name
CerocopithecidaeLong-tailed MacaqueMacaca fascicularis
Dusky-leaf MonkeyTrachypithecus obscurus
SuidaeWild PigsSus scrofa
SciuridaePlantain SquirrelCallosciurus notatus

4. Discussion

The recording of a higher diversity of avian, fish, reptile, mammal and aquatic invertebrate species illustrated that Marudu Bay mangrove and river tributary habitats had attracted a wide array of fauna species. It has been stated that mangrove habitats may harbor a wide range of animals such as birds, mammals, reptiles, fishes, and aquatic invertebrates [25,26,27,28]. The presence of a higher diversity of fauna could be due to the habitat’s pristine condition (i.e., no disturbance), complex vegetation structure and composition [29,30], the availability and richness of food resources such as fish, polychaetes, mollusks, crabs, and crustaceans [31,32,33] and low predation risk [25]. The vegetation structure and composition, occurrence of mudflat and richness of food resources are the major driving factors that influence the distribution and diversity of animals directly or indirectly. Vegetation heterogeneity abundance of food resources and habitat diversity may increase avian richness and diversity [34,35]; i.e. they provide suitable foraging and chick rearing grounds, and protection from harsh weather and predators [2].
The recording of a higher number of fish species illustrated that Marudu Bay mangrove areas serve as a nursery ground for various juvenile fish communities [36,37,38,39,40]. It may be that these areas are rich in invertebrate assemblages such as crustaceans (crabs, prawns and shrimps), mollusks (snails, clams, periwinkle, murex and oysters) and worms (lugworms, tube worms, eunicid worms and polychaete worms). In addition, the extensive root systems of mangroves create habitat heterogeneity and complexity, offering suitable foraging sites for juvenile fishes and protecting them from predators by reducing their visibility [32,33]. Habitat heterogeneity and complexity is a major factor that influences fauna diversity and distribution [6,41,42,43].
The sampling of a higher number of aquatic invertebrate species—i.e., 22 species including crustacean, mollusk, periwinkle, murex and worm species—indicated that the Marudu Bay mangrove and river tributary habitats are rich in organic food material that created suitable habitats for them. The presence of the high diversity of invertebrates could also be due to the availability of sheltered beaches and tidal mudflats, which are rich in organic matter. It has been stated that aquatic invertebrates such as periwinkle inhabit the bottom of mudflats (periwinkle—Tympanotonus fuscatus, oysters—Crassostrea sp., mangrove crab—Goniopsis sp., mud crab—Panopeus sp., land crab—Cardiosoma sp.) [44]. Mangrove aquatic invertebrates are a major dietary component of birds, fishes and even other invertebrates.
The recording of sufficient numbers of threatened, nearly threatened and rare bird species such as Oriental Darter, Chinese Egret, Lesser Adjutant, Black-bellied Malkoha, Nordmann’s Greenshank, and Grey–tailed Tattler shows that Marudu Bay mangrove forest is potentially vital habitat for a wide array of avian species. These avian species utilize these areas as an important wintering ground, i.e., they fulfill their daily requirements such as habitat, water and food and also protection from predators and harsh weather. These endangered avian species has become threatened from habitat loss and destruction due to conversion of mangrove areas into oil palm plantation and coastal development. The habitat loss and degradation has seriously affected on their population. For their continuous survival and existence, they need special attention for protection and conservation.

5. Conclusion

Based the results of this study, it is concluded that Marudu Bay mangrove forest, Sabah, Malaysia, must be protected in a sustainable way in order to protect its diverse aquatic and terrestrial fauna species for future generations.

Author Contributions

Mohamed Zakaria Reviewed and edited the manuscript.
Muhammad Nawaz Rajpar Developed the experimental design, Collected and analyzed the data and wrote the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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MDPI and ACS Style

Zakaria, M.; Rajpar, M.N. Assessing the Fauna Diversity of Marudu Bay Mangrove Forest, Sabah, Malaysia, for Future Conservation. Diversity 2015, 7, 137-148. https://doi.org/10.3390/d7020137

AMA Style

Zakaria M, Rajpar MN. Assessing the Fauna Diversity of Marudu Bay Mangrove Forest, Sabah, Malaysia, for Future Conservation. Diversity. 2015; 7(2):137-148. https://doi.org/10.3390/d7020137

Chicago/Turabian Style

Zakaria, Mohamed, and Muhammad Nawaz Rajpar. 2015. "Assessing the Fauna Diversity of Marudu Bay Mangrove Forest, Sabah, Malaysia, for Future Conservation" Diversity 7, no. 2: 137-148. https://doi.org/10.3390/d7020137

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