No. 4/2008
ISSN 1823-3902
Research Article
Floral survey of Laiban sub-watershed in the Sierra Madre Mountain Range in
the Philippines
Karl L. VILLEGAS and Filiberto A. POLLISCO ........................................................................
1
Research Article
Diversity of gingers at Serudong, Sabah, Malaysia
Januarius GOBILIK ....................................................................................................................
15
23
Research Article
Horizontal distribution of intertidal nematode from Sabah, Malaysia
SHABDIN Mohd. Long and OTHMAN Haji Ross.......................................................................
39
Research Article
Stand structure and tree composition of Timbah Virgin Jungle Reserve, Sabah, Malaysia
Januarius GOBILIK ....................................................................................................................
55
Research Article
Preliminary molecular phylogeny of Bornean Plagiostachys (Zingiberaceae)
based on DNA sequence data of internal transcribed spacer (ITS)
Avelinah JULIUS, Monica SULEIMAN and Atsuko TAKANO ...................................................
67
Research Article
Bats (chiropteran) recorded with Aspergillus species from Kubah National Park,
Sarawak, Malaysia
JAYA SEELAN Sathiya Seelan,Faisal Ali ANWARALI KHAN,
SEPIAH Muid and M.T. ABDULLAH .........................................................................................
81
Short Notes
Rapid assessment on the abundance of bird species utilising the
Kota Kinabalu Wetland Centre Mangroves, Sabah, Malaysia
Andy Russel MOJIOL, AFFENDY Hassan, Jocelyn MALUDA
and Suzen IMMIT ........................................................................................................................
99
Short Communication
A preliminary study on the morphometrics of the Bornean Elephant
NURZHAFARINA Othman, MARYATI Mohamed, Abdul Hamid AHMAD, Senthivel NATHAN,
Heather Thomas PIERSON and Benoit GOOSSENS ..................................................................
109
Checklist
A preliminary survey on the butterfly fauna of Sungai Imbak Forest Reserve,
a remote area at the centre of Sabah, Malaysia
Mohd. Fairus JALIL, Hairul Hafiz MAHSOL, Nordin WAHID and
Abdul Hamid AHMAD ................................................................................................................
115
ISSN 1823-3902
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No. 4/2008
Research Article
Biodiversity assesment in a Sarawak lowland dipterocarp rainforest of Niah
National Park
Faisal Ali ANWARALI KHAN, Mohamad Faishal BUJANG, Mohd. Azmin KASSIM,
YAP Sheau Yuh, Besar KETOL, Wahap MARNI, Isa SAIT, C.J. LAMAN,
Abang Arabi ABG AIMRAN, Zaidi MAWEK, Abang Abdul Mutalib ABG TAJUDIN,
Haidar ALI and M.T. ABDULLAH ..............................................................................................
Journal of Tropical Biology and Conservation
Journal of Tropical Biology and Conservation
No. 4/2008
ISSN 1823-3902
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CONTENTS
No. 4/2008
Research Article
Floral survey of Laiban sub-watershed in the Sierra Madre Mountain Range in
the Philippines
Karl L. VILLEGAS and Filiberto A. POLLISCO .......................................................................
1
Research Article
Diversity of gingers at Serudong, Sabah, Malaysia
Januarius GOBILIK .......................................................................................................................
15
Research Article
Biodiversity assesment in a Sarawak lowland dipterocarp rainforest of Niah
National Park
Faisal Ali ANWARALI KHAN, Mohamad Faishal BUJANG, Mohd. Azmin KASSIM,
YAP Sheau Yuh, Besar KETOL, Wahap MARNI, Isa SAIT, C.J. LAMAN,
Abang Arabi ABG AIMRAN, Zaidi MAWEK, Abang Abdul Mutalib ABG TAJUDIN,
Haidar ALI and M.T. ABDULLAH ................................................................................................
23
Research Article
Horinzontal distribution of intertidal nematode from Sabah, Malaysia
SHABDIN Mohd. Long and OTHMAN Haji Ross.....................................................................
39
Research Article
Stand structure and tree composition of Timbah Virgin Jungle Reserve, Sabah, Malaysia
Januarius GOBILIK .......................................................................................................................
55
Research Article
Preliminary molecular phylogeny of Bornean Plagiostachys (Zingiberaceae)
based on DNA sequence data of internal transcribed spacer (ITS)
Avelinah JULIUS, Monica SULEIMAN and Atsuko TAKANO ...............................................
67
Research Article
Bats (chiropteran) recorded with Aspergillus species from Kubah National Park,
Sarawak, Malaysian
JAYA SEELAN Sathiya Seelan, Faisal Ali ANWARALI KHAN,
SEPIAH Muid and M.T. ABDULLAH .......................................................................................
81
Short Notes
Rapid assessment on the abundance of bird species utilising the
Kota Kinabalu Wetland Centre Mangroves, Sabah, Malaysia
Andy Russel MOJIOL, AFFENDY Hassan, Jocelyn MALUDA
and Suzen IMMIT ...........................................................................................................................
99
Short Communication
A preliminary study on the morphometrics of the Bornean Elephant
NURZHAFARINA Othman, MARYATI Mohamed, Abdul Hamid AHMAD,
Senthivel NATHAN, Heather Thomas PIERSON and Benoit GOOSSENS ........................
109
Checklist
A preliminary survey on the butterfly fauna of Sungai Imbak Forest Reserve,
a remote area at the centre of Sabah, Malaysia
Mohd. Fairus JALIL, Hairul Hafiz MAHSOL, Nordin WAHID and
Abdul Hamid AHMAD .............................................................................................................
115
JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 1 – 14, 2008
Research Article
Floral survey of Laiban sub-watershed in the Sierra Madre Mountain Range
in the Philippines
Karl L. VILLEGAS1, 3 and Filiberto A. POLLISCO 2, 4, Jr.
1
Cagayan Valley Programme on Environment and Development,
Isabela State University, Cabagan Isabela 3328, Philippines
2
Environmental Science Institute, Miriam College,
Loyola Heights, Quezon City 1101, Philippines
3
Institute of Environmental Sciences, Leiden University,
2300 RA Leiden, The Netherlands
4
ASEAN Centre for Biodiversity, University of the Philippines
Los Banos, College, Laguna 4031, Philippines
ABSTRACT
The Laiban sub-watershed is part of the Kaliwa
watershed nestled in the Sierra Madre Mountain
Range in Luzon Island, Philippines. The
watershed was identified as one of the 14
priority biodiversity conservation sites within
the Sierra Madre Biodiversity Corridor. This
study presents the results of the vegetation
survey, which aimed to characterize various
vegetation types and determine species
richness and composition. Endangered, rare and
endemic species were also identified. Land uses
were surveyed and representative vegetation
types were selected using patch and quadrat
sampling techniques. Existing trail systems
served as transect lines in conducting the rapid
vegetation assessment during the transect walk.
A total of 121 species belonging to 102 genera
and 56 families were recorded during the
survey. Of the 121 species recorded, 20% of
these were endemics. Indigenous species
Keywords: Plant Survey, Laiban, Kaliwa Watershed,
Sierra Madre
comprised about 53% while exotic species was
27%. Many of the abundant and common
plants were exotics and indigenous species,
which comprised majority of the total species
recorded. The endangered species consisted
only 4% of the total species recorded. The
vegetation types identified were: 1) secondary
forests that are scattered in patches along the
slopes; 2) grassland, which could be seen with
distinct boundaries; 3) plantation forest; and
4) bamboo (Schizostachyum lumampao) that
may be the dominant vegetation. The subwatershed is degraded and characterized by the
presence of kaingin areas, grasslands, Buho
bamboo (S. lumampao) and fragmented
patches of secondary forests and brushland
mosaics.
INTRODUCTION
The Philippines is considered as one of the
mega-biodiversity hotspots in the world (World
Bank, 2004). A biodiversity hotspot is defined
as “an area featuring exceptional
2
FLORAL SURVEY OF LAIBAN IN SIERRA MADRE
concentrations of endemic species and
expressing exceptional loss of habitat” (Myers
et al., 2000). In the Philippines, there are over
6,000 endemic species with 80% of forest cover
loss over the last century. It is no wonder that
the country is a mega-biodiversity hotspot.
One of the major biogeographic regions in the
country is the Sierra Madre Mountain Range.
In the southeastern portion of the range, the
Kaliwa Watershed forms part of the Sierra
Madre Biodiversity Corridor (SMBC). This
watershed including its microbasin, the Laiban
sub-watershed, was recently identified as one
of the 14 priority biodiversity conservation sites
within the SMBC (Miriam College, 2004). On
the other end, there has been increasing
interest in this sub-watershed as an alternative
water source for Metro Manila residents.
The Kaliwa Watershed has been widely
studied, but previous studies have been
devoted mainly in other sites. To date, there
has been no documented survey conducted in
the Laiban sub-watershed. This study was
designed to generate baseline information on
the vegetative types and composition of the
sub-watershed; and to identify the
conservation status of plant species in the area.
MATERIALS AND METHODS
The study site is the Laiban sub-watershed,
which serves as an important microbasin of the
bigger Kaliwa Watershed, nestled in the Sierra
Madre Mountain Range. It is located in the east
of Metro Manila in the district (Barangay) of
Laiban, municipality of Tanay in the province
of Rizal, the Philippines (Fig. 1). The village
Project Site
Legend
Luzon Island
Tree cover broadleaved evergreen
Inland water
0
25
50
Figure 1: Location of the study site in Barangay Laiban
100 kilometres
3
KARL L.VILLEGAS & FILIBERTO A. POLLISCO
community in the site belongs to the
indigenous people called the Dumagats and
Remontados. The sub-watershed is a 180 ha
area which is generally characterized by
mountainous terrain with steep slopes in all
sides. This consisted of cultivated land and
forested hills with slash and burn cultivation
(kaingin) areas present in the cup of the
inverted U-shape (Fig. 2) and along the lower
slopes of the study site. Some small creeks run
through the lower slopes and connect to the
main river beyond the village.
The Kaliwa Watershed was classified as a forest
reserve and a portion of the watershed was
declared as a National Park and Wildlife
Sanctuary. At present, the Kaliwa Watershed
is reclassified as a protected area under the
National Integrated Protected Areas System
(REECS, 1999 as cited in Miriam College, 2004).
However, the area is considered degraded due
to anthropogenic pressures. Upland farms or
kaingin areas were mainly established by the
indigenous people.
The vegetation survey of the sub-watershed
was conducted from February to May 2005. The
Patch Sampling Technique (Ohsawa, 1991; Rice
& Lambshead, 1994) was used based on
identified land uses and survey objectives. This
approach uses the selection of patches as a
landscape element to determine the vegetation
composition. Nested plots using the Quadrat
Sampling Method (QSM) were laid out within
patches of vegetation to gather biological data.
Sampling plots measuring 20 m × 20 m were
established to identify vegetation in the canopy
stratum; 5 m × 5 m for the intermediate
vegetation; and 1 m × 1 m quadrats for the
ground vegetation. The transect walk method
was also done for the rapid vegetation
assessment using the existing trail system
covering most of the area. The sampling plots
and transect walk site are as shown in Figure 2.
1
4
Tower
2
3
Transect Walk Site
0 0.25 0.5
1 kilometres
Figure 2: Location of sampling plots and transect walk in the sub-watershed
4
The identification of plant species was done
through referral to literatures and specimen
verification at the herbarium laboratory of the
College of Forestry and Natural Resources in
University of the Philippines Los Banos. The
International Plant Name Index website
(www.ipni.org) was consulted in verifying the
names of plant taxa. In addition, the 2004 IUCN
Red List of Threatened Species
(www.iucnredlist.org) also served as an online
information database in checking the
conservation status of plants.
RESULTS AND DISCUSSION
A study on floral diversity was previously
conducted in other areas of the Kaliwa
Watershed (DENR, 2005). This characterized
the bigger watershed into various community
types such as Imperata stand, Saccharum
stand, bamboo thicket and shrubland
vegetation. For this study, the vegetation type
and composition of the Laiban sub-watershed
were surveyed and characterized.
The Laiban sub-watershed was degraded and
characterized by the presence of kaingin areas,
grasslands, Buho bamboo (S. lumampao) and
patches consisting of secondary forests and
brushlands. The kaingin areas were mostly
devoid of trees and made up of agricultural
crops such as Manihot esculenta, Arachis
hypogaea, Zea mays and Citrus sp. The plants
outside the kaingin area were mostly grasses
and small shrubs.
The vegetation types identified during the
survey were: 1) secondary forests that are
scattered in patches along the slopes;
2) grassland, which could be seen with distinct
boundaries; 3) plantation forest; and 4) bamboo
(S. lumampao) that may be the dominant
vegetation.
The secondary forest is situated on the
midslopes of the site just above the kaingin
area tilled by the ‘Chieftain’ of the indigenous
FLORAL SURVEY OF LAIBAN IN SIERRA MADRE
people. The elevation is recorded at 290 m asl
along a west-facing slope. Six medium-sized
trees were recorded in the canopy vegetation
of the sampling plot. These included Ficus gul,
Strombosia philippinensis, Ficus nota,
Leucaena leucocephala, Artocarpus ovatus
and Buchanania nitida. All of these species
usually thrive along slopes near tributaries,
except for L. leucocephala, which could also
persist in the other surrounding habitat types,
e.g. brushlands. Ten species were identified in
the intermediate vegetation. These were
Alphonsea arborea, Myristica philippinensis,
S. philippinensis, Bridelia penangiana,
Hedyachras philippinensis, Terminalia
foetidissima,
Pisonia
umbellifera,
Gomphandra luzoniensis, Dinochloa
acutiflora and Leea aculeata. There were only
six species recorded at the ground level. These
included the Aglaonema sp., Curculigo
capitulate, L. aculeata, Centrosema
pubescens, Mikania cordata and Donax
cannaeformis. Other species were recorded
during the transect walk within the secondary
forest and brushland mosaic (Table 1).
The grassland vegetation (160 m asl) is
dominated by the grass species, Imperata
cylindrica. The tree species found in the area
are sparse. However, there were still three
species recorded such as Antidesma
ghaesembilia, Bauhinia malabaricum and
Gmelina arborea. The former two species are
both indigenous and naturally growing in the
area. They are quite common in grassland
vegetation throughout the Sierra Madre
Mountain Range. Gmelira arborea, on the
other hand is introduced, as an attempt on
reforesting the area. There were six species
representing the intermediate stratum as
follows: Melastoma malabathricum,
Cananga odorata, Cratoxylon formosum,
A. ghaesembilia, B. malabaricum and Psidium
guajava. The ground vegetation consisted only
of two species, I. cylindrica and C. odorata.
KARL L.VILLEGAS & FILIBERTO A. POLLISCO
At almost 500 m asl, the grassland vegetation
in the ridge is slightly different from the
grassland found in the lower altitude. Different
vegetative composition was observed except
for the common presence of I. cylindrica. There
were six tree species recorded which were the
Ficus septica, Ficus nota, Macaranga
tanarius, Cordia dichotoma, F. gul and
Acalypha stipulacea. The presence of Ficus
trees in this grassland is unusual, however,
these species have also been recorded in high
elevation mossy forest types in the Bicol
Region (Pollisco, 2002). Other species included
in the sampling plot were six pioneer species.
These were the Lantana camara, D.
cannaeformis, C. odorata, Saccharum
spontaneum and two vine species. No species
were recorded in the ground layer because
honey gatherers sporadically burned the area.
This demonstrated that anthropogenic
pressures are being exerted aside from the
kaingin activities found in the lower slopes.
At 180 m asl, the plantation forest is
characterized by more or less evenly spaced
trees. There were only three dominant species
of trees, Swietenia macrophylla, Acacia
auriculiformes and G. arborea. The
intermediate vegetation consisted of mostly
indigenous species. These included
Buchanania arborescens, Semecarpus
cuneiformis,
Guioa
koelreuteria,
Pterospermum celebicum, Pittosporum
pentandrum and Hibiscus tiliaceus. In the
undergrowth, only four species were recorded.
These were the Chromolaena odorata,
Lygodium flexuosum, M. malabathricum and
Leukosyke capitallata. Chromolaena odorata
and M. malabathricum are both exotics.
The Buho (S. lumampao) bamboo represents
another vegetation type occupying a large
portion of the site. On the other hand, they are
subjected to the kaingin practice of the local
people, hence, most of these are being cut down
and burned to make way for cash crops. Being
5
a grass species, the Buho bamboo is able to
reestablish during the period when the local
people shift to another adjacent area and the
cycle starts all over again.
A total of 121 species belonging to 102 genera
and 56 families were recorded. Table 1 shows
the checklist of vegetation found in Laiban
sub-watershed.
The site harboured about eight plant habits or
form. Out of 121 species documented, 69 were
tree species, 17 shrubs, nine herbs, seven vines,
six grasses, five palms and four species for both
bamboo and fern. There were no large trees
found in the area, however, there were tree
species that belong to the large size category
such as the Koordersiodendron pinnatum and
Shorea contorta. Another large tree was the
Albizzia acle. All of three species belong to
the endangered species list under the CITES
(PAWB-DENR, 2000) and IUCN (2004), though
with varying conservation status. Many of the
shrubs were less than a metre tall which
occupied the ground stratum. Most of these
were found in open areas such as
Stachytarpheta jamacaensis, Moghania
strobilifera and Mussaenda sp. The fern plants
were mostly located in the upper slopes
adjacent to water sources or where there is high
moisture and shade.
Endemicity is defined as the state of having
limited geographic range, which could be
confined to an area or to a country (Williams et
al., 1996). Some species in the watershed were
classified as endemics, either within the Sierra
Madre Mountain Range or as country endemic.
Of the 121 species recorded, 20% or 24 of these
were endemics. The proportion of endemics to
exotic and indigenous species is shown in
Figure 3. Examples of these endemic
species were A. acle, Artocarpus blancoi,
S. philippinensis and M. philippinensis.
6
Table 1: List of vegetation found during the survey in Laiban sub-watershed
SCIENTIFIC
NAME
PLANT
HABIT
VEGETATION TYPE
ENCOUNTERED
ECOLOGICAL CONSERVATION
STATUS
STATUS
Acanthaceae
Pachystachys lutea
Nees
Cordyline fruticosa (L.)
A. Chev.
shrub
plantation forest
exotic
common
shrub
plantation forest
exotic
abundant
large tree
plantation forest
indigenous
depleted
medium to large tree
grassland, plantation forest
indigenous
depleted
small to medium tree
small to medium tree
indigenous
indigenous
rare
depleted
exotic
abundant
endemic
indigenous
rare
endangered
Agavaceae
Anacardiaceae
Koordersiodendron pinnatum
(Blanco) Merr.
Buchanania arborescens (Blume)
Blume
Buchanania nitida Engl.
Semecarpus cuneiformis Blanco
Mangifera indica L.
large tree
Annonaceae
Platymitra arborea (Blanco) Kesler
Cananga odorata (Lamk.) Hook.f.
& Thoms.
large tree
medium tree
plantation/secondary forest
plantation/secondary
forest/brushland mosaic
plantation/secondary
forest/brushland mosaic
secondary forest
secondary forest
Apocynaceae
Alstonia parvifolia Merr.
small tree
grassland, plantation forest
endemic
depleted
Araceae
Aglaonema commutatum Schott
Colocasia esculentum (L.) Schott
herb
herb
secondary forest
secondary forest
indigenous
exotic
common
abundant
Araliaceae
Polyscias nodosa (Blume) Seem.
medium tree
plantation/secondary
forest/brushland mosaic
indigenous
depleted
Arecaceae
Areca catechu L.
palm
secondary forest/
brushland mosaic
endemic
common
FLORAL SURVEY OF LAIBAN IN SIERRA MADRE
FAMILY
NAME
SCIENTIFIC
NAME
PLANT
HABIT
VEGETATION TYPE
ENCOUNTERED
ECOLOGICAL
STATUS
CONSERVATION
STATUS
Arecaceae
Arenga pinnata (Wurmb) Merr.
palm
indigenous
common
Veitchia merrillii Becc. H.E. Moore
Cocos nucifera L.
palm
palm
endemic
exotic
abundant
abundant
Calamus merrillii Becc.
rattan
secondary forest/
brushland mosaic
plantation forest
plantation/secondary forest
brushland mosaic
plantation/secondary forest
brushland mosaic
endemic
endangered
Aspleniaceae
Asplenium musaefolium Mett.
fern
secondary forest
indigenous
common
Asteraceae
Crassocephalum crepidioides
(Benth.) S. Moore
Chromolaena odorata (L.) R.M.
King & M. Robinson
Mikania cordata (Burm. f.) B.L. Rob.
shrub
plantation forest
indigenous
common
shrub
exotic
common
vine
grassland/ridge grassland,
plantation forest
secondary forest
exotic
common
Bombacaceae
Ceiba pentandra (L.) Gaertn.
large tree
ridge grassland
exotic
common
Boraginaceae
Cordia dichotoma G. Forst.
small tree
ridge grassland
indigenous
depleted
Burseraceae
Canarium asperum Benth. ssp.
asperum var. asperum
large tree
plantation forest
indigenous
depleted
Clusiaceae
Cratoxylum formosum (Jack)
Dyer ssp. Formosum
small tree
grassland, plantation forest
indigenous
depleted
Combretaceae
Terminalia foetidissima Griff.
large tree
plantation/secondary forest
endemic
depleted
Convulvulaceae
Ipoemoea batatas (L.) Lamk
vine
secondary forest
indigenous
abundant
Cyperaceae
Cyperus rotundus L.
Cyperus sp.
sedge
sedge
plantation forest
plantation forest
indigenous
indigenous
common
common
KARL L.VILLEGAS & FILIBERTO A. POLLISCO
FAMILY
NAME
7
8
SCIENTIFIC
NAME
PLANT
HABIT
VEGETATION TYPE
ENCOUNTERED
ECOLOGICAL CONSERVATION
STATUS
STATUS
Datiscaceae
Octomeles sumatrana Miq.
large tree
ridge grassland
indigenous
indeterminate
Dipterocarpaceae
Shorea contorta Vidal
large tree
secondary forest/
brushland
endemic
critically
endangered
Euphorbiaceae
Homonoia riparia Lour.
Neotrewia cumingii (Muell.-Arg.)
Pax & K. Hoffm.
Antidesma ghaesembilla Gaertn. var.
ghaesembilla
small tree
small tree
ridge grassland
secondary forest
indigenous
endemic
common
depleted
small tree
indigenous
common
Macaranga tanarius (L.) Muell.-Arg.
small tree
indigenous
abundant
Acalypha amentacea Roxb.
Manihot esculenta Crantz
Macaranga bicolor Muell.-Arg.
Aleurites moluccana (L.) Willd.
Codiaeum variegatum (L.) Blume
Bridelia penangiana Hook. f.
small tree
shrub
small to medium tree
large tree
small tree
small tree
grassland, plantation/
secondary forest/
brushland mosaic
ridge grassland, secondary
forest/brushland mosaic
ridge grassland
plantation forest
secondary forest
plantation forest
plantation forest
secondary forest
indigenous
exotic
endemic
exotic
exotic
indigenous
common
abundant
vulnerable
abundant
common
depleted
Bauhinia malabarica Roxb.
small tree
indigenous
abundant
Centrosema pubescens Benth.
Calopogonium mucunoides Desv.
vine
vine
grassland, secondary
forest/brushland mosaic
secondary forest
plantation forest
exotic
exotic
common
common
Pterocarpus indicus Willd. Forma
indicus
large tree
plantation forest
indigenous
endangered
Flemingia strobilifera (L.)
Roxb. ex W. Aiton
Samanea saman (Jacq.) Merr.
vine
plantation forest
indigenous
common
large tree
plantation forest
exotic
abundant
Flacourtiaceae
Flacourtia jangomas (Lour.) Raeusch.
small tree
plantation forest
exotic
common
Heliconiaceae
Heliconia psittacorum L.f.
herb
plantation forest
exotic
abundant
Fabaceae
Fabaceae
FLORAL SURVEY OF LAIBAN IN SIERRA MADRE
FAMILY
NAME
PLANT
HABIT
VEGETATION TYPE
ENCOUNTERED
ECOLOGICAL CONSERVATION
STATUS
STATUS
Hypoxidaceae
Curculigo capitulata (Lour.)
O. Kuntze
herb
secondary forest,
ridge grassland
indigenous
common
Icacinaceae
Gomphandra luzoniensis (Merr.)
Merr.
medium tree
secondary forest
endemic
indeterminate
Leeaceae
Leea aculeata Blume ex Spreng.
small tree
secondary forest/
brushland mosaic
indigenous
common
Malvaceae
Hibiscus rosasinensis L.
Urena lobota L.
Hibiscus tiliaceus L.
Rubus sp.
small tree
shrub
small tree
small tree
plantation forest
plantation forest
plantation forest
ridge grassland
exotic
exotic
indigenous
indigenous
abundant
common
common
depleted
Marantaceae
Donax cannaeformis (Forst.)
K. Schum
herb
secondary forest/brushland
mosaic, ridge grassland
indigenous
rare
Melastomataceae
Melastoma malabathricum L.
shrub
grassland, plantation forest indigenous
common
Meliaceae
Swietenia mahogani (L.) Jacq.
large tree
exotic
endangered
Dysoxylum cumingianum C. DC.
small to medium tree
plantation/secondary
forest/brushland mosaic
secondary forest
indigenous
depleted
Albizia acle (Blanco) Merr.
medium to large tree
Acacia auriculiformis A. Cunn.
small to medium tree
ex. Benth
Leucaena leucocephala (Lam.) de Wit small tree
Mimosa pudica L.
shrub
plantation forest
plantation forest
endemic
exotic
depleted
abundant
secondary forest
plantation forest
exotic
exotic
abundant
common
Artocarpus blancoi (Elmer) Merr.
large tree
endemic
vulnerable
Artocarpus ovatus Blanco
Ficus gul Laut. et K. Schum. var. gul
small tree
small tree
endemic
indigenous
abundant
depleted
Ficus septica Burm. F. var. septica
small tree
plantation/secondary
forest
secondary forest
secondary forest, ridge
grassland
secondary forest, ridge
grassland
indigenous
common
Mimosaceae
Moraceae
9
SCIENTIFIC
NAME
KARL L.VILLEGAS & FILIBERTO A. POLLISCO
FAMILY
NAME
PLANT
HABIT
VEGETATION TYPE
ENCOUNTERED
ECOLOGICAL CONSERVATION
STATUS
STATUS
Moraceae
Ficus ulmifolia Lam.
Artocarpus heterophyllys Lamk.
Ficus congesta Roxb. var. congesta
Ficus pseudopalma Blanco
Ficus odorata (Blanco) Merr.
Artocarpus communis J.R. & G. Forst.
Ficus variegata Blume var. variegate
Ficus nota (Blanco) Merr.
small tree
small to medium tree
medium tree
small tree
small to medium tree
large tree
large tree
small tree
secondary forest
plantation forest
plantation forest
grassland, secondary forest
secondary forest
plantation forest
plantation forest
plantation/secondary
forest, ridge grassland
endemic
exotic
indigenous
endemic
endemic
exotic
indigenous
indigenous
vulnerable
abundant
depleted
common
depleted
common
common
common
Moringaceae
Moringa oleifera Lamk.
small tree
plantation forest
exotic
abundant
Musaceae
Musa textiles Nees
Musa sapientum L.
herb
herb
secondary forest
plantation forest
indigenous
exotic
abundant
abundant
Myristicaceae
Myristica philippinensis Lam.
medium tree
secondary forest
endemic
vulnerable
Myrsinaceae
Ardisia squamulosa Presl
small tree
plantation/secondary forest endemic
vulnerable
Myrtaceae
Psidium guajava L.
Syzygium cumini (L.) Skeels
Syzygium calubcob (C.B.Rob) Merr.
small tree
medium tree
medium tree
grassland
ridge grassland
secondary forest/
grassland mosaic
exotic
indigenous
indigenous
abundant
abundant
indeterminate
Nyctaginaceae
Pisonia umbellifera (Forst.) Seem.
small tree
secondary forest
indigenous
indeterminate
Olacaceae
Strombosia philippinensis
(Baill.) Rolfe
medium tree
secondary forest
endemic
depleted
Passifloraceae
Passiflora foetida L.
vine
ridge grassland
exotic
common
Pittosporaceae
Pittosporum pentandrum
(Blanco) Merr.
small tree
plantation/secondary
forest/brushland mosaic
indigenous
indeterminate
FLORAL SURVEY OF LAIBAN IN SIERRA MADRE
SCIENTIFIC
NAME
10
FAMILY
NAME
SCIENTIFIC
NAME
PLANT
HABIT
VEGETATION TYPE
ENCOUNTERED
ECOLOGICAL CONSERVATION
STATUS
STATUS
Poaceae
Dinochloa acutiflora (Munro)
S. Dransf.
Schizostachyum lumampao
(Blanco) Merr.
Bambusa merrilliana (Elmer)
Rojo & Roxas
Imperata cylindrica (L.) Beauv.
bamboo
secondary forest
indigenous
common
bamboo
plantation forest
endemic
common
bamboo
secondary forest/
brushland mosaic
grassland/ridge grassland,
plantation forest
indigenous
rare
indigenous
abundant
Zea mays L.
Saccharum spontaneum L.
grass
grass
plantation forest
grassland/ridge grassland
exotic
indigenous
abundant
abundant
Polygalaceae
Xanthophyllum vitellinum
(Blume) Dietr.
small tree
ridge grassland
indigenous
indeterminate
Polypodiaceae
Diplazium esculentum (Retz.) Sw.
fern
indigenous
common
Nephrolepis sp.
fern
indigeneous
common
Rosaceae
Prunus grisea (Blume) Kalkm.
var. grisea
small to medium tree
secondary forest, ridge
grassland
plantation/secondary
forest/brushland mosaic,
ridge grassland
secondary forest
indigenous
indeterminate
Rubiaceae
Nauclea orientalis (L.) L.
Neonauclea auriculata Quis. &
Merr.
Mussaenda philippica A. Rich. var.
aurorae Sul.
medium to large tree
plantation forest
indigenous
depleted
small tree
plantation forest
indigenous
common
Rubiaceae
Psychotria luzoniensis (Cham. &
Schlecht.) F. -Vill.
small tree
secondary forest
indigenous
common
Rutaceae
Micromelum inodorum (Blanco) Tan.
Micromelum compressum
(Blanco) Merr.
small tree
small tree
secondary forest
secondary forest/
brushland mosaic
indigenous
indigenous
indeterminate
indeterminate
grass
KARL L.VILLEGAS & FILIBERTO A. POLLISCO
FAMILY
NAME
11
12
SCIENTIFIC
NAME
Sapindaceae
Guioa koelreuteria (Blanco) Merr.
small tree
Glenniea philippinensis (Radlk.) Leenh. small to medium tree
plantation/secondary forest endemic
secondary forest
endemic
rare
rare
Sapotaceae
Chrysophyllum cainito L.
medium tree
plantation forest
exotic
common
Schizaeaceae
Lygodium japonicum Sw.
fern
indigenous
common
Lygodium circinnatum (Burm. f.) Sw.
fern
secondary forest/
brushland mosaic
plantation/secondary
forest/brushland mosaic
indigenous
common
Pterospermum niveum Vidal
small tree
indigenous
depleted
Pterospermum obliquum Blanco
small tree
plantation/secondary
forest/brushland mosaic
secondary forest/
brushland mosaic
indigenous
depleted
Tiliaceae
Diplodiscus paniculatus Turcz.
medium tree
secondary forest
endemic
vulnerable
Ulmaceae
Celtis luzonica Warb.
large tree
secondary forest
endemic
vulnerable
Urticaceae
Leucosyke capitellata (Poir.) Wedd.
small tree
plantation forest
indigenous
indeterminate
Verbenaceae
Premna odorata Blanco
Gmelina arborea Roxb.
Stachytarpheta jamaicensis (L.) Vahl.
Lantana camara L.
small tree
large tree
shrub
shrub
indigenous
exotic
exotic
exotic
abundant
abundant
common
common
Clerodendrum bethunianum
small tree
plantation forest
grassland, plantation forest
plantation forest
plantation/secondary
forest/brushland mosaic,
ridge grassland
ridge grassland
indigenous
common
Kolowratia elegans Presl.
herb
secondary forest, ridge
grassland
endemic
common
Sterculiaceae
Zingiberaceae
PLANT
HABIT
VEGETATION TYPE
ENCOUNTERED
ECOLOGICAL CONSERVATION
STATUS
STATUS
FLORAL SURVEY OF LAIBAN IN SIERRA MADRE
FAMILY
NAME
13
KARL L.VILLEGAS & FILIBERTO A. POLLISCO
20%
Indigenous
Exotic
Endemic
53%
27%
Figure 3: Proportion of ecological status of species in the Laiban sub-watershed
The endangered species consisted only 4%
of the total species listed in the sampling area
(Table 2). These endangered species were
C. odorata, Pterocarpus indicus, Calamus
merrillii, S. contorta and S. macrophylla.
Most of these are listed in the IUCN Red List
of Threatened Species while the others are
listed under the Convention on International
Trade of Endangered Species (CITES). The
tree, S. macrophylla, though classified as
exotic is quite common, but also listed under
both CITES and IUCN because of its high value
in the international trade. Vulnerable species,
on the other hand, comprised 6% of the total
species recorded. Some of these were
A. blancoi, Diplodiscus paniculatus,
Macaranga bicolor, F. ulmifolia, and
M. philippinensis.
Table 2: Conservation status of plant species
Conservation
Status
Number
of Species
Percentage
(%)
Abundant
Common
Depleted
Vulnerable
Rare
Endangered
Indeterminate
27
44
22
7
6
5
10
22
36
18
6
5
4
8
Total
121
100
Many of the abundant and common plants
consisted of exotics and indigenous species.
This comprised majority of the total species
recorded. Men often introduce exotic species
due to their aesthetic value, whereas wildlife
disperses the indigenous ones. The complete
list of the conservation status of species is
found in Table 1.
ACKNOWLEDGEMENTS
We would like to thank our colleagues whom in
one way or another, have contributed to the
completion of the project, especially
Drs. Angelina Galang and Donna Reyes of the
Environmental Science Institute of Miriam
College. Our sincere gratitude also goes to the
local people of Laiban who accompanied us
during the fieldwork and accommodated us
during our stay in the barangay. Finally, we
also would like to acknowledge Dr. Rodel Lasco
for commenting on this paper.
REFERENCES
Department of Environment and Natural
Resources (DENR). 2005. Watershed
Research and Development Support
Project for Kaliwa Watershed. Project
Report. University of the Philippines Los
Baños Foundation, Inc. College, Laguna.
14
IUCN Red List of Threatened Species. 2004.
http://www.iucnredlist.org/
Miriam College. 2004. Comprehensive Plan
of the Southern Sierra Madre Wildlife
Center Project. (unpublished).
Myers, N., R.A. Mittermeier, G.A.B. Da Fonseca
and J. Kent. 2000. Biodiversity hotspots
for conservation priorities. Nature. 403:
853 – 858.
Ohsawa, M. 1991. Structural comparison of tropical
montane rainforest along latitudinal and
altitudinal gradients in South and East Asia.
Vegetation. 97: 1 – 10.
PAWB-DENR. 2000. Statistics on Philippine
Protected Areas and Wildlife Resources.
DENR, Quezon City, Philippines.
Pollisco, F.A. Jr. 2002. Biophysical Assessment
of the Quinale a river Watershed in Albay,
Bicol. Final Report to the DENR Region V
and World Bank. Hassalts and Assoc., Inc.
(unpublished).
FLORAL SURVEY OF LAIBAN IN SIERRA MADRE
Rice, A.L. and P.J.D. Lambshead. 1994. Patch
dynamics in the deep sea benthos: The role
of a heterogeneous supply of organic
matter. Pp.469 – 499. In: Giller, P.S., Hildrew,
A.G. and D.G. Raffaelli (Eds). Aquatic
Ecology: Scale, pattern and process.
Proceedings of the 34th Symposium of the
British Ecological Society. Oxford:
Blackwell Scientific Publications.
The International Plant Name Index. 2005.
Published on the Internet. http://
www.ipni.org/ (accessed 16 November 2005).
Williams, P., D. Gibbons, C. Margules, A.
Rebelo, C. Humphries and R. Pressey.
1996. A Comparison of Richness Hotspots,
Rarity Hotspots, and Complementary
Areas for Conserving Biodiversity of
British Birds. Conservation Biology. 10:
155 – 174.
World Bank. 2004. Philippines Environment
Monitor: Assessing Progress. The World
Bank Group.
JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 15 – 21, 2008
Research Article
Diversity of gingers at Serudong, Sabah, Malaysia
Januarius GOBILIK
Sabah Forestry Department, Forest Research Centre
P.O. Box 1407, Sepilok
90715 Sandakan, Sabah, Malaysia
ABSTRACT
The species richness and abundance of the
Zingiberaceae (hereafter gingers) were
studied in five study plots in Serudong and
in one study plot in an adjacent area. The
study plots were in undisturbed upland
kerangas forest (mossy kerangas forest), one
in an undisturbed lower montane-kerangas
forest, one in disturbed upland mixed
dipterocarp forest, and three in upland mixed
dipterocarp-kerangas forest (disturbed,
partially disturbed and undisturbed,
respectively). Thirty-nine species were
documented from the general area; eight of
which were found outside the plots. Eightyone percents of the species were recorded
from the disturbed forest plots. None of the
species were recorded from the undisturbed
upland kerangas and lower montanekerangas forest plots. Species richness
averaged 11 species per hectare. The index
of diversity of gingers for the study area was
estimated to be 2.0 (Shannon diversity index,
H’) and it was highest in the disturbed upland
mixed dipterocarp forest plot. At the scale of
this study, the diversity of gingers in
Serudong is found to be lower than that of
many other forest reserves in Sabah. The most
novel collection was Geostachys, a genus
that was documented in Sabah only recently.
Keywords: Gingers, species composition, Borneo
This finding was the second for a species of
this genus in Sabah.
INTRODUCTION
The diversity of gingers in Serudong has not
been well documented. Therefore, in 2006, a
team from the Sabah Forestry Department
carried out an expedition to study the density
and composition of these plants in this area.
The collected information can be used to
assess the importance of Serudong as an
in-situ conservation area for gingers in Sabah.
The results are reported in this paper.
METHODS
Study Site
Serudong is a 123,643 ha forest management
unit (FMU25) situated in southern Sabah on
the border to Kalimantan (4°12 – 33’N, 117°8
– 32’E; Fig. 1). The elevation is 450 – 1,300 m
above sea level but only a few hills rise above
1,000 m (Sabah Forestry Department, 2005).
The daily temperature fluctuates from 21°C
to 32°C. The annual rainfall is 2,500 – 3,500
mm. The area is characterized by the Kapilit
geological formation and Lokan and Crocker
are the main soil associations; others are
Maliau, Labau, Kalabakan, Serudong and
Gomantong associations. Its main soil unit is
orthic acrisol, which is sandy and less fertile.
16
DIVERSITY OF GINGERS AT SERUDONG, SABAH
Figure 1: Location of Serudong (FMU25) in Sabah (insert picture) and locations of the study plots in FMU
(plot 1–5). The control plot (plot 6) was established in Nurod-Urod Forest
The natural vegetation of the area is
composed of upland mixed dipterocarpkerangas (59.1%); lower montane-kerangas
(17.8); lowland mixed dipterocarp-kerangas
(7.1); lowland mixed dipterocarp (6.6); upland
mixed dipterocarp (4.9); upland kerangas (4.4;
mossy kerangas forest sensu Fox, 1972); and
lowland kerangas forests (0.1). A large portion
of the forest is in secondary and logged-over
conditions.
Sampling Method
Five study plots (1–5) were established in
four of the major forest types in Serudong
(Table 1). The locations of the plots were preidentified on a satellite image of the study
area and were visited on the ground. One
control plot (Plot 6) was established in Nurod
Urod Forest Reserve, a forest reserve in
adjacent area to Serudong.
In the plots, gingers were identified and
counted. Relative density of the species was
calculated as sum of density of the species
divided by sum of density of all species and
multiplied by 100. From these data, the
diversity of the gingers was estimated using
PCORD® (McCune & Mefford, 1999; version
4.14). The same software was used to run a
cluster analysis to find out the similarity of
composition of gingers between the studied
forest types (distance measure: Sorensen
(Bray-Curtis); linkage: group average). The
gingers were also qualitatively surveyed
along the trail to the peak of Gunung Maliat
(1,300 m), which is situated on the
international boundary that separates Sabah
and Kalimantan, Indonesia. Voucher
specimens were kept at Sandakan Herbarium
(SAN).
17
JANUARIUS GOBILIK
Table 1: The five plots established at Serudong (plot 1–5) and the one from Nurod Urod (plot 6)
and their characteristics
Plot
1
2
3
4
5
6
Forest Type
Disturbance
Size (m 2 )
Upland kerangas
Lower montane-kerangas
Upland mixed dipterocarp
Upland mixed dipterocarp-kerangas
Upland mixed dipterocarp-kerangas
Upland mixed dipterocarp-kerangas
Undisturbed
Undisturbed
Disturbed
Disturbed
Partially disturbed
Undisturbed
4
4
4
4
4
4
RESULTS
No gingers were recorded from the
undisturbed upland kerangas forest (Plot 1)
and undisturbed lower montane-kerangas
forest plots (Plot 2). The remaining plots
harboured 31 species (Table 2). Eight
additional species were found outside the
plots (Burbidgea schizocheila Hackett,
Elettariopsis kerbyi R.M. Sm., Etlingera
rubromarginata A.D. Poulsen & Mood,
Etlingera brachychila var. vinosa A.D.
Poulsen, Geocharis fursiformis var.
borneensis R.M. Sm., Hedychium
cylindricum Ridl., Hedychium sp., and
Zingiber argenteum Theilade & Mood). Of
these 39 species, eight taxa were identified
only to the genus due to the lack of flowers
for a thorough identification.
Species richness averaged 11 species per
hectare (ranged 7–17 per plot). The index of
diversity and species evenness of gingers
and species evenness in the area were
estimated to be 2.0 (Shannon diversity index,
H’) and 0.9, respectively (Table 3). Relative
density averaged 3(±6) stems per hectare.
Index of diversity, species count, relative
density and species evenness were highest
in the disturbed forest plots. In terms of
species composition and relative density, the
cluster analysis showed that Plots 3 and 4
×
×
×
×
×
×
20
50
190
300
400
500
Elevation (m)
770
1300
860
700
720
760
were inseparable from each other and were
distinctively dissimilar (100%) from Plots 5
and 6. Plots 5 and 6, on the other hand, were
only 57% similar.
The most interesting collection was that of
Geostachys, a genus that was found
occurring in Sabah only recently at Maliau
Basin (see Lim & Lau, 2006). Serudong is thus
a new locality for its occurrence. The species
was represented by 22 clumps in the partially
disturbed upland mixed dipterocarpkerangas forest plot (Plot 5). This species has
a potential as an ornamental; the leaves were
dark green with burgundy underneath and
the stem was dark green with reddish base.
The old and dried inflorescence was found
with old floral bracts congested at its top and
the old fruits appear to be oblong; this species
is distinct from that described from Maliau Basin.
DISCUSSION
At the scale of this study, the diversity of
gingers in Serudong is found to be lower than
that of many other forest reserves in Sabah.
There are about 168 species of gingers in
Sabah (see: Gobilik & Yusoff, 2005; Gobilik et
al., 2005a; Poulsen, 2006; Julius et al., 2007),
but only 23% are found at Serudong. The
number of species in this area can be ranked
as lower than that of Mt. Kinabalu (Gobilik &
Yusoff, 2005), Imbak Valley (Gobilik et al.,
18
DIVERSITY OF GINGERS AT SERUDONG, SABAH
Table 2: List, relative mean density and evenness of ginger species in the study plots
No.
Species
Mean (±SD)
Evenness
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
Alpinia ligulata K. Schum.
Alpinia nieuwenhuizii Val.
Amomum borealiborneense I.M. Turner
Amomum coriaceum R.M. Sm.
Amomum dimorphum M. Newman
Amomum oliganthum K. Schum.
Amomum sp.
Amomum testaceum Ridl.
Amomum uliginosum Koenig
Boesenbergia variegata R.M. Sm.
Elettaria surculosa (K. Schum.) Burtt & R.M. Sm.
Etlingera albolutea A.D. Poulsen
Etlingera baculutea A.D. Poulsen
Etlingera brevilabrum (Val.) R.M. Sm.
Etlingera inundata Sakai & Nagam.
Etlingera velutina (Ridl.) R.M. Sm.
Geostachys sp.
Globba pendula Roxb.
Globba propinqua Ridl.
Hornstedtia reticulata K. Schum.
Hornstedtia sp.
Plagiostachys breviramosa Cowley
Plagiostachys aff. roseiflora A. Julius & A. Takano
Plagiostachys oblanceolata J. Gobilik & A. Lamb
Plagiostachys sp. a
Plagiostachys sp. b
Plagiostachys strobilifera (Bak.) Ridl.
Zingiber pseudopungens R.M. Sm.
Zingiber sp. a
Zingiber sp. b
Zingiber viridiflavum Theilade & Mood
5.9 (6.9)
3.2 (6.5)
1.6 (1.9)
4.3 (8.6)
2.2 (2.9)
1.4 (1.7)
3.6 (7.1)
5.6 (11.2)
11.7 (14.8)
1.2 (2.4)
3.6 (5.8)
0.6 (1.2)
0.5 (1.0)
2.7 (4.7)
5.0 (3.6)
1.2 (2.4)
11.2 (22.5)
1.2 (2.4)
0.3 (0.6)
0.5 (1.0)
0.6 (1.2)
1.2 (2.4)
0.3 (0.6)
8.1 (10.6)
1.5 (2.9)
3.1 (6.1)
6.3 (9.7)
2.9 (4.5)
1.1 (1.3)
0.6 (1.2)
0.3 (0.6)
1.0
0.0
0.9
0.0
0.9
0.9
0.0
0.0
0.9
0.0
0.6
0.0
0.0
0.5
1.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.9
0.0
0.0
0.7
0.7
1.0
0.0
0.0
3.0 (4.9)
0.3
Averages:
Table 3: Relative mean density, species count (S), evenness (E) and diversity index of gingers in the
study plots (H = Shannon’s diversity index; D = Simpson’s diversity index)
Plot
Mean (±SD)
S
E
H
D
Forest Condition
3
4
5
6
2.4
3.2
3.2
3.2
(3.5)
(4.9)
(9.2)
(7.8)
17
12
8
7
0.9
0.9
0.7
0.9
2.5
2.4
1.5
1.7
0.9
0.9
0.7
0.8
Disturbed
Disturbed
Partially disturbed
Undisturbed
Averages:
3.0 (6.4)
11
0.9
2.0
0.8
JANUARIUS GOBILIK
2005b), Tabin Wildlife Reserve (Gobilik, 2002),
Crocker Range Park (Gobilik & Yusoff, 2005),
Danum Valley (Magintan, 2000), Maliau Basin,
and Tawau Hills Park (Gobilik, 2005;
unpublished expedition data). Nevertheless,
Serudong harbours more gingers than the
Mt. Trus Madi area (Gobilik & Yusoff, 2005),
another area in Sabah where the upland mixed
dipterocarp forest type is also prominent.
The low diversity of gingers in Serudong can
be associated with many factors. The most
important could be the distribution of
kerangas (heath) soil, degrees of forest
disturbance, and altitudes in the study area.
Kerangas forest is known to be infertile
(Newbery, 1991), and this forest will not
support many ginger species, which are
generally known to grow well only on moist
and high-organic-content soils (Larsen et al.,
1999). The low species count in the
undisturbed upland mixed dipterocarpkerangas forest plots indicates the adverse
effect of kerangas soil to recruitment of
gingers. Most of the species are even
occurring at a very low frequency and
abundance as one can interpret from the very
low evenness of the species (see Table 2).
Gingers are generally non-specialist
regarding substrate (Theilade, 1998) especially
in kerangas forest, perhaps with the exception of
Etlingera dictyota (Poulsen, 2006).
Forest destruction reduces plant diversity
(Slik et al., 2002), but to a certain degree, it
could cause the contrary (Connell, 1978). In
Serudong, the latter appears to be case
because the disturbed forest plots harbour
more species than the undisturbed forest
plots (Table 3). Thus it could be that in the
forest where the soil is infertile such as in
kerangas forest, logging would instead
increase soil fertility as well as ginger
diversity. It is quite logic to assume that
nutrients from the rotting tree branches and
stumps are recycled into the soil and are
19
consumed by the gingers. The gingers would
then have more energy to reproduce as one
can interpret from their slightly higher
Simpson’s diversity index from the disturbed
forest plots (Table 3; Simpson’s diversity
index is reported to be positively dependent
on species’ abundance – see Magurran,
1988). This scenario, however, does not imply
that the disturbed kerangas forest could
facilitate a recruitment of gingers beyond that
of forests of fertile soils.
Although some gingers are confined in
montane forests (Beaman & Beaman, 1998),
the richness of ginger species decreases with
increasing altitude (Gobilik & Yusoff, 2005).
Hence the low diversity of gingers in this
study can be associated with the fact that
the study plots (all) were established in
upland forest, which is occurring just above
the so-called lowland forest, a forest where
gingers are usually abundant (Gobilik &
Yusoff, 2005). As evidence, none of the
species were found in the undisturbed lower
montane-kerangas forest plot (1,300 m) or
along the trail to the peak of the Gunung
Maliat (1,000 – 1,300 m). Moreover, gingers
have not yet been reported to inhabit mossy
forest (>2,300 m elevation), even on large
mountains such as Mt. Kinabalu and Mt. Trus
Madi (Gobilik & Yusoff, 2005). Therefore, they
are not expected to inhabit upland kerangas
forest, which is a mossy forest sensu Fox
(1972). In Serudong, mossy forest took event
at lower altitude (700 m in this study) due to
‘Massenerhebung effect’, a reduction in the
lower altitudinal limits of vegetation zones
on isolated hills of infertile soils, a common
phenomenon which occurs in south-eastern
of Sabah (Fox, 1972).
Light and precipitation are the other two
factors for the higher density and species
richness of gingers in the disturbed forest.
This is because many gingers are growing
well only in open, wet and humid conditions
20
(Larsen et al., 1999; Poulsen, 2006). In other
word, the previous logging activities in the
study area had opened the forest canopy and
facilitated more light to reach the gingers on
the ground, and in Serudong, where the
precipitation is relatively high (2,500–3,500
mm), water does not limit their survival even
after they were being exposed to heavy
sunlight by the logging activities. On the
other hand, they generate more energy to
reproduce, because they receive enough
light, water, and nutrient (from the rotting tree
stems and branches) to carry out a productive
photosynthesis. In other words, the open
canopy, high precipitation, and nutrient from
the rotting wood debris left by the logging
are at least compensating the adverse effect
of kerangas soil on ginger’s recruitment in
the study area.
The present results also underline the
importance of gingers as indicators of forest
disturbance. The composition of gingers
reflects the disturbance level of the forest
very well as one can interpret from the Cluster
Analysis’s result. Nevertheless, none of the
species are confined in either forest condition.
Similar results had also been reported from Tabin
Wildlife Reserve (Gobilik, 2002).
As a summary, 62% of the species in Serudong
are widespread gingers in Sabah, 13% are
locally abundant at several districts and 5%
are locally rare. Of the remaining 21% nonidentified species, only the species of
Geostachys may be confined to this area. In
addition, this species could be new species
since it is distinct from that was described
from Maliau Basin. If so, at the scale of this
study, the importance of Serudong as an insitu conservation area for gingers can be
highlighted only by the occurrence of this
species and the 5% locally rare species of
DIVERSITY OF GINGERS AT SERUDONG, SABAH
the area. Many more special gingers may,
however, be found at this area in the future if
intensive inventories were to be carried out.
ACKNOWLEDGMENTS
I would like to thank the Sabah Biodiversity
Centre for funding the expedition to Serudong
and also to Dr Axel Poulsen for reviewing the
early version of this paper.
REFERENCES
Beaman, J. H. and R. S. Beaman. 1998. The
Plants of Mount Kinabalu: Gymnosperms
and Non-orchid Monocotyledons. Kota
Kinabalu: Natural History Publications
(Borneo).
Connell, J. H. 1978. Diversity in tropical rain
forest and coral reefs. Science. 199: 1302 –
1310.
Fox, J. E. D. 1992. The natural vegetation of
Sabah and natural regeneration of the
dipterocarp forests. PhD thesis. University
of Wales (unpublished).
Gobilik, J. 2002. Some aspects of abundance
and distribution of Zingiberaceae and
Costaceae in Tabin Wildlife Reserve, Sabah.
MSc thesis. Universiti Malaysia Sabah,
Kota Kinabalu, Sabah (unpublished).
Gobilik, J. and M. Yusoff. 2005. Zingiberaceae
and Costaceae of the Trus Madi Range.
Journal of Tropical Biology and
Conservation. 1: 79 – 93.
Gobilik, J., A. Lamb and M. Yusoff. 2005a. Two
new
species
of
Plagiostachys
(Zingiberaceae) from Sabah, Borneo.
Sandakania. 16: 49 – 56.
Gobilik, J., M. Yusoff and A. D. Poulsen. 2005b.
Species richness and diversity of
Zingiberaceae, Costaceae and Marantaceae
in the Imbak Valley (unpublished expedition
report).
JANUARIUS GOBILIK
Julius, A., M. Suleiman and A. Takano. 2007.
Five new species of Plagiostachys
(Zingiberaceae) from Borneo. Acta
Phytotaxonomy and Geobotany. 58: 1 – 17.
Larsen, K., H. Ibrahim, S. H. Kaw and L. G.
Saw. 1999. Gingers of Peninsular Malaysia
and Singapore. Kota Kinabalu: Natural
History Publications (Borneo).
Lim, C. K. and K. H. Lau. 2006. A new
Geostachys species from Maliau Basin,
Sabah. Folia Malaysiana. 7: 33 – 40.
Magintan, D. 2000. Diversity, abundance and
distribution of ground herbs in primary and
selectively logged forest of Danum Valley
(North Eastern Borneo). MSc thesis.
Universiti Malaysia Sabah, Kota Kinabalu
(unpublished).
Magurran, A. E. 1998. Ecological diversity and
its measurement. Cambridge, London:
University Press.
McCune, B. and M. J. Mefford. 1999. PCORD®. Multivariate Analysis of
Ecological Data. Version 4.14. MjM
Software Design, Gleneden Beach,
Oregon. USA.
21
Newberry, D. M. 1991. Floristic variation within
kerangas (heath) forest: Re-evaluation of
data from Sarawak and Brunei. Vegetation.
96: 43 – 86.
Poulsen, A. D. 2006. Etlingera of Borneo. Kota
Kinabalu: Natural History Publications
(Borneo).
Sabah Forestry Department. 2005.
Sustainable Forest Management Plan for
Forest Management Unit Serudung, FMU
25. Sabah Forestry Department, Sandakan,
Sabah (unpublished).
Slik, J. W. F., R. W. Verburg and P. J. A. Keßler.
2002. Effects of fire and selective logging
on the tree species compisition of lowland
dipterocarp forest in East Kalimantan,
Indonesia. Biodiversity and Conservation.
11: 85 – 98.
Thelaide, I. 1998. The genus Zingiber in
Thailand and Malaysia: Taxonomy, biology
and uses. PhD thesis. University of
Aarhus, Denmark (unpublished).
JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 23 – 37, 2008
Research Article
Biodiversity assesment in a Sarawak lowland dipterocarp rainforest of Niah
National Park
Faisal Ali ANWARALI KHAN1, 2, Mohamad Faishal BUJANG2, Mohd. Azmin KASSIM2,
YAP Sheau Yuh2, Besar KETOL2, Wahap MARNI2, Isa SAIT2, C.J. LAMAN2, Abang Arabi
ABG AIMRAN3, Zaidi MAWEK3, Abang Abdul Mutalib ABG TAJUDIN3, Haidar ALI3 and
M.T. ABDULLAH2
1
Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131, USA
2
Department of Zoology, Faculty of Resource Science and Technology, Universiti Malaysia
Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia
3
Sarawak Forestry Corporation, Level 12, Office Tower, Hock Lee Centre, Jalan Datuk Abang
Abdul Rahim, 93450 Kuching, Sarawak, Malaysia
ABSTRACT
A transect survey was conducted from 2 – 6
December 2004 in Niah National Park to
estimate species diversity and relative
abundance of birds and mammals. This study
was conducted in four forest line transects:
Madu Trail (TR1), Sungai Tangap (TR2), Niah
Great Cave (TR3), Bukit Kasut (TR4), and one
river transect along the Niah River (RT). A total
of 521 birds representing 59 species from 23
families were recorded. The Black-Nest Swiftlet
(Aerodramus maximus) and the Mossy-Nest
Swiftlet (Aerodramus salanganus) were the
most common species in the park. The family
Timaliidae (babblers), with nine species, was
recorded as the most diverse family, whereas
Strigidae (owls) and Hirundinidae (swallows)
were the least diverse families with one species
in each. A total of 29 mammalian individuals
representing seven species from four families
were recorded. The family Sciuridae (squirrels)
with three species was recorded as the most
diverse family, whereas Cynocephalidae (flying
lemurs) and Muridae (rodents) were the least
Keywords: Birds, mammals, Niah National Park,
relative abundance, species diversity, transect
diverse families with one species and one
individual each. TR1 was recorded with the
highest Shannon-Weiner index (diversity index)
of H’ = 4.75 and H’ = 2.20 for birds and mammals
respectively. The lowest bird H’ = 3.73 was
recorded for TR2, whereas the lowest mammal H’
= 0 was recorded for TR2 and RT. Although this
study does not identify factors that contribute to
different species diversity at each transect line,
field observations suggest that vegetation and
human activities were the major elements that
contributed to the observations found at each
transect in this study. Studies on the vegetation
types and potential disturbances that influence
the faunal diversity will provide useful insights in
conservation and management planning of this
park.
INTRODUCTION
Extended to an area of only 31.4 km sq (3,140
hectares), Niah National Park is one of Sarawak’s
smallest National Parks (Bennett, 1992). Its
uniqueness for paleontology studies (e.g.,
Harrisson, 1958, Piper et al., 2007) and diverse
ecology has attracted visitors, naturalists and
scientists. The park is located 16 km inland, on
24
TRANSECT SURVEY IN NIAH NATIONAL PARK
Figure 1: Map showing the locations of sampling areas in Niah National Park (adapted and modified from
Hazebroek & Abang Morshidi 2000). All details and symbols were included inside the map. Transects
were shaded with different colours as described in the map. Different colours of land cover refer to
different elevations in the park.
FAISAL ALI ANWARALI KHAN et. al.
the northern region of Sarawak (Hazebroek &
Abang Morshidi, 2000). It is about 110
kilometres southwest of Miri and located near
the Niah River, approximately 3.8 km from the
small town of Batu Niah (Bransbury, 1993;
Hazebroek & Abang Morshidi, 2000). Niah cave
was first established as a National Historic
Monument in 1958, and later as national park
on 23 November, 1974. It was officially opened
to the public on 1 January, 1975. Niah National
Park has been proposed as a World Heritage
Site by United Nations (UNESCO) owing to the
important fact that it holds prehistoric human
civilization remains (from 49,000 years ago) in
Niah cave (Hazebroek & Abang Morshidi, 2000).
Limestone forest, mixed dipterocarp forest, peat
swamp forest and regenerated forest are the
main vegetations found in this park (Good, 1991;
Anderson, 1996). About 60% to 70% of the park
is dominated by Gunung Subis (394 m), which
is a large and almost vertical limestone structure
(Hazebroek & Abang Morshidi, 2000). In terms
of the parks biodiversity, previous studies have
documented approximately 190 species of birds,
64 species of mammals, 48 species of snakes
and 22 species of frogs (Good, 1991). Niah cave
serves as the main habitat for thousands of
swiftlets and various species of bats (Medway,
1997). Black-Nest Swiftlets (Aerodramus
maximus) and Mossy-Nest Swiftlets
(Aerodramus salanganus) are the major
occupants of this cave. These swiftlets also
contribute as the major source of income for the
local people (especially those in the Chang longhouse inside the park; Figure 1) that collect
swiftlets nests, which are in demand in the
market for medical reasons.
Although the park harbours diverse wildlife, no
studies have been conducted utilizing transect
lines to survey, document, or update the current
list of fauna with estimated relative abundance
and diversity. This technique works best with
diurnal animals and is usually biased towards
highly social animals. However, there are also
25
several advantages that have made this method
a useful tool to measure species diversity. This
includes the ability to provide a broader range
of species than the trapping method due to the
dependency on trapping method’s limitation that
it depends on trap numbers, bait types, position
of traps and season (dry or monsoon). Therefore
studies using transect surveys are able to
provide a quick and reliable estimation of
species diversity, especially to monitor the trend
of faunal diversity in the park as a result of
urbanization or disturbances in the surrounding
areas.
Past logging operations that began in the 1960s
have led to the emergence of town like Batu
Niah that further explains the forest
fragmentation found around Niah National Park.
It is estimated that about 40% of Niah River
water catchment areas (land cover areas) were
transformed into a palm oil plantations in 2002.
Only 22% of the forest catchment area from 1972
still remains in 2005 (Hansen, 2005). It was also
noted that the native people from the long-house
inside the park have started to cultivate inside
the park boundary. Shifting cultivation and
poaching were practised by the locals
threatened the forest ecosystem, and thereby
affecting wildlife (Hansen, 2005). In view of these
threats, a study was conducted in five transects
to document the species diversity, and relative
abundance as an estimate of bird and mammal
diversity in Niah National Park. This study also
was aimed to facilitate park management by
providing a list of fauna sighted along the
walkways as a reflection of potential attractions.
It is expected that this baseline data can be useful
for future monitoring, management planning and
conservation of wildlife in this park.
MATERIALS AND METHODS
Study Area
Transect line surveys were carried out at five
different transect lines. Four of them were
26
conducted along popular visitors trails: Madu
Trail, Sungai Tangap Trail, Great Cave Trail and
Bukit Kasut Trail in the forest, whereas the last
one was along the Niah River, which flows along
the national park boundary. The location and
the range of each transect is shown in Figure 1.
Field Methodology
A transect line survey for data collection of birds
and mammals was used without disruption on
these faunas, as this involves only
observations, rather than direct handling of the
animals. The survey was conducted in 1 km
distance for each transect line and 3.2 km
distance for the river transect as illustrated in
Figure 1. The presence of birds and mammals in
each area was recorded based on direct and
indirect observations. Direct observations were
conducted by sighting the animals with
binoculars whereas indirect observations were
conducted based on the presence of signs such
as vocalizations, footprints, faeces, feeding
marks on fruits, nests and wallows (Mohd. Nor
et al., 1992). Birds and mammals found along
transects were identified using identification
keys by Smythies (1981, 1998, 1999), Payne et
al. (1985), Lekagul & Round (1991), Bond (1993),
MacKinnon & Philipps (1993), Gregory-Smith
(1995), Davison & Chew (1996), Harris et al.
(1996), and Francis (1998). Individual bird and
mammal surveys were recorded according to the
species identifications. Observations were
performed by several small groups that collected
the data independently to reduce the double
counting. Data was frequently compared
between groups to avoid any miscalculation or
misidentification. In some cases (mainly
swiftlets), average record from all the groups
was used as the final observation count. Thus,
the data presented herein is the best estimate of
faunal diversity.
Transects Lines
Surveys were conducted at four locations as
following: transect line one (TR1), transect line
TRANSECT SURVEY IN NIAH NATIONAL PARK
two (TR2), transect line three (TR3) and transect
line four (TR4). Surveys were conducted by
groups of 8 to 10 people equipped with
binoculars, field identification keys, and
inventory lists. First, transects were measured
and marked with coloured plastic-flagging tags
at each 25 m interval as the observation point
along transects. Survey hours were divided into
three sessions: morning (from 0600 hours to
1000 hours), evening (1600 hours to 1800 hours),
and at night (1930 hours to 2130 hours) to obtain
the best estimation of both nocturnal and diurnal
animals in the park. Observers walked at a speed
of approximately 500 metres per hour and
stopped for one minute at each 25 metre mark to
observe and listen for any movement, calls, or
signs of animals. This was repeated for five days
at four different transects simultaneously by five
different groups (including those in river
transect). Each group was shuffled between
transects to randomize observers and reduce
observation errors. This method was useful to
document diversity for a large area in a short
time, as the length of the survey relies mainly
on funding and manpower availabilty.
River Transect
Surveys along the Niah River were conducted
by boat from Pangkalan Lobang dock to Bukit
Kasut dock in a distance of about 3.2 km. The
survey was conducted between 0630 hours to
0700 hours, 1200 hours to 1230 hours, and 1600
hours to 1635 hours. Boat speed was set at
approximately 7.1 km per hour. The boat engine
will be off to listen to the animals sound. Other
surveys methods follow the description in
transect line methods above.
Data Analysis
Observation counts in the transect line study
were used to calculate the relative abundance
of each species. Species diversity indices were
calculated for birds and mammals for each line
transect. The Shannon-Wiener Index and
Evenness were calculated using the DIVERS
FAISAL ALI ANWARALI KHAN et. al.
program (Krebs, 1989), which has been modified
(methods for data entry and retrieval has been
changed) for ease of data input and output
(Laman, 2001). Lastly, the diversity indices
between transects were statistically compared
using pairwise diversity comparisons following
t-test method from Zar (1996).
RESULTS
Bird Species Diversity and Abundance
A total of 521 individuals of birds representing
59 species from 23 families were recorded (see
Table 1). The family Timaliidae was recorded as
the most diverse family with nine species,
followed by Cuculidae with six species, and both
Nectariniidae and Pycnonotidae with five
species. According to Sarawak's legislation
(1998), a total of 15 species from eight families
are under Part I and Part II Wildlife Protection
Ordinance 1998, which are protected in Sarawak.
This study has recorded one species,
Anthracoceros malayanus (family Bucerotidae;
Black Hornbill) that is listed under Part I (Totally
Protected Animals) as well as Egretta garzetta
(family Ardeidae; Little Egret), Loriculus
galgalus (family Psittacidae; Blue-crowned
Hanging Parrot), Ninox scutulata (family
Strigidae; Brown Hawk-owl), Copsychus
malabaricus (family Turdidae; White-rumped
Shama), all species of swiftlets (family
Apodidae), all species of kingfishers (family
Alcedinidae), and all species of woodpeckers
(family Picidae) that are listed in Part II
(Protected Animals) of Wildlife Protection
Ordinance 1998. The avifauna of the park was
dominated by the Black-Nest Swiftlet
(Aerodramus maximus) with the highest relative
abundance at each transect and was followed
by Mossy-Nest Swiftlet (Aerodramus
salanganus). The family Apodidae recorded the
highest relative abundance with 32.1% (or 167
out of 521 individuals). Generally all birds, except
for owls, are active during the day. The only
nocturnal avian species observed was the
Brown Hawk Owl.
27
Table 2 shows the Shannon-Weiner Index for
diversity analysis of each transect. Species
diversity index was highest at TR1 (4.75),
followed by RT (4.26), TR4 (4.07), TR3 (4.03),
and finally TR2 (3.73). Zar’s t-test calculation at
a = 0.05 indicates that there were significant
differences in diversity indices between TR1 vs.
TR2, TR1 vs. TR3, and TR1 vs. TR4. In contrast,
the result indicates that there were no significant
differences between TR2 vs. TR3, TR2 vs. TR4,
and TR3 vs. TR4. The analysis did not include
the comparison with the river transect as the
observations for the river transect were set at
3.2 km whereas the rest of transects were
calculated for 1 km range.
Mammal Species Diversity and Abundance
A total of 29 individuals of mammals
representing seven species from four families
were recorded (see Table 3). The mammals were
recorded using observation and vocalization
techniques for the following families:
Cynocephalidae, Cercopithecidae, Sciuridae and
Muridae. Following Sarawak's legislation (1998),
only flying lemurs (family Cynocephalidae) were
included in Part II of Wildlife Protection
Ordinance. Only the Plaintain Squirrel
(Callosciurus notatus) and Prevost’s Squirrel
(Callosciurus prevostii) from the family
Sciuridae were recorded at RT (two individuals)
and TR2 (one individual) respectively. Although
this suggests a 100% relative abundance at each
transect, they were represented by less than
two individuals that may provide a biased
estimation of the overall mammals in those
transects. Highest relative abundance was
followed by the Pig-Tailed Macaque (Macaca
nemestrina) and the Plain Pigmy Squirrel
(Exilisciurus exilis), with both at 22.2% for TR1
and TR3 respectively. In general, the highest
relative abundance for mammals was dominated
by the family Sciuridae with 65.5% (19 out of 29
individuals).
Table 4 shows the Shannon-Weiner Index for
the diversity analysis of each transect. Species’
Family
Species and Common Name
Total
Ardeidae
Accipitridae
Rallidae
Psittacidae
Cuculidae
Strigidae
Apodidae
Alcedinidae
Picidae
Eurylaimidae
Hirundinidae
Aegithinidae
3
2
12
5
3
6
11
3
1
19
1
103
64
1
1
5
2
16
2
3
5
20
1
2
10
1
2
6
3
Transect
2
3
4
RT
Relative Abundance (%)
TR1 TR2
TR3
TR4
3
1
1
3
1
5
1
4
1
1
2
2
2
13
10
32
17
3
1
23
17
2
4
3
1
7
1
2
2
9
2
1
8
4
2
5
2
4
1
7
6.0
0.9
0.9
2.8
7
2
2
2
0.9
4.6
2
1
5
29 6
16 4
1
1
3
2
0.9
3.5
0.9
0.9
1.7
1.8
1.7
11.9
9.2
27.8
14.8
2.6
0.9
1
1
5.2
1.8
1.8
1.8
2.7
0.9
20.4
15.0
1.5
3.0
0.8
5.2
21.6
11.9
1.8
3.7
1
5
6.4
0.9
1.8
1.8
8.0
1.8
0.9
7.0
3.5
1.7
4.4
2
1
1
4
4.0
2.0
10.0
12.0
8.0
2.0
2.0
6.0
4.0
0.8
3.7
2.0
0.8
1
2
1
RT
2.0
4.0
0.9
1.7
0.9
0.9
3.0
TRANSECT SURVEY IN NIAH NATIONAL PARK
Bucerotidae
Megalaimidae
Egretta garzetta (Little Egret)
Spilornis cheela (Crested Serpent-eagle)
Amaurornis phoenicurus (White-breasted Waterhen)
Loriculus galgalus (Blue-crowned Hanging Parrot)
Cuculus micropterus (Indian Cuckoo)
Cacomantis merulinus (Plaintive Cuckoo)
Surniculus lugubris (Drongo Cuckoo)
Phaenicophaeus chlorophaeus (Raffles’s Malkoha)
Phaenicophaeus sumatranus (Chestnut-bellied Malkoha)
Centropus sinensis (Greater Coucal)
Ninox scutulata (Brown Hawk-owl)
Aerodramus maximus (Black-nest Swiftlet)
Aerodramus salanganus (Mossy-nest Swiftlet)
Actenoides concretus (Rufous-collared Kingfisher)
Todirhamphus chloris (White-collared Kingfisher)
Halcyon capensis (Stork-billed Kingfisher)
Alcedo atthis (Common Kingfisher)
Ceyx rufidorsus (Rufous-backed Kingfisher)
Anthracoceros malayanus (Black Hornbill)
Megalaima rafflesii (Red-crowned Barbet)
Megalaima mystacophanos (Red-throated Barbet)
Megalaima australis (Little Barbet)
Sasia abnormis (Rufous Piculet)
Picus puniceus (Crimson-winged Woodpecker)
Eurylaimus ochromalus (Black-and-yellow Broadbill)
Hirundo tahitica (Pacific Swallow)
Aegithina tiphia (Common Iora)
Chloropsis cyanopogon (Lesser Green Leafbird)
Chloropsis cochinchinensis (Blue-winged Leafbird)
1
28
Table 1: Composition and relative abundance of avifauna recorded in Niah National Park. Total individuals captured and their associated relative abundance are
showed according to transect lines (TR = Transect and RT = River Transect)
Species and Common Name
Total
Pycnonotidae
Turdidae
Timaliidae
Sylviidae
Muscicapidae
Dicaeidae
Nectariniidae
Sturnidae
Dicruridae
Pycnonotus goiavier (Yellow-vented Bulbul)
Pycnonotus plumosus (Olive-winged Bulbul)
Pycnonotus brunneus (Red-eyed Bulbul)
Alophoixus bres (Grey-cheeked Bulbul)
Alophoixus phaeocephalus (Yellow-bellied Bulbul)
Trichixes pyrropyga (Rufous-tailed Shama)
Copsychus saularis (Magpie Robin)
Copsychus malabaricus (White-rumped Shama)
Trichastoma rostratum (White-chested Babbler)
Malacocincla malaccensis (Short-tailed Babbler)
Malacopteron magnum (Rufous-crowned Babbler)
Malacopteron cinereum (Scaly-crowned Babbler)
Malacopteron magnirostre (Moustached Babbler)
Napothera atrigularis (Black-throated Wren Babbler)
Macronous gularis (Striped Tit Babbler)
Macronous ptilosus (Fluffy-backed Tit Babbler)
Stachyris erythroptera (Chestnut-winged Babbler)
Orthotomus sericeus (Rufous-tailed Tailorbird)
Rhipidura perlata (Spotted Fantail)
Prionochilus maculatus (Yellow-breasted Flowerpecker)
Dicaeum trigonostigma (Orange-bellied Flowerpecker)
Anthreptes malacensis (Brown-throated Sunbird)
Hypogramma hypogrammicum (Purple-naped Sunbird)
Nectarinia jugularis (Olive-backed Sunbird)
Arachnothera longirostra (Little Spiderhunter)
Arachnothera robusta (Long-billed Spiderhunter)
Aplonis panayensis (Asian Glossy Starling)
Acridotheres tristis (Common Myna)
Cracula religiosa (Hill Myna)
Dicrurus paradiseus (Greater Racket-tailed Drongo)
4
4
12
1
2
1
6
12
11
1
5
1
3
4
3
1
20
27
4
26
1
7
3
7
19
6
3
2
2
10
Total number of individuals
Total number of families
Total number of species
521
23
59
1
Transect
2
3
4
RT
TR1
Relative Abundance (%)
TR2
TR3
TR4 RT
4
2
1
2
1
2
1
1
5
1
4
1
4
5
1
3
3
2
1
2
2
4
3
1
8.0
1.8
0.9
1.8
0.9
2
2
1.8
0.9
0.9
4.6
0.9
3
2
1
1
2
6
4
5
7
7
4
6
7
8
4
7
1
5
9
1
1
2
0.9
3.5
4.4
2.2
1.5
0.9
1.8
1.5
3.0
2.2
2.0
4.0
4.0
2.6
2
2
2
4
6
3.5
0.9
2.7
FAISAL ALI ANWARALI KHAN et. al.
Family
4
5
2
7
1
1
1
1
1.8
0.9
0.9
1.8
5.5
3.7
4.6
1.5
1.5
6.1
6.1
3.5
5.3
5.2
6.0
3.5
6.2
0.9
4.4
6.7
0.8
0.8
1.7
3.5
4.4
1.5
5.2
1.8
3.7
5.5
3
2
1
3
2
1
1
109
19
37
115 113 134 5 0
15 17 13 13
23 26 26
4
2.0
2.0
2.0
2.0
6.0
4.0
0.9
2.8
1.7
0.9
0.9
3.0
23
29
30
TRANSECT SURVEY IN NIAH NATIONAL PARK
Table 2: Shannon - Weiner Index and evenness of avifauna (above), and comparison of diversity
indices between two transects using the Zar t-test (below). The Zar t-test is calculated by comparing
each transect line with other transect lines studied here. The river transect was not included for
the Zar t-test, as explained in the results section (TR = Transect; RT = River Transect; α = 0.05)
TR 1
TR2
TR3
TR4
RT
Number of individuals
Number of families
Number of species
Shannon-Weiner Index (H’)
Evenness
109
19
37
4.75
0.04
115
15
23
3.73
0.12
113
17
26
4.03
0.09
134
13
26
4.07
0.08
50
13
23
4.26
0.04
Transect
t-calculated
t-critical
Significant/Not significant
Transect 1 vs. Transect 2
Transect 1 vs. Transect 3
Transect 1 vs. Transect 4
Transect 2 vs. Transect 3
Transect 2 vs. Transect 4
Transect 3 vs. Transect 4
22.07
17.10
17.56
– 5.19
– 5.28
– 0.74
1.96
1.96
1.96
1.96
1.96
1.96
diversity index was highest at TR1 (2.20)
followed by TR3 (1.84), and TR4 (1.75). However,
the result of the diversity index for mammals at
TR2 and RT was zero. This is due to the small
number of individuals at both line transects. The
Zar t-test calculations at α = 0.05 showed that
there was a significant difference between the
diversity indices of TR1 vs. TR3, and TR1 vs.
TR4. In contrast, results showed that there was
no significant difference between TR3 vs. TR4.
DISCUSSION
Bird Species Diversity and Abundance
Results from this study showed that the avian
family Apodidae had the highest relative
abundance. This was probably due to high
spotting chances compared to other animals,
as they fly in a range and become detectable to
the naked eye. The occurrence of limestone
caves also explains this observation. Both the
Black-Nest Swiftlet (A. maximus) and the
Significant
Significant
Significant
Not significant
Not significant
Not significant
Mossy-Nest Swiftlet (A. salanganus) were
recorded with the highest relative abundance
at all transects. According to Rahman &
Abdullah (2002), abundance of swiftlets is
influenced by the presence of caves and cliffs
that serves as their major roosting site.
Hazebroek & Abang Morshidi (2000) also
reported that the Niah Great Cave is one of the
largest limestone caves in Sarawak, with a high
number of fauna occupying this habitat. In this
cave, swiftlets were estimated to reach a total of
150,000 individuals. Three swiftlet species were
found in the park: Black-Nest, Mossy-Nest and
White-Bellied Swiftlets. Of these, Black-Nest
Swiftlets are the most common found in Borneo
and form the main population in the park
(Hazebroek & Abang Morshidi, 2000). During
this survey, most of the swiftlets were recorded
in the morning and evening owing to the fact
that they hunt and feed during the daytime.
Swiftlets were observed on a regular day
leaving their roosting cave as early as 0600 hours
and returning as early as 1600 hours (also see
Medway, 1997; Lim & Cranbrook, 2002).
Family
Species
Total
Cynocephalidae
Cercopithecidae
Sciuridae
Muridae
1
Transect
2
3
Cynocephalus variegatus (Flying Lemur)
Macaca fascicularis (Long-tailed Macaque)
Macaca nemestrina (Pig-tailed Macaque)
Callosciurus prevostii (Prevost’s Squirrel)
Callosciurus notatus (Plantain Squirrel)
Exilisciurus exilis (Plain Pigmy Squirrel)
Sundamys muelleri (Muller’s Rat)
1
2
1
6
13
5
1
1
3
2
1
1
Total number of individuals
Total number of families
Total number of species
29
4
7
9
3
5
1
1
1
4
RT
Relative Abundance (%)
TR1 TR2
TR3 TR4
1
RT
12.5
2
22.2
1
2
4
2
2
4
1
2
9
2
4
8
2
4
2
1
1
11.1
33.3
22.2
11.1
100.0
11.1
22.2
44.4
22.2
25.0
50.0
12.5
FAISAL ALI ANWARALI KHAN et. al.
Table 3: Composition and relative abundance of mammals recorded in Niah National Park. Total individuals captured and their associated relative abundance
are showed according to transect lines (TR = Transect; RT = River Transect)
100. 0
31
32
TRANSECT SURVEY IN NIAH NATIONAL PARK
Table 4. Shannon - Weiner Index and evenness of mammals (above), and comparison of diversity
indices between two transects using the Zar t-test (below). The Zar t-test was calculated by
comparing each transect line with other transect lines studied here. The river transect was not
included for the Zar t-test, as explained in the results section (TR = Transect; RT = River Transect;
t-critical is at 1.96 at α = 0.05)
TR1
TR2
TR3
TR4
RT
Number of individuals
Number of families
Number of species
Shannon-Weiner Index (H’)
Evenness
9
3
5
2.20
0.16
1
1
1
0.00
0.00
9
2
4
1.84
0.27
8
2
4
1.75
0.30
2
1
1
0.00
Infinite
Transect
t-calculated
t-critical
Transect 1 vs. Transect 2
Transect 1 vs. Transect 3
Transect 1 vs. Transect 4
Transect 2 vs. Transect 3
Transect 2 vs. Transect 4
Transect 3 vs. Transect 4
4.06
4.48
0.87
2.57
2.57
2.78
Previous study by Rahman et al. (2004) at Fairy
Cave and Wind Cave Bau, have also recorded
Mossy-Nest Swiftlet with highest relative
abundance: 18.2% (14 individuals). Similarly,
Hassin (2004) also indicated that Mossy-Nest
Swiftlet was the dominant species in Bau
limestone forest with relative abundance of
25.74% (or 26 out of 101 individuals) when using
mist-net techniques. Although the current study
has reported lower swiftlet abundance compared
to those in Bau limestone forests, it indicates
nothing more than the difference in techniques
used and number of species recorded in each
study rather than the diversity of the site. Our
study in Niah National park has recorded more
than 500 individual of birds compared to those
at Bau (Hassin, 2004) which recorded only 101
individuals through trapping techniques. This
also indicates that the transect survey is able to
cover a broader range of bird species in
comparison to trapping techniques that depend
on trap efficiency and positioning.
Significant/Not significant
No comparison
Significant
Significant
No comparison
No comparison
Not significant
Babblers from the family Timaliidae were
recorded with the highest number of species.
This family was easily identified in the field
compared to other families through their
conspicuous calls. These species forage at both
forest floor and under canopy (Strange &
Jeyarajasingam, 1993). They feed on various
types of food such as insects, larvae, and worms,
and inhabit primary and secondary lowland
forest. In Peninsular Malaysia, babblers alone
contribute up to 25% of forest community
species richness (Madoc, 1992). Cuckoo species
from the family Cuculidae were recorded with
the second highest number of species. These
species were found mainly in open areas and
river habitats. Sunbirds and spiderhunters of
the family Nectariniidae were recorded with the
third highest number of species. These birds
were recorded in various types of habitats such
as primary forest, secondary forest, gardens,
plantations and peat swamp forest. These
habitats provide this group of birds with a large
FAISAL ALI ANWARALI KHAN et. al.
range of food sources, microhabitats, and
protection from predators.
TR1 was recorded with the highest diversity
index followed by TR4. Both areas were
categorized as less disturbed, and this may be
the reason for their high species diversity.
Generally, not many visitors or local commuters
pass by this area. TR4 was not open to the public
during this study. TR1 consisted of secondary
forest, with patches of mixed dipterocarp forest.
This type of forest provides variety of food
sources such as seeds, fruits, small mammals,
insects and larvae. Conversely, TR4 is situated
in an area covered by secondary lowland forest,
but surrounded by primary forest. This area is
less disturbed and appropriate as foraging areas
for birds. This study has recorded TR1 (4.75)
and TR2 (3.73) diversity indices higher than
those by Kon et al. (2004) which used mist-nets
at similar transects (TR1 = 3.1 and TR2 = 3.15).
Generally, the advantage of a wildlife survey
compared to the mist-nets method is the ability
to cover a larger sampling area, in both horizontal
and vertical space. Transect surveys also
enable the observer to cover all forest levels
from above canopy, canopy, middle canopy,
under canopy and forest floor levels with the
aid of binoculars and animal calls. The mistnetting technique is more passive, selective, and
is usually designed for capturing avifauna under
canopy. Trapping techniques also depend on
net position across flyway direction. This will
influence the capture rate of the study. The
transect survey technique is more general for
broader coverage of species diversity.
A previous study by Rahman et al. (2004) at
Bau limestone forest indicated that less
disturbed areas have H’ = 1.03, whereas
disturbed areas have H’ = 1.30. In comparison
to our study, birds at Niah National Park were
more diverse than those from Bau limestone
forest. This was mainly due to the differences
in level of disturbance, availability of food
resources and forest vegetation in both study
sites. Results from this study also indicated that
33
the evenness index for all line transects were
below 0.50. Low evenness index suggests that
the number of individuals from each species
were significantly different from each other in
this study. This was mainly due to the large gap
between high swiftlet count and any other
species in this study which recorded
observation rates of less than half that of the
the swiftlet count.
Bird diversity indices showed significant
differences in the following transect
comparisons: TR1 vs. TR2, TR1 vs. TR3 and
TR1 vs. TR4. This may be due to the differences
in vegetation types and levels of disturbance at
these transects. Secondary forest, with patches
of primary mixed dipterocarp forest dominated
the TR1 area. Vegetations in primary forest and
lowland mixed dipterocarp forest provide a
greater variety of fruit compared to those in
secondary forests (Smythies & Davison, 1999).
Fruits are an important source of food for the
majority of bird species. Fewer visitors and
reduced local activities, along with food source
availability in TR1 were the major factors that
resulted in significant differences between
these transects. TR2 and TR4 were dominated
by secondary forest, whereas TR3 was mainly
dominated by limestone vegetation, which is
known for lower biodiversity than any other
forest types in Borneo (MacKinnon & Phillipps,
1993). Seasonal swamp forest that emerged
during the rainy season also may have reduced
foraging activities by the birds in TR2 areas
throughout this study period.
In contrast, results do not show any significant
difference in the following diversity indices
comparisons; TR2 vs. TR3 and TR2 vs. TR4.
Both, TR2 and TR3 can be categorized as
disturbed areas, as there was a great amount of
human activity, especially due to visitors and
local sounds (e.g., walking, talking) that may
have reduced bird activity around these areas.
Both of these trails are popular trails that lead
to the Niah Great Cave and the Long House
inside the park. Both of these transects faced
34
similar problems, as they were adjacent to each
other in this study. Although fewer visitors and
human activities were observed at TR4 than at
TR2 and TR3, statistical analysis indicates that
there were no significant differences between
TR2 vs. TR4 and TR3 vs. TR4. This may be due
to the similarity in secondary forest vegetation
found in both TR2 and TR4 that subsequently
supported similar bird species composition at
both of the transects.
Although both TR3 and TR4 were observed with
different vegetation types and levels of
disturbance, and both were situated at a
distance from each other, statistical analysis
showed no significant difference between TR3
vs. TR4. However, after considering the park
boundary, we found that TR4 was adjacent to
the cultivated lands and logging camps, whereas
TR3 was situated near limestone forest. These
separate habitats may have resulted in a similar
level of ecology and diversity constraint at both
transects that could not be differentiated in
statistical analyses.
Mammal Species Diversity and Abundance
Exilisciurus exilis and C. notatus from the
family Sciuridae were common throughout the
study. Results indicate that both species were
recorded with the highest density and relative
abundance. Squirrels are the small mammals that
visitors most often encountered in Niah National
Park (Hazebroek & Abang Morshidi, 2000). The
availability of food sources, such as fruits,
seeds, leaves, and other smaller animals might
sustain their high population. Sciuridae can also
adapt to various types of forest vegetation and
is able to partition the space in trees within other
species in the family. Plain Pigmy Squirrels (E.
exilis) often forage on tree trunks, Plaintain
Squirrels (C. notatus) forage on branches and
on the ground, whereas Prevost’s Squirrels (C.
prevostii) forage in the canopies of high and
big tree branches. Fungi that were found in all
vegetation types on tree trunks, branches, twigs,
left litter, soil and dead plant materials also serve
TRANSECT SURVEY IN NIAH NATIONAL PARK
as the major source of food for this family
(Hazebroek & Abang Morshidi, 2000). Figs,
especially Ficus benjamina were identified as
an important food resource for all frugivorous
animals in the park. This plant can be regarded
as the ‘keystone’ species that promotes the
diversification of other fauna in the park (sensu
Marduka 2001).
The Long-Tailed Macaque and the Pig-Tailed
Macaque were the only large mammals recorded
and representative throughout the study. Most
of the large mammals were shy and they usually
hide when encountered with humans. Seasonal
effect during monsoon season (e.g., seasonal
swamp: Karim et al., 2004) and short study period
may have influenced the low number of large
mammals recorded in this study. Apart from this,
hunting pressure by the locals also may have
contributed to the reduction of large mammals
recorded in the park (Mohd. Nor et al., 1992).
Only one individual of Prevost’s Squirrel was
recorded at TR2 and two individuals of Plantain
Squirrel were recorded at RT in this study. This
may be due to the condition of the area which
can be categorized as disturbed, with high
frequency of visitors and local activity along
the transect. The seasonal swamp at TR2 also
might have reduced the foraging range of any
ground dwelling animal, especially the small
mammals in this area. TR1 had the highest
diversity index as recorded in birds. Lowland
dipterocarp forest was the main factor that
contributed to the richness of mammals’
community in the park as it provided optimal
food resources for diverse groups of animals
(Hazebroek & Abang Morshidi, 2000; Karim et
al., 2004). TR2 and RT were recorded with 0.0
diversity index with only one species in both of
the survey sites (refer Ludwig & Reynolds, 1988).
Previous study by Karim et al. (2004) at Bau
limestone area using trapping methods
indicated that a total of 42 species from 17
families were recorded. Both Muridae and
Sciuridae dominated that area with Muller’s Rat
FAISAL ALI ANWARALI KHAN et. al.
(Sundamys muelleri) as the most common
species there. However current study only
recorded 29 individuals representing seven
species and four families in Niah National Park.
A study by Nyaun et al. (2004) using trapping
techniques (cage traps) at Madu Trail showed
a higher value of diversity indices compared to
those of similar sites in the study. This is mainly
due to the baits that were used in traps that
made it possible to attract shy animals into the
traps. Hence, the probability of documenting
small mammals (mostly shy) is higher using
traps compared to direct observation, which
depends on skill and chance of sighting
mammals in the dense tropical rainforest.
Therefore, differences in survey method may
contribute to the variation between trapping and
observation techniques, as traps were found
more efficient in documenting, both volant and
non-volant small mammals. Previous studies,
using traps (e.g., mist-nets, harp traps, cage
traps, camera traps) have documented new
geographic records for the park and Sarawak
(e.g., Hall et al., 2002; Abdullah 2003; Azlan &
Sharma, 2006; Jayaraj et al., 2006; Anwarali et
al., 2007).
A study at Tanjung Berlipat, Niah National Park
(north to our study site), was recorded with a
total of 35 species from 16 families of mammals.
Tanjung Berlipat was reported to have less
disturbed vegetation and reduced number of
visitors. However, the small mammal species
account compiled by the Niah National Park
Management for Tanjung Berlipat does not
provide details on the field methods and
sampling effort used. This may represent a
compilation of all other previous surveys
performed in the park.
An analysis on small mammal diversity showed
that there are significant differences between
TR1 vs. TR3 and TR1 vs. TR4 diversity indices.
This correlates with different forest vegetation
and levels of human disturbance found at each
transect. The level of disturbance was
significant at TR4, as this transect is situated
35
opposite Batu Niah town and exposed to vehicle
sounds and boat engines along the nearby river.
This may be the major factor that influences the
mammals’ species compositions in this area.
CONCLUSIONS AND RECOMMENDATIONS
Species diversity is a simple measure of
community stability and persistence of the
ecosystem in the face of disturbances (Hamilton,
2005). The transect line is a useful tool for rapid
assessment of the diversity of birds and
mammals in a tropical rainforest. However, this
method is limited due to the behaviour of the
animals, experience of the observer, and
visibility of the target taxa in the dense tropical
lowland forest. Increased survey period with
more replicates to take account of seasonal and
habitat differences will provide better estimates
of the faunal diversity. This is also important to
ensure the consistency of data in providing the
best interpretation of diversity, density, and
relative abundance of the studied faunas at a
particular site. Wildlife surveys also require
special skills to enable the observer to identify
the birds and mammals from a distance, and
possibly from their calls and footprints.
The faunal lists compiled in this transect survey
can be improved by including trapping
techniques that would enable the researcher to
overcome some of the disabilities in transect
surveys. The amount of line transects can be
increased, so that at least 10% of the study is
covered to provide a better estimation of
diversity. The study should also be conducted
away from the park walkways to reduce
disturbance on the animals by park visitors
when observations are conducted. As this
survey was done during monsoon season,
seasonal swamp might have influenced animals
activity, especially ground dwelling mammals.
Therefore, surveys during dry or fruiting season
might increase the number of animals observed.
36
ACKNOWLEDGEMENTS
We are particularly grateful to Miss Nafisah
Tahir and Sabrina Reduan for volunteering in
this wildlife survey. We thank Peter A. Larsen,
John R. Middleton, Sergio Solari and
anonymous JTBC reviewers for constructive
comments on the previous draft. We also thank
Mary Belden and Nur Qasdina Jeeta Abdullah
for proofreading this manuscript. We thank the
Sarawak Forestry Corporation (SFC) for
permission to conduct wildlife research in Niah
National Park, Sarawak. We thank Niah National
Park management for providing accommodation
and other logistic facilities for our study group
during the field expedition. This study would
not have been possible if not for the collecting
efforts by members of the Zoology Department.
FAAK was supported through the length of his
study at Texas Tech University with Dr Robert
J. Baker by the Higher Education Ministry of
Malaysia and UNIMAS. The raw substance in
this manuscript was submitted by FAAK to the
Sarawak Forestry Corporation as partial
fulfillment of the permit requirement. Financial
support for field workwas provided by UNIMAS
to the Zoology Department.
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TRANSECT SURVEY IN NIAH NATIONAL PARK
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JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 39 – 53, 2008
Research Article
Horizontal distribution of intertidal nematode from Sabah, Malaysia
SHABDIN Mohd. Long1 and OTHMAN Haji Ross2
1
Department of Aquatic Science, Faculty of Resource Science and Technology, Universiti
Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia
E-mail: lshabdin@frst.unimas.my
2
School of Environmental and Natural Resources Sciences, Faculty of Science and Technology,
Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia
ABSTRACT
The aim of this study is to determine the
horizontal distribution of nematodes species
density, species diversity and feeding types
on the intertidal area of Lok Kawi beach, Sabah,
Malaysia. The approach taken was to sample
the nematodes and measured selected
parameters of the hole water from high-water
to low-water marks. The results show that the
nematode feeding type non selective deposit
feeders (1B) and epigrowth feeders (2A)
groups, species diversity, evenness, species
richness and species number increased towards
the low tide level. The height of the beach did
not clearly show their influence on the
horizontal distribution of the nematodes.
Pearson correlation coefficient shows that there
is a significant correlation (R = 0.64, p < 0.05)
between the height of the beach and the species
diversity of the nematodes. However, the
cluster and factor analysis of the stations did
not show clearly about the influence of height
of the beach on nematodes densities.
Therefore, we conclude that there were no
definite and universal causative factors, which
controlled the horizontal distribution of
nematodes species diversity in the intertidal
Keywords: Water parameters, density, diversity,
feeding types
sandy and muddy habitats of the Lok Kawi
beach, Sabah.
INTRODUCTION
Previous studies on horizontal distribution of
nematodes have been carried out along salinity
gradients in estuaries (Warwick, 1971), across
intertidal sandy habitats (Blome,1983) and with
increasing water depth both onto the
continental shelf and into the deep sea
(Tietjen,1976). Most of the studies were carried
out in the temperate countries.
Several species groups have been suggested
across the sandy intertidal habitats. Firstly,
species often restricted to certain zones namely
sublittoral fringe guild, secondly, eurytopic
species (usually with their distribution centred
on the lower shore) and thirdly, species
confined to the upper shore (Coull, 1988). Four
strata of meiofauna distribution was proposed
during low tide on sandy beaches (McLachlan,
1980); namely, (1) a dry sand stratum – near the
top of the beach where the upper sand layers
are >50% desiccated; (2) a moist sand stratum,
which underlies the dry sand stratum and
extends seaward. It reaches until the depth of
the permanent water table; desiccation is < 50%
and oxygen levels are high (>70 % saturation);
(3) Water table stratum crossing the beach and
40
lying underneath strata 1 and 2. The sand is
always moist and oxygen saturation is 40 to
70%; (4) a low oxygen stratum underneath
stratum 3, which may be very deep in high
energy beaches, where oxygen tension is < 30%
saturated. This pattern can be modified by a
variety of factors such as a change in wave
action or sediment grain size, change in beach
slope, freshwater seepage, tidal amplitude,
temperature as it affects desiccation
(McLachlan, 1980). Other authors have reported
similar patterns from other areas of the world
but they use different kind of controlling factors
(Pollock & Hummon, 1971).
Studies on horizontal distribution of nematode’s
community on the intertidal area of Sabah are
still limited (Shabdin & Othman, 1999; Shabdin
& Othman, 2000; Shabdin & Othman, 2005).
Moreover, studies on the ecology of Malaysian
freeliving nematodes (to date, have generally)
are limited to the higher major taxa
(Sasekumar,1994) with the exception for study
carried out in Merbok mangrove, Kedah
(Somerfield et al.,1998). However, the Merbok
mangrove study only examined the community
level of nematodes at High Water Neap (HWN)
and High Water Spring (HWS). The question
of how the distribution of species diversity of
freeliving nematodes from high water to low
water on the intertidal area of monsoonalmaritime-tropical country like Sabah, Malaysia
is still unclear.
Therefore the objectives of the present study
are; (i) to examine the nematode community
structure from Mean High Water Neap
(MHWN) to Mean Low Water Neap (MLWN),
(ii) to determine the relationship between
nematode species diversity, horizontal
distribution and physico-chemical parameters
of the water in Lok Kawi beach, Kota Kinabalu,
Sabah, Malaysia.
HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE
METHODOLOGY
Study Area
The general climate of Sabah west coast is
monsoonal-maritime-tropical, i.e. generally hot
and humid with very heavy rainfall. Seasonal
variations in climate and weather are not
equated with temperature, as it is relatively high
and constant, but due to variations in moisture
associated with the northeast and southwest
monsoons. The onset and retreat of the
monsoons generally follow the same temporal
pattern but variations from year to year are not
uncommon. The monsoons also vary in
strength and constancy from year to year. The
northeast monsoon is generally from December
and February or early March and southwest
monsoon is from late June to early November.
There are also successive inter-monsoons from
April to May (Meteorological Department
Sabah, 1993).
Lok Kawi beach was chosen in the present
study because of its accessibility from Kota
Kinabalu city which is about 6 km to the south.
It is located at 5° 52’ N and 116° 2’ E. Two
habitats, sandy and muddy substratum existed
together and thus it would be logistically easier
to carry out sampling process. The beach lies
in a southwest to north direction and stretching
approximately 4.5 km along the Lok Kawi
coastline parallel to the Putatan road. The
beach extends about 0.6 km out into the shallow
foreshore water of the Lok Kawi coast during
low tide (Fig. 1).
The northeast of the Lok Kawi beach consists
of muddy area. The area is sheltered due to the
presence of sandbar in front of it. Scattered
patches of the seagrass beds (Enhalus sp.)
have been found in the area. The southern part
of the muddy area is the sand flats. Small
isolated patches of coral reefs mostly covered
by patches of dead coral rubbles and sand can
be seen at the western part of the beach.
SHABDIN MOHD. LONG & OTHMAN HAJI ROSS
41
PHILIPPINES
Mangroves
Coral remains
Quadrat
Casuarina
Figure 1: Map shows the location of sampling stations at Lok Kawi beach (T1 to T4 – Transect)
42
Meiofauna Sampling and Physico-chemical
Parameters Measurement
Sampling was carried out on May 1992. Four
transects perpendicular to the coastline were
set up on the beach during low tide at Lok Kawi
beach (Fig. 1). Transect 1 (T1) was in the muddy
area (mangrove) while transects 2 (T2), 3 (T3)
and 4 (T4) were located on the sandflats.
Five quadrats running from Mean High Water
Neap (MHWN) to Mean Low Water Neap
(MLWN) were located along the transect
generally at height intervals of 0.95 metres
measured using a standard surveying
technique (Moore,1979). One of these stations
was then levelled to the nearest standard Chart
Datum point, which in every case was a tide
gauge. Height of stations relative to Chart
Datum and the tidal constant were calculated
from data derived from the local chart and by
courtesy of the Marine Department of Kota
Kinabalu, Sabah.
Preliminary meiofauna survey on the Lok Kawi
beach shows that the vertical distribution of
meiofauna was up to 30 cm depth. In order to
minimize sampling error from spatial
heterogeneity in species composition and
abundance, a subsampling strategy was
adopted. At each quadrat, eight 30 cm sediment
cores were collected over an area 0.25 metre2
on the beach using the 7.01 cm2 transparent
tube. The sediment from these cores were put
into separate labelled plastic bags and
preserved in 5% neutralized seawater formalin.
Variance to mean ratios of faunal counts of the
first eight random samples taken at the first
sampling was not significant at the 5% level
(F test). Hence the samples were homogenous
and all samples at each tide level and then
subsequent ones were drawn from the same
parent population.
In the laboratory, meiofauna was extracted from
the substrate either by sieving or combination
of sieving and centrifuging techniques.
HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE
Meiofauna samples from sandy habitat were
extracted using the sieving method only while
samples from muddy habitat were extracted by
a combination of sieving and centrifuging
techniques (Shabdin, 1985).
The materials retained on the 32 µm sieve then
washed into 100 ml specimen bottles. Then the
eight cores of extracted sediments (meiofauna
in the eight specimen bottles) were pooled
together into 1 litre measuring cylinder and
made up to 1 litre with freshwater to be
subsampled. A simple device used for
subsampling is called ‘meiofauna subsampler’
(Moore et al., 1987). One subsample of 50 ml
will generally yield sufficient nematodes for
analysis although several subsamples were
taken in case of low density. The subsamples
were allowed to pass through a 32 µm sieve
and rinsed with freshwater to remove salt. The
material retained on the 32 µm sieve (sample
from sandy habitat) was made concentrated by
washing it to the edge of the sieve and then
washed it with water from the wash bottle into
a grid Petri dish. The subsampled specimens of
the nematodes then were scattered in a grid
Petri dish. Next, the total number of nematodes
in the grid Petri dish was counted under a SV5
Zeiss stereomicroscope. The numbers of
organisms were finally converted to densities
in units of individuals/10 cm square. Using a
fine end of pipette blocked with cotton wool at
the other end and the mouth piece, all the
nematodes were sucked and transferred to a
glass cavity block containing 5% glycerine: 5%
pure ethanol: 90% freshwater by volume and
left in desiccator for a few days (Platt &
Warwick,1983). This would allow the ethanol
and water to evaporate slowly leaving the
nematodes in pure glycerine. Finally, the
nematodes were transferred to a fresh drop of
anhydrous glycerine (phenol added) on a slide
and a cover slip added, supported by several
small glass blocks at both ends. Glyceel was
used as a sealant. The nematodes were
identified to the species level under a compound
microscope. Illustrations of each nematode
SHABDIN MOHD. LONG & OTHMAN HAJI ROSS
species were made using a camera lucida and
identifications were performed using the key
by Platt & Warwick (1983, 1988) and verified by
various keys in the literatures.
Environmental parameters of the pore water
such as temperature, salinity, dissolved oxygen
and pH value were measured in situ at each
quadrate using Hydrolab Environmental Data
System (model SVR-2 – Susonde Unit).
For every quadrat, one core of sediment up to
30 cm depth was taken for particle size analysis.
A piston-style corer, marked with permanent
marker at every 1 cm was used to sample three
cores of sediment for chlorophyll a analysis.
The sediment for chlorophyll a and
phaeopigments analyses were put into the
cooler box and brought back to the laboratory
for further analysis. The standard methods were
followed for the analyses of particle size and
chlorophyll a.
Clustering of the stations using the cluster
neighbour-joining methods and Detrended
correspondence analysis (Saitou & Ney,1987)
of the stations (quadrats) within four transects
at Lok Kawi were based on density of 85
nematodes species and the environmental
parameter values such as height above chart
datum, temperature, pH, salinity, dissolved
oxygen, median particle size, percentage silt
and clay, chlorophyll a and pheopigment.
RESULTS
Environmental Parameters
The variations of environmental factors such
as intertidal height, temperature, pH, salinity,
dissolved oxygen, median particle size, silt and
clay, chlorophyll a and pheopigment in Lok
Kawi beach are summarized in Table 1. The
record of these factors were expressed by
following the quadrats sequence from MHWN
to MLWN.
43
Intertidal heights of quadrats were plotted in
relation to the Chart Datum and the tidal
constants in Table 1. Most of the Quadrats 1
within the four transects were closer to the
MHWN level and therefore considered as
MHWN quadrats. Their heights above Chart
Datum were between 4.50 and 4.60 metres.
Quadrats 2, 3 and 4 in all transects were in the
range of 3.70 to 2.30 metres above Chart Datum
and considered as Mid-Tide Level (MTL)
quadrats. Quadrats 5 in all transect were
located closer to MLWN and ranged in heights
above Chart Datum between 1.40 to 1.60 m.
There was little variation in pore water
temperature at the four transects at Lok Kawi
beach, this being not greater than about 2.9°C.
Temperatures were generally within the range
of 28.5 to 31.4°C (Table 1) and close to the
temperature of the sea. In general, the pore water
temperature within four transects was quite
similar. The pH values of pore water within the
four transect were ranged from 7.0 to 8.5 and
shows the basic pH. The variation of pH is 1.5.
There was a wide variation in pore water
salinity at the four transects at Lok Kawi beach
but this being not greater than 15.5 Practical
Salinity Unit (PSU) (Table 1). The pore water
salinity within four transects were ranged from
14.7 to 30.2 PSU. Salinity values at Quadrats 5
and 1, Transect 4 were much lower (14.7 & 17.5
PSU) due to the influence of freshwater
intrusion from Desa Cattle drainage after a
heavy rainfall in the night before sampling. Both
of the quadrates were located close to the Desa
Cattle channel on the beach. Similarly, salinity
values at Quadrat 1 Transect 2 were also low
(16.1 PSU) due to the freshwater seepage from
the supralittoral area after a heavy rain in the
night before sampling. The salinity at Lok Kawi
beach was influenced by freshwater seepage
and the salinity values at all transects were
found to be lower than the surface sea water
adjacent to it.
44
HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE
Table 1: Summary of Environmental parameters at Lok Kawi, Sabah (Tran.–transect, TL–tide level,
Quadrat, HCD–Height above Chart Datum (m), Tem.–temperature (°C), Sal.–salinity (PSU), DO–dissolved
oxygen (mg/l), Med.-median (Ø, particle size), S&C-percentage silt and clay, Chlo.-Chlorophyll a (mg/m3),
Pheo–Pheopigment (mg/m3). MHWN – Mean High Water Neap, MTL – Mid-Tide Level and MLWN –
Mean Low Water Neap)
Tran.
TL
Q
HCD
Tem.
pH
Sal.
DO
Med.
S&C
Chlo.
Pheo.
1
MHWN
MTL
1
2
3
4
5
4.55
3.70
2.95
2.30
1.40
29.5
29.6
30.8
30.3
31.4
7.0
7.0
7.1
7.5
7.6
25.8
29.9
26.1
29.0
25.5
0.3
0.4
0.9
0.2
0.4
2.8
5.2
3.0
2.6
2.7
35.9
69.3
43.9
35.9
36.6
5.02
4.00
3.94
3.50
5.76
3.52
7.87
13.88
10.75
7.69
1
2
3
4
5
4.60
3.65
3.10
2.40
1.60
30.5
30.0
29.4
29.0
30.1
7.8
7.8
8.0
7.9
7.7
16.1
29.7
30.2
29.3
27.7
1.1
1.1
1.6
2.1
0.7
1.5
1.2
0.9
1.1
1.2
7.4
7.2
10.1
9.1
6.5
1.81
5.32
3.44
3.40
2.62
7.69
2.20
0.75
1.12
1.62
1
2
3
4
5
4.60
3.70
3.05
2.30
1.55
30.6
30.0
29.9
29.1
28.9
7.5
7.8
7.8
8.5
8.5
21.9
28.9
27.8
21.1
17.5
1.1
1.6
1.5
0.9
0.6
1.1
1.4
2.2
1.5
2.3
11.3
3.4
4.2
6.2
11.4
2.50
4.60
1.73
2.99
4.01
2.68
2.15
1.36
0.15
5.76
1
2
3
4
5
4.50
3.65
3.00
2.40
1.60
28.5
29.4
29.8
29.8
30.6
7.9
8.0
8.0
8.2
7.9
17.5
27.9
27.8
28.3
14.7
0.8
0.8
0.9
0.9
0.6
1.3
1.1
1.4
1.4
2.0
4.1
4.1
3.6
3.3
4.4
0.94
0.91
4.74
7.61
2.39
0.61
0.40
1.97
2.40
1.00
MLWN
2
MHWN
MTL
MLWN
3
MHWN
MTL
MLWN
4
MHWN
MTL
MLWN
Dissolved oxygen values of the pore water are
listed in Table 1. On all transects the values
were variables ranging from 0.2 (Transect 1) to
2.1 mg/l (Transect 2). The lowest value were
recorded along the mangrove transect
(Transect 1). The minimum value (0.2 mg/l) was
recorded at Quadrat 4 Transect 1.
Median particle size in Transect 1 ranged from
2.6 to 5.2 ∅ whereas the values in other
transects ranges from 0.9 (Transect 2) to 2.3 ∅
(Transect 3) (Table 1). The silt and clay
percentages was higher in Transect 1 compared
to the other transects. The lowest value in the
mangrove transect (Transect 1) was 35.9%
whereas the highest value in the sandy
transects was only 11.4% (Transect 3).
There was a wide variation in the distribution
of chlorophyll a in all transects (Table 1) with
no horizontal trends apparent. The mean
concentration of the four transects ranged from
3.17 (Transect 3) to 4.44 mg/m3 (Transect 1).
The distribution of pheopigment varied along
all transects and no horizontal trend was
apparent (Table 1). The mean concentration of
four transects ranged from 1.28 (Transect 4) to
8.74 mg/m3 (Transect 1). Most of the values in
Transect 1 (mangrove area) were either similar
or higher (7.69 to 13.88 mg/m3) than the other
sandy transects (Transects 2, 3 and 4).
Nematode’s Distribution
Total density
The maximum nematode’s density recorded at
Lok Kawi beach was 7,015 (Quadrat 5, Transect
4) and minimum of 413 ind./10 cm square
(Quadrat 2, Transect 2) (Table 2). The mean
SHABDIN MOHD. LONG & OTHMAN HAJI ROSS
nematode’s density ranged from 1,473 (Transect
3) to 3,055 ind./10 cm square (Transect 4).
Higher densities of nematodes in the lower half
of the beach at Transects 2 to 4. They appeared
to be a gradual increase in density from the
upper shore towards the lower shore except for
Quadrat 1 in Transects 2 and 3 where densities
of nematodes were higher than some MTL
quadrats. However, no horizontal trend was
apparent in Transect 1 (mangrove area).
Horizontal distribution of nematode species
Considering the horizontal distribution of
nematode’s species as a whole within all
transects and tide levels at Lok Kawi, beach,
five groups of species can be observed (Fig.
2). Firstly, the nematode’s species distributed
from MHWN to MLWN. A total of 24 species
were included in this group. Five species were
distributed from MHWN to MTL only and
considered as the second group. The third
group which comprised of 19 species was zoned
from MTL to MLWN. The fourth group
45
contained 1 species and its distribution was at
MHWN and MLWN. The fifth group of
nematode species was distributed either at
MHWN or MTL or MLWN only and comprised
of 34 species (MHWN: 6 species, MTL: 12
species, and MLWN: 16 species).
Horizontal distribution of nematode feeding
types
By considering the horizontal distribution of
the nematode feeding type groups as a whole
at Lok Kawi beach, four trends can be observed
(Fig. 3). The group selective deposit feeders
(1A) varied erratically along transect with its
density average ranged from 244 to 996 ind./10
cm square. The non-selective deposit feeders
(1B) and epigrowth feeders (2A) groups show
a clear increase in density towards the lower
half of the beach. However, the density of the
predators/omnivorous (2B) group seemed to
be stable from MHWN to MLWN.
Table 2: Total density of the nematodes in all transects at Lok Kawi beach
Transect
Tide Level
Quadrat
Density
1
MHWN
MTL
1
2
3
4
5
1
2
3
4
5
1
2
3
4
5
1
2
3
4
1846
785
4032
1760
4281
4088
413
447
1181
5494
1113
452
1737
1919
2142
554
1059
2437
4211
5
7015
2
MLWN
MHWN
MTL
3
MLWN
MHWN
MTL
4
MLWN
MHWN
MTL
MLWN
46
HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE
Desmodora cazca
Metacomesoma aequale
Maryllynnia gerlachi
Theristus pertenuis
Gammanema sp.1
Daptonema spirum
Viscosia meridionalis
Prochromadora sp.
Spirinia parasitifera
Eleutherolaimus hopperi
Daptonema articulatum
Ptycholaimellus macrodentatus
Oncholaimus oxyuris
Stylotheristus mutilus
Paradontophora pacifica
Metalinhomoeus karachiensis
Terschellingia communis
Sphaerolaimus penicillus
Haliplectus sp.
Leptolaimus venustus
Leptolaimus luridus
Sphaerotheristus macrostoma
Ingenia mirabilis
Metalinhomoeus insularis
Oncholaimus campylocercoides
Tripyloides sp.
Minolaimus sp.
Ironid gen.1
Terschellingia longicaudata
Terschellingoides filiformis
Halichoanolaimus chordiurus
Halalaimus supercirrhatus
Cyatholaimid sp.1
Molgolaimus sp.
Metacyatholaimus sp.
Xyala
Metachromadora onyxoides
Chromadorella sp.1
Chromadorella sp.2
Chromadorella filiformis
Hypodontolaimus pumilio
Aegialoalaimus sp.2
Siphonolaimus purpureus
Paracomesoma inaequale
Trichotheristus sp.
Nannolaimoides decoratus
Ironid gen.2
Paralinhomoeus conspicuus
Daptonema sp.
Oncholaimus sp.
Steineria ampullacea
Richtersia sp.
Desmocolex sp.
Acanthonchus cobbi
Aponema sp.
Paracanthoncus sp.
Setoplectus sp.
Quadricoma sp.
Gairleanema sp.
Parodontophora sp.
Ceramonema filum
Chromadorita c.f. luekarti
Platycomopsis sp.
Gammanema sp.2
Paralongicyatholaimus macramphis
Dorylaimopsis turneri
Oncholaimus brachycercus
Spilophorella sp.
Rhynchonema cinctum
Rhabdocoma sp.
Chromadorita tenuis
Conilia sp.
Paramesonchium sp.
Oxystomina elongata
Gammanema kosswigi
Neotonchus sp.
Nemanema sp.
Prooncholaimus sp.
Linhomoeus sp.
Cyatholaimid sp.2
Trissonchulus sp.
Anoplostoma subulatum
Daptonema kornoeense
Figure 2: Horizontal distribution of nematodes species in Lok Kawi beach, Kota Kinabalu, Sabah, Malaysia
* Combination of nematodes distribution in all transects
SHABDIN MOHD. LONG & OTHMAN HAJI ROSS
47
Figure 3: Horizontal distribution of nematodes feeding types (mean values for 4 transects) in Lok
Kawi beach (Q1: Mean High Water Neap, Q2 to Q4: Mid-Tide Level, Q5: Mean Low Water Neap,
1A: Selective deposit feeders, 1B: Non selective deposit feeders, 2A: Epigrowth feeders and 2B:
Predators/Omnivorous)
Species diversity of nematodes
When considering the horizontal distribution
of species number, species diversity, and
evenness as a whole at Lok Kawi beach, these
values were found to be generally increased
towards the low water (Fig. 4).
This shows that the nematode parameters
decreases as the beach Chart Datum increases
except for the species diversity. Species
diversity phenomenon is common due to a
higher species density at low tide stations
leading to the domination of one or two species
so that the species diversity become low if we
compared with the stations higher on the beach.
Statistical Analysis
Pearson correlation analysis results shows that
there was a significant correlation between the
height above Chart Datum and total nematodes,
nematode feeding type non-selective deposit
feeders (1B), nematode feeding type epigrowth
feeders (2A), nematode species diversity,
nematode evenness, nematode species
richness and number of nematode species
(Table 4).
Cluster analysis of the stations (quadrats)
within four transects at Lok Kawi beach showed
at least two major groups of stations are
clustered in the dendrogram (Fig. 5). The first
cluster included stations from T2Q5 to T1Q1.
One station (T4Q5) is separated from the main
2 clusters. The cluster analysis did not show
clearly about the influence of height of the beach
on meiofaunal densities. Detrended
correspondence analysis of the stations also
showed similar results (Fig. 6).
HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE
Species no.
Diversity and evenness
48
Quadrate
Figure 4: Horizontal distribution (mean values of 4 transects) of Shannon – Weiner diversity index
(H’), Pielou’s evenness (J’) and species no. of nematodes (S) (Q1: Mean High Water Neap, Q2 to Q4:
Mid-Tide Level, Q5: Mean Low Water Neap)
Table 4: Pearson correlation coefficient of nematodes and beach height
Nematode parameters
Total nematodes
Nematodes feeding type non-selective deposit
feeders (1B)
Nematodes feeding type Epigrowth feeders (2A)
Shannon-Wiener diversity
Pielou’s evenness
Nematodes species number
Height above Chart Datum
R = -0.55, P<0.05
R = -0.57, P<0.05
R = -0.61, P<0.05
R = 0.64, P<0.05
R = -0.46, P<0.05
R = -0.63, P<0.05
SHABDIN MOHD. LONG & OTHMAN HAJI ROSS
49
2500
Linkage Distance
2000
1500
1000
500
Group 2
Group 1
Factor 2
Figure 5: Dendrogram illustrating the similarity of the stations (quadrats) at Mean High Water Neap
(Q1), Mid-Tide Level (Q2 to Q4) and Mean Low Water Neap (Q5) T1 to T4 (Transects)
Factor 1
Figure 6: Detrended correspondence analysis of the nematodes species at Mean High Water Neap
( ), Mid-Tide Level ( ) and Mean Low Water Neap ( )
T1Q1
T1Q2
T2Q2
T2Q3
T2Q4
T3Q2
T4Q1
T3Q4
T3Q3
T3Q1
T3Q5
T1Q3
T1Q4
T1Q5
T2Q5
T2Q1
T4Q2
T4Q3
T4Q4
T4Q5
0
50
DISCUSSION
The density of nematodes in the mangrove and
sandy sediments varied considerably both on
a global and local scales (Dye,1983; Hodda &
Nicholas, 1985; Alongi, 1987; Olafsson, 1995).
This variation is within the recorded range from
other intertidal habitat. Several authors have
found significant differences in tropical
meiofaunal densities among intertidal positions
in mangrove and sandy areas with highest
abundance at low water stations (Dye, 1983;
Hodda & Nicholas, 1985; Alongi, 1990;
Sasekumar, 1994) although Dye (1983) found
that meiofauna in highest number at mid-water
level. The similar result was also known in
certain areas (Moore, 1979). Animal tolerant to
higher temperatures, lower values of water
saturation and oxygen tension, appeared to
occupy higher tidal levels (Rao & Misra, 1983).
Alongi (1990) concluded that physical factor
(temperature, grain size, salinity, infrequent tidal
inundation limiting dispersal) accounted for the
differences observed rather than biological
variables. In the present study, Pearson
correlation showed that the species density
and diversity of the nematodes were influenced
by the height of the beach, however clustering
and Detrended correspondence analysis did
not clearly show the influences of this factor.
Therefore, in this case the conclusion by Coull
(1988) that there were no unequivocal and
universal causative factors controlling the
nematode’s species density on the sandy and
muddy intertidal habitats in a tropical country
like Malaysia can be supported.
The study of nematode species zonation
across the intertidal habitat have been
conducted both in temperate and tropical
regions (Moore, 1979; Coull, et al., 1979; Alongi,
1987). Three groups of species have been
suggested across the sandy intertidal habitats.
Firstly, the species often restricted themselves
to sublittoral fringe guild, secondly, eurytopic
species where their distribution are centred on
HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE
the lower shore and thirdly, the species that
confined to the upper shore only (Coull, 1988).
The current study found that five groups of
nematode’s species were distributed
horizontally along the intertidal height. The
species distributed from MTL to MLWN or
found only at MTL were considered as
stenotopic species. These species possibly
prefer a more stable condition towards low-tide
zone. However, the species that were
distributed from MHWN to MLWN were
considered as eurytopic and able to tolerate to
the changes in the environmental parameters
while the species that were restricted in
distribution to a certain tide level such as
between MHWN and MTL can only tolerate
desiccation during exposure on the beach
(Tengku Balkis, 2000; Farizah, 2001; Shabdin,
2006).
Deposit feeders nematodes usually outnumber
other feeding guilds in the Australian mangrove
(Hodda & Nicholas, 1986). In Lok Kawi beach,
the non-selective deposit feeder (1B) was
dominant in both the mangrove (T1) and sandy
sediment (T4) transects. The epigrowth feeders
(2A) were dominant in other sandy sediment
transects (Transects 2 and 3). The current
finding is in accordance with the general trend
for the proportion of epistrate feeders to be
higher in the more sandy sediments and for
deposit feeders to dominate in finer sediments
(Hodda & Nicholas, 1986; Olafsson, 1995).
However, the non-selective deposit feeders
were also dominant in one of the sandy
transects (Transect 4). This finding had
deviated from the general trends. The nonselective deposit feeders (1B) were able to
ingest particles of a wider size range including
benthic diatoms (Platt & Warwick, 1983). The
occurrence of maximum chlorophyll a value
recorded at Quadrat 4, Transect 4 explains this
situation.
Based on several studies in India (Fell et al.,
1975; Krishnamurthy et al., 1984) predatory
SHABDIN MOHD. LONG & OTHMAN HAJI ROSS
nematodes were more abundant in the tropics
than in other intertidal areas. The results of this
study do not support the generalization that
predatory fauna is more abundant in tropical
sediments. The deposit feeders were abundance
in the mangrove and one of the sandy sediment
transects (Transect 4) in Lok Kawi beach. It
appears that the proportion of nematodes
feeding groups is as variable in the tropical
sediments as in other intertidal areas. The nonselective deposit feeders (1B) and epigrowth
feeders (2A) groups increased in density
towards MLWN. This is possibly due to the
more stable condition towards low-tide level
(Tietjen, 1977, Shabdin, 2006).
When the nematode’s diversity values were
compared, one trend is apparent. The diversity,
species richness, evenness and number of
species increased towards the low-tide level.
Pearson correlation coefficient shows that there
is a significant correlation between the height
of the beach and the species diversity of the
nematodes and this is possibly due to the stable
condition towards low-tide level. However, the
cluster and Detrended correspondence
analysis of the stations did not show clearly
the influence of height of the beach on
meiofaunal densities. The different of results
between both analyses were due to the nature
of analysis. Cluster and factor analysis of the
stations within four transects were based on
density of 85 nematodes species and the values
of physico-chemical parameters which
compared to the Pearson correlation analysis
that only calculated based on the total density
of nematodes and the physico-chemical
parameters values. However, the results of the
cluster – factor analysis are more reliable due
to the more accurate results obtained as
compared to the Pearson correlation analysis
(Moore, 1983).
Therefore, we conclude that there were no
definite and universal causative factors, which
controlled horizontal distribution of freeliving
51
nematode in the intertidal sandy and muddy
habitats of the Lok Kawi beach.
ACKNOWLEDGEMENTS
We wish to thank Universiti Malaysia Sarawak
(UNIMAS) for their financial support and the
Zoology Department, Universiti Kebangsaan
Malaysia for the use of their laboratory
facilities. We wish to thank Associate Prof. Dr
Tajuddin Abdullah, for his comment to improve
the manuscript and Prof. Y. Shirayama from Seto
Marine Biological Laboratory, Kyoto
University, Japan for providing us the
nematode’s literature of Prof. S.A. Gerlach
collections.
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Dudley. 1979. Zonation of meiobenthic
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on high energy sandy beaches in the
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B.J. Bett. 1987. Estimation of meiobenthic
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Freeliving marine nematodes, part 1.
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(Copepoda:Harpacticoida) in muddy and
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Sabah, Malaysia. The Raffles Bulletin of
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Tietjen, J.H. 1977. Population, distribution and
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JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 55 – 66, 2008
Research Article
Stand structure and tree composition of Timbah Virgin Jungle Reserve, Sabah,
Malaysia
Januarius GOBILIK
Sabah Forestry Department, Forest Research Centre
P.O. Box 1407, Sepilok
90715 Sandakan, Sabah, Malaysia.
ABSTRACT
The stand structure and tree composition of
Timbah Virgin Jungle Reserve (VGR Timbah)
were studied. Three locations in the VJR were
selected, and at each location, 1-ha study plot
was established. The plots were sub-divided
into 10×10 m2 sub-plots, and in each sub-plot,
stem diameters of trees > 5 cm diameter-at-breastheight (DBH) were measured. The trees were
identified, and their relative density and relative
basal area per hectare were calculated. Little
difference was found in tree density and basal
area per ha between the plots. From the plots,
2,369 trees > 5 cm DBH were enumerated. Total
basal area of the trees was 119.5 m2. Stem
diameter class distribution of the trees was found
to follow the inverse J-shape pattern. Many of
the trees had 5 – < 20 cm DBH (75.9 % of the
total stem). Only 4.2% had > 60 cm DBH. Total
densities of the trees > 5 cm and > 10 cm DBH
were 790 and 474 trees ha–1, respectively and
total basal areas per ha were 39.8 and 38.4 m2
ha–1, respectively. In this study, 47 tree families,
118 genera and 117 species of trees were
identified. Many of the trees were
Dipterocarpaceae (20% of the total stems). The
most abundant species was Dryobalanops
beccarii (4.3% of the total stems; 34 trees ha–1).
Keywords: Sabah, Timbah Virgin Jungle Reserve, forest
ecology
Pioneer and disturbed forest trees were found
at a very low density. The results suggest that
VJR Timbah's soils are infertile, since D.
beccarii, the most abundant species in the plots,
prefers leached whitish or yellowish sandy
soils. The results also suggest that the VJR had
experienced a less significant logging
encroachment or invasion of disturbed forest
trees. The results imply that VJR Timbah still
maintains its undisturbed forest stand structure
and tree composition, although it is relatively
small in size and surrounded by a large matrix of
heavily logged forest.
INTRODUCTION
Of the many forest enumeration activities in
Sabah, only a few are in virgin jungle reserves
(VJR). The scenario would be that many
foresters and researchers are not interested to
study the biological components of VJRs
because many of these forests are comparatively
small and surrounded by a dense matrix of
disturbed forests. To date, little is documented
about the stand structure and tree composition
of the forests in VJRs. In this paper, the stand
structure and tree composition of VJR Timbah
are reported. The information would be important
to assist in the development of management
prescriptions for the VJR or for the logged-over
commercial forest surrounding the VJR.
STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH
56
METHODS
Study Site
VJR Timbah is a 110 ha area situated in
compartment 53 of the Tangkulap Forest Reserve
(Fig. 1). The general climatic and ecological
condition of the VJR have not yet been
described. In Tangkulap, the annual rainfall
averages 3,000 mm, but it is highly variable (1,777
mm to 3,708 mm), with a major deficit occurs
every 6 years (Sabah Forestry Department,
2006). May – August and November – February
are the wettest seasons and March – April and
September – October are the driest seasons.
The daily temperature averages 27°C. The main
rock types of the area derived from Kolapis
formation and Ultrabasic Igneous. The main soil
association is Lokan with orthic acrisol as the
main soil unit. The natural vegetation of the area
is predominantly lowland mixed dipterocarp
forest and is dominated by Shorea johorensis
and its associated Dipterocarpus species, or by
Dryobalanops beccarii and its associated
Shorea species (Sabah Forestry Department,
2006).
Vegetation Sampling and Data Analysis
The study was carried out in 2004. Three 1-ha
plots were established in the VJR at 2 km interval
distance: plot 1 (5°26'8.099”N; 117°12'12.036”E),
plot 2 (5°26'5.411”N; 117°12'2.793”E) and plot 3
(5°26'2.218”N; 117°11'54.296”E; Figure 1). The
plots were sub-divided into 10×10 m2 sub-plots
to facilitate the enumeration of trees down to 5
cm stem-diameter at breast-height (DBH). The
DBH of the trees was measured and the trees
Figure 1: Location of VJR Timbah in Sabah and the three study plots (P1 – P3) in the VJR
JANUARIUS GOBILIK
57
were identified. The number of saplings of
dipterocarps (< 5 cm DBH to down to 50 cm
tall) was also counted. Relative density and
basal area per ha were calculated for every
species. Relative density (or relative basal area
per ha) of species was calculated as sum of
density (or sum of relative basal area per ha)
of the species divided by sum of density (or
sum of relative basal area per ha) of all species.
Voucher specimens were kept at Sandakan
Herbarium (SAN). Nomenclature in this study
follows largely the Tree Flora of Sabah and
Sarawak (Soepadmo et al., 1995, 1996, 2000,
2002 & 2004).
RESULTS
Little difference was found in tree density and
basal area per ha between the plots. The three
1-ha study plots included 2,369 trees > 5 cm
DBH (average = 790 trees ha–1) and 1,411 trees
>10 cm DBH (average = 474 trees ha–1). Many
of the trees had 5 < 20 cm DBH (75.9%; Figure
2 and Table 1 – see DBH's mode). Only 4.2%
had > 60 cm DBH. Dipterocarps composed
45.0
most of the trees > 60 cm DBH (Appendix 1 – see
Maximum DBH). At 180 cm DBH, Dryobalanops
beccarii (Dipterocarpaceae) was the largest tree
in the plots.
Total basal area of the trees > 5 cm DBH was 119.5
m2 (average = 39.8 m2 ha–1). For the trees > 10 cm
DBH, it was 115.3 m2 (average = 38.4 m2 ha–1). As
was expected, trees > 100 cm DBH had the highest
contribution to the total basal area per ha (24.3%;
Fig. 2). It was followed by the trees 10 < 30 cm
DBH (22%). Stocking of dipterocarp saplings in
the plots were 558 saplings ha–1.
There were 47 families, 118 genera and 117 species
identified from the plots. Most of the species were
Dipterocarpaceae (35 species), Euphorbiaceae (20
species), Anacardiaceae (7 species), Sapotaceae
(6 species), and Moraceae (5 species; Appendix 1).
A small number of the trees (14.4%), however, were
unable to be identified to genus or species.
The most abundant trees in the plots were
Dipterocarpaceae, Euphorbiaceae, Myristicaceae,
Myrtaceae and Lauraceae. The relative densities
Relative density
Relative basal area/ha
40.0
35.0
30.0
25.0
20.0
15.0
10.0
5.0
Size class (DBH, cm)
Figure 2: Size class distribution for all trees = 5 cm DBH in the study plots
>100
90-<100
80-<90
70-<80
60-<70
50-<60
40-<50
30-<40
20-<30
10-<20
0.0
5-<10
%
58
STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH
of trees from these families were 20%, 10.4%,
8.5%, 7.6% and 4.3% respectively (Table 1).
Other important families were Annonaceae,
Anacardiaceae, Burseraceae, Clusiaceae,
Bombacaceae and Verbenaceae. The relative
densities of trees from the latter were 3.5%, 2.7%,
2.6%, 2.5%, 2.4% and 2.4% respectively.
Thirteen (29.8%) of the families had <5
individuals (<0.2% relative density).
In terms of basal area, Dipterocarpaceae had
the highest contribution to the total basal area
per ha (55.4%), followed by Myrtaceae (4.5%),
Myristicaceae (3.4%), Euphorbiaceae (3%),
Sterculiaceae (2.8%), Lauraceae (2.5%) and
Bombacaceae (2.2%; Table 1). Other families that
had more than 1% contribution to the total basal
area per ha were Clusiaceae (1.3%), Fagaceae
(1.3%), Anacardiaceae (1.2%), Moraceae
(1.2%), Sapotaceae (1.2%), Burseraceae (1.1%),
Lecythidaceae (1.1%) and Melastomataceae
(1.1%).
Of the 117 species known from the plots, only
six had more than 1% relative density (>24 trees
ha-1), namely, Dryobalanops beccarii (4.3%),
Pternandra coerulescens (1.9%), Knema
laurina (1.6%), Shorea mecistopteryx (1.5%),
Teijsmanniodendron simplicifolium (1.2%) and
Durio grandiflorus (1%; Appendix 1). Only 16
species of these 117 species had more than 1%
(>1.2 m2 ha–1) contribution to the total basal area
per ha. They were mainly dipterocarps (13
species): Dryobalanops beccarii (14%), Shorea
mecistopteryx (4.5%), Dipterocarpus stellatus
(2.6%), Dipterocarpus pachyphyllus (1.8%),
Shorea argentifolia (1.7%), Dryobalanops
lanceolata (1.7%), Shorea pauciflora (1.2%),
Shorea laevis (1.1%), Shorea hypoleuca (1.1%),
Shorea macroptera (1%), Parashorea tomentella
(1%) and Dipterocarpus globosus (1%).
DISCUSSION
The results indicate that much of VJR Timbah's
stand structure and tree composition are similar
to that of undisturbed mixed dipterocarp forests.
Stem diameter class distribution of trees in the
VJR follows the inverse J-shape pattern, which
is similar to that of lowland primary forest of
Danum Valley (Newbery et al., 1992; Newbery
et al., 1996) and Segaliud-Lokan (Fox, 1967). The
VJR, however, supports a slightly lower density
of trees compared with several other
undisturbed mixed dipterocarp forests. Its
density of trees >10 cm DBH was 474 trees ha–1
compared to 487 – 569 trees ha–1 in Danum Valley
(Newbery et al., 1999; Bischoff et al., 2005), 477
trees ha–1 in Sungai Menyala and 546 trees ha–1 in
Pasoh (Manokaran & Swaine, 1994). On the other
hand, it appears to facilitate many large trees to
co-exist compared to the other forests, just as
one could imply from its higher total basal area
per hectare (38.4 m2 ha–1). In Danum Valley,
Sungai Menyala and Pasoh, the average basal
areas per ha of trees >10 cm DBH were 30.6, 31.8
and 29.1 m2 ha–1, respectively. It has a closely
similar average basal area per ha to Bukit Lagong
(41.1 m2 ha–1; Manokaran & Swaine, 1994), a hill
mixed dipterocarp forest in Peninsular Malaysia,
but again its density of trees >10 cm DBH is lower
than that of the latter. Generally, the results imply
that VJR Timbah still maintains its undisturbed
forest stand structure and tree composition,
although it is relatively small and being
surrounded by a large matrix of logged forest.
The VJR has a closely similar number of families
and genera (47 and 118, respectively) to Sungai
Menyala (45 and 116, respectively). However,
those numbers are lower than that of Danum
Valley (59 and 164 respectively) and Bukit
Lagong (51 and 139 respectively). It has again a
similar number of families to Pasoh (45-48), but
its number of genera is lower than that of the
latter (125-14). Even so, the top-ten list of family
of higher density in the VJR is closely similar to
that of Danum Valley, Bukit Lagong, Sungai
Menyala and Pasoh. The list differs only in the
positions of the families in the ranking. On the
top the ranking are Dipterocarpaceae and
Euphorbiaceae, and these families are followed
by any of these families: Myristicaceae,
Myrtaceae, Annonaceae, Anacardiaceae,
JANUARIUS GOBILIK
59
Table 1: Family composition, density (D), relative density (Rd) and relative basal area per hectare (Rba/
ha) of trees > 5 cm DBH in the study plots (N = number of individuals; Total = 2,369)
Family
Alangiaceae
Anacardiaceae
Annonaceae
Apocynaceae
Bombacaceae
Burseraceae
Celastraceae
Chrysobalanaceae
Combretaceae
Crypteroniaceae
Dilleniaceae
Dipterocarpaceae
Ebenaceae
Elaeocarpaceae
Euphorbiaceae
Fagaceae
Flacourtiaceae
Clusiaceae
Hypericaceae
Icacinaceae
Lauraceae
Lecythidaceae
Leguminosae
Magnoliaceae
Melastomataceae
Meliaceae
Moraceae
Myristicaceae
Myrsinaceae
Myrtaceae
Olacaceae
Oleaceae
Unidentified taxon
Polygalaceae
Rhamnaceae
Rubiaceae
Rutaceae
Sabiaceae
Sapindaceae
Sapotaceae
Simaroubaceae
Sterculiaceae
Theaceae
Thymelaeaceae
Tiliaceae
Ulmaceae
Verbenaceae
N
9
65
82
2
58
61
10
10
4
2
1
473
46
3
247
30
30
59
1
6
103
35
30
4
46
19
28
203
2
181
5
1
227
10
5
47
3
1
16
46
6
38
3
13
39
1
58
D (trees
ha –1 )
Rd (%)
Rba/ha (%)
Maximum
DBH (cm)
3
21.7
27.3
0.7
19.3
20.3
3.3
3.3
1.3
0.7
0.3
157.7
15.3
1
82.3
10
10
19.7
0.3
2
34.3
11.7
10
1.3
15.3
6.3
9.3
67.7
0.7
60.3
1.7
0.3
75.7
3.3
1.7
15.7
1
0.3
5.3
15.3
2
12.7
1
4.3
13.0
0.3
19.3
0.4
2.7
3.5
0.1
2.4
2.6
0.4
0.4
0.2
0.1
0.0
20.0
1.9
0.1
10.4
1.3
1.3
2.5
0.0
0.3
4.3
1.4
1.3
0.2
1.9
0.9
1.2
8.5
0.1
7.6
0.2
0.0
9.6
0.4
0.2
2.0
0.1
0.0
0.7
1.9
0.3
1.6
0.1
0.5
1.6
0.0
2.4
0.1
1.2
0.9
0.1
2.2
1.1
0.3
0.1
0.0
0.1
0.0
55.4
0.6
0.0
3.0
1.3
0.9
1.3
0.0
0.1
2.5
1.1
0.7
0.0
1.1
0.4
1.2
3.6
0.0
4.5
0.2
0.0
8.4
0.5
0.3
0.7
0.0
0.0
0.4
1.2
0.1
2.8
0.0
0.1
0.4
0.0
0.9
20.4
39.5
51.6
35.4
125.0
52.5
35.4
24.2
8.0
25.8
14.0
180.0
53.2
15.0
90.0
70.0
80.0
55.4
25.5
15.6
78.0
90.0
69.0
13.4
38.2
44.6
71.0
70.0
8.3
72.0
43.3
7.3
92.0
72.0
46.8
41.4
13.7
6.4
44.9
51.6
27.1
79.3
16.6
29.0
25.8
5.1
36.9
DBH's mode
6.4
7.0
8.9
18.5
5.7
7.2
8.0
7.0
6.1
17.5
14.0
5.4
6.1
10.2
6.4
12.1
10.2
10.2
25.5
8.0
7.3
8.9
5.4
8.9
6.1
22.3
6.4
7.6
8.0
10.2
11.5
7.3
6.1
5.7
20.1
6.1
8.6
6.4
10.2
7.0
4.8
8.9
6.1
5.1
9.6
5.1
11.1
60
STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH
Burseraceae, Lauraceae, Clusiaceae, and
Bombacaceae. The position of the families,
however, changes with inclusion of trees
< 10 cm DBH or < 5 cm DBH in the data analyses.
Such inclusion favours families composed mainly
by small-sized trees to be on the top of the ranking.
The number of known species in the VJR (117
species) is incomparable to that of Danum Valley
(307; Bischoff et al., 2005), Bukit Lagong (253),
Sungai Menyala (232) and Pasoh (235 – 276).
This is because the number of species identified
positively in this study is much lower than that
of the latter. Notwithstanding, of the known
species, the top-ten list of abundant species in
the VJR is differing from that of the latter. Of the
10 abundant species in the VJR, none is found
in Danum Valley, only one in Bukit Lagong (S.
laevis), three in Pasoh (Ochanostachys
amentacea, Shorea parvifolia, S. pauciflora),
and four in Sungai Menyala (S. macroptera, O.
amentacea, S. parvifolia, S. pauciflora).
In the VJR, Dryobalanops beccarii, a
dipterocarp, was the common species, but in
Danum Valley, Bukit Lagong, Sungai Menyala
and Pasoh, it was the non-dipterocarps. It was
Mallotus wrayi in Danum (Newbery et al., 1992),
Hydnocarpus filipes in Bukit Lagong, Santiria
laevigata in Sungai Menyala and Xerospermum
noronhianum in Pasoh. A strong preference of a
few dipterocarp species for certain soil conditions
has been reported in Borneo (Palmiotto et al.,
2004). In Sabah, D. beccarii was reported to prefer
leached whitish or yellowish sandy soils and to
occur as a pure stand in areas of such soil
condition (Fox, 1972). Thus the latter could explain
the above result, although the density of D.
beccarii in the VJR appears to be lower than that
of found by Fox (1972) in the forest at the mouths
of the Segama and Sugut Rivers or that of forest
at the upper stream of the Imbak River (personal
observation, 2005).
The high density of D. beccarii and Shorea
mecistopteryx in the study plots suggests that
VJR Timbah has a slightly different ecological
condition than that of Parashorea tomentellaEusideroxylon zwageri forest type, the forest
type of the general area (Tangkulap Forest
Reserve) where the VJR is situated. While these
two species were found abundantly in the plots,
Parashorea tomentella and its three common
associated species, Dryobalanops lanceolata,
Dipterocarpus caudiferus and Shorea
leprosula, occur at very low density. Shorea
johorensis and Eusideroxylon zwageri, the
other two important species associated with
Parashorea tomentella, were also not found in
the plots. In other words, Parashorea
tomentella and its associated species are very
scarce in the plots, although they are markedly
abundant in the adjacent forests to the VJR (Fox,
1967; Seino et al., 2005). Therefore, based on
Fox's (1972) classification of forest types in
Sabah, VJR Timbah's vegetation can be loosely
classified as lowland mixed dipterocarp forest of
Parashorea tomentella-Eusideroxylon zwageri
forest type with a strong influence of inland heath
forest of swampy-padang forest type.
There are five important points that can be
postulated from the results. First, soil
characteristics are suspected to be the
determining factor for the current tree
composition in the VJR. The two abundant trees
in the VJR, D. beccarii and S. mecistopteryx,
are reported to prefer leached whitish or
yellowish sandy soils. Thus only trees that
could tolerate such soil condition would
successfully populate the VJR. Secondly, there
will be other sites in Tangkulap that have similar
soil condition to VJR Timbah. Such similarity
also means that the sites are infertile. If so, the
common and abundant trees in the typical
Parashorea tomentella-Eusideroxylon zwageri
forest type would not be suitable as planting
material to reforest some degraded sites in
Tangkulap. The sites could instead be
appropriately reforested with D. beccarii, S.
mecistopteryx and S. macroptera. Thirdly, the
suspicion that many of the small VJRs in Sabah
JANUARIUS GOBILIK
had experienced heavy logging encroachment
may only be half true. This is because a small
VJR such as VJR Timbah has still had stand
structure and tree composition that are similar
to that of undisturbed forests, although it is
surrounded by forest that was heavily logged.
Fourthly, the invasion of disturbed forest trees
into small VJRs is less prominent. As was the
scenario in VJR Timbah, pioneer and disturbed
forest trees were scarcely found in the study
plots, although these trees were predominantly
abundant in the adjacent forest to the VJR.
Fifthly, as was the scenario in VJR Timbah, many
of the small VJRs in Sabah may still maintain
their undisturbed forest stand structures and
tree compositions. If so, these VJRs still reserve
important information on the pre-disturbance
stand structures and tree compositions of the
disturbed forests in adjacent areas to them.
Therefore, future studies on the stand structures
and species compositions of the forests in these
VJRs are highly encouraged so that this
information can be used in the management of
the disturbed forests.
ACKNOWLEDGEMENTS
I would like to thank Prof. Dato' Dr Abdul Latiff
Mohamad of Universiti Kebangsaan Malaysia
for his constructive suggestions, which have
improved this paper significantly.
REFERENCES
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R. Schnaeckel, G. H. Petol, L. Madani and
C. E. Ridsdale. 2005. Secondary
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Fox, J. E. D. 1967. An enumeration of lowland
dipterocarp forest in Sabah. The Malayan
Forester. 30: 263 – 279.
Fox, J. E. D. 1972. The natural vegetation of
Sabah and natural regeneration of the
dipterocarp forests. PhD thesis. University
of Wales, Wales.
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Manokaran, N. and M. D. Swaine. 1994.
Population dynamics of trees in dipterocarp
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Madani and C. E. Ridsdale. 1999. Primary
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forest at Danum Valley, Sabah, Malaysia and
the role of the understorey. Philosophical
Transactions of the Royal Society, London
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Newbery, D. M., E. J. E. Campbell, J. Proctor
and M. J. Still. 1996. Primary lowland
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patterns in the understorey. Vegetatio. 122:
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Newbery, D. M., E. J. F. Campbell, Y. F. Lee, C.
E. Ridsdale and M. J. Still. 1992. Primary
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Palmiotto, P. A., S. J. Davies, K. A. Vogt, M. S.
Ashton, D. J. Vogt and P. S. Ashton. 2004.
Soil related habitat specialization in
dipterocarp rain forest tree species in
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Sabah Forestry Department. 2006. Forest
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and R. C. Ong. 2005. Floristic
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STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH
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– 1 December 2005. pp 29 – 52.
Soepadmo, E. and K. M. Wong. (Eds.). 1995.
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(Eds.). 2002. Tree Flora of Sabah and
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JANUARIUS GOBILIK
63
Appendix 1: Species composition; N = Number of individuals; D = Density (trees ha–1); Rd = Relative
density; Rba/ha = Relative basal area per hectare of trees > 5 cm DBH in the study plots; Max DBH =
Maximum DBH (cm); Total = 2,369
Species
Family
N
Actinodaphne sp.
Adinandra dumosa
Aglaia spp,
Alangium javanicum
Alseodaphne sp.
Antidesma leucopodum
Aporusa elmerii
Aporusa grandistipulata
Aporusa spp,
Aquilaria malaccensis
Archidendron jiringa
Ardisia elliptica
Artocarpus anisophyllus
Artocarpus dadah
Artocarpus elasticus
Artocarpus kemando
Artocarpus spp,
Artocarpus tamaran
Atuna cordata
Atuna sp.
Baccaurea latifolia
Baccaurea macrocarpa
Baccaurea parviflora
Baccaurea spp,
Barringtonia macrostachya
Barringtonia spp,
Barringtonia stipulata
Beilschmiedia sp.
Blumeodendron tokbrai
Calophyllum spp,
Canarium odontophyllum
Canarium sp.
Castanopsis motleyana
Chionanthus pluriflorus
Chisocheton pentandrus
Chisocheton sp.
Cleistanthus megacarpus
Cratoxylum cochinchinense
Croton oblongus
Crypteronia griffithii
Cryptocarya spp,
Dacryodes costata
Dehassia incrassata
Dillenia excelsa
Dimocarpus sp.
Diospyros discocalyx
Diospyros elliptifolia
Diospyros spp,
Diploknema sebifera
Lauraceae
Theaceae
Meliaceae
Alangiaceae
Lauraceae
Euphorbiaceae
Euphorbiaceae
Euphorbiaceae
Euphorbiaceae
Thymelaeaceae
Leguminosae
Myrsinaceae
Moraceae
Moraceae
Moraceae
Moraceae
Moraceae
Moraceae
Chrysobalanaceae
Chrysobalanaceae
Euphorbiaceae
Euphorbiaceae
Euphorbiaceae
Euphorbiaceae
Lecythidaceae
Lecythidaceae
Lecythidaceae
Lauraceae
Euphorbiaceae
Clusiaceae
Burseraceae
Burseraceae
Fagaceae
Oleaceae
Meliaceae
Meliaceae
Euphorbiaceae
Hypericaceae
Euphorbiaceae
Crypteroniaceae
Lauraceae
Burseraceae
Lauraceae
Dilleniaceae
Sapindaceae
Ebenaceae
Ebenaceae
Ebenaceae
Sapotaceae
3
3
12
9
4
2
21
3
10
1
2
2
2
6
1
7
10
1
6
3
5
18
16
26
5
26
3
4
1
29
2
3
15
1
2
3
2
1
1
3
12
3
3
1
6
4
3
38
3
D
Rd
(%)
Rba/ha
(%)
Max
DBH
DBH's
mode
1
1
4
3
1.3
0.7
7
1
3.3
0.3
0.7
0.7
0.7
2
0.3
2.3
3.3
0.3
2
1
1.7
6
5.3
8.7
1.7
8.7
1
1.3
0.3
9.7
0.7
1
5
0.3
0.7
1
0.7
0.3
0.3
1
4
1
1
0.3
2
1.3
1
12.7
1
0.1
0.1
0.5
0.4
0.2
0.1
0.9
0.1
0.4
0.0
0.1
0.1
0.1
0.3
0.0
0.3
0.4
0.0
0.3
0.1
0.2
0.8
0.7
1.1
0.2
1.1
0.1
0.2
0.0
1.2
0.1
0.1
0.6
0.0
0.1
0.1
0.1
0.0
0.0
0.1
0.5
0.1
0.1
0.0
0.3
0.2
0.1
1.6
0.1
0.1
0.0
0.4
0.1
0.0
0.0
0.2
0.0
0.1
0.1
0.0
0.0
0.3
0.3
0.3
0.2
0.1
0.0
0.1
0.0
0.2
0.4
0.1
0.5
0.1
0.3
0.1
0.3
0.1
0.6
0.0
0.0
0.9
0.0
0.0
0.0
0.0
0.0
0.0
0.1
0.5
0.0
0.0
0.0
0.2
0.0
0.0
0.6
0.0
42.7
16.6
44.6
20.4
17.8
22.0
21.7
10.2
18.8
29.0
9.9
8.3
70.0
45.2
71.0
32.5
33.1
11.8
18.2
13.1
38.2
42.0
13.7
37.3
26.1
29.0
26.8
53.5
32.2
55.4
14.0
9.9
70.0
7.3
11.8
10.8
13.4
25.5
7.6
25.8
59.2
14.0
22.0
14.0
44.9
7.6
17.5
53.2
10.2
6.4
6.1
22.3
6.4
5.4
6.7
8.6
5.7
9.6
29.0
6.4
8.0
7.6
7.0
71.0
7.6
6.4
11.8
8.6
8.3
7.0
7.0
5.7
6.4
10.2
6.7
12.4
12.1
32.2
6.1
9.2
6.7
6.7
7.3
5.4
7.0
10.8
25.5
7.6
17.5
6.1
5.7
8.0
14.0
7.6
5.1
9.2
7.0
6.1
64
STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH
Species
Family
Dipterocarpus acutangulus
Dipterocarpus applanatus
Dipterocarpus caudiferus
Dipterocarpus confertus
Dipterocarpus globosus
Dipterocarpus pachyphyllus
Dipterocarpus spp,
Dipterocarpus stellatus
Dryobalanops beccarii
Dryobalanops keithii
Dryobalanops lanceolata
Drypetes longifolia
Drypetes sp.
Durio grandiflorus
Durio spp,
Dyera costulata
Dysoxylum sp.
Elaeocarpus stipularis
Elateriospermum tapos
Eurycoma longifolia
Ficus sp.
Fordia splendidissima
Ganua kingiana
Ganua sarawakensis
Garcinia mangostana
Garcinia parvifolia
Garcinia parvifolia
Gironniera nervosa
Gluta oba
Gluta spp,
Gluta swintonia
Gonystylus bancanus
Gymnacranthera spp,
Heritiera spp,
Hopea beccariana
Hopea nervosa
Hopea pentanervia
Hydnocarpus borneensis
Hydnocarpus woodii
Irvingia malayana
Knema laurina
Koompassia excelsa
Koompassia malaccensis
Koordersiodendron pinnatum
Lansium domesticum
Lithocarpus echinifer
Lithocarpus spp,
Litsea spp,
Lophopetalum beccariana
Lophopetalum javanicum
Lophopetalum sp.
Macaranga sp.
Macaranga winkleri
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Euphorbiaceae
Euphorbiaceae
Bombacaceae
Bombacaceae
Apocynaceae
Meliaceae
Elaeocarpaceae
Euphorbiaceae
Simaroubaceae
Moraceae
Leguminosae
Sapotaceae
Sapotaceae
Clusiaceae
Clusiaceae
Euphorbiaceae
Ulmaceae
Anacardiaceae
Anacardiaceae
Anacardiaceae
Thymelaeaceae
Myristicaceae
Sterculiaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Flacourtiaceae
Flacourtiaceae
Simaroubaceae
Myristicaceae
Leguminosae
Leguminosae
Anacardiaceae
Meliaceae
Fagaceae
Fagaceae
Lauraceae
Celastraceae
Celastraceae
Celastraceae
Euphorbiaceae
Euphorbiaceae
N
5
1
14
4
4
10
43
20
102
1
4
5
6
24
22
2
1
3
5
2
1
19
10
1
3
16
1
1
20
26
4
12
43
32
2
7
1
17
10
4
38
2
3
1
1
1
11
18
1
6
3
1
5
D
1.7
0.3
4.7
1.3
1.3
3.3
14.3
6.7
34
0.3
1.3
1.7
2
8
7.3
0.7
0.3
1
1.7
0.7
0.3
6.3
3.3
0.3
1
5.3
0.3
0.3
6.7
8.7
1.3
4
14.3
10.7
0.7
2.3
0.3
5.7
3.3
1.3
12.7
0.7
1
0.3
0.3
0.3
3.7
6
0.3
2
1
0.3
1.7
Rd
(%)
0.2
0.0
0.6
0.2
0.2
0.4
1.8
0.8
4.3
0.0
0.2
0.2
0.3
1.0
0.9
0.1
0.0
0.1
0.2
0.1
0.0
0.8
0.4
0.0
0.1
0.7
0.0
0.0
0.8
1.1
0.2
0.5
1.8
1.4
0.1
0.3
0.0
0.7
0.4
0.2
1.6
0.1
0.1
0.0
0.0
0.0
0.5
0.8
0.0
0.3
0.1
0.0
0.2
Rba/ha
(%)
1.6
0.0
0.2
0.0
1.0
1.8
4.5
2.6
14.6
0.0
1.1
0.1
0.1
0.3
1.6
0.1
0.0
0.0
0.0
0.0
0.0
0.0
0.1
0.1
0.1
0.2
0.0
0.0
0.5
0.3
0.1
0.1
0.4
2.4
0.6
0.2
0.0
0.2
0.6
0.1
0.4
0.0
0.5
0.0
0.0
0.0
0.3
0.8
0.0
0.2
0.0
0.0
0.1
Max
DBH
109.2
14.6
33.8
10.5
112.0
112.0
125.0
95.9
180.0
17.2
98.0
26.8
25.5
28.0
125.0
35.4
15.0
15.0
10.5
6.7
10.5
10.2
22.0
42.7
26.4
26.1
4.8
5.1
39.5
29.9
34.1
20.1
33.1
79.3
75.0
29.9
5.7
28.3
80.0
27.1
22.3
9.2
69.0
20.1
6.4
20.4
36.3
78.0
22.9
35.4
8.9
5.7
19.1
DBH's
mode
38.2
14.6
4.8
9.2
13.4
9.9
6.1
12.4
5.7
17.2
4.8
5.4
6.7
9.6
29.6
18.5
15.0
10.2
6.4
4.8
10.5
5.4
6.4
42.7
12.4
5.4
4.8
5.1
7.0
5.7
5.1
5.1
8.3
8.9
59.2
9.2
5.7
4.8
5.1
9.6
10.2
8.3
24.5
20.1
6.4
20.4
10.2
7.3
22.9
9.9
8.0
5.7
8.9
JANUARIUS GOBILIK
65
Species
Family
Madhuca sp.
Magnolia sp.
Mallotus muticus
Mallotus pinangensis
Mallotus spp,
Mallotus stipularis
Mallotus wrayi
Mangifera pajang
Mangifera sp.
Melanochyla beccariana
Melicope luna-akenda
Meliosma sumatrana
Memecylon laevigatum
Mesua macrantha
Microcos crassifolia
Microcos spp,
Myristica spp,
Nauclea sp.
Neesia spp,
Nephelium lappaceum
Ochanostachys amentacea
Orophea sp.
Palaquium rostratum
Parashorea malaanonan
Parashorea tomentella
Parinari sp.
Parishia insignis
Payena accuminata
Payena macrophylla
Peltophorum racemosum
Pentace adenophora
Pentace laxiflora
Pentace sp.
Pentaspadon motleyana
Pleiocarpidia sandakanica
Polyalthia spp,
Polyalthia sumatrana
Pternandra coerulescens
Ryparosa acuminata
Santiria sp.
Scaphium sp.
Scorodocarpus borneensis
Shorea accuminatissima
Shorea argentifolia
Shorea falciferoides
Shorea fallax
Shorea gibbosa
Shorea hypoleuca
Shorea laevis
Shorea leprosula
Shorea macrophylla
Shorea macroptera
Shorea mecistopteryx
Shorea ovalis
Sapotaceae
Magnoliaceae
Euphorbiaceae
Euphorbiaceae
Euphorbiaceae
Euphorbiaceae
Euphorbiaceae
Anacardiaceae
Anacardiaceae
Anacardiaceae
Rutaceae
Sabiaceae
Melastomataceae
Clusiaceae
Tiliaceae
Tiliaceae
Myristicaceae
Rubiaceae
Bombacaceae
Sapindaceae
Olacaceae
Annonaceae
Sapotaceae
Dipterocarpaceae
Dipterocarpaceae
Chrysobalanaceae
Anacardiaceae
Sapotaceae
Sapotaceae
Leguminosae
Tiliaceae
Tiliaceae
Tiliaceae
Anacardiaceae
Rubiaceae
Annonaceae
Annonaceae
Melastomataceae
Flacourtiaceae
Burseraceae
Sterculiaceae
Olacaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
N
1
4
3
6
66
24
14
3
2
4
3
1
1
11
2
21
122
6
12
10
2
7
4
7
5
3
3
3
7
1
10
5
1
2
7
60
16
45
4
4
6
3
3
6
3
17
6
2
2
4
9
20
36
10
D
0.3
1.3
1
2
22
8
4.7
1
0.7
1.3
1
0.3
0.3
3.7
0.7
7
40.7
2
4
3.3
0.7
2.3
1.3
2.3
1.7
1
1
1
2.3
0.3
3.3
1.7
0.3
0.7
2.3
20
5.3
15
1.3
1.3
2
1
1
2
1
5.7
2
0.7
0.7
1.3
3
6.7
12
3.3
Rd
(%)
0.0
0.2
0.1
0.3
2.8
1.0
0.6
0.1
0.1
0.2
0.1
0.0
0.0
0.5
0.1
0.9
5.1
0.3
0.5
0.4
0.1
0.3
0.2
0.3
0.2
0.1
0.1
0.1
0.3
0.0
0.4
0.2
0.0
0.1
0.3
2.5
0.7
1.9
0.2
0.2
0.3
0.1
0.1
0.3
0.1
0.7
0.3
0.1
0.1
0.2
0.4
0.8
1.5
0.4
Rba/ha
(%)
0.0
0.0
0.1
0.1
0.3
0.1
0.1
0.0
0.0
0.0
0.0
0.0
0.0
0.5
0.0
0.1
2.8
0.1
0.3
0.1
0.0
0.2
0.1
0.5
1.0
0.1
0.0
0.1
0.0
0.0
0.1
0.1
0.0
0.2
0.2
0.6
0.2
1.1
0.1
0.3
0.4
0.2
0.0
1.7
0.2
0.5
0.6
1.1
1.1
0.3
0.3
1.0
4.5
0.1
Max
DBH
24.2
13.4
36.0
17.2
14.6
13.7
13.7
18.8
19.4
20.1
13.7
6.4
8.9
37.9
10.5
21.7
70.0
26.1
38.9
31.2
21.3
51.6
30.6
75.0
84.0
24.2
8.3
39.5
15.6
15.9
22.3
25.8
9.9
39.2
41.4
24.2
28.3
38.2
22.9
52.5
64.6
43.3
24.2
89.0
42.0
40.8
90.0
99.0
104.0
68.5
41.4
58.6
170.0
24.5
DBH's
mode
24.2
8.9
7.6
4.8
7.6
5.4
4.8
7.0
9.6
7.0
8.6
6.4
8.9
37.9
5.7
9.6
10.8
9.6
7.3
10.2
11.5
5.4
13.4
5.4
11.8
7.0
5.1
9.9
7.0
15.9
12.1
10.2
9.9
28.3
6.1
8.9
8.0
6.1
6.4
5.7
6.7
11.8
5.7
13.4
6.4
7.3
8.9
82.0
75.0
5.4
5.4
12.4
10.5
4.8
66
STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH
Species
Family
Shorea parvifolia
Shorea pauciflora
Shorea smithiana
Shorea spp,
Shorea superba
Shorea waltonii
Shorea xanthophylla
Sindora beccariana
Stemonurus scorpioides
Syzygium spp,
Teijsmanniodendron
bogoriensis
Teijsmanniodendron
holophyllum
Teijsmanniodendron
pteropodum
Teijsmanniodendron
simplicifolium
Terminalia sp.
Trigonobalanus verticillata
Trigonopleura malayana
Triomma malaccensis
Unidentified taxon
Unidentified taxon
Unidentified taxon
Unidentified taxa
Urophyllum spp,
Vatica dulitensis
Vatica oblongifolia
Vatica spp,
Xanthophyllum ellipticum
Zizyphus angustifolius
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Leguminosae
Icacinaceae
Myrtaceae
Verbenaceae
N
D
Rd
(%)
Rba/ha
(%)
Max
DBH
DBH's
mode
1
2
3
59
5
1
4
4
6
180
1
0.3
0.7
1
19.7
1.7
0.3
1.3
1.3
2
60
0.3
0.0
0.1
0.1
2.5
0.2
0.0
0.2
0.2
0.3
7.6
0.0
0.4
1.2
0.0
11.3
0.1
0.7
0.0
0.7
0.1
4.5
0.0
78.3
135.0
17.2
140.0
29.6
105.0
17.5
90.0
15.6
72.0
14.6
78.3
19.1
6.4
6.4
5.4
105.0
8.0
12.1
8.0
10.2
14.6
Verbenaceae
22
7.3
0.9
0.5
36.9
6.1
Verbenaceae
6
2
0.3
0.1
22.0
11.1
Verbenaceae
29
9.7
1.2
0.4
34.7
5.4
4
3
3
9
40
58
16
227
34
16
11
25
10
5
1.3
1
1
3
13.3
19.3
5.3
75.7
11.3
5.3
3.7
8.3
3.3
1.7
0.2
0.1
0.1
0.4
1.7
2.4
0.7
9.6
1.4
0.7
0.5
1.1
0.4
0.2
0.0
0.1
0.0
0.0
0.7
0.6
0.6
8.4
0.4
0.3
0.2
0.5
0.5
0.3
8.0
25.2
13.4
11.1
41.1
28.7
51.6
92.0
29.9
48.4
25.8
31.8
72.0
46.8
6.1
25.2
9.6
7.0
7.3
5.7
10.2
6.1
7.0
5.4
6.4
9.6
5.7
20.1
Combretaceae
Fagaceae
Euphorbiaceae
Burseraceae
Burseraceae
Lauraceae
Sapotaceae
Other trees
Rubiaceae
Dipterocarpaceae
Dipterocarpaceae
Dipterocarpaceae
Polygalaceae
Rhamnaceae
JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 67 – 80, 2008
Research Article
Preliminary molecular phylogeny of Bornean Plagiostachys (Zingiberaceae)
based on DNA sequence data of internal transcribed spacer (ITS)
Avelinah JULIUS¹*, Monica SULEIMAN² and Atsuko TAKANO³
¹Tropical Forest Biodiversity Centre, Forest Research Institute Malaysia,
52109 Kepong, Selangor, Malaysia
E-mail: plagiovel80@yahoo.com
²Institute for Tropical Biology and Conservation,
Universiti Malaysia Sabah, Locked Bag 2073, 88999 Kota Kinabalu, Sabah, Malaysia
³Museum of Nature and Human Activities Hyogo,
6 Chome, Yayoigaoka, Sanda, Hyogo 669-1546, Japan
ABSTRACT
A molecular phylogenetic analysis based on
DNA sequence data of internal transcribed
spacer region (ITS 1, ITS 2) and 5.8S gene and
re-evaluation of morphological characters were
performed in order to examine the relationships
of Plagiostachys and related genera, and to
elucidate the previous informal grouping of
Bornean Plagiostachys. A total of 111 taxa,
including 25 taxa of Plagiostachys were included
in the analysis. The strict consensus tree (length
= 1094; CI = 0.482; HI = 0.518) showed that
Plagiostachys consisted a strong supported
(BS = 96%) clade with some Alpinia species
that belong to section Alpinia. However, species
of Plagiostachys comprised three subclades (A,
B and C) and each subclade was moderately to
strongly supported with relatively high
bootstrap values. The three subclades of
Plagiostachys were also recognized
morphologically by the combination of
inflorescence and capsule characters. Poor
resolved tree prevent us to conclude
phylogenetic status of the genus
Plagiostachys, but at the moment we propose
Keywords: Bornean, phylogeny, Plagiostachys,
Zingiberaceae
this genus remain an independent genus and
wait for further analysis. Previous informal
grouping of Bornean Plagiostachys was not
supported from both molecular and
morphological analyses.
INTRODUCTION
Plagiostachys Ridl., is relatively small but
complex genus in Zingiberaceae. It is distributed
mainly in the Malesian region with the centre of
diversity in Borneo, where currently 10 species
of Plagiostachys are known. The genus is
distinguished from the other genera in
Zingiberaceae by the tightly congested,
apparently lateral inflorescence, which is, in fact,
terminal on the short stem of the leafy shoots,
and usually breaks through the leaf sheaths just
above ground level or sometimes in the middle
(Smith, 1990). The flower is subtended by a
usually tubular bracteole, and the labellum is
small and rather fleshy, with diverged venation
of petaloid in some species. The bracteoles and
flowers are very mucilaginous and tend to decay
within one day in some species. Such a
mucilaginous nature makes herbarium works
difficult, therefore relatively few studies have
been done in this genus (Smith, 1985; Cowley,
68
PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS
1999; Sakai & Nagamasu, 2003; Gobilik et al.,
2005). In order to study Plagiostachys,
collecting sufficient number of spirit specimens
of flowers, inflorescences and observations of
morphological characters in the field or a living
status are vital.
Smith (1985) divided the Bornean Plagiostachys
into two informal groups, Group 1 and Group 2
(Table 1). Species belonging to Group 1 have
bilobed ligule, mucilaginous inflorescence,
distinctly tubular and early decaying bracteoles,
yellow and white with some pink flowers, fleshy
and soon-decaying calyx, style that adnate to
corolla wall, and oblong-pyriforms capsules. On
the other hand, species of Group 2 have
truncate or emarginate ligule, tubular at base or
open bracteoles, pinkish-red with yellow
labellum flowers, papery calyx, style that free
from the corolla wall, and globose capsules. The
grouping was, however, disputed by Cowley
(1999) and Sakai & Nagamasu (2003) as the
characters used for the grouping did not fit with
any species described recently. Cowley (1999)
mentioned that the characters of the ligule, style
and capsule of P. parva J. Cowley belonged to
Smith’s Group 1, whereas characters of the calyx,
bracteole and non-mucilaginous nature of the
inflorescence belonged to Group 2. Another
species, P. breviramosa J. Cowley differed from
Smith’s Group 2 by its adnated style to the
corolla tube, non-globose capsule and bilobed
ligule. Similarly, the species described recently
by Gobilik et al. (2005), i.e. P. lasiophylla Gobilik
& A. L. Lamb and P. oblanceolata Gobilik & A.
L. Lamb also belong to neither Smith’s groups.
Although Gobilik et al. (2005) placed their two
new species in Smith’s Group 2 on the basis of
the not mucilaginous inflorescences, but the
characters of the style, capsule shape and ligule
Table 1: Characters used for the classification of the genus Plagiostachys (after Smith, 1985)
Character
Group 1
1. Inflorescence Mucilaginous
Group 2
Non-mucilaginous
2. Bracteole
Distinctly tubular, early decaying, Tubular at base or open, partially
only the very basal part remaining decaying or persistent at fruiting stage
3. Calyx
Fleshy, at least decaying in
upper part
Calyx not fleshy, not decaying
4. Style
Sometimes adnate to the wall of
the corolla tube above the
epigynous glands
Usually free from the wall of the
corolla-tube at the base
5. Capsule
Oblong-pyriform, angled, rarely
globose
Globose
6. Ligule
Bilobed
Truncate or emarginate, rarely bilobed
7. Floral colour Yellow and white with some pink
Pinkish-red with yellow labellum
AVELINAH JULIUS et al.
of these two species belong to Smith’s Group 1.
Thus, the reliability of Smith’s classification
became doubtful. Re-evaluation of these
morphological characters used for the informal
grouping and grouping itself should be needed.
Recent molecular phylogenetic analyses based
on DNA sequence data (plastid matK and
nuclear rDNA ITS) done by Kress et al. (2002,
2005 & 2007) and Pedersen (2004) confirmed that
Plagiostachys and Alpinia were sister group.
Kress et al. (2002, 2005 & 2007) also showed
that Amomum and Alpinia were polyphyletic
groups and Plagiostachys was embedded
within Alpinia. Plagiostachys was moderately
to strongly supported (BS>70%) as a
monophyletic group. Unfortunately only two
species of the genus were included in their
analyses, making the phylogenetic position of
Plagiostachys within Alpinioideae remained
inconclusive.
In this preliminary study, we examined
morphological characters of Plagiostachys used
for classification and analyzed DNA sequences
of the internal transcribed spacer (ITS) from an
expanded taxon sampling of the genus
Plagiostachys, together with related genera of
the Alpinioideae previously used in the
investigation of Kress et al. (2005) in order to
(1) resolve the position of Plagiostachys within
Alpinioideae, (2) evaluate the informal grouping
within Plagiostachys as proposed by Smith
(1985) and (3) evaluate the morphological
characters used in classification of the genus
with respect to our phylogenetic results.
MATERIALS AND METHODS
Morphological Study
Plant collection and observation were mainly
made during December 2003 to July 2004, late
February to early March and from November to
December 2005 in Sabah, Malaysia. These
specimens were deposited at BORH, HYO and
69
SAN. Additional materials, i.e. specimens and
digital images of specimens of Plagiostachys
(including type specimens) from BO, E, Fl, G,
IBSC, K, NHM and PR were also consulted.
Morphological attributes used in Smith’s
informal grouping were examined for the 17 taxa
of Plagiostachys: ligule, bracteole, floral colour,
calyx, style and capsule.
Taxon Sampling
The sources of plant material with voucher and
accession numbers are represented in Table 2.
The 19 taxa of Plagiostachys and three taxa of
Alpinia were newly sequenced. The expanded
sampling of Bornean Plagiostachys is well
represented by both Smith’s Group 1 and Group
2. In addition, 89 accessions including 58
species of Alpinia representing all six major
clades of Kress et al. (2005) were downloaded
from GenBank. In total 111 taxa were used for
the analysis. The tribe Riedelieae represented
by four genera (Burbidgea, Pleuranthodium,
Riedelia and Siamanthus) and the incertae
sedis Siliquamomum were selected as
outgroups.
Genomic DNA Extraction, PCR Amplification
and Sequencing
Fresh or silica gel dried leaf tissues were used for
total DNA extraction using a modified CTAB
(hexadecyltrimethyl-ammonium bromide) method
(Doyle & Doyle, 1987; Takano & Okada, 2002).
The entire ITS1-5.8S-ITS2 region was amplified
via polymerase chain reaction (PCR) using ITS5P
(5’-GGAAGGAGAAGTCGTAACAAGG-3’)
and ITS8P (5’-CACGCTTCTCCAGACTACA3’) of Möller & Cronk (1997). The thermal
cycling parameters were: initial denaturation at
94°C for 30 seconds, primers annealing at 48°C
for 2 minutes, and extension at 72°C for 45
seconds. A final extension at 72°C for 7 minutes
was done at the end of the amplification. PCR
products were then purified by using High Pure
PCR Product Purification kit (Roche Diagnostic
70
PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS
Table 2: List of taxa used in this study with information related to taxonomy, collections, vouchers and
GenBank accession number. Data are presented in the following sequence: Taxon name, Voucher (if available),
Collection site/ Source of DNA (if available) and GenBank accession numbers for ITS1, 5.8S and ITS2.
“¯ ” indicates voucher and collection site/ source of DNA is not available.
Outgroup:
Burbidgea nitida Hook.f., J. Mood 96p81, —, AF414494; B. pauciflora Valeton, S. Sakai 241
KYO, AB097253; B. pubescens Ridl., J. Mood 990, —, AF414495; B. schizocheila Hort., Rangsiruji
& M. Newman s.n. E, AY769821; B. stenantha Ridl., —, —, AJ388308; Riedelia sp., —, —,
AF478785; Pleuranthodium floccosum (Valeton) R. M. Sm., —, —, AY742333; P. trichocalyx
(Valeton) R. M. Sm., —, —, AY742332; Siamanthus siliquosus K. Larsen & J. Mood, Living
collection RBGE 20001319 E, Thailand, AY769820; Siliquamomum tonkinense Baill., Kress #006802 US, —, AF478791; Renealmia alpinia (Rottb.) Maas, Kress #99-6407 US, Tropical America,
AF478778; R. batternbergiana Bak., Kress #94-5277 US, Tropical Africa, AF478779.
Ingroup:
Aframomum luteoalbum K. Schum., A. D. Poulsen 708 AAU, Africa, AF414493; Afra. verrucosum
J.M. Lock, A. D. Poulsen 771 AAU, Africa, AF414492; Alpinia aenea Argent, G. Argent et al. 0016
E, Indonesia, AY769833; Alp. aquatica (Retz.) Roscoe, —, —, AY742335; Alp. arctiflora (F.
Muell.) Benth., —, —, AY742336; Alp. argentea (B. L. Burtt & R. M. Sm.) R. M. Sm., —, Sumatra,
AY742337; Alp. bilamellata Makino, —, —, AY742339; Alp. blepharocalyx K. Schum., Kress
#98-6136 US, AF478709; Alp. caerulea Benth., —, —, AY742342; Alp. calcarata Roscoe, Kress
#94-3675 US, China, AF478710; Alp. carolinensis Koidz., Kress #99-6404 US, Micronesia,
AF478711; Alp. conchigera Griff., Kress #00-6706 US, China, AF478712; Alp. cylindrocephala
K. Schum., —, —, AY742345; Alp. elegans K. Schum., Kress #99-6412 US, Philippines, AF478713;
Alp. eremochlamys K. Schum., —, —, AY742346; Alp. fax B. L. Burtt & R. M. Sm., —, —, AY742348;
Alp. formosana K. Schum., —, —, AY742350; Alp. foxworthyi Ridl., Kress #98-6293 US, Philippines,
AF478713; Alp. galanga (L.) Willd., Kress #94-5263 US, Ex hort. Hawaii, AF478715; Alp.
guangdongensis S. J. Chen & Z. Y. Chen, —, —, AY742352; Alp. haenkei C. Presl, —, —, AY742354;
Alp. hainanensis K. Schum., —, —, AY742355; Alp. hansenii R. M. Sm., A. Julius 155 BORH,
Sabah, DQ507828; Alp. havilandii K. Schum., Cultivated, Mountain Garden, K. Park, Sabah,
DQ507829, Alp. hookeriana Valeton, —, —, AY742356; Alp. intermedia Gagnep., Kress #97-5780
US, Japan, AF478716; Alp. japonica (Thunb.) Miq., ¯ , ¯ , AY742358; Alp. jianganfen T. L. Wu,
—, —, AY188289; Alp. ligulata K. Schum., ¯ , Borneo, AY742361; Alp. maclurei Merr., —, —,
AY742362; Alp. monopleura K. Schum., —, —, AY742363; Alp. nanchuanensis Z. Y. Zhu, —, —
, AY188290; Alp. napoensis H. Dong & G. J. Xu, —, —, AF254466; Alp. nigra (Gaertn.) B. L. Burtt,
—, —, AF254459; Alp. nieuwenhuizii Valeton, —, Sabah, DQ507830; Alp. novaepommeraniae K.
Schum., —, —, AY742368; Alp. nutans K. Schum., —, —, AY742369; Alp. officinarum Hance,
Kress #00-6614 US, China, AF478718; Alp. oxyphylla Miq., —, —, AY742372; Alp. pinetorum
Loes. AY742373; Alp. pinnanensis T. L. Wu & Senjen Chen, —, —, AF254470; Alp. polyantha
Fang, —, —, AY745692; Alp. pricei Hayata, —, —, AY742374; Alp. pumila Hook “f.”, Kress #976119 US, China, AF478719; Alp. rosea Elmer, —, Philippines, AY742377; Alp. rubricaulis K.
Schum., —, Sumatra, AY742378; Alp. rugosa J. -P. Liao ined., —, —, AY742379; Alp. sibuyanensis
Elmer, —, Philippines, AY742381;
AVELINAH JULIUS et al.
71
Table 2 continues:
Alp. species #2, —, —, AY742383; Alp. species #1, —, —, AY742382; Alp. stachyoides Hance, —
, —, AY742384; Alp. strobiliformis T. L. Wu & Senjen Chen var. glabra T. L. Wu, —, —, AF254471;
Alp. suishaensis Hayata, —, —, AY742385; Alp. tonkinensis Gagnep., —, —, AY742386; Alp.
vittata Bull., Kress #99-6415 US, Polynesia, AF478720; Alp. warburgii K. Schum., ¯ , Sumatra,
AY742388; Alp. zerumbet (Pers.) B. L. Burtt & R. M. Sm., ¯ , ¯ , AY742389;A. aff. calycodes Baker,
W. Baker 1051 K, Indonesia, AY769834; Amomum angustipetalum S. Sakai & Nagam., S. Sakai 389
KYO, Sarawak, AB097245; Amo. calyptratum S. Sakai & Nagam., S. Sakai 363 KYO, Sarawak,
AB097239; Amo. dimorphum M. F. Newman, S. Sakai 372 KYO, Sarawak, AB097244; Amo. durum
S. Sakai & Nagam., S. Sakai 362 KYO, Sarawak, AB097241; Amo. oliganthum K. Schum., S. Sakai
370 KYO, Sarawak, AB097243; Amo. roseisquamosum Nagam. & S. Sakai, S. Sakai 188 KYO,
Sarawak, AB097246, Amo. somniculosum S. Sakai & Nagam., S. Sakai 373 KYO, Sarawak, AB097247;
Amo. villosum Lour., Kress #01-6978 US, —, AF478724; Etlingera triorgyalis (Baker) R. M. Sm.,
L.B. Pedersen & B. Johans. 1065 C, —, AF414475; Etl. yunnanensis (T. L. Wu & Senjen Chen) R.
M. Sm., W.J. Kress 95-5511 US, —, AF414468; Hornstedtia gracilis R. M. Sm., J. Mood 996,
AF414482; H. hainanensis T. L. Wu & Senjen Chen, Kress #97-5769 US, —, AF478766; Leptosolena
haenkei C. Presl, —, —, AY742331; Plagiostachys albiflora Ridl. 1, A. Julius & P. Jimbau 2 BORH,
Sabah, DQ507835; P. albiflora Ridl. 2, A. Julius & A. Takano AT34 BORH, HYO, Sabah, DQ507834;
P. brevicalcarata Julius & A. Takano, A. Julius & A. Takano AT35 SAN, HYO, Sabah, DQ507839;
P. crocydocalyx (K. Schum.) B. L. Burtt & R. M. Sm., A. Julius & A. Takano AT1 SAN, HYO,
Sabah, DQ507837; P. glandulosa S. Sakai & Nagam., S. Sakai 374 KYO, Sarawak, AB097251; P.
lasiophylla Gobilik & A. L. Lamb, Cultivated. Sandakan, Sepilok, RDC, Evo. Trail, Sabah,
DQ507843; P. longicaudata Julius & A. Takano, A. Julius & A. Takano AT76 SAN, HYO, Sabah,
DQ507832; P. megacarpa Julius & A. Takano, A. Julius et al. AGS2 SAN, HYO, Sabah, DQ507844;
P. mucida Holttum, Khaw Siok Hooi 741 E, KEP, Malay Peninsula, AY769841; P. oblanceolata
Gobilik & A. L. Lamb, A. Julius et al. ATW34 BORH, HYO, Sabah, DQ507848; P. breviramosa
complex, A. Julius & A. Takano AT63 SAN, HYO, Sabah, DQ507842; P. parva J. Cowley, AMGB
1 BORH, SNP, Sabah, DQ507840; P. roseiflora Julius & A. Takano, A. Julius & A. Takano AT64
SAN, HYO, Sabah, DQ507846; P. strobilifera (Baker) Ridl. 1, A. Julius & A. Takano AT61 BORH,
Sabah, DQ507833; P. strobilifera (Baker) Ridl. 2, ¯ , Sabah, DQ507849; P. strobilifera (Baker)
Ridl. #3, S. Sakai 361 KYO, Sarawak, AB097252; P. parva complex, A. Julius & A. Takano AT65
SAN, HYO, Sabah, DQ507841; P. viridisepala Julius & A. Takano, A. Julius 198 SAN, HYO,
Sabah, DQ507838; P. species 3, Cultivated. Sandakan, Sepilok, RDC, Evo. Trail, Sabah, DQ507836;
P. odorata C. K. Lim, Kress #99-6330 US, Thailand, AF478772; P. species #1, Kress #00-6745US,
Sabah, AF478773; P. aff. albiflora, Khaw Siok Hooi 745 KEP & E, Peninsular Malaysia, AY769840
P. aff. megacarpa, A. Julius et al., ATS2 BORH, Sabah, DQ507845; P. aff. breviramosa complex, A.
Julius & A. Takano AT2 BORH, Sabah, DQ507831.
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PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS
GmbH, Germany). Automated sequencing was
conducted using ABI Prism® BigDyeTM
Terminator Ready Cycle Sequencing kits on an
Applied Biosystems HITACHI 3100 Genetic
Analyzer Automated Sequencer, using both the
PCR primers and another two internal primers,
ITS2K (5’-GGCACAACTTGCGTTCAAAG-3’)
(Rangsiruji et al., 2000) and ITS3P (5’GCATCGATGAAGAACGTA-3’) (Möller &
Cronk, 1997).
Phylogenetic Analysis
Following the published sequence of the 5.8S
rDNA gene and the ITS region in P. glandulosa
(AB097251), sequence boundaries of 5.8S rDNA
gene and both ITS1 and ITS2 regions of the 22
taxa yielded in this study were determined. The
aligned matrix was then submitted to the
GenBank with accession number from
DQ507828 to DQ507849. Clustal X version 1.8
(Thompson et al., 1997) was used for multiple
alignment of complete sequences with default
settings. Nucleotide composition and G+C
content were analyzed using MEGA Ver.3.0
(Kumar et al., 2004). Phylogenetic analysis was
performed using PAUP* Version 4.0b8
(Swofford, 2001). Characters were left unordered
and equally weighted. Maximum parsimony
(MP) analysis of the ITS sequence data was
conducted using heuristic search methods (10
Random Addition Replicates) with Tree
Bisection Reconnection (TBR) branch
swapping to find the most parsimonious trees,
COLLAPSE option in effect, MULTREES and
steepest descent options were not in effect. In
order to evaluate the relative support of the
clades, bootstrap analysis was executed using
1000 replicates heuristic with TBR.
RESULTS
Phylogenetic Analysis
Alignment of the sequences yielded a data
matrix of 640 total characters, of which 260 were
phylogenetically informative. The complete ITS
sequences of Plagiostachys varied in length
from 542 to 574 bp data matrix (without coded
gap). The length of ITS1 ranged from 159 to 164
bp with a GC content of 55.6%, the 5.8S ranged
from 183 to 186 bp and GC of 50.1%, while that
of ITS2 was greater and ranged from 198 to 226
bp with GC content of 58.6%.
The strict consensus of 100 equally
parsimonious trees with accompanying
bootstrap values were given in Figure 1 (length
= 1094; CI = 0.482; RC = 0.389). The homoplasy
index (HI) of the data was 0.518. As shown in
Figure 2, Plagiostachys made a strongly
supported clade (BS = 96%) with some Alpinia
species of Smith’s (1990) section Alpinia
subsections Cenolophon and Paniculatae. The
Plagiostachys can be further subdivided into
three major subclades (A, B and C) with
moderate to strong support (BS > 70%).
Subclade A composed of species found only in
Borneo and moderately supported with 76%
bootstrap value. Three small groups of species
can be found within this first subclade: (i) P.
lasiophylla, P. megacarpa Julius & A. Takano,
P. aff. megacarpa, P. oblanceolata, P. roseiflora
Julius & A. Takano, Plagiostachys sp. 3
(BS = 61%), (ii) three replicates of P. strobilifera
(BS = 64%), and (iii) P. parva, P. parva complex
and Plagiostachys sp. 2 (BS = 91%). Thirteen
taxa of Plagiostachys formed the moderatesupported subclade B with 72% bootstrap
value. Species consists within this second
subclade can be found in Borneo, Malay
Peninsula and Thailand. Three small groups of
species are found in Plagiostachys subclade B:
i) P. breviramosa complex and P. aff.
breviramosa (BS = 78%), ii) P. aff. albiflora and
Plagiostachys odorata C. K. Lim (BS=76%), and
iii) P. albiflora Ridl., P. brevicalcarata Julius &
A. Takano, P. glandulosa S. Sakai & Nagam., P.
longicaudata Julius & A. Takano, P. mucida
Holttum and Plagiostachys sp. 4 (BS = 75%).
The third well-supported subclade C composed
of two species, P. crocydocalyx (K. Schum.) B.
L. Burtt & R. M. Sm. and P. viridisepala Julius
& A. Takano, which are only found in Borneo
(BS = 99%).
AVELINAH JULIUS et al.
73
Figure 1: Strict consensus tree of 100 equally parsimonious trees with emphasis on the Plagiostachys
resulting from the ITS sequence data (length = 1094; CI = 0.483 excluding informative characters; HI=0.517)
showing bootstrap values from the parsimony analysis (above the line if > 50 %)
(Abbreviation: ITS = Internal Transcribed Spacer; CI = Consistency Index; HI = Heuristic Index)
74
PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS
Figure 2: The Plagiostachys + some species of Alpinia clade resulting from MP analysis (see Fig. 1). The
clade contains three subclades of Plagiostachys (subclades A, B and C) and few species of Alpinia from
section Alpinia. Bootstrap values for MP is shown above the line (if > 50 %)
(Abbreviation: Alp. = Alpinia; Plg. = Plagiostachys)
AVELINAH JULIUS et al.
75
MORPHOLOGICAL STUDY
DISCUSSION
The status of vegetative and floral characters
examined was summarized in Table 3. In each
character, it is stable within species. Only one
species, P. albiflora matched with Smith’s
criteria in all morphological status, however, the
rest of the species showed mixed character
status of groups 1 and 2 as in P. breviramosa
and P. parva.
Phylogenetic Position of Plagiostachys and its
Relationship with Related Genera
The present ITS analysis focused on
phylogenetic position of Plagiostachys showed
that the species of the genus are divided into
three major subclades A, B and C with 76%,
72% and 99% bootstrap supports respectively.
These subclades consist of strongly supported
clade with Alpinia nieuwenhuizii Valeton and
A. ligulata K. Schum. (BS = 98%) + A.
rubricaulis K. Schum., A. warburgii K. Schum.
and A. argentea B. L. Burtt & R. M. Sm
(BS = 54%) + A. hansenii R. M. Sm. and A.
havilandii K. Schum. (BS = 85%). Our result is
basically congruent with Kress et al. (2002, 2005
& 2007), since most of the members of the clade
are that of A. glabra clade of Kress et al. (2005),
together with A. hansenii and A. havilandii,
the newly analyzed taxa. The reason why these
two Alpinia were added was because both
species have lateral inflorescence as in
Plagiostachys. It is interesting both Alpinia also
become sisters taxa to Plagiostachys, since it
might indicate that the event having lateral
inflorescence had happened only in the
Plagiostachys + some species of Alpinia clade.
However, other Alpinia species in this clade
have a terminal inflorescence, and as shown in
Figure 2, subclades within the Plagiostachys +
some species of Alpinia clade are unresolved,
so the phylogenetic relationships among these
subclades of Plagiostachys’s and Alpinia’s
remain unknown. Therefore, we could not
discuss the evolution of lateral inflorescence
further. At least we could mention that the
species of Plagiostachys and Alpinia do not
mix up with each other in these subclades. By
adding more data such as extending the taxon
sampling on both Plagiostachys and Alpinia,
and employing more than one gene markers as
others did (e.g. ITS and trnL-F by
Ngamriabsakul et al., 2004; ITS and rps16 by
Pedersen, 2004; ITS and matK by Xia et al.,
Figure 3 shows the distribution of morphological
character status which was used by Smith (1985)
for informal groupings of Plagiostachys. As
suggested from this study, Plagiostachys is
subdivided into three major subclades (A, B and
C) with moderate to strong support (BS > 70%),
and each character used by Smith was scattered
into these three subclades: not mucilaginous
inflorescence was found in the species of
subclade A and part of subclade B, and
mucilaginous status was found in part of
subclade B and subclade C. Both character
status of ligule (bilobed vs. truncate), of
bracteole (distinctly tubular and early decaying
vs. tubular at base or open and persistent), of
style (adnate to vs. free from the corolla wall),
and of capsule (oblong-ovoid or pyriform vs.
globose) are also found in subclades A and B.
Instead, the hairiness of capsules seems to be
useful character: all species bearing glabrous
capsules were gathered in the subclade B, and
species with pubescent capsules were in the
subclades A and C. Therefore, the combination
of those inflorescence and hairiness of capsules
could be used to distinguish the three subclades:
the species of subclade A has not mucilaginous
inflorescence status and pubescent capsules,
those of subclade B show not – or mucilaginous
inflorescence but glabrous capsules, and those
of subclade C has mucilaginous inflorescence but
pubescent capsules.
76
Table 3: Comparison of some keys morphological characters for Bornean Plagiostachys
PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS
Table 3 Continues:
AVELINAH JULIUS et al.
77
78
PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS
2004), we could obtain more resolved tree and
answer how we should treat Plagiostachys in
the near future. At the moment, the possibility
of monophyly of Plagiostachys is still remain,
therefore we suggest to leave Plagiostachys as
an independent genus.
Evaluation of Smith’s Informal Grouping within
Bornean Plagiostachys
Our examination of morphological characters
used by Smith’s informal grouping (Tables 1 &
3) revealed that only one species could
completely satisfy her criteria. Additionally, the
molecular phylogenetic analysis showed that
Plagiostachys is divided into three subclades
with moderate to strong support and not
correspond to previous informal grouping (Fig.
3). Therefore, we conclude that Smith’s grouping
should no longer be used for Bornean
Plagiostachys as Cowley (1999) and Sakai &
Nagamasu (2003) suggested.
Evaluation of the Morphological Characters
Used for Classification in Plagiostachys
In molecular phylogenetic analysis, we found
three subclades in Plagiostachys: subclades A,
B and C (Fig. 2), and among morphological
characters examined, the status of ligule,
bracteole, floral colour and calyx were scattered
into these subclades (Fig. 3). This indicates these
characters are useful for species recognition but
less significant for infrageneric grouping. On
the contrary, combination of those inflorescence
(mucilaginous vs. not-mucilaginous) and
hairiness of capsules (pubescent vs. glabrous)
could be used to recognize the three subclades.
Smith (1985) used the shape of the capsule to
distinguish between groups 1 and 2, but did
not mention the hairiness of capsules. However,
as inflorescence character, also it could be a
useful character for classification.
ACKNOWLEDGEMENTS
We thank Januarius Gobilik (Forest Research
Centre, Sandakan, Sabah) for providing materials
of P. lasiophylla and Plagiostachys sp. 3, Prof.
Dr Menno Schilthuizen (National Museum of
Natural History ‘Naturalis’, Leiden), Dr Takuji
Tachi (Hokkaido University), Mr Liew Thor
Seng (UMS), Mrs Lam Nyee Fan (UMS), Mr
Freddy Disuk (UMS), Dr Suzan Benedict (UMS)
and Dr Nazirah Mustafa (UMS) for technical
assistance. We acknowledge Dr Hidetoshi
Nagamasu for providing invaluable comments
on the manuscript. Part of this study was based
on the Master’s thesis of Avelinah Julius, which
was submitted to Universiti Malaysia Sabah.
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proposed new infrageneric classification.
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(and other methods). Sunderland, MA:
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occurrences of triploid formation in
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JAYA
SEELAN
SATHIYA
SEELAN
et.al.
JOURNAL
OF TROPICAL
BIOLOGY
AND
CONSERVATION, 4 (1) : 81 – 97, 2008
81
Research Article
Bats (chiropteran) reported with Aspergillus species from Kubah National
Park, Sarawak, Malaysia
JAYA SEELAN Sathiya Seelan1, Faisal Ali ANWARALI KHAN2, SEPIAH Muid3, M.T.
ABDULLAH4
1
Institute for Tropical Biology and Conservation, Locked bag 2073, Universiti Malaysia
Sabah, 88999 Kota Kinabalu, Sabah, Malaysia
2
Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409-3131,
USA
3
Department of Plant Science and Environmental Ecology
Department of Zoology, Faculty of Resource Science and Technology, 94300 Kota
Samarahan, Sarawak, Universiti Malaysia Sarawak, Malaysia
4
ABSTRACT
A preliminary survey of chiropterans (bats)
with potential zoonotic fungi was conducted
as part of the Sowell-UNIMAS Expedition 2006.
This survey was conducted at Kubah National
Park, Matang, Sarawak from 14th to 16th August
2006. The main aim of this survey was to
document variety of fungal isolates from bats
external (ears) and internal (saliva and anal)
swabs. All of the fungi species were subjected
to both macroscopic and microscopic
observations to characterize their morphology.
Out of 23 species of bats observed, 13 (56.5%)
species were found to contain 17 fungi isolates
of the genus Aspergillus from five subgenera,
five sections and six species. The fungi isolates
were Aspergillus restrictus, A. sydowii, A.
fumigatus, A. niger, A. clavatus and A.
japonicus. The highest numbers of isolates
recorded was for A. restrictus with six isolates
followed by A. fumigatus and A. sydowii with
two isolates respectively. Where as, A. niger,
A. clavatus and A. japonicus each recorded with
one isolate only. Aspergillus fumigatus was the
Keywords: Aspergillus, bats, pathogenic, thermophilic
first record isolated from bats the samples (n =
64) from Sarawak. It was reported that this
isolate is a pathogenic and thermophilic (able
to grow up to 65°C) isolate which was found to
be on a lesion near ear opening of Hipposideros
cervinus. Further work should be done to
discover potential mycoflora in wildlife
mammals.
INTRODUCTION
Wildlife has been an important vector of
infectious diseases as they can transmit these
diseases to human through direct or indirect
contact. Today, zoonoses found in wildlife
constitute a major public health problem,
affecting all continents. Wild animals seem to
be involved in the epidemiology of most
zoonoses and serve as major reservoirs for
transmission of zoonotic agents to domestic
animals and humans (Frederick, 1998; Hilde
et al., 2004).
The importance of such zoonoses is
increasingly being recognized, and the needs
for more attention in this area have been widely
expressed (Hilde et al., 2004; Chomel et al.,
82
CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK
2007). Recent studies showed that wildlife
diseases were expanding in geographic range,
transferred from one host species to another,
increased in impact or severity, undergone a
change in pathogenesis, and might also have
emerged by recently evolved pathogens
(Lederberg et al., 1992; Krause, 1992; Krause,
1994; Daszak et al., 2000). Most of the outbreak
of new viruses and emergence of newly evolved
pathogens are known mainly from wildlife
population (Morse, 1993; Dobson &
Foufopoulos, 2001; Antia et al., 2003).
region (Raper & Fennell, 1977). Aspergillus
fumigatus is the most important group of fungi
as a cause of systemic human and animal
diseases (Raper & Fennell, 1965; 1977). Since
Aspergillus species can be found on many
different substrates, they have been
extensively studied from animal dung, lungs,
ears, intestinal, blood vessels, kidney, bladder,
brain and skin for pathogenic strains that leads
to fungal infections on wild animals
(Ainsworth, 1952). Among wildlife population,
several studies have been documented
different pathogenic fungi from different hosts
(Coon & Locke, 1968; Trevino, 1972; Kaliner &
Cooper, 1973; Tham & Purcell, 1974; Ramirez et
al., 1976; Peden & Richard, 1985; Speare et al.,
1994; Mancianti et al., 1997; Cork et al., 1999;
Monteros et al., 1999; Leotta et al., 2002).
Fungi are distributed worldwide, with particular
species being endemic in particular regions. The
species are grouped by natural environment
habitat as being primarily associated with
humans (anthrophilic), other animals
(zoophilic), or soil (geophilic) (Brandt &
Warnock, 2003). Zoosporic fungi are one of the
key areas around these issues that are
currently receiving more attention with regards
to the wildlife diseases and yet to be explored
as other charismatic pathogens (e.g. virus,
bacteria and protozoan). Worldwide distribution
of some common wild animal fungal diseases
such as Aspergillosis, Chytridiomycosis,
Coccidioimycosis, Cephalosporiosis and
Otomycosis have the potential to be a major
threat to human being as they starts to be
transmitted from animal to human (Gitter &
Austwick, 1962). Previous cases of fungal
infections in wild animals have caused
inflammatory lesions in the brains,
subcutaneous infections, urinary tract
infections, otitis, infraocular infections and
genital infections (Halloran, 1955; Conen et al.,
1962). For example, chytridiomycosis has
caused near extinction of some amphibians
(Dendrobates tinctorius) in Australia and other
parts of the world (Ells et al., 2003).
Bats have been shown to be both important
recidence and vectors of pathogens. Some of
the pathogens that have been recently reported
to be associated with this fauna were rabies
(Paez et al., 2003), European lyssavirus (Fooks
et al., 2002), Hendra (Halpin et al., 2000) and
Menangle (Bowden et al., 2001) in Australia,
Nipah and Tioman viruses in Malaysia (Chua
et al., 2002a and b), hantaviruses in Korea (Kim
et al., 1994) and etc. (Chua et al., 2005). With
respect to fungal pathogens, insectivorous bats
are known to be the prime contenders as
reservoirs of fungi such as Histoplasma
capsulatum,
Coccidioides
immitis,
Cryptococcus laurentii and Blastomyces
dermatitidis (Yamamoto et al., 1995; GarciaHermoso et al., 1997; Mattsson et al., 1999;
Bunnell et al., 2000). Besides from becoming
contagious to human, these diseases also have
resulted in mass mortalities, population
declines, and even extinctions in such wildlife
population (Wobeser, 1994).
Fungal species in wild animals (from samples
of tissues, saliva and anal swab) such as A.
fumigatus, A. terreus, A. restrictus, A.
versicolour and A. glaucus were the common
fungi that have been isolated from temperate
Viewing such a condition is important for both
human and wildlife, the present study has been
initiated in order to screen for pathogenic
strains of Aspergillus residing in bats of Borneo
Island. This genus is known to be commonly
JAYA SEELAN SATHIYA SEELAN et.al.
83
distributed in the environment as well as
pathogenic (Raper & Fennell, 1965; Klich, 2001).
ectoparasites from some specimens were
preserved in 75% ethanol.
MATERIALS AND METHODS
Bats were sampled in Kubah National Park,
Sarawak, Malaysian Borneo (01°36' 42.3"N 110°
26' 39.3"E – elevation 8-35 m) from 14th to 16th
August 2006. The study area was mainly
covered with mixed dipterocarp forest with a
small stream flowing through this park from Mt.
Serapi.
Anal, ear and saliva swabs were performed
using sterile cotton buds and inoculated into
screw-capped centrifuge tubes containing
900 μl of PBS buffer to prevent drying. Samples
were serially diluted 10-fold up to 10–5. Of the
10–3 to 10–5 dilution, 0.1 ml of aliquots were
spread on sabouroud’s agar plates. Three
replicates were prepared for each dilution and
incubated at 25°C and 37°C for five days. After
five days, the mycelia were transferred into
selective media for fungal identification.
Sampling Method
Fungi Identification
Ten mist-nets and four harp traps were set in
each night. Nets and traps were deployed at
night from 6.00 p.m. and were closed at 7.00
a.m. the following day. Nets were checked every
20 minutes during the first 6 hours. Harp traps
are much more independent, rarely any bat
caught in the pouch can escape and they are
not tangled (nor stressed), so these traps were
checked at least three times each night, so as
to make sure the animals were fine. Bats were
also sampled using scoop nets inside roosts
(like culverts).
The fungi isolates were grown on five different
media i.e., Czapek Yeast Extract Agar incubated
at 25°C (CYA25), CYA37 incubated at 37°C,
CY20S added with 20% sucrose incubated at
25°C, Czapek’s agar (CZ) and Malt Extract Agar
(MEA). For each culture, five plates were used
as replicates were made. Each plate was
inoculated at three points, equidistant from the
centre and incubated in the dark for seven days.
The strains were identified using current
universal identification keys described by
Raper & Fennell (1965) and Klich (2002).
All the samples were identified to species in
the field following the identification keys from
Payne et al. (1998); Corbet & Hill, (1992);
Kingston et al. (2006); and Khan (1986). A
maximum of five individuals per species were
taken as voucher specimens. An extra of
another three individual were collected for the
species, which is identified to have different
morphological attributes within the population.
Samples were then tagged and field standard
measurements were recorded. All specimens
were prepared as museum voucher specimens,
either as skin and skeletal or as fluid preserved
specimen. Tissue samples from liver and muscle
were preserved in lysis buffer (Longmire et al.,
1997) and ethanol vials, blood samples were
collected using Nobuto blood filter strips and
Microscopic Observation
Study Area
Microslide culture technique was used to
observe the micromorphological features of the
Aspergillus species. A small tuft of mycelium
and conidiophores were lifted from a young
section of the colony, placed in a drop of alcohol
on a microscope slide and gently teased out. A
drop of lactophenol blue or acid fuschin was
used as a stain. The appearance of foot cell,
conidiophores, presence of metulae
(sterigmata) and conidia were examined and
measurements were recorded. Images were
taken using digital camera.
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CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK
RESULTS
Thirteen species from a total of 23 species of
bats caught were found to host 17 Aspergillus
isolates. Isolates were identified to five
subgenera, five sections and six species. The
isolates were identified as A. restrictus, A.
sydowii, A. fumigatus, A. niger, A. clavatus and
A. japonicus (Figures 1– 6 ). Aspergillus
restrictus was recorded with the highest number
of isolates (six isolates), followed by A.
fumigatus (two isolates) and A. sydowii (two
isolates) and A. niger, A. japonicus and A.
clavatus were recorded with lowest number of
isolates (one each) (Table 1).
Fungal infection was observed near the ear
opening of a single insectivorous bat,
Hiposideros cervinus. This fungus was
incubated at 37°C and was confirmed that this
infection was due to the A. fumigatus.
Morphological characteristics of all the six
species isolated from the bats are described.
Table 1: Total number of Aspergillus species isolated from anal, ear and saliva of the bats
Family
Host Species Name
Pteropodidae
Cynopterus brachyotis
C. brachyotis
C. brachyotis
C. brachyotis
C. brachyotis
C. brachyotis
C. brachyotis
Penthetor lucasi
P. lucasi
P. lucasi
Balionycteris maculata
Hipposideridae
Hipposideros cervinus
H. cervinus
H. cervinus
H. cervinus
H. cervinus**
H. cervinus
H. cervinus
Rhinophidae
Rhinolopus sedulous
R. trifoliatus
Rhinolopus borneensis
Vespertilionidae
Myotis muricola
Glischropus tylopus
Fungal Species
Source
A. restrictus
A. restrictus
A. restrictus
A. restrictus
–
–
A. sydowii
A. restrictus
A. clavatus
A. fumigatus
A. sydowii
Anal
Anal
Ears
Ears
–
–
A. restrictus
–
A. fumigatus
–
–
Ears
Anal
Anal
Ears
Ears, anal
Anal
Ears, anal, saliva
No. of
No. of
Isolates
Isolates
1
1
1
1
0
0
1
1
1
1
2
0
0
1
0
4
0
0
A. japonicus
–
–
Anal
1
0
0
A. niger
–
Ears
1
0
**Detected with fungal infection; – is negative
JAYA SEELAN SATHIYA SEELAN et.al.
Aspergillus japonicus Saito
Subgenus: Circumdati Section: Nigri
Colony on Czapek’s yeast extract agar (CYA) 60
– 75 mm in diameter (7 days, 25°C), conidial heads
on this media was very dark brown to purple
brown or purple black; mycelium white to
yellowish; no sclerotia was observed; reverse
dull brown to purple brown; no exudates present;
colonies velutinous to slightly floccose, plane
to radially sulcate.
On CYA37, the colony diameter was 40 – 50 mm
in diameter (7 days, 37°C); reverse brown to
black, yellow to brown soluble pigment present;
slow growth colony and radially sulcate. On
CY20S, colony was rapidly growing and no
soluble pigment was observed. On MEA, this
isolate can grow about 70 – 80 mm in diameter (7
days, 25°C); conidial heads was brownish black;
mycelium yellow in colour. No growth at 5°C
and this isolate can grow moderately at 45°C.
Conidial heads were radiate; stipes 400 – 600
μm, smooth-walled, uncoloured. Vesicles 15 –
25 μm wide, globose shaped, uniseriate;
Phialides (4.5 – 7) × (3 – 4) μm, covering the
upper half of the vesicle. Conidia were globose
to subglobose, occasionally ellipsoidal,
measuring (3 – 4) × (4 – 5) μm, surface
echinulate. This isolate produces black spinose
conidia (Figure 1, pg. 88).
Aspergillus niger Tiegh
Subgenus: Circumdati Section: Nigri
Colony on Czapek’s yeast extract agar (CYA) 57
– 58 mm in diameter (7 days, 25°C), wrinkled,
dense and velutinous, exudates present, white
at first and becomes dark brown with forming of
conidial heads, reverse dark yellow.
Colony on malt extract agar (MEA) 52 – 56 mm
in diameter (7 days, 25°C) similar to those on
CYA but less dense and conidia in duller colours,
reverse dirty yellow. On Czapek’s, morphological
characters were similar to those on MEA. No
85
growth at 5°C. Growth at 37°C is exceptionally
rapid, colonies on CYA 38 – 40 mm in diameter
in three days. This strain can grow at 45°C.
Conidial apparatus develops as erect
conidiophores. Tips of conidiophores enlarge
and form vesicles with many phialides
producing conidia in long chains. Conidial
heads are compactly columnar, 40 – 48 μm in
diameter, black. Conidiophores are unbranched,
smooth and dark brown, stipes 200 – 300 μm × 3
– 4 μm in size. Vesicles are round to globose
shaped, 20 – 30 μm in diameter. Phialides
crowded dark brown, 5 – 7 μm long. Conidia are
globose to subglobose, roughened, hyaline and
often decidous spinules when young and
verruculose when it matures (Figure 2, pg. 88).
Aspergillus sydowii (Bain. & Sart.) Thom and
Church
Subgenus: Nidulantes Section: Versicolores
Colony on Czapek’s yeast extract agar (CYA) 20
– 40 mm in diameter (7 days, 25°C), heavily
sporulating in dark turquoise to dark green
colours, mycelium white, forming white conidial
heads, reverse reddish brown to maroon in
colour; exudates reddish brown to dark brown
when present; soluble pigment was maroon on
CYA; colony dense, velutinous to lanose,
radially sulcate.
Colony on malt extracts agar (MEA) 30 – 40 mm
in diameter (7 days, 25°C); conidia on MEA was
dark greenish after seven days; mycelium white;
colony texture granular and plane. Colony on
CY20S was similar to colonies on CYA
except exudates usually not formed and texture
was more floccose. Colony on CY37 was less
dense and the conidial colours less intense.
Colony on Czapek’s agar growing 30 – 40 mm
with close textured and velvety with crowded
conidiophores. No growth at 5°C. Growth at 37°C
is moderate. This strain cannot grow at 45°C.
Conidial apparatus develops as erect
conidiophores. Conidial heads are radiate, 100
86
CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK
– 150 μm in diameter, and white in colour. Stipes
(200 – 30) μm × (3 – 7) μm smooth, thick-walled
colourless, expanding into spathulate vesicles.
Vesicles are hyaline, radiate to spathulate
shaped, 6 – 15 μm in width; usually sterigmata
in two series (biseriate), metulae (4 – 5) × (2 – 3)
μm in diameter, phialides (5 – 7) × (2 – 3) μm.
Diminutive conidial structures produced by this
isolate, looks like penicillate heads. Conidia are
spherical, very rough to spinose, 3 – 4 μm in
diameter. Hulle cells present in this isolate
(Figure 3, pg. 88).
Aspergillus restrictus G. Smith
Subgenus: Aspergillus Section: Restricti
Colony on Czapek’s yeast extract agar (CYA)
4 – 8 mm in diameter (7 days, 25°C), Conidia on
CYA25 dull green to grey green; mycelium white
or inconspicuous; reverse uncoloured to brown;
exudates absent; colonies velutinous, centrally
floccose.
Colony on malt extract agar (MEA) 3 – 6 mm in
diameter (7 days, 25°C); conidia on MEA was
dark greenish after seven days; mycelium white;
reverse uncoloured to pale tan colour; irregular
margin. Conidia on CY20S, dark green,
mycelium inconspicuous, reverse uncoloured,
colony very slow growth, dense and plane.
Colony on Czapek’s agar growing 3 – 5 mm;
conidia dark green; mycelium inconspicuous,
slow growth and less sporulation. No growth at
5°C. Growth at 37°C is very slow. This strain
cannot grow at 45°C.
Conidial heads are columnar; conidiophores up
to (100 – 200) × (4 – 7) μm, smooth and
colourless, stipes (200 – 30) μm × (3 – 7) μm
smooth, uncoloured, expanding into pyriform
or hemispherical vesicles. Vesicles 8 – 18 μm in
wide; uniseriate to biseriate. Phialides (6 – 10) ×
(2 – 3) μm in diameter. Conidia are variable,
often cylindrical when borne, at maturity
ellipsoidal or pyriform, rough walled, (4 – 6) ×
(2 – 3) μm. (Figure 4, pg. 88).
Aspergillus fumigatus Fresenius
Subgenus: Fumigati Section: Fumigati
Colony diameter on CYA attaining about 50 –
75 mm (7 days at 25°C); conidia on this media
was dark blue greenish; mycelium white;
exudates absent; reverse uncoloured; soluble
pigment absent; texture floccose; heavy
sporulation.
On MEA, colony growth was about 50 – 60 mm
(7 days at 25°C); conidial colour was dark
bluish green; reverse uncoloured; texture as on
CYA25. On CY20S and Cz, the colony colour
was similar as in CYA25. Colony on CYA37 was
exceptionally rapid, heavy sporulation; conidia
colour was greyish green. This isolate cannot
grow at 5°C and able to grow until 65°C.
Conidial heads was columnar; conidiophores
uncoloured, smooth-walled (200 – 350)
× (6 – 10) μm, pyriform to spathulate vesicles.
Vesicles 15 – 28 μm in diameter; uniseriate;
phialides (5 – 7) × (2 – 3) μm, all phialides are
parallel to each other and the conidiophore axis.
Conidia globose to broadly ellipsoidal, smooth
to finely roughned, 2 – 2.5 μm in diameter
(Figure 5, pg. 89).
Aspergillus clavatus Desm
Subgenus: Clavati Section: Clavati
Colony on CYA (7 days at 25°C) was 40 – 45
mm; conidia dull green, dark turquoise or green;
mycelium white, inconspicuous to floccose;
exudates absent; reverse dull yellow to orange
brown in colour; colonies dense, radially
furrowed. Yellow soluble pigment present.
On MEA, colony attaining about 40 – 50 mm in
diameter (7 days at 25°C); conidia were dull green
to grey green in colour, irregularly distributed;
dark yellow soluble pigment present; mycelium
white, inconspicuous; colony thin and low
except for conidial areas more floccose. On
CY20S and CZ colonies were similar as those
on CYA 25. Colony on CYA (7 days at 37°C) was
JAYA SEELAN SATHIYA SEELAN et.al.
very slow, conidia less abundant. This isolate
cannot grow at 5°C and colony growth was
moderate at 37°C.
Conidial heads radiate, splitting into columns
when matured; conidiophores rose up to (1000
– 2000) × (15 – 30) μm, smooth-walled,
colourless, expanding slowly into clavate
a
b
87
vesicles. Vesicles 50 – 70 μm wide, smaller
vesicles, conidia zone extended from 30 – 175
μm down from the apices of the vesicles;
uniseriate, phialides (8 – 11) × (2 – 3) μm. Conidia
smooth-walled, ellipsoidal, occasionally pyriform, almost cylindrical, (3 – 5) × (3 – 3.5) μm
(Figure 6, pg. 89).
c
d
Figure 1: (a – b) Colonies on CYA at 25°C; 37°C; (c) Biseriate conidial head; (d) Conidia
a
b
c
d
Figure 2: (a – b) Colony on CYA at 25°C; 37°C; (c) Biseriate conidial head; (d) Conidia
a
b
c
d
Figure 3: (a – b) Colony on CYA at 25°C; colony on MEA at 37°C; (c) Conidial head; (d) Hulle cells
a
b
c
d
Figure 4: (a) Colony on CYA at 25°C; (b) Colony on MEA at 25°C; (c) Conidial head; (d) Biseriate
conidial head
88
CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK
a
d
b
c
e
f
Figure 5: (a – b) Colony on CYA at 25°C; 37°C; (c) Conidial heads columnar; (d – e) Uniseriate conidial
head; (f) Conidia shape globose
a
d
b
c
e
Figure 6: (a) Colony on MEA at 25°C; (b) Colony on CYA at 25°C; (c) Conidia shape ellipsoidal;
(d – e) Uniseriate conidial head
JAYA SEELAN SATHIYA SEELAN et.al.
DISCUSSIONS
In this preliminary study, six species of
Aspergillus were isolated from 13 species of
bats. As few studies have been conducted on
mycoflora from wild animals, all the Aspergillus
species recorded in this study were presumed
to be first record for this genus found in bats at
least in Sarawak, Borneo. Previous studies done
by Kuthubutheen & Webster (1986) have
isolated coprophilous fungi from the bats,
samba deer and elephants dung in the natural
environment. Furthermore, Candida lusitaniae
and Debaryomyces hansenii were isolated from
bat guano (Takashi et al., 2005). Several
pathogenic fungi from different bats species
were reported from Brazilian Amazon. In the
search of Paracoccidioides from the bats’
viscera, Silva-Vergara et al. (2005) have also
documented other types of mycoflora such as
Candida krusei, Trichosporum sp.,
Scytalidium sp., and one unidentified yeastlike fungus from liver, spleen and lungs of
frugivorus bats (Carollia perspicillata and
Sturnira lilium), Glossophaga soricina
(nectarivorous bats) and Desmodus rotundus
(hematophagous bat) respectively.
In another study by Koilraj et al. (1999) on the
distribution of Aspergillus in caves soil from
India, documented 13 different species of
Aspergillus such as A. niger, A. japonicus,
A. flavus, A. versicolour, A. tamarii, A. sydowii,
A. chevalieri, A. ochraceous, A. parasiticus,
A. fumigatus, A. terreus, A. wentii and
Aspergillus sp. Besides that, a study done by
Moraes et al. (2001), have proved that arthopod
vectors like Culex and Aedes have became as
carrier for the Aspergillus species like A. niger,
A. flavus, A. nidulans, A. fischerianus and
A. heteromorphus. Hence, the transmission of
the fungal spores in bats may be due to the
mosquitoes bites in their habitat where they
live in.
Although our sample size is not really large to
conclude statistically in which swab location
89
(ear, saliva or anal) contains the highest number
of Aspergillus species, but this preliminary data
showed that the most diversity of this fungus
were observed in anal swabs of frugivorous
bats. Thus, this indicates that various types of
substrates such as anal, ears, saliva and feaces
(guano) results different types of mycoflora in
the wild animal population. The high number
of fungal isolates documented in frugivorous
bats compared to insectivorous bats also does
show some correlation on food sources and
their roosting site with the number of fungus
isolated in this study.
Based on the morphological examinations, some
colony and microscopic characteristics of the
Aspergillus species were found to be different
from those stated by Raper & Fennell (1965)
and Klich (2002). For example, the colony
diameter of A. restrictus on CYA was smaller. It
was determined that the colony diameter of
A. restrictus ranged between 4.0 – 8.0 mm on
CYA and the diameter of the vesicles varied up
to 8 – 18μm. The most distinguishing property
of A. clavatus, dull green or grey green conidial
heads on MEA as stated by Raper & Fennel
(1965) was observed in this strain. At the same
time, a strong yellow soluble pigment present
on this media was another important new
characteristic that was observed in this study
probably might be a different strain.
Moreover, there was a similar morphological
characteristics were observed in A. japonicus,
A. niger, A. sydowii and A. fumigatus as
described by Raper & Fennell (1965), Samson
& Pitt (1990), Klich (2002). However, a
pathogenic strain of A. fumigatus that was
isolated from the Hipposideros cervinus
showed thermophilic properties as these
isolates able to survive under a wide range of
temperature (25 – 65°C). According to Gilman
(1959), A. fumigatus strains can grow rapidly
up to 35 – 60°C. This study showed that the
A. fumigatus isolated from Hipposideros
cervinus could grow up to 65°C.
90
CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK
In Borneo, the most widespread species of the
genus Aspergillus are A. niger Tieghem,
A. flavus Link, A. fumigatus Fres, A. ochraceus
Wilhelm, A. terreus Thom and A. wentii Wehmer
(personal communication). These isolates have
been isolated from different types of soil, plants
(fresh and senescent leaves), fruits, leaf litters,
water samples, food products, indoor and
outdoor environments. Thus, Aspergillus could
also be isolated from wild animal population
because it is thought that these species are more
adapted to the prevailing ecological conditions
(Sepiah, 1985; Jaya Seelan & Sepiah, 2006).
This study provides a comparative analysis on
Aspergillus species available in the
chiropterans samples from Kubah National Park
might be due to climatic agents such as flood
and air or wind which can help to introduce
fungal spores and mycelium into the cave
environment. Besides that, fungal spores might
also enter into cave through organic substances
such as plant which are carried into the cave
by trogloxenes (Cubbon, 1970).
Since bats are widely distributed in the cave
environment, fungal spores might cause
infection for bats when they are exposed or
even live as symbionts. Yamamoto et al. (1995)
investigated that the bat guano may mediate
the exchange of pathogenic fungi just as pigeon
excreta mediate the exchange of Cryptococcus
neoformans, the causal agent of
cryptococcosis.
Apart from that, fruits consumed by the
frugivore bats are also important factor in
understanding the ecology of bats. Sometimes
the infected fruit may contain pathogenic
microorganisms that present during the fruit
decay process (Sepiah, 1985). So, this would
be a key factor how the fungi are transmitted to
bats since frugivorous bats consume fruits as
their main diet.
CONCLUSION
This study has provided a preliminary list of
Aspergillus species found on chiropterans.
There were six species of Aspergillus
successfully isolated from the 13 species of bats.
This study has documented the diversity of
Aspergillus species in bats while
understanding the macro and microscopic
characteristic of this fungus cultured in different
media sources. Pathogenic strains of
microorganisms could be studied in order to
understand their host relationship and also
ecological significance in the wild animal
population in Malaysia. In general, this
preliminary analysis provides novel and basic
information on potential sources of mycoflora
from the wild animals in Borneo. Malaysian bats
may contain several novel fungi species and
may be of significant mycological interest.
Further study is needed in order to conserve
wild animals from emerging infectious diseases.
ACKNOWLEDGEMENTS
Authors would like to thank Universiti Malaysia
Sarawak (UNIMAS) and Texas Tech University
(TTU) for giving the opportunity to participate
in Sowell-UNIMAS Expedition 2006. The
authors are also grateful to Prof. Maren Klich
of the United States Agricultural Department
(USDA) and Prof. Jens Frisvad Denmark
Technical University (DTU) for providing
information on the Aspergillus species
identification. Authors would also like to thank
all members of all individuals participated in
Sowell-UNIMAS 2006 Expedition from TTU,
Faculty of Resource Science and Technology,
Sarawak Forest Department and Sarawak Forest
Cooperation.
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JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 99 – 107, 2008
Short Notes
Rapid assessment on the abundance of bird species utilising the Kota
Kinabalu Wetland Centre mangroves
Andy Russel MOJIOL1, AFFENDY Hassan1, Jocelyn MALUDA2 and Suzen IMMIT3
1
School of International Tropical Forestry, Universiti Malaysia Sabah, 88999 Kota
Kinabalu, Sabah
2
Kota Kinabalu Wetland Centre, Off Jalan Bukit Bendera Upper, 88400 Likas, Kota
Kinabalu, Sabah
3
Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, 88999
Kota Kinabalu, Sabah
ABSTRACT
INTRODUCTION
Kota Kinabalu Wetland Centre (KKWC)
mangroves have an essential role as a green
ecosystem in Kota Kinabalu. The aim of this
study was to assess the usefulness of mangrove
areas as a site for birdlife by estimating the
number of bird species and family, and the
population density of bird species. The most
frequent bird groups found in KK Wetland
Centre were waders (14.70%) followed by
herons, storks and bitterns (12.59%), raptors
(8.15%) and bulbuls (7.41%). The population
density of bird found in KKWC was between
12 – 17 birds/km2. The result shows an estimated
population of 3526 individuals from 83 species
of birds covering an area of 24 ha. As a
conclusion, this area is important as an urban
bird habitat in Kota Kinabalu. Conservation of
adequate and contiguous suitable mangrove
habitat may provide a sanctuary for bird to live
and feed between their territories. Ecological
improvements of green mangrove ecosystem
could be of immediate benefit to the bird
population.
Swamps, marshes and other wetlands that were
once regarded as useless to agricultural and
industrial development are now recognized for
their great values in recycling chemical and
biological materials, and especially for their rich
biological diversity. Wetlands filter pollutants,
act as reservoirs of nutrients in food chains,
produce forage for domestic animals and fuel
for humans, provide aesthetics, recreational and
cultural benefits to society and are habitats for
thousands of unique species of plants and
animals (Eric et al., 2000).
Keywords: Bird checklist, mangrove environment,
birdlife area, conservation and population density
The mangrove area is one type of wetlands and
in Sabah it consisted of 322,349 hectares which
most of them have been constituted as
Mangrove Forest Reserve (Sabah Forestry
Department, 2003). The ecological importance
of mangrove areas can hardly be overestimated
as they form the feeding and nursery grounds
for many species of birds and other invertebrate
species. Mangrove vegetation protects the
coastal areas from erosion and acts as a buffer
zone against tidal currents, floods and storms.
100
ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE
In wetland areas, birds are expected to be an
important resource as tourist attraction. Certain
species of birds are fully dependent on the
mangrove for their habitat and food. Birds play
important roles in maintaining wetlands
ecosystem which include being pollinators,
seed dispersers, pollution regulators providing
food for other animal predators, and also
contribute in nutrient recycling processes. Birds
are closely related to the habitat conditions.
Each species rarely occurs in only one type of
habitat. They are completely dependent on their
habitat, for cover and rich food resources.
Habitat type, size of the area, plant community
structure and landscape pattern can have a
great effect on bird community structure in a
given habitat (Wijesekara, 1999).
observation was made using a pair of binocular
(10 × 50). Each individual bird or groups of birds
seen or heard would be identified on the spot
using bird checklist book of Borneo (Mackinnon
& Phillipps, 1993). This point count method used
to record a variety of birds that provides a
uniform way of counting birds over time or
across locations. Point counts are a
standardized method (Ralph et al., 1993) of
assessing the diversity and abundance of birds
by counting (detected by hearing and by sight)
at points (Knapp & Keeley, 2001). In large areas,
allocated point counts can be used as
representative samples for the area. Point counts
are visited over a period of several days or
longer to assess how many and what types of
birds are found in an area.
The aim of this study was to conduct rapid
assessment on the density and abundance of
bird species utilising the Kota Kinabalu Wetland
Centre (KKWC) mangrove area.
A total of 32 sampling points were established
for bird survey in KKWC. Each point was
selected by considering/ marking every 100
metres walk from the provided transect
(boardwalk). At each point, the count was last
exactly five minutes. Then, waiting around 2 – 4
minutes at each point before counting.
MATERIALS AND METHODS
Secondary data were obtained from literature,
books and scientific reports available from
World Wildlife Fund (WWF-Kota Kinabalu) and
Sabah Wildlife Department. Secondly are from
field survey and observation as a complement
and confirmation to the mechanisms. For this
study, the chosen location is the mangrove areas
in KKWC which is located two kilometres northeast of Kota Kinabalu City centre. This location
was chosen due to the large diversity of birds
and in addition, it is a suitable location for tourist
attraction. KKWC, which covers an area of 24
hectares, is the only remaining patch of once an
extensive mangrove forest existed in much of
the area in the coastal town of Kota Kinabalu
(Fig. 1).
Seven days were spent in the field from 14th to
20th November 2005. Point count method had
been carried out and species of birds was
identified through their vocalization from 6 a.m.
to 11 a.m. and 4.30 p.m. to 6.30 p.m. The
Every bird species observed was recorded
between distances from the 10 – metre intervals
out to 100 metres. All individuals of all species
detected were counted, and a bird seen first was
distinguished from birds heard first. Horizontal
distance of the bird relative to the survey point
and the distance from above the ground were
recorded (Fig. 2). The abundance of bird was
analyzed using distance sampling following
Buckland et al. (2001).
RESULTS AND DISCUSSIONS
The total of bird species recorded in KKWC
during the survey were 83 species from 31
families and 60 genera (Appendix 1). The group
category was based from Clements (1991). The
highest abundance of bird group/class observed
was heron, storks and bitterns (10.4%), followed
by waders (8.9%), pigeons, doves and parrots
(5.2%) and kingfishers (3.7%). This group of
ANDY RUSSEL MOJIOL et al.
101
Figure 1: Location of Kota Kinabalu Wetland Centre
Source: Mapping Department Malaysia, 1998
102
ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE
Figure 2: Detailed point count plot for bird survey
birds, as exemplified by Purple Heron (Ardea
purpurea), Little Egret (Egretta garzetta),
Common Greenshank (Tringa nebularia),
Sandpiper (Actitis hypoleucos) and Cinnamon
Bittern (Ixobrychus cinnamomeus) that fed on
small fishes and crustaceans. The pigeon,
doves and parrots are usually seen above the
mangrove canopy that feed the mangrove flower
of Sonneratia alba, Avicennia alba and
Lumnitzera racemosa. While the kingfishers such
as the Common Kingfisher (Alcedo atthis), Blueeared Kingfisher (Alcedo meninting) and
Collared Kingfisher (Halcyon chloris) are
usually associated within seasides or river
mouths and become predator for small fishs and
mudskippers (Periophthalmodon schlosseri).
The largest bird family recorded from the study
was Ardeidae (13 species) followed by
Scolopacidae (9 species), Columbidae (7
species), Alcedinidae (5 species), and
Nectariniidae (5 species). The most common bird
family found in KKWC is Ardeidae which
consists of herons, storks and bitterns which
usually easy to be spotted flying in the
mangrove mud and coastal areas. Sometimes
this bird is known as 'Bangau Air' by the local.
Most of the birds observed in KKWC are
resident bird with 66% from the total of overall
birds surveyed, whereas migratory bird consists
of 32% and 2% includes for both resident and
migratory bird. Resident bird means, the bird is
breeding and stay in the same area or location
throughout the year and does not migrate. From
ANDY RUSSEL MOJIOL et al.
103
the distance sampling analysis, the estimated
population density of birds in KKWC was 14.11
individuals/km2. Its density lies in between a
range of 11.53 – 17.25 birds/km2, within 95%
confidence interval. The total population of birds
was 3526 individuals in an area of about 24
hectares (Table 1). Two assumptions are
essential for reliable estimation of density from
point transect sampling are; (1) bird directly on
the point are always detected at their initial
location, prior to any movement in responsive
to the observer. (2) Distances are measured
accurately or objects are correctly counted in
the proper distance interval.
In this survey, rare species that were difficult to
be spotted belong to woodpeckers, wablers
(Tailorbird and Snipe), and sunbird and
spiderhunter, while the remotes detected birds
are raptors. Sometimes they were spotted flying
a distance of 75 m in the sky and only could be
identified using binoculars. Generally, the
detection function decreases with increasing
distance (Buckland et al., 1993). This was correct
in this survey when using point count method,
where the detection of bird decrease at the
distance of 75 m (Fig. 3).
Table 1: Population density and abundance of birds in KKWC
D (Density)
N (Abundance)
Estimate
%CV
df
95%
Confidence
Interval
14.105
3526.0
10.26
10.26
461
461
11.534
2884.0
17.248
4312.0
1,953
1,7577
1,5824
Detection Probability
1,3671
1,1718
0,9765
0,7812
0,5859
0,3906
0,1953
0
0
10
20
30
40
50
60
70
80
Perpendicular distance in metres
Figure 3: Detection probability of all birds recorded perpendicular to distance using point count method in
KKWC
104
ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE
Sampling error also influence the detection
probability, that not all individuals bird species
could be detected in the investigated areas, due
to numerous variables such as the observer's
visual acuity, hearing ability, and experience, the
length of time spent at a station, the season of
the year, the time of the day, wind, temperature,
and other weather conditions, the habitat
features and the bird's reproductive status and
behaviour. These variables affected the
detection function and the occurrence of birds
in each survey
(a) Natural areas which are currently rich in
birdlife and may act as population
reservoirs for birds. Adequate protection
of these reservoirs may provide a sanctuary
for residence and migratory birds.
(b) Improvement of vegetated corridors along
mangrove areas, swamp areas and green
spaces would be of immediate benefit to
the bird habitat. These corridors may
provide cover, shelter, water, food and
space for those birds to move between
habitats.
CONCLUSIONAND RECOMMENDATIONS
ACKNOWLEDGEMENT
Kota Kinabalu Wetland Centre mangroves can
be considered as one of the most important
habitats for birds. Most of the recorded bird
species belong to the family of Ardeidae (13
species), Scolopacidae (9 species), Columbidae
(7 species), Alcedinidae (5 species) and
Nectariniidae (5 species) respectively. This area
is also an important habitat for kingfishers
which eat small fishes (Mudskipper;
Periophthalmodon schlosseri), crustaceans
(Mud Lobster; Thalassina anomala) and small
aquatic invertebrates, like the Common
Kingfisher (Alcedo atthis), Blue-eared
Kingfisher (Alcedo meninting) and Collared
Kingfisher (Halcyon chloris) they can usually
be observed near the mangrove fringe and river
mouths. Herons, Bitterns and Storks belong to
the Ardeidae family and which usually easy to
be spotted flying in the mangrove mud. Most
of the birds observed in KKWC are resident
birds with 66% of the total overall bird's survey;
whereas migratory bird consists of 32%. An
estimated population of 3,526 individuals in 24
hectares is considered very high. As
recommendations, the presence of birdlife in
KKWC environment is a testimony to the quality
of the environment. It is an indicator that some
balance between the natural and the built
environment could be achieved. To enhance the
birdlife, it would be necessary to consider a few
particular types of bird areas, namely:
The authors wish to thank to the management
of Kota Kinabalu Wetland Centre, for the
support and permission to conduct this study.
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106
ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE
Appendix 1: Taxonomic list of bird species recorded at Kota Kinabalu Wetland Centre
Family
Species
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ardeidae
Ciconiidae
Charadriidae
Charadriidae
Scolopacidae
Scolopacidae
Scolopacidae
Scolopacidae
Scolopacidae
Scolopacidae
Scolopacidae
Scolopacidae
Scolopacidae
Recurvirostridae
Alcedinidae
Alcedinidae
Alcedinidae
Alcedinidae
Alcedinidae
Meropidae
Pandionidae
Accipitridae
Accipitridae
Accipitridae
Rallidae
Rallidae
Rallidae
Columbidae
Columbidae
Columbidae
Columbidae
Columbidae
Columbidae
Columbidae
Cuculidae
Cuculidae
Cuculidae
Caprimulgidae
Apodidae
Apodidae
Ardea purpurea
Ardea cinerea
Nycticorax caledonicus
Nycticorax nycticorax
Egretta intermedia
Egretta eulophotes
Egretta sacra
Egretta alba
Egretta garzetta
Butorides striatus
Ixobrychus sinensis
Ixobrychus cinnamomeus
Gorsachius melanolophus
Leptoptilos javanicus
Pluvialis fulva
Charadrius dubius
Tringa tetanus
Tringa glareola
Tringa nebularia
Tringa stagnatilis
Actitis hypoleucos
Xenus cinereus
Tringa brevipes
Gallinago megala
Gallinago sp.
Himantopus himantopus
Alcedo atthis
Alcedo meninting
Halcyon chloris
Halcyon pileata
Pelargopsis capensis
Merops viridis
Pandion haliaetus
Haliaeetus leucogaster
Haliastur indus
Spilornis cheela
Rallus striatus
Amaurornis phoenicurus
Gallinula chloropus
Chalcophaps indica
Columba livia
Ducula aenea
Geopelia striata
Streptopelia chinensis
Treron olax
Treron vernans
Cacomantis merulinus
Centropus bengalensis
Centropus sinensis
Caprimulgus macrurus
Apus affinis
Collocalia esculenta
Observed No.
2
1
3
2
6
8
2
4
5
1
1
1
2
1
1
1
12
15
4
4
2
1
1
1
1
2
1
1
1
1
1
1
1
1
1
1
2
1
1
1
1
1
3
3
2
1
1
2
2
1
5
2
Estimated No. Protection Status*
1–5
1–5
1–5
1–5
10 – 20
10 – 20
1–5
5 – 10
5 – 10
1-5
1–5
1–5
1–5
1–5
1–5
1–5
10 – 20
10 – 20
5 – 10
5 – 10
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
1–5
P, I
P, I
P
P
P, I
P, VU, I
P, I
P, I
P, I
P, I
P
P
P
P, VU
I
P, I
I
P, I
P, I
I
I
I
P, I
III
I
I
I
I
I
-
ANDY RUSSEL MOJIOL et al.
107
Family
Species
Observed No.
Picidae
Hirundinidae
Hirundinidae
Artamidae
Campephagidae
Aegithinidae
Aegithinidae
Irenidae
Pycnonotidae
Pycnonotidae
Pycnonotidae
Pycnonotidae
Muscicapidae
Timaliidae
Sylviidae
Sylviidae
Sylviidae
Cisticolidae
Corvidae
Laniidae
Sturnidae
Motacillidae
Sturnidae
Nectariniidae
Nectariniidae
Nectariniidae
Nectariniidae
Nectariniidae
Estrildidae
Estrildidae
Passeridae
Picoides moluccensis
Hirundo rustica
Hirundo tahitica
Artamus leucorhynchus
Lalage nigra
Aegithina tiphia
Aegithina viridissima
Chloropsis sonnerati
Pycnonotus goiavier
Pycnonotus plumosus
Pycnonotus brunneus
Pycnonotus zeylanicus
Copsychus saularis
Trichastoma bicolor
Megalurus palustris
Orthotomus sericeus
Orthotomus ruficeps
Prinia flaviventris
Rhipidura javanica
Lanius cristatus
Aplonis panayensis
Anthus rufulus
Sturnus sinensis
Anthreptes malacensis
Hypogramma hypogrammicum
Nectarinia jugularis
Arachnothera longirostra
Prionochilus percussus
Lonchura fuscans
Lonchura malacca
Passer montanus
1
6
5
2
1
1
1
1
3
2
2
3
1
1
1
1
1
1
1
1
1
1
1
1
2
3
1
1
2
2
2
Estimated No. Protection Status*
1
5
5
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
5
10
10
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
I
I
I
I
II
I
I
I
-
*Notes: (P) – Protected under Schedule 2, Part 1, Section 25(2) protected animals under Wildlife Conservation Enactment 1997, Sabah:
(NT) - Near Threatened; (VU) – Vulnerable; Species are classified under IUCN Red Data List, 2006:
Appendix I (CITES) - species threatened with extinction. Trade in specimens of these species is permitted only in exceptional circumstances
Appendix II (CITES) - species not necessarily threatened with extinction, but in which trade must be controlled in order to avoid utilization incompatible with their
survival
Appendix III (CITES) - contains species that are protected in at least one country, which asked other CITES Parties for assistance in controlling the trade.
(CITES = Convention on International Trade in Endangered Species of Wild Flora and Fauna)
JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 109 – 113, 2008
Short Communication
A preliminary study on the morphometrics of the Bornean Elephant
NURZHAFARINA Othman1,2, MARYATI Mohamed1, Abdul Hamid AHMAD1, Senthivel
NATHAN3, Heather Thomas PIERSON2 and Benoit GOOSSENS1,2
1
Institute for Tropical Biology and Conservation (ITBC), Universiti Malaysia Sabah,
Locked Bag No. 2073, 88999 Kota Kinabalu, Sabah, Malaysia
2
Cardiff University, PO Box 915, Cathays Park, Cardiff CF10 3TL, Wales UK
3
Sabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, 88100 Kota Kinabalu, Sabah,
Malaysia
ABSTRACT
This is the first morphometric study on the
Bornean subspecies of the Asian elephant
(Elephas maximus borneensis). The
morphological measurements of captive E. m.
borneensis in Sabah were taken and compared
to those of the captive elephants (E. m. indicus)
in Peninsula Malaysia in an attempt to see if
there were any morphological differences. No
significant differences were found in the
selected measurements between Bornean
elephants and Peninsula Malaysia elephants
(ANCOVA, r > 0.05). Results indicated that there
is positive relationship between age and the
selected morphometric measurements.
INTRODUCTION
The Asiatic elephant is a widely distributed
species covering much of South Asia in the
west to Indochina in the east and a larger part
of Southeast Asia including Peninsular
Malaysia, Sumatra and Borneo. Some
populations are distinguishable through
morphological characters such as the colour of
Keywords: Bornean
measurements
elephant,
morphometric
skin, pigmentation and sometimes by the
characteristics veins in the ears (Kurt &
Kumarasinghe, 1998). Sometimes, different
populations prefer to live in certain habitats.
These differences accounted for the recognition
of different subspecies. Three are currently
recognized i.e Elephas maximus indicus (Indian
elephant), E. m. maximus (Sri Lankan elephant)
and E. m. sumatrensis (Sumatran elephant)
(Sukumar, 1989; Sukumar et al., 1991; Fleischer
et al., 2001). The main reason on why the
Bornean elephant is categorized under Indian
or Sumatran sub-species was because the
inadequacy of the original descriptions of the
Bornean conspecific in terms of the
morphological characters and sample size
(Fernando et al, 2003).
Although a number of morphometric studies
on Asian elephant were done and published
(Wemmer & Krishnamurthy, 1992; Daniel, 1998;
Othman, 1990; Othman, 2003) there was no
morphometric study carried out to differentiate
the sub-species. The Bornean elephant, the
newly classified sub-species, is believed to be
the smallest in size and observed to have larger
ears, longer tails, straighter tusks and a more
rounded body (Fernando et al., 2003). The subspecies, however, was classified based on
genetic analysis by Fernando et al. (2003)
110
despite the known historical accounts of its
origin (De Silva, 1968; Ibbotson, 2003; Shim,
2003). A morphological study is desirable to
confirm a distinct group of organism
(Hawksworth, 1995), which prompted this study.
MATERIALS AND METHODS
The Captive Populations
External morphological measurements of fifteen
captive elephants from Peninsular Malaysia
were made from April to May 2005 at Malacca
Zoo and at Kuala Gandah Elephant
Conservation Centre in Pahang. Measurements
of six elephants from Sabah were taken at the
Lok Kawi Zoological and Botanical Park from
July 2005 to January 2006. Measurements were
made on selected characters as follows: (a) ear
length (EL), (b) ear width (EW), (c) tail length
(TL) and (d) chest girth (CG), using a tailor’s
tape (Butterfly; 150 cm) and a longer measuring
tape (Tricle; 30 m/100 feet) depending on the
characters measured (Figure 1). The
measurements were repeated three times for
each elephant and averaged. Data were analyzed
using the Analysis Covariance (ANCOVA)
carried out via SPSS version 12.0 (SPSS Inc,
Chicago). Elephants are known to grow
throughout life and age is an important factor
determining their morphological characteristics
(Koehl, 1996; Daniel, 1998; Reilly, 2002). Since
the sample size was small (Sabah population, n
= 6, West Malaysia population, n = 15), we used
ANCOVA to control for the age factor in both
populations.
RESULTS
Based on the ANCOVA and controlling for age
(Figure 2), there was no significant difference
in any of the characters between the two
captive populations (p>0.05). However there
was a significant relationship between age and
each variable (p<0.05), stressing the important
influence of age on the morphology of elephants.
THE MORPHOMETRICS OF THE BORNEAN ELEPHANT
DISCUSSION
Morphology is the basic method to classify
species but measurements on exceptionally
large wild animals are difficult to make.
Consequently, most studies were done based
on cranial measurements or dental
characteristics of museum specimens or fossils
(du Toit et al., 1987; Hillis, 1987). Unfortunately,
even when using preserved material the most
common problem still concerns inadequate data
for reliable statistical analysis, a problem
especially true for specimens of exceedingly
large animals.
The physical characteristics of Bornean
elephant as being smaller and different in certain
characters were not confirmed in this study.
The measurements to be tested were not
available elsewhere for the Bornean elephant
and our data provide the only measurements
on those characteristics. Obviously, the
confirmation would require many sets of data
from many individuals representing all age
classes.
In some circumstances, such measurements can
be done on many animals prior to translocation
programs or when the animals are using
grassland or opened forests. Othman (2003)
analyzed morphometric data from wild elephant
gathered over a ten-year translocation program
(1993 to 2003) in Peninsular Malaysia. Similarly,
Daniel (1998) conducted a five year study on
the growth of the Indian elephant and measured
them every year on the same dates and
replicated each measurement four times. In
Borneo, such extensive replication is impossible
because of the scattered elephant populations,
the typically impregnable forest habitat and the
tiny number of individuals in captivity. The
importance of morphological analysis is so
crucial until Fernando et al. (2003) suggested
that a formal reinstatement of the E. m.
borneensis taxa await a detailed morphological
analysis of Bornean elephants and their
comparison with other populations.
NURZHAFARINA OTHMAN et al.
111
Figure 1: The external morphological measurement of each variable in cm (EL = ear width, EL = ear length,
TL = tail length, CG = chest girth) The drawings are not to scale
Measurements definition
Ear width : From the starts of the ear to the widest point of the ear
Ear length : The upper end of the ear to the lowest point of the ear
Tail length : The tail along its entire length and measure at the end of the last vertebra (not
including the hair)
Chest girth : Measured immediately behind the forelegs by wrapping the tape around the torso
112
THE MORPHOMETRICS OF THE BORNEAN ELEPHANT
Figure 2: Interactive scatter plot graphs that showed the linear relationship between each variable and age
while the tables below showed the ANCOVA’s results
NURZHAFARINA OTHMAN et al.
ACKNOWLEDGEMENTS
We thank the Sabah Wildlife Department and
Malacca Zoo for allowing us to collect data on
captive elephants. We are indebted to Jubius
Dausip and the team, Ahmad Tajuddin Ali, Dr.
Symphorosa Sipangkul, Norsham Mohd Noor
and the team and also Nasaruddin Othman for
their kind assistance during the data collection.
We also thank David Bignell for reviewing an
earlier version of this manuscript.
REFERENCES
Daniel, J. C. 1998. The Asian Elephant: A
Natural History. Dehradun: Natraj
Publishers.
De Silva, S. G. 1968. Elephants of Sabah. Sabah
Society Journal. III(4): 169 – 181.
Du Toit, F. R., J. T. Foose and M. H. D. Cumming.
1987. The existing basis for subspecies
classification of black and white rhinos.
Pachyderm No. 9. International Union for
Conservation of Nature and Natural
Resources. Nairobi.
Fernando, P., T. N. C. Vidya, J. Payne, M. Stuewe,
G. Davison, R. J. Alfred, P. Andau, E. Bosi,
A. Kilbourn and D. J. Melnick. 2003. DNA
analysis indicates that Asian elephants are
native to Borneo and are therefore a high
priority for conservation. Public Library of
Science Biology. 1: 1 – 6.
Fleisher, C. R., K. Muralidharan, A. E. Perry,
E. E. Steven and M. C. Wemmer. 2001.
Phylogeography of the Asian Elephant
(Elephas maximus) based on mitochondrial
DNA. Evolution. 55(9): 1882 – 1892.
Hawksworth, D. I. 1995. Biodiversity
Measurement and Estimation. London:
The Royal Society.
Hillis, M. D. 1987. Molecular versus
morphological approaches to systematic.
Annual Review of Ecology, Evolution and
Systematics. 18: 23 – 42.
113
Ibbotson, R. 2003. Domesticated elephants in
Borneo. Sabah Society Journal. 20: 1 – 6.
Koehl, R. A. M. 1996. When does morphology
matter? Annual Review of Ecology,
Evolution and Systematics. 27: 501 – 542.
Kurt, F. and J. c. Kumarasinghe. 1998. Remarks
on body growth and phenotypes in Asian
elephant Elephas maximus. Acta
Theriologica. 5 (Supply): 135 – 153.
Othman, N. 2003. Kajian Penggunaan Ukuran
Tapak kaki bagi Menjangkakan Berat,
Kelas Umur dan Jantina Gajah Asia
(Elephas maximus) di Semenanjung
Malaysia. BSc thesis. Universiti
Kebangsaan Malaysia. (Unpublished).
Kuala Lumpur.
Othman, S. 1990. Biometric relationship of
elephant measurements. The Journal of
Wildlife and Parks. IX: 125 – 131.
Reilly, J. 2002. Growth in the Sumatran
elephant (Elephas maximus sumatranus)
and age estimation based on dung
diameter. Journal of Zoology London. 258:
205 – 213.
Shim, P. S. 2003. Another look at the Borneo
elephant. Sabah Society Journal. 20: 7 – 14.
Sukumar, R. 1989. The Asian Elephant:
Ecology and Management. Cambridge:
Cambridge University Press.
Sukumar, R., D. L. Alwis, J. Barnett, L. K. D.
Choudhury, P. C. Lee, A. Luxmoore and J.
Shoshant. 1991. The Illustrated
Encyclopedia of Elephants. New York:
Salamander Books Ltd.
Wemmer, C. and V. Krishnamurty. 1992. The
Asian Elephant: Ecology, Biology,
Diseases, Cinservation and Management.
Kerala Agri.
JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 115 – 120, 2008
Checklist
A preliminary survey on the butterfly fauna of Sungai Imbak Forest Reserve,
a remote area at the centre of Sabah, Malaysia
Mohd. Fairus JALIL¹,2, Hairul Hafiz MAHSOL¹,2, Nordin WAHID² and Abdul Hamid AHMAD¹,2
¹ Centre for Primate Studies Borneo, Institute for Tropical Biology & Conservation,
Universiti Malaysia Sabah, 88999 Kota Kinabalu, Sabah, Malaysia
²Institute for Tropical Biology & Conservation, Universiti Malaysia Sabah, 88999 Kota
Kinabalu, Sabah, Malaysia
ABSTRACT
This paper reports result from a study to
document the composition and distribution of
butterflies in the Imbak Valley region of the
Sungai Imbak Forest Reserve. One hundred and
seventy four species (18.6%) of butterflies with
six endemic species were recorded from the area.
Results also showed that Imbak Valley is
valuable for conservation purposes based on
its unique butterfly fauna.
INTRODUCTION
The current rate of species extinction and
habitat modification is increasing alarmingly.
During the last decades, many of the forested
areas are logged, cleared or converted into
plantation (Groombridge, 1992; Padoch &
Peluso, 1996; John, 1997; Laurance &
Bierregaard, 1997). Among the remaining
primary forest left are the Sungai Imbak Forest
Reserve which consist of several virgin jungle
reserve (VJR) located at the centre of Sabah.
On the 8th of June 2000, Imbak Valley Scientific
Expedition was hosted by the Forestry
Department of Sabah, during this one-month
Keywords: Butterfly, Imbak, Sabah
expedition, flora and fauna were censuses and
documented. During this expedition, the
butterfly research group of the Institute for
Tropical Biology and Conservation, UMS
carried out a 14-day surveyed of butterfly fauna
within the valley. Objectives of the survey were
to document the butterfly fauna of the area and
then mapped the data obtained into the
WorldMap IV program (Mahadimenakbar, 1999).
METHODS
Butterfly were surveyed using all available
methods that include trapping, netting and
transect methods (DeVries, 1987; Upton, 1991).
Trapping was carried out using fruit baited
traps. Netting was carried out along the ridges,
river and other suitable areas. Transect methods
were carried out only by experienced staff to
ensure reliability of identification. Sweep
netting were also carried out at low bushes to
chase out crepuscular and resting butterflies.
Butterfly were surveyed at the transit camp,
logging road leading to base camp, hilltop area
near the base camp, forest adjacent to the base
camp and along the river.
The checklist of butterfly species recorded
from Imbak Valley (5° 7’N; 117° 3’E) is presented
in a systematic order, arranged by family,
116
BUTTERFLIES OF SUNGAI IMBAK FOREST RESERVE
subfamily and genera (Appendix 1). For
taxonomy and nomenclature, we follow recent
classification and standard reference works by
Eliot (1992), Maruyama & Otsuka (1992) and
Otsuka (1988).
RESULTS AND DISCUSSION
A total of 174 species of butterflies from five
families, Papilionidae, Pieridae, Nymphalidae,
Lycaenida and Hesperiidae were recorded from
the survey (Table 1).
The majority of the species collected were from
the family of Pieridae, Papilionidae and
Nymphalidae which contribute about 90%.
Lycaenidae and Hesperiidae contribute less that
10% of the total figure even though both are
the largest and second largest family in Borneo.
Comparison of Different Microhabitats
Among all the sites, hilltop area is the most
interesting area, which observed many rare and
endemic species. The wet seepage area at the
hilltop is also an excellent place where many
Pierids and Papilionids were found
congregating in moderate number. The
regenerating forest between transit camp and
base camp was not explored thoroughly, it was
generally poor in species, though not
necessarily in numbers of individuals.
Graphium sarpedon, G. doson, Eurema spp. and
Catopsilia pomona were characteristic species.
DISCUSSION
Looking at the hilltop, most of the species
found were characteristic of canopy with many
species that are usually rare and only
occasionally found at the lower level. It was
interesting to note that Imbak Valley has four
representative of Bornean birdwing namely,
Troides brookiana, Troides amphrysus, T.
helena and T. andromache. Troides
andromache was observed only at the forestcovered hilltop near the base camp with
exception of two sighting of females flying
above the waterfall. A single female T. helena
was captured while nectaring at flowering
bushes at the logging road towards the base
camp, others were observed nectaring and
flying near the hill top. The most common
species of Troides notable for this expedition
were T. amphrysus and T. brookiana.
General Composition
Conservation
Overall the species collected were characteristic
of lowland forest with several representative
from the mid to highland forest. Most of the
species collected however showed a very low
frequency of butterflies. Nevertheless several
endemic species and many rare species were
collected during the study. Most of the family
was well represented except for Lycaenidae and
Hesperiidae, each with less than 10% species
collected.
Even though the number of endemic species in
Imbak Valley is low, some of the species
observed here were considered rare and
endangered. Some species collected were
already included in the list of protected fauna
of Malaysia (Anon., 1991). With many species
found in the area are listed in the list of protected
species of Malaysia, Imbak Valley is indeed
valuable in conservation of butterfly fauna.
Table 1: Percentage of butterfly recorded in Imbak
Valley compared to the total number of species
recorded in Borneo
FAMILY
BORNEO
IMBAK
%
Papilionidae
Pieridae
Nymphalidae
Lycaenidae
Hesperiidae
44
42
241
394
214
21
26
110
15
2
47.7%
61.9%
45.6%
3.8%
0.9%
TOTAL
935
174
18.6%
MOHD. FAIRUS JALIL et al.
ACKNOWLEDGEMENTS
We would like to thank the Forestry Department
of Sabah and Forest Research Centre for
inviting us to participate in the expedition. We
wish to acknowledge the kind assistance of the
organizing committee of Imbak Valley Scientific
Expedition 2000 who helped with all the logistics
and transportation during the study. We also
would like to acknowledge the kind assistance
of Jacqueline, P.K. for painstakingly spreading
all the butterflies from Imbak Valley. This
research was partially funded by Universiti
Malaysia Sabah through the Institute for
Tropical Biology and Conservation.
REFERENCES
Anon. 1991. Laws of Malaysia: Act A337 –
Protection of Wildlife 1972 (Amendment)
1976, PU(A)306/91. Kuala Lumpur:
Percetakan Nasional Malaysia Berhad.
De Vries, P. J. 1987. The butterflies of Costa
Rica and their Natural History. Vol. 1. New
Jersey: Princeton University Press.
Eliot, J. N. (Ed.). 1992. The Butterflies of
Malays Peninsula. (4th Ed.). Malayan
Nature Society. Malaysia. Kuala Lumpur.
Groombridge, B. (Ed.). 1992. Global
biodiversity: Status of the earth’s living
resources. London: Chapman & Hall.
John, A. G. 1997. Timber production and
biodiversity conservation I tropical
rainforest. (2nd Ed.). United Kingdom:
Cambridge University Press.
117
Laurance, W. F. and R. O. Bierregaard. 1997.
Preface – A crisis in the making. In:
Laurance W. F. and R. O Bierregaard (Eds.).
Tropical forest remnants – ecology,
management and conservation of
fragmented communities. Chicago:
Chicago University Press.
Mahadimenakbar, M. D. 1999. Potential use of
WorldMap for exploring aspect of spatial
pattern in biological data: An introduction
use on butterfly diversity assessment in
Borneo. In: Hassan, S. T. S., I. Azhar, O.
Dzolkhifli and A. S. Sajap. (Eds.).
Entomology in Malaysia beyond 2000:
Exploration,
imploration
and
digitalization.
Maruyama, K. and K. Otsuka. 1991. Butterflies
of Borneo. Vol. 2, No. 2. Tokyo: Tobishima
Corporation.
Otsuka, K. 1988. Butterflies of Borneo. Vol. 1.
Tokyo: Tobishima Corporation.
Padoch, C. and N. L Peluso. 1996. Borneo
people and forests in transition: An
introduction. In: Padoc, C. and N. L. Peluso
(Eds.). Borneo in transition: people,
forests, conservation and development.
Oxford University Press.
Upton, M. S. 1991. Methods for collecting,
preserving and studying insects and
allied forms. Australian Entolomological
Society. Miscellaneous Publication No. 3.
(4th Ed.). Brisbane. Australia.
118
BUTTERFLIES OF SUNGAI IMBAK FOREST RESERVE
Appendix 1: Distributional checklist of butterflies from the Imbak Valley region of Sungai Imbak Forest
Reserve ‘*’ indicates the species is endemic to Borneo
FAMILY PAPILIONIDAE
Subfamily Papilioninae
Atrophaneura nox (Swainson, [1822])
Graphium agamemnon (Linnaeus, 1758)
Graphium antiphates (Cramer, [1775])
Graphium bathycles (Zinken, 1831)
Graphium doson (Felder & Felder, 1864)
Graphium evemon (Boisduval, 1836)
Graphium procles Grose-Smith, 1887*
Graphium sarpedon (Linnaeus, 1758)
Pachliopta antiphus (Fabricius, 1793)
Pachliopta neptunus (Guérin-Méneville,
1840)
Papilio demoleus Linnaeus, 1758
Papilio demolion Cramer, [1776]
Papilio helenus Linnaeus, 1758
Papilio memnon Linnaeus, 1758
Papilio nephelus Boisduval, [1836]
Papilio palinurus Fabricius, 1787
Papilio polytes Linnaeus, 1758
Troides amphrysus (Cramer, [1779])
Troides andromache (Staudinger, 1892)*
Troides brookiana (Wallace, [1856])
Troides helena (Linnaeus, 1758)
FAMILYPIERIDAE
Subfamily Pierinae
Appias albina (Boisduval, 1836)
Appias cardena (Hewitson, [1861])
Appias indra (Moore, 1857)
Appias lyncida (Cramer, [1777])
Appias nero (Fabricius, 1793)
Appias pandione (Geyer, 1832)
Appias paulina (Cramer, [1777])
Cepora iudith (Fabricius, 1787)
Cepora pactolicus Butler, 1865*
Delias hyparete (Linnaeus, 1758)
Hebomoia glaucippe (Linnaeus, 1758)
Leptosia nina (Fabricius, 1793)
Pareronia valeria (Cramer, [1776])
Phrissura cynis (Hewitson, 1866)
Prioneris cornelia (Vollenhoeven, 1865)*
Saletara panda (Godart, 1819)
Subfamily Coliadinae
Catopsilia pomona (Fabricius, 1775)
Catopsilia pyranthe (Linnaeus, 1758)
Dercas gobrias (Hewitson, 1864)
Eurema ada (Distant & Pryer, 1887)
Eurema hecabe (Linnaeus, 1758)
Eurema lacteola (Distant, 1886)
Eurema nicevillei (Butler, 1898)
Eurema sari (Horsfield, [1829])
Eurema simulatrix (Semper, 1891)
Gandaca harina (Horsfield, [1829])
FAMILYNYMPHALIDAE
Subfamily Danainae
Danaus chrysippus (Linnaeus, 1758)
Danaus genutia (Cramer, [1779])
Euploea algea (Godart, 1819)
Euploea camaralzeman Butler, 1866
Euploea crameri Lucas, 1853
Euploea eyndhovii Felder & Felder, [1865]
Euploea leucostictos (Gmelin, [1790])
Euploea modesta Butler, 1866
Euploea mulciber (Cramer, 1777])
Euploea radamanthus (Fabricius, 1793)
Euploea sylvester (Fabricius, 1793)
Euploea tulliolus (Fabricius, 1793)
Idea hypermnestra (Westwood, 1848)
Idea stolii (Moore, 1883)
Ideopsis gaura (Horsfield, [1829])
Ideopsis vulgaris (Butler, 1874)
Parantica agleoides (Felder & Felder, 1860)
Parantica aspasia (Fabricius, 1787)
Parantica luzonensis (Felder & Felder, 1863)
Tirumala septentrionis (Butler, 1874)
MOHD. FAIRUS JALIL et al.
Subfamily Satyrinae
Elymnias dara Distant & Pryer, 1887
Elymnias nesaea (Linnaeus, 1764)
Elymnias panthera (Fabricius, 1787)
Erites argentina Butler, 1868
Erites elegans Butler, 1868
Lethe europa (Fabricius, 1775)
Melanitis leda (Linnaeus, 1758)
Melanitis zitenius (Herbst, 1796)
Mycalesis amoena Druce, 1873*
Mycalesis anapita Moore, [1858]
Mycalesis fusca (Felder & Felder, 1860)
Mycalesis horsfieldi Fruhstorfer, 1908
Mycalesis janardana Moore, [1858]
Mycalesis kina Staudinger, 1892*
Mycalesis oroatis Hewitson, [1864]
Mycalesis orseis Hewitson, [1864]
Neorina lowii (Doubleday, [1849])
Ragadia makuta (Horsfield, [1829])
Xanthotaenia busiris Westwood, [1858]
Ypthima baldus (Fabricius, 1775)
Ypthima pandocus Moore, [1858]
Subfamily Morphinae
Amathusia phidippus (Linnaeus, 1763)
Amathuxidia amythaon (Doubleday, 1847)
Discophora necho Felder & Felder, [1867]
Discophora sondaica Boisduval, 1836
Faunis canens Hübner, [1826]
Faunis stomphax (Westwood, 1858)
Taenaris horsfieldii (Swainson, [1820])
Thaumantis klugius (Zinken, 1831)
Thaumantis odona (Godart, [1824])
Thauria aliris (Westwood, [1858])
Zeuxidia amethystus Butler, 1865
Zeuxidia doubledayi Westwood, [1851]
Subfamily Nymphalinae
Amnosia decora Doubleday, [1849]
Athyma kanwa Moore, 1858
Athyma larynma (Doubleday, [1848])
Athyma nefte (Cramer, [1779])
Athyma selenophora (Kollar, [1844])
119
Bassarona dunya (Doubleday, [1848])
Bassarona teuta (Doubleday, [1848]
Cethosia biblis (Drury, [1773])
Cethosia hypsea Doubleday, [1847]
Chersonesia rahria (Moore, [1858])
Cirrochroa emalea (Guérin-Méneville, 1843)
Cirrochroa malaya Felder & Felder, 1860
Cirrochroa tyche (Felder & Felder, 1861)
Cupha erymanthis (Drury, [1773])
Cyrestis cocles (Fabricius, 1787)
Cyrestis maenalis Erichson, 1834
Cyrestis nivea (Zinken, 1831)
Doleschalia bisaltide Felder & Felder, 1860
Dophla evelina (Stoll, 1790)
Euripus nyctelius (Doubleday, 1845)
Euthalia monina (Fabricius, 1787)
Hypolimnas anomala (Wallace, 1869)
Hypolimnas bolina (Linnaeus, 1758)
Junonia atlites (Linnaeus, 1763)
Junonia hedonia (Linnaeus, 1764)
Junonia iphita (Cramer, [1779])
Kallima limborgi Moore, [1879]
Kaniska canace (Linnaeus, 1763)
Laringa castelnaui (Felder & Felder, 1860)
Lasippa tiga (Moore, 1858)
Lebadea martha (Fabricius, 1787)
Lexias canescens (Butler, [1869])
Lexias dirtea (Fabricius, 1793)
Lexias pardalis (Moore, 1878)
Moduza procris (Cramer, [1777])
Neptis clinia Moore, 1872
Neptis duryodana Moore, 1858
Neptis hylas (Linnaeus, 1758)
Neptis nata Moore, 1857
Paduca fasciata (Felder & Felder, 1860)
Pandita sinope Moore, [1858]
Parthenos sylvia (Cramer, [1775])
Phalanta alcippe (Stol, 1782)
Rhinopalpa polynice (Cramer, [1779])
Tanaecia clathrata (Vollenhoeven, 1862)
Tanaecia iapis (Godart, [1824])
Terinos atlita (Fabricius, 1787)
Terinos terpander Hewitson, 1862
Vindula dejone (Erichson, 1834)
Vindula erota (Fabricius, 1793)
120
BUTTERFLIES OF SUNGAI IMBAK FOREST RESERVE
Subfamily Charaxinae
Subfamily Miletinae
Agatasa calydonia (Hewitson, [1854])
Charaxes bernardus (Fabricius, 1793)
Polyura athamas (Drury, [1773])
Polyura delphis (Doubleday, 1843)
Polyura hebe (Butler, [1866])
Polyura schreiber (Godart, [1824])
Prothoe franck (Godart, [1824])
Logania malayica Distant, 1884
FAMILYLYCAENIDAE
FAMILYHESPERIIDAE
Subfamily Riodininae
Subfamily Pyrginae
Abisara saturata (Moore, 1878)
Paralaxita damajanti (Felder & Felder, 1860)
Paralaxita orphna (Boisduval, 1836)
Paralaxita telesia (Hewitson, [1861])
Celaenorrhinus ficulnea (Hewitson, 1868)
Subfamily Lycaeninae
Amblypodia narada (Horsfield, [1828])
Arhopala epimuta (Moore, [1858])
Caleta elna (Hewitson, [1876])
Cheritra freja (Fabricius, 1793)
Drupadia ravindra (Horsfield, [1828])
Loxura cassiopeia Distant, 1884
Udara placidula (Druce, 1895)
Subfamily Curetinae
Curetis santana (Moore, [1858])
Curetis sperthis (Felder & Felder, [1865])
Curetis tagalica (Felder & Felder, 1862)
Subfamily Hesperiinae
Koruthaialos rubecula (Plötz, 1882)