Diversity of Small Mammals at Less Distu
STH 2113 FIELD ECOLOGY
FIELD SAMPLING REPORT
DEPARTMENT OF ZOOLOGY
Faculty of Resources Science and Technology
University of Malaysia Sarawak
Semester 1, Sesi 2013/2014
Diversity of Small Mammals at Less Disturbed
Primary Forest of Gunung Gading National Park
GROUP 1: MAMMALS
MEMBERS:
AHMAD FARHAN BIN MOHAMMED AMIN
MALINKA AK SIKIM
RIDHWAN BIN ABDUL RAHIM
ABANG MOHD HARIZT BIN ABG ABD KHALEX
AISYA FATHIYA BINTI CHE ROSLI
RACHEAL AK ROSEDY
PHILOVENNY ANAK PENGIRAN
EMY RITTA AK JINGGONG
BRENDA MAY ENGKIAN AK NANDONG @ SULIE
CHRIST HANI BT LIAN LEE
HILDA JELEMBAI AK NEILSON ILAN
DATE OF SUBMISSION: 10th DECEMBER 2014
LECTURER:
Dr. Mohd Azlan Jayasilan
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TABLE OF CONTENTS
Page
Abstract......................................................................................................................................... 3
1
Introduction...................................................................................................................... 5
-Objectives........................................................................................................................ 5
2
Materials and Methods..................................................................................................... 6
-Study Area....................................................................................................................... 6
-Field Methodology.......................................................................................................... 7
-Statistical Analysis.......................................................................................................... 8
-Species Identification and Preservation.......................................................................... 10
3
Results.............................................................................................................................. 11
4
Discussion........................................................................................................................ 18
5
Conclusion........................................................................................................................ 25
6
Recommendation............................................................................................................. 26
7
Acknowledgement........................................................................................................... 27
8
References........................................................................................................................ 28
9
Appendices....................................................................................................................... 30
2
Diversity of Small Mammals at Less Disturbed Primary
Forest of Gunung Gading National Park
M.AMIN, A.F., SIKIM, M., A.RAHIM, R., A.A.KHALEX, A.M.H., C.ROSLI, A.F., ROSEDY, R.,
PENGIRAN, P., JINGGONG, E.R., N.SULIE, B.M.E., L.LEE, C.H & N.ILAN, H.J.
Animal Resource Science and Management Program,
Faculty of Resource Science &Technology,Universiti Malaysia Sarawak,
94300 Kota Samarahan, Sarawak, Malaysia.
ABSTRACT
A study of field ecology aimed to document small mammals (volant and non-volant) was
conducted at less disturbed primary forest of Gunung Gading National Park (GGNP) from 18th to
23rd October 2014. This was a practical study on Field Ecology under the Department of Zoology
of Universiti Malaysia Sarawak (UNIMAS). Ten mist nets, two harp traps complete with bags
and 45 cage traps were set up for six sampling days. A total of 45 individuals from three orders,
six families and 25 species were caught in this study. Of the 12 species, four were frugivorous
bats and eight were insectivorous bats. On the other hand, there were comprised of 13 species of
non-volant small mammals, seven of them are from the family Muridae, four species from
Tupaiidae and two species from family Sciuridae. Our sampling site has several layers of
understory and mainly covered with lowland primary forest. This is evidence by the highest
abundance of Rhinolophus affinis and R. luctus for volant small mammals, and Maxomys
whiteheadi for non-volant small mammals. The increasing species cumulative curve for nonvolant small mammals indicates that there may be more species yet to be recorded from this
study site compared to Chiropteran. As a whole the study indicates that species diversity of
volant and non-volant small mammals is associated with the forest type and level of disturbance
in a particular area.
Keyword: Chiroptera, Rodentia, Scandentia, species diversity, primary forest, Gunung Gading
National Park
3
ABSTRAK
Satu kajian ekologi lapangan bertujuan untuk mendokumentasikan mamalia kecil telah
dijalankan di hutan asal Taman Negara Gunung Gading dari 18hb hingga 23hb Oktober 2014.
Ini merupakan kajian praktikal dalam kursus Ekologi Lapangan di bawah Jabatan Zoologi
Universiti Malaysia Sarawak (UNIMAS). Sebanyak sepuluh jaring kabus, dua perangkap 'harp
trap' lengkap dengan beg dan 45 perangkap tikus biasa telah digunakan sepanjang 6 hari kajian
tersebut. Sebanyak 45 individu daripada tiga order, enam famili dan 25 spesies telah ditangkap
dalam kajian ini. Daripada 12 spesies, empat adalah daripada kelawar jenis pemakanan buah
dan lapan adalah kelawar pemakanan serangga. Sebaliknya, daripada 13 spesies mamalia kecil
daratan, tujuh daripada mereka adalah dari famili Muridae, empat spesies dari Tupaiidae dan
dua spesies daripada famili Sciuridae. Kawasan lapangan kami mempunyai beberapa lapisan
tanah hutan yang terutamanya diliputi dengan hutan primer yang bertanah rendah. Disebabkan
itu, kelimpahan yang tinggi oleh Kelawar Ladam Hutan (Rhinolophus affinis) dan R. luctus
untuk mamalia kecil terbang, dan Maxomys whiteheadi untuk mamalia kecil daratan. Graf
kumulatif spesies yang masih meningkat menunjukkan potensi penemuan banyak lagi spesies
yang masih belum direkodkan di kawasan ini, terutamanya bagi spesies mamalia kecil daratan
berbanding mamalia kecil terbang iaitu kelawar. Secara keseluruhannya kajian ini menunjukkan
bahawa kepelbagaian spesies kelawar dan mamalia kecil daratan dikaitkan dengan jenis hutan
dan tahap gangguan dalam suatu kawasan tertentu.
Kata kunci: Chiroptera, Rodentia, Scandentia, kepelbagaian spesies, hutan primer, Taman
Negara Gunung Gading
4
INTRODUCTION
The small mammals can be defined as a group of mammal that are small in size and
weight less than 5 kg. Small mammals can be divided into two types, namely volant and nonvolant. Non-volant small mammals belong to orders Scandentia, Rodentia, and Insectivora which
are non-flying mammals. Whereas volant small mammals exclusively are belong to order
Chiroptera. Bats are mammals in order Chiroptera. They are different from other mammals
because they can fly. They are the second largest order in class Mammalia after rats and squirrels
in term of biodiversity (Rahman et al. 2011). According to Payne et al. (2007), species of bats in
Borneo are classified into 8 families. They are distinguished based on ear shape, muzzle shape,
tail pattern and presence of noseleaf (Payne et al. 2007). Chiroptera are further divided into
suborder Megachiroptera and Microchiroptera. In terms of bats diversity, there are 96 species of
bats in Borneo harbours (Struebig et al, 2010), which made up 42% of mammals species in
Borneo. Sarawak itself recorded 73 species of bats (Jayaraj, 2008).
The most abundant group comprises of rats and mice (Muridae), which can be found on
the ground but also in the canopy. In contrast, treeshrew (Scandentia) have basically diversified
on the ground, with only two out of five abundant lowland species exploring the canopy space,
Tupaia minor and Ptilocercus lowii (Sargis, 2002; Wells et al., 2004).
OBJECTIVES
1. To determine the species diversity of volant and non-volant small mammals at less disturbed
primary forest in Gunung Gading National Park.
2. To determine the species richness and relative abundance of volant and non-volant small
mammals.
3. To compare the findings with previous studies on small mammals in Sarawak and Peninsular
Malaysia.
5
MATERIALS AND METHODS
Study Area
A sampling survey of small mammals was conducted at Gunung Gading National Park
(N O10 42.00’ E 1090 50.20’) Lundu, southeast of Sarawak which is located 80 km from west of
Kuching. Gunung Gading NP is mainly composed by tropical rainforest which most species-rich
terrestrial ecosystem on earth. The highest peak Of Gunung Gading NP rises to the height of
965m above sea level (a.s.l) which composed of remains of an old British jungle base during the
communist insurgency of the 1960's. It has a wide range of habitats including the riverine
vegetation, hill dipterocarp forest, lower and upper montane forest. Gunung Gading NP are fully
reserve forest under Sarawak Forestry Department, Malaysia and were gazetted as a park in
August 1983 primarily to provide a conservation zone for protection of the Rafflesia (Sarawak
Forestry Corporation, 2006) and it is now well known as place for camping, mother nature
exploration and recreation.
During the field ecology work, a survey was done mainly on species diversity of small in
the primary forest. Our sampling site was conducted at less disturbed primary forest that covered
with mixed dipterocarp forest, full ceiling canopy and several layers of understory. The ground
floor is generally clear of heavy vegetation. The primary forest is labelled as less disturbed forest
where less human intervention occurs in the forest. Therefore, we were interested to discover the
species diversity of the forest.
6
Figure 1: Location of study (source: Google map, 2013), Gunung Gading NP that
has an area of 4,106 hectares.
Field Methodology
A sampling survey of small mammals was conducted from from 18th until 23rd October
2014. There were ten mist nets, two harp traps complete with bags and 45 cage traps were set up
throughout the sampling period. Mist nets that shared with aves taxa, were put up along the
forest trail and over the stream. The harp traps were deployed between trees and narrow paths in
the forest. The mist nets and harp traps were checked regularly at 0530 and for every two hours
from 1800 to 2400 hours for 6 sampling days. The cage traps were placed on the ground near to
the main trail, a distance of 5 meters between the centre points along the trail and approximate
distance of 10 meters apart form each other. These traps were checked twice a day and re-baited
if necessary. The first checking was done in the morning around 1000 hours and the second
checking was done around 1700 hours in the evening. For the first sampling day we used
pineapples for bait and the second day onwards we switched the bait by using banana.
7
Statistical Analysis
Diversity Indices
In order to have an effective measure of diversity in a community, we need to account (in
most instances) for both species richness and the evenness with which individuals are distributed
among species. Species diversity is a measure of the diversity within an ecological community
that incorporates both species richness (the number of species in a community) and the evenness
of species abundances. Species richness is the number of different species in a particular area.
Species evenness is the relative abundance with which each species are represented in an area.
One way to do this is through the use of a proportional abundance index. While more than 60
indices have been described, we used the two most widely used in the ecological literature:
Simpson's and Shannon-Weiner Index.
1) Shannon Index (H´)
The Shannon's diversity index (H’), also known as communication entropy, was
introduced by Claude Shannon (1948). The Shannon-Weaver Index (H’) measures overall
biodiversity. It assumes that all species are represented in a sample and the sample was obtained
randomly. H is maximized when all species have the same number of animals collected.
Shannon Index was also used for the calculation in Zar (1999) modified t-test to test the
hypotheses that the two sampling areas (primary and secondary forest) were different in species
abundance.
S
H pi . ln( pi )
i 1
where:
H’= Shannon diversity index
S = numbers of species encountered
pi is the proportion of individuals found in the ith species.
ln is the natural logarithm.
8
2) Simpson’s Index (1-D)
Simpson's Index is considered a dominance index because it weights towards the
abundance of the most common species. Simpson's Index gives the probability of any two
individuals drawn at random from an infinitely large community belonging to different species.
The bias corrected form of Simpson's Index is:
ni ni 1
i 1 N N 1
S
Ds
Where
ni = number of individuals in ith species
N = number of individuals in all species
Simpson’s Index of Diversity = 1-D
Simpson’s Reciprocal Index = 1/D
Rank Abundance Curve
The rank abundance curve/plot is plotted by ranking from the highest abundance to the
lowest abundance in X-axis. Ranking species from most abundant to least provides another
useful way to visualize community data, this allow us to make comparisons of samples of
different sizes. It is the comparison of abundance of the species of a group of organisms in a
given locality. Y-axis shows the relative species abundance measured in a log scale, because
plotting the data on a log scale allows for better data visualization. It can also be used to visualise
species richness and species evenness. It overcomes the shortcomings of biodiversity indices that
cannot display the relative role different variables played in their calculation.
9
Species Accumulation Curve
A species accumulation curve is the graph of the cumulative number of observed species
as a function of some measure of sampling effort (Colwell et al. 2004). The species accumulation
curve also indicates whether we have captured all the species which we suppose to catch in the
population of our study site. So this graph can also be used to estimate the species richness,
which important to estimate the number of overall species present at the site. Species richness is
the most commonly used biodiversity indicators for conservation correspondence.
Non-parametric estimator
Species richness can be estimated by using three approaches (Magurran 2004), but for
this study we used non-parametric estimators. This method is for estimating species richness
from samples which were adapted from mark-recapture applications for estimating population
size. They also require no assumptions about community structure (Colwell and Coddington
1995). Species richness estimators attempt to predict the asymptote of the species accumulation
curve, thus correcting for the downward bias inherent in observed species richness. Richness
estimators predict richness, including species not discovered in the sample, from the proportional
abundances of species within the total sample (Sobero´n and Llorente 1993; Colwell 2005).
Species Identification and Preservation
Species identification and measurement followed A Field Guide to the Mammals of
Borneo (Payne et al. 2007). For each individual caught, external measurements were conducted,
recorded and used to identify the species before released back to the forest. There were two
species include both volant and non-volant small mammals that were collected as wet specimens
preserved in 70% ethanol. The specimens were deposited in Universiti Malaysia Sarawak
(UNIMAS) Zoological Museum.
10
RESULTS
A total of 45 individuals of small mammals from Order Chiroptera, Rodentia and Scandentia
were caught during the sampling period. From the six days of trapping, 25 species of small
mammals were recorded. These were eight insectivorous bats, four frugivorous bats, seven rats,
two squirrels and four treeshrews (Table 1 and 2). The insectivorous bats captured were
representing the family Rhinolophidae and Hipposideridae, whereas the frugivorous bats were
from the family Pteropodidae. As for the rodents, rats were from the family Muridae and
squirrels from the family Sciuridae, while treeshrews from the family Tupaiidae.
Table 1: List of volant species in Gunung Gading NP (18th -23rd October 2014).
N=Total individuals, RA=Relative abundance
Family
Species Name
Common Name
N
RA%
Hipposideridae
Hipposideros cervinus
Fawn Roundleaf Bat
2
9.09
Hipposideros dyacorum
Dayak Roundleaf Bat
1
4.54
Cynopterus brachyotis
Short-nose Fruit Bat
3
13.64
Penthetor lucasii
Dusky Fruit Bat
2
9.09
Dyacopterus spadiceus
Dayak Fruit Bat
1
4.54
Balionycteris maculata
Spotted-winged Fruit Bat
1
4.54
Rhinolopus arcuatus
Arcuate Horseshoe Bat
1
4.54
Rhinolopus affinis
Intermediate Horseshoe Bat
4
18.18
Rhinolopus luctus
Great Woolly Horseshoe Bat
4
18.18
Rhinolopus borneensis
Bornean Horseshoe Bat
1
4.54
Rhinolopus trifoliatus
Trefoil Horseshoe Bat
1
4.54
Rhinolopus creaghi
Creagh’s Horseshoe Bat
1
4.54
22
100
Pteropodidae
Rhinolophidae
Total
12
11
Table 2: List of non-volant species in Gunung Gading NP (18th -23rd October 2014).
N=Total individuals, RA=Relative abundance
Order
Family
Species
Common Name
N
RA%
Rodentia
Muridae
Sundamys muelleri
Muller’s Rat
1
4.35
Maxomys whiteheadi
White Head’s Rat
4
17.4
Maxomys surifer
Red Spiny Rat
1
4.35
Maxomys rajah
Brown Spiny Red
1
4.35
Niviventer cremoriventer Dark-tailed Tree Rat
2
8.7
Rattus tiomanicus
Malaysian Field Rat
1
4.35
Leopoldamys sabanus
Long-tailed Giant Rat
1
4.35
Lariscus insignis
Three-striped Ground Squirrel
2
8.7
Sundasciurus lowii
Low’s Squirrel
1
4.35
Large Treeshrew
3
13.64
Tupaia minor
Lesser Treeshrew
2
8.7
Tupaia gracilis
Slender Treeshrew
2
8.7
Tupaia picta
Painted Treeshrew
2
8.7
23
100
Sciuridae
Scandentia Tupaiidae Tupaia tana
Total
13
For the species richness, the most recorded order for small mammals is order Chiroptera
with 12 species. There are six families of small mammals recorded, and family Muridae has the
most caught species of non-volant small mammals with 7 species.
The relative abundance was estimated by the total number of individuals per species
divided by the total number of individuals. The values for relative abundance in accordance to
both volant and non-volant are shown in table 1 and 2. By referring to the table, we can see that
the Rhinolopus affinis and Rhinolopus luctus recorded the highest relative abundance (18.18%)
of volant small mammals while Maxomys whiteheadi is the highest number of individuals
captured of non-volant small mammals (17.4%).
12
The species accumulation curve (Figure 2) and rank abundance plot/curve (Figure 3) for
small mammals were plotted to measure the sampling effort of total six days.
Species Accumulation Curve
14
Number of Species
12
10
8
Volant
6
Non-volant
4
2
0
1
2
3
4
5
6
Sampling Days
Figure 2: Observed species cumulative graph for volant and non-volant small mammals caught in
Gunung Gading NP for 6 days of sampling
The figure shows the accumulative number of species within days caught for volant and
non-volant small mammals. For volant, the number of species caught on the first day is 2 and
was increasing to 4 on the second day of sampling. As for non-volant, there were no species
captured on the first day, but it turned up to one species caught on the next day. On the third day,
9 and 6 species were recorded for volant and non-volant respectively. There were additional of 2
species for volant and 4 species of non-volant on the fourth day trapping. The number of species
captured was increasing on day 5 which shows 12 species of volant, while 11 species of nonvolant. On the last day of sampling, the number of species of volant has reached the asymptote
condition and it remained of 12 total species captured. However, for non-volant, there were still
one additional species recorded during the last day of sampling and this suggested that the
number of species caught might be increased as the total of the sampling day being increased.
As suggested by Rahman et al. (2010), species cumulative curve based on the trapping day,
indicate that more species could be yielded if a longer period of survey was conducted since the
number of non-volant small mammals has not reached the asymptote level (Figure 2).
13
Rank Abundance Curve
20
18
Log abundance
16
14
12
Volant
10
Non-volant
8
6
4
2
0
1
2
3
4
5
6
7
8
9
10
11
12
13
Figure 3: The rank abundance curve for volant and non-volant small mammals
The shape of the rank abundance curve can provide an indication of dominance or
evenness while the width of the horizontal curve indicates the species richness. In this study, the
species rank is based on the number of individuals of each species that we had caught during the
sampling days. Based on the Rank Abundance Curve for volant, the first and second rank species
have the highest relative abundance of 18.18% which ran for both Rhinolophus affinis and
Rhinolopus luctus. As for Rank Abundance Curve for non-volant, Maxomys whiteheadi (Rank 1)
has the highest relative abundance of 17.4%. This indicates that within 6 sampling days, all 3
species have the highest number of captured individuals than the other species for both volant
and non-volant small mammals.
14
Table 3: Diversity indices used to measure the species diversity in the primary forest
Diversity Index
Volant
Non-volant
Shannon
2.311
2.450
Simpson’s
0.8843
0.9036
The value of species diversity indices for volant and non-volant can be seen in Table 3.
Species diversity of small mammals was measured using the Shannon-Wiener Index (H’), which
is sensitive to changes in the abundance of rare species in a community, and the Simpson’s Index
(1-D), which is sensitive to changes in the most abundant species in a community (Solow, 1993).
The total number of volant species caught was 12 (H’= 2.311), while non-volant species captured
was 13 (H’= 2.450). Based from the table, the diversity indices for non-volant showed higher in
value compared to volant with the difference of
H’=0.139 and 1-D=0.193. The slightly
difference in diversity values of volant and non-volant is because there is only one species of
non-volant that makes it difference from volant small mammals in terms of the total species and
individuals captured. As a result, the diversity indices of non-volant small mammals indicates
that it has more species diversity by having higher number of unique species or greater species
evenness.
The use of species accumulation functions for the prediction of species richness. Almost
without exception, species richness can be neither accurately measured nor directly estimated by
observation because the observed number of species is a downward-biased estimator for the
complete (total) species richness of a local assemblage (Colwell et al. 2011). EstimateS by
Colwell (2005) computes seven non-parametric estimators of species richness and three of them
were used in this study. The estimated species richness using the formulae of Chao1, Jack1 and
ACE (Abundance Coverage-based Estimator) are three estimators that use a total abundance of 1
(singletons) or 2 (doubletons) in an abundance-based sample to estimate rare species in the few
samples.
15
Species Richness Estimation Curves (Volant)
30
No. of species
25
24
21
18
20
ACE Mean
15
Chao I mean
10
Jack 1 Mean
5
0
1
2
3
4
5
6
Sampling days
Figure 4: Species richness estimation curves for volant in Gunung Gading NP
by using EstimateS (Colwell, 2009)
From the above graph, ACE mean shows that the expected number of species is 24, while
Chao1 mean and Jack1 mean stated that there are 21 and 18 species respectively. Based on the
graph plotted, estimated potential species to be found at our study site is more higher than the
actual value of observed species found, which is only 12 species of volant. There are about
around 6 to 12 more species that can be discovered at our study site during six days of sampling.
This is casually caused by several factors that affecting our results. The unexpected weather of
heavy rains during the fourth day of sampling could lead to the declination of bats distribution in
the area. Another possible reason that could have cause to low capture of fruit bats, especially
(only 32% of total bats captured) and as a result of this above graph, there are few of human
disturbance mainly, tourism at present, as the primary forest has been less disturbed.
16
Species Richness Estimation Curves (Non-Volant)
25
21
18
16
No. of species
20
15
ACE Mean
10
Chao I mean
Jack 1 Mean
5
0
1
2
3
4
5
6
Sampling days
Figure 5: Species richness estimation curves for non-volant small mammals in
Gunung Gading NP by using EstimateS (Colwell, 2009)
For non-volant small mammals, the estimator of ACE mean, Chao1 mean and Jack1
mean stated that there are 21, 18 and 16 estimated potential species to be found at our study site.
However, the total species of non-volant that we found were only 13 species. Means, the unseen
species in the sampling site are about 3 to 8 species. This might due to insufficient skills, no
replacement of cage traps, lack of baits variability and the effect of habitat degradation. In
addition to this, the weather condition also a factor that contributes to this result.
17
DISCUSSIONS
Overall, there were 45 individuals and 25 species of small mammals captured during this
survey. We account for species diversity to show the species richness and species evenness in
our study site as it is one of the component of the concept of biodiversity. According to Krebs
(1989), species richness is the oldest and the simplest concept of species diversity that accounts
for the number of species in the community.
All bats comes from the order Chiroptera and a total of 12 species captured in primary
forest of Gunung Gading NP comprising 22 individuals throughout the six sampling days which
4 individuals come from family Pteropodidae, 6 individuals come from family Rhinolophidae
and lastly 2 individuals from family Hipposideridae. The most abundance species recorded are 4
individuals of species Rhinolophus affinis and Rhinolophus luctus respectively which both
species come from family Rhinolophidae.
More insectivorous bats than frugivorous bats were captured in this study (68% of the
total bat captured). This also representing 12.5% of the 96 chiropteran species recorded in
Borneo (Struebig et al, 2010). The trappings were focused in the forest understorey. This can be
mainly a result of insectivorous bats behaviour that forage understorey in a lowland forest, and
some of these bats is known to forage in groups (e.g. Hipposideros cervinus, Payne & Francis et
al. 1985). In this study, species from the family Hipposideridae and Rhinolophidae that were
caught mostly in harp traps, were one of the most common insectivorous families in the forest
interior with high manoeuvrability in light and good echolocators that allow them to efficiently
avoid mist nets (Francis 1989). Besides we also captured Rhinolophus trifoliatus and the
conservation status for this species was listed as least concern (IUCN 2010).
The number of bats captured in less disturbed primary forest was mostly occupied by
family Rhinolophidae (covered half of bats species captured) since they are nocturnal, active at
night. They would go search for food (insects) during that time. The existence of the
Rhinolophidae in primary forest abundantly is probably due to the suitability of roosting site
(Mohd-Azlan et al. 2005) as the habitat is less disturbed. The land in less disturbed forest had not
been explored and this is the reason why the amount of food source were enough for them to
18
survive. The traps including harp trap and mist net were all placed at unexposed areas. 10 mist
nets and 2 harp traps were used to set up at primary forest during the six days of sampling.
Whenever we captured bats in small number of individuals on certain sampling day, we
would try to relocate some of the mist net and harp trap and placed at more strategic place such
as between openings of two trees along the trail. As a result, the species accumulation graph that
we constructed has reached the asymptote. If the species are randomly and sequentially recorded
one after another within a sampling area, then the resulting accumulation curves are individualbased (Gotelli and Colwell 2001). This as a result of 22 individuals of volant captured which are
enough for our study purposes. Eventhough the species accumulation curve reaches an
asymptote after 6 days of sampling, the overall species diversity may not represent the bat fauna
of the entire Gunung Gading NP due to the limited number of sampling methods, duration of the
study, and types and structure of forest. These factors directly affect the number of species and
individuals that are likely to be captured (Kingston et al. 2003).
For the six sampling days of trapping non-volant, we managed to set up 45 cage traps at
the primary forest of Gunung Gading NP. Twenty cage traps, numbered from 1 until 20, were set
at trail A, while 25 cage traps, numbered from 21 until 45, were set at trail B. The cage trap that
we used in this study, is one of the most commonly used traps for small mammals such as rats,
squirrels and treeshrews (Payne et al. 2007). On our first sampling day, the cage traps was baited
with pineapple. As we got only one species on the first and second day of trapping, then we
decided to change the bait with banana. For the third day onwards, the number of species
captured kept increasing from 6 to 13 species. This is suggested that banana was shown to be the
most effective bait to attract small mammals and as for bait preference in our study. According to
Payne et al. (2007), small ripe bananas are one of the easiest to obtain and most effective baits.
Tuen (2000), also suggested that banana is the most effective bait to capture rodent in Sarawak.
As a result more rodents were captured compared to treeshrews in terms of species diversity.
During the six days of sampling, we managed to capture 23 individuals of 13 species
from three families from the order Scandentia (family Tupaiidae) and order Rodentia (family
Sciuridae and family Muridae). From these 23 individuals, nine individuals were under family
Tupaiidae, three individuals under family Sciuridae and the rest (11 individuals) were under
family Muridae. The most abundance species are Maxomys whiteheadi from the family Muridae
19
and this further supports that habitat in Gunung Gading NP where these specimens were
collected at less disturbed primary forest. The difference in numbers of species caught was due to
the soil and vegetation type. This also might be the sampling site was a less disturbed forest,
where there are fewer disturbances especially from humans. Species of the genus Maxomys are
the most common rodents in the Indo–Malayan region. They are distributed from mainland
Southeast Asia, throughout much of the Peninsular Malaysia to Borneo, Sulawesi, Sumatera,
Java and Palawan Island in the Philippines, as well as on several of the smaller islands of Sunda
Self (Anang Setiawan Achmadi, 2010).
As we constructed the species accumulation graph of these captured non-volants, our
graph did not reached its asymptote condition and the number of species kept increasing during
the six sampling days. This might due to insufficient skills, no replacement of the cage traps,
lack of baits variability and the effect of habitat degradation. As for that, there are many other
species of non-volant small mammals that have to be discovered.
Table 4: Diversity index and tests of significance for the two different study sites in
Gunung Gading National Park
Primary forest
Secondary forest
No. of species
25
19
Total individuals
45
53
3.075
2.534
Shannon diversity index
Significant test
Abundance species
p
FIELD SAMPLING REPORT
DEPARTMENT OF ZOOLOGY
Faculty of Resources Science and Technology
University of Malaysia Sarawak
Semester 1, Sesi 2013/2014
Diversity of Small Mammals at Less Disturbed
Primary Forest of Gunung Gading National Park
GROUP 1: MAMMALS
MEMBERS:
AHMAD FARHAN BIN MOHAMMED AMIN
MALINKA AK SIKIM
RIDHWAN BIN ABDUL RAHIM
ABANG MOHD HARIZT BIN ABG ABD KHALEX
AISYA FATHIYA BINTI CHE ROSLI
RACHEAL AK ROSEDY
PHILOVENNY ANAK PENGIRAN
EMY RITTA AK JINGGONG
BRENDA MAY ENGKIAN AK NANDONG @ SULIE
CHRIST HANI BT LIAN LEE
HILDA JELEMBAI AK NEILSON ILAN
DATE OF SUBMISSION: 10th DECEMBER 2014
LECTURER:
Dr. Mohd Azlan Jayasilan
1
40396
41989
43824
40320
40457
43768
43733
41118
40747
40907
41423
TABLE OF CONTENTS
Page
Abstract......................................................................................................................................... 3
1
Introduction...................................................................................................................... 5
-Objectives........................................................................................................................ 5
2
Materials and Methods..................................................................................................... 6
-Study Area....................................................................................................................... 6
-Field Methodology.......................................................................................................... 7
-Statistical Analysis.......................................................................................................... 8
-Species Identification and Preservation.......................................................................... 10
3
Results.............................................................................................................................. 11
4
Discussion........................................................................................................................ 18
5
Conclusion........................................................................................................................ 25
6
Recommendation............................................................................................................. 26
7
Acknowledgement........................................................................................................... 27
8
References........................................................................................................................ 28
9
Appendices....................................................................................................................... 30
2
Diversity of Small Mammals at Less Disturbed Primary
Forest of Gunung Gading National Park
M.AMIN, A.F., SIKIM, M., A.RAHIM, R., A.A.KHALEX, A.M.H., C.ROSLI, A.F., ROSEDY, R.,
PENGIRAN, P., JINGGONG, E.R., N.SULIE, B.M.E., L.LEE, C.H & N.ILAN, H.J.
Animal Resource Science and Management Program,
Faculty of Resource Science &Technology,Universiti Malaysia Sarawak,
94300 Kota Samarahan, Sarawak, Malaysia.
ABSTRACT
A study of field ecology aimed to document small mammals (volant and non-volant) was
conducted at less disturbed primary forest of Gunung Gading National Park (GGNP) from 18th to
23rd October 2014. This was a practical study on Field Ecology under the Department of Zoology
of Universiti Malaysia Sarawak (UNIMAS). Ten mist nets, two harp traps complete with bags
and 45 cage traps were set up for six sampling days. A total of 45 individuals from three orders,
six families and 25 species were caught in this study. Of the 12 species, four were frugivorous
bats and eight were insectivorous bats. On the other hand, there were comprised of 13 species of
non-volant small mammals, seven of them are from the family Muridae, four species from
Tupaiidae and two species from family Sciuridae. Our sampling site has several layers of
understory and mainly covered with lowland primary forest. This is evidence by the highest
abundance of Rhinolophus affinis and R. luctus for volant small mammals, and Maxomys
whiteheadi for non-volant small mammals. The increasing species cumulative curve for nonvolant small mammals indicates that there may be more species yet to be recorded from this
study site compared to Chiropteran. As a whole the study indicates that species diversity of
volant and non-volant small mammals is associated with the forest type and level of disturbance
in a particular area.
Keyword: Chiroptera, Rodentia, Scandentia, species diversity, primary forest, Gunung Gading
National Park
3
ABSTRAK
Satu kajian ekologi lapangan bertujuan untuk mendokumentasikan mamalia kecil telah
dijalankan di hutan asal Taman Negara Gunung Gading dari 18hb hingga 23hb Oktober 2014.
Ini merupakan kajian praktikal dalam kursus Ekologi Lapangan di bawah Jabatan Zoologi
Universiti Malaysia Sarawak (UNIMAS). Sebanyak sepuluh jaring kabus, dua perangkap 'harp
trap' lengkap dengan beg dan 45 perangkap tikus biasa telah digunakan sepanjang 6 hari kajian
tersebut. Sebanyak 45 individu daripada tiga order, enam famili dan 25 spesies telah ditangkap
dalam kajian ini. Daripada 12 spesies, empat adalah daripada kelawar jenis pemakanan buah
dan lapan adalah kelawar pemakanan serangga. Sebaliknya, daripada 13 spesies mamalia kecil
daratan, tujuh daripada mereka adalah dari famili Muridae, empat spesies dari Tupaiidae dan
dua spesies daripada famili Sciuridae. Kawasan lapangan kami mempunyai beberapa lapisan
tanah hutan yang terutamanya diliputi dengan hutan primer yang bertanah rendah. Disebabkan
itu, kelimpahan yang tinggi oleh Kelawar Ladam Hutan (Rhinolophus affinis) dan R. luctus
untuk mamalia kecil terbang, dan Maxomys whiteheadi untuk mamalia kecil daratan. Graf
kumulatif spesies yang masih meningkat menunjukkan potensi penemuan banyak lagi spesies
yang masih belum direkodkan di kawasan ini, terutamanya bagi spesies mamalia kecil daratan
berbanding mamalia kecil terbang iaitu kelawar. Secara keseluruhannya kajian ini menunjukkan
bahawa kepelbagaian spesies kelawar dan mamalia kecil daratan dikaitkan dengan jenis hutan
dan tahap gangguan dalam suatu kawasan tertentu.
Kata kunci: Chiroptera, Rodentia, Scandentia, kepelbagaian spesies, hutan primer, Taman
Negara Gunung Gading
4
INTRODUCTION
The small mammals can be defined as a group of mammal that are small in size and
weight less than 5 kg. Small mammals can be divided into two types, namely volant and nonvolant. Non-volant small mammals belong to orders Scandentia, Rodentia, and Insectivora which
are non-flying mammals. Whereas volant small mammals exclusively are belong to order
Chiroptera. Bats are mammals in order Chiroptera. They are different from other mammals
because they can fly. They are the second largest order in class Mammalia after rats and squirrels
in term of biodiversity (Rahman et al. 2011). According to Payne et al. (2007), species of bats in
Borneo are classified into 8 families. They are distinguished based on ear shape, muzzle shape,
tail pattern and presence of noseleaf (Payne et al. 2007). Chiroptera are further divided into
suborder Megachiroptera and Microchiroptera. In terms of bats diversity, there are 96 species of
bats in Borneo harbours (Struebig et al, 2010), which made up 42% of mammals species in
Borneo. Sarawak itself recorded 73 species of bats (Jayaraj, 2008).
The most abundant group comprises of rats and mice (Muridae), which can be found on
the ground but also in the canopy. In contrast, treeshrew (Scandentia) have basically diversified
on the ground, with only two out of five abundant lowland species exploring the canopy space,
Tupaia minor and Ptilocercus lowii (Sargis, 2002; Wells et al., 2004).
OBJECTIVES
1. To determine the species diversity of volant and non-volant small mammals at less disturbed
primary forest in Gunung Gading National Park.
2. To determine the species richness and relative abundance of volant and non-volant small
mammals.
3. To compare the findings with previous studies on small mammals in Sarawak and Peninsular
Malaysia.
5
MATERIALS AND METHODS
Study Area
A sampling survey of small mammals was conducted at Gunung Gading National Park
(N O10 42.00’ E 1090 50.20’) Lundu, southeast of Sarawak which is located 80 km from west of
Kuching. Gunung Gading NP is mainly composed by tropical rainforest which most species-rich
terrestrial ecosystem on earth. The highest peak Of Gunung Gading NP rises to the height of
965m above sea level (a.s.l) which composed of remains of an old British jungle base during the
communist insurgency of the 1960's. It has a wide range of habitats including the riverine
vegetation, hill dipterocarp forest, lower and upper montane forest. Gunung Gading NP are fully
reserve forest under Sarawak Forestry Department, Malaysia and were gazetted as a park in
August 1983 primarily to provide a conservation zone for protection of the Rafflesia (Sarawak
Forestry Corporation, 2006) and it is now well known as place for camping, mother nature
exploration and recreation.
During the field ecology work, a survey was done mainly on species diversity of small in
the primary forest. Our sampling site was conducted at less disturbed primary forest that covered
with mixed dipterocarp forest, full ceiling canopy and several layers of understory. The ground
floor is generally clear of heavy vegetation. The primary forest is labelled as less disturbed forest
where less human intervention occurs in the forest. Therefore, we were interested to discover the
species diversity of the forest.
6
Figure 1: Location of study (source: Google map, 2013), Gunung Gading NP that
has an area of 4,106 hectares.
Field Methodology
A sampling survey of small mammals was conducted from from 18th until 23rd October
2014. There were ten mist nets, two harp traps complete with bags and 45 cage traps were set up
throughout the sampling period. Mist nets that shared with aves taxa, were put up along the
forest trail and over the stream. The harp traps were deployed between trees and narrow paths in
the forest. The mist nets and harp traps were checked regularly at 0530 and for every two hours
from 1800 to 2400 hours for 6 sampling days. The cage traps were placed on the ground near to
the main trail, a distance of 5 meters between the centre points along the trail and approximate
distance of 10 meters apart form each other. These traps were checked twice a day and re-baited
if necessary. The first checking was done in the morning around 1000 hours and the second
checking was done around 1700 hours in the evening. For the first sampling day we used
pineapples for bait and the second day onwards we switched the bait by using banana.
7
Statistical Analysis
Diversity Indices
In order to have an effective measure of diversity in a community, we need to account (in
most instances) for both species richness and the evenness with which individuals are distributed
among species. Species diversity is a measure of the diversity within an ecological community
that incorporates both species richness (the number of species in a community) and the evenness
of species abundances. Species richness is the number of different species in a particular area.
Species evenness is the relative abundance with which each species are represented in an area.
One way to do this is through the use of a proportional abundance index. While more than 60
indices have been described, we used the two most widely used in the ecological literature:
Simpson's and Shannon-Weiner Index.
1) Shannon Index (H´)
The Shannon's diversity index (H’), also known as communication entropy, was
introduced by Claude Shannon (1948). The Shannon-Weaver Index (H’) measures overall
biodiversity. It assumes that all species are represented in a sample and the sample was obtained
randomly. H is maximized when all species have the same number of animals collected.
Shannon Index was also used for the calculation in Zar (1999) modified t-test to test the
hypotheses that the two sampling areas (primary and secondary forest) were different in species
abundance.
S
H pi . ln( pi )
i 1
where:
H’= Shannon diversity index
S = numbers of species encountered
pi is the proportion of individuals found in the ith species.
ln is the natural logarithm.
8
2) Simpson’s Index (1-D)
Simpson's Index is considered a dominance index because it weights towards the
abundance of the most common species. Simpson's Index gives the probability of any two
individuals drawn at random from an infinitely large community belonging to different species.
The bias corrected form of Simpson's Index is:
ni ni 1
i 1 N N 1
S
Ds
Where
ni = number of individuals in ith species
N = number of individuals in all species
Simpson’s Index of Diversity = 1-D
Simpson’s Reciprocal Index = 1/D
Rank Abundance Curve
The rank abundance curve/plot is plotted by ranking from the highest abundance to the
lowest abundance in X-axis. Ranking species from most abundant to least provides another
useful way to visualize community data, this allow us to make comparisons of samples of
different sizes. It is the comparison of abundance of the species of a group of organisms in a
given locality. Y-axis shows the relative species abundance measured in a log scale, because
plotting the data on a log scale allows for better data visualization. It can also be used to visualise
species richness and species evenness. It overcomes the shortcomings of biodiversity indices that
cannot display the relative role different variables played in their calculation.
9
Species Accumulation Curve
A species accumulation curve is the graph of the cumulative number of observed species
as a function of some measure of sampling effort (Colwell et al. 2004). The species accumulation
curve also indicates whether we have captured all the species which we suppose to catch in the
population of our study site. So this graph can also be used to estimate the species richness,
which important to estimate the number of overall species present at the site. Species richness is
the most commonly used biodiversity indicators for conservation correspondence.
Non-parametric estimator
Species richness can be estimated by using three approaches (Magurran 2004), but for
this study we used non-parametric estimators. This method is for estimating species richness
from samples which were adapted from mark-recapture applications for estimating population
size. They also require no assumptions about community structure (Colwell and Coddington
1995). Species richness estimators attempt to predict the asymptote of the species accumulation
curve, thus correcting for the downward bias inherent in observed species richness. Richness
estimators predict richness, including species not discovered in the sample, from the proportional
abundances of species within the total sample (Sobero´n and Llorente 1993; Colwell 2005).
Species Identification and Preservation
Species identification and measurement followed A Field Guide to the Mammals of
Borneo (Payne et al. 2007). For each individual caught, external measurements were conducted,
recorded and used to identify the species before released back to the forest. There were two
species include both volant and non-volant small mammals that were collected as wet specimens
preserved in 70% ethanol. The specimens were deposited in Universiti Malaysia Sarawak
(UNIMAS) Zoological Museum.
10
RESULTS
A total of 45 individuals of small mammals from Order Chiroptera, Rodentia and Scandentia
were caught during the sampling period. From the six days of trapping, 25 species of small
mammals were recorded. These were eight insectivorous bats, four frugivorous bats, seven rats,
two squirrels and four treeshrews (Table 1 and 2). The insectivorous bats captured were
representing the family Rhinolophidae and Hipposideridae, whereas the frugivorous bats were
from the family Pteropodidae. As for the rodents, rats were from the family Muridae and
squirrels from the family Sciuridae, while treeshrews from the family Tupaiidae.
Table 1: List of volant species in Gunung Gading NP (18th -23rd October 2014).
N=Total individuals, RA=Relative abundance
Family
Species Name
Common Name
N
RA%
Hipposideridae
Hipposideros cervinus
Fawn Roundleaf Bat
2
9.09
Hipposideros dyacorum
Dayak Roundleaf Bat
1
4.54
Cynopterus brachyotis
Short-nose Fruit Bat
3
13.64
Penthetor lucasii
Dusky Fruit Bat
2
9.09
Dyacopterus spadiceus
Dayak Fruit Bat
1
4.54
Balionycteris maculata
Spotted-winged Fruit Bat
1
4.54
Rhinolopus arcuatus
Arcuate Horseshoe Bat
1
4.54
Rhinolopus affinis
Intermediate Horseshoe Bat
4
18.18
Rhinolopus luctus
Great Woolly Horseshoe Bat
4
18.18
Rhinolopus borneensis
Bornean Horseshoe Bat
1
4.54
Rhinolopus trifoliatus
Trefoil Horseshoe Bat
1
4.54
Rhinolopus creaghi
Creagh’s Horseshoe Bat
1
4.54
22
100
Pteropodidae
Rhinolophidae
Total
12
11
Table 2: List of non-volant species in Gunung Gading NP (18th -23rd October 2014).
N=Total individuals, RA=Relative abundance
Order
Family
Species
Common Name
N
RA%
Rodentia
Muridae
Sundamys muelleri
Muller’s Rat
1
4.35
Maxomys whiteheadi
White Head’s Rat
4
17.4
Maxomys surifer
Red Spiny Rat
1
4.35
Maxomys rajah
Brown Spiny Red
1
4.35
Niviventer cremoriventer Dark-tailed Tree Rat
2
8.7
Rattus tiomanicus
Malaysian Field Rat
1
4.35
Leopoldamys sabanus
Long-tailed Giant Rat
1
4.35
Lariscus insignis
Three-striped Ground Squirrel
2
8.7
Sundasciurus lowii
Low’s Squirrel
1
4.35
Large Treeshrew
3
13.64
Tupaia minor
Lesser Treeshrew
2
8.7
Tupaia gracilis
Slender Treeshrew
2
8.7
Tupaia picta
Painted Treeshrew
2
8.7
23
100
Sciuridae
Scandentia Tupaiidae Tupaia tana
Total
13
For the species richness, the most recorded order for small mammals is order Chiroptera
with 12 species. There are six families of small mammals recorded, and family Muridae has the
most caught species of non-volant small mammals with 7 species.
The relative abundance was estimated by the total number of individuals per species
divided by the total number of individuals. The values for relative abundance in accordance to
both volant and non-volant are shown in table 1 and 2. By referring to the table, we can see that
the Rhinolopus affinis and Rhinolopus luctus recorded the highest relative abundance (18.18%)
of volant small mammals while Maxomys whiteheadi is the highest number of individuals
captured of non-volant small mammals (17.4%).
12
The species accumulation curve (Figure 2) and rank abundance plot/curve (Figure 3) for
small mammals were plotted to measure the sampling effort of total six days.
Species Accumulation Curve
14
Number of Species
12
10
8
Volant
6
Non-volant
4
2
0
1
2
3
4
5
6
Sampling Days
Figure 2: Observed species cumulative graph for volant and non-volant small mammals caught in
Gunung Gading NP for 6 days of sampling
The figure shows the accumulative number of species within days caught for volant and
non-volant small mammals. For volant, the number of species caught on the first day is 2 and
was increasing to 4 on the second day of sampling. As for non-volant, there were no species
captured on the first day, but it turned up to one species caught on the next day. On the third day,
9 and 6 species were recorded for volant and non-volant respectively. There were additional of 2
species for volant and 4 species of non-volant on the fourth day trapping. The number of species
captured was increasing on day 5 which shows 12 species of volant, while 11 species of nonvolant. On the last day of sampling, the number of species of volant has reached the asymptote
condition and it remained of 12 total species captured. However, for non-volant, there were still
one additional species recorded during the last day of sampling and this suggested that the
number of species caught might be increased as the total of the sampling day being increased.
As suggested by Rahman et al. (2010), species cumulative curve based on the trapping day,
indicate that more species could be yielded if a longer period of survey was conducted since the
number of non-volant small mammals has not reached the asymptote level (Figure 2).
13
Rank Abundance Curve
20
18
Log abundance
16
14
12
Volant
10
Non-volant
8
6
4
2
0
1
2
3
4
5
6
7
8
9
10
11
12
13
Figure 3: The rank abundance curve for volant and non-volant small mammals
The shape of the rank abundance curve can provide an indication of dominance or
evenness while the width of the horizontal curve indicates the species richness. In this study, the
species rank is based on the number of individuals of each species that we had caught during the
sampling days. Based on the Rank Abundance Curve for volant, the first and second rank species
have the highest relative abundance of 18.18% which ran for both Rhinolophus affinis and
Rhinolopus luctus. As for Rank Abundance Curve for non-volant, Maxomys whiteheadi (Rank 1)
has the highest relative abundance of 17.4%. This indicates that within 6 sampling days, all 3
species have the highest number of captured individuals than the other species for both volant
and non-volant small mammals.
14
Table 3: Diversity indices used to measure the species diversity in the primary forest
Diversity Index
Volant
Non-volant
Shannon
2.311
2.450
Simpson’s
0.8843
0.9036
The value of species diversity indices for volant and non-volant can be seen in Table 3.
Species diversity of small mammals was measured using the Shannon-Wiener Index (H’), which
is sensitive to changes in the abundance of rare species in a community, and the Simpson’s Index
(1-D), which is sensitive to changes in the most abundant species in a community (Solow, 1993).
The total number of volant species caught was 12 (H’= 2.311), while non-volant species captured
was 13 (H’= 2.450). Based from the table, the diversity indices for non-volant showed higher in
value compared to volant with the difference of
H’=0.139 and 1-D=0.193. The slightly
difference in diversity values of volant and non-volant is because there is only one species of
non-volant that makes it difference from volant small mammals in terms of the total species and
individuals captured. As a result, the diversity indices of non-volant small mammals indicates
that it has more species diversity by having higher number of unique species or greater species
evenness.
The use of species accumulation functions for the prediction of species richness. Almost
without exception, species richness can be neither accurately measured nor directly estimated by
observation because the observed number of species is a downward-biased estimator for the
complete (total) species richness of a local assemblage (Colwell et al. 2011). EstimateS by
Colwell (2005) computes seven non-parametric estimators of species richness and three of them
were used in this study. The estimated species richness using the formulae of Chao1, Jack1 and
ACE (Abundance Coverage-based Estimator) are three estimators that use a total abundance of 1
(singletons) or 2 (doubletons) in an abundance-based sample to estimate rare species in the few
samples.
15
Species Richness Estimation Curves (Volant)
30
No. of species
25
24
21
18
20
ACE Mean
15
Chao I mean
10
Jack 1 Mean
5
0
1
2
3
4
5
6
Sampling days
Figure 4: Species richness estimation curves for volant in Gunung Gading NP
by using EstimateS (Colwell, 2009)
From the above graph, ACE mean shows that the expected number of species is 24, while
Chao1 mean and Jack1 mean stated that there are 21 and 18 species respectively. Based on the
graph plotted, estimated potential species to be found at our study site is more higher than the
actual value of observed species found, which is only 12 species of volant. There are about
around 6 to 12 more species that can be discovered at our study site during six days of sampling.
This is casually caused by several factors that affecting our results. The unexpected weather of
heavy rains during the fourth day of sampling could lead to the declination of bats distribution in
the area. Another possible reason that could have cause to low capture of fruit bats, especially
(only 32% of total bats captured) and as a result of this above graph, there are few of human
disturbance mainly, tourism at present, as the primary forest has been less disturbed.
16
Species Richness Estimation Curves (Non-Volant)
25
21
18
16
No. of species
20
15
ACE Mean
10
Chao I mean
Jack 1 Mean
5
0
1
2
3
4
5
6
Sampling days
Figure 5: Species richness estimation curves for non-volant small mammals in
Gunung Gading NP by using EstimateS (Colwell, 2009)
For non-volant small mammals, the estimator of ACE mean, Chao1 mean and Jack1
mean stated that there are 21, 18 and 16 estimated potential species to be found at our study site.
However, the total species of non-volant that we found were only 13 species. Means, the unseen
species in the sampling site are about 3 to 8 species. This might due to insufficient skills, no
replacement of cage traps, lack of baits variability and the effect of habitat degradation. In
addition to this, the weather condition also a factor that contributes to this result.
17
DISCUSSIONS
Overall, there were 45 individuals and 25 species of small mammals captured during this
survey. We account for species diversity to show the species richness and species evenness in
our study site as it is one of the component of the concept of biodiversity. According to Krebs
(1989), species richness is the oldest and the simplest concept of species diversity that accounts
for the number of species in the community.
All bats comes from the order Chiroptera and a total of 12 species captured in primary
forest of Gunung Gading NP comprising 22 individuals throughout the six sampling days which
4 individuals come from family Pteropodidae, 6 individuals come from family Rhinolophidae
and lastly 2 individuals from family Hipposideridae. The most abundance species recorded are 4
individuals of species Rhinolophus affinis and Rhinolophus luctus respectively which both
species come from family Rhinolophidae.
More insectivorous bats than frugivorous bats were captured in this study (68% of the
total bat captured). This also representing 12.5% of the 96 chiropteran species recorded in
Borneo (Struebig et al, 2010). The trappings were focused in the forest understorey. This can be
mainly a result of insectivorous bats behaviour that forage understorey in a lowland forest, and
some of these bats is known to forage in groups (e.g. Hipposideros cervinus, Payne & Francis et
al. 1985). In this study, species from the family Hipposideridae and Rhinolophidae that were
caught mostly in harp traps, were one of the most common insectivorous families in the forest
interior with high manoeuvrability in light and good echolocators that allow them to efficiently
avoid mist nets (Francis 1989). Besides we also captured Rhinolophus trifoliatus and the
conservation status for this species was listed as least concern (IUCN 2010).
The number of bats captured in less disturbed primary forest was mostly occupied by
family Rhinolophidae (covered half of bats species captured) since they are nocturnal, active at
night. They would go search for food (insects) during that time. The existence of the
Rhinolophidae in primary forest abundantly is probably due to the suitability of roosting site
(Mohd-Azlan et al. 2005) as the habitat is less disturbed. The land in less disturbed forest had not
been explored and this is the reason why the amount of food source were enough for them to
18
survive. The traps including harp trap and mist net were all placed at unexposed areas. 10 mist
nets and 2 harp traps were used to set up at primary forest during the six days of sampling.
Whenever we captured bats in small number of individuals on certain sampling day, we
would try to relocate some of the mist net and harp trap and placed at more strategic place such
as between openings of two trees along the trail. As a result, the species accumulation graph that
we constructed has reached the asymptote. If the species are randomly and sequentially recorded
one after another within a sampling area, then the resulting accumulation curves are individualbased (Gotelli and Colwell 2001). This as a result of 22 individuals of volant captured which are
enough for our study purposes. Eventhough the species accumulation curve reaches an
asymptote after 6 days of sampling, the overall species diversity may not represent the bat fauna
of the entire Gunung Gading NP due to the limited number of sampling methods, duration of the
study, and types and structure of forest. These factors directly affect the number of species and
individuals that are likely to be captured (Kingston et al. 2003).
For the six sampling days of trapping non-volant, we managed to set up 45 cage traps at
the primary forest of Gunung Gading NP. Twenty cage traps, numbered from 1 until 20, were set
at trail A, while 25 cage traps, numbered from 21 until 45, were set at trail B. The cage trap that
we used in this study, is one of the most commonly used traps for small mammals such as rats,
squirrels and treeshrews (Payne et al. 2007). On our first sampling day, the cage traps was baited
with pineapple. As we got only one species on the first and second day of trapping, then we
decided to change the bait with banana. For the third day onwards, the number of species
captured kept increasing from 6 to 13 species. This is suggested that banana was shown to be the
most effective bait to attract small mammals and as for bait preference in our study. According to
Payne et al. (2007), small ripe bananas are one of the easiest to obtain and most effective baits.
Tuen (2000), also suggested that banana is the most effective bait to capture rodent in Sarawak.
As a result more rodents were captured compared to treeshrews in terms of species diversity.
During the six days of sampling, we managed to capture 23 individuals of 13 species
from three families from the order Scandentia (family Tupaiidae) and order Rodentia (family
Sciuridae and family Muridae). From these 23 individuals, nine individuals were under family
Tupaiidae, three individuals under family Sciuridae and the rest (11 individuals) were under
family Muridae. The most abundance species are Maxomys whiteheadi from the family Muridae
19
and this further supports that habitat in Gunung Gading NP where these specimens were
collected at less disturbed primary forest. The difference in numbers of species caught was due to
the soil and vegetation type. This also might be the sampling site was a less disturbed forest,
where there are fewer disturbances especially from humans. Species of the genus Maxomys are
the most common rodents in the Indo–Malayan region. They are distributed from mainland
Southeast Asia, throughout much of the Peninsular Malaysia to Borneo, Sulawesi, Sumatera,
Java and Palawan Island in the Philippines, as well as on several of the smaller islands of Sunda
Self (Anang Setiawan Achmadi, 2010).
As we constructed the species accumulation graph of these captured non-volants, our
graph did not reached its asymptote condition and the number of species kept increasing during
the six sampling days. This might due to insufficient skills, no replacement of the cage traps,
lack of baits variability and the effect of habitat degradation. As for that, there are many other
species of non-volant small mammals that have to be discovered.
Table 4: Diversity index and tests of significance for the two different study sites in
Gunung Gading National Park
Primary forest
Secondary forest
No. of species
25
19
Total individuals
45
53
3.075
2.534
Shannon diversity index
Significant test
Abundance species
p