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Diet of Five Common Anurans Found In Disturbed Areas in Northern

Peninsular Malaysia
Thesis · February 2015

DOI: 10.13140/RG.2.1.4481.9443
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DIET OF FIVE COMMON ANURANS FOUND IN
DISTURBED AREAS IN NORTHERN
PENINSULAR MALAYSIA
by
YAP CHEE HUI
A thesis submitted in fulfilment of the

requirements for the degree of Master of
Science in Zoology.
February 2015
ACKNOWLEDGEMENT
I would like to express my utmost gratitude to my supervisor Prof. Ibrahim
Jaafar for his guidance, help and advice during the period of my study. His
understanding and support not only brought about the fruition of this thesis, but also
boost my personal development and character building.
Also, many thanks to the members of my supervisory committee, for their
suggestions and constructive critiques. I am also grateful for the assistance and
recommendations from my fellow colleagues: Amirah Hurzaid and Zalina Awang; and
for the dedication and support of field assistant Mohd Azmeer Abu Bakar. I am
grateful to my family, for their unwavering support and encouragement.
Additionally, I would like to thank the School of Biological Sciences and
School of Distance Education, Universiti Sains Malaysia for facilities provided. Last
but not least, this study would not have been possible without the research grant by
IPS Graduate Fund 1001/PJJAUH/834068 and USM Fellowship.
ii
TABLE OF CONTENTS
pages
Acknowledgment ii
Table of Contents iii
List of Figures vi
List of Tables viii
List of Symbols and Abbreviations x
Abstrak (Abstract in Malay Language) xi
Abstract xiii
CHAPTER 1 - INTRODUCTION
1.1 Introduction 1
1.2 Objectives 3
CHAPTER 2 - LITERATURE REVIEW
2.1 Amphibians in General 4
2.2 Habitat and Distribution 7
2.3 Anuran in General 8
2.4 Classification of Frog and Toad 15
2.5 Description of Specimens 17
2.6 Digestive System 26
2.7 Diet and Feeding Ecology 29
2.8 Food Availability 32
2.9 Species Niches 33
2.10 Ecological Roles of Amphibians 34
2.11 Amphibian Decline 37
iii
CHAPTER 3 - MATERIALS AND METHODS
3.1 Study Sites 39
3.2 Experimental Procedures 42
3.2.1 Collection of Specimens 43
3.2.2 Morphometric Measurements 45
3.2.3 Collection of Stomach Content 46
3.3.4 Data Analysis 47
CHAPTER 4 - RESULTS
4.1 Basic Morphology of Specimens 52
4.2 Specimen Availability According to Study Sites 58
4.3 Prey Availability of Study Sites 60
4.4 Stomach Contents of the Specimens 62
4.4.1 Stomach Contents of Duttaphrynus 68
melanostictus
4.4.2 Stomach Contents of Microhyla butleri 71
4.4.3 Stomach Contents of Microhyla fissipes 74
4.4.4 Stomach Contents of Microhyla heymonsi 77
4.4.5 Stomach Contents of Polypedates leucomystax 79
4.5 Mouth Width and Its Effect on Size of Prey 81
4.6 Diversity Index, Niche Breath and Niche Overlap 83
iv
CHAPTER 5 - DISCUSSIONS
5.1 Basic Morphometry of the Five Anurans 84
5.2 Specimen Availability to Study Sites 87
5.3 Prey Availability of Study Sites 88
5.4 Diet 89
5.4.1 Diet of Duttaphrynus melanostictus 91
5.4.2 Diet of Microhylids 94
5.4.3 Diet of Polypedates leucomystax 97
5.5 Relationships of Morphology of the Anurans and Prey 99
5.6 Dietary Niches of the Anurans 100
CHAPTER 6 - CONCLUSIONS 102
Bibliography 105
List of Publications 118
Appendices 119
v
LIST OF FIGURES
Figure 2.1 External characteristics of frogs and toads.
Figure 2.2 The digestive system of a frog. (modified from Md Hanapi &
Ibrahim, 1986)
Figure 3.1 Location of study sites: In Langkawi island, Kedah: (A) site TT; (B)
site PK; (C) site UM; In Penang state, (D) site SB; (E) site TRTB;
(F) site USM; (G) site PSD; In Kedah state, (H) site KR; (I) site UP;
(J) site SD; (K) site BP; In Perak state, (L) site GLRP. (Google
Maps, 2013)
Figure 3.2 Research flow chart.
Figure 4.1 Number of specimens collected, according to species
Figure 4.2 Frogs and toad species: (A) Duttaphrynus melanostictus; (B)
Microhyla butleri; (C) Microhyla fissipes; (D) Microhyla heymonsi;
and (E) Polypedates leucomystax.
Figure 4.3 The number of sub-adults (juvenile males and females), adult males
and adult females across species.
Figure 4.4 Empty versus non-empty stomachs, according to species.
Figure 4.5 (A) Percentage of insect versus non-insect diet in overall diet
composition; (B) Percentage of insect vs non-insect diet of D.
melanostictus; (C) Percentage of insect vs non-insect diet of M.
butleri; (D) Percentage of insect vs non-insect diet of M. fissipes; (E)
Percentage of insect vs non-insect diet of M. heymonsi; (F)
Percentage of insect versus non-insect diet of P. leucomystax.
vi
Figure 4.6 (A) Percentage of pest versus non-pest diet in overall diet
composition; (B) Percentage of pest vs non-pest diet of D.
melanostictus; (C) Percentage of pest vs non-pest diet of M. butleri;
(D) Percentage of pest vs non-pest diet of M. fissipes; (E) Percentage
of pest vs non-pest diet of M. heymonsi; (F) Percentage of pest
versus non-pest diet of P. leucomystax.
Figure 4.7 Scatterplot of MW versus prey volume of Duttaphrynus

melanostictus, showing the linear regression (VMAX: y=11.71x –
52.36, r2=0.3461; VMIN: y=5.748x - 22.62, r2=0.1630)
Figure 4.8 Combined scatterplot of MW versus VMAX of Microhyla butleri

(M.b), Microhyla fissipes (M.f) and Microhyla heymonsi (M.h).
Figure 4.9 Combined scatterplot of MW versus VMIN of Microhyla butleri

(M.b), Microhyla fissipes (M.f) and Microhyla heymonsi (M.h).
vii
LIST OF TABLES
Table 3.1 Criteria for habitat disturbances.
Table 4.1 The mean, maximum value, and minimum value of snout-to-vent
length (SVL, mm) of specimens, separated by sex.
Table 4.2 Maximum, minimum, and mean of male and female specimens’
weight (g).
Table 4.3 Range and mean of mouth width (MW, mm) of specimens.
Table 4.4 Relative abundance of amphibian species according to study sites.
Table 4.5 Prey items found in study sites.
Table 4.6 Non-prey items that were consumed and found in stomachs of
specimens.
Table 4.7 The dietary composition (N; as a % of the total number of recorded
prey items), and frequency of occurrence (F; the number of anurans,
as a %, of each species) of the dietary items of Duttaphrynus
melanostictus, Polypedates leucomystax, Microhyla butleri,
Microhyla fissipes, and Microhyla heymonsi in this study. (Total=the
total number of prey items).
Table 4.8 The dietary composition (N; % of the total number of recorded prey
items), frequency of occurrence (F; % of the number of stomachs),
volume (V; % of the total volume of prey items), and Importance
Index (AI) of the dietary items of Duttaphrynus melanostictus in this
study.
Table 4.9 The Formicidae diet (N; % of the total number of recorded prey
Index (AI) of the dietary items of Duttaphrynus melanostictus in this
study.
viii
Index (AI) of the dietary items of Microhyla butleri.
Index (AI) of the dietary items of Microhyla butleri in this study.
Index (AI) of the dietary items of Microhyla fissipes.
Index (AI) of the dietary items of Microhyla fissipes.
Index (AI) of the dietary items of Microhyla heymonsi.
Index (AI) of the dietary items of Microhyla heymonsi.
volume (V; % of the total volume of prey items), and Importance Index
(AI) of the dietary items of Polypedates leucomystax in this study.
Table 4.17 Diversity index (H’), niche breadth (B), standardized niche breadth
(BA), and niche overlap (O) of specimens.
ix
LIST OF SYMBOLS AND ABBREVIATIONS
USM Universiti Sains Malaysia
USMARC Universiti Sains Malaysia Amphibian Reptile
Collection
o
”’ degree minute second
a.s.l. above sea level
MW mouth width
SVL snout to vent length
df degree of freedom
P probability
VMAX maximum prey volume
VMIN minimum prey volume
x
PEMAKANAN LIMA SPECIES KATAK YANG BIASA
DITEMUI DI KAWASAN TERGANGGU DI UTARA
SEMENANJUNG MALAYSIA
ABSTRAK
Analisis kandungan perut lima spesies katak yang biasa dijumpai di kawasan
terganggu , iaitu Duttaphrynus melanostictus (Schneider, 1799), Polypedates
leucomystax (Gravenhorst, 1829), Microhyla heymonsi (Vogt, 1911), Microhyla
butleri (Boulenger, 1900) dan Microhyla fissipes (Boulenger, 1884), telah dijalankan
dari Oktober 2012 hingga Mac 2013. Sebanyak 387 spesimen telah dikumpulkan dari
dua belas terganggu kawasan di utara Semenanjung Malaysia, yang terdiri daripada
120 ekor D. melanostictus, 86 ekor M. butleri, 77 ekor M. fissipes, 53 ekor M.
heymonsi dan 51 ekor P. leucomystax. Sebanyak 42 kumpulan mangsa telah dikenal
pasti (sekurang-kurangnya ke tahap famili), dengan 14 kumpulan mangsa yang juga
ditemui dalam persekitaran kawasan kajian dengan menggunakan perangkap pelekat.
Platygasteridae, Formicidae dan Araneae hadir dalam diet kesemua spesies katak.
Makanan dominan untuk D. melanostictus ialah semut (F= 30.91) dan kumbang tanah
(F=13.18), untuk tiga spesies katak Microhyla ialah semut (F>50), dan untuk P.
leucomystax ialah rama-rama (F=18.52) dan kumbang daun (F=14.81). Formicidae
merupakan mangsa utama yang ditemui kerana banyak terdapat dalam persekitaran
(43.20%). Analisa pemakanan menunjukkan bahawa P. leucomystax ialah pemangsa
umum atau “generalist” dan D. melanostictus adalah generalist yang memberi
xi
keutamaan kepada semut. Sementara itu, M. butleri , M. fissipes , dan M. heymonsi
ialah pemangsa pakar semut atau “ant-specialist”. Kajian ini juga menunjukkan
bahawa saiz mangsa D. melanostictus mempunyai korelasi positif dengan lebar mulut
(PVmax<0.0001, PVmin=0.0017). Bagi katak Microhyla, lebar mulut tidak memberi
kesan kepada saiz mangsa (P>0.5). Dari segi kepelbagaian mangsa, hanya D.
melanostictus dan P. leucomystax menunjukkan kepelbagaian mangsa tinggi. Namun
keluasan nic pemakanan kesemua spesies menunjukkan nilai yang rendah, dengan
pengecualian kepada P. leucomystax. Pertindihan nic adalah sangat kecil antara katak-
katak Microhyla dengan P. Leucomystax.. Kajian ini menyumbang sedikit pemahaman
kepada evolusi myrmecophagy pada amfibia secara keseluruhannya.
xii
DIET OF FIVE COMMON ANURANS FOUND IN
DISTURBED AREAS IN NORTHERN PENINSULAR
MALAYSIA
Abstract
Analyses of stomach contents of five species of commonly found disturbed
area frogs, namely Duttaphrynus melanostictus (Schneider, 1799), Polypedates
leucomystax (Gravenhorst, 1829), Microhyla heymonsi (Vogt, 1911), Microhyla
butleri (Boulenger, 1900) and Microhyla fissipes (Boulenger, 1884), were carried out
from October 2012 until March 2013. A total of 387 specimens were collected from
twelve disturbed areas in northern Peninsular Malaysia, consisting of 120 individuals
of D. melanostictus, 86 M. butleri, 77 M. fissipes, 53 M. heymonsi and 51 P.
leucomystax. A total of 42 prey groups were identified (at least to family level), with
14 of the prey groups also found in the environment using glue traps. Platygasteridae,
Formicidae and Araneae were present in the diets of all five anuran species. The
dominant prey items for D. melanostictus were ants (F=30.91) and ground beetles
(F=13.18), for the three microhylids were ants (F>50), and for P. leucomystax were
moths (F=18.52) and leaf beetles (F=14.81). Formicidae was the major prey of five
anurans, because of its abundance in the environment (43.20%). Diet analysis shows
that P. leucomystax was most probably a generalist and D. melanostictus was a
generalist with preference for ants. Meanwhile, M. butleri, M. fissipes, and M.
heymonsi were ant-specialists. This study also shows that prey size of D. melanostictus
xiii
was positively correlated with mouth width (PVmax<0.0001, PVmin=0.0017). For the
microhylids, mouth width had no effect on prey size (P>0.5). In terms of prey diversity,
only D. melanostictus and P. leucomystax showed high prey diversity, but for dietary
niche breadth, all species showed low values, except for P. leucomystax. The least
niche overlap was shown between the microhylids and P. leucomystax. This study
contributes some understanding to the evolution of myrmecophagy in amphibians as a
whole.
xiv
CHAPTER 1
Introduction
1.1 Introduction
Malaysia is one of the hotspots for tropical biodiversity in the world (Ibrahim
& Nurul Dalila, 2008). The warm and moist tropical climate of Malaysia encourages
the growth and evolution of the animals in the region, especially the amphibians that
thrive in such environment. Within its 329, 847 km2 of land, Malaysia is currently
home to 233 species of amphibians, with at least 63 endemic species found exclusively
in the country, and more waiting to be discovered in its forest (IUCN, 2008). Just
within the last five years, scientists have discovered 7 new species and 1 new genus in
Peninsular Malaysia, while 11 species were discovered in Borneo. Yet, there are still
many amphibians to be discovered, and also those look-alikes that were wrongly
grouped as a single species pending to be re-described as new species. As of year 2009,
Chan et al. (2010) listed as many as 107 species of amphibians in Peninsular Malaysia.
Frogs and toads are integral parts of the food web in the ecosystem. As tadpoles,
they graze on a variety of algae and detritus gleaned from the water column or found
on the bottom substrates. On the other hand, they become food for predators, such as
insects and fish. As adults, frogs and toads eat insects and other small invertebrates
and vertebrates, and, in turn, are preyed upon by snakes, birds, humans and a host of
other predators (Ibrahim, 2004).
Anderson et al. (1999) mentioned that the knowledge of diet and feeding
ecology is crucial to the understanding of life histories, population fluctuations, and
1
the impact of habitat modification on anuran populations. The diet composition of an
anuran is influenced by prey size, mobility, availability, palatability and nutritional
value, and also by the frog’s morphology and behaviour, which are subjected to
evolutionary processes, and the anuran’s previous experience (Santos et al., 2003).
Amphibians are carnivores, and, are opportunistic feeders that target moving prey
crossing their line of vision, although the size of their chosen prey is limited by their
gape width (Toft, 1981). They are known to prey on a wide spectrum of invertebrates
including annelids, arachnids, centipedes, millipedes, molluscs and especially insects
(Anderson et al., 1999; Dietl et al., 2009; Hirai & Matsui, 2000a, 2000b, 2000c, 2002;
Ibrahim & Nurul Dalila, 2008; Santos et al., 2004; Soléet al., 2009).
Considering the vast variety of anurans available in Malaysia, there are
relatively few publications on the diet of anurans (Berry & Bullock, 1962; Berry, 1965,
1966, 1970; Elliott & Karunakaran, 1974; Erftemeijer & Boeadi, 1991; Ibrahim &
Nurul Dalila, 2008; Ibrahim & Sofrina, 2001; Ibrahim, 2004; Kueh et al., 2010; Yap
& Ibrahim, 2012), as most of the studies focused on refining the inventory (Berry,
1975; Chan et al., 2010; J. L. Grismer et al., 2004; Grismer et al., 2006; Grismer et al.,
2010; Ibrahim at al., 2008; Inger & Tan, 1996; Norhayati et al., 2005; Shahriza et al.,
2011; Shahriza, Ibrahim, & Shahrul Anuar, 2011), breeding (Berry, 1964; Church,
1960; Inger & Bacon, 1968; Inger & Greenberg, 1963), ecology (Emerson & Inger,
1992; Inger, 1969, 2003), descriptive notes and zoogeography (Berry, 1975;
Boulenger, 1912; Das, 2008; Inger & Iskandar, 2005; Inger et al., 2009; Inger &
Stuebing, 1992, 2005; Inger & Voris, 2001) of the amphibians.
Common Asian toad (Duttaphrynus melanostictus), Painted chorus frog
(Microhyla butleri), Dark-sided chorus frog (Microhyla heymonsi), Paddy rice frog
(Hylarana erythraea), and Golden tree frog (Polypedates cf. leucomystax) are the five
2
species commonly found living commensally with human, and can be found in many
disturbed areas in Malaysia. There is however a lack of studies on these species,
especially on their diet. As Breen (1974) mentioned, mankind has only thorough
studied of a handful of very common species, but of the vast majority we know little.
Our appreciation of nature is heightened when our awareness of the environment is
increased, and frogs are well-known bio-indicators of the environment. For this reason,
the aims for this study were to determine the relative abundance of these species in a
disturbed area and their diets in order to gain more insights on the animals.
1.2 Objectives
1. To determine the prey items consumed by the five anurans commonly

found in disturbed areas (Duttaphrynus melanostictus, Microhyla butleri,
Microhyla fissipes, Microhyla heymonsi, and Polypedates leucomystax) in
order to infer predation strategies.
2. To determine the correlation between the mouth width of the anurans and
volume of the prey items in order to infer predation strategy of each species.
3. To study the difference in morphometry and prey compositions of male and

female anurans.
4. To determine the niche breath and niche overlap of these anurans in order
to infer whether there is a strong or weak interspecific competition between
the five species.
3
CHAPTER 2
Literature Review
Herpetology, is the study of two distinct clades of vertebrata, the reptiles and
amphibians, known to laymen as the "creepy crawlies". The term is derived from
ancient Greek "herpeton", which carries the meaning "crawling things". Herpetology
examines the natural history, physiology, and phylogenetic of these animals and their
ecological importance at a global scale (Porter, 1972). The study on amphibian alone
is a sub-discipline of herpetology that is termed batrachology.
2.1 Amphibians in General
“Amphibia”, derived from an ancient Greek word "amphibios" meaning both
kinds of life, was first coined by Linnaeus in year 1758 for an assemblage of half
terrestrial and half aquatic vertebrates with amphibious habit. Adaptive radiation in
modern amphibians is chiefly reproductive and coping with the need of water for
breeding (Webb et al., 1981). Amphibians are animals that live alternately on land and
in water. These animals in general have a soft, moist scaleless skin; their eggs lack a
protective shell; and they typically develop through an aquatic larval stage followed
by metamorphosis transformation into an adult that may be amphibious or wholly
aquatic. Amphibians prefer moist, humid habitat and constantly bathe in water to
maintain their moist skins and to avoid water loss (Duellman & Trueb, 1986).
Amphibia, in general, is defined as an ectothermal vertebrate with a smooth or
rough glandular skin, no scale or if scales are present, they are hidden in the skin
4
(Noble, 1954). In general, taxonomist tried to classify and categorize the amphibians
according to shared features and structures, which are then further supported by the
behavioural types and evolutional relationships of the amphibians. Thus, the
classification and taxa of the amphibians helps predict the behaviour and life cycle of
unfamiliar amphibians by comparing with others under the same taxon. The class
Amphibia is divided into 3 surviving orders: Anura, Caudata, and Gymnophiona.
Caecilians are classified under the order Gymnophiona, salamanders and newts are
under the order Caudata, whereas frogs and toads are from order Anura.
Caudata has an elongated body, a long tail, and with exception of Sirenidae
family, two pairs of limbs that are of the same size. Like all amphibians, caudates are
restricted to wet places. Among Caudata, there are species that gave up their
amphibious lifestyle. They are either totally aquatic or highly terrestrial in their adult
stage. Aquatic caudates are commonly called newts, and live in streams, lakes, marshes,
and even in subterranean waters. Terrestrial caudates, the salamanders, may be found
burrowing under earth, hiding between stones, holing up in caves or in trees. For
example, Dendrotriton sp., a genus of plethodontid salamanders that is also called
bromeliad salamanders, live and reproduce in pineapple plants (family, Bromeliaceae)
(Wake, 1987). There is a unique phenomenon among caudates, where the amphibian
reaches sexual maturity in its aquatic larval stage. This phenomenon is known as
paedogenesis, and can be seen in the axolotl (Ambystoma mexicanum) (Webb et al.,
1981).
Gymnophiona, or previously known as the order Apoda, are an obscure order
of legless amphibians, known as caecilians. Caecilians can be found in tropical forests,
burrowed in soft damp earth. Morphologically, caecilians resemble large earthworms,
with cylindrical body lined with minute dermal scales, no limbs, and no tail (Webb et
5
al., 1981). Caecilians also have a unique tentacle beneath its functionless eye,
presumably for sensory to compensate the loss of sight.
The order Anura, with the word Anura derived from ancient Greek meaning
"without tail", is a diverse group of carnivorous frogs and toads. In a narrow sense,
members of the family Bufonidae are considered as toads (Duellman & Trueb, 1986).
Different species of anurans adapt to living in different habitat via intrinsic changes
rather than extrinsic, by altering their physiology, behaviour, and reproductive
methods (Webb et al., 1981). Anurans are ectothermic, tetrapod vertebrates with a
generally smooth, moist and glandular skin (Noble, 1954). The skin of anuran is very
permeable, thus they are often semi-aquatic and inhabit humid areas. Anurans are most
conspicuous by the males' advertisement calls, which can be heard during the night or
some times, even during the day.
6
2.2 Habitat and Distribution
Amphibians can be found all over the world, with the exception of Antarctica
where the weather is extremely cold (Noble, 1954). They inhabit any type of habitat
as long as there is enough moisture readily available. Globally, the distribution of
anurans is more concentrated near the equator, thus there are higher species diversity
and more endemic species in the tropical regions (Inger, 2005).
The classification of anurans is affected in some degree by the habitat of the
anurans. For example, all anurans from the family Megophryidae are known leaf litter
frogs, while those under family Rhacophoridae are all tree frogs. Due to its permeable
skin and a life cycle that requires water to breed, anurans are bounded to areas with
presence of water. However, anurans are fresh water species. Anurans cannot survive
in salt water due to their inability to concentrate urine. Only a few species are able to
tolerate the salinity of brackish water, such as Fejervarya cancrivora that are found
living in mangrove areas of Malaysia (Inger & Stuebing, 2005).
Blessed with frequent rain and steady tropical climate, anurans are omnipresent
in Malaysia. The majority of the anurans are found in and around the forest area, where
humidity is high and the climate change is modest. Though nowadays, due to the
expansion of human activities into the habitat of anurans, more and more anurans are
becoming human commensal (Norhayati et al., 2005). The amphibian habitats that are
in frequent contacts with human over a long period (disturbed areas) show fewer
species and those where human presences are lesser or none (undisturbed areas) show
higher number of species richness (Mohamed Ali Abdu Assalam, 2000). Though for
the fewer species that live in man-altered environment, they thrive in numbers. The
relationship between the diversity and abundance of amphibians, and the density of
human population is complex (Porter, 1972).
7
2.3 Anurans in General
Anurans undergo metamorphosis and the life cycle comprises four main stages:
egg, tadpole, froglet and adult. Anurans’ egg is shell-less, the embryo is protected in
highly permeable mucoid capsule, and thus must develop in moist situations
(Duellman & Trueb, 1986). Eggs hatch into tailed larvae called tadpoles that grow
quickly, and then metamorphose into small froglets. As the froglets grow, the tail
shrinks until it’s absent in the adult. There is no distinct neck in the froglet and adult
stages, as the head of an anuran is externally continuous with the body.
An egg consists of the vitellus (the embryo) encompassed by several gelatinous
layers. The number of eggs laid in a single brood differs from species to species. An
amphibian may lays its eggs in forms of single egg that sink to the bottom of the
breeding pond or are attached to submerged vegetation, in small packet of eggs, in
strings or files wrapped around emergent vegetation (e.g. Duttaphrynus melanostictus),
in a surface film that floats on the water surface (e.g. Kaloula pulchra), in clusters that
are usually attached to emergent aquatic vegetation, or in a foam nest attached to
overhanging vegetation (e.g. Rhacophorus nigropalmatus) (Duellman & Trueb, 1986;
Haas et al., 2013; Porter, 1972).
A tadpole has a body and a tail. Its keratinous beaks and denticles serve as
larval mouthparts, which differentiate it from a typical fish. There is also a single
median spiracle in the larva that is characteristic of Orton's Type 3 tadpole. The tail of
a tadpole consists of the centre axis of muscle segments, and crests that are the upper
and lower fins (Duellman & Trueb, 1986).
8
Adult anurans have elongated tarsal bones, and complex pectoral girdle. There
is an absence of a prefrontal bone. They have 5 to 9 presacral vertebrae, so that the
trunk is shortened for jumps. Hind limbs are considerably larger and more muscular
than fore limbs, as they are used for jumping and swimming. The radius and ulna of
the arm are fused, and same goes with tibia and fibula of the leg. Their ankle bones,
tibiale and fibulare, are both elongated. Most anurans are oviparous, some species are
ovoviviparous and others viviparous, but all fertilisations happen externally (Md
Hanapi & Ibrahim, 1986; Webb et al., 1981).
Matured amphibians show secondary sexual characteristics. In general, the
more active males are inclined to darker dorsal colours compared to the females. Males
also tend to be more self-coloured than the females, which may be more spotted, such
as the brown tree toad (Pedostibes hosii) (Haas et al., 2013). On the other hand, females
tend to be larger in size, with the exception of few species. Other examples of sexual
dimorphisms include the pronounced differences in throat colouration in bufonids
(whereby males have marked yellow colouration and females have none), enlarged
tympana in males, enlarged thumb or presence of pad in males, skin or body
projections in males, and presence of throat sac in males (Katsikaros & Shine, 1997;
Webb et al., 1981).
Tropical anurans have acyclic breeding patterns and many species breed all
year round, as studies found no evidence of seasonal trends in the reproductive
activities of several rainforest anurans (Berry, 1964; Inger & Bacon, 1968; Inger &
Greenberg, 1963; Inger & Voris, 1993). This is attributed to the constant climate of
tropics. However, the anurans breeding periodicity is affected less by the variation in
precipitation and more on the presence of water in their local environment (Alcala,
1962; Ibrahim, 2004; Inger & Voris, 1993). As their breeding rhythms are direct
9
adaptations to local extrinsic factors, rainfall variation may cause immediate shift in
reproductive pattern, i.e. Duttaphrynus melanostictus’s peak spawning occurs with the
influx of rainwater after an extended period of dry weather (Church, 1960).
Gross & Shine (1981) and Crump (1996) recognised six modes of amphibian
parental care: egg attendance, egg transport, tadpole attendance, tadpole transport,
tadpole feeding, and internal gestation in the oviduct. Parental care in amphibians
increases survivorship of the offspring, and is most commonly found in geographical
areas of correspondingly high species richness. Famous examples of amphibians that
practice parental care include mid-wife toad (Alytes obstetricans), Surinam toad (Pipa
pipa), Darwin's frog (Rhinoderma darwinii) and more.
Generally, anurans do not possess unique features, and each species is defined
by a combination of characteristics. As of current, Frost (2013) listed as many as 7044
species of amphibians known worldwide. These are 6200 species of Anura (88%), 652
species of Caudata (9%) and 192 species of Gymnophiona (3%). IUCN, Conservation
International, & NatureServe (2008) assessment (also known as IUCN Red List) of
6260 species of amphibian determined that as many as 2030 species or nearly one-
third of the species (32.4%) is globally threatened or extinct. About 1533 species
(24.5%) cannot be assessed due to the lack of data, though among these species may
contain a significant proportion of threatened species. IUCN (2008) also assesses that
the threat level for Anura was average, 31.6% (1749 species) currently threatened or
extinct. On the other hand, about half of the Caudata species (49.8%) are threatened or
extinct. The seemingly low threat of Gymnophiona (3.4%) however is due to the
majority of the species do not have sufficient data for assessment. Family-wise,
Sooglossidae Noble, 1931 and Calyptocephalellidae Reig, 1960 are most vulnerable,
as all of the species under both families are either vulnerable or endangered.
10
Malaysia, with its west peninsular joined to the Southeast Asia mainland, and
Sabah and Sarawak from Borneo Island, is home to 8 genera and 233 species of
amphibians (Chan et al., 2010; Haas et al., 2013; Norhayati et al., 2009). Over 90% of
them are anurans. In Peninsular Malaysia itself, Chan et al. (2010) listed a total of 105
anuran species from six families, consisting of 18 species from Dicroglossidae, 10
species from Megophryidae, 18 species from Bufonidae, 20 species from
Microhylidae, 18 species from Ranidae and 21 species from Rhacophoridae.
Dicroglossidae Anderson, 1871 has previously been grouped together as
Ranidae until recent molecular works suggested otherwise. This family is distributed
in Europe, Northwest Africa and throughout Asia. There are only 181 species of frogs
from this ancient clade (Frost, 2013). There are very few external features that unite
the species within this family, though they generally resemble the true frog of ranids.
All species of this family are ground-dwelling and are usually found close to bodies of
water. Malaysia is currently home to 4 genera and 25 species of dicroglossids (Chan
et al., 2010; Haas et al., 2013). Malaysia’s dicroglossid includes two of the country’s
largest frog species, peat swamp frog (Limnonectes malesianus) and Blyth’s river frog
(Limnonectes blythii).
The Asian toad of Megophryidae Bonaparte, 1850 are a family of South Asian
frogs spread from Pakistan and India to the Southeast Asian countries such as Malaysia,
Philippines and Indonesia. Frost (2013) listed 10 genera and 171 species from this
family. They are the most ecologically and morphologically diverse group of non-
neobatrachian frogs. In Malaysia, Megophryidae family consists of 6 genera and 29
species. Megophryids are small to medium sized frogs, with the snout-vent length
ranging from 20 mm to 125 mm (Norhayati et al., 2005). They are nocturnal species
that burrow in the day (Breen, 1974). Most Megophryids are also poor jumpers, and
11
prefer to crawl along, even when disturbed. Another common feature of this family is
the possession of a flat tongue and a spade-like hind foot, which gives rise to the name
“spadefoot toad” (Breen, 1974).
The colouration of Megophryids is typically dull and earth tone. Certain
species of Megophryids possess skin projections that resembled dead leaves, for
example, horned frog (Megophrys nasuta) has dermal projections all over its body
ridges, so that when among the forest litter, it can easily mimicked one of the fallen
leaves (Duellman & Trueb, 1986). Megophryids in Malaysia are experts in
camouflaging themselves among ground litters, which earns them the name “leaf-litter
frogs” (Berry, 1975).
Bufonidae Gray, 1825 or the true toads made up the third largest family of the
anurans with 571 species scattered all over the world (Frost, 2013). Presently,
approximately 44.1% of the total species in this family are considered to be either
threatened or extinct and 6 species has already lost forever to mankind (IUCN, 2008).
Being the second largest family in Malaysia, Bufonids face the same grim situation
when 58% of the total 42 species are threatened (Norhayati et al., 2005). The six genera
of Malaysian Bufonids made up of the genus Ansonia, with 19 species, followed by
Pelophryne (8 species), Ingerophrynus (5 species), Pedostibes (3 species), Phrynoidis
(2 species), and one species each under these genera: Bombina, Duttaphrynus,
Leptophryne, Pseudobufo and Sabahphrynus.
Bufonids are found throughout temperate and tropical regions, with the
exception of Australopapua region, Madagascar and Oceania. The only toad found east
of the Wallace’s Line is cane toad (Rhinella marina, previously known as Bufo
marinus) that is introduced in Australia along with the sugar cane from South America
12
(Frost, 2013). All bufonids are very much alike in over-all appearance. Compared to
frogs, toads are typically dull in colouration, have dry warty skins, and lack true teeth
(Breen, 1974).
Microhylidae Günther, 1858, as the name indicates, comprises of a family of
small-size frogs, though some among them reach medium-size. The snout-vent length
of these microhylids range from 7 mm to 100 mm. Nevertheless, the most
distinguishable feature that defines this family is their narrow mouths. Therefore, they
are collectively known as narrow-mouth frogs (Frost, 2013; Norhayati et al., 2005).
Microhylids have rounded bodies, and some species namely the bullfrogs will further
puff up their size when under threat, as seen on Kaloula pulchra. Despite their
relatively small size, microhylids make the loudest calls that preceded their presence
(Haas et al., 2013; Norhayati et al., 2005).
Since this is a family of tiny frog, it is no wonder that the world’s smallest
vertebrate is categorized under its wing. Formally described at year 2012,
Paedophryne amanuensis from New Guinea is the smallest amphibian measured at 7
mm long. The tiny species of Paedophryne genus from the eastern forests of Papua
New Guinea were identified quite recently, as they are hard to spot, camouflaging
among forest floor leaf-litters, and have calls that resembled insects (Black, 2012).
A relatively young clade of anuran family in the term of phylogenetic evolution,
Microhylidae has over 519 species distributed worldwide, with the exception of the
Antarctic continent (Frost, 2013). Malaysia is home to 40 species of microhylids under
9 different genera. Microhylids are separated into burrowing group and arboreal group.
Burrowing microhylids usually emerge after heavy rains, usually to breed (Norhayati
13
et al., 2005). Arboreal microhylids take shelter in tree holes, or hiding underneath
leaves of epiphytes.
Frogs from the family of Ranidae Rafinesque, 1814 are considered the “true
frogs”. The layman generalization of the forms and functions of frog comes from
ranids. Ranidae is the world fifth largest anuran’s family comprising 355 species (Frost,
2013). Ranids are Old-World frogs, its distribution world-wide with the exception of
temperate South America, West Indies, most of Australia, and Oceanic islands. In
Australia only a single species, Hylarana daemeli, is recorded from northern
Queensland and north-east Northern Territory of Australia. Ranidae in Malaysia
consisting of 9 genera; 38 species (Chan et al., 2010; Haas et al., 2013). Ranid’s
pectoral girdle is firmisternal, with the sternum fused to the pectoral arch and the
epicoracoidal cartilages fused (Duellman & Trueb, 1986). Appearance-wise, its skin
is smooth and moist, there is a dorso-lateral skin fold from behind the eye to the hind
limb and maxillary teeth are present. Ranids are riparian and cosmopolitan, found in
in forests, swamps, paddy fields, lakes, rivers, and even in garden ponds.
Ranids can be as small as 20 mm to 300 mm in snout-vent length. The largest
frog in the world – goliath frog (Conraua goliath) endemic to Cameroon and Equitorial
Guinea, comes from the family Ranidae (Amiet, 2004). This family also housed
Malaysia’s largest frog – Blyth’s giant frog (Limnonectes blythii), which is also an
economically important species in the country. Tanah Rata wart frog (Limnonectes
nitidus) is the only endangered ranids in Malaysia (Leong & Yaakob, 2004).
If the ranids are “true frogs”, Rhacophoridae Hoffman, 1932 are a family of
Old World tree frogs that occurs in Asia and Africa. Two subfamilies are recognized
under Rhacophoridae: Buergeriinae, and Rhacophorinae (Frost, 2013). Due to the
14
arboreal nature of the frogs in this family, they are commonly known as shrub frogs,
bush frogs and tree frogs, and most spectacularly, the gliding frogs in this family are
also called flying frogs. In Malaysia, Rhacophoridae is the largest family comprising
52 species, and 6 genera.
Rhacophorids’ size range from 15 mm to 120 mm. Morphologically, tree frogs
are fully adapted to living in the canopy. They seldom leave the protection of the
foliage unless to mate and lay eggs at the nearest streams. As such, rhacophorids have
enlarged toe disks to facilitate climbing and to hold onto tree branches and leaves; full
webbings between the fore fingers and hind toes for gliding through the air while they
leap from one tree to another. They also possess flattened bodies, no ribs, broad flat
skulls, dentate upper jaw, and cartilaginous intercalary elements between the terminal
and penultimate phalanges (Norhayati et al., 2009).
2.4 Classification of Frog and Toad
While there are no true clear guide to the classification of frogs and toads, there
are a few external features or characteristics that are used to distinguish between a frog
and a toad (Fig. 2.1). In a broad sense, toads are those anurans from the family
Bufonidae, also called bufonids.
In general, toads have dry, warty skin and possess elevated ridges (cranial
crests) between and at the back of the eyes. In addition, a prominent, raised, glandular
area (parotoid gland) behind the eye is found on toads (Duellman & Trueb, 1986).
Toad tends to have rounder, blunter snout compared to frog. Since toads generally
15
crawl, and only make short distance jump, they have stout but shorter hind legs. With
the exception of some tree toads, toads commonly have pointy fingers with no toe
disks. Webbings between the toes are usually absent in toads.
On the contrary, true frogs have moist, smooth skin with or without a ridge
(dorsolateral fold) extending from the ear drum (tympanum) along the side of the back
to the hip or groin area (Berry, 1975). Most frogs have longer pointy snout. They also
have long slim but muscular hind limbs for long leaps. Almost all frogs have toe disks
on their hind legs, some more prominent than others, though toe disks may or may not
be absent on the fore fingers (Duellman & Trueb, 1986). Due to their liking of wet
habitat, frogs are likely to have webbings between their toes to help them wade through
water.
Figure 2.1 External characteristics of frogs and toads.
16
2.5 Descriptions of Specimens
2.5.1 Duttaphrynus melanostictus Schneider, 1799
Classified under family Bufonidae, D. melanostictus used to be named Bufo
melanostictus, Bufo tienhoensis, and Ansonia kamblei (Frost, 2013). It is commonly
called common Sunda toad, Asian common toad, Asian toad, Javanese toad, or black-
spectacled toad (Van Dijk, Iskandar, Lau, et al., 2004). Local calls it katak puru biasa,
or simply katak puru. The average snout-to-vent length (SVL) of an adult male ranges
from 57 mm to 83 mm, and female ranges from 65 mm to 85 mm (Norhayati et al.,
2009).
As with most toads, this species has a stocky body, with dark elevated
supraorbital and supratympanic bony ridges on its head, but no parietal ridges
(Norhayati et al., 2005). Duttaphrynus melanostictus can be easily differentiated from
other toads with its distinctly large and elongated oval-shaped parotoid glands on the
back of its neck (Fig. 3.3). The parotoid glands are usually covered with black spots.
Its head width is longer than head length. Its snout is obtusely pointed. It has distinct
tympanum, which is about half the size of its eye. The finger and toe tips are blunt.
There is presence of supernumerary metacarpal tubercles on fore limb and two
metatarsal tubercles on hind limbs, and also conspicuous subarticular tubercles on its
limbs. Hind limbs are more than half webbed between the toes, with third and fifth
toes usually with one phalanx free of web, and fourth toe with three phalanges free of
web (Berry, 1975). The dorsal skin is rough and overall very warty. Its colour varies
from greyish to reddish-brown or yellowish. The ventral is usually pale brown or pale
yellow in colour. Male D. melanostictus has distinct yellow-tinted chin.
17
This species spread widely from Bangladesh, Southern China to South East
Asia. Duttaphrynus melanostictus is ubiquitous in disturbed areas all over Malaysia.
It is a well-known human commensal species, found in disturbed open areas, villages,
towns and rarely in primary forest. Duttaphrynus melanostictus is mainly a lowland
disturbed areas species, hard to be found in a closed forest. Hence, it’s a good indicator
of habitat disturbance. It has also been recorded from sea level up to 1,800 m a.s.l.
Listed as least concern (LC) in the IUCN Red List of Threatened Species, this species
global population is speculated to be increasing (Van Dijk et al., 2004).
Typically found hiding under ground cover or hiding under low foliage, adults
D. melanostictus are terrestrial and only gather at nearby freshwater for breeding. This
species breeds in still water bodies, such as permanent or temporary pond and pool, or
slow-moving rivers. The eggs are laid in strings that are strewn across the bottom of
the water or the aquatic vegetation under water. In a tropical country, such as Malaysia,
D. melanostictus breeds all year round as long as there is ample standing water nearby
(Berry, 1964).
2.5.2 Microhyla butleri Boulenger, 1900
Commonly called Butler's rice frog, painted chorus frog, tubercled pygmy frog,
or katak padi Butler in local tongue, it is a tiny frog under the family Microhylidae.
Male's SVL ranges from 21 mm to 23 mm, whereas female's SVL ranges from 23 mm
to 26 mm (Norhayati et al., 2009).
18
It has a rounded snout, and no visible tympanum. Its finger tips are dilated into
small but well-developed disks, with its first finger much shorter than the second finger.
The tips of its toes are like those of fingers, disks with circum-marginal groove and
median notch, and webbed at the base. The hind limbs subarticular tubercles are small.
There are two very small metatarsal tubercles (Berry, 1975).
Its skin maybe smooth or some time speckled with smooth warts. The dorsal is
greyish with symmetrical dark brown, wavy markings which extended down onto its
sides, forming bars on the hind limbs (Fig. 3.3). Markings sometimes accompanied by
oblique white streak. The insertions are speckled with several granules or glandular
tubercles (Norhayati et al., 2005). Its sides and limbs is pale reddish in colour, with or
without small scarlet spots on the sides. Occasionally, specimens are found with white
dot on the end of the snout. The ventral is whitish, with throat and breast speckled with
brown (Berry, 1975).
This is known to be found in China, Hong Kong, Taiwan, Vietnam, Myanmar,
Thailand, Malaysia and Singapore. This species inhabits lowland forests, freshwater
wetlands, cultivated areas and grasslands where they are usually found on the ground
among low vegetation, such as bushes, shrubs and grasses. It is found up to 1,000 m
a.s.l. (Norhayati et al., 2005). Microhyla butleri has a very loud and distinct call that
this species’ presence is always preceded by the choruses of their calls.
While this species is abundant in Southeast Asian countries, its distribution is
deemed rare in Taiwan and fragmented in China. It is considered a Class II protected
species in Taiwan. Contradictory to its ever presence in local paddy fields, no
population of M. butleri was ever found in the paddy field in Taiwan, presumably due
to the use of harming chemical pesticides and fertilizers. Nonetheless, it is still listed
19
as least concern (LC) in the IUCN Red List of Threatened Species justified by the
species wide distribution, its ability to tolerate a broad range of habitat, and the
unlikelihood of the presumably large population to decline in the near future (Van Dijk
et al., 2009).
M. butleri is a terrestrial riparian species. Due to its small size and the inability
to hold a large amount of water in its body, M. butleri does not stray far from moisture.
This species breeds in relatively permanent standing water, for example, ponds, pools,
marshes, and paddy field. It has no reproductive cycle in relation to the climate (Berry,
1964).
2.5.3 Microhyla fissipes Boulenger, 1884
Also named Microhyla eremita, this is another small frog under family
Microhylidae (Frost, 2013). This species does not actually have its own common name
due to the fact that it is easily mistaken as ornate narrow-mouthed frog (Microhyla
ornata) from South Asian region. SVL of males range from 22 mm to 27 mm, while
females range from 25 mm to 28 mm.
Morphologically, this species is similar to M. butleri, with little difference.
Appearance-wise, M. fissipes is indistinguishable from M. ornata. It has smooth skin.
Its dorsal back is reddish or greyish olive coloured, with a large dark brown marking
on the centre, beginning between the eyes and widening as it extends to the hind part
of the body. On each side of this marking, wavy dusky lines are often present (Fig.
3.3). There is a dark band along the side of the head and body. Its hind limbs maybe
20
with or without dark cross-bars. The ventral throat and chest are generally greyish
brown, dotted with white, whereas the remainder of the lower ventral surface whitish,
and unspotted (Norhayati et al., 2009).
Prior to the study by Matsui et al. (2005), there is confusion between M. fissipes
and M. ornata, resulted in many scientists wrongly identified M. fissipes in the
Southeast Asia region as M. ornata. However, the boundary between these two species
is still not clear, and it has been arbitrarily set at the border of Myanmar until there is
further clarification on the matter.
Known to be omnipresent all over mainland Southeast Asia, with only a record
from a single locality in the north of Sumatra, Indonesia, this species inhabits lowland
forests, disturbed areas where they are usually found on the ground or low vegetation,
and around paddy fields. Sub-fossorial in habit, it can also be spotted hiding among
forest floor leaf-litter. There is report that M. fissipes was found up to 2,000 m a.s.l.
Like M. butleri, M. fissipes is considered least concern (LC) by IUCN Red List of
Threatened Species in view of its expanded distributions, the sheer number of
populations, its high adaptation to various habitats, and the improbability of sudden
decline (Lau et al., 2008).
M. fissipes is a species nocturnal in nature, only active diurnally during rainy
season for breeding (Lau et al., 2008). While there is no known study on M. fissipes
breeding rhythm, it is believed that it has a noncyclic pattern similar to its closest
cousin Microhyla heymonsi and M. butleri. It lays clutches of egg mass at the surface
of both permanent and temporary still water bodies.
21
2.5.4 Microhyla heymonsi Vogt, 1911
Another small frog under family Microhylidae, it is commonly called dark-
sided chorus frog, Taiwan rice frog, arcuate-spotted pygmy frog, or locally, katak
bising. SVL of adult males range from 16 mm to 21 mm, while SVL of adult females
range from 22 mm to 26 mm (Berry, 1975).
It has a slight glandular fold from posterior corner of the eye to its fore limb.
Morphologically similar to M. butleri, M. heymonsi is the easiest to identify microhylid.
It has smooth dorsal and ventral skins. Dorsally pinkish or greyish in colour with a
black lateral band extending from the snout tip to the vent, and entirely covering the
sides of the head (Fig. 3.3). This band is sharply defined above but merging gradually
into the colour of the bellow beneath. A fine white vertebral line form from its snout
to vent. There is a small characteristic black mark on each side of the line on the middle
of the back. There may be an additional pair of similar but smaller marks between its
shoulders. Its ventral skin colour is dirty white (Berry, 1975).
A widespread species found in China and most of South East Asia. This
cosmopolitan species can usually be found alongside M. fissipes as they share the same
microhabitat. Microhyla heymonsi inhabits mainly disturbed areas, such as riverbanks,
gardens, paddy fields, grasslands, savannah forest and any patch of secondary
vegetation. It is known to live up until an altitude of 945m a.s.l. (Imbun et al., 2010).
Due to its widespread distribution, large global population, high tolerance to different
habitats, and unlikely drop in numbers, IUCN Red List of Threatened Species places
M. heymonsi as least concern (LC). Nevertheless, it is a Class II protected species in
Taiwan (Van Dijk et al., 2004).
22
One of the noisiest frogs around (hence the local name “katak bising”, which
can be literally translated to “noisy frog”), this frog’s loud calls can be heard all year
round. This species reproductive pattern is acyclic and independent of the climate
(Berry, 1964). It breeds in temporary rain puddles, ditches, marches, paddy fields,
small streams and also slow-flowing rivers.
2.5.5 Polypedates leucomystax Gravenhorst, 1829
Classified under family Rhacophoridae, its vernacular names include four-
lined tree frog (as some individuals have four longitudinal dorsal stripes, Fig. 3.3),
common tree frog, Java whipping frog, brown tree frog, Malayan house frog, Malayan
tree frog, white-lipped tree frog, bamboo tree frog, house tree frog, jar tree frog, and
stripe tree frog. This species is considered a species complex because the exact
demarcation between close species is still cryptic. Therefore, myriad nomenclature
actually point to this species, i.e. Hyla leucomystax, Hyla sexvirgata, Hyla
quadrilineata, Hyla leucopogon, Hyla quadrivirgata, Polypedates rugosus,
Polypedates quadrilineatus, Limnodytes celebensis, Rhacophorus maculatus var.
quadrilineata, Hylorana longipes, Rhacophorus leucomystax, Rhacophorus
leucomystax leucomystax, Rhacophorus leucomystax quadrilineatus, Rhacophorus
leucomystax sexvirgata, Rhacophorus leucomystax quadrilineata, Rhacophorus
maculatus leucomystax, Rhacophorus maculatus himalayensis, Hyla wirzi,
Rhacophorus (Polypedates) leucomystax, Rhacophorus (Polypedates) quadrilineatus,
Rhacophorus kampeni, Rhacophorus (Rhacophorus) kampeni, Rhacophorus
(Rhacophorus) leucomystax, Rhacophorus (Rhacophorus) himalayanus, Rhacophorus
23
(Rhacophorus) leucomystax leucomystax, Rhacophorus (Rhacophorus) wirzi, and
Rhacophorus leucomystax quadrilineatus (Frost, 2013).
P. leucomystax can grow up to 80 mm in snout-vent length. Its head length is
longer than its head width. With a pointed round snout, it has distinct round tympanum
that is about ¾ of its eye diameter. The tips of its fingers dilated into disks with circum-
marginal grooves, with the widest disks about 2/3 of its tympanum diameter. These
grooves provide suction at the finger tips, which in turn giving P. leucomystax the
ability to climb on any vertical surface (Inger & Stuebing, 2005). The webbings
between its first two fingers do not reach the subarticular tubercles, and less developed
in its outer fingers. Its toe tip disks is smaller than those of its fingers, but the webbings
usually reach the bases of disks on outer edge of first three toes and on inner edge of
fifth toe, and the fourth toe has two phalanges free of broad web on outer edge (Berry,
1975).
Its skin smooth dorsally and ventrally, with the exception of adult male that
has coarse granules on its throat. A broad, smooth-edged flap of skins is formed along
the forearm and tarsus expanding along outer edges of its fourth finger and fifth toe.
There is a broad round flap at the heel. Supratympanic fold is also present. Polypedates
leucomystax dorsal colour is highly variable, from brown, light tan or grey, with or
without dark interorbital bar, dark cruciform mark or dark, dorsal spots. Its dorsum is
usually spotted irregularly with brown, black, blue, yellow or orange. There are dark
cross-bars on its hind limbs. The ventral surface is usually whitish or pale yellowish
in (Norhayati et al., 2009).
Though its geographical distribution is still provisional, there were records of
P. leucomystax found in Nepal, China, India and throughout Southeast Asia. So far, it
24
is known to be introduced into Japan and Papua New Guinea. This species inhabits
lowland primary forests and disturbed areas. As it is very adaptable and commensal, it
thrives in all human habitations such as cultivated agricultural fields, ditches, artificial
ponds and lakes, gardens, even in peoples’ houses. It occurs at elevations up to 1500
m a.s.l. (Diesmos et al., 2004).
P. leucomystax is a species of frog that is able to tolerate environmental
changes (Bickford et al., 2010). Hence, it is not subject to any degree of disturbance
that threatens its species survival. In fact, P. leucomystax appears to depend on human
activities to create suitable habitats. The high tolerance and human adaptation put P.
leucomystax as a least concern (LC) species in IUCN Red List of Threatened Species
(Diesmos et al., 2004). Occasionally, P. leucomystax can be found in the international
pet trade but at levels that do not currently pose a threat to the species survival.
P. leucomystax often perches on leaves and branches 1-3 m above the ground,
usually in the vicinity of water. This tree frog and its mass of foam nest can be found
inside houses, on walls, in irrigation ditches and drainage canals, and some time, even
on parked vehicles. This species lacks any type of breeding cycle in relation to the
climate (Berry, 1964).
25
2.6 Digestive System
After metamorphosis, the anurans’ morphological transformation changes an
anuran from an herbivorous tadpole to a carnivore. As with any other higher terrestrial
vertebrates, the digestive tract of an anuran starts with its mouth, with a tongue for aid
in seizing food, short oesophagus, stomach, intestines, and ends at the cloaca (Fig. 2.5).
The tongue of an amphibian is formed by the addition of a glandular fold anterior and
lateral to the piscine tongue rudiment. Most amphibians have mucous glands in their
mouth, which releases a sticky secretion to the tongue providing more adhesive feature.
Furthermore, the amphibian’s tongue is attached to the front angle of the jaw by
resistant tissue and is capable of projection, when the frog flaps the posterior part of
the tongue over and beyond the anterior. This gives the tongue the shape of a
mushroom, or boletoid tongue, when projected (Noble, 1954).
Most amphibians have true teeth, which are teeth with a hard layer of enamel
covering the softer dentine and central pulp cavity, The teeth of amphibians are simple,
cone-shaped and only located on the upper jaw. The main function of the teeth is not
to chew, but to provide a firm grip on preys (Md Hanapi & Ibrahim, 1986). The
oesophagus of the amphibian is very short, separated from the mouth cavity by a fold
and is lined with cilia to help in sweeping the food particles into the stomach. Pepsin-
secreting oesophagus glands can be found in most modern amphibians (Goin & Goin,
1971).
The stomach of an amphibian usually lies to the right of the midline with a
slight curve to the right. A full stomach sometimes caused the right side of the frog to
bulge. The stomach has a cardiac end leading from the oesophagus and a short, narrow,
pyloric end leading into the intestines (Goin & Goin, 1971). The stomach also serves
26
as food storage, since frog feed irregularly and many frogs are able to expand their
stomach enormously when food is taken in large amounts (Noble, 1954). The intestine
of the frog is a tube with almost uniform width, widens at the posterior end to form the
large intestine. In some frogs, the small intestine and large intestine are also
differentiated by a valve or ring fold that separated both the intestines from one another.
Figure 2.2 The digestive system of a frog. (modified from Md Hanapi &
Ibrahim, 1986)
27
An adult frog’s diet consists of protein rich insects or other invertebrate prey
(Noble, 1954). Digestion of an amphibian begins in the stomach with the secretion of
pepsin and hydrochloric acid that breaks down the protein to smaller molecular weight,
and is continued in the intestine whereby more enzymes are secreted (Reeder, 1964).
The digestive process of an amphibian is affected by the environmental temperature,
as the optimum temperature of the frog pepsin is 40°C, and the body temperature of a
frog is directly affected by its environment (Noble, 1954).
The products of the digestion are absorbed by the walls of the intestine. The
much needed nutrients are gathered up by the mesenteric veins and then distributed to
the body tissues. Excess energy that is not in use is carried to the liver to be stored as
fat (Reeder, 1964). Amphibians are known to be able to survive long fasts. Anurans
are ectotherm, thus with their low metabolic rate is expected to go longer without food
than warm-blooded animals. However, their ability to live with only their own tissues
for months is remarkable for such active vertebrates.
The balance between consumption and metabolic rates has a profound effect
on an anuran’s growth and development. The rates of consumption, digestion,
assimilation and metabolic rates of anurans generally increase with increased
temperature, and feeding increases to an optimum peak then declines as temperatures
become too high. Goncharov et al., (1989) studied digestibility of a large range of
species, in which the highest was larvae of the house fly (Acheta domestica), lower for
newborn mice (Mus musculus) and the cinereous cockroach (Nauphaeta cinerea), and
the lowest for A. domestica imago.
28
2.7 Diet and Feeding Ecology
In general, anurans are thought to be opportunistic feeders that prey on any
smaller organisms that crossed their line of vision (Toft, 1981). However, a few studies
on the feeding ecology of anurans had shown that some species are picky in choice of
food. Many factors affect the diet and feeding ecology of anurans. There are extrinsic
factors such as prey availability, taste of prey, presence of competition for food, and
intrinsic factors such as mouth width, and the size of the anuran.
According to Noble (1954), although anurans are omnivorous during larval
stage, all adult anurans are carnivorous. The prey items of anurans include insects,
spiders, worms, flies and also small aquatic organisms. It was proven in the laboratory
that anuran was able to learn from past experience, to choose between favourable and
unfavourable insects, as was shown by a toad trying to regurgitate a pentatomid bug
that it had previously swallowed (Noble, 1954).
Toft (1980) mentioned in her study that there are anurans that prey on ants,
termed "ant-specialist". Since ant is a relatively small prey, therefore they are
consumed in great numbers at one time. For larger arthropods, such as beetles and
crickets, the prey size are larger, therefore they take up more space in the anuran’s
stomach, and are not consumed in large number at a time. Those that are non ant-
specialist are usually generalist feeders.
The study of Hirai & Matsui (2000a) on Narrow-mouthed frog, Microhyla
ornata showed that this frog is an ant specialist. There was a high proportion of ants
found in the stomach contents than those found in the frogs’ surrounding. The study
showed that there were 77.1% of ants in number and 44.6% in volume of M. ornata
29
prey compositions. In their study, they also compared the snout-vent length (SVL) of
the male and the female toads. The SVL and mouth width (MW) of female frogs were
bigger than those of the males, and thus, the consumed prey was also relatively larger
in size.
On the other hand, another study by Hirai & Matsui (2002) on the feeding
ecology of Bufo japonicus formosus from the montane area of Kyoto, Japan showed
that adult toads preyed on arthropods from several taxa. The main prey composition
was from the order Coleoptera, which are the beetles. This was followed by ants from
the order Hymenoptera and millipedes from the class Diplopoda. There was also a
positive correlation between the size of the toad and the size of the prey consumed. It
is proven that when the size of the toad is larger, they tend to prey on larger organisms
and ignore the smaller ones.
The study of Van Sluys et al. (2006) on the microhylid frog Chiasmocleis
capixaba shows that the diet of C. capixaba was dominated by mites, ants and
collembolans. Their study shows a difference in the preferences of prey between males
and female frogs, as mites were the most frequent (93.8%) and numerous (46.7%) prey
ingested by males, whereas ants were the most frequent (90.3%) and numerous (66.4%)
prey consumed by females. However, according to the index of importance of their
study, ants were the most important prey for this species of frog.
In the tropical forest of Mindanao island, Philippines, Ates et al., (2007)
examined stomach contents of six species of anurans, Kaloula conjuncta, Philautus
acutirotris, Polypedates leucomystax, Occidozyga laevis, Fejervarya cancrivora and
Rana granducola, which indicated that ants (Hymenoptera, Formicidae) were the most
frequently occurring food item, and also the preferred food item for K. conjuncta and
30
P. leucomystax. This was followed by Coleoptera, Diptera and Orthoptera. Although
the degree of food preference differed for each food item, O. laevis was also reported
to be batracophagy in this study.
The study of Dietl et al., (2009) on the diet of Ischnocnema henselii from a
subtropical Araucaria forest through stomach flushing had successfully identified that
the prey items of the frogs comprised arthropods, such as spiders, ants, orthopterans,
collembolans and homopterans. I. henselii is considered to be a nocturnal and
opportunistic sit-and-wait predator that prefers small animals. They found that the prey
in the stomach contents reflected the habitat's leaf-litter mesofauna well, with the only
exceptions of mites, the most abundant leaf-litter inhabitants, which frogs either
avoided or ignored.
Active foragers, such as Dendrobates pictus, constantly look for prey by
actively tracking down the prey and consume a large amount of preys at one time (Toft,
1980b). Those that do not actively hunt for prey are cryptic, sit-and-wait predators.
This type of anurans wait patiently until a suitable prey crossed their line of vision,
and then pounces on the unexpected prey. However, the prey must be within a range
reachable to the anuran and the prey size must be suitable for the anurans to consume.
31
2.8 Food availability
Food availability plays a vital role in the survival of all animals, including
amphibians. The seasonal abundance and availability of food influences the diet and
feeding behaviour of amphibians living in a habitat (Duellman & Trueb, 1986). Many
scientists determined that two major factors control the metamorphic growth of
amphibians, namely the food availability and ambient temperature (Briggs & Storm,
1970; Duellman & Trueb, 1986; Dunham et al., 1989; Dunham, 1978; Wilbur, 1977a,
1977b, 1988). In the tropics, where the ambient temperature is warm and constant,
food availability is also plenty and constant. Thus, tropical amphibian growth rates are
faster and more consistent than those that inhabit the temperate zones (Brown & Alcala,
1970; Duellman & Trueb, 1986; Porter, 1972; Turner, 1962). Turner (1962) further
suggested that tropical anurans have shorter life spans and higher turnover rates than
temperate anurans.
32
2.9 Species Niches
Margalef (1963) states that as the relationship between species becomes more
specialised, the stenography and other precise relationships increase in the
communities. Niche overlap occurs when occasional restriction of certain resources or
occasional fluctuation in the physical qualities of an environment resulting in the
elimination of some niches. Heyer & Berven (1973) speculate that the niche overlap
of tropical amphibians is higher than those of temperate zone. Wissinger (1992) has
used of niche overlap and size variation within populations to predict the potential for
competition and intragulid predation between the size-structured populations in his
study.
In their study on the niche overlap and interspecific competition of
Limnonectes blythii, L. ibanorum and L. macrodon in the tropical forest of Sarawak,
Inger & Greenberg (1966) concluded that the degree of niche overlap in related species
is ecologically significant. In the study by Inger & Voris (1993), environmental
variations, particularly stream width and gradient, affect both intra- and inter-locality
species niche overlap among amphibian communities across Bornean forests. They
also gather that despite the variation of rainfall across the habitats, it did do not affect
the overlaps among or within communities.
Dash & Mahanta (1993) separate amphibians into high niche breadth scorers
and low niche breadth scorers. Habitat generalists usually possess high niche breadth
score, utilised a broad spectrum of environment gradient and thrive in all sorts of
habitats. On the contrary, low niche breadth scorers are habitat specialists, they live in
a narrow range of environmental spectrum and are restricted in their distribution. For
example, Fejervarya limnocharis, Duttaphrynus melanostictus and Euphlyctis
cyanophlyctis are all found to have high niche breadth scores and are habitat
generalists.
33
2.10 Ecological Roles of Amphibians
Amphibians are an integral part of our natural heritage and are vital to the
ecosystem. They are especially vulnerable to environmental and habitat changes due
to their high skin permeability, amphibious lifestyle of living both on land and in the
water, and metamorphosis life cycle. They also play a key role in the food web, acting
as predator to smaller organisms yet falling prey to larger vertebrate. Hence, losing of
amphibians proves to be a significant loss of biomass that will disrupt a potentially
extensive prey-predation cycle in the habitat.
Despite being found in almost all nooks and corners of the earth, most
amphibians have very narrow tolerance range for moisture and temperature that are
out of their established habitat. Amphibian’s sensitivity and vulnerability to habitat
changes serve as a good biological indicator of the habitat quality. Mohamed Ali Abdu
Assalam (2000) while studying niches of anurans according to area disturbance in
Malaysia, discovered that Duttaphrynus melanostictus, Polypedates leucomystax,
Microhyla heymonsi, and Kaloula pulchra were only found in human disturbed areas,
and could be a good indicator to human presence. In this regard, amphibians as bio-
indicators are taxonomically well-known, the biology and general life history are well
understood, the habitat and geographical range are broad, and the patterns observed in
the indicator taxon are reflected in other related taxa (Norhayati et al., 2005).
Traditionally, frogs are recognized as rain indicators (Ibrahim, 1996). Some
species are known to start croaking long before the first raindrop hit the earth. The
frogs’ ability to predict the coming of rain can be attributed to its moisture sensitivity
as its nose can detect water molecules in the air (Chapman & Chapman, 1958). Kiew
(1984) also suggested that a frog’s tympanum can sense the drop in air pressure prior
34
to the coming of a rain or storm. There is even a joke circulating around that if one’s
singing is so bad (like a frog’s croak) rain would start falling, which stems from the
Malay local saying “katak panggil hujan” (literal translation would be “frog call rain”).
Aside from that, there is also a common misconception that frogs are poisonous and
toads cause warts. While the blame is totally wrong for the toads, some species of frogs
are poisonous, such as the group of poisonous dart frogs (Dendrobates sp.) from South
America (Porter, 1972).
Amphibians are also familiar characters in folklores and folk songs. One
famous example is Kermit the Frog from a well-known children television show
Sesame Street ®. Some species of frogs are farmed for their meat, such as
Hoplobatrachus rugulosus that often found in Chinese and French cuisines. The thick
skin of toads (e.g. Phrynoidis aspera) is made into leather for purses. Many herptile
hobbyists keep amphibians as pet for companionship.
In research, amphibians are used as animal testing since the past century.
Biologist Luigi Galvani discovered the link between bioelectricity and the nervous
system by the twitching of the muscles of frog’s leg when struck by a spark. African
clawed frog (Xenopus laevis) has been used extensively as a laboratory research animal
in the field of vertebrate embryology. During the 1940's, female X. laevis were widely
used in laboratories in pregnancy assays known as “Hogben test” (Garvey, 2000).
Frogs and toads are also useful for medicinal purpose, as amphibian skin has
been the sources of biologically active compounds (Costa-Neto, 2005; Garg et al.,
2008; Gomes et al., 2007; Simmaco et al., 1998). Granular glands on amphibian skins
secrete acrid poisons or toxins, which help in providing protection from predators, so
that only those that can tolerate the toxins can prey on them, such as hognose snake
35
(Family, Colubridae) (Breen, 1974; Garg et al., 2008). Traditional Chinese medicine
“huachansu” comes from the dried venom secreted by the skin glands of toads (Bufo
bufo gargarizans), and is widely used to treat patients with liver, lung, colon and
pancreatic cancer. In modern medicine, magainin, a compound found in X. laevis, has
antibiotic, antifungal, antiparasitic, and antiviral properties, and can be
commercialised as antibiotic cream (Clarke, 1997).
Amphibians play an important role in the control of garden and agricultural
pests. Toads are particularly effective as biological control agent for insect pests, as
they tend to feed more frequently than frogs (Breen, 1974). For example, the cane toad
(Rhinella marina) has been introduced into sugar cane plantation of many countries
(Takano, 1940). Over the centuries of modern human invasions, some species have
learned to depend on and benefited by varying degrees upon symbiotic relations with
human (Porter, 1972).
Due to salt intolerance in amphibians, they cannot survive in salt water (Inger
& Voris, 2001). Not even those that thrive in coastal mangrove habitat, such as the
crab-eating frog (Fejervarya cancrivora). As a consequence, amphibians have
difficulty in crossing seas to spread from one continent to another. Therefore,
amphibians make good material to study the origin of continents. Their fossil records
help in understanding the breakup of Pangaea and filling in the blanks in evolutional
phylogenetic clades (Cannatella, 2008).
36
2.11 Amphibian Decline
The worldwide decline of amphibian species first alerted mankind with the
extinction of the celebrated gastric-brooding frogs, Rheobatrachus silus and
Rheobatrachus vitellinus in the mid-1980s. Recent years, many scientists and
herpetologists have notice the keen decline of local frogs, in numbers and at species
level. According to IUCN Red List (2008), more than a third of world’s amphibian
species are at the risk of extinction, making them the world’s most threatened group
of animals.
Unfortunately, threats to the amphibians are often difficult to quantify due to
the varying amphibian population. The decline in numbers in a certain year may be
part of a long-term fluctuation. Prolonged measures are required to fully comprehend
the population trend of the amphibians in a habitat, but with the rolling speed of
deforestation and habitat conversion, many populations were lost before we manage
to study them. Nevertheless, many studies that examined the factors that contributed
to the decline of amphibians are being carried out. Climate change, habitat loss and
alteration, exposure to pesticides and pollutants, diseases, increased exposure to UV
radiation, and introduction of exotic species which induce tough inter-species
competition on food and shelters (Alford & Richards, 1999; Bickford et al., 2010;
Blaustein & Bancroft, 2007; Daszak et al., 2003; Duellman & Trueb, 1986; Ibrahim,
2004; Kiesecker et al., 2001; Pounds et al., 2006; Whitfield et al., 2007).
One example of amphibian species extinction in the wild due to habitat loss is
the case of Kihansi spray toad (Nectophrynoides asperginis), which has the smallest
habitat distribution range in vertebrate animals, and endemic to the spray zone around
the Kihansi waterfalls in the southern Udzungwa Mountains in Tanzania. The
37
construction of Kihansi Dam, coupled with chytridiomycosis disease destroys the
formerly large population in the limited habitat. The last recorded wild Kihansi spray
toad was in year 2004 (Channing et al., 2009).
Amphibians are very susceptible to diseases caused by bacteria and fungi. One
individual of a population that contracted a contagious disease could spread the disease
to others in a short period, and the whole population would be wiped out in a short
matter of time (Daszak et al., 1999). This scenario is especially true for captive
herptiles, either in the zoos or hobbyists’ private collections. The most commonly
encountered amphibian disease is the red-leg disease, caused by the infection of
bacterium Aeromonas hydrophila. This infection is not only communicable from frog
to frog; it can also be passed along to salamanders and snakes. An amphibian that
contracted red-leg disease becomes badly bloated and appears to be water-logged. A
suffusion of red over the underside hind legs becomes apparent. The infected animal
will cease to feed and eventually succumbed to death by starvation (Breen, 1974).
Aside from that, the chytrid fungus infection or also called chytridiomycosis is
an infamous and deadly disease that keeps herpetologists and veterinarians all over the
world worrying about the amphibian populations. It is caused by the waterborne, non-
hyphal zoosporic fungus, Batrachochytrium dendrobatidis. Chytridiomycosis
develops in keratinised cells, causes hyperkeratosis, and disturbs the ﬂuid and
electrolyte balance which promptly leads to the death (Mcleod & Sheridan, 2008;
Rollins-Smith et al., 2002). Nowadays, scientists uncover growing evidence of global
amphibian declines that are caused by chytrid fungus, for examples, the extinction of
Costa Rican variable harlequin toad (Atelopus varius), sharp snouted day frog
(Taudactylus acutirostris) and golden toad (Incilius periglenes) (Daszak et al., 2003;
Pounds et al., 2006).
38
CHAPTER 3
Materials and Methods
3.1 Study Sites
This study was conducted in Northern Peninsular Malaysia, which includes the
states of Kedah, Pulau Pinang and Perak. The study sites comprised Sungai Burung
(SB), Taman Rimba Teluk Bahang (TRTB), Universiti Sains Malaysia main campus
(USM), and Permatang Sungai Dua (PSD) in Penang; Karangan (KR), Ulu Paip (UP),
Sedim (SD), and Bukit Panchor (BP) in Kedah; Gunung Lang Recreational Park
(GLRP) in Perak; Telaga Tujuh (TT), Pantai Kok (PK), and Ulu Melaka (UM) in
Langkawi, Kedah.The sites were chosen mainly based on human activities that
resulted in disturbance to the local ecosystem (Table 3.1). All study sites were areas
with habitats that were altered to a certain degree by human presence, such as: (a)
highly disturbed areas: sites USM, PSD, GLRP & PK; (b) moderately disturbed areas:
sites SB, SD, BP & UM; and (c) slightly disturbed areas: TRTB, KR, UP & TT.
Location of each study sites is shown in Figure 3.1.
Environmental parameters of study sites and other details including the flora
and fauna of each site can be found in Appendix 1 and 2.
39
Table 3.1 Criteria for habitat disturbances.
Study Type locality Human Buildings Noise
Sites population (within 200 m) (vehicles)
SB Paddy field Moderate Residential house Moderate
TRTB Recreational park Low Park building Low
USM University campus High Residential building Very high
and faculty
PSD Paddy field Moderate None Moderate
KR Oil Palm Plantation Low None Moderate
UP Forest reserve Low Park building Low
SD Recreational forest Low Park building Low
BP Recreational forest Moderate Camp site & public Low
toilets
GLRP Parking lot Moderate Car park Very high
TT Recreational park Low Park building Moderately
Low
PK Grazing field Moderate Hotel High
UM Paddy field Seasonal None Moderate
40
N
Peninsular
Malaysia
200 km
Figure 3.1 Location of study sites: In Langkawi island, Kedah: (A) site TT; (B) site
PK; (C) site UM; In Penang state, (D) site SB; (E) site TRTB; (F) site USM; (G) site
PSD; In Kedah state, (H) site KR; (I) site UP; (J) site SD; (K) site BP; In Perak state,
(L) site GLRP. (modified from Google Maps, 2013)
41
3.2 Experimental Procedures
Research procedures of the experiment are shown as below (Fig. 3.2).
Collection of prey
Collection of specimens
from the field items in the
environment
Measuring of specimens
morphometrical data
Releasing of
Stomach flushing of specimens back into
specimens the wild
Identification and analysis

of stomach content
Data analysis
Report
Figure 3.2 Research flow chart.
42
3.2.1 Collection of Specimens
Collection of frogs was carried out either weekly or twice weekly from October
2012 until March 2013. Random samplings were employed during the night from 2000
h to 2200 h. Despite being time consuming and tedious, random sampling was chosen
as this method ensures a high degree of representativeness of each specimen. The
collection method was based on the standard frog sampling method for arboreal,
terrestrial and riparian frogs, in which rocks were turned, logs were rolled over, litters
were raked and vegetation were examined for frogs (Inger, 1980). Frogs were most
often caught by hand, but sometimes with the aid of tools, such as nets and poles. Since
all samplings were done at night, headlamps and torchlights were also utilised. Frogs
were located through opportunistic encounters, the calls of anuran, and also the
reflection of light from the torchlight by the eyes. Total search effort was 234 person-
hours. All frogs caught were placed into individual plastic bags and brought back to
the laboratory in Universiti Sains Malaysia, Penang for stomach content analysis, with
the exception of anurans from Langkawi. The anurans were then measured, stomach-
flushed and released on the island.
The weather, temperature and humidity for each sampling location were
recorded using E-Sun ETP101 Thermo-hygrometer as references. Prey or
invertebrates in the environment were also collected during specimen collection. A 30-
cm x 20 cm glue trap were placed at a random spot on the ground during sampling.
Glue trap samples were stored in a freezer until prey items were identified. All
invertebrates were counted and sorted to order and lowest recognizable taxonomic unit.
Anurans were identified based on Berry (1975) and the amphibian database
compiled by Norhayati et al. (2009). Species names were updated according to Frost
43
(2013). Males were identified based on the presence secondary sex characteristics,
such as the presence of vocal sacs (P. leucomystax), nuptial pads or spines (D.
melanostictus and P. leucomystax), yellowish colouration of under throat (D.
melanostictus), ovaries observed through translucent ventral skin (M. heymonsi, M.
butleri and M. fissipes) and a pair of openings present at base of lower jaw (M.
heymonsi, M. butleri, M. fissipes and P. leucomystax). Frogs were categorized into
adult and sub-adult according to their snout-vent length (SVL). We used the adult SVL
ranges of Berry (1975) or Norhayati et al. (2009) to assign individuals to adult or sub-
adults.
44
3.2.2 Morphometric Measurements
Back in the lab, each individual anuran's snout-ventral length (SVL), and head
width or mouth width (MW) were measured using Pro'sKit® electronic digital
callipers (±0.01cm). Frog body weight was measured using Acculab© VI-400 digital
scale to the nearest 0.1 g.
Two individuals of each species were euthanized and kept in Amphibian
Reptile Collection of School of Distance Education, Universiti Sains Malaysia as
voucher specimens (USMARC 13001 to USMARC 13012). The rest of the frogs was
released into the wild after recovery. Voucher specimens were euthanized using
intracoelomic injection of 1% tricaine methanesulfonate (MS-222) solution at doses
of 250 to 500 mg/kg frog bodyweight before setting and kept in 70% alcohol solution
in the laboratory. The photographs of the amphibians were taken in the lab using
camera of the model Canon PowerShot A590 IS.
45
3.2.3 Collection of Stomach Content
Stomach contents of the frog were flushed out using stomach flushing method
as suggested by Soléet al. (2005). Stomach flushing technique involved inserting a
soft blunt infusion tube (connected to a syringe filled with water) into the stomach of
the frog through its mouth. The size of infusion tube was adjusted in accordance to the
mouth width of the frogs, i.e. a 2 mm diameter infusion tube was used for M. heymonsi
while a 5 mm diameter infusion tube was used for D. melanostictus. The water in the
syringe was then flushed into the stomach and any content that is forced out is collected
in the sieve. The collected stomach contents were transferred into a labelled
microcentrifuge tube containing 10% formalin. This is to preserve and retain the
stomach contents for future references.
Stomach contents were then sorted and observed under a light microscope to
identify the prey items to the lowest recognizable taxonomic unit (RTU), typically
familial or ordinal level. Family Formicidae was further identified to species level and
sorted as a separate category. Taxonomic identification of invertebrate prey items
follows Borror & White (1970) whereas ant species identification was according to
Hashimoto (2003) and AntWeb (2013). Pest or non-pest classification is based on
Vreden & Ahmadzabidi (1986) and Khoo et al., (1991), although in general, pests
mentioned in this study refer to insect pests that caused nuisance to humans.
The identified stomach contents were later air-dried using Memmert
AtmoSAFE® Model 100-800 and the dry weight of prey items were measured using
Radwag AS 200/X Precision Balance to the nearest 0.001g.
46
3.2.4 Data Analysis
Measurements of SVL, MW and weight were compared intraspecies, between
sexes. Unpaired t-test with Welch's correction was run to compare and analyse the
three basic morphometric measurements using GraphPad Prism version 6.04 for
Windows and Free statistical software by Wessa (2014). Mann-Whitney unpaired t-
tests were applied to compare the diet differences between male and female anurans.
The relationships between size of body and prey was examined by regressing volume
of the largest (VMAX) and smallest prey (VMIN) in a stomach on anurans SVL and
calculating correlation coefﬁcients. Only anuran specimens with at least three prey
items in their stomachs were included in this analysis. Jaccard similarity coefficient is
used for comparing the similarity and diversity of sampling sites (Tan et al., 2005).
Stomach contents data was analysed using the method of stomach content analysis
proposed by Lima-Junior & Goitein (2001).
3.2.4.1 Frequency of Occurrence (Fi)
The frequency of occurrence used the formula (Hyslop, 1980):
100𝑛𝑖
𝐹𝑖 =
𝑛
where,
Fi : frequency of occurrence of i prey item in the sample;
ni : number of stomachs in which i prey item is found;
n : total number of stomachs with food in the sample.
47
3.2.4.2 Jaccard Similarity Coefficient (J)
The presence of anurans in each sampling sites was turned into binary attributes,
1 was given if there was presence of anuran species, and 0 if not. Jaccard coefficient
was used to measure the overlap of any two sampling sites, using the following
formula (Jaccard, 1912; Tan et al., 2005):
𝑀11
𝐽=
𝑀01 + 𝑀10 + 𝑀11
where,
M11 : total number of attributes where both sites have a value of 1;
M01 : total number of attributes where the attribute of site i is 0 and the attribute
of site j is 1;
M10 : total number of attributes where the attribute of site i is 1 and the attribute
of site j is 0.
3.2.4.3 Volumetric Analysis Index (Vi)
The Volumetric Analysis Index indicates the relative abundance of a particular
item found in the stomach samples, based on points ascribed to distinct prey items. V i
is calculated using the formula (Lima-Junior & Goitein, 2001):
𝑉𝑖 = 25 𝑀𝑖
where:
Vi : Volumetric Analysis Index of the i prey item in the sample;
25 : multiplication constant to obtain a percentage;
Mi : mean of ascribed points for the i prey item.
This procedure is executed with a constant reference called Standard Weight
(SW). The Standard Weight (SW) is the arithmetic mean of weights of stomach
contents of specimens caught in a previous collection.
48
Total stomach content weight
Mean weight of stomach contents (SW) = × 100%
total anuran weight
The calculated SW in the first sample was used as a constant value for
analysing and comparison of subsequent samples. Once SW was determined, integer
points were ascribed to each prey items according to weight in relation to SW. A prey
items with a weight of approximately 25% of SW was ascribed 1 point. The points
were distributed among the prey items in the stomach in proportion to the volume each
item occupies, minimally at 0.5 point. Consequently, the less abundant items present
in the stomach content were not focused on. 𝑀𝑖 calculated for each state was postulated
showing v3 frequency of occurrence of prey items. The points ascribed were later
transformed into an arithmetical mean:
∑𝑖
𝑀𝑖 =
𝑛
where:
Mi: mean of the ascribed points for the i prey item;
Σi : sum of the ascribed points for the i prey item;
n: total number of stomachs with food in the sample.
3.2.4.4 Importance Index
Importance Index indicated the relative importance a prey item in the diet
composition, and was obtained using the formula:
AIi=Fi . Vi
where:
AIi: Importance Index of the i prey item in the sample;
Fi: Occurrence Frequency of the item;
Vi: Volumetric Analysis Index of the item.
49
3.2.4.5 Diversity Index (H’)
Diversity index was used to indicate the range of prey types (on family level)
that the anuran fed on. The higher the index value, the more the types of prey that were
consumed by the specimen. The formula used in this experiment was Shannon-Wiener
Index, which range from 0 to 5.0.
H ’=- ∑(pi )(log 10 pI )

i=1
where,
H’ : Shannon-Wiener Index;
pi : percentage of prey item i in specimen;
S : total type of prey consumed by specimen.
3.2.4.6 Prey selection
Jacobs’ prey electivity formula (Jacobs, 1974) was used to determine the prey
selection and preference. Electivity values range from -1 to +1, where negative values
indicate voidance of a prey category, and positive values indicate preference. Mean D i
values <≤ 0.70 and > 0.70, indicated strong preference for invertebrate taxa that
represented > 2% of the diet or environmental samples were presented (Hirai & Matsui,
2002; Toft, 1981).
(𝑝𝑠 − 𝑝𝑒 )
𝐷𝑖 =
(𝑝𝑠 + 𝑝𝑒 ) − (2 ∙ 𝑝𝑠 ∙ 𝑝𝑒 )
where, ps : proportion of each prey taxon in stomachs;
pe : proportion of each prey category in the environment.
50
3.2.4.7 Niche breadth
Niche breath of each species is also calculated using the reciprocal of
Simpson's Index (Krebs, 1999):
1
𝐵=
∑ 𝑝𝑖2
where pi is the proportion of i prey item.
Measures are standardized on a scale of 0 to 1 by using the formula:
𝐵−1
𝐵𝐴 =
𝑛−1
where, BA : the standardized niche breadth,
n : the total number of food items for the species of interest.
3.2.4.8 Niche overlap
Niche overlap is the measure of the association between species, as it refers to
the similar requirements of the species with respect to some dimensions of the niche
hyper volume. The higher the niche overlaps between two species, the more likely that
they shared resources and the more probable that they are sympatric species. Pianka
(1986) niche overlap, measures range from 0 (no resources used in common) to 1
(complete overlap), is calculated as (Krebs, 1999):
where,
Ojk : Pianka’s measure of overlap between species j and species k,
pij : the proportion that resource i is of the total resources used by species j,
pik : the proportion that resource i is of the total resources used by species k.
51
CHAPTER 4
Results
4.1 Basic Morphology of Specimens
A total of 387 individuals of frogs and toads were collected, in which 120
individuals (31.0%) were Duttaphrynus melanostictus, followed by 86 individuals
(22.2%) of Microhyla butleri, 77 individuals (19.9%) of Microhyla fissipes, 53
individuals (13.7%) of Microhyla heymonsi, and 51 individuals (13.2%) of
Polypedates leucomystax (Fig.4.1).
51
120
53
77
86
Duttaphrynus melanostictus Microhyla butleri

Microhyla fissipes Microhyla heymonsi
Polypedates leucomystax
Figure 4.1 Number of specimens collected, according to species.
52
1 cm
1 cm
A B
1 cm C D 1 cm
E 1 cm
Figure 4.2 Frogs and toad species: (A) Duttaphrynus melanostictus; (B) Microhyla
butleri; (C) Microhyla fissipes; (D) Microhyla heymonsi; and (E) Polypedates
leucomystax.
53
In three species (Duttaphrynus melanostictus, Microhyla butleri and Microhyla
fissipes) more than half of their sampled populations was subadults while in two
species (Microhyla heymonsi and Polypedates leucomystax) the majority was adults.
Adult females were very poorly represented in three species (D. melanostictus, M
heymonsi and P. leucomystax) while in two species (M. butleri and M, fissipes) there
was no adult female at all. The smallest percentage of females was shown by D.
melasnostictus (6%), followed by M. heymonsi (13%) and P. leucomystax (20%). A
summary of the number of individuals in different maturity stages and sexes were
shown in Figure 4.3.
0 20 40 60 80 100 120
Duttaphrynus melanostictus 73 39 7
Microhyla butleri 71 15
Microhyla fissipes 72 5
Microhyla heymonsi 14 34 5
Polypedates leucomystax 41 10
Sub-adult Adult male Adult female
Figure 4.3 The number of sub-adults (juvenile males and females), adult males and
adult females across species.
54
Table 4.1 The mean, maximum value, and minimum value of snout-to-vent length
(SVL, mm) of specimens, separated by sex.
Specimens n Mean Max Min

Duttaphrynus female 55 51.56 77.21 29.92
melanostictus male 65 59.29 72.61 35.17
Microhyla butleri female 31 20.18 21.81 18.40
male 55 20.10 21.81 17.80
Microhyla fissipes female 28 20.53 22.34 16.25
male 49 20.47 23.73 18.36
Microhyla heymonsi female 15 20.39 24.03 13.51
male 38 18.49 23.73 13.50
Polypedates leucomystax female 10 57.56 70.50 38.36
male 41 42.24 48.97 31.10
The mean, maximum value and minimum value of snout-to-vent length (SVL)
of all five species, separated by sexes, are recorded in Table 4.1. Three of the anuran
species showed sexual dimorphism in body sizes, in which there were significant
differences between the SVLs of males and females. Of these three, only Duttaphrynus
melanostictus had larger males (t=4.512, df=118, P<0.0001), whereas for both
Polypedates leucomystax (t=6.593, df=49, P<0.0001) and Microhyla heymonsi
(t=2.373, df=51, P=0.0215), females were significantly larger than males. There were
no significant differences in body sizes of males and females of Microhyla butleri
(t=0.4287, df=84, P=0.6692) and Microhyla fissipes (t=0.2048, df=75, P=0.8383).
55
Table 4.2 Maximum, minimum, and mean of male (m) and female (f) specimens’
weight (g).
Specimens n Mean Max Min

Duttaphrynus f 55 13.1 ±1.3 48.3 2.6
melanostictus m 65 17.9 ±0.9 34.2 2.9
Microhyla f 31 0.8 ±0 1 0.6
butleri m 55 0.7 ±0 1 0.5
Microhyla f 28 0.8 ±0 0.9 0.6
fissipes m 49 0.8 ±0 1.4 0.6
Microhyla f 15 0.8 ±0 1.3 0.3
heymonsi m 38 0.6 ±0 1.2 0.4
Polypedates f 10 13.4 ±3.7 32.9 3.1
leucomystax m 41 4.2 ±0.5 7.3 2.1
Table 4.2 above showed the mean, maximum, and minimum body weight of
the five species of anurans. Corresponding to the result of body size, males D.
melanostictus were significantly heavier than the females (t=3.076, df=102.4,
P=0.0027), as were the females of P. leucomystax (t=2.468, df=9.041, P<0.0001) and
M. heymonsi (t=2.677, df=17.86, p=0.0082) heavier than their males counterpart,
while there was no significant weight difference between the sexes of M. butleri
(t=1.775, df=69.53, P=0.4327). The only discrepancy in this was M. fissipes, whereby
despite the lack of significant difference in body sizes of male and female frogs, males
were found to be significantly heavier (t=0.05284 df=74.72, P=0.0007).
56
As mouth width positively correlated with body size, the sexual dimorphism in
mouth width of the five studied species conforms to the findings in body size, in which
mouth width of male D. melanostictus was wider than the females (t=2.858, df=99.18,
P=0.0069), while females had larger mouth width in P. leucomystax (t=3.906,
df=9.730, P< 0.0001) and M. heymonsi (t=4.405, df=19.74, P=0.0891). No significant
different in the mouth widths of male and female was shown of both M. butleri
(t=1.058, df=69.15, P=0.4579) and M. fissipes (t=0.9401, df=56.45, P> 0.9999).
Additionally, the mean, maximum and minimum values of mouth width (MW) were
presented in Table 4.3.
Table 4.3 Range and mean of mouth width (MW, mm) of specimens.
Specimens n Mean (±SEM) Range

Duttaphrynus female 55 16.59 (±.66) 9.70 – 30.99
melanostictus male 65 18.83 (±0.43) 14.26 – 27.09
Microhyla butleri female 31 5.37 (±0.09) 4.30 – 6.50
male 55 5.51 (±0.08) 4.20 – 6.50
Microhyla fissipes female 28 5.25 (±0.10) 3.88 – 6.50
male 49 5.37 (±0.08) 4.26 – 7.45
Microhyla heymonsi female 15 5.66 (±0.19) 5.00 – 7.20
male 38 4.73 (±0.09) 3.90 – 5.81
Polypedates female 10 17.57 (±1.13) 12.19 – 21.53
leucomystax male 41 13.07 (±0.40) 10.00 – 16.65
57
4.2 Specimen Availability According to Study Sites
Study sites from highly disturbed areas showed 65% of similarity in Jaccard
coefficient (J), while the mean coefficient of communities of moderately disturbed
areas was 44%, and mean coefficient of slightly disturbed areas was 50%. The mean
coefficient of all 12 study sites (66 pairs) obtained was 49%. Detailed findings at each
sampling site can be found in Table 4.4.
Most specimens were caught in highly disturbed areas (62%), with nearly half
of the specimens came from site USM alone (47%), as the catch dwindled at less
disturbed areas. There was a higher probability of finding the five species of “disturbed
area anurans” in highly disturbed areas (P=0.75), and sites USM and GLRP were the
only two study sites where all five species of the anurans were found. Microhyla
butleri was found in all highly disturbed areas, and site SB, which showed a high
similarity to other highly disturbed sites (J=0.78).
Among the five species of frogs and toad, only D. melanostictus was found at
all study sites. This species was also the sole disturbed species present in site PK and
site TT in Langkawi Island, Kedah. It also comprised the highest number of specimens
(120 individuals) caught in this study. Although found only in five of the study sites,
Microhyla butleri was the second most caught specimens (86 individuals), with site
USM being the main contributor site, followed by site GLRP. Despite being the least
in number, Microhyla heymonsi was the more widespread species among the three
Microhyla in the study (found at 8 sites out of 12), yet it was not found in all three
Langkawi sites during the sampling period. Polypedates leucomystax comprised the
smallest number of specimens, found exclusively in study sites with tall vegetation
and trees.
58
Table 4.4 Relative abundance of amphibian species according to study sites.
Study Sites\ Species DM MB MF MH PL Total

SB 4 12 37 6 0 59
TRTB 1 0 0 0 7 8
USM 84 54 23 9 10 180
PSD 1 6 0 14 0 21
KR 2 0 1 2 6 11
UP 3 0 4 1 16 24
SD 3 0 0 9 10 22
BP 2 0 0 5 0 7
GLRP 1 13 10 7 2 33
TT 12 0 0 0 0 12
PK 1 1 2 0 0 4
UM 6 0 0 0 0 6
Note:
SB=Sungai Burung, TRTB=Taman Rimba Teluk Bahang, USM=Universiti Sains

Malaysia, PSD=Permatang Sungai Dua, KR=Karangan, UP=Ulu Paip, SD=Sedim,
BP=Bukit Panchr, GLRP=Gunung Lang Recreational Park, TT=Telaga Tujuh,
PK=Pantai Kok, UM=Ulu Melaka; DM=Duttaphrynus melanostictus, MB=Microhyla
butleri, MF=Microhyla fissipes, MH=Microhyla heymonsi, PL=Polypedates
leucomystax.
59
4.3 Prey Availability of Study Sites.
Table 4.5 summarises the presence of invertebrates and possible prey items
that were trapped by the glue traps placed at study sites during sampling periods. A
total of 125 invertebrates were caught and identified. Dominant prey items caught by
the trap were a tie between flying and phytophagous invertebrates (43.2%) and ants
(Formicidae, 43.2%). The largest prey items that were caught on trap was a cricket
(Orthoptera: Tetrigidae) with the size of 3360 mm3. However, due to the limitation of
glue traps, the invertebrates represented by Table 4.5 may not truly reflect the
availability of prey items of the study sites.
All 14 prey categories found in glue traps (Table 4.5) were found in stomach
contents of the specimens (Table 4.7). More gnats (Cecidomyiidae) were trapped than
were found in the stomach contents. Ants (Formicidae), termites (Termitidae), ground
beetles (Carabidae) and spiders (Aranaea) were more frequent in the diet than in the
environment. 13 out of 14 prey in the environment were also found in D. melanostictus
diet. Consequently, Jacobs’ prey electivity index showed toads preferred ants (D=0.72)
and showed slight avoidance towards spiders (D=-0.28). Only 6 types of prey found
in the environment were encountered in P. leucomystax diet. The electivity index
showed that P. leucomystax showed no favouritism towards ants or spiders (D=0.03
and 0.18, respectively). Microhyla butleri preyed on 9 of the prey found in the
environment, with a very strong preference towards ants (D=0.93) and some avoidance
towards spiders (D=-0.32). Microhyla fissipes dietary composition only had 6 of the
prey categories found in the environment, favouring ants (D=0.94) and avoiding
spiders (D=-0.39). Only 5 of the prey categories found in the environment were also
found in the stomach contents of M. heymonsi. While highly preferring ants (D=0.97),
M. heymonsi showed a slight avoidance to spiders (D=-0.29).
60
Table 4.5 Prey items found at study sites.
Class: Order: Family SB TRTB USM PSD KR UP SD BP GLRP TT PK UM

Blattellidae - - - - - - - 1 - - - -
Blattodea
Termitidae 3 1 7 - - - - - - - - -
Carabidae - - - - - - 1 - - - - -
Coleoptera
Coccinellidae - - - - 1 - - - 2 - - -
61
Cecidomyiidae 4 - - 11 12 - 9 - - - - -
Insecta Diptera Culicidae - - 1 - - - - - - 2 - -
Muscidae 1 - - 1 - - - - - - - 2
Hymenoptera Formicidae 6 2 7 5 4 1 5 6 4 5 6 3
Odonata Coenagrionidae - - - - - - - - - 1 - -
Tetrigidae - - - - - - - - - - 1 -
Orthoptera
Gryllidae 1 - - 1 - - 1 - - - - 2
Arachnida Araneae 1 - - - - - - - 2 - - -
Chilopoda - - - - - 1 - - - - - -
Diplopoda - - 1 - - - - - - - - -
4.4 Stomach Contents of the Specimens
Empty Non-empty
Polypedates leucomystax 26 25
Microhyla heymonsi 9 44
Microhyla fissipes 23 54
Microhyla butleri 9 77
Duttaphrynus melanostictus 2 118
0% 20% 40% 60% 80% 100%
Figure 4.4 Empty versus non-empty stomachs, according to species.
Figure 4.4 shows the overall percentage of empty and non-empty stomachs of
specimens. Total number of stomachs containing prey items of all five species was
318 (82.2%). Out of these, D. melanostictus had the highest percentage of non-empty
stomachs (98.3%), while P. leucomystax had least (49.0%). Four out of five species
(exception on P. leucomystax) were found with more than 50% of individuals with
stomach contents.
In total, 2830 prey items in 42 prey categories were identified from the stomach
contents. Ants (Hymenoptera: Formicidae), were the most numerous prey items in the
diets of all five anuran species (Table 4.7). Hemipterans and Araneae were the only
orders present in the diets of all five anuran species. Platygasteridae made up only a
small proportion (ca. ≤ 1%) of the diet composition, thus, inter-species comparisons
were not feasible.
62
Table 4.6 Non-prey items that were consumed and found in stomachs of specimens.
Number of stomachs
Non-prey Duttaphrynus Microhyla Microhyla Microhyla Polypedates
items melanostictus butleri fissipes heymonsi leucomystax
Parasites 0 0 0 0 10
Skin 4 0 0 0 0
Egg 1 0 0 0 0
Plant 40 26 16 6 1
Inorganic
19 11 9 5 0
materials
Number of prey items consumed varied vastly across species (F=0.98, df=4,
P=0.4212), ranged from 42 (D. melanostictus) to 13 (P. leucomystax). Of the overall
prey compositions, 95.4% was insects (Fig. 4.5), which contributed to 109.67 cm3 in
volume. Almost all of the insect prey was pest (91.7%, Fig.4.6). Intake of vegetation
materials by the anuran specimens included small blades of grasses, leaves and fibril
roots; while inorganic materials consumed were sands and stones (size 2 – 7 mm)
(Table 4.6). Cannibalism occurred in one specimen of D. melanostictus as three eggs
were found among its stomach contents. Several specimens of D. melanostictus
ingested (possibly its own) shredded skins. In the case of P. leucomystax, gut parasites
(nematodes) were flushed out along with stomach contents.
Total stomach content weight showed that female of D. melanostictus and M.
butleri consumed more than the males; whereas stomach weight analysis of P.
leucomystax, M. fissipes and M. heymonsi displayed the opposite result. The weight of
stomach contents hardly contributes to total body weight of the amphibians (0.02% –
4%).
63
Table 4.7 The dietary composition (N; as a % of the total number of recorded prey items), and frequency of occurrence (F; the number of
anurans, as a %, of each species) of the dietary items of Duttaphrynus melanostictus, Polypedates leucomystax, Microhyla butleri, Microhyla
fissipes, and Microhyla heymonsi in this study. (Total=the total number of prey items).
Duttaphrynus Polypedates Microhyla

Microhyla butleri Microhyla fissipes
Taxa melanostictus leucomystax heymonsi
N F N F N F N F N F
Blattellidae 0.42 1.82
Termitidae 1.79 2.27 20.41 3.70 0.20 1.01
Bostrichidae 0.21 0.91 0.39 2.02 0.63 3.08
Carabidae 8.97 13.18 2.04 3.70 1.18 3.51
Chrysomelidae 0.84 3.18 10.20 14.81 0.78 3.03 0.21 1.54
64
Coccinellidae 0.21 0.91 0.39 2.02 0.21 1.54

Dytiscidae 0.11 0.45 0.24 0.58 0.20 1.01
Scarabaeidae 0.11 0.45
Staphylinidae 0.32 0.45 2.04 3.70
Tenebrionidae 2.11 4.09 1.06 2.34 1.37 6.06 1.05 3.08
Carcinophoridae 1.27 4.09 0.35 1.75 0.78 3.03 0.42 3.08
Cecidomyiidae 0.42 1.36 0.71 2.92 0.39 2.02
Culicidae 0.35 1.17 0.98 3.03 0.21 1.54
Muscidae 0.11 0.45 4.08 7.41 0.20 1.01
Baetidae 0.11 0.45 0.94 4.09 0.59 3.03 0.42 3.08
Alydidae 0.74 2.27 0.12 0.58 0.39 1.01
Coreidae 0.63 1.82 0.20 1.01
Gerridae 0.11 0.45 0.47 1.17 0.39 2.02
Pentatomidae 0.21 0.91 4.08 7.41 0.12 0.58 0.21 1.54
Platygasteridae 0.42 1.36 6.12 7.41 0.47 1.75 0.78 4.04 0.21 1.54
Ponerinae 12.13 10.91 20.41 11.11 2.48 2.34 0.39 2.02 0.21 1.54
Table 4.7 (cont’d)
Duttaphrynus Polypedates Microhyla

Microhyla butleri Microhyla fissipes
Taxa melanostictus leucomystax heymonsi
N F N F N F N F N F
Formicinae 16.77 7.73 6.12 3.70 35.42 14.62 54.90 22.22 78.78 33.85
Myrmicinae 41.14 12.27 51.71 43.86 32.75 24.24 14.50 23.08
Lepidoptera 0.32 1.36 2.04 3.70 0.20 1.01
Crambidae 0.11 0.45 0.12 0.58
Pyralidae 0.95 1.82 14.29 18.52
Philopteridae 0.11 0.45 0.12 0.58
Coenagrionidae 0.11 0.45 4.08 7.41 0.59 2.02
Gomphidae 0.21 0.91
65
Tetrigidae 0.42 1.36 0.12 0.58

Gryllidae 0.53 2.27
Siphonaptera 0.21 0.91
Plecoptera 0.11 0.45 0.24 1.17 0.39 2.02 0.42 3.08
Acarina 0.11 0.45 0.24 1.17 0.20 1.01 0.21 1.54
Araneae 1.16 4.55 2.04 3.70 1.18 4.09 0.98 3.03 1.26 9.23
Tetranychoidae 0.21 0.91 0.59 2.92 0.20 1.01 0.63 4.62
Armadillidiidae 3.80 3.64 0.47 1.17 0.78 3.03 0.21 1.54
Chilopoda 0.53 1.36
Diplopoda 0.63 1.82 0.24 1.17 0.21 1.54
Oligochaeta 0.53 1.82 0.12 0.58 0.20 1.01
Gastropoda 0.21 0.91
Crustacea 0.11 0.45
Unidentified prey 0.53 1.82 2.04 3.70 0.94 4.68 0.39 2.02
Total 948 49 847 510 476
Non- Overall Non- Duttaphrynus
insect insect
4.56% 7.70%
melanostictus
Insect Insect
95.44% 92.30%
Non-
Microhyla Non- Microhyla
insect
3.54%
butleri insect
2.55%
fissipes
Insect Insect
96.46% 97.45%
Non-
Microhyla Non- Polypedates
insect
2.31%
heymonsi insect
4.08%
leucomystax
Insect Insect
97.69% 95.92%
Figure 4.5 (A) Percentage of insect versus non-insect diet in overall diet
composition; (B) Percentage of insect vs non-insect diet of D. melanostictus; (C)
Percentage of insect vs non-insect diet of M. butleri; (D) Percentage of insect vs non-
insect diet of M. fissipes; (E) Percentage of insect vs non-insect diet of M. heymonsi;
(F) Percentage of insect versus non-insect diet of P. leucomystax.
66
Non-pest Duttaphrynus
8.30% Overall Non-pest
11.60% melanostictus
Pest Pest
91.70% 88.40%
Non-pest Microhyla Non-pest Microhyla

6.26%
butleri 7.25%
fissipes
Pest Pest
93.74% 92.75%
Microhyla Polypedates
Non-pest Non-pest
3.57% heymonsi 36.73%
leucomystax
Pest
Pest 63.27%
96.43%
Figure 4.6 (A) Percentage of pest versus non-pest diet in overall diet composition;
(B) Percentage of pest vs non-pest diet of D. melanostictus; (C) Percentage of pest vs
non-pest diet of M. butleri; (D) Percentage of pest vs non-pest diet of M. fissipes; (E)
Percentage of pest vs non-pest diet of M. heymonsi; (F) Percentage of pest versus
non-pest diet of P. leucomystax.
67
4.4.1 Stomach Contents of Duttaphrynus melanostictus
A total of 39 prey items of the order Insecta were recorded from D.
melanostictus stomach contents from a total of 948 prey items (Table 4.8). Most of D.
melanostictus diet was found to be pest (88.40%, Fig. 4.8). Of this, the most important
prey items (ca. ≥ 10%) were ants (Formicidae) and ground beetle (Carabidae).
Formicidae was not only consumed in the greatest amount (n=664), but was also the
most encountered prey items of D. melanostictus (F=30.91).
Mean prey consumption of D. melanostictus was 8.04 ±1.04 prey items. Mann-
Whitney rank t-test showed that the amount of prey consumed by females (mean=6.35
±1.23) and males (mean=9.52 ±2.39) were not significantly different (Mann-Whitney
U=1729, P=0.9838). Maximum prey items found in a single toad was 114 in a stomach
of an adult male, and 58 in a female. The mean prey per stomach was 1.88 ±0.09 prey
items. None of the sex had more diet variety than the other (Mann-Whitney U=1479,
P=0.1418). Females’ mean prey per stomach was 2.56 ± 0.15, while the males’ prey
per stomach was 1.71 ±0.11 prey items. The most variety of prey items in one stomach
of a female was 5 prey items, and of a male was 4 prey items.
Table 4.9 showed that the most dominant prey items of D. melanostictus in the
family Formicidae, were Centromyrmex sp., Pheidole megacephala, and Solenopsis
geminata, in that order. Tropical fire ants Solenopsis geminata was found the most,
totalling at 207 ants (31.37%). Centromyrmex sp. was the prey choice of most D.
melanostictus (F=32.35).
68
items), frequency of occurrence (F; % of the number of stomachs), volume (V; % of
the total volume of prey items), and Importance Index (AI) of the dietary items of
Duttaphrynus melanostictus in this study.
Taxa N F V AI
Blattellidae 0.42 1.82 1.88 3.42
Termitidae 1.79 2.27 2.72 6.18
Bostrichidae 0.21 0.91 0.05 0.04
Carabidae 8.97 13.18 21.69 285.96
Chrysomelidae 0.84 3.18 1.65 5.27
Coccinellidae 0.21 0.91 0.53 0.48
Dytiscidae 0.11 0.45 0.28 0.13
Scarabaeidae 0.11 0.45 0.21 0.10
Staphylinidae 0.32 0.45 0.49 0.22
Tenebrionidae 2.11 4.09 2.90 11.84
Carcinophoridae 1.27 4.09 1.90 7.78
Cecidomyiidae 0.42 1.36 0.43 0.59
Muscidae 0.11 0.45 0.38 0.17
Baetidae 0.11 0.45 0.08 0.04
Alydidae 0.74 2.27 0.93 2.12
Coreidae 0.63 1.82 0.98 1.79
Gerridae 0.11 0.45 0.02 0.01
Pentatomidae 0.21 0.91 0.06 0.06
Platygasteridae 0.42 1.36 0.84 1.14
Formicidae 70.04 30.91 43.92 1357.38
Lepidoptera 0.32 1.36 0.97 1.32
Crambidae 0.11 0.45 0.39 0.18
Pyralidae 0.95 1.82 2.51 4.57
Philopteridae 0.11 0.45 0.02 0.01
Coenagrionidae 0.11 0.45 0.17 0.08
Gomphidae 0.21 0.91 0.84 0.76
Tetrigidae 0.42 1.36 1.67 2.28
69
Table 4.8 (cont’d)
Taxa N F V AI
Gryllidae 0.53 2.27 0.90 2.04
Siphonaptera 0.21 0.91 0.25 0.23
Plecoptera 0.11 0.45 0.02 0.01
Acarina 0.11 0.45 0.04 0.02
Araneae 1.16 4.55 1.57 7.14
Tetranychoidae 0.21 0.91 0.30 0.27
Armadillidiidae 3.80 3.64 3.30 12.01
Chilopoda 0.53 1.36 1.65 2.26
Diplopoda 0.63 1.82 1.81 3.30
Oligochaeta 0.53 1.82 0.76 1.38
Gastropoda 0.21 0.91 0.16 0.15
Crustacea 0.11 0.45 0.23 0.10
Unidentified prey 0.53 1.82 0.48 0.87
Total 948 82.14 cm3
Table 4.9 The Formicidae diet (N; % of the total number of recorded prey items),
frequency of occurrence (F; % of the number of stomachs), volume (V; % of the total
volume of prey items), and Importance Index (AI) of the dietary items of
Duttaphrynus melanostictus in this study.
Formicidae N F V AI
Centromyrmex sp. 16.42 32.35 15.95 516.19
Harpegnathos sp. 0.90 2.94 1.24 3.66
Other Formicinae 15.96 14.71 5.17 75.99
Lasius niger 3.01 7.35 1.21 8.89
Paratrechina sp. 4.82 1.47 1.11 1.63
Prenolepis imparis 0.15 1.47 0.12 0.17
Monomorium floricola 4.82 13.24 4.29 56.80
Pheidole megacephala 13.55 11.76 31.39 369.28
Solenopsis geminata 31.17 5.88 36.24 213.15
Tetramorium caespitum 9.19 8.82 3.28 28.98
70
4.4.2 Stomach Contents of Microhyla butleri
Microhyla butleri in this study showed a strong preference in insect diet, as a
mere 3.54% of its diet was non-insect prey (Fig. 4.5). However, 93.74% of the
consumed prey was considered pest to human (Fig. 4.6). Microhyla butleri in this study
fed on 948 prey, from 22 prey categories, with 8 unidentifiable prey (Table 4.10).
Index of importance indicated that ants were the dominant diet of M. butleri
(AI=4915.11), which were also the most dominant in terms of number (759 ants found),
frequency of occurrence (104 stomachs containing), and volume (9431.19 mm3).
Mean prey consumption per individual of M. butleri was 11.00 ± 1.47 prey
items. Male M. butleri (mean=10.82 ± 2.03) and female M. butleri (mean=11.35 ±
1.78) had similar mean prey consumption (Mann-Whitney U=544, P=0.2012).
Maximum prey ingested by male M. butleri was 66 prey and by a female was 37 prey.
Mean prey diversity per stomach of M. butleri was 2.22 ± 0.14 prey items. No
significant difference (Mann-Whitney U=559.5, P=0.2502) was shown by the females
(mean=2.5 ± 0.27) and males (mean=2.08 ± 0.15). Highest prey diversity in a female
was 6 prey items while males had 5 prey items. Mean prey volume per stomach was
151.6 ±16.3 mm3, with no significant difference (Mann-Whitney U=527.5, P=0.1459)
between males (mean=143.3 ±20.7 mm3) and females (mean=167.8 ±26.3 mm3). The
largest single prey volume was an undigested wasp found in a female (51.2 mm3).
Table 4.11 showed the most significant ant species in the diet of M. butleri, in
order of descending importance, were Big-headed ants (Pheidole megacephala)
pharaoh ants (Monomorium pharaonis), Arboreal flower ants (Monomorium floricola),
fire ants (Solenopsis geminata), and Black garden ants (Lasius niger).
71
Table 4.10 The dietary composition (N; % of the total number of recorded prey items),
volume of prey items), and Importance Index (AI) of the dietary items of Microhyla
butleri.
Taxa N F V AI
Carabidae 1.18 3.51 3.04 10.68
Dytiscidae 0.24 0.58 0.75 0.44
Tenebrionidae 1.06 2.34 3.32 7.78
Cecidomyiidae 0.71 2.92 0.40 1.18
Culicidae 0.35 1.17 0.13 0.15
Baetidae 0.94 4.09 1.55 6.36
Alydidae 0.12 0.58 0.04 0.03
Gerridae 0.47 1.17 0.17 0.20
Pentatomidae 0.12 0.58 0.08 0.05
Formicidae 89.61 60.82 80.82 4915.11
Crambidae 0.12 0.58 0.36 0.21
Philopteridae 0.12 0.58 0.24 0.14
Tetrigidae 0.12 0.58 0.35 0.21
Plecoptera 0.24 1.17 0.28 0.33
Acarina 0.24 1.17 0.18 0.21
Araneae 1.18 4.09 2.12 8.66
Diplopoda 0.24 1.17 0.29 0.34
Oligochaeta 0.12 0.58 0.43 0.25
Total 847 171 11.67 cm3
72
butleri in this study.
Formicidae N F V AI
Centromyrmex sp. 0 0 0 0
Lasius niger 21.21 11.54 12.68 146.30
Paratrechina sp. 11.46 4.81 5.34 25.65
Monomorium pharaonis 16.86 19.23 19.62 377.27
73
4.4.3 Stomach Contents of Microhyla fissipes
Figure 4.5 shows that M. fissipes had an insect dominant diet (97.45%), while
Figure 4.6 shows that majority of its diet was pests (92.75%). M. fissipes preyed on
510 prey from 24 different prey families (Table 4.12), contributed mainly by the males
(21 prey items), as females fed on a more narrow spectrum of prey items (11 prey
items). Most important prey items were ants (Formicidae), although darkling beetles
(Tenebrionidae) and wasps (Platygasteridae) also had a certain importance (AI ≥20)
in M. fissipes diet. Hence, ants had the highest value in prey number (n=449),
frequency of occurrence (F=48), and volume (V=89.18 cm3).
Microhyla fissipes had an average prey consumption of 9.44 ±1.29 prey items.
Mann-Whitney test (Mann-Whitney U=145.5, P=0.0002) indicated that males
(mean=12.38 ± 1.65) consumed more prey than females (mean=5.18 ± 1.74). The
maximum prey number found in one stomach for males and females, were 38 prey
items and 31 prey items respectively. Mean prey variety per stomach of this anuran
was 1.83 ± 0.16 prey items, whereby the mean prey variety of males was 2.18 ± 0.22
prey items, and the females was 1.32 ±0.15 prey items. Males prey on a significantly
wider variety of prey items than the females (Mann-Whitney U=196.5, P=0.0022). The
average stomach content volume of M. fissipes was 238.2 ±24.4 mm3, in which males’
stomachs (mean=297.4 ± 31.0 mm3) were significantly fuller than the females
(mean=152.1 ±32.2 mm3 ; Mann-Whitney U=161, P=0.0006).
Microhyla fissipes favoured ants from the subfamily Formicinae, which also
includes Lasius niger (third in rank of AI), Paratrechina sp., and Prenolepsis imparis
(Table 4.13). Bicoloured trailing ants (Monomorium floricola) was the second in terms
of dietary importance of M. fissipes.
74
Microhyla fissipes.
Taxa N F V AI
Termitidae 0.20 1.01 1.46 1.47
Bostrichidae 0.39 2.02 0.35 0.71
Chrysomelidae 0.78 3.03 3.27 9.91
Coccinellidae 0.39 2.02 1.39 2.81
Dytiscidae 0.20 1.01 0.30 0.31
Tenebrionidae 1.37 6.06 4.04 24.51
Cecidomyiidae 0.39 2.02 0.55 1.11
Culicidae 0.98 3.03 0.76 2.30
Muscidae 0.20 1.01 0.12 0.12
Baetidae 0.59 3.03 1.48 4.48
Alydidae 0.39 1.01 0.19 0.20
Coreidae 0.20 1.01 0.41 0.41
Gerridae 0.39 2.02 0.28 0.57
Formicidae 88.04 48.48 69.34 3361.74
Lepidoptera 0.20 1.01 3.89 3.93
Plecoptera 0.39 2.02 0.19 0.39
Acarina 0.20 1.01 0.33 0.33
Araneae 0.98 3.03 1.68 5.10
Oligochaeta 0.20 1.01 0.30 0.31
Total 510 99 12.86 cm3
75
fissipes.
Formicidae N F V AI
Centromyrmex sp. 0.45 4.17 0.46 1.90
Lasius niger 9.80 14.58 8.96 130.73
Paratrechina sp. 7.13 6.25 4.49 28.03
76
4.4.4 Stomach Contents of Microhyla heymonsi
Table 4.14 showed that M. heymonsi consumed 16 type of prey items consisted
of 476 prey. In this study, this anuran preyed dominantly on insects (97.69% of total
diet, Fig. 4.5), and was a predator of pests (96.43%, Fig. 4.6). Formicidae appeared to
be the dominant prey items of M. heymonsi (N=445, F=38, V=3.98 cm3, AI=4653.76).
Mean prey consumed by M. heymonsi was 10.82 ± 2.18 prey items. The
average prey consumed by males was 11.93 ± 3.13 prey items and the average prey
consumption of females was 8.67 ± 2.07 prey items were not significantly different
(Mann-Whitney U=210.5, P=0.8679). Maximum prey consumption of one frog was
66 prey by a male M. heymonsi and 20 prey by a female. The average prey variety per
stomach of this species was 1.47 ±0.11 prey items. Male M. heymonsi (mean=1.59 ±
0.14) and female M. heymonsi (mean=1.27 ±0.15) preyed on similar type and the same
variety of prey (Mann-Whitney U=164, P=0.1372). Both males and females had a
maximum prey variety of 3 prey items per stomach. Mean prey volume per stomach
was 110.7 ±18.3 mm3. There was no significant difference (Mann-Whitney U=172.5,
P=0.2712) in the mean prey volume of male (mean=132.6 ±26.0 mm3) and female M.
heymonsi (mean=68.24 ±14.2 mm3).
For prey items under the family Formicidae, the most dominant ants were ants
of subfamily Formicinae, Black garden ants (Lasius niger), Big-headed ants (Pheidole
megacephala), and Crazy ants (Paratrechina sp.), in that order (Table 4.15).
77
Microhyla heymonsi.
Taxa N F V AI
Bostrichidae 0.63 3.08 1.540436 4.739
Chrysomelidae 0.21 1.54 1.497647 2.304
Coccinellidae 0.21 1.54 1.497647 2.304
Tenebrionidae 1.05 3.08 6.221652 19.143
Culicidae 0.21 1.54 0.12837 0.197
Baetidae 0.42 3.08 0.770218 2.369
Pentatomidae 0.21 1.54 0.240693 0.370
Formicidae 93.49 58.46 79.60 4653.758
Plecoptera 0.42 3.08 0.256739 0.789
Acarina 0.21 1.54 0.12837 0.197
Araneae 1.26 9.23 3.163778 29.204
Tetranychoidae 0.63 4.62 1.045296 4.824
Diplopoda 0.21 1.54 0.36104 0.555
3
Total 476 65 4.87 cm
heymonsi.
Formicidae N F V AI
Centromyrmex sp. 0.22 2.63 0.20 0.53
Lasius niger 9.66 18.42 7.90 145.56
Paratrechina sp. 8.99 10.53 6.45 67.90
78
4.4.5 Stomach Contents of Polypedates leucomystax
Polypedates leucomystax of this study fed on a relatively narrow spectrum of
prey items, 48 prey of 12 prey categories were identified from the stomach contents of
this frog (Table 4.16). The greater part of P. leucomystax diet was insects (Fig. 4.5),
however, only a little more than half of its diet composed of pests (Fig. 4.6).
Importance index indicated that the dominant prey items of this frog were snout moths
(Pyralidae), leaf beetles (Chrysomelidae), termites (Termitidae), and wasps
(Platygasteridae), in order of descending importance. In terms of number, ants
(Formicidae) were the most numerous prey items found in the stomach contents of P.
leucomystax. On the other hand, snout moths were the most commonly encountered
prey items, followed, in a tie, by leaf beetles and wasps.
Mean prey consumption of P. leucomystax was 1.96 ±0.42 prey items per frog,
with no significant difference (Mann-Whitney U=59.50, P=0.9167) between males
(mean=2.11 ± 0.57) and females’ consumption (mean=1.57 ± 0.37). Maximum prey
consumed by a male P. leucomystax was 10 prey items, whereas the maximum prey
consumed by a female was only 3 prey items. Mean prey variety per stomach was 1.08
± 0.06 prey items. Females (mean=1.14 ± 0.14) and males (mean=1.06 ± 0.06) prey
variety were very similar (Mann-Whitney U=57.50, P> 0.9999). Maximum prey
variety of both sexes was 2 prey items. The average total prey volume was 322.5 ±
79.51 mm3. No significant difference between males (mean=325.7 ± 100.4 mm3) and
females (mean=314.3 ± 219.9 mm3) was found using Mann-Whitney test (Mann-
Whitney U=62.50, P=0.9879).
Since ants were not the main diet, Centromyrmex sp. (N=1, F=1, V=25.00
mm3), Harpegnathos sp. (N=9, F=2, V=225.00 mm3) and a few ants from subfamily
79
Formicinae (N=3, F=1, V=37.50 mm3) were the only ants consumed by the specimens
in this study.
Polypedates leucomystax in this study.
Taxa N F V AI
Termitidae 20.41 3.70 23.26 86.13
Carabidae 2.04 3.70 0.31 1.15
Chrysomelidae 10.20 14.81 12.40 183.75
Staphylinidae 2.04 3.70 3.57 13.21
Muscidae 4.08 7.41 3.10 22.97
Pentatomidae 4.08 7.41 0.31 2.30
Formicidae 26.53 14.81 3.57 52.81
Lepidoptera 2.04 3.70 6.20 22.97
Pyralidae 14.29 18.52 30.39 562.73
Araneae 2.04 3.70 1.24 4.59
Total 49 27 8.06 cm3
80
4.5 Mouth Width and Its Effect on Size of Prey
After controlling for SVL, the anuran’s maturity stages did not affect the prey
volume (F=2.059, df=4, P=0.0595). Pearson product-moment correlation test on MW
versus VMAX of D. melanostictus showed a moderate positive correlation, indicating
that there is a tendency for high VMAX with high MW, and vice curse (r=0.5883,
df=72, t= 6.1738). Test on MW versus VMIN showed a weak positive correlation (r2=
0.163, df=72, t= 3.7439). Linear regression of VMAX versus MW and VMIN versus
MW is plotted in Figure 4.7. Correlation test on all three microhylids indicated that
MW had no effect on both VMAX (Fig. 4.8) and VMIN (Fig. 4.9). Since there was
less than 10 specimens of P. leucomystax with at least three prey items, Pearson
product-moment correlation test was not run on this species.
400
VMAX
350 VMIN
Linear (VMAX)
300
Linear (VMIN) R²= 0.3461
250
Volume (mm3)
200
150 R²= 0.163
100
50
0
5 10 15 20 25 30
MW (mm)
Figure 4.7 Scatterplot of MW versus prey volume of Duttaphrynus melanostictus,

showing the linear regression (VMAX: y=11.71x – 52.36; VMIN: y=5.748x – 22.62)
81
140
M. heymonsi
120 M. fissipes
M. butleri
100
VMAX (mm3 )
80
60
40
20
0
3 4 5 6 7 8
MW (mm)
Figure 4.8 Combined scatterplot of MW versus VMAX of Microhyla butleri (M.b),
Microhyla fissipes (M.f) and Microhyla heymonsi (M.h).
80
M. heymonsi
70 M. fissipes
60 M. butleri
50
VMIN (mm3 )
40
30
20
10
0
3 4 5 6 7 8
MW (mm)
Figure 4.9 Combined scatterplot of MW versus VMIN of Microhyla butleri (M.b),
Microhyla fissipes (M.f) and Microhyla heymonsi (M.h).
82
4.6 Diversity Index, Niche Breath and Niche Overlap
Based on the Shannon Diversity Index, P. leucomystax had the highest prey
diversity, followed by D. melanostictus, M. butleri, M. fissipes and M. heymonsi, in
that order (Table 4.17). As for the niche breadth, P. leucomystax had the broadest
dietary niche breadth, followed by D. melanostictus, M. fissipes, M. heymonsi and M.
butleri, in descending order. There were also substantial dietary overlaps among the
five species of anurans, and the degree of dietary overlap according to Pianka’s
measure of overlap was presented in Table 4.17.
Table 4.17 Diversity index (H’), niche breadth (B), standardized niche breadth (B A),
and niche overlap (O) of specimens.
NICHE O
n H’ B BA D.m M.b M.f M.h P.l
D.m 41 2.12 15.297 0.357 -
M.b 24 1.33 4.078 0.133 0.660 -
M.f 26 1.33 7.821 0.272 0.672 0.888 -
M.h 18 0.82 5.395 0.258 0.608 0.788 0.943 -
P.l 13 2.29 9.388 0.699 0.425 0.085 0.200 0.164 -
Note: D.m=Duttaphrynus melanostictus, M.b=Microhyla butleri, M.F=Microhyla

fissipes, M.h=Microhyla heymonsi, and P.l=Polypedates leucomystax.
83
CHAPTER 5
Discussions
5.1 Basic Morphometry of the Five Anurans
The body size of all five anurans in this study falls within the size range of
these anurans sampled by other studies (Berry, 1975; Norhayati et al., 2009). More
than half of the D. melanostictus were considered sub-adults, and 80% of these sub-
adults were collected from Site USM. The most likely reason for the smaller size of
toad in this location may be the bimonthly trimming of weeds and grass. The lack of
tall grass means less cover from predators (i.e. birds) and direct exposure to the
elements (i.e. sunlight, wind, rain, etc.). Larger toads are more vulnerable in such
habitat as they have lesser shelter and are more visible.
Most of M. butleri and M. fissipes of this study were determined as sub-adults
according to the size range by Norhayati et al. (2009). However, some of these “sub-
adults” were captured during amplexus, and some females even carry eggs (seen
through the translucent ventral skin). Regardless, since this study does not study the
maturity stages of the frogs, size range by Norhayati et al. (2009) was followed to
avoid confusion. Further studies are required to review the adult size ranges of these
two species.
Specimens of P. leucomystax that show secondary sex characteristics were
treated as adults, as there is yet any study on the SVL of the species. Thus, a thorough
study on the maturity stages and size range of the frog is greatly required to better
understand this species.
84
Since MW is positively correlated to SVL of the anuran, specimens with larger
SVL have larger MW (Hirai & Matsui, 2000a; Toft, 1980a). The MW of D.
melanostictus and P. leucomystax are about a third of their SVL, whereas for the
narrow-mouthed microhylids, their MW are only about a quarter of their SVL.
Wilbur (1977b) stated that both food and density had significant effects on
growth rate and body size. Thus, the heavier the anuran is, the more likely that it will
grow larger in size. Findings of this study conform to the statement. Males D.
melanostictus in this study were heavier than their female counterparts, and their size
were relatively larger than the females, whereas females of M. heymonsi and P.
leucomystax were heavier and larger in size. For M. butleri, while there is no sex
weight bias, the relationship between body mass and SVL is positively correlated. The
only inconsistency is M. fissipes, in which the males were found to be heavier than the
females. Many factors may have contributed to this inconsistency, though the small
sample size of female M. fissipes may have been the primary reason of the skewness.
In natural populations, body size decreases with density as if food were in short supply
(Wilbur, 1977a).
85
5.1.1 Sexual Dimorphism of the Anurans
Sexual dimorphism is one of the factors that allows the autonomous living of
an organism, as such is the case of many amphibians. Many studies have shown size
differences between sexes of anurans, with females typically larger than males (Berry,
1975; Ibrahim, 2004; Norhayati et al., 2009; Shine, 1979; Van Sluys et al., 2006;
Woolbright, 1983). Shine (1979) reported that females grow larger than the males in
90% of anurans. Findings of this study, on M. heymonsi and P. leucomystax conform
to the general assumption and previous studies. Larger female in M. heymonsi agrees
with the findings of Woolbright (1983) that species that breed explosively tend to have
female-biased sexual size dimorphism. This female-biased sexual size dimorphism is
due to fecundity selection. Although Woolbright (1983) argued that energetic
constraints on reproductive males, caused by the costs of advertising, maintaining
territories, and lowering food intake, can affect body size.
Result of the body size of D. melanostictus of the study shows opposite result
than those of Gramapurohit & Radder (2012), with females found to be statistically
larger than the males. However, as mentioned by Gramapurohit & Radder (2012),
operational sex ratio was skewed in the favour of males, as successful males were
larger in length than their unsuccessful competitors. Hence, this may explain the larger
size of the males. Shine (1979) also reported that larger male size is common in species
that are relatively invulnerable to predation by virtue of large body size or toxic skin
secretions.
86
5.2 Specimens Availability According to Study Sites
As the five anuran species studied are disturbed area species, they are more
readily available in more disturbed areas (Table 4.4). In fact, result showed that the
more disturbed an area was, the more individuals and more species were to be found
in the area. As untouched areas are generally believed to have a larger habitat diversity
and more species (Graae & Heskjar, 1997), study sites grouped as “slightly disturbed
areas” had higher species diversity than those of “moderately disturbed areas”.
Although the number of target specimens found in slightly disturbed areas were low
possibly due to the presence of non-target specimen frogs, such as Fejervarya
cancrivora and Fejervarya limnocharis, which shared similar niche in the habitat.
Aside from disturbance, many other factors affect the prevalence of a disturbed
area species in the study site, such as the presence of trees, climate, and the presence
of other frogs (which were not categorised as common disturbed area species in this
study). The most apparent case in this study was shown by Polypedates leucomystax,
in which it was only found in study sites that had tall vegetation. The significantly low
number of specimens from all three sites from Langkawi was a direct result from the
long drought that had gripped the island throughout the month of January 2014, as
amphibians are especially susceptible to the lack moisture in the environment (Ibrahim,
1996).
87
5.3 Prey Availability of study Sites
Invertebrates available as prey to the amphibians was represented by Table 4.5,
although it may not truly reflect the availability of prey items of the study sites, due to
the limitation of glue traps on trapping non-flying insects. Despite being poorly
represented in Table 4.5, Formicidae are the most abundant terrestrial and arboreal
insects in the tropics (Lee, 2002; Rizali et al., 2008). As the glue traps were placed on
ground at the study sites, prey that were available to the anurans (especially to P.
leucomystax) which were hiding among the bushes and vegetation, was missed by the
glue traps. Thus, the findings in Table 4.5 was used only as a reference and was not
able to accurately reflect the prey availability.
88
5.4 Diet
All five species of anurans in this study fed on arthropods almost exclusively.
It is also worth noting that all of the common invertebrates recorded in the studies done
in the area where the frogs were collected were also present in the diets of the anurans.
Ants (Formicidae) and spiders (Araneae) were identified in the diets of all five species
of anurans, ranging from 26% to 94% (ants) and 1 to 2% (spiders) of the total items
consumed. This result conforms to previous studies of Toft (1980, 1981), which
concluded that tropical anurans that forage widely rely largely on ants and termites as
prey. The omnipresence of ants in the stomach contents of anurans in this study is on
the account of the fact that ants are the most abundant terrestrial and arboreal
arthropods in the tropics (Lee, 2002; Rizali et al., 2008) and that they are small-sized
prey available for predators of any size.
However, most species of spiders are limited to high elevation habitats and not
likely to be a major component of the ground-dwelling toad and frogs’ diet (with the
exception to P. leucomystax) within their present distribution. The second most
frequently collected insects from the environment were gnats (Cecidomyiidae), which
only infrequently appeared in the diet of D. melanostictus, M. butleri and M. fissipes.
The most plausible reason for this outcome is that four of the anuran species (with the
exception of P. leucomystax) in this study are terrestrial, therefore their diet would
naturally be the prey items that were encountered on the ground. Another aspect that
could affect the diet preferences of the anurans is activity patterns (Freed, 1980). The
anurans in this study were primarily nocturnal, as such, it is assumed that anurans are
primarily predators of nocturnal terrestrial arthropods.
89
When almost completely digested, only head capsule of ants and termites that
form the larger part of stomach contents of the anurans remained in the stomachs. In
case of other insects, heads, tegmina, elytra and other associated parts of exoskeleton
that were indigestible were left in the stomachs. Soft bodied animals (such as
caterpillars, slugs and isopods), if eaten by the anurans, may be under represented in
an almost digested stomach, as they do not have indigestible parts and would not leave
a trace (Jamdar & Shinde, 2013).
The inorganic materials, plant materials, and debris present among the diet of
the anurans may have been ingested incidentally along with the prey. The presence of
stones and plant matter in the stomach contents of anurans has been reported by earlier
studies of anurans’ feeding analyses (Berry & Bullock, 1962; Dietl et al., 2009;
Ibrahim & Nurul Dalila, 2008; Ibrahim, 2004; Santos et al., 2004; Toft, 1980a; Yap &
Ibrahim, 2012). Despite the high occurrence of plant materials in the diet of D.
melanostictus, it seems not to be the case of herbivory, as all of the ingested plant
materials were observed to be detritus. It is quite possible that the ingestion of
inorganic materials, such as stones and sand grains, aids the mechanical breakdown of
food in the stomach (Santos et al., 2004). Anderson et al. (1999) speculated that plant
contents may help in the elimination of intestinal parasites, or provide nutrients and an
additional source of water. There is also the possibility that fallen grains, seeds, flower
buds are probably mistaken for food (Ates et al., 2007; Jamdar & Shinde, 2013; Solé
et al., 2009; Yap & Ibrahim, 2012). Nonetheless, information on plant consumption
may also contribute to the understanding of behavioural patterns of the anuran.
90
5.4.1 Diet of Duttaphrynus melanostictus
Toads from the family Bufonidae are commonly thought to be non-
discriminatory predators that feed exclusively on the ground with arthropods being
their dominant prey item (Berry, 1965; Duellman & Trueb, 1986; Salahuddin et al.,
1990; Toft, 1981). The diet of this toad consisted of invertebrates; no vertebrate prey
were encountered in the stomach contents. Corresponding to the findings of Berry &
Bullock (1962) and Jamdar & Shinde (2013), Duttaphrynus melanostictus is not found
to ingest vertebrate prey. Hence, the discovery of a Brahminy blindsnake
(Ramphotyphlops braminus) in a D. melanostictus by O’Shea et al., (2013) was indeed
a rarity. Results from this study also indicated that this toad is primarily insectivorous.
Furthermore, representations from a wide spectrum of prey taxa from diverse habitats:
terrestrial, aquatic and agricultural ecosystems, showed the affinity of D. melanostictus
to a wide range of habitats.
This study reaffirms that D. melanostictus is a natural predator of various insect
pests especially phytophagous pests, indicating its usefulness as a biological control
agent. Duttaphrynus melanostictus fed on beetles, ants, snails, and most of the
arthropods that are harmful to crops (88.40% of ingested prey are pests). In this study,
one specimen of D. melanostictus consumed as much as 114 individuals of fire ants
(Solenopsis geminata), which is not only known to damage seedlings of vegetables
crops, but also a notorious pest that give painful sting that sometime proven to be fatal
(Havaldar et al., 2011). Many other Bufonidae species have been proven as effective
biological control agents in controlling of agricultural pests, for examples, Rhinella
marina (Takano, 1940), Duttaphrynus stomaticus (Battish et al., 1989), and
Duttaphrynus melanostictus (Berry & Bullock, 1962). With its worldwide distribution,
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D. melanostictus is a useful amphibian for the control of arthropod pests and thus,
plays a crucial role in the economy of nature.
Although this is the first study that tried to compare the dietary composition
between male and female D. melanostictus, the result showed that there is no sex
differences in dietary preferences (Appendix 7). Both sexes equally preyed on ants as
their most dominant prey and ground beetles as the second most dominant prey items.
None of the sexes showed any favouritism towards any particular type of prey.
When the relative abundance of potential prey in the environment was
compared to the abundance of prey items in stomach contents, D. melanostictus took
some prey taxa in different proportions from the availability in the environment. Over
representation of ants and ground beetles in the diet suggests this species of toad
preferred these prey items, which is also supported statistically using Jacob’s electivity
index (Dants=0.72, Dbeetle=0.87). Prey selectivity, and prey availability affect the
amphibian’s predation strategy. In the case of D. melanostictus of present study, this
species can be concluded as a generalist feeder with a strong affinity to ants. The result
of this study on D. melanostictus conformed to the many previous studies on toads
from family Bufonidae (Berry & Bullock, 1962; R. D. Clarke, 1974; Hirai & Matsui,
2002; Jamdar & Shinde, 2013).
The preference for ground beetles might be due to their profitability, as prey
from this taxon have large bodies and higher nutritional value (Olson, 2011). Generally,
ants and carabid beetles are unpalatable to many predators due to their high level of
formic acids and quinones (Daly et al., 2002; Daly et al., 2005; Saporito et al.,
2007).While Dendrobatids incorporate the noxious chemicals produced by such
arthropods into their own defensive mechanisms to ward off predators, thus selectively
92
prey on such invertebrates, further study is required to be certain of such claim in D.
melanostictus (Clark et al., 2005; Daly et al., 2002; Saporito et al., 2007). Nevertheless,
skin secretions of Duttaphrynus melanostictus possess hypotensive, cardiotoxic,
neurotoxic compounds that may cause death (Das et al., 2000). Clarke (1974)
suggested that this type of food habits that exploited prey unpalatable for other
predators, and reducing dietary competition with other insectivorous predators,
accounted for the worldwide success of toads from the genus Bufo. The same
explanation might hold for the worldwide distribution of D. melanostictus.
Toads are reported to be carnivorous and often times cannibalistic by
Boulenger (1900), Noble (1954) and Pizzatto & Shine (2008). In this study on D.
melanostictus, one female specimen were found with three conspecific eggs in its
stomach. Though it is not known whether the ingestion of the eggs were purely
accidental or on purpose, it is worth noting that the eggs were found among other
consumed terrestrial arthropods and some plant materials. This study is also the first
to report D. melanostictus consumption of its own shed skins. Three of the specimens
had (possibly its own) shed skins among their flushed stomach contents, while one
specimen apparently ate nothing but its own shed skins. This event does not seem to
be triggered by the lack of food as environmental prey is abundant, and other toads
that are caught at the same time in the same habitat have had fed. It is possible that this
epidermal protein recycling occurs as the shed skins contain some nutritional value.
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5.4.2 Diet of Microhylids
The result of this study shows that Microhyla butleri, Microhyla fissipes and
Microhyla heymonsi feed exclusively on the ground, as their prey items are terrestrial
and most taxa are fossorial or semi-fossorial. Even though most frogs were thought to
be opportunistic feeders, and that the majority of litter anurans do not specialize on
ants and mites (Simon & Toft, 1991), present study shows differently. All there species
of microhylids show a high affinity towards ants, similar to the results of many other
previous studies (Berry, 1965; Erftemeijer & Boeadi, 1991).
Toft (1980) stated that many species from the families Bufonidae,
Microhylidae and Dendrobatidae are specialists, characterized by the preference of
some arthropods. Such is the case for Microhyla butleri, M. fissipes and M. heymonsi
in this study, as ants made up the majority of prey items and were selected in far higher
proportions than those available in the environment (D=0.93, 0.94 and 0.97,
respectively). The high selectivity of ants indicates that all three microhylids studied
are “ant-specialists”. These ant-specialists also took a variety of other prey items,
including spiders, beetles, mites, small orthopterans and small lepidopteran. Diet
compositions of microhylids were mainly smaller types of prey, limited by their small
size and narrow mouth width.
The reason behind this is because ants present low costs of search and pursuit
effort, as ants are small in size, usually aggregated in high numbers, and are slow-
moving relative to the microhylids. Hence, in the optimal theory of foraging (Pyke,
1984), ants present easy targets. On the other hand, due to their small size and large
surface-to-volume ratio, ants contain a relatively high proportion of chitin (especially
of the head), which reduces the profitability of ants as prey (Olson, 2011; Simon &
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Toft, 1991). Ants constituted volumetrically less than 1 % of the diet individually. This
high selectivity for ants suggests that ants have some qualities (i.e. nutritional value)
that is not evaluated quantitatively in volumes.
Specialization in feeding and foraging is a well-known major trigger for
evolutionary novelty and adaptive radiation (Streelman & Danley, 2003). Some
anurans, like the dendrobatids and bufonids, incorporate the noxious chemicals, some
highly toxic alkaloids (pumiliotoxins), produced by ants and termites into their own
defensive mechanisms, and thus selectively prey on such invertebrates (Daly et al.,
2007; Daly et al., 2002; Simon & Toft, 1991). The potential that predation on ants by
Microhyla butleri, Microhyla fissipes, and Microhyla heymonsi may also play a role
in their defensive mechanisms should also be explored. A study on biologically active
substances from amphibians in Thailand involving M. heymonsi revealed that while
there were no lipophilic alkaloids found in the skins of the species, there was a slight
taste in the secretion indicating possible chemical defensive mechanism (Daly et al.,
2004).
In studies on a seemingly ant-specialist Plethodon cinereus, many scientists
found that red back salamanders switch away from more chitinous prey when other
more favourable prey are available, as simple optimal foraging theory would predict
(Pyke, 1984). More studies on the diet of Microhylids are required to fully understand
whether these trade-offs would occur if less chitinous prey were as abundant as ants
were in the environment. It is not possible to determine the food values of certain prey
items or if some prey items might serve some special physiological purpose or if others
might even have deleterious effects from the result of this study. Thus further study is
required to fully determine the functions and effects of prey items on the physiology
of the anurans.
95
It is possible that interspecific competition between these three cohabiting
species may be reduced by seasonal variation, whereby different species were more
abundant in different months of the year. Although, this is just a theory and more
studies are required to test the possibility, nonetheless, it is worth to note that these
microhylids are numerous in habitats with plenteous prey and are moisture rich, which
may reduce food competition as there is enough for everyone. Toft (1985) mentioned
that habitat rather than food choice tends to cause resource partitioning among
amphibians. Staudt et al., (2010) revealed that the toxic diet of strawberry poison frog
(Oophaga pumilio), which are formicine and myrmicine ants, may be linked to
territoriality.
Diet composition of these three microhylids also do not show any sex-biased
preferences. Nonetheless, statistically, male M. fissipes fed on more prey, and had a
wider prey spectrum than the females. Due to the lack of data, the true reason behind
this occurrence could not yet be determined. Further studies on the feeding analysis of
M. fissipes are required to solidify the dietary disparity between males and females.
Many studies on family Microhylidae revealed microhylids’ ant-specialists
diet (Berry, 1965; Erftemeijer & Boeadi, 1991; Hirai & Matsui, 2000a). Likewise this
study supports the conclusion of Hirai and Matsui (2000a) that members of the genus
Microhyla are ant-specialists. Attempts to reconstruct the evolution of myrmecophagy
in anurans have only been made within the frog family Dendrobatidae (Caldwell, 1996;
Toft, 1995). Nothing is known of the digestive physiology of anurans that specialize
on mites and ants (Simon & Toft, 1991). More detailed diet studies are needed in many
species within different phylogenetic lineages of amphibians, including microhylids,
to better understand the evolution of myrmecophagy in amphibians as a whole.
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5.4.3 Diet of Polypedates leucomystax
Although the limited sampling period and number of individuals could only
provide a preliminary estimation of the species actual dietary composition,
Polypedates leucomystax in this study shows an affinity to opportunistic feeding.
Despite the species relatively narrow range of prey categories (only 12 prey categories
identified), this species indicates no strong selectivity towards any type of prey items
(0.03<D>0.69), with the ants being the least preferred, and termites being the most
favourable prey. The overall spectrum of its prey consumption, lower number of prey,
and wide MW, all point to a generalist, “sit-and-wait” foraging strategy.
Among the five anurans studied, P. leucomystax consumed the most flying
insects (8 out of 12 prey categories), such as leaf beetles (Chrysomelidae), flies
(Muscidae), rove beetles (Staphylinidae), wasps (Platygasteridae), stink bugs
(Pentatomidae), damselflies (Coenagrionidae), snout moth (Pyralidae), and butterflies
(Lepidoptera). This may be a direct result of the microhabitat preference of the frog,
as P. leucomystax is arboreal species.
Termites eaten by specimens in present study were mainly soldiers. This may
be because as the frog come across a termite trail, soldier termites that rushed out to
defend the workers were devoured instead. Like any anuran that favour distasteful and
chitinous prey, such as termites, it is possible that P. leucomystax also incorporates the
arthropods toxic chemicals into its own predator defence. Daly et al. (2004) found that
the skin secretion of P. leucomystax has a slight taste with numbing effect on the
tongue. Additionally, widely foraging frogs often have toxins that apparently serve to
deter predators attracted by their movement (Toft, 1981). Green tree frog (Litoria
97
caerulea) produces toxic skin secretions to ward off infection and predation by
blowflies Calliphora stygia and Lucilia cuprina (Williams et al., 1998).
Ants may be among the dominant prey items of P. leucomystax because they
were the most abundant in study sites. By volume, this category of prey was not very
important food source, as it only comprised 3.57% of total volume. The high frequency
of hymenoptera found in the stomach of the frog can be associated with the fact that
there is a high amount of ants dominating the tropical vegetation (Rizali et al., 2008).
As Dietl et al. (2009) stated in their study, generally the availability of prey in the
habitat is an important element for predators with a limited feeding territory. Hence,
due to the richness of ants on the lower vegetation, they become the main dietary
composition of Polypedates leucomystax.
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5.5 Relationships of Morphology of the Anurans and Prey
Generally, a significant relationship between mouth width and prey sizes is
expected for frogs as they do not chew their prey, thus being restricted to eating items
that can fit in their mouths, although Simon & Toft (1991) argue that this relationship
depends on the prey taxon.
Statistically significant positive correlations of toad SVL and MW with prey
volume indicates that D. melanostictus may have selected prey large enough to
compensate the loss of energy involved in predation and ingestion (Hirai & Matsui,
2002). Similar to Hirai and Matsui’s study on Bufo japonicus, large adult D.
melanostictus in this study preferred coleopterans, followed by ants, whereas the
dominant stomach content of juvenile toads is ants. Larger toads overlooking smaller
prey that were preyed upon by smaller toads may have played a part in reducing the
intra-specific competition for food.
Mouth width did not affect prey size chosen by all three species of microhylids
of present study. The lack of a mouth size-prey size relationship in the microhylids of
this study could be resulting from the small range of body sizes and the small size of
the frogs, which also limits the size range of potential prey.
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5.6 Dietary Niches of the Anurans
The stronger the selectivity on a certain prey item by the frog, the smaller is
the niche breadth of the frog (Stamps et al., 2011). From this study, dietary niche
breadth of D. melanostictus (BA=0.357) indicates a weak specialization on certain prey,
P. leucomystax appears to be generalist (BA=0.699), while M. butleri, M. fissipes and
M. heymonsi show food specialization (BA=0.133, 0.272, 0.258, respectively).
Lima & Magnusson (1998) mentioned that competition for food can be avoided
through differences between the microhabitat exploited, type of food consumed, and
time of activity. In this study, microhabitat could only vary among the ground-dwelling
species at a small spatial scale, since they forage within a few meters from one another.
Van Sluys & Rocha (1998) reported that two syntopic frog species in the Amazon
overcome interspecific competition by the differences in their body size,
microenvironment exploration, and activity time.
Duttaphrynus melanostictus had a certain degree of dietary niche overlaps with
the three microhylids (M=1.278, 0.940, 1.024), due to their favouritism towards ants.
However, the interspecific competition was reduced by D. melanostictus preying on
larger ants, such as those from subfamily Myrmicinae, while the microhylids fed more
ants of subfamily Formicinae (with the exception of M. butleri, which also preferred
Myrmicinae). Duttaphrynus melanostictus was seen foraging during the day, although
more actively in the evening, a behaviour that may have contributed to the species
widely diverse diet.
On the other hand, P. leucomystax was very unlikely to compete for the same
food resource with the other four disturbed area species that coexisted in the same area.
This species fed on fast-moving flying insects that are infrequently chance upon by
100
ground-dwelling D. melanostictus, and prefers larger prey items that are too big for
the microhylids. Strictly speaking, the very low dietary niche overlap between P.
leucomystax and the other anurans may be the result of spatial segregation, an
important mechanism to reduce competition for resources, and the use of the habitat.
While all five species share the same water body for breeding, P. leucomystax usually
remains above the ground for other needs.
In spite of competitive exclusion principle stating that coexistence can occur
only if the species niches are different enough to limit competition between them
(Kalmykov & Kalmykov, 2013), the three microhylids of this study cohabit the same
habitat and share similar resources. Very high dietary niche overlaps between the
microhylids stems from their equally strong preference on ants. Hence, these species
influence each other’s population growth through interspecific competition. This can
be seen evidently from the samplings effort, as study site with high number of M.
butleri has fewer individuals of M. fissipes and M. heymonsi (site USM); while site
with more M. fissipes has lower number of the other two microhylids (site SB); sites
with many M. heymonsi has few other microhylids (site PSD, SD and BP).
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CHAPTER 6
Conclusions
In conclusion, this study on the five species of amphibians commonly found in
disturbed areas in northern Malaysia has shown that Duttaphrynus melanostictus,
Microhyla butleri, M. fissipes, M. heymonsi and Polypedates leucomystax are nature’s
biological control for pest insects (>90%), particularly of the ant species
(Hymenoptera, Formicidae). Overall, 42 prey categories were identified from the
stomach contents, with 14 of the prey families also found in the environment.
Platygasteridae, Formicidae and Araneae were the only prey families present in the
diets of all five anurans. The dominant prey items of D. melanostictus were ants and
ground beetles, while ants were the common most prevalent diet of the three
microhylids. Moths and leaf beetles formed the majority of P. leucomystax diet
composition.
Prey selectivity depends on the availability of the prey items in the environment.
Formicidae was the major diet of five anurans due to its abundance in the environment,
and that ants were the preferred prey of D. melanostictus, M. butleri, M. fissipes and
M. heymonsi. Duttaphrynus melanostictus is not really an ant-eating specialist, as it
consumed a relatively wide arrays of prey, although this species tends to lean towards
ant diet. The three microhylids are proven to be true ant-eating specialists, with
Formicidae making up more than 90% of their diet. Polypedates leucomystax is a
generalist feeder that eats what was chanced upon.
Duttaphrynus melanostictus consumed on average 8 prey items per meal
making up on average 696.1 mm3 in volume, and can chance upon on average 2
102
different types of prey every meal. On the other hand, P. leucomystax diet usually
consist of a single prey item, roughly the size of 322.5 mm3. Microhyla butleri has a
mean prey consumption of 11 prey per individual per meal, averaging at 151.6 mm3 in
volume, and usually feed on two different types of prey. Microhyla fissipes typically
feeds on 9 prey and volume up to about 238.2 mm3 per meal. Though, this species
sticks to only 1 to 2 types of prey on average. Meanwhile, M. heymonsi consumed 10
prey on average, usually about 110.7 mm3 in volume, and most of the time only on
one type of prey.
This study also concludes that the toads with larger mouth width will feed on
larger prey, although mouth width does not affect the overall prey volume ingested by
D. melanostictus. For the microhylids, mouth width has no effect on the prey size
selection, as the frogs have narrow mouths which limit their prey choice. Nonetheless,
the frogs compensate the lack of prey size by ingesting in a larger quantity. There were
not enough specimens of P. leucomystax to conclude the effect of MW on prey volume.
Different maturity stages does not affect the prey types, the body size of the anurans
seem to be the main reason of prey choice. The larger the size (SVL) of the anuran,
the larger the mouth width of the anuran, and thus larger prey can fit into the mouth.
There is also no sex difference in choice of prey. The weight of stomach contents did
not affect the body mass of both large-sized and small-sized anurans.
High diversity yet low niche breadth of D. melanostictus yet again indicates its
generalist feeding strategy with a priority for its favourite prey, the ants. Low niche
overlaps among the other four anurans and D. melanostictus indicates that the toad did
not suffer any interspecific competition for food resource. Polypedates leucomystax
generalist foraging strategy was shown by its high prey diversity and high niche
breadth, with half of its food resource shared by D. melanostictus. Niche overlaps show
103
that there is next to no food interaction between the three microhylids and P.
leucomystax. Microhyla butleri, M. heymonsi and M. fissipes had equally low prey
diversity and small niche breadth, typical of “ant-specialists”. These frogs compete
fervently among each other for the same food resource, that each species influences
the growth of the other two. To reduce the interspecific competition, there is spatial
segregation among the species, so that only one species will thrive at a local habitat.
The indiscriminating diet choice of toads from family Bufonidae, including D.
melanostictus in this study, is among the reason for their high survival and dispersal.
The use of different microhabitats in a local habitat ensures that P. leucomystax
included, are able to survive in various disturbed areas. The spatial segregation also
reduce interspecific competition with local species, allowing P. leucomystax to
disperse. Microhylids of the study thrives on the most abundant prey items on tropical
grounds, the ants, which sheer amount guaranteed the survival of the anurans.
This study contributes some understanding to the evolution of myrmecophagy
in amphibians as a whole. More studies are required to test the probability that the
species studied utilise the pumiliotoxins from chitinous insects, such as ants and
termites, for their own predator defence. The epidermal protein recycling of D.
melanostictus also needs to be further explored.
104
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Woolbright, L. L. (1983). Sexual Selection and Size Dimorphism in Anuran

Amphibia. The American Naturalist, 121(1), 110.
Yap, C. H., & Ibrahim, J. (2012). Feeding analysis of Hylarana cf. labialis,
Leptobrachium hendricksoni, and Occidozyga laevis (Amphibia: Anura) from a
lowland dipterocarp forest in Kedah, Malaysia. Herpetological Review, 43(1),
41–44.
117
LIST OF PUBLICATIONS
Yap C.H. and Ibrahim J, (2011) stomach content analysis of tropical forest toads
Ingerophrynus parvus and Phrynoidis aspera (Anura: Bufonidae) from Kedah,
Malaysia. Programme and Abstracts. Taxonomist and Ecologist Conference
2011, Univ. Malaysia Sarawak. Pp 31.
Yap C.H. and Ibrahim, J. (2012). Feeding analysis of Hylarana cf labialis,

Leptobrachium hendricksoni and Occidozyga laevis (Amphibia: Anura) from a
lowland dipterocarp forest in Kedah, Malaysia. Herpetological Review 43(1):
41-44 I.F. 0.68
Ibrahim Jaafar, Amirah Hurzaid, Shahriza Shahrudin, Nurhafizah Ibrahim, Zalina

Awang, Yap Chee Hui, Nurliza A Majid and NurHafizah Che Zaaba. (2013)
Additions to the herpetofauna of Jerejak Island, Penang, Peninsular Malaysia.
Malayan Nature Journal 64 (4): 213-232
Amirah H., Yap, C. H., Mohd Azmeer A. B., Ahmad R. Y. A. and Ibrahim J. (2013)
Diversity and density of amphibians at Sungai Enam, Temengor Forest
Reserve, Perak, Malaysia. In A. Latiff Mohamad eds. Proceedings of the 2nd
Temengor Scientific Expedition 2012. Pulau Banding Foundation. Pp 353-364
Yap C. H., Nurul Dalila A. R., Shahriza S., Ibrahim J. (2014) Feeding habits of River
Toad Phrynoidis aspera (Anura: Bufonidae) from lowland dipterocarp forest in
Kedah, Malaysia. Pensee Journal, 76(5):182-188.
Yap C. H., Zalina A., Amirah H., Belabus, D., and Ibrahim J. (2014) Diversity and
density of amphibians at Sungai Kampi, Pulau Pinang National Park, Penang,
Malaysia. Journal of Wildlife and Park 27:105-109.
Ibrahim J., Yap C.H., Amirah H. and Azmeer A. B. (2014) Amphibian density and
diversity in a disturbed habitat in Belum-Temengor Forest Complex, Perak,
Malaysia. Journal of Wildlife and Park 28:143-145.
118
APPENDICES
Appendix 1 Environmental parameters of study sites
Study
Longitude AL T RH
pH
Sites Latitude (m a.s.l.) (C) (%)
SB 520’56”N
3 26.6 ±0.9 78 ±5 6.23
10012’10”E
TRTB 526 ’47”N
39 23.6 ±0.8 80 ±2 5.64
10013’0”E
USM 521’28”N 78
16 24.0 ±2 6.42
10017’42”E ±12
PSD 5°28'5"N
3 26.9 ±0.4 80 ±1 4.27
100°26'12"E
KR 5°31' 42" N
18 27.3±1.0 70 ±2 6.12
100°39' 30"E
UP 523’39” N
77 26.3 ±0.6 86 ±3 5.81
10039’59”E
SD 525’11”N 27.0
203 82 ±11 5.27
10047’59”E ±1.2
BP 5°9' 32."N
27 24.8 ±1.2 86 ±4 5.21
100°32' 4"E
GLRP 437’40”N
46 28.0 ±0.5 80 ±2 5.13
1015’26”E
TT 622’13”N
16 26.9 ±0.6 78 ±3 5.65
9940’25”E
PK 622’14”N 25.6
9 73 ±2 6.26
9940’59”E ±1.2
UM 621’0”N
14 23.7 ±0.6 85 ±5 5.48
9946’15”E
Notes:
1. Longitude and latitude are based on Google Maps (2013).

2. AL=altitude; T=temperature; and RH=relative humidity.
3. All climate measurements were taken at night during samplings.
4. pH value indicated above is of surface soil pH.
Appendix 2 Flora and fauna observed at the study sites, with brief notes describing the sites.
Study
Vegetation Fauna Brief Note
Site
Rice (Oryza sativa), Blanket grass Cattle egret (Bubulcus ibis),
The study site is not actually in the muddy paddy
(Axonopus compressus), Panicum grass, White-throated kingfisher
SB, field, but the grassy patches along the deep drain
(Echinochola crus-galli), Sprangletop (Halcyon smyrnensis), House crow
Pulau and road running across the fields. There are also
(Leptochola chinensis), Lalang (Corvus splendens), Enhydris
Pinang jogging and cycling trails along the roads crossing
(Imperata cylindrica), Spermacoce plumbea, annelids, millipedes,
the paddy field.
exilis, Cowfoot grass (Eleusine indica) centipedes, insects
This study site is within Teluk Bahang Forest
Crab-eating macaque (Macaca
Thickhead (Crassocephalum Ecopark. It’s a camping and picnic site for family
fascicularis), House sparrow
crepidioides), Bird nest fern (Asplenium outdoor activities. There are also forest hiking
TRTB, (Passer domesticus), Smith's leaf-
nidus), Kassod tree (Senna siamea), trails and a stream running across. However,
Pulau toed hecko (Hemidactylus smithi),
Forked fern (Dicranopteris linearis), during the sampling, this ecopark has been closed
Pinang Eared-nightjar (Eurostopodus
Star apple tree (Chrysophyllum cainito), to public for 6 months due to detection of
temminckii), annelids, millipedes,
Cowfoot grass (Eleusine indica) Leptopirosis and presence of Leptospira bacteria
centipedes, insects
in the stream.
Common myna (Acridotheres
This study site consists of a small field
tristis), House sparrow (Passer
Blanket grass (Axonopus compressus), surrounding outdoor monkey bars with a 2 m2
USM, domesticus), East Indian brown
spurge (Euphorbia sp.), Smut grass cement pool base, which is part of the training area
Pulau mabuya (Eutropis multifasciata),
(Sporobolus indicus), Thickhead of USM PALAPES. Water in the pool is
Pinang House gecko (Hemidactylus
(Crassocephalum crepidioides) periodically change and constantly overflows from
frenatus), annelids, centipedes and
heavy rain.
insects
Appendix 2 (Cont’d)
Study
Site
Cattle (Bos sp.), Common myna As with site SB, this study sites is the grassy
Rice flatsedge (Cyperus iria), Cowfoot
PSD, (Acridotheres tristis), House crow patches along the deep drain and road running
grass (Eleusine indica), Jungle rice
Kepala (Corvus splendens), Great Egret across the fields. However, noise pollution at the
(Echinochloa colona), Willow herbs
Batas, (Ardea alba), Javan myna site is at times high due to overhead air force
(Jussiaea linifolia), coconut (Cocos
Penang (Acridotheres javanicus), annelids, airplanes, as the sky ahead is part of Royal
mucifera), Banana (Musa sp.)
millipedes, centipedes, insects Malaysia Air Force training area.
Windmill grass (Chloris barbata),

Forked fern (Dicranopteris linearis), Green garden lizard (Calotes This study site is along the deep ditch and grassy
KR, Blanket grass (Axonopus compressus), versicolor), Common myna road shoulder wedges between Jalan Batu Putih
Kedah Sleeping grass (Mimosa pudica), giant (Acridotheres tristis), annelids, and oil palm plantations. There is also a rubber
Sensitive plant (Mimosa diplotricha), millipedes, centipedes, insects plantation about 100m from the site.
Wild tea (Acalypha siamensis)
Cowfoot grass (Eleusine indica), Blue-winged pitta (Pitta

Wrinkle duck-beak (Ischaemum moluccensis), Malayan forest
The study site is along the hedges and grassy road
UP, rogusom), Buas-buas (Premna gecko (Cyrtodactylus pulchellus),
shoulder that runs along Sungai Kob. There is a
Kedah serratifolia), Blanket grass (Axonopus Wild boar (Sus scrofa), snail
thick large water pipe along the roadside.
compressus), Bemban (Donax (Family, Cyclophoridae),
grandis) centipedes, insects
Study
Site
Dusky leaf monkey (Trachypithecus
Bamboo (Bambusa sp.), cowfoot The study site is a small patch of grassy
obscurus), Great hornbill (Buceros bicornis),
grass (Eleusine indica), blanket clearing nearby the torrent river of Sungai
SD, insects, Blue-winged pitta (Pitta moluccensis),
grass (Axonopus compressus), Sedim. It is located in Gunung Inas Forest
Kedah Large forest gecko (Gekko smithii), snail
wild tapioca (Manihot glaziovii), Reserve, which is mainly a lowland
(Family, Cyclophoridae), Great anglehead
Dipterocarpus sp. dipterocarp forest.
lizard (Gonocephalus grandis)
Molinera latifora, Cowfoot grass
(Eleusine indica), Blanket grass Wagler’s pit viper (Tropidolaemus wagleri), This study site is within Bukit Panchor
(Axonopus compressus), yam Spiny terrapin (Heosemys spinosa), state park, located by the banks of Sungai
BP,
(Colocasia esculenta), Common Anglehead lizard (Gonocephalus grandis), Buaya, and part of Bukit Panchor forest
Kedah
water hyacinth (Eichhornia House sparrow (Passer domesticus), Wild reserve which is a lowland dipterocarp and
crassipes), Tongkat ali (Eurycoma boar (Sus scrofa) peat swamp forest.
longifolia), Shorea sp.
This study site is a parking area of GLRP,
Tiger’s tongue grass (Leersia
carp (Cyprinidae), cichlid (Tilapia sp.), thus the ground is mostly covered with
hexandra), Heliconia caribaea,
GLRP, Amboina box turtle (Cuora amboinensis), asphalt. It is adjacent to a man-made lake
Blanket grass (Axonopus
Ipoh, House sparrow (Passer domesticus), White- from former tin mine and the disrupted
compressus), Sleeping grass
Perak throated kingfisher (Halcyon smyrnensis), swampy landscape surrounding the lake.
(Mimosa pudica), Hedyotis
insects GLRP is located only 5 km from Ipoh
auricularia
town.
Study Site Vegetation Fauna Brief Note

White-throated kingfisher
Cowfoot grass (Eleusine indica), This study site consists of the joint of a wide
(Halcyon smyrnensis), Black-
TT, yam (Colocasia esculenta), drain (from the nearby recreational park) and
naped oriole (Oriolus
Langkawi, Kedah Common water hyacinth Sungai Perangin river to a wetland, and the
chinensis), House sparrow
(Eichhornia crassipes) immediate areas.
(Passer domesticus), insects
Drought grass (Ischaemum Located directly next to Perdana Quay, and
muticum), Windmill grass (Chloris opposite The Danna, this study site is a
cattle (Bos sp.), rat (Rattus sp.),
barbata), Cowfoot grass (Eleusine livestock (mainly cattle) grazing field framed at
PK, goat (Capra aegagrus hircus),
indica), Sensitive plant (Mimosa its 3 sides by wide drains and asphalt road.
Langkawi, Kedah annelids, millipedes,
sp.), Lalang (Imperata cylindrica), While human presence here is moderately low,
centipedes, insects
Blanket grass (Axonopus the field is considered highly disturbed due to
compressus) the sheer number of livestock.
Cowfoot grass (Eleusine indica),
Located directly next to the main road, this
Blanket grass (Axonopus
Paddyfield pipit (Anthus study site is a small barren field among the
UM, Langkawi, compressus), Windmill grass
rufulus), millipedes, centipedes, paddy fields. At the time of sampling, there was
Kedah (Chloris barbata), Tapioca
insects a long drought in Langkawi, drying up the tall
(Manihot esculenta), Aglaia
grasses and weeds in the site.
duperreana
Notes: The vegetation and fauna noted were just a few examples of the biodiversity at the study sites that were observed and recorded during
samplings.
Appendix 3 Stomach contents of anurans expressed as percentage of total body weight
with respect to sex.
Anuran Species Overall (%) Male (%) Female (%)

D. melanostictus 0.35 0.34 0.40
P. leucomystax 0.31 0.52 0.15
M. butleri 4.12 4.07 4.23
M. fissipes 2.52 3.12 1.65
M. heymonsi 3.80 2.06 1.25
Appendix 4 Pearson product-moment correlation test result of MW versus VMAX

of Microhyla butleri (M.b), Microhyla fissipes (M.f) and Microhyla heymonsi (M.h).
PPMCC
Pearson’s r r2 t-test df p-value p-value
(2-sided) (1-sided)
M.b 0.0961 0.0092 0.7413 59 0.4614 0.2307
M.f -0.0561 0.0031 -0.3276 34 0.7452 0.3726
M.h -0.1174 0.0138 -0.6477 30 0.5221 0.2610
Appendix 5 Pearson product-moment correlation test result of MW versus VMIN of

Microhyla butleri (M.b), Microhyla fissipes (M.f) and Microhyla heymonsi (M.h).
PPMCC
Pearson’s r r2 t-test df p-value p-value
(2-sided) (1-sided)
M.b 0.0763 0.0058 0.5881 59 0.5587 0.2793
M.f 0.0901 0.0081 0.5275 34 0.6012 0.3006
M.h -0.0404 0.0016 -0.2214 30 0.8263 0.4131
Appendix 6 Examples of prey items from the stomachs of anurans.
Appendix 7 Prey composition of male and female D. melanostictus.
Male Female
Taxa N F V% AI N F V% AI
Blattellidae 3 2.78 2.52 6.99 1 0.88 1.07 0.95
Termitidae 17 4.63 4.85 22.45 0 0.00 0.00 0.00
Bostrichidae 1 0.93 0.04 0.04 1 0.88 0.05 0.05
Carabidae 39 16.67 17.75 295.76 46 9.73 26.74 260.27
Chrysomelidae 4 2.78 1.48 4.10 4 3.54 1.88 6.67
Coccinellidae 0 0.00 0.00 0.00 2 1.77 1.21 2.15
Dytiscidae 1 0.93 0.50 0.46 0 0.00 0.00 0.00
Scarabaeidae 1 0.93 0.38 0.35 0 0.00 0.00 0.00
Staphylinidae 0 0.00 0.00 0.00 3 0.88 1.12 0.99
Tenebrionidae 3 1.85 0.77 1.43 17 6.19 5.60 34.72
Carcinophoridae 8 4.63 2.26 10.46 4 3.54 1.44 5.11
Cecidomyiidae 0 0.00 0.00 0.00 4 2.65 0.99 2.62
Muscidae 0 0.00 0.00 0.00 1 0.88 0.87 0.77
Baetidae 0 0.00 0.00 0.00 1 0.88 0.18 0.16
Alydidae 7 4.63 1.67 7.71 0 0.00 0.00 0.00
Coreidae 5 2.78 1.46 4.06 1 0.88 0.37 0.33
Gerridae 0 0.00 0.00 0.00 1 0.88 0.03 0.03
Pentatomidae 1 0.93 0.05 0.05 1 0.88 0.07 0.06
Platygasteridae 1 0.93 0.37 0.35 3 1.77 1.43 2.54
Formicidae 474 33.33 54.06 1802.05 190 28.32 30.95 876.59
Lepidoptera 0 0.00 0.00 0.00 4 3.54 2.21 7.82
Crambidae 0 0.00 0.00 0.00 1 0.88 0.88 0.78
Pyralidae 4 1.85 1.99 3.69 5 1.77 3.18 5.63
Philopteridae 0 0.00 0.00 0.00 1 0.88 0.03 0.03
Coenagrionidae 0 0.00 0.00 0.00 1 0.88 0.39 0.35
Gomphidae 1 0.93 0.75 0.69 1 0.88 0.95 0.84
Tetrigidae 2 0.93 1.49 1.38 2 1.77 1.91 3.37
Gryllidae 4 3.70 1.28 4.75 1 0.88 0.41 0.36
Siphonaptera 0 0.00 0.00 0.00 2 1.77 0.58 1.03
Plecoptera 0 0.00 0.00 0.00 1 0.88 0.03 0.03
Acarina 0 0.00 0.00 0.00 1 0.88 0.10 0.09
Araneae 4 3.70 1.02 3.77 7 5.31 2.28 12.08
Tetranychoidae 1 0.93 0.26 0.24 1 0.88 0.34 0.30
Armadillidiidae 7 0.93 1.14 1.06 29 6.19 6.06 37.53
Chilopoda 0 0.00 0.00 0.00 5 2.65 3.77 10.00
Diplopoda 4 1.85 2.16 3.99 2 1.77 1.38 2.44
Oligochaeta 2 1.85 0.54 1.01 3 1.77 1.04 1.84
Gastropoda 2 1.85 0.29 0.53 0 0.00 0.00 0.00
Crustacea 1 0.93 0.41 0.38 0 0.00 0.00 0.00
Unidentified prey 3 1.85 0.51 0.95 2 1.77 0.44 0.77
2178.70 36.07
Total 600 cm3 349 cm3 1279.29
Appendix 8 Prey composition of male and female P. leucomystax.
Male Female
Termitidae 10 5.26 31.98 31.98 0 0.00 0.00 0.00
Carabidae 0 0.00 0.00 0.00 1 12.50 1.14 1.14
Chrysomelidae 4 15.79 13.65 40.94 1 12.50 9.09 9.09
Staphylinidae 0 0.00 0.00 0.00 1 12.50 13.07 13.07
Muscidae 2 10.53 4.26 8.53 0 0.00 0.00 0.00
Pentatomidae 2 10.53 0.43 0.85 0 0.00 0.00 0.00
Formicidae 10 15.79 4.26 12.79 1 12.50 1.70 1.70
Lepidoptera 0 0.00 0.00 0.00 1 12.50 22.73 22.73
Pyralidae 4 15.79 23.88 71.64 2 25.00 47.73 95.45
Coenagrionidae 2 10.53 8.53 17.06 0 0.00 0.00 0.00
Araneae 0 0.00 0.00 0.00 1 12.50 4.55 4.55
5.86 22.00
Total
38 cm3 8 cm3 147.73
Appendix 9 Prey composition of male and female M. heymonsi.
Male Female
Bostrichidae 3 4.55 1.95 8.87 0 0.00 0 0
Chrysomelidae 1 2.27 1.90 4.31 0 0.00 0.00 0.00
Coccinellidae 1 2.27 1.90 4.31 0 0.00 0.00 0.00
Tenebrionidae 5 4.55 7.88 35.81 0 0.00 0.00 0.00
Culicidae 1 2.27 0.16 0.37 0 0.00 0.00 0.00
Baetidae 2 4.55 0.98 4.43 0 0.00 0.00 0.00
Pentatomidae 1 2.27 0.30 0.69 0 0.00 0.00 0.00
Formicidae 320 54.55 76.98 4198.64 125 73.68 89.48 6593.07
Plecoptera 2 4.55 0.33 1.48 0 0.00 0.00 0.00
Acarina 1 2.27 0.16 0.37 0 0.00 0.00 0.00
Araneae 4 9.09 2.67 24.28 2 10.53 5.02 52.80
Tetranychoidae 2 4.55 0.88 4.01 1 5.26 1.66 8.72
Diplopoda 1 2.27 0.46 1.04 0 0.00 0.00 0.00
3.85 10.24
Total
346 cm3 130 cm3
Appendix 10 Prey composition of male and female M. butleri.
Male Female
Carabidae 2 0.94 0.97 0.92 8 7.69 6.51 50.10
Dytiscidae 2 0.94 1.19 1.13 0 0.00 0.00 0.00
Tenebrionidae 9 3.77 5.31 20.04 0 0.00 0.00 0.00
Cecidomyiidae 5 3.77 0.54 2.03 1 1.54 0.18 0.28
Culicidae 3 1.89 0.21 0.39 0 0.00 0.00 0.00
Baetidae 4 3.77 1.24 4.68 4 4.62 2.08 9.59
Alydidae 1 0.94 0.07 0.06 0 0.00 0.00 0.00
Gerridae 4 1.89 0.27 0.52 0 0.00 0.00 0.00
Pentatomidae 1 0.94 0.13 0.12 0 0.00 0.00 0.00
Formicidae 492 55.66 79.39 4419.09 267 69.23 83.20 5759.80
Crambidae 1 0.94 0.58 0.55 0 0.00 0.00 0.00
Philopteridae 0 0.00 0.00 0.00 1 1.54 0.63 0.97
Tetrigidae 1 0.94 0.56 0.53 0 0.00 0.00 0.00
Plecoptera 1 0.94 0.22 0.21 1 1.54 0.37 0.57
Acarina 1 0.94 0.14 0.14 1 1.54 0.24 0.37
Araneae 7 5.66 2.37 13.39 3 1.54 1.70 2.61
Tetranychoidae 4 3.77 0.78 2.96 1 1.54 0.33 0.50
Diplopoda 2 1.89 0.47 0.88 0 0.00 0.00 0.00
Oligochaeta 1 0.94 0.68 0.65 0 0.00 0.00 0.00
7.31 43.63 5839.77
Total
552 cm3 295 cm3
Appendix 11 Prey composition of male and female M. fissipes.
Male Female
Taxa N F% V% AI N F% V% AI
Termitidae 0 0.00 .000 0.00 1 3.45 5.55 19.12
Bostrichidae 1 1.52 0.24 0.36 1 3.45 0.67 2.31
Chrysomelidae 2 1.52 2.22 3.36 2 6.90 6.22 42.92
Coccinellidae 1 1.52 0.94 1.43 1 3.45 2.64 9.11
Dytiscidae 1 1.52 0.41 0.63 0 0.00 .000 0.00
Tenebrionidae 6 7.58 4.70 35.63 1 3.45 2.20 7.58
Carcinophoridae 4 4.55 1.95 8.84 0 0.00 .000 0.00
Cecidomyiidae 2 3.03 0.74 2.25 0 0.00 .000 0.00
Culicidae 3 3.03 0.62 1.87 2 3.45 1.15 3.98
Muscidae 1 1.52 0.16 0.25 0 0.00 .000 0.00
Baetidae 3 4.55 2.00 9.11 0 0.00 .000 0.00
Alydidae 2 1.52 0.26 0.40 0 0.00 .000 0.00
Coreidae 1 1.52 0.55 0.84 0 0.00 .000 0.00
Gerridae 1 1.52 0.38 0.58 0 0.00 .000 0.00
Formicidae 333 43.94 74.84 3288.29 100 55.17 53.91 2974.32
Coenagrionidae 3 3.03 1.11 3.37 0 0.00 .000 0.00
Acarina 1 1.52 0.44 0.67 0 0.00 .000 0.00
Araneae 4 3.03 1.83 5.53 1 3.45 1.28 4.41
Tetranychoidae 1 1.52 0.13 0.20 0 0.00 .000 0.00
Armadillidiidae 4 4.55 1.91 8.70 0 0.00 .000 0.00
Lepidoptera 0 0.00 .000 0.00 1 3.45 14.79 50.99
Plecoptera 0 0.00 .000 0.00 2 6.90 0.74 5.10
Oligochaeta 1 1.52 0.41 0.63 0 0.00 .000 0.00
Unidentified prey 2 3.03 0.26 0.80 0 0.00 .000 0.00
9.48 33.81
Total
379 cm3 3385.46 114 cm3 3194.68
Appendix 12 Animal ethics approval letter.
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Diet of Five Common Anurans Found In Disturbed Areas in Northern

Thesis · February 2015

Chee hui Yap

The user has requested enhancement of the downloaded file.

YAP CHEE HUI

A thesis submitted in fulfilment of the

I would like to express my utmost gratitude to my supervisor Prof. Ibrahim

boost my personal development and character building.

Also, many thanks to the members of my supervisory committee, for their

grateful to my family, for their unwavering support and encouragement.

Additionally, I would like to thank the School of Biological Sciences and

IPS Graduate Fund 1001/PJJAUH/834068 and USM Fellowship.

Table of Contents iii

List of Tables viii

List of Symbols and Abbreviations x

Abstrak (Abstract in Malay Language) xi

CHAPTER 2 - LITERATURE REVIEW

2.1 Amphibians in General 4

2.2 Habitat and Distribution 7

2.3 Anuran in General 8

2.4 Classification of Frog and Toad 15

2.5 Description of Specimens 17

2.6 Digestive System 26

2.7 Diet and Feeding Ecology 29

2.8 Food Availability 32

2.9 Species Niches 33

2.10 Ecological Roles of Amphibians 34

2.11 Amphibian Decline 37

3.1 Study Sites 39

3.2 Experimental Procedures 42

3.2.1 Collection of Specimens 43

3.2.2 Morphometric Measurements 45

3.2.3 Collection of Stomach Content 46

3.3.4 Data Analysis 47

4.1 Basic Morphology of Specimens 52

4.2 Specimen Availability According to Study Sites 58

4.3 Prey Availability of Study Sites 60

4.4 Stomach Contents of the Specimens 62

4.4.1 Stomach Contents of Duttaphrynus 68

4.4.2 Stomach Contents of Microhyla butleri 71

4.4.3 Stomach Contents of Microhyla fissipes 74

4.4.4 Stomach Contents of Microhyla heymonsi 77

4.4.5 Stomach Contents of Polypedates leucomystax 79

4.5 Mouth Width and Its Effect on Size of Prey 81

4.6 Diversity Index, Niche Breath and Niche Overlap 83

5.1 Basic Morphometry of the Five Anurans 84

5.2 Specimen Availability to Study Sites 87

5.3 Prey Availability of Study Sites 88

5.4.1 Diet of Duttaphrynus melanostictus 91

5.4.2 Diet of Microhylids 94

5.4.3 Diet of Polypedates leucomystax 97

5.5 Relationships of Morphology of the Anurans and Prey 99

5.6 Dietary Niches of the Anurans 100

CHAPTER 6 - CONCLUSIONS 102

List of Publications 118

Figure 2.1 External characteristics of frogs and toads.

Figure 3.2 Research flow chart.

Figure 4.1 Number of specimens collected, according to species

Figure 4.4 Empty versus non-empty stomachs, according to species.

Figure 4.7 Scatterplot of MW versus prey volume of Duttaphrynus

Figure 4.8 Combined scatterplot of MW versus VMAX of Microhyla butleri

Figure 4.9 Combined scatterplot of MW versus VMIN of Microhyla butleri