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Diet habits of frogs (Family: Megophryidae) in Kubah National Park

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The Megophryidae (commonly known as the litter frogs) is a large family of frog native to the warm southeast Asia. The aim of this study was to determine the diet choice of frogs in family Megophyridae and whether there is relationship between predator snout vent length and prey length. The present study has been conducted in a well-known hotspot for frogs in Kubah National Park comprising of primary rainforest. Frogs had been caught in the field and their stomachs were flushed and extracted. Stomach flushing method can be used for large and small size frogs while the stomach extracting method is used for smaller size frogs. The stomach content was be retrieved, sorted to prey categories and the diet was analyzed. The stomach contents were also analyzed and identified in laboratory using microscope. Based on the results, it is shown that the diet habits of frog in family Megophryidae were influenced by predator snout vent length as the bigger SVL consume the bigger length of prey. Keywords: diet, Megophryidae family, snout ventral length, stomach flushing, stomach extracting
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DIET HABITS OF FROGS (FAMILY: MEGOPHRYIDAE) IN KUBAH NATIONAL
PARK, SARAWAK, BORNEO
Muhamad Affan bin Ab Azid (45700)
Bachelor of Science with Honors
(Animal Resource Science and Management)
2017
Diet Habits of Frogs (Family: Megophryidae) in Kubah National Park, Sarawak, Borneo
Muhamad Affan bin Ab Azid (45700)
This project is submitted in partial fulfilment of the requirement for the degree of Bachelor of
Science with Honors
(Animal Resource Science and Management Program)
Faculty of Resource Science and Management
Universiti Malaysia Sarawak
2017
I
ACKNOWLEDGEMENT
Throughout this project, I have learnt many experiences and skills that I would never
forget. I would like to show my greatest appreciation to my supervisor, Madam Christharina S
Gintoron for her guidance and encouragement until the end of this project. Her patience and
understanding make me feel comfortable whenever I have lost my path throughout this project.
Next, I would also like to take this opportunity to thank AP Dr Ramlah binti Zainudin as
my co-supervisor. Without her opinion, I will not have any ideas about how to do flushing
method for diet studies. Other than that, I really appreciated her guidance through completing
the project.
Besides, I want to show my thankfulness to the postgraduate students for helping me
during the sampling period at the field and lab session. I never forget their kindness for guiding
me throughout the project. Along with me is my fellow friends because they are very supportive
who always concern about my projects. They help me to search information and compiled diet
data.
Finally, I would like to show my gratefulness to my beloved parents, Ab Azid bin Mat
Jusoh and Nazrini bt Mat Zain, who always gave me motivation and courage to finish my final
year project. I want to show my special gratitude to all my course mates for their companionship.
II
DECLARATION
I hereby declare that no portion of the work referred to in this thesis has been submitted in
support of an application for another degree or qualification to this or any other university or
institute of higher learning.
……………………………..
MUHAMAD AFFAN BIN AB AZID
Animal Resource Science and Management Program
Department of Zoology
Faculty of Resource Science and Technology`
Universiti Malaysia Sarawak
III
TABLE OF CONTENTS
Acknowledgement ......................................................................................
I
Declaration ..................................................................................................
II
Table of Contents ........................................................................................
III
List of Abbreviations ..................................................................................
IV
List of Tables and Figures ..........................................................................
V
Abstract .......................................................................................................
1
1.0 Introduction ...........................................................................................
2
1.1 Problem statement ..........................................................................
3
1.2 Objectives .......................................................................................
4
1.3 Hypothesis
4
2.0 Literature review ...................................................................................
5
2.1 Diversity of Megophryidae family in Borneo ................................
5
2.2 Ecosystem of Kubah National Park ................................................
7
2.3 Insects as prey .................................................................................
8
2.4 Importance of different diet ............................................................
9
2.5 Stomach flushing and stomach extracting method ........................
10
2.6 Previous studies of diet of frogs .....................................................
11
3.0 Materials and Method ...........................................................................
14
3.1 Sampling site ..................................................................................
14
3.2 Sampling method ............................................................................
16
3.2.1 Sampling and identification ...................................................
16
3.2.2 Stomach flushing method ......................................................
16
3.2.3 Stomach extracting method ...................................................
17
3.2.4 Stomach content analysis .......................................................
18
3.2.5 Statistical analysis ..................................................................
19
IV
4.0 Results ...................................................................................................
21
4.1 Frogs collected ................................................................................
21
4.2 Prey items .......................................................................................
22
4.3 Diet analysis ....................................................................................
22
4.3.1 Diet analysis of the frogs in Kubah National Park …………
22
4.3.2 Analysis of predator snout vent length and prey length ……
26
5.0 Discussion .............................................................................................
30
5.1 Frogs collected ................................................................................
30
5.2 Prey items .......................................................................................
31
5.3 Diet analysis ....................................................................................
31
6.0 Conclusion & recommendations ...........................................................
35
7.0 References .............................................................................................
36
Appendices .................................................................................................
39
Appendix 1 ...........................................................................................
39
Appendix 2 ...........................................................................................
42
Appendix 3 ...........................................................................................
43
Appendix 4 ...........................................................................................
43
Appendix 5 ...........................................................................................
44
Appendix 6 ...........................................................................................
44
Appendix 7 ...........................................................................................
45
Appendix 8 ...........................................................................................
46
V
LIST OF ABBREVIATIONS
KNP
Kubah National Park
SVL
Snout-vent length
HW
Head width
km
Kilometre
m
Metre
cm
Centimetre
ml
Milimetre
Ha
Hectare
m asl
Metre above sea level
sq-km
Square kilometer
IRI
Index of relative importance
VI
LIST OF TABLES
Table 1
Summary of previous studies of diet that use stomach flushing method
13
Table 2
Number of individuals of frogs collected at Kubah National Park, Sarawak
21
Table 3
Prey items of family Megophryidae
22
Table 4
Prey types in the diet of frogs from Kubah National Park: O, occurrence; %
O, percentage of occurrence; N, number of individuals; % N, percentage of
number individuals; V, volume in mm3; % V, percentage of volume; IRI,
index of relative importance (IRI), showed for each prey item.
24
VII
LIST OF FIGURES
Map of Kubah National Park
15
Stomach flushing apparatus
17
Stomach contents that preserved in 10% formalin
18
Regression between maximum prey length and predator
snout ventral length (SVL) of Leptolalax dringi
26
Regression between minimum prey length and predator
snout ventral length (SVL) of Leptolalax dringi
27
Regression between maximum prey length and predator
snout ventral length (SVL) of Leptolalax gracilis
28
Regression between minimum prey length and predator
snout ventral length (SVL) of Leptolalax gracilis
29
1
Diet habits of frogs (Family: Megophryidae) in Kubah National Park, Sarawak, Borneo
Muhamad Affan bin Ab Azid (45700)
Animal Resource Science and Management Program
Faculty of Resource Science and Technology
Universiti Malaysia Sarawak
ABSTRACT
The Megophryidae (commonly known as the litter frogs) is a large family of frog native to the warm southeast
Asia. The aim of this study was to determine the diet choice of frogs in family Megophyridae and whether there is
relationship between predator snout vent length and prey length. The present study has been conducted in a well-
known hotspot for frogs in Kubah National Park comprising of primary rainforest. Frogs had been caught in the
field and their stomachs were flushed and extracted. Stomach flushing method can be used for large and small size
frogs while the stomach extracting method is used for smaller size frogs. The stomach content was be retrieved,
sorted to prey categories and the diet was analyzed. The stomach contents were also analyzed and identified in
laboratory using microscope. Based on the results, it is shown that the diet habits of frog in family Megophryidae
were influenced by predator snout vent length as the bigger SVL consume the bigger length of prey.
Keywords: diet, Megophryidae family, snout ventral length, stomach flushing, stomach extracting
ABSTRAK
Megophryidae (dikenali sebagai katak tanah) merupakan famili katak yang besar yang berasal dari Asia Tenggara.
Tujuan kajian ini adalah untuk menentukan pilihan diet katak-katak dalam famili Megophryidae dan sama ada
terdapat kaitan antara panjang muncung ventral pemangsa dan panjang mangsa. Kajian ini telah dilakukan di
satu lokasi yang dikenali sebagai habitat katak-katak iaitu Taman Negara Kubah yang merangkumi hutan hujan
primer. Katak-katak telah ditangkap di lokasi dan perut dibedah. Teknik curahan perut telah digunakan untuk
katak yang bersaiz kecil dan besar manakala teknik pengekstrakan perut digunakan untuk katak yang bersaiz kecil.
Isi kandungan perut telah diambil, disusun mengikut kategori pemangsa dan diet katak-katak dianalisa. Isi
kandungan katak telah dianalisa dan dikenalpasti di dalam makmal menggunakan mikroskop. Berdasarkan hasil
kajian, rutin diet dalam family Megophryidae dipengaruhi oleh kepanjangan muncung ventral memandangkan
semakin besar SVL akan mengambil kepanjangan mangsa yang lebih besar.
Kata kunci: diet, famili Megophryidae, panjang muncung ventral, curahan perut, pengekstrakan perut
2
1.0 INTRODUCTION
Basically, amphibians spend part of their life in water and subsequently changing to
terrestrial adult or as an animal that alternate life in and out of water (Duellman & Trueb, 1985).
Their distinctive features including lack of a tail, stocky body, long hind legs, large bulking eyes
and wide mouth (Inger & Stuebing, 2005). In Borneo, most of the frog species live in the hilly
terrain of the lowland forests, which is warm and humid.
There have been a number of studies of the anuran amphibians throughout the years,
which mostly on the faunas of lowlands and hilly dipteroscarp forests (Inger & Voris, 1993).
According to Haas and Das (2011), there are currently 172 species of frogs on Borneo. The
familes represented include Bombinatoridae (Firebelly Toads), Bufonidae (True Toads),
Ceratobatrachidae, Dicroglossidae (True Frogs I), Megophryidae (Litter Frogs), Microhylidae
(Narrow-mouthed Frogs), Ranidae (True Frogs) and Rhacophoridae (Afro-Asian Tree Frogs).
Each of the Bornean families is divided into group of related species of genera.
Foraging tactics are the central subject of modern behavioral ecology and predatory
animals are known to efficiently capture prey, thus, maximizing energy gain under any given
environmental conditions (Krebs & Davies, 1997). Like most predators, anurans forage in one
of two foraging modes which are some are very active, searching foragers, whereas others are
more sedentary, sit-and-wait foragers (Duellman & Trueb, 1986). The tactics utilized by
predators have been regarded as species-specific because predator foraging activities are
regulated by various intrinsic factors, such as physiological tolerance and morphological
constraint (Duellman & Trueb, 1986). Anurans are generally regarded as gape-limited predators
and body size or mouth width are known to influence dietary patterns in various anuran species
(Berry, 1965). Therefore, growth, which releases anuran predators from such morphological
3
constraints, would allow individuals to feed on larger prey and subsequently may enable
individuals to shift predatory tactics onto genetically (Christian, 1982).
Based on the diets, amphibians are known as opportunistic feeders. However, less is
known about their feeding behavior in the wild except that their dietary mainly comprises insects
and arthropods. Some are with specialized diet according to availablity of prey in their habitat.
They can change their mode of diet depending on the habitat. Some frogs that specialize in
eating ants can be generalize when there is less availability of ants in their habitat.
1.1 PROBLEM STATEMENT
In Borneo, there are many species of frogs that live in diverse habitat especially in
tropical rainforests. They feed on various prey depending on their habitat and environment.
Some group feed on different things than others group. What kind of prey that the organisms
are eating is one of the most crucial thing that should be studied in order to determine their diet.
The problems are to know what is the frogs´ main diet in the tropical forest, Borneo. The prey
was analyzed and categorized into sub categories. Then, the factors of prey selection also one
of the crucial thing that should be studied either it is depends on prey availability in that
environment or is there any relationship between the frogs’ snout vent length and the prey length
that it consumed. In this study, Megophryidae family was used as sample in order to determine
their types of prey items and relationship between their SVL and prey length. This family was
chosen because it includes various type of life. For instance, genus Megophrys, Leptobrachium
and Leptolalax are terrestrial while Leptobrachella are stream frog. Comparison of size and the
menu of diet among these genera had been studied. Such comparison will be useful when to
study the ecological diversification of this family.
4
1.2 OBJECTIVES
The objectives of the study are:
i) To determine the prey items of family Megophryidae.
ii) To study the relationship between frog snout vent length (SVL) and prey length it may
consume.
1.3 HYPOTHESIS
HO : There are no significant relationship between frog SVL and prey length it may consume.
HA : There are significant relationship between frog SVL and prey length it may consume.
5
2.0 LITERATURE REVIEW
2.1 Diversity of Megophryidae family in Borneo
The Megophryidae family are known as Asian toad frogs and one of the largest and
diverse family of frogs (Frost & Darrel, 2006). The Asian toad frogs account for 40% of the tiny
and outlandish complement of the ancient frogs and toads. These species are found in India,
Pakistan, and eastward into Southeast Asia, Borneo and the Philippines to the Sunda Islands
(Grafe, 2011). They are the largest and most ecologically diverse group of frogs in the region.
Ranging in size from about 20 to 125 mm, many are large, highly-camouflaged, forest-floor
dwellers with adaptations for hunting large prey (Inger, 2009). Their skin is often modified so
that they closely-resemble dead leaves on the forest floor, complete with mottled brown
coloration and raised lines across the skin that mimic leaf veins (Anstis, 2002). Some species
have pointed projections of skin above their eyes, which further enhances the dead leaf illusion
(Grafe, 2011). Others are small, with adhesive discs on their fingers and are found on rocks
along streams. The large horned frogs (genus Megophrys) of this family can perform impressive
defensive displays. They inflate their lungs, elevate their bodies, open their mouths and scream
loudly, before jumping at their adversary (Frost, 2013).
There are about 136 known species of Megophryidae family (Hance, 2013). They
diverged from all other amphibian families about 70 million years ago, which makes them as
different from their closest relatives in the Pelobatidae family (the spadefoot toads) as pigs are
from giraffes (Myers et al., 2000). There are just seven species in the genus Leptobrachella (the
“Borneo frogs”).
6
According to Inger (2009), the Megophryids are notable for their camouflage, especially
those that live in forests, which often look like dead leaves. The camouflage is accurate to the
point of some having skin folds that look like leaf veins, and at least one species, the long-nosed
horned frog (Megophrys montana) has sharp projections extending past the eye and nose, which
disguise the frog shape (Zweifel & Richard, 1998). Warty specimens of frogs tend to be called
toads as there are really no other differences. They are large, common, distinct frog found in
southern Thailand, Malaya, Singapore, Sumatra and Borneo. The extended eyelids and snout
give them the horned appearance. They feed on spiders, small rodents, lizards and other frogs.
Their habitats are damp and cool lowland and sub-montane forests living among the leaf litter
(Anstis, 2002).
According to Frost and Darrel (2013), the long-nosed horned frog (Megophrys nasuta),
also known as the Malayan horned frog or Malayan leaf frog is a species of frog restricted to
the rainforest areas of southern Thailand and Peninsular Malaysia to Singapore, Sumatra and
Borneo. However, records from Thailand to the Sunda Shelf may apply to another, possibly
unnamed species M. nasuta is a common species in the lowlands of Borneo, but also occurs up
to montane level (Cogger et al., 2004).
It is regularly encountered and its characteristic call is frequently heard in suitable
habitat. It is uncommon in Singapore (Lim & Lim, 1992). This species is known from southern
Thailand (Taylor, 1962), throughout Peninsular Malaysia (Berry, 1975; Dring, 1979), Tioman
Island, Singapore (Lim & Lim, 1992; Leong, 2000), Sumatra, Bintan, all parts of Borneo and
the Natuna Islands. It occurs up to 1,000 m asl. M. nasuta can be found on the forest floors of
Southeast Asia, from the foothills of the Himalayas to the Indo-Australian Archipelogo (Obst et
al., 1984).
7
Megophryids range in size from 2.0 to 12.5 cm in length. The adults' tongues are
noticeably paddle-shaped. Their tadpoles can be found in a variety of waters, but especially
ponds and streams. The tadpoles are extremely diverse in form because of the variety of habitats
they inhabit (Frost & Darrel, 2014).
Family Megophryidae are the largest, most ecologically and morphologically diverse
group of non-neobatrachia frogs in South and Southeast Asia, extending through India, Pakistan,
Southeast Asia, Borneo, Phillippines, and Sunda Islands. Tadpoles are aquatic with buccal
adaptations. M. nasuta, when viewed dorsally, resembles a leaf with its coloration, overall shape
and even leaf-vein looking epidermal growths.
2.2 Ecosystem of Kubah National Park
Kubah National Park consists of mixed dipterocarp forest, among the lushest and most
threatened habitats in Borneo, is front and centre at this 22-sq-km national park. Scientists have
found here an amazing 98 species of palm, out of 213 species known to live in Sarawak and
they have identified 61 species of frog and toad out of Borneo’s more than 190 species. In 2012,
researchers identified what they believe to be a new species of frog, adding it to a list that
includes the aptly named (but oddly shaped) horned frog and a flying frog that can glide from
tree to tree. The forest is also home to a wide variety of orchids. Kubah’s trails offer a good
degree of shade, making the park ideal for the sun-averse.
This habitat supports a rich variety of frogs. Over 60 species of frogs are found at Kubah,
including one of the smallest species of frog in the world which is the Matang narrow mouth
frog. This pea-size frog lives inside and around pitcher plants. A natural frog pond is one of the
8
best places to see frogs in Sarawak. Species found at Kubah include the File-eared frog, Bornean
horned frog, Wallace’s flying frog, Mahogany frog, Dark-eared tree frog, Lowland litter frog,
Harlequin tree frog, Black spotted tree frog, Peat swamp frog, Kuhl’s creek frog and many more.
2.3 Insects as prey
Frogs are one of a few types of animals that undergo the metamorphosis process, which
in turn affects their dietary habits and needs (Wells, 2007). As baby frogs, tadpoles eat pond
plants and algae, as they grow and turn into adult frogs with four limbs, they become carnivorous
(Begon et al., 2006). Different species have different diets, but most frog species eat mostly
insects.
In fact, the frogs actually do eat other live prey and are definitely not vegetarians by any
means. Insects, snails, spiders, worms and even small fish have all been known to be part of a
frog’s diet and while some bigger frogs had been known to go after something as big as a mouse,
there are still those frogs that just stick to insects (Dure & Kehr, 2001).
Frogs hunt live prey, eating snails, spiders, worms, slugs, termites, dragonflies, crickets
and larvae. Depending on the size of the frog, the type and size of insect will vary. Smaller frogs
may eat more gnats, ants, fruit flies and red worms, whereas larger frogs may prefer roaches,
earthworms, small fish and invertebrates. In the wild, frogs will try to eat anything that moves,
even if the prey is too large, but in captivity, its best to offer insects that are smaller than the
width between its eyes.
According to Wells (2007), mostly frogs are either insectivorous or carnivorous as adult.
Most of them are generalist feeders which hunting for variety of insects and other invertebrates,
depending on body size and microhabitat used (Nishikawa, 2000). Small anuran amphibians and
9
those with narrow heads such as microhylids often eat particular prey such as mites,
collembolans, ants and termite which has small sizes (Mitchell & Altig, 1983).
CiCek (2011) investigated food composition of Uludag frog, Rana macrocnemis
Boulenger in Bursa Turkey. From the analysis, the prey items are in the classes Arachnida
(Araneae), Chilopododa (Lithobiomorpha), Diploloda (Julida), Insecta (Odonata, Plecoptera,
Heteroptera, Homoptera, Hymenoptera, Coleoptera, Diptera, Tricoptera, Lepidoptera and
Collembola) and Amphibian (Anura). Based on the results, it is concluded that insects constitute
a large proportion on frog diet which indicate that frogs are generalist feeder.
Another study conducted by Mahan and Johnson (2007) regarding diet composition of
Hyla versicolor (Gray Treefrog). Stomach flushing technique first done by Patto (1983), was
modified to facilitate dietary study. It was found that hymenopterans fill most of the stomach
content followed by coleopteran, and there is a slight number of beetle eaten by frogs in
terrestrial habitat and ponds.
2.4 Importance of different diet
As mentioned earlier, diet of frogs comprised of two which are generalist and specialist
feeders. These kinds of diet are important because it contribute to resource partitioning which
give benefits to a group of amphibians in particular ecosystem. Based on the study of diversity
of frog by Fu et al., (2006) at Henduan Mountain, China, a large number of frogs peaked at mid
elevation. Thus, it can expect that there will be some competition in acquiring food.
Resource partitioning is thought to be the basis of theory for closely-related species,
whereby the niche (such as diet, microhabitat and time) of each species differ from all niches
used by other species, reducing competition for food, space and time, and provide evidence of
10
competition (Campbell, 1997). According to Schoener (1974), the major purposes of resource
partitioning studies is to analyze the limits inter specific competition place on the number of
species that can stably coexist. In each community, the species separate according to various
mixtures of differences in vertical and horizontal habitat, and food type to reduce competition.
Brown (1984) said that species with broad ecological niches should be a generalist feeder
as there will be many prey encountered while foraging. On the other hand, species with narrow
niches restrict a species to a specialist feeder as the number of prey available will be limited.
Species with the most geographical overlap with other species was the one with the most
distinctive diet (William et al., 2006). There is case where the diets of Australian rainforest
microhylids have been overlapping but the species still occur in such high abundance due to
dietary partitioning (Toft, 1980).
2.5 Stomach flushing and stomach extracting method
There are many techniques for investigating the diets of frog such as by observing the
collected feces or directly observed the food that been eaten by frogs or by flushing their
stomach or through dissecting their stomach (Hirschfeld & Rodel, 2011). However, among the
four methods, by observing feces and by directly observed the frog methods are quite irrelevant
because the methods are difficult and the prey items might be completely digested or
unrecognizable. According to Rice and Taylor (1993), flushing and extracting method are useful
for dietary analyses of protected species or populations under long term study as this method
does not require killing the animals to obtain dietary data.
Stomach flushing is an effective method to analyze relative food consumption and
feeding habits of amphibians. Since reports of declines among amphibian populations have been
11
postulated (Wake, 1991; Roberts, 1992), killing frogs for dietary analyses is even less justified.
Stomach flushing has become an increasingly favored alternative to obtain diet data. Flushing
techniques are especially useful for dietary analyses of protected species or populations under
long-term study. To date, such techniques have been successfully used in a variety of groups
including fishes (Swenson & Smith, 1973; Dos Santos & Jobling, 1988; Hopkins & Larson,
1990), crocodilians (Taylor & Webb, 1978; Fitzgerald, 1989;), lizards (Legler & Sullivan, 1979;
James, 1990), turtles (Balazs, 1980), and salamanders (Fraser, 1976; Joly & Giacoma, 1992).
Although flushing techniques have been attempted on some species of frogs and toads (Legler
& Sullivan, 1979; Gittins, 1987; Joly, 1987), the method has not been extended to large ranid
frogs.
Furthermore, stomach extracting method is also another method to analyze food contents
in the stomach of frogs. The method is more convenient as it does not need much apparatus as
stomach flushing method. The method was used to determine the stomach contents for smaller
frogs.
2.6 Previous studies of diet of frogs
A study on prey specialization and diet of frogs was carried out by Kristoffer Ahlm in
2015. The same method was used which is stomach flushing method to determine the stomach
content. But then, stomach extracting method by using forceps are not used in the study. The
study was conducted in a primary rainforest in Ulu Temburong National Park, in Brunei, Borneo
near the border to Sarawak, Malaysia. He conducted the research on five families which are
Bufonidae, Dicroglossidae, Megophryidae, Microhylidae and Ranidae. The results show that
the most common food source was ants, which constituted 63.7% of the total food for all studied
12
frog families. Based on his study, he stated that Megophryidae family are specialist and did not
eat ants and termites. This is shown by analysis of Shannon’s diversity index which had a
significantly lower mean diversity index compared to the other generalist family.
Furthermore, another previous study of diet of frogs that use the same method which is
stomach flushing method was by Jorn Dietl, Wolf Engels and Mirco Solec in 2009. The study
was conducted in Araucaria rain forests on the Serra Geral of Rio Grande do Sul, Brazil. They
analyzed the diet of Ischnocnema henselii. Based on the stomach flushing process, they found
that the identified prey items comprised arthropods such as spiders, ants, orthopterans,
collembolans and homopterans.
The next previous study that used the same stomach flushing method was by Ferreira
(2015). The study was conducted in Maui, Hawaii. The aim of the study was to determine the
diet of the non-native greenhouse frog (Eleutherodactylus planirostris). The Greenhouse Frog
is one of the most widespread frog species in the world. They analyzed stomach contents of 397
frogs from 10 study sites in Maui. Based on study, they found that the greenhouse frogs are
active, ant specialist predators in the leaf litter. Ants were the dominant prey found in stomachs
in both number and volume. Furthermore, only ants were consumed in a higher proportion than
they were sampled in the environment.
The other previous study that use stomach flushing method was by Sole et al. in 2005.
The study was conducted in Araucaria forests, southern Brazil. Frogs and toads belonging to
five families were collected manually in their habitats and taken immediately to the laboratory
for flushing. They applied this method in the study of seasonal nutrition of anurans of 15 species
at an Araucaria forest habitat on the Serra Geral of Rio Grande do Sul, Brazil. Over 500 frogs
and toads of different body size were handled in order to evaluate an improved protocol without
13
narcosis using soft infusion tubes in order to avoid negative effects of the flushing procedure.
The specimens were treated soon after capture and then returned to the sampling sites. The
results are discussed with reference to the few studies on stomach flushing in amphibians. The
improved technique is recommended to avoid killing of numerous animals for nutritional
studies, in particular because of the worldwide threatening of amphibian populations.
Table 1: Summary of previous studies of diet that use stomach flushing method
Previous studies
Family/species
Outcomes
Sole et al. (2005)
Five families of frogs & toads
Stomach flushing is a
recommended method to
avoid killing animals for
nutritional studies
Jorn Dietl, Wolf Engels and
Mirco Solec (2009)
Ischnocnema henselii
Identical prey items comprise
arthropods such as spiders,
orthopterans, collembolans,
ants and homopterans
Ferreira (2015)
Eleutherodactylus
planirostris
The species is specialist frog
and ant were dominant prey
Kristoffer Ahlm (2015)
Bufonidae, Dicroglossidae,
Megophryidae, Microhylidae
and Ranidae
Most prey items are
comprised of ants. However,
Megophryidae family is
specialist and did not eat ants
and termites
14
3.0 MATERIALS AND METHODS
3.1 Sampling site
The sampling process was conducted in Kubah National Park, Sarawak (Figure 1).
Kubah has three mountain peaks which are the 911 m high Gunung Serapi and the slightly
smaller Gunung Selang and Gunung Sendok. Kubah is situated 22 km from Kuching. The Park
covers an area of 2,230 ha and comprises the heavily forested slopes and ridges of the Serapi
range. At heights of between 150 - 450 m, Kubah’s soft sandstone is punctuated with bands of
hardened limestone which have created a number of beautiful waterfalls.
Kubah provides an interesting range of treks and forest walks, from the gentle to the
downright arduous. Some of the park’s jungle trails begin on the Gunung Serapi Road which is
a sealed track that starts at the Park HQ and leads to telecommunication tower at the summit of
Gunung Serapi. There are seven trails in KNP which are Waterfall trail, Rayu trail, Main trail,
Selang trail, Summit trail, Palmetum trail and Belian trail. The trails that were used to collect
the samples are Waterfall and Main trail.
15
Figure 1: Map of Kubah National Park, Sarawak (Source: Das & Haas, 2010)
16
3.2 Sampling method
3.2.1 Sampling and identification
In the study, the samples were collected and identified by using active method collection
specimens, namely visual encounter survey (VES) and acoustic encounter survey (AES). This
field survey was conducted for five months starting from 17th August 2016 until 18th January
2017 and seven days for each sampling period. The frogs were collected mainly during night-
time when frogs are most active which is 1900 until 2200. Visual surveys were conducted with
headlamps along trails and streams. Experienced members in the research group had located
certain frogs with just acoustical aid. Frogs were collected by hand and put in small plastic.
Then, the frogs were identified and measured. Every sample was identified following
Inger and Stuebing (2005) and Indraneil Das (2002). The parameters taken for each frog was
species, snout-vent length (SVL), head width length (HW) and body mass. The frogs were
measured by using digital calipers and weighted by using Pesola of 10 g and 50 g, according to
their size. Frog specimens were labelled with the name of species, name of collector, sex,
weight, SVL (mm), time of capture and date, elevation of capture and tagged on their right hind
limbs.
3.2.2 Stomach flushing method
To start stomach flushing the frogs, a spatula or a feather weight forceps was used to
gently open the frogs´ mouth. Thereafter, the mouth of the frog was fixed with a finger when
inserting a soft, flexible tube attached to a syringe as done by Mahan and Johnson (2007). The
tube was introduced through the frogs’ esophagus into the stomach. The was inserted through
17
the tube using a flushing syringe of either 50 ml, 20 ml or 10 ml. Different syringe was used
with different size of frogs.
The frog was placed on a petri dish. The frog will then throw up and the stomach content
was collected. The flushed stomach content was then poured into a petri dish. The method was
repeated until only water came out from the frog stomach, typically this was made three to four
times. The stomach contents were extracted from the water using forceps and the contents were
preserved in the tube of 10% formalin before being analyzed in the laboratory. Figure 2 shows
the apparatus that were used for stomach flushing technique.
3.2.3 Stomach extracting method
For smaller size frogs, stomach extracting method was utilized. This is done by the same
procedure as stomach flushing method but easier and convenient. The forceps were used to open
the frog’s mouth and then put into the stomach. After that, all the stomach contents were
extracted away from the stomach. After the flushing and extracting process, stomach contents
were collected into a small tube filled with 10% formalin to preserve the stomach content for
Figure 2: Stomach flushing apparatus (Source: Muhamad Affan, 2016)
18
later analysis. The arthropod samples will be analyzed in the laboratory at the field site into
different prey categories. All frogs were released within one hour at their capture site to
minimize stress for the animals.
3.2.4 Stomach contents analyses
All prey item in the stomach that were preserved in 10% formalin (Figure 3) was
identified to ordinal or family level whenever possible and numbers of individuals for each prey
items were counted under a stereo microscope by using numerical method of Hyslop (1980)
(Refer to Appendix 8). The prey item was counted as individual based on the number of the
head observed in the prey samples.
After the prey item individuals had been categorized into order, fluid displacement
method was used to investigate the relationship between the volumes of prey items with anuran
diet. Volume of prey items were determined by immersing each prey items into 8 ml water. The
higher volumes of the prey items immersed indicate type of prey preferred by frog.
Figure 3: Stomach contents that preserved in 10% formalin (Source:
Muhamad Affan, 2016)
19
3.2.5 Statistical analyses
3.2.5.1 Index of relative importance (IRI)
The index of relative importance was used to reduce bias in the description of diet.
Occurrence of prey item is calculated based on how frequent the prey item species occur in all
the individuals. To describe the importance of each item consumed, the index of relative
importance (IRI) (Pinkas et al., 1971) was calculated as:
IRIt = (POt) x (PIt + PVt)
IRIt = index of relative importance of the prey items consumed
POt = percentage of occurrence in the diet of the individual (100 x number of individual
percentage of occurrence / total number of individuals)
PIt = percentage of individuals in the diet of the frogs (100 x total number of t in all individuals
/ total number of individuals of all taxa in all individuals)
PVt = percentage of volume of a species in the diet of frog (100 x total volume of individuals of
t in all individuals / total volume of all taxa in all individuals)
3.2.5.2 Regression
Regression between the prey length (minimum and maximum of each prey) and
predator size (SVL) were made using Minitab 17 Statistical software. The r2 value in the
regression indicates the strength of the regression. Value +1 or -1 indicates a strong linear
association.
20
HO : There are no significant relationship between frog SVL and prey length it may consume.
HA : There are significant relationship between frog SVL and prey length it may consume.
If p calculated < p critical, this means that the null hypotheses (HO) is rejected.
If p calculated > p critical, this means that the null hypotheses (HO) is accepted.
21
4.0 RESULTS
4.1 Frogs collected
From the sampling period, a total of 31 individuals of amphibians from family
Megophryidae had been caught and analyzed. Out of 31 individuals, only 13 individuals
comprising of five species and four genera of amphibians have stomach contents (Table 2). Most
of the frogs collected belongs to the genus Leptolalax, with ten individuals and two species. The
other genera were Leptobrachium, Leptobrachella and Megophrys with only single individual
each.
Table 2: Number of individuals of frogs collected in Kubah National Park, Sarawak
Genus
Species
Individuals
Leptobrachium
Leptobrachium abboti
1
Leptolalax
Leptolalax dringi
5
Leptolalax gracilis
5
Leptobrachella
Leptobrachella mjobergi
1
Megophrys
Megophrys nasuta
1
Total
13
The most abundant species are L. dringi and L. gracilis from the genus Leptolalax with
five individuals each. The least frequently captured species which became the representative of
each genus were L. abboti, L. mjobergi and M. nasuta with only single species each.
22
4.2 Prey items
From the stomach flushing and extracting method, a total of 85 individuals of prey items
were collected comprising of five orders of insect and some indeterminate insects from stomach
of the amphibians (Table 3). Based on the result obtained, the highest number of prey items
collected belonged to order Isoptera which was 24 individuals, followed by order Hymenoptera
that have 21 individuals. The least number of prey items collected was order Lepidoptera with
only single individual. Meanwhile, the number of individuals of indeterminate insects was 12.
Table 3: Prey items of family Megophryidae
Prey items
Number of prey items collected
Coleoptera
13
Hymenoptera
21
Isoptera
24
Lepidoptera
1
Orthoptera
14
Indeterminate insects
12
TOTAL
85
4.3 Diet analysis
4.3.1 Diet analysis of the frogs in Kubah National Park
From the total five species caught, only M. nasuta undergone stomach flushing method
due to its large size, whereas L. abboti, L. dringi, L. gracilis and L. mjobergi were stomach
23
extracting method. The diet of the captured frogs contains at least two prey items in their
stomach of the prey types as identified in Table 4.
Occurrence of prey item was calculated based on how frequent the prey items were
present in the 13 individuals of family Megophryidae. Number of individual of prey items
altogether with volume of each prey items in each stomach were also calculated to determine
the index of relative importance of diet in each frog species.
24
Table 4: Prey types in the diet of frogs from Kubah National Park: O, occurrence; % O, percentage of occurrence;
N, number of individuals; % N, percentage of number individuals; V, volume in mm3; % V, percentage of volume;
IRI, index of relative importance (IRI), showed for each prey item
Predators
Prey items
O
% O
N
% N
V
%V
IRI
Leptobrachium
abboti (n=1)
Orthoptera
Indeterminate
insects
1
1
100.00
100.00
2
3
40.00
60.00
50
30
62.50
37.50
10250
9750
Leptolalax
dringi (n=5)
Coleoptera
Orthoptera
Indeterminate
insects
1
2
2
20.00
40.00
20.00
2
4
1
28.57
57.14
14.29
100
350
50
20.00
70.00
10.00
971
5086
486
Leptolalax
gracilis (n=5)
Coleoptera
Orthoptera
2
4
40.00
80.00
4
8
33.33
66.67
100
400
20.00
80.00
2133
11734
Leptobrachella
mjobergi (n=1)
Lepidoptera
Coleoptera
Isoptera
Indeterminate
insects
1
1
1
1
100.00
100.00
100.00
100.00
1
2
5
3
9.09
18.18
45.45
27.27
100
50
100
30
35.71
17.86
35.71
10.71
4480
3604
8116
3798
Megophrys
nasuta (n= 1)
Hymenoptera
Isoptera
Coleoptera
Indeterminate
insects
1
1
1
1
100.00
100.00
100.00
100.00
21
19
5
5
42.00
38.00
10.00
10.00
250
100
150
150
38.46
15.38
23.08
23.08
8046
5338
3308
3308
In L. gracilis, its SVL ranged from 27.54 to 48.88 mm (mean 39.36 ± SE 8.08) and
contained four individuals of Orthoptera that occured in five individuals stomach and thus
making it the dominant diet of this species with index of relative importance (IRI) of 11734.
25
This is followed by two individuals of Coleoptera which occured in five stomach of individuals
of L. gracilis. These prey items have body length ranged from 0.21 to 9.10 mm while the prey
volume of Coleoptera and Orthoptera were 100 mm3 and 400 mm3 respectively.
L. mjobergi which has SVL of 18 mm had a diet dominated by Isoptera (IRI=8116) with
five individuals and prey volume of 100 mm3. Other prey items for this species were Lepidoptera
(IRI=4480), some indeterminate insects (IRI=3798) and Coleoptera (IRI=3604). All these prey
items have body length ranged from 0.01 to 21.00 mm (mean 1.98 ± SE 1.90), prey volume
ranged from 30 to 100 mm3 (mean 70 ± SE 17.8).
L. abboti which has SVL of 31.28 mm only have two individuals of prey items.
However, after being extracted, only single individual of prey was identified which was order
Orthoptera with length 9.10 mm and prey volume of 50 mm3. It is followed by indeterminate
insect (IRI = 9750).
The SVL of L. dringi was ranged from 29.42 to 44.04 mm (mean 35.07 ± SE 6.21).
There were four individuals of Orthoptera (IRI = 5086) and followed by Coleoptera and
indeterminate insects with IRI were 971 and 486 respectively. These prey items have body
length ranged from 0.31 to 0.075 to 9.0 mm.
In M. nasuta which has SVL of 71.89 mm, stomach flushing method was used and 50
prey items were obtained. The diet of this frog was dominated by Hymenoptera (IRI = 8046)
with total of 21 individuals. The other prey items were comprised of Isoptera (IRI = 5338),
Coleoptera (IRI = 3308) and some indeterminate insects (IRI = 3308). All these prey items have
body length ranged from 0.01 to 0.52 mm (mean 0.0776 ± SE 0.0137), prey volume ranged from
100 to 250 mm3 (mean 162.50 ± SE 62.92).
26
4.3.2 Analysis of predator snout vent length and prey length
Regression analysis between the prey size (minimum and maximum prey length in each
frog species) and predator SVL were conducted for species with five individuals by using at
least one prey individual which have full body. Because of that, linear regression analysis could
not be done to M. nasuta, L. abboti and L. mjobergi as these species only have single individual
respectively. The value of each prey sizes and the predator SVL were transformed into log 10
to give a normal distribution curves in the regression as frogs captured were not from three life
stage but only in adult stage.
For L. dringi, the regression between predator SVL and maximum prey length shows a
positive correlation (r2: 0.972; p-value < 0.05) (Figure 4). This graph shows that the bigger the
sizes of predator, the bigger the size of the prey that can be consumed as the SVL reflect the
head width of a particular frog. There was a trend in the choice of maximum prey length of L.
dringi as the frog chooses the prey length between 1 to - 0.5 mm.
Figure 4: Regression between maximum prey length and predator snout ventral length (SVL) of
Leptolalax dringi
27
Based on the Figure 5, there is no significant regression between SVL of L. dringi and minimum
prey length (r2: 0.851; p-value>0.05).
Figure 5: Regression between minimum prey length and predator snout ventral length (SVL) of Leptolalax
dringi
28
Figure 6 shows the regression between SVL of L. gracilis and maximum prey length shows
positive correlation (r2: 0.988; p-value<0.05) which states that this species has a specific
maximum length that can be consumed according to its SVL.
Figure 6: Regression between maximum prey length and predator snout ventral length (SVL) of Leptolalax
gracilis
29
Regression between SVL of L. gracilis and minimum prey length shows positive correlation (r2:
0.993; p-value < 0.05) (Figure 7). This graph indicated that L. gracilis have a specific minimum
length that can be consumed according to its SVL.
Figure 7: Regression between minimum prey length and predator snout ventral length (SVL) of Leptolalax
gracilis
30
5.0 DISCUSSION
5.1 Frogs collected
Based on the result, the total number of individuals of family Megophryidae that were
caught throughout the sampling period was 31 individuals comprising of four genera. However,
after the stomach flushing and extracting method had been conducted, the result showed that
only 13 individuals have prey items. It indicated that either the food already digested by the frog
or the frog did not consume any food at that time. Because of that, no stomach contents were
obtained from the stomach of the particular amphibians. According to study conducted by Ahlm
(2015), the digested food was found in all families but the highest proportion was in family
Megophryidae which was about 26% of the food content. It is concluded that Megophryidae
digested their food quicker than other families.
From the diet data, it is showed that genus Leptolalax have the highest number of
individuals which was ten individuals comprising of two species. Meanwhile, the other genus
only has single individual of prey item each. Some reason could be the Leptolalax digested their
food slower than other genus due to smaller size. Leptolalax are typically small in size compared
to other genus in family Megophryidae. Another possible reason was the extracting method
which could be the most suitable technique in analyzing the diet of Leptolalax because of small
size. Because of that, the analysis of prey items became more efficient and produce reliable
result. Stomach extracting method is suitable for any frogs but more suitable for smaller size
frogs.
31
5.2 Prey items
In the present study, insects were commonly found as prey among frogs. This is in line
with previous studies stating that most adult anurans are insectivorous (Da Silva, 1989). The
highest number of individuals of prey items collected was Isoptera which is termites. These
results indicate that termites are the most abundant group of preys found in the forest understory
and thus frogs might simply be capturing prey in direct proportion to their availability or gape
size. Since the study was not involved the survey on insect populations in the study sites, it is
difficult to determine whether frogs simply eat whatever they can find or whether they prefer
certain prey items. In other words, termites were abundant in that particular habitat which is the
main diet of Megophryidae. This is because Megophryidae is generalist feeder as mentioned by
Emerson et al. (1994) and Wells (2007). Generalist feeders depend on availability and
abundance of prey in that habitat.
Studies by Vitt and Zani (1998) stated that Megophryidae are mostly opportunistic and
that prey availability drives what the frogs mainly tend to eat. The least number of prey items
was Lepidoptera which is moth. This is due to low population of moth in that area or the frogs
faced difficulties in catching the moths. The number of indeterminate insects also higher which
was 12 individuals. Indeterminate insects were prey items that are partially or fully digested
which cannot be recognized by using microscope. As mentioned earlier, there is study that stated
Megophryidae have high proportion of digested food compared to other family.
5.3 Diet analysis
Based on the IRI analysis, most diet of frogs was dominated by Orthoptera as it has the
largest IRI value in three species. It is showed that Orthoptera are abundant in the habitat that
32
frogs are living and can be easily found. Orthopterans are found in virtually all terrestrial habitats
were plants can live and where one can find insects, being absent only in oceans, polar regions,
and extreme alpine environments (Rowell & Flook, 2001; Grizmek et al., 2004). Another
possible reason was the preference of Megophryidae on Orthoptera which were found the most.
In the diet of amphibians, the prey selection in each species was influenced by three
factors which are SVL of the frog, prey abundance and gape size in the environment. In other
species, the amphibians’ size is highly correlated with prey size which may be useful in
maximizing the net energy gain of energy intake when hunting for prey (Mitchell, 1983;
Maneyro et al., 2004). The diet of frogs is related with basic assumption of the ‘optimal foraging
theory’ as maximum efficiency in energy intake is favored by natural selection as deducted by
Pyke (1984). From this example, it is shown that the energy gain in larger frogs might be
enhanced by the consumption of larger prey (Low & Torok, 1998).
Based on the result, bigger sized frog such as Megophryidae tend to choose prey like
Orthoptera and Coleoptera which is bigger than other prey even though the most preferred food
is Hymenoptera. This is because there is relationship between the selectivity of prey length and
predator SVL which resulted from the niches partitioning between the individuals of the same
species to enable them to live in the same community. This makes niches partitioning even more
fine and efficient.
This is proven by linear regression analysis that had been done to selected frogs; mostly
the prey selection is highly correlated with predator SVL. For example, the SVL of L. gracilis
is 27.54 mm has prey selection ranged from 0.21 mm to 5.30 mm (Figure 6 & 7). As mentioned
earlier, prey size plays an important role in the foraging strategies of most amphibians. In other
words, frogs that have bigger SVL tends to eat the prey that have bigger prey length and vice
33
versa. It is concluded that in the diet of frogs, there are correlation which is inter specific
correlation between jaw size and shape of amphibians. Predators such as frogs that swallow
their food in whole requires gape size that sets an upper limit to ingestible prey size of
swallowing capacity (Reynold & Scott, 1982). According to Hespenheide (1973), gape size and
swallowing capacity are often positively correlated with SVL of the frogs.
However, regression analysis of L. dringi showed that there is no relationship between
SVL of frogs and minimum prey length. It is concluded that the frogs can feed on any preys
independent of prey size. However, there is limit of prey length that it can consume. This is
because there is positive correlation of regression between frogs SVL and prey length which
shows that the prey selection was limited by maximum prey length.
The relationship between gape size and foraging success also had been proven based on
the food content found in the stomach of M. nasuta as the stomach contain Hymenoptera,
Isoptera, Coleoptera and some unidentified insects that in total were about 50 individuals. It is
assumed that M. nasuta can open their mouth wider because of their bigger body size than small
frogs and therefore can put up larger prey, but they still can eat small preys as well (Emerson et
al., 1994). However, small frogs that have narrow head often eat particular preys like mites,
collembolans, ants and termite which has tiny size (Michell & Altig, 1983).
The challenges and limitations of the study were less data obtained for statistical analysis
purposes. Linear regression analysis could not be conducted because of insufficient data for
genus Leptobrachella, Leptobrachium and Megophrys. This is because small number of
individuals of frogs that contains prey items were collected because the contents already
digested. Digested food caused no data obtained for diet analysis and partially digested food
also caused some prey items could not be identified which called as indeterminate insect,
34
making it hard to determine their diet and food selection. Some reasons that caused digested
food were the stomach flushing and extracting process are conducted late after the frogs being
caught.
Another reason is lack of observation, skills and less sampling effort had make the study
less accurate. In addition, identifications of prey based on the sample collected is hard because
most of the insects are only able to be identified through specific part of body. Other than that,
number of individuals of Megophryidae that were caught was also quite fewer because the
weather condition had affect most of sampling day because the sampling always been delayed
if there is rain. Due to shifting weather much work time in the field was lost and therefore a
smaller data set than expected was obtained. The rainforest fauna is still not completely
documented and many species are not known, which makes these sorts of studies very
challenging.
35
7.0 CONCLUSION & RECOMMENDATIONS
Based on diet analysis, diet of family Megophryidae were comprised of insects which
were Coleoptera, Hymenoptera, Isoptera, Lepidopteraa and Orthoptera. The most abundant prey
item was Isoptera as it has the most number of individuals caught but the highest IRI belonged
to Orthoptera. Furthermore, diet habits of family Megophryidae are influenced by snout vent
length (SVL) of predator and length of prey. The bigger size predator SVL will consume bigger
prey length and vice versa. However, there is no relationship between frog SVL and minimum
prey length in L. dringi.
Mostly the prey items already digested by the frogs and cause no diet data obtained. One
of the improvement that can be made is the stomach extracting process should be done early so
that the prey items would not be digested by the amphibians. Furthermore, the relatively small
sample size will affect the results. This limitation could have been circumvented if more time
was allocated for the project and also if unknown prey items could have been identified to a
larger extent by other methods such as DNA barcoding. With more highly trained personnel,
more of the collected data would have been able to be identified, but due to the project time
limits everything had to be identified in the laboratory during the research period. In other
words, larger sample size need to be collected in order to obtain more reliable and accurate data
for diet analysis. In order to so, sampling effort need to be longer so that more samples can be
collected.
36
6.0 REFERENCES
Ahlm, K. (2015). Prey specialization and diet of frogs in Borneo, Sweden, Umea University.
Anstis, M. (2002). The tadpoles of South-Eastern Australia. New Holland Publishers
(Australia), Sydney, Auckland, London, Cape Town.
Begon, M.T., Colin, R., & Harper, J.L. (2006). Ecology; from individuals to ecosystems.
Oxford: Blackwell.
Brown, J. H. (1984). On the relationship between abundance and distribution of species.
American Naturalist, 124, 255-279.
Campbell, N.A. (1997). Bilogy, 4th ed. University of California, Riverside. The
Benjamin/Cummings Publishing Company; New York, pp. 1266.
CiCek, K. (2011). Food composition of Uludag frog, Rana macrocnemis Boulenger, 1985 in
Uludag (Bursa, Turkey), Acta Herpetologica, 6(1), 87-99.
Christian, K.A. (1982). Changes in the food niche during postmetamorphic ontogeny of the
frog Pseudacris triseriata. Copeia 1982: 73-80.
Cogger, H.G., & Zweifel, R.G. (2004). Encyclopedia of Reptiles and Amphibians. San Diego:
Academic Press. p. 88.
Dietl, J., Engels, W., & Sole, M. (2009). Diet and feeding behavior of the leaf-litter frog
Ischnocnema henselii (Anura: Brachycephalidae) in Araucaria rainforests on the Serra
Geral of Rio Grande do Sul, Brazil. Journal of Natural History, 43(23-24), 1473-1483.
Duellman, W.E., & Trueb, L. (1986). Biology of amphibians. New York: McGraw Hill.
Emmerson, S. B., Greene, H.W. & Charnov, E.L. (1994). Allometric aspect of predator prey
interaction. In Ecological Morphology. (Weinwright, P. C. and Reily, S. M., Ed.).
Chicago: University of Chicago Press, pp. 123-139.
Frost, D.R. (2013). "Megophrysnasuta (Schlegel, 1858)". Amphibian Species of the World
5.6, an Online Reference. American Museum of Natural History. Retrieved 30 June
2013.
Frost, D.R. (2015). Amphibian Species of the World: An Online Reference. Version 6.0.
Fu, C., Hua, X., Li, J., Chang, Z., Pu, Z., & Chen, J. (2006). Elevational patterns of frog species
richness and endemic richness in the Hengduan Mountains, China: geometric
constraints, area and climate effect, Ecography, 29, 919-927.
Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.html.
American Museum of Natural History, New York, USA.
37
Grafe, T.U., Stewart, M., Lampert, K., & Rödel, M.O. (2011). Putting toe clipping into
perspective: a viable method for marking anurans. Journal of Herpetology.
45:28-35.
Hance, J. (2013). Captive frogs may be spreading diseases to wild cousins across Southeast
Asia. Retrieved May 2013 from
http://news.mongabay.com/2013hancefrogschytridcaptive.U
Haas, A., Das, I., & Hertwing, S. (2014). FROGS OF BORNEO: The frogs of East Malaysia and their larval
forms. Retrieved February, 8, 2014 from http://www.frogsofborneo.org/.
Hespenheidae, H. A. (1973). Ecological inferences from morphological data. Annual Review of Ecological
System, 4, 213-229.
Inger, R.F. & Stuebing, R.B. (1997). A Field Guide to the Frogs of Borneo. Borneo Natural
History Publishers, Kota Kinabalu, Malaysia.
Inger, R.F. & Stuebing, R.B. (2005). A Field Guide to the Frogs of Borneo (second edition).
Natural History Publication (Borneo), Kota Kinabalu. 133pp.
Inger. R. F. (2005). The Systematics and Zoogeography of The Amphibian Of Borneo. Natural
History Publications (Borneo).
Jacob. (1984). Atlas of Reptiles and Amphibians for the terrarium. Neptune, City, NJ: T.F.H.,
Publishing, Inc.
Low, P., & Torok, J. (1998). Prey size selection and food habits on water frogs and moor frogs
from Kis-Balaton, Jungary, Herpetozoa, 11(30), 71-78.
Mahan, R. D., & Johnson, J. R. (2007). Diet of the Gray Treefrog (Hyla Versicolor) in relation
to foraging site location. Journal of Herpetology. 41 (1), 16 23.
Maneyro, R., Naya, D. E., Rosa, I. D. Canavero, A., & Camargo, A. (2004). Diet of
SouthAmerican frog Leptodactylus ocellatus (Anura, Leptodactylidae) in Uruguay.
Iheringia, Ser. Zool., Porto Alegre, 94(1), 57-61.
Mattison, C. (1987). Frogs and toads of the world. Blandford Press, U.K.
Mitchell, S. L. (1983). The feeding ecology of Sooglossus gardineri. Journal of Herpetology 17:
281-282.
Myers, N., Mittermeier, R.A., Mittermeir, C.G., Da Fonseca, G.A. & Kent. J. (2000).
Biodiversity hotspots for conservation priorities. Nature, 403: 853858.
Obst, F., Richter, K., & Jacob, U. (1984). Atlas of Reptiles and Amphibians
interrarium.Neptune, City, NJ. T. F. H., Publishing, Inc.
Pinkas, L., Oliphant, M., S., & Iverson, I., L., K. (1971). Food habits of albacore, bluefin tuna,
and bonito in California waters, Freshwater Biology, 49, 274-285.
38
Pyke, G. H. (1984). Optimal foraging theory: a critical review, Annual Review of Ecology, 15,
523-575.
Schoener, T.W. (1974). Resources partitioning in ecological communities. Science. 27-39.
Sole, M., Beckman, O., Pelz, B., Kwet, A., & Engels, W. (2005). Stomach flushing for diet
analysis in anurans: an improved protocol evaluated in a case study in Araucaria forests,
southern Brazil. Studies on Neotropical Fauna and Environment, 40:23-28.
Sole, M., Beckman, O., Pelz, B., Kwet, A., & Engels, W. (2005). Stomach-flushing for diet
analysis in anurans: An improved protocol evaluated in a case study in Araucaria forests,
southern Brazil. Studies on Neotropical Fauna and Environment, 40(1), 23-28.
Smith, G.R., Ballinger, R.E., & Congdon, J.D. (1993). Thermal ecology of the high altitude
bunch grass lizard, Sceloporusscalaris. Can J Zool 71: 21522155.
Toft, C.A. (1980). Feeding ecology of thirteen syntopic species of anurans in a seasonal tropical
environment. Oecologia, 45: 131-141.
Toft, C.A. (1981). Feeding ecology of Panamanian litter anurans: Patterns in diet and foraging
mode. J Herpetol 15: 139144
Wells, K.D. (2007). The ecology and behavior of amphibians. University of Chicago Press,
Chicago, London.
Williams, Y.M., Williams, S.E., Alford, R.A., Waycott, M., & Johnson, C.N. (2006). Niche
breadth and geographical range: ecological compensation for geographical rarity in
rainforest frogs. Biology Letters(2). 531-535.
Wygoda, M.L., Williams A.A. (1991). Body temperature in free-ranging tree frogs (H. cinerea):
a comparison with “typical” frogs. Herpetologica 47: 32833
39
Appendix 1: List of anurans captured in Kubah National Park
No
Field ID
Species
Date
Hour
SVL
(mm)
Weight
(g)
Locality
Tibia
length
(mm)
1
KNP1377
Leptobrachium ingeri
17/08/16
2108
38.85
4.9
Palm Trek Trail,
KNP
16.34
2
KNP1384
Leptolalax gracilis
17/08/16
2130
37.60
1.6
Belian Trail, KNP
20.25
3
KNP1385
Leptobrahium abotti
17/08/16
2141
45.09
2.2
Belian Trail, KNP
16.62
4
KNP1387
Megophrys nasuta
17/08/16
2300
102.00
66.0
HQ Park, KNP
38.00
5
KNP1389
Leptobrachella mjobergi
18/08/16
1919
20.05
0.5
Hostel stream,
KNP
1.37
6
KNP1391
Leptobrachella mjobergi
18/08/16
1930
13.82
0.3
Hostel stream,
KNP
9.32
7
KNP1480
Leptobrachium ingeri
21/08/16
2145
34.44
2.1
Palm Trail, KNP
15.43
8
KNP1481
Leptoalalax gracilis
21/08/16
2155
43.87
5.8
Selang Trail, KNP
23.53
40
9
KNP1509
Megophrys nasuta
24/08/16
10
KNP1534
Leptobrachium abotti
24/10/16
1939
31.38
2.0
Waterfall Trail,
KNP
13.53
11
KNP1536
Leptolalax dringi
24/10/16
2155
44.04
5.5
Frog Pond, KNP
23.72
12
KNP1543
Leptolalax dringi
24/10/16
1858
38.78
5.8
Frog Pond, KNP
23.09
13
KNP1555
Leptolalax gracilis
25/10/16
1945
48.88
6.1
Frog Pond, KNP
25.83
14
KNP1579
Leptobrachella mjobergi
26/10/16
1902
16.93
0.4
Main Trail, KNP
9.70
15
KNP1591
Leplolalax dringi
27/10/16
1849
32.84
2.4
Waterfall Trail,
KNP
19.22
16
KNP1592
Leptolalax gracilis
27/10/16
1853
27.54
2.1
Waterfall Trail,
KNP
13.48
17
KNP1593
Leptolalax dringi
27/10/16
1900
29.42
3.8
Waterfall Trail,
KNP
15.37
18
KNP1598
Leptobrachium abotti
27/10/16
1954
70.56
25.0
Waterfall Trail,
KNP
25.79
41
19
KNP1599
Leptolalax gracilis
27/10/16
1958
43.52
5.0
Waterfall Trail,
KNP
23.05
20
KNP1617
Leptobrachium abotti
17/01/17
2028
40.22
4.5
Frog Pond, KNP
17.45
21
KNP1623
Megophrys nasuta
17/01/17
2141
56.86
7.4
Main Trail, KNP
19.28
22
KNP1624
Leptobrachium abotti
17/01/17
2151
36.85
2.6
Main Trail, KNP
15.12
23
KNP1632
Leptobrachella mjobergi
18/01/17
1931
17.50
0.6
Frog Pond, KNP
10.40
24
KNP1633
Leptobrachella mjobergi
18/01/17
1950
35.90
0.7
Frog Pond, KNP
10.70
25
KNP1639
Leptolalax gracilis
19/01/17
1927
41.00
3.4
Frog Pond, KNP
23.00
26
KNP1642
Leptolalax gracilis
19/01/17
2030
33.00
4.3
Frog Pond, KNP
23.00
27
KNP1643
Leptobrachella mjobergi
19/01/17
2110
10.00
0.1
Frog Pond, KNP
5.00
28
KNP1649
Megophrys nasuta
20/01/17
1915
60.00
10.00
Frog Pond, KNP
20.00
29
KNP1652
Leptolalax gracilis
20/01/17
1942
42.20
3.2
Frog Pond, KNP
20.40
30
KNP1658
Leptobrachella mjobergi
20/01/17
2008
18.00
0.4
Frog Pond, KNP
9.0
31
KNP1661
Leptolalax gracilis
20/01/17
2043
23.00
0.8
Frog Pond, KNP
12.50
42
Appendix 2: Analysis on insect found in the stomach of family Megophryidae
Species
Diet
Order
Insect part
Leptobrachium abboti
Orthoptera
Legs
Indeterminate insect
Exoskeleton scattered
Leptolalax dringi
Orthoptera
Exoskeleton scattered
Coleoptera
Full body
Indeterminate insect
Antennae scattered
Leptolalax gracilis
Coleoptera
Full abdomen
Orthoptera
Legs
Megophrys nasuta
Hymenoptera
Head
Isoptera
Full body
Coleoptera
Thorax
Head
Indeterminate insect
Antennae scattered
Leptobrachella mjobergi
Lepidoptera
Full body
Coleoptera
Full body
Isoptera
Full body
43
Appendix 3: Measurements of body length
Appendix 4: Measurement of gape size
44
Appendix 5: Measurement of tibia-fibula length
Appendix 6: Preparation of stomach flushing
45
Appendix 7: Stomach flushing in the field
46
Appendix 8: Prey items found in the stomach of Megophryidae
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