DIET OF TADPOLES AT THREE LOCALITIES IN SARAWA!{

Sandra James Tinggom

Bachelor of Science with Honours (J. ( Resource Science and Management) 668 E2 2005 5194 2005 P.KHIDMAT MAKLUMAT AKADEMIK UNIMAS ~usal Khidmal MaklUmal Akaoerr UNIVERSITI MALAYSIA SARAWA 1111111111111111111 111111111 Q4)no KOla Samarahan 1000143775 DIET OF TADPOLES AT THREE LOCALITIES IN SARA W AK

SANDRA JAMES TINGGOM

This project is submitted in partial fulfillment ofthe requirements for the degree of Bachelor ofScience with Honours (Animal Resource Science and Management Program)

Faculty of Resource Sciences and Technology UNIVERSITI MALAYSIA SARA W AK 2005

QL I

DECLARATION

No portion of the work referred to in this dissertation has been submitted in support of an application for another degree of qualification of this or any other university or institution of higher learning.

Sandra James Tinggom

Program of Animal Resource Science and Management

Faculty of Resource Sciences and Technology

University Malaysia LIST OF FIGURES

FIGURE 1: Study site in Kubah National Park. 7

FIGURE 2: Study site in Gunung Gading National Park. 8

FIGURE 3: Cluster analysis based on overlap data on diet of representative tadpole

from all the three sites (Gunung Gading, Kubah and Desa Ilmu). 24

FIGURE 4: Cluster analysis based on overlap data on diet of representative tadpoles

in Gunung Gading National Park. 29

FIGURE 5: Cluster analysis based on overlap data on diet of representative tadpoles

in Kubah National Park. 31

FIGURE 6: Cluster analysis based on overlap data on diet of representative of

tadpoles in Desa Ilmu. 33 LIST OF TABLES

TABLE 1: Raw collection data of tadpoles and their localities. 9

TABLE 2: Data on tadpoles collected from three sites in Sarawak. 15

TABLE 3: Summary ofdietary composition based on gut samples of tadpoles from

localities in Sarawak. 19

TABLE 4: Summary ofthe food types and feeding strategies in larval

families. 20 LIST OF APPENDICES

FIGURE 1: Surface feeding type, represented by Megophrys nasuta. Gosner Stage

23-25, total length 24.52 mm. Top: view of body; Bottom: view of oral

disc, showing funnel-like structure. I

FIGURE 2: Generalized type, represented by Rana chalconota. Gosner Stage 26, total

length 26.9 mm. Top: view of body; Bottom: view of oral disc. I

FIGURE 3: Mountain-stream type, represented by Meristogenys sp. Gosner Stage 26,

total length 20.6 mm. Top: view of body, Bottom: view of oral disc,

showing ventral sucking type. II

FIGURE 4: Images of selected larval stages of from this study. III

l TABLE 1: Tadpole species collected from three sites in Sarawak. IV

TABLE 2: Presence and absence offood types from the gut of tadpoles. VI

TABLE 3: Frequency of food types from the gut of tadpoles. VII

TABLE 4: Summary of26-46 developmental changes oftadpoles as described by

Gosner (1960). IX

TABLE 5: Data on the food types identification for each tadpole species. X

TABLE 6: Result ofthe proximity analysis of different food types based on overlap

data on diets from Kubah National Park, Gunung Gading National Park and

Desa Ilmu. XXII

TABLE 7: Result of the proximity analysis of different food types based on overlap

data on diets from Kubah National Park. XXIII

TABLE 8: Result of the proximity analysis of different food types based on overlap

data on diets from Gunung Gading National Park. XXIV

TABLE 9: Result of the proximity analysis of different food types based on overlap

data on diets from Desa Ilmu. XXIV ACKNOWLEDGEMENTS

Thanks are due to Datuk Cheong Ek Choon, Controller of National Parks and Nature

Reserves, and Bolhan Budeng, Sarawak Forest Department, for permits. Personally, I would like to extend my outmost appreciation and gratitude to my supervisor, Assoc.

Prof. Dr. Indraneil Das for his dedication, constant guidance and support, time and hard work. Besides, I would also like to express my sincerest thanks to my co­ supervisor, Mdm. Ramlah Zainuddin -for her time to proof-read and advice. Field work was funded by a grant from Volkswagen Stiftung, Germany (Grant Number 1/79405).

My thanks also goes to field-mates, Ms. Lily Sir, Ms. Cynthia Boon, Ms. Sylvia Ng,

Mr. Castro Michael, Mr. Andre Jankowski and Prof. Alexander Hass who have been there through 'thick and thin' . My thanks also go to Mr. Wan Hairulhaizal Wan

Halkap, the Lab Assistant for his time, cooperation and patience, and Mr. Jeet

Sukumaran for his help in computing data. Last but not least, those who have given support and encouragement in a way or another, a very big Thank You. · ~usat Khidmat Mak.umat Akademr& UNIVERSITI MALAYSIA SARAWA¥ Q4100 KOla Samar(lhan

TABLE OF CONTENTS

ABSTRACT 1

1.0 INTRODUCTION 2-4

2.0 LITERA TURE REVIEW 4-6

3.0 OBJECTIVE 6

4.0 MATERIALS AND METHODS 6-13

4.1 METHODS

4.11 Study Sites

4.12 Sampling Period

4.13 Sampling Techniques

4.14 Food Sample Identification

4.15 Fixation

4.2 MATERIALS

5.0 DAT A ANALYSIS 14

6.0 RESUL TS AND DISCUSSION 15-33

7.0 COMPARISON WITH PREVIOUS 34-35

STUDY

8.0 CONCLUSIONS 36-37

9.0 RECOMMENDATIONS 38

10.0 REFERENCES CITED 39-42

11.0 APPENDICES I-XXIV Diet of Tadpoles at Three Localities in Sarawak

Sandra James

Animal Resource Science and Management Program Faculty of Resource Sciences and Technology Universiti Malaysia Sarawak

ABSTRACT

A study on Bomean tadpoles was conducted on fieldworks basis from August 2004 to October 2004. The tadpole collection was done from three collection sites; two were from forested area, namely Gunung Gading National Park and Kubah National Park. The other site was at a human settlement area; Desa Ilmu, Kota Samarahan, Sarawak. Five representative families of tadpoles, , Bufonidae, Microhylidae, Ranidae and were collected during this sampling period. The contents of the gut of tadpole identified showed that there was a major overlap of ingested food and blue-green algae were ingested, the most (42%). Resource partitioning were practiced by tadpoles and diet composition was affected by feeding strategies, mouth parts, stages of organisms and the type of environment the organism lives in.

Key words: tadpoles, forested area, human settlement, blue-green algae, resource partitioning

ABSTRAK

Satu kajian mengenai berudu di telah dijalankan berdasarkan kerja lapangan dari Ogos 2004 hingga Oktober 2004. Persampelan berudu telah dijalankan di tiga kawasan; di mana dua daripadanya terdiri daripada kawasan hutan iaitu Taman Negara Gunung Gading dan Taman Negara Kubah. Tempat persampelan ketiga telah dija/ankan di kawasan dengan penempatan penduduk, Desa llmu, Kota Samarahan, Sarawak. Lima famili yang mewakili berudu telah berjaya diperoleh, Megophryidae, Bufonidae, Microhylidae, Ranidae dan Rhacophoridae dalam jangkamasa kerja lapangan dijalankan. Kandungan perut berudu yang dicamkan menunjukkan terdapat pertindihan dalam jenis makanan dan alga biru hijau adalah makanan yang paling tinggi dicerna (42%). Berudu didapati mengamalkan 'resource partitioning' dan pemilihan komposisi makanan dipengaruhi oleh keadah pemakanan, morfologi mulut, peringkat pertumbuhan dan habitat berudu.

Kata kunci: berudu, kawasan hutan, penempatan penduduk, alga biru hijau, 'resource partitioning'

1 1.0 Introduction:

Amphibians are intermediate in some ways between the fully aquatic fish and the terrestrial amniotes. The term 'amphibian' can be interpreted in two ways, firstly, as an animal spending part of its life in water and subsequently changing to an aquatic adult, or as an animal that alternates life in and out ofwater, such as the so-called pond (Duellman and Trueb, 1985). Amphibians can be defined as quadrupedal vertebrates having two occipital condyles on the skull and not more than one sacral vertebra. The skin is glandular and lacks epidermal structures, i.e., scales, feathers and hair. In frogs, the postsacral vertebrae are fused into a single rodlike element, the coccycx, the tail is absent and the hind limbs are elongated and modified for jumping.

The skin is highly glandular and contains both mucous with glandular (poison) glands.

However, true claws are absent but horny tips are present on the toes of some frogs.

The internal structure of living amphibians is intermediate between fishes and amniotes. The heart has two artria, a single ventricle that may be partially divided; and a distinct conus arteriosus with several valves with symmetrical aortic arches.

Amphibians have pedicellate teeth and specialized papillae in the inner ear and anurans have green rods in the retina of the eye. Typical frogs have several modes of reproduction, which include direct development of terrestrial eggs, ovoviviparity and viviparity. Most species of frogs have external fertilization. All amphibian eggs must develop in moist conditions although they have numerous protective mucoid capsules.

This is because the capsules are highly permeable. The eggs lack a shell and the embryonic membranes, i.e., amnion, allantois and chorion of higher vertebrates. In those amphibians that have aquatic larvae, the larvae undergo metamorphosis into the adult form that caused a dramatic change in frogs (Duellman and Trueb, 1985).

2 Tadpoles can be termed as the transition of newly hatched organism to an adult with several accompanying changes. Amphibians are different from other vertebrates as their development can be divided into two stages, a larval stage and an adult stage. The process that lies behind each life cycle of an amphibian is called metamorphosis. It is a postembryonic period of profound morphological changes by which the animal alters its mode of living and is known to occur in all major living groups except amniotes (Shi, 1999). Unlike most adult amphibians, tadpoles are easily found and can be seen by day (Anstis, 2002). Tadpoles are species-specific organism in modes of feeding and niches and are sensitive towards their environment.

Tadpoles morphological changes are affected by light, salinity, temperature, food supply; externally and hormonal changes, changes in yolk reserves; internally (Shi,

1999). They show direct-development and stay within the egg capsules or shells until their development is complete and hatches as a replicate of their adult. (Zug, 1993). In addition, tadpoles possess a mechanism for extracting suspended particles of food from water. (Kenny, 1969b, Severtzov, 1969; Wassersug, 1972). The adult is short­ bodied and usually tailless, while the larva possesses tail and usually well-developed caudal fin in order to propel itself through the water (Duell man and Trueb, 1985).

In this study, tadpoles were collected from the forested and non-forested habitats at three localities in Sarawak, western Borneo: Kubah National Park, Gunung

Gading National Park and Desa Ilmu, Kota Samarahan from habitats such as streams, including torrents, riffles, shingles, open pools, side pools, potholes, seepage areas and pools of intermittent stream.

3 There is a general shortage of information on the tadpoles of Borneo. The most substantial work has been that of Inger (1985, 1986), but there have not been much subsequent documentation on the subject. As suspected by Inger, tadpoles possess more morphological characteristic that are destroyed in preservatives, compared to adult frogs, making manipulation of preserved specimens difficult.

Studies on diet on free-living tadpoles are relatively rare, compared to those of adult amphibians, and one specific for Borneo is that of Inger (1986). Elsewhere, workers have looked at diets of extralimital species (Inger, 1986).

2.0 Literature Review:

Resource partitioning is thought to be the basis of syntopy of closely-related species, Whereby the niche (such as diet, microhabitat or use of time) of each species differ from all the niches used by other species, reducing competition for food, space and time, and provides evidence of competition (Campbell, 1997). Competition may cause tadpoles to switch their niches and evolve behaviour and morphologies that allow them to use different ranges of resources and aid in the survival of the species for exploitation of new ecological niches (Shi, 1999). Tadpoles possess morphological specializations that are related to the size or kind of food ingested. Their specialized feeding habits require mouthparts and a digestive system that is typically different from the adult frog. Inger (1986) found that primary ingested food of Bornean tadpoles were algae (mainly blue-greens), diatoms, fungi, ciliates, euglenoids, amoebae, miscellaneous protists, tracheoid plant fragments, rotifers, insect and crustaceans. The

temal morphology and function of the buccopharyngeal portrays the feeding strategies that each tadpole possesses. Among the feeding types that tadpoles possess

4 are obligate benthic (Ranidae), macrophagous (Megophyridae), midwater suspension

(Rhacophoridae and Microhylidae), surface film (Megophryidae and Microhylidae),

and bottom suspension feeders (Ranidae and Bufonidae) (Duellman and Trueb, 1985;

Inger, 1986).

The external morphology of a tadpole that are of systematic value includes,

nares (nostrils), eyes, spiracle, vent tube, tail musculature, tail shape, oral disc and

pigmentation. Oral disc is one of the major diagnostic character identification of

tadpoles. It includes the upper and lower labia, jaw sheaths, papillae and tooth rows.

According to Wassersug (1980), internal morphology can be used to infer

feeding strategies. Therefore, it can be used to describe the type of microhabitat and

behaviour, which is highly correlated with the external morphology (Duellman and

Trueb, 1985; Inger, 1986). Orton (1953) defined seven adaptive types (including direct development) of tadpoles based on position and size of mouth, and development of the

caudal musculature and fins.

In this study, Cluster Analysis was used to analyse the data on diets in tadpole communities. Jaccard Index is represented by Cj value for estimating differences among food resources between cooccurring species. Jaccard index can be calculated with the following;

Cj = j / ( a + b - j ) ; where

j = number of resource states in common between two species

a = number of resource states in species A

5 b = number of resource states in species B

3.0 Objective:

The purpose of this study is to investigate the different types of food ingested

among tadpoles and the differences of food types ingested between species.

4.0 Material and Methods:

4.1 Study sites:

4.1.1 Kubah National Park

Kubah National Park is located at 10 36'396" to the North and 1100 11 '323" to

the East; approximately 20-22 km on the north - west side of Kuching; at the ridge of

Gunung Serapi massif. It is the main water catchment area for the Rayu River; mainly

"

consisting sand and mud deposited alluvium. The Park consists of fairly steep terrain;

with streams and drains flanking the mountain. The altitude ranges between 20 and

777 m above sea level. It is covered by kerangas (heath) forest with some pitcher plant

species and is drained by Sungei Rayu. Above 300 m from the sea level, peaty soils

are common and the soil development is greatly affected by high water availability at

these altitudes (Hazebroek & Abang Kashim, 2000). At Kubah, the tadpoles were

collected at different elevations ranging from 152.4 m to 298.4 m above sea level.

6

l FIGURE 1: Study site in Kubah National Park.

(Hazebroek & Abang Kashim, 2000).

4.1.2 Gunung Gading National Park

Gunung Gading National Park consists of an isolated mountain on the west of the town of Lundu. It is located 1°41 '715" to the North and 109°50'498" to the East with an approximate of 37 miles on the west of Kuching. The park has many clear streams to form the Lundu River. It consists of primary rain forest. The park is rich with beautiful beaches along side with flora and fauna inhabiting the area. Among those is the Rajjlesia tuan-mudae, stem fig trees, small mammals and invertebrates

(Hazebroek & Abang Kashim, 2000). At Gunung Gading, the tadpoles were collected from different elevations ranging from 16.8 m to 94.2 m above sea level.

7 FIGURE 2: Study site in Gunung Gading National Park.

(Hazebroek & Abang Kashim, 2000).

4.1.3 Desa IImu, Kota Samaraban, Sarawak

The tadpoles were collected from human habitation and land clearing site with an elevation of 13.4 m above sea-level; 1° 27' 377" to the North and 110°27'341" to the East.

4.2 Sampling Period

Field surveys were done from August to October 2004 on a weekly basis from

Friday to Sunday. Collection dates and places visited were shown in Table 1.

8 TABLE 1: Raw collection data of tadpoles and their localities.

Field No. Species Collection Locality

IDates

001 Rana 12 August 2004 Waterfall 1, Gading

chalconota; National Park,

Ranidae Elevation: 16.7 m I I o1.41 .S17N/l 09 .SO.S98E

002 Megophrys 12-13 August Stream behind waterfall 1,

nasuta; 2004 Gunung Gading National

Megophryidae Park,

Elevation: 94.1 m

01.41.71SN/I 09 .SO.498E

003 Meristogenys ' 12-13 August Stream behind lodge,

sp.; Ranidae 2004 Gunung Gading National

Park,

Elevation: S2.1 m

01.41.476N/I09.S0.788E

004 Fejervarya IS August 2004 Isolated drain by roadside,

cancrivora; Desa Ilmu, Kota

Ranidae Samarahan, Sarawak.

Elevation: 13.4 m.

01.27.377NIl1O.27.341E I OOS Bufo IS August 2004 Isolated drain by roadside, I I I melanostictus; Desa Ilmu, Kota

Bufonidae Samarahan, Sarawak.

9 Elevation: 13.4 m

01.27.377NIlI0.27.341E

006 Ferjevarya 15 August 2004 Isolated drain by roadside,

II'Imnoc h ans;' Desa Ilmu, Kota

I Ranidae Samarahan, Sarawak.

Elevation: 13.4 m

01.27.377NIlI0.27.341E

007 Megophrys 18 September Hill stream,

nasuta; 2004 Kubah National Park,

Megophryidae Matang, Sarawak.

Elevation: 298.4 m

01.36.396N/II0.11.323E

008 Rhacophorus 18 September Kidney shaped pool,

pardalis; 2004 Kubah National Park,

Rhacophoridae Matang, Sarawak.

Elevation: 265.8 m

01.36.394NIl 10.1 1.344E

10 009 18 September Kidney shaped pool,

otilophus; 2004 Kubah National Park,

Rhacophoridae Matang, Sarawak. I

Elevation: 265.8 m

01.36.394NI11O.11.344E

010 Leptobrachium 18 September Hill stream,

abbottii; 2004 Kubah National Park,

Megophryidae Matang, Sarawak.

Elevation: 298.4 m

01.36.396N/IlO.11.323E

011 Megophrys 18-19 September Stream behind lodge,

nasuta; 2004 Kubah National Park,

Megophryidae Matang, Sarawak.

Elevation: 152.4 m I

I 01.36.706N/IlO.11.717E

012 Microhyla sp.; 28 October 2004 Picher plant cup,

Megophryidae Kubah National Park,

Matang, Sarawak.

Elevation: 235.6 m

01.36.397N/IlO.11.343E

11 4.3 Sampling Techniques

Tadpoles were collected with tray nets or other nets and placed in a plastic aquarium or mineral water bottles for rearing. Sampling sites include waterfall, stream, ditches, potholes, pig wallow and drains. The tadpoles were captured during the day or at night. They were anesthetized with Tricane or MS 22 before photographs were taken. After capture, the anesthetized tadpoles were preserved since the measurement

of body and fins may change after capture (Anstis, 2002). The samples consisted of

about 20 individuals for dietary studies. Tadpoles ranging from Stages 30-36 are

suitable for morphological description and identification (A. Haas, pers. comm.). Some

tadpoles that could not be identified on site will be taken back to the laboratory for

identification. The feeding behaviour was determined through observations on position

of mouth parts, as defined by Orton (1953). Tadpoles were identified based on Inger

(1985), Malkmus et at. (2002) and Inger and Stuebing (2005). Gosner Tables (1960)

were used to determine the stage of tadpoles for the purpose of identification.

4.4 Food Sample Identification

The foregut of a tadpole close to the esophagus was cut and its contents teased

on to a glass slide or petri dish. Gut wall and visible portions of lining were removed

with several drops of distilled water. The gut contents were spread as thinly as

possible; a cover slip placed over it and the edges sealed. Each smear was observed

within a few days of preparation using a compound microscope. The remainder that

could not be identified will be placed in a cryogenic vial containing 4% buffered

formalin. The identification of food types were based on Jahn et at. (1949), Prescott

12 (1951), Prescott (1954), Webb et al. (1975), Pennak (1989), Shanna (1989) and

Lokman (1991).

4.5 Fixation

For identification purposes, tadpoles were stored in a 4% buffered formalin solution; with a dilution of 1:9 of 39-40% fonnaldehyde stock solution (Tyler, 1963).

Some voucher specimens were kept for future studies: for molecular studies, the specimens were kept in 4% ethanol. Specimens were anesthetized before being preserved.

4.2 Material:

1.0 Tray nets and other nets

2.0 Chemicals for fixing; 4% Fonnaldehyde and Ethanol

3.0 Empty Mineral water bottles

4.0 Dissecting Set

5.0 Measuring tape (in m)

6.0 Plastic vials

7.0 Plastic zip-lock bags

8.0 Camera (SLR)

9.0 Stereoscopic microscope

10.0 Swift Compound microscope (10/0.25)

11.0 GPS

13 5.0 Data Analysis:

Data being analyzed based on observation both in the field and laboratory include:

1.0 Date and time

2.0 Name of observer/collector

3.0 Locality description

4.0 Habitat description

5.0 Behavioural description, for example feeding behaviour

6.0 Identification of food types

Data was analyzed using SPSS Version 11.5 for Cluster Analysis using Jaccard

Index to measure the similarities between species described by presence-absence attributes (Jacquard, 1908).

14 6.0 Results and Discussion

A total of 12 types of tadpole samples representing 5 families, Megophyridae,

Bufonidae, Mirohylidae, Ranidae and Rhacophoridae (Table 2). Megophryidae consisted of Lep/obrachium abbotti and Megophrys nasuta; Bufonidae consisted of

Bufo melanostic/us, Microhylidae consisted of Microhyla sp.; Ranidae consisted of

Fejervarya cancrivora, Fejervarya limnocharis, Meristogenys sp. and Rana chalconota and Rhacophoridae consisted of Polypedates otilophus and Rhacophorus pardalis.

TABLE 2: Data on tadpoles collected from three sites in Sarawak.

Species Locality(s) Microhabitat type

Family Megophryidae

Leptobrachium abbottii Kubah National Park, Hill stream

Cochran Matang, Sarawak.

Megophrys nasuta Schlegel Gunung Gading National Isolated portions of slow

Park and Kubah National or fast-flowing streams

Park, Matang, Sarawak.

Family Bufonidae

Bufo melanostictus Desa Ilmu, Kota Drain

Schneider Samarahan, Sarawak.

Family Microhylidae

Microhyla sp. Kubah National Park, Pitcher-plant cup;

Matang, Sarawak. Nepenthes sp. I

•

15