STUDY ON THE POPULATION BIOLOGY OF SOLDIER (Osteogeneiosus militaris, Linnaeus 1758) IN THE COASTAL AREA OF PENANG.

By RADZIAH BINTI JANTAN

UNIVERSITI SAINS MALAYSIA 2014

STUDY ON THE POPULATION BIOLOGY OF SOLDIER CATFISH (Osteogeneiosus militaris, Linnaeus 1758) IN THE COASTAL AREA OF PENANG.

by RADZIAH BINTI JANTAN

Thesis submitted in fulfillment of the requirements for the Degree of Master of Science

UNIVERSITI SAINS MALAYSIA FEBRUARY 2014

ACKNOWLEDGEMENT

Pertama sekali, ucapan syukur tidak terhingga ke hadrat Illahi kerana dengan –Nya saya

dapat juga menyiapkan desertasi ini. Terlalu banyak dugaan serta cabaran dalam proses

menyiapkan penyelidikkan serta tesis ini. Saya tidak dapat menyangka akhirnya dapat

juga impian ini direalisasikan. Sepanjang proses penyediaan tesis ini, dorongan,

sokongan, doa serta kritikan yang membina yang banyak saya perolehi dari kedua ibu

bapa tercinta yang saya anggap sebagai tulang belakang kerna mereka sentiasa setia

berada bersama dikala jatuh bangunnya saya iaitu emak, Pn. Nor‟aini Manap dan ayah,

En. Mohd Yusof Jani, Mak Nah serta ahli keluarga di kampong. Tunjuk ajar yang tidak

putus-putus dari dua orang insan yang saya gelarkan mentor serta sifu iaitu penyelia saya,

Dr. Mansor Mat Isa dan Dr. Khairun Yahya bagi memastikan produk yang dihasil adalah

yang terbaik. Tanpa peluang serta kepercayaan yang diberikan oleh Dr. Mansor dan Dr.

Khairun, tidak mungkin saya mampu mencapai impian ini. Jutaan ribuan terima kasih

saya ucapkan. Antara nama-nama lain yang turut menyumbang jasa dalam kejayaan

desertasi ini termasuklah Dr. Amiruddin Shah serta pensyarah-pensyarah di USM

khususnya di PPSK yang sudi memberikan nasihat disaat saya menemui jalan buntu.

Kepada rakan-rakan yang sentiasa bersama ketika jatuh bangun saya, terima kasih saya

ucapkan; Rabiatul Adawiyah Abdul Mutalib, Khairani Amir, Kak Zue, Mohd Asyraf

Osman, Farah Alia Nordin, Ayun, Shafiq, Fatin, Aleeyanie, Kak Ayu, Adib, Farah,

Sham, Ruziah, Asyraf, Shafikah, Aziella, Wan Neeza dan Azman Aziz. Tidak dilupakan

Universiti Sains Malaysia, Perpustakaan Hamzah Sendut II serta warga Pusat Pengajian

Sains Kajihayat USM, terutamanya En. Nazri dan Miss Shantini, yang banyak

meyediakan kemudahan sepanjang penyelidikan saya ini dijalankan. Tanpa bantuan

3

kewangan USM Fellowship dari IPS USM serta Research University Grant Universiti

Sains Malaysia 304/PBIOLOGI/638147, penyelidikan ini tidak dapat dilaksanakan.

TABLES OF CONTENTS

Acknowledgement ii

Tables of Contents iv

List of Tables viii

List of Figures ix

List of Publication xii

Abstrak xiii

Abstract xv

CHAPTER 1: INTRODUCTION

1.1 General Overview 1

1.2 Objectives of Study 6

CHAPTER 2: LITERATURE REVIEW

2.1 Osteogenesis militaris 7

2.2 Length-Weight Relationship (LWR) 8

2.3 Relative Condition Factor (Kn) 13

2. 4 Reproductive Biology 14

2.5 Feeding Habits 17

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2.6 Growth 21

CHAPTER 3: METHODOLOGY

3.1 Samping Site And Sampling Techniques 25

3.2 Laboratory Work 25

3.2.1 Identification on Osteogeneiosus militaris 27

3.2.2 Length- Weight Relationship 27

3.2.3 Relative Condition Factor 29

3.2.4 Reproductive Biology 30

3.2.4.1 Maturity Stages 30

3.2.4.3 Sex Ratio 34

3.2.4.4 Length at First Maturity 34

3.2.4.5 Spawning Season 35

3.2.4.6 Fecundity 36

3.2.4.7 Oocytes-Size Frequency 36

3.2.5 Feeding Habits 37

3.2.6 Growth Parameter Estimation and Mortality Rate 40

3.2.6.1 Growth Parameters 40

3.2.6.1.1 Linkage Means 42

3.2.6.1.2 Ford-Walford plots 42

3.2.6.1.3 Powel- Wetherall 43

3.2.6.1.4 ELEFAN I 43

3.2.6.2 Mortality Parameters 44

3.2.6.3 Recruitment Pattern 44

3.2.6.4 Length at First Capture 45

3.2.6.4 Exploitation Status 45

CHAPTER 4: RESULTS

4.1.1 Length - Weight Relationship Osteogeneiosus militaris 46

4.1.2 Relative Condition Factor 50

4.1.3 Reproductive Biology 53

4.1.3.1 Maturity Stages 54

4.1.3.2 Sex Ratio 58

4.1.3.3 Length at First Maturity 60

4.1.3.4 Spawning Season 61

4.1.3.4 (a) Frequency of Maturity 62

4.1.3.4 (b) Gonadosomatic Index (GSI) 63

4.1.3.5 Oocyte – Size Frequency 65

4.1.3.6 Fecundity 67

4.1.4 Feeding Habits 67

4.1.5 Growth Estimation 71

CHAPTER 5: DISCUSSION

5.1 Length - Weight Relationship 82

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5.2 Relative Condition Factor 83

5. 3 Reproductive Biology 84

5.3.1 Sex Ratio 85

5.3.2 Spawning Season 85

5.3.3 Length at First Maturity 87

5.3.4 Fecundity and Mean size of eggs 87

5.4 Feeding habits 88

5. 5 Growth Parameter Estimation 91

5. 6 Mortality Parameter Estimation 93

5. 7 Recruitment Pattern 94

5. 8 Probability of Capture 94

CHAPTER 6: CONCLUSION

6.1 General Conclusion 95

6.2 Recommendation 99

REFERENCES 100

APPENDICES A Statistical Analysis for Length-Weight Relationship 125

APPENDICES B Abstract for Poster Presentation. 126

LIST OF TABLE

Table 3.0 Macroscopic characteristics of testis in O. militaris 31 modified from Kailola (2003), Murua et al., (2003), and Gomes and Araujo (2004).

Table 3.1 Macroscopic characteristics of ovaries in O. militaris 32 modified from Kailola (2003), Murua et al., (2003), and Gomes and Araujo (2004). . Table 4.0 Length and weight parameters with body group for 47 O. militaris in Southwestern part of Penang coastal waters from February 2009 to August 2010. . Table 4.1 Sex ratio data for O. militaris during the period of 59 February 2009 to August 2010 in southwestern part of Penang coastal water.

Table 4.2 The percentage of relative importance index (IRI%) 69 showing the importance food items that contain in the O. militaris’s stomach content from March 2009 until September 2009 in southern part of Penang coastal waters according to (a) sex and (b) length class.

Table 4.3 Summary of growth parameters values estimated from 71 different routine for O. militaris.

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LIST OF FIGURE

Figure 1.0 Landing trend of from 2000 to 2010 in Malaysia 3 waters; a) West coast Peninsular Malaysia; b) Penang waters.

Figure 2.0 Dorsal (a) and ventral (b) view of Osteogeneiosus militaris 10 found in Penang coastal waters.

Figure 2.1 Morphology of head and teeth of Osteogeneiosus militaris 12

Figure 2.2 Two type of teeth found in Ariidae species 19 (a) viliform; (b) globular

Figure 3.0 Standard measurements of bony fish. 26

Figure 3.1 Measurement for length of the gastro-intestinal 38 tract (GIT) in fish.

Figure 4.0 Frequency distribution for the mid length class SL 48 with 1.0 cm interval according to the sexes in O. militaris collected from February 2009 to August 2010 in the southwest Penang coastal water.

Figure 4.1 The length weight relationship of O. militaris in 49 parabolic form (a) immature, (b) female and (c) male.

Figure 4.2 Monthly data mean relative condition factor (Kn) 51 and total rainfall (mm) collected in Bayan Lepas represents the rainfall in southeast Penang coastal water from January 2009 to December 2010: (a) immature; (b) female; (c) male.

Figure 4.3 Mean relative condition factor (Kn) against 52 the length class SL for O. militaris from February 2009 to August 2010: (a) immature; (b) female; (c) male.

Figure 4.4 The gonad of immature O. militaris in threadlike shape. 54

Figure 4.5 Female gonad macroscopic examination for gonad 55 maturity stages identification on O. militaris

Figure 4.6 O. militaris’s gonad development in (i) immature 56 stage to (ii) maturing.

Figure 4.7 Male O. militaris with ripe eggs in mouth for oral incubation. 57

Figure 4.8 Male gonad macroscopic examinations for gonadal maturity 57 stages in O. militaris: MI – immature stage, whitish color with ribbon-like shape; MII – developing stage, gonad increase in size.

Figure 4.9 A logistic relationship between the numbers of reproductive 62 individuals expressed as a proportion of the reproductive population and standard length (cm) for O. militaris in the southwest Penang coastal water from February 2009 to August 2010.

Figure 4.10 The monthly frequency of maturity stages in female 62 O. militaris obtained from southeast Penang coastal water from February 2009 to August 2010.

Figure 4.11 The monthly frequency of maturity stages in male 62 O. militaris obtained from southeast Penang coastal water from February 2009 to August 2010.

Figure 4.12 Mean monthly in gonadosomatic index (GSI) (±SE) of 63 O. militaris from February 2009 to August 2010 in southeast Penang coastal water: (a) female; (b) male.

Figure 4.13 Mean monthly in gonadosomatic index (GSI) of O. militaris 64 and total rainfall (mm) from February 2009 to August 2010 in southeast Penang coastal water: (a) female; (b) male.

Figure 4.14 Frequency of oocytes diameter in O. militaris (a) female in 66 stage 3 (b) female in stage 4.

Figure 4.15 The monthly of von Bertalanffy plot from February 2009 73 to August 2010 for O. militaris generated from FiSAT software.

Figure 4.16 Linking mean routine from FiSAT software. 74

Figure 4.17 The Ford – Walford routine with the value of 74 L∞ = 44.61 cm and K = 0.18 years-1 were obtain from this routine.

Figure 4.18 Powell – Wetherall routine from FiSAT software to 75 generated the VBGF parameters; L∞ = 44.61 cm and K = 0.75 years-1.

Figure 4.19 ELEFAN I routine from FiSAT software to generated 76 VBGF parameters; (a) K Scan routine and (b) Response Surface routine.

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Figure 4.20 VBGF curve from ELEFAN I routine with different 77 value of starting length and starting sample indicating that the first cohort spawn in May and June.

Figure 4.21 Length converted catch curve routine from FiSAT 78 software to generated Z, M, F and E values.

Figure 4.22 The recruitment pattern estimated from FiSAT software to find 79 how many patterns of recruitment in one years of O. militaris could have. Figure 4.23 Probability capture routine from FiSAT software to estimated 80 length of fish captured.

Figure 4.24 Relative yield per recruit (Y’/R) and relative biomass per 81 recruit (B’/R) of O. militaris collected in southern part of Penang coastal waters. The value of B’/R = 75% is E0.1 = 0.407; optimum Y’/R (Emax = 0.487); B’/R = 50% is 0.287.

LIST OF PUBLICATION

1. Radziah, J., Mansor, M. I., and Khairun, Y. (2012). Length-weight relationship of Ariidae collected from southwest Penang coastal waters. South China Sea 2012 conference: sharing knowledge, resources and technologies for sustainable South China Sea at University of Malaya, 21-24 October 2012, Kuala Lumpur, Malaysia.

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KAJIAN POPULASI BIOLOGI IKAN DURI TEGAR MISAI (Osteogeneiosus militaris, Linnaeus 1758) DI KAWASAN PERRSISIRAN PANTAI PULAU PINANG

ABSTRAK

Satu kajian ke atas biologi populasi ikan duri marin daripada famili Ariidae telah dijalankan di kawasan pinggir pantai Pulau Betong di Pulau Pinang telah dikaji. Kajian tersebut telah dijalankan dari Februari 2009 sehingga Ogos 2010. Kajian ini melibatkan beberapa aspek biologi seperti hubungan antara panjang dan berat (LWR), kondisi ikan

(Kn), tabiat pemakanan, biologi pembiakan dan maklumat pertumbuhan. Persamaan

LWR bagi ikan betina, jantan dan yang belum matang adalah W=0.01L3.095;

W=0.027L2.763 dan W=0.013L2.975, masing-masing. Nilai Kn adalah melebihi 1 menunjukkan O. militaris dari kawasan Pulau Betong berada dalam keadaan yang baik.

Analisa panjang salur pemakanannya pula menunjukkan O. militaris adalah omnivor

(GIT = 1.62). Jenis makanan yang dijumpai di dalam perut O. militaris termasuklah panaeids, ophiurids, holothuroids, Setipinna spp., bivalvia, ketam brachyuria, rangka ikan, nematodes, telur ikan, isopoda and otolith ikan dan organism yang tidak dapat dikenalpasti,. Keputusan daripada kajian pembiakan pula menunjukkan musim bertelur

O.militaris adalah berlaku sepanjang tahun. Walau bagaimana pun kemuncak bagi aktiviti pembiakan bagi spesies ini dijumpai berlaku pada Jun - Julai 2009, Disember

2009 - Februari 2010. Panjang badan pada tahap kematangan pertama populasi O. militaris adalah 25.5 cm SL. Julat diameter telur pula adalah dari 4.5-11.5 mm per ovary di peringkat kematangan 3 dan 19-39 biji telur per ovary bagi peringkat kematangan 3 sehingga 18-49 biji telur per ovary bagi peringkat kematangan 4. O. militaris mengambil masa selama 10 tahun untuk mencapai panjang 37.03 cm. Penganggaran parameter

pertumbuhan dan kematian bagi O. militaris ialah Lmax=30.88 cm; L∞=37.03 cm;

Lc=21.40 cm; K=0.37 year-1; ø’ =2.64; Z=1.23 years-1; M=0.75; F=0.49. Kadar ekspoitasi yang dianggarkan ialah E =0.39 atau 39%, rendah dari B‟/R (E0.1=0.41) atau dari nilai

Y‟/R (Emax=0.49).

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STUDY ON THE POPULATION BIOLOGY OF SOLDIER CATFISH (Osteogeneiosus militaris, Linnaeus 1758) IN THE COASTAL AREA OF PENANG

Abstract

A study on population biology of marine catfish of the family Ariidae, Osteogeneiosus militaris was conducted from Pulau Betong in southwestern part of Penang. The study was conducted from February 2009 to August 2010. This study includes the biological aspects such as length-weight relationship (LWR), relative condition factor (Kn), feeding habits, reproductive biology and growth determination. The LWR equation obtained for female, male and immature O. militaris were W=0.01L3.095; W=0.027L2.763 and

W=0.013L2.975, respectively. The value of Kn is more than 1 showing that O. militaris in

Pulau Betong were having a good body condition. Analyses of the gastro-intestinal tract length shows that O. militaris having omnivorous feeding habits (GIT=1.62). The food items found in the stomach of O. militaris comprised of, panaeids, ophiurids, holothuroids, Setipinna spp., bivalves, brachyurans crab, fish skeleton, nematode, fish eggs, isopoda, fish otolith and unidentified organism. Result from the reproductive biology shows that the spawning period for O.militaris occurred throughout the year.

However, spawning peak for this species were detected in June - July 2009 and

December - February 2010. Length at first maturity for population of O. militaris in Pulau

Betong is at 25.5 cm SL. The oocytes diameter ranged from 4.5-11.5 mm and the fecundity were ranged from 19-39 eggs per ovaries in stage 3 and from 18-49 eggs per ovaries in stage 4. O. militaris takes about 10 years to attains the length size of 37.03 cm.

Growth and mortality parameter estimation for O. militaris were Lmax=30.88 cm;

L∞=37.03 cm; Lc=21.40 cm; K=0.37 year-1; ø’ =2.64; Z=1.23 years-1; M=0.75; F=0.49.

The exploitation rate estimated from length converted catch curve (E =0.39 or 39%) lower than the B‟/R (E0.1=0.41) or in Y‟/R (Emax=0.49).

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CHAPTER 1: INTRODUCTION

1.1 General Overview

Fishery sector is one of the important contributors to Malaysia‟s economy‟s growth.

Many sectors gain advantages from the marine resources directly or indirectly. Young

(2006) reported that fisheries sector in Malaysia not just contributed 1.54% to Gross

Domestic Production (GDP) and has been recognized as the major protein source.

Malaysia Adult Nutrition Survey (MANS) (2008), also reported that fish has been highly consumed daily by urban and rural Malaysian adults (Nurnadia et al., 2011).

According to the Fishery Department of Malaysia (2007), 80.5% of the fishery sources for fish as food come from the marine capture fishery and follow with 19.5% from the aquaculture sector. Generally marine resources are renewal resources. However this resource is overexploited which cause depleted (King, 1995; Kolbert, 2008). Thus it will take longer time for the fish stock to recovery back to its nature state.

Marine of the family of Ariidae are among the fish landed in Malaysia. Ariidae inhabits in estuarine and marine environment in tropical and subtropical region (Giarrizzo and Saint-Paul, 2008; Yáñez-Arancibia and Lara-Dominguez, 1988). They are characterized as eurythermal and euryhaline species where some live primarily in sea and some strictly in freshwater with little tolerance to brackish or marine condition (Yáñez-

Arancibia and Lara-Dominguez, 1988). They are locally abundant in mangrove areas,

large rivers, and in turbid waters (Kent and Niem, 1999). The distribution of Ariidae are widespread in continental shelves of Atlantic, Indian and Pacific oceans (Acero and

Betancur, 2007; Ferraris, 2007; Nirchio et al., 2010).

Ariidae are normally caught by gill nets, trammel nets and barrier nets thus it contribute to the socio – economics of the artisanal fisheries. Even though Ariidae is not in the group of the high demand of fishes in the market in contrast to other commercial fishes like lutjanids, carangids, serranids and the catfish-ell like (Plotosus sp.) but Ariidae is considered the cheapest and affordable sources of protein for the middle to poor class consumer. In India, Ariidae are among the important commercial fishes (Jayaram, 1986;

Vidthayanon, 1998; Jalal et al., 2012). According to Menon (2004), Ariidae are utilized in various form of fresh, processed, dried and salted.

In Figure 1.0 (a) shows landing trend of ariids in Malaysia for eighteen years and there is no sign of drastic drop for marine catfish. However there was a decrease in the annual catch of marine catfish in Penang (Figure 1.0 (b)), especially in 2005 then followed with high quantity of catch in 2007. This might be due tsunami phenomena occurred in 2004.

Such incident requires knowledge on the biological information of that certain species in order to understand more about the behavior and causes of the sudden incident.

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a)

9 8 7 6 5 4 3 2 1 0 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010

Ariidae Landing ( x1000 Tonne metric) Tonne ( x1000 Landing Ariidae Year

b)

9 8 7 6 5 4 3 2 1

0 Ariidae Landing ( x1000 Tonne metric) Tonne ( x1000 Landing Ariidae year 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 Year

Figure 1.0 Landing trend of Ariidae from 2000 to 2010 in Malaysia waters; a) West coast

Peninsular Malaysia; b) Penang waters.

As the world starting to change rapidly through the climate, environment and resources thus this also give significant effect on the species. The results can be seen in the size of the population either the species can tolerate with the changes or extinct. Apart from that, human activities such over-fishing, habitat destruction and pollutions give a significant contribution on the changes of growth in the species population size (Cheung et al.,

2009).

Information on biological aspects of species is a major concern and fundamental for future management purposes. This information includes the diet of the species, the spawning season, age at the first maturity, type of growth models and the status of the population. Apart from that length – weight relationship (LWR) provide fundamental information on the fish biology. LWR parameters are used to generate other components of population dynamics which in return used for fish management program. All the biological information is used for the conservation and management program of the species. Furthermore in aquaculture sectors, the information is used to show the performance of the fishes.

Various studies have been done on Ariidae species from different part of the region. For instances many researches on marine catfishes biology come from the Indian waters includes study on barbells of Arius thalassinus (Kapoor and Bhargava, 1967), biology information of Tachysurus tenuispinis in Visakhapatnam (Dan, 1977) and A. caelatus and

O. militaris from Mumbai (Raje, 2006). Another study was conducted to find out the

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vulnerability of catfish in terms of the diet, growth and reproductive biology to the fishing activities in Mumbai (Raje and Vivekanandon, 2008). Gunamickrama (2009) conducted a morphometric analysis study on Arius jella from five different estuaries in

Sri Lanka.

Other researches on Ariidae in another part of the region such as in New Guinea and

Australia (Kailola, 1990), Colombia (De la Hoz, 2009; Duarte, 1999), Mexico (Tenorio –

Colin et al., 2010; Yáñez-Arancibia and Lara-Dominguez, 1988), Malaysia (Lim 1994;

Jalal et al., 2012; Mansor et al., 2012; Singh, 2003), Brazil (Barbieri et al., 1992;

Giarrizzo et al. 2006; Haimorici and Velasco, 2000), Philippine (Garcia, 2010),

Venezuela (Etchevers, 1978) and Africa (Ecoutin et al., 2005; Harrison, 2001).

Ecology study have been done on three marine catfishes (A. felis, A. melanopus and

Bagre marinus) in tropical coastal ecosystem in southern Gulf of Mexico to find out the distribution and abundance, feeding habits, and spawning season has been conducted by

Yáñez-Arancibia and Lara-Dominguez (1988). Singh (2003) study the biology of the estuarine Ariidae in Matang mangrove and generated a key for the eight species. Warburton (1978) estimated the age and growth of marine catfish by using the otolith. Among other studies covered on Ariidae includes feeding analysis (Tommaso and

Saint – Paul ,2008), reproductive biology (Mansor et al., 2012) and parasits in Ariidae

(Lim, 1994). Phylogenetic study on Ariidae is controversial due to the number of species and genera uncertain thus many researches were covered to entangled the issues (Tenorio

– Colin et al., 2010; Sczepanski et al., 2010).

1.2 Objectives of study

The fluctuation trends on Ariidae landing give the significance starting point to initiate the study on the biology information for the management and conservation purposes.

Apart from that, the information regarding the information on population biology of

Osteogeneiosus militaris in southwest Penang coastal waters somehow still scanty.

The main objectives of the present study include:

1) To study the length-weight relationships and condition factors for soldier catfish,

Osteogeneiosus militaris.

2) To study the diet of the soldier catfish, O. militaris and their relation between

length, sex and season

3) To determine the spawning season, fecundity, sex ratio and length at 1st maturity of

O. militaris.

4) To determine the growth parameters, mortality rate, recruitment pattern, length at

1st capture and the exploitation rate of O. militaris.

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CHAPTER 2: LITERATURE REVIEW

2.1 Family Ariidae

Catfishes belong to order Siluriformes contain about 3088 species of 36 families (Burton,

1996; Acero and Betancur, 2007). Ariidae can be found in tropic of areas of South

America, Africa and Asia (Burton, 1996; Acero and Betancur, 2007; Ferraris, 2007).

Only Ariidae and Plotosidae are predominantly marine family. Marine catfish from the family Ariidae contain 133 species and 26 genera.

Ariidae is one of the earliest catfish family found in the fossil record (Kailola, 1990;

Burton, 1996). The ability to adapt very wide range of salinity is one of the remarkable characters that contribute to their abundance and global distribution. Another modification that contributed the success of its existence is the oral incubation during the spawning season by male (Kailola, 1990; Bruton, 1996). Among other reproductive behavior such guarding nesting site and burrowing the fertilized eggs, this method allow

Ariidae species to disperse effectively to wide range of space and habitat.

Cylindrical body shape in cross section, naked skin, complete lateral line, has pairs of whiskers or barbells and dorsal and pectoral fin equip with sharp spine are few characters belong to the marine catfish. Catfishes show greatest adaptation to the stagnant condition.

The carnivores species of catfish which lives at the bottom and muddy areas, they often have small eye and used barbells to detect foods, danger and other stimuli. As a bottom dweller, their swim bladder is reduced and depressed body form (Marshall, 1971).