A STUDY OF THE BIOLOGY AND ECOLOGY OF THE BLACK SPONGE CHONDROSIA SP.

COLONIZATION IN SEMPORNA ISLANDS, AND ITS IMPACT

ON THE REEF ECOSYSTEM

AMIRIN @ ADRIAN ANGKA. JI

3`.,

L. I'.

\ýý'.. "'ýC

U'ý3YýtRS1Tl ýý: ii. tý'ý°J. LA

JASAH

THESIS SUBMITTED IN FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF

MASTER OF SCIENCE

BORNEO MARINE RESEARCH INSTITUTE UNIVERSITI MALAYSIA SABAH

KOTA KINABALU 2007

UNIVERSITI MALAYSIA SABAH

BORANG PENGESAHAN STATUS TESIS°

JUDUL :A STUDY OF THE BIOLOGY AND ECOLOGY OF THE BLACK SPONGE CHONDROSIA SP. COLONIZATION IN SEMPORNA ISLANDS, AND ITS IMPACT ON THE REEF ECOSYSTEM.

IJAZAH : SAR)ANA SAINS (SAINS MARIN).

SESI PENGA]IAN : 1998-2006

Saya, A]IRIN @ ADRIAN ANGKAII mengaku membenarkan tesis Sarjana ini disimpan di Perpustakaan Universifi Malaysia Sabah dengan syarat-syarat kegunaan seperä berikut:

1. Tesis adalah hak milik Universiti Malaysia Sabah. 2. Perpustakaan Universiti Malaysia Sabah dibenarkan membuat salinan untuk

tujuan pengajian saya. 3. Perpustakaan dibenarkan membuat salinan tesis ini sebagai bahan pertukaran

antara Institusi Pengajian Tinggi 4. TIDAK TERHAD.

Disahkan oleh

(Penulis: AIIRI IIRI

l

m ADRIAN ANGKAJI) (TANDATANGAN PUSTAKAWAN)

Alamat: P. O. BOX 680, 89208, Tuaran, Sabah, MALAYSIA.

(Penyelia: Prof. Dr. Hj. Ridzwan Abdul Rahman)

13"0ioSaool . Tarikh: 8 Ogos 2007 Tarikh:

CATATAN: Tesis dimaksudkan sebagai tesis Ijazah Doktor Falsafah dan Sarjana secara penyelidikan atau disertassi bagi pengajian secara kerja kursus dan penyelidikan, atau laporan Projek Sarjana Muda (LPSM)

DECLARATION

The materials in this thesis are original except for quotations, excerpts, summaries and references, which have been duly acknowledged.

AJIRIN @ ADRIAN ANGKA]I PS98-001-053 18 JUNE 2007

ABSTRACT

A STUDY OF THE BIOLOGY AND ECOLOGY OF THE CHONDROSIA SP. COLONIZATION IN SEMPORNA ISLANDS, AND ITS IMPACT

ON THE REEF ECOSYSTEM

This study involved carrying out research into the biology and ecology of an invasive species

of sponge called the black sponge from 1999 to 2004. The aim was to investigate its impact

on the reef ecosystem and consider the implications of the infestation on reef management. The sponge was found to be locally common at depths between 2.0 - 20.0 m during

surveys carried out in the initial phase (Phase I) of the Sempoma Islands Project, in Sabah,

Malaysia. It occur as a thin film growing over rock, rubble and dead corals, leaving only

isolated patches and certain dead corals uncovered. It is particularly common at Bodgaya

West reef, Maiga South and Maiga West reefs. This phenomenon have not previously been

described for the area and it was for this reason that a study on its biology and ecology was

carried out. The research included identifying the black sponge, comparing results of Line

Intercept Transect (LIT) method surveys and studying the spread of the sponge over different substrata. It was found that the black sponge can move over the substratum at

rates of 1.8 - 1.9 mm2 per day. The fastest spread occurred where the sponge was growing

over the dead part of live hard coral or other non-living substratum. The fastest spread rates

recorded were over terracotta brick where the sponge grew at an average of 1.9 mm2 per day, and over dead coral where the sponge grew at 1.8 mm2 per day. However, the area,

which was initially dominated by the black sponge species, has been reduced year-by-year from 61% in 1999 to 3% in 2004. The black sponge was eventually identified and confirmed

as an undescribed species of Chondrosia by a sponge expert Dr. Michelle Kelly and Dame Professor Patricia R. Bergquist, Emeritas Professor, Department of Anatomy, School of Medical and Health Sciences, University of Auckland, New Zealand.

i

ABSTRAK

KIVIAN TERHADAP BIOLOGI DAN EKOLOGI CHONDROSIA SP. DI KEPULAUAN SEMPORNA DAN KESAN KEATAS EKOSISTEM TERUMBU

KARANG

Kajian ini bertujuan untuk mengkaji bio%gi dan eko%gi serb kesan jangka panjang

terhadap ekosistem terumbu karang berikutan pertumbuhan meluas saty spesies span baru

yang dikenali sebagai span hitam di pu/au pu/au Sempoma. Pertumbuhan meluas span hitam to/ah dikesan pada keda/aman 2.0 - 20.0 m keboka kerja-kerja penyel/dikan awal

terumbu karang Projek Pu/au-Pu/au Sempoma (fasa I) di Sempoma, Sabah bermu/a. Span

hitam yang menyerupai fl/em hitam nipis, tumbuh di alas serp/han terumbu karang mat);

wa/aupun bukan kese/uruhannya. Span h/tam in/ bo%h ditemu/ dengan banyak di bahag/an

Barat Pu/au Bodgaya, Se/atan dan Barat Pu/au Ma/ga. Kaj/an terperind terhadap

pertumbuhan span h/tam /n/ amat penting kerana tidak ada kaj/an mahupun laporan tentang

kewujudan fenomena sebe/um /n/. 0%h /tu kaj/an terperinä to/ah d#a/ankan secara lidak

langsung dad tahun 1999 h/ngga/ah 2004. In/ me//babFan kerja kerja pengena/pastian

spes/es span h/tam, perbandingan terhadap peratusan pertumbuhan span h/tam

menggunakan tekn/k Line Intercept Transect (LIT), kadar pertumbuhan span h/tam

menggunakan video digital serta mengukur kadar pertumbuhan dad masa ke semasa. Kawasan kajian IN merupakan antara kawasan yang teruk di tumbuhi o%h span h/tam.

Kadar pertumbuhan spes/es in/ juga menunjukkan bahawa spes/es /ni bo%h bergerak dan

tumbuh keatas sesuatu substrat mad pada kadar 1.8mm per. segi/har/ hingga 1.9mm1 /har/.

Kadar pertumbuhan tercepat direkodkan pada terumbu karang mad /aity pada kadar 1.8

mm? / had diikutr pada bata merah, 1.9 mmz / had. Walau bagaimana pun, kajian

berterusan dari tahun 1999 hingga 2004 menunjukkan penurunan peratusan span hitam di

kawasan kaj/an dad 61% kepada 3%. Sexara kese/uruhannya kaj/an terpen%ncr terhadap fenomena /n/ amat penting terutama sekali da/am pengurusan terhadap ekos/stem terumbu

karang da/am jangka masa panjang. Hasi/ dad kajian, span hitam tersebut akhimya dikena/paste sebagai sate spes/es baru da/am genus Chondrosia sp. o%h pakar Span Dr.

Michelle Kelly dan Professor Patricia R. Bergqu/sty Emerilas Professor, labatan Anatom/,

Seko/ah Sains Perubatan dan Kesihatan, Universiti AupF/and, New Zea/and.

ii

ACKNOWLEDGEMENTS

I wish to extend my sincere thanks my supervisors, Prof. Dr. Ridzwan Abd. Rahman and Prof. Dr. Salem Mustafa (Director of Borneo Marine Research Institute) for their help, guidance and continuous encouragement during the course of this study.

I am particularly grateful to my co-supervisors Dr. Elizabeth Wood & Dr. Frances Dipper (Marine Conservation Society) for their help, guidance, commented, edited the drafts of this report, and giving me a big opportunity to further my studies in University Malaysia Sabah during the Sempoma Islands Project 1998-2000.

I am also very grateful to Dr Michelle Kelly, NIWA, and Dame Professor Patricia R. Bergquist, Emeritas Professor, Department of Anatomy, School of Medical and Health Sciences, University of Auckland, New Zealand for helping me to identify sponge species.

I also would like to thank Dr. Majaji for her help in thesis correction, Dr. Charles Vairappan for his help in Scanning Electron Microscope (SEM), Mr. Julian Rangsangan for the histological studies in Universiti Malaysia Sabah, and Dr. David A Johnston, researcher in Parasite Genome Analysis, Biomedical Parasitology Division, Department of Zoology, Natural History Museum London. I also would like to thank the Sabah Parks Department and WWF Malaysia (Sabah) for giving me permission to conduct and to carry out continues this study. I am not forgetting to Sabah Parks Staff in Semporna, for their help during the course of this study.

This study would not have been completed without the support, patience and understanding of my wife Elve, my son Alvin and daughter Valenthyna and my parents. To them, I am very much indebted.

III

CONTENTS

Page ABSTRACT I ACKNOWLEDGEMENTS iii LIST OF FIGURES iv LIST OF TABLES xi

CHAPTER 1: INTRODUCTION

1.1 Background 1 1.2 Aims and Objectives 3

CHAPTER 2: LITERATURE REVIEW

2.1 General biology and morphology of sponges 5 2.2 Skeleton 6 2.3 Longevity, size and growth rate of sponges 8 2.4 General ecology and habitats of sponges 9 2.5 Reproduction 10

CHAPTER 3: METHODS

3.1 Study area 12 3.2 Distribution of the 'black sponge' and selection of study

sites. 12 3.3 Line Intercept Transect (LIT) Method 14 3.4 Identification of the black sponge 16

3.4.1 Collection and Preservation 3.4.2 Laboratory Examination

3.5 Spread rate observations 18 3.6 Spread and colonization rate observations of black 18

sponge over live hard coral 3.7 Spread and colonization of black sponge on the dead 21

part of live hard coral 3.8 Spread and colonization of black sponge on dean 23

terracotta brick 3.9 Scraped and re-scraped experiment 23 3.10 Estimation of the black sponge colonies spread rate 24 3.11 Extent of Infestation 25 3.12 Statistical analysis 25 3.13 Management strategies 25

CHAPTER 4: RESULTS AND DISCUSSION

4.1 Sponge Taxonomy 26 4.1.1 Systematics Summary 27 4.1.2 Guide to Identification (Boury-Esnault and Lopes 27

1985) 4.1.3 Description of genus Chondrosia (Adapted from 27

Boury-Esnault and Lopes, 1985)

iv

4.1.4 Description of the unidentified species of 30 Chondrosia sp.

4.1.4.1 Locality and habitat 30 4.1.4.2 Shape and size 30 4.1.4.3 Colour 30 4.1.4.4 Surface 31 4.1.4.5 Texture 31 4.1.4.6 Histology 31 4.1.4.7 Skeleton 33 4.1.4.8 Associations with other organism 34

4.2 Distribution and Abundance 38

4.2.1 The status of Chondrosia sp. in terms of 38 percentage cover in 1999

4.2.2 The status of Chondrosia sp. in terms of 42 percentage cover between 1999 to 2004 in Bodgaya West (black sponge site)

4.3 Spread Rates 45

4.3.1 Spread and colonization of Chondrosia sp. on live 45 hard corals

4.3.1.1 Diploastrea heliopora border 46 4.3.1.2 Favia rotumana and Favia sp. border 46 4.3.1.3 Porites sp. border 47

4.3.2 Spread and colonization of Chondrosia sp. on the 56 dead parts of live hard coral

4.3.3 Spread and colonization of Chondrosia sp. on 56 terracotta brick

4.3.4 Scraped and re-scraped experiments over 57 Chondrosia sp.

4.3.5 Average spread rates 57 4.3.6 Others 57 4.3.7 Discussion 70

4.4 Possible Cause(s) of Colonization and Regression 72

CHAPTER 5: CONCLUSION AND RECOMMENDATION

5.1 Management strategies 80 5.2 Conclusion 80

Appendix 1: Sites Surveyed Within the Tun Sakaran Marine 82 Park

Appendix II. - Statistical Analysis 84 References 86

V

LIST OF FIGURES

FIGURE CONTENTS PAGE

Figure 1.1 Sabah Map - Research Location 4

Figure 2.1 A, siliceous spicules (oxeas) glued together at their tips 7 with spongin to form a network in haliclona rosea. B. spongin fibers with embedded siliceous spicules (oxeas) form a reinforced network in endectyon. (Aaopw lrcvn. " "Porilera" and P/acozaä in hß. ///64.78.63.75/sa17ýp/es/09BIORu pertlnvertebrateZoo 7ch5pdf)

Figure 2.2 Porifera: body wall and skeleton of calcifying sclerosponge 7 (demospongiae: ceratoporellidae). The calcareous exoskeleton is secreted by the basal exopinacoderm and contains embedded siliceous spicules. siliceous spicules also occur in the mesohyl of the living tissue. (Adaptedlmm: "Parift'a° and Placozoa", in ht p. //64.78.63.75Lsa /es/O4BIORu eýtlnvertebrateZoo%y7ch5, pdt)

Figure 3.1 Sempoma Islands Reef (Recently gazetted Tun Sakaran 13 Marine Park in June 2004)

Figure 3.2 Line Intercept Transect (LIT) method 14

Figure 3.3 Border between black sponge and live hard coral 19 Diploastrea he/iopora (13 July, 1999)

Figure 3.4 Border between black sponge and Facia rotumana. A piece 19 of string (marked with white dot-line) was used as a mark around between the two colonies (21 July, 1999)

Figure 3.5 Border between black sponge and Pontes sp. (13 July, 20 1999)

Figure 3.6 Border between black sponge and Pontes sp. (13 July, 20 1999)

Figure 3.7 The spread of black sponge over dead parts of Diploashea 21 heiiopora (Observation I: 13 July, 1999)

Figure 3.8 The spread of black sponge over dead parts of Diploashea 22 heiiopora (Observation II: 13 July, 1999)

Figure 3.9 The spread of black sponge over dead parts of Dip/oastrea 22 heliopora (Observation III: 13 July, 1999)

Figure 3.10 The brick laid vertically on the top of the black sponge 23 colonies (22 February, 2000)

vi

Figure 3.11 A colony of Porites sp. with the area that had been 24 scraped clean shown by the dotted white line.

Figure 3.12 Estimation of the area covered by the black sponge colony 24 using grid system

Figure 4.1 Chondrosse. A, In situ photograph of a Mediterranean 28 specimen of Chondrosia reniformis (J. Vacelet slide collection) Scale bar: 0.5 cm. B, microphotograph of histological slide from the Lendenfeld collection in the BMNH 96.11.5.109 (abbreviations: CO cortex; CH choanosome; sp: foreign spicule; arrow: cribriporal chone) Scale bar: 400 pm. (Taken From ORDER CHONDROSIDA BOURY-ESNAULT & LOPES, 1985. FAMILY CHONDRILLIDAE GRAY, 1872 NICOLE BOURY-ESNAULT Universite de la Mediterrane, Centre d'Oceanologie de Marseille, Station marine d'Endoume, UMR CNRS 6540, rue de la Batterie des Lions, 13007-Marseille, France (esnault(-@com. univ-mrs. fr)

Figure 4.2 Fluorescent in situ hybridization with the universal Probe 29 EUB338 in thin sections of the sponge Chondrosia renifornmis Each bright signal can be assigned to a single bacterial cell (Taken from Osinga, et at. 2001)

Figure 4.3 SEM micrograph (PELDRI-dried) of the tissue of the 29 coralline demosponge daceletia crypta from reef caves of the Great Barrier Reef (Northern Australia). Within the mesohyl mobile sponge cells are visible (S). Bacteria (B) are abundant in the mesohyl, most of them are Vibri o- types. C= canal, CHC = choanocyte chamber, P= endopinacocyte (cell lining the internal surfaces). (Taken from Osinga, R. eta/. 2001)

Figure 4.4 Chondross sp. A: In situ photograph of a specimen of 32 Chondrosia sp. From underwater close-up photograph (by Frances dipper) Abbreviation: OSC, osculum and semi-thin section microphotograph of histological slide showing. B: CO cortex, CH choanosome (40 X) C: CC Choanocyte chamber, ca Canal (200 X).

Figure 4.5 A: Photomicrograph from SEM of spongin fibers by the 33 incorporation of foreign material (8.00 K X), B: A Close-up SEM photomicrograph (40.00 K X) of spongin fibers.

Figure 4.6 SEM micrograph of a diatoms magnification = 188 X; 35 20µm, slime growing under the surface of Chondrosia sp.. Predominant diatoms are species of Amphora.

Figure 4.7 A close-up SEM photomicrograph of diatoms Amphora sp. 36 magnification = 1.50 K X, 10um.

VII

Figure 4.8 A close-up SEM photomicrograph of diatoms Amphora sp. 36 magnification = 2.50 K X, Zum;

Figure 4.9 A close-up SEM photomicrograph of diatoms Amphora sp. 37 magnification = 4.00 K X, 2um.

Figure 4.10 A close-up SEM photomicrograph of diatoms Amphora sp. 37 magnification = 10.00 K X, Zum.

Figure 4.11 Other sites of the reefs investigated within the Tun 40 Sakaran Marine Park

Figure 4.12 Reef check summary of the 9 study sites at 3 metres 41

Figure 4.13 Reef check summary of the 9 study sites at 10 metres 41

Figure 4.14 Change in percentage cover of the black sponge 42 Chondrosia sp. at Bodgaya West site

Figure 4.15 Photographs showing the growing margins of Chondrosia 48 sp. and live Dip/oastrea he/iopora, and the minimal changes over a period of 361 days (Depth 4.3m)

Figure 4.16 Photographs showing the growth of Chondrosia sp. over 49 dead parts of the coral Favia rotumana (d), which had been probably killed by crown-of-thorns starfish Acanthaster p/ancii.

Figure 4.17 A) Crown-of-thorns (COT) Starfish Acanthaster p/anti 50 eating coral on the Bodgaya West reef ( April, 25 2000) (B) Coral killed by COT C) live coral, and D) the same coral after attack by COT (The death of the coral allowed the Chondrosia sp. to colonize).

Figure 4.18 Growth rate observation on Favia sp. Figure (D) shows 51 rapid growth of Chondrosia over the dead part of the coral, which had probably been killed by crown-of-thorns starfish Acanthaster p/ancii (BS: Black sponge)

Figure 4.19 Photographic record of the movement of Chondrosia on 52 Favia sp. The sponge had receded in Nov 1999 grown back slightly in Jan 2000 and then receded again in April 2000.

Figure 4.20 Photographs showing the growth of Chondrosia. over the 53 live part of Po, ites sp. followed by overgrowth by a fast growing encrusting sponge Acervaha/ina confosa (greeny black) (3.8m depth)

VIII

Figure 4.21 The percentage cover of Acervochalina confosa. over a 54 period of 286 days on Porites sp. fig A is an original photograph taken underwater, B is a sketch from photographsto show the growth of the Acervocha/ina confosa (see table 4.3 for the area cover in cm2/day).

Figure 4.22

Figure 4.23

Figure 4.24

Growth rate summary of Acervocha/ina confosa - another 55 species of encrusting sponge over the Chondrosia sp to date.

Photographs showing the spread of Chondrosia over dead 58 parts of Diploastrea Heliopora (Experiment A), (figure 4.24 and table 4.4)

Spread rate over 280 days mesured (using grid system) as 59 change in percentage cover of Chondrosia sp. on the dead part Dip/oastrea he/iopora (refer to table 4.4 and figure 4.25)

Figure 4.25 Growth rate summary of Chondrosia in cm2 within 223 60 days over the dead part of Diploastrea heliopora.

Figure 4.26 B&C- Photographs showing the growth of Chondrosia 61 sp. on dead parts of Diploastrea heliopora.

Figure 4.27 Photographs showing the spread of black sponge on a 62 clean terracotta brick. This experiment was started on February 22nd 2000 (A-I & All) and the vertical growth rate was taken. Figure B shows that the Chondrosia had grown 1.45cm upright after 22 days (B-I & B-II) and 2.10cm after 35 days (CI-CII). It had grown vertically to 3.6 cm after 63 days (D-1 & DII). (Please refer to table 4.5 & Figures 4.28 and 4.29)

Figure 4.28 Photograph shows that the brick was completely covered 63 after nine months

Figure 4.29 Change in percentage cover of the Chondrosia sp. over the 64 terracotta brick over 63 days (Please refer to table 4.5 & figure 4.30)

Figure 4.30 Spread rate summary of Chondrosia sp. on the brick 65 experiment over 63 days.

Figure 4.31 (A) The area within the white dotted line had previously 66 been scraped out with a knife. (B) The drawing shows the cover by Chondrosia sp. on the scraped area in experiments El and E2.

Ix

Figure 4.32 The average spread rate comparison of Chondrosia sp. 67

Figure 4.33 Photographs showing the growth of Chondrosia sp on the 69 Bodgaya West reef. It is growing over or around the following: (a) Dysidea sp., (b) Small Turbinaria sp. Plate and Sty/opohora mordax, (c) Favites sp. (d) live sea squirts, (e) Hard Coral, (f) Brain Coral.

Figure 4.34 A group of black damselfish seems to feed on the 77 Chondrosia sp. colony.

X

LIST OF TABLES

TABLE CONTENTS PAGE

Table 3.1 Sample from LIT data form 15

Table 3.2 Substratum categories and abbreviations 15

Table 3.3 Summary of histological procedure 17

Table 4.1 Measurements of percentage cover at 3m and 10m depth 39 by different benthic categories at 9 study sites within the Tun Sakaran Marine Park.

Table 4.2 (Two-Way ANOVA) - Temporal Change In the relative 44 abundace of each Benthic category within six years of Monitoring (1999-2004)

Table 4.3 Spread of encrusting sponges Acervocha/ina confosa over 55 Chondrosia within 245 days (please refer to figure 6.6 & 6.7)

Table 4.4 Spread rate (area covered in sq. cm) of Chondrosia sp. 60 over the dead part of Dipioastrea heiiopora to date using grid system.

Table 4.5 Spread rate of Chondrosia sp. over the brick to date in sq 65 cm over a period of 63 days.

Table 4.6 Growth rate of Chondmsia sp. over the scraped and re- 67 scraped area of a dead part of Paites sp., calculated using a grid system.

Table 4.7 Average spread rate comparison of Q)arad vs is sp. over; 68 A-dead part of Diplo a heligao, ra B-terracotta brick; C- Acermadiafiha ainf sa over the Chond a sp., D-Scraped and re-scraped area of dead part of Pofites sp.

XI

CHAPTER 1

INTRODUCTION

1.1 Background

Coral reefs are among the most biologically diverse marine ecosystems with high

biological diversity on earth (English et a/ 1997), rivalled only by the tropical

rainforests on land. Coral reefs deserve protection for their intrinsic natural value,

and for their importance to humans. People obtaining part of the protein in their diet

from coral reefs are estimated to number in tens of millions (Salvat, 1992). Coral

reefs not only contribute directly to human livelihoods but also indirectly, for example

as a main food supplier for both oceanic and inshore pelagic fishes (Birkeland, 1997),

which are utilized by fishers throughout the world.

Importantly, some of the economic, fishing and recreational resources of

tropical areas around the world depend upon healthy coral reef systems. However,

there is now widespread concern about threats facing reefs, which are affecting their

sustainability and biodiversity. These threats and documented impacts are due to a

variety of factors, which fall within two categories: natural disturbances and

anthropogenic (man-made) disturbances. Although natural disturbances may cause

severe changes in coral communities, anthropogenic disturbances have been linked

to major and widespread degradation of reefs and their resources. Hodgson (1999),

refers to "coral reef health" as a general concept to a balance in the ecosystem that

might be shifted by human activities.

1

The proposed Semporna Islands Park, covering an area of 350 sq. km, is

situated off the east coast of Sabah (figure 1.1). The natural resources of the

proposed park are of considerable biological, social, cultural and economic value, and

the reefs and islands have a natural beauty and interest that provide enormous

potential for eco-tourism. The coral reefs are of particular significance because of

their high biodiversity, unique species and value to local communities (Wood, 1998).

The Semporna Islands Project (SIP) began in 1998 under the leadership of

Dr. Elizabeth Wood, Coral Reef Conservation Officer of the Marine Conservation

Society, UK. It is a collaborative venture between the Marine Conservation Society

(MCS), Sabah Parks, WWF Malaysia and Nature Unk. The project was funded by the

European Community under its global environment budget line. The aim of the

project was to produce a plan for effective management and to ensure a healthy

future for the area by safeguarding livelihoods, promoting sustainable use of natural

resources and encouraging environmentally-sensitive development (Wood, 1998).

During the surveys carried out in the initial phase of the project, one of the

reef sites investigated (Bodgaya West) was found to be severely affected by a black

organism of uncertain identity that grew as a very thin film over rock, rubble and

corals, leaving only isolated patches and certain corals uncovered (Wood, pers.

Comm. ). It was confirmed to be black sponge following examination of specimens at

the Natural History Museum London, and by Dr. Michelle Kelly, a sponge expert from

the Marine Ecology and Aquaculture Group, National Institute of Water and

Atmospheric Research (NIWA), New Zealand.

This sponge infestation had not previously been reported for the area, or

from elsewhere in Sabah, but was dearly having a profound effect on the reef.

Research into the phenomena of ecological significance is vital, and it was for this

reason that a decision was made to carry out a full investigation of the biology and

2

ecology of the sponge. The study was also important because this area is a proposed

marine park, and particular management strategies may be required for the affected

reef.

1.2 Aims and Objectives

The overall aim of this project was to carry out research into the biology and ecology

of the black sponge, investigate its impact on the reef ecosystem and consider the

implications of the infestation on reef management. The specific objectives of this

research were to:

1. Describe the sponge and determine its identity.

2. Map the main area on Bodgaya West reef covered by the black sponge and

investigate its occurrence elsewhere in the proposed Park and on adjacent

reefs.

3. Determine how fast the sponge grows and spreads over the reef.

4. Determine the impact of the sponge infestation by investigating which reef

organisms are being smothered and which are apparently able to withstand

the spread of the sponge .

5. Consider whether particular management strategies may be required for the

affected reef.

3

I

NOW

ASn643

8b

N N

Ll W

. ! 4 '

fl

«

A. _ tv

i

H

= (0

fo L

ýl3 N

.... C

W mm ý

N

£ t

C

!

co

W

af

a

----- --- -- -- ý äcn 4

-- ------ -- lip

113

ä

t m W cc =

tm a

ý- ý

v z R ý ý

iý

4

CHAPTER 2

LITERATURE REVIEW

2.1 General Biology and Morphology of Sponges

Sponges are the most ancient, and primitive of all multicellular aquatic animals. They

are present at water depths from the tidal zones to the deepest regions (abyss)

(Sorokin, 1993; Hooper, 2000). As an element of the sessile benthos, sponges are

second most important after coral and zoantharians in terms of functions and roles

on the coral reef ecosystem (Sorokin, 1993). Moreover the role of sponges is similar

to some of the functions of coral on the coral reef ecosystem (Sorokin, 1993). For

instance, the calcareous sponges produce lime and take part in the reef-building

processes cementing carbonaceous material during the formation of reef-flat rocks.

Sponges are essentially divided into two main morphological categories

encrusting and free standing. Encrusting sponges are similar to moss because they

tend to cover the surface or grow attached to shells, stones, rocks or any solid object

on the bottom. Free standing sponges, the type most commonly known, grow into

odd shapes, may be quite large (up to two meters in diameter), and have a

significant amount of inner volume compared with their surface area (Hayden,

1999). The sponge phylum Porifera, is divided into three lasses: Calcispongiae,

Hyalospongiae and Demospongiae, based on the composition of the skeletal

elements (Hooper, 2000).

The colour of sponges variy according to the species, but also varies within

species. Sometimes the colour is influenced by the depth where it is growing. For

instance, deep-water sponges usually show a neutral drab or brownish colour, while

5

shallow-water sponges are generally brightly coloured, ranging from red, yellow, and

orange to violet and occasionally black (Hooper, 2000). Certain sponges (e. g. the

Verongida), contain what are known as aerophobic pigments that darken upon

contact with air (Hooper, 2000). Some species of sponges such as the Family

Spongilidae are often greenish because green algae live in symbiotic relationship

within them, and others are violet or pinkish, because they harbour symbiotic blue

green algae (Hooper, 2000).

2.2 Skeleton

Most sponges live in moving water and support themselves with a well-developed

skeleton. The skeleton of the sponges are formed by units called spicules which are

either scattered throughout the sponge or united to form fibres. Spicules are

classified as megascleres, which function in support, and microscleres which function

in protection and aid in support (Hooper, 2000). In most species of sponges, spongin

and spicules occur together. As shown in figure 2.1 A, spongin welds together the

bps of spicules to form a skeletal network. Figure 2.1 B, spicules are embedded into

spongin fibres themselves. Some species of sponges lack spicules, but secrete

organic spongin. For example, in some species of demosponges (Sderesponges), the

siliceous spicules are secreted in the mesohyl (Figure 2.2).

6

A B

Figure 2.1: A. siliceous spicules (oxeas) glued together at their tips with spongin to form a network in Ha/idona rosea. B. spongin fibers with embedded siliceous spicules (oxeas) form a reinforced network in endectyon. (Adopted from: "Porifera° and Placozoa°' in http: //64.78.63.75/samples/O4BIORuppertln vertebrateZoology7ch5. pdt)

Figure 2.2: Porifera: Cross section body wall and skeleton of calcifying sclerosponge (Demospongiae: Ceratoporellidae). The calcareous exoskeleton is secreted by the basal exopinacoderm and contains embedded siliceous spicules. siliceous spicules also occur in the mesohyl of the living tissue. (Adapted from: "Porifera° and Placozoa' in http: //64.78.63.75/samples/O481ORuppertrnveiiebrateZoology7ch5. pdf)

7

2.3 Longevity, Size and Growth Rates of Sponges

Longevity is highly variable among sponges, but in general, and especially in the

tropics, they tend to live on average from 20 to 100 years (Toonen, 1996). However,

according to Hooper (2000) sponges appear as long lived animal, although growth

rates vary enormously between different groups but some sponges, like haplosderids

can grow several centimetres in weeks but may have short life span. The size of

sponges is very variable, ranging from a few centimeters in diameter to vase, tube

and barrel sponges that can grow one to two meters tall and broad rounded masses

may be one to two meters in diameter (Hooper, 2000).

Encrusting sponges, which cover a very large area, can also be considered

enormous individuals. Some sponges, like Terpios sp. from Guam, grow an average

of 2.3 cm per month (Toonen, 1996). However, the growth rate and size within a

species of sponge may be influenced by many factors, such as the individual's age,

environmental conditions - current, sedimentation, light availability, food supply, and

the genetic potential of the species (Hooper, 2000). A study on the transplantation

of marine sponges to different conditions of light and current on natural reefs by

Wilkinson & Vacelet (1979) showed that growth of species with obligate symbionts

(e. g., Verongia aerophoba) was enhanced by high light levels, whereas growth of

species without symbionts (e. g., Chondrosia reniformis) was inhibited by strong

lighting. Species such as Chondri//a nucula and Pebosia ficiformis, which contained

facultative symbionts, did not appear to be affected by the light regime (Wilkinson &

Vacelet, 1979).

8

2.4 General Ecology and Habitats of Sponges

In general, little is known about sponge ecology, compared with other animal groups

but most sponges are very sensitive to a wide range of ecological factors (Hooper,

2000). As immobile animals, sponges are vulnerable to being overgrown, and have

to compete for space to survive (Shimek, 1997). It has been shown that some of

them are able to move slowly (up to 4 mm per day) within aquaria but it is still

unknown whether this movement occurs in the wild and is important for sponge

ecology under natural conditions.

Sponges may compete with other reef organisms for space on the reef

including species with defense mechanisms such as sweeper tentacle formation or

morphological adaptations (Vicente, 1993). Studies have indicated that sponges are

the superior competitors in 80% of these encounters (Vicente, 1987). In addition,

Bryan (1973) has also documented the extensive takeover of a section of reef in

Guam by an encrusting species of the sponge Terpios hoshinata. Among coral-

overgrowing and coral-killing sponges, the most notorious to date is probably Terpios

hoshinata (Bryan 1973, Plucer-Rosario, 1987), or Terpios hoshinota respectively

(Antonius, 1993, Rüttler & Muzik, 1993). Terpios hoshinota has infested hundreds

of meters of coral reef in Micronesia (Bryan, 1973), and has also been reported from

Nothern Pacific, from Samoa (Plucer-Rosario, 1987), from southern Japan (Rüttler &

Muzik, 1993), as well as from Mauritius and Sinai (Antonius, 1993). However, it was

never observed in Atlantic waters (Antonius, 1996).

According to Hooper (2000) and Porter and Targett (1988), sponges may use

chemicals made from the most poisonous materials found in nature (Shimek, 1997)

to compete for space and protect themselves from predators. In addition, sponges

may release chemicals to poison corals and other animals that would tend to

overgrow them. Other sponges that try to grow into corals spaces do not succeed. In

9

spite of the abundance and competitive dominance of sponges, consistently high

coral cover on Caribbean reefs indicates that sponges are somehow prevented from

reaching their competitive potential (Shimek, 1997). Some predators have enzymes

that allow them to detoxify the sponge chemical. They may have an advantage over

other predators in the exploitation of that sponge, and this may put the sponge at a

disadvantage (Shimek, 1997).

Light is one of the most important factors in influencing the distribution of

sponges, as it is one of the limiting factors for their survival. Some species of, littoral-

dwelling sponges are not dependent on light and generally occur in caves, on

shadowed walls, or under small shelters such as those provided by crevices. Others,

mainly in the tropics, are covered by a meter or less of water and thus are almost

completely exposed to irradiation from the sun. Symbiotic relationships between

algae and sponges usually occur in these strongly illuminated zones, and the algae

may act as a protective device because they deposit pigments in the superficial cell

layers of the sponge. In some sponges (e. g., Petrosia ficiformis), colour is related to

the density of symbionts within the sponge tissue. In a cave, for example, the

sponge gradually change from intensely coloured specimens to light-coloured,

sometimes white, once in the depth of the cave where the number of algae

decreases (Sorokin, 1993).

2.4 Reproduction

Sponges reproduce both sexually and asexually. Most are hermaphrodites, meaning

that male and female germ cells are in one individual. During sexual reproduction,

sperm are spawned from one sponge and transported by water currents, to another

individual. They are captured by specialised cells called choanocytes, and fertilization

10

REFERENCES

Aerts, L. A. M. 2000. Dynamics behind standoff interactions in three reef sponge species and the coral Montastraea cavernosa. Pubblicazioni della Stazione Zoological di Napoli. Marine Ecology. 21: 191-204.

Alino P. M., Sammarco P. W. and Coil J. C. 1992. Competitive strategies in soft corals (Coelenterata, Octocorailia), 4: Evironmentally induced reversals in competitive superiority. Marine Ecology Progress Series 81: 129-145

AntDnius, A. and Ballesteros, E. 1998. Epizoism: A new threat to coral health in Caribbean reefs. Revista Biology Tropical. 5: 145-156.

Antonius, A. 1993. Coral reef health in Mauritius Abstract First European Meeting International Sodety for Reef Studies. Austria: University of Vienna.

AntDnius, A. 1996. Sinai coral reef health survey 11: Gulf of Aqaba, Straits ofTiran, and Ras Mohamed. Report to Ras Mohamed National Park Service, Sinai, Egypt 29 pp.

Aronson, R. B., Precht, W. F., Toscano, M. A. and Koltes, K. H. 2002. The 1998 bleaching event and its aftermath on a coral reef in Belize. Marine Biology. 141: 435-447.

Bavestrello, G., Arillo, A., Calcinai, B., Cattaneo-Vietti, R., Cerrano, C., Gaino, E., Penna, A. and Sara, M. 2000. Parasitic diatoms inside Antartic sponges. Biological Bulletin. 198: 29-33.

Beller, P. 2000. Sponges. San Diego Natural History Museum. Httn: //www. oceanoasis. org fi/ eldguide/s{onges. html

Birkeland, C. 1989. The influence of echinoderms on coral reef communities. in, Jangoux, M. and Lawrence, J. M. (eds. ). Echinoderm Studies 3 pp. 1-79. Rotterdam: Balkema Press.

Birkeland, C. 1997 (ed. ). Life and Death of Coral reefs. New York: Chapman and Hall.

Bond, C. 1992. Continuos cell movements rearrange anatomical structures in lack sponges. Journal of Experimental Zooogica/. 263: 284-302.

Boury-Esnault, N. and Lopes, M. T. 1985. Order Chondrosida Boury-Esnault and Lopes, 1985. Family Chondrillidae Gray, 1872. France: Universite de la Mediterranee.

Brosnan, M. D., 1996. Volcanic impacts on the Coral Reefs. HtW: //www. sei. org/imgMcts. htmi.

Bryan, P. G. 1973. Growth rate, toxicity, and distribution of the encrusting sponge Terpios sp. (Hadromerida: Suberitidae) in Guam, Mariana Islands. Micronesia. 9: 237-242.

86

Buss, L. W. and Jackson, J. B. C. 1979. Competitive networks: nontransitive competitive relationships in coral reef environments. Am Nature. 113: 223-234

Buss, L. W., 1986. Competition and community organization on hard surfaces in the sea. In Diamond, J. and Case, T. J. (eds. ). Community Ecology, pp. 517-536. New York: Harper & Row.

Callow, M. E and Callow, J. A 2002. Marine biofouling: a sticky problem. Biologist 49: 10-14.

Carpenter, R. C. 1986. Partitioning herbivory and its effects on coral reef algal communities. Ecological Monographs 56: 345-363.

Chapin, F. S., Zavaleta, E. S., Eviner, V. T., Naylor, R. L., Vitousek, P. M., and Reynolds, H. L. 2000. Consequences of changing biodiversity. Nature. 405: 234-242.

Charlton, R. G., and Richardson, L. L. 1995. Oxygen and sulfide dynamics in a horizontally migrating cyanobacterial mat: Black band disease of corals. FEMS Microbiology Ecology. 18: 155-162.

Chomesky E. A. 1989. Repeated reversal during spatioal competition between corals. Ecology. 70: 843-855

"Coral Reef Creatures - Sponges (Porifera)" in http: //www. szgdocent. org/ff/f- reeflx. htm. Printed 28th March 2001.

Conn, D. B., 1993. Atlas of Invertebrate Reproduction and Development pp. 252. New York: John Wiley and Sons.

Duffy, J. E. and Hay, M. E. 2001. The ecology and evolution of marine consumer-prey Interactions. In Bertness, M. D., Hay, M. E. and Gaines, S. D. (eds. ). Marine Community Ecology, pp. 131-157. Sunderland: Sinauer Associates.

Duffy, I. E., Richardson, J. P., and Canuel, E. A. 2003. Grazer Diversity Effects on Ecosystems functioning in Seagrass Beds. Ecology Letters. 6: 637-645.

English, S., Wilkinson, C., and Baker, V. 1997. Survey manual for tropical marine resources 2nd Edition. Townsville: Australian Institute of Marine Science.

Franks, K. T., Petrie, B., Choi, J. W., and Legget, W. C. 2005. Tropic cascades in a formerly cod-dominated ecosystem. Science 308: 1621-1623.

Gaino, E. & Rebora, M. 2003. Ability of mobile cells of the freshwater sponge Ephydatia fluviatilis (Porifera, Demospongiae) to digest diatoms. Italian Journal of Zoology. 70: 17 - 22.

Hartman, W. D. & Goreau, T. F. 1970. Coral Reef Ecology. Symposium Zoological. 25: 205-243

Hayden, A. 1999. Real Brief - All about sponges. The Island Newspaper, Ambergris Caye, Belize, 18 November 1999.

87

Hill, M. S. 1998. Spongivory on Carribean reefs releases corals from competition with sponges. Decologia. 117: 143-150

Hodgson, G. 1999. A Global Assessment of Human Effects on Coral Reefs. Marine Pollution Bulletin. 38(5) : 345-355.

Hodgson, G., Maun, L. and Shuman, C. 2003. Reef check survey manual for coral reefs of Indo-Pacific, Hawaii, Adantic, /Caribbean, Red Sea and Arabian Gulf Reef Check Institute of the Environment Los Angeles: University of California.

Hooper, J. N. A, 2000. 'Sponguide; Guide to Sponge Collection and Identification. Australia: Queensland Museum.

Hughes, T. 1994. Catastrophes, phase shifts and large-scale degradation of a Caribbean coral reef. Science. 265: 1547-1551.

Jackson, J. B. C., Kirby, M. X., Berger, W. H., Bjomdal, K. A., Botsford, L. W. and Bourque, B. J. 2001. Historical overfishing and the recent collapse of ecosytems.. Scrence. 293: 629-638.

Jones, C. G., Lawton, J. H. & Shachak, M. 1994. Organisms as ecosystem engineers. Mos. 69: 373-386.

Lewis, S. M. 1986. The role of herbivorous fishes in the organization of a Carribean reef community. Ecological Monographs 56: 183-200.

Liew, H. C. 1994. Kaedah Penye/idikan dan Statistik, Faku/ti Perikanan dan Sains Samudera. Kuala Lumpur: Universiti Pertanian Malaysia.

Mc Clanahan, T. R. 1995. A coral reef ecosystem fisheries model: Impacts of fishing intensity, and catch selection on reef structure of coral reef structure and proceses. Ecological Modelling. 80: 1-19.

Mc Clanahan, T. R., Kamukuru, A. T., Muthiga, N. A., Yebio, M. G. and Obura, D. 1996. Effect of sea urchin reductions on algae coral and fish populations. Conservation Biology. 10: 136-154.

McCook, L. J., Jompa, J. and Diaz-Pulido, G., 2001. Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs. 19: 400-417.

Miller, M. W. 1998. Coral/Seaweed competition and the control of reef community structure within and between latitudes. Oceanography and Marine Bio%ogy, An Annual Review. 36: 65-96.

Naiman, R. J. 1988. Animal influences on ecosystems dynamics, large animals are more than passive components of ecological systems. Bioscpence. 38: 750- 752.

Pandolfi, J. M. 2005. Are U. S. coral reefs on the slippery slope to slime?. Science 307: 1725-1726.

88

Pawlik, J. R. 1997. Fish predation on Caribbean reef sponges: An emerging perspective of chemical defenses. Proceeding 8th International Coral Reef Symposium. 2: 1255-1258

Pawlik 1. R. 1998. Coral reef sponges: Do predatory fishes affect their distributions? Limnology Oceanography. 43: 1396-1399.

ocean Animals - Sponges, 1995. The Evergreen Project, Inc. httT? "//www mobotOrrg/MBGnetisaittanimals/sRgnnges htm

Peters, C. E. 1997. Diseases of Coral Reef Organisms. In Birkeland, C. 1997 (ed. ). Life and death of corals Reefs New York: Chapman & Hall.

Pipper, M. 1981. Report on human settlements. WWF Survey Expedition to Sempoma 1980. Kota Kinabalu: Sabah Museum.

Plucer-Rosario, G. 1987. The effect of substratum on the growth of Terpios sp. an encrusting sponge which kills corals. Coral Reefs. 5: 197-200.

"Poriferap and Placozoar in hip: //64 78 63 75/samples/04BIORuDoertInvertebrateZooloay7ch5 pdf Printed 28th March 2002.

Porter, I. W. and Targett, N. M. 1988. Allelochemical interactions between sponges and corals. Biological Bulletin. 175: 230-239.

Roberts, C. M. 1995. Effects of fishing on the ecosystem structure of coral reefs. Conservation biology. 9: 988-995.

Romano, S. L. 1990. Long-terol effects of interspecific aggression on growth of the reef building corals Cyphastrea ocellina (Dana) and Pociilopora damicornis (Unnaeus). Journal of Experimental Marine Biology and Ecology. 140: 135- 146.

Rützler, K. & Muzik, K. 1993. Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs. In Uriz, M. J. and Rützler, K. (eds. ). Recent Advances in Ecology and Systematics of Sponges, pp. 395-403. Barcelona: Scientia Marina.

Salvat, B. 1992. Coral reefs challenging ecosystem for human societies. Global Environmental Change. 2: 12-18.

Sara, M. 2000. Sponge. 1999-2001 Britannica. com Inc. hIU2: //www. britannica. com/eb]Mnt? = 118994

Schmidt, A. 1984. Atlas Per Diatomaceen-Kunde Begründer Von Ado/f Schmidt Germany: Koeltz Scientific Books Koenigstein.

Shimek, R. L. 1997. its (in) the water ... Aquarium. Net: http: //www. reefs. org/library/aquarium_net/0997/0997_4. htmi.

89

Singapore Zoological Gardens Docents, 2000. htt2: //www. szgdocent. org/ff/f- reef4. htm

Sorokin, Y. I (ed). 1993. Coral Reef Ecology. Ecological Studies 102 Springer Verlag. , pp. 4-28. Berlin:

Suchanek, T. H., Carpenter, R. C., Witman, J. D. & Harvell, C. D. 1985. Sponges as important space competitors In deep Canbbean coral reef communities. In Reaka, M. L. (ed). The ecology of deep and shallow coral reefs, pp. 55-60. Washington: Symposia series for undersea research 1, National Oceanic and Atmospheric Administration.

Sutherland, J. P. & Karison, R. H. 1977. Development and stability of the fouling community at Beaufort, North Carolina. Ecological Monographs. 47: 425-446.

Toonen, R. J. 1996. A reefkeeper's guide to introductory invertebrate zoology. Part 1. Sponges, www. aquarium. net/1196/1196_7. html

United Nations Educational, Scientific and Cultural Organization (UNESCO), 1984. Comparing Coral Reef Survey Methods, Report of a Regional UNESCO/UNEP Workshop Phuket Marine Biological Centre Thailand, 13-17 December 1982.

Vacelet, J. and Perez, T. 1998. Two new genera and species of sponges (Porifera, Demospongiae) without skeleton from a Mediterranean cave. Zoosystema. 20(1): 5-22.

Vicente, V. P. 1987. The ecology of the encrusting demosponge Chondri/la nucu/a (Schmidt) in a coral reef community in Puerto Rico. Department of Marine Sciences Puerto Rico: University of Puerto Rico, Mayaguez.

Vicente, V. P. 1993. Structural changes and vulnerability of a coral reef (Cayo Enrique) in La Parguera, Puerto Rico. In Ginsburg, R. N.. Global aspects of coral reefs: Health, hazards and history. Rosentiel school of Marine and Atmospheric Science, pp. 420. Miami: University of Miami.

Wilkinson, C. R. and Vacelet, ]. 1979. Transplantation of marine sponges to different conditions of light and current. Journal of Experimental Marine Biology and Ecology. 37: 91-104.

Wilkinson, C. R. 1987. Inter ocean differences in size, and nutrition of coral reef sponge populations. Science 236: 1654-1657.

William, R. B. 1991. Acrorhagi, catch tentacles and sweeper tentacles: a synopsis of 'aggression' of actiniarian and sderactinian Cnidaria. In: Williams, R. B., Cornelius, P. F. S., Hughes, R. G., Robson, E. A. (eds. ). Coelenerate Biology. - Recent Research on Cnidara and Ctenophore, pp. 539-545. Belgium: Kluwer Academic Publishers.

Wood, E. 1977. Coral reefs in Sabah: present damage and potential dangers. Journal of Malaya Nature 31: 49-57.

90

Wood, E. 1998. Semporna Islands Project Proposal. A proposal submitted to Sabah Parks. Kota Kinabalu: Sabah Parks.

Wood, E., Dipper. F, Wood, C., Angkaji, A., Daly, S., and Lane, D. 1998. Reef Survey and Assesment Marine Conservation Society and Sabah Parks. Kota Kinabalu: Sabah Parks.

Wood, E. 2000. Managing the Proposed Sempoma Islands Park - Options for discussion. Kota Kinabalu: Sabah Parks.

Wood, E. 2001. Management Plan fo the Semporna Islands Park. Kota Kinabalu: Sabah Parks.

Wood, E., Dipper, F., Wood, C., Angkaji, A., Davis, C., Haynes, R., McKeown, and T. 2002. Coral Reef Monitoring in the Proposed Sempoma Islands Park. Kota Kinabalu: Sabah Parks.

Wood, E., Dipper, F. and Angkaji, A. 2004. Patterns of change in reef communities revealed by the monitoring programme for the Semporna Is/and reefs, Sabah, Malaysia. Kota Kinabalu: Sabah Parks.

91