DISTRIBUTION AND ABUNDANCE OF BENTHIC

FORAMINIFERA IN THE COASTAL WATERS AROUND

PENANG NATIONAL PARK

By

FATIN IZZATI MINHAT

Thesis submitted in fulfillment of the requirements for the degree of

Master of Science

MAY 2013
 ACKNOWLEDGEMENT

In the name of Allah, the beneficent the merciful

Firstly, I would like to extend my heartfelt gratitude to my supervisor, Dr.

Khairun Yahya for her continuous guidance, patience and encouragement throughout

my graduate career. I am deeply indebted to Mr. Omar Ahmad, Dr. Anita and

Professor Norenburg for their knowledge, advice and comments. I would also like to

acknowledge Mr. Abdul Latif Omar and Mr. Rajindran A/L Suppiah and other

CEMACS’s lab assistance, for helping me out during field sampling. Without them

this research would not have been possible. Special thanks and appreciation goes to

my laboratory members, Ms. Alianie Mustaffa and Ms. Nurul Ruhayu for their

encouragement, assistance and guidance in field as well as laboratory work.

The funding of this study was provided by the Research University Grant

(1001/PPANTAI/815052) of Universiti Sains Malaysia. My greatest appreciation is

to Universiti Sains Malaysia (USM) and Centre for Marine and Coastal Studies

(CEMACS) for the facilities and support in this study.

I dedicate this thesis to my beloved family who has been a source of

encouragement and motivation to me throughout my life.

ii
 TABLE OF CONTENTS

ACKNOWLEDGEMENT ii

TABLE OF CONTENTS iii

LIST OF TABLES vii

LIST OF FIGURES viii

LIST OF APPENDICE xii

LIST OF PUBLICATION & SEMINARS xiii

ABSTRAK xiv

ABSTRACT xvii

CHAPTER 1- INTRODUCTION 1

CHAPTER 2 – LITERATURE REVIEW 7

2.1 Systematic of Foraminifera 7

2.2 Morphology and anatomy of benthic Foraminifera 9

2.2.1 General morphology for classification 9

2.2.2 Test wall composition 14

2.2.3 Chamber arrangement 15

2.3 Habitat and ecology of benthic Foraminifera 16

2.3.1 Distribution and diversity 16

2.3.2 Nutrition 18

2.3.3 Reproduction 19

2.4 Significant of benthic Foraminifera 19

2.5 Past studies on Foraminifera 24

2.5.1 Biological indicator of the environment 26

2.5.2 Foraminifera study in Asia 27

CHAPTER 3 – MATERIAL AND METHODS 29

iii
3.1 Sampling location 29

3.1.1 Teluk Bahang 32

3.1.2 Teluk Aling 33

3.1.3 Teluk Ketapang 34

3.1.4 Pantai Acheh 35

3.2 Field sampling 36

3.2.1 Samples collections 36

3.2.2 Environmental parameters data collections 37

3.3 Laboratory analysis 38

3.3.1 Foraminiferal samples sorting and quantification 38

3.3.2 Species identification 39

3.3.3 Scanning Electron Microscope methods 40

3.3.4 Nutrient determination 41

3.3.4.1 Nitrite 41

3.3.4.2 Nitrate 42

3.3.4.3 Ammonia 43

3.3.4.4 Ortho phosphate 43

3.3.5 Total suspended solids (TSS) analysis 44

3.4 Sediment quality analysis 45

3.4.1 Particle size analysis 45

3.4.2 Organic matter 47

3.5 Community Structure Analysis 48

3.5.1 Shannon- Wiener Diversity Index 48

3.5.2 Evenness index (J’) 49

3.5.3 Dominance index 49

iv
3.6 Statistical analysis 50

3.6.1 Pearson’s correlation test 50

3.6.2 Two-way analysis of variance (ANOVA) 50

3.6.3 Cluster analysis 50

3.6.4 Ammonia-Elphidium Index (AEI) & FORAM

51
(Foraminifera in Reef Assessment and Monitoring) Index

CHAPTER 4 - RESULTS

4.1 Benthic Foraminifera distribution, composition and abundance 53

4.1.1 Teluk Bahang 60

4.1.2 Teluk Aling 66

4.1.3 Teluk Ketapang 73

4.1.4 Pantai Acheh 80

4.2 Comparison on species distribution and composition 86

4.3 Nutrients determination 94

4.3.1 Nitrite 95

4.3.2 Nitrate 95

4.3.3 Ammonia 96

4.3.4 Ortho-phosphate 96

4.4 Physical and chemical parameters of bottom water layer 99

4.4.1Temperature 100

4.4.2 Salinity 100

4.4.3 Dissolved oxygen 101

4.4.4 Water pH 102

4.4.5 Total suspended solid 102

4.5 Sediment quality analysis 104

v
 4.5.1 Organic matter 105

4.5.2 Sediment particle size 108

4.6 Pearson’s correlation 110

4.7 Cluster analysis 113

CHAPTER 5 – DISCUSSION 115

5.1 Foraminifera composition and abundance in shallow coastal water

115
of north-west Penang Island.
5.2 Cluster analysis: Relationship between physicochemical parameters
123
and foraminiferal distribution
5.3 Ammonia-Elphidium index (AEI) as hypoxic indicator 127

5.4 FORAM index in monitoring water and sediment quality 128

CHAPTER 6 - CONCLUSION 132

REFERENCES 134

APPENDICES 143

vi
 LIST OF TABLES
Table Title Page
Table 2.1 FORAM index functional groups, genera and their
distribution. (Modified from Hallock et al, 2003 and 22
Carnahan, 2009).
Table 3.1 The GPS coordinates for all 24 sampling points around the
31
coastal waters of Penang National Park.
Table 3.2 Classification of particle size according to Wentworth, 1922. 46
Table 4.1 List of Foraminifera assemblages found at Teluk Bahang,
53
Teluk Aling, Teluk Ketapang and Pantai Acheh.
Table 4.2 Benthic Foraminifera functional groups and identified genera
at Teluk Bahang, Teluk Aling, Teluk Ketapang and Pantai 54
Acheh.
Table 4.3 Table 4.3 Abundance of Foraminifera genus (mean ± S.E)
and functional groups at Teluk Bahang. (FORAM index
61
functional groups, ST = stress-tolerant taxa, AG =
agglutinated taxa, OSM = other heterotrophic groups).
Table 4.4 Abundance of Foraminifera genus (mean ± S.E) and
functional groups at Teluk Aling. (FORAM index functional
67
groups, ST = stress-tolerant taxa, AG = agglutinated taxa,
OSM = other smaller miliolids).
Table 4.5 Abundance of Foraminifera genus (mean ± S.E) and
functional groups at Teluk Ketapang. (FORAM index
74
functional groups, ST = stress-tolerant taxa, AG =
agglutinated taxa, OSM = other smaller miliolids).
Table 4.6 Abundance of Foraminifera genus (mean ± S.E) and
functional groups at Pantai Acheh. (FORAM index
81
functional groups, ST = stress-tolerant taxa, AG =
agglutinated taxa, OSM = other smaller miliolids).
Table 4.7 List of Foraminifera and their frequency of occurrences at
each sampling station. S1- 200m, S2- 400m, S3-600m, S4-
88
800m, S5- 1000m & S6- 1200m. The presence of each genus
is represented by + symbol while absence – symbol.

vii
Table 4.8 Mean species density with standard error (S.E) for Teluk
89
Bahang, TelukAling, Teluk Ketapang and Pantai Acheh.
Table 4.9 Two-way analysis of variance (p <0.05) on all Foraminifera
90
genera collected throughout the sampling period.
Table 4.10 Two-way analysis of variance (p <0.05) on all Foraminifera
91
genera collected throughout the sampling period. Cont.
Table 4.11 Analysis of variance using two-way ANOVA for nutrients
content around the coastal waters of Penang National Park 94
between October 2010 and September 2011.
Table 4.12 Two-way ANOVA on in situ parameters measured around
the coastal waters of Penang National Park between October 99
2010 and September 2011.
Table 4.13 Two-way ANOVA on Total Suspended Solids (TSS)
collected at all sampling stations between October 2010 and 102
September 2011.
Table 4.14 Two-way ANOVA on sediment quality at all sampling
104
stations between October 2010 and September 2011.
Table 4.15 Pearson's correlation coefficients of physical, chemical
parameters to Foraminifera genera, FORAM index and
111
Ammonia-Elphidium index (AEI) (N = 144, * significant at
0.05, ** significant at 0.01)
Table 4.16 Pearson's correlation coefficients of organic matter and
particle size to Foraminifera genera, FORAM index and
112
Ammonia Elphidium index (AEI) (N = 144, * significant at
0.05, ** significant at 0.01).
Table 5.1 One-way ANOVA for Foraminifera density, water quality,
environmental parameters and sediment quality between 126
clusters.

viii
 LIST OF FIGURES
Figure Title Page
Figure 2.1 Types of wall composition and structure used in taxonomic 8
work. (Scott et. al, 2001)
Figure 2.2 General Foraminifera test morphology (Murray, 1979) 10
Figure 2.3 Reticulate pseudopodia used for feeding, mating and locomotion 10
(Goldstein, 2003).
Figure 2.4 Diagram on general morphology of Foraminifera according to 11
Cushman (1928) & Sen Gupta (2003).
Figure 2.5 Chamber arrangement use in identification (Sen Gupta, 2003; 12
Leoblich & Tappan, 1988)
Figure 2.6 Types of aperture in Foraminifera that are used in identification 13
(Sen Gupta, 2003; Leoblich & Tappan 1988)
Figure 2.7 Examples of test deformation and abnormalities in Foraminifera. 21
Figure 3.1 Map of sampling location: A- location of Penang Island along 30
the Malacca Strait; B- North-west part of Penang Island; C-
sampling stations along each transect in coastal waters.
Figure 3.3 Floating-cage culture activities near the coastal water of Teluk 32
Bahang.
Figure 3.4 Facilities built for Centre for Marine and Coastal Studies 33
(CEMACS) in Teluk Aling.
Figure 3.5 Teluk Ketapang sampling site. 34
Figure 3.6 Pantai Acheh sampling site. 35
Figure 4.1 Scanning Electron Micrographs (SEM) of order Rotaliida 55
collected during this study. A- umbilical view of Ammonia
parkinsoniana (d’Ornigny, 1839) B- spiral side of Ammonia
tepida C- umbilical view of Ammonia tepida (Cushman, 1926).
D – Elphidium advenum, E – Nonionoides sp.1, F –Elphidium
hughesi.
Figure 4.2 SEM of order Bulimida found in this study. 56
A – Bolivina sp.1, B – Bolivina durrandii (Millett, 1900), C –
Bolivina striatula (Cushman, 1928). D – Lagena sp.1, E –
Ammobaculites sp. 1, F –. Ammobaculites sp. 2.

ix
Figure 4.3 SEM on some benthic Foraminifera collected during the study. 57
A – Quinquelocolina sp.1, B – side view of Eggerella sp.1, C –
dorsal view of Eggerella sp.1, D – Textularia sp.1.
Figure 4.4 Relative abundances of benthic Foraminifera collected form 59
Teluk Bahang, Teluk Aling, Teluk Ketapang and Pantai Acheh
between October 2010 and September 2011.
Figure 4.5 The average density (A) and relative abundance (B) of benthic 63
Foraminifera collected bimonthly from October 2010 to
September 2011along the transects in Teluk Bahang.
Figure 4.6 The temporal distribution of Foraminifera along the transect at 64
Teluk Bahang.
Figure 4.7 Diversity indices, FORAM index and Ammonia-Elphidium index 65
observed according to distances at Teluk Bahang sampling site.
Figure 4.8 The average density (A) and relative abundance (B) of benthic 70
Foraminifera collected bimonthly from October 2010 to
September 2011along the transects in Teluk Aling.
Figure 4.9 The temporal distribution of Foraminifera along the transect at 71
Teluk Aling.
Figure 4.10 Diversity indices, FORAM index and Ammonia-Elphidium index 72
observed according to distances at Teluk Aling sampling site.
Figure 4.11 The average density (A) and relative abundance (B) of benthic 76
Foraminifera collected bimonthly from October 2010 to
September 2011along the transects in Teluk Ketapang.
Figure 4.12 The temporal distribution of Foraminifera along the transect at 77
Teluk Ketapang.
Figure 4.13 Diversity indices, FORAM index and Ammonia-Elphidium index 79
observed according to distances at Teluk Ketapang sampling
site.
Figure 4.14 The average density (A) and relative abundance (B) of benthic 83
Foraminifera collected bimonthly from October 2010 to
September 2011along the transects in Pantai Acheh.

x
Figure 4.15 The temporal distribution of Foramnifera along the transect at 84
Pantai Acheh
Figure 4.16 Diversity indices, FORAM index and Ammonia-Elphidium index 85
observed according to distances at Pantai Acheh sampling site.
Figure 4.17 Diversity indices, FORAM index and Ammonia-Elphidium index 93
obtained from samples collected at all sites between October
2010 and September 2011.
Figure 4.18 The spatial distribution on mean concentrations of nitrite (NO2), 97
nitrate (NO3), ammonia (NH4) and ortho- phosphate (PO4)
collected throughout the study period (October 2010 –
September 2011).
Figure 4.19 Monthly distribution of mean concentration of nitrite (NO2), 97
nitrate (NO3), ammonia (NH4) and ortho-phosphate (PO4)
collected from Teluk Bahang, Teluk Aling, Teluk Ketapang and
Pantai Acheh.
Figure 4.20 Mean temperature and salinity recorded between sampling 101
periods throughout the study.
Figure 4.21 Mean dissolved oxygen concentrations and pH measured 103
between sampling periods throughout the study
Figure 4.22 Mean concentrations of total suspended solid observed between 103
sampling months.
Figure 4.23 The spatial distribution of organic matter concentration collected 105
in this study between October 2010 and September 211.
Figure 4.24 The mean concentrations of organic matter collected at each 106
sampling station between October 2010 and September 2011.
Figure 4.25 The mean concentration of organic matter at each sampling site 107
according to temporal distribution.
Figure 4.26 Average sediment particle size and characteristic of sediments 109
collected at Teluk Bahang, Teluk Aling, Teluk Ketapang and
Pantai Acheh throughout the study period. (Sample size, n=144).

xi
Figure 4.27 Dendrogram obtained by cluster analysis using Ward’s method 114
and Euclidean distance for all 24 stations.
(TB= Teluk Bahang; TA= Teluk Aling; TK= Teluk Ketapang;
PA=Pantai Acheh; 200, 600, 800, 1000 & 1200 = distances (m))

Figure 5.1 The differences in pore size on test wall with relation to the 120
availability of oxygen observed in Ammonia collected from
Teluk Bahang (A) and Pantai Acheh (B).
Figure 5.2 The comparison between Ammonia test collected from; A- Teluk 124
Bahang and B- Pantai Acheh. Bigger test was observed in Teluk
Bahang (width= 320 µm) compared to Pantai Acheh (width=
230 µm).

xii
 LIST OF APPENDICE

Appendix Title Page

Appendix 1 Example of transect layout in Teluk Bahang, Teluk Aling, Teluk 143
Ketapang and Pantai Acheh. (The distance in this figure is not
the accurate distance).

Appendix 2 GPS points for each station at every sampling sites and depth 145
range in (m).

Appendix 3 Two-way ANOVA for Foraminifera density, water quality, 146

environmental parameters and sediment quality at Penang
National Park coastal waters.

Appendix 4 Homogenous subsets for water quality and environmental 150

parameters between months based on Tukey HSD Test.

Appendix 5 Homogenous subsets for Foraminifera density, water quality, 153

sediment quality and environmental parameters between
sampling sites based on Tukey HSD Test.

Appendix 6 Homogenous subsets between distance from shore (stations) for 156
Foraminifera density and sediment quality based on Tukey HSD
Test. * 1= 200m, 2=400m, 3=600m, 4=800m, 5= 1000m &
6=1200m.

Appendix 7 One-way ANOVA for Foraminifera density, water quality, 160

environmental parameters and sediment quality between
clusters.

Appendix 12 Tukey’s HSD Test used to determine the homogenous subsets 163
between clusters.

xiii
 LIST OF PUBLICATIONS & SEMINARS

Appendix Title Page

Appendix 9 Fatin Izzati, M., Anita, T. Omar, A. & Khairun, Y. (2012). 170
Benthic Foraminifera species distribution in the subtidal of
Penang National Park. In: Taxonomy and Ecology: Beyond
Classical Approaches. Proceedings of Taxonomist and Ecologist
Conference 2011, 19-20 April 2011. Faculty of Resource and
Technology, Universiti Malaysia Sarawak, Sarawak, Malaysia.

Appendix 10 Fatin Izzati, M., Khairun, Y., Anita, T. & Omar, A. (2011). A 171
survey of benthic foraminiferal assemblages in relation to water
quality in Penang coastal waters. In: Cemacs Posgraduate
Colloquim 2011, 9 November 2011. Centre for Marine and
Coastal Studies, Universiti Sains Malaysia, Pulau Pinang,
Malaysia.

Appendix 15 Fatin Izzati, M., Khairun, Y., Anita, T. & Omar, A. (2012). 172
Benthic foraminiferal assemblage as potential ecological proxies
for environmental monitoring in coastal water. In: 2nd
International Conference on Environment and BioScience,
IPCBEE. IACST Press, Singapore. 40: 60-64.

xiv
 TABURAN DAN KEPADATAN FORAMINIFERA BENTIK DI PESISIRAN

PANTAI SEKITAR TAMAN NEGARA PULAU PINANG

ABSTRAK

Satu kajian mengenai taburan dan kelimpahan Foraminifera bentik telah

dijalankan di sekitar perairan Taman Negara Pulau Pinang, Malaysia. Empat lokasi

(Teluk Bahang, Teluk Aling, Teluk Ketapang dan Pantai Acheh) telah dipilih

berdasarkan tahap aktiviti antropogenik. Sebanyak 192 sampel tanah telah dikutip

dua bulan sekali antara bulan Oktober 2010 dan September 2011. Semua sampel

tanah, sampel air dan parameter persekitaran telah diambil di sepanjang transet

dengan selaan 200 m, bermula dari zon sub pasang surut sehingga jarak 1200 m dari

pantai. Himpunan Foraminifera merangkumi 14 genera iaitu Ammonia, Elphidium,

Ammobaculites, Nonionoides, Bolivina, Asterorotalia, Reophax, Eggerella,

Textularia, Quinqueloculina, Astacolus, Lagena, Fissurina dan Hopkinsina yang

telah dikenalpasti. Kumpulan yang mempunyai toleransi terhadap tekanan iaitu

Ammonia (56.35%) dan Elphidium (9.11%) mendominasi himpunan Foraminifera

bentik di setiap lokasi. Sementara itu, kumpulan lain (seperti miliolids kecil dan

agglutinat) yang hadir <5% dianggap sebagai spesies nadir. Indeks diversiti

menunjukkan bahawa Pantai Acheh mempunyai himpunan Foramininifera dengan

kepelbagaian spesies tertinggi (H’ = 0.57) diikuti oleh Teluk Ketapang (H’ = 0.47),

Teluk Bahang (H’ = 0.43) dan Teluk Aling (H’ = 0.35). Himpunan spesies juga

menunjukkan bahawa kesan antropogenik terhadap Foraminifera berkurang apabila

lebih jauh dari kawasan pantai. Aplikasi indeks FORAM (FI = 1.0 ~ 2.0) dan indeks

xv
Ammonia-Elphidium (AEI = 85 ~ 100) mencadangkan bahawa keadaan tertekan di

sepanjang lokasi penyempelan. Tambahan pula, kesan antropogenik yang lebih hebat

boleh diperhatikan berhampiran dengan kawasan pantai terutamanya di Teluk

Bahang dan Teluk Aling. Pencemaran bahan organik daripada aktiviti akuakultur di

Teluk Bahang menyebabkan saiz test Ammonia secara signifikannya lebih besar.

Analisis kluster mengelaskan semua stesen kepada empat kumpulan, setiap satunya

dipengaruhi oleh tahap tekanan antropogenik yang berbeza. Kumpulan A (pada jarak

200m di Teluk Bahang dan Teluk Aling) secara signifikannya menunjukan kuantiti

bahan organik yang tinggi (17.14%, p< 0.05, ANOVA satu hala), keadaan hipoksik

yang kuat (AEI=98, p< 0.05, ANOVA satu hala) dan jumlah pH yang rendah (8.37,

p< 0.05, ANOVA satu hala). Kumpulan ini mempunyai kelimpahan Foraminifera

yang empat puluh kali ganda lebih tinggi tetapi mempunyai diversiti yang lebih

rendah. Kumpulan B merangkumi stesen yang terletak lebih jauh daripada kawasan

pantai dan menunjukkan kandungan bahan organik yang rendah secara signifikan

(9.67%, p< 0.05, ANOVA satu hala). Kumpulan C mewakili kawasan pinggiran

yang bercirikan substrat berlumpur dengan jumlah pepejal terampai yang tinggi

secara signifikan (166.03 mg/L, p< 0.05, ANOVA satu hala). Kumpulan D

menunjukkan ciri-ciri kepadatan yang rendah dan kepelbagaian spesies yang rendah.

Secara keseluruhan, taburan ruangan parameter in situ (suhu = 29.97 ± 0.05 °C,

kemasinan = 29.52 ± 0.08 ‰, oksigen terlarut = 5.21 ± 0.08 mg/L dan pH = 8.43 ±

0.01) dan nutrien terpilih (NO2, NO3, NH4 and PO4) tidak menunjukan perbezaan

yang signifikan (ANOVA dua hala, p< 0.05). Sementara itu, kualiti enapan dan

bahan organik mempunyai perbezaan yang signifikan di antara stesen dan transek

(ANOVA dua hala, p< 0.05). Ujian kolerasi Pearson menunjukkan terdapat korelasi

kuat antara kepadatan Foraminifera dengan kualiti enapan (pasir kasar, r=0.48; pasir

xvi
sederhana, r=0.57; pasir halus, r=0.55; pasir sangat halus, r=0.66; kelodak dan tanah

liat, r=-0.58, p< 0.01). Taburan ruangan Foraminifera dengan jelas dipengaruhi oleh

persekitaran enapan dan bahan organik. Oleh itu, walaupun kualiti air tidak

menunjukan tanda-tanda pencemaran, kajian teliti Foraminifera membuktikan

sebaliknya. Secara keseluruhan, kajian ini menyimpulkan bahawa himpunan

Foraminifera berubah sebagai tindak balas terhadap kehadiran stresor antropogenik

yang tenggelam dan terkumpul di dasar laut. Oleh yang demikian, Foraminifera telah

terbukti sebagai penunjuk biologi yang sangat baik dan murah di sekitar perairan

Malaysia.

xvii
 DISTRIBUTION AND ABUNDANCE OF BENTHIC FORAMINIFERA IN

THE COASTAL WATERS AROUND PENANG NATIONAL PARK

ABSTRACT

A study on the distribution and abundance of benthic Foraminifera was

conducted along the coastal waters of Penang National Park, Malaysia. Four selected

sites (i.e Teluk Bahang, Teluk Aling, Teluk Ketapang and Pantai Acheh) were

chosen based on the degree of anthropogenic activities. A total of 192 sediment

samples were collected bimonthly between October 2010 and September 2011. Bulk

sediments samples, water samples and environmental parameters were collected

along the transect at 200 m intervals from the subtidal zone and extending up to 1200

m offshore. Foraminiferal assemblages comprised of 14 genera which include

Ammonia, Elphidium, Ammobaculites, Nonionoides, Bolivina, Asterorotalia,

Reophax, Eggerella, Textularia, Quinqueloculina, Astacolus, Lagena, Fissurina and

Hopkinsina were identified. The stress-tolerant taxa, Ammonia (56.35 %) and

Elphidium (9.11 %) dominated the assemblage at all sites. Meanwhile, the other

functional groups (i.e. other smaller miliolids and agglutinated) which occurred <5%

were considered as rare or accidental species. Diversity indices showed that Pantai

Acheh has a diverse assemblage (H’ = 0.57) followed by Teluk Ketapang (H’ =

0.47), Teluk Bahang (H’ = 0.43) and Teluk Aling (H’= 0.35). Species assemblage

indicated the anthropogenic effect on Foraminifera reduced with increase distance

from the shore. Application of FORAM index (FI = 1.0 ~ 2.0) and Ammonia-

xviii
Elphidium index (AEI = 85 ~ 100) suggested a stressed condition along the study

sites. In addition, a greater effect from anthropogenic stressor was observed at area

closer to the shore especially in Teluk Bahang and Teluk Aling. Organic matter

pollution from aquaculture activity in Teluk Bahang resulted in significantly larger

test size of Ammonia. Cluster analysis classified the stations into four groups, each

influenced by different degree of anthropogenic stressors. Group A (i.e 200 m at

Teluk Bahang and Teluk Aling) was characterized by significantly high organic

matter (17.14%, one-way ANOVA, p< 0.05), strong hypoxic condition (AEI= 98,

one-way ANOVA, p< 0.05) and low pH value (8.37, one-way ANOVA, p< 0.05).

This group has forty times higher foraminiferal abundance but relatively low in

diversity. Group B consisted of stations situated further away from the shore and

showed significantly low organic matter content (9.67%, one-way ANOVA, p<

0.05). Group C represented the marginal environmental condition with muddy

substrate and significantly high total suspended solids (166.03 mg/L, one-way

ANOVA, p< 0.05). Group D is characterized by low mean abundance and low

diversity. Overall, the spatial distribution of in situ parameters (temperature = 29.97

± 0.05 °C, salinity = 29.52 ± 0.08 ‰, dissolved oxygen = 5.21 ± 0.08 mg/L and pH =

8.43 ± 0.01) and selected nutrients (NO2, NO3, NH4 and PO4) showed no significant

difference (two-way ANOVA, p< 0.05). Meanwhile, the sediment quality and

organic matter were significantly different between stations and transects (two-way

ANOVA, p< 0.05). The Pearson’s correlation test indicated a strong correlation

between foraminiferal density and sediment quality (coarse sand, r=0.48; medium

sand, r=0.57; fine sand, r=0.55; very fine sand, r=0.66; silt and clay, r=-0.58, p<

0.01). The spatial distribution of Foraminifera was clearly associated with benthic

sedimentary environment and organic matter. Therefore, although water quality

xix
indicated no sign of pollution, details study on Foraminifera revealed otherwise.

Overall, this study concludes that foraminiferal assemblages changed in response to

the presence of anthropogenic stressor that sink and accumulated on the sea bottom.

Hence, Foraminifera was proven to be an excellent and cheap bio-indicator in

Malaysian coastal waters.

xx
1.0 INTRODUCTION

The coastal zones which include mangrove forest, estuaries, lagoons and coastal

plains are areas where terrestrial and marine ecosystems interact. These areas face

various stressor either natural (e.g temperature and salinity changes) or human

derived stressor (such as siltation) and causes changes to the environment. Hence, the

worldwide urbanization in the coastal zones had contributed many human-derived

contaminants. The marginal marine ecosystems act as natural sink for the pollutant

whereas the sediments trap and accumulate pollutant from the water column above.

Over the time, the levels of pollutants accumulated create inhabitable condition for

certain benthic faunas especially those with low tolerance level. The accumulation of

pollutants interrupts the food web and causes deterioration of the aquatic ecosystem.

The Strait of Malacca is known as the busiest route on west coast of Peninsular

Malaysia. Penang Island is one of the islands situated at the northern part of the

Malacca Strait. The island is divided into two parts; the South West Penang Island

and North East Penang Island. The island experiences tropical climates with an

average rainfall of 2500 mm (Malaysian Meteorological Department, 2010). There

are two monsoon seasons that have pronounced effect on Penang Island. The North

East monsoon brings precipitate rain to Peninsular Malaysia in December and

February. The South East Monsoon is known as dry seasons and occurs between

June and August (Chuah et al., 2000).

By year 2011, Penang state was reported to have the highest population density

in Malaysia in which 2 457 people per sq km were recorded on the island while 1on

the main land the density is 1056 people per sq km. More than 80% of the total

population in Penang Island live in the coastal areas. Due to the limited land area in

1
Penang Island (292 km2) and fast growing population, many coastal land reclamation

projects have been carried out to meet the demand. These have started as early as

1970s. As a result of poor planning and rapid development, Penang Island is now on

the edge of losing its natural heritage (Chan et al., 2003; Hong & Chan, 2010).

Thus in 2003, Penang National Park which was formerly known as Pantai Acheh

Reserved Forest is gazetted under the National Park Act of 1980. Penang National

Park hosts unique ecosystems including meromictic lake, mangrove swamp, sandy

beaches and rocky beaches (Hong & Chan, 2010). Sandy beaches in Penang National

Park have long served as nesting area for Green Turtle (Chelonia mydas) and Olive

Ridley Turtle (Lepidochelys olivacea) (Sarahaizad et al., 2012). The presence of rich

biodiversity both in flora and fauna in Penang National Park has made conservation

work more essential.

The main issue faces by Penang Island is the damages of its natural diversities

due to the rapid development. Siltation from construction, poorly managed

ecotourism and fishing activities are among the causes that contribute to this

problem. Hence, despite the conservation efforts that have been made, coastal waters

around Penang National Park are still on threat as marine pollution could not be stop

due to the boundless characteristics of the ocean.

In order to promote better management of land use and coastal waters, it is

important to distinguish the present condition of sediment and water quality around

Penang National Park. A good bio-indicator, the benthic organisms for instance,

would make a good tool for such monitoring. This includes the prominent benthic

macrofauna and meiofauna. In this study, benthic Foraminifera are chosen to be the

monitoring tool as they are proven to be an excellent indicator for sediment quality,

2
heavy metal pollution, organic pollution and water quality (Carnahan, 2005; Hallock

et al., 2003; Sen Gupta, 2003 and Alve, 1995).

Foraminifera are single-celled organisms that consist of cytoplasm with one or

more nuclei (Murray, 1979). Foraminifera have existed as fossil and they are still

living in the modern ocean now. The presence of Foraminifera has been recorded as

early as the Cambarian era. It was during Phanerozoic era, that Foraminifera evolve

and conquer various marine environments and some fresh water biota (Goldstein,

2003). The only reason that makes dating possible in Foraminifera is because they

have shell like structure, known as test. The presence of test which encloses the soft

part of Foraminifera, distinguish this group from other living amoeboid protists

(Phleger, 1960). Most forams possess test which is made from calcium carbonate.

Some with chitinous test and others with agglutinated sand grains test (Phleger,

1960).

Another special feature of Foraminifera is the presence of pseudopodium which

involves with basic functions such as feeding, movement and mating (Goldstein,

2003).

So far, over 40000 species of Foraminifera have been described (Cortés et al.,

2009). Many of the species belong to the benthic groups while a smaller group

belong to the planktonic groups. The planktonic groups reside in the water column

and recorded higher rate of movement. On the other hand, benthic groups reside

within the sediment on the seafloor and have lower rate of movement (Murray, 2006;

Bellier et al., 2010). Identification of Foraminifera is based on several morphological

features. The principle types of chamber arrangement, aperture and test structure are

widely used as keys to classification.

3
 Foraminifera are ubiquitous; they have been recorded on various continental

shelves and slopes (Sen Gupta, 2003). The distribution of Foraminifera is mainly

affected by several microhabitat factors. One of the factors is the combination

between physical, chemical and biological conditions that allows certain species to

successfully survive the ecology while inhabitable to others (Jorissen, 2003).

The Foraminifera has various nutritional modes (Bellier et al., 2010). Therefore

they have successfully dominated most of the marginal and marine habitat. The

Foraminifera’s feeding modes include deposit feeding, carnivore, parasitism,

suspension feeding, grazing, symbiosis and some direct uptake of dissolved organic

carbon (DOC). Foraminifera use their pseudopodial net to trap suspended food

particles and extract food from substrates (Murray, 1979).

Locomotion in forams depends on the pseudopodia. Foraminifera normally have

their pseudopodial net spreads over the substrate and their test aperture facing the

substrate (Murray, 1979).

Foraminifera undergo alteration of sexual and asexual generations (Goldstein,

2003) and grow by increasing their size or by adding new chamber (Goldstein,

2003). Foraminifera play an important role in the trophic level. They serve as food

source to selected shrimps, molluscs and deposit eating invertebrates (Murray, 1979).

They also hold a significant importance as marine heterotrophic protest (Sen

Gupta, 2003). The evolution of Foraminifera, especially those related to

paleoceanographic construction, has received a great attention for the past decade

(Pawlowski et al., 2003). Foraminifera are known for their excellent fossil records,

which allow the study of evolutionary history of the early ocean (Phleger, 1960).

Until recently, Foraminifera have become a famous indicator for pollution

monitoring. Firstly, the presence of shell-like-structure (test) enables Foraminifera to

4
be preserved, hence making the study of the present and past possible (Scott et al.,

2001; Carnahan, 2005). Secondly, the sampling of Foraminifera is cost effective and

by it leaves negligible impacts towards the ecosystem (Alve, 1995). Thirdly, since

Foraminifera occur in high density, small sample is enough to satisfy the statistical

requirement. Finally, the assemblage of Foraminifera is very specific and changes

according to their environment (Alve, 1995; Culver & Buzas, 1995). Hence, many

researchers utilise Foraminifera as indicator in coral reef, subtidal area, estuaries, salt

marshes and mangroves (Scott et al., 2001; Sen Gupta, 2003; Murray, 2006).

Since the assemblage of Foraminifera shifts according to its immediate

environment, many authors have proposed the use of a Foraminifera index. Many of

these indices compare the density of highly tolerant taxa with sensitive taxa. The

Ammonia-Elphidium index was proposed by Sen Gupta (1996) where he uses this

index to represent the presence of oxygen within the sediment. Another index is the

FORAM index (Hallock et al., 2003). This index serves as a monitoring tool that

represents the water quality as well as sediment quality at a particular area. In 2012,

Hallock wrote a review on this index, looking at its problems, advantages and its

applicability. She mentioned that this index has been used successfully in areas

which formerly suspected to require some alterations in the calculations (Hallock,

2012).

Study on Foraminifera in Malaysian waters has started from 2000 by Razarudin.

Later in 2007, several researchers give focus on Foraminifera distribution in

mangrove area. These include studies done by Mohd Lokman et al., (2007) and Wan

Nurzalia (2011). However, the application of Foraminifera as pollution indicator

only takes place in Setiu, Terengganu (Culver et al., 2012). So far, there was no

study on Foraminifera conducted in the vicinity of coastal waters around Penang

5
Island. Thus, it will be such an interesting study to explore the application of

Foraminifera as a monitoring tool and to determine the actual condition of coastal

area surrounding Penang National Park. Moreover, this research will also make a

good baseline study for both, future and present time.

This study used physical and chemical parameters together with foraminiferal

assemblage to determine the present health condition of the coastal waters and

sediment quality around Penang National Park.

Objectives:

The aims of this study are:

1) to determine the distribution and composition of benthic Foraminifera;

2) to assess the state of water quality and sediment quality around the Penang

National Park; and

3) to recognize the possibility in utilising Foraminifera as bio-indicator as an

early pollution indicator.

6
2.0 LITERATURE REVIEW

2.1 Systematic of Foraminifera

When Foraminifera was first discovered in 1700, they were regarded as

Cephalopods. Many naturalists in the early days considered Foraminifera as Nautilus

(Sen Gupta, 2003). Up to the early nineteenth century, the identification of

Foraminifera was based on the aspect of test morphology, particularly the chamber

arrangement. In 1852, d’Orbigny‘s classification changes the way we look at

Foraminifera today (Sen Gupta, 2003). D’Orbigny concluded that, Foraminifera are

unicellular cells and they differ from those found in cephalopods. He classified

Foraminifera within the Class Sarcodina (Sen Gupta, 2003). Carpenter et al., (1862)

focused on wall structure for foraminiferal classification. Joseph A. Cushman, who

was one of the famous Foraminifera taxonomists, started a new classification method

which included the morphology, geological history and regions of distribution

(Cushman, 1928). Important taxonomic work done by Cushman in 1920s’-1940s’

was widely accepted and had influenced the classification of Foraminifera until today

(Sen Gupta, 2003; Murray, 2006).

Two decades after Cushman’s works, Loeblich & Tappan (1964) introduced a

better classification technique by comparing the wall composition and its structure

(Figure 2.1). Recent classification by Lee (1990a) has promoted Foraminifera as a

class instead of an order. Sen Gupta (2003) summarized the recent classification of

Foraminifera in his book; Modern Foraminifera. Currently, this study refers to the

most recent systematic classification of Foraminifera as proposed by Sen Gupta

(2003).

7
Figure 2.1 Types of wall composition and structure used in taxonomic work (Scott et.

al, 2001)

Modern classification places Foraminifera under the kingdom of Protoctista, phylum

Granuloreticulosa and class Foraminifera. There are altogether 16 orders with more

than 4000 living species identified (Bellier et al., 2010).

8
2.2 Morphology and anatomy of benthic Foraminifera

Foraminifera are also known as the hole bearers, made up from cytoplasm,

nuclei and most of them, test. The test comes in various forms and types of wall

composition with obvious soft parts, the reticulate pseudopodia (Murray, 1979). The

wall’s composition and structure is an important feature for classification and

identification purposes (Murray, 1979; Cushman, 1928; Sen Gupta, 2003). The

simplest test form is in Allogromiidae (Cushman, 1928). These single celled protists

accomplish their essential life functions with the help of pseudopodia that may split

and rejoin (Goldstein, 2003).

2.2.1 General morphology for classification

Foraminifera’s simplest test consists of a single chamber while more complex

form can be made up of numerous chambers that are arranged according to growth

pattern (Murray, 1979). The test’s shapes range from coiled to elongate or even a

cylindrical spiral. Primitive and modern foraminifera can be distinguished based on

their shapes. More primitive group in foraminifera tend to be uncoiled compared

with the recent group like Rotaliidae (Cushman, 1928). The basic morphology of test

are; chambers, suture, umbilicus, aperture, rental process, keel and tubercle.

However, not all species possess the entire characteristic mentioned. Figure 2.2 &

2.3 shows a basic diagram of general feature on Foraminifera’s test and the

pseudopodia. Figure 2.4 shows a general morphology used in species identification.

9
 Tubercle

Apertural face Retral process

Aperture

Umbilicus

Suture

Keel

Figure 2.2 General Foraminifera test morphology (Murray, 1979).

Pseudopodia

Figure 2.3 Reticulate pseudopodia used for feeding, mating and locomotion

(Goldstein, 2003)

10
 General morphology of
Foraminifera

Aperture
Chamber arrangement Ornamentation
(Figure 2.6)
Test walls (Figure 2.5) 4a. spines
3a. terminal radiate
1a. organic wall 2a. single chamber 4b. knobs
3b. terminal slit
1b. agglutinated 2b. uniserial 4c. sutures
3c. umbilical
1c. calcareous 2c. biserial 4d. spiral sutures
3d. long-shaped
2d. triserial 4e. costae
3e. interiomarginal
2e. planaspiral evolute
3f. apertural lip
2f. planaspiral involute
3g. simple tooth
2g. milioline
3h. umbilical teeth
2h. streptospiral
3i. phialine lip
2i. trochospiral

Figure 2.4 Diagram on general morphology of Foraminifera according to Cushman (1928) & Sen Gupta (2003).

11
 2a. single chamber 2b. uniserial 2c. biserial

2d. triserial 2e. planaspiral envolute 2f. planaspiral involute

2g. milioline 2h. streptospiral 2i. trochospiral

Figure 2.5 Chamber arrangement used in identification (Sen Gupta, 2003; Loeblich

& Tappan, 1988)

12
 3a. terminal radiate 3b. terminal slit 3c. umbilical

3d. loop-shaped 3e. interiomarginal 3f. apertural lip

3g. simple tooth 3h. umbilical teeth 3i. phialine lip

Figure 2.6 Types of aperture in Foraminifera that are used in identification (Sen

Gupta, 2003; Loeblich & Tappan 1988). Red arrow indicates the aperture opening

13
2.2.2 Test wall composition

The test of forams can be classified into groups based on the materials that

made up the test’s wall. The major groups are; 1) organic-walled test group. It builds

up its test with the secretion of organic materials, 2) agglutinated test group. It makes

its test by agglutinating particles from its immediate environment (Sen Gupta, 2003),

3) calcareous test group refers to forams that has its test wall made up from secreted

calcium carbonate and 4) siliceous test refers to forams that has its test wall made of

silica.

The agglutinated test of forams might contain a wide range of foreign

agglutinated particles such as sand grains, sponge spicules and mica plates. They are

cemented together during test constructions (Bellier et al., 2010; Goldstein, 2003;

Cushman 1928). Certain species in this group use whichever particles that are

available, while others may be selective (sponge spicules, quartz grains or mica

flakes) when constructing their test (Cushman, 1928; Sen Gupta, 2003; Goldstein,

2003; Bellier et al., 2010).

14
2.2.3 Chambers arrangement

The number of chambers present in forams and their form of arrangements

are of great diversity. Below are common types of chambers arrangement of benthic

forams along Penang coastal waters. The simplest form of chamber arrangement is

the single chambered test that consists of spherical or tubular chamber (as shown in

Fig 2.4 2a). Single series chamber that is added in straight line or slight curved

alignment is uniserial and double linear series chamber is biserial. On the other hand,

triple linear series chamber is triserial and multiserial if more than three chambers are

arranged together in a linear series. The planaspiral test has its chambers arranged in

spiral within a single plane. This type of chamber arrangement may make the test

looks similar on both sides. The evolute planaspiral (Fig 2.4 2e) has visible whorls

while involute planaspiral (Fig 2.4 2f) has only the last whorl is visible. The

trochospiral chamber arrangement (Fig 2.4 2i) is almost similar to the planaspiral but

in trochospiral test, the dorsal’s and ventral’s face are different. However, in the

miliolids group, the curved chambers are arranged in series where each successive

chamber is placed at an angel up to 180⁰ from the previous one (Fig 2.4 2g).

Numerous other types of chamber arrangement may also present in Foraminifera.

15
2.3 Habitat and ecology of benthic Foraminifera.

2.3.1 Distribution and diversity

There are two main groups of Foraminifera. First, is the highly diverse

benthic group and second, is the planktonic group (Sen Gupta, 2003; Murray, 2006).

The distributions of planktonic groups are confined to open water settings (Bellier et

al., 2010). They are usually found floating in near-surface waters to depth of several

hundred meters. Benthic Foraminifera on the other hand, which are a more sessile

group may be found on the surface of the sediment, within the sediment or found

attached to substrates (Murray, 2006). They occupy in all marine habitats including

marginal environment (lagoons, estuaries, deltas, mangroves and saltmarshes),

coastal water and deep sea (Scott et al., 2001). However, it is obvious that many

species prefered relatively shallow waters, where there will be enough light

penetration and food supply (Bellier et al., 2010). Therefore, higher diversity of

Foraminifera was discovered on continental shelf, especially in reef environments

(Scott et. al, 2001; Murray, 2006; Bellier et al., 2010).

The distributions of Foraminifera species were determined by environmental

factors such as oxygen level, organic matter content, salinity and temperature. The

agglutinated Foraminifera species preferred area with low temperature and salinity

(Scott et al., 2001). The larger carbonate secreting species on the other hand chose to

live in area with high as well as stable temperature, salinity and pH (coral reef

environment).

Benthic Foraminifera’s species that inhabit marginal environment (e.g.

mangrove) are characterized with high tolerances towards alternation of salinity,

temperature and pH. Typical Foraminifera that inhibit the mangrove environment

16
largely possess agglutinated and hyaline test (e.g. Ammonia, Quienquloculina,

Ammotium, Arenoparrella, Cribrononion, Elphidium) (Sohrabi-Mollayousefy et al.,

2006; Murray, 2006; Javaux & Scott, 2003; Scott et al., 2001). A study done by

Biswas (1976) on foraminiferal assemblage in Sumatra mangrove indicated the

presences of common species belong to agglutinated forms.

Nearshore environment with shallow water condition (1 m – 20 m) favours

the distribution from the order of Rotaliida, Buliminida and Textulariida (Murray,

2006, Phleger, 1960). According to Sen Gupta (2003) typical intertidal communities

are includes the calcareous species such as Ammonia beccarii and Elphidium

williamsoni. In many shallow near shore settings, several significant factors that

may influence the communities are types of substrate, current, salinity, pore-water

oxygen content and wave action. Coastal waters with high organic matter and low

oxygen content seem to favour less number of species. These species are usually

known either as stress-tolerant taxa or opportunistic taxa (Hallock, 2003; Carnahan,

2005). Therefore, Ammonia and Elphidium (both stress-tolerant taxa) are usually

found to dominate the assemblages in polluted coastal environment (Alve, 1995;

Scott et al., 2001).

Symbiont-bearing Foraminifera are known to host various types of algae.

This group of Foraminifera is usually larger in size and prefers places that receive

enough sunlight. Due to this, the symbiont-bearing Foraminifera exhibit high

diversity at tropical regions especially in coral reef ecosystem (Hallock, 2003). As

larger symbiont-bearing Foraminifera prefer more stable environment (Murray,

2006), any subtle changes (i.e. nutrient loading, increase in temperature) may cause

serious threat to its existence. Consequently, as proposes by Hallock et al. (2003)

symbiont-bearing Foraminifera will make a good indicator for the reef vitality

17
2.3.2 Nutrition

Foraminifera practise various types of nutrition modes which includes

grazing, carnivory, herbivory, direct uptake of dissolved organic carbon (DOC),

omnivorous, passive suspension feeding, parasitism, resource partitioning and

symbiosis (Goldstein, 2003; Murray, 2006).

Herbivory group of Foraminifera is divided into two; 1) passive herbivore -

they have restricted movement and only feed on food availability around the sites of

attachment and 2) active herbivore - they use reticulopodia to move and collect food

particles (Murray, 2006). Herbivorous Foraminifera feed on algae, diatoms and

bacteria that are abundant at the euphotic zone. Carnivorous feeding mode can be

found in both benthic and planktonic groups (Goldstein, 2003). Omivorous group is

also common in benthic Foraminifera. They feed on both animals and plants that are

easily available for this kind of group (Murray, 2006).

Foraminifera which are passive suspension feeder are usually either epifaunal

or sessile. They attach to hard substrate and filter food particles as water current pass

through them (Murray, 2006).

Some species of free-living Foraminifera practice parasitism nutrition mode.

This group usually infests on other Foraminifera, mollusc, sponges or stone coral

(Goldstein, 2003).

Apart from that, symbiosis nutrition mode occurs in the symbiont-bearing

Foraminifera where by larger Foraminifera host autotrophic endosymbiotic algae

(Murray, 2006). This mode of feeding is more common in larger tropical

Foraminifera (Hallock, 2003). Hallock (2003) lists three potential benefits of

18
endosymbiosis to Foraminifera; 1) energy from photosynthesis, 2) enhancement of

test calcification and 3) uptake of host waste metabolites by algae.

2.3.3 Reproduction

Generally, Foraminifera are characterized with a complex life cycle known as

the alternation of generations i.e. alternation between haploid and diploid generations

(Goldstein, 2003). However, not all species perform the same life cycle. In some

species, alternation of generation reproduction is known to be obligatory while others

may be facultative (Goldstein, 2003). The Foraminifera are known as gamont during

haploid phase and agamont during diploid phase

2.4 Significant of benthic Foraminifera

Benthic foraminiferal assemblage has various significant usage and

application. Among these are biostratigraphy (Culver & Buzas, 2003; Afzal et al.,

2005), paleoecology (Culver, 1996) and paleoceanography study (Ta et al., 2001;

Horton et al., 2007). Moreover, Foraminifera are highly utilised as proxy for

anthropogenic pollution (Burone et al., 2007; Carnahan et al., 2009; Martinez-Colon

& Hallock, 2010; Buosi et al., 2010), coral reef condition (Hallock et al., 2003) and

other environmental changes (Mendes et al., 2004).

In the early days, the applications of Foramnifera were formerly associated

with paleontology and oil exploration. It was about three decades ago, scientists had

started using forams in pollution monitoring study. A case study in Chesapeake Bay

showed that the abundance of Ammonia has significantly increased between 1680

and 1970 (Murray, 2006). Scientist believed that the increased of Ammonia is due to

hypoxic condition brought by anthropogenic activities. Alve (1995) had done an

extensive review on Foraminifera as indicators in marginal environment, in which

19
she compared the characteristic of foraminiferal assemblages with the types of

pollutant. She founds that the ability of different species to withstand different types

of pollution, made Foraminifera as excellent proxies of pulp (paper), chemical, heavy

metal, oil, thermal and aquaculture originated pollutants. Study by Frontalini and

Coccioni (2008) confirmed the suitability of benthic Foraminifera as indicator for

heavy metal pollution in marine coastal settings. Test deformation (Figure 2.7) in

Foraminifera species is typical at sites that are affected with heavy metal pollution.

Similar results are obtained from a research done by Carnahan (2005) in Biscayne

Bay. Ammonia beccarii and Elphidium excavatum are two common species

confirmed to be associated with pollution (Murray, 2001).

Figure 2.7 Examples of test deformation and abnormalities in Foraminifera (modified

from Sen Gupta, 2003)

The symbiont-bearing groups are Foraminifera that perform symbiosis with

the algae found in coral reef area. Several authors utilize the symbiont-bearing

Foraminifera to monitor water quality (Uthicke & Nobes, 2008; Uthicke et al., 2010;

Narayan & Pandolfi, 2010) while others use this group to indicate the health of coral

reef (Hallock et. al, 2003; Suhartati, 2010). Hallock et al. (2003) has suggested an

application of Foraminifera in Reef Assessment and Monitoring (FORAM) Index to

monitor the condition of coral reef and environment suitability for the continuation

20
of reef growth. This index also provides a measurement of the water quality at the

monitoring area. As Foraminifera index shifts according to their immediate

environment, Hallock et al. (2003) divides them into functional groups. Table 2.1

shows the functional groups and the genera classified under them. Symbiont-bearing

groups are reef-associated Foraminifera and they live side by side with symbiotic

algae. The stress-tolerance taxa on the other hand are an opportunistic group. They

may tolerate larger environmental changes. Hence, more symbiont-bearing taxa over

stressed-tolerant taxa indicate better water quality.

In biostratigraphy and palaecology study, researchers utilize the modern

foraminiferal assemblage as analogues of the past in an attempt to understand the

past environmental conditions (Murray, 2006; Friedrich, 2010; Ta et al., 2001).

Preservation of their test in marine sediment over the years has created a timeline.

For example, foraminiferal test near Mekong River are used in carbon dating in an

attempt to understand the sea level changes since the late Pleistocene (Ta et al.,

2001). One research in the Gulf of Mexico has employed Foraminifera as a tool in

dating the age of the Gulf (Arz et al., 2004).

In palaeoceanography study, Foraminifera play a role as indicator of sea level

changes. Foraminifera offer accurate zonation that enables us to detect even small

sea-level changes (Scott et al., 2001). Besides that, coastal Foraminifera were also

used to interpret seismic events and tsunami occurrence by looking at species

assemblages in the sediment. (Scott et al., 2001; Hawkes et al., 2007)

21
Table 2.1 FORAM index functional groups, genera and their distribution. (Modified from Hallock et al., 2003 and Carnahan, 2005).

Functional Group Order Family Genera Distribution

Amphisteginidae Amphistegina Circumtropical
Rotaliida Calcarinidae 5 genera Indo-Pacific
Nummulitidae Heterostegina Circumtropical
Alveolinella Indo-Pacific
Alveolinidae
Symbiont-bearing Borelis Circumtropical
Peneroplidae Several genera Circumtropical
Miliolida
Sorites Circumtropical
Soritidae Amphisorus Circumtropical
Marginopora Indo-Pacific
Trochamminida Trochamminidae Several genera Cosmopolitan
Textulariida Lituolidae Several genera Cosmopolitan
Bolivinidae Several genera Cosmopolitan
Stress-tolerant Buliminida
Buliminidae Several genera Cosmopolitan
Rotaliidae Ammonia Cosmopolitan
Rotaliida
Elphidiidae Elphdium Cosmopolitan
Miliolida Most execpt larger taxa noted above Cosmopolitan
Rotaliida Most except those noted above Cosmopolitan
Other Small Taxa Other Most Cosmopolitan
Textulariidae Textularia Cosmopolitan
Textulariida
Astrohizidae Bigenerina Cosmopolitan

22
 Oxygen is one of the limiting factors towards benthic foraminifera in shallow

region (Scott et al., 2001) thus benthic Foraminifera make an excellent indicator of

sediments hypoxic condition (Bernhard et al., 1997). Certain species of forams are also

known as the opportunistic species. They may strive better in oxygen depleted

environment compare to others. Therefore, suggestion in using Ammonia – Elphidium

Index is very applicable in monitoring the bottom water oxygen concentration (Sen

Gupta, 2003).

The ability of Foraminifera to indicate changes makes it as a popular tool in

ocean monitoring. The availability of various indices related to Foraminifera makes

them easy to be employed at most study sites.

23
2.5 Past studies on Foraminifera.

The discovery of Foraminifera dated back to the eighteenth century when the

invention of microscope takes place. A drawing of Elphidium by Leeuwenhoek proves

the discovery of Foraminifera as early as 1700. However, the name ‘Foraminifera’ was

not yet introduced back then. Most authors have mistaken Foraminifera with mollusk,

cephalopods and even worm (Sen Gupta, 2003; Murray, 2006).

During the nineteenth century, works that have been done were more focused on

classifying these shelled protists. A famous researcher, d’Orbigny (1826) classified

Foraminifera within the class Cephalopodes. He named the order Foraminifera (hole

bearing) after the discovery of hole on the test (Sen Gupta, 2003; Lipps et al., 2011).

Another distinguish taxonomic work was carried out by Brady (1884), in which he

examined samples from the Challenger expedition (Sen Gupta, 2003). Other major

contributors in the nineteenth century include work from Williamson and Carpenter

(Murray, 2006; Lipps et al., 2011).

There were increases of ecological works as well as acknowledged classification

on Foraminifera throughout the twentieth century. Authors that contributed to taxonomic

work during that time were Cushman (1928), Loeblich & Tappan (1964) and Lee

(1990a). The ecological work on Foraminifera started in 1935 by Rhumber (Murray,

2006). Since then, growing interest in Foraminifera reproduction mode, habitat, nutrition

and growth, had led to the increase of ecological works done by other researchers.

According to Sen Gupta (2003), the research in Foraminifera ecology were intensified

due to their ability in providing clues to the understanding of geological changes in the

past. Early works on significant use of benthic Foraminifera as proxy indicator were

initiated by Resig (1960) and Watkins (1961) in the early 1960s’ (Alve, 1995). In late
24