STUDY ON DISTRIBUTION OF CORALS AND OTHER ASSOCIATED COMMUNITIES IN THE COASTAL WATERS OF

By Amjad Ali M.Phil.

Centre of Excellence in Marine Biology, University of , Karachi, Pakistan 2017 STUDY ON DISTRIBUTION OF CORALS AND OTHER ASSOCIATED COMMUNITIES IN THE COASTAL WATERS OF PAKISTAN

Thesis submitted to the for the partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ph.D)

By Amjad Ali M.Phil.

Centre of Excellence in Marine Biology, University of Karachi, Karachi, Pakistan 2017 Declaration

I Amjad Ali s/o Roshan Din do hereby declare that this work has been originally carried out by me under the guidance of Dr. Pirzada Jamal A. Siddiqui, Professor, Centre of Excellence in Marine Biology, University of Karachi for the partial fulfillment of the requirements for the degree of Doctor of Philosophy and this work has not been submitted elsewhere for any other degree.

Amjad Ali Center of Excellence in Marine Biology. Universityof Karachi.

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Certificate

This thesis by Mr. Amjad Ali is accepted in the present form by the Centre of Excellence in Marine Biology, University of Karachi, as satisfying the requirements for the degree of Doctor of Philosophy in Marine Biology.

Internal Examiner Thesis supervisor

External Examiner

Director Center of Excellence in Marine Biology, University of Karachi

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Dedicated to my Late Father Roshan Din, Loving and

caring Mother for their efforts to educate me, Wife,

Brothers, Sisters, Nephews for moral support

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Lovely Daughter, Noor Fatima

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Table of Contents

Title page Declaration ii Certificate iii Dedication iv Table of contents v List of figures vii List of tables ix Acknowledgements x Abstract () xi Abstract (English) xiii List of publications xv

Chapter 1 1.1. General Introduction 02 1.2. Materials and Methods 10 1.2.1. Study sites 10 1.2.2. Methods 10 1.2.2.1. Field techniques for coral, invertebrate and fish communities 10 1.2.2.2. Field techniques for macroalgal communities 11 1.2.2.3. Field techniques for fossil coral communities 11 1.2.2.4. Sea water physico-chemical parameters 12 1.2.2.5. Elemental analysis of coral skeletons 13 1.2.3. Statistical analysis 13 Chapter 2 Physico-chemical Conditions 20 2.1. Abstract 21 2.2. Introduction 22 2.3. Materials and Methods 24 2.4. Results 24 2.4.1. Seawater physico- organic parameters 24 2.4.2. Dissolved inorganic nutrients 24 2.4.3. HCO3-, CO3- and HO- concentrations 24 2.4.4. Elemental analysis of coral skeletons 25 2.5. Conclusions 31 Chapter 3 Reef and Associated Fauna in the Coastal Waters of , Pakistan 32 and an Assessment of Environmental Impacts 3.1. Abstract 33 3.2. Introduction 34 3.3. Material and Methods 36 3.4. Results 36 3.4.1. Description of survey sites 36

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3.4.2. Coral communities 36 3.4.3. Fish communities 37 3.4.4. Invertebrate communities 38 3.4.5. Seawater physico-chemical parameters and elemental composition of 39 coral skeletons 3.5. Discussion 57 3.5.1. Coral communities 57 3.5.2. Fish communities 59 3.5.3. Invertebrate communities 60 3.6. Threats and recommendations 60 Chapter 4 Characterization of Macroalgal Communities in the Coastal Waters of 62 Sindh (Pakistan), a Region under the Influence of Reversal Monsoons 4.1. Abstract 63 4.2. Introduction 64 4.3. Materials and Methods 65 4.4. Results 65 4.4.1. Description of survey sites 65 4.4.2. Benthic macroalgal communities 65 4.4.2.1. Pre-cyclonic communities 66 4.4.2.2. Post-cyclonic communities 66 4.5. Discussion 73 4.6. Threats and recommendations 75 Chapter 5 Quaternary Fossil Coral Communities in the Uplifted Strata along the 76 Balochistan Coast of Pakistan: Understanding Modern Coral Decline in the 5.1. Abstract 77 5.2. Introduction 78 5.3. Materials and Methods 80 5.3.1. Geological description of sites 80 5.3.1.1. Gwadar headland 80 5.3.1.2. Jiwani 80 5.4. Results 81 5.4.1. Description of survey sites 81 5.4.2. Fossil corals 81 5.5. Discussion 92 5.6.Threats and recommendations 95 Chapter 6 General Discussion 97 References 102

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List of Figures

S# Page# 1.1 World distribution of corals (Courtesy NOAA) 09 1.2 Arabian Sea with adjacent gulfs and seas 09 1.3 Map of Pakistan coast line with inset showing the study sites for 14 coral, seaweed, fish and invertebrate communities 1.4 Map showing Makran subduction zone (MSZ) in the coastal reagion 14 of Pakistan and Iran and other structural features in northern Arabian Sea. Inset showing study sites at Gawadar and Jiwani, Blaochistan coast for fossil corals 2.1 Mean (n = 3) seawater physical and organic parameters recorded 26 once from surface and bottom at 4 locations along the Sindh coast, Pakistan 2.2 Mean (n = 3) dissolved nutrient concentrations recorded once from 27 surface and bottom at 4 locations along the Sindh coast, Pakistan 2.3 HCO3- (mg/L), CO32- (mg/L) and HO- (mg/L) concentrations of 28 seawater recorded once during sampling period with initial temperature(°C) and pH recorded at the time of analysis 2.4 Total hardness of (n=3) of seawater samples recorded once during 29 sampling period 2.5 Elemental concentrations of EDS spectrum of coral skeletons 30 collected from different locations along the Sindh coast of Pakistan 3.1 A-B Diversity of stony coral species recorded from the littoral waters of 46-47 Sindh, Pakistan 3.2 Corals degredation due to bleaching, bioerrosion and change in 48 community structure at Mubarak Village and Churna Island 3.3 Cluster analysis for coral communities at 8 diving sites based on 49 root transformation of data and Bray Curtis similarity index using group average linkage techniques 3.4 The K dominance curves (a: cumulative, b: partial) for coral 49 communities at 8 dive sites 3.5 A-C Diversity of fishes recorded from the littoral waters of Sindh, 50-52 Pakistan 3.6 Cluster analysis for fish communities at 9 dive sites based on 52 presence-absence data and Bray Curtis similarity index using group average linkage techniques 3.7 The K dominance curves for fish communities at 9 diving sites 53 3.8 A-B Diversity of invertebrates recorded from the littoral waters of Sindh, 54-55 Pakistan 3.9 Cluster analysis for invertebrate communities at 9 dive sites based 56 on root transformation data and Bray Curtis similarity index using group average linkage techniques 3.10 The K dominance curve (Cumulative dominance) for invertebrate 56 communities at 9 dive sites

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4.1 A-B Diversity of macroalgal species recorded from littoral waters of 70-71 Sindh, Pakistan 4.2 Cluster analyses for macroalgal species conducted at 5 dive sites on 72 the bases of presence-absence data and Bray–Curtis similarities 4.3 K. dominance curves (cumulative dominance) for macroalgal 72 species at 5 dive sites 5.1 A-B Diversity of fossil corals recorded from uplifted strata at Jiwani and 86-87 Gwadar along Balochistan (Makran) coast, Pakistan 5.2 Comparison of modern corals collected from coastal waters with 88 fossil corals from coastal uplifted strata (Makran, Balochistan), Pakistan 5.3 Comparison of modern Porites species collected from coastal waters 89 with fossil Porites species collected from coastal uplifted strata (Makran, Balochistan), to check the effects of bioerrosion 5.4 Cluster analyses of similarities between fossil coral community 89 composition at 9 transacts, based on presence-absence data and Bray–Curtis similarities 5.5 K. dominance curves (a: cumulative dominance, b: partial) for fossil 90 coral communities at 9 transacts 5.6 Cluster analyses of species composition of Quaternary, modern and 91 Miocene coral communities based on presence-absence data and Bray–Curtis similarities 5.7 Cluster analyses of genera composition of Quaternary, modern and 91 Miocene based on presence-absence data and Bray–Curtis similarities

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List of Tables

S# Page# 1.1 Abundance ranking for coral and invertebrate communities 15 1.2 General observations recorded at each site with GPS coordinates and 16 respective depths 1.3 General observations recorded at each site with GPS coordinates and 19 elevations from sea level 2.1 Percentage weight concentrations of different elements in coral skeletons 25 collected from different locations along the Sindh coast of Pakistan 3.1 Hard coral species recorded from 8 diving sites 40 3.2 Abundance and distribution of hard coral species collected from 18 dive sites 41 located along the coast of Pakistan with respective depth 3.3 Diversity of fishes recorded at 9 diving sites 43 3.4 Diversity of Invertebrates recorded at 9 diving sites with relative abundance 45 4.1 Distribution and abundance of macroalgal species collected before and after 68 cyclone from 5 dive sites situated along the Sindh coast of Pakistan 5.1 List of fossil coral, collected from an uplifted location at Ras Gunz near 82 Jiwani, Balochistan 5.2 List of fossil corals collected from uplifted strata at Gawadar (GH) and 83 Jiwani (J1, J2, along Balochistan coast of Pakistan. 5.3 List of families and genera of Quaternary and modern corals recorded in 85 uplifted strata of Balochistan and coastal waters

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Acknowledgements

Innumerable thanks to Almighty Allah for countless blessing and keeping determinant during study period. A great number of people have helped and been of assistance to me during study. I would like to thank them all. I would particularly like to thank my research supervisor Dr. Pirzada Jamal A. Siddiqui, Professor Centre of Excellence in Marine Biology University of Karachi for his guidance and supervision during the period of study. My special and sincere thanks to Professor Dr. Rupert Ormond, Ex. Director, University of London, Marine Biological Station Milport for introducing me the wonders of the sea. Thanks to Professor Dr. Tasneem Adam Ali, Director of Center of Excellence in Marine Biology, University of Karachi for providing facilities.

Special thanks to my colleagues especially Dr. Pervaiz Iqbal (University of Poonch, Azad Jammu & Kashmir) and Naveed Khan (CEMB), for their help during sampling from uplifted strata along the Balochistan coast. I am also thankful to my collegues especially, Dr. Munawwer Rashid, Dr Muhammad Ibrahim (PSQCA, Karachi) and Dr. Seema Shafique for their their help in chemical analyses of water samples. Many thanks to my dive patner Mr. Javed Saqi (Ex. commando ) for providing safety during the period of underwater surveys.

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Abstract

This study deals with the distribution pattern and diversity of hard corals and associated and non-associated communities (fish, invertebrates and seaweeds) in the coastal waters of Sindh as well as paleodiversity of hard coral settings in the uplifted strata along Balochistan coast of Pakistan. Chapter 2 reports on live corals collected through SCUBA surveys, coral-associated fauna (fish, invertebrates), and environmental impacts on the calcareous (corals). A total of 21 hard coral are first report from Pakistan. All together 50 live coral species recorded from Pakistan. In addition, 13 molluscs, 3 , 3 sea anemones, 3 echinoderms, 2 and 54 fish species were also identified and recorded. Fishes were not documented scientifically but relayed on photographs taken in situ for identification. Semi-quantitative measure of relative abundance (DACFOR scale) of corals and other invertebrate fauna indicated that northern sheltered sites of Churna Island followed by Mubarak Village support high - 2- - diversity of corals, and other associated fauna. HCO3 , CO3 and OH were determined. No significant acidification impacts were noted as pH values remained in the normal range particularly in offshore waters (Churna Island) but pH levels are decreasing. Fish and invertebrates distribution patterns appeared to be associated with habitat complexity. Further studies on large scale with special focus on chemical and environmental parameters are recommended. Chapter 3 deals with characterization of macroalgal communities in the subtidal coastal waters of Sindh. Rich algal flora is reported from the coast of Pakistan supported by nutrient loadings through convective mixing and up- sloping of nutrient rich upwelled waters. Previous studies on seaweeds in Pakistan are mainly confined to intertidal areas or on the basis of drift samples with much emphasis on and phycochemistry without an in-depth study of the ecology. The present study reports for the first time the outcome of underwater surveys at 5 dive sites. Quadrat techniques were used to determine the relative diversity and abundance of benthic macroalgal communities. A total of 36 species (16 Phaeophyceae, 12 Rhodophyta, and 8 Chlorophyta) were recorded. An increase in diversity and distribution patterns was noted from west to east along the coast. High diversity occurred at Hawks Bay followed by French Beach. The coral sites (northern sheltered site of Churna Island and Mubarak Village) had less diversity. Very few recorded species had a restricted distribution (Yemen, Oman and India). One species (Stypopodium shameelii) was found endemic to Pakistan whereas the rest are widely distributed in the entire Indian Ocean, Atlantic and

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Pacific. Distribution and diversity patterns appeared to be linked with habitat type, topography, wave exposure and prevailing climatic conditions. Growth of seaweed appears to be impacted through oceanic processes. For example, stunted growth of Sargassum species and changes in community structure were observed after the Cyclone ‘NILOFAR’. Anthropogenic threats currently are not evident on seaweed communities. Huge beds of Sargassum were observed in submerged habitats along the Karachi coast. Their sustainable use can provide alternative source of livelihood for coastal communities and can reduce pressure on fisheries sector that is already under stress. The fossil coral communities in the uplifted strata along Balochistan coast of Pakistan and their comparison with the modern distribution of hard corals in Pakistan waters is reported in Chapter 4. Being important palaeoclimate archives and a rich source of information on past, uplifted Quaternary terrain along Balochistan coast is the perfect place to study the palaeoclimatic and geological changes that have shaped the Balochistan coast. The present study fills the gap exists in the knowledge pool on the palaeodiversity of corals in this region. The samples collected using line intercept method from four uplifted sites (Balochistan coast: one at Gwadar, and three at Jiwani) were analysed for relative distribution and diversity of Scleractinian fossil corals. A total of 48 fossil coral species were recorded in nine families and 22 genera. High diversity of corals was recorded in the uplifted landward sites of Jiwani and Gwadar headland. Terraces close to the shore at Jiwani had lower diversity. The corals seem to be Quaternary; most likely Pleistocene to Holocene. Comparing fossil fauna with modern distribution indicated that modern fauna lacks many species recorded in the fossil community, thus suggesting a faunal turnover in diversity and redistribution of coral fauna, which may be linked with past geological events and increasing anthropogenic pressure. Finely, for the development of effective conservation strategy detailed studies are desiredable in uplifted strata and submerged habitats with respect to climatological, environmental, anthropogenic and geological variations. As coastal environment does not seem to favour coral growth, conservation of already existing coral sites is necessary. The local community and wider public may be involved in restoration work so that they can appreciate the importance of these natural resources. Development of artificial reef at suitable low energy submerged habitats would provide a chance for many species to grow. These reefs and natural coral sites (Churna and Astola Islans) may be used as sites for pleasure diving and for the promotion of ecotourism.

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List of Publications

Following articles has been published from this work:

1. Siddiqui, P. J.A., Ali, A., Bromfield, K. Iqbal, P. & Shoaib, N. (2011). Identification of fossil corals inhabiting an uplifted area of Ras Gunz near Jiwani, Balochistan, Pakistan. Pakistan Journal of Zoology. 43 (3), 523-527. 2. Ali, A., Siddiqui, P.J.A. & Aisha, K. (2017). Characterization of macroalgal communities in the coastal waters of Sindh (Pakistan), a region under the influence of reversal monsoons. Regional Studies in Marine Science, 14, 84–92.

3. Ali, A., Siddiqui, P.J.A., Bromfield, K., Khan, A.A., & Iqbal, P. (2017). Quaternary fossil coral communities in uplifted strata along the Balochistan coast of Pakistan: understanding modern coral decline in the Arabian Sea. Arabian Journal of Geosciences (Accepted).

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Chapter 1

General Introduction

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1.1. General Introduction Coral reefs are the most composite marine communities representing a bank of biological diversity and provide ecological goods and services to many countries (Connell, 1978; Reaka-Kudla, 1997; Moberg and Folke, 1999). About 30 billion US$ are annually contributed by reef system to world economy through tourism, coastal protection and fisheries (Paulay, 1997; Cesar, 2003). Besides live corals, the fossil corals also serve as important palaeoclimate archives (Felis and Patzold, 2003) and have great geologic and archaeological significance (Moursi, Hoang, and Fayoumy, 1994; Walter et al., 2000). They provide a rich source of information on: the past physical and geochemical changes; biological diversity over large temporal scales; and the response of living organisms to past and present climatic changes in their surroundings (Sepkoski, 1997; Gagan et al., 2000; Honisch et al., 2004; Pandolfi and Greenstein, 2007). Globally, reefs are distributed in a circum-tropical band mostly between Latitudes 20o North and 20o South. The western Atlantic and the Indo-Pacific are the two main coral reef provinces in the world (Fig.1) (Gosliner, Behrens, and Willians, 1996). Instead of large number of benefits, the reef system globally and on regional scale facing serious impacts, both human and natural (Endean, Cameron and Devantier, 1988; Foster et al., 2011; Riegl et al., 2012; Bauman et al., 2013; Burt, 2014; Burt et al., 2016; Warner, Fitt, and Schmidt, 1996; Mc Clanahan, 2004; Coles, 2008; Crabbe, 2008; Mumby et al., 2014; Bozec and Mumby, 2015; Rogers, 1990; Riegl, 1995; Erftemeijer et al., 2012; Bartley et al., 2014; Junjie et al., 2014; Jones, Ricardo, and Negri, 2015). The manmade threats mostly include high sedimentation rates due to land clearing and coastal development, chemical and nutrient pollution, ocean acidification and global warming due to rapid industrialization, habitat destruction due to overfishing and use of destructive fishing techniques such as use of dynamite and cyanide, recreational use, breakage of corals for sale and causing impacts due to faulty boat anchoring and tourism trampling. The natural threats mostly include cyclones, hurricanes, El Nino, action of earthquakes and volcanoes and periodic population pressure of Acanthaster planci. Outbreaks of A. planci are considered to be enhanced by human activities of nutrient enrichment promoting larval survival and/or removal of predators (Brodie et al., 2005; Rotjan and Lewis, 2008; Stella et al., 2011; Brodie, Devlin, and Lewis, 2017). During recent decades, as a result of industrialization and burning of fossil fuels, the level of atmospheric carbon dioxide increased drastically. Due to the absorption of extra atmospheric carbon dioxide, a

2 change occurred in ocean chemistry that ultimately effect on calcifying animals (corals, mulluscs, shell forming echinoderms) and fish (Zeebe and Gladrow, 2001; Royal Society, 2005; Hoegh-Guldberg et al., 2007; Fabry et al., 2008; Doney et al., 2009). Reef formation is basically the accretion of CaCO3 secreted by corals. Decline in calcification reduced the process of reef formation. It is expected that aragonite saturation state will decrease up to 30 % due to increase in concentration of carbon dioxide in 2050 (Kleypas et al., 1999). In addition to ocean acidification, rising sea surface temperature is considered as a major threat for reef system across the globe. Degradation of corals on large scale has been occurred during different bleaching events. About 16% tropical reef has been destroyed completely during the bleaching event of 1998. Around 42 % reefs bleached in Great Barrier Reef while around 18% seriously bleached. During the bleaching event of 2002, about 54 % corals bleached in the Great Barrier Reef (Wilkinson 2002; Berkelmans et al., 2004). On large scale, mortality of corals also reported from Eastern Pacific. For example, in Galápagos Islands, the mortality of Pocilloporaspp species occured on a large scale as a result of ENSO (ElNino southern oscilation) (Baums et al., 2014). Incidents of coral bleaching due to increase in sea surface temperature also reported from different parts of the Arabian/ Red Sea. In Bahrain, during the 1996 bleaching event, Acropora species mostly growing in shallow waters were completely removed whereas two third of reefs bleached at deeper depth (40 m). During the bleaching event of 1996, coral cover in Jebel Ali and Ras Hasyan (UAE) reduced from 90 % to 26%. Further bleaching event of 1998, reduced the coral cover from 26 to 22 %. Overall, 90% coral loss in Arabian Sea region was mainly due to increase in sea surface temperature (Wilkinson, 1998; Uwate and Shams, 1999; Al-Kuwari, 2006; Furby, Boumeester, and Berumen, 2013). High sea temperatures and ocean acidification leading towards increase in habitat marginality. It is expected that near the end of this century, major reef centers will be marganilized. The areas of high biodiversity will face high temperature situations. On the other hand, positive effects will be inserted on areas that are currently subjected to low temperature. In this regard, the future of coral reef will depend up on acclimative and adaptive abilaties of communities and organisms (Guinotte, Buddemeier, and Kleypas, 2003; Hoegh-Guldberg et al., 2007). Marginal environment is basically a condition where coral grow in a stressful environment i.e. high or low nutrient concentrations, poor visibility (either by phytoplankton blooms or high sediment load), temperature fluctuations and minimum aragonite saturation settings (Kleypas, McManus, and Menez, 1999; Perry and

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Larcombe, 2003). Physico-chemical limits for reef development are known (see Kleypas, McManus, and Menez, 1999). Marginal communities due to their survival in already strained conditions have abilaties to adopt environment altered by worldwide climate change (Glynn, 1996: Riegl and Piller, 2003).

Cyclones, earthquakes and tsunamis are also considered as major threats for corals. About 50 % coral cover was damaged by cyclone ‘GONU’ in the Gulf of Oman (Foster et al., 2011). On large scale, corals were destroyed due to the earthquake of 26th December 2004 (with a moment magnitude 9.0), occurred in offshore waters of northern Sumatra (Indonesia). At Simeulue Island (Indonesia), large raised reef came out of water. High tsunamis (about 20 meters at some locations) generated as a result of earthquake also damaged corals on larger scale in Indonesia and Thailand. About 7.2% to 39.7% of the total live coral cover was damaged at Mu Ko Similan Marine National Park, Thailand. Further underwater surveys at different reef sites in Indonesia indicated that physical damage to corals by tsunami was minor compare to damage caused by earthquake (Chavanich et al., 2008; Foster et al., 2006; Pomonis et al., 2006; Sheth et al., 2006). Cyclonic histry of the Arabian Sea from 1891-2010, revealed a positive trend in frequency data of the cyclones. Most of the cyclones occurred during the months of October (43) and November (37). Minimum cyclonic frequencies were noted during the months of February (0), January (1), March (0) and April (8) (Hussain, Abbas, and Ansari, 2011). Since 1945, about 29 major cyclones were recorded in the Arabian Sea. Among them, the cyclone ‘NILOFAR’ occurred in the Arabian Sea during the last week of October, 2014, was considered as strongest tropical cyclone. With in few days, the cyclone got an intensity of 950 mbar. 4. The storm pursued northeastwards and produced high waves (12.8 m) especially in the middle part of the Arabian Sea that sustained for a short period of time (13.3 s) while waves with height greater than 8 m, sustained for at least a peiod of half day. Low cyclonic intensity was observed especially along the coast of Oman (Sarker, 2017).

Located on northern side of the Indian Ocean, the Arabian Sea is bounded on the east by India, by Arabian Peninsula on the north-west, by Pakistan and southern part of Iran on the north-east and by Somalia and Socotra on the south-west. It has two important branches, the Gulf of Aden on the southwest and the Gulf of Oman on the northwest. The Gulf of Aden connects it with Red Sea via strait of Bab-el-Mandeb and Gulf of

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Oman with Arabian-Persian Gulf. Besides two larger branches, there are also the Gulf of Khambahat and Gulf of Kutch on the Indian side. The overall surface area of the Arabian Sea is 386200 km2 with a maximum depth 4652 m (Fig. 1.2).

The climate of the Arabian Sea region is strongly affected by tropical cyclones, winter weather disturbances (cyclonic, anti-cyclonic, and meridional) in the Mediterranean Sea and the seasonal migration of the Inter Tropical Convergence Zone (ITCZ) (Snead, 1968; Sheppard, Price, and Roberts, 1992; Djamali et al., 2010; Rojas et al., 2013). The ITCZ appears each year on the south of the equator during fully developed winter monsoon (during January). The wind blows from the northeast during this period. During summer, the ITCZ migrates northwards, resulting in strong south westerly winds. This summer monsoon blows warm surface water offshore due to Ekman effect thus leads to an upwelling of deep, cold and nutrient rich water. The upwelling effects during summer monsoon are prominent along the coasts of Yemen and Oman and are greater in areas that have narrow continental shelf. The upwelled water is colder and more nutrient rich than typical for tropical seas and the areas within the Arabian Sea where upwelling is highest are subject to high pseudo latitude effect (Sheppard, Price, and Roberts, 1992). The phytoplankton blooms also occurring during winter monsoon through convective mixing resulting from cold and dry atmospheric conditions thus making the Arabian Sea productive throughout the year (Wiggert et al., 2000; Mara and Barber, 2005).

Pakistan covers a considerable portion of the Arabian Sea on its northern side with a coastline about 1050 km. The coast is shared between Balochistan (800 km) and Sindh (250 km) provinces with different features (Ali and Memon, 1995; Saifullah, 1999). Mud flats, sandy beaches and creeks are the main features of the Sindh coast with a broader continental shelf (Haq, Moazzam, and Rizvi, 1978; Saifullah, 1999). The 800 km long Balochistan or Makran coast (a part of Makran Subduction Zone (MSZ) extends from NW of Karachi in the east to Gwatar Bay (Iranian border) in the west with a narrow tectonically active continental shelf (Haq, 1988; Ali and Memon, 1995; McCall, 1997). The tectonic and stratigraphic history of MSZ has been described by Harms, Cappel, and Frances, (1984), and can be summarised as follows relevant to this study. As a result of jostling between the continental plates, complex geotectonic changes are divided into three significant stages: the middle Miocene, the late Miocene to middle Pliocene, and the middle Pleistocene to Recent. During the middle Miocene, the deposition of

5 turbidites dominated. The late Miocene to middle Pleistocene was dominated by progradation of the plains, shelf, slope and landward margin, as well as regional uplifting and folding. The middle Pleistocene to Recent phase was largely characterised by further uplift and faulting. The palaeoclimatic and geological changes that occurred during sea level lowering stage on regional and global levels have shaped the Balochistan coast of Pakistan (Lambeck, 1996; Banerjee, 2000; Prins and Postma, 2000; Kusky, Robinson, and El- Baz, 2005; Mossadegh et al., 2013; Pain and Abdelfattah, 2015). Sedimentation is a continuous process along the Makran coast and is a feature of dynamic plate margins (Prins and Postma, 2000; Prins, Postma, and Weltje, 2000; Schluter et al., 2002; Grando and McClay, 2007; Mouchot et al., 2010; Haghipour et al., 2012). The sedimentation rate in the Arabian Sea (northern Arabian Sea) was 1.2 mm/yr for the last 5000 years (Prins and Postma, 2000).

The climate of coastal areas of Pakistan is semi-arid ranging mainly from dry to hyper dry conditions with less than 254 mm annual rain fall (Salma, Rehman, and Shah, 2012). Historically, great variations in monsoon patterns, temperature, productivity, turbidity, sedimentation rates and upwelling have been noted for the Arabian Sea. Overall, the monsoon was characterised by large temporal scale changeability. The south-west monsoon was stronger during Interglacial and weakest during the last Glacial Maximum (Tiwari, Singh, and Ramesh, 2011). During the glacial periods Marine Isotope Stage (MIS) 3 (60500–50500 yr B.P) and (MIS) 8 (299 ka BP), sea surface temperatures were lower than during interglacial periods (Imbrie et al., 1984; ten Haven and Kroon, 1991; Shane and Sandiford, 2003). Productivity and turbidity in the Arabian Sea were high during (MIS) 13 (∼ 500 000 yr B.P) and possibly associated with the beginning of a harsh meridional overturning circulation in the Atlantic Ocean at the end of the middle Pleistocene (Gupta, 1999; Prins, Postma, and Weltje, 2000; Ziegler et al., 2010; Ziegler, Tuenter, and Lourens, 2010).

With respect to coral growth and development, the Arabian Sea shores are inappropriate habitat. The stressful conditions (large temperature fluctuations, nutrient rich water) produced as a result of upwelling fuel macroalgal growth which restricts coral growth. In some areas there is lack of hard substrate for coral settlement and high turbidity conditions at some localities (Gulf areas) (Sheppard and Sheppard, 1991; Coles, 2003) also limit the distribution of corals. Depending on stressful physical conditions, coral

6 communities range from true reefs with a characteristic reef topography to coral framework with high coral cover but no reef topography (Sheppard and Salm, 1988).

As noted above, the Pakistan coast is subjected to repeated reversal of monsoons (Kazmi and Kazmi, 1998) without conventional upwelling, but up sloping of the topography of the ocean floor brings up nutrient rich water (Wiggert et al., 2000; Mara and Barber, 2005). During summer monsoon, strong winds leads to high turbidity (Kazmi and Kazmi, 1998). Due to the warm climate and nutrient loading through convective mixing, the coast of Pakistan has a rich algal diversity and biomass (Shameel and Tanaka, 1992). Nutrient and metal pollution level increased along both coasts during 20th century due to rapid urbanization and industrial revolution. Today, the industrial wastes from many industries including textile, chemical, weaving, plastic, and paper industries as well as domestic sewage are directly discharged to sea through small rivers (for example, Layari and Malir Rivers) is a major cause affecting marine life (Rizwi, Saleem, and Baquer, 1988; Munshi et al., 2004; Qari, Siddiqui, and Qureshi, 2005; Shahzad et al., 2009; Hunter, Khan, and Shieh, 2012; Saleem et al., 2013). About 450,000 gallons of industrial and domestic sewage is discharged along the Karachi coast on daily basis through Lyari and Malir river sytems. Heavy metals, such as, Pb (930 to 1230 mg/ kg), Cd (987 to 1240 mg/ kg), Zn (1260 to 1410 mg/kg), Hg (118 to 242 mg/kg) and Cr (428 to 706 mg/kg) are reported with high concentrations from the sediments along Karachi coast (Nergis et al., 2012). Similarly, high concentrations of nutrients (NO3, 1-8 µM; NH4, 2-15 µM; SiO4, 3-20 µM; PO4, 0.2-2 µM) are reported from creek areas along the Sindh coast. The nutrient rich water than transformed in coastal environment through tidal currents (Harrison et al., 1997).

Literature indicates an information gap on existence of both fossil and live corals in submerged habitats along the Pakistan coast and in uplifted strata along the coast. Only few reports (e.g. Kazmi and Kazmi, 1998; Ishaq, Amjad, and Chaudhri, 2003; Wilkinson, 2004) on the presence of live corals are available and no details were provided. Similarly, Crame (1984) and Ali and Memon, (1995), reported the presence of Neogene and Quaternary corals and molluscs entrenched in different lithostratigraphic units, but taxonomic details were not provided. Siddiqui et al., (2011), reported 14 fossil corals from Ras Gunz near Jiwani, Balochistan. However, 29 hard corals, 1 black and 8 soft corals from coastal waters of Pakistan have been reported earlier by Ali et al. (2014).

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No significant studies were conducted to check the physico-chemical effects on marine organisms in the coastal waters of Pakistan, however various publications are available on various type of pollution i.e. chemical and heavy metal concentration in different marine organisms and in coastal sediment (e.g. Rizwi, Saleem, and Baquer, 1988; Munshi et al., 2004; Qari, Siddiqui, and Qureshi, 2005; Shahzad et al., 2009; Hunter, Khan, and Shieh, 2012; Chaudhary et al.,2012; Chaudhary et al., 2013; Saleem et al., 2013; Saher and Siddiqui, 2016; Khan, Ayub, and Siddiqui, 2015). Best Information on coral communities located close to Pakistan is available from Oman, Gulf of Kutch, India and Socotra Archipelago (Yemen). In Oman the coral fauna comprises 91 species in 47 genera and is more diverse. The coral growth is mainly limited by upwelling and lack of hard substrate. The reef formation mostly occurs in restricted embayments or leeward sides of the Islands, mainly due to less wave action (Sheppard and Salm, 1988; Salm, 1993; Coles, 2001). Best coral growth occurs around Daymaniyat Islands and decreases towards south (Dhofar area). The dominant reef builders along the coast of Oman include Pocillopora, Acropora and Porites (Sheppard and Salm, 1988; Coles, 2001). Regarding Gulf of Kutch, shallow patch reef host only 37 species, growing on a sandy sandstone platform that surrounds 34 Islands. The poor coral fauna is mainly due to high turbidity, sedimentation and temperature and salinity fluctuations (Pillai, 1972; Pillai, Rajagopalan and Vargehees, 1980). The corals in Socotra Archipelago (Yemen) consisting of small communities growing on non-reefal substrate. Instead of deficiency of reef builder, the Archipelago favours a diverse coral fauna (253 species in 58 genera and 16 families) (DeVantier et al., 2004).

The general lack of data on corals and the associated communities in submerged habitats along Pakistan coast has led to the current research. The specific objectives of the research were: 1. To record the distribution and diversity of corals and their associated communities in the coastal waters of Sindh 2. To record the fossil coral fauna from uplifted strata along the Balochistan coast of Pakistan and compare them with modern corals 3. To analyse the physico-chemical parameters of sea water and calcareous animals from the sampling sites

8

Figure 1. 1. World distribution of corals (Courtesy NOAA)

.

Figure 1. 2. Map of the Arabian Sea with adjacent gulfs and seas.

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1.2. Materials and Methods 1.2.1. Study sites The study was conducted at 4 localities (Hawks Bay (HB), French Beach (FB), Mubarak Village (MV) and Churna Island (CI) (Fig. 1.3) along the Sindh coast of Pakistan. The sites were selected on the basis of habitat complexity and wave exposure. For fossil corals, the study sites for the present work are located in the Gwadar and Jiwani Formations along the Balochistan coast of Pakistan (Fig. 1.4). On the basis of preliminary surveys four sites were selected, one in the Gwadar headland and three in the Jiwani, located tens of meter above mean sea level.

1.2.2. Methods 1.2.2.1. Field techniques for coral, invertebrate and fish communities SCUBA diving was conducted at 9 diving sites, 2 at HB, 1 at FB, 2 at MV and 4 at CI during January- March 2013, 2014. Coral and invertebrate communities were recorded using DACFOR scale (Table 1.1). Pieces of hard corals and samples of invertebrates (molluscs, echinoderms) were collected for the purpose of identification, while crustaceans (crabs), sponges, and zoanthids were not sampled but relayed on in situ photographs for identification. The samples were collected using hammer and chisel. Percentage cover was determined visually to the nearest percent. Fishes were identified from photographs taken in situ. Fishes were further classified on the basis of trophic level using the website (www.fishbase.org). Underwater images were taken using a digital camera (Fujifilm Fine Pix F550 EXR) in an underwater housing.

The samples were brought to the laboratory. Hard corals were washed with fresh water. Molluscs and sea-urchins (Echinometra mathaei, Diadema setosum) were preserved in field using 5% formalin in plastic bottles while Holothuria sp. was preserved in 70% alcohol to avoid termination of calcareous ossicle. The samples were stored at the Centre of Excellence in Marine Biology, University of Karachi, for future record. Identification of species was made using the online website (www.coralsoftheworld.org), Riegl et al. (2012) and available literature for hard corals, Kuiter and Debelius (2007) and online website (www.fishbase.org) for fish communities, Dance (1974) and Bosch et al. (1995)

10 for molluscs, Mustaqeem and Rabbani (1976) for crabs, Coleman (1991) and England (1987) for zoanthids and Hooper (2003) for sponges.

1.2.2.2. Field techniques for macroalgal communities Underwater surveys were conducted by the first author at 5 dive sites (2 at HB and one each at FB, MV and at the northern sheltered side of CI) from January to March 2014. Sites were again revisited in February 2015 to observe the effects of cyclone ‘‘NILOFAR’’, which occurred in the Arabian Sea during the end of October 2014, on community structure. The samples were collected by SCUBA diving. Relative abundance was determined quantitatively using a 1 m2 quadrat, made up of PVC pipes. To avoid floating, the quadrat was suitably weighted with iron rods. As a whole, 45 quadrats were deployed randomly (10 each at HB sites 1, 2, FB, MV and 5 at CI). Species within the quadrats were uprooted with the help of a scalper, chisels and hammer, stored in plastic bags and then counted in the field. Still photographs were also taken for species identification. In situ images were taken using a digital camera (Fujifilm Fine Pix F550 EXR) in an underwater housing. Percentage cover was estimated visually. The samples were brought to the laboratory, pressed on herbarium sheets, also preserved in 4% formalin and archived at Centre of Excellence in Marine Biology, University of Karachi for future record. Identification was made using the herbaria at the Center of Excellence in Marine Biology, Karachi University and available literature (e.g. Shaikh and Shameel, 1995; Aliya and Shameel, 1996; Carpenter and Niem, 1998). At each site habitat features, depth, GPS position and general observations on coral, macroalgal, fish and invertebrate communities were noted (Table 1.2).

1.2.2.3. Field techniques for fossil coral communities The sampling surveys were undertaken during September 2012 and October 2013. Position and general observations for each site were recorded (Table 1.3). Location and height above sea level was determined using a Garmin Etrex 10 GPS. At three sites in the Jiwani Formation, samples were collected using line intercept method (Loya, 1972), a more effective method for reef slopes than quadrat method and is less time consuming (Ohlhorst et al., 1988; Beenaerts and Berghe, 2005). Transects (50m each) were laid considering the nature of the sites (e.g. topography, width, coral cover). One transact at Jiwani site 1 (J1); five transects at Jiwani site 2 (J2; large area about 1 km2) and two

11 transects at Jiwani site 3 (J3) were laid. Transects at J2 were at least 100 m apart and at J3 they were separated by 10 m. Gwadar headland (GH) was ecologically disturbed and corals were counted and not recorded systematically. Each species was assigned a rank number (1-5) depending on its abundance: 6 = >50 individuals, 5= >40 individuals, 4= 25-40 individuals, 3= 16-24 individuals, 2= 8-15 individuals and 1= 1-7 individuals.

For detailed examination of identifiable taxonomic features small samples were collected using hammer and chisel and carefully washed. The overall and magnified images were made of individual samples with the help of Canon Power Shot A1100IS digital camera for the identification of coral species following Veron (2000) and Bromfield (2013). Specimens are stored at the Centre of Excellence in Marine Biology, University of Karachi for future reference. Skeletons of same taxa from fossil corals (this study) and modern corals (collected during this study and earlier; Ali et al., 2014) were compared to assess the effects of sediment stress and primary productivity following the methods described earlier by Klein, Mokady, and Loya, (1991) and Edinger and Risk, (1994).

1.2.2.4. Sea water physico-chemical parameters Seawater physico-chemical parameters were recorded. Physical parameters (temperature, pH, dissolved oxygen) and organic content () for each location were recorded once in triplicate from surface (about 16 cm) and bottom using Eureka Manta 2 Multiprobe Water Quality Recorder by inserting sensors directly on surface and bottom water. Before data recording, sensors were calibrated according to the instructions given by the manufacturer. Water samples at each location from the surface and bottom were collected once in triplicate for nutrient analysis such as nitrate, nitrite, phosphate and ammonia using glass bottles covered with lids. Samples were fixed in chloroform to stop microbial activity. The samples were brought to the laboratory in an ice box and analyzed following the method of Strickland and Parsons (1972).

- 2- - Concentrations of HCO3 , CO3 and HO were determined following the ASTM (American Society for Testing and Materials) standard test method D 3875 – 08. CP-401 (2003). pH meter from Elmetron (Poland) was used for titrimetric analysis. 2+ 2+ Standardization of acid was done using Na2CO3. Total hardness (Ca , Mg ) of seawater was determined using standard method AWWA/APHA 3500-Ca B (2005).

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1.2.2.5. Elemental analysis of coral skeletons To determine the calcium carbonate concentrations and environmental conditions of the water, percentage weight concentrations of different elements in coral skeletons collected from different locations along the Sindh coast of Pakistan were determined. For elemental analysis, coral skeletons were sent to centralized laboratories, Karachi University. The metal concentrations were analyzed using EDX (energy dispersive X-ray analysis) techniques. Before sending samples to centralized laboratories, slabs were made by cutting the samples vertically using a low speed electric cutter. For SEM images, the surface areas of vertical sections were further layered with 300O gold. EDX method basically involves the production of a high spectrum of charged particles (electrons, protons) or X-rays to a sample under investigation. The high spectrum of charged particle accelerates the resting electron within the sample and removes it from shells. As a result, a hole is created. This gap is filled by an electron from high energy spectrum. The difference between high and low energy shell is released in the form of X- rays. The energy and number of X-rays released from the sample being under investigation then measured by an energy dispersive spectrometer.

1.2.3. Statistical analysis

The relationship between sites for coral (modern, fossil), fish and macroalgal communities was investigated using cluster analysis on the basis of presence/ absence, square root transformation data and zero-adjusted Bray–Curtis similarity index (Bray and Curtis, 1957). Bray–Curtis index have advantages over other indexes because in case of identical samples, considers a value of 100 whereas in case of dissimilar samples, considers a value of zero. Moreever, addition or removel of species does not effect on values. The dendrograms was constructed using the group average linkage technique (Clarke, 1993; Clarke and Warwick, 2001). Species frequency distributions were observed using K. dominance curves following Lambshead, Platt, and Shaw, (1983). To map any decline or change in coral communities from the Quaternary to the present in Pakistan, a comparison was made using the Quaternary coral data from current study and Siddiqui et al., (2011), and data on modern corals distribution in Pakistan from this study and Ali et al., (2014). Further cluster analysis was conducted to compare the species and genera composition of Quaternary (current study and Siddiqui et al., 2011) and modern corals collected during recent surveys (21 species) and Ali et al., (2014) from Pakistan

13 and Miocene corals reported from southern Iran (McCall, Rosen, and Darrell, 1984). Analyses were done using PRIMER v6 software package (Clarke and Gorely, 2006).

Figure 1.3. Map of Pakistan coast line with inset showing the study sites for coral, seaweed, fish and invertebrate communities.

Figure 1.4. Map showing Makran subduction zone (MSZ) in the coastal region of Pakistan and Iran and other structural features in northern Arabian Sea. Inset showing study sites at Gawadar and Jiwani, Blaochistan coast for fossil corals.

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Table 1.1. Abundance ranking for coral and invertebrate communities.

Ranking Abundance D (6) Dominant, up to 300 specimens A (5) Abundant, up to 200 specimens C (4) Common, up to 100 specimens F (3) Frequent, up to 30 specimens O (2) Occasional, up to 10 specimens R (1) Rare, up to 5

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Table 1.2 General observations recorded at each site with GPS coordinates and respective depths. CI-C4: Churna Island dive sites 1-4; MV 1-2: Mubarak Village dive sites 1-2; FB: French Beach; HB 1–2: Hawks Bay dive sites 1–2.

Site name Depth (m) Geographical General observations position CI 1 7 24° 54'.053'’ N, The habitat was rocky with uplifted rocks and 66° 36'.436'’ E boulders. The coral communaty was diverse. Hard coral cover was about 60%. Porites cf.annae, Porites cf.columnaris, Porites cf. densa were dominating the site, whereas Cyphastrea serailia, Porites lobata and Goniopora sp.2 were rarely distributed CI 2 7 24° 53'.982'’ N, Habitat was found similar to previous site. The 66° 36'.464'’ E cover of the stony corals was about 80%. The dominat species were Porites cf. columnaris and Porites cf. densa. Porites cf.annae, Porites harrisoni*, Cyphastrea serailia, Goniopora sp.2, Porites lobata, Porites sp. Favites pentagona*, Plesiastrea versipora*, Leptastrea transversa and Psammocora sp.1 had a frequent to rare distribution. CI 3 7 24° 53'.939'’ N, Similar habitat and coral cover was observed at 66° 36'.486'’ E this site as in site 2. Porites cf. columnaris, Porites cf. densa and Porites cf. annae recorded as abundant species while, Porites lobata, Psammocora sp.1, Psammocora cf. superficialis*, Porites sp., Gonastrea sp. 2, Pseudosiderastrea tayami, Psammocora sp. 2, Favites spinosa* were rarely distributed. Macroalgal diversity was quite low with up to 5 % cover. CI 4 8 24° 53'.878'’ N, Habitat was similar to previous sites. Hard coral 66° 36'.547'’ E cover was about 40 %. Porites cf. densa was recorded as abundant species. Porites cf. annae, Porites cf. columnaris, Porites lobata, Gonastrea sp.3, Gonastrea sp.1, Cyphastrea serailia, Favites Pentagona* and Psammocora cf. superficialis* had common to rare distribution. ? Dendostrea sp. was abundant here embedded in vertical rocks. Fish diversity at all 4 sites of the Island was higher than any other site while patches of Pinna species were observed in sandy habitat at marginal environment. Over all, fishes were abundant at 4 sites of CI compare to any other site. The commonest species including Neopomacentrus sindensis, Neopomacentrus cyanomos, Neopomacentrus bankieri, Abudefduf vaigiensis and Sphyraena obtusata. Overall the community was dominated by damselfishes.

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MV1 2-6 24° 51'.625'’ N, The habitat was rocky with shoals. Hard coral 66° 39'.780'’ E cover was about 20 %. Porites cf. densa, Porites lobata, Goniopora sp.2 were recorded. Macroalgae (coralline algae dominating) was dominant with about 60 % cover. The dominant species were Ceramium sp., Galaxaura sp., Lobophora variegata and Padina pavonica. Fishes were moderately abundant and the community was dominated by Neopomacentrus sindensis, Pristiapogon fraenatus, Pempheris malabarica and Pomacentrus caeruleus Invertebrate fauna mostly consisted of Echinometra mathaei, Diadema setosum, zoanthids ((Palythoa sp.) and rarely distributed molluscs (Turbo bruneus, Erosaria turdus, Purpura bufo and Cantharus sp.). MV2 3 24° 51'.602'’ N, The habitat was rocky. Hard coral cover was 66° 39'.751'’E about 5 %. Goniopora sp.1, Porites decasepta and Porites lobata were rarely distributed. Corals degradation was observed at both sites of Mubarak Village. Fish and Invertebrate fauna was almost similar to MVI. Algal diversity was also quite low. Fish diversity was low and the community was dominated by Neopomacentrus sindensis followed by Neopomacentrus bankieri and Abudefduf vaigiensis. FB 10 24° 50'.171'’ N, The habitat was rocky with uplifted rocks, ledges 66° 49'.034'’E and gullies. Macroalgal cover was about 80 %. Few patches of Goniopora columna*, Goniopora sp.3 Coscinaraea columna and Goniastrea sp.4 were noted. Percentage cover of Soft corals (sea fans) was high than hard corals. Overall percentage cover was about 5 %. A water current with high intensity was observed during post- cyclonic observations. Algal cover was about 83 %. The dominant species were Codium fragile, Sargassum lanceolatum, Caulerpa chemnitzia, Caulerpa taxifolia, and Sargassum swartzii. The invertebrate fauna mostly consisted of molluscs (Perna viridis) and zoanthids (Palythoa species). Fish diversity was low and only 8 species were recorded at this site. The dominant species were Neopomacentrus sindensis followed by Heniochus acuminatus, Heniochus diphreutes and Neopomacentrus bankieri.

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HB1 4 24° 51'.113'’ N, The site was located 400 m offshore, formed of 66° 49'.955'’ E uniformly distributed habitat, mostly consisting of rocky bed with sandy patches. The intertidal area was quite large. No coral species were recorded here. Overall, the area was dominated by Sargassum species during both pre and post- cyclonic observations. The currents were found higher during post-cyclonic observations than pre-cyclonic observations. Algal cover was up to 80%. The dominant genus was Sargassum with up to 70 % cover. HB2 6 24°51'.167’' N, The site was located 500 m offshore. Habitat was 66° 50'.734'’E similar to HB 1. Few colonies of Favites vasta was recorded here growing over hangs. Vertebrate fauna was very poor. Again Sargassum species dominated the area during both pre- and post-cyclonic observations. Fish diversity was very low and only two species (Neopomacentrus bankieri, Neopomacentrus sindensis) were recorded. Invertebrate fauna was very poor. Over all changes in algal communities were observed at all sites before and after cyclone “NILOFAR” except at CI.

Note. The species shown with * i.e. Porites harrisoni* means already shown in Ali et al., (2014) and are not included in this list.

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Table 1.3. General observations recorded at each site with GPS coordinates and elevations from sea level.

Site name Geographical position with General observations elevation from sea level

Gwadar headland 250 06. 017” N, 620 19. 937” E The habitat near the site was mostly (GH) Elevation: 90 m rocky, composed of sandstone. The site was ecologically disturbed. Eighteen corals were recorded at this site. The dominant genera were Favia and Favites species. Jiwani 1(J1) 25o 02. 714” N, 61o 43. 954” E The habitat was mostly rocky, Elevation: 2 -4 m consisting of sandstone and pebble beds. The coral cover was about 25%. Only two species (Favites complanata and Favites spinosa) were dominant, the majority of colonies scattered freely in coarse sand while few were tightly packed. Jiwani 2 (J2) 25o 04. 079” N, 61o 47 .443”E The coral colonies were scattered in Elevation: 67 m large patches on about more than 1km2 area. The habitat was mostly rocky, composed of sand stones with fine and coarse sand, boulders and mudstone. Thirty coral species were recorded at this site. Many species were found scattered but a considerable proportion was tightly packed. Coral cover was about 33 %. Prominent genera were Favia (11 %), Favites (4 %). Jiwani 3 (J3) 25o 06. 611” N, 61o 48. 528” E to This site was steeply sloped. The 25o 06.635” N, 061 o 48.504” E; habitat mostly comprised of Elevation: 4 -26 m sandstone with fine sand, shale, limestone and boulders. Majority of corals were loosely packed. Thirty one coral species were recorded at this site. The coral cover was about 19 %. The dominant genera were Favia (5 %), Astreopora (3%), Favites (2 %), and Blastomussa (2 %).

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Chapter 2

Physico-chemical Conditions

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2.1. Abstract

Healthy environment of the seawater play a basic role for the proper growth of corals and other marine communities. The present study recorded the physico-chemical parameters of seawater from 4 sampling locations along the Sindh coast. The details about sampling and analyzing techniques are included in chapter 1 (section 1.2). Physical parameters were found fluctuating; similarly concentrations of organic (chlorophyll) and inorganic nutrients (nitrate, nitrite, phosphate and ammonia) were also found fluctuating. High values of organic and inorganic nutrients were recorded at locations located close to shoreline (HB, FB, MV) while less concentrations were recorded in offshore waters (CI). Concentrations of bicarbonate ions were found high in water samples compare to carbonate ions. High Mg2+ values were noted in seawater samples compare to coral skeletons. Variations in physical parameters appeared to link with sampling time, water depth and prevailing climatic conditions while high concentrations of inorganic nutrients in coastal areas may be linked with upsloping and mainly due to discharge of domestic seawage in these areas through different river systems. Although no significant ocean acidification impacts were noted but nevertheless increasing.

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2.2. Introduction

Optimal ranges of seawater physico-chemical parameters such as temperature, pH, salinity, sedimentation, nutrients and calcium carbonate saturation rates are necessary for suitable growth of marine communities (e.g. corals, seaweeds). Any change in physico- chemical conditions of seawater can effect on the physiological processes of marine communities (Coles and Jokiel, 1978; Luning and Neushul, 1978; Anthony and Connolly, 2004; Steen, 2004, Middelboe & Hansen, 2007; Kuffner et al., 2008; Diaz- Pulido et al., 2012; Juneja et al., 2013). Among the seawater physico-chemical parameters, temperature is an important factor, effects on growth rate, biochemical composition, cell size, nutrient requirements (Renaud et al., 2002, Harley et al., 2012) and alters other physical parameters such as salinity and pH ((Liu et al., 2012, Marinho- Soriano 2012).

Among marine communities, corals are highly sensitive and are susceptible to climate change (Glynn, 1993). Their growth and structure is affected by a number of physico- chemical and biotic factors (Ammar and Mahmoud, 2006; Wood, 1983). Temperature is a major factor affecting growth and distribution of corals. Major cause of coral reefs degradation across the world is subjected to increase in ocean temperatures (Wellington and Dunbar, 1995; Selig, Casey and Bruno, 2012). The best temperature for coral growth is 25 to 28°C (Precht, and Aronson, 2004). Temperatures, below about to16°C to 18°C halt coral growth. A temperature more than 30°C to 32°C induces coral bleaching and subsequent mortality (Gosliner, Behrens, and Willians, 1996). Similarly, an increase or decrease in salinity reduces corals growth and causes coral bleaching (Glynn, 1993). A salinity range of 34 to36 ‰ is considered to be best for the growth of coral (Vine, 1986). Moreover, inorganic nutrients also effects on coral growth. Other factors such as high concentration of ammonium and low concentration of phosphorus reduce coral growth (Ferrier-Pages et al., 2000). Reefs generally prefer to grow in waters with low concentration of inorganic nutrients (Furnas, 1991). Hydrogen ions concentration (pH) is another important factor for proper reef development. Burning of fossil fuel is a main source of atmospheric carbon dioxide, decreases in pH of the ocean and alter the carbonate chemistry of seawater. The major impact is the depressing of calcium carbonate permeation state (Doney et al., 2009).

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Along the northern part of the Arabian Sea, fluctuating physico-chemical parameters of seawater are reported. Sea surface water temperatures vacillated between 22.5 to 28.5 °C with a gradual increase from north to south. High fluctuations in temperatures are recorded during south west monsoon. Salinity vacillated between 35.4 to 36. 6 ‰. High salinity is reported in south side compare to northern part. Dissolved oxygen concentrations mostly ranged between 4.2 to 5.2 ml/ l-2. Also an increase in oxygen concentration was noted from north to south. Surface water phosphate concentrations ranged from 0.5 to 1.75 µg l-1. Highest values were recorded at deeper depths (central part) with a gradual increase in northern and south western parts. Surface water nitrate- nitrogen concentrations ranged from 0.01 to 25.50 µg l-1 and remained high during south west monsoon. High chlorophyll concentration was reported in euphotic zone. Also a a high primary production rate is reported in the Arabian Sea. About 530x106 tons of carbon produced each year and 25% of the photosynthetic production occurs in 8% area of the northern part (Qasim, 1982).

Physical factors described from Karachi waters were quite variable. The salinity ranged between 34.30 ‰ and 39.48 ‰. Oxygen levels ranged between 3.00 and 6.55 ml-1. The semi-diurnal tides range up to 3.5 m (Haq et al., 1978; Saifullah, 1999; Sultana and Mustaquim, 2003). Although a number of studies have conducted on physico-chemal parameters (e.g. Qari and Siddiqui, 2005; Munir et al., 2013; Naz et al., 2014; Khokhar et al., 2016; Munir et al., 2016;; Shoaib et al., 2017) along the Sindh coast of Pakistan, but none was undertaken with reference to the effects of these parameters on corals from the coastal waters of Pakistan. The present study was undertaken to ascertain the environmental conditions and its impact on corals through the analysis of physico- chemical parameters of seawater and elemental composition of coral skeletons from submerged habitats along the Sindh coast of Pakistan.

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2.3. Materials and Methods The details about study sites and methods are included in chapter 1 (section 1.2).

2.4. Results 2.4.1. Seawater physico-organic parameters Variations in physical parameters were recorded. Low surface water temperature (21.950 °C) was noted at HB during February and high (25.813 ◦C) at MV during March. High surface pH (8.623) value was noted at FB and low at CI (8.570). Low surface dissolved oxygen (% saturation) value was noted at HB (58.600% saturation) and high at MV (94.667% saturation). High surface chlorophyll value was noted at HB (1.253 μg/L) during February and low at CI (0.810 μg/L) during March. Mean values of each parameter recorded from surface and bottom with sampling dates are shown in (Fig. 2.1).

2.4.2. Dissolved inorganic nutrients Like physical parameters, variations in nutrient concentrations were recorded at sites during different time periods. High surface nitrate concentration was recorded at FB (2.657 μM/L) and low at MV (0.743 μM/L). High surface phosphate concentration was noted at HB (0.203 μM/L) and low at FB (0.135 μM/L). Mean concentrations of nutrient recorded from surface and bottom waters with sampling dates are displayed in (Fig. 2.2).

2.4.3. HCO3- , CO32- and HO- concentrations

Low surface and bottom mean bicarbonate values (106.46, 96.78 mg/L) were noted at MV while high surface and bottom bicarbonate values (166.47, 160.66 mg/L) were noted at CI. Low surface and bottom mean carbonate values (7.61, 5.71 mg/L) were noted at FB while high surface and bottom carbonate values (11.42, 19.04 mg/L) were noted at MV. Mean values of each parameter with sampling dates recorded from surface and bottom are shown in Fig. 2.3. High Mg2+ concentration were noted in water samples. Overall total water hardness was found high in bottom waters than surface waters. Calcium and Magnesium has been analyzed following AWWA/APHA 3500-Ca B (2005), therefore the values of hardness are mentioned as total hardness specially in case of seawater is expected to originate from the total count of Ca2+ and Mg2+ (Fig. 2.4).

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2.4.4. Elemental composition of coral skeletons The EDS spectra of coral skeletons are shown in Fig. 2.5. Calcium, Carbon and Oxygen were found as major elements in almost all the samples. The percentage weight concentration of each element in coral skeletons, calculated quantitatively from beam or spectra are displayed in Table 2.1.

Table 2.1. Percentage weight concentrations of different elements in coral skeletons collected from different locations along the Sindh coast of Pakistan. Abbreviations used as MV: Mubarak Village; CI: Churna Island; HB: Hawks Bay; FB: French Beach.

Species name Location Ca Mg O C Sr Na Al Si S Cl K Fe

Porites sp. 1 MV 38.83 - 51.16 10.01 ------Porites sp. 2 CI 25.43 0.74 62.87 6.27 1.2 0.37 1.3 0.9 1 - - C. serailia CI 21.13 - 62.43 15.17 1 0.7 ------P.columnaris CI 34.79 - 55.32 9.88 ------F. vasta HB 46.68 - 45.21 6.95 - - 0.69 0.5 - - - - F.pentagona CI 24.01 0.78 52.87 10.72 - - 3.16 6.2 - - 0.8 1.39 Goniopora FB 20.81 1.18 46.54 3.71 - - 7.32 14 - - 2.6 3.95 sp.

25

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0 SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW HB FB MV CI HB FB MV CI HB FB MV CI HB FB MV CI Temperature (⁰C) pH Dissolved Oxygen (% saturation) Chlorophyll ((μg/L)

Figure 2.1. Mean (n = 3) seawater physical and organic parameters recorded once from surface and bottom at 4 locations along the Sindh coast, Pakistan. HB: Hawks Bay; FB: French Beach; MV: Mubarak Village; CI: Churna Island; SW: Surface water; BW: Bottom water

26

3

2.5

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1.5

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0.5

0 SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW HB FB MV CI HB FB MV CI HB FB MV CI HB FB MV CI Nitrate (µm/L) NitrIte (µm/L) Phosphate (µm/L) Ammonia (µm/L)

Figure 2.2. Mean (n = 3) dissolved nutrient concentrations recorded once from surface and bottom at 4 locations along the Sindh coast, Pakistan. Abbreviations are same as in Figure 2.1.

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0 SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW HB FB MV CI HB FB MV CI HB FB MV CI HB FB MV CI HB FB MV CI HCO3- (mg/L) CO32- (mg/L) HO- (mg/L) Initial Temperature (°C) Initial Ph

Figure 2.3. HCO3- (mg/L), CO32- (mg/L) and HO- (mg/L) concentrations of seawater recorded once during sampling period with initial temperature(°C) and pH recorded at the time of analysis. Abbreviations are same as in Figure. 2.1.

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0 SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW SW BW HB FB MV CI HB FB MV CI HB FB MV CI HB FB MV CI Ca2+ (mg/L) Mg2+ (mg/L) T. Hardness (mg/L) T. Hardness (% difference)

Figure 2.4. Total hardness of (n=3) of seawater samples recorded once during sampling period. The abbreviations used are same as in Figure 2.1.

29

Figure 2.5. Elemental concentrations of EDS spectrum of coral skeletons collected from different locations along the Sindh coast of Pakistan. A: Porites sp.1; B: Porites sp.2; C: C. serailia; D: P.columnaris; E: F. vasta; F: F.pentagona; G: Goniopora sp.

30

2.5. Conclusions The following may be deduced from the research reported in this chapter: 1. Water temperature in the area remains with the close proximity of upper and lower limits of optimum temperature conditions for coral growth (25-28°C). Higher temperature during summer is a limiting factor. 2. Concentration of inorganic nutrients (nitrate, nitrite, phosphates) is high in the coastal waters supporting high primary productivity (suspended load) which will have a negative impact on corals. 3. High bicarbonate concentration (HCO3) in seawater indicates acidic nature of water which is implicated with the calcification rates. 4. Although calcium and magnesium are present in water in sufficient quantities, the low magnesium in coral skeleton reflects stressed growth.

31

Chapter 3

Reef and Associated Fauna in the Coastal Waters of Sindh, Pakistan and an Assessment of Environmental Impacts

32

3.1. Abstract

Reef system across the globe is facing serious natural and manmade threats and impacts, affecting their ecosystem services and natural capital. The current study recorded the hard corals and their related populations in the littoral waters of Sindh, Pakistan and an assessment of environmental impacts. In present study, 21 species of hard corals, 54 fish and 24 invertebrate species (13 molluscs, 3 sponges, 3 sea anemones, 3 echinoderms and 2 crustaceans) were recorded. Samples were collected by SCUBA diving. Relative abundance of corals and invertebrate communities were recorded semi quantitatively using DACFOR scale while fishes were not recorded systematically but were indentified from underwater photographs. High corals, fish and invertebrate diversity was recorded at northern sheltered sites of Churna Island and at Mubarak Village whereas high corals degredation was observed at Mubarak Village compare to Churna Island. Fish and invertebrates distribution patterns were found associated with habitat complexity. Physico-chemical parameters were found fluctuating. No significant acidification impacts were noted particularly in offshore waters (Churna Island) but nevertheless increasing. Compare to coral skeletons, high Mg2+ values were noted in sea water samples. Calicum, Carbon and Oxygen were found as major elements in coral skeletons excluding other trace elements. Due to surving in harsh environmental conditions, the coral communities of Pakistan seemed to have the features of marginal communities. To understand better the impacts of acidification and other physic-chemical parameters, further studies are recommended in terms of biological and environmental changes. Also to mitigate the climate changes, there is need to establish marine protected areas especially near coral habitats including all factors necessary to design effective marine protected areas.

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3.2. Introduction

Reef system is very beneficial to mankind. World third of marine fish species reside in reef environment (Veron et al., 2009; Plaisance et al., 2011). Reef provides 25% of the total fish, consumed by humans. Several millions of people living in at least 99 countries (having coast line with reefs) depend on corals for their food requirements (Teh et al., 2013). Reefs also protect the land from hurricanes by acting as barriers. Being a productive marine ecosystem, reefs are highly susceptible to changes occur in their environment (Glynn, 1993; Walker, 2005). The survival and growth of corals relay on a number of factors i.e. temperature, pH, salinity, nutrient concentrations, sedimentation load, water depth and turbidity and CaCo3 saturation (Coles and Jokiel, 1978; Anthony and Connolly, 2004; Walker, 2005; Marubini et al., 2008). Among these factors, temperature plays a vital role for corals growth and distribution patterns. A temperature of 30°C for a long period, starts bleaching, increases mortality rates and reduces calcification process, while at 32°C, deaths occur within few days. Lower thermal limits are more dangerous than upper limits (Jokiel and Coles, 1977). Extension and calcification rates of coral are highly linked with surface temperatures of the sea rather than the solar radiations coming inside (Edmunds, 2008).

Bleaching is the loss or whitening of zooxanthellae (photosynthetic microalgae). Bleaching occurs when coral is exposed to temperature that is above or below normal limits. High temperature also causes irradiance on large scale (Gleason and Wellington, 1993; Brown, 1997; Glynn, 1984). Levels of bleaching are variable even within and among coral colonies even in reef communities. Bleaching events at small scale may be linked with particular disturbances e.g. increase or decrease in temperature and solar irradiance, sedimentation, diseases, subaerial exposure, freshwater input and contaminants. Large scale bleaching mostly occurs at 100 to thousands of km2 area. Bleaching decreases the rate of coral growth, sediment shedding ability, reproductive activity and ability to compete with invader species and diseases. In some cases, recovery takes several years. In case of swear bleaching, the chances of recovery are diminished (Glynn, 1996; Done, 1999). It is estimated that during 1998 bleaching event, above than 16% of the tropical reefs degraded completely while 50–90% mortality occurred in some areas (Wilkinson 2002). According to Berkelmans et al., (2004), the bleaching ratio in Great Barrier Reef was around 42% during 1998 event with about 18%

34 intensely bleached whereas in 2002, the overall bleaching ratio was around 54% with 18% bleached intensely. Bleaching and max3d sea surface temperature relationship modeling indicates that a 1°C will increase occurrence of reef bleaching from 50% to 82%. A 2 °C rise in temperature will increase bleaching up to 97% awhile a 3 °C will increase to 100 100%. Incidents of corals mortality due to bleaching has been reported on global (Great Barrier Reef, Australia) and regional (Bahrain, Oman, UAE) scale (Wilkinson, 1998; Uwate and Shams, 1999; Riegl, 2002; Wilkinson 2002; Berkelmans et al., 2004; Al-Kuwari, 2006). Ocean acidification is another threat being faced by corals, other calcifiers and noncalcifying organisms. As a result of industrial revolution, the concentration of atmospheric carbon dioxide increased (Kleypas et al., 2006; Hoegh- Guldberg et al., 2007; Doney et al., 2009). The increase in carbon dioxide reduces the pH of the ocean and makes an overall shift in carbonate chemistry and changes the element and compounds of many biogeochemical cycles (Doney et al., 2009).

Sindh coast of Pakistan starts from Sir Creek near India to near Karachi and covers a distance of 250 km. The coast mainly consists of creeks, sandy beaches, mud flats with few rock habitats near Karachi (Moazzam, and Rizvi, 1978; Saifullah, 1999). Due to the discharge of industrial and domestic effluents through many small rivers (Layari, Malir and Hub Rivers), metal and nutrient pollution levels have increased along the coast (Rizwi, Saleem, and Baquer, 1988; Munshi et al., 2004; Qari, Siddiqui, and Qureshi, 2005; Shahzad et al., 2009; Hunter, Khan, and Shieh, 2012; Mashiatullah et al., 2013; Saleem et al., 2013).

Studies on corals in Pakistan are at initial stage. Up to year 2000, it was widely believed that no coral occur in Pakistan. The previous reports (e.g. Kazmi and Kazmi, 1998; Ishaq et al., 2003; Wilkinson, 2004) just mentioned the presence of corals along the coast without ecological and taxonomic details. However, Ali et al., (2014), reported 29 hard, one black and 8 soft corals from different localities along the coast. No significant studies were conducted to access the impacts of physico-chemical parameters especially on corals in the coastal waters of Pakistan, however various publications are available on various type of pollution i.e. chemical and heavy metal concentration in different marine organisms and in coastal sediments (e.g. Rizwi, Saleem, and Baquer, 1988; Munshi et al., 2004; Qari, Siddiqui, and Qureshi, 2005; Shahzad et al., 2009; Hunter, Khan, and

35

Shieh, 2012; Chaudhary et al.,2012; Chaudhary et al., 2013; Saleem et al., 2013; Saher and Siddiqui, 2016; ; Khan, Ayub and Siddiqui, 2015 ).

Lack of data regarding corals, their associated communities and environmental impacts on coral communities in submerged habitats along Pakistan coast has led to undertake the current research. The specific objectives of the research were 1) To record the distribution and diversity of corals and their associated communities (fish, invertebrates) in the coastal waters of Sind and 2) To access the impacts of Physico-chemical parameters of sea water on corals.

3.3. Material and Methods

Details about study sites and methods are included in chapter 1 (section 1.2).

3.4. Results 3.4.1. Description of survey sites Habitat features, general under water observations noted at each site along with depth and GPS positions are encompassed in Table 1.2 (section 1.2).

3.4.2. Coral communities In the current study, 21 hard corals species in 4 families and 10 genera were recorded. Comparative abundance of coral species at each dive site is set out in Fig. 3.1 (A-B) and Table 3.1. Out of 21 stony corals, 7 were identified up to species level, 10 up to genus level, 1 species could not be identified with certainty while there is doubt about 3 species. Overall, 50 hard coral species have been recorded from coastal waters of Pakistan including Ali et al., (2014) Table (3.2). Diverse corals forms and some degree of reef formation were observed at northern sheltered sites of CI especially at site 2 and 3. Porites cf. columnaris. Porites cf. annae and Porites cf densa formed large single species stands. Compare to CI at MV (comparatively sheltered), the community was dominated by the members of family Poritidae, distributed patchily. The highly exposed sites i.e. HB 2 and FB had very poor coral fauna and only few hard corals (Favites vasta, Psammocora sp. 1, Goniopora sp.3, Coscinaraea columna and Gonastrea sp.4) were observed at these sites. Out of 21 species, 2 species (Porites decasepta, Porites cf.

36 columnaris) had a restricted distribution (Arabian Sea, Red Sea and western Indian Ocean), 6 species (Porites cf densa, Favites vasta, Pseudosiderastrea tayami, Cyphastrea serailia, Coscinaraea columna, Physogyra sp.) are distributed in entire Indian and Pacific Ocean, 3 species (Porites lobata, Porites cf. annae, Leptastrea transversa) had a wide range of distribution (Indian, Atlantic and Pacific Oceans) while the distribution range of 10 species (Porites sp., Goniopora sp.1, Goniopora sp.2, Goniopora sp.3, Gonastrea sp.1, Gonastrea sp.2, Gonastrea sp.3, Gonastrea sp.4, Psammocora sp.1, Psammocora sp. 2) is not clear.

High bioerrosion due to (Cliona sp.), shift in community structure (dominance of Ceramium sp.) and corals bleaching on large scale was observed at MV compare to CI (Fig. 3.2). A cluster analysis of above mentioned communities at 8 diving sites indicated that the northern sheltered sites of CI (NSS2 and NSSI) and MV sites (MVI and MV2) formed well defined clusters at a similarity level of about 80% and 75 %. FB, HB2, and sheltered sites of CI (NSS3 and NSS4) formed distinct clusters at similarity levels 0%, 5%, 60% and 65% correspondingly. (Fig. 3.3). The K dominance curves designated that species-frequency distribution is high at NSS 3, NSS2 followed by NSS4, NSS1, MVI, MV2 and HB2 (Fig.3.4)

3.4.3. Fish communities A total of 56 fish species in 33 genera and 24 families were recorded at 9 different dive sites. Among these, 51 species were identified at species level whereas 5 up to genus level. High diversity was noted at northern sheltered sites of CI followed by MV, MV2 and FB and appeared to be correlated with habitat complexity. Fish diversity and distribution is shown in Table 3.3 and Fig. 3.5 (A-C). Neopomacentrus sindensis, Neopomacentrus bankieri, Abudefduf vaigiensis, were recorded as abundant and from maximum sites whereas Abalistes stellatus, Plectorhinchus gattuerinus, Amphiprion sandaracinos and Scorpaenopsis barbatus included as rare species recorded once. Out of 56 species 7 (Chromis flavaxilla, Pseudochromis aldabraensis, Pseudochromis omanensis, Pseudochromis springeri, Scarus arabicus, scarus zufar, Scorpaenopsis barbatus) have a confined distribution, mostly limited to Red Sea, Arabian Sea region. Two species (Diplodus capensis, Abudefduf vaigiensis) also reported from Atlantic including western Indian Ocean, whereas 47 have a wide distribution (Indian or western

37

Indian Ocean). Based on feeding level, majority of fishes were invertivorous (18 species) followed by pankrtivorous (17 species), herbivorous (10 species), carnivores (7 species), invertivorous and carnivorous (2 species) and omnivorous (2 species). A cluster analysis of fish communities at 9 diving sites showed that the northern sheltered site (NSS3 and NSS1) of CI and HB1 and HB2 formed well clusters at similarity levels of about 68% and 100 % while MV1, NSS4, NSS2, FB and MV2 formed distinct cluster at a similarity level of about 40 %, 50 %, 50 %, and 63 %, 22% and 40% respectively (Fig. 3.6). The K dominance curves showed that species-frequency distribution is high at NSS 4, followed by NSS2, NSS1, MVI, NSS3, MV2, FB and HB sites (Fig. 3.7).

3.4.4. Invertebrate communities In present study 24 species of invertebrates (13 species of molluscs in10 families and 12 genera, 3 species of sponges in 2 families and 2 genera, 3 species of sea anemones in 2 families and 2 genera, 3 species of echinoderms in 3 families and 3 genera and 2 species of crustaceans in 2 families and 2 genera) were recorded. Among 24 invertebrate species 12 (9 molluscs, 2 echinoderms and 1 ) were identified up to species level, 9 up to genus level (3 molluscs, 3 sea anemones, 2 sponges, 1 echinoderm and 1 crustaceans). 2 species could not identify with certainty while there is doubt about 1 species. High diversity was noted at MV and CI diving sites. The sea urchin Echinometra mathaei followed by Diadema setosum was abundant at MVI and almost all sites of CI. Sea anemones were mostly common at MV2, NSS4 and at FB2. Overall, the patterns of distribution were found linked with habitat complexity. A list of invertebrate species with site to site heterogeneity and relative abundance is shown in Table 3.4 and Fig. 3.8 (A-B). A cluster analysis of invertebrate communities at 9 sites showed that HB1 and HB2, the northern sheltered site of CI (NSS1 and NSS2) and MV1 and MV2 formed well clusters at similarity levels of about 50%, 75% and 70% while FB, NSS3 and NSS4 formed distinct cluster at a similarity level of about 0 %, 75 % and 60 % respectively (Fig. 3.9). The K dominance curve indicated that species-frequency distribution is high at MV2, followed by MV1, NSS4, NSS3, NSS1, NSS2, HB2, FB2 and HB1 (Fig. 3.10).

38

3.4.5. Physico-chemical parameters of sea water and elemental composition of coral skeletons Results regarding seawater physico-chemical parameters are included in chapter 2. Overall fluctions in physical, organic (Fig. 2.1) and inorganic nutrients (Fig, 2.2) were noted. Also variations in the concentrations of HCO3- , CO32- , HO- (Fig. 2.3) and Ca2+ and Mg2+ (Fig. 2.4) were noted. Similarly calcium, magnesium and oxygen were recorded as major elements on the skeletons of coral. The percentage weight concentration of each element in coral skeletons are presented in Table 2.1 while the EDS spectra of coral skeletons are displayed in Fig. 2.5.

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Table 3.1. Hard coral species recorded from 9 diving sites with relative abundance (6: Dominant, up to 300 individuals; 5: Abundant, up to 200 individuals; 4: Common, up to 100 individuals; 3: Frequent, up to 30 individuals; 2: Occasional, up to 10 individuals; 1: Rare, up to 5 individuals). Genera with a question mark indicate uncertainty in indentification.Where there is some doubt about identification the term cf. is used. Abbreviations used are as follow: CI: Churna Island; MV: Mubarak Village; FB: French Beach; HB: Hawks Bay; NSS1-4: Northern sheltered sites 1-4; MV1-2: Mubarak Village sites 1-2.

Hard corals Family CI MV FB HB NSS1 NSS2 NSS3 NSS4 MV1 MV2 HB1 HB2

Porites decasepta Poritidae 1

Porites lobata Poritidae 1 1 1 2 1 1

Porites cf. annae Poritidae 5 3 5 4

Porites cf. columnaris Poritidae 5 5 5 4

Porites cf densa Poritidae 6 5 6 6 2

Porites sp. Poritidae 1 1

Goniopora sp.1 Poritidae 1 1

Goniopora sp.2 Poritidae 1 1 1 1

Goniopora sp.3 Poritidae 1

Gonastrea sp.1 Faviidae 1

Gonastrea sp.2 Faviidae 1

Gonastrea sp.3 Faviidae 1

?Gonastrea sp.4 Faviidae 1

Favites vasta Faviidae 1

Cyphastrea serailia Faviidae 1 1 1

Leptastrea transversa Faviidae 1

Pseudosiderastrea tayami Siderastreidae 1

Coscinaraea columna Siderastreidae 1

Psammocora sp.1 Siderastreidae 1 1 1

Psammocora sp. 2 Siderastreidae 1

Physogyra sp. Euphyllidae 2 Total species 6 9 9 8 4 4 3 2

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Table 3.2. Abundance and distribution of hard coral species collected from 18 dive sites located along the coast of Pakistan with respective depth. Values of coral abundance is according to DACFOR numerical (1-6) scale: 6 = Dominant: up to 500 individuals; 5 =Abundant: up to 100 individuals; 4 = Common: up to 50 individuals; 3 = Frequent: up to 10 individuals; 2 =Occasional: up to 3 individuals; & 1 = Rare: 1 individual. Abbreviations are as follow. SS 1-2: Sandspit dive sites 1-2; BU: Buleji; GAR: Goth Abdul Rehman; MV: Mubarak Village; CI 1-2:; Churna Island sites 1-2; RS 1-3: Roadrigues Shoals 1-3 ; AT 1-6: sites 1-6; RO: Rocky Outcrops. Modified from Ali et al., (2014).

Hard coral species Sindh coast Balochistan coast

Gadani Ormara Astola Island Jiwani

m m

m

m m m m

m m

m

m

m

m

m m

SS2, 7.6 m BU, 3.7 GAR, 4.6 MV, 7.6 CI1, 8 CI2, 7 6.4 m RS1, 12.7 RS2, 10.9 RS3, 14 AT1, 4.5 AT2, 5.3 AT3, 4.5 AT4, 3.3 AT5,10 AT6, 18 RO, 6m SS1, 8.3 Family: Poritidae

?Goniopora albiconus 2 1

Goniopora columna 2

Goniopora djiboutiensis 2 2 1

Goniopora cf. savignyi 2 2 2 1 2

Goniopora somaliensis 2 2 2

Porites harrisoni 3 4 4 3

Porites lutea/lobta 3 2 3 3 2

Porites monticulosa 3 4

Porites nodifera 3 5 3 5

Porites solida 3 2 2 1

Alveopora sp. 3 1 2

Family Faviidae

Continued… 41

Favites complanata 4 4 3 3 2 2 3 1

Favites pentagona 1 2 4 5 5 3 1

Favites spinosa 2

?Leptastrea pruinosa 2 3 4

Leptastrea cf. bottae 3 1

Plesiastrea versipora 1 1 1

Family Siderastreidae

Coscinaraea monile 1 2 2 3 3 2

Coscinaraea sp. 2 2

Psammocora obtusangulata 3 4

Psammocora superficialis 2

Psammocora sp. 3 2

Family Dendrophylliidae

?Dendrophyllia robusta 2 3

Turbinaria spp. 2

Family Mussidae

Acanthastrea hillae 2 2 2 2

Acanthastrea maxima 2 2 1

Family Pocilloporidae

Pocillopora damicornis 5 5 5

Family Acroporidae

Montipora mollis 2 2 3 2 1

Family Agariciidae

Pavona explanulata 1 Total species 2 . - - 2 8 2 - 4 3 4 13 16 17 15 3 3 -

42

Table 3.3. Diversity of fishes recorded at 9 dive sites. The abbreviations used as; P: Present, other abbreviations used are similar as in Table 3.1.

Fish species Family Feeding level CI MV FB HB NSS1 NSS2 NSS3 NSS4 MV1 MV2 Ctenochaetus striatus Acanthuridae Invertivorous p p p p Pristiapogon fraenatus Apogonidae Planktivorous p Apogonichthyoides pseudotaeniatus Apogonidae Planktivorous p p Apogonichthyoides sialis Apogonidae Planktivorous p Ostorhinchus cookii Apogonidae Invertivorous p Ostorhinchus flagelliferus Apogonidae Invertivorous p Abalistes stellatus Balistidae Invertivorous p Heniochus acuminatus Chaetodontidae Planktivorous p p Heniochus diphreutes Chaetodontidae Planktivorous p p Sardenella sp. Clupeidae Planktivorous? p p Platax teira Ephippidae Omnivorous p p Plectorhinchus gattuerinus Haemulidae Invertivorous p Plectorhinchus sordidus Haemulidae Invertivorous p p p Pomadasys stridens Haemulidae Carnivorous p p Labroides dimidiatus Labridae Invertivorous p Halichoeres dussumieri Labridae Invertivorous p p p p Halichoeres scapularis Labridae Invertivorous p p daura Invertivorous p p p Lutjanus lutjanus Lutjanidae Invertivorous+Carnivorous p Lutjanus vitta Lutjanidae Invertivorous+ Carnivorous p p Scolopsis vosmeri Nemipteridae Invertivorous p p p Pempheris malabarica Pempheridae Planktivorous p p Abudefduf bengalensis Pomacentridae Planktivorous p p p p p Abudefduf sexfasciatus Pomacentridae Planktivorous p p Abudefduf vaigiensis Pomacentridae Planktivorous p p p p p p p Amphiprion sandaracinos Pomacentridae Omnivorous p p Chromis flavaxilla Pomacentridae Planktivorous p p

Continued… 43

…. Chromis sp. Pomacentridae Planktivorous p p Neopomacentrus bankieri Pomacentridae Planktivorous p p p p p p p p Neopomacentrus cyanomos Pomacentridae Planktivorous p p p p Neopomacentrus sindensis Pomacentridae Planktivorous p p p p p p p p Neopomacentrus miryae Pomacentridae Planktivorous p p p p Pomacentrus caeruleus Pomacentridae Planktivorous p p Pseudochromis aldabraensis Pseudochromidae Invertivorous p p p p Pseudochromis nigrovittatus Pseudochromidae Invertivorous p p Pseudochromis omanensis Pseudochromidae Invertivorous p p Pseudochromis springeri Pseudochromidae Invertivorous p p p p p Chlorurus bowersi Scaridae Herbivorous p p p p Chlorurus capistratoides Scaridae Herbivorous p p p Chlorurus sordidus Scaridae Herbivorous p p Scarus arabicus Scaridae Herbivorous p p Scarus zufar Scaridae Herbivorous p p Coeroichthys brachysoma Scombridae Carnivorous? p p Scorpaenopsis barbatus Scorpaenidae Carnivorous p Epinephelus malabaricus Serranidae Carnivorous p Signanus javus Siganidae Herbivorous p p p Siganus luridus Siganidae Herbivorous p p p Signanus sp. Siganidae Herbivorous p Acanthopagurs catenula Sparidae Invertivorous p Acanthopagurs bifasciatus Sparidae Invertivorous p Diplodus capensis Sparidae Invertivorous p p Sphyraena obtusata Sphyraenidae Carnivorous p Pseudosynanceia sp Synanceiidae Carnivorous p Lagocephalus sp. Tetraodontidae Carnivorous p p p Torpedo fuscomaculata Torpedinidae Carnivorous p Torpedo sinuspersici Torpedinidae Carnivorous p p Total species number 25 29 22 24 19 9 8 2

44

Table 3.4. Diversity of Invertebrates recorded at 9 diving sites with relative abundance. The abundance rating scale, abbreviations signs used for species identification is same as mentioned in Table 3.1.

Invertebrate species Phylum Family CI MV FB HB NSS1 NSS2 NSS3 NSS4 MV1 MV2 HB1 HB2

Pinna bicolor Mollusca Pinnidae 4 1 1 Atrina pectinata Mollusca Pinnidae 1 Perna viridis Mollusca Mytilidae 2

Mimachlamys townsendi Mollusca Pectinidae 1 ?Dendostrea sp. Mollusca Ostreidae 5 Turbo bruneus Mollusca Turbinidae 1 1 1 Astralium cf. Semicostatum Mollusca Turbinidae 1 1 Erosaria turdus Mollusca Cypraeoidea 1 1 Babylonia spirata Mollusca Babyloniidae 1 1 Turbinella pyrum Mollusca Turbinellidae 1 Purpura bufo Mollusca Muricidae 1 1 Purpura sp. Mollusca Muricidae 1 1 Cantharus sp. Mollusca Buccinidae 1 Palythoa sp. 1 Cnidaria Zoanthidae 2 2 2 Palythoa sp. 2 Cnidaria Zoanthidae 2 1 Boloceroides sp. Cnidaria Boloceroididae 1 Callyspongia sp.1 Porifera Callyspongiidae 2 2 3 3 1 Callyspongia sp.2 Porifera Callyspongiidae 1 1 1 ?Cliona sp. Porifera Clionaidae 1 Echinometra mathaei Echinodermata Echinometridae 2 2 3 3 3 2 Diadema setosum Echinodermata Diadematidae 2 2 3 3 3 2 Holothuria sp. Echinodermata Holothuriidae 1 Portunus sanguinolentus Arthropoda Portunidae 1 Atergatis sp. Arthropoda Xanthidae 1 1 Total species number 5 4 8 9 9 12 2 1 3

45

Figure 3.1 A. Diversity of stony corals recorded from the littoral waters of Sindh, Pakistan: 1) Porites decasepta; 2) Porites lobata; 3) Porites cf. annae; 4) Porites cf. columnaris; 5) Porites cf densa; 6) Porites sp.; 7) Goniopora sp.1; 8) Goniopora sp.2; 9) Goniopora sp.3; 10) Gonastrea sp. 1; 11) Gonastrea sp. 2; 12) Gonastrea sp. 3.

46

Figure 3.1 B. Diversity of stony corals recorded from the littoral waters of Sindh, Pakistan: 13) ?Gonastrea sp.4; 14) Favites vasta; 15) Cyphastrea serailia; 16) Leptastrea transversa; 17) Pseudosiderastrea tayami; 18) Coscinaraea columna; 19) Psammocora sp. 1; 20) Psammocora sp. 2; 21) Physogyra sp.

47

Figure 3.2. Corals degredation due to bleaching, bioerrosion and change in community structure at Mubarak Village and Churna Island. a-b: bleaching effects; c: bioerrosion due to Cliona sp. and d: shift in community structure due to cyclone ‘NILOFAR’ at Mubarak Village, e-f: coral mortality due to bleaching at Churna Island.

48

Figure 3.3. Cluster analysis for coral communities at 8 dive sites excluding HB1 based on root transformation and Bray Curtis similarity index using group average linkage techniques. Symbols used FB: French Beach; HB2: Hawks Bay 2; MV1: Mubarak Village site 1; MV2: Mubarak Village site 2; NSS1-4: northern sheltered sites 1-4.

Figure 3.4. The K dominance curves (a: cumulative, b: partial) for coral communities at 8 diving sites excluding HB1 following Lambshead, Platt, and Shaw, (1983). Abbreviations are same as in Figure 3.3.

49

Figure 3.5 A. Diversity of fishes recorded from the littoral waters of Sindh, Pakistan: 1) Ctenochaetus striatus; 2) Pristiapogon fraenatus; 3) Apogonichthyoides pseudotaeniatus; 4) Apogonichthyoides sialis; 5) Ostorhinchus cookie; 6) Ostorhinchus flagelliferus; 7) Abalistes stellatus; 8) Heniochus acuminatus; 9) Heniochus diphreutes; 10) Sardenella sp.; 11) Platax teira; 12) Plectorhinchus gattuerinus; 13) Plectorhinchus sordidus; 14) Pomadasys stridens; 15) Labroides dimidiatus; 16) Halichoeres dussumieri; 17) Halichoeres scapularis; 18) Karalla daura; 19) Lutjanus lutjanus; 20) Lutjanus vita; 21) Scolopsis vosmeri; 22) Pempheris malabarica; 23) Abudefduf bengalensis ; 24) Abudefduf sexfasciatus.

50

Figure 3.5 B. Diversity of fishes recorded from the littoral waters of Sindh, Pakistan: 25) Abudefduf vaigiensis; 26) Amphiprion sandaracinos; 27) Chromis flavaxilla; 28) Chromis sp; 29) Neopomacentrus bankieri; 30) Neopomacentrus cyanomos; 31) Neopomacentrus sindensis; 32) Neopomacentrus miryae; 33) Pomacentrus caeruleus; 34) Pseudochromis aldabraensis; 35) Pseudochromis nigrovittatus; 36) Pseudochromis omanensis; 37) Pseudochromis springeri; 38) Chlorurus bowersi; 39) Chlorurus capistratoides; 40) Chlorurus sordidus; 41) Scarus arabicus; 42) Scarus zufar; 43) Coeroichthys brachysoma; 44) Scorpaenopsis barbatus; 45) Epinephelus malabaricus; 46) Signanus javus; 47) Siganus luridus; 48) Siganus sp.

51

Figure 3.5 C. Diversity of fishes recorded from the littoral waters of Sindh, Pakistan: 49) Acanthopagurs catenula; 50) Acanthopagurs sp.; 51) Diplodus capensis; 52) Sphyraena obtusata; 53) Pseudosynanceia sp; 54) Lagocephalus sp; 55) Torpedo fuscomaculata; 56) Torpedo sinuspersici.

Figure 3.6. Cluster analysis for fish communities at 9 dive sites based on presence and absence data and Bray Curtis similarity index using group average linkage techniques. Symbols used as FB: French Beach; HB1-2: Hawks Baysites 1-2; MV1- 2: Mubarak Village sites 1-2; NSS1-4: northern sheltered sites 1-4.

52

Figure 3.7. The K dominance curves (a: Cumulative dominance; b: Partial dominance) for fish communities at 9 dive sites following Lambshead, Platt, and Shaw, (1983). Abbreviations are same as in Figure 3.6.

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Figure 3.8 A. Diversity of invertebrates recorded from the littoral waters of Sindh, Pakistan: 1) Pinna bicolor; 2) Atrina cf. fragilis; 3) Perna viridis; 4) Mimachlamys townsendi; 5) Dendostrea sp.; 6) Turbo bruneus; 7) Astralium cf. Semicostatum; 8) Erosaria turdus; 9) Babylonia spirata; 10) Turbinella pyrum; 11) Purpura bufo; 12) Purpura sp.

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Figure 3.8 B. Diversity of invertebrates recorded from the littoral waters of Sindh, Pakistan: 13) Cantharus sp.; 14) Palythoa sp. 1; 15) Palythoa sp. 2; 16) Boloceroides sp.; 17) Callyspongia sp.1; 18) Callyspongia sp.2; sp.; 19) ?Cliona sp.; 20) Echinometra mathaei; 21) Diadema setosum; 22) Holothuria sp.; 23) Portunus sanguinolentus; 24) Atergatis sp.

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Figure 3.9. Cluster analysis for invertebrate communities at 9 dive sites based on root transformation and Bray Curtis similarity index using group average linkage techniques. Symbols used as FB: French Beach; HB1-2: Hawks Bay sites 1-2; MV1- 2: Mubarak Village sites 1-2; NSS1-4: northern sheltered sites 1-4.

Figure 3.10. The K dominance curve (Cumulative dominance) for invertebrate communities at 9 dive sites following Lambshead, Platt, and Shaw, (1983). Abbreviations are same as in Figure. 3.9.

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3.5. Discussion 3.5.1. Coral communities During recent surveys, some degree of reef formation appeared in waters off the coastal areas, particularly at northern sheltered side of Churna Island, whereas poor coral growth observed in coastal environments. Corals in these environments were mostly patchily distributed with Porites dominating. Diverse hard coral communities at northern sheltered sites of Churna Island might be due to its considerable distance from coast, presence of hard substrate for coral attachment, less turbid water conditions and perhaps fewer nutrients, so that macroalgae do not outcompete corals. The water currents in such environments are considerably high that helps solar heating to higher water temperature (Sheppard, Price, and Roberts, 1992). Poor coral cover in coastal habitats is mainly due to high wave action that stirs up sediment, leading to high turbid conditions. Further, the coastal waters seemed to be nutrient rich with dense green phytoplankton blooms also leading to very poor visibility (Naz et al., 2014; Munir et al., 2016) thus preventing zooxanthellae to photosynthesize. Moreover the polyps of some hard coral species easily become clogged by settlement of suspended sediment therefore not well adopted to survive in turbid environments (Rogers, 1990; Philipp and Fabricius, 2003; Fabricius, 2005). Dominance of Porites species in coastal environments especially at Mubarak Village might be its ability to tolerate high sediment load ((Riegl, 1999). In addition, it is suggested that hard corals, distribution and diversity appear to be linked with environmental and geological settings. For example, small to medium size corals (with 3 to 8 mm corallites) were dominant in turbid environments, while medium to large size (with 8 to 15 mm corallites) remained the characteristic of clear water conditions (Flugel, 1982; Kiessling, Flugel, and Golonka,1999; Dupraz and Strasser, 2002; Flugel, 2002; Flugel and Kiessling, 2002; Leinfelder et al., 2002; Perrin, 2002; Wilson and Lokier, 2002; Stanley, 2003; Olivier et al., 2004; Sanders and Baron-Szabo, 2005). No significant ocean acidification impacts were observed but nevertheless increasing as bicarbonate values were noted high. Also a slight decrease in pH values was noted particularly at Churna Island compare to pre-industrial time (Royal Society, 2005). High Mg values in waters samples and no values in majority of coral skeletons might be due to poor biological control on structural composition as Mg2+ is mostly used by corals to strongly control the growth of different structural components (Meibom et al., 2004). Though calcium carbonate was the main skeleton builder of the analyzed coral samples

57 but other trace metals were observed (Table 2.7). The ratios of trace metals are mostly controlled either by biological or environmental factors (Livingston and Thompson, 1971).

High corals degradation due to bleaching, bioerrosion by Cliona species and shift in community structure at Mubarak Village might be due to thermal stress and nutrient concentrations which is much higher than that preferred by the corals. It is evident that bleaching effects in shallow coastal environments are higher compare to offshore deeper waters (Furby, Boumeester, and Berumen, 2013). Further, nutrient rich water (ammonium: 0.2 -0.5 µM, nitrite: 0.1-0.5 µM, phosphorus: less than0.3 µM) enhances the growth of macroalgae and coral eroding sponge (Cliona sp.) (Furnas, 1991) which restricts coral growth and distribution.

Seawater temperature data indicated that temperature remained with the close proximity of upper and lower limits of optimum temperature conditions for coral growth (25-28°C) compare to surrounding localaties (e.g. Oman, Arabian-Persian Gulf, Yemen). However, higher temperature during summer could be a limiting factor. High nutrient concentrations, poor visibility due to sediment load and phytoplankton blooms, high sediment load due to strong wave action in coastal areas, rich macroalgal growth, distribution of coral communities to a restricted depth (not more than 15 m) and specially the lack of hard substrate for larval attachment ((personal observations) indicated that Pakistan coral fauna have the features of a marginal community surviving in stressful environmental conditions. According to Kleypas, Buddemeier, and Gattuso (1999), marginal coral communities survive in harsh environmental conditions (i.e. low and high water temperature, aragonite saturation and light penetrations). Increase in sediment load reduces biotic area, species abundance, coral cover and irradiances (Rogers, 1990; Fabricius; 2005).

Comparing hard coral fauna, including 29 species reported by Ali et al., ( 2014), with the surrounding highly marginalized communities i.e. 34 species in 25 genera from Kuwait (Hodgson and Carpenter, 1995), 253 species in 58 genera from Socotra Archipelago (Yemen) (DeVantier et al., 2004), 37 species in 24 genera from Gulf of Kutch (Pillai and Patel, 1988), 91 species in 47 genera from Oman (Sheppard and Salm, 1988), 28 species from Bahrain (Sheppard, 1988), 34 species in 16 genera from UAE

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(Riegl, 1999), the coral fauna of Pakistan is similar to some parts of the region i.e. UAE, Kuwait and Persian Gulf.

Biogeographically, the fauna of the Arabian Sea is a subset of total Indian Ocean corals (with 11.3 % endemism of hard corals) mixed with regional endemics (Sheppard, Price, and Roberts, 1992). There are some dispersal barriers between the Arabian Sea and Indo- Pacific. Potential conditions for these barriers are upwelling processes and dominance of soft substrate in the Gulf of Oman (Sheppard and Sheppard 1991; Sheppard, Price, and Roberts, 1992). Many of the present day distribution within the Arabian region may be no more than chance distribution. The chance playing a major role in determining the identity of the discrete fauna for subset of Arabian corals since there is only widely scattered habitats suitable for coral settlement over great distances (Sheppard and Sheppard 1991; Sheppard, Price, and Roberts, 1992).

No recorded species was found endemic to the Pakistan coast; however, there are four potential candidates, Physogyra species, one species of Gonastrea, one species of Porites and one species of Goniopora might be new species.

3.5.2. Fish communities High fish diversity was recorded at CI and MV. This might be due to habitat complexity at these sites structured by rich coral cover, rocky outcrops and mounds, provided shelter from predators. Several studies (Lukhurst and Lukhurst, 1978; Bell and Galzin, 1984; Sale and Douglas; 1984; Roberts and Ormond, 1987; Chabanet et al., 1997; Friedlander and Parrish, 1998; Ferreira, Goncalves, and Coutinho, 2001; Almany, 2004; Sandin et al., 2008) have been undertaken regarding the link between fish diversity and habitat complexity. Dominance of planktivorous fishes indicated that nutrient rich water fuel a trophic chain from phytoplankton to zooplankton to planktivorous species that are ultimately consumed by predators. Similar trends were reported from Oman where community was dominated by planktivorous species (Burt et al., 2011).

Comparing reef-fish fauna with surrounding reef associated fishes in the region i.e. 511 fish species from Oman (Fouda, Harmosa, and Harthi,1998), 187 species from northern Arabian Gulf (Krupp and Miiller, 1994), 71 species from Bahrain (Smith et al., 1987),

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101 species from Arabian Gulf (Coles and Tarr, 1990), and 797 species from Red Sea (List of reef fishes of Red Sea, 2015), reef associated fish diversity in coastal waters of Sindh seemed to be much lower but comparable to Bahrain. However, fish reported here were only recorded on a small scale, and it is assumed that during further surveys at sheltered sites along the whole coast and especially at Astola Island, may increase by a considerable number reef associated fishes in Pakistan.

3.5.3. Invertebrate communities Most invertebrates were recorded from Mubarak Village and Churna Island with only few encountered at Hawks Bay and French Beach. High invertebrates diversity at Mubarak Village and Churna Island is mainly due to complex habitat structure at these sites (mounds, ridges, gullies, outcrops, corals, coralline and fleshy algae etc.), that provide shelter from predation, reduce competition and predation outcomes, reduce attack rates between predator and prey by providing excessive food (Murdoch and Oaten, 1975; Hixon and Menge, 1991; Almany, 2004). Dominance of Sea-urchins at MV and CI might be due to availability of hiding places from predators and sufficient food (seaweeds, algal turf etc). The presence of boring sponge Cliona sp. at MV also is consistant with the coastal environment being more polluted than offshore waters.

2.6. Threats and Recommendations Anthropogenic and environmental impacts on coral and fish fauna of Pakistan are though minor but nevertheless increasing. To understand better, the impacts of ocean acidification, further studies in terms of biological and environmental changes are recommended.

The effects of were observed on northern sheltered side of the Churna Island (with high coral abundance) mainly because of the use of Island as a training pool by non-registered tourism promoters. Breakage of coral colonies was also observed by nets entangled with corals. Besides these activities, breakage of fragile corals for ornaments was also observed in the city. Similar threats were observed earlier at Astola Island (along Balochistan coast). Fishermen were observed to use nets that got entangled in the corals causing coral breakage and the uprooting of whole colonies. Mechanical damage

60 was also inflicted on the corals by the use of lobster pots that were deployed in shallow areas.

As the coral communities of Pakistan are surviving in a stressful environment, there is need to establish marine protected areas at least in areas where Charna and Astola Islands are located. Although, Astola Island has already been declared as a marine protected area (Dawn, 2017) but there is need to include all parameters necessary for the design of effective marine protected areas to mitigate the climate change impacts. Marine protected areas increase the resistance ability of corals against environmental changes by directly extenuating other stressors such as sediments input from land, overfishing and nutrient inputs (Grimsditch and Salm, 2005). Future coastal protection efforts should focus particularly on the involvement of local community and wider public so that they can admire the importance of these natural resources. Moreover, the regular monitoring of the coral communities at these Islands will surely help to understand the effects interms of biological or environmental changes. As information, gathered from amateur divers and fishermen, rich coral communities do occur close to shore and an investigation of more sites in particular around Gwadar and other sheltered sites along Balochistan coast should be undertaken.

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Chapter 4

Characterization of Macroalgal Communities in the Coastal Waters of Sindh (Pakistan), a Region under the Influence of Reversal Monsoons

This chapter has published as: Ali, A., Siddiqui, P.J.A. & Aisha, K. (2017). Characterization of macroalgal communities in the coastal waters of Sindh (Pakistan), a region under the influence of reversal monsoons. Regional Studies in Marine Science, 14, 84-92.

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4.1. Abstract

Marine benthic seaweeds have a significant academic, biological, environmental and economic importance. Coastal waters of Pakistan have a rich algal resource due to nitrate fluctuations caused by convective mixing and up-sloping. Studies on seaweeds in Pakistan are mainly confined to intertidal areas or on the basis of drift samples with much emphasis on taxonomy and phycochemistry without an in-depth study of the ecology. In the present study, samples were collected by SCUBA diving from 5 dive sites. Quadrat techniques were used to determine the relative diversity and abundance of benthic macroalgal communities. A total of 36 species (16 Phaeophyceae, 12 Rhodophyta, and 8 Chlorophyta) were recorded. An increase in diversity and distribution patterns was noted from west to east ward. High diversity occurred at Hawks Bay followed by French Beach. The coral sites (northern sheltered site of Churna Island and Mubarak Village) had a less diversity. Very few recorded species had a restricted distribution (Yemen, Oman and India). One species (Stypopodium shameelii ) was found endemic to Pakistan whereas the rest are widely distributed in the entire Indian Ocean, Atlantic and Pacific. Stunted growth of Sargassum species and changes in community structure were observed after the Cyclone ‘NILOFAR’. Distribution and diversity patterns appeared to be linked with habitat type, topography, wave exposure and prevailing climatic conditions.

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4.2. Introduction

Marine benthic seaweeds have a significant biological, environmental and economic role in coastal ecosystems (Chopin and Sawhney, 2009). Seaweeds, especially coralline algae are foremost reef builders as they consolidate the building material produced by corals, enhance the process of coral colonization and facilitate the endurance of coral larvae through chemical interactions (Dowson, 1961b; Fabricius et al., 2015). A wealth of information is available on the geographic distribution of seaweeds. The tropical Indo– West Pacific is considered as the region with the highest diversity of seaweeds (with 2991 species) (Briggs, 1974; Breeman, 1988; Silva, Basson, and Moe, 1996; Adey and Steneck, 2001).

The Arabian Sea especially the Gulf areas, is relatively unattractive for marine life due to high latitude effect and prevailing seasonal harsh environmental conditions (temperature, salinity fluctuations). In shallow areas, these fluctuations are high compared to any other coastal regions in the world (Coles, 1988; Coles and Fadlallah, 1991; Sheppard, Price, and Roberts, 1992; Price, Sheppard, and Roberts, 1993; John and Al-Thani, 2014). However, reversal of monsoons, an important feature of the Arabian Sea, affects its climatic conditions (Weller et al., 1998). Due to Ekman effect, the warm surface water moves offshore thus leads to an upwelling of deep, cold and nutrient rich water. The upwelled water not only reduces the temperature salinity fluctuations but also makes the water highly nutrient rich, thus acting as fuel for phytoplankton growth (Weller et al., 1998; Sheppard and Sheppard, 1991; Sheppard, Price, and Roberts, 1992; Coles, 2001; Salm, 1993). There are several studies conducted on the taxonomy (Basson, 1979 a, b; Basson, Mohamed, and Arora,1989; Wynne and Banaimoon, 1990; Cardero, 1992; Wynne and Jupp, 1998; Sohrabipour and Rabi, 1999; Wynne, 2001, 2003; Wynne and de Jong, 2002; Gharanjik, 2003; Hosseinim and Gharanjik, 2003; Schils and Coppejans, 2002; Schils, Wynne and Freshwater, 2004; Dadolahi and Savari, 2005; Noormohammadi et al., 2010; Noormohammadi, Baraki, and Sheidai, 2011 ) and ecology (Barratt et al., 1984; Banaimoon, 1988; Ormond and Banaimoon, 1994; Gharanjik et al., 2011; Dadolahi et al., 2012; John, 2012) of the benthic marine algae in the Arabian Sea region.

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Pakistan coast is subjected to repeated summer and winter monsoon that causes profound convective mixing (Wiggert et al., 2000), although there was no difference between phytoplankton biomass and primary productivity during both monsoons periods (Marra et al., 1998). Due to the warm climate and nutrient supplementation through convective mixing, the coast of Pakistan has a rich algal diversity and biomass. A wealth of information on taxonomy (Nizamuddin, 1964; Nizamuddin and Begum, 1973; Saifullah and Nizamuddin, 1977; Shameel, 1987, 2008; Shameel, Afaq-Husain, and Shahid- Husain, 1989; Shameel and Tanaka, 1992; Amjad and Shameel, 1993; Aliya and Shameel, 1996; Shameel, Aisha, and Khan, 1996), ecology (Saifullah, 1973; Saifullah, Shaukat, and Khan, 1984; Qari and Qasam, 1988; Hameed and Muzammil, 1999) and phycochemistry (Memon et al., 1991; Qasim, 1992; Aliya and Shameel, 2003; Rizvi and Shameel, 2003; Rizvi, 2010; Haq et al., 2011) now exists.

The previous studies were mostly confined to intertidal areas and/or on the basis of drift samples with much emphasis on taxonomy and biochemistry without a deep knowledge of ecology. The present study presents the results of preliminary survey conducted at a number of sites along the Sindh coast of Pakistan. An overview of surveyed habitats and their macroalgal communities is given.

4.3. Materials and Methods

The details about study sites, techniques used in field and statisticle analysis are included in chapter 1(section 1.2).

4.4. Results 4.4.1. Description of survey sites Habitat features, under water observations, GPS positions and depth recorded at each site along with depth and GPS positions are included in Table 1.2 (section 1.2).

4.4.2. Benthic macroalgal communities In the present study, 36 species, (16 Phaeophyceae, 12 Rhodophyta, and 8 Chlorophyta) belonging to 14 families and 22 genera were recorded before and after the cyclone at 5

65 dive sites from the coastal waters along the Sindh coast, Pakistan. Out of 36 species, 33 were identified to species level and 3 up to genus level. High diversity occurred at HB followed by FB, MV and CI. One of the recorded species (Stypopodium shameelii) was found endemic to Pakistan, 2 species (Scinaia hatei, Codium indicum) had a restricted distribution (India, Yemen, Oman), 6 species ( hauckiana, Stoechospermum polypodioides, Sargassum lanceolatum, Iyengaria stellata, Botryocladia leptopoda, Coelarthrum opuntia) are distributed in the entire Indian Ocean whereas the rest were widely spread in Indian Ocean, Atlantic and Pacific.

4.4.2.1. Pre-cyclonic communities Thirty three species were recorded during pre-cyclone observations. Variations in species composition and distribution patterns were noted between sites. HB sites (1, 2) were dominated by large size Sargassum species (1 to 4 m) forming mono-specific stands. The other macroalgae with comparatively small size e.g. , Dictyota hauckiana, Stypopodium shameelii, Colpomenia sinuosa, Iyengaria stellata, Padina pavonica, Solieria robusta, Scinaia hatei, Asparagopsis taxiformis, Halymenia porphyroides, Coelarthrum opuntia, Amphiroa anceps, Caulerpa taxifolia, Caulerpa scalpelliformis, Codium indicum and Codium decorticatum were mostly confined to marginal environments or at places where a considerable space was available between Sargassum species.

A clear zonation pattern was observed at FB. Codium fragile, Caulerpa chemnitzia, Caulerpa taxifolia and Caulerpa scalpelliformis were confined to a depth of 3 to approximately 7 m, while Codium latum, Sargassum lanceolatum and Sargassum aquifolium were found to occur at the lower side of the ledge and at the base. Contrasting to HB and FB, at MV, the community was dominated by coralline algae whereas at CI few species of fleshy algae were found. These are mainly confined to marginal environments.

4.4.2.2. Post-cyclonic communities A total of 30 species were recorded during post- cyclonic observations. 6 species (Dictyota hauckiana, Iyengaria stellata, Solieria robusta, Scinaia hatei, Calliblepharis sp. and Codium indicum), recorded during pre-cyclonic period were not found during

66 post-cyclonic period. Three species (Dictyota implexa, Sargassum cinctum, and Botryocladia leptopoda), recorded during post-cyclonic period was not found during pre- cyclonic observations. Mixed community structure and stunted growth of Sargassum species were observed especially at HB sites. Dictyota implexa was recorded as a significant species at HB site 2. Also a stunted growth of Sargassum species was noted at FB and with a small change change in species percentage cover. Contrasting to HB and FB, a marked change was recorded in abundance patterns of some species (Table 4.1). Ceramium sp., which had a limited distribution before cyclone, was recorded as an abundant species followed by Galaxaura sp., Lobophora variegata and Padina pavonica. No marked changes were noted at CI except the removal of Meristotheca papulosa. A detailed list of species recorded during pre and post-cyclonic periods is given in Fig. 4.1 (A-D) and Table 4.1, which also indicates their relative abundance.

Cluster analysis of macroalgal communities recorded before and after cyclone at the 5 dive sites showed that the CIBC and CIAC, MVBC and MVAC, FBBC and FBAC and HB1BC and HB2BC constructed well defined clusters at similarity levels of about 80 %, 83 %, 95 % and 90 %, while the HB2ACand HB1AC formed separate clusters at similarity levels of 60% and 65% respectively (Fig. 4.2). K. dominance curve indicated that species-frequency distribution before cyclone is high at HB 2 followed by HB 1, FB, MV and CI and high at HB1 followed by HB2, FB, MV and CI after the cyclone (Fig. 4.3).

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Table 4.1. Distribution and abundance of macroalgal species collected before and after cyclone from 5 dive sites situated along the Sindh coast of Pakistan. Abundance rating is as follow 1 = up to 5 plants; 2= up to 15 plants; 3 = up to 30 plants; 4 = up to 60 plants; 5= up to 200 plants; 6 = up to500 plants. Abbreviations used: HB 1-2: Hawks Bay dive site 1-2; FB: French Beach; MV: Mubarak Village; CI: Churna Island; BC: Before cyclone; AC: After cyclone.

Species Family Group HB FB MV CI HB1 HB2 BC AC BC AC BC AC BC AC BC AC Dictyota dichotoma Phaeophyceae 2 4 2 4 1 3 3 Dictyota implexa Dictyotaceae Phaeophyceae 4 Dictyota hauckiana Dictyotaceae Phaeophyceae 1 Stoechospermum polypodioides Dictyotaceae Phaeophyceae 1 4 1 2 Stypopodium shameelii Dictyotaceae Phaeophyceae 1 1 1 2 2 3 Stypopodium zonale Dictyotaceae Phaeophyceae 1 3 1 4 1 2 Spatoglossum asperum Dictyotaceae Phaeophyceae 1 1 Lobophora variegata Dictyotaceae Phaeophyceae 3 5 Padina pavonica Dictyotaceae Phaeophyceae 1 3 1 3 4 Sargassum cinctum Sargassaceae Phaeophyceae 1 1 Sargassum aquifolium Sargassaceae Phaeophyceae 4 3 3 2 2 2 Sargassum ilicifolium Sargassaceae Phaeophyceae 1 1 1 1 Sargassum lanceolatum Sargassaceae Phaeophyceae 4 5 4 5 3 3 Sargassum swartzii Sargassaceae Phaeophyceae 2 1 Colpomenia sinuosa Scytosiphonaceae Phaeophyceae 2 1 1 1 1 Iyengaria stellata Scytosiphonaceae Phaeophyceae 2 2 Meristotheca papulosa Solieriaceae Rhodophyta 1 2 1 1 1 Solieria robusta Solieriaceae Rhodophyta 1 2 Scinaia hatei Solieriaceae Rhodophyta 1 1 Botryocladia leptopoda Rhodymeniaceae Rhodophyta 2 Coelarthrum opuntia Rhodymeniaceae Rhodophyta 1 2 1 Tricleocarpa fragilis Galaxauraceae Rhodophyta 1 1 1 1 Galaxaura sp. Galaxauraceae Rhodophyta 4 6

Continued… 68

Asparagopsis taxiformis Bonnemaisoniaceae Rhodophyta 2 2 Halymenia porphyroides Halymeniaceae Rhodophyta 1 1 1 1 Ceramium sp. Ceramiaceae Rhodophyta 3 6 Amphiroa anceps Corallinaceae Rhodophyta 1 1 1 1 Calliblepharis sp. Cystocloniaceae Rhodophyta 1 Codium decorticatum Codiaceae Chlorophyta 1 1 1 2 2 Codium fragile Codiaceae Chlorophyta 1 6 5 Codium indicum Codiaceae Chlorophyta 1 1 Codium latum Codiaceae Chlorophyta 2 1 Caulerpa chemnitzia Caulerpaceae Chlorophyta 4 3

Caulerpa scalpelliformis Caulerpaceae Chlorophyta 1 1 3 1 3 3 Caulerpa taxifolia Caulerpaceae Chlorophyta 1 1 3 3 3 1 Udotea Indica Udoteaceae Chlorophyta 1 1 Total species 19 17 24 15 13 12 9 7 3 2

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Figure 4.1. A. Diversity of macroalgal species recorded from littoral waters of Sindh, Pakistan: (1) Dictyota dichotoma; 2) Dictyota divaricata; 3) Dictyota hauckiana; 4) Stoechospermum polypodioides; 5) Stypopodium Shameelii; 6) Stypopodium Zonale; 7) Spatoglossum asperum 8) Lobophora variegata; 9) Padina pavonica. 10) Sargassum cinctum: 11) Sargassum aquifolium; 12) Sargassum ilicifolium; 13) Sargassum lanceolatum; 14) Sargassum swartzii; 15) Colpomenia sinuosa; 16) Iyengaria stellata; 17) Meristotheca papulosa; 18) Solieria robusta.

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Figure 4.1. B. Diversity of macroalgal species recorded from littoral waters of Sindh, Pakistan: 19) Scinaia hatei; 20) Botryocladia leptopoda; 21) Coelarthrum opuntia; 22) Tricleocarpa fragilis; 23) Galaxaura sp.; 24) Asparagopsis taxiformis; 25) Halymenia porphyroides; 26) Ceramium sp.; 27) Amphiroa anceps. 28) Calliblepharis sp.; 29) Codium decorticatum; 30) Codium fragile; 31) Codium indicum; 32) Codium latum; 33) Caulerpa chemnitzia; 34) Caulerpa scalpelliformis; 35) Caulerpa taxifolia; 36) Udotea indica.

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Figure 4.2. Cluster analyses for macroalgal species conducted at 5 dive sites on the bases of presence-absence data and Bray–Curtis similarities. HB 1-2: Hawks Bay dive site 1-2; FB: French Beach; CI: Churna Island; MV: Mubarak Village; BC: Before cyclone; AC: After cyclone.

Figure 4.3. K. dominance curves (cumulative dominance) for macroalgal species at 5 dive sites following Lambshead, Platt, and Shaw, (1983). Abbreviations are same as in Figure4.2.

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4.5. Discussion

The study is a first account of work on the distribution and diversity of benthic macroalgal communities in the coastal waters of the Sindh along the Pakistan coast. The surveys indicated the presence of healthy algal growth along the Karachi coast, particularly at HB, FB and MV. Presence of huge mono-specific strands of Sargassum in near and offshore waters at HB might be due to a uniformly distributed habitat with a large intertidal area that ultimately dissipates the wave energy, and also to shading caused by the large-size Sargassum spp. that eliminated the small-sized macroalgae toward the marginal environments or to places where a considerable space was available between Sargassum spp. Change in community structure and zonation patterns at FB were possibly due to wave action, topography (Druehl and Green, 1982), the invasive nature of Codium fragile (Trowbridge, 1998; Provan, Murphy, and Maggs, 2005; Chavanich et al., 2006; Mc Donald et al., 2015) or due to other factors such as depth, size of plants, plants flexibility, morphology and sea state conditions (Gaylord, Blanchette, and Denny, 1994; Gaylord and Denny, 1997). In contrast to HB and FB, the dominance of coralline algae at MV might be due to further habitat complexity that supported grazers (i.e. sea urchins and herbivorous fishes). There is evidence of the dominance of crustose corallines in areas grazed by sea urchins (John, 2012; Steneck, 1986). Furthermore, the physical anti-fouling effects and chemicals produced by coralline algae also inhibit the growth of other algae (Boas and Figueiredo, 2004; Vermeiji, Dailer, and Smith, 2011). Effects of habitat, currents, and topography on distribution patterns and shading caused by macroalgae (Kelps) and Sargassum species are reported from different localities (Druehl and Green, 1982; Steneck, 1986, Seymour, et al., 1989; Jenkens, Norton, and Hawkins, 1999 a; Jenkins, Hawkins, and Norton, 1999 b; Britton-Simmons, 2004; Thakur, Reddy, and Bhavanath, 2008). Nutrients certainly control the growth of marine algae (Larned, 1998; Harrison and Hurd, 2001; Juneja, Ceballos, and Murthy, 2013; Endo et al., 2015). Comparatively low algal diversity at CI might be due to low nutrient concentrations and grazing effects. Nutrients and herbivore have synergistic affects on seaweeds (Miller and Hay, 1996).

Changes in community structure and stunted growth of Sargassum species, particularly at HB and FB, after the cyclone “NILOFAR” might be due to prologed effect of cyclone on sea surface water conditions caused by the generation of high energy winds. As a

73 result, Sargassum species could not grow at their seasonal optima. The availability of sufficient light due to stunted growth of Sargassum species permitted Dictyota and other species to grow out. Light enhances the growth of Dictyota species more than nutrients (Cronin and Hay, 1996). Increase in the growth of epiphytic alga (Ceramium sp.) at MB was possibly due to increase in the growth of coralline algae. There is evidence of the increase of the biomass of epiphytic algae by increasing the growth of sea grass and coralline algal communities (Borowitzka, Lethbridge, and Charlton, 1990). Incidences of the effects of physical disturbance on coralline algae are reported from different parts of globe (Steneck, 1986).

Rich algal growth along the Sindh coast of Pakistan was also reported during the winter monsoon compared to the summer monsoon by Hameed and Muzamal, (1999). High growth during the winter monsoon may be due to nitrate fluctuation caused by convective mixing and up-sloping (Wiggert et al., 2000), accompany with low water temperature and settled surface waters conditions due to dry and moderate winds moving in a southwesterly direction. During the summer monsoon, there was a decline in algal growth due to high-energy waves, generated by strong winds and warm climate (Weller et al., 1998; Tomczak and Godfrey, 1994; Schoot and McCreary Jr., 2001; Wiggert et al., 2000). Temperature surely effects the algal growth rate, biochemical composition, cell size and nutrient requirements (Renaud et al., 2002; Harley et al., 2012) and alters other physical parameters such as salinity and pH (Marinho-Soriano, 2012).

Sargassum species were widely distributed in near and offshore waters especially at HB forming huge beds, as also reported from southern Iran (Hosseinim and Gharanjik, 2003; Noormohammadi et al., 2010: Noormohammadi, Baraki, and Sheidai, 2011) and Oman (Cordero, 1992). Comparing the macroalgal diversity with the other submerged studies undertaken in the region i.e. 42 species from southern Iran (Gharanjik, 2003), 27 species from Hallaniyat Islands and 50 species from Muscat area, Oman (Cordero, 1992; Wynne, 2001) 37 species from northern coasts of Persian Gulf, Bushehr Province (Dadolahi- Sohrab et al., 2012), 90 species from Jubail Marine Wildlife Sanctuary, Saudi Arabia (De Clerck and Coppejans, 1996), 88 species from Bahrain (Basson, Mohamed, and Arora, 1989), indicated that algal flora reported from coastal habitats along the Sind coast is quite good, given the relatively large scale studies in surrounding localities compared to the smaller size of our studies.

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There are considerable chances of increasing the algal diversity, if further underwater surveys on a larger scale are conducted in the coastal waters of Sindh, Pakistan as many submerged rocky habitats and Sargassum beds are still unexplored.

4.6. Threats and Recommendations

No anthropogenic threat currently observed to seaweed communities. Huge beds of Sargassum species were observed in submerged habitats along the Karachi coast. Sustainable use of Sargassum species and other algae (pharmaceutical industries, food and other industrial applications such as fodder, fertlizars, use in aquaculture, formaseutical etc.) can provide alternative source of livelihood for coastal communities and can reduce pressure on fisheries sector that is already under stress.

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Chapter 5

Quaternary Fossil Coral Communities in the Uplifted Strata along the Balochistan Coast of Pakistan: Understanding Modern Coral Decline in the Arabian Sea

This chapter has published as: Siddiqui, P. J.A., Ali, A., Bromfield, K. Iqbal, P. and Shoaib, N. (2011). Identification of fossil corals inhabiting an uplifted area of Ras Gunz near Jiwani, Balochistan, Pakistan. Pakistan Journal of Zoology. 43 (3), 523-527. Ali, A., Siddiqui, P.J.A., Bromfield, K., Khan, A.A., & Iqbal, P. (2017). Quaternary fossil coral communities in uplifted strata along the Balochistan coast ofPakistan: understanding modern coral decline in the Arabian Sea. Arabian Journal of Geosciences (Accepted).

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5.1. Abstract

Uplifted reefs due to being important palaeoclimate archives and a rich source of information on past physical and geochemical changes globally have become the centre of marine research. The uplifted fossil Quaternary coral communities of Jiwani and Gwadar are perfect places to study the palaeoclimatic and geological changes that have shaped the Balochistan coast. Studies on the palaeodiversity of corals along the Makran coast of Pakistan are lacking. In the present study, the samples collected using line intercept method from four uplifted sites (Balochistan coast: one at Gwadar, and three at Jiwani), were analysed.The relative distribution and diversity of Scleractinian fossil corals was determined, and the factors responsible for coral decline along Pakistan coast were compared with modern coral distribution and diversity. A total of 48 fossil coral species were recorded in nine families and 22 genera. High coral diversity was recorded in the uplifted landward sites of Jiwani and Gwadar headland. Terraces close to the shore at Jiwani had lower diversity. The corals seem to be Quaternary; most likely Pleistocene to Holocene. The modern fauna lacks many species recorded in the fossil community, thus suggesting a faunal turnover in diversity and redistribution of coral fauna which may be linked with past geological events and increasing anthropogenic pressure.

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5.2. Introduction

Uplifted reefs serve as important palaeoclimate archives (Felis and Patzold, 2003) and have great geologic and archaeological significance (Moursi, Hoang, and Fayoumy,1994; Walter et al., 2000).They are a rich source of information on: the past physical and geochemical changes; biological diversity over large temporal scales; and the response of living organisms to past and present climatic changes in their surroundings (Sepkoski, 1997; Gagan et al., 2000; Honisch et al., 2004; Pandolfi and Greenstein, 2007). Useful data on the significance and distribution of Quaternary corals is available on both the regional and global scales (e.g. Chappell, 1974; Newton, Mullins, and Gardulski, 1987; Dullo, 1990; Kora and Fattah, 2000; Moustafa et al., 2000; Pandolfi and Jackson, 2001; Bruggemann et al., 2004; Crabbe, Wilson, and Smith, 2006; Edinger et al., 2007; Greenstein and Pandolfi, 2008; El-Sorogy et al., 2013; Mossadegh et al., 2013; Pellissier et al., 2014).

The Makran coast of Pakistan is a part of Makran Subduction Zone (MSZ; defines a 900 km long area located in the southern part of Pakistan and Iran) (Fig.1.4) where the oceanic crust of the Arabian plate is being subduced northward below the Eurasian plate since at least the Cretaceous to the Recent, with a convergence rate of 4.2cmy-1 in east Makran and 4cmy-1in west Makran (White, 1982; Harmz, Cappel, and Frances,1984; Byrne, Sykes, and Davis, 1992; Burg et al., 2008). The 800 km Makran coast extends from NW of Karachi (Fig. 1.4) in the east to Gwatar Bay (Iranian border) in the west with a narrow tectonically active continental shelf (Haq, 1988; Ali and Memon, 1995; Mc Call, 1997). ). The principal geomorphic features of the Makran coast are cliffs, headlands, stacks, spits, terraces, raised beaches and mud volcanoes. Rocks exposed along the coast in the headlands, terraces and coastal cliffs are assemblages of sandstone and mudstone (Page et al. 1979; Ali and Memon 1995).

The tectonic and stratigraphic history of MSZ has been described by Harmz, Cappel, and Frances, (1984), and can be summarised as follows. As a result of jostling between the continental plates, complex geotectonic changes are divided into three significant stages relevant to this study: the middle Miocene, the late Miocene to middle Pliocene, and the middle Pleistocene to Recent. During the middle Miocene, the deposition of turbidites dominated. The late Miocene to middle Pleistocene was dominated by progradation of

78 the plains, shelf, slope and landward margin, as well as regional uplifting and folding. The middle Pleistocene to Recent phase was largely characterised by further uplift and faulting.

The climate of coastal areas of Pakistan is mainly dry to hyper dry (Salma, Rehman, and Shah, 2012), and is strongly affected by tropical cyclones, winter weather disturbances (cyclonic, anti-cyclonic, and meridonal) in the `Mediterranean Sea, reversal of the monsoon, and the cyclic migration of the Inter Tropical Convergence Zone (ITCZ). Yearly rain fall is less than 254 mm (Snead, 1968; Sheppard, Price, and Roberts, 1992; Djamali et al., 2010; Rojas et al., 2013). Historically, great variations in monsoon patterns, temperature, productivity, turbidity, sedimentation rates and upwelling have been noted for the Arabian Sea. Overall, the monsoon was characterised by large temporal scale changeability. The south-west monsoon was stronger during Interglacial and weakest during the last Glacial Maximum (Tiwari, Singh, and Ramesh, 2011). During the glacial periods Marine Isotope Stage MIS 3 and MIS 8, sea surface temperatures were lower than during interglacial periods (ten Haven and Kroon, 1991). Productivity and turbidity in the Arabian Sea were high during MIS 13 and possibly associated with the beginning of a harsh meridional overturning circulation in the Atlantic Ocean at the end of the middle Pleistocene (Gupta, 1999; Prins, Postma, and Weltje, 2000; Ziegler, Tuenter, and Lourens, 2010).The sedimentation rate in the Arabian Sea (northern Arabian Sea) was 1.2 mm/yr for the last 5000 years (Prins and Postma, 2000).

The uplifted Jiwani and Gwadar areas are perfect places to study Quaternary coral communities with respect to the palaeoclimatic and geological changes that have shaped the Balochistan coast of Pakistan. No significant studies have previously been undertaken in this area other than by Crame (1984) and Siddiqui et al. (2011). Crame (1984) and Ali and Memon (1995) reported the presence of Neogene and Quaternary molluscs and corals embedded in different lithostratigraphic units, but no taxonomic details were provided; and Siddiqui et al. (2011) reported only 14 fossil coral species from uplifted reefs at Ras Gunz near Jiwani (see Table 5.1). Duncan (1880) reported 55 Miocene corals from Sindh province of Pakistan. Studies on the palaeodiversity of corals along the Makran coast of Pakistan are lacking, and this is one of the first studies of its kind in the region. Previous studies (Siddiqui et al., 2011; Ali et al., 2014) showed that

79 modern fauna lacks many species recorded in the fossil community. The present study was carried out to further explore and compare recent and fossil coral distribution and to discuss the changes in coral communities with respect to the past geological history and increasing anthropogenic pressure in recent time.

5.3. Materials and Methods

The details abiut materials and methods is included in chapter 1 (section 1.2)

5.3.1. Geological description of sites 5.3.1.1. Gwadar headland The Gwadar headland is located ~543 km west from Karachi. The northern side of the headland is composed of thick shell and coquina beds, deposited in 15 to 20 m thick massive mudstone units. The upward trending lithologies are a succession of pebbly sandstones transitioning upwards to fine sands, interbedded with coquinas and conglomerates. The Gwadar headland is a part of the Gwadar Formation (20,000 and 30,000 yrs; Kazmi and Jan, 1997) which extends eastward up to the Hingol River and to Jiwani in the west with variable thickness (Crame, 1984).

5.3.1.2. Jiwani The Jiwani is located about 720 km from Karachi on the Balochistan coast of Pakistan and 60 km from Gwadar towards the west, close to the border of Iran. Folding, faulting and elevated terraces, possibly late Pleistocene time, are the major features of the formation (Hussain, Butt, and Pervaiz, 2002).The formation is largely comprised of porous shell fragments, hard and pebbly shale and limestone deposited in mudstone, interbedded with a conglomerate of rounded sandstone, pebbles, cobbles, limestone and red jasper, with bedding up to 3 m. The colour is mostly greyish brown to dark ferruginous brown. This study site is part of Jiwani Formation generally confined to the southern part of the Makran division (Hunting Survey, 1961; Crame, 1984; Shah, 2009). The formation is considered as younger extending from late Pleistocene to Holocene (Crame, 1984; Raza, Ahmed, and Ali, 1991) compared to Gwadar Formation.

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5.4. Results 5.4.1. Description of survey sites General features of the sites, GPS position and elevation of sites from main sea level are included in Table 1.3.

5.4.2. Fossil corals A total of 48 species of fossil corals belonging to 9 families and 22 genera (Table 5.2; Fig. 5.1 A-B) were recorded during this study. Among these, 18 were identified to species level, 25 up to genus level due to the loss, during burial and diagenesis, of many characters used in identification while 5 species could indentified with certainaty. The landward sites (J2, J3) had high diversity and density, compared to GH and the shoreward site J1.

Skeletal comparison of fossil and modern corals showed slight difference between corallites morphology (Fig. 5.2). Bioeroding effects were found high in fossil corals (Fig.5.3). A cluster analysis of the coral communities at all sites showed that J2 (4) and J3 (2), J2 (2) and J2 (3), J2 (1) and J3 (1) and J1 and J2 (5) formed well defined clusters at a similarity levels of about 55%, 65%, 67% and 40 % while GH formed a separate cluster at a similarity level of about 45% respectively (Fig. 5.4). K. dominance curves specified that species-frequency is high at J3 (1) followed by J2 (1), J2 (2), GH, J2 (3), J3 (2), J2 (4), J2 (5) and J1 (Fig. 5.5).

Comparing fossil coral fauna with modern distribution (Table 5.3) indicated that diversity was high in the past (Pleistocene) in comparison with recent coral fauna suggesting a faunal turnover in coral fauna. For example, Faviidae and Acroporidae are well represented in the fossil fauna but show considerable extension. On the other hand Poritidae, not abundant in the fossil fauna, is common in the recent fauna (Ali et al., 2014). Comparison between species and genera composition between three communities showed that for species composition, the Quaternary communities showed a higher similarity to Miocene communities (southern Iran) at a similarity level of about 42% than to the modern coral communities of Pakistan (Fig. 5.6). Regarding genera composition,

81 the Quaternary coral communities were more similar to modern coral communities at a similarity level of about 50 % than to the Miocene communities (Fig. 5.7).

Table 5.1. List of fossil corals collected from an uplifted location at Ras Gunz near Jiwani, Balochistan. Taxa with a question mark were not identified with certainty. From Siddiqui et al., (2011).

Species Family Favia truncatus? Faviidae Favia lizardensis Faviasp.1 Favia sp. 2 Favia sp.3 Favia sp.4 Favites cf. acuticollis Favites sp. Goniastrea cf. retiformis Platygyra daedalea Cladocora cf. caespitosa Cyphastrea serailia Astreopora sp. Acroporidae Acropora sp.

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Table 5.2. List of fossil corals collected from uplifted strata at Gawadar (GH) and Jiwani (J1, J2, along Balochistan coast of Pakistan. Values are relative abundance based on number of individual of each species in a sample.

Fossil corals GH J1 J2 J3

J2 (1) J2 (2) J2( 3) J2 (4) J2 (5) J3 (1) J3 (2) Family: Faviidae Blastomussa sp. 5 3 2 2 Caulastrea sp. 2 2 Cyphastrea hexasepta 2 1 Cyphastrea sp. 1 1 2 Cyphastrea sp. 2 1 Cyphastrea sp.3 1 Echinopora sp. 2 Favites complanata 1 4 2 3 3 2 2 3 3 Favites spinosa 2 4 1 3 Favites cf. abdita 1 1 2 Favites cf. chinensis 2 2 Favia pallida 2 4 2 3 4 4 Favia speciosa 2 4 2 3 2 4 2 Favia favus 2 4 2 3 1 4 2 Favia sp. 1 4 3 Favia sp. 2 4 2 2 3 Goniastrea columella 1 Goniastrea aspera 2 4 2 2 Goniastrea sp. 2 3 3 Leptastrea transversa 2 Leptastrea sp. 2 Platygyra pini 2 2 2 2 3 1 Platygyra sinensis 2 3 2 2 2 1 2 1 Plesiastrea versipora 1 1 Family: Acroporidae Acropora sp. 1 2 Acropora sp. 2 1 1 1 Acropora sp. 3 1 1 Acropora sp. 4 1 1 1 1 Astreopora sp.1 1 Astreopora sp. 2 2 Astreopora sp. 3 1 Astreopora sp. 4 1 Family: Pociloporidae Pocillopora damicornis 2 1 Pocillopora verrucosa 1 1 1 1 Pocillopora cf. eydouxi 1 Stylophora pistillata 3 2 2 2 1 Family: Poritidae Porites sp. 1 1 Porites sp. 2 2 Goniopora sp. 1 1 Goniopora sp. 2 1 1 Family: Merulinidae Hydnophora exesa 3 1 1 1 Hydnophora microconis 2 1 Family: Dendrophyliidae Turbinaria sp. 1

Continued… 83

Family: Fungiidae Cycloseris sp. 1 Fungia sp. 1 Family: Musidae Acanthastrea hillae 1 Acanthastrea cf. echinata 1 Family: Agaracidae Leptoseris cf. mycetocoides 1 Total species 18 2 30 18 11 5 3 31 10

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Table 5.3. List of families and genera of Quaternary and modern corals recorded in uplifted strata of Balochistan and coastal waters. Numbers of species found in each genus are also shown. A significantly high diversity is evident from Quaternary period compared to currently recorded live coral species.

Family/Genera Quaternary Status1 Current status2

Family: Faviidae Blastomussa spp. 1 Cladocora spp. 1 Caulastrea spp. 1 Cyphastrea spp. 5 1 Echinopora spp. 1 Favites spp. 6 4 Favia spp. 11 Goniastrea spp. 4 4 Leptastrea spp. 2 3 Platygyra spp. 3 Plesiastrea sp. 1 1 Family: Acroporidae Acropora spp. 5 Astreopora spp. 5 Montipora spp. 1 Family: Pociloporidae Pocillopora spp. 3 1 Stylophora spp. 1 Family: Poritidae Alveopora spp. 1 Porites spp. 2 11 Goniopora spp. 2 8 Family: Siderastreidae Coscinaraea spp. 3 Psammocora spp. 5 Pseudosiderastrea spp. 1 Family: Merulinidae Hydnophora spp. 2 Family: Family:Dendrophyliidae Dendrophyllia spp. 1 Turbinaria spp. 1 1 Family: Fungiidae Cycloseris spp. 1 Fungia spp. 1 Family: Musidae Acanthastrea spp. 2 2 Family: Agaracidae Leptoseris spp. 1 Pavona spp. 1 Family: Euphyllidae ?Physogyra sp. 1 Total species 62 50

1Numbers of fossil corals also includes species that have been mentioned in Siddiqui et al., (2011) 2Numbers of live coral species also includes species that have been mentioned in Ali et al., (2014).

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Figure 5.1 A. Diversity of fossil corals recorded from uplifted strata at Jiwani and Gwadar along Balochistan (Makran) coast, Pakistan.1) Blastomussa sp.; 2) Caulastrea sp.; 3) Cyphastrea hexasepta; 4) Cyphastrea sp. 1; 5) Cyphastrea sp. 2; 6) Cyphastrea sp. 3) 7) Echinopora sp.; 8) Favites complanata; 9) Favites spinosa; 10) Favites cf. abdita; 11) Favites cf. chinensis; 12) Favia pallida; 13) Favia speciosa; 14) Favia favus; 15) Favia sp. 1; 16) Favia sp. 2; 17) Goniastrea columella; 18) Goniastrea aspera; 19) Goniastrea sp.; 20) Leptastrea transversa; 21) Leptastrea sp.; 22) Platygyra pini; 23) Platygyra sinensis; 24) Plesiastrea versipora.

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Figure 5.1 B. Diversity of fossil corals recorded from uplifted strata at Jiwani and Gwadar along Balochistan (Makran) coast, Pakistan. 25) Acropora sp. 1; 26) Acropora sp. 2; 27) Acropora sp. 3; 28) Acropora sp. 4; 29) Astreopora sp. 1; 30) Astreopora sp. 2; 31) Astreopora sp. 3; 32) Astreopora sp. 4; 33) Pocillopora damicornis; 34) Pocillopora verrucosa; 35) Pocillopora cf. eydouxi; 36) Stylophora pistillata; 37 Porites sp. 1; 38) Porites sp. 2; 39) Goniopora sp. 1; 40) Goniopora sp. 2; 41) Hydnophora exesa; 42) Hydnophora microconos; 43 Turbinaria sp.; 44) Cycloseris sp.; 45) Fungia sp.; 46) Acanthastrea hillae; 47) Acanthastrea cf. echinata; 48) Leptoseris cf. mycetocoides.

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Figure 5.2. Comparison of modern corals (a, c, e, g) collected from coastal waters with fossil corals (b, d, f, h) from coastal uplifted strata (Makran, Balochistan), Pakistan. a- b Favites species, c- d Leptastrea species, e- f Cyphastrea species, g - h Porites species.

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Figure 5.3. Comparison of modern Porites species (a,b) collected from coastal waters with fossil Porites species (c,d) collected from coastal uplifted strata (Makran, Balochistan), to check the effects of bioerrosion

Figure 5.4. Cluster analyses of similarities between fossil coral community composition at 9 transacts, based on presence-absence data and Bray–Curtis similarities. JI: Jiwani site 1, J2 (1-5): Jiwani site 2 (1-5), J3 (1-2), Jiwani site 3 (1-2), GH: Gwadar headland.

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Figure 5.5. K. dominance curves (a: cumulative dominance, b: partial dominance) for fossil coral communities at 9 transacts following Lambshead, Platt, and Shaw, (1983). Abbreviations are same as in Figure 5.

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Figure 5.6 Cluster analyses of species composition of Quaternary, modern and Miocene coral communities based on presence -absence data and Bray–Curtis similarities.

Figure 5.7. Cluster analyses of genera composition of Quaternary, modern and Miocene based on presence-absence data and Bray–Curtis similarities based on presence absence data and Bray–Curtis similarities.

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5.5. Discussion The term ‘Quaternary communities’ was assigned on the basis of different studies conducted on sediments and palaeo diversity (Crame, 1984; McCall, Rosen, and Darrell, 1984; Hosseini-Barzi and Talbot, 2003; Hosseini-Barzi, 2010; Kober et al., 2013) in southern Iran and coastal Makran (Pakistan). Proper dataing of the strata from the coral sites is however required. A variety of factors influence coral growth, among them thermal stress (Warner, Fitt, and Schmidt, 1996; Mc Clanahan, 2004; Mc Clanahan et al., 2007; Coles, 2008; Crabbe, 2008; Munday, McCormick, and Nilsson, 2012; Weber et al., 2012; Roth and Deheyn, 2013; Mumby et al., 2014; Bozec and Mumby, 2015), and sedimentation load (Rogers, 1990; Riegl, 1995; Erftemeijer et al., 2012; Bartley et al., 2014; Junjie et al., 2014; Perez 111 et al., 2014; Jones, Ricardo, and Negri, 2015) are important. However, many species of corals have some adaptations that enable them to cope with such stressors to a critical level (Sanders and Baron-Szabo, 2005; Bellantuono et al., 2012; Doney et al., 2012; Erftemeijer et al., 2012). Anthropogenic impacts also play a key role in the decline of corals across the globe (Edinger, Pandolfi, and Kelley, 2001; Pandolfi, 2002; Pandolfi et al., 2003; Hughes et al., 2003; Chabanet et al., 2005; Pandolfi and Jackson, 2006; Halpern et al., 2008; Hughes et al., 2010; Bellwood, Hoey, and Hughes, 2012; Jackson et al., 2013; Edwards et al., 2014). Large number of boring holes and imprints of organisms on fossil corals are indications that fossil corals existed in a nutrient rich environment. According to Klein, Mokady, and Loya, (1991), primary productivity levels were high in Red Sea during late Quaternary as high numbers of eroding organisms were found in fossil records.

High coral diversity at landward sites might be due to less turbid environment. According to Prins et al., (2000) and Luckge et al., (2001), fluvial input increased between 5000 to 3000 years BP due to climatic and hydrological changes in this area. Lithogenic fluxes derived from the Makran were highest during the Pleistocene and the sediment load increased as a result of uplifting and sea level fluctuations. Sedimentation rates during the Holocene were high in deeper parts of the Arabian Sea and on the upper continental slope during the last Glacial Maximum and remained high during the whole deglaciation (von Rad et al., 1999; Prins, Postma, and Weltje, 2000). Skeletal comparison indicated the presence of healthy environment as no signs of sediment stress was observed possibly due to the existence of Pleistocene corals for a short period of

92 time (Edinger and Risk, 1994). The size of a corallite is affected by sediment stress that ultimately affects septal growth (Ketcher and Allmon, 1993). Globally, some Pleistocene events made the environment less favourable for corals (Bromfield and Pandolfi, 2012), although there were also periods of vigorous reef growthin the inter-glacials.

Comparing fossil coral fauna with modern distribution indicated a disappearance of some genera in the modern fauna. Among the faviids, the apparent disappearance of Favia and Platygyra from contemporary coral communities is interesting as some species in each genus are known to tolerate high sedimentation environments by virtue of having large calices (>10 mm), which help in rejecting sediment more easily than species with smaller calices (Stafford-Smith and Ormond, 1992; Xiu Bao et al., 2013). Individual species of coral can tolerate sediment stress up to critical levels, and there are contradictory tolerances among species (Fabricius, 2005). Acroporidae has less ability to tolerate turbid conditions than Faviidae and Poritidae (Riegl, 1999), which may explain why it is not found in modern fauna. Communities with higher sediment tolerance are known to replace coral communities composed of species with lower sediments tolerance (Xiu Bao et al., 2013), and this partially explains the faunal turnover observed on the Makran coast. Today, species of Poritidae (20 species) dominate coral fauna of Pakistan followed by Faviidae (14 species) and Siderastreidae (9 species), a fact also noted from other places in the Arabian Sea (Wilkinson, 2004); whereas Acroporidae were under represented (Coles, 2003). A gradual increase in sediment load due to frequent geological events may have caused replacement of corals having less sediment tolerance by more tolerant species. Similar changes have been seen in the Persian Gulf where Platygyra species were recorded as dominant during MIS 7.5 and MIS 7.1 at Kish Island, but are not prevalent in the modern coral fauna (Mossadegh et al., 2013). The hard coral diversity and distribution during their evolution to emerging modern forms appear to be linked with environmental and geological settings. Solitary and small to medium size corals (with corallites 3 to 8 mm) were dominant in turbid environments, while solitary and medium to large size (with corallites8 to 15 mm) remained the characteristic of clear water conditions (Flugel, 1982; Kiessling, Flügel, and Golonka, 1999; Dupraz and Strasser, 2002; Flugel, 2002; Flugel and Kiessling, 2002; Leinfelder et al., 2002; Perrin, 2002; Wilson and Lokier, 2002; Stanley, 2003; Olivier et al., 2004; Sanders and Baron- Szabo, 2005).

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Sedimentation is a continuous process along Makran coast and is a feature of dynamic plate margins (Prins and Postma, 2000; Prins, Postma, and Weltje, 2000; Schluter et al., 2002; Grando and McClay, 2007; Mouchot et al., 2010; Haghipour et al., 2012).

Tectonic factors may also be responsible for habitat destruction in the waters of Makran (Balochistan) coast. Abundant and active mud volcanoes on and offshore in coastal areas of Makran are reported at Haro Range, Chandragup area (Ormara), and in the vicinity of Gwadar. As a result of these eruptions, numerous ephemeral islands have appeared, and some have survived, e.g. Khandwari Mud Volcano, though many of these have disappeared due to strong wave action (Hunting Survey, 1961; Snead, 1964; Wiedicke, Neben, and Spiess, 2001; Delisle et al., 2002; Schluter et al., 2002; Delisle, 2004; Grando and Mc Clay, 2007; Kassi et al., 2014). A recent example is the emergence of a new island in 2013, near Gwadar, that also caused the uplift of hard and soft corals (see Kumar, 2014). Meanwhile, human impacts (industrial and domestic pollution, high sedimentation load due to coastal development, overfishing, spear fishing, boat anchor damage, and habitat loss due to the sale of broken coral) due to rapid urbanization along the coast could be another factor responsible for coral deprivation. Tectonic factors also play a key role in generating biodiversity spots (Renema et al., 2008). Arabian Peninsula including Pakistan remained a hot biodiversity spot including corals during the Eocene period. Habitat destruction caused by past geological events in the area, for example collision of Arabian and Eurasian plate during middle to late Miocene shifted biodiversity from this region (Kay, 1996; Harzhauser et al., 2007; Renema, 2007). Further Pleistocene changes such as formation of numerous palaeoshorelines, sedimentary sequence, habitat loss and changes in environmental settings on regional and global scale have occurred during sea level lowering stage (Lambeck, 1996; Pandolfi, 1999; Banerjee, 2000; Prins and Postma, 2000; Bruggemann et al., 2004; Kusky, Robinson, and El- Baz, 2005; Gharibreza and Motamed, 2006; Mossadegh et al., 2013; Pain and Abdelfattah, 2015). It might be possible that changes (reduction in continental shelf, habitat destruction, transition from sheltered to open water conditions) occurred gradually, thereby making the environment less favourable for corals, not only along the coast of Pakistan, but along the shores of Arabian Sea as a whole. Today in the Arabian Sea, reef or proto-reef assemblages are mostly confined to sheltered embayment or on the leeward sides of islands (Sheppard and Salm, 1988; Coles, 2001; Wilson et al.,

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2002, Ali et al., 2014) where water is less turbid (Sheppard, Price, and Roberts, 1992; Hearn, Atkinson, and Falter, 2001).

Comparing Pakistan's fossil fauna with Miocene corals reported from mountain range of southern Iran by McCall, Rosen, and Darrell, (1984), indicated that Pakistani fossil fauna, of atleast 62 species, was quite rich, although less than the 90 species reported from the Iran. However, the spatial scale of the Iran study was quite large compared to this report. This also indicates that fossil coral fauna reported form uplifted strata along Balochistan coast of Pakistan is likely to be much younger and existed in a less turbid environment as most of the Miocene fauna has been extinct and existed in turbid or calm water conditions (Edinger and Risk, 1994; McCall, Rosen, and Darrell, 1984). The fossil corals reported in this study are most likely Late Pleistocene in age and could form a part of the expansion of Indian Ocean coral reefs occurred during the start of upper Pleistocene (Hopely, 1982; Crame, 1984). During recent years, several events of coral mass mortality occurred in Arabian Sea and the adjacent Red Sea, mainly due to thermal, anthropogenic and natural stresses (DeVantier et al., 2000; DeVantier et al., 2004; Bauman et al., 2010; Bruke et al., 2011; Foster et al., 2011; Riegl et al., 2012; Bauman et al., 2013; Burt, 2014; Coles, Looker, and Burt, 2015). Similarly, many species occur in deeper depths and further investigation of a wide area and depth range are necessary before the absence of Acropora and other genera can be confirmed with more certainty. Regarding this, additional detail studies on a large scale in uplifted strata along the coast and in submerged habitats with emphasis on environmental, anthropogenic and geological parameters are recommended.

5.6. Threats and Recommendations

Like live corals, recent rapid urbanization along whole coast of Pakistan poses serious threats to fossil corals through breaking/damaging corals and destruction of their habitat. A large number of fossil corals from uplifted strata at Jiwani have already been removed by the local community for the construction of houses. Fossil corals serve as time capsules. It is highly recommended that there should be complete ban on illegal collection of fossil corals on large scale. .

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Chapter 6

General Discussion

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General Discussion

The study deals with distribution pattern and diversity of hard corals and their associated communities in submerged habitats along the Sindh coast and paleo diversity of hard corals in uplifted strata along the Balochistan (Makran) coast of Pakistan. Overall, 183 taxa were recorded belonging to three major groups i.e. invertebrates, vertebrates and seaweeds. Among them 21 were live corals, 48 fossil corals, 13 molluscs, 3 sea anemones, 3 sponges, 3 echinoderms, 2 crustaceans, 54 fishes and 36 macroalgae. No recorded species of coral was found endemic to the Pakistan coast; however, there are four potential candidates, Physogyra species, one species of Goniastrea, one species of Porites and one species of Goniopora might be new species. Recent surveys and a study conducted by Ali et al., (2014), indicated that proto-reef formation appeared in waters off the coastal areas, particularly at northern sheltered sides of Astola (Balochistan coast) and Churna (Sindh coast) Islands, whereas poor coral growth was observed in coastal environments. Corals in these environments were mostly patchily distributed with Porites dominating. Diverse hard coral communities at northern sheltered sites of both Islands might be due to their considerable distance from coast, presence of hard substrate for coral attachment, less turbid water conditions and perhaps fewer nutrients, so that macroalgae do not outcompete corals. The water currents in such environments are considerably high that helps solar heating to higher water temperature (Sheppard et al., 1992). Poor coral cover in coastal habitats is mainly due to high wave action that stirs up sediment, leading to highly turbid conditions (Personal observations). Further, the coastal waters seemed to be nutrient rich with dense green phytoplankton blooms also leading to very poor visibility thus preventing zooxanthellae from photosynthesizing. Moreover the polyps of many hard coral species easily become clogged by settlement of suspended sediment, and therefore are not well adapted to survive in turbid environments (Rogers, 1990; Philipp and Fabricius, 2003; Fabricius, 2005).

The majority of fossil coral fauna collected from uplifted strata possibly of late Pleistocene period appeared to more diverse coral community with majority having large size corallites (8-16 mm) suggest less turbid environment during that period. Hard coral distribution and diversity, from evolutionary to emerging modern forms, appear to be linked with environmental and geological settings. For example, corals with 3 to 8 mm corallites were dominant in turbid environments, while solitary and medium to large size

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(with corallites 8 to 15 mm) were more characteristic of clear water conditions (Flugel, 1982; Kiessling, Flügel, and Golonka,1999; Dupraz and Strasser, 2002; Flugel, 2002; Flugel and Kiessling, 2002; Leinfelder et al., 2002; Perrin, 2002; Wilson and Lokier, 2002; Stanley, 2003; Olivier et al., 2004; Sanders and Baron-Szabo, 2005). The further Pleistocene events (glaciations) made the environment less favourable for corals (Bromfield and Pandolfi, 2012).

Comparing the modern coral fauna recorded in this study and previously by Ali et al., (2014) with fossil coral fauna indicates that diversity was higher in the past (Pleistocene) suggesting a faunal turnover in coral fauna. This turnover, an ongoing process, presumably has occurred many times in geological time, notably during the repeated glacial and inter-glacial cycles of the Pleistocene epoch. For example, Faviidae and Acroporidae are well represented in the fossil fauna but show considerable local extinction in modern fauna. On the other hand, the family Poritidae, not abundant in the fossil fauna, is commonly represented in the recent fauna. This appears to be the function of geological changes (i.e., formation of numerous palaeo-shorelines, sedimentary sequence, habitat loss and changes in environmental settings) occurred during sea level lowering stage (last glacial/inter glacial period) on regional and global scale (Lambeck, 1996; Pandolfi, 1999; Banerjee, 2000; Prins and Postma, 2000; Bruggemann et al., 2004; Kusky, Robinson, and El- Baz, 2005; Gharibreza and Motamed, 2006; Mossadegh et al., 2013; Pain and Abdelfattah, 2015). It might be possible that changes (reduction in continent shelf, habitat destruction, transition from sheltered to open water conditions) occurred gradually, thereby making the environment less favourable for corals, not only along the coast of Pakistan, but along the shores of the Arabian Sea as a whole. Similar changes occured in the Persian Gulf where Platygyra species were recorded as dominant during MIS 7.5 and MIS 7.1 at Kish Island, but is not prevalent in modern corals (Mossadegh et al., 2013). Tectonic factors may also be responsible for habitat destruction along Balochistan (Makran) coast. Abundant and active mud volcanoes on and offshore in coastal areas of Balochistan are reported at Haro Range, Chandragup area (Ormara), and in the vicinity of Gwadar. As a result of these eruptions, numerous ephemeral islands have appeared, and some have survived, e.g. Khandwari Mud Volcano, though many of these have disappeared due to strong wave action (Hunting Survey, 1961; Snead, 1964; Wiedicke, Neben, and Spiess, 2001; Delisle et al., 2002; Schluter et al., 2002; Delisle, 2004; Grando and Mc Clay, 2007; Kassi et al., 2014). A

98 recent example is the emergence of a new island in 2013, near Gwadar, that also caused the uplift of hard and soft corals (see Kumar, 2014). From 1668 to date at least 28 earthquakes have been occurred in this area with a magnitude of 7 or greater than 7 (Ambrasseys and Bilham, 2003). Among them, the earthquake of 1945 with a magnitude of 8.1, occurred in the northern Arabian sea about 100 km south of Karachi largely destroyed the underwater habitats. Eruption of mud volcano occurred few miles away from Makran coast. Also 4 new islands are formed as a result of this eruption (Times of India, 1945; Wadia, 1981; Pacheco and Sykes, 1992; Pararas-Carayannis, 2006). Tectonic events played a major role in shifting biodiversity hotspots. Arabian Sea region including Pakistan remained a rich biodiversity spot till late Eocene. Depletion of this fauna was mainly due to habitat destruction caused by uplifting events due to collision between Arabian and Eurasian plates during middle to late Miocene. As a result of habitat destruction, the biodiversity shifted towards Indonasia and Australian region (Kay, 1996; Harzhauser et al., 2007; Renema, 2007). Studies indicated that biodiversity loss as a result of tectonic events is comparatively large than damage caused by tsunami and cyclones. A study conducted in Indonesia after the earthquake of 2004, indicated that physical damage to corals due to earthquake was quite large than the damage caused by tsunami (Foster et al., 2006).

Today, species of family Poritidae dominate coral fauna of Pakistan followed by Faviidae and Siderastreidae, a fact also recorded from other locations in the Arabian Sea (Wilkinson, 2004); whereas Acroporidae were under represented (Coles, 2003). A gradual increase in sediment load due to frequent geological events may have caused replacement of corals having less sediment tolerance by the tolerant species. Sedimentation is a continuous process noted along the Balochistan (Makran) coast of Pakistan and is a result of dynamic plate margins (Prins and Postma, 2000; Prins, Postma, and Weltje 2000; Schluter et al., 2002; Grando and McClay, 2007; Mouchot et al., 2010; Haghipour et al., 2012). According to Prins et al., (2000) and Luckge et al., (2001), fluvial input increased between 5000 to 3000 years BP due to climatic and hydrological changes in this area. Lithogenic fluxes derived from the Makran were highest during the Pleistocene and the sediment load increased as a result of uplifting and sea level fluctuations. Sedimentation rates during the Holocene were high in deeper parts of the Arabian Sea and on the upper continental slope during the last Glacial Maximum

99 and remained high during the whole deglaciation (von Rad et al., 1999; Prins, Postma, and Weltje, 2000).

The major constraints observed regarding reef development in Pakistan includes nutrient rich water, poor visibility, sediment load, lack of hard substrate and swere wave action. Variations in thermal stress and salanaties are not too much high and low comparing to surrounding locations (Oman, Arabian-Persian Gulf etc) where temperature and salanities fluctuations are extremely high and low. Moreever, recent rapid urbanization along whole coast of Pakistan poses threats to corals through breaking/damaging corals and destruction of their habitat. Large scale removal of corals (live and fossil) has been observed for sale as ornaments and construction of houses, etc. A large number of fossil coral colonies from uplifted strata at Jiwani has already been removed by the local community. Similarly, Acropora and some other genera are not represented in the modern coral setting. This may be attributed to the fact that many of them grow in deeper waters and the current surveys have been restricted to the shallow depths. Further investigations covering wider area and depth ranges are required before the absence in the modern setting of Acropora and other genera can be confirmed with more certainty. Also the events of coral mass mortality during recent years have been recorded in Arabian Sea including Red Sea mainly due to thermal, anthropogenic and natural stresses (Bauman et al., 2010; Bruke et al., 2011; Foster et al., 2011; Riegl et al., 2012; Bauman et al., 2013; Burt, 2014; Burt et al., 2016; Coles, Looker, and Burt, 2015). Thermal stress is considered as a serious threat to corals than ocean acidification. Incidents of coral degredation as a result of thermal stress has been reported both on regional and global scale. The bleaching event of 1996 has completely removed Acropora from shallow habitats in Bahrain. About two third of corals were bleached at a depth of 40 m at Bulthama reef and half of them died later (Wilkinson, 1998; Uwate and Shams, 1999; Al-Kuwari, 2006). During the bleaching incidents of 1996 and 1998, huge coral mass mortality occurred in Jebel Ali and Ras Hasyan (UAE). In 1996, coral cover reduced from 90% to approximately 26% whereas in 1998, the coral cover further reduced from 26% to 22%. During both incidents, the genus Acropora effected badly and the coral fauna reduced from 34 to 27 species (Riegl, 2002). Evidence of coral mass mortality was also reported from Red Sea. High mortality was reported from coastal areas than offshore waters particularly genus Acropora which is reportedly most effected by bleaching (DeVantier et al., 2000; Furby, Boumeester, and Berumen, 2013).

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For developing effective conservation strategy detail studies are desired on a large scale in uplifted strata and submerged habitats along the coast and in deeper waters with respect to climatological, environmental, anthropogenic and geological variations. Furthermore, coastal environment does not seem to favour coral growth, except for sheltered low energy areas, conservation of already existing coral sites is necessary. The local community and wider public may be involved in restoration work so that they can admire the importance of these natural resources. Development of artificial reef at suitable low energy submerged habitats would provide a chance for many species to grow. These reefs and natural coral sites (Churna and Astola Islands) may be used as sites for pleasure diving and for the promotion of ecotourism.

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