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Patterns of Coral Species Richness and Reef Connectivity in Malaysia Patterns of coral species richness and reef connectivity in Malaysia Waheed, Z. Patterns of coral species richness and reef connectivity in Malaysia PhD thesis, Leiden University Cover design: Yee Wah Lau Printed by: Gildeprint, Enschede ISBN: 978 94 6233 460 1 © 2016 by Z. Waheed, all rights reserved. Funding. This thesis was accomplished with financial support from the Ministry of Higher Education Malaysia, with additional support from Universiti Malaysia Sabah, WWF-Malaysia, the A.M. Buitendijkfonds, and TREUB-maatschappij (Society for the Advancement of Research in the Tropics). Disclaimer. Following the recommendation of Article 8.2 of the International Code of Zoological Nomenclature, I declare that this publication is not issued for public and permanent scientific record, or for purposes of zoological nomenclature, and therefore not published within the meaning of the Code. Patterns of coral species richness and reef connectivity in Malaysia Proefschrift ter verkrijging van de graad van Doctor aan de Universiteit Leiden, op gezag van de Rector Magnificus prof. mr. C.J.J.M. Stolker, volgens besluit van het College voor Promoties te verdedigen op dinsdag 22 november 2016 klokke 13:45 door Zarinah Waheed geboren te Kota Kinabalu, Maleisië in 1978 Promotiecommissie Prof. dr. L.M. Chou (National University of Singapore, Singapore) Prof. dr. M. Schilthuizen (Universiteit Leiden & Naturalis Biodiversity Center) Prof. dr. H.P. Spaink (Universiteit Leiden) Prof. dr. P.C. van Welzen (Universiteit Leiden & Naturalis Biodiversity Center) Dr. F. Benzoni (University of Milano-Bicoca, Italy) Dr. C.H.J.M. Fransen (Naturalis Biodiversity Center) Promoter Prof. dr. E. Gittenberger (Universiteit Leiden & Naturalis Biodiversity Center) Copromoter Dr. B.W. Hoeksema (Naturalis Biodiversity Center) For my parents Contents Chapter 1 General Introduction 9 Chapter 2 A tale of two winds: species richness patterns of reef corals 29 around the Semporna peninsula, Malaysia Chapter 3 Coral reefs at the northernmost tip of Borneo: an assessment of 49 scleractinian species richness patterns and reef benthos assemblages Chapter 4 Diversity patterns of scleractinian corals at Kota Kinabalu, 77 Malaysia, in relation to depth and exposure Chapter 5 Scleractinian corals (Fungiidae, Agariciidae and Euphylliidae) 97 of Pulau Layang-Layang, Spratly Islands, with a note on Pavona maldivensis (Gardiner, 1906) Chapter 6 Reef coral species richness gradient across Malaysia 129 Chapter 7 Connectivity of reef invertebrate populations in Malaysia: 161 perspectives of a mushroom coral, a blue seastar and a boring giant clam References 193 Affiliation of co-authors 219 Summary 221 Nederlandse samenvatting 225 Ringkasan Bahasa Malaysia 229 Acknowledgements 233 Curriculum vitae 235 Publications 237 Chapter 1 General Introduction Reef corals Coral reefs are among the most productive ecosystems on earth. They provide goods and services to millions of people worldwide, directly or indirectly, in the form of food, coastline protection, tourism, pharmaceuticals, and other sources of income (Moberg and Folke 1999, Wilkinson 2008). They also have recreational and cultural importance for local communities. Shallow tropical coral reefs have much value as habitat, providing shelter to innumerable marine species, making them the most species-rich marine ecosystem in the world. Hard corals (Scleractinia) form the backbone of tropical coral reefs. They are the main builders in the reef ecosystem, which supports the wealth of marine biodiversity. Naturally, the corals themselves also contribute to this diversity. Hard coral is composed of an individual polyp or a group of polyps that live together to form a coral colony. The ability of hard corals to build reefs stems from their symbiotic relationship with unicellular algae, zooxanthellae of the genus Symbiodinium. The photosynthesizing zooxanthellae, which live within the coral tissue, influence the growth rate and calcium carbonate (CaCO3) deposition of corals. The success of building and maintaining the three-dimensional reef structures relies on environmental parameters such as light, temperature, and nutrient levels (Barnes and Chalker 1990; Falkowski et al. 1990; Atkinson 2011; Dubinsky and Falkowski 2011). Equally important is the coral resilience to competition, and disturbance or stress of natural or anthropogenic origin. Most hard corals are colonial. Many coral species can easily be identified in situ, whereas others exhibit a wide range of morphological variation and plasticity, which makes their identification difficult (Veron 1995; Todd 2008). Such variation in coral appearance can be in the form of 1) corallite variation within a coral colony, usually in different parts of the colony, 2) colony growth form due to different environmental conditions such as depth or proximity to land, 3) coral colony variation between regions, most likely related to environmental gradients, genetic isolation, or a combination of these factors, and 4) soft tissue variation, such as in corals with fleshy polyp tissue, like Euphyllia, Plerogyra and Physogyra (see Veron 1995). In recent times, coral taxonomy has moved beyond using solely morphological characters for defining species boundaries. Increasingly frequent, molecular data and additional micro-morphological/microstructure traits are applied to support new species descriptions (Benzoni and Stefani 2012; Terraneo et al. 2014), and taxonomic classifications or revisions (Budd et al. 2012; Huang et al. 2014), while resolving problematic species or species complexes (Stefani et al. 2008, 2011; Benzoni et 9 Chapter 1 al. 2010, 2014; Gittenberger et al. 2011; Keshavmurthy et al. 2013; Forsman et al. 2015). At present, more than 800 species of scleractinian reef corals have been described (Paulay 1997, Veron et al. 2015). The highest biodiversity in the marine world can be found in the Coral Triangle. This centre of maximum marine biodiversity spans across six countries (Indonesia, Malaysia the Philippines, Timor-Leste, Papua New Guinea, and the Solomon Islands), and is named after the somewhat triangular shape of the area (see Hoeksema 2007). It covers < 1.6% of the world’s ocean area (Veron et al. 2011), yet it contains over 600 scleractinian reef coral species, accounting for almost 75% of the world’s reef coral species (Veron et al. 2015). Marine diversity decreases along latitudinal and longitudinal gradients with increasing distance from this centre (e.g. Hoeksema 2007; Barber 2009; Bellwood and Meyer 2009; Carpenter et al. 2011). Several hypotheses have been proposed as explanatory models for this centre of maximum marine diversity (Rosen 1988; Hoeksema 2007; Bellwood et al. 2012). However, it is likely that a combination of factors may be at work to explain the patterns and species richness in the region (Hoeksema 2007; Halas and Winterbottom 2009; Cowman and Bellwood 2013). Although famed for its astounding biodiversity, the reefs of the Coral Triangle are also known to be highly vulnerable, with more than 85% of the reefs threatened by unsustainable fisheries, coastal development and pollution, and this percentage increases to over 90% when thermal stress and coral bleaching is taken into account (Burke et al. 2012). Based on estimates of coral cover data, Indo-Pacific reefs had an average of only 22% cover in 2003, and coral cover loss was approximately 2% between 1997 and 2003 (Bruno and Selig 2007). Such numbers are worrying, and initiatives are being made to conserve and effectively manage coral reefs area through the establishments of marine protected areas (MPAs) or marine managed areas (e.g. Burke et al. 2012, White et al. 2014; Weeks at al. 2014). Diversity measures and patterns Documenting, mapping and explaining patterns of biodiversity are the essence of ecological studies (Magurran 2004). Understanding the current status of biodiversity is important in order to predict its response to environmental changes (Gaston 2000), and to identify systematic conservation planning and its sustainable use (Margules and Pressey 2000). Biodiversity can be grouped into three main components: genetic diversity, species diversity and ecosystem diversity (Norse et al. 1986; Heywood and Baste 1996; Gaston and Spicer 2004; Gaston 2010). Genetic diversity reflects the variation of genes within a species, and species diversity refers to the different number of species in an area, whereas ecosystem diversity is the variation in ecosystems through its communities and habitats in a region. Aspects of the first two components of diversity are examined in this thesis. 10 General Introduction Genes are the essence of a species. Genetic diversity can be measured by assessing and comparing DNA sequence data (Culver et al. 2011). Genetic data is increasingly being applied to resolve taxonomic uncertainties (as mentioned in the previous section). At the population level, genetic diversity is evaluated within and among populations to quantify the distribution and pattern of genetic variation of a species (Templeton 1998). Such population genetics studies have revealed various patterns of connectivity or disjunction among populations. Species diversity is commonly quantified in terms of species counts to represent richness (McIntosh 1967; Magurran 2004), but it can be measured through other components such as species evenness, abundance, commonness, and rarity. Although species richness appears to be the simplest measure of diversity, the success of documenting species is highly dependent upon
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