Reproduction Patterns of Scleractinian Corals in the Central Red Sea Dissertation/Thesis by Jessica Bouwmeester In Partial Fulfillment of the Requirements For the Degree of Doctor of Philosophy King Abdullah University of Science and Technology Thuwal, Kingdom of Saudi Arabia December 2013 2 EXAMINATION COMMITTEE APPROVALS FORM The dissertation/thesis of Jessica Bouwmeester is approved by the examination committee. Committee Chairperson: Dr. Michael Berumen Committee Members: Dr. Christian Voolstra Dr. Ibrahim Hoteit Dr. Andrew Baird 3 © December 2013 Jessica Bouwmeester All Rights Reserved 4 ABSTRACT Reproduction Patterns of Scleractinian Corals in the Central Red Sea Jessica Bouwmeester Early work on the reproductive seasonality of corals in the Red Sea suggested that corals exhibit temporal reproductive isolation, unlike on the Great Barrier Reef where many species spawn in synchrony. More recent work has however shown high synchrony in the maturity of gametes in Acropora species, suggesting multi-specific spawning is likely to occur in the Red Sea. In this thesis I investigate the patterns of coral reproduction in the central Red Sea. The spawning season in the central Red Sea lasts four months, from April to July and spawning occurs on nights around the full moon. During this period Acropora species show a peak of spawning in April, with some species spawning again in May. The level of synchrony, quantified with a spawning synchrony index, is comparable to other locations where multi-specific spawning has been reported. Observations over two consecutive years show that the synchrony of spawning was lower in spring 2012 than in spring 2011, and thus that spawning patterns are variable from one year to the other. Coral settlement patterns on artificial substrata confirmed a main spawning season in the spring but also supported reproductive data suggesting that some Porites spawn in October-November. Settlement was studied over 2.5 years on a reef, which had suffered recently from high mortality after a local bleaching event. Settlement appeared low but post-bleaching studies from other locations indicated similar abundances and showed that recruits generally did not increase until 5 years after the 5 bleaching event. Abundance of juvenile corals however started to increase significantly three years after the bleaching. Successful recruitment, although low suggests that the coral assemblage on the affected reef will most likely recover as long as it is not affected by another disturbance. 6 ACKNOWLEDGEMENTS I would like to thank my advisors Dr. Michael Berumen and Dr. Andrew Baird who have provided strong support throughout my PhD education and during my thesis writing, as well as my other committee members Dr. Christian Voolstra and Dr. Ibrahim Hoteit. I particularly thank Michael for the numerous opportunities that I have been given in the past years as a member of the Reef Ecology Lab in the King Abdullah University of Science and Technology. I am also very grateful to the Reef Ecology Lab and of course KAUST for strong financial support throughout my thesis. I thank all the numerous divers from the Reef Ecology Lab, Red Sea Research Centre, KAUST community and the Coastal Marine Resources Core Lab for the time invested in supporting me in the field mostly underwater, specifically Maha Khalil, Pedro De La Torre, Francis Mallon and David Pallett. I would also like to thank the logistics team of CMOR for their support with organising a big part of the fieldwork conducted for this thesis. I am fortunate to have met many amazing people from all over the world during my PhD years in KAUST and am especially grateful to all my freediving buddies as well as the music community on campus and outside, who strongly contributed to making my time here a rich and unique multicultural experience. Last but not least I would like to thank my family for their strong support in all my projects since I left home nearly a decade ago and I would like to specially thank my brother Daniël for his engineering knowledge and expertise (and for fixing my matlab files), and for having always been there for me. Merci Dan! 7 TABLE OF CONTENTS EXAMINATION COMMITTEE APPROVALS FORM…………………………………… 2 COPYRIGHT PAGE………………………………………………………………………… 3 ABSTRACT………………………………………………………………………………… 4 ACKNOWLEDGEMENTS………………………………………………………………... 6 TABLE OF CONTENTS…………………………………………………………………... 7 LIST OF ABBREVIATIONS……………………………………………………………… 8 LIST OF FIGURES………..………………………………………………………………. 9 LIST OF TABLES…………………………………………………………………………. 11 CHAPTER 1: INTRODUCTION………………………………...…………………………. 12 CHAPTER 2: REPRODUCTIVE SEASONALITY OF THE ACROPORA ASSEMBLAGE 32 SUPPLEMENTARY DATA……………………………………………………………….... 55 CHAPTER 3: MULTISPECIFIC SPAWNING SYNCHRONY …………………………… 59 SUPPLEMENTARY DATA……………………………………………………………….... 98 CHAPTER 4: POST-BLEACHING CORAL RECOVERY AND SETTLEMENT.……. 103 CHAPTER 5: GENERAL DISCUSSION……………………….………………………… 125 APPENDIX 1: LIST OF PUBLICATIONS……………………………………………. 136 BOUWMEESTER ET AL. 2011 CORAL REEFS…………………………………………. 137 BOUWMEESTER ET AL. 2011 GALAXEA…..…………………………………………. 138 RODER ET AL. 2013 NATURE SCIENTIFIC REPORTS………………………………. 142 RODER ET AL. 2013 SUPPLEMENTARY DATA……………………..……..…………. 152 BERUMEN ET AL. 2013 CORAL REEFS……………………………………………...…. 155 FURBY ET AL. 2013 CORAL REEFS……………………………………………………. 167 APPENDIX 2: LIST OF CONFERENCE PRESENTATIONS……………………………. 176 8 LIST OF ABBREVIATIONS ANOVA Analyse of variance CCA Crustose coralline algae FM Full moon GBR Great Barrier Reef KAUST King Abdullah University of Science and Technology NM New Moon SM (A) Marquis’ index of synchrony at the assemblage level SM (S) Marquis’ index of synchrony at the species level SST Sea surface temperatures 9 LIST OF FIGURES CHAPTER 1: INTRODUCTION…………………………………………………………….... 12 Figure 1 Map of the Red Sea CHAPTER 2: REPRODUCTIVE SEASONALITY OF THE ACROPORA ASSEMBLAGE IN THE CENTRAL RED SEA……………………….…………………………………………. 32 Figure 1 Map of the Red Sea showing Thuwal and Al Lith Figure 2 Proportion of Acropora colonies with mature, immature or no visible eggs and proportion of Acropora species with at least one mature Figure 3 Spawning synchrony calculated with the Marquis synchrony index SM CHAPTER 3: MULTISPECIFIC SPAWNING SYNCHRONY WITHIN SCLERACTINIAN CORAL ASSEMBLAGES IN THE RED SEA……………………………………………… 59 Figure 1 Map of the Red Sea showing Al Fahal and Dreams Beach Reef Figure 2 Moon phases in Thuwal in 2011, 2012 and 2013 Figure 3 Stages of gametogenesis of some scleractinian corals throughout the reproductive season from April to July Figure 4 Stages of gametogenesis of Porites species Figure 5 Setting and spawning behaviour Figure 6 Number of species observed to spawn in various locations Figure 7 Hourly water temperatures from April to July in 2011, 2012 and 2013 Figure S1 Porites columnaris Figure S2 Porites lobata Figure S3 Porites lutea Figure S4 Porites solida 10 CHAPTER 4: CORAL RECOVERY AND RECRUITMENT AFTER A BLEACHING EVENT IN THE CENTRAL RED SEA……………………………………………………………… 103 Figure 1 Maps indicating Thuwal and Abu Shosha Figure 2 Relative abundance of coral genera in the adult assemblage and relative distribution of each genus on the sheltered versus the exposed side Figure 3 Average coral on the exposed and sheltered side of Abu Shosha. Figure 4 Exposed side of Abu Shosha Reef at 1-5m Figure 5 Relative abundance of the abundant genera of juvenile corals Figure 6 Average number of juveniles Figure 7 Average number of recruits per 100 cm2 tile and proportion of recruits from Acroporidae, Pocilloporidae, Poritidae and other families 11 LIST OF TABLES CHAPTER 2: REPRODUCTIVE SEASONALITY OF THE ACROPORA ASSEMBLAGE IN THE CENTRAL RED SEA……………………………………………………………………. 32 Table S1 Proportion of Acropora colonies with white and mature eggs Table S2 Proportion of Acropora colonies in each species with white and mature eggs CHAPTER 3: MULTISPECIFIC SPAWNING SYNCHRONY WITHIN SCLERACTINIAN CORAL ASSEMBLAGES IN THE RED SEA…………...…………………………………… 59 Table 1 Criteria for classification of oocytes and spermatocytes into developmental stages Table 2 Stages of gametogenesis on various dates throughout the spawning season in 2011. Table 3 List of corals recorded to spawn in 2011, 2012 and 2013. 12 CHAPTER 1: INTRODUCTION Introduction Coral reefs are one of the most spectacular and fragile of underwater environments, covering less than one percent of the ocean floor but supporting an estimated 25 percent of all marine life. They are one of the most diverse and productive ecosystems in the world and provide many important ecosystem services such as coastal protection, an important source of food for millions of people, a source of income from recreational activities and a source of potential medicine to cure human diseases (Connell 1978; Moberg and Folke 1999). They are formed primarily by hermatypic scleractinian corals; commonly known as reef-building corals. Unfortunately they are considered one of the most highly impacted marine ecosystems on earth. Following the 1997-1998 ENSO event, corals all over the world suffered from intense bleaching, followed by high mortality rates in many regions (Wilkinson 1999; Baker et al. 2008). Such events are likely to happen again and the predicted consequences on coral reefs under likely climate change scenarios are extreme (Hoegh-Guldberg 1999; Hoegh-Guldberg et al. 2007; Halpern et al. 2008). Under the current trends of climate change and the rise in disturbances to corals leading to mortality (Graham et al. 2011), successful reproduction of the adult