Ecology of Crustose Coralline Algae; Interactions with Scleractinian Corals and Responses to Environmental Conditions

Thesis submitted by Lindsay Mortan Harrington Bsc (California) in August 2004

For the Degree of Doctor of Philosophy In the School of Marine Biology and Aquaculture at James Cook University Statement of Contributions by Others

I gratefully acknowledge the support of an International Postgraduate Research Scholarship (IPRS) Award from the James Cook University (JCU). I would like to extend my gratitude to the Cooperative Research Centre for the Great Barrier Reef World Heritage Area (CRC Reef), and the Australian Institute of Marine Science (AIMS) for funding this research.

Some of the work I carried out for my PhD was collaborative, jointly published and/or done with technical, theoretical, statistical, editorial or physical assistance of others. I fully acknowledge the contributions by others as outlined below and detailed in the acknowledgements. To the best of my knowledge, all other work was done and written independently.

Chapter 2 Dr. Glenn De'ath provided statistical assistance. Dr. Katharina Fabricius and Dr. Robert Steneck contributed to the intellectual and editorial work.

Chapter 3 This chapter contains research that is part of a jointly published paper. Geoff Eaglesham conducted water analysis and characterization. Sediment analysis and characterization was carried out by Miriam Weber (Diplom thesis, 2003). Both Dr. Katharina Fabricius and Dr. Andrew Negri contributed to the intellectual, written and editorial work (see Appendix one, publication No. 2).

Chapter 4 This chapter contains research that is part of a collaborative effort (see Appendix one, publication No. 3). Tiles were deployed by myself (inshore reefs GBR), Emre Turak (offshore reefs GBR) and Robert Steneck (reefs in the Caribbean). Both Dr. Robert Steneck and Ernre Turak contributed to the intellectual work. Dr. Glenn De'ath provided statistical advice and Dr. Katharina Fabricius assisted with editorial work. Statement of Contribution by Others iv

Chapter 5 This chapter contains research that is part of a jointly published paper. Dr. Glenn De'ath provided statistical assistance. Dr. Andrew Negri performed CCA chemical extractions, and provided theoretical and editorial assistance to the manuscript. Dr. Katharina Fabricius contributed to.the intellectual and editorial work (see Appendix one, publication No. 1). Acknowledgments v

Acknowledgments

Firstly I want to thank my supervisors who each, uniquely, provided me with the support I needed to complete my PhD. Katharina Fabricius, my primary supervisor, thank you for your time, constant support, patience and generosity. I could never have done this without you. Bob Steneck, thank you for sharing your knowledge about corallines with me, your encouragement and for including me in the Caribbean research. Finally, John Collins, thank you for being curious about every aspect of the science, and for believing that I would get this done, I always walked out of your office feeling better.

I was fortunate to work along side of many others who each brought something to this thesis, sharing with me their expertise. I specifically acknowledge the support, advice, friendship and continuous assistance of Luke Smith (MIGU), Andrew Negri, Glenn De'ath and Emre Turak- all my gratitude for your time, help, encouragement and knowledge. Many thanks to the people at AIMS and JCU who helped me in invaluable ways, especially Steve Delean, Andrew Baird, Tim Phillips, John Brodie, Jenny McGregor, Tim Simmonds, Howard Choat and Terry Done. Special thanks to Gilianne Brodie, you're the reason I came to Townsville, you've been a mentor and a true friend.

Numerous people assisted me in the field and participated during experiments. This project would not have been possible without their time, assistance, friendship and kindness. I especially want to thank Chico Birrell and Greg Suosarri (for always getting me through the channel), Luke Smith, Miriam Weber, Claudia Vollhart, Sally Sue Ingelton, Juliane Metmer, Andrew Negri, Tony Lamby, Harry Harrington, the staff at Lizard Island Research Station, the staff on Glovers Reef, the crew on the RV Lady Basten and Cape Ferguson, all of whom were willing to lift a hand to help regardless of weather, hour or mental state.

A heart felt thank you to my friends and colleagues who have helped me to survive over the last few years, sharing many laughs and wiping away many tears. Days were made ten times easier with support and love provided by Krina Colombini, Monique Myers, The Beatties, The Phillips, MSD, Paul Detwiler, Stephanie Geier, Anke Klueter, Mary Wakeford, Dave Hawkins, Scott Wooldridge, Tim Cooper, Neal Cantin, Jennifer Morrow, Debbie Dexter, Constance Gramlich, Gilda Zayas, Chris Bowden, and numerous others, too many to mention, but none I'll ever forget.

Finally thank you to my family - I never had a chance to love anything else more than the ocean with a family like mine. You all stood by believing in, supporting and loving me. Thank you to my little sister, who has patiently been waiting for me to come home and play with her since she was four years old and recently started asking, "When will that BOOK be done??'To my parents, thank you for letting me point out the strawberry sea anemones and holding my hand at the sanctuary. You always knew when to be there and when to let me go. I am not sure how you did it, but you did and you did it perfectly. You two have been the best part of my world, not only have you been amazing parents, you have been my best friends. Dedication

For all the women who made me strong, for all the mermaids who coaxed me under the sea and for the man who first took me diving, Daddy Abstract

Crustose coralline algae (CCA) are considered a key functional group in coral reef ecosystems. Changes in the abundances of certain CCA species can directly regulate the abundance of other components of reefs, in particular corals, and can therefore result in changes in structure and function of this marine ecosystem. This thesis assesses important questions on what controls distribution and abundance patterns of tropical CCA species along environmental gradients, their responses to sedimentation and the herbicide diuron, and species-specific differences in their roles in inducing or inhibiting coral recruitment, hence contributing to the structuring of coral reefs.

The taxonomic composition of CCA is described for the inshore and offshore reefs within the central and northern Great Barrier Reef (GBR). Twenty-three species from twelve genera and three subfamilies of Corallinaceae were identified to species level using reproductive and vegetative morphology and anatomical features as diagnostic characters. Distribution and relative abundance of the species were compared along gradients in depth and across the shelf, and along a set of environmental variables such as slope angle and sedimentation. Changes across the continental shelf were observed in CCA cover and CCA community composition, as well as in the environmental variables slope angle, sediment deposits, and water clarity. Percent cover of CCA increased more than four-fold across the shelf. Inshore reefs were dominated by thin leafy non-adherent corallines (i.e. Mastophora paci$ca), whereas offshore reefs were dominated by thick adherent species (i.e. Porolithon onkodes and Neogoniolithon fosliei). Abundances of several species were significantly related to cross-shelf distance, depth and sedimentation. For example, the most abundant CCA, Porolithon onkodes was 4 times more abundant on offshore reefs compared to inshore reefs, and preferred shallow depths (2 to 5 m) and low sediment deposits. Conversely, the most abundant species on the inshore reefs, Hydrolithon reinboldii, decreased in abundance across the shelf, preferred deeper depths (8 to 12 m) and was not affected by high levels of sediment. Differences in CCA communities between inshore and offshore reefs may however be additionally related to the factors of wave force, grazing and water clarity. On the inshore reefs, the reduced cover of CCA, the dominance of thin and leafy species and the reduced abundance of thick consolidators have profound implications for differences in the ecosystem structure.

At present, the degree to which human activity can affect abundance and species composition of CCA on reefs is poorly understood. The herbicide diuron (N'-(3,4- dichloropheny1)-N, N-dimethylurea) is detectible in many inshore sediment samples along the central Queensland coast. Organisms living on some of the inshore coral reefs of the GBR are regularly exposed to river plumes transporting this herbicide. This study compares physiological responses and survival of CCA that were exposed to diuron and to sedimentation, separately and in combination, in controlled time course laboratory experiments, using pulse-amplitude modulation chlorophyll fluorometry. The results demonstrate that sediment deposition and exposure to diuron when applied in isolation can negatively affect the photosynthetic activity of CCA, but were often reversible depending on diuron concentration and sediment type. Significant reductions in effective quantum yields (AFIF,,,,) of photosystem I1 in CCA species were observed at nominal diuron concentrations greater than 1 yg L-'. Exposure to fine (<63 pm grain size) nutrient-rich estuarine sediments reduced AFIF,,,, more than exposure to the same amount of fine (<63 ym grain size) calcareous sediments. There are clear differences in sedimentation tolerance between species, with an inshore species (H. reinboldii) being more sediment tolerant than two offshore species (P. onkodes and N. fosliei). Sedimentation stress is however significantly enhanced by trace concentrations of diuron, and recovery from a combined sediment and diuron exposure was still incomplete after 9 days. The finding of synergistic effects of simultaneous exposure to sedimentation and diuron on CCA has implications for the recruitment of the vast number of reef organisms specialized to settle on CCA.

The ability of coral larvae to identify an appropriate site for settlement and metamorphosis is critical for recruitment. Crustose coralline algae are known to induce metamorphosis of coral larvae in the laboratory. The aim of this field study was to determine what types of substrata (namely reef-dwelling species of CCA) coral recruits settle on and at what orientation (i.e. upper, lower or vertical surfaces). This study was conducted in 3 regions: in the GBR on inshore and offshore reefs, and in the Caribbean. After one year, the amount of unoccupied substrata (bare), and the space occupancy of CCA, Peyssonnelia sp., invertebrates and turf algae on the settlement tiles varied between the 3 regions. On offshore reefs in the GBR the percent of CCA on the tiles was greatest (26%) and turf algae lowest (5%). On average, 89% of coral recruits were found on the bottoms and sides of the settlement tiles. Most coral recruits in the GBR and in the Caribbean attached to a widespread but rare CCA, Titanodermaprototypum, that overall comprised less the 5% of the coralline flora on natural reef surfaces, but as a pioneer species, nevertheless covered 2.5% of the settlement tiles. Most other reef-dwelling organisms, such as other encrusting algae (i.e. the CCA species H. reinboldii and Porolithon sp. and the non-coralline crust Peyssonnelia sp., which induce metamorphosis under laboratory conditions), and some invertebrates (specifically polychaetes, foraminifera and attached bivalves), supported significantly lower coral recruit densities. In all regions combined, only 0.1% of the coral recruits settled onto turf algae despite it covering 14% of the tiles, and 0% settled on sediment-covered surfaces, macroalgae and certain species of dominant CCA. Titanoderma prototypum may provide a good attachment surface in microhabitats where competition and grazing from other reef organisms is low. This research identifies the available settlement substrata for coral settlement in the GBR and Caribbean and highlights the critical role a single species can play in the structure and function of a highly complex ecosystem.

Several species of CCA are known to induce coral settlement, however CCA also employ physical and biological anti-settlement defence strategies at varying effectiveness. This study describes the chemical and physical recognition and ranking of five CCA species and inert settlement substrata by coral larvae, and the subsequent survival of these larvae on the varying substrata. Settlement on the most preferred substratum, T. prototypum, was 15 times higher than on the least preferred substratum, N. fosliei. The rates of post-settlement survival of the corals also varied among CCA species in response to their anti-settlement strategies (shedding of surface cell layers, overgrowth and potential chemical deterrents). Rates of larval settlement, post-settlement survival and the sensitivity of larvae to chemical extracts of CCA were all positively correlated across the five species of CCA. Non-living settlement substrata on coral reefs are sparse, consequently the presence of only a few CCA species that facilitate coral recruitment has important implications for structuring the reef ecosystem.

These four studies have extended our knowledge of basic ecology of CCA and their important role in structuring coral reefs. They have also advanced our knowledge of how the mosaic of benthic organisms, influenced by human disturbances, affect coral settlement. A small and inconspicuous species of CCA that strongly facilitates and catalyzes coral recruitment on reefs has been identified. The information gained from these studies assists in the understanding of reef recovery, and therefore may contribute to the management and conservation of reef ecosystems. Table of Contents xii

Table of Contents

Page TITLE PAGE .1. STATEMENT OF ACCESS AND SOURCES DECLARATION .11. . STATEMENT OF CONTRIBUTIONS BY OTHERS 111 ACKNOWLEDGEMENTS v DEDICATION vii... ABSTRACT Vlll TABLE OF CONTENTS xii LIST OF TABLES xv LIST OF FIGURES xvii

CHAPTER 1 General introduction 1

1.1 Introduction 2 1.2 Thesis outline 4

CHAPTER 2 The community structure of crustose coralline algae (Rhodophyta: Corallinaceae) in the central and northern Great Barrier Reef 7

2.1 Abstract 8 2.2 Introduction 9 2.3 Materials and Methods 10 2.3.1 Study sites 10 2.3.2 Surveys 12 2.3.3 Environmental variables 13 2.3.4 Data analyses 13 2.4 Results 15 2.4.1 Large scale spatial patterns across the shelf 18 2.4.2 Differences between the two inshore regions WT and PCB 20 2.4.3 Depth zonation 20 2.4.4 Morphological trends and depth zonation 26 2.4.5 Environmental variables 27 2.5 Discussion 3 1 2.5.1 General 3 1 2.5.2 Environmental variables 3 1 2.5.3 Large scale spatial patterns across the shelf 33 2.5.4 Differences between the two inshore regions, WT and PCB 34 2.5.5 Depth zonation 3 5 2.5.6 Morphological trends and zonation 3 5 2.5.7 Taxonomy 37 2.5.8 Conclusions 3 8 Table of Contents xiii

CHAPTER 3 Synergistic effects of diuron and sedimentation on the photophysiology and survival of CCA

3.1 Abstract 3.2 Introduction 3.2.1 Sedimentation on the Great Barrier Reef 3.2.2 Herbicides on the Great Barrier Reef 3.2.3 Potential effects of terrestial runoff on crustose coralline algae 3.3 Materials and Methods 3.3.1 CCA collection and preparation 3.3.2 Sediment collection and preparation 3.3.3 Diuron stock preparation 3.3.4 Measurements of photosynthetic yields using Pulse amplitude modulated (PAM) fluorometry 3.3.5 Exploratory studies 3.3.6 Sediment exposure 3.3.7 Combined diuron and sediment exposure 3.3.8 Extraction and analysis of diuron 3.3.9 Data analyses 3.4 Results 3.4.1 Exploratory studies 3.4.2 Sediment exposure 3.4.3 Combined diuron and sediment exposure 3.5 Discussion 3.5.1 Application of PAM fluorometry to CCA 3.5.2 Effects of Sediments 3.5.3 Bleaching as visible sign of stress 3.5.4 Effects of diuron 3.5.5 Sediments mixed with diuron: Synergistic effects 3.5.6 Environmental relevance - Impacts on coral reefs ecosystems 3.5.7 Conclusion

CHAPTER 4 The role of crustose coralline algae in coral recruitment

4.1 Abstract 4.2 Introduction 4.3 Materials and Methods 4.3.1 Study sites 4.3.2 Tile deployment 4.3.3 Tile retrieval and processing 4.3.4 Determination of coral recruitment patterns 4.3.5 Data analyses 4.4 Results 4.4.1 Inshore reefs in the central and northern GBR 4.4.2 Offshore reefs in the central and northern GBR 4.4.3 Caribbean 4.4.4 Comparison of three regions Table of Contents xiv

4.5 Discussion 4.5.1 Available settlement substrata 4.5.2 Recruitment patterns and recruit interaction with sessile organisms 4.5.3 CCA as settlement substrata 4.5.4 Other available settlement substrata 4.5.5 Macroalgae 4.5.6 Spatial competition and Post-settlement mortality 4.5.7 Spat recruitment orientation 4.5.8 Ecology of Titanoderma 4.5.9 Conclusion

CHAPTER 5 Habitat selection determines post settlement survival in corals 100

5.1 Abstract 101 5.2 Introduction 102 5.3 Materials and Methods 104 5.3.1 Obtaining coral larvae 105 5.3.2 Collection of non-geniculate crustose coralline algae 107 5.3.3 Substratum-specific settlement rates 107 5.3.4 Post-settlement survival 108 5.3.5 Investigating chemical responses 109 5.3.6 Data analyses 110 5.4 Results 112 5.4.1 Substratum-specific settlement rates of Acropora tenuis and A. millepora larvae 112 5.4.2 Survival of Acropora tenuis spat 113 5.4.3 Larval metamorphosis in response to CCA morphogen 116 5.4.4 Synthesis of the three experiments 117 5.5 Discussion 118 5.5.1 Settlement cues for coral larvae 118 5.5.2 Anti-settlement defense strategies of CCA 120 5.5.3 Larval ranking of potential settlement substrata 122 5.5.4 Conclusion 123

CHAPTER 6 General discussion and conclusions 124

6.1 Ecology of crustose coralline algae species and communities 125 6.2 Interactions between crustose coralline algae and scleractinian corals 127 REFERENCES 131 APPENDIX ONE: PUBLICATIONS ARISING FROM THIS THESIS 149