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The Role of Territorial Grazers in Coral Reef Trophic Dynamics from Microbes to Apex Predators

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The Role of Territorial Grazers in Coral Reef Trophic Dynamics from Microbes to Apex Predators ResearchOnline@JCU This file is part of the following reference: Casey, Jordan Marie (2015) The role of territorial grazers in coral reef trophic dynamics from microbes to apex predators. PhD thesis, James Cook University. Access to this file is available from: http://researchonline.jcu.edu.au/41148/ The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owner of any third party copyright material included in this document. If you believe that this is not the case, please contact [email protected] and quote http://researchonline.jcu.edu.au/41148/ The role of territorial grazers in coral reef trophic dynamics from microbes to apex predators Thesis submitted by Jordan Marie Casey April 2015 For the degree of Doctor of Philosophy ARC Centre of Excellence for Coral Reef Studies College of Marine and Environmental Sciences James Cook University ! Acknowledgements First and foremost, I thank my supervisory team, Sean Connolly, J. Howard Choat, and Tracy Ainsworth, for their continuous intellectual support throughout my time at James Cook University. It was invaluable to draw upon the collective insights and constructive criticisms of an ecological modeller, an ichthyologist, and a microbiologist. I am grateful to each of my supervisors for their unique contributions to this PhD thesis. I owe many thanks to all of the individuals that assisted me in the field: Kristen Anderson, Andrew Baird, Shane Blowes, Simon Brandl, Ashley Frisch, Chris Heckathorn, Mia Hoogenboom, Oona Lönnstedt, Chris Mirbach, Chiara Pisapia, Justin Rizzari, and Melanie Trapon. I also thank the directors and staff of Lizard Island Research Station and the Research Vessel James Kirby for efficiently facilitating my research trips. I appreciate laboratory help from Bill Leggat, Daisie Ogawa, and Sue Reilly, and for assistance with the microbiome analysis pipeline QIIME, I thank David Bourne, Bill Leggat, and Jean-Baptiste Reina. The Ecological Modelling Research Group at James Cook University has provided me with ample modelling support, and I am also grateful for their tolerance of my practice seminars that were full of microbiology and not much modelling. I especially thank Shane Blowes and Loic Thibaut for guidance in statistical modelling. For conceptual advice and other various help, I appreciate discussions with and feedback from Andrew Baird, Dave Bellwood, Simon Brandl, Daniela Ceccarelli, James Guest, Lindsay Harrington, Jean-Paul Hobbs, Morgan Pratchett, and Brett Taylor. Lastly, I thank my parents, Sharon and Mike Casey, for facilitating all of my educational endeavours with endless support and encouragement. I am also thankful for my Aussie sister, Kristen Anderson, for her friendship and keeping things entertaining. And of course, I have infinite gratitude for my partner, Simon Brandl, for being my greatest ally and infusing my life with birds, adventure, and perpetual smiles. ii" Statement of the Contribution of Others This thesis was funded by the ARC Centre of Excellence for Coral Reef Studies, a Graduate Research Scheme grant from James Cook University, and a Great Barrier Reef Marine Park Authority Science for Management Award. I was supported by a James Cook University International Prestige Research Scholarship, a Doctoral Completion Scheme grant from James Cook University, and a NCAA Postgraduate Scholarship. This thesis was conducted under the supervision of Sean Connolly, J. Howard Choat, and Tracy Ainsworth. For Chapter 2, I was given conceptual advice from David Bellwood, and I obtained field assistance from Kristen Anderson, Shane Blowes, and Chris Heckathorn. I received editorial assistance from Shane Blowes and Simon Brandl. Contributions of co- authors are as follows: • Jordan Casey: design of study, collection of data, performance of lab work, analysis of data, writing of manuscript • Tracy Ainsworth: design of study, writing of manuscript • J. Howard Choat: design of study, writing of manuscript • Sean Connolly: design of study, writing of manuscript For Chapter 3, I obtained field assistance from Kristen Anderson, Shane Blowes, Simon Brandl, Chris Heckathorn, and Mia Hoogenboom. Contributions of co-authors are as follows: • Jordan Casey: design of study, collection of data, performance of lab work, analysis of data, writing of manuscript • Sean Connolly: design of study, writing of manuscript • Tracy Ainsworth: design of study, writing of manuscript For Chapter 4, I was given conceptual advice from Morgan Pratchett, and I obtained field assistance from Kristen Anderson, Shane Blowes, and Melanie Trapon. Contributions of co- authors are as follows: iii" • Jordan Casey: design of study, collection of data, analysis of data, writing of manuscript • J. Howard Choat: design of study, writing of manuscript • Sean Connolly: design of study, writing of manuscript For Chapter 5, I was given conceptual advice from J. Howard Choat, and I obtained field assistance from Oona Lönnstedt. Contributions of co-authors are as follows: • Jordan Casey: design of study, collection of data (territorial damselfishes in the Ribbon and Swain Reefs), analysis of data (mixed-effects models for structural equation modelling and other analyses), writing of manuscript • Andrew Baird: design of study, collection of data (benthic composition in the Ribbon and Swain Reefs), writing of manuscript • Simon Brandl: collection of data (mesopredators and mobile herbivores in the Swain Reefs), analysis of data (R code for structural equation modelling), writing of manuscript • Mia Hoogenboom: design of study, collection of data (benthic composition in the Ribbon Reefs), writing of manuscript • Justin Rizzari: design of study, collection of data (mesopredators and mobile herbivores in the Ribbon Reefs), writing of manuscript • Ashley Frisch: design of study, collection of data (apex predators in the Ribbon Reefs), writing of manuscript • Christopher Mirbach: collection of data (apex predators in the Swain Reefs), writing of manuscript • Sean Connolly: design of study, writing of manuscript All work was carried out under the Great Barrier Reef Marine Parks Authority Permits No. G11/34774.1, No. G09/32834.1, and No. G13/36059.1. iv" Abstract Territories of grazing fishes in the family Pomacentridae have been documented to cover a substantial proportion of shallow coral reefs, and these fishes can have profound effects on benthic dynamics. By cultivating palatable filamentous algae, excluding fleshy macroalgae, and aggressively defending their resources, territorial damselfishes indirectly impact coral- algal competition and play a substantial role in shaping benthic community composition, including the recruitment and post-settlement survival of scleractinian corals. Marine microbes are known to be important drivers of environmental change, and microbial community structure on coral reefs is strongly influenced by coral-algae interactions; however, the extent to which this influence is mediated by territorial grazers is unknown. Territorial damselfishes occur in distinct behavioural guilds ranging from indeterminate territorial grazers with thin algal turfs and low rates of territorial aggression to intensive territorial grazers with thick turfs and high rates of aggression. Members of the genus Stegastes are intensive territorial grazers and are known to play a major role in coral-algal dynamics. Further, most previous studies of territorial grazer effects on corals have focused on back-reef habitats although the reef crest is a highly productive environment with elevated rates of coral recruitment and settlement. Lastly, removal of marine predators via fishing is often theorized to alter community structure through trophic cascades, but empirical evidence for this phenomenon is often circumstantial on coral reefs. Given declines of predators on the Great Barrier Reef (GBR), trophic cascade theory would predict ecosystem repercussions to lower trophic levels, but it is unknown how a predator density gradient impacts the distribution of territorial damselfishes. Thus, the overall objective of this thesis was to examine the role of territorial grazers in shaping the structure and dynamics of benthic communities and the extent to which this may be mediated by higher-level trophic interactions across a gradient of fishing pressure. v" To achieve this objective, I employed a variety of microbial sampling regimes and survey methods to reveal the role of territorial grazers in trophic dynamics on the GBR, Australia. To elucidate how Stegastes apicalis and S. nigricans may alter benthic microbial assemblages and coral health, I determined the benthic community composition (epilithic algal matrix (EAM) and prokaryotes) and coral disease prevalence inside and outside of damselfish territories. To determine the impact of territorial grazers on coral microbial assemblages, I established a coral transplant inside and outside of Stegastes’ territories. Over the course of one year, the percent mortality of transplanted corals was monitored and coral samples were collected for microbial analysis. To assess the impact of territorial grazers on the establishment of juvenile corals, I surveyed the reef crest habitat of Lizard Island using fixed transects to assess the effects of indeterminate and intensive territorial grazers on juvenile coral abundance and taxonomic composition. In addition, the turnover of territorial pomacentrids was monitored, as well as the effects of turnover on juvenile coral assemblages. To examine
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