The grazing impact of common surgeonfish on algal dynamics of the Great Barrier Reef Alyssa Louise Marshell M.Sc. A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2014 School of Biological Sciences Thesis Abstract Herbivory is a key ecological process that structures coral reef benthic communities, and consequently is important for ecosystem resilience. Most species of the family Acanthuridae (surgeonfish, unicornfish and tangs) are herbivores, and are widespread, abundant members of Indo-Pacific coral reef fish assemblages. Despite the prevalence of acanthurids on coral reefs, there are few investigations of their feeding ecology and functional role as herbivores. This lack of knowledge limits predictions of the impacts of acanthurid exploitation, which is important because many acanthurids are heavily targeted by coral reef fisheries and the aquarium trade. Therefore, the overall objective of this thesis was to investigate the ecological role of herbivorous acanthurids on coral reefs. Chapter 2 examines the grazing impact of herbivorous fishes on macroalgal dynamics (Sargassum spp.) amongst coral reef zones (inner, mid and outer reef flat, and at 4 m deep on the reef slope). Settlement tiles were deployed for five weeks within three treatments (caged, partially-caged, and open plots). Grazing reduced the abundance of Sargassum recruits on partially-caged and open tiles, and patterns of Sargassum recruitment reflected adult distribution (e.g., most Sargassum zygotes settled in the inner reef flat zone where adult plants proliferate). Settlement tiles were then used in aquarium experiments to quantify the removal of Sargassum recruits by key herbivorous fish species from three functional groups (‘scraping’ parrotfish, ‘cropping’ surgeonfish, blennies and surgeonfish that ‘comb’ the substrate). All fishes, except blennies, removed Sargassum recruits through their foraging activity, highlighting their role in mitigating macroalgal blooms through their impact on developmental stages of macroalgae. Importantly, this is the first documentation of this functional role by acanthurids. Chapter 3 investigates the grazing impact of the most abundant and common surgeonfishes, Acanthurus nigrofuscus and Ctenochaetus striatus, on algal turf dynamics. A. nigrofuscus is a grazer that crops algal turfs, while C. striatus is detritivorous and was thought to ‘brush’ detritus from the surface of algal turfs, causing little damage. In experimental aquaria trials, both surgeonfish fed more intensively upon sparse/short algal turfs even though the yield of algae per bite was greater for dense/long algal turfs. Surprisingly, C. striatus removed significantly more algal turf per hour than A. nigrofuscus, irrespective of canopy height. The capability of C. striatus to remove significant quantities of algal turf through their foraging activity implies that this abundant ii and widespread species needs to be considered as a potentially important influence on reef algal turf dynamics. Chapter 4 explores spatial variability in algal turf dynamics (productivity and grazed standing crop biomass), herbivorous fish biomass (Acanthuridae, Labridae, and Siganidae), and grazing intensity at different depths and exposures of reef slope habitats. This aim was achieved through controlled field experiments, fish visual censuses, and in situ video surveys of fish grazing intensity. Algal turf productivity was highest in windward and shallow sites, and herbivorous fish biomass mirrored this pattern. However, there was no difference in the algal turf standing crop biomass or total number of bites taken daily among habitats. To identify the daily grazing impact of surgeonfish species on algal turfs, data on total surgeonfish biomass and grazing intensity were combined with algal turf productivity estimates. In the most productive reef slope habitat (windward-shallow), surgeonfishes accounted for 74% of the total herbivore biomass, took 51% of the total bites and removed 73% of daily turf productivity. This study highlights the critical functional role of surgeonfishes in algal turf dynamics on reef slopes, and hence maintaining benthic community structure. In Chapter 5, a grazing simulation model was developed to investigate the interactions between fish grazing intensity and algal turf dynamics at different depths (shallow, deep) and exposures (leeward, windward) on reef slope habitats. The model predicts turf biomass that closely matches the observed turf biomass in three of four reef slope habitats. However, the model output currently underestimates the amount of observed turf biomass in the most productive habitat (windward- shallow), suggesting that there are gaps in our knowledge of turf dynamics in this zone. The model provides new insights into the fine spatial and temporal scales of algal turf dynamics on reefs, and enhances our knowledge of processes involved these dynamics. Furthermore, the grazing model is an adaptive tool that will be developed further as additional empirical data become available, facilitating investigations into the potential outcomes of different management scenarios, and adding to our understanding of complex processes that prevent or reverse coral-algal shifts following large-scale reef disturbances. In summary, this thesis fills critical knowledge gaps in acanthurid feeding ecology by quantifying acanthurid grazing impact, identifying the role of key species, and examining the influence of acanthurids on algal community dynamics. These data clearly demonstrate the importance of acanthurids to reefs. This research also provides insights into the implications of acanthurid exploitation and provides a clear rationale for their protection. iii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the General Award Rules of The University of Queensland, immediately made available for research and study in accordance with the Copyright Act 1968. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. iv Publications during candidature Rogers A, Harborne AR, Brown CJ, Bozec Y-M, Castro C, Chollett I, Hock K, Knowland C, Marshell A, Ortiz JC, Razak T, Roff G, Samper-Villarreal J, Saunders M, Wolff N, Mumby PJ (2014) Anticipative management for coral reef ecosystem services in the 21st century. Global Change Biology (doi: 10.1111/gcb.12725) Taylor, BM, Rhodes KL, Marshell A, McIlwain JL (2014) Age-based demographic and reproductive assessment of orangespine, Naso lituratus, and bluespine, Naso unicornis, unicornfishes. Journal of Fish Biology 85:901-916 Hartup JA, Marshell A, Stevens G, Kottermair M, Carlson P (2013) Manta alfredi target multispecies surgeonfish spawning aggregations. Coral Reefs Reef Site 32:367 Marshell A, Mumby PJ (2012) Revisiting the functional roles of the surgeonfish Acanthurus nigrofuscus and Ctenochaetus striatus. Coral Reefs 31:1093-1101 Doropoulos C, Ward S, Marshell A, Diaz-Pulido G, Mumby PJ (2012) Interactions among chronic and acute impacts on coral recruits: the importance of size-escape thresholds. Ecology 93:2131- 2138 Marshell A, Mills J, McIlwain JL, Rhodes KL (2011) Passive acoustic telemetry reveals highly variable home range and movement patterns among unicornfish within a marine reserve. Coral Reefs 30:631-642. Publications included in this thesis Incorporated as Chapter 3: Marshell A, Mumby PJ (2012) Revisiting the functional roles of the surgeonfish Acanthurus nigrofuscus and Ctenochaetus striatus. Coral Reefs 31:1093-1101 Contributor Statement of contribution Alyssa Marshell Designed and analysed experiments (70%) Wrote the paper (80%) Peter J. Mumby Designed experiments (30%) Wrote and edited paper (20%) v Contributions by others to the thesis Peter J Mumby contributed to the thesis funding, conception, design, conduct, data analysis, interpretation, and editing of all Chapters. Alastair Harborne contributed to the design, data analysis, interpretation, and editing of Chapters 1 and 2. Christopher Doropoulos contributed to the design, data analysis, interpretation and editing of Chapter 2. Alice Rogers contributed to the editing of Chapter 4. Yves-Marie Bozec and Iliana Chollett contributed to the design, interpretation, and editing of Chapter 5. Statement of parts of the thesis submitted to qualify for the award of another degree None. vi