Population biology and grazing processes of the sea urchin Centrostephanus tenuispinus (Clark, 1914) inhabiting coral and macroalgal dominated reefs Rathnayaka Mudiyanselage Gayani Nilupika Thilakarathna, BSc This thesis is presented for the degree of Doctor of Philosophy of Murdoch University 2017 i Declaration I declare that this thesis is my own account of my research and contains as its main content work which has not previously been submitted for a degree at any tertiary education institution. .................................... (Gayani N. T. Rathnayaka Mudiyanselage) December 2017 ii Abstract Sea urchins play a key role as herbivores and bio-eroders, impacting the organization and structure in many marine benthic habitats. Hall Bank reef (32°2.002´S and 115°42.957´E) off Western Australia is unique having high coral cover, which is unusual for high latitude reefs. Although the high density of Centrostephanus tenuispinus is believed to be the reason for the absence of macroalgae, lack of knowledge on the biology and ecology of this species hampers our understanding of the functioning these reefs. The main objective of this study was to evaluate the role of C. tenuispinus in structuring and functioning of Hall Bank reef with respect to macroalgae- dominated Minden Reef. Benthic surveys and monthly sample collections were carried out at two sites, to assess temporal variation of substrate cover, urchin density, reproductive patterns, feeding habits and bio-erosion. Higher density (2.94 ± 0.14 m-2) of C. tenuispinus with small tests at Hall Bank reef indicated low food availability, while lower densities (0.14 ± 0.01 m-2) of larger urchins at Minden Reef indicated high productivity in the habitat. A clear synchronised annual reproductive cycle was recorded. The gametogenic cycle was initiated by decreasing seawater temperature and day length in March, leading to spawning in winter. Minden Reef urchins had a higher Gonadosomatic Index, coinciding with high food availability. Less seasonal variability in substrate composition influenced the reduced variability in diet at Hall Bank reef while pronounced seasonal variation in the diet of Minden Reef urchins coincided with seasonal changes of substrate cover. Bio-erosion rates were positively correlated with sea water temperature. The annual bio-erosion rate in Hall Bank reef was 1017.69 g -2 -1 CaCO3 m y . Changes in the population of Centrostephanus tenuispinus, being the dominant grazer and bio-eroder in Hall Bank reef, can greatly influence the structure and species composition of the reef, and could lead to ecological phase shifts in this reef system at extremes. The comprehensive knowledge acquired through this study on Centrostephanus tenuispinus provides baseline data for the region on this particular species which could be used in monitoring and managing reefs with current trends in climate change. iii Acknowledgements While I alone am responsible for this thesis, it is nonetheless at least as much a product of years of interaction with, and inspiration by, a larger number of colleagues and peers as it is my own work. For this reason, I humbly take this opportunity to acknowledge debt to all those people whose comments, questions, criticism, support and encouragement, personal and academic, have left a mark on this work. The first gratitude goes to my supervisors Dr. Mike van Keulen and Dr. John Keesing. I am very grateful for your encouragement and for not giving up on me with my limited underwater experience. Your ideas and passions in the field of marine sciences have exceptionally inspired and enriched my growth as a student, a researcher and a budding scientist. Your understanding, encouraging and personal guidance have provided a good basis for the present thesis. My appreciation is also extended to the Murdoch University for providing me the Murdoch International Scholarship (MIPS). I am very grateful for generous support with field work from Steven Goynich, Michael Taylor, Ian Dapson, Claudia Muller, Amy Kirke, Peter Howie, Phillip Good, Mark Thiele, Brodee Elsdon and Justine Arnold. You all have been a source of inspiration through your tremendous support in an extraordinary manner to move my field work forward, also in encouraging me to pursue ideas. I would like to express my deep and sincere gratitude, to Dr. John Huisman, Director West Australian Herbarium, for his tremendous help in identification of algae. Also I would like to thank Dr. James Tweedley for his generous help with Primer. My deepest gratitude goes Gordon Thomson for his generous support and advice with histology work. I owe my sincere gratitude for Dr. Damian Thomson, CSIRO for providing water temperature data, Department of Water and Environmental Regulation for providing water quality data, Department of Biodiversity, Conservation and Attractions, WA and Department of Fisheries, WA for providing permission for the sample collections. iv My deepest gratitude goes to Dr. Dileepa de Croos for being my mentor in most of my carrier and for his encouragement and guidance during my PhD career. I am grateful for my uncle Dr. Thilak Gunattilake, aunty Mrs. Chandra Guantillake and my friends Piyumi Fonseka and Nadhe Fonseka for being my family and being there for me whenever I needed for last four years. I also owe my thanks to Shashikala, Shanika, Thusitha, Aurelie and all of my colleagues for their immense encouragement and support for last four years. I cannot forget my cousin Sajith Udayanga, uncle Mr. PA Dayarathna and aunties Mrs. Sriyani Manage and Ms. Chandra Rathnayaka for taking care of my mother in my absence in Sri Lanka. Finally, I owe my loving thanks to my mother and late father. It is my father who made me enthusiastic for the world of science since my childhood. I have learned so much from my parents and I appreciate all of the sacrifices that they have made for me. My mother in particular, sacrificed everything for my studies and was the guardian angel of my life. Without her encouragement and understanding it would have been impossible for me to be where I am today. Therefore, I dedicate this dissertation to her with my affection and my never-ending appreciation for all she has done for me. v Table of Contents Declaration .......................................................................................................................... ii Abstract ......................................................................................................................... iii Acknowledgements ............................................................................................................ iv List of Tables .................................................................................................................... xiii Chapter 1 - Literature Review and Introduction .................................................................. 1 1.1 General Introduction ............................................................................................................1 1.2 Impact of climate change on urchin habitats ......................................................................1 1.2.1 Global warming and latitudinal shifts of species ..........................................................2 1.2.2 Impact of Ocean Acidification .......................................................................................3 1.3 Ecology of temperate reefs ..................................................................................................4 1.3.1 Tropical reefs Vs Temperate reefs ................................................................................4 1.3.2 Ecological interactions in temperate latitude reefs ......................................................4 1.3.3 Keystone species ...........................................................................................................5 1.3.4 Drivers of coral-macroalgae phase shifts ......................................................................5 1.3.5 Predicting ecological interactions- food web analysis ..................................................9 1.4 Ecological role of sea urchins on coral reefs ..................................................................... 10 1.5 Sea urchin Biology ............................................................................................................. 12 1.5.1 Sea urchin feeding ...................................................................................................... 12 1.5.2 Sea urchin population size regulation ........................................................................ 13 1.5.3 Sea urchin reproduction ............................................................................................ 15 1.6 Temperate sea urchins ...................................................................................................... 16 1.7 Centrostephanus spp. ....................................................................................................... 16 1.7.1 Centrostephanus tenuispinus in Western Australia ................................................... 18 1.7.2 Centrostephanus tenuispinus population in Hall Bank reef ....................................... 19 1.8 Thesis Aims:....................................................................................................................... 19 Chapter 2 – Population status and size distribution of Centrostephanus tenuispinus: Hall Bank reef vs Minden Reef .............................................................................