Habitat driven responses of reef fish: temporal change, niche partitioning and selection Adam Gouraguine A thesis submitted for the degree of Doctor of Philosophy Department of Biological Sciences University of Essex Date of Submission (March 2018) i Dedicated to my mother ii Abstract Shallow water tropical and temperate marine habitats are changing dramatically in response to many stressor-driven effects. The change in turn threatens the associated fish communities relying on their maintenance for habitat provision. At present, a much better understanding of the interaction between changing habitats and the associated fish is necessary. To address the lack of understanding of the habitat – fish association, mechanisms which underpin the habitat driven responses of reef fish were examined, from entire communities down to species level, across tropical and temperate ecosystems. Using a highly biodiverse ecosystem as the model system, effects of changing habitat on the associated fish community were observed, consequently demonstrating how important, in terms of shelter and food resources, the overall habitat is in structuring the fish community. Furthermore, patterns of habitat use of certain fish species within and across tropical and temperate ecosystems were examined. Variation in the size of the habitat used and its overlap between species within systems, and uniform patterns in habitat use and comparable fish habitat size and overlap across systems, were discovered. By looking at fish habitat use within systems, invaluable knowledge was gained on ecological interactions between habitat and fish on a small scale. At the same time, detection of similar mechanisms of fish habitat use across ecosystems indicates to possible uniform response of fish communities to habitat change at a large-scale. Finally, by looking at fish habitat selection using olfaction, in a temperate model system, a range of subtle behavioural responses displayed during habitat selection were detected. These results highlighted the extent of complexity of the mechanisms used in fish habitat selection and the ubiquitous importance of the habitat and its properties for the associated fish. In addition to, and based on the ecological significance of the findings, a number of potential management and conservational applications of the research were given within the thesis. iii Acknowledgements Draga majko, bez tvoje ljubavi, pomoći i beskrajnog hrabrenja, siguran sam da bi mi bilo teže i da bi mi trebalo mnogo duže da završim ovaj doktorat. Beskrajno ti hvala na podršci, moralnoj i prehrambenoj. Joan Moranta, sense tu aquesta tesi no seria possible. Mai et podré agrair prou per acceptar de ser el meu director. Per a mi has estat una gran influencia, tant científicament com personalment. Espero ser teu amic per sempre. Dave Smith, thank you for starting me on this PhD journey and being a “yes type of supervisor”, always encouraging and supporting my scientific ideas. Hilmar Hinz, although you were not my official supervisor, more than often your scientific input into the PhD matched that of one. You significantly improved the quality of my research, as well as me as a scientist. I am really glad we also became friends along the way. Olga Reñones, sin tu ayuda con el trabajo del campo, organización de campañas y recogida de datos, todavía estaría pendiente de muestreo. Tampoco hubiese disfrutado de él, tanto. Aparte, a lo largo de los últimos años siempre has estado pendiente de mí y me has apoyado muchas veces cuando el más lo he necesitado. Lucia Rueda, tu extenso conocimiento de R y constante disponibilidad frente mis preguntas me han ahorrado muchísimo tiempo y nervios a lo largo de la tesis. Manolo Hidalgo y Cova Orejas dedicaron su tiempo e interés a escuchar sobre mi trabajo científico y me ayudaron con sus consejos expertos. Emma Revill, University of Essex graduate administrator, showed limitless patience with my inquiries and requests, often going out of her way to help me. University of Essex contributed in funding several of my scientific trips and conferences. My stay at the Spanish Institute of Oceanography (Instituto Español de Oceanografía) and the resulting opportunities within this research environment increased the quality of my PhD and formed an invaluable part in my scientific development. Klemen Vute, tvoje drugarstvo mi je pomoglo da ostanem veseo tokom doktorata, ali šta je za mene možda i važnije, fizicki spreman. Finally, Heather Baxter, from being the best expedition iv buddy to being the best life buddy I could wish for, your presence, love and support made this PhD journey a lot happier for me. v Contents Abstract ................................................................................................................................. ii Acknowledgements .............................................................................................................. iii Contents ................................................................................................................................. v List of Tables....................................................................................................................... vii List of Figures .................................................................................................................... viii Publications and conferences ............................................................................................... ix List of abbreviations ............................................................................................................... x 1 Chapter 1: General introduction ..................................................................................... 1 1.1 The habitat ............................................................................................................... 1 1.1.1 Description ....................................................................................................... 1 1.1.2 Coral and macroalgae roles and ecosystem services........................................ 4 1.1.3 Threats .............................................................................................................. 6 1.2 Fish community ....................................................................................................... 9 1.3 Long-term habitat change ...................................................................................... 11 1.4 Habitat use ............................................................................................................. 12 1.5 Fish habitat selection ............................................................................................. 13 1.5.1 Chemical cues and habitat selection .............................................................. 15 1.6 Conservation .......................................................................................................... 17 1.7 Aims of the thesis .................................................................................................. 19 2 Chapter 2: The effect of habitat change on the associated fish community in a tropical coral reef ecosystem ............................................................................................................. 21 2.1 Introduction ........................................................................................................... 21 2.2 Materials and methods ........................................................................................... 24 2.2.1 Study site ........................................................................................................ 24 2.2.2 Sampling ........................................................................................................ 26 2.2.3 Temperature data and benthic habitat surveys ............................................... 27 2.2.4 Fish surveys .................................................................................................... 28 2.2.5 Monitoring participants and data treatment ................................................... 29 2.2.6 Statistical analysis .......................................................................................... 30 2.3 Results ................................................................................................................... 32 2.3.1 Temperature anomalies and benthic habitat ................................................... 32 2.3.2 Fish community .............................................................................................. 40 2.4 Discussion ............................................................................................................. 64 2.5 Supplementary material ......................................................................................... 70 2.5.1 Most abundant species (copyright FishBase) ................................................. 70 vi 3 Chapter 3: Fish habitat use within and across tropical and temperate reefs ................ 74 3.1 Introduction ........................................................................................................... 74 3.2 Materials and methods ........................................................................................... 77 3.2.1 Sampling habitats and species ........................................................................ 77 3.2.2 Behaviour ....................................................................................................... 80 3.2.3 Convex Hull and Standard Ellipse Area