Effects of macroalgal habitats on the community and population structure of temperate reef fishes by Alejandro Pérez Matus A thesis submitted to Victoria University of Wellington in fulfilment of the requirements for the degree of Doctor of Philosophy in Marine Biology Victoria University of Wellington Te Whare Wānanga o te Ūpoko o te Ika a Māui 2010 This thesis was conducted under the supervision of: Dr. Jeffrey S. Shima (Primary Supervisor) Victoria University of Wellington, Wellington, New Zealand Dr. Russell Cole National Institute of Water and Atmospheric Research (NIWA), Nelson, New Zealand and Dr. Malcolm Francis National Institute of Water and Atmospheric Research (NIWA), Wellington, New Zealand Notolabrus fucicola over Carpophyllum flexuosum, Kapiti Island, Wellington “Among the fishes, a remarkably wide range of biological adaptations to diverse habitat has evolved” Dr. T. Pitcher. Abstract Two families of brown macroalgae that occur in sympatry dominate temperate subtidal rocky coasts: the Laminareales, and the Fucales. Both of these families are habitat-forming species for a wide variety of invertebrates and fishes. Variation in the presence, density, and composition of brown macroalgae can have large influences on the evolution and ecology of associated organisms. Here, using a series of observational and experimental studies, I evaluated the effects of heterogeneity in the composition of brown macroalgal stands at the population and community levels for reef fishes. A central ecological challenge is the description of patterns that occur at local scales, and how these are manifested at larger ones. I conducted further sampling across a set of sites nested within locations over three regions, Juan Fernández Islands (Chile), Northern New Zealand, and Tasmania (Australia), to evaluate patterns of variation in the diversity and composition of fish assemblages. Specifically, I explored spatial variation in fish assemblages as a function of rocky reef habitats (dominated by brown-macroalgae) and other sources of variation (abiotic and biotic factors) that potentially mediate the relationship between fishes and reef habitats. Analyses suggest that spatial variation in diversity (e.g., species and trophic) may be explained by spatial variation in depth, temperature, and composition of macroalgal habitats. At each location, only 2-3 families dominated the composition of fish assemblages, but species identities varied among locations. In a subsequent study, I assessed the fish-habitat associations from sites within the Juan Fernández Islands, an isolated eastern Pacific Island that lack large brown macroalgae. I found that, despite the close proximity of these Islands to the South American continent, fish i assemblages were mostly composed of endemic representatives from families that dominate the fish assemblages in New Zealand and Australia. Spatial variation in depth and temperature did not contribute to the observed variation in fish abundance. Instead, I found that benthic habitat-forming species (particularly foliose brown macroalgae) appeared to limit the abundance of some reef fishes. These results suggest that a mixture of large-scale (e.g., stochastic recruitment) and small-scale processes (i.e., relating to habitat heterogeneity) influence the diversity, composition and abundance of fish assemblages. Subsequently, I evaluated relationships between reef fishes and macroalgae composition across multiple sites, surveyed repeatedly over four seasons. I found that fishes were associated with different components of heterogeneity in macroalgal habitats, potentially indicating interspecific partitioning of resources that may arise from differential feeding habits and size- susceptibility to predation. Seasonal variation in the fish-habitat associations was detected, and site differences in macroalgal composition explained significant variation in the local diversity of fishes. Using a series of small-scale lab and field-based manipulative experiments, I determined the demographic and behavioural responses of reef- associated fishes to heterogeneity in the composition of brown macroalgal habitats. I found that (i) different fish species distinguished between monospecific macroalgae stands (macroalgal identity affected the abundance of 7 of 15 reef fish species); (ii) there is within-species variation in the response of fishes to macroalgal composition (suggesting ontogenetic habitat shifts); and (iii) the abundance of 5 of 7 reef fish species, and the overall structure of the local fish assemblage, varied with the composition of mixed-species macroalgal stands. Lastly, I evaluated the potential for fishes to provision demographic feedbacks to macroalgae. Specifically, I conducted a mesocosm experiment to evaluate the effects of fishes on grazing amphipods, and therefore, the potential indirect-effects of fishes on large-brown macroalgae. I found that only one of the two fish species studied reduced grazer abundance. Although the second fish species did not consume grazing amphipods, its presence altered amphipod behaviour to significantly reduce grazing efficiency on the macroalgal-host. This study illustrates how density and trait-mediated indirect interactions can have similar effects on primary producers. Overall, my observational and experimental components of this thesis emphasize the influence of heterogeneity in macroalgal structures on the breadth of habitat use for reef fishes at multiple locations. I found strong behaviourally mediated linkages between the abundance of reef fishes and composition of macroalgal stand. I also provide some evidence that mutualistic relationships may exist between kelp and associated fishes. Dedicated to my grandfather Acknowledgments Although most of the Chapters here are written in first person, I have to mention that without the support that I have received from many people and institutions, this thesis would have never to come to an end. I have to thank them all. All my family and particularly Isabel, Barbara, Maria Isabel and my father, and Katja have done everything for me to make this journey possible. In all the moments I have received their support, thanks. The completion of this thesis is indebted to my supervisors. I have to say that I have world-class researchers in my committee. I had contributions from all of them. First, I have received valuable guidance, encouragement, support, and friendship from my primary supervisor, Dr. Jeff Shima. I am impressed by the amount of knowledge that Jeff has as a marine ecologist and his writing skills. I consider myself fortunate to be his student. Second, I was pleased to have Russell Cole. Despite his claims to a lack of memory, he is a library of information regarding the ecology of fishes and statistics. I learned a lot from him particularly through the editing of this thesis. But this all started when Malcolm Francis went to Chile with Eduardo Villouta. With Malcolm’s Book of reef fishes from New Zealand, I started to get on track. Every fish scientist knows Malcolm’s work. His support of my thesis and me has been priceless. I have received incredible support and several researchers have influenced me. Special mentions are deserved to Dr. Shirley Pledger (how lucky I was to meet her, thanks for sharing your knowledge in stats and in R), KC Burns, Nicole Phillips, Joe Zuccarello, Nokuthaba Sibanda, Shane Geange and Phil Neubauer who have helped me a lot in analyzing data and commenting on v my work. From other universities and institutions I must thank Dr. Alistair Poore (University of South Wales), Dr. Michael Graham (Moss Landing Marine Lab, California), Dr. Giacomo Bernardi (University of California), Dr. Patricio Ojeda (Pontificia Universidad Católica de Chile), Dr. Alvaro Palma (Pontificia Universidad Católica de Chile), Dr. Martin Thiel (Universidad Católica del Norte, Chile), Dr. Carlos Gaymer (Universidad Católica del Norte, Chile), Dr. Clive Roberts (Museum of NZ Te Papa Tongarewa), Dr. Franz Smith (CSIRO), Dr. Andrew Stewart (Museum of NZ Te Papa Tongarewa), Clinton Duffy and Helen Kettles (Department of Conservation, New Zealand). Lastly special recognition of this work goes to Dr. Steve Swearer (University of Melbourne), Dr. Richard Taylor (Auckland University), and Dr. Stephen Hartley (Victoria University of Wellington) who have provided reviews and useful comments that improved the quality of this work. The data from this thesis involved a lot of fieldwork; I travelled and dived into many different places. In most, I was pleased to meet friends and spend long days in the field. I started here in Wellington with my friend, Anna Smith, who helped me in the first data chapter. Her support was incredible and I don’t think I would have finished without her support. Without the help of el tila (no one in Chile could mentioned Tyler Eddys’s name properly) and Fabian Ramírez (very motivated student specially when diving), the surveys at Juan Fernández Islands in Chile would have been hard to do. My trip to north New Zealand was extraordinary with my friend Phillip (filipa) Neubauer and Anto do Santos. In Tasmania Carolina Zagal, Nikita and her pelirojo (Simon) hosted me and gave me all the support and friendship I could ask for. I have to thank a very keen diver and boat master, Paul Di Benedetto, and his family who provided support and help in the field with his boat and scuba tanks while in Tasmania. Benjamin Magaña, Alejandra Perea-Blazquez, Ursula Rojas, Katja Klopfer, Pelirojo Salinas, Gareth Williams, Claudio