THE EFFECT OF INVASIVE LIONFISH ON REEF FISH COMMUNITY STRUCTURE ALONG THE MESOAMERICAN BARRIER REEF Serena Hackerott A thesis submitted to the faculty at the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Master of Science in the Department of Marine Sciences. Chapel Hill 2014 Approved by: John F. Bruno Karl D. Castillo Craig A. Layman © 2014 Serena Hackerott ALL RIGHTS RESERVED ii ABSTRACT Serena Hackerott: The effect of invasive lionfish on reef fish community structure along the Mesoamerican Barrier Reef (Under the direction of John F. Bruno) Lionfish are invasive predators, native to the Indo-Pacific, assumed to be negatively affecting Caribbean coral reefs. Small-scale studies suggest lionfish can reduce the abundance and diversity of small prey individuals. However, it is unclear whether lionfish predation affects entire reef fish communities. Our goal was to assess the effect of lionfish on coral reef fish communities across a complex reef system. We quantified fish abundance, diversity, and community composition at sixteen reefs along ~250km of the Mesoamerican Barrier Reef in Belize over five years, including the onset of the invasion. Lionfish had no effect on reef fish community structure on our sites in Belize. The effects of lionfish may be density dependent, and current densities in Belize are likely due to a combination of natural factors and lionfish removals. Because current densities have no effect on reef fish communities, additional lionfish removal efforts may not be necessary to prevent impacts. iii To my parents, Walter and Teressa Hackerott, thank you for learning to SCUBA dive from a random guy in a bar and starting the wonderful adventure that ultimately led to this research. Your passion for traveling and diving, as well as your continued support has been indispensable throughout my research career. I love you both and thank you for everything. iv ACKNOWLEDGEMENTS Thank you to my advisor, John Bruno, and my fellow lab members, Abel Valdivia and Courtney Cox, for their continued assistance throughout this project and the opportunities they have provided during my time in the Bruno lab. I would also like to thank my lab members Lindsay Carr, Rachel Gittman, and Emily Darling, and my committee members Karl Castillo and Craig Layman for their support throughout my research career at UNC, as well as field technicians Katie DuBois and Ivana Vu for their field assistance. Additional thanks to the Marine Sciences graduate students who have made this experience so much more than just an academic program. Finally, I would like to thank our funding sources including The University of North Carolina at Chapel Hill, UNC’s Office of Undergraduate Research, The National Science Foundation, The Rufford Foundation, and National Geographic’s Committee for Research and Exploration. v TABLE OF CONTENTS LIST OF TABLES.................................................................................................................viii LIST OF FIGURES..................................................................................................................ix LIST OF ABBREVIATIONS....................................................................................................x THE EFFECT OF INVASIVE LIONFISH ON REEF FISH COMMUNITY STRUCTURE ALONG THE MESOAMERICAN BARRIER REEF......................................1 Introduction....................................................................................................................1 Methods..........................................................................................................................4 2.1 Study Sites and Reef Fish Surveys..............................................................4 2.2 Reef Fish Community Structure..................................................................5 2.3 Prey Community Structure..........................................................................5 2.4 Abiotic Covariates.......................................................................................6 2.5 Analysis of Effects of the Lionfish Invasion...............................................7 Results............................................................................................................................9 Discussion....................................................................................................................11 Conclusion...................................................................................................................19 FIGURES.................................................................................................................................21 vi APPENDIX 1: SUPPLEMENTAL TABLES.........................................................................26 APPENDIX 2: SUPPLEMENTAL FIGURES........................................................................33 APPENDIX 3: SUPPLEMENTAL TEXT..............................................................................38 REFERENCES........................................................................................................................39 vii LIST OF TABLES Table S1. Site Information and Coordinates............................................................................26 Table S2. Prey Species and Sources........................................................................................27 Table S3. Coefficient Estimates and p-values for Each Model...............................................29 Table S4. Competitor Species and Sources.............................................................................31 viii LIST OF FIGURES Figure 1. Location of Survey Sites..........................................................................................21 Figure 2. Average Lionfish Abundance from 2009 to 2013....................................................22 Figure 3. Coefficient Estimates (mean ± 95% confidence interval) for Each Model........................................................................................................................23 Figure 4. Total Fish and Prey Fish Community Composition in 2010 and 2013..........................................................................................................................24 Figure 5. Lionfish Abundance in Native and Invaded Ranges and Estimated Impact Threshold....................................................................................................25 Figure S1. Boxplots of Lionfish Abundance, Prey Fish Diversity, and Total and Prey Fish Abundance........................................................................................33 Figure S2. Lionfish Abundance from 2009 to 2013 on Each Site...........................................34 Figure S3. Quantile-Quantile Plot of the Residuals of the Model of Total Fish Species Diversity................................................................................................35 Figure S4. Abundance of Native Competitors 2009-2013.......................................................36 Figure S5. Biomass of Lionfish and Native Competitors from 2009 to 2013............................................................................................................................37 ix LIST OF ABBREVIATIONS AIC Akaike's “An Information Criterion” ANOSIM Analysis of Similarity BACI Before After Control Impact MBR Mesoamerican Barrier Reef MPA Marine Protected Area NMDS Non-metric Multidimensional Scaling NTZ No-Take Zone PERMANOVA Permutational Multivariate Analysis of Variance SE Standard Error TL Total Length VIF Variance Inflation Factor x CHAPTER 1: THE EFFECT OF INVASIVE LIONFISH ON REEF FISH COMMUNITY STRUCTURE ALONG THE MESOAMERICAN BARRIER REEF Introduction Invasive species are widely recognized as a major threat to biodiversity and an important conservation priority (Bax et al. 2003, Pimentel et al. 2005, Molnar et al. 2008, Vilà et al. 2011). While the qualities conferring invasiveness of a species or “invasibility” of an ecosystem have been thoroughly explored, mostly in terrestrial ecosystems (Rejmánek and Richardson 1996, Levine and D’antonio 1999, Lonsdale 1999, Richardson and Pyšek 2006, Van Kleunen et al. 2010), studies quantifying the factors influencing the impact of an invasive species on the recipient community are less represented (Parker et al. 1999). Furthermore, the invasiveness of a species does not predict the impact it will have on invaded ecosystems (Ricciardi and Cohen 2007). Studies of invasion success can contribute to policies aimed at preventing invasions, but impact-focused studies are essential to developing conservation strategies once an invasive species has already become established. The impact of an invasion can also vary between invaded habitats, specifically across gradients of habitat connectivity. When exotic predators become invasive within isolated systems, prey populations are often decimated. For example, feral cats introduced to islands have caused an estimated 14% of the global extinctions of birds, mammals, and reptiles (Medina et al. 2011). However, invasive predators may have less of an impact on prey communities within more connected, open systems due to re-colonization through meta- population dynamics or “the rescue effect”(Gotelli 1991). 1 Indo-Pacific lionfish (Pterois volitans and Pterois miles, hereafter called “lionfish”) are one of the first exotic predators to invade an open marine system, and the first to become established across