ECOLOGY AND EVOLUTION OF THE LIONFISH INVASION OF CARIBBEAN CORAL REEFS: RESISTANCE, ADAPTATION AND IMPACTS Andrea Anton Gamazo A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Curriculum for the Environment and Ecology. Chapel Hill 2013 Approved by: Charles Peterson Karl Castillo Joel Kingsolver Johanna Rosman Paula Whitfield ©2013 Andrea Anton Gamazo ALL RIGHTS RESERVED ii ABSTRACT ANDREA ANTON GAMAZO: Ecology and evolution of the lionfish invasion of Caribbean coral reefs: resistance, adaptation and impacts (Under the direction of Charles Peterson) The lionfish ( Pterois volitans ) invasion of the Caribbean is a notable example of the successful establishment of a predatory marine fish outside of its native range. In 20 years lionfish have spread over most of Caribbean and the western Atlantic. Lionfish densities in their new range can be up to fifteen times higher than in their native range. On reefs in the Caribbean, lionfish reduce fish populations to the point that this invasive species is considered one of the top ten most serious emerging environmental issues in the world. Native prey can be vulnerable to consumption by exotic predators with which they lack an evolutionary history. Such prey naiveté has been assumed to be a major cause of extinction for endemic species. Yet prey naiveté has been tested rigorously in few cases and never in the marine environment. In Chapter 1 and 3 of my dissertation I used metrics of predator avoidance by small, native Caribbean and Pacific fishes to quantify their responses to lionfish. Field experiments and observations revealed that Caribbean native prey do not recognize of lionfish as a predator, indicating prey naiveté towards this exotic threat. In Chapter 2 and 4, I tested biotic and environmental resistance to the early success of the lionfish invasion in two Bahamian islands and the Belizean Mesoamerican Barrier Reef. Lionfish abundance was negatively related to large grouper biomass in Belize but not in the Bahamas. Wave exposure and marine protection from iii reef fishing were also negatively related to lionfish abundance and field observations suggested that high-energy of exposed environments might be the dominant determinant of the lionfish density pattern. The direct and indirect effects of lionfish on marine ecosystems in the Caribbean are of great concern for conservation. In Chapter 4 I assessed lionfish impacts on abundance and community structure of reef-fish at large spatial scales. Surveys at 15 sites located along the Belizean Mesoamerican Barrier Reef were performed before and after the lionfish invasion. A negative effect of lionfish abundance on the reef-fish abundance and community composition was detected only 2 years after first lionfish detection on Belizean coral reefs. iv DEDICATION Para Nate y Mochuelo Todo pasa y todo queda. Caminante no hay camino sino estelas en la mar… Caminante no hay camino se hace camino al andar - Antonio Machado v ACKNOWLEDGEMENTS I love science and I am tremendously grateful to the many people who have contributed to the process of making me a better scientist. I take this opportunity to express my fondest gratitude to my advisor and mentor Pete Peterson. I cannot simply thank him enough for his support, courage, and mentorship. Without him, this dissertation would not have materialized. I am also grateful to my committee members Paula Whitfield, Joel Kingsolver, Karl Castillo, and Johanna Rosman for their guidance and support. I have been fortunate to be a part of an exceptional group of researchers at the University of North Carolina. In particular, I would like to specially thank Nate Geraldi and Beth VanDusen for their editorial help and valuable comments. This dissertation would have not been possible without collaborators Michael Simpson, Katherine Cure, Riikka Puntila, Ivana Vu, and Craig Layman. Funding for these projects has come from a number of sources. In particular, thank you to the Graduate School at UNC, the National Science Foundation, the PADI Foundation, and the Center for Global Initiatives. I am lucky to be part of a great family and to have remarkable friends. Special thanks to Nate Geraldi and my parents, and siblings for being there, love me, and be part of my life. I would also like to send a thank you across the oceans to Allende, Sira, Daniela, Marta, and Berta. In addition to science, I enjoy sports. I am grateful to Rafael Nadal for being such a great player and inspirational role model. vi TABLE OF CONTENTS List of Tables .............................................................................................................................x List of Figures .......................................................................................................................... xi Chapter 1: Prey naiveté towards an invasive marine predator as compared to native predators in reef-fish communities ............................................... 1 Abstract .......................................................................................................... 1 Introduction .................................................................................................... 1 Methods ......................................................................................................... 4 Results .......................................................................................................... 11 Discussion .....................................................................................................13 Tables ........................................................................................................... 19 Figures ..........................................................................................................22 References .................................................................................................... 31 Chapter 2: Environmental resistance to and biological facilitation of lionfish early invasion success in Bahamian coral reefs ........................................36 Abstract .........................................................................................................36 Introduction ...................................................................................................37 Methods ........................................................................................................39 Results ...........................................................................................................45 Discussion .....................................................................................................47 vii Tables ..................................................................................................................53 Figures ................................................................................................................55 Supplementary Material .....................................................................................59 References ...........................................................................................................61 Chapter 3: Comparison of anti-predator responses to lionfish in native and invasive range by small reef-fish ....................................................................................65 Abstract ...............................................................................................................65 Introduction .........................................................................................................66 Methods ..............................................................................................................68 Results .................................................................................................................74 Discussion ...........................................................................................................75 Tables ................................................................................................................. 79 Figures ................................................................................................................81 Supplementary Material .....................................................................................84 References ...........................................................................................................85 Chapter 4: Effects of biotic and abiotic factors on the early lionfish invasion of Belizean coral reefs and its impacts ...............................................................89 Abstract ...............................................................................................................89 Introduction .........................................................................................................90 Methods ..............................................................................................................92 Results .................................................................................................................96 Discussion ...........................................................................................................98 Tables ................................................................................................................102 viii Figures ..............................................................................................................103 Supplementary