UNIVERSITY OF CALIFORNIA, SAN DIEGO Planktivorous Fish Link Coral Reef and Oceanic Food Webs: Causes and Consequences of Landscape-Scale Patterns in Fish Behavior, Diet and Growth A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Oceanography by Katharine Mary Winston Hanson Committee in charge: Professor James J. Leichter, Chair Professor Ian S. Abramson Professor Lihini I. Aluwihare Professor Lisa A. Levin Professor Mark D. Ohman 2011 Copyright Katharine Mary Winston Hanson, 2011 All rights reserved. The Dissertation of Katharine Mary Winston Hanson is approved, and it is acceptable in quality and form for publication on microfilm and electronically: Chair University of California, San Diego 2011 ! ! """! DEDICATION I dedicate this dissertation to my parents, Gene Paul Hanson and Mary Winston Hanson, to my daughter, Eva Marie Karaköylü, and to Dr. Peter Franks for supporting me in big ways and in small and encouraging me when I needed it the most. ! "#! EPIGRAPH “C’est une merveille de voir chacun de ces atollons, environné d’un grand banc de pierre tout autour, n’y ayant point d’artifice humain.” -François Pyrard de Laval, 1605 ! "! TABLE OF CONTENTS SIGNATURE PAGE…………………………………………………..……………...iii DEDICATION………………………………………………………….……………..iv EPIGRAPH…………………………………………………………………...………..v TABLE OF CONTENTS……………………………………………………………...vi LIST OF TABLES……………………………………………………………...….…xii LIST OF FIGURES……………………………..……………………...……...…….xiii ACKNOWLEDGEMENTS……………..………………………...……...………….xvi VITA…………….………..……………………………………….…...………...…xxvi ABSTRACT OF THE DISSERTATION………………………………………….xxvii CHAPTER 1. Introduction…………….………………………………….…………1 The coral reef paradox…………….….…………………………………………...…1 Overview of the dissertation…………….………………………………………...…9 References…………….………………………………………………….…………14 CHAPTER 2. The contribution of oceanic and reef food sources to the diet and secondary production of coral reef fishes ………………………...……….………19 Abstract…………….………………………………………………… ……………19 Introduction…………….…………………………………….……………………...20 Methods…………….………………………………………...……………………..25 Study site and species…………….………………………………………......25 Sample collection: fish…………….……………………...…………………..27 ! "#! Sample collection: zooplankton…………….……………..……………….…29 Gut content analysis…………….…………………………………………….29 Stable isotope analysis…………….………………………………………….30 Mass balance isotope mixing model of fish diet……………….……………..31 Statistical analysis…………….……………………………………...……….33 Results……………………………………………...……………………………….33 Quantifying fish diet using gut content analysis…………….…….………….33 Habitat-dependent stable isotope ratios in Dascyllus flavicaudus………....…36 Habitat-dependent stable isotope ratios in a suite of planktivorous fishes…...39 Isotope mass balance model of fish diet…………….………………….…….40 Discussion…………….………………………………………………………….…43 Acknowledgements……………………………..….……………………………….51 Tables…………….………………………………………………...……………….52 Figures…………….………………………………………………….……………..53 References…………….…………………………………………………………….75 Appendices…………….………………………………..………………………..…82 Appendix 2A. Published data on carbon and nitrogen stable isotope ratios measured in coral reef organisms…………….………….…….……………...82 Appendix 2B. Diurnal zooplanktivorous fishes common to the island of Moorea……………………………………………………….……………….86 Appendix 2C. Data on the biomass of twelve zooplankton prey groups…......88 Appendix 2D. Analytical precision and error related to stable isotope analysis of zooplankton and fish muscle tissue samples…………………………...….91 ! "##! CHAPTER 3. Selective feeding increases the contribution of oceanic zooplankton to the diet of planktivorous coral-reef fish………………………….…………...…93 Abstract…………….……………………………………………………….………93 Introduction…………….………………………………..………………………….94 Methods…………….……………………………...………………………………..97 Study location and species…………….……………………………………...97 Prey use…………….…………………………………………...…………….98 Prey availability…………….…………………………..…………………….99 Examining random feeding………………………………..…..…………….100 Feeding electivity…………….………………………………………...……101 Influence of feeding electivity on fish diet……………………..………..….103 Results…………….……………………………………..………………………...104 Prey use…………….………………………………..………………………104 Prey availability…………….……………………………..………………...105 Non-random feeding in Dascyllus flavicaudus………………...……………106 Feeding electivity…………….…………………………………………...…106 Influence of feeding electivity on fish diet……………….…….…...………107 Discussion…………….…………………………………………………...………108 Acknowledgements……………………………..….…………………………...…114 Tables……………………………………………....……………………………...115 Figures………………………………………….….………………………………120 References…………….……………………………………………………….......127 ! "###! Appendices……………………………………..….……………………………....132 Appendix 3A. Taxonomic detail of prey groups used in the study of the diet of Dascyllus flavicaudus. ………………………………………………….......132 Appendix 3B. The abundance of zooplankton groups in gut content samples and environmental samples as related to sub-sampling and enumeration methodology…………….………………………………………………...…136 Appendix 3C. Details of biomass conversions used to calculate the contribution of oceanic food sources to the diet of Dascyllus flavicaudus…………….………………………………………..………...…138 Appendix 3D. Details of the calculation of log-likelihood statistics used to evaluate the hypothesis of random feeding in Dascyllus flavicaudus……….140 Appendix 3E. Details of the calculation of forage ratios used to evaluate selective feeding in Dascyllus flavicaudus………………………………….152 CHAPTER 4. The influence of food availability and habitat quality on growth in a planktivorous reef fish ………………………………………………...…….......158 Abstract…………….………………………………........………………………...158 Introduction…………….………………………………..………………………...159 Methods…………….…………………………………...…………………………162 Study site and species……………………………………..…..….…………162 Fish growth and long-term zooplankton abundance………....…..….………163 Fish growth, consumption of zooplankton prey, and reef habitat……...…...166 Statistical analysis…………….…………………...………………………...167 ! "#! Results……………………………………………...……………………………...168 Fish growth and long-term zooplankton abundance………..…….…………168 Comparing metrics of fish growth…………………...……………………...169 Fish growth and consumption of zooplankton prey………...…………..…...170 Fish growth and reef habitat…………….………...…………………………171 Discussion…………….…………………………………………………………...172 Acknowledgements………………………………...……………………………...177 Figures………………………………………….….………………………………179 References…………………………………….……………………………….......189 Appendices…………………………………..…….………………………………195 Appendix 4A. Details of size metrics measured from juvenile fish………...195 Appendix 4B. Details of recovery rates for the 2008 and 2009 transplant experiments……………………………………………………………..…...197 Appendix 4C. Time series of zooplankton abundance sampled from four locations on Moorea’s north shore…………………………..………………198 Appendix 4D. Total length as a metric of fish growth………………………202 Appendix 4E Details of the gut content analysis for Dascyllus flavicaudus..203 CHAPTER 5. Summary of the dissertation ……………………….......................205 Review of hypotheses and main findings……………………………………..........205 Future research on plankton and planktivores in coral reef ecosystems…….............213 Tables..........................................................................................................................217 Figures.........................................................................................................................218 ! "! References...................................................................................................................219 ! "#! LIST OF TABLES CHAPTER 2 Table 2.1 The habitat association of twelve zooplankton prey groups that comprise the diet of the reef fish Dascyllus flavicaudus………………………………………........52 CHAPTER 3 Table 3.1 The habitat association of sixteen zooplankton prey groups that comprise the diet of the reef fish Dascyllus flavicaudus ……………………………………...115 Table 3.2 The occurrence of sixteen zooplankton prey groups in the diet of the reef fish Dascyllus flavicaudus. ……………………………………...............................116 Table 3.3 Log-likelihood statistics for goodness-of-fit tests of random feeding in Dascyllus flavicaudus.……………………………………........................................117 Table 3.4 Electivity designations calculated for 16 zooplankton prey groups sampled from gut contents of Dascyllus flavicaudus collected at six reef locations.….......…118 CHAPTER 5 Table 5.1 Landings of artisanal lagoon fisheries on Moorea and Tikehau islands....217 ! "##! LIST OF FIGURES CHAPTER 2 Figure 2.1 Carbon (!13C) and nitrogen (!15N) isotope ratios measured in coral reef organisms.………………………………………………................................……….53 Figure 2.2 Map of the island of Moorea, French Polynesia (bottom panel) and the island’s regional location in the South Pacific (top panel). …………….....................54 Figure 2.3 Schematic of the dominant reef habitats in Moorea and cross-shore patterns of density for three oceanic indicator zooplankton taxa and three reef indicator taxa…………................................................................................................................55 Figure 2.4 Percent contribution of three major zooplankton prey types to total prey items sampled from guts of D. flavicaudus. ……………............................................56 Figure 2.5 The percent contribution of zooplankton prey groups to total gut contents sampled from D. flavicaudus. ……………..................................................................57 Figure 2.6 The percent contribution