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Ph.D. Final Countdown UNIVERSITY OF CALIFORNIA, SAN DIEGO The Ecology of Coral-Microbe Interactions A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Marine Biology by Kristen Laura Marhaver Committee in charge: Professor Stuart A. Sandin, Chair Professor Jeremy B. C. Jackson, Co-Chair Professor Eric E. Allen Professor Douglas H. Bartlett Professor Richard D. Norris Professor Forest Rohwer Professor Christopher Wills 2010 i Copyright Kristen Laura Marhaver, 2010 All rights reserved. ii The Dissertation of Kristen Laura Marhaver is approved, and it is acceptable in quality and form for publication on microfilm and electronically: Co-Chair Chair University of California, San Diego 2010 iii EPIGRAPH WHEN I heard the learn’d astronomer; When the proofs, the figures, were ranged in columns before me; When I was shown the charts and diagrams, to add, divide, and measure them; When I, sitting, heard the astronomer, where he lectured with much applause in the lecture-room; How soon, unaccountable, I became tired and sick; Till rising and gliding out, I wander’d off by myself; In the mystical moist night-air, and from time to time, Look’d up in perfect silence at the stars. Walt Whitman iv TABLE OF CONTENTS SIGNATURE PAGE ............................................................................................................. iii EPIGRAPH............................................................................................................................ iv TABLE OF CONTENTS ...................................................................................................... v LIST OF FIGURES................................................................................................................ vi LIST OF TABLES.................................................................................................................. viii ACKNOWLEDGEMENTS.................................................................................................. ix VITA ....................................................................................................................................... xv ABSTRACT ........................................................................................................................... xvi INTRODUCTION The Ecology of Coral-Microbe Interactions ................................... 1 CHAPTER 1 Microbes from adult corals cause distance-dependent mortality in nearby juveniles .................................................................................................. 9 CHAPTER 2 Observation of ciliates grazing around early post-settlement coral recruits ............................................................................................................ 41 CHAPTER 3 Effects of water column microbial environments and penicillin treatment on larval swimming and settlement behaviors in the Caribbean coral Montastraea faveolata................................................................... 46 CHAPTER 4 Observation of post-metamorphosis Montastraea faveolata polyps moving across surfaces using their tentacles...................................................... 78 CHAPTER 5 Five different antibiotics enhance survivorship but cause abnormal behavioral profiles in planula larvae of the Caribbean coral Montastraea faveolata................................................................................................ 84 CHAPTER 6 Abnormal morphologies of post-metamorphosis coral settlers exposed to the broad-spectrum antibiotic penicillin ......................................... 107 CHAPTER 7 Considering adaptive coral bleaching from a new angle ...................... 112 CHAPTER 8 Observation of bleached corals extending mesenterial filaments into nearby algal turfs ............................................................................................ 133 CHAPTER 9 Viral communities associated with healthy and bleaching corals........ 139 CONCLUSIONS................................................................................................................... 181 v LIST OF FIGURES Figure 1.1. Experimental methods.................................................................................... 29 Figure 1.2. Survivorship of Montastraea faveolata coral recruits and seawater microbial abundance vary with distance from conspecific adults .................. 30 Figure 1.3. Survivorship of M. faveolata recruits is reduced in the presence of conspecific adults .................................................................................................... 31 Figure 1.4. Survivorship of M. faveolata planula larvae is reduced in water collected near conspecific adults........................................................................... 32 Figure 1.5. Settlement of surviving M. faveolata planulae is reduced in water collected near conspecific adult colonies............................................................. 33 Figure 2.1. Ciliates grazing on and around coral settlers.............................................. 44 Figure 3.1. Life stages of the focal species Montastraea faveolata................................... 65 Figure 3.2. Swimming behavior of M. faveolata planulae in different microbial environments ........................................................................................................... 66 Figure 3.3. Proportion of surviving M. faveolata planulae swimming......................... 67 Figure 3.4. Behavioral profiles of M. faveolata planulae in water filtration and penicillin treatments ............................................................................................... 68 Figure 3.5. Effects of penicillin on rate and location of planula swimming behavior.................................................................................................................... 69 Figure 3.6. Inhibition of settlement by penicillin............................................................ 70 Figure 3.7. Swimming speed and pattern of M. faveolata larvae in control and penicillin treatments ............................................................................................... 71 Figure 4.1. Movement of post-metamorphosis M. faveolata polyps............................. 82 Figure 5.1. Survivorship of Montastraea faveolata planulae in three water filtration and five antibiotic treatments ............................................................... 98 Figure 5.2. Daily probability of planula mortality in different water filtration and antibiotic treatments ....................................................................................... 99 Figure 5.3. Behavioral profiles of Montastraea faveolata planulae in three water filtration and five antibiotic treatments. .............................................................. 100 Figure 5.4. Behavioral profiles of surviving planulae on day 1 ................................... 101 vi Figure 5.5. Behavioral profiles of surviving planulae on day 31 ................................. 102 Figure 6.1. Abnormal morphologies observed among M. faveolata settlers in penicillin-treated water .......................................................................................... 110 Figure 7.1. Montastraea faveolata colonies damaged and/or moved by wave action and flying rubble demonstrate the force of Tropical Storm Omar ...... 127 Figure 7.2. Colonies exhibit partial bleaching after being reoriented by wave action......................................................................................................................... 128 Figure 7.3. Examples of M. faveolata colonies that survived whole-colony rotations in the past ................................................................................................ 129 Figure 8.1. Bleached corals with mesenterial filaments extended into nearby algal turfs.................................................................................................................. 137 Figure 9.1. Epifluorescent micrographs of samples before and after viral particle isolation ...................................................................................................... 160 Figure 9.2. Alignment of coral virus sequences to alphaherpesvirus genomes......... 161 vii LIST OF TABLES Table 1.1. Wind speed, wind direction, and wave direction during distance- dependence field experiment with M. faveolata settlers .................................... 34 Table 5.1. Mechanisms of action and toxicity of antibiotics used in the behavior experiment............................................................................................... 103 Table 9.1. Summary of TBLASTX hits to GenBank NR and ENV databases ............. 162 Table 9.2. Summary of TBLASTX hits to GenBank NR database................................. 163 Table 9.3. Viral particle abundance in raw and homogenized DsH tissue blastate...................................................................................................................... 164 Table 9.4. TBLASTX hits to virus sequences in GenBank ............................................. 165 Table 9.5. BLASTX hits to herpesvirus genes.................................................................. 169 Table 9.6. BLASTX hits to genes from algae viruses (family Phycodnaviridae)........ 170 Table 9.7. BLASTX hits to cyanophage genes in the Phage Sequence Databank....... 173 Table 9.8. BLASTX hits to vibriophage genes ................................................................
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