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The Salmon Louse Lepeophtheirus Salmonis (Caligidae) As a Vector of Aeromonas Salmonicida

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The Salmon Louse Lepeophtheirus Salmonis (Caligidae) As a Vector of Aeromonas Salmonicida THE SALMON LOUSE LEPEOPHTHEIRUS SALMONIS (CALIGIDAE) AS A VECTOR OF AEROMONAS SALMONICIDA by Colin William Novak B.Sc., Vancouver Island University, 2009 A THESIS SUBMITTED IN PARTIAL FULLFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (Animal Science) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) July 2013 © Colin William Novak, 2013 Abstract The sea louse, Lepeophtheirus salmonis, has been hypothesized to be a vector of fish pathogens and previous studies have isolated viral and bacterial pathogens from L. salmonis parasitizing farmed salmon. To examine the potential transmission of A. salmonicida by preadult and adult L. salmonis via parasitism of Atlantic salmon (Salmo salar), an in vivo bacteria-parasite challenge model was tested. Two pathogen challenge trials were performed, in which sea lice from donor (Aeromonas salmonicida-injected) fish were allocated among recipient fish for 14 days. Three hypotheses were examined: (i.) L. salmonis can acquire A. salmonicida from donor fish via parasitism; (ii.) A. salmonicida-exposed sea lice can transmit the pathogen to recipient Atlantic salmon via parasitism and (iii.) L. salmonis and A. salmonicida infections can cause synergistic effects on host fish. Sea lice acquired A. salmonicida externally (Trial 1 and 2, 100%) and internally (Trial 1, 100%) from parasitizing donor fish. Trial 1 (~44g fish) demonstrated a successful transfer of bacteria from lice to salmon (mucus, 100%; kidney, 77.3%), with a decrease (t = 5.29, df = 6, p = 0.00186) in mean fish condition factor and 59.1% cumulative fish mortality. Conversely, there was no evidence of bacteria transfer, no fish mortality and no decrease in mean fish condition factor in Trial 2 (~155g fish). In addition, histological examination revealed widespread inflammatory responses in small salmon (~46 g) infected with A. salmonicida and sea lice. Thus, preadult and adult L. salmonis can acquire and transmit A. salmonicida to recipient fish via parasitism under experimental conditions. However, the following conditions of pathogen, environment and host are required: (i.) a large inoculum of A. salmonicida (106 - 107 colony forming units (CFU) mL-1), (ii.) internal acquisition of bacteria by sea lice and, (iii.) young Atlantic salmon post-smolts (~44g) as hosts. ii Preface Chapter 2 has been submitted for publication. I am first author and I wrote most (~95%) of the manuscript. The section on sea lice in A. salmonicida water baths was originally drafted by D. E. Barker and is based on work conducted by D. L. Lewis, K. Verkaik and B. Collicutt at Vancouver Island University (VIU). I was responsible for the in vivo bacteria-parasite challenge models containing sea lice, A. salmonicida and Atlantic salmon, conducted fish and sea lice sampling, and performed daily water parameter tests. This research was performed under VIU animal use protocols 2010-05 TR (15/6/2010 – 14/6/2011) and 2010-05 TR-1 (15/6/2011 – 15/6/2012). Some aspects of chapter 2 have been published as a long abstract in the Aquaculture Association of Canada 2011 conference proceedings. Novak, C., Barker, D. and McKinley, S. 2011. First evidence of the salmon louse, Lepeophtheirus salmonis (Caligidae), as a vector of Aeromonas salmonicida. AAC Special Publication. 20:84-87. I conducted all testing and wrote the manuscript. The Appendices section is based on work conducted in the Centre of Shellfish Research building (VIU) and the Pacific Biological Station (PBS) in Nanaimo, BC. I conducted most of the testing. The skin plugs and histology performed in section “B-Pilot Study” was conducted by L. M. Braden (Ph.D. candidate, University of Victoria), and was not used in her thesis. iii Table of Contents Abstract ........................................................................................................................................ ii Preface ......................................................................................................................................... iii Table of Contents ....................................................................................................................... iv List of Tables .............................................................................................................................. vi List of Figures ............................................................................................................................ vii List of Abbreviations ............................................................................................................... viii Acknowledgements ..................................................................................................................... x Dedication ................................................................................................................................... xi 1 Introduction ..................................................................................................................... 1 1.1 Ectoparasites as Vectors ............................................................................................. 1 1.2 Sea Lice as Vectors ..................................................................................................... 3 1.3 Aeromonas salmonicida as a Model Pathogen ........................................................... 9 1.4 Objectives ................................................................................................................. 12 2 Transmission of Aeromonas salmonicida Via a Possible Vector: the Salmon Louse Lepeophtheirus salmonis (Caligidae) ................................................................ 14 2.1 Introduction ............................................................................................................... 14 2.2 Materials and Methods .............................................................................................. 17 2.2.1 Sea Lice Collection ................................................................................................ 17 2.2.2 Experimental Fish and Holding Conditions ........................................................... 18 2.2.3 Aeromonas salmonicida Preparation ..................................................................... 19 2.2.4 Bacteriology and A. salmonicida Confirmation from Lice and Fish ..................... 19 2.2.5 Sea lice and A. salmonicida Challenges ................................................................ 20 2.2.6 Data Analyses ........................................................................................................ 22 2.3 Results ....................................................................................................................... 24 2.3.1 Hypothesis 1........................................................................................................... 24 iv 2.3.2 Hypothesis 2........................................................................................................... 25 2.3.3 Hypothesis 3........................................................................................................... 26 2.4 Discussion ................................................................................................................. 32 3 General Discussion ........................................................................................................ 38 3.1 Sea Lice Acquisition of A. salmonicida .................................................................... 38 3.2 Aeromonas salmonicida Transmission Via Sea Lice................................................ 41 3.3 Pilot Experiment ....................................................................................................... 46 3.4 Serendipitous Discoveries ......................................................................................... 48 3.5 Future Research ........................................................................................................ 49 3.6 Research Implications ............................................................................................... 51 Works Cited ............................................................................................................................... 54 Appendices ................................................................................................................................. 65 Appendix A: Supplemental Data .................................................................................... 65 Appendix B: Pilot Study ................................................................................................. 67 Appendix C: Serendipitous Discoveries ......................................................................... 70 v List of Tables Table 2.1 Husbandry Conditions of Experimental Fish and Sea Lice Density .......................... 24 Table 2.2 Data Collected from Sea Lice Parasitizing Experimental Fish................................... 29 Table A.1 Mean Seawater Parameters in Tanks Containing Treatment Fish ............................. 66 vi List of Figures Figure 1.1 Lepeophtheirus salmonis Life Cycle .................................................................... 4 Figure 2.1 Mean Daily Cumulative Percent Mortality of Salmo salar Parasitized with Aeromonas salmonicida-infected Sea Lice................................................. 30 Figure 2.2 Mean Fish Condition Factor of Reference and Recipient S. salar Before and After Lepeophtheirus salmonis Infections
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