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Amphibian Fungal Disease and the Cutaneous Microbiome

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Amphibian Fungal Disease and the Cutaneous Microbiome AMPHIBIAN FUNGAL DISEASE AND THE CUTANEOUS MICROBIOME A Thesis Submitted to the Faculty Of Drexel University by Patrick Joseph McLaughlin in partial fulfillment of the requirements for the degree of Doctor of Philosophy June 2015 © Copyright 2015 Patrick J. McLaughlin. All Rights Reserved. iii DEDICATIONS To my mother, who taught me more than all the textbooks and professors combined, especially about how to be a good person. To my father, who instilled in me his deep appreciation for nature, which has dictated my path ever since. To my brother, who has always been there to lean on, look up to, and save my ass. To my sister, who constantly reminds me what is truly important in life. To my Philadelphia friends for all the love, support, and beer that got me through. Lastly, to the frogs, I am sorry I had to kill some of you, I did not enjoy it, it was for science… forgive me. iv ACKNOWLEDGEMENTS This work was supported by Drexel University, ExxonMobil Foundation, Mobil Equatorial Guinea Incorporated, la Universidad Nacional de Guinea Ecuatorial, The Explorers Club, U.S. Fish & Wildlife Service, Hudson Valley Herpetological, North Carolina Museum of Natural Sciences, and the Bioko Biodiversity Protection Program. J. Rosado (Museum of Comparative Zoology, Harvard University) and J. Friel (Cornell University Museum of Vertebrates) loaned specimens in their care. Research and specimen export permits were provided by the Ministerio de Información, Cultura y Turismo, Republica de Guinea Ecuatorial, and the Facultad de Medio Ambiente. T. Butynski, G. R. Mene, A. Fertig, M. Cuzzocreo, K. Fugett, A. Byrne, N. Stanek, R. Sicheneder, R. Bell, B. Stuart, J. Owens, D. Cronin, D. B. Mene, P. Łukasik, N. Wong, S. Woloszynek, and D. Rock assisted with fieldwork, labwork, statistics, and/or general improvements to this thesis. Special thanks to my dissertation committee of G. Hearn, M. O’Connor, J. Russell, D. Blackburn, and S. Honarvar who each contributed essential guidance throughout all facets of this research. v TABLE OF CONTENTS LIST OF TABLES ..................................................................................................................... viii LIST OF FIGURES ...................................................................................................................... ix ABSTRACT ....................................................................................................................................x 1. BIOKO ISLAND AMPHIBANS ................................................................................................1 1.1 Arthroleptis bioko .....................................................................................................................6 1.2 Wolterstorffina parvipalmata ....................................................................................................7 1.3 Didynamipus sjostedti ...............................................................................................................8 1.4 Phlyctimantis boulengeri ........................................................................................................11 2. A NEW LEPTOPELIS (AMPHIBIA: ARTHROLEPTIDAE) FROM BIOKO ISLAND, EQUATORIAL GUINEA ............................................................................................................12 2.1 Abstract ...................................................................................................................................12 2.2 Introduction .............................................................................................................................12 2.3 Materials and Methods ............................................................................................................14 2.4 Species Description .................................................................................................................16 2.4.1 Holotype ...............................................................................................................................16 2.4.2 Paratypes ..............................................................................................................................16 2.4.3 Referred Materials ...............................................................................................................18 2.4.4 Diagnosis ..............................................................................................................................18 2.4.5 Description of Holotype .......................................................................................................20 2.4.6 Coloration in Preservative ....................................................................................................22 vi 2.4.7 Coloration in Life ..................................................................................................................23 2.4.8 Variation ..............................................................................................................................23 2.4.9 Molecular Divergence ..........................................................................................................23 2.4.10 Distribution and Natural History .......................................................................................23 2.4.11 Etymology ...........................................................................................................................24 2.5 Discussion ...............................................................................................................................24 3. PREVALENCE OF THE AMPHIBIAN CHYTRID PATHOGEN ( Batrachochytrium dendrobatidis ) ON BIOKO ISLAND, EQUATORIAL GUINEA ................................................27 3.1 Introduction .............................................................................................................................27 3.2 Origin and Spread of Chytridiomycosis ..................................................................................27 3.3 Materials and Methods ............................................................................................................34 3.4 Results .....................................................................................................................................37 3.5 Discussion ...............................................................................................................................44 4. CHARACTERIZATION OF THE AMPHIBIAN CUTANEOUS MICROBIOME ...............47 4.1 Introduction .............................................................................................................................47 4.2 Materials and Methods ............................................................................................................49 4.2.1 Processing Swabs .................................................................................................................52 4.2.2 Statistical Analysis ...............................................................................................................54 4.3 Results .....................................................................................................................................56 4.3.1 Metabolites: Adonis and Principle Coordinates Analysis (PCoA) ......................................56 4.3.2 Bacteria (97% OTU Composition): Adonis and Principle Coordinates Analysis (PCoA) ..60 vii 4.4 Discussion ...............................................................................................................................65 4.5 Further Analysis ......................................................................................................................66 5. LIST OF REFERENCES ..........................................................................................................67 6. APPENDIX 1: Arthroleptis bioko IUCN Red List Assessment ...............................................76 7. APPENDIX 2: Specimens Examined .......................................................................................79 8. VITA .........................................................................................................................................80 viii LIST OF TABLES 1. Amphibian Species Inventory for Bioko Island, Equatorial Guinea ..........................................5 2. Measurements of Adult Types of Leptopelis pictilis sp. nov. ...................................................19 3. Distribution of Bd Across Sampled Amphibian Species ..........................................................38 4. Distribution of Bd During Wet and Dry Seasons Across Sampling Localities ........................39 5. Amphibian Taxa Sampled for Cutaneous Bacteria and Metabolites ........................................51 6. Genus:Species Abbreviations for Sample ID ...........................................................................55 ix LIST OF FIGURES 1. Map of Bioko Island, Equatorial Guinea ....................................................................................4 2. Range Map for Didynamipus sjostedti in Pico Basilé National Park .......................................10 3. Sampling Localities for Leptopelis pictilis ................................................................................ 17 4. Leptopelis pictilis Holotype ......................................................................................................21 5. Bd Sampling Localities .............................................................................................................35
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