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The Biogeography, Phylogeny, and Dispersal of Freshwater and Terrestrial Free-Living Ciliates in Florida, USA

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The Biogeography, Phylogeny, and Dispersal of Freshwater and Terrestrial Free-Living Ciliates in Florida, USA The biogeography, phylogeny, and dispersal of freshwater and terrestrial free-living ciliates in Florida, USA A thesis submitted for the degree of DOCTOR OF PHILOSOPHY Hunter Nicholas Hines Faculty of Science and Technology Bournemouth University March 2019 This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognize that its copyright rests with its author and due acknowledgement must always be made of the use of any material contained in, or derived from, this thesis. i ABSTRACT Microbial ecology: the biogeography, phylogeny, and dispersal of ciliates in Florida, USA Hunter Nicholas Hines As organisms at the foundations of food webs, ciliated protozoa are an integral part of the microbial loop and the ecosystems they support. This project was designed to explore the freshwater and terrestrial ciliate populations of sub-tropical Florida, USA, an uninvestigated geographic range with similar environmental characteristics to those found in previously- studied locations in sub-tropical and tropical Africa. Through extensive sample collection covering a wide variety of habitats, morphological and molecular techniques were used to describe the target ciliate taxa present in these environments and to determine their presence/absence and their geographical distribution. Of special interest were the ‘flagship’ ciliate species found, with some recorded outside of Africa for the first time, and the first records made for the Americas of both freshwater and terrestrial flagships. As a result of major sampling, some ciliate species were found to be new to science, and these are described in detail at both morphological and molecular levels. The 18S rRNA gene sequences were obtained for several species, some for the very first time, and are provided here to investigate phylogeny. Long-term monitoring of four sites produced a large dataset of water parameters and occurrence of target ciliate species, allowing a better understanding of the niche requirements for these ciliates. The development of dynamic models was undertaken to enhance discussions surrounding potential dispersal mechanisms of target ciliate species over large distances. Agent based models were constructed to visualize microcosm interactions of a target ciliate species to various environmental stimuli. ii LIST OF CONTENTS 1. A REVIEW OF THE LITERATURE AND AN OVERVIEW OF THE PROJECT……………………………………………………...... 1 1.1 Background………………………………………………………… 1 1.2 ‘Flagship species’ as a conservation biology concept ……………. 2 1.3 The term ‘Flagship’ as it applies to ciliates……………………….. 3 1.4 Is ‘everything everywhere’? ………………………………………. 4 1.5 Why was this study needed? …………………………...………….. 6 1.6 Aim and Objectives ……………………………………………...… 8 2. METHODS …………………………………………………………….…… 11 2.1. Study sites and sample collection…………………….…………… 11 2.2 Ciliate and algal cultures……………………………...…………… 18 2.3 Observations and microscopy……………………………………… 19 2.4 Molecular biology …………………………………………….…… 23 2.5 Soil samples …………………………………………………….….. 27 2.6 Data analysis ………………………………………………………. 29 2.7 Applications …………………………………………...…………… 29 3. FLAGSHIP FRESHWATER CILIATES OF FLORIDA ………………. 30 3.1 Hypothesis …………………………………………….…………… 30 3.2 Introduction ……………………………………………………….. 30 3.3 Methods ……………………………………………………………. 31 3.4 Loxodes rex …………………………………………………….….. 31 3.5 Other flagship ciliates found in Florida ………………………….. 51 3.6 Conclusions ………………………………………………..……… 65 4. FRESHWATER CILIATE SPECIES NEW TO SCIENCE DISCOVERED IN FLORIDA …………………………………………………………...….. 67 4.1 Hypothesis……………………………………………..…………… 67 iii 4.2 Introduction ……………………………………………..………… 67 4.3 Methods ……………………………………………………..…….. 68 4.4 Sonderia n. sp. a ciliate species new to science …………..……… 68 4.5 A brackish-water Sonderia ………………………………………… 80 4.6 Novel Colpodea species ……………………………………...…….. 81 4.7 Two new species of Prorodon …………………………..………… 83 4.8 Pseudoblepharisma tenue var. viride sp. ……………………..….. 89 4.9 Discussion …………………………………………………..…….. 95 4.10 Conclusions …………………………………………………..….. 103 5. FLAGSHIP SOIL CILIATES OF FLORIDA …………………………… 104 5.1 Hypothesis ………………………………………………………….. 104 5.2 Introduction ……………………………………………………..…. 104 5.3 Methods …………………………………………………………….. 106 5.4 Condylostomides etoschensis ……………………………………… 108 5.5 Condylostomides coeruleus ……………………………….………. 112 5.6 Laboratory cultures ……………………………………….………. 115 5.7 Discussion …………………………………………………….…… 117 5.8 Conclusions …………………………………………….………….. 119 6. COMBINING DYNAMIC MODELING WITH INVESTIGATIONS INTO CILIATE BIOGEOGRAPHY AND ECOLOGY ........................................... 121 6.1 Hypothesis ……………………………………………...………….. 121 6.2 Overview ……………………………………………………....…… 121 6.3 Introduction ……………………………………………………….. 122 6.4 Background ………………………………………………..………. 126 6.5 Methodology ……………………………………………..………… 132 6.6 Dispersal Models ………………………………………………..…. 141 6.7 Bottle Model ………………………………………………...……… 142 6.8 Results …………………………………………………………….... 145 6.9 Discussion …………………………………………………………. 159 6.10 Conclusions ………………………………………………...…….. 164 iv 7. CONCLUSIONS, DISSEMINATION AND FUTURE DIRECTIONS … 166 7.1 Flagship freshwater ciliates of Florida …………………………… 166 7.2 Freshwater ciliate species new to science discovered in Florida …..167 7.3 Soil ciliates of Florida ………………………………………………168 7.4 Combining dynamic modeling with investigations into ciliate Biogeography and ecology……………………………….…………….. 168 7.5 Outreach and dissemination of results through Social Media: Instagram ……………………………………………………… 169 7.6 Overall conclusions …………………………………….………….. 171 7.7 Limitations of study …………………………………...…………… 172 7.8 Future directions for research …………………………………….. 173 REFERENCES ………………………………………………………...……… 176 APPENDIX ………………………………………………………...………….. 201 v ACKNOWLEDGEMENTS Thanks to all members of my supervisory team, in particular: Dr. Genoveva F. Esteban (BU) for her enthusiastic and constant support throughout the project. Although often physically separated, Dr. Esteban was never more than a ‘ding’ away on the cellphone, providing an incredible wealth of knowledge and assistance as well as discussions in real time. I thank Dr. Esteban for inspiring me to pursue a PhD, and providing me all the necessary training and passion along the way to make it a reality. Dr. Peter J. McCarthy (HBOI) for his patience, constant involvement, and unwavering interest throughout the project at all stages. Dr. McCarthy went well beyond his duties by accompanying me on nearly all sampling trips, including the frequent sampling for long-term monitoring, and large transects into unexplored territory to collect water metadata. Sampling ciliates in wild subtropical Florida is extreme, with temperatures often >32°C, and high (60-90%) humidity in full sun very common. Constant mosquitoes and other insect pests, as well large reptiles (venomous snakes and alligators) were an omnipresent factor of Florida sampling. I am grateful for his perseverance in safeguarding the success of this project. Bournemouth University: Thanks to Louise Pearson of the Graduate College for her assistance. FAU Harbor Branch Oceanographic Institute: Thanks to all members of the McCarthy Microbiology lab (MBBR) at HBOI. The following members are acknowledged for their helpful contributions throughout the project. Research Technician Dedra Harmody for her extreme patience and availability to assist with even the most annoying of questions throughout the entire project. Dee was able to (literally) put out all fires, and was instrumental in optimizing my performance with some equipment, and developing additional microbiology laboratory skills. Dr. Gabrielle Barbarite was a PhD student at the time I started this project and was instrumental in showing me the workings of the lab and campus. Dr. Barbarite was also extremely helpful by assisting in the creation of poster presentations, and helped me develop skills used in figure production. vi PhD student David J. Bradshaw II is acknowledged for assisting with obtaining some of the soil metadata presented here. David was a willing understudy on several local sampling occasions and was luckily quite skilled with a machete. Thanks to librarian Pamela Alderman for tracking down even the most obscure of old texts. Other: Paula L. Hunter is acknowledged for her assistance with proofreading and overall support throughout. Dr. Joseph J. Abram, a PhD student at the time, was hosted at HBOI for several weeks and worked directly alongside me as the computer coding expert, assisting in creating the model codes and perfecting user interfaces for the modeling aspects of this project. Travel: Thanks goes to the late Dr. John C. Clamp, who I never had the privilege of meeting, but was instrumental in obtaining grants used for travel during this project. Through the IRCN-BC [grant number NSF-DEB 1136580, USA] during 2016-2017 travel was awarded for conference attendance. I am especially grateful to the late Dr. Dennis Lynn, whom I had the privilege of meeting twice at international conferences. He was instrumental in obtaining and issuing travel funds to me via the Holtz-Connor Award with ISOP for 2015, 2017, and 2018. The project benefited further from his careful analysis and discussions with me during my poster presentations at the conferences. Further travel support was provided by the Microbiology Society (UK) in 2017 and the Society for Applied Microbiology (UK) in 2018. vii Declaration I declare that the work in this thesis was made in accordance with the requirements of the University’s Code of
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