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Intestinal Protozoa in Wildlife: Parasite Transmission at the Wildlife-Human-Domestic Animal Interface

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Intestinal Protozoa in Wildlife: Parasite Transmission at the Wildlife-Human-Domestic Animal Interface Intestinal Protozoa in Wildlife: parasite transmission at the wildlife-human-domestic animal interface Philosophiae Doctor (PhD) Thesis John James Debenham Department of Companion Animal Clinical Sciences Faculty of Veterinary Medicine Norwegian University of Life Sciences Adamstuen (2017) Thesis number 2017:56 ISSN 1894-6402 ISBN 978-82-575-1998-8 1 2 To my dearest Lilly, may science and a caring heart guide you through life. 3 4 1. Contents 1. Contents ........................................................................................................ 5 2. Acknowledgements ...................................................................................... 7 3. Abbreviations .............................................................................................. 11 4. Scientific Papers ......................................................................................... 13 5. Summary ..................................................................................................... 15 6. Sammendrag (Norwegian summary) .......................................................... 17 7. Introduction ................................................................................................ 19 7.1 Background ............................................................................................................. 19 7.2 Nomenclature and taxonomy .................................................................................. 21 7.3 Infection and transmission ...................................................................................... 26 7.4 Diagnosis ................................................................................................................ 31 7.5 Clinical disease ....................................................................................................... 34 7.6 Epidemiology .......................................................................................................... 35 7.7 Emerging diseases at the wildlife–human–domestic animal interfaces.................. 39 7.8 Disease: a major conservation concern ................................................................... 42 7.9 Knowledge gaps ...................................................................................................... 43 8. Aims of the Study ....................................................................................... 45 9. Summary of the papers ............................................................................... 47 10. Materials and Methods ............................................................................ 51 10.1 Target wildlife populations ..................................................................................... 51 10.2 Collecting faeces in the field .................................................................................. 53 10.3 Faecal preservation ................................................................................................. 54 10.4 Concentration techniques ........................................................................................ 55 10.5 Oocyst sporulation .................................................................................................. 56 10.6 Oocyst description .................................................................................................. 56 10.7 Immunomagnetic separation ................................................................................... 56 10.8 Immunofluorescent antibody testing ...................................................................... 56 10.9 DNA isolation ......................................................................................................... 57 10.10 Conventional polymerase chain reaction ............................................................ 57 10.11 Sanger sequencing ............................................................................................... 58 10.12 GenBank survey .................................................................................................. 60 5 10.13 Sequence alignment ............................................................................................ 61 10.14 Phylogenetic tree construction and annotation ................................................... 61 10.15 Testing for phylogenetic incongruence ............................................................... 62 10.16 Statistics .............................................................................................................. 62 11. Results and General Discussion .............................................................. 63 11.1 Prevalence of Giardia in NHPs .............................................................................. 63 11.2 Molecular characterization of Giardia in NHPs ..................................................... 66 11.3 Meta-analysis of G. duodenalis isolates in NHPs .................................................. 69 11.4 Cryptosporidium in NHPs ...................................................................................... 73 11.5 Entamoeba in urban-living wild rhesus macaques ................................................. 75 11.6 Eimeria in wild ungulates at the wildlife-livestock interface ................................. 76 11.7 Giardia and Cryptosporidium in wild ungulates .................................................... 83 11.8 Giardia in wild Swedish red foxes ......................................................................... 84 11.9 Giardia and Cryptosporidium in captive Norwegian reptiles ................................ 86 12. Concluding remarks and future perspectives .......................................... 89 13. References ............................................................................................... 93 14. Compilation of papers ………………………………………………..115 6 2. Acknowledgements Tonje Brinchmann You are the source of all my energy and happiness, and have been the pillar I leant on over the years as I toiled on this thesis. Lucy J. Robertson Not only a dear friend and academic supervisor, Lucy you have become one of my life mentors, to who’s standards I strive, and for whom I wish to make proud. You took me under your wing when I first wandered the streets of Oslo, and it has been such a great scientific journey since then. Your brilliant mind, endless dedication, and encouraging energy are all that one could wish for in a supervisor and mentor. Fred Midtgaard Thank you for encouraging me to seek and pursue a career in the natural sciences, and for helping to manage the logistics of remote field work in Africa. I will always remember those hot sweaty days driving around the savanna in search of ‘Gnu bæsj. Ellen Skancke Thank you for your kind words and support, not only through this PhD and my scientific pursuits, but also during my time as a newly graduated intern in the small animal clinic. Your ability to combine a successful career as a leading veterinary clinician, educator and scientist, is something that I strive towards. Kristoffer Tysnes You have been a great mate and big brother over the last years, always ready to lend a helping hand in the lab or with some useful advice. I can see that the future for you in research and education is bright, and look forward to watching you morph into the tweed-jacket wearing, white haired professor I see lurking under your skin today. Ann Margaret Grøndahl, Anna Vigdis Eggertsdottir, & Anne Storset Thank you for being such warm and encouraging leaders, and for believing in me and taking a gamble on the field of zoo / wildlife / exotics. Never did I come to your offices and leave with a “no”, and I really value your dedication to finding a solution that was in line with my own personal ambitions. Jan Šlapeta Thank you for first pushing me down the road of science when I was still in vet school. Your enthusiasm and drive for the truth were contagious. You also taught me that a 7 manuscript draft covered in red was a positive thing, something which has served me well whilst under the reign of LJR. Debby Cox Thank you for being one of my life mentors, for challenging the way I look at the world, and for encouraging me to follow my desire to conserve nature. Without your help, much of the work on primates in this thesis would not have been possible. Robert Johnson Thank you for being both a friend and a mentor, for first pointing me in the direction of Jan, and encouraging me to align myself with those that will teach me something. You have taught me the importance of being patient, to treat the janitor as you would the king, and that if you are tough enough, not even a brown snake can take you down. Parasitology lab mates Kjersti Utaaker, Jemere B. Harito, Jonathan Myhren, and Nina Myhr. Thank you for making the lab such a fun place to be, and for there always being someone to share a cup of tea with, no matter what day / time it is. Hanna Landuyt, Freya Cools, Sandhya Khunger, & Omar Ismail You are all great scientists and have been a pleasure to work with. Without your hard work and dedication, some of the work presented here would not have been possible, and for that I am deeply grateful. Karin Troell Thank you for being a fellow agent in Operation Fox, for helping me pick myself up after repeated PCR fails, and for pushing the agenda of wildlife parasitology. Rebeca Atencia, the staff and the chimps at the Jane Goodall Institute’s Tchimpounga Chimpanzee Rehabilitation Centre. Thank you for the permission and the pleasure to work with
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