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Faculdade De Medicina Veterinária UNIVERSIDADE DE LISBOA Faculdade de Medicina Veterinária VECTOR-BORNE PATHOGENS FOUND IN CARNIVORES IN WILD NAMIBIA MARIA CAROLINA REGATEIRO MACHADO E COSTA CONSTITUIÇÃO DO JÚRI: ORIENTADOR Doutor Virgílio da Silva Almeida Doctor Georg von Samson-Himmelstjerna Doutor Luís Manuel Madeira de Carvalho Doutora Solange Judite Roque Coelho CO-ORIENTADOR Alves Gil Doutor Luís Manuel Madeira de Carvalho 2019 LISBOA UNIVERSIDADE DE LISBOA Faculdade de Medicina Veterinária VECTOR-BORNE PATHOGENS FOUND IN CARNIVORES IN WILD NAMIBIA MARIA CAROLINA REGATEIRO MACHADO E COSTA DISSERTAÇÃO DE MESTRADO INTEGRADO EM MEDICINA VETERINÁRIA ORIENTADOR CONSTITUIÇÃO DO JÚRI: Doctor Georg von Samson-Himmelstjerna Doutor Virgílio da Silva Almeida Doutor Luís Manuel Madeira de Carvalho CO-ORIENTADOR Doutora Solange Judite Roque Coelho Doutor Luís Manuel Madeira de Carvalho Alves Gil 2019 LISBOA To H, who first introduced me to the magic and wonders of animals vi Acknowledgements I would like to thank first and foremost to Doctor Jürgen Krücken, my closest supervisor at the Institut für Parasitologie und Tropenveterinärmedizin in Berlin for all the patience and explanations and all the help he provided me with. His wisdom and guidance were crucial to this dissertation and my knowledge has grown immensely whilst under his wing. To my supervisor Professor Doctor Georg von Samson-Himmelstjerna I am deeply grateful, for welcoming me to his incredible laboratory, giving me a chance to work alongside some incredible scientists, even though I didn’t even speak German. Thank you for investing in me. I would also like to express my wholehearted appreciation for Professor Doctor Luís Madeira de Carvalho, for always believing in me and in my abilities. Thank you so much for all the support and friendship. I also want to thank Flávia and Mariana, my Portuguese speaking “partners in crime” in Berlin, without whom my experience would definitely not have been the same. Flávia for not only mentoring me, but also for teaching me persistence and how to see the good things in life, but most importantly for all the special memories in this brand new really cold city. And Mariana, for bringing joy and light and always laughing with me, even when we were way out of our depth and didn’t know what we were doing. I am also really grateful for everyone at the Institute, especially Sabrina and all the PhD students, with their good disposition and patience for all of my questions and doubts and for teaching me and giving me some of their time without a second thought. Monika and Catarina as well, for being a part of this project and doing some of the work. And lastly I would like to thank Bettina Wachter, Gabor Czirják, Marion East and Ortwin Aschenborn, without them this project would have never existed. To my girls from FMV, Bina, Tina, Lenka, Mer e Bea for putting up with me. I have grown, changed and been through a lot during this past few years but you have made everything better and easier, and I could not have asked for better company and friends. Words cannot express how lucky I am to have you in my life and to have shared this journey with you, forever as minhas linduxas. To my incredible friends Rita, Bea, Mary, Ana, Mafaldas, Herberto, Miguel, Monty e Bernardo, for all the love and support and for accepting me exactly as I am, weirdness and all. And to everyone else who has crossed my life and contributed somehow to the person I am today, I am forever grateful. And lastly to my family, for your unconditional love. Thank you Avó, for not understanding what I was doing, but still supporting me through it. Thank you Isinha, Nena and Lu for becoming a part of my family, even though you were not in it initially. Thank you Pai for your constant support, interest and for showing me that constantly wanting to know more is perfectly normal. Thank you Henrique for shining a light on me from wherever you are. Thank you Maggie for being the best sister I could have asked for, and for being weird and random with me. And lastly, thank you Mãe, my biggest rock, for raising me and giving everything you had to your children, for being the most incredible person I know and one of my major inspirations. Love every single one of you with all my heart. vii This study was a partnership between the Institute for Parasitology and Tropical Veterinary Medicine of Freie Universität in Berlin, the Leibniz Institute for Zoo and Wildlife Research and the Research Training Group 2046 "Parasite Infections: From Experimental Models to Natural Systems" viii Abstract Vector-borne pathogens found in carnivores in wild Namibia This dissertation aimed to identify and molecularly characterize vector-borne pathogens from several parasite families, all possessing stages found in peripheral blood, from a wide variety of free-ranging carnivores living in Namibia, in the southern part of Africa. Blood samples collected from 9 bat-eared foxes (Otocyon megalotis), 17 brown hyenas (Parahyaena brunnea), 19 spotted hyenas (Crocuta crocuta) and 85 cheetahs (Acinonyx jubatus) were screened by Polymerase Chain Reactions (PCRs) and tested for pathogens of the Onchocercidae family, the order Piroplasmida, bacteria from the Anaplasmataceae and the Rickettsiaceae families and, lastly, the Hepatozoidae family. The PCRs targeted both the ITS-2 and 12S, 18S, 16S, 18S and 18S rRNA genes respectively and were followed by nucleotide sequencing. In total, sampled animals showed a 43.1% rate of Onchocercidae infection, 67.7% of Piroplasmida, 60% of them were positive for Anaplasmataceae, 10% for Rickettsiaceae and Hepatozoidae were detected in 47.7% of them. Obtained filaroid sequences showed high homologies with both Acanthocheilonema reconditum and Acanthocheilonema dracunculoides and further phylogenetic analysis were performed in both brown and spotted hyenas, with the construction of a phylogenetic tree. Piroplasmida results were not studied any further. For Anaplasmataceae, subsequent sequencing results indicated high similarity with both Anaplasma phagocytophilum and Anaplasma platys and varied PCR protocols were conducted in order to differentiate between these organisms, but no conclusions were reached. The Rickettsiaceae found displayed high homologies with Rickettsia raoultii. And finally, the Hepatozoidae infection showed to be a mixed one with both Hepatozoon canis and Hepatozoon felis. These results are important not only on a conservation level for the infected host species, but are also relevant for domestic animals coexisting in the surrounding areas, as well as humans, especially since a few of the parasites found may have zoonotic potential. Future studies should focus on understanding vectors, transmission routes, infection dynamics and host specificity in order to better evaluate the possible danger these infections may withhold. Key-words: Bat-eared fox; Brown hyena; Spotted hyena; Cheetah; Parasitology; Wildlife; Africa; Namibia; Acanthocheilonema; Anaplasma; Rickettsia; Hepatozoon. ix Resumo Agentes patogénicos transmitidos por vetores presentes em carnívoros na Namíbia Esta dissertação teve como principal objetivo identificar e caracterizar molecularmente agentes patogénicos transmitidos por vetores de várias famílias parasitárias, com o aspeto em comum de todas possuírem fases do desenvolvimento encontradas no sangue, de espécies variadas de carnívoros selvagens que habitam na Namíbia, no Sul de África. Foram testadas amostras sanguíneas de 9 raposas-orelhas-de-morcego (Otocyon megalotis), 17 hienas-castanhas (Parahyaena brunnea), 19 hienas-malhadas (Crocuta crocuta) e 85 chitas (Acinonyx jubatus) por PCR e analisadas para pesquisa de parasitas da família Onchocercidae, da ordem Piroplasmida, bactérias das famílias Anaplasmataceae e Rickettsiaceae e, finalmente, da família Hepatozoidae. Os PCRs foram direcionados aos genes do rRNA ITS-2 e 12S, 18S, 16S, 18S e 18S respetivamente e foram seguidos de sequenciação de nucleótidos. Na totalidade, os animais testados mostraram uma taxa de infeção de 43.1% por Onchocercidae, de 67.7% de Piroplasmida, 60% deles tiveram resultados positivos para Anaplasmataceae, 10% para Rickettsiaceae e Hepatozoidae foram detetados em 47.7% da população. As sequências obtidas de filarídeos, mostraram possuir elevadas homologias com Acanthocheilonema reconditum e Acanthocheilonema dracunculoides, e estudos filogenéticos mais intensivos foram realizados, nomeadamente uma árvore filogenética que inclui ambas as espécies de hienas. Os resultados relativos a Piroplasmida não foram aprofundados. Para as Anaplasmataceae, as sequenciações subsequentes indicaram elevada similaridade com Anaplasma phagocytophilum e Anaplasma platys e múltiplos protocolos de PCRs foram efetuados, com o intuito de diferenciar entre estas duas espécies, mas não foram retiradas quaisquer conclusões. As Rickettsiaceae presentes evidenciaram fortes semelhanças com Rickettsia raoultii. E finalmente, as infeções por Hepatozoidae mostraram ser uma infeção mista por ambos Hepatozoon canis e Hepatozoon felis. A importância destes resultados não se limita apenas à conservação das espécies animais em causa, mas são também relevantes em termos dos animais domésticos coabitantes na mesma região, assim como humanos, especialmente tendo em conta o possível potencial zoonótico de algumas espécies parasitárias. Estudos futuros devem ter como principais objetivos o estudo dos vetores respetivos, tipo de transmissão, dinâmica da infeção e especificidade parasitária, para melhor avaliar os possíveis perigos que podem advir
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