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RICARDO BASSINI SILVA Chigger Mites of Brazilian RICARDO BASSINI SILVA Chigger mites of Brazilian birds: morphological studies and investigation of the presence of associated pathogens São Paulo 2021 RICARDO BASSINI SILVA Chigger mites of Brazilian birds: morphological studies and investigation of the presence of associated pathogens Thesis submitted to the Postgraduate Program in Experimental Epidemiology applied to Zoonoses of the School of Veterinary Medicine and Animal Science of the University of São Paulo to obtain the Doctor’s degree in Sciences. Department: Preventive Veterinary Medicine and Animal Health Area: Experimental Epidemiology Applied to Zoonoses Advisor: Prof. Darci Moraes Barros Battesti, Ph.D. Co-Advisor: Prof. Fernando de Castro Jacinaivicus São Paulo 2021 Total or partial reproduction of this work is permitted for academic purposes with the proper attribution of authorship and ownership of the rights. DADOS INTERNACIONAIS DE CATALOGAÇÃO NA PUBLICAÇÃO (Biblioteca Virginie Buff D’Ápice da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo) T. 4048 Silva, Ricardo Bassini FMVZ Chigger mites of Brazilian birds: morphological studies and investigation of the presence of associated pathogens / Ricardo Bassini Silva. – 2021. 552 f. : il. Título traduzido: Ácaros trombiculídeos de aves brasileiras: estudos morfológicos e investigação da presença de patógenos associados. Tese (Doutorado) – Universidade de São Paulo. Faculdade de Medicina Veterinária e Zootecnia. Departamento de Medicina Veterinária Preventiva e Saúde Animal, São Paulo, 2021. Programa de Pós-Graduação: Epidemiologia Experimental Aplicada às Zoonoses. Área de concentração: Epidemiologia Experimental Aplicada às Zoonoses. Orientadora: Profa. Dra. Darci Moraes Barros Battesti. Co-orientador: Prof. Dr. Fernando de Castro Jacinavicius. 1. Trombiculídeos. 2. Taxonomia. 3. Aves. 4. DNA. 5. Rickettsia. I. Título. Ficha catalográfica elaborada pela bibliotecária Denise Yamashita, CRB-8/8931, da FMVZ/USP. EVALUATION FORM Author: BASSINI-SILVA, Ricardo Title: Chigger mites of Brazilian birds: morphological studies and investigation of the presence of associated pathogens Thesis submitted to the Postgraduate Program in Experimental Epidemiology applied to Zoonoses of the School of Veterinary Medicine and Animal Science of the University of São Paulo to obtain the Doctor’s degree in Sciences. Date: _____/_____/_____ Committee Members Prof. _______________________________________________________________ Institution:__________________________ Decision: _________________________ Prof. _______________________________________________________________ Institution: __________________________ Decision: _________________________ Prof. _______________________________________________________________ Institution: __________________________ Decision: _________________________ Prof. _______________________________________________________________ Institution:__________________________ Decision: _________________________ Prof. _______________________________________________________________ Institution:__________________________Decision:_________________________ This thesis is dedicated to my family – Mother, father and brother are here represented ACKNOWLEDGEMENTS To my advisor Darci Moraes Barros Battesti, who helped me in all stages of the writing of this thesis and gave me valuable tips that improved it. For believing, encouraging and always being present in my nine-year scientific journey. To my great friend and co-advisor Fernando de Castro Jacinavicius, who was also present in all stages of this thesis, which at the same time helped me in my professional life, and in my personal life. And that this partnership that started nine years ago will be forever. To all the colleagues of the Laboratory of Zoological Collections (Butantan Institute), especially the friends Gabrielle Ribeiro de Andrade, Maria Cristina do Rosário, and Livia Marcia Correa. And to Antonio Domingues Brescovit, Director of the Laboratory of Zoological Collections, Cristina Anne Rheims, Researcher of the same laboratory, and Valeria Castilho Onofrio, Curator of the Acari Collection, for allowing access to the collection and development of the thesis. To Beatriz Mauricio of the Laboratory of Cellular Biology of the Butantan Institute, for providing the images obtained in the Scanning Electron Microscopy. To Erika Hingst-Zaher from Museu Biológico, Butantan Institute, to confirm and identify all birds and help in the chigger collection. To Sebastián Muñoz Leal and Marcelo Bahia Labruna, Faculty of Veterinary Medicine and Zoology at USP, to help in the molecular techniques and all the valuable suggestions that improves this thesis. To Ronald Ochoa, curator of the USNM Smithsonian Acari Collection, for having welcomed me for nine months in his collection, helped me with all the information and equipment I needed to carry out the chapters of this thesis. To Cal Welbourn, Smithsonian Institute, for his valuable suggestions and improvements in all chapters of this thesis. To Gary Bauchan, in memorian, research of the Electron & Confocal Microscopy Unit, United States Department of Agriculture, Agriculture Research Service, for the valuable information that contributed to the development of this thesis. To Debra D. Creel, Andrew Ulsamer and Armando Rosario Lebron for technical assistance and valuable feedback while I was working at the USDA. To the acarologists that provide information and suggestions in each chapter of this thesis. In special to Lee Goff (Chaminade University of Honolulu), Donald Gettinger (University of Nebraska at Lincoln), and Barry M. OConnor (University of Michigan). To the whole of my family, but especially to Ivone (mother), Carlos (father), and Rafael (brother), who was also present at all stages of this thesis, which saw all my effort and hours to write this thesis. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq no. 454907/2014-1 and 377976/2014-8) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP no. 2010/51875-9; 2017/01416-7, 2018/24667-8 and 2019/19853-0). Also, this study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. Finally, I thank all those who contributed directly to this work, and those who indirectly, knowing it or not, was present in my life. “Don't tell me the sky's the limit; When there's footprints on the moon” - Emerson Drive RESUMO BASSINI-SILVA, R. Ácaros trombiculídeos de aves brasileiras: estudos morfológicos e investigação da presença de patógenos associados. 2021. 552 p. Tese (Doutorado em Ciências) – Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, 2021. O Brasil possui 63 espécies de trombiculídeos parasitando diferentes grupos de animais. E destas, somente 8 espécies foram reportadas para aves, uma pertencente ao gênero Apolonia, duas para Blankaartia, duas para Eutrombicula, uma para Neoschoengastia e duas para Parasecia. As larvas destes ácaros podem provocar lesões profundas e pruriginosas no local da picada, com reações cutâneas intensas no hospedeiro, causando uma dermatite conhecida popularmente como trombiculíase. Em vários países, os departamentos de saúde pública se depararam com a necessidade de catalogação e conhecimento da biologia desses ácaros, por serem considerados potenciais vetores de patógenos. No Brasil, casos de Febre Maculosa Brasileira (FMB) diagnosticados em São Paulo, foram associados a esses ácaros, no entanto, o seu papel na epidemiologia de patógenos não foi confirmado. Ao final deste estudo, um catálogo de tipos da coleção UNSM foi elaborado contendo 1.026 espécies tipos. Seis espécies foram redescritas e imagens de microscopia foram fornecidas para auxiliar na descrição dessas espécies. Novos registros de localidade e associação com hospedeiros foram fornecidos para as espécies B. sinnamaryi, E. alfreddugesi, E. batatas, E. goeldii and E. tinami. Cinco espécies novas do gênero Eutrombicula foram descritas. A espécie E. butantanensis foi reestabelecida como uma espécie válida, e E. ophidica está sendo sinonimizada com E. butantanensis. Por fim, duas cepas diferentes de Rickettsia sp. foram detectadas em B. sinnamaryi and E. tinami parasitando aves no Brasil. Palavras-chave: Trombiculídeos, taxonomia, Aves, DNA, Rickettsia ABSTRACT BASSINI-SILVA, R. Chigger mites of Brazilian birds: morphological studies and investigation of the presence of associated pathogens. 2021. 552 p. Tese (Doutorado em Ciências) – Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, 2021. Brazil has 63 species of chiggers parasitizing different groups of animals. And of these, only 8 species were reported to birds, and one belongs to the genus Apolonia, two from Blankaartia, two from Eutrombicula, one from Neoschoengastia, and two from Parasecia. These mites' larvae can cause deep and itchy lesions at the bite side, with to intense skin reactions in the host, causing dermatitis popularly known as thrombiculiasis. In several countries, public health departments faced the need for cataloging and knowledge of these mites' biology as they are considered potential vectors of pathogens. In Brazil, cases of Brazilian Spotted Fever (FMB) diagnosed in São Paulo were associated with these mites because they were found in the disease's outbreaks. However, its role in the epidemiology of pathogens has not been confirmed. In this study, a type catalog of the UNSM collection was
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