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The Best Paper Ever University of São Paulo “Luiz de Queiroz” College of Agriculture Taxonomic studies of Macrochelidae mites (Acari: Mesostigmata) and their potential use to control Stomoxys calcitrans and Musca domestica (Diptera: Muscidae) Letícia Henrique de Azevedo Thesis presented to obtain the degree of Doctor in Science. Area: Entomology Piracicaba 2017 Letícia Henrique de Azevedo Agronomist Taxonomic studies of Macrochelidae mites (Acari: Mesostigmata) and their potential use to control Stomoxys calcitrans and Musca domestica (Diptera: Muscidae) Advisor: Prof. Dr. GILBERTO JOSÉ DE MORAES Thesis presented to obtain the degree of Doctor in Science. Area: Entomology Piracicaba 2017 2 Dados Internacionais de Catalogação na Publicação DIVISÃO DE BIBLIOTECA – DIBD/ESALQ/USP Azevedo, Letícia Henrique de Taxonomic studies of Macrochelidae mites (Acari: Mesostigmata) and their potential use to control Stomoxys calcitrans and Musca domestica (Diptera: Muscidae) / Letícia Henrique de Azevedo. - - Piracicaba, 2017. 276 p. Tese (Doutorado) - - USP / Escola Superior de Agricultura “Luiz de Queiroz”. 1. Controle biológico 2. Catálogo 3. Ácaros predadores 4. Mosca-dos- estábulos I. Título 3 This work is especially dedicated To GOD My mother Maria Paula Henrique da Silva Azevedo My husband Diego Luis Prado My brother Matheus Henrique de Azevedo For all the love and support offered to me To Prof. Dr. Gilberto José de Moraes For his valuable guidance, friendship and recognition of my work Special thanks 4 ACKNOWLEDGEMENTS I am grateful to God for supporting me in my way. To Escola Superior de Agricultura “Luiz de Queiroz” (ESALQ), Universidade de São Paulo (USP), for giving me the opportunity to conduct my studies. I am especially grateful to Dr. Raphael de C. Castilho (FCAV/UNESP, Brazil), for his great friendship, valuable suggestions and advices, and for all his support during my Doctorate studies. To Professor Dr. Carlos H. W. Flechtmann (ESALQ) for all your lessons, all his assistance provided whenever needed and help with translations of German, Latin and French publications. To Dr. Rowan M. Emberson, retired professor of Entomology at the University of Lincoln (Canterbury, New Zealand), for his great collaboration in chapter 1 and 2 of this thesis, by sending me the file with the listing of species of world Macrochelidae, in other words, for turning possible the conduction of those studies. To Dr. Gerald W. Krantz for important personal information provided and for the examination specimens of the new species described in this thesis. To “Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA) Gado de Corte”, Campo Grande, State of Mato Grosso do Sul (Brazil) for providing the facilities for the conduction of the predation tests with the stable fly and horn fly. To Dr. Paulo H. D. Cançado and Dr. Antonio Thadeu M. Barros, for the guidance and valuable suggestions for the success of the tests conducted at EMBRAPA. To Taciany F. S. Dominghetti and her husband André Dominghetti for the help and the hospitality during the time spent in Campo Grande. To EMBRAPA´s laboratory technicians Ronaldo Souza and Marco Antonio Silva, for the help in the laboratory activities. To Dr. Bruce Halliday for his great help in the interpretation of the spermathecal apparatus of new species, for promptly providing me with several hard-to-get publications I needed and for the stimulating contacts. To Diana M. Rueda for kindly assisting me with the statistical analysis; To Springer International Publishing for granting permission to reproduce the title “Macrochelid Mites (Mesostigmata: Macrochelidae) as Biological Control Agents” as an introductory chapter of this thesis; 5 To “Programa de Pós-Graduação em Entomologia”, especially to its coordinator, Dr. Fernando L. Cônsoli, and the secretary Andrea V. Sintoni, for supporting my activities. To USP COMUT-Librarians for providing copies of many papers. To Lásaro V. F. da Silva (ESALQ/USP, Brazil), for logistic support and laboratory help. To my friends of Acarology Laboratory of ESALQ/USP, Camila Tavares, Diana M. Rueda, Fernanda de C. N. Esteca, Geovanny S. P. Barroso, Grazielle F. Moreira, Jandir C. Santos, João B. da Cruz, João Paulo Z. Narita, João Pedro Martin, Marcela M. R. da Silva, Márcia Daniela, Marina F. C. Barbosa, Michele Ennes, Renan V. da Silva, Reham Abo- Shnaf, Tiago Casaroto. Special thanks to Marielle de M. Berto and Murilo P. Ferreira for the outstanding collaboration in mite samplings and laboratory tests. To the laboratory and administrative staff members of “Departamento de Entomologia e Acarologia” of ESALQ/USP, José L. F. Piedade, Josenilton L. Mandro, Maria Marta Coletti, Rosângela A. da Silva. To Eriana F. Prado and Wilson F. Prado, my parents in law, who always supported me and encouraged my studies. To Débora P. Zamboni, my sister in law, and her husband Giuliano Zamboni for all the affection. To my great friend Marielle de M. Berto for all the affection and friendship. To all my family and especially to the relatives of my husband, for their warm support and love. To “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq, Brazil) for the scholarship that supported me during my Doctoral studies. And to those who in one way or another helped me in this work. Thank you! 6 “Work gives you meaning and purpose and life is empty without it.” − Stephen Hawking 7 CONTENTS RESUMO ................................................................................................................................................................ 9 ABSTRACT .......................................................................................................................................................... 10 1. INTRODUCTION ............................................................................................................................................. 11 MACROCHELID MITES (MESOSTIGMATA: MACROCHELIDAE) AS BIOLOGICAL CONTROL AGENTS ...................... 11 1.1. MORPHOLOGICAL CHARACTERIZATION ...................................................................................................... 12 1.2. TRENDS IN UNDERSTANDING THE MORPHOLOGY, TAXONOMY, AND BIOLOGY OF MACROCHELIDS ............. 12 1.3. DIVERSITY OF THE MACROCHELIDAE ......................................................................................................... 14 1.4. ASSOCIATIONS WITH OTHER ORGANISMS .................................................................................................... 15 1.5. PREDATION POTENTIAL AND LIFE CYCLE .................................................................................................... 17 1.6. REPRODUCTION .......................................................................................................................................... 25 1.7. BEHAVIOUR ................................................................................................................................................ 26 1.8. POTENTIAL FOR THE PRACTICAL USE OF MACROCHELIDS IN BIOLOGICAL CONTROL ................................... 28 1.9. REARING TECHNIQUES ................................................................................................................................ 31 1.10. INTEGRATED MANEGEMENT ..................................................................................................................... 32 1.11. POSSIBLE LIMITATIONS ............................................................................................................................. 33 1.12. SUGGESTED COMPLEMENTARY STUDIES ................................................................................................... 34 References ............................................................................................................................................................. 36 2. CATALOGUE OF THE FAMILY MACROCHELIDAE VITZTHUM (ACARI: MESOSTIGMATA) ......... 49 Abstract ................................................................................................................................................................. 49 2.1. INTRODUCTION ........................................................................................................................................... 49 2.2. MATERIAL AND METHODS .......................................................................................................................... 50 2.3. RESULTS ..................................................................................................................................................... 52 2.4. DISCUSSION .............................................................................................................................................. 201 References ........................................................................................................................................................... 202 3. MACROCHELID MITES (MESOSTIGMATA: MACROCHELIDAE) FROM SÃO PAULO STATE, BRAZIL, AND DESCRIPTION OF A NEW SPECIES OF Macrocheles ......................................................... 225 Abstract ............................................................................................................................................................... 225 3.1. INTRODUCTION ......................................................................................................................................... 225 3.2. MATERIAL AND METHODS .......................................................................................................................
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