3 University of São Paulo “Luiz de Queiroz” College of Agriculture Soil mesostigmatid mites (Acari: Mesostigmata) inhabiting rose fields and neighboring vegetation in the Bogota plateau and their potential role as biological control agents of Frankliniella occidentalis (Insecta: Thysanoptera) Diana Marcela Rueda-Ramírez Thesis presented to obtain the degree of Doctor in Science. Area: Entomology Piracicaba 2018 2 Diana Marcela Rueda-Ramírez Biologist Soil mesostigmatid mites (Acari: Mesostigmata) inhabiting rose fields and neighboring vegetation in the Bogota plateau and their potential role as biological control agents of Frankliniella occidentalis (Insecta: Thysanoptera) Advisor: Prof. Dr. GILBERTO JOSÉ DE MORAES Co-Advisor: Prof. Dra. AMANDA VARELA-RAMÍREZ Thesis presented to obtain the degree of Doctor in Science. Area: Entomology Piracicaba 2018 2 Dados Internacionais de Catalogação na Publicação DIVISÃO DE BIBLIOTECA – DIBD/ESALQ/USP Rueda-Ramírez, Diana Marcela Soil mesostigmatid mites (Acari: Mesostigmata) inhabiting rose fields and neighboring vegetation in the Bogota plateau and their potential role as biological control agents of Frankliniella occidentalis (Insecta: Thysanoptera) / Diana Marcela Rueda-Ramírez. - - Piracicaba, 2018. 237 p. Tese (Doutorado) - - USP / Escola Superior de Agricultura “Luiz de Queiroz”. 1. Mesostigmata 2. Controle biológico 3. Presa complementar 4. Riqueza de espécies 5. Tabela de vida 6. Predação I. Título 3 To My Family For being an inspiration 4 ACKNOWLEDGEMENTS I am grateful to my family for being my support and my inspiration. To my parents Nora Elena Ramirez and Hernando Manuel Rueda for always having stimulated me to study and to progress, and for always being on my side (in addition to helping me many times as my laboratory and field assistants!). To my siblings Camila and Andres Mauricio, for being so wonderful and for making me want to be better every day. To Andres Puerta Gonzalez for having been by my side in key moments, for having spent sleepless nights just accompanying me to do multiple things of the project, for challenging me and for simply supporting me. To my adviser and guide, Prof. Dr. Gilberto J. de Moraes, who believed in me from the beginning and always keeping the door open for any question, even if it was silly. To my co-adviser Prof. Dr. Amanda Varela, who supported me throughout the conduction of the studies in Colombia and who was always on my side since the beginning of my undergraduate studies. To Dr. Johan Manuel Bogoya for accepting to be part of this project and supporting it, despite being a totally new area for him. To Diana Marcela Rios Malaver and Mayerly Alejandra Castro, who helped me in several steps in this project. Both are true co-authors of some chapters of this thesis and, without them, it would have been impossible to carry out many of the sampling, experiments, mite mounting and measures of specimens. To Everth Ebratt Ravelo, for helping me with the thrips identification, and to Jessica Lorena Vaca for helping me with mites and thrips mounting. To Ferdy Alfonso Alvarado for supporting me and believing in my projects, so much so that he always managed to help me make them come true. To the Association of Colombian Flower Exporters – ASOCOLFLORES – for helping me get in touch with the staff of each farm to carry out the collections. To the staff of each of the farms, especially Rafael Boada, José Manuel Pardo (Agua Clara y Vuelven), Andres Millan (Flores el Futuro), Maria del Pilar Bravo (Wayuu Flowers), Karen Tatiana Peña (Elite Flowers) and each one of the monitors, for their willingness to receive me, help me with the collections, trip counts and for providing me information. Without their help this project would not have been possible to conduct. 5 To Maria del Pilar Blanco and Carlos Cuervo of Granja El Porvenir for their willingness to help me and to let me do the collections at their site, to contribute a little to the important project they have. To all people who accompanied me and helped during the collections (Agustin Salazar, Andres Puerta, Andres Rueda, Diana Rios, Giovanna Arboleda, Dr. Juan Pablo Botero, Tatiana Cuervo). All were excellent field assistants! To Augusto Ramirez-Godoy, Universidad Nacional de Colombia, for granting laboratory for processing the samples and for the support and friendship. To Juan Carlos Pinzón for helping me with several things during my time at Universidad Nacional de Colombia. To Dr. Jandir C. Santos, Sofia Jimenez Jorge and Dr. Leticia Azevedo for their friendship and help with identifications. To Santiago Correa for his support at the beginning of this process and his unconditional friendship. To Dr. Rafael Moral for always being willing to answer my multiple questions in each of the statistical models that occurred to me. To Dr. Alireza Nemati, Dr. Bruce Halliday, Dr. David Walter, Dr. Frederick Beaulieu, Dr. Grazielle Furtado, Dr. Mariusz Lewandowski, Dr. Mohamed W Negm and Dr. Shahrooz Kazemi for answering every single question about taxonomy and biology of each mite group. To Lasaro Vanderlei Fernandes da Silva for his help and disposition. 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 my friends of the Acarology Laboratory, Fernanda de C. N. Esteca, Geovanny S. P. Barroso, Grazielle F. Moreira, Jandir C. Santos, João B. da Cruz, João Paulo Z. Narita, Lina Marcela Gonzalez, João Pedro Martin, Marcela M. R. da Silva, Marina F. C. Barbosa, Marielle de M. Berto, Michele Ennes, Murilo P. Ferreira, Renan V. da Silva, Tiago Casaroto and Vinicius Borges da Silva for the help, making unforgettable my passage through the laboratory. All great people. To Eric and Anat Palevsky for their friendship and unforgettable experiences and lessons. To Professor Dr. Carlos H. W. Flechtmann (ESALQ) for his permanent availability to provide me information. 6 To “Programa de Pós-Graduação em Entomologia”, especially to the coordinator, Professor Dr. Fernando L. Cônsoli, and the secretary Andrea V. Sintoni, for supporting my activities. To Escola Superior de Agricultura "Luiz de Queiroz" (ESALQ), University of São Paulo (USP), for the opportunity to carry out the course. To Pontificia Universidad Javeriana for the opportunity to do the Double-Diploma. To COLCIENCIAS (Departamento Administrativo de Ciencia, Tecnología e Innovación, Colombia) for granting the scholarship (Process No. 617-2013, Chapter 3). To “Vicerrectoria Academica” of “Pontificia Universidad Javeriana (Project No. 000000000007367) for partially support this research. To council members (Peter Reutimann, Reinhard Gerecke, Peter Martin, Heinrich Schatz) of the Pro Acarologia Basiliensis foundation, Switzerland, for the donation of the microscope that was very useful for the identification of the specimens collected in this study. To Dr. Jason Dunlop and Anja Friederichs of the Arachnologische Sammlung des Museums für Naturkunde (Berlin, Germany) for the loan of type specimens. 7 “I want to live in a world in which beings are only human, with no other titles than that, without hitting the head with a rule, with a word, with a label. I do not want anyone to be persecuted. I want the vast majority, the only majority, everyone, to be able to speak, read, listen, flourish. I never understood the fight but for it to end. I never understood rigor, but so that rigor does not exist. I have taken a path because I believe that this path brings us all to that lasting kindness. I fight for that obvious, extensive, inexhaustible kindness. I still have an absolute faith in human destiny, a conviction that is increasingly aware that we are approaching a great tenderness. I write knowing that over our heads, over all heads, there is the danger of the bomb, of the catastrophe, but this does not alter my hope. In this critical minute, in this flicker of agony, we know that the definitive light will enter through the half- open eyes. We will all understand each other. We will progress together. And this hope is irrevocable.” Translation of a fragment of “Confieso que he vivido” – Pablo Neruda 8 CONTENTS RESUMO ................................................................................................................................ 11 ABSTRACT ............................................................................................................................ 14 RESUMEN .............................................................................................................................. 16 1. INTRODUCTION .............................................................................................................. 19 1.1. THRIPS IN ROSE PRODUCTION ......................................................................................... 21 1.2. MESOSTIGMATA: IMPORTANT EDAPHIC PREDATORS ....................................................... 24 1.3. CONTEXT OF THE RESEARCH .......................................................................................... 25 1.4. RESEARCH STRATEGY .................................................................................................... 26 REFERENCES ......................................................................................................................... 26 2. EDAPHIC NON-UROPODINA MESOSTIGMATID MITES (ACARI: MESOSTIGMATA) AND THRIPS (INSECTA: THYSANOPTERA) IN ROSE CULTIVATION AND SECONDARY VEGETATION AREAS IN THE BOGOTÁ PLATEAU,