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UNIVERSIDAD VERACRUZANA Elucidating Intrinsic Properties Of UNIVERSIDAD VERACRUZANA INSTITUTO DE NEUROETOLOGÍA Doctorado en Neuroetología Elucidating intrinsic properties of ant-plant mutualistic networks TESIS QUE PARA OBTENER EL GRADO DE DOCTOR EN NEUROETOLOGÍA Presenta: M. en C. Wesley Francisco Dáttilo da Cruz Director de tesis: Dr. Víctor Rico-Gray Instituto de Neuroetología, Universidad Veracruzana Xalapa, Veracruz, México, Agosto 2015 2 TUTORIAL COMMITTEE Dr. Víctor Rico-Gray (Advisor) Instituto de Neuroetología, Universidad Veracruzana Xalapa, Veracruz. Mexico Dra. Cecília Díaz-Castelazo Red de Interacciones Multifróficas Instituto de Ecología A.C. Xalapa, Veracruz. Mexico Dra. Laura Teresa Hernández Salazar Instituto de Neuroetología, Universidad Veracruzana Xalapa, Veracruz. Mexico Dr. Armando Martínez Chacón Instituto de Neuroetología, Universidad Veracruzana Xalapa, Veracruz. Mexico 3 "It is interesting to contemplate a tangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent upon each other in so complex a manner, have all been produced by laws acting around us." (Charles Darwin, 1859) 4 ACKNOWLEDGMENTS After three academic degrees, at three different universities (Universidade Estadual do Norte Fluminense, Universidade Federal de Mato Grosso, and Universidad Veracruzana), in two different countries (Brazil and Mexico), I have learned one thing – I could never have done any of this, particularly the research and writing that went into this thesis, without the support and encouragement of a lot of people. Words can never be enough in expressing how grateful I am to those incredible people in my life that made this thesis possible. I would like an attempt to thank them for making my time during my research in the Institute of Neuroethology at Universidad Veracruzana an amazing period. First and foremost I want to thank my advisor PhD. Víctor Rico-Gray, especially by accepting a Brazilian student still unknown at that moment for him. It has been an honor to be his Ph.D. student. He has taught me, both consciously and unconsciously, how the good and old natural history can help us to understand complex patterns of species interactions. I appreciate all his contributions of time and ideas to make my Ph.D. experience productive and stimulating. The enthusiasm he has for his research was contagious and motivational for me, even during tough times in the Ph.D. I am also thankful for the excellent example he has provided as a successful ecologist and professor. I would also like to thank all my co-authors of the papers generated in this thesis, but especially to Dr. Thiago Izzo (Universidade Federal de Mato Grosso, Brazil) and Dr. Kléber Del Claro (Universidade Federal de Uberlândia, Brazil), that even far were important throughout my training as a scientist in Mexico. I would also like to thank to Dr. Pedro Jordano, I am very appreciative of his generosity with his time, advice, data analysis and all help when I was a visiting student in 2014 into his lab at the Estación Biológica de Doñana in Seville, Spain. For this thesis I would like to thank my reading committee members: Dra. Laura Teresa Hernández Salazar (Universidad Veracruzana), Dr. Armando Jesús Martínez Chacón (Universidad Veracruzana) and Dra. Cecília Díaz Castelazo (Instituto de Ecología, A.C.) for 5 their time, interest, and insightful questions and comments. I gratefully acknowledge the funding sources that made my Ph.D. work possible. I was funded by the National Council of Science and Technology of Mexico (CONACYT) through the fellowship no. 489746. Mexico is a wonderful country, full of culture and food (mainly peppers and tequila) and my time over the years was made enjoyable in large part due to the many friends that became a part of my life. I am grateful also to my friends and brothers Armando Aguirre, Dulce Rodríguez Morales and Juan C. Serio Silva who over the years have patiently endured my highs and lows and have kept me sane and entertained. Last but not least, I would like to thank my family for all their love and encouragement. Without your unending support and love from childhood to now, I never would have made it through this process or any of the tough times in my life. And most of all for my loving, supportive, encouraging, and patient wife Jessica Falcão whose faithful support during the final stages of this Ph.D. is so appreciated. Thank you for being there for me from the very beginning since my undergraduate studies. Thank you everybody for believing in me. 6 CONTENTS 1.) ABSTRACT. …………………………………………………………….. p. 7 2.) RESUMEN. ……………………………………………………………… p. 8 3.) General introduction. ………………………….……………….………. p. 9 4.) Chapter I – Strength of the modular pattern in Amazonian symbiotic ant-plant networks. ………………………………………………………….. p. 19 5.) Chapter II – Different tolerances of symbiotic and nonsymbiotic ant- plant networks to species extinctions. ……………………………………….. p. 27 6.) Chapter III – Soil and vegetation features determine the nested pattern of ant-plant networks in a tropical rainforest. ………………………………. p. 40 7.) Chapter IV – Importance of interaction frequency in analysis of ant- plant networks in tropical environments. ……………………………………. p. 48 8.) Chapter V – Ant dominance hierarchy determines the nested pattern in ant-plant networks. ……………………………………………………........... p. 53 9.) General conclusion………………………………………………………. p. 64 7 ABSTRACT: Ants and plants can interact positively in different ways, from facultative to highly specialized relationships. Over spatial and temporal scales different ant and plant species can interact with each other and generate complex ecological networks of interactions. In this doctoral thesis, the text was divided into five interrelated chapters to evaluate how different biotic and abiotic factors and the specialization level among species structuring ecological networks involving ants and plants with extrafloral nectaries (nonsymbiotic interactions) and myrmecophytes (symbiotic interactions). Moreover, I also evaluated the robustness of such networks to simulated species extinctions and disturbances caused by human modification of the landscape. I showed for the first time that symbiotic ant-plant networks are highly specialized and with low overlap in the use of partners. Consequently, such symbiotic networks were less robust for both ants and plants species extinction compared to nonsymbiotic networks (i.e, those involving ants and plants with extrafloral nectaries). In addition, soil pH was an important factor structuring the nested pattern in nonsymbiotic networks. However, unlike binary networks, quantitative networks are often significantly non-nested. I also show that although ants have an extremely territorial effect only near their nests, competition among ants is strong enough to structure ant-plant networks. Specifically, I found that ant position within the nested ant-plant network can be predicted only by differences among the competitive ability (numerical dominance and recruitment) of ant species. In short, my results in this doctoral thesis highlight the importance of the level of specialization and abiotic and biotic factors in the maintenance of the structure of ant-plant mutualistic networks. Keywords: ant-plant interactions, dominance hierarchy, mutualistic networks, modularity, nestedness, and robustness. 8 RESUMEN: Las hormigas y las plantas interactuan positivamente de diferente manera, desde facultativa hasta relaciones altamente especializadas. A lo largo de diferentes escalas espaciales y temporales, diferentes especies de hormigas y plantas pueden interactuar entre sí y generar redes ecológicas complejas de interacciones. En esta tesis de doctorado, el texto se divide en cinco capítulos interrelacionados para evaluar cómo los diferentes factores bióticos y abióticos y el nivel de especialización entre las especies estructuran las redes ecológicas que involucran hormigas y plantas con nectarios extraflorales (interacciones no simbióticas) y mirmecófitas (interacciones simbióticas). Por otra parte, también evalué la robustez de dichas redes para la extinción simulada de especies y para las perturbaciones causadas por la modificación humana del paisaje. Muestro por primera vez que las redes simbióticas hormiga- planta son altamente especializadas y con una baja superposición en el uso de los socios. En consecuencia, este tipo de redes simbióticas fueron menos robustas tanto para la extinción de especies de hormigas y plantas en comparación con las redes no simbióticas (es decir, las interacciones entre hormigas y plantas con nectarios extraflorales). Además, el pH del suelo fue un factor importante para estructurar el patrón anidado en las redes no simbióticas. Sin embargo, a diferencia de las redes binarias, las redes cuantitativas fueron frecuentemente no- anidadas. También muestro que aunque las hormigas tienen un efecto marcadamente territorial sólo cerca de sus nidos, la competencia entre las hormigas es fuerte y lo suficiente para estructurar las redes no simbióticas involucrando hormigas y plantas. Específicamente, muestro que la posición de las hormigas dentro de la red anidada puede predecirse sólo por las diferencias entre la capacidad competitiva (dominancia numérica y reclutamiento) de las especies de hormigas. En resumen, mis resultados en esta tesis doctoral ponen de relieve la importancia del nivel de especialización
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