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Ecological and Genetic Analysis of Plant-Animal Interactions in Mediterranean Environments

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Ecological and Genetic Analysis of Plant-Animal Interactions in Mediterranean Environments UNIVERSIDAD DE MURCIA ESCUELA INTERNACIONAL DE DOCTORADO Ecological and Genetic Analysis of Plant-Animal Interactions in Mediterranean Environments Análisis Ecológico y Genético de Interacciones Planta-Animal en Ambientes Mediterráneos D. Vicente Martínez López 2018 Ecological and genetic analysis of plant-animal interactions in Mediterranean environments Análisis ecológico y genético de interacciones planta-animal en ambientes mediterráneos Tesis Doctoral Vicente Martínez López 2018 Escuela Internacional de Doctorado de la Universidad de Murcia (EIDUM) Universidad de Murcia Directores: Dra. Mª Pilar De la Rúa Tarín Dr. Francisco Robledano Aymerich Con el apoyo de (support): Esta tesis ha sido realizada en los Departamentos de Zoología y Antropología Física y Ecología e Hidrología de la Universidad de Murcia bajo de dirección de los doctores Mª Pilar De la Rúa Tarín y Francisco Robledano Aymerich. El autor ha sido beneficiario de un Contrato Predoctoral para la Formación del Profesorado Universitario (FPU) del Ministerio de Educación, Cultura y Deporte (referencia FPU 13/05115). Además ha realizado dos estancias predoctorales de tres meses de duración cada una financiada también por el Ministerio de Educación, Cultura y Deporte en régimen de concurrencia competitiva en la Universidad de Marburg (Alemania), supervisado por la Dra. Nina Farwig, y en CIBIO/InBIO (Universidad de Oporto, Portugal), supervisado por la Dra. Cristina García. Las investigaciones realizadas en el presente trabajo han recibido financiación de los proyectos de la Fundación Seneca: Consecuencias ecogeomorfológicas del abandono de campos de cultivo en la Región de Murcia (15233/PI/10), y Proyecto para grupos de excelencia (19908/GERM/2015). El capítulo IV de esta tesis ha sido realizado en el marco del proyecto ―Polinizadores en riesgo: análisis de redes de polinización y dispersión de patógenos en zonas semiáridas‖, concedido al autor de esta tesis por la Asociación Española de Ecología Terrestre (AEET) en la Convocatoria de concesión de ayudas a proyectos de investigación en Ecología liderados por jóvenes investigadores del año 2016. Gracias a este proyecto el beneficiario pudo realizar una estancia breve de una semana en el Centro Regional Apícola de Marchamalo (Guadalajara) bajo la supervisión de los doctores Mariano Higes y Raquel Martín-Hernández. ―What escapes the eye, however, is a much more insidious kind of extinction: the extinction of ecological interactions‖ Daniel Janzen (1974) CONTENTS (Índice) SPANISH SUMMARY (Resumen en español) 1 GENERAL INTRODUCTION 25 CHAPTER I. Intercontinental long-distance seed dispersal 73 explains population genetic structure in a fleshy-fruited shrub spanning the Mediterranean Basin CHAPTER II. Ecological and genetic consequences of 135 fragmentation in a semiarid Mediterranean urban forest CHAPTER III. Barcoding as an ancillary technique to uncover 163 mechanisms of seed dispersal in demanding environments - and to help to restore them CHAPTER IV. Contrasting effects of beekeeping and land use on 211 plant-pollinator networks and pathogen prevalence in a Mediterranean semiarid ecosystem GENERAL CONCLUSIONS 251 ACKNOWLEDGEMENTS 257 ANNEX I. Curriculum Vitae of the author 263 SPANISH SUMMARY (Resumen en español) Spanish summary (resumen en español) 1. Mutualismos planta-animal. Importancia y técnicas de estudio El mutualismo es un proceso ecológico en el que dos especies interactúan entre sí y ambas reciben un beneficio por tal interacción (Bronstein, 2015). Las interacciones mutualistas están extendidas en los ecosistemas naturales (Janzen, 1985), y juegan un papel clave en el mantenimiento de la biodiversidad y de los servicios ecosistémicos en todo el mundo (p. ej. Albrecht et al., 2014). Todos los organismos están directa o indirectamente involucrados en interacciones mutualistas (Thompson, 2009). De hecho, todos los eucariotas podrían considerarse como mutualistas en sí mismos, ya que de acuerdo con la teoría endosimbiótica la célula eucariota es el resultado de multiples procesos de asociación entre diferentes células procariotas (Margulis, 1967). Se han descrito muchos tipos de mutualismos en la naturaleza: hongos interactuando con las raíces de las plantas para incrementar la movilidad de los nutrientes (micorrizas, Van Der Heijden, Martin, Selosse, & Sanders, 2015); bacterias y nódulos de las raíces de las plantas leguminosas para fijar nitrógeno en el suelo (Kiers, Rousseaus, West, & Denison, 2003; Heath & Tiffin, 2007); líquenes formados por la asociación de hongos y algas (Grube & Wedin, 2016); ácaros y hojas de las plantas (domatía, Romero & Benson, 2005) (Figura 1) y plantas y animales (p. ej. polinización, Willmer, 2011; y dispersion de semillas, Howe & Smallwood, 1982). De entre todas estas interacciones, esta tesis se centra en la polinización y la dispersion de semillas, que son dos tipos de interacciones mutualistas cruciales en el ciclo reproductivo de las plantas que dependen de animales para la polinización de sus flores y/o la dispersion de sus semillas (Jordano, 2000; Ollerton, Winfree, & Tarrant, 2011). Las interacciones mutualistas han llamado la atención de los científicos durante milenios. Las primeras descripciones de mutualismos datan de la Antigua Grecia. Hay mucha bibliografía de finales del siglo XIX describiendo la historia natural de diferentes mutualismos. Sin embargo, el campo no avanzo conceptualmente hasta la década de 1960, y la mayoría de los estudios fueron realizados a partir de 1980 (Bronstein, 2009; Bascompte & Jordano, 2013). Los estudios de Janzen (1966) sobre la interacción entre las acacias (Acacia cornigera (L.) Willd) y las hormigas que las habitan (Pseudomyrmex ferruginea F. Smith) son un ejemplo de estos estudios pioneros que proporcionaron unas bases sólidas en el campo 3 del estudio de los mutualismos. El papel de las hormigas que viven en acacias había sido discutido por muchos científicos desde que Belt describió la interacción en 1874. Decenas de investigadores, incluyendo a Darwin (1877), participaron en ese intenso debate que dio lugar a diferentes hipótesis sobre la interacción acacia-hormiga. Mientras algunos científicos consideraban a las hormigas como protectoras de la planta, otros las veían cómo parasitos. Sin embargo, faltaban estudios experimentales para testar estas teorías que estaban principalmente basadas en observaciones. El debate permaneció abierto hasta los estudios de Janzen (1966). El describió el mutualismo que ocurría entre la acacia y las hormigas tras eliminar las hormigas en algunos árboles y registrar su desarrollo en contraste con el de acacias todavía ocupadas por hormigas. Encontró que los árboles no ocupados sufrían una presión de herbivoría más elevada y una mayor competición con otras plantas en comparación con las ocupadas, en las cuales las hormigas protegían al árbol de los herbívoros y eliminaban a otras plantas competidoras en los alrededores de la acacia. Figura 1. Diferentes ejemplos de domatía entre ácaros y plantas. En estas interacciones las plantas ofrecen refugio a los ácaros, mientras que los ácaros protegen a las plantas de patógenos y herbívoros. Las barras de escala representan 0,5 mm (Figura de Romero & Benson, 2005). Los estudios de interacciones planta-animal generalmente han sido realizados en grupos pequeños de especies (Nilsson, 1988; Johnson & Steiner, 1997). Sin embargo, los mutualismos planta-animal forman redes 4 Spanish summary (resumen en español) complejas de interacciones entre especies. Por tanto, el funcionamiento del sistema solo puede entenderse si se estudian las interacciones al nivel de comunidad (Jordano, Bascompte, & Olesen, 2003). Los parámetros estructurales de estas redes complejas tienen consecuencias importantes para la estabilidad de las comunidades, así que las redes mutualistas han sido consideradas como la arquitectura de la biodiversidad (Bascompte & Jordano, 2007) y comprenderlas es crucial para la conservación de los sistemas ecológicos (p. ej. Rico-Gray & Oliveira, 2007). Aunque este enfoque ya se aplicó en algunos estudios durante la década de 1980 (p. ej. Janzen, 1980; Herrera, 1982; Jordano, 1987), no se desarrolló hasta la aparición de herramientas analíticas adecuadas que pudieran desvelar las propiedades estructurales de estos sistemas complejos de interacciones. En este sentido, el desarrollo de redes bipartidas (aquellas en las cuales las especies están divididas en dos niveles tróficos y que no pueden interactuar con las especies en el mismo nivel, Figura 2) (Jordano et al., 2003) al principio del siglo XXI, ha incrementado la cantidad de estudios realizados en el campo de los mutualismos a nivel de comunidad. Figura 2. Red bipartida cuantitativa de dispersores de semillas (animales, arriba) y plantas (abajo) in el Gran Rift. Principales dispersores: 1. Pycnonotus tricolor, 2. Civettictis civetta, 3. Loxodonta africana, 4. Cercopithecus pygerythrus, 5. Papio ursinus, 6. Hystrix africaeaustralis, y 7. Redunca arundinum. Plantas que fueron más comúnmente dispersadas: a Centaurea praecox, b Grewia inaequilatera, c Hyphaene natalensis, d Sclerocarya birrea, e Tamarindus indica, y f Ziziphus mucronata. Los enlaces representan la interacción entre los taxones animales y vegetales, y su grosor es proporcional al número de interacciones (Figura de Timóteo, Correia, Rodríguez- Echeverría, Freitas, & Heleno, 2018). La estructura de las redes mutualistas condiciona su resiliencia a perturbaciones antrópicas (Fortuna & Bascompte, 2006). Por tanto, es 5 fundamental comprender
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