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Petrocoptis Grandiflora Implicaciones ecológicas y evolutivas del robo de néctar Ecological and evolutionary implications of nectar robbery TESIS DOCTORAL Opta al título de “DOCTOR INTERNACIONAL” SANDRA VICTORIA ROJAS NOSSA Vigo Abstract Plants interact simultaneously with a great variety of organisms that modify their biological success and act as selective agents. In the mutualistic interactions of pollination plants receive the benefit of pollen carryover between flowers, while animals obtain resources as reward. However, rewards and other parts of the plant are also consumed by exploiters which apparently do not provide any benefit in return. Nectar robbers are insects, birds and mammals that use a hole made in the corolla to extract the nectar accumulated at the base of the flowers or spurs without entering "legitimately" through the opening of the flower. Nectar robbery has consequences that differ in direction and magnitude for the reproduction of plants through direct and indirect mechanisms, according to the characteristics of the participants in the interactions. As a result, nectar robbers may act as selective agents, modify population dynamics and constitute important pieces for the maintenance of mutualisms. However, few biological systems have been thoroughly studied making the information about this phenomenon still too scarce, fragmented and limited to specific geographic areas, hindering generalizations. The main goal of this dissertation is to study the ecological and evolutionary implications of nectar robbery from a multiscale perspective. To achieve this we first studied the spatial and temporal variability in the robbery frequency of a vulnerable plant species. We analyzed the consequences of nectar robbery for male and female components of the reproductive success in two plant species of the Iberian Peninsula with different life histories: Petrocoptis grandiflora a perennial herb, self-compatible and restricted distribution, and Lonicera etrusca a scandent shrub, pollinator-dependent and common in Mediterranean ecosystems. The direction and magnitude of the effects of two types of exploiters (nectar robbers and sap-sucking herbivores) for the pollination of L. etrusca were studied. We developed a model to calculate and compare the pollination effectiveness of floral visitors for pollinator-dependent plants that include aspects of foraging behaviour and pollen carryover. Then, the frequency of nectar robbery by insects and birds in plant communities from temperate and tropical regions was studied and compared. Finally, we assessed the association between the frequencies of nectar robbery with several plant traits related with floral visitors. The results show that the percentage of robbed flowers in P. grandiflora was highly variable over 12 years, but not among populations. Strong changes in climatic conditions that affected population abundances of the main primary nectar robbers (Xylocopa violacea and Bombus terrestris) are the most likely cause of this variation. The nectar robbery increased fruit set and distance of pollen dispersal in P. grandiflora. Unlike, in L. etrusca nectar robbery did not modify nor male neither female components of reproductive success. These robbers promote cross-pollination as they move among flowers, pierce the base of the perianth and extract nectar. In both plants robbers have positive effects for pollination, but differences in the reproductive system and the morphological match between insect and flower determine the changes in the reproductive success of the plants. On an opposite direction, aphids extract sap from branches and petioles of L. etrusca before blooming causing morphological and physiological changes driving a reduction in subsequent pollination and post-pollination processes. Despite the flowers of the plant have characteristics associated with a specialized hawkmoth pollination system, pollination is commonly performed by a wide arrange of insects. Hawkmoths are in fact high qualitative pollinators in terms of one single visit to one flower. However, at the population level, hymenopterans behaving as legitimate visitors and primary robbers are the most effective pollinators of L. etrusca. This result is related to their behaviour, their morphology and the high frequency of floral visits. In contrast, the beetles that behave as primary robbers are the less effective pollinators and cause considerable damages to the corolla and the reproductive structures. These results demonstrate that two groups of floral visitors which apparently behave similarly (i.e. behave as primary nectar robbers) have opposite consequences for the reproduction of the same plant species. These consequences are related to their morphology, behaviour and visit frequency. This reflects the importance of detailed studies of pollination systems that analyze and compare objectively the role of nectar robbers in plant-animal interactions. The results demonstrate that nectar robbery is a very common phenomena in plant communities of temperate and tropical regions. However, within communities a high variation of the frequency of robbery among species occurs. Such variation depends on the presence of animals with the capacity (morphological and behavioural) to rob nectar, but it is also related with mechanisms that operate at different scales. At a fine-scale the floral morphology, the nectar properties and the presence of physical barriers are the most relevant characters to determine the frequency of this behaviour. On a larger ecological scale, nectar robbery is a dense- dependent phenomenon which occurs more frequently in those species that represent abundant energetic resources. Thus, nectar robbery is a frequent phenomenon in angiosperms with long and narrow flowers with high nectar production and high density of flowers. In cases when the levels of robbery are lower than expected based on plants’ traits, the evolution of defensive mechanisms against robbery (such as mechanical or barriers or chemical deterrents) is highly likely. The study of selective scenarios involving the role of robbers and legitimate visitors in the evolution of plants’ traits is a promising study field that requires further attention. Also, researches regarding the role of these floral visitors in the stability of trophic networks are needed to obtain a more complete picture on this complex phenomenon and its consequences for the functioning of mutualisms. A Dieter y Amber, a mis padres, hermanas y sobrinos A mi gran familia colombiana, austríaca y sudafricana Abejas, trabajadoras puras, ojivales obreras, finas, relampagueantes proletarias, perfectas, temerarias milicias que en el combate atacan con aguijón suicida, zumbad, zumbad sobre los dones de la tierra, familia de oro, multitud del viento, sacudid el incendio de las flores, la sed de los estambres, el agudo hilo de olor que reúne los días, y propagad la miel sobrepasando los continentes húmedos, las islas más lejanas del cielo del Oeste. Pablo Neruda, 1957 Agradecimientos Cielo, aire, luz, fuerza, motivo. Compañeros de viaje, campo, y copas. Dieter y Amber, de ustedes también es este paso. Gracias a mi gran familia que desde todos los rincones me ha querido y me ha dado su apoyo de diferentes formas. Agradezco a Luis y Pepe por haber compartido conmigo las historias del Bierzo y sus habitantes. Su guía, apoyo y labor han sido imprescindibles para que esta tesis se realice. También quiero agradecer sus enseñanzas, ideas, sueños y discusiones a otros profesores que han sido importantes durante todo el proceso: Gary, Marisol y Rodulfo. A los profesores del programa de doctorado y miembros del Departamento de Biología Vegetal y Ciencia del suelo de la Universidad de Vigo por contribuir a mi formación. Agradezco la disposición y los valiosos comentarios de los miembros del tribunal que evalúa esta tesis. A Danny Rojas y Rodulfo Ospina por revisar y corregir este manuscrito. A Silvia Castro por revisar y corregir el capítulo 2. Gracias a las personas del Laboratorio de Ecología y Evolución de Plantas, del Grupo de Ornitología de la Universidad Nacional de Colombia, a los estudiantes del Curso de Biología de la Polinización 2011 (U. Nal.) que aportaron con el trabajo en campo, ideas y buena onda. A Danny por su ayuda con la estadística, por llevarme a conocer los colibríes cubanos y por toda su colaboración y apoyo durante este trabajo. A Ángel por ser el ángel del lab, por su generosidad, por la ilustración de la flor y por las muchas muchas ideas que genera. A Vicky por su ayuda en todo. A los chicos de Divulgare por las risas, por compartir sus conocimientos sobre el manejo de imágenes y por las ideas y comentarios sobre la portada. Agradezco a las autoridades que dieron los permisos para el trabajo de campo. En particular la ayuda y compromiso de los administradores, habitantes y trabajadores de los conjuntos residenciales La Floresta y Torca, y del Parque Natural Serra da Enciña da Lastra. A Paola Pedraza por la identificación y los comentarios sobre las ericáceas andinas. A Nicolás Pérez Hidalgo por la identificación de los áfidos. A Francisco López por la identificación de los coleópteros. A Sandra Nicolás por su hospitalidad y ayuda en el trabajo en el Bierzo. A Erika Keller por su ayuda en Austria. A Alejandro Rico por facilitar los equipos de fotografía y por su apoyo. A Yaiza Lechuga por colaborar con el análisis de cargas polínicas. A Oscar González por las discusiones e ideas que han enriquecido este trabajo. Las fotografías en SEM fueron hechas en colaboración
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