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RIUNNE FACENA TD Guidetti Universidad Nacional del Nordeste Facultad de Ciencias Exactas y Naturales Servicios ecosistémicos brindados por aves frugívoras dispersoras de semillas en bosques con ganadería extensiva del Espinal de la provincia de Entre Ríos Brenda Yamile Guidetti Director: Guillermo C. Amico Co-director: Sebastián Dardanelli Lugar de trabajo: Grupo ECODES, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires e IEGEBA (UBA-CONICET) Tesis presentada en cumplimiento parcial de los requisitos para optar al título de Doctora de la Universidad Nacional del Nordeste en Biología 2020 Resumen El objetivo de esta tesis fue caracterizar el servicio ecosistémico de dispersión de semillas brindado por aves en bosques bajo ganadería extensiva del Espinal de la provincia de Entre Ríos. Entre los años 2015 y 2018 se realizaron muestreos en 11 sitios de estudio con distintos niveles de ganadería extensiva. Se observó el consumo de frutos carnosos y se tomaron muestras de heces y regurgitados, identificando las especies de aves que dispersan semillas y categorizándolas de acuerdo a su efectividad. Las especies que más aportaron al servicio fueron Saltator aurantiirostris, Elaenia parvirostris, Thraupis sayaca, Turdus amaurochalinus y Turdus rufiventris. Una gran cantidad de aves granívoras, insectívoras u omnívoras también dispersaron semillas, reforzando la idea de que la frugivoría es un rasgo relativamente oportunista en ambientes estacionales. El comportamiento de estas especies promueve el movimiento ocasional de semillas desde el interior de la cobertura del bosque hasta bordes y áreas abiertas degradadas. La red conformada por plantas de frutos carnosos y aves dispersoras de semillas que interactúan en el bosque de Espinal entrerriano tiene dependencias asimétricas, siguiendo un modelo donde muchas especies interaccionan con pocas especies del otro grupo y vice-versa. Los índices que describen la estructura de la red revelaron baja conectividad, poco anidamiento y cierta modularidad. De acuerdo a la posición central que ocupan en la red de interacciones, las aves identificadas como principales dispersoras de semillas también constituyen eslabones claves para mantener la cohesión y la estabilidad del entramado. Además, fueron analizados los factores que podrían tener relación con los componentes cuantitativos y cualitativos del ensamble de dispersoras y semillas dispersadas. La abundancia y la riqueza de las aves dispersoras de semillas y la abundancia de semillas dispersadas se relacionaron positivamente con la disminución de la cobertura arbustiva, la extracción de madera seca para leña y una mayor carga ganadera instantánea. La altura del pasto, asociada con la intensidad de pastoreo, actuó de manera inversa al resto de las variables vinculadas con la actividad ganadera. Además, quedó en evidencia que la abundancia y la riqueza de las aves dispersoras de semillas, pero sobre todo la abundancia de semillas dispersadas, se relacionan positivamente con la riqueza específica de la vegetación leñosa. La abundancia de semillas dispersadas disminuyó con el aumento de la riqueza de aves dispersoras de semillas (lo que podría tener relación con la variabilidad en la efectividad de dispersión de las distintas especies), mientras que la riqueza de especies de semillas dispersadas aumentó a mayor abundancia de aves dispersoras de semillas (probablemente debido a una mayor exploración de los recursos disponibles). La riqueza de aves dispersoras y sobre todo la abundancia de semillas dispersadas estuvieron positivamente relacionadas con la abundancia de frutos, sin embargo la abundancia de aves dispersoras se relacionó de manera contraria (probablemente porque al aumentar la disponibilidad de frutos, las aves que los consumen se distribuyen de manera más homogénea en todo el parche, o bien, porque al aumentar la densidad de individuos entran en juego procesos como competencia y territorialidad). Finalmente, entre los años 2014 y 2016 se realizó una experiencia a campo y una serie de meta-análisis a escala global para evaluar la efectividad de las perchas artificiales en áreas donde los bosques nativos fueron reemplazados por cultivos, pastizales o pasturas. Los resultados indicaron que el 2 uso de perchas produce una lluvia de semillas más abundante y rica en especies en comparación con la que reciben las áreas abiertas sin ningún tipo de intervención. La gran magnitud de semillas dispersadas de Ligustrum sp., Morus alba y Asparagus setaceus pone en duda si no sería conveniente evitar el uso de perchas en sitios invadidos por especies de plantas exóticas. No obstante, las perchas artificiales se presentaron como una práctica capaz de superar la falta de llegada de semillas de frutos carnosos, promoviendo la sucesión y la regeneración vegetal en áreas deforestadas y/o degradadas dentro de un amplio rango de ecosistemas nativos. Los aportes de este trabajo enriquecen las bases para la valoración del servicio ecosistémico de dispersión de semillas por aves y su integración en el planeamiento y la toma de decisiones en relación al uso sustentable, monitoreo, conservación y restauración del bosque en el Espinal de la provincia de Entre Ríos. Palabras clave: aves frugívoras, bosque de Espinal entrerriano, dispersión de semillas, ganadería extensiva, perchas artificiales, redes de interacción, restauración de ecosistemas. 3 Abstract The aim of this thesis was to characterize the ecosystem service of seed dispersal provided by birds in the forests of the province of Entre Ríos. Between 2015 and 2018, 11 study sites with different levels of extensive livestock were sampled. Observations of fleshy fruits consumption were made and feces and regurgitated samples were took, identifying seed dispersal species and categorizing them according to their effectiveness. The species that most contributed with the service were Saltator aurantiirostris, Elaenia parvirostris, Thraupis sayaca, Turdus amaurochalinus and Turdus rufiventris. A large number of granivorous, insectivorous and omnivorous birds also dispersed fleshy fruits seeds, reinforcing the idea that frugivory is an opportunistic trait in seasonal environments. The behavior of these bird species promote occasional seeds movement from the forest cover interior to degraded and open areas. The network constituted by fleshy fruits plants and all the seed dispersal birds that interact in the Espinal forest of Entre Ríos have asymmetric dependencies, fitting a model where many species interact with few species of the other group and vice versa. Descriptive indexes of network structure reveal low connectivity, low nesting and certain modularity. According to their central position in the network, bird species identified as main seed dispersers are also key links that maintain framework cohesion and stability. As well, the factors that could be related with quantitative and qualitative components of the seed dispersal birds assemblage and dispersed seeds were analyzed. The abundance and richness of seed dispersal birds and the dispersed seeds abundance, related positively with shrub cover reduction, extraction of firewood and higher livestock density. The grass height, asociated to the grazing intensity, acted inversely to the rest of the variables involved with livestock activity. Further, it was evident that abundance and richness of the seed dispersal birds, and even more abundance of dispersed seeds, relate positively to woody vegetation specific richness. The abundance of dispersed seeds decreased with the increase of the seed dispersal birds richness (which can have to do with variability in dispersal effectiveness between bird species), while the richness of dispersed seeds was greater with higher amount of seed dispersal birds (probably due to further exploration of resources). The richness of seed dispersal birds and the abundance of dispersed seeds were positively related to the abundance of fruits, but the abundance of frugivores was related in a contrary way (probably because when availability of fruits increase, the birds that consume them distribute more homogeneously throughout the patch, or because, when individuals density increase, competition and territoriality processes come into play). Finally, between 2014 and 2016, a field experiment and a series of global scale meta- analyses were conducted to evaluate the effectiveness of artificial perches in areas where native forests were replaced by crops, grassland or pastures. The use of perches produced a more abundant seed rain and with higher species richness compared to that one received by open areas without intervention. The magnitude of dispersed Ligustrum sp., Morus alba and Asparagus setaceus seeds question whether it would not be convenient to avoid the use of perches in sites invaded by exotic species. However, perches were presented as a practice able to overcome the lack of fleshy fruits seeds arrival, promoting succession and plant regeneration in deforested and/or degraded areas within a wide range of native ecosystems. The contributions of this work improve the bases for the valuation of the ecosystem service of seed dispersal by frugivorous birds, and its integration into planning and decision-making regarding the sustainable use, monitoring, conservation and restoration of the Espinal forest in Entre Ríos. Keywords: artificial perches, ecosystem restoration, Espinal forest of Entre Rios Province, extensive livestock, frugivorous birds, networks, seed dispersal. 4 Índice Agradecimientos
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