Colonization of Abandoned Land by Juniperus thurifera Is Mediated by the Interaction of a Diverse Dispersal Assemblage and Environmental Heterogeneity

et al. (2012) Colonization of Abandoned Land by Juniperus thurifera Is Mediated by the Interaction of a Diverse Dispersal Assemblage and Environmental Heterogeneity. PLoS ONE 7(10): e46993. doi:10.1371/journal.pone.0046993 Colonization of Abandoned Land by Juniperus thurifera Is Mediated by the Interaction of a Diverse Dispersal Assemblage and Environmental Heterogeneity Gema Escribano-Avila 0 Virginia Sanz-Pe rez 0 Beatriz Pas 0 Emilio Virgo s 0 Adria n Escudero 0 Fernando Valladares 0 Anna Traveset, Institut Mediterrani d'Estudis Avancats (CSIC/UIB), SPAIN 0 1 Departamento de Biolog a y Geolog a, Universidad Rey Juan Carlos , Madrid , Spain , 2 Facultad de Ciencias Ambientales, Universidad de Castilla-La Mancha , Toledo , Spain , 3 Departamento de Biolog a Vegetal I, Universidad Complutense de Madrid , Madrid , Spain , 4 Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cient ficas , Madrid , Spain Land abandonment is one of the most powerful global change drivers in developed countries where recent rural exodus has been the norm. Abandonment of traditional land use practices has permitted the colonization of these areas by shrub and tree species. For fleshy fruited species the colonization of new areas is determined by the dispersal assemblage composition and abundance. In this study we showed how the relative contribution to the dispersal process by each animal species is modulated by the environmental heterogeneity and ecosystem structure. This complex interaction caused differential patterns on the seed dispersal in both, landscape patches in which the process of colonization is acting nowadays and mature woodlands of Juniperus thurifera, a relict tree distributed in the western Mediterranean Basin. Thrushes (Turdus spp) and carnivores (red fox and stone marten) dispersed a high amount of seeds while rabbits and sheeps only a tiny fraction. Thrushes dispersed a significant amount of seeds in new colonization areas, however they were limited by the presence of high perches with big crop size. While carnivores dispersed seeds to all studied habitats, even in those patches where no trees of J. thurifera were present, turning out to be critical for primary colonization. The presence of Pinus and Quercus was related to a reduced consumption of J. thurifera seeds while the presence of fleshy fruited shrubs was related with higher content of J. thurifera seeds in dispersers' faeces. Therefore environmental heterogeneity and ecosystem structure had a great influence on dispersers feeding behaviour, and should be considered in order to accurately describe the role of seed dispersal in ecological process, such as regeneration and colonization. J. thurifera expansion is not seed limited thanks to its diverse dispersal community, hence the conservation of all dispersers in an ecosystem enhance ecosystems services and resilience. - Funding: Gema Escribano-A vila was supported by a FPU-MEC doctoral grant from the Spanish Ministry for Education (http://www.educacion.gob.es/portada. html). Funding was provided by the Spanish Ministry for Innovation and Science (http://www.idi.mineco.gob.es/) with the grants CGL2010-16388/BOS, Consolider Montes (CSD2008_00040), VULGLO (CGL2010-22180-C03-03) and CALCOFIS (CGL2009-13013), and by the Community of Madrid grant (http://www.madrimasd. org/) REMEDINAL 2 (CM-S2009/AMB-1783). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Ecosystems are changing at an unprecedented rate in response to global change [1]. One of its most powerful and probably least studied drivers is land use change. During the last century two opposing forces have coexisted in well-developed regions, such as at the northern fringe of the Mediterranean basin [2], regarding land use: either intensification or abandonment [3,4]. Abandonment is currently occurring in low productive areas (e.g. difficult accessible slopes, steep mountain areas) where the rural exodus has been very significant [5]. Current vegetation dynamics in abandoned fields is modulated by factors such as, past use and management history, soil characteristics, climate and propagules availability [6]. The arrival of seeds to non-forested areas is a key stage in the process of colonization of abandoned agricultural lands [7] as seed dispersal decreases with the distance to the forest edge [8]. For fleshy fruited species the arrival of seeds to non-forested areas is a function of the abundance, composition and behaviour of the members of the dispersers community [9]. The service provided by each disperser to a given plant species varies according to differences in both, the quantitative and qualitative components of the dispersal process [10]. The quantitative components are related to differences in the number of visits to a feeding plant, fruits dispersed per visit and local abundance of dispersers. While qualitative component would be mediated by differences in seed retention time, gut treatment and movement behaviours such as home versus foraging range and daily movement patterns (e.g. scent marking, anti-predator behaviour) [11]. Despite dispersers differ in these dispersal components [12,13,14], most of the research on seed dispersal mutualisms has been focused on single species, or at the best, in single functional groups. However the few works in which the complete assemblage was considered have reinforced the idea that each species differentially contributed to the quantitative and qualitative terms of the dispersal process [12,15,16,17]. In order to assess how seed dispersal contributes to critical ecological processes such as forest maintenance, regeneration and colonization, the complete community of potential dispersers and their differential behaviour need to be taken into account [16,18,19]. Composition of the dispersers community and their behavior could vary according to the environmental heterogeneity and ecosystem structure (e.g. woody and shrub cover, fruiting environment) [19,20]. This knowledge seems critical in order to unveil how woodland expansion due to land abandonment operates and to develop adequate management strategies. Woodlands of Juniperus thurifera have been subjected to a traditional management (e.g. logging, grazing and destruction for crop cultivation), however since the middle of the XIX century these activities have drastically decreased allowing the species to increase in density and currently to colonize abandoned fields [21,22] which is provoking a spectacular shift into new colonization areas [23]. J. thurifera is a fleshy fruited relict tree with a diverse assemblage of legitimate seed dispersers, such as thrushes Turdus spp. [24,25]; carnivores, such as red foxes (Vulpes vulpes) and stone martens (Martes foina) [12,15]; herbivores, as rabbits (Oryctolagus cuniculus) [12 (...truncated)