Frugivory and Spatial Patterns of Seed Deposition by Carnivorous Mammals in Anthropogenic Landscapes: A Multi-Scale Approach

Gonzalez-Varo JP (2011) Frugivory and Spatial Patterns of Seed Deposition by Carnivorous Mammals in Anthropogenic Landscapes: A Multi-Scale Approach. PLoS ONE 6(1): e14569. doi:10.1371/journal.pone.0014569 Frugivory and Spatial Patterns of Seed Deposition by Carnivorous Mammals in Anthropogenic Landscapes: A Multi-Scale Approach Jose V. Lo pez-Bao 0 Juan P. Gonza lez-Varo 0 Dennis Marinus Hansen, Stanford University, United States of America 0 1 Department of Conservation Biology , Estacio n Biolo gica de Do n ana (CSIC), Seville , Spain , 2 Departamento de Biolog a Vegetal y Ecolog a, Universidad de Sevilla , Seville , Spain Background: Knowledge about how frugivory and seed deposition are spatially distributed is valuable to understand the role of dispersers on the structure and dynamics of plant populations. This may be particularly important within anthropogenic areas, where either the patchy distribution of wild plants or the presence of cultivated fleshy-fruits may influence plant-disperser interactions. Methodology/Principal Findings: We investigated frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes considering two spatial scales: 'landscape' (,10 km2) and 'habitat type' (,1-2 km ). 2 We sampled carnivore faeces and plant abundance at three contrasting habitats (chestnut woods, mosaics and scrublands), each replicated within three different landscapes. Sixty-five percent of faeces collected (n = 1077) contained seeds, among which wild and cultivated seeds appeared in similar proportions (58% and 53%) despite that cultivated fruiting plants were much less abundant. Seed deposition was spatially structured among both spatial scales being different between fruit types. Whereas the most important source of spatial variation in deposition of wild seeds was the landscape scale, it was the habitat scale for cultivated seeds. At the habitat scale, seeds of wild species were mostly deposited within mosaics while seeds of cultivated species were within chestnut woods and scrublands. Spatial concordance between seed deposition and plant abundance was found only for wild species. Conclusions/Significance: Spatial patterns of seed deposition by carnivores differed between fruit types and seemed to be modulated by the fleshy-fruited plant assemblages and the behaviour of dispersers. Our results suggest that a strong preference for cultivated fruits by carnivores may influence their spatial foraging behaviour and lower their dispersal services to wild species. However, the high amount of seeds removed within and between habitats suggests that carnivores must play an important role - often overlooked - as 'restorers' and 'habitat shapers' in anthropogenic areas. - Funding: This research was funded by the project PGIDIT 05RFO 20001 PR (Conselleria de Educacion Xunta de Galicia) coordinated by the Grupo Biologa Evolutiva de Plantas (Universidad de Santiago de Compostela). The funders had no role in 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. Ecological processes associated with frugivory, seed dispersal and recruitment of endozoochorous plants are spatially structured due not only to plant distribution and habitat heterogeneity [1,2], but also to the local abundance and behaviour of seed dispersers [3,4]. The spatial scale at which plant-disperser interactions occur may determine the distribution, dynamics and genetic structure of plant populations and, therefore, of plant species assemblages [57]. Despite the well-known role of carnivorous mammals (Carnivora) as fruit consumers and seed dispersers [810], during the past three decades birds have captured almost all of the attention devoted to the study of frugivory and seed dispersal in temperate climate zones [11,12]. These studies have addressed a wide range of topics, including spatio-temporal variations in frugivore assemblages and frugivory, seed rain patterns, as well as their implications for the demography of plant populations [1114]. However, most studies performed to date with carnivores as legitimate seed dispersers have focused on a mere description of mutualistic relationships [8,1517] or on the evaluation of the effects of gut passage on seed viability and germination [1820], and only recently new topics have been addressed [21,22]. During the last decade, the spatial scale at which plant-disperser interactions are distributed have been addressed on different plantfrugivore systems, although mostly including birds [1,2,23,24]. However, none of the previous studies dealing with carnivores as seed dispersers have included or analyzed the mutualistic interaction at more than one spatial scale [8,15,1921,25]. Therefore, the spatial scale at which the ecological processes involving carnivores and fleshy-fruited plants take place remains largely unexplored [25,26]. Carnivores greatly differ from birds in terms of feeding behaviour, mobility, gut retention time, habitat use and spatial patterns of seed deposition [20,25,27], which are pivotal features in determining the spatial scale of plant-disperser interactions. For instance, differences in spatial mobility between frugivores may determine whether the patterns of frugivory and seed deposition are mostly influenced by local patch features or landscape configuration, which has important ecological implications in the dispersal ecology of plants [23]. This information is essential to understand the role of carnivores as dispersal vectors in a spatial context. Anthropogenic landscapes are characterized by the transformation of the original vegetation cover into man-made habitats such as managed forests, agricultural fields, orchards and pastures [28]. Hence, these landscapes typically are comprised of habitat patches that differ greatly in vegetation structure and composition, degree of perturbation, successional stage and current management [29]. Such spatial heterogeneity determines non-uniform distribution of fleshy-fruited species, which is expected to shape spatial patterns of carnivore-mediated seed deposition. Furthermore, anthropogenic systems may provide resources to fruit consumers in the form of cultivated fleshy-fruits [30], which may interfere with the dispersal mutualism of wild plant species [15]. Thus, the importance of studies of carnivore-mediated seed deposition in anthropogenic landscapes at multiple spatial scales is two-fold: (i) to understand the influence of the patchy distribution of plants on this mutualism, and (ii) to gauge the influence of cultivated fruits on native plant-carnivore interactions. Emergent information will improve our knowledge about the functioning of human-modified ecosystems in terms of plantcarnivore interactions [31] and, ultimately, about the services that carnivores provide as restorers of fleshy-fruited plant assemblag (...truncated)