The outcomes of plant–animal mutualisms involving seed dispersal directly influence plant population recruitment patterns (Nathan & Muller-Landau 2000), their genetic structure (Hamrick, Murawski & Nason 1993), and their spatial dynamics within and among populations (Hubbell 2001; Levin et al. 2003). The frugivorous vertebrates generate seed rain patterns that capture the foraging and post-feeding movements of these animals; sites chosen for roosting, resting, perching or displaying frequently receive a disproportionate number of seeds generating spatially clumped seed rain patterns (Howe & Smallwood 1982; Schupp, Milleron & Russo 2002). The spatial distribution of the maternal progenies in the seed rain is reported to determine the recruitment patterns (Augspurger & Kitajima 1992; Donohue 2003). Seed clumps with mixed maternal seed sources showed increased seedling survival compared with genetically homogeneous seed clumps in certain microhabitats (i.e. a context-dependent response). Furthermore, kin-structured dispersal observed in multi-seeded fruits dispersed by frugivores results in strong patterns of genetic structure even in the presence of long-distance dispersal (Torimaru et al. 2007). In spite of having pervasive effects in determining plant population recruitment, the embedded genetic patterns arising from frugivore activity in heterogeneous landscapes remain virtually unknown.
Frugivore activity results in recruitment limitation when dispersed seeds fail to reach distant sites (distance limitation), when they are distributed among a few available sites (spatial limitation) or when seeds are selectively dispersed from few fruiting trees (source-biased dispersal) (Jordano & Godoy 2002; Schupp, Milleron & Russo 2002). In vertebrate-dispersed species inhabiting heterogeneous landscapes, these three types of seed dispersal limitation are likely to occur simultaneously. Furthermore, frequent visits of frugivorous vertebrates from certain fruiting trees to selected deposition sites result in a high number of correlated dispersal events, i.e. seeds are dispersed from the same maternal tree to the same deposition site (Epperson & Álvarez-Buylla 1997). This is the case for numerous frugivorous birds and mammals that frequently revisit certain sites for displaying (Wenny & Levey 1998), roosting (Jordano & Schupp 2000) or resting (Russo & Augspurger 2004). These foraging patterns likely result in a highly source-biased and/or spatially aggregated dispersal where we can expect an uneven contribution of the source trees to the seed rain and a highly non-random distribution of their progeny among microhabitat types (Hampe et al. 2008). These two key aspects of the seed rain, i.e. the identity of the contributing trees and the distribution of their maternal progenies after dispersal by frugivorous vertebrates in an environmentally structured landscape remain unexplored in spite of their potential influence in determining plant recruitment patterns.
In this study, we applied a direct maternal assignment method to describe how different maternal trees distribute their seed progeny among different microhabitat types in Prunus mahaleb, a fleshy-fruited species dispersed by frugivorous birds and mammals. The study site was located in a mosaic-like landscape with physiognomically distinct vegetation patches and soil types (hereafter microhabitats). Most frugivore species showed a strong preference for covered microhabitats and avoided open ones (without woody plant cover) (Jordano & Schupp 2000; García-Castaño 2001). Previous work has documented the foraging patterns of a diverse assemblage of frugivorous birds with a prevalent role as seed dispersers for Phoenicurus ochruros, Turdus viscivorus, Erithacus rubecula and Sylvia communis and of carnivorous mammals (Jordano & Schupp 2000; Jordano et al. 2007). These studies showed that the effectiveness of seed dispersal by frugivorous vertebrates varied widely among fruiting trees (source-biased dispersal) and that the number of dispersed seeds per deposition site strongly depended on microhabitat and spatial location (spatially aggregated dispersal, see Jordano & Schupp 2000; García-Castaño 2001; Jordano et al. 2007).
Given the seed rain that frugivorous vertebrates generate, we ask how different source trees contribute seeds to specific microhabitat types in the population and how genetically related the seeds dispersed to the same deposition site are. By genotyping the endocarp of dispersed seeds (a tissue of maternal origin), we specifically pursue to identify the source tree of dispersed seeds in the population (Godoy & Jordano 2001) and to estimate the maternal genetic correlations set in the seed rain following a similar approach as in Grivet, Smouse & Sork (2005). Maternal genetic correlations were assessed as: (i) the number of distinct contributing trees to different microhabitats (hereafter maternal richness); (ii) the relatedness among trees contributing seeds to one deposition site (maternal relatedness); and (iii) the probability that two seeds drawn at random from the same seed trap come from the same mother tree (hereafter correlated maternity).
By using a thorough sample of a vertebrate-dispersed seed rain that has been spread all over the population and a maternity analysis that allows to identify the source tree of dispersed seeds (Godoy & Jordano 2001; Ziegenhagen et al. 2003; Grivet, Smouse & Sork 2005; Jones et al. 2005), we aim to: (i) identify the source trees contributing to the seed rain; (ii) describe how maternal trees distribute their progeny among microhabitats; (iii) characterize the maternal genetic correlations in the seed rain; and (iv) assess the role of landscape features linked to the location of the seed traps in shaping the maternal genetic correlation patterns in the seed rain. We finally interpret our results considering previous information on the feeding and post-feeding movement patterns of frugivores to depict a comprehensive picture of the role of frugivores in determining the spatial genetic features in the seed rain.