The English yew, Taxus baccata L., once widespread, is now a relict forest tree species in Europe (Thomas & Polwart, 2003). Over the past centuries, yew populations have been declining in number, size, and therefore in connectivity (Dovčiak, 2002; Linares, 2013), especially at the margins of its geographical range (Sanz, 2008; González-Martínez et al., 2010). In the Iberian Peninsula, T. baccata is widespread, but most populations are small and suffer from lack of regeneration due to constrained recruitment (Abel et al., 2007; Sanz et al., 2009; Linares, 2013). Two major causes have been evoked to explain recruitment limitations: either too few seeds are produced and dispersed (seed limitation) or, even if produced in great number, these seeds do not reach favorable microsites for establishment of new individuals (establishment limitation; Mendoza et al., 2009). In yew populations, current empirical evidences showed that seed dispersal is strongly biased in space at a very fine scale, thus supporting the latter statement (Hulme, 1996; García & Obeso, 2003; Martínez et al., 2008; Sanz et al., 2009; Linares, 2013). Indeed, emergence and survival of T. baccata seedlings are highly sensitive to water availability (Sanz et al., 2009), herbivory (García et al., 2000; García & Obeso, 2003), light availability (Svenning & Magard, 1999; Devaney et al., 2014), and conspecifics density (Dovčiak, 2002; Devaney et al., 2014). Given these restrictions, the fine-scale pattern of seed dispersal, by setting the initial template for establishment, is a crucial determinant of population renewal (Schupp & Jordano, 2011; Beckman & Rogers, 2013).

As many fleshy-fruited plants, yew relies on the interaction with frugivorous animals for efficient dispersal, therefore, for establishment and survival of new individuals (Howe & Smallwood, 1982; Jordano & Schupp, 2000; Schupp et al., 2010). Both the number of dispersed seeds and the place where they are deposited strongly depend upon the identity and the behavior of the frugivorous animals (Jordano & Schupp, 2000; González-Varo et al., 2014). In temperate ecosystems, the main seed dispersers of fleshy-fruited trees are carnivorous mammals and birds (Guitián & Munilla, 2010; García et al., 2010; Peredo et al., 2013). Birds typically account for a large proportion of dispersed seeds (Jordano, 1987; Herrera, 1998; Martínez et al., 2008), depositing them at very short distances from mother trees (Godoy & Jordano, 2001; Jordano et al., 2007; Martínez et al., 2008), and usually under tree canopies as a result of their active selection of forest habitats (Alcántara et al., 2000; Jordano & Schupp, 2000; Martínez et al., 2008; Martínez & García, 2015a). This is the case of yew in the Cantabrian mountains (N Spain), for which birds tend to disproportionately disperse the seeds beneath conspecific adult trees (García et al., 2005b; Martínez et al., 2008), a pattern that may hamper recruitment due to increase predation, pathogen attack, and competition in high-density seed or seedling clumps (Janzen-Connell effects; Janzen, 1970; Schupp & Jordano, 2011; Devaney et al., 2014). In any case, birds also disperse some seeds underneath heterospecific trees or shrubs, both of which may provide suitable microsites for seedling survival (Giertych, 2000; García et al., 2000; García & Obeso, 2003; García et al., 2005b). Additionally, carnivorous mammals have been found to disperse a small fraction of seeds and contribute rather differently, as they frequently defecate the seeds in open areas such as trails or rocks, but generating very big clumps in faeces and latrines (Guitián & Munilla, 2010; Peredo et al., 2013). Although germination rate and seedling survival after mammal deposition are likely to be low, mammal seed dispersal may still play a role in re-colonizing deforested and distant areas (Jordano et al., 2007; Escribano-Avila et al., 2012; Peredo et al., 2013).

Besides the spatial components, an important feature of plant-frugivore interactions is their temporal variability (Jordano, 1993). The amount of fruits available for frugivores usually varies within and between years (Herrera, 1998; Guitián & Munilla, 2010). Similarly, the abundance of frugivores also shows inter-annual fluctuations, especially when they belong to migrant species (e.g. Turdus spp., Jordano, 1993; Tellería et al., 2014). Thus, the yearly patterns of yew seed dispersal are expected to change, as conditioned by both community-whole fruit availability and frugivore abundance (see Martínez & García, 2015a, for other tree species with similar dispersal syndrome).

The seed dispersal system of many fleshy-fruited trees have been found to display strong spatio-temporal variability (Jordano, 1993; Herrera, 1998; Perea et al., 2013). However, few studies have actually assessed how consistent or inconsistent are those systems. On one hand, discerning whether the local, small-scale patterns of seed dispersal – with most of seeds being deposited under conspecific trees but very few out of forest – are generalized across yew distribution range is a prerequisite for the development of integrative and large-scale management plans (see also Sanz et al., 2009). On the other hand, understanding the magnitude and the sense of inter-annual variability in yew seed dispersal patterns is key to assess the ability of the species to cope with rapid ecological changes, especially those derived from human impact (Hampe, 2011).

In this study, we have explored the variability in the seed dispersal system of T. baccata L. over a large geographic extent in the Iberian Peninsula and across different years. We selected yew populations encompassing contrasted biogeographical conditions (Eurosiberian vs Mediterranean), and studied the seed dispersal patterns during two consecutive years. Specifically, we i) quantified the small-scale spatial heterogeneity of the seed rain, ii) identified the assemblage of frugivorous animals interacting with T. baccata, assessing the relative contribution of different frugivore types to the seed rain, and iii) discussed the relevance of observed spatio-temporal consistencies, or inconsistencies, in terms of regeneration limitations in the context of yew large-scale conservation and management.

For fleshy-fruited trees, the interaction with frugivorous species is key to prevent vulnerable populations from collapsing (Farwig & Berens, 2012; Caughlin et al., 2015). Due to a low population growth rate associated with reduced recruitment, Taxus baccata is highly vulnerable to landscape degradation and climate change (Dovčiak, 2002; Thomas & Polwart, 2003; Abel et al., 2007). Therefore, comprehending its seed dispersal dynamics is of particular importance for the persistence, hence the conservation, of the species. In this study, we have analysed the spatial and temporal variability in the seed dispersal system of T. baccata along a large geographic gradient representing contrasted biogeographical (Eurosiberian vs Mediterranean), demographic (large vs relictual populations), and ecological (rich vs poor forest communities) conditions. Despite environmental variability, we found a consistent pattern in the three study sites, with the vast majority of the seeds dispersed beneath the canopy of conspecific trees, and very few in open areas. Also, we identified thrushes, Turdus spp., as the main, if not exclusive, seed dispersers.

Overall, our results showed that the bird-dispersed seeds were non-randomly distributed in the landscape, but were rather aggregated into a limited number of microhabitat types while many others received little or no seeds (Figure 2). Trees concentrated on average 98.8% of the bird-dispersed seeds, 80% being under yew females. Open microhabitats received virtually no seeds in all three study sites (Figure 2). These results were in agreement with previous studies at Peña Mayor study site (García et al., 2005b; Martínez et al., 2008) and in other study systems (Jordano et al., 2007; González-Varo et al., 2014), therefore suggesting temporal consistency over a longer time scale, but go beyond when scaling-up seed dispersal patterns from a local to a geographical extent.

Considering that the landscape itself was highly heterogeneous at the three study sites, the aggregated distribution of the seed rain could reflect the local patchiness of the microhabitats (Nathan & Muller-Landau, 2000). Nonetheless, some studies have shown that seed dispersal patterns do not necessarily match with microhabitat availaibility (Bartuszevige & Gorchov, 2006; Lavabre et al., 2014). Actually, at Escobarejos, 84 % of the bird-dispersed seeds were found beneath female yews in both years when these barely cover 0.4% of the landscape (Lavabre et al., 2014). This seems to be also the case for the other sites studied here, where the cover of yew canopies represents a small part of the local surface but the open habitat is dominant.

Our experimental design could have, to some extent, affected the observed seed rain heterogeneity – at Peña Mayor and Esocbarejos study sites – because open quadrats are prone to seed losses due to either abiotic (e.g. strong wind) or biotic (e.g. seed removal by rodents) factors. Nonetheless, if the losses are homogeneous among the seed-plots, we might have quantitatively, but not qualitatively, underestimated the number of dispersed seeds. Indeed, abiotic factors are not expected to unevenly affect the seed-plots. Rodents, on the contrary, are known to be selective, both for the species they feed on and the microhabitat where they forage (Hulme, 1997; García et al., 2005a). Since we have counted the predated seeds as part of the dispersed seeds, we have accounted for a part of the potential bias due to rodent seed removal. In addition, the microhabitats usually showing the highest predation rate are those for which we found the highest seed densities, i.e. yew trees (Figure 2A; García et al., 2005a). In the case that, in spite of accounting for predated seeds, we have still underestimated the number of seeds dispersed beneath yew trees, then it would suggest that these microhabitats received even higher seed densities that what we found, thus reinforcing the present differences between microhabitats.

In addition to the general spatial patterns in the bird-generated seed rain, we observed subtle interannual variations (Figure 2B). For example, at Peña Mayor, the relative importance of many microhabitats varied between years. In 2006, the year with the largest bird-generated seed rain, a smaller fraction of seeds was dispersed under yew females, but a bigger proportion of seeds reached yew males and other tree species canopies (fleshy-fruited or not), suggesting that more seeds escaped from maternal neighborhood in 2006 than in 2007.

The coarse composition of the frugivore assemblage was, in general terms, consistent between sites and years (Figure 3). The main seed dispersers of T. baccata were always frugivorous birds, especially thrushes (Turdus merula, T. viscivorous, T. iliacus, and T. philomelos) since they accounted, on average, for 83% of the seed rain. As a group, thrushes largely select forested habitats, or trees when forest fragments are scarce, and usually avoid open habitats (Jordano & Schupp, 2000; García et al., 2010; Martínez & García, 2015a). In autumn, during the fruiting season of the fleshy-fruited species at our study sites, thrushes’ behavior is principally driven by fruit resource-tracking and protection against predators (García et al., 2011; Morales et al., 2013; Martínez & García, 2015b). This spatial behavior would then explain the skewed spatial patterns of seed dispersal in yew across its Iberian distribution range.

In spite of this general behavior, the different thrushes displayed some specificities in their patterns of fruit resource-tracking which likely translates into the seed rain (Morales et al., 2013). Turdus merula and T. iliacus preferentially forage around the focal trees, sometimes in big flocks (T. iliacus), and fly short distances towards the neighbouring microhabitats (Martínez et al., 2008), thus most likely dispersing the seeds within forest patches. On the other hand, Turdus viscivorus tends to fly long distances and hence would disperse a substantial amount of seeds among forest patches (Jordano & Schupp, 2000; Martínez et al., 2008; Morales et al., 2013). Indeed, Morales et al. (2013) showed that T. merula generated a more locally aggregated seed rain than T. viscivorus, who produced a more homogeneous seed rain at the landscape scale. We observed similar patterns at our study sites. For example, at Escobarejos, T. baccata female trees are mainly surrounded by conspecific males and open areas (Sanz, 2008; Lavabre et al., 2014). These were, indeed, the microhabitats receiving a greater fraction of bird-dispersed seeds in 2006, when T. merula was the dominant seed disperser. Similarly, in 2007, the increase in the percentage of seeds dispersed into microhabitats “non fleshy-fruited tree” and “fleshy-fruited tree” (Figure 2B) was consistent with the foraging behavior of T. viscivorus, who preferentially selects tall or fruit-bearing trees for perching or feeding, respectively.

The contribution of carnivorous mammals as seed dispersers was always low relative to birds’ role, even considering a potential overestimation due to differences in sampling structure. In any case, we found some inter-annual differences in some sites, such as in Peña Mayor, where their contribution in 2006 was twofold that in 2007. As judged from the differences in the density of dispersed seeds (18907 seeds in 2006 vs 2372 in 2007, Figure 2), we expect a yew fruit production bigger in 2006 than in 2007, to which mammals would have responded by increasing this species in their diet (see also Guitián & Munilla, 2010). Similarly at Escobarejos, the density of dispersed seeds in 2006 suggests a smaller fruit production than in 2007, which might explain the absence of mammal scats for this year. Despite their potential to disperse the seeds over long distances (Jordano et al., 2007; Matías et al., 2009), their role as efficient seed dispersers remain unclear. Indeed, Peredo et al. (2013) found that they deposited a large fraction of the seeds into unsuitable microhabitats for germination and seedling establisment, such as latrines in the case of badgers, a microsite where seeds are probably faced to overcrowding and recurrent disturbance (but see Escribano-Avila et al., 2012).

In sum, our results showed a consistent pattern of spatially-restricted seed dispersal that would help to explain the constrained yew regeneration and null population expansion in all studied environmental settings. Most of seeds were deposited under yew adults, likely suffering from the effects of density-dependent seed and seedling mortality (Janzen-Connell effects; Steinitz et al., 2011; Devaney et al., 2014), and few seeds were dispersed outside forest stands and far from established populations. Moreover, in the three study sites, regeneration was also probably establishment-limited since the availability of suitable sites for seedling recruitment was reduced. Indeed, open microhabitats were dominant but harmful for seedlings due to summer drought, in the Mediterranean region, or overbrowsing, in the Eurosiberian region (García & Obeso, 2003; Mendoza et al., 2009). Only fleshy-fruited trees of other species and shrubs seem favorable sites for establishment (García et al., 2000; García & Obeso, 2003), but these microhabitats are still scarce and received few seeds.

Such geographically consistent patterns have important consequences for the persistence of the species. A generalized spatially-restricted seed dispersal limits considerably the capacity of the species to cope with ecological disturbances such as fragmentation, habitat loss or human activities. On the long-term, ecological limitations – restricted dispersal and the concomitant recruitment bottleneck – translate to the genetic structure of the species, causing genetic erosion and elevated inbreeding (Hilfiker et al., 2004b, 2004a; Dubreuil et al., 2010; González-Martínez et al., 2010).

The seed-dispersal patterns of Taxus baccata were the result of complex interactions between the microhabitat mosaic within the landscape, the identity of the frugivore species and the combination of specific feeding behaviors within the frugivore assemblage. This study highlights the consistency of this mutualistic system and its derived ecological patterns across the species range in the Iberian Peninsula. Although a large proportion of the seeds lands underneath conspecifics, the fraction that escapes from the neighborhood of T. baccata trees is crucial for subsequent stages of the species’ population dynamics (González-Martínez et al., 2010; Schupp & Jordano, 2011). As the main driver of seed flow, frugivorous birds play a pivotal role for yew populations, however carnivorous mammals should not be neglected since they contribute to the recolonization process through long distance dispersal (Escribano-Avila et al., 2012). Conservation and management practices should focus on maintaining a frugivore assemblage as diverse as possible to allow for complementary seed dispersal (García & Martínez, 2012; Escribano-Avila et al., 2014), thus increasing the chance for a seed to reach favourable conditions and at some distance from the mother tree. Given the large-scale approach from which these recommendations emerge, we encourage to consider these guidelines in a trans-regional strategy for the conservation of yew populations in Southern Europe.