a) Regeneration dynamics of Quercus
Succession was considerably arrested in the plots without tree remnants two to three decades after cultivation abandonment. Similar trends have been observed in other studies, where 45 years after abandonment Cistus-dominated shrublands prevailed with scarce or absent oak recruitment (Acácio and Holmgren 2014). Cistus-dominated shrublands, as well as acorn availability and drought stress, exert competition and inhibition effects over Quercus recruitment and appear as highly resilient systems (Pérez-Devesa et al. 2008, Rolo and Moreno 2011, Acácio and Holmgren 2014). However, shrub cover (mainly characterized by Cistus, Halimium and Lavandula spp.) was quite low in plots in old fields (< 10%, Table S2) and vegetation was dominated by annual herbaceous species, likely due to low rainfall combined with high sand and low organic soil contents that exacerbated hydric stress (Fernández-Ales et al. 1993, Rawls et al. 2003, Nunes et al. 2017). Q. ilex was the only tree species successfully recruiting in the open old fields, although slowly and with low densities, despite Q. suber being the dominant tree species in the landscape with respect to density and basal area. Two processes are likely involved in the success of Q. ilex over other Quercus species in the open plots. First, although Quercus species share the same animal dispersers, most studies have shown that acorns from Q. ilex are preferred over other Quercus species by the main oak disperser the Eurasian jay (Garrulus glandarius) and by small rodents (Pons and Pausas 2007ac, del Arco et al. 2018). Since the Eurasian jay is a forest species that has never been detected in the study area, mice species are the main candidates for acorn dispersal. Pilferage rates are reduced by caching the seeds preferentially outside the canopies of scattered trees, increasing the survival of cached acorns in open areas (Muñoz and Bonal 2011). However, limited facilitative shrub cover reduces successful recruitment causing a low density of Q. ilex seedlings (Pulido and Díaz 2005, Smit et al. 2009, Rolo and Moreno 2011). Second, although both evergreen species, Q. suber and Q. ilex, are well adapted to the summer drought of the Mediterranean climate (Mediavilla and Escudero 2003, González-Rodríguez et al. 2011, San-Eufrasio et al. 2020), previous studies have shown a higher survival rate for Q.ilex seedlings than for Q.suber (Plieninger et al. 2010, González-Rodríguez et al. 2011). In addition, Q. ilex has lower conductance and maximum transpiration rates than Q. suber, which delays leaf desiccation thanks to a more conservative use of water (Mediavilla and Escudero 2003, San-Eufrasio et al. 2020), which decreases growth suppression under high water stress (Caldeira et al. 2014).
Our results indicate that remnant oak trees are great accelerators of forest recovery after cultivation abandonment. Also, old fields with tree remnants boost oak regeneration almost 40-fold in comparison to old fields without trees, and woodlands show a 2-fold increase in oak regeneration in comparison to old fields with tree remnants. Tree cover is considered to play a fundamental role in Quercus recruitment through several processes. First, acorns are heavy fruits with limited dispersal, where most of the acorns produced only reach areas situated close to the parent trees (Pulido and Díaz 2005, Acácio et al. 2007, Pausas et al. 2009b). Second, facilitation effects caused by tree cover are key in the regeneration of Quercus species, especially in Mediterranean environments (Caldeira et al. 2014, Costa et al. 2017). Facilitation includes several direct and indirect mechanisms with positive effects on both survival and Quercus seedling growth. Drought stress and summer seedling survival during the first years of establishment is usually considered one of the main bottlenecks in Quercus regeneration (Díaz and Pulido 2005, Silla and Escudero 2004, Smit el al. 2009, Pérez-Ramos et al. 2012). Therefore, tree cover improves microclimate conditions reducing high summer temperatures and alleviating heat stress (Díaz and Pulido 2005, Pausas et al. 2009, Smit el al. 2009) and reduces competition with herbaceous vegetation (Caldeira et al. 2014). Our results are also consistent with these patterns, as tree basal area and density were strongly correlated with the first RDA ordination axis that ordered sites with a strong gradient of seedling density from right to left (Fig. 4). Additionally, the spatial analysis of small seedlings of Q. suber and Q.ilex, which accounted for most of the seedling abundance (71.6%) showed a clustered pattern associated with Quercus trees in both woodlands and old fields with tree remnants, although at shorter distances in Q. ilex than in Q. suber. By contrast, Quercus large seedlings showed a random spatial pattern independent of the trees, highlighting that tree cover is only a limiting factor during seedling establishment. These changes in the spatial pattern with ontogenetic development support previous findings that suggest that the positive effects of shaded microhabitats are reversed for seedling development (Pérez-Ramos et al 2011, Pausas et al. 2009b). In Q. suber and Q. ilex, seedling establishment and survival are improved under shade (Espelta et al. 1995, Pausas et al. 2009b, Smit et al. 2009, Pérez-Ramos et al. 2012). However, it has been also shown that low light suppresses growth, that these species establish ‘seedling banks’ under dense tree cover and that more open canopy conditions are required for saplings and trees to develop (Espelta et al. 1995, Pausas et al. 2009b, Pérez-Ramos et al. 2010, 2012). In addition, we also found significant differences in the regeneration densities of Q. suber,Q. ilex, Q. faginea, with the abundance of Q. suber strongly correlated with the basal area and tree density of stands. In woodlands, Q. suber dominated seedling regeneration in the categories with the shortest height, but the differences in seedling abundance between Q. ilex and Q. suber disappeared in the tallest categories and showed similar densities. In the old fields with tree remnants, Q. ilex and Q. suber showed similar seedling densities, and although the interaction was not significant, the abundance of Q. ilex large seedlings was 5-6 fold higher than that of Q. suber. These results indicate that Q. ilex has a higher seedling survival rate and more likely to reach the sapling stage, probably due to their higher tolerance to shade (Sevilla 2008), and in particular their greater tolerance to hydric stress during the summer (Plieninger et al. 2010, González-Rodríguez et al. 2011, San-Eufrasio et al. 2020). Thus, although Q. suber trees dominate the landscape of our study area, the results indicate that Q. ilex can produce a greater number of young trees as compared to Q. suber (Fig. 2b), owing to the better performance of Q. ilex seedlings. Only in woodlands can Q. suber partially compensate for their lower performance and survival, producing a higher number of seedlings. Conversely, the deciduous Q. faginea present the lowest abundance, especially in the old fields (with or without tree remnants), which is in line with its lower tolerance to drought compared to evergreen species (Silla and Escudero 2004, González-Rodríguez et al. 2011, San-Eufrasio et al. 2020).
The presence of tree remnants showed a strong effect over soil parameters with higher concentrations of organic matter, N, exchangeable cations (K+, Ca2+, Mg2+) and slightly less acidic soils than in old fields without tree remnants (Table S2). The deep root system of Q. suber trees uptakes and pumps basic cations, especially Ca2+, from the deep to upper soil layers throughout litterfall production and decomposition, which significantly improves soil nutrient availability (Serrasolses et al. 2009, Rossetti et al. 2015). The results of the variance partitioning showed that soil and stand structural parameters explain a significant amount of the shared variation in the amount of regeneration of Quercus species (Fig. 5), which makes sense since the influence of trees on soil characteristics are spatially correlated. However, soil variables also explain a significant amount of the variance (27.1%) not explained by structural stand variables and are important for understanding the differences found in Quercus regeneration between plots. Among soil variables, organic matter content summarizes most information on nutrient availability with which is strongly correlated (Table S2, Fig. S1), but it is also directly involved in improving soil water retention in abandoned cultivars, especially in soils with high sand content (Rawls et al. 2003, Costa et al. 2017).
b) Climate-growth relationships of suber trees
Analysis of the impact of climatic conditions on the tree-ring growth of Q. suber is challenging due to the difficulty in identifying ring boundaries in trees being managed for cork extraction (Costa et al. 2003). Only two previous studies have reported successful tree ring chronologies involving Q. suber in the Mediterranean region (Costa et al. 2003, Zribi et al. 2016) that have been complemented with short chronologies from cork growth-rings (Caritat et al. 1996, Costa et al 2016, Leite et al. 2019). As shown in these studies, winter and spring precipitation exerted a large positive effect on tree-ring growth due to the replenishment of soil water reserves before the onset of the favorable growing season (Costa et al. 2001, Jovellar et al. 2010, Costa et al 2016, Zribi et al. 2016, Leite et al. 2019). In our study site, Q. suber showed the latest leaf emergence of all coexisting Quercus species, with budbreak and emergence of the new leaf cohort occurring between the end of May and the beginning of June (del Río et al. 2015). However, in relation to other studies where temperature has been found to have an insignificant or negative effect over cork or ring growth (Caritat et al. 1996, Costa et al. 2001, Zribi et al. 2016), in our study site, the mean and minimum temperatures during winter and/or spring and the mean and maximum temperatures during September exerted a positive influence on tree growth. This is consistent with the cold temperature conditions occurring in winter and early spring in our study area, located at the leading temperature edge of its distribution limits in the Iberian Peninsula. The large vessels in oak trees are very sensitive to winter embolisms caused by freezing temperatures, and in spring the reactivation of growth is greatly dependent on hydraulic conductivity recovery (Hacke and Sauter 1996, Lebourgeois et al. 2004). This highlights the importance of mild winter-early spring temperatures on Q. suber tree growth in the “cold leading edge” of its distribution. However, although winter temperatures are a limiting factor and warming has room for net positive effects on tree growth (Sánchez-Salguero et al., 2015), climatic data did not reveal a significant temperature increase during winter and early spring in this study site. On the other hand, minimum temperatures during September have significantly increased during the last decades and have had a positive impact on tree growth by most likely extending the favorable weather (Marqués et al. 2018). However, the positive effect of an extended growing season in early autumn can be counteracted by a decrease in rainfall, especially in the study area where annual rainfall is also in the lower edge of Q. suber distribution limits, as has also been recently observed in Mediterranean forest at the limits of species distribution (Madrigal-González et al. 2018, Marqués et al. 2018). Although no significant decreasing trends were found in the more critical months (Fig. 6a), there is a decreasing trend in mean annual rainfall (Fig. S3), so more detailed studies will be needed to understand the combined effects of temperature and rainfall on tree growth within future climate change scenarios.