Can natural forest expansion contribute to Europe's restoration policy agenda? An interdisciplinary assessment.

Natural forest expansion (NFE), that is, the establishment of secondary forest on non-forested land through natural succession, has substantially contributed to the widespread expansion of forests in Europe over the last few decades. So far, EU policies have largely neglected the potential of NFE for meeting policy objectives on restoration. Synthesising recent interdisciplinary research, this paper assesses the challenges and opportunities of NFE in view of contributing to European forest and ecosystem restoration. Specifically, we discuss the potential for supporting climate change mitigation and adaptation, biodiversity conservation, and forestry and economic use, summarize the current knowledge about societal perceptions and the policymaking on NFE, and make policy recommendations to better use the potential of NFE. We conclude that NFE has the potential to contribute to the European restoration policy agenda if local contexts and possible trade-offs are properly considered.

Masting is uncommon in trees that depend on mutualist dispersers in the context of global climate and fertility gradients.

The benefits of masting (volatile, quasi-synchronous seed production at lagged intervals) include satiation of seed predators, but these benefits come with a cost to mutualist pollen and seed dispersers. If the evolution of masting represents a balance between these benefits and costs, we expect mast avoidance in species that are heavily reliant on mutualist dispersers. These effects play out in the context of variable climate and site fertility among species that vary widely in nutrient demand. Meta-analyses of published data have focused on variation at the population scale, thus omitting periodicity within trees and synchronicity between trees. From raw data on 12 million tree-years worldwide, we quantified three components of masting that have not previously been analysed together: (i) volatility, defined as the frequency-weighted year-to-year variation; (ii) periodicity, representing the lag between high-seed years; and (iii) synchronicity, indicating the tree-to-tree correlation. Results show that mast avoidance (low volatility and low synchronicity) by species dependent on mutualist dispersers explains more variation than any other effect. Nutrient-demanding species have low volatility, and species that are most common on nutrient-rich and warm/wet sites exhibit short periods. The prevalence of masting in cold/dry sites coincides with climatic conditions where dependence on vertebrate dispersers is less common than in the wet tropics. Mutualist dispersers neutralize the benefits of masting for predator satiation, further balancing the effects of climate, site fertility and nutrient demands.

Demographic and spatially explicit landscape genomic analyses in a tropical oak reveal the impacts of late Quaternary climate change on Andean montane forests.

The tropical Andes are one of the most important biodiversity hotspots on Earth, yet our understanding of how their biotas have responded to Quaternary climatic oscillations is extraordinarily limited and the alternative models proposed to explain their demographic dynamics have been seldom formally evaluated. Here, we test the hypothesis that the interplay between the spatial configuration of geographical barriers to dispersal and elevational displacements driven by Quaternary cooling-warming cycles has shaped the demographic trajectories of montane oak forests (Quercus humboldtii) from the Colombian Andes. Specifically, we integrate genomic data and environmental niche modelling at fine temporal resolution to test competing spatially explicit demographic and coalescent models, including scenarios considering (i) isotropic gene flow through the landscape, (ii) the hypothetical impact of contemporary barriers to dispersal (i.e., inter-Andean valleys), and (iii) distributional shifts of montane oak forests from the Last Glacial Maximum to the present. Although our data revealed a marked genetic fragmentation of montane oak forests, statistical support for isolation-with-migration models indicates that geographically separated populations from the different Andean Cordilleras regularly exchange gene flow. Accordingly, spatiotemporally explicit demographic analyses supported a model of flickering connectivity, with scenarios considering isotropic gene flow or currently unsuitable habitats as persistent barriers to dispersal providing a comparatively worse fit to empirical genomic data. Overall, these results emphasize the role of landscape heterogeneity on shaping spatial patterns of genomic variation in montane oak forests, rejecting the hypothesis of genetic continuity and supporting a significant impact of Quaternary climatic oscillations on their demographic trajectories.

Tolerance to seed predation mediated by seed size increases at lower latitudes in a Mediterranean oak.

BACKGROUND AND AIMS: The ability of plants to allocate energy to resistance against herbivores changes with abiotic conditions and thus may vary along geographical clines, with important consequences for plant communities. Seed size is a plant trait potentially influencing plant tolerance to endoparasites, and seed size often varies across latitude. Consequently, plant tolerance to endoparasites may change across geographical clines. METHODS: The interaction between Quercus ilex (holm oak) and seed-predating Curculio spp. (weevils) was explored along most of the latitudinal range of Q. ilex. This included quantification of variation in seed size, survival likelihood of infested seeds, multi-infestation of acorns and community composition of Curculio weevils in acorns. KEY RESULTS: Larger seeds had a higher probability of surviving weevil attack (i.e. embryo not predated). Southern populations of oak produced on average four times larger seeds than those of northern populations. Consequently, the probability of survival of infested acorns decreased with latitude. The community composition of Curculio varied, with large weevils (C. elephas) dominating in southern populations and small weevils (C. glandium) dominating in northern populations. However, damage tolerance was robust against this turnover in predator functional traits. Furthermore, we did not detect any change in multi-infestation of acorns along the geographical gradient. CONCLUSIONS: Quercus ilex tolerance to seed predation by Curculio weevils increases toward the southern end of its distribution. Generally, studies on geographical variation in plant defence against enemies largely ignore seed attributes or they focus on seed physical barriers. Thus, this research suggests another dimension in which geographical trends in plant defences should be considered, i.e. geographical variation in tolerance to seed predators mediated by seed size.

Distribution and space use of seed-dispersing rodents in central Pyrenees: implications for genetic diversity, conservation and plant recruitment.

The function and conservation of many forest ecosystems depend on the distribution and diversity of the community of rodents that consume and disperse seeds. The habitat preferences and interactions are especially relevant in alpine systems where such granivorous rodents reach the southernmost limit of their distribution and are especially sensitive to global warming. We analyzed the community of granivorous rodents in the Pyrenees, one of the southernmost mountain ranges of Europe. Rodent species were identified by DNA with particular attention to the Apodemus species, which are prominent seed-dispersing rodents in Europe. We confirmed for the first time the presence of the yellow-necked mouse, Apodemus flavicollis, in central Pyrenees, a typical Eurosiberian species that reaches its southernmost distribution limit in this area. We also found the wood mouse, Apodemus sylvaticus, a related species more tolerant to Mediterranean environments. Both rodents were spatially segregated by altitude. A. sylvaticus was rare at high altitudes, which might cause the genetic differentiation between populations of the different valleys reported here. We also found other seed consumers like dormice, Elyomis quercinus, and voles, Myodes glareolus, with marked habitat preferences. We suggest that population isolation among valleys may increase the genetic diversity of rodents, like A. sylvaticus. We also highlight the potential threat that global warming may represent for species linked to high-altitude refuges at the southern edge of its distribution, like Apodemus flavicollis. Finally, we discuss how this threat may have a dimension in the conservation of alpine forests dispersed by these rodent populations.

Role of seed size, phenology, oogenesis and host distribution in the specificity and genetic structure of seed weevils (Curculio spp.) in mixed forests.

Synchrony between seed growth and oogenesis is suggested to largely shape trophic breadth of seed-feeding insects and ultimately to contribute to their co-existence by means of resource partitioning or in the time when infestation occurs. Here we investigated: (i) the role of seed phenology and sexual maturation of females in the host specificity of seed-feeding weevils (Curculio spp.) predating in hazel and oak mixed forests; and (ii) the consequences that trophic breadth and host distribution have in the genetic structure of the weevil populations. DNA analyses were used to establish unequivocally host specificity and to determine the population genetic structure. We identified 4 species with different specificity, namely Curculio nucum females matured earlier and infested a unique host (hazelnuts, Corylus avellana) while 3 species (Curculio venosus, Curculio glandium and Curculio elephas) predated upon the acorns of the 2 oaks (Quercus ilex and Quercus pubescens). The high specificity of C. nucum coupled with a more discontinuous distribution of hazel trees resulted in a significant genetic structure among sites. In addition, the presence of an excess of local rare haplotypes indicated that C. nucum populations went through genetic expansion after recent bottlenecks. Conversely, these effects were not observed in the more generalist Curculio glandium predating upon oaks. Ultimately, co-existence of weevil species in this multi-host-parasite system is influenced by both resource and time partitioning. To what extent the restriction in gene flow among C. nucum populations may have negative consequences for their persistence in a time of increasing disturbances (e.g. drought in Mediterranean areas) deserves further research.

The Moran effect and environmental vetoes: phenological synchrony and drought drive seed production in a Mediterranean oak.

Masting is the highly variable production of synchronized seed crops, and is a common reproductive strategy in plants. Weather has long been recognized as centrally involved in driving seed production in masting plants. However, the theory behind mechanisms connecting weather and seeding variation has only recently been developed, and still lacks empirical evaluation. We used 12-year long seed production data for 255 holm oaks (Quercus ilex), as well as airborne pollen and meteorological data, and tested whether masting is driven by environmental constraints: phenological synchrony and associated pollination efficiency, and drought-related acorn abscission. We found that warm springs resulted in short pollen seasons, and length of the pollen seasons was negatively related to acorn production, supporting the phenological synchrony hypothesis. Furthermore, the relationship between phenological synchrony and acorn production was modulated by spring drought, and effects of environmental vetoes on seed production were dependent on last year's environmental constraint, implying passive resource storage. Both vetoes affected among-tree synchrony in seed production. Finally, precipitation preceding acorn maturation was positively related to seed production, mitigating apparent resource depletion following high crop production in the previous year. These results provide new insights into mechanisms beyond widely reported weather and seed production correlations.

The role of nutrients, productivity and climate in determining tree fruit production in European forests.

Fruit production (NPPf ), the amount of photosynthates allocated to reproduction (%GPPf ) and their controls for spatial and species-specific variability (e.g. nutrient availability, climate) have been poorly studied in forest ecosystems. We characterized fruit production and its temporal behaviour for several tree species and resolved the effects of gross primary production (GPP), climate and foliar nutrient concentrations. We used data for litterfall and foliar nutrient concentration from 126 European forests and related them to climatic data. GPP was estimated for each forest using a regression model. Mean NPPf ranged from c. 10 to 40 g C m-2  yr-1 and accounted for 0.5-3% of GPP. Forests with higher GPPs produced larger fruit crops. Foliar zinc (Zn) and phosphorus (P) concentrations were associated positively with NPPf , whereas foliar Zn and potassium (K) were negatively related to its temporal variability. Maximum NPPf and interannual variability of NPPf were higher in Fagaceae than in Pinaceae species. NPPf and %GPPf were similar amongst the studied species despite the different reproductive temporal behaviour of Fagaceae and Pinaceae species. We report that foliar concentrations of P and Zn are associated with %GPPf , NPPf and its temporal behaviour.

The Interplay among Acorn Abundance and Rodent Behavior Drives the Spatial Pattern of Seedling Recruitment in Mature Mediterranean Oak Forests.

The patterns of seedling recruitment in animal-dispersed plants result from the interactions among environmental and behavioral variables. However, we know little on the contribution and combined effect of both kinds of variables. We designed a field study to assess the interplay between environment (vegetation structure, seed abundance, rodent abundance) and behavior (seed dispersal and predation by rodents, and rooting by wild boars), and their contribution to the spatial patterns of seedling recruitment in a Mediterranean mixed-oak forest. In a spatially explicit design, we monitored intensively all environmental and behavioral variables in fixed points at a small spatial scale from autumn to spring, as well as seedling emergence and survival. Our results revealed that the spatial patterns of seedling emergence were strongly related to acorn availability on the ground, but not by a facilitation effect of vegetation cover. Rodents changed seed shadows generated by mother trees by dispersing most seeds from shrubby to open areas, but the spatial patterns of acorn dispersal/predation had no direct effect on recruitment. By contrast, rodents had a strong impact on recruitment as pilferers of cached seeds. Rooting by wild boars also reduced recruitment by reducing seed abundance, but also by changing rodent's behavior towards higher consumption of acorns in situ. Hence, seed abundance and the foraging behavior of scatter-hoarding rodents and wild boars are driving the spatial patterns of seedling recruitment in this mature oak forest, rather than vegetation features. The contribution of vegetation to seedling recruitment (e.g. facilitation by shrubs) may be context dependent, having a little role in closed forests, or being overridden by directed seed dispersal from shrubby to open areas. We warn about the need of using broad approaches that consider the combined action of environment and behavior to improve our knowledge on the dynamics of natural regeneration in forests.

Complex selection on life-history traits and the maintenance of variation in exaggerated rostrum length in acorn weevils.

Trophic interactions can trigger the development of exaggerated specialized characters and promote morphological diversification. For example, acorn weevils (genus Curculio) present strikingly long rostrums, which are used by females to perforate oviposition holes through the seed coat. Species exhibiting longer rostrums are known to exploit larger acorns, and therefore rostrum length is thought to be subject to selection to match the preferred acorn type. However, rostrum length is strongly correlated with body size, and morphological divergence could result from either selection on rostrum length for optimal food exploitation or from other pressures acting on body size. We collected infested acorns at oak forests where the large Curculio elephas and the small-bodied Curculio glandium co-occur. There were no interspecific differences in adult female body size to rostrum length allometric relationships, and rostrum length is equally correlated with body size in either species. MtDNA-based species identification showed that C. glandium larvae were present within acorns of all sizes, whereas C. elephas larvae were restricted to acorns above a minimum size, irrespective of oak species. Hence, exploitation of large acorns can hardly have triggered rostrum enlargement, as the small sized C. glandium adults (with short rostrums) could perforate and oviposit in both small and large acorns. Rather, increased rostrum length is probably a by-product of the larger body sizes of individuals emerging from bigger acorns, which allow increased larval size and enhance larval survival likelihood. Summarizing, when exaggerated feeding traits co-vary with other body features, interspecific morphological variability may result from contrasting selective pressures acting on these correlated characters.

Trade-offs between vegetative growth and acorn production in Quercus lobata during a mast year: the relevance of crop size and hierarchical level within the canopy.

The concept of trade-offs between reproduction and other fitness traits is a fundamental principle of life history theory. For many plant species, the cost of sexual reproduction affects vegetative growth in years of high seed production through the allocation of resources to reproduction at different hierarchical levels of canopy organization. We have examined these tradeoffs at the shoot and branch level in an endemic California oak, Quercus lobata, during a mast year. To determine whether acorn production caused a reduction in vegetative growth, we studied trees that were high and low acorn producers, respectively. We observed that in both low and high acorn producers, shoots without acorns located adjacent to reproductive shoots showed reduced vegetative growth but that reduced branch-level growth on acorn-bearing branches occurred only in low acorn producers. The availability of local resources, measured as previous year growth, was the main factor determining acorn biomass. These findings show that the costs of reproduction varied among hierarchical levels, suggesting some degree of physiological autonomy of shoots in terms of acorn production. Costs also differed among trees with different acorn crops, suggesting that trees with large acorn crops had more available resources to allocate for growth and acorn production and to compensate for immediate local costs of seed production. These findings provide new insight into the proximate mechanisms for mast-seeding as a reproductive strategy.

Acorn crop size and pre-dispersal predation determine inter-specific differences in the recruitment of co-occurring oaks.

The contribution of pre-dispersal seed predation to inter-specific differences in recruitment remains elusive. In species with no resistance mechanisms, differences in pre-dispersal predation may arise from differences in seed abundance (plant satiation) or in the ability of seeds to survive insect infestation (seed satiation). This study aimed to analyse the impact of pre-dispersal acorn predation by weevils in two co-occurring Mediterranean oaks (Quercus ilex and Quercus humilis) and to compare its relevance with other processes involved in recruitment. We monitored the patterns of acorn production and acorn infestation by weevils and we conducted experimental tests of acorn germination after weevil infestation, post-dispersal predation and seedling establishment in mixed forests. Monitoring and experimental data were integrated in a simulation model to test for the effects of pre-dispersal predation in recruitment. In both oaks pre-dispersal acorn infestation decreased with increasing acorn crop size (plant satiation). This benefited Q. ilex which exhibited stronger masting behaviour than Q. humilis, with almost a single and outstanding reproductive event in 6 years. Acorn infestation was more than twice as high in Q. humilis (47.0%) as in Q. ilex (20.0%) irrespective of the number of seeds produced by each species. Although germination of infested acorns (seed satiation) was higher in Q. humilis (60%) than in Q. ilex (21%), this could barely mitigate the higher infestation rate in the former species, to reduce seed loss. Conversely to pre-dispersal predation, no inter-specific differences were observed either in post-dispersal predation or seedling establishment. Our results indicate that pre-dispersal predation may contribute to differences in seed supply, and ultimately in recruitment, between co-existing oaks. Moreover, they suggest that seed satiation can barely offset differences in seed infestation rates. This serves as a warning against overemphasising seed satiation as a mechanism to overcome seed predation by insects.

Masting mediated by summer drought reduces acorn predation in Mediterranean oak forests.

Temporally variable production of seed crops by perennial plants (masting) has been hypothesized to be a valuable mechanism in the reduction of seed predation by satiating and starving seed consumers. To achieve these benefits, coexisting species subjected to the same predator would benefit from a similar pattern of seeding fluctuation over time that could lead to a reduction in predation at the within-species level. We tested for the existence of an environmental factor enforcing synchrony in acorn production in two sympatric Mediterranean oaks (Quercus ilex and Q. humilis) and the consequences on within-species and between-species acorn predation, by monitoring 15 mixed forests (450 trees) over seven years. Acorn production in Q. ilex and Q. humilis was highly variable among years, with high population variability (CVp) values. The two species exhibited a very different pattern across years in their initial acorn crop size (sum of aborted, depredated, and sound acorns). Nevertheless, interannual differences in summer water stress modified the likelihood of abortion during acorn ripening and enforced within- and, particularly, between-species synchrony and population variability in acorn production. The increase in CVp from initial to mature acorn crop (after summer) accounted for 33% in Q. ilex, 59% in Q. humilis, and 60% in the two species together. Mean yearly acorn pre-dispersal predation by invertebrates was considerably higher in Q. humilis than in Q. ilex. Satiation and starvation of predators was recorded for the two oaks, and this effect was increased by the year-to-year variability in the size of the acorn crop of the two species combined. Moreover, at a longer time scale (over seven years), we observed a significant reduction in the mean proportion of acorns depredated for each oak and the variability in both species' acorn production combined. Therefore, our results demonstrate that similar patterns of seeding fluctuation over time in coexisting species mediated by an environmental cue (summer drought) may contribute to the reduction of the impact of seed predation at a within-species level. Future research should be aimed at addressing whether this process could be a factor assisting in the coexistence of Q. ilex and Q. humilis.