Current habitat conservation policies (e.g. European Union’s Habitats Directive 92/43/CEE) state that management in abandoned and degraded habitats should aim to re-establish the structure and function of native plant communities (SER 2002). However, most current ecological approaches to this issue in the Mediterranean region are relatively simplistic because they measure the success of restoration techniques in terms of juvenile establishment, without explicit consideration of recovery of species composition, structure and properties similar to natural reference communities. In contrast to other studies in the Mediterranean region, here we have shown that nurse-assisted planting is not merely successful in achieving seedling establishment of many species but, more importantly, in assisting the recovery of community structure and properties. Thus, it should be preferred to traditional reforestation or no intervention in degraded Mediterranean mountain areas.
Establishment success using different restoration techniques
Traditional techniques for reforestation frequently show low establishment success because of summer mortality through water stress (Meson & Montoya 1993). In contrast with these practices, many studies have shown that the regeneration niche of woody species in the Mediterranean mountains is positively associated with shrubs (Rousset & Lepart 1999; García et al. 2000; Rey & Alcántara 2000). These studies confirmed a facilitative effect of shrubs and grasses on the early establishment of planted woody species. New restoration techniques for Mediterranean landscapes have been developed using naturally established shrubs and herbs as microhabitat for planting seedlings of woody species (Maestre et al. 2001; Castro et al. 2004, 2006; Gómez-Aparicio et al. 2004). Our results support this view, showing that post-fire establishment of planted tree seedlings is several times higher under the canopy of nurses (spontaneously established vegetation) than in open interspaces. Studies in Mediterranean environments have concluded that summer drought occurring during the first years after planting is the most limiting factor for the establishment of planted seedlings (García-Salmeron 1995; Rey-Benayas 1998; Gómez-Aparicio et al. 2004; Rey et al. 2004). The facilitative effect of nurses is primarily due to micro-environmental amelioration of water stress and irradiance and, secondarily, to improvement of soil texture and nutrient availability or grazing avoidance (Pugnaire et al. 1996; Gómez-Aparicio, Gomez, & Zamora 2005; Padilla & Pugnaire 2006; Baraza et al. 2006). Our results, showing increased seedling establishment under nurses compared with open interspaces, support the idea that a shift from traditional to nurse-assisted planting techniques will enhance post-fire seedling establishment of Mediterranean vegetation (Castro et al. 2004, 2006; Gómez-Aparicio et al. 2004) through alleviation of drought stress.
Community-level restoration profiles
The aims of ecological restoration should move beyond merely enhancing seedling establishment. A successful restoration project must achieve a community with the native components (species) and properties (structure, dynamics and resilience) of natural mature communities. Restoration techniques in seriously degraded areas should thus promote necessary changes in species composition and dynamics to eventually achieve the mature community (SER 2002). However, traditional techniques of reforestation have paid little attention to community properties and species composition. More surprisingly, more ecologically based techniques of restoration in the Mediterranean focus mainly on the establishment of multiple species and most frequently assume, rather than demonstrate, the recovery of community properties (but see Tucker & Murphy 1997; Shono et al. 2006 for other ecosystems, and Siles et al. 2008 in the Mediterranean). This study has attempted to bridge this gap, applying widely used community structure analytical tools to compare the community profiles resulting from different restoration practices, with control plots in naturally regenerating forest and reference plots in remnants of well-preserved communities.
Rarefaction analysis showed increased diversity of both trees and tall-shrubs in nurse-based restoration compared with traditional reforestation. Seedling diversity of planted trees can be doubled using nurse plants. Because we planted the same number of species in each treatment, the bank of juvenile tree species was comparable among treatments, and the results suggest that facilitation is shaping the diversity of the juveniles. Moreover, if planted tall-shrubs are also considered, the species diversity is almost five times higher than in traditional plantings. It could be argued that this last difference is artificially inflated as no shrubs were planted in the traditional treatment. However, we think that our conclusion is not an artefact of experimental design. First, traditional reforestation tends to eliminate rather than support shrub species, while more ecologically based techniques, such as nurse-based restoration, implement planting of tall-shrubs as important components of succession (Gómez-Aparicio et al. 2004; Castro et al. 2006). Secondly, we have additional evidence corroborating that most species of tall-shrubs fail to establish in our study area when planted without nurses (traditional reforestation) and that the mechanisms acting in their establishment under nurses are, primarily, due to amelioration of abiotic stresses and, secondarily, protection against ungulate grazing (G. Siles, P.J. Rey & J.M. Alcántara, unpublished data). Therefore, we believe the inclusion of tall-shrubs is a valid comparison of these restoration practices.
More interestingly, nurse-based restoration substantially increased the overall diversity when both planted seedlings and naturally regenerated species were considered. The community of established juveniles became extremely similar to that of adjacent well-preserved vegetation (i.e. the natural reference community). If compared with control plots of post-fire natural regeneration and traditional reforestation, the expected number of species of the nurse-based restoration was significantly higher and more similar to the reference community, indicating that planting under nurses effectively enriches the post-fire regenerated community, approaching the reference community in terms of both species composition and structure.
Evenness was very high in all treatments (including the reference community), except in the grazing-free control. This means that recruited seedlings were evenly distributed among species in the natural community and that the high evenness initially generated by planting did not result in an artefact in the structure of the restored community. In spite of these similarities, the rarefaction curves for nurse-based restoration and traditional planting saturated at lower richness, and showed higher evenness, than the curves for the reference community (which showed significantly higher Chao 2 richness than any management practice). Apart from the effect on evenness created by an even planting (in both traditional and nurse-based reforestation), the lower evenness and highest Chao 2 in juveniles of the reference community reveal the lack of rare species in the restored community. Multiple factors (not considered in our restoration practices) determine differences in natural recruitment among species, including species-specific seed removal, dispersal and predation, germination rate and seedling survival (Rey et al. 2002, 2004; Ramírez et al. 2006; Acacio et al. 2007). We would expect that evenness in planting treatments will approach that of the reference community as differential mortality among planted species occurs over time. Interestingly, the lower evenness in grazing-free controls of spontaneous regeneration, compared with exposed controls, suggests that frequency-dependent ungulate grazing is controlling species that otherwise would dominate the regenerated community.
The better community performance resulting from nurse-based restoration is also confirmed by the comparison of other community parameters, including woody cover, and number and diversity of growth forms. All these parameters are favoured under this restoration practice as it does not involve elimination of the naturally regenerated vegetation. The number of different growth forms is higher in the reference community, similar among the controls of natural regeneration and nurse-based restoration, but lower under traditional reforestation. The single type of life-form missing under nurse-based restoration is vines (which only appeared in the reference community), but these are expected to spontaneously enter the community some years after planting. Chao 2 richness of the nurse-based restoration community is then expected to approximate that of the reference community. Of particular importance is the lack of SPYN and vines, most frequently fleshy-fruited species, in traditional reforestation plots. We have evidence that the absence of fleshy fruits in burned areas decreases their attractiveness for frugivorous birds (Siles, Rey & Alcántara, unpublished; R. Zamora, personal communication), which are the major agents of seed dispersal in Mediterranean vegetation. Lack of fleshy fruits may thus cause succession to remain arrested in these zones (Debussche, Escarre, & Lepart 1982; McClanahan & Wolfe 1993; Acacio et al. 2007).
Restoration practices should favour species compositions and assemblages such that the successional pathways conducive to a defined reference community are promoted (SER 2002). It is too soon to draw these conclusions from our short-term study, and it is clear that long-term surveys using experimental designs like the ones presented here are needed to confirm such possibility. However, there is now some experimental and modelling evidence that suggests the capability of nurse-based restoration to launch secondary succession (see Gómez-Aparicio et al. 2004). In a parallel study in the same region, we simulated the post-fire dynamics of 20-year-old burned areas through Markovian models of species substitution (Siles et al. 2008). We corroborated that sites with frequent establishment of tall-shrub and tree seedlings under nurse plants projected a stable community of similar composition to a defined reference community (indicative of successful secondary succession). In contrast, sites with low seedling establishment under the established vegetation projected a pioneer community (indicative of a situation of arrested succession).
The modelling example above may also serve as an indicator of success in achieving another desired ecosystem property, the resilience or ability to quickly recover after a disturbance (SER 2002). Regardless of such findings, we believe that the much higher expected species richness obtained for nurse-based restoration in our experiments renders a quick increase in ecosystem resilience, as most of the naturally regenerated and planted species have resprouting capacity (Pausas & Verdú 2005). In contrast, the loss of tall-shrubs and trees in plots under traditional reforestation would imply a lowered resilience, as this technique causes an impoverishment of functionally redundant species, and a concomitant increase in the ecosystem’s sensitivity to disturbances (Fonseca & Ganade 2001).
To conclude, our study is the first to demonstrate that nurse-assisted restoration contributes to the recovery of important community properties. Many studies have shown that nurse-based planting enhances the establishment of woody species. We move beyond the species level to assess the efficacy of this technique at the community level. Compared with traditional reforestation and/or no intervention, the nurse-assisted restoration enhances: (i) species and life-form diversity in the community, (ii) late-successional species cover, (iii) the chance for secondary succession and, presumably, (iv) resilience in the restored community. In contrast, traditional techniques of reforestation in Mediterranean regions fall short of obtaining communities similar to reference communities. Therefore, nurse-assisted restoration should be implemented when the aim of management is the restoration of native communities.