Recovery of Native Grasslands after Removing ... - Moodle UFSC

Recovery of Native Grasslands after Removing Invasive Pines Yannina A. Cuevas1,2 and Sergio M. Zalba1 Abstract The advance of exotic tree and shrub species is one of the main threats to conservation of the last relicts of natural grassland in South America; however, control actions in the region are still scarce and there are almost no evaluations of the recovery of natural ecosystems after removing invasive plants. Monitoring of the vegetation during the years after removal of invasive trees is critical in order to decide whether an active restoration strategy is necessary. The recovery of montane grassland four years after the control of a dense invasion of Aleppo pine (Pinus halepensis) is described in this study. Experimental clearing areas were followed during four years and compared to grassland controls. Variation was seen in the levels of

Introduction Biological invasions might be considered as the greatest and fastest growing threat to global diversity (Williamson 1996, 1999). The advance of terrestrial plants causes the widest and most intensive changes on natural ecosystems. Exotic trees, shrubs, and herbs have demonstrated their capacity of colonizing natural habitats throughout the whole planet, altering nutrient cycles, extracting water from the water table, changing the frequency and intensity of natural fires, and provoking the decline of native plants and animals (Vitousek 1990; Cronk & Fuller 1995; Higgins et al. 1999). There are numerous cases of trees introduced for productive purposes, wind protection, or as ornamentals that then become aggressive invaders, usually as the result of alterations in natural disturbance regimes (Hobbs 1991; Richardson & Bond 1991; Calder et al. 1992; Richardson 1998; Mack et al. 2000). Pines, for example, have advanced over vast extensions of shrubland and grassland in the whole southern hemisphere, changing dominant life forms, reducing structural diversity, and modifying patterns of vegetation and nutrient cycles (Chilvers & Burdon 1983; Macdonald & Jarman 1985; Macdonald et al. 1989; Richardson et al. 1990, 1994; Richardson & Bond 1991; Richardson 1998; GISP 2005). 1 Gekko-Grupo de Estudios en Conservacioń y Manejo. Departamento de Biologıá, Bioquı´mica y Farmacia, Universidad Nacional del Sur, San Juan 670, Bahıá Blanca, 8000 Buenos Aires, Argentina 2 Address correspondence to S. M. Zalba, email [email protected]

Ó 2009 Society for Ecological Restoration International doi: 10.1111/j.1526-100X.2008.00506.x

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recovery in function of the proximity of sectors of grassland that are free of invasive species and/or the density of invasive trees before control. Native species slowly replaced many exotic herbs that had appeared as pioneers, there was low recruitment of pine seedlings in spite of the quantity of seeds from trees that surrounded the clearings, and species richness and diversity were restored, including cover of the typical grasses in the controls. Recovery of grassland after felling was shown to be successful and does not seem to be seed limited if tree removal occurs early in the invasion process. Key words: control, invasive alien species, Pinus halepen-

sis, restoration, South American grasslands.

Extensive areas of grasslands in South America have been used by the forestry industry, largely for planting different species of pine. Exotic species of pine have been also used for urban and rural forestation, as windbreaks, and for lining roads. In many cases, these species have spread further afield, provoking significant impacts on the scarce remnants of grassland that have historically remained untouched by agricultural activities. However, the control of invading trees in the region is still at an early stage (GISP 2005). In general terms, the control of invasive species is intended to reverse the associated impact by recovering the structure and composition of natural communities, as well as reducing the area covered and preventing their expansion (Zalba & Ziller 2007). The effectiveness of this process will depend on the density, extension, and time lapsed since the species invaded the area. The persistence of a seed bank of native species that would be adequate for the restoration of native communities once the invaders have been eliminated would be most affected by greater areas, denser populations, and longer times of invasion. Sometimes the removal of invasive trees is sufficient for recuperating the structure and composition of natural communities, whereas in other cases, control of invasive species has to be complemented with other management interventions such as the enrichment or stimulation of seed banks of native species (Bakker et al. 1996; Holmes & Cowling 1997; Bakker & Berendse 1999; Holmes et al. 2000; Warren et al. 2002). So monitoring of the vegetation during the years after removal of invasive trees is critical in order to decide whether an active restoration strategy is necessary or whether complementary

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actions should be implemented for the control of other invasive species that might colonize the cleared areas. In the particular case of the Southern Cone grasslands of South America, where the vegetation evolved in the absence of native trees (Parodi 1942; Facelli & Leoń 1986), it is expected that dense stands of invasive woody species would result in a significant reduction in the quantity of seeds of native species, which would condition the local survival of seed-regenerating species and the global regenerative capacity of the ecosystem, as occurs in the South African fynbos (Holmes & Cowling 1997); however, recuperation of these ecosystems after the removal of alien woody plants has not been studied previously. In this article, we evaluate vegetation succession four years after removing dense stands of Aleppo pine (Pinus halepensis) in an area of montane grasslands in central Argentina. Evidence is gathered to evaluate if vegetation changes associated to the presence of pines are due to light interference or to more persistent alterations like changes in soil properties, to test if seed banks allow the regeneration of native grasslands after 12 years of pines invasion, to determine the importance of seed input from the vicinity of the cleared areas, and to evaluate the possible colonization by other non-native plants. We expect that time elapsed since the invasion, and the concomitant increase in pines density and basal area would reduce the regeneration capacity of the community and that this effect could be at least partly counteracted by seed input from patches of natural grassland in the vicinity of cleared areas. We finally give practical advice on management actions that can help the restoration process.

southwest slopes of the main chain of mountains in the reserve. The maximum age of the trees in the sector was 12 years at the time of felling, and the density oscillated between 2,100 and 3,200 trees/ha (Zalba et al. 2007). Experimental Control of Pines

In June 1999, as part of an adaptive management strategy of invasive pines, 17 circular clearings of 10 m in diameter were opened with no further manipulation. Cleared areas were established every 20 m at two altitudes: 550 (n ¼ 9) and 700 m (n ¼ 8). Plots at the lower altitude were completely surrounded by dense pinewood, whereas at the higher altitude, they were placed on the highest edge of the pinewood, adjacent to natural grassland above (Fig. 1). All mature pines in each plot were felled with a chainsaw at 10 cm above ground level, and the younger ones were cut with a machete or pulled up by hand. Diameters of tree trunks exceeding 3 cm were recorded and so was the height of the smaller trees. All cut pines were removed from the cleared areas. The density and basal area were estimated from the data of felled pines at both altitudes (Sutherland 1996). Monitoring of Vegetation in Cleared Areas

A study of the succession of vegetation was initiated immediately after removing the pines. A 5 3 5–m plot

Methods Study Area

This study was carried out in Ernesto Tornquist Provincial Park (lat 38°S, long 61°W), one of the few reserves designed to conserve the last relicts of natural grassland in Argentina (Bertonatti & Corcuera 2000; Bilenca & Minãrro 2004). It is located at a mountainous area, up to 1,200 m. It has a temperate climate, with an average temperature of 14.6°C (Frangi & Bottino 1995) and precipitations averaging 990 mm annual during the past 15 years, with more rain falling from October to March (unpublished data). The dominant vegetation is grassland, dominated by Stipa, Piptochaetium, Festuca, and Briza (Cabrera 1976). The invasion by exotic woody species is so great in this reserve that its value as a conservation area is seriously conditioned (Zalba 1995; Fiori et al. 1997; Zalba 2001). Aleppo pine (Pinus halepensis) is one of the most invasive trees; it has expanded exponentially and is high priority for control in the area. A plan for mechanical control of exotic woody species was carried out in the park in 1999 together with a research project to optimize management interventions (Zalba et al. 2000, 2003). This work was undertaken in a spontaneous wood of P. halepensis on the

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Figure 1. Study area (scale 1:5,000): Pinus halepensis wood on the southwest slope of the principal mountain chain in Sierra de la Ventana (Buenos Aires, Argentina). The cleared areas are shown by dotted arrows at 700 m and continuous arrows at 550 m.

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was placed in the center of each of the 17 cleared areas. Plant species cover was estimated for each plot according to a modified Braun-Blanquet scale (Mueller-Dombois & Ellenberg 1974). Recorded plants were identified to species level following the nomenclature of Zuloaga and Morrone (1996, 1999), except in the case of the grasses, which were grouped together due to difficulties of identifying them at some of the sampling dates. Control plots measuring 5 3 5 m were placed in native grassland from nearby sectors not affected by pine invasion, seven at 550 m and six at 700 m, and the same variables were measured as in the cleared areas. Sampling was repeated every spring and summer from 1999 to September 2003 when a natural fire burned the study area. The percent cover of grasses, nongrass species richness and diversity (Shannon–Weiner), and the percent cover of exotic species were calculated from data of each vegetation census for the cleared plots and for the control areas at both altitudes. Statistical Analysis

The relationship between density and basal area of the pines with grass cover, nongrass species richness and diversity, and the percent cover of exotic species was evaluated by means of regression analysis at the time of felling in the cleared plots at both altitudes. Likewise, t tests were carried out in order to compare the six variables mentioned between both altitudes. The normality and homoscedasticity of the data were verified using Barlett’s test, and the most appropriate transformation was applied in cases where it was necessary. Changes in percent cover of grasses, nongrass species richness and diversity, and percent cover of exotic species over time were compared using t tests. These analyses were used to evaluate differences in these variables between plots at the higher altitude and their controls, between plots at the lower altitude and their controls, and between cleared plots and natural grassland at both altitudes for each sampling date. Appropriate transformations that complied with the requisites of normality and homoscedasticity were applied. Differences in species composition between the cleared areas and the controls at the start and end of the sampling

period were analyzed by a principal components analysis (PCA) using the matrices of covariance of the percent cover of species transformed to the arcsin of the square root (Gauch 1982; Dytham 1999).

Results Effects of the Presence of Pines on Grassland Vegetation

The plots at the higher altitude showed a mean density of 2,700 pines/ha (SE ¼ 700) and a basal area of 35.73 m2/ha (SE ¼ 5.5) at the time of felling, which was significantly lower than the values found for the plots at the lower altitude, with a density of 10,600 pines/ha (SE ¼ 3,400) and a basal area of 51.6 m2/ha (SE ¼ 4.04) (t ¼ 23.05, p ¼ 0.008; t ¼ 22.36, p ¼ 0.032, respectively). No significant differences were found in the percent cover of grasses, number and diversity of nongrass species, and percent cover of exotic species between both altitudes at the time of felling. However, a lower percent cover of grasses, nongrass species richness and diversity was evident in the cleared areas at both altitudes compared with their respective grassland controls. On the other hand, there were no significant differences between the cleared areas and their respective controls in respect of the percent cover of exotic species, neither in terms of the alien species that were present, mostly represented by three forbs: Cerastium arvense, Carduus pycnocephalus, and Crepis capillaris (Table 1). Cleared areas at the higher altitude showed a slight significant negative response in the percent cover of grasses at growing pines densities (F ¼ 6.85, r2 ¼ 0.533, p ¼ 0.04, n ¼ 8), but we did not find a significant relationship between both variables for plots at the lower altitude (p ¼ 0.23) and neither when both strata were plotted together (p ¼ 0.06). Changes in Cleared Areas During the Study

No significant differences were found in the percent cover of grasses between the control areas at the higher and lower altitude at any time during the study (p > 0.964). Cleared areas at both altitudes showed smaller mean values of grass cover than controls over the study

Grass Cover.

Table 1. Mean grass cover, nongrass species richness and diversity, and percentage of exotic species cover at time of felling in cleared areas at 550 and 700 m and their respective controls. Higher Altitude Cleared Areas

Controls

Lower Altitude Cleared Areas

Controls

Grass cover (%) 13.12 (2.1) 56.66 (3.33) t ¼ 210.42, p < 0.0001 10.55 (1.94) 58.75 (2.2) t ¼ 214.6, p < 0.0001 Nongrass species richness 8.75 (0.99) 13.3 (0.55) t ¼ 23.51, p < 0.0001 9.88 (1.66) 15 (0.56) t ¼ 22.84, p ¼ 0.01 Nongrass diversity (Shannon) 2.23 (0.22) 3.25 (0.2) t ¼ 23.25, p < 0.0001 2.29 (0.4) 3.35 (0.08) t ¼ 22.57, p ¼ 0.03 Exotic species cover (%) 1.87 (0.91) 3.33 (1.05) t ¼ 1.04, p ¼ 0.31 1.11 (0.73) 3.75 (1.25) t ¼ 1.83, p ¼ 0.08 Figures for SE in brackets.

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(p < 0.01). However, a gradual increase in the mean grass cover in cleared areas over time was observed at both altitudes. Recuperation of grass cover was more noticeable in plots at the higher altitude (Fig. 2). At the end of the study period, cleared areas at the higher altitude showed a significantly negative association between the percentage of grass cover and the basal area of pines at the time of felling (r ¼ 20.67, p ¼ 0.04), but this was not detected at the lower altitude. Nongrass Species Richness and Diversity. Nongrass spe-

cies richness in cleared areas showed an initial increase that exceeded the figures of grassland controls, but it later decreased to an average value similar to that found in areas of noninvaded grasslands. Controls at the higher and lower altitudes on the other hand did not show significant differences during the whole study period (p > 0.99). Equivalent values for nongrass species richness were observed for both altitudes when the felled areas were compared, except at the end of the survey when plots at the lower altitude showed significantly higher species richness (Fig. 3). Nongrass plant species diversity followed similar behavior to species richness. Grassland controls at both altitudes did not show any significant differences in this variable at any of the times of sampling (p > 0.727).

Figure 3. Mean nongrass species richness for cleared areas at high and low altitude and for their respective controls. The bars represent the SE. Continuous lines represent cleared areas and dotted lines the controls, black lines correspond to the higher altitude, and gray lines to the lower altitude. Changes in Floristic Composition

Exotic Species Cover. Percent cover of exotic species did not exhibit significant differences between grassland controls at the different altitudes throughout the study period. Exotic species cover in cleared areas showed an increase in the stages following the elimination of pines that was specially evident in the case of the lower stratum. At the end of the study, cleared areas at the higher altitude were statistically equivalent to grassland controls in respect of this variable, but the percentage of exotic species cover was still higher in the felled plots that were not in direct contact with grassland (p ¼ 0.04) (Fig. 4).

A total of 58 plant species were identified in the cleared plots and control areas of natural vegetation over the whole study period, as well as species of Poaceae that were counted together as one unit. To better interpret the results obtained is important to note that, according to previous work, the number of grass species in the sampling area is circa 15 species including genus like Piptochaetium, Stipa, Hordeum, and Briza (Zalba 1995). The PCA performed with data at the time of felling separated the cleared areas from the controls on the first component (33% of the variance) (Fig. 5). This discrimination was due mainly to the controls that showed higher values for the cover of grasses and Eupatorium buniifolium, Lucilia acutifolia, Hypochoeris chondrilloides, Grindelia buphthalmoides, and Baccharis rufescens, whereas the cleared areas showed higher values for Ipheion uniflorum, Solanum chenopodioides, Solidago chilensis, and Euphorbia portulacoides. The second component (13% of

Figure 2. Mean percentage of grass cover over time for cleared areas at the higher and lower altitudes and for their respective control areas not invaded by pines. The bars represent the SE. Continuous lines represent cleared areas and dotted lines controls, black lines correspond to the higher altitude, and gray lines to the lower altitude.

Figure 4. Mean percentage of exotic species cover for cleared areas at the higher and lower altitudes and for their respective control areas. The bars represent SE. Continuous lines represent cleared areas and dotted lines the controls, black lines correspond to the higher altitude, and gray lines to the lower.

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Figure 5. Vegetation samples in the principal component space as defined by the matrix of covariance of cover data for plant species present in the cleared areas at the higher altitude (s) and their grassland controls (h), at lower altitudes (d) and their controls (n) at the time of felling the pines.

variance) separated the plots in function of their altitude. The cleared areas and grassland controls at 700 m showed higher values of cover of Discaria americana, I. uniflorum, Conyza bonariensis, and E. buniifolium, whereas the cleared areas and controls at 550 m showed higher values of cover of B. articulata, Eryngium stenophyllum, C. arvense, and Achyrochline satureioides. Fifty-one months after felling and clearing of pines, the PCA separated cleared areas at the lower altitude from the rest of the plots (cleared areas at the higher altitude and both control areas) on the first principal component that represents 33% of variance (Fig. 6). This discrimination was largely because the controls and the areas at the higher altitude showed higher values of cover of grasses, L. acutifolia, E. stenophyllum, C. arvense, and Adiantum raddianum, whereas the plots at the lower altitude showed higher values for Dichondra sericea, Plantago berroi, D. americana, and Pinus halepensis. The second principal component separated cleared areas at the higher altitude from those at the lower altitude (11% variance). This discrimination was largely because the former showed higher values of cover of E. stenophyllum, Anemone decapetala, C. bonariensis, Geranium sp., and L. acutifolia and the latter of S. chilensis, A. raddianum, E. paniculatum, E. buniifolium, Echium plantagineum, and D. americana (Fig. 6). Discussion Our results emphasize the capacity for spontaneous recovery of the grassland in early stages of invasion, which reinforces the need for an early control of the problem.

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Figure 6. Vegetation samples in the principal component space as defined by the matrix of covariance of cover data of plants species present in cleared areas at the higher altitude (s) and their grassland controls (h), in cleared areas at the lower altitude (d) and their controls (n) at the end of the study period.

Likewise, variation is seen in the levels of recovery in function of the proximity of sectors of grassland that are free of invasive species and/or the density of invasive trees before control. Effects of the Presence of Pines on Grassland Vegetation

The Pampas region was naturally free of trees (Parodi 1942; Facelli & Leoń 1986) that were introduced with the advance of European colonization but only becoming frequent toward the beginning of the 20th century (Zalba & Villamil 2002). Exotic trees significantly change the structure and composition of grassland plant communities (Zalba & Villamil 2002) and the associated wildlife (Zalba 2001). In this study, the effect of the presence of invasive pines on the vegetation is seen in the characteristics of the plots at the time of felling, with a significant reduction in grass cover and lower values of nongrass species richness and diversity in comparison with the natural grassland controls. These changes might be a response to the interference of sunlight by invasive species and/or to modifications in the physicochemical or biological soil conditions. Sunlight interference has been frequently reported as the main cause of changes in plant communities associated to the invasion of alien plants (Woods 1993; Gould & Gorchov 2000). Changes in pH, nitrogen cycling, litter dynamics, and soil microbiology are also cited as proximate causes for alterations in vegetation related to the spread of invasive plants (Mitchell et al. 1999; Ehrenfeld et al. 2001; Callaway & Ridenour 2004; Heneghan et al. 2006; Stinson et al. 2006). In our study, the rapid recovery

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of vegetation after pines felling appears to indicate that changes were probably due to shade, which would be neutralized on removal of the trees, more than to other alterations of a more intense or permanent nature. It is known that older pines produce significant changes to soil characteristics in the region, including a decrease in pH, base saturation, exchangeable Ca21, Mg21, and K1 and increase in Na1, Al31, and particularly H1 that eventually become irreversible (Amiotti et al. 2000, 2007) and so, if present over a longer time in the area, the ecological alterations that control the recuperation capacity of grassland may become disrupted. An interesting result of this study is the fact that no significant differences were recorded in the percent cover of exotic species in pinewoods in comparison with grassland controls. Zalba and Villamil (2002), who worked in woods near to our study area, did detect significant increases in the abundance of exotic plants in the woods that exceeded in more than 20% the number of native species in the case of a mature wood of Pinus halepensis. This contrast might be due to several factors, including the fact that we did not include grass species in our richness and diversity estimates. There is a great chance for grasses to be more diverse in natural openings than under exotic trees and so we could be underestimating both variables at control plots. Another difference is that the wood studied by Zalba and Villamil (2002) was a mature stand, planted 40 years earlier, whereas the wood in our study was much younger. It is possible that in the case of the mature wood, there were more profound changes in soil characteristics, as discussed in the previous paragraph, which would favor opportunist exotic species rather than native grassland plants. Changes in Cleared Areas During the Study

When considering the recovery process of vegetation after felling, it is important to note that clearing pines from the plots represents a sudden change in the insolation and water dynamics of the soil. Once the trees are removed, the vegetation of the cleared plots in our study area responded rapidly, showing increases in nongrass species richness and diversity that were higher than in the controls unaffected by the invasion. Part of this change is due to a temporary increase in the richness of exotic species, especially in the case of the areas surrounded by closed woods; however, the percent cover of exotic species became significantly reduced over the study period. The situation was different in the case of the percent cover of grasses that remained lower in cleared areas than in the controls four years after felling, even though more than 100% increase was seen in some cases. The changes observed in nongrass species richness and diversity after felling the pines are consistent with the hypothesis of intermediate disturbance, specifically with the prediction proposing that species richness will be highest at intermediate time spans during postdisturbance

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(Connell 1978). In this case, removal of tree cover exposes the soil to direct light, opening a colonization window for pioneer species, and with time, this space is shared by plants of higher competitive ability that latter become dominant. Changes in Floristic Composition

Plants present in the cleared plots immediately after removing the pines included opportunist exotic species such as Medicago lupulina or species native to the area but frequently cited as weeds in Argentina and/or other regions, e.g., Ipheion uniflorum, Solanum chenopodioides, Solidago chilensis, and Euphorbia portulacoides (Randall 2002). Whereas at the same time, control areas contained a significant number of species adapted to direct insolation, such as Lucilia acutifolia and Grindelia buphthalmoides. Samples corresponding to the intermediate periods in this study (19–33 months after felling) include both pioneer species and plants found in the more advanced stages of succession. It is very noticeable that recruitment of pines in the cleared plots was very low in spite of an expectable high propagule pressure from the surroundings and environmental conditions that appear to be appropriate for the species (direct sunlight and sparse vegetation cover) (Ne’eman et al. 1992; Thanos et al. 1996; Ne’eman & Izhaki 1998; Thanos & Daskalakou 2000; Tsitsoni & Karagiannakidou 2000). It is highly likely that the percentage of germination and establishment would be the cause of the low abundance of pines in the cleared plots. Pinus halepensis is a serotinous pine, adapted to establish when there is reduced competition in the regeneration niche, after fire (Trabaud et al. 1985; Richardson 1988; Ne’eman et al. 1992; Thanos et al. 1996; Higgins & Richardson 1998; Richardson & Higgins 1998, Rouget et al. 2001). In our work, clearing was carried out in winter while recruitment of pine seedlings occurs in autumn in this area (Cuevas 2005). In this way, the recovery of native vegetation may have significantly interfered with pines germination and establishment during the following seed release that occurred almost a year after felling. A key issue in restoration plans is whether native species would have the capacity to spontaneously recolonize the site, what in turn depends on recruitment from the soil seed bank, growth of persistent species that have survived underneath the pines, and arrival of seeds from the surroundings. Studies on grassland communities have shown that seed bank may be very important, especially in the first stages of succession that follow restoration actions (Pa¨rtel et al. 1998; Holmes et al. 2000; Mayer et al. 2004; Go¨tmark et al. 2005). An important number of grassland species form persistent seed banks that remain as a vestige of the previous vegetation even when grassland is replaced by shrubs or woods (Davies & Waite 1998), and the presence of these kind of long-term seed banks has been recorded for other mountain grasslands of central

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Argentina (Funes et al. 2001). Considering that pine felling in our study took place in June and that the period of seed liberation in these grasslands occurs from October to March (A. Long 2007, Botany Department, Universidad Nacional del Sur, personal communication), the contribution of seeds from outside the plots before the first sampling can be discarded, and the plants recorded in all plots immediately after felling were those that survived the presence of pines or germinated from a preexistent seed bank under the pines. It is expected for seed immigration to become more important at the following stages in the succession of felled areas, with sites next to natural grassland (in our case, the plots at the higher altitude) receiving a larger quantity of seeds. In accordance with this, the PCA carried out at the beginning and at the end of the sampling period showed a significant convergence of the vegetation toward states similar to the original in the case of the plots at the higher altitude, whereas cleared plots lower down in the middle of the dense wood were still separated from the corresponding controls even 51 months after felling. Plots at the higher altitude had a more significant and faster recovery in respect of most variables under study; however, these results must be looked at carefully because, apart from differences in their distance from seed sources, both strata were also different in the density, basal area, and mean age, of the pines, and eventually also in the original composition of native plant communities. Supporting the hypothesis of variations due to different seeds inputs from the surrounding areas is the fact that no significant differences were found in the percentage of grass cover, species richness and diversity, and percentage of exotic species between both altitudes at the time of felling. When projecting the restoration process, attention has to be paid to the proliferation of invasive alien plants that might benefit from the presence of invasive woods: it has been shown that pinewoods provide an appropriate habitat for opportunistic birds that may have advanced due to the expansion of exotic trees (Zalba 2001), some of these species are frugivore generalists that aid the dispersal of invasive exotic species like Prunus mahaleb and Rubus ulmifolius, whose seedlings were common in the cleared areas. Both species are known as aggressive invaders and their presence could lead to shrub-dominated states if not controlled (Montaldo 2000; Swearingen 2008).

Implications for Practice All the conclusions originated from our results have to be taken with care considering the lack of true replicates and the short time elapsed since the removal of pines. Nevertheless, these first stages of vegetation succession after pine removal give valuable insights that could help in deciding the eventual need of complementary restoration actions:

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d

d

d

The regeneration of grassland communities following the removal of conifer trees in the study site is unlikely to be seed limited if tree removal occurs early in the invasion process and there does not seem to be any need for an artificial input of diaspores. But, if pine removal occurs later, more intense changes in soil properties are expected, severely conditioning the recovery of natural communities. Proximity from patches of natural vegetation speeds up the restoration. Considering this feature, the progressive opening of clearings inside stands of invasive species may provide sites with conditions favorable for the regeneration of native vegetation that would act as seed sources in later stages of the restoration process. Finally, complementary restoration measures could be necessary to counteract colonization by perennial alien plants, like bird dispersed exotic shrubs. Major sources of seed spread in the vicinity of clearance areas should be identified and removed.

Acknowledgments This work was funded by Consejo Nacional de Investigaciones Cientı´ficas y Tećnicas and Universidad Nacional del Sur, Argentina. We are grateful to R. Scoffield, who helped us with the language.

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