Environ Sci Pollut Res (2016) 23:13606–13616 DOI 10.1007/s11356-015-5681-2

HOW CAN WE RESTORE THE BIODIVERSITY AND ECOSYSTEM SERVICES IN MINING AND INDUSTRIAL SITES?

Natural forest expansion on reclaimed coal mines in Northern Spain: the role of native shrubs as suitable microsites Josu G. Alday 1,2 & Pilar Zaldívar 3 & Paloma Torroba-Balmori 4,5 & Belén Fernández-Santos 6 & Carolina Martínez-Ruiz 3,5

Received: 9 April 2015 / Accepted: 22 October 2015 / Published online: 31 October 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract The characterization of suitable microsites for tree seedling establishment and growth is one of the most important tasks to achieve the restoration of native forest using natural processes in disturbed sites. For that, we assessed the natural Quercus petraea forest expansion in a 20-year-old reclaimed open-cast mine under sub-Mediterranean climate in northern Spain, monitoring seedling survival, growth, and recruitment during 5 years in three contrasting environments (undisturbed forest, mine edge, and mine center). Seedling density and proportion of dead branches decreased greatly from undisturbed forest towards the center of the mine. There was a positive effect of shrubs on Q. petraea seedling establishment in both mine environments, which increase as the environment undergoes more stress (from the mine edge to the center of the mine), and it was produced by different shrub structural features in each mine environment. Seedling survival reduction through time in three environments did not lead to a density Responsible editor: Hailong Wang * Carolina Martínez-Ruiz [email protected] 1

School of Environmental Sciences, University of Liverpool, Liverpool L69 3GP, UK

2

Department of Crop and Forest Sciences—AGROTECNIO Center, Universitat de Lleida, 25198 Lleida, Spain

3

Agroforestry Sciences Department, University of Valladolid, Campus La Yutera, Avda. de Madrid 44, 34071 Palencia, Spain

4

CIFOR-INIA (Center of Forest Research), Carretera de La Coruña km 7.5, 28040 Madrid, Spain

5

Sustainable Forest Management Research Institute UVa-INIA, Campus la Yutera, Avda de Madrid 44, 34071 Palencia, Spain

6

Ecology Area, University of Salamanca, Campus Miguel de Unamuno 37071, Salamanca, Spain

reduction because there was a yearly recruitment of new seedlings. Seedling survival, annual growth, and height through time were greater in mine sites than in the undisturbed forest. The successful colonization patterns and positive neighbor effect of shrubs on natural seedlings establishment found in this study during the first years support the use of shrubs as ecosystem engineers to increase heterogeneity in microenvironmental conditions on reclaimed mine sites, which improves late-successional Quercus species establishment. Keywords Quercus petraea . Seedling recruitment . Survival . Growth . Shrub protection . Sub-Mediterranean environment

Introduction Forest restoration in disturbed sites, such as old fields, landfills, and open-cast mines, is one of the most important challenges facing restoration ecology nowadays (Onaindia et al. 2013; Prach et al. 2014; Stanturf et al. 2014), and its interest is rising due to the increase in forest land degradation worldwide (Kissinger et al. 2012). Moreover, forest restoration improves the provision of multiple ecosystem services, including carbon storage, water flow regulation, and habitat for plants and animals (MEA Millennium Ecosystem Assessment 2005). The recovery of native tree species in these degraded areas is a hard task (Frouz et al. 2015), mainly due to the environmental hardness of disturbed ecosystems (Brooker et al. 2008), which can be even harder if coupled with summer drought. In the search for an effective re-establishment of forest, the focus has turned towards the identification of suitable microsites and mechanisms that facilitate the natural tree seedling establishment and growth, emphasizing the potential of natural

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processes to achieve the restoration of native forest (Onaindia et al. 2013; Prach et al. 2014). Open-cast coal mining is an extended activity in Northern Spain (Alday et al. 2011a) and particularly in the north of the Palencia region, where Quercus petraea at its southernmost distribution limit (do Amaral 1990) is one of the major forest species. There has been a substantial progress in post-mining restoration practices over the last 20 years, especially focusing on plant community assemblages and soil development (Alday et al. 2011a, b, 2012). However, the recovery of latesuccessional broadleaf species present before the mining operations, such as Q. petraea, has received less attention. Recent experiments carried out in the area to identify the best protocols to re-establish native Quercus species suggest that planting seedlings and seeding acorns under native colonizer shrubs produce better results than in open areas (TorrobaBalmori et al. 2015). Nevertheless, one particularity of these reclaimed mines is that they are surrounded by well-managed Quercus forest, acting as ample source of acorns capable of establishing in these mines. Thus, it would be interesting to use restoration procedures based on natural processes, such as natural tree colonization, to enhance the late-successional broadleaf species establishment in these mines (Walker et al. 2014). In this sense, man-induced establishment of seedlings and acorns would be expected to be more appropriate on mine sites isolated from seed sources, whereas mines surrounded by seed sources may rely on the natural colonization by trees (Prach and Pyšek 2001). In any case, the first main challenge is to characterize the microsites that facilitate or impede the native forest expansion in mined lands. The natural establishment of Quercus acorns on Mediterranean mine sites is a complex process limited by ecological filters like (1) migration barrier produced by seed dispersal mechanisms (i.e., barochory and zoochory; Gómez et al. 2003, 2008), (2) summer drought being increased in reclaimed mined sites by a lack of soil structure such as in forest systems (Alday et al. 2012), and (3) herbivory which can occur through trampling and browsing by livestock and wild ungulates (Torroba-Balmori et al. 2015). Recent works on forest species regeneration in Mediterranean ecosystems have demonstrated that facilitation mediated by shrubs can help to reduce the impact of these filters on tree species establishment and growth (Gómez-Aparicio et al. 2004; Castro et al. 2006). However, the assumption that naturally colonizing shrubs in mined sites generate suitable microsites facilitating the natural establishment and growth of Q. petraea has seldom been tested (but see Torroba-Balmori et al. 2015), and especially considering a clear microclimatic, seed reduction and water stress gradient from the undisturbed native forest towards the open mine area (Milder et al. 2013). Therefore, further efforts are needed to characterize what microsites facilitate the natural expansion of Q. petraea in places far from optimal, providing clues on how to improve the natural and

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man-induced establishment of Quercus species in more extreme environments. In the present study, we assessed the natural Q. petraea forest expansion in a reclaimed open-cast mine in northern Spain. The aim of the study was to characterize the mine microsites where natural colonization of Q. petraea takes place. In addition, we aimed to quantify Q. petraea seedling survival and growth during the first 5 years. For that, we compared seedling establishment on three contrasting environments: (1) the undisturbed native Q. petraea forest acting as control, (2) the mining area in contact with the forest edge with a canopy influence and notable seed supply, and (3) the mining area further away from the forest edge, i.e., a water stress site far from seed source. It is assumed that sessile oak is a competitive species in areas where water and light resources are abundant (Rodríguez-Calcerrada et al. 2008). However, it must be considered that in these mined sites, the summer drought effects are increased by the lack of developed soil, which reduces water holding capacity and consequently restricts the development of Quercus species (Torroba-Balmori et al. 2015). Therefore, the description of suitable microsites for Q. petraea seedlings might help to design improved and more effective tree restoration strategies in sub-Mediterranean mine sites. Here, our hypotheses were (1) seedling establishment would be influenced by the three environments considered, being lower in the more stressed environments far away from seed sources (i.e., mined sites); (2) the location of Q. petraea seedlings in mine environments would be positively related to the shrubs’ presence (possibly nurse effect); (3) the positive effect of shrubs on Q. petraea seedling establishment would increase as the environment undergoes greater water stress (i.e., the stress gradient hypothesis; Bertness and Callaway 1994), and here it happens towards the center of the mine area; and (4) Q. petraea seedling survival, recruitment, and annual growth through the first 5 years would be lower in mined sites than in undisturbed forest, although shrubs and soil moisture would have a positive effect on seedlings. It is expected that this approach would lead to improve the current restoration methods using novel approaches based on the ecosystem concepts like microsites to accelerate the natural and man-induced tree seedling establishment process in similar reclaimed areas.

Materials and methods Site description and mine restoration treatment The study site was located in a 5-ha reclaimed open-cast coal mine near Guardo, Palencia, Northern Spain (lat 42° 47′ N, long 4° 50′ W, ca. 1110 m a.s.l.). The climate is sub-humid Mediterranean (Torroba-Balmori et al. 2015), with annual mean temperature of 9.3 °C and average annual precipitation of 977 mm (1971–2007 temperature means and 1932–2007

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precipitation means from Guardo meteorological station). Rainfall is not distributed regularly throughout the year, with a pronounced dry season in summer (July and August). The vegetation surrounding the mine consisted of broad-leaved woodlands dominated by Q. petraea and some shrubs such as Cytisus scoparius and Genista florida (Milder et al. 2013). The open-cast mine was reclaimed in 1990, using a combination of topsoil addition with a very poor seed bank (GonzálezAlday et al. 2009), amended with cattle manure and followed by hydroseeding with a grassland species mixture (for further reclamation details, see Milder et al. 2013). The reclaimed area had a patchy natural colonization of shrubs, mainly C. scoparius and G. florida, being grazed freely by animals (deer, cattle, and horses), and the land slope from the surrounding forest to the reclaimed mine varied around 18–30°. The current soil texture is described as clay loam with a pH of 6.5 and with an effective depth of 10–15 cm (López-Marcos 2012).

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and shrubs, and the prevailing environment (García et al. 2000). At each sampling plot (n=60), the seedling density, stem height (cm) and diameter at root collar (mm), and number of total and dead branches of each individual were measured; dead branches proportion was used here as a proxy of initial growing space (Kuehne et al. 2013). At the same time, information on a range of variables related with the microhabitat surrounding each individual were also collected. These were bryophyte cover (%), which was used as a surrogate measure of soil moisture availability (Hettenbergerová et al. 2013; Alday et al. 2014); shrub cover (%); angle of contact (°) between seedling and the surrounding shrubs based on García et al. (2000), as a proxy of light interception; shrubs lateral protection which is the percentage of intersections between woody vegetation and soil surface in four 1-m transects in the cardinal axis centered on the seedling and with sampling points at 0.25, 0.5, 0.75, and 1 m from the oak (for further details, see García et al. 2000); and shrub species (i.e., G. florida or C. scoparius) and shrub height (cm).

Sampling design and data collection Permanent plot study Forest expansion study and microsite characterization Previous works in the study area have demonstrated that there is a clear microclimatic and water stress gradient, combined with a reduction of seed input from undisturbed surrounding native forest towards the center of the reclaimed mined sites (Milder et al. 2013). This gradient might have a clear influence on the establishment of Quercus seedlings. As a consequence, the experimental setup in the mine area consisted of the selection of three different sites (i.e., environments) along this gradient: (1) the undisturbed native Q. petraea forest (Fo), being a band 12 m wide in contact with the reclaimed mine site, acting as acorn supplier to mining area and providing a reference of the optimal oak regeneration in natural conditions. (2) The mining area close to the forest edge or mine edge (M1), being a band that covers approximately the first 6 m from the forest edge towards the mine site, and it is characterized by a great canopy influence (lateral shading and litter-fall) and a notable acorn supply by gravity, as well as a great shrub cover (75 %), which can influence the oak regeneration. (3) The mining area without forest contact (M2) is a band 8 m wide from the edge of the M1 towards the mining surface, and it is characterized by a lack of forest influence but high shrub cover (65 %) which may influence the oak regeneration. However, the acorn arrival is a limiting factor in M2 because it is only directly related with barochory (wind blows and slope; Gómez et al. 2003) and zoochory (e.g., Garrulus glandarius, Apodemus sylvaticus; Gómez et al. 2003; Den Ouden et al. 2005). Oak seedling abundance (individuals below 3 years old determined by having still attached cotyledons) and their characteristics were sampled in autumn of 2010. At each site (Fo, M1, M2), 20 sampling plots of 4 m2 (2×2 m) were located randomly to provide a statistically rigorous sample of both seedlings

For seedling survival, growth, and recruitment monitoring, 9 of the 20 sampling plots (4 m2) previously selected in each mine environment (M1 and M2, n=9) and 4 of the 20 sampling plots previously established in the undisturbed forest environment (Fo, n=4) were randomly marked as permanent plots in 2010, and each oak seedling in them was permanently marked. These permanent plots were revisited in autumn every year until 2014 (i.e., 5 years of monitoring) tagging new seedlings and measuring new and old ones. The lower number of permanent plots established in the forest responded to the higher homogeneity of this environment and its higher seedling density. Seedling growth was measured in two ways: (1) as the increase in seedling height (cm) through time and (2) as the annual increment of shoot growth that is composed up to four to five growth flushes in Q. petraea if growing in favorable conditions (see Collet et al. 1997). Recruitment referred to the number of new seedlings colonizing each plot. Data analysis All statistical analyses were implemented in the R software environment (version 2.15.3; R Development Core Team 2013). Seedling density and growth analyses (i.e., height, diameter, and dead branches proportion) between the three environments were carried out with nlme package for Linear Mixed Models (LMM, Pinheiro et al. 2013). Structural Equation Models were calculated using the lavaan package (SEMs, Rosseel 2012), while seedling survival, recruitment, and growth through time were analyzed using lme4 package for Generalized Linear Mixed Models (GLMM, Bates et al. 2013). First, the differences in seedling densities (individuals/m2) between the three different environments (Fo, M1, M2) were

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analyzed using GLMs with a Poisson error distribution. At the same time, LMMs with normal distribution were used to analyze the effect of the three different environments in seedling growth variables (i.e., seedling height, diameter, and dead branches proportion). In these models, individuals nested with plots were included as random effects accounting for spatial pseudo-replication (Pinheiro and Bates 2000). The dead branches proportion data (%) was arcsine-transformed (sin−1 √(x/100)) (Crawley 2007). Second, we used Structural Equation Models (SEMs) to explore to what extent the location of Quercus seedlings in mine environments (M1, M2) was related to the shrubs’ presence (i.e., acting as nurse plants) and soil moisture. The SEM approach is based on a general linear model and enables the simultaneous assessment of multiple relationships (direct and indirect) between variables (Grace 2006). These relationships between variables can be represented in a Bpath^ diagram where the variables are connected by arrows representing the theoretical structural model for the system under consideration (Rosseel 2012). We developed an a priori conceptual model describing the Quercus seedling establishment related with shrubs and soil moisture multiple pathways (Fig. 1). Here, we hypothesized that Quercus seedling establishment occurred as a result of positive effects of shrubs improving environmental conditions and acting as nurse plants (Alday et al. 2014). In this model, the direct effect of shrub lateral protection, shrub angle of contact, shrub height, and shrub species combined with soil moisture on seedlings were tested (Fig. 1). At the same time, shrub height and species (i.e., Cytisus or Genista) are hypothesized to be directly related with soil moisture since it improves the growth and establishment of these species (Torroba-Balmori et al. 2015). Finally, shrub height could also lead to an increase of shrub angle of contact (light interception) and lateral protection. Separate SEMs were fitted to each mine environment (M1 and M2) to test if the effects of shrub on seedling establishment differed between two environments. SEMs model simplification method was based on

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Akaike Information Criterion (AIC) deleting all the nonsignificant model’s path coefficients. The goodness of fit of each model was evaluated with the chi-square statistic, the root mean square error of approximation (RMSEA), and the goodness-of-fit index (GFI). Chi-square values higher than 0.05, RMSEA below 0.08, and a GFI above 0.90 indicate an acceptable fit for the model (Grace 2006). For clarity, only the standardized path coefficients are reported in the figures. Third, the role that environment (Fo, M1, and M2) and time played in seedling survival was analyzed using GLMMs, whereas their effects in seedling annual growth and height were tested using LMMs. At the same time, considering only the mined sites (M1, M2), the effect of shrubs (presence/absence) and soil moisture (presence/absence of bryophytes) on survival and growth (seedling annual growth and height) through time was also analyzed. In model construction, we started with the full model including the interaction between environments and time as fixed effects, plus a four-level interaction with shrubs and soil moisture for mine site models. Here, individuals nested with plots were included as random effects. The survival data showed a binary response (live or not); hence, a binomial error distribution with a logit-link function was used, while annual growth and height were tested using a normal distribution. In these two models, the homoscedasticity was corrected using the varIdent function and defining different variances for each environment and time (Pinheiro and Bates 2000). In addition, annual growth was square-root-transformed to accomplish normality assumptions. In the case of Quercus seedling density and recruitment, GLMs using the poisson and quasipoisson error distributions, respectively, were fitted to test the role of environment and time. In all analyses, model simplification guidelines followed Crawley (2007) using the Akaike information criterion (AIC, Pinheiro and Bates 2000). Starting from the full model, the minimal adequate GLMM, LMM, and GLM were obtained by sequential removal of non-significant model terms until no further reduction in AIC was observed.

Results Differences in seedling density and growth parameters between environments

Fig. 1 Conceptual model of Quercus seedling establishment relating different shrub and soil microsite variables and their hypothesized relationships in reclaimed open-cast coal mines in Spain. The model is drawn to demonstrate relationships that may arise in reclaimed mines if shrubs influence Quercus seedling establishment via nurse effect

The GLM showed that there were significant differences between the three environments in the number of established seedlings (Z=50.79, P<0.001; Fig. 2a). Undisturbed forest had the greatest density (16±3.78 ind/m2), being five times greater than M1 density (3±0.44 ind/m2), while the density inside the mine (M2) is only 1±0.15 ind/m2. However, the LMMs showed that seedling height was only significantly greater in mine edge (M1=15.50±0.60 cm, F=4.42, P= 0.016; Fig. 2b), showing Fo and M2 similar seedling heights (Fo=11.21±0.14 cm, M2=12.17±0.90 cm). Seedling diameter

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0

c Fo

M1

20 5

M2

Fo

M2

60 a 40

b c

0

0

20

3 2 1

M1

Environments

Dead branches (%)

4

Environments

Seedlings diameter (mm)

a

a

10

15

b

0

b

Seedlings height (cm)

a

5

10 15 20 25

2

Number of seedlings (ind/m )

13610

Fo

M1

M2

Environments

Fo

M1

M2

Environments

Fig. 2 Differences in seedling density (ind/m2), stem height (cm), diameter (mm), and dead branches proportion (%) between the three environments selected. Fo undisturbed native Q. petraea forest (n=20), M1 the mining area in contact with the forest edge (n=20), M2 the mining area further away (n=20). Different letters above the bars indicate significant differences (P<0.05)

was not significantly different between the three environments, with an average value of 2.95±0.10 mm (F=1.76, P=0.181; Fig. 2c). On the other hand, dead branches proportion showed significant differences between three environments (F=15.98, P<0.001; Fig. 2d), with a decreasing trend from the forest edge towards the center of the mine (Fo=45.63±0.73 % vs. M1= 37.27±1.87 % vs. M2=24.30±3.91 %).

Shrub effects on seedling establishment in mined sites (M1, M2) Both structural equations models at M1 and M2 environments showed a reasonably good fit as the RMSEA were around 0.08 and GFI values greater than 0.98 (Fig. 3). The SEMs clearly show differences in the way in which Quercus seedling establishment is affected by shrub features and soil moisture. In the mine edge M1 (Fig. 3a), standardized path coefficients indicate that seedling establishment was mainly controlled by shrub height (0.50), followed by lateral protection (0.44) and slightly by soil moisture (0.12). In contrast, in the strictly mine environment M2 (Fig. 3b), the shrub height increased its effect over seedling establishment (0.50 in M1 vs. 0.68 in M2), although the other patterns observed were slightly different with a positive effect of shrub angle of contact (0.19) and negative of Cytisus species (−0.25). On the other hand, some shrub features are positively related in both environments such as shrub angle and shrub height (0.48 and 0.49, respectively)

Fig. 3 Conceptual model of Quercus seedling establishment at two mined sites (M1, M2) relating different shrub and soil microsite features and their hypothesized relationships in reclaimed open-cast coal mines in Spain. M1 the mining area in contact with the forest edge, M2 the mining area further away

or shrub height and Cytisus species (−0.65 and −0.54, respectively), indicating some shrub structural relationships. It is interesting to highlight the negative effect of soil moisture in the shrub height at M2 (−0.35; Fig. 3b). Seedling survival, recruitment, and growth through time The GLMMs of Quercus seedling survival showed three interesting patterns (Table 1). First, there was a negative time effect on survival independently of the environment considered, indicating a reduction of seedling survival per year (i.e., 11.77± 1.31 % per year). Second, there were differences on survival between environments, being the undisturbed forest the environment with lower survival in comparison with mined sites (Fo-survival2014 =0.48 % vs. M1-survival2014 =0.71 % and M2-survival2014 =0.68 %; Fig. 4a). Third, in mined sites (M1, M2), there were no significant effects of shrubs and soil moisture in Quercus survival through time (shrubs—Z=0.47, P= 0.643; soil moisture—Z=−0.25, P=0.980). However, the analysis of seedling density only reveals that density was constant through time in the three environments (Fig. 4b), but significantly different between them (Fo=12±2 ind/m2 vs. M1=4± 23 ind/m2 vs. M2=1±0.07 ind/m2; Z>6.50, P<0.001). The survival decrease through time did not lead to a density

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13611

P value

6.86

<0.001

5.06±0.85 4.39±1.19

5.97 3.70

<0.001 0.001

−2.47±0.27 (b) Seedling recruitment (ind/m2)

−9.27

<0.001

M1 M2 Time

0.8

M1 M2

0.6

Fo 0.4

0.2

0.0

1.39±0.37 −1.46±0.26

3.76 −5.73

<0.001 <0.001

M2 Time

−2.53±0.38 0.45±0.11

−6.59 4.03

<0.001 <0.001

2010

(c) Seedling annual growth (cm) Intercept_Fo M1

1.32±0.08 0.26±0.10

16.25 2.61

<0.001 0.021

M2

0.26±0.12

2.21

0.039

(d) Seedling height (cm) Intercept_Fo 10.00±2.50 M1 5.69±3.07

3.99 1.85

0.001 0.079

M2 Time

3.70±3.22 2.07±0.06

1.15 34.26

0.265 <0.001

M1×time M2×time

0.77±0.11 0.76±0.17

6.69 4.56

<0.001 <0.001

2011

2012

2013

2014

Years

b 2

Intercept_Fo M1

Environment

25

Fo 20

M1 M2

15 10 5 0

2 Fo 010 2 Fo 011 20 Fo 1 2 2 Fo 013 20 M 1 1 4 2 M 01 1 0 2 M 01 1 1 20 M 1 1 2 2 M 01 1 3 20 M 1 2 4 2 M 01 2 0 20 M 1 2 1 2 M 01 2 2 20 M 1 2 3 20 14

(a) Seedling survival probability Intercept_Fo 9.54±1.40

Value

Seedling density - Ind/m

Estimate±SE

1.0

Fo

Fixed effects

a Seedling survival probability

Table 1 Model parameters estimates derived from GLMM and GLM models for (a) Quercus seedling survival (Z values), (b) seedling recruitment (t values), (c) seedling annual growth (t values), and (d) seedling height (t values) (Fo—undisturbed forest as intercept)

Years

2

c 45

Environment

40

Fo

35

M1

30

M2

25 20 15 10 5 0

Fo

20 Fo 1 1 20 Fo 12 20 Fo 13 20 M 14 1 20 M 11 1 20 M 12 1 20 M 13 1 20 M 14 2 20 M 11 2 20 M 12 2 20 M 13 2 20 14

Seedling recruitment - Ind/m

reduction as a consequence of the significant recruitment of seedlings through time in the three environments (Table 1, Fig. 4c). Seedling recruitment was especially evident in 2013 and 2014 in the three sites, although the mean annual recruitment was always greater in the forest (Fo=14±3 ind/m2) than in mined sites (M1=3±1 ind/m2 vs. M2=1±0.27 ind/m2). The seedling annual growth only differed significantly between environments (Table 1). Seedling annual growth was significantly lower in Fo than in M1 and M2 mined sites, and no differences in growth were found between mined sites (Fo= 1.99 ± 0.07 cm vs. M1 = 2.87 ± 0.11 cm and M2 = 3.01 ± 0.20 cm). The seedling annual growth was constant in the three sites through time, and in mined sites (M1, M2) there were no significant effect of shrubs and soil moisture in seedling annual growth (shrubs—t=−0.55, P=0.585; soil moisture—t=1.21, P=0.230). In contrast, the LMM for Quercus seedling height showed an environment×time interaction (Table 1). Both mined sites (M1, M2) showed a significant seedling height increase with time, being always greater than the increase produced in the undisturbed forest (Fo, Fig. 5a). It is interesting to mention that considering only the mined sites, there was an environment×time×shrub interaction over seedling height (t=2.58, P=0.010; Fig. 5b). Although seedling height increased with time in both mined sites, in M1 the seedling height

Years

Fig. 4 Probability of Quercus seedling survival (a), seedling density (ind/m 2 ) (b), and seedling recruitment (ind/m 2 ) (c) in the three environments through time. The fitted line in (a) represents the minimal adequate GLMM. Fo undisturbed native Q. petraea forest, M1 the mining area in contact with the forest edge, M2 the mining area further away

was greater in microsites covered by shrubs (Fig. 5b), while the height increase through time is greater in microsites not protected by shrubs (slopes shrub—2.12±0.68 vs. no shrub—

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Seedling height (cm)

a

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30 25 20 15 Environment

10

Fo M1

5

M2 0 2010

2011

2012

2013

2014

Years

Seedling height (cm)

b

30

25

20 Env_Shrub

M1 N

15

M1 S 10

M2 N M2 S

5 2010

2011

2012

2013

2014

Years

Fig. 5 Changes in seedling height (cm) in the three environments through time (a), and the height changes in mined sites (M1, M2) related to environment×time×shrub interaction (b). The fitted lines represent the minimal adequate LMM with ±SE. M1 the mining area in contact with the forest edge, M2 the mining area further away. S and N following the mine site abbreviation refer to microsites covered or not by shrubs, respectively

4.20±0.70), reaching to similar seedling height values in 2014. Conversely, in M2, there was a significant positive relationship of seedling height with the presence of shrubs (Fig. 5b). It is interesting to mention that the lower height increase occurred in M2 with no shrub protection, where complete seedling mortality happened in 2014 (Fig. 5b).

Discussion Differences in seedling density and growth parameters between environments As expected, seedling density was influenced by the three environments considered, decreasing greatly from undisturbed forest (16±3.78 ind/m2) towards the center of the mine, where M2

showed the lowest values (1±0.15 ind/m2). These results were in accordance with Milder et al. (2013) who described that 94 % of the Quercus seedlings colonizing mine sites were found in the first 5 m from the forest edge, corresponding to our M1 area (3± 0.44 ind/m2). This seedling density reduction along the environmental gradient from forest to mine may be basically explained by its primary mechanism of dispersion (i.e., barochory) that determines a decrease in seedling density with distance from seed source (Müller et al. 2007), here the undisturbed forest (Fo). Beyond 6 m from the forest edge, seedling arrival is mainly due to a secondary dispersal mechanism like animals (i.e., zoochory), especially European jay and small rodents like wood mouse (Gómez et al. 2003, 2008; Den Ouden et al. 2005). In addition, most seedlings in M1 and especially in M2 (>85 %) are located under the influence of two shrubs C. scoparius and G. florida, suggesting that even if acorns overcome the dispersal barrier, they have to reach to suitable microsites under shrubs on the mine sites for an effective germination and growth (Gómez et al. 2008; Frouz et al. 2015). In any case, seedling density found in 2010 at the three environments was high and hence probably enough to ensure natural regeneration of Q. petraea in the undisturbed forest, although in mined areas regeneration would be limited by the colonization patchiness and the survival of colonizing seedlings. Seedling density of Q. petraea in the undisturbed forest is greatly above 12,000 seedlings per hectare recommended as minimum initial stocking to provide a total of at least 250 potential crop oaks of reasonable stem quality and acceptable crown form (Kuehne et al. 2013), or >7000–15,000 seedlings per hectare recommended in particular for Q. petraea (Burschel and Huss 2003). In contrast, seedling density in M1 and M2 mine sites decreased considerably, but it can be considered high for natural regeneration on disturbed mine site. The analysis of growth parameters between environments in 2010 reveals that there were no differences in seedling diameter mainly because during the first years (mainly the first one), seedling growth is related to seed mass rather than to abiotic factors like light (Pérez-Ramos et al. 2010). Nevertheless, there were differences in seedling height, being greater in M1 (ca. 4 cm higher) than in the other two environments (Fo and M2). It is well known that light increased the above-ground biomass of Quercus seedlings (GómezAparicio et al. 2004), enhancing seedling growth (PérezRamos et al. 2010); therefore, it would be expected that seedling height was greater in well-lit mined sites (M1, M2). However, M2 showed intermediate seedling height values between M1 and the undisturbed forest, which might be caused by the hard environmental conditions of M2 for acorn establishment during the first year in comparison with M1. In any case, further research will be needed to clarify the exact causes of seedling height differences between M1 and M2. Recent research on the importance of initial growing space for quality development of individual trees have shown that a

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higher stand density was related to a lower probability of branchiness and a higher proportion of dead branches in Quercus seedlings (Kuehne et al. 2013). In our study, the observed pattern of decreasing dead branches proportion as increasing seedling density from undisturbed forest towards the center of the mine is consistent with these findings. Probably, a higher seedling density increases the intraspecific competition (Kuehne et al. 2013) between Quercus seedlings for light, soil moisture, or nutrients, and contributes together with browsing, trampling, frost and disease damage, and root structure damage to a higher proportion of dead branches (Sprugel 2002). Shrub effects on seedling establishment in mined sites (M1, M2) We found mixed results concerning the way in which Quercus seedling establishment is affected by shrub features and soil moisture in the two mine environments. In both sites (M1 and M2), we have found evidence of positive relations between shrubs and Q. petraea seedlings; therefore, our hypothesis that the location of Q. petraea seedlings in mine environments is positively related with shrubs is accepted. As expected, naturally established seedlings were found in greater proportions under shrubs than in open areas (85 vs. 15 %), indicating positive neighbor effects of shrubs on Quercus seedlings (GómezAparicio 2009). It is well known that shrubs promote islands of fertility around them (Pajunen et al. 2012), modifying microenvironmental conditions (Gómez-Aparicio et al. 2005) and favoring the acorn establishment and growth (TorrobaBalmori et al. 2015). In particular, García-Ibáñez (2001) demonstrated that C. scoparius and G. florida have a positive effect on soil moisture and fertility. However, the shrubs’ positive effects are produced by different shrub structural features depending on the mine environment considered (M1 vs. M2). In M1 shrub height, lateral protection and soil moisture are positively related with seedlings, but no effect of shrub angle and shrub species was found (Fig. 3a). In forest-mine edge areas (M1), the forest canopy influence is still present, softening the hard environmental conditions of the mine environment (Milder et al. 2013), but there is an important acorn consumption and seedling trampling produced by an intense animal activity (Milder et al. 2008), which have a great influence on seedling establishment and survival (Pérez-Ramos and Marañón 2008, 2012). As a consequence, the colonizer oaks in the forest-mine edge do not need an excess of coverage by shrubs to improve environmental hardness (i.e., lack of shrub angle effect); instead, in this area, it seems more important that acorns and seedlings get some physical protection (i.e., shrub lateral protection) and establish under greater height shrubs, which increased water and nutrient availability for seedlings (Padilla and Pugnaire 2006). Simultaneously, light arrival to the ground increases as shrub height increases

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caused by shrubs’ architecture (Torroba-Balmori et al. 2015) and also because these broom species shed most of their leaves in early summer (García-Ibáñez 2001). It is interesting to mention that the positive effect of shrubs over Quercus seedlings increased from M1 to M2 (standardized path coefficients for shrub height=0.50 vs. 0.68, and shrub angle=0 vs. 0.19); therefore, the hypothesis that the positive shrub effects would increase as the environment undergoes more stress is accepted (from M1 to M2). It is well known that the positive effects of nurse shrubs over seedlings increase with increasing severity of the abiotic conditions (Padilla and Pugnaire 2006). Here, the abiotic conditions in M2 are more stressful than in M1 (i.e., higher irradiance and water stress), and thus the intensity of shrub features that improve environmental conditions for an effective seedling establishment increased. Therefore, the possibility of using nurse plants as tree restoration measure also increases with increasing severity conditions. Even in more mesic reclaimed mine sites, without summer drought, Sena et al. (2014, 2015) suggested that colonization of shrubs and forbs can enhance the growth and survival of planted trees. However, this benefit may also be balanced by negative competitive effects of especially invasive shrubs and trees. In any case, we must consider that in any mine site reclamation scheme, the nurse effect may be insufficient to favor seedling growth if abiotic conditions are particularly severe. In M2, only shrub height and shrub angle are positively related with seedlings, whereas shrub species is negatively related (Fig. 3b). Towards the mine center (M2), the shrub colonization takes longer than in forest-edge areas; therefore, the shrub abundance, height, and age are lower (Milder et al. 2008), and thus the environmental conditions are not as soft as in the forest edge. Hence, it seems that when seedlings reaches to the center of the mine site, their successful establishment depends more on shrubs’ features that ameliorate these hardest ecological conditions (i.e., light protection and soil fertility and water improvements; Alday et al. 2014) than on physical protection. This result highlights how in short distances the neighbor effects on seedlings can be produced by different shrub structural features depending on the environmental conditions that seedlings may overcome. An interesting result was the negative effect of Cytisus species on seedling establishment, which suggests that Quercus seedlings in M2 are more abundant under G. florida shrubs. This result may be produced because (1) Genista is the dominant colonizer shrubs of reclaimed mine sites after 20 years (Alday et al. 2011a), being most abundant in M2 than Cytisus, and showing greater structural development (Genista height 254 cm vs. Cytisus height 150 cm); and (2) Genista shrubs, being greater, give more protection to animals related with secondary dispersal of acorns (i.e., rodents and birds; Pérez-Ramos and Marañón 2008), and hence shrubs act as acorn traps supporting seedling establishment

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(Padilla and Pugnaire 2006). In any case, independently of the mine site considered (M1, M2), the positive neighbor effect of shrubs on seedlings during the first years supports the idea of using shrubs as ecosystem engineers in order to improve latesuccessional species establishment (Bradshaw 1997; Alday et al. 2014). Seedling survival, recruitment, and growth through time As expected, seedling survival was reduced through time independently of the environment considered. The high content of nutrient reserves of acorns lasts some months, but once these reserves are depleted, mortality affects those seedlings that cannot find appropriate abiotic and biotic conditions to growth (e.g., light, moisture, soil nutrients, competition). Moreover, the new seedlings are still exposed to predators that consume cotyledons; while cotyledon predation by jays and wood mouse might not lead to seedling mortality, wild boar predation almost always ensures seedling death (Den Ouden et al. 2005). On the other hand, in 2014, the survival of seedlings was significantly lower in the undisturbed forest than in both mine sites. This result could be related to (1) intra-specific competition among seedlings (Kuehne et al. 2013); (2) the moderate degree of shade tolerance of Q. petraea seedlings under forest canopies (Serrada et al. 2008), which reduces the seedling growth (e.g., significantly lower in Fo than in mined sites); and (2) the lower seedling protection in the forest to trampling and wild boar digging, whereas in mine sites seedlings were mostly under shrubs (C. scoparius and G. florida), considered to be nonpalatable and even of some toxicity to ungulates (Ammar et al. 2004). In any case, the high Quercus seedling survival after 4 years in mined sites highlights the importance for acorns to find suitable microsites for a successful colonization and survival. Here, more than 85 % of seedlings monitored during 4 years appeared under shrubs’ protection. Seedling survival reduction did not lead to a density reduction through time in the three environments, mainly because there was a yearly recruitment of new seedlings, which replaced the dead ones. It is well known that acorn production is dependent on favorable and unfavorable conditions among years (Shaw 1968). Here, we found higher seedling recruitment, for the three environments, in 2013 and 2014 following moderate crop years (2012 and 2013), although recruitment was always greater in undisturbed forest than on mined sites by the proximity to seed sources (Müller et al. 2007). It would be interesting to identify the productive years for Q. petraea in the area and use the acorn overproduction to seed it in the mine sites under shrubs as a reclamation measure to improve recruitment. Seedling annual growth and height through time was greater in mined sites (M1, M2) than in undisturbed forest (Fo). As previously commented, in more lighting environments, seedling growth and height are enhanced (Gómez-Aparicio et al. 2008; Pérez-Ramos et al. 2010); seedlings growing under shrub

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canopy benefit from more light intensity since C. scoparius and G. florida shed their leaves in early summer (García-Ibáñez 2001). However, in these mine sites (M1, M2), there was an environment×time×shrub interaction over seedling height in the way of the path models for establishment described for M1 and M2. In M2, shrubs produced a positive effect through time on seedling heights, with no seedlings surviving more than 3 years in open spaces. In contrast, although in M1 seedling height was greater under shrubs, the height increase through time was steeper in seedlings located in open spaces, probably because under shrubs there was a synergistic shade effect on oak seedlings from the shrub and forest canopies.

Conclusions 1. Seedling establishment differed among three environments considered, showing that mined sites (M1, M2) have lower values than undisturbed forest (Fo). However, seedling survival in mined sites was greater than expected, being optimal for natural regeneration of disturbed mine sites. 2. There was a positive effect of shrubs on Q. petraea seedling establishment in both mine environments (M1, M2), which increase as the environment undergoes more stress (from the mine edge (M1) to the center of the mine (M2)), and it was produced by different shrub structural features in each mine environment. 3. Seedling survival reduction through time in three environments did not lead to a density reduction because there was a yearly recruitment of new seedlings. However, seedling survival through time was lower in the undisturbed forest whereas seedling annual growth and height through time were greater in mine sites. 4. The positive neighbor effect of shrubs on Quercus seedlings found during the first years supports the use of shrubs as ecosystem engineers to increase heterogeneity in micro-environmental conditions improving latesuccessional species establishment. 5. Future reclamation strategies in similar areas should include shrub species (seeds or seedlings), especially G. florida, in order to create a quick and heterogeneous shrub cover that will provide suitable microsites for Quercus seedling establishment. Acknowledgments We thank the mining company BUMINSA^ for the information on their restoration procedures and permission to work at this mine, AEMET (Meteorological Spanish Agency) for providing meteorological data, and Fernando Valenciano Velasco for fieldwork assistance. We also thank three anonymous reviewers for their kind comments and valuable corrections to improve the manuscript. This study was supported by the Project VA042A10-2 from Junta de Castilla y León to C. Martínez-Ruiz, the BPrograma I: Programa de financiación de grupos de investigación^ from the Salamanca University to B. Fernández-Santos, and a FPU grant from Spanish Ministry of Education to P. Torroba (FPU 12/00125).

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