RESEARCH ARTICLE Mid-term effects on ecosystem services of quarry restoration with Technosols under Mediterranean conditions: 10-year impacts on soil organic carbon and vegetation development Vicenç Carabassa1,2,3 , Xavier Domene1,2 , Elisa Díaz1,4 , Josep M. Alcañiz1,2 The use of Technosols for the restoration of limestone quarries overcomes the usual “in situ” scarcity of soil and/or its poor quality. The use of mine spoils, improved with mineral and/or organic amendments, could be an efficient and environmentally friendly option. Properly treated sewage sludge from urban wastewater treatment plants could be a suitable organic amendment and fertilizer (rich in N and P) whenever its pollutant burden is low (heavy metals and/or organic pollutants). Its appropriate use could improve essential soil physical and chemical properties and, therefore, promote key ecosystem services of restored areas, such as biomass production and carbon sequestration, as well as biodiversity and landscape recovery. However, the mid-term impacts of these restoration practices on soil functioning and their services have rarely been reported in the available literature. In this study we assess the mid-term effects (10 years) of the use of sewage sludge as a Technosol amendment on soil organic carbon (SOC), nutrient status, and plant development in several restored quarries. Soils restored using sewage sludge showed a threefold increase in SOC compared to the corresponding unamended ones, despite the moderate sludge dosage applied (below 50 tonnes/ha). Plant cover was also higher in amended soils, and recruitment was not affected by sludge amendment at these doses. This study demonstrates that, used at an appropriate rate, sewage sludge is a good alternative for the valorization of mine spoils in quarry restoration, improving some important regulatory ecosystem services such as carbon sequestration, without compromising woody plant encroachment. Key words: organic amendments, quarry restoration, sewage sludge, soil organic carbon sequestration, Technosol depleted (Moreno-Peñaranda et al. 2004). Manufactured soils Implications for Practice (Technosols) could be a viable soil source when the availabil- • The use of sewage sludge as organic amendment in mine ity of suitable natural soils is limited (Watkinson et al. 2017), spoil-based Technosols is an environmentally friendly and with this technology being emblematic of the issues we face for economically suitable option for the restoration of land the management of the soils of the Anthropocene (Leguédois degraded by quarrying and could allow a fast recovery of et al. 2016). The use of organic waste for Technosol construc- the ecosystem services lost. tion is a widely used practice in mine restoration (Asensio et al. • After 10 years, sludge-amended Technosols boosted pri- 2013; Lomaglio et al. 2017; Watkinson et al. 2017), with the mary production and promoted a threefold increase in aim of speeding up the biological colonization of a relatively organic carbon stocks without compromising woody plant inert initial substrate. Specifically, the use of sewage sludge for encroachment. • The use of digested municipal sewage sludge with a high degree of stability (>30%), at moderate doses (ca. Author contributions: VC, JMA conceived and designed the research; VC, ED performed the experiments; VC, XD, ED analyzed the data; VC, XD, JMA wrote and 45 tonnes/ha), in Technosol construction minimizes envi- edited the manuscript. ronmental risks and maximizes ecosystem services in 1 CREAF, E08193 Bellaterra (Cerdanyola del Vallès), Catalonia Spain terms of carbon sequestration and plant biodiversity. 2 UniversitatAutònoma de Barcelona, E08193 Bellaterra (Cerdanyola del Vallès), Catalonia, Spain 3 Address correspondence to V. Carabassa, email v.carabassa@creaf.uab.cat 4 Wageningen University and Research, Wageningen, The Netherlands Introduction © 2019 The Authors. Restoration Ecology published by Wiley Periodicals, Inc. on Quarrying activities produce severe impacts on important eco- behalf of Society for Ecological Restoration logical functions that provide ecosystem services contributing This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided to human well-being. In most of the scenarios, restoring ecosys- the original work is properly cited. tem services after finishing the exploitation implies the recov- doi: 10.1111/rec.13072 Supporting information at: ery of vegetation in sites where soil fertility levels have been http://onlinelibrary.wiley.com/doi/10.1111/rec.13072/suppinfo Restoration Ecology 1 Carbon sequestration in quarry Technosols quarry restoration is a management option that contributes to the influenced by its biochemical recalcitrance, its stabilization as valorization of mine spoils and sludge from urban wastewater organomineral aggregates, the occlusion in soil aggregates, or treatment plants (Sopper 1993), in agreement with the EU prin- its transportation into the subsoil (Lal 2003). Sewage sludge, ciples for a more circular economy (Mosquera-Losada et al. as a biomass derived residue, may directly contribute to soil 2017). When a Technosol approach is taken, sewage sludge carbon sequestration through its stabilization in soil, and indi- is applied once, at a moderate dosage, to act both as fertilizer rectly through the increase in plant biomass production and and organic amendment, and usually mixed with mining debris litter intake (Ojeda et al. 2015). However, the relatively low before their spreading as a topsoil layer in the restored areas. stability of sewage sludge (Mattana et al. 2014) is expected to Sewage sludge is then an interesting option for valorizing mine cause transient effects on soil organic matter pools, as mid-term spoils due to its fertilizing properties (Van-Camp et al. 2004) soil organic carbon (SOC) sequestration relies more on the and its known positive effects on soil aggregate stability (Car- subsequent evolution of OC inputs from plant debris intake to avaca et al. 2002; Ojeda et al. 2008), soil water retention (Ojeda soil rather than on the OC provided by the sludge (Ojeda et al. et al. 2010, 2011), and vegetation recovery (Moreno-Peñaranda 2015). Organic matter improvements, in turn, can contribute et al. 2004; Ortiz & Alcañiz 2006; Carabassa et al. 2018). How- to other relevant ecosystem services in rehabilitated land such ever, sewage sludge application also requires strong supervision as raw materials production (for fuel, construction materials, and monitoring due to certain environmental risks related to its etc.), nutrient cycling, climate regulation, or improving soil as potentially harmful heavy metals and persistent organic pollu- habitat for organisms (Baveye et al. 2016). However, little is tant content (Düring & Gäth 2002; Carabassa et al. 2010a). known about the efficiency of Technosol approaches in terms Pedogenic processes occurring in Technosols are similar to of soil carbon storage (Ojeda et al. 2015), and especially in those of natural soils (Leguédois et al. 2016), although the the mid and long term, which could be of interest for offset- components used can strongly influence their evolution and ting the emissions of mining activities closely linked to the their capacity to behave as a soil, and therefore, to provide the cement industry, one of the main contributors to industrial CO2 associated ecosystem services. However, they tend to have a emissions (Imbabi et al. 2012). fast evolution compared to natural soils, including biological The use of sewage sludge in Technosols is expected to activity (Leguédois et al. 2016). The last is of importance since enhance the biological colonization in the initial stages of soil fauna and vegetation are key factors for the provision of the restoration. In previous studies, the use of sewage sludge ecosystem services in soils (Tate 2005), but biological activity was shown to strongly influence plant community structure also drives soil pedogenesis itself, e.g. through its role in carbon in the short term in a shrubland intended to be converted and nitrogen dynamics (Frouz et al. 2013). into a dehesa (Ferreiro-Domínguez et al. 2011; Tarrasón et al. Soils are responsible for a variety of natural processes known 2014). On the contrary, no significant effects on diversity as soil functions that are the basis of the delivery of the so-called were found when the reference was the neighboring forest ecosystem services (Adhikari & Hartemink 2016). While soil or shrubland (Moreno-Peñaranda et al. 2004). Some negative functions refer to the soil benefits for all the ecosystem species, ecological effects of the use of sewage sludge have been including humans, the term ecosystem service specifically refers reported elsewhere, such as declines in microbiota, meso- to human benefits (Adhikari & Hartemink 2016; Baveye et al. fauna, and macrofauna sensitive taxa (Barrera et al. 2001; 2016). Because of the difficulties in the direct assessment of Giller et al. 2009; Andrés et al. 2011), the promotion of exotic ecosystem services, soil functions have been used as indica- species (Alpert et al. 2000), and decreases in plant biodiver- tors of the provision of those services (Baveye et al. 2016). sity (Ferreiro-Domínguez et al. 2011). This is of concern given For instance, organic carbon (OC) content has been used as a the ecosystem services driven by plants (Lavorel 2013) and soil proxy of carbon sequestration, while the biodiversity of particu- organisms (Lavelle et al. 2006). lar groups of organisms has been related to the habitat function To prevent the negative effects of excessive dosing of sewage of soil. The provision of ecosystem services is the main reason sludge that might compromise the provision of ecosystem ser- for soil rehabilitation, due to their direct connection with human vices of rehabilitated land, some recommendation protocols well-being (UNEP 2008). In the last decade, the ecosystem ser- have been proposed, such as the one used since 2008 in Catalo- vices concept has been successfully adopted by environmental nia by the local environmental authorities (Alcañiz et al. 2009; scientists, media, and governmental agencies, boosted by the Carabassa et al. 2010a, 2010b; Department of Territory and Sus- publication of the Millennium Ecosystem Assessment (2005). tainability 2015). This guideline takes into account the mineral Thus, ecosystem services approaches have been included in a substrate characteristics, the stability of the sewage sludge used variety of applications, from land planning and the assessment (recommended to be over 30%), its pollutant burden, the site of particular soil management alternatives, to the assessment aptitude (sewage sludge should not be used near wells, water of restoration success, given the increasing social expectations courses, nitrate vulnerable zones, or highly frequented or inhab- toward soils in the Anthropocene (Leguédois et al. 2016). ited areas), among other environmental restrictions. The pro- Regarding carbon sequestration in soil, it is generally tocol also states a dosing limit for sludge (50 tonnes/ha) and a achieved by any biomass input that originated through a pro- maximum increase in labile organic matter in the receiving soils cess causing a net removal of atmospheric CO2 -C by plants, or substrates (0.5%). and then stored as stable soil organic matter. The storage The main goal of this article is to assess the mid-term effects efficiency of the different pools of organic matter is highly (10 years), on two key ecosystem services (carbon sequestration 2 Restoration Ecology Carbon sequestration in quarry Technosols Figure 1. Location of the evaluated quarries on the NE Iberian Peninsula. and habitat function), of the use of sewage sludge in Technosol plants. All of them had enough quality to be used in agriculture, construction for limestone quarry restoration, under Mediter- i.e. had relatively high stability (48% as average) and low heavy ranean conditions. metal content (Table 3). As usually found in sewage sludge, P concentrations were very high. Sludge was dosed according to Methods its organic matter content, stability degree, and the properties of the mineral substrate (stoniness and bulk density), follow- Study Sites ing Alcañiz et al. (2009) and Carabassa et al. (2010a, 2010b). A set of seven limestone quarry sites, restored 10 years The average sludge dose used in the different sites was around ago using Technosols, were selected, all of them located in 45 tonnes/ha (dry weight), and its field application was con- the Mediterranean climatic area of Catalonia (NE Iberian ducted between autumn 2006 and spring 2007. Peninsula) (Fig. 1). Each experimental site corresponded to a Technosol constructed using sewage sludge, and a neighbor- ing control area corresponding to a Technosol with the same Field Sampling and Laboratory Analysis mineral substrate but without adding sludge (Table 1). Climatic The parameters assessed in the rehabilitated areas reflect the conditions in the different sites mostly differed in terms of water sludge-based Technosols’ ability to improve soil quality, min- availability, since mean annual precipitation ranged from 400 to imize degradation processes, and promote vegetation develop- 700 mm (from wet to semiarid Mediterranean climate). The ref- ment. Soil samplings were carried out in 2007 (4–6 months erence ecosystem for the restoration was a Mediterranean forest after sludge application) and in May–June 2017 (10–11 years that predominates in the study area, dominated by Aleppo pine after sludge application). Vegetation measures were carried out (Pinus halepensis) usually mixed with holm oak (Quercus ilex) in May–June 2017 after 10–11 years of the sludge applica- and accompanying shrub species (Table 1). Prior to restoration, tion. Soil sampling involved taking a composite sample of cores the areas were used for limestone exploitation for aggregate or (n = 12–20, depth = 0–20 cm) for each restored zone with an concrete production. The evaluated sites (sludge amended and Edelman auger. controls) had an average surface area of 3,000 m2 , and covered The soil parameters analyzed were particle size determined many facings, from the most favorable (N face) to the most by sedimentation—Robinson pipette (Clarke Topp & Ferré challenging (S face). The dominant geomorphologic (land- 2002), equivalent CaCO3 by CO2 volume released after HCl form) type is the terrace/berm embankment with steep slopes, addition—Bernard calcimeter method, electrical conductivity some approaching 45∘ . The subsoil of embankments primarily of 1:5 (w:v) water extract, SOC content by acid dichromate consisted of fine and/or rocky fractions from extraction debris oxidation, total nitrogen using the Kjeldahl method, avail- or excavations, and sometimes with blasting debris. able phosphorous—Olsen, and available potassium (Ameri- can Society of Agronomy 1982). In each restored area, veg- Technosols Construction etation measures were taken according to Carabassa et al. The mineral substrate used for Technosol construction mostly (2019): establishing 6 × 10 m transects and measuring the main consisted of rocky debris, sometimes mixed with topsoil kept cover types (herbaceous, shrubs, trees, organic debris, bare aside from mine topsoiling or excavations. In some cases, the soil) by contact-point each 20 cm; shrub and tree density stoniness was very high (over 80%), having a high proportion by identifying and counting all the seedlings in 3 × 100-m2 of carbonates and very low organic matter content (Table 2). plots; flora inventories identifying all the species present; Sewage sludge consisted of an anaerobically digested sludge species abundance by qualitative observation of its respective coming from medium-size municipal wastewater treatment cover. Restoration Ecology 3 4 Table 1. Quarry sites, their location, climatic conditions (precipitation and temperature), slope characteristics (orientation, morphology, steepness, filler material, and lithology), and reference system (plant community of the surrounding area). *Material used to fill the excavation hole for giving the final morphology (geomorphic reclamation) to the restored areas (De la Vergne 2006). Mean Mean Annual Annual Carbon sequestration in quarry Technosols Latitude Longitude Precipitation Temperature Maximum Site (N) (E) (mm) (∘ C) Orientation Landform Slope (∘ ) Filler* Dominant Lithology Reference System Aiguamolls 41∘ 28′ 31′′ 0∘ 49′ 39′′ 451 14.9 W Terrace/berm 42 Rocky debris Marl Thymus vulgaris and embankment Rosmarinus officinalis with steep slope shrubland with Pinus halepensis Ponderosa 41∘ 15′ 41′′ 1∘ 09′ 27′′ 589 14.9 E Terrace/berm 42 Soil and rocky Limestone Pinus halepensis forest embankment debris with steep slope Lázaro 41∘ 12′ 07′′ 1∘ 28′ 57′′ 505 15.9 SE Terrace/berm 43 Rocky debris Limestone Pinus halepensis forest embankment with steep slope Fou 41∘ 21′ 32′′ 1∘ 54′ 34′′ 684 13.2 NE Terrace/berm 33 Rocky debris Limestone Pinus halepensis forest embankment with steep slope Vallcarca 41∘ 15′ 13′′ 1∘ 52′ 25′′ 535 15.6 NO Terrace/berm 42 Without filler, Marl and limestone Mixed forest: Quercus ilex embankment blasting debris and Pinus halepensis with steep slope Falconera 41∘ 15′ 40′′ 1∘ 53′ 12′′ 545 15.5 NO Terrace/berm 33 Soil and mining Limestone Pinus halepensis forest embankment wastes with steep slope Montlleó 41∘ 41′ 35′′ 1∘ 49′ 39′′ 630 13.7 S Terrace/berm 40 Rocky debris Marl Thymus vulgaris and embankment Rosmarinus officinalis with steep slope shrubland with Pinus halepensis Restoration Ecology Carbon sequestration in quarry Technosols Table 2. Properties of the soils and mining debris used for the Technosols’ construction. *Referring to the fine fraction (<2 mm). Organic Electrical Bulk <2 mm Sand* Silt* Clay* Carbonate* Matter* Conductivity Density Site (%) (%) (%) (%) (g/kg) pH (g/kg) (1:5 extract, dS/m) (mg/m3 ) Aiguamolls 22 14 50 36 421 8.8 1.0 0.48 1.8 Ponderosa 45 34 33 34 314 8.3 7.0 0.90 1.5 Lázaro 17 50 22 28 734 8.3 2.7 0.27 1.6 Fou 22 21 30 49 426 8.2 7.0 0.58 1.4 Vallcarca 57 46 22 32 271 8.3 3.7 0.37 1.5 Falconera 55 58 21 21 207 8.1 11.9 1.16 1.4 Montlleó 75 41 40 19 390 8.4 8.0 1.96 1.2 Table 3. Physicochemical characterization of the sewage sludge used for Technosol construction. *Percentage of organic matter resistant to acid hydrolysis. Parameter Average Max. Min. SD Dry matter (%) 24.5 26.8 22.5 12.6 Organic matter (%) 57.7 70.7 39.2 27.1 Degree of stability (%)* 48.1 60.1 31.8 17.2 Conductivity (1:5 extract. dS/m 25∘ C) 2.0 3.0 1.0 0.7 pH (water 1:10 w:v) 7.7 8.5 6.9 0.6 N-Kjeldhal (g/kg) 36.8 63.4 11.5 19.8 N-ammonia (g/kg) 10.7 21.5 1.8 7.3 P-total (g/kg) 38.3 64.4 24.5 23.5 K (g/kg) 2.8 5.7 1.0 1.5 Cu (mg/kg) 322.3 580.0 102.0 170.6 Ni (mg/kg) 23.0 43.3 15.5 13.9 Cr (mg/kg) 56.6 85.6 12.5 35.7 Pb (mg/kg) 54.3 64.2 29.5 28.1 Hg (mg/kg) 2.0 4.2 0.2 1.3 Cd (mg/kg) 3.7 10.0 0.9 3.6 Zn (mg/kg) 1, 037.6 2, 199.0 375.0 512.6 Data Analysis largest contrast between amended and control soils, with very Analysis of variance (one-way ANOVA and repeated mea- high contents in the sludge-amended Technosols, which were sures ANOVA) was used to examine differences between 10 times higher than in unamended soils where values showed treatments (amended and control soils) regarding soil prop- a clear deficiency. erties (organic matter, N, and P contents), proportion of soil Regarding soil C:N ratio (Fig. 3), most soils were well bal- cover in each category (herbaceous, total vegetal, organic anced, with a ratio between 8 and 12, which are typical val- debris) and herbaceous development (height), using p < 0.05 ues for A horizons of calcareous Mediterranean forest soils. In as the cut-off value for statistical significance throughout the general, ratios were similar for amended and unamended soils, manuscript. except in the Lázaro control treatment, where the C:N ratio was extremely high due its very low N content. Regarding the N:P ratio, controls were deficient in available P and highly unbal- Results anced, mainly when rocky debris without including topsoil were used for Technosol construction. Soil Properties Comparing the soil property values shortly after Technosol After 10 years of Technosol construction, sludge-amended soils construction (4–6 months) with the results after 10 years had significantly higher organic matter, N, and P contents com- (Fig. 4), it was shown that SOC increased in both amended pared to the unamended ones (Fig. 2), achieving a fivefold and unamended soils (control areas) but more strongly in the content increase in one of the sites. Some unamended Tech- sludge-amended plots, with a 2.1-fold increase compared to the nosols were clearly deficient in organic matter, with SOC values 1.6-fold increase in the unamended Technosols. After 10 years, below 0.5%. These differences were even stronger in the case the control Technosols also failed to achieve the initial SOC of N, where sludge-amended Technosols had more than three levels of sludge-amended ones. Amended soils tended to show times higher contents compared to unamended ones, which were significant increases in N and P content after 10 years, but this extremely poor in N, especially when only mine spoils were trend was not observed for P, with nonsignificant changes, used as mineral substrate. Moreover, P contents showed the despite a tendency to increase (Fig. 5). Restoration Ecology 5 Carbon sequestration in quarry Technosols Figure 3. C:N and N:P ratios of sludge-amended and control Technosols 10 years after construction, in the different sites studied. plots. The average herbaceous cover over all plots was less than 50% (Fig. 6). However, herbaceous vegetation was still more developed in amended plots, where organic debris accumula- tion was also higher (Fig. 6). Regarding herbaceous species composition, sludge-amended Technosols showed a higher fre- quency of ruderal species, such as Chenopodium album, Malva sylvestris, and Cardus spp. (Table S1), but they were not domi- nant. Colonization by native neighboring species was observed in both Technosol approaches. Some silt-tolerant and halophyte plants, like Salsola kali or Atriplex halimus, were more frequent in sludge-amended soils despite salinity not being significantly higher. Some invasive species such as Arundo donax were iden- Figure 2. SOC, Kjeldhal N, and Olsen P content in sludge-amended and tified in amended plots, despite the fact that their vegetation control Technosols 10 years after their construction. The error bars represent +SE and different letters indicate significant differences at a cover is minimal, and its presence cannot be attributed to sludge p < 0.05 level. amendment but to its introduction as rhizomes in the exogenous soil used for Technosol construction. Regarding the shrub and tree strata, sludge-amended plots Considering only the topsoil layer (first 20 cm depth), the presented higher woody cover (shrubs and trees), mainly due average organic C sequestration in sludge-amended Technosols to enhanced pine growth, which explains the higher total plant was 28 tonnes C/ha after 10 years, and 9 tonnes C/ha was con- cover in this treatment (Fig. 6). The presence of shrubs and tained in the unamended ones, which represents a threefold trees is mainly explained by plantation actions carried out after increase in the sequestered C. Technosol spreading. However, in most areas, recruitment of at least one wild shrub species took place, while this was also true Plant Community and Development but less usual for tree species. The most common tree species After 10 years, herbaceous cover was still dominant in most of found was Aleppo pine (Pinus halepensis), although in some the areas evaluated, irrespective of controls or sludge-amended cases holm oak (Quercus ilex) was also present at much lower 6 Restoration Ecology Carbon sequestration in quarry Technosols increase with increasing rock fragment content, and that spread- ing farmyard manure and slurry induces higher carbon concen- trations mostly in wet and stony grasslands. Similarly, Arias et al. (2017) found gains of up to 10 tonnes C/ha in the tilled layer (0–30 cm) of stony soils only after 2 years of irrigation. After 10 years of restoration works, the average SOC of soils amended with sewage sludge was relatively high, while the SOC content in the control areas was very low and clearly deficient (Carabassa et al. 2010a, 2010b; Carabassa et al. 2015). In any case, both amended and unamended soils were still far from the SOC average for Mediterranean forest soils (Lal 2005; Rovira & Ramón Vallejo 2007; Doblas-Miranda et al. 2013), and therefore probably far from any C saturation situation, especially considering the relatively high clay content of soils in this study. Despite the fact that SOC fractioning was not available in Figure 4. Initial (t0 , 4–6 months) and 10 years (t10 ) soil organic carbon this study, previous studies on Technosols from quarries con- (SOC) contents in sludge-amended and control Technosols of studied firmed that SOC tends to be more stabilized over time in quarries. The error bars represent +SE and different letters indicate significant differences at a p < 0.05 level. sewage-amended soils, doubling the fraction of nonhydrolyz- able carbon in the mid term (Ojeda et al. 2015). Considering that many organic compounds of this nonhydrolyzable fraction densities (see Table S1). Regarding shrubs, Dittrichia viscosa, are hard to mineralize (Rovira & Ramón Vallejo 2007), we state an extremely common Mediterranean plant of the first stages that this SOC fraction of the sludge-amended mine Technosols of secondary succession, had colonized almost all the areas could be considered as sequestered carbon. Moreover, in this evaluated. Rosemary (Rosmarinus officinalis), mastic (Pistacia study all the Technosols had a high carbonate content, which lentiscus), and cotton lavender (Santolina chamaecyparissus) contributes to the formation of aggregates and to the physical were also found in many of the areas evaluated. Most specimens protection of SOC (Amézketa 1999). of these bushes were planted, although natural recruitment Regarding the total amount of carbon sequestered in soils at was also observed, especially in the case of mastic. There a world level, the vast majority of the SOC reservoir is reported were no notable differences between treatments regarding the to be below 20 cm (Fontaine et al. 2007). This deep carbon recruitment of shrub or tree species (see Table S1). is highly persistent because it is bonded to soil minerals and it is less accessible for decomposers (Wattel-Koekkoek et al. 2003). However, we only considered the first top 20 cm of soil in Discussion our carbon stock estimations. Consequently we underestimated After 10 years, Technosols constructed using sewage sludge as the total SOC, especially on amended plots, due to the strong an amendment had three times more SOC than the unamended plant growth in the first years after Technosol construction ones. On one hand, it is clear that sewage sludge has contributed (Carabassa et al. 2018). This plant growth, which included to changes in the organic matter content of the soil, but most trees, could have increased deep C through root growth, as of its organic matter is labile, which suggests that the direct shown by Simón et al. (2018) in mine Technosols in SE Spain effects of sludge on soil have only been transient (Tarrasón et al. 6 years after their establishment. Nevertheless, this plausible 2010). On the other hand, plant debris from vegetation grown underestimation might be limited considering the reduced soil in restored areas contributes to increased SOC (Muñoz-Rojas depth of the Technosols included in this study. et al. 2016) that tends to be stabilized and concentrated in the Regarding nutrient content, some control Technosols were fine fraction (<2 mm). For this reason, the increase in SOC clearly deficient and unbalanced in N and P. This fact might observed in amended plots after 10 years is more likely due to explain the low vegetation success in sites with relatively low the contributions of vegetation growth in the area than from hydric stress (700 mm annual precipitation), as N and P are the OC directly provided by the sludge. These differences were the two main macronutrients limiting plant primary production higher in extremely stony soils (<20% fine fraction) located in terrestrial ecosystems (Elser et al. 2007). This is especially in moderately rainy regions (700 mm annual precipitation) that true in Mediterranean forest ecosystems with calcareous soils allowed herbaceous vegetation to grow after sludge applica- that reduce P bioavailability (Sardans et al. 2004). Furthermore, tion and rain events. In contrast, fine soils in semi-arid regions nutrient imbalances in the stoichiometric relationship between (500 mm annual precipitation) did not accumulate such quanti- N and P can have significant impacts on soil functions, affecting ties of C in amended soils, due to the smaller positive impact of the development of vegetation and microbial activity (Sardans the amendment on growth of herbaceous vegetation, and con- et al. 2012). sequently differences with respect to control were also lower. On the contrary, sludge-amended Technosols still presented This seems to be confirmed by Meersmans et al. (2012), who high N and P concentrations after 10 years, and in the spe- detected that OC concentrations in fine particle-size fraction cific case of N, more than in the short term after sludge Restoration Ecology 7 Carbon sequestration in quarry Technosols Figure 5. Kjeldhal N and Olsen P contents in sludge-amended Technosols 4–6 months (t0 ) and 10 years (t10 ) after sludge application. The error bars represent +SE and different letters indicate significant differences at a p < 0.05 level. 100 100 b 80 80 a Total vegetal cover (%) Herbaceous cover (%) 60 a 60 a 40 40 20 20 0 0 Control Sludges Control Sludges 100 100 b 80 80 Organic debris cover (%) Herbaceous height (cm) 60 60 a 40 40 b 20 20 a 0 0 Control Sludges Control Sludges Figure 6. Percentage of plant cover type distribution (herbaceous, total vegetal, organic debris) and herbaceous development (height [cm]) on sludge-amended and control Technosols 10 years after sludge application. The error bars represent +SE and different letters indicate significant differences at a p < 0.05 level. 8 Restoration Ecology Carbon sequestration in quarry Technosols amendment. Although nitrogen leaching is plausible with the linked to the two main soil ecosystem services that are intended sludge treatment, it would mainly take place during the first to recover in the restoration of quarrying activities, which are 4 months due to the high mineralization rates of organic N biological habitat and carbon sequestration. Furthermore, we from sludge (Carabassa et al. 2018). After this period, leaching demonstrate that the valorization of “in situ” mine spoils can should decrease quickly due to reduced sludge decomposition be successful and improved by the use of sewage sludge, in rates and the enhanced nitrate absorption by the growing vegeta- agreement with the current principles of the circular economy. tion (Tarrasón et al. 2008; Jordán et al. 2017). As SOC becomes stabilized over time in sludge-amended Technosols (Ojeda et al. 2015), N stabilization in organic forms is also expected, as shown by the balanced C:N ratios observed. Regarding P, and Acknowledgments despite its high levels, a low availability is expected due to the This study was funded by the Department of Territory and Sus- alkaline pH of the highly calcareous materials used for Tech- tainability of the Government of Catalonia through the project nosol construction that causes a fast immobilization of P as “Research and innovation on the control and the restoration of calcium triphosphate (Tunesi et al. 1999). extractive activities.” Regarding total plant cover, significant differences between amended and control Technosols persisted after 10 years. How- LITERATURE CITED ever, despite herbaceous cover being similar in both treatments, Adhikari K, Hartemink AE (2016) Linking soils to ecosystem services—a global herbaceous vegetation was more developed in sludge-amended review. Geoderma 262:101–111 areas, which was coupled to an enhanced accumulation of Alcañiz JM, Ortiz O, Carabassa V (2009) Utilización de lodos de depu- organic debris and the consequent higher content of SOC radora en restauración. Manual de aplicación en actividades extractivas (Wambsganss et al. 2017). Even though the absolute herbaceous y terrenos marginales. Agència Catalana de l’Aigua, Generalitat de cover was less than 50% in both treatments, this was not of Catalunya, Barcelona, Spain. http://mediambient.gencat.cat/web/.content/ concern due to the effective protection against erosion because home/ambits_dactuacio/empresa_i_produccio_sostenible/restauracio_ dactivitats_extractives/Productes-emprats-restauracio-ambiental/ of the high stoniness of these soils. Moreover, sludge-amended restauracio_dactivitats_extractives_amb_fangs_de_depuradora/ areas had higher cover of woody plants, associated with the high documentos/protocol_fangs_cast.pdf fertilizing effect on pine growth, which in turn also plausibly Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of contributed to the increased SOC. This tree-specific fertilizing environmental stress in the spread of non-native plants. Perspectives in effect has been described elsewhere and shown as higher tree Plant Ecology, Evolution and Systematics 3:52–66 growth ratios in soils amended with sludge for restoration pur- American Society of Agronomy (1982) Methods of soil analysis. Part 2. Chem- poses (López-Díaz et al. 2009; Tarrasón et al. 2014). ical and microbiological properties. Second edition. Soil Science Society Regarding plant composition, and coupled to the higher N of America, Madison, Wisconsin Amézketa E (1999) Soil aggregate stability: a review. Journal of Sustainable levels, higher relative abundance of nitrophilous species was Agriculture 14:83–151 observed in sludge-amended soils, though those species were Andrés P, Mateos E, Tarrasón D, Cabrera C, Figuerola B (2011) Effects of not dominant in the community after 10 years. Thus, the species digested, composted, and thermally dried sewage sludge on soil microbiota compositions in both types of Technosols were similarly rud- and mesofauna. Applied Soil Ecology 48:236–242 eral, in agreement with previous studies conducted 5 years after Arias N, Orcaray L, Bescansa P, Enrique A, Virto I (2017) Implications of sludge application (Moreno-Peñaranda et al. 2004). Despite rock fragments for soil quality evaluation: assessing changes in a gravelly the slowness of this process and the fact that woody species irrigated soil following no till adoption. Communications in Soil Science and Plant Analysis 48:1–15 were also present in unamended Technosols (including natu- Asensio V, Vega FA, Andrade ML, Covelo EF (2013) Technosols made of ral recruitment), enhanced woody (shrubs and trees) species wastes to improve physico-chemical characteristics of a copper mine soil. recruitment was observed in sludge-amended plots, which rep- Pedosphere 23:1–9 resents an important goal in the restoration of these areas due to Barrera I, Andrés P, Alcañiz JM (2001) Sewage sludge application on soil: effects the beneficial effect on ecosystem functioning (Soliveres et al. on two earthworm species. Sort 129:319–332 2014). This show that Technosols constructed with mine spoils Baveye PC, Baveye J, Gowdy J (2016) Soil “ecosystem” services and natural without organic amendment are less successful in terms of veg- capital: critical appraisal of research on uncertain ground. Frontiers in Environmental Science 4:41 etation development and community complexity, mostly due to Carabassa V, Serra E, Ortiz O, Alcañiz JM (2010a) Sewage sludge applica- the extremely low fertility of the quarry substrates. tion protocol for quarry restoration (Catalonia). Ecological Restoration In summary, after a decade, Technosols constructed with 28:420–422 moderate dosages of sewage sludge boosted soil organic matter Carabassa V, Vizcano M, Serra E, Ortiz O, Alcañiz JM (2010b) Getting real: enrichment and carbon sequestration, as they contained three a procedure for self-evaluation of quarry restorations. In: 7th University times more SOC than the unamended ones. This was the result of Avignon, Avignon, France. https://ser-koha.inbo.be/cgi-bin/koha/opac- of increased primary production due to the high nutrient content detail.pl?biblionumber=1008 Carabassa V, Ortiz O, Alcañiz JM (2015) Evaluación y seguimiento de la of sludge, which was still visible after 10 years. 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Guest Coordinating Editor: António Mira Received: 27 February, 2019; First decision: 25 June, 2019; Revised: 23 October, 2019; Accepted: 23 October, 2019 Restoration Ecology 11