Nutrient Contribution of Litterfall in a Short Rotation Plantation of Pure or Mixed Plots of Populus alba L. and Robinia pseudoacacia L.

Article Nutrient Contribution of Litterfall in a Short Rotation Plantation of Pure or Mixed Plots of Populus alba L. and Robinia pseudoacacia L. Isabel González 1, Hortensia Sixto 1, Roque Rodríguez-Soalleiro 2and Nerea Oliveira 1,* 1 Forest Research Centre, National Institute for Agriculture and Food Research and Technology (INIA-CIFOR), Crta, de la Coruña km 7.5, E-28040 Madrid, Spain; [email protected] (I.G.); [email protected] (H.S.) 2Sustainable Forest Management Group, University of Santiago de Compostela, C/Benigno Ledo s/n, E-27002 Lugo, Spain; roque.r[email protected] *Correspondence: oliveira.ner[email protected] Received: 6 October 2020; Accepted: 23 October 2020; Published: 25 October 2020   Abstract: This study aims to quantify the potential contribution of nutrients derived from leaf litter in a short rotation coppice plantation which includes monocultures of the species Populus alba (PA) and Robina pseudoacacia (RP) as well as a mixture of 50PA:50RP, in the middle of the rotation. TheP. alba monoculturewasthatwhichprovidedthemostleaflitter(3.37mgha −1 yr −1 ), followedbythe 50PA:50RP mixture (2.82 mg ha −1 yr −1 ) and finally the R. pseudoacacia monoculture (2.55 mg ha −1 yr −1 ). In addition to producing more litterfall, leaves were shed later in the P. alba monoculture later (December) than in the R. pseudoacacia monoculture (October) or the mix (throughout the fall). In terms of macronutrient supply per hectare, the contributions derived from leaf litter were higher for K, P and Mg in the case of P. alba and for N in R. pseudoacacia, the mix presenting the highest Ca content and intermediate concentrations for the rest of the nutrients. In addition, other factors such as C:N or N:MO ratios, as well as the specific characteristics of the soil, can have an important impact on the final contribution of these inputs. The carbon contribution derived from leaf fall was higher in the P. alba monoculture (1.5 mg ha −1 yr −1 ), intermediate in the mixed plot (1.3 mg ha −1 yr −1 ) and slightly lower for the R. pseudoacacia monoculture (1.3 mg ha −1 yr −1 ). Given these different strategies of monocultures with regard to the dynamism of the main nutrients, species mixing would appear to be suitable option to achieve a potential reduction in mineral fertilization in these plantations. Keywords: short rotation coppice (SRC); biomass; white poplar; black locust; monocultures; mixture; leaf litter 1. Introduction Forest plantations of fast-growing species under a short rotation coppice system (SRC) can contribute to the supply of biomass for use in bioenergy and bioproducts within the context of the bioeconomy [ 1 ]. Salicaceae (poplars and willows) are suitable species for this purpose due to their high productivity, ease of vegetative multiplication and ample availability of genetic material [ 2 ], resulting in crops of this family of genotypes being common in many areas of the world [ 3 ]. To a lesser extent, other species have been considered for SRC [ 4 , 5 ]. Among the latter, Robinia pseudoacacia L., of de Fabaceae family, is also a fast-growing species, with a certain degree of drought tolerance, capable of sprouting from the stumps and with a high nitrogen fixing capacity [ 6 ]. For these reasons, Robinia is considered suitable for cultivation in SRC in some areas of Europe [ 7 , 8 ], although it is also considered an invasive species introduced into Europe in the 17th century [9]. MostSRC plantationsare establishedasmonocultures withasinglespecies, althoughthepossibility of mixed stands has also been explored [ 10 – 12 ]. Mixed plantations, in addition to increasing genetic Forests 2020,11, 1133; doi:10.3390/f11111133 www.mdpi.com/journal/forests Forests 2020,11, 1133 2 of 19 variability and favoring tolerance to certain stresses, can also provide productive benefits based on complementary or facilitation strategies [13]. One of the main internal flows of the continuous vegetation–soil–fauna dynamic in forestry or agroforestry ecosystems is leaf litter, the subsequent decomposition process, and the consequent incorporation of organic matter and nutrients, needed for growth, into the soil [ 14 – 16 ]. Leaf litter is therefore part of a key mechanism of recycling and redistribution of nutrients. Litterfall quantification allows the potentiality as regards the degree of annual return of nutrients to the soil to be assessed. The quantity of litterfall will depend on different factors such as the genotype, the climatic factors such as temperature and light, fertility and degree of soil moisture, type of management or age of the plot, among others [17–20]. In plantations with fast-growing species, the leaf litter plays an important role within the nutrient cycle, allowing the replacement of a high percentage of mineral nutrients to the soil [ 21 – 24 ]. Soil fertility and nutrient recycling is one of the main concerns in relation to sustainability [ 25 ] and the assessment of forest plantations on agricultural soils is therefore pertinent. In the specific case of deciduous Populus spp., it is estimated that around 88% of N, 83% P and 78% K are returned through leaf litter in mature plantations [ 26 ]. Other authors, however, report lower return rates of between 20 and 40% and suggest that the rate depends highly on the genotype [ 27 ]. In general, nutrient cycling in poplar stands is considered efficient, with no significant loss of nutrients according to Meiresonne et al. [ 28 ] and returns via leaf litter are also often rich in basic cations [ 29 , 30 ]. Data on these nutrient returns in the specific case of poplar growing in short rotation coppice point to between 60–80% of the nutrients absorbed being returned annually through litterfall [ 31 ]. However, in SRC plantations with another fast-growing species such as eucalyptus, Guo et al. [ 32 ] reported rates of return of around 24% for N, although in this case it is an evergreen species. Leaf litter decomposition rate is also important for determining how nutrients enter the soil and will also determine the amount of organic matter which accumulates. This rate is controlled by both biotic and abiotic factors, with the chemical composition of the leaf litter (especially N and P concentration and C:N ratio) being one of the main influencing factors [ 33 – 35 ]. The variability of the chemical composition of the leaf litter will be determined, among other factors, by the efficiency of the reabsorption and relocation of nutrients at species level and by their interspecific variation [36]. Additionally, to quantify the contribution of SRC to carbon content it is necessary to determine the sources of variation in C concentration and to address potential sequestration in these farming systems [ 37 ]. In recent years, studies have pointed to the high potential contribution of plantations with fast-growing species to the global carbon budget [ 38 , 39 ]. Moreover, such plantations have been proposed as part of a strategy to mitigate global warming in the short term [40,41]. In forest plantations with fast-growing species, and specifically in the case of high density, short rotation plantations for biomass production, this evaluation is necessary not only to promote more sustainable management, but also in order to value the ecosystem services associated with them. Furthermore, it is necessary to evaluate the potential adverse effects on forest soils associated with the implementation of intensive plantations [ 42 – 44 ] on highly managed agricultural land, since these plantations are established on this type of land in many countries. Hence, the aims of this work are (i) to quantify the annual production of leaf litter and its composition in pure and mixed plots of high density, short rotation coppice (SRC) under Mediterranean conditions; and (ii) to determine the nutrient dynamics in this type of plantation and the potential impact on the soil. We hypothesized that mixed plantations improve the quality of the leaf litter with respect to monocultures, and consequently increase soil fertility. Forests 2020,11, 1133 3 of 19 2. Material and Methods 2.1. Study Area The experimental plantation is located in the center of the Iberian Peninsula (40 ◦ 28 0 N, 3 ◦ 22 0 W) at an elevation of 595 m, average mean temperature 15.3 ◦ C (mean absolute maximum 28.8 ◦ C and mean absolute minimum of 3.1 ◦C), with annual precipitation of 281 mm. The main edaphic features are detailed in Table 1. Table 1. Average values ± standard deviation of physical-chemical parameters and concentrations of assimilable Phosphorus and interchangeable elements (Potassium, Calcium, Magnesium and Sodium) on the surface horizon of the soil (0–30 cm). Parameters Before Plantation Texture Sandy-loam pH H2O 8.65 ±0.10 EC mS cm−10.59 ±0.24 Carbonates % 10.08 ±1.00 Ng kg−10.81 ±0.08 OM % 0.68 ±0.08 C:N 23.77 ±1.97 Pmg kg−1<4 Kcmol kg−10.30 ±0.05 Ca cmol kg−138.71 ±0.87 Mg cmol kg−14.71 ±0.44 Na cmol kg−10.73 ±0.30 Granulometric analysis was recorded by the Bouyoucus method; The pH and electrical conductivity (EC) was potentiometrically determined; Total nitrogen (N) was calculated according to Kjeldahl modified method; the soil organic matter (OM) was calculated by Walkley–Black method; carbonates was calculated according to Bernard calcimeter method; assimilable P was calculated according to Olsen; and the concentrations of exchangeable Ca, Mg, Na and K were determined by extracting with ammonium acetate (1N) and subsequently analyzing using ICP-OES (Optima 5300 DV, Perkin-Elmer, Massachusetts, MA, USA). The plantation was established in 2012 with the aim of evaluating biomass yield under different species compositions. Different mixing ratios of two fast-growing species were tested under a high-density (10,000 trees ha −1 , spacing 2.5 m × 0.40 m) short rotation coppice system. The two species were Populus alba L., genotype ‘111PK’, and Robinia pseudoacacia L., genotype ‘Nyirsegy’, and the trial included P. alba monoculture (PA), R. pseudoacacia monoculture (RP) and a mixture of both at a ratio of 50PA:50RP. The 50PA:50RP mix of both species was done tree by tree within the row and between rows. The figure design and the results of this research are described in Oliveira et al. [ 12 ]. The plantation was established using stem cuttings (unrooted in the case of P. alba and rooted for R. pseudoacacia) having followed the standard soil preparation procedure described for SRC plantations [ 45 ]. Since the Mediterranean climate is characterized by severe summer drought, the plantation was irrigated from June to September using a drip application system. No fertilization treatment was applied. The experimental design included three blocks, each containing the P. alba and R. pseudoacacia monocultures as well as the 50PA:50RP mix of both species. Each block and plot contained 64 trees in total. Further details on the experimental design are given in Oliveira et al. [12]. 2.2. Litterfall Collection Litterfall samples were collected from September to December in the 1st vegetative period of the 2nd rotation (R4S1, where R is the root age and S is the stool age), being the value of basal area of basal diameters (BA) and the height (H) of the species the following: the P. alba monoculture (BA =23.94 cm 2 and H =5.46 m); the R. pseudoacacia monoculture (BA =11.73 cm 2 and H =3.92 m) and the mix (BA =20.75 cm 2 and H =4.89 m for PA and BA =14.80 cm 2 and H =4.50 m for RP). Twelve litterfall traps (perforated plastic boxes with a surface area of 0.17 m 2 and a height of 23 cm) were randomly Forests 2020,11, 1133 4 of 19 placed in the rows of each block and plot and within the row, equidistant between two trees. The final number of traps was thirty-six. The monthly accumulated litterfall was taken to the laboratory where leaves were separated from the rest, which included twigs, bark, seeds, shoots, and other released components. The leaves were then dried at 65 ◦ C to constant weight and finally weighed. The leaf litter contribution in each subplot was calculated by adding the results for the different traps. The calculation per unit area was performed by dividing the sum of the total dry weight of the different fractions by the area of the trap, extrapolating the result obtained to one hectare. The unit to express the contribution of leaf litter is therefore mg ha−1yr−1in dry matter. Prior to the abscission of the leaf (end of August), when it was probable that the translocation of nutrients from the leaves to the reserve organs had not yet begun [ 2 , 46 ], fresh green leaves were collected from the trees in the same blocks and plots where the traps had been placed for further analysis. 2.3. Foliar Nutrient Analysis The following analyses were performed on both the green leaves and senescent leaves collected over 3 months: Total C and N by dry combustion using an elemental analyzer (CNS-2000, LECO, St Joseph, MI, USA); and P, K, Ca and Mg were determined by optical emission spectroscopy using ICP-OES (Optima 5300 DV, Perkin-Elmer, Massachusetts, MA, USA) after wet digestion of the sample with nitric acid in a closed microwave system (Ethos plus, Milestone, Sorisole, Italy). The percentage of nutrient resorption efficiency (NRE; hereafter retranslocation) between the two types of leaves (green and senescent) was calculated according to the following Equation [47]: NRE =(Nugreen −Nusenescent)/Nugreen ×100 (1) where Nu green is the nutrient concentration in the green leaf and Nu senescent is the concentration in senescent leaf. The nutrient use efficiency index was determined according to Vitousek [ 48 ], through the relationship between dry mass and nutrient concentration ratio of leaf litter. 2.4. Data Analysis A multivariate analysis of variance was performed to assess the effect of the treatments (plot type and sampling time) on leaf litter production and the chemical composition. A one-way ANOVA was performed when evaluating the effect of a single factor. Fisher’s Least Significant Difference (LSD) test was used to establish those means that are significantly different. A non-parametric analysis was performed when the assumptions of the one-way ANOVA test were not met, using the Kruskal–Wallis test in these cases. We worked with weighted annual averages according to weight fraction at subplot level when analyzing data related to leaf nutrients due to the variability in both concentration and input over the sampling period. The software package used was the R statistical program. 3. Results and Discussion 3.1. Leaf Litter Supply The most representative fraction of litterfall in all plots of the plantation (both monocultures and 50PA:50RP mixture) corresponded to leaves (around 98%); therefore, we will refer to this component from now on, with leaf litter being understood as all the leaves falling into the litterfall traps. However, according to Medina-Villar et al. [ 49 ], the leaf percentages for both species growing in the riparian ecosystem were lower (69%), probably because the litterfall trap contents comprised the entire annuity. Leaf detachment in deciduous species mainly takes place throughout the fall. Abscission can occur at any time during this period, depending on various factors such as weather and edaphic Forests 2020,11, 1133 5 of 19 conditions (water stress and soil fertility) but also on the species [ 50 ]. In our study, under the same soil and climate conditions, the maximum leaf litter values for the P. alba monoculture were reached in December, while leaf shedding in the R. pseudoacacia monoculture occurred earlier, reaching maximum values in October (Figure 1). This fact is in accordance with observed differences in phenology, as winter buds are formed earlier in R. pseudoacacia (early September) and later in P. alba (late October). This finding has previously been reported by Medina-Villar et al. [ 49 ] for natural stands in a study area proximate to that of the present study and supports previous findings by Gonz á lez-Muñoz et al. [ 51 ] and Castro-D í ez et al. [ 52 ]. Furthermore, it may be attributable to differences in the strategies for minimizing the energy expenditure required to keep tissues alive when the temperatures fall [53]. Forests 2020, 11, x FOR PEER REVIEW 5 of 20 Forests 2020, 11, x; doi: FOR PEER REVIEW www.mdpi.com/journal/forests conditions (water stress and soil fertility) but also on the species [50]. In our study, under the same soil and climate conditions, the maximum leaf litter values for the P. alba monoculture were reached in December, while leaf shedding in the R. pseudoacacia monoculture occurred earlier, reaching maximum values in October (Figure 1). This fact is in accordance with observed differences in phenology, as winter buds are formed earlier in R. pseudoacacia (early September) and later in P. alba (late October). This finding has previously been reported by Medina-Villar et al. [49] for natural stands in a study area proximate to that of the present study and supports previous findings by González-Muñoz et al. [51] and Castro-Díez et al. [52]. Furthermore, it may be attributable to differences in the strategies for minimizing the energy expenditure required to keep tissues alive when the temperatures fall [53]. Figure 1. Monthly contribution (mg ha−1 yr−1) of the leaf litter in the P. alba (PA) and R. pseudoacacia (RP) monocultures, and the 50PA:50RP mixture. Since a greater amount of the leaves in the total leaf litter of the mixture corresponded to P. alba (60 % PA to 40% RP) (Figure 2), and as this species sheds most of its leaves in December (82%), this was the month in which leaf litter in the mixture reached a maximum. Figure 2. Percentage contribution of P. alba (PA) and R. pseudoacacia (RP) to the total leaf litter of the 50PA:50RP mixture. Figure 1. Monthly contribution (mg ha −1 yr −1 ) of the leaf litter in the P. alba (PA) and R. pseudoacacia (RP) monocultures, and the 50PA:50RP mixture. Since a greater amount of the leaves in the total leaf litter of the mixture corresponded to P. alba (60 % PA to 40% RP) (Figure 2), and as this species sheds most of its leaves in December (82%), this was the month in which leaf litter in the mixture reached a maximum. Forests 2020, 11, x FOR PEER REVIEW 5 of 20 Forests 2020, 11, x; doi: FOR PEER REVIEW www.mdpi.com/journal/forests conditions (water stress and soil fertility) but also on the species [50]. In our study, under the same soil and climate conditions, the maximum leaf litter values for the P. alba monoculture were reached in December, while leaf shedding in the R. pseudoacacia monoculture occurred earlier, reaching maximum values in October (Figure 1). This fact is in accordance with observed differences in phenology, as winter buds are formed earlier in R. pseudoacacia (early September) and later in P. alba (late October). This finding has previously been reported by Medina-Villar et al. [49] for natural stands in a study area proximate to that of the present study and supports previous findings by González-Muñoz et al. [51] and Castro-Díez et al. [52]. Furthermore, it may be attributable to differences in the strategies for minimizing the energy expenditure required to keep tissues alive when the temperatures fall [53]. Figure 1. Monthly contribution (mg ha−1 yr−1) of the leaf litter in the P. alba (PA) and R. pseudoacacia (RP) monocultures, and the 50PA:50RP mixture. Since a greater amount of the leaves in the total leaf litter of the mixture corresponded to P. alba (60 % PA to 40% RP) (Figure 2), and as this species sheds most of its leaves in December (82%), this was the month in which leaf litter in the mixture reached a maximum. Figure 2. Percentage contribution of P. alba (PA) and R. pseudoacacia (RP) to the total leaf litter of the 50PA:50RP mixture. Figure 2. Percentage contribution of P. alba (PA) and R. pseudoacacia (RP) to the total leaf litter of the 50PA:50RP mixture. Forests 2020,11, 1133 6 of 19 The total leaf litter expressed in Mg per hectare in the different plots is shown in Table 2. Although the amounts of leaf litter among plots were not significantly different (p-value =0.2160), the annual inflow of leaves was more than 20% higher in the P. alba monoculture compared to R. pseudoacacia and the 50PA:50RP mixture. This trend contrasts with that described by Medina-Villar et al. [ 49 ], who reported greater leaf litter for R. pseudoacacia and pointed to generally higher growth rates due to the invasive character of this species compared to native species [ 51 , 52 ]. These conflicting findings may be due to the rapid growth rate of the P. alba genotype in our case compared to R. pseudoacacia over two rotations of 3 years [12,54,55]. Table 2. Leaf litter total annual weight in P. alba or R. pseudoacacia monocultures and 50PA:50RP mixture plantations. Plots Leaf Litterfall (mg ha−1yr−1) P. alba monoculture 3.37 ±0.79 50PA:50RP mixture 2.82 ±0.37 R. pseudoacacia monoculture 2.55 ±0.16 In contrast, the leaf litter production recorded in the P. alba monoculture (3.37 mg ha −1 yr −1 ) was similar to that obtained by Guenon et al. [ 56 ], who reported 3.1 mg ha −1 yr −1 in SRC plantations of Populus deltoides × P. nigra, although in that case the planting density was lower (7200 tree ha −1 ). However, other authors have reported higher values for the same species growing in SRC plantations (5.3 mg ha −1 yr −1 ) [ 57 ]. The amount of leaf litter was much lower for both species (0.77 mg ha −1 yr −1 in P. alba and 1.02 mg ha −1 yr −1 in R. pseudoacacia) in the riparian ecosystems described by Medina-Villar et al. [ 49 ], which is probably because of the lower tree density and the lower growth rate. The leaf litter in R. pseudoacacia plantations found by Tateno et al. [ 58 ] was around 3.8 mg ha −1 yr −1 , which is higher than the amounts obtained in the present study (2.55 mg ha −1 yr −1 ), despite having a lower planting density. In the mixed plantation, leaf litter accounted for 2.82 mg ha −1 yr −1 , with this value being between that of the two monocultures although closer to that for the R. pseudoacacia monoculture, despite the greater contribution P. alba leaves. 3.2. Foliar Nutrient Concentration and Retranslocation Rate in Green Leaves and Senescent Leaves 3.2.1. Macronutrients and C Leaf N concentration was significantly higher in green leaves compared to senescent leaves in all test plots (p-value =0.0002 for PA; p-value =0.0001 for 50PA:50RP and p-value =0.0004 for RP) (Figure 3). This result was expected, since nitrogen resorption from senescent leaves at the end of the growing season is a key function in plants [59]. In green leaves, the concentration of N did not differ significantly between the different plots (p-value =0.217). However, in absolute terms, the N concentration was higher in the R. pseudoacacia monoculture, the values for the mixed plantation being intermediate and the lowest values being those forP. alba, although stillgreater than25 gkg −1 , whichisconsidered thethresholdfor nutrient-demanding broadleaves [ 60 ]. A higher concentration of N in the green leaves of a P. deltoides L.—Alnus glutinosa (L). Gaertn mixture in comparison to the monoculture of P. deltoides was also observed by Koupar et al. [ 61 ]. The N efficiency index showed non-significant differences (p-value =0.0582), although a higher mean efficiency value was observed for P. alba (357.36) in relation to that of R. pseudoacacia (171.38). The 50PA:50RP mixture showed an intermediate ratio (240.27) that did not differ significantly from monocultures. The low efficiency of R. pseudoacacia, which may be attributable to its N 2 -fixing character, has been previously reported by González -Muñoz et al. [51]. The average concentration of N in senescent leaves was also significantly higher in the R. pseudoacacia monoculture and the 50PA:50RP mixture in comparison to the P. alba monoculture Forests 2020,11, 1133 7 of 19 (p-value =0.0258), with the 50PA:50RP mixture presenting intermediate concentrations (Figure 3). The concentrations detected in senescent leaves are in line with those described by Lee et al. [ 62 ] for R. pseudoacacia leaf litter (19.9 g kg −1 ), Cotrufo et al. [ 57 ] in relation to P. alba (9.6 g kg −1 ) or Das and Chaturvedi [ 26 ] for P. deltoides (11.4 g kg −1 ). Similar trends, although with notably higher concentrations, are mentioned by Medina-Villar et al. [ 49 ]. However, Koupar et al. [ 61 ] found higher concentrations of N in senescent leaves in mixed Populus and Alnus plantations than in their respective monocultures. Forests 2020, 11, x FOR PEER REVIEW 7 of 20 Forests 2020, 11, x; doi: FOR PEER REVIEW www.mdpi.com/journal/forests concentrations detected in senescent leaves are in line with those described by Lee et al. [62] for R. pseudoacacia leaf litter (19.9 g kg−1), Cotrufo et al. [57] in relation to P. alba (9.6 g kg−1) or Das and Chaturvedi [26] for P. deltoides (11.4 g kg−1). Similar trends, although with notably higher concentrations, are mentioned by Medina-Villar et al. [49]. However, Koupar et al. [61] found higher concentrations of N in senescent leaves in mixed Populus and Alnus plantations than in their respective monocultures. Similarly, in relation to P, the concentration in green leaves was significantly higher than in senescent leaves in all plots (p-value < 0.0001 for PA; p-value = 0.0091 for 50PA:50RP; and p-value = 0.0002 for RP) (Figure 3). In the case of green leaves (50PA:50RP mixture and monocultures) no significant differences among species were observed for P concentration (p-value = 0.6340), although absolute values were higher in P. alba. In senescent leaves, no significant differences were detected (p-value = 0.613), the highest concentrations corresponding to the 50PA:50RP mixture and the lowest to the R. pseudoacacia monoculture (Figure 3). There were no significant differences in P use efficiency (p-value = 0.2881), with P. alba presenting the highest absolute value (6801), followed by R. pseudoacacia (5585) and finally the mixed plantation (5078). Figure 3. Weighted annual averages according to weight fraction and their standard deviation for macronutrients and C in green and senescent leaves of P. alba (PA) and R. pseudoacacia (RP) monocultures and 50PA:50RP mixture. The significance between plot types for green leaves, and also for senescent leaves, is shown by letters; and the significance between green and senescent leaves within the same plot (PA, 50PA:50RP and RP respectively) is shown with asterisks. Both letters and asterisks are only shown when significant differences were found. In this study, the P concentrations in senescent leaves were lower than those detected in other studies. Lee et al. [62] obtained mean values of 0.63 g kg−1 in R. pseudoacacia or ranges from 1.14 g kg−1 to 1.37 g kg−1 in Populus spp. [26,63]. Figure 3. Weighted annual averages according to weight fraction and their standard deviation for macronutrients and C in green and senescent leaves of P. alba (PA) and R. pseudoacacia (RP) monocultures and 50PA:50RP mixture. The significance between plot types for green leaves, and also for senescent leaves, is shown by letters; and the significance between green and senescent leaves within the same plot (PA, 50PA:50RP and RP respectively) is shown with asterisks. Both letters and asterisks are only shown when significant differences were found. Similarly, inrelationto P,the concentrationin greenleaves wassignificantly higherthan insenescent leaves in all plots (p-value <0.0001 for PA; p-value =0.0091 for 50PA:50RP; and p-value =0.0002 for RP) (Figure 3). In the case of green leaves (50PA:50RP mixture and monocultures) no significant differences among species were observed for P concentration (p-value =0.6340), although absolute values were higher in P. alba. In senescent leaves, no significant differences were detected (p-value =0.613), the highest concentrations corresponding to the 50PA:50RP mixture and the lowest to the R. pseudoacacia monoculture (Figure 3). There wereno significantdifferencesin P use efficiency (p-value=0.2881), with P. alba presenting the highest absolute value (6801), followed by R. pseudoacacia (5585) and finally the mixed plantation (5078). In this study, the P concentrations in senescent leaves were lower than those detected in other studies. Lee et al. [ 62 ] obtained mean values of 0.63 g kg −1 in R. pseudoacacia or ranges from 1.14 g kg −1 to 1.37 g kg−1in Populus spp. [26,63]. Forests 2020,11, 1133 8 of 19 The stoichiometric N:P ratio in green leaves, widely used as an indicator of probable N:P deficiency, showed values above 16 in our study, which is the upper threshold identified by Aerts and Chapin [ 64 ] to indicate P deficiency, meaning that both species are far from displaying N deficiency. The leaves in our plots showed ratios close to normality in the P. alba monoculture (17.02). However, this proportion was 19.67 in the 50PA:50RP mixture and 21.34 in the case of the R. pseudoacacia monoculture, which could imply a progressive loss of fertility as regards P in these soils, since the leaf decomposition provides the main supply of this nutrient [65,66]. N 2 -fixing species such as R. pseudoacacia may have more demand for P than non-fixing species and this element may be the most limiting for its growth [ 62 ]. Cao and Chen [ 67 ] also reported that P was more limiting than N for mature R. pseudoacacia plantations. Regarding K concentration, even though the concentration in green leaves is always higher than that of senescent leaves in absolute terms, significant differences were only found in the R. pseudoacacia monoculture (p-value =0.0004) (Figure 3), whereas no significant differences were found in the P. alba monoculture (p-value =0.08) or the 50PA:50RP mixture (p-value =0.132). No significant differences were detected among the plots (monocultures and 50PA:50RP mixture) (green leaves: p-value =0.352; and senescent leaves: p-value =0.311). This may be because K is a highly mobile element, both in plants and in the soil [ 68 ], which is reflected in a high variability of the concentration detected in the leaves in all plots. K concentration in senescent leaves reported in the literature for Populus spp. ranges widely from 1.2 to 10.8 g kg −1 [ 26 , 27 , 63 , 69 , 70 ], the K concentration found in this study presenting intermediate values. Less information appears to be available for K concentration in senescent R. pseudoacacia leaves, although Lee et al. [62] report levels of around 10.97 g kg−1, which is more than twice our values. The greater difference in K detected between senescent and green leaves of R. pseudoacacia (7.22 mg g −1 ) in comparison to P. alba (3.77 mg g −1 ) could indicate greater importance of retranslocation as compared to recirculation via leaf litter. According to the literature, the optimal range of NPK in green leaves for Populus species is 17–30 g kg −1 for N, 1.0–4.4 g kg −1 for P and 7–20 g kg −1 for K [ 71 – 76 ]. Narrower optimal ranges are established for site-demanding broadleaved [ 60 ] and more specifically for Populus [ 77 ] species, with 18–25 g kg −1 for N, 1.8–3.0 g kg −1 for P and 12–20 g kg −1 for K. The concentrations of N obtained in the green leaves of all our plots were above the optimal range, while in the case of P, they were very close to the lower limit. In the case of K, the levels indicate deficiency. Sardans et al. [ 78 ] found green-leaf NPK ranges for P. alba at 41 different study points of 26.8–31.2, 1.96–2.08 and 4.8–26.5 g kg −1 respectively. The values for the P. alba monoculture plots were within this range for N and K in our study, although in the case of P, the concentrations were lower. The green-leaf NPK concentration reported by Ozbucak et al. [ 36 ] for R. pseudoacacia ranged from 20.0–44.2, 0.60–2.47 and 2.1–12 g kg −1 , the concentrations detected in our plots being within these ranges. For the same species, Sardans et al. [ 78 ] reported N and P ranges within those defined by Ozbucak et al. [ 36 ] (35.2–44.2 and 1.94–2.48 g kg −1 , respectively), although much higher for K (14.3–20.1 g kg −1 ), the values obtained in this study being below those ranges for P and K, and very close to the lower limit in the case of N. However, if we take into account the ranges for optimum nutrition of demanding broadleaves [ 60 , 77 ], the concentrations obtained in this study for R. pseudoacacia are below the critical levels for P and K. In contrast, in the case of N, the concentrations obtained were above the optimal range, as expected, since R. pseudoacacia is an N2-fixing species. The low concentrations of K obtained in green leaves in this study could be due to the antagonistic relationship between Ca and K, given the high concentrations of interchangeable Ca in the soil (38.71 cmol kg −1 ) (Table 1). This could cause less absorption of K by the plant due to a lower presence of this element in the soil solution as both elements compete for plasma membrane absorption sites [ 77 , 79 ]. As regards Ca, the absolute values of the mean concentrations were higher in senescent leaves than in green leaves in the monocultures. However, the differences between the two types of leaves were only significant in the 50PA:50RP mixture (p-value =0.0877 for PA; p-value =0.0018 for 50PA:50RP Forests 2020,11, 1133 9 of 19 and p-value =0.263 for RP) (Figure 3), which would indicate that a greater amount of Ca is returned to the soil in the mixed plot in comparison to the monocultures plots. This finding is consistent with that of Sayyad et al. [ 80 ] in pure and mixed stands of Populus deltoides and Alnus subcordata. The increase in the concentration in the senescent leaf is due to the low mobility of Ca, which is not an element retranslocated by plants. This low mobility causes Ca to be immobilized once assimilated, accumulating in structural components of the leaf such as membranes, cell walls and vacuoles [ 77 ]. Tzvetkova and Petkova [ 81 ] also found that Ca concentrations for R. pseudoacacia increased in the leaves that fall later. In senescent leaves, no significant differences were observed between the different plots (both monocultures and the mixture) (p-value =0.287), while significant differences were found in green leaves between the R. pseudoacacia monoculture and both the P. alba monoculture and the mixture (p-value =0.0017). Although no significant differences were detected in the Ca use-efficiency index (p-value =0.1479), higher values were observed in the P. alba monoculture (132.87) than in the R. pseudoacacia monoculture (71.06), with mixed plots presenting an intermediate value (87.18). In the case of Mg, as for Ca, the concentrations in absolute values were higher in senescent leaves than in green leaves for the P. alba monoculture and 50PA:50RP plots, these differences being significant for the mixture (p-value =0.538 for PA and p-value =0.0378 for 50PA:50PR) (Figure 3). However, in the R. pseudoacacia monoculture, despite no significant differences being detected (p-value =0.437), the mean concentration of Mg was slightly higher in green leaves than in senescent leaves. This may be because Mg is an element with partial mobility, which, in addition to its involvement in photosynthesis, is a cofactor of numerous enzymatic activities, among which is the nitrogenase activity involved in the fixation of N 2 [ 82 ], and therefore this N 2 -fixing species, with a higher photosynthetic activity [ 83 ], may have a greater requirement for this element. Sayyad et al. [ 80 ] found no significant differences in Mg concentrations between green and senescent leaves for the monoculture and Populus and Alnus mixture plantations. However, in R. pseudoacacia plantations, Tzvetkova and Petkova [ 81 ] observed a slight decrease in Mg concentrations in leaves that fall later, in agreement with our findings (from 5.15 g kg−1in October to 2.37 g kg−1in December). No significant differences were found in the concentration of Mg between the different plots either for green leaves (p-value =0.390) or senescent leaves (p-value =0.132), although in terms of absolute values, the mean concentration of Mg was lower in the senescent leaves in the R. pseudoacacia monoculture. As in this study, Sayyad et al. [ 80 ] found lower Mg concentrations, both in green and senescent leaves in the N2-fixing species. Harvey and Van den Driessche [ 63 ] also reported higher concentrations of Ca and Mg in senescent leaves than in green leaves for Populus (15.80 and 4.78 g kg −1 vs. 9.65 and 3.14 g kg −1 ), these concentrations being lower than those obtained in this study. Lagani è re et al. [ 70 ] and Yanai et al. [ 69 ] found ranges of between 10.8 and 18.9 g kg −1 for Ca and between 1.8 and 2.7 g kg −1 for Mg in senescent leaves of Populus, both of which are lower than the amounts found in this study. In the case of green leaves, Sardans et al. [ 78 ] reported a range of between 21.3–48.5 g kg −1 for Ca and between 1.9–7.2 g kg −1 for Mg in P. alba and Mart í n-Garc í a et al. [ 84 ] reported values for the ‘I-214’ genotype of more than 26.4 g kg −1 for Ca and lower than 3.6 g kg −1 for Mg. However, Elferjani [ 85 ] reported values for hybrid poplar genotypes of between 7.9–12 g kg −1 for Ca and 2.0–2.8 g kg −1 for Mg, these values again being lower than those obtained in this study. According to the literature, the optimal Ca and Mg in green leaves of Populus species ranges from 3–17 g kg −1 for Ca and 1.4–4.0 g kg −1 for Mg [ 71 – 76 ]. However, Bergmann [ 77 ] established narrower optimal ranges for Populus of 3–15 g kg −1 for Ca and of 2.0–3.0 g kg −1 for Mg. Hence, our Ca values for Populus are at the upper limit of the optimal range and above the optimal range in the case of Mg. As regards R. pseudoacacia, Sardans et al. 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