Trees modify the physico-chemical and biological properties of the soil underneath. Here we present results for seven tree species planted at a site that was contaminated by a mine spill – after which soil was cleaned up and remediated – and later was afforested. We studied the chemical composition (24 elements) in five ecosystem compartments (leaves, forest floor, roots, topsoil and deep soil). The variation in chemical concentration was highest at the level of canopy leaves and lowest at deep soil. The identity of tree species significantly affected the composition of all elements in the canopies but none in the deep soil underneath. Although the observed tree effects on topsoil chemistry were weak, the footprint is expected to be reinforced with age of the plantation, contributing to the phytostabilization of contaminating elements and to the carbon sequestration.
Trees are ecosystem engineers, modifying soil physico-chemical properties, nutrient cycling and microbial communities (Vesterdal and Raulund-Rasmussen, 1998; Aponte et al., 2011, 2013). The behaviour of different elements in the afforested biogeochemical landscape will depend on their sources, their chemical bonding properties and their degree of biological control (Ladanai et al., 2010).
Chemical composition of forest superficial soil is influenced mainly by leaf-fall quality, but also by atmospheric deposition, leaching and root exudates (Aponte et al., 2011). In contaminated soils, the potentially toxic elements can be partially immobilized by afforestation; this soil remediation measure is known as “phytostabilization” (Bolan et al., 2011).
The Guadiamar Green Corridor (SW Spain) is a large-scale example of phytostabilization. After a mine spill (in 1998) that contaminated about 4000 ha, soil was cleaned up and remediated, and later the site was afforested with several native shrub and tree species (Domínguez et al., 2008). In this study we explored the chemical composition of five ecosystem compartments in the established mixed forest: canopy leaves, forest floor, tree roots, topsoil and deep soil.
The objectives were to characterize the chemical heterogeneity at canopy level, originated by planting different tree species, and to evaluate the strength of their footprint on soil properties, 16 years after plantation. Specific questions were, what was the rank of variability among chemical elements by compartment? What was the mean chemical variability by ecosystem compartment? Was there a significant difference among tree species for every chemical element by ecosystem compartment? In particular, was there a significant tree-species effect on soil?
Variability of the concentration of 23 chemical elements in five ecosystem compartments: mean, maximum and minimum values of CV. Tree-species effect indicated by the number of chemical elements showing significant variability due to tree-species identity, according to the ANOVA or Kruskal–Wallis results.
The study area was the Guadiamar Green Corridor (Sevilla, Spain). Its climate is
Mediterranean, with mild rainy winters and warm dry summers. Average
annual temperature is 19
Soil properties within the plot were similar before afforestation, and
therefore we could infer tree effects in this common garden experiment. Soil
was Fluvisol type, had a loamy texture (42 % sand and 19 % clay),
was acidic (pH about 4), and was nutrient-poor (0.07 % N, 8 mg kg
Samples of the three plant materials and two soil layers were processed and analysed for the composition of 22 chemical elements (Al, As, B, Ba, Ca, Cd, Co, Cr, Cu, Fe, K, Li, Mg, Mn, Na, Ni, P, Pb, S, Sr, V, Zn) by inductively coupled plasma optical emission spectrometry (ICP-OES), and of C and N by elemental analysis (see general methods in Madejón et al., 2006; Domínguez et al, 2008). A total of 23 elements were considered for plant materials (Li was under detectable levels in plants) and also 23 for soil samples (B was under detectable levels in soils).
The variability in the concentration of each chemical element by ecosystem level was measured by the coefficient of variation (CV). Elements under biological control were expected to have lower variability in plant compartments than in soil (Ladanai et al., 2010). Global chemical heterogeneity at each ecosystem level was evaluated as the mean CV of the 23 measured elements by compartment. We expected higher heterogeneity at superficial soil (more affected by leaf-fall) than at deeper soil.
The source of variation due to the tree species was tested by analysis of
variance (one-way ANOVA) for each chemical element and ecosystem
compartment. Previously data were tested for normality (Shapiro–Wilk
test) and homoscedasticity (Levene test) and log-transformed if necessary.
Alternatively a non-parametric Kruskal–Wallis test was applied. In addition
to the global comparison, the chemical composition of topsoil under
contrasted tree species was compared by pair-wise Student's
Tree canopies had the highest variability in the concentration of 23 elements; the mean CV was 79 % (Table 1). Elements with the lowest CV values were C (7 %), N (20 %) and K (26 %), in general those under higher biological control. The highest variability was shown by Cd (226 %), Zn (158 %), V (126 %) and Mn (123 %), non-limiting elements, which excess uptake was poorly regulated (Ladanai et al., 2010).
The identity of tree species was a major source of variation for the
concentration of all the 23 elements in leaves (Table 1). The presence of
accumulator species explained the high variability of certain elements. For
example, the higher accumulation of Cd and Zn in leaves of
The mass accumulated under the tree canopy was the net result of litter production and decomposition, and its chemical composition would reflect both litterfall and decomposers (Vesterdal and Raulund-Rasmussen, 1998; Ladanai et al., 2010). The forest floor heterogeneity was high (mean CV of 65 %). Minimum CV value was found for C (12 %) and Mg (20 %), whereas the maximum variability was presented by non-essential elements Cd (130 %), As (100 %) and Pb (98 %).
Forest floor mirrored the chemical patterns of the canopy, with peaks of Cd
and Zn under
The average variability of root chemical composition was also high (mean CV of 62 %), with the minimum CV value for C (7 %) and P (30 %), those elements under higher biological control. In contrast, the non-essential elements Cr (135 %), As (94 %) and Pb (91 %) presented the highest variability in roots.
Bivariate diagram of the concentration of Cd and S (log scale) in
the superficial soil under the 35 trees of 7 species. For illustrative
purpose two contrasted species,
Roots had also a characteristic tree-species signal with significant
among-species variance for 22 out of 23 elements (Table 1). However, the
pattern was quite different from leaves; for example, there was no
significantly higher accumulation of Cd and Zn in
The heterogeneity of chemical concentration of 23 elements in topsoil was lower than in the three plant compartments; the mean CV was 25 % (Table 1). Elements presenting lowest variability were V (12 %), P (13 %) and Fe (13 %), whereas the highest values were found for S (86 %), Pb (41 %) and As (36 %). Forest soil heterogeneity is originated by changes in soil-forming factors, management and stochastic variation (Quilchano et al., 2008).
Tree-species identity was the source of significant difference for only
three elements (Cd, Co and Li) in topsoil. Despite the strong differences
in chemical composition of leaves and roots among tree species the chemical
footprint in the topsoil was weak. However, contrasted species had
significant pair-wise differences in the soil underneath (detected by
Student's
Probably the elapsed time (16 years) was not enough to detect a significant and strong tree signal in the soil. In a review of 70 studies Li et al. (2012) found that age after plantation was a major factor explaining the dynamics of soil C (significantly increased after 30 years) and N (significant after 50 years).
The chemical composition of deeper soil (10–30 cm) was even less heterogeneous; mean CV was 22 %. The least variable elements were Cu (11 %), P (12 %) and V (12 %), whereas the highest heterogeneity was presented by S (65 %), Na (37 %) and Cd (34 %). There was no significant effect of the species of tree planted aboveground for any chemical element in that deeper horizon (Table 1). In general, the tree effects on soil nutrients tend to disappear with depth, and subsoil features are frequently used as proxy of the original soil conditions (Aponte et al., 2013).
In conclusion, the chemical footprint in the soil by the seven tree species was still weak, partly due to their young age (only 16 years after plantation). However, those trees planted in a contaminated and remediated soil are contributing effectively to the phytostabilization of trace elements by their immobilization in roots and organic matter, and to the carbon sequestration in biomass and soil, thus providing valuable ecosystem services.
Thanks to J. M. Alegre for helping during sampling and to P. Burgos for chemical analyses. The research leading to these results has received funding from the European Union Seventh Framework Programme (FP7/2007–2013) under grant agreement no. 603498 (RECARE) and from the Spanish RESTECO (CGL2014-52858-R) project. Edited by: D. Montesinos Reviewed by: two anonymous referees