1. Introduction
Land use and land management are some of the most important factors that influence soil key properties and the environment [
1,
2,
3]. The recent years have seen dynamic changes in the use of agricultural land. They mainly concern transformation of farmland for abandonment land [
4,
5]. The definition of term “agricultural land abandonment” refers to land that has not been used for a minimum of two to five years, which means total cessation of agricultural activities [
6,
7]. Agricultural land abandonment is a common process in parts of North America and Europe [
8]. This process can be triggered a combination of socio-economic, political factors, farm structure, agricultural viability, and constraints to the natural environment [
5,
9]. The European Commission denote an alarming trend concerning that, in the period 2015–2030, about 11% (more than 20 million ha) of agricultural land in the EU can be at potential risk of abandonment, bringing the total abandoned land to 5.6 million ha by 2030, the equivalent of 3% of the total agricultural land [
10]. Bell (2020) [
11] suggested strategies that can be applied in the process of abandoned land management. These strategies underline, i.e., the importance of the multi-functionality of agriculture and renewable energy sources, including bio-energy crops. The multifunctionality of agriculture is an essential condition for sustainable development. In addition, the multifunctionality of agriculture is understood as the phenomenon that, in addition to the basic function of agriculture, which is the production of food products and other organic raw materials, generates additional income through the production of goods other than those traditionally associated with agricultural production [
12,
13,
14]. The attractive strategy for farmers is recultivating abandoned agricultural lands, especially where biophysical conditions are favourable, and transforming them into sustainable and multifunctional bioenergy crops, assuring climate change mitigation, energy security, and increased economic opportunities [
8,
15]. In this regard, the cultivation of bioenergy trees/short rotation forestry have received great interest as a potential alternative to agri-food production, guiding the world towards a sustainable and circular bioeconomy [
16,
17,
18]. However, soil quality indicators, such as microbial and metabolic parameters, have been less studied in the assessment of soil response to reclamation of land abandonment.
Short rotation forestry (SRF) does not compete with traditional crops for the most productive agricultural land because they are usually cultivated on lower-class agricultural land, reclaimed land, previously uncultivated land, or land that had been abandoned [
19]. The genus
Paulownia contains fast-growing varieties of deciduous trees, which belong to the Paulowniaceae family.
Paulownia spp. grows on different types of soil, as well as degraded soils [
20,
21]. However, the most appropriate soils are those that are loose and permeable, with a pH ranging from 5 to 8 [
21,
22].
The microbial activity is important for plant growth and development in natural ecosystems [
23,
24]. In forest ecosystems, trees influence the metabolism and structure of soil microorganisms through root secretions and leaf litter fall [
25,
26]; however, they also directly affect the chemical and physical properties of soil [
27]. Microbiological activity is a significant element of soil quality. All disturbances and changes in environmental ecosystems are reflected by changes in the diversity and metabolic activity of microorganisms, with changes in both their distribution and nutrients intake [
28]. Microbiological parameters that are widely used in the analysis of the soil environment status are represented by community level physiological profiles (CLPP) [
29,
30] and enzymatic activity [
30,
31], as well as microbial biomass C and N [
31,
32,
33]. The EcoPlate test contains 31 of the most useful carbon sources for microbial community analysis [
34], enabling for community-level physiological profiling (CLPP) of microorganisms. This method for the analysis of environmental samples was proposed by Garland and Mils [
35]. In addition, Lehman et al. [
36] confirmed that the selected set of compounds is appropriate for the characterisation of soil in terms of their metabolism. The population of microorganisms gives a characteristic response pattern called a metabolic fingerprint [
29]. However, Ros et al. (2008) [
37] argue that the Biolog test does not reflect the functional capacities of the all microorganisms in the sample, but only reflects the capacities of a limited subset of the microbial community. The use of single biological parameters when assessing soil condition is burdened with many limitations. It is therefore recommended that the results of analysis are developed based on the group of parameters, for example, the Biolog EcoPlates technique with the assessment of enzymatic activity and microbial biomass [
38].
Land-use transition from agricultural to bioenergy crops has become increasingly common in Europe. However, we have a poor understanding of the effect of these land conversions on soil quality attributes on abandoned land. There were previously such studies, but they were based on different plant species and performed on arable land. Most ecological studies have focused on regions of America and tree taxa, i.e., poplar and willow [
39,
40,
41]. The information about microbiological properties of soil in
Paulownia plantations is limited. Only a few studies on this subject have been done in Europe, especially concerning the long-term research of the microbial properties of soil in
Paulownia plantations [
42,
43,
44]. Analysing the biological soil quality, it becomes important to understand the diversity, activity, and functioning of microbial communities, as well the need to protect edaphic species of microorganisms [
43,
45]. Thus far, less attention has been given to assessing microbiological indicators of soil quality in bioenergy crops on abandoned land.
The aim of the study was to assess the potential of Paulownia bioenergy crops, which is applicable in multifunctional agriculture for the reclamation and redevelopment of abandoned lands. Therefore, this research explored the responses and changes of the activity of three soil enzymes (acid and alkaline phosphatase, dehydrogenases), microbial biomass, and functional diversity in two soils under plantations of Paulownia elongata × Paulownia fortunei in a temperate climate in Poland established on abandoned lands, taking into account sampling date and distance from the tree, in order to identify the actual status and the future prospects for this type of land transformation.
4. Discussion
Abandoned and marginal lands are considered a promising strategy for producing biomass (Short rotation plantations) and avoiding conflicts with food production. Abandoned land is a land lower in agricultural value and mostly less profitable for agricultural production. Thus, fast growing plants (including
Paulownia sp.) on unused plots constitute an economically interesting option for farmers. In Eastern Europe, land abandonment is common process [
55,
56]. Therefore, this study focused on the region in central Poland (a country facing worrying abandoned land trends), which, due to the occurrence of
Paulownia plantations (bioenergy crops), was appropriate for our research [
10].
Land use change can transform key soil properties, influencing the capacity of soil to maintain ecological functions. Providing an evidence base of the impacts of Paulownia sp. on microbiological activity of soils is an important element in understanding the sustainability of these bioenergy crops and their potential for reclaiming abandoned land.
The microbiological properties of soil in SRF are important, particularly in the context of soil biodiversity and protection against the loss of its quality. SRF is expected to have a positive effect on biodiversity [
57,
58], as well as on soil [
59]. Microorganisms are the major factors of biological and biochemical processes in the soil. They are much more sensitive than physiochemical factors to changes in the soil ecosystem, and therefore, they are excellent indicators of agricultural sustainability [
60]. Porta et al. [
41] found little variation in physicochemical properties because the parental rock material, climatic conditions and geomorphology were very similar in the studied area. Therefore, in this study, we analysed several microbiological and biochemical properties. An evaluation of soil microbiological properties under
P. elongata ×
P. fortunei trees was important to understand the role of microbes and its biodiversity in soil.
The soils of P. P. elongata × P. fortunei plantations from Podkampinos and Otrębusy differed in their chemical properties and textures. The soil from Podkampinos was a sandy loam, whereas that from Otrębusy was loamy sand. The selected plots are characterised by favourable conditions for plant growth. However, for economic and social reasons, these plots were abandoned. On these soils of relatively high fertility, the Paulownia tree may produce more green biomass.
Acosta-Martınez et al. [
61] reported that soil physicochemical properties, such as pH, organic matter, and texture, could influence soil enzyme activities, which provides information on biological activity and the maintenance of soil fertility. The overall microbial properties were closely related to the soil physiochemical properties, which showed better values in loamy sand soil. These changes could be attributed to the content of nutrient elements. The loamy sand soil had higher values of parameters such as nitrogen as nitrates (N-NO
3), TON, TOC, exchangeable Ca, and the level of humus than soil from Podkampinos. However, it had lower values for nitrogen as ammonium compounds (N-NH
4) and exchangeable K (
Table 2). Das et al. [
62] showed that the amount of soil microorganisms exhibited positive correlation with the available K
+, as well as the exchangeable Ca
2+ and Mg
2+ of soil, which is confirmed by our research. The better microbiological activity, assessed by various methods, was shown in the loamy sand texture soil with a higher content of exchangeable Ca
2+ and Mg
2+. Consistent to our finding, Liu et al. [
63] found that the soil microbes in agroforestry systems are shaped by soil physiochemical properties. Pang’s [
64] findings suggest that soil microbial functional diversity, evaluated on Biolog EcoPlates, is governed by soil physicochemical properties in subtropical forests.
Moreover, among soil attributes, pH is considered the main variable of soil. It influences microorganisms, thereby determining plant growth and biomass yield [
65]. The values of the soil pH recorded for both soil textures (sandy loam and loamy sand) were slightly acidic. Hinsinger et al. [
66] and Hagen-Thorn et al. [
67] showed that the roots of trees acidified the soil through the release of acidic compounds and microbial respiration. Moreover, Khan et al. [
68] found that several physicochemical properties of the soil in plantations of
Robinia pseudoacacia, e.g., pH, were modified through the decomposition of leaves. The slightly lower pH was noted for the sandy loam soil, which may be reflected in the different microbial activity. Xu et al. [
69] emphasised that pH and soil texture exerted a significant impact on microbial community structure. Similarly, Rousk et al. [
70] investigated the influence of pH on the microorganisms in soil, and this study showed that higher values of pH favoured microorganism growth.
It has been reported that growth of tree species affects the physicochemical and biological properties of soils [
25,
26,
27,
71]. Thus, the structure, diversity, and metabolic activity of soil microorganisms are dependent on the tree species [
72]. In general, a relationship between parameters (MBC, MBN, DHA, AcP activities, and the metabolic diversity of microorganisms) was observed. Soil enzyme activities and parameters used to describe microbial functional diversity were generally higher at the tree row than at the middle of the alley. The increased activity abundance of soil microorganisms in the nearest tree of the agroforestry systems corroborated previous findings of trends of the amount of bacteria in the Canadian agroforestry systems [
73]. Similarly, Mungai et al. [
74] studies indicated that microbiological activity expressed as AWCD, substrate richness, and the Shannon diversity index are positively linked with distance from the analysed plants, whereas these parameters are higher in the tree row. The observed trend may indicate the existence of metabolically and functionally different microorganisms at the two distances of 0.1 m and 1 m. These changes could be attributed to reserves of nutrients in the soil that come from leaves incorporated into the soil. In close proximity to the tree stem, there is more leaf residue and root secretions, and hence, there is higher microbiological activity. The higher biological activities in the soil near the tree can be due to an increased supply of carbon and nutrients from litter, dead root cells, and rhizo- depositions [
75,
76]. Yadav et al. [
76] have also recorded higher dehydrogenase activity under trees. Similarly, Wan and Chen [
77] observed higher microbial activities under trees, probably resulting from the increased content of carbon, nutrients, leaf residues, and root secretions in the soil. Decomposition processes of leaf residue and root secretions are the result of the most active microorganisms, whose main goal is to obtain nutrients. The high content of organic compounds in the substrate contributes to a significant increase in the number of microorganisms and changes in their structure, thus improving the soil microbial activity [
78,
79,
80]. Furthermore, these microorganisms can have a beneficial effects on plant productivity and also agroecosystem stability [
80].
In the current study, much higher microbiological activity and metabolic diversity were observed in the October (autumn period) in both soil textures, which could be associated with the large amount of abscised leaves and the climatic conditions, such as high humidity. Notably, leaves of
Paulownia spp. contain many nutrients, such as nitrogen, phosphorus, and potassium, and, in China, they are used as a green fertilizer [
77,
81]. Wang and Shogren [
82] confirmed that leaves of
Paulownia spp. could be a valuable source of organic matter and nutrients. In addition, they emphasised the potential of autumn leaves. Plant phenology and photosynthetic activities affect seasonal dynamics of microorganisms because plants influence C and N availability for soil microorganisms as a result of the exudation of labile C through the roots and the substrate input by litter fall [
83]. Plant root exudates provide labile carbon in summer, while winter microorganisms use dead plant material [
84,
85,
86] and microbial cellular products [
87]. At the end of summer, when the plants join the aging phase, microorganisms have access to easily available plant litter and show less competition for nutrients and minerals [
84,
86,
88]. The results of our study are consistent with the results of Mungai et al. [
74] from a 21-year-old pecan (
Carya illinoinensis) and a 12-year-old silver maple (
Acer saccharinum), and Koranda et al. [
89] from a
Fagus sylvatica as well as Bini et al. [
90] from mixed plantations of
Eucalyptus grandis and
Acacia mangiu. In the autumn period, higher MCB values were observed for Mixed Middle—Aged, Deciduous Young, and Deciduous Mature forests than in the summer period. However, dehydrogenase activity was higher in the autumn for Coniferous Young and Mixed Mature. The seasonal dynamics of the metabolic activity of microorganisms and soil biological activity are a frequently observed phenomenon [
91,
92,
93]. Understanding the seasonal dynamics (intra-annual) of soil microbial communities and their activity is very important for improving the ecosystem management policy and can help us clarify the drivers of community stability and ecosystem functioning [
91,
94].
Chauhan et al. [
95] emphasised that SRF has an enormous potential in maintaining physical, chemical, and biological properties of the soil, e.g., enhanced productivity, nutrient recycling, erosion control, and reclamation of problematic/degraded land. In the research of Swamy et al. [
96], Singh and Sharma [
97], and Gupta et al. [
98], they revealed significant improvements in available nitrogen, phosphorus, potassium, and organic carbon content in soil under agroforestry plantations. Turley et al. [
99] indicated that the restoration of abandoned land increased bacterial diversity by 13.8% and fungal diversity by 60.1%. Xu et al.’s [
100] results indicate that recovery after cropland abandonment causes an increase in microbial activity in the soil and depends on plant characteristics and soil physicochemical parameters. Therefore, it is so important to choose a suitable plant species. Our study presents the status of microbial activity in soil under
Paulownia plantations, considering variability of date and distance of sampling. This research emphasised the importance of fast-growing
Paulownia as a plant with great potential to reclaim the abandoned land due to the improvement of the soil enzyme activities, microbial biomass, and metabolic diversity of microorganisms. Overall,
Paulownia crops can be ecologically and economically profitable as an alternative to agri-food productions and as renewable energy sources.