Introduction

Giant reed (Arundo donax L.) is a perennial grass that reproduces by producing large fleshy rhizomes (from 5 to 50 cm in length) under the soil surface [1]. Under Mediterranean conditions, giant reed can grow well and produce high and stable yields of dry biomass (38 t ha−1 year−1), although results vary depending on the exact location [2]. Perennial grasses such as giant reed have the capacity to store both nutrient and carbohydrates, which allows them to start the growth process early and survive under unfavorable circumstances [3]. The fibrous roots originating from the rhizomes are able to grow into the soil to 5 m in depth, supporting stems that can reach more than 8 m in height under optimal growth conditions [4], with growth rates ranging from 4 to 7 cm per day [4, 5]. Even though giant reed is a C3 plant, it shows high photosynthetic rates and unsaturated photosynthetic potential compared to C4 plants [6]. Giant reed is able to grow in a very wide range of soils, including apparently inhospitable and marginal land, sites of high moisture, salinity, and pH, even though the best growth are obtained in well irrigated, well-drained soils [5, 7]. Giant reed is widely cultivated as a non-food crop [6] that can meet requirements for energy, paper pulp production, biofuels, and construction of building materials, but it is also used for musical instruments, medicine, and soil erosion control through re-vegetation [8]. However, as giant reed does not produce fertile, viable seed outside its original home range in south Asia, its only weed risk is by the spreading of vegetative parts in flood-prone riparian zones. In that context, Arundo donax can be controlled mechanically [9], herbicide treatments [9], and/or combination of the previous (Team Arundo del Norte 2007, http://www.ceres.ca.gov/tadn/) and can be confined to plots of specific size; therefore fear of invasiveness should not be a barrier to its usage [10, 11].

Bushfires are uncontrolled fires occurring in the rural landscape. Fire is a major landscape-scale perturbation in many ecosystems throughout the world, but it is especially frequent in the tropical climate. Nevertheless, its cumulative effect has a major impact on the ecosystem functioning. During the last two decades, bushfires have been identified as one of the causes of the decline in soil fertility. Fire is the most devastating factor contributing to loss of vegetation, nutrients, and especially to natural resource degradation [12]. During biomass combustion, nutrients can be volatilized or transferred to the atmosphere as particulate matter. The particles are likely to be deposited on or near the site of fire, but this is not the case for volatile elements such as carbon and nitrogen [13].

The refining of bauxite to alumina through the Bayer process results in the production of a large quantity of a solid waste called “red sludge” or more euphemistically “red mud” (the production of 1 t of alumina generally results in the creation of 0.5–2.5 t of red mud) [7]. Bauxite residues are strongly alkaline and have a high salt content and electrical conductivity (EC), dominated by sodium (Na+). Its constituent particles are compacted upon drying imparting a high-bulk density, and the trace metal content of red mud depends on the source of the bauxite from which the alumina was refined. Red mud contains toxic metals such as arsenic, chromium, cadmium, and nickel [14]. On the other hand, some articles documented the possibility of using red mud as soil amendment to reduce the concentration of heavy metal ions in both weakly and severely polluted soils with heavy metals [15–17]. Snars et al. [18] reported that adding red mud to agricultural soil reduced available P by up to 60 %. The increase of soil pH by adding red mud might increase pasture growth which can be limited by acidity on these soils. The increase of EC is not sufficient to adversely affect crop growth. Thus, addition of red mud to these soils is therefore likely to be beneficial and there is a much smaller effect of red mud on extractable P than that reported in studies where fresh P was added to the soils.

Soil quality or soil health, refers to the capacity of soil to perform agronomic and environmental functions. Changes in soil quality, resulting from, for example, bush fires or the presence of waste residues from bauxite mining (through the Bayer process) can be measured through physical, chemical, and biological indicators. The chemical indicators include pH, EC, soil organic carbon (SOC), phosphorus availability, nutrient cycling, and the presence of contaminants such as heavy metals, organic compounds, and radioactive substances. These indicators determine the presence of soil–plant-related organisms and nutrient availability [19]. SOC is an important indicator of soil quality; it has positive effects on soil physical properties and promotes water infiltration, storage, and drainage [5], and is directly related to the maintenance of soil structure, presence of different groups of microorganisms, mineralization of organic matter, and nutrient availability. The biological indicators that have been widely studied are the chemical compounds or metabolic products of organisms, particularly enzymes such as cellulases, arylsulfatase, phosphatases, urease, and dehydrogenase related to specific functions of substrate degradation or mineralization of organic N, S, or P. Soil enzymatic activity assays act as potential indicators of ecosystem quality being operationally practical, sensitive, integrative, described as “biological fingerprints” of past soil management that relate to soil tillage and structure [20]. Microorganisms are also widely used as soil quality indicators. Soil contains a large variety of microbial taxa with a wide diversity of metabolic activities [21]. Soil microbial biomass is a sensitive indicator of soil health and is influenced by different ecological factors like plant diversity, soil organic matter content, moisture, and climate changes. Microorganisms play a key role in nutrient cycling and energy flow. Microbial communities respond to environmental stress or ecosystem disturbance, affecting the availability of energetic compounds that support microbial population [22].

Our previous research work investigated the remediation capacity of giant reed on bauxite-derived red mud-contaminated soil [7]. The results showed that the giant reed is able to remediate not only red mud-contaminated soils but also pure red mud. According to other articles which reported the possibility of using red mud as soil amendment, we aimed in this paper to (1) investigate the influence of giant reed plants on ecosystems of red mud-amended soil (in case of adding red mud to marginal and wetland soils) especially after exposure to high temperatures, (2) to monitor the changes in soil microbial community and soil enzyme activities under giant reed cultivation in case of heated soil compared to control soil, and (3) to investigate the effects of soil heating on giant reed seedling growth and biomass production.

Materials and Methods

Soil Sampling and Preparation

In early spring 2011, two composite top-soil samples (0–25 cm) were collected from the demonstration garden of Debrecen University, Debrecen city (47°32′0″ N; 21°38′0″ E). The first soil sample (S1) was collected from a field, which had had grass coverage for the previous 9 years and S2 was collected from a field of 1-year-old giant reed. An additional two composite soil samples and a sample of red mud (also 0–25 cm) were collected from Kolontár town, western Hungary (47°5′3.97″ N, 17° 28′30.08″ E); S3 was collected from a field with a maize, sun flower, and rapeseed crop rotation; S4 (mud-polluted soil) was collected from a red mud-polluted field. The red mud sample was collected from flooded grassland [7]. After sampling, a portion of each fresh soil sample was sieved through 8 mm and used directly for enzyme activity measurements and microbial counts (Table 1). The rest was air dried 25 °C, ground in stainless steel crushing machine, and sieved at 2 mm, then kept in plastic bags for further chemical analysis at 25 °C (Table 1).

Table 1 Chemical and biochemical properties for different soils and red mud before giant reed cultivation
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Plant Material

The plant material used for the current study was somatic embryo-derived plantlets of the Blossom ecotype of giant reed (Arundo donax L.) obtained from the University of South Carolina and propagated in the Ottó Orsós Laboratory, Department of Plant Biotechnology, Debrecen University, Hungary. Sterile plantlets were directly transplanted to autoclaved samples; the other sterile plantlets were acclimatized to the greenhouse environment before potting in non-autoclaved samples.

Experimental Design

The experimental layout was a completely randomized design with three replications. To study the effects of giant reed on soil enzyme activities and microbial community, soil samples were divided into two portions; the first portion was autoclaved at 121.5 °C and 1.5 atm. for 1 h for three consecutive days with incubation at 28 °C between autoclaving. The second half was left without autoclaving to compare the soil enzyme activities and microbial community under giant reed. From each soil sample, 300 g were added into plastic pots and irrigated with tap water and left alone for one night. The next morning, two seedlings were planted in each per pot; the seedling height ranged between 10 and 12 cm. Five days later, half the seedlings received 10 ml of a commercial biofertilizer (CB) (Azotobachter croococcum and Bacillus megaterium), and half the pots left unfertilized as a control (Cont). The water content was kept at field capacity during the experimental period.

Plant Analysis

The giant reed plants were harvested 3 months after planting. Fresh mass and length of shoot and root portions were measured. For nitrogen–phosphorous–potassium (NPK) content, a 0.5-g sample was digested by addition of 10-ml H2SO4 and 1.0-ml HClO4 [23]. The tissue concentration of N, P, and K was determined both colorimetrically [23] and by flame photometer [22].

Soil Chemical Analysis

Available N, P, and K and SOC analyses were carried out in triplicate for each treatment. Available P was determined colorimetrically [25]. Available N was evaluated by the macro Kjeldahl digestion procedure [23]. Available K was determined using flame photometry [24]. SOC was determined using the modified Walkley–Black wet combustion method [23].

Soil Microbiological Components Analysis

Soil microbial activities were measured in fresh samples before potting and after harvesting giant reed. The serial dilution pipette method was used for the microbial counts on different selective media [26]. Phosphatase activity was measured as described by [27]. Dehydrogenase, urease, and catalase activities were determined using the procedures of [28–30], respectively.

Statistical Analysis

Data analysis was performed using Microsoft Excel 2003 (mean values and standard deviation). The effect of giant reed on soil properties before and after experiment was compared with paired t tests. An effect was considered significant at the 5 % level. The three-way fixed-effects analysis of variance was conducted using the SPSS 13.0 software package (SPSS Inc., Chicago, IL). Dependent variables were checked for normality and homoscedasticity and transformed as necessary. Separation of means was performed by post hoc test (Scheffe test), and significant differences were accepted at the level p < 0.05. All values are presented as untransformed means and standard deviations.

Results

Soil Properties

Planting giant reed affected some soil chemical and biochemical properties after 3 months (Table 2). For instance, soil pH increased by 5–9 % in all soils by the end of experiment, except for red mud where planting giant reed decreased pH by 1 % (Table 2). EC for all soils was decreased by 24–82 % in non-autoclaved and autoclaved soils, respectively; the EC of red mud planted with giant reed was decreased by 63 %. Planting the test soils with giant reed had a variable effect on SOC after 3 months. For instance, without addition of inorganic fertilizers, SOC slightly decreased in most soils, e.g., by 11 % in soil S3, but SOC was increased in S1 and S4 (Fig. 1). With respect to available soil P, a sharp decrease was observed in all autoclaved and non-autoclaved soils. The amount of available potassium was increased more than 15–150 % in most soils relative to levels before experimentation, but there were no significant differences between treatments.

Table 2 Soil chemical properties after giant reed cultivated in different soils treated by biofertilizer with and without autoclaving compared to before experiment
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Fig. 1
figure 1

Soil organic carbon (SOC) content in soils and red mud after giant reed plantation. S1 soil after grass; S2 soil after giant reed; S3 soil after maize, sun flower, and rapeseed rotation; and S4 mud-polluted soil. Non-aut non-autoclaved; aut autoclaved; CB commercial biofertilizer. Vertical bars represent the standard error (n = 3)

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Soil Enzyme Activities

Dehydrogenase Activity

Overall, we detected high increasing in dehydrogenase activity for all soils and red mud compared to initial status before giant reed plantation (Fig. 2). Twelve weeks after planting of the giant reed was enough to significantly increase the activity of dehydrogenase in all soils and the red mud. Compared to the status of samples before the treatment, it is clear that giant reed has induced the intracellular enzyme (dehydrogenase) activity. In general, dehydrogenase activity has increased by 187–425 % in non-autoclaved soils compared to 262–705 % increases after autoclaving. Significant differences were found between autoclave and non-autoclaved treatments, where dehydrogenase possessed higher activity in autoclaved soils than non-autoclaved soils. Moreover, using commercial biofertilizer did not significantly affect dehydrogenase activity.

Fig. 2
figure 2

Some soil enzyme activities in different soils and red mud cultivated by giant reed using commercial biofertilizer. S1 soil after grass; S2 soil after giant reed; S3 soil after maize, sun flower, and rapeseed rotation; and S4 mud-polluted soil. Non-aut non-autoclaved; aut autoclaved; CB commercial biofertilizer. Vertical bars represent the standard error (n = 3)

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Urease Activity

Urease activity is sensitive to autoclaving. A significant decrease in urease activity was found under autoclaved-tested soils and red mud in comparison with non-autoclaved soils and red mud (Fig. 2). Planting giant reed in non-autoclaved soils significantly increased urease activity compared to the activity seen before giant reed plantation. Increasing of urease activity ranged between 195–591 and −35 to 46 % in non-autoclaved and autoclaved soils, respectively. Similarly, there were no significant differences between control and biofertilizer in most soils and red mud with or without soil autoclaving.

Alkaline Phosphatase Activity

Alkaline phosphatase activity decreased in all tested soils and red mud compared to that observed in soils before experimentation (Fig. 2). In autoclaved and non-autoclaved samples, biofertilizer did not affect alkaline phosphatase activity significantly. The reduction of phosphatase activity ranged between 0.3–0.8 folds in both autoclaved and non-autoclaved studied soils.

Catalase Activity

In general, the variation of catalase activity in all soils was similar to the variation in dehydrogenase activity. However, catalase activity increased in tested soils and red mud by 51–385 and 87–207 % in non-autoclaved and autoclaved-tested soils respectively, comparing with activity before giant reed plantation (Fig. 2). Autoclaving treatment significantly affected catalase activity in all soils except in the case of red mud since higher activity for catalase was recorded in non-autoclaved red mud. On the other hand, biofertilizer has no significant effects on catalase activity in both autoclaved and non-autoclaved samples.

Microbial communities

Total Bacterial Count

Generally, total bacterial count decreased after planting giant reed, these variations ranged between 29–93 %. The highest reduction was recorded under mud-polluted soil (S4), as a result for unfavorable conditions after contamination with red mud (Fig. 3). An increase in total bacterial count was found with soil S3 (maize, sun flower, and rapeseed rotation). On the contrary, total microbial count was positively affected by soil autoclaving than non-autoclaved samples.

Fig. 3
figure 3

Total bacterial and fungi counts in autoclaved and non-autoclaved soils and red mud planted with giant reed. S1 soil after grass; S2 soil after giant reed; S3 soil after maize, sun flower, and rapeseed rotation; and S4 mud-polluted soil. Non-aut non-autoclaved; aut autoclaved; CB commercial biofertilizer. Vertical bars represent the standard error (n = 6)

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Total Fungal Count

Total fungi count was higher in autoclaved samples than in non-autoclaved samples (Fig. 3). In general, after the giant reed experiment, the total fungi number has increased in most soils. This increase ranged between 45 and 136 %, except soil S1 (9-year grass) and soil S4 (mud-polluted soil). Similarly, biofertilizer did not affect total fungi count in both autoclaved and non-autoclaved-tested soils and red mud.

Growth Performance of A. donax L

Giant reed plants in autoclaved soils possessed more robust root systems (short, very branched) than those in non-autoclaved soils (long, little branched), which means the former plants have a greater ability to uptake NPK and other micronutrients from the soils. The wet weight and length of shoots and roots were higher in autoclaved treatments than non-autoclaved (Fig. 4). Giant reed stem weight and length were greater when grown in red mud-contaminated samples compared to the non-contaminated soils, with or without autoclaving. Macronutrient (NPK) concentrations were higher in the shoots than in the roots of giant reed (Fig. 5), although there were no differences between autoclaved and non-autoclaved treatments. However, the highest N concentrations in shoots and roots were 1.3 and 0.8 % under S4 (red mud-contaminated soils) and S2, respectively, whereas the highest concentrations for P were 3.4 and 2.5 % for shoots and roots under S2 and S4. On the other hand, the highest K concentrations in shoots and roots, 1.7 and 1.4 % respectively, were recorded in S1.

Fig. 4
figure 4

Wet weight and plant length of giant reed plants grew in different soils and red mud with and without soil autoclaving. S1 soil after grass; S2 soil after giant reed; S3 soil after maize, sun flower, and rapeseed rotation; and S4 mud-polluted soil. Non-aut non-autoclaved; aut autoclaved; CB commercial biofertilizer. Vertical bars represent the standard error (n = 8)

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Fig. 5
figure 5

NPK content of giant reed plants grew in soils and red mud after soil autoclaving. S1 soil after grass; S2 soil after giant reed; S3 soil after maize, sun flower, and rapeseed rotation; and S4 mud-polluted soil. Non-aut non-autoclaved; aut autoclaved; CB commercial biofertilizer

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Discussion

Soil Chemical Properties

The presence of giant reed significantly increased the amount of available N in all soils (Table 2). It was observed that non-autoclaved samples had significantly higher concentrations of available N than autoclaved samples. These results are in agreement with results from Alshaal et al. [7], who reported that giant reed increased available nitrogen in red mud and mud-polluted soil. The effects of autoclaving on the remineralization of labile inorganic P were clear—giant reed growth was much higher in autoclaved soils than non-autoclaved. In this study, P concentrations were between 1.3–2.6 % in shoots, and 0.7–1.7 % in roots produced on autoclaved soils. Plant available P is a critical growth determining factor, and it has been observed that the densest, tallest stands of giant reed growing along streams and drains in Egypt do so beside drains with high concentrations of soluble P. In addition, giant reed was one of the fast growing plants in fields that had been burned deliberately to control vegetation. These results are in agreement with results from Alshaal et al. [7], who reported that giant reed increased available NPK in red mud sample and mud-polluted soil.

Soil Enzyme Activities

Soil enzymes are good indicators of soil quality because: (1) they are closely related to organic matter, physical characteristics, microbial activity, and biomass in the soil and (2) they provide early information about changes in soil quality and are assessed more rapidly [31]. Dehydrogenase requires an intracellular environment (viable cells) to express its activity [20], the higher activity found in planted soils compared to unplanted controls indicates that giant reed has a unique microbial community which associates with its robust root system, where, after using sterile seedlings of giant reed and autoclaved samples, high numbers of bacteria and fungi were counted indicating the ability of giant reed to induce the growth of microbial community around its root system [7].

Urease has been widely used to evaluate changes on soil quality related to management. This enzyme is an extracellular enzyme representing up to 63 % of total activity in soil. It has been show that its activity depends on the microbial community, physical, and chemical properties of soil [32].

Phosphatases are a group of enzymes that catalyze hydrolysis of esters and anhydrides of phosphoric acid. Its activity, as extracellular enzymes, can be free in the soil water phase or stabilized in the humic fraction or clay soil content [33]. Phosphatase activity in temperate grassland was investigated by Turner and Haygarth [33], and they found a strong correlation between enzyme activity and soil properties such as pH, total N, organic P, and clay content. The significant decreasing of alkaline phosphatase activity in tested soils may refer to shortage of available P concentration in the soils after experiment. These results emphasize that A. donax L. is a good candidate for marginal and wetland soil construction with soil health point of view.

Microbial Communities after A. donax L

Microorganisms play a key role in nutrient cycling and energy flow. Microbial communities respond to environmental stress or ecosystem disturbance, affecting the availability of energetic compounds that support microbial population [22]. Soil autoclaving did not negatively affect significantly the microbial communities (e.g., bacterial, fungal and actinomycestes counts) growth under giant reed, but autoclaved treatment recorded higher numbers than non-autoclaved treatment, maybe because autoclaving allowed a large number of bacteria in autoclaved soil to grow within a less diverse community. These findings may demonstrate that giant reed has special microbial community, so further studies about microbial communities that associate with giant reed root system are needed. Also, biofertilizer addition did not affect the total bacterial count in significant way.

A. donax L. Growth and Biomass Production

Effects of heating and/or autoclaving on the soil properties have been widely documented [34, 35]. However, heating affects the nature of soil minerals and most probably, their interactions with other plant nutrients. Soil temperatures in excess of 500 °C can be reached during fires, which will modify many hydroxylated soil minerals thereby changing their nature and nutrient retention properties [36]. Heat generated during fire not only induces chemical oxidation of soil organic matter by altering carbon and nitrogen transformations but also has potential effects on the soil microbial communities since higher temperatures than 50 °C are enough to kill the heat-sensitive microbes specially fungi, and temperatures higher than 70 °C can directly affect cover vegetation [34–37]. However, exposure to high temperature and pressure for a long time has negative effects on soil ecology where almost all enzyme activity stops and microbial groups are going to disappear, but on the other hand, there are some positive effects such as remineralization of nutrients such as P. Anderson and Magdoff [35] reported that autoclaving soil resulted in almost 60 % more available P compared to non-autoclaved samples, with 78 % more orthophosphate monoesters, 60 % more orthophosphate diesters, and 54 % more soluble inorganic P. Although at the same time, other nutrients like N and C may be lost by volatilization. In this study, giant reed grew more vigorously in autoclaved soils and red mud than non-autoclaved soils and red mud. The most promising and encouraging data was the higher biomass production of giant reed growing in autoclaved-tested soils especially in pure red mud. These findings demonstrate that under these conditions, high temperature and pollution by red mud (a caustic medium with high EC and trace metal content), giant reed could be an effective solution to restore this soil soon and at the same time produce significant biomass production. The root system architecture was entirely different and extraordinary between autoclaved and non-autoclaved soils. There were no clear explanations for why giant reed roots were short and denser in autoclaved treatment comparing with long and few roots in non-autoclaved. Anyway, the root architecture for giant reed still needs more investigations to get a clear view for using giant reed as a construct plant in marginal soils. This data encourages using giant reed as a good candidate to restore soil ecosystems after exposure to high temperatures for a long time.

A. donax L. and red mud-contaminated soil

Recycling of bauxite-derived red mud becomes urgent where huge amounts of red mud are generated every year, since 1 t of alumina generally results in the creation of 0.5–2.5 t of red mud. There is limited information on the use of red mud as soil amendment. However, red mud was used to reduce the availability of trace metals in different environments because of its high pH [17]. Moreover, leaching of phosphorus was decreased by adding red mud to soil as a result for the high retention capacity of fine particles in red mud and its high pH [7]. Our study aimed to investigate the possibility using of red mud in wetland and marginal soils and the ability of giant reed to recover red mud-affected soil after exposure to high temperatures. The data showed that giant reed is able to improve soil quality after heating and after contamination with red mud. No wild fires were recorded in the soil sampling area in Hungary, but bauxite mining occurs in other parts of the world where wild fires do occur, and the results from this study suggest that in those areas, giant reed can be used to rehabilitate soil containing red mud.

Conclusion

The present study is on giant reed highlights and its ability to restore and recover soil ecosystems after exposure to natural disasters such as bushfires. In addition, giant reed showed considerable potential for recovering red mud-affected soils. The cultivation of giant reed increased the activities of most soil enzymes, especially dehydrogenase, urease, and catalase. In addition, cultivation of giant reed enriched soil NPK and decreased electrical conductivity after autoclaving. Concerning soil organic carbon, no big changes were detected since the experiment was done without any addition of inorganic fertilizers. Biomass production of giant reed was higher in red mud-contaminated samples compared to autoclaved soils. In summary, giant reed appears to be a good candidate species to restore ecosystems in wetland and marginal soils, while at the same time generating feedstocks for the production of bioenergy.