Abstract
Purpose
This study aimed to improve the phosphorus (P) fertilizer value of sewage sludge ashes and biochars through different pre-treatments and application methods.
Methods
In experiment 1, two sewage sludges, their respective ash, and biochar underwent three chemical pre-treatments (H2SO4, NaOH, and Ca(OH)2. These materials were utilized as P fertilizers in a maize plant trial), using two application methods (mixed and placed). In experiment 2, biochars sourced from four sewage sludges were pre-treated with H2SO4 and NaOH and then employed as P fertilizers in a barley plant trial.
Results
Experiment 1 revealed a significant impact of application method on shoot dry matter, with mixing outperforming placement. Acidification pre-treatment of the ash led to significantly higher shoot dry matter (2.7 ± 0.3 g) and P uptake (7.9 ± 0.9 mg per plant) compared to untreated ash (0.7 ± 0.1 g; 1.9 ± 0.2 mg per plant). Similarly, NaOH-treated biochar caused elevated shoot dry matter (2.6 ± 0.4 g) and P uptake (6.9 ± 0.4 mg per plant) compared to untreated biochar (0.7 ± 0.2 g; 1.9 ± 0.1 mg per plant). These outcomes highlight the dependence of pre-treatment efficacy on biomaterial composition. Experiment 2 demonstrated that despite differing elemental compositions of the biochars, NaOH treatment led to significantly greater shoot dry matter and P uptake compared to untreated and acidified treatments.
Conclusions
Chemical pre-treatments have the potential to enhance the short-term P fertilizer value of ashes and biochar. However, further studies are essential to assess the economic feasibility and potential environmental risks, including increased heavy metal solubility.
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Statement of Novelty
Enhancing sustainable sewage sludge management is crucial for a circular economy. Thermal methods such as incineration and pyrolysis reduce organic contaminants but yield ashes and biochars with a high content of phosphorus that is often poorly available to plants. Our study explored chemical pre-treatments to boost phosphorus solubility in these materials for improved plant uptake. We found that treatment effectiveness was linked to phosphorus speciation in the materials. Ashes, rich in Ca–P, responded well to acidification, while NaOH treatment worked better for biochars with higher Al– and Fe–P contents. These pre-treatments demonstrated promising results on increasing the phosphorus fertilizer value of sewage sludge byproducts. Therefore, this research is in line with circular economy goals and supports environmentally friendly waste utilization to replace mineral P fertilizers.
Introduction
A considerable part of the phosphorus (P) used in the European Union (EU) ends up in sewage sludge [1] and, if appropriately managed, has the potential to meet a significant proportion of the EU’s agricultural phosphorus demand [2]. Previously, risk assessments have found that application of sewage sludge to agricultural land is a safe and appropriate management solution [3, 4] and, recently, Magid et al. [5] found that the risks associated with land application of Danish sewage sludge would be comparable to that of pig slurry, when EU limits to use of Cu and Zn in animal feed have been implemented.
However, the application of sewage sludge to agricultural land remains controversial due to its potential content of contaminants such as pharmaceutical residues, pathogens, and heavy metals [6]. European countries differ considerably in their approaches to sewage sludge disposal and phosphorus recycling strategies [7]. While mono-incineration has become the prevailing practice in the Netherlands, Switzerland, and Belgium [6], recent legislative developments in Sweden, the Czech Republic, and Denmark have allowed for the agricultural application of sludge biochar [8].
Both incineration and pyrolysis offer advantages, including volume reduction, increased phosphorus concentration, pathogen elimination or reduction, and potential energy recovery. However, these benefits depend on process parameters such as temperature and retention time [9,10,11] and treatments can be costly [12, 13]. Additionally, pyrolysis offers an advantage in the formation of recalcitrant carbon, which can contribute to soil carbon sequestration and climate change mitigation [14, 15]. However, the recycling of phosphorus through thermally treated sludge faces a significant constraint: a decrease in phosphorus availability, commonly observed in sludge ash and biochar after pyrolysis or incineration [16,17,18], due to the formation of more insoluble phosphorus species with consequently lower plant availability [19].
The water- and bicarbonate- extractable P pools in the materials are considered labile P and can be correlated with short-term plant P availability [20, 21]. However, P species commonly formed after thermal treatment of sludge are poorly soluble Al and Fe phosphates, Ca phosphates such as apatite or di-or tricalcium phosphates [11, 19, 22]. The limited availability of phosphorus in thermally treated sludge biochars and ashes is a challenge, especially in light of the existing phosphorus application limits in some EU countries [23]. This limitation gives rise to concerns regarding farmers’ inclination to use fertilizers with low phosphorus availability in the short term, as well as the potential accumulation of poorly available phosphorus in agricultural soils over time. Consequently, chemical pre-treatments and alternative application methods that can increase the phosphorus availability of sewage sludge ashes and biochars merit research.
The concept of localized application has been suggested as a strategy to improve the phosphorus use efficiency of mineral fertilizers [24]. However, when it comes to sewage sludge and sewage sludge ash, previous studies on localized application have yielded unconvincing results in terms of P uptake and plant biomass [25, 26]. Based on this knowledge, Sica et al. [27] proposed the use of acidification and alkalinization pre-treatments to enhance the P solubility of localized applied biowastes. However, the efficacy of pretreatments and placement methods remains untested in plant growth experiments. Additionally, there are significant variations in elemental composition and phosphorus speciation among sewage sludge materials due to different P removal techniques and salt additions [28, 29], which will also affect their responsiveness to pre-treatments.
Sequential extractions performed on sludge, sludge biochars, and ashes have revealed that a significant portion of the P in these materials is typically soluble in acid [27, 30, 31]. Conversely, other studies have observed high levels of NaOH-extractable P in sequential extractions from sludges, sludge biochars, and ashes [32,33,34]. Furthermore, alkaline pre-treatments, such as the use of NaOH, have shown increased P diffusion and apparent recovery when compared to acidification with H2SO4 for both sewage sludge and sewage sludge ash [27]. In addition, previous studies suggest that plant P uptake can be enhanced by pre-treating sewage sludge with lime due to an increase of the bicarbonate-extractable P pool [29, 35].
Consequently, chemical pre-treatments with H2SO4, NaOH, and Ca(OH)2 may affect the P speciation of sewage sludge ash and biochar, thereby increasing short-term P availability [27]. This enhancement may improve their fertilizer value, especially for crops with shorter cycles that are responsive to P fertilization, such as spring cereals (e.g., maize, spring wheat, and spring barley). This, in turn, may increase farmers’ interest in using these materials to replace mineral P fertilizers and, in the case of biochar, to sequester carbon in the soil [15].
Based on this background, the objective of this study was to assess how different chemical pre-treatments would affect the P solubility, speciation, and availability of sewage sludge ash and biochar. The following hypotheses were tested:
-
1.
Chemical pre-treatments can alter the P fractions of sewage sludge and its respective biochar and ash, increasing the P solubility and, consequently, the plant P uptake.
-
2.
The efficacy of pre-treatments will be dependent on the predominant phosphorus species present in the biomaterials. Specifically, acidification is expected to be more effective for calcium-bound P, whereas alkalinization is expected to be more effective for iron- and aluminum-bound P.
-
3.
Placement of pre-treated biomaterials with increased P solubility will result in enhanced plant P uptake.
To test these hypotheses, two experiments were conducted. In experiment 1, all three hypotheses were tested by pre-treating two types of sewage sludge and the derived ash and biochar with Ca(OH)2, H2SO4, and NaOH. We evaluated the impact of these pre-treatments on P speciation (Hedley fractionation), solubility, and plant availability when the materials were either mixed with the soil or placed close to the seeds. For this experiment, we chose maize based on previous studies that have shown its responsiveness to the placement of soluble P forms [25]. As expected, the sewage sludge ash reacted very positively to acidification in experiment 1, probably due to the predominance of Ca-phosphates typical for SS ashes incinerated at higher temperatures [33]. However, the P speciation in SS biochars seems to be more variable depending on the different pyrolysis settings combined with different sludge materials, as also indicated by the results of experiment 1. Therefore, we selected NaOH and H2SO4 to be tested in four different sewage sludge biochars in experiment 2. As placement was not a treatment in experiment 2, a different crop could be selected with the aim of assessing whether the response remained consistent with spring barley, one of the most cultivated crops in the Nordic countries.
Materials and Methods
Table 1 gives an overview of the different materials used in the two experiments, their origin and the P removal method used at the wastewater treatment plant. In addition, the experimental set-up of experiments 1 and 2 is shown.
Sludge Materials
The chemical composition of the biomaterials used in both experiments 1 and 2 is presented in Table 2. The dewatered sewage sludge (SS-R) and sewage sludge ash (IA-R) were collected from the BIOFOS wastewater treatment plant (www.biofos.dk) in Avedøre, Greater Copenhagen, which combines biological and chemical (iron salts) P removal. At this plant, the sewage sludge undergoes the following processes: mesophilic anaerobic digestion, dewatering, drying, and mono-incineration to produce the ashIA-R). More information on SSR and IA-R processing can be found in Lemming et al. [30] and López-Rayo et al. [36].
The biochar used in both Experiments 1 and 2 was derived from sewage sludge from a wastewater treatment plant in Lund, Sweden (SS-SE). The plant uses FeCl3 for P removal and the sludge is anaerobically digested. For biochar production, the sludge was pyrolyzed in a pilot plant at temperatures above 700 °C.
BC-Fe was obtained from sludge from VandCenter Syd’s wastewater treatment plant, Odense, Denmark, which uses iron salts and biological P removal processes. The sludge was anaerobically digested before being pyrolyzed at 650 °C in a pyrolysis pilot plant.
BC-Bio was produced using sludge feedstock obtained from the Gårdeby wastewater treatment plant, Aabenraa, Denmark, that does not apply chemical P removal. The sludge used for BC-Al was sourced from the Bjergmarken wastewater treatment plant in Roskilde, Denmark. During the wastewater treatment process at this plant, iron salts are added for chemical P removal, followed by the addition of aluminum chloride (AlCl3). The sludge is then anaerobically digested for three weeks in a thermophilic processs. Both BC-Bio and BC-Al were produced in smaller batches within a chamber reactor, under a N2 atmosphere, at a temperature of 600 °C at the Technical University of Denmark.
Experiment 1
Titration Curves
SS-R, SS-SE, IA-R and BC-SE (used in experiment 1) were treated with H2SO4 (1 M, 2.5 M, 5 M, 7.5 M, 10 M), NaOH (1 M, 2.5 M, 5 M, 7.5 M, 10 M) and Ca(OH)2 (2.5%, 5%, 10%, 15%, ww−1) according to the procedure previously described by Sica et al. [27]. Briefly, for the NaOH and H2SO4 treatments, 5 g of each dried biomaterial was added to 50 mL centrifuge tubes and 2.5 mL of solution (ratio 2:1 wv−1) was applied. For the Ca(OH)2 treatments, 5 g of biomaterial was added to 50 mL centrifuge tubes and the appropriate amount of Ca(OH)2 powder and 2.5 mL of Mili-Q water was added. The biomaterials and chemicals were carefully mixed with a disposable spoon and placed in an oven at 65 °C for 48 h. After that, subsamples were collected to analyze pH (1:5 in H2O, shaken for 1 h) and water-extractable phosphorus (WEP, ratio: 1:60 wv−1 in water, shaken for 1 h). For the Ca(OH)2 treated biomaterials, bicarbonate-P was determined (1:60 wv−1, shaken for 1 h). After extraction with water and bicarbonate, samples were centrifuged and filtered through Whatman No. 5 filter papers. The ortho-P content in all extracts was analyzed using the molybdenum blue method on a flow injection analyzer (FIAstar 5000, Foss Analytical, Denmark).
Based on the results of increasing WEP (or bicarbonate-P for the Ca(OH)2) from the titration curves, one concentration of each chemical was selected for the sequential extraction and application in the pot experiment 1: for both sewage sludges = 5 M H2SO4, 5 M NaOH, and 15% Ca(OH)2; for the ash and biochar = 10 M H2SO4, 10 M NaOH, and 15% Ca(OH)2. The dried biomaterials were crushed using a ball mill and sieved to a particle size of 2 mm.
Sequential Extraction
A simplified Hedley P fractionation scheme [29, 37] was used to determine the effects of treatments on the different inorganic P pools of the biomaterials used in experiment 1. The modified fractionation consisted of the sequential extraction of an equivalent of 0.5 g dry matter of the biomaterial into four fractions. The first extraction was performed by adding 30 mL of deionized water (1:60 ratio), extracting for 16 h in an end-over-end shaker, and centrifuging (15 min, 5000 rpm). The supernatant was collected and filtered. The remaining solids were used for the following extraction with 35 mL of 0.5 M NaHCO3. The same procedures (35 mL of extractant, 16 h shaking, centrifugation for 15 min at 5000 rpm and filtration of the supernatant) were followed for the subsequent extractions with 0.1 M NaOH and 1 M HCl. The ortho-P content in all extracts was analyzed using the molybdenum blue method on a flow injection analyzer (FIAstar 5000, Foss Analytical, Denmark). All fractionations were carried out in triplicate.
Plant Growth Trial with Maize
Experiment 1 assessed the effects of H2SO4, Ca(OH)2, and NaOH pre-treatments of the two sewage sludge materials (SS-R and SS-SE) and their respective ash or biochar on P solubility and uptake by maize when either applied mixed into the soil or placed 5 cm below the soil surface. The soil used in this experiment was collected at the University of Copenhagen’s experimental farm in Taastrup, Denmark (55° 40′ N, 12° 16′ E) from the unfertilized treatment in the CRUCIAL long-term fertilization trial, which has been mainly cultivated with spring cereals. The soil was a low-phosphorus (WEP = 2 mg kg−1) sandy loam (a Luvisol according to the FAO classification) with a pH of 6.6, a clay content of 12.6%, a silt content of 14.3% and a sand content of 69.8%. After collection, the soil was air-dried and sieved to 4 mm. More information about the soil and the CRUCIAL long-term fertilization trial can be found in by Gómez-Muñoz et al. [38], Lemming et al. [39], and López-Rayo et al., [36].
For each experimental unit, 1.875 kg of dried soil was placed in a plastic bag with a 3:1 soil-sand mixture (0.4–0.8 mm quartz sand), resulting in a total dry weight of 2.5 kg. The soil-sand mixture (hereafter referred to as “soil”) was homogenized and all necessary plant nutrients, with the exception of phosphorus, were added at the following rates (in mg per kg of soil): N = 150; K = 150; Ca = 40; Mg = 40; S = 20; Cu = 1.5; Zn = 1.2; Mo = 0.1; Fe = 3; B = 0.3; Mn = 3.
For the mixed treatments, the P fertilizers (80 mg of total P per kg of soil) were added to the bags, mixed, and carefully transferred to the pots. For the placed treatments, the dried soil was added, and a tube (5 cm diameter) was used to make a hole in the center of the pot, 5-cm below the soil surface, into which the biomaterials were placed.
The pots were placed in a growth chamber, divided into four blocks and randomly distributed within the blocks. Seeds of maize (Zea mays) cv. ‘Ambition’ (Limagrain SE) were pre-germinated and one seedling was transplanted into the center of each pots. Every 3 days, the pots were randomly rotated within each block to minimize the influence of any temperature or light gradients in the growth chamber and watered by weight to maintain the soil moisture content at 70% of the water-holding capacity (WHC). The climate chamber was set to a day cycle of 16 h at a photon flux density of 600 µmol m−2 s−2 and a constant temperature of 19 °C. The night cycle was 8 h at a constant temperature of 15 °C. The plants were harvested 35 days after emergence (when the 5th leaf was visible, maize growth stage V5).
After harvesting, soil samples were collected from the exact location where the biomaterials had been placed and for the mixed treatments from a region corresponding to the placement location, and the pH was measured.
Experiment 2: Plant Growth Trial with Barley
Based on the results of experiment 1, experiment 2 assessed the effects of acid (H2SO4) and alkaline base (NaOH) pre-treatments on different types of sludge biochars.
The soil used in the experiment was collected at the University of Copenhagen’s experimental farm in Taastrup, Denmark (55° 40′ N, 12° 16′ E) from the long-term Nutrient Depletion Trial, previously annually fertilized with animal slurry (120 kg NH4-N ha−1y−1) since 1996 and additionally with mineral P fertilizer (20 kg P ha−1y−1) since 2010. The soil was a sandy loam consisting of 164 g kg−1 clay, 173 g kg−1 silt, 333 g kg−1 fine sand, 312 g kg−1 coarse sand and 17 g kg−1 organic matter [40]. The soil pH was 5.9 and water-extractable P was 8 mg kg−1. The soil was collected, air-dried and sieved to 4 mm. For each experimental unit, a 2:1 soil-sand mixture (0.4–0.8 mm quartz sand, hereafter referred to as “soil”) was placed in a plastic bag, resulting in a total dry weight of 2 kg. The soil was fertilized with nutrient solutions to provide all nutrients, except phosphorus, as described in the previous section.
In Experiment 2, the same amounts as in Experiment 2 of H2SO4 and NaOH were applied to pre-treat the biochars. For the biochar treatments, the biochar (80 mg of total P per kg of soil) was added to the bags, mixed, and carefully transferred to the pots. The 56 pots were then placed in a greenhouse in a completely randomized design. Three seeds of spring barley (Hordeum vulgare) cv. Feedway were sown at a depth of 1 cm. The pots were randomly rotated four times a week to minimize the influence of any temperature or light gradients in the greenhouse and watered by weight to maintain the soil moisture content at 60% of the WHC. During the experiment, daytime temperatures ranged from a minimum of 13 °C to a maximum of 28 °C, while the temperature at night ranged from 6 to 18 °C. The aboveground biomass of the spring barley was harvested 42 days after sowing. Soil samples were taken from each pot to measure pH and WEP.
Plant Analyses
After harvest, the plant shoots were dried at 65 °C for 48 h and the dry matter was determined. The dried shoots were then ground to a fine powder and homogenized.
To determine the total P content of the shoots, subsamples of 100 ± 10 mg were ashed in small crucibles at 550 °C for one hour. The ash was transferred to a 50-mL centrifuge tube, shaken on an end-over-end shaker for 16 h with 50 mL of 0.5 M H2SO4 and subsequently filtered through Whatman No. 42 ashless filter papers. The ortho-P content of the extract was determined using a flow-injection analyzer (FIAstar 5000, FOSS, Denmark).
The mineral fertilizer equivalent (MFE) was calculated as (Eq. 1):
where, APRbiomaterial is the apparent P recovery from the biomaterial and APRmineralP is the apparent P recovery from the mineral fertilizer applied mixed with the soil. APR was calculated as:
Statistics
All statistical analyses were performed in R version 4.0.2 (R core team). All data was tested for normal distribution and homogeneity of variance of the data. In experiment 1, differences between pre-treatments within each material in the sequential fractionation were tested using a one-way ANOVA. For the plant growth trial in experiment 1, differences between treatments within each material were tested using a two-way ANOVA with pretreatment and application method as factors. For the plant growth trial in Experiment 2, the two-way ANOVA was performed with pre-treatment and biochar as factors. Student’s T-tests and Tukey’s HSD test were used for the comparison of means. Comparison of treatments with the control treatment in experiment 1 and 2 was performed using a Dunnett’s test. The level of significance was set to p ≤ 0.05. The specific analyses applied for each parameter are indicated in the figure and table captions. Further, a Pearson correlation was performed for the correlation between mineral fertilizer equivalent (MFE) and the sum of the biomaterials’ water extractable P and bicarbonate.
Results
Experiment 1
Titration Curves
The acidification of sewage sludge using H2SO4 resulted in a significant increase in the water-extractable phosphorus (WEP) content, representing approximately 80% and 95% of the total phosphorus content at concentrations of 7.5 M and 10 M, respectively (Fig. 1). When 10 M sulfuric acid was applied to char and ash, the WEP content increased to about 20% of the total phosphorus content. Alkalinization with NaOH had a pronounced effect on the WEP pool of SS-SE, with approximately 75% of the total phosphorus content being extracted using a 10 M NaOH solution (Fig. 2). When 10 M NaOH was applied to BC-SE and SS-R, approximately 20% of the total phosphorus content was extracted by water. However, NaOH alkalinization had a negligible effect on the WEP content of IA-R. Treatment with Ca(OH)2 led to an increase in bicarbonate-extractable P for SS-SE, SS-R, and IA-R, although to a lesser extent, reaching approximately 4% of the total phosphorus content (Figure S1).
Effects of Treatments on Inorganic P Pools
The acidification treatment yielded the highest water-extractable phosphorus (WEP) pool for SS-SE, SS-R, and IA-R, resulting in a significant increase in WEP, bicarbonate-P (except for SS-R), and NaOH-P fractions, while reducing the HCl-P fractions compared to the respective untreated biomaterials (Table 3). In the case of BC-SE, the NaOH treatment showed the highest WEP pool.
Pot Experiment with Maize
Shoot dry matter was significantly affected by pre-treatment and application method and the interaction of both (Fig. 3). The placement of triple superphosphate resulted in a significant increase in shoot dry matter compared to the mixed application (Table S1). Application of both H2SO4-treated sewage sludges mixed with the soil significantly increased shoot dry matter when compared to the respective untreated materials (Fig. 3). For BC–SE materials, the NaOH-treatment mixed with the soil showed the highest shoot dry matter, while for IA-R, the acidified treatment showed a significantly higher shoot dry matter than the other treatments. Considering the application methods, the placement of all H2SO4– and NaOH-treated biomaterials significantly reduced the shoot dry matter compared to the respective mixed treatment.
For each of the materials, pre-treatment and application method and the interaction of both was significantly affecting P uptake (Fig. 4). The placement of triple superphosphate significantly increased the P uptake when compared to the mixed application (Table S1). For both SS-SE, the acidified mixed treatment showed the significantly highest P uptake, whereas for SS-R the acidified mixed treatment was not significantly different from the untreated mixed treatment. For BC-SE, the NaOH treatment showed the highest P uptake. For the IA-R, the acidified mixed and placed treatments showed the significantly highest P uptake (Fig. 4).
The sum of water extractable-P and bicarbonate-P fractions had a positive and significant correlation with the mineral fertilizer equivalent values for the materials applied mixed with the soil (R2: 0.35; p-value: 0.02). However, for the materials placed close to the seeds, this correlation was not significant (R2: 0.011; p-value: 0.72) (Fig. 5).
Experiment 2
Effects of Pre-treatments on the Biochar’s WEP and pH
The ability of the NaOH and H2SO4 pre-treatments to dissolve P varied significantly between the biochars. The NaOH treatment showed a significant increase in the water-extractable phosphorus (WEP) content of all biochars compared to the respective untreated biomaterials. The WEP ranged from 16% for BC-Bio to 40% of the total phosphorus content for BC-SE. Similarly, the H2SO4 treatment also showed a significant increase in WEP, ranging from 16% for BC–Fe and BC-SE to 81% of the total phosphorus content for BC-Bio. The pH values of the NaOH-treated biochars ranged from 10.7 (BC–Al) to 11.5 (BC–Fe). In contrast, the pH values of the acidified biochars ranged from 1.4 (BC-SE) to 2.4 (BC–Fe and BC-Bio) (Table 4).
Pot Experiment with Barley
The shoot biomass of barley was significantly affected by the pre-treatment and the material, but not the interaction of both (Table 3). Of the untreated biochars, only BC-Al and BC-Bio showed significantly higher shoot dry matter compared to the negative control. For all four biochars, the alkalinization treatment (NaOH) consistently resulted in significantly higher shoot dry matter than the untreated materials. In contrast, the acidification treatment did not result in a significant difference compared to the respective untreated biomaterials for any of the four biochars.
The P uptake of barley was significantly affected by the pre-treatment, the material and the pre-treatment/material interaction (Table 3). Of the untreated biochars, only BC-Al and BC-Bio showed a significantly higher phosphorus (P) uptake compared to the negative control. The NaOH pre-treated BC-Bio showed the highest P uptake with 29.6 mg per plant, resulting in a mineral fertilizer equivalent (MFE) of 79.4%, significantly higher than all other treatments. Also for BC-Fe and BC-SE, pre-treatment with NaOH resulted in a higher plant P uptake than acidification, while BC-Al was the only biochar where the acidification treatment resulted in the highest P uptake and MFE. However, this difference was not statistically significant compared to the NaOH-treated BC–Al (Table 3).
The NaOH treated biochar significantly increased the soil pH compared to the negative control at the end of the experiment. In contrast, the acidification treatment had no effect on soil pH. At the end of the experiment, none of the untreated biochar treatments showed a significant difference in WEP compared to the negative control. For BC–Al and BC-Bio, the acidified treatment showed a significantly higher WEP compared to the respective untreated biomaterials, whereas, for BC-SE, the NaOH treatment had a higher soil WEP compared to the respective untreated biochar (Table S2).
Discussion
Effects of the Application Method: Mixed vs Placed
In experiment 1, we examined the effects of different application methods for both untreated and pre-treated biomaterials on maize P uptake. We observed that the placement of TSP led to a significant increase in phosphorus uptake and shoot dry matter compared to TSP mixed with the soil. These findings are consistent with those reported by Lemming et al. [25], who also found a significant increase in P uptake and maize shoot dry matter when comparing TSP mixed with the soil to TSP placed in the soil [25].
The correlation analysis carried out on the results of experiment 1 shows a positive and significant correlation between labile P (WEP + bicarbonate-P) and maize mineral fertilizer equivalent for the mixed treatments, as shown in Fig. 5. However, when the materials were placed close to the seeds, an increase;e in the labile P did not result in a corresponding increase in the mineral fertilizer equivalent. Therefore, these results do not support our third hypothesis that the “placement of pretreated biomaterials with increased P solubility will result in enhanced plant P uptake”. We speculate that the correlation curves suggest that for the placed fertilizers, potential toxicity effects arising from extreme pH levels in the placement zone may have inhibited plant growth and P uptake.
For all biomaterials, the acidification and alkalinization pre-treatments required very low (< 2) and high (> 11) pH levels, respectively, to extract substantial amounts of P. It is known that extreme pH levels can also dissolve components containing other elements besides P [41], such as iron and aluminum from sewage sludge at pH values below 2 [42]. Additionally, root growth is negatively affected at pH levels below 4.5, with further aggravation occurring within the range of 3.5 to 4.0 [43]. Hence, we speculate that the extreme pH levels (< 5 and > 7.5) in the placement zone, coupled with the dissolution of other elements (e.g., Al) due to the pre-treatment, may have created a toxic zone, inhibiting root growth and impeding the plants’ access to P from the fertilizer. It is worth noting that the extreme pH levels were mainly confined to the placement zone, as when the treated materials were mixed with the soil, the effects on pH were low or negligible, as shown in Fig. 5 and Table S2.
It is important to note that the experimental setup used for the mixed application, involving sieved soil (4 mm) mixed with sand and homogeneously combined with the P fertilizer, is not representative of field conditions. In the field, fertilizers and/or biomaterials are typically distributed heterogeneously, leading to nutrient-rich patches in the soil [44], with the contact area between the soil and the fertilizer being usually limited to bands or patches [45]. The results obtained in this study using the mixed application method may therefore overestimate the fertilizer value of the biomaterials. Conversely, under field conditions, localized application/placement of fertilizers is often done in bands [46, 47], which promotes better fertilizer distribution and increased contact with the soil. In experiment 1, the placed fertilizers were applied in a small spot, which may have increased the potential toxicity effects of the pre-treated biomaterials [48]. Thus, the placement in pots may underestimate the effectiveness the pre-treatments compared to their potential under field conditions. Therefore, experiments under field conditions are necessary in order to properly assess these effects.
Interestingly, the placement of acidified IA-R significantly increased shoot dry matter and P uptake compared to the respective untreated biomaterials, with no significant difference observed compared to the acidified IA-R mixed application in terms of P uptake. Hence, we consider that the acidification of ash could be a promising treatment for enhancing P use efficiency, regardless of the application method.
Effects of Acidification and Alkalinization Pre-treatments on P Solubility and Availability of Sewage Sludge and Its Derived Ash and Biochar
Ca(OH)2
The application of Ca(OH)2 treatment resulted in the almost complete elimination of water-extractable phosphorus (WEP) in all four biomaterials (Table 2), as anticipated due to the expected binding of calcium with soluble phosphorus, as shown by Sica et al. [27]. Interestingly, this treatment also significantly increased the pools of HCl-P and bicarbonate-P for both sewage sludges (SSs), consistent with the findings of Alvarenga et al. [29] and Ylivainio et al. [35]. However, in contrast to these previous studies, the Ca(OH)2 treatment did not lead to an increase in phosphorus uptake from any of the biomaterials when they were either mixed or placed in the soil [29, 35, 49].
NaOH
The NaOH treatment showed a significant increase in the water-extractable phosphorus (WEP) pool for all biomaterials compared to their respective untreated forms. Interestingly, this treatment did not significantly affect the NaOH pool and primarily resulted in a decrease in the HCl pool. These findings suggest that the NaOH treatment primarily solubilized phosphorus from the HCl-P pool, which contradicts the results reported in other studies [42, 50] and deviates from the principles proposed by the Hedley sequential extraction method [37]. However, it is important to note that the use and accuracy of the Hedley fractionation technique in determining phosphorus fractions in biowastes and soils have been subject to debate, with concerns been raised regarding its applicability and reliability [51,52,53]. Benzing and Richardson [54], for example, have demonstrated that due to high pH Fe– and Al-bound P could be resorbed or precipitate as Ca-bound P, underestimating the Fe– and Al-bound P and overestimating the HCl-P pool [54]. Therefore, caution should be exercised when interpreting these results as the observed differences could also be due to different concentrations of NaOH applied in both the pre-treatment and the Hedley sequential fractionation.
Although the NaOH treatment led to a significant increase in phosphorus solubility for all biomaterials, the BC-SE showed the highest water-extractable phosphorus (WEP) content of all biomaterials after this treatment. Consequently, only the BC-SE applied mixed with the soil showed a significant increase in total phosphorus uptake compared to the untreated BC-SE, achieving a remarkable increase in its mineral fertilizer equivalent (MFE) value to 49.3%. This MFE value was significantly higher than that observed for the untreated BC-SE and relatively better than findings reported in other studies evaluating sewage sludge biochars [55, 56]. Additionally, this particular biomaterial caused a significant increase in shoot biomass in response to the NaOH treatment, which was higher than in the treatments with the original sewage sludge. These findings suggest that the NaOH treatment has great potential for enhancing the phosphorus fertilizer value of BC-SE.
H2SO4
The acidification significantly increased the WEP pool of all biomaterials compared to the negative control and was significantly the highest for SS-SE, SS-R, and IA-R. In addition, for all four biomaterials the HCl-P was significantly reduced, indicating that the P was mainly extracted from this pool. In the case of IA-R, this is expected, as the incineration at high temperatures favours the formation of Ca-P compounds [19, 57], converting Al- and Fe-bound phosphates into Ca-phosphates [33]. Ca-phosphates are expected to be extractable under acidic conditions, thus sewage sludge incineration ashes usually have large HCl-extractable P pools, as shown by Lemming et al. [30] and Sica et al. [27]. Interestingly, the NaOH-P of all acidified biomaterials increased significantly. According to Petzet et al. [34], the formation of Al-P in sewage sludge is favored at pH 2.5–3.5, which may indicate that after acidification, the pH could have slightly increased again and some of the dissolved P was transferred to the NaOH-P pool as Al-P [34].
The mixed application of all H2SO4-treated biomaterials significantly increased maize growth compared to the respective untreated biomaterials. This increase was most pronounced for IA-R. Indeed, for IA-R, the acidified mixed and placed treatments showed a high P uptake and MFE, reaching 59.1% for the acidified material mixed with the soil. This value was much higher than the untreated biomaterial (4.16%) and compared to previous work assessing the P fertilizer value of sewage sludge ashes [30, 35]. Indeed, [58] found that the acidification of different ashes and biochar significantly increase their P solubility, which was highly correlated with the P uptake by maize.
These findings are consistent with our second hypothesis, in which we stated that: “The efficacy of pre-treatments will be dependent on the predominant phosphorus species present in the biomaterials. Specifically, acidification is expected to be more effective for calcium-bound P, whereas alkalinization is expected to be more effective for iron- and aluminum-bound P”.
NaOH vs H2SO4 Pre-treatments for Different Biochar Materials
The results of both experiment 1 and experiment 2 suggest that the NaOH and H2SO4 pre-treatments of ash and biochar can significantly increase the labile P pools (WEP and bicarbonate-P pools), as well as the P uptake and plant growth of maize and barley. This supports our first hypothesis that “chemical pre-treatments can modify the P fractions of sewage sludge and its respective biochar and ash, leading to increased P solubility and, consequently, higher plant P uptake”.
The observed low phosphorus uptake from the untreated biochars BC-Al, BC-Al, and BC-Fe is consistent with their low water-extractable phosphorus (WEP) values and supports the findings of previous studies that have reported limited immediate P availability and fertilizer value from sludge biochars [16, 55]. Notably, the slightly higher P availability from BC-Al compared to the other untreated biochars suggests that the findings regarding increased P availability from aluminum-precipitated sludge ashes [19, 30, 59] can also be extended to biochars, as shown by Steckenmesser et al. [60]. Among the biochars tested, BC-Bio had the lowest iron and calcium content, as well as a lower Ca/P molar ratio (0.3), which can be attributed to the lack of addition of Fe salts during the treatment process and to the fact that the water in South Jutland (Denmark), where the plant is located, contains low amounts of Ca. Consequently, Bio-BC had the highest P fertilizer value among the untreated biochars.
Both NaOH and H2SO4 pre-treatments have shown their ability to enhance phosphorus solubility in sewage sludge and its derived ash and biochar. However, the acidification demonstrated greater efficacy for IA-R in experiment 1, while the NaOH pre-treatment showed more promising results for BC-SE and BC-Fe in both experiments, respectively. Both BC-SE and BC-Fe were treated with Fe salts, leading to higher iron contents in the biochar [61]. At lower pyrolysis temperatures, Fe-treated sewage sludge tends to form higher amounts of Fe3(PO4)2 [60], which may be extracted at alkaline conditions [50]. These findings are in agreement with our second hypothesis that “The efficacy of pre-treatments will be dependent on the predominant phosphorus species present in the biomaterials. Specifically, acidification is expected to be more effective for calcium-bound P, while alkalinization is for iron- and aluminum-bound P”.
According to Qian et al. [62], biochars derived from biologically treated sewage sludge tend to contain polyphosphates as the primary P species, which are relatively easier to extract. This characteristic may explain why BC-Bio showed the highest water-extractable phosphorus (WEP) when subjected to acidification, reaching almost 80% of the total P content, and thus was the only biochar for which the acidification treatment yielded significantly higher WEP compared to the NaOH treatment.
The BC-Al biochar showed similar WEP values for both acidification and alkalinization treatments, consistent with its more balanced Ca/P (1.0) and (Al + Fe)/P (1.1) molar ratios. As previously shown by Steckenmesser et al. [60] with K-edge Xanes spectra, Al-treated sewage sludge with a Ca/P molar ratio of 1 may form both Ca-phosphates (CaNaPO4, Ca3(PO4)2, and CaHPO4) and Al-phosphates (AlPO4).
Although the NaOH treatment did not show promising results in terms of increasing the water-extractable phosphorus of BC-Bio and BC-Al compared to the H2SO4 treatment, all four biochars treated with NaOH showed significantly higher shoot dry matter compared to the untreated and acidified treatments, as already observed for BC-SE in the pot experiment with maize. Interestingly, for BC-Bio, the NaOH treatment resulted in the lowest WEP, but we observed significantly higher phosphorus uptake and mineral fertilizer equivalent (MFE) compared to all the other treatments. This finding in experiment 2 is consistent with the results of Sica et al. [27] who reported that although alkalinization with NaOH was less effective than acidification with sulfuric acid in increasing phosphorus solubility in sewage sludge ash, the P diffusion and apparent recovery of NaOH-treated ash were significantly higher when applied to the soil [27]. This could be an effect of the change in soil pH, which increased from 5.5 to around 6.2–6.4, which is in the range where the soil has the lowest P sorption capacity and highest P availability (Penn and Camberato, [63]). This may be the reason why the NaOH-treated biochar, although having a lower WEP, resulted in a higher P availability when applied to the soil.
Both acidified BC-Bio and BC-Al had the highest residual soil WEP, which corresponded to their significantly higher WEP values compared to the other acidified biochar treatments. This suggests that phosphorus in these treatments was solubilized but not effectively taken up by plants. It is noteworthy that BC-Al had the highest aluminum content (> 45 g kg−1) among the biochars and it is known that at low pH, Al may be almost completely dissolved in long-term equilibrium [42]. Therefore, it could be speculated that acidification led to Al solubilization [41], potentially resulting in Al toxicity, inhibiting P uptake and reducing plant growth [64].
It is worth noting that the higher P solubility in the pre-treated materials may increase the P diffusion in the soil [27], as well as P losses through runoff and leaching [65]. However, the acidification and alkalinization pre-treatments increased the initial WEP of ash and biochar to a maximum value of ~ 40% in both experiments. These values are still considerably lower than commercial mineral fertilizers, which can have up to 90% of the total P soluble in water [35]. Thus, although we found relatively low MFE in the short-term pot experiments, these fertilizers may have P in pools that will be slowly released over longer periods of time. The results confirm that, in terms of P solubility and P uptake, the efficacy of the pre-treatment depended on the P removal method used and consequently on the P speciation in the biochars, confirming hypothesis 2. However, in terms of plant growth the NaOH-pretreatment seemed to be more favorable for biochar.
Conclusion
The aim of this study was to assess the effects of different pre-treatments on ash and biochar P speciation, solubility, and availability to maize and barley. Overall, our results demonstrate that chemical pre-treatments can increase the short-term P fertilizer value of thermally treated sewage sludge by increasing the fraction of more labile P species in the material when mixed with the soil. However, the placement did not yield promising results, probably because it enhanced toxic effects in the placement zone due to extreme pH levels and/or dissolution of undesirable elements (e.g. aluminum).
Acidification was more promising with ash, where the P compounds primarily consist of calcium-bound species. Among the untreated biochars, the one derived from biologically treated sludges stood out with a very high P availability. In terms of P solubility and P uptake, the biochars differed in their response to alkalinization and acidification depending on the sludge P removal method. However, for all four tested biochars, the NaOH pre-treatment was more effective in increasing shoot biomass than acidification, potentially due to dissolution of aluminum with acidification. Therefore, the acidification (H2SO4) of sewage sludge ash and the alkalinization (NaOH) of sewage sludge biochar showed the potential to enhance their fertilizer value, although still to a lesser extent than triple superphosphate.
Data Availability
All data will be openly available online in ERDA, the repository of the University of Copenhagen, in the following https://doi.org/10.17894/ucph.64ff8012-ae8f-48c3-b2f8-335ef00fb4b3.
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Kopp, C., Sica, P., Eising, A.G. et al. Enhancing Phosphorus Fertilizer Value of Sewage Sludge Ashes and Biochars Through Chemical Pre-treatments and Application Methods. Waste Biomass Valor 15, 4291–4307 (2024). https://doi.org/10.1007/s12649-023-02351-w
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DOI: https://doi.org/10.1007/s12649-023-02351-w